Paediatric Scoliosis 9819930162, 9789819930166

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Paediatric Scoliosis Balaji Zacharia S. Dilip Chand Raja Nikhil KV Editors

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Paediatric Scoliosis

Balaji Zacharia  •  S. Dilip Chand Raja Nikhil KV Editors

Paediatric Scoliosis

Editors Balaji Zacharia Department of Orthopaedics Government Medical College Kozhikode, Kerala, India

S. Dilip Chand Raja Department of Orthopaedic and Spine Kauvery Hospital Chennai, Tamil Nadu, India

Nikhil KV Department of Spine Surgery Meitra Hospital Kozhikode, Kerala, India

ISBN 978-981-99-3016-6    ISBN 978-981-99-3017-3 (eBook) https://doi.org/10.1007/978-981-99-3017-3 © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 This work is subject to copyright. All rights are solely and exclusively licensed 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 Singapore Pte Ltd. The registered company address is: 152 Beach Road, #21-01/04 Gateway East, Singapore 189721, Singapore Paper in this product is recyclable.

Foreword 1

Children are not “miniature adults.” This is a statement, true in most aspects but especially more in the field of pediatric spinal deformities. The growing spine is a unique entity and completely different to the matured spine, and the treating surgeon should have a thorough understanding of the various different etiopathologies, possible associated anomalies and alterations in other organs, influence of growth on the deformity and vice versa, and special challenges associated with the implant fixation of the immature skeleton. Frequently, these patients also require staged interventions, and the surgeon needs to counsel the parents accordingly. The worry and anxiety of the patients only add to the complexity of the situation. I should congratulate the editors of this book for planning the chapters in a way that it provides a comprehensive cover of the entire spectrum of the principles and practice of pediatric spinal deformity. On browsing through the various chapters, I am happy to note the extensive coverage of topics by surgeons who have extensive experience in this field. The authors have brought the current literature mixed with their personal experience, making each chapter very interesting and useful. I am sure that this book will find a valued place in the library of training and trained surgeons alike. Department of Orthopaedics Ganga Hospital, Coimbatore, India

S. Rajasekaran

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Foreword 2

Dr. Balaji Zacharia, by a commendable effort, has ventured to compile a textbook on the subject of pediatric scoliosis. So far, there are chapters included in standard textbooks on the subject. And you will agree with me that the information may have become out of date and may not contain adequate material on recent advances, which are essential for both postgraduates and practitioners. At the beginning of every chapter, there is a comprehensive description of the content and message. Dr. Balaji studied with me. Please note that I have not used the term “under me.” To him, learning was not just collecting information or tapping into other people’s experiences. He would question and search for evidence at each step of the way. He, I believe, broke the tradition that the teacher can be followed blindly. His presence with me was educative for me also. I still feel enthusiastic about interacting with him after all these years. As knowledge increases by leaps and bounds, this book will certainly be an asset for practicing spine surgeons and postgraduates in orthopedics and neurosurgery. I appreciate the endeavor, and I wish all success to the chief editor’s efforts.

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I must also mention with great appreciation Dr. Dilip Chand Raja and Dr. Nikhil KV, two young dedicated enterprising and trained practicing spine surgeons who are associate editors. Department of Orthopedics Government Medical College, Kozhikode, Kerala, India

George Itty

Preface

Management of spinal deformities has evolved steadily over the decades. There has been a tremendous improvement in the understanding of various etiologies of pediatric spinal deformities and how they behave over time and respond to different modalities of conservative or surgical treatment. Technological advances in the form of robust spinal instrumentation, computer navigation, and robotic spine surgery have improved patient satisfaction and surgical outcomes. Surgical techniques and procedures have also undergone a paradigm shift in the past two decades. Most of the recent literature focuses on achieving better deformity correction and minimizing complications of surgical interventions. This book on pediatric spinal deformities focuses on the basic understanding of the pathomechanisms of scoliosis and various classification systems, principles, and modalities of conservative and surgical treatment. This unique book dedicated to pediatric spine deformities has four parts. The first part addresses adolescent idiopathic scoliosis, which is the most common cause of pediatric spinal deformity, its classification, therapeutic strategies, and surgical remedies, and has 16 chapters. The second part, with 11 chapters, deals extensively with early-onset scoliosis, where international experts and renowned Indian spine surgeons discuss the classification system, natural history based on a broad spectrum of pathologies, latest management techniques, novel nonfusion strategies, and evidence-based optimal strategies for efficient management of these complex deformities. The third part, with 12 chapters, focuses on specific pathologies, such as neurofibromatosis, neuromuscular scoliosis, intraspinal anomalies, and rare causes of pediatric deformities. In addition, interesting chapters on the role of traction, navigation, and robotics have also been included. The final part of eight chapters addresses anesthetic considerations, neuromonitoring, psychological issues, patient outcomes, development of the spinal column and lung, and complications in the management of pediatric spinal deformities. The book has contributions from many senior members of the Association of Spine Surgeons of India and internationally renowned authors who have contributed significantly to their field of interest, and I thank all authors for having contributed to this book. This book would not have been possible without the herculean efforts ix

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of my associate editors Dr. Dilip Chand Raja and Dr. Nikhil KV, who have gone through the chapters meticulously. I sincerely thank them for the time and dedicated effort they have put into this book. A special thanks to Prof. Dr. K. Venugopal Menon, who has been my mentor and guide and has worked very hard along with me in finalizing the list of chapters along with the final list of contributing authors. All the chapters have a separate highlights section to bring the keynote messages out of each chapter. I am sure that this book, with 47 chapters dedicated to pediatric spinal deformities, will comprehensively cover all that is required for diagnosis, classification, and stratifying management and will serve as an up-to-date reference resource for orthopedic surgeons, neurosurgeons, spine fellows, and spine consultants. I once again thank all who were involved in this book. Kozhikode, Kerala, India

Balaji Zacharia

Acknowledgments

We would like to express our deep and sincere gratitude to Dr. K. Venugopal Menon, MS, MCh, MSc, Chairman, Head of the Department and Clinical Professor of Orthopaedics, Bharati Vidyapeeth Deemed University, Pune, India, for the guidance and help given to us in this arduous journey, from selecting topics to suggesting and pursuing many eminent authors in contributing to our book. It always seems to be an impossible task, and we would not have completed it without his encouragement and instructions. “Sometimes, all you need is a push to change your life in a big way,” and we would like to say this about meeting Dr. K. Venugopal Menon as a delegate during the scoliosis week. A week’s training changed our perspective on not only managing scoliosis but also how we should change our lives to be better people, surgeons, and students. His support and inspiration have led us to undertake this humble venture to publish a book that we wish to help spine surgeons with their practice in managing scoliosis. He has taught us never to stop learning because life never stops teaching, and we have tried to follow his path, be it in changing our surgical practice or personal life. We decided to evolve from the comfort zone and undertake purposeful tasks,

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following his path which showed us that a man can never discover new oceans unless he dares to lose sight of the shore. We should say that when we needed a teacher and mentor, the right person showed up, which has changed our life into what we are now. As he said, we tried to become gentlemen surgeons. Words can never express our gratitude for the support, encouragement, and kindness he showed us. We thank him for being a wonderful teacher and mentor.

Contents

Part I Adolescent Idiopathic Scoliosis Adolescent Idiopathic Scoliosis����������������������������������������������������������������������    3 Balaji Zacharia  Natural History of Idiopathic Scoliosis����������������������������������������������������������   15 A. Shiju Majeed  Preoperative Evaluation and Imaging in AIS������������������������������������������������   31 Bhavuk Garg and Aayush Aryal  Classification of Adolescent Idiopathic Scoliosis������������������������������������������   55 Nishat Ahmed, Karthik Ramachandran, and Ajoy Prasad Shetty Adolescent Idiopathic Scoliosis: The Classification Systems Pearls and Pitfalls������������������������������������������������������������������������������   73 Provash Chandra Saha  Lenke Classification of Scoliosis and Its Application������������������������������������   95 Kshitij Chaudhary and Pratik Patel  Orthotic Management in Adolescent Idiopathic Scoliosis (AIS) ����������������  115 Jayashree Nair and K. Venugopal Menon  Posterior Approach to Scoliosis Surgery��������������������������������������������������������  139 Jim F. Vellara and Harshal Bamb Posterior Scoliosis Correction Indications, Planning, and Operative Techniques ������������������������������������������������������������������������������  157 Naveen Tahasildar and K. Venugopal Menon  Anterior Scoliosis Surgery: Current Role ����������������������������������������������������  175 Ramachandran Govindasamy, Vishnu Prasath CS, and Yogesh Kumar  The Story of Shoulder Balance in AIS ����������������������������������������������������������  195 K. Venugopal Menon xiii

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Rib Hump ��������������������������������������������������������������������������������������������������������  213 Youssry Elhawary, Yehia Elbromboly, and Mohamed Khattab  Top vs. Side-Loading Implants for Scoliosis Correction������������������������������  229 Máximo-Alberto Díez-Ulloa  The Role of Pedicle Screws in Scoliosis Surgery ������������������������������������������  241 Nandan Marathe, Ayush Sharma, M. K. Deepak, Rudra Prabhu, Shiv Kumar Bali, and Laura Nanna Lohkamp Long-Term Effects of Idiopathic Scoliosis with Specific Reference to Back Pain, Cardiorespiratory Sequelae, Mortality Rate, and Psychological Issues������������������������������������������������������  255 Thomas J. Kishen  Scoliosis Surgery in Oman: Achievements and Challenges ������������������������  265 Renjit Kumar Jayachandran and Khalifa Abdullah Al Ghafri Part II Early-Onset Scoliosis Early-Onset Scoliosis (EOS): Definition, Etiology, and Clinical Features ��������������������������������������������������������������������������������������  281 Sajan K. Hegde  Growing Vertebral Column and Lung Development������������������������������������  293 Ashish Shankar Naik, K. S. Sri Vijay Anand, and Ajoy Prasad Shetty  Classification (C-EOS) and Natural History ������������������������������������������������  305 Thirumurugan Arumugam, Yogin Patel, and Ajoy Prasad Shetty Congenital Scoliosis ����������������������������������������������������������������������������������������  317 Macherla Haribabu Subramaniam and Muralidharan Venkatesan Syndromic Scoliosis ����������������������������������������������������������������������������������������  337 Macherla Haribabu Subramaniam and Muralidharan Venkatesan  Casting in Early-Onset Scoliosis��������������������������������������������������������������������  351 Susan Liew and Rejith Mannambeth Principles of Management and Current Treatment Recommendations in EOS������������������������������������������������������������������������������  359 Saumyajit Basu and Kushal Gohil  Surgical Goals and Correction Techniques in EOS Management��������������  377 Vigneshwara Badikillaya, Umesh P. Kanade, and Appaji Krishnan  Growth Rods and Guided Growth Techniques in the Treatment of Early-­Onset Scoliosis ����������������������������������������������������  391 Kiran Rajappa, M. S. Rudraprasad, and Puneeth Katapadi Pai  Nonfusion Techniques in Pediatric Scoliosis��������������������������������������������������  413 Abhishek Srivastava, Anuj Gupta, Vikas Hanasoge, and Arvind Jayaswal

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Thoracic Insufficiency Syndrome������������������������������������������������������������������  433 Akshay Gadiya, Arjun Dhawale, and Abhay Nene Role of Spinal Osteotomies and Techniques in Adolescent Idiopathic Scoliosis and Early Onset Scoliosis����������������������������������������������  447 Alok Gupta, Siddharth Katkade, and Siddharth Aiyer  Complications in the Management of EOS ��������������������������������������������������  461 Vibhu Krishnan Viswanathan, Surabhi Subramanian, and Ajoy Prasad Shetty  Late Sequelae of Untreated Pediatric Scoliosis ��������������������������������������������  475 Charanjit Singh Dhillon, Vijay Kumar Loya, and T. V. Krishna Narayan Long-term Outcomes in the Surgical Management of Adolescent Idiopathic Scoliosis and Early-Onset Scoliosis����������������������  495 G. Sudhir, Nayeem Sharief, and K. Karthik Kailash Part III Neuromuscular Scoliosis  Introduction to Neuromuscular Scoliosis������������������������������������������������������  505 K. V. Nikhil, V. Vinod, and George Abraham  Scoliosis in Cerebral Palsy������������������������������������������������������������������������������  529 N. V. Ankith and Amritlal A. Mascarenhas Intraspinal Anomalies with Scoliosis��������������������������������������������������������������  543 Sachin Anil Borkar, Ravi Sharma, Priya Narwal, and Shashank S. Kale Scoliosis in Neurofibromatosis������������������������������������������������������������������������  557 Nalli Ramanathan Uvaraj and Aju Bosco Is Scoliosis Associated with Neurofibromatosis Different from AIS? The Highlights��������������������������������������������������������������  583 Balaji Zacharia  Scoliosis in Muscular Dystrophy and Spinal Muscular Atrophy����������������  595 Ranjith Unnikrishnan and Rohan Gala  Rare Causes of Scoliosis in Children: A Bird’s Eye View����������������������������  607 Balaji Zacharia  Management of Neuromuscular Scoliosis������������������������������������������������������  615 Yat-wa Wong  Spondylolisthesis Associated with Scoliosis in Adolescent Children ����������  633 Balaji Zacharia  The Role of Traction in Pediatric Spinal Deformation Correction ������������  641 Shanmuganathan Rajasekaran and Dilip Chand Raja Soundararajan

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 Role of Navigation and Robotics in AIS and EOS����������������������������������������  653 Sajan K. Hegde, Vigneshwara Badikillaya, Umesh P. Kanade, Sharan Achar T, and Harith B. Reddy  Spinal Deformity Surgery in Children and Its Complications��������������������  683 Ashok Ramakrishnan  Painful Scoliosis in Children ��������������������������������������������������������������������������  697 Balaji Zacharia and P. J. Arun Prakas  The Sagittal Plane in Pediatric Scoliosis��������������������������������������������������������  711 K. Venugopal Menon Part IV Allied Topics  Anesthetic Considerations for Scoliosis Correction��������������������������������������  731 Binu Sajid and Bindu Meleveetil  Intraoperative Neuromonitoring in Pediatric Scoliosis Surgery ����������������  743 Siby Gopinath, Abhishek Gohel, and Rutul Shah  Development and Growth of the Spine and Lungs ��������������������������������������  767 Kishore Puthezhath  Perioperative Spirometry in Scoliosis������������������������������������������������������������  777 Sunny George  Psychosocial Problems in Children with Scoliosis and Their Parents��������  789 Anoop Raveendran Nair Lalitha and Manisha Mishra  Measuring Outcomes in Pediatric Scoliosis��������������������������������������������������  801 Gurudip Das

Part I

Adolescent Idiopathic Scoliosis

Adolescent Idiopathic Scoliosis Balaji Zacharia

Highlights • Idiopathic scoliosis is a three-dimensional deformity with lateral angulation of more than 10°, hypokyphosis, and axial rotation of the spine with translation. • The exact etiology of AIS is unknown. Genetic hormonal, environmental, evolutionary, and biomechanical factors have been implicated as causes. • Cosmetic problems are the main concern for the child and parents. • Clinical evaluation is required for assessing the location, type, magnitude, and flexibility of the curve. • Screening for scoliosis is not recommended in asymptomatic children. • A standing posteroanterior, and lateral view of the spine, supine right and left bending views are the basic radiographs required. • Radiographs are essential for classification, measurement of curves, identification of major and minor curves, identification of strategic vertebrae, and planning the treatment. • Knowledge of the natural history of AIS is essential for its management. • Observation, orthosis, and operation are the modalities for the treatment of AIS.

1 Introduction Descriptions of spinal deformities are present in ancient literature. This was mentioned in Edward Smith Papyrus, who addresses the illness and injuries of workers who built pyramids. The crooked-back individuals were forbidden from offering sacrifices to the Lord (Bible). The term “Scoliosis” is usually attributed to B. Zacharia (*) Department of Orthopaedics, Government Medical College, Kozhikode, Kerala, India e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. Zacharia et al. (eds.), Paediatric Scoliosis, https://doi.org/10.1007/978-981-99-3017-3_1

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Hippocrates. However, he did not differentiate coronal and sagittal deformities as different entities. He treated such deformities by tying the person to a padded ladder and hoisting it while the patient was still on the ladder and distracting it by giving manual traction at either end. The ancient Greeks treated spinal deformities with a mixture of gymnastics, faith healing, spa, and applied psychology. Galen in the second AD advocated direct pressure and traction as well as lever pressure and traction for the treatment. There was also mention of this condition in Arabic literature. Mohammed al Gafequi of Cordoba (1265) advocated spinal fusion using fish bones. It was Ambrose Paré who described the deformity as we recognize it today in the sixteenth century. Later, the pathogenesis was postulated by Andry. Robert Chessher treated spinal deformities by first relaxing the contracted muscles with fomentation, friction, and machinery and then with splints [1]. The term scoliosis was derived from the Greek word “skolios” meaning crooked or curved. Scoliosis is defined as a lateral curvature of the spine greater than 10°. Adolescent idiopathic scoliosis is a three-dimensional deformity with lateral curvature, hypokyphosis, and vertebral rotation. As a result, there is a lateral translation of the apical vertebra. Etiologically, scoliosis can be divided into idiopathic and nonidiopathic. Approximately 85% of cases are idiopathic. Nonidiopathic cases can be due to congenital, neuromuscular, or associated syndromes. Idiopathic scoliosis is further classified by age of onset as infantile (0–3 years), juvenile (4–9 years), and adolescent (≥10 years). The prevalence of AIS is 1–3% in the general population. AIS is common in girls. For curves up to 10°, an equal incidence is seen in both boys and girls. The female to male ratio increases with increasing age. It ranges from 1.4:1 in curves of 10° to 20°. The ratio increases to 7.2:1 of curves more than 40°. The progression of curves requiring surgical treatment is common in girls. The right-sided thoracic and left-sided lumbar are the most common curve types [2].

2 Etiology The exact etiology of AIS is unknown. Genetic, hormonal, neuromuscular, and vestibular dysfunction are some of them. Tall and slender spines are more prone to lateral curvature and its progression. Schultz confirmed experimentally that buckling of the spine is directly proportional to its height. He also demonstrated that girls have a long and slender spine compared to boys. Generalized ligamentous laxity was another factor predisposing patients to AIS. The dangerous triad of joint laxity, skeletal immaturity, and asymmetrical loading of the spine was thought to be the reason for the increased prevalence of AIS among girls engaged in gymnastics (Tanchev et  al.). Attainment of menarche is associated with the cessation of the progression of scoliosis. It has been suggested that delayed puberty and delayed onset of menarche are associated with the prevalence of AIS. Low body mass index is associated with delayed menarche and a high prevalence of menarche.

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Genetic Factors There is an increased prevalence of AIS among family members. There is a higher incidence of AIS among twins, especially among monozygotic twins. There is variability in expression among family members or even among twins. There is no confirmation about the mode of transmission as sex-linked or autosomal modes [3–5]. There is a higher incidence of the Vang-like protein 1 (VANGL1) mutation among AIS children. Genetic studies have shown many genes potentially associated with AIS. Calmodulin 1 (CALM1), matrillin 1 (MATN 1), tissue inhibitor of metalloproteinase 2 (TIMP2), matrix metalloproteinase 3 (MMP3), estrogen receptor alpha (ESR1), interleukin 6 (IL6), vitamin D receptor (VDR), melatonin receptor type 1b (MTRN1B), ladybird homeobox 1 gene (LBX1), fibrillin 1 and 2 (FBN 1, FBN 2), and insulin-like growth factor 1 (IGF1) are some of them. However, there is no conclusive evidence for any of the above genes as a causative factor for AIS. Therefore, in conclusion, AIS is a condition inherited by a polygenic mode with variable penetrance. It has a multifactorial origin, including genetic and environmental factors [6–8].

Hormonal Factors Recently, leptin has been implicated in the causation of AIS. Leptin plays a role in central nervous system development. Asynchronous neuro-osseous growth is seen with low levels of leptin. This can cause tethering on the neuraxis and scoliosis. Low levels of leptin are seen in persons with low BMI. Low-fat mass, low BMI, low circulating levels of leptin, and high levels of adiponectin levels are seen in prepubertal children. This can lead to scoliosis in adolescents [7, 9, 10]. Melatonin is another hormone affecting bone growth. It decreases bone degradation and increases bone formation. It has a role in the onset of puberty. Low levels of melatonin are found in AIS compared to the normal population. Significantly low levels of melatonin are associated with progressive curves [11–13]. Calmodulin is a calcium-­ binding receptor protein. It regulates smooth muscle contraction. There is an increased level of calmodulin in platelets of AIS patients compared to normal controls. There is an asymmetrical distribution of calmodulin in the paraspinal muscles in AIS. Increased levels are seen in the convexity of the curve. Platelet calmodulin levels are correlated with the progression of AIS. There is no causative association between calmodulin and AIS.  Melatonin is an antagonist of calmodulin [4, 14]. There is an increased growth hormone and decreased levels of FSH, LH, and estradiol in children with AIS compared to normal premenarcheal girls. There are reports of elevated levels of testosterone, progesterone, alkaline phosphatase, and osteocalcin in girls with AIS [15, 16].

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Environmental Factors Environmental stresses causing instability were suggested as a cause of scoliosis. These factors could be nutrition, alcohol, smoking, viruses, drugs, medications, and toxins [17]. A high concentration of copper has been demonstrated in the hair of children with AIS. Copper is a part of lysyl oxidase. This enzyme is required for the cross-linking of collagen and elastin. Pratt and Phippen (1980) suggested that copper may be a factor in the development of scoliosis. There is also a high concentration of zinc and low levels of selenium in children with scoliosis. Implicated as a causative factor in AIS since it is found in higher concentrations in the hair of AIS children. Malnutrition is implicated as a cause of AIS. AIS patients are shown to have a significantly lower intake of vitamin D and calcium. Generalized osteopenia is seen in AIS [18–20]. A study conducted on adolescent girls could not establish a relationship between AIS and dietary habits [21].

Evolutionary Theory Bipedalism in humans has been suggested as an evolutionary cause of scoliosis. No other apes have this deformity and are thought to be due to the peculiarity of our spine. Humans have a long and mobile lumbar spine. The lumbar spine is susceptible to deviations. Subtle changes in the lumbar spine can initiate the formation of a dorsal curve. Naturally occurring scoliosis is seen only in humans [22].

Neuromuscular Factors A muscular imbalance was proposed as a probable cause of AIS. The asymmetric muscle action potential and electromyography pattern on either side of the curve were demonstrated in certain studies, but it was found to be due to improper positioning [23]. Positional and spontaneous nystagmus is common in children with AIS. It has no relationship with curve size or posture. There has been a significant association between vestibular dysfunction and AIS [24]. The asynchronous neuro-­ osseous growth due to disproportionate growth occurring between the skeletal and neural systems can be the cause of AIS. This happens due to the rapid growth of the spine during a growth spurt and the spinal cord being short. However, MRI studies showed in severe curves that the vertebral column length is longer compared to normal controls but with no detectable change in cord length [25–27]. Anterior spinal overgrowth leads to stretching of the spinal cord and cauda equina, leading to

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hypokyphosis and deformity of the thoracic spine leading to scoliosis. This type of tethering of the cord may be a cause of AIS. A scoliotic deformity is seen in patients with tethered cord syndrome, Arnold Chiari malformation, and syringomyelia. The release of tethering or decompression of the syrinx can cause a reduction in the curvature [28].

Biomechanical Factors There is a relative increase in the growth of anterior elements in AIS. The anterior elements are taller than the posterior ones. However, this ‘Relative Anterior Spinal Overgrowth’ (RASO) concept has not been proven to cause AIS [29]. HueterVolkmann’s law suggests that increased pressure on the epiphysis retards and that decreased pressure accelerates its growth. Accordingly, there is less growth in the concave side of the curve compared to the convex side. This asymmetrical loading in a vicious cycle can lead to progressive wedging of the vertebra during growth. This leads to a progression of the curve in scoliosis (Stokes et al.) [30].

3 Clinical Evaluation The aim of clinical examination of a child with scoliosis is to assess the curve pattern, its extent, flexibility, and any complications and to determine whether it is an idiopathic or secondary curve. The examination begins with taking a proper history. It is important to determine who and how they noticed the deformity. In the majority of cases, parents or friends are the ones to notice the curve. In some cases, it is detected during school screening programs. Age of onset is another important factor, although, in many patients, it may not be accurate. Next, we asked about the progression of the curve. The parents are taught how to look for the standing and sitting height during follow-up. This can give a rough idea regarding the progression of the curve. We have to enquire regarding the onset of menarche. It is important to ask about pain, breathlessness, and any neurological problems associated with scoliosis. The majority of the children are worried about the cosmesis. Rib humb is a problem for some. The asymmetry of the shoulder or pelvis is worrisome for others. Trunk shifts and abnormal flank creases can cause cosmetic problems. Some children may find it difficult to wear certain types of dresses. Painful scoliosis always makes the surgeon think of an underlying cause for the deformity. Respiratory problems and neurological deficits are rare in AIS, unlike early-onset scoliosis. We have to discuss the condition, its course, investigations, and management plan with the child and with the parents to alleviate their concerns.

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4 Head-to-Foot Examinations A general physical examination is important in all cases. We have to look for facial asymmetry, dentition, hairline, sitting and standing height, weight, and nutritional status. Some findings, such as café au lait spots, axillary and inguinal freckles, and cutaneous swellings, may provide a clue for the diagnosis of neurofibromatosis. Tall stature, generalized ligamentous laxity, and high arched palate are seen in Marfan’s syndrome. Short stature, triangular facies, multiple deformities of the limbs, and blue sclera may be associated with imperfect osteogenesis. Hypotonia, spasticity, or pseudohypertrophy of the muscles are seen in neuromuscular scoliosis. We have to get an idea regarding the intelligence of the child or any abnormal movements or posture to rule out any associated syndromes. AIS is common in girls. A right-sided dorsal curve is the most common pattern. Lumbar curves are usually toward the left. Adam’s forward bending test is used to determine the structural curves. The position of the head and neck tilt needs to be determined. The trapezius muscle on the convex side is prominent. Usually, the right shoulder is at a higher level. The presence of a higher left shoulder is an indication of a structural proximal thoracic curve. The breast on the concave side is more prominent. There is a rib humb on the convex side. The size, shape, and level of the scapula must be assessed. In scoliosis, the medial border of the scapula on the concave side is nearer the spinous process. There is a pseudo winging on the concave side. There is crowding of the ribs on the concave side. The arm chest distance is increased on the concave side of the curve. An abnormal flank crease may be seen on the concave side. The iliocostal distance on the concave side of the curve is less than that on the convex side. The paraspinal muscles on the convex side of the lumbar curve will be prominent. The level of the anterior superior iliac spine needs to be assessed to determine fixed pelvic obliquity. Finally, we have to look for limb length inequality. A neurological examination is important in all cases. We have to check for abdominal reflex in all cases because its absence may indicate subtle neurological involvement. A left thoracic curve, right lumbar curve, painful scoliosis, cafe au lait spots, and scoliosis with neurological deficits are considered red flag signs and need further evaluation to determine any underlying cause [31, 32]. The flexibility of the curve is assessed by looking for a reduction of the curve in convex side bending, push prone test, or forward bending. Chin lift can also be used for assessing flexibility but is not commonly recommended. Screening tests are used to detect scoliosis in school children. Forward bending and measurement of the rotation of the trunk using a scoliometer is a commonly used test for screening. The Haptometer, plumbline test, and Moire topography are other screening tests. The US Preventive Task Force does not recommend routine screening in asymptomatic children, as there is insufficient evidence for or against it [33]. The ScoliScore test is a DNA test used to predict the probability of progression of the curve in children with AIS. It is done using saliva. It can be done as an office procedure [34].

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5 Radiological Assessment Standing posteroanterior and lateral radiograms of the spine, including the cervical spine superiorly and the pelvis inferiorly, are taken initially. Supine right and left lateral bending films were also taken. These are the basic radiograms needed for the assessment of the curves. A Stagnara view is occasionally taken to assess the rib humb. X-rays are required to identify the structural curves and major and minor curves. It is useful for the identification of strategic vertebrae (apical vertebra, end vertebrae, neutral and stable vertebra). Radiographs are needed for measurement of the curve, its classification, assessing the skeletal maturity, assessing the progression of the curve, and planning of surgery. Other imaging modalities, such as computed tomography (CT) and magnetic resonance imaging (MRI), are also needed. CT scans are rarely needed in AIS. In congenital scoliosis and AIS cases, when we expect a small and dysplastic pedicle, we can take a CT scan. A limited scan is often advisable to reduce radiation exposure. An MRI scan is performed in all cases of atypical curves. It is useful to identify syringomyelia, craniovertebral junctional anomalies, tethered cord, and intraspinal space-occupying lesions sometimes associated with spinal deformities [34, 35]. A cardiology and pulmonology evaluation with an assessment of pulmonary functions are performed routinely as a preoperative workup.

6 Treatment Adolescent idiopathic scoliosis is a benign condition. Long-term studies are available regarding the natural history of AIS. The progression of the curve is common in premenarchal girls. Thoracic curves, double major curves, curves greater than 30° at the time of presentation, and ectomorphic body habitus are some factors associated with curve progression. Respiratory problems are rare in AIS. Pulmonary problems are seen in patients with curves greater than 80°. Respiratory failure is common when vital capacity is less than 45% and in curves more than 110°. There is a slightly increased prevalence of back pain compared to the normal population in adults with untreated AIS. Psychosocial problems are seen in approximately 19% of cases of AIS in adults. It is common in curves more than 40°. Adults with untreated AIS are less satisfied with their body images and appearance in clothes. Compared to the general population, there is no difference between their abilities to undertake activities or quality of life. Neurological involvement is very rare. The management modality depends on many factors. The age of the child, remaining years of growth, and the magnitude of the curve at the time of presentation. There is a rapid progression of the curve during the period of peak height velocity. The curve usually progresses in Risser stage zero to three; thereafter, the progression slows down. The usual modes of treatment are observation, orthosis, and surgery.

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In skeletally immature children with AIS of less than 25° can be observed. They should be followed regularly every 6 months for curve progression. The children should be followed up until maturity and a few years beyond maturity. In a skeletally mature child with a curve, less than 45° can be observed. The orthosis in AIS aims to prevent the progression of the curve. It is indicated in skeletally immature children with curves between 25° and 45°. It is effective in Risser stage zero to two. A CTLSO is given when the apical vertebra is above the D8 level and a TLSO when it is below D8. Braces are contraindicated after skeletal maturity. The indication for surgery in AIS is a correction of the cosmetic deformity. Complete correction of the deformity is not possible in all cases. Corrective surgery aims to obtain a balanced spine with solid fusion and preservation of maximum mobile segments. It prevents the progression of the curve. The surgical approaches used for the corrective surgery are anterior, posterior, or combined. Surgery is indicated when the curve magnitude is more than 40° in a skeletally immature child. It is also indicated in a progressive curve of 30° in a skeletally immature child. In a skeletally mature child, surgical correction is indicated in curves greater than 50°. Currently, the anterior approach is used rarely. The most common indication is the type V Lenke curve. It can also be used in type 1 curves. A combined approach can be used in severe and rigid deformities. The advantages of the anterior approach are fewer fusion levels, easy correction of sagittal deformities, and better fusion. An anterior approach can prevent the crankshaft phenomenon in younger children. The thoracoscopic approach can be used for anterior release. However, there is an early deterioration of pulmonary functions when an anterior approach is used [36]. With the advancement of surgical techniques and implant designs, the posterior approach is the preferred approach for scoliosis correction. Posterior osteotomies and VCR help surgeons correct even complex deformities through a posterior approach. Pedicle screws are used for posterior fixation in most cases. Hooks, wires, and cables can be used in certain situations. Maneuvers such as concave rod rotation, vertebral derotation, simultaneous double rod rotation, vertebral column rotation, rod translation, cantilever rod bending, and vertebral coplanar alignment are some of the methods used for correction. Concave side distraction and convex side compression alone are rarely used as corrective maneuvers [37]. There are nonfusion techniques that do not require fusion of the vertebrae. Tethering of the vertebral bodies is performed using staples or polyester threads. It cannot be performed in children younger than 10 years [38]. The following chapters in this section will give details of every aspect of adolescent idiopathic scoliosis.

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7 Conclusions The exact etiology of AIS is unknown. Clinical and radiological evaluations are essential for classifying and planning treatment for AIS. Knowledge of natural history and the progression of curves is essential. Advancement in implant and instrumentation techniques and posterior surgery can correct most AISs.

8 Case Illustration A 14-year-old girl with adolescent idiopathic scoliosis salient points to be noted in the clinical examination (Figs. 1 and 2). Fig. 1  Adam’s forward bending test demonstrates a structural curve and rib hump on the right side

12 Fig. 2  Clinical features of right dorsal scoliosis. (1) Left shoulder higher due to structural proximal thoracic curve. (2) Increased spinoscapular distance on the convex side. (3) Increased arm chest distance on the convex side. (4) Abnormal flank crease on the concave side. (5) Prominent paraspinal muscle on the lumbar curve

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References 1. Bettany-Saltikov J, Turnbull D, Ng SY, Webb R. Management of spinal deformities and evidence of treatment effectiveness. Open Orthop J. 2017;11(1):1521–47. 2. Konieczny MR, Senyurt H, Krauspe R.  Epidemiology of adolescent idiopathic scoliosis. J Children’s Orthop. 2013;7(1):3–9. 3. Andersen MO, Thomsen K, Kyvik KO.  Adolescent idiopathic scoliosis in twins. Spine. 2007;32(8):927–30. 4. Antón-Tay F, Martínez I, Tovar R, Benitez-King G. Modulation of the subcellular distribution of calmodulin by melatonin in MDCK cells. J Pineal Res. 1998;24(1):35–42. 5. Kesling KL, Reinker KA. Scoliosis in twins. Spine. 1997;22(17):2009–14. 6. Qin X, Xu L, Xia C, Zhu W, Sun W, Liu Z, et al. Genetic variant of GPR126 gene is functionally associated with adolescent idiopathic scoliosis in Chinese population. Spine. 2017;42(19):E1098–103. 7. Burwell RG, Clark EM, Dangerfield PH, Molton A. Adolescent idiopathic scoliosis (AIS): a multifactorial cascade concept for pathogenesis and embryonic origin. Scoliosis. 2016;11(1):8. 8. Xu L, Sheng F, Xia C, Qin X, Tang NL-S, Qiu Y, Cheng JC-Y, Zhu Z. Genetic variant of PAX1 gene is functionally associated with adolescent idiopathic scoliosis in the Chinese population. Spine. 2018;43(7):492–6.

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9. Clark EM, Taylor HJ, Harding I, Hutchinson J, Nelson I, Deanfield JE, et  al. Association between components of body composition and scoliosis: a prospective cohort study reporting differences identifiable before the onset of scoliosis. J Bone Miner Res. 2014;29(8):1729–36. 10. Burwell RG, Aujla RK, Grevitt MP, Dangerfield PH, Molton A, Randell TL, et al. Pathogenesis of adolescent idiopathic scoliosis in girls—a double neuro-osseous theory involving disharmony between two nervous systems, somatic and autonomic expressed in the spine and trunk: possible dependency on sympathetic nervous system and hormones with implications for medical therapy. Scoliosis. 2009;4(1):24. 11. Fagan AB, Kennaway DJ, Sutherland AD.  Total 24-hour melatonin secretion in adolescent idiopathic scoliosis. Spine. 1998;23(1):41–6. 12. Hilibrand AS, Blakemore LC, Loder RT, Greenfield ML, Farley FA, Hensinger RN, et  al. The role of melatonin in the pathogenesis of adolescent idiopathic scoliosis. Spine. 1996;21(10):1140–6. 13. Brzezinski A. Melatonin in humans. N Engl J Med. 1997;336(3):186–95. 14. Lowe T, Lawellin D, Smith D, Price C, Haher T, Merola A, et al. Platelet calmodulin levels in adolescent idiopathic scoliosis. Spine. 2002;27(7):768–75. 15. Skogland LB, Miller JAA. Growth related hormones in idiopathic scoliosis: an endocrine basis for accelerated growth. Acta Orthop Scand. 1980;51(1–6):779–89. 16. Kulis A, Goździalska A, Drąg J, Jaśkiewicz J, Knapik-Czajka M, Lipik E, et al. Participation of sex hormones in multifactorial pathogenesis of adolescent idiopathic scoliosis. Int Orthop (SICOT). 2015;39(6):1227–36. 17. Goldberg CJ, Dowling FE, Fogarty EE, Moore DP. Adolescent idiopathic scoliosis as developmental instability. Genetica. 1995;96(3):247–55 [cited 2022 Mar 13]. 18. Dastych M, Cienciala J, Krbec M. Changes of selenium, copper, and zinc content in hair and serum of patients with idiopathic scoliosis. J Orthop Res. 2008;26(9):1279–82. 19. Batista R, Martins DE, Hayashi LF, Lazaretti-Castro M, Puertas EB, Wajchenberg M. Association between vitamin D serum levels and adolescent idiopathic scoliosis. Scoliosis. 2014;9(S1):O45. 20. Cheung CSK, Lee WTK, Tse YK, Lee KM, Guo X, Qin L, et al. Generalized osteopenia in adolescent idiopathic scoliosis–association with abnormal pubertal growth, bone turnover, and calcium intake? Spine. 2006;31(3):330–8. 21. Asakura K, Michikawa T, Takaso M, Minami S, Soshi S, Tsuji T, Okada E, Abe K, Takahashi M, Matsumoto M.  Dietary habits had no relationship with adolescent idiopathic scoliosis: analysis utilizing quantitative data about dietary intakes. Nutrients. 2019;11(10):2327. Accessed 1 Dec 2019. 22. Lovejoy C.  The natural history of human gait and posture part 1. Spine and pelvis. Gait Posture. 2005;21(1):95–112. 23. Alexander MA, Season EH. Idiopathic scoliosis: an electromyographic study. Arch Phys Med Rehabil. 1978;59(7):314–5. 24. Sahlstrend T, Petruson B. Postural effects on nystagmus response during caloric labyrinthine stimulation in patients with adolescent idiopathic scoliosis 77. An electro-nystagmographic study. Acta Orthop Scand. 1979;50(6):771–5. 25. Porter RW. Idiopathic scoliosis. Spine. 2000;25(11):1360–6. 26. Porter RW. The pathogenesis of idiopathic scoliosis: uncoupled neuro-osseous growth? Eur Spine J. 2001;10(6):473–81. https://doi.org/10.1007/s005860100311. 27. Chu WCW, Lam WWM, Chan Y, Ng BKW, Lam T, Lee K, et al. Relative shortening and functional tethering of spinal cord in adolescent idiopathic scoliosis? Spine. 2006;31(1):E19–25. 28. Barutcuoglu M, Selcuki M, Umur A, Mete M, Gurgen S, Selcuki D. Scoliosis may be the first symptom of the tethered spinal cord. Indian J Orthop. 2016;50(1):80. 29. Brink RC, Schlösser TPC, Colo D, Vavruch L, van Stralen M, Vincken KL, et  al. Anterior spinal overgrowth is the result of the scoliotic mechanism and is located in the disc. Spine. 2017;42(11):818–22.

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30. Stokes IA.  Mechanical effects on skeletal growth. J Musculoskelet Neuronal Interact. 2002;2(3):277–80. 31. Horne JP, Flannery R, Usman S. Adolescent idiopathic scoliosis: diagnosis and management. Am Fam Physician. 2014;89(3):193–8. 32. Kelly JJ, Shah NV, Freetly TJ, Dekis JC, Hariri OK, Walker SE, et al. Treatment of adolescent idiopathic scoliosis and evaluation of the adolescent patient. Curr Orthop Pract. 2018;29:1. 33. Screening for idiopathic scoliosis in adolescents: recommendation statement: United States Preventive Services Task Force. IJPN. 2004;4(1). 34. Kim YJ, Bridwell KH, Lenke LG, Rhim S, Cheh G. An analysis of sagittal spinal alignment following long adult lumbar instrumentation and fusion to L5 or S1: can we predict ideal lumbar lordosis? Spine. 2006;31(20):2343–52. 35. Horton WC, Brown CW, Bridwell KH, Glassman SD, Suk S-I, Cha CW. Is there an optimal patient stance for obtaining a lateral 36″ radiograph? Spine. 2005;30(4):427–33 [cited 2019 Nov 30]. https://doi.org/10.1097/01.brs.0000153698.94091.f8. 36. Jada A, Mackel CE, Hwang SW, Samdani AF, Stephen JH, Bennett JT, et al. Evaluation and management of adolescent idiopathic scoliosis: a review. Neurosurg Focus. 2017;43(4):E2. 37. Theruvath AS, Rajat M, Gururaj M, et al. Correction maneuvers in scoliosis surgery: an overview. Kerala J Orthop. 2012;25:73–7. 38. Cuddihy L, Danielsson AJ, Cahill PJ, Samdani AF, Grewal H, Richmond JM, et al. Vertebral body stapling versus bracing for patients with high-risk moderate idiopathic scoliosis. Biomed Res Int. 2015;2015:1–7.

Natural History of Idiopathic Scoliosis A. Shiju Majeed

Highlights • The spine measures 20 cm on average at birth from the first dorsal vertebra to the first sacral vertebra, and this becomes 45 cm on average at skeletal maturity. • Boys have a higher preponderance for infantile idiopathic scoliosis, with a predominance of major left thoracic or thoracolumbar curves. Spontaneous resolution is expected in 80–90% of cases. Double major curves have a higher potential for progression. • Progression in infantile idiopathic scoliosis is likely if the Mehta angle (RVAD) is more than 20°. • AIS has a more benign course than early-onset scoliosis. A higher chance of progression is seen in curves more than 20° with Risser grades 2 or less. • The peak height velocity (PHV) is usually attained 1 year before menarche in girls. AIS curves greater than 30° at PHV are at a higher risk for progression. • Polymorphisms in estrogen receptor genes and melatonin receptor genes are associated with progression in AIS curves. • After skeletal maturity, the general rule is that curves >30° progress at a rate of 1°/year. The progression of the curves is also influenced by the location of the curves, with thoracic curves being more prone to progression. Degenerative changes in adulthood and osteoporosis can result in radiological progression with or without clinical significance. • Lung alveolar development reaches its peak below 5 years of age; however, the bronchial tree and chest wall grow until skeletal maturity. • When the thorax no longer allows normal breathing or a mismatch between alveolar growth and lung compliance occurs, thoracic insufficiency syndrome can occur. A. Shiju Majeed (*) Orthopedic Surgery, Government Medical College, Thiruvananthapuram, Kerala, India e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. Zacharia et al. (eds.), Paediatric Scoliosis, https://doi.org/10.1007/978-981-99-3017-3_2

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• The effect on pulmonary function is largely dependent on the age of onset of scoliosis. • Early-onset scoliosis has a higher mortality rate than adolescent idiopathic scoliosis. • A higher incidence of back pain, cardiorespiratory difficulties (depending on curve magnitude), and low self-esteem in the physical image are noted in untreated AIS in adulthood.

1 Introduction  hy Is It Important to Understand the Natural History W of Scoliosis? The natural history of disease describes 1. The progress of a disease process. 2. How does that disease behave in an individual over time in the absence of intervention? 3. The factors affecting its incidence and distribution. The natural history of the disease and its causative factors are important in disease prevention and control.

Longitudinal Growth of the Human Spine The average length of the spine from D1 to S1 measures 20 cm at birth and increases to 45 cm at skeletal maturity. Longitudinal growth of the spine is important in the development of lung alveoli and pulmonary capacity. The rates of longitudinal growth of the spine vary between different segments and different ages. The restriction to pulmonary function is more pronounced in early-onset scoliosis than in adolescent-­onset scoliosis. A ready reckoner chart of this segmental variation in growth at different ages is given below in Table 1.

Table 1  Rates of longitudinal growth of the spine at different ages (measurements taken from the upper endplate of the upper vertebra to the lower endplate of the lower vertebra) Birth (cm) T1–T12 11–12 L1–S1 7 T1 = S1 20

0–5 years (cm/year) +1.3 +0.7 +2.0

5 years (cm) 18–19 10.5 30

5–10 years (cm/year) +0.7 +0.4 +1

10 years (cm) 22 12.5 35

During puberty (cm/year) +1.1 +0.7 +1.8

At skeletal maturity (cm) 26–28 16 43–45

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According to the age at the onset of presentation, scoliotic curves can be classified into four types: Infantile: develops before 3 years of age Juvenile: 3–10 years of age Adolescent: after 10 years of age and before the onset of maturity Adult: after skeletal maturity Infantile idiopathic scoliosis (ISS) is more frequent in boys, with a predominance of major left thoracic or thoracolumbar curves. There are four types of curves in IIS according to progression or regression 1. Resolving (early resolving or late resolving) 2. Benign progressive 3. Malignant progressive 4. Dysplastic Resolving curves in IIS can be four types depending on the relation between apical vertebral rotation and Cobb angle. Type 1: Cobb angle resolves without detectable AVR at diagnosis Type 2a: Cobb angle resolves synchronously with AVR Type 2b: Cobb angle resolves without resolution of AVR, which continues to increase for 2 years Type 2c: Cobb angle resolved after AVR Thoracic or thoracolumbar curves tend to resolve compared with double major curves, which are likely to progress [1]. Four types of progressive curves are also noted in IIS [2] judged by the relation of the resolution of the Cobb angle to the resolution of apical vertebral rotation (AVR). 1. Type 1: Cobb angle and AVR progress simultaneously 2. Type 2: Cobb angle progresses while AVR shows some resolution 3. Type 3: The Cobb angle shows some resolution while the AVR continues to increase 4. Type 4: Cobb angle and AVR each show some resolution before progressing again

Prognostic Factors in Determining Progression in IIS We can expect spontaneous resolution in 80% to 90% of IIS cases [2, 3]. The majority of resolution is likely to occur by the age of three; however, some curves may linger into later childhood before complete resolution [4]. Studies have shown three important predictors of progression in infantile idiopathic scoliosis.

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The literature identifies three important parameters to assess the risk of progression in IIS. They are: 1. Rib-vertebral angle [5, 6] 2. The specific rotation angle of Perdriolle [7] 3. Vertebral counterrotation at D4 [8] Mehta et al. in their classic paper published in 1972, defined the rib-vertebral angle RVA. It is the angle formed between each side of the apical thoracic vertebra and its corresponding rib. The rib-vertebra angle difference (RVAD) is the difference between the RVA values on the convex and concave sides of a curve at any given level [5]. Phase 1: In anteroposterior X-rays, the head of the apical rib on the convex side of a curve is seen to be distinct from the upper corner of the apical vertebra. Phase 1 is an early stage of scoliosis (Fig. 1). The R-V angle is measured when the apical rib head is in Phase 1. Phase 2: In anteroposterior views, the rib shadow overlaps the upper corner of the vertebra (Fig. 2). This indicates progressive scoliosis. In a normal spine, the RVAs formed on either side of a vertebra are equal. Alternatively, a gap of 2–4 mm separates the head of the rib and the upper corner of the corresponding vertebra; in other words, the rib head is in Phase 1. 1. Measurement of the R-V angle: A line perpendicular to the middle of either the upper or lower border of the apical vertebra is drawn. This is the reference line for that vertebra. The second line is drawn from the midpoint of the head of the rib to the midpoint of the neck of the rib. The neck of the rib is just medial to the region where the neck widens into the shaft of the rib. This second line is extended medially to intersect the vertebral line to make the R-V angle (Fig. 3). The chance of progression of the curve is high if

(a) Apical RVAD greater than 20° [5]. (b) If there is a progression from phase 1 to phase 2 [5]. (c) If the apical convex RVA is greater than 27° [6]. (d) If the RVAD at D6 shows a greater difference than the rest of the thoracic levels [8]. Note: An early indication of a double curve is the downward slope of the twelfth rib on the concave side. This can create a low or even negative RVAD of the thoracic curve [6]. Recognizing this pattern can help avoid erroneous interpretations of a progressive curve as a resolving curve.

Fig. 1  Shows the rib-vertebra relationship in Phase 1

convex phase 1

concave

Natural History of Idiopathic Scoliosis

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2. Specific rotation angle of Pedrioli [7]: The sum of the two angles of rotation measured on the two vertebrae adjacent to the upper end—vertebra is the specific rotation of Pedrioli. This can be used as a prognostic indicator in IIS (Pedrioli and Vidal). 3. Vertebral counterrotation at D4 [8]: Higher degrees of upper-end vertebral counterrotation were found to influence apical vertebral rotation (Fig. 4). Fig. 2  Shows the rib-vertebra relationship in Phase 2

convex

concave phase 2

Fig. 3  Shows the construction of the rib-vertebra angle the construction of rib-vertebra angle Progressive IIS: plot of T4 counter-rotation pre-op against apical vertebral rotation at follow-up (n = 21)

Pre-op rotation at T4 (degrees)

-2

-5

-10 r = -0.54

p = 0.01

y = -1.909 -0.100x

-15 10

15 20 25 30 35 40 45 Apical vertebral rotation at follow-up (degrees)

50

Fig. 4  Shows the plot of T4 counterrotation pre-op against apical vertebral rotation at follow-up. (Figure adapted from Graves T, Burwell R, Purdue M, Webb JK, Melton A. The rib cage deformity in infantile idiopathic scoliosis—The funnel-shaped upper chest in relation to specific rotation as a prognostic factor. An evaluation of thoracic shape in progressive scoliosis and control children during growth. Surface Topography and Spinal deformity VI. 1992, page 93–109)

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2 Adolescent Idiopathic Scoliosis Studies on Prevalence The incidence is similar between boys and girls for smaller curves. However, girls have more curve progression. In an epidemiological study based on the school screening of 26,947 students by Rogallo et al., the following pattern of prevalence was observed (Table 2) [9]. The report of the result of the screening of 82,900 Greek school children aged between 9 and 14 years over 1 year showed a prevalence of 1.7% (Stuccos et al.). A total of 2.6% of the girls and 0.9% of the boys had a Cobb angle of 10° or more. They also noted a variation in prevalence with age—0.07% of the children had scoliosis by the age of 9, 0.2% by age 10, and 0.4% by age 14.5 [10]. The prevalence of AIS in Singaporean school children was found to be 0.04% by the age of 7, 0.19% by the age of 10, and 1.44% by the age of 14. The overall predicted prevalence rate for children 9–14 years of age was 0.78% (1.23% in girls and 0.33% in boys) (Wong et al.) [11].

Long-Term Complications of Untreated Scoliosis Undetected and untreated AIS can lead to many potential complications. In a 38-year follow-up study conducted by Nachemson on the outcome of 130 untreated scoliosis patients, approximately 38% were disabled due to their deformity. The mortality rate was 100% above that of the normal population. Thirty-seven percent had constant backache, and 14% had cardiopulmonary symptoms [12]. Nilsonne and Lundgren (50-year follow-up of 113 patients from Scandinavia) reported a mortality rate twice that of the general population. Half of the remaining patients were unable to work. Back pain was seen in 90%, and 30% were on disability pensions [13, 14]. The abovementioned studies also included patients with other causes of scoliosis. A significant number of cases of idiopathic scoliosis were of infantile and juvenile types. Therefore, the conclusions may not completely apply to children with Table 2  Summarizes the epidemiological data of the study by Rogallo et al. [9] Curve in degrees 6–10 11–20 21 or more On treatment

Number of girls 316 299 65 36

Number of boys 322 208 12 5

The ratio between girls and boys 1:1 1.4:1 5.4:1 7.2:1

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Natural History of Idiopathic Scoliosis

AIS. The natural history of AIS in the long term would be better analyzed from the results of studies that only include patients with AIS.  A long-term outcome of a group of 194 patients with untreated AIS with an average age of 53  years was reported by Weinstein and Ponseti [15, 16]. Out of the 194, all but 4 were normally active. Twenty-one percent had mild psychological reactions to their deformity and were unwilling to wear tight dresses or bathing suits. Backache was common but not disabling. There was no increased mortality rate compared to a matched group. Cor pulmonale caused death in one patient.

Factors That Predict Curve Progression in AIS Age at presentation, the magnitude of the curve, menarchal status, Risser sign, and skeletal maturity are some of the factors that measure the risk of progression of the curve in AIS. However, until now, an accurate mathematical predictive model has not been available. Studies performed by Brooks et  al., Soucacos et  al., Rogala et al., Lonstein and Carlson, and Tan et al. have analyzed the progression of scoliosis in school children (Table 3). The factors that were associated with progression included sex (female), initial curve magnitude, curve pattern (right thoracic), and maturity (premenarchal). However, these studies were heterogeneous in their definition of scoliosis and what constitutes progression [9, 10, 17–19]. Surprisingly, many authors have noted spontaneous curve correction rates of 20–35% [9, 10, 17]. Curves with left thoracic and thoracolumbar curves had a higher chance of regression. Lonstein and Carlson examined the risk of curve progression in AIS based on Risser grading for skeletal maturity and curve magnitude [18]. Table  4 and Fig. 5.

Table 3  Summary of major studies on scoliosis curve progression before skeletal maturity Number of children enrolled 474

Study Brooks et al. Soucacos 839 et al. Rogala et al. 603 Lonstein 727 and Carlson

Inclusion criteria (Cobb angle) >5°

Progression Definition of progress rate 7° 5%

Regression rate 22%

>10°

5°

14.7%

35%

6° or more 29° or less

5° 10° or more if curve +20° of kyphosis. The largest curve is defined as the major curve when multiple curves are present. Minor curves can also be structural. The selection of appropriate vertebral levels for fusion was the basis of Lenke classification system. Types 1 and 5 can be treated either anteriorly or posteriorly. Types 2, 3, 4, and 6 should be treated by the posterior approach only. Selective thoracic fusion is advocated in patients with lumbar modifiers A or B. This will avoid the fusion of lumbar vertebrae as much as possible. For curves with lumbar modifier C, selective thoracic fusion is not applicable.

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Fig. 2  The Lenke classification of AIS. It describes the curve type (1–6), Lumbar spine modifier (A, B, C), Thoracic sagittal modifier (−, N, +) (Retrieved from Ovadia D, Classification of Adolescent Idiopathic Scoliosis (AIS). J Child Orthop. 2013;7(1):25–8. https://doi.org/10.1007/s 11832-012-0459-2)

Adolescent Idiopathic Scoliosis: The Classification Systems Pearls and Pitfalls

a

b

79

c

Fig. 3 This figure illustrates Lenke’s lumbar modifiers. (a) Type A has the CSVL between the pedicles of the lumbar apex. (b) Type B has the CSVL touching the apical vertebral body. (c) Type C has the CSVL completely medial to the vertebral body. (Retrieved from Han Jo Kim, Marinus de Kleuver, Keith Luk, AO Surgery reference)

Advantages The following features made Lenke classification more acceptable for deformity surgeons. 1. It is a comprehensive system that includes all types of curves. 2. Two-dimensional classification emphasizing sagittal plane alignment along with coronal deformity. 3. Allowed selective fusion when appropriate by recommending arthrodesis of ­necessary curves only. 4. Interobserver and intraobserver reliability were good-to-excellent. 5. Clinically more practical and easier to understand.

Limitations Although the reliability of Lenke’s system ranged from 0.5 to 0.97, it had some limitations. There are 42 potential curve patterns. It is very complex and might not be easy for a busy orthopedic surgeon [7]. However, the curve types should be well-­ known to surgeons who treat scoliosis. However, modifiers can only be added to provide additional information. There is a greater need for a three-dimensional evaluation of the curves, especially in cases of severe deformity. The Lenke classification system does not provide a three-dimensional evaluation. This can be done with a CT scan. However, radiation exposure is a problem.

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This classification system is only validated for AIS.  It relies on supine side-­ bending films, traction films, or lateral films with patients lying over a bolster. Most surgeons obtain bending films when surgery is planned. It is also important to understand that this classification is only validated for AIS. In the case of syndromic scoliosis or congenital scoliosis, applying the system is improper. Last, there remains a subset of “rule-breaker” curves in which the treatment did not follow the surgical recommendations made by the Lenke system. However, the least common AIS curve types 3, 4, and 6 have a higher percentage of “rule-­ breakers” than before [14, 15]. A study by Clements et al. [14] showed that there had been a significant reduction in the variation of treatment strategies after the introduction of the Lenke system.

4 The Peking Union Medical College Classification System of AIS References • The spinal curvatures were divided into three main categories based on the number of apexes. • Type I for 1 apex, type II for 2, and type III for 3 apexes • There are a total of 13 subtypes. • It is simple, with less inter- and intraobserver variability, with corresponding surgical fusion guidance and planning. • Considers the flexibility of the curve for surgical planning.

In 2005, a Chinese group of authors (Qiu G, Zhang J, et al., 2005) [9] introduced this new PUMC classification system for AIS. Here, spinal curvatures were divided into three main categories according to the number of apexes. Type I for 1, type II for 2, and type III for 3 apexes. There were several subtypes for each curve type, with a total of 13 subtypes (Fig. 4). Here, characterization of the curves was performed based on 3-D deformities and the flexibility of the curvature. This system considers coronal, sagittal, and axial spinal deformities. It is useful for selecting a surgical approach and fusion level. It is understandable and memorable. Compared to King’s system, it has better interobserver reliability and intraobserver reproducibility [17]. PUMC Type I: Single Curve Subtype Ia. Thoracic curve, apex between T2 and T11–T12 disc. Subtype Ib. Thoracolumbar curve, apex at T12, T12L1 disc, and L1. Subtype Ic. Lumbar curve, apex between the L1–L2 and L4–L5 intervertebral discs.

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a

b

c

d

e

f

g

h

81

Fig. 4 (a–h) Schematic drawing and related radiograph films of PUMC classification. (a) PUMC Ia, (b) PUMC Ib, (c) PUMC Ic, (d) PUMC IIa, (e) PUMC IIb, (f) PUMC IIc, (g) PUMC IId, (h) PUMC III. The dotted line is the plumb line passing the spinous process of C7, and the black line is the center sacrum vertical line. (Adopted from Qiu G, Zhang J, Wang Y, Xu H, Zhang J, Weng X, et al. A new operative classification of idiopathic scoliosis: A Peking union medical college method. Spine (Phila Pa 1976) 2005; 30:1419–26)

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PUMC Type II: Double Curves • Subtype IIa. This subtype has double thoracic curves • Subtype IIb. For the thoracic curve plus thoracolumbar/lumbar curve, the former is at least 10° higher than the latter. It is further divided into two subtypes: IIb1 and IIb2. –– Subtype IIb1 should meet all the following four criteria: (1) no thoracolumbar/lumbar kyphosis; (2) Cobb angle of the thoracolumbar/lumbar curve of less than 45°; (3) rotation of the thoracolumbar/lumbar curve of less than 2°; and (4) flexibility of the thoracolumbar/lumbar curve of 70%. –– Subtype IIb2 does not meet any of the aforementioned four criteria. • Subtype IIc. For the thoracic curve plus thoracolumbar/lumbar curve, the curve magnitude difference is less than 10°. By comparing the curve flexibility, it is further divided into three subtypes. –– IIc1: Flexibility: The thoracic curve is more than the thoracolumbar/lumbar curve; the Cobb angle of the thoracic curve on a convex bending radiograph is 25°. –– IIc2: Flexibility: The thoracic curve is more than the thoracolumbar/lumbar curve; the Cobb angle of the thoracic curve on a convex bending radiograph is more than 25°. –– IIc3: Flexibility: The thoracic curve is less than the thoracolumbar/lumbar curve. PUMC Type III: Triple Curves Subtype IIIa. The distal curve meets the criteria of the IIb1 lumbar curve; therefore, a selective fusion of the two proximal curves is suggested without needing to fuse the distal lumbar curve because it is milder and more flexible. Subtype IIIb. All three curves should be fused because the distal lumbar curve is larger and more rigid. Decompensation will occur in the future in case of failure to fuse all the curves, According to Qiu G, Li Q et al. (2008), the average percentages of the inter- and intraobserver agreement for PUMC classification are 91.0% (kappa coefficient 0.896) and 90.2% (kappa coefficient 0.892), respectively (Table 1). For Lenke curve type classification, those were 86.5% (kappa coefficient 0.808) and 87.4% (kappa coefficient 0.826), respectively. The reliability of both the PUMC classification and Lenke curve type classification was good-to-excellent. PUMC classification is relatively simple, with less inter- and intraobserver confusion, with corresponding surgical fusion guidance and planning [17] (Table 2).

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Table 1  The interobserver analysis Observer 1–2 1–3 1–4 1–5 1–6 2–3 2–4 2–5 2–6 3–4 3–5 3–6 4–5 4–6 5–6 Mean

No. of same classification 25 26 24 24 25 24 23 24 23 25 25 26 26 25 24

Percentage of same classification (N = 29) 86 90 83 83 86 83 79 83 79 86 86 90 90 86 83 85

Kappa coefficient 0.847 0.886 0.809 0.809 0.847 0.809 0.771 0.809 0.771 0.847 0.847 0.886 0.886 0.847 0.809 0.832

Reliability of PUMC classification (Adopted from Qiu G, Zhang J, Wang Y, Xu H, Zhang J, Weng X, et al. A new operative classification of idiopathic scoliosis: A Peking union medical college method. Spine (Phila Pa 1976) 2005; 30:1419–26)

Table 2  The intraobserver analysis Observer 1 2 3 4 5 6 Mean

Percentage of the same repeated classification (N = 29) 93 86 86 93 93 93 91

Kappa coefficient 0.924 0.847 0.847 0.924 0.924 0.924 0.898

Reproducibility of PUMC classification (Adopted from Qiu G, Zhang J, Wang Y, Xu H, Zhang J, Weng X, et al. A new operative classification of idiopathic scoliosis: A Peking union medical college method. Spine (Phila Pa 1976) 2005; 30:1419–26)

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5 Three-Dimensional Classifications References • For acquiring the precise spatial orientation of the spine in three dimensions, particularly the “top-down view” (Da Vinci view), computerized image acquisition emerged as a promising tool. • Identifying the barycenter (axis of gravity) and the relationship of various curves to this axis is crucial. • Five 3D sub-groups are included in this classification system: (a) 3D-SG1, important Cobb angle, reduced kyphosis, and lordosis; (b) 3D-SG2, very important Cobb angle, reduced kyphosis and maintained lordosis; (c) 3D-SG3, important Cobb angle, maintained kyphosis and reduced lordosis; (d) 3D-SG4, medium Cobb angle, mild apical rotation, and medium PMC rotation; and (e) 3D-SG5, important Cobb angle, very low kyphosis, medium apical rotation, and high PMC rotation. • Because of the inherent complexity in interpretation, heterogeneity of works, and instrumentation methods, it became less intuitive for clinicians.

The existing classification systems are two-dimensional. There is a handicap when we use this system for newly developed technologies. Currently, surgeons can readily collect and automatically measure more data related to the third dimension of the spine with the help of new technologies. We can analyze the top view of the spine, the intervertebral rotation of each segment of the spine, differences in vertebral wedging, torsion at the maximum curvature point, and others [18]. Lonstein JE et al. highlighted that because of the multiplicity of risk factors and the developmental complexity of scoliosis, it is important to determine a tailored treatment personalized according to the characteristics of each patient [19]. Three-dimensional classification systems for patients with AIS have gained increasing attention in recent years. However, translating a complex geometrical concept into a clinically applicable paradigm is still critical and difficult; it remains an open question as well [20]. Some top-view parameters seem to represent the ideal parameter able to globally define the characteristics of different scoliosis patterns [21–23]. According to Nault et  al. (2014), moving from a 2D to a 3D classification system will facilitate the management of AIS mainly in two crucial aspects. First, it will help to perform a more precise prognosis for every single patient, and second, it will help clinicians apply more effective treatment [24]. Many French and French–Canadian surgeons have been working on it using computerized image acquisition tools to acquire the actual spatial orientation of the spine in three dimensions, particularly the “top-down view” (Da Vinci view).

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The measurements that are obtained are then related to identifying the barycenter (axis of gravity). The relationships of various curves to this axis of gravity (Barycenter) are then determined. Typically, the plane of maximum deformity and the degree of displacement from the center are measured (Fig. 5). This concept is similar to deformity correction planning by Taylor Spatial frame software (Smith + Nephew Inc., Andover, MA, USA) [25]. Although these proposed measures provided a more precise idea of the orientation and balance of the spine, trunk, pelvis, and chest wall, they failed to detail the strategy of treating a given case, for example, the selection of fusion levels, implant density, or correction maneuvers, at least according to recent knowledge. Duong, Sangole, and others [26] selected some classificatory parameters based on the following: • Planes • The plane of maximal curvature (PMC) (Fig. 6) is the plane described by the end and apex vertebrae. The SRS committee introduced a schematic representation of the scoliotic spine called the “da Vinci representation” (Fig. 6), which illustrates the orientation of the planes of maximum curvature of the segments in the transverse view. [27] • The best-fit plane (BFP) [18] (Fig. 6) is defined as the plane that minimizes the distances between the curves defined by the centroid of each vertebral body of a specified region of the spine. • Angles. • Classic Cobb angles of each curve in the bodily frontal and sagittal planes. • Cobb angles in PMC [27]. • Rotations. • Axial rotation of the apical vertebra. • Geometric torsion. Kohashi [21] and Negrini [23] used the regional (spinal) top view of the spine (Fig. 7); they described the geometrical parameters of the top view to classifying patients as follows: • Related to the area of the top view: –– The ratio of the frontal and sagittal size [21]: the scoliotic angle becomes large, and scoliotic deformity becomes flat on the sagittal surface when the ratio of the frontal size (deviation on the anterior and posterior surfaces) and the sagittal size (deviation on the lateral surface) is smaller than one. –– Phase [23]: Phase is a measure of the 3D spatial evolution of the curve; it takes into account the reciprocal relationship (localization and morphology) among spinal curves projected in the frontal and sagittal planes. • Related to the posteroanterior direction of the top view: –– Overall direction: The angle between the AP normal spinal axis and the AP pathological spinal axis.

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Fig. 5  Graphical representation of 3D clinical indices used for the evaluation of spinal deformities. (a) Computer Cobb angle in the coronal plane; (b) Kyphosis and lordosis in the sagital plane; (c) axial rotation of the apical vertebra; (d) projection of the maximal curvature plane in 3D view; (e) plane of maximal curvature in the top view. (Adopted from Kadoury S, Labelle H. Eur Spine J (2012) 21:40–49)

–– The direction of the two vectors describing the maximum curvature in the thoracic and lumbar segments [21]: the vectors from the center to the ­furthermost points of each curve from the spinal axis have a magnitude and can be balanced or not. • Related to the barycenter (center of mass) of the top view: –– Shift [23] is the displacement of the barycenter of the top view concerning the spinal normal vertical axis.

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Fig. 6  The “Plane of maximal curvature” is described by the end and apex vertebrae of each curve. The SRS committee introduced a schematic representation of the scoliotic spine called the “da Vinci representation,”, which illustrates the orientation of the planes of maximum curvature of the segments in the transverse view. (Adopted from Donzelli S, Poma S et al. State of the art of current 3-D scoliosis classifications: a systematic review from a clinical perspective, Journal of Neuro Engineering and Rehabilitation (2015) 12:91)

All authors proposed sub-groups (SGs) according to the specific methodology they followed in their studies. Some were comparable but others were not. • 3D Sub-Group 1, classified as SG5 by Duong and SG2 by Kadoury, was characterized by an important Cobb angle (42°–39°), reduced kyphosis (23°–26°), and lordosis (30°–32°). They have been defined by the authors as Class 5 (a double thoracic curve similar to a King V or Lenke Type 2 curve) and Cluster 2 (low kyphosis and normal lordosis, with high rotation of PMC) (Fig. 8a). • 3D Sub-Group 2, classified as SG1 by Duong and SG1 by Kadoury, was characterized by a very important Cobb angle (43°–53°), reduced kyphosis (25°–31°), and maintained lordosis (38°–39°). They have been defined by the authors as Class 1 (single thoracic curve pattern similar to a King Type III or a Lenke Type 1 curve, with thoracic hypokyphosis and lumbar hypolordosis in the sagittal plane; the deformity is mainly located in the frontal plane) and Cluster 1 (normal kyphosis with hyperlordosis and high Cobb angles of the main thoracic curve) (Fig. 8b). • 3D Sub-Group 3, classified as SG3 by Duong and SG4 by Kadoury, is characterized by an important Cobb angle (41°–45°), maintained kyphosis (29°–39°), and reduced lordosis (33°–33°). They have been defined by the authors as Class 3

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Frontal size

Barycentre

Sagittal size

Diagonal

Aº Y Bº

AP spinal axis

X

Fig. 7  Regional spinal top view parameters as defined by Kohashi [21] and Negrini [23]. They identified the “Ratio of the frontal and the sagittal size” of the Top Vies, the “Phase” (obtained dividing the Top View area for the diagonal of the minimum rectangle in which the Top View is inscribable), the “Direction” (angle between the AP pathological and the AP normal spinal axes), the “Direction of the thoracic and lumbar vectors” (vectors alpha and beta, describing the maximum curvature in the thoracic and lumbar segments), the “Shift” (the displacement of the barycentre of the Top View with respect to the spinal normal vertical axis. (Adopted from Donzelli S, Poma S et al. State of the art of current 3-D scoliosis classifications: a systematic review from a clinical perspective, Journal of Neuro Engineering and Rehabilitation (2015) 12:91)

(thoracic and lumbar curve patterns similar to King I or II or Lenke Type 3 curves) and Cluster 4 (hyperkyphosis with strong vertebral rotation) (Fig. 8c). • 3D Sub-Group 4, classified as SG1 by Sangole and SG1 by Stokes, is characterized by a medium Cobb angle (22°–27°), mild apical rotation (6°–5°), and medium PMC rotation (38°–57°). They have been defined by the authors as G1 (smaller, nonsurgical-minor curves) and Group 1 (both curve regions with a plane of maximum curvature rotated counterclockwise viewed from above) (Fig. 8d). • 3D Sub-Group 5, classified as SG3 by Sangole and SG3 by Kadoury (Fig. 5a–e), was characterized by an important Cobb angle (45°–41°), very low kyphosis

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a

b

c

d

Fig. 8  The graphical representations clearly show the similarities among the sub-groups identified by different authors with different methods in different populations of patients. The five 3D Sub-­ Groups that we found comparing the results of the different authors included the following: (a) 3D-SG1, important Cobb angle, reduced kyphosis and lordosis; (b) 3D-SG2, very important Cobb angle, reduced kyphosis and maintained lordosis; (c) 3D-SG3, important Cobb angle, maintained kyphosis and reduced lordosis; (d) 3D-SG4, medium Cobb angle, mild apical rotation, and medium PMC rotation; (e) 3D-SG5, important Cobb angle, very low kyphosis, medium apical rotation, and high PMC rotation. (Images were taken from the papers according to Refs. [14, 19, 20]. Adopted from Donzelli S, Poma S et al. State of the art of current 3-D scoliosis classifications: a systematic review from a clinical perspective, Journal of Neuro Engineering and Rehabilitation (2015) 12:91)

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(19°–17°), medium apical rotation (16°–11°), and high PMC rotation (45°–90°). They were defined by the authors as G3 (surgical curves with important PMC rotation and low kyphosis) and Cluster 3 (hypo-kyphosis and hyperlordosis).

Limitations In reality, these proposals of 3D classification have neither gained wide acceptance nor are they used in clinical practice. The following are the reasons: 1. Because of extreme complexity in interpretation, clinicians failed to become familiar with those schemes for use in everyday clinical practice. 2. Essentially equipment dependent. User-friendly technology with minimal radiation hazard potential is of high priority. 3. It must be shown that these classifications are valid and clinically relevant. 4. A vast change in clinicians’ attitudes is needed to adopt newer complex methods. 5. The heterogeneity of instrumental works and the 3D analysis methods and results obtained are the hindering factors for any kind of systematic comparison and true meta-analysis.

Advantages With all these new automated technologies, the ready acquisition of different parameters is achieved. They can offer clinicians the advantage of acquiring a larger amount of standardized data from long-term follow-up, with significant time savings.

6 Comparison Between Different Classification Systems of AIS (Table 3) References • The newer classification systems offer a more comprehensive radiographic evaluation of patients with adolescent idiopathic scoliosis. • They have limitations concerning interobserver and intraobserver reliability for planning operative treatment. • PUMC classification is relatively simple, with less inter- and intraobserver confusion.

3 Main 13

5 Main 0

4 Main 8

PUMC

King-Moe

Suk

EV rotation

Sagittal plane

Lumbar apex

Stable vertebral location

Easy

Easy

Easier

Poor

Ease of memorizing

Not defined

Possible

Not defined

Outliers+

Defined

Defined

Defined

Defined

Fusion Comprehen­ levels siveness defined

Defined

Defined

Defined

Defined

Correction Maneuver

Shoulder level

Defined+

Not defined

Not defined Not defined

Not defined Not assesed

Not defined Not defined

Implant placement

Not assesed

Not assesed

Not assesed

Not assesed

Trunk shift

Not assesed

Not assesed

Not assesed

Not assesed

Spinal balance

Not seen

Not seen

Not seen

Not seen

Barycentric axis

Not known

Not known

Possible

Limited

Scope for expansion

Not known

Moderate

Moderate

Moderate

Reliability

X-ray AP

X-ray AP

X-ray AP

X-ray AP + Lateral

Imaging

Spinal balance

Adopted from Menon KV. Classification systems in adolescent idiopathic scoliosis revisited: Is a three-dimensional classification needed? Indian Spine J 2020;3:143–50

6 Main 42

Lenke

Subtypes

Types

Classification

Additional features

Table 3  Comparison of different classification systems of AIS

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A recent multi-surgeon comparative study conducted by Richards et al. [28] found the King’s classification to be better than had been reported recently. The Lenke classification system for AIS was found to be less reliable than previously reported when the radiographs were premeasured. Good intraobserver and fair interobserver reliability was found for the King’s classification system. The average intraobserver percentage of agreement was 83.5% (kappa coefficient, 0.81). The interobserver percentage of agreement averaged 68.0% (kappa coefficient, 0.61). All three parameters of the overall Lenke curve classification demonstrated fair reliability. The average intraobserver percentage of agreement was 65.0% (kappa coefficient, 0.60). The interobserver percentage of agreement averaged 55.5% (kappa coefficient, 0.50). Although this new classification system has limitations concerning interobserver and intraobserver reliability, for the purpose of planning operative treatment, it offers a more comprehensive radiographic evaluation of patients with AIS than previous systems. Qui et al. [9] found that the reliability of both PUMC classification and Lenke curve type classification were categorized as good-to-excellent. PUMC classification is relatively simple, with less inter- and intraobserver confusion, with corresponding surgical fusion guidance and planning. The mismatch of curve classification had less influence on PUMC’s fusion range selection than that of Lenke’s system.

7 The Future of Classification Systems References • The content-based image retrieval (CBIR) system is gradually taking the upper hand over manual measurement for more accurate and rapid documentation of AIS images and their retrieval. • The employment of artificial intelligence and robotic technologies may infinitely enhance the potential of the available resources. • A large multicenter database of similar curves may eliminate complex classification systems by employing more patient-specific surgical planning. • Low-dose radiation, such as EOS, appears to be the method of choice for the evaluation of AIS in the future.

Older classifications focused on curve location only (Ponsetti/Friedman) [4]; King/ Moe [6] and subsequently PUMC [11] enhanced the system by adding curve flexibility (to include or exclude secondary curves in fusion). Lenke added the sagittal profile into the decision-making equation. From five basic curve types, the subtypes have increased to 42 potential curve patterns by the addition of one parameter!! Menon et  al. (2014) [29–31] described that the content-based image retrieval (CBIR) system is gradually taking the upper hand over manual measurement for

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more accurate and rapid documentation of AIS images and their retrieval as well. In the future, we may be able to identify curves based on just pictorial features and in fingerprinting or retina scanning. Machine-described e-learning, complex logicbased algorithms, and artificial intelligence are emerging to interact to revolutionize the management strategy for AIS.  In the future, as we better understand the 3-D geometry of these curves, we may want to add more measurable items (such as the degree of rotation), and by adding one term, surprisingly, the number of subtypes would be 128. The employment of artificial intelligence and robotic technologies may infinitely enhance the potential of the available resources. In the future, we may eliminate classifications to decide on curve types and for surgical planning and recall from a large multicenter database of similar curves and their surgical plan. Three-­ dimensional imaging modalities, especially with low-dose radiation, such as EOS, appear to be the method of choice for the evaluation of AIS in the future, but until they become affordable to developing countries.

References 1. Schulthess W. Die pathologie und therapie der Rückgratsverkrümmungen. In: Joachimsthal G, editor. Handbuch der orthopädischen Chirurgie, vol. 1. Jena: Fischer; 1906. p. 1905–7. 2. James JIP. Idiopathic scoliosis. The prognosis, diagnosis and operative indications are related to curve patterns and age of onset. J Bone Joint Surg. 1954;36-B:36–49. 3. Ponseti IV, Friedman B.  Prognosis in idiopathic scoliosis. J Bone Joint Surg Am. 1950;32A:381–95. 4. Harrington PR. Technical details in relation to the successful use of instrumentation in scoliosis. Orthop Clin North Am. 1972;3:49–67. 5. Goldstein LA, Waugh TR. Classification and terminology of scoliosis. Clin Orthop Relat Res. 1973;93:10–22. 6. King HA, Moe JH, Bradford DS, Winter RB. The selection of fusion levels in thoracic idiopathic scoliosis. J Bone Joint Surg Am. 1983;65:1302–13. 7. Dickson R, Harms J, editors. Modern management of spinal deformities. Stuttgart, Germany: Thieme; 2018. 8. Lenke LG, Betz RR, Harms J, Bridwell KH, Clements DH, Lowe TG, et al. Adolescent idiopathic scoliosis: a new classification to determine extent of spinal arthrodesis. J Bone Joint Surg Am. 2001;83:1169–81. 9. Qiu G, Zhang J, Wang Y, Xu H, Zhang J, Weng X, et  al. A new operative classification of idiopathic scoliosis: a Peking union medical college method. Spine (Phila Pa 1976). 2005;30:1419–26. 10. Elsebaie HB, Dannawi Z, Altaf F, Zaidan A, Al-Mukhtar M, Shaw MJ, et  al. Erratum to: clinically orientated classification incorporating shoulder balance for the surgical treatment of adolescent idiopathic scoliosis. Eur Spine J. 2016;25:969. 11. Bago J, Sanchez-Raya J, Perez-Grueso FJ, Climent JM. The trunk appearance perception scale (taps): a new tool to evaluate subjective impression of trunk deformity in patients with idiopathic scoliosis. Scoliosis. 2010;5:6. 12. Menon KV.  Classification systems in adolescent idiopathic scoliosis revisited: is a three-­ dimensional classification needed? Indian Spine J. 2020;3:143–50. 13. Ovadia D. Classification of adolescent idiopathic scoliosis (AIS). J Child Orthop. 2013;7:25–8.

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14. Clements DH, Marks M, Newton PO, Betz RR, Lenke L, Shufflebarger H, Harms Study Group. Did the Lenke classification change scoliosis treatment? Spine (Phila Pa 1976). 2011;36:1142–5. 15. Slattery C, Verma K. Classifications in brief: the Lenke classification for adolescent idiopathic scoliosis. Clin Orthop Relat Res. 2018;476:2271–6. 16. Lenke LG, Betz RR, Bridwell KH, Clements DH, Harms J, Lowe TG, Shufflebarger HL. Intraobserver and interobserver reliability of the classification of thoracic adolescent idiopathic scoliosis. J Bone Joint Surg Am. 1998;80:1097–106. 17. Qiu G, Li Q, Wang Y, Yu B, Qian J, Yu K, Lee CI, Zhang J, Shen J, Zhao Y, Weng X, Wang T, Aladin DMK, Lu WW.  Comparison of reliability between the PUMC and Lenke classification systems for classifying adolescent idiopathic scoliosis. Spine (Phila Pa 1976). 2008;33:E836–42. 18. Stokes IA.  Three-dimensional terminology of spinal deformity: a report presented to the Scoliosis Research Society by the Scoliosis Research Society Working Group on 3-D terminology of spinal deformity. Spine. 1994;19:236–48. 19. Lonstein JE, Carlson JM. The prediction of curve progression in untreated idiopathic scoliosis during growth. J Bone Joint Surg Am. 1984;66(7):1061–71. 20. Donzelli S, Poma S, et al. State of the art of current 3-D scoliosis classifications: a systematic review from a clinical perspective. J Neuro Eng Rehabil. 2015;12:91. 21. Kohashi Y, Oga M, Sugioka Y. A new method using top views of the spine to predict the progression of curves in idiopathic scoliosis during growth. Spine. 1996;2(2):212–7. 22. Poncet P, Dansereau J, Labelle H. Geometric torsion in idiopathic scoliosis: three-dimensional analysis and proposal for a new classification. Spine (Phila Pa 1976). 2001;26(20):2235–43. 23. Negrini S, Atanasio S, Fusco C, Zaina F, Negrini A. 3-DEMO classification of scoliosis: a useful understanding of the 3(rd) dimension of the deformity. Stud Health Technol Inform. 2008;135:139–53. 24. Nault ML, Mac-Thiong JM, Roy-Beaudry M, Turgeon I, Deguise J, Labelle H, et al. Three-­ dimensional spinal morphology can differentiate between progressive and nonprogressive patients with adolescent idiopathic scoliosis at the initial presentation: a prospective study. Spine (Phila Pa 1976). 2014;39(10):E601–6. 25. Dubousset J. Recorded webinar. Seattle, WA: Seattle Science Foundation; 2020. Available at: www.ssftv.org. Last accessed on 30 Apr 2020. 26. Duong L, Cheriet F, Labelle H, Cheung KMC, Abel MF, Newton PO, McCall RE, Lenke LG, Stokes IAF. Interobserver and intraobserver variability in the identification of the Lenke classification lumbar modifier in adolescent idiopathic scoliosis. J Spinal Disord Tech. 2009;22:448–55. 27. Nguyen VH, Leroux MA, Badeaux J, Zabjek K, Coillard C, Rivard CH. Classification of left thoracolumbar scoliosis according to its radiologic morphology and its postural geometry. Ann Chir. 1998;52(8):752–60. 28. Richards BS, Sucato DJ, Konigsberg DE, Ouellet JA. Comparison of reliability between the Lenke and King classification systems for adolescent idiopathic scoliosis using radiographs that were not premeasured. Spine (Phila Pa 1976). 2003;28:1148. 29. Coonrad RW, Murrell GA, Motley G, Lytle E, Hey LA. A logical coronal pattern classification of 2,000 consecutive idiopathic scoliosis cases based on the Scoliosis Research Society-­ defined apical vertebra. Spine (Phila Pa 1976). 1998;23:1380–91. 30. Menon KV, Dinesh Kumar VP, Tessamma T.  Experiments with novel content-based image retrieval software: can we eliminate classification systems in adolescent idiopathic scoliosis? Global Spine J. 2014;4:13–20. 31. Bridwell KH, Betz R, Capelli AM, Huss G, Harvey C. Sagittal plane analysis in idiopathic scoliosis patients treated with Cotrel Dubousset instrumentation. Spine (Phila Pa 1976). 1990;15:644–9.

Lenke Classification of Scoliosis and Its Application Kshitij Chaudhary and Pratik Patel

1 Introduction The most common scoliosis diagnosed in the adolescent age group (10–18 years) is adolescent idiopathic scoliosis. A diagnosis can be made only when other causes of scoliosis, such as congenital, neuromuscular, or other syndromes, are ruled out. Although it affects 2–3% of the adolescent population, the prevalence of curves above 40° that may require surgical treatment is only 0.1% [1]. Surgical treatment is usually considered in patients who have progressive curves greater than 45–50°. Understanding the pattern of AIS deformities is important to choosing the appropriate surgical treatment. This chapter discusses the most popular classification for AIS, described by Lenke et al. [2]. Apart from the surgical treatment recommendations put forth by Lenke et al. [2], the classification has become the default communication tool and a common language in which researchers, surgeons, and trainees communicate.

2 History of Classification Systems for AIS Classifications for AIS have been around for a long time. Ponseti and Friedman 1950 studied 444 patients with idiopathic scoliosis, but spinal fusion was performed in 50 patients. They described five curve types (thoracic, lumbar, thoracolumbar, and cervicothoracic and combined). However, this paper was primarily to present the prognosis of different curve patterns rather than for surgical recommendations [3]. K. Chaudhary (*) · P. Patel Spine Surgery Unit, Department of Orthopedics, PD Hinduja National Hospital and Medical Research Centre, Mumbai, India e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. Zacharia et al. (eds.), Paediatric Scoliosis, https://doi.org/10.1007/978-981-99-3017-3_6

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The first classification to present a philosophy and treatment recommendations according to curve types was King’s classification published in 1983 [4]. The selection of fusion levels for AIS was an area of controversy leading up to this paper. There were many propositions, however, most conceded that the fusion area must include all the vertebrae within the measured curve. However, a more detailed study covering different types of curve patterns, especially the double curve pattern, was lacking, and the default treatment was to fuse both curves. For 25 years, before the 1983 publication, the Twin Cities Scoliosis Center in Minneapolis followed the teachings of John Moe, who had developed treatment guidelines for treating AIS patients, especially for the combined thoracic and lumbar curve pattern and the double thoracic curve pattern. Moe and his colleagues, along with their fellow Howard King, retrospectively reviewed approximately 400 thoracic scoliosis cases treated at the Twin Cities Scoliosis Center using these guidelines over 30 years. The purpose of this project was not to propose a classification but to validate the philosophy and teachings of John Moe. However, the types of thoracic scoliosis patterns described in the paper have been the gold standard classification for AIS for nearly two decades [4]. The King’s classification has five types with recommendations for specific vertebral levels for spinal arthrodesis. The key concept that emerged from King’s classification was that some double curve patterns (or S-shaped curves where both curves cross the midline) could be treated by selective thoracic fusion. In such a curve, if the lumbar curve was more flexible and had fewer structural characteristics than the thoracic curve (Type 2), Moe advocated a selective fusion of only the thoracic curve. This was in keeping with his philosophy that a mobile curved lumbar spine is better than a stiff straight spine. Over the years, this idea has given rise to significant controversy, despite published reports of good long-term outcomes of selective thoracic fusion [5]. The King’s paper also identified for the first time two variants of the single thoracic curve pattern where the lumbar curve did not cross the midline. The first was a double thoracic curve pattern (Type 5) with the left shoulder higher and the T1 vertebra tilted into the convexity of the PT. In this case, they recommended fusion of both PT and MT curves to avoid shoulder imbalance. The second variant was a long thoracic-type pattern (Type 4) where T4 was tilted into the thoracic curve. Here, they recommended that the LIV should go down to the stable vertebra to avoid a distal add-on. As we shall see subsequently, these concepts of King-Moe classification recur in the Lenke classification and its modifications. In fact, for understanding the treatment recommendations (including the rule-breakers) made by the Lenke classification, it is imperative to understand the conceptual framework laid down by the King-Moe classification. The major problem with the King’s classification was it is fair to poor intra- and interobserver reliability, as reported by several studies performed at separate centers [6, 7]. The primary driver of its unreliability was the confusion between the Type 2 and Type 3 curves. The paper does not clearly define when the lumbar curve should be labeled as one that crosses the midline [King and Moe]. In the Lenke classification, such curves are the B modifier curves, which are labeled either Type 2 or Type 3 by the King’s classification [6]. Please note that the treatment recommendation for

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both Type 2 and Type 3 King was to fuse the thoracic curve only with the LIV being the stable vertebra. However, this labeling confusion led to the poor reliability of this classification. The King’s classification is also a one-dimensional classification without a sagittal plane assessment. It was not comprehensive, as double and triple major curves and isolated thoracolumbar/lumbar curves were not included. The recommendations of King’s classification were based on Harrington instrumentation, which by the end of the millennium had become outdated in the era of segmental spinal instrumentation. To address these limitations of King’s classification system, a new AIS classification system was proposed in 2001 [2]. The classification was developed by five members of the Scoliosis Research Society, which included the lead author of the paper, Lawrence Lenke. The goals of the classification were as follows: 1. To be comprehensive include all curve types. 2. Emphasize the importance of sagittal plane. 3. To define standardized treatment according to curve types. 4. Have good-to-excellent interobserver and intraobserver reliability. 5. Based on objective criteria to separate each curve type. 6. Be practical and easily understood in the clinical setting.

3 Basic Definitions The radiographs required for the Lenke classification are the standing frontal, lateral, and supine left and right side-bending flexibility radiographs.

Location of Curves The SRS definitions for the location of curves were used to determine the curve types. • Proximal thoracic curve (PT)—apex at T3, T4, or T5 • Main thoracic curve (MT)—apex between the T6 and T11–12 disc • Thoracolumbar curve (TL)—apex between the cephalad border of T12 and the caudad border of L1 • Lumbar curve (L)—apex between the L1–L2 disc and the caudad border of L4

Major Versus Minor Curves The largest measured curve on an upright coronal radiograph is called the “Major” curve, and by default, it is a structural curve, irrespective of its flexibility. If MT is equal to or less than 5° smaller than the TL/L curve, then MT is considered the

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major curve by default. The smaller curves are termed “Minor” (note that PT curves are always minor curves). Minor curves can be structural or nonstructural.

Structural Versus Nonstructural Minor Curves The SRS definition of a nonstructural curve is a curve that completely corrects or overcorrects on side bending. A structural curve is a curve whose Cobb measurement fails to correct past zero on supine maximal voluntary lateral side bending X-ray [8]. However, to simplify the classification, an arbitrary 25° cut-off was used in the Lenke classification. In addition, a 20° cut-off was chosen as the upper limit of kyphosis in the T2–T5 and T10–L2 regions to define the structurality of the curve. Thus, the definitions of structural minor curves as per this classification are: • Structural PT curve—on side-bending radiographs, the residual PT curve measures 25° or more (irrespective of the T1 tilt) and/or has T2–T5 kyphosis of +20° or more. • Structural MT curve—on side-bending radiographs residual MT curve measures 25° or more and/or has T10–L2 kyphosis of +20° or more. • Structural TL or L curve—on side-bending radiographs residual TL/L curve measures 25° or more and/or has T10–L2 kyphosis of +20° or more.

4 Lenke Curve Types There are six types of curves with two modifiers to each curve: the lumbar modifier and the sagittal thoracic modifier (Table 1). Type 1—Main Thoracic—The MT is the major curve, and the PT and the TL/L curve are minor nonstructural curves. Type 2—Double Thoracic—The MT is the major curve, and the PT is a minor structural curve. The TL/L curve is minor and nonstructural. It is called a double Table 1  Lenke classification system (six curve types), built on the structurality of the PT, MT, and TL/L regions Curve type 1 2 3 4 5 6

PT NS Sa NS Sa NS NS

MT Sa Sa Sa Sa NS Sa

S structural, NS nonstructural a   Major (largest curve)

TL/L NS NS Sa Sa Sa Sa

Description Main thoracic (MT) Double thoracic (DT) Double major (DM) Triple major (TM) Thoracolumbar/lumbar (TL/L) Thoracolumbar/lumbar-main thoracic (TL/L-MT)

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thoracic curve because it is a double structural curve with the apices of both structural curves in the thoracic region. Type 3—Double Major—The MT and TL/L curves are structural, while the PT is nonstructural. Although called a double major curve, this is technically a double structural curve where the MT is the major curve. If MT is equal to or within ±5° of the TL/L curve, then MT is considered the major curve by default. This is compared to Type 6, where TL/L is the major curve. Type 4—Triple Major—The PT, MT, and TL/L curves are structural. Although called a triple major curve, this is technically a triple structural curve, where either the MT or the TL/L curve can be the major curve. Type 5—Thoracolumbar/lumbar—The TL/L curve is the major curve and is structural. The PT and MT curves are nonstructural. Type 6—Thoracolumbar/lumbar-main thoracic—This is a double structural curve where the TL/L curve is the major curve and measures at least 5° more than the MT, which is also a structural curve. PT is nonstructural. This is compared with Type 3, where MT is always the major curve, whereas, in Type 6, TL/L is always the major curve. Note: If the difference between the MT and TL/L curves is less than 5° (the measurement error of radiographic Cobb measurement for AIS), then both curves are considered of equal magnitude, with MT being the major curve by default. Such curve patterns can be classified as Type 3 (if PT is nonstructural), Type 4 (if PT is structural), or Type 5 (if MT is nonstructural).

Lumbar Modifier Lumbar modifier (A, B, or C) is determined by the relationship of CSVL with the apex of the lumbar curve. It is a measure of the coronal position of the lumbar spine in relationship with the pelvis. • Modifier A: CSVL is between the lumbar pedicles up to the level of the stable vertebra. This modifier can only be used for curves with MT as the major curve. It cannot be used to define thoracolumbar major curves (Type 5 and Type 6). • Modifier B: The lumbar spine deviates from the midline. The CSVL is between the medial border of the concave pedicle and the concave lateral margin of the apical lumbar body or bodies (if the apex of the lumbar curve is a disc). Here, again, the MT is the major curve, and TL/L major curves are excluded. • Modifier C: The lumbar spine is more deviated from the midline than modifier B such that the CSVL falls entirely medial to the concave lateral aspect of the TL/L curve apical body or bodies (if the apex is the disc). Here, the curve may have a major curve with an apex at the MT or TL/L level. Type 1 to 4 curves may have a C-modifier; however, Types 5 and 6 by default are all C-modifier curves. Note—If there is doubt about whether the CSVL is clear of the lateral margin of the apex, then a B-modifier is used (Fig. 1).

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b

c

Fig. 1  Lumbar modifier based on the central sacral vertical line (CSVL)

Certain definitions have to be clarified to determine the lumbar modifier: 1. CSVL: The CSVL is a vertical line (parallel to the edge of the radiograph) drawn from the geometric center of S1 (bisecting the cephalad aspect of the sacrum). Note that the center of S1 is not defined clearly and can be interpreted in several ways, such as selecting the S1 spinous process, the midpoint of the lateral borders of the S1 facets, or the midpoint of the lateral edges of the sacral ala. This probably accounts for some variability when classifying borderline patterns, such as A versus B or B versus C [9]. This definition of CSVL does not account for small amounts of pelvic obliquity. Only if the pelvic obliquity is more than 2 cm is a shoe raise recommended during the coronal radiograph. This is different from the way the CSVL was defined in King’s paper, where the CSVL was perpendicular to the level of the pelvis.

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2. Lumbar apex: By definition, the apex of a curve is the most horizontal and laterally deviated vertebra or the disc from the CSVL. For A modifier curves, the lumbar spine does not cross the midline, and the apex is the most horizontal vertebra. When more than one vertebra is horizontal and in the midline, then the middle vertebra or the disc is considered the apex. For example, in an A-modifier curve, if there are two stacked vertebrae, then the disc is the apex, or if there are three stacked vertebrae, then the middle vertebra is the apex (Fig.  2). For B-­modifier curves (lumbar curve partially crosses the midline) and for C-­modifier curves (lumbar spine completely crosses the midline), the lumbar apex is the most horizontal and the most laterally deviated vertebra or the disc from the CSVL. 3. Stable vertebra: The stable vertebra is the most cephalad lumbar or thoracic vertebra that is most closely bisected by the CSVL.

Two Stacked Vertebrae (Apex = Disc)

Three Stacked Vertebrae (Apex = Middle Vertebra)

Four Stacked Vertebrae (Apex = Middle Disc)

Note all three are A modifier curves.

Fig. 2  Defining the lumbar apex based on CSVL (all three are A-modifier curves)

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Sagittal Thoracic Modifier • Thoracic modifier is measured between the superior endplate of T5 to the inferior endplate of T12 on the lateral standing radiograph. • Minus (−) modifier is used to identify hypokyphosis (less than +10°). • Normal (N) modifier is used to identify normal kyphosis (+10 to +40). • Plus (+) modifier is used to identify hyperkyphosis (more than +40°).

5 42 Curve Possibilities in the Lenke Classification Six curve types, three lumbar modifiers, and three sagittal modifiers should result in 54 curve types. However, all TL/L major curves (Types 5 and 6) are always completely deviated from the midline and have a C-modifier. Hence, the curve possibilities are: 1. Lumbar modifier A curves (4)—1A, 2A, 3A, 4A 2. Lumbar modifier B curves (4)—1B, 2B, 3B, 4B 3. Lumbar modifier C curves (6)—1C, 2C, 3C, 4C, 5C, 6C Each of these 14 curve types listed above can have a sagittal thoracic modifier as −, N, or +, thus creating 42 curve types.

Treatment Recommendations The general guidelines of this classification are that the major curve, which is always considered a structural curve irrespective of its flexibility, should be fused. Minor curves that are structural should be included in the fusion, and nonstructural minor curves should be left alone, as they are expected to correct spontaneously. One must bear in mind that these are not rules to be followed rigidly. The classification itself has many limitations, and more factors than just radiographic features of the curve need to be considered for decision-making.

Prevalence of Lenke Curve Types The most common patterns are 1AN (19%), 1BN (11%), 2AN (10%), 5CN (10%), and 1CN (8%), which account for approximately 60% of surgically treated AIS cases [10].

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Lumbar modifier A was the most common (41%), followed by B (37%) and C (22%). Normal kyphosis was most prevalent and found in 75% of the curves, with 14% being hypokyphotic and 11% hyperkyphotic. Sagittal plane minor structural criteria (kyphosis >20°) as the sole determinant of the surgical structural curve without the coronal plane being structural were rare.

Comparison with King’s Types (Table 2)

Reliability of the Lenke Classification The Lenke classification has been shown to have reliability ranging from 0.5 to 0.97 [11]. Most studies have shown that the Lenke classification has better intra- and intraobserver reliability than the King’s classification when premeasured radiographs are used. However, when unmeasured radiographs are analyzed, both classifications suffer from reliability because of the known variability in choosing the end vertebra. This is a real-life situation. One study has shown that on unmeasured radiographs, the King’s classification faired better than the more comprehensive Lenke classification. Intraobserver 83.5% and interobserver 68% for King versus 65% and 55% for Lenke classification, respectively. When only the curve types are compared without considering the modifiers, then the Lenke classification faired as well as the King [12]. Ogon et al. found that disagreement in the Lenke classification is commonly seen when assessing lumbar modifiers (A versus B or B versus C) and sagittal modifiers and determining whether the PT is structural [13]. The problem of borderline lumbar curves is well known even when the King’s classification is used (King 2 vs 3). However, A/B or B/C borderline cases do not make a significant clinical difference in decision-making. For A versus B, it makes no difference, as the lumbar region is not fused. For B versus C, the lumbar curve is quite small such that even if the lumbar curve on bending is defined as structural by the classification, invariably it will not be fused, and selective thoracic fusion will be performed. Hence, the classification for such borderline cases defaults the classification to the B modifier as stated above.

Table 2  Comparison of Lenke classification curve types with King’s curve pattern

Comparison with King’s types King’s classification 1 2 3 4 5

Lenke classification 6C 1C, 1B, some 3C 1A, 1B 1AR 2A, 2B

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Overall, despite these problems, the Lenke classification has improved its reliability compared to the older King’s system [11].

Limitations of the Lenke Classification 1. The Lenke classification, although quite comprehensive, can be daunting and complex for a busy orthopedic surgeon. 2. The classification does not give specific recommendations for upper instrumented vertebra (UIV) or lower instrumented vertebra (LIV) selection. At least for the LIV, for some curve patterns, the addition of another modifier (the touched vertebra) helped. 3. It does not consider many clinical parameters that are crucial for decision-­ making, such as age and maturity, clinical appearance, the relative size of thoracic and lumbar prominence on scoliometer, and clinical shoulder levels. 4. The structurality rule (cut-off 25°) for minor uses is arbitrary. Moreover, the bending X-ray correctability depends on the patient’s effort. Some surgeons use fulcrum bending X-rays, which might show more correctability. In addition, following the 25° cut-off for determining whether a minor curve should be fused or not can lead to nonselective fusions for many double major curves where selective thoracic fusion could have been possible. 5. There is no rotational assessment of the deformity. The developers of the classification tried to incorporate Nash-Moe’s grading into the Lenke classification, but the reproducibility of the classification suffered [2]. Therefore, they removed the rotational assessment from the classification. The Lenke classification thus remains a 2D classification. With the advent of EOS, we realized that two Lenke 1AN curves might differ significantly in the rotational component of the deformity. Future 3D classifications are being developed by the SRS to address this issue. 6. Not all Lenke 1 curves are the same. Out of the 611, Lenke 1 patient studies by the Harms Study Group, typical curves with apex between T7/8 and T10 were approximately 85% [14]. Fifteen percent of curves were atypical curves. Some had a proximal apex between T4 and T7 or a distal apex between T10/11 and T11/12. The curves with distal apex have characteristics similar to Lenke 5 curves and are treated with a similar strategy. Moreover, some Lenke 1A curves with a typical apex can have a long thoracic curve pattern similar to that described in King 4. The risk of the distal add-on is much higher in these curve patterns. Such atypical patterns are not uncommon and do not find a separate place in the Lenke system, making comparisons difficult. 7. Lumbar modifier, especially the B-modifier does not predict the treatment in any significant way. It is very unlikely that a B-modifier lumbar curve will ever be included in the fusion. Inclusion of the B-modifier in the Lenke classification only improves the reliability of the classification (making clear the distinction between King 2 and 3) compared to recommending a specific treatment.

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6 Additional Modifiers To address some of the limitations, some modifications have been added to the Lenke classification. 1. Last touched vertebra: To address the limitation that the Lenke classification does not recommend the LIV, Lenke et al. introduced a third modifier called the last touched vertebra. It is defined as the most distal vertebral level in the curve touched by the CSVL. Thus, the curve in Fig. 1 is classified as Lenke 1AN/L1, where L1 is the LTV.  A modification of this is the last substantially touched vertebrae (LSTV), which is the most distal vertebral level in the curve whose pedicle is touched by the CSVL (Lenke third modifier) [15]. 2. AR modifier: The Lenke 1A and 2A pattern curves have two patterns depending on the tilt of the L4 vertebra. If the L4 vertebra is tilted to the left, then a Lenke 1A curve is classified as Lenke 1A-L, which is similar to the King 3 pattern curve. However, if the L4 vertebra is tilted to the right, then the curve is classified as Lenke 1A-R, which is similar to the long thoracic pattern curve or King 4 [16].

7 Did the Lenke Classification Help Guide Treatment? Overall, most studies have shown that approximately 90% of patients follow the recommendations of the Lenke classification [2]. When the recommendations of the classifications are not followed, then the curves are called rule-breakers (e.g., Type 3CN Treated with an STF). In a review of 1310 AIS patients, the Harms Study Group found that since the introduction of the Lenke classification, there has been a reduction in the variation in treatment approaches [17]. Overall, there were 191 patients (15%) in whom the recommendations of the classification were not followed (rule-breakers). The rule-­ breakers were 18% before 2001 when the classification was introduced, which decreased to 12%. However, the percentage of rule-breakers varied with the curve types, ranging from 6% for Lenke 1 to 29% for Lenke 3. For the common curve types Lenke 1, 2, and 5, the guidelines helped reduce variability. However, for the uncommon curve types, Lenke 3, 4, and 6 (13% of total cases), the classification did not reduce the number of rule-breakers; for most of these curves, the incidence of rule-breakers was reported to have increased. In Lenke 3, 4, and 6 curve patterns, the structural nature of the minor curves is open to interpretation. This is primarily because of the arbitrary definition of a structural minor curve (bending to 1.2). (b) The apex MT curve is 20% more translated from the midline compared to the apex of the TL/L curve (apical vertebral translation AVT >1.2). (c) The rotation of the apex of the MT is more than the rotation of the apex of the TL/L curve (apical vertebral rotation >1). (d) There is no thoracolumbar kyphosis (18 h) is associated with a much lower surgical rate than wearing the brace part time (100 >120

Possible clinical manifestations Normal Causes an increase in pulmonary artery pressure Surgical intervention should be considered Probable significant decrease in lung volume Dyspnea on exertion Probable alveolar hypoventilation Chronic respiratory failure

children with EOS [18]. Adequate volume of the lung and appropriate movement of both the thorax and diaphragm are essential for proper lung function.

11 Pulmonary Function Tests Pulmonary reserve in a child with early-onset scoliosis can be assessed by the methods described below:

Single Breath Count Test The normal value ranges from 40 to 50. A count less than 15 indicates low vital capacity and respiratory muscle weakness. Overactivity of accessory muscles of respiration is a good clinical indicator of respiratory insufficiency in a child with early-onset scoliosis.

Six-Minute Walk Test In patients with moderate-to-severe pulmonary illness, the 6-minute walk test (6MWT) is a low-tech method of evaluating functional exercise capacity. The distance covered in meters is recorded as the major outcome measure when a child is asked to walk as far as they can along a 30-meter corridor with low traffic for 6 min [21].

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Spirometry The most commonly used PFT, which is sensitive to all pathophysiological processes of EOS, is vital capacity, which is used to evaluate and monitor the effects of the chest wall and restrictive lung disease. Spirometry is a cost-effective, noninvasive, readily available pulmonary function test that measures forced vital capacity (FVC). Since spirometry also measures airflow, it can diagnose airway obstruction in approximately 33% of children with EOS [22]. In these children, bronchoscopy can identify the narrowing of the mainstem bronchi caused by direct compression of the airway by the vertebra and mediastinal structures due to the deformity. To rule out mainstem bronchial compression even when FVC is decreased by a restrictive skeletal process, the ratio of FEV1 (forced expiratory volume in 1 s) divided by FVC should be more than 80% [10]. .

12 Radiographic Evaluation Determination of Lung Capacity Campbell defined Space Available for Lungs (SAL) as the ratio of the concave hemithorax height to the convex hemithorax height expressed as a percentage (Fig. 2). Worsening of SAL on sequential X-rays is suggestive of the progression of thoracic deformity, affecting lung development and thus function [23]. Fig. 2  Space available for the lung (SAL). The SAL is a ratio expressed as a percentage of the distance from the diaphragm to the apex of the lung (A/B) measured on an upright radiograph of the chest when comparing one side to the other

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The thoracic distortion index described by Gollogly et al. quantifies the thorax’s area compared to age-matched normal children. It can predict the degree of pulmonary impairment due to spinal deformities [15]. The spinal penetration index (SPI), first described by Dubousset et al., measures the amount of the thorax inhabited by the spine. Ilharreborde et al. described SPI with the help of low-dose biplanar stereo radiography and assessed the 3D volume of the thorax, which correlated with pulmonary function tests [24]. Dynamic lung MRI (dMRI): A technique to evaluate the thoracic dynamics of the respiratory cycle is dynamic lung MRI (dMRI). Independent of age or participation, dMRI is a noninvasive imaging technique used to assess lung function in children [25]. dMRI has the potential to be the “holy grail outcome tool” for EOS to evaluate pulmonary improvement following surgical correction of spine and chest wall abnormalities [26]. Normative CT scan lung volumes have also been reported. Thus, specific CT scan lung-volume investigations can be used to evaluate EOS individuals who might not be able to cooperate with regular pulmonary function testing and determine their “percent normal computed tomographic scan lung volume” [15].

Sleep Studies Recurrent hypoxemia has been reported in up to 90% of EOS patients. Patients with EOS can be diagnosed with underlying recurrent hypoxemia using overnight polysomnograms (PSGs). Following the recommendation of noninvasive positive pressure ventilation (NPPV) at night (e.g., CPAP) for more than half of these individuals, their sleep quality improved.

13 Summary The close association between the growing vertebral column and pulmonary development in the first decade is well understood. The implications of early-onset scoliosis and spinal fusion surgery on respiratory function are devastating. Hence, it is imperative to have a bearing on the choice of treatment in managing early-onset scoliosis. In light of the knowledge of the relationship between spinal growth and lung function, growth-friendly interventions are preferred in early-onset scoliosis in the first decade.

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References 1. Canavese F, Dimeglio A. Normal and abnormal spine and thoracic cage development. World J Orthop. 2013;4(4):167–74. https://doi.org/10.5312/wjo.v4.i4.167. 2. Kaplan KM, Spivak JM, Bendo JA. Embryology of the spine and associated congenital abnormalities. Spine J. 2005;5(5):564–76. 3. Dimeglio A. Growth of the spine before age 5 years. J Pediatr Orthop B. 1993;1:102–7. 4. Dimeglio A, Bonnel F. Le rachis en croissance. Paris, France: Springer Verlag; 1990. 5. Dimeglio A, Bonnel F, Canavese F. Normal growth of the spine and thorax. In: Akbarnia B, Yazici M, Thompson GH, editors. The growing spine. New York: Springer; 2009. p. 11–41. 6. Emans JB, Ciarlo M, Callahan M, Zurakowski D. Prediction of thoracic dimensions and spine length based on individual pelvic dimensions in children and adolescents: an age-independent, individualized standard for evaluation of outcome in early onset spinal deformity. Spine (Phila Pa 1976). 2005;30:2824–9. 7. Akbarnia BA, Campbell RM, Dimeglio A, Flynn JM, Redding GJ, Sponseller PD, Vitale MG, Yazici M. Fusionless procedures for the management of early-onset spine deformities in 2011: what do we know? J Child Orthop. 2011;5:159–72. 8. Charles YP, Diméglio A, Marcoul M, Bourgin JF, Marcoul A, Bozonnat MC. Influence of idiopathic scoliosis on three-dimensional thoracic growth. Spine (Phila Pa 1976). 2008;33:1209–18. 9. Dubousset J, Wicart P, Pomero V, Barois A, Estournet B. Thoracic scoliosis: exothoracic and endothoracic deformations and the spinal penetration index. Rev Chir Orthop Reparatrice Appar Mot. 2002;88:9–18. 10. Redding GJ. Early onset scoliosis: a pulmonary perspective. Spine Deform. 2014;2(6):425–9. https://doi.org/10.1016/j.jspd.2014.04.010. 11. Joshi S, Kotecha S.  Lung growth and development. Early Hum Dev. 2007;83(12):789–94. https://doi.org/10.1016/j.earlhumdev.2007.09.007. Epub 2007 Oct 1. 12. Kotecha S. Lung growth: implications for the newborn infant. Arch Dis Child Fetal Neonatal Ed. 2000;82:F69–74. 13. Ochs M, Nyengaard JR, Jung A, Knudsen L, Voigt M, Wahlers T, et al. The number of alveoli in human lung. Am J Respir Crit Care Med. 2004;169:120–4. 14. Kotecha S. Lung growth for beginners. Paediatr Respir Rev. 2000;1(4):308–13. 15. Gollogly S, Smith JT, White SK, Firth S, White K. The volume of lung parenchyma as a function of age: a review of 1050 normal CT scans of the chest with three-dimensional volumetric reconstruction of the pulmonary system. Spine (Phila Pa 1976). 2004;29:2061–6. 16. DeGroodt EG, van Pelt W, Borsboom GJ, Quanjer PH, van Zomeren BC. Growth of lung and thorax dimensions during the pubertal growth spurt. Eur Respir J. 1988;1:102–8. 17. Pehrsson K, Larsson S, Oden A, Nachemson A.  Long-term follow-up of patients with untreated scoliosis. A study of mortality, causes of death, and symptoms. Spine (Phila Pa 1976). 1992;17:1091–6. 18. Koumbourlis AC. Scoliosis and the respiratory system. Paediatr Respir Rev. 2006;7(2):152–60. https://doi.org/10.1016/j.prrv.2006.04.009. 19. Redding G, Song K, Inscore S, Effmann E, Campbell R. Lung function asymmetry in children with congenital and infantile scoliosis. Spine J. 2008;8(4):639–44. 20. Koumbourlis AC.  Chest wall abnormalities and their clinical significance in childhood. Paediatr Respir Rev. 2014;15(3):246–54, quiz 254–255. 21. Kawakami N, Matsumoto H, Saito T, Tauchi R, Ohara T, Redding G. Preoperative six minute walk performance in children with congenital scoliosis. Spine Deform. 2017;5(6):442. 22. McPhail GL, Howells SA, Boesch RP, Wood RE, Ednick M, Chini BA, Jain V, Agabegi S, Sturm P, Wall E, Crawford A, Redding G. Obstructive lung disease is common in children with syndromic and congenital scoliosis: a preliminary study. J Pediatr Orthop. 2013;33(8):781–5. https://doi.org/10.1097/BPO.0000000000000078.

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Classification (C-EOS) and Natural History Thirumurugan Arumugam, Yogin Patel, and Ajoy Prasad Shetty

1 Introduction The Scoliosis Research Society defines early onset scoliosis (EOS) as a lateral curvature of the spine that begins before the age of 10 and is less than 10°. EOS includes a myriad of conditions causing scoliosis in young children [1, 2]. The condition includes spinal deformity resulting from congenital malformations (defects in vertebral formation and segmentation), neuromuscular conditions (cerebral palsy, muscular dystrophy, etc.), bone dysplasias (fused ribs, chest wall anomalies, etc.), syndromes and idiopathic cases with no underlying disorder [2, 3]. Considering that the spine and lungs are still developing, treating scoliosis in a young child involves unique challenges. This condition differs from other types of scoliosis in terms of both treatment plans and results. Patients are more at risk for spinal deformity advancement in the first few years of life because growth might promote deformity progression. According to Dickson et al., there should be two categories of idiopathic scoliosis: early onset (0–5 years old) and lalate onset (>5 years old) [4]. Children presenting under the age of 6 years comprise the high-risk group for developing thoracic insufficiency syndrome, defined as an inability of the thorax to support normal respiration and lung growth [5]. Thoracic insufficiency syndrome, which is defined as the thorax’s inability to sustain regular breathing and lung expansion, poses a significant risk of developing in children under the age of 6 years. Restrictive pulmonary disease, pulmonary artery hypertension, and cor pulmonale development are most likely to occur in the early-onset group. Hence, this makes a compelling case for classifying these patients separately, where the emphasis is not necessarily on treating the spine deformity but also on maintaining the growth of the T. Arumugam · Y. Patel · A. P. Shetty (*) Department of Spine Surgery, Ganga Medical Centre and Hospital, Coimbatore, Tamil Nadu, India e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. Zacharia et al. (eds.), Paediatric Scoliosis, https://doi.org/10.1007/978-981-99-3017-3_19

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spine and thorax to promote increased lung volume throughout the critical first decade of life. The Scoliosis Research Society modified and changed the initial definition of the EOS criterion to encompass any scoliotic abnormalities that arise and manifest before the age of 10. The reason is that up to the age of 10 years, the management principle is similar, and most of the patients receive growth-friendly interventions as the primary treatment. The use of this universal terminology is essential for research, communication, and teaching. This chapter discusses various classifications of early-onset scoliosis, risk progression, and our understanding of the natural history of each etiology of EOS.

2 Classification Etiological Classification The classification of scoliosis based on etiology [6] is as follows: A. Idiopathic Scoliosis: Scoliosis of unknown cause. Classification based on age Infantile Idiopathic Scoliosis—Birth to 3 years Juvenile Idiopathic Scoliosis—4–9 years B. Congenital Scoliosis: Vertebral anomaly: Structural anomaly of vertebra present since birth. It can be –– Failure of formation –– Failure of segmentation –– Mixed Neuropathic: Spina bifida, Tethered Cord, Myelomeningocele, Chiari I malformation C. Neuromuscular Scoliosis: Neuropathic (cerebral palsy, spinocerebellar degeneration, etc.) Myopathic (muscle dystrophies, etc.) D. Developmental Scoliosis: Skeletal Dysplasias—Osteogenesis Imperfecta, Mucopolysaccharidoses, SED, etc. Skeletal Dysostosis—Marfan’s and Ehlers–Danlos syndrome, Neurofibromatosis, etc. Etiological classification has been widely used until recently because the natural history and progression of scoliosis depend on the etiology causing the spinal deformity (Fig. 1). This helped in establishing an appropriate surgical strategy. One of the main limitations of etiological classification is that it did not incorporate radiological parameters and the relationship between pulmonary development and spine growth. The linkage between the spine, thorax, and lung growth and function has been brought to light by Campbell et  al. They described thoracic insufficiency

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a

b

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c

Fig. 1 (a) Congenital scoliosis (b) Idiopathic scoliosis (c) Dystrophic scoliosis Neurofibromatosis- 1

syndrome as the thorax’s inability to sustain normal lung development and function [7]. Several studies have shown that new alveolar growth occurs up to the age of 7 years. Therefore, pulmonary function is permanently compromised by deformity before this age, regardless of whether the alignment is restored later in life [8]. The etiological classification also had less data to guide the choice of treatment in earlyonset scoliosis. It has been challenging to make meaningful comparisons between outcomes before and after therapy in children with EOS without a reliable classification system [9].

C-EOS Classification C-EOS was developed and later verified to enhance clinician communication, which would eventually result in better patient outcomes [10]. This is a comprehensive classification system that helps physicians make difficult treatment decisions in this very heterogeneous group of patients. The C-EOS consists of a continuous age prefix, etiology (congenital or structural, neuromuscular, syndromic, and idiopathic), major curve angle (1–4), kyphosis (−, N, or +), and an optional progression modifier (P0, P1, or P2) [11]. The etiology subgroups are listed from congenital/structural, neuromuscular, syndromic, and idiopathic in order of highest to lowest priority. When there are many diagnoses, the highest priority subgroup decides the etiology. (Table 1) 1. Major curve angle (measurement of the major spinal curve at the center of gravity) is divided into four groups:

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Table 1  C-EOS classification Age Continuous age prefix

Etiology Congenital/structural (C) Neuromuscular (M) Syndromic (S) Idiopathic (I)

Fig. 2  A case of juvenile idiopathic scoliosis, C-EOS type I2(N). (a) Cobb angle- 45° (b) Kyphosis- 26°.

a

Major curve angle 1: 90°

Kyphosis (−) 20°/year

b

90°. 2. Kyphosis (measurable maximum kyphosis between any two levels) differentiates into Hypokyphotic (50°). 3. Annual progression ratio modifier (optional): progression per year with a minimum of 6 months between observations. Curve progression has been included as an optional modifier (Fig. 2). Based on the progression of the curve during serial visits of patients with EOS, the decision can arrive at a treatment strategy to be followed (Fig. 3). This novel classification has shown promise in guiding future research and clinical decision-making in early onset scoliosis. Reproducibility of the classification of early onset scoliosis (C-EOS) has been reported in many pieces of literature now [11–13]. It has been validated as having excellent intraobserver and interobserver

Classification (C-EOS) and Natural History Fig. 3  An example of dystrophic scoliosis showing curve progression of more than 20° in a year. Annual Progression Ratio (Apr) P2 > 20°

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Cobb angle 68.4° at 9 years Cobb angle 94.5° at 10 years of age of the age

reliability [6, 13]. Cobb angle and kyphosis showed nearly complete agreement during C-EOS reliability testing, whereas etiology showed good agreement, and curve progression showed moderate agreement [14]. Recent research has demonstrated that the pace of vertical expandable prosthetic titanium rib (VEPTR) proximal anchor failure correlates with C-EOS [12]. For clinical and research purposes, C-EOS enables medical professionals to classify patients according to their etiology and radiographic characteristics. The parent-­ reported health-related quality of life outcomes of EOS appear to be significantly influenced by the underlying etiology of the condition. In comparison to congenital and idiopathic diagnoses, syndromic and neuromuscular diagnoses are associated with lower EOSQ scores before therapy. EOSQ scores are only slightly influenced by radiographic severity assessments [15].

3 Natural History and Risk Progression Early onset scoliosis has an unknown true prevalence that varies based on the etiology. Understanding the natural history of the disease is necessary to comprehend and appreciate the impact of treatment alternatives. Since EOS can have a wide range of etiologies, the diagnosis of a child who has a spinal deformity usually determines the natural history [2].

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Idiopathic Scoliosis Approximately 1% of cases of idiopathic scoliosis are infantile idiopathic scoliosis (IIS). IIS is more prevalent in men, tends to be left-sided, and occurs in the mid- to lower-thoracic spine 70–90% of the time. Idiopathic curves can increase quickly in rapidly growing infants. This is followed by a long latent period with little curve progression in the juvenile phase. Progressive curves significantly change their behavior during the adolescent growth spurt. Curves may also change patterns during growth, such as the development of a secondary lumbar curve from an initial single thoracic curve pattern. It has been known for at least three decades that untreated scoliosis that manifests before the age of 5–8  years causes respiratory failure, with a death rate that is twice that of the general population [16]. In contrast to the general population, untreated Swedish patients with infantile (0–3 years) and juvenile (4–9 years) onset were found to have a significantly higher observed mortality rate; patients with adolescent onset had the same observed mortality rate as the general population [17]. Untreated individuals with curves greater than 70° have a higher death risk than patients with fewer curves, which is related to the severity of scoliosis [17]. A reduction in vital capacity was directly correlated with growing deformity in a Scottish study of children with infantile-onset idiopathic or congenital curves, while no influence on vital capacity was observed with increasing Cobb angle in adolescents with the same deformity [18]. In general, the combination of onset before 6 years or a Cobb magnitude of 100° and in association with muscle weakness or rib anomalies can produce respiratory failure as early as the third decade [19]. Mehta was instrumental in establishing the natural history and progression of IIS [20]. Deformity progression correlates with the curve magnitude at presentation, being either ≤25 or ≥25°. Smaller curves are more likely to be nonprogressive, and they actually resolve with age. The presence of the “phase” of the rib, or overlap of the rib heads onto the vertebral bodies at the curve’s apex on an anteroposterior radiograph, is predictive in curves with Cobb angles greater than 25°. Patients who have stage 2 ribs are more likely to advance and truly need treatment. Quantifying the RVAD (rib vertebral angle difference) of Mehta in patients without rib overlap (phase 1 ribs) might assist in distinguishing between patients who are expected to worsen (RVAD >20°) and those who are unlikely to advance (Figs. 4 and 5).

Fig. 4  Technique for measuring the rib–vertebra angle difference (RVAD) as described by Mehta. The rib–vertebral angle is made from inferiorly between the apical rib neck and perpendicular to the apical vertebral inferior endplate. The rib–vertebral angle difference is computed by subtracting the concave from the convex rib–vertebral angle [20]

Classification (C-EOS) and Natural History Fig. 5  The rib phase is distinguished by rib head overlap of the vertebral body at the curve apex with phase 1 showing no overlap and phase 2 showing overlap on the anteroposterior radiograph [20]

311 Convex Phase 1

Convex

Concave

Concave Phase 2

In Europe and the United States, 8–12% of children (3–10 years old) have juvenile idiopathic scoliosis, compared to 13–16% in Europe [21, 22]. By the age of 6–7  years, the deformity is typically clinically recognized [23]. With age, the female-to-male ratio increases from 1.6:1 to 4.4:1 [24]. Compared to AIS, juvenile scoliosis is more likely to develop, respond poorly to bracing, and require surgical intervention. The most helpful feature in identifying the prognosis of individuals with juvenile idiopathic scoliosis appears to be the level of the most rotated vertebra at the peak of the original curve. By the age of 15, 80% of those who have a curve apex at T8, T9, or T10 will need spinal arthrodesis [22]. Two other factors, left-­ sided curves in boys and thoracic kyphosis of fewer than 20°, were originally believed to be associated with a poor prognosis, but their predictive value is currently unknown. Twenty percent of children with both infantile and juvenile scoliosis have central axis abnormalities, which have an impact on the course of treatment and prognosis. Restrictive lung disease is caused by rib rotation and curve progression, which limits the lungs’ capacity to develop properly. In children identified with otherwise idiopathic scoliosis before the age of 3 who are left untreated, this leads to a noticeably earlier age at death [17].

Congenital Scoliosis Congenital scoliosis affects approximately 1 in 1000 live births and is more prevalent in females. Scoliosis caused by one or more malformed vertebrae at birth is known as congenital scoliosis. They take place during 6 weeks of fetal age during embryogenesis, which is also a crucial time for the kidneys’ and the heart’s healthy development. Although the vertebral abnormality is present at birth, the deformity normally only becomes apparent as a child becomes older. Since many individuals also have concomitant heart abnormalities, their prognosis is determined by how severe the cardiac condition is as opposed to how severe their scoliosis is [2]. Natural history takes one of these courses: (1) Deformity being severe from the beginning. (2) The deformity may be stable during the early years, after which a severe progression may occur. (3) The deformity remains stable throughout the growing period [25].

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The prognosis also depends strongly on the type of anomaly and location of the anomalous vertebra (e) [26]. Patients with stable abnormalities, including congenitally fused block vertebrae, have a lower chance of curve advancement, and their natural histories are more favorable. A very high probability of advancement with growth exists in children with unstable malformations, such as hemivertebrae contralateral to fused unilateral bars [27]. There is little space for growth in the abnormal vertebrae in patients with severe multisegmented congenital spinal abnormalities. This causes the thoracic spine to shorten and reduces the amount of room for the lungs. Additionally, they have rib deformities that restrict intercostal mobility during breathing, leading to a condition known as thoracic insufficiency syndrome. Due to a unilateral failure of vertebral segmentation, congenital rib abnormalities frequently develop on congenital scoliosis concavities, although they have no adverse effects on the curve’s size or pace of growth [28]. Simple segmented lumbar and lumbosacral hemivertebrae can produce progressive trunk shift due to worsening lumbosacral take off. The natural history of these patients treated with hemivertebra resection and limited fusions is comforting. McMaster proposed that certain variables predicted curve progression in congenital scoliosis, such as [27]. –– Level of Anomaly: Junctional level vertebral anomalies have high curve progression ranging from 1°/year in block/wedge vertebra to greater than 10°/year in unilateral unsegmented bar and contralateral hemivertebrae. –– Type of Anomaly: Block and wedge vertebra have the least chance of curve progression than hemivertebra. The unilateral unsegmented bar has a high chance of progression. However, the greatest curve progression and poor prognosis are associated with unilateral unsegmented bars and contralateral hemivertebrae. –– Surgical correction is advised when curve progression is documented clinically and radiologically (Table 2).

Neuromuscular Scoliosis Spinal deformity is a well-documented effect of neuromuscular conditions. Ultimate prevalence values vary in the literature. Typically, neuromuscular scoliosis is severe and rapidly progressing. Asymmetric paraplegia-related mechanical force imbalances, congenital and intraspinal anomalies, and abnormal posture via central pathways are all factors that contribute to this spinal deformity. Significant physiologic constraints in daily living activities were caused by a spinal deformity in combination with restrictions brought on by an underlying neuromuscular disorder. With risks ranging from 80 to 100% in nonambulatory individuals, ambulatory status is inversely linked with the likelihood of developing scoliosis [29]. In patients with severe CP, progressive scoliosis has been reported to range from 64 to 74%. For DMD, this ranges from 33 to 100% in the literature, while scoliosis in patients with spinal muscular atrophy type II has been found to range from 78 to almost 100% [30–32].

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Table 2  Progression of curve in congenital scoliosis Unilateral Site of

Block

Wedge

Hemivertebra

Curvature

Vertebra

Vertebra Single

Double

Unilateral

Unsegmented unsegmented bar with Bar

contralateral hemivertebra

Upper thoracic

50% of adjacent uninvolved vertebra) Anterior vertebral scalloping Transverse process spindling (Fig. 3d) Widening of interpedicular distance Enlargement of neuroforamina Lateral vertebral scalloping (Fig. 3e) Dysplasia of the pedicle (Fig. 3f, g) Paravertebral soft tissue mass

Incidence (%) 62 51 41 36 31 31 29 25 13

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Nondystrophic Scoliosis This is the most common curve type, the natural history and curve morphology of which are similar to those of adolescent idiopathic scoliosis [3]. Features of nondystrophic scoliosis are presented in Table 1. A few non-dystrophic curves can undergo modulation to transform into dystrophic curves [2]. Dystrophic Scoliosis This subtype is characterized by the presence of typical dystrophic vertebral changes on plain radiographs, MRI, or CT scans (Table 2). The etiology of dystrophic scoliosis is multifactorial like asymmetric growth of endplates, dysregulation of bone metabolism, biomechanical instability, and mass effect on vertebrae from dural ectasia or paraspinal/intraspinal tumors [4, 5]. Dystrophic scoliosis and kyphosis progressed at an average rate of 8.1° and 11.2° per year, respectively. In the presence of anterior vertebral scalloping, the average annual rates of progression for scoliosis and kyphosis were 22.6° and 23.3°, respectively [19]. Features of dystrophic scoliosis are presented in Table 1. They are characterized by early onset and rapid progression and are challenging to treat [18, 42]. Pathognomonic to this subset of scoliosis is the presence of bony dysplastic changes (Table 2). Widening of the spinal canal and neural foramina consequent to mass effect by intraspinal tumors or an ectatic dura are typical features. Neurofibromas (intraspinal, paravertebral, or dumbbell type) can cause neural compression. Vertebral scalloping and meningocele formation can result from the erosion of the spinal osteoligamentous structures by an ectatic expanding dura [6].

5  Diagnosis and Evaluation The clinical diagnosis of NF-1 is based on the criteria defined by the National Institute of Health Consensus Development Conference [2]. All preadolescent children with neurofibromatosis should be screened for the presence of spinal deformity. A detailed clinical and radiological evaluation of the patient is mandatory, as NF-1 is a multisystemic phakomatosis, and the involvement of other organ systems must be taken into consideration before drafting a treatment plan. Patients with NF-1 often have systemic hypertension secondary to renal artery stenosis or pheochromocytoma [43]. A detailed investigation to identify the presence and cause of elevated blood pressure is an essential aspect of the preoperative workup. A meticulous radiological screening for the presence of dystrophic changes is a must, as the prognosis and management depend on whether the deformity is

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dystrophic or nondystrophic. A standing anteroposterior and lateral radiograph of the whole spine from the occiput to just below the lesser trochanter is essential to look for the presence of associated deformities in other regions of the spine (such as cervical or cervicothoracic kyphosis, thoracic lordosis, and spondylolisthesis) or pelvis. While one should look for the presence of obvious bony dysplastic changes (Table 2) in dystrophic scoliosis, meticulous scrutiny for early signs of vertebral dysplasia in nondystrophic scoliosis is of utmost importance for early identification of a curve transformation from the nondystrophic to the dystrophic side of the spectrum. Radiographic screening of the cervical spine (Fig. 1a, b) is essential to rule out cervical spine deformities or instability in NF-1 scoliotic patients who require endotracheal anesthesia, those who are planned for halo traction or those who present with torticollis or dysphagia possibly secondary to neck tumors [2]. While a true lateral view of the cervical spine is useful to screen for dystrophic changes in the vertebrae, oblique views reveal widening of the neuroforamina consequent to dumbbell lesions caused by neurofibromas exiting from the spinal canal. Dynamic lateral views of the cervical spine are useful to diagnose the presence of instability. Preoperative screening with dynamic lateral radiographs of the lumbosacral spine helps in diagnosing occult instability. Pretreatment evaluation of the spine with a CT scan, MRI, or high-volume myelography is mandatory before drafting a treatment plan. MRI or high-volume myelography is useful to assess the spinal cord and to look for the presence of neurofibromas (intraspinal, paraspinal, dumbbell lesions), dural ectasia, meningocele, and pseudomeningocele (Fig. 1c). Neurofibromas are seen in 1.5–24% of cases and may cause neural compression [44]. Paraspinal neurofibromas are associated with increased apical vertebral rotation and subluxation [11]. Dural ectasia (Fig.  3h) has been observed in up to 29% of dystrophic scoliosis patients and 11% of patients with nondystrophic scoliosis [45]. These lesions may be the cause of an existing neural compression or may compromise the neural elements during corrective surgery [3, 6]. Durrani and colleagues recommend an early MRI evaluation of all deformities showing signs of progression [40]. With early advanced imaging, modulation of a few nondystrophic deformities to dystrophic types can be identified before typical dysplastic changes are seen on plain radiographs. A preoperative CT scan with three-dimensional reconstruction (Fig. 3c) is mandatory in patients with dystrophic scoliosis. It enables the surgeon to have a three-­ dimensional orientation of the deformity and to identify dysplastic pedicles (Fig. 3f, g), thereby aiding in planning suitable anchor points for instrumentation. CT scans are the most sensitive tool to diagnose intraspinal rib dislocation/subluxation causing spinal cord compression [46].

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6 Challenges in Management The management of dystrophic scoliosis and other dystrophic spinal deformities in neurofibromatosis is one of the most challenging scenarios for a spine surgeon. The early onset and aggressive nature of these deformities make treatment challenging. Infantile, juvenile, and young adolescent patients who have dystrophic scoliosis represent challenging treatment groups [2]. A surgeon must be prepared to encounter the following factors in tandem. 1. A constantly evolving deformity with an inherent potential to undergo modulation and progress rapidly at any point in time during treatment and even after a successful spinal arthrodesis. 2. Exposure of the spine without injury to the dura and the intradural elements is challenging in the presence of dural ectasia, thinned-out laminae, and severe kyphotic deformities. In the presence of an ectatic dura, there is a high risk of CSF leakage while performing decompression or osteotomy [6]. 3. Bleeding from highly vascular neurofibromatous soft tissues and intraosseous venous sinusoids can lead to excessive intraoperative bleeding, postoperative hemorrhage, and hematoma formation [47]. Another factor contributing to excessive bleeding during surgery is the common association of systemic hypertension secondary to renal artery stenosis or pheochromocytoma [43]. Dissection to access the vertebrae/discs through an anterior approach is challenging due to excessive bleeding from the paraspinal neurofibromas and the plexiform venous channels in the soft tissues surrounding the vertebrae [3]. Bleeding from the engorged vascular sinusoids within the cancellous vertebrae is not uncommon. 4. The altered vertebral anatomy secondary to dystrophic osseous changes (thinning of the pedicles, laminae, and transverse processes) makes instrumentation challenging and ineffective (Fig. 1a). Very often, severely dysplastic or aplastic pedicles preclude the placement of pedicle screws [6]. Furthermore, instrumenting the pediatric spine is challenging due to the paucity of options for implant placement. Pedicle screw placement by the freehand technique is associated with a high rate of malpositioned screws []. 5. Coexisting osteoporosis and less bone volume often result in suboptimal implant anchorage and a high risk of instrumentation failure resulting from implant pull-­ out or cut-through after surgery [48, 49]. 6. Correction of rigid dystrophic deformities necessitates the use of high-grade osteotomies such as VCR (Vertebral Column Resection) or PSO (Pedicle Subtraction Osteotomy), which demands surgical expertise. 7. Dural tears are common during exposure, during osteotomies, and while performing corrective maneuvers. This can result in a high-volume CSF leak due to the presence of an ectatic dura housing a large volume of CSF.  Performing a primary repair of a thinned-out dura is challenging, leaving patients at risk of further complications such as CSF leak, wound healing problems, or meningitis (septic or aseptic).

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8. Up to 58% of NF-1 patients have spinal nerve sheath tumors [50]. There may be a need to resect tumors circumferentially encroaching on the spine before performing deformity correction. Plexiform neurofibromas (seen in 30% of cases) are unpredictably vascular (Fig. 10a–f) [18, 51]. Meticulous hemostasis is crucial, especially in the pediatric age group, as high-volume blood loss can lead to hemodynamic instability, coagulopathy, and physiological extremes. The need to resect intraspinal neurofibromas (foraminal, extraforaminal, and/or intradural) depends on whether they cause neural compression or pose a risk of neurological compromise during deformity correction maneuvers [50]. 9. A prevalence of pseudoarthrosis of up to 60% has been reported in the literature after posterior spinal fusion only [4, 18, 52, 53]. The low bone volume and small surface area of the fusion bed due to dysplastic vertebral elements contribute significantly to pseudoarthrosis.

7 Management of Spinal Deformities in NF-1 Nondystrophic Scoliosis The principles of management are similar to those of idiopathic scoliosis [54]. Curves of less than 20 degrees’ magnitude are kept under close observation at regular 6-month intervals, with careful monitoring for clinical/radiological signs of curve progression. For skeletally immature patients presenting with curves of magnitude 20–40°, corrective bracing is instituted [6, 17, 55]. Children with NF-1 often have cognitive impairment, intellectual disabilities, psychiatric problems, personality disorders, seizures, poor attentiveness, and social, emotional, and psychological problems. Hence, compliance with brace treatment can be challenging [56]. For patients presenting with curves of >40°, posterior segmental instrumentation, deformity correction, and fusion are recommended. For curves of >55–60°, evidence in the literature is divided between standalone posterior instrumented deformity correction and spinal fusion versus circumferential (combined anterior and posterior) spinal fusion. Traditionally, a combined approach with circumferential spinal fusion is advocated to correct the deformity, restore spinal balance, and prevent the progression of the deformity. This can be accomplished through deformity correction by anterior release and discectomy with intervertebral fusion, followed by segmental instrumentation-mediated deformity correction and fusion through a posterior approach [4, 17, 47, 57]. Circumferential arthrodesis can be performed as a staged procedure through separate anterior and posterior approaches or in a single stage through an all-posterior approach. However, studies published after the advent of third-generation spinal instrumentation have shown good short-term and mid-term outcomes with segmental instrumentation-­ mediated (standalone pedicle screws/hybrid) deformity correction and posterior

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spinal fusion through a standalone posterior approach for scoliosis of up to 90° with an associated kyphosis of up to 90° [58–60]. These patients must be kept under close observation and periodic follow-up with radiographs taken at 6-month intervals for the following reasons: 1. Curve transformation to the dystrophic subtype due to modulation of the deformity. 2. The possibility that occult or subtle dystrophic changes could have been missed on initial radiologic evaluation [6]. 3. The possibility that dystrophic changes have not yet appeared in these skeletally immature patients, with seemingly nondystrophic curves. 4. For early diagnosis of deformity progression due to pressure-induced morphological changes in the vertebrae consequent to the development of intraspinal or paraspinal neurofibromas [15, 40].

Dystrophic Scoliosis Observation of dystrophic spinal deformities is generally not recommended although some authors recommend observation of curves less than 20° (mild deformity) with serial radiographs taken at 3- to 6-month intervals to identify sudden progression and promptly institute surgical treatment [4, 6]. For curves between 20 and 40° (moderate deformity), the natural history is one of constant progression and relentless deterioration [6, 19]. Hence, observation is not justifiable. Brace treatment is not recommended, as published data report its ineffectiveness in controlling these dystrophic curves [51]. Ninety-nine percent of patients on corrective bracing experienced curve progression and ultimately required surgical treatment [19, 61]. For all moderate deformities regardless of the skeletal maturity or extent of the curve, early as well as aggressive surgical treatment is advocated due to their unfavorable natural history and the fact that these curves have a strong tendency to progress even after successful spinal fusion [3, 19]. For dystrophic scoliosis between 20 and 40°, with an associated kyphosis of up to 50°, posterior segmental instrumentation-mediated deformity correction and posterior spinal fusion of all articular facets with autografts are recommended [6, 62, 63]. There is no consensus in the literature regarding the upper limit of the magnitude of the deformity (scoliosis/kyphosis) above which a combined anterior-posterior fusion must be performed. The literature is conflicting and controversial due to the heterogeneity of existing studies concerning the patient population and the implants used. Studies published before the advent of pedicle screw fixation reported a high incidence of pseudarthrosis (60%) with posterior spinal fusion alone. When dystrophic curves with kyphosis of >50° were treated with posterior fusion alone, Sirios et al. and Winter et al. reported failure rates of 64% and 72%, respectively [18, 33]. Parisini et  al. reported a failure rate of 47–63% in dystrophic scoliosis with an

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associated kyphosis of >50° [63]. He recommended early and aggressive combined anterior-posterior fusion in such cases. Hsu LCS et al. observed that achieving successful arthrodesis was challenging in dystrophic scoliosis associated with significant kyphosis [47]. Hence, circumferential spinal fusion (anterior and posterior fusion) was recommended for scoliosis of more than 40° and kyphosis greater than 50° to prevent deformity progression and the occurrence of the crankshaft phenomenon by achieving circumferential spinal arthrodesis [6, 15, 19]. However, the conclusions drawn from these studies are based on the older techniques of instrumentation (Harrington and Luque rods, hooks, and sublaminar wires) [28, 41, 47]. These constructs had suboptimal fixation strength in the dysplastic bone and an increased tendency to pull-out. Hence, they had poor control over the deformity and difficulty in maintaining the correction, leading to a high risk of implant failure. To avoid these complications, concomitant anterior spinal fusion was recommended [6, 15, 19, 47, 63]. Even with circumferential arthrodesis, the incidence of pseudoarthrosis and loss of correction remains high (15–31%) [18]. Moreover, the combined approach is an extensive and more invasive procedure. It requires staged surgeries, longer operative times, and excessive blood loss and is associated with greater morbidity and a higher risk of complications [47, 63]. The scenario changed with the advent of pedicle screws. In comparison to the previous implants, pedicle screws can provide a stronger anchorage with a 3-column fixation and have a higher pull-out strength. Hence, pedicle screw-based constructs enable the surgeon to perform a three-dimensional correction of the deformity through better apical vertebral derotation, greater correction of deformity, and maintenance of correction for a longer duration, thereby preventing loss of correction [64]. When combined with osteotomies, the all-posterior pedicle screw technique can be used to correct rigid deformities. If the curve flexibility was 95° or apical vertebra below T8, the authors recommend a combined anterior-posterior spinal fusion [53].

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In scenarios where there is a neurological deficit due to compression of the spinal cord anteriorly or in the presence of paraspinal neurofibromas, a combined approach should be adopted as recommended by Shen et al. He also recommends a combined anterior–posterior fusion in lumbar and thoracolumbar curves [53]. In the presence of vertebral subluxation, expansion of the spinal canal, and dysplastic thin pedicles, deformity progression is inevitable despite well-performed circumferential fusion. In such scenarios, revision surgeries to increase the extent of fusion segments may be needed [41].

Key Surgical Strategies to Achieve Optimal Outcomes Taking into consideration, the aforementioned challenges in the management of dystrophic spinal deformities in NF-1, the management strategy should focus on patient optimization to mitigate intraoperative and perioperative complications and overcome perioperative morbidities. Detailed surgical planning, including alternative surgical strategies, optimal execution of the surgery, and preparedness to handle possible intraoperative complications as well as perioperative morbidity, ensures a safe postoperative period. Such a systematic approach enables the accomplishment of surgical goals while minimizing perioperative morbidities/complications, thereby ensuring optimal clinical outcomes. 1. A meticulous diagnostic workup is essential in patients with coexistent systemic hypertension to rule out renal artery stenosis or pheochromocytoma. Hypotensive anesthesia during exposure and meticulous subperiosteal dissection minimize bleeding from highly vascular neurofibromatous soft tissues. Hemostasis can be achieved with thrombin-soaked gel foam, bone wax, Surgicel, Floseal, and bipolar electrocautery. It is recommended to perform discectomies using Bovie cautery and a rongeur through the annulus rather than performing sharp dissections through the endplate apophysis, which results in excessive bleeding from the cancellous vertebral bone [2]. While planning the resection of plexiform neurofibromas, careful planning for the need and extent of resection, staging the surgeries, and the need for early blood transfusions help in avoiding complications, especially in pediatric populations with small blood volumes. 2. In the presence of thinned-out laminae, severe kyphosis, or an ectatic dura, the surgeon should perform a meticulous subperiosteal dissection using electrocautery rather than with periosteal elevators to avoid plunging into the dura inadvertently resulting in direct injury to the dura, spinal cord, or neural structures. Cottonoid patties can be used to protect the dura during exposure. It is recom-

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mended to use monopolar cautery at a lower temperature along with intermittent saline irrigation to avoid thermal injury to the dura and its contents. 3. The instruments and suture materials to repair the dura, including dural sealants (Tisseel), must be kept ready to handle an inadvertent dural tear. 4. A detailed plan of the strategic levels for pedicle screw placement and the feasibility of placing screws at those levels (dysplastic or aplastic pedicles), as well as the need for alternative strategies (hooks, sublaminar wires/tapes), helps in executing the surgery safely without complications. The surgeon must be well versed with alternate techniques of instrumentation (hooks, sublaminar wires, tapes) to tackle these complex deformities. The use of assistive technology such as navigation combined with intraoperative neuromonitoring (IONM) greatly enhances patient safety during surgery [66]. 5. The use of pedicle screw constructs or pedicle screw-based hybrid constructs wherever possible minimizes the chance of implant loosening and loss of correction [67]. 6. The incidence of pseudoarthrosis has decreased significantly with the use of segmental pedicle screw instrumentation. One of the key strategies to achieve successful fusion is to preserve as much native vertebral bone as possible and to have a reasonably adequate fusion bed. The fusion bed must be well prepared with meticulous decortication. Autologous bone grafting from the posterior superior iliac crest has been recommended to enhance bony fusion. In standalone posterior spinal fusions, the fusion should include the neutral and stable vertebrae in both planes. 7. Osteotomies aid greatly in the correction of complex deformities. The surgeon must be familiar with performing various osteotomies to correct complex deformities.

8 Outcomes of Treatment of Spinal Deformities in NF-1 Li M et al. and Li S et al. observed a significant improvement in self-image, functional outcomes, and mental health following surgical treatment of spinal deformities in NF 1 [58, 68]. Betz et al. observed that 80% of patients reported satisfactory outcomes after surgery [52]. Koptan and ElMiligui observed a significant correlation between the magnitude of kyphosis and postoperative clinical outcomes. Deformities with a larger kyphotic component (>45°) are associated with a higher loss of correction, more blood loss, prolonged duration of surgery, and a lower score on the SRS-30 questionnaire [69].

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9 Complications of Surgical Treatment of Spinal Deformities in NF-1 1. The nonneurological perioperative complication rate was 14% (0–72%) [2]. Wound infections (4.2%), dural tears (2.4%), postoperative hematoma with spinal cord compression, and pulmonary complications (direct injury, hemothorax) were the most common complications reported in the literature [16, 47]. 2. The overall incidences of temporary postoperative and residual permanent neurological deficits were 2.1% and 1.2%, respectively [61]. These neurological deficits comprised both spinal cord and nerve root injuries [16, 19, 41, 47, 69– 71]. Additionally, 58.3% of new postoperative deficits persisted at the last follow-­up. While nerve root deficits showed recovery, spinal cord injuries resulted in permanent neurological damage. Postoperative paralysis resulting from injury to the neural structures during exposure due to unexpected areas of lamina erosion caused by an underlying ectatic dura has also been reported in the literature [51]. 3. Pedicle dysplasia results in high rates of malpositioned screws, with one study reporting an incidence of 30.5% (9.9% medial and 20.6% lateral) with the freehand insertion technique [68]. Jin et  al. reported that even with navigation-­ guided pedicle screw placement, 20% of screws were malpositioned due to a lack of osseous volume [72]. 4. There was a need for revision surgeries in 21.5% of cases (range, 0–82%) [61]. Mechanical and implant-related complications, such as loosening of anchors, implant failure, proximal junctional kyphosis, and pseudarthrosis, were the most common reasons for performing revision surgeries [16, 18, 19, 47, 58–60, 68– 70, 73–82]. Case Illustration 1 - Dystrophic Thoracolumbar Kyphoscoliosis (Figs. 4a–f and 5a–f) A 16-year-old male presented with a deformity of the back and back pain that was progressively increasing over a 4-year duration. He had clinical and radiological features of dystrophic thoracic kyphoscoliosis with coronal imbalance. His neurological examination was unremarkable. Side bending films (Fig. 4e and f) demonstrated the flexibility of the curve, an important prerequisite for performing a posterior instrumented deformity correction and fusion through a posterior approach. A posterior instrumented (all pedicle screws construct) deformity correction and fusion was performed. Postoperative radiographs (Fig. 5a, b) taken at 42 months follow-up, showing a good correction of deformity with the restoration of global spinal balance in the sagittal and coronal planes. Case Illustration 2 - Early Onset Scoliosis in Neurofibromatosis (Figs. 6a–d, 7a–h, 8a, b) A 9-year-old female presented with deformity of the back and back pain that was progressively increasing over a 2-year duration. A meticulous clinicoradiological evaluation showed that she had a dystrophic thoracic scoliosis with coronal

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e

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Fig. 4 (a) Clinical photograph of the patient showing the presence of shoulder imbalance and coronal imbalance. (b) Side view in standing position shows the presence of a prominent rib hump. Anteroposterior (c) and lateral (d) radiographs of the whole spine showing an acute angular scoliosis and kyphosis, respectively, in the thoracolumbar region. Side bending films (e, f) demonstrating the flexibility of the curve

imbalance and an elevated right shoulder. Her neurological examination was unremarkable. Side bending films (Fig. 6c, d) showing thoracic curve correction from 39 to 14°. The authors planned to control the progression of the spinal deformity while facilitating the growth of the spine by using growing rods. Postoperative radiographs (Fig. 7a, b) after the application of the growing rod instrumentation in 2013 showed moderate correction of the deformity. Six distractions were performed at serial intervals to slow down the progression of the deformity until the patient was nearing the end of skeletal growth. Plain radiographs (Fig. 7c–h) taken after serial distractions from 2014 to 2019 show a slowing progression of the deformity. Finally, posterior instrumented deformity correction and fusion were performed at 15 years of age. Plain radiographs (Fig. 8a, b) were taken at 34 months after posterior instrumented deformity correction and fusion showed good correction of deformity with the restoration of global spinal balance. Case Illustration 3 - Dystrophic Thoracolumbar Kyphoscoliosis with an Associated Plexiform Neurofibroma A 15-year-old female presented with a deformity of the back and back pain that was progressively increasing over a 2-year duration. She had clinical and radiological features of dystrophic thoracolumbar kyphoscoliosis with coronal imbalance (Fig. 9a–f). Her neurological examination was unremarkable. She also had swelling (plexiform neurofibroma) in the midline of the lower back (Fig. 10a, b). Owing to its midline location and the highly vascular nature of such tumors, we planned to excise the tumor before deformity correction. With precautions to achieve hemostasis (Floseal, Gel foam) and adequate blood reserved for transfusion in the event of excessive bleeding, the tumor was meticulously dissected and removed from the underlying muscle to avoid hindrance in the exposure of the spine (Fig. 10c–f). A

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Fig. 5  Postoperative radiographs (a, b) taken at 42 months follow-up, showing a good correction of deformity with restoration of global spinal balance in the sagittal and coronal planes. Preoperative clinical photographs (c, d) showing the deformity with associated spinal imbalance. Postoperative clinical photographs (e, f) at 42 months follow-up, showing a good correction of the deformity with restoration of global spinal balance in the sagittal and coronal planes

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Fig. 6  Anteroposterior (a) and lateral (b) radiographs of the whole spine showing structural thoracic scoliosis from T6 to T11 and a compensatory lumbar scoliosis from T11 to L3, respectively, with coronal imbalance. Posteroanterior side bending films (c, d) show good flexibility of the curve

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Fig. 7  Plain radiographs of the whole spine (a, b) taken after application of growing rod instrumentation. Postoperative radiographs (c–h) taken after serial growing rod distractions Fig. 8  Anteroposterior (a) and lateral (b) radiographs of the whole spine taken after posterior instrumented deformity correction and fusion

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useful tip while attempting resection of plexiform neurofibromas is to separate the tumor from the surrounding tissues by meticulous dissection rather than cutting through the substance of the tumor. Dissection through the tumor may result in undue bleeding from the engorged sinusoids, which may be difficult to control. This was followed by a posterior instrumented deformity correction and fusion (Fig. 11a, b).

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Fig. 9  Clinical photographs of the patient (a, b) showing the presence of shoulder imbalance and coronal imbalance. Anteroposterior (c) and lateral (d) radiographs of the spine showing an angular kyphoscoliosis of the thoracolumbar spine. Side bending films (e, f) demonstrating the flexibility of the curve

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Fig. 10 (a) Clinical photograph of the patient showing the plexiform neurofibroma located in the midline of the back in the lumbosacral region. (b) Mid-sagittal T2W MRI of the lumbosacral spine, showing the plexiform neurofibroma located subcutaneously in the lumbosacral spine. Intraoperative photograph (c) showing the plexiform neurofibroma meticulously dissected from the underlying muscle to aid in the exposure of the spine. (d) Intraoperative photograph after removal of the plexiform neurofibroma. (e) Photograph of the removed plexiform neurofibroma. (f) Intraoperative photograph showing the plan of wound closure

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Fig. 11 Postoperative radiographs (a, b) taken at 25 months follow-up showing good correction of the deformity

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References 1. Tamura R. Current understanding of neurofibromatosis type 1, 2, and Schwannomatosis. Int J Mol Sci. 2021;22(11):5850. https://doi.org/10.3390/ijms22115850. 2. Crawford AH, Herrera-Soto J. Scoliosis associated with neurofibromatosis. Orthop Clin North Am. 2007;38(4):553–62. 3. Crawford AH, Parikh S, Schorry EK, Von Stein D. The immature spine in type-1 neurofibromatosis. J Bone Joint Surg Am. 2007;89(suppl 1):123–42. 4. Crawford AH. Pitfalls of spinal deformities associated with neurofibromatosis in children. Clin Orthop Relat Res. 1989;245:29–42. 5. Akbarnia BA, Gabriel KR, Beckman E, et  al. Prevalence of scoliosis in neurofibromatosis. Spine (Phila Pa 1976). 1992;17(8 Suppl):S244–8. 6. Tsirikos AI, Saifuddin A, Noordeen MH.  Spinal deformity in neurofibromatosis type-1: diagnosis and treatment. Eur Spine J. 2005;14(5):427–39. https://doi.org/10.1007/ s00586-­004-­0829-­7. 7. Gould EP.  The bone changes occurring in von Recklinhausen’s disease. Q J Med. 1918;11:221–8. 8. Funasaki H, Winter RB, Lonstein JB, Denis F. Pathophysiology of spinal deformities in neurofibromatosis. J Bone Joint Surg Am. 1994;76A:692–700. 9. Crawford AH, Bagamery N.  Osseous manifestations of neurofibromatosis in childhood. J Pediatr Orthop. 1986;6:72–88. 10. Riccardi VM.  Neurofibromatosis: phenotype, natural history, and pathogenesis. Baltimore: Johns Hopkins University Press; 1992. p. 158–65. 11. Hu Z, Liu Z, Qiu Y, Xu L, Yan H, Zhu Z. Morphological differences in the vertebrae of scoliosis secondary to neurofibromatosis type 1 with and without paraspinal neurofibromas. Spine (Phila Pa 1976). 2016;41(7):598–602.

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61. Neifert SN, Khan HA, Kurland DB, Kim NC, Yohay K, Segal D, Samdani A, Hwang S, Lau D.  Management and surgical outcomes of dystrophic scoliosis in neurofibromatosis type 1: a systematic review. Neurosurg Focus. 2022;52(5):E7. https://doi.org/10.3171/2022.2.F OCUS21790. 62. Halmai V, Doman I, de Jonge T, et al. Surgical treatment of spinal deformities associated with neurofibromatosis type 1. Report of 12 cases. J Neurosurg. 2002;97(3 Suppl):310–6. 63. Parisini P, DiSilvestre M, Greggi T, Paderni S, Cervellati S, Savini R. Surgical correction of dystrophic spinal curves in neurofibromatosis: a review of 56 patients. Spine (Phila Pa 1976). 1999;24:2247–53. 64. Wang Z, Fu C, Leng J, Qu Z, Xu F, Liu Y. Treatment of dystrophic scoliosis in neurofibromatosis type 1 with one-stage posterior pedicle screw technique. Spine J. 2015;15(4):587–95. https://doi.org/10.1016/j.spinee.2014.10.014. 65. Sun D, et al. Posterior-only spinal fusion without rib head resection for treating type I neurofibromatosis with intra-canal rib head dislocation. Clinics (Sao Paulo). 2013;68:1521–7. 66. Shao X, Huang Z, Yang J, Deng Y, Yang J, Sui W.  Efficacy and safety for combination of t-EMG with O-arm assisted pedicle screw placement in neurofibromatosis type I scoliosis surgery. J Orthop Surg Res. 2021;16(1):731. https://doi.org/10.1186/s13018-­021-­02882-­9. 67. Wang JY, Lai PL, Chen WJ, Niu CC, Tsai TT, Chen LH. Pedicle screw versus hybrid posterior instrumentation for dystrophic neurofibromatosis scoliosis. Medicine (Baltimore). 2017;96(22):e6977. 68. Li S, Mao S, Du C, et al. Assessing the unique characteristics associated with surgical treatment of dystrophic lumbar scoliosis secondary to neurofibromatosis type 1: a single-center experience of more than 10 years. J Neurosurg Spine. 2021;34(3):413–23. 69. Koptan W, ElMiligui Y. Surgical correction of severe dystrophic neurofibromatosis scoliosis: an experience of 32 cases. Eur Spine J. 2010;19(9):1569–75. 70. Mladenov KV, Spiro AS, Krajewski KL, Stücker R, Kunkel P. Management of spinal deformities and tibial pseudarthrosis in children with neurofibromatosis type 1 (NF-1). Childs Nerv Syst. 2020;36(10):2409–25. 71. Singh K, Samartzis D, An HS. Neurofibromatosis type I with severe dystrophic kyphoscoliosis and its operative management via a simultaneous anterior-posterior approach: a case report and review of the literature. Spine J. 2005;5(4):461–6. 72. Jin M, Liu Z, Liu X, et  al. Does intraoperative navigation improve the accuracy of pedicle screw placement in the apical region of dystrophic scoliosis secondary to neurofibromatosis type I: comparison between O-arm navigation and free-hand technique. Eur Spine J. 2016;25(6):1729–37. 73. Li Y, Yuan X, Sha S, et  al. Effect of higher implant density on curve correction in dystrophic thoracic scoliosis secondary to neurofibromatosis type 1. J Neurosurg Pediatr. 2017;20(4):371–7. 74. Bouthors C, Dukan R, Glorion C, Miladi L. Outcomes of growing rods in a series of early-­ onset scoliosis patients with neurofibromatosis type 1. J Neurosurg Spine. 2020;33(3):373–80. 75. Cai S, Cui L, Qiu G, Shen J, Zhang J. Comparison between surgical fusion and the growing rod technique for early-onset neurofibromatosis type-1 dystrophic scoliosis. BMC Musculoskelet Disord. 2020;21(1):455. 76. Cai S, Li Z, Qiu G, et al. Posterior only instrumented fusion provides incomplete curve control for early-onset scoliosis in type 1 neurofibromatosis. BMC Pediatr. 2020;20(1):63. 77. Deng A, Zhang HQ, Tang MX, Liu SH, Wang YX, Gao QL. Posterior-only surgical correction of dystrophic scoliosis in 31 patients with neurofibromatosis type 1 using the multiple anchor point method. J Neurosurg Pediatr. 2017;19(1):96–101. 78. Iwai C, Taneichi H, Inami S, et al. Clinical outcomes of combined anterior and posterior spinal fusion for dystrophic thoracolumbar spinal deformities of neurofibromatosis-1: fate of nonvascularized anterior fibular strut grafts. Spine (Phila Pa 1976). 2013;38(1):44–50.

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79. Jain VV, Berry CA, Crawford AH, Emans JB, Sponseller PD. Growing rods are an effective fusionless method of controlling early-onset scoliosis associated with neurofibromatosis type 1 (NF1): a multicenter retrospective case series. J Pediatr Orthop. 2017;37(8):e612–8. 80. Xu E, Gao R, Jiang H, Lin T, Shao W, Zhou X. Combined halo gravity traction and dual growing rod technique for the treatment of early onset dystrophic scoliosis in neurofibromatosis type 1. World Neurosurg. 2019;126:e173–80. 81. Yao Z, Guo D, Li H, et al. Surgical treatment of dystrophic scoliosis in neurofibromatosis type 1: outcomes and complications. Clin Spine Surg. 2019;32(1):E50–5. 82. Yao Z, Li H, Zhang X, Li C, Qi X.  Incidence and risk factors for instrumentation-related complications after scoliosis surgery in pediatric patients with NF-1. Spine (Phila Pa 1976). 2018;43(24):1719–24.

Is Scoliosis Associated with Neurofibromatosis Different from AIS? The Highlights Balaji Zacharia

1 Introduction • Neurofibroma is a Phacomatosis. It has hamartomatous lesions in the skin and central and peripheral nervous systems. It involves the neuroectoderm, endoderm, and mesoderm. It affects skin, bones, soft tissues, and bones. • There are two forms of neurofibromatosis (NF). The peripheral type NF-1 and central type are characterized by tumors in the CNS, such as acoustic neuroma NF-2. • NF-1 (von Recklinghausen disease) is an autosomal dominant disorder. Multiple neurofibromas and cafe-au-lait spots are the characteristic findings. This affects approximately one in 4000 people. • The diagnostic criteria for NF-1 1. 6 or more cafe-au-lait spots >5 mm in prepubertal children and >15 mm in postpubertal children. 2. Two or more neurofibroma of any type or single plexiform neurofibroma. 3. Axillary or inguinal freckling. 4. Optic glioma. 5. 2 or more Lisch nodules. 6. Bony lesions like sphenoid dysplasia, thinning of the cortex of long bones with or without pseudarthrosis. 7. A first-degree relative identified with the above criteria. • There are many cutaneous manifestations, such as cafe-au-lait spots, cutaneous neurofibromas (fibroma molluscum), pigmented nevi (nevus lateralus), axillary and inguinal freckles, and verrucous hyperplasia of the skin. B. Zacharia (*) Department of Orthopedics, Government Medical College, Kozhikode, Kerala, India e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. Zacharia et al. (eds.), Paediatric Scoliosis, https://doi.org/10.1007/978-981-99-3017-3_36

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• Soft tissue hypertrophy can lead to localized gigantism, pachydermatocele, elephantiasis, and plexiform neurofibromatosis. • The orthopedic manifestations include spinal deformities, pseudarthrosis of the tibia, hemihypertrophy, and neoplasms.

2 Scoliosis in NF-1 • Scoliosis is the most common skeletal complication associated with NF-1. The exact incidence of it in neurofibromatosis is unknown. Nonstructural scoliosis due to limb hypertrophy or dysplasias is common in NF-1. Screening by Adam forward bending must be performed in all children with neurofibromatosis. • Thoracic scoliosis is the most common type. Endocrine dysplasia, osteomalacia, and neurofibroma erosion or infiltration of the vertebrae are some of the proposed causes, but the exact etiology is unknown. • There are two varieties of scoliosis in neurofibromatosis nondystrophic scoliosis and dystrophic scoliosis.

3 Imaging • Routine radiographs of the spine in frontal and lateral views are required in all cases. This should include the entire spine from the cervical to the sacral region. Otherwise, we may miss cervical kyphosis or lumbar spondylolisthesis associated with scoliosis. Before surgical treatment, an MRI scan or high-volume CT myelogram in the prone, supine, and lateral positions of the spine should be performed. This will help to determine whether intraspinal neurofibroma, dural ectasia, and pseudo meningocele are present.

4 Nondystrophic Scoliosis • Nondystrophic scoliosis is a common spinal deformity in NF-1. The clinical findings are similar to those of adolescent idiopathic scoliosis (AIS). There is an increased incidence of progression of the curve compared to AIS. There can be intraspinal neurofibromatosis with canal widening and dystrophy of the vertebrae. • In some cases, there is a definite tendency for nondystrophic curves to become dystrophic later. This is termed “modulation.” This is common in deformities appearing early in life. It is a characteristic of deformities associated with NF. it indicates rapid progression. It can occur slowly or aggressively. We have to closely follow up with these children if the curve acquires more than three

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penciled-­ out ribs or three dystrophic features, there is a definite risk of progression. • The treatment principles of nondystrophic scoliosis are similar to the principles of treatment of AIS. Curves >20° need to be observed. Bracing can be tried for curves up to 30–35°. For curves, more than 35° posterior release instrumentation and fusion are recommended. Anterior release and bone grafting followed by posterior instrumented fusion. Fusion of the facets with segmental instrumentation is essential for preventing pseudarthrosis. There is a high rate of pseudarthrosis even in nondystrophic scoliosis associated with NF-1.

5 Dystrophic Scoliosis • Dystrophic scoliosis is a short and sharply angulated curve. It usually involves 4–6 vertebrae. They are common in the upper thoracic region. It may be seen in early childhood. • Radiologically dystrophic curves are characterized by wedging of the vertebrae, vertebral scalloping, widening of the interpedicular distance, widening of the spinal canal, and severe rotation of the vertebrae. Anteroposterior rotation of the ribs makes it look abnormally thin on radiographs. Other findings, such as penciling of the ribs, the spindled appearance of the transverse processes, and the presence of a paravertebral soft tissue mass, can also be present. • The widening of the canal can be due to intraspinal neurofibroma or dural ectasia (an increase in the width of the thecal sac). Both conditions will increase the hydrostatic pressure, causing expansion and erosion of the vertebral body and spinal canal. This expansion leads to severe angular deformities without neurological compromise. • Children with nonprogressive curves should be closely followed up to determine whether the curves are turning into a dystrophic type. • It is very important to determine dystrophic curves. They will progress. There is no role for observation and bracing in dystrophic curves. These curves can progress even after fusion. • Children with curves less than 20 degrees must be observed for progression every 6  months. Curves between 20 and 40° are treated by posterior release, segmental instrumentation, and fusion. In curves, more than 40° of anterior release bone grafting followed by posterior segmental instrumentation and fusion is recommended. The extent of fusion is between the upper and lower neutral vertebrae. There is a high incidence of pseudarthrosis in dystrophic scoliosis, so the fusion of facet joints is necessary. • Fusion can be performed at an early age in progressive curves. Since these are short curves with less growth potential in the affected vertebra, early fusion has a minimal effect on the longitudinal growth of the spine.

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6 Kypholosis • Kyphosis and lordosis are associated with dystrophic scoliosis. • Kyphoscoliosis is associated with sharp posterior angulation. The apical vertebra is severely deformed and attenuated and sometimes may not be visible in the X-ray. In severe cases, there can be bayonet apposition of the vertebral segments above and below the apex of the kyphosis. This is due to lateral subluxation of the vertebrae due to dystrophic changes. Kyphoscoliosis can produce paraplegia. Kyphosis is responsible for paraplegia. The kyphotic angulation leads to undue elongation and stretching of the spinal cord, causing neurological impairment. • There are two types of dystrophic kyphoscoliosis. Type 1 kyphosis is less than 50° (posterior surgery alone), and Type II kyphosis is more than 50° (combined anterior and posterior surgery). • Combined anterior and posterior surgeries give the best results for dystrophic kyphoscoliosis. The entire curve needs to be fused anteriorly. Vascularized or nonvascularized fibulas can be used for anterior grafting. Fusion failure occurs even after combined fusion. Improper anterior fusion is the major cause of failure. Dural ectasia and intraspinal neurofibroma are the other causes of failure. Postoperative immobilization may be required in most cases. • Laminectomy is contraindicated in neurological deficits associated with kyphoscoliosis. The stretching of the cord is due to angulation of the spine anteriorly laminectomy cannot relieve it. Additionally, laminectomy destabilizes the spine, leading to progression of kyphosis. All patients should undergo anterior decompression and fusion.

7 Lordoscoliosis • There is a small subset of dystrophic scoliosis where the sagittal alignment of the thoracic spine is negative; these deformities are termed lordoscoliosis. Lack of reporting of such cases may be the reason for the low incidence. Kyphosis may develop above the deformity in such cases. Posterior segmental instrumentation and fusion is the preferred treatment. Posterior element thinning due to dystrophy and dural ectasia makes planning and instrumentation challenging in such cases.

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8 Expected Complications • There can be excessive bleeding during surgery. This is common with anterior surgery. The plexiform venous anomalies in the soft tissues around the spine are the reason for the bleeding. The excessive vascularity of the neurofibromatosis tissue is another reason. • Due to osteopenia and osteomalacia, fewer pedicle screws were purchased. Sublaminar wires are an alternative in such cases. • The change in the alignment of the spine in kyphoscoliotic deformities makes the placement of the fibular graft difficult. Adequate strut grafting on the concave side should be performed during anterior fusion. Convex discectomies can further destabilize the spine. • Cervical deformities, especially kyphosis in the cervical spine, may be seen in NF-1. This should be identified and treated preoperatively. It can cause difficulties during the induction of anesthesia. Lumbar spondylolisthesis may also be seen in NF-1. • There can be thinning of the posterior elements, especially the lamina. Care must be taken during exposure to avoid injuring the cord by inadvertent fracture of the lamina. This can occur in cases with dural ectasia. • Pheochromocytomas are seen rarely in neurofibromatosis. This can cause challenges to anesthesia. Case Illustration A 13-year-old boy noticed progressive deformity of the back. Examination at the time of presentation showed a short stiff right thoracic curve and multiple café au lait spots. The anteroposterior radiograph showed short right-sided scoliosis with wedging of the vertebrae, severe apical rotation, and penciling of the ribs (Fig. 1). The lateral view showed normal thoracic kyphosis (Fig.  2). Dystrophic scoliosis with NF-1 was the diagnosis. The patient was treated by anterior release instrumentation and fusion (Figs. 3 and 4). Postoperatively, the boy received a nice correction of the deformity, and the figure also shows café au lait spots (Figs. 5 and 6).

588 Fig. 1  The anteroposterior radiograph showing a short right-sided scoliosis with wedging of the vertebrae, severe apical rotation, and penciling of the ribs

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Is Scoliosis Associated with Neurofibromatosis Different from AIS? The Highlights Fig. 2  The lateral radiograph showing the kyphosis

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590 Fig. 3  The anteroposterior X-ray after anterior release and instrumentation with fusion

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Is Scoliosis Associated with Neurofibromatosis Different from AIS? The Highlights Fig. 4  The lateral radiograph after corrective surgery

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592 Fig. 5  The clinical photograph after correction

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Is Scoliosis Associated with Neurofibromatosis Different from AIS? The Highlights Fig. 6  The rib hump reduced after correction

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Scoliosis in Muscular Dystrophy and Spinal Muscular Atrophy Ranjith Unnikrishnan and Rohan Gala

Highlights • Duchenne muscular dystrophy and spinal muscular atrophy lead to scoliosis due to progressive muscular weakness, with a significant number of patients being wheelchair-bound or “sitters.” • Surgery is inevitable in the majority of these patients due to rapid progression leading to severe pain, costopelvic impingement, truncal asymmetry, and imbalance along with a reasonable degree of deterioration of pulmonary function. • Pelvic obliquity is an important factor in deciding whether the fusion needs to be extended up to the pelvis. • Halo is an excellent adjunct that can be used preoperatively in both optimizing nutrition and pulmonary function so that this subset of patients can tolerate any kind of surgical intervention. • Surgical interventions are mainly posterior arthrodesis, with anterior surgeries reserved in select cases. • Due to the high incidence of perioperative complications (cardiopulmonary, gastrointestinal, neurological), a multidisciplinary approach is required in managing these patients for an optimum outcome. • Intraoperative neural monitoring adds to intraoperative safety while surgically managing these patients. Nusinersen is a recently approved drug and can be used intraoperatively in spinal muscular atrophy patients. • Iatrogenic complications such as implant failure, infections, and pseudoarthrosis are more common in these patients.

R. Unnikrishnan (*) KIMS Hospital, Trivandrum, Kerala, India e-mail: [email protected] R. Gala D.Y. Patil Hospital and Research Centre, Navi Mumbai, Maharashtra, India © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. Zacharia et al. (eds.), Paediatric Scoliosis, https://doi.org/10.1007/978-981-99-3017-3_37

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1 Introduction of Neuromuscular Scoliosis Neuromuscular scoliosis includes a large number of underlying pathologies and varied diagnoses describing spinal deformities that are noncongenital in origin with any type of preexisting neuromuscular disorder. They include a diverse group of central and peripheral disorders, among which the most commonly seen are those secondary to cerebral palsy, Duchenne muscular dystrophy (DMD), myelomeningocele, spinal muscular atrophy (SMA), Friedreich ataxia, and spinal cord injury. The Scoliosis Research Society (SRS) has classified them as neuropathic, with central or peripheral motor neuron involvement or both, or myopathic [1]. However, as per the Dutch guideline laid in 2008, the definition is any defect in the functioning of the peripheral nerve system, the neuromuscular junction, or muscles that causes muscle weakness in patients [2]. Among these, scoliosis secondary to DMD and SMA is most commonly seen. Both disorders, although diverse, have some similarities, including the genetic origin of the disease and/or the development of scoliosis secondary to progressive muscular weakness.

2 Why Surgery in These Patients? Neuromuscular scoliosis is typically characterized by C-shaped thoracolumbar and lumbar curves with a long collapsing spine, an oblique pelvis, and changes in sagittal plane balance that can affect sitting and cardiopulmonary function with underlying neuromuscular pathologies. They tend to progress rapidly in patients who have concomitant congenital anomalies and certain negative predictors, such as osteopenia. A significant proportion of these curves do not respond to orthotic management due to their rapidly progressive nature. The progressive nature of these curves not only causes discomfort but also interferes with health and well-being, ambulation, wheelchair transmission, and sitting balance. Sequelae in these patients if left untreated or if the progression of the curve is not halted further lead to worsening of pulmonary function, costopelvic impingement and pain, truncal asymmetry, and pelvic asymmetry, thereby causing severe discomfort for sitters. Surgery is therefore indicated in these patients to prevent complications due to curve progression, develop a better coronal and sagittal balance, and more importantly develop a good sitting balance by addressing the pelvic obliquity. Overall improve the health-related quality of life in these patients.

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Scoliosis in Muscular Dystrophy and Spinal Muscular Atrophy

3 Key Elements Duchenne Muscular Dystrophy (DMD) DMD is an X-linked (Xp21) recessive disorder affecting males who inherit the genetic mutation from the mother. Patients show progressive muscle weakness and wasting, leading to the inability to walk and becoming wheelchair-dependent by the age of 10. During puberty, there is a progressive weakness of all four limbs and the torso leading to scoliosis causing gradual deterioration of respiratory function in this phase. Cardiac dysfunction is also seen in a proportion of these patients, and nearly 40% of DMD patients have mild mental retardation. DMD is diagnosed by repeated determination of extremely elevated creatine kinase (CPK-MM) levels in the bloodstream and dystrophin gene mutations on the X-chromosome or a muscle biopsy showing the absence of dystrophin [2].

Spinal Muscular Atrophy (SMA) SMA is an autosomal recessive disease that includes a group of neuromuscular disorders characterized by degeneration of alpha motor neurons in the spinal cord with muscular hypotonia, hyporeflexia symmetrical weakness, and atrophy of the skeletal muscles. It is caused by deletion or mutation in the telomeric survival motor neuron gene (telSMN-gene. SMN-1) on chromosome 5q13 [2]. It is further divided into four types [3] (Table 1).

Table 1  Types of spinal muscular atrophy. (With permission from Fujak et al.: Natural course of scoliosis in proximal spinal muscular atrophy type II and IIIa: a descriptive clinical study with retrospective data collection of 126 patients. BMC Musculoskeletal Disorders 2013 14:283) Types Ia more severe Ib less severe

Manifestation Prenatal (30%) to 3–6 months Like Ia II intermediate Birth -18 months IIIa mild, retarded motor To 3 years development >3–30 years IIIb mild, normal motor development IV adult >30 years

Function Unable to roll over or sit Like Ia Sitting Walking Walking

Life expectancy 25 kg/m2 by Ramo et al. [14]

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Pulmonary Preoperative assessment of respiratory function is of vital importance to prevent postoperative respiratory complications. The first step is a preoperative assessment to identify patients at risk of postoperative respiratory complications. Hypoventilation daytime or at night, ineffective coughing, and forced vital capacity