International Journal of Health Sciences and Research www.ijhsr.org ISSN: 2249-9571

Review Article

Jabuticaba Fruit Peel: Better Than the Pulp?

Flavia M. V. Farinazzi-Machado, Adriana M. R. Fiorini

Faculty of Food Technology of Marilia (FATEC) Marilia/SP – Brazil Av. Castro Alves, 62, Marilia 17506-000, SP, Brazil

Corresponding Author: Flavia M. V. Farinazzi-Machado

ABSTRACT

The native Brazilian Jabuticaba fruit has a reddish, almost black peel and white pulp, and it is rich in vitamins, minerals and phenolic compounds. The peels are considered to be household and industrial waste in the manufacture of juices and pulps, but they have significant concentrations of phytochemicals, especially anthocyanins. The objective of this review was to gather references in the literature demonstrating the presence of important phytochemicals in the Jabuticaba fruit peel, its beneficial metabolic and physiological effects, and its use in processed foods for human consumption. To this end, the Pubmed, Google Scholar, Scielo and Lilacs databases were used to include in this review the relevant publications written mostly in the last ten years, although some older article citations and three technical papers were required to classify and characterize the genre.

Key words: Myrciaria – peels – phytochemicals – antioxidant – food

INTRODUCTION generally have a single seed, but they can The Jabuticaba tree is a Myrtaceae have up to four seeds per fruit. [5] native to Brazil, which grows from the far The 'Sabará' jabuticaba fruit south to the far north of the country. With occupies the largest cultivated area in Brazil the change in botanical nomenclature and bears fruits of 20 to 30 mm in diameter suggested by Sobral [1] due to the presence and a smooth and juicy pulp with a sub-acid of seeds with separated cotyledons and taste. [6] According to Mota et al., [7] the congested inflorescences and cauliflora, fruits have a small pedicel and are produced which are typical characteristics of the in large quantities along the trunk or in the Plinia genus, there is still disagreement axil of already abscised leaves (Figure 1). regarding the classification of the species: Myrciaria spp O. Berg (1854) or Plinia spp. (O. Berg) Kausel (1956). The main species discussed in the literature, considering the first classification, are Myrciaria cauliflora and M. jabuticaba, and the species M. jabuticaba (Vell) Berg (Jabuticaba Sabará) and the Plinia trunciflora and P. Cauliflora stand out in the second classification. [2-4] These plants produce globose berries with a reddish, almost black peel and a mucilaginous white pulp. The fruits Figure 1. Fruits of Myrciaria cauliflora

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The fruit pulp has mean values directly influenced by the expressive ranging from 14.86 mg 100-1g to 42.34 mg presence of anthocyanin compounds, 100-1g for vitamin C and minerals, including chemically classified as flavonoids, which iron, calcium, phosphorus and potassium. are the main natural pigments for the colors [8,9] Some studies have also found the pink, red, violet and blue in vegetables, presence of phenolic compounds (408.9 mg fruits, flower petals and leaves. [17, 18] 100-1g and 460.80 mg 100-1g) in the pulp of According to Abe et al., [19] the the jabuticaba fruit. [10, 11] anthocyanin concentrations in jabuticaba The Jabuticaba fruit can be fruit peels increase during the ripening consumed both in natura and in processed process of the fruits, with the presence of form as jellies, jams, brandy, liquor, wine these compounds not being identified in the and vinegar. [12] In the manufacture of jams seeds and pulp of this fruit during the and fermented products, the peels and seeds ripening stages. of the fruits represent around 50% of the According to Giusti and Wrolstad, total weight and are considered to be waste, [20] several factors influence the stability of being discarded by the food industry. [13] anthocyanins, such as their chemical However, studies have shown that structure (number of hydroxyls, degree of the jabuticaba fruit peels have significant methylation and glycosylation); pH; levels of phytochemical compounds with temperature; light; the presence of oxygen; functional and technological properties, enzymatic degradation; and interactions which are currently being included in with other food components, such as processed foods. [14-16] The objective of this ascorbic acid, sugars, metal ions and review was to show that several references copigments. Anthocyanins are very soluble in the literature have demonstrated the in polar solvents, being easily extracted with presence of important phytochemical water, methanol and ethanol. [21] compounds in the Jabuticaba fruit peel, in In a study conducted by Lima et al., addition to its beneficial metabolic and [5] the peel of the Sabará variety had the physiological effects and its use in highest levels of polyphenols (11.99 g 100- processed foods for human consumption. 1g) followed by the Paulista variety (11.18 g 100-1g). Cyanidin 3-O-glucoside is the METHODS major pigment in the peel, followed by This literature review was carried delphinidin 3-glucoside, malvidin and out through the search of relevant scientific malvidin-3-O-glucoside. [21,22] Through publications in the Portuguese and English mass spectrometry, Calloni [23] identified languages in the Pubmed, Google Scholar, that the mass of the jabuticaba fruit peel not Scielo and Lilacs databases, mostly written only contained the cyanidin 3-O-glucoside in the last ten years, although older article compound in greater quantities, but also citations and three technical papers were kaempferol, hexadecanoic acid and required for the classification and octadecanoic acid. Plaza et al. [24] observed characterization of the genre. the presence of kuromanin, myrtillin, casuarictin, casuarinin, ellagic acid, RESULTS AND DISCUSSION pedunculagin and a non-identified phenolic Phytochemicals in the Jabuticaba fruit compound in the jabuticaba fruit peels. peels Extraction of the jabuticaba fruit The coloring of the jabuticaba fruit peels with solutions of 4:1 methanol-water, peel has intensified the scientific research 4:1 ethanol-water, 3:2 ethanol-water and 3:2 into the phytochemical compounds present acetone-water, using the Folin-Denis in this waste for some years now, since it method, revealed high phenolic compound has always been discarded by the juice & contents (18.95; 14.06; 12.93; 11.99 mg -1g pulp industry. The color of the peel is of gallic acid, respectively) in a study by

International Journal of Health Sciences & Research (www.ijhsr.org) 283 Vol.7; Issue: 9; September 2017 Flavia M. V. Farinazzi-Machado et al. Jabuticaba Fruit Peel: Better Than the Pulp?

Araújo et al. [25] In a study by Lenquiste et measured through DPPH (2.2-diphenyl-1- al., [26] the aqueous extract of lyophilized picrylhydrazyl), ABTS (2.2 azinobis (3- peels had higher levels of gallic acid when ethylbenzothiazoline-6-sulfonic acid) compared to the methanolic extract, but in diammonium salt), FRAP (ferric reducing this latter extract the concentration of ellagic antioxidant power) and ORAC (oxygen acid was higher than in the aqueous extract. radical absorbance capacity test) tests in a As already mentioned, the study by Lenquiste et al. [26] The study phytochemical levels also vary according to revealed that, in the DPPH and ORAC the degree of ripening. The jabuticaba fruit trials, the antioxidant capacity of the peels of the Sabará cultivar had high methanolic extract was more efficient concentrations of ellagic acid that ranged (346.77 and 317.98 Trolox μM g-1, from 22.5 ± 1.3 g kg-1 to 43.95 ± 0.24 g kg-1, respectively) than the aqueous extract. The depending on the ripeness stage of the fruit. results of the FRAP trials were statistically These values were higher than the levels of similar for both extracts, and in the ABTS ellagic acid observed in the pulp of the trials, the antioxidant activity showed higher jabuticaba fruits (4.6 ± 0.2 g kg-1 to 36.8 ± values in the aqueous extract (223.10 Trolox 2.5 g kg-1) in a study conducted by Abe et μM g-1). al. [19] In a study conducted by Lima et al., In addition to the significant levels [21] the jabuticaba fruit peels of the Sabará of phenolic compounds, the jabuticaba fruit variety had a higher antioxidant activity peels are also rich sources of food fibers. In (1.56 mmol L-1 g-1 in Trolox equivalents) a study by Lima et al., [5] the peel had when compared to the Paulista variety (2.06 expressive levels of total fibers: 33.80 g mmol L-1 g-1 in Trolox equivalents). The 100-1g in the Paulista and 33.23 g 100-1g in pulps and seeds had the lowest antioxidant the Sabará variety, with the largest activity in both varieties, while the values percentage being insoluble fibers. were intermediate in the whole fruit. According to Araújo et al., [25] potassium is The hydroalcoholic extract of the the element found in greater proportion in jabuticaba fruit peels showed significant the peel of this fruit, followed by antioxidant activity, with a DPPH radical phosphorus, calcium, magnesium and iron. sequestering percentage from 83.6% to In vitro and in vivo antioxidant activity 91.88% in a study conducted by Pitz et al. Oxidative stress is a condition in [31] which an imbalance between the production According to Kumar and Pandey, [32] of free radicals and endogenous antioxidant the free radical sequestering capacity is defenses occurs, culminating in the decrease attributed mainly to the high reactivity of of the antioxidant capacity of the cells. [27] the hydroxyl substituents of the flavonoid This imbalance has been implicated in a structure. The presence of hydroxyl in number of patho-physiologic processes position on the ring, B 3' and 4', is the most related to many chronic and degenerative significant factor in the capture of nitrogen disorders. Studies have shown that the species (RNS) and reactive oxygen species ingestion of phytochemical compounds has (ROS) because it confers a high stability to a protective effect against oxidative the formed radical. The presence and the processes. [28-30] In this context, the total number of hydroxyl groups, therefore, jabuticaba fruit peels emerge as potential can substantially influence the various alternatives for the prevention and treatment antioxidant activity mechanisms. of disorders related to oxidative stress, since The antioxidant activity of they are important sources of the already lyophilized jabuticaba fruit peels was tested described phenolic compounds. in male Wistar rats for a period of 28 days. The antioxidant capacity of the [33] The study revealed that the dose used to extracts of the jabuticaba fruit peels was achieve maximum antioxidant capacity was

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2% (20 g kg-1) of lyophilized jabuticaba cytotoxic properties in the animals under fruit peels), with plasma ORAC values of study. 22.96 Trolox equiv μL-1, representing an In a study by Araujo et al., [40] antioxidant capacity 1.3 times greater than experimental models treated with a diet rich the control group. in fats and jabuticaba fruit peel flour in In a study by Plaza et al., [24] different concentrations had their levels of ellagitannins and gallotannins (hydrolysable total cholesterol, plasma triglycerides and tannins) were the phenolic class that glucose levels significantly reduced after contributed most to the total antioxidant four weeks of treatment. capacity of M. jabuticaba (43%), followed In a study by Batista et al., [41] the by anthocyanins (38%), other unidentified serum levels of triglycerides and total phenolic compounds (12%), ellagic acid and cholesterol observed in groups of animals derivatives (6%) and flavonols (1%), when treated with 4% of lyophilised jabuticaba analyzed through high-performance liquid fruit peel flour not only reduced, but a chromatography. reduction in hyperinsulinemia and hepatic Red wine made with the jabuticaba inflammation was also observed. These fruit had a superior antioxidant activity than authors also observed in this study that the wine made with grapes when using the daily consumption of bioactive compounds carotene/linoleic acid system in a study from jabuticaba fruit peels improved the conducted by Barros et al., [34] who obtained antioxidant status of the plasma, even in the oxidation inhibition values close to BHT (a conditions of 12 hours of fasting to which synthetic antioxidant used in the food the animals were subjected. industry), with an inhibition of around 65%. On the other hand, the This study also revealed that jabuticaba administration of a feed with lyophilized wines are good free radical sequesters. jabuticaba fruit peels did not exert a Physiological and metabolic effects protective effect on the weight gain induced In popular medicine, jabuticaba fruit by a diet rich in fats, on hyperleptinemia, peels are often used for the treatment of and on the glucose intolerance of the rats. diarrhea and skin irritations, in The supplementation was effective, inflammations of the intestines and however, in reducing insulin resistance and hemoptysis, in addition to traditionally in the expression of such pro-inflammatory showing anti-asthmatic and anti- cytokines as IL-1b and IL-6 in all rats inflammatory properties of the amigdalas in treated with jabuticaba. [42] the decoction from). [35-37] Currently, some Lobo de Andrade et al. [43] in vivo studies have shown the metabolic conducted studies with hydroalcoholic and antimutagenic properties of jabuticaba extracts of M. cauliflora in experimental fruit peel extracts. models, revealing that the intravenous Lage et al. [38] observed that the infusion of the extract produced addition of 3% of jabuticaba fruit peel flour hypotension and vasodilation in the rats, increased the HDL-c (high density increasing the flow of blood without lipoprotein) plasma levels by 20.23% in changes in heart rhythm. experimental models, in addition to Calloni [44] found in his in vitro reducing hepatic lipid peroxidation by 50% studies that the jabuticaba fruit peel extract when compared to the control group. These (P. trunciflora) minimized the increase in findings corroborate the results from lipid peroxidation, the levels of nitric oxide [39] Lenquiste et al., who treated obese rats and the loss of viability induced by H2O2 in with jabuticaba fruit peels and observed an fibroblasts of the human lung, revealing the increase in the HDL-c levels and a ability to reduce oxidative/nitrosactive significant improvement in insulin damage via modulation of the mitochondrial resistance, with the doses used not showing function in mammalian cells.

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Studies using an ethanolic extract of antioxidant activity with jabuticaba fruit the jabuticaba fruit peel demonstrated an in peels. vitro anti-proliferative effect on tumor cells Dessimoni-Pinto et al. [50] developed of the prostate (PC-3) and leukemia (K- jellies with jabuticaba fruit peels, showing 562), and an in-vivo antimutagenic effect in the presence of total phenolic compounds mice treated with the extract of the (148.00 mg to 216.44 mg 100g-1 of gallic jabuticaba fruit peel, administered by acid) and flavonoids (10.42 mg 12.10 gavage for a period of 15 days. [45] mg.100 g-1 of catechin), in addition to an acceptability index of 80% among the Adding jabuticaba fruit peels to food tasters who performed the sensory Considering the results of the evaluation of the developed jellies. scientific studies, the jabuticaba fruit peels Baldin et al. [15] added have been incorporated in food products in microencapsulated extracts of jabuticaba order to make use of the fruit's typical fruit peels to fresh sausages, and observed coloring phytochemical pigments and the antioxidant and anti-microbial effects during beneficial functional properties in its a period of 15 days under refrigeration, in composition. addition to an improvement of some sensory Color is often lost during the food characteristics of the products. Almeida et processing stages, and dyes are added to al., [51] on the other hand, did not observe these products in order to restore the microbial stability during storage when original color and/or make them more adding jabuticaba peel extracts to Bologna- visually appealing. The anthocyanins type sausages, but the peels did positively present in the jabuticaba fruit peels are a influence the oxidative stability of the viable alternative to provide the color red in sausages. foods from natural sources, in addition to Pereira et al. [16] studied the being soluble in water, which facilitates interfering effects of incorporating the their incorporation in aqueous systems. [46] extract obtained by the supercritical According to Rosso, [47] however, there are extraction of jabuticaba fruit peels obtained limitations to the commercial application of from jelly manufacturing waste, in the anthocyanins due to their stability, which formulation of a probiotic Petit suisse. The depends, among other factors, on the study revealed that the samples with the chemical structure of the pigments, pH, jabuticaba extract had better viscosity after temperature, the presence of oxygen, light 28 days of storage, but the scores awarded and the concentrations of ascorbic acid in by the tasters in the sensory analysis were the food. between 4.68 (flavor) and 6.25 (aroma), Silva et al. [48] extracted food which was lower than the scores attributed colorings from the jabuticaba fruit peel to the commercial samples. Faria et al. [52] through atomization in a mini spray drier observed good stability in the growth of system, conveyed with the stabilizers Lactobacillus ssp in fermented milk with the maltodextrin and gum arabic. Through addition of lyophilized jabuticaba fruit colorimetric analysis and the determination peels. of anthocyanins, they found, however, that Jabuticaba fruit peel flour was also there was a significant degradation of added to cookie dough in a study by Ferreira anthocyanin pigments in the colorings et al. [53] The researchers found that the flour exposed to light at an average temperature had a positive influence on texture and of 25 ºC. Santos et al., [49] on the other hand, softness, but at concentrations above 10% in used extraction methods with low-cost the formulations, they did not result in good ultrasonic irradiation and obtained a low acceptability regarding taste, sweetness and degradation of anthocyanins and a higher acidity. Padilha and Basso, [54] on the other hand, observed a high acceptability index

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(87.1%) in cookies made with dehydrated 4. Zerbielli L, Nienow AA, Dalacorte L, jabuticaba fruit peels from industrial waste. Jacobs R, Daronch T. Physical and In cereal bars, the addition of dried and chemical diversity of jaboticaba trees ground jabuticaba fruit peels in different fruit on a site of natural occurrence. concentrations also revealed high levels of Braz J Fruits. 2016; 38(5):107-116. 5. Lima AJB, Corrêa AD, Alves APC, acceptability, especially for the attributes Abreu CMP, Dantas-Barros AM. color, taste and texture, in a study by Appelt [55] Caracterização química do fruto et al. jabuticaba (Myrciaria cauliflora Berg) e Isotonic drinks were prepared with de suas frações. Arch Latin Nutricion. extracts from the jabuticaba fruit peels in a 2008; 58(4): 416-425. study conducted by Cipriano, [56] and with 6. Magalhães MM, Barros RS, Finger FL. the ultrafiltration permeate of the milk with Changes in structural carbohydrates in the addition of anthocyanic extracts from developing fruit of Myrciaria the jabuticaba fruit peels in a study by jabuticaba. Sci Horticulturae. 1996; Valente. [57] In the first study, the drink had 66(1-2): 17-22. 9.44 mg L-1 of anthocyanins and showed no 7. Mota WF, Salomão LCC, Pereira MCT, Cecon PR. Influência do tratamento significant difference in the sensory pós-colheita com cálcio na conservação acceptance when compared to commercial de jabuticabas. Braz J Fruits. 2002; beverages, revealing a high antioxidant 24(1): 49-52. activity through the radical cation ABTS 8. Pereira MCT, Salomão LCC, Mota WF, test. In the second study, the anthocyanins Vieira G. Atributos físicos e químicos content was 15.98 mg L-1 and the de frutos de oito clones de antioxidant activity through the radical jabuticabeiras. Braz J Fruits. 2000; 22: ABTS and DPPH tests were 2.43 and 2.72 16-21. μM, Trolox equivalent mL-1, respectively. 9. Oliveira AL, Brunini MA, Salandini Concluding remarks CAR, Bazzo FR. Caracterização Jabuticaba fruit peels have tecnológica de jabuticabas ‘sabará’ provenientes de diferentes regiões de significant concentrations of phytochemical cultivo. Braz J Fruits. 2003; 25(3): 397- compounds, especially anthocyannins and 400. ellagic acid, and they have shown 10. Assis SA, Vellosa JC, Brunetti IL, antioxidant effects and hypolipidemic and Khalil NM, Leite KM, Martins AB, antimutagenic activity in in vitro Oliveira OM. Antioxidant activity, experiments and in experimental models. As ascorbic acid and total phenol of exotic such, jabuticaba fruit peels may have great fruits occurring in Brazil. Inter J Food potential as a functional ingredient Sci Nutrition. 2009; 60(5): 439-48. incorporated into processed foods for 11. Vieites RL, Daiuto ER, Moraes MR, human consumption. Neves LC, Carvalho LR. Physiochemical, biochemistry and REFERENCES functional characterization of jabuticaba 1. Sobral M. Changes in Nomenclatures stored under different temperatures. Plinia (Myrtaceae). Bulletin of the Braz J Fruits. 2011; 33(2): 362-375. Botanical Museum of Curitiba, Curitiba, 12. Brunini MA, Coelho CV. Influência de Brazil, 1985. p. 1-4. embalagens em jabuticabas 'Sabará. 2. Mattos JLR. Frutíferas nativas do 'Rev Nucleus. 2005; 3(1): 1-8. Brasil. São Paulo: Nobel, 1983. 92p 13. Asquieri ER, Silva ADM, Cândido MA. 3. Manica I. Frutas nativas, silvestres e Aguardente de jabuticaba obtida da exóticas 1: técnicas de produção e casca e borra da fabricação de mercado: abiu, amora-preta, araçá, fermentado de jabuticaba. Braz J Food bacuri, biribá, carambola, cereja-do-rio- Technol. 2009; 29(4): 896–904. grande, jabuticaba. Porto Alegre: Cinco 14. Wu SB, Long C, Kennelly EJ. Continentes. 2000. 327 Phytochemistry and health-benefits of jaboticaba, an emerging fruit crop from

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How to cite this article: Farinazzi-Machado FMV, Fiorini AMR. Jabuticaba fruit peel: better than the pulp? Int J Health Sci Res. 2017; 7(9):282-290.

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International Journal of Health Sciences & Research (www.ijhsr.org) 290 Vol.7; Issue: 9; September 2017