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Effect of grape antioxidant dietary fiber on the lipid oxidation of raw and cooked chicken hamburgers
LWT - Food Science and Technology 42 (2009) 971–976
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Effect of grape antioxidant dietary fiber on the lipid oxidation of raw and cooked chicken hamburgers ˜ i a, * S.G. Sa´yago-Ayerdi a, A. Brenes b, I. Gon a b
Department of Nutrition, Faculty of Pharmacy, Universidad Complutense de Madrid, 28040 Madrid, Spain Department of Nutrition and Metabolism, Instituto del Frı´o, CSIC, Madrid 28040, Madrid, Spain
a r t i c l e i n f o
a b s t r a c t
Article history: Received 28 April 2008 Received in revised form 24 July 2008 Accepted 17 December 2008
Efficiency of four concentrations (0.5, 1, 1.5 and 2%) of grape antioxidant dietary fiber (GADF) on susceptibility of raw and cooked chicken breast hamburger to lipid oxidation was investigated after 0, 3, 5 and 13 days of refrigerated storage at 4 C. Color changes, sensorial qualities and acceptability by panellist were evaluated. Lipid oxidation was assessed by monitoring malondialdehyde formation with 2-thiobarbituric acid (TBARS) assay and radical scavenging capacity by ABTS method. A significant reduction in lightness and yellowness and a significant increase in redness as a result of GADF addition were observed in raw and chicken hamburgers. Addition of GADF significantly improved the oxidative stability and the radical scavenging activity in raw and cooked chicken hamburgers. The ability of GADF to prevent lipid oxidation was concentration-dependent. Acceptability of chicken meat was not affected by the addition of GADF. These results show that GADF is a very effective inhibitor of lipid oxidation and has potential as a natural antioxidant in raw and chicken cooked meats. Ó 2009 Elsevier Ltd. All rights reserved.
Keywords: Antioxidant dietary fiber Grape polyphenols Lipid peroxidation Chicken meat
1. Introduction Meat and meat products are essential components in the diets of developed countries. Their consumption is affected by various factors. The most important ones are product characteristics, consumer and environment related (Jime´nez-Colmenero, Carballo, & Cofrades, 2001). Health promoting functional foods, prepared on basis of meat is becoming more and more popular. Chicken meat has many desirable nutritional characteristics such as a low lipid content and relatively high concentration of polyunsaturated fatty acids which can be further increased by specific dietary strategies (Bourre, 2005). However, a high degree of polyunsaturation accelerates oxidative processes leading to deterioration in meat flavor, color, texture and nutritional value (Mielnick, Olsen, Vogt, Adeline, & Skrede, 2006). The major strategies for preventing lipid oxidation are the use of antioxidants and restricting the access to oxygen during storage vacuum-packaging (Tang, Kerry, Sheehan, Buckley, & Morrissey, 2001). The antioxidant additives are added to fresh and further processed meats to prevent oxidative rancidity, retard development of off-flavors, and improve colour stability (Nam & Ahn, 2003). Synthetic antioxidants such as butylated hydroxytoluene * Corresponding author. Departamento de Nutricio´n I, Facultad de Farmacia, Avda. Complutense s/n. Ciudad Universitaria, 28040 Madrid, Espan˜a. Tel.: þ34 91 394 18 12; fax: þ34 91 394 17 32. ˜ i). E-mail address: [email protected] (I. Gon 0023-6438/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.lwt.2008.12.006
(BHT) and butylated hydroxyanisole (BHA) have been used to control lipid oxidation in meat. However, recent concern over their use (Okada et al, 1990) has created a need and prompted research for alternatives antioxidants, particularly from natural sources. The use of natural preservatives to increase the shelf life of meat products is a promising technology since many vegetal substances have antioxidant and antimicrobial properties. Functional ingredients in meat products may improve the nutritional and health qualities and prolonging their self-life (Ferna´ndez-Gine´s, Ferna´ndez-Lo´pez, Sayas-Barbera´, & Pe´rez-Alvarez, 2005). Plants’ extracts rich in polyphenols are good candidates, since they are easily obtained from natural sources and they efficiently prevent lipid oxidation in food products. Grape seed extract has been evaluated for its antioxidative effect on a few meat types and has been reported to improve the oxidative stability of cooked beef (Ahn, Grun, & Fernando, 2002), turkey patties and cooled stored turkey meat (Lau & King, 2003; Mielnick et al., 2006). Dietary fiber has been considered as a functional ingredient in meat products (Cofrades, Serrano, Ayo, Solas, Carballo, & Jime´nez-Colmenero, 2004; Serrano, Cofrades, & Jime´nez-Colmenero, 2006). The inclusion of dietary fiber may improve texture (Cofrades et al., 2004), increase the cooking yield due to water-holding and fat binding properties and also dietary fiber may generate technological properties that improve physicochemical and sensory properties (Jime´nez-Colmenero et al., 2003).
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Dietary fiber and natural antioxidants are two dietary factors involved in health promoting. A natural product that combines high amounts of dietary fiber and phenolics antioxidants such as pehnolics acids, anthocyanidins, proanthocyanidins, catechins and other flavonoides is grape antioxidant dietary fiber (GADF) (Saura˜ i, CSIC-UCM, ES 2259258A1; Calixto, 1998, Saura-Calixto & Gon Saura-Calixto & Larrauri, CSIC, ES 2130092A1). Recently, GADF had been successfully used as an ingredient in minced fish (Sa´nchezAlonso, Jime´nez-Escrig, Saura-Calixto, & Borderı´as, 2007). The present study was designed to study the effect of grape antioxidant dietary fiber (GADF) on breast chicken hamburgers to reach two objectives: 1) To assess the effectiveness of GADF on lipid stability during refrigerated storage for increasing the shelf life of the food and 2) to incorporate dietary fiber in a meat product to enhance health-beneficial properties. Sensory qualities and acceptability by panellists were also evaluated. 2. Materials and methods 2.1. Preparation of meat and samples Six weeks old male broilers (body weight, 2.2 0.2 kg) were supplied by the Veterinarian Faculty of the Complutense University of Madrid. Chickens were fed a commercial corn–soybean diet formulated to meet the minimum National Research Council (1994) requirements for broiler chickens. All housing and handling were approved by the University Complutense of Madrid Animal Care and Ethics Committee in compliance with the Ministry of Agriculture, Fishery and Food for the Care and Use of the Animals for Scientific Purpose. Twelve birds were slaughtered and carcass was immediately trimmed for breast meat. Fresh breast meat (about 2 kg) was minced twice (4 mm plate) using a grinder (Mainica, Granollers, Spain) and it was packed on four portions to be used and analyzed on day 0 and after 3, 5, and 13 days of storage at 4 C. Red grape pomace (Vitis vinifera var. Cencibel, La Mancha, Spain) obtained from winery was processed following a patented proce˜ i, CSIC-UCM, ES 2259258A1; Sauradure (Saura-Calixto & Gon Calixto & Larrauri, CSIC, ES 2130092A1), freeze-dried, milled to a particle size less than 0.5 mm. The final product, named grape antioxidant dietary fiber (GADF), was used as a functional ingredient in the formulation of minced chicken breast meat. Hamburgers were prepared following a homemade formulation, using these ingredients: breast meat (85.4%), whole egg (6.8%), breadcrumbs (6.8%) and species (1%). The minced breast was treated with four concentrations of GADF (0.5, 1, 1.5 and 2%). Controls without GADF were used in all assays. Ingredients and GADF were blended in a bowl mixer (Hobart, Model N50, USA) during 3 min, to ensure uniform distribution of the added ingredients. Ready-meat hamburgers were packed (300 g per trial) in vacuum high oxygen barrier bags (nylon/polyethylene, 9.3 ml O2/m2/24 h at 0 C, Koch Kansas City, MO) and were stored in refrigeration at 4 C. The first day of analysis in each trial, the bag was broken and four portions were formed to be analyzed on day 0 and after 3 and 5 days of storage at 4 C. These portions were wrapped in a transparent oxygen-permeable polyvinyl chloride film (13,500 cm3/m2/day), and was stored at 4 C. Hamburgers (50 g) were formed using a conventional burgermaker. They were cooked in an electric pan previously greased with ˜ a) at olive oil (Plactronic, Selecta, J.P. Selecta, S. A. Barcelona, Espan 170 C and pressed 30 s. After 1.5 min hamburgers were turned over and left for another 1.5 min. Finally, it was cooled for 2 min, served to panelists and a portion of cooked meat hamburger was reserved for further analysis. The same procedure was followed for cooking meat hamburger after 3 and 5 days. A portion of raw meat
hamburger was stored on refrigeration and used for further analysis (days 0, 3, 5 and 13). 2.2. Chemical analysis The proximate analyses in GADF were determined using AOAC (2000) methods: protein (Method 950.48), fat (Method 969.24), and moisture (Method 925.09). Protein content was evaluated using a Nitrogen Determinator LECO FP-2000 (Leco Corporation, St Joseph, MI, USA). 2.2.1. Dietary fiber Dietary fiber (DF) in GADF, was analyzed by the AOAC (2000) enzymatic–gravimetric method (Method 991.42) modified in our ˜ as & Saura-Calixto, 1995). The sample was treated laboratory (Man with heat stable a-amylase A-3306 (Sigma Chemical CO, St Louis MO, USA), protease P-3910 (Sigma Chemical CO, St Louis MO, USA) and amyloglucosidase A-9913 (Sigma Chemical CO, St Louis MO, USA) to remove protein and starch. Remaining residues were separated by centrifugation (15 min, 25 C, 3000 g) instead of filtration to separate the soluble and insoluble fractions. The supernatants were dialysed against water to avoid losses of soluble dietary fiber (SDF), substituted ethanol precipitation of SDF. Dialysates were submitted to acid hydrolysis with 1 M sulphuric acid, and SDF was measured spectrophotometrically (Englyst & Cummings, 1988) with dinitrosalysilic acid (Panreac 162837, Barcelona, Spain). Residues from centrifugation were quantified gravimetrically. This value was insoluble dietary fiber (IDF). 2.2.2. Extraction of phenolics GADF sample was 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, 3000 g) supernatants were combined and used to determine extractable polyphenols content and free radical scavenging assay (ABTS). Extractable polyphenols were determined by the Folin–Ciocalteau procedure (Montreau, 1972) using gallic acid as standard. 2.2.3. Non-extractable polyphenols Proanthocyanidins (condensed tannins) and hydrolysable phenols were determined in the residues of the methanol–water and acetone–water extraction in GADF. The residue was treated with 5 ml/L HCl–Butanol (3 h, 100 C) (Reed, McDowell, Van Soest, & Horvarth, 1982) for proanthocyanidins hydrolysis. Proanthocyanidins were calculated from the absorbance at 550 nm using Mediterranean carob pod (Ceratonia siliqua L.), supplied by Nestle´ S.A. as standard. Hydrolysable phenols were determined by a methanol/H2SO4 90:10 (v/v) hydrolysis at 85 C for 20 h (Hartzfeld, Forkner, Hunter, & Hagerman, 2002) of the residues from of methanol–water and acetone–water extraction. Samples were centrifuged (15 min, 25 C, 3000 g) and the hydrolysable polyphenols were determined in supernatants by Folin–Ciocalteau procedure (Montreau, 1972), using gallic acid as standard. 2.3. Color measurement Hunter L* (lightness), a* (redness), and b* (yellowness) were evaluated for raw (day 0) and cooked hamburger meat in 0, 3 and 5 days. Samples were prepared as described before. Surface color measurements were determined using a Hunter Lab model D12-9 (D65/10 ) (Hunter Associates Laboratory In., Reston, VA). The chromameter was calibrated on the Hunterlab color space system using a white tile.
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2.4. Lipid stability measurements 2.4.1. Measurement of lipid oxidation. Thiobarbituric acid index (TBARS) The extent of lipid oxidation was determined by measuring the TBARS-reacting substances at days 0, 3, 5 and 13 in raw hamburgers and days 0, 3 and 5 in cooked hamburgers. Values were expressed as mg of malondialdehyde per kilogram of sample using the procedure described by Salih, Smith, Price, and Dawson (1987). Briefly, 10 g of meat was homogenized with 35 mL of 3.86% perchloric acid in an Ultra-Turrax (IKA Works Inc., Wilmington NC) at 13,800 rpm for 1 min. BHA was added before homogenization at a level of 125 mg/mg of fat. The blended was filtered through Wathman 2V filter into 50 mL Erlenmeyer flasks. The filtrate (5 mL) was mixed with 5 mL of 0.02 M thiobarbituric acid (TBA) in distilled water in capped test tubes. Tubes were incubated in boiling water for 30 min. The absorbance was determined at 531 nm against a blank containing 5 mL of distilled water and 5 mL of 0.02 M TBA solution. The antioxidant effectiveness was calculated as per cent inhibition of oxidation (% I) as described by Frankel (1998): % I ¼ ((c s)/c) 100, where c ¼ high increment of control in the experiment and s ¼ increment of sample with added GADF at the same time. High levels of % I indicate greater antioxidant effectiveness. 2.4.2. Free radical scavenging. ABTS assay The antioxidant capacity was estimated in terms of radical scavenging activity following the procedure described elsewhere (Re et al., 1999) with some modification (Pulido, Herna´ndez-Garcı´a, & Saura-Calixto, 2003). Briefly, ABTS [2,2-azinobis(3-ethilenzotiazolin)-6-sulfonate] radical cation (ABTSþ) was produced by reacting 7 mmol/L ABTS stock solution with 2.45 mmol/L potassium persulphate in the dark at room temperature for 12–16 h before use. The ABTSþ solution was diluted with methanol to an absorbance of 0.70 0.02 at 730 nm. ABTSþ solution (3.9 mL) and phenolic extract (0.1 mL) were mixed and the absorbance was read every 20 s using a Beckman DU-640 spectrophotometer. The reaction was monitored during 6 min. Inhibition of absorbance vs time was plotted and the area below the curve (0–6 min) was calculated. The antioxidant results were expressed as mmol equivalents of trolox per gram of sample (dry matter).
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The hamburgers were cooked and cut into four similar pieces and served warm (w45 C) to the panelists in individual cage. They used a structured scale to evaluate the samples from very undesirable (value 0) to very desirable (value 5) for each evaluated parameter (ISO, 1985). 2.6. Statistical analysis Results were expressed by means standard error of three or more separate determinations. Comparison of means was performed by one-way and two-way analysis of variance (ANOVA). Tukey HSD test was used to determine the differences in the mean values (P < 0.05). Data were analyzed using SPSS V.13.0 software (SPSS Institute Inc., Cary, NC). 3. Results and discussion 3.1. Characterization of grape antioxidant dietary fiber The proximal composition of the GADF might change slightly due to the vintage. Dietary fiber and phenolic compounds are the main components of the GADF (Table 1). It is worth noting that the soluble dietary fiber content of GADF is relatively high. The other majority components, phenolic components of GADF, may be associated to dietary fiber matrix as to soluble and insoluble ˜ i, & Saura-Calixto, 2007). This composicomponents (Serrano, Gon tion confers appreciable nutritional properties to the whole. Phenolic compounds represent around 23% dry matter of the sample. This value corresponds to the total extracted and nonextracted polyphenols by organic solvents. Extractable polyphenols represent only 21% of total phenolic compounds contained in the sample being the main components catechins (46.8%), benzoic acids (16%), flavonols (14%) and anthocyanidins (16.2%) (Pe´rezJime´nez et al., 2008). On the other hand, non-extractable polyphenols represent 17.5% of GADF dry matter and the major part corresponds to condensed tannins. The presence of phenolic compounds may be significant on health properties because they show antioxidant capacity (Yilmaz & Toledo, 2004), but this property may depend on the degree of polymerization (Blazso´, Ga´bor, & Rohdewald, 1997; Serrano et al., 2007). GADF exhibited relatively ˜ i & Serrano, 2005) and it may be high antioxidant activity (Gon considered as antioxidant dietary fiber (Saura-Calixto, 1998).
2.5. Sensory evaluation 3.2. Color measurement or stability 2.5.1. Preference test Control and GADF (0.5, 1, 1.5 and 2%) hamburgers were cooked, cut into pieces of uniform size and served warm (w45 C) to a fifteen non-trained panel members. Volunteers classified the samples in order of preference (from 1, like much to 4, like less) without allowing ties between samples (ISO, 1985). Results were analyzed using a Friedman repeated measures analysis of variance on ranks procedure. Statistical analysis was run using the computer SPSS V.13.0 software (SPSS Institute Inc., Cary, NC). In this test, panelists decided the preference levels of GADF. The identification codes of the samples were the following: CK(cooked)-GADF-0.5%; CK-GADF-1%; CK-GADF-1.5%; CK-GADF-2%. 2.5.2. Affective test Control and GADF (1 and 2%) hamburgers were selected previously by the panelists in preference test to run the affective test. The evaluations were made in cooked samples after 0, 3 and 5 days of storage of raw hamburger at 4 C. The panelist members (n ¼ 15) were selected in preliminary sessions and received a description of attributes and terminology used in the test. The sensory parameters for the cooked hamburgers were taste, tenderness, color and odor.
The color of chicken product is one of the main factors by which consumers judge their acceptability. It depends on various factors, including the concentration and chemical state of meat pigment, physical characteristics of the meat and the presence of non-meat ingredients (Hunt & Kropf, 1987). The addition of no chicken ingredients like GADF and the storage conditions can cause changes Table 1 Proximate composition of grape antioxidant dietary fiber (g dry matter per 100 g). Protein Fat Ash Fibera Soluble Dietary Fiber Insoluble Dietary Fiber
11.08 0.46 7.69 0.49 5.25 0.19 77.60 3.01 15.53 0.11 62.07 3.01
Polyphenols Extractable polyphenols Condensed tannins Hydrolizable tannins
4.93 0.03 14.81 0.19 2.70 0.19
a
Residual polyphenolic contents may be included in this value.
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Table 2 Color changes (Lightness L*, redness a*, yellowness b*) for raw (day 0) and cooked chicken hamburger containing added grape antioxidant dietary fiber (GADF) during 0, 3 and 5 days of storage. Storage/
Sample
L*
Day 0
Raw hamburger RW-C RW-GADF-1 RW-GADF-2
a*
b*
58.1 0.1a 44.8 0.2d 41.9 1.0e
1.7 0.1a 2.7 0.1ab 3.3 0.5ab
16.2 0.2a 9.2 0.1b 4.5 0.1d
Cooked hamburger CK-C 77.4 1.3b CK-GADF-1 75.6 1.0b CK-GADF-2 60.4 0.6a
0.2 0.1e 1.8 0.3ab 2.8 0.6ab
19.6 0.7a 22.5 0.4a 11.6 0.9c
Day 3
CK-C CK-GADF-1 CK-GADF-2
72.4 1.5c 58.9 0.8a 55.3 0.9d
3.5 0.9b 3.3 0.5b 4.8 0.6bc
22.8 0.7a 11.8 0.9cd 9.9 0.8c
Day 5
CK-C CK-GADF-1 CK-GADF-2
69.7 1.6c 57.3 1.3ad 50.8 0.5f
3.7 1.0b 4.0 0.5bc 5.4 0.6c
21.6 0.8a 12.5 1.3c 11.0 0.5c
Means in a column not sharing the same letter are significantly different (P < 0.05), values are mean SEM, n ¼ 6.
in poultry products. This fact had been observed in other similar meat products (Lau & King, 2003). Effect of GADF on color stability (Lightness L*, redness a*, yellowness b*) in cooked chicken hamburgers is shown in Table 2. Significant reduction in the lightness values, as a result of GADF addition was observed at day 0 in raw (up to 28%) and at day 5 in cooked chicken hamburger (up to 27%) in comparison to controls. This effect could be a consequence of the structural disintegration of the muscle, during the grinding because it augments the surface area exposed to oxygen, and it causes the meat to brown more readily than whole meat (Young & West, 2001). Addition of GADF also resulted in significant reduction (up to 24%) in lightness values, relative to controls in cooked chicken hamburgers after 3 and 5 days of refrigerated stored at 4 C. This effect has been attributed to the dilution of meat pigment in other meat products due to the presence of non-meat ingredients (Rocha-Garza & Zayas, 1996). However, this parameter was not different (P > 0.05) in CK-C and CK-GADF-1 hamburgers in day 0. The redness values as a result of GADF addition were higher in raw and cooked chicken hamburger (up to 2.8 times) in comparison to controls in day 0. These a* values were stabilized among storage period in hamburger added with GADF. Addition of GADF also resulted in a significant increase (2.22 times) in redness values, relative to controls, in cooked chicken hamburger after 3 and 5 days of storage. This could be due to phenolics present in GADF that
could stabilize redness among storage. Similar effect has been observed using a high dose of green tea ethanolic extract in raw patties (Jo, Son, Son, & Byun, 2003) and in beef patties (Tang et al., 2001; Tang, Kerry, Sheehan, & Morrissey, 2000). The enhancing effect of GADF is also possibly due to the red color of this product. Similar results have been reported by Carpenter, O’Grady, O’Callaghan, O’Brien, and Kerry (2007) in raw and cooked pork using grape seed extract. Significant reduction in the yellowness values in raw chicken hamburger was expected due to the GADF added. However, the b* values among days 3 and 5 were stable in cooked hamburgers added with 1 and 2% GADF. The yellowness values obtained in the cooked hamburger were similar to those reported by Mitsumoto, O’Grady, Kerry, and Buckley (2005) for chicken patties by the addition of tea catechins. Addition of GADF also resulted in significant reduction (up to 52%), relative to controls, only after 3 days of storage at 4 C. 3.3. Lipid oxidation The extent of lipid oxidation in raw chicken hamburger meat stored for 0, 3, 6, and 13 days is illustrated in Table 3. Storage period had significant influence on the development of lipid oxidation in the chicken meat resulting in an increase of TBARS values during the 13 days of storage. The lipid oxidation index was most efficient in 1% GADF added raw hamburger than 2% GADF raw hamburger. TBARS values increased significantly in raw and cooked control hamburgers. However, when GADF was added, the chicken hamburger meat resisted the lipid oxidation and showed similar values of TBARS during the storage. GADF showed a significant protective effect towards lipid oxidation. This effect may be depending on the concentration of GADF because the highest concentration of antioxidant (2% GADF) retarded the oxidation process most efficiently by maintaining TBARS values during 13 days storage. Similar values of TBARS were reported by Tang et al. (2001) for chicken breast. Our study also confirms in vitro observations that the addition of wine polyphenols to various food systems (fish lipids, frozen fish and turkey meat) inhibits lipid oxidation (Lau & King 2003; Mielnick et al., 2006). The mechanism of the protective effect on lipid oxidation may be due to the presence in GADF of a number of oligomer procyanidins, such as catechin and epicatechin (Yilmaz & Toledo, 2004). The malondialdehyde content in the CK-C and CK-GADF-1 was increased among storage in refrigeration. However, CK-GADF-2 did not show statistical differences (P > 0.05) during storage in TBARS values. This could be due to a better inhibitory effect of 2% GADF added instead of 1%.
Table 3 Effect of grape antioxidant dietary fiber (GADF) on TBARS values (mg malondialdehyde/kg meat) in raw chicken hamburger (0, 3, 5 and 13 days) and cooked chicken hamburger after 0, 3 and 5 days of refrigerated storage. Storage day
%I
0
3
5
13
Raw hamburger RW-C RW-GADF-1 RW-GADF-2
0.84 0.04aA 0.89 0.01aA 1.09 0.02aB
0.99 0.01bA 1.01 0.01bA 1.16 0.02abB
1.15 0.04cA 0.92 0.01aB 1.18 0.02bA
2.05 0.09dA 1.30 0.01cB 1.42 0.01cC
0 36.6 30.5
Cooked hamburger CK-C CK-GADF-1 CK-GADF-2
1.36 0.17aA 1.10 0.01aA 1.42 0.08aB
1.42 0.02bA 1.31 0.0abB 1.56 0.06aC
1.82 0.01cA 1.59 0.08bB 1.35 0.08aC
ndd nd nd
0 12.6 25.8
Means in a row (a–d) not sharing the same letter are significantly different (P < 0.05), values are mean SEM (n ¼ 6). Different letter within the same column (A–C) differ (P < 0.05), values are the mean SEM (n ¼ 6). % I ¼ ((c s)/c) 100, where c ¼ high increment of control in the experiment and s ¼ increment of sample with added GADF at the same time. High levels of % I indicate greater antioxidant effectiveness. nd ¼ not determined.
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The cooked hamburgers were more susceptible to lipid oxidation than raw meat because heating accelerates oxidative reactions in meat (Kingston, Monahan, Buckley, & Lynch, 1998). The membranal phospholipids, which are high in polyunsaturated fatty acids, are responsible for the initial development of oxidation in raw and cooked meat (Gray & Pearson, 1987). Cooked samples also showed TBARS index values lower in samples with GADF added, being the highest concentration of antioxidant (2% GADF) most efficient to maintain a retarded oxidation process. The rate of inhibition at 5 days of storage was 13% for the 1% GADF sample while this index was 26% for the samples with 2% added antioxidant fiber. 3.4. Scavenging effect The grape polyphenols have considerable potential as antioxidants, based on the combined actions of extractable polyphenols (anthocyanins, flavonols, flavan-3-ols and phenolic acids) and nonextractable polyphenols (polymeric proanthocyanidins and high molecular weight hydrolysable tannins), both are able to scavenge radicals which are important in preventing the development of rancidity in foods. The addition of GADF, increased significantly (P < 0.05) the radical scavenging effect of raw and cooked hamburgers (Table 4). This increment was according to the percentage of GADF added. The evolution of this parameter was different depending on the treatment. Raw meat hamburger maintained similar values during storage period, being always more elevated for added GADF samples. However, cooked hamburgers showed a light increase after third day of storage for control samples, while added GADF samples followed different evolution according to the percentage of GADF. Meat samples with 1% GADF maintained values during 13 days storage, while samples with 2% significantly decreased the radical scavenging capacity. TBARS values and radical scavenging capacity values are in accordance. Both values seem to indicate that antioxidant compounds contained in GADF are effectively used to inhibit or to retard the oxidative process in the meat.
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Table 5 Sensory evaluation test in cooked chicken hamburgers containing added grape antioxidant dietary fiber (GADF) levels. Preference test Friedman’s test
Affective test C-CK CK-GADF-1 CK-GADF-2
CK-GADF-0.5 1.9 1.1a
CK-GADF-1 3.3 1.0b
CK-GADF-1.5 2.6 1.0c
CK-GADF-2 2.58 1.2c
Flavor
Tenderness
Odor
Color
2.7 1.1a 2.6 0.8a 2.6 0.9a
3.1 0.9a 2.9 0.9a 2.7 1.0a
3.0 1.0a 2.7 0.9a 2.9 1.1a
3.35 1.2a 2.56 0.7b 2.32 0.7b
Pool of results in hamburgers cooked. Means in a row not sharing the same letter are significantly different (P < 0.05). Different letter within the same column differ (P < 0.05), values are the mean ED, n ¼ 39.
values to hamburgers prepared with 1.5 and 2.0% (P > 0.05) of GADF. Therefore, 2% was chosen for further evaluations. The affective test was passed in three times corresponding to the meat on refrigeration during 0, 3 or 5 days. The values obtained every day did not show statistical differences (P > 0.05). Results are shown in a pool expressed in Table 5. Flavor, tenderness, and odor were similar (P > 0.05) for all samples. Flavor expresses the taste experience when a condiment is taken into a mouth; tenderness shows the easiness to cut or chew the hamburger; and odor describes as the sensation that results when olfactory receptors in the nose are stimulated. The dietary fiber content in the hamburgers added with GADF might improve stability in flavor and tenderness in spite of the phenolics compounds present in the samples. The soluble dietary fiber content in GADF might supply texture, water-holding and avoid the lost of these sensorial attributes in the samples. The color was other attribute evaluated by panelist (Table 5) and by chromameter (Table 2). In both cases were detected differences in the appearance of the hamburger described in terms of a person perception of the hue and lightness. This fact was expected because GADF shows and intense color due to the presence of phenolic compounds in the sample. However, this parameter did not affect the acceptance of hamburgers by the panelists.
3.5. Sensory evaluation at hamburgers The preference test was carried out in order to choose the better level of GADF added (0.5, 1, 1.5 and 2% respectively). The statistical analysis of the test (Table 5) showed that the hamburgers prepared with 1.0, 1.5 and 2.0% added of GADF obtained the higher mark values (P < 0.05) in sensory evaluation. Panelists gave similar
Table 4 Radical scavenging capacity (ABTS method) of raw and cooked chicken hamburgers containing added grape antioxidant dietary fiber (GADF) during 0, 3 and 5 days of refrigerated storage (at 4 C)a,b. Storage day 0
3
5
Raw hamburger RW-C RW-GADF-1 RW-GADF-2
4.94 0.19aA 8.08 0.17aB 12.02 0.3aC
5.23 0.41aA 8.14 0.43aA 12.35 0.29aC
5.66 0.18aA 8.47 0.23aB 12.57 0.43aC
Cooked hamburger CK-C CK-GADF-1 CK-GADF-2
5.22 0.06aA 9.08 0.16aB 11.02 0.14aC
6.42 0.32bA 9.20 0.73aB 12.70 0.30bC
6.56 0.14bA 10.18 0.15aAB 10.36 0.12aB
Means in a row (a–c) not sharing the same letter are significantly different (P < 0.05), values are mean SEM (n ¼ 6). Different letter within the same column (A–C) differ (P < 0.05), values are the mean SEM (n ¼ 6). RW-C: control raw.
4. Conclusions The addition of GADF in breast chicken meat inhibited oxidation during 13 days of refrigeration storage, increasing the lipid stability and the shelf life of the food. Moreover, the addition of a quality dietary fiber to a meat product enhanced the health-beneficial properties and improves stability without affecting the acceptability of the food. Due to concerns regarding the safety and toxicity of synthetic antioxidants, GADF may prove useful, as safe, natural, health promoting antioxidants to the meat industry. Acknowledgements The authors acknowledge to Direccio´n General de Eduacio´n Superior Tecnolo´gica (DGEST) in Me´xico for a scholarship (PROMEP, 022005009P), the support of the Spanish Comisio´n Interministerial de Ciencia y Tecnologı´a (Project AGL2005-04769). References Ahn, J. H., Grun, I. V., & Fernando, L. N. (2002). Antioxidant properties of natural plants extract containing polyphenolic compounds in cooked ground beef. Journal of Food Science, 67, 1364–1368. AOAC. (2000). Official methods of analysis of AOAC international (17th ed.). MD, USA: Association of Official Analytical Chemistry.
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Blazso´, G., Ga´bor, M., & Rohdewald, P. (1997). Antiinflammatory activities of procyanidin-containing extracts from Pinus pinaster Ait. Pharmazie, 52, 380–382. Bourre, J. M. (2005). Where to find omega-3-fatty acids and how feeding animals with diet enriched in omega-3-fatty acids to increase nutritional value derived products for human: what is actually useful? Journal of Nutrition, Health and Aging, 9, 232–242. Carpenter, R., O’Grady, M. N., O’Callaghan, Y. C., O’Brien, N. M., & Kerry, J. P. (2007). Evaluation of the antioxidant potential of grape seed and bearberry extracts in raw and cooked pork. Meat Science, 76, 604–610. Cofrades, S., Serrano, A., Ayo, J., Solas, M. T., Carballo, J., & Jime´nez-Colmenero, F. (2004). Restructured beef with different proportions of walnut as affected by meat particle size. European Food Research and Technology, 218, 230–236. Englyst, H. N., & Cummings, J. H. (1988). Improved method for the measurement of dietary fiber as nonstarch polysaccharides in plant foods. Journal of Association of Official Analytical Chemistry, 71, 808–814. Ferna´ndez-Gine´s, J. M., Ferna´ndez-Lo´pez, J., Sayas-Barbera´, E., & Pe´rez-Alvarez, J. A. (2005). Meat products as functional foods: a review. Journal of Food Science, 70, 37–43. Frankel, E. N. (1998). Antioxidants. In Lipid oxidation. Dundee, Scotland: The Oily Press. ˜ i, I., & Serrano, J. (2005). The intake of dietary fiber from grape seeds modifies Gon the antioxidant status in rat cecum. Journal of the Science of Food and Agriculture, 85, 1877–1881. Gray, J. I., & Pearson, A. M. (1987). Rancidity and warmed over flavour. Advances in Meat Research, 3, 221–229. Hartzfeld, P. W., Forkner, R., Hunter, D. M., & Hagerman, A. E. (2002). Determination of hydrolyzable tannins (gallotannins and ellagitanins) after reaction with potassium iodate. Journal of Agricultural and Food Chemistry, 50, 1785–1790. Hunt, M. C., & Kropf, D. H. (1987). Color and appearance. In A. M. Pearson, & R. T. Dutson (Eds.), Restructured meat and poultry products, advanced in meat research, Vol. 3 (pp. 125–159). New York: Van Nostrand. ISO. (1985). Sensory analysis. Methodology. General guidance. ISO-DP 6658. Ge´neve: International Organization for Standardization. Jime´nez-Colmenero, F., Carballo, S., & Cofrades. (2001). Review. Healthier meat and meat products: their role as functional foods. Meat Science, 59, 5–13. Jime´nez-Colmenero, F., Serrano, A., Ayo, J., Solas, M. T., Cofrades, S., & Carballo, J. (2003). Physicochemical and sensory characteristics of restructured beef steak with added walnuts. Meat Science, 65, 1391–1397. Jo, C., Son, J. H., Son, C. B., & Byun, M. W. (2003). Functional properties of raw and cooked pork patties with added irradiated, freeze-dried green tea leaf extract powder during storage at 4 C. Meat Science, 64, 13–17. Kingston, E. R., Monahan, F. J., Buckley, D. J., & Lynch, P. B. (1998). Lipid oxidation in cooked pork as affected by vitamin E, cooking and storage conditions. Journal of Food Science, 63, 386–389. Lau, D. W., & King, A. J. (2003). Pre- and post-mortem use of grape seed extract in dark poultry meat to inhibit development of thiobarbituric acid reactive substances. Journal of Agricultural and Food Chemistry, 51, 1602–1607. ˜ as, E., & Saura-Calixto, F. (1995). Dietary fiber analysis: methodological error Man sources. European Journal of Clinical Nutrition, 49, 158–162. Mielnick, M. B., Olsen, E., Vogt, G., Adeline, D., & Skrede, G. (2006). Grape seed extract as antioxidant in cooked, cold stored turkey meat. LWT Food Science and Technology, 39, 191–198. Mitsumoto, M., O’Grady, M. N., Kerry, J. P., & Buckley, D. J. (2005). Addition of tea catechins and vitamin C on sensory evaluation, colour and lipid stability during chilled storage in cooked or raw beef and chicken patties. Meat Science, 69, 773–779.
Montreau, F. R. (1972). Sur le dosage des compose´s phe´noliques totaux dans les vins par la methode Folin–Ciocalteau. Connaiss. Vigne Vinifera, 24, 397–404. Nam, K. C., & Ahn, D. U. (2003). Use of antioxidants to reduce lipid oxidation and off-odor volatiles of irradiated pork homogenates and patties. Meat Science, 63, 1–8. National Research Council. (1994). Nutrient requirements of poultry (9th Rev. National ed.). Washington, DC: Academic Press. Okada, Y., Okajima, M., Konoshi, H., Teranchi, M., Ishii, K., Lin, I. M., et al. (1990). Antioxidant effect of naturally occurring furan fatty acids on oxidation of linoleic acid in aqueous dispersion. Journal of American Oil Chemical Society, 67, 858–862. Pe´rez-Jime´nez, J., Serrano, J., Tabernero, M., Arranz, S., Dı´az-Rubio, M. E., Garcı´aDı´z, L., et al. (2008). Effects of grape antioxidant dietary fiber in cardiovascular disease risk factors. Nutrition, 24, 646–653. Pulido, R., Herna´ndez-Garcı´a, M., & Saura-Calixto, F. (2003). Contribution of beverages to the intake of lipophilic and hydrophilic antioxidants in the Spanish diet. European Journal of Clinical Nutrition, 57, 1275–1282. Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., & Rice-Evans, C. (1999). Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology of Medicine, 26, 1231–1237. Reed, J., McDowell, R. E., Van Soest, P. J., & Horvarth, P. J. (1982). Condensed tannins: a factor limiting the use of cassava forage. Journal of the Science of Food and Agriculture, 33, 213–230. Rocha-Garza, A. E., & Zayas, J. F. (1996). Quality of broiled beef patties supplemented with wheat germ protein flour. Journal of Food Science, 61, 418–421. Salih, A. M., Smith, D. M., Price, J. F., & Dawson, L. E. (1987). Modified extraction 2-thiobarbituric acid method for measuring lipid oxidation in poultry. Poultry Science, 66, 1483–1488. Sa´nchez-Alonso, I., Jime´nez-Escrig, A., Saura-Calixto, F., & Borderı´as, A. J. (2007). Effect of grape antioxidant dietary fiber on the prevention of lipid oxidation in minced fish: evaluation by different methodologies. Food Chemistry, 101, 372–378. Saura-Calixto, F. (1998). Antioxidant dietary fiber product: a new concept and a potential food ingredient. Journal of Agricultural and Food Chemistry, 48, 4303–4306. ˜ i, I. Functional formulation based on antioxidant dietry fiber Saura-Calixto, F., & Gon and soluble fiber. CSIC-UCM, ES 2259258A1. Saura-Calixto, F., & Larrauri, J. A. Concentrado de fibra diete´tica natural de uva y su procedimiento de obtencio´n. CSIC, ES 2130092A1. Serrano, A., Cofrades, S., & Jime´nez-Colmenero, F. (2006). Characteristics of restructured beef steak with different proportions of walnut during frozen storage. Meat Science, 72, 108–115. ˜ i, I., & Saura-Calixto, F. (2007). Food antioxidant capacity determined Serrano, J., Gon by chemical methods may underestimate the physiological antioxidant capacity. Food Research International, 40, 15–21. Tang, S., Kerry, J. P., Sheehan, D., Buckley, D. J., & Morrissey, P. A. (2001). Antioxidative effect of added tea catechins on susceptibility of cooked red meat, poultry and fish patties to lipid oxidation. Food Research International, 34, 651–657. Tang, S. Z., Kerry, J. P., Sheehan, D., & Morrissey, P. A. (2000). Dietary tea catechins and iron-induced lipid oxidation in chicken meat, liver and heart. Meat Science, 56, 285–290. Yilmaz, Y., & Toledo, R. T. (2004). Major flavonoids in grape seed and skins: antioxidant capacity of catechin, epicatechin and gallic acid. Journal of Agricultural and Food Chemistry, 52, 255–260. Young, O. A., & West, J. (2001). Meat color. In Y. H. Hui, W.-K. Nip, R. W. Rogers, & O. A. Young (Eds.), Meat science and applications (pp. 39–69). New York: Marcel Dekker.
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Effect of grape antioxidant dietary fiber on the lipid oxidation of raw and cooked chicken hamburgers ˜ i a, * S.G. Sa´yago-Ayerdi a, A. Brenes b, I. Gon a b
Department of Nutrition, Faculty of Pharmacy, Universidad Complutense de Madrid, 28040 Madrid, Spain Department of Nutrition and Metabolism, Instituto del Frı´o, CSIC, Madrid 28040, Madrid, Spain
a r t i c l e i n f o
a b s t r a c t
Article history: Received 28 April 2008 Received in revised form 24 July 2008 Accepted 17 December 2008
Efficiency of four concentrations (0.5, 1, 1.5 and 2%) of grape antioxidant dietary fiber (GADF) on susceptibility of raw and cooked chicken breast hamburger to lipid oxidation was investigated after 0, 3, 5 and 13 days of refrigerated storage at 4 C. Color changes, sensorial qualities and acceptability by panellist were evaluated. Lipid oxidation was assessed by monitoring malondialdehyde formation with 2-thiobarbituric acid (TBARS) assay and radical scavenging capacity by ABTS method. A significant reduction in lightness and yellowness and a significant increase in redness as a result of GADF addition were observed in raw and chicken hamburgers. Addition of GADF significantly improved the oxidative stability and the radical scavenging activity in raw and cooked chicken hamburgers. The ability of GADF to prevent lipid oxidation was concentration-dependent. Acceptability of chicken meat was not affected by the addition of GADF. These results show that GADF is a very effective inhibitor of lipid oxidation and has potential as a natural antioxidant in raw and chicken cooked meats. Ó 2009 Elsevier Ltd. All rights reserved.
Keywords: Antioxidant dietary fiber Grape polyphenols Lipid peroxidation Chicken meat
1. Introduction Meat and meat products are essential components in the diets of developed countries. Their consumption is affected by various factors. The most important ones are product characteristics, consumer and environment related (Jime´nez-Colmenero, Carballo, & Cofrades, 2001). Health promoting functional foods, prepared on basis of meat is becoming more and more popular. Chicken meat has many desirable nutritional characteristics such as a low lipid content and relatively high concentration of polyunsaturated fatty acids which can be further increased by specific dietary strategies (Bourre, 2005). However, a high degree of polyunsaturation accelerates oxidative processes leading to deterioration in meat flavor, color, texture and nutritional value (Mielnick, Olsen, Vogt, Adeline, & Skrede, 2006). The major strategies for preventing lipid oxidation are the use of antioxidants and restricting the access to oxygen during storage vacuum-packaging (Tang, Kerry, Sheehan, Buckley, & Morrissey, 2001). The antioxidant additives are added to fresh and further processed meats to prevent oxidative rancidity, retard development of off-flavors, and improve colour stability (Nam & Ahn, 2003). Synthetic antioxidants such as butylated hydroxytoluene * Corresponding author. Departamento de Nutricio´n I, Facultad de Farmacia, Avda. Complutense s/n. Ciudad Universitaria, 28040 Madrid, Espan˜a. Tel.: þ34 91 394 18 12; fax: þ34 91 394 17 32. ˜ i). E-mail address: [email protected] (I. Gon 0023-6438/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.lwt.2008.12.006
(BHT) and butylated hydroxyanisole (BHA) have been used to control lipid oxidation in meat. However, recent concern over their use (Okada et al, 1990) has created a need and prompted research for alternatives antioxidants, particularly from natural sources. The use of natural preservatives to increase the shelf life of meat products is a promising technology since many vegetal substances have antioxidant and antimicrobial properties. Functional ingredients in meat products may improve the nutritional and health qualities and prolonging their self-life (Ferna´ndez-Gine´s, Ferna´ndez-Lo´pez, Sayas-Barbera´, & Pe´rez-Alvarez, 2005). Plants’ extracts rich in polyphenols are good candidates, since they are easily obtained from natural sources and they efficiently prevent lipid oxidation in food products. Grape seed extract has been evaluated for its antioxidative effect on a few meat types and has been reported to improve the oxidative stability of cooked beef (Ahn, Grun, & Fernando, 2002), turkey patties and cooled stored turkey meat (Lau & King, 2003; Mielnick et al., 2006). Dietary fiber has been considered as a functional ingredient in meat products (Cofrades, Serrano, Ayo, Solas, Carballo, & Jime´nez-Colmenero, 2004; Serrano, Cofrades, & Jime´nez-Colmenero, 2006). The inclusion of dietary fiber may improve texture (Cofrades et al., 2004), increase the cooking yield due to water-holding and fat binding properties and also dietary fiber may generate technological properties that improve physicochemical and sensory properties (Jime´nez-Colmenero et al., 2003).
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Dietary fiber and natural antioxidants are two dietary factors involved in health promoting. A natural product that combines high amounts of dietary fiber and phenolics antioxidants such as pehnolics acids, anthocyanidins, proanthocyanidins, catechins and other flavonoides is grape antioxidant dietary fiber (GADF) (Saura˜ i, CSIC-UCM, ES 2259258A1; Calixto, 1998, Saura-Calixto & Gon Saura-Calixto & Larrauri, CSIC, ES 2130092A1). Recently, GADF had been successfully used as an ingredient in minced fish (Sa´nchezAlonso, Jime´nez-Escrig, Saura-Calixto, & Borderı´as, 2007). The present study was designed to study the effect of grape antioxidant dietary fiber (GADF) on breast chicken hamburgers to reach two objectives: 1) To assess the effectiveness of GADF on lipid stability during refrigerated storage for increasing the shelf life of the food and 2) to incorporate dietary fiber in a meat product to enhance health-beneficial properties. Sensory qualities and acceptability by panellists were also evaluated. 2. Materials and methods 2.1. Preparation of meat and samples Six weeks old male broilers (body weight, 2.2 0.2 kg) were supplied by the Veterinarian Faculty of the Complutense University of Madrid. Chickens were fed a commercial corn–soybean diet formulated to meet the minimum National Research Council (1994) requirements for broiler chickens. All housing and handling were approved by the University Complutense of Madrid Animal Care and Ethics Committee in compliance with the Ministry of Agriculture, Fishery and Food for the Care and Use of the Animals for Scientific Purpose. Twelve birds were slaughtered and carcass was immediately trimmed for breast meat. Fresh breast meat (about 2 kg) was minced twice (4 mm plate) using a grinder (Mainica, Granollers, Spain) and it was packed on four portions to be used and analyzed on day 0 and after 3, 5, and 13 days of storage at 4 C. Red grape pomace (Vitis vinifera var. Cencibel, La Mancha, Spain) obtained from winery was processed following a patented proce˜ i, CSIC-UCM, ES 2259258A1; Sauradure (Saura-Calixto & Gon Calixto & Larrauri, CSIC, ES 2130092A1), freeze-dried, milled to a particle size less than 0.5 mm. The final product, named grape antioxidant dietary fiber (GADF), was used as a functional ingredient in the formulation of minced chicken breast meat. Hamburgers were prepared following a homemade formulation, using these ingredients: breast meat (85.4%), whole egg (6.8%), breadcrumbs (6.8%) and species (1%). The minced breast was treated with four concentrations of GADF (0.5, 1, 1.5 and 2%). Controls without GADF were used in all assays. Ingredients and GADF were blended in a bowl mixer (Hobart, Model N50, USA) during 3 min, to ensure uniform distribution of the added ingredients. Ready-meat hamburgers were packed (300 g per trial) in vacuum high oxygen barrier bags (nylon/polyethylene, 9.3 ml O2/m2/24 h at 0 C, Koch Kansas City, MO) and were stored in refrigeration at 4 C. The first day of analysis in each trial, the bag was broken and four portions were formed to be analyzed on day 0 and after 3 and 5 days of storage at 4 C. These portions were wrapped in a transparent oxygen-permeable polyvinyl chloride film (13,500 cm3/m2/day), and was stored at 4 C. Hamburgers (50 g) were formed using a conventional burgermaker. They were cooked in an electric pan previously greased with ˜ a) at olive oil (Plactronic, Selecta, J.P. Selecta, S. A. Barcelona, Espan 170 C and pressed 30 s. After 1.5 min hamburgers were turned over and left for another 1.5 min. Finally, it was cooled for 2 min, served to panelists and a portion of cooked meat hamburger was reserved for further analysis. The same procedure was followed for cooking meat hamburger after 3 and 5 days. A portion of raw meat
hamburger was stored on refrigeration and used for further analysis (days 0, 3, 5 and 13). 2.2. Chemical analysis The proximate analyses in GADF were determined using AOAC (2000) methods: protein (Method 950.48), fat (Method 969.24), and moisture (Method 925.09). Protein content was evaluated using a Nitrogen Determinator LECO FP-2000 (Leco Corporation, St Joseph, MI, USA). 2.2.1. Dietary fiber Dietary fiber (DF) in GADF, was analyzed by the AOAC (2000) enzymatic–gravimetric method (Method 991.42) modified in our ˜ as & Saura-Calixto, 1995). The sample was treated laboratory (Man with heat stable a-amylase A-3306 (Sigma Chemical CO, St Louis MO, USA), protease P-3910 (Sigma Chemical CO, St Louis MO, USA) and amyloglucosidase A-9913 (Sigma Chemical CO, St Louis MO, USA) to remove protein and starch. Remaining residues were separated by centrifugation (15 min, 25 C, 3000 g) instead of filtration to separate the soluble and insoluble fractions. The supernatants were dialysed against water to avoid losses of soluble dietary fiber (SDF), substituted ethanol precipitation of SDF. Dialysates were submitted to acid hydrolysis with 1 M sulphuric acid, and SDF was measured spectrophotometrically (Englyst & Cummings, 1988) with dinitrosalysilic acid (Panreac 162837, Barcelona, Spain). Residues from centrifugation were quantified gravimetrically. This value was insoluble dietary fiber (IDF). 2.2.2. Extraction of phenolics GADF sample was 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, 3000 g) supernatants were combined and used to determine extractable polyphenols content and free radical scavenging assay (ABTS). Extractable polyphenols were determined by the Folin–Ciocalteau procedure (Montreau, 1972) using gallic acid as standard. 2.2.3. Non-extractable polyphenols Proanthocyanidins (condensed tannins) and hydrolysable phenols were determined in the residues of the methanol–water and acetone–water extraction in GADF. The residue was treated with 5 ml/L HCl–Butanol (3 h, 100 C) (Reed, McDowell, Van Soest, & Horvarth, 1982) for proanthocyanidins hydrolysis. Proanthocyanidins were calculated from the absorbance at 550 nm using Mediterranean carob pod (Ceratonia siliqua L.), supplied by Nestle´ S.A. as standard. Hydrolysable phenols were determined by a methanol/H2SO4 90:10 (v/v) hydrolysis at 85 C for 20 h (Hartzfeld, Forkner, Hunter, & Hagerman, 2002) of the residues from of methanol–water and acetone–water extraction. Samples were centrifuged (15 min, 25 C, 3000 g) and the hydrolysable polyphenols were determined in supernatants by Folin–Ciocalteau procedure (Montreau, 1972), using gallic acid as standard. 2.3. Color measurement Hunter L* (lightness), a* (redness), and b* (yellowness) were evaluated for raw (day 0) and cooked hamburger meat in 0, 3 and 5 days. Samples were prepared as described before. Surface color measurements were determined using a Hunter Lab model D12-9 (D65/10 ) (Hunter Associates Laboratory In., Reston, VA). The chromameter was calibrated on the Hunterlab color space system using a white tile.
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2.4. Lipid stability measurements 2.4.1. Measurement of lipid oxidation. Thiobarbituric acid index (TBARS) The extent of lipid oxidation was determined by measuring the TBARS-reacting substances at days 0, 3, 5 and 13 in raw hamburgers and days 0, 3 and 5 in cooked hamburgers. Values were expressed as mg of malondialdehyde per kilogram of sample using the procedure described by Salih, Smith, Price, and Dawson (1987). Briefly, 10 g of meat was homogenized with 35 mL of 3.86% perchloric acid in an Ultra-Turrax (IKA Works Inc., Wilmington NC) at 13,800 rpm for 1 min. BHA was added before homogenization at a level of 125 mg/mg of fat. The blended was filtered through Wathman 2V filter into 50 mL Erlenmeyer flasks. The filtrate (5 mL) was mixed with 5 mL of 0.02 M thiobarbituric acid (TBA) in distilled water in capped test tubes. Tubes were incubated in boiling water for 30 min. The absorbance was determined at 531 nm against a blank containing 5 mL of distilled water and 5 mL of 0.02 M TBA solution. The antioxidant effectiveness was calculated as per cent inhibition of oxidation (% I) as described by Frankel (1998): % I ¼ ((c s)/c) 100, where c ¼ high increment of control in the experiment and s ¼ increment of sample with added GADF at the same time. High levels of % I indicate greater antioxidant effectiveness. 2.4.2. Free radical scavenging. ABTS assay The antioxidant capacity was estimated in terms of radical scavenging activity following the procedure described elsewhere (Re et al., 1999) with some modification (Pulido, Herna´ndez-Garcı´a, & Saura-Calixto, 2003). Briefly, ABTS [2,2-azinobis(3-ethilenzotiazolin)-6-sulfonate] radical cation (ABTSþ) was produced by reacting 7 mmol/L ABTS stock solution with 2.45 mmol/L potassium persulphate in the dark at room temperature for 12–16 h before use. The ABTSþ solution was diluted with methanol to an absorbance of 0.70 0.02 at 730 nm. ABTSþ solution (3.9 mL) and phenolic extract (0.1 mL) were mixed and the absorbance was read every 20 s using a Beckman DU-640 spectrophotometer. The reaction was monitored during 6 min. Inhibition of absorbance vs time was plotted and the area below the curve (0–6 min) was calculated. The antioxidant results were expressed as mmol equivalents of trolox per gram of sample (dry matter).
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The hamburgers were cooked and cut into four similar pieces and served warm (w45 C) to the panelists in individual cage. They used a structured scale to evaluate the samples from very undesirable (value 0) to very desirable (value 5) for each evaluated parameter (ISO, 1985). 2.6. Statistical analysis Results were expressed by means standard error of three or more separate determinations. Comparison of means was performed by one-way and two-way analysis of variance (ANOVA). Tukey HSD test was used to determine the differences in the mean values (P < 0.05). Data were analyzed using SPSS V.13.0 software (SPSS Institute Inc., Cary, NC). 3. Results and discussion 3.1. Characterization of grape antioxidant dietary fiber The proximal composition of the GADF might change slightly due to the vintage. Dietary fiber and phenolic compounds are the main components of the GADF (Table 1). It is worth noting that the soluble dietary fiber content of GADF is relatively high. The other majority components, phenolic components of GADF, may be associated to dietary fiber matrix as to soluble and insoluble ˜ i, & Saura-Calixto, 2007). This composicomponents (Serrano, Gon tion confers appreciable nutritional properties to the whole. Phenolic compounds represent around 23% dry matter of the sample. This value corresponds to the total extracted and nonextracted polyphenols by organic solvents. Extractable polyphenols represent only 21% of total phenolic compounds contained in the sample being the main components catechins (46.8%), benzoic acids (16%), flavonols (14%) and anthocyanidins (16.2%) (Pe´rezJime´nez et al., 2008). On the other hand, non-extractable polyphenols represent 17.5% of GADF dry matter and the major part corresponds to condensed tannins. The presence of phenolic compounds may be significant on health properties because they show antioxidant capacity (Yilmaz & Toledo, 2004), but this property may depend on the degree of polymerization (Blazso´, Ga´bor, & Rohdewald, 1997; Serrano et al., 2007). GADF exhibited relatively ˜ i & Serrano, 2005) and it may be high antioxidant activity (Gon considered as antioxidant dietary fiber (Saura-Calixto, 1998).
2.5. Sensory evaluation 3.2. Color measurement or stability 2.5.1. Preference test Control and GADF (0.5, 1, 1.5 and 2%) hamburgers were cooked, cut into pieces of uniform size and served warm (w45 C) to a fifteen non-trained panel members. Volunteers classified the samples in order of preference (from 1, like much to 4, like less) without allowing ties between samples (ISO, 1985). Results were analyzed using a Friedman repeated measures analysis of variance on ranks procedure. Statistical analysis was run using the computer SPSS V.13.0 software (SPSS Institute Inc., Cary, NC). In this test, panelists decided the preference levels of GADF. The identification codes of the samples were the following: CK(cooked)-GADF-0.5%; CK-GADF-1%; CK-GADF-1.5%; CK-GADF-2%. 2.5.2. Affective test Control and GADF (1 and 2%) hamburgers were selected previously by the panelists in preference test to run the affective test. The evaluations were made in cooked samples after 0, 3 and 5 days of storage of raw hamburger at 4 C. The panelist members (n ¼ 15) were selected in preliminary sessions and received a description of attributes and terminology used in the test. The sensory parameters for the cooked hamburgers were taste, tenderness, color and odor.
The color of chicken product is one of the main factors by which consumers judge their acceptability. It depends on various factors, including the concentration and chemical state of meat pigment, physical characteristics of the meat and the presence of non-meat ingredients (Hunt & Kropf, 1987). The addition of no chicken ingredients like GADF and the storage conditions can cause changes Table 1 Proximate composition of grape antioxidant dietary fiber (g dry matter per 100 g). Protein Fat Ash Fibera Soluble Dietary Fiber Insoluble Dietary Fiber
11.08 0.46 7.69 0.49 5.25 0.19 77.60 3.01 15.53 0.11 62.07 3.01
Polyphenols Extractable polyphenols Condensed tannins Hydrolizable tannins
4.93 0.03 14.81 0.19 2.70 0.19
a
Residual polyphenolic contents may be included in this value.
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Table 2 Color changes (Lightness L*, redness a*, yellowness b*) for raw (day 0) and cooked chicken hamburger containing added grape antioxidant dietary fiber (GADF) during 0, 3 and 5 days of storage. Storage/
Sample
L*
Day 0
Raw hamburger RW-C RW-GADF-1 RW-GADF-2
a*
b*
58.1 0.1a 44.8 0.2d 41.9 1.0e
1.7 0.1a 2.7 0.1ab 3.3 0.5ab
16.2 0.2a 9.2 0.1b 4.5 0.1d
Cooked hamburger CK-C 77.4 1.3b CK-GADF-1 75.6 1.0b CK-GADF-2 60.4 0.6a
0.2 0.1e 1.8 0.3ab 2.8 0.6ab
19.6 0.7a 22.5 0.4a 11.6 0.9c
Day 3
CK-C CK-GADF-1 CK-GADF-2
72.4 1.5c 58.9 0.8a 55.3 0.9d
3.5 0.9b 3.3 0.5b 4.8 0.6bc
22.8 0.7a 11.8 0.9cd 9.9 0.8c
Day 5
CK-C CK-GADF-1 CK-GADF-2
69.7 1.6c 57.3 1.3ad 50.8 0.5f
3.7 1.0b 4.0 0.5bc 5.4 0.6c
21.6 0.8a 12.5 1.3c 11.0 0.5c
Means in a column not sharing the same letter are significantly different (P < 0.05), values are mean SEM, n ¼ 6.
in poultry products. This fact had been observed in other similar meat products (Lau & King, 2003). Effect of GADF on color stability (Lightness L*, redness a*, yellowness b*) in cooked chicken hamburgers is shown in Table 2. Significant reduction in the lightness values, as a result of GADF addition was observed at day 0 in raw (up to 28%) and at day 5 in cooked chicken hamburger (up to 27%) in comparison to controls. This effect could be a consequence of the structural disintegration of the muscle, during the grinding because it augments the surface area exposed to oxygen, and it causes the meat to brown more readily than whole meat (Young & West, 2001). Addition of GADF also resulted in significant reduction (up to 24%) in lightness values, relative to controls in cooked chicken hamburgers after 3 and 5 days of refrigerated stored at 4 C. This effect has been attributed to the dilution of meat pigment in other meat products due to the presence of non-meat ingredients (Rocha-Garza & Zayas, 1996). However, this parameter was not different (P > 0.05) in CK-C and CK-GADF-1 hamburgers in day 0. The redness values as a result of GADF addition were higher in raw and cooked chicken hamburger (up to 2.8 times) in comparison to controls in day 0. These a* values were stabilized among storage period in hamburger added with GADF. Addition of GADF also resulted in a significant increase (2.22 times) in redness values, relative to controls, in cooked chicken hamburger after 3 and 5 days of storage. This could be due to phenolics present in GADF that
could stabilize redness among storage. Similar effect has been observed using a high dose of green tea ethanolic extract in raw patties (Jo, Son, Son, & Byun, 2003) and in beef patties (Tang et al., 2001; Tang, Kerry, Sheehan, & Morrissey, 2000). The enhancing effect of GADF is also possibly due to the red color of this product. Similar results have been reported by Carpenter, O’Grady, O’Callaghan, O’Brien, and Kerry (2007) in raw and cooked pork using grape seed extract. Significant reduction in the yellowness values in raw chicken hamburger was expected due to the GADF added. However, the b* values among days 3 and 5 were stable in cooked hamburgers added with 1 and 2% GADF. The yellowness values obtained in the cooked hamburger were similar to those reported by Mitsumoto, O’Grady, Kerry, and Buckley (2005) for chicken patties by the addition of tea catechins. Addition of GADF also resulted in significant reduction (up to 52%), relative to controls, only after 3 days of storage at 4 C. 3.3. Lipid oxidation The extent of lipid oxidation in raw chicken hamburger meat stored for 0, 3, 6, and 13 days is illustrated in Table 3. Storage period had significant influence on the development of lipid oxidation in the chicken meat resulting in an increase of TBARS values during the 13 days of storage. The lipid oxidation index was most efficient in 1% GADF added raw hamburger than 2% GADF raw hamburger. TBARS values increased significantly in raw and cooked control hamburgers. However, when GADF was added, the chicken hamburger meat resisted the lipid oxidation and showed similar values of TBARS during the storage. GADF showed a significant protective effect towards lipid oxidation. This effect may be depending on the concentration of GADF because the highest concentration of antioxidant (2% GADF) retarded the oxidation process most efficiently by maintaining TBARS values during 13 days storage. Similar values of TBARS were reported by Tang et al. (2001) for chicken breast. Our study also confirms in vitro observations that the addition of wine polyphenols to various food systems (fish lipids, frozen fish and turkey meat) inhibits lipid oxidation (Lau & King 2003; Mielnick et al., 2006). The mechanism of the protective effect on lipid oxidation may be due to the presence in GADF of a number of oligomer procyanidins, such as catechin and epicatechin (Yilmaz & Toledo, 2004). The malondialdehyde content in the CK-C and CK-GADF-1 was increased among storage in refrigeration. However, CK-GADF-2 did not show statistical differences (P > 0.05) during storage in TBARS values. This could be due to a better inhibitory effect of 2% GADF added instead of 1%.
Table 3 Effect of grape antioxidant dietary fiber (GADF) on TBARS values (mg malondialdehyde/kg meat) in raw chicken hamburger (0, 3, 5 and 13 days) and cooked chicken hamburger after 0, 3 and 5 days of refrigerated storage. Storage day
%I
0
3
5
13
Raw hamburger RW-C RW-GADF-1 RW-GADF-2
0.84 0.04aA 0.89 0.01aA 1.09 0.02aB
0.99 0.01bA 1.01 0.01bA 1.16 0.02abB
1.15 0.04cA 0.92 0.01aB 1.18 0.02bA
2.05 0.09dA 1.30 0.01cB 1.42 0.01cC
0 36.6 30.5
Cooked hamburger CK-C CK-GADF-1 CK-GADF-2
1.36 0.17aA 1.10 0.01aA 1.42 0.08aB
1.42 0.02bA 1.31 0.0abB 1.56 0.06aC
1.82 0.01cA 1.59 0.08bB 1.35 0.08aC
ndd nd nd
0 12.6 25.8
Means in a row (a–d) not sharing the same letter are significantly different (P < 0.05), values are mean SEM (n ¼ 6). Different letter within the same column (A–C) differ (P < 0.05), values are the mean SEM (n ¼ 6). % I ¼ ((c s)/c) 100, where c ¼ high increment of control in the experiment and s ¼ increment of sample with added GADF at the same time. High levels of % I indicate greater antioxidant effectiveness. nd ¼ not determined.
S.G. Sa´yago-Ayerdi et al. / LWT - Food Science and Technology 42 (2009) 971–976
The cooked hamburgers were more susceptible to lipid oxidation than raw meat because heating accelerates oxidative reactions in meat (Kingston, Monahan, Buckley, & Lynch, 1998). The membranal phospholipids, which are high in polyunsaturated fatty acids, are responsible for the initial development of oxidation in raw and cooked meat (Gray & Pearson, 1987). Cooked samples also showed TBARS index values lower in samples with GADF added, being the highest concentration of antioxidant (2% GADF) most efficient to maintain a retarded oxidation process. The rate of inhibition at 5 days of storage was 13% for the 1% GADF sample while this index was 26% for the samples with 2% added antioxidant fiber. 3.4. Scavenging effect The grape polyphenols have considerable potential as antioxidants, based on the combined actions of extractable polyphenols (anthocyanins, flavonols, flavan-3-ols and phenolic acids) and nonextractable polyphenols (polymeric proanthocyanidins and high molecular weight hydrolysable tannins), both are able to scavenge radicals which are important in preventing the development of rancidity in foods. The addition of GADF, increased significantly (P < 0.05) the radical scavenging effect of raw and cooked hamburgers (Table 4). This increment was according to the percentage of GADF added. The evolution of this parameter was different depending on the treatment. Raw meat hamburger maintained similar values during storage period, being always more elevated for added GADF samples. However, cooked hamburgers showed a light increase after third day of storage for control samples, while added GADF samples followed different evolution according to the percentage of GADF. Meat samples with 1% GADF maintained values during 13 days storage, while samples with 2% significantly decreased the radical scavenging capacity. TBARS values and radical scavenging capacity values are in accordance. Both values seem to indicate that antioxidant compounds contained in GADF are effectively used to inhibit or to retard the oxidative process in the meat.
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Table 5 Sensory evaluation test in cooked chicken hamburgers containing added grape antioxidant dietary fiber (GADF) levels. Preference test Friedman’s test
Affective test C-CK CK-GADF-1 CK-GADF-2
CK-GADF-0.5 1.9 1.1a
CK-GADF-1 3.3 1.0b
CK-GADF-1.5 2.6 1.0c
CK-GADF-2 2.58 1.2c
Flavor
Tenderness
Odor
Color
2.7 1.1a 2.6 0.8a 2.6 0.9a
3.1 0.9a 2.9 0.9a 2.7 1.0a
3.0 1.0a 2.7 0.9a 2.9 1.1a
3.35 1.2a 2.56 0.7b 2.32 0.7b
Pool of results in hamburgers cooked. Means in a row not sharing the same letter are significantly different (P < 0.05). Different letter within the same column differ (P < 0.05), values are the mean ED, n ¼ 39.
values to hamburgers prepared with 1.5 and 2.0% (P > 0.05) of GADF. Therefore, 2% was chosen for further evaluations. The affective test was passed in three times corresponding to the meat on refrigeration during 0, 3 or 5 days. The values obtained every day did not show statistical differences (P > 0.05). Results are shown in a pool expressed in Table 5. Flavor, tenderness, and odor were similar (P > 0.05) for all samples. Flavor expresses the taste experience when a condiment is taken into a mouth; tenderness shows the easiness to cut or chew the hamburger; and odor describes as the sensation that results when olfactory receptors in the nose are stimulated. The dietary fiber content in the hamburgers added with GADF might improve stability in flavor and tenderness in spite of the phenolics compounds present in the samples. The soluble dietary fiber content in GADF might supply texture, water-holding and avoid the lost of these sensorial attributes in the samples. The color was other attribute evaluated by panelist (Table 5) and by chromameter (Table 2). In both cases were detected differences in the appearance of the hamburger described in terms of a person perception of the hue and lightness. This fact was expected because GADF shows and intense color due to the presence of phenolic compounds in the sample. However, this parameter did not affect the acceptance of hamburgers by the panelists.
3.5. Sensory evaluation at hamburgers The preference test was carried out in order to choose the better level of GADF added (0.5, 1, 1.5 and 2% respectively). The statistical analysis of the test (Table 5) showed that the hamburgers prepared with 1.0, 1.5 and 2.0% added of GADF obtained the higher mark values (P < 0.05) in sensory evaluation. Panelists gave similar
Table 4 Radical scavenging capacity (ABTS method) of raw and cooked chicken hamburgers containing added grape antioxidant dietary fiber (GADF) during 0, 3 and 5 days of refrigerated storage (at 4 C)a,b. Storage day 0
3
5
Raw hamburger RW-C RW-GADF-1 RW-GADF-2
4.94 0.19aA 8.08 0.17aB 12.02 0.3aC
5.23 0.41aA 8.14 0.43aA 12.35 0.29aC
5.66 0.18aA 8.47 0.23aB 12.57 0.43aC
Cooked hamburger CK-C CK-GADF-1 CK-GADF-2
5.22 0.06aA 9.08 0.16aB 11.02 0.14aC
6.42 0.32bA 9.20 0.73aB 12.70 0.30bC
6.56 0.14bA 10.18 0.15aAB 10.36 0.12aB
Means in a row (a–c) not sharing the same letter are significantly different (P < 0.05), values are mean SEM (n ¼ 6). Different letter within the same column (A–C) differ (P < 0.05), values are the mean SEM (n ¼ 6). RW-C: control raw.
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