yes Amazon acai: Chemistry and biological activities: A review [1/1, 1 ed.]

Citation preview

Food Chemistry 179 (2015) 137–151

Contents lists available at ScienceDirect

Food Chemistry journal homepage: www.elsevier.com/locate/foodchem

Review

Amazon acai: Chemistry and biological activities: A review Klenicy Kazumy de Lima Yamaguchi a, Luiz Felipe Ravazi Pereira a, Carlos Victor Lamarão a Emerson Silva Lima b, Valdir Florêncio da Veiga-Junior a,⇑ a b

Chemistry Department, Amazonas Federal University, Av. Rodrigo Octávio, 6.200, Japiim, Manaus, AM 69080-900, Brazil Pharmaceutical Sciences Faculty, Amazonas Federal University, Alexandre Amorin Street, 330, Aparecida, Manaus, AM 69010300, Brazil

a r t i c l e

i n f o

Article history: Received 30 June 2014 Received in revised form 5 December 2014 Accepted 8 January 2015 Available online 4 February 2015 Keywords: Amazon Euterpe genus Polyphenols Pharmacological activities

a b s t r a c t Acai (acai or assai) is one of the Amazon’s most popular functional foods and widely used in the world. There are many benefits to its alleged use in the growing market for nutraceuticals. The acai extracts have a range of polyphenolic components with antioxidant properties, some of those present in greater quantity are orientin, isoorientin and vanillic acid, as well as anthocyanins cyanidin-3-glucoside and cyanidin3-rutinoside. The presence of these substances is linked mainly to the antioxidant, anti- inflammatory, anti-proliferative and cardioprotective activities. Importantly, there are two main species of the Euterpe genus which produce acai. There are several differences between them but they are still quite unknown, from literature to producers and consumers. In this review are highlighted the chemical composition, botanical aspects, pharmacological, marketing and nutrition of these species based on studies published in the last five years in order to unify the current knowledge and dissimilarities between them. Ó 2015 Elsevier Ltd. All rights reserved.

Contents 1. 2. 3. 4.

5.

6. 7.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acai botanical description . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Production and market value . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Biological studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Traditional applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. E. oleracea versus E. precatoria – pulp activities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.1. General . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.2. E. oleracea pulp: in vitro assay . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.3. E. oleracea pulp: cell assays . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.4. E. oleracea pulp: in vivo studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.5. E. oleracea: biological activities of other Euterpe palm tree parts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Phytochemical constituents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1. Chemical studies of acai pulp . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Chemical constituents from other parts of the palm tree: roots, leaves and flowers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nutritional composition and other considerations about the Acai fruit and its beverages . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.1. The beverages from acai and other by-products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2. Biocosmetics and cosmetology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.3. Pharmaceutical and functional applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

⇑ Corresponding author. Tel.: +55 92 9903 6771. E-mail address: [email protected] (V.F. da Veiga-Junior). http://dx.doi.org/10.1016/j.foodchem.2015.01.055 0308-8146/Ó 2015 Elsevier Ltd. All rights reserved.

138 138 139 139 139 139 139 140 140 141 141 142 142 148 148 148 148 148 149 149 149

138

K. K. d. L. Yamaguchi et al. / Food Chemistry 179 (2015) 137–151

1. Introduction Acai pulp has received much attention in recent years as one of the new ‘‘superfruits’’. The consumption of acai from the Amazon has been increasing, mainly due to the benefits that are being screened by scientific works. The Euterpe species has a high economic potential, mainly due to the use of its fruits in the preparation of acai beverages which are exported all over the world as an energetic drink. The review paper published by 2002 (Silva, Munaro, & Pereira, 2002) was almost strictly related to the management and operation of acai as a source of palm hearts for the food industry. Fruit production was designed especially for the local and regional market, and acai palm was identified as the palm tree of great cultural, economic and social importance in the northern region of Brazil (Queiroz & Melém Junior, 2001). The initial studies involving the biological activities of acai were based on the description of its popular use by the Amazonian communities. The main parts that were listed for medicinal use were leaves and roots, which, according to residents, had anti-inflammatory and antimalarial activities; this was later confirmed by scientific studies (Bourdy et al., 2000; Ruiz, MacO, Cobos, Gutierrez-Choquevilca, & Roumy, 2011). In the past decade there has been a notable increase in the use of acai berry as an energetic drink with simultaneous studies showing its anti-aging properties and the presence of bioactive compounds, leading to a significant increase in scientific research during this period. Currently, the acai fruit is one of those most studied by researchers, worldwide, and its use is widespread in the food market and in the pharmaceutical and cosmetic industry. The consumption is no longer simply for locals in the northern Brazilian estates, normally as a sidedish accompanying fish and tapioca flour. It is now also consumed by the southern and southeastern Brazilian populations and also in many countries of Europe, United States, Japan and China. Amazonian acai health benefits are associated with the chemical composition, especially the presence of bioactive substances, such as phenolics, flavonoids and anthocyanins. Acai has been the subject of studies for the food industry, and also for the cosmetic and pharmaceutical industries (Costa, Garcia-Diaz, Jimenez, & Silva, 2013; Menezes, Deliza, Chan, & Guinard, 2011; PachecoPalencia & Talcott, 2010; Sabbe, Verbeke, Deliza, Matta, & Van Damme, 2009). Various biological activities are described in acai studies for both Euterpe oleracea and Euterpe precatoria. Despite the many published papers, few studies make reference to the different acai

plant species; although both are widely used by the population, they exhibit distinct chemical compositions. Many studies have been performed to evaluate various pharmacological activities, using the acai from the Amazon region. The antioxidant activity of the pulp is the most evaluated by different tests, including the scan of free radicals in vitro in human plasma and in cell models. In 2011, a review was published by Heinrich, Dhanji, and Casselman (2011), revealing mainly some bioactive metabolites and pharmacological activities. This review was only focussed on the E. oleracea species, showing 20 chemical structures and 10 major pharmacological studies of this species. The present study aims to expand the knowledge about the chemical composition, biological activities and pharmacological activities of acai from the Amazon region, highlighting the most recent and important studies about botanical, chemical and pharmacological properties, with a focus on food industrial applications and market data, for the two acai species consumed worldwide. 2. Acai botanical description The Euterpe genus has about 28 species located in Central and South America and distributed throughout the Amazon basin. The three species that occur most frequently are E. oleracea, E. precatoria and Euterpe edulis. However, only the first two species are commercially used for their fruits. The major difference between the two species is the way the palms grow. E. precatoria is a native of the state of Amazonas, popularly known as ‘‘acai-do-amazonas’’ and is found in the Amazonas River Basin, in a land area of upland and lowland, most commonly seen south of the equator (Choi, Lee, Lee, Lee, & Park, 1998) and especially in occidental Amazonia (Fig. 1). On the other hand, E. oleracea, popularly known as ‘‘acaido-pará’’, is found mainly in lowland and in flooded forest land of the Amazon River estuary, in the Brazilian estates of Pará, Maranhão, Tocantins, Amapá, and also in Guyana and Venezuela. Despite the greater amount of Euterpe specimens concentrated in the eastern side of the Amazon forest, it is also observed in the setentrional area of South America (Choi, Lee, Lee, Lee, & Park, 1998; Muñiz-Miret, Vamos, Hiraoka, Montagnini, & Mendelsohn, 1996). E. precatoria palm tree has an average height of 20 m. The inflorescences develop the armpit leaves, after senescence of the older leaves and are protected by sheaths. The fruits are globose, measuring 0.9–1.3 cm in diameter, green when immature, red in the middle stage and dark purple when ripe, with a juicy mesocarp. There is one seed per fruit, with a solid and homogeneous

Fig. 1. Seeds and palm trees of (A) E. precatoria and (B) E. oleracea and (C) botanical distribution of the two species.

K. K. d. L. Yamaguchi et al. / Food Chemistry 179 (2015) 137–151

endosperm (Henderson, 1995). Bovi and Castro (1993) described the species as one that has continuously formed adventitious roots at the base of the trunk, where they form a thick ring (1.5 cm) of purplish aerial roots around its base which can reach 80 cm deep in soil. The inflorescence is composed of a hard central rachis, approximately 56 cm long, with an average of 54 rachilles (Bovi & Castro, 1993). Adult subjects produce from 1 to 4 bisexual inflorescences per flowering period. Each inflorescence has numerous male and female flowers with sizes of 4.5  2.7 mm (male) and 3.2  2.6 mm (female). Male flowers provide pollen before the female flowers are receptive. Thus the species is predominantly allogamous (performs cross-fertilization). The presence of pneumatophores in the plant that help the root system to breathe in flooded soils, suggests that it is well adapted to periodically flooded land (Bovi & Castro, 1993). Henderson (1995) suggests that the adaptation of E. precatoria in flooded land seems to be physiological rather than morphological. E. oleracea is a multicaule palm, with up to 25 stems per clump. The trunks in adults have heights ranging between 3 m and 20 m and a diameter of 7 cm to 18 cm. Each stem holds, at its end, a set of 8–14 compounds, pinnate leaves and spiral arrangement, with 40–80 pairs of leaflets, opposite or sub-opposite. The inflorescence of this acai is leaf below, protected from the sun; this is different from other species of the genus Euterpe, where the inflorescence is arranged almost horizontally. In the first twothirds of each raquila, flowers are arranged in triads, with each female flower flanked by two male flowers. In the third terminal of rachilles, usually only the male flowers lie. The inflorescences are, on average, 80.5% of male flowers and 19.5% of female flowers. The fruit ripening is complete in about 175 days, presenting a violet color and diameter about 13.5 mm in Henderson (1995). At harvest, one can differentiate the species through the botanical characteristics of the palm tree and also by the fruit size, but when it is prepared for consumption, it is not possible to know which type of acai that is being consumed. The fruits and the palm trees of the two species can be seen in Fig. 1.

3. Production and market value The consumption of the two main species of acai has increased considerably. According to IBGE (2013), Brazil produced, in 2011, a total of 215.4 thousand tons of acai berries. The state of Pará was the main contributor, with 50.8% of national production in 2011. The state of Amazonas comes next, accounting for 41.5% of Brazil’s total. According to the latest data from the Brazilian Statistical Institute (IBGE, 2013), by the year 2010, the production of acai in the state of Amazonas was negligible, having a historical representation of only 2–3% of the national total production. The state of Para was the major producer, holding an average record of about 85% of the national supply. However, in 2011 the situation changed with strong advances in the Amazonas state production of acai, initiating a new milestone as it went from 3.3 thousand tons of fruit in 2010 to approximately 89.5 tons, threatening the historical control from the Pará estate, which grew only 2.6% from 2010 to 2011, from 106.6 to 109.3 thousand tons (Herculano, 2013). As each state produces acai pulp fruits mainly from one species, after processing it is impossible to make a distinction visually. Differences in state production affect the chemical composition and biological properties for industry and consumers. When combined with the output of all Brazilian producing states, the acai production in 2011 was approximately 215.3 thousand tons, generating an estimated monetary movement of US$ 700,000 (IBGE, 2013). According to this, the price per ton of acai was about US$ 3.22 million, thus surpassing the price per ton of soybeans with a market

139

value of US$ 2208, and also of other food products exported, e.g. the Brazilian-nut with a market value of US$ 2415 million per ton (CONAB, 2014). 4. Biological studies 4.1. Traditional applications Some factors, e.g. the geographic isolation and limited access to medical care in some places, have resulted in a unique, complex and reliable traditional medicine. In Latin America, many communities use plants as a single resource to search for a cure for many diseases. In ethnomedicine, E. precatoria is widely used by the local population. The stem of the leaf is used against snake bites and muscular aches, while the leaf is used to relieve chest pain. The seeds are used to prepare a dark green oil, popularly used as an antidiarrheal agent (Brian, 1998; Galotta & Boaventura, 2005). Most of the reported applications describe the use of the plant’s roots by the population of different countries of Latin America and the main activity is related to the use against malaria. In Bolivia, roots are used traditionally to treat inflammatory processes and antiplasmodial activity. They are administered in the form of a decoction or syrup to alleviate strong muscle, back or sciatic pains or even liver pain, and also as a general tonic for people prone to illnesses (Bourdy et al., 2000). In the Amazonian part of Ecuador, roots are also used, but as a muscle pain reliever. In Iquitos (Peru), indigenous and mestizo populations from the river Nanay in Loreto, the root decoction is used to treat kidney and liver disease and is known for being effective in all skin ulceration and healing problems, malaria treatment, and edema (Brian, 1998; Ruiz et al., 2011). E. oleracea roots are also used in French Guiana as an antimalarial agent in popular medicine, but always in combination and preferably with other medicinal plants such as Caricapapaya, Citrus sp. (lemon) and Quassia amara (Vigneron, Deparis, Deharo, & Bourdy, 2005), showing low activity when compared with other species. Besides this activity, there are reports that these species are also used as subcutaneous treatment against leishmaniasis by the French Guiana population. In Colombia and Suriname, it is used medically in the treatment of diarrhea (Gallori, Bilia, Bergonzi, Barbosa, & Vincieri, 2004; Odonne, Berger, Stien, Grenand, & Bourdy, 2011; Pacheco-Palencia, Mertens-Talcott, & Talcott, 2008). 4.2. E. oleracea versus E. precatoria – pulp activities 4.2.1. General There are few biological studies with E. precatoria; however, this is a changing situation since its production is increasing. Studies with E. oleracea are the most numerous, among other factors, due to the greater use of its fruit pulp worldwide. Studies comparing the two pulp species, employing multiple assays associated with different ROS/RNS (in vitro) and in cellular models, have shown that the antioxidant activities of the E. precatoria fruit pulp were superior to those of the E. oleracea fruit pulp in all assays reported (Kang et al., 2012). The activities described for both species can be seen in Table 1. The results suggest that E. precatoria contains much stronger water-soluble antioxidants that can enter the live cells and effectively inhibit ROS formation better than those from E. oleracea. The phenolic compounds were not correlated with antioxidant capacities, suggesting that other compounds, yet to be identified, may contribute considerably to the wide free radicalscavenging capacities of this pulp. However, the fruit pulp polyphenol-rich extract inhibited NF-jB activation, as assessed by the secreted embryonic alkaline phosphatase (SEAP) reporter assay, suggesting that the fruit pulp has potential anti-inflammatory

140

K. K. d. L. Yamaguchi et al. / Food Chemistry 179 (2015) 137–151

Table 1 Biological activities tested in different Euterpe species. Species

Part of plant

Biological activity evaluated

References

E. oleracea

Pulp

Scavenging free radicals and inhibition of the oxidation activity of liposomes

Pulp Pulp

Inhibition of activity in cultured MCF-7 cells stressed by H2O2 Inhibition of the nitrite oxide production and expression of iNOS

Pulp Pulp Pulp Pulp Pulp Pulp Pulp

Reduction in oxidative damage and inflammation in brain cells Reduction of coronary disease risk due to the vasodilation effect Inhibition of pro-inflammatory cytokines through regulating inflammatory mediators Antigenotoxic effects Protective effect against rat colon carcinogenesis Protective effect by reducing pulmonary harm induced by cigarette smoke Inhibition of adenocarcinoma cells of HT- 29 human colon

Pulp Pulp pulp pulp

Antiproliferative activity by brain glioma cells and MDA-468 human breast cancer cells Antiproliferative activity and pro-apoptótica against HL-60 cells responsible for leukemia Antinociceptive effect Atheroprotective effect

Pulp Flowers and pulp Pulp Pulp Root

Hypocholesterolemic effect Inhibition of nitric oxide production from RAW 264.7 cells in culture stimulated with bacterial lipopolysaccharide (LPS) and interferon-alpha (IFN-alpha) Reductions in lipid peroxidation during oxidative stress and cellular protection from reactive oxygen species in humans Antioxidant capacity in plasma Immunomodulatory activity

Lichtenthaler et al. (2005), Hassimotto et al. (2005), Schauss et al. (2006a) and Rufino et al. (2011) Chin et al. (2008) and Spada et al. (2009) Matheus et al. (2003) and Matheus et al. (2006) Poulose et al. (2012) Rocha et al. (2007) Xie et al. (2011) Ribeiro et al. (2010) Fragoso et al. (2012), Fragoso et al. (2013) Moura et al. (2011) and Moura et al. (2012) Pacheco-Palencia et al. (2008) and PachecoPalencia and Talcott (2010) Hogan et al. (2010) Del Pozo-Insfran et al. (2006) Marinho et al. (2002), Favacho et al. (2010) Souza et al. (2010), Sun et al. (2010) and Feio et al. (2012) Souza et al. (2012) Matheus et al. (2003)

Root Seed

Antiplasmodial activity Antioxidant activities against the oxidation of linoleic acid and free radical-scavenging

Mertens-Talcott et al. (2008) Desmarchelier et al. (1997) and Deharo et al. (2004) Jensen et al. (2002) Choi et al. (1998) and Rodrigues et al. (2006)

Pulp Pulp Root

Free radical-scavenging and antioxidant capacity by cellular models Potential anti-inflammatory effects Cytotoxic and antioxidant activity

Kang et al. (2012) Kang et al. (2012) Galotta et al. (2008)

E. precatoria

effects. Thus, although the literature about E. precatoria remains limited, many studies, involving antioxidant activity, anti-inflammatory, characterization and reaction mechanisms of E. precatoria, are likely to emerge in the coming years. 4.2.2. E. oleracea pulp: in vitro assay Among the activities under study, the antioxidant and antiinflammatory effects are the most commonly reported. Assessments of the significant antioxidant capacity of acai pulp in free radicals have been published. Results show a high antioxidant activity against the DPPH radical, anion superoxide, peroxyl radical, hydroxyl radicals and inhibition of oxidation of liposomes (Hassimotto, Genovese, & Lajolo, 2005; Lichtenthaler et al., 2005; Rufino, Alves, Fernandes, & Brito, 2011; Schauss et al., 2006a). In comparison with fifteen samples of pulps from Amazonian fruits (abiu, acerola, acai, arassa-boi, bacaba, bacuri, buriti, caja, cajarana, cupuassu, cashew, graviola, murici, noni and tamarindo), the acai pulp showed the best results for retention capacity of the ABTS radical, and also for the amounts of ascorbic acid and total phenols remaining high compared with standards (Canuto, Xavier, Neves, & Benassi, 2010). 4.2.3. E. oleracea pulp: cell assays To evaluate the antioxidant capacity, the combination of both chemical and cell-based assays provides a useful approach to explain the mechanisms involved with the activities found and possible behavior during in vivo assays. Combination of assays has been conducted. In cellular models, E. oleracea pulp showed antioxidant activity in the cerebral cortex, hippocampus and cerebellum of rats treated with the oxidant hydrogen peroxide (H2O2), suggesting a positive contribution to the development of age-related neurodegenerative diseases (Spada et al., 2009). The extracts of this species were able

Jensen et al. (2008)

to inhibit nitric oxide production and iNOS expression from cell culture (Matheus et al., 2003, 2006). Among these biological evaluations, antioxidant effects have been the most frequently investigated and the key constituents have been described. In a work by Chin, Chai, Keller, and Kinghorn (2008), bioactivity-guided fractionation of E. oleracea (acai) fruit extracts led to the isolation of bioactive compounds, where dihydroconiferyl alcohol, (+)-lariciresinol, (+)-pinoresinol, (+)-syringaresinol, and protocatechuic acid methyl ester exhibited cytoprotective activity in cultured MCF-7 cells stressed by H2O2. In a cell-based assay, procatechuic methyl ester was found to be the most cytoprotective compound (74%), comparable to the positive control used, quercetin (60%). Dihydroconiferyl alcohol, protocatechuic methyl ester, chrysoeriol, and dihydrokaempferol showed antioxidant effects (IC50 0.91, 1.1, 1.4, and 2.7 lg/ml, respectively) in hydroxyl radical-scavenging assay. Nine lignans of the aryltetrahydronaphthalene, dihydrobenzofuran, furofuran, 8-O-40 neolignan, and tetrahydrofuran structural types showed antioxidant activity in vitro in hydroxyl radical-scavenging assay (IC50 < 2.7 lg/ml). The pulp showed effective reduction of oxidative damage and inflammation in brain cells, being an effective intervention to reduce the incidence of age-related neurodegenerative disorders. The effects of different fractions of acai pulp were tested on BV-2 microglial cells subjected to LPS-induced insults, through the measurement of oxidative- and inflammatory-stress-induced signals, including nitric oxide (NO) release, and levels of inducible nitric oxide synthase (iNOS), cyclooxygenase-2 (COX-2), mitogen-activated protein kinase (MAPK), tumor necrosis factor a (TNFa), and nuclear factor jB (NF-jB) (Poulose et al., 2012). Recently, extracts from acai pulp have been correlated with a reduction in the risk of heart diseases. Rocha et al. (2007) observed that extracts from acai induced a vasodilator effect in the rat

K. K. d. L. Yamaguchi et al. / Food Chemistry 179 (2015) 137–151

mesenteric vascular bed and they suggested the possible use of extracts of E. oleracea in the treatment of cardiovascular diseases. A study by Xie et al. (2011) reported indication that acai juice protects against atherosclerosis in a hyperlipidemic-deficient model and has an athero-protective effect and that this is, in part, due to reduced lipid peroxidation and it may also exert a protective effect against the development of atherosclerosis by inhibiting proinflammatory cytokines by regulating inflammatory mediators. Another disease involved with reactive species and free radicals is cardiotoxicity which is caused by the generation of reactive oxygen species (ROS). The antigenotoxic effects of acai pulp were also investigated against DXR-induced micronuclei and DNA damage in mice. The results showed that acai pulp administered by gavage were not genotoxic in mouse bone marrow or liver and kidney cells in the micronucleus test and comet assay. This pulp also played a role in inhibiting the genotoxicity induced by the antitumoral agent DXR with protective effects (Ribeiro et al., 2010). According to some authors, fruits rich in polyphenols, e.g. acai, are categorized as chemopreventive agents because they can quench or prevent the formation of reactive oxygen and nitrogen species that can drive genetic mutations, genomic instability and ultimately carcinogenesis in different target organs (Kang et al., 2011). Recent studies have shown that the acai berry can be an antitumor agent by protecting the injured tissue and the carcinogenic activity. The mechanism of action is still unknown; however, several studies are underway and preliminary results are reported in the literature. Fragoso, Prado, Barbosa, Rocha, and Barbisan (2012) showed that acai fruit inhibits the transitional cell carcinoma development in male Swiss mice, probably due to its potential antioxidant action. Fragoso, Romualdo, Ribeiro, and Barbisan (2013) confirmed the potential of this fruit, demonstrating that, when fed at the concentration of 5.0%, the dried pulp fruit significantly attenuated DMHinduced early and late colon carcinogenesis in male rats. This study indicates that acai has a potential protective effect against rat colon carcinogenesis, using aberrant crypt foci (ACF) formation and tumor development as the end-points. Another study suggests that addition of a hydroalcoholic extract of acai berry to cigarettes may reduce pulmonary damage induced by cigarette smoke with a protective effect, against emphysema in mice, likely due to the reduction of the oxidative process and inflammatory reactions (Moura et al., 2011). More recent results have confirmed these data, showing that the inflammatory process and oxidant actions of cigarette smoke reduced oxidative stress and TNF-a expression (Moura et al., 2012). Acai oil shows a significant influence on cell proliferation. A study reported that a non-anthocyanin polyphenolic fraction from the acai pulp extract inhibited proliferation of HT- 29 human colon adenocarcinoma cells (Pacheco-Palencia et al., 2008). Anthocyanins have also presented promising results. The antiproliferative activity of the anthocyanin fractions was evaluated in HT-29 human colon adenocarcinoma cells. The monomeric fractions (0.5–100 lg cyanidin-3-glucoside equivalents/ml) presented a proliferation inhibition of up to 95.2%, using HT-29 colon carcinoma cells and the polymeric anthocyanin fractions (0.5–100 lg cyanidin-3-glucoside equivalents/ml) induced up to 92.3% inhibition (Pacheco-Palencia & Talcott, 2010). The anthocyanin-rich extract also showed antiproliferative activity against C-6 rat brain glioma cells and MDA-468 human breast cancer cells (Hogan et al., 2010). In addition, the extract had no effect on the growth of MDA-468 human breast cancer cells, suggesting that it may specifically target C-6 glioma cells and the DNA results indicated that acai induces apoptosis in C-6 glioma cells. In another study by Del Pozo-Insfran, Percival, and Talcott (2006), the antiproliferative and pro-apoptotic induction activity of acai polyphenolics against HL-60 cells causing leukemia, was

141

elucidated. The mechanism described was based on caspase-3 activation in a dose- and time-dependent manner. Furthermore, in other studies, it was shown that E. oleracea has an antinociceptive effect, reducing up to 50% of the number of writhings (Favacho et al., 2010; Marinho et al., 2002). Studies have been performed in order to prove that the consumption of acai improves the lipidic profile with an atheroprotective effect, promoting an improvement in the markers of metabolic disease. High levels of total and non–high-density lipoprotein (HDL) cholesterol (HDL-C) in the serum, and the atherogenic index of rats fed a hypercholesterolemic diet, were reduced after diet enrichment with acai pulp (Souza, Silva, Silva, Oliveira, & Pedrosa, 2010). In others’ works, this hypothesis was confirmed, with the addition of 2% of acai to the food leading to an increase of the lifespan of sod1 RNAi female flies that were fed a high-fat diet compared with nonsupplemented control flies. Furthermore, acai administration decreased the transcript level of phosphoenol-pyruvate carboxykinase (Pepck), a key enzyme controlling gluconeogenesis (Sun et al., 2010). The long-term administration of acai seed extract protected C57BL/6J mice fed a high-fat diet that was designed to promote the phenotypic and metabolic characteristics of metabolic syndrome (Souza et al., 2010). Acai juice had atheroprotective effects in hyperlipidemic apolipoprotein E-deficient mice fed a high-fat diet and markedly improved the lipid profile and attenuated atherosclerosis in New Zealand rabbits fed a cholesterol-enriched diet (Feio et al., 2012). Souza et al. (2012), demonstrated that the ingestion of acai pulp improved the lipid profile in various animal models by modulating the expression of the genes involved in cholesterol homeostasis in the liver and increased fecal excretion, thus reducing serum cholesterol. They suggested that acai pulp promoted a hypocholesterolemic effect in a rat model of dietary-induced hypercholesterolemia through an increase in the expression of ATP-binding cassette, subfamily G transporters, and LDL-R genes. 4.2.4. E. oleracea pulp: in vivo studies Due the antioxidant and anti-inflammatory properties of the acai pulps, scientific studies with isolated components are being conducted to identify those responsible for the biological activities found. In the study performed by Kang et al. (2011), five compounds were isolated and they were tested for anti-inflammatory and antioxidant activities. The flavone velutin showed excellent anti-inflammatory capacity in mouse macrophages, indicating a potential athero-protective effect. This anti-inflammatory potential was confirmed by inhibiting the expression of proinflammatory cytokines (Xie et al., 2012). The health benefits of acai pulp consumption have been demonstrated in humans, in a randomized, doubleblind, placebo-controlled, crossover study, with healthy subjects from 19 to 52 years of age administered an acai pulp-rich juice in which the pulp had not been clarified or filtered. The study reported significant reductions in lipid peroxidation during oxidative stress, as well as a rapid increase in antioxidant activity in the serum, increasing cellular protection from reactive oxygen species, as measured by the cell-based antioxidant protection in erythrocytes (CAP-e) assay (Jensen et al., 2008). In a study with human volunteers, consumption of juice and pulp caused an increase of two to three times the antioxidant capacity in plasma. Results demonstrated the absorption and antioxidant effects of anthocyanins in acai, in plasma, in a critical human consumption trial (Mertens-Talcott et al., 2008), proving the beneficial effects of acai-based beverage consumption. 4.2.5. E. oleracea: biological activities of other Euterpe palm tree parts Scientific studies showed that root extracts have antioxidant activities (Desmarchelier, Repetto, Coussio, Llesuy, & Ciccia,

142

K. K. d. L. Yamaguchi et al. / Food Chemistry 179 (2015) 137–151

1997) and immunomodulatory activity, using complement cascade inhibition, confirming the traditional anti-inflammatory activity and the inhibition of the complement cascade, as well as the cyclo-oxygenase pathway inactivation (Deharo, Baelmans, Gimenez, Quenevo, & Bourdy, 2004). Jensen, Kvist, and Christensen (2002) proved the antiplasmodial activity of the ethyl acetate extract of comminuted roots and their lignin constituent. The extracts of fruits and flowers from E. oleracea were able to inhibit the production of nitric oxide from RAW 264.7 cells in culture stimulated with bacterial lipopolysaccharide (LPS) and interferon-alpha (IFN-alpha), thus confirming the activity described by the population for the anti-inflammatory activity (Matheus et al., 2003). It is well known that nitric oxide and free radicals are present in inflammatory processes and monitoring is used as a tool to analyze substances having anti-inflammatory activity. Free radicals liberated from phagocyte cells are important in inflammatory processes because they are implicated in the activation of nuclear factor jB (NF-jB), which induces the transcription of inflammatory cytokines and COX-2. Hence, the free radical inhibition is an indication of the anti-inflammatory action mechanism. In a study on the antioxidant activities of extracts from tropical and oriental medicinal plants, E. oleracea seed extracts showed strong antioxidant activities against the oxidation of linoleic acid, as well as a potent scavenging capacity against DPPH radicals and superoxide anion (Choi et al., 1998). The extracts of seeds were tested in three other radical species (peroxyl radicals, peroxynitrite and hydroxyl radicals). The extracts exhibit good antioxidant capacity against peroxyl radicals, similar to that obtained by the pulp extracts. The antioxidant capacity against peroxynitrite and hydroxyl radicals is even higher. The main antioxidants identified by chromatographic methods are five different procyanidins (di- through pentamers), while protocatechuic acid and epicatechin were identified as minor compounds. According to the authors, these are the compounds responsible for the high antioxidant activity detected (Rodrigues et al., 2006). The pulp accounts for 10% of the final weight, resulting in 85– 95% of waste, which is normally discarded (Pompeu, Silva, & Rogez, 2009; Yuyama et al., 2011). Currently, this by-product has been used as a fertilizer for plants and for the making of natural artcraft jewelries. Some studies suggest its use as a source of fiber as a food additive and also as an energetic source (Silva & Tavares, 2013). The study on the biological activities of seeds has become an opportunity for large-scale use of a raw material that is currently being discarded and that can also generate sustainable biotechnological products.

5. Phytochemical constituents 5.1. Chemical studies of acai pulp Chemically, the fruit berries from E. oleracea and E. precatoria species are characterized by the presence of bioactive substances. About 90 substances have been described, of which approximately 31% consists of flavonoids, followed by phenolic compounds (23%), lignoids (11%) and anthocyanins (9%). Other classes include fatty acids, quinones, terpenes and norisoprenoids. The chemical structures of the compounds mentioned can be seen in Figs. 2–5. There are few studies that attempt to differentiate both Euterpe species. Both have phenolic and anthocyanin contents that correlate with a high biological activity (Kuskoski, Asuero, Morales, & Fett, 2006; Menezes et al., 2008). The amount of anthocyanins in acai pulp is so high that lyophilized samples have been used to obtain isolated standards of cyanidin-3-O-glucoside and cyanidin-3-O-rutinoside (Gouvêa et al., 2012).

Anthocyanins are glycosides of anthocyanidins. They belong to the class of flavonoids and have, in their basic core, the 4-hydroxyflavilium ion. They have been characterized as the responsible compounds for the determination of the color of a variety of vegetables, including the purple color, and also for the antioxidant activity of acai (Del Pozo-Insfran, Brenes, & Talcott, 2004). The chemical structures of anthocyanins found in acai are shown in Fig. 2. Regarding the two species, in the study of Pacheco-Palencia, Duncan, and Talcott (2009), the total content of anthocyanins was 50% higher in E. precatoria than in E. oleracea. Although the amounts of these substances are different for the two species, most of the anthocyanin profiles of the pulps were similar when tested by high performance liquid chromatography (HPLC). Both species were characterized by the predominance of cyanidin-3-glucoside and cyanidin-3-rutinoside. The difference was the presence of pelargonidin-3-glucoside in E. precatoria, and peonidin-3-rutinoside in E. oleracea. Analytical tests were done in order to quantify the amount of anthocyanins in each species. Some of the techniques, such as NMR, require specific reagents and qualified personnel, which limit their application in most laboratories. Dias et al. (2012) were able to remove the lipophilic compounds and perform the quantification of anthocyanins by using a UHPLC–PDA method. Cyanidin-3arabinoside and cyanidin-3-arabinosylarabinoside were reported as major anthocyanin compounds present. It was a faster method (17 min) than other HPLC–UV methods and allowed the separation of 3 other anthocyanins (peonidin-3-glucoside, pelargonidin-3glucoside and peonidin-3-rutinoside), that are dominant in other common fruits. The detection (the first time) of cyanidin-di-O-glycosides was also reported. Inácio, Lima, Lopes, Pessoa, and Teixeira (2013) also achieved a rapid and non-destructive method to determine total anthocyanin compounds, using near-infrared reflectance spectroscopy and multivariate calibration, indicating that the model developed can be used as an alternative to UV–Vis measurement. The main differences in the amounts of anthocyanins reported in acai are also described in other studies. Rogez, Pompeu, Akwie, and Larondelle (2011) determined the kinetics of anthocyanin accumulation during the ripening of the acai fruits to understand the beginning of maturation. Both anthocyanins were present in similar proportions; however, in the last maturation stages, cyanidin-3-glucoside became less abundant than cyanidin-3-rutinoside. Through this work, the importance of selecting the best stage for harvesting in order to achieve an anthocyanin-rich fruit is clear, given that these polyphenols are of great interest and may have different proportions, depending on the time of harvest. Regarding the phenolic profile, in the characterization described by Del Pozo-Insfran et al. (2004), the predominant phenolic acids in descending order in E. oleracea pulp were: ferulic acid, phydroxybenzoic, gallic, protocatechuic, ellagic, vanillic, p-coumaric acids, and ellagic acid glycoside. These compounds were identified by HPLC and mass spectrometry. This profile of phenolic compounds was later confirmed by other studies and, additionally, other substances, e.g. caffeic, benzoic, syringic, chlorogenic acids and resveratrol were also described (see Fig. 3) (Del Pozo-Insfran et al., 2004; Gallori et al., 2004; Gordon et al., 2012; Lichtenthaler et al., 2005; Ribeiro et al., 2010; Rojano et al., 2011). When comparing the chemical profile with E. precatoria, there were similarities regarding p-hydroxybenzoic, vanillic, syringic, ferulic and protocatechuic acids as the major constituents in both species (Pacheco-Palencia et al., 2009). In the fixed oils of E. oleracea there was a similar profile to that described for the pulps, where the major phenolic compounds were gallic acid, cyanidin-3-O-glucoside and cyanidin-3-O-rutinoside. The main difference was the presence of luteolin-C-8 -glucoside

143

K. K. d. L. Yamaguchi et al. / Food Chemistry 179 (2015) 137–151

OH

OH

OH

OH +

HO

+

HO

O

O

OH

OH

O

O OH

OH

O

OH

O

HO

HO

OH

OH OH a,b

cyanidin 3-sambubioside O

OH

OH +

HO

O

O

O

O OH

HO

HO

O

O

CH3

HO

cyanidin 3-rutinoside

a

OH peonidin 3-rutinoside

O

O

CH3

OH OH

a

CH3

OH +

O

HO

OH

OH

OH

OH +

HO

+

HO

O

O

O

O

O OH

O

O

HO OH

OH

OH

O

O

HO

HO

a,b

CH3

OH +

OH

OH

OH

cyanidin 3-glucoside

HO

O

OH

OH

OH

OH OH

OH a

OH

O

HO

HO

OH

cyanidin 3-arabinoside

OH

O

OH

peonidin 3-glucoside

a

pelargonidin 3-glucoside

b

Fig. 2. Anthocyanins detected in acai (E. precatoriaa and E. oleraceab).

(orientin) and luteolin-6-C-glucoside (homo-orientin) in larger quantities than in the work reported by other authors (Silva & Rógez, 2013). The other phenolic flavonoids that have been described are epicatechin, catechin, rutin, orientin, homoorientin, isovitexin, escoparin, deoxyhexose taxifolin, apigenin, crisoeirol, dihydrokaempferol, velutin, 5,40 -dihydroxy-7, 30 ,50 -trimethoxy flavone, luteolin diglycoside and procyanidin dimers (Fig. 4) (Bobbio, Druzian, Abrao, Bobbio, & Fadelli, 2000; Gallori et al., 2004; Del Pozo-Insfran et al., 2006; Kang et al., 2010; Kang et al., 2011; Pacheco-Palencia et al., 2009; Ribeiro et al., 2010; Rojano et al., 2011; Rosso et al., 2008; Schauss et al., 2006b). Another 22 compounds of the fruits from E. oleracea were identified by Chin et al. (2008), including nine lignans (+)-isolariciresinol, (+)-5-methoxy-isolariciresinol, erythro-1-(4-hydroxy-3methoxyphenyl)-2-[4-(3-hydroxypropyl)-2-methoxyphenoxy]-1, 3-propanediol, threo-1-(4-hydroxy-3-methoxyphenyl)-2-[4-(3hydroxypropyl)-2-methoxyphenoxy]-1,3-propanediol, ( )-(7R, 8S)-dihydrodehydroconiferyl alcohol, (+)-(7R,8S)-5-methoxydihydrodehydroconiferyl alcohol, (+)-lariciresinol, (+)-pinoresinol, (+)-syringaresinol, four simple benzenoids: 3-hydroxy-1-(4hydroxy-3,5-dimethoxyphenyl)-1-propanone, 3,40 -dihydroxy-30 methoxypropiophenone, dihydroconiferyl alcohol, protocatechuic acid methyl ester; three flavonoids: chrysoeriol, (2R,3R)dihydrokaempferol, apigenin, a benzoquinone, 2,6-dimethoxy-1,

4-benzoquinone, three monoterpenoids, (+)-menthiafolic acid, (E,Z)-2,6-dimethyl-2,6-octadiene-1,8-diol, (E,E)-2,6-dimethyl-2, 6-octadiene-1,8-diol; and two norisoprenoids: ( )-loliolide and (4R)-4-[(1E)-3-hydroxy-1-butenyl]-3,5,5-trimethyl-2-cyclohexen1-one. Lignans are macromolecules, polymers of basic units of C6-C3 n-propylbenzenes, which are linked by the b carbon by their side chains (C3). They are dimers, formed by oxidative coupling of cinnamyl alcohols to each other or with cinnamic acids. They have diverse biological activities, such as insecticide, antimicrobial and antitumoral. Through the results of these authors, it becomes clear that the biological activities described for acai pulp do not come exclusively from phenolic substances (phenolic acids, flavonoids and anthocyanins). Therefore, these lignoids are included among the antioxidant constituents of acai fruits. The lignoids described for the acai species are illustrated in Fig. 5. In addition, fatty acids from acai have also been reported (Schauss et al., 2006a,b). Linoleic acid, oleic acid and palmitic acid were reported as major poly and monounsaturated fatty acids and also linolenic acid (Schauss et al., 2006a), and quercetin hydroxylmethylglutaryl-rhamnoside (Mulabagal & Calderón, 2012). In a study of the different parts of the seed of E. oleracea, pericarp, endocarp and the whole fruit, the profiles of the chemical composition of the nonpolar compounds were very similar in all

144

K. K. d. L. Yamaguchi et al. / Food Chemistry 179 (2015) 137–151

O

OH

R

O

OH

O

OH

R

OH

O

OH R - H: vanillic acid

p-hydroxybenzoic acid

benzoic acid

R - OCH 3: syringic acid

OH

OH

OH

O

O

OH

OH

OH

O

OH

CH3

3,4'-dihydroxy-3'-

dihydroconiferyl alcohol

HO H3C

OH

O

CH3

OH

protocatechuic acid

methoxypropiophenone

methyl ester

OH

CH3 HO

OH O

O

O CH3

O

R

R - H: coumaric acid R - OH: caffeic acid R - OCH 3: ferulic acid

OH

OCH3

OH

R - OH: gallic acid R - H: protocatechuic acid O

OH

resveratrol OH

lariciresinol O

O

OH O

OH

OH

HO OH

H3C

O

O

O

HO

H3C

CH3

O dihydroconiferyl alcohol

ellagic acid H3C

O OH

CH3

3-hydroxy-1-(4-hydroxy-3,5dimethoxyphenil)-1-propanone

O O

OH

OH

O O

R

OH HO

R O

O OH OH

HO O H3C

R - H: pinoresinol R - OCH 3: syringaresinol

chlorogenic acid

OH

Fig. 3. Phenolic compounds detected in acai (E. precatoria and E. oleracea).

of them. No chemical differences were observed regarding fatty acid compositions when these three extracts were analyzed (Mantovani, Fernandes, & Menezes, 2003). There was a predominance of the unsaturated forms, including mostly: oleic acid (45.1%, 45.7%, 45.5% for pericarp, endocarp and whole fruit, respectively), followed by palmitoleic acid to a lesser extent (4.2%, 4.8%, 4.3% for pericarp, endocarp and whole fruit, respectively). These acids accounted for more than 50% of the total fatty acids analyzed in the samples. The lipid profiles of both species of the acai reinforce the idea that this food is a source of monounsaturated fatty acids, mainly oleic, and it also contains considerable amounts of essential fatty acids, e.g. linoleic and linolenic acids. This is a positive result because stud-

ies have shown the impact of these fatty acids in reducing total cholesterol, LDL-cholesterol (low density lipoprotein) and blood triacylglycerols, without changing HDL cholesterol (high density lipoprotein) and VLDL (very low density lipoprotein) (Lima, Menezes, Tavares, Szarfac, & Fisberg, 2000; Yuyama et al., 2012). According to Rogez (2000), acai oil, just like olive and avocado oil, is rich in monounsaturated and polyunsaturated fatty acids, respectively (60% and 14% of its composition). In E. precatoria, the main fatty acids found in fruit juice are: oleic acid (18:1) with an average concentration in the order of 68.2%, followed by 17.5% of palmitic acid (16:0). With regard to polyunsaturated fatty acids, linolenic acid (18:2, 7.5%) and linoleic acid (18:3, 1.7%) were the main compounds (Yuyama et al., 2012). The results were similar

145

K. K. d. L. Yamaguchi et al. / Food Chemistry 179 (2015) 137–151

OH HO

OH

O

HO

O

O

OH

O

OH

O

OH

R - H: dihydrokaempferol R - OH: taxifolin

chrysoeriol

HO

OH

OH HO

O

O

OH

OH

OH

OH

OH

OH

OH

(-)-epicatechin

O

quercetin

(+)-catechin

OH

OH HO

O

O OH

OH O

O OH

OH

OH

O

HO

O

apigenin

OH HO

O

HO

R

CH3 OH

OH

OH

OH

O

O

HO

OH O

O H3C

OH

OH OH

OH

astilbin quercetin arabinopyranoside

OH OH

H3C

O

O

HO

O OH O

O

OH

OH

O

OH HO

OH OH

CH3

OH OH

OH OH

O

OH

quercetin rhamnoside

OH

protoanthocyanidin

OH OH HO

O OH

HO

O

CH3

OH

OH

OH

OH

O

OH OH

O

O OH OH OH

procyanidin dimeric

O OH

O

OH

O OH HO

OH OH

quercetin rutinoside

Fig. 4. Flavonoids detected in acai (E. precatoria and E. oleracea).

to those found by Nascimento, Couril, Antoniassi, and Freitas (2008) with monounsaturated in the range of 68–71%, and polyunsaturated 7.7–10.6%. Nascimento et al. (2008), using enzymatic extraction, demonstrated the composition of the lipid fraction of E. oleracea, comprising about 71% of unsaturated fatty acids, 60.8% monounsaturated and 10.4% of poly-unsaturated. These results are of great interest for the functional food markets, since these figures are recommended for the prevention of cardiovascular diseases. These facts explain the nomenclature of the species, being ‘‘oleracea’’, originating the word ‘‘oil’’, which means the fruit is rich in oil, since unsaturated fatty acids are more fluid than are saturated fatty acids.

Small amounts of carotenoids, e.g. b-carotene, a-carotene, lutein and a-tocopherol, were detected in E. oleracea pulp (Costa, Ballus, Teixeira, & Godoy, 2010; Ribeiro et al., 2010). According to Darnet, Serra, Rodrigues, and Silva (2011), acai pulp is rich in tocopherols (a-, b-, c- and d-tocopherol), confirming the nutritional properties of acai with the presence of vitamin E (394 lg g 1 dry matter of a-tocopherol). The major components found in acai pulp can be detected through chemical fingerprinting and mass profiling methods. Mulabagal and Calderón (2012) achieved the fingerprinting of extracts of E. oleracea and 40 components were detected using liquid chromatography coupled with mass spectrometry with an

146

K. K. d. L. Yamaguchi et al. / Food Chemistry 179 (2015) 137–151

OH

R O

HO

OH

CH3 O

OH

HO

HO

O

CH3

HO

O

O

R

O OH

HO OH

O

OH

O

R - H: isovotexin

OH

R - OH: homoorientin

R - OCH 3: scoparin R - OH: orientin

OH HO

OH HO

O

CH3 O

O

O

OH OH

O

OH

O O

OH HO

O

H3C

OH

OH OH

OH

isoorientin

kaempferol rhamnoside

OH

OH HO

HO

OH O

O

OH

HO

O

HO

O

OH

O

O

O O

CH3

HO OH

HO OH

O vitexin OH

HO

OH

OH OH kaempferol rutinoside

OH OH

O OH HO

O

O OH

OH

O

O

O H3C

O

OH

O

OH O

OH HO

OH HO

O

OH

OH OH

OH rutin

quercetin 3-glucoside Fig. 4 (continued)

efficient separation of fatty acids, non-anthocyanin polyphenols and anthocyanins in assai raw materials. Combined chemical techniques have been useful and provide knowledge of the chemical composition of samples of acai, assisting in the identification of the species, since both have peculiarities of chemical composition, as well as detection of adulteration of food products originating from these species. Several tests have been studied, not only to identify, but also to quantify the acai organic components. Mass spectrometry with inductively coupled plasma MS (ICP-MS) was used for the determination of metal concentrations, since its low detection limit allows for the differentiation of closely related species. This technique has

been reported for studies attempting to segregate fruits by region or distinguish similar fruits from each other. Santos, Nardini, Cunha, Barbosa, and Teixeira (2014) investigated the differentiation of acai (E. oleracea) and juçara fruits (E. edulis), using the ICP-MS technique and linear discriminant analysis to assess claims of origin and also for other purposes. It was used to correctly differentiate acai, and the authors suggested that this test can be used as a prerequisite for commercialization, quality control and authentication as different batches of fruit might have different concentrations due to the origins of their raw materials. Thus, future analyses, such as these, can also be used to differentiate species of E. precatoria and E. oleracea.

147

K. K. d. L. Yamaguchi et al. / Food Chemistry 179 (2015) 137–151

CH3 O

OH

OH

CH3

O O

OH HO

OH

R

HO

O OH

O

CH3

OH

H3C erytro and threo-1-(4-hydroxy-3-methoxyphenyl)-

R - H: isolariciresinol

2-[4-(3-hydroxypropyl)-2-methoxyphenoxy]-1,3-propanediol

R - OCH3: 5-methoxyisolariciresinol

OH

OH

OH

O

CH3 OH

R O

O

O HO

H3C

HO

O

O

H3C

H3C

lariciresinol

R - H: dihydrodehydroconiferyl alcohol R - OCH3: methoxydihydrodehydroconiferyl alcohol

O

CH3 OH

OH O

O

O

O CH3

CH3

CH3

CH3

O

O

O

O HO

HO

O

pinoresinol

syringaresinol

H3C

O OH

CH3 O

HO

CH2

O

CH3

CH3

CH3

CH3

HO

O

CH3

CH3

CH3

CH3

3-Hydroxy-1-butenyl-3,5,5-trimethyl-2-cyclohexen-1-one

loliolide

menthiafolic acid O

OH

CH3

O O

O

O

CH3

H3C CH2

HO O benzoquinone

OH

CH3

O 2,6-dimethoxy-1,4,benzoquinone

menthiafolic acid O

OH

R OH

CH3 HO HO

CH3

2,6-Dimethyl-2,6-octadiene-1,8-diol

O H3C R - H: 3-hydroxy-1-(4-hydroxy-3,5-dimethoxyphenyl)-1-propanone R - OCH 3: 3,4'dihydroxy-3'-methoxypropiophenone

Fig. 5. Lignoids and other compounds detected in acai (E. precatoria and E. oleracea).

148

K. K. d. L. Yamaguchi et al. / Food Chemistry 179 (2015) 137–151

7. Applications

erages, concentrated juices, frozen fruit pulps, isotonic drinks, lyophilized pulp and oils for pharmaceutical purposes (PachecoPalencia, Hawken, & Talcott, 2007a; Pacheco-Palencia, Hawken, & Talcott, 2007b; Sabbe et al., 2009; Schauss, 2010). The acai juice is obtained by mechanical extraction, either by machines or manually. Traditionally, the preparation of this beverage is done in two steps: during the first step, the fruits are immersed in warm water, and in the second step, the pulp is removed, using proper machinery and using water (Nogueira, Figueirêdo, & Muller, 2005; Rogez, 2000). Depending on the amount of water used during the extraction process, the beverage is classified according to the regulation of the Ministry of Agriculture, Fishery and Supply. It is classified according to the addition or absence of water and its derivatives as: (I) Acai pulp (no water added), (II) Special acai or thick acai (Type A) (more than 14% of total solids), (III) Regular or medium acai (Type B) (from 11% to 14% total solids), and (IV) Thin acai or popular acai (Type C) (between 8% and 11% total solids). When the pulp is removed without the addition of water, the whole acai pulp is obtained, which may contain at least 40% total solids. This method of production has been used mostly for research purposes and is directed to markets located far away from the production centers. However, none of the commercially available machines used to remove the pulp is able to efficiently process the fruit without the addition of water (Nogueira et al., 2005; Rogez, 2000). The search for quality standardization of this product is related to the increase in the consumption of acai in large urban national and international centers (Pagliarussi, 2010). Besides its traditional form of consumption, acai pulp is also used for industrial and traditional manufacturing of ice-creams, soft-creams and jams. In recent years, several other ways of using this product are being introduced in the market, for example, pasteurized acai, acai with guarana syrup, powdered acai, condensed milk with acai, jam and acai liquor. The prospects of using this fruit as a natural color additive are significant and also important as an ingredient for energetic soft drinks. This makes the acai a relevant commercial product for countries in Europe and North America (Alexandre & Cunha, 2004; Heinrich et al., 2011; Homma, Maia, & Nicoli, 2006; Pagliarussi, 2010). In other regions of Brazil, e.g. the mid-west, south, southeast and northeast the normal acai consumption is different from that of the Amazon region. In the estate of Para, acai is normally eaten as a main meal, or as a beverage, either simple or mixed with tapioca flour, with or without sugar. In other places, acai is normally eaten mixed with guarana syrup and with other fruits, e.g. banana, orange, strawberry, pineapple, mango, passion-fruit, avocado and kiwi (Menezes et al., 2008; Pagliarussi, 2010). The demand for acai is increasing nationally, mostly in the midsouth region, in the estates of Rio de Janeiro and São Paulo, and the typical consumers are defined as: a young ‘‘healthy-generation’’ that are attracted by the high caloric, medical and nutritional properties of this beverage (Rogez, 2000). Soft beverage industry has made significant progress during the last two decades in terms of rise in production and consumption; however, there is a limited range of fruit juice-based RTS beverages available in the world market. Looking to the fast-growing market segment of functional beverages, it appears appropriate to use the acai extract as a natural flavouring agent in the development of whey-based RTS (Ready To Serve) beverage from acai juice to reach the higher market demand (Balaswamy, Rao, Nagender, & Satyanarayana, 2011; Boghani, Raheem, & Hashmi, 2012).

7.1. The beverages from acai and other by-products

7.2. Biocosmetics and cosmetology

From the juice obtained from the acai fruits, several by-products are produced industrially and in research, mostly bottled bev-

The acai berry has been widely studied and used, applied as an antioxidant in anti-aging formulas, as well as in the treatment and

5.2. Chemical constituents from other parts of the palm tree: roots, leaves and flowers Other plant parts of the E. precatoria species studied were leaves and roots. In the roots, the isolation of p-hydroxybenzoic acid and dihydrodiconiferyl dibenzoate lignin was described (Jensen et al., 2002). In the study of Galotta and Boaventura (2005), using the roots and stalks of the leaves, compounds, such as stigmast-4-en6b-ol-3-one, sitosterl 3b-OD-glucopyranoside, sitosteryl palmitate, b-sitosterol and stigmasterol mixtures, a - b-amyrin, lupeol, friedelin-3-one, 28-hydroxy-friedelin-3-one and a- and b-D-glucose, were isolated. Besides these substances, other studies report that p-hydroxybenzoic acid and the flavonoids quercetin, catechin, epicatechin, rutin and astilbin, were also isolated, with a strong retention capacity of the free radical DPPH and low cytotoxicity (Galotta, Boaventura, & Lima, 2008). Besides the presence of phenolic substances, there are several other classes of substances that are of great industrial interest, such as terpenes and isoprene and benzophenones, making the species of acai, an important biotechnological source (Fig. 5). 6. Nutritional composition and other considerations about the Acai fruit and its beverages The acai berry has many essential properties important in human nutrition. It is a source of energy, fiber, anthocyanins, minerals and fatty acids. For this reason it is considered to be a functional food, helping the prevention of several degenerative diseases (Pacheco-Palencia & Talcott, 2010; Rosso et al., 2008; Yuyama et al., 2011). In literature reports most papers on nutritional value are related to the species E. oleracea. Several studies show that, for both species, the acai juice is mainly considered as an energetic drink. The lipids account for 70–90% of the total calories found in the juice. The high content of lipids gives the acai juice an energetic value more than twice that found in milk (50 kcal/100 ml) (Crozier et al., 2011; Rogez, 2000; Rufino et al., 2010; Souza et al., 2010). Several studies have presented works with the characterization of acai from E. oleracea regarding its nutritional composition. The main constituents found in dry matter are lipids (50%), fibers (25%) and proteins (10%). Acai is a highly caloric food given its high amounts of lipids, its main constituent. Lipids represent just about 90% of the total calories present in the acai juice which are present as the acai oil. Hence, the consumption of this fruit provides a good intake of mono- and poly-unsaturated fatty acids. A liter of acai contains 12.6 g of protein, representing 25–30% of the recommended daily intake. Regarding the amino acid profile, just like in the egg, methionine is the first-limiting amino acid (chemical index 60%), and the second-limiting amino acid is lysine, with an excess of phenylalanine and threonine. The amount of carbohydrates (glucose, fructose and sucrose) is relatively low, between 2.96% and 3.55% of total day matter. Acai is also a good source of inorganic compounds, such as phosphorus, sodium, zinc, iron, manganese, copper, boron, chromium, calcium, magnesium, potassium and nickel (Costa et al., 2013; Rogez, 2000; Rufino et al., 2010; Souza et al., 2010). The inconsistencies within the results published are probably due to the industrial processing of the pulp, but another reason could be the high genetic variability within these species (Menezes et al., 2008).

K. K. d. L. Yamaguchi et al. / Food Chemistry 179 (2015) 137–151

prevention of cutaneous disorders (Frasson & Canssi, 2008; Spada et al., 2009; Youdim, Martin, & Joseph, 2000). According to Herculano (2013), some examples of cosmetic products, using acai (E. oleracea Mart.), are shampoos, conditioners, anti-wrinkle creams, hydrating body milk and foot creams. The author also made an enquiry on the number of companies that produce cosmetics in an industrial way using the acai fruit, and this revealed the existence of 27 Brazilian companies and 7 international companies, making a total of 34. He also noted that some of the positive aspects linked to the produced cosmetics, according to the manufacturers, are related in the popular knowledge of the Amazonian people. The use of acai extracts and oils is found in shampoos, conditioners, hair creams and hydrating body milks, focussing on hydration and promoting the improvement in hair structure and conditioning. The high levels of anthocyanins found in the acai fruits may be useful in the prevention and treatment of cutaneous disorders (Herculano, 2013; Pacheco-Palencia et al., 2009). Up to this moment there is no optimized technology for the acai oil extraction, even though it has been already used in the formulation of cosmetics. The commercial method used for the extraction applies the pressing of the fruits with conditions adapted from other raw materials from oil seeds, with yields below 50%. Research studies (on laboratory scale) suggest the use of enzymes for the aqueous acai oil extraction obtained from the commercially available pulp (Nascimento et al., 2008).

7.3. Pharmaceutical and functional applications Within the pharmaceutical industry there are a number of products that contain acai in their formulations. In its majority, the pulp of E. oleracea is used as an additive due to its high antioxidant activity, leading to an increased product shelf life. In a study performed by Clewell et al. (2010), the analysis of a pharmaceutical product named 112 Degress™, reveals that it contains in its formulation the following ingredients: amino acid L-tyrosine; and the herbs E. oleracea fruit, Tribulus terrestres seed extract, Panax ginseng root extract, Butea superba root and Pueraria mirifica root. The article demonstrates that the drug (for erectile dysfunction) works on rats and shows no toxicological issues. According to Córdova-Fraga et al. (2004), the acai may also be used as a contrast agent for magnetic resonance examination of the gastrointestinal tract. The authors detected the presence of metals, e.g. iron, manganese and copper, in the acai. Comparative tests were performed using metal solutions, water and a commercially available contrast agent, and they found a good comparison between the contrast produced from acai and that of the commercial product with the advantage that acai does not have any collateral effects. The ingestion of acai enhanced the contrast and increased the examination definition in the stomach, in tests done with humans, ensuring its potential for clinical applications. The rheological properties of the dehydrated acai pulp are another important aspect that has been gaining more attention in the functional by-products market of dehydrated acai products (Carneiro, Silva, Figueiredo, Sousa, & Maia, 2012). The is very significant because the acai pulp has been submitted to a dehydration process, which is not only being used as a preservative method, preventing food decay and a loss in the market value, but also increases the product benefits (Carneiro et al., 2012; Tonon, Alexandre, Hubinger, & Cunha, 2009). The acai main product obtained by dehydration, generally using a lyophilization process, is the acai powder or lyophilized acai, which is, later applied in the formulation of several food supplements. These products may come in the shape of tablets, capsules or as energetic drinks, but also as additive for beverages, concen-

149

trated juices, and yogurt, and as individual sachets (Carneiro et al., 2012; Vandresen, Quadri, Souza, & Hotza, 2009). According to Bobbio et al. (2000), acai may be used as a rawmaterial for the preparation of natural color additives given the fact that its aqueous extracts do not show any toxic effects and it has a high content of anthocyanins. Constant (2003) developed an extraction method specific for the removal of anthocyanins of acai; the color additive was prepared with maltodextrin and bcyclodextrin; the solution was dried, using a spray-drier and lyophilization. This color additive was applied in yogurt, petit Suisse type cheese, isotonic drink and as a powder. For comparison purposes, it was used as a commercially available color additive with anthocyanins from grapes. Among all the tested food products with the color additive from acai, the only product that was not suitable for this application was the isotonic drink due to the considerable anthocyanin degradation therein. The color additive prepared from acai was more efficient in comparison with the color additive from grapes because the color was stable for a longer period. The food industry also uses acai in the composition of many byproducts, for example: gelatine capsules, powders to be used as shakes, teas, juice and pulp, powders divided in bags to use in shakes, ready-made soups, and liquid phytotherapic products, such as teas and infusions (Costa et al., 2013). Acknowledgments This study was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), FAPEAM and CAPES. References Alexandre, D., & Cunha, R. L. (2004). Conservação do açaí pela tecnologia de obstáculos. Ciências e Tecnologia em Alimentos, 24(1), 114–119. Balaswamy, K., Rao, P. P., Nagender, A., & Satyanarayana, A. (2011). Preparation of sour grape (Vitis vinifera) beverages and evaluation of their storability. Journal of Food Processing and Technology, 2, 1000116. Bobbio, F. O., Druzian, J. I., Abrao, P. A., Bobbio, P. A., & Fadelli, S. (2000). Identification and quantification of anthocyanins from the acai fruit (Euterpe oleracea) Mart. Ciência e Tecnologia de Alimentos, 20, 388–390. Boghani, A. H., Raheem, A., & Hashmi, S. I. (2012). Development and storage studies of blended papaya–aloe vera ready to serve (RTS) beverage. Journal of Food Processing and Technology, 3, 1000185. Bourdy, G., Dewalt, S. J., Michel, L. R. C., Roca, A., Deharo, E., Muñoz, V., et al. (2000). Medicinal plants uses of the Tacana, an Amazonian Bolivian ethnic group. Journal of Ethnopharmacology, 70, 87–109. Bovi, M. L. A., & Castro, A. Assaí. In: Clay, J.W. & Clement, C.R. (Eds.) (1993). Selected species and strategies to enhance income generation from amazonian forests. Roma: Food and Agriculture Organization of the United Nations, 58–67. Brian, M. B. (1998). Ethnobotany of the Chacobo Indians and their Palms. Advanced in economic botany. New York: The New York Botanic Garden. Canuto, G. A. B., Xavier, A. A. O., Neves, L. C., & Benassi, M. T. (2010). Physical and chemical characterization of fruit pulps from Amazonia and their correlation to free radical scavenger activity. Revista Brasileira de Fruticultura, 32, 1196–1205. Carneiro, A. P. G., Silva, L. M. R., Figueiredo, R. W., Sousa, P. H. M., & Maia, G. A. (2012). Efeito da Temperatura no Comportamento Reológico de Pó de Açaí (Euterpe oleracea) Reconstituído. UNOPAR Científica Ciências Biológicas e da Saúde, 14, 241–245. Chin, Y. W., Chai, H. B., Keller, W. J., & Kinghorn, A. D. (2008). Lignans and other constituents of the fruits of Euterpe oleraceae (acai) with antioxidant and cytoprotective activities. Journal of Agricultural and Food Chemistry, 56, 7759–7764. Choi, W. S., Lee, S. E., Lee, H. S., Lee, Y. H., & Park, B. S. (1998). Antioxidative activities of methanol extracts of tropical and oriental medicinal plants. Han’guk Nonghwa Hakhoechi, 41, 556–559. Clewell, A., Qureshi, I., Endres, J., Horváth, J., Financsek, I., Neal-Kababick, J., et al. (2010). Toxicological evaluation of a dietary supplement formulated for male sexual health prior to market release. Regulatory Toxicology and Pharmacology, 57, 55–61. CONAB – COMPANHIA NACIONAL DE ABASTECIMENTO. Política de garantia de preços mínimos. Disponível em: . Acesso em: May 4th, 2014. Constant, P. B. L. (2003). Extração, caracterização e aplicação de antocianinas de açaí (Euterpe oleracea, M.). Doctor Scientiae em Ciência e Tecnologia de Alimentos) – Universidade Federal de Viçosa, Viçosa, MG. 183p.

150

K. K. d. L. Yamaguchi et al. / Food Chemistry 179 (2015) 137–151

Córdova-Fraga, T., de Araujo, D. B., Sanchez, T. A., Elias, J., Jr., Carneiro, A. A., BrandtOliveira, R., et al. (2004). Euterpe oleracea (Açaí) as an alternative oral contrast agent in MRI of the gastrointestinal system: Preliminary results. Magnetic resonance imaging, 22, 389–393. Costa, A. G. V., Garcia-Diaz, D. F., Jimenez, P., & Silva, P. I. (2013). Bioactive compounds and health benefits of exotic tropical red-black berries. Journal of Functional Foods, 5, 539–549. Costa, P. A., Ballus, C. A., Teixeira, J., & Godoy, H. T. (2010). Phytosterols and tocopherols content of pulps and nuts of Brazilian fruits. Food Research International, 43, 1603–1606. Crozier, S. J., Preston, A. G., Hurst, J. W., Payne, M. J., Mann, J., Hainly, L., et al. (2011). Cacao seeds are a ‘‘Super Fruit’’: A comparative analysis of various fruit powders and products. Chemistry Central Journal, 5. http://dx.doi.org/10.1186/1752153X-5-5. Darnet, S., Serra, J. L., Rodrigues, A. M. C., & Silva, L. H. M. (2011). A highperformance liquid chromatography method to measure tocopherols in assai pulp (Euterpe oleracea). Food Research International, 44, 2107–2111. Deharo, E., Baelmans, R., Gimenez, A., Quenevo, C., & Bourdy, G. (2004). In vitro immunomodulatory activity of plants used by the Tacana ethnic group in Bolivia. Phytomedicine, 11, 516–522. Del Pozo-Insfran, D., Brenes, C. H., & Talcott, S. T. (2004). Phytochemical Composition and Pigment Stability of Açai (Euterpe oleracea Mart.). Journal of Agricultural and Food Chemistry, 52(6), 1539–1545. Del Pozo-Insfran, D., Percival, S. S., & Talcott, S. T. (2006). Acai (Euterpe oleracea Mart.) polyphenolics in their glycoside and aglycone forms induce apoptosis of HL-60 leukemia cells. Journal of Agricultural and Food Chemistry, 54, 1222–1229. Desmarchelier, C., Repetto, M., Coussio, J., Llesuy, S., & Ciccia, G. (1997). Total reactive antioxidant potential (TRAP) and total antioxidant reactivity (TAR) of medicinal plants used in Southwest Amazonia (Bolivia and Peru). International Journal of Pharmacognosy, 35(4), 288–296. Dias, A. L. S., Rozet, E., Chataigné, G., Oliveira, A. C., Rabelo, C. A. S., Hubert, P., et al. (2012). A rapid validated UHPLC-PDA method for anthocyanins quantification from Euterpe oleracea fruits. Journal of Chromatography B, 907, 108–116. Favacho, H. A. S., Oliveira, B. R., Santos, K. C., Medeiros, B. J. L., Sousa, P. J. C., Perazzo, F. F., et al. (2010). Anti-inflammatory and antinociceptive activities of Euterpe oleracea Mart., Arecaceae, oil. Revista Brasileira de Farmacognosia, 21, 105–114. Feio, C. A., Izar, M. C., Ihara, S. S., Kasmas, S. H., Martins, C. M., Feio, M. N., et al. (2012). Euterpe oleracea (açai) modifies sterol metabolism and attenuates experimentally-induced atherosclerosis. Journal of Atherosclerosis and Thrombosis, 19(3), 237–245. Fragoso, M. F., Prado, M. G., Barbosa, L., Rocha, N. S., & Barbisan, L. F. (2012). Inhibition of mouse urinary bladder carcinogenesis by açai fruit (Euterpe oleracea Martius) intake. Plant Foods for Human Nutrition, 67, 235–241. Fragoso, M. F., Romualdo, R. G., Ribeiro, D. A., & Barbisan, L. F. (2013). Açai (Euterpe oleracea Mart.) feeding attenuates dimethylhydrazine-induced rat colon carcinogenesis. Food and Chemical Toxicology, 58, 68–76. Frasson, A. P., & Canssi, C. M. (2008). Análise da qualidade de cremes com hidroquinona 2% manipulados no município de Ijuí/RS. Revista de Ciências Farmacêuticas Básica e Aplicada, 29, 197–201. Gallori, S., Bilia, A. R., Bergonzi, M. C., Barbosa, W. L. R., & Vincieri, F. F. (2004). Polyphenolic constituents of fruit pulp of Euterpe oleraceae Mart. (acai palm). Chromatographia, 59, 739–743. Galotta, A. L. Q. A., & Boaventura, M. A. D. (2005). Chemical constituents from roots and leaf stalks of açaí (Euterpe precatoria Mart., Arecaceae). Química Nova, 28(4), 610–613. Galotta, A. L. Q. A., Boaventura, M. A. D., & Lima, L. A. R. S. (2008). Antioxidant and cytotoxic activities of ‘açaí’ (Euterpe precatoria Mart.). Química Nova, 31(6), 1427–1430. Gordon, A., Cruz, A. P. G., Cabral, L. M. C., De Freitas, S. C., Dib Taxi, C. M. A., Donangelo, C. M., et al. (2012). Chemical characterisation and evaluation of antioxidant properties of Açai fruits (Euterpe oleracea Mart.) during ripening. Food Chemistry, 133, 256–263. Gouvêa, A. C. M. S., Araujo, M. C. P., Schulz, D. F., Pacheco, S., Godoy, R. L. O., & Cabral, L. M. C. (2012). Anthocyanins standards (cyanidin-3-O-glucoside and cyaniding-3-O-rutinoside) isolation from freeze-dried açaí (Euterpe oleracea Mart.) by HPLC. Ciência e Tecnologia de Alimentos, 32, 43–46. Hassimotto, N. M. A., Genovese, M. I., & Lajolo, F. M. (2005). Antioxidant activity of dietary fruits, vegetables, and commercial frozen fruit pulps. Journal of Agricultural and Food Chemistry, 53, 2928–2935. Heinrich, M., Dhanji, T., & Casselman, I. (2011). Açaí (Euterpe oleracea) – A phytochemical and pharmacological assessment of the species health claims. Phytochemistry Letters, 4, 10–21. Henderson, A. (1995). The Palms of the Amazon. New York: Oxford University Press. Herculano, F. E. B. (2013) Produção industrial de cosméticos: o protagonismo da biodiversidade vegetal da Amazônia. Tese. UFAM, 146p. Hogan, S., Chung, H., Zhang, L., Li, J., Lee, Y., Dai, Y., et al. (2010). Antiproliferative and antioxidant properties of anthocyanin-rich extract from açai. Food Chemistry, 118, 208–214. Homma, A. K., Maia, C., & Nicoli, L. (2006). Açaí: novos desafios e tendências. Amazônia: Ciência & Desenvolvimento, 1, 7–23. IBGE – INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. Contas Regionais do Brasil 2008. Disponível em: . Acesso em: 26 junho. 2014. Inácio, M. R. C., Lima, S. M. G., Lopes, V. G., Pessoa, J. D., & Teixeira, G. H. T. (2013). Total anthocyanin content determination in intact acai (Euterpe oleracea Mart.) and palomitero–jucara (Euterpe edulis Mart.) fruit using near infrared

spectroscopy (NIR) and multivariate calibration. Food Chemistry, 136, 1160–1164. Jensen, G. S., Wu, X., Patterson, K. M., Barnes, J., Carter, S. G., Scherwitz, L., et al. (2008). In vitro and in vivo antioxidant and anti-inflammatory capacities of an antioxidant-rich fruit and berry juice blend. Results of a pilot and randomized, double-blinded, placebo-controlled, crossover study. Journal of Agricultural and Food Chemistry, 56(18), 8326–8333. Jensen, J. F., Kvist, L. P., & Christensen, S. B. (2002). An antiplasmodial lignan from Euterpe precatoria. Journal of Natural Product, 65, 1915–1917. Kang, J., Li, Z., Wu, T., Jensen, G. S., Schauss, A. G., & Wu, X. (2010). Anti-oxidant capacities of flavonoid compounds isolated from acai pulp (Euterpe oleracea Mart.). Food Chemistry, 122, 610–617. Kang, J., Thakali, K. M., Xie, C., Kondo, M., Tong, Y., Ou, B., et al. (2012). Bioactivities of açaí (Euterpe precatoria Mart.) fruit pulp, superior antioxidant and antiinflammatory properties to Euterpe oleracea Mart. Food Chemistry, 133, 671–677. Kang, J., Xie, C., Li, Z., Nagarajan, S., Schauss, A. G., Wu, T., et al. (2011). Flavonoids from acai (Euterpe oleracea Mart.) pulp and their antioxidant and antiinflammatory activities. Food Chemistry, 128(1), 152–157. Kuskoski, E. M., Asuero, A. G., Morales, M. T., & Fett, R. (2006). Frutos tropicais silvestres e polpas de frutas congeladas: atividade antioxidante, polifenóis e antocianinas. Ciência Rural, 36, 1283–1287. Lichtenthaler, R., Rodrigues, R. B., Maia, J. G. S., Papgiannopoulos, M., Fabricius, H., & Marx, F. (2005). Total oxidant scavenging capacity of the Euterpe oleracea Mart. (Açaí) fruits. International Journal of Food Sciences and Nutrition, 56(1), 56–64. Lima, F. E. L., Menezes, T. N., Tavares, M. P., Szarfac, S. C., & Fisberg, R. M. (2000). Fatty acids and cardiovascular diseases: a review. Revista de Nutrição, 13, 73–80. Mantovani, I. S. B., Fernandes, S. B. O., & Menezes, F. S. (2003). Constituintes apolares do fruto do açaí (Euterpe oleracea M. – Arecaceae). Revista Brasileira de Farmacognosia, 13, 41–42. Marinho, B. G., Herdy, S. A., Sá, A. C., Santos, G. B., Matheus, M. E., Menezes, F. S., et al. (2002). Atividade antinociceptiva de extratos de açaí (Euterpe oleraceae Mart.). Revista Brasileira de Farmacognosia, 12, 52–53. Matheus, M. E., Fernandes, S. B. d. O., Silveira, C. S., Rodrigues, V. P., Menezes, F. d. S., & Fernandes, P. D. (2006). Inhibitory effects of Euterpe oleracea Mart. on nitric oxide production and iNOS expression. Journal of Ethnopharmacology, 107, 291–296. Matheus, M. E., Mantovani, I. S. B., Santos, G. B., Fernandes, S. B. O., Menezes, F. S., & Fernandes, P. D. (2003). Ação de extratos de açaí (Euterpe oleraceae Mart.) sobre a produção de óxido nítrico em células RAW 264.7. Revista Brassileira de Farmacognosia, 13, 3–5. Menezes, E. M. S., Rosenthal, A., Sabaa-Srur, A., Carmargo, L., Calado, V., & Santos, A. (2008). High hydrostatic pressure effect on enzyme activity of açaí pulp. Ciência e Tecnologia de Alimentos, 28, 14–19. Menezes, E., Deliza, R., Chan, H. L., & Guinard, J. X. (2011). Preferences and attitudes towards açaí-based products among North American consumers. Food Research International, 44, 1997–2008. Mertens-Talcott, S. U., Rios, J., Jilma-Stohlawetz, P., Pacheco-Palencia, L. A., Meibohm, B., Talcott, S. T., et al. (2008). Pharmacokinetics of anthocyanins and antioxidant effects after the consumption of anthocyanin-rich acai juice and pulp (Euterpe oleracea Mart.) in human healthy volunteers. Journal of Agricultural and Food Chemistry, 56, 7796–7802. Moura, R. S., Ferreira, T. S., Lopes, A. A., Pires, K. M. P., Nesi, R. T., Resende, A. C., et al. (2012). Effects of Euterpe oleracea Mart. (açaí) extract in acute lung inflammation induced by cigarette smoke in the mouse. Phytomedicine, 19, 262–269. Moura, R. S., Pires, K. M. P., Ferreira, T. S., Lopes, A. A., Nesi, R. T., Resende, A. C., et al. (2011). Addition of açaí (Euterpe oleracea) to cigarettes has a protective effect against emphysema in mice. Food and Chemical Toxicology, 49, 855–863. Mulabagal, V., & Calderón, A. I. (2012). Liquid chromatography/mass spectrometry based fingerprinting analysis and mass profiling of Euterpe oleracea (açaí) dietary supplement raw materials. Food Chemistry, 134, 1156–1164. Muñiz-Miret, N., Vamos, R., Hiraoka, M., Montagnini, F., & Mendelsohn, R. O. (1996). The economic value of managing the acai palm (Euterpe oleracea mart.) in the floodplains of the Amazon estuary, Para, Brazil. Forest Ecology and Management, 87, 163–173. Nascimento, R. J. S., Couril, S., Antoniassi, R., & Freitas, S. P. (2008). Composição em ácidos graxos do óleo da polpa de açaí extraído com enzimas e com hexano. Revista Brasileira de Fruticultura, 30, 498–502. Nogueira, O. L., Figueirêdo, F. J. C. & Muller, A. A. (2005) Açaí. (1th ed.). Belém: Embrapa Amazônia Oriental. Odonne, G., Berger, F., Stien, D., Grenand, P., & Bourdy, G. (2011). Treatment of leishmaniasis in the Oyapock basin (French Guiana): A K.A.P. survey and analysis of the evolutionary of phytotherapy knowledge amongst Wayãpi Indians. Journal of Ethnopharmacology, 137, 1228–1239. Pacheco-Palencia, L. A., Duncan, C. E., & Talcott, S. T. (2009). Phytochemical composition and thermal stability of two commercial acai species, Euterpe oleracea and Euterpe precatoria. Food Chemistry, 115, 1199–1205. Pacheco-Palencia, L., Hawken, P., & Talcott, S. (2007a). Juice matrix composition and ascorbic acid fortification effects on the phytochemical, antioxidant, and pigment stability of açai (Euterpe oleracea Mart.). Food Chemistry, 105, 28–35. Pacheco-Palencia, L., Hawken, P., & Talcott, S. (2007b). Phytochemical, antioxidant and pigment stability of açai (Euterpe oleracea Mart.) as affected by clarification, ascorbic acid fortification and storage. Food Research International, 40, 620–628. Pacheco-Palencia, L. A., & Talcott, S. T. (2010). Chemical stability of açai fruit (Euterpe oleracea Mart.) anthocyanins as influenced by naturally occurring and

K. K. d. L. Yamaguchi et al. / Food Chemistry 179 (2015) 137–151 externally added polyphenolic cofactors in model systems. Food Chemistry, 118, 17–25. Pacheco-Palencia, L. A., Mertens-Talcott, S., & Talcott, S. T. (2008). Chemical composition, antioxidant properties, and thermal stability of a phytochemical enriched oil from Açai (Euterpe oleracea Mart.). Journal of Agricultural and Food Chemistry, 56, 4631–4636. Pagliarussi, M., S. A. cadeia produtiva agroindustrial do açaí: estudo da cadeia e proposta de um modelo matemático. 65f. TCC, Escola de Engenharia de São Carlos, Universidade de São Paulo, 2010. Pompeu, D. R., Silva, E. M., & Rogez, H. (2009). Optimisation of the solvent extraction of phenolic antioxidants from fruits of Euterpe oleracea using response surface methodology. Bioresource Technology, 100, 6076–6082. Poulose, S. M., Fisher, D. R., Larson, J., Bielinski, D. F., Rimando, A. M., Carey, A. N., et al. (2012). Anthocyanin-rich acai (Euterpe oleracea Mart.) fruit pulp fractions attenuate inflammatory stress signaling in mouse brain BV-2 microglial cells. Journal of Agricultural and Food Chemistry, 60, 1084–1093. Queiroz, J. A. L., & Melém Junior, N. J. (2001). Efeito do tamanho do recipiente sobre o desenvolvimento de mudas do açaí (Euterpe oleracea Mart.). Revista Brasileira de Fruticultura, 23, 460–462. Ribeiro, J. C., Antunes, L. M., Aissa, A. F., Darin, J. D., De Rosso, V. V., Mercadante, A. Z., et al. (2010). Evaluation of the genotoxic and antigenotoxic effects after acute and subacute treatments with acai pulp (Euterpe oleracea Mart.) on mice using the erythrocytes micronucleus test and the comet assay. Mutation Research, 695, 22–28. Rocha, A. P., Carvalho, L. C., Sousa, M. A., Madeira, S. V., Sousa, P. J., Tano, T., et al. (2007). Endothelium-dependent vasodilator effect of Euterpe oleracea Mart. (acai) extracts in mesenteric vascular bed of the rat. Vascular Pharmacology, 46, 97–104. Rodrigues, R. B., Lichtenthaler, R., Zimmerman, B. F., Papgiannopoulos, M., Fabricius, H., & Marx, F. (2006). Total oxidant scavenging capacity of Euterpe oleracea Mart. (Acai) seeds and identification of their polyphenolic compounds. Journal of Agricultural and Food Chemistry, 54, 4162–4167. Rogez, H. (2000). Açaí: preparo, composição e melhoramento da conservação (1th ed.). Belém: UFPA. Rogez, H., Pompeu, D. R., Akwie, S. N. T., & Larondelle, Y. (2011). Sigmoidal kinetics of anthocyanin accumulation during fruit ripening: A comparison between açai fruits (Euterpe oleracea) and other anthocyanin-rich fruits. Journal of Food Composition and Analysis, 24, 796–800. Rojano, B. A., Vahos, I. C. Z., Arbeláez, A. F. A., Martínez, A. J. M., Correa, F. B. C., & Carvajal, L. G. (2011). Polifenoles y Actividad Antioxidante del Fruto Liofilizado de Palma Naidi (Açaí Colombiano) (Euterpe oleracea Mart.). Revista Facultad Nacional de Agronomía Medellín, 64, 6213–6220. Rosso, V. V., Hillbrand, S., Montilla, E. C., Bobbio, F. O., Winterhalter, P., & Mercadante, A. Z. (2008). Determination of anthocyanins from acerola (Malpighia emarginata DC.) and açaí (Euterpe oleracea Mart.) by HPLC–PDA– MS/MS. Journal of Food Composition and Analysis., 21, 291–299. Rufino, M. S. M., Alves, R. E., Fernandes, F. A. N., & Brito, E. S. (2011). Free radical scavenging behavior of ten exotic tropical fruits extracts. Food Research International, 44, 2072–2075. Rufino, M. S. M., Alves, R. E., Brito, E. S., Pérez-Jiménez, J., Saura-Calixto, F., & Mancini-Filho, J. (2010). Bioactive compounds and antioxidant capacities of 18 non-traditional tropical fruits from Brazil. Food Chemistry, 121, 996–1002. Ruiz, L., MacO, M., Cobos, M., Gutierrez-Choquevilca, A. L., & Roumy, V. (2011). Plants used by native Amazonian groups from the Nanay River (Peru) for the treatment of malária. Journal of Ethnopharmacology, 133, 917–921. Sabbe, S., Verbeke, W., Deliza, R., Matta, V., & Van Damme, P. (2009). Effect of a health claim and personal characteristics on consumer acceptance of fruit juices with different concentrations of acai (Euterpe oleracea mart). Appetite, 53, 84–92. Santos, V. S., Nardini, V., Cunha, L. C., Jr., Barbosa, F., Jr., & Teixeira, G. H. A. (2014). Identification of species of the Euterpe genus by rare earth elements using inductively coupled plasma mass spectrometry and linear discriminant analysis. Food Chemistry, 153, 334–339.

151

Schauss, A. G. (2010). Acai (Euterpe oleracea Mart.): A macro and nutrient rich palm fruit from the Amazon rain forest with demonstrated bioactivities in vitro and in vivo. In D. R. Watson & V. R. Preedy (Eds.), Bioactive foods promotion health (pp. 479–490). Oxford: Academic Press. Schauss, A. G., Wu, X., Prior, R. L., Ou, B., Patel, D., Huang, D., et al. (2006a). Phytochemical and nutrient composition of the freeze-dried amazonian palm berry, Euterpe oleraceae Mart. (acai). Journal of Agricultural and Food Chemistry, 54, 8598–8603. Schauss, A. G., Wu, X., Prior, R. L., Ou, B., Huang, D., Owens, J., et al. (2006b). Antioxidant capacity and other bioactivities of the freeze-dried Amazonian palm berry, Euterpe oleracea Mart. (acai). Journal of Agricultural and Food Chemistry, 54, 8604–8610. Silva, J. A. P., & Tavares, F. F. C. (2013). Estudo da aplicação de sementes de açaí (Euterpe oleracea Mart.) para produção de carvão ativado. Revista de Ciências da Amazônia, 1, 55–66. Silva, J. J. M., & Rógez, H. (2013). Avaliação da estabilidade oxidativa do óleo bruto de açaí (Euterpe oleracea) na presença de compostos fenólicos puros ou de extratos vegetais amazônicos. Química Nova, 36, 400–406. Silva, J. A., Munaro, E., & Pereira, L. R. (2002). Produtos florestais não madeireiros: Açaí. Brasília: Ibama/CNPT. Souza, M. O., Silva, L. S., Magalhães, C. L. B., Figueiredo, B. B., Costa, D. C., Silva, M. E., et al. (2012). The hypocholesterolemic activity of açaí (Euterpe oleracea Mart.) is mediated by the enhanced expression of ATP-binding cassette, subfamily G transporters 5 and 8 low-density lipoprotein receptor genes in rat. Nutrition Research, 32, 976–984. Souza, M. O., Silva, M., Silva, M. E., Oliveira, R. P., & Pedrosa, M. L. (2010). Diet supplementation with açaí (Euterpe oleracea Mart.) pulp improves biomarkers of oxidative stress and the serum lipid profile in rats. Nutrition, 26, 804–810. Spada, P. D., Dani, C., Bortolini, G. V., Funchal, C., Henriques, J. A., & Salvador, M. (2009). Frozen fruit pulp of Euterpe oleraceae Mart. (acai) prevents hydrogen peroxide-induced damage in the cerebral cortex, cerebellum, and hippocampus of rats. Journal of Medicinal Food, 12, 1084–1088. Sun, X., Seeberger, J., Alberico, T., Wang, C., Wheeler, C. T., Schauss, A. G., et al. (2010). Açaí palm fruit (Euterpe oleracea Mart.) pulp improves survival of flies on high fat diet. Experimental Gerontology, 45, 243–251. Tonon, R. V., Alexandre, D., Hubinger, M. D., & Cunha, R. L. (2009). Steady and dynamic shear rheological properties of açai pulp (Euterpe oleraceae Mart.). Journal of Food Engineering, 92, 425–431. Vandresen, S., Quadri, M. G. N., Souza, J. A. R., & Hotza, D. (2009). Temperature effect on the rheological behavior of carrot juices. Journal of Food Engineering, 92, 269–274. Vigneron, M., Deparis, X., Deharo, E., & Bourdy, G. (2005). Antimalarial remedies in French Guiana: A knowledge attitudes and practices study. Journal of Ethnopharmacology, 98, 351–360. Xie, C., Kang, J., Burris, R., Ferguson, M. E., Schauss, A. G., Nagarajan, S., et al. (2011). Açaí juice attenuates atherosclerosis in ApoE deficient mice through antioxidant and anti-inflammatory activities. Atherosclerosis, 216, 327–333. Xie, C., Kang, J., Li, Z., Schauss, A. G., Badger, T. M., Nagarajan, S., et al. (2012). The açaí flavonoid velutin is a potent anti-inflammatory agent: Blockade of LPSmediated TNF-aand IL-6 production through inhibiting NF-jB activation and MAPK pathway. Journal of Nutrition Biochemistry, 23, 1184–1191. Youdim, K. A., Martin, A., & Joseph, J. A. (2000). Incorporation of the elderberry anthocyanins by endothelial cells increases protection against oxidative stress. Free Radical Biology & Medicine, 29(1), 51–60. Yuyama, L. K. O., Aguiar, J. P. L., Filho, D. F. S., Yuyama, K., Varejão, M. J., Fávaro, D. I. T., et al. (2011). Physicochemical characterization of acai juice of Euterpe precatoria Mart. from different Amazonian ecosystems. Acta Amazônica, 41, 545–552. Yuyama, L. K. O., Aguiar, J. P. L., Silva Filho, D. F. S., Yuyama, K., Varejão, M. J., Favaro, D. I. T., et al. (2012). Caracterização físico-química do suco de açaí de Euterpe precatoria Mart. oriundo de diferentes ecossistemas amazônicos. Acta Amazônica, 41, 545–552.