Bioactive Compounds in Underutilized Vegetables and Legumes (Reference Series in Phytochemistry) 3030574148, 9783030574147

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Reference Series in Phytochemistry Series Editors: J.-M. Mérillon · K. G. Ramawat

Hosakatte Niranjana Murthy Kee Yoeup Paek  Editors

Bioactive Compounds in Underutilized Vegetables and Legumes

Reference Series in Phytochemistry Series Editors Jean-Michel Mérillon Faculty of Pharmaceutical Sciences Institute of Vine and Wine Sciences University of Bordeaux Villenave d’Ornon, France Kishan Gopal Ramawat Department of Botany University College of Science M. L. Sukhadia University Udaipur, Rajasthan, India

This series provides a platform for essential information on plant metabolites and phytochemicals, their chemistry, properties, applications, and methods. By the strictest definition, phytochemicals are chemicals derived from plants. However, the term is often also used to describe the large number of secondary metabolic compounds found in and derived from plants. These metabolites exhibit a number of nutritional and protective functions for human wellbeing and are used e.g. as colorants, fragrances and flavorings, amino acids, pharmaceuticals, hormones, vitamins and agrochemicals. The series offers extensive information on various topics and aspects of phytochemicals, including their potential use in natural medicine, their ecological role, role as chemo-preventers and, in the context of plant defense, their importance for pathogen adaptation and disease resistance. The respective volumes also provide information on methods, e.g. for metabolomics, genetic engineering of pathways, molecular farming, and obtaining metabolites from lower organisms and marine organisms besides higher plants. Accordingly, they will be of great interest to readers in various fields, from chemistry, biology and biotechnology, to pharmacognosy, pharmacology, botany and medicine. The Reference Series in Phytochemistry is indexed in Scopus. More information about this series at http://www.springer.com/series/13872

Hosakatte Niranjana Murthy • Kee Yoeup Paek Editors

Bioactive Compounds in Underutilized Vegetables and Legumes With 89 Figures and 81 Tables

Editors Hosakatte Niranjana Murthy Department of Botany Karnatak University Dharwad, Karnataka, India Research Center for the Development of Advanced Horticultural Technology Chungbuk National University Cheongju, Korea (Republic of)

Kee Yoeup Paek Research Center for the Development of Advanced Horticultural Technology Chungbuk National University Cheongju, Korea (Republic of)

ISSN 2511-834X ISSN 2511-8358 (electronic) ISBN 978-3-030-57414-7 ISBN 978-3-030-57415-4 (eBook) ISBN 978-3-030-57416-1 (print and electronic bundle) https://doi.org/10.1007/978-3-030-57415-4 © Springer Nature Switzerland AG 2021, corrected publication 2021 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG. The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Preface

Vegetables and legumes are the major components of a balanced human diet and they provide essential nutrients such as carbohydrates, proteins, fat, vitamins, and minerals. Researches are in the exploration of various plants other than traditional vegetables and legumes to meet the global food demands and promote the plants which have been neglected and underutilized. Nutritional and phytochemical analysis of many neglected and underutilized vegetables and legumes has revealed that they are source nutrients, proteins, and vitamins. Further, underutilized vegetables and legumes are also proved to be rich in valuable secondary metabolites which account for bioactive principles. This book encompasses research work on bioactive compounds of underutilized vegetables and legumes across the globe to present the latest research on these plants for the enhanced appreciation of this topic. The chapters presented in this volume throw light on several research subjects that have provided critical information on the synthesis of plant secondary metabolites and their bioactive principles specifically from underutilized/neglected vegetables and legumes. Each chapter also provides background information of the plant, parts used, and their nutritional composition, chemical compounds, and their biological activities. Self-explanatory illustrations and tables have been incorporated in each chapter complementary to the main text. The topics included in this volume are not intended to be comprehensive, but our approach has been wide-ranging, presenting the most exciting aspects of bioactive compounds from underutilized vegetables and legumes. We would like to thank and express our deepest gratitude to all contributors who helped us to complete this book. We also thank Professor Jean-Michel Merillon and Professor Kishan Gopal Ramawat, Series Editors, for their constant encouragement. We thank Dr. Sylvia Blago, Dr. Sofia Costa, and Dr. Johanna Klute for their support. Finally, we also express indebtedness and thankfulness to the Springer team for completing this assignment successfully. India Korea (Republic of) 2021

Hosakatte Niranjana Murthy Kee Yoeup Paek

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Contents

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1

Part I Bioactive Compounds in Underutilized Vegetables: Leafy Vegetables . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

37

1

Health Benefits of Underutilized Vegetables and Legumes Hosakatte Niranjana Murthy and Kee Yoeup Paek

2

Bioactive Compounds of Amaranth (Genus Amaranthus) . . . . . . . Puneet Gandhi, Ravindra M. Samarth, and Kavita Peter

39

3

Bioactive Compounds of Fat-Hen (Chenopodium album L.) Amrita Poonia

.....

75

4

Bioactive Compounds of Paracress [Acmella oleracea (L.) R.K. Jansen] . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Moacir Couto Andrade Jr

87

5

Bioactive Compounds of Goosefoot (Genus Chenopodium) . . . . . . Paraskev T. Nedialkov and Zlatina Kokanova-Nedialkova

6

Bioactive Compounds of Asian Spider Flower (Cleome viscosa Linn.) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Veenu Kaul and Shveta Saroop

7

Bioactive Compounds of Mallow Leaves (Corchorus Species) . . . . Shashi Bhushan Choudhary, Neetu Kumari, Hariom Kumar Sharma, Pankaj Kumar Ojha, and J. Uraon

8

Bioactive Compounds of Ceylon Spinach [Talinum Triangulare (Jacq.) Willd.] . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Kandikere Ramaiah Sridhar and Mundamoole Pavithra

Part II Bioactive Compounds in Underutilized Vegetables: Fleshy Petioles, Cladodes, Fruits . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

Bioactive Compounds of Prickly Pear [Opuntia ficus-indica (L.) Mill.] . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Imen Belhadj Slimen, Taha Najar, and Manef Abderrabba

97

121 141

151

169

171 vii

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10

11

12

Contents

Bioactive Compounds of Swahili [Cyphostemma adenocaule (Steud. ex A. Rich.) Desc. ex Wild and R.B. Drumm.] . . . . . . . . . . Oluwasesan Micheal Bello, Abiodun Busuyi Ogbesejana, Oluwasogo A. Dada, Oluwatoyin E. Bello, and Mojeed O. Bello Bioactive Compounds of Barbados Gooseberry (Pereskia aculeata Mill.) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Mariana Buranelo Egea and Gavin Pierce

225

...........

239

Bioactive Compounds of Rhubarb (Rheum Species) Rajeev Bhat

Part III Bioactive Compounds in Underutilized Vegetables: Seeds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13

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Bioactive Compounds of Ajwain (Trachyspermum ammi [L.] Sprague) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Hafiz Muhammad Asif and Hafiz Abdul Sattar Hashmi

Part IV Bioactive Compounds in Underutilized Vegetables: Tuberous Vegetables . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

255

257

275

14

Bioactive Compounds of Allium Species . . . . . . . . . . . . . . . . . . . . . Rajeev Bhat

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15

Bioactive Compounds of Turmeric (Curcuma longa L.) . . . . . . . . . Josemar Gonçalves de Oliveira Filho, Micael José de Almeida, Tainara Leal Sousa, Daiane Costa dos Santos, and Mariana Buranelo Egea

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Part V Bioactive Compounds in Underutilized Vegetables: Unripe Fruits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16

17

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Bioactive Compounds of Culinary Melon (Cucumis melo subsp. agrestis var. conomon) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Hosakatte Niranjana Murthy, So Young Park, and Kee Yoeup Paek Bioactive Compounds of Horned Melon (Cucumis metuliferus E. Meyer ex Naudin) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Elsa F. Vieira, Clara Grosso, Francisca Rodrigues, Manuela M. Moreira, Virgínia Cruz Fernandes, and Cristina Delerue-Matos Bioactive Compounds of Hog Plums (Spondias Species) Salma Sameh, Eman Al-Sayed, Rola M. Labib, and Abdel Nasser B. Singab

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319

321

341

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Contents

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Bioactive Compounds of Ridge Gourd (Luffa acutangula (L.) Roxb.) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sateesh Belemkar, Mayank Sharma, Piyush Ghode, and Parshuram Nivrutti Shendge

Part VI Bioactive Compounds in Underutilized Vegetables: Shoots . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20

Bioactive Compounds in Bamboo Shoot . . . . . . . . . . . . . . . . . . . . . Harjit Kaur Bajwa, Oinam Santosh, and Nirmala Chongtham

Part VII Bioactive Compounds in Underutilized Vegetables: Bark . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21

Bioactive Compounds of Cinnamon (Cinnamomum Species) . . . . . Visweswara Rao Pasupuleti

Part VIII

Bioactive Compounds in Underutilized Legumes . . . . . .

22

Bioactive Compounds of Jack Beans (Canavalia Species) . . . . . . . Kandikere Ramaiah Sridhar and Bhagya Balakrishna Sharma

23

Bioactive Compounds of Royal Poinciana (Delonix regia (Hook.) Raf.) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Shweta Jain, Ankur Vaidya, Nancy Jain, Vimal Kumar, and Anuj Modi

403

417 419

441 443

453 455

483

24

Bioactive Compounds of Moringa (Moringa Species) . . . . . . . . . . . N. Kumar, Pratibha, and S. Pareek

503

25

Bioactive Compounds of Petai Beans (Parkia speciosa Hassk.) . . . Nisha Singhania, Navnidhi Chhikara, Sunil Bishnoi, M. K. Garg, and Anil Panghal

525

26

Bioactive Compounds of Velvet Bean (Mucuna pruriens L.) Seeds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Markusse Deli, Richard Marcel Nguimbou, Elie Baudelaire Djantou, Léopold Tatsadjieu Ngoune, and Nicolas Njintang Yanou

27

Bioactive Compounds of Runner Bean (Phaseolus coccineus L.) . . . Leticia X. Lopez-Martinez

28

Bioactive Compounds of Horse Gram (Macrotyloma uniflorum Lam. [Verdc.]) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Krishnananda Pralhad Ingle, Jameel M. Al-Khayri, Pritha Chakraborty, Gopal Wasudeo Narkhede, and Penna Suprasanna

545

565

583

x

29

Contents

Bioactive Compounds of Black Bean (Phaseolus vulgaris L.) . . . . . Balkisu O. Abdulrahman, Muntari Bala, and Oluwasesan Micheal Bello

Part IX Bioactive Compounds in Forage and Medicinal Legumes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30

Bioactive Compounds of Legume Seeds . . . . . . . . . . . . . . . . . . . . . Jatinder Pal Singh, Balwinder Singh, and Amritpal Kaur

623

643 645

Correction to: Bioactive Compounds of Prickly Pear [Opuntia ficusindica (L.) Mill.] . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Imen Belhadj Slimen, Taha Najar, and Manef Abderrabba

C1

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

667

About the Editors

Hosakatte Niranjana Murthy, professor in the PostGraduate Department of Botany, Karnatak University, Dharwad, India, has obtained his Ph.D. degree from Karnatak University, India. He has a tremendous passion for research and academics. Since 1986, he has served various positions in the Post-Graduate Department of Botany, Karnatak University, Dharwad, India. Apart from his teaching experience of 35 years, he possesses extensive research experience in the area of plant biotechnology. He has postdoctoral and collaborative research experience in many foreign research institutes. Professor Murthy has worked at Biotechnology Division, Tata Energy Research Institute, New Delhi, India (1992); Crop Science Department, University of Guelph, Guelph, Canada (1993); Research Centre for the Development of Horticultural Technology, Chungbuk National University, Cheongju, South Korea (2000–2001; 2002; 2004, 2006–2007, 2013– 2014); and Department of Biological Sciences, University of Nottingham, Nottingham, United Kingdom (2005–2006), as a postdoctoral fellow/visiting scientist. He is a recipient of various prestigious fellowships, including Biotechnology National Associate and Biotechnology Overseas Associate (awarded by Department of Biotechnology, Ministry of Science and Technology, Government of India); Brain Pool Fellowship (awarded by Korean Society of Science and Technology, South Korea); Visiting Fellowship (awarded by Korea Science and Engineering Foundation, South Korea); and Commonwealth Post-doctoral Fellowship (awarded by the Association of Commonwealth Universities, UK). He has completed more than 15 research projects funded by various agencies and guided several xi

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About the Editors

Ph.D. students. Professor Murthy has published more than 225 research articles in international peer-reviewed journals with high impact factors. His research work has been cited more than 4300 times by fellow researchers and has an H-index (Hirsch index) of 34 as recorded by Scopus. Professor Murthy has developed biotechnological methods for the production of pharmaceutically important secondary metabolites from cell and organ cultures of ginseng, Siberian ginseng, Echinacea, and St. John’s wort using large-scale bioreactors along with South Korean collaborators. His experimental investigations on the use of adventitious root cultures and bioreactor technologies for the production of biomass and secondary metabolites have paved the way for the commercialization of plant secondary metabolites. Various ginsengbased commercial products have been released and are currently available in the market. Professor Kee Yoeup Paek received his Ph.D. degree in 1984 from the Kyungbuk National University, South Korea, and he worked at Chungbuk National University, South Korea, for 40 years as assistant professor, associate professor, and professor. He has received large funds from various agencies and established the Research Center for the Development of Advanced Horticultural Technology at Chungbuk National University, South Korea, and he was the director of this center till his superannuation. On the research front, he has worked on large-scale production of secondary metabolites from medicinal plant tissue culture and bioreactor culture technology; mass propagation of horticultural plants through bioreactor technology; morphological, physiological, and biochemical responses of in vitro produced plants during acclimatization; and flowering physiology of ornamental plants. Professor Paek was the president of the Korean Orchid Society, Korean Society for Horticultural Sciences, and Korean Plant Biotechnology Society. He has worked at the Institute of Plant Physiology, Russia; Department of Horticulture, Chiba University, Japan; University of Calgary, Canada; and University of California, Riverside, USA. He has published 630 papers including several books published

About the Editors

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by reputed journals and publishers. He has guided 47 Ph.D. students, 38 postdoctoral students, and active member of numerous research projects. He has ten international patents awarded by Korea, Japan, and the USA. Professor Paek has developed biotechnological methods for the production of pharmaceutically important secondary metabolites from cell and organ cultures of ginseng, Siberian ginseng, Echinacea, and St. John’s wort using large scale bioreactors. His experimental investigations on the use of adventitious root cultures and bioreactor technologies for the production of biomass and secondary metabolites have paved the way for the commercialization of plant secondary metabolites. Various ginseng-based commercial products have been released and are currently available in the market.

Contributors

Manef Abderrabba Laboratory of Materials, Molecules and Applications, Preparatory Institute for Scientific and Technical Studies, Tunis, Tunisia Balkisu O. Abdulrahman Department of Biochemistry and Molecular Biology, Faculty of Life Sciences, Federal University Dutsin-Ma, Dutsin-Ma, Katsina, Nigeria Jameel M. Al-Khayri Department of Agricultural Biotechnology, College of Food and Agriculture Sciences, King Faisal University, Al-Ahsa, Saudi Arabia Eman Al-Sayed Department of Pharmacognosy, Faculty of Pharmacy, Ain-Shams University, Cairo, Egypt Moacir Couto Andrade Jr Post-Graduation Department, Nilton Lins University, Manaus, Brazil Post-Graduation Department, School of Public Health (Escola de Saúde Pública – ESAP), Manaus, Brazil Hafiz Muhammad Asif Faculty of Medicine and Allied Health Sciences, University College of Conventional Medicine, The Islamia University of Bahawalpur, Bahawalpur, Pakistan Muntari Bala Department of Biochemistry, Faculty of Basic Medical Sciences, Bayero University, Kano, Nigeria Sateesh Belemkar Department of Pharmacology, School of Pharmacy and Technology Management, SVKM’s NMIMS, Shirpur Campus, Dhule, Maharashtra, India Imen Belhadj Slimen Department of Animal Sciences, National Agronomic Institute of Tunisia, Tunis, Tunisia Laboratory of Materials, Molecules and Applications, Preparatory Institute for Scientific and Technical Studies, Tunis, Tunisia

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Contributors

Oluwasesan Micheal Bello National Center for Natural Products Research, School of Pharmacy, The University of Mississippi, University, MS, USA Department of Applied Chemistry, Faculty of Physical Sciences, Federal University, Dutsin-Ma, Katsina, Nigeria Oluwatoyin E. Bello Department of Crop Protection, University of Ilorin, Ilorin, Nigeria Mojeed O. Bello Department of Chemistry, University of Ilorin, Ilorin, Nigeria Rajeev Bhat ERA-Chair for Food (By-) Products Valorisation Technologies (VALORTECH), Estonian University of Life Sciences, Tartu, Estonia Sunil Bishnoi Department of Food Technology, Guru Jambheshwar University of Science and Technology, Hisar, India Pritha Chakraborty Department of Microbiology, St. Joseph’s College, Bangalore, Karnataka, India Navnidhi Chhikara Department of Food Technology, Guru Jambheshwar University of Science and Technology, Hisar, India Nirmala Chongtham Department of Botany, Panjab University, Chandigarh, India Shashi Bhushan Choudhary ICAR-National Bureau of Plant Genetic Resources, Regional Station Ranchi, Ranchi, Jharkhand, India Oluwasogo A. Dada Industrial Chemistry Unit, Department of Physical Sciences, Nanotechnology Laboratory, Landmark University Omu-aran, Omu-Aran, Kwara State, Nigeria Micael José de Almeida Instituto Federal de Educação, Ciência e Tecnologia Goiano, Rio Verde, GO, Brazil Josemar Gonçalves de Oliveira Filho School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, SP, Brazil Cristina Delerue-Matos REQUIMTE/LAQV, Instituto Superior de Engenharia do Porto, Instituto Politécnico do Porto, Porto, Portugal Markusse Deli ENSAI, Department of Food Sciences and Nutrition, University of Ngaoundere, Ngaoundere, Cameroon Elie Baudelaire Djantou ENSAI, Department of Food Sciences and Nutrition, University of Ngaoundere, Ngaoundere, Cameroon Daiane Costa dos Santos Institute of Tropical Pathology and Public Health, IPTSP – UFG, Goias Federal University (UFG), Goiânia, GO, Brazil Mariana Buranelo Egea Instituto Federal de Educação, Ciência e Tecnologia Goiano, Rio Verde, GO, Brazil

Contributors

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Virgínia Cruz Fernandes REQUIMTE/LAQV, Instituto Superior de Engenharia do Porto, Instituto Politécnico do Porto, Porto, Portugal Puneet Gandhi Department of Research, R & T Block, Bhopal Memorial Hospital and Research Centre, Bhopal, India M. K. Garg Department of Processing and Food Engineering, AICRP-PHET, Chaudhary Charan Singh Haryana Agricultural University, Hisar, India Piyush Ghode Department of Pharmaceutical chemistry, School of Pharmacy and Technology Management, SVKM’s NMIMS, Shirpur Campus, Dhule, Maharashtra, India Clara Grosso REQUIMTE/LAQV, Instituto Superior de Engenharia do Porto, Instituto Politécnico do Porto, Porto, Portugal Hafiz Abdul Sattar Hashmi Faculty of Medicine and Allied Health Sciences, University College of Conventional Medicine, The Islamia University of Bahawalpur, Bahawalpur, Pakistan Krishnananda Pralhad Ingle Biotechnology Centre, Department of Agricultural Botany, Post Graduate Institute, Dr. Panjabrao Deshmukh Krishi Vidyapeeth, Akola, Maharashtra, India Nancy Jain Department of Pharmaceutical Sciences, Dr. Hari Singh Gour University (A Central University), Sagar, Madhya Pradesh, India Shweta Jain Sir Madanlal Institute of Pharmacy, Etawah, Uttar Pradesh, India Veenu Kaul Department of Botany, University of Jammu, Jammu, India Amritpal Kaur Department of Food Science and Technology, Guru Nanak Dev University, Amritsar, Punjab, India Harjit Kaur Bajwa Department of Botany, Panjab University, Chandigarh, India Zlatina Kokanova-Nedialkova Department of Pharmacognosy, Faculty of Pharmacy, Medical University of Sofia, Sofia, Bulgaria N. Kumar Department of Agriculture and Environmental Sciences, National Institute of Food Technology Entrepreneurship and Management, Sonipat, India Vimal Kumar School of Pharmacy, ITM (SLS) Baroda University, Vadodara, India Neetu Kumari Birsa Agricultural University, Ranchi, Jharkhand, India Rola M. Labib Department of Pharmacognosy, Faculty of Pharmacy, Ain-Shams University, Cairo, Egypt Leticia X. Lopez-Martinez CONACYT-Centro de Investigación en Alimentación y Desarrollo A. C., Laboratorio de Antioxidantes y Alimentos Funcionales, Hermosillo, Sonora, Mexico

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Contributors

Anuj Modi Department of Pharmacy, Integrated Institute of Technology, New Delhi, India Manuela M. Moreira REQUIMTE/LAQV, Instituto Superior de Engenharia do Porto, Instituto Politécnico do Porto, Porto, Portugal Hosakatte Niranjana Murthy Department of Botany, Karnatak University, Dharwad, Karnataka, India Research Center for the Development of Advanced Horticultural Technology, Chungbuk National University, Cheongju, Korea (Republic of) Taha Najar Department of Animal Sciences, National Agronomic Institute of Tunisia, Tunis, Tunisia Laboratory of Materials, Molecules and Applications, Preparatory Institute for Scientific and Technical Studies, Tunis, Tunisia Gopal Wasudeo Narkhede Department of Agricultural Botany (Genetics and Plant Breeding), Vasantrao Naik Marathwada Krishi Vidyapeeth, Parbhani, Maharashtra, India Paraskev T. Nedialkov Department of Pharmacognosy, Faculty of Pharmacy, Medical University of Sofia, Sofia, Bulgaria Richard Marcel Nguimbou ENSAI, Department of Food Sciences and Nutrition, University of Ngaoundere, Ngaoundere, Cameroon Nicolas Njintang Yanou ENSAI, Department of Food Sciences and Nutrition, University of Ngaoundere, Ngaoundere, Cameroon Faculty of Science, Department of Biological Sciences, University of Ngaoundere, Ngaoundere, Cameroon Abiodun Busuyi Ogbesejana Department of Applied Chemistry, Federal University Dutsin-Ma, Dutsin-Ma, Nigeria Pankaj Kumar Ojha Acharya Narendra Deva University of Agriculture and Technology, Kumarganj, Faizabad, Uttar Pradesh, India Kee Yoeup Paek Research Center for the Development of Advanced Horticultural Technology, Chungbuk National University, Cheongju, Korea (Republic of) Anil Panghal Department of Processing and Food Engineering, AICRP-PHET, Chaudhary Charan Singh Haryana Agricultural University, Hisar, India S. Pareek Department of Agriculture and Environmental Sciences, National Institute of Food Technology Entrepreneurship and Management, Sonipat, India So Young Park Research Center for the Development of Advanced Horticultural Technology, Chungbuk National University, Cheongju, Korea (Republic of) Visweswara Rao Pasupuleti Department of Biomedical Sciences and Therapeutics, Universiti Malaysia Sabah, Kota Kinabalu, Sabah, Malaysia

Contributors

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Department of Biochemistry, Faculty of Medicine and Health Sciences, Abdurrab University, Pekanbaru, Riau, Indonesia Mundamoole Pavithra Department of Biosciences, Mangalore University, Mangalore, Karnataka, India Kavita Peter Department of Biotechnology, Barkatullah University, Bhopal, India Gavin Pierce Departament of Food Science and Technology, Oregon State University, Corvallis, OR, USA Amrita Poonia Department of Dairy Science and Food Technology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, India Pratibha Department of Food Business Management and Entrepreneurship Development, National Institute of Food Technology Entrepreneurship and Management, Sonipat, India Francisca Rodrigues REQUIMTE/LAQV, Instituto Superior de Engenharia do Porto, Instituto Politécnico do Porto, Porto, Portugal Ravindra M. Samarth Department of Research, R & T Block, Bhopal Memorial Hospital and Research Centre, Bhopal, India Salma Sameh Department of Pharmacognosy, Faculty of Pharmacy, Ain-Shams University, Cairo, Egypt Oinam Santosh Department of Botany, Panjab University, Chandigarh, India Shveta Saroop Department of Botany, Government Degree College, Kathua, India Bhagya Balakrishna Sharma Centre for Environmental Studies, Yenepoya (deemed to be) University, Mangalore, Karnataka, India Hariom Kumar Sharma ICAR-Directorate of Rapeseed-Mustard Research, Bharatpur, Rajasthan, India Mayank Sharma Department of Pharmaceutics, School of Pharmacy and Technology Management, SVKM’s NMIMS, Shirpur Campus, Dhule, Maharashtra, India Parshuram Nivrutti Shendge Department of Pharmacology, School of Pharmacy and Technology Management, SVKM’s NMIMS, Shirpur Campus, Dhule, Maharashtra, India Abdel Nasser B. Singab Department of Pharmacognosy, Faculty of Pharmacy, Ain-Shams University, Cairo, Egypt Center of Drug Discovery Research and Development, Faculty of Pharmacy, Ain-Shams University, Cairo, Egypt Balwinder Singh P.G. Department of Biotechnology, Khalsa College, Amritsar, Punjab, India

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Contributors

Jatinder Pal Singh Department of Food Science and Technology, Guru Nanak Dev University, Amritsar, Punjab, India Nisha Singhania Department of Food Technology, Guru Jambheshwar University of Science and Technology, Hisar, India Tainara Leal Sousa Institute of Tropical Pathology and Public Health, IPTSP – UFG, Goias Federal University (UFG), Goiânia, GO, Brazil Kandikere Ramaiah Sridhar Centre for Environmental Studies, Yenepoya (deemed to be) University, Mangalore, Karnataka, India Department of Biosciences, Mangalore University, Mangalagangotri, Mangalore, Karnataka, India Penna Suprasanna Nuclear Agriculture and Biotechnology Division, Bhabha Atomic Research Centre, Mumbai, Maharashtra, India Léopold Tatsadjieu Ngoune University Institute of Technology, University of Ngaoundere, Ngaoundere, Cameroon J. Uraon Birsa Agricultural University, Ranchi, Jharkhand, India Ankur Vaidya Pharmacy College Saifai, Uttar Pradesh University of Medical Sciences, Saifai, Etawah, Uttar Pradesh, India Elsa F. Vieira REQUIMTE/LAQV, Instituto Superior de Engenharia do Porto, Instituto Politécnico do Porto, Porto, Portugal

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Health Benefits of Underutilized Vegetables and Legumes Hosakatte Niranjana Murthy and Kee Yoeup Paek

Contents 1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 Nutritional Benefits of Underutilized Vegetables and Legumes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 Bioactive Compounds of Underutilized Vegetable and Legumes . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1 Polyphenols . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 Terpenes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3 Alkaloids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4 Volatiles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5 Lectins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6 Glucosinolates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.7 Organic Acids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 Biological Activities of Phytochemicals Isolated from Underutilized Vegetables and Legumes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1 Antidiabetic Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2 Anticancer Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3 Antimicrobial Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4 Antihypertensive Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5 Antioxidant Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.6 Hepatoprotective Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.7 Anti-inflammatory Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

2 3 15 15 17 17 20 20 21 21 22 22 22 25 25 28 29 29 29 30

H. N. Murthy (*) Department of Botany, Karnatak University, Dharwad, Karnataka, India Research Center for the Development of Advanced Horticultural Technology, Chungbuk National University, Cheongju, Korea (Republic of) K. Y. Paek Research Center for the Development of Advanced Horticultural Technology, Chungbuk National University, Cheongju, Korea (Republic of) © Springer Nature Switzerland AG 2021 H. N. Murthy, K. Y. Paek (eds.), Bioactive Compounds in Underutilized Vegetables and Legumes, Reference Series in Phytochemistry, https://doi.org/10.1007/978-3-030-57415-4_1

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H. N. Murthy and K. Y. Paek

Abstract

Plants existing in nature could be used as source of nutrition and bioactive compounds. Some of the wild and underutilized plants such as African baobab, amaranth, tarragon, Malabar spinach, borage, Ethiopian rape, goosefoot, chicory, spider plant, mallow, sea kale, curcuma, squash, roselle, water spinach, bitter melon, drumstick, tassel hyacinth, prickly pear, parsnip, tomatillo, Indian poke, purslane, yellow cresses, black nightshade, and water leaf are used as vegetables, and some other wild leguminous plants including jack bean, rattlepod, Hausa groundnut, lablab bean, pea vines, subabul, Andean lupin, horse gram, deer-eye bean, stinky bean, winged bean, African yam bean, adzuki bean, bambara groundnut, and rice bean are used for proteins and other nutrients. These plants are sources of nutrients and are also rich in bioactive compounds. Studies carried out during the past several decades have shown that bioactive compounds obtained from the underutilized vegetables and legumes (UVLs) have important role in preventing chronic diseases like cancer, diabetes, and coronary heart diseases. Phytochemicals present in UVLs have demonstrated antioxidant, anticancer, antimicrobial, antihypertensive, anti-inflammatory, and hepatoprotective activities. In the current chapter, we are presenting a review on importance of UVLs, their nutritional value, bioactive compounds, and their biological activities. Keywords

Alkaloids · Bioactive compounds · Biological activity · Phenolics · Terpenoids · Organic acids · Underutilized vegetables and legumes

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Introduction

The greatest threats in the world in the recent years are increase of human population and depletion of natural resources which have led to hunger, undernutrition, and poor health of people. The United Nations Food and Agriculture Organization (FAO) estimates that about 815 million of the 7.6 billion people in the world, or 10.7%, were suffering from chronic undernourishment in 2016 [1]. The vast majority of hungry people live in the lower- and middle-income regions [2]. Africa has the highest prevalence of undernourishment, but as the most populous region of the world, Asia has the highest number of undernourished people [2]. Currently, people are cultivating a handful of major agricultural crops which are used as grains, vegetables, and fruits, by using improved cultivars/varieties and modern agricultural practices. However, there are many plant species still lying underutilized or underexploited. Underutilized plants, in general, constitute those plant species that occur as life-support species in extreme environmental conditions, and threatened habitats, having genetic tolerance to survive under harsh conditions and possess nutritional, phytochemical, and therapeutic qualities [3–5]. In the era of climate change and

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Health Benefits of Underutilized Vegetables and Legumes

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vulnerability of agriculture and horticulture, underutilized plants are alternatives for their cultivation and utilization. Understanding nutritional value, phytochemical status of underutilized plants may help to contribute to the food security, nutrition, health, and income generation of people [6]. Many traditional and underutilized vegetables such as African baobab, amaranth, tarragon, Malabar spinach, borage, Ethiopian rape, goosefoot, chicory, spider plant, mallow, sea kale, curcuma, squash, roselle, water spinach, bitter melon, drumstick, tassel hyacinth, prickly pear, parsnip, tomatillo, Indian poke, purslane, yellow cresses, black nightshade, and water leaf (Table 1) are rich sources of food, fodder, oil, and medicine [3, 32]. Similarly, underutilized legumes like jack bean, rattlepod, Hausa groundnut, lablab bean, pea vines, subabul, Andean lupin, horse gram, deer-eye bean, stinky bean, winged bean, African yam bean, adzuki bean, bambara groundnut, and rice bean (Table 2) are sources of proteins, essential amino acids, polyunsaturated fatty acids, dietary fibers, essential minerals, and bioactive phytochemicals [3, 50]. These underutilized vegetables and legumes are having considerable commercial value and thus can make a significant contribution to household income and sustainable agriculture [51]. The major focus of this book is to illustrate the bioactive compounds of underutilized vegetables and legumes and their biological activities. Researchers from various parts of the world have illuminated nutritional and bioactive compounds of varied underutilized vegetables and legumes. Nutrition is one of the most important determinants of health, and increasing evidence suggests that diets rich in vegetables and legumes may prevent a wide range of diseases [32, 50]. Many of the phytochemicals present in underutilized vegetables and legumes possess the ability to interfere with body metabolism and functions, thereby alleviating health problems [52]. Keeping this in view, the present review highlights the possibilities of exploring underutilized vegetables and legumes as a source of nutrients and pharmaceuticals.

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Nutritional Benefits of Underutilized Vegetables and Legumes

Table 3 depicts the proximate composition of some of the underutilized vegetables and legumes (UVLs). UVLs contain good quantities of carbohydrate, protein, and fat. The amount of carbohydrate varies from 3.13 g/100 g in water convolvulus (Ipomoea aquatica) [53] to 57.24 g/100 g in horse gram (Macrotyloma uniflorum) [55]. Protein content ranges from 0.84 g/100 g in bitter gourd (Momordica charantia) [53] to 27.5 g/100 g in stinky bean (Parkia speciosa) [54]. Fat values vary from 0.1 g/100 g in adzuki bean (Vigna angularis) [53] to 13.3% in stinky bean (Table 3) [54]. The energy values of underutilized vegetables and legumes vary from 19 kcal/100 g in bitter gourd and water convolvulus (Convolvulus aquatica) [53] to 346 kcal/100 g in rice bean (Vigna umbellata) [55]. Thus, UVLs can be alternatives to conventional vegetables and leguminous crops. UVLs are also rich in minerals including iron, magnesium, phosphorous, potassium, sodium, zinc, copper, manganese, and selenium (Table 3). For example,

Shona cabbage, African cabbage, spiderwisp, spider plant, cat’s whiskers, stinkweed

Chicory

Goosefoot, fat-hen, lamb’s quarters

Ethiopian rape

Borage

Malabar spinach

Tarragon

Amaranth

Common name(s) African baobab

Cleome gynandra (Cleomaceae)

Botanical name Adansonia digitata (Malvaceae) Amaranthus spp. (Amaranthaceae) Artemisia dracunculus (Asteraceae) Basella alba and B. rubra (Basellaceae) Borago officinalis (Boraginaceae) Brassica carinata (Brassicaceae) Chenopodium album (Amaranthaceae) Cichorium intybus (Asteraceae) Leaves, shoots

Leaves, roots

Leaves

Leaves, seeds

Leaves, seeds

Leaves

Leaves

Leaves, seeds

Plant parts used Leaves, fruits, seeds

Table 1 Names and uses of some underutilized vegetables

Leaves and roots are used for culinary purpose. Roots are coffee substitute, food additive. Medicinal value Leafy vegetable

Leafy vegetable, seeds are also used

Leafy vegetable, seed oil

Vegetable, spice, seed oil, herbal medicine

Leafy vegetable

Culinary, medicinal

Leafy vegetable, oil, pigments

Known uses Valued for sources of food, health remedies

Native of Africa but has become widespread in many tropical and sub-tropical countries

Europe, Africa, Australia, North America, Oceania; cultivated in North India Europe, North America, China, and Australia

Ethiopia

Mediterranean

India, Southeast Asia, China

Native to Mexico and Central America; worldwide Eurasia and North America

Place of origin and distribution Native of Africa; common in African countries

[15]

[14]

[13]

[12]

[11]

[10]

[9]

[8]

References [7]

4 H. N. Murthy and K. Y. Paek

Cucurbita spp. (Cucurbitaceae) Hibiscus sabdariffa (Malvaceae)

Ipomoea aquatica (Convolvulaceae) Momordica spp. (Cucurbitaceae) Moringa oleifera (Moringaceae) Leopoldia comosa (Asparagaceae) Opuntia spp. (Cactaceae) Pastinaca sativa (Apiaceae)

Squash, pumpkin

Water spinach, water morning glory, water convolvulus, Chinese spinach Bitter melon, gac, spiny gourd

Parsnip

Prickly pear

Moringa, drumstick tree, horseradish tree Tassel hyacinth

Roselle

Curcuma

Sea kale

Corchorus spp. (Malvaceae) Crambe spp. (Brassicaceae) Curcuma spp. (Zingiberaceae)

Mallow leaves

Leaves or cladodes Roots

The leaves (or cladodes) are cooked and eaten as a vegetable Root vegetable like carrot

Leaves and fruits are used for culinary purpose Bulbs are used as vegetable

Fruits are used as vegetable

Fruits Leaves, fruits, seeds Bulbs

Leaves are used for culinary purpose; dried sepals (calyces) are used in preparation of juice and jam Leafy vegetable

Leaves are flavoring, roots are edible, rhizomes are culinary spice, dyeing, used in Indian traditional medicine Fruits are having culinary uses

Leafy vegetable

Leafy vegetable

Leaves, fruits, seeds Leaves, flower buds, sepals of the flower Leaves

Rhizomes, roots, leaves

Leaves

Leaves

(continued)

[25]

[24]

[23]

Southeast Europe to Turkey

South America and North America Europe and Asia

[22]

[21]

[20]

[19]

[18]

[17]

[13]

[16]

Indian subcontinent

Africa, Asia, Australia

Southeast Asia

Andeans, Mesoamerica, throughout the world West Africa, Sudan Cultivated in Indian subcontinent and China

Indian subcontinent, Africa, New Guinea, Southern China, Australia

Asia, the middle East, North and West Africa Europe

1 Health Benefits of Underutilized Vegetables and Legumes 5

Water leaf, Ceylon spinach

Black nightshade

Yellowcresses

Common purslane

Indian poke

Common name(s) Tomatillo

Table 1 (continued)

Talinum triangulare (Talinaceae)

Botanical name Physalis philadelphica (Solanaceae) Phytolacca acinosa (Phytolaccaceae) Portulaca oleracea (Portulacaceae) Rorippa indica (Brassicaceae) Solanum nigrum (Solanaceae) Leaves

Tender shoots, leaves Leaves, fruits (berries)

Leaves, stem

Leaves

Plant parts used Fruits

Leafy vegetable

Leaves and berries are routinely consumed as food after cooking

Leafy vegetable

Leafy vegetable

Leafy vegetable

Known uses Green fruits are used as vegetable

Common in Europe and Asia. Introduced in the America, Australia, and South Africa Africa, Southeast Asia

Northern Africa, Southern Europe, Indian subcontinent, Southeast Asia, Australia Southeast Asia

Southeast Asia

Place of origin and distribution Central America, Mexico

[31]

[30]

[29]

[28]

[27]

References [26]

6 H. N. Murthy and K. Y. Paek

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Health Benefits of Underutilized Vegetables and Legumes

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Table 2 Names and uses of some underutilized legumes Common name(s) Jack beans, sword bean

Botanical name Canavalia spp. (Fabaceae)

Plant parts used Pods, seeds

Rattlepods

Crotalaria spp. (Fabaceae)

Leaves, flowers, pods, seeds

Ground bean, Hausa groundnut, or Kersting’s groundnut Hyacinth bean, Lablab bean Peavines, vetchlings

Macrotyloma geocarpum (Fabaceae)

Seeds (like peanut)

Lablab purpureus (Fabaceae) Lathyrus spp. (Fabaceae)

Leaves, seeds

White lead tree, subabul

Leucaena leucocephala (Fabaceae) Lupinus mutabilis (Fabaceae)

Pods

Macrotyloma uniflorum (Fabaceae) Mucuna spp. (Fabaceae)

Seeds

Parkia speciosa (Fabaceae)

Pods, seeds

Andean lupin, South American lupin, Peruvian field lupin, pearl lupin Horse gram

Deer-eye beans, donkey-eye bean Stinky bean

Pods, seeds

Seeds

Seeds

Known uses Pods are used as vegetable, seeds used for culinary purpose Leafy vegetable; seeds used for culinary purpose Seeds used for culinary purpose

Place of origin and distribution Hawaii

References [33]

Asia, Africa, Australia, Central America

[34–36]

Western Africa

[37]

Africa, Southeast Asia North America, South America, Europe, Asia Mexico, Central America Ecuador, Peru, Bolivia

[38]

Seeds used for culinary purpose Seeds used for culinary purpose

India and Sri Lanka

[42]

Tropical forests

[24]

Pods and seeds are used for culinary purpose

India, Malaysia, Indonesia, Thailand, Singapore, Borneo, Philippines, Africa

[43]

Seeds used for culinary purpose Seeds used for culinary purpose

Young pods are used as vegetable Seeds used for culinary purpose

[39]

[40]

[41]

(continued)

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H. N. Murthy and K. Y. Paek

Table 2 (continued) Common name(s) Winged bean

African yam bean

Botanical name Psophocarpus tetragonolobus (Fabaceae)

Plant parts used Leaves, flowers, roots, bean pods, seeds

Known uses Entire winged been plant is edible, eaten raw or cooked Seeds used for culinary purpose Seeds used for culinary purpose

Sphenostylis stenocarpa (Fabaceae) Vigna aconitifolia (Fabaceae)

Seeds, tubers

Adzuki bean

Vigna angularis (Fabaceae)

Seeds

Seeds are cooked along with rice. It is made in to sweets and juice

Bambara nut, Bambara groundnut

Vigna stenocarpa (Fabaceae)

Seeds

Rice bean

Vigna umbellata (Fabaceae)

Seeds

The seeds are used for food and beverage because of their high protein content Seeds used for culinary purpose

Moth bean

Pods, seeds

Place of origin and distribution South and Southeast Asia, Africa, Latin America

References [44]

Africa

[45]

India, Pakistan. Introduced to Australia, Southeast Asia, and USA Japan, China, Korea. It is also cultivated in USA, South America, and India West Africa

[46]

Indo-China

[49]

[47]

[48]

calcium values vary from 9 mg/100 g in bitter gourd to 290 mg/100 g in rice bean [53, 55]. Magnesium concentration ranges from 16 mg/100 g in bitter gourd to 230 mg/100 g in rice bean [53, 55]. Potassium levels vary from 208 mg/100 g in roselle (Hibiscus sabdariffa) to 1400 mg/100 g in rice bean (Table 3) [53, 55]. Consequently, UVLs are useful in providing mineral nutrients as well. Mineral elements are very much essential in the human body for growth and development. For instance, calcium ion is one of the elements that regulate muscle contraction, enzyme activities, nerve function, and blood clotting and is an integral component of the bone [56]. Deficiency of calcium is responsible for rachitis and osteoporosis. Iron is a crucial element of blood and plays an important role in oxidation and reduction

0.38 mg 16 mg 36 mg 319 mg 6 mg 0.77 mg 0.033 mg 0 mg 0.2 μg 33 mg 0.051 mg

Protein Fat Ash Carbohydrate Dietary fiber Total sugars Calcium, Ca

Iron, Fe Magnesium, Mg Phosphorous, P Potassium, K Sodium, Na Zinc, Zn Copper, Cu Manganese, Mn Selenium, Se Vitamin C, total ascorbic acid Thiamin

1.48 mg 51 mg 37 mg 208 mg 6 mg 0 mg 0 mg 0 mg 0 mg 12 mg 0.011 mg

1.99 mg 68 mg 44 mg 494 mg 45 mg 0.17 mg 0.113 mg 0.303 mg 0.9 μg 21 mg 0.047 mg

84 kJ 2.03 g 0.36 g 1.36 g 3.39 g 0g 0g 65 mg

79 kJ 0.84 g 0.18 g 0.71 g 4.32 g 2g 1.95 g 9 mg

Components Water Energy 205 kJ 0.96 g 0.64 g 0.51 g 11.31 g 0g 0g 215 mg

Purslanea 92.86 g 20 kcal

Underutilized vegetables Bitter gourd, podsa Rosellea 93.95 g 86.58 g 19 kcal 49 kcal

1.67 mg 71 mg 39 mg 312 mg 113 mg 0.18 mg 0.023 mg 0.16 mg 0.9 μg 55 mg 0.03 mg

80 kJ 2.6 g 0.2 g 1.6 g 3.13 g 2.1 g 0g 77 mg

Water Convolvulusa 92.47 g 19 kcal

Table 3 Proximate composition of some underutilized vegetables and legumes (per 100 g)

2 mg 52 mg 168 mg 532 mg 8 mg 1.77 mg 0.298 mg 0.573 mg 1.2 μg 0 mg 0.115 mg

536 kJ 7.52 g 0.1 g 1.33 g 24.77 g 7.3 g 0g 28 mg 12.5 mg 230 mg 340 mg 1400 mg 1 mg 3 mg 0.74 mg 2.7 mg 3 μg 0 mg 0.46 mg

1448 kJ 20.3 g 1.6 g 20.3 g 4.32 g 21.7 g ND 290 mg

Underutilized pulses Adzuki Rice beansa beanb 66.29 g 16.3 g 128 kcal 346 kcal

8.76 mg 152 mg 298 mg 1065 mg 12.14 mg 2.71 mg 1.29 mg 3.13 mg 29.49 mg 0 mg 0.32 mg

1379 kJ 21.73 g 0.62 g 3.24 g 57.24 g 7.88 g 0.35 g 269 mg

Horse gramb 9.28 g 329 kcal

Health Benefits of Underutilized Vegetables and Legumes (continued)

Stinky beanc ND 91.0– 441.5 kcal ND 6.0–27.5 g 1.6–13.3 g 1.2–4.6 g 13.2–52.9 g ND ND 108.0– 265.1 mg 2.2–2.7 mg 29.0 mg 115.0 mg 341.0 mg ND 8.2 ppm 36.7 ppm 42 ppm ND 19.3 mg 0.28 mg

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Components Riboflavin Niacin Pantothenic acid Vitamin B-6 Folate, total Folic acid Folate, food Folate, DFE Choline, total Vitamin B-12 Vitamin A, RAE Ratinol Carotene, beta Carotene, alpha Cryptoxanthin, beta Vitamin A, IU Lycopene Lutein + Zeaxanthin Vitamin E (alpha-tocopherol) Vitamin E, added Vitamin D (D2 + D3) Vitamin K (phylloquinone) Fatty acids, total saturated 4:0

Table 3 (continued)

Underutilized vegetables Bitter gourd, podsa Rosellea 0.053 mg 0.028 mg 0.28 mg 0.31 mg 0.193 mg 0 mg 0.041 mg 0 mg 51 μg 0 μg 0 μg 0 μg 51 μg 0 μg 51 μg 0 μg 10.8 mg 0 mg 0 μg 0 μg 6 μg 14 μg 0 μg 0 μg 68 μg 0 μg 0 μg 0 μg 0 μg 0 μg 113 IU 287 IU 0 μg 0 μg 1323 μg 0 μg 0.14 mg 0 μg 0 mg 0 μg 0 μg 0 μg 4.8 μg 0 μg 0.014 g 0g 0g Purslanea 0.112 mg 0.48 mg 0.036 mg 0.73 mg 12 μg 0 μg 12 μg 12 μg 12.8 μg 0 μg 0 μg 0 μg 0 μg 0 μg 0 μg 1320 IU 0 μg 0 μg 0 μg 0 μg 0 μg 0 μg 0 μg 0g

Water Convolvulusa 0.1 mg 0.9 mg 0.141 mg 0.096 mg 57 μg 0 μg 57 μg 57 μg 0 μg 0 μg 315 μg 0 μg 0 μg 0 μg 0 μg 0 μg 0 μg 0 μg 0 μg 0 μg 0 μg 0 μg 0g 0g

Underutilized pulses Adzuki Rice beansa beanb 0.064 mg 0.14 mg 0.717 mg 1.7 mg 0.43 mg 0.35 mg 0.096 mg 0.253 mg 121 μg 180 μg 0 μg 0 μg 121 μg 180 μg 121 μg 180 μg 0 μg 0 μg 0 μg 0 μg 0 μg 0 μg 0 μg 2 μg 0 μg 68 μg 0 μg 0 μg 0 μg 0 μg 6 IU 0 IU 0 μg 0 μg 0 μg 0 μg 0 μg 0 mg 0 μg 0 mg 0 μg 0 μg 0 μg 28 μg 0.036 g 0g 0g 0g Horse gramb 0.24 mg 1.82 mg 1.58 mg 0.59 mg 163 μg 0 μg 163 μg 163 μg 0 μg 0 μg 0 μg 0 μg 58 μg 0 μg 0 μg 0 IU 0 μg 70.1 μg 0 μg 0 μg 0 μg 0 μg 135 mg ND

Stinky beanc ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND

10 H. N. Murthy and K. Y. Paek

0g 0g 0g 0g 0g 0g 0g 0g 0g 0g 0g 0g 0g 0g 0g 0g 0g 0g

0g 0g 0g 0g 0g 0.01 g 0.004 g

0.033 g

0g 0.033 g 0g 0g 0.078 g

0.078 g 0g 0g 0g 0g 0g 0g 0g 0g 0g 0 mg 0 mg

6:0 8:0 10:0 12:0 14:0 16:0 18:0

Fatty acids, total monounsaturated 16:1 18:1 20:1 22:1 Fatty acids, total polyunsaturated 18:2 18:3 18:4 20:4 20:5 n-3 (EPA) 22:5 n-3 (DPA) 22:6 n-3 (DHA) Fatty acids, total trans Cholesterol Alcohol, ethyl Caffeine Theobromine 0g 0g 0g 0g 0g 0g 0g 0g 0 mg 0g 0 mg 0 mg

0g 0g 0g 0g 0g

0g

0g 0g 0g 0g 0g 0g 0g

0g 0g 0g 0g 0g 0g 0g 0g 0 mg 0g 0 mg 0 mg

0g 0g 0g 0g 0g

0g

0g 0g 0g 0g 0g 0g 0g

0.021 g 0g 0g 0g 0g 0g 0g 0g 0g 0g 0 mg 0 mg

0g 0.009 g 0g 0g 0.021 g

0.009 g

0g 0g 0g 0g 0g 0g 0g

0g 0g 0g 0g 0g 0g 0g 0g 0g 0g 0 mg 0 mg

0g 0g 0g 0g 0g

0g

0g 0g 0g 0g 0g 0g 0g

207 mg 1.68 mg 0 mg 0 mg 0 mg 0 mg 0 mg 0 mg 0 mg 0g 0g 0g

0 mg 13.59 mg 0 mg 0 mg 258 mg

ND ND ND 0 mg 0 mg 114,g 13 0.59 mg 68.89 mg

Health Benefits of Underutilized Vegetables and Legumes (continued)

ND ND ND ND ND ND ND ND ND ND ND ND

ND ND ND ND ND

ND

ND ND ND ND ND ND ND

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Underutilized vegetables Bitter gourd, podsa Rosellea ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND Purslanea ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND

a

g gram, mg milligram, μg microgram, ppm parts per million, ND not detected USDA [53] b Longvoh et al. [54] c Kamisah et al. [55]

Components Tryptophan Threonine Isoleucine Leucine Lysine Methionine Cystine Phenylalanine Tyrosine Valine Arginine Histidine Alanine Aspartic acid Glutamic acid Glycine Proline Serine

Table 3 (continued) Water Convolvulusa 0g 0.14 g 0.104 g 0.146 g 0.109 g 0.044 g 0.028 g 0.127 g 0.08 g 0.135 g 0.148 g 0.047 g 0.109 g 0.65 g 0.252 g 0.099 g 0.088 g 0.122 g

Underutilized pulses Adzuki Rice beansa beanb 0g ND 0.255 g ND 0.3 g ND 0.632 g ND 0.567 g ND 0.079 g ND 0.07 g ND 0.398 g ND 0.224 g ND 0.387 g ND 0.486 g ND 0.198 g ND 0.439 g ND 0.891 g ND 1.173 g ND 0.286 g ND 0.331 g ND 0.369 g ND Horse gramb 1.08 g 3.32 g 3.72 g 6.79 g 6.24 g 0.73 g 0.75 g 8.08 g 3.18 g 4.16 g 5.87 g 2.70 g 4.60 g 11.24 g 18.54 g 4.03 g 3.72 g 5.19 g

Stinky beanc ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND

12 H. N. Murthy and K. Y. Paek

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Health Benefits of Underutilized Vegetables and Legumes

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processes [56]. Iron deficiency leads to anemia. Phosphorous is a necessary element for the growth of bones and teeth. Consumption of underutilized vegetables and legumes will suffice mineral nutrition in humans. Vitamins are crucial constituents of the diet and are required for varied essential functions in the human body. For example, thiamine (vitamin B1) is important for utilization of carbohydrates, and lack of thiamine in diet leads to beriberi [57]. Riboflavin (vitamin B2) is an important component of protein metabolism, and scarcity of riboflavin causes glossitis, angular cheilitis, and seborrheic dermatitis [58]. Nicotinic acid (vitamin B3) is essential in oxidative reactions and is involved in metabolism of carbohydrates, proteins, and fats. Deficiency of nicotinic acid in the body leads to pellagra [57]. Ascorbic acid (vitamin C) is essential for collagen synthesis which is essential component of the gums, bones, and skin. It is also essential in the functioning of immune system in the body [59], and deficiency of ascorbic acid leads to scurvy. UVLs are also rich sources of vitamins (Table 3). Ascorbic acid concentration is 12 mg/100 g in roselle and 55 mg/100 g in water convolvulus (Table 3); thus underutilized vegetables are rich in vitamin C. Thiamin levels in UVLs were ranging from 0.011 mg/100 g in roselle to 0.46 mg/100 g in rice bean. Riboflavin levels were 0.028 mg/100 g (roselle) to 0.24 mg/100 g (horse gram), and niacin content was 0.28 mg/100 g (bitter gourd) to 1.82 mg/100 g (horse gram). UVLs also possessed pantothenic acid, vitamin B6, and folate in considerable levels (Table 3). Dietary fibers (roughage) consist of complex polysaccharides including cellulose, hemicelluloses, lignins, and others [60]. Dietary fibers are important in improving the digestive system, controlling blood glucose levels in diabetes and cholesterol levels in cardiovascular diseases, and prevention of bowel cancer [60–62]. UVLs are abundant in dietary fibers, and their levels vary from 2 g/100 g in bitter gourd to 21.7 g/100 g in rice bean (Table 3). Nutrient composition of major vegetables and legumes is compared with underutilized vegetables and legumes in Tables 4 and 5. From the data it is clear that UVLs are abundant with essential nutrients such as proteins, fats, dietary fibers, Table 4 Nutrient values of some major vegetables in comparison with underutilized vegetables (per 100 g fresh weight) Total Protein lipid Items (g) (g) Major vegetables Tomato 0.9 0.2 Cabbage 1.28 0.1 Potato 2.0 0.09 Underutilized vegetables Bitter 0.84 0.18 gourd Roselle 0.96 0.64 Purslane 2.03 0.36

Fiber (g)

Calcium (mg)

Iron (mg)

Zinc Vit C (mg) (mg)

Folate (μg)

Vit A (μg)

1.2 2.5 2.2

10 40 12

0.3 0.47 0.78

0.17 0.18 0.29

13 76 19.7

15 43 0.30

880 0 2

2

9

0.38

0.77

33

51

6

0 0

215 65

1.48 1.99

0 0.17

12 21

0 12

14 0

Data source: USDA nutrient database [53]

7.3 21.77 7.88

16.3 9.3 17.4

1.2 19.9 6.0

0.1 1.6 0.62

Fiber (g)

Total lipid (g)

Data source: USDA nutrient database [53]

Items Protein (g) Major vegetables Mung bean 23.9 Soybean 36.5 Chickpea 19.3 Underutilized vegetables Adzuki bean 7.52 Rice bean 20.3 Horse gram 21.73 28 290 269

132 277 105

Calcium (mg)

2 12.5 8.76

6.7 15.7 6.2

Iron (mg)

1.77 3 2.71

2.68 4.89 3.43

Zinc (mg)

0 0 0

4.8 6 4

Vit C (mg)

Table 5 Nutrient values of some major legumes in comparison with underutilized legumes (per 100 g fresh weight)

121 180 163

625 375 557

Folate (μg)

0 0 0

11.4 2.2 6.7

Vit A (μg)

14 H. N. Murthy and K. Y. Paek

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minerals, and vitamins on par with major vegetables and legumes. Therefore, UVLs are alternatives in terms of food security, poverty elimination, and environmental sustainability [4].

3

Bioactive Compounds of Underutilized Vegetable and Legumes

Vegetables and legumes are abundant with varied phytochemicals, and they have been listed in Fig. 1. These are generally classified into polysaccharides or carbohydrates which include monosaccharides, disaccharides, oligosaccharides, and sugar alcohols; organic acids and lipids; nitrogen-containing compounds including amines, cyanogenic glycosides, glucosinolates, purines, and miscellaneous nitrogen compounds; alkaloids including pyridine alkaloids, betalain alkaloids, indole alkaloids, indolizidine alkaloids, pyrrolidine alkaloids, quinoline alkaloids, steroidal alkaloids, and tropane alkaloids; phenolics such as flavonoids (anthocyanins, flavanols, flavonols, dihydroflavonols, flavones, isoflavonoids, flavanones, dihydrochalcones), phenolic acids (hydroxybenzoic acids, hydroxycinnamic acids), lignans, coumarins (coumestans, furanocoumarins), phenols (alkylphenols, methoxyphenols), phenylpropanoids (benzodioxoles, cucuminoids, hydroxyphenylpropenes), quinones (benzoquinones, naphthoquinones, anthraquinones), stilbenoids, and xanthones; and terpenoids including monoterpenoids (phenolic terpenes), sesquiterpenoids, diterpenoids, triterpenoids (phenolic terpenes, saponins, phytosterols), and tetraterpenoids (carotenoids) [63]. Most of these phytochemicals are isolated and assessed from UVLs.

3.1

Polyphenols

Polyphenols are the compounds that have an aromatic ring carrying one or more hydroxyl moieties. Polyphenols are broadly classified into two main groups, namely, flavonoids and nonflavonoids. Flavonoids are further divided into flavanones, flavones, dihydroflavonols, flavonols, flavan-3-ols, anthocyanins, isoflavones, and proanthocyanidins, whereas nonflavonoids group is categorized into simple phenols, benzoic acids, hydrolysable, tannins, acetophenones, phenylacetic acids, hydroxycinnamic acids, coumarins, benzophenones, xanthones, stilbenes, chalcones, lignans, and secoiridoids [64]. Polyphenols are reported to possess potent antioxidant activities and involved in scavenging free radicals, chelation and stabilization of divalent cations, and modulation of endogenous antioxidant enzymes [65, 66]. Phenolic acids and flavonoids have anti-carcinogenic and antimutagenic effects since they act as protective agents of DNA against free radicals, by inactivating carcinogens, by inhibiting enzymes involved in pro-carcinogen activation, and by activating xenobiotics detoxification enzymes [67]. For example, caffeic acid and chlorogenic acid were reported to form mutagenic and carcinogenic Nnitroso compounds in vitro [68]. Recent studies have shown that catechin and its

16

H. N. Murthy and K. Y. Paek

Fig. 1 Phytochemicals of vegetables and legumes

derivatives served as neuroprotective agents and exhibited their use in curing neurodegenerative disorders such as Parkinson’s disease and Alzheimer’s disease [69]. Tannins have been reported to exert physiological effects, such as accelerate blood clotting, reduce blood pressure, decrease the serum lipid level, and modulate immunoresponses [70]. Phenolic acids, stilbenes, tannins, and isoflavones

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Health Benefits of Underutilized Vegetables and Legumes

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have been reported to possess antimicrobial activities [71]. UVLs are also rich in polyphenols (Table 6). Varied phenolic compounds, namely, gallic acid, protocatechuic acid, gentisic acid, vanillic acid, chlorogenic acid, tannic acid, caffeic acid, p-coumaric acid, p-hydroxybenzoic acid, syringic acid, ferulic acid, and sinapic acid; diverse flavonoids including catechin, epicatechin, quercetin, apigenin, myricetin, luteolin, and kaempferol; and carotenoids such as lutein, α-carotene, zeaxanthin, ß-cryptoxanthin, and lycopene have been isolated from bitter gourd [72]. Anthocyanins [delphinidin-3-sambubioside (hibiscin), cyanidin-3-sambubioside (gossypicyanin), cyanidin-3,5-diglucoside, delphinidin (anthocyanidin)], flavonoids [(hibiscitrin (hibiscetin-3 glucoside), sabdaritrin, gossypitrin, gossytrin and other gossypetin glucosides, quercetin, luteolin, chlorogenic acid, protocatechuic acid, pelargonic acid, eugenol] sterols (ß-sitosterol and ergosterol) were reported from roselle [73]. Similarly, several phenolics and flavonoids were recorded in purslane, water convolvulus, adzuki bean, rice bean, horse gram, and stinky bean (Table 6) [74– 78]. All these reports suggest that UVLs could be good sources of dietary polyphenols.

3.2

Terpenes

Terpenes are natural compounds synthesized in plants from isoprene subunits. The classification of terpenoids is based on the number of isoprenoid units present in their structure. This group consists of compounds with two (monoterpenes), three (sesquiterpenes), four (diterpenes), five (sesterterpenes), six (triterpenes), and eight (tetraterpenes) isoprenoid units [79]. Terpenes have exhibited a wide variety of biological activities and health effects. For instance, monoterpenes isolated from Mentha piperita have shown antibacterial, antispasmodic, antiseptic, and antiulcer activities [80]. Diterpene lactone of Andrographis paniculata is a very good anticancer drug [81]. Sesquiterpene lactone obtained from Artemisia species is a popular antimalarial drug [82]. Cucurbitacin B (triterpene) isolated from Cucurbitaceae members (Momordica spp., Cucumis spp., Bryonia spp.) is a potent anticancer, hepatoprotective, and anti-inflammatory drug. UVLs are storehouse of terpenoid compounds (Table 6). For example, bitter gourd possesses terpenoids including triterpenes, saponins, and phytosterols (Table 6) [72]. Portulosides A and B, monoterpene glycosides, and portulenes are reported from purslane (Table 6) [74]. Varied phytosterols such as ß-sitosterol, stigmasterol, lupeol, campesterol, and squalene were reported from stinky bean [43].

3.3

Alkaloids

Alkaloids are a group of organic compounds that contain basic nitrogen atoms [83]. Various alkaloids are pharmacologically well characterized and are used as clinical drugs, ranging from cancer chemotherapeutics to analgesic agents. For example, vinblastine and vincristine are vinca alkaloids obtained from the

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H. N. Murthy and K. Y. Paek

Table 6 Phytochemicals in some underutilized vegetables and legumes Common name Bitter gourd

Botanical name Momordica charantia

Roselle

Hibiscus sabdariffa

Major phytochemicals Phenolics: gallic acid, protocatechuic acid, gentisic acid, vanillic acid, chlorogenic acid, tannic acid, caffeic acid, p-coumaric acid, phydroxybenzoic acid, syringic acid; ferulic acid, sinapic acid Flavonoids: catechin, epicatechin, quercetin, apigenin, myricetin, luteolin, kaempferol Carotenoids: lutein, α-carotene, zeaxanthin, ßcryptoxanthin, lycopene Triterpenoids: cucurbita-6,22(E),24-trien-3βol-19,5β-olide, 5β,19-epoxycucurbita-6,22 (E),24-triene-3β,19-diol,3β-hydroxycucurbita-5 (10),6,22(E),24-tetraen-19-al, 19dimethoxycucurbita-5(10),6,22(E),24-tetraen3β-ol,19-nor-cucurbita-5(10),6,8,22(E),24pentaen-3β-ol; charantagenins D and E; (23E)3β,25-dihydroxy-7β-methoxycucurbita-5,23dien-19-al, (23S*)-3 β-hydroxy-7β,23dimethoxycucurbita-5,24-dien-19-al, (23R*)-23O-methylmomordicine IV, (25§)-26hydroxymomordicosideL, 25-oxo-27normomordicoside L, and 25-Omethylkaravilagenin D Saponins: charantosides (I–VIII), momordicosides U, V, W; momordicoside M, N, O, L, triterpenoids A, B, C, D, E balsaminapentaol, balsaminol A, balsaminol B, cucurbalsaminol A, cucurbalsaminol B. Polysterols: decortinone, decortinol, clerosterol, ergosterol peroxide, 3 β-hydroxy-(22E,24R)ergosta-5,8,22-trien-7-one,22-diene-3β,7α-diol, 5 α,6 α-epoxy-(22E,24R)-ergosta-8, 6α-epoxy(22E,24R)-ergosta-8,22-diene-3 β,7 β-diol, 5 α,6 α-epoxy-(22E,24R)-ergosta8,22-diene-3β,7αdiol, and 5 α,6 α-epoxy-3β-hydroxy-(22E,24R)ergosta-8,22-dien-7-one Organic acids: citric acid, hydroxycitric acid, hibiscus acid, malic acid, and tartaric acid Anthocyanins: delphinidin-3-sambubioside (hibiscin), cyanidin-3-sambubioside (gossypicyanin), cyanidin-3,5-diglucoside, delphinidin (anthocyanidin) Flavonoids: hibiscitrin (hibiscetin-3 glucoside), sabdaritrin, gossypitrin, gossytrin and other gossypetin glucosides, quercetin, and luteolin Sterols: b-sitosterol and ergosterol Volatiles: 2-ethylfuran, hexanal, furfural, 5methyl-2-furaldehyde, eugenol, terpenes 1,4cineole and limonene

References [72]

[73]

(continued)

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Health Benefits of Underutilized Vegetables and Legumes

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Table 6 (continued) Common name Purslane

Botanical name Portulaca oleracea

Water convolvulus

Ipomoea aquatica

Adzuki bean

Vigna angularis

Rice bean

Vigna umbellata

Horse gram

Macrotyloma uniflorum

Stinky bean

Parkia speciosa

Major phytochemicals Flavonoids: kaempferol, apigenin, luteolin, myricetin, quercetin, portulacanones A-D Alkaloids: N-trans-feruloyltyramine, dopa, dopamine, noradrenaline, oleracein A-E, (3R)3,5-bis(3-methoxy-4-hydroxyphenyl)-2,3 dihydro-2(1H)-pyridinone and 1,5-dimethyl-6phenyl-1,2-dihydro-1,2,4-triazin-3(2H)-one Terpenoids: portuloside A and B, other monoterpene glycosides, portulene Flavonoids:3α,7β-Odiglycopyranosyldihydroquercetin Alkaloids: calystegine B1, calystegine B2, calystegine C1, calystegine B3 Phenolics: N-cis-feruloyl tyramine, N-transferuloyl tyramine, 3,5-di-O-caffeoyl-quinic acid (isoclorogenic acid a), 3,4-di-O-caffeoyl-quinic acid (isoclorogenic acid b), 4,5-di-O-caffeoylquinic acid (isoclorogenic acid c) Phenolics: catechin glycosides, quercetin glycosides, myricetin 3-rhamnoside, peonidin-3rutinoside and malvidin-3-O-glucoside, procyanidin dimmers Phenolics: catechin, epicatechin, p-coumaric acid, ferulic acid, vitexin, isovitexin, sinapic acid, quercetin Flavonoids: quercetin, kaempferol, myricetin, daidzein, genistein Phenolics: gallic acid., protocatechuic acid, ρhydroxybenzoic acid, vanillic acid, syringic acid, caffeic acid, chlorogenic acid, ferulic acid, sinapic acid, ρ-coumaric acid Flavonoids: quercetin, myricetin, luteolin, kaempferol, apigenin Phenolics: gallic acid, catechin, ellagic acid, quercetin Terpenoids: ß-sitosterol, stigmasterol, lupeol, campesterol, squalene

References [74]

[75]

[76]

[77]

[78]

[43]

Madagascar periwinkle (Catharanthus roseus) [84]. Several classes of alkaloids including terpenoidal, indole, bisindole, quinoline, and isoquinoline alkaloids were recognized with a promising antimalarial activity [85]. Morphine (isoquinoline alkaloid; opium poppy) and arecoline (pyridine alkaloids; areca nut) have been proven to be useful in curing neurodegenerative diseases such as Alzheimer’s and schizophrenia, respectively [86]. Purslane an underutilized vegetable is reported to contain alkaloids such as N-trans-feruloyltyramine, dopa, dopamine, noradrenaline, oleracein A-E, (3R)-3,5-bis(3-methoxy-4-hydroxyphenyl)-2,3 dihydro-

20

H. N. Murthy and K. Y. Paek

2(1H)-pyridinone, and 1,5-dimethyl-6-phenyl-1,2-dihydro-1,2,4-triazin-3(2H)one (Table 6) [74]. Similarly, calystegine B1, calystegine B2, calystegine C1, and calystegine B3 were isolated from water convolvulus (Table 6) [75].

3.4

Volatiles

Volatiles or essential oils are natural products belonging to varied classes, viz., terpenoids, fatty acid degradation products, phenylpropanoids, amino acid derivatives, alkanes, alkenes, alcohols, esters, aldehydes, and ketones [87]. Numerous essential oils are historically used in cosmetics and perfume industries; also, they have depicted varied biological activities in human. For example, ßcaryophyllene (lipophilic sesquiterpene) has demonstrated a potent anti-inflammatory activity in mice model [88]. Zerumbone (a humulene sesquiterpene) showed anti-cancer and chemoprotective activities, and it induces G2/M cell cycle arrest and apoptosis via mitochondrial pathway in Jurkat cancer cell lines [89]. Similarly, many more volatiles isolated from plants have demonstrated bactericidal, virucidal, fungicidal, antiparasitic, and insecticidal activities [90]. Underutilized vegetables are reported to possess volatiles; for instance, 2ethylfuran, hexanal, furfural, 5-methyl-2-furaldehyde, eugenol, terpenes 1,4-cineole, and limonene were reported from roselle (Table 6) [73]. β-caryophyllene, ethyl linolenate, methyl salicylate, β-pinene, hexadecanoic acid, methyl linolenate, benzyl alcohol, germacrene D, carene, β-elemene, and decanal were isolated from tomatillo [26].

3.5

Lectins

Lectins are non-catalytic sugar-binding proteins (glycoproteins) of non-immune origin and are widely distributed in plants especially in legumes. These proteins bind to sugars on the surfaces of cells in the gut wall, thereby interfering with nutrient breakdown and absorption; therefore, these are called antinutrients. Lectins from legumes are relatively stable, heat denaturation, proteolytic digestion and have varied biological activities such as immunomodulating effects, cytotoxicity against cancer cells, and antimicrobial and insecticidal effects [91]. Plant lectins have been regarded as natural defense molecules against insects, and they bind to insect gut and exhibit insecticidal activity against a large array of insect species. The effects of lectins following ingestion by insect larvae include growth inhibition; reduced size and weight gain; interference in female fecundity, as well as reduced pupation and percentage of adult emergence; and increased total development time, which in some case resulted in the death of insect larvae. Such lectins are suggested to be promising against insect pests and have been transferred into a variety of crops via genetic transformation [92]. Some of the lectins have been reported to possess antitumor activities and possess significant antiproliferative and apoptosis-inducing effects towards a variety of cancer cell types [93]. Lectins have been shown to have

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antimicrobial activity and inhibit the growth of several bacteria and fungi [94, 95]. Lectins were also isolated from two underutilized legumes, viz., Canavalia ensiformis [96] and Lathyrus cicera [97].

3.6

Glucosinolates

Glucosinolates are a group of plant thioglucosides found among several plants especially Brassicaceae members such as brussel sprouts, cabbage, broccoli, and cauliflower. These are a class of organic compounds containing sulfur and nitrogen and are derived from glucose and an amino acid [98]. Plants possessing glucosinolates also contain the enzyme thioglucoside glucohydrolase (myrosinase). When glucosinolates and myrosinase come in contact with each other in the presence of water, the enzyme immediately causes the hydrolysis of the parent glucosinolate. The hydrolysis products consist of an aglycone moiety, glucose, and sulfate. The aglycone moiety is unstable and rearranges to form isothiocyanates, thiocyanates, nitriles, oxazolidinethiones, and epithionitriles depending upon the structure of the glucosinolate [99]. Isothiocyanates, thiocyanates, nitriles, oxazolidinethiones and epithionitrites possess diverse biological activities including protection against various pathogens and weeds in case of plants and are potent anticarcinogens. For instance, glucosinolate products, namely, glucoiberin, glucoerucin, glucoheirolin, and glucotropaeolin, were reported to inhibit the growth of plant pathogens (Rhizoctonia solani, Sclerotinia sclerotiorum, Diaporthe phaseolorum, and Pythium irregulare) reported that the hydrolysis products of alkyl and aryl glucosinolates were cytotoxic to Salmonella typhimurium [100, 147]. Therefore, alkyl isothiocyanates are used as a preservative in food industry. Glucosinolate hydrolysis products are bioactive and have the potential to be used as naturally produced pesticides for the control of a number of soil-borne pests such as nematodes [101]. Glucosinolates and their hydrolysis products are reported to have antimutagenic and chemopreventive activities [99]. Underutilized vegetables such as yellowcresses (Rorippa indica) and sea kale (Crambe maritima) also possessed glucosinolates, and these could be used as alternative sources of these compounds [102, 103].

3.7

Organic Acids

Underutilized vegetables are rich sources of organic acids; for instance, roselle contains citric acid, hydroxycitric acid, hibiscus acid, malic acid, and tartaric acid (Table 6) [73]. Hydroxycitric acid is reported to be a major organic acid found in fruits of brindle berry (Garcinia gummigutta) and kokum (Garcinia indica) [104], and it is an antiobesity (decreased lipogeneis and enhanced fat oxidation) drug [105]; in the background of this, roselle calyces (calyx of flowers) could be an alternative source of hydroxycitric acid. Tartaric acid, malic acid, and citric acid are used as antioxidants [106]; therefore, roselle calyx extract could be also used as a source of antioxidants.

22

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Biological Activities of Phytochemicals Isolated from Underutilized Vegetables and Legumes

Phytochemicals isolated from UVLs have exhibited several biological effects including antidiabetic, anticancer, antimicrobial, antioxidant, antihypertensive, anti-inflammatory, and hepatoprotective effects (Table 7; Fig. 2). These biological effects of phytochemicals of UVLs demonstrate that consumption of UVLs has been strongly associated with reduced risk of cardiovascular disease, cancer, and diabetes.

4.1

Antidiabetic Activity

Diabetes mellitus is a chronic metabolic disorder of endocrine system, and it is characterized by persistent hyperglycemia which results in chronic complications in body metabolism. Diabetes can be classified as type 1 diabetes mellitus, type 2 diabetes mellitus, and gestational diabetes [135]. Studies have shown that phytochemicals isolated from UVLs have antidiabetic properties. It was reported that isolated compounds from bitter gourd such as charantin (charantin is a mixture of two steroidal saponins, ß-sitosteryl glucoside and 5,22-stigmasteryl glucoside; Fig. 3 (20), momordicilin [Fig. 3 (25)], and karavilosides [Fig. 3 (26)] have demonstrated potential effect in lowering blood sugar by increasing glucose uptake and glycogen synthesis in the liver, muscles, and fat cells and activating insulin receptor substrate1 in skeletal muscle by tyrosin phosphorylation [107–109]. The ethanolic extracts of rice bean containing catechin [(Fig. 3 (6)], epicatechin [Fig. 3 (7)], p-coumaric acid [Fig. 3 (3)], ferulic acid [Fig. 3 (4)], vitexin [Fig. 3 (10)], isovitexin [Fig. 3 (9)], sinapic acid [Fig. 3 (5)], and quercetin [Fig. 3 (8)] have been reported to have antidiabetic potential. Research work done by Jamaluddin et al. [133, 134] showed the hypoglycemic activities of chloroform extract from seeds and empty pods of stinky bean containing stigmasterol [Fig. 3 (23)], ß-sitosterol [Fig. 3 (22)], and stigmast-4-en-3-one [Fig. 3 (21)]. Kuriya et al. [129] revealed that flavonoids, namely, catechin 7-O-β-D-glucopyranoside [Fig. 3 (11)], epicatechin 7-O-β-Dglucopyranoside [Fig. 3 (12)], and catechin which were isolated from adzuki bean had antihyperglycemic effects. These reports display the role of UVLs in the treatments of diabetes.

4.2

Anticancer Activity

Cancer is one of the most deadly diseases; the global cancer burden is estimated to have risen to 18.1 million new cases and 9.6 million deaths in 2018. One in five men and one in six women worldwide develop cancer during their lifetime, and one in eight men and one in eleven women die from the disease. Worldwide, the total number of people who are alive within 5 years of a cancer diagnosis, called the 5-year prevalence, is estimated to be 43.8 million [136]. Chemotherapy is one of the main methods used in systemic therapy with side effects. Varied evidences

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Table 7 Biological activities of phytochemicals isolated from some underutilized vegetables and legumes Common name Bitter gourd

Botanical name Momordica charantia

Biological activity Antidiabetic activity Anticancer activity

Roselle

Hibiscus sabdariffa

Antimicrobial activity Antioxidant activity Hepatoprotective activity Anticancer activity Antihypertensive activity

Purslane

Water Convolvulus

Portulaca oleracea

Antioxidant activity

Ipomoea aquatica

Antiinflammatory activity Antidiabetic activity Cytotoxic activity

Adzuki bean

Vigna angularis

Antioxidant activity

Phytochemicals responsible for biological activities Triterpenoids: momordicilin charntin, karavilosides Saponin: 3β,7βdihydroxy-25methoxycucurbita-5,23diene-19-al Phenolic acid: protocatechuic acid Polyphenols: delphinidin3-glucoside and protocatechuic acid Phenolic acid: protocatechuic acid Phenolic acid: protocatechuic acid Anthocyanins: delphinidin-3-Osambubioside (hibiscin) and cyanidin-3-Osambubioside (gossypicyanin) Phenolic acids: chlorogenic, caffeic, pcoumaric, ferulic, and rosmarinic acids Flavonoids: quercetin and kaempferol Alkaloid: oleracein Alkaloid: oleracein

Polyphenols: isochlorogenic acids a, b, and c Flavonoid glycoside: 3α,7β-O-Ddiglycopyranosyldihydroquercetin Flavonoids: procyanidins B-1 and B-3, peonidin-3rutinoside and malvidin-3O-glucoside Phenolic acids: caffeic acid, ferulic acid

References [107–109]

[110]

[111] [112–114]

[112, 115, 116] [117–119] [120, 121]

[122]

[123]

[124]

[125]

[126–128]

(continued)

24

H. N. Murthy and K. Y. Paek

Table 7 (continued) Common name

Botanical name

Biological activity Antihyperglycemic activity

Rice bean

Vigna umbellata

Antioxidant activity

Antidiabetic activity

Horse gram

Stinky bean

Macrotyloma uniflorum

Antimicrobial activity

Parkia speciosa

Antioxidant activity Antioxidant activity Hypoglycemic activity

Phytochemicals responsible for biological activities Flavonoids: catechin 7-Oβ-D-glucopyranoside (C7G), epicatechin 7-O-βD-glucopyranoside (E7G), and catechin Phenolics: catechin, epicatechin, p-coumaric acid, ferulic acid, vitexin, isovitexin, sinapic acid, quercetin Phenolics: catechin, epicatechin, p-coumaric acid, ferulic acid, vitexin, isovitexin, sinapic acid, quercetin Polysaccharides: Dribose, D-arabinose, Dxylose, D-mannose, Dgalactose, and D-glucose Anthocyanins: cynidin, petunidin, delphinidin Polyphenols: gallic acid, catechin, ellagic acid, quercetin Phytosterols: stigmast-4en-3-one, β-sitosterol and stigmasterol

References [129]

[77]

[77]

[130]

[131] [132]

[133, 134]

suggest that bioactive compounds isolated from botanical sources are quite useful in cancer treatments [137]. Recent accumulating evidences have demonstrated that phytochemicals isolated from UVLs have shown anticancer activities and are useful in cancer treatment (Table 7). For example, 3β,7β-dihydroxy-25methoxycucurbita-5,23-diene-19-al (saponin) [Fig. 3 (24)] isolated from bitter gourd exhibited anticancer activity [137]. Protocatechuic acid (phenolic acid) [Fig. 3 (1)] extracted from roselle depicted antitumor activity [117–119]. Similarly, the crude methanolic extract of Ipomoea aquatica as well as its column fraction and the purified compound 3α,7β-O-D-diglycopyranosyl-dihydroquercetin (flavonoid) [Fig. 3 (13)] isolated from water convolvulus were investigated for cytotoxic properties against normal and cancer cell lines, Vero (normal African green monkey kidney) and Hep-2 (human larynx epithelial carcinoma) cell and A-549 (human small-cell lung carcinoma). The purified compound showed cytotoxicity towards cell cultures with CTC50 values of 387 mg/ml against normal Vero cell line and 156 and 394 mg/ml against Hep-2 and A-549 cell lines, respectively [125].

1

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Fig. 2 Biological activities of phytochemicals isolated from underutilized vegetables and legumes

4.3

Antimicrobial Activity

Microbial infection is one of the great threats to human health; therefore, looking for safe, effective, and specific antimicrobial phytochemicals has always been a rewarding research. The in vitro inhibitory effect of roselle calyx extract and protocatechuic acid (phenolic) [Fig. 3 (1)] derived from roselle calyx was studied by Liu et al. [111] on the growth of methicillin-resistant Staphylococcus aureus, Klebsiella pneumoniae, Pseudomonas aeruginosa, and Acinetobacter baumannii. The data from inhibition zone and the minimum inhibitory concentration (MIC) values showed that both roselle calyx extract and protocatechuic acid inhibited effectively the growth of all test bacterial pathogens, the antibacterial activity of protocatechuic acid being significantly greater than roselle calyx extract. Similarly, Basu et al. [130] demonstrated antibacterial activity of several polysaccharides such as D-ribose, Darabinose, D-xylose, D-mannose, D-galactose, and D-glucose isolated from horse gram against Staphylococcus aureus, Bacillus subtilis, Escherichia coli, and Pseudomonas aeruginosa. In summary, phytochemicals of UVLs have broad medicinal prospects including antimicrobial activities.

4.4

Antihypertensive Activity

Hypertension is the most chronic health problem among the people, in which the blood pressure in the arteries is persistently elevated. Long-term blood pressure is a

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Fig. 3 (continued)

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Fig. 3 Structures of some of the phytochemicals isolated from underutilized vegetables and legumes

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major risk factor for coronary artery disease, stroke, heart failure, atrial fibrillation, peripheral arterial disease, vision loss, chronic kidney disease, and dementia [138]. Worldwide, hypertension is estimated to cause 7.5 million deaths, about 12.8% of all total deaths [139]. The use of herbal medicine and phytochemicals from herbal plants as a treatment modality has significantly increased over the several decades [140]. Several UVLs are reported to be very much useful in combating hypertension; for example, dried roselle (Hibiscus sabdariffa) calyces are widely used in preparation of beverage to overcome hypertensions. Tea of roselle calyces showed 1.2% reduction of systolic blood pressure and 10.7% decrease in diastolic pressure [141]. Effectiveness and tolerability of a standardized extract were tested on patients/ human volunteers with mild to moderate hypertension which revealed a reduction in systolic and diastolic blood pressure by more than 10% [120]. In another set of investigation, Herrera-Arellano [142] carried out the randomized, double-blind, lisinopril-controlled clinical trials by using standardized herbal medicinal product of roselle on patients with hypertension, and their results revealed that the antihypertensive activity was due to diuretic activity and inhibition of angiotensinconverting enzyme. Ojeda et al. [121] isolated and characterized anthocyanins, namely, delphinidin-3-O-sambubioside [Fig. 3 (16)] and cyanidin-3-Osambubioside [Fig. 3 (17)], and these two compounds displayed angiotensinconverting enzyme activity. These results are in good agreement with the folk medicinal use of roselle calyces as antihypertensive drug.

4.5

Antioxidant Activity

Several types of reactive species are generated in the body as a result of metabolic reactions in the form of free radicals or non-radicals. These species may be either oxygen-derived or nitrogen-derived. They attack macromolecules including protein, DNA, and lipid, causing cellular/tissue damage. Oxidants also cause varied chronic disorders, cardiovascular problems, diabetes, cancer, and rheumatoid arthritis [143]. Many phytochemicals are antioxidants which will minimize the oxidant levels in the body; these include phenolics, terpenoids, flavonols, volatile oils, and plant pigments [115]. UVLs are abundant with phytochemicals which have depicted potent antioxidant activity (Table 7). It was demonstrated that protocatechuic acid (phenolic acid) [Fig. 3 (1)] isolated from roselle (Hibiscus sabdariffa) flowers has a protective effect against cytotoxicity and genotoxicity induced by tert-butyl hydroperoxide in a primary culture of rat hepatocytes, and it was proposed that one of the mechanisms of this protective effect was associated with the scavenging of free radicals [112]. Another compound, viz., delphinidin-3-glucoside (anthocyanin), obtained from roselle also showed potent antioxidant activity (trolox equivalent antioxidant capacity test) [113]. Varied compounds of purslane (Portulaca oleracea), namely, chlorogenic, caffeic, p-coumaric, ferulic, and rosmarinic acids, quercetin, kaempferol, and oleraceins depicted strong antioxidant activities [122]. Flavonoids {procyanidin B-1 [Fig. 3 (14)] and B-3 [Fig. 3 (15)], peonidin 3-rutinoside [Fig. 3 (18)], and malvidin-3-O-glucoside [Fig. 3 (19)]} and phenolic acids {caffeic acid

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[Fig. 3 (2)] and ferulic acid [Fig. 3 (4)]} of adzuki bean (Vigna angularis) were also very good antioxidants [126–128]. Polyphenols (catechin, epicatechin, p-coumaric acid, ferulic acid, vitexin, isovitexin, sinapic acid, quercetin) of rice bean, anthocyanins (cynidin, petunidin, delphinidin) of horse gram, and polyphenols (gallic acid, catechin, ellagic acid, quercetin) of stinky bean also have demonstrated powerful antioxidant activities [77, 131, 132].

4.6

Hepatoprotective Activity

The liver is one of the vital organs in the human body which is involved in the secretion of bile and helps in metabolisms of carbohydrates and fats. Many biological and chemical factors may cause hepatic diseases, and healthy diet rich in phytochemicals may be helpful in overcoming hepatic diseases [144]. Underutilized vegetables are good source of phytochemicals which are reported to protect against hepatic injury. Protective effects of flower extracts of roselle against oxidative stress in rat primary hepatocytes were demonstrated [117]. Protocatechuic acid (phenolic compound) isolated from roselle showed curative effect against cytotoxicity and genotoxicity of hepatocytes induced by tert-butyl hydroperoxide. One of the mechanisms associated with its property is scavenging of free radicals [117, 145]. Similarly, the role of protocatechuic acid in overcoming lipopolysaccharide-induced rat hepatic damage was demonstrated by Lin et al. [116].

4.7

Anti-inflammatory Activity

Inflammation is part of the complex biological response of body tissues to infection, injury, or irritation. Various studies have suggested that the anti-inflammatory effect is mediated through the regulation of various inflammatory cytokines, such as nitric oxide, interleukins, tumor necrosis factor alpha, and interferon gamma [146]. UVLs contain several phytochemicals that show anti-inflammatory effects. For example, oleracone {6-acetyl-2,2,5-trimethyl-2,3-dihydrocyclohepta[b]pyrrol-8(1H)-one; an alkaloid [Fig. 3 (27)]} isolated from purslane (Portulaca oleracea) showed antiinflammatory ability with lipopolysaccharide-stimulated macrophages [123].

5

Conclusions

UVLs are good sources of macronutrients such as proteins, carbohydrates, and fat (Table 3). They are also storehouses of minerals, vitamins, amino acids, and nonnutritional bioactive compounds (Tables 3, 4, 5, and 6). The amounts of nutrients present in UVLs are on par with major vegetables and legumes (Tables 4 and 5). Wide range of phytochemicals including polyphenols, terpenoids, alkaloids, and nitrogen-containing compounds (Table 6) are abundant in UVLs, and these phytochemicals showed a wide range of health benefits such as protection against

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cardiovascular diseases, diabetes, cancer, and dementia and improved cognitive functions (Table 7). Therefore, popularization, cultivation, and utilization of UVLs are necessary especially in thickly populated, poverty-stricken countries. Many of the UVLs are valuable components to attain nutritional security, have commercial value, and are therefore an important source of household income. Acknowledgments This work was supported by UGC-BSR mid-career award grant [No. F. 19223/2018(BSR)].

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106. Cunha SC, Fernandes JO, Ferreira IM (2002) HPLC/UV determination of organic acids in fruit juices and nectars. Eur Food Res Technol 214:67–71 107. Prakash A, Ng TB, Tso WW (2002) Purification and characterization of charantin, a napin-like ribosome-inactivating peptide from bitter gourd (Momordica charantia) seeds. J Peptide Res 59:197–202 108. Akihisa T, Higo N, Tokuda H, Ukiya M, Akazawa H, Tochigi Y, Kimura Y, Suzuki T, Nishino H (2007) Cucurbitane-type triterpenoids from the fruits of Momordica charantia and their cancer chemopreventive effects. J Nat Prod 70:1233–1239 109. Begum S, Ahmed M, Siddiqui BS, Khan A, Saify ZS, Arif M (1997) Triterpenes, a sterol and a monocyclic alcohol from Momordica charantia. Phytochemistry 44:1313–1320 110. Weng JR, Bai LY, Chiu CF, Hu JL, Chiu SJ, Wu CY (2013) Cucurbitane triterpenoid from Momordica charantia induces apoptosis and autophagy in breast cancer cells, in part, through peroxisome proliferation activated receptor γ-activation. Evid Based Complement Alternat Med 2013:1–12. Article ID 935675. https://doi.org/10.1155/2013/935675 111. Liu KS, Tsao SM, Yin MC (2005) In vitro antibacterial activity of roselle calyx and protocatechuic acid. Phytother Res 19:942–945 112. Tseng TH, Kao ES, Chu CY, Chou FP, Lin Wu HW, Wang CJ (1997) Protective effects of dried flower extracts of Hibiscus sabdariffa L. against oxidative stress in rat primary hepatocytes. Food Chem Toxicol 35:1159–1164 113. Degenhardt A, Knapp H, Winterhalter P (2000) Separation and purification of anthocyanins by high-speed countercurrent chromatography and screening for antioxidant activity. J Agric Food Chem 48:338–343 114. Mohd-Esa N, Hern FS, Ismail A, Yee CL (2010) Antioxidant activity in different parts of roselle (Hibiscus sabdariffa L.) extracts and potential exploitation of the seeds. Food Chem 122:1055–1060 115. Brewer MS (2011) Natural antioxidants: sources, compounds, mechanism of action, and potential applications. Compr Rev Food Sci Food Saf 10:221–247 116. Lin WL, Hsieh YJ, Chou FP, Wang CJ, Cheng MT, Tseng TH (2003) Hibiscus protocatechuic acid inhibits lipopolysaccharide-induced rat hepatic damage. Arch Toxicol 77:42–47 117. Tseng TH, Wang CJ, Kao ES, Chu HY (1996) Hibiscus protocatechuic acid protects against oxidative damage induced by tert-butyl hydroperoxide in rat primary hepatocytes. Chem Biol Interact 101:137–148 118. Tseng TH, Hsu JD, Lo MH, Chu CY, Chou FP, Huang CL, Wang CJ (1998) Inhibitory effect of Hibiscus protocatechuic acid on tumor promotion in mouse skin. Cancer Lett 126:199–207 119. Tseng TH, Kao TW, Chu CY, Chou FP, Lin WL, Wang CJ (2000) Induction of apoptosis by Hibiscus protocatechuic acid in human leukemia cells via reduction of retinoblastoma (RB) phosphorylation and Bcl-2 expression. Biochem Pharmacol 60:307–315 120. Herrera-Arellano A, Flore-Romero S, Chavez-Soto MA, Tortoriello J (2004) Effectiveness and tolerability of standardized extract from Hibiscus sabdariffa in patients with mild to moderate hypertension: a controlled and randomized clinical trial. Phytomedicine 11:375–382 121. Ojeda D, Jimenez-Ferrer E, Zamilpa A, Herrera-Arellano A, Tortoriello J, Alvarez L (2010) Inhibition of angiotensin converting enzyme (ACE) activity by the anthocyanins delphinidinand cynidin-3-O-sambubiosides from Hibiscus sabdariffa. J Enthnopharmacol 127:710 122. Erkan N (2012) Antioxidant activity and phenolic compounds of fractions from Portulaca oleracea L. Food Chem 133:775–781 123. Meng Y, Ying Z, Xiang Z, Hao D, Zhang W, Zheng Y, Gao Y, Ying X (2017) The antiinflammation and pharmacokinetics of a novel alkaloid from Portulaca oleracea L. J Pharm Pharmacol 68:397–405 124. Okudaira R, Kyanbu H, Ichiba T, Toyokawa T (2005) Ipomoea extracts with disaccharideinhibiting activities. Jpn Kakai Tokkyo Koho JP 5:213–221 125. Prasad KN, Ashok G, Raghu C, Shivamurthy GR, Vijayan P, Aradhya SM (2005) In vitro cytotoxic properties of Ipomoea aquatica leaf. Indian J Pharmacol 37:397–398

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126. Ariga T, Koshiyama IK, Fukushima D (1988) Antioxidative properties of procyanidins B-1 and B-3 from azuki beans in aqueous systems. Agric Biol Chem 52:2717–2722 127. Han KH, Kitano-Okada T, Seo JM, Kim SJ, Sasaki K, Shimada K, Fukushima M (2015) Characterization of anthocyanins and proanthocyanidins of adzuki bean extracts and their antioxidant activity. J Funct Foods 14:692–701 128. Shi Z, Yao Y, Zhu Y, Ren G (2017) Nutritional composition and biological activities of 17 Chinese adzuki bean (Vigna angularis) varieties. Food Agric Immunol 28:78–89 129. Kuriya K, Nishio M, Ono N, Masuda Y, Katsuzaki H, Kondo S, Sono J, Nakamura M, Umekawa H (2019) Isolation and characterization of antihyperglycemic compounds form Vigna angularis extracts. J Food Sci 84:3172–3178 130. Basu S, Ghosh M, Bhunia RK, Ganguly J, Banik BK (2017) Polysaccharides from Dolichos biflorus Linn. and Trachyspermum ammi Linn. seeds: isolation, characterization and remarkable antimicrobial activity. Chem Cent J 11:118 131. Sreerama YN, Sashikala VB, Pratape VM (2010) Variability in the distribution of phenolic compounds in milled fractions of chickpea and horse gram: evaluation of their antioxidant properties. J Agric Food Chem 58:8322–8330 132. Ko HJ, Ang LH, Ng LT (2014) Antioxidant activities and polyphenolic constituents of bitter bean Parkia speciosa. Int J Food Properties 17:1977–1986 133. Jamaluddin F, Mohamed S, Lajis MN (1994) Hypoglycaemic effect of Parkia speciosa seeds due to the synergistic action of ß-sitosterol and stigmasterol. Food Chem 49:339–345 134. Jamaluddin F, Mohamed S, Lajis MN (1995) Hypoglycemic effect of stigmast-4-en-3-one, from Parkia speciosa empty pods. Food Chem 54:9–13 135. IDF (2018) International Diabetes Federation (IDF), diabetes atlas, 6th edn. International Diabetes Federation, Brussels 136. IARC (2018) International agency for research on cancer. World Health Organization, Lyon 137. Wang H, Khor TO, Shu L, Su Z, Fuentes F, Lee JH, Kong ANT (2012) Plants against cancer: a review on natural phytochemicals in preventing and treating cancers and their druggability. Anti Cancer Agents Med Chem 12:1281–1305 138. Lackland DT, Weber MA (2015) Global burden of cardiovascular disease and stroke: hypertension at the core. Can J Cardiol 31:569–571 139. WHO (2020) Cardiovascular diseases (CVDs). World Health Organization, Geneva 140. Al Disi SS, Anwar MA, Eid AH (2016) Anti-hypertensive herbs and their mechanisms of action: Part I. Front Pharmacol 6:323 141. Haji-Faraji M, Haji-Tarkhani A (1999) The effect of sour tea (Hibiscus sabdariffa) on essential hypertension. J Ethnopharmacol 65:231–236 142. Herrera-Arellano A, Miranda-Sanchez J, Avila-Castro P, Herrera-Alvarez S, Jimenez-Ferrer JE, Zamilpa A, Roman-Ramos R, Ponce Monter H, Tortoriello J (2007) Clinical effect produced by a standardized herbal medicinal product of Hibiscus sabdariffa on patients with hypertension. A randomized, double blind, lisinopril-controlled clinical trial. Planta Med 73:6–12 143. Liochev SI (2013) Reactive oxygen species and the free radical theory of aging. Free Radic Biol Med 60:1–4 144. Madrigal-Santillan E, Madrigal-Bujaidar E, Alvarez-Gonzalez I, Sumaya-Martinez MT, Salinas JG, Bautista M, Morales-Gonzalez A, Gonzalez-Rubio MGL, Aguilar-Faisal JL, Morales-Gonzalez JA (2014) Review of natural products with hepatoprotective effects. World J Gasterotenterol 20:14787–14804 145. Liu CL, Wang JM, Chu CY, Cheng MT, Tseng TH (2002) In vivo protective effect of protocatechuic acid on tert-butyl hydroperoxide induced rat hepatotoxicity. Food Chem Toxicol 40:635–641 146. Zhu F, Du B, Xu B (2017) Anti-inflammatory effects of phytochemicals from fruits, vegetables, and food legumes: a review. Crit Rev Food Sci Nutr 58:1260–1270 147. Manici LM, Lazzeri L, Palmieri S (1997) In vitro fungitoxic activity of some glucosinolates and their enzyme-derived products toward plant pathogenic fungi. J Agric Food Chem 45:2768–2773

Part I Bioactive Compounds in Underutilized Vegetables: Leafy Vegetables

2

Bioactive Compounds of Amaranth (Genus Amaranthus) Puneet Gandhi, Ravindra M. Samarth, and Kavita Peter

Contents 1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1 This Plant Needs to Be Seen in a Different Perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 Bioactive Compounds in Amaranthus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 Use in Ancient Medicine . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1 Traditional Uses in India . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 Traditional Uses in the Rest of the World . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 Clinical Studies of Amaranthus Species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 Fortified Food Products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 Cosmetic Applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 Toxicity Issues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.1 Food Allergy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2 Livestock Poisoning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

41 41 44 57 57 60 61 62 62 67 67 68 68 68

Abstract

Several species of Amaranthus have a long history of consumption as a vegetable/ cereal and usage in traditional medicine. A great miscellany of healthful compounds such as fatty acids, steroids, lipids, amino acids, vitamins, minerals, and bioactives, including alkaloids, flavonoids, glycosides, phenolic acids, saponins, terpenoids, tannins, and carotenoids have been found in Amaranthus seeds, roots, stem, and leaves, depending on the plant maturity stage, cultivar type, and geographical location. Preclinical studies have shown that the extracts and bioactive constituents of Amaranthus spp. confer several biological activities, P. Gandhi (*) · R. M. Samarth Department of Research, R & T Block, Bhopal Memorial Hospital and Research Centre, Bhopal, India K. Peter Department of Biotechnology, Barkatullah University, Bhopal, India © Springer Nature Switzerland AG 2021 H. N. Murthy, K. Y. Paek (eds.), Bioactive Compounds in Underutilized Vegetables and Legumes, Reference Series in Phytochemistry, https://doi.org/10.1007/978-3-030-57415-4_3

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including antioxidant, immunomodulatory, hepatoprotective, gastroprotective, cardioprotective, hypolipidemic, anticancerous, antidiabetic, and antimicrobial, which has ignited the interest of researchers in this modest vegetable all over the world. Although some potential health benefit-based mechanistic studies are available, a need exists to investigate in-depth the roles of these specific bioactives sourced from Amaranthus for their potential use in disease treatment and daily diet for a holistic well-being. Lately, investigators have also started to examine the use of amaranth leaves and seeds for the development of fortified food products whose consumption can lead to beneficial biological effects. Conversely, the plant is still missing recognition in the pharmaceutical and commercial food packaging sectors. The present chapter provides a detailed exploration of current research on the bioactive-constituents of amaranth, its use in traditional medicine, clinical studies validating traditional claims and recent trends in usage of this underutilized vegetable as a nutraceutical and functional food. This insight will be beneficial for encouraging exhaustive research which will promote effective utilization of amaranth. Keywords

Amaranth · Bioactives · Biological activity · Fortified food · Nutraceutical · Traditional medicine Abbreviations

BMI CE DM
DM DW FW GAE GAF GST Hb HDL HIV LPO MDA MRS NO QE RBC RDA RE SOD SP

Body mass index Catechin equivalent Dry matter Diabetes mellitus Dry weight Fresh weight Gallic acid equivalent Germinated amaranth flours Glutathione-S-transferase Hemoglobin High-density lipoprotein Human immunodeficiency virus Lipid peroxidation Malondialdehyde Menopause rating scale Nitric oxide Quercetin equivalent Red blood cells Recommended dietary allowance Rutin equivalent Superoxide dismutase Soluble protein

2

Bioactive Compounds of Amaranth (Genus Amaranthus)

SPF TAC TAC* TFC TPC TTC UTI UV *

41

Sun protection factor Total antioxidant capacity Total anthocyanin content Total flavonoid content Total phenolic content Total tannin content Urinary tract infection Ultraviolet Denotes that the index term is used for less commonly used parameter

1

Introduction

1.1

This Plant Needs to Be Seen in a Different Perspective

Amaranthus L. is an herbaceous eudicot genus of the Amaranthaceae family of the order Caryophyllales and is commonly known as the pigweed or amaranth. Domesticated in the American continents about 6000 years ago, it was revered by many pre-Columbian civilizations, but it was practically dropped out of use after the Spanish colonization. The Spaniards discouraged the cultivation of Amaranthus as according to their belief; the use of grain amaranth was the very symbol of heathen idolatry [1]. It was only at the end of the last century in the 1980s, when the US National Academy of Sciences carried out a research project on Underexploited Tropical Plants with Promising Economic Value, that amaranth was elected from among 36 of the world’s most promising crops. Amaranthus is now acknowledged as a dual crop plant with major health and economic potential [2]. In current times, a major challenge for the human race is to cope up with selfcreated health issues particularly lifestyle diseases, which has led to an increasing awareness for more nutritiously balanced and organically grown vegetables and crops, putting the spotlight back on amaranth. The ≈75 species of amaranth are classified into three subgenera. These are found both as cultivated and as wild-type species that are used as food grains, leafy vegetables, potential forages, and ornamentals (Fig. 1). There are only three grainproducing species among which A. cruentus (purple amaranth) is the major one as it is cultivated in most parts of the globe [3]. A. hypochondriacus (prince’s feather) is also commonly grown for grain, while the third one, A. caudatus (love-lies-bleeding), also produces grain but it is more often grown as an ornamental. When used for its seed, A. caudatus varieties are best adapted to the tropical highlands. A. tricolor (tampala) is the most widely grown variety for its leaves which serve as a vegetable in many cuisines around the world. Other vegetable amaranths are represented by A. dubius, A. blitum (A. lividus), A. cruentus, A. hybridus, and A. viridis [4]. Amaranth leaves are a source of high-quality protein, as well as dietary fiber, in addition to other important bioactive components like essential amino acids, vitamins, minerals, flavonoids, and unsaturated fatty acids [5]. A total of six species under the genus Amaranthus were reviewed by Hussain [6] namely, A. retroflexus, A. spinosus,

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Fig. 1 Some commonly cultivated and wild type species of amaranth in India: A. hybridus, A. tricolor, A. cruentus, and A. viridis that have multiple uses as forage, grain production, and leafy vegetable

A. viridis, A. caudatus, A. hypochodriacus, and A. tricolor and 65 molecules were reported as phyto-constituents, majorly belonging to sesquiterpenes, glucosides, phenol compounds, steroidal molecules, terpenoids, saponins, flavonoids, and fatty acids (Fig. 2). Amaranth seed is frequently categorized as a pseudocereal, it is gluten-free, and it can be used by people with stomach ailments like celiac disease. The seed contains desirable levels of amino acids particularly lysine, minerals, essential oils, special lipids such as phytosterols, squalene, and polyphenols, and unsaturated fatty acids like tocopherols and tocotrienols required for a complete nutritious diet. These are not present in the same composition in other common oils, specifically, the high proportion of squalene, which has been shown to have antitoxic, antioxidant, and hepatotropic properties [7].

2

Bioactive Compounds of Amaranth (Genus Amaranthus)

43

Fig. 2 Biochemical structures of some important bioactives from Amaranthus spp. Source: (National Center for Biotechnology Information (2020). PubChem Compound Summary. Retrieved August 13, 2020 from https://pubchem.ncbi.nlm.nih.gov/compound/)

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There is now an increasing awareness on the use of Amaranth for people belonging to specific age groups such as high-performance athletes, malnourished children, or persons afflicted with diseases like diabetes and hypercholesterolemia. In a survey in Trinidad and Tobago, it was observed that younger people were more conscious of amaranth’s diet potential and taste, while the older native generation preferred it for its nutritional benefits [8]. Another extensive survey of households conducted by Coetzee [9] in Potchefstroom Campus of the North-West University, South Africa, revealed that the food security situation and nutritional intake of households could be improved by enriching the bread with up to 25% of grain amaranth flour, which the locals know to possess exceptional nutritional value and acceptable sensory characteristics. Thus, this less used vegetable and its seed are unique in composition with various bioactive compounds that make it pleiotropic in its biological activity. The health-promoting bioactives confer medicinal benefits such as hypocholesterolemic, antioxidant, anti-inflammatory, anticancer, antidiabetic, antinociceptive, antimicrobial, antimalarial, hepatoprotective, cardioprotective, and gastroprotective [10]. Amaranth is therefore a good substitute for traditional cereals and vegetables since it is affordable and widely available. This chapter presents the ancient and underutilized vegetable amaranth in a new perspective, highlighting its nutritional and health benefits attributable to its bioactives and its use as a modern-day food additive and clinical studies validating the traditional use.

2

Bioactive Compounds in Amaranthus

A bioactive compound is a component of food that can affect the physiological or cellular activities of the body on consumption and may provide desirable health benefits beyond basic nutrition. In the Indian subcontinent, Mexico, and countries of South Africa, where malnourishment and food security issues are imminent in the public health domain, consumption of local vegetables and their cooking methods are being given due consideration for maintaining a healthy living. There is accumulating scientific evidence that regular consumption of vegetables like Amaranthus is associated with lower the risk of life-style diseases like diabetes mellitus, hypertension, cardio-vascular disease, as the multiple bioactives act together for simultaneous targeting of various cell signaling pathways that regulate organ pathologies. Extensive reviews and dedicated book series have been published in the last quinquennial on Amaranthus and its utility, but the focus has now shifted to its bioactive compounds which actually bestow it with nutritional and health benefits. An exhaustive literature survey resulted in the following detailed analyses (Table 1) of bioactive compounds and elemental constituents from different plant parts (Fig. 3) of various species of Amaranthus, with the stated utilization, which make it a “super crop.” The enormous number of bioactive compounds in Amaranthus spp. as listed above, confer it with a greater potential for development of new nutraceutical supplements and functional foods. Laboratory studies indicate that the health

Extract type Methanolic

Aqueous

50% ethanolic

Amaranth species Matured leaf of A. spinosus

Leaf and stem of A. hybridus

Leaf and stem of A. viridis

Kumasi, Ghana

City of Potchefstroo, North-West Province, South Africa

Geographic region Mekelle, Tigray Province, Ethiopia

Bioactive compounds present/main biological activity reported Alkaloids, tannins, saponins, and glycosides were present with high content of total phenolics/strong antioxidant and antimicrobial activity The extract was rich in polyphenols (total phenolic contents: 2181.2 mg/ 100 g dm, total carotenoids (113.6 mg/ 100 g dm), and β-carotene (18.4 g/ 100 g dm). Lipid profile showed significant amounts of the fatty acids, linolenic, linoleic, and palmitic with moderate concentrations of palmitoleic, stearic, and lignoceric acid. It was rich in folic acid (72 mg/100 g dm), Ca, Mg, Fe, Zn, Se/improvement in cell viability accompanied with a significant decrease in DNA damage and genotoxic effects against two potent mycotoxins The phytochemicals present in the powder and of stems and leaves were rich in tannins, saponins, general glycosides, and alkaloids. Flavonoids were conspicuously absent/antioxidant and anticancer

Table 1 Qualitative and quantitative evaluation of bioactive compounds of different species of Amaranthus

(continued)

[13]

[12]

References [11]

2 Bioactive Compounds of Amaranth (Genus Amaranthus) 45

Extract type 70% ethanol

Methanolic

Amaranth species Matured fresh leaf, inflorescence, seed and root of A. blitum, A. caudatus, A. tricolor, A. blitoides, A. cruentus, A. albus, A. retroflexus

Leaf of A. tricolor

Table 1 (continued)

Guntur, Andhra Pradesh, India

Geographic region Tehran Province, Iran

Bioactive compounds present/main biological activity reported All examined taxa had flavonoid sulfate, flavon C & C-/O glycosides in all of their examined organs with the exception of A. tricolor. A. retroflexus root lacked flavon C & C-/ O glycosides Kaempferol, rutin, myercetin, quercetin, and vitexin were found in all of studied taxa inflorescences Leaves had isorhamnetin, kaempferol, and rutin. Quercetin was found in all of the studied species with the exception of A. blitum and A. caudatus species Seeds of all studied taxa with the exception of three species (A. blitum, A. blitoides, and A. retroflexus) contained chrycin All of taxa roots had kaempferol, quercetin, and rutin/antioxidant activities Preliminary phytochemical screening revealed the presence of phytoconstituents such as amino acids, carbohydrates, proteins, cardiac glycosides, steroids, alkaloids, flavonoids, and tannins/antibacterial against pathogens associated with UTIs [15]

References [14]

46 P. Gandhi et al.

Ibadan, Nigeria

–

Methanolic

Seed of A. cruentus A. hybridus A. caudatus A. hypochondriacus A. hybridus

Matured leaves and seeds of A. viridis

Lalliyan City, Sangli, India

Chennai, Tamil Nadu, India

Aqueous, butanol, acetone, chloroform, and aqueousbenzene

Leaf of A. viridis

Embrapa Cerrados, Brazil

Hexane

Seed- flour of A. cruentus Three major peptides under 3 kDa were detected, which exhibited HMG-CoA reductase inhibition/ hypocholesterolemic effect Aqueous and butanolic extracts had tannins whereas flavonoids and saponins were present only in aqueous extract. Acetonic extract showed the presence of saponins and cardiac glycosides while chloroform extract additionally had alkaloids and tannins. Aqueous-benzene extract had flavonoids and alkaloids/analgesic and antipyretic activity Highest tannin content (0.14 g/100 g) and Fe chelating (66.72%) capacity was recorded in A. caudatus A. cruentus had the highest total flavonoid (9.93 mg CE/100 g) content A. hybridus had the highest phytate (1.58 g/100 g) and total polyphenols (30.79 mg GAE/100 g)/food biofortification Phytochemical investigation showed tannins (6.07–5.96%), alkaloids (13.14– 11.42%). The extracts also contained appreciable levels of total phenolic contents (2.81–3.61 GAE, g/100 g), total flavanoid contents (18.4–5.42 QE, g/100 g)/free radical scavenging activity

Bioactive Compounds of Amaranth (Genus Amaranthus) (continued)

[19]

[18]

[17]

[16]

2 47

Extract type Methanolic

Aqueous, acetone, chloroform, ethanol, and methanol

Ethanolic and aqueous

Amaranth species Leaf of A. spinosus

Fresh leaf of A. spinosus

Powder of entire plant parts of A. viridis A. polygonoides

Table 1 (continued)

Erode, Tamil Nadu, India

Ahmednagar, India

Geographic region Redeyef, Tabarka, and Nasrallah, Tunisia

Bioactive compounds present/main biological activity reported Redeyef samples had the highest level of leaf protein content (3.54 g/100 g dry weight [DW]) and also were the richest source of carbohydrates (31.9 g/100 g DW). K, Ca, and Mg were the major nutrients. For micronutrients, only Fe was significantly higher than Zn and Mn. A total of 24 essential oils from leaf were identified, highest 90.77% being in Tabarka. Oxygenated monoterpenes, sesquiterpenes were the most abundant/ antioxidant and antihemolytic activities Different classes of secondary metabolites such as alkaloids, steroids, flavonoids, terpenoids, saponins, cardiac glycosides, and tannins were present/potential as a source of therapeutic agents Contains mostly tannins, saponins, alkaloids, steroids, terpenoids, proteins, cardioglycosides, and phenols Flavanoids were missing in both plant extracts. Ethanol extracts possess more constituents than aqueous extracts and they were more in A. viridis/ antioxidant activity

[22]

[21]

References [20]

48 P. Gandhi et al.

Petroleum ether, benzene, chloroform, and ethanolic extracts

Chloroform, ethyl acetate, acetone, ethanol, and aqueous –

Leaf of A. tristis

Aerial parts of A. cruentus

Seeds of A. hypochondriacus A. cruentus

–

Entire plant of A. cruentus A. hypochondriacus A. caudatus

Central Italy

Pune, Maharashtra, India

Gingee Fort, Tamil Nadu, India

Bydgoszcz, Poland

The highest amounts of protein were found in plants harvested at the beginning of blossoming (128 g/ kg DM) The highest content of Ca, Mg, and P were found in A. hypochondriacus. The whole plants of amaranth were found to contain on average 236.4 mg/kg of Fe in addition to Zn, Mn, and Cu A. hybridus had higher phenol content and pigments betanine and amaranthine than the other two plant cultivars/free radical scavenging activity Presence of carbohydrates, alkaloids, flavonoids, tannins, steroidal glycosides, and phenols was detected which was the maximum in ethanolic extract/potent hypoglycemic activity Ethanol extract of aerial parts contain high amounts of phenol and flavonoid compounds/antioxidant potential The crude oil content in seed ranged from 7.5% to 6.0%, with linoleic, palmitic, and oleic acids as the major fatty acids of the oil in both genotypes. The unsaponifiable fraction was rich in sterols (campesterol, stigmasterol, and β-sitosterol), and significant levels of squalene were found/unique nutraceutical properties (continued)

[26]

[25]

[24]

[23]

2 Bioactive Compounds of Amaranth (Genus Amaranthus) 49

Extract type Aqueous extract

Methanol, distilled water, chloroform hexane extract

Methanol extract

Amaranth species Plant of A. spinosus

Leaf of A. viridis

Leaf and seed of A. hypochondriacus

Table 1 (continued)

Mexico

Six Mile, Guwahati, India

Geographic region Kolhapur, Maharashtra, India

Bioactive compounds present/main biological activity reported Tannins, coumarin, saponin, proteins, amino acids, flavonoids, and cardial glycosides were present/potency for use in producing pharmaceutical bioactive compounds for therapeutic drugs Analysis revealed the presence of major phytochemical compounds, including flavonoids, alkaloids, phenolics, steroids, terpenoids, saponins, cardiac glycosides, and tannins. TPC, TFC, and TTC were found to be 16.4  0.45 mg CE/g of dry weight, 5.28  0.33 mg QE/g of dry weight, and 1.76  0.21 mg CE/g of dry weight/ antioxidant, antityrosinase, and antigenotoxicity potential Higher values of total phenolic compounds, total anthocyanins and condensed tannins were found in leaves and seed of plants grown in green houses as compared to open fields/ antioxidant capacity and higher secondary metabolites

[29]

[28]

References [27]

50 P. Gandhi et al.

Guntur, Andhra Pradesh, India

Sonepat, Haryana, India

Aqueous extract

–

Air-dried leaf of A. viridis

Roots of A. tricolor

Bangladesh

Acetone and methanolic extract

Leaf of A. tricolor

Pigments, β-carotene, vitamin C, TPC, TFC, TAC, phenolic acids, and flavonoids were detected in leaves. Trans-cinnamic acid was the newly identified phenolic acid. Salicylic acid, vanilic acid, trans-cinnamic acid, gallic acid, chlorogenic acid, rutin, isoquercetin, and m-coumaric acid were the most abundant phenolic compounds increased with the severity of salinity stress/good antioxidant and antiaging source Presence of flavonoids, saponins, and terpenoids was recorded while tannins were present in considerable amount/ free radical inhibition was high, source can be used as raw ingredient in the preparation of herbal-based drugs Phytochemical screening showed the presence of alkaloids, flavonoids, glycosides, tannins, proteins, and amino acids/antioxidant capacity (continued)

[32]

[31]

[30]

2 Bioactive Compounds of Amaranth (Genus Amaranthus) 51

Turin, Italy

–

Aqueous, methanol, ethanol, chloroform, and acetone

Leaf and seed of A. caudatus in various phases of plant growth

Fresh leaf of A. cruentus

Coimbatore, Tamil Nadu, India

Geographic region Rivers State and University of Port Harcourt, Nigeria

Extract type –

Amaranth species Leaf and root of A. hybridus A. spinosus

Table 1 (continued) Bioactive compounds present/main biological activity reported Flavonoids, alkaloids, glycoside, and phenolics were present. The total alkaloids contents varied form 29.69 g/ 100 g in the root of A. hybridus to 50.89 g/100 g in the root of A. spinosus. Flavonoids varied from 16.70 g/100 g in A. spinosus root to 23.08 g/100 g in A. hybridus. The concentration of phenolics ranged from 12.29 g/100 g in A. hybridus to 19.27 g/100 g in A. spinosus. There was no variation in alkaloid concentrations/Antimicrobial, antioxidant, antidiuretic, and valuable source of dietary vitamins The phenolic profile was characterized by 17 compounds in which rutin was predominant. Flavonols were most abundant in early flowering and seed fill stages. Highest content of hydroxycinnamic acid derivatives was found in early vegetative stage/ Valuable source of antioxidant Alkaloids, flavanoids, glycosides, amino acids, fatty acids, carbohydrates, saponins, proteins, phenolic compounds, tannins, sterols, terpenoids, anthocyanins, leuco-anthocyanins, and emodins were found to be present/ antidiabetic potential. [35]

[34]

References [33]

52 P. Gandhi et al.

San Luis Potosí, México

Bangladesh

–

–

Leaves at full flowering stage of A. hypochondriacus

Leaf of amaranth red morph

Flavonoids detected in leaves were rutin, isoquercetin, nictoflorin, and percentage of rutin was the highest among all medicinal plants reported till date. Accumulation of rutin increased when plants were grown under abiotic stress. Ten phenolic acids were detected; ferulic acid was only detected in red leaves, while coumaric acid was found only in green leaves. Caffeic acid was the main phenolic acid in both red and green leaves/mainly used for edible seed production, can also be used as vegetable because its leaves are a rich source of phytochemicals An excellent source of dietary fiber, carbohydrates, moisture, and protein. There were remarkable quantities of K, Ca, Mg (96, 10.13, 30.01 mg g1), Fe, Mn, Cu, Zn (1089.19, 243.59, 25.77, 986.61 μg g1), chlorophyll, β-cyanins, total flavonoids (102.10 RE μg g1 DW), β-xanthins, betalains (33.30, 33.09, 66.40 μg 100 g1), carotenoids, total phenolics (172.23 GAE μg g1 DW), β-carotene (1225.94, 1043.18 μg g1), vitamin C (955.19 μg g1)/for attaining nutritional and antioxidant sufficiency (continued)

[37]

[36]

2 Bioactive Compounds of Amaranth (Genus Amaranthus) 53

Amaranth species Leaf of A. tricolor A. lividus

Table 1 (continued)

Extract type –

Geographic region Bangladesh

Bioactive compounds present/main biological activity reported A. tricolor genotypes were an excellent source of pigments like betalain (1122.47 ng g1 FW), β-xanthin (585.22 ng g1 FW), β-cyanin (624.75 ng g1 FW), carotenoids (55.55 mg 100 g1 FW), vitamin C (122.43 mg 100 g1 FW), TFC (312.64 RE μg g1 DW), TPC (220.04 GAE μg g1 DW), TAC (DPPH and ABTS+) (43.81 and 66.59 TEAC μg g1 DW) compared to green color (A. lividus) genotype Remarkable phenolic acids namely, salicylic acid, vanillic acid, protocatechuic acid, gallic acid, gentisic acid, β-resorcylic acid, phydroxybenzoic acid, syringic acid, ellagic acid, chlorogenic acid, sinapic acids, trans-cinnamic acid, m-coumaric acid, caffeic acid, p-coumaric acid, ferulic acid, and flavonoids, such as rutin, hyperoside, isoquercetin, myricetin, quercetin, apigenin, kaempferol, and catechin were observed in the red color genotypes, which was much higher compared to the green color genotype. Four new flavonoids namely, quercetin, catechin, myricetin, and apigenin were identified/an excellent source of antioxidants

References [38]

54 P. Gandhi et al.

–

Germinated flour and amaranth grain Mexico

Ya’an city, China

Asterik mark (*) denotes the less commonly used index term for the parameter.

Hot aqueous extract

Aerial part of A. hybridus

Two purified acidic polysaccharides were obtained/the total antioxidant capacity of each milligram was higher than ascorbic acid GAF exhibited an increase in the concentrations of soluble protein, TPC, TFC, and TAC*/to produce functional ingredients for food product development [40]

[39]

2 Bioactive Compounds of Amaranth (Genus Amaranthus) 55

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P. Gandhi et al.

Fig. 3 Major bioactive constituents from seed, leaf/stem, and root of Amaranthus and their pharmacological activities

benefits can be attributed to the additive or synergistic interactions among the various phyto-constituents present in the whole plant. Amaranthus can thus serve as a safe, optimal, cost-effective source of nutraceutical as opposed to the expensive, synthetic, dietary supplements generally used by health-conscious consumers and from a practical point of view, it can be translated into popularizing the use of its leaves as vegetable and the grain for flour. Nonetheless, a gap analysis of this data indicates that still more detailed research is required to create a database of Amaranthus bioactives and validation of the biological effects so as to stimulate effective utilization of the vegetable and to bring into practice scientific-based dietary recommendations.

2

Bioactive Compounds of Amaranth (Genus Amaranthus)

3

57

Use in Ancient Medicine

Amaranthus extracts have been used in ancient India to treat several conditions. A. tricolor L. is documented in the Indian Ayurvedic pharmacopoeia as Ramasitalika (W.P.) [41]. The whole plant is dried and advocated in the treatment of Daha, Sosa, Visphota, and Vrana. It means A. tricolor can be used to treat Daha – burning sensation of the body, Sosa – destroying disease, Visphota – blistering skin disease, and Vrana – a nonhealing wound. The most important formulation is the Candrakali Rasa. Its cited preparation is 250 mg in water and the dose is twice a day, 10–20 ml of the drug in juice form [42]. In rural India, particularly the ethnic communities not only use their plant resources for food and livelihood but also utilize it to address any health issues. Generally, due to their low economic status and poor access to modern health facilities, ethnic tribes are forced to use the traditional health system to treat various ailments. Several attempts have been made to document and popularize such Indian folk medicine in a scientific manner (Fig. 4). Studies conducted in different parts of the globe in the last decade present a fair idea of Amaranth’s extensive traditional uses (Fig. 5).

3.1

Traditional Uses in India

Aphrodisiac: It was discovered that 78 plant species growing in the Himalayan region have aphrodisiac properties. An ethnobotanical study conducted in Kashmir

Fig. 4 Traditional uses of Amaranthus spp. in India

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Fig. 5 Traditional uses of Amaranthus spp. from the globe

revealed that the decoction obtained from A. spinosus is taken orally to treat erectile dysfunction and premature ejaculation [43]. Blood purifier: A. viridis L. is used as a blood purifier, in the treatment of piles, and as a digestive agent by Pawara, Bhil, and Pardhi tribes in Satpuda region of Dhule and Jalgaon districts of Maharashtra, India [44]. Chronic dysentery: A small piece (1–2 grams) of A. spinosus L. root is used as oral medicine for chronic dysentery according to a study conducted in three southern districts of West Bengal, India. The root paste is taken with water after mixing with some sugar and salt and the treatment is continued for 5–7 days [45]. Diarrhea, stomachache, and laxative: The Lepcha and Bhutia, the earliest ethnic groups in Sikkim, use A. viridis L. to treat diarrhea, gastroenteritis, and arthritis. They believe that curry prepared from “lattay sag” can stop diarrhea. Seeds, ground into powder, are mixed with water and are taken as an infusion to cure general gastric problems [46]. A survey at the study sites in Diamond Harbour, South 24-Parganas, West Bengal revealed that A. viridis L. whole plant decoction is used for stomach-ache and as laxative [47]. Digestive system disorders: A. spinosus L. decoction of fresh leaves and stem are taken orally twice a day for 3 days to cure indigestion among Paliyar and Muthuvar tribals in Theni District (Western Ghats), Southern India [48].

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A. spinosus L. leaf paste along with lemon juice is taken with food to cure stomach ulcers by the Adiya tribe in Wayanad district, Kerala [49]. Eczema and skin allergy: A. spinosus L. shoot infusion is applied for eczema until cured and this remedy is used in several villages of Sivagangai district in Tamil Nadu, India [50]. A decoction of the leaves is used during bath for treating skin allergy, by traditional healers in the silent valley of Kerala, India [51]. Fever and infection: A. viridis L. leaves are used for fever and eye infections in the Neerody coastal villages of Kanniyakumari district, Tamil Nadu, India [52]. Hair fall treatment: The juice of leaves of A. spinosus L. is applied to the hair to prevent premature greying and falling of hair by people in Madurai district, Tamil Nadu, India [53]. Jaundice/liver enlargement: An extract of A. spinosus L. whole plant is used for treating jaundice and liver enlargement by traditional healers in Alagar hills of Madurai district, Tamil Nadu, India [54]. Kidney stone: A. caudatus L. leaf extract is taken as a treatment for kidney stones traditionally in the Aravali region of Rajasthan [55]. As laxative and for pains in the limbs: A. cruentus L. whole plant is used as a laxative and for pain in the limbs by people in the Neerody coastal Villages of Kanniyakumari district, Tamil Nadu, India [52]. Leprosy: In the last few years, about 40 plant families and 75 species are documented on the basis of respective families, genera, and species for use against leprosy disease in India. A. viridis L. is used by the people of East Godavari area district of Andhra Pradesh for the treatment of leprosy [56, 57]. Piles and wounds: A mixture of the leaves of A. spinosus (Amaranthaceae) is used against piles and wounds by Pahari community of subdivision Mendhar, District Poonch, Jammu & Kashmir, India [58]. Pain during menstruation: Decoction of leaves of A. tristis Roxb. is given to drink for 3 days to reduce the pain during menstruation among the rural people in Sivagangai district of Tamil Nadu, Southern India [50]. The root paste of A. spinosus L. is mixed with a little amount of molasses before eating it in the morning to cure leucorrhoea and other menstruation-related problems in southern districts of West Bengal, India. Four to five grams of root is given daily for 15 days to achieve the desired result [59]. Skin diseases: A. tricolor L. is recommended for dandruff and ringworm in the coastal parts of Central Western Ghats, Karnataka, India [60]. Snakebite treatment: A. viridis L. leaves or stem paste is applied externally for the treatment of snakebite in Sugali tribes of Yerramalais of Kurnool district, Andhra Pradesh, India [61]. A. viridis leaf paste is also helpful for scorpion sting, according to the information collected on the basis of oral interview of old persons of the village, vadiyas, hakims, herbalists, and tribes in Jind district of Haryana [62]. Urinary disorder: A. spinosus L. leaves are used orally as a diuretic and herbal medicine by the Meena community in Rajasthan [63]. Wounds: A. graecizans L. leaf paste is applied twice a day for 3–5 days to cure wounds among the rural people in Sivagangai district of Tamil Nadu, Southern India [50].

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Traditional Uses in the Rest of the World

3.2.1 Africa Maternal health: A. cruentus leaf decoction in water is given orally 2 g/day for 7 days to stop bleeding during pregnancy. A. hybridus leaves and stem are macerated and soaked in water to be given orally at a dose of 1 g/day for 60 days to facilitate delivery and subside swelling of legs and ankles [64]. Spice and herb: A. caudatus L. and A. hybridus L. leaves are used in culinary practices as leafy vegetables and in the form of a decoction to be therapeutically used as an astringent, anti-helminthic, and diuretic, and for treating scrofulous sores [65]. Functional or nutraceutical food: Amaranth leaves are used as functional or nutraceutical food against constipation, stomachache, as a diuretic, against worms, for convalescent persons, for quick growth of children and for tooth arising of babies, in Africa [66]. 3.2.2 Bangladesh Against sexually transmitted diseases: Roots of A. spinosus L. plant are used to treat gonorrhea by the Garo tribe and local traditional healers in Madhupur, Tangail district in Bangladesh [67]. 3.2.3 Ethiopia Skeleto-muscular diseases: A. dubius and A. graecizans L. leaves are used topically for healing chest bone fracture in children and backbone pain [68]. 3.2.4 Indonesia Anemia due to iron deficiency: According to study participants in Indonesia, A. tricolor can increase the value of Hb significantly in anemic patients with iron deficiency [69]. 3.2.5 Kenya Chronic joint pains: Ground seeds or dried leaf powder of A. albus L. is soaked in water for making an infusion and this is drunk as one glass 2–3 times daily, for 2 weeks or until recovery, for the management of chronic joint pains in Machakos and Makueni counties of Kenya [70]. 3.2.6 Malaysia Cough: Boiled roots of Amaranthus spp. are taken as a drink for the treatment of cough by Bajau community in Malaysia [71]. 3.2.7 Nepal Ethno-medicinal use: A. caudatus is used for stomach-ache and piles. A. lividus is used for liver disorders and anemia. A. spinosus is also used for liver disorders. A. tricolor is used as an antipyretic, for treating piles and for gastritis. A. viridis is used as a decoction in toothache and for piles [72]. Malla and his group [73] have also reported the use of A. caudatus L. root juice, about 4 teaspoons twice a day for

2

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61

3 days to cure fever and urinary problems. It is also used as a laxative for children and in diarrhea.

3.2.8 Pakistan Pulmonary congestion, flu, and cold: Ethnobotanical use of medicinal plants for respiratory disorders is prevalent among the inhabitants of Gallies – Abbottabad, Northern Pakistan. A decoction or paste of the whole plant of A. caudatus L. is used for pulmonary congestion A decoction or paste of the whole plant of A. caudatus L. is used for pulmonary congestion; similarly the paste, powder, or decoction of leaf, stem, roots as well as the whole plant of A. viridis L. is used for flu and cold [74]. Eye vision: Decoction of A. viridis L. leaves and roots (two cups of decoction at one time are given once per day for 2–3 days) is used for joint pain and backache due to its analgesic and anti-inflammatory activity. The plant is also used in the treatment of eye vision and against weakness [75]. 3.2.9 Philippines Traditional healers: Decoction of leaves of A. spinosus is used for cough and asthma in Laguna, the Philippines [76]. 3.2.10 Turkey Interviews with the local people living in Elazığ and villages of Turkey indicated that out of 62 traditional plants used for food purposes, A. retroflexus L. is utilized as a cooked vegetable dish whereas A. viridis L. is eaten fresh or leaves are cooked as vegetable or an egg-vegetable dish [77]. 3.2.11 Uganda Tuberculosis and related ailments: A. spinosus L. leaves are used for the treatment of tuberculosis and allied diseases by traditional medicine practitioners in Uganda [78]. Diarrheal infections: The leaf of A. spinosus L. is ground fresh, steeped in hot water, and drunk as one teaspoon three times daily for diarrheal infections, among the local communities of western Uganda [79]. 3.2.12 United Arab Emirates (UAE) Scorpion stings, snake bites, and itchy skin rash: A. graecizans L. and A. viridis L. leaves are crushed and applied on scorpion stings, snake bites, and itchy skin rash by traditional medicine practitioners in the United Arab Emirates [80].

4

Clinical Studies of Amaranthus Species

As discussed in Sect. 3, Amaranthus spp. are rich in flavonoids (rutin, quercetin, myricetin, anthocyanins, apigenin, kaempferol, catechins), phenolic acids (salicylic acid, vanillic acid, gallic acid, p-hydroxybenzoic acid, syringic acid, ellagic acid, sinapic acids, trans-cinnamic acid, caffeic acid, coumaric acid, ferulic acid), ascorbic

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acid, and tocopherols. These phytochemicals can combat oxidative stress and scavenge free radicals as they are excellent antioxidants. The plant is also a rich source of folic acid, Fe, Ca, Mg, Zn, Mn, and other micronutrients. It has been suggested that incorporation of amaranth as dietary supplement can help treat folic acid deficiency in pregnant women to curb spina bifida and heart defects in newborns, can aid in bone health due to the presence of good Ca content, and may aid in regulating blood glucose levels due to its high Mn levels [5]. This genre of research together with popularization of traditional medicine in the recent past has attracted attention of the scientific fraternity and led various groups to investigate its potential health benefits. Many preclinical studies have shown that Amaranthus seeds, leaves, stem, roots exhibit a wide range of pharmacological activities which have been reviewed by Peter and Gandhi [10]. However, there are limited clinical studies that have been conducted on its pharmacological properties. The use of bioparts of the Amaranthus plant, such as seeds, leaves, roots; directly or as formulations have been tested clinically for their therapeutic efficacy and are summarized in Table 2. It is evident from the studies cited in Table 2 that the actual benefit is accrued from a synergistic combination of different class of compounds in this vegetable and its regular consumption. The impetus sparking such research on bioactives are the clinical studies which suggest a benefit with the inclusion of this vegetable in diet to ward off various chronic ailments.

5

Fortified Food Products

The history of traditional consumption, health benefits, and gluten-free nature of amaranth seed have led many investigators to efficiently exploit it for fortification as functional food in products such as bread, cookies, cake, and pasta. Amaranth laddoo is a very popular delicacy in India especially during the fasting periods, as it is rich in antioxidants, dietary fiber, proteins, minerals, fatty acids, and various other bioactives discussed in the previous sections. Today, there is experimental evidence for the positive effect of consumption of amaranth laddoo made from popped seeds on hemoglobin and RBC count in young girls [99]. In the Western world, for example in Mexico, commercial production of the amaranth candy “alegria” and the drink “atole” dates back to the sixteenth century [100]. Similarly, the leaves of the plant are known to be utilized for preparing porridge in Africa. Amaranth leaves are a rich source of vitamin A and iron and thus helpful in prevention and treatment of anemia. A detailed account of the studies conducted in the last decade on Amaranthus spp. using its leaves or seed as functional food is listed in Table 3.

6

Cosmetic Applications

Other than its important functional food status, Amaranth has recently been documented to have a cosmetic value with an enormous commercial potential. Amaranthus spp. seed extracts were shown to possess potential skin-whitening

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Table 2 Studies establishing the biological activities of extracts due to bioactives present in Amaranthus Target Antioxidant

Physical form/ species Alkaloids from leaf powder of A. viridis

Seed oil of A. cruentus

Anemia and Vitamin A deficiency

Herbal formula containing A. tricolor

Sun-dried Amaranthus leaf formulation

Cardiovascular protective

Amaranth extract

Amaranth powder containing bioactive peptides

Particulars of study/dosage The alkaloids prevented the decline of antioxidant status which in turn decreases LPO levels by preventing MDA formation in erythrocytes. The results confirm the protective effect of alkaloids against free radical induced oxidative damage in human erythrocytes Amaranth oil (20 ml/d) supplementation in 19 obese patients together with calorie restriction for 3 weeks presented immunostimulating effects on oxidative burst activity in neutrophils Consumption for 4 weeks improved hemoglobin, mean corpuscular volume, serum iron, total iron binding capacity, and quality of life of 64 iron deficient anemic patients Intervention among preschool children significantly improved serum beta-carotene, retinol, and hemoglobin levels reflecting its utility in fighting vitamin A deficiency and anemia, among children and lactating mothers Administration of 2 g single dose amaranth extract in 16 healthy individuals increased the NO3ˉ and NO2ˉ level in plasma and saliva compared to placebo. This rise is expected to help in increasing the overall performance of people involved in vigorous physical activities. Since deficiency of NO is one of the prime reasons for endothelial dysfunction it may also be beneficial for the cardiovascular disease patients and aged individuals Consumption of 20 g amaranth for 3 months improved blood pressure in DM patients with hypertension as comorbidity. The cardiovascular risk biomarker plasminogen activator inhibitor 1 also decreased

References [81]

[82]

[69]

[83]

[84]

[85]

(continued)

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Table 2 (continued) Target

Physical form/ species A. cruentus oil

Gastroprotective

Amaranth oil

A. cruenthus seed oil

Antidiabetic

Amaranth containing bioactive peptides for three months.

A. hybridus

Antiobesity

Amaranth seed oil

Women health

Leaf extract of A. spinosus

Particulars of study/dosage Supplementation with 1 ml of concentrated oil in DM* patients and athletes for 28 days caused mild prooxidant activity resulting in improved uptake of oxidative destruction products and modulation of catalase and SOD activity with subsequent development of an antioxidant effect with increased production of endogenous oxygen and enhancement of the cardiorespiratory function 1 ml of concentrated amaranth seed oil as substrate on human fecal microbiota displayed increase of selected groups present in the intestinal microbiota, presenting prebiotic potential improving gastrointestinal health Supplementation of amaranth oil in addition to standard antiHelicobacter pylori treatment significantly reduced accumulation of lipid peroxidation product 4-hydroxynonenal-histidine adducts in gastric mucosa and increased heart rate variability in 36 duodenal peptic ulcer patients Consumption of 20 g in patients with diabetes melitus-2 and obesity daily resulted in reduction of BMI, leptin, resistin, and visfatin (serum markers related with obesity) It is rich in dietary fiber (3.6 g/100 g) and its consumption could be beneficial for the diabetics Supplementation of 20 ml/d of amaranth oil in 81 obese participants for 3 weeks resulted in significant reduction in the weight, BMI, waist, and hip circumference with improved insulin levels and HDL% Administration of 14 mg/day extract showed significant effect in increasing the prolactin levels and breast milk production in 15 postpartum mothers

References [86]

[87]

[88]

[85]

[89]

[90]

[91]

(continued)

2

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65

Table 2 (continued) Target

Physical form/ species Leaf extract of A. tricolor

Leaf extract of A. tricolor

Anticancer

Ethanolic extract of seeds of A. cruentus, A. hypochondriacus, A. caudatus, A. pumilus

Antimicrobial

Dry leaf methanolic extracts of A. tricolor A. viridis A. caudatus Ethanolic extract of flower of A. deflexus Ethanolic extract of root of A. hybridus Methalonic extract of leaves and stem of A. retroflexus Seed of A. cruentus

Particulars of study/dosage Supplementing 15 postpartum mothers with 1400 mg/day extract thrice for 14 days improved hemoglobin and erythrocyte count Biochemical analysis of 90 postmenopausal women supplemented daily with 9 g powder for a period of 3 months revealed significant increase in serum retinol, serum ascorbic acid, hemoglobin, GST, SOD while decrease in MDA, fasting blood glucose, and MRS (Menopause Rating Scale) score indicating antioxidant and therapeutic potential for postmenopause complications The extracts were shown to possess hemagglutination activity due to the presence of high lectin in seeds. Lectins have been reported to possess remarkable antitumor and growth inhibitory activity, exerting apoptotic role by preferential binding to cancer cell membranes with subsequent cytotoxicity The extracts possess antibacterial and antifungal properties against commercial bacterial and fungal strains The extracts possess antifungal activity against five fungal stains

References [92]

Daily consumption of 100 g amaranth grain porridge significantly increased CD4 count and decreased illness from baseline in Human Immunodeficiency Virus patients not on antiretroviral therapy

[98]

[93, 94]

[95]

[96]

[97]

properties as they inhibited melanin synthesis in vitro even better than the standard arbutin due to the presence of myoinositol and squalene [116]. Collagen biosynthesis is known to be inhibited by UVA (ultraviolet A) the in skin fibroblasts, but oil from

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Table 3 Health benefits of value added products from Amaranthus species Fortified food Product constituents and preparation Preparations from seeds Bread Partial substitution of amaranth flour with wheat flour significantly raised bread’s nutritional value by increasing protein content, dietary fiber, micro- and macro-minerals without changing product quality Incorporating of whole amaranth flour in the form of cheese bread formulation resulted in a product with higher dietary fiber and iron and similar acceptance as that of the control preparation Cakes and Incorporation of amaranth flour in the conventional sponge cake muffins formulation improved its nutritional value Partial replacement of wheat flour with amaranth flour enhanced antioxidative activity, mono- and polyunsaturated fatty acids, fiber content, nutritional, and sensory properties effectively inhibiting hydroperoxide decomposition, thus preventing generation of toxic secondary lipid oxidation products compared to control muffins Pasta Substitution of whole wheat flour partly with amaranth flour improved nutritional and functional properties with acceptable quality Cookies and Gluten-free germinated amaranth cookies exhibited highest biscuits antioxidant activity, total dietary fiber and protein content as compared to raw amaranth and wheat flour cookies Amaranth oat sugar cookies developed using gluten free amaranth flour containing essential amino acids and minerals improved their nutritional and physical quality Fortified cookies formulated using the amaranth grains (A. hypochondriacus L.), oats and refined wheat flour were observed to be a rich source of natural antioxidants, minerals, protein, carbohydrates, and dietary fiber and hence a potential source of energy Biscuits with best suited nutritional and sensory attributes were formulated using A. paniculatus commonly known as Rajgira, an important food in Indian fasting rituals owing to its health benefits Soup Amaranth-based vegetable soups contributed 25% of the adolescent RDA requirements for carbohydrate, protein, dietary fiber, vitamin A, and iron, thus improving the nutritional status Sprouts Amaranth sprouts are a nutritive food with antioxidant capacity, dietary fiber, and proteins. Thus having health promoting properties Laddoo Amaranth seed powder incorporation in laddoo improved hemoglobin and RBC count among young girls Sports Amaranth-based beverage enhanced the cycling performance beverage compared to participants consuming commercial sports beverage Preparation from leaves Maize snack Amaranth leaf powder improved the phenolic content, antioxidant properties, and pro-vitamin A content of extruded pro-vitamin A biofortified maize snacks

References [101, 102]

[103]

[104] [105]

[106]

[107]

[108]

[109]

[110]

[111]

[112]

[99] [113]

[114]

(continued)

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Table 3 (continued) Fortified food Product constituents and preparation Preparation from leaves and seeds Pasta Dried amaranth leaves and seed flour as ingredients for pasta production decreased cooking time, increased cooking loss percentage, decreased luminosity values, demonstrated highest protein, and crude fiber content compared with semolina as control pasta. The addition of its leaves resulted in higher contents of iron, zinc, magnesium, potassium, and antioxidant capacity compared with the control

References [115]

A. cruentus seeds was shown to provide pre- and post-UVA protection in skin fibroblasts and thus can be used in cosmetic formulations of anti-aging creams and as a natural sun protection factor (SPF) component [117]. In another study, Amaranth oil-based hydrogel nano-delivery system (nanostructured lipid carriers) resulted in sustained release of the natural antioxidant hesperidin and entrapped UVA and UVB filters (diethylamino-hydroxybenzoyl hexyl benzoate, 2-ethylhexyl salicylate) which assured absorption of 99% UVB radiations (SPF ¼ 46/50.5) and had an ability to combat 83% of UVA radiation in the formulation. Due to entrapment with Amaranth oil, the amount of UV filters used in the formulation was extremely reduced in comparison to the measure that is existent in commercial creams. The resulting superior photo-protection and enhanced antioxidant properties in the sunscreen formulation are expected to reduce the incidence of skin cancer on regular use and delay the process of photoaging [118]. Another cosmetic product, an herbal lipstick formulation was developed using aqueous extract of A. cruentus L. which showed good results as per the evaluated parameters and was costeffective. This was done to promote the use of natural dyes and natural formulations and avoid the side effects associated with use of synthetic ones [119]. A. tricolor is also mentioned in literature to be used in beauty care for face spa in Bangladesh [120]. It has been suggested by Busa and Getalado [121] that the anthocyanin-rich A. gangeticus leaf extract can be used as a natural hair colorant and can be a good substitute for synthetic hair dyes which are toxic.

7

Toxicity Issues

7.1

Food Allergy

A single case of systemic allergic reaction from A. paniculatus has been reported. A 19 year old patient developed symptoms of vomitting and wheezing on consumption of chapati made from its gluten free flour. He demonstrated severe skin test positive reaction, a prior sensitization to pigweed had caused an anaphylactic reaction upon ingestion, thus making it the first case of anaphylactic reaction to amaranth in the United States [122].

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Livestock Poisoning

An outbreak of spontaneous poisoning by A. hybridus in cattle in southern Rio Grande do Sul Brazil was reported in 2013 [123]. Another outbreak of Amaranthus poisoning was reported in sheep grazing in the Wagga–Wagga area of New South Wales, Australia, where ingestion of fresh green or senescing Amaranthus foliage was associated with the poisoning incidents [124]. A. retroflexus L. has also been associated with acute renal failure and/or mortality in a number of livestock species in southern Australia. Qian and coworkers [125] reported the presence of a sphingolipid, sterols, flavonoids, and tryptophan in extracts of A. retroflexus, but suggested no association between these metabolites and toxicity or renal failure. Recently, Weston et al. [126], after a chemometric analysis of A. retroflexus in relation to toxicity proposed a modified peptide to be responsible for acute renal failure in grazing livestock.

8

Conclusion

Amaranth is a dual utility crop with both greens and seeds of commercial value. Irrespective of the enormous and varied phytochemical content, claims in traditional medicine, health benefits, potential in food and cosmetic industry, Amaranth remains underutilized. There is a need to popularize the use of this underutilize vegetable in the daily diet. With emerging research, the grain and leaves are being already developed as one of the ingredients or functional food to be incorporated with cereals in breads, cakes, pastas, cookies, but the horizon needs to be widened. Thus, the need of the hour is to explore amaranth bioactives in depth at clinical research level, leading to its efficient exploitation for commercialization in various sectors such as pharmaceuticals, natural health supplements, packaged food, and cosmetic industry. Acknowledgments The authors would like to thank all the researchers who have shared their work on the subject in the public domain. We have tried our best to cite all relevant data pertaining to the subject in the last decade; however, any overlook is purely unintentional and may please be excused.

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Bioactive Compounds of Fat-Hen (Chenopodium album L.) Amrita Poonia

Contents 1 2 3 4

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Traditional Importance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nutritional Composition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Bioactive Compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1 Phytoconstituents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2 Phenols and Lignins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3 Alkaloids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4 Glycosides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5 Saponins and Phytate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.6 Flavonoids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.7 Tannins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 Pharmacological Significance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1 Antioxidant Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2 Antimicrobial Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3 Spasmolytic Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4 Gastroprotective and Hepatoprotective Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.5 Anticancer Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 Future Prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Abstract

Chenopodium album L. (family Chenopodiaceae) is a widely distributed species commonly known as fat-hen, white goosefoot, pigweed, lamb’s quarters, and various other names in different regions of the world. It is rich in nutrients and can be used in various value-added food products. Medicinally, it is used to treat the A. Poonia (*) Department of Dairy Science and Food Technology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, India © Springer Nature Switzerland AG 2021 H. N. Murthy, K. Y. Paek (eds.), Bioactive Compounds in Underutilized Vegetables and Legumes, Reference Series in Phytochemistry, https://doi.org/10.1007/978-3-030-57415-4_6

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diseases of blood, spleen, heart, and eye and possess anticancer, antipruritic, and antinociceptive properties. The main phytoconstituents isolated from C. album includes phenols, alkaloids, glycosides, saponins, and flavonoids. Chenopodium album can be considered as a nutraceutical food due to its bioactive compounds and pharmacological activities. C. album is viewed as a potential vegetable and is worth in exploration and utilization. Keywords

Antioxidant · Bioactive compounds · Chenopodium · Pharmacology · Phytochemicals

1

Introduction

Chenopodium album L. (family: Chenopodiaceae) is an annual herb which is naturally distributed in Asia, Europe, North America, and Africa. It grows luxuriantly in cultivated fields and commonly known as fat-hen, white goosefoot, etc. In subtropical areas, it is most common in wheat, chickpea, barley, sunflower, soybean, and maize fields. Kokanova et al. [1] reported that Chenopodium genus consists of 120 species and 10 of which are distributed in Egypt. It is an important food crop and medicinal plant in many countries and is extensively used around the world. It is widely cultivated and consumed in North region of India as a food crop. This chapter highlights the traditional uses and pharmacological potential of Chenopodium album Linn.

2

Traditional Importance

C. album is used as vegetable in India and has high biological potential in addition to basic nutritional benefits. Young leaves were used as a salad for human consumption [28]. Tender branches and leaves of the plant are eaten raw as salad or mixed with other leafy vegetables for cooking in different regions of the world. Leaves are also used with curd as “Raita” (Raita is a condiment made out of yoghurt together with raw and cooked vegetables) in India. The dried leaves of C. album can also be added in many traditional food items for enhancing the nutritional profile of the enriched products and adds variety in the diet. The dried leaves are also stored for later use. They are also used for making Parathas and Chapati (a flatbread made out of wheat flour) in different parts of India. Leaves and seeds of C. album are seed in the preparation of herbal medicine. Leaves are rich in essential oils and contain enough quantity of albuminoids, minerals, mainly in potash salts and other compounds [30]. Luvaud [2] and Horio [4] isolated a phenolic amide and saponins from the roots of C. album, and sitosterol and oleanolic acid from flowers. The leaves are used for treatment of bug bites,

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sunstroke, rheumatic joints, and swollen feet. Leaves possessed anthelmintic, antiphlogistic, antirheumatic, and laxative properties. They are also used for arthritis and rheumatism by washing the joints and limbs with decoction. A warm poultice of the leaves is used to treat headache [29]. Gogoi and Zaman [5] reported that leaves can also be used in constipation. Leaves have ascaridole which is used for treating roundand hookworms. Plant is recommended for the treatment of splenic enlargement and hepatic disorders [30]. The juice of the stems was applied to freckles and sunburn. Seeds are chewed in the treatment of urinary problems and were considered useful for relieving the discharge of semen through the urine. The oil also contains traces of ascaridole. Seeds isolated cryptomeridiol which showed significant growth promoting activity [24]. The roots of C. album are used in hepatic diseases like jaundice, rheumatism, and for urinary diseases. Ahmad and Hussain [3] reported that the fruits and roots of the plant are recognized as an antitoxin to snake venom. The juice of the root was used in the treatment of bloody dysentery.

3

Nutritional Composition

C. album leaves are rich in carbohydrates (40.84%), protein (28.69%), and less amount of fat content (4.40%). C. album also contains potassium, sodium, calcium, magnesium, zinc, and iron in higher amounts [6]. Adedapo [7] reported that C. album leaves contains sodium (0.4), calcium (2.2), potassium (6.9), zinc (50), iron (255), magnesium (0.7), copper (13.0), and manganese (118.0) mg/100 g dry weight basis, respectively. Afolayan and Jimoh [8] detected vitamin C and β-carotene from the young shoots and mature plants and also revealed that these vegetables could constitute an important source of these vitamins in the diet [9]. Leaves and seeds are also good source of vitamin A and vitamin C. Physicochemical composition of C. album leaves and seeds is given in Table 1. C. album leaves contains 0.64% essential oil (v/w). Usman et al. [10] reported that the essential oil from leaves contains tricyclene, α-thujene, camphene, sabinene, myrecene, benzyl alcohol,1,8-cineole, cis-ocimene, γ-terpinene, neral, linalool, allo ocimene, citronellal, borneol, geranial, borneol acetate, thymol, carvacrol, acetyl eugenol, elemicin, benzyl benzoate, and citronella. Oil also contains p-cymene: 40.9%, α-pinene: 7.0%, β-pinene: 6.2% limonene: 4.2%, pinane-2-ol: 9.9%, ethyl cinnamate: 3.7%, a-terpineol: 6.2%, ascaridole: 15.5%, and linalyl acetate: 2.0% [11].

4

Bioactive Compounds

Different bioactive compounds found in C. album are phenolics, flavonoids, tannins, betalains, anthocyanins carotenoids, sterols, and glucosinolates.

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Table 1 Physicochemical composition of C. album Constituents Moisture Protein Fat Ash Total sugar Lipid content Sodium Potassium Magnesium Calcium Phosphorus Manganese Iron Vitamin A Vitamin C

Leaves 89.65% 3.70% 0.40% 2.07% 2.90% (other carbohydrates) ND 0.0004% (d.w.) 0.007% (d.w.) 0.118% (d.w.) 0.015% 0.008% 0.002% (d.w.) 0.004% ND ND

Seeds 11.30% 3.30% 3.0–6.20% 2.40% 3.70% 3.50–5.80% 0.018–0.026% 0.471–0.551% 0.135–0.176% 0.067–0.015% 0.463% 0.0008–0.0011% 0.0057% 0.0066% 0.0113%

References [6, 12] [11, 13] [14] [12, 15] [6] [11] [11] [7] [7] [6] [6, 12] [1] [7, 12] [12] [12]

ND not detected

4.1

Phytoconstituents

The main phytoconstituents isolated from various parts like leaves, roots, stems of the plant are nonpolar lipids, phenols, lignins, alkaloids flavonoids, glycosides, saponins, ascorbic acid, β-carotene, catechin, gallocatechin, caffeic acid, p-coumaric acid, ferulic acid, β-sitosterol, campesterol, xanthotoxin, stigmasterol, n-triacontanol, imperatorin, ecdysteroid, cryptomeridiol, ntransferuloyl-4O-methyl dopamine, β-sitosterol, lupeol, and 3 hydroxy nonadecyl henicosanoate [17] (Table 2). Leaf extract of C. album was found to contain 0.94% total phenolic contents (gallic acid equivalent) and 0.27% total flavonoid contents (catechin equivalent) [16]. Alkaloids in crude form are found in higher amount (9.7 g/100 g of dry matter) and less amount of saponins (0.46 g/100 g of dry matter). Pandey and Gupta [6] reported that total phenolic content was found in highest amount (57.0 μg/GAE/mg) in ethyl acetate extract of C. album as compare to other extraction solvents. The flavonoid contents are also high (42.74 μg/GAE/mg) in a mixture of solvents. Adedapo et al. [7] reported proanthocyanidins (4.51 mg quercetin equivalent/g), total flavonol (1.34 mg equivalent quercetin/g) in acetone extract. C. album was reported to have trypsin inhibitor activity (0.11–0.17 TIU/mg), simple phenols (72.50–101.007 mg GAE/100 g), total phenols (224.99–304.98 mg GAE/100 g), tannins (152.49– 203.91 mg GAE/100 g), flavonoids (220.0–406.67 mg/100 g), phytic acid (238.3–268.33 mg/100 g), phytate phosphorus (67.16–75.62 mg/100 g), saponin (0.043–0.867 g/100 g), alkaloids (1.27–1.53 mg/100 g), and oxalates (394.19– 477.08 mg/100 g) [7, 18].

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Table 2 Phytochemical composition of Chenopodium album leaves Phytoconstituents Pentoses and methylpentoses Amino acids Nonpolar constituents

Phenols and lignin

Sterols (pytosterols) Alkaloids Carotenoid terpenoids Glycosides Flavonoids

Saponins

Amides Vitamins

4.2

Compounds Ribosa

References [11]

Glutamic acid, alanine, asparagine, and lysine n-tetradecane, n-pentadecane, n-hexadecane, n-heptadecane, 2,6-dimethylheptadecane 2,6,10,14-tetramethylheptadecane, n-octadecane, 2-methyloctadecane, palmitic acid, methyl palmitate, ethyl palmitate, stearic acid, methyl stearate, linoleic acid, methyl linoleate, methyl linolenate, oleic acid, n-eicosane, n-heneicosane, 9Z,12Z-octadecadien1-ol, n-octacosane, n-octacosanal, octacosanyl acetate, n-nonacosane, n-pentatriacontane, n-tetracontane, n-hexadecanal, n-octadecanal, n-tritetracontane 20 Cinnamic acid, 4-hydroxy-cinnamic acid, ferulic acid, methyl ferulate, sinapic acid, methyl 3-(4-hydroxy-3methoxyphenyl)propanoate, 4-(1-hydroxyethyl)-2methoxyphenol, vanillyl alcohol, 4-(hydroxymethyl)-2methoxyphenol, 4-hydroxy-3-methoxybenzoic acid, 4-vinylphenol, 4-methylbenzaldehyde, N-[2-(1H-indol-3-yl) ethyl]acetamide, pinoresinol, syringaresinol, lariciresinol, 5,50 -dimethoxy-lariciresinol, threo-guaiacylglycerol-β-O-4syringaresinol ether Sitosterol, sitostanol, campesterol, stigmasterol, spinasterol Cholesterol Chenoalbicin, a novel cinnamic acid S-(+)-abscisic alcohol, blumenol A (+)-dehydrovomifoliol grasshopper ketone and racemic allenic ketones Oleanolic acid as glycon and glucose and glucuronic acid Kaempferol-3-O-(4-β-D-xylopyranosyl)-α-Lrhamnopyranoside-7-O-α-Lrhamno pyranoside, 3-O-(4-β-Dapiofuranosyl)-α-L-rhamnopyranoside-7-O-α-Lrhamnopyranoside, 3,7-di-O-α-L-rhamnopyranoside, 3-Oglucopyranoside, quercetin 3,7-di-O-β-D-glucopyranoside, 3-O-glucosylglucuronide, 3-O-α-L-rhamnopyranosyl(1 ! 6)-β-D-glucopyranoside, 3-O-β-D-glucopyranoside Calenduloside E, chikusetsusaponin IVa and 3-O-(39-O(20-O-Glycolyl)-glyoxylyl-b-D-glucuronopyranosyl) oleanolic acid Choline, novel cinnamic acid amide alkaloid, chenoalbicine Vitamin A, folic acid, thiamine, and niacin

[11] [11, 13]

[19]

[20] [21] [22] [22] [23]

[24]

[25] [26]

Phenols and Lignins

Francesca et al. [19] reported that C. album contain phenols and lignins, i.e., cinnamic acid, 4-hydroxy-cinnamic acid, ferulic acid, sinapic acid, methyl 3-(4-hydroxy-3methoxyphenyl) propanoate, methyl ferulate, 4-(1-hydroxyethyl)-2-methoxyphenol, 4-(hydroxymethyl)-2-methoxyphenol, vanillyl alcohol, 4-methylbenzaldehyde, N-[2(1H-indol-3-yl)ethyl]acetamide, pinoresinol, syringaresinol, lariciresinol, 4-hydroxy-

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3-methoxybenzoic acid, 4-vinylphenol, 5,50 -dimethoxy-lariciresinol, and threoguaiacylglycerol-β-O-4-syringaresinol ether. They also reported two new sesquilignans, i.e., threo-guaiacylglycerol-α-O-methyl-β-O-4-syringaresinol ether and threo-syringylglycerol-α-O-methyl-β-O-4-syringaresinol ether on the basis of spectroscopic data, including two-dimensional NMR analysis.

4.3

Alkaloids

Alkaloids were found in higher amount (9.7 g/100 g of dry matter) in C. album. Chenoalbicin, a novel cinnamic acid amide alkaloid from C. album, was characterized by extensive spectroscopic investigation, especially one-dimensional and two-dimensional NMR spectroscopy. Adedapo et al. [7] reported that C. album contains 1.8 mg/100 g d.w. of alkaloid and lower than the values reported for the leafy vegetables like Aspilia africana, Bryophyllum pinnatum, Cleome rutidosperma, and Emilia coccinea.

4.4

Glycosides

C. album seeds were reported to contain oleanolic acid as glycon, glucose, and glucuronic acid as monosaccharide which has the sperm-immobilizing effects. Nahar and Sarker [27] isolated a new phenolic glycoside named chenoalbuside from C. album and was assessed by the DPPH assay. They also reported its RC50 value as 1.4  104 mg/ml.

4.5

Saponins and Phytate

The roots of C. album contain saponins. Saponins have hypocholesterolemic, anticarcinogenic, antioxidant, and immunostimulant properties. Seven cinnamic acid amides have been isolated from the plant. Three saponins from the roots of C. album namely calenduloside E, chikusetsusaponin, and 3-O-(39-O-(20-OGlycolyl)-glyoxylyl b-D-glucuronopyranosyl) oleanolic acid were reported [24]. Adedapo et al. [7] reported that C. album contains 5.3 mg/100 g d.w. saponins and phytate 18.1 mg/100 g d.w. Pachauri et al. [12] also reported that C. album contains 0.27% saponins and 7.4 mg/g of phytic acid.

4.6

Flavonoids

Mainly two flavonoids are found in C. album, i.e., kaempferol and quercetin. They can be considered more into flavanols, isoflavones, flavanones, flavones, flavanonols, and flavans (catechins and proanthocyanidins) and anthocyanidins [28]. Pachauri et al. [12] reported that C. album contains 84 mg/100 g flavonoids

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on dry weight basis. Flavonoid concentration in C. album was 83 mg/100 g, which have health promoting properties. Polyphenolic and flavonoid content of different C. album aerial parts extracts were in the range of 14.56  0.21–42.00  0.2 mg (gallic acid equivalent/g extract) and 2.20  0.003–7.33  0.5 mg (rutin equivalent/ g extract), respectively [13]. Eight flavonoid compounds were isolated from C. album L. namely kaempferol-3-O-(4-β-D-xylopyranosyl)-α-L-rhamnopyranoside7-O-α-Lrhamno pyranoside, 3-O-(4-β-D-apiofuranosyl)-α-L-rhamnopyranoside7-O-α-L-rhamnopyranoside, 3,7-di-O-α-L-rhamnopyranoside, 3-O-glucopyranoside, quercetin 3,7-di-O-β-D-glucopyranoside, 3-O-glucosylglucuronide, 3-O-α-L-rhamnopyranosyl-(1 ! 6)-β-D-glucopyranoside, and 3-O-β-D-glucopyranoside [23].

4.7

Tannins

C. album contains 119 mg/100 g tannins on dry weight basis [12]. Tannin levels may vary due to the variety and growing conditions of the plant.

5

Pharmacological Significance

Recently, much attention has been paid to naturally occurring antioxidants, which may show an important role in inhibiting both free radicals and oxidative chain reactions within tissues and membranes. Polyphenols are important components of C. album and some of their pharmacological effects could be attributed to the presence of these valuable constituents. They seem to have additive effects on endogenous scavenging compounds [29]. Pharmacological effects of C. album are presented in Fig. 1.

5.1

Antioxidant Activity

Nahar and Sarker [27] isolated a new phenolic glycoside, i.e., chenoalbuside from C. album and assessed by the DPPH assay, and the RC50 value was found to be 1.4  104 mg/ml. The antioxidant activity (expressed as percent inhibition relative to control, using β-carotene bleaching method) of aqueous and ethanolic extracts of C. album were 64.5% and 60.5%, respectively [30].

5.2

Antimicrobial Activity

The aqueous leaf extracts showed strongest antibacterial activity against Staphylococcus aureus, Salmonella typhimurium, Pseudomonas aeruginosa, and Salmonella typhimurium [31, 33]. Similarly, Pandey and Gupta [6] demonstrated the antimicrobial activity of methanolic extract of C. album against Staphylococcus aureus, Staphylococcus epidermidis, Bacillus subtilis, Escherichia coli, and Proteus

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Antioxidant Activity

Antimicrobial Activity

Hepatoprotecti ve activity

Pharmacological activities Aninflammatory Acvity

Gastroprotecti ve Activity

Anti cancer Activity

Spasmolytic Activity

Fig. 1 Pharmacological effects of C. album

mirabilis. Methanolic extract of C. album inflorescence showed highest antifungal activity against fungal strains [32].

5.3

Spasmolytic Activity

Ethanolic extract of C. album and subsequent ethyl acetate, chloroform, n-butanol, and water fractions showed a dose-dependent increase in relaxation of smooth muscles, starting from 5 mg/ml. The maximum effect was found at 20 mg/ml (92.86%). All the fractions were experimented on rabbit’s intestine at 15 mg/ml dose. The ethyl acetate and chloroform fractions of C. album exhibited relaxation of the intestinal muscles (43.48% and 51.52%, respectively), whereas, n-butanol fraction of C. album produced strong relaxant effect (91.18%) [34].

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Bioactive Compounds of Fat-Hen (Chenopodium album L.)

5.4

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Gastroprotective and Hepatoprotective Activity

Nigam and Paarakh [35] studied the effect of alcoholic extract of C. album to evaluate the antiulcer activity in rats and reported that alcoholic extract significantly decreases the volume of gastric acid secretion, free acidity, and total acidity. A dose of 450 mg/kg of extract of C. album showed inhibition of high biochemical parameters related with induction of hepatotoxicity by CCl4. Baldi and Choudhary [36] studied the activities of dried whole plant of C. album in acetone and methanol extracts in ratio of (50:50) against paracetamol-induced hepatic injury. They reported that acetone and methanol extract treatment of experimental animals at a dose of 400 mg/kg showed significant (P < 0.001) hepatoprotective activity and their effect was similar to the standard drug, silymarin.

5.5

Anticancer Activity

Solvent extracts from C. album leaves namely petroleum ether, ethyl acetate, and methanol were assessed for their cytotoxicity using Trypan blue exclusion and MTT [3-(4,5-dimethyl thiazol-2-yl)-2,5-diphenyl tetrazolium] bioassay. It was found that methanolic extract showed maximum cancer activity having IC50 value of 27.31 mg/ ml against MCF-7 cell line. Substantial percent inhibition (94.06%) was observed for MeOH extract of C. album at 48 h of exposure and concentration 100 mg/ml (P < 0.05) against MCF-7 breast cancer cell line [37].

6

Conclusions

C. album was reported to possess essential nutrients such as carbohydrates, protein, and mineral elements. This plant contains a number of important chemical constituents like saponins, flavonoids, and phenolic compounds. Varied biological activities such as antibacterial, anticancer, antiulcer, anti-inflammatory, antioxidant, anthelmintic, hepatoprotective, spasmolytic and analgesic, antipruritic, and antinociceptive are attributed due to this plant. Due to economical and enormously rich in nutrients, C. album can be a substitute to overcome the various deficiency diseases occurs due to micronutrients among the susceptible groups of society. This plant may be explored as an important functional food by keeping in view the traditional uses, pharmacological activities, and bioactive compounds.

7

Future Prospects

The nutritional properties and presence of variety of active phytochemical constituents of C. album make it more interesting nutraceutical food in future. There is a great scope for further research in the area of pharmacological research on C. album. Due to its great potential as dietary therapeutic agents, more research is required in

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this area. The bioactive compounds can be isolated from C. album for further evaluation and development of drugs from these bioactive compounds. Being economical and rich source of nutrients, C. album may play an important role as an alternate to control the macro- and micronutrient deficiencies among the society.

References 1. Kokanova-Nedialkova Z, Nedialkov P, Nikolov S (2009) The genus Chenopodium: phytochemistry, ethnopharmacology and pharmacology. Pharmacogn Rev 3:280–306 2. Lavaud C, Voutquenne L, Bal P, Pouny I (2000) Saponins from Chenopodium album. Fitoterapia 71:338–340 3. Nadkarni KM (1982) Indian material medica, 3rd edn. Popular Prakashan Pvt Ltd, Bombay 4. Horio T, Yoshida K, Kikuchi H, Kawabata J, Mizutani J (1993) A phenolic amide from roots of Chenopodium album. Phytochemistry 33:807–808 5. Gogoi B, Zaman K (2013) Phytochemical constituents of some medicinal plant species used in recipe during “Bohag Bihu” in Assam. J Pharmacogn Phytochem 2:30–40 6. Pandey S, Gupta R (2014) Screening of nutritional, phytochemical, antioxidant, antibacterial activity of Chenopodium album. J Pharmacogn Phytochem 3:1–9 7. Adedapo A, Jimoh F, Afolayan A (2011) Comparison of the nutritive value and biological activities of the acetone, methanol and water extracts of the leaves of Biden spilosa and Chenopodium album. Acta Pol Pharm Drug Res 68:83–92 8. Afolayan J, Jimoh FO (2009) Nutritional quality of some wild leafy vegetables in South Africa. Int J Food Sci Nutr 60:424–431 9. Gqaza BM, Njume C, Goduka NI, George G (2013) Nutritional assessment of Chenopodium album L. (Imbikicane) young shoots and mature plant-leaves consumed in the Eastern Cape Province of South Africa. Int Proc Chem Biol Environ Eng 53:97–102 10. Usman LA, Hamid AA, Muhammad NO, Olawore NO, Edewor TI, Saliu BK (2010) Chemical constituents and anti-inflammatory activity of leaf essential oil of Nigerian grown Chenopodium album L. EXCLI J 9:181–186 11. Dahot MU, Soomro ZH (1997) Proximate composition, mineral and vitamin content of Chenopodium album. Sci Int 9:405–407 12. Pachauri T, Lakhani A, Kumari KM (2017) Nutritional and antinutritional characterization of Chenopodium album seeds: a neglected wild species. Int J Nutr Agric Res 4:9–21 13. Leicach SR, Yaber Grass MA, Gorbino GB, Pomilio AB, Vitale AA (2003) Nonpolar lipid composition of Chenopodium album grown in continuously cultivated and nondisturbed soils. Lipids 38:567–572 14. Prakash D, Nath P, Pal M (1993) Composition, variation of nutritional contents in leaves, seed protein, fat and fatty acid profile of Chenopodium species. J Sci Food Agric 62:203–205 15. Singh L, Yadav N, Kumar AR, Gupta AK, Chacko J, Parvin K, Tripathi U (2007) Preparation of value added products from dehydrated bathua leaves (Chenopodium album Linn.). Nat Prod Radiance 6:6–10 16. Choudhary SP, Sharma DK (2014) Bioactive constituents, phytochemical and pharmacological properties of Chenopodium album: a miracle weed. Int J Pharmacogn 1:545–552 17. Esmai A, Snafi AI (2015) The chemical constituents and pharmacological effects of Chenopodium album – an overview. Int J Pharmacol Screen Methods 5:10–17 18. Sood P, Modgil R, Sood M, Chuhan PK (2012) Anti-nutrient profile of different Chenopodium cultivars leaves. Annals Food Sci Technol 13:68–74 19. Francesca C, Marina D, Melania G, Lucio P, Armando Z (2006) Phenols and lignin’s from Chenopodium album. Phytochem Anal 17:344–349 20. Salt TA, Adler JH (1985) Diversity of sterols composition in the family Chenopodiaceae. Lipids 20:594–601

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21. Brigida DA, Marina DG, Armando Z (2004) Chenoalbicin, a novel cinnamic acid amide alkaloid from Chenopodium album. Chem Biodivers 1:1579–1583 22. Dembitsky V, Shkrob I, Hanus LO (2008) Ascaridole and related peroxides from the genus Chenopodium. Czech Repub 152:209–215 23. Ibrahim LF, Kawashty SA, Ayman RB, Shabana MM (2007) A comparative study of the flavonoids and some biological activities of two Chenopodium species. Chem Nat Compd 43:24–28 24. Catherine LU, Laurence V, Philippe B, Isabelle P (2000) Saponins from Chenopodium album. Fitoterapia 71:338–340 25. Cutillo F, Abrosca BD, DellaGreca M, Di Marino C, Golino A, Previtera L, Zarrelli A (2003) Cinnamic acid amides from Chenopodium album: effects on seeds germination and plant growth. Phytochemistry 64:1381–1387 26. Aliotta G, Pollio A (1981) Vitamin A and C contents in some edible wild plants in Italy. Riv Ital EPPOS 63:47–48 27. Nahar L, Sarker SD (2005) Chenoalbuside: an antioxidant phenolic glycoside from the seeds of Chenopodium album L. (Chenopodiaceae). Braz J Pharmacogn 15:279–282 28. Ververidis F, Trantas E, Douglas C, Vollmer G, Kretzschmar G (2007) Biotechnology of flavonoids and other phenylpropanoid-derived natural products. Part II: Reconstruction of multienzyme pathways in plants and microbes. Biotechnol J 2:1235–1249 29. Poonia A, Upadhayay A (2015) Chenopodium album Linn: review of nutritive value and biological properties. J Food Sci Technol 52:3977–3985 30. Kaur C, Kapoor HC (2002) Anti-oxidant activity and total phenolic content of some Asian vegetables. Int J Food Sci Technol 37:153–161 31. Singh KP, Dwevedi AK, Dhakre G (2011) Evaluation of antibacterial activities of Chenopodium album. Int J Appl Biol Pharm Technol 2:398–401 32. Javid A, Muhammad A (2009) Antifungal activity of methanol and n-hexane extracts of three Chenopodium species against Macrophomina phaseolina. Nat Prod Res 23:1120–1127 33. Elif Korcan S, Aksoy O, Erdoğmuş SF, Ciğerci İH, Konuk M (2013) Evaluation of antibacterial, antioxidant and DNA protective capacity of Chenopodium album’s ethanolic leaf extract. Chemosphere 90:374–379 34. Ahmad M, Mohiuddin OA, Mehjabeen, Jahan N, Anwar M, Habib S, Alam SM, Baig IA (2012) Evaluation of spasmolytic and analgesic activity of ethanolic extract of C. album Linn and its fractions. J Med Plant Res 6:4691–4697 35. Nigam V, Paarakh PM (2011) Anti-ulcer effect of Chenopodium album Linn. against gastric ulcers in rats. Int J Pharm Sci Drug Res 3:319–322 36. Baldi A, Choudhary NK (2013) In vitro antioxidant and hepatoprotective potential of Chenopodium album extract. Int J Green Pharm 7:50–56 37. Khoobchandani M, Ojeswi BK, Sharma B, Srivastava MM (2009) Chenopodium album prevents progression of cell growth and enhances cell toxicity in human breast cancer cell lines. Oxidative Med Cell Longev 2:160–165

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Bioactive Compounds of Paracress [Acmella oleracea (L.) R.K. Jansen] Moacir Couto Andrade Jr

Contents 1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 Major Bioactive Compounds of Paracress and Their Properties . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1 Alkaloids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Phenolic Compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3 Phytosterols . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4 Saponins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.5 Spilanthol . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.6 Terpenes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 Other Pharmacological Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 Nutritional Features of Paracress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 Toxicological Traits in Zebrafish . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Abstract

Acmella oleracea (L.) R.K. Jansen is an Amazonian leafy vegetable (Peru) popularly known as jambu (in Portuguese and Spanish) and paracress (in English), with great nutritional and bioactive potential. This herbaceous plant is particularly rich in spilanthol, a versatile bioactive compound that is further discussed in this text. However, plants such as paracress are complex organisms with different phytochemical composition according to the investigated organ (e. g., flowers, leaves, stems). The present work attempts to sum up the nutritional, pharmacological, and toxicological aspects of the bioactive compounds of this promising medicinal plant. M. C. Andrade Jr (*) Post-Graduation Department, Nilton Lins University, Manaus, Brazil Post-Graduation Department, School of Public Health (Escola de Saúde Pública – ESAP), Manaus, Brazil © Springer Nature Switzerland AG 2021 H. N. Murthy, K. Y. Paek (eds.), Bioactive Compounds in Underutilized Vegetables and Legumes, Reference Series in Phytochemistry, https://doi.org/10.1007/978-3-030-57415-4_2

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Keywords

Alkaloids · Flavonoids · Phytosterols · Saponins · Spilanthol · Tannins · Terpenes

1

Introduction

Acmella oleracea (L.) R.K. Jansen is an annual herbaceous plant native to the Amazonian region (Peru) belonging to the Asteraceae family [1–3]. In English, it is called paracress [4]. In both Portuguese and Spanish, it is mostly known as jambu [4]. It is now widely distributed throughout tropical and subtropical regions of the world, including Africa, South America, Borneo, India, Sri Lanka, and Southeast Asia [2, 5, 6]. This plant is almost entirely edible, and its inflorescences, leaves, as well as stems, are part of delicious traditional dishes of the Brazilian cuisine (e.g., tacacá, pato no tucupi) [4, 7]. Tacacá (Fig. 1), especially, is a famous, composite, Brazilian delicacy, made of tucupi (a fermented sauce of cassava – Manihot esculenta Crantz), cassava gum, paracress stems and leaves (and other herbs), and shrimps [3, 7, 8]. Paracress leaves, in particular, have an appreciated numbing effect on the tongue and the mouth because of their flavor often compared to that of pepper [3, 4]. This unique organoleptic property is due to an olefinic alkylamide named spilanthol, further discussed in this text [2]. Additionally, this plant extract has been an important commercial product in oral health care, and for this reason, it has been attributed a common name, i.e., the toothache plant [2, 3, 6]. Thus, Acmella oleracea (L.) R.K. Jansen is also known for its health-promoting properties, thereby drawing the attention of researchers worldwide. These properties cover such a wide range of potential health benefits to the point that paracress is used as a panacea in certain countries (e.g., Sumatra, in Indonesia) [6]. Hence, the present

Fig. 1 The tacacá dish

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work attempts to summarize the nutritional, pharmacological, and toxicological traits of the bioactive compounds of this promising medicinal plant.

2

Major Bioactive Compounds of Paracress and Their Properties

2.1

Alkaloids

The occurrence of alkaloids in Acmella oleracea (L.) R.K. Jansen was confirmed by Mayer’s test, Dragendorff’s test, Wagner’s test, and Hager’s test in a recent study [9]. However, these data are still incipient and must be further developed. What’s more, alkaloids were not detected by these very same tests in two older studies [2, 5]. Maybe these discrepancies explain in part why the species Acmella oleracea (L.) R. K. Jansen was not listed among those related to alkaloid production and belonging to the Asteraceae family in a very recent review work [10].

2.2

Phenolic Compounds

Phenolic compounds are secondary metabolites usually involved in plant adaptation to environmental stress conditions (e.g., ultraviolet radiation, pathogenic attack) that have evolutionary importance [7]. Flavonoids constitute the most important single group of phenolic compounds and tannins belong to the flavonoid class [7, 11]. The potent antioxidant activity in the crude ethanol extract of paracress leaves was attributed to the presence of phenolic compounds, flavonoids, and tannins [6]. Additionally, the antipyretic activity of paracress is attributed to the presence of flavonoids, which are predominant inhibitors of either cyclooxygenase or lipoxygenase (i.e., both enzymes are involved in the proinflammatory response and regulation of inflammation and, therefore, represent interesting drug targets) [6, 12]. Besides, flavonoids also exert an analgesic activity as potent inhibitors of prostaglandins at later stages of acute inflammation [6]. It is important to know that paracress leaves are richer in total phenolics (mg Gallic Acid Equivalent (GAE) g 1 Dry Weight (DW), i.e., 3.19 mg GAE g 1 DW) and in total flavonoids (mg Rutin Equivalent (RE) g 1 DW, i.e., 11.45 mg RE g 1 DW) than paracress flowers (1.98 mg GAE g 1 DW and 5.91 mg RE g 1 DW, respectively) than yet paracress stems (1.37 mg GAE g 1 DW and 3.80 mg RE g 1 DW, respectively) [13]. This preferential distribution of phenolic compounds was observed in paracress cultivated in both conventional and hydroponic systems [13]. In a recent study, tannin was found to be present in paracress in one of the tests, i.e., lead acetate test, but not in FeCl3 and K2Cr3O7 tests [9]. In contrast, tannin was detected by these same two last tests in two older studies, showing perhaps methodological inconsistencies [2, 5]. Nevertheless, it is worth noting that tannins from different plants are shown to have antitumor, antibacterial, and antiviral activities, among other beneficial effects

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on human health, justifying every effort to discover new natural sources of these compounds [2]. Vanillic acid is also a phenolic compound found in whole Acmella oleracea plant [3].

2.3

Phytosterols

Phytosterols, i.e., the sterol fraction in vegetable oils, are poorly absorbed (e.g., 90% of β-sitosterol consumed is recovered in the stool), and can block the intestinal absorption of endogenous and exogenous cholesterol on a 1:1 basis [14, 15]. This inhibitory action improves cholesterol profile in the blood, lowering total and low-density lipoprotein (LDL) cholesterol, and decreasing the risks of cardiovascular diseases [16, 17]. Phytosterols are, therefore, important functional ingredients for human health. Other phytosterols found in paracress are β-sitostenone (an oxidized product of β-sitosterol; both saturated fatty acids sharing a very similar chemical structure), stigmasterol, α-amyrin, and β-amyrin [3, 18]. However, β-sitosterol stands out in paracress with the highest contents, followed by stigmasterol and campesterol [16]. Of interest, the nutritional composition of the raw paracress differs from that of the processed paracress. Subsequently, the total phytosterol levels are 18.89 mg 100 g 1 and 20.56 mg 100 g 1 for the raw and processed paracress, respectively, although not significantly different [16]. These levels are higher than those found in popular fruits such as bananas (16 mg 100 g 1), apples (12 mg 100 g 1), and tomatoes (7 mg 100 g 1) [15].

2.4

Saponins

Saponins may be defined as glycosides of both triterpenes and steroids, and because of their antioxidant and antimicrobial activities, they are valuable in wound contraction and epithelialization at an eminent rate [19]. However, there were also divergences regarding the phytochemical detection of saponins in paracress studies that use the foam test. That is, these glycosides were present in one recent study [9] but absent in two older studies [2, 5].

2.5

Spilanthol

The interest for this outstanding representative molecule of the N-alkylamides has increased in the last two decades, not only for its action in the protection of plants and biocid products, functional foods, cosmetics, and pharmaceutical components, but also for its great variety of beneficial biomedical activities [20]. Besides spilanthol, whose chemical structure and some of its bioactivities are schematically presented in Fig. 2, paracress has also a minor medicinal constituent,

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Fig. 2 Biological activities of spilanthol

i.e., a 2-ketol ester (7Z,9E)-2-oxo-undeca-7,9-dienyl 3-methylbut-2-enoate, actually known as acmellonate [21]. Both molecules are used to reduce the pain associated with toothaches and induce salivary secretion [6]. Some bioactivities highlighted in Fig. 2 must be further discussed here. For instance, the presence of spilanthol is an important factor for the acaricidal activity of Acmella oleracea extract, and fraction extracts with 24.5, 48, and 100% of spilanthol have similar acaricidal activity on a tick (Rhipicephalus microplus), a hematophagous ectoparasite [22]. Recently, a large Brazilian industry has begun the production of an anti-wrinkle cream made with paracress extract (it inhibits contractile activity in subcutaneous face muscles) [3, 23]. Of importance, the yield of spilanthol (by supercritical CO2) in paracress flowers extracts is 65.4%, followed by 47.3% in the stems, and 19.7% in the leaves [20]. Accordingly, the spilanthol content is higher in paracress flowers, and at Brazilian restaurants which sell typical foods, most of the Acmella oleracea flowers are not used, since their excessive use masks the taste of the culinary preparations [23]. Lastly, there is pharmacological potential of alkylamides from Acmella oleracea flowers to treat inflammatory pain [24]. Furthermore, the use of enzyme-linked immunosorbent assay (ELISA) revealed a reduction in the release of interleukin8 and tumor necrosis factor-alpha by leukocytes exposed to spilanthol [25]. 5-Fluorouracil is an antimetabolite fluoropyrimidine analog that is prescribed as a chemotherapy drug, and spilanthol also attenuates 5-fluorouracil-induced intestinal mucositis in mice [26, 27].

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Terpenes

Terpenes may be chemically defined as a group of molecules whose structure is various but having a certain number of isoprene units [28]. They are classified according to the number of isoprene in the basic molecular skeleton (e.g., monoterpenes (10 carbon atoms), sesquiterpenes (15 carbon atoms), diterpenes (20 carbon atoms), sesterpenes (25 carbon atoms), and triterpenes (30 carbon atoms)) [28, 29]. β-caryophyllene, β-pinene, myrcene, caryophyllene oxide, and limonene are examples of terpenes found in paracress flowers [3]. β-caryophyllene is a bicyclic sesquiterpene responsible for the anti-inflammatory, antiedema, antitumor, bactericidal, insecticidal, and spasmolytic properties [30]. βpinene is a potential agent for anticancer and anti-inflammatory drugs [31]. Myrcene is a monoterpene with antioxidant and anti-inflammatory properties [32]. Caryophyllene oxide is of ecological importance to the plant, having great value for the perfume industry due to its characteristic aroma [33]. Limonene has good antibacterial activity against food-borne pathogens (e.g., it may act as a potential inhibitor against Listeria monocytogenes) [34].

3

Other Pharmacological Aspects

If, on the one hand, drug molecules generally have one or two active compounds associated in order to trigger well-known effects, on the other hand, plant organs have numerous bioactive ingredients, acting in synergy (or not) to trigger various effects, usually not clearly known, especially in the traditional medicine. Nevertheless, great effort has been made to understand this complex pharmacology of plants with medicinal potential. For example, diuretic activity may be achieved with paracress flowers (cold water extract) using albino rats as animal models (although the diuretic activity is also found in the whole plant) [6]. Antifungal activity is also found in paracress flowers [6]. Another example may be the pancreatic lipase inhibition, which is the most widely studied mechanism for the identification of potential anti-obesity agents [35]. This pharmacological activity may be achieved with paracress flowers using in vitro model [6]. Vasorelaxant activity may also be achieved with paracress flowers, partially inducing nitric oxide and prostaglandin 2 in albino rats as animal models [6]. However, it is remarkable how most pharmacological activities cannot be compartmentalized in plant organs and can be achieved using the whole paracress plant (e.g., local anesthetic, antipyretic, anti-inflammatory (leaves in particular), analgesic, antioxidant (leaves in particular), antimalarial and larvicidal, aphrodisiac, antinociceptive, immunomodulatory, bioinsecticidal (leaves in particular), and convulsant activities) [6]. This knowledge of the tissue compartmentalization of pharmacological activities is essential for the study and the extraction of the bioactive compounds of the plant.

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Nutritional Features of Paracress

As a food item, paracress is a leafy vegetable mainly consumed after cooking process. Hence, the nutritional composition of the raw paracress differs from that of the processed paracress (as mentioned above), and it is instructive to be discussed briefly here. The chemical and nutritional characterization of paracress shows that the content of protein, ash, carbohydrate, total fiber, mineral, phytosterol, and amino acid (e.g., asparagine, valine, glutamic acid, and isoleucine) levels are interesting, and despite the nutrient loss during the hydrothermal process, the nutritional content of paracress is still higher or similar to those of many conventional vegetables [16]. Therefore, both raw and processed paracress sources have proven to be good alternatives for the conventional vegetables even with nutrient loss after the boiling process [16]. It is worth highlighting the Acmella oleracea macronutrients and micronutrients with the highest content levels such as protein (24.01%), ash (10.92%), total fiber (62.61%), Ca (2551.56 mg 100 g 1), Mg (734 mg 100 g 1), and Cu (2.09 mg 100 g 1), and amino acids such as asparagine (32.01 mg g 1), glutamic acid (28.26 mg g 1), valine (14.55 mg g 1), and isoleucine (14.19 mg g 1) [16].

5

Toxicological Traits in Zebrafish

Zebrafish is a small cyprinoid fish that is native to subtropical India, Nepal, and Bangladesh [36]. Because zebrafish embryo test is highly sensitive to toxicity test of chemical substances on animals, the result can be used as basic data for the toxicity test in higher animals and environmental contamination regulation [6]. The treatment of parental generation of zebrafish with Acmella oleracea flowers (21.873 and 44.457 mg kg 1) and spilanthol (3 mg kg 1) caused severe changes in the gonads and on fertility (however, on the embryo, the most striking effects in the development were recorded in the groups in which the parental generation was treated with the Acmella oleracea flowers, whereas the spilanthol influenced the lethality of the embryos) [37]. Treatment with hydroethanolic extract of Acmella oleracea flowers caused significant behavioral changes and death in zebrafish (the calculated median lethal dose (LD50) was 148.42 mg kg 1, and the calculated median lethal concentration (LC50) was 320 μg L 1) [38].

6

Conclusions

There is a growing body of evidence highlighting the potential use of spilanthol from Acmella oleracea in the treatment of various diseases. Nonetheless, research groups bioprospecting for other bioactive compounds as important as plant alkaloids, phenolic compounds (flavonoids, tannins), saponins, in paracress herb, should carefully standardize their methodologies applied in qualitative tests with the aim of obtaining more reproducible results. On the other hand, quantitative tests are in

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fact more expensive, more laborious, and time-consuming; however, their results are more accurate. Nonetheless, both approaches are undeniably crucial for the advancement in this dynamic multidisciplinary field of science. The phytochemical investigation of Acmella oleracea (L.) R.K. Jansen will greatly benefit from both methodological approaches. Acknowledgments The author expresses special thanks to Raimunda Santos da Cruz for the preparation of the tacacá dish. The author is enduringly grateful to Maria Costa Correa, a beloved friend considered his second mother, and a true guardian angel (in memoriam).

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16. Neves DA, Schmiele M, Pallone JAL, Orlando EA, Risso EM, Cunha ECE, Godoy HT (2019) Chemical and nutritional characterization of raw and hydrothermal processed jambu (Acmella oleracea (L.) R.K. Jansen). Food Res Int 116:1144–1152 17. Tapiero H, Townsend DM, Tew KD (2003) Phytosterols in the prevention of human pathologies. Biomed Pharmacother 57:321–325 18. Kadu C, Parich A, Schueler S, Konrad H, Muluvi G, Eyog-Matig O, Muchugi A, Williams V, Rarnarnonjisoa L, Kapinga C, Foahom B, Katsvanga C, Hafashirnana D, Obama C, Vinceti B, Schumacher R, Ceburek T (2012) Bioactive constituents in Prunus africana: geographical variation throughout Africa and associations with environmental and genetic parameters. Phytochemistry 83:70–78 19. Krishnan KA, Thomas S (2019) Recent advances on herb-derived constituents-incorporated wound-dressing materials: a review. Polym Adv Technol 30:823–838 20. Barbosa AF, Pereira CSS, Mendes MF, De Carvalho Junior RN, De Carvalho MG, Maia JGS, Oliveira AU (2016) Spilanthol content in the extract obtained by supercritical CO2 at different storage times of Acmella Oleracea L. J Food Process Eng 40:7 21. Ley J, Blings M, Krammer G, Reinders G, Schmidt C, Bertram H (2006) Isolation and synthesis of acmellonate, a new unsaturated long chain 2-ketol ester from Spilanthes acmella. Nat Prod Res 20:798–804 22. Marchesini P, Barbosa A, Sanches M, Do Nascimento R, Vale F, Fabri R, Maturano R, De Carvalho M, Monteiro C (2020) Acaricidal activity of Acmella oleracea (Asteraceae) extract against Rhipicephalus microplus: what is the influence of spilanthol? Vet Parasitol 283:109170 23. Balieiro O, Da Silva Pinheiro M, Silva S, Oliveira M, Silva S, Gomes A, Pinto L (2020) Analytical and preparative chromatographic approaches for extraction of spilanthol from Acmella oleracea flowers. Microchem J 157:105035 24. Dallazen JL, Maria-Ferreira D, Da Luz BB, Nascimento AM, Cipriani TR, De Souza LM, Felipe LPG, Silva BJG, Nassini R, De Paula Werner MF (2020) Pharmacological potential of alkylamides from Acmella oleracea flowers and synthetic isobutylalkyl amide to treat inflammatory pain. Inflammopharmacology 28:175–186 25. De Freitas Blanco VS, Michalak B, Zelioli IAM, De Oliveira AS, Rodrigues MVN, Ferreira AG, Garcia VL, Cabral FA, Kiss AK, Rodrigues RAF (2018) Isolation of spilanthol from Acmella oleracea based on green chemistry and evaluation of its in vitro anti-inflammatory activity. J Supercrit Fluids 140:372–379 26. Emamian R, Ebrahimi M, Karimi-Maleh H (2020) A sensitive sensor for nano-molar detection of 5-fluorouracil by modifying a paste sensor with graphene quantum dots and an ionic liquid. J Nanostruct 10:230–238 27. De Freitas-Blanco VS, Monteiro KM, De Oliveira PR, De Oliveira ECS, De Oliveira Braga LE, De Carvalho JE, Rodrigues RAF (2019) Spilanthol, the principal alkylamide from Acmella oleracea, attenuates 5-fluorouracil-induced intestinal mucositis in mice. Planta Med 85:203–209 28. Sezen S, Güllüce M, Kesmez Can F, Alaylar B (2019) Essential oils and antimicrobial effects. 4th international conference on advances in natural & applied sciences. Ağrı 29. Brocksom T, De Oliveira K, Desiderá A (2017) The chemistry of the sesquiterpene alkaloids. J Braz Chem Soc 28:933–942 30. Daniel P, Lourenço E, Da Cruz R, De Souza Gonçalves C, Das Almas L, Hoscheid J, Da Silva C, Jacomassi E, Junior BL, Alberton O (2020) Composition and antimicrobial activity of essential oil of yarrow (Achillea millefolium L.). AJCS 14:545–550 31. Mendoza G, Oviedo M, Pinos J, Lee-Rangel H, Vázquez A, Flores R, Pérez F, Roque A, Cifuentes O (2020) Milk production in dairy cows supplemented with herbal choline and methionine. Rev Fac Cienc Agrar 52:332–343 32. Hoseini S, Khalili M, Rajabiesterabadi H, Hoseinifar S, Van Doan H (2020) Effects of dietary monoterpene, myrcene, administration on immune- and health-related genes expression in common carp gill following exposure to copper sulfate. Fish Shellfish Immun 98:438–445 33. Souza M, Guzatti J, Martello R, Schindler M, Calisto J, Morgan L, Aguiar G, Locateli G, Scapinello J, Müller L, Oliveira J, Magro J (2020) Supercritical CO2 extraction of Aloysia gratissima leaves and evaluation of anti-inflammatory activity. J Supercrit Fluid 159:104753

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Bioactive Compounds of Goosefoot (Genus Chenopodium) Paraskev T. Nedialkov and Zlatina Kokanova-Nedialkova

Contents 1 2 3 4 5 6

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Polysaccharides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Lectins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Amines and Amides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Phenolics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Flavonoids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.1 Flavonoids with Radical-Scavenging and Antioxidant Activities . . . . . . . . . . . . . . . . . . 6.2 Flavonoids with Hepatoprotective Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.3 Flavonoids with Neuroprotective Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.4 Flavonoids with Anti-α-Glucosidase and Prolipase Activities . . . . . . . . . . . . . . . . . . . . . 6.5 Flavonoids with Antiadipogenic Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 Saponins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.1 Saponins with Antibacterial and Antifungal Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2 Saponins with Cytotoxic Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.3 Saponins with Hepatoprotective Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.4 Saponins with Immunoadjuvant and Immunomodilatory Activity . . . . . . . . . . . . . . . . . 7.5 Saponins with Anti-inflammatory Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.6 Saponins with Hemolytic Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 Sterols . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 Essential Oils and Terpenes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.1 Essential Oils with Antibacterial Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.2 Essential Oils with Antifungal Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.3 Essential Oils and Terpenes with Antiparasitic Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.4 Essential Oils and Terpenes with Antineoplastic Activity . . . . . . . . . . . . . . . . . . . . . . . . . 9.5 Essential Oils with Antioxidant Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.6 Essential Oils with Acetylcholinesterase, Butyrylcholinesterase, and Tyrosinase Activities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.7 Essential Oils and Terpenes with Anti-inflammatory Activity . . . . . . . . . . . . . . . . . . . .

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P. T. Nedialkov (*) · Z. Kokanova-Nedialkova Department of Pharmacognosy, Faculty of Pharmacy, Medical University of Sofia, Sofia, Bulgaria e-mail: [email protected]fia.bg; [email protected]fia.bg © Springer Nature Switzerland AG 2021 H. N. Murthy, K. Y. Paek (eds.), Bioactive Compounds in Underutilized Vegetables and Legumes, Reference Series in Phytochemistry, https://doi.org/10.1007/978-3-030-57415-4_7

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9.8 Essential Oils with Sedative and Analgesic Activities . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.9 Essential Oils with Wound Healing Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.10 Toxicity of Essential Oils and Their Constituents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Abstract

The biologically active compounds isolated from Chenopodium species are reviewed. These include compounds of diverse chemical nature: polysaccharides, lectins, amines and amides, phenolics and flavonoids, saponins, sterols, monoterpenes, and essential oils. The data for the biological activity of more than 70 compounds isolated or detected in goosefoot species are found in the literature. A wide range of pharmacological activities of chenopods: antimicrobial, antifungal, antiparasitic, antioxidant, hepatoprotective, neuroprotective, anti-α-glucosidase, prolipase, antineoplastic, anti-inflammatory, hemolytic, wound healing, sedative, and analgesic that appeared in the literature are discussed. The research found in literature was done mainly on C. album, C. ambrosioides, C. bonushenricus, C. botrys, and C. quinoa.

Keywords

Antifungal activity · Antimicrobial activity · Antioxidant activity · Antiparasitic activity · Chenopodium · Essential oils · Flavonoids Abbreviations

3 T3-L1 6-OHDA ABTS+ AChE BALB/c BChE BHT BV-173 C/EBPα Caco-2 CCl4 CCRF-CEM DNA DPI DPPH+ ED50

Mouse fibroblast cells 6-Hydroxydopamine 2,20 -Azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt Acetylcholinesterase Albino immune-deficient inbred mouse strain Butyrylcholinesterase Butylated hydroxytoluene Human B-cell precursor leukemia cell line Cytosine-cytosine-adenosine-adenosine-thymidineenhancer-binding protein alpha Human colorectal adenocarcinoma cell line Carbon tetrachloride Human acute T-lymphoblastic leukemia cell line Deoxyribonucleic acid Days post-injury 2,2-Diphenyl-1-picrylhydrazyl Median effective dose

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EO ESR EtOAc FRAP GSH HeLa HepG2 HL-60 Hoechst33258 IC50 IFN-α IFN-γ IgM IL-6 Jurkat E6-1 K-562 L02 LC-MS LDH LPLAFT LPS LYSO MBC MCF 10A MCF-7 MDA-MB-231 MIC MTT NO PHA/PMA PPARγ RAW264.7 ROS SC50 SKW-3 SMMC 7721 SREBP-1c TNF-α TPA UPLC/Q-TOF-MS WHO

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Essential oil Electron paramagnetic resonance Ethyl acetate Ferric reducing/antioxidant power Glutathione Human cervical adenocarcinoma cell line Human liver cancer cell line Human acute promyelocytic leukemia cell line Pentahydrate (bis-benzimide) – 10 mg/mL solution in water Half maximal inhibitory concentration Interferon-alpha Interferon-gamma Immunoglobulin M Interleukin 6 Human acute T-cell leukemia cell line Human chronic myelogenous leukemia cell line Human normal liver cells Liquid chromatography coupled with mass spectrometry Lactate dehydrogenase Lipid peroxidation of linoleic acid by ferric thiocyanate Lipopolysaccharide Lysozyme Minimum bactericidal concentration Human normal breast epithelial cell line Human breast cancer cell line Human mammary gland/breast adenocarcinoma cell line Minimum inhibitory concentration 3-(4,5-Dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide Nitric oxide Phytohemagglutinin/phorbol 12-myristate 13-acetate Peroxisome proliferator-activated receptor gamma Abelson murine leukemia virus-transformed macrophage Reactive oxygen species Half maximal scavenge capacity Human T-cell leukemia cell line Human liver cancer cell line Sterol regulatory element-binding protein 1c Tumor necrosis factor-alpha 12-O-tetradecanoylphorbol-13-acetate Ultra-performance liquid chromatography coupled with quadrupole time-of-flight mass spectrometry World Health Organization

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Introduction

According to a study by the World Health Organization (WHO), about three-quarters of the world’s population use traditional herbal medicines for the health care of local people. The plants are the oldest companions of humans and were used not only for food and shelter but also provided mankind with cures for different ailments [1]. The goosefoot genus (Chenopodium, family Chenopodiaceae) numbers a wide range of species and is native to all the continents with exception of Antarctica as well as in some distant archipelagoes (such as Juan Fernandez, New Zealand, and Hawaii) [2]. It includes more than 200 species and most of these are colonizing herbaceous annuals, but some suffrutescent and arborescent perennials were also known. The goosefoot species with great economic importance are C. album, C. berlandieri subsp. nuttalliae, C. pallidicaule, and C. quinoa [3]. The seeds from C. quinoa are used to produce a flour that is incorporated in several toasted and baked goods, while the quinoa leaves are eaten similarly like spinach. Moreover, the germinated quinoa seedlings (quinoa sprouts) are used in salads [4]. C. pallidicaule (Cañihua) is found in Peru and Bolivia where its seeds are put in soups or are ground into flour which is used to prepare fermented drinks, cakes, and bread [5]. C. berlandieri subsp. nuttalliae is a Mesoamerican annual plant that has two vegetable cultigens, Huauzontle and Quelite, as well as the seed crop Chia roja [6]. C. album is mainly employed as a leafy vegetable and foliage crop, though some Himalayan cultivars are planted for grain [3]. Many species of this genus are used as medicinal agents in some traditional systems of medicine. The chenopods with ethnopharmacological data for their medicinal uses are C. album, C. ambrosioides, C. bonus-henricus, C. botrys, C. californicum, C. capitatum, C. chilense, C. cristatum, C. graveolens, C. pallidicaule, C. schraderianum, C. scoparia, and C. vulvaria [7]. C. album is traditionally used as a sedative, hepatoprotective, diuretic, blood purifier, laxative, antiscorbutic as well as an anthelmintic against worms. Pharmacological investigations have shown that the plant possesses contraceptive, sperm immobilizing, and anthelmintic properties. There is also data for antinociceptive and antipruritic activities [8]. C. ambrosioides has various pharmacological indications: treatment of influenza, cold, gastrointestinal, and respiratory ailments as well as vomiting. Also, the extracts or essential oil (EO) from C. ambrosioides is employed as an antihelmintic agent for the healing of skin ulceration due to leishmaniasis infection; they also possess anti-inflammatory and antitumor properties [9]. C. bonus-henricus is another popular goosefoot species and it is used to treat skin ailments, panaritium, bladder trouble, scurvy, swollen legs, and feet as well as a mild laxative [10]. In traditional medicine, C. botrys is applied in the therapy of different inflammatory disorders, cutaneous wounds, diabetes, gastric ulcer, and infectious diseases of different origin [11]. In this chapter, we review the biologically active principles isolated from Chenopodium species. Compounds of diverse chemical nature (polysaccharides, lectins, amines and amides, phenolics and flavonoids, saponins, sterols, monoterpenes, and essential oils) isolated from different Chenopodium species were

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included. A wide range of pharmacological activities of these biologically active compounds that appeared in the literature was discussed as well. We hope that this review will draw the attention of the scientists to more in-depth research of isolated biologically active substances from Chenopodium species and the discovery of lead compounds that can serve as models for the synthesis of new pharmacological agents.

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Polysaccharides

The seeds of Chenopodium quinoa yielded arabinan and arabinan-rich pectic polysaccharides that showed gastroprotective activity on ethanol-induced acute gastric lesions in rats [12]. A novel polysaccharide fraction with low molecular weight (8852 Da) was isolated from the seed of C. quinoa. Its monomers were found to be galacturonic acid and glucose monosaccharides. The polysaccharide exhibited significant free radical scavenging activity against 2,2-diphenyl-1-picrylhydrazyl (DPPH+) and 2,20 -azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt (ABTS+). This polysaccharide promoted the Abelson murine leukemia virustransformed macrophage (RAW264.7) proliferation, while suppressed the nitric oxide (NO) production on inflammatory RAW264.7 macrophage in a dose- and time-dependent manner. Furthermore, its cytotoxic activity was evaluated on the human normal liver (L02), human normal breast epithelial (MCF 10A), human liver cancer (SMMC 7721), and human breast cancer (MCF-7) cells lines by 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay in vitro. It showed cytotoxicity against cancer cells while leaving normal cells intact [13]. A polysaccharide with a molecular weight of 34.0 kDa was isolated from the soluble nonstarch polysaccharide fraction of C. quinoa seeds. The analysis revealed that it was mainly composed of mannose, rhamnose, galacturonic acid, glucose, galactose, xylose, and arabinose. It showed significant immune-enhancing activity through successfully improving the serum levels of interferon-gamma (IFN-γ), interleukin 6 (IL-6), interferon-alpha (IFN-α), immunoglobulin M (IgM), and lysozyme (LYSO). Besides, the polysaccharide enhanced the phagocytic function of mononuclear macrophages and ameliorated delayed allergy in mice [14].

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Lectins

A novel heterodimeric lectin was isolated from the seeds of Chenopodium quinoa. Its molecular weight was approximately 60 kDa and consisted of two subunits of about 25 and 35 kDa. The lectin was found to effectively inhibit three Gram-negative strains: Escherichia coli, Pseudomonas aeruginosa, and Salmonella enterica. Also, it was shown that it agglutinated human erythrocytes. Its activity remained stable under a wide range of pH levels and temperatures but was inhibited by mannose and glucose [15].

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Amines and Amides

Compounds (1–3) (Fig. 1) were isolated from the ethanol extract of C. ambrosioides and showed moderate antioxidant and anti-inflammatory activities against lipopolysaccharide (LPS)-induced tumor necrosis factor-alpha (TNF-α) and IL-6 gene expression [16]. The ethanolic extract from the seeds of C. formosanum (Djulis) as well as one of its main constituents betanin (4) (Fig. 1) suppressed the lipid accumulation in vitro in mouse fibroblast (3 T3-L1) adipocytes by decreasing the gene expression of the important proteins responsible for the lipid biosynthesis (PPARγ, C/EBPα, and SREBP-1c) [17].

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Phenolics

The methanol extract from the seeds of C. album led to the isolation of a new phenolic glycoside named, chenoalbuside (5) (Fig. 2). The antioxidant properties of chenoalbuside were tested by the DPPH assay with half-maximal scavenge capacity (SC50) of 0.14 μg/mL [18].

Fig. 1 The structures of bioactive amines and amides Fig. 2 The structure of a phenolic glycoside from C. album seeds

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Flavonoids

6.1

Flavonoids with Radical-Scavenging and Antioxidant Activities

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Six flavonol glycosides of kaempferol (6–9) and quercetin (10–11) (Fig. 3) were isolated from C. quinoa seeds. Quercetin-3-glycosides, 10 (IC50 ¼ 10 μM) and 11 (IC50 ¼ 11 μM), showed much stronger DPPH radical scavenging activity compared to kaempferol-3-glycosides 6 (IC50 ¼ 82 μM), 7 (IC50 ¼ 86 μM), 8 (IC50>100 μM) and 9 (IC50>100 μM). The results confirmed that flavonoids with free orthodihydroxy groups in B ring express better antioxidant properties than those where it is missing or is blocked by substituents [19]. Three kaempferol glycosides (12–14) and kaempferol (15) itself (Fig. 3) were found in the leaves of C. ambrosioides. Their antioxidant properties were assessed by the DPPH+ test using ascorbic acid as a positive control. The results showed that kaempferol exhibited more potent antioxidant compared to its glycosides 12–14 [20]. The methanol extract from the aerial parts of C. foliosum gave three flavonol glycosides of gomphrenol (17–19) (Fig. 4) that were tested for radical-scavenging activity using DPPH+ and ABTS+ tests. The results showed that DPPH+ activity of flavonoids 17 and 18 was low or lacking, but they possessed moderate ABTS+ radical-scavenging (29.22% and 28.30%, respectively) when compared to vitamin C (91.60%) and similar activity to butylated hydroxytoluene (BHT) (26.49%), while 19 showed a low ABTS+ (IC50 141.03 μM) and DPPH+ (IC50 690.48 μM) activities [21–23]. Besides, compound 19 did not show any activity on ferric

Fig. 3 The structures of bioactive glycosides of kaempferol and quercetin

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Fig. 4 The structures of gomphrenol and 6-methoxyflavonol glycosides

reducing/antioxidant power (FRAP) and inhibition of lipid peroxidation of linoleic acid by ferric thiocyanate (LPLAFT) tests [22]. Nine glycosides of 6-metoxyflavonol aglycones 6-methoxykaempferol, patuletin, and spinacetin 20–28 (Fig. 4) were isolated and identified from the methanol extract of C. bonus-henricus aerial parts [10]. Compounds 20–22 were also found in the aerial parts of C. foliosum [21], while 22, 23, and 25 were detected in the roots of C. bonus-henricus [24]. Radical scavenging and antioxidant activities of compounds 20–28 were established using DPPH+ and ABTS+ tests as well as by LPLAFT method. Patuletin glycosides 21, 24, and 27 showed the highest DPPH+ and ABTS activity compared to vitamin C. Spinacetin glycosides 22, 25, and 6-methoxykaempferol glycosides 20, 23 possessed a significantly low DPPH+ activity and demonstrated high ABTS+ radical-scavenging activity. Spinacetin and 6-methoxykaempferol glycosides 28 and 26, containing esterified ferulic acid in their moiety, demonstrated a moderate DPPH+ and high ABTS+ activity. All flavonoids inhibited significantly the lipid peroxidation of linoleic acid [25].

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Kaempferitrin 17 (Fig. 3) found in the aerial parts of C. ambrosioides, C. murale, and C. ficifolium growing in Egypt were assessed on a rabbit cardiovascular system and expressed dose-dependent bradycardia and hypotension. Furthermore, kaempferitrin also showed dose-dependent hypotension in genetically modified hypertensive rats. Also, it was tested on isolated guinea-pig aortic strip and atria and did not block α1 or β1-adrenoceptors, respectively [26].

6.2

Flavonoids with Hepatoprotective Activity

Flavonoids 19–28 (Fig. 4) significantly reduced the rat hepatocyte damage caused by carbon tetrachloride (CCl4) by preserving cell viability and glutathione (GSH) levels, decreasing lactate dehydrogenase (LDH) leakage, and reducing lipid damage [10, 22].

6.3

Flavonoids with Neuroprotective Activity

The compounds 20–28 (glycosides of patuletin, 6-methoxykaempferol, and spinacetin) showed statistically significant neuroprotective activities on isolated rat brain synaptosomes using 6-hydroxydopamine (6-OHDA) in vitro model by preserving synaptosome viability and reducing GSH levels. Among the tested compounds, 6-methoxykaempferol glycoside 26 expressed the most prominent neuroprotective and antioxidant effects compatible with silibinin [27].

6.4

Flavonoids with Anti-α-Glucosidase and Prolipase Activities

Anti-α-glucosidase and lipase activities of nine glycosides of patuletin, 6-methoxykaempferol, and spinacetin (20–28) were established by measuring the levels of the released 4-nitrophenol using LC-MS. Patuletin glycosides 21 and 27 possessed similar anti-α-glucosidase activity to acarbose. All tested flavonoids exhibited prolipase activity and could be used in the treatment of cachexia. The results have shown that the effective anti-α-glucosidase and prolipase activity possessed the flavonoids with 30 ,40 -orthodihydroxy configuration in B ring. Esterification of flavonoids with ferulic acid also increased their activities [27].

6.5

Flavonoids with Antiadipogenic Activity

The kaempferol 15 and rutin 16 (Fig. 3) found in an ethanolic extract from the seeds of C. formosanum (Djulis) suppressed the lipid accumulation in vitro in 3 T3-L1 adipocytes by decreasing the gene expression of the critical molecules involved in lipid synthesis (PPARγ, C/EBPα, and SREBP-1c) [17].

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Saponins

Saponins from seeds and bran of Chenopodium quinoa have been heavily studied for their structural diversity and biological properties. Two reviews by Kuljanabhagavad and Wink [28] as well as by El Hazzam et al. [29] on quinoa saponins chemistry and biological properties have appeared recently.

7.1

Saponins with Antibacterial and Antifungal Activity

A new 29 triterpene saponin together with five known major saponins 30–34 (Fig. 5) was isolated from the quinoa seeds and was tested for antifungal activity against Candida albicans. The crude saponin mixture inhibited the growth of C. albicans, while the pure individual saponins showed little or no activity, which suggested a possible synergistic effect between these saponins [30]. Recently, six different compounds 35–40 (Fig. 5) were isolated and identified from quinoa husks. The disk diffusion method and assessment of the MIC/MBC were employed for the establishment of anti-bactericidal effects against six bacterial species (Bacillus cereus, Listeria ivanovii, Pseudomonas aeruginosa, Salmonella enteritidis, Staphylococcus aureus, and S. epidermidis). All the tested compounds expressed bactericidal effects against foodborne pathogens B. cereus, S. aureus, and S. epidermidis. The tested saponins caused a degradation of the bacterial cell wall followed by disruption of the cytoplasmic membrane and membrane proteins, thus leading to a leakage of the cell contents [31].

7.2

Saponins with Cytotoxic Activity

The cytotoxicity of the triterpene saponins 41–44 isolated from C. quinoa seeds together with their aglycones 45–47 (Fig. 5) were tested in human cervical adenocarcinoma (HeLa) cells. The bidesmosidic saponins 41–44 showed marginal cytotoxicity with IC50 > 100 μg/mL while their aglycones 45–47 were more cytotoxic with IC50 ranging from 25.4 to 50.5 μg/mL. The apoptotic levels of human colorectal adenocarcinoma (Caco-2) cells, established by flow cytometry, showed that the aglycones 45–47 were more active than corresponding saponins 41–44 [32]. Four glycosides of 30-normedicagenic acid 48–51 (Fig. 6) were isolated from C. foliosum. These compounds showed marginal cytotoxicity on a panel of leukemic tumor cell lines (BV-173, SKW-3, HL-60) [33]. Compounds 52 and 53 (Fig. 7), found in C. album seeds, induced apoptosis in MCF-7 cell line by effectively inhibiting human topoisomerases I and II as well as by blocking the cell cycle at S phase in vitro [34]. Six triterpene saponins 54–59 (Fig. 8) isolated from the roots of C. bonushenricus showed weak to marginal cytotoxicity on five leukemic cell lines (HL-60, SKW-3, BV-173, K-562, and Jurkat E6-1) [35].

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Fig. 5 The structures of bioactive triterpene saponins from quinoa

Fig. 6 The structures of 30-normedicagenic acid glycosides

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Fig. 7 The structures of cytotoxic saponins from C. album

Fig. 8 The structures of triterpene saponins isolated from C. bonus-henricus

7.3

Saponins with Hepatoprotective Activity

The saponins 54–59 showed protective activity compatible to silymarin against the toxic effects of CCl4 on rat hepatocytes by preserving cell viability and GSH level, decreasing LDH leakage, and reducing lipid damage [36].

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7.4

109

Saponins with Immunoadjuvant and Immunomodilatory Activity

Two saponin fractions, each containing up to 10 bisdesmosides of phytolaccagenic acid, serjanic acid, oleanolic acid, and hederagenin were obtained from quinoa seeds. The adjuvant activity of the fractions was tested on mice by immunization subcutaneously with ovalbumin alone or adjuvanted Quil A (adjuvant control) and with saponin fractions. It was found that both saponin fractions significantly enhanced the production of humoral and cellular immune responses to ovalbumin in mice [37]. The ability of the 30-normedicagenic acid glycosides 48–51, isolated from C. foliosum as well as triterpene saponins 54–59, isolated from the roots of C. bonus-henricus to modulate the interleukin-2 production in PHA/PMA stimulated Jurkat E6-1 cells was studied. In this experimental system compounds 50, 51, and 54 were showed to be the most potent [33, 35].

7.5

Saponins with Anti-inflammatory Activity

Four saponin fractions containing 11 triterpene bisdesmosidesaponins of 3,23,30trihydroxyolean-12-en-28-oic acid, phytolaccagenic acid, and hederagenin were isolated from the seeds of C. quinoa planted in China. All tested fractions showed anti-inflammatory activity by inhibition of the NO production as well as by releasing of TNF-α and IL-6 in a dose-dependent manner in lipopolysaccharide-induced RAW264.7 cells [38].

7.6

Saponins with Hemolytic Activity

The hemolytic activity on erythrocytes of saponins 29–34, isolated from quinoa seeds and their derived monodesmosides were evaluated. It was established that monodesmosides possess a higher degree of hemolytic activity compared to their respective bisdesmosides [30].

8

Sterols

Eight phytoecdysteroids 46–53 (Fig. 9) were isolated from the seeds of C. quinoa and showed satisfactory results on the calfskin collagenase inhibitory test, on their effectiveness to scavenge the DPPH+ free radicals, as well as on their ability to chelate the iron metal ions. The results of this study suggested that ecdysteroids could be used as potent molecules to prevent or delay both oxidative stress and collagenase-related skin damages [39]. The ethyl acetate fraction of C. badachschanicum Tzvelev gave a new sterol named chenisterol 54 (Fig. 10) that was found to be significantly active against

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Fig. 9 The structures of phytoecdysteroids isolated from C. quinoa seeds Fig. 10 The structure of antibacterial steroid from C. badachschanicum

Bacillus subtilis, Cornybacterium diptheriae, Klebsiella pneumoniae, and Staphylococcus epidermidis [40].

9

Essential Oils and Terpenes

9.1

Essential Oils with Antibacterial Activity

The essential oil (EO) from aerial parts of Chenopodium botrys showed significant bactericidal activity against some Gram-positive (Staphylococcus aureus and Bacillus subtilis) and gram-negative (Escherichia coli, Pseudomonas aeruginosa, Klebsiella pneumoniae, Salmonella enteridis, Sarcina lutea, and Shigella flexneri) bacterial strains compared to the reference antibiotics amikacin and cefotaxime [41]. The study on EO from C. botrys collected from Bulgaria expressed significant

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111

antibacterial activity against Salmonella aureus and Bacillus cereus [42], while the EO from the same species growing in Saudi Arabia showed activity against Staphylococcus aureus and Bacillus subtilis [43]. An EO of C. Botrys collected in Iran expressed strong antimicrobial activity against Staphylococcus saprophyticus while Bacillus cereus, Klebsiella pneumoniae, Listeria monocytogenes, Salmonella typhimurium, Staphylococcus epidermidis and Streptococcus mutans were less affected [44]. Alternative research of Iranian EO of C. botrys showed that it inhibited the growth of Escherichia coli and Staphylococcus aureus cultures in concentrations of 7 mg/mL [45]. It was found that an EO from C. ambrosioides growing wildly in Egypt exhibited antibacterial activity against Bacillus subtilis and Escherichia coli [46]. In other research, the agar cavity diffusion method was employed to test the antibacterial activity of EO from C. ambrosioides on Escherichia coli, Listeria monocytogenes, Salmonella choleraesuis, and Staphylococcus aureus bacterial strains. The EO showed antibacterial activity for both Gram-negative and Gram-positive bacteria with minimal inhibitory concentrations ranged from 62.5 to 250 μL/mL [47]. Shi et al. investigated the inhibitory effects of the EO from C. foetidum on Escherichia coli and Bacillus subtilis using the filter paper diffusion test. This EO prevented from the growth of both bacterial strains but the inhibition of B. subtilis was much more significant [48].

9.2

Essential Oils with Antifungal Activity

The EO obtained from the leaves of C. ambrosioides completely seized the micellar growth of Aspergillus flavus and also showed broad antifungal activity against A. niger, A. fumigatus, Botryodiplodia theobromae, Cladosporium cladosporioides, Helminthosporium oryzae, and Pythium debaryanum at 0.1 mg/mL [49]. In an alternative investigation, the fungitoxic properties of EO from C. ambrosioides L. were assessed by the poison food assay at three concentrations (0.3%, 0.1%, and 0.05%) on eight postharvest deteriorating fungi (Aspergillus flavus, A. glaucus, A. niger, A. orchaceus, Colletotrichum gloesporioides, C. musae, Fusarium oxysporum, and F. semitectum) [50]. The in vitro and in vivo antifungal properties of C. ambrosioides EO against candida species (Candida albicans, C. glabrata, C. guilliermondii, C. krusei, C. lusitaniae, C. parapsilosis, and C. tropicalis) were established. The in vitro fungitoxic activity was shown to be concentrationdependent while the MIC was within the range of 0.25–2 mg/mL. The induced vaginal candidiasis rat model was employed to assess in vivo antifungal activity. It did not show dose-dependent fungitoxicity. It took 12 days of treatment to recover the mice from the induced infection [51]. In vitro and in vivo antifungal activity of EOs of C. ambrosioides and Cymbopogon martini as well as their synergism against Aspergillus, Microsporum, and Trichophyton species were investigated. The MICs of the EOs and their combination were found between 150 and 500 ppm, while those of known antifungal drugs (griseofulvin, ketoconazole, and fluconazole) ranged from 1000 to 5500 ppm. Ointments with EOs were prepared and applied against

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induced ringworm in a guinea pig model and disease removal was observed in 7–21 days. The synergistic effect of C. ambrosioides and C. martini EOs in a 1:1 ratio was found to be more efficient than C. ambrosioides EO but less effective than C. martini EO [52]. The EO from the aerial parts of C. botrys showed significant fungitoxic activity against Aspergillus niger and Candida albicans comparable to the reference fungistatic nystatin and amphotericin [41]. Furthermore, it expressed a strong activity against the dermatophytes Trichophyton mentagrophytes, Epidermophytonfloccosum, and Microsporum canis [53].

9.3

Essential Oils and Terpenes with Antiparasitic Activity

It was found that the EO produced from C. ambrosioides inhibited Trichomonas vaginalis with a MIC of 25 mg/mL [54]. Monzote et al. [55] studied the toxicity of an EO of C. Ambrosioides on Leishmania amazonensis. The tested EO significantly inhibited promastigote and amastigote forms, with ED50 values of 0.0037 and 0.0046 mg/mL, respectively [55]. Different routes of administration of EO in BALB/c mice infected with L. amazonensis were also investigated. An intraperitoneal administration of the EO (dose of 30 mg/kg) prevented the lesion development and decreased the parasite burden, while the oral administration retarded the infection compared with untreated mice. The both routes of administration with doses of 30 mg/kg EO outperformed the positive reference amphotericin B (1 mg/kg) [56]. The co-administration of EO from C. ambrosioides with pentamidine showed a synergic effect against promastigotes of L. amazoniensis [57]. Also, the oral treatment with the EO against cutaneous leishmaniasis in BALB/c mice caused by L. amazonensis was studied. The infected mice were treated with doses of 30– 150 mg/kg of the EO for 15 days. The antileishmanial effect of EO was compared with the reference drugs glucantime (28 mg/kg), amphotericin B (1 mg/kg), and pentamidine (4 mg/kg) that were administered daily over 15 days by the intraperitoneal route. A dose of 150 mg/kg was the most effective, and no macroscopic toxic effects were observed and outperformed the reference drugs [58]. Furthermore, the in vitro effect of the EO against L. donovani was investigated. The EO significantly inhibited promastigotes and amastigotes with EC50 of 0.00445 and 0.0051 mg/mL, respectively. The growth of promastigotes was irreversibly inhibited after treatment with 0.1 or 0.01 mg/mL EO for 1 or 24 h, respectively [59]. Recently, the in vitro antileishmanial activity of the EO from C. ambrosioides and its major components ascaridole (55), carvacrol (56), and caryophyllene oxide (57) (Fig. 11) were tested against a panel of Leishmania species as well as Plasmodium falciparum and Trypanosoma brucei. All tested products were active against promastigote and amastigote forms of Leishmania species. Ascaridole exhibited the best antileishmanial activity while the EO had the highest selectivity index. Only the EO showed an antiprotozoal effect against P. falciparum and T. brucei [60]. An alternative investigation showed that ascaridole itself was found to be a successful inhibitor of P. falciparum

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Fig. 11 The structures of bioactive terpenoids from C. ambrosioides

growth. After 3 days, the growth development was arrested by a drug concentration of 0.05 μM, and at 0.1 μM and no parasites can be found in the culture. At lower concentrations of ascaridole, the effect was observed mainly at the trophozoite stage, whereas the ring stage was marginally affected but could not continue normal development and ceased to grow at a later stage [61]. The EO of C. ambrosioides L. was found to inhibit successfully in vitro the thirdstage larvae of Ancylostoma spp. at a concentration of 0.150 μL mL1.The herbal cookies containing 37.5 μL g1 of the EO significantly reduced the number of eggs per gram in feces of dogs naturally infected with Ancylostoma spp. [62]. Four monoterpene hydroperoxides 58–61 (Fig. 11) along ascaridole isolated from C. ambrosioides were assessed in vitro for trypanocidal activity against Trypanosoma cruzi. The minimal concentrations of ascaridole and compounds 58– 61 that killed the epimastigotes of T. cruzi were within the range of 0.8–23 μM [63].

9.4

Essential Oils and Terpenes with Antineoplastic Activity

It was found that the EO of C. ambrosioides expressed a dose- and time-dependent cytotoxic effect on human breast cancer MCF-7 cell line with IC50 values within the range of 9.45–18.75 μg/mL depending incubation period. Besides, the OE induced apoptosis, as well [64]. Alternative research on cytotoxicity of EO and its main components p-cymene (62) and α-terpinene (63) (Fig. 11) on MCF-7 suggested that the mechanism of action of inhibition of cell proliferation and death was by inducing oxidative damage. The results showed that the main components of EO were less cytotoxic than the EO itself [65]. It was established that the EO can inhibit the proliferation of human liver cancer SMMC-7721 cell line, which may be related to inducing cell cycle arrest and caspase-dependent apoptosis [66]. Ascaridole showed significant in vitro antineoplastic properties of different tumor cell lines in vitro (CCRF-CEM, HL60, MDA-MB-231). Thus pointing out that ascaridole may be a promising novel drug candidate for the treatment of cancer [67].

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Essential Oils with Antioxidant Activity

The EO from C. ambrosioides assessed for radical scavenging activity on the ABTS+ method. It showed the highest antioxidant activity (95.66%) at concentrations of 3 mg/mL [49]. The antioxidant activity of the EO of C. botrys L. collected from three different parts of Turkey using free radical scavenging, phosphomolybdenum, ferrous ion chelating, and reducing power assays was established. The highest antioxidant activity on all test systems with exception of superoxide anion radical scavenging assay showed the EO from Isparta sample while the EO from Afyonkarahisar sample performed better on phosphomolybdenum, ferrous ion chelating, and reducing power assays [68].

9.6

Essential Oils with Acetylcholinesterase, Butyrylcholinesterase, and Tyrosinase Activities

The inhibitory activities on acetylcholinesterase (AChE), butyrylcholinesterase (BChE), and tyrosinase of the EO from C. botrys L. were established. The EO from Konya samples expressed maximal activity on AChE and tyrosinase inhibition assays with 0.87 mg GALAEs/g oil and 0.82 mg KAEs/g oil, respectively. Furthermore, the EO from Afyonkarahisar sample showed the best performance on BChE inhibition assay with 1.02 mg GALAEs/g oil [68].

9.7

Essential Oils and Terpenes with Anti-inflammatory Activity

Usman et al. [69] investigated the anti-inflammatory activity of leaf EO of C. album L. The EO displayed strong anti-inflammatory activity against 12-O-tetradecanoylphorbol13-acetate (TPA)-induced ear edema in mice [69]. Seven hydroxyl monoterpenes 64–70 (Fig. 11) were isolated from C. ambrosioides and were assessed for anti-inflammatory activity. The compound 64 was found to moderate the ability of LPS-stimulated RAW 264.7 macrophages to inhibit NO production with an IC50 value of 16.83 μM [70].

9.8

Essential Oils with Sedative and Analgesic Activities

The oral administration of ascaridole (100 mg/kg) showed the hypothermic effect and an analgesic effect on acetic acid-induced writhing in mice. Prolongation of the anesthesia-induced by sodium pentobarbital was also observed at the same dose of this compound. Besides, ascaridole reduced the methamphetamine enhanced locomotor activity. The administration of higher doses (300 mg/kg) of this compound led to convulsions and lethal toxicity in mice [71].

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9.9

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Essential Oils with Wound Healing Activity

The study on the effects of EO of C. botrys on skin wound healing markers in Sprague-Dawley male rats was undertaken. The animals treated with EO demonstrated a significant decrease in the wound area during the treatment. Parameters such as alignment of the healing tissue, re-epithelialization, and epithelial formation in treated with the EO group showed a significant increase. Besides, treatment with EO lowered the wound surface area and the number of lymphocytes and neutrophils and increased the number of blood vessels, ratio of collagen to total, and ratio of collagen to the cell [11].

9.10

Toxicity of Essential Oils and Their Constituents

The mechanism of toxicity of the EO of C. ambrosioides and its major ingredients (ascaridole, carvacrol, and caryophyllene oxide) concerning mammalian cells and mitochondria was studied. It was observed that the mitochondrial electron transport chain was inhibited by all products. This effect for carvacrol and caryophyllene oxide was mediated via direct complex I inhibition. The Fe2+ ions were crucial for the toxicity of ascaridole to mammalian mitochondria than other major ingredients. It was shown that Fe2+ potentiated the toxicity of ascaridole on oxidative phosphorylation of rat liver mitochondria. The increase of the α-tocopherol quinone/αtocopherol ratio under these conditions indicated the initiation of lipid peroxidation by Fe2+-mediated ascaridole cleavage. Furthermore, the ESR spin-trapping experiments showed that in addition to Fe2+, reduced hemin, but not mitochondrial cytochrome c can activate ascaridole. This phenomenon explained why ascaridole exhibited higher toxicity in peritoneal macrophages from BALB/c mice rather than in isolated mitochondria [72]. The EO of C. ambrosioides and its main components ascaridole, isoascaridole (71) (Fig. 11), and p-cymene possessed fumigant toxicity against male German cockroaches with LC50 values of 4.13, 0.55, 2.07, and 6.92 μg/L air, respectively. Topical application bioassay showed that all tested products were toxic to male German cockroaches, and ascaridole was the strongest with an LD50 value of 22.02 μg/adult while the EO with an LDM50 value of 67.46 μg/adult [73].

10

Conclusion

This chapter briefly reviews the bioactive compounds isolated or detected in Chenopodium species. The research was done mainly on C. album, C. ambrosioides, C. bonus-henricus, C. botrys, and C. quinoa. Seventy-one compounds of diverse chemical nature (polysaccharides, lectins, amines and amides, phenolics and flavonoids, saponins, sterols, monoterpenes, and essential oils) isolated from different species were included. A wide range of pharmacological activities of goosefoot species such as antimicrobial, antifungal, antiparasitic, antioxidant, hepatoprotective, neuroprotective,

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anti-α-glucosidase, prolipase, antineoplastic, anti-inflammatory, hemolytic, wound healing, sedative, analgesic, etc., that appeared in the literature have been discussed as well. The authors hope that this review will draw the attention of the scientists to more in-depth research of isolated biologically active substances from Chenopodium species and the discovery of lead compounds that can serve as models for the synthesis of new pharmacological agents.

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Bioactive Compounds of Asian Spider Flower (Cleome viscosa Linn.) Veenu Kaul and Shveta Saroop

Contents 1 2 3 4 5 6

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nutraceutical Importance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . As Ayurvedic and Folkloric Asset . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ethno Medicinal Profile . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Phytochemistry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Biological Activities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.1 Antimicrobial Potential . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2 Hepatoprotective Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.3 Antitumor Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.4 Anthelmintic Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.5 Antidiarrheal Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.6 Antipyretic Property . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.7 Nematicidal Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.8 Insecticidal Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.9 Antifibrotic Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.10 Antiemetic Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.11 Psychopharmacological Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.12 Immunomodulatory Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.13 Anti-inflammatory Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.14 Antioxidant Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.15 Gastro-Protective Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.16 Anticonvulsant Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

123 124 125 126 126 128 128 130 131 131 131 131 132 132 132 132 133 133 133 133 134 134 135 135

V. Kaul (*) Department of Botany, University of Jammu, Jammu, India S. Saroop (*) Department of Botany, Government Degree College, Kathua, India © Springer Nature Switzerland AG 2021 H. N. Murthy, K. Y. Paek (eds.), Bioactive Compounds in Underutilized Vegetables and Legumes, Reference Series in Phytochemistry, https://doi.org/10.1007/978-3-030-57415-4_8

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Abstract

The present review puts forth a comprehensive bioactive profile of a Neglected and Underutilized Species (NUS), Cleome viscosa Linn. in the perspective of its ethno-pharmaceutical potential. Commonly known as “Asian spider flower, Bee plant, Tickweed, Cleome, Wild and Dog mustard,” it is an extensively proliferating weed inhabiting the tropics throughout world including India. The species is reported to be a traditional and folkloric asset in India and Thai medicinal systems. The species is bestowed with antiseptic, antihelmintic, carminative, rubefacient, vesicant, febrifuge, and cardiac stimulant properties. Owing to the rich bioactive profile, its pharmacological screening and tremendous biological properties thus inferred is intensifying day-by-day in the scientific world. On account of the immense bioactive potential, the species use can be strategized for ensuring and stabilizing medico-nutritional food security.

Keywords

Antimicrobial · Antioxidant · Bioactive · Cleome · NUS · Traditional

Abbreviations

ABTS AIDS ALP ALT AST BACs CCl4 DPPH FRAP HIV IC50 LC LNA MES MIC NUS PGE2 PTZ TBL TFC TPC WBC

2–20 -Azino-di-[3-ethylbenzthiazoline sulfonate] Acquired immunodeficiency syndrome Alkaline phosphatase Alanine transaminase Aspartate transaminase Bioactive compounds Carbon tetrachloride 3 2,2-Diphenyl-1-picrylhydrazyl Ferric-reducing antioxidant power Human immunodeficiency virus Half-maximal inhibitory concentration Lethal Concentration 2-amino-9-[4-oxoazetidin-2-yl]-nonanoic acid Maximal electroshock induced seizures (MES) Minimum inhibitory concentration Neglected and Underutilized Species Prostaglandin E2 Pentylenetetrazole induced seizures Serum total bilirubin Total flavonoid content Total phenol content White Blood Cell

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Bioactive Compounds of Asian Spider Flower (Cleome viscosa Linn.)

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Introduction

In the era of biodiversity crisis and global eco-economical stress on medicinal plants, much of the focus is on traditional or indigenous medicinal practices or systems also called “little traditions” as per anthropological terminology. The knowledge about therapeutic properties of these botanical resources is prevalent among small sociocultural tribes inhabiting limited geographical regimes. To discover and promote Indian herbal drugs, there is an imperative/urgent need to assess the therapeutic potentials of these wild indigenous, native plant species also termed as Neglected and Underutilized Species (NUS). Contributing to regional nutritional and medicinal security, these plants are well adapted to local bio-eco-sociological conditions and require little venture to improve their productivity or quality [1, 2]. Beyond this, these NUS can improve livelihoods via income generation by small farmers, streamline local laborers, or landholders and provide local market setups. Contributing to the diversity and the stability of agro-ecological systems, and buffering the sustained nutritional security and of natural products to conservation of cultural/regional identity of local communities, the potential of NUS is debatable worldwide. Nevertheless, these NUS are now-a-days overlooked as a choice for sustainable food systems under climate change due to their inherent virtue as stress managers/mitigating units, higher survival strategists, and proliferation processors. Further, due to their adaptability to marginal environments with low-input and low greenhouse gas emissions (low carbon footprint), these plants can address socioeconomic and environmental conflicts amidst climate change thereby sustaining as Climate Change Mitigation agro-ecosystems [3, 4]. NUS are invaluable assets to indigenous systems of medicine owing to their therapeutic properties. These owe to a wealthy spectrum of bioactive compounds (abbreviated as BACs). Also termed as plant secondary metabolites, these BACs are the derivatives of primary metabolic products obtained through different metabolic pathways. Together with pharmacological, antipathogenic, herbivory, drought, and stress tolerant properties, these confer survival potentialities on the plants [5–7]. Rich in bioactive compounds, the standardized extracts from a wide array of medicinal NUS provide diverse opportunities for isolation and characterization of new drugs [8]. Use of BACs in various commercial sectors like pharmaceuticals, food, and agro-industries signifies the same. These are rapidly replacing the synthetic medicines in recent societies due to their cheapness, easy accessibility, and availability and above all, negligible side effects. Multifaceted approaches involving botanical, phyto-chemical, biological, and molecular techniques are heading towards drug discovery from medicinal plants [9]. In recent years, fertilizers, herbicides, and fungicides from biological sources are being studied, formulated and evaluated, and then released for immediate use. Apart from that, breeding these nutrient-rich neglected leafy vegetables can serve as effective means of achieving bio-fortification in the era of nutritional insufficiency and insecurity. The present communication serves both as a review of traditional knowledge, bioactive diversity, and values in pharmaceutical profile and nutraceutical stuffs of one such NUS, Cleome viscosa.

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C. viscosa, the species under investigation, is commonly known as Asian spider flower, Bee plant, Tickweed, Cleome, Wild and Dog mustard. Its synonyms are Polanisia viscosa (L.) DC., Cleome icosandra L., P. icosandra L. and Arivela viscosa (L.) Raf) [10, 11]. Its Indian vernaculars and common names in countries other than India are tabulated below. Scientific Names: Arivela viscosa var. deglabrata (Backer) M.L.Zhang & G.C.Tucker; Arivela viscosa (L.) Raf.; Cleome icosandra L.; Cleome acutifolia Elmer; Cleome viscosa var. nagarjunakondensis Sundararagh; Cleome viscosa var. parviflora Kuntze; Cleome viscosa f. deglabrata (Backer) Jacobs; Cleome viscosa var. viscosa (L.); Polanisia viscosa (L.) DC; Polanisia microphylla Eichler; Polanisia icosandra (L.) Wight & Arn; Polanisia viscosa var. deglabrata Backer; Polanisia viscosa (L.) Blume; Polanisia viscosa var. icosandra (L.) Schweinf. ex Oliv. Common Names: Wild mustard; Cleome; Tickweed; Dog mustard; Mouzambe jaune; Barba de chivo; Yellow mesambay, Jitomate; Frijolillo; Plantanillo; Sambo; Brède caya; Ttabaquillo, Collant Indian Vernaculars: Pivala tilavan, Hurhuria or Bagra (Bengali), Hulhul (Urdu), Peeli Neoli (Dogri), Hurhur (Hindi), Naikkaduku or Nayikkaduga (Tamil), Naivela (Malayalam), Pilitalvani (Hindi) and Nayibela (Gujarati), Kanphuti (Marathi), Nal Sirio (Jharkhand), Kukkavaminta (Telugu), adityabhakta, arka (Sanskrit)

Native to Australia, the said species grows abundantly in northern and central Australia [12]. The species has also spread to various warmer regions of the world like India [11, 13]; Japan [14]; West Pakistan [10]; Ethiopia, Zanzibar West Africa, peninsular Arabia, Indonesia, Cambodia, and Bangladesh [15]. In India, C. viscosa is distributed abundantly in Himachal Pradesh, Delhi, Haryana, Chhattisgarh, Bihar [16], Odisha [17], Uttar Pradesh [18], Gujarat [19]), Rajasthan [20, 21], Kerala [22], Andhra Pradesh [23], Tamil Nadu [24], and Maharashtra [25]. The species is growing extensively as a prolific weed all along wastelands, roadsides, fallow lands, and other degraded regions of Jammu province, Jammu and Kashmir [26–29].

2

Nutraceutical Importance

Plant parts are used by local communities to meet their food, nutritional, and health needs thus entitling it as a future crop with promising potential. In India, the seeds are used in pickles and as a substitute for cumin (Cuminum cyminum) and mustard. Its seeds contain amino acids, proteins, lipids, fatty acids such as oleic and linoleic acids of dietary importance. Seed oil is used for cooking vegetables, curries, and pulses [30, 31]. Cleome viscosa along with its sister species C. gynandra are two wild or semi-domesticated herbaceous weeds highly consumed as traditional leafy vegetables in Southern Benin [32]. Certain ethnic groups of Benin like Goun, Sahoue, Adja Aizo, and Mina use these species in tribal medicinal systems to cure fever and chronic malaria. In Benin, the Cultural Importance (CI) indices like food (CIUA), medicinal (CIUM), and cultural value (CI) indices work at 0.02, 0.45, and

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0.51, respectively. It is also said to have medico-magical utility. For example, the crushed leaves with perfume are thought to attract happiness conferring thereby the epithet of “lucky plant” on this species. In tropical Africa, bitter leaves of C. viscosa are consumed in all forms; these are eaten fresh, dried, or cooked. The leaf and seed powder is added as a supplement to improve narcotic property of tobacco [33] in Sumatra. The plant parts being rich in fibers and low in fat are pickled and thus used [34, 35]. Elemental composition of leaves include macroelements like Nitrogen (2.8%), Potassium (0.07%), Phosphorus (0.3%), Iron (0.04%), Calcium (0.3%), Magnesium (0.3%), and Copper (0.006%) and micronutrients like Sodium, Zinc, Boron, Manganese, Chlorides, and Silicon. Together, these also add to the therapeutic and nutraceutical utility of the plants. The plant parts possess on an average 54.33 mg g1 Crude protein, 2.02 mg g1 Vitamin C, 0.015 mg g1 fat, and 81.33 mg g1 total sugar [35]. Many tribes of Garhwal Himalaya, Chhattisgarh, Jharkhand (Oraon tribals of district Latehar), Odisha, Kerala, and Rajasthan, India, meet their nutritional requirements by using young shoots and leaves as a vegetable and seeds as condiment [22, 35, 36]. The seed oil possesses high nutritional value and defatted seeds are often used to prepare cake [21].

3

As Ayurvedic and Folkloric Asset

The plant species is a popular Ayurvedic medicine. Leaf juice is used against earache and skin diseases and leaf paste for headache. It is also reported to remove “Kapha” (phlegm) [37]. Leaves are effective against conjunctivitis, stomach troubles, headaches, neuralgia, arthritis, constipation, chest pain, fever, herpes, and thread-worm infections. Leaf sap is squeezed into nostrils, ears, and eyes to treat ear ache and epileptic seizures. Application of leaves over external wounds and ulcers prevents sepsis. Decoction of leaves is used as an expectorant and digestive stimulant to cure dysentery and colic pain. The reports on leaf juice to be beneficial for piles, malaria, and lumbago [38] are also known. Seeds are proved to be useful against cough, fever, ulcers, tumors, worm infestations, inflammations, uterine complaints, cardiac disorders, liver diseases, infantile convulsions, and many more [39]. Seed decoction is used against rheumatism, gonorrhea, diarrhea, dysentery, and in piles. Oil derived from its seeds has rubefacient, vesicant, carminative, and anthelmintic activities. Decoction of roots is used as a febrifuge. In Ayurvedic medicinal system, C. viscosa is used in the treatment of diseases termed as karnaroga (ear diseases), kandu (pruritus), krmiroga (worm infection), asthila (prostate enlargement), and gulma (any tumor, lump, or diverticulosis) [40]. In Thai traditional medicine, the plant recognized to have chemo-preventive activity is used to treat gastrointestinal ailments. Moreover, plant parts are also used for Osteoarthritis of the knee [41]. The roots and seeds are considered a cardiac stimulant and prescribed for snake-bite in Sri Lanka. The aboriginals of Australia use the leaves to relieve headaches [38]. The plant is used to treat diabetes in Israel.

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In the Unani system of medicine, the seeds have been used against diarrhea and fever [42]. The plant’s parts are used as a green cover and as manure in areas of species abundance (e.g., in Ghana). The prominence of C. viscosa in ethnobotany, agroeconomy, and yield and costbenefit analysis has been extensively studied and highlighted by Maikhuri et al. [43]. Locally called as Jakhiya, the species perpetuates naturally from seed in rain fed agricultural and abandoned land areas at 500 to 1500 meters altitudes in the Garhwal Himalayan region. Grain and by-product yield of the species in pure crop strands are 600 and 950 kg/ha, respectively, which is approx. three times higher than those maintained under mixed cropping conditions (i.e., along with other crops). Rising consumption of its seeds resulted in the commercialization of the said species in Garhwal Himalayas, thereby providing economic benefits to the local farmers. The seeds are exchanged by the traditional farmers there with those from nearby areas where it does not grow. Farmers sell Cleome seeds for Rs 10.00 per kg to middlemen traders who in turn resell it in the nearby semi-urban and urban centers for Rs 40.00 to Rs.70.00 per kg [43]. However, the wider utility of its seed as a condiment has raised its efficiency as a bio-prospecting resource like many other traditional crops. Defatted seeds serve as alternative source of fodder in many drier regions and for production of biogas. Due to volatile activity of plant parts, it reduces infestation of termites thus enhancing the crop yield [44].

4

Ethno Medicinal Profile

C. viscosa is known to possess gastroprotective [45], antidiarrheal, analgesic, anti-inflammatory, antipyretic [46–48]; anthelmintic [49]; antibacterial [50, 51]; insecticidal, repellent, nematicidal [52]; anticonvulsant [53]; antimicrobial and allelopathic [54]; hepatoprotective [55, 56]; antifungal, nephrotoxic, immunomodulatory, and psychopharmacological [57, 58]; mutagenic [59], and carminative, ant scorbutic, sudorific, febrifuge [13] properties (Table 1).

5

Phytochemistry

The species possesses immense phytochemical benefits owing to the wide variety of bioactive compounds present in its different plant parts. Major contributions to pharmacology have been made by [13, 38, 60, 61] to name a few. Bioactive compounds like dihydrokaempferol-40 -xyloside, dihydrokaempferide 3-glucuronide, naringenin-4-glycoside, docosanoic acid, β-amyrin, and lupeol isothiocyanate producing glucosides and stigmasta-5,24[28]-diene-3β-O-α-L-rhamnoside are present in the roots [62–65] and querection 3–0-(200 -,acetyl)-glucoside in leaves. Glycosides, namely, quercetin 7-O-α-L-rhamnopyranoside quercetin 3-O-β-D-glucopyranoside 7-O-α-L-rhamnopyranoside, kaempferol 3-O-β-D-glucopyranoside 7-O-α-L-rhamnopyranoside, astragalin, visconoside C, kaempferitrin,

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Table 1 The ethno-medicinal profile of C. viscosa Whole plant/extract Act as rubefacient, anthelmintic, and antimicrobial Used in treatment of septic ears, migraine, diphtheria, headache, pneumonia, and stomach ailments Has insecticidal, antifeedant and repellent and antitick property Act as mosquito repellent thus used as antimalarial bio agent Curative medicine for neuralgia, headache, cough, wounds, and counterirritant Has anti-HIV potential Leaves and young shoots Act as vesicant and rubefacient thus used against rheumatism and localized pains Decoction of leaves relieves headaches to treat neuralgia and stiff neck As a leafy vegetable Used in treatment of arthritis, skin diseases, and uterine complaints Has anti-irritant, antipyretic, analgesic, antiseptic, anti-inflammatory, hepatoprotective, immunomodulatory, anthelmintic, antidiarrheal, carminative, sudorific, febrifuge, cardiac stimulant, psychopharmacological, anticonvulsant, antinociceptive, and antioxidant activities Leaf juice is applied externally during pyorrhea and used as wormicide Juice of leaves is a remedy for ear pain Leaf juice is used against lumbago, piles, ulcers, and external wounds Leaf juice or its oil is applied for eye wash and epileptic fits Flower Used in treatment of oral ailments, chest pain, thread-worm infection, constipation, conjunctivitis, and convulsions Decoction is used against chronic fever Act as antiarthritic, anticough, toxic, antimalarial, and anti-inflammatory Fruit Has antinociceptive and anti-inflammatory property Roots Root decoction used to treat fevers Used in the prevention of miscarriages and treatment of colic pains Root decoction or infusion is used to facilitate childbirth Seed Have anthelmintic and rubefacient, carminative and antispasmodic property Internally used for expelling roundworms and externally as counter-irritant Are nutritive. Possess Dietary amino acids, proteins, lipids, fatty As a substitute for mustard An infusion is administered to reduce coughing Seed Oil Biodiesel property Insecticidal activity especially against ticks Seed cake Used as animal food/fodder.

kaempferol 3-O-(4-O0 Acetyl)-α-L-rhamnopyranoside, kaempferol 7-O-α-L-rhamnopyranoside, were isolated from the leaves by chromatography techniques. While cleomiscosins A, B, and C, coumarinolignoids [66], stigmasta-5,24[28]-diene3β-O-α-l-rhamnoside [64], 30 ,40 -dihydroxy-5-methoxy flavanone-7-O- α -Lrhamnopyranoside, eridoil-5-rhamnoside [63]; 5,40 - di-O-methyl eriodictyol-7-O-

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β -d-glucopyranoside, ergast-5-ene-3-O- α -l-rhamnopyranoside [65], Viscosin (monomethoxy trihydroxyflavone), docosanoic acid, lactam nonanoic acid, fatty acids, and taxicol [54] have been found in seeds [51, 67, 68] (Table 2). Cleomiscosin D (a minor coumarino-lignan; a regioisomer of clemiscosin C) and cleosandrin (derivative of umbelliferone) [69] have also been isolated from seeds. Adding to this, C. viscosa harbors varied diterpenes like macrocyclic diterpene [3E, 7E, 11E]-20-oxocembra-3, 7, 11, 15-tetraen-19-oic acid and bicyclic diterpene cleomeolide [70, 71]. Chattopadhyay et al. (2011) isolated an optically active nevirapine, a dipyrido diazepine metabolite (a nonnucleoside inhibitor of HIV-1 reverse transcriptase) from seeds. The compound is likely to find utility in treating AIDS [72]. The chemical compounds isolated from the whole plant include glyco flavanone (30 ,40 -dihydroxy-5-methoxy flavanone-7- O-α-l-rhamnopyranoside); glycoside (eriodictyol-5-rhamnoside), saponin (ergast-5-ene-3-O-β-l-rhamnopyranoside, stigmasta5,24(28)-diene- 3β-O-α-l-rhamnoside and 5,40 - di-O-methyl eriodictyol-7-O-β-dglucopyranoside); glucosinolates (glucocleomin and glucocapparin); cleomaldeic acid ((3E, 7E, 11E) 20-oxocembra-3,7,11,15-tetraen- 19-oic acid), a macrocyclic diterpene [64, 65, 73]. Apart from these specific compounds, rich array of secondary metabolites like phenols, alkaloids, flavonoids, saponins, steroids, tannins, glycosides, cardiac glycosides, cyanogenic terpenoids (epi-lupeol and lupeol), coumarins, proanthocyanidins, leuco- and anthocyanins are found in the said species [74, 75]. As per Ezeabara and Nwafulugo [76], mean percentages of flavonoid, saponin, tannin, protein, and fat proportion in the leaves of C. viscosa are 0.57  0.02, 0.52  0.02, 0.36  0.00, 11.73  0.18, and 2.13  0.02, respectively. Being allelopathic, all plant parts like root, stem, leaves, flowers, seeds, and plant litter liberate a certain quantity of allelo-chemicals into the surrounding environments. The root and stem extracts are reported [77] to be autotoxic and inhibit seed germination and rooting in Bruguiera gymnorhiza.

6

Biological Activities

6.1

Antimicrobial Potential

The plant extracts are active against varied microbes ranging from bacteria to fungi. Owing to the occurrence of a 14-member ring of cembranoid diterpenes in leaves and stems, the species is effective against several bacteria and fungi. Minimum inhibitory concentration (MIC) values on Pseudomonas fluorescens (Gramnegative) and Bacillus subtilis (Gram-positive) were, respectively, found to be 1.0 μg/spot and 5.0 μg/spot for this diterpene. The leaf and flower ethanol extracts also exhibited remarkable antimicrobial activity against Proteus vulgaris, Escherichia coli, and Pseudomonas aeruginosa. That towards Staphylococcus aureus (Gram-positive bacteria) is ascribed to quercetin 3–0-(200 -acetyl)-glucoside, a flavonoid glycoside [74].

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Table 2 List of bioactive compounds and their phytochemical properties in C. viscosa Bioactive compounds Arginine, aspartic acid, lysine, histidine, tyrosine and seed oils (fatty acids, phytosterols, linoleic acid, oleic acid, palmitic acid, arachidic acid, stearic acid, octadec(11E)-enoicacid; palmitoleic acid; linolenic acid; arachidic acid, eicosa-(11Z) enoic acid, hexacosanoic acid, 12-oxo-stearic acid and pentacosanoic acid Querection 3–0-(200 -acetyl)-glucoside; cleomaldeic acid; 2-amino-9-(4-oxoazetidin-2-yl)-nonanoic acid Anthocyanins Chrysosplenetin; 5,7,40 -trihydroxy3,30 -dimethoxyflavone Kaempferide 3-glucuronide Cyanogenic glycosides, isothiocyanate-producing glucosides, lignoceric acid; monoacylated and diacylated Cyanidin 3-sophoroside-5-glucosides Aromatic amines and alkynes Flavonoids, alkaloids, phenols Carotenoids Cardiac glycosides Cabralealactone Cleogynol (20s, 24 s) -epoxy-19,25-dihydroxy Dammarane-3-one hemiketal Triterpenes (lupeol, epi-lupeol); Macrocyclic diterpene Saponins Tannins Isokaempferide Stigmasta-5,24 (28)-diene-3β-O-α-L-rhamnoside and Jaceosidin, penduletin Ursolic acid Axillarin Sesquiterpenes; Triterpene; 5,30 -dihydroxy3,6,7,40 50 -pentamethoxyflavone 5-hydroxy-3,6,7,30 ,40 ,50 -hexamethoxyflavone; 5,40 -dihydroxy-3,6,7,8,30 -pentamethoxyflavone Cleomiscosins A and B; bicyclic diterpene cleomeolide Cleomiscosins (A, B and C); coumarino-lignoids (Naringenin glycoside) Nevirapine Triterpenes (Dammarane-type) 5,7,40 -trihydroxy-6,30 ,50 -trimethoxyflavone Phytol, (+)-cedrol and octacosane Butane Unsaturated cembrane acids, glutamic acid

Property Nutritive

Cytotoxic Chemo-preventive Anticancer Antimicrobial, toxic Antiparasitic, poisonous

Antiplasmodial, antibacterial Antioxidant, anticancer Free radical scavenging capacity, nutritive Used against congestive heart failure, cardiac contraction, arrhythmia Analgesic, anti-inflammatory, and antiemetic Anticancer, antibacterial Antitumor Antifeedants, plant defense Repellent and insecticidal Cytotoxic, anticancer Anti-inflmmatory Analgesic, antiemetic Toxic Antimicrobial, insecticidal

Antibacterial Hepato-protective Anti-proliferative Antimicrobial Insecticidal Toxic and repellent Anti-parasitic, Fuel Cytotoxic and anti-inflammatory (continued)

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Table 2 (continued) Bioactive compounds Cleomeprenols; Macrocyclic diterpene Anthraquinones Glycosides; luteolin-7-O-glucoside; kaempferol-3-Oglucoside; glucocapparin, heneicosanoic acid, behenic acid; flavonoids Flavanols Cleomeolide Rutin Alkanes Triacontane, tetracosane Pentacosane-nonacosane, hentriacontane, and dotriacontane

Property Antimicrobial, anti-oxidant Antiplasmodial, anticancer Antimicrobial

Anticonvulsant Antiarthritic properties Anti-inflammatory inhibits platelet aggregation, hemorrhoids, varicosis Insecticidal

A crystalline compound, Allantoin, isolated from the plant’s methanol extract exhibited in vitro antibacterial activity against Gram-negative and Gram-positive bacteria. MIC (Maximum Inhibitory Concentrations) of Allantoin was reported to be 8 μg/mL for Klebsiella pneumoniae, Escherichia coli, and Staphylococcus aureus while 4 μg/mL for Bacillus subtilis [78]. Crude methanolic extract exhibits antibacterial activity against Vibrio cholerae, Staphylococcus saprophyticus, S. aureus, Shigella sonnie, Shigella flexneri, Salmonella typhi, and Streptococcus epidermidis, with inhibition zone ranging from 10.76 to 16.34 mm [79]. Methanol extract possesses promising potential against Pseudomonas aeruginosa, P. vulgaris, Escherichia coli, Staphylococcus aureus, and Klebsiella pneumoniae [80]. LNA (2-amino-9-[4-oxoazetidin-2-yl]-nonanoic acid) isolated from the root exudates is effective against Staphylococcus aureus, Pseudomonas aeruginosa, E. Coli and Aspergillus niger, A. fumigatus, and A. tamarii. Dosage of 500 ppm and above proved to be effective against S. aureus and P. aeruginosa while for E. coli it remained unaffected. Mishra et al. [81] reported the toxicity against ringworm-causing fungi. The aqueous leaf extract is effective against Trichophyton mentagrophytes, Epidermophyton floccosum, and Microsporum gypseum [81]. The aqueous extract of aerial parts at 30 and 40 mg/mL concentration values showed high inhibition activity against Aeromonas hydrophila and Bacillus cereus [82].

6.2

Hepatoprotective Activity

Ethanolic leaf/seed extract of the said species exhibited strong activity against both paracetamol- and thioacetamide-induced hepatotoxic albino rats under in vitro conditions [56]. The activity is inferred by restoration of various parameters like total protein,

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ALT (alanine transaminase), TBL (serum total bilirubin), ALP (alkaline phosphatase), and AST (aspartate transaminase). Hepatoprotective potential of aqueous and ethanolic extracts was evaluated against carbon tetrachloride (CCl4)-induced hepatotoxicity in albino rats [56]. This activity was conferred by the presence of coumarinolignoids (namely cleomiscosins A, B, and C) in seeds. The extract was also reported to be effective in reducing the thiopental induced sleep in carbon tetrachloride treated animals. According to Sengottuvelu and co-workers [55], the hepatoprotective activity of this species is comparable (similar) to standard “Silymarin,” a standard agent [55].

6.3

Antitumor Activity

Antimutagenicity of seed oil was testified in S. typhimurium strains TA 98 and TA 100 using Ames mutagenicity assay [59]. The methanolic extract causes significant reduction in tumor cell volume and their viable counts and extended life time in Ehrlich ascites carcinoma-bearing mice acting thereby as antitumor agent. The antitumor potential has been attributed to triterpenoids and flavonoids present in these extracts.

6.4

Anthelmintic Activity

The aqueous and alcoholic seed extracts at 10 to 100 mg/mL concentration value showed anthelmintic activity against Ascaridia galli and Pheretima posthuma with significant results at 100 mg/mL [83].

6.5

Antidiarrheal Activity

Cleome viscosa is an effective anti-diarrheal ayurvedic medicine. This traditional folklore utility was confirmed by various in vitro studies. The methanol extract of the entire plant was tested for antidiarrheal potential in experimental rats. The same extract also exhibited significant inhibitory potential against castor oil induced diarrhea and prostaglandin E2 (PGE2)-induced enteropooling in rats. Similarly methanolic extract of C. viscosa induces significant diminution that was observed in gastrointestinal motility in rats via the charcoal meal test [46].

6.6

Antipyretic Property

The antipyretic potential of C. viscosa was worked out by Devi et al. [48]. They studied the effect of methanol extract on two parameters, namely, normal body temperature and yeast-induced pyrexia in albino rats under experimental condition. The dosage ranging from 200 to 400 mg/kg body weight resulted in significant reduction in body temperature in the two types. In fact, the antipyretic effect was found similar to that of standard paracetamol (150 mg/kg body weight).

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Nematicidal Activity

Cleome viscosa solvent extracts possess nematicidal activity against Meloidogyne javanica (root-knot nematode) and M. incognita Chitwood [plant parasitic nematode] [84]. The nematicidal activity of a 72.69% Abbott’s value against Meloidogyne incognita Chitwood is on record.

6.8

Insecticidal Activity

Plant bears a wide range of phytocidal chemical components and essential oils thatare toxic and have oviposition inhibitory and insect repellent properties. Significant repelling results were found against Clavigralla tomentosicollis (cevopea pod suckling bugs), Cylas formicarius elegantulus, Aedes aegypti, Callosobruchus chinensis (pulse beetle) [85]. High percentage oviposition deterrence index (56.31–85.51%) of the plant extracts in C. chinensis revealed the extent of their oviposition inhibition. Leaf extracts of the species are found to be effective against the pest, Spodoptera litura [86]. The ethanol extract of the leaves exhibited good larvicidal potential against 2nd and 4th stage instar larvae of the malarial vector, Anopheles stephensi. Similar response was reported against A. aegypti (Linnaeus) and Culex quinquefasciatus (Say) [87]. The LC50 values reported against third instar larvae of A. aegypti were 126.12, 82.43, 179.26, and 123.34 ppm in response to C. viscosa extract. As per ethnomedical report by Saxena et al. [88], Santhal tribals of Madhya Pradesh, India, burn off the leaves to repel mosquitoes.

6.9

Antifibrotic Activity

Cleome viscosa also acts as an antifibrotic agent. The same was conferred by the affectivity of ethanolic extract against carbon tetrachloride induced liver fibrosis in rats. In Carbon tetrachloride-induced liver fibrosis, there is an elevated level of thiobarbituric acid, hydroxyproline and serum enzymes, and decrease in total platelet counts in the liver. The ethanolic plant extracts decreased the thiobarbituric acid, hydroxyproline, and serum enzyme levels thereby acting as an effective antifibrotic drug [13].

6.10

Antiemetic Activity

Cleome viscosa seed oil showed antiemetic activity in chicks [89]. Fixed oil doses in proportion to 75 mg/kg body weight, 100 mg/kg body weight, and 125 mg/kg body weight significantly reduced the retches number by 84.43%, 85.56%, and 91.77%, respectively. Interestingly, seed oil of C. viscosa inhibited emesis significantly than chlorpromazine [89].

6

Bioactive Compounds of Asian Spider Flower (Cleome viscosa Linn.)

6.11

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Psychopharmacological Activity

The plant derived extracts also exhibited psychopharmacological effects. Significant ones were found in exploratory and general body behavior in rats and mice. Similarly, effects were also reflected in muscle relaxant movement, fluctuations in normal body temperature, and phenobarbitone induced sleeping time. The application of extract caused decreased spontaneous activity, reduced patterning in exploratory behavior tested via head dip and Y-maze test, lower body temperature, and less muscle relaxation as examined by rotarod. In addition to this, extract significantly enhanced the phenobarbitone-induced sleeping time. An extract dosage of 200–400 mg/kg produced remarkable psychopharmacological effects [90].

6.12

Immunomodulatory Activity

The immunomodulatory potentials of both ethanol and aqueous extracts of the aerial plant parts were assessed by various hematological and serological tests. These extracts assayed significant immunosuppressant properties expressed by decreasing splenic lymphocytes and WBC counts, cellular and humoral antibody responses, and reduced phagocytic index in mice [61]. Further, in vivo investigation by Bawankule et al. [91] confirmed the immunomodulatory role of seed coumarino-lignoids.

6.13

Anti-inflammatory Activity

C. viscosa showed significant anti-inflammatory activity against histamine, dextranand carrageenan-induced rat paw edema under in vivo conditions. The presence of flavonoid glycoside inhibits the prostaglandin synthesis thus contributing to the antiinflammatory potential. Quercetin 3–0-(200 -acetyl)-glucoside obtained from ethyl acetate extract showed resistance towards carrageenan-induced rat paw edema. Similarly, oral administration of seed coumarinolignoids in a dose dependent manner showed strong anti-inflammatory potential [92]. Coumarinolignoids significantly repress the pro-inflammatory mediators and enhance the production of antiinflammatory mediators [66]. Parimala and co-authors [93] demonstrated significant anti-inflammatory activity of plant extracts in contrast to a nonsteroidal antiinflammatory standard, Diclofenac sodium (20 mg/kg).

6.14

Antioxidant Activity

As already mentioned earlier, leaves of the said species are rich in phenols and flavonoids. These secondary metabolites confer the species with great antioxidant and free radical scavenging potential. The antioxidant profile of the species has been

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confirmed by Pillai and Nair [94] using FRAP (ferric-reducing antioxidant power), ABTS, hydroxyl, DPPH, superoxide, nitric oxide, and hydrogen peroxide assays. The total phenol (TPC) and total flavonoid (TFC) contents of C. viscosa leaves were 66.38  0.82 mg/g and 0.54  0.04 mg/g, respectively. The antioxidant activity value was 77.30%. A significant free radical scavenging activity of the leaf extracts was observed in terms of low IC50 values in DPPH (373.18 mg/ml) and hydroxyl radical (573.55 mg/ ml) [94]. The high quantum of hexacosanol and kaempferol further increases the radical scavenging activity. Similarly, presence of compounds like gallotannins, free gallic acid, iridoid, saponins, and poly-phenolic compounds in MeOH extract confer high antioxidizing properties to this species [95, 96].

6.15

Gastro-Protective Activity

Helicobacter pylori, a Gram-negative bacterium, causes gastrointestinal disorders including peptic ulcer, dyspepsia, and gastritis, in human beings. In an attempt to find relief against these disorders, Bhamarapravati and co-researchers [97] reported the gastroprotective activity of C. viscosa. They observed the in vitro susceptibility of Helicobacter pylori strains against plant’s methanol extract. The study revealed the inhibitory effect of methanol extract on the growth of Helicobacter pylori with a MIC (minimum inhibitory concentration) of 50 μg/mL [97].

6.16

Anticonvulsant Activity

Anticonvulsant activity of Cleome viscosa seed extract was performed via Maximal Electroshock induced seizures (MES) and Pentylenetetrazole induced seizures (PTZ) tests. Both aqueous and ethanol seed extracts showed significant activity in both PTZ and MES induced convulsions. Applications in nanotechnology and biodiesel production are the recent areas of interest and investigation in this species. Extracts of plant parts are employed in synthesizing silver phyto-nanoparticles, an ecofriendly and cost effective alternative to conventional chemically commercialized protocols. The process of synthesis involves reduction of silver ions in aqueous silver nitrate solution treated with plant extract [98]. The seed oil (26%) serves as a rich source of unsaturated and free fatty acids. Major oil components include linoleic acid (47.0–61.1%), oleic acid (16.9–27.1%), palmitic acid (10.2–13.4%), and stearic acid (7.2–10.2%) [99]. Some other components like octadec-(11E)-enoicacid, palmitoleic acid, arachidic acid, eicosa-(11Z) enoic acid, heneicosanoic acid, 12-oxo-stearic acid linolenic acid, behenic acid, pentacosanoic acid, lignoceric acid, and hexacosanoic acid add to the total oil composition. Minor and trace oil constituents include triacontane, hentriacontane, dotriacontane tetracosane, pentacosane, hexacosane, heptacosane, octacosane, nonacosane, and alkanes. The fatty acid profile of the oil along with physico-chemical

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characteristics is akin to that of Pongamia and Jatropha (nonedible biodiesel crops) reflecting upon the promising potential of present species as biodiesel resource [34, 100]. As per Saroop and Kaul [75], several features of the plant like annual lifecycle, rapid growth rate, easy cultivation on marginal lands, and huge seed production through mixed mating further increase the chances of utilizing the crop for biodiesel production.

7

Conclusions

Extensive cultivation and improved commercialization practices of NUS like present species is enviable due to their excellent medicinal, nutritional, pharmaceutical, and economic potential to stabilize medicinal and food security. Raising awareness about the hidden potentials of said species will contribute to genetic, physiological, biochemical, and molecular investigations underlying the key traits of food, medicinal, and nutritional interest. A triangular value chain network involving traditional indigenous knowledge with scientific pharmaceutical background coupled with genetics and genome-enabled research strategies should be designed to systemize the utility of such a wonder plant, Cleome viscosa.

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85. Krishnappa K, Elumalai K (2013) Mosquitocidal properties of Basella rubra and Cleome viscosa against Aedes aegypti (Linn.) (Diptera: Culicidae). Eur Rev Med Pharmacol Sci 17:1273–1277 86. Phowichit S, Buatippawan S, Bullangpoti V (2008) Insecticidal activity of Jatropha gossypifolia L. (Euphorbiaceae) and Cleome viscosa L. (Capparidacae) on Spodoptera litura (Lepidoptera: Noctuidae). Toxicity and carboxylesterase and glutathione-S-transferase activities studies. Commun Agric Appl Biol Sci 73:611–619 87. Bansal SK, Singh KV, Sharma S (2014) Larvicidal potential of wild mustard (Cleome viscosa) and gokhru (Tribulus terrestris) against mosquito vectors in the semi-arid region of Western Rajasthan. J Environ Biol 35:327–332 88. Saxena BR, Koli MC, Saxena RC (2000) Preliminary ethnomedical and phytochemical study of Cleome viscosa L. Ethnobotany 12:47–50 89. Ahmad LS, Suktana M, Hasan MM, Azhar I (2011) Analgesic and antiemetic activity of Cleome viscosa. Pak J Bot 43:119–122 90. Parimala Devi B, Boominathan R, Mandal SC (2004) Studies on psychopharmacological effects of Cleome viscosa Linn. Extract in rats and mice. Phytother Res 18:169–172 91. Bawankule DU, Chattopadhyay SK, Pal A, Saxena K, Yadav S, Yadav NP, Srivastava A, Gupta AK, Khanuja SPS (2007) An in- vivo study of the immunomodulatory activity of coumarinolignoids from Cleome viscosa. Nat Prod Commun 2:923–926 92. Meena A, Yadav DK, Srivastava A, Khan F, Chanda D, Chattopadhyay SK (2011) In silico exploration of anti-inflammatory activity of natural coumarinolignoids. Chem Biol Drug Des 78:567–579 93. Parimala B, Boominathan R, Mandal SC (2003) Evaluation of anti-inflammatory activity of Cleome viscosa. Indian J Nat Prod 19:8–12 94. Pillai LS, Nair BR (2013) Radical scavenging potential of Cleome viscosa l. and Cleome burmanni W and A (Cleomaceae). Int J Pharm Sci Res 4(2):698–705 95. Jane RR, Patil SD (2012) Cleome viscosa: an effective medicinal herb for otitis media. Int J Sci Nat 3(1):153–158 96. Koppula S, Ammani K, Bobbarala V (2011) Assessment of medicinal potentials of Cleome viscosa L. methanol extract. Int J Chem Anal Sci 2:12–14 97. Bhamarapravati S, Pendland SL, Mahady GB (2003) Extracts of spice and food plants from Thai traditional medicine inhibit the growth of the human carcinogen Helicobacter pylori. Vivo (Attiki) 17(6):541–544 98. SudhaLakshmi YG (2011) Green synthesis of silver nanoparticles from Cleome viscosa: synthesis and antimicrobial activity. In: International conference on bioscience, biochemistry and bioinformatics (IPCBEE), vol 5. IACSIT Press, Singapore 99. Prasad RR, Azeemoddin G, Ramayya DA, Thirumala SD, Devi KS, Pantulu AJ et al (1980) Analysis and processing of Cleome viscosa seed and oil. Eur J Lipid Sci Technol 82:119–121 100. Kumari R, Jain VK, Kumar S (2012) Biodiesel production from seed oil of Cleome viscosa L. Indian J Exp Biol 50(7):502–510

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Bioactive Compounds of Mallow Leaves (Corchorus Species) Shashi Bhushan Choudhary, Neetu Kumari, Hariom Kumar Sharma, Pankaj Kumar Ojha, and J. Uraon

Contents 1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 Nutritional Composition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1 Protein, Fatty Acid, β-Carotene, and Vitamin C . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Essential Minerals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3 Dietary Fiber . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4 Culinary Advantages . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Abstract

The genus Corchorus consists more than 50 species with diverse origin and applications. Economically the genus is popular as a natural fiber crop (C. olitorius and C. capsularis) particularly in Asian countries. However, utilization of Corchorus leaves as health promoting food gained fresh momentum in today’s health conscious consumer dominating market. In this context, present chapter discussed active bio compounds facilitating possible commoditization of the genus. S. B. Choudhary (*) ICAR-National Bureau of Plant Genetic Resources, Regional Station Ranchi, Ranchi, Jharkhand, India N. Kumari · J. Uraon Birsa Agricultural University, Ranchi, Jharkhand, India H. K. Sharma ICAR-Directorate of Rapeseed-Mustard Research, Bharatpur, Rajasthan, India P. K. Ojha Acharya Narendra Deva University of Agriculture and Technology, Kumarganj, Faizabad, Uttar Pradesh, India © Springer Nature Switzerland AG 2021 H. N. Murthy, K. Y. Paek (eds.), Bioactive Compounds in Underutilized Vegetables and Legumes, Reference Series in Phytochemistry, https://doi.org/10.1007/978-3-030-57415-4_9

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Keywords

Corchorus · Dietary fiber · Malvaceae · Minerals · Nutritional value · Vitamin

1

Introduction

The genus Corchorus belongs to family Malvaceae and distributed throughout the tropical countries [1–3]. It comprises more than fifty species that locally known by various vernacular names (Table 1). All species of the genus are diploid (2n ¼ 2 ¼ 14) except C. siliquosus L., a wild species from Central America [4, 5]. Africa appears to be the primary center of diversity and origin [1, 2, 6], whereas Indo-Myanmar region identified as a secondary center of origin of the genus [3]. Young tender leaves of the genus frequently consumed as a leafy vegetable across continents [1, 7]. Morphological characters of individual plant like number of leaves, leaf area, plant height, fresh leaf weight, total plant weight, and leafy vegetable harvest index have been identified as important yield attributing traits in the genus for leafy vegetable purpose [8]. Wide range of reported genetic diversity of these component traits in jute germplasm resources of Asia [9] and Africa [10, 11] can be effectively used to realize the potential benefits of the genus as a functional food.

2

Nutritional Composition

2.1

Protein, Fatty Acid, β-Carotene, and Vitamin C

Jute leaves have significantly high (80–82%) moisture content that gives satiety to the consumers without increasing their energy intake. Fresh 100 g tender leaves contain 80–100 mg fat rich in essential fatty acids like linolenic and linoleic acids, whereas saturated fatty acids are low that help to maintain good Table 1 Vernacular names of Corchorus species Country India Bangladesh China South Africa, Nigeria Zimbabwe Egypt Botswana Japan Malaysia Philippines

Vernacular name Mithapat (C. olitorius), Teetapat (C. capsularis) Mithapat (C. olitorius), deshipat (C. capsularis) Hunag ma (C. capsularis) Jews mallow/Bush okra (C. olitorius) Derere (C. tridens) Malukhiyah (C. olitorius) Delele (C. olitorius/C. tridens) Nalta Jute (C. olitorius) Kancingbaju (C. olitorius), Rumputbayam (C. capsularis) Saluyot (C. olitorius)

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health upon consumption [12]. Among leafy vegetable, jute leaves are a good source of crude protein (3.2–4.7 g/100 g fresh weight) and supply either comparable or higher amount of dietary protein than commonly consumed leafy vegetables in rural and tribal belts of Africa as well as Asia like Spinacia oleracea (spinach) [13], Amaranthus cruentus (amaranth), Telpheria occidentalis (fluted pupkin), Celosia argentea (soko), Talinum triangulare (water leaf), Vernonia amygdalina (bitter leaf), Gongronem alatifolium (bush buck), Ocimum gratissimum (scent leaf), Piper guineense (black pepper), Basella rubra (Indian spinach) [14], Brassica rapa L. subsp. chinensis (Chinese cabbage), Solanum retroflexum (black night shade), and Cucurbita maxima (pumpkin) [15]. Usually, leafy vegetables are deficient in one or more essential amino acids but jute leaf contains almost a balanced protein rich in all the essential amino acids except marginal deficiency of methionine [16]. Therefore, jute leaves can be effectively supplement dietary protein requirement especially in developing countries where cereal-based diets dominate and populations are at the greatest risk of dietary indispensable amino acid inadequacy. Such a complementary food strategy by using protein rich food like legumes is already in practice in Latin America, Eastern Africa, Brazil, and Asia [17–19]. Further, fresh leaves of the genus are also rich in beta carotene, a pro-vitamin A carotenoid (5132–6410 μg/100 g) [15, 20–22] that aids in repairing the body’s cells and essential for vision [23]. Daily dietary intake of 90 g cooked jute leaves can meet 55% of the daily requirement of 4–8 years’ child, whereas 130 g cooked C. olitorius leaves can meet 45% of the daily requirement of 19–30 years old women, for the vitamin [15]. Fresh Corchorus leaves also contain good amount (87–94 mg/100 g) of vitamin C or ascorbic acid [24] that protects the body against cancer and other degenerative diseases such as arthritis, type II diabetes mellitus besides helping in the development of strong immune cells, connective tissue formation, healing enzymes activation, clotting prevention [14, 25]. Presence of considerable amount of vitamin C in the Corchorus spp. leaves promoted their applications in herbal medicines used for the treatment of common cold and other diseases like prostate cancer [26]. Vitamin C richness of the leaves also helps to enhance bioavailability of minerals like nonheme iron in human body either by chelating the minerals or maintaining in the reduced forms [27]. The vitamin significantly inhibits iron absorption by dietary phytates and so enhances its bioavailability [28].

2.2

Essential Minerals

Corchorus leaves are essential source of dietary minerals required for proper physiological and metabolic functions of human body. Good amount of calcium (310–586 mg /100 g fresh leaf), potassium (217.9–407.0 mg/100 g fresh weight), phosphorus (112–138 mg /100 g fresh leaf), magnesium (18.7–87.0 mg /100 g fresh leaf), and nonheme iron (6.5–7.8 mg iron/100 g fresh leaf) in the genus reported [15, 20–22, 29], subjected to genotype, soil nutrient status [30], nutrient management

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[31, 32], and leaf developmental stage at harvest [24]. Overall, minerals contents of the leaf are either comparable or better than most of the leafy vegetables like Brassica rapa L. subsp. chinensis (Chinese cabbage), Solanum retroflexum (black night shade), Cucurbita maxima (pumpkin), and Vigna unguiculata (cowpea) [13–15]. Bioavailability of dietary minerals in leafy vegetables is adversely affected by phytate [33] mediated precipitation [34]. In jute leaves, phytate content is relatively low that enhances their bio-availability [13]. In general, 90 g cooked jute leaves are sufficient to meet 27%, 44%, 29%, 24%, and 37% of the daily requirement of 4–8 years child for calcium, magnesium, copper, iron, and manganese, respectively, whereas 130 g cooked jute leaves can meet 38%, 27%, 20%, 19%, and 44% of the daily requirement of 19- to 30-year-old women for calcium, magnesium, copper, iron, and manganese, respectively [15]. These nutritional properties of jute leaves reinforce the growing awareness that underutilized leafy vegetable can contribute useful amount of essential nutrients including fatty acids, amino acids, vitamins, and dietary mineral, to human diets.

2.3

Dietary Fiber

Dietary fibers, chemically characterized as nonstarch polysaccharides, are an indigestible component of human diet that improves food ingestion by adding certain texture [14]. These fibers play protective role against some serious health problems like cardiovascular diseases, rectal cancer, obesity, and diabetes [35–38]. Jute leaves are richer in these dietary fibers (108 g/ kg fresh leaves) than most of the common leafy vegetables [15]. These fibers clean the digestive tract, remove potential carcinogens [39], and lower cholesterol load in the body. They have effective role in regulating lipid metabolism in animals including human [40, 41]. Directly these fibers lower the digestive absorption of cholesterol and increase dietary cholesterol excretion in feces as bile [40, 41]. Further, fermentation of the dietary fibers in the large intestine leads to production of short chain fatty acids like propionate, the most effective cholesterol lowering agent [42], and so reduce overall cholesterol load of the body [40, 41]. Therefore, adequate intake of jute leaf enriched with beneficial dietary fibers can lower the serum cholesterol level, risk of coronary heart disease, hypertension, constipation, diabetes, colon and breast cancer [43, 44]. Clinically, these fibers aid in suppressing blood glucose elevation probably due to delayed absorption of glucose from the intestinal membrane in the upper digestive tract [45]. Due to these, intrinsic nutraceutical properties of jute leaves have been an integral component of poor man’s healthy diet across continents.

2.4

Culinary Advantages

Jute leaves have unique culinary advantage due to presence of mucilage that aids in making sauces while consuming along with coarse starchy foods. These proteinaceous molecules [46] appear as a gum like substances and are rich in uronic

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acid (65%) that consist of rhamnose, glucose, galactouronic acid, and glucuronic acid in a molar ratio of 1.0:0.2:0.2:0.9:1.7 in addition to the acetyl (3.7%) group [47]. The mucilage has ability to buffer excess acid, acts as a natural laxative, and protects the sensitive intestinal lining and improves regularity without side effects. The yield of this hydrocolloid from jute leaves has been estimated to be as high as 4.5% (w/w) based on dry mass [48]. Table 2 presents the comparative nutritional content of the leaves of different Corchorus spp. [20]. With the emerging worldwide interest in botanicals with pharmaceutical properties, the evaluation of the Corchorus spp. is essential. These leaves are a time honored medicinal vegetable in North Africa and East and Southeast Asia. Comprehensive details of known phytochemicals of the genus with their respective biological activities were mentioned in Table 3. Detail medicinal role of the genus was elaborated by Kumari et al. [49]. In addition, the genus is gaining importance due to antitoxicological effects. Exposure to environmental contaminants like dioxins can cause serious toxicological effects such as tumor promotion, immune toxicity, lethality, and so on [56]. Most of these responses expressed through interaction between dioxins

Table 2 Nutrient composition of Corchorus species leaves [20] Corchorus species C. olitorius C. capsularis C. trilocularis C. fascicularis C. aestuans C. tridens

Protein (%) 3.2 3.8 3.6 3.8 3.7 3.7

Iron (mg/ 100 g dry matter) 8.3 7.1 5.4 5.8 18.2 6.9

Potassium (mg/100 g dry matter) 426 405 387 390 401 384

Vitamin A (mg/100 g dry matter) 8.1 6.1 3.6 6.3 7.7 4.8

Leaf area (cm2) 17.8 13.4 5.1 6.9 8.1 3.9

Foliage yield (q/ha) 1.7 1.4 0.6 0.7 0.9 0.4

Table 3 Biological activities of phytochemicals found in Corchorus species Chemical compound Strophanthidin, Corchoroside Corchorol, Capsularo Corchorusosides Cordepressic acid Corchoionosides

Corchorus species C. olitorius, C. capsularis

C. olitorius C. depressus, C. olitorius

Biological actions Digitalis genins like effect on cardiac activities

References [50–52]

Inhibitory action against Na, K-ATPase Antipyratic activity on yeast induced pyrexia of mouse Inhibit histamine release from mouse peritoneal exudates cell induced by antigenantibody reaction

[53] [54] [55]

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and aryl hydrocarbon receptor (AhR) and its subsequent transformation [57]. In vitro study on rat revealed that ethanol extract of C. olitorius can effectively suppress transformation of AhR probably due to presence of some AhR antagonistic bioagents [58]. These protective effects of Corchorus spp. leaves on metal toxicity are mentioned in Table 4. There are some concerns on possible presence of antinutrients such as oxalate [63] and phytic acid [64] in leafy vegetables. Agbaire et al. [65] reported very low levels of these antinutrients in Corchorus spp. Further, Ndlovu and Afolayan [13] revealed that the nutritional qualities of the genus are better than popular leafy vegetables like spinach particularly due to lower phytate content. Further, available toxicological data are although limited, but in support of the assessment [66–68]. Table 4 Protective effects and mechanism of Corchorus spp. leaves on metal toxicity Toxic metal Mycotoxin (Aflatoxin B1 Fumonisin B1) Lead

Administered form C. olitorius aqueous extract (20 or 40 μg/mL)

Phytochemical Flavonoids and chlorophyll

Animal model Rat hepatoma cells (H4IIEluc)

Protective mechanisms Reduce damage to DNA through antioxidant activities Free radical scavenging through a flavonoids and phenolic redox cycle that reduce oxidative damage to cellular DNA and cell membrane lipid Up-regulation of mitochondrial signaling proteins, namely, Bad, NF-jB, caspase 3, and caspase 9, and down-regulation of Bcl-2 involves in cellular apoptotic pathway Protective effect against sodium arsenate induced hepatic and renal oxidative damages

C. olitorius aqueous extract (14.4%) (w/w)

Phenolic compounds and flavonoids

Two- to threemonth-old Wistar rats (200  20 g)

Cadmium

C. olitorius aqueous extract (14.4%) (w/w)

Rutin, quercetin, gallic acid, chlorogenic acid, p-cumaric acid, ferulic acid and ellagic acid, ascorbic acid, and α-tocopherol

Adult male Swiss albino mice (25  5 g) and male Wistar rats (150  20 g)

Arsenic

C. olitorius aqueous extract (14.4%) (w/w)

Phyto-phenolics

Thirty male (age: 2– 3 months) Wistar rats weighing 180–200 g

Ref [59]

[60]

[61]

[62]

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Conclusion

In nutshell, Corchorus species is a rich source of health promoting nutrients without any significant antinutritional factors. The available information on Corchorus spp. reinforced traditional application of the genus to enhance vigor and strength beside inspiring for elaborate chemical profiling of the plant extracts, its standardization and understanding biological role of principal compound(s). These endeavors will lead to realize commercial potential of the genus as a healthy botanical.

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Bioactive Compounds of Ceylon Spinach [Talinum Triangulare (Jacq.) Willd.] Bioactive Compounds of Ceylon Spinach Kandikere Ramaiah Sridhar and Mundamoole Pavithra

Contents 1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 Nutraceutical Perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1 Proximal Qualities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Minerals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3 Amino Acids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4 Fatty Acids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 Bioactive Potential . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1 Bioactive Components . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 Vitamins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3 Antioxidant Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 Pharmaceutical Properties . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1 Anemia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2 Diabetes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3 Hepato- and Neuro-disorders . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4 Cardiovascular Diseases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5 Other Ailments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 Conclusions and Prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

152 153 153 154 156 156 157 157 159 161 162 162 163 163 163 164 164 165

Abstract

Leafy vegetables are dominant source of nutrition as well as therapeutic potential such as proteins, minerals, amino acids, fatty acids, vitamins, and bioactive components. Talinum spp. are wide spread globally and utilized for nutritional, K. R. Sridhar (*) Centre for Environmental Studies, Yenepoya (deemed to be) University, Mangalore, Karnataka, India Department of Biosciences, Mangalore University, Mangalagangotri, Mangalore, Karnataka, India M. Pavithra Department of Biosciences, Mangalore University, Mangalore, Karnataka, India © Springer Nature Switzerland AG 2021 H. N. Murthy, K. Y. Paek (eds.), Bioactive Compounds in Underutilized Vegetables and Legumes, Reference Series in Phytochemistry, https://doi.org/10.1007/978-3-030-57415-4_10

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medicinal, and ornamental purposes. Talinum triangulare (Jacq.) Willd. is a tropical cosmopolitan leafy vegetable commonly called Ceylon spinach, a wellknown vegetable in Africa, America, and Asia. This review provides a cross section of nutraceutical potential and bioactive attributes of T. triangulare. Being traditionally used, T. triangulare possess several health benefits to combat anemia, diabetes, hepato-disorders, neuro-disorders, cardiovascular diseases, and other ailments. Although T. triangulare is well-known traditionally for its versatility of nutrition and medicinal values, it has been neglected as a useless weed. This leafy vegetable is capable to safeguard its nutraceutical and medicinal attributes in spite of oven-drying at 60 °C without substantial loss which is an added advantage for industrial applications. Further insight on the mucilage and pigments of T. triangulare will open up new avenues in food, health, and pharmaceutical industries. Keywords

Bioactive principles · Leafy vegetables · Lifestyle diseases · Nutraceuticals · Pharmaceuticals

1

Introduction

The genus Talinum (family, Portulacaceae) is well-known for its edible and medicinal properties consisting of 15 species with wide geographic distribution [1]. Kumar and Prasad [2] reported the geographical distribution of eight Talinum species, namely, T. calcaricum, T. calycinum, T. cuneifolium, T. mengesii, T. paniculatum, T. parviflorum, T. teretifolium, and T. triangulare occurring in Africa, America, Arabia, India, Japan, and Trinidad. All these species are used as ornamentals, two species each as vegetables (T. cuneifolium and T. triangulare) and two species for medicinal purposes (T. cuneifolium and T. paniculatum). Among the three Talinum spp. reported from India (T. cuneifolium, T. portulacifolium, and T. triangulare), the T. triangulare is one of the major green leafy vegetables. It is native to the tropical America and also grown in the West Africa, Southeast Asia, and warmer parts of North and South Americas, while it is also a major leafy vegetable in Nigeria [3]. This plant species was first introduced into the southern parts of India from Sri Lanka and cultivated in Tamil Nadu as Ceylon spinach [4]. It has been domesticated, diversified, and used extensively as leafy vegetable in Sri Lanka [5]. Plants of T. triangulare are erect and branched and grow about 50–100 cm height; stem is succulent, triangular, and green or purple at the base and possesses swollen tap root system; leaves are simple, sessile, alternate, and succulent; flowers are purple and bisexual and produce globose dehiscent fruits with many seeds (Fig. 1). This chapter provides the nutraceutical properties, bioactive potential, and pharmaceutical values of the T. triangulare grown and used as vegetable and medicinal purposes in different geographical regions.

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Fig. 1 Group of Talinum triangulare grown in an organic farm (a), leaf pattern (b), inflorescence (b, c) and root system (d) (scale bar, 1 cm)

2

Nutraceutical Perspectives

2.1

Proximal Qualities

Nutritional qualities of T. triangulare have been evaluated from Côte d’Ivoire, Ghana, India, and Nigeria (Table 1). Several studies are available from the Nigerian region. The carbohydrate content is highest in all studies followed by protein content. Substantial quantity of fiber is present (2–14.1%) followed by lipid component (0.7–8.6%). Carbohydrate serves as a major energy source along with proteins, which is almost equivalent to the edible pulses in almost all studies. Similarly, the high fiber content with low total lipids is the suitable traits for human diet. Different parts of T. triangulare (leaf, stem, and root) showed difference in proximal components [14]. The stem consists of high amount of crude protein, total lipid, and ash contents than the leaf and root part. Adetuyi and Dada [15] evaluated nutritional composition of mucilage of T. triangulare and found highest quantity of crude protein (54.3%) followed by total lipids (29%), ash (7.8%), carbohydrates (5.4%), and crude fiber (3.5%).

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Table 1 Nutritional composition Talinum triangulare from different regions (% dry mass) Côte d’Ivoire Ghana India India Nigeria Nigeria Nigeria Nigeria Range

Protein 17.2 27.6 19.2 30.9 18.1 32.4 25.4 13.2 13.2–32.4

Carbohydrate 52.8 – – 38.2 61.7 28.9 46.7 58.1 28.9–61.7

Lipid 4.9 – 6.7 4.3 4.4 5.0 8.6 0.7 0.7–8.6

Fiber 13.9 – 7.0 14.1 2.0 6.2 4.2 13.6 2–14.1

Reference [6] [7] [8] [9] [10] [11] [12] [13]

Processing methods influence the proximate composition of leafy vegetables. Cooking of T. triangulare decreased the amount of total lipids (1.14 vs. 1.08%) and ash (1.8 vs. 1.5%), while increased the crude fiber (3.3 vs. 3.5%) in Nigeria [16]. Oluwalana et al. [11] from Nigeria reported the effect of sun-drying as well as different oven-drying temperatures (60, 70, and 80 °C) on proximal components of T. triangulare. The sun-dried samples showed high carbohydrate content, total lipids, crude fiber, and ash, while the crude protein attained the highest level in ovendried sample at 60 °C. The pressure-cooked samples of T. triangulare showed significantly high quantities of total lipids, crude fiber, and carbohydrates than the uncooked samples [9]. Applications of different fertilizers influence the nutritional values of T. triangulare in Nigeria [10]. Increase in carbohydrates and total lipid contents with decrease in crude protein content were seen across the rates of various fertilizer applications. Andarwulan et al. [17] reported the impact of organic and conventional fertilizers on the dietary fiber contents of T. triangulare in different seasons. This study showed that the conventional samples contain higher dietary fiber than the organically fertilized samples except for pectic substances in the dry season. The soluble dietary fiber content was high especially in the dry season. Different tribes in the Wayanad district (Kerala, India) consume about 13 wild leafy vegetables, among them Talinum portulacifolium is widely consumed [18]. It possesses moderate amount of crude protein, fiber, and total lipid contents with several minerals [18]. The same leafy vegetable collected from Thrissur (Kerala, India) also endowed with minerals like calcium, magnesium, phosphorus, potassium (dominant), and sodium [18, 19]. Another species, the Talinum fruticosum, in Ghana possess high amount of carbohydrates (68.2%), crude protein (18.1%), crude fiber (6%), and low total lipids (0.9%) [20].

2.2

Minerals

Assessment of mineral composition in T. triangulare (Côte d’Ivoire, Ghana, India, and Nigeria) also showed a slight variation between geographic locations (Table 2).

NRC-NAS (children) NRC-NAS (adults)

Côte d’Ivoire Ghana Ghana India Nigeria Nigeria Range

Na 2.6 – 0.02 0.5 0.4 – 0.022.6 0.12–0.4 0.5

K 50.5 – 8.93 132.4 0.3 – 0.3132.4 0.5–1.6 1.6–2

Ca 6.0 – – 12.2 0.1 0.8 0.112.2 0.6–0.8 0.8 0.0003–0.003 0.002–0.005

Mn – – – 1.7 – – 1.7

Table 2 Mineral components of Talinum triangulare (mg/g dry mass)

0.01 0.01–0.02

Fe 1.0 0.3 0.1 4.4 0.04 0.04 0.04–4.4 0.005–0.01 0.012–0.015

Zn 0.4 – 0.2 0.5 0.1 0.2 0.1–0.5

Mg 7.6 – 0.3 19.9 0.1 0.8 0.119.9 0.06–0.8 0.8

P 2.4 0.8 – 4.6 0.1 1.3 0.14.6 5–8 8

Ratio Na/K 0.05 – 0.002 0.004 1.3 – 0.0021.3

Ca/P 2.5 – – 2.7 1.0 0.6 0.62.7

[24] [24]

Reference [6] [21] [7] [9] [22] [23]

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The potassium content is highest followed by magnesium, calcium, phosphorus, iron, and sodium. Except for the iron and phosphorus, the rest of the minerals fulfill NRC-NAS pattern for children as well as adults NRC-NAS [24]. Except for one study, the ratio of Na/K is 1. The low Na/K (1) combats loss of calcium in urine as well as restores calcium in bones (Shills and Young) [26]. Calcium is well-known for its involvement in development of bones; thus it protects from rickets as well as osteoporosis [27]. The high magnesium content is responsible to combat coronary diseases as well as stroke. Adetuyi and Dada [15] evaluated the mucilage of T. triangulare for mineral constituents and found the highest quantity of calcium (78.8 ppm) followed by magnesium (27.5%), iron (11.9%), and zinc (0.8%). Different drying methods (sun-drying, shade-drying, cabinet-drying, and microwave-drying) also showed increased mineral contents of T. triangulare than the fresh samples [28]. This study also showed that the rich mineral contents of T. triangulare are responsible to enhance the shelf life (up to 6 months) by cabinet- and microwavedried than the sun-dried and shade-dried samples. Processing method especially cooking decreased the contents of minerals (calcium, iron, magnesium, phosphorus, and zinc) of T. triangulare in Nigeria [23]. Pressure-cooked samples of T. triangulare drastically decreased the minerals than uncooked samples probably due to mineral drain indicating necessity of suitable methods to avoid mineral loss [9].

2.3

Amino Acids

Among the indispensable amino acids in T. triangulare, lysine and leucine were dominant, whereas among the dispensable amino acids, glycine was dominant (Table 3). Expect for threonine, tryptophan, and valine, the rest of the dispensable amino acids are comparable or surpassed the FAO-WHO recommended pattern [29]. According to Omoyeni et al. [30], T. triangulare in Nigeria consisted of a total of 17 amino acids (essential amino acids, histidine, isoleucine, leucine, lysine, methionine, cystine, phenylalanine, tyrosine, threonine, and valine; dispensable amino acids, alanine, arginine, glycine, aspartic acid, glutamic acid, proline, and serine) with glutamic acid as the dominating amino acid. Fasuyi [22] reported presence of tryptophan also in T. triangulare collected from Nigeria, which is not present in Nigerian and Indian samples. Pressure-cooking of T. triangulare resulted in significant increase of histidine, isoleucine, leucine, phenyl alanine, and valine, while the lysine, methionine, cystine, and tyrosine were significantly high in uncooked samples [9].

2.4

Fatty Acids

Sridhar and Lakshminarayana [31] documented different classes of lipids in six edible leafy vegetables from Hyderabad (India) with a variety of fatty acids in

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Table 3 Amino acid profile of Talinum triangulare (g/100 g protein) from [9] Indispensable amino acids Histidine Isoleucine Leucine Lysine Methionine Cystine Phenyl alanine Tyrosine Threonine Tryptophan Valine Dispensable amino acids Alanine Aspartic acid Arginine Glycine Glutamic acid Proline Serine a

India 1.9 5.0 7.3 13.0 2.4 0.2 3.8 3.7 4.3 – 5.0

FAO-WHO [29] 1.9 2.8 6.6 5.8 2.5a 6.3b 3.4 1.1 3.5

7.5 7.5 6.2 10.9 9.8 5.4 4.6

Met+Cys Phe + Tyr

b

T. triangulare (saturated fatty acids, capric, lauric, myristic, palmitic, and stearic acids; unsaturated fatty acids, oleic, linoleic, and linolenic acids). In addition to the fatty acids, it also consisted of ɑ-tocopherol. Pavithra [9] reported palmitic acid as a major saturated fatty acid while linoleic acid as a major unsaturated fatty acid in T. triangulare. Pressure-cooking significantly increased the palmitic acid in T. triangulare, while the linoleic acid was significantly high in uncooked samples [9].

3

Bioactive Potential

3.1

Bioactive Components

Bioactive compounds of T. triangulare have been assessed from Côte d’Ivoire, India, Indonesia, and Nigeria (Table 4). The qualitative analysis of T. triangulare showed higher number of phytochemicals in aqueous extract than the methanol extract (alkaloid, cardiac glycoside, flavonoids, phenol, phlobatannins, saponins, and tannins) [38]. The total phenolic content was also higher in aqueous extract compared to methanol extract (0.5 vs. 0.3 mg/g), but inhibition of the lipid peroxidation was higher in methanolic extract than the aqueous extract (74 vs. 72%). The qualitative analysis of phytochemicals in different extracts of T. triangulare collected

Côte d’Ivoire India India Indonesia Nigeria Nigeria Nigeria Nigeria Nigeria Nigeria Nigeria Range

Total phenolics 1.5 0.3 5.0 – – – – 1.5 0.001 – 0.2 0.001–5

Flavonoids – 0.2 0.07 0.04 – – 0.7 0.1 0.03 0.3 2.4 0.03–2.4

Phytates 0.3 – 0.06 2.5 – – – – – – 0.06–2.5

Tannins – – 0.4 0.6 – 0.01 – 0.002 0.7 2.7 0.002–2.7

Table 4 Bioactive components of Talinum triangulare (mg/g dry mass) Alkaloid – 0.6 – – – – 0.6 – 0.01 0.4 3.8 0.01–3.8

Saponin – – – – – – 0.02 – 0.04 0.8 6.2 0.02–6.2

Reference [32] [4] [9] [33] [34] [35] [36] [37] [10] [23] [13]

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from Chennai (India) showed the presence of alkaloids, saponins, steroids, and terpenoids in hexane extract; presence of flavonoids, saponins, steroids, and terpenoids in chloroform extract; presence of alkaloids, flavonoids, saponins, tannins, steroids, and terpenoids in ethyl acetate extract; and presence of alkaloids, flavonoids, saponins, tannins, and terpenoids in methanol extract [4]. The T. triangulare from Nigeria consisted of good quantities of phytic acid (250 mg/100 g), oxalate (110 mg/100 g), and tannin (62 mg/100 g) [34]. The T. triangulare from Nigeria also showed high quantity of vitamin C (116 mg/100 g) and moderate amount of total phenolics (22 mg/100 g) [35]. Adetuyi and Dada [15] evaluated the mucilage of T. triangulare for bioactive component and found the highest quantity of tannins (50 mg/100 g) followed by saponins (9.3 g/100 g) and phytate (2.4 mg/100 g). Based on the assessment of bioactive components in T. triangulare from Nigeria, Okpalanma and Ojimelukwe [39] recommended its use to fulfill the nutritional requirements of children as well as adults. Adefegha and Oboh [37] from Nigeria studied the impact of cooking methods on bioactive compounds and reported the enhancement of total phenolics and antioxidant activities of tropical green leafy vegetables by steam-cooking. This study showed the loss up to 64% of vitamin C in T. triangulare on cooking, while cooking gained 86% of total phenolics, and 57% of flavonoid contents resulted in increased antioxidant potential (DPPH and ABTS radical-scavenging activities). However, the domestic cooking of T. triangulare from Nigeria showed decreased bioactive components (vitamin C, carotenoids, tannin, alkaloid, flavonoids, sterol, and saponin) with low antioxidant activity (DPPH radical-scavenging) [40]. Cooking of T. triangulare for 15, 25, and 45 min resulted in decreased oxalate, phytate, vitamin C, polyphenols, carotenoids and antioxidant activity as reported from the Southern Côte d’Ivoire [32]. The impact of inorganic and organic fertilizers on T. triangulare (NPK, pig manure, and chicken manure) showed the presence of saponins, tannins, flavonoids, phenols, and alkaloids [10]. This study concluded that the fertilizer applications may not have strong influence on phytochemical components. Planting and harvesting seasons (winter and summer) and time (30 and 60 days) influenced the polyphenol content and antioxidant activity of T. triangulare [41]. The production of polyphenol was highest in winter planting and harvesting at 30 days, while the antioxidant activity (DPPH free-radical method) also followed the same trend.

3.2

Vitamins

The content vitamins in T. triangulare have been evaluated from Côte d’Ivoire, India, and Nigeria (Table 5). Vitamin C content was predominant compared to other vitamins followed by carotenoids, tocopherol, niacin, riboflavin, and thiamin. Waterand fat-soluble vitamins play a key role in several body functions of human beings [16]. The riboflavin is involved in carbohydrate metabolism as well as regulatory functions of hormones; niacin is helpful for normal functioning of the skin, intestinal tract, and nervous system; tocopherol and vitamin C act as powerful antioxidants.

Côte d’Ivoire India Nigeria Nigeria Nigeria

Thiamin – – – – 0.03

Riboflavin – – – – 0.17

Niacin – – – – 0.45

Table 5 Vitamin content of Talinum triangulare (mg/100 g dry mass) Tocopherol – – – – 22.7

Vitamin C 50 13.5 120 550 49.0

Carotenoids 2.0 – – – 264.6

Reference [6] [42] [35] [37] [16]

160 K. R. Sridhar and M. Pavithra

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Carotenoids are antioxidants play a major role in human health by preventing several diseases (e.g., cancer, vision-related ailments, cardiovascular diseases, and infertility) [16, 23]. The vitamin C as an antioxidant plays significant role in heart health. A review by Moser and Chun [43] provides a detailed account on the role of vitamin C in protection of heart health and its action against cardiovascular diseases and atherosclerosis. Babalola et al. [44] reported the impact of different processing methods (sundrying, blanching, boiling, squeeze-washing, and squeeze-washing with salt and squeeze-washing + boiling) on vitamin C content of T. triangulare in comparison with fresh samples. Methods of drying like sun-drying and oven-drying at different temperatures (60, 70, and 80 °C) showed differences in vitamin C content of T. triangulare [11]. Fresh samples showed the highest amount of vitamin C followed by sun-dried and temperature-treated samples (60, 70, and 80 °C). A study from Nigeria revealed higher thiamine, riboflavin, niacin, tocopherol, vitamin C, and carotenoid contents in T. triangulare in uncooked than cooked samples [16].

3.3

Antioxidant Activity

Many studies have been carried out on the antioxidant activity of T. triangulare from India, Indonesia, Malaysia, Nigeria, and Taiwan. Uncooked samples of T. triangulare from India showed high ferrous ion-chelation capacity, while the cooked samples showed high total antioxidant activity as well as DPPH radical-scavenging activity [42]. From Indonesia samples of T. triangulare endowed with several bioactive components such as total phenolics and flavonoids (apigenin, kaempferol, luteolin, myricetin, and quercetin) with good antioxidant potential (ABTS and DPPH radical-scavenging activities; ferric ion-reducing power; inhibition of lipid peroxidation) [33]. The T. triangulare collected from Malaysia showed appreciable quantity of total phenolic content (164.4 mg/g) as well as the DPPH radicalscavenging potential [45]. The HPLC analysis of flavonoids revealed presence of catechin, epicatechin, kaempferol, myricetin, and quercetin. A study from Nigeria on T. triangulare reported high quantity of flavonoids (81.5 mg/g), total phenolics (49.3 mg/g), and vitamin C (29.3 mg/g) with high DPPH radical-scavenging activity (22.2%) [46]. In another study, the T. triangulare from Nigeria showed low amount of total phenolics (9 mg/g), flavonoids (7 mg/g), and flavonol (5.3 mg/g), which resulted in low DPPH radical-scavenging activity (2.3%) [47]. Different extracts of T. triangulare from Taiwan showed presence of various flavonoids (diosmin, hesperisin, hesperetin, naringin, and quercetin) and phenolic compounds (caffeic acid, catechin, chlorogenic acid, ferulic acid, gallic acid, protocatechuic acid, and vanillic acid) with high antioxidant potential (reducing power, ferrous-ion chelating ability, DPPH radical-scavenging activity, and Trolox-equivalent antioxidant capacity) in various extracts [48]. It is known that different extracts of the leafy vegetables influence the quantity of bioactive components as well as extent of antioxidant activities. The ethanol extract of T. triangulare showed high total phenolics, while ethyl acetate extract

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showed high flavonoid contents [49]. Antioxidant activities like ferric-reducing antioxidant potential (FRAP) was higher in ethyl acetate as well as aqueous extracts; the DPPH radical-scavenging activity was high in ethyl acetate extract followed by ethanol extract; the hydroxyl radical-scavenging ability was high in aqueous extract, and ferrous ion-chelation capacity was high in ethyl acetate extract. The ethyl acetate extract fraction of T. triangulare showed significantly increase in phenolic content with increased antioxidant activity [50]. It also showed in vitro ferrous ion-induced lipid peroxidation in selected tissue homogenates in albino rats.

4

Pharmaceutical Properties

The subtopics discussed above provide an insight that T. triangulare possesses many versatile bioactive components in addition to nutritionally valued constituents, which are capable to combat human lifestyle diseases like anemia, diabetes, gastrointestinal disorders, and cardiovascular diseases. Polyphenols in T. triangulare provide many health benefits by different mechanisms like elimination of free radicals, protection from generation of dietary antioxidants, and chelation of prooxidant metals [51]. Tannins in T. triangulare possess potent antioxidant activity, which is effective against cancer, neuropathy, and cardiovascular diseases [52]. Since T. triangulare possess flavonoids, tannins, and saponins, capable to combats diabetes, shows hypoglycemic activity and lowers the cholesterol level, respectively [23]. The phytic acid in T. triangulare has the capability to bind with proteins by forming phytate-protein complex, which affects the digestibility of proteins through inhibiting a number of digestive enzymes (e.g., pepsin) [34]. Liao et al. [48] evaluated the extracts of T. triangulare and found immunomodulatory effects through secretion of cytokines leading to combat infectious, degenerative, autoimmune diseases, and tumors.

4.1

Anemia

The oral administration of methanol extract of T. triangulare to experimental rats showed the improvement of serum RBC level without affecting serum urea and creatinine [53]. This shows that the erythropoietin-promoting activity of the plant extract is useful in management of anemia as well as kidney-related ailments. The oral intake of methanolic extract of T. triangulare leaves at different doses (100, 200, and 400 mg/kg) showed dose-dependent suppression of oxidative damage in the liver cells as well as significant increase in the levels of serum aspartate amino transferase and RBC in adult albino rats [54]. Thus, the T. triangulare could be used for treatment of anemia as well as to boost the blood level in children and pregnant women. Adetuyi and Dada [15] evaluated the mucilage of T. triangulare for mineral constituents and found adequate quantity of iron (11.9%) which is important to combat anemia.

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163

Diabetes

The polysaccharides extracted from T. triangulare showed a high hypoglycemic effect in streptozotocin-induced type 2 diabetic male mice indicate antidiabetic function [55]. The methanolic extract of T. triangulare leaves showed antihyperglycemic activity in streptozotocin-induced diabetic rats [3]. It also found to be effective in managing the other complications associated with diabetes like hyperlipidemia as well as defect in lipid metabolism. Similarly, the methanol extract of leaves of Talinum portulacifolium showed a significant and consistent antihyperglycemic activity against alloxan-induced diabetic rats [56]. The hexane extract of leaves of T. portulacifolium showed significantly higher antihyperglycemic activity than an oral hypoglycemic agent (glibenclamide) in streptozotocin-induced (STZ) diabetic rats [57]. The ethanolic extract of T. portulacifolium and nano-formulation (T-SLN) at a dose of 250 mg/kg showed significant antidiabetic activity in STZ and high fat diet-induced diabetic rats [58]. Thus, T. triangulare also possess similar properties to combat diabetes.

4.3

Hepato- and Neuro-disorders

The polysaccharides extracted from T. triangulare showed hepatoprotective activity in vivo against carbon tetrachloride-induced liver damage in mice [59]. A study on the aqueous extract of leaves of T. triangulare on the activities of enzymes (aspartate amino-transaminase, alanine amino-transaminase, and alkaline phosphatase) in serum and tissue homogenates (liver, kidney, and brain) of albino rats exhibited that the extract is biologically active and it could serve as a potent remedy against hepatocellular injuries as well as inflammation [60]. In some part of southwest Nigeria, the leaves of T. triangulare are used against neurodegenerative disorders [61]. The treatment with 300 and 400 ml T. triangulare leaf extract showed the best weight gain, feed-conversion ratio, and improved immunity against Newcastle disease virus in broiler chickens [62]. Leaf meal prepared out of T. triangulare showed good performance without deleterious effect in broiler chickens in Ibadan, and it was a cost-effective replacement of other feeds especially soya bean meal and ground nut cake [63].

4.4

Cardiovascular Diseases

According to Aja et al. [36], the T. triangulare possess medicinal potential in manage cardiovascular diseases especially stroke and obesity. It possesses cardioprotective and hypolipidemic effects owing to presence of squalene in leaves [64, 65]. Tender leaves and stem of T. triangulare are used as potential vegetable possessing adequate quantity of fiber; its significant increase on cooking will be immense value for patients suffering from cardiovascular problems. Magnesium is known as an essential mineral prevents diseases like cardiomyopathy, bleeding disorders, and ischemic

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heart ailment [66, 67]. The ω-3 and ω-6 fatty acids in foodstuffs have the capacity to combat heart diseases [68–70]. In uncooked and cooked T. triangulare, presence of linoleic as well as α-linolenic acids, respectively, is an added advantage in disease prevention [9]. In addition, increased ratio of polyunsaturated/saturated fatty acid on cooking T. triangulare facilitates to combat cardiovascular risks.

4.5

Other Ailments

Traditionally in Nigeria, the leaves of T. triangulare ground and the paste are applied to cure boils [71]. The aqueous root extract of T. triangulare showed anti-diarrheal effects against castor oil-induced diarrhea in rat model [72]. The hydroalcoholic extracts of T. triangulare showed potent cholesterol-lowering effects, which is greater than the nicotinic acid and atorvastatin [73]. Satyanarayana et al. [74] also reported the analgesic activity of Talinum portulacifolium. The methanolic extract of T. portulacifolium roots showed analgesic properties at the dose of 2 g/kg in experimental Swiss albino mice.

5

Conclusions and Prospects

The T. triangulare is a tropical cosmopolitan leafy vegetable well-known for its nutritional and health benefits in Southwestern India. The leaves are endowed with a variety of bioactive compounds responsible for antioxidant activities. Several components in the leaves such as phenolics, flavonoids, vitamin C, and phytic acid are known for its versatility, in turn helping to control, treat, and manage coronary heart diseases. This leafy vegetable also possesses several nutritionally beneficial components (e.g., protein, fiber, minerals, and essential fatty acids); thus there is a wide scope to utilize as nutraceutical resource. Owing to presence of multifunctional nutraceutical components, it will serve as a potent source of health food. Liao et al. [48] based on bioactive components in the extracts of T. triangulare considered its use as health food with immunomodulatory impacts. Ikewuchi et al. [75] assessed the aqueous extract of T. triangulare leaves in Nigeria and found 10 known carotenoids, 6 hydroxycinnamates, 8 lignans, and 30 flavonoids. In Nigeria, T. triangulare is used intensively as part of savory dishes with salt [76]. Interestingly, oven-drying of leaves at 60 °C has not resulted in substantial loss of nutritional and sensory properties and opens up avenues for several industrial applications [11]. The leaves and stem of T. triangulare produce a lot of mucilage; a study in Nigeria showed potent antioxidant activities of mucilage (FRAP and DPPH radical-scavenging potential) [15]. The hydromethanolic extract of stem of T. triangulare consisted of phenolic compounds with high antioxidant potential [77]. Future studies should focus to support the specific bioactive component and the optimum dose necessary in relation to age, sex, status of health, and other relevant parameters to prove its efficiency in control or treatment of coronary heart diseases. For instance, among flavonoid classes, only two are involved in lowering mortality

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by coronary heart disease (flavonol and flavone) [78]. Similarly, betalain pigment classes (produced during extreme environmental conditions in stem, leaf and flowers) in T. triangulare are known for radical-scavenging activity [79]. The betalain pigments are also potential interest in production of natural food colors; beverages have dual advantages as antioxidants and also useful in management of cardiovascular diseases.

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40. Ogungbenle HN, Otemuyiwa FF (2015) Food properties and amino acid composition of Celosia spicata leaves. Adv Anal Chem 5:1–7 41. Brasileiro BG, Leite JPV, Casali VWD, Pizziolo VR, Coelho OGL (2015) The influence of planting and harvesting times on the total phenolic content and antioxidant activity of Talinum triangulare (Jacq.) Willd. Maringá 37:249–255 42. Pavithra M, Sridhar KR, Greeshma AA (2017) Bioactive attributes of traditional leafy vegetable Talinum triangulare. In: Watson RR, Zibadi S (eds) Handbook of nutrition in heart health. Wageningen Academic Publishers, Netherlands, pp 357–372 43. Moser MA, Chun OK (2016) Vitamin C and heart health: a review based on findings from Epidemiologic studies. Int J Mol Sci 17:1–9 44. Babalola OO, Tugbobo OS, Daramola AS (2010) Effect of processing on the vitamin C content of seven Nigerian green leafy vegetables. Adv J Food Sci Technol 2:303–305 45. Mustafa RA, Hamid AA, Mohamed S, Bakar FA (2010) Total phenolic compounds, flavonoids, and radical scavenging activity of 21 selected tropical plants. J Food Sci 75:C28–C35 46. Olajire AA, Azeez L (2011) Total antioxidant activity, phenolic, flavonoid and ascorbic acid contents of Nigerian vegetables. Afr J Food Sci Technol 2:22–29 47. Ademoyegun OT, Akin-Idowu PE, Ibitoye DO, Adewuyi GO (2013) Phenolic contents and free radical scavenging activity in some leafy vegetables. Int J Veg Sci 19:126–137 48. Liao DY, Chai YC, Wang SH, Chen CW, Tsai MS (2015) Antioxidant activities and contents of flavonoids and phenolic acids of Talinum triangulare extracts and their immunomodulatory effects. J Food Drug Anal 23:294–302 49. Afolabi OB, Oloyede OI (2014a) Antioxidant properties of the extracts of Talinum triangulare and its effect on antioxidant enzymes in tissue homogenate of Swiss albino rat. Toxicol Int 21:307–313 50. Afolabi OB, Ibitayo AO, Jaiyesimi KF, Olayide II, Adewumi DF (2016) Inhibitory effect of ethyl acetate fraction of Talinum triangulare (Jacq.) Willd. on Fe2+ induced lipid peroxidation in albino rat tissue homogenates - in vitro. Pharmaceut Chem J 3:120–124 51. Lima GPP, Vianello F, Corrêa CR, Campos RADS, Borguini MG (2014) Polyphenols in fruits and vegetables and its effect on human health. Food Nutr Sci 5:1065–1082 52. Ghosh D (2015) Tannins from foods to combat diseases. Int J Pharma Res Rev 4:40–44 53. Ezekwe CI, Ikechukwu OJ, Okechukwu UPC, Ezea SC (2013) The effect of methanol extract of Talinum triangulare on some selected haematological and kidney parameters of experimental rats. World J Pharm Pharmaceut Sci 2:4383–4396 54. Ezekwe CI, Chidinma RU, Okechukwu PCU (2013) The effect of methanol extract of Talinum triangulare (waterleaf) on the hematology and some liver parameters of experimental rats. Global J Biotechnol Biochem 8:51–60 55. Xu W, Zhou Q, Yin J, Yao Y, Zhang J (2015) Anti-diabetic effects of polysaccharides from Talinum triangulare in streptozotocin (STZ)-induced type 2 diabetic male mice. Int J Biol Macromol 72:575–579 56. Rao TN, Kumarappan CT, Lakshmi MS, Subhash CM (2007) Antidiabetic activity of leaves of Talinum portulacifolium (Forssk) in alloxan-induced diabetic rats. Pharmacol Online 2:407–417 57. Babu RK, Vinay K, Sameena SK, Prasad SV, Swapna S, Rao AC (2009) Antihyperglycemic and antioxidant effects of Talinum portulacifolium leaf extracts in streptozotocin diabetic rats: a dose-dependent study. Pharmacog Mag 5:1–10 58. Bindu RH, Lakshmi SM, Himaja N, Nirosha K, Pooja M (2014) Formulation, characterization and antidiabetic evaluation of Talinum portulacifolium (Forssk.) loaded solid lipid nanoparticles in streptozotocin and high fat diet induced diabetic rats. J Global Tr Pharmaceut Sci 5:2108–2114 59. Liang D, Zhou Q, Gong W, Wang Y, Nie Z, He H, Li J, Wu J, Wu C, Zhang J (2011) Studies on the antioxidant and hepatoprotective activities of polysaccharides from Talinum triangulare. J Ethnopharmacol 136:316–321 60. Afolabi OB, Oloyede OI (2014b) Effects of aqueous extract of Talinum triangulare (leaves): evaluation of enzymes activities in tissue homogenates of albino rats. Pharmacol Online 3:67–73

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61. Sonibare MA, Ayoola IO (2015) Medicinal plants used in the treatment of neurodegenerative disorders in some parts of Southwest Nigeria. Afr J Pharm Pharmacol 9:956–965 62. Sanda ME (2015) Effects of waterleaf (Talinum triangulare) extract on performance and immune responses of boilers vaccinated with Newcastle disease vaccine (LaSota). Int J Food Agric Vet Sci 5:60–63 63. Nworgu F, Alikwe PCN, Egbunike GN, Ohimain EI (2015) Economic imortance of growth rate of broiler chickens fed with water leaf (Talinum triangulare) meal supplements. Asian J Agric Ext Econ Sociol 4:49–57 64. Biona K, Shen CC, Ragasa CY (2015) Chemical constituents of Talinum triangulare. Res J Pharmaceut Biol Chem Sci 6:167–171 65. Farvin KHS, Anandan R, Hari S, Kumar S, Shing KS, Mathew S, Sankar TV, Nair PGV (2006) Cardioprotective effect of squalene on lipid profile in isoprenaline-induced myocardial infarction in rats. J Med Food 9:531–536 66. Chaturvedi VC, Shrivastava R, Upreti RK (2004) Viral infections and trace elements: a complex trace element. Cur Sci 87:1536–1554 67. Gafar MK, Itodo AU (2011) Proximate and mineral composition of hairy indigo leaves. Res J Pharmaceut Biol Chem Sci 2:669–682 68. Harris WS, Mozaffarian D, Rimm E, Kris-Etherton P, Appel LJ, Engler MM, Engler MB, Sacks F (2009) Omega-6 fatty acids and risk for cardiovascular disease. Circulation 119:902–907 69. Katan MB (2009) Omega-6 polyunsaturated fatty acids and coronary heart disease. Am J Clin Nutr 89:1283–1284 70. Roosha P, Parloop B (2010) Omega-3 polyunsaturated fatty acid and cardiovascular disease: a review. Gujarat Med J 65:66–70 71. Erinoso SM, Aworinde DO (2012) Ethnobotanical survey of some medicinal plants used in traditional health care in Abeokuta areas of Ogun State, Nigeria. Afr J Pharm Pharmacol 6:1352–1362 72. Adeyemi O, Oyeniyi O, Mbagwu H, Jackson C (2011) Evaluation of the gastrointestinal activity of the aqueous root extracts of Talinum triangulare. Res Pharmaceut Biotechnol 3:61–67 73. Madariaga YG, Alfonso OC, Muñoz DS, Linares YM, Machado FB (2015) Assessment of hypolipidemic action of Talinum triangulare (waterleaf) and Abelmoschus esculentus (okra). Rev Cub Pl Med 20:290–300 74. Satyanarayana K, Krishnaveni K, Mishra R, Kumar KS (2012) Evaluation of analgesic activity of Talinum portulacifolium root extract on experimental animal model. J Pharm Res 5:4100– 4102 75. Ikewuchi CC, Ikewuchi JC, Ifeanacho MO (2016) Bioactive phytochemicals in an aqueous extract of the leaves of Talinum triangulare. Food Sci Nutr 5:696–701 76. Agunbiade SO, Ojezele MO, Alao OO (2015) Evaluation of the nutritional, phytochemical compositions and likely medicinal benefits of Vernomia amygdalina, Talinum triangulare and Ocimum basilicum leafy-vegetables. Adv Biol Res 9:151–155 77. Amorim APO, Campos de Oliveira MC, Amorim TDA, Echevarria A (2013) Antioxidant, iron chelating and tyrosinase inhibitory activities of extracts from Talinum triangulare Leach stem. Antioxidants 2:90–99 78. Peterson JJ, Dwyer JT, Jacques PF, McCullough ML (2012) Do flavonoids reduce cardiovascular disease incidence or mortality in US and European populations? Nutr Rev 70:491–508 79. Swarna J, Lokeswari TS, Smita M, Ravindhran R (2013) Characterisation and determination of in vitro antioxidant potential of betalains from Talinum triangulare (Jacq.) Willd. Food Chem 141:4382–4390

Part II Bioactive Compounds in Underutilized Vegetables: Fleshy Petioles, Cladodes, Fruits

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Bioactive Compounds of Prickly Pear [Opuntia ficus-indica (L.) Mill.] Imen Belhadj Slimen, Taha Najar, and Manef Abderrabba

Contents 1 Introduction: An Historical Overview of the Opuntioid Cacti . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 Polyphenolic Compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1 Organic Acids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Phenolic Acids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3 Flavonoids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4 Structure-Activity Relationship of Phenolic Acids and Flavonoids . . . . . . . . . . . . . . . . 3 Betalains . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 Carotenoids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 Vitamins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 Biothiols . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 Taurine . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 Fatty Acids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 Phytosterols . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 Saponins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11 Global Antioxidant Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

172 174 175 181 185 186 187 188 191 192 193 194 196 197 198 199 199

The original version of this chapter was revised. Correction to this chapter can be found at https:// doi.org/10.1007/978-3-030-57415-4_39 I. Belhadj Slimen (*) · T. Najar Department of Animal Sciences, National Agronomic Institute of Tunisia, Tunis, Tunisia Laboratory of Materials, Molecules and Applications, Preparatory Institute for Scientific and Technical Studies, Tunis, Tunisia e-mail: [email protected] M. Abderrabba Laboratory of Materials, Molecules and Applications, Preparatory Institute for Scientific and Technical Studies, Tunis, Tunisia e-mail: [email protected] © Springer Nature Switzerland AG 2021, corrected publication 2021 H. N. Murthy, K. Y. Paek (eds.), Bioactive Compounds in Underutilized Vegetables and Legumes, Reference Series in Phytochemistry, https://doi.org/10.1007/978-3-030-57415-4_12

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Abstract

Opuntia ficus-indica (L.) Mill, commonly called prickly pear or nopal cactus, belongs to the Cactaceae family. Opuntia ficus-indica (L.) Mill is a dicotyledonous angiosperm plant, known, since the dawn of time, for its ability to thrive under environments recognized as stressful for most plant species. Opuntia ficusindica has been used for a long time as diet, fodder, and beverage for both humans and animals, as well as to prevent soil erosion and to combat desertification. Opuntia ficus-indica has traditionally marked the folk medicine, owing to its therapeutic properties to a plethora of bioactive molecules, involving organic acids, phenolic acids, flavonoids, betalains, carotenoids, vitamins, biothiols, taurine, saponins, fatty acids, and phytosterols. The content of these bioactive molecules varies within cladodes, fruits or prickly pears, peels, seeds, and flowers. Whereas pears were commonly considered as noble fruits, peels have been arisen in the last decades as a promising by-product for both animals and humans health and nutrition. Nowadays, there is compelling evidence that Opuntia cacti are functional foods, source of nutrients, and bioactive molecules endowed with high antioxidant potential, and a large specter of biological, medicinal, and pharmacological applications. Indeed, Opuntia ficus-indica is highlighted as an excellent source of natural pigments, having promising applications in food industry and cosmetic. The present chapter aims to stressing the major classes of bioactive phytochemicals from Opuntia ficus-indica, with a deep understanding of the basis of their antioxidant activities, as well as an overview of their biological and medicinal properties. Keywords

Antioxidant activity · Bioactive molecule · Cactus pear · Cladode · Nopal · Opuntia ficus-indica

1

Introduction: An Historical Overview of the Opuntioid Cacti

Opuntia ficus-indica (L.) Mill, the commonly so-called prickly pear or nopal cactus, is a long domesticated and the most widespread cactus specie throughout the world. It has been and continues to be the most conspectus and characteristic of the arid and the semiarid climates. Opuntia ficus-indica belongs to the dicotyledonous angiosperm Cactaceae family which includes about 1500 species. Cacti are distinctive and unusual plants perfectly adapted to the extremely arid climates thanks to their CO2 fixation capacity (Crassulacean Acid Metabolism). Their stems expand into green succulent structures containing the chlorophyll, while the leaves are the spines for which cacti are well-known. Opuntia fruits are fleshy and elongated berries, varying in shape, size, and color (orange, yellow, red, purple, green, and white). They have a consistent number of hard seeds [1]. Their weight varies from 80 to 140 g, and the average of edible portion is about 54.18% [2].

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Early historic observations and archaeological data indicate that O. ficus-indica appears prominently in the folklore of the ancient middle-American civilizations as a “sacred tree” allowing quenching thirst and hunger [3]. Between 7500 and 5000 years BC, the prehistoric indigenous nomads living in the semiarid basins and valleys of the states of Hidalgo, Mexico, Morelos, Guerrero, Puebla, and Oaxaca started learning how to cultivate Opuntia which became later their basic foodstuff. The Aztecs, a Nahuatl-speaking people who rule Mexico on the fourteenth to the early of the sixteenth century, recognize mythically Opuntia as a “sacred tree.” Their prophecy reports that, according to Huitzilopochtli, the Sun and War god, the Aztecs had to leave where they lived and to build a new country where they would spot an eagle perched upon a prickly pear cactus, devouring a snake. They found a suitable place to build their future capital and named it “Tenochtitlàn,” which means “place of the prickly pear cactus.” This ancient capital is now in the center of Mexico City. Since the arrival of man in the desert of Mexico, Opuntia became an important source to agave food and beverage and was considered as a symbol of hope and endurance. Interestingly, the Mexican flag narrates this historical and cultural significance through the image of the eagle with a snake in its mouth sitting on top of the cactus. The genus Opuntia spread thereafter from Mexico to practically the entire American continent (from Alberta, Canada, to Patagonia, Argentina), Spanish, and the rest of the world [4]. In 1700, Tournefort gave the name of Opuntia for the first time, because of their similarity to a thorny plant that grew in the town of Opus, Greece [5]. The origin of O. ficus-indica was also investigated using Bayesian phylogenetic analyses of nrITS DNA sequences. This approach supports that “O. ficus-indica is close relative of a group of arborescent, fleshy-fruited prickly pears from central and southern Mexico; that the center of domestication for this species is in central Mexico; and that the taxonomic concept of O. ficus-indica may include clones derived from multiple lineages and therefore be polyphyletic” [6]. The most compelling archeological evidence that Opuntia was used as dietary source is found in the rockshelters of the Lower Pecos, just west of the South Texas Plains. At Hinds Cave, prickly pear seeds were found in some deposits at high densities, which argues strongly that prickly pear was one of the most common plant foods for the people who lived along the lower Pecos River. O. ficus-indica was historically used as a source of food, drink, and medicine. In the beginnings of the sixteenth century, Fray Bernardino de Sahagún reported in his book “Historia General de las Cosas de la Nueva España,” that native Americans were “healthy and strong” because of the diet they ate, which included “prickly pear leaves, prickly pear fruits, roots, mesquite pods, and yucca flowers which they called czotl, honey and rabbits, hares, deer, snakes and fowl” [7]. Another author, Friar Toribio Motolinia explained the use of Opuntia as beverage by the Aztecs: “. . . these Indians whom I refer to, because they are from a land so sterile that at times they lack water, drink the juice of these leaves of nocpal. . .” In the same way, Ramírez-Guzmán and his coauthors [8] reported in their chapter “Traditional fermented beverages in Mexico,” that indigenous peoples from Aztec, Chihuahua and Sonora, especially the Tarahumaras and Yaquis, as well as the mestizos of Zacatecas and San Luis Potosí, Querétaro, Guanajuato, and

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Hidalgoused to drink Colonche, a pleasant-tasting alcoholic beverage made from the fermented juice of the prickly pears (tuna) [9, 10]. The use of Opuntia in medicine dates back centuries. It is traditionally relevant to the Native Americans who used to consume Opuntia as a valuable health support nutrient and were consequently “healthy and strong” as described by [7]. More recently, the vegetative parts of Opuntia have been traditionally used in folk medicine. Cactus pear fruit has been used for a long time to heal wounds and to treat different pathologies, such as ulcers, dyspnea, glaucoma, liver diseases, and fatigue. Moreover, the consumption of the fruits and their juices has traditionally been recommended for their diuretic, hypoglycemic, antiallergic, analgesic, and anti-inflammatory effects, as well as for gastritis relief. Cladodes are still used for gastric ulcer treatment and for its healing activities. The infusions of cactus dried flowers function to prevent prostate cancer and urological problems [11]. Bioactive compounds are defined as compounds that occur in nature and are part of the food chain. They have the ability to interact with one or more compounds of the living tissue, by showing an effect on human health [12]. The infinite ramifications of functional groups, such as hydroxyls, alcohols, aldehydes, alkyls, benzyl rings, and steroids, results in a huge diversity of bioactive compounds, each one with particular characteristics [13]. Recent scientific reports highlighted the presence of several bioactive molecules that argue the medicinal applications and pharmacological properties of O. ficusindica (L.) Mill. These molecules include a variety of secondary metabolites known for their antioxidant and biological activities, fibers, vitamins, amino acids, sugars, fatty acids, and minerals [14–19]. The main objective of this chapter is to review these functional nutraceuticals and to highlight their interest in human and livestock health and medicine.

2

Polyphenolic Compounds

Phenolics are minor plant secondary metabolites that possess an aromatic ring with at least one hydroxyl group. Based on the nature and the number of linked functional groups, the structure of polyphenols diverges from simple molecules to more complex ones with a high molecular weight exceeding 30,000 Da [20, 21]. Within the vegetal kingdom, more than 8000 phenolic compounds are identified, among them, over 4000 flavonoids are currently known [19, 21, 22]. Phenolics are involved in the attraction of pollinators, the protection against UV radiation, microbial, and herbivore invasion, and in some structural functions of the plant [19, 23, 24]. In plants, most of the polyphenols occur as glycosides having different sugar ramifications [25]. Two major classifications of phenolic compounds were proposed. The first one implies the subdivision of phenolics in two main groups: flavonoids and nonflavonoid polyphenols. This classification is commonly used in the literature [26, 27]. The second one is based on the number of phenol rings constituting the aglycone, and allows differentiating polyphenols into phenolic acids, flavonoids, stilbenes, and lignins [23, 28]. This latter categorization will be adopted in this review (Fig. 1).

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Fig. 1 Main classes and subclasses of polyphenols, with their basic backbone

Flavonoids are the most common phenolics in the plant kingdom. They have a diphenylpropane core structure (C6-C3-C6) that involves two aromatic rings linked by an oxygenated heterocycle. The lowest contents of phenolics and flavonoids were recorded in the fruits and the seeds of O. ficus-indica, whereas the highest amounts were quantified mainly in peels, flowers, and cladodes. The phenolic profile of the whole Opuntia plant includes (40) phenolic acids, (1) gallotannin, (3) flavanones, (8) flavanols, (18) flavonols, (3) flavononols, and (9) flavones. In addition to these phenolic compounds, three organic acids were identified (Table 1).

2.1

Organic Acids

“Acid” is derived from the Latin acidus, meaning “to be sour.” Usually, any compound (organic or inorganic) that provides a sour taste is termed an acid. In plants, organic acids are involved in many important metabolic processes such as acidifying the extracellular medium, maintaining the ionic gradients on membranes, mediating the synthesis of phenolics and other metabolites, ensuring the redox equilibrium, and regulating the production of reactive oxygen and nitrogen species [50]. Based on their functional group, organic acids can be divided into vinylogous carboxylic acids, phenolic-type acids, and carbon-based acids. Although they are

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Table 1 Phenolic and organic contents (mg/100 g FW) in Opuntia ficus-indica Molecule Total phenolics (mg GAE/100 g FW) Total flavonoids (mg QE/100 g FW) Total tannins (mg MGE/100 g) Total anthocyanins (μg QE/100 g) Organic acids Quinic acid

430–620

Fruits 48.11– 218.8 2.60– 15.560 N.A.

0.05*– 0.34*

N. App.

42.983– 436.96 3124– 4421.7 77.15– 88.63

45.471

145.071

N.A.

N.A.

[31, 41–43]

N.A.

N.A.

N.A.

N.A.

[43]

N.A.

N.A.

N.A.

N.A.

[43]

D.

N.A.

N.A.

N.A.

N.A.

[43]

0.64–2.37

N.A.

N.A.

N.A.

[30, 44]

Salicylic acid Vanillic acid Piscidic acid Protocatachuic acid

0.58–3.54 D. N.A. D.

0–16.59 N.A. D. 0.015

N.A. N.A. N.A. N.A.

Caffeic acid trans-Caffeic acid 4-O-Caffeoylquinic acid Syringic acid

0.008 D. 0.007

0–8.04 N.A. D. 0.012– 0.061 0.040

3.539*– 4900 N.A. 4.940* N.A. N.A.

0.017

0.012

0.050

N.A. N.A. N.A.

1.40* N.A. N.A.

[41, 42, 44] [43] [31, 42]

N.D.

N.A.

4.590*

1,3-Di-Ocaffeoylquinic acid Caffeic acid 4-Oglucuronide Ferulic acid

0.017

0.085– 0.155 0.012

0.079

N.A.

N.A.

[31, 41, 42, 44] [31, 42]

N.A.

D.

D.

N.A.

N.A.

[45]

0.377

N.A.

74.88*

N.A. N.A. N.A.

N.A. D. D.

N.A. N.A. N.A.

[30, 31, 41, 42, 44] [41] [46] [46]

N.A. 0.040

D. N.D.

N.A. D.

N.A. N.A.

0.025

N.A.

N.A.

N.A.

Malic acid trans-Aconitic acid Gallotannins Tannic acid Phenolic acids Gallic acid

Isoferulic acid Ferulic acid glucoside Ferulic acid 4-Oglucuronide Dihydroferulic acid O-Coumaric acid m-Coumaric acid

Cladodes 390.90 73

0.301

0.11–34.77 0.00– 0.416 N.A. 4.322 N.A. N.A. N.A. N.A. N.A. 14.08– 16.18 N.A.

Peels 45.700– 425.59 6.95– 23.96 23*– 144* N. App.

Seeds 48– 89 1.5– 2.6 4.1– 205* N.A.

Flowers 12022*– 27090* 6081*– 6267* 768.67*

References [29–32, 35–38] [29–32, 36–38] [29, 36, 39]

N.A.

[40]

[29, 30, 41] [43, 44] [45] [31, 41–43]

[45] [30, 31, 42, 46] [41] (continued)

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Table 1 (continued) Molecule p-Coumaric acid

Cladodes 0.009

Fruits 0.168

Peels 0.039

Seeds N.A.

Flowers 13.371*

p-Coumaric acid 4-Oglucoside Salviolinic acid Rosmarinic acid Gentisic acid 3,4-Dihydroxybenzoic acid 4-Hydroxybenzoic acid Feruloyl-sucrose isomer 1 Feruloyl-sucrose isomer 2 trans-Cinnamic acid 3.4Dimethoxycinnamic acid Sinapoyl-diglucoside

N.A.

D.

D.

N.A.

N.A.

References [41, 42, 44, 45] [45]

0.024 N.A. N.A. 0.06–5.02

0.006 N.A. 0.019 N.A.

0.17 N.A. N.A. N.A.

N.A. N.A. N.A. N.A.

N.A. 16.065* N.A. N.A.

[31, 42] [44] [41] [30]

0.5–4.72 N.A.

0.355 N.A.

N.A. N.A.

N.A. N.A.

[30, 41] [34]

N.A.

N.A.

N.A.

N.A.

[34]

N.D. N.A.

0.429 0.072

0.864 N.A.

N.A. 7.36– 17.62 2.9– 17.1 N.A. N.A.

N.A. N.A.

[31, 42] [41]

N.A.

N.A.

N.A.

N.A.

[34]

N.A.

N.A.

N.A.

12.6– 23.4 D.

N.A.

[46]

N.A.

D.

N.A.

N.A.

N.A.

[47]

N.A. N.A. N.A.

D. D. D.

N.A. N.A. N.A.

N.A. N.A. N.A.

N.A. N.A. N.A.

[47] [47] [47]

N.A. N.A. 0.163 N.A.

0.102 0.004 N.A. N.A.

N.A. N.A. N.A. N.A.

N.A. N.A. D. N.A.

N.A. N.A. N.A. 5.057*

[41] [41] [42, 46] [44]

0.033 D. 16.177– 17.459

0.106 0.0 N.A.

0.17 0.037 N.A.

N.A. N.A. N.A.

N.A. N.A. N.A.

[31, 42] [31, 42, 43] [43]

2.36–26.17 0.3180

5.166

N.A.

N.A.

0.681– 0.698 N.D. N.A.

9

4.32

N.A.

6.340*

0.003 D.

0.30 N.A.

N.A. N.A.

14.159* N.A.

[30, 31, 42, 43] [30, 43, 44, 47] [31, 42, 44] [47]

1,2-Di-O-Sinapoyl glucose Benzyl-O-β-Dglucopyranoside Picein Androsin 1-O-feruloyl-β-Dglucopyranoside trans-Sinapic acid cis-Sinapic acid Chlorogenic acid Cinnamic acid Flavanones Naringin Naringenin Hesperidin Flavonols Rutin Quercetin Quercetrin Quercetin-3-methyl ether

(continued)

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Table 1 (continued) Molecule Isoquercetin Quercetin-3-Ogalactoside (hyperoside) Quercetin-3-Oglucoside Quercetin-3-Orutinoside Flavan-3-ol Catechin (+) Flavonols Rhamnetin Isorhamnetin

Cladodes Fruits 2.29–39.67 N.A. 0.005– 0.023 6.209

Peels N.A. 0.167

Seeds N.A. N.A.

Flowers N.A. 9.84*– 35.86

References [30] [42–44, 48]

N.A.

0.023

N.A.

N.A.

N.A.

N.A.

N.A.

N.A.

19.25*– 474 14.58*– 709

[31, 44, 48, 49] [44, 48, 49]

N.D.

0.007

N.D.

N.A.

5.095*– 823

[31, 42, 44]

D. N.A.

N.A. 4.94

N.A. 2.41–91

N.A. D.

N.A. N.A.

[43] [30, 32, 46, 47] [30, 44, 48]

Isorhamnetin-3-Oglucoside Isorhamnetin 3-ORobinobioside Isorhamnetin 3-Ogalactoside Isorhamnetin 3-Ogalactoside 7-ORhamnoside Isorhamnetin 3-Orutinoside Isorhamnetin-3-O-β-Dglucopyranoside Isorhamnetin 3-Oglucoside 7-Orhamnoside Isorhamnetin glucosides Narcissin

4.59–32.21 N.A.

N.A.

N.A.

N.A.

N.A.

N.A.

N.A.

7.896*– 724 4269

N.A.

N.A.

N.A.

N.A.

7.27*–979

[44, 48, 49]

N.A.

D.

D.

N.A.

N.A.

[45]

N.A.

N.A.

N.A.

N.A.

[44, 48]

N.A.

D.

N.A.

N.A.

4.395*– 172.72 N.A.

N.A.

D.

D.

N.A.

N.A.

[45]

N.A.

50.6

N.A.

N.A.

N.A.

[30]

D.

N.A.

N.A.

N.A.

[30, 47]

Myricetin Kaempferol

14.69– 137.1 N.A. D.

N.A. 0.27– 2.7 2.89–146.5 N.A.

N.A. 0.22

D. N.A.

N.A. N.A.

N.A.

D.

6.42–400

[46] [30, 32, 33, 43, 47] [30, 46, 48, 49]

N.A.

N.A.

N.A.

N.A.

4.78*–324

[44, 48, 49]

N.A.

D.

N.A.

N.A.

N.A.

[47]

Kaempferol-3-ORutinoside (Nicotiflorin) Kaempferol-3-OArabinoside Kaempferol-3-methyl ether

[49]

[47]

(continued)

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Table 1 (continued) Molecule Kaempferol 3-O-(200 rhamnosylgalactoside) 7-O-rhamnoside Kaempferol 3-Orhamnosyl-rhamnosylglucoside Flavononols Taxifolin (+)-Taxifolin (+)-Aromadendrin Flavones Luteolin

Cladodes N.A.

Fruits D.

Peels D.

Seeds N.A.

Flowers N.A.

References [45]

N.A.

D.

D.

N.A.

N.A.

[45]

N.A. N.A. N.A.

D. D. D.

D. N.A. N.A.

N.A. N.A. N.A.

N.A. N.A. N.A.

[45] [47] [47]

N.D.

0.001

N.A.

N.A.

[31, 32, 42]

Luteolin-7-O-glucoside Apigenin Apegenin-7-Oglucoside Cirsiliol Amentoflavone Lupinisoflavone Chrysin Acacetin

0.014 0.001 0.001

0.001– 0.84 0.006 0.001 0.002

0.007 0.001 0.003

N.A. N.A. N.A.

N.A. N.A. N.A.

[31, 42] [31, 42] [31, 42]

1.502 N.A. N.A. D. 0.734

0.88 N.A. N.A. N.A. 0.719

0.658 N.A. N.A. N.A. 0.694

N.A. D. D. N.A. N.A.

N.A. 8.674* N.A. N.A. N.A.

[31, 42] [44, 46] [46] [43] [31, 42]

*Dry weight basis, N.A.: Data not available, N. App.: Not applicable, D.: Detected pic

weak acids, their structural diversity results in a wide range of pKa values from as low as 3 (carboxylic) to as high as 9 (phenolic). In O. ficus-indica, three major organic acids were identified: malic, quinic, and aconitic acids. The highest amounts were quantified in peels and cladodes. Further investigations are needed to assess the corresponding levels in flowers and seeds. Malic acid (C4H6O5) belongs to the family of vinylogous carboxylic acids characterized by a juxtaposition of a hydroxyl group in conjugation with a carbonyl one (Fig. 2). The proton behaves as if it were attached to a carboxylic acid rather than an alcohol. Malic acid is responsible of the sour taste in cladodes and peels, mainly. From a chemical point of view, the acidity of vinylogous carboxylic acids increases as the number of vinyl groups separating the hydroxy and the carbonyl groups increases. The calculated increase in acidity can be thought to arise from the dispersal of the negative charge between the two oxygens in the anion [51]. In higher plants, malic acid (Fig. 2) is involved in the cell redox metabolism and signaling in photosynthetic tissues [50]. In food industry, malic acid is used as a pH regulator and flavor enhancer. Moreover, several studies reported bacteriostatic and bactericidal properties [52–54]. After oral administration, this dicarboxylic acid stimulates the secretion of gastric juices and increases peristalsis [52]. Quinic acid (C7H12O6) is a ubiquitous plant metabolite containing a cyclohexane carboxylic skeleton (Fig. 2). Quinic acid is an important intermediate product in the

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Fig. 2 Organic acids from O. ficus-indica

biosynthesis of aromatic compounds (flavonoids and phenol carboxylic acids) in higher plants, humans, and animals [55]. Besides its antibacterial activity [56], D-()-Quinic acid has been reported to have antioxidant, anti-inflammatory, and antiproliferative properties [57, 58]. Neuro- and radio-protective effects were also attributed to this molecule [59, 60]. In addition, synergic effects were revealed between quinic acid and quercetin to alleviate structural degeneration in liver, kidney, and pancreas tissues of diabetic rats [61]. trans-Aconitic acid (Fig. 2) belongs to the class of organic compounds known as tricarboxylic acids and derivatives. It is a small unsaturated and a weakly acidic compound (pKa ¼ 3.15). trans-Aconitic is the natural isomer of cis-aconitic acid in the tricarboxylic acid (TCA) cycle [62]. Outside the human body, trans-Aconitic acid is highly produced by sugar-containing plants [63, 64] and some bacteria, as a virulence factor [65]. In plants, it has been speculated that trans-Aconitic acid can neutralize alkaline compounds absorbed by roots [64] and acts as an antifeedant against the rice pest brown planthopper [66]. trans-Aconitic acid is normally present in normal human urine. This could make trans-aconitic acid a potential biomarker for the consumption of some foods. trans-Aconitic acid is closely related to the central cellular metabolism of the TCA cycle since it was known to be a strong inhibitor of aconitase [67]. As an antimicrobial agent trans-Aconitic acid is used as an antileishmanial to prevent the transformation of L. donovani from amastigotes to promastigotes [68]. Although it is responsible of tetany in grazing cattle when it exceeds 5% in ration, trans-Aconitic acid is recognized as safe under the provisions of the Code of Federal Regulations (21 CFR 121.101, revised April 1, 1974). Moreover, both natural and esterified forms of this acid were reported for their anti-inflammatory activity [69]. Interestingly, its isomer, cisaconitic acid, was shown to inhibit carcinogenesis induced by 3,4-benzopyrene in experimental animals [70]. No trials were reported for trans-aconitic acid in this field, and the chemical reaction leading to the formation of the cis isomer from the trans one is endothermic, and not spontaneous. There is a lack of data with regard to the organic acids profile in the different O. ficus-indica vegetative parts. Further investigations are required in order to understand the biogenesis and the metabolic pathways of these compounds, as well as the biological activities that they may exhibit.

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2.2

181

Phenolic Acids

2.2.1 Structure and Chemical Properties Phenolic acids are compounds featuring one or more hydroxyl groups (–OH) directly linked to the aromatic system [71]. All carbons of the aromatic ring are sp2 hybridized. The C-O bond is formed from Csp2-Osp3, whereas the O-H bond is formed from Osp3-H1s. The two other orbitals of oxygen atom are occupied by two nonbonded electron pairs. Since oxygen is more electronegative than carbon and hydrogen, C-O and the H-O bonds are polar [72]. Moreover, the conjugation of electron pairs of oxygen atom with the aromatic system results in a partial transfer of negative charge from oxygen to the ring, and in a further delocalization of this charge. The polarization of the O-H bond is therefore strengthened. Phenols gain an acidic character and an ability to form a resonance-stabilized phenoxide anion [71, 72]. Figure 3 illustrates the charge transfer among phenol and phenoxide anion. Such resonance is at the origin of the antioxidant properties of phenolic acids. The above-described structural features result in several specific physical and chemical properties of phenolic acids: low melting point, high boiling point, odd smell, and water-soluble crystalline solid. pKa values of most phenols range from 8 to 10. This means that these acids are stronger than water (pKa of water 15.7) but weaker than carbonic acid (pKa of 6.4). This acidity of phenol is the result of negative charge’s delocalization over the aromatic ring and the resonance effect. The ability to donate or to withdraw electrons, the position, and the number of functional groups attached to the ring can alter significantly the chemical properties of phenolic acids [73].

Fig. 3 Resonance stabilization of phenol and phenoxide anion

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Biological Activities of Some Phenolic Acids from O. ficus-indica (L.) Mill Phenolic acids are split into two subgroups: hydroxybenzoic and hydroxycinnamic acids [74]. Hydroxycinnamic acids are derivatives of cinnamic acid. These are simple esters with quinic acid or glucose. The most abundant hydroxycinnamic acids in O. ficus-indica are cinnamic, chlorogenic, coumaric, and ferulic acids. Lower concentrations of caffeic, sinapic, and dimethoxycinnamic acids were reported (Table 1). Hydroxybenzoic acids are derived from benzoic acid and are recognized by their common C6-C1 structure. They occur in a soluble form, a conjugated form with sugars or organic acids, or bound with lignin and other cell-wall fractions [75]. As compared to hydroxycinnamic acids, hydroxybenzoic acids are generally found in lower concentrations in O. ficus-indica. The commonly found hydroxybenzoic acids are 4-hydroxybenzoic, protocatechuic, vanillic, syringic, salicylic, gallic, and gentisic acids (Table 1). Even their complete roles remain unknown in the plant kingdom; phenolic acids are the most polyphenols produced by plants and are precursor of the bioactive molecules used in therapeutics, cosmetic, and food industry [76, 77]. Phenolic acids are involved in different functions such as photosynthesis, synthesis of proteins, uptake of nutrients, and cell signaling. Indeed, phenolic acids are featured within the structural components. They are also implicated in enzyme activity and allelopathy [78]. 2.2.2

Gallic Acid Gallic acid, known also as 3,4,5-trihydroxybenzoic acid, was identified in cladodes and flowers of O. ficus-indica. It is found in plants as a free acid, an ester, a catechin derivative, or hydrolyzable tannin. Gallic acid and its derivatives have been reported to elicit a myriad of biological activities such as antiproliferative, bactericide, antiviral, antifungal, inflammation modulator, and antidiabetic activities [79–83]. The great interest in these compounds is also due to their pharmacological activity as radical scavenger. Preventive and curative effects of gallic acid and its derivatives were reported in many pathologies where the oxidative stress has been implicated, such as cancer, cardiovascular disorders, neurodegenerative troubles, and aging [84–86]. It has been also reported that gallic acid has antimicrobial activity against methicillin-resistant Staphylococcus aureus and Helicobacter pylori [87, 88]. In addition, the scientific literature described several pharmacological activities. Gallic acid and its derivatives were investigated as antidepressant [89], antiParkinson [90], antimalarial [91], diuretic [92], wound healing [93], anthelmintic [94], and anxiolytic [95] agents. This myriad of biological activities introduces gallic acid as a potential molecule for drug development. Protocatechuic Acid Protocatechuic acid (PCA), or 3, 4-dihydroxybenzoic acid, is a dihydroxybenzoic acid in which the hydroxy groups are linked in positions 3 and 4. Recent studies indicate that PCA could be used as a protective agent against cardiovascular diseases and neoplasms. Its mechanism of action is mostly related to its radical scavenging activity allowing to inhibiting the generation of free radicals and up-regulating enzymes which participate in radicals’ neutralization [96]. PCA has been reported as potent antioxidant.

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PCA was also described as antibacterial, anticancer, antiulcer, antidiabetic, antiageing, antifibrotic, antiviral, inflammation modulator, analgesic, antiatherosclerotic, cardiac, hepatoprotective, neurological, and nephron-protective agent [97]. Cinnamic Acid and Derivatives Cinnamic acid (C9H8O2) is an organic acid found in plants. It has low toxicity and a wide spectrum of antioxidant and biological properties [98]. Interestingly, the antioxidant capacity of cinnamic acid derivatives is higher than their benzoic acid counterparts [99]. In the recent decades, cinnamic acid and its derivatives (natural and nonnatural compounds) had been proven to possess a range of pharmacological actions such as antimicrobial [100], antiparasitic [101], antifungal [102], anticancer [103], anti-inflammatory [104], and antihuman immunodeficiency virus (HIV) [105]. Moreover, cinnamic acid derivatives were shown to induce neural progenitor cell proliferation [106]. The high antioxidant activity of cinnamic acid and its derivatives, in addition to the biological properties cited above, suggest the use of these promising molecules as potent compounds for drug development. Chlorogenic Acid Chlorogenic acid (C16H18O9), or 3-O-caffeoylquinic acid, is a cinnamate ester obtained through formal condensation of the carboxy group of trans-caffeic acid with the 3-hydroxy group of quinic acid. Chlorogenic acid is ubiquitous in the plant kingdom, and the most abundant phenolic acid in coffee. It has been also isolated from leaves and fruits of dicotyledonous plants. In a typical human diet, a daily intake of around 2–3 g of chlorogenic acid per human is estimated, providing the main motivation for the investigation of chlorogenic acid chemistry and biological activities [107]. For a long time, chlorogenic acid was known as an antioxidant. In fact, there is accumulated evidence that this phenolic acid is involved in glucose and lipid metabolism. Chlorogenic acid was reported as insulin sensitizer which enhances glucose tolerance and insulin resistance. Hence, it is not surprising that chlorogenic acid was associated with a lower risk of type 2 diabetes mellitus [108, 109]. Moreover, chlorogenic acid was shown to modulate lipid metabolism through reducing serum and hepatic triglyceride levels, lowering LDL susceptibility to oxidation, decreasing MDA and cholesterol values, hindering fat absorption, activating fat metabolism in the liver, and enhancing of obesity-related hormones levels [109]. These effects suggest chlorogenic acid as a good candidate to prevent and treat obesity, diabetes mellitus, and metabolic syndrome. Indeed, the antioxidant, anticarcinogenic, and anti-inflammatory impacts may provide a nonpharmacological and noninvasive approach for treatment or prevention of some chronic diseases [108]. However, further investigations are needed to elucidate conclusively the mechanism of action and the dose–response relationship. Coumaric Acid and Derivatives p-Coumaric acid (C9H8O3), or 4-hydroxycinnamic acid, is a cinnamic acid derivative in which the hydroxyl group is located at C-4 of the phenyl ring. It is a conjugate of 4-coumarate. p-Coumaric acid is synthesized principally from tyrosine and phenylalanine. It is a major precursor in the synthesis of other phenolic acids, such

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as caffeic, chlorogenic, rosmarinic, and ferulic acids. Studies on p-coumaric acid stated that this bioactive molecule is a relatively potent antioxidant and a scavenger of reactive oxygen species and free radicals [110]. In animal models, p-coumaric acid was shown to be more effective than vitamin E in decreasing oxidative stress [111]. Indeed, p-coumaric showed antimicrobial activity implying the disruption of bacterial membranes and intercalating the groove in bacterial DNA [112]. Besides, pCoumaric acid showed anti-inflammatory effects and improved immune response [113]. In addition, p-coumaric acid has been reported to inhibit proliferation and migration of cancer cells and promote apoptotic cancer cell death, supporting its potential anticancer effects [114]. Its chemopreventive effects against colon cancer have been also demonstrated in animal models [115]. Moreover, p-coumaric acid has been highlighted as an active ingredient in cosmetics [116]. Preparations comprising p-coumaric acid have been described for their antioxidant and antimicrobial properties, helping the regeneration of wounded skin [117]. In addition, p-coumaric acid was demonstrated to have good potential to be used as a skin-lightening active ingredient in cosmetics. It allowed decreasing skin hyperpigmentation and preventing the catalytic activity of tyrosinase as well as cellular melanogenesis [116]. Indeed, p-coumaric acid was stated to exhibit protective effects of skin cells against UV radiation, and to attenuate the light-induced oxidative damage of in the eye in vitro and in vivo models [116]. Future studies are needed to develop optimized cosmetic formulations for the best performance in skin lightening and eye care. Ferulic Acid Ferulic acid (FA) is a trans-cinnamic acid bearing methoxy and hydroxy groupments, respectively, at positions 3 and 4 on the phenyl ring. It is a ubiquitous phytochemical found in plant cell walls. It occurs mainly in seeds and leaves in both free (rarely) and covalently linked form one to lignin and other biopolymers. However, there is no available information about the content of ferulic acid in seeds of O. ficus-indica. Due to its phenolic nucleus and the extended side-chain conjugation (carbohydrates and proteins), FA easily forms a resonance stabilized phenoxyl radical which accounts for its potent antioxidant potential. Ferulic acid acts as an antioxidant [118] and exhibited promising effects in reducing oxidative damage and amyloid pathology in Alzheimer’s disease [119]. In atherosclerosis, trans-ferulic acid exhibited moderate inhibitory actions on the Hsp60-induced cell proliferation [120]. Once supplemented in other foods, FA enhances the development of the reproductive tract and ovarian activity of ewes in the natural anestrus season. This finding may be attributed to the enhancement of glucose-insulin system [121]. FA has been recognized for several biological activities, including antioxidant, anti-inflammatory, antiviral, antiallergic, antimicrobial, antithrombotic, anticarcinogenic, and hepatoprotective actions [122, 123]. Recent findings on the biological and pharmacological activities of FA were reviewed by Kim and Park [124]. The bioavailability of FA was also investigated and the results indicated that the peak time for maximal urinary excretion is approximately 7 h. The recovery of FA in the urine, on the basis of total free FA and feruloyl glucuronide excreted, is 11–25% of that ingested [125].

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Caffeic Acid Caffeic acid (3, 4-dihydroxycinnamic acid) is structurally composed of both phenolic and acrylic functional groups [126]. It was quantified in high amounts in O. ficus-indica fruits and flowers and was reported to exhibit a large spectrum of biological activities. Caffeic acids demonstrated protective effects against phosphatidylcholine peroxidation initiated by UV radiation, which is a major constituent of the lipid bilayers of cell membranes [127]. In this direction, it was proven that caffeic acid is able to permeate all the skin layers of pig ear [128] despite the pH of the receptor solution [129], due to its high lipophilicity allowing to reach the stratum corneum [130]. Caffeic acid was then considered as a promising molecule able to promote satisfactory photo protection [131]. Antioxidant and antimicrobial activities of caffeic acid are pH dependent. At pH interval varying from 3 to 5, caffeic acid exhibited antimicrobial effects against various microorganisms including E. coli, Pseudomonas aeruginosa, Bacillus cereus, Kocuria rhizophila, Staphylococcus aureus, Listeria monocytogenes, and Candida albicans [132]. The mechanism of action implied an increase of the pathogen membrane permeability and leads to a loss of cellular constituents. In addition, caffeic acid was responsible of the inactivation of some pathogen enzymes involved in the energy production process of and in the synthesis of structural components, as well as the destruction or inactivation of functional genetic material [133]. In another research side, caffeic acid and its derivatives have been reported for their proven efficacy against colon and oral cancer as well as hepatic-carcinoma, and are considered as inhibitors of cyclooxygenase II in tumors [134–136]. Although many trials confirmed the antitumor activity of caffeic acid, some studies reported carcinogenetic effects, even at low administration levels [137]. Interestingly, caffeic acid is listed under some Hazard Data and the International Agency for Research on Cancer has classified it in group 2B as a substance that is “possibly carcinogenic to humans.” Hence, further investigations are needed to make concluding remarks about the protective or the carcinogenic potential of caffeic acid.

2.3

Flavonoids

2.3.1 Flavonols Flavanols are a structurally complex subclass of phenolic compounds, ranging from simple monomers (such as catechin) to oligomers (from dimers to decamers), polymers (>10 mers), and more complex derived compounds (such as theaflavins and thearubigins). The major flavanols of O. ficus-indica are quercetin and its derivatives, rutin, and catechin, a flavan-3-ol. Although this latter was not detected in Opuntia cladodes and peels, trace amounts were quantified in fruits and high contents were calculated in flowers. The greatest amount of flavanols were recorded in flowers, followed by cladodes, peels, than in fruits. Additional investigations are needed to assess the flavanols contents in seeds. Rutin is also called rutoside, quercetin-3-O-rutinoside, and sophorin. This glycoside combines the flavonol quercetin and the disaccharide rutinose. Rutin is an extremely potent molecule since it exhibits strong antioxidant activity. It was described

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not only for its antimicrobial, antifungal, and antiallergic activity, but it is also used to treat various chronic diseases such as cancer, diabetes, hypertension, and hypercholesterolemia. Compared to other flavonoids, rutin is considered as a nontoxic and nonoxidizable molecule [138]. Quercetin, a flavonol with proven health-promoting properties, is one of the most potent antioxidants among polyphenols [139, 140]. Quercetin derivatives can be both lipo- and hydrophilic, depending on the type of substituents in the molecule. Glycosylation of at least one hydroxyl group of quercetin derivatives results in an increase of its hydrophilicity [141].

2.3.2 Flavanones Within the plant secondary metabolites, flavanones, also called as dihydroflavones, are defined as one of the minor classes of flavonoids. Flavones are obligate intermediates in flavonoid biosynthesis and occur as glycosides in nature. Structurally, flavanones are composed of two benzene rings (A and B), which are linked by a heterocyclic ring (C). Interestingly, the C-ring is saturated. At C2-position, the carbon is asymmetric. The content of flavanones may control the sweetness or bitterness of fruits [142]. Three flavanones were detected in O. ficus-indica: naringin, naringenin, and hesperidin. The highest contents were attributed to hesperidin which was detected only in cladodes (16.18–17.46 mg/100 g), then naringin, especially in peels (0.17 mg/100 g). Low amounts of naringenin were quantified in peels, and traces were found in fruits. Once again, O. ficus-indica peels are confirmed as a valuable source of flavanones, whereas cladodes contain the greatest amounts of hesperidin. Further investigations are needed to assess these compounds in seeds and flowers. In addition to its functional properties in preventing cardiovascular disease, type II diabetes, and its anti-inflammatory effects, recent studies have highlighted numerous benefits of hesperidin (hesperetin-7-rutinoside) for cutaneous functions. For instance, hesperidin was described for wound healing, UV protection, antimicrobial, antiproliferative, and skin lightening properties. In addition, hesperidin enhances the homeostasis of the epidermal barrier in both young and aged skins. The mechanisms by which hesperidin improves cutaneous functions are explained by its antioxidant properties, inhibition of MAPK-dependent signaling pathways, and stimulation of epidermal proliferation, differentiation, and lipid production [143]. Naringin (C27H32O14), a polymethoxylated flavonoid, is the glycosylated form of naringenin (C15H12O15). Both naringin and naringenin are potent antioxidants [144, 145]. However, the former is less stronger than the latter because the sugar moiety in naringin causes steric hindrance of the scavenging group. Naringin was reported for its favorable effects on obesity, hyperlipidemia, hypertension, cardiac function, hyperglycemia, and diabetes, hepatic function, inflammation, oxidative stress, and free radical damage [146, 147].

2.4

Structure-Activity Relationship of Phenolic Acids and Flavonoids

Phenolic acids possess much higher in vitro antioxidant activity than well-known antioxidant vitamins [148]. However, because phenolics have a wide array of chemical structures, it is not surprising that antioxidant activities vary greatly.

Bioactive Compounds of Prickly Pear [Opuntia ficus-indica (L.) Mill.]

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187

(i) The ability of phenolic acids and flavonoids to donate hydrogen to the radical leads to the formation of a decreased energy phenoxide radical (Eq. 1).   Ä Ä PhðOHÞ þ Rn ! Ph On þ RH

ð1Þ

Such radical is stable and don’t mediate autooxidation reactions. The electron reduction potential (E°0 ) of a good hydrogen donator (especially that of the oxygen–hydrogen bond) should be below than that of the free radical, in order to allow an efficient and rapid transfer of the hydrogen to the oxidizing molecule, unless the reaction is kinetically unfeasible [14, 149]. (ii) Phenolic acids and flavonoids are effective free radical scavengers because they produce low-energy radicals after oxidation reactions, thanks to the delocalization of quenched radicals throughout the phenolic ring structure. Thus, the likelihood of the resulting antioxidant radical to mediate auto-oxidation reaction is low [149]. (iii) Polyphenols are also effective free radical scavengers because the radicals they produce do not react quickly with oxygen to form hydroperoxides, which are able to autoxidize and promote oxidations reaction chains [149]. (iv) In the termination step, antioxidant radicals may undergo additional reactions in order to remove the quenched radical from their molecules, and retrieve again their initial structure. In instance, phenolic radicals may interact, for a second time, with another radical to end the reaction and form a nonradical product [149].

3

Betalains

Betalains are hydro-soluble pigments that contain nitrogen. They are localized in the vacuolar sap wherein they are dissolved as bis-anions [150]. Structurally, betalamic acid (Fig. 4) [4-(2-oxoethylidene)-1,2,3,4-tetrahydropyridine-2,6-dicarboxylic acid] is considered as the common skeleton of all betalains. Betalamic acid may condense either with cyclo-DOPA [cyclo-L-(3,4-dihydroxyphenylalanine)] or its glucosyl derivates to give violet betacyanins (Greek: kyaneos ¼ blue), or with amino acids or their derivates to form yellow betaxanthins (Greek: xanthos ¼ yellow) (Fig. 4).

Fig. 4 Basic structures of betalamic acid, betaxanthins, and betacyanins

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Betalains were recorded in the pulp and the peel of O. ficus-indica at high amounts. Betaxanthins are abundant in fruits (53.27 vs. 40.72 mg/kg) whereas betacyanins are highly available in peels (19.43 vs. 6.76 mg/kg). Total betalains are greater in peels than in fruits. Similarly, betanin contents are higher in peels than in fruits (2473 vs. 1616 mg/kg) [42]. Betacyanins and betaxanthins concentrations were closely linked to the color of the fruit [42]. In addition to neobetanin, betanin, isobetanin, betanidin, and indicaxanthin are present in Opuntia fruits [151–153]. Betanin and indicaxanthin were detected in the peel [153]. Gomphrenin I, portulacaxanthin I, portulacaxanthin III, muscaaurin, (S)-serine-betaxanthin, (S)-valine-betaxanthin, (S)-isoleucine-betaxanthin, (S)- Phenylalaine-betaxanthin, Vulgaxanthin I, Vulgaxanthin II, Vulgaxanthin IV, and Miraxanthin II were also reported [154–157]. Several studies reported a high radical scavenging potential of betalains, and considered them as a class of dietary cationized antioxidants [158]. The antioxidant activity of betalains was shown to be much higher than that of α-tocopherol, trolox, ascorbic acid, ß-carotene, catechin, and rutin [158–162]. Betalamic acid was able to reduce two molecules of Fe3+ in Fe2+. This means that betalamic acid is able to donate two electrons to an oxidizing agent [163]. Regarding betaxanthins, the catechol substructure allows increasing the antioxidant activity at higher pH [159]. As the reduction potentials of betanin and indicaxanthin are equals, respectively, to 0.4 and 0.6 V, these two pigments are able to donate easily their electrons. Interestingly, betanin was reported to inhibit lipoperoxidation even at very low concentrations [161, 164]. However, indicaxanthin was revealed to be less effective than betanin in radical scavenging reactions [164]. Besides, betanin was demonstrated to act as an oxidation retarder. Additive effects of betanin and indicaxanthin with α-tocopherol were also reported [165]. Betalains are very stable molecules, even upon oxidation reaction. This stability is structurally ensured through: (i) Resonance stability in phenoxyl anion, (ii) hydrogen bonding, and (iii) common resonance shared between the imino and the tetrahydropyridine groups [166] (Fig. 5). As phytoantioxidants, betalains are able to activate the mammalian stress response and to induce heat shock proteins (HSPs) synthesis, which are considered as molecular chaperones involved in the repair of stress denatured proteins [167]. Moreover, our recent studies showed that betalains ensure the thermoprotection of sheep lymphocytes by scavenging their H2O2 production level and preventing oxidative-induced apoptotic cell death [168].

4

Carotenoids

Carotenoids are tetraterpene pigments that exhibit a range of colors varying from yellow to purple. Structurally, carotenoids consist of a polyene chain containing eight isoprene units of about 40 carbons, with nine conjugated double bonds and an end group localized at both ends of the polyene chain (Fig. 6). Most of carotenoids are C-40 carotenoids. Those having more than 40 carbons’ core structure are called higher carotenoids. And those having fewer than 40 carbons are called

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Fig. 5 Stabilization systems in betalains upon unpaired electron abstraction: (a) Resonance stability in phenoxyl anion. (b) Hydrogen bonding. (c) Common resonance system shared between the imino and the tetrahydropyridine groups

Fig. 6 Major carotenoids of O. ficus-indica

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apocarotenoids [169]. Interestingly, vitamin A is considered as an apocarotenoid, since it is the result of the symmetrical oxidative cleavage of β-carotene [170]. Carotenoids are classified as carotenes and xanthophylls. The former are exclusively hydrocarbons. The latter contain polar ends groups suggesting an oxidative step in their formation. Carotenes are structurally the simplest carotenoids. They include α-carotene, β-carotene, β, ψ-carotene (γ-carotene), and lycopene [171]. On the other hand, xanthophylls are oxygenated carotenoids which contain several functional groups such as hydroxyl (lutein and zeaxanthin), epoxy (violaxanthin, neoxanthin, and fucoxanthin), keto (astaxanthin and canthaxanthin), and methoxyl (spirilloxanthin) ones [172]. Opuntia carotenoids are generally formed from eight C5 isoprenoid units joined head to tail, except at the center, where a tail-to-tail linkage reverses the order and results in a symmetrical molecule [46]. O. ficus-indica contains high amounts of carotenoids, and their concentration is significantly higher in the peel than in the pulp. The stage of maturity of cladodes impacts deeply the carotenoids content, as lutein, β-carotene, and β-criptoxanthin are the most abundant carotenoids in fresh cladodes [173]. Indeed, cladodes contain more carotene than the fruit, in spite of the cultivar [174]. Similarly, peels contain considerably higher amounts of carotenoids than fruits (12.58–16.83 μg/g and 2.58–6.68 μg/g, respectively) [32, 175]. The carotenoid profile of fruits consists mainly of nine xanthophylls (84–86% of the total carotenoids) and four carotenes. The predominant xanthophyll compounds were lutein and violaxanthin (respectively, ≈69–72% and 5% of the total carotenoid content in the whole fruit), whereas the major carotene pigment is β-carotene, accounting for 12–14% of the total carotenoid content. Zeaxanthin, anteraxanthin, and neoxanthin were reported in lower concentrations [175]. The highest values were recorded in the cultivars having orange color [176, 177]. The carotenoid profile of peels is dominated by lutein, β-carotene, and violaxanthin, which represent, respectively, 66.86%, 11.83%, and 5.53% of the total carotenoids content. Zeaxanthin, lycopene, anteraxanthin, and neoxanthin were also recorded at lower concentrations. Very small amounts of α-carotene and β-criptoxanthin were also quantified [175]. In cladodes, lutein, β-carotene, and α-cryptoxanthin are the predominant carotenoids, accounting for 111.03, 90.40, and 46.37 μg/g of dry matter, respectively [178]. In young cladodes, concentrations vary between 0.047 and 0.077 mg/100 g [179]. In foods, light will activate chlorophyll, riboflavin, and heme-containing proteins to high-energy excited states. These photoactivated molecules can free radical reactions when interacting directly with an oxidized compound to produce free radicals, or when initiating a reaction with triplet oxygen to form singlet oxygen (1O2), or when transferring an electron to triplet oxygen to form the superoxide anion. The presence of carotenoids in food allows inactivating these photoactivated sensitizers by quenching the excited electrons. Hence, the carotenoid molecule moves to the excited state, and returns thereafter to the ground one after energy transfer into the surrounding solvent by vibrational and rotational mechanisms [149]. Carotenes and xanthophylls were confirmed to be efficient quenchers of 1O2 and peroxyl radicals [180, 181]. Carotenoids can inactivate 1O2 by both chemical and physical quenching. Chemical quenching consists of a direct addition of 1O2 to the carotenoid, leading to the formation of carotenoid breakdown products and loss of

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Fig. 7 Resonance stabilization of β-carotene after peroxyl radical quenching

antioxidant activity. Physical quenching occurs because the energy levels of carotenoids are close to those of 1O2, thus enabling energy transfer from 1O2 to the pigment. This reaction results in an excited state of the carotenoid and a ground state of the triplet oxygen [149]. Indeed, the lipophilicity of carotenoids allows scavenging peroxyl radicals and forming a resonance stabilized carbon-centered radical (Fig. 7) [182]. Therefore, it is not surprising that carotenoids have a strong ability to protect cellular membranes and lipoproteins from oxidative damage [182]. The absorption of carotenoids is ensured through passive diffusion. However, its bioavailability depends on several factors: (i) an optimal digestion of the food matrix allowing the release of carotenoids, (ii) the formation of lipid micelles in the small intestine, (iii) the uptake of carotenoids by the intestinal microvilli, and (iv) the efficient transport of carotenoids and/or their metabolic products to the lymphatic or portal circulation [183]. After absorption, carotenoids are transported by the chylomicrons to the liver, and are released to the bloodstream thereafter [184]. The hydrocarbon carotenes are carried by VLDL and LDL lipoproteins, whereas the more complexed xanthopylls are taken by HDL [185]. Carotenoids are stored mainly in the adipose tissues and liver. Indeed, adrenal gland, kidney, and testes were reported to contain considerable amounts of carotenoids. In the liver, β-carotenes and provitamin A carotenoids are converted into vitamin A [186]. Interestingly, 1 mg of retinol can be replaced by 2 μg of β-carotene to alleviate vitamin A deficiency in humans [187].

5

Vitamins

Opuntia ficus-indica is enriched with vitamins, mainly ascorbic acid, vitamin B, and α-tocopherol. As summarized in Table 2, vitamins’ concentrations vary among the different Opuntia matrices. The highest vitamin contents were recorded in peels, source of hydro- and fat-soluble vitamins. Ascorbic acid acts as a water-soluble free radical scavenger in both plant and animal tissues. Ascorbate has a reduction potential below that of peroxyl radicals

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Table 2 Distribution and contents of some vitamins in different O. ficus-indica parts (mg/100 g)

Ascorbic acid α-Tocopherol β-Tocopherol γ-Tocopherol σ-Tocopherol Total tocopherols Thiamine Riboflavine Niacine Vitamin K1

Cladodes 7–22 1.76 – – – 2.18

Fruits 1–48 84.9 12.6 7.9 422 527.4

Peels 59.82 1760 222 174 26 2182

Seeds – – – 1.23 – –

Seed oil – 5.6 1.2 33 0.5 40.3

0.14 0.6 0.46 –

– – – 53.2

– – – 109

– – – 52.5

– – – 5.25

References [1, 30, 33, 42, 188–192]

(E°0 ¼ 282 and 1000 mV, respectively) allowing inactivating peroxyl radicals. Indeed, ascorbate’s reduction potential is lower than that of α-tocopherol radical (E°0 ¼ 500 mV), meaning that ascorbate may have an additional role in the regeneration of oxidized α-tocopherol. Although ascorbate seems to be a strong antioxidant, this is not always true. Ascorbate is a potent prooxidant, especially at low pH, in the presence of free transition metals or iron-binding protein, leading to the conversion of hydrogen and lipid peroxides into free radicals. In living tissues, these prooxidative reactions don’t occur regularly thanks to the tight control of free metals by systems that prevent metal reduction and reactivity. However, in foods, the typical control of metals can be lost by processing operations that cause protein denaturation. Oxidative reactions can be, therefore, accelerated [149]. Vitamin E or α-tocopherol is a plant phenolic required in the diet of humans and animals. Tocopherols are a group of phenolic free radical scavenger isomers (α, β, δ, and γ). Interactions between tocopherols and fatty acid peroxyl radicals produce fatty acid hydroperoxides and several resonance structures of tocopheroxyl radicals. These later can mediate reactions with themselves or with other compounds leading to the generation of diverse products, depending on the oxidation rates, radical species, lipid state (e.g., bulk vs. membrane lipids), and tocopherol concentrations. When the oxidation rate is low rates in lipid membrane systems, two tocopheroxyl radicals initiate reaction and lead to the formation of tocopherylquinone and the regeneration of tocopherol. Tocopherylquinone can also be regenerated back to tocopherol in the presence of reducing agents (such as ascorbic acid). In addition, tocopherol dimers can also be formed through the interaction of two tocopheroxyl radicals [149].

6

Biothiols

Biological thiols (biothiols) are an important functional biomolecules, referred as alkyl mercaptans. Their basic structure includes one or more SH groups and resembles to that of alcohols. It is generated by replacing the OH group by the SH one. Thiols are

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Fig. 8 Direct radical scavenging by glutathione

found in nature and are among the most important antioxidants that protect human cells against oxidative damage [193]. In recent decades, it has been shown that metabolic disorders of biothiols lead to extreme damage in humans and animals [194, 195]. The important biothiols include glutathione (GSH), cysteine (Cys) and lipoic acid. Glutathione is a tripeptide (γ-glutamyl-cysteinylglycine) where cysteine can be in either the reduced or the oxidized glutathione state. Reduced glutathione inhibits lipid oxidation in two ways: (i) directly by quenching free radicals to form a relatively unstable sulfhydryl radical (Fig. 8), (ii) indirectly as an electron donator, which allows glutathione peroxidase to decompose hydrogen and lipid peroxides. The bioavailability of glutathione in rats has also been reported to be low. This may be due to the hydrolysis of the tripeptide by gastrointestinal protease [149]. O. ficus-indica fruits were reported to contain considerable amounts of GSH ranging from 3.4 to 8.1 nmol/g edible pulp [33], which is greater than those quantified in mango, strawberry, grapefruit, and papaya [196]. GSH amounts are higher in the yellow cultivars than those in red and white cultivars. However, the white cultivar was found to contain greater Cys contents than the red and the yellow ones (1.21, 0.77, and 0.72 mg/100 g, respectively) [33]. Although they are important bioactive molecules, there is lack of reports regarding the biothiols contents in O. ficus-indica. Further investigations are need.

7

Taurine

Taurine (C2H7NO3S) is an organic osmolyte, and one of the few amino acids which are not incorporated into proteins. Taurine is one of the ubiquitous amino acids of the brain, retina, muscle, and organs throughout the body. Taurine, considered a cell-

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protective β-amino acid [197, 198] with antioxidative effects [199, 200], is involved in a huge number of functions, from development to cytoprotection. All ocular tissues contain taurine, which is the most abundant amino acid in the retina, vitreous, lens, cornea, iris, and ciliary body. In the retina, taurine is critical for photoreceptor development and acts as a cytoprotectant against stress-related neuronal damage and other pathological conditions [201]. Taurine deficiency is associated with cardiomyopathy, renal dysfunction, developmental abnormalities, and severe damage to retinal neurons [201]. In contrast to the majority of other fruits, high amounts of taurine have been reported in cactus pear cultivars from Mexico and South Africa [202]. Fernández-López and his co-authors [32] and Tesoriere and his collaborators [33] reported amounts ranging from of 7.7 to 11.7 mg/100 g in yellow O. ficus-indica cultivars, and lower amounts in red and white cultivars. Taurine contents in cladodes, peels, and seeds need to be investigated.

8

Fatty Acids

Total lipids were assessed in different vegetative parts of O. ficus-indica using chromatographic approaches (Table 3). Linoleic acid (C18:2, ω-6 fatty acid) was shown to be the major polyunsaturated fatty acid in cladodes, and contributes for 32.83% of the total fatty acid content. Linolenic acid (C18:3, as ω-3 fatty acid), palmitic acid (C16:0), oleic acid (C18:1), and linoleic acid (C18:2) represent together over 90% of total fatty acids in cladodes [203]. In fruits, monounsaturated and polyunsaturated fatty acids contents ranged from 16.9% to 40.2% and 35.2% to 53.9% of the total fatty acid content, respectively. Peels contain lower amounts of monounsaturated fatty acids (6.90–31%), but are higher of polyunsaturated ones (37.0–63.2%) [204]. Similarly, seed oil contains high amounts in polyunsaturated fatty acids (57.90–63.29%), but low contents of monounsaturated ones (19.81–23.30%) [205]. Interestingly, linoleic acid is the most abundant fatty acid in fruits, peels, and seed oil. Its relative content is higher in peels than that recorded in fruits [204]. Moreover, cactus seed oil contains about 0.39% of very long-chain saturated fatty acids which are fatty acids with chain length exceeding 20 carbons. These fatty acids are important constituents and intermediates of the cuticular surface layers of plant tissues [206]. The consumption of monounsaturated and polyunsaturated fatty acids has been recommended for its health-promoting properties. Nowadays, there is clinical evidence that PUFAs are able to alleviate symptoms of some diseases such as coronary heart, stroke, and rheumatoid arthritis [209]. They also contribute to improve various health conditions related to obesity, diabetes mellitus, and even some types of cancer [210, 211]. After consumption, linoleic acid, or ω-6 fatty acid, is converted into precursors of eicosanoids, essentials for vascularization, and for blood coagulation. In addition, beneficial properties for skin were described [212, 213]. Linolenic acid or ω-3 fatty acid is also present in appreciable level (ca. 0.5%). This fatty acid is important in the prevention of coronary heart disease and cancer [214]. These reports

Peels Seeds Seed oil

Fatty acid Cladodes Fruits

C12:0 1.33 0.46– 3.92 0.71 – –

C14:0 1.96 1.44– 2.55 1.95 0.14 –

C16:0 13.87 18.2– 29.0 23.1 12.24 9.32– 20.1

2.48 0.38 1.42– 1.80

C16:1 0.24 N.D.

C18:0 3.33 3.77– 6.90 2.67 3.69 2.72– 3.11

C18:1 11.16 16.9– 40.2 24.1 12.51 16.77– 18.3

C18:2 34.87 20.2– 27.0 32.3 56.63 53.5– 70.29

C18:3 33.23 10.8– 20.8 9.27 0.47 2.58 – 0.24

– 0.36 –

0.5 0.19 –

C20:1 C22:0 – – – –

C20:0 – 4.55

Table 3 Fatty acid composition of O. ficus-indica cladodes, fruits, peels, and seed oil (g/100 g FA)

– 0.05 –

– 0.14 –

C22:1 C24:0 – – – –

0.41 – –

[189] [207] [203, 208]

C24:1 References – [203] – [204]

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motivate the possible use of cactus peels and seed oil as a natural source of PUFAs for nutritional, industrial, and pharmaceutical purposes.

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Phytosterols

Sterols, also known as steroid alcohols, are a subgroup of steroids with a hydroxyl group at the 3-position of the A-ring (Fig. 9). The hydroxyl group on the A ring is polar. The rest of the aliphatic chain is nonpolar. Sterols are amphipathic lipids produced from acetyl-coenzyme A [215]. Sterols occur in the membranes of plants, animals, and microorganisms and are called phytosterols, zoosterols, and mycosterols, respectively. Cholesterol is the most known zoosterol. Phytosterols include campesterol, sitosterol, and stigmasterol. β-sitosterol has been reported to be the most important sterol isolated from fruit oil and pulp, peel, and seeds of O. ficus-indica, with contents varying from 6.75 to 21.1 g/kg [190, 203]. Campesterol was extracted from fruits, peels, and seeds with amounts ranging from 1.66 to 8.76 g/kg. Small amounts of other phytosterols such as lanosterol, stigmasterol, Δ5-Avenasterol, Δ7-Avenasterol, and ergosterol were also reported (Table 4). Ergosterol (ergosta-5,7,22-trien-3β-ol) is the sterol characteristic of cell membranes of fungi and protozoa. It undertakes the same roles of cholesterol in animal cells. In human nutrition, ergosterol is a provitamin of vitamin D2. Surprisingly, ergosterol was found in Opuntia peels in small amounts. This may be an indicator of some fungi living in symbiosis. In cladodes, phytosterols content is highly impacted by the stage of maturity. Figueroa-Pérez and his collaborators reported values of 24.3, 33.2, and 18.7 mM Eq/g, respectively, for young, mature, and old cladodes. The decreased content of phytosterols in old cladodes may be Fig. 9 Basic structure of sterols

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Table 4 Phytosterols from O. ficus-indica (g/kg) Sterol β-Sitosterol Campesterol Campestanol Lanosterol Stigmasterol Δ5-Avenasterol Δ7-Avenasterol Fucosterol Ergosterol

Cladodes 16.53 5.7 6.4 – 14.03 7.26 11.6 – –

Fruits 11.2 8.74 – 0.76 0.73 1.43 – – –

Peels 21.1 8.76 – 1.66 2.12 2.71 – – 0.68

Seeds 6.75 1.66 – 0.28 0.30 0.29 0.05 – –

Seed oil 2.80 0.51 – – N.D. –

References [39, 189, 190, 192]

0.27 –

attributed to their conversion into steroidal hormones and vitamins, which regulate growth and development of immature tissues in plants [34]. Sterols are involved in the formation of liquid-ordered (lo) membrane states (lipid “rafts” [216] that are supposed to play an important role in infectious diseases, signal transduction, cytoskeleton reorganization, asymmetric growth, and cellular sorting. They have been proposed as key molecules to maintain the fluidity steady-state of membranes, optimal for function [217, 218]. Phytosterols were also associated with a reduction in common cancers, such as cancers of the colon, breast, and prostate. For instance, phystosterols were reported to boost the immune recognition of the cancer, influence hormonal dependent growth of endocrine cancers, induce apoptosis, and inhibit tumor growth and metastasis [215].

10

Saponins

Saponins are naturally occurring glycosides known for the soap-like foaming, and therefore, they produce foams when shaken in aqueous solutions. While saponins can be structurally defined as a combination between an aglycone, or sapogenin unit, linked to one or more sugar chains at C3 (Fig. 10), the nature of the aglycone allows defining three groups of saponins: (1) saponins containing a steroidal aglycone, (2) saponins containing a triterpenoid aglycone, and (3) saponins containing an alkaloid aglycone [219]. Scientific literature reported that saponins exhibited a large spectrum of biological activities including antibacterial [220], antifungal [221], antiviral [222], insecticidal [223], anti-inflammatory [224], cytotoxic [225], and antiproliferative effect [226]. Saponins in O. ficus-indica need more investigations. Halmi and his collaborators [227] revealed the presence of saponins in the aqueous extract of O. ficus-indica cladodes. Touré and his co-authors [228] reported amounts of 20.4, 6.36, and 8.72 g/ kg for seeds, peels, and cladodes, respectively. Figueroa-Pérez and his collaborators [39] reported higher amounts in cladodes, averaging at 28.13 g equivalents/kg. Noteworthy, they concluded that young and mature cladodes recorded high saponins content than their old counterparts. The saponins profile in O. ficus-indica cladodes is defined by the

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Fig. 10 Basic structure of saponins

presence of sitosteryl 3β-D-glucopyranoside, stigmasteryl 3β-D-glucopyranoside, and campesteryl 3β-D-glucopyranoside, respectively, at 39.1%, 21%, and 17.9%. Despite these findings, further investigations are needed to define saponins profile in O. ficusindica fruits and peels.

11

Global Antioxidant Activity

The antioxidant activity of three O. ficus-indica f. inermis matrices (cladodes, fruits, and peels) was screened using the free radical DPPH reduction method. Our findings showed that the highest antioxidant activity was recorded for Opuntia peels, followed by cladodes at different ages, then fruits. Indeed, cladodes’ antiradical activity varies significantly with age, and it seems that only ascorbic acid contributes significantly to this variance [42]. To understand the antioxidant properties in relation to the different classes of phytochemicals, Pearson pairwise correlations were calculated between the antioxidant activity, total phenolics, flavonoids, betacyanins, betaxanthins, and ascorbic acid. Our findings showed that the antioxidant activity was highly correlated with total phenolics, flavonoid, betacyanins, and betaxanthins. Surprisingly, no correlation between ascorbate and the antioxidant activity was found [42]. In this direction, Fernández-López et al. [32] and Stintzing et al. [157] confirmed that ascorbic acid did not contribute to the radical scavenging activity of cactus pear fruits. All of these findings show clearly that ascorbic acid is not involved in the antioxidant activity of

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the peels, fruits, as well as cladodes, and lead to suggest a high solicitation of ascorbic acid in plant. However, the correlation matrix should be extended to include the contents of the other bioactive phytochemicals. Hence, more concise conclusions would be drawn.

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Conclusions

“Back to nature” is the nowadays’ motto revealed by both researchers and citizens. “Back to nature” implies an increased interest in natural healing and attests a revolution of the green chemistry and the phytomedicine, a use of new approaches to the concept of health promotion, wellness, illness treatment, and drug development. Day by day, healthy lifestyle and diet are strongly recommended by scientists, to keep a healthy body. A healthy diet means, inter alia, a regular consumption of fruits and vegetables in order to reduce the risk of chronic diseases. Such protective role is ascribed to the interaction of a myriad of bioactive phytochemicals. Opuntia ficus-indica (L.) Mill. has been exploited for a long time, in the traditional medicine, and recently, for its beneficial bioactive molecules. Research investigations revealed a wonderful combination between phenolic acids, flavonoids, betacyanins, betaxanthins, carotenoids, different vitamins, saponins, phytosterols, biothiols, and fatty acids. Besides, the nutritionists have described a diversity of nutrients including sugars, amino acids, fibers, and minerals. All of these compounds make Opuntia cacti not only a functional and as a nutraceutical food, but also a valuable source that supplies active principles and adjuvants for pharmacy, promising pigments for industry, and cladodes for green energy (bioethanol and biogas) production. Lastly, further studies on the valorization of Opuntia peels should be performed. The complete profiling of the bioactive molecules in flowers and seed should be established in order to ascertain their possible therapeutic applications.

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Bioactive Compounds of Swahili [Cyphostemma adenocaule (Steud. ex A. Rich.) Desc. ex Wild and R.B. Drumm.]

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Oluwasesan Micheal Bello, Abiodun Busuyi Ogbesejana, Oluwasogo A. Dada, Oluwatoyin E. Bello, and Mojeed O. Bello

Contents 1 2 3 4

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nutritional Importance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Phytochemistry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Bioactive Compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1 Pentacyclic Triterpenes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2 Carotenoids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3 Coumarins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4 Polyphenols . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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O. M. Bello (*) National Center for Natural Products Research, School of Pharmacy, The University of Mississippi, University, MS, USA Department of Applied Chemistry, Faculty of Physical Sciences, Federal University, Dutsin-Ma, Katsina, Nigeria e-mail: [email protected] A. B. Ogbesejana Department of Applied Chemistry, Federal University Dutsin-Ma, Dutsin-Ma, Nigeria O. A. Dada Industrial Chemistry Unit, Department of Physical Sciences, Nanotechnology Laboratory, Landmark University Omu-aran, Omu-Aran, Kwara State, Nigeria e-mail: [email protected] O. E. Bello Department of Crop Protection, University of Ilorin, Ilorin, Nigeria M. O. Bello Department of Chemistry, University of Ilorin, Ilorin, Nigeria e-mail: [email protected] © Springer Nature Switzerland AG 2021 H. N. Murthy, K. Y. Paek (eds.), Bioactive Compounds in Underutilized Vegetables and Legumes, Reference Series in Phytochemistry, https://doi.org/10.1007/978-3-030-57415-4_11

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Abstract

Food from plants and its parts have often been an easy answer to micronutrient deficiencies and undernourishment problems experienced especially in the developing nations of the world. Alongside the well-known and cultivated vegetables, there exist a large number of noncultivated, wild, and neglected vegetables. Revalorizing these plants’ species is a necessity and must in recent times to validate their importance especially exposing their inherent phytocompounds. Cyphostemma adenocaule is commonly known as Swahili, one of such neglected vegetable, eaten by rural people in most countries of West Africa. Phytochemistry of C. adenocaule shows only 12 compounds have been isolated from it, these include ceanothane-type triterpenoids though quantification for polyphenols, flavonoids, and phenolics have been reported. These identified compounds have been reported to have health-promoting ability. This overview reports the importance of Swahili and gives evidences why this vegetable needs to be explore more and not neglected. Keywords

Ceanothane-type triterpenoids · Cyphostemma adenocaule · Micronutrients · Neglected vegetables Abbreviations

ABTS ATPases

CAT DPPH EthOs OATD PCNA and Ki67 ROS SOD TPA UIVs

1

2,20 -azino-bis (3-ethylbenzothiazoline-6-sulfonic acid are a group of enzymes that catalyze the hydrolysis of a phosphate bond in adenosine triphosphate (ATP) to form adenosine diphosphate (ADP) catalase 2,2-diphenyl-1-picrylhydrazyl e-theses online service Open Access Theses and Dissertations popular proliferation marker Reactive oxidative species Superoxide dismutase 12-O-tetradecanoylphorbol-13-acetate Underutilized and indigenous vegetables

Introduction

A recent and meaningful collection of studies will be needed to establish linkages between biodiversity, food, and nutrition. Lack of nutritional and agronomic knowledge, negative attitude to traditional indigenous foods (known as “food for the poor”), policies that do not adequately recognize that plant foods have a significant role for human health and against food insecurity, and a shortage of supports and advocates and champions to foster wild and indigenous foods are all obvious restraints [1–5]. Food systems from traditional and local origin can easily be lost, reiterating the

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Bioactive Compounds of Swahili [Cyphostemma adenocaule (Steud. ex. . .

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necessity for prompt evidence, compilation and propagation of the eroding knowledge of species diversity, and the use of food culture for advocating sustainable diets [2, 6– 9]. Indigenous foods ignored and neglected by those in the food sectors and agriculture as well as by urban clienteles can be an essential component in alleviating malnutrition, food shortage, hunger, and environmental conservation [10–12]. Plants are a priceless bequest to human race, in mostly developing nations of the world; the rural populace depends on noncultivated edible plants and parts of these plants to meet their daily nutritional requirements and food security. Nigeria, being one of the developing nations, is blessed with different climatic conditions; it has a huge collection of noncultivated, wild, and underutilized vegetables. Many of which are locally available and are employed as culturally as source of food as they contain micro and macronutrient and phytocompounds which can nourish and also help against some ailments for the ever-growing human populace [4, 7, 8]. These vegetables grow mostly in the wild; they are found growing without any meticulous cultivation or attended needs. They are adaptive, hardy, strong, and can do well under harsh weather conditions than the exotic and popular ones [2, 9]. They have persistently been neglected despite their advantages, i.e., can be cultivated at an abstemiously economical cost and on a poor soil, contain health-promoting compounds [13, 14]. Most rural populace continues to make use of the plants species to enhance nutrition, generate income, and afford food security [14–16]. These wild and underutilized vegetables afford us an essential and important component of human diet, giving the human body more than culinary uses. About 1500 to 2000 various species of plants were employed as vegetables globally, for Southern part of Asia, around 1000 species are known for use as vegetables. Among such, around 120 species are grown for commercially purposes or for private consumption [17, 18]. Cyphostemma adenocaule (Steud. ex A. Rich.) as shown in Fig. 1, is one of these underutilized and indigenous vegetables (UIVs), belongs to the genus Cyphostemma which is narrowly related to Cissus. This genus includes over 240 species; most of these species can be found in sub-Saharan Africa. Cyphostemma belongs to the Vitaceae family, and it is mostly gathered from the wild for use [2–4]. C. adenocaule is commonly called as “Swahili” and eaten in most Africa countries, i.e., Angola, Congo, Eritrea, Ethiopa, Ghana, Nigeria, Senegal, and

Fig. 1 (A) Swahili’s plant (B) leaves (C) tubers

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Uganda; it is grown in Ethiopia. This plant is popular in the savannah regions of tropical Africa, and it is most seen in bushlands, thickets, grasslands with or without sparse trees, rainforests and gallery forests, supplementary forests, sandy banks of rivers, granite rocks, and abandoned farmland [16, 17, 19, 20]. Swahili is an annual herbaceous stem climber hurled from a broad bulbous perennial rootstock (caudex) with slightly fleshy 5-foliolate leaves and branched tendril. The flowers are green and red in color. Swahili’s population is highly variable, ranging from glabrous to strongly pubescent and from nonglandular to heavily glandular [19, 20]. This review summarizes the importance of the secondary metabolites isolated and identified from various parts of Swahili which makes this plant species relevant in the traditional food systems. To collect the literature on Swahili, various queries were made on various search engines, dissertation search engines, journal sites, and plant databases, i.e., “PubMed,” “Scopus,” “Google Scholar,” “Science-Direct,” Web of Science, Elsevier, Plant List, Springer, ProQuest, Open-thesis, EthOs, and OATD. Words like Cissus adenocaulis Steud. ex A. Rich., Cissus serjanioides, Cyphostemma adenocaule, Vitis adenocaulis, and Vitis adenantha were employed.

2

Nutritional Importance

Bello et al. [2] reported that in Uganda, Kenya, Ghana, and DR Congo, the leaves and fruits of Swahili are popular as vegetables, and they are also eaten as soup or salad. The leaves are delicacy eaten with cooked sesames, pigeon peas, groundnuts, and beans. The fruit of Swahili is a delicacy in Côte d’Ivoire and Tanzania; in Ethiopia, the roots are cooked and eaten; in Uganda, the dried roots are stored and eaten during famine times after been pounded. Nutritional facts and antioxidant disposition are some of the main definition for the nutritional quality and healthpromoting ability of plant food [110]. Employing different assays, i.e., DPPH, ABTS, inhibition of lipid peroxidation, hydroxyl radical, hydrogen peroxide, nitric oxide radical, and superoxide radical system. It was reported the polar extract of this plant showed an average anti-oxidative activity in all the assays used [21]. The leaves are found to contain coumarins, saponins, flavonoid glycosides, and carbohydrates; the total flavonoids and total phenol contents were determined by Asso et al. [21]. The authors were satisfied with the results and further recommend that the vegetable should not be neglected. Though the leaves and fruits contain a little content of oxalic acid which is responsible for the faintly acrid taste [109]. Assob et al. [21] confirm Swahili’s nutritional quality.

3

Phytochemistry

Chouna et al. [22] carried out the phytochemical investigation of the polar extract of Swahili; some of the compounds isolated was shown Fig. 2. These secondary metabolites isolated are cyphostemmic acid A (1), zizyberanal acid (2), betulinic

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Bioactive Compounds of Swahili [Cyphostemma adenocaule (Steud. ex. . .

HOH2C

O

COOH

HO

215

COOH

COOH

COOH

COOH 1

HO

2

3 O

HOH2C

COOH CH2OH

HO

HOH2C HO

4

HO

COOH COOH

5

6 O

HOH2C

COOH

HOH2C

COOH

COOH COOH

7

9

8

O

CH2OH HO

HO

HO 10

HO 11

O O

12

HO

Fig. 2 Isolated Compounds from C. adenocaulis

acid (3), cyphostemmic acid B (4), lupeol (5), cyphostemmic acid C (6), epigouanic acid A (7), betulin (8), cyphostemmic acid D (9), 3β, 28-dihydroxy30-norlupan- 20-one (10), β-sitosterol (11), and its glucoside (12) [22]. Al-Duais et al. [23] reportedly identify the presence of some secondary metabolites from C. adenocaule, these are xanthophylls, vitamin C, tocotrienols, carotenoids (carotenes), and tocopherols. The presence of these compounds was further confirmed by other authors [23–25]. Assob et al. [21] reported the presence of flavonoid glycosides, coumarins, and saponins; the authors further quantify the phenolic and flavonoid content in C. adenocaule. The authors fail to identify the specific member of flavonoid and phenolic compounds present in the underutilized vegetable though the antioxidant activity of the C. adenocaule was established employing various assays [21].

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4

Bioactive Compounds

4.1

Pentacyclic Triterpenes

Triterpenes are secondary metabolites found in medicinal plants, vegetables, and fruits; they are a unique class of biologically active compounds that have displayed various pharmacological in both in vivo and in vitro studies [26]. They reputed as the largest and most extensive class of secondary metabolites. The triterpenes identified in Swahili belong to the lupane-type pentacyclic triterpenes mostly consisting of four six-membered rings and one five-membered ring; pentacyclic triterpenes are secondary plant constitutes which are formed from cyclization of squalene [27]. During the past few years, many studies and publications have stressed the wide range of biological activities of these types of triterpenes. However, due to their unique skeleton structure, they possess low water solubility; some of their biological effects include antioxidant, antiangiogenic as well as anti-inflammatory effects and the ability to enhance cell differentiation; these organic compounds are more than ordinary cytotoxic anticancer drug and have been reported appropriate for contemporary cancer approaches. Furthermore, they are considered as vital components of human nutrition because of their chemopreventive ability to defend against some diseases [27–30]. Some of the pentacyclic triterpenes isolated in C. adenocaule are cyphostemmic acid A (1), zizyberanal acid (2), betulinic acid (3), cyphostemmic acid B (4), lupeol (5), cyphostemmic acid C (6), epigouanic acid A (7), betulin (8), and cyphostemmic acid D (9). Among these tripterpenes, lupeol (5), and betulin (8) are renowned and popular as natural products from natural sources employed as health-promoting compounds. Data from research papers propose that triterpenoids, i.e., lupeol (Lup-20 [21]-en3β-ol) (5) and betulin (8) display cytotoxicity against various cancerous cells, e.g., breast, colon, kidney, lung, liver, ovary, and prostate cancers as well as leukemia and melanoma cell lines [30–32]. Some authors have shown the ability of lupeol (5) to slow down the growth of melanoma, human pancreatic, and neck and head cancer in xenograft models of laboratory mice [33–35]. Betulin as well as betulinic acid and lupeol induced the process of melanogenesis in B16 2F2 melanoma cells in mouse [36], for example, lupeol [5]’s cytotoxicity activity was displayed against testosterone-induced prostate development in rats; this was achieved by stimulating apoptosis in the hypodiploid areas and in human tumor prostate source in a xenograft model in rats [37, 38]. New results have disclosed that Lup-20 [21]-en-3β-ol (5) (40 mg/kg bw used 3x/wk) impedes the development of extremely belligerent human metastatic melanoma cells (451Lu) in an athymic nude xenograft model of rat. The immunohistochemical investigation of the tissue extracted from the tumor site showed that animals receiving lupeol (5) displayed PCNA and Ki67-positive cells, signifying the antiproliferative ability of Lup-20 [21]-en-3β-ol (5) [39]. From many studies, it can be noticed that lupeol (5) displayed inhibition against large range of cancers, i.e., pancreatic, liver, leukemia, prostate, and skin cancer, by employing different mechanism either by inducing apoptosis or lowering the levels of anti-apoptotic proteins [37–39].

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Reactive oxidative species (ROS) have been popular in playing active dual functions by been deadly yet helpful species. Highly regulated enzymes usually produced ROS, and they preserve require concentrations and give physiological effects, for instance, in the responses of the cells to noxia or in the immune responses’ regulation [40–42]. Oxidative stress is the basis of overproduction of these latter, and this can be an essential go-between of cell structures’ damage. Pentacyclic triterpenes especially lupeol (5), betulin (6), and ursolic acid are renowned for their antioxidant activity. They are compounds that display antioxidant effects through various mechanisms [41–43]. These class of organic compounds activate the system of enzymes by intensifying the activity of CAT as well as SOD and glutathione peroxidase and glutathione S-transferase [41–45]. One of the antioxidant effects of lupeol was authenticated in the case of hyperoxaluria in laboratory mice [45]. Just like lupeol (5), betulin (6) (35 mg/kg bw daily/21 days) controls the glutathione level, reduces the peroxidation reaction of lipid of erythrocyte membrane, controls the activity of membrane bound ATPases, and increases the activity of the SOD and CAT [46–48]. Lupeol has shown many encouraging activity and has been patented as an essential ingredient in cosmetic formation to help against tissue degeneration [49], an antifungal agent [50] and an antitumor agent [51]. There is also much work discovered on the cytoprotective activity of triterpene acids and betulin (6). Although most triterpenes are popular as anti-inflammatory agents especially lupeol (5) and its analogue, i.e., betulin (6) and betulinic acid. Oleananes, ursanes, and lupanes smeared topically or orally displayed important anti-inflammatory effects in vitro and in vivo. This was validated in carrageenan, croton oil, or serotonin stimulated paw/ear edema tests, 12-O-tetradecanoylphorbol-13-acetate (TPA) and also in arthritic mice models, and various underlying mechanisms have been proposed [52–57]. The anti-inflammatory potency of lupeol (5) has been compared with acetylsalicyclic acid either orally or intraperitoneally [58, 59], both exhibit neither gastric side effects nor toxicity [60, 61]. Lupeol (5) have been exhibited significant anti-inflammatory activity in laboratory mice by 50% when smeared topically at 1 mg [62]. In detail, lupeol (5) shows undoubted effects especially on persistent inflammatory diseases but mostly as a chemoprotective agent. Most of the beneficial pentacyclic triterpenoids, i.e., betulin (6), lupeol (5), and ursolic acid have few benefits over other phytoconstituents because they have no obvious side effects [60, 61].

4.2

Carotenoids

Carotenoids are naturally occurring compounds popularly found in plants and many photosynthetic entities such as fungi, algae, and bacteria [63]; studies have suggested that over 600 carotenoids have been known [64]. This class of organic compounds are divided into two major groups, namely, xanthophylls and carotenes, although only 14 carotenoids have noticed in human peripheral and plasma tissues through careful uptake in the digestive tract [65, 66]. Carotenes are made of entirely of carbon and hydrogen, e.g., carotene (β, α, γ, δ), phytoene and lycopene, and (ii) the

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oxygenated derivatives of these constituents are known as xanthophylls, e.g., zeaxanthin, lutein, violaxanthin, and astaxanthin [67]. Beta carotene is an upstanding part of the carotenoid family and an abundant orange-red pigment in plants and fruits. β-carotene is known to be the largest carotenoid in human diet and is the primary source of vitamin A in humans. This is a precursor of vitamin A that can generate two molecules of retinol in the presence of oxygen through the action of βcarotene [68]. It is believed that various carotenoids present in different foods, such as β-carotene, lycopene, lutein, and zeaxanthin, play a role in preserving body functions and in preventing disease. β-carotene is a source of provitamin A alongside many other carotenoids [69]. A fat-soluble vitamin called vitamin A is an essential nutrient not only for the vision and the prevention of nyctolapia (night blindness) and xerophthalmia (lack of tears/abnormal dryness) but also promotes better the immune system’s ability to withstand infection, development, proper growth, reproductive system function, and gastrointestinal function. Humans lack the capacity to synthesize vitamin A de novo and must thus receive sufficient quantities from dietary sources, abundant in β-carotene, such as dark green leafy vegetables (e.g., C. adenocaule), fruits [69, 70]. Epidemiological research and clinical studies have identified a range of possible health benefits for β-carotene, e.g., decreased risk of some cancers, heart disease, age-related macular degeneration and cataracts, and improved immune response [71–73].

4.3

Coumarins

Coumarins is a popular class of naturally occurring compounds found in various plant sources which show significant range of biochemical and pharmacological behavior, some of which indicate that the role of some members of coumarin family can considerably impact the role and function of different human cellular systems [74–76]. Coumarins have activities such as antioxidant, anticoagulant, anti-inflammatory, antiviral, anticancer, and so on. And they have great medicinal potential. Several recent reviews summarize advances in coumarins use, in particular with respect to its antioxidant properties [76–78].

4.4

Polyphenols

Polyphenols are the most abundant and diverse group of bioactive molecules and are widely distributed. Polyphenols are of two general groups, one being flavonoids and the other being phenolic acids. Dietary polyphenols which include flavonoids and phenolic compounds are considered to be the primary dietary important constituents in many food substances, vegetables, and fruits, for the prevention of many diseases and aiding health conditions of people. The different but significant activities that polyphenols displayed are usually centered on the functional group on their moiety which has the ability to receive a free radical. Products based on plants which can protect humans against oxidative damage have recently drawn worldwide attention.

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Polyphenols are plant principal group of antioxidant which can minimize body oxidative stress, holding a balance of oxidants and antioxidants due to their free radical scavenging or metal reduction chelating activities. There are rising and huge evidences giving solid credence to the therapeutic and chemopreventive effects of this class of compounds (polyphenols and phenolic compounds) against cardiovascular disease [79–83], obesity [84, 85], diabetes [86–89], osteoporosis [90–92], microbes [93–95], as an antioxidant [94, 96–99] and anticoagulant [100], different types of cancer [101–105], anti-inflammatory [99, 106–108], has invigorated the clinical trials in order to address the mechanism, efficacy, pharmacokinetics, and safety of these compounds in human lives.

5

Conclusion

As the trend, “let your food be medicine and let your medicine be food” is becoming increasingly growing globally, underutilized and indigenous vegetables (UIVs) with chemopreventive and disease-promoting abilities will be the focus of many studies and researches. Pentacyclic triterpenes, coumarins, carotenes, and flavonoids are important bioactive components found and isolated in C. adenocaule. This study identifies some of their chemopreventive abilities against some diseases affecting humans. This review attempt to highlight the nutritive value and health benefits of these compounds hence the inherent advantages that this underutilized and wild vegetables (UIVs) possesses. Other works have emphasized the ethnomedicinal uses of C. adenocaule [2], but this chapter connects its bioactive constituents with human nutrition and underscores the importance of these health-promoting secondary metabolites to mostly rural populace who are plagues with malnutrition-related ailments. C. adenocaule’s phytochemistry is sparse; this calls for concerted effort on research by food scientists, nutritionists, natural products chemists, and pharmacists, so as to justify its immense benefits.

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Bioactive Compounds of Barbados Gooseberry (Pereskia aculeata Mill.)

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Mariana Buranelo Egea and Gavin Pierce

Contents 1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 Nutritional Composition and Antinutritional Factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1 Polysaccharides in P. aculeata Leaves . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Lipids in P. aculeata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3 Phenolic Compounds and Antioxidant Activity in P. aculeata . . . . . . . . . . . . . . . . . . . . . . 3 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Abstract

Pereskia aculeata Mill., a species of the family Cactaceae, is considered a nonconventional leafy vegetable. This species has been consumed mainly for its protein and mineral (iron and calcium) content, and represents a strategy for improving the nutritional value of diets in rural communities. P. aculeata protein is of high quality (with an abundance of the essential amino acids lysine and tryptophan) and high digestibility. Additionally, P. aculeata seems to be a promising thickening ingredient as it is rich in a mucilage, which has potential to serve as a functional food ingredient that contributes to favorable sensory properties and to dietary soluble fiber requirements. Further, P. aculeata leaves are an abundant source of vitamin C, the provitamin A carotenoids α- and β-carotene, and several xanthophylls, including lutein and violaxanthin. Additionally, the P. aculeata essential oil contains several terpenes and terpenoids commonly found M. B. Egea (*) Instituto Federal de Educação, Ciência e Tecnologia Goiano, Rio Verde, GO, Brazil e-mail: [email protected] G. Pierce Departament of Food Science and Technology, Oregon State University, Corvallis, OR, USA e-mail: [email protected] © Springer Nature Switzerland AG 2021 H. N. Murthy, K. Y. Paek (eds.), Bioactive Compounds in Underutilized Vegetables and Legumes, Reference Series in Phytochemistry, https://doi.org/10.1007/978-3-030-57415-4_13

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in herbs and spices used as culinary seasonings and in traditional medicinal practices. The objective of this chapter was to gather information on the active compounds present in P. aculeata leaves that can demonstrate beneficial health effects. Keywords

Cactus · Carotenoids · α-carotene · Hydrocolloid · Leafy vegetable · Lutein · Mucilage · Tryptophan Abbreviations

AI ABTS DPPH FM GAE MRSA PI RAE RDA TBARS

1

Atherogenic index 2,20 -azino-bis (3-ethylbenzothiazoline-6-sulphonic acid) 2,2-diphenyl-1-picrylhydrazyl Fresh matter Gallic acid equivalent Methicillin-resistant Staphylococcus aureus Protection index Retinol activity equivalents Recommended daily allowance Thiobarbituric acid reactive substances

Introduction

Nonconventional vegetables are valuable alternatives to traditional food crops due to their abundant content of macro- and micronutrients. The use of nonconventional vegetables has been increasing, mainly due to the increase in adherence to vegan or vegetarian diets for health reasons, and increasing consumer awareness and concern with climate change [1, 2]. Pereskia aculeata Mill., a species of the family Cactaceae, grows naturally in the American continent, South and Southeast Africa, Northeast and Southeast Australia. It is popularly known as “Barbados Gooseberry” and in Brazil such as “ora-pro-nobis” (Latin, pray-for-us) [3–5]. The flower is perigynous and presents a hypanthium with bracteoles and aculeus. The fruit is pomaceous, type cactídio, with succulent hypanthium, pericarp, and seeds immersed in a yellowish gelatinous mass. The seed is exotestal and develops from an amphitropous, bitegmic, and crassinucelate ovule [6, 7] (Fig. 1). The common edible part is the leaves that has been used in local cuisine as a source of digestible vegetable protein, vitamins, and minerals. In general, the production and commercialization of P. aculeata leaves is still rudimentary, which hinders its establishment as an agricultural crop and value-added commercial product [8–11]. Among the bioactive compounds reported for P. aculeata leaves are phenolic compounds such as caftaric acid, rutin, and narcissin; carotenoids including pro-vitamin A carotenoids and bio-compatible xanthophylls, and

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Fig. 1 Flowers and leaves (a) and ripe fruits (b) of Pereskia aculeata

betalains [12–14], among others, which contribute to the biological activity of this plant. P. aculeata leaves have been used in the interior states of Brazil, mainly in Minas Gerais, as a traditional medicinal treatment for iron deficiency anemia, as a therapeutic agent for cancer, for the prevention or treatment of osteoporosis, and for the treatment of intestinal constipation [15]. However, few studies have yet demonstrated the biochemical components of P. aculeata that contribute to its healing action [16], apoptosis in breast carcinoma [17], antibacterial activity [13], antiinflammatory activity [18], and antinociceptive potential [19]. As this plant has been reported as an important source of nutrients, it can be utilized as a practical vegetable for economically disadvantaged populations of Brazil, both in urban and rural environments to increase their nutrient intake [15, 20]. Several researches have been developing methods to include the leaves of P. aculeata as a functional ingredient in food products such as bread rolls [21], noodles [22], pasta dough [23–25], juices [26], ice cream [27], cake [28, 29], emulsified cooked sausages [30], and milk beverages [31], among others. The objective of this chapter was to gather information on the active compounds present in the leaves of P. aculeata that confer health effects.

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Nutritional Composition and Antinutritional Factors

Table 1 shows the proximal composition P. aculeata leaves on a dry basis. Fresh leaves have an average of ~90% moisture [32], which can hinder its shelf life and utility as a fresh vegetable. The available literature highlights the large amount of proteins (~24%), lipids (4%), and carbohydrates (~40%), with emphasis on the high content of dietary protein (~24%) present in the dried matter. As it is a vegetable source of essential amino acids, P. aculeata leaves may be an important contributor to the protein content of the human diet moving forward, to reflect changes in consumer preferences. A major concern when considering potential plant-based protein sources is the quality of the protein sources provided. Dietary protein quality is rated based on the essential amino acid composition of a protein, as it relates to human needs, in addition to the ability of the protein to be digested, absorbed, and retained by the body [39]. P. aculeata leaves have shown less true protein digestibility (~75%) [40, 41] than casein (96%) [40], however, this value is comparable to other hallmark plant sources of protein such as soy, oat, and quinoa [42]. Additionally, protein digestibility can be modified with different methods of Table 1 Chemical composition of P. aculeata leaves Average Macronutrients Moisture (g 100 g1) Protein (g 100 g1) Lipid (g 100 g1) Ash (g 100 g1) Carbohydrate (g 100 g1) Total dietary fiber (g 100 g1) Soluble fiber (g 100 g1) Insoluble fiber (g 100 g1) Energy (g 100 g1) Total sugar (g 100 g1) Uronic acid (g 100 g1) Micronutrients Iron (mg 100 g1) Zinc (mg 100 g1) Calcium (mg 100 g1) Magnesium (mg 100 g1) Phosphorus (mg 100 g1) Potassium (mg 100 g1) Copper (mg 100 g1) Boron (mg 100 g1) Manganese (mg 100 g1) Sulphur (mg 100 g1)

Median

Range

8.3 23.8

7.6 22.9

5.9–12.5 12.4–40.7

4.0 16.6 43.7 30.2

3.7 16.1 45.5 39.1

2.4–5.2 14.8–18.8 29.5–59.0 8.7–41.8

4.3 29.0 288.2 48.0 26.0

5.2 33.9 271.8

2.4–5.2 19.2–33.9 269.2–323.6

19.8 5.7 2679.3 1065.3 447.4 3266.0 0.7 4.1 23.6 640.8

15.6 5.9 2880.0 680.0 320.0 3380.0 0.9 4.1 24.5 716.7

9.4–38.7 4.0–7.3 1346.7–3660.0 450.0–2560.0 150.0–1130.0 2420.0–3910.0 0.1–1.2 2.8–5.5 2.8–43.5 150.0–980.0

References [21, 24, 25, 30, 33, 34] [21, 22, 24, 25, 30, 32– 35] [21, 24, 25, 30, 32–34] [21, 24, 25, 30, 32–34] [21, 24, 25, 33, 34] [21, 25, 32, 34, 36] [32, 34, 36] [32, 34, 36] [21, 24, 33] [35] [35] [23, 25, 37] [23, 37] [23, 25, 37, 38] [23, 25, 37, 38] [23, 25, 37, 38] [23, 25, 37, 38] [23, 37] [23, 37] [23, 37, 38] [23, 25]

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food preparation, such as cooking time or drying [32, 43], and may be underestimated since fermentable fibers increase the activity of intestine microbiome and may indirectly increase protein digestibility [40]. The amino acid profile (mg g1 of protein) of P. aculeata leaves can contain different amounts of phenylanine + tyrosine (53.7 and 84.4), leucine (69.0 and 66.3), valine (50.1), lysine (53.4 and 41.7), isoleucine (36.9 and 40.87), threonine (30 and 36.64), methionine + cystine (17.18 and 22.26), histidine (24.0 and 16.23), and tryptophan (21.1 and 5.10), as reported by Zem et al. [40] and Silveira et al. [41], respectively. Silveira et al. [41] highlight the presence of leucine (6.96%), lysine (5.37%), and phenylalanine (5.02%), while Takeiti et al. [32] and Zem et al. [40] highlight tryptophan in P. aculeata leaves. This amino acid profile demonstrates that this leaf has similar essential amino acids to legumes, mainly for lysine (high in beans) and tryptophan (high in garbanzo). Still, proteins from Pereskia are classified as incomplete, as they are insufficient sources of some essential amino acids [41]. This highlights the importance of a diverse diet in order to obtain the full spectrum of essential amino acids. For adults between 19 and 50 years old, the contribution of 40 grams of P. aculeata dried leaves to the RDA for micronutrients for females and males [44], respectively is 524 and 410% of manganese, 107% of calcium (for both genders), 137% and 107% of magnesium, 50% and 38% of potassium, 44% and 99% of iron, 26% of phosphorus (for both genders), and 29% and 21% of zinc. P. aculeata leaves appear to be an excellent source of minerals and may even serve as a food supplement in areas where human malnutrition is a problem. Vegetarian and vegan diets often contain low amounts of calcium that can be resolved with ingestion of 40 grams (~2 spoons) of P. aculeata dried leaves. Dietary calcium optimizes bone density and protect against bone resorption reducing risk of osteoporosis [45, 46]. P. aculeata leaves showed ~20 mg 100 g1 FM of folic acid, ~186 mg 100 g1 FM of vitamin C (determined using titration method) [32], and 439 μg 100 g1 FM of vitamin E including α-tocopherol was the major 91%, followed by γ-tocopherol (5%), α-tocotrienol (3%), and β-tocopherol (1%) [47]. The antinutritional factors studied for P. aculeata are oxalic acid, saponins, trypsin-inhibiting tannins, and hemagglutination activity. Oxalic acid has been reported between 41 and 99 mg 100 g1, total tannins between 1813 and 3804 mg 100 g1, trypsin inhibitory activity between 0.2 and 1.8 UTI mg1, saponins of 0.3 mg 100 g1, and no hemagglutination activity [34, 41, 43]. Although it has become better known and introduced in food recently and there is a concern with the presence of antinutrients and alkaloids, the toxicity of P. aculeata extracts against the liver primary culture PLP2 [13] or growth and development of Wistar rats has not been reported [37], demonstrating that it is safe for human consumption.

2.1

Polysaccharides in P. aculeata Leaves

P. aculeata leaves and fruits have been reported as a plant source of hydrocolloids that are commonly referred to as mucilage. This mucilage mainly contains type I

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arabinogalactan with partially esterified galacturonic acid and fucose, and to a lesser extent galactose, rhamnose, and galacturonic acid, which are highly ramified [35, 48–50]. The composition of the mucilage from P. aculeata leaves has been linked to wound healing properties [16, 51, 52]. The P. aculeata mucilage generally contains the saccharides arabinose, galactose, rhamnose, and galacturonic acid in a mole ratio of 5.1: 8.2: 1.8: 10 [48]. The mucilage contains abundant carboxyl groups, which may serve as ion binding sites that contribute to its gel-forming ability (ability to interact with water to form a proper gel) [53]. Under standard conditions, P. aculeata hydrocolloids obtained by hot water extraction exhibits apparent viscosity values that decrease with the shear rate until stabilization (pseudoplastic fluid) and thixotropic behavior that increases with relation to mucilage concentration. The addition of salts to P. aculeata mucilage decreases viscosity by the presence of positive ions that reduce repulsion and molecule expansion. Conversely, viscosity and thermal stability are increased by the presence of sucrose [54]. The mucilage of P. aculeata possesses characteristics similar to Arabic gum and cashew gum, which are commonly utilized in the food industry as a beverage thickener and to replace fat in fermented milk products [31]. Addition of this arabinose- and galactose-rich mucilage to films provides increased tolerance to salinity, but the surface of the films the demonstrated the low capacity of the binding of Arabic gum over the fibers of cellulose [55, 56]. The dietary fiber content in the leaves of P. aculeata is ~23 g 100 g1. P. aculeata has been extensively utilized in traditional medicine for its beneficial health effects. Among the applications of this plant, the literature has highlighted it as a source of bioactive fiber, with the potential to increase intestinal motility, reduce total body weight and visceral fat gain, increase the protection index (PI), and reduce the Atherogenic index (AI) (per Lee index) to confer heart protection, as has been demonstrated in mice [33]. The beneficial properties of the fiber were confirmed by Vieira et al. [57], in their in vivo study (men, 20–50 years old) which found the improvement of gastrointestinal symptom rating scores, flatulence reduction, and increase of satiety when cookies with P. aculeata flour (36 g of cookie providing 6.42 g fiber day1) were consumed during a14-week period.

2.2

Lipids in P. aculeata

Lipids comprise 0.4% of fresh P. aculeata leaves, and ~4.0% of the dried leaf matter (Table 1), as determined using the Soxhlet method [32]. These levels are comparable to other leafy green vegetables, as lipids represent 0.4% of the weight of fresh spinach leaves (Spinacia oleaceae). Hydrodistillation of the dried leaves yielded 0.02% essential oil, indicating that P. aculeata leaves primarily contain non-volatile lipids. Modest quantities of tocopherols and tocotrienols have been found in fresh P. aculeata leaves (436.68 μg 100 g1). While the quantities of tocopherols and tocotrienols are unlikely to represent a significant contribution to the human diet,

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the primary vitamin E compound found in tested samples was α tocopherol, the most bioactive vitamin E molecule, at 400.34 μg 100 g1 [18].

2.2.1 P. aculeata Essential Oils The composition of the essential oil on P. aculeata leaf lipids consists of monoterpenes, diterpenes, hydrocarbons, and select fatty acids. Dietary fatty acids found in P. aculeata leaves are primarily palmitic acid (16:0) and linoleic acid (18:1, ω-6) [58, 59]. The essential oil of P. aculeata leaves consist primarily of terpenes and terpenoids. Many of the terpenes and terpenoids present within P. aculeata are found in common medicinal plants, herbs, and spices. Essential oils constitute a minor portion of P. aculeata, leaves, but they may represent a contributor to the bioactive properties of the vegetable in vivo. Hydrodistillation of dried P. aculeata yields 0.02–0.03% of essential oils, comprised of 30 compounds. The composition of the P. aculeata leaves appear to be highly variable, as samples collected from the same campus (Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil) at the same time of year (October), from the same lab had dramatically different composition when harvested two years apart. Whether these differences are due to differences in the annual weather or inter or intra-plant differences remains to be determined. Two dietary fatty acids, linoleate and palmitate, are found in the essential oil. The remaining compounds in the essential oil include oxygenated monoterpenes, oxygenated sesquiterpenes, oxygenated diterpenes, diterpene hydrocarbons, hydrocarbons, and phytol. Aside from fatty acids, the most abundant compounds in samples analyzed are phytol (29.4%) or acorone (30%) depending on the study used for reference. As both the samples in Table 2 are from the same lab, it is possible that the acute differences in lipid composition are due to annual changes in weather. The essential oil has been demonstrated to act as a bactericidal to Bacillus cereus, Bacillus subtilis, and Staphylococcus epidermidis ATCC 25923 at 100 μg/mL, although it does not appear to act as a bactericidal agent towards Gram-negative bacteria [59]. 2.2.2 Carotenoids The leaves and fruit of P. aculeata are both exceptionally rich in carotenoids, rivaling other common dietary sources (Table 3). The leaves of P. aculeata are especially rich in the xanthophylls, lutein, and zeaxanthin, while the fruits are rich in both α- and β-carotene, thus providing pro-vitamin A activity. A useful tool for determining the vitamin A activity of foods and supplements is retinol activity equivalents (RAE), where the standard is 1 μg of retinol. Absorption of carotenes is critical for vitamin A activity to be obtained, with dietary fats facilitating the absorption of carotenes. β-carotene is absorbed more readily than α-carotene, and thus confers greater provitamin A activity, Supplemental carotenes are not bound in a food matrix, and are absorbed six times higher than dietary carotenoids, and so dietary β-carotene has a RAE ration of 12:1, and αcarotene has a RAE of 24:1. The presence of abundant α-carotene is relatively uncommon in popular edible fruits. Leaf carotenoids appear to fluctuate in response to sunlight, with shady conditions favoring increased production of all

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Table 2 Lipids in essential oil of Pereskia aculeata obtained via hydrodistillation (mg 100 g1) Essential oil compounds (5E,9E)-Farnesyl acetone (E)-β-Ionone (Z )-3-Hexenyl salicylate (Z,Z)-Methyl-4,6-hexadecanolide 14-Hydroxy-(Z )-caryophyllene 14-Hydroxy-4,5-dihydro-caryophylle 14-Hydroxy-9-epi-(E)-caryophyllene 1-Hexadecene 1-Nonadecen-ol 1-Octadecene 1-Tetradecene 2-Hexyl-(E)-cinnamaldehyde 2-Ethylhexyl salicylate 6-Methyl-α-ionone Acorone ar-Tumerone Caryophyllene oxide cis-Dihydro-mayurone cis-Thujopsenal Citronellyl butyrate Cyclopentadecanolide Dihydro-β-agarofurann Ethyl hexadecanoate Eudesma-4(15),7-dien-1β-ol Heptadecane Hexadecanoic acid Isopropyl hexadecanoate Linoleic acid Methyl hexadecanoate Methyl isovalerate Methyl linoleate Methyl octadecenoate n-Eicosane n-Hexadecene n-Octadecane Nonadecane n-Pentadecane Phytol α-Cadinol α-Muurolol

[59] 0.1

0.6 1.6 0.6 0.3 6.18

[58] 5.70 0.75 0.17 16.34 0.29 0.28

0.62 0.2 0.60 1.73 7.2

0.3 Trace 0.9 0.3 Trace 0.6 0.3 1.9 17.4 0.7 12.7 2.6 0.4 3.0 2.9 1.3 1.0 2.9 0.3 29.4 0.9 0.5

30.0 1.10 0.51 0.17

5.48 0.57

0.42 4.74 4.92 4.44 0.69

5.11 0.22

carotenoids measured. Total carotenoids shifted from 119 μg g1 in the leaves when grown in full sun to 210 μg g1 when grown in half shade. The profound difference in leaf carotenoid content suggests that growing methods could be

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Table 3 Carotenoids in P. aculeata leaves and berries (μg g1) Compounds Lutein α-carotene α-cryptoxanthin/ zeaxanthin (allE)β-carotene (9Z)β-carotene (13Z)β-carotene Cis-β-carotene Neoxanthin Violaxanthin Lutein-like Zeaxanthin-like Total

Leaves, sun [14] 57.4 3.8

Leaves, shade [14] 102 11.9

Berries [14] 2.3 18.9

Berries [61] 6.5 22.7 2.7

18.6 3.0 0.7

35.1 5.1 2.9

29.2

34.3

9.3 20.0 2.5 3.3 186

16.1 27.3 5.0 5.3 375

3.0 2.8

53.3

71.7

manipulated to yield exceptionally high-carotenoid leaves, for use as a vegetable or dietary supplement [14]. The quantity of xanthophylls in the leaves is substantial. Lutein and zeaxanthin are known to aculeate in the macula to protect the eye from blue light [60]. Although xanthophylls do not have any provitamin-A activity, their biocompatibility and protective properties in vivo have prompted the production of lutein + zeaxanthin supplements, which generally contain up to 20 mg of lutein, approximately the same amount as is supplied by 100 g of cooked kale (18 mg). Raw shade-grown P. aculeata leaves contain over five times as much lutein as cooked kale leaves, making this vegetable a richer source of lutein than any commonly consumed leafy vegetables on a w/w basis.

2.3

Phenolic Compounds and Antioxidant Activity in P. aculeata

Phenolic compounds vary from 5 to 118 mg GAE g1 in P. aculeata leaves, according to the solvent used in the extraction (petroleum ether, chloroform, methanol, water, ethanol, or acetone) [13, 34, 62]. In the P. aculeata berries, phenolic compounds were ~65 mg GAE g1 [61]. Phenolic compounds are known for their high antioxidant activity. In the extract of P. aculeata leaves the antioxidant activity has ranged from 7 to 107 mg mL1 to sequestre 50% of DPPH radicals [13, 34, 58, 62], IC50 of 40 μg mL1 using ABTS method, IC50 of 39 μg mL1 using TBARS method, and 63–82% of inhibition of β-carotene oxidation [62]. Among the compounds found in the leaves are (in ascending order of amount) (mg g1): cis caftaric acid (9.5), quercetin-3-O-rutinoside (3.56), isorhamnetin-Opentoside-O-rutinoside (2.27), trans caftaric acid (2.22), quercetin-O-pentoside-Orutinoside (2.11), isorhamnetin-3-O-rutinoside (1.30), kaempferol-3-O-rutinoside

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(0.81), quercetin-O-pentoside-O-hexoside (0.74), isorhamnetin-O-pentoside-Ohexoside (0.63), and caffeic acid derivative (0.57) [13]. Caftaric acid, an ester form of caffeic acid, was the most abundant in P. aculeata leaves, and this phenolic acid has demonstrated to have excellent antioxidant and anti-inflammatory activity [63]. Rutin was the second most abundant phenolic compound reported for P. aculeata. This compound has been linked to its antibacterial activity more active against Gram positive bacteria (Enterococcus faecalis, Listeria monocytogenes, and MRSA – Methicillin-resistant Staphylococcus aureus) than against Gram-negative bacteria (Escherichia coli, Klebsiella pneumoniae, Morganella morganii, Proteus mirabilis, and Pseudomonas aeruginosa) [13].

3

Conclusions

P. aculeata has a potential as a vegetable, functional food, and source of bioactive compounds including protein, mucilage, and carotenoids. While the protein in P. aculeata is not considered complete, the abundance of lysine and tryptophan make it an excellent complimentary protein, as many plant proteins are deficient in these amino acids. Further, P. aculeata leaves serve as a rather unusual delivery method for plant proteins, providing the potential for enrichment of dishes that are not traditionally protein rich. There are several other components of P. aculeata that position the plant as a unique health-promoting vegetable. In addition to being high in protein, this vegetable is rich in mucilage that serves as a source of a unique soluble fiber. While no studies have yet investigated the effects of P. aculeata on the gut microbiome, it is probable that this fiber contains unique prebiotic activity, as a consequence of its unique chemical composition. Further, the abundance of vitamin C, minerals, and carotenoids poise P. aculeata to become an important nutrient-dense food for the future. Acknowledgments The authors acknowledge Matilde Buranelo Egea, Luis Egea Benitez, and José Carlos Becker de Oliveira e Silva for the P. aculeata pictures. The authors acknowledge the financial support of CNPq, FAPEG, CAPES, and IF Goiano.

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Bioactive Compounds of Rhubarb (Rheum Species)

12

Rajeev Bhat

Contents 1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 Botanical Descriptions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 General Uses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 Bioactive Compounds and Biological Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 Toxicity and Safety . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Abstract

Rhubarb (Rheum rhabarbarum L.; family, Polygonaceae) is a perennial herbaceous plant widely sought for their rich nutraceutical values. Several cultivated and wild species of rhubarb commands high demand in international market. Leaves are toxic, while stalk or the petioles are edible as food. Dried root/rhizome command usage in traditional medicine and is scientifically proven to impart a wide array of health benefits. Rhubarb’s therapeutic value is accredited to the presence of bioactive compounds such as anthraquinones, hydroxyanthraquinone, aloe-emodin, emodin, rhein, stilbene, rhaponticin, dietary fiber, and much more. These bioactive compounds are established for exhibiting antioxidant, anticancer, antimicrobial, antidiarrheal, antidiabetic, anti-inflammatory, diuretic, hepatoprotective activities, and much more. Even though several published works are available on rhubarb, in majority of the instances, information remains scattered, especially for the sub-cultivars, and for the actual mechanism of action imparted by the bioactive compounds. In this chapter, some of the interesting research themes published on rhubarb’s use, food and therapeutic R. Bhat (*) ERA-Chair for Food (By-) Products Valorisation Technologies (VALORTECH), Estonian University of Life Sciences, Tartu, Estonia e-mail: [email protected] © Springer Nature Switzerland AG 2021 H. N. Murthy, K. Y. Paek (eds.), Bioactive Compounds in Underutilized Vegetables and Legumes, Reference Series in Phytochemistry, https://doi.org/10.1007/978-3-030-57415-4_14

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values, composition (nutritional and bioactive compounds), and proved bioactivity are presented. Keywords

Bioactive compounds · Bioactivity · Rhubarb · Traditional use · Therapeutic values

1

Introduction

Herbal plants with rich nutraceutical values have been an integral part of human civilization. Traditionally, majority of the herbal plants are used for culinary purpose as well as in medicines. Ethno-pharmaceutical uses of popular herbal plants remain well documented in Asia, Africa, and parts of Europe. Rhubarb (Rheum sp.; family, Polygonaceae) is a perennial herbaceous plant widely sought for their rich nutraceutical values. This plant is mostly grown under shade as a garden ornamental plant (garden rhubarb) or sometimes are cultivated for their use in food and medicine. However, wild plants of rhubarb are documented to grow in hilly regions and mountains (e.g. R. australe). The English name ‘rhubarb’ is derived from Latin (rhabarbarum) and Greek words (rhabarbaron) [1https://www.etymonline.com/ word/rhubarb, assessed on July7 2020]. Many researchers have considered rhubarb plant to be a native of China (or rather native to central Asia); however, this plant finds wide distribution in Europe, Russia, parts of America, and Asia too (India, Tibet, Korea, Japan). It is also duly acknowledged that rhubarb to be a native of Siberia and was identified to grow on “Volga river” banks. Rhubarb’s extensive use in Persia and Syria, as early as during the thirteenth century is also recognized. Rhubarb plants presence in Turkey and Russia and later being planted in England during 1777 is documented [2]. However, as a garden plant, rhubarb is also grown in majority of the subtropical and temperate countries. Generally, petiole or the thick succulent stem portion are edible, while leaves are discarded owing to high levels of toxic anthrone glycosides and oxalic acids. During the early nineteenth century (between 1830–1840; in Britain and United States), appropriately cooked petiole/ stems of rhubarb were considered to be a delicacy [3]. As of today, the market demands are growing for rhubarb plant extracts owing to their rich therapeutical values (Fig. 1).

2

Botanical Descriptions

Rhubarb belongs to Polygonaceae family and has many species and/or cultivars included in the genus Rheum L. Some of the popular species include Rheum palmatum L. (Turkey rhubarb), Rheum tanguticum Maxim. Ex Balf., Rheum officinale Baillon (Chinese rhubarb), Rheum emodi wall. ex Meissn, Rheum australe L. (synonym Rheum emodi; Himalayan Rhubarb), R. rhaponticum L. (European

12

Bioactive Compounds of Rhubarb (Rheum Species)

241

Fig. 1 Rhubarb plant and bioactive compounds: (a) In natural habitat (b) Leaves and petiole (c) Roots (d) Emodin (e) Aloe emdoin-8-O-glucoside (f) Rhein glucoside (g) Sulfemodin-8 Oglucoside

rhubarb; false rhubarb), R. turkestanicum (Eshghan), Rheum x hybridum (garden rhubarb), Rheum franzenbachii, R. hotaoense, R. spiciforme, R. qinjingense, and R. glabricaule. The species Rheum rhabarbarum L. (R. undulatum) or the garden rhubarb is presumed to have been cultivated in Europe during the eighteenth century. The edible portion (petiole or the stalk) are pink to red in color with long leaves (~ 45 cm occurring in 6–7 lobes) and have a thick leathery texture. Though many cultivars are widely popular with a common name “rhubarb,” mainly three categories have been scientifically evaluated for commercial purposes, viz., Indian (R. emodi, R. webbianum), Chinese (R. officinale, R. palmatum, R. tanguticum) and Rhapontic rhubarb (Rheum rhaponticum L). The rhapontic rhubarb usually grows in wild and are popular as “false rhubarb.” Further, the best growing conditions for rhubarb are designated to be the cold wintery weather.

3

General Uses

Traditionally, edible and non-toxic rhubarb species, as well as the cultivars of some species have been used as food and as medicines. Owing to rich nutritional value, petiole or the leaf stalks (stem) are often used as a vegetable (after cooking) and for other food purposes. Rhubarb stalk color depends on the cultivar/variety and can be pink or pinkish-red or green, and is believed to influence the taste. Many people have opined that the stalk tastes sour to sweet. However, cooking along with sugar is the most preferred mode. Red and pink stalks/petiole are considered to be much sweeter than green [4, 5]. Juice preparation, pickle, salads, sauce, jam, and sweet pie are some of the popular foods prepared from rhubarb. Though the petioles are

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considered to have nutraceutical value, dried rhizome (root) also holds equal medicinal values. Traditional Chinese medicine (TCM) recommends use of rhubarb to treat fever, constipation, abdominal pain, appendicitis, kidney failure, liver cancer, and hypertension [6, 7]. Traditionally, dried rhubarb root has been used as an effective cathartic too [8]. The laxative effects of rhubarb are documented [9] and are believed to promote weight loss in obese people. Besides, rhubarb’s benefits imparted as a purgative, as an antimicrobial agent, and an effective remedy to treat wounds and cold sores of skin are evidenced in Indian traditional medicine. Besides, in Indian subcontinent, rhubarb extracts have been used traditionally for treating boils and abdominal disorders [10].

4

Bioactive Compounds and Biological Activity

The presence of bioactive compounds and the bioactivity of rhubarb are well recognized. In majority of the rhubarb (Rheum species), bioactive compounds have been isolated from petiole (the stalk) and root portions. Some of the isolated compounds of commercial interest include anthrone, anthraquinone glycoside, acylglucoside, chromenes, chromone glycosides, citreorosein, hydroxyanthraquinone, aloe-emodin, emodin, rhein, chrysophanol, pyrone, plumbagin, stilbene, resveratrol, protocatechuic acid, vanillic acid derivatives, dietary fiber, and vitamins [7, 11–15]. Besides, antioxidant-rich compounds like polyphenols, gallic acid, flavonoids, procyanidins, catechin, epicatechin, and tannin have been isolated from rhubarb species [16–20]. In addition, volatile oils and polysaccharides were also isolated from various rhubarb species [21, 22]. The presence of organic acids such as citric, oxalic, fumaric, and malic acid is considered to contribute to the taste [23]. Composition wise, rhubarb is high in vitamin K (~20–25%) and vitamin C (~5– 6%) and calcium (~12–15%; occurring as calcium oxalate), potassium (~2%), and dietary fiber (~2–3%) [24]. Investigations have demonstrated on the impact of season on chemical composition of petiole in three garden rhubarbs (Rheum sp.) under open field growing condition. Accordingly, oxalates (~1.3 mg/100 g) and vitamin C contents (46–69 mg/100 g) were observed to have significantly increased during the months of May/June. The observed bioactivity of rhubarb, such as anticancer, antioxidant, antimicrobial, antidiarrheal, antidiabetic, anti-inflammatory, diuretic, hepatoprotective, gallbladder protective, and laxative properties, is contributed to the presence of the above specified biocompounds [9, 25–30].Nevertheless, scientific study undertaken have pointed directly to the presence of anthraquinone compounds (rhein, aloe-emodin, emodin, and chrysophanol) to be mainly responsible for the protective effects [30]. Further, rhubarb is also identified to possess gut protective effects against pathogenic bacteria and help in stabilizing intestinal microenvironment [31]. Available reports have indicated rhubarb extract to impart positive influence on overcoming pathogenic bacterial diseases in aquatic fish-like blunt snout bream, common carp, and freshwater prawn [32–34]. Recently, Kuo et al. [35] have investigated antimicrobial properties of rhubarb extracts (Rheum

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officinale) on the non-specific immune parameter of orange-spotted grouper fish under in vitro and in vivo conditions. Results of this study showed rich antibacterial activity exhibited against six bacterial pathogens. Further, anthraquinone compounds were established to inhibit oxidative stress and hepatic oxidation via inhibiting lipid peroxidation, intracellular ROS as well as by enhancing intracellular antioxidant activity by scavenging oxygen-free radicals [36]. Marsupsin and maesopsin, the two bioactive compounds obtained from the rhizome of R. emodi are testified to possess high antioxidant activity [37]. Root of R. emodi extracted with methanol and water exhibited rich antioxidant activities [38]. On the other note, Kalisz et al. [5] quantified the effects of harvest time on rhubarb stalks of two Polish variety polyphenol contents. Results of this study showed “Viktoria” and “Red Malinowy” to be good source of flavonols (50–73), flavan-3ols (87–1968), anthocyanins (4–96), and gallotannin (6.32–14) (all expressed as mg/ 100 g d.w.). Liver or the hepatoprotective effects of rhubarb is well recognized. Rhubarb’s role to induce physiological pathways in overcoming liver cancer is reported by Tsai et al. [39]. Anthraquinone compounds have been designated to be mainly responsible for the observed liver protective effects [40]. Active protection of the liver was observed for viral hepatitis and nonalcoholic fatty liver disease [41, 42]. As per Lin et al. [43], reduction in the hepatic stellate cell activities tends to provide protection against liver damage (e.g., fibrosis and cirrhosis). Further, hepatoprotective activity is reported to be exhibited by extracts of R. emodi rhizome under in vitro and in vivo conditions in the liver injury induced by Carbon tetrachloride (CCl4 ) [44]. Moreover, anthraquinone compounds like aloe-emodin, emodin, and rhein are well established compounds whcih are reported to contribute to the antitumor/ anticancer activities. These compounds inhibited the proliferation of leukemia, liver, prostate, gastric, breast, lung, and ovarian cancer cells. In addition, various mechanisms of inhibition are also well studied for the bioactive compounds identified [28, 45–54]. Anticancer activity of aloe-emodin against Hep G2 and Hep 3B human cancer cell lines is reported. This compound inhibited cell proliferation as well as induced apoptosis in these two cell lines [55]. Bioactive compound rhein is asserted to overcome insulin resistance and lipid metabolic disorders as well as provide active protection against nonalcoholic steatohepatitis [41, 56]. Rhein is also described to impart positive effects in hemolysis-induced rat models [57]. Rhubarb being a good source of dietary fiber is considered to impart lipid/ cholesterol lowering effects. Clinical trials undertaken on rhubarb extracts have shown significant improvements in the endothelial functions in patients suffering by atherosclerosis, wherein serum total cholesterol and LDL were reduced [58]. Rhubarb exhibited effective anticholesterol activities mediated by inhibition of squalene epoxidase [59]. Anthraquinone derivative sennoside A and rheinosides are well-established laxatives, isolated from rhubarb [26, 60]. Rhein is designated to significantly reduce cholesterol and lipid levels (improve dyslipidemia), recover renal lesion, and inhibit renal tubular epithelial cell hypertrophy [61]. Rhubarb stalk fiber extract exhibited cholesterol-lowering effect in hypercholesterolemic men. On treating for 4 weeks, serum total cholesterol and the LDL (low-density

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lipoproteins) cholesterol were significantly reduced without altering the good cholesterol/HDL (high-density lipoproteins) [62]. Further, to establish anti-atherosclerotic effects of emdoin, molecular mechanism-based studies were undertaken which showed an overall improvement in the cholesterol efflux. Here, the expression of LXR-α, ABCA1, ABCG1, apoA-I, and PPARγ in oxidized low lipoproteins laden THP-1 macrophage was observed to increase [63]. Moreover, reduction in LDL cholesterol and triglycerides coupled with improvement in diabetic dyslipidemia in streptozotocin-induced diabetic rats is also reported [64]. Anti-inflammatory properties of rhubarb (owed to rhein, emdoin, rhapontigenin, and rhaponticin) are well-known. Anti-inflammatory effects via inhibition of expression of iNOS have been testified for rhein [65]. Zhang et al. [66] studied the antiinflammatory effects of emdoin in the lungs of animal model (rat). Moon et al. [29] reported suppression of vascular inflammatory process by aqueous extract of rhubarb. Anti-inflammatory effects via inhibition of activation of NF-κB and iNOS (blocking of MAPK and PI3K pathway signals) have been attributed to emodin [54]. Further, antiplatelet aggregation activity/anticoagulant activity is proved for stilbenes isolated from rhubarb rhizome (Rheum undulatum and R. palaestinum) and the aerial parts of R. palaestinum [67–70]. Various researchers [71–74] have reported antidiabetic effects of rhubarb. Compounds isolated from rhizome such as emdoin, rutin, chrysophanol, and its glucoside are identified to contribute for the observed antidiabetic effects. Additionally, Arvindekar et al. [75] reported antihyperglycemic activity of five major anthraquinones isolated from rhubarb. Nephroprotective role of emodin and quercetin rhubarb is also well established [5, 76–79]. Emodin significantly reduced the cisplatin toxicity in human kidney cells (HEK 293) via scavenging of free radicals, whereas quercetin offered protection to kidneys from mercury toxicity via inhibition of apoptotic cells [78, 79]. Rheum turkestanicum has been confirmed to impart protective effects against cisplatin (via reducing oxidative stress in kidney tissue) and against mercuric chloride-induced hepatorenal toxicity (in rat model) [76, 77]. Rhubarb (R. emodi) rhizome extract was shown to impart neuroprotective effects against glutamate toxicity (in IMR32 cells) [80]. Further, inhibition of oxidative stress by aloe-emodin has been illustrated to induce neuroprotective effects [81]. Inhibition of MAO-B by emdoin is considered to very effective in prevention/treatment of Parkinson’s disease [82]. The antimicrobial activity of rhubarb is documented in traditional medicine systems (TCM and in Ayurveda). The anthraquinones and rhein in rhubarb exhibited in vitro antibacterial (against a wide-spectrum of gram-negative and gram-positive bacteria) and antifungal activities [83, 84]. The ethanolic extract of Rheum emodi showed antibacterial activity against pathogenic Helicobacter pylori strains, which were originally obtained from gastric biopsy samples [85]. Rhein in rhubarb is identified to weaken pathogenicity of Porphyromonas gingivalis via interfering with the transcription of genes that code for the perceived virulence factor [86]. Further, aloe-emodin and emodin isolated from rhubarb are established to damage the cell membrane and inhibit biofilm formations in pathogenic bacteria like

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Pseudomonas aeruginosa, Stenotrophomonas maltophilia, and Streptococcus mutans [87, 88]. Further, emodin obtained from the roots of R. tanguticum is proven to be active against herpes simplex virus [89]. Anthraquinone chrysophanol 8-O-βD-glucoside obtained from ethanol extract of R. Palmatum was shown to impart significant activity against viral hepatitis B (Li et al. 2007) [90]. Rhubarb root ethanol extract (mainly rhein compound) considerably inhibited the growth of Salmonella typhimurium [91]. In a recent study by Ding et al. [92], rhubarb water extracts (at the sub-minimum inhibitory concentration) was observed to inhibit biofilm formation by Streptococcus suis. The mechanism of inhibition was also identified in this study. As per the available reports, many studies have been undertaken to explore and establish the bioactivity imparted via bioactive compounds isolated from rhubarb. However, future detailed studies are warranted to establish the actual mechanism of these activities at the microenvironment/molecular levels.

5

Toxicity and Safety

Culinary use of cooked rhubarb leaves as an alternative for spinach was promoted as early as during the First World War, but this had negative impacts leading to high mortality rate [93]. However, the death rates were later attributed to oxalic acid poisoning. As of today, many rhubarb cultivars (species) have been developed offering food and medicinal values. To date, safer limits of consuming rhubarb (stem and/or dried roots/rhizome) remains controversial. Majority of the reports available have indicated leaf portion to be more toxic and remains non-edible as a food or for direct use as medicines. Death in a child owed to oxalic acid poisoning on eating rhubarb leaves are documented [94]. Low-level exposure to oxalates from rhubarb can cause gastrointestinal disturbances in young children [95]. Rhubarb poisoning is mainly attributed to the presence of high amount of oxalates (occurring as calcium oxalates) in the leaves rather than in the edible petiole portion [96]. Oxalate crystal-mediated poisoning on consumption of rhubarb contributes toward renal failure [97]. Diffey et al. [98] have reported on the occurrence of photosensitivity dermatitis (photoallergic contact dermatitis) and vesiculobullous due to rhubarb consumption (as wine), though this is considered to be of rare occurrence. There is also a report indicating on atrophy of renal tubules, renal fibrosis, and acute renal failure after the intake of a non-steroidal antiinflammatory drug (diclofenac) which had anthraquinone derivative obtained from rhubarb (Rhizoma rhei L.) [99]. In animal model (rats), raw rhubarb was identified to induce tissue toxicity when compared with steam-cooked rhubarb. The cause of toxicity is accredited to the presence of rhein compound [100]. As it is a well-established fact that anthraquinones from plants lead to nephrotoxicity, genotoxicity, gastrointestinal problems, and liver damage [101], rhubarb or

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their extract needs to be carefully used while taking internally. Further, there are reports available on hepatotoxicity, histopathological changes, and liver injury occurring via rhubarb [102–104]. The mechanism is correlated to the effects on normal metabolism and functioning leading to acute liver damage [105]. Continued usage of rhubarb anthraquinones (main component being sennoside A) is correlated with occurrence of colonic toxicity and enhanced risks of colon cancer. Recently [106], animals (rats) which were fed with rhubarb anthraquinones have been shown to induce colon toxicity. Based on the cell culture experiments, apoptosis and autophagy stimulated by rhein the likely mechanism involved in inducing chronic toxicity were considered. However, with the ever-increasing demand of rhubarb, it is vital that additional future research activities undertaken will focus much more on the mechanism of toxicity induced under in vivo conditions, especially among humans.

6

Conclusions

In the present day, global scenario demands for natural plant-based nutraceuticals are gaining high importance and marketability. In this regard, renewed interests are being created to explore those herbs, which have proved traditionally usage in culinary and for medicinal purposes. In traditional usage, plants belonging to rhubarb species/cultivars have been proved for their various bioactivities (mainly root/rhizome and stalk) as well as their use (mainly the petiole/stalk) as food. Scientific evidences have demonstrated beyond doubt that rhubarb imparts a wide array of bioactivities under in vitro and in vivo conditions such as anticancer, antidiarrheal, antidiabetic, anti-inflammatory, diuretic, hepatoprotective, and others. With the ever-growing demand for rhubarb in international markets, appropriate authentication and identification of rhubarb cultivars need to be established to prevent commercial frauds. When rhubarb is sold as a medicine in the processed form (as powder or as capsules), utmost care needs to be taken on the safety and quality. Developing appropriate authentication methods/analytical techniques is much desirable. More research works are warranted in the future, especially relevant to toxicity of rhubarb under in vivo conditions or as human clinical trials. Further, more scientific database needs to be created to understand the basic mechanisms of the bioactivity exhibited, precisely at the molecular level. More detailed clinical trials need to be undertaken to establish the bioactivity of rhubarb prior to development of any food and/or pharmaceutical product. Owing to large market demands, overexploitation of rhubarb, especially the wild cultivars needs to be circumvented to preserve their natural habitat and genetic identity. Further, a sustainable approach needs to be adopted for cultivation of rhubarb, and this needs to be extended along the entire production and supply chain of rhubarb-based products. Finally, research activities are also required to be initiated to effectively valorize rhubarb wastes/by-products by identifying their bioactive potential, especially for tapping their potential in food, cosmetics, and pharmaceutical applications (Table 1).

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Table 1 Selected bioactivities reported in rhubarb Investigations undertaken Emodin was tested for the pathological cardiac hypertrophy via inhibition of histone deacetylase (HDAC)

Rhubarb extracts and five isolated anthraquinones were studied for insecticidal activities

Rhubarb extracts were studied for antifungal activities

Effects of rhubarb on extravascular lung water (EVLW) in patients with acute respiratory distress syndrome (ARDS) Effects of crude rhubarb extract as an alternative therapy to somatostatin in patients suffering from acute pancreatitis was analyzed via metaanalysis

In vivo and in vitro experiments were carried out to investigate whether rhubarb bioactive compounds protected the blood-brain barrier (BBB) after traumatic brain injury Dual HIV-1 inhibitors and small molecules capable of inhibiting two viral functions at a given time period were studied in rhubarb extracts (R. palmatum L. and R. officinale Baill.)

Observations The study showed cardio protective effects of emodin which was translated to angiotensin II in the mouse model. Emodin and emodin-rich rhubarb inhibited HDAC activity and cardiac myocyte hypertrophy Results revealed emodin compound to exhibit insecticidal activity (LC50 ¼ 84.30 μg/mL) against Nilaparvata lugens and Mythimna separata (LC50 ¼ 548.74 μg/mL) Results revealed plumbag into show broader range of antifungal activity against eight phytopathogenic fungi (EC50 value range: 2.84 to 10.53 μg/ mL) compared to a commercial fungicide, azoxystrobin (EC50 range: 20.40 to>100.00 μg/mL). Further, plumbag in significantly damaged the cell/mitochondrial membrane and initiated the release of cellular content along with production of reactive oxygen species in the mycelia of Rhizoctonia solani Results revealed rhubarb to decrease EVLW as well as enhance oxygenation in patients with ARDS Crude rhubarb imparted additional benefits in patients with acute pancreatitis. Compared with somatostatin, crude rhubarb + somatostatin significantly reduced certain complications (RR 0.55; 95% CI 0.41–0.73) and APACHE II scores (WMD  1.16; 95% CI -1.91 to  0.41). The combination also minimized the period of elevated serum amylase, abdominal pain, and duration of hospital stay Results showed rhein and rhubarb to be effective in protecting BBB via inhibition of signaling cascade that involved antioxidative molecular mechanism Both the extracts (rhein and rhubarb) were recorded to inhibit HIV-1 RTassociated RNase H activity. Sennosides A and B were found to be effective on RDDP and RNase H RT-

Reference Evans et al. 11]

Shang et al. [15]

Shang et al. [15]

He et al. [107] Zhou et al. [108]

Wang et al. [109]

Esposito [110]

(continued)

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Table 1 (continued) Investigations undertaken

Hepatoprotective effects of rhubarb extract in mouse model (binge drinking) and contribution of gut microbiota were correlated with metabolic effects

Renal toxicity of rhubarb and its mechanism of action were investigated in rat model. Dose administered was 16 and 2 g/kg

Effects of rhubarb on neonatal rats with bronchopulmonary dysplasia (BPD) induced by hyperoxia studied in rat model was evaluated Treatment of intestinal dysmotility with rhubarb used as a laxative in critically ill patients placed on mechanical ventilation was investigated Changes in brain protein in intracerebral hemorrhage (ICH) rats treated with rhubarb were investigated. In addition, multi-target mechanism of rhubarb in the treatment of ICH via bioinformatics analysis of differentially expressed proteins was also studied

A constipation model was used to study 2 main effects of rhubarb (Rhei Radix) rhizome, which was comparable with the characteristics of TCM syndrome

The effect of combination treatment of ulinastatin(UTI) and rhubarb on sepsis patients

Observations associated functions. From the study, sennoside A was concluded to be useful for developing HIV-1 dual RT inhibitors Results showed selected bacterial genders involved in gut barrier functions were stimulated by phytochemicals in the extract and were involved in modulation of the susceptibility to hepatic diseases and linked to acute alcohol consumption Results revealed low-dose of rhubarb not to contribute for renal toxicity. However, higher dose contributed for mild to moderate renal injury. In addition, in the kidney tissue, a downregulation of cluster in mRNA expression was also observed Protective role of BPD induced by hyperoxia via inhibiting inflammatory response and oxidative stress was observed in rats Based on the observations, rhubarb was recommended for treatment of gastric and intestinal motility in critically ill patients This study provided evidence to the clinical applications of rhubarb for ICH. This was achieved via dopaminergic synapse pathway during ICH treatment. Further, ICH treating mechanism was found to be involved in the antioxidative stress, calcium-binding protein regulation, angiogenic regulation as well as improvement in the energy metabolism Concentration of rhubarb liquid for overall efficacy was suggested to be between middle, and highest dose of Chinese pharmacopoeia (six doses used were 0.135, 0.27, 0.81, 1.35, 4.05, 8.1 g/kg) UTI alone, rhubarb alone, or combination of UTI + rhubarb significantly reduced C-reactive protein levels, WBC density, lactic acid, and APACH II scores. An elevation in the levels of CD4/CD8, with UTI + rhubarb treatment decreased procalcitonin levels. Protective effect of rhubarb

Reference

Neyrinck [111]

Deng [112]

Yin et al. [113]

Shimizu et al. [114] Liu et al. [115]

Chen et al. [116]

Meng et al. [117]

(continued)

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Table 1 (continued) Investigations undertaken

Anti-amebic effects of Chinese rhubarb (Rheum palmatum) leaves extract and isolated/synthetic anthraquinones on pathogenic amoeba were investigated

Observations

Reference

combined with ulinastatin was established in patients suffering from sepsis Experimental evidence was provided to prove rhubarb leaves extract (anthraquinone rhein) to inhibit growth of Entamoeba histolytica trophozoite under in vitro conditions

Espinosa [118]

Acknowledgments This chapter theme is based on the ongoing project-VALORTECH, which has received funding from the European Union’s Horizon 2020 research and innovation program under grant agreement No 810630.

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Part III Bioactive Compounds in Underutilized Vegetables: Seeds

Bioactive Compounds of Ajwain (Trachyspermum ammi [L.] Sprague)

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Hafiz Muhammad Asif and Hafiz Abdul Sattar Hashmi

Contents 1 2 3 4 5

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Synonyms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Botanical Description . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Phytoconstituents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pharmacological Properties of Bioactive Compounds of Ajwain Seeds . . . . . . . . . . . . . . . . . . . 5.1 Thymol . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2 Carvacrol . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3 Monoterpenes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 Toxicity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 Drug Interactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Abstract

Plants are the rich source of valuable biochemical and bioactive compounds and therefore have been widely utilized for the management of variety of disorders. Current estimate reveal that 25% of the commonly used modern medicines contain compounds isolated from plants. Ajwain or Trachyspermum ammi Linn. (T. ammi) is a medicinal herb belonging to the Apiaceae family; its leaves and seed-like fruits are used as spice. It possesses many extractable compounds such as carbohydrates, proteins, sterols, fibers, alkaloid, tannins, saponins, and flavonoids. Volatile oil extracted from the fruit of ajwain includes thymol, p-cymene, c-terpinene, and α- and β-pinene. Minerals included calcium, iron, phosphorus, and nicotinic acid. Fruits extract revealed the presence of H. M. Asif (*) · H. A. S. Hashmi Faculty of Medicine and Allied Health Sciences, University College of Conventional Medicine, The Islamia University of Bahawalpur, Bahawalpur, Pakistan e-mail: [email protected] © Springer Nature Switzerland AG 2021 H. N. Murthy, K. Y. Paek (eds.), Bioactive Compounds in Underutilized Vegetables and Legumes, Reference Series in Phytochemistry, https://doi.org/10.1007/978-3-030-57415-4_16

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monoterpenes, monoterpenoids, gluside, glucoside, and aromatic compounds. Choline and acetylcholine and anticalcifying agents were also reportedly present in ajwain seeds. Scientific reports exhibited that ajwain possesses carminative, diuretic, anticancer, hepatoprotective, stimulant, antiviral, bronchodilatory, antihypertensive, antihyperlipidemic, antiseptic, nematicidal, antiulcer, antiplatelet, antitussive, and anesthetic effects. Keywords

Bioactive compounds · Medicinal properties · Phytoconstituents · Trachyspermum ammi

1

Introduction

Ajwain plants have been widely utilized throughout the world for the management of variety of disorders due to the presence of valuable biochemical and bioactive compounds. Incorporation of plant-based natural medicinal product is being encouraged in main health care system in developed countries and its utilization is increasing day by day. Moreover, it has now become possible to isolate extremely pure compounds from medicinal plants with the recent advancement in scientific techniques. Current estimate reveal that 25% of the commonly used modern medicines contain compounds isolated from medicinal plants. Ajwain or Trachyspermum ammi Linn. (T. ammi) is an aromatic annual medicinal herb belonging to the Apiaceae family [1]. It is native to Egypt, Iran, India, and Pakistan. It is cultivated in South Asian Countries including Afghanistan, Bangladesh, India, and Pakistan [2]. Ajwain is also found in natural climate of Canada, Greenland, Alaska, Hawaii, North America, and France. Ajwain is found at arid and semiarid land areas and can be cultivated in variety of soils. Ajwain is drought tolerant and often requires fertilizers [3]. Its chief commercial source consisted of dried seed-like fruits which are used as spice and condiment [4].

2

Synonyms

Ammi copticum (L.), Carum ajowan (Benth. & Hook.f.) commonly known as Ajowan or Ajwain [4]. Details of synonyms are given in Table 1.

3

Botanical Description

Ajwain is an erect annual herb reached up to 90 cm height, with branched glabrous stem, leaves are filiform ultimate segments and much divided, 5–8 linear involucres, pinnate, petiolated; petiole is 5–10 cm long, outline is triangular ovate, 3–8 bracts, 6–20 rays, pinnate bractlets, 5–10 bractioles, and pedicel are twofold long to fruit.

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Bioactive Compounds of Ajwain (Trachyspermum ammi [L.] Sprague)

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Table 1 Synonyms and vernacular names of Trachyspermum ammi Scientific Names Ammi copticum (L.) Ammi glaucifolium (Blanco) Apium ammi (L.) Bunium copticum (L. Spreng.) Carum ajowan (Benth. & Hook.f.) Cyclospermum ammi (L.) Lag. Trachyspermum copticum (L.) Link Daucus copticus (L.) Carum copticum (L.) Benth. & Hook. f. ex C.B. Clarke Seseli foeniculifolium Poir

Vernacular Names Arabic: Ajwân, Al-Yunan, AnîsûnBarrî, Taleb El Koubs Armenian: Hounastan Burmese: Sa.mwat China: Xi Ye Cao Guo Qin, YìnDùZàngHuíXiāng (Mandarin), Yan DouhJòhngWùihHèung (Cantonese) Danish: Ajwan Dutch: Ajowan English: Ajowan caraway French: Ammi De L’inde, Ajouan, Ajowan, Ammi, Anis De L’ Inde, Sison German: Adiowan, Ajowan, Ägyptischer Kümmel, Herren kümmel, Indischer Kümmel, Königs kümmel; Hungarian: Ajova

Fruit is 2 mm long; ridges are not prominent, conical stylopodium and flower with 0.5–4 mm pedicel. Different parts of ajwain are given in Fig. 1.

4

Phytoconstituents

Phytochemical analysis revealed that ajwain consists of carbohydrates (47.54%), proteins (20.23%), and fibers (4.3%). Secondary metabolites include alkaloid, tannins, saponins, flavonoids, and sterols [5]. Volatile oils present in fruits of ajowan are thymol, p-cymene, c-terpinene, and alpha and beta-pinene [6]. Minerals included calcium, iron, phosphorus, and nicotinic acid [7–9]. Twenty-five compounds were reported from water-soluble extract fraction of fruits containing monoterpenes, glucosides, and aromatic compounds [10]. Choline and acetylcholine and anticalcifying agents were also reported in ajwain seeds [11, 12]. Kaur et al. [12] reported absence of flavonoids in seeds. Glycoproteins extracted from ajwain were reported to consist of serine, glutamic acid, proline, and aspartic acid and are the glycans made one-third portion of glycoproteins and sugar constituents constructing glycoprotein molecules galactose (45.7%), mannose (5%), arabinose (34.5%), xylose (4%), and glucose (7%), while in small quantities alanine, isoleusine, lysine, leucine, arginine, valinine, threonine, and histidine are present [13]. Essential oils components in ajwain analyzed through gas chromatographic mass spectrometry containing flavonoids and phenols consisted of chiefly thymol (63.4%), p -cymene (19%), and γterpinene (16.9%) [14, 15]. Ajwain also contains minerals and iron with essential amino acids [16, 17]. Minerals like aluminium, (Al), magnesium (Mg), manganese (Mn), calcium (Ca), and boron (B) were also reported to be present in ajwain seeds [18, 19]. Essential oils contained chiefly thymol and monoterpenes [20]. Ajwain

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Fig. 1 Different Parts of Ajwain (Trachyspermum ammi [L.])

seeds` contain variety of compounds including monoterpenes hydrocarbons, oxygenated monoterpenes, aldehydes, ketones, aromatic hydrocarbons, nitrogenous compounds, and polyphenolic compounds like ellagic acid [21, 23]. Details are given in Tables 2 and 3.

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Table 2 Chemical Constituents of Ajwain Seeds Monoterpenes Hydrocarbons Tricyclene 0.008 mg/100 g α-Pinene 2.444 mg/100 g α-Thujene 5.934 mg/100 g Camphene 0.135 mg/100 g β-Pinene 18.45 mg/100 g Sabinene 1.39 mg/100 g δ-3-Carene 0.688 mg/100 g β-Myrcene 7.9 mg/100 g α-Terpinene 6.895 mg/100 g γ-Terpinene 166.4 mg/100 g β-Phellandrene 5.197 mg/100 g (Z)-β-Ocimene 0.148 mg/100 g (E)-β-Ocimene 0.05 mg/100 g Limonene 3.105 mg/100 g ρ-Cymene 164.4 mg/100 g α-Terpinolene 0.9 mg/100 g ρ-Cymenene 0.3 mg/100 g Oxygenated Monoterpenes 2,3-Dehydro-1,8-cineole 0.066 mg/100 g 1,8-Cineole 0.83 mg/100 g 6,7-Epoxymyrcene 0.075 mg/100 g β-Thujone 0.025 mg/100 g (E)-Sabinene hydrate 1.363 mg/100 g Linalool 0.774 mg/100 g (Z)-Sabinene hydrate 4.814 mg/100 g (Z)-q-2-Menthen-1-ol 0.6 mg/100 g Fencol 0.008 mg/100 g Terpinen-4-ol 5.021 mg/100 g 4-terpinenyl acetate 0.077 mg/100 g Umbellulone 0.069 mg/100 g (E)-Pinocarveol 0.135 mg/100 g (E)-2,8-Menthadienol 0.036 mg/100 g δ-Terpineol 0.023 mg/100 g (Z)-Piperitol 0.064 mg/100 g 1,8-Menthadien-4-ol 0.109 mg/100 g α-Terpineol 1.541 mg/100 g Terpinyl acetate 0.1 mg/100 g Carvone 0.582 mg/100 g (E)-Piperitol 0.379 mg/100 g ρ-Cymen-8-ol 0.512 mg/100 g

Geraniol Piperitenone Caryophyllene oxide Perilla alcohol Cuminyl alcohol ar-Tumerone Aromatic hydrocarbons 2-AmylFuran Estragole Methyl salicylate Cuminaldehyde anethole 2-Phenethyl alcohol 6-Allyl-2-cresol ρ-Cresol Methyl-ρ-anisate Thymol Carvacrol m-Cresol Dihydroactinidiolie Dihydroactinidiolie Esters Methyl-2-methylbutanoate Aldehydes Hexanal` Heptanal Octanal Nonanal Furfural (E)-Non-2-enal Ketones 3-Hexen-2-one 2-Octanone 2-Nonanone Coumarin Nitrogenous compounds Pyridine 3-Butenyl isothiocyanate Miscellaneous Myristicin Phytol

0.122 mg/100 g 1.064 mg/100 g 0.033 mg/100 g 0.084 mg/100 g 0.277 mg/100 g 0.112 mg/100 g 0.019 mg/100 g 0.081 mg/100 g 0.114 mg/100 g 0.105 mg/100 g 0.450 mg/100 g 0.06 mg/100 g 0.414 mg/100 g 0.021 mg/100 g 0.026 mg/100 g 434.1 mg/100 g 13.53 mg/100 g 0.021 mg/100 g 0.03 mg/100 g 0.564 mg/100 g 0.178 mg/100 g 0.025 mg/100 g 0.034 mg/100 g 0.045 mg/100 g 0.049 mg/100 g 0.067 mg/100 g 0.034 mg/100 g 0.009 mg/100 g 0.009 mg/100 g 0.026 mg/100 g 0.054 mg/100 g 0.011 mg/100 g 0.041 mg/100 g 0.308 mg/100 g 0.102 mg/100 g

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Table 3 Constituents of Ajwain Seeds

5

Proteins Carbohydrate Fats Essential Oils Thiamine Riboflavin Nicotinic acid Carotenes Minerals Calcium Phosphorous (total) Iron Sodium Potassium Magnesium Zinc Manganese Nickel Aluminum Boron Copper Lithium

17.1% 21.1% 24.6% 2–4% 0.21% 0.28% 02.1% 71 μg/100 g 7.9 mg/100 g 1450 mg/100 g 909 mg/100 g 19.4 mg/100 g 3.19 mg/100 g 1519 mg/100 g 304 mg/100 g 4.8 mg/100 g 4.3 mg/100 g 0.72 mg/100 g 31.71 mg/100 g 1.32 mg/100 g 0.86 mg/100 g 0.21 mg/100 g

Pharmacological Properties of Bioactive Compounds of Ajwain Seeds

Ajwain is commonly used for the management of gastrointestinal disorders, respiratory problems, and urinary ailments. The seeds of ajwain possess carminative, diuretic, anticancer, hepatoprotective, stimulant, antiviral, bronchodilatory, antihypertensive, antihyperlipidemic, antiseptic, nematicidal, antiulcer, antiplatelet, antitussive, and anesthetic effects. The major bioactive compounds and their pharmacological properties are given hereunder.

5.1

Thymol

5.1.1 Anticancer Activity Ethanolic extract of ajwain seed showed anticancer potential against MCF-7 cell line. MTT assay was employed to assess IC50 and to investigate the cytotoxic effect of ajwain seeds. Assay result showed concentration of 25 μg/mL had highest cytotoxic and apoptotic activity. Ethanolic extract also showed cell apoptotic signs like shrinking of cell, blebbing, and fragmentation of DNA – assessed through RTPCR analysis. MCF-7 cell lines treated with ethonolic extract showed enhanced

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expression of gene p53 and expression of Bcl-2; an apoptotic gene was reduced in MCF-7 cell lines. Ajwain seeds exhibit anticancer potential against breast cancer cell lines [22]. Polyphenolic compounds like ellagic acid exhibited anticancer activity by reducing 70% growth of leukemia cell line THP-1 and lung cancer cell line A-549 at concentration of 1  10 5 M and effect was comparable with standard drugs [23]. Thymol showed anticancer activity on promyelotic leukemic HL-60 cell lines. HL60 cells were exposed to 24 h and cytotoxic effect was measured. Thymol showed dose-dependent cytotoxic effect on cell line. Thymol arrested cell cycle at substage of cell division. Cytotoxic effect was observed by DNA fragmentation–based apoptotic cell death, increased activity of reactive oxygen species, depolarization of mitochondrial membrane potential, and enhancing H2O2 production; Bcl-2 protein expression was reduced in dose-dependent manner and thymol-induced caspase 3, 8, and 9 and apoptosis were observed occurring dependently and independently [24]. Thymol exhibited antitumor action against oral squamous carcinoma cells by mitochondrial dysfunctioning independent of TRPA-1 activity [25]. In another study thymol showed anticancer effects in human glioblastoma cells by cell death induced through [Ca2+] increased by releasing Ca2+ from endoplasmic reticulum induced by protein kinase C and phospholipase C [26]. Thymol exhibited Ca2+ dispersiondependent cell death in human prostatic cancer PC-3 cells [27]. Thymol showed anticancer property in glioma cells C6 and halted phosphorylation of signal kinases regulated by extracellular signals and protein kinase C-α, and MMP9 and 6 were diminished to exhibit anticancer effect [28]. In another study thymol showed significant effect on expression of P21 and P53 genes in MCF7 cells exposed to thymol after 48 h and 72 h at IC50 concentration of 54 μg/mL and 62 μg/mL, respectively [29]. Ajwain seeds oil containing thymol (42%) revealed antitumor potential on human breast cancer cell lines SKOV3 and MDA-MB231 cells through MMT assay with IC50 for antitumor activity 208 μg/mL and 236 μg/mL, respectively [30]. Carvacol, thymol, γ-terpinene and ρ-cymene are volatile oils obtained in n-hexane extract of ajwain seeds and were reported to possess anticancer activity against hepatocellular carcinoma (HepG2) cell lines with IC50 of 9.57 μg/mL and 17.42 μg/mL concentration [31].

5.1.2 Antioxidant Activity Thymol has extensively studied for its antioxidant potential exerted by enhancing levels of various antioxidant enzymes activities through endogenous activation. Most studied enzymes are catalase enzymes, superoxide dismutase, glutathione S transfereases, and glutathione peroxidases. Thymol also showed antioxidant activity through non-enzymatic antioxidant agents like vitamin C, E, and glutathione in reduced form [32]. Thymol showed high potential of oxidative protection of lipids and high reducing power against free radical scavenging activity, DPPH, hydroxyl radical scavenging activity, and superoxide reducing potential [33]. Thymol was studied on V79 Chinese hamster lung fibroblast cells for its antioxidant potential and moderate antioxidant activity was reported. Thymol was reported to show potent antioxidant effect by altering enzymatic action and reducing oxidation of lipids under gamma rays exposed to V79 Chinese hamster cells. It also showed

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radioprotective effects and anticarcenogenic activity in gamma radiation–induced white albino rats [34]. Thymol inhibited myeloperoxidase in neutrophils and decreased production of reactive oxygen species [35]. Thymol (24.7 mg/kg) reduced aflatoxin-induced oxidative stress through supplementation in rats [36]. Thymol is potent against deranged lipid profile, glycogen catabolism, disturbance in homeostasis, and apoptotic cell death owing to its antioxidant property [32, 33].

5.1.3 Antimicrobial Activity Thymol alone and in combination with other ingredient exhibited potent antimicrobial effect in a variety of pathogens including antiparasitic, antifungal, antibactierial, and antimicrobial effects. Thymol showed potent bacteriostatic property in both gram-positive and gram-negative bacterial cultures. Minimum inhibitory concentration (MIC) reported against Salmonella typhimurium (1.0 mmol/L), Escherichia coli (1.2 mmol/L and 5 mg/mL), and Staphylococcus aureus (0.31 mg/mL) attributed to plasma membrane destabilization and destruction resulting leakage of cytosol [37, 38]. Escherichia coli growth inhibition was induced by permeabilization and depolarization of bacterial membrane with concentration of 200 mg/mL [39]. Synergism was reported for antibacterial agents with thymol against various strains of bacteria [40]. Antibacterial property was exhibited by thymol against verocytoxigenic Escherichia coli and esters derived from thymol exhibited strong effects against streptococcus species [41, 42]. Benzyl-thymol derived from thymol-exhibited antileishmanial activity against Leishmania infantum and Leishmania chagasi at concentration of 8.67 μg/mL [43]. Antifungal property of thymol was attributed to 0.12% concentration against Candida albicans through MTCC 227 biofilm inhibition [44]. Antibiotic potential was reported against gram-negative bacteria Erwinia carotovora to inhibit growth to 43.0 mm diameter with concentration of 300 ppm and 46.67 mm growth inhibition was observed with concentration of 400 ppm, and this antibacterial potential was attributed to thymol and carvacol phenolic contents of ajwain seed [45]. 5.1.4 Anti-Inflammatory Activity Macrophages-based inflammation induced by interferon gamma and lipopolysaccharides was reduced through mRNA inhibition to reduce nitric oxide induction in J774A.1 cell lines at concentration of 84 μg/mL [46]. Chemotactic peptides–induced release of an inflammatory substance elastase was inhibited by thymol at concentration of 10–20 μg/mL in human neutrophil cells and also inhibited neutrophil release of serine protease in dose-dependent manner [47]. Tymol in concentration of 0.2 μM showed IC50 for inflammatory pathways to inhibit cyclooxygenase-I (COX-I) attributed its potential being a nonsteroidal anti-inflammatory agent in similar way to NSAID [48]. Formalin-induced pain during inflammatory process was reduced to attribute anti-inflammatory potential of thymol observed in mice model [49]. 5.1.5 Immunomodulatory Activity Chauhan and his colleagues [50] described immunomodulator potential of thymol in Swiss albino rats treated with cyclosporine-A to enhance expression of both cluster

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of differentiations CD4 and CD8, γ-INF upregulation, T-helper cell cytokines, and enhanced interleukine-12 secretion [50].

5.2

Carvacrol

5.2.1 Transient Receptor Potential (TRPV1, TRPV3) Agonist Carvacrol is reported to act as agonist of transient receptor potential (TRPV1 and TRPV3) in regulation health and pain sensation. Carvacrol along with thymol and alone exhibit some important pharmacological activities. Carvacrol and thymol exhibit antimicrobial activity [39, 41]. Carvacrol agonize function of TRPV3 present in epithelial cell to sense the temperature and feeling of warmth produced. It also agonized TRPV3 receptor in colon epithelium of mouse and was supposed to provide temperature sensing, cell proliferation, and immune response. Carvacrol acts through intracellular calcium ion influx regulation and developed sensation of warmth [51]. Carvacrol agonized TRPV1 receptor and soon desensitized, thus reducing pain sensation. 5.2.2 Neuroprotective Activity Carvacrol was reported to protect neurons from demyelination and degeneration. One study demonstrated that neuroprotective effect was observed by carvacrol to prevent 6-OHDA-induced damage in dopaminergic neuron cell line (PC12) in animal model. Neuroprotective effect of carcrol was thought to be attributed to its antioxidative and free radical scavenging potential to elicit protective response in nerve tissues. A study also demonstrated to provide carvacrol-based prevention of impaired locomotor function induced by treatment of 6-OHDA in dopmernergic neurons [52]. 5.2.3 Antimicrobial Activity Carvacrol exerted antibiotic action on both gram-positive and gram-negative bacteria though bacteriostatic and bactericidal effects attributed to permeablization of bacterial cell membrane and deranged ion channels of bacterial membrane became more liquidized in presence of carvacrol [53, 57]. Antibacterial effect was reported against Vibrio cholerae, Campylobacter jejuni, Escherichia coli, Listeria monocytogenes, Salmonella enterica, Staphylococcus aureus, Staphylococcus epidermidis, Lactobacillus sakei, Pseudomonas aeruginosa, Pseudomonas putida, Streptococcus mutans, and Bacillus subtilis [42, 54–56]. Antibacterial action of carvacrol is believed to be due to its transmembrane potential to cross-bacterial membrane and reduced intracellular potassium concentration leaking out potassium ions, decreasing cytosolic pH, abolishing production of ATP by bacterial cell lead to disruption of bacterial cell structure and cell death [58]. Carvacrol was appeared to inhibit the formation of biofilms by bacteria by intervening formation of biofilms and neutralizing on surface of steel and plates of polystyerene microtiters [59, 60]. Carvacrol had showed strongest antifungal effect against resistant biofilms of Candida albicans [61]. Another study explained that antifungal property of carvacrol is

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owing to suppression of Ca2+ channels and inhibition of target of rapamycin (TOR) pathway, alteration in pH level for longer duration, interruption and upregulation of genes involved in energy production, and metabolic pathway, drug influx, and cell death [62]. Ergosterol is the main component as sterol in fungal cell membrane like cholesterol as important component in animal membrane. Ergosterole is responsible for membrane gradients and stability of fungal cells. Carvacrol in combination with thymol synergized antifungal effects on various resistant clinical strains of candidia including Candida albicans, Candida glabrata, Candida tropicalis, Candida krusei, and Candida parapsilosis by membrane gradients and decreasing ergosterol production [63].

5.2.4 Antioxidant Activity Antioxidant and free radical scavenging activity of carvacrol was reported in limited studies. Potent radical scavenging potential was reported against hepatocarcinogens compounds including N-nitrosodiethylamine (DEN) and lipid peroxidation. Carvacrol prevented radical damage induced by hepatocarcinogens and lipid peroxidation by enhancing endogenous production of antioxidant protective pathway [64]. In the presence of iron(III) ascorbate, carvacrol decreased peroxy racdical and liposomal phospholipid peroxidation induced by radiolysis pulse [65]. 5.2.5 Antiobesity Activity Carvacrol was reported to reduce body fats in animal model fed with dietary carvacrol at concentration of 100 mg/Kg and high-fat diet. Mice group fed with dietary carvacrol was found that body fats and visceral fats were reduced [66]. Antiobesity action of carvacrol was attributed to multiple pathways including alteration in thermogenesis and adipogenesis in visceral fats, reduced pro-inflammatory substances like cytokines induced through toll-like receptors (TLR) 2 and 4 pathway and inhibition of TLR pathway [66]. 5.2.6 Vasorelaxant Activity Carvacrol showed vascular epithelial relaxation in isolated aorta of rat. Vasorelaxation effect was thought due to transduction pathway involvement for calcium ion efflux of sarcoplasmic reticulum or thought to be due to calcium ion sensitivity system regulation. It was also reported that carvacol inhibits calcium ion influx from membrane at low concentration [67]. Relaxant activity was also demonstrated in muscle cell through blocking or reducing calcium ion influx to smooth muscles from extracellular calcium and also inhibited response of serotinine, histamine, acetylcholine, and nicotine [68]. 5.2.7 Anti-Inflammatory Activity Carvacrol was described as anti-inflammatory agent by inhibiting lipopolysaccharidesinduced cyclo-oxygenase 2 mRNA expression in macrophage cell lines. This action was attributed to PPARs (α & γ) activation in cell line to inhibit prostanoids and NO production through inhibition of NO synthase [69]. One study revealed that TNF-αinduced mechanical hypernoiception protected carvacrol pretreatment in animal

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model. Pretreatment did not affect PGE2 and dopamine-mediated carrageenan activated cascade. Carvacrol was proved to reduce leukocytes infiltration and NO production in murine macrophages induced by carrageenan [70].

5.2.8 Antitumor Activity Hepatic tumor induced by diethylnirotosamine carcinogen in Wistar rats was reduced with use of carvacrol supplementation at concentration of 15 mg/Kg. Antitumor effect was probably due to protection of antioxidant potential, free radical scavenging activity, and reduction of lipidperoxidation and liver cell damage [71]. Another study revealed that upto 30% Wistar rats were protected from tumor development after treatment with carcinogen 3,4-benzopyrene. Carvacrol receiving Wistar rats also showed longer life span as compared to other group not receiving carvacrol. Proposed mechanism was attributed to free radical scavenging potential and antioxidant activity of carvacrol [72].

5.3

Monoterpenes

5.3.1 Antimicrobial Activity Monoterpenes are essential component of the ajwain seed oil present in various percentages with changes in geographical position of ajwain seeds. Essential oil of ajwain seeds contain high percentage of monoterpenes and responsible for biological activities of essential oil. Ajwain essential oil is reported to be rich in paracymes 14%, gamma terpinine 7%, alpha terpinene 1.1%, thymol 74%, and carvacol 0.6% [73]. Monoterpenes and its fractions were determined for their antibacterial activity against multidrug resistance strains and antifungal activities were also determined. Monterpenes from ajwain seed oil was analyzed to contain compound like γterpinene 48%, ρ-cymene was 33% and thymol concentration was 17%. Antibacterial and antifungal activities were assessed through microdilution method. Fraction II obtained from petroleum ether and diethyl ether had showed higher antibacterial activity as compared to fraction I obtained from pretrolium ether and total essential oil of ajwain seed and standard thymol. Fraction 1 contained thymol 17%, γ-terpinene 48%, and ρ-cymene 33% as compared to fraction 3 which contained thymol 63%, γ-terpinene 10%, and ρ-cymene 6%, and n-Decane 10% showed greater activity for fraction II which was attributed to synergistic effects of compounds present in fraction as compared to standard thymol. Antibacterial activity was assessed on bacterial cultures of Escherichia coli, Salmonella enterica, Staphylococcus aureus, and Staphylococcus epidermidis and antifungal property was evaluated on nine American fungal cultures including Aspergillus flavus, Aspergillus fumigates, Aspergillus oryzae, Aspergillus clavatus, Candida albicans, Candida glabrata, Candida tropicalis, Candida krusei, Candida parapsilosis, and Candida dubliniensis [74]. Antifungal action of essential oil with main ingredients of cymene, DL-limonene, 1,8-cineole, and γ-terpinene reported against Aspergillus flavus showed MIC 0.8 μL/mL [75]. Another study showed strong antibacterial activity against waterborne bacteria including Escherichia coli, Vibrio cholera,

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Salmonella typhi, and Shigella dysenteriae. MIC observed was 0.087 mg/mL, 0.128 mg/mL, 0.107 mg/mL, 0.109 mg/mL, and 0.162 mg/mL respectively. Essential oil was analyzed for constituents containing thymol 80.70%, ρ-cymene 11.40%, and γ-pinene 7.90% [76].

5.3.2 Antioxidant Activity Different studies showed antioxidant potential of essential oil containing monoterpenes and thymol. Antioxidant potential was evaluated by 2,2-diphenyl-1picryhyrazyl inhibition assay, β-carotene/linoleic acid assay inhibit with 50% concentration of ingredient showed IC50 of 34 μg/mL. IC50 showed inhibition of 82% in resemblance to antioxidant effect of butylated hydroxytolune [14, 77]. Essential oil from ajwain seeds was reported to exhibit antioxidant activity in ABTS free radical assay, DPPH free radical scavenging activity was not upto the mark as compared to ABTS. Essential oil showed a high reducing potential in FRAT reduction assay [78]. 5.3.3 Anticancer Activity Essential oil having main ingredients as thymol 67%, ρ-cymene 17%, γ-terpinene 11%, and carvacrol 0.9% was observed for their anticancer potential in natural combination with all ingredients of essential oil obtained from ajwain seed. Nineteen monoterpenes compounds were analyzed in the oil. Anticancer activity was performed on three cell lines employing MTT assay. All three cell lines were human tumor cell lines for malignant melanoma A375, MDA-MB231 cell line of breast adenocarcinoma, and HCT116 colon carcinoma cell clines. All cell lines were treated with essential oil for 72 h and anticancer potential was assessed. Essential oil showed antiproliferative and inhibitory effect on all cell lines with concentration 0.78–200 μg/mL in a dose-dependent manner [78]. Oil ingredient was able to induce T-cell/lymphocytes proliferation when cell cultures were treated with mitogen production obtained in PBMC method. Mitigation was achieved through PHA and PWM method. All concentration was active against proliferation. Cell mitigated with PHA showed slight high T-cell lymphocytes proliferation [78].

6

Toxicity

Ajwain seed extract ingredients showed cytotoxic effect in animal model. Median lethal dose for rats given through oral route contained carvacrol 810 mg/Kg bodyweight [79], while intravenous administered median lethal dose of carvacrol was suggested between 73 and 80 mg/Kg bodyweight [80]. Mixture of thymol and carvacrol was reported to exhibit cytotoxic effect at 24 h and 48 h in intestinal cell lines Caco-2. Cellular toxicity was exhibited by alteration in cell organelles and structures along with changes in cytoplasm and development of vacuolization in cytoplasm [81]. One study also reported complex I inhibition by carvacrol at negligibly low concentration [82]. Carvacrol was also reported for its cytotoxic effects on various cancer cell lines AGS and WS-1 cell line in combination with cytotoxic effect in normal cells low in intensity as compared to cancer cell lines.

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Carvacrol-induced cellular responses were observed in in vivo and in vitro experiment showed DNA damage, cytotoxic and apoptotic effect measured in cancer cells, while intensity was low as compared to cancer cells [83].

7

Drug Interactions

Thymol reduced extracellular calcium level upto 80% and various drugs interact with pharmacological action of thymol and carvacrol. Drugs including calcium channel blockers like amlodipine, protein kinases inhibitors, calcium ion regulators like nefidipine, antifungal drugs like econazole, and calcium pump inhibitors like thapsigargin interact with functioning of ajwain seed extract and inhibited extracellular calcium concentration and antagonized actions of ajwain ingredients actions [84].

8

Conclusion

Ethnobotanical and traditional uses of natural compounds, especially of plant origin received much interest during the last couple of decades because they are scientifically tested for their effectiveness and generally believed to be harmless for human use. Eventually, the pharmaceutical sector is now paying attention towards design and development of new indigenous plant-based drugs through screening of bioactive compounds. Ajwain revealed the fact that it is a popular remedy among the various ethnic groups and traditional practitioners for treatment of different types of ailments. Volatile oil extracted from fruit of ajwain includes thymol, p-cymene, cterpinene, and a- and b-pinene. Minerals like calcium, iron, and phosphorus were also reported. Scientific reports exhibited that ajwain possesses carminative, diuretic, anticancer, hepatoprotective, stimulant, antiviral, bronchodilatory, antihypertensive, antihyperlipidemic, antiseptic, nematicidal, antiulcer, antitussive, antiplatelet, and anesthetic effects. Keeping in view the presence of above-mentioned compounds in ajwain, further studies are recommended to evaluate more pharmacological activities and therapeutic potential of ajwain.

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27. Yeh JH, Chou CT, Chen IS, Lu T, Lin KL, Yu CC, Liang WZ, Chang HT, Kuo CC, Ho CM, Chang WT (2017) Effect of thymol on Ca 2+ homeostasis and viability in PC3 human prostate cancer cells. Chin J Physiol 60:32–40 28. Lee KP, Kim JE, Park WH, Hong H (2016) Regulation of C6 glioma cell migration by thymol. Oncol Lett 11:2619–2624 29. Seresht HR, Albadry BJ, Al-mosawi AK, Gholami O, Cheshomi H (2019) The cytotoxic effects of thymol as the major component of Trachyspermum ammi on breast cancer (MCF-7) cells. Pharm Chem J 53:101–107 30. Mohammadpour G, Tahmasbpour R, Rahmani A, Esfahani AA (2018) Chemical compounds, in vitro antitumor and antibacterial activities of Trachyspermum copticum L. essential oil. Iranian J Pharmacol Ther 16:1–6 31. Abdel-Hameed ES, Bazaid SA, Al Zahrani O, El-Halmouch Y, El-Sayed MM, El-Wakil E (2014) Chemical composition of volatile components, antimicrobial and anticancer activity of n-hexane extract and essential oil from Trachyspermum ammi L. seeds. Orient J Chem 30:1653– 1662 32. NagoorMeeran MF, StanelyMainzen Prince P (2012) Protective effects of thymol on altered plasma lipid peroxidation and nonenzymic antioxidants in isoproterenol-induced myocardial infarcted rats. J Biochem Mol Toxicol 26:368–373 33. Meeran MF, Jagadeesh GS, Selvaraj P (2015) Thymol attenuates altered lipid metabolism in βadrenergic agonist induced myocardial infarcted rats by inhibiting tachycardia, altered electrocardiogram, apoptosis and cardiac hypertrophy. J Funct Foods 14:51–62 34. Archana PR, NageshwarRao B, SatishRao BS (2011) Modulation of gamma ray–induced genotoxic effect by thymol, a monoterpene phenol derivative of cymene. Integr Cancer Ther 10:374–383 35. Pérez-Rosés R, Risco E, Vila R, Peñalver P, Cañigueral S (2016) Biological and nonbiological antioxidant activity of some essential oils. J Agric Food Chem 64:4716–4724 36. El-Nekeety AA, Mohamed SR, Hathout AS, Hassan NS, Aly SE, Abdel-Wahhab MA (2011) Antioxidant properties of Thymus vulgaris oil against aflatoxin-induce oxidative stress in male rats. Toxicon 57:984–991 37. Olasupo NA, Fitzgerald DJ, Gasson MJ, Narbad A (2003) Activity of natural antimicrobial compounds against Escherichia coli and Salmonella enterica serovar Typhimurium. Lett Appl Microbiol 37:448–451 38. Trombetta D, Castelli F, Sarpietro MG, Venuti V, Cristani M, Daniele C, Saija A, Mazzanti G, Bisignano G (2005) Mechanisms of antibacterial action of three monoterpenes. Antimicrob Agents Chemother 49:2474–2478 39. Xu J, Zhou F, Ji BP, Pei RS, Xu N (2008) Carvacrol and thymol had desired antimicrobial effect on E. coli. The antibacterial effects were attributed to their ability to permeabilize and depolarize the cytoplasmatic membrane. Lett Appl Microbiol 47:174–179 40. Palaniappan K, Holley RA (2010) Use of natural antimicrobials to increase antibiotic susceptibility of drug resistant bacteria. Int J Food Microbiol 140:164–168 41. Rivas L, McDonnell MJ, Burgess CM, O’Brien M, Navarro-Villa A, Fanning S, Duffy G (2010) Inhibition of verocytotoxigenic Escherichia coli in model broth and rumen systems by carvacrol and thymol. Int J Food Microbiol 139:70–78 42. Mathela CS, Singh KK, Gupta VK (2010) Synthesis and in vitro antibacterial activity of thymol and carvacrol derivatives. Acta Pol Pharm 67:375–380 43. de Morais SM, Vila-Nova NS, Bevilaqua CM, Rondon FC, Lobo CH, Moura AD, Sales AD, Rodrigues AP, de Figuereido JR, Campello CC, Wilson ME (2014) Thymol and eugenol derivatives as potential antileishmanial agents. Bioorg Med Chem 22:6250–6255 44. Pemmaraju SC, Pruthi PA, Prasad R, Pruthi V (2013) Candida albicans biofilm inhibition by synergistic action of terpenes and fluconazole. Indian J Exp Biol 51:1032–1037 45. Jafarpour M, Golparvar AR, Lotfi A (2013) Antibacterial activity of essential oils from Thymus vulgaris, Trachyspermum ammi and Mentha aquatica against Erwinia carotovora in vitro. J Herb Drugs 4:115–118

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Part IV Bioactive Compounds in Underutilized Vegetables: Tuberous Vegetables

Bioactive Compounds of Allium Species

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Contents 1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 Botanical Distribution and Bioactive Compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 Bioactivity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1 Antioxidant Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 Anticancer Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3 Antimicrobial Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4 Antihyperlipidemic/Anti-hypercholesterolemic Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5 Other Bioactivities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 Toxicity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Abstract

Evaluation of different plant species of Allium has resulted in identification of several bioactive constituents/phytochemicals. Some of the bioactive phytochemical constituents include organosulfur compounds, thiosulfinates, polysulfanes, polyphenols, tannins, flavonoids, alkaloids, saponins, fructans, fructo-oligosaccharides, essential oils, amino acids, vitamins, pigments, and much more. Traditionally, majority of the plants belonging to Allium sp. have been proved to be effective in treating flu, cold, cough, asthma, headache, stomachache, arthritis, and other common ailments. Besides, bioactive compounds identified in some of the commonly used Allium sp., they are scientifically proven to contribute towards a wide range of bioactivities such as antioxidant, antimicrobial, anti-inflammatory, antidiabetic, anticancer, antiR. Bhat (*) ERA-Chair for Food (By-) Products Valorisation Technologies (VALORTECH), Estonian University of Life Sciences, Tartu, Estonia e-mail: [email protected]; [email protected] © Springer Nature Switzerland AG 2021 H. N. Murthy, K. Y. Paek (eds.), Bioactive Compounds in Underutilized Vegetables and Legumes, Reference Series in Phytochemistry, https://doi.org/10.1007/978-3-030-57415-4_17

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hypercholesterolemic activities and much more. In the present chapter, attempts have been made to identify and report on some of the popular, widely consumed, and scientifically proven bioactivities of plants belonging to Allium species. Keywords

Allium species · Bioactivity · Bioactive compounds · Bulbs · Phytochemicals · Toxicity

1

Introduction

Nutraceutically valued plant-based food offers wide prospective to provide health benefits with a natural approach. Effective utilization of traditionally recognized agri-food produce (e.g. herbs and spices) not only supports reduction in the costs incurred for health care but can also be a potential source of revenue for farming communities. Among a wide array of herbs traditionally used for culinary and therapeutic uses, plants belonging to Allium sp. command high value. Allium species comprises of plants which serve the purpose either as an ornamental, as a culinary ingredient, or as a traditional therapeutic agent, routinely used in traditional herbal drug preparations. Nevertheless, since time immemorial, edible plant parts of Allium sp. have been used in cooking as a flavoring agent/spice or are consumed raw (as salads) or extracted with solvents (mainly water) for medicinal purposes. Being natural, majority of the edible plants of Allium sp. are safe for consumption without any undue toxicity exhibited in humans. Plants belonging to Allium sp. are commonly referred to as “bulb crops” or as “bulb vegetables.” In traditional medicines, herbal formulations prepared from majority of the Allium sp. have been used to treat or manage common flu, cold, cough, asthma, headache, stomachache, and arthritis. Besides being abundant in nutrition, this group of plants is also high in bioactive compounds and exhibits rich bioactivity (e.g. antioxidant, antimicrobial, anticancer, anti-cholesterolemic activity). Some of the common and popular plants belonging to Allium sp. include onion, shallots, Welsh onion, Chinese onion, garlic (wild garlic, white garlic, and rosy garlic), leeks, wild leeks, chives, and others. In the present chapter, attempt has been made to identify and report on some of the popular, widely consumed, and scientifically proven bioactivities of plants belonging to Allium sp.

2

Botanical Distribution and Bioactive Compounds

The distribution of plants of Allium sp. is covered under family Amaryllidaceae and sub-family Allioideae/Alliaceae. Previously, this group of plants was placed under family Liliaceae. The plants belonging to this species extensively grow in a varied range of temperatures (temperate, tropical, and subtropical conditions). It is broadly considered that there might be nearly 800–900 species of plants belonging to Allium. However, onion (Allium cepa), Welsh onion (Allium fistulosum), Chinese onion

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(Allium chinense), tree onion or the Egyptian walking onion (A. cepa var. viviparum/ proliferum), garlic (Allium sativum var. ophioscorodon and var. sativum), leeks (Allium tuberosum), chives (Allium schoenoprasum), and shallots (Allium hirtifolium) remain as the most widely consumed species. In Fig. 1, a pictorial representation of some of the popular plants of Allium sp. is shown. Besides, there are wildly growing species without much commercial values such as Allium altaicum, Allium roylei, Allium galanthum, and Allium pskemense. Some of the other species are reported to have presence of high amounts of bioactive compounds exhibiting good bioactivity, and these include Allium ascalonicum, Allium autumnale, Allium ampeloprasum (var. porrum), Allium fistulosum, Allium hirtifolium (Allium stipitatum), Allium jesdianum, A. melanantherum, A. flavum, Allium macrostemon, Allium tripedale, Allium schoenoprasum, and Allium thunbergii. Majority of the plants belonging to Allium sp. are perennial. Further, depending on the species, the edible portion remains either single or clustered bulbs, flowers, leaves, stem, and/or stalks. The size of the bulbs and leaves varies depending on the plant types. The plants generally have a taproot system and grow up to a height of 120–150 cm [1]. In some species, the height recorded is as low as 5–10 cm. Further, the flowers are produced on the upper part of leafless stalk and represent the form of an umbel. In general, majority of the Allium sp. plants contain bioactive phytochemicals such as sulfur (organosulfur compounds), alliin, alliinase, allicin along with polyphenols, quercetin, tannins, flavonoids, gallic acid, ferulic acids, cinnamic acid, N-caffeoyltyramine, carotenoids, anthocyanins, polysulfanes, alkaloids, saponins, vitamins (B1, B2, C, and E), selenium, organoselenium, fructo-oligosaccharides, and chlorophyll [2–6].

Fig. 1 Pictorial representation of some popular plants of Allium sp. (a) Shallot onion; (b) green onion; (c) tree onion; (d) altai onion; (e) black garlic; (f) wild leek

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Besides, soluble dietary fibers such as fructans and fructosyl are present in ample amounts too. Nevertheless, most of the edible bulbs have a unique and a characteristic intense sulfurous aroma (odor). Henceforth, relationship of sulfur compounds in Allium sp. imparting unique flavor quality has been well established [7–9]. On the other hand, there are black onions and black garlic bulbs that possess a distinctive odor and are less pungent compared to fresh ones. This is owed to decreased levels of organosulfur compounds and nitrogen oxides during processing stages [9–11]. Recently, hairy garlic (Allium subhirsutum) which is widely consumed as a spice in the Mediterranean regions was identified to contain rich amounts of flavonoids, sulfur compounds, and phenylpropanoid derivatives and is recommended to be a good alternative for garlic (A. sativum) [12]. Bulbs of wild onions (genus Allium sect. Codonoprasum) have a mild odor and distinctive flavor and contains dimethyl disulfide and methiin (S-methyl-L-cysteine sulfoxide) as the dominant volatiles [13, 14]. In shallots, volatile compounds involved in imparting flavor were identified to be sulfides, dimethyl trisulfide, furfural, 2,5-dimethylpyrazine, and thiophenes [15]. In black garlic, presence of amino acids like leucine, isoleucine, and phenylalanine is reported [10]. Same authors observed substantial increase of amino acids during production of black garlic. Additionally, significant increase in fructose during black garlic production is also stated [11]. Further, wild leeks (Allium ampeloprasum) are reported to contain copious amounts of flavor precursor compounds as methiin and propiin [13]. The precursors of distinctive flavor and health-promoting potential of Allium sp. vegetables are linked with S-alk(en)ylcysteine sulfoxides [16, 17]. It was observed that bioactive sulfur compounds are released after their enzymatic breakdown in combination with other polyphenolic compounds imparting various bioactivities [18, 19]. In fresh garlic, S-allyl-L-cysteine sulfoxide (or the alliin) alone forms majority of the cysteine sulfoxides. Chive flowers have been reported to contain sulfur compounds like 3,5-dihydroxy-6-methyl-2,3-dihydro-4H-pyran-4-one, proved to prevent colon cancer in humans [20–22]. Of late, new Allium cultivars are being developed with distinctive and sweet aroma devoid of sulfur compounds and which holds a pleasant mouth feel for consumers [23]. Fatty acid composition of edible parts of onion, garlic, and leek is reported to have linoleic (~45–50%), palmitic (~20–23%), oleic (~4–13%), and linolenic (~3–7%) acids as the major fatty acids [24]. Essential oil obtained from onion seeds (Allium roseum) was identified to contain nearly 48 compounds [25]. Further seed oil of onion and chives is reported to contain ample amount of fats which ranged between 25–30% and 16%, respectively [26], with linoleic acid (~44%) being the major fatty acid detected. Fatty acid analysis of chive flowers was reported to contain palmitic acid (5–17%), linoleic acid (8–14%), stearic acid (3–31%), γ-sitosterol (3– 6%), campesterol (0.3–0.6%), and fucosterol (0.3–0.5%) [21]. Further, Nehdi et al. [27] investigated wild leeks seed oil (Allium ampeloprasum) and found them to have approximately 18% of oil with major components being linoleic acid (~72%), oleic acid (~14%), and palmitic acids (~7%). Moreover, γ- and δ-tocotrienols (~80% and 52% of oil, respectively) were detected to be the main tocols in the oil. Additionally, ramp bulbs (Allium tricoccum) have been described to contain ample amounts of

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sulfur compounds, mainly thiosulfinate allicin in ramp bulbs [28]. Leaves of wild leeks have been reported as a good source of vitamin C, while in stem portion, the major flavonol glycosides identified were quercetin and kaempferol sophoroside glucuronide conjugates [29, 30]. In Fig. 2, structure of some of the bioactive compounds isolated from Allium species is provided.

3

Bioactivity

In general, bioactivities exhibited by plants belonging to Allium sp. include antioxidant, anti-flu, antibacterial, antiviral, anti-asthmatic, antidiabetic, antitumor, antimutagenic, antiprotozoal, antiproliferative, anti-inflammatory, and chemo-preventative activities [31–45]. In the preceding text, some of the vital biological activities exhibited by various plants belonging to Allium sp. are being highlighted.

3.1

Antioxidant Activity

Studies available have indicated rich antioxidant potential of plants belonging to Allium species. A range of polyphenolic compounds and phenolic acids have been isolated, which are established antioxidant compounds. Some of the main polyphenolic acids identified include gallic, ferulic, p-coumaric, protocatechuic, and sinapic acids [46]. Flavonoids identified in vegetables of Allium sp. were quercetin aglycone and quercetin di-glucosides [47, 48]. In onion and garlic, bioactive flavonoids, quercetin, cyanidin, and selenium have been correlated with the antioxidant activities exhibited [19, 49–52]. It is opined that onion by-products possess rich antioxidant properties, which can find potential applications as a functional food components [53]. Furthermore, Škerget et al. [54] have reported free radical scavenging activity of skin wastes and edible pulp part of red onions. Varied skin-colored onions (red, white, and yellow from Pusa, India) have been identified for high antioxidant activities [52, 55]. Interesting reports are available wherein each of the layers in the onion bulb (red and yellow colored) had varied flavonoid contents, which contributed for the observed antioxidant activity [56]. Onion essential oil has also been shown to have antioxidant potential. Effectiveness of onion oil to minimize oxidative damage produced in rats (via nicotine) was comparable with vitamin E [57]. Onion oil extracted with supercritical CO2 has been demonstrated to show antioxidant properties [58]. Accordingly, results of this study for ABTS+ and DPPH metal chelating assay indicated IC50 to be 0.67, 0.63, and 0.51 mg/ml, respectively. Rich antioxidant potential of leaves, stalk, and bulb of chives is described by Stajner et al. [59]. Moreover, Persian shallot (A. hirtifolium) is presented to exhibit free radicals scavenging/antioxidant activity, and this was owed to the presence of high polyphenolic contents [60]. Further, spring onion (A. ascalonicum L.) is also shown to exhibit rich antioxidant activities [61, 62]. On studying the antioxidant effects of garlic and aged garlic extracts, high polyphenolic content was recorded when compared to raw and heated garlic extracts [63]. With regard to chives, antioxidant

Fig. 2 Structure of some bioactive compounds isolated from Allium species: (a) alliin; (b) allicin; (c) cycloalliniin; (d) quercetin; (e) diallyl disulfide; (f) γglutamyl-S-allyl-L-cysteine; (g) E-ajoene; (h) methiin

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activity (aerial parts and bulb) has been correlated to the presence of kaempferol, quercetin, dl-α-tocopherol, sulfur, and polyphenolic compounds [64–66].

3.2

Anticancer Activity

The majority of studies undertaken on antitumor/anticancer activities in Allium sp. have focused mainly on onion and garlic. Regular consumption of onion and garlic is reported to minimize occurrence of esophageal, breast, colon, and prostate cancers. Organosulfur compounds and allicin have been linked with providing protective effects against many cancer cell lines [67–72]. Regular consumption of onion is related to significant reduction in the occurrence and risks associated with endometrial, cervical, stomach, and colorectal cancers [42, 73–76]. The mechanism of action is related to the presence of flavonoids, quercetin, polyphenols, and organosulfur compounds that are capable of constraining tumor cells and inhibition of enzymes such as protein tyrosine kinases and fatty acid synthase along with alteration of phase II detoxifying enzymes [77–79]. Further, consumption of garlic on daily basis is reported to show reduction in gastric cancer [80], and this type of anticancer effect has been correlated to inhibition of nitrosamines [81]. Allicin’s role in interference with tumor angiogenesis and anti-apoptotic proteins is well established [82, 83]. Induction of apoptosis by activation of proapoptotic “Bax molecule” in ovarian cancer cell lines is documented for allicin [84]. Restriction of leukemia cell lines via bioactive compound ajoenea derivative of allicin is described [85, 86]. Nevertheless, crushing of garlic cloves prior to cooking is reported to retain their anticancer properties [87]. Cytotoxic potential against various cancer cell lines by saponins derived from A. porrum is documented [88, 89]. Chinese chive (A. tuberosum) has been confirmed to impart anti-inflammatory and anticancer effects [90]. In addition, chive flowers have been proved to exhibit anti-proliferative and antitumor activities in HaCaT cancer cells. Antitumor potential against Ehrlich carcinoma in mice by aqueous extracts of chive (Allium schoenoprasum) leaves is reported by Shirshova et al. [91]. Anticancer activity against human colon cancer cell lines by chives extract is also reported [92]. Further, Ismail et al. [93] have confirmed Persian shallot (A. hirtifolium) to exhibit effective anticancerous activity. Azadi et al. [94] recorded inhibition of HeLa and MCF7 cancer cells in solvent extracts (chloroform and water) of Persian shallot in mouse used as animal model. In another study, methanolic extract of A. jesdianum was reported to exhibit cytotoxic effect and inhibition of HeLa and K562 cell lines [95]. The mechanism is correlated to the presence of polyphenolic compounds and chive-derived glycolipids [96]. Chive flowers containing sulfur compound such as 3,5-dihydroxy-6-methyl-2,3-dihydro-4H-pyran-4-one has been proved to prevent colon cancer in human cell lines [20–22]. Dry and fresh spring onion (A. ascalonicum/shallot) has been reported to be a potential resourceful material effective against HepG2 cancer cell line [37]. Efficiency of shallot plants as a potential candidate for developing novel anticancer drugs is specified by Abdelrahman et al. [97]. Welsh onion (A. fistulosum) is

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quantified to exert DNA protective effects against genotoxic materials and showed anticancer activities [98]. Aerial parts of methanolic extract of wild edible onion A. flavum exhibited anti-proliferative activities against human colorectal carcinoma, breast adenocarcinoma, and cervix epithelioid carcinoma [99–101]. These plants contain high amounts of aglycones, polyphenols, quercetin, and flavonoids capable of imparting high antioxidant and cytotoxic activities. Besides, methanolic extract of A. cornutum was proved to exhibit genotoxic effects and inhibit cancer cells [32]. Besides, methanolic extract of Egyptian Allium kurrat is shown to impart cytotoxic and antitumor effects against the HepG2 and Caco-2 cancer cell lines [102]. Further, Isbilen et al. [34] have reported anticancer potential of A. autumnale extracts against breast cell lines (MCF-7 and MDA-MB-231).

3.3

Antimicrobial Activity

Antimicrobial effects imparted by Allium species have been well documented [40, 103–105]. The presence of various bioactive compounds is recognized to contribute against human bacterial and viral pathogens. Thiosulfinates present in onion, garlic, ramp, and other Allium species are documented to impart antimicrobial activities [106–109]. Thiosulfinate analogues of allicin are also reported to impart rich antimicrobial activities against Gram-positive and Gram-negative bacteria, fungi, and virus [110]. Effective use of shallots as a potential antimicrobial agent to treat dermatomycosis, as an antifungal agent (to be used as a possible alternative for chemical-based antifungal agents), and as a potential anti-candida agent to treat chronic candidiasis is reported by many researchers [111–113]. Influenza A virus inhibitory activities of fructan obtained from Welsh onion (A. fistulosum) has been established in animal models [114]. Antiviral activities of shallots, garlic, onions, leeks, and green onions extract against adenovirus were investigated by Chen et al. [115]. Results of this study revealed shallots to exhibit highest antiviral activity for both ADV41 and ADV3, followed by garlic and onions. Freshly prepared garlic extract is reported to have high anti-candida activity compared to extracts prepared using dried garlic powder. Water extract of A. tripedale, a wild onion species was highly effective against Candida sp. infection [116]. Methanolic and water extracts of Persian shallot (A. hirtifolium) is reported to exhibit antimicrobial properties [40, 103]. Further, chive essential oil is reported to possess antimicrobial activities. Sulfur compounds (diallyl disulfide, diallyl trisulfide, and diallyl tetrasulfide) in chive oil offers bactericidal activity [117]. Going ahead, inhibitory activity of chives essential oil against food-borne pathogenic bacteria such as Bacillus cereus, Campylobacter jejuni, Staphylococcus aureus, etc. is reported by Mnayer et al. [66]. Significant reduction in pathogenic E. coli bacteria with a corresponding increase in Lactobacillus and Streptococcus sp. was established in onion-fed broilers [118, 119]. Further, antimicrobial effects of A. schoenoprasum extracts (water and alcoholic) on bacterial pathogens have been described [120]. Phytochemicals in A. sativum extract were used for CuO nanoparticle synthesis, which showed antimicrobial activity, and this was considered

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effective against bacteria as well as fungi [121]. Recently, by employing in silico method, 11 compounds from onion oil (Allium cepa) were evaluated for their binding efficiency with selected proteins of dengue virus. Results showed hexadecanoic acid (and compound K) to be having high binding affinity for the selected proteins and is recommended to be used as an efficient target drug to treat dengue virus [122]. Recently, use of Allium sativum as a preventive measure against COVID-19 infection to enhance the immune system as well as to suppress proinflammatory cytokine production is also being reported [123].

3.4

Antihyperlipidemic/Anti-hypercholesterolemic Activity

Various plants of Allium sp. are well established for their active role played in reducing cholesterol levels under in vitro and in vivo conditions. Investigating on effect of garlic in chicken hepatocytes, Qureshi et al. [124] have reported inhibition of fatty acid biosynthesis in liver enzymes as well as cholesterol. Antihyperlipidemic effects of onion peels are reported in animal models [125]. Further, in STZ-induced diabetic rats, Baragob et al. [126] have reported antihyperlipidemic effects of ethanolic extracts of onion. Results of this study revealed significant reductions in the serum total cholesterol, triglycerides, and the LDL or the bad cholesterol within insulin-treated groups. Inhibition of cholesterol synthesis by constraining 3-hydroxy-3-methyl-glutaryl-coenzyme-A reductase via organosulfur compounds is reported [127]. Cardioprotective role via reduction in blood pressure, vasodilator, smooth muscle relaxant, and hypotensive potential of allicin and ajoene, obtained from garlic, is confirmed [128]. Cholesterol-lowering effects are also attributed to steroidal saponins (e.g., in garlic), wherein inhibition of cholesterol absorption and metabolism is regulated [129]. Improved vasodilatation, reduction in bad cholesterol, and suppression of cholesterol biosynthesis are reported for many of the Allium sp. [130, 131]. Reports on black garlic have indicated reduction in blood lipid parameters [132]. Significant effects imparted by garlic in management of dyslipidemia, hypertension, and protection against cardiovascular risk factors are also well established [133–135].

3.5

Other Bioactivities

Anti-inflammatory activities of A. jesdianum (an onion species mainly grown in Iran) with unconfirmed mechanism are reported [136]. Anti-inflammatory properties 2-[(methylthio)methyldithio]pyridine N-oxide compound isolated from Persian shallot have been confirmed by Krejcova et al. [137]. Anti-inflammatory properties of extract obtained from chive leaves against turpentine oil-induced inflammation in rat model are documented by Parvu et al. [138]. Antihypertensive activity of chives bulb extract was confirmed via in vivo studies undertaken in Wistar rats [139]. Anti-obesity effects/ability to manage adipogenesis by onion peel extract possessing high quercetin contents is validated [140–142]. Aqueous extract of Allium hookeri root was investigated for their effectiveness on adipogenesis in 3T3-L1 cells and

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high-fat diet-induced obese mice models [143]. Results of this study revealed extracts to augment metabolic alteration by altering the gene expression levels are involved in adipogenesis, lipogenesis, and lipolysis. Antiplatelet activity of Allium sp. is reported (mainly for garlic) and is related with pyruvates produced by alliinase on crushing [144–146]. Human platelet antiaggregation activity is reported in leeks, and the activity was attributed to isolated steroidal saponin and flavonoids [147]. In case of garlic cloves, to retain antiplatelet activity and minimize decline in thiosulfinate contents, it is advised to crush the cloves prior to use [144]. Combination of garlic and onion showed significant decrease in liver steatosis, serum liver enzymes, and lipid peroxidation. Antithrombotic potential is reported for ajoene obtained from onions [148]. Anthelmintic activity of chives and onion powder revealed decrease in worm counts in mice intestine [149]. Protective role of extract prepared from shallot is reported to be effective against CsA-induced nephrotoxicity in rat models [150]. Angiogenesis disease disorder preventive role of shallots is well documented [151]. Regarding leeks, immune-stimulating role of two isolated pectic polysaccharides (galacturonic and glucuronic acid) is documented [152]. Regular intake of leek (Allium ampeloprasum) was found to improve sexual impotency [153, 154]. Besides, administration of leeks over a month is showed to be useful in the management of diabetes mellitus too [155]. Effects of Allium mongolicum Regel on constipation were studied in mice model by Chen et al. [156]. Results of this study revealed oral administration of 50% ethanolic extract to significantly enhance the luminal side water content as well as regulate intestinal movement rhythm to normalize the stool. This effect was contributed to the presence of three major flavonoids present in A. mongolicum. Antiallergic activity of shallot (Allium ascalonicum) extract was investigated by Arpornchayanon et al. [157]. Improvement of posttreatment visual analog scores of overall symptoms after 4 weeks of treatment was observed among 63% of patients in shallot group and 38% patients in control group. Edible plants of Allium sp. as a potential source of nutrition and as a poultry feed additive have been reviewed recently [158], thus opening up a new phase of research avenue.

4

Toxicity

In majority of the instances, toxicity is linked with inappropriate consumption or with wrong identity of plants considered to belong to edible Allium species. For example, mistaken identity for wild garlic (Allium ursinum) had led to accidental poisoning (misidentity with Autumn crocus or the Colchicum autumnale). The patient who had consumed this had showed mild gastrointestinal symptoms followed by agranulocytosis, paraparesis, and delirium [159]. Death camas (Toxicoscordion venenosum), a plant looking like Allium sp., is considered as highly poisonous. However, these plants are devoid of the unique odor of garlic or onion [160]. Further there are ornamental onions (Allium giganteum or Allium procerum), which have pink- to purple-colored flowers with garlic onion odor, but are non-edible. These

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plants grow naturally in hilly regions of Himalayas and can be mildly poisonous if not properly processed and cooked. Reports are available wherein some of the Allium species have led to toxicity in domesticated animals like cattle, horse, sheep, and dogs [161–165]. Onion and garlic poisoning via oxidizing sulfur-containing compounds is also being documented [166]. Onion stimulated hemolytic anaemia from allyl-propylisulfide and di-propyl-disulfide is well-defined [165, 167]. Formation of Heinz body in erythrocytes leading to hemolytic anemia in dogs is reported on intake of boiled onions [168]. However, reports available on toxicity induced in humans still remain scarce.

5

Conclusions

Plants belonging to Allium species have tremendous potential to be used in food and pharmaceutical applications. Majority of the popular plants have been proved to have traditional values and have been used over centuries for many of the culinary and medicinal purposes. With a wide range of bioactivity exhibited by a range of phytochemicals isolated and identified, definitely there is ample scope for future innovations to be undertaken on the use of natural plant-based bioactive compounds from Allium sp. over those of chemically synthesized ones. Though only few selected plant species of Allium has been studied, it is worth to explore the potential of other wild and underutilized species too. In this regard, research focus needs to be initiated to collect, preserve, and assess the germplasm of superior genotypes to study bioactive compounds of interest. In majority of the instances, studies undertaken on bioactivity still remains scattered. Hence, research efforts need to be initiated to undertake in vitro and in vivo studies toward establishing the bioactive potential of various edible plants of Allium sp. On the other note, modern-day green processing methods (e.g. supercritical CO2 extraction, microwaves, ultrasound, etc.) can be explored for better extraction of bioactive compounds. Besides, biotechnological tools such as metabolic engineering, omics data, tissue culture, and others can be explored for better understanding of the therapeutic potential of plants belonging to Allium sp. Nevertheless, going with the present-day trend, efforts need to be initiated to effectively and efficiently valorize the wastes and by-products (e.g. onion and garlic skin, stem, stalk, and other wastes) which are envisaged to encompass rich amounts of bioactive compounds of economic importance. Acknowledgments The theme of this chapter is based on ongoing project VALORTECH, which has received funding from the European Union’s Horizon 2020 research and innovation program under grant agreement No 810630.

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Bioactive Compounds of Turmeric (Curcuma longa L.)

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Josemar Gonc¸alves de Oliveira Filho, Micael Jose´ de Almeida, Tainara Leal Sousa, Daiane Costa dos Santos, and Mariana Buranelo Egea

Contents 1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 Nutritional Composition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 Essential Oils from C. longa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 Phenolic Compounds of C. longa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 In Vitro and In Vivo Antioxidant Activity of C. longa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Abstract

Curcuma longa, a native species to South Asia, is commonly known as turmeric and traditionally used as a spice and dye in culinary preparations and as a traditional herbal medicine. The bioactive compounds of C. longa have different effects such as antioxidant, antitumor, antimicrobial, insecticide, larvicide, repellent, anticancer, anti-inflammatory, healing, and gastroprotective properties. In this chapter, we describe the major chemical compounds present in C. longa and how these compounds demonstrate biological potential in human health. C. longa and its bioactive compounds have important health-promoting effects and have the potential for the development of pharmaceuticals, nutraceuticals, or food ingredients. J. G. de Oliveira Filho School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, SP, Brazil M. J. de Almeida · M. B. Egea (*) Instituto Federal de Educação, Ciência e Tecnologia Goiano, Rio Verde, GO, Brazil e-mail: [email protected] T. L. Sousa · D. C. dos Santos Institute of Tropical Pathology and Public Health, IPTSP – UFG, Goias Federal University (UFG), Goiânia, GO, Brazil © Springer Nature Switzerland AG 2021 H. N. Murthy, K. Y. Paek (eds.), Bioactive Compounds in Underutilized Vegetables and Legumes, Reference Series in Phytochemistry, https://doi.org/10.1007/978-3-030-57415-4_37

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Keywords

Antimicrobial activity · Antioxidant activity · Curcumin · Essential oils · Phenolic compound Abbreviations

2-DR ABTS CAT COX CUPRAC DPPH EO FDA FRAP GAE HDL IC50 IL-1/IL-6 iNOS LPS LPSE MCP-1 MDA MMP-9 MPNST NF-κB NO ORAC RDA SOD TE TEAC TNF WHO

1

2-Deoxyribose 2,20 -Azinobis-(3-ethylbenzthiazolin-6-sulfonic acid Catalase Cyclooxygenase Cupric reducing antioxidant capacity 1,1-Diphenyl-2-picrylhydrazyl Essential oil Food and Drug Administration Ferric ion reducing antioxidant power Gallic acid equivalent High-density lipoproteins 50% inhibitory concentration values Interleukin 1/interleukin 6 Inducible nitric oxide synthase Lipopolysaccharide Low-pressure solvent extraction Monocyte chemoattractant protein-1 Malondialdehyde Matrix metallopeptidase 9 Malignant peripheral nerve sheath tumor Factor nuclear kappa B Nitric oxide Oxygen radical absorbance capacity Recommended daily allowance Superoxide dismutase Trolox equivalent Trolox equivalent antioxidant capacity Tumor necrosis factors World Health Organization

Introduction

Curcuma longa L., popularly known as “turmeric” belongs to the family Zingiberaceae, has been used since ancient times as a condiment, preservative, flavoring, and coloring, as well as a folk remedy for the treatment of various types of diseases mainly in Asia [1, 2]. More than 70 varieties of turmeric are known, produced, and marketed and may differ in chemical properties [3].

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Bioactive Compounds of Turmeric (Curcuma longa L.)

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Turmeric is grown in many hot regions of the world, mainly in India, which is the largest producer, consumer, and exporter [4, 5]. In India, turmeric is grown on about 180,000 ha, producing 25 million tons per year [5]. The plant is exported to the United States, the United Kingdom, Japan, Iran, United Arab Emirates, Saudi Arabia, the Netherlands, South Africa, and Singapore in the form of dry rhizome, turmeric powder, oleoresin, essential oil, curry powder, or curcumin [6, 7]. Turmeric is commercially available as a powdered rhizome. Usually fresh rhizomes are boiled in water and dried in the shade or by other methods to reduce the amount of water, and finally the dry extract is homogenized. The powder is used for culinary purposes as a coloring and flavoring for foods such as sauces, cheeses, soups, spices, drinks, baked products, cookies, cake toppings, canned drinks, dairy products, ice cream, yellow cakes, yogurt, orange juice, popcorn, candies, sauces, and jellies, among others [4, 8, 9]. The largest bioactive component of turmeric is a phenolic compound of the curcumin class (2–9% of the total composition) known as curcumin (70–75%) [10, 11], followed by demethoxycurcumin (10–25%) and bisdemetoxicurcumin (5–10%). These compounds are also responsible for the characteristic yellow color, and this composition may vary depending on the condition of the soil and the source where it is grown, as well as with the processing steps [12, 13]. Precisely due to its chemical composition, powdered turmeric as well as its isolated phenolic compounds has wide important pharmacological applications in humans for pain management [14], against skin disease [15], Crohn’s disease, and ulcerative colitis [16], as well as antioxidant, anti-inflammatory [17, 18], antibacterial [19–22], antifungal [21–25], antidiabetic [13], insecticidal, and larvicidal [5, 26, 27] activities, among others. Thus, the objective of this chapter is to describe the compounds present in C. longa that have biological functions in the human organism and which, therefore, make this food a source of bioactive compounds.

2

Nutritional Composition

Table 1 shows the proximal composition for turmeric on a dry basis. The available literature highlights the large amount of carbohydrate (~40%), with emphasis on the high content of dietary fibers, proteins (~17%), and lipids (~5%), in addition to vitamins and minerals (~3%) such as magnesium and iron (which are counted within the ash content), among other nutrients [33]. Turmeric contains a high carbohydrate content (~42 g 100 g1), which makes it a good source of energy and contributes to the digestion and assimilation of other nutrients [34]. Among these carbohydrates, the percentage of the native starch found in C. longa (22%) is similar to the amount of starch found in the potato and shows a more orderly and crystalline structure and a triangular shape with smooth surfaces [35]. In addition, turmeric has a high content of total dietary fiber (~36 g 100 g1) compared with the Brazilian legislation, which recommends 6 g of fiber per 100 g of product [36]. Meanwhile, the US Food and Drug Administration (FDA)

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Table 1 Proximal composition of the turmeric Contents Moisture (g 100 g1) Protein (g 100 g1) Lipid (g 100 g1) Ash (g 100 g1) Carbohydrate (g 100 g1) Crude fiber (g 100 g1) Total dietary fiber (g 100 g1) Soluble fiber (g 100 g1) Insoluble fiber (g 100 g1) Energy (kcal 100 g1)

Range 7.83–44.38 2.03–39.50 0.91–8.09 1.84–13.5 9.83–67.38 2.60–10.60 35.60–35.60 – – 275.46–275.46

Median 16.07 5.87 4.35 2.85 46.15 3.60 35.60 – – 275.46

Mean 18.67 9.61 4.34 5.59 41.12 4.89 35.60 – – 275.46

References [28–32]

recommends that the dietary fiber recommended daily allowance (RDA) for adults (male/female) is 21/38 g, which can be supplied by ingesting approximately 100 g of turmeric [37]. Quantities of minerals and vitamins in turmeric (per 100 g dry matter) include 200 mg of calcium, 260 mg of phosphorus, 2500 mg of potassium, 47.5 mg of iron, 0.9 mg of thiamine (B1), 0.19 mg of riboflavin (B2), 4.8 mg of niacin (B3), and 50 mg of ascorbic acid [38]. However, minerals reported for C. longa leaves (per g) include 6.43 mg of potassium, 9.06 mg of calcium, 0.23 mg of iron, 11.23 mg of magnesium, 2.25 mg of manganese, 0.07 mg of zinc, and 5.49 mg of phosphorus [34]. Considering adults between 19 and 50 years old, the contribution of 100 grams of turmeric to the RDA for females and males, respectively, is 594 and 264% of iron, 96 and 74% of potassium, 37% of phosphorus (for both genders), and 20 and 17% of calcium for minerals and 75 and 82% of thiamin, 30 and 35% of niacin (B3), and 14 and 17% of riboflavin (B2) [37]. Turmeric stands out for improving the supply of iron, which is important in immune function, cognitive development, temperature regulation, and metabolism [39].

3

Essential Oils from C. longa

Table 2 shows the essential oil (EO) composition from different parts of C. longa. Some differences are presented in this composition that may depend on genetics, nature of the raw material (dry or fresh) and part of the plant, harvest time, geographical conditions, light, and method used in oil extraction [45]. Several studies in the literature have revealed that the C. longa EO has several bioactivities such as antimicrobial larvicide, repellent, antioxidant, anti-inflammatory, and anticancer. The antioxidant activity has been estimated using several methods such as elimination of 1,1-diphenyl-2-picrylhydrazyl (DPPH), 2,20 azinobis-(3-ethylbenzthiazolin-6-sulfonic acid (ABTS), ferric ion reducing antioxidant power (FRAP) assay, Trolox equivalent antioxidant capacity (TEAC), and

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Table 2 Compounds responsible for the bioactive potential of the essential oil of C. longa Vegetable part Rhizome

Leaves

Leaves Rhizome

Rhizome

Rhizome

Rhizome Rhizome

Rhizome

Rhizome Rhizome

Majority compounds Ar-turmerone, curlone, β-turmerone, 8,9-dehydro-9-formylcycloisolongifolene, βsesquiphellandrene, germacrone, arcurcumene, α-himachalene, and andledane α-Phandandrene, α-pinene, β-pinene, myrcene, ρ-cymene, limonene, and 1,8cineole Cis-sesquisabinene hydrate, curzerenone, β-bisabolol, and farnesol α-Turmerone, β-turmerone, αphellandrene, terpinolene, αzingiberene, β-sesquiphellandrene, arturmerol, curzerenone, and arturmerone 1,8-Cineole, α-phellandrene p-cymene, terpinolene α-zingiberene, and βsesquiphellandrene Ar-turmerone, β-turmerone, αturmerone, ar-curcumene, βphellandrene, α-terpinene, limonene, γterpinene, and α-phellandrene – Ar-turmerone, β-turmerone, αzingiberene, ar-curcumene, and βsesquifelandreno Ar-turmerone, α-turmerone, βturmerone, α-phellandrene, αzingiberene, β-sesquiphellandrene, arcurcumene, and eucalyptol Aromatic-turmerone, α-turmerone, and β-turmerone –

Bioactivity(ies) Anti-age

References [40]

Larvicide

[5]

Antioxidant and antimicrobial Antioxidant, antifungal, and antimicrotoxigenic

[6]

Anxiolytics, sedatives, and anticonvulsants

[41]

Antimicrobial

[42]

Antifungal and antiaflatoxigenic Antimicrobial, antioxidant, cytotoxicity, and anti-inflammatory Antioxidant

[43]

Antioxidant

[44]

Repellent

[26]

[24]

[19]

[8]

metal chelation [6, 19, 24, 44]. The EO antioxidant activity can be attributed to its radical reducing and scavenging capabilities from phenolic compounds. These compounds, present in EO, are excellent free radical scavengers because the reduction potential (phenolic radical) is less than the oxygen reduction potential [6]. C. longa EO has shown the ability to inhibit the growth of Mycobacterium smegmatis [6], Fusarium verticillioides [24], Microsporum gypseum, Epidermophyton floccosum, Trichophyton mentagrophytes, Trichophyton rubrum [25], Escherichia coli, Pseudomonas aeruginosa, Staphylococcus aureus, Candida albicans, and Saccharomyces cerevisiae [19]. The EO antimicrobial activity is attributed to its

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hydrophobic nature, which alters the integrity of the microorganism’s membrane, resulting in the loss of cytoplasmic material [24]. Compounds isolated from C. longa have demonstrated excellent antibacterial activity such as ar-curcumene [46] and αzingiberene (Fig. 1) [20], as well as antibacterial and antifungal activities such as arturmerone, curdione, curzerene, and β-elemenone [21, 22]. The EO still inhibits the production of mycotoxins from Aspergillus flavus through the negative regulation of the expression of the aflatoxin gene [43]. The larvicidal, insecticidal, and repellent potential of C. longa EO has also been reported [5, 26, 27]. The larvicidal activity of C. longa EO is associated with αphellandrene, its majority component [5]. The insect repellent [26] and insecticide [27] potentials of C. longa EO are strongly associated with ar-turmerone, one of the main compounds found in this oil [47]. The antitumor activity of C. longa EO has been reported in vitro against prostate cancer cells (LNCaP) and melanoma (B16) [19] and has been associated with the presence of some compounds such as α-zingiberene [48], β-turmerone, αzingiberene [18], ar-turmerone, β-elemenene, germacrone, and β-sesquiphellandrene [49, 50] (Fig. 1). C. longa EO had anti-inflammatory activity and was able to prevent inflammation of mouse ear tissues [19]. The anti-inflammatory actions of C. longa EO are related to the negative regulation of inflammatory cytokines. Naked mice exposed to UVB light previously treated with C. longa essential oil showed a significant reduction in the levels of pro-inflammatory cytokines (IL-1β and TNF-α) in the dorsal tissues, suggesting that topical treatment with this essential oil can suppress inflammatory reactions in UVB-induced skin [40]. In addition, the ar-turmerone was able to suppress Aβ-induced expression and activation of MMP-9, iNOS, and COX-2, to reduce TNF-α, IL-1β, IL-6, and MCP-1 production in microglial cells, impairing the inflammatory response [51]. A β-turmerone and ar-turmerone inhibited lipopolysaccharide (LPS)-produced prostaglandin E2 in the mouse macrophage cell and showed inhibition of LPS-induced nitric oxide (NO) formation [52].

Fig. 1 Major essential oils of Curcuma longa

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The antiaging activity of the C. longa EO has been reported through its ability to reduce skin photoaging in a naked mouse model irradiated using UVB [40]. According to the authors, the compounds ar-turmerone, curlone, and β-turmerone were the main contributors to the antiaging effect of the skin of the C. longa EO. The antiaging potential of this EO is related to its anti-inflammatory capacity [40]. Therefore, C. longa EO is a potential raw material for the development of pharmaceuticals, nutraceuticals, or food ingredients with functional properties. Moreover, EO still demonstrates having a fatty acid profile. Unsaturated or polyunsaturated fatty acids are considered better for human health compared to saturated or less unsaturated fatty acids. However, more unsaturated fatty acids are also more prone to oxidation in food products [53]. Monounsaturated fatty acids such as oleic acid (56.24–58.88%) have been reported as the main component of this group for C. longa from different regions of Bangladesh [54], followed by linoleic acid (10.90–12.82%), linolenic acid (4.15–5.46%), and eicosanoid acid (2.72– 3.25%). Among the saturated fatty acids present in the oil samples were mainly myristic acid (16.25–17.71%) and palmitic acid (5.59–6.00%) [54].

4

Phenolic Compounds of C. longa

Table 3 shows the phenolic compounds from turmeric. Turmeric curcuminoids are mainly accumulated in rhizomes (plant part known as turmeric), and their content often varies with their varieties, sources, geographic areas, and growing conditions (before and after planting) [77–79], planting maturity or time [79, 80], and extraction conditions of the compounds (solvent, time, and temperature) [3]. Rhizomes and epicarp of C. longa are sources of phytochemicals including phenolic compounds (4–17 g GAE 100 g1 of sample), and mainly the curcumin content varies from 4 to 7 mg g1. In dry powder, a commonly commercialized form, the turmeric presents ~42% less total phenolic compounds compared with fresh matter [81, 82]. This is because higher temperatures in the drying process affect the extraction yield and content of curcuminoids, resulting in greater losses of volatile substances, degradation of pigments, and lower yields when compared to lower temperatures [83, 84]. On the other hand, drying using microwaves has proven to be the most suitable method for the production of dry C. longa leaves, causing less degradation of phenolic compounds in comparison with lyophilization [34]. Use of high-temperature exposures of curcumin to oxygen and light promotes the degradation of this molecule [85], limiting the efficiency of processes and the application of turmeric in food products [83]. Turmeric also contains total flavonoids and tannins from 0.4 to 10 g catechin equivalent 100 g1 of sample and 0.8 to 30 g TE 100 g1 of sample, respectively [82]. On the other hand, C. longa leaves showed 412.29 mg 100 g1dry matter of total phenolic content, 330.32 mg 100 g1 dry matter of content of hydrolyzed tannins, and 1756.43 mg 100 g1 dry matter of condensed tannins [34]. In general, this value was higher than that reported for leaves of edible parts of carrots (3.54 mg GAE100 g1) and beets (5.36 mg GAE 100 g1) [86]. The literature has excellently demonstrated the difference in determining these phytochemicals in terms of their

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Table 3 Phenolic compounds from turmeric No 1

Phenolic compounds Bisdemethoxycurcumin

2

Caffeic acid

3

Catechin

4 5 6 7

Chlorogenic acid t-Cinnamic acid Cinnamic acid p-Coumaric acid

8 9

Coumarin Curcumin

10 11

Cyclobisdemethoxycurcumin Demethoxycurcumin

12 13

Epicatechin Ferulic acid

14

Gallic acid

15 16 17 18 19 20 21 22 23 24

Genistein Myricetin Protocatechuic acid Quecercetin Quercetin Rutin Syringic acid Sinapic acid Salicylic acid Vanillic acid

Amount 875.6 mg 100 g1 100 mg 100 g1 1000 mg 100 g1 12.1 mg 100 g1 25 mg 100 g1 10.8 mg 100 g1 20.3# mg 100 g1 17.9# mg100 g1 22.0 mgkg1 10.3#–13.2## mg100 g1 16.2 mg 100 g1 5.9 mg 100 g1 15 mg 100 g1 25.0# mg 100 g1 1326.2 mg 100 g1 2120 mg 100 g1 2590 mg 100 g1 98.6#–108## mg 100 g1 0.1 μmol g1 825.7 mg 100 g1 460 mg 100 g1 1980 mg 100 g1 28.0##–45.5# mg 100 g1 47.4 mg 100 g1 17.6 mg 100 g1 187# mg 100 g1 0.7 mg 100 g1 749##–781# mg 100 g1 33.1# mg 100 g1 5.3## mg 100 g1 21.6##–33.1# mg 100 g1 4.8# mg 100 g1 2746.2 mg kg1 8.0##–19.9# mg 100 g1 27.8 mg kg1 417.4 mg kg1 11.1 mg kg1 83.2 mg kg1

References [3] [3] [55] [55] [56] [55] [57] [57] [55] [57] [55] [58] [56] [57] [3] [59] [55] [57] [3] [3] [59] [55] [57] [55] [56] [57] [55] [57] [57] [57] [57] [57] [55] [57] [55] [55] [55] [55]

# and ## different extraction methods described in Table 4

origin. However, all of these phytochemicals also vary according to the form of extraction and methods used in the determination and quantification, as shown in Table 4.

1, 11, 9, 13, 24, 1,5-bis(4-hydroxy-3-methoxyphenyl)-penta-(1E,4E)1,4-dien-3-one, vanillin, 1,5-bis(4-hydroxyphenyl)-1,4-pentadiene3one, and (1E,4E)-1,5-bis(4-hydroxy-3methoxyphenyl)-penta-1,4dien-3-one

1, 11, 9, (1E,6E)-1-(3,4-dihydroxyphenyl)-7 (4hydroxyphenyl)-1,6 heptadiene-3,5-dione, (1E,6E)-1-(3,4-dihydroxyphenyl)-7-(4hydroxy-3-methoxyphenyl)-1, 6-heptadiene-3,5-dione, 1,7-bis(3,4dihydroxyphenyl)-1, 6-heptadiene-3,5-dione, curcumalongin C, 1,5bis-(4-hydroxyphenyl)-1,4-pentadiene3-one, (4Z,6E)-5-hydroxy-1,7bis-(4hydroxyphenyl)-4,6-heptadien-3-one, (4Z,6E)-(+)-1,5dihydroxy-1,7-bis-(4hydroxyphenyl)-4,6-heptadien-3-one, 4Z,6E)()-1,5-dihydroxy-1-(4-hydroxy-3methoxyphenyl)-7-(4hydroxyphenyl)-4,6heptadien-3-one, (4Z,6E)-(+)-1,5-dihydroxy-7(4-hydroxy-3methoxyphenyl)-1-(4-hydroxyphenyl)-4,6heptadien-3one, (4Z,6E)-1,5-dihydroxy-1,7-bis(4-hydroxy-3methoxyphenyl)4,6-heptadien-3-one, (6E)-()-3-hydroxy-1,7-bis (4hydroxyphenyl)-6-heptene-1,5-dione, (1E,4E,6E)-1,7-bis(4hydroxyphenyl) hepta-1,4,6-trien-3-one, curcumalongin A, and curcumalongin B 1,5-Epoxy-3-carbonyl-1,7-bis(4-hydroxyphenyl)-4,6-heptadiene

1 and 9

Compoundsa 1, 11, 9, and 10

Dried extraction with tetrahydrofuran of the rhizome from Thailand (air for 2 days + 50 °C for 24 h) Extraction (3) using MeOH for 3 days of the dry rhizome from Taitung (Taiwan)

Sample description Extraction using MeOH (200 mL) for 2 days (25 °C) with magnetic stirring of the rhizome in dry powder (50 °C for 72 h) Extraction using dichloromethane with reflux system of the turmeric powder from the local market (New Delhi, India) Extraction using MeOH (3) of the dry rhizomes from Jeonnam (Korea)

Table 4 Origin of turmeric, extraction methods, and phenolic compounds found in C. longa

(continued)

[62]

[61]

[60]

[59]

References [3]

15 Bioactive Compounds of Turmeric (Curcuma longa L.) 305

1-(4-Hydroxy-3-methoxyphenyl)-7-(3, 4-dihydroxyphenyl)-1, 6heptadiene-3, 5-dione, 1-(4-hydroxyphenyl)-7-(3, 4dihydroxyphenyl)-1, 6-heptadiene-3, 5-dione, 3-hydroxy-1,7-bis-(4hydroxyphenyl)-6-heptene-1,5-dione, 1,5-dihydroxy-1-(4-hydroxy3-methoxyphenyl)-7-(4-hydroxyphenyl)-4,6-heptadiene-3-one, 1,5dihydroxy-1-(4-hydroxyphenyl)-7-(4-hydroxy-3-methoxyphenyl)4,6-heptadiene-3-one, 1,5-dihydroxy-1,7-bis(4-hydroxy-3methoxyphenyl)-4,6-heptadiene-3-one, 1,5-dihydroxy-1,7-bis(4hydroxyphenyl)-4,6-heptadiene-3-one, and 1-(4-hydroxy-3methoxyphenyl)-5-(4-hydroxyphenyl)-1, 4-pentadiene-3-one Terpecurcumin A, bisabolocurcuminether, demethoxybisabolocurcuminether, didemethoxybisabolocurcuminether, terpecurcumin B, terpecurcumin C, terpecurcumin D, terpecurcumin E, terpecurcumin F, terpecurcumin G, terpecurcumin J, terpecurcumin H, terpecurcumin I, and terpecurcumin T

5-Hydroxyl-1-(4-hydroxy-3-methoxyphenyl)-7-(4-hydroxyphenyl)4,6-heptadiene-3-one, 5-hydroxyl-1,7-bis(4-hydroxy-3methoxyphenyl)-4,6-heptadiene-3-one, and 1,7-bis(4hydroxyphenyl)-1-heptene-3,5-dione, and5-hydroxyl-7-(4-hydroxy3-methoxyphenyl)-1-(4-hydroxyphenyl)-4,6-heptadiene-3-one 1, 11, 9, 13, 24, p-Hydroxycinnamic acid, and coniferyl aldehyde

1, 11, 9, and p-Hydroxycinnamic acid, and coniferyl aldehyde

Compoundsa 1, 11, and 9

Table 4 (continued)

Extraction with 95% EtOH at 80 °C of the dry rhizomes from Sichuan (China)

Extraction with ethanol or methanol and agitation for 15 min of the turmeric powder purchased from Touch of Asia (Hamilton, NJ) Extraction with 95% ethanol (3) by percolation of the dry rhizomes from Sichuan (China)

Sample description Ultrasound extraction for 25 min three times, once with 80% methanol, followed by extraction with 50% methanol and finally with 100% methanol from dry rhizome from China MeOH extraction for 5 days of air-dried rhizomes from Chunnam (Korea) Acetonitrile extraction of lyophilized rhizomes from Okinawa

[68]

[67]

[66]

[65]

[64]

References [63]

306 J. G. de Oliveira Filho et al.

11, 9, (1E,4E)-1-(4-Hydroxy-3-methoxyphenyl)-5(4hydroxyphenyl)-1,4-pentadien-3-one, (1E,4E)-1,5-bis(4-hydroxy3methoxyphenyl)-penta-1,4-dien-3-one, and bisabocurcumin

2 and 7

Terpecurcumin A, bisabolocurcuminether, demethoxybisabolocurcuminether, terpecurcumin U, terpecurcumin S, didemethoxybisabolocurcuminether, terpecurcumin B, terpecurcumin F, terpecurcumin G, terpecurcumin J, terpecurcumin L, terpecurcumin M, terpecurcumin N, terpecurcumin O, terpecurcumin P, terpecurcumin V, terpecurcumin W, terpecurcumin H, terpecurcumin T, terpecurcumin X, and terpecurcumin Y 1, 11, 9, Apigenin, apigenin-7-O-β-d-glucopyranoside, luteolin, luteolin-7-O-β-d-glucopyranoside, and luteolin-7-O-(600 -phydroxybenzoyl-β-d-glucopyranoside 1,7-Bis-(4-hydroxyphenyl)-1,4,6-heptatrien-3-one and 1,5-bis(4hydroxyphenyl)-penta-(1E,4E)-1,4-dien-3-one 13 and 7

5-Hydroxyl-1-(4-hydroxy-3-methoxyphenyl)-7-(4-hydroxyphenyl)4,6-heptadiene-3-one, and 1,7-bis-(4-hydroxy-3-methoxyphenyl)1,4,6-heptatrien-3-one 1, 11, 9, and tetrahydroxycurcumin

Terpecurcumin K, terpecurcumin L, terpecurcumin M, terpecurcumin N, terpecurcumin O, terpecurcumin P, terpecurcumin Q, terpecurcumin R, terpecurcumin V, and terpecurcumin W 1, 11, 9, 14, 21, 2, 24, 13, 19, 3, 5, 7, 22, and 21

[74]

Extraction with EtOH (95%) of rhizomes collected in Shuangliu (China) Extraction using enzymes in a water bath for 1 h at 37 °C, maintained at 20 °C/24 h + methanol + sonication and agitation for 10 min of the lyophilized rhizomes from Jurbo Agro (Poland) Aqueous extraction with reflux at 95 °C for 30 min of the rhizomes (dried at 50 °C) from the local market in Chiang Rai (Thailand) Extraction with petroleum ether and EtOAc of the turmeric powder from Sichuan (China)

Bioactive Compounds of Turmeric (Curcuma longa L.) (continued)

[75]

[56]

[58]

[73]

[72]

[71]

Extraction with EtOH (80%) at 80 °C of the rhizomes from the local market (Cairo, Egypt)

Extraction with methanol (two times) at 24–26 °C for 2 days of dry rhizomes from the local market (Seoul, South Korea) Extraction with methanol of the dry rhizomes

[55]

Extraction with methanol for 72 h and continuous agitation of rhizomes from all India Extraction with methanol (90%) overnight (3) by percolating turmeric (Swagger Foods Corporation, Vernon Hills, IL) [70]

[69]

Extraction with 95% EtOH at 80 °C twice of the air-dried rhizomes from Sichuan (China)

15 307

References [76]

[57]

Sample description Extraction with petroleum ether and AcOEt of the turmeric powder from Sichuan (China) Ultrasonic extraction with ethanol (80%) at 35 °C (#) or conventional extraction (water bath) with ethanol (80%) at 35 °C (##) of the turmeric powder acquired from Shopping Taobao (Zhejiang, China)

The compounds in this column that are numbered were previously described in Table 3 # and ## different extraction methods that result in different phenolic compound profiles previously demonstrated in Table 3

a

Compoundsa 1,5-Bis-(4-hydroxyphenyl)-1,4-pentadiene3-one, (1E,4E,6E)-1,7-bis (4-hydroxyphenyl)-1,4,6heptatrien-3-one, and bisabolocurcuminether 9, 14, 17, 4, 13, 20, 3, 12, 8, 16, 6, 15, and 18

Table 4 (continued)

308 J. G. de Oliveira Filho et al.

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The phenolic compounds present in the turmeric can be extracted using various techniques such as hydrodistillation, low-pressure solvent extraction, Soxhlet, supercritical extraction (carbon dioxide and co-solvents), ultrasonic method, and microwave [83, 87–90]. The use of water does not favor the extraction of total phenolic compounds, flavonoids, and curcumin [91], due to the low solubility of curcuminoids in water [92]. However, the previous immersion of the rhizome contributes positively in the extraction of these compounds [88]. On the other hand, the extraction with ethanol presents higher yields and a high concentration because it favors the solubilization of the most polar substances present in rhizomes (9 times higher phenolic compounds, 12 times higher total flavonoids, and 160 times higher curcumin) [84, 91]. The most used technique for extracting curcuminoids is acetonitrile/methanol extraction for protein precipitation and liquid-liquid extraction [93]. In addition to the form of extraction to identify these compounds, the form of extraction for direct availability also influences both the quantity and bioavailability of curcumins. For example, micellar and micronized formulations of curcumin products can result in higher absorption and bioavailability of free and bioactive curcumin and its metabolites (100–400 times higher absorption) compared to unformulated curcumin [94]. The main phenolic compounds present in C. longa include demethoxycurcumin and bisdemethoxycurcumin, which are rich in curcumin (main active compound) (Fig. 2) [3, 95]. The World Health Organization (WHO) suggests that the minimum content of 3.0% curcumin for turmeric increase the importance of determining curcumin for turmeric. High content of curcumin in these rhizomes, associated with the intensity of the orange color, shows high antioxidant activity and superior health-promoting properties [55].

Fig. 2 Major chemical compounds found in C. longa

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The effect of curcumin is associated with the chelation of transition metals (iron and copper), resulting in its antioxidant capacity, protecting it from oxidative stress, and resulting in its anti-inflammatory action [96]. Regarding its antiobesogenic effect [97], curcumin can modulate molecular markers in the synthesis of HDL-c [98, 99], causing a reduction in total plasma cholesterol levels [100–102]; increase the elimination of cholesterol from the diet [100, 103] and decrease intestinal cholesterol absorption even in cases of high-fat diets [103, 104]; and decrease the attenuation of atherosclerotic lesions for modulating the pro-inflammatory cytokine levels and altering adhesion molecules and MMP gene expression [101]. In addition, curcumin, demethoxycurcumin, and bisdemethoxycurcumin can act to inhibit the enzymes acetylcholinesterase and butyrylcholinesterase, serving as potential drugs for Alzheimer’s disease, and inhibit the enzyme α-glucosidase, demonstrating antidiabetic activity [105]. Another phenolic that has a great potential as a bioactive compound is calebin A because it has an anti-tumor effect against colon [106] and stomach [107, 108] cancers; exhibits anti-MPNST effect, inhibiting the proliferation of malignant peripheral nerve sheath tumor (MPNST) and primary neurofibroma cells, with suppression of survivin and hTERT [108]; inhibits adipogenesis [109]; deregulates osteoclastogenesis by suppressing kB signaling (RANKL) [110]; protects neuronal cells from amyloid beta (peptides involved in Alzheimer’s disease) [70]; and inhibits the activity of histone acetyltransferase (HAT) and the factor associated with P300/ CBP (PCAF) [111].

5

In Vitro and In Vivo Antioxidant Activity of C. longa

Food oxidation can alter the quality, safety, and sensory characteristics. This process involves a chain reaction of free radicals, usually initiated by exposure to light, heat, and metal ions. The use of compounds with antioxidant activity is of great importance because it inhibits the oxidation of free radicals and prevents the oxidation of lipids in food [44]. Although synthetic antioxidant agents are widely used to prevent lipid deterioration in food, they often have serious side effects. Therefore, other natural compounds, such as phenolic compounds, are considered strong radical scavengers and can be considered as a good strategy [112]. In this sense, C. longa is a recognized source of compounds with antioxidant activity that seems to be its most promising quality with a beneficial health effect [9, 82]. In vitro antioxidant capacity of C. longa has been reported in several studies by different methods (DPPH, FRAP, ABTS, TAC, CUPRAC, ORAC, and 2-DR methods). Tavir et al. [82] evaluated the antioxidant activity of aqueous and ethanolic extracts of popular varieties of C. longa from Bangladesh using the DPPH and FRAP methods. The extracts showed DPPH radical scavenging activity with 50% inhibitory concentration values (IC50) ranging from 1.08 to 16.55 μg mL1 and FRAP values ranging from 646.67 to 4204.46 μM Fe [II] 100 g1. The authors attributed the antioxidant activity of the extracts to the high content of phenolics and flavonoids with greater reducing capacity. Denre [113] observed IC50 of 5.99 mg mL1 using

15

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DPPH radical scavenging of C. longa from West Bengal (India). Widowati et al. [114] observed an IC50 value of 8.33 μgmL1 using DPPH radical scavenging of C. longa from Indonesia. Muhamed et al. [115] observed IC50 of 21.25 μg mL1 using DPPH radical scavenging of C. longa from Malaysia. Akter et al. [3] evaluated the antioxidant activity of different Curcuma species and varieties and observed that C. longa Ryudai developed in Japan had the highest DPPH radical scavenging activity (IC50, 26.4 μg mL1), ORAC (14,090 μmol Trolox equivalent g1 of extract), reduced energy absorbance (0.33), and hydroxyl radical scavenging activity (IC50, 7.4 μg mL1). The isolated compounds, such as bisabolone-9-one (1), 4-methylene-5-hydroxybisabola-2,10-diene-9-one (2), turmeronol B (3), 5-hydroxy-1,7-bis(4-hydroxy-3-methoxyphenyl)-1-hepten-3-one (4), 3-hydroxy-1,7-bis(4-hydroxyphenyl)-6-heptene-1,5-dione (5), cyclobisdemetoxicurcumin (6), bisdemetoxicurcumin (7), demethoxycurcumin (8), and curcumin (9), also demonstrated antioxidant activity. The IC50 for the DPPH radical scavenging activity was 474, 621, 234, 29, 39, 257, 198, 47, and 18 μM, and the hydroxyl radical scavenging activity was 25.1, 24.4, 20.2, 2.1, 5.1, 17.2, 7.2, 3.3, and 1.5 μM for compounds 1, 2, 3, 4, 5, 6, 7, 8, and 9, respectively. The antioxidant activity of different extracts (ethanolic, methanolic, water, and acetone) of C. longa was evaluated by the DPPH and FRAP methods, and the results showed that the ethanolic presented antioxidant activity, which shows to be the best solvent that results in maximum extraction of antioxidant compounds [116, 117]. The relationship between the quantification of the antioxidant potential (DPPH, ABTS, TAC, and CUPRAC) of 45 genotypes of C. longa suggested that it is high in most genotypes with dark orange rhizomes [55], which is related to the high content of phenolic compounds present in turmeric [116]. Curcumin, a phenolic compound present in turmeric, exhibits antioxidant activity preventing lipid peroxidation in several cells, including erythrocytes, liposomes, and macrophages. The presence of phenolic groups in the structure of curcumin explains its ability to react with reactive oxygen and nitrogen species [118]. Although the in vitro activity is an important determination because it allows the screening of the antioxidant capacity, the antioxidant activity in biological tissue results in the real interaction between food and the bioactive compounds present in the food. Antioxidant and anti-inflammatory effects of C. longa extract and curcumin were demonstrated in an animal model of asthma. The animals showed an increase in the total and differential count of leukocytes, NO2, NO3, and MDA and a decrease in lymphocytes, SOD, CAT, and thiol compared to controls. The increase in eosinophils, neutrophils, and monocytes demonstrated that both C. longa and curcumin have potential to improve immunity in the model studied [119].

6

Conclusion

C. longa has a high content and good quality of carbohydrates, fibers, proteins, and lipids (mainly oleic acid). Essential oils and phenolic compounds of C. longa have been associated with several bioactivities such as antioxidant, antitumor,

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antimicrobial, insecticide, larvicide, repellent, anticancer, anti-inflammatory, healing, and gastroprotective activities. Knowledge of the health benefits of C. longa and its bioactive compounds contributes to its use in the development of pharmaceuticals, nutraceuticals, and food ingredients. Acknowledgments The authors acknowledge the financial support of CNPq, FAPEG, CAPES, and IF Goiano.

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Part V Bioactive Compounds in Underutilized Vegetables: Unripe Fruits

Bioactive Compounds of Culinary Melon (Cucumis melo subsp. agrestis var. conomon)

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Hosakatte Niranjana Murthy, So Young Park, and Kee Yoeup Paek

Contents 1 2 3 4 5 6

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Origin and Domestication . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Morphology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nutritional Compositions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Bioactive Compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Biological Activities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.1 Biological Activities of Fragrant Compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2 Biological Activities of Polyphenols . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.3 Biological Activities of Phytosterols . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Abstract

Culinary melon (Cucumis melo subsp. agrestis var. conomon) is an important vegetable crop cultivated in India, China, Southeast Asia, Korea, and Japan. Fruits are used for preparation of sambar, curry, chutney, and dosa in India, and in Japan fruits are used for preparation of pickles (therefore it is popular as oriental pickling melon) and juice. Seeds are good source of edible oil. Varied phytochemicals such as fragrant compounds, polyphenols, and phytosterols are isolated from this plant. Antioxidant, anticancer, anticarcinogenic, antidiabetic, H. N. Murthy (*) Department of Botany, Karnatak University, Dharwad, Karnataka, India Research Center for the Development of Advanced Horticultural Technology, Chungbuk National University, Cheongju, Korea (Republic of) S. Y. Park · K. Y. Paek Research Center for the Development of Advanced Horticultural Technology, Chungbuk National University, Cheongju, Korea (Republic of) e-mail: [email protected] © Springer Nature Switzerland AG 2021 H. N. Murthy, K. Y. Paek (eds.), Bioactive Compounds in Underutilized Vegetables and Legumes, Reference Series in Phytochemistry, https://doi.org/10.1007/978-3-030-57415-4_20

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antimicrobial, and antimutagenic properties are attributed to these compounds. In this chapter we reviewed the research work carried out on phytochemicals and their biological activities of this plant. Keywords

Culinary melon · Fragrant compounds · Oriental pickling melon · Polyphenols · Phytosterols

1

Introduction

Melon (Cucumis melo L.) belongs to family Cucurbitaceae, and it is one of the important horticultural crops cultivated throughout the world. Unripened fruits are used as vegetables and ripened once are used as desserts. Tremendous phenotypic variability has been found among cultivars, landraces, and feral and wild plants [1, 2]. Variations are also observed in flesh color (orange, green, and pink), rind color (green, yellow, white, orange, red, grey, and blend of these colors), rind texture (smooth, warty, striped, netter, rough, or combination of these textures), form/shape (round, flattened, or elongated), and size (from 4 cm up to 200 cm among the cultivars and landraces) [3]. Exclusively vegetable and dessert types have been evolved during the course of evolution and domestication of melons [1]. Culinary melon (Cucumis melo subsp. agrestis var. conomon) is a non-dessert type which is cultivated in India, China, Korea, Japan, and Southeast Asia, and the fruits are used solely as vegetables. It is also popular as oriental pickling melon or Japanese pickling melon. It is popular by varied vernacular names such as Cai Gua, Yue Gua (Chinese), Melon Sucrin, Melon Sucre (French), Gemuse-Melone, Zuckermelone (German), Ketimun Kari, Kari (Indonesian), Katsura-Uri, Shiro Uri (Japanese), Wolgwa (Korean), Dynia Ovoscenaja (Russian), Melon Manzana, Pepino Limon (Spanish), Taeng-Thai, Taeng-Lai (Thai), Dua Gang, and Dua Gang Trai Tron (Vietnamese) [4]. Culinary melon is also called as culinary cucumber in India which is widely cultivated in Karnataka, Kerala, Tamil Nadu, Telangana, and Andhra Pradesh [5]. Culinary melon depicts tremendous variability in South Indian states, and it is popularly known as “sambar cucumber” in Karnataka, “dosakaya” in Telangana and Andhra Pradesh, “Malabar cucumber”/“kani vellari”/“vellarikai” in Kerala, and “Madras cucumber” in Tamil Nadu [5]. Immature and mature fruits of culinary melon are eaten raw, cooked, pickled, and used in preparation of sweets and juice [4]. The usage of culinary melon (CM) fruits varied in the different regions of Southeast and East Asia. In Japan immature and mid-ripened fruits of Katsura-uri are traditionally used in the preparation of pickles; therefore, it is popular as “oriental pickling melon” [6]. However, in the modern days, its usage has reduced, and hence to popularize the usage of Katsura-uri, Sasaki et al. [6] has developed a low-calorie juice from a fully ripened Katsura-uri which is a very popular “functional drink” these days. Recently, various contemporary dishes, namely, “Gomafumi-ae,” boiled Katsura-uri fruit dressed in vinegar blended with soy sauce, sugar, sesame oil, and sesame seeds; “Tosa-ae,” salt-rubbed Katsura-uri fruit sprinkled

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with katsuobushi on entire surface; “Age-dashi,” deep-fried Katsura-uri fruit soaked with dashi; “Ikomi,” minced chicken stuffed into Katsura-uri fruit hollowed out in a semicircular shape; “Kimpira,” saturated finely cut strips of Katsura-uri fruit with soy sauce and sugar; and “Kanten-yose,” mashed, boiled Katsura-uri fruit jellified with dashi and agar, have been introduced by Sasaki et al. [7] which are also very popular dishes in Japan. In Southeast Asia, both immature and ripe fruits of CM are used in preparation of pickles, chutney, and sweets. In Indonesia, ripe fruits of CM are made into juice and mixed with sugar or honey and ice, this juice which is very popular drink during Ramadhan (fasting month in Indonesia). CM is made into special dish called “Rujak Cingur” fruit salad with savory and spicy peanut. The fruits can be finely diced and used as a seasoning in salads and soups. In Thailand, mature fruits are eaten fresh or cooked in sour curry. CM from India has a special feature that the fruits can be stored up to 8–10 months without losing their freshness [5]. The fruits are stored for many months by hanging them from the ceiling, firmly bound by thin coconut fiber ropes. The fruits are used as year-round vegetable in the preparation of dosa (a dosa is a cooked rice pancake, originating from South India; hence fruits are called dosakaya), chutney (a special sauce nature Indian subcontinent), curry, sambar (is a lentil-based vegetable stew, cooked with dal and tamarind broth, hence fruits are also called as “sambar cucumber” or “sambar melon”), and pickles. Thus, CM is a popular vegetable crop in India, Korea, Japan, and Southeast Asia. In view of the above, the current review is prepared to summarize the nutritional composition of CM fruits/seeds and bioactive compounds derived from CM fruits and their biological activities.

2

Origin and Domestication

Melon (Cucumis melo L.) has represented great variation in morphological and physiological characters such as size, shape, color, and taste of melon fruit. Naudin [8] classified cultivated melon (Cucumis melo L.) into var. reticulatus, var. inodorus, var. cantalupensis, var. makuwa, and var. conomon, while wild melon into var. agrestis. Later, Whitaker and Davis [9] subdivided C. melo subsp. melo into seven horticulturally important groups, and Munger and Robinson [10] reclassified the seven horticultural groups. More recently, Pitrat et al. [11] divided C. melo into two subspecies, ssp. agrestis and ssp. melo. Taxonomically, these two subspecies have distinct characteristics, i.e., C. melo subsp. melo having pilose or lanate ovaries with long hairs and C. melo subsp. agrestis having ovaries with short, appressed hairs [3]. Accordingly, C. melo subsp. melo consists of 11 varieties, namely, cantalupensis, reticulatus, adana, chandalak, ameri, inodorus, chate, flexuosus, dudaim, tibish and chito; and C. melo subsp. agrestis consists of 5 varieties, viz., momordica, conomon, chinensis, makuwa, and acidulus [11]. Phyto-geographical, historical, morphological, and cytological accounts suggest that sub-Saharan Africa is the place of origin of melon with India as the secondary center of diversity [9, 12]. However, various researchers have reported much diversity in melon landraces, cultivars in Asia [2, 13]. Further, crossing experiments and successful recovery of F1 offsprings could be achieved with Asian species rather

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than African species [14]. These evidences encourage researchers to think in favor of the Asian origin of melon; however, still more research evidences are needed to prove this hypothesis. More recently, Endl et al. [15] are of the view that two domestication events, viz., one in Africa and another in Asia, might have led the origin and diversification of melons. These views need further evaluation of domestication events by taking various lines of evidences and experimental proofs. CM is considered to be the most ancient form of melon domesticated in China [16, 17] from wild species C. agrestis var. agrestis, as evidenced by its information in the books of 1000 and 500 years BC [17]. According to Munger and Robinson [10], two types of landraces were evolved in ancient times, i.e., one type of fruits which is nonsweet, which exclusively evolved as vegetable type (which are currently eaten raw and pickled) and another type of fruits which are sweetish and evolved as dessert type. Only the first one has survived in the conomon group [18]. Extensive research has been carried out on East and South Asian melons since these melons are important genetic resources, having resistance to powdery mildew, downy mildew, stem blight, fusarium wilt, Aphis gossypii, and several viruses [9, 19–23]. However, classification of East and South Asian melons is still unclear, and antithetical opinions have been proposed. All cultivated melons other than var. momordica were classified as var. conomon by Munger and Robinson [10], while Naudin [8] classified all types of cultivated melon as var. acidulous. In contrast, Pitrat et al. [11] classified East and South Asian melon into five varieties, conomon, makuwa, chinensis, momordica, and acidulus, all of which belong to C. melo subsp. agrestis. Most recent molecular genetic analysis (AFLP, amplified fragment length polymorphism) carried out by Yashiro et al. [24] among the East and South Asian melons comprising of 99 melon accessions/cultivars mainly from India, Myanmar, China, Korea, and Japan has revealed that accession related to vars. Makuwa and conomon was found in East India, and they were considered as possible candidates of prototype of vars. Makuwa and conomon. These research evidences have clearly suggested that the conomon group of varieties conomon, makuwa, chinensis, momordica, and acidulous have evolved either in China and India, and hence Indo-China might be the original home of the conomon group of melons.

3

Morphology

Cucumis melo subsp. agrestis var. conomon are trailing, prostrate, or climbing, much-branched, annual, monoecious, herbs with angular, hirsute stem having a diameter of 5.5–8.5 mm., and tendrils simple, unbranched. Leaves are alternate, simple, suborbicular to ovate, shallowly 5–7 lobed, finely dentate margin and deeply cordate base, dark green, 7–18 cm long by 7–15 cm wide, 8–15 cm across, and both surfaces covered with villous hairs (Fig. 1a). Flowers andromonoecious yellowish on 3–5 cm long peduncle (Fig. 1b). Male flowers are fasciculated 2–4 flowered, 26– 44 mm across, calyx campanulate, sepals subulate, corolla campanulate, 5-parted, yellow, and stamens three. Perfect flowers solitary with a short sericeous (short,

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Fig. 1 Morphology of culinary melon (A) Trailing berb; (B) Flowers; (C) Fruit; (D) Longitudinal section of fruit showing firm flesh and seeds

adpressed hairs) ovary inferior, 3–5 carpels. Fruit, polymorphous, ellipsoid, ovaloblong, pyriform, globose, elongate pepo 11–30 cm long, smooth, glabrescent, color variable white (Fig. 1c), yellow, golden-yellow, yellowish-white, yellowish with white longitudinal stripes, green, green with dark green longitudinal stripes (Fig. 2), edible insipid to mildly sweet flesh, white, orange, yellow, or pink and numerous white, elliptic, small ( C. maritima. There are several factors that influence the proximal qualities of Canavalia. For instance, it depends on the nature of seeds (split beans of dry, germinated, and ripened seeds) and methods of processing (cooking, roasting, fermentation, and irradiation). The crude protein content showed a decreasing trend: raw seeds > roasted seeds > cooked seeds of C. cathartica, while it was opposite for total lipids and crude fiber [15, 16]. Raw, roasted, and cooked seeds of C. maritima showed a decreasing trend of crude protein, total lipid, and crude fiber [15, 17]. Significant increase of all proximal components of C. cathartica was seen on fermentation of cooked split beans with Rhizopus oligosporus, while a significant increase was seen in only crude proteins and carbohydrates in C. maritima [18, 19]. The electron beam (EB) irradiation (2.5–15 kGy) of C. cathartica seeds did not have any impact on the crude protein content of split beans and carbohydrate content significantly increased, while the total lipid and crude fiber contents showed a significant decrease [20]. Split beans of C. maritima showed a significant decrease of crude protein and carbohydrates (10 kGy), while total lipids and crude fibers significantly decreased (10 kGy) [21]. The sprouted seeds of C. cathartica by pressure-cooking significantly lost the crude protein and crude fiber in their split beans, while a significant increase was seen in total lipids and carbohydrates [22]. Unlike C. cathartica, there was no change in the crude protein, total lipids, and crude fiber in cooked germinated seeds of C. maritima, while the carbohydrates increased significantly [23]. The ripened whole seeds of C. cathartica showed decreased crude protein and total lipids on cooking, while crude fiber and carbohydrates increased [24]. Cooking the whole ripened seeds of C. maritima resulted in decreased crude protein, total lipids, and crude fiber, while an increase in carbohydrates [25]. Ripened split beans of C. cathartica on cooking showed a decrease in crude protein, while increase in total lipid, crude fiber, and carbohydrates [26]. The ripened split beans of C. maritima on cooking showed a decrease in crude protein and total lipids, while an increase in crude fiber and carbohydrates [26]. The proximal composition of seeds of nine accessions of C. ensiformis obtained from different agroclimatic regions of southern India showed differences in proximal properties possibly due to environmental and soil edaphic factors [27]. Fermentation of whole seeds of C. ensiformis (submerged in water for 72 h in dark) showed an improvement in nutritional constituents [28]. Although proximal qualities of Canavalia seeds showed favorable changes due to different methods of processing, such changes may be responsible for the loss of minerals and bioactive components (e.g., vitamins); thus, caution needs to be exercised to select the method of processing to avoid such shortcomings. Those changes will reflect in the calorific value; ratios of minerals, amino acids, and fatty acids; protein efficiency; and in vitro or in vivo protein digestibility.

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2.2

Bioactive Compounds of Jack Beans (Canavalia Species)

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Minerals

Micro- and macrominerals of seeds have a major impact on human health. Those seeds with low sodium and high calcium have appreciable benefits to combat blood pressure and prevention of calcium loss, respectively. Several minerals serve as prosthetic groups in functional macromolecules, involve in the regulation of transcription of receptors, and are necessary for antioxidant activities. Their deficiency leads to diseases like diarrhea, tooth decay, neuromuscular diseases, bone demineralization, tissue calcification, and so on. Minerals in Canavalia seeds are comparable or higher than some of the edible legume seeds [11]. Among them, the potassium is in the highest quantity, followed by phosphorus, calcium, and magnesium. However, with a few exceptions, none of the minerals fulfilled the dietary allowance stipulated by the NRC-NAS [29] for adults as well as children. Further decrease in minerals takes place while cooking; hence, caution needs to be exercised to follow the method of processing Canavalia seeds to avoid extensive loss of minerals. A comparison of minerals in raw, roasted, and cooked seeds of C. cathartica and C. maritima showed a decreasing trend of sodium, potassium, magnesium, and iron [15, 16, 30]. Only potassium content in raw and roasted seeds fulfilled the NRC-NAS pattern [29]. All the minerals significantly increased in the split beans of C. cathartica and C. maritima on fermentation with Rhizopus oligosporus [18, 19]. On EB irradiation (2.5–25 kGy), seeds of C. cathartica did not affect some of the minerals (sodium, potassium, calcium, iron, zinc, manganese), while phosphorus significantly decreased and a significant increase was seen in magnesium and copper [20]. In C. maritima, sodium, calcium, and zinc did not alter on EB irradiation, while depending on the doses, potassium, phosphorus, magnesium, and selenium increased and iron, copper, and manganese decreased [21]. Germinated C. cathartica and C. maritima lost most of the minerals on pressure-cooking [22, 23]. However, the cooked germinated seeds fulfilled the NRC-NAS [29] recommended pattern for magnesium, iron, copper, zinc, and manganese. Cooking the whole ripened seeds of C. cathartica and C. maritima resulted in a decrease of minerals [24, 25]. In raw and cooked seeds of both ripened seeds, only potassium, manganese, and zinc contents fulfilled the NRC-NAS pattern [29]. Ripened split beans of C. cathartica on cooking showed a significant decrease of minerals, while in C. maritima significant a decrease was seen only in potassium, while calcium, phosphorus, and iron increased significantly [26]. Ripened split beans of C. cathartica fulfilled the NRC-NAS recommended pattern [29] of magnesium, copper, and manganese, while in addition to these minerals, potassium and iron were also fulfilled in C. maritima [26]. The mineral composition of seeds of nine accessions of C. ensiformis from different agroclimatic regions of southern India showed drastic differences in mineral composition [27]. The N/K ratio in foodstuffs serves as an important index of health concern. Those foodstuffs consist of N/K ratio 1 to prevent the calcium loss in urine and restoration of calcium in the bones [32]. Almost all seeds of C. cathartica as well as C. maritima assessed showed the desired Na/K

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Table 1 Ratio of Na/K and Ca/P of Canavalia seeds

Split beans of dry seeds Split beans of roasted seeds Split beans of cooked seeds Split beans cooked and fermenteda Split beans of seeds EB irradiatedb Split beans of germinated seeds Split beans of cooked germinated seeds Ripened whole seeds Ripened cooked whole seeds Ripened split beans Ripened cooked split beans a

C. cathartica Na/K Ca/P