Nutritional compositions and health promoting phytochemicals of camu-camu (myrciaria dubia) fruit: A review

Nutritional compositions and health promoting phytochemicals of camu-camu (myrciaria dubia) fruit: A review

Food Research International 44 (2011) 1728–1732 Contents lists available at ScienceDirect Food Research International j o u r n a l h o m e p a g e ...

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Food Research International 44 (2011) 1728–1732

Contents lists available at ScienceDirect

Food Research International j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / f o o d r e s

Review

Nutritional compositions and health promoting phytochemicals of camu-camu (myrciaria dubia) fruit: A review Mst. Sorifa Akter a, Sejong Oh b, Jong-Bang Eun a, Maruf Ahmed a,b,c,⁎ a b c

Department of Food Science and Technology and Functional Food Research Center, Chonnam National University, Gwangju, South Korea Department of Animal Science and Biotechnology, Chonnam National University, Gwangju, South Korea Department of Food Processing and Preservation, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh

a r t i c l e

i n f o

Article history: Received 20 November 2010 Accepted 22 March 2011 Keywords: Camu-camu Vitamin C Phenolic compounds Carotenoids Antioxidant capacity

a b s t r a c t Camu-camu (Myrciaria dubia) fruits are promising sources of various bioactive compounds such as vitamin C, phenolic compounds and carotenoids. Camu-camu fruits are also good sources of potassium, iron, calcium, phosphorous and various kinds of amino acids such as serine, valine and leucine. Therefore, the presence of different bioactive compounds in camu-camu fruits could be used to retard or prevent various diseases such as cardiovascular and cancer. This is an update report on nutritional compositions and health promoting phytochemicals of camu-camu fruits. This review reveals that camu-camu fruits might be used as functional foods or for nutraceutical purposes. © 2011 Elsevier Ltd. All rights reserved.

Contents 1. 2.

Introduction . . . . . . . . . . . . . . . . . . . . . . . Characterization and nutritional compositions of camu-camu 2.1. Proximate composition . . . . . . . . . . . . . . . 2.2. Bioactive compounds of camu-camu fruits. . . . . . 2.2.1. Polyphenols compounds . . . . . . . . . . 2.2.2. Antioxidant capacity . . . . . . . . . . . . 2.2.3. Carotenoid compositions . . . . . . . . . . 2.2.4. Vitamin C . . . . . . . . . . . . . . . . . 3. Health benefit properties of camu-camu fruits . . . . . . . 3.1. Biological effects of polyphenol . . . . . . . . . . . 3.2. Antioxidative and anti-inflammatory properties . . . 3.3. Antimicrobial activity . . . . . . . . . . . . . . . 3.4. Aldose reductase inhibitors . . . . . . . . . . . . . 4. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . fruits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction Fruits are essential for sound health. Consumption of fruits has been increased because of their high content of bioactive compounds. The ⁎ Corresponding author at: Department of Animal Science and Biotechnology, Chonnam National University, 77 Yongbong-ro Buk-gu, Gwangju, 500-757, South Korea. Tel.: + 82 062 530 0822; fax: + 82 062 530 2129. E-mail address: [email protected] (M. Ahmed). 0963-9969/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodres.2011.03.045

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most common bioactive compounds are vitamin C, polyphenol, βcarotene and lycopene contents. In recent years, there has been a global trend toward the use of natural phytochemical as antioxidants and functional ingredients, which are present in natural resources such as vegetables, fruits, oilseeds and herbs, (Elliott, 1999; Kaur & Kapoor, 2001; Larson, 1988; Namiki, 1990). Natural antioxidants from plant extracts have attracted considerable attention due to their safety. Camu-camu (Myrciaria dubia) is a member of the Myrtaceae family and it is native to the Amazon region. Camu-camu is an

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important source of nutritional antioxidant, vitamins C, β-carotene, and phenolic compounds (Chirinos, Galarza, Betalleluz-Pallardel, Pedreschi, & Campos, 2010). Camu-camu fruits are considered the richest natural source of vitamin C in Brazil (Vidigal et al., in press). Bioactive compounds in camu-camu fruits are not only responsible of vitamin C but also responsible of other compounds such as phenolic compounds and β-carotene contents (Chirinos et al., 2010; Zanatta, Cuevas, Bobbio, Winterhalter, & Mercadante, 2005; Zanatta & Mercadante, 2007). Camu-camu fruits are also good source of potassium, iron, calcium and phosphorous and various kinds of amino acids such as serine, valine and leucine (Zapata & Dufour, 1993). Japan and the European Union are main export markets for camucamu products such as pulp, extract and juice. Camu-camu pulps are used as sherbets and puree. Camu-camu whole fruits and slices might be used to make dried camu-camu products. It seems that camu-camu fruits are promising sources of bioactive compounds which could be used as a functional food not only in the Amazon region but also around the world. Therefore, the objective of this review is to provide existing information of the proximate composition and health promoting phytochemicals mainly vitamin C, polyphenol and β-carotene contents of camu-camu fruits.

2. Characterization and nutritional compositions of camu-camu fruits 2.1. Proximate composition The shape of the camu-camu fruits is round and the diameter and length are 1.0 to 3.2 cm and 1.2–2.5 cm, respectively (Fig. 1). Nutritional compositions of camu-camu fruits are shown in Table 1. Camu-camu fruits are good source of minerals such as sodium, potassium, calcium, zinc, magnesium, manganese and copper. It also contains small amount of pectin and starch. Glucose and fructose are the major sugar for camucamu fruit (Zapata & Dufour, 1993). Camu-camu fruits also contain different types of amino acids such as serine, valine, leucine, glutamate, 4-aminobutanoate, proline, phenylalanine, threonine, alanine (Zapata & Dufour, 1993). Different organic acids such as citric acid, isocitric acid and malic acid also have been identified in camu-camu fruits (Zapata & Dufour, 1993). In addition, camu-camu pulps also contain different kinds of fatty acids mainly stearic, linoleic, oleic, γ-linolenic, α-linolenic, tricosanoic, eicosadienoic (Justi et al., 2000). There are twenty one volatile compounds found in camu-camu fruits (Franco & Shibamoto, 2000).

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Table 1 Nutritional composition of camu-camu fruits. Moisture (g/100 g) Protein (g/100 g) Ash (g/100 g) Crude fiber (g/100 g) Lipids (g/100 g) Sodium (mg/kg) Potassium (mg/kg) Calcium (mg/kg) Magnesium (mg/kg) Iron (mg/kg) Manganese (mg/kg) Zinc (mg/kg) Copper (mg/kg) TSS (0Brix) Total titrable acidity (%) pH Glucose (g/kg fresh weight) Fructose (g/kg fresh weight) Total sugar (%) Total pectin (%) Starch (%)

94.1 ± 0.1 0.4 ± 0.0 0.3 ± 0.0 0.1 ± 0.0 0.2 ± 0.0 111.3 ± 4.3 838.8 ± 36.2 157.3 ± 4.4 123.8 ± 8.7 5.3 ± 0.4 21.1 ± 1.1 3.6 ± 0.1 2.0 ± 0.2 6.40 ± 0.0 2.86 ± 0.0 2.44 ± 0.0 8.16 ± 0.0 9.51 ± 0.0 1.28 ± 0.0 0.21 ± 0.0 0.44 ± 0.0

(Source from Alves et al., 2002; Justi et al., 2000; Zapata & Dufour, 1993).

2.2. Bioactive compounds of camu-camu fruits Camu-camu fruits are considered significant sources of different bioactive compounds. Many researchers have already identified different bioactive compounds in camu-camu fruits (Tables 2–3). In this section we have described different types of bioactive compounds of camu-camu fruits. 2.2.1. Polyphenols compounds Polyphenol groups are flavonoids, phenolic acids, tannins (hydrolysable and condensed), stilbenes and lignans (D'Archivio et al., 2007). Different types of flavonoids such as flavanols, flavonols, flavanones, anthocyanins are found in camu-camu fruits. Polyphenolic compounds of camu-camu fruits depend on the state of maturity. In order to improve the extraction of bioactive compounds solvent extraction methods such as methanol/water/acetic acid (70:30:5 v/v) (Goncalves et al., 2010); methanol/water (50:50 v/v) followed by acetone/water (70:30 v/v) (Rufino et al., 2010); 50% aqueous acetone (Myoda et al., 2010); methanol/ formic acid (9:1) (Reynertoson, Yang, Jiang, Basile, & Kennelly, 2008); 80% methanol followed by acidified methanol (0.01% HCl) (Chirinos et al., 2010); ethanol/1.5 N HCl (85:15 v/v) (Zanatta et al., 2005) were used. Table 2 Individual polyphenols of camu-camu fruits. Flavanols Catechin (mg/100 g fresh weight) Flavonols Quercetin (mg/100 g dry weight) Rutin (mg/100 g fresh weight) Kaempferol (mg/100 g dry weight) Flavanones Naringenin (mg/100 g fresh weight) Eriodictyol (mg/100 g fresh weight) Anthocyanins Delphidinin-3-glucoside (%) Cyanidin-3-glucoside (%) Free ellagic acid (mg/100 g dry weight) Total ellagic acid (mg/100 g dry weight) Total phenolic content of fresh camu-camu (mg gallic acid/100 g) Total phenolic content of dried camu-camu (mg gallic acid/100 g) Total phenolic content in seed (mg gallic acid/100 g) Total phenolic content in peel (mg gallic acid/100 g)

Fig. 1. Camu-camu (Myrciaria dubia) fruit. (Source from Zanatta et al., 2005).

2.2 42.0 4.0 2.1 6.9 0.6 4.2 89.5 16.0 490 1176 1161 369 203

(Source from Chirinos et al., 2010; Goncalves et al., 2010; Rufino et al., 2010; Myoda et al., 2010).

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Table 3 Carotenoid compositions and vitamin A of camu-camu harvested in Iguape and Mirandopolis, Sao Paulo, Brazil. (Source Zanatta & Mercadante, 2007). Carotenoid

Neoxanthin cis-neoxanthin Violaxanthin(all-trans* + cis) Luteoxanthin Not identified-436 Flavoxanthin* + mixture 5,6-epoxy-lutein 5,8-epoxy-zeaxanthin 5,6-epoxy-zeaxanthin All-trans-lutein Zeaxanthin Sintaxanthin b-Cryptoxanthin(all-trans* + cis) 5,8-Epoxy-b-carotene Not identified-427 β-carotene Total carotenoids Vitamin A value(RE/100 g)

Concentration (μg/100 g) Iguape

Mirandopolis

3.9 ± 1.7 2.1 ± 1.8 12.0 ± 19.3 21.5 ± 13.4 2.3 ± 2.7 9.4 ± 4.9 2.1 ± 3.7 9.2 ± 9.8 12.9 ± 22.3 160.5 ± 114.0 22.9 ± 13.0 1.11 ± 0.4 9.9 ± 3.7 3.6 ± 2.4 8.6 ± 9.4 72.8 ± 74.6 354.8 ± 260.5 14.2 ± 13.4

20.8 ± 13.3 16.0 ± 10.2 115.6 ± 62.4 60.0 ± 20.7 26.1 ± 6.1 6.7 ± 0.6 8.6 ± 8.6 nd 47.7 ± 22.7 601.9 ± 92.5 38.0 ± 12.7 1.0 ± 0.3 6.9 ± 0.2 1.2 ± 2.0 2.8 ± 3.7 142.3 ± 23.7 1095.3 ± 237.0 24.5 ± 4.1

nd, not detected; and *, major.

2.2.1.1. Total polyphenols. Camu-camu fruits contain high amount of total phenolics. Usually total phenolics were performed by Folin– Ciocalteu assay. Reynertoson et al. (2008) found that camu-camu fruits powder had much higher total phenolic content than that of other fruits such as Myrciaria vexato, Myrciaria cauliflora.Genovese, Da Silva Pinto, De Souza Schmidt Gonçalves, and Lajolo (2008) reported higher level of total phenolics in camu-camu fruits as compared to passion fruits cambuci and araca. According to Rufino et al. (2010) total phenolic content was higher in camu-camu fruits as compared to the acerola. Very recently, the Peru research group (Chirinos et al., 2010) reported that total phenolic contents in camu-camu fruits depend on the maturity stages. Recently, a Japanese research group (Myoda et al., 2010) found that the total phenolic content of camucamu seed and peel was much higher than those of other fruit residues such as acerola, pineapple and passion fruits. Other studies showed that camu-camu exhibited ten times higher total phenolic content than those of tucuma and uxi fruits (Goncalves et al., 2010). 2.2.1.2. Individual polyphenols. Various kinds of polyphenol compounds such as flavanols, flavonols, flavanones, anthocyanins, catechin, flavan-3ol, rutin are found in camu-camu fruits. The amount of flavonoids in camu-camu fruits was 20.1 ± 4.4 mg/100 g fresh mater (Rufino et al., 2010). In another study, Chirinos et al. (2010) showed that the total flavanol content in camu-camu fruits was 11.6 mg catechin equivalent/100 fresh weight. The content of quercetin (42 mg/100 g dry weight) and kaempferol (0.4 to 2.5 mg/ 100 g dry weight) was found in camu-camu (Goncalves et al., 2010). However, Genovese et al. (2008) found quercetin (4.1 mg/100 fresh weight) and kaempferol (0.21 mg/ 100 g fresh weight) contents in camu-camu fruits. Reynertoson et al.'s (2008) research group found quercetin (0.24 mg/g, dry weight basis) and rutin (0.13 mg/g, dry weight basis) in camu-camu fruit powder. Chirinos et al. (2010) mentioned that camu-camu fruits also contain catechin, rutin, flavan3ol, flavanone, hydrolysed tannins (gallotannins or ellagitannins). The flavonoids in camu-camu were higher than in acerola (9.6 ± 1.4 mg/ 100 g fresh mater), bacuri (16.9 ± 1.7 mg/100 g fresh mater) fruits but lower than in cashew apple (63.8 ± 26.5 mg/100 g fresh mater) (Rufino et al., 2010). However, Chirinos et al. (2010) found total flavonoids in camu-camu were similar to the mashua tuber (12.4 mg catechin equivalent/100 fresh weight) and acai fruits (12 mg catechin equivalent/100 fresh weight). The highest content of quercetin was found in camu-camu fruits as compared to other fruits such as araca

(40 mg/100 g dry weight), cambuci (21.6 mg/100 g dry weight), araca-boi (14.4 mg/100 g dry weight (Goncalves et al., 2010). There is very few information about anthocyanin content of camucamu fruits. However, the anthocyanin content of camu-camu was higher as compared to others fruits. The total anthocyanin content in the camu-camu fresh peel was 54.0 ± 25.9 mg/100 g (Zanatta et al., 2005). Zanatta et al. (2005) mentioned that the cyanidin-3-glucoside was the major anthocyanins in camu-camu fruits followed by delphinidin-3-glucoside. However, Reynertoson et al. (2008) found that the total anthocyanin content of camu-camu dried fruits powder was very low (below 0.01 mg/g dry weight). Very recently, other research groups (Rufino et al., in press) showed the total anthocyanin content of camu-camu fruits was 42.2 ± 14.0 mg/100 g fresh weight. Goncalves et al. (2010) and Chirinos et al. (2010) also reported that delphinidin-3-glucoside and cyanindin-3-glucoside were the main types of anthocyanins in camu-camu fruits. Chirinos et al. (2010) indicated that green and green-reddish, only traces were present, but in mature camu-camu fruits, they found 22.4 and 2.2 mg/100 g of cyanidin-3-glucoside and delphinidin-3-glucoside. Zanatta et al. (2005)showed that anthocyanin content of camu-camu fruits was higher than the strawberries (21 mg/100 g), red grapes (27 mg/ 100 g) but lower than black berries (245 mg/100 g) and blueberries (387 mg/100 g). Galic and ellagic acids were found in camu-camu fruits after acid hydrolysis of extract (Chirinos et al., 2010). Goncalves et al. (2010) revealed that free ellagic acid (16 mg/100 g dry weight) and total ellagic acid (490 mg/100 g dry weight) in camu-camu fruits were higher than those of other fruits such as cambuci (ellagic acid 2.5 mg/100 g dry weight and total ellagic acid 240 mg/100 g dry weight), araca ellagic acid 7.4 mg/100 g dry weight and total ellagic acid 262 mg/100 g dry weight). 2.2.2. Antioxidant capacity Different methods such as ferric reducing antioxidant powder (FRAP), organic radical-scavenging capacity [ABTS-2, 2-azino-bis (3-ethyl-benz-thiazoline-6-sulfonicacid)], DPPH (2, 2-Diphenyl1-picrylhydrazil) and peroxyl radical-scavenging capacity (ORACoxygen radical absorbance capacity), β-carotene and linoleic acid bleaching methods are used to determine the antioxidant capacity. Camu-camu exhibited the highest antioxidant capacity followed by tucuma and uxi fruits (Goncalves et al., 2010). These research groups also found a positive correlation between the antioxidant capacity with ORAC and the total phenolic content. Genovese et al. (2008)observed that DPPH radical scavenging activity for camu-camu was more than ten times as compared to other fruits such as araca-boi, araca, and cambuci. They also found a good correlation between total phenols and DPPH scavenging activity for all fruits (r= 0.997). However no correlation was found for total phenolic content and β-carotene bleaching. Rufino et al. (2010) found that total phenolic content was correlated with ABTS (r= 0.92) and reducing power (r = 0.89). However, total phenolic content was negatively correlated with DPPH radical scavenging (r= −0.72). These research groups displayed the DPPH antioxidant capacity has the same trend as the total phenolic content. Chirinos et al. (2010) groups also revealed good correlation between total phenolic content and DPPH antioxidant capacity (r2 = 0.93). However, Reynertoson et al. (2008) demonstrated that total phenolic content was not correlated with DPPH. Japanese research groups (Myoda et al., 2010) explored that DPPH (IC50 values) radical scavenging activities of 25–75% MeOH camucamu seed extract (12.8 ± 0.7 to 20.7 ± 0.9 μg/g) were higher than that of ascorbic acid (21.4 ±0.1 μg/g). They also found that the total phenolic content was highly correlated with DPPH radical scavenging activities (r= 0.97) and the reducing power (r = 0.97) for both seed and peel extract. Chirinos et al. (2010)have demonstrated that vitamin C contributes about 70% to the total antioxidant capacity of camu-camu fruits. According to Rodridues, Papagiannopoulos, Maia, Yuyama, and Marx (2006)the reactive oxygen species of camu-camu juice was higher than other juices such as acai, apple, blueberry and orange juice.

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2.2.3. Carotenoid compositions Carotenoids such as β-carotene, lycopene, lutein and zeaxanthine are known to exhibit antioxidant activity. The carotenoid profile of camu-camu fruits are shown in Table 3. Azevedo-Meleiro and Rodriguez-Amaya (2004) mentioned that lutein was the major carotenoid followed by β-carotene and zeaxanthin. However, neoxanthin, β-cryptoxanthin, β-carotene,-5, 6-epoxide and cis-β-carotene were also identified at very low levels. In another study, all-trans-lutein was the major carotenoids followed by β-carotene, violaxanthin and luteoxanthin for both regions Zanatta & Mercadante, 2007). They also mentioned that camu-camu fruits' carotenoid was higher than that of cashew-apple but lower than mango and acerola fruits. Finally, these authors summarized that lutein is higher as compared to all fruits and comparable to some leafy vegetables. Therefore, camu-camu fruits could be used as a good source of lutein. Very recently, Rufino et al. (2010) mentioned that total carotenoid of camu-camu fruits was 0.4 mg/100 g fresh matter.

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peel showed antimicrobial activity to Staphylococcus aureus due to lipophilic constituents. 3.4. Aldose reductase inhibitors Aldose inhibitors are able to reduce diabetic complications (Mizuno, Kato, Makino, Suzuki, & Shindo 1999). Therefore, Japanese researchers (Ueda et al. 2004) investigated the aldose reductase inhibitors of leaves of camu-camu fruits. According to these groups (Ueda et al. 2004) they isolated ellagic acid, 4-0-methylellagic acid and 4-(α-rhamnopyranosyl) ellagic acid from leaves of Myrciaria dubia (H. B. & K.) McVaugh. They found that the compound of 4(α-rhamnopyranosyl) ellagic acid had strongest inhibition against human recombinant aldose reductase and rat lens aldose reductase even the inhibitory activity of the compound of 4-(α-rhamnopyranosyl) ellagic acid was 60 times higher than quercetin. 4. Conclusion

2.2.4. Vitamin C Many researchers have already considered that camu-camu fruits are a good source of vitamin C. Vitamin C contents found were 2061.01 mg/100 g in purple camu-camu and 1910.31 mg/100 g in green camu-camu fruits (Alves et al., 2002). Recently, Rufino et al. (2010) exhibited vitamin C content (1882 ± 43.2 mg/100 g fresh matter) in camu-camu fruits. According to Chirinos et al. (2010) the vitamin C of camu-camu fruits depends on the maturity stages. These authors showed that fully matured (red stage) camu-camu fruits contained 2010 ± 65 mg/100 g fresh matter of vitamin C whereas at full green stage it was 2280 ± 34 mg/100 g fresh matter. Vitamin C content in camu-camu was higher than other seventeen nontraditional Brazilian fruits such as acerola (1357 ± 9.5 mg/100 g fresh matter), acai, and assai (84.0 ± 10 mg/100 g fresh matter) (Rufino et al. 2010). 3. Health benefit properties of camu-camu fruits 3.1. Biological effects of polyphenol Polyphenol compounds such as anthocyanins, flavonoids and phenolic acids are responsible to reduce oxidative stress (Inoue, Komoda, Uchida, & Node 2008; Liu, Qiu, Ding, & Yao 2008). It has already been proven that different exotic fruits such as durian, snake fruits mangosteen, mango, kiwi, and avocado significantly reduced the plasma lipids (total cholesterol, low-density lipoprotein cholesterol and triglycerides) (Gorinstein et al. in press). Camu-camu fruits are rich in polyphenols which could be used to retard or prevent various human diseases. However, there are few evidence in in vivo studies on the polyphenol of camu-camu fruits. 3.2. Antioxidative and anti-inflammatory properties Inoue et al. (2008) found powerful antioxidative and antiinflammatory properties of camu-camu in vivo in humans. Inoue et al. (2008) pointed out that camu-camu had higher antioxidative and antiinflammatory properties as compared to the vitamin C tablets. These authors suggested that vitamin C or other antioxidant components such as anthocyanins and β-carotene may affect on antioxidative and antiinflammatory properties of camu-camu fruits. 3.3. Antimicrobial activity Recently a Japanese research group (Myoda et al. 2010) investigated the effects of different concentrations of MeOH extract of camucamu juice residue such as seed and peel on various antimicrobial such as Staphylococcus aureus, Escherichia coli and Saccharomyces cerevisiae. This research group mentioned that the extract of seed and

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