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Passiflora edulis Peel Flour and Health Effects
C H A P T E R
20 Passiflora edulis Peel Flour and Health Effects Milena Morandi Vuolo*, Glaucia Cariello Lima†, and Ma´rio Roberto Maro´stica Junior* *Department of Food and Nutrition, Faculty of Food Engineering, University of Campinas, Sa˜o Paulo, Brazil † Nutrition School-Federal University of Goias, Goi^ania, Brazil
O U T L I N E Introduction
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Passion Fruit
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Passion Fruit Peel: Chemical Aspects and Bioactive Compounds 250 Effects of Passion Fruit Peel on Gut Health
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Effects of Passiflora edulis Peel Flour in Metabolic Parameters
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Conclusions
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Acknowledgments
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References
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INTRODUCTION Over the years, the fruit juice industry has become very important economically.1 In 2015, global juice and drink consumption surpassed 80 billion liters. The projections for this market in the future are even greater, reaching 105 billion liters by 2020 (according to the specialist food-and-drink consultancy Zenith International). The expansion of juice production creates a huge amount of waste. This agroindustrial waste has a substantial economic and environmental impact, causing disposal problems due to the high costs related to drying, storage, and shipment, and can pollute the environment.2 Fruits from tropical and subtropical zones have smaller amounts of edible portions and are known to produce higher ratios of wastes (more commonly called by-products) than those from temperate zones. Such fruits generate a significant amount of waste material, such as peels, seeds, and stones.3 These residues are also sources of fibers and many bioactive compounds, which also may be useful to the food industry as functional ingredients, which also helps in solving environmental problems resulting from its disposal.4–10 In this context, the processing of Passiflora edulis Sims (mainly the variety P. edulis Sims f. floricarpa, also known as yellow passion fruit) results in large quantities of residues due to its large cultivation and juice production, especially in Brazil. This plant is grown mainly in Brazil, Colombia, and Ecuador and has high economic importance in these countries.11 Brazil is the largest producer and consumer of P. edulis f. flavicarpa in the world (accounting for 60% of the total world production). To solve the huge amount of residues generated by the juice industry, the study of P. edulis Sims by-products as a functional ingredient is an interesting and feasible approach.12 P. edulis Sims peel flour (PESPF) (yellow and purple varieties) provides significant amounts of phenolic compounds, showing antioxidant capacity and high dietary fiber content.4, 9, 10, 13–16 Studies have demonstrated the ability of PESPF to improve some health issues, such as hypertension, glycemia, dyslipidemia, and obesity complications.4, 7, 17–20
Flour and Breads and their Fortification in Health and Disease Prevention https://doi.org/10.1016/B978-0-12-814639-2.00020-4
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© 2019 Elsevier Inc. All rights reserved.
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20. PASSIFLORA EDULIS PEEL FLOUR AND HEALTH EFFECTS
The interest in sources of bioactive compounds is linked to the decrease in oxidative stress, which is commonly seen as a key factor in several chronic diseases. Fibers, mainly soluble fibers like pectin, can control glycemia, improves lipid profiles, and produces short-chain fatty acids, which in turn are related to anti-inflammatory effects.21, 22 Shortchain fatty acids lower colonic pH, which can affect the microbiota composition, leading to an improvement of gut health.23, 24 This chapter will approach the chemical aspects, bioactive compounds, and health effects of PESPF.
PASSION FRUIT The genus Passiflora belongs to the Passifloraceae family and Passiflorales order,25 and it encompasses about 500 species distributed mainly in the warm temperate and tropical regions of America, Asia, Australia, and tropical Africa.26 Brazil and Colombia account for approximately 30% of Passiflora species, being centers of diversity.11 The Passiflora genus is the most economically exploited of the Passifloraceae family.27 The most widespread species are P. edulis Sims, which includes such varieties as yellow passion fruit, purple passion fruit, and sour passion fruit; and Passiflora alata, while only sporadic reports are available on other species of Passiflora.28, 29 Passiflora is an exotic genus, usually used for its fruits, derivatives, and as a medicinal plant. Also, many of these species are still cultivated for their beautiful ornamental flowers, which have great ornamental value in the United States and certain European countries.11, 30 The P. edulis Sims species is the most popular, being widely used by the food industry for juice and pulp production. In the America and Europe, their leaves are applied as sedatives or tranquilizers. The fruits are a berry type and come in many shapes, such as globular, ovoid, and oblong. They have a sour taste and a strong and exotic aroma, and the weight varies from 30 to 300 g per fruit, diameter from 4.9 to 9 cm, and length from 4.3 to 7.2 cm. The color ranges diversely, being purple, yellow, reddish, and greenish.25 The passion fruit is basically composed of epicarp, which corresponds to the external layer; mesocarp, which is the white internal layer; endocarp or pulp; fresh mucilage; and seeds.25 P. edulis f. flavicarpa is commonly called yellow passion fruit, yellow granadilia, or pomme liane jaune;31 and P. edulis Sims edulis is known as purple passion fruit or purple granadilia.26 Brazil produced 703,489 tons of P. edulis Sims in 2016, mainly concentrated in the northeastern part of the country; this constitutes approximately 70% of the national crop according to the Brazilian Institute of Geography and Statistics (IBGE 2016).32 P. edulis f. flavicarpa is the variety on which the world’s commercial production is based.33 The cultivation is focused on juice and pulp industrial production, especially due to its more acidic flavor and higher financial income. In order to get the citrus pulp, peel, and bagasse (seeds and mucilage) are separated, resulting in by-products from industrial processing. The seeds and peels represent up to 26% and 50% of the fruit’s weight, respectively, generating huge amounts of waste.11 In many situations, this amount of biomass is used in animal feed or as fertilizers.33 Peels account for 50% of the fruit’s weight and are also used for flour production;25 furthermore, they have been used by industry as an alternative to pectin.13, 34 The seeds represent 4%–12% of passion fruit and contain around 30% of the oil in the plant. This oil is extracted for cosmetic production.35 The exploitation of by-products brings economic and environmental advantages, generating income through the formulation of products with high added value and avoiding the inappropriate discard of biomass into the environment.25 Despite current efforts toward the reutilization of industrial residues, large amounts of passion fruit peels remain underutilized. Efforts have been under way to find new uses for passion fruit peel flour.33 In the past decades, much progress has been made, including findings related to nutritional composition, bioactive molecules, and their correspondence with health benefits.33
PASSION FRUIT PEEL: CHEMICAL ASPECTS AND BIOACTIVE COMPOUNDS Studies revealed that PESPF presents low caloric value and is abundant in potassium (K) and also has significant iron (Fe), zinc (Zn), and manganese (Mn) content (Table 1). Such micronutrients are important for the metabolism, and P. edulis Sims peel can be considered as an alternative source for the intake of these minerals.33 Furthermore, PESPF is constituted for 60%–70% of fiber (nearly 20% of soluble fiber and 40%–50% of insoluble fiber) (Table 1).37, 40–42 Among the passion fruit fibers, pectin could be highlighted as a complex carbohydrate from plants with technological and physiological function.10, 37 Soluble fibers are able to form a gel in the surface intestinal absorption, complicating the transport of glucose, lipids, and cholesterol, which delays energy supply, avoiding its excessive consumption.43 Soluble fibers (pectins, hemicelluloses, and gums) or resistant starches are also substratum to fermentation by enteric bacteria, following by the production of short-chain fatty acids such as butyrate, propionate, and acetate.44, 2. FLOURS AND BREADS
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PASSION FRUIT PEEL: CHEMICAL ASPECTS AND BIOACTIVE COMPOUNDS 45
Butyrate represents a primary source of energy to colonocytes, and it may stimulate mucus secretion, vascular flow, barrier permeability, motility, and water and electrolyte absorption.45 Insoluble fiber improves the bowel transit time, whereas soluble fiber is involved in the reduction of both blood cholesterol and intestinal glucose absorption.10, 45 The interest in PESPF has increased due to its being a great source of phytochemical substances that could have therapeutic action as immunomodulators, anticarcinogens, and antioxidants46, 47 because of their high content of alcaloides, flavonoids, and carotenoids.15 Powders of residues by-products of passion fruit showed higher amounts of total phenolic compounds (TPC) compared to the pulp of this fruit—around five times more [103 10.4 and 20 2.6 mg gallic acid equivalent (GAE)].48 Methanolic extract of PESPF (the yellow variety) showed considerable amounts of the flavonoid isoorietin and high antioxidant power, due to its ability to decrease reactive oxygen species (ROS) production by activated neutrophils; furthermore, it was also able to lower myeloperoxidase activity, demonstrating effects on inflammation16 (Table 2). PESPF also showed phytic acid and tannis (Table 1). Albedo from P. edulis shows significant phenolic and flavonoid content in the methanol, water and dimethyl sulfoxide (DMSO) extract. TPC ranges from 0.64–1.86 mg GAE g1, and total flavonoid (TF) content ranges from 0.64 to 5.12 mg rutin equivalent (RE) g1 of sample. Isoorietin and isovitexin were identified in the albedo; the highest amount of such compounds was found in the DMSO extract.51 TABLE 1 Proximate, Phytochemical Composition, and Antioxidant Capacity of P. edulis Sims Peel Proximate
Fresh peel (g/100g)14
Peel flour (g/100 g)36
Peel flour (g/100 g)37
Moisture
84.21
7.42
Energy (kcal/g)
29.91
122.95
Protein (g)
0.67
8.87
3.94
Fat (g)
0.01
3.39
0.31
Carbohydrates (g)
6.78
14.24
79.39
Total dietary fiber (g)
4.33
60.08
65.22
Insoluble dietary fiber (g)
39.96
48.12
Soluble dietary fiber (g)
20.13
17.11
Soluble pectin Ash (g)
Peel flour (mg/g)9
Peel flour38
Peel flour39
9.48
4.85 0.57
6.00
6.88
MINERALS Calcium (mg) Iron (mg) Magnesium (mg)
44.51 0.89 27.82
Phosphorum (mg) Potassium (mg) Sodium (mg)
178.40 43.77
Zinc (mg)
0.32
Copper (mg)
0.04
PHYTOCHEMICALS Isoorietin Phytic acid Tannin
0.653 37.0 308.21
Cyanidin 3-O-glucoside
Qualitative analysis
Quercitin 3-O-glucoside
Qualitative analysis Continued
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20. PASSIFLORA EDULIS PEEL FLOUR AND HEALTH EFFECTS
Proximate, Phytochemical Composition, and Antioxidant Capacity of P. edulis Sims Peel—cont’d Fresh peel (g/100g)
Proximate
Peel flour (g/100 g)
Peel flour (g/100 g)
Peel flour (mg/g)
Peel flour
Edulic acid
Qualitative analysis
Catechin
Qualitative analysis
Epicatechin
Qualitative analysis
Kampferol-3-O-glucoside
Qualitative analysis
Kampferol
Qualitative analysis
Luteolin-8C-neohesperoside
Qualitative analysis
Luteolin-8C-neohesperoside
Qualitative analysis
Protocatechuic acid
Qualitative analysis
Prunasin
Qualitative analysis
Peel flour
Total phenolic compounds (mg GAE g-1)
4.67 0.38
Flavonoids (mg catechin-1)
1.17 0.05
DPPH (%)
29.6 0.66 to 46.35 0.85
FRAP
34.95 2.02 to 38.65 1.55
ORAC
40.83 1.75 to 68.58 0.06
DPPH, assay 2,2-diphenyl-1-picrylhydrazyl; FRAP; Ferric Reducing Antioxidant Power assay (μmol Trolox equivalent (TE) g1 of sample); ORAC, Oxygen Radical Absorbance Capacity (μmol TE g1 of sample).
TABLE 2
Therapeutic Properties of the Most Studied P. edulis Sims
P. edulis Sims
Extract
Bioactive compounds
Experimental model
Main results
References
P. edulis Sims f. flavicarpa
Methanolic extract
Isoorietin
Isolated neutrophils Antioxidant assay
Decrease ROS production and inflammation toward myeloperoxidase and on equine neutrophils
16
P. edulis Sims f. flavicarpa
Hot water extract
Not identified
Rats
Old rats were divided into two groups (control and fed with P. edulis peel flour); after 15 days, the experimental group showed lower antioxidant status in serum (ORAC assay) and lower lipid peroxidation in kidneys and higher in liver compared to the control
39
P.edulis Sims edulis
Methanolic extract
Cyanidin 3-O-glucoside, quercitin 3-O-glucoside and edulic acid
Humans
Human with stage 1 or 2 essential hypertension were treated with P.edulis Sims edulis extract pill (200 mg, twice a day) for 4 weeks showed a decrease in SBP and DBP compared to the control group
7
P. edulis Sims f. flavicarpa
Not evaluated
Not evaluated
Humans
P. edulis Sims f. flavicarpa peel flour intake (30 g/day–2 months) by type 2 diabetes mellitus patients improves insulin resitance
6
P. edulis Sims f. flavicarpa
Not evaluated
Not evaluated
Humans
P. edulis Sims f. flavicarpa peel flour intake (30 g/day–1 and 2 months) by women presenting dyslipedemia decrease total and LDL blood cholesterol concentration
49
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EFFECTS OF PASSION FRUIT PEEL ON GUT HEALTH
TABLE 2
Therapeutic Properties of the Most Studied P. edulis Sims—cont’d
P. edulis Sims
Extract
Bioactive compounds
Experimental model
Main results
References
P.edulis Sims edulis
Methanolic extract
Cyanidin-3O-glucoside, quercitin 3-O-glucoside and edulic acid
Humans
Purple passion fruit peel was able to decrease cardiovascular risk factors in type 2 diabetic subjects. A significant reduction in SBP and fasting and postprandial blood glucose levels was observed in the purple passion fruit– treated group (220 mg/day) after 16 weeks
18
P. edulis Sims f. flavicarpa
Not evaluated
Not evaluated
Rats
Diabetic rats fed on a diet (AIN93 M) supplemented with yellow passion fruit peel flour (5%) decrease the serum glucose level in 59%, reaching smilar values of the control group
41
P. edulis Sims f. flavicarpa
Not evaluated
Not evaluated
Rats
Ingestion ofpassion fruit peel flour by rats with 2,4,6-trinitrobenzenesulfonic acid-induced colitis protected the colon of animals from lipid peroxidation and improve antioxidant status in serum compared to the control
50
P. edulis Sims f. flavicarpa
Not evaluated
Not evaluated
Rats
Rats fed on a high-fat diet with passion fruit peel flour saw decreased adiposity and leptin level; increased CART, GLP1, hypothalamic cocaine expression, and improved insulin sensitivity
4
PESPF (yellow variety) extracted with boiled water showed amounts of TPC of 4.67 0.38 mg GAE g1 of sample and flavonoids of 1.17 0.05 mg catechin g1 of sample. The aqueous, methanolic/acetone, and ethanolic extracts of PESPF differed in the TPC range from 2.06 0.08 to 2.53 0.03, with the greater amount being water extract; for the 2,2-diphenyl-1-picryhydrazyl free radical (DPPH) (%) assay, the range was from 29.6 0.66 to 46.35 0.85; with the greater amount also being water extract; for the Ferric Reducing Antioxidant Power (FRAP) assay, the range was from 34.95 2.02 to 38.65 1.55 μmol Trolox equivalent (TE) g1 of sample, with the greater amount being methanolic/ acetone extract; and for the Oxygen Radical Absorbance Capacity (ORAC) assay, the range was from 40.83 1.75 to 68.58 0.06 μmol TE g1 of sample, with the greater amount being methanolic/acetone extract.39 Another study with the same sample was shown to have water extract flavonoid amounts of 1.17 0.05 mg catechin g1.38 PESPF (purple passion fruit) contains cyanidin 3-O glucoside, quercitin 3-O glucoside, and edulic acid7 as the major components; proto-catechuic acid, (–)-catechin, prunasin + acid glycoside, (+)-epicatechin, , kaempferol-3O-glucoside, luteolin-8-C-neohesperidoside, uteolin-8-C-digitoxoside, and kaempferol.52
EFFECTS OF PASSION FRUIT PEEL ON GUT HEALTH Dietary fiber intake has been shown to modulate gut microbiota by altering bacterial fermentation, colony size, and species composition. Consumption of fermentable dietary fiber provides substrates for microbial activity, but it will also increase the concentrations of fermentation products, such as short-chain fatty acids. Increased levels of shortchain fatty acids, in turn, lower the colonic pH, affecting the microbiota composition.23 Short-chain fatty acids, mainly butyrate, are important substrates for maintaining the colonic epithelium. Butyrate is the preferred fuel used by coloncytes, and the primary site of butyrate sequestration in the body is the gut epithelium. The short-chain fatty acids are related to several other positive health effects, including those related with management of obesity, glucose homeostasis, appetite, and dyslipidemia.36 The passion fruit pericarp (epicarp, the white part; and mesocarp, the yellow part) is rich in dietary fiber, both insoluble and soluble (mainly pectin).50 Although the studies indicate a large amount of dietary fiber in PESPF, its effect on gut health specifically remains little explored. The effect of passion fruit peel on colitis models is already reported.24, 53
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Long-term PESPF intake promoted improvement in antioxidant status, modulated the microbiota, and increased short-chain fatty acids in 2,4,6-trinitrobenzene sulfonic acid (TNBS)-induced colitis in rats.53 Also, PESPF intake exerted an intestinal anti-inflammatory effect and attenuated the colonic damage in the dextran sodium sulfate model of mouse colitis.24 The authors found reduced pro-inflammatory cytokine expression and an enhanced intestinal protective barrier, as shown by biochemical and molecular analyses. Further, they increase short-chain fatty acid formation (acetic acid and butyric acid) in vitro, thus supporting a prebiotic effect.24 The effects of PESPF intake were evaluated in rats as well.54 However, this study revealed elevated butyrate amount in cecal content without alteration in microbiota (Lactobacillus, Bifidobacterium, Enterobacteriaceae, and Total Aerobic Microbial Content). Also, the addition of PESPF in the diet did not change the antioxidant enzyme activity (glutathione reductase, glutathione peroxidase, and superoxide dismutase) and thiol groups (glutathione) in intestine tissue.54 These studies suggest that PESPF may improve gut health by increasing short-chain fatty acid production, especially on inflammatory bowel diseases. Therefore, more studies, especially clinical trials, on the effects of PESPF on the colonic fermentation and its consequences are necessary.
EFFECTS OF PASSIFLORA EDULIS PEEL FLOUR IN METABOLIC PARAMETERS PESPF has demonstrated positive effects in metabolic parameters such as control of glycemia, lipid profiles, and antioxidant status of tissues in animals and humans.37, 38, 40, 49, 55, 56 The ingestion of PESPF (the yellow variety) by diabetic rats decreased serum glucose level by 59% compared to the diabetic rats that did not receive treatment, reaching the normal glycemic amount (112.6 mg/dL) and an increment of 71% in hepatic glycogen was found (Fig. 1). Such results suggest that the PESPF mechanism that decreases blood glucose level is the transformation of blood glucose into liver glycogen.42 Similar results were showed in a clinical study in which the intake of 30 g/day of PESPF (the yellow variety) for 2 months by type 2 diabetes mellitus patients improves blood glucose fasting, homeostatic model assessment (HOMA-IR), and glycated hemoglobin (Fig. 1). Such results showed that supplementation of PESPF decreased insulin resistance in type 2 diabetes mellitus patients, suggesting that it could be used as an adjuvant therapy in conventional treatments.6 The same dose of PESPF (the yellow variety) showed to reduce blood cholesterol concentration in women with dyslipidemia. Reductions of 31.7 28 mg/dL and 47.0 29.5 28 mg/dL in total blood cholesterol concentration were observed after 30 and 60 days of treatment, respectively, and both were statistically significant (Fig. 1).57 Similar results
FIG. 1 The main effects of Passiflora edulis Sims peel flour intake in health parameters.
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EFFECTS OF PASSIFLORA EDULIS PEEL FLOUR IN METABOLIC PARAMETERS
FIG. 2
255
Possible action routes of Passiflora edulis Sims peel flour in the metabolic parameters.
were observed when HIV patients were treated with PESPF (the yellow variety) (30 g/day for 30 days) effectively reduced the cholesterol and triacylglyceride levels. Furthermore, the ingestion of 30 g/day of PESPF for 90 days ameliorated lipodystrophy on these patients.19 In another study, the intake of PESPF (the yellow variety) by rats fed on a high-fat diet counteracted cumulative body weight gain and increased hypothalamic cocaine and amphetamine-regulated transcript expression (CART), indicating regulation of satiety. Furthermore, PESPF, in the same study, decreased adiposity and leptin level whereas increased glucose-dependent insulinotropic polypeptide, adiponectin, glucagon-like peptide-1 (GLP-1), and improve insulin sensitivity4 (Fig. 1). In old rats, the ingestion of PESPF (the yellow variety) modulates in different ways the antioxidant tissue status, and in kidneys it decreases lipid peroxidation, in contrast to those found in liver, in which lipid peroxidation was higher than the control group.38 The possible explanation for the effects cited in the studies discussed up to now would be the presence of fiber in passion fruit peel (mainly pectin), which encourages gel formation, leading to changes in gastric-emptying time and intestinal transit, decreasing the velocity of absorption of carbohydrates and fat. In addition, it may inhibit micelle formation. Furthermore, this gel can complex with bile salts increasing cholesterol excretion21, 22 (Fig. 2). In addition, the fibers of the Passiflora peel may be fermented in the colon and, beyond the effects on bowel heath noted in this chapter, it might increase butyrate and propionate, two short-chain fatty acids that have shown antiinflammatory capacity, as they can kβ-activation.58, 59 Activated NF-kβ promotes the expression of TNF-α, inducible nitric oxide synthrase (iNOS), and cyclooxygenase (COX), which induce the action of lymphocytes, monocytes, and endothelial cells, triggering or increasing inflammation.58, 60 As for PESPF (the purple passion variety), positive effects on health parameters have been demonstrated in the scientific literature, such as oral administration of PESPF extract (150 mg/day) for patients with asthma for 4 weeks in a randomized, placebo-controlled, and double-bind study. It was found to improve wheeze, cough, and shortness compared to placebo. Such results are given for the presence of flavonoids in PESPF extract, which can decrease oxidative stress involved in the pathophysiology of asthma. They can inhibit histamine release, arachidonic acid metabolism, and cytokine production.5 In another study, humans with stage 1 or 2 essential hypertension were treated with PESPF extract pill (200 mg, twice a day) for 4 weeks, and they showed decreases in systolic blood pressure (SBP) and diastolic blood pressure (DBP) compared to the control group.7 PESPF (the purple passion variety) was also able to decrease cardiovascular risk factors in type 2 diabetic subjects. Such individuals had fasting blood glucose levels >140 mg/dL and SBP/DBP >140/90 mm Hg. A significant reduction in SBP, fasting blood glucose levels (22.6 + 10.8 mg/dL; P ¼ 0.4), and postprandial blood glucose levels (21.8 + 21.9 mg/dL; P ¼ 0.33) were observed in the PESPF-treated group (220 mg/day) after 16 weeks.18 Epidemiological studies have indicated a significant inverse association between dietary flavonoids and mortality from coronary heart disease.61 Flavonoids (mainly quercetin) have been shown to decrease arterial blood pressure, decrease aortic medial thickening, and attenuate cardiac hypertrophy in various animal models of cardiovascular disease.62, 63 Quercetin,
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luteolin, and cyanidin 3-O-glucoside can downregulate iNOS expression or scavenging of nitric oxide (NO), affecting the endogenous antioxidant system and leading to the modification of vascular tone and peripheral vessel resistance, thus lowering blood pressure (Fig. 2).7, 17 Therefore, including PESPF in the diet could increase the dietary intake of fiber and antioxidants. In addition, it could aid in the prophylaxis and therapeutic of some diseases. Furthermore, the aggregate value in by-products is of economic, scientific, and technological interest and may minimize the generation of industrial processed residuals and environment impact, as well as increasing industrial profitability.4, 8–10, 16, 19, 22, 33, 47, 48
CONCLUSIONS Food waste, or by-products, are a topic of concern in modern society. This represents not only a resource problem, but also environmental and economic ones. Thus, searching for solutions to incorporate by-products into the food industry is a concern as well. Emerging studies support the positive effect of PFF intake on gut health and other metabolic benefits. This fiber-rich by-product could fortify foods, increase their dietary fiber and other bioactive compound content, and create healthy products. However, clinical trials are needed to determine what dose is safe and effective for showing benefits to health.
Acknowledgments MRMJ acknowledges CNPq (301108/2016-1) and FAPESP (2012/12322-0 and 2015/50333-1) for financial support.
References 1. Singh GM, Micha R, Khatibzadeh S, et al. Global, regional, and national consumption of sugar-sweetened beverages, fruit juices, and milk: a systematic assessment of beverage intake in 187 countries. PLoS One 2015;10(8):1–21. https://doi.org/10.1371/journal.pone.0124845. 2. Papargyropoulou E, Lozano R, Steinberger JK, Wright N, Bin Ujang Z. The food waste hierarchy as a framework for the management of food surplus and food waste. J Clean Prod 2014;76:106–15. https://doi.org/10.1016/j.jclepro.2014.04.020. 3. Schieber A, Stintzing F, Carle R. By-products of plant food processing as a source of functional compounds—recent developments. Trends Food Sci Technol 2001;12(2001):401–13. https://doi.org/10.1016/S0924-2244(02)00012-2. 4. Lima GC, Vuolo MM, Batista ÂG, Dragano NRV, Solon C, Maróstica Junior MR. Passiflora edulis peel intake improves insulin sensitivity, increasing incretins and hypothalamic satietogenic neuropeptide in rats on a high-fat diet. Nutrition 2016;32(7-8):863–70. https://doi.org/10.1016/j. nut.2016.01.014. 5. Watson RR, Zibadi S, Rafatpanah H, et al. Oral administration of the purple passion fruit peel extract reduces wheeze and cough and improves shortness of breath in adults with asthma. Nutr Res 2008;28(3):166–71. https://doi.org/10.1016/j.nutres.2008.01.003. 6. de Queiroz M do SR, Janebro DI, da Cunha MAL, et al. Effect of the yellow passion fruit peel flour (Passiflora edulis f. flavicarpa deg.) in insulin sensitivity in type 2 diabetes mellitus patients. Nutr J 2012;11(1):89. https://doi.org/10.1186/1475-2891-11-89. 7. Zibadi S, Farid R, Moriguchi S, et al. Oral administration of purple passion fruit peel extract attenuates blood pressure in female spontaneously hypertensive rats and humans. Nutr Res 2007;27(7):408–16. https://doi.org/10.1016/j.nutres.2007.05.004. 8. de Oliveira AC, Valentim IB, Silva CA, et al. Total phenolic content and free radical scavenging activities of methanolic extract powders of tropical fruit residues. Food Chem 2009;115(2):469–75. https://doi.org/10.1016/j.foodchem.2008.12.045. 9. Zeraik ML, Yariwake JH, Wauters JN, Tits M, Angenot L. Analysis of passion fruit rinds (Passiflora edulis): isoorientin quantification by HPTLC and evaluation of antioxidant (radical scavenging) capacity. Quim Nova 2012;35(3):541–5. https://doi.org/10.1590/S0100-40422012000300019. 10. Yapo BM, Koffi KL. Dietary fiber components in yellow passion fruit rind—a potential fiber source. J Agric Food Chem 2008;56(14):5880–3. https://doi.org/10.1021/jf073247p. 11. Cerqueira-Silva CBM, Jesus ON, Santos ESL, Corr^ea RX, Souza AP. Genetic breeding and diversity of the genus Passiflora: progress and perspectives in molecular and genetic studies. Int J Mol Sci 2014;15(8):14122–52. https://doi.org/10.3390/ijms150814122. 12. López-Vargas JH, Fernández-López J, Perez-Álvarez JA, Viuda-Martos M. Chemical, physico-chemical, technological, antibacterial and antioxidant properties of dietary fiber powder obtained from yellow passion fruit (Passiflora edulis var. flavicarpa) co-products. Food Res Int 2013; 51(2):756–63. https://doi.org/10.1016/j.foodres.2013.01.055. 13. Liew SQ, Chin NL, Yusof YA. Extraction and characterization of pectin from passion fruit peels. Agric Agric Sci Procedia 2014;2:231–6. https:// doi.org/10.1016/j.aaspro.2014.11.033. 14. Córdova KRV, Gama TMMTB, Winter CMG, Kaskantzis Neto G, Freitas RJS. Características físico-químicas da casca do maracujá amarelo obtida por secagem. Bol do Cent Pesqui Process Aliment 2005;23(2):221–30. https://doi.org/10.5380/cep.v23i2.4491. 15. Zeraik ML, Yariwake JH. Quantification of isoorientin and total flavonoids in Passiflora edulis fruit pulp by HPLC-UV/DAD. Microchem J 2010; 96(1):86–91. https://doi.org/10.1016/j.microc.2010.02.003. 16. Zeraik ML, Serteyn D, Deby-Dupont G, et al. Evaluation of the antioxidant activity of passion fruit (Passiflora edulis and Passiflora alata) extracts on stimulated neutrophils and myeloperoxidase activity assays. Food Chem 2011;128(2):259–65. https://doi.org/10.1016/j.foodchem.2011.03.001. 17. Barbalho SM, Damasceno DC, Spada APM, et al. Effects of Passiflora edulis on the metabolic profile of diabetic wistar rat offspring. J Med Food 2011;14(12):1490–5. https://doi.org/10.1089/jmf.2010.0318.
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REFERENCES
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18. Raju IN, Reddy KK, Kumari CK, et al. Efficacy of purple passion fruit peel extract in lowering cardiovascular risk factors in type 2 diabetic subjects. J Evid Based Complementary Altern Med 2013;18(3):183–90. https://doi.org/10.1177/2156587213475627. 19. do Socorro Fernandes Marques S, RMF L, AUO S-S, et al. Evaluation of the effects of passion fruit peel flour (Passiflora edulis fo. flavicarpa) on metabolic changes in HIV patients with lipodystrophy syndrome secondary to antiretroviral therapy. Rev Bras Farmacogn 2016;26(4):420–6. https://doi.org/10.1016/j.bjp.2016.03.002. 20. Salgado JM, Dias Bombarde TA, Mansi DN, de Stefano Piedade SM, Molina Meletti LM. Effects of different concentrations of passion fruit peel (Passiflora edulis) on the glicemic control in diabetic mice. Cienc E Tecnol Aliment 2010;30(3):784–9. 21. Rahman S, Zhao A, Xiao D, Park E, Edirisinghe I, Burton-Freeman BM. A randomized, controlled trial evaluating polydextrose as a fiber in a wet and dry matrix on glycemic control. J Food Sci 2017;82(10):2471–8. https://doi.org/10.1111/1750-3841.13855. 22. Jesch ED, Carr TP. Food ingredients that inhibit cholesterol absorption. Prev Nutr Food Sci 2017;22(2):67–80. https://doi.org/10.3746/ pnf.2017.22.2.67. 23. Sawicki CM, Livingston KA, Obin M, Roberts SB, Chung M, Mckeown NM. Dietary fiber and the human gut microbiota: application of evidence mapping methodology (Cvd), 1-21. doi: https://doi.org/10.3390/nu9020125 24. Garrido-mesa J, Guerra-hernández E, Aparecida P, et al. Intestinal anti-inflammatory effects of Passiflora edulis peel in the dextran sodium sulphate. J Funct Foods 2016;26:565–76. https://doi.org/10.1016/j.jff.2016.08.020. 25. Viganó J, Martinez J. Trends for the application of passion fruit industrial by-products: a review on the chemical composition and extraction techniques of phytochemicals. Food Public Health 2015;5(5):164–73. https://doi.org/10.5923/j.fph.20150505.03. 26. Dhawan K, Dhawan S, Sharma A. Passiflora: a review update. J Ethnopharmacol 2004;94(1):1–23. https://doi.org/10.1016/j.jep.2004.02.023. 27. da Silva JK, Cazarin CBB, Colomeu TC, et al. Antioxidant activity of aqueous extract of passion fruit (Passiflora edulis) leaves: in vitro and in vivo study. Food Res Int 2013;53(2):882–90. https://doi.org/10.1016/j.foodres.2012.12.043. 28. Tommonaro G, Segura Rodríguez CS, Santillana M, et al. Chemical composition and biotechnological properties of a polysaccharide from the peels and antioxidative content from the pulp of Passiflora liguralis fruits. J Agric Food Chem 2007;55(18):7427–33. https://doi.org/10.1021/ jf0704615. 29. Benincá JP, Montanher AB, Zucolotto SM, Schenkel EP, Fr€ ode TS. Evaluation of the anti-inflammatory efficacy of Passiflora edulis. Food Chem 2007;104(3):1097–105. https://doi.org/10.1016/j.foodchem.2007.01.020. 30. Abreu PP, Souza MM, Santos EA, Pires MV, Pires MM, De Almeida AAF. Passion flower hybrids and their use in the ornamental plant market: perspectives for sustainable development with emphasis on Brazil. Euphytica 2009;166(3):307–15. https://doi.org/10.1007/s10681008-9835-x. 31. Sunitha M, Devaki K. Antioxidant activity of Passiflora edulis Sims leaves. Indian J Pharm Sci 2009;71(3):310–1. https://doi.org/10.4103/0250474X.56038. 32. IBGE—Produc¸ão Agrícola Municipal. IBGE—Produc¸ão Agrícola Municipal. http://www.cnpmf.embrapa.br/Base_de_Dados/index_pdf/ dados/brasil/maracuja/b1_maracuja.pdf; 2016. Accessed 5 May 2018. 33. Corr^ea RCG, Peralta RM, Haminiuk CWI, Maciel GM, Bracht A, Ferreira ICFR. The past decade findings related with nutritional composition, bioactive molecules and biotechnological applications of Passiflora spp. (passion fruit). Trends Food Sci Technol 2016;58:79–95. https://doi.org/ 10.1016/j.tifs.2016.10.006. 34. Seixas FL, Fukuda DL, Turbiani FRB, et al. Extraction of pectin from passion fruit peel (Passiflora edulis f. flavicarpa) by microwave-induced heating. Food Hydrocoll 2014;38:186–92. https://doi.org/10.1016/j.foodhyd.2013.12.001. 35. Malacrida CR, Jorge N. Yellow passion fruit seed oil (Passiflora edulis f. flavicarpa): physical and chemical characteristics. Brazilian Arch Biol Technol 2012;55(1):127–34. https://doi.org/10.1590/S1516-89132012000100016. 36. Lin HV, Frassetto A, Kowalik EJ, et al. Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS One 2012;7(4):1–9. https://doi.org/10.1371/journal.pone.0035240. 37. Lima GC, Vuolo MM, Batista AG, Dragano NRV, Solon C, Maróstica Junior MR. Passiflora edulis peel intake improves insulin sensitivity, increasing incretins and hypothalamic satietogenic neuropeptide in rats on a high-fat diet. Nutrition 2016;32(7-8):863–70. https://doi.org/10.1016/j. nut.2016.01.014. 38. da Silva JK, Cazarin CBB, Batista ÂG, Maróstica M. Effects of passion fruit (Passiflora edulis) byproduct intake in antioxidant status of Wistar rats tissues. LWT—Food Sci Technol 2014;59(2):1213–9. https://doi.org/10.1016/j.lwt.2014.06.060. 39. Cazarin CBB, da SJK, Colomeu TC, Zollner R de L, Maróstica Junior MR. Capacidade antioxidante e composic¸ão química da casca de maracujá (Passiflora edulis). Ci^encia Rural 2014;44(9):1699–704. https://doi.org/10.1590/0103-8478cr20131437. 40. Cazarin CBB, Da Silva JK, Colomeu TC, Zollner RL, Maróstica Junior MR. Antioxidant capacity and chemical composition of passion fruit peel (Passifl ora edulis j Capacidade antioxidante e composic¸ão química da casca de maracujá) (Passifl ora edulis). Cienc Rural 2014;44(9):1699–704. https://doi.org/10.1590/0103-8478cr20131437. 41. Zeraik ML, Pereira CAM, Zuin VG, Yariwake JH. Maracuj: Um alimento functional? Braz J Pharmacogn 2010;20(3):459–71. https://doi.org/ 10.1590/S0102-695X2010000300026. 42. Salgado JM, Bombarde TAD, Mansi DN, Piedade SMDS, Meletti LMM. Effects of different concentrations of passion fruit peel (Passiflora edulis) on the glicemic control in diabetic rat. Ci^encia e Tecnol Aliment 2010;30(3):784–9. https://doi.org/10.1590/S0101-20612010000300034. 43. Kabir AU, Samad MB, D’Costa NM, Akhter F, Ahmed A, Hannan JMA. Anti-hyperglycemic activity of Centella asiatica is partly mediated by carbohydrase inhibition and glucose-fiber binding. BMC Complement Altern Med 2014;14: https://doi.org/10.1186/1472-6882-14-31. 44. Thibault R, Blachier F, Darcy-Vrillon B, De Coppet P, Bourreille A, Segain JP. Butyrate utilization by the colonic mucosa in inflammatory bowel diseases: a transport deficiency. Inflamm Bowel Dis 2010;16(4):684–95. https://doi.org/10.1002/ibd.21108. 45. Giacco R, Costabile G, Riccardi G. Metabolic effects of dietary carbohydrates: the importance of food digestion. Food Res Int 2015;88:336–41. https://doi.org/10.1016/j.foodres.2015.10.026. 46. Zeraik ML, Yariwake JH, Wauters J-N, Tits M, Angenot L. Analysis of passion fruit rinds (Passiflora edulis): isoorientin quantification by HPTLC and evaluation of antioxidant (radical scavenging) capacity. Quim Nova 2012;35(3):541–5. https://doi.org/10.1590/S0100-40422012000300019. 47. Zeraik ML, Pereira CAM, Zuin VG, Yariwake JH. Maracujá: Um alimento functional? Brazilian J Pharmacogn 2010;20(3):459–71. https://doi.org/ 10.1590/S0102-695X2010000300026.
2. FLOURS AND BREADS
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20. PASSIFLORA EDULIS PEEL FLOUR AND HEALTH EFFECTS
48. Oliveira DA, Angonese M, Gomes C, Ferreira SRS. Valorization of passion fruit (Passiflora edulis sp.) by-products: Sustainable recovery and biological activities. J Supercrit Fluids 2016;111:55–62. https://doi.org/10.1016/j.supflu.2016.01.010. 49. de Queiroz M do SR, Janebro DI, da Cunha MAL, et al. Effect of the yellow passion fruit peel flour (Passiflora edulis f. flavicarpa deg.) in insulin sensitivity in type 2 diabetes mellitus patients. Nutr J 2012;11(1):89. https://doi.org/10.1186/1475-2891-11-89. 50. Lima GC, Vuolo MM, Batista TG, Dragano NRV, Solon C, Maróstica Junior MR. Passiflora edulis peel intake improves insulin sensitivity, increasing incretins and hypothalamic satietogenic neuropeptide in rats on a high-fat diet. Nutrition 2016;32(7-8). https://doi.org/10.1016/j. nut.2016.01.014. 51. López-Vargas JH, Fernández-López J, Perez-Álvarez JA, Viuda-Martos M. Chemical, physico-chemical, technological, antibacterial and antioxidant properties of dietary fiber powder obtained from yellow passion fruit (Passiflora edulis var. flavicarpa) co-products. Food Res Int 2013; 51(2):756–63. https://doi.org/10.1016/j.foodres.2013.01.055. 52. Chilakapati SR, Serasanambati M, Manikonda PK, Chilakapati DR, Watson RR. Passion fruit peel extract attenuates bleomycin-induced pulmonary fibrosis in mice. Can J Physiol Pharmacol 2014;92(8). https://doi.org/10.1139/cjpp-2014-0006. 53. Cazarin CBB, da Silva JK, Colomeu TC, et al. Passiflora edulis peel intake and ulcerative colitis: approaches for prevention and treatment. Exp Biol Med 2014;239(5):542–51. https://doi.org/10.1177/1535370214525306. 54. da Silva JK, Cazarin CBB, Bogusz Junior S, Augusto F, Maróstica Junior MR. Passion fruit (Passiflora edulis) peel increases colonic production of short-chain fatty acids in Wistar rats. LWT—Food Sci Technol 2014;59(2P2):1252–7. https://doi.org/10.1016/j.lwt.2014.05.030. 55. Batista ÂG, Ferrari AS, Da Cunha DC, et al. Polyphenols, antioxidants, and antimutagenic effects of Copaifera langsdorffii fruit. Food Chem 2016;197:1153–9. https://doi.org/10.1016/j.foodchem.2015.11.093. 56. Clifford MN, Scalbert A. Review ellagitannins—nature , occurrence and dietary burden. J Sci Food Agric 2000;80(November 1999):1118–25. https://doi.org/10.1002/(SICI)1097-0010(20000515). 57. Ramos AT, Cunha MAL, Sabaa-Srur AUO, et al. Uso de Passiflora edulis f. flavicarpa na reduc¸ão do colesterol. Brazilian J Pharmacogn 2007; 17(4):592–7. https://doi.org/10.1590/S0102-695X2007000400019. 58. Miles-Brown JP, Chassaing B, Gewirtz AT. Microbiota metabolism of soluble fiber protects against low-grade inflammation and metabolic syndrome. Gastroenterology 2015;148(4):S541. https://rsm.idm.oclc.org/login?url¼https://www.rsm.ac.uk.htm?url¼https://dialog.proquest.com/ professional/professional/docview/1682704799?accountid¼138535%0Ahttp://vw4tb4ff7s.search.serialssolutions.com?ctx_ver¼Z39.88-2004& ctx_enc¼info:ofi/enc:UTF-8&rfr_id. 59. Cani PD, Osto M, Geurts L, Everard A. Involvement of gut microbiota in the development of low-grade inflammation and type 2 diabetes associated with obesity. Gut Microbes 2012;3(4). https://doi.org/10.4161/gmic.19625. 60. Panasevich MR, Allen JM, Wallig MA, Woods JA, Dilger RN. Moderately fermentable potato fiber attenuates signs and inflammation associated with experimental colitis in mice. J Nutr 2015;145(12):2781–8. https://doi.org/10.3945/jn.115.218578. 61. Feliciano RP, Pritzel S, Heiss C, Rodriguez-Mateos A. Flavonoid intake and cardiovascular disease risk. Curr Opin Food Sci 2015;2:92–9. https:// doi.org/10.1016/j.cofs.2015.02.006. 62. Duarte J, Perez-Palencia R, Vargas F, et al. Antihypertensive effects of the flavonoid quercetin in spontaneously hypertensive rats. Br J Pharmacol 2001;133(1):117–24. https://doi.org/10.1038/sj.bjp.0704064. 63. Mu MM, Chakravortty D, Sugiyama T, et al. The inhibitory action of quercetin on lipopolysaccharide-induced nitric oxide production in RAW 264.7 macrophage cells. J Endotoxin Res 2001;7:431–8. https://doi.org/10.1179/096805101101533034.
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20 Passiflora edulis Peel Flour and Health Effects Milena Morandi Vuolo*, Glaucia Cariello Lima†, and Ma´rio Roberto Maro´stica Junior* *Department of Food and Nutrition, Faculty of Food Engineering, University of Campinas, Sa˜o Paulo, Brazil † Nutrition School-Federal University of Goias, Goi^ania, Brazil
O U T L I N E Introduction
249
Passion Fruit
250
Passion Fruit Peel: Chemical Aspects and Bioactive Compounds 250 Effects of Passion Fruit Peel on Gut Health
253
Effects of Passiflora edulis Peel Flour in Metabolic Parameters
254
Conclusions
256
Acknowledgments
256
References
256
INTRODUCTION Over the years, the fruit juice industry has become very important economically.1 In 2015, global juice and drink consumption surpassed 80 billion liters. The projections for this market in the future are even greater, reaching 105 billion liters by 2020 (according to the specialist food-and-drink consultancy Zenith International). The expansion of juice production creates a huge amount of waste. This agroindustrial waste has a substantial economic and environmental impact, causing disposal problems due to the high costs related to drying, storage, and shipment, and can pollute the environment.2 Fruits from tropical and subtropical zones have smaller amounts of edible portions and are known to produce higher ratios of wastes (more commonly called by-products) than those from temperate zones. Such fruits generate a significant amount of waste material, such as peels, seeds, and stones.3 These residues are also sources of fibers and many bioactive compounds, which also may be useful to the food industry as functional ingredients, which also helps in solving environmental problems resulting from its disposal.4–10 In this context, the processing of Passiflora edulis Sims (mainly the variety P. edulis Sims f. floricarpa, also known as yellow passion fruit) results in large quantities of residues due to its large cultivation and juice production, especially in Brazil. This plant is grown mainly in Brazil, Colombia, and Ecuador and has high economic importance in these countries.11 Brazil is the largest producer and consumer of P. edulis f. flavicarpa in the world (accounting for 60% of the total world production). To solve the huge amount of residues generated by the juice industry, the study of P. edulis Sims by-products as a functional ingredient is an interesting and feasible approach.12 P. edulis Sims peel flour (PESPF) (yellow and purple varieties) provides significant amounts of phenolic compounds, showing antioxidant capacity and high dietary fiber content.4, 9, 10, 13–16 Studies have demonstrated the ability of PESPF to improve some health issues, such as hypertension, glycemia, dyslipidemia, and obesity complications.4, 7, 17–20
Flour and Breads and their Fortification in Health and Disease Prevention https://doi.org/10.1016/B978-0-12-814639-2.00020-4
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© 2019 Elsevier Inc. All rights reserved.
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20. PASSIFLORA EDULIS PEEL FLOUR AND HEALTH EFFECTS
The interest in sources of bioactive compounds is linked to the decrease in oxidative stress, which is commonly seen as a key factor in several chronic diseases. Fibers, mainly soluble fibers like pectin, can control glycemia, improves lipid profiles, and produces short-chain fatty acids, which in turn are related to anti-inflammatory effects.21, 22 Shortchain fatty acids lower colonic pH, which can affect the microbiota composition, leading to an improvement of gut health.23, 24 This chapter will approach the chemical aspects, bioactive compounds, and health effects of PESPF.
PASSION FRUIT The genus Passiflora belongs to the Passifloraceae family and Passiflorales order,25 and it encompasses about 500 species distributed mainly in the warm temperate and tropical regions of America, Asia, Australia, and tropical Africa.26 Brazil and Colombia account for approximately 30% of Passiflora species, being centers of diversity.11 The Passiflora genus is the most economically exploited of the Passifloraceae family.27 The most widespread species are P. edulis Sims, which includes such varieties as yellow passion fruit, purple passion fruit, and sour passion fruit; and Passiflora alata, while only sporadic reports are available on other species of Passiflora.28, 29 Passiflora is an exotic genus, usually used for its fruits, derivatives, and as a medicinal plant. Also, many of these species are still cultivated for their beautiful ornamental flowers, which have great ornamental value in the United States and certain European countries.11, 30 The P. edulis Sims species is the most popular, being widely used by the food industry for juice and pulp production. In the America and Europe, their leaves are applied as sedatives or tranquilizers. The fruits are a berry type and come in many shapes, such as globular, ovoid, and oblong. They have a sour taste and a strong and exotic aroma, and the weight varies from 30 to 300 g per fruit, diameter from 4.9 to 9 cm, and length from 4.3 to 7.2 cm. The color ranges diversely, being purple, yellow, reddish, and greenish.25 The passion fruit is basically composed of epicarp, which corresponds to the external layer; mesocarp, which is the white internal layer; endocarp or pulp; fresh mucilage; and seeds.25 P. edulis f. flavicarpa is commonly called yellow passion fruit, yellow granadilia, or pomme liane jaune;31 and P. edulis Sims edulis is known as purple passion fruit or purple granadilia.26 Brazil produced 703,489 tons of P. edulis Sims in 2016, mainly concentrated in the northeastern part of the country; this constitutes approximately 70% of the national crop according to the Brazilian Institute of Geography and Statistics (IBGE 2016).32 P. edulis f. flavicarpa is the variety on which the world’s commercial production is based.33 The cultivation is focused on juice and pulp industrial production, especially due to its more acidic flavor and higher financial income. In order to get the citrus pulp, peel, and bagasse (seeds and mucilage) are separated, resulting in by-products from industrial processing. The seeds and peels represent up to 26% and 50% of the fruit’s weight, respectively, generating huge amounts of waste.11 In many situations, this amount of biomass is used in animal feed or as fertilizers.33 Peels account for 50% of the fruit’s weight and are also used for flour production;25 furthermore, they have been used by industry as an alternative to pectin.13, 34 The seeds represent 4%–12% of passion fruit and contain around 30% of the oil in the plant. This oil is extracted for cosmetic production.35 The exploitation of by-products brings economic and environmental advantages, generating income through the formulation of products with high added value and avoiding the inappropriate discard of biomass into the environment.25 Despite current efforts toward the reutilization of industrial residues, large amounts of passion fruit peels remain underutilized. Efforts have been under way to find new uses for passion fruit peel flour.33 In the past decades, much progress has been made, including findings related to nutritional composition, bioactive molecules, and their correspondence with health benefits.33
PASSION FRUIT PEEL: CHEMICAL ASPECTS AND BIOACTIVE COMPOUNDS Studies revealed that PESPF presents low caloric value and is abundant in potassium (K) and also has significant iron (Fe), zinc (Zn), and manganese (Mn) content (Table 1). Such micronutrients are important for the metabolism, and P. edulis Sims peel can be considered as an alternative source for the intake of these minerals.33 Furthermore, PESPF is constituted for 60%–70% of fiber (nearly 20% of soluble fiber and 40%–50% of insoluble fiber) (Table 1).37, 40–42 Among the passion fruit fibers, pectin could be highlighted as a complex carbohydrate from plants with technological and physiological function.10, 37 Soluble fibers are able to form a gel in the surface intestinal absorption, complicating the transport of glucose, lipids, and cholesterol, which delays energy supply, avoiding its excessive consumption.43 Soluble fibers (pectins, hemicelluloses, and gums) or resistant starches are also substratum to fermentation by enteric bacteria, following by the production of short-chain fatty acids such as butyrate, propionate, and acetate.44, 2. FLOURS AND BREADS
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PASSION FRUIT PEEL: CHEMICAL ASPECTS AND BIOACTIVE COMPOUNDS 45
Butyrate represents a primary source of energy to colonocytes, and it may stimulate mucus secretion, vascular flow, barrier permeability, motility, and water and electrolyte absorption.45 Insoluble fiber improves the bowel transit time, whereas soluble fiber is involved in the reduction of both blood cholesterol and intestinal glucose absorption.10, 45 The interest in PESPF has increased due to its being a great source of phytochemical substances that could have therapeutic action as immunomodulators, anticarcinogens, and antioxidants46, 47 because of their high content of alcaloides, flavonoids, and carotenoids.15 Powders of residues by-products of passion fruit showed higher amounts of total phenolic compounds (TPC) compared to the pulp of this fruit—around five times more [103 10.4 and 20 2.6 mg gallic acid equivalent (GAE)].48 Methanolic extract of PESPF (the yellow variety) showed considerable amounts of the flavonoid isoorietin and high antioxidant power, due to its ability to decrease reactive oxygen species (ROS) production by activated neutrophils; furthermore, it was also able to lower myeloperoxidase activity, demonstrating effects on inflammation16 (Table 2). PESPF also showed phytic acid and tannis (Table 1). Albedo from P. edulis shows significant phenolic and flavonoid content in the methanol, water and dimethyl sulfoxide (DMSO) extract. TPC ranges from 0.64–1.86 mg GAE g1, and total flavonoid (TF) content ranges from 0.64 to 5.12 mg rutin equivalent (RE) g1 of sample. Isoorietin and isovitexin were identified in the albedo; the highest amount of such compounds was found in the DMSO extract.51 TABLE 1 Proximate, Phytochemical Composition, and Antioxidant Capacity of P. edulis Sims Peel Proximate
Fresh peel (g/100g)14
Peel flour (g/100 g)36
Peel flour (g/100 g)37
Moisture
84.21
7.42
Energy (kcal/g)
29.91
122.95
Protein (g)
0.67
8.87
3.94
Fat (g)
0.01
3.39
0.31
Carbohydrates (g)
6.78
14.24
79.39
Total dietary fiber (g)
4.33
60.08
65.22
Insoluble dietary fiber (g)
39.96
48.12
Soluble dietary fiber (g)
20.13
17.11
Soluble pectin Ash (g)
Peel flour (mg/g)9
Peel flour38
Peel flour39
9.48
4.85 0.57
6.00
6.88
MINERALS Calcium (mg) Iron (mg) Magnesium (mg)
44.51 0.89 27.82
Phosphorum (mg) Potassium (mg) Sodium (mg)
178.40 43.77
Zinc (mg)
0.32
Copper (mg)
0.04
PHYTOCHEMICALS Isoorietin Phytic acid Tannin
0.653 37.0 308.21
Cyanidin 3-O-glucoside
Qualitative analysis
Quercitin 3-O-glucoside
Qualitative analysis Continued
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252 TABLE 1
20. PASSIFLORA EDULIS PEEL FLOUR AND HEALTH EFFECTS
Proximate, Phytochemical Composition, and Antioxidant Capacity of P. edulis Sims Peel—cont’d Fresh peel (g/100g)
Proximate
Peel flour (g/100 g)
Peel flour (g/100 g)
Peel flour (mg/g)
Peel flour
Edulic acid
Qualitative analysis
Catechin
Qualitative analysis
Epicatechin
Qualitative analysis
Kampferol-3-O-glucoside
Qualitative analysis
Kampferol
Qualitative analysis
Luteolin-8C-neohesperoside
Qualitative analysis
Luteolin-8C-neohesperoside
Qualitative analysis
Protocatechuic acid
Qualitative analysis
Prunasin
Qualitative analysis
Peel flour
Total phenolic compounds (mg GAE g-1)
4.67 0.38
Flavonoids (mg catechin-1)
1.17 0.05
DPPH (%)
29.6 0.66 to 46.35 0.85
FRAP
34.95 2.02 to 38.65 1.55
ORAC
40.83 1.75 to 68.58 0.06
DPPH, assay 2,2-diphenyl-1-picrylhydrazyl; FRAP; Ferric Reducing Antioxidant Power assay (μmol Trolox equivalent (TE) g1 of sample); ORAC, Oxygen Radical Absorbance Capacity (μmol TE g1 of sample).
TABLE 2
Therapeutic Properties of the Most Studied P. edulis Sims
P. edulis Sims
Extract
Bioactive compounds
Experimental model
Main results
References
P. edulis Sims f. flavicarpa
Methanolic extract
Isoorietin
Isolated neutrophils Antioxidant assay
Decrease ROS production and inflammation toward myeloperoxidase and on equine neutrophils
16
P. edulis Sims f. flavicarpa
Hot water extract
Not identified
Rats
Old rats were divided into two groups (control and fed with P. edulis peel flour); after 15 days, the experimental group showed lower antioxidant status in serum (ORAC assay) and lower lipid peroxidation in kidneys and higher in liver compared to the control
39
P.edulis Sims edulis
Methanolic extract
Cyanidin 3-O-glucoside, quercitin 3-O-glucoside and edulic acid
Humans
Human with stage 1 or 2 essential hypertension were treated with P.edulis Sims edulis extract pill (200 mg, twice a day) for 4 weeks showed a decrease in SBP and DBP compared to the control group
7
P. edulis Sims f. flavicarpa
Not evaluated
Not evaluated
Humans
P. edulis Sims f. flavicarpa peel flour intake (30 g/day–2 months) by type 2 diabetes mellitus patients improves insulin resitance
6
P. edulis Sims f. flavicarpa
Not evaluated
Not evaluated
Humans
P. edulis Sims f. flavicarpa peel flour intake (30 g/day–1 and 2 months) by women presenting dyslipedemia decrease total and LDL blood cholesterol concentration
49
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EFFECTS OF PASSION FRUIT PEEL ON GUT HEALTH
TABLE 2
Therapeutic Properties of the Most Studied P. edulis Sims—cont’d
P. edulis Sims
Extract
Bioactive compounds
Experimental model
Main results
References
P.edulis Sims edulis
Methanolic extract
Cyanidin-3O-glucoside, quercitin 3-O-glucoside and edulic acid
Humans
Purple passion fruit peel was able to decrease cardiovascular risk factors in type 2 diabetic subjects. A significant reduction in SBP and fasting and postprandial blood glucose levels was observed in the purple passion fruit– treated group (220 mg/day) after 16 weeks
18
P. edulis Sims f. flavicarpa
Not evaluated
Not evaluated
Rats
Diabetic rats fed on a diet (AIN93 M) supplemented with yellow passion fruit peel flour (5%) decrease the serum glucose level in 59%, reaching smilar values of the control group
41
P. edulis Sims f. flavicarpa
Not evaluated
Not evaluated
Rats
Ingestion ofpassion fruit peel flour by rats with 2,4,6-trinitrobenzenesulfonic acid-induced colitis protected the colon of animals from lipid peroxidation and improve antioxidant status in serum compared to the control
50
P. edulis Sims f. flavicarpa
Not evaluated
Not evaluated
Rats
Rats fed on a high-fat diet with passion fruit peel flour saw decreased adiposity and leptin level; increased CART, GLP1, hypothalamic cocaine expression, and improved insulin sensitivity
4
PESPF (yellow variety) extracted with boiled water showed amounts of TPC of 4.67 0.38 mg GAE g1 of sample and flavonoids of 1.17 0.05 mg catechin g1 of sample. The aqueous, methanolic/acetone, and ethanolic extracts of PESPF differed in the TPC range from 2.06 0.08 to 2.53 0.03, with the greater amount being water extract; for the 2,2-diphenyl-1-picryhydrazyl free radical (DPPH) (%) assay, the range was from 29.6 0.66 to 46.35 0.85; with the greater amount also being water extract; for the Ferric Reducing Antioxidant Power (FRAP) assay, the range was from 34.95 2.02 to 38.65 1.55 μmol Trolox equivalent (TE) g1 of sample, with the greater amount being methanolic/ acetone extract; and for the Oxygen Radical Absorbance Capacity (ORAC) assay, the range was from 40.83 1.75 to 68.58 0.06 μmol TE g1 of sample, with the greater amount being methanolic/acetone extract.39 Another study with the same sample was shown to have water extract flavonoid amounts of 1.17 0.05 mg catechin g1.38 PESPF (purple passion fruit) contains cyanidin 3-O glucoside, quercitin 3-O glucoside, and edulic acid7 as the major components; proto-catechuic acid, (–)-catechin, prunasin + acid glycoside, (+)-epicatechin, , kaempferol-3O-glucoside, luteolin-8-C-neohesperidoside, uteolin-8-C-digitoxoside, and kaempferol.52
EFFECTS OF PASSION FRUIT PEEL ON GUT HEALTH Dietary fiber intake has been shown to modulate gut microbiota by altering bacterial fermentation, colony size, and species composition. Consumption of fermentable dietary fiber provides substrates for microbial activity, but it will also increase the concentrations of fermentation products, such as short-chain fatty acids. Increased levels of shortchain fatty acids, in turn, lower the colonic pH, affecting the microbiota composition.23 Short-chain fatty acids, mainly butyrate, are important substrates for maintaining the colonic epithelium. Butyrate is the preferred fuel used by coloncytes, and the primary site of butyrate sequestration in the body is the gut epithelium. The short-chain fatty acids are related to several other positive health effects, including those related with management of obesity, glucose homeostasis, appetite, and dyslipidemia.36 The passion fruit pericarp (epicarp, the white part; and mesocarp, the yellow part) is rich in dietary fiber, both insoluble and soluble (mainly pectin).50 Although the studies indicate a large amount of dietary fiber in PESPF, its effect on gut health specifically remains little explored. The effect of passion fruit peel on colitis models is already reported.24, 53
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Long-term PESPF intake promoted improvement in antioxidant status, modulated the microbiota, and increased short-chain fatty acids in 2,4,6-trinitrobenzene sulfonic acid (TNBS)-induced colitis in rats.53 Also, PESPF intake exerted an intestinal anti-inflammatory effect and attenuated the colonic damage in the dextran sodium sulfate model of mouse colitis.24 The authors found reduced pro-inflammatory cytokine expression and an enhanced intestinal protective barrier, as shown by biochemical and molecular analyses. Further, they increase short-chain fatty acid formation (acetic acid and butyric acid) in vitro, thus supporting a prebiotic effect.24 The effects of PESPF intake were evaluated in rats as well.54 However, this study revealed elevated butyrate amount in cecal content without alteration in microbiota (Lactobacillus, Bifidobacterium, Enterobacteriaceae, and Total Aerobic Microbial Content). Also, the addition of PESPF in the diet did not change the antioxidant enzyme activity (glutathione reductase, glutathione peroxidase, and superoxide dismutase) and thiol groups (glutathione) in intestine tissue.54 These studies suggest that PESPF may improve gut health by increasing short-chain fatty acid production, especially on inflammatory bowel diseases. Therefore, more studies, especially clinical trials, on the effects of PESPF on the colonic fermentation and its consequences are necessary.
EFFECTS OF PASSIFLORA EDULIS PEEL FLOUR IN METABOLIC PARAMETERS PESPF has demonstrated positive effects in metabolic parameters such as control of glycemia, lipid profiles, and antioxidant status of tissues in animals and humans.37, 38, 40, 49, 55, 56 The ingestion of PESPF (the yellow variety) by diabetic rats decreased serum glucose level by 59% compared to the diabetic rats that did not receive treatment, reaching the normal glycemic amount (112.6 mg/dL) and an increment of 71% in hepatic glycogen was found (Fig. 1). Such results suggest that the PESPF mechanism that decreases blood glucose level is the transformation of blood glucose into liver glycogen.42 Similar results were showed in a clinical study in which the intake of 30 g/day of PESPF (the yellow variety) for 2 months by type 2 diabetes mellitus patients improves blood glucose fasting, homeostatic model assessment (HOMA-IR), and glycated hemoglobin (Fig. 1). Such results showed that supplementation of PESPF decreased insulin resistance in type 2 diabetes mellitus patients, suggesting that it could be used as an adjuvant therapy in conventional treatments.6 The same dose of PESPF (the yellow variety) showed to reduce blood cholesterol concentration in women with dyslipidemia. Reductions of 31.7 28 mg/dL and 47.0 29.5 28 mg/dL in total blood cholesterol concentration were observed after 30 and 60 days of treatment, respectively, and both were statistically significant (Fig. 1).57 Similar results
FIG. 1 The main effects of Passiflora edulis Sims peel flour intake in health parameters.
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Possible action routes of Passiflora edulis Sims peel flour in the metabolic parameters.
were observed when HIV patients were treated with PESPF (the yellow variety) (30 g/day for 30 days) effectively reduced the cholesterol and triacylglyceride levels. Furthermore, the ingestion of 30 g/day of PESPF for 90 days ameliorated lipodystrophy on these patients.19 In another study, the intake of PESPF (the yellow variety) by rats fed on a high-fat diet counteracted cumulative body weight gain and increased hypothalamic cocaine and amphetamine-regulated transcript expression (CART), indicating regulation of satiety. Furthermore, PESPF, in the same study, decreased adiposity and leptin level whereas increased glucose-dependent insulinotropic polypeptide, adiponectin, glucagon-like peptide-1 (GLP-1), and improve insulin sensitivity4 (Fig. 1). In old rats, the ingestion of PESPF (the yellow variety) modulates in different ways the antioxidant tissue status, and in kidneys it decreases lipid peroxidation, in contrast to those found in liver, in which lipid peroxidation was higher than the control group.38 The possible explanation for the effects cited in the studies discussed up to now would be the presence of fiber in passion fruit peel (mainly pectin), which encourages gel formation, leading to changes in gastric-emptying time and intestinal transit, decreasing the velocity of absorption of carbohydrates and fat. In addition, it may inhibit micelle formation. Furthermore, this gel can complex with bile salts increasing cholesterol excretion21, 22 (Fig. 2). In addition, the fibers of the Passiflora peel may be fermented in the colon and, beyond the effects on bowel heath noted in this chapter, it might increase butyrate and propionate, two short-chain fatty acids that have shown antiinflammatory capacity, as they can kβ-activation.58, 59 Activated NF-kβ promotes the expression of TNF-α, inducible nitric oxide synthrase (iNOS), and cyclooxygenase (COX), which induce the action of lymphocytes, monocytes, and endothelial cells, triggering or increasing inflammation.58, 60 As for PESPF (the purple passion variety), positive effects on health parameters have been demonstrated in the scientific literature, such as oral administration of PESPF extract (150 mg/day) for patients with asthma for 4 weeks in a randomized, placebo-controlled, and double-bind study. It was found to improve wheeze, cough, and shortness compared to placebo. Such results are given for the presence of flavonoids in PESPF extract, which can decrease oxidative stress involved in the pathophysiology of asthma. They can inhibit histamine release, arachidonic acid metabolism, and cytokine production.5 In another study, humans with stage 1 or 2 essential hypertension were treated with PESPF extract pill (200 mg, twice a day) for 4 weeks, and they showed decreases in systolic blood pressure (SBP) and diastolic blood pressure (DBP) compared to the control group.7 PESPF (the purple passion variety) was also able to decrease cardiovascular risk factors in type 2 diabetic subjects. Such individuals had fasting blood glucose levels >140 mg/dL and SBP/DBP >140/90 mm Hg. A significant reduction in SBP, fasting blood glucose levels (22.6 + 10.8 mg/dL; P ¼ 0.4), and postprandial blood glucose levels (21.8 + 21.9 mg/dL; P ¼ 0.33) were observed in the PESPF-treated group (220 mg/day) after 16 weeks.18 Epidemiological studies have indicated a significant inverse association between dietary flavonoids and mortality from coronary heart disease.61 Flavonoids (mainly quercetin) have been shown to decrease arterial blood pressure, decrease aortic medial thickening, and attenuate cardiac hypertrophy in various animal models of cardiovascular disease.62, 63 Quercetin,
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luteolin, and cyanidin 3-O-glucoside can downregulate iNOS expression or scavenging of nitric oxide (NO), affecting the endogenous antioxidant system and leading to the modification of vascular tone and peripheral vessel resistance, thus lowering blood pressure (Fig. 2).7, 17 Therefore, including PESPF in the diet could increase the dietary intake of fiber and antioxidants. In addition, it could aid in the prophylaxis and therapeutic of some diseases. Furthermore, the aggregate value in by-products is of economic, scientific, and technological interest and may minimize the generation of industrial processed residuals and environment impact, as well as increasing industrial profitability.4, 8–10, 16, 19, 22, 33, 47, 48
CONCLUSIONS Food waste, or by-products, are a topic of concern in modern society. This represents not only a resource problem, but also environmental and economic ones. Thus, searching for solutions to incorporate by-products into the food industry is a concern as well. Emerging studies support the positive effect of PFF intake on gut health and other metabolic benefits. This fiber-rich by-product could fortify foods, increase their dietary fiber and other bioactive compound content, and create healthy products. However, clinical trials are needed to determine what dose is safe and effective for showing benefits to health.
Acknowledgments MRMJ acknowledges CNPq (301108/2016-1) and FAPESP (2012/12322-0 and 2015/50333-1) for financial support.
References 1. Singh GM, Micha R, Khatibzadeh S, et al. Global, regional, and national consumption of sugar-sweetened beverages, fruit juices, and milk: a systematic assessment of beverage intake in 187 countries. PLoS One 2015;10(8):1–21. https://doi.org/10.1371/journal.pone.0124845. 2. Papargyropoulou E, Lozano R, Steinberger JK, Wright N, Bin Ujang Z. The food waste hierarchy as a framework for the management of food surplus and food waste. J Clean Prod 2014;76:106–15. https://doi.org/10.1016/j.jclepro.2014.04.020. 3. Schieber A, Stintzing F, Carle R. By-products of plant food processing as a source of functional compounds—recent developments. Trends Food Sci Technol 2001;12(2001):401–13. https://doi.org/10.1016/S0924-2244(02)00012-2. 4. Lima GC, Vuolo MM, Batista ÂG, Dragano NRV, Solon C, Maróstica Junior MR. Passiflora edulis peel intake improves insulin sensitivity, increasing incretins and hypothalamic satietogenic neuropeptide in rats on a high-fat diet. Nutrition 2016;32(7-8):863–70. https://doi.org/10.1016/j. nut.2016.01.014. 5. Watson RR, Zibadi S, Rafatpanah H, et al. Oral administration of the purple passion fruit peel extract reduces wheeze and cough and improves shortness of breath in adults with asthma. Nutr Res 2008;28(3):166–71. https://doi.org/10.1016/j.nutres.2008.01.003. 6. de Queiroz M do SR, Janebro DI, da Cunha MAL, et al. Effect of the yellow passion fruit peel flour (Passiflora edulis f. flavicarpa deg.) in insulin sensitivity in type 2 diabetes mellitus patients. Nutr J 2012;11(1):89. https://doi.org/10.1186/1475-2891-11-89. 7. Zibadi S, Farid R, Moriguchi S, et al. Oral administration of purple passion fruit peel extract attenuates blood pressure in female spontaneously hypertensive rats and humans. Nutr Res 2007;27(7):408–16. https://doi.org/10.1016/j.nutres.2007.05.004. 8. de Oliveira AC, Valentim IB, Silva CA, et al. Total phenolic content and free radical scavenging activities of methanolic extract powders of tropical fruit residues. Food Chem 2009;115(2):469–75. https://doi.org/10.1016/j.foodchem.2008.12.045. 9. Zeraik ML, Yariwake JH, Wauters JN, Tits M, Angenot L. Analysis of passion fruit rinds (Passiflora edulis): isoorientin quantification by HPTLC and evaluation of antioxidant (radical scavenging) capacity. Quim Nova 2012;35(3):541–5. https://doi.org/10.1590/S0100-40422012000300019. 10. Yapo BM, Koffi KL. Dietary fiber components in yellow passion fruit rind—a potential fiber source. J Agric Food Chem 2008;56(14):5880–3. https://doi.org/10.1021/jf073247p. 11. Cerqueira-Silva CBM, Jesus ON, Santos ESL, Corr^ea RX, Souza AP. Genetic breeding and diversity of the genus Passiflora: progress and perspectives in molecular and genetic studies. Int J Mol Sci 2014;15(8):14122–52. https://doi.org/10.3390/ijms150814122. 12. López-Vargas JH, Fernández-López J, Perez-Álvarez JA, Viuda-Martos M. Chemical, physico-chemical, technological, antibacterial and antioxidant properties of dietary fiber powder obtained from yellow passion fruit (Passiflora edulis var. flavicarpa) co-products. Food Res Int 2013; 51(2):756–63. https://doi.org/10.1016/j.foodres.2013.01.055. 13. Liew SQ, Chin NL, Yusof YA. Extraction and characterization of pectin from passion fruit peels. Agric Agric Sci Procedia 2014;2:231–6. https:// doi.org/10.1016/j.aaspro.2014.11.033. 14. Córdova KRV, Gama TMMTB, Winter CMG, Kaskantzis Neto G, Freitas RJS. Características físico-químicas da casca do maracujá amarelo obtida por secagem. Bol do Cent Pesqui Process Aliment 2005;23(2):221–30. https://doi.org/10.5380/cep.v23i2.4491. 15. Zeraik ML, Yariwake JH. Quantification of isoorientin and total flavonoids in Passiflora edulis fruit pulp by HPLC-UV/DAD. Microchem J 2010; 96(1):86–91. https://doi.org/10.1016/j.microc.2010.02.003. 16. Zeraik ML, Serteyn D, Deby-Dupont G, et al. Evaluation of the antioxidant activity of passion fruit (Passiflora edulis and Passiflora alata) extracts on stimulated neutrophils and myeloperoxidase activity assays. Food Chem 2011;128(2):259–65. https://doi.org/10.1016/j.foodchem.2011.03.001. 17. Barbalho SM, Damasceno DC, Spada APM, et al. Effects of Passiflora edulis on the metabolic profile of diabetic wistar rat offspring. J Med Food 2011;14(12):1490–5. https://doi.org/10.1089/jmf.2010.0318.
2. FLOURS AND BREADS
REFERENCES
257
18. Raju IN, Reddy KK, Kumari CK, et al. Efficacy of purple passion fruit peel extract in lowering cardiovascular risk factors in type 2 diabetic subjects. J Evid Based Complementary Altern Med 2013;18(3):183–90. https://doi.org/10.1177/2156587213475627. 19. do Socorro Fernandes Marques S, RMF L, AUO S-S, et al. Evaluation of the effects of passion fruit peel flour (Passiflora edulis fo. flavicarpa) on metabolic changes in HIV patients with lipodystrophy syndrome secondary to antiretroviral therapy. Rev Bras Farmacogn 2016;26(4):420–6. https://doi.org/10.1016/j.bjp.2016.03.002. 20. Salgado JM, Dias Bombarde TA, Mansi DN, de Stefano Piedade SM, Molina Meletti LM. Effects of different concentrations of passion fruit peel (Passiflora edulis) on the glicemic control in diabetic mice. Cienc E Tecnol Aliment 2010;30(3):784–9. 21. Rahman S, Zhao A, Xiao D, Park E, Edirisinghe I, Burton-Freeman BM. A randomized, controlled trial evaluating polydextrose as a fiber in a wet and dry matrix on glycemic control. J Food Sci 2017;82(10):2471–8. https://doi.org/10.1111/1750-3841.13855. 22. Jesch ED, Carr TP. Food ingredients that inhibit cholesterol absorption. Prev Nutr Food Sci 2017;22(2):67–80. https://doi.org/10.3746/ pnf.2017.22.2.67. 23. Sawicki CM, Livingston KA, Obin M, Roberts SB, Chung M, Mckeown NM. Dietary fiber and the human gut microbiota: application of evidence mapping methodology (Cvd), 1-21. doi: https://doi.org/10.3390/nu9020125 24. Garrido-mesa J, Guerra-hernández E, Aparecida P, et al. Intestinal anti-inflammatory effects of Passiflora edulis peel in the dextran sodium sulphate. J Funct Foods 2016;26:565–76. https://doi.org/10.1016/j.jff.2016.08.020. 25. Viganó J, Martinez J. Trends for the application of passion fruit industrial by-products: a review on the chemical composition and extraction techniques of phytochemicals. Food Public Health 2015;5(5):164–73. https://doi.org/10.5923/j.fph.20150505.03. 26. Dhawan K, Dhawan S, Sharma A. Passiflora: a review update. J Ethnopharmacol 2004;94(1):1–23. https://doi.org/10.1016/j.jep.2004.02.023. 27. da Silva JK, Cazarin CBB, Colomeu TC, et al. Antioxidant activity of aqueous extract of passion fruit (Passiflora edulis) leaves: in vitro and in vivo study. Food Res Int 2013;53(2):882–90. https://doi.org/10.1016/j.foodres.2012.12.043. 28. Tommonaro G, Segura Rodríguez CS, Santillana M, et al. Chemical composition and biotechnological properties of a polysaccharide from the peels and antioxidative content from the pulp of Passiflora liguralis fruits. J Agric Food Chem 2007;55(18):7427–33. https://doi.org/10.1021/ jf0704615. 29. Benincá JP, Montanher AB, Zucolotto SM, Schenkel EP, Fr€ ode TS. Evaluation of the anti-inflammatory efficacy of Passiflora edulis. Food Chem 2007;104(3):1097–105. https://doi.org/10.1016/j.foodchem.2007.01.020. 30. Abreu PP, Souza MM, Santos EA, Pires MV, Pires MM, De Almeida AAF. Passion flower hybrids and their use in the ornamental plant market: perspectives for sustainable development with emphasis on Brazil. Euphytica 2009;166(3):307–15. https://doi.org/10.1007/s10681008-9835-x. 31. Sunitha M, Devaki K. Antioxidant activity of Passiflora edulis Sims leaves. Indian J Pharm Sci 2009;71(3):310–1. https://doi.org/10.4103/0250474X.56038. 32. IBGE—Produc¸ão Agrícola Municipal. IBGE—Produc¸ão Agrícola Municipal. http://www.cnpmf.embrapa.br/Base_de_Dados/index_pdf/ dados/brasil/maracuja/b1_maracuja.pdf; 2016. Accessed 5 May 2018. 33. Corr^ea RCG, Peralta RM, Haminiuk CWI, Maciel GM, Bracht A, Ferreira ICFR. The past decade findings related with nutritional composition, bioactive molecules and biotechnological applications of Passiflora spp. (passion fruit). Trends Food Sci Technol 2016;58:79–95. https://doi.org/ 10.1016/j.tifs.2016.10.006. 34. Seixas FL, Fukuda DL, Turbiani FRB, et al. Extraction of pectin from passion fruit peel (Passiflora edulis f. flavicarpa) by microwave-induced heating. Food Hydrocoll 2014;38:186–92. https://doi.org/10.1016/j.foodhyd.2013.12.001. 35. Malacrida CR, Jorge N. Yellow passion fruit seed oil (Passiflora edulis f. flavicarpa): physical and chemical characteristics. Brazilian Arch Biol Technol 2012;55(1):127–34. https://doi.org/10.1590/S1516-89132012000100016. 36. Lin HV, Frassetto A, Kowalik EJ, et al. Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS One 2012;7(4):1–9. https://doi.org/10.1371/journal.pone.0035240. 37. Lima GC, Vuolo MM, Batista AG, Dragano NRV, Solon C, Maróstica Junior MR. Passiflora edulis peel intake improves insulin sensitivity, increasing incretins and hypothalamic satietogenic neuropeptide in rats on a high-fat diet. Nutrition 2016;32(7-8):863–70. https://doi.org/10.1016/j. nut.2016.01.014. 38. da Silva JK, Cazarin CBB, Batista ÂG, Maróstica M. Effects of passion fruit (Passiflora edulis) byproduct intake in antioxidant status of Wistar rats tissues. LWT—Food Sci Technol 2014;59(2):1213–9. https://doi.org/10.1016/j.lwt.2014.06.060. 39. Cazarin CBB, da SJK, Colomeu TC, Zollner R de L, Maróstica Junior MR. Capacidade antioxidante e composic¸ão química da casca de maracujá (Passiflora edulis). Ci^encia Rural 2014;44(9):1699–704. https://doi.org/10.1590/0103-8478cr20131437. 40. Cazarin CBB, Da Silva JK, Colomeu TC, Zollner RL, Maróstica Junior MR. Antioxidant capacity and chemical composition of passion fruit peel (Passifl ora edulis j Capacidade antioxidante e composic¸ão química da casca de maracujá) (Passifl ora edulis). Cienc Rural 2014;44(9):1699–704. https://doi.org/10.1590/0103-8478cr20131437. 41. Zeraik ML, Pereira CAM, Zuin VG, Yariwake JH. Maracuj: Um alimento functional? Braz J Pharmacogn 2010;20(3):459–71. https://doi.org/ 10.1590/S0102-695X2010000300026. 42. Salgado JM, Bombarde TAD, Mansi DN, Piedade SMDS, Meletti LMM. Effects of different concentrations of passion fruit peel (Passiflora edulis) on the glicemic control in diabetic rat. Ci^encia e Tecnol Aliment 2010;30(3):784–9. https://doi.org/10.1590/S0101-20612010000300034. 43. Kabir AU, Samad MB, D’Costa NM, Akhter F, Ahmed A, Hannan JMA. Anti-hyperglycemic activity of Centella asiatica is partly mediated by carbohydrase inhibition and glucose-fiber binding. BMC Complement Altern Med 2014;14: https://doi.org/10.1186/1472-6882-14-31. 44. Thibault R, Blachier F, Darcy-Vrillon B, De Coppet P, Bourreille A, Segain JP. Butyrate utilization by the colonic mucosa in inflammatory bowel diseases: a transport deficiency. Inflamm Bowel Dis 2010;16(4):684–95. https://doi.org/10.1002/ibd.21108. 45. Giacco R, Costabile G, Riccardi G. Metabolic effects of dietary carbohydrates: the importance of food digestion. Food Res Int 2015;88:336–41. https://doi.org/10.1016/j.foodres.2015.10.026. 46. Zeraik ML, Yariwake JH, Wauters J-N, Tits M, Angenot L. Analysis of passion fruit rinds (Passiflora edulis): isoorientin quantification by HPTLC and evaluation of antioxidant (radical scavenging) capacity. Quim Nova 2012;35(3):541–5. https://doi.org/10.1590/S0100-40422012000300019. 47. Zeraik ML, Pereira CAM, Zuin VG, Yariwake JH. Maracujá: Um alimento functional? Brazilian J Pharmacogn 2010;20(3):459–71. https://doi.org/ 10.1590/S0102-695X2010000300026.
2. FLOURS AND BREADS
258
20. PASSIFLORA EDULIS PEEL FLOUR AND HEALTH EFFECTS
48. Oliveira DA, Angonese M, Gomes C, Ferreira SRS. Valorization of passion fruit (Passiflora edulis sp.) by-products: Sustainable recovery and biological activities. J Supercrit Fluids 2016;111:55–62. https://doi.org/10.1016/j.supflu.2016.01.010. 49. de Queiroz M do SR, Janebro DI, da Cunha MAL, et al. Effect of the yellow passion fruit peel flour (Passiflora edulis f. flavicarpa deg.) in insulin sensitivity in type 2 diabetes mellitus patients. Nutr J 2012;11(1):89. https://doi.org/10.1186/1475-2891-11-89. 50. Lima GC, Vuolo MM, Batista TG, Dragano NRV, Solon C, Maróstica Junior MR. Passiflora edulis peel intake improves insulin sensitivity, increasing incretins and hypothalamic satietogenic neuropeptide in rats on a high-fat diet. Nutrition 2016;32(7-8). https://doi.org/10.1016/j. nut.2016.01.014. 51. López-Vargas JH, Fernández-López J, Perez-Álvarez JA, Viuda-Martos M. Chemical, physico-chemical, technological, antibacterial and antioxidant properties of dietary fiber powder obtained from yellow passion fruit (Passiflora edulis var. flavicarpa) co-products. Food Res Int 2013; 51(2):756–63. https://doi.org/10.1016/j.foodres.2013.01.055. 52. Chilakapati SR, Serasanambati M, Manikonda PK, Chilakapati DR, Watson RR. Passion fruit peel extract attenuates bleomycin-induced pulmonary fibrosis in mice. Can J Physiol Pharmacol 2014;92(8). https://doi.org/10.1139/cjpp-2014-0006. 53. Cazarin CBB, da Silva JK, Colomeu TC, et al. Passiflora edulis peel intake and ulcerative colitis: approaches for prevention and treatment. Exp Biol Med 2014;239(5):542–51. https://doi.org/10.1177/1535370214525306. 54. da Silva JK, Cazarin CBB, Bogusz Junior S, Augusto F, Maróstica Junior MR. Passion fruit (Passiflora edulis) peel increases colonic production of short-chain fatty acids in Wistar rats. LWT—Food Sci Technol 2014;59(2P2):1252–7. https://doi.org/10.1016/j.lwt.2014.05.030. 55. Batista ÂG, Ferrari AS, Da Cunha DC, et al. Polyphenols, antioxidants, and antimutagenic effects of Copaifera langsdorffii fruit. Food Chem 2016;197:1153–9. https://doi.org/10.1016/j.foodchem.2015.11.093. 56. Clifford MN, Scalbert A. Review ellagitannins—nature , occurrence and dietary burden. J Sci Food Agric 2000;80(November 1999):1118–25. https://doi.org/10.1002/(SICI)1097-0010(20000515). 57. Ramos AT, Cunha MAL, Sabaa-Srur AUO, et al. Uso de Passiflora edulis f. flavicarpa na reduc¸ão do colesterol. Brazilian J Pharmacogn 2007; 17(4):592–7. https://doi.org/10.1590/S0102-695X2007000400019. 58. Miles-Brown JP, Chassaing B, Gewirtz AT. Microbiota metabolism of soluble fiber protects against low-grade inflammation and metabolic syndrome. Gastroenterology 2015;148(4):S541. https://rsm.idm.oclc.org/login?url¼https://www.rsm.ac.uk.htm?url¼https://dialog.proquest.com/ professional/professional/docview/1682704799?accountid¼138535%0Ahttp://vw4tb4ff7s.search.serialssolutions.com?ctx_ver¼Z39.88-2004& ctx_enc¼info:ofi/enc:UTF-8&rfr_id. 59. Cani PD, Osto M, Geurts L, Everard A. Involvement of gut microbiota in the development of low-grade inflammation and type 2 diabetes associated with obesity. Gut Microbes 2012;3(4). https://doi.org/10.4161/gmic.19625. 60. Panasevich MR, Allen JM, Wallig MA, Woods JA, Dilger RN. Moderately fermentable potato fiber attenuates signs and inflammation associated with experimental colitis in mice. J Nutr 2015;145(12):2781–8. https://doi.org/10.3945/jn.115.218578. 61. Feliciano RP, Pritzel S, Heiss C, Rodriguez-Mateos A. Flavonoid intake and cardiovascular disease risk. Curr Opin Food Sci 2015;2:92–9. https:// doi.org/10.1016/j.cofs.2015.02.006. 62. Duarte J, Perez-Palencia R, Vargas F, et al. Antihypertensive effects of the flavonoid quercetin in spontaneously hypertensive rats. Br J Pharmacol 2001;133(1):117–24. https://doi.org/10.1038/sj.bjp.0704064. 63. Mu MM, Chakravortty D, Sugiyama T, et al. The inhibitory action of quercetin on lipopolysaccharide-induced nitric oxide production in RAW 264.7 macrophage cells. J Endotoxin Res 2001;7:431–8. https://doi.org/10.1179/096805101101533034.
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