Article pubs.acs.org/JAFC
Release of Antioxidant Capacity from Five Plant Foods during a Multistep Enzymatic Digestion Protocol Valentina Azzurra Papillo,† Paola Vitaglione,† Giulia Graziani,† Vural Gokmen,‡ and Vincenzo Fogliano*,§ †
Department of Agriculture and Food Science, University of Naples “Federico II”, Naples, Italy Food Engineering Department, Hacettepe University, 06800 Beytepe, Ankara, Turkey § Food Quality and Design Group, Wageningen University and Research Centre, P.O. Box 8129, 6700 EV Wageningen, The Netherlands ‡
ABSTRACT: This study aimed at elucidating the influence of food matrix on the release of antioxidant activity from five plant foods (apple, spinach, walnut, red bean, and whole wheat). To this purpose a protocol based on sequential enzymatic digestion was adopted. The total antioxidant capacity (TAC) of both solubilized and insoluble materials was measured at each step. Results showed that the overall TAC obtained by enzyme treatments was usually higher than that obtained by chemical extraction-based methods. In apple most of the TAC was released upon water washing and after pepsin treatment, whereas in spinach, beans, and whole wheat the TAC released by treatments with bacterial enzymes was prominent. Walnut had the highest TAC value, which was mainly released after pancreatin treatment. Therefore, the enzyme treatment is fundamental to estimate the overall potential TAC of foods having a high amount of polyphenols bound to dietary fiber or entrapped in the food matrix. KEYWORDS: in vitro digestion, foods, antioxidant capacity, phytochemicals, bioaccessibility
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acids in cereal/nut/legume dietary fiber) or physically aggregated with chloroplast proteins (as occurs to carotenoids in tomatoes or spinach).11−15 In nuts, fruits, and vegetables, phytochemicals are present mainly in free form that can be extracted in water or hydroalcoholic solutions. Contrarily, in whole cereals and legumes, bound antioxidants are the most dominant form that can be extracted only after chemical hydrolysis. Apples’ main antioxidant molecules are soluble polyphenols such as chlorogenic acid, catechin, epicatechin, and phloridzin.16 Spinach composition is similar to that of apple with many free phenolic compounds; however, they have a more consistent fiber structure that could limit the phytochemicals’ extractability.17 Walnut antioxidant capacity was principally attributed to ellagic and gallic acids that are present as polymers and bound to sugars, forming hydrolyzable tannins; their solubility depends on their degree of polymerization.18 Polyphenol compounds are the major phytochemicals in red beans, 19,20 and many of them are bound to polysaccharides and proteins of cell wall with ester and ether links.21,22 Whole wheat antioxidant capacity is due to phenolic acids, principally to ferulic acid and flavonoids: 90% of them are covalently bound to cell wall polysaccharides that are insoluble in organic solvents.23,24 After ingestion, the digestion processes modified foods’ physical structure regulating the bioaccessibility (i.e., the possibility to be released in the lumen and eventually absorbed) as well as the antioxidant capacity (i.e., availability to react with oxidant species) of bound phytochemicals in the GI environment. We have previously demonstrated that an in vitro
INTRODUCTION Epidemiological studies have associated the consumption of fruits, vegetables, whole grains, and legumes to a reduced risk of chronic diseases such cardiovascular diseases, diabetes, and some type of cancers, especially colorectal cancer.1−4 The amount and the type of dietary fiber and phytochemicals were recognized as major determinants responsible for the health benefits of these foods. Many phytochemicals are chemically reactive compounds that can counteract the action of reactive oxygen species, thus preventing the oxidation of biological substrates such as lipids, DNA, and proteins. During the past 20 years researchers’ attention was focused on phytochemicals antioxidant properties and vast knowledge was built over time on specific food molecules, body metabolites, and cellular mechanisms acting in biological systems following their ingestion.5,6 It was well established that even for phytochemicals showing a high antioxidant capacity in vitro this property alone cannot explain the systemic health benefits. The extended biotransformation of many dietary phytochemicals once ingested and their low bioavailability led to tissue concentrations that are much below those showing antioxidant ability in vitro. Mounting evidence indicated that other biological properties including modulation of inflammation, detoxification, and immune response can play a major role in body defense at a systemic level.7−10 On the other hand, inside the gastrointestinal (GI) tract (stomach, small intestine, and lower gut) the antioxidant activity of dietary phytochemicals may have a central role: their concentration is mainly dependent on the amount in the ingested food, and their chemical form is usually the same present in the food. Phytochemicals can be found in food in either free or bound form. In the latter case they can be covalently linked to polysaccharides (as occurs to phenolic © 2014 American Chemical Society
Received: Revised: Accepted: Published: 4119
November 11, 2013 April 8, 2014 April 10, 2014 April 10, 2014 dx.doi.org/10.1021/jf500695a | J. Agric. Food Chem. 2014, 62, 4119−4126
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sequential enzyme digestion of the water-insoluble fraction of cocoa resulted in the release of antioxidant capacity (due to material solubilized by digestion) and in a contemporary increase of the antioxidant capacity of the remaining insoluble material.25 Moreover, it has been recently reported that the antioxidant capacity of the insoluble wheat bran can be restored by treatment with an antioxidant-rich soluble beverage.26 In vitro digestion protocols have been widely used to study the digestibility, bioaccessibility, and structural changes of food macronutrients, particularly proteins and starch.27 Recently, also the effects of digestive process on the food antioxidant activity and on some phytochemicals were studied. Saura-Calixto et al.28 studied the bioaccessibility of polyphenols from different foods after enzymatic hydrolysis and after colonic fermentation: results indicated that about 48% of polyphenols are bioaccessible in the small intestine, whereas 42% become bioaccessible in the large intestine. More recently, Pastoriza et al.29 developed the global antioxidant response (GAR) measuring the total antioxidant capacity (TAC) of the soluble and insoluble fraction throughout an in vitro digestion. They found that after digestion TAC was higher than that obtained with the usual chemical extraction and the QUENCHER method. Finally, Gong et al.30 studied the TAC of cereals after in vitro digestion. Also, these authors confirmed that TAC measured after enzymatic digestion is much higher than that observed on undigested foods. This study aimed at (i) elucidating the influence of food matrix and phytochemical disposition on the potential food antioxidant activity, (ii) providing a complete picture of the contribution of different plant foods to keep a redox balance inside the GI environment, and (iii) giving useful data to design foods providing a controlled release of phytochemicals. To this purpose five plant foods (apple, spinach, walnut, red bean, and whole wheat) having different physical structures, as well as different macronutrient and phytochemical compositions and forms, were selected; a sequential multistep enzyme treatmentbased protocol was developed; and the release of antioxidant activity as well as the antioxidant capacity of insoluble food material was measured at each step.11
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Table 1. Macronutrient Composition of the Studied Foods Expressed in Percentage by Dry Weight
apple spinach bean whole wheat walnut
protein
fat
carbohydrate
dietary fiber
insoluble vs total DF (%)
2 37 23 12
1 0 2 2
80 39 56 73
17 24 19 13
65 77 77 84
15
73
5
7
87
Chemical Extractions. Hydroalcoholic Extraction. One gram of dry food was extracted with 10 mL of methanol/water (70:30 v/v) for 30 min in an ultrasonic bath. The solution was centrifuged at 2800g for 5 min at 4 °C, and the antioxidant activity of the supernatant was measured with the DPPH assay as described below.28 The TAC of hydroalcoholic extract (HAE_TAC) was expressed as millimoles of Trolox equivalent (TE) per kilogram of dry matter. Alkaline Hydrolysis. Alkaline hydrolysis was performed on the pellets obtained after hydroalcoholic extraction that were added with 20 mL of 4 M NaOH for 2 h under agitation.12 At the end of the reaction, the pH was brought between 2 and 3 with 6 M HCl, and the sample was centrifuged at 2800g for 15 min at 4 °C. The supernatant was extracted three times with 50 mL of ethyl acetate, and the combined extracts were evaporated to dryness and subsequently dissolved in methanol/water (70:30 v/v). Ten milliliters of methanol/ water (70:30 v/v) was added to the pellet, and the mixture was kept in agitation for 30 min; mixture centrifugation and supernatant collections followed. The antioxidant activity of individual extracts was measured by the DPPH assay as above-described and finally summed to obtain the total antioxidant activity of the chemical extraction (TPE_TAC). In Vitro Digestion Procedure. Each food was digested using a protocol including water washing and a sequential multistep enzymatic treatment.29 Samples were incubated with the enzymes in agitation to 120 oscillations/min at 37 °C using a shaking thermostatic bath. The digestion scheme is summarized in Figure 1: at the end of each digestion step the soluble and insoluble materials were separated by centrifugation (2800g for 3 min, 4 °C). The soluble part was used for the TAC measurement, whereas the insoluble part was further digested in the following step. The final insoluble material obtained
MATERIALS AND METHODS
Chemicals and Reagents. 6-Hydroxy-2,5,7,8-tetramethylchroman-2-carboxylic acid (Trolox), 2,2-diphenyl-1-picrylhydrazyl (95%), sodium bicarbonate, and sodium hydroxide were purchased from Sigma-Aldrich (Milan, Italy). Cellulose (powder from spruce) was purchased from Fluka (Buchs, Switzerland). All chemicals and solvents used were of HPLC grade; ethanol was purchased from Carlo Erba (Milan, Italy), whereas the other solvents were from Merck-Millipore (Darmstadt, Germany). The enzymes pepsin (≥250 U/mg solid) from porcine gastric mucosa, pancreatin (4 × USP) from porcine pancreas, protease from Streptomyces griseus, called also Pronase E (≥3.5 U/mg solid), and Viscozyme L were purchased from Sigma-Aldrich (Milan, Italy). Samples. The tested plant foods were apple (var. annurca) without skin, frozen spinach after microwave cooking, walnuts, canned red beans, and whole wheat breakfast cereals. As whole grain, Shredded Wheat (General Mills, Minneapolis, MN, USA) was used, whereas the other foods were purchased at a local market and immediately freezedried. The macronutrient composition of foods expressed as percentage of each nutrient class by total weight is shown in Table 1. After freeze-drying, all samples were ground by a mill (GrindomixRetsch GM200 type), and the digestion protocols were run three times on each sample. The TAC of each sample was also measured in triplicate.
Figure 1. Protocol of the in vitro multistep enzymatic digestion. 4120
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after the four enzymatic digestions (sample 5°I) and the soluble fractions were used to calculate the overall TAC. Five grams of milled dry sample of each food was subjected to in vitro digestion. The first step was done by suspending the material in 50 mL of water to extract all of the water-soluble component. After 30 min at 37 °C under stirring, the samples were centrifuged, and the pellets obtained by centrifugation (1°I) were resuspended in acidified water (6 M HCl up to pH 2); 5 mL of pepsin solution (12.5 mg/mL 0.1 M HCl) was added, and the mixture was incubated for 1 h (gastric phase). The subsequent centrifugation of the mixture allowed the recovery of the insoluble material (2°I); after increase of the pH to 7.5 with NaHCO3, 5 mL of a 10 mg/mL pancreatin solution was added, and the mixture was kept for 5 h in agitation (duodenal phase). Finally, the remaining insoluble materials were treated first (3°I) with 5 mL of 1 mg/mL Pronase E solution (pH 8, 1 h) and then (4°I) with 150 μL of Viscozyme L (16 h, pH 4), obtaining the final pellet (5°I). Pronase E could simulate bacterial protease activity and is particularly suitable to hydrolyze insoluble material, whereas Viscozyme L, containing a mix of enzymes hydrolyzing complex polysaccharides, was used to obtain a final disruption of the plant food matrix chemical structures. At each step the antioxidant activities of both soluble and insoluble parts were measured. In particular after separation, both supernatants and the pellets were weighed; then an aliquot of the supernatant was used to calculate the dry weight of the supernatant, whereas the remaining part was stored at −40 °C to measure soluble antioxidant activity. A small aliquot ( whole wheat (∼84%) > beans = spinach (about 77%) > apple (about 65%).45,46 In this study the contribution of phytochemicals bound to the fiber was considered in the calculation of the OP_TAC, using a multienzyme complex (Viscozyme L) containing a wide range of carbohydrases (including arabanase, cellulase, β-glucanase, hemicellulase, and xylanase). Moreover also Pronase E, a preparation containing a mixture of bacterial protease particularly suitable for insoluble material, was adopted. This difference in the experimental approach with respect to the works previously performed was of utmost importance. In fact, data clearly showed that in foods having a high amount of insoluble dietary fiber and/or phytochemicals bound to dietary fiber or entrapped in the food structures (as in whole wheat, spinach, and bean), the action of bacterial enzymes might dramatically increase the antioxidant potential of the food residues in the lower GI tract. We have previously highlighted the physiological importance of this phenomenon for cereal dietary fiber and whole grains.41 Here this relevance was extended to all foods having a strong fiber structure, such as spinach,47 as well as to other polyphenol-rich foods having a significant amount of insoluble component made up of polysaccharides and proteins bound with phenolic acids, flavonols, anthocyanins, and proanthocyanidins.19−22 It is worth remembering that this in vitro approach does not take into account the bacterial biotransformation, being focused only on the relationship between disruption of food structure and release of TAC from chemical and enzyme points of view. Have These Findings Any Possible Health Implications? Epidemiological studies indicated that dietary fiber content in plant foods may majorly contribute to the negative associations between their intake and colorectal cancer risk.48−50 Looking at the results of this paper with a wider physiological prospective, they suggested that the TAC of the insoluble material produced at each step of the digestion, more than the simple amount of dietary fiber, might be considered for a more reliable evaluation of the potential benefits of some foods inside the GI tract. It has been recently reported that individuals with a low bacterial richness harbored a more pronounced inflammation-associated microbiota when compared with high bacterial richness individuals.51 The insoluble material present in the colon after the whole digestion, through a chemical action in the gut environment, may play a major role in reducing local oxidative stress and in modifying microbiota composition, consequently ameliorating gut permeability and boosting anti-inflammatory mechanisms and immunity. The data demonstrated that for those foods having a high amount of polyphenols bound to dietary fiber or entrapped in the food matrix, the action of bacterial enzyme is fundamental
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AUTHOR INFORMATION
Corresponding Author
*(V.F.) Phone:+31 (0)317485171. Fax: +31 (0)317485171. Email:
[email protected]. Notes
The authors declare no competing financial interest.
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ABBREVIATIONS USED AHE_TAC, TAC of alkaline hydrolysis extract; PB_TAC, TAC potentially bioaccessible (sum of the five digestion soluble fractions); BOUND_TAC, bound TAC (PB_TAC − FREE_TAC); HAE_TAC, TAC of hydroalcoholic extract; FREE_TAC, free TAC (1°S of digestion); OP_TAC, overall potential TAC (PB_TAC + 5°I_TAC); TAC, total antioxidant capacity; TPE_TAC, AHE_TAC + HAE_TAC; W_TAC, TAC of whole food measured with QUENCHER
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