Opuntia ficus-indica (cactus pear) produces edible tender stems and fruits with a high nutritional value in terms of minerals, protein, dietary fiber and phytochemicals. Around 20% of fresh weight of cladodes and 45% of fruits are by-products.
Opuntia ficus-indica (cactus pear) produces edible tender stems and fruits with a high nutritional value in terms of minerals, protein, dietary fiber and phytochemicals. Around 20% of fresh weight of cladodes and 45% of fruits are by-products.
Opuntia ficus-indica (cactus pear) produces edible tender stems and fruits with a high nutritional value in terms of minerals, protein, dietary fiber and phytochemicals. Around 20% of fresh weight of cladodes and 45% of fruits are by-products.
of Antioxidant Dietary Fiber Sara Bensadn & Deisy Hervert-Hernndez & Sonia G. Syago-Ayerdi & Isabel Goi Published online: 10 July 2010 # Springer Science+Business Media, LLC 2010 Abstract Dietary fiber and bioactive compounds are widely used as functional ingredients in processed foods. The market in this field is competitive and the development of new types of quality ingredients for the food industry is on the rise. Opuntia ficus-indica (cactus pear) produces edible tender stems (cladodes) and fruits with a high nutritional value in terms of minerals, protein, dietary fiber and phytochemicals; however, around 20% of fresh weight of cladodes and 45% of fresh weight of fruits are by- products. The objective of this study was therefore to determine the nutritional value of by-products obtained from cladodes and fruits from two varieties of Opuntia ficus-indica, examining their dietary fiber and natural antioxidant compound contents in order to obtain quality ingredients for functional foods and increase the added value of these by-products. Keywords Antioxidant dietary fiber . By-products . Functional ingredients . Opuntia spp. Abbreviations ABTS 2,2-azinobis-(3-ethyl-benzothiazoline-6-sulfonic acid) AC Antioxidant capacity DF Dietary fiber EP Extractable polyphenols FRAP Ferric reducing ability assay IDF Insoluble dietary fiber NEP Non extractable polyphenols SDF Soluble dietary fiber TDF Total dietary fiber Introduction Opuntia ficus-indica (cactus pear) is a cactus well adapted to extreme climate and edaphic conditions. The semiarid regions of the central part of Mexico host the greatest diversity of this cactus in the world [1]. In Mexico, the cultivated area for human consumption is around 10,000 Ha. Under optimal conditions annual production can reach 50 tons of dry matter per hectare. The genus Opuntia embraces about 1,500 species of cactus and many of them produce edible tender stems and fruits [2]. The tender young part of the cactus stem, or cladode, is frequently consumed as a vegetable in salads, while the cactus pear fruit is consumed as a fresh fruit. This cactus is a common item of consumption in Mexico (1017 g/person/day) [3]. Chemical composition depends on variety, maturation stage and environmental conditions [46]. Previous studies on the chemical composition of the edible portion of cladodes and fruits from Opuntia ficus-indica show that these foods have a high nutritional value, mainly due to their mineral, protein, dietary fiber and phytochemical contents [4, 5, 7, 8]. Interestingly, antioxidant activity has also been reported [9, 10]. Besides being a traditional source of vegetables, cladodes also have medical and animal breeding applica- tions [7, 11]. S. Bensadn : D. Hervert-Hernndez : S. G. Syago-Ayerdi : I. Goi Nutrition and Gastrointestinal Health Unit UCM/CSIC, Department of Nutrition I, Faculty of Pharmacy, University Complutense of Madrid, Madrid, Spain I. Goi (*) Departamento de Nutricin y Bromatologa I (Nutricin), Facultad de Farmacia, Universidad Complutense de Madrid, Ciudad Universitaria s/n, 28040 Madrid, Spain e-mail: igonic@farm.ucm.es Plant Foods Hum Nutr (2010) 65:210216 DOI 10.1007/s11130-010-0176-2 From a health standpoint they are interesting as a source of nutrients in the normal diet. Moreover, we should also bear in mind that industrial food processing (preparation, packaging, etc.) generates a large amount of agricultural by- products that could potentially be used as sources of food ingredients in the functional food industry. In fact, in recent years there has been a global trend toward the use of natural plant food components, such as dietary fiber and phyto- chemicals, as ingredients in functional foods. Opuntia ficus- indica is rich in dietary fiber and phytochemicals [7, 11]. The by-products are the outer coating of these plants, which is removed before food preparation and contains spines and a large quantity of glochids and pulp. Around 20% and 45% of the fresh weight of cladodes and fruits respectively are by-products [12]. By-products are expected to be natural materials rich in dietary fiber, minerals and antioxidant bioactive compounds. Dietary fiber and bioactive compounds are widely used as functional ingredients in processed foods. The market in this field is competitive and the development of new types of quality ingredients is a challenge for the food industry. There is therefore an interest in considering not only the nutritional quality of the ingredient, but also its distribution, cost and other additional benefits, since the use of these materials as ingredients would make them added-value products. The aim of this study was to evaluate the nutritional value of by-products obtained from cladodes and fruits of two varieties of Opuntia ficus-indica by examining their contents in dietary fiber and natural antioxidants com- pounds with a view to obtaining quality ingredients for functional foods and increasing the added value of these by-products. Materials and Methods Plant Materials and Sample Preparation Young stems (cladodes) of two varieties of Opuntia ficus- indica, Milpa Alta and Atlixco, and fruits of two varieties of cactus pear, Alfajayucan (green tuna) and Pelon Rojo (red tuna), were supplied by a Mexican association (CoMenTuna, Actopan, Hidalgo, Mexico). Plant materials were harvested at the usual range of maturation for optimal human consumption from a growing area in Mexico (Hidalgo State) and were manually collected during the spring of 2008. Most of the spines were removed mechanically on-site before being sent to Spain by refrigeration transport for analysis in June 2008. The cactus pear samples were peeled in the normal way for human consumption. Spines, epidermis and glochids were manually removed from the cladodes and cactus pear fruits. The edible portion was then discarded so that the by- product samples for analysis comprised the spines, epider- mis and glochids that had been removed. The amount of by-products obtained from cladodes and cactus pear fruits was estimated at around 17% and 53% (fresh weight) respectively for a 5 kg batch. By-product samples were cut into small pieces, freeze-dried, ground to fine powder (100- mesh sieve) and stored in the dark at 20 C until analysis. Chemical Analysis Proximate Analysis Samples were analyzed using AOAC methods [13]: protein (Method 950.48), fat (Method 983.23), ash (Method 940.26) and moisture (Method 925.09). Dietary Fiber Determination as Indigestible Fraction The procedure to determine the indigestible fraction was described by Saura-Calixto et al. [14]. Samples were incubated with digestive enzymes to simulate digestion in the small intestine. Briefly, 300 mg of sample was incubated with pepsin (0.2 ml of a 300 mg/ml solution in HCl-KCl 0.2 M buffer, pH 1.5, 40 C, 1 h, Merck 7190), pancreatin (1 ml of a 5 mg/ml solution in phosphate buffer 0.1 M; pH 7.5, 37 C, 6 h, Sigma P-1750), lipase (2 ml of a 7 mg/ml solution in phosphate buffer 0.1 M; pH 7.5, 37 C, 6 h, Sigma L-3126), bile extract porcine (2 ml of a 17.5 mg/ml solution in phosphate buffer 0.1 M; pH 7.5, 37 C, 6 h, Sigma B-8631) and -amylase (1 ml of a 120 mg/ml solution in tris-maleate buffer 0.1 M; pH 6.9, 37 C, 16 h, Sigma A-3176). Then samples were centrifuged (15 min, 3,000 g) and supernatants removed. Residues were washed twice with distilled water (5 ml) and all supernatants combined. Residues were dried overnight at 105 C and quantified gravimetrically as the insoluble indigestible fraction. Each supernatant was incubated with 100 l of amyloglucosidase (Roche, 102 857) for 45 min at 60 C and they were transferred into dialysis tubes (1200014000 MWCO; Dialysis Tubing Visking, Medicell International Ltd., London, UK), and dialyzed against water for 48 h at 25 C (water flow 7 l/h) to eliminate digested components. Non-starch polysaccharides were measured by dinitrosalicilic method [15] in insoluble residue (insoluble DF) and in the dialysis retentante (soluble DF). Total indigestible fraction was the sum of soluble and insoluble indigestible fractions. Carotenoids Determination Carotenoids were extracted according to Quakenbush [16] with some modifications. Briefly, freeze-dried samples (30 mg) were incubated (30 min, 50 C) in dimethyl sulphoxide (2.5 ml) with sodium sulphate, sodium carbonate and 2,6-Di-ter-Butil-4- Metilfenol (BHT) (Panreac Qumica S.A., Barcelona, Plant Foods Hum Nutr (2010) 65:210216 211 Spain). After incubation, methanol (5 ml) was added and vortexed. Samples were centrifuged (4,200 g, 3 min) and supernatants collected. Methanol washes were employed until colorless (absorbance 0.001); all supernatants were combined. The carotenoids extract was saponificated according to Granado et al. [17] with some modifications. Briefly, carotenoids methanolic extract (2 ml), diethyl ether stabilized with 6 mg/l of BHT (4 ml) (Panreac Qumica, Barcelona, Spain) and saturated KOH in water (0.5 ml) was saponified for 30 min in darkness. After saponification, distilled water (5 ml) was added, vortexed for 15 s and centrifuged (4,200 g, 3 min). Ether layer was collected and ether washes were done until colorless (absorbance 0.01). Absorbance values at 450 nm were used to determine carotenoids content using a UV-1800 UV-VIS spectropho- tometer (Shimadzu Europe GmbH, Germany). Extraction and Quantification of Phenolics Compounds Samples were extracted by shaking at room temperature with methanol-water (50:50 v/v, 50 ml/g sample, 60 min, constant shaking) and acetone-water (70:30 v/v, 50 ml/g sample, 60 min, constant shaking). After centrifugation (15 min, 25 C, 3,000 g) supernatants were combined and used to determine extractable polyphenols content and antioxidant activity. Extractable polyphenols (EP) were determined by the Folin-Ciocalteau procedure [18], using gallic acid as standard. Non extractable polyphenols (NEP), in the form of proanthocyanidins and hydrolyzable tannins, were measured in the extraction residues, using a UV-1800 UV-VIS spectrophotometer (Shimadzu Europe GmbH, Germany). The residue was treated with 5 ml/l HCl-Butanol (3 h, 100 C) [19] for proanthocyanidins hydrolysis. Proanthocyanidins were calculated from the absorbance at 550 nm using as standard Mediterranean carob pod (Ceratonia siliqua L.) supplied by Nestl S.A. The residue of the methanol/acetone/water extraction was treated with methanol/H 2 SO 4 90:10 (v/v) hydrolysis (85 C, 20 h) [20] to determine hydrolyzable tannins. Samples were centrifuged (15 min, 25 C, 3,000 g) and the hydrolyzable polyphenols were determined in supernatants by Folin-Ciocalteau reagent using gallic acid as standard. Antioxidant Capacity Determination FRAP Assay The method followed was described by Benzie & Strain [21]. Briefly, FRAP reagent, containing 2,4,6-tri(2-pyridyl)-s- triazine(TPTZ) (Fluka Chemicals, Madrid, Spain), FeCl 3 , and acetate buffer, was mixed with 90 l of distilled water and 30 l of the sample or the blank. Absorbance values at 595 nm were taken every 15 s at 37 C, using a UV-1800 UV-VIS spectrophotometer (Shimadzu Europe GmbH, Germany). The readings at 30 min were selected for calculations of FRAP values. A standard curve of Trolox was used to estimate antioxidant capacity of samples and it was expressed as Trolox (6-hydroxy-2,5,7,8-tetramethylchro- man-2-carboxylic acid, a water-soluble analogue of vitamin E) equivalents. Free Radical Scavenging ABTS Assay The antioxidant capacity was estimated in terms of radical scavenging activity following the procedure described elsewhere [22] with some modifications. Briefly, ABTS [2,2-azinobis-(3- ethyl-benzothiazoline-6-sulfonic acid)] radical cation (ABTS+) was produced by reacting 7 mmol/l ABTS stock solution with 2.45 mmol/l potassium persulfate in the dark at room temperature for 1216 h before use. The ABTS+ solution was diluted with methanol to an absorbance of 0.700.02 at 730 nm. After addition of 0.1 ml of sample to 3.9 ml of diluted ABTS+ solution, absorbance readings were taken every 20 s using a UV-1800 UV-VIS spectro- photometer (Shimadzu Europe GmbH, Duisburg, Ger- many). The reaction was monitored for 6 min. The percentage of inhibition of absorbance vs. time was plotted, and the area under the curve (06 min) was calculated. Solutions of known trolox concentration were used as antioxidant capacity equivalents. Statistical Analysis Results were expressed as mean standard deviation of three or more separate determinations. Comparison of means was performed by t-test or one-way ANOVA followed by Tukey HSD test to identify significant differ- ences (P<0.05) among samples. Data were analyzed using SPSS V.13.0 software (SPSS Institute Inc., Cary, NC). Results and Discussion The edible portion of cladodes (nopal) and fruits (tuna) of Opuntia-ficus has considerable nutritional value. For comparative purposes the proximate composition reported in the literature is indicated in Table 1. These foods are rich in digestible carbohydrates, dietary fiber and minerals and are relatively low in protein and fat. However, levels of digestible carbohydrates and dietary fiber (DF) are high. Potassium and calcium are the most abundant minerals in these foods [4, 7, 8]. Digestible carbohydrate content is higher in fruit, constituting more than 50% of the pulp [23]. Glucose and fructose are the predominant sugars, although starch is also present in low concen- trations. Both tender stems and fruits have high DF contents. These values are similar when the two are compared on a fresh weight basis, but are significantly higher in the tender stems when the values are expressed on a dry matter basis (Table 1). 212 Plant Foods Hum Nutr (2010) 65:210216 The by-products are epidermis, glochids, and a portion of the edible part that cover both tender stems and fruits. According to the literature, the spines account for about 8% of the whole cladodes on a dry weight basis [24] and contain around 96% of the polysaccharides, with equal amounts of cellulose and arabinans, which are generally associated with pectin substances [25]; whereas the largest part of DF in pulp fruit is pectin, followed by hemicellulose and cellulose [23]. The composition of by-products from cladodes and fruits (dry weight) in this work was similar to that of the edible parts of cladodes and fruits as reported in the literature. By-products had low protein and fat contents, consistent with their edible portion. An important differ- ence was observed in total DF contents, which were quite high in the by-products. The majority component of the four samples studied was DF. These results are summa- rized in Table 2. DF is not a defined chemical group but a combination of chemically heterogeneous substances. Nowadays, there is scientific evidence that the primary characteristics of DF assigned to non starch polysaccharides and lignin (resis- tance to digestion and absorption in the small intestine and fermentation in the large intestine) can be extended to other indigestible food constituents. As a whole, it has been defined as food indigestible fraction [14]. On this basis, DF may also include associated compounds, such as polyphe- nols and carotenoids, both phytochemicals present in our samples. The values shown in Table 2 correspond to the indigestible fraction of the samples and include non-starch polysaccharides, Klason lignin and associated compounds. Total indigestible fraction content (Table 2) in the by- products was higher than in common diet foods, such as bean (44% dm), lentil (29% dm), apple (17% dm) and orange (26% dm) [14] and was similar to plant materials, such as grape pomace, guava fruit peel or Fucus vesiculo- sus [26], which are considered very DF-rich materials. The TDF content was significantly higher in cladodes than fruits. However, there were no significant differences between varieties (Atlixco and Milpa Alta) as regards soluble and insoluble DF in the case of cladodes, whereas in the case of cactus pear fruits insoluble DF was significant higher (80%) in Alfajayucan than in Pelon Rojo. Fiber is an essential component in a healthy diet and is needed to maintain optimal health. However, dietary fiber intake is often deficient in any population [27]. For that reason fiber is a widely-used ingredient in the functional foods industry. The soluble/insoluble DF ratio is an important nutritional parameter, like TDF content, because of the different physiological effects [28]. Soluble dietary fiber (SDF) is usually constituted by compounds with high water holding capacity, which are substrates for intestinal microbiota, contributing to health status. Both cladodes and fruits contain high concentrations of SDF. About 15% of the fiber in the two varieties of cladodes was soluble whereas Table 1 Composition of cladodes and fruits of Opuntia ficus-indica (g/100 g edible fresh weight) Cladode (Nopal) Cactus pear fruit (Tuna) [7] [23] Moisture 91.04 80.45 Protein 0.80 1.00 Fat 0.42 0.19 Digestible carbohydrates Starch 1.17 0.89 Sugars 0.54 11.40 Total dietary fiber 3.75 4.01 Ash 2.09 1.66 Values obtained from references 7 and 23 Table 2 Composition of cladodes and fruits dry by-products of Opuntia ficus-indica varieties (g/100 g dry matter) Cladodes Fruits Atlixco Milpa Alta Green tuna Red tuna Moisture 5.650.36 A 5.810.36 A 5.410.17 A 7.520.24 A Protein 1.130.47 A 1.140.31 A Traces Traces Fat 1.220.16 A,B 1.420.01 A 1.140.03 B 0.940.001 B Ash 16.540.15 A 16.290.56 A 17.070.19 B 13.140.31 A Dietary fiber (as indigestible fraction) a Soluble 9.80.55 A 8.920.27 A,B 7.980.47 B 8.120.05 B Insoluble 54.451.23 A 53.133.72 A 34.950.74 B 19.391.57 C Values are mean SD (n3). Values in a row not sharing the same upper case letter are significantly different (P<0.05), determined by one-way ANOVA followed by Tukey HSD test except for protein (t-test) a Includes non-starch polysaccharides, Klason lignin and associated compounds [10] Plant Foods Hum Nutr (2010) 65:210216 213 samples of green and red fruit varieties contained 18 and 29% of SDF, respectively (Table 2). DF from plant foods may transport a significant amount of bioactive compounds, such as polyphenols and carote- noids, linked to the fiber matrix through the human gut [29, 30]. Polyphenols bound to DF can account for a substantial part of total polyphenols in foods and beverages, which is another quality feature. On average, 2.5% of insoluble dietary fiber (IDF) in common fruit and vegetables consists of polyphenols [30]. The concentrations of phenolic compounds and carotenoids found in the four samples studied were very high (Table 3). As regards EP content, there were no significant variety-dependent (Atlixco or Milpa Alta) differences between tender stems. On the other hand, the EP content in Alfajayucan cactus pear was significantly higher (around 80%) than in Pelon Rojo. NEP and EP were determined, but neither proanthocyani- dins nor hydrolyzable tannins were detected in the samples (Table 3). However, the EP content was relatively higher when compared with values in common dietary foods [30]. EPs are compounds with a low degree of polymerization that can be extracted using aqueous-organic solvents with properties such as antioxidant capacity (AC). Total carotenoid contents of the by-product samples (Table 3) were quite high but consistent with reports for the edible portion of wild cladodes with a water content of 74.2% (5.696.55 mg/g dry weight for carotenoids and 5.696.72 mg/g dry weight for xanthophylls) [6], or similar to carotenoid contents reported for the edible part of cactus pear fruits (4.66 mg/g dry weight, considering a water content of 87.55%) [5]. In the case of both cactus pear fruits and young stems, there were no significant variety- dependent differences in carotenoid content. Carotenoid content in nopal is distributed as -carotene (36%), lutein (46%) and -cryptoxanthin (18%) [6]. Like polyphenols, some of the carotenoids contained in plant foods could be bound to the DF matrix. For instance, between 20 and 70% of the -carotene and lutein in green leafy vegetables have been found to be associated with the DF matrix [31]. The key step in the carotenoid absorption process is release from the food matrix. A significant inverse correlation has been found between small intestine bioavailability of carotenoids (lutein and carotene) and DF content in green leafy vegetables [31]. Our samples are DF concen- trates with a high proportion of IDF, and therefore, the bioavailability of carotenoids and polyphenols from these samples is a crucial point in the assessment of their physiological role. Among the noteworthy properties of polyphenols and carotenoids are their antioxidant and free radical scaveng- ing capacities. The AC values of cladodes and fruits of Opuntia ficus-indica by-products (Table 3) were similar to other foods such as nuts and fruits [32]. When AC was measured by FRAP assay, significant variety-dependent differences were observed in both cladodes and pear cactus fruits. However, the varietydependent difference in AC determined in terms of free radical scavenging capacity was significant only in the case of young stems. The AC of a food is derived from the cumulative, synergistic antioxidant power of vitamins, polyphenols, carotenoids and other Table 3 Phenolic compounds (extractable, non-extractable), carotenoids contents and antioxidant activity of cladodes and fruits by-products of Opuntia ficus-indica varieties Cladodes Fruits Atlixco Milpa Alta Green tuna Red tuna Phenolic compounds: Extractable a 2.690.85 A 3.711.18 B 2.760.20 C 1.540.19 D Non-extractable: Proanthocyanidins ND b ND ND ND Hydrolyzable tannins ND ND ND ND Carotenoids c 21.320.36 A 22.840.06 A 16.010.11 B 15.160.12 B Total antioxidant capacity d FRAP method 52.221.07 A 65.332.23 B 40.391.62 C 47.352.10 A ABTS method 52.372.00 A 57.551.83 B 66.332.61 C 65.762.02 C Values are mean SD (n3). Values in a row not sharing the same upper case letter are significantly different (P<0.05), determined by one-way ANOVA followed by Tukey HSD test a Measured as gallic acid equivalents and expressed as g/100 g of dry matter b ND: not detected c Measured as -carotene equivalents and expressed as mg/g of dry matter d Expressed as mol trolox equivalents/g of dry matter 214 Plant Foods Hum Nutr (2010) 65:210216 minor constituents [33]. In our case, the AC was deter- mined in the total extract from the samples, and so the individual contributions of polyphenols, carotenoids and other antioxidant compounds such as ascorbic acid to total AC could not be differentiated. In this connection Butera et al. [34] found that ascorbic acid accounted only for 3040% of the total AC in cactus pear fruits. There have been reports on the AC of the edible part of cactus pear fruits [5, 6, 10, 34], but the results are not consistent, possibly due to differences in methodology, maturation stage and Opuntia variety. DF and antioxidants as functional ingredients are generally addressed separately in both technological and nutritional studies. However, the fact that a substantial proportion of dietary antioxidant polyphenols are linked to DF is important because the postulated benefits of fiber intake may be attributable to associated bioactive compounds. By-products from cladodes and fruits of Opuntia ficus-indica could combine the physiological effects of both DF and antioxidants in a single material meeting the criteria for consideration as an antioxidant dietary fiber [35]. The combination of high DF and associated phytochemicals in a single matrix results in samples with specific properties suitable for use as dietary supplements and food ingredients. 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