- Email: [email protected]
Lipid oxidation stability of omega-3- and conjugated linoleic acid-enriched sous vide chicken meat
Lipid oxidation stability of omega-3- and conjugated linoleic acid-enriched sous vide chicken meat C. Narciso-Gaytán,*1 D. Shin,† A. R. Sams,‡ J. T. Keeton,§ R. K. Miller,§ S. B. Smith,§ and M. X. Sánchez-Plata#
ABSTRACT Lipid oxidation is known to occur rather rapidly in cooked chicken meat containing relatively high amounts of polyunsaturated fatty acids. To assess the lipid oxidation stability of sous vide chicken meat enriched with n-3 and conjugated linoleic acid (CLA) fatty acids, 624 Cobb × Ross broilers were raised during a 6-wk feeding period. The birds were fed diets containing CLA (50% cis-9, trans-11 and 50% trans-10, cis-12 isomers), flaxseed oil (FSO), or menhaden fish oil (MFO), each supplemented with 42 or 200 mg/kg of vitamin E (dl-α-tocopheryl acetate). Breast or thigh meat was vacuum-packed, cooked (74°C), cooled in ice water, and stored at 4.4°C for 0, 5, 10, 15, and 30 d. The lipid oxidation development of the meat was estimated by quantification of malonaldehyde (MDA) values, using the 2-thiobarbituric acid reactive substances analysis. Fatty acid, nonheme iron, moisture, and fat analyses were performed as well. Results showed that dietary CLA induced deposition of cis-9, trans-11 and trans-10, cis-12 CLA isomers, increased the proportion
of saturated fatty acids, and decreased the proportions of monounsaturated and polyunsaturated fatty acids. Flaxseed oil induced higher deposition of C18:1, C18:2, C18:3, and C20:4 fatty acids, whereas MFO induced higher deposition of n-3 fatty acids, eicosapentaenoic acid (C20:5), and docosahexaenoic acid (C22:6; P < 0.05). Meat lipid oxidation stability was affected by the interaction of either dietary oil or vitamin E with storage day. Lower (P < 0.05) MDA values were found in the CLA treatment than in the MFO and FSO treatments. Lower (P < 0.05) MDA values were detected in meat samples from the 200 mg/kg of vitamin E than in meat samples from the 42 mg/kg of vitamin E. Nonheme iron values did not affect (P > 0.05) lipid oxidation development. In conclusion, dietary CLA, FSO, and MFO influenced the fatty acid composition of chicken muscle and the lipid oxidation stability of meat over the storage time. Supranutritional supplementation of vitamin E enhanced the lipid oxidation stability of sous vide chicken meat.
Key words: conjugated linoleic acid, n-3 fatty acid, chicken meat, lipid oxidation 2011 Poultry Science 90:473–480 doi:10.3382/ps.2010-01002
INTRODUCTION
tional value. Omega-3 fatty acids, particularly eicosapentaenoic acid (EPA; C20:5) and docosahexaenoic acid (DHA; C22:6), have shown functional properties that promote health benefits in humans, including a reduction of the risk associated with cardiovascular problems, rheumatoid arthritis, depression, inflammation, and some types of cancers (Tamura et al., 1986; Nestel 1990; Horrocks and Yeo 1999). In addition, conjugated linoleic acid (CLA) has shown to benefit human and animal health by reducing obesity and some types of cancers (Blankson et al., 2000; Krauss et al., 2000; Wang and Jones 2004). Conjugated linoleic acid iso-
Poultry products enriched with n-3 fatty acids have been developed in an attempt to meet the growing consumer demand for functional food products, that is, those that promote health benefits beyond their nutri-
©2011 Poultry Science Association Inc. Received July 9, 2010. Accepted November 12, 2010. 1 Corresponding author: [email protected]
473
Downloaded from http://ps.oxfordjournals.org/ at University of Michigan on February 10, 2015
*Colegio de Postgraduados Campus Córdoba, Km. 348 Carr. Fed. Córdoba-Veracruz, Congregación Manuel León, Amatlán de los Reyes, Ver. Apartado Postal 143 Córdoba, Ver. C.P. 94946, Mexico; †Department of Poultry Science, Texas A&M University, 101 Kleberg Building, 2472 TAMU, College Station 77843-2472; ‡College of Agriculture and Life Sciences, Texas A&M University, 109 Kleberg Building, 2402 TAMU, College Station 77843-2402; §Department of Animal Science, Texas A&M University, 133 Kleberg Building, 2471 TAMU, College Station 77843-2471; and #Inter-American Institute for Cooperation on Agriculture, 5757 Blue Lagoon Drive, Suite 200, Miami, FL 33126
474
Narciso-Gaytán et al.
The objectives of the present study were to evaluate the effect of dietary-rich sources of CLA and n-3 fatty acids and supranutritional supplementation of vitamin E on the fatty acid composition of chicken muscle and the lipid oxidation stability of meat processed as sous vide.
MATERIALS AND METHODS Broiler Production and Processing Six hundred twenty-four Cobb × Ross 1-d-old chicks were raised under simulated commercial conditions during a 6-wk period at the Poultry Science Research Center, Texas A&M University. Broilers were randomly assigned to 6 treatments with 4 replications, each with 26 broilers. The birds were fed a basal corn-soybean meal diet (Table 1) that included 2% of CLA (LutaCLA 60, BASF, Florham Park, NJ), FSO (Pizzey’s Milling Co., Gurnee, IL), or menhaden fish oil (MFO; Virginia Prime Silver, Omega Protein, Inc., Hammond, LA). Tables 2 and 3 show the fatty acid composition of the oils and diets used, respectively. The diet for each oil type was supplemented with 42 or 200 mg/kg of dlα-tocopheryl acetate (Rovimix 50% Absorbate, DSM Inc., Parsippany, NJ). Feed and water were provided ad libitum. All experimental diets were kept under refrigeration at 4°C, without light, before feeding to the broilers, to prevent the oxidation development of the lipid components of the feed.
Slaughtering and Processing At the end of the feeding period, broilers were processed under simulated commercial conditions. Feed was withdrawn for 8 h, and then the birds were transported to the pilot processing plant for slaughter. Birds were shackled and stunned with an electric knife to render them unconscious. The birds were slaughtered by cutting the jugular and carotid veins, bled for 3 min, scalded at approximately 62°C for 45 s, defeathered in a rotary drum picker, and manually eviscerated. Carcasses were prechilled for 15 min at 45°C, and then chilled for 45 min in ice water at approximately 0°C. Afterward, they were aged for 5 h at 4°C, and breast and thigh meat samples were collected for preparation of sous vide meat.
Sous Vide Meat Preparation Breast and thigh meat samples were skinned, deboned, trimmed of connective and adipose tissues, and dissected into 5 × 5 × 5 cm cubes. From each muscle type, 3 muscle pieces were vacuum-packed (model C200, Multivac Inc., Kansas City, MO) in heat-resistant boilable pouches (4 MIL Boil Vac Pouch, Ultravac Solutions, Kansas City, MO) and cooked in a water bath (model GP-400, Neslab Instruments Inc. Newington, NH)
Downloaded from http://ps.oxfordjournals.org/ at University of Michigan on February 10, 2015
mers can be naturally found in beef and dairy products (Fritsche and Fritsche, 1998; Ma et al., 1999). Their addition to food products was recently accepted by the US Food and Drug Administration (2008), which released a response letter acknowledging CLA as generally recognized as safe (GRAS), allowing it to be added to food products such as milk, yogurt, and nutritional bars; however, its addition to meat and meat products has yet to be approved. Thus, scientific research is still required to understand the effects of these fatty acids on the nutrient composition, quality, and shelf life of the meat and processed meat products. Enrichment of chicken meat with n-3 and CLA fatty acids has been successfully demonstrated in multiple studies through the dietary inclusion of primarily marine (tuna, menhaden, salmon, red fish, and algae) and plant lipid sources [flaxseed oil (FSO); Marion and Woodroof 1963; Hulan et al., 1989; Ajuyah et al., 1991; Mooney et al., 1998; López-Ferrer et al., 2001], and commercial concentrates of CLA (Szymczyk et al., 2001), respectively. However, chicken meat and meat products containing relatively high amounts of polyunsaturated fatty acids (PUFA) present a challenge for the food industry to maintain lipid oxidation stability during a prolonged storage time, particularly in aerobic conditions. Ajuyah et al. (1993) reported that an increase of n-3 fatty acids in chicken muscle resulted in accelerated development of lipid oxidation in cooked chicken meat, despite the supplementation of natural antioxidants; signs of lipid spoilage were reported at d 5 of refrigerated aerobic storage. In contrast, inclusion of CLA in meats has been shown to prevent the development of lipid oxidation. Chae et al. (2004) reported that adding CLA oil to raw and cooked ground beef patties reduced the development of lipid oxidation, extending the shelf life of the meat. Because the lipid oxidation stability of the meat can be challenged by PUFA, particularly in conventional cooking and packaging systems, alternative cooking methods, such as sous vide, should be explored to prolong the shelf life of chicken meat. Sous vide food products are thermally processed and stored in vacuum conditions, and because of their ease of handling and convenient preparation, there is a growing demand for these methods by restaurant and catering, retail, and food-service establishments (Bertelsen and Juncher, 1996; Gorris, 1996). In a previous study, Narciso-Gaytán et al. (2010) observed that sous vide chicken meat had low lipid oxidation development during refrigerated storage up to 40 d, regardless of differences in the type and amount of fatty acids present in the meat, when broilers were fed diets including animal and vegetable, palm kernel, or soybean oil. However, because these dietary fats could be considered as having a low degree of unsaturation, it is necessary to determine the lipid oxidation stability of sous vide chicken meat when it contains high amounts of PUFA, such as n-3 and CLA fatty acids.
475
SOUS VIDE CHICKEN MEAT LIPID OXIDATION STABILITY Table 1. Broilers basal experimental diets Item
Grower (4 to 5 wk)
Finisher (6 wk)
58.81 34.81 1.67 1.52 2.00 0.51 0.25 0.20 0.10 0.08 0.05 —
63.97 29.94 1.59 1.45 2.00 0.45 0.25 0.07 0.10 0.08 0.05 0.05
68.84 25.32 29.93 27.81 2.00 0.31 0.25 — 0.10 — 0.05 0.21
22.00 3,007.00 0.95 0.47 0.53 0.90 1.18 0.82 0.22
20.00 3,056.22 0.90 0.45 0.38 0.72 1.05 0.75 0.21
18.15 3,105.14 0.85 0.42 0.32 0.63 0.92 0.68 0.20
1Biophos
(Marshal Minerals, Marshal, TX). premix (Sanderson, DSM Nutritional Products Inc., Parsippany, NJ): vitamin A, 14,000,000 IU; vitamin D3, 5,000,000 IU; vitamin E, 60,000 IU; vitamin B12, 24 mg; riboflavin, 12,000 mg; niacin, 80,000 mg; d-pantothenic acid, 20,500 mg; vitamin K, 2,700 mg; folic acid, 1,800 mg; vitamin B6, 5,000 mg; thiamine, 4,000 mg; d-biotin, 150 mg. 3Coban 60 (Elanco, Indianapolis, IN). 4Mineral premix (Tyson Poultry 606 premix, Tyson Foods, Springdale, AR): Ca, 1.20%; Mn, 30.0%; Zn, 21.0%; Cu, 8,500 mg; I, 2,100 mg; Se, 500 mg; Mo, 1,670 mg/kg. 2Vitamin
up to an internal temperature of 74°C. The internal temperature of the meat was recorded with an Omega Type-T thermometer (model HH501BT, Omega Engineering Inc., Stamford, CT). After reaching the target internal temperature, the cooked meat packages were immediately chilled in ice water and later stored under refrigeration (model 2005, VWR, Cornelious, OR) at 4.4°C for 0, 5, 10, 15, and 30 d. On each sampling day, 4 packages of meat were analyzed.
Lipid Oxidation Analysis At each storage day, 2-thiobarbituric acid reactive substances analysis was conducted to estimate the development of lipid oxidation in the meat. Each meat sample was analyzed in duplicate; 30 g of meat was blended with 15 mL of 0.5% EDTA-propyl gallate (Sigma-Aldrich, St. Louis, MO) solution and 45 mL of double-distilled water at 50°C for 2 min. The meat slurry was placed in 500-mL flasks, and added with Slipicon spray, boiling chips, 4 N 2.5 mL of hydrochloric acid, and 76.5 mL of double-distilled water at 50°C. On distillation, 50 mL of malonaldehyde was collected and a 5-mL quantity was mixed with 5 mL of TBA solution in 25-mL test tubes. The solution was boiled in a water bath for 35 min and cooled for 10 min. Malonaldehyde values were quantified using a spectrophotometer (Cary 300 Bio UV-Visible Spectrophotometer, Varian, Walnut Creek, CA) set at a wavelength of 531 nm (Rhee, 1978).
Physicochemical Analysis of the Meat Fatty acid methyl esters in raw meat samples were determined using the method established by Smith et al. (2002). In cooked meat, nonheme iron values were analyzed following the procedure established by Ahn et al. (1993), in which 4 g of ground meat was placed in a 50-mL test tube, 12 mL of double-distilled water was added, and the meat was homogenized. Aliquots of 1.5 mL of the mixture were obtained, and 0.5 mL of 2% ascorbic acid (Sigma-Aldrich) solution was added. After a 5-min rest at room temperature, 1 mL of 11.3% Table 2. Fatty acid composition (% of total fat) of dietary oils1 Fatty acid
CLA
FSO
MFO
C12:0 C14:0 C16:0 C16:1 C18:0 C18:1 C18:1 cis-11 cis-9, trans-11 CLA trans-1, cis-12 CLA C18:2 C18:3 C20:4 C20:5 C22:6
— 0.05 5.36 — 4.35 22.64 0.57 30.04 30.24 0.33 0.28 0.58 — —
— 0.06 5.72 — 3.28 20.55 0.60 — — 15.12 53.03 0.14 — —
0.25 10.92 20.96 13.10 3.53 8.21 3.68 — — 1.25 0.81 0.91 7.49 9.72
1CLA = conjugated linoleic acid; FSO = flaxseed oil; MFO = menhaden fish oil. n = 5.
Downloaded from http://ps.oxfordjournals.org/ at University of Michigan on February 10, 2015
Ingredient (%) Corn Soybean meal Biophos1 Limestone Oil Salt Vitamin premix2 dl-Methionine Choline Coban 603 Mineral premix4 Sodium bicarbonate Calculated nutrient content CP (%) ME (kcal/kg) Calcium (%) Available phosphorous (%) Methionine (%) Methionine + cystine (%) Lysine (%) Threonine (%) Sodium (%)
Starter (0 to 3 wk)
476
Narciso-Gaytán et al.
trichloroacetic acid was added, followed by centrifugation (model RT6000B, Sorvall, Dupont Comp, Wilmington, DE) at 1,200 × g at 10°C for 15 min. Samples were read at 562 nm with a spectrophotometer (model DU64, Beckman Instruments Inc., Fullerton, CA). Muscle total fat and moisture analysis were performed using microwave drying and nuclear magnetic resonance through the use of a CEM Smart Track System (CEM, Matthews, NC). Meat was thoroughly ground and analyzed in duplicate, and approximately 3 to 5 g of meat was weighed.
Statistical Analysis
RESULTS The results showed no interactions between dietary oils and vitamin E level in chicken muscle fatty acid composition, or fat, moisture, and cooked yield percentages in sous vide meat. The fatty acid composition was influenced by oil type in both breast and thigh muscles (P < 0.05), but not by vitamin E level (data not shown; Table 4). Conjugated linoleic acid induced the deposition of cis-9, trans-11 and trans-10, cis-12 CLA isomers, and it significantly (P < 0.05) increased the proportion of saturated fatty acids (SFA; C16:0, and C18:0)
Table 3. Fatty acid composition (% of total fat) of experimental diets1 Fatty acid
Basal
CLA
FSO
MFO
C12:0 C14:0 C16:0 C16:1 C18:0 C18:1 C18:1 cis-11 cis-9, trans-11 CLA trans-1, cis-12 CLA C18:2 C18:3 C20:4 C20:5 C22:6
0.96 0.26 14.64 0.22 3.22 28.24 0.82 — — 47.03 2.36 0.25 — —
0.52 0.38 10.89 0.33 3.53 24.41 0.76 11.09 11.01 29.41 3.50 0.38 — —
0.56 0.52 11.56 0.48 3.08 23.82 0.84 — — 36.80 20.03 0.26 — —
1.14 3.03 15.58 3.73 3.04 20.26 1.60 — — 32.99 1.91 0.51 4.17 3.22
1CLA
= conjugated linoleic acid; FSO = flaxseed oil; MFO = menhaden fish oil. n = 6.
Downloaded from http://ps.oxfordjournals.org/ at University of Michigan on February 10, 2015
Data were analyzed independently in each muscle type (breast and thigh) using the GLM procedure of SAS (SAS Institute, 2002). A completely randomized design with a 3-factor factorial arrangement, including dietary oil (CLA, FSO, and MFO), dietary supplementation level of vitamin E (42 and 200 mg/kg of feed), and storage time (0, 5, 10, 15, and 30 d) was used, considering first-order interactions. On each storage day, 4 replications per treatment were analyzed, for a total of 24 replications, to the end of the storage time. Least squares means separation was conducted by pairwise comparison. In both breast and thigh cooked sous vide meat, correlation coefficients between malonaldehyde (MDA) and nonheme iron values were calculated.
and decreased the proportion of monounsaturated fatty acids (MUFA; C16:1, C18:1, and C18:1cis-11) and PUFA. In contrast, FSO induced higher deposition of oleic (C18:1), linoleic (C18:2), linolenic (C18:3), and arachidonic (C20:4) fatty acids, particularly in thigh muscle, whereas MFO induced a higher deposition of n-3 fatty acids, EPA, and DHA compared with the other oil treatments. In both breast and thigh cooked sous vide meat, total fat, total moisture, and cooked yield were not significantly (P > 0.05) different between treatments. In addition, dietary oil and vitamin E level did not affect these meat components (Table 5). Table 6 shows that nonheme iron values of cooked sous vide meat were significantly (P < 0.0001) affected by dietary oils, but not by vitamin E level (P > 0.05). Breast meat samples from the CLA treatment showed higher nonheme iron values than those from the FSO and MFO treatments. However, in thigh meat, both the CLA and MFO treatments showed higher values than those from the FSO treatment. No effect of vitamin E level was detected in either breast or thigh meat (P > 0.05). The lipid oxidation stability in both breast and thigh meat was affected independently by the interaction of oil type or vitamin E level with storage time. Significantly (P < 0.05) higher MDA values were found in meat samples from the MFO and FSO treatments compared with those from the CLA treatment, beginning at d 5 of storage in both breast and thigh meat. These differences remained throughout the rest of the storage time. At d 30, the maximum MDA values in breast meat from the CLA, FSO, and MFO treatments were 2.51, 3.52, and 3.53 mg/kg, respectively, and in thigh meat, these values were 2.16, 3.54, and 3.70 mg/kg, respectively (Figures 1 and 2). Regarding the vitamin E level, higher (P < 0.05) MDA values were detected in meat samples from the low dietary level of vitamin E, beginning at d 5 in breast meat and at d 10 in thigh meat. At d 30 of storage, meat samples from the low level of vitamin E had
477
SOUS VIDE CHICKEN MEAT LIPID OXIDATION STABILITY Table 4. Fatty acid composition (% of total fat) of chicken muscle affected by dietary oil Breast
type1 Thigh
CLA
MFO
FSO
Root MSE2
CLA
MFO
FSO
Root MSE
C14:0 C16:0 C16:1 C18:0 C18:1 18:1 cis-11 C18:2 cis-9, trans-11 CLA trans-10, cis-12 CLA C18:3 C20:4 C20:5 C22:6 SFA MUFA PUFA SFA:PUFA Total n-3
1.19a 31.34a 1.90b 13.06a 20.07c 1.16b 16.99 3.28 2.05 0.94b 1.17 0.56c 0.84b 44.23a 23.75c 20.12c 2.22a 2.07b
1.35a 24.67b 3.18a 9.38b 25.10b 2.31a 16.47 — — 1.81b 1.76 1.69a 3.93a 34.73b 30.55b 25.37b 1.35b 7.67a
0.54b 21.33b 3.72a 7.83c 28.45a 2.07a 17.49 — — 5.46a 1.87 1.07b 1.40b 29.38c 33.95a 27.53a 1.08c 7.80a
0.47 4.48 1.22 0.96 1.58 0.22 1.30 0.67 0.53 1.10 0.57 0.27 0.83 3.62 2.49 1.77 0.23 0.98
1.08b 29.92a 2.16c 13.76a 21.13c 1.17c 17.01b 3.36 2.08 0.99c 1.08b 0.53b 0.88b 44.76a 24.46b 20.31c 2.21a 2.40c
1.53a 24.65b 5.13a 8.27b 28.03b 2.05a 17.21b — — 1.86b 1.35b 1.68a 2.49a 34.35b 35.21a 24.59b 1.41b 6.03b
0.47c 20.11c 4.03b 7.23c 31.09a 1.82b 18.62a — — 7.31a 1.89a 0.66b 0.79b 27.72c 36.95a 29.28a 0.96c 8.76a
0.30 2.76 0.84 0.96 1.80 0.18 1.30 0.38 0.32 0.41 0.44 0.19 0.33 2.70 2.38 1.97 0.16 0.57
a–cLeast
squares means within a row with different superscripts are significantly different (P < 0.05). = conjugated linoleic acid; MFO = menhaden fish oil; FSO = flaxseed oil; SFA = saturated fatty acids (C14:0, C16:0, and C18:0); MUFA = monounsaturated fatty acids (C16:1, C18:1, and C18 cis-11); PUFA = polyunsaturated fatty acids (C18:2, C18:3, C20:4, C20:5, and C22:6); SFA:PUFA = ratio of SFA to PUFA; total n-3 = n-3 fatty acids (C18:3, C20:5, and C22:6). 2Root mean square error. 1CLA
approximately 1.25- and 1.23-fold higher MDA levels than breast and thigh meat samples, respectively, from the treatment with the high supplemented level of vitamin E (Figures 3 and 4).
DISCUSSION As expected, the fatty acid composition of chicken muscles reflected the fatty acid composition of the dietary oils. Dietary CLA induced the highest proportion of SFA and the lowest proportions of MUFA and PUFA, resulting in the highest SFA:PUFA ratio in both breast and thigh muscles. It was clear that feeding broilers CLA induced the deposition of cis-9, trans-11 and trans-10, cis-12 CLA fatty acid isomers, at approximately 3.3 and 2.1%, respectively. Du and Ahn (2002) reported
that inclusion of 2% of CLA in broiler diets induced the deposition of cis-9, trans-11 and trans-10, cis-12 fatty acids in chicken breast meat, at approximately 3.48 and 4.10%, respectively. In addition, it was reported previously that dietary CLA induced deposition of cis-9, trans-11 and trans-10, cis-12, increased SFA, and decreased MUFA and PUFA in broilers (Szymczyk et al., 2001; Badinga et al., 2003) and egg yolks (Cherian et al., 2002) when compared with other dietary oils, such as linseed oil, corn oil, or MFO. Flaxseed oil induced the lowest proportion of SFA, the lowest SFA:PUFA ratio, and the highest proportions of MUFA and PUFA. Linolenic (C18:3) acid in particular, when compared with CLA and MFO, was 5.9- and 3.0-fold higher in breast muscle and 7.4- and 3.9-fold higher in thigh muscle, respectively. Menha-
Table 5. Total fat, moisture, and cooked yield (%) of sous vide chicken meat affected by dietary oil and vitamin E level1 Breast meat Effect oil2
Dietary CLA FSO MFO P-value Vitamin E level3 42 (mg/kg) 200 (mg/kg) P-value Root MSE4 1CLA
Thigh meat
Fat
Moisture
Cooked yield
1.57 1.55 1.43 0.437
70.71 71.02 71.17 0.461
83.50 83.94 84.99 0.373
1.58 1.45 0.340 0.34
71.25 70.69 0.078 1.07
84.34 83.95 0.662 4.82
= conjugated linoleic acid; MFO = menhaden fish oil; FSO = flaxseed oil. = 8. 3n = 16. 6Root mean square error. 2n
Fat
Moisture
Cooked yield
3.63 3.70 3.25 0.235
72.80 72.28 72.35 0.100
84.55 83.94 84.99 0.387
3.38 3.67 0.780 0.78
72.49 72.46 0.891 0.72
84.81 84.17 0.308 3.32
Downloaded from http://ps.oxfordjournals.org/ at University of Michigan on February 10, 2015
Fatty acid
478
Narciso-Gaytán et al.
Figure 3. Lipid oxidation development in sous vide chicken breast meat influenced by dietary supplementation level (42 and 200 mg/kg) of vitamin E (VE) over storage time (P < 0.05). n = 16.
den fish oil induced the highest deposition of EPA and DHA. These results indicate that when including these lipid sources in broiler diets, the meat will be enhanced with n-3 fatty acids, as reported previously in other studies in which broilers were fed MFO or FSO (Marion and Woodroof 1963; Gonzalez-Esquerra and Leeson 2000; López-Ferrer et al., 2001). Previously, Du and Ahn (2002) reported that dietary CLA reduced the fat deposition in broiler carcasses. However, our results showed that dietary CLA oil had no effect on either breast or thigh muscle total fat, which suggests that CLA may reduce the adipose tissue deposition only in the abdominal cavity and not in the muscle tissue. Sirri et al. (2003) also observed no changes in total lipid content of chicken breast or drumstick meat when feeding different dietary levels of CLA, compared with feeding soybean oil. According to Pariza (2004), a reduction of body fat would be expected by dietary CLA because of its inhibitory ef-
fect on adipocyte differentiation and lipid accretion, by decreasing the activity of adipocyte lipoprotein lipase, on which the trans-10, cis-12 CLA isomer has shown the strongest physiological effects. Regarding the lipid oxidation stability of the meat, the results indicate that as the proportions of MUFA and PUFA in chicken meat increased, the susceptibility of sous vide meat to lipid oxidation also increased over the storage time. Meat samples from broilers fed MFO or FSO were more susceptible to lipid oxidation than were their counterparts from the CLA treatment. The higher susceptibility of unsaturated fatty acids to peroxidation was described previously by Dahle et al. (1962), who showed that as the amount of double bonds increased in the carbon chain of fatty acids, and so did the production of MDA and the peroxide values. The enhancement of chicken meat with unsaturated fatty acids, especially PUFA, has been shown to reduce the lipid oxidation stability of the meat drastically, in
Figure 2. Lipid oxidation development in sous vide chicken thigh meat influenced by dietary conjugated linoleic acid (CLA), flaxseed oil (FSO), and menhaden fish oil (MFO) over storage time (P < 0.05). n = 8.
Figure 4. Lipid oxidation development in sous vide chicken thigh meat influenced by dietary supplementation level (42 and 200 mg/kg) of vitamin E (VE) over storage time (P < 0.05). n = 16.
Downloaded from http://ps.oxfordjournals.org/ at University of Michigan on February 10, 2015
Figure 1. Lipid oxidation development in sous vide chicken breast meat influenced by dietary conjugated linoleic acid (CLA), flaxseed oil (FSO), and menhaden fish oil (MFO) over storage time (P < 0.05). n = 8.
SOUS VIDE CHICKEN MEAT LIPID OXIDATION STABILITY Table 6. Nonheme iron values (µg/g) of sous vide meat affected by dietary oil and vitamin E level1 Meat Effect oil2
Dietary CLA FSO MFO Dietary oil P-value Vitamin E level3 42 (mg/kg) 200 (mg/kg) Vitamin E level P-value Root MSE4
Breast
Thigh
0.28a 0.22b 0.23b 0.001
0.37a 0.26b 0.33a 0.001
0.25 0.24 0.605 0.04
0.31 0.32 0.507 0.04
particular with low supplementation of an active antioxidant in the diet (Ajuyah et al., 1993; Morrissey et al., 1998). It is important to point out that early research indicated that in aerobic conditions, faster lipid oxidation development occurs in cooked thigh meat, rather than in breast meat (Ajuyah et al., 1993), which has been attributed to the higher catalytic “free” iron activity (Kanner et al., 1988a). However, in the present study, no effect from nonheme iron was exerted on MDA values in either type of meat, which can be explained by the anaerobic condition of sous vide meat. The lipid oxidation stability of sous vide meat seems to be prolonged because of the anaerobic condition of the packaging system. Studies of canned turkey meat (Kanner et al., 1988b) and sous vide turkey rolls (Smith and Alvarez 1988) showed low MDA values during a prolonged storage time, but rapid lipid oxidation was detected soon after the meat was exposed to the environment. The results support the view that lipid oxidation in sous vide meat is not dependent on nonheme iron values (Narciso-Gaytán et al., 2010). Analysis of the correlation coefficient between MDA and nonheme iron values was not significant (P > 0.05) in breast meat and was low and negative (−0.27) in thigh meat. The process of nonheme iron release from meat components is known to be affected by cooking temperatures (Bochowski et al., 1988), a situation that did not apply in the present experiment because the meat packages were cooked in batches that included samples from all the treatments, thus ruling out a cooking effect. The high supplementation of vitamin E (200 mg/ kg) was more effective at inhibiting the development of lipid oxidation than was the commercial level used (42 mg/kg), especially in thigh meat. Thus, it could be inferred that the higher deposition of α-tocopherol in the muscle tissues, induced by the high supplemental level of vitamin E, had higher antioxidant activity in
the meat. In chicken muscle tissues, the accumulation of α-tocopherol is dependent on the amount of vitamin E supplemented in the diet and the feeding period, which directly influence the lipid oxidation stability of the meat and processed meat products (Asghar et al., 1990; Sheehy et al., 1991; Bartov and Frigg 1992; Jensen et al., 1999). Hence, higher antioxidant activity in the meat would be expected as the supplementation level is increased in the broiler diets, independent of the anaerobic condition of the sous vide meat. In conclusion, feeding broilers CLA induced deposition of CLA isomers in the muscle tissues. Both FSO and MFO induced relatively high deposition of n-3 fatty acids. Changes in the composition, proportion, and degree of unsaturation of fatty acids in the muscle influenced the lipid oxidation stability of sous vide chicken meat when dietary oils with a relatively high degree of unsaturation were used. Sous vide chicken meat enriched with CLA fatty acids showed higher lipid oxidation stability than did chicken meat enriched with n-3 fatty acids. Dietary supranutritional supplementation of vitamin E was more effective at inhibiting the development of lipid oxidation in sous vide meat than was the commercial level of vitamin E used by the poultry industry.
ACKNOWLEDGMENTS The authors thank the Texas A&M-Consejo Nacional de Ciencia y Tecnologia (CONACYT, Mexico, D.F.): Collaborative Research Grant Program for the financial support for this research. In addition, we thank Omega Protein Inc. (Hammond, LA), BASF Co. (Florham Park, NJ), Pizzey’s Milling Co. (Gurnee, IL), and DSM Inc. (Parsippany, NJ) for providing the ingredients for broiler production.
REFERENCES Ahn, D. U., F. H. Wolfe, and J. R. Sim. 1993. The effect of free and bound iron on lipid peroxidation in turkey meat. Poult. Sci. 72:209–215. Ajuyah, A. O., D. U. Ahn, R. T. Hardin, and J. S. Sim. 1993. Dietary antioxidants and storage effect chemical characteristics of ω-3 fatty acid enriched broiler chicken meats. J. Food Sci. 58:43–46. Ajuyah, A. O., K. H. Lee, R. T. Hardin, and J. S. Sim. 1991. Changes in the yield and in the fatty acid composition of whole carcass and selected meat portions of broiler chickens fed full-fat oil seeds. Poult. Sci. 70:2304–2314. Asghar, A., C. F. Lin, J. I. Gray, D. J. Buckley, A. M. Booren, and C. J. Flegal. 1990. Effects of dietary oils and α-tocopherol supplementation on membranal lipid oxidation in broiler meat. J. Food Sci. 55:46–50., 118. Badinga, L., K. T. Selberg, A. C. Dinges, C. W. Comer, and R. D. Miles. 2003. Dietary conjugated linoleic acid alters hepatic lipid content and fatty acid composition in broiler chickens. Poult. Sci. 82:111–116. Bartov, I., and M. Frigg. 1992. Effect of high concentrations of dietary vitamin E during various age periods on performance, plasma vitamin E and meat stability of broiler chicks at 7 weeks of age. Br. Poult. Sci. 33:393–402. Bertelsen, G., and D. Juncher. 1996. Oxidative stability and sensory quality of sous vide cooked products. Page 134–145 in 2nd
Downloaded from http://ps.oxfordjournals.org/ at University of Michigan on February 10, 2015
a,bLeast squares means between rows with different letters are significantly different. 1CLA = conjugated linoleic acid; MFO = menhaden fish oil; FSO = flaxseed oil. 2n = 8. 3n = 16. 4Root mean square error.
479
480
Narciso-Gaytán et al. long-chain fatty acids in chicken diets and their influence on meat quality: Fish oil. Poult. Sci. 80:741–752. Ma, D. W. L., A. A. Wierzbicki, C. J. Field, and M. T. Clandinin. 1999. Conjugated linoleic acid in Canadian dairy and beef products. J. Agric. Food Chem. 47:1956–1960. Marion, J. E., and J. G. Woodroof. 1963. The fatty acid composition of breast, thigh, and skin tissues of chicken broilers as influenced by dietary fats. Poult. Sci. 42:1202–1207. Mooney, J. W., E. M. Hirschler, A. K. Kennedy, A. R. Sams, and M. E. Van Elswyk. 1998. Lipid and flavor quality of stored breast meat from broilers fed marine algae. J. Sci. Food Agric. 78:134– 140. Morrissey, P. A., P. J. A. Sheehy, K. Galvin, J. P. Kerry, and D. J. Buckley. 1998. Lipid stability in meat and meat products. Meat Sci. 49:S73–S86. Narciso-Gaytán, C., D. Shin, A. R. Sams, C. A. Bailey, R. K. Miller, S. B. Smith, O. R. Leyva-Ovalle, and M. X. Sánchez-Plata. 2010. Soybean, palm kernel, and animal-vegetable oil and vitamin E supplementation effect on lipid oxidation stability of sous vide chicken meat. Poult. Sci. 89:721–728. Nestel, P. J. 1990. Effect of n-3 fatty acids on lipid metabolism. Annu. Rev. Nutr. 10:149–167. Pariza, M. W. 2004. Perspective on the safety and effectiveness of conjugated linoleic acid. Am. J. Clin. Nutr. 79:1132S–1136S. Rhee, K. S. 1978. Minimization of further lipid peroxidation in the distillation 2-thiobarbituric acid test of fish and meat. J. Food Sci. 43:1776–1778. SAS Institute. 2002. SAS/STAT Guide for Personal Computers. 8th ed. SAS Inst. Inc., Cary, NC. Sheehy, P. J. A., P. A. Morrissey, and A. Flynn. 1991. Influence of dietary α-tocopherol on tocopherol concentration in chick tissues. Br. Poult. Sci. 32:391–397. Sirri, F., N. Tallarico, A. Meluzzi, and A. Franchini. 2003. Fatty acid composition and productive traits of broiler fed diets containing conjugated linoleic acid. Poult. Sci. 82:1356–1361. Smith, D. M., and V. B. Alvarez. 1988. Stability of vacuum cook-inbag turkey breast rolls during refrigerated storage. J. Food Sci. 53:46–48., 61. Smith, S. B., T. S. Hively, G. M. Cortese, J. J. Han, K. Y. Chung, P. Castañeda, C. D. Gilbert, V. L. Adams, and H. J. Mersmann. 2002. Conjugated linoleic acid depresses the Δ9 desaturase index and stearoyl coenzyme A desaturase enzyme activity in porcine subcutaneous adipose tissue. J. Anim. Sci. 80:2110–2115. Szymczyk, B., P. M. Pisulewski, W. Szczurek, and P. Hanczakowski. 2001. Effects of conjugated linoleic acid on growth performance, feed conversion efficiency, and subsequent carcass quality in broiler chickens. Br. J. Nutr. 85:465–473. Tamura, Y., A. Hirai, T. Terano, M. Takenaga, H. Saitoh, K. Tahara, and S. Yoshida. 1986. Clinical and epidemiological studies of eicosapentaenoic acid (EPA) in Japan. Prog. Lipid Res. 25:461– 466. Wang, Y. W., and P. J. H. Jones. 2004. Conjugated linoleic acid and obesity control: Efficacy and mechanisms. Int. J. Obes. Relat. Metab. Disord. 28:941–955.
Downloaded from http://ps.oxfordjournals.org/ at University of Michigan on February 10, 2015
Eur. Symp. Sous Vide. Katholieke Universiteit Leuven, Leuven, Belgium. Blankson, H., J. A. Stakkestad, H. Fagertun, E. Thom, J. Wadstein, and O. Gudmundsen. 2000. Conjugated linoleic acid reduces body fat mass in overweight and obese humans. J. Nutr. 130:2943–2948. Bochowski, M. S., A. W. Mahoney, C. E. Carpenter, and D. P. Cornforth. 1988. Heating and the distribution of total and heme iron between meat and broth. J. Food Sci. 53:43–45. Chae, S. H., J. T. Keeton, and S. B. Smith. 2004. Conjugated linoleic acid reduces lipid oxidation in aerobically stored, cooked ground beef patties. J. Food Sci. 69:S306–S309. Cherian, G., M. P. Goerner, and D. U. Ahn. 2002. Dietary conjugated linoleic acid with fish oil alters yolk n-3 and trans fatty acid content and volatile compounds in raw, cooked, and irradiated eggs. Poult. Sci. 81:1571–1577. Dahle, L. K., E. G. Hill, and R. T. Holman. 1962. The thiobarbituric acid reaction and the autoxidation of polyunsaturated fatty acid methyl esters. Arch. Biochem. Biophys. 98:253–261. Du, M., and D. U. Ahn. 2002. Effect of dietary conjugated linoleic acid on the growth rate of live birds and on the abdominal fat content and quality of broiler meat. Poult. Sci. 81:428–433. US Food and Drug Administration. 2008. Agency response letter GRAS notice No. GRN 000232. CFSAN/Office of Food Additive Safety. July 11, 2008. US Food and Drug Administration, Silver Spring, MD. Fritsche, S., and J. Fritsche. 1998. Occurrence of conjugated linoleic acid isomers in beef. J. Am. Oil Chem. Soc. 75:1449–1451. Gonzalez-Esquerra, R., and S. Leeson. 2000. Effects of menhaden oil and flaxseed in broiler diets on sensory quality and lipid composition of poultry meat. Br. Poult. Sci. 41:481–488. Gorris, L. G. M. 1996. 2nd European Symposium on sous vide. Trends Food Sci. Technol. 7:303–306. Horrocks, L. A., and Y. K. Yeo. 1999. Health benefits of docosahexaenoic acid (DHA). Pharmacol. Res. 40:211–225. Hulan, H. W., R. G. Ackman, W. M. N. Ratnayake, and F. G. Proudfoot. 1989. Omega-3 fatty acid levels and general performance of commercial broilers fed practical levels of redfish meal. Poult. Sci. 68:153–162. Jensen, S. K., R. M. Engberg, and M. S. Hedemann. 1999. All-racα-tocopherol acetate is a better vitamin E source than all-rac-αtocopherol succinate for broilers. J. Nutr. 129:1355–1360. Kanner, J., B. Hazan, and L. Doll. 1988a. Catalytic “free” iron ions in muscle foods. J. Agric. Food Chem. 36:412–415. Kanner, J., I. Shegalovich, S. Harel, and B. Hazan. 1988b. Muscle lipid peroxidation dependent on oxygen and free metal ions. J. Agric. Food Chem. 36:409–412. Krauss, R. M., R. H. Eckel, B. Howard, L. J. Appel, S. R. Daniels, R. J. Deckelbaum, J. W. Erdman, P. Kris-Etherton, I. J. Goldberg, T. A. Kotchen, A. H. Lichtenstein, W. E. Mitch, R. Mullis, K. Robinson, J. Wylie-Rosett, S. St. Jeor, J. Suttie, D. L. Tribble, and T. L. Bazzarre. 2000. AHA dietary guidelines: A statement for healthcare professionals from the nutrition committee of the American Heart Association. Circulation 102:2284–2299. López-Ferrer, S., M. D. Baucells, A. C. Barroeta, and M. A. Grashorn. 2001. n-3 enrichment of chicken meat. 1. Use of very
ABSTRACT Lipid oxidation is known to occur rather rapidly in cooked chicken meat containing relatively high amounts of polyunsaturated fatty acids. To assess the lipid oxidation stability of sous vide chicken meat enriched with n-3 and conjugated linoleic acid (CLA) fatty acids, 624 Cobb × Ross broilers were raised during a 6-wk feeding period. The birds were fed diets containing CLA (50% cis-9, trans-11 and 50% trans-10, cis-12 isomers), flaxseed oil (FSO), or menhaden fish oil (MFO), each supplemented with 42 or 200 mg/kg of vitamin E (dl-α-tocopheryl acetate). Breast or thigh meat was vacuum-packed, cooked (74°C), cooled in ice water, and stored at 4.4°C for 0, 5, 10, 15, and 30 d. The lipid oxidation development of the meat was estimated by quantification of malonaldehyde (MDA) values, using the 2-thiobarbituric acid reactive substances analysis. Fatty acid, nonheme iron, moisture, and fat analyses were performed as well. Results showed that dietary CLA induced deposition of cis-9, trans-11 and trans-10, cis-12 CLA isomers, increased the proportion
of saturated fatty acids, and decreased the proportions of monounsaturated and polyunsaturated fatty acids. Flaxseed oil induced higher deposition of C18:1, C18:2, C18:3, and C20:4 fatty acids, whereas MFO induced higher deposition of n-3 fatty acids, eicosapentaenoic acid (C20:5), and docosahexaenoic acid (C22:6; P < 0.05). Meat lipid oxidation stability was affected by the interaction of either dietary oil or vitamin E with storage day. Lower (P < 0.05) MDA values were found in the CLA treatment than in the MFO and FSO treatments. Lower (P < 0.05) MDA values were detected in meat samples from the 200 mg/kg of vitamin E than in meat samples from the 42 mg/kg of vitamin E. Nonheme iron values did not affect (P > 0.05) lipid oxidation development. In conclusion, dietary CLA, FSO, and MFO influenced the fatty acid composition of chicken muscle and the lipid oxidation stability of meat over the storage time. Supranutritional supplementation of vitamin E enhanced the lipid oxidation stability of sous vide chicken meat.
Key words: conjugated linoleic acid, n-3 fatty acid, chicken meat, lipid oxidation 2011 Poultry Science 90:473–480 doi:10.3382/ps.2010-01002
INTRODUCTION
tional value. Omega-3 fatty acids, particularly eicosapentaenoic acid (EPA; C20:5) and docosahexaenoic acid (DHA; C22:6), have shown functional properties that promote health benefits in humans, including a reduction of the risk associated with cardiovascular problems, rheumatoid arthritis, depression, inflammation, and some types of cancers (Tamura et al., 1986; Nestel 1990; Horrocks and Yeo 1999). In addition, conjugated linoleic acid (CLA) has shown to benefit human and animal health by reducing obesity and some types of cancers (Blankson et al., 2000; Krauss et al., 2000; Wang and Jones 2004). Conjugated linoleic acid iso-
Poultry products enriched with n-3 fatty acids have been developed in an attempt to meet the growing consumer demand for functional food products, that is, those that promote health benefits beyond their nutri-
©2011 Poultry Science Association Inc. Received July 9, 2010. Accepted November 12, 2010. 1 Corresponding author: [email protected]
473
Downloaded from http://ps.oxfordjournals.org/ at University of Michigan on February 10, 2015
*Colegio de Postgraduados Campus Córdoba, Km. 348 Carr. Fed. Córdoba-Veracruz, Congregación Manuel León, Amatlán de los Reyes, Ver. Apartado Postal 143 Córdoba, Ver. C.P. 94946, Mexico; †Department of Poultry Science, Texas A&M University, 101 Kleberg Building, 2472 TAMU, College Station 77843-2472; ‡College of Agriculture and Life Sciences, Texas A&M University, 109 Kleberg Building, 2402 TAMU, College Station 77843-2402; §Department of Animal Science, Texas A&M University, 133 Kleberg Building, 2471 TAMU, College Station 77843-2471; and #Inter-American Institute for Cooperation on Agriculture, 5757 Blue Lagoon Drive, Suite 200, Miami, FL 33126
474
Narciso-Gaytán et al.
The objectives of the present study were to evaluate the effect of dietary-rich sources of CLA and n-3 fatty acids and supranutritional supplementation of vitamin E on the fatty acid composition of chicken muscle and the lipid oxidation stability of meat processed as sous vide.
MATERIALS AND METHODS Broiler Production and Processing Six hundred twenty-four Cobb × Ross 1-d-old chicks were raised under simulated commercial conditions during a 6-wk period at the Poultry Science Research Center, Texas A&M University. Broilers were randomly assigned to 6 treatments with 4 replications, each with 26 broilers. The birds were fed a basal corn-soybean meal diet (Table 1) that included 2% of CLA (LutaCLA 60, BASF, Florham Park, NJ), FSO (Pizzey’s Milling Co., Gurnee, IL), or menhaden fish oil (MFO; Virginia Prime Silver, Omega Protein, Inc., Hammond, LA). Tables 2 and 3 show the fatty acid composition of the oils and diets used, respectively. The diet for each oil type was supplemented with 42 or 200 mg/kg of dlα-tocopheryl acetate (Rovimix 50% Absorbate, DSM Inc., Parsippany, NJ). Feed and water were provided ad libitum. All experimental diets were kept under refrigeration at 4°C, without light, before feeding to the broilers, to prevent the oxidation development of the lipid components of the feed.
Slaughtering and Processing At the end of the feeding period, broilers were processed under simulated commercial conditions. Feed was withdrawn for 8 h, and then the birds were transported to the pilot processing plant for slaughter. Birds were shackled and stunned with an electric knife to render them unconscious. The birds were slaughtered by cutting the jugular and carotid veins, bled for 3 min, scalded at approximately 62°C for 45 s, defeathered in a rotary drum picker, and manually eviscerated. Carcasses were prechilled for 15 min at 45°C, and then chilled for 45 min in ice water at approximately 0°C. Afterward, they were aged for 5 h at 4°C, and breast and thigh meat samples were collected for preparation of sous vide meat.
Sous Vide Meat Preparation Breast and thigh meat samples were skinned, deboned, trimmed of connective and adipose tissues, and dissected into 5 × 5 × 5 cm cubes. From each muscle type, 3 muscle pieces were vacuum-packed (model C200, Multivac Inc., Kansas City, MO) in heat-resistant boilable pouches (4 MIL Boil Vac Pouch, Ultravac Solutions, Kansas City, MO) and cooked in a water bath (model GP-400, Neslab Instruments Inc. Newington, NH)
Downloaded from http://ps.oxfordjournals.org/ at University of Michigan on February 10, 2015
mers can be naturally found in beef and dairy products (Fritsche and Fritsche, 1998; Ma et al., 1999). Their addition to food products was recently accepted by the US Food and Drug Administration (2008), which released a response letter acknowledging CLA as generally recognized as safe (GRAS), allowing it to be added to food products such as milk, yogurt, and nutritional bars; however, its addition to meat and meat products has yet to be approved. Thus, scientific research is still required to understand the effects of these fatty acids on the nutrient composition, quality, and shelf life of the meat and processed meat products. Enrichment of chicken meat with n-3 and CLA fatty acids has been successfully demonstrated in multiple studies through the dietary inclusion of primarily marine (tuna, menhaden, salmon, red fish, and algae) and plant lipid sources [flaxseed oil (FSO); Marion and Woodroof 1963; Hulan et al., 1989; Ajuyah et al., 1991; Mooney et al., 1998; López-Ferrer et al., 2001], and commercial concentrates of CLA (Szymczyk et al., 2001), respectively. However, chicken meat and meat products containing relatively high amounts of polyunsaturated fatty acids (PUFA) present a challenge for the food industry to maintain lipid oxidation stability during a prolonged storage time, particularly in aerobic conditions. Ajuyah et al. (1993) reported that an increase of n-3 fatty acids in chicken muscle resulted in accelerated development of lipid oxidation in cooked chicken meat, despite the supplementation of natural antioxidants; signs of lipid spoilage were reported at d 5 of refrigerated aerobic storage. In contrast, inclusion of CLA in meats has been shown to prevent the development of lipid oxidation. Chae et al. (2004) reported that adding CLA oil to raw and cooked ground beef patties reduced the development of lipid oxidation, extending the shelf life of the meat. Because the lipid oxidation stability of the meat can be challenged by PUFA, particularly in conventional cooking and packaging systems, alternative cooking methods, such as sous vide, should be explored to prolong the shelf life of chicken meat. Sous vide food products are thermally processed and stored in vacuum conditions, and because of their ease of handling and convenient preparation, there is a growing demand for these methods by restaurant and catering, retail, and food-service establishments (Bertelsen and Juncher, 1996; Gorris, 1996). In a previous study, Narciso-Gaytán et al. (2010) observed that sous vide chicken meat had low lipid oxidation development during refrigerated storage up to 40 d, regardless of differences in the type and amount of fatty acids present in the meat, when broilers were fed diets including animal and vegetable, palm kernel, or soybean oil. However, because these dietary fats could be considered as having a low degree of unsaturation, it is necessary to determine the lipid oxidation stability of sous vide chicken meat when it contains high amounts of PUFA, such as n-3 and CLA fatty acids.
475
SOUS VIDE CHICKEN MEAT LIPID OXIDATION STABILITY Table 1. Broilers basal experimental diets Item
Grower (4 to 5 wk)
Finisher (6 wk)
58.81 34.81 1.67 1.52 2.00 0.51 0.25 0.20 0.10 0.08 0.05 —
63.97 29.94 1.59 1.45 2.00 0.45 0.25 0.07 0.10 0.08 0.05 0.05
68.84 25.32 29.93 27.81 2.00 0.31 0.25 — 0.10 — 0.05 0.21
22.00 3,007.00 0.95 0.47 0.53 0.90 1.18 0.82 0.22
20.00 3,056.22 0.90 0.45 0.38 0.72 1.05 0.75 0.21
18.15 3,105.14 0.85 0.42 0.32 0.63 0.92 0.68 0.20
1Biophos
(Marshal Minerals, Marshal, TX). premix (Sanderson, DSM Nutritional Products Inc., Parsippany, NJ): vitamin A, 14,000,000 IU; vitamin D3, 5,000,000 IU; vitamin E, 60,000 IU; vitamin B12, 24 mg; riboflavin, 12,000 mg; niacin, 80,000 mg; d-pantothenic acid, 20,500 mg; vitamin K, 2,700 mg; folic acid, 1,800 mg; vitamin B6, 5,000 mg; thiamine, 4,000 mg; d-biotin, 150 mg. 3Coban 60 (Elanco, Indianapolis, IN). 4Mineral premix (Tyson Poultry 606 premix, Tyson Foods, Springdale, AR): Ca, 1.20%; Mn, 30.0%; Zn, 21.0%; Cu, 8,500 mg; I, 2,100 mg; Se, 500 mg; Mo, 1,670 mg/kg. 2Vitamin
up to an internal temperature of 74°C. The internal temperature of the meat was recorded with an Omega Type-T thermometer (model HH501BT, Omega Engineering Inc., Stamford, CT). After reaching the target internal temperature, the cooked meat packages were immediately chilled in ice water and later stored under refrigeration (model 2005, VWR, Cornelious, OR) at 4.4°C for 0, 5, 10, 15, and 30 d. On each sampling day, 4 packages of meat were analyzed.
Lipid Oxidation Analysis At each storage day, 2-thiobarbituric acid reactive substances analysis was conducted to estimate the development of lipid oxidation in the meat. Each meat sample was analyzed in duplicate; 30 g of meat was blended with 15 mL of 0.5% EDTA-propyl gallate (Sigma-Aldrich, St. Louis, MO) solution and 45 mL of double-distilled water at 50°C for 2 min. The meat slurry was placed in 500-mL flasks, and added with Slipicon spray, boiling chips, 4 N 2.5 mL of hydrochloric acid, and 76.5 mL of double-distilled water at 50°C. On distillation, 50 mL of malonaldehyde was collected and a 5-mL quantity was mixed with 5 mL of TBA solution in 25-mL test tubes. The solution was boiled in a water bath for 35 min and cooled for 10 min. Malonaldehyde values were quantified using a spectrophotometer (Cary 300 Bio UV-Visible Spectrophotometer, Varian, Walnut Creek, CA) set at a wavelength of 531 nm (Rhee, 1978).
Physicochemical Analysis of the Meat Fatty acid methyl esters in raw meat samples were determined using the method established by Smith et al. (2002). In cooked meat, nonheme iron values were analyzed following the procedure established by Ahn et al. (1993), in which 4 g of ground meat was placed in a 50-mL test tube, 12 mL of double-distilled water was added, and the meat was homogenized. Aliquots of 1.5 mL of the mixture were obtained, and 0.5 mL of 2% ascorbic acid (Sigma-Aldrich) solution was added. After a 5-min rest at room temperature, 1 mL of 11.3% Table 2. Fatty acid composition (% of total fat) of dietary oils1 Fatty acid
CLA
FSO
MFO
C12:0 C14:0 C16:0 C16:1 C18:0 C18:1 C18:1 cis-11 cis-9, trans-11 CLA trans-1, cis-12 CLA C18:2 C18:3 C20:4 C20:5 C22:6
— 0.05 5.36 — 4.35 22.64 0.57 30.04 30.24 0.33 0.28 0.58 — —
— 0.06 5.72 — 3.28 20.55 0.60 — — 15.12 53.03 0.14 — —
0.25 10.92 20.96 13.10 3.53 8.21 3.68 — — 1.25 0.81 0.91 7.49 9.72
1CLA = conjugated linoleic acid; FSO = flaxseed oil; MFO = menhaden fish oil. n = 5.
Downloaded from http://ps.oxfordjournals.org/ at University of Michigan on February 10, 2015
Ingredient (%) Corn Soybean meal Biophos1 Limestone Oil Salt Vitamin premix2 dl-Methionine Choline Coban 603 Mineral premix4 Sodium bicarbonate Calculated nutrient content CP (%) ME (kcal/kg) Calcium (%) Available phosphorous (%) Methionine (%) Methionine + cystine (%) Lysine (%) Threonine (%) Sodium (%)
Starter (0 to 3 wk)
476
Narciso-Gaytán et al.
trichloroacetic acid was added, followed by centrifugation (model RT6000B, Sorvall, Dupont Comp, Wilmington, DE) at 1,200 × g at 10°C for 15 min. Samples were read at 562 nm with a spectrophotometer (model DU64, Beckman Instruments Inc., Fullerton, CA). Muscle total fat and moisture analysis were performed using microwave drying and nuclear magnetic resonance through the use of a CEM Smart Track System (CEM, Matthews, NC). Meat was thoroughly ground and analyzed in duplicate, and approximately 3 to 5 g of meat was weighed.
Statistical Analysis
RESULTS The results showed no interactions between dietary oils and vitamin E level in chicken muscle fatty acid composition, or fat, moisture, and cooked yield percentages in sous vide meat. The fatty acid composition was influenced by oil type in both breast and thigh muscles (P < 0.05), but not by vitamin E level (data not shown; Table 4). Conjugated linoleic acid induced the deposition of cis-9, trans-11 and trans-10, cis-12 CLA isomers, and it significantly (P < 0.05) increased the proportion of saturated fatty acids (SFA; C16:0, and C18:0)
Table 3. Fatty acid composition (% of total fat) of experimental diets1 Fatty acid
Basal
CLA
FSO
MFO
C12:0 C14:0 C16:0 C16:1 C18:0 C18:1 C18:1 cis-11 cis-9, trans-11 CLA trans-1, cis-12 CLA C18:2 C18:3 C20:4 C20:5 C22:6
0.96 0.26 14.64 0.22 3.22 28.24 0.82 — — 47.03 2.36 0.25 — —
0.52 0.38 10.89 0.33 3.53 24.41 0.76 11.09 11.01 29.41 3.50 0.38 — —
0.56 0.52 11.56 0.48 3.08 23.82 0.84 — — 36.80 20.03 0.26 — —
1.14 3.03 15.58 3.73 3.04 20.26 1.60 — — 32.99 1.91 0.51 4.17 3.22
1CLA
= conjugated linoleic acid; FSO = flaxseed oil; MFO = menhaden fish oil. n = 6.
Downloaded from http://ps.oxfordjournals.org/ at University of Michigan on February 10, 2015
Data were analyzed independently in each muscle type (breast and thigh) using the GLM procedure of SAS (SAS Institute, 2002). A completely randomized design with a 3-factor factorial arrangement, including dietary oil (CLA, FSO, and MFO), dietary supplementation level of vitamin E (42 and 200 mg/kg of feed), and storage time (0, 5, 10, 15, and 30 d) was used, considering first-order interactions. On each storage day, 4 replications per treatment were analyzed, for a total of 24 replications, to the end of the storage time. Least squares means separation was conducted by pairwise comparison. In both breast and thigh cooked sous vide meat, correlation coefficients between malonaldehyde (MDA) and nonheme iron values were calculated.
and decreased the proportion of monounsaturated fatty acids (MUFA; C16:1, C18:1, and C18:1cis-11) and PUFA. In contrast, FSO induced higher deposition of oleic (C18:1), linoleic (C18:2), linolenic (C18:3), and arachidonic (C20:4) fatty acids, particularly in thigh muscle, whereas MFO induced a higher deposition of n-3 fatty acids, EPA, and DHA compared with the other oil treatments. In both breast and thigh cooked sous vide meat, total fat, total moisture, and cooked yield were not significantly (P > 0.05) different between treatments. In addition, dietary oil and vitamin E level did not affect these meat components (Table 5). Table 6 shows that nonheme iron values of cooked sous vide meat were significantly (P < 0.0001) affected by dietary oils, but not by vitamin E level (P > 0.05). Breast meat samples from the CLA treatment showed higher nonheme iron values than those from the FSO and MFO treatments. However, in thigh meat, both the CLA and MFO treatments showed higher values than those from the FSO treatment. No effect of vitamin E level was detected in either breast or thigh meat (P > 0.05). The lipid oxidation stability in both breast and thigh meat was affected independently by the interaction of oil type or vitamin E level with storage time. Significantly (P < 0.05) higher MDA values were found in meat samples from the MFO and FSO treatments compared with those from the CLA treatment, beginning at d 5 of storage in both breast and thigh meat. These differences remained throughout the rest of the storage time. At d 30, the maximum MDA values in breast meat from the CLA, FSO, and MFO treatments were 2.51, 3.52, and 3.53 mg/kg, respectively, and in thigh meat, these values were 2.16, 3.54, and 3.70 mg/kg, respectively (Figures 1 and 2). Regarding the vitamin E level, higher (P < 0.05) MDA values were detected in meat samples from the low dietary level of vitamin E, beginning at d 5 in breast meat and at d 10 in thigh meat. At d 30 of storage, meat samples from the low level of vitamin E had
477
SOUS VIDE CHICKEN MEAT LIPID OXIDATION STABILITY Table 4. Fatty acid composition (% of total fat) of chicken muscle affected by dietary oil Breast
type1 Thigh
CLA
MFO
FSO
Root MSE2
CLA
MFO
FSO
Root MSE
C14:0 C16:0 C16:1 C18:0 C18:1 18:1 cis-11 C18:2 cis-9, trans-11 CLA trans-10, cis-12 CLA C18:3 C20:4 C20:5 C22:6 SFA MUFA PUFA SFA:PUFA Total n-3
1.19a 31.34a 1.90b 13.06a 20.07c 1.16b 16.99 3.28 2.05 0.94b 1.17 0.56c 0.84b 44.23a 23.75c 20.12c 2.22a 2.07b
1.35a 24.67b 3.18a 9.38b 25.10b 2.31a 16.47 — — 1.81b 1.76 1.69a 3.93a 34.73b 30.55b 25.37b 1.35b 7.67a
0.54b 21.33b 3.72a 7.83c 28.45a 2.07a 17.49 — — 5.46a 1.87 1.07b 1.40b 29.38c 33.95a 27.53a 1.08c 7.80a
0.47 4.48 1.22 0.96 1.58 0.22 1.30 0.67 0.53 1.10 0.57 0.27 0.83 3.62 2.49 1.77 0.23 0.98
1.08b 29.92a 2.16c 13.76a 21.13c 1.17c 17.01b 3.36 2.08 0.99c 1.08b 0.53b 0.88b 44.76a 24.46b 20.31c 2.21a 2.40c
1.53a 24.65b 5.13a 8.27b 28.03b 2.05a 17.21b — — 1.86b 1.35b 1.68a 2.49a 34.35b 35.21a 24.59b 1.41b 6.03b
0.47c 20.11c 4.03b 7.23c 31.09a 1.82b 18.62a — — 7.31a 1.89a 0.66b 0.79b 27.72c 36.95a 29.28a 0.96c 8.76a
0.30 2.76 0.84 0.96 1.80 0.18 1.30 0.38 0.32 0.41 0.44 0.19 0.33 2.70 2.38 1.97 0.16 0.57
a–cLeast
squares means within a row with different superscripts are significantly different (P < 0.05). = conjugated linoleic acid; MFO = menhaden fish oil; FSO = flaxseed oil; SFA = saturated fatty acids (C14:0, C16:0, and C18:0); MUFA = monounsaturated fatty acids (C16:1, C18:1, and C18 cis-11); PUFA = polyunsaturated fatty acids (C18:2, C18:3, C20:4, C20:5, and C22:6); SFA:PUFA = ratio of SFA to PUFA; total n-3 = n-3 fatty acids (C18:3, C20:5, and C22:6). 2Root mean square error. 1CLA
approximately 1.25- and 1.23-fold higher MDA levels than breast and thigh meat samples, respectively, from the treatment with the high supplemented level of vitamin E (Figures 3 and 4).
DISCUSSION As expected, the fatty acid composition of chicken muscles reflected the fatty acid composition of the dietary oils. Dietary CLA induced the highest proportion of SFA and the lowest proportions of MUFA and PUFA, resulting in the highest SFA:PUFA ratio in both breast and thigh muscles. It was clear that feeding broilers CLA induced the deposition of cis-9, trans-11 and trans-10, cis-12 CLA fatty acid isomers, at approximately 3.3 and 2.1%, respectively. Du and Ahn (2002) reported
that inclusion of 2% of CLA in broiler diets induced the deposition of cis-9, trans-11 and trans-10, cis-12 fatty acids in chicken breast meat, at approximately 3.48 and 4.10%, respectively. In addition, it was reported previously that dietary CLA induced deposition of cis-9, trans-11 and trans-10, cis-12, increased SFA, and decreased MUFA and PUFA in broilers (Szymczyk et al., 2001; Badinga et al., 2003) and egg yolks (Cherian et al., 2002) when compared with other dietary oils, such as linseed oil, corn oil, or MFO. Flaxseed oil induced the lowest proportion of SFA, the lowest SFA:PUFA ratio, and the highest proportions of MUFA and PUFA. Linolenic (C18:3) acid in particular, when compared with CLA and MFO, was 5.9- and 3.0-fold higher in breast muscle and 7.4- and 3.9-fold higher in thigh muscle, respectively. Menha-
Table 5. Total fat, moisture, and cooked yield (%) of sous vide chicken meat affected by dietary oil and vitamin E level1 Breast meat Effect oil2
Dietary CLA FSO MFO P-value Vitamin E level3 42 (mg/kg) 200 (mg/kg) P-value Root MSE4 1CLA
Thigh meat
Fat
Moisture
Cooked yield
1.57 1.55 1.43 0.437
70.71 71.02 71.17 0.461
83.50 83.94 84.99 0.373
1.58 1.45 0.340 0.34
71.25 70.69 0.078 1.07
84.34 83.95 0.662 4.82
= conjugated linoleic acid; MFO = menhaden fish oil; FSO = flaxseed oil. = 8. 3n = 16. 6Root mean square error. 2n
Fat
Moisture
Cooked yield
3.63 3.70 3.25 0.235
72.80 72.28 72.35 0.100
84.55 83.94 84.99 0.387
3.38 3.67 0.780 0.78
72.49 72.46 0.891 0.72
84.81 84.17 0.308 3.32
Downloaded from http://ps.oxfordjournals.org/ at University of Michigan on February 10, 2015
Fatty acid
478
Narciso-Gaytán et al.
Figure 3. Lipid oxidation development in sous vide chicken breast meat influenced by dietary supplementation level (42 and 200 mg/kg) of vitamin E (VE) over storage time (P < 0.05). n = 16.
den fish oil induced the highest deposition of EPA and DHA. These results indicate that when including these lipid sources in broiler diets, the meat will be enhanced with n-3 fatty acids, as reported previously in other studies in which broilers were fed MFO or FSO (Marion and Woodroof 1963; Gonzalez-Esquerra and Leeson 2000; López-Ferrer et al., 2001). Previously, Du and Ahn (2002) reported that dietary CLA reduced the fat deposition in broiler carcasses. However, our results showed that dietary CLA oil had no effect on either breast or thigh muscle total fat, which suggests that CLA may reduce the adipose tissue deposition only in the abdominal cavity and not in the muscle tissue. Sirri et al. (2003) also observed no changes in total lipid content of chicken breast or drumstick meat when feeding different dietary levels of CLA, compared with feeding soybean oil. According to Pariza (2004), a reduction of body fat would be expected by dietary CLA because of its inhibitory ef-
fect on adipocyte differentiation and lipid accretion, by decreasing the activity of adipocyte lipoprotein lipase, on which the trans-10, cis-12 CLA isomer has shown the strongest physiological effects. Regarding the lipid oxidation stability of the meat, the results indicate that as the proportions of MUFA and PUFA in chicken meat increased, the susceptibility of sous vide meat to lipid oxidation also increased over the storage time. Meat samples from broilers fed MFO or FSO were more susceptible to lipid oxidation than were their counterparts from the CLA treatment. The higher susceptibility of unsaturated fatty acids to peroxidation was described previously by Dahle et al. (1962), who showed that as the amount of double bonds increased in the carbon chain of fatty acids, and so did the production of MDA and the peroxide values. The enhancement of chicken meat with unsaturated fatty acids, especially PUFA, has been shown to reduce the lipid oxidation stability of the meat drastically, in
Figure 2. Lipid oxidation development in sous vide chicken thigh meat influenced by dietary conjugated linoleic acid (CLA), flaxseed oil (FSO), and menhaden fish oil (MFO) over storage time (P < 0.05). n = 8.
Figure 4. Lipid oxidation development in sous vide chicken thigh meat influenced by dietary supplementation level (42 and 200 mg/kg) of vitamin E (VE) over storage time (P < 0.05). n = 16.
Downloaded from http://ps.oxfordjournals.org/ at University of Michigan on February 10, 2015
Figure 1. Lipid oxidation development in sous vide chicken breast meat influenced by dietary conjugated linoleic acid (CLA), flaxseed oil (FSO), and menhaden fish oil (MFO) over storage time (P < 0.05). n = 8.
SOUS VIDE CHICKEN MEAT LIPID OXIDATION STABILITY Table 6. Nonheme iron values (µg/g) of sous vide meat affected by dietary oil and vitamin E level1 Meat Effect oil2
Dietary CLA FSO MFO Dietary oil P-value Vitamin E level3 42 (mg/kg) 200 (mg/kg) Vitamin E level P-value Root MSE4
Breast
Thigh
0.28a 0.22b 0.23b 0.001
0.37a 0.26b 0.33a 0.001
0.25 0.24 0.605 0.04
0.31 0.32 0.507 0.04
particular with low supplementation of an active antioxidant in the diet (Ajuyah et al., 1993; Morrissey et al., 1998). It is important to point out that early research indicated that in aerobic conditions, faster lipid oxidation development occurs in cooked thigh meat, rather than in breast meat (Ajuyah et al., 1993), which has been attributed to the higher catalytic “free” iron activity (Kanner et al., 1988a). However, in the present study, no effect from nonheme iron was exerted on MDA values in either type of meat, which can be explained by the anaerobic condition of sous vide meat. The lipid oxidation stability of sous vide meat seems to be prolonged because of the anaerobic condition of the packaging system. Studies of canned turkey meat (Kanner et al., 1988b) and sous vide turkey rolls (Smith and Alvarez 1988) showed low MDA values during a prolonged storage time, but rapid lipid oxidation was detected soon after the meat was exposed to the environment. The results support the view that lipid oxidation in sous vide meat is not dependent on nonheme iron values (Narciso-Gaytán et al., 2010). Analysis of the correlation coefficient between MDA and nonheme iron values was not significant (P > 0.05) in breast meat and was low and negative (−0.27) in thigh meat. The process of nonheme iron release from meat components is known to be affected by cooking temperatures (Bochowski et al., 1988), a situation that did not apply in the present experiment because the meat packages were cooked in batches that included samples from all the treatments, thus ruling out a cooking effect. The high supplementation of vitamin E (200 mg/ kg) was more effective at inhibiting the development of lipid oxidation than was the commercial level used (42 mg/kg), especially in thigh meat. Thus, it could be inferred that the higher deposition of α-tocopherol in the muscle tissues, induced by the high supplemental level of vitamin E, had higher antioxidant activity in
the meat. In chicken muscle tissues, the accumulation of α-tocopherol is dependent on the amount of vitamin E supplemented in the diet and the feeding period, which directly influence the lipid oxidation stability of the meat and processed meat products (Asghar et al., 1990; Sheehy et al., 1991; Bartov and Frigg 1992; Jensen et al., 1999). Hence, higher antioxidant activity in the meat would be expected as the supplementation level is increased in the broiler diets, independent of the anaerobic condition of the sous vide meat. In conclusion, feeding broilers CLA induced deposition of CLA isomers in the muscle tissues. Both FSO and MFO induced relatively high deposition of n-3 fatty acids. Changes in the composition, proportion, and degree of unsaturation of fatty acids in the muscle influenced the lipid oxidation stability of sous vide chicken meat when dietary oils with a relatively high degree of unsaturation were used. Sous vide chicken meat enriched with CLA fatty acids showed higher lipid oxidation stability than did chicken meat enriched with n-3 fatty acids. Dietary supranutritional supplementation of vitamin E was more effective at inhibiting the development of lipid oxidation in sous vide meat than was the commercial level of vitamin E used by the poultry industry.
ACKNOWLEDGMENTS The authors thank the Texas A&M-Consejo Nacional de Ciencia y Tecnologia (CONACYT, Mexico, D.F.): Collaborative Research Grant Program for the financial support for this research. In addition, we thank Omega Protein Inc. (Hammond, LA), BASF Co. (Florham Park, NJ), Pizzey’s Milling Co. (Gurnee, IL), and DSM Inc. (Parsippany, NJ) for providing the ingredients for broiler production.
REFERENCES Ahn, D. U., F. H. Wolfe, and J. R. Sim. 1993. The effect of free and bound iron on lipid peroxidation in turkey meat. Poult. Sci. 72:209–215. Ajuyah, A. O., D. U. Ahn, R. T. Hardin, and J. S. Sim. 1993. Dietary antioxidants and storage effect chemical characteristics of ω-3 fatty acid enriched broiler chicken meats. J. Food Sci. 58:43–46. Ajuyah, A. O., K. H. Lee, R. T. Hardin, and J. S. Sim. 1991. Changes in the yield and in the fatty acid composition of whole carcass and selected meat portions of broiler chickens fed full-fat oil seeds. Poult. Sci. 70:2304–2314. Asghar, A., C. F. Lin, J. I. Gray, D. J. Buckley, A. M. Booren, and C. J. Flegal. 1990. Effects of dietary oils and α-tocopherol supplementation on membranal lipid oxidation in broiler meat. J. Food Sci. 55:46–50., 118. Badinga, L., K. T. Selberg, A. C. Dinges, C. W. Comer, and R. D. Miles. 2003. Dietary conjugated linoleic acid alters hepatic lipid content and fatty acid composition in broiler chickens. Poult. Sci. 82:111–116. Bartov, I., and M. Frigg. 1992. Effect of high concentrations of dietary vitamin E during various age periods on performance, plasma vitamin E and meat stability of broiler chicks at 7 weeks of age. Br. Poult. Sci. 33:393–402. Bertelsen, G., and D. Juncher. 1996. Oxidative stability and sensory quality of sous vide cooked products. Page 134–145 in 2nd
Downloaded from http://ps.oxfordjournals.org/ at University of Michigan on February 10, 2015
a,bLeast squares means between rows with different letters are significantly different. 1CLA = conjugated linoleic acid; MFO = menhaden fish oil; FSO = flaxseed oil. 2n = 8. 3n = 16. 4Root mean square error.
479
480
Narciso-Gaytán et al. long-chain fatty acids in chicken diets and their influence on meat quality: Fish oil. Poult. Sci. 80:741–752. Ma, D. W. L., A. A. Wierzbicki, C. J. Field, and M. T. Clandinin. 1999. Conjugated linoleic acid in Canadian dairy and beef products. J. Agric. Food Chem. 47:1956–1960. Marion, J. E., and J. G. Woodroof. 1963. The fatty acid composition of breast, thigh, and skin tissues of chicken broilers as influenced by dietary fats. Poult. Sci. 42:1202–1207. Mooney, J. W., E. M. Hirschler, A. K. Kennedy, A. R. Sams, and M. E. Van Elswyk. 1998. Lipid and flavor quality of stored breast meat from broilers fed marine algae. J. Sci. Food Agric. 78:134– 140. Morrissey, P. A., P. J. A. Sheehy, K. Galvin, J. P. Kerry, and D. J. Buckley. 1998. Lipid stability in meat and meat products. Meat Sci. 49:S73–S86. Narciso-Gaytán, C., D. Shin, A. R. Sams, C. A. Bailey, R. K. Miller, S. B. Smith, O. R. Leyva-Ovalle, and M. X. Sánchez-Plata. 2010. Soybean, palm kernel, and animal-vegetable oil and vitamin E supplementation effect on lipid oxidation stability of sous vide chicken meat. Poult. Sci. 89:721–728. Nestel, P. J. 1990. Effect of n-3 fatty acids on lipid metabolism. Annu. Rev. Nutr. 10:149–167. Pariza, M. W. 2004. Perspective on the safety and effectiveness of conjugated linoleic acid. Am. J. Clin. Nutr. 79:1132S–1136S. Rhee, K. S. 1978. Minimization of further lipid peroxidation in the distillation 2-thiobarbituric acid test of fish and meat. J. Food Sci. 43:1776–1778. SAS Institute. 2002. SAS/STAT Guide for Personal Computers. 8th ed. SAS Inst. Inc., Cary, NC. Sheehy, P. J. A., P. A. Morrissey, and A. Flynn. 1991. Influence of dietary α-tocopherol on tocopherol concentration in chick tissues. Br. Poult. Sci. 32:391–397. Sirri, F., N. Tallarico, A. Meluzzi, and A. Franchini. 2003. Fatty acid composition and productive traits of broiler fed diets containing conjugated linoleic acid. Poult. Sci. 82:1356–1361. Smith, D. M., and V. B. Alvarez. 1988. Stability of vacuum cook-inbag turkey breast rolls during refrigerated storage. J. Food Sci. 53:46–48., 61. Smith, S. B., T. S. Hively, G. M. Cortese, J. J. Han, K. Y. Chung, P. Castañeda, C. D. Gilbert, V. L. Adams, and H. J. Mersmann. 2002. Conjugated linoleic acid depresses the Δ9 desaturase index and stearoyl coenzyme A desaturase enzyme activity in porcine subcutaneous adipose tissue. J. Anim. Sci. 80:2110–2115. Szymczyk, B., P. M. Pisulewski, W. Szczurek, and P. Hanczakowski. 2001. Effects of conjugated linoleic acid on growth performance, feed conversion efficiency, and subsequent carcass quality in broiler chickens. Br. J. Nutr. 85:465–473. Tamura, Y., A. Hirai, T. Terano, M. Takenaga, H. Saitoh, K. Tahara, and S. Yoshida. 1986. Clinical and epidemiological studies of eicosapentaenoic acid (EPA) in Japan. Prog. Lipid Res. 25:461– 466. Wang, Y. W., and P. J. H. Jones. 2004. Conjugated linoleic acid and obesity control: Efficacy and mechanisms. Int. J. Obes. Relat. Metab. Disord. 28:941–955.
Downloaded from http://ps.oxfordjournals.org/ at University of Michigan on February 10, 2015
Eur. Symp. Sous Vide. Katholieke Universiteit Leuven, Leuven, Belgium. Blankson, H., J. A. Stakkestad, H. Fagertun, E. Thom, J. Wadstein, and O. Gudmundsen. 2000. Conjugated linoleic acid reduces body fat mass in overweight and obese humans. J. Nutr. 130:2943–2948. Bochowski, M. S., A. W. Mahoney, C. E. Carpenter, and D. P. Cornforth. 1988. Heating and the distribution of total and heme iron between meat and broth. J. Food Sci. 53:43–45. Chae, S. H., J. T. Keeton, and S. B. Smith. 2004. Conjugated linoleic acid reduces lipid oxidation in aerobically stored, cooked ground beef patties. J. Food Sci. 69:S306–S309. Cherian, G., M. P. Goerner, and D. U. Ahn. 2002. Dietary conjugated linoleic acid with fish oil alters yolk n-3 and trans fatty acid content and volatile compounds in raw, cooked, and irradiated eggs. Poult. Sci. 81:1571–1577. Dahle, L. K., E. G. Hill, and R. T. Holman. 1962. The thiobarbituric acid reaction and the autoxidation of polyunsaturated fatty acid methyl esters. Arch. Biochem. Biophys. 98:253–261. Du, M., and D. U. Ahn. 2002. Effect of dietary conjugated linoleic acid on the growth rate of live birds and on the abdominal fat content and quality of broiler meat. Poult. Sci. 81:428–433. US Food and Drug Administration. 2008. Agency response letter GRAS notice No. GRN 000232. CFSAN/Office of Food Additive Safety. July 11, 2008. US Food and Drug Administration, Silver Spring, MD. Fritsche, S., and J. Fritsche. 1998. Occurrence of conjugated linoleic acid isomers in beef. J. Am. Oil Chem. Soc. 75:1449–1451. Gonzalez-Esquerra, R., and S. Leeson. 2000. Effects of menhaden oil and flaxseed in broiler diets on sensory quality and lipid composition of poultry meat. Br. Poult. Sci. 41:481–488. Gorris, L. G. M. 1996. 2nd European Symposium on sous vide. Trends Food Sci. Technol. 7:303–306. Horrocks, L. A., and Y. K. Yeo. 1999. Health benefits of docosahexaenoic acid (DHA). Pharmacol. Res. 40:211–225. Hulan, H. W., R. G. Ackman, W. M. N. Ratnayake, and F. G. Proudfoot. 1989. Omega-3 fatty acid levels and general performance of commercial broilers fed practical levels of redfish meal. Poult. Sci. 68:153–162. Jensen, S. K., R. M. Engberg, and M. S. Hedemann. 1999. All-racα-tocopherol acetate is a better vitamin E source than all-rac-αtocopherol succinate for broilers. J. Nutr. 129:1355–1360. Kanner, J., B. Hazan, and L. Doll. 1988a. Catalytic “free” iron ions in muscle foods. J. Agric. Food Chem. 36:412–415. Kanner, J., I. Shegalovich, S. Harel, and B. Hazan. 1988b. Muscle lipid peroxidation dependent on oxygen and free metal ions. J. Agric. Food Chem. 36:409–412. Krauss, R. M., R. H. Eckel, B. Howard, L. J. Appel, S. R. Daniels, R. J. Deckelbaum, J. W. Erdman, P. Kris-Etherton, I. J. Goldberg, T. A. Kotchen, A. H. Lichtenstein, W. E. Mitch, R. Mullis, K. Robinson, J. Wylie-Rosett, S. St. Jeor, J. Suttie, D. L. Tribble, and T. L. Bazzarre. 2000. AHA dietary guidelines: A statement for healthcare professionals from the nutrition committee of the American Heart Association. Circulation 102:2284–2299. López-Ferrer, S., M. D. Baucells, A. C. Barroeta, and M. A. Grashorn. 2001. n-3 enrichment of chicken meat. 1. Use of very