Supplementation with curcuminoids and tuna oil influenced skin yellowness, carcass composition, oxidation status, and meat fatty acids of slow-growing chickens

Supplementation with curcuminoids and tuna oil influenced skin yellowness, carcass composition,... Abstract The present study aimed to determine the effects of dietary curcuminoids combined with tuna oil on the growth performance, meat quality, thiobarbituric acid reactive substances (TBARS) values in the plasma and raw meat, and fatty acid profile of chicken meat. A total of 480 21-day-old mixed-sex slow-growing chickens was assigned to a completely randomized design model with 6 treatments and 4 replicates (pens) per treatment. The basal diet based on corn-soybean and 4% tuna oil was used as the negative control. The experimental diets comprised the basal diet supplemented with curcumin removed turmeric oleoresin to provide 20, 40, 60, or 80 mg/kg curcuminoids (CUR-20, CUR-40, CUR-60, and CUR-80, respectively) or dl-α-tocopheryl acetate at 200 ppm as the positive control (E-200). Finally, the vacuum-packed carcasses were stored frozen at −20°C for 3 mo to examine the effect of curcuminoids on changes in the TBARS values and fatty acid composition of the breast and thigh meat. Increasing the levels of curcuminoids tended to improve the feed conversion ratio (linear, P = 0.065) and significantly increased the proportion of breast fillet (linear, P = 0.037) and the yellowness of the skin of both the breast (linear, P = 0.016) and the thigh (linear, P = 0.023). The curcuminoids exhibited antioxidant properties, but their effect was not dose dependent. The CUR-20 and CUR-40 treatments increased the linoleic acid content but decreased the C22:6n-3 (DHA) content of the breast meat. The CUR-60 treatment inhibited oxidation (measured by TBARS) in the chicken meat similarly to dl-α-tocopheryl acetate but had no effect on the proportion of DHA in the breast or thigh meat. Auto-oxidation occurred in the breast meat but not in the thigh meat during the 3 mo of frozen storage. The present study showed that a suitable level of curcuminoids in the diet of slow-growing chickens was 60 mg/kg. INTRODUCTION Meat enriched with n-3 polyunsaturated fatty acids (PUFA) makes it more susceptible to lipid oxidation (Cortinas et al., 2004), which causes deterioration in the flavor, color, texture, and nutritive value of the meat and the production of toxic compounds (Kanner, 1994). Therefore, antioxidants are used in poultry feed to limit the rate of oxidation in the bird itself, and in the subsequent poultry products (Leeson, 2012). Antioxidants from natural sources are usually considered “generally recognized as safe” (GRAS) and so can be suitable alternatives to synthetic antioxidants. The antioxidant properties of curcumin and its derivatives have been studied extensively (Masuda et al., 1999; Barclay et al., 2000; Fujisawa et al., 2004). Curcumin can help to stabilize free radicals (Barzegar and Moosavi-Movahedi, 2011) and increase the activities of antioxidant enzymes (Aggarwal, 2010). Its derivatives, demethoxycurcumin and bisdemethoxycurcumin, also have antioxidant effects (Chattopadhyay et al., 2004). Therefore, it is hypothesized that curcuminoids could prevent oxidation in meat enriched with n-3 PUFA. Dietary turmeric powder in broiler diets has been shown to decrease the content of triglycerides and saturated fatty acids (SFA) in thigh meat (Daneshyar et al., 2011). Combining with curcuminoids and long-chain n-3 PUFA might have synergetic effects and enhance the accumulation of C22:6n-3 (DHA) in chicken meat. Therefore, it can be hypothesized that a combination of curcuminoids and tuna oil, rich in DHA, can protect chicken meat from lipid oxidation and influence its fatty acid (FA) profile. To the best of our knowledge, there have been no studies on the effect of supplementing the diet of slow-growing chickens with different levels of curcuminoids from curcumin removed turmeric oleoresin combined with tuna oil. Such a study could be a model for types of slow-growing chickens in various countries to produce value-added chicken meat with high n-3 PUFA, and so improve the competitiveness of small- and medium-sized farms. Therefore, the present study aims to determine the effects of dietary curcuminoids combined with tuna oil on the growth performance, carcass yield, skin color, and drip loss of chicken meat, the levels of thiobarbituric acid reactive substances (TBARS) in the plasma and raw chicken meat, and the FA profile of chicken meat. It also aims to evaluate the oxidative inhibition property of curcuminoids on TBARS values and the FA composition of meat during 3 mo of frozen storage at −20°C. MATERIALS AND METHODS Birds, Experimental Design, and Diets All procedures used in the present study were approved by the Ethics Committee on Animal Use of the Suranaree University of Technology (SUT). The study used a type of Thai indigenous crossbred chicken, the “Korat meat chicken” (male Lueng Hang Khao and female SUT line). Four-hundred-eighty one-day-old mixed-sex chicks were housed and cared for following the SUT farm guidelines. The chicks were fed a corn-soybean meal based diet (21% CP and 3,100 kcal ME/kg) from d 1 to 21. On d 21, the chicks, with an average BW of 289.05 ± 6.66 g, were randomly allotted to 6 experimental diets with 4 replications of 20 birds each in a completely randomized design. The study lasted for 63 d, from d 22 to 84. The chicks were fed ad libitum throughout the experimental period. For all treatments, the birds were reared in floor pens (8 birds/m2) in an open-sided house. The basal ration (Table 1), containing 2% crude rice bran oil (RBO; Thai Ruam Jai Korat Co. Ltd., Nakhon Ratchasima, Thailand) and 4% tuna oil (TO; feed grade; T. C. Union Agrotech Co. Ltd., Bangkok, Thailand), was used as the negative control diet. The positive control diet (E-200) was the basal ration supplemented with dl-α-tocopheryl acetate [Zagro (Thailand) Co. Ltd., Pathum Thani, Thailand] at 200 mg/kg. The other treatment diets, CUR-20, CUR-40, CUR-60, and CUR-80, comprised the basal ration with added curcumin removed turmeric oleoresin (Government Pharmaceutical Organization, Bangkok, Thailand) to provide diets with 20, 40, 60, or 80 mg/kg curcuminoids, respectively. The total curcuminoids content of the curcumin removed turmeric oleoresin was 21.6 ± 0.62% by weight. Table 1. Ingredients and nutrient composition of the basal diets (as-fed basis). Items  Grower   Finisher    (d 22 to 42)  (d 43 to 84)   Soybean meal (44% CP)   33.55   26.55   Corn (8% CP)   50.36   51.50   De-oil rice bran   6.11   12.48   Tuna oil   4.00   4.00   Rice bran oil   2.00   2.00   DL-Methionine   0.25   0.19   L-Lysine   0.13   0.10   L-Threonine   0.10   0.06   Salt   0.35   0.28   CaCO3   1.57   1.42   Monocalcium phosphate (21% P)   1.08   0.92   Premix1   0.50   0.50  Calculated nutrients level (% unless stated otherwise)   ME (kcal/kg)   3100   3100   CP   19.0   17.0   Digestible lysine   1.00   0.85   Digestible methionine   0.51   0.43   Digestible Met + Cys   0.76   0.65   Digestible threonine   0.69   0.58   Calcium   0.90   0.80   Available phosphorus   0.35   0.30  Analyzed nutrient level (%)   Total lipid2 (%)   7.30   7.74  Fatty acid profile (% of total fatty acid)   Saturated fatty acids   31.98   30.33   Monounsaturated fatty acids   32.93   32.56   Polyunsaturated fatty acids   35.09   37.11   n-6   26.58   26.89   n-3   8.51   10.22   n-6/n-3   3.12   2.63  Items  Grower   Finisher    (d 22 to 42)  (d 43 to 84)   Soybean meal (44% CP)   33.55   26.55   Corn (8% CP)   50.36   51.50   De-oil rice bran   6.11   12.48   Tuna oil   4.00   4.00   Rice bran oil   2.00   2.00   DL-Methionine   0.25   0.19   L-Lysine   0.13   0.10   L-Threonine   0.10   0.06   Salt   0.35   0.28   CaCO3   1.57   1.42   Monocalcium phosphate (21% P)   1.08   0.92   Premix1   0.50   0.50  Calculated nutrients level (% unless stated otherwise)   ME (kcal/kg)   3100   3100   CP   19.0   17.0   Digestible lysine   1.00   0.85   Digestible methionine   0.51   0.43   Digestible Met + Cys   0.76   0.65   Digestible threonine   0.69   0.58   Calcium   0.90   0.80   Available phosphorus   0.35   0.30  Analyzed nutrient level (%)   Total lipid2 (%)   7.30   7.74  Fatty acid profile (% of total fatty acid)   Saturated fatty acids   31.98   30.33   Monounsaturated fatty acids   32.93   32.56   Polyunsaturated fatty acids   35.09   37.11   n-6   26.58   26.89   n-3   8.51   10.22   n-6/n-3   3.12   2.63  1Premix (0.5%) provided the following per kilogram of diet: 15,000 IU of vitamin A; 3000 IU of vitamin D3; 25 IU of vitamin E; 5 mg of vitamin K3; 2 mg of vitamin B1; 7 mg of vitamin B2; 4 mg of vitamin B6; 25 μg of vitamin B12; 11.04 mg of pantothenic acid; 35 mg of nicotinic acid; 1 mg of folic acid; 15 μg of biotin; 250 mg of choline chloride; 1.6 mg of Cu; 60 mg of Mn; 45 mg of Zn; 80 mg of Fe; 0.4 mg of I; 0.15 mg of Se. 2Extracted by chloroform: methanol (2:1 vol/vol). View Large Sampling and Storage Conditions On d 84, chickens whose weight was within 10% of the mean of the experimental unit were transported to the university slaughterhouse, where they were stunned using electricity, bled, scalded, de-feathered by machine, then manually eviscerated. The carcasses were washed with clean water, weighed, then cooled in a chill room (4°C, 24 h) before cutting into portions. The carcass composition of 48 birds (one male and one female per experimental unit) was measured. After chilling, samples of breast and thigh meat were used to evaluate skin color and drip loss. A total of 144 birds was harvested (3 males and 3 females per pen), then the whole carcasses were vacuum-packed and chilled for 24 h at 4°C, followed by freezing at −20°C and 15, 60, or 90 d of frozen storage. Before analysis, the carcasses were thawed in ice-slurry, followed by manually separating the breast and thigh meat (without skin). The chilled breast and thigh meat were chopped then blended individually immediately after separation. The individually minced meat samples were used to determine the TBARS levels and FA composition. Measurements and Chemical Analysis Growth Performance and Carcass Composition The BW and feed intake per pen were monitored each wk to allow the ADG, ADFI, and feed conversion ratio (FCR) values to be calculated. The occurrence of mortality also was recorded. The abdominal fat was considered as the fat extending within the ischium, surrounding the cloaca, and adjacent to the abdominal muscles. The dressed weight and weight of abdominal fat were then calculated as a proportion of the live BW of the chicken. The weight of the breast fillet, thigh, and drumstick were expressed as a percentage of the chilled carcass weight. Skin Color Measurement The skin color was measured using a Hunter Lab ColorQuest XE spectrophotometer with QC Software (Reston, VA) calibrated against black and white reference tiles. The L* (lightness), a* (redness), and b* (yellowness) values were obtained by an illuminant/observer D65/10°. The measurements were made through the transparent packaging material. Three random readings were taken from the sample surface then averaged for statistical analysis. Drip Loss of Meat. Pieces of breast and thigh muscles from the same location were cut to a shape of 1.5 × 3.0 × 0.5 cm. The samples were suspended inside a chilled storage room at 4°C for 24 h using airtight containers. The drip loss was expressed as a percentage of the initial weight. Plasma TBARS Measurement Blood samples were collected from 8 chickens per treatment (one male and one female per pen) into EDTA-treated tubes, then gently shaken and kept and handled on wet ice. The plasma was separated by centrifuging the blood samples at 1,000 × g for 10 min at 4°C, then transferred to 1.5-mL microcentrifuge tubes and stored at −80°C. The TBARS values of the EDTA-treated plasma were measured using the modified method of Grotto et al. (2007). A standard curve for 1,1,3,3-tetramethoxypropane (Sigma-Aldrich Pte Ltd., Singapore) was used, and the concentration was expressed as nmol MDA/mL solution. The TBARS values were then determined using a Bio-Rad Benchmark Plus Microplate Reader (Bio-Rad Laboratories Inc., Hercules, CA). Meat TBARS Measurement The TBARS values of duplicate 5-g samples of the raw chicken meat were measured following the protocol of Leick et al. (2010). The samples, blanks, and standards were read at 530 nm using a Bio-Rad Benchmark Plus Microplate Reader. Meat Fatty Acid Profile The lipids were extracted from approximately 5 g of each muscle sample using 90 mL of chloroform: methanol (2:1, vol/vol) (Folch et al., 1957). After between 20 and 25 mg of the extracted fat had been methylated (Metcalfe et al., 1966), the FA methyl esters were analyzed using gas chromatography (Hewlett-Packard 7890A; Agilent Technologies, Santa Clara, CA) using a capillary column (SP 2560, Supelco Inc., Bellefonte, PA, 100 m × 0.25 mm i.d., 0.20-μm film thickness) and a flame ionization detector. The carrier gas was helium at a flow rate of 0.95 mL/min. The temperatures of the injector and detector were 260°C. The initial column temperature was 70°C, which was then raised to 175°C at a rate of 13°C/min, then finally to 240°C at a rate of 4°C/min. Statistical Analysis The mean values from each pen were used as the experimental unit for all analyses. Analysis of variance was performed using the GLM procedure of SAS University Edition (SAS Institute Inc., Cary, NC). The data from the FA profiles and the TBARS contents of the chicken meat during storage were analyzed by the PROC MIXED and REPEATED procedures in SAS. Orthogonal polynomial contrasts were used to test the linear and quadratic effects of increasing the levels of curcuminoids (0, 20, 40, 60, and 80 mg/kg) in the diet. The differences between the means of the curcuminoids-treated and control groups were tested by orthogonal contrast, while Dunnett's test was used to compare the effects of each curcuminoids level with the positive controls. Overall differences between treatment means were considered to be significant at P ≤ 0.05, with a tendency toward significance being declared at 0.05 < P ≤ 0.1. Data were expressed as the mean ± SEM, representing the pooled SEM for the model. RESULTS AND DISCUSSION Growth Performance and Carcass Yield The mortality of chickens observed in the negative control, CUR-60, and CUR-80 treatments were 2.50, 3.75, and 2.50%, respectively. The dietary treatments had no effect on the final BW or ADG of the chickens compared with the control treatments (Table 2). Increasing the level of curcuminoids tended to improve the overall FCR linearly (P = 0.065 by orthogonal polynomial contrast). Table 2. Growth performance of slow-growing chickens fed experimental diets.1 Treatment2  BW d 21 (kg/b)  BW d 84 (kg/b)  ADG (g/b/d)  ADFI (g/b/d)  FCR  Control  0.27  1.79  24.13  70.99  2.94  CUR-20  0.27  1.75  23.48  68.26  2.91  CUR-40  0.28  1.80  24.23  70.91  2.93  CUR-60  0.27  1.79  24.11  69.37  2.88  CUR-80  0.27  1.77  23.71  67.24  2.84  E-200  0.27  1.78  23.89  68.12  2.85  SEM  0.01  0.05  0.84  2.11  0.08  P-value  0.889  0.781  0.793  0.103  0.307  Contrast3 for the effect of different levels of curcuminoids  Linear  0.651  0.840  0.880  0.091  0.065  Quadratic  0.582  0.774  0.820  0.485  0.591  Treatment2  BW d 21 (kg/b)  BW d 84 (kg/b)  ADG (g/b/d)  ADFI (g/b/d)  FCR  Control  0.27  1.79  24.13  70.99  2.94  CUR-20  0.27  1.75  23.48  68.26  2.91  CUR-40  0.28  1.80  24.23  70.91  2.93  CUR-60  0.27  1.79  24.11  69.37  2.88  CUR-80  0.27  1.77  23.71  67.24  2.84  E-200  0.27  1.78  23.89  68.12  2.85  SEM  0.01  0.05  0.84  2.11  0.08  P-value  0.889  0.781  0.793  0.103  0.307  Contrast3 for the effect of different levels of curcuminoids  Linear  0.651  0.840  0.880  0.091  0.065  Quadratic  0.582  0.774  0.820  0.485  0.591  1Each mean of growth performance represents values from 4 replicates (20 birds/replicate). 2Treatments consisted of basal diet without antioxidant supplement (Control); basal diet added 200 ppm alpha-tocopherol acetate (E-200); basal diet added turmeric oleoresin to provide 20 ppm (CUR-20), 40 ppm (CUR-40), 60 ppm (CUR-60), and 80 ppm (CUR-80) curcuminoids. 3 3P-values were obtained by orthogonal polynomial contrasts to test the effect of different levels of curcuminoids (0, 20, 40, 60, or 80 ppm), excluding positive control (E-200). View Large The growth performance in the present study was in line with that reported elsewhere (Emadi and Kermanshahi, 2006; Mehala and Moorthy, 2008; Rahmatnejad et al., 2009). The tendency of improving the FCR in the present study agreed with Rajput et al. (2013b) who demonstrated that supplementing the diet with 200 mg/kg pure curcumin improved the feed efficiency of broiler chickens. The dressing percentage was not significantly affected by the different diet treatments (Table 3) agreeing with the findings of Abou-Elkhair et al. (2014). The present study showed a linear effect (P = 0.039; by polynomial contrast) of the different levels of curcuminoids in the diet on the amount of abdominal fat. Nouzarian et al. (2011) supplemented the diet of broiler chickens with turmeric powder (38.28 mg/kg curcumin content) and found a statistically significant decrease in the amount of abdominal fat while Rajput et al. (2013a) using 150 mg/kg pure curcumin in the diet of broiler chickens showed no similar effect. These inconsistent results may have been caused by the different forms of the supplements, and the amount of abdominal fat might have been influenced by the turmeric oils or by the synergetic effects of the oil and curcuminoids rather than by the pure curcumin itself, as reported by Honda et al. (2006). The percentage of breast fillet increased linearly (P = 0.037) with increasing levels of curcuminoids. Such an improvement partly agreed with the findings of Wang et al. (2015) who found that dietary supplementation with turmeric rhizome extract at 300 mg/kg increased the breast-to-carcass weight ratio of broilers. Table 3. Carcass composition of slow-growing chickens fed experimental diets.1 Treatment2  Dressing (%)  Breast fillet4 (%)  Thigh4 (%)  Drumstick4 (%)  Abdominal fat (%)  Control  68.61  16.09  17.43  16.28  0.41  CUR-20  68.28  16.38  17.05  16.18  0.75  CUR-40  67.73  17.09  17.61  15.86  0.66  CUR-60  69.35  17.49  17.42  15.59  0.87  CUR-80  68.17  16.79  17.42  15.74  0.88  E-200  68.19  16.82  16.76  16.01  0.72  SEM  1.19  0.69  0.71  0.56  0.30  P-value  0.535  0.694  0.577  0.513  0.312  Contrast3 for the effect of different levels of curcuminoids  Linear  0.928  0.037  0.776  0.066  0.039  Quadratic  0.846  0.100  0.985  0.579  0.525  Treatment2  Dressing (%)  Breast fillet4 (%)  Thigh4 (%)  Drumstick4 (%)  Abdominal fat (%)  Control  68.61  16.09  17.43  16.28  0.41  CUR-20  68.28  16.38  17.05  16.18  0.75  CUR-40  67.73  17.09  17.61  15.86  0.66  CUR-60  69.35  17.49  17.42  15.59  0.87  CUR-80  68.17  16.79  17.42  15.74  0.88  E-200  68.19  16.82  16.76  16.01  0.72  SEM  1.19  0.69  0.71  0.56  0.30  P-value  0.535  0.694  0.577  0.513  0.312  Contrast3 for the effect of different levels of curcuminoids  Linear  0.928  0.037  0.776  0.066  0.039  Quadratic  0.846  0.100  0.985  0.579  0.525  1Carcass composition represents values from 4 replicates (2 samples/replicate). 2Treatments consisted of basal diet without antioxidant supplement (Control); basal diet added 200 ppm alpha-tocopherol acetate (E-200); basal diet added turmeric oleoresin to provide 20 ppm (CUR-20), 40 ppm (CUR-40), 60 ppm (CUR-60), and 80 ppm (CUR-80) curcuminoids. 3P-values were obtained by orthogonal polynomial contrasts to test the effect of different levels of curcuminoids (0, 20, 40, 60, or 80 ppm), excluding positive control (E-200). 4Expressed as percentage of chilled carcass weight. View Large Skin Color Supplementation with curcuminoids was expected to increase the yellowness of chicken skin because in certain regions of the world consumers prefer such a trait. In the present study, the yellowness values (b*) of the breast and thigh skin increased linearly (P = 0.016 and 0.023, respectively) with increasing levels of dietary curcuminoids (Table 4). However, the L* and a* values of the skin showed no similar effect. In the present study, the effect of curcuminoids on the skin color of chickens was similar to the effect of marigold flower extract (lutein) (Wang et al., 2017). Table 4. Skin color of the breast and thigh of slow-growing chickens fed experimental diets.1 Treatment2  Breast skin  Thigh skin    L*  a*  b*  L*  a*  b*  Control  69.92  4.62  10.01  70.83  3.07  6.19  CUR-20  68.54  4.46  10.00  70.75  3.55  7.3  CUR-40  68.87  4.33  10.71  70.52  3.58  8.12  CUR-60  68.36  4.98  11.56  70.44  3.88  8.52  CUR-80  69.42  4.60  11.59  70.12  3.87  8.76  E-200  70.54  4.27  10.18  69.95  3.62  7.56  SEM  1.15  0.65  1.17  1.95  0.63  1.58  P-value  0.104  0.682  0.206  0.985  0.510  0.268  Contrast3 for the effect of different levels of curcuminoids  Linear  0.479  0.621  0.016  0.612  0.084  0.023  Quadratic  0.051  0.774  0.919  0.936  0.570  0.480  Treatment2  Breast skin  Thigh skin    L*  a*  b*  L*  a*  b*  Control  69.92  4.62  10.01  70.83  3.07  6.19  CUR-20  68.54  4.46  10.00  70.75  3.55  7.3  CUR-40  68.87  4.33  10.71  70.52  3.58  8.12  CUR-60  68.36  4.98  11.56  70.44  3.88  8.52  CUR-80  69.42  4.60  11.59  70.12  3.87  8.76  E-200  70.54  4.27  10.18  69.95  3.62  7.56  SEM  1.15  0.65  1.17  1.95  0.63  1.58  P-value  0.104  0.682  0.206  0.985  0.510  0.268  Contrast3 for the effect of different levels of curcuminoids  Linear  0.479  0.621  0.016  0.612  0.084  0.023  Quadratic  0.051  0.774  0.919  0.936  0.570  0.480  1Each mean represents values from 4 replicates (2 samples/replicate). 2Treatments consisted of basal diet without antioxidant supplement (Control); basal diet added 200 ppm alpha-tocopherol acetate (E-200); basal diet added turmeric oleoresin to provide 20 ppm (CUR-20), 40 ppm (CUR-40), 60 ppm (CUR-60), and 80 ppm (CUR-80) curcuminoids. 3P-values were obtained by orthogonal polynomial contrasts to test the effect of different levels of curcuminoids (0, 20, 40, 60, or 80 ppm), excluding positive control (E-200). View Large Drip Loss of the Meat The drip losses from the breast meat showed no significant differences between treatments (Figure 1), but those from the thigh meat of the antioxidant-treated groups tended to be lower (P = 0.06) than those from the control treatment. Increasing the levels of curcuminoids produced a linear effect (P = 0.035) on the drip loss from the thigh meat but had no effect on the breast meat. The higher fat content of the thigh meat might have resulted in the higher accumulation of curcuminoids or its metabolites in the muscle. The drip loss results agreed with those of Wang et al. (2015) because the oxidative defense system of muscle has a direct effect on water-holding capacity (Huff-Lonergan and Lonergan, 2005). Curcuminoids might have the potential to inhibit oxidation in membrane lipids, as suggested by Menon and Sudheer (2007), resulting in the increased integrity of the muscle cell membrane so that water entrapped in the meat can be retained. The results of the present study partly agreed with Zhang et al. (2015) who supplemented broiler diets with 50, 100, and 200 mg/kg curcumin. Figure 1. View largeDownload slide Drip loss (Mean ± SEM; n = 4/treatment; 2 samples/replicate) of the breast and thigh meat. Increasing level of curcuminoids linearly (P = 0.035) decreased the drip loss of thigh meat. Solid line represents for breast meat and dotted line for thigh meat. Figure 1. View largeDownload slide Drip loss (Mean ± SEM; n = 4/treatment; 2 samples/replicate) of the breast and thigh meat. Increasing level of curcuminoids linearly (P = 0.035) decreased the drip loss of thigh meat. Solid line represents for breast meat and dotted line for thigh meat. TBARS Value of Plasma and Meat There were no significant differences between the mean plasma TBARS levels (Figure 2) for treatments in which the basal ration was supplemented with either dl-α-tocopheryl acetate or different levels of curcuminoids and those for the control treatment. In the present study, the TBARS values in the plasma differed from those found by Akhavan-Salamat and Ghasemi (2016) using dietary 0.2% turmeric powder under heat stress conditions and those by Hosseini-Vashan et al. (2012) using 0.4 and 0.8% turmeric powder under normal conditions from d 0 to 28 and under heat stress conditions thereafter. In particular, the plasma TBARS levels from the E-200, CUR-40, and CUR-80 treatments were lower than the control treatment by 7.37, 9.41, and 10.03%, respectively. For the curcuminoids treatments, the pattern of the plasma TBARS levels corresponded with that of the drip loss from the breast and thigh meat, confirming the antioxidant effect of dietary curcuminoids on the chicken meat. Figure 2. View largeDownload slide Plasma TBARS (Mean ± SEM; n = 4/treatment; 2 samples/replicate) of chickens. Figure 2. View largeDownload slide Plasma TBARS (Mean ± SEM; n = 4/treatment; 2 samples/replicate) of chickens. The TBARS levels in the chicken meat exhibited significant differences (P < 0.01) between treatments and meat type (Table 5). The TBARS levels in the breast and thigh meat both shared the same trend, with the lowest value from the E-200 treatment. In the present study, the TBARS values from the frozen samples were measured during the 3-month storage period from different carcasses. There was no interaction between the dietary treatment and frozen storage time, implying that, in the present study, dietary curcuminoids could not protect the breast and thigh meat from oxidation during frozen storage. Indeed, the difference between the curcuminoids group and the negative control was not statistically significant (by orthogonal contrast). Table 5. TBARS value of the breast and thigh meat of slow-growing chickens fed experimental diets.1 Items    Breast  Thigh  Treatment (diet)2  Control    0.22ns  0.37ns  CUR-20    0.22†  0.36ns  CUR-40    0.31**  0.62**  CUR-60    0.19ns  0.43†  CUR-80    0.25*  0.55**  E-200    0.15  0.17  Time  1st Month    0.26  0.42  2nd Month    0.23  0.40  3rd Month    0.18  0.44  SEM    0.01  0.04  P-value  Diet  0.002  0.006    Time  0.003  0.664    Diet × Time  0.697  0.139  Items    Breast  Thigh  Treatment (diet)2  Control    0.22ns  0.37ns  CUR-20    0.22†  0.36ns  CUR-40    0.31**  0.62**  CUR-60    0.19ns  0.43†  CUR-80    0.25*  0.55**  E-200    0.15  0.17  Time  1st Month    0.26  0.42  2nd Month    0.23  0.40  3rd Month    0.18  0.44  SEM    0.01  0.04  P-value  Diet  0.002  0.006    Time  0.003  0.664    Diet × Time  0.697  0.139  1 1Each mean represents values from 4 replicates (2 samples/replicate/month). 2 2Treatments consisted of basal diet without antioxidant supplement (Control); basal diet added 200 ppm alpha-tocopherol acetate (E-200); basal diet added turmeric oleoresin to provide 20 ppm (CUR-20), 40 ppm (CUR-40), 60 ppm (CUR-60), and 80 ppm (CUR-80) curcuminoids. The label expressed the difference from the treatments to positive control (E-200) within each type of meat by Dunnett's Test, where “ns,” “†,” “*,” or “**” means no significance (P > 0.1), tending significance (0.05 < P ≤ 0.1), significance (P ≤ 0.05), or highly significance (P ≤ 0.01), respectively. View Large Increasing the supplementation with curcuminoids caused no dose-dependent response, as reported recently (Daneshyar, 2012; Zhang et al., 2015). The TBARS values in the meat exhibited the opposite pattern to that in the plasma. Lower plasma TBARS values were found in meat from the CUR-40 and CUR-80 treatments compared with those from the CUR-20 and CUR-60 treatments but the TBARS values in the breast and thigh meat were reversed. Under certain conditions, curcumin can exhibit pro-oxidant properties (Kelly et al., 2001; Galati et al., 2002), depending on its concentration and the presence of metal ions, but the mechanism in vivo has not been clearly determined (Joe et al., 2004). In the present study, it could be suggested that curcuminoids might switch from providing anti-oxidative activity in the living birds to become a pro-oxidative agent in the postmortem aging process. The changes in TBARS values during frozen storage (−20°C) are shown in Table 5. There was a significant difference (P < 0.05) in the TBARS values from the breast meat over the 3 mo of frozen storage, while that of the thigh meat showed no significant difference. The pattern of TBARS values in the thigh meat agreed with that found by Botsoglou et al. (2003) who found that the MDA values, measured in the breast and thigh muscles of chickens fed 6.06% soybean oil, stayed relatively constant up to mo 6 then rapidly increased thereafter up to 9 mo of frozen storage. Flavia et al. (2014) also found that the TBARS values of poultry fat did not differ significantly from d 1 until d 90 during frozen storage at −18°C. To evaluate the extent of lipid oxidation, the TBARS value is often used. However, lipid oxidation is a dynamic process, and the TBARS value of meat is likely to increase during storage, reach a peak, then decline (Larick and Parker, 2001). In the present study, a steady decrease in the TBARS values of the breast meat suggested that a significant breakdown of hydroperoxides occurred before the first measurement had been made. The difference in the influence of antioxidant between the breast and thigh meat in the present study agreed with results from Delles et al. (2016) who suggested that dietary antioxidants can ameliorate meat quality of broilers fed oxidized oil, and that this effect was more pronounced in the thigh than in the breast muscle. In the present study, the proportion of total PUFA, especially n-3 PUFA, was higher in the breast meat than in the thigh meat, probably because more antioxidant had been incorporated into the thigh meat, as reported by Botsoglou et al. (2003). Fatty Acid Profile of the Breast and Thigh Meat Supplementation with curcuminoids showed remarkable effects on certain FA in the breast meat (Table 6). The CUR-20 treatment led to the highest proportions of C18:2n-6 (linoleic acid) and total n-6 PUFA, significantly higher (P < 0.01) than those from the E-200 treatment. The CUR-40 treatment tended to increase (P < 0.10) the proportion of C18:1n-9 (oleic acid) compared with the E-200 treatment. A study by Daneshyar et al. (2011) determined that supplementation with 0.75% turmeric powder caused a significant decrease in the total SFA of thigh meat. Curcumin also was shown to inhibit the microsomal Δ5 and Δ6 desaturases of rat liver (Shimizu et al., 1992). Therefore, curcumin is likely to be involved in the regulation of the biosynthesis of PUFA in chicken. In fact, the linoleic acid content, constituting approximately 25% of total FA in the diets, accumulated in the breast meat of the curcuminoids groups significantly (P < 0.05) more than in the breast meat from the E-200 treatment. Supplementing with 20 mg/kg curcuminoids exhibited a larger down-regulation effect on FA synthesis than the other curcuminoids treatment levels by inhibiting the synthesis of longer chain PUFA in breast meat, which exhibited the highest content of linoleic acid and lowest proportion of DHA compared with either the control or the E-200 diet. The CUR-40 and CUR-60 treatments led to proportions of linoleic acid and DHA in the breast meat similar to those of the control. The CUR-60 treatment can therefore be used to provide the best response in terms of DHA content in the breast meat. Table 6. Fatty acid profile (g/100 g total FA) of the breast meat of the chickens. Items  Treatment (Diet)1  Time  SEM  P-value    Control  CUR-20  CUR-40  CUR-60  CUR-80  E-200  1st Month  2nd Month  3rd Month    Diet  Time  Diet × Time  C14:0  0.88  1.14  1.03  0.83  0.95  0.93  1.15  0.82  0.91  0.09  0.282  0.003  0.290  C16:0  23.91  23.28  24.01  23.80  23.15  23.83  25.21  22.52  23.25  1.29  0.547  <0.001  0.569  C18:0  11.70  11.14  11.43  11.36  11.12  11.86  10.26  11.81  12.22  1.64  0.753  <0.001  0.124  C20:0  0.31  0.25  0.23  0.41  0.23  0.28  0.50  0.36  0.00  0.08  0.699  <0.001  0.402  C22:0  0.51  0.40  0.41  0.62  0.44  0.49  0.31  0.42  0.69  0.08  0.250  <0.001  0.951  C16:1  1.18  1.32  1.51  1.24  1.47  1.14  1.71  1.19  1.04  0.31  0.540  0.003  0.043  C17:1  0.90  0.86  0.67  0.88  0.63  1.00  0.20  1.20  1.07  0.33  0.596  <0.001  0.795  C18:1n-9  23.15ns  24.47†  24.68†  21.57ns  24.33ns  22.56  27.22  21.79  21.37  6.56  0.0592  <0.001  0.589  C20:1  0.07  0.27  0.12  0.16  0.21  0.05  0.28  0.02  0.15  0.04  0.302  0.001  0.137  C18:2n-6  15.23ns  17.53**  16.28*  15.92†  16.87**  14.73  17.61  15.50  15.14  2.69  0.010  <0.001  0.155  C20:4n-6  5.93  5.29  5.48  6.24  5.47  6.63  4.29  6.48  6.74  1.51  0.212  <0.001  0.424  C18:3n-3  0.37  0.37  0.25  0.33  0.38  0.33  0.64  0.36  0.01  0.06  0.752  <0.001  0.960  C20:5n-3  1.63  1.81  1.52  1.83  1.65  1.77  1.40  1.80  1.94  0.15  0.571  <0.001  0.424  C22:6n-3  13.34ns  11.17*  11.93†  14.27ns  12.42ns  13.89  8.60  14.90  15.10  7.31  0.044  <0.001  0.739  SFA  37.74  36.63  37.43  37.35  36.29  37.70  37.89  36.55  37.13  3.44  0.498  0.065  0.148  MUFA  25.36  27.04  27.04  23.90  26.76  24.86  29.48  24.30  23.69  8.85  0.106  <0.001  0.305  PUFA  36.90  36.33  35.54  38.76  36.95  37.44  32.69  39.07  39.19  6.26  0.141  <0.001  0.872  Total n-6  21.56ns  22.98**  21.84ns  22.32†  22.49*  21.46  22.03  22.16  22.15  0.97  0.021  0.884  0.153  Total n-3  15.34ns  13.35*  13.70*  16.43ns  14.45ns  15.98  10.65  16.99  17.04  7.55  0.0612  <0.001  0.736  n-6/n-3  1.51  2.01  1.77  1.46  1.77  1.42  2.29  1.33  1.36  0.33  0.262  <0.001  0.727  Items  Treatment (Diet)1  Time  SEM  P-value    Control  CUR-20  CUR-40  CUR-60  CUR-80  E-200  1st Month  2nd Month  3rd Month    Diet  Time  Diet × Time  C14:0  0.88  1.14  1.03  0.83  0.95  0.93  1.15  0.82  0.91  0.09  0.282  0.003  0.290  C16:0  23.91  23.28  24.01  23.80  23.15  23.83  25.21  22.52  23.25  1.29  0.547  <0.001  0.569  C18:0  11.70  11.14  11.43  11.36  11.12  11.86  10.26  11.81  12.22  1.64  0.753  <0.001  0.124  C20:0  0.31  0.25  0.23  0.41  0.23  0.28  0.50  0.36  0.00  0.08  0.699  <0.001  0.402  C22:0  0.51  0.40  0.41  0.62  0.44  0.49  0.31  0.42  0.69  0.08  0.250  <0.001  0.951  C16:1  1.18  1.32  1.51  1.24  1.47  1.14  1.71  1.19  1.04  0.31  0.540  0.003  0.043  C17:1  0.90  0.86  0.67  0.88  0.63  1.00  0.20  1.20  1.07  0.33  0.596  <0.001  0.795  C18:1n-9  23.15ns  24.47†  24.68†  21.57ns  24.33ns  22.56  27.22  21.79  21.37  6.56  0.0592  <0.001  0.589  C20:1  0.07  0.27  0.12  0.16  0.21  0.05  0.28  0.02  0.15  0.04  0.302  0.001  0.137  C18:2n-6  15.23ns  17.53**  16.28*  15.92†  16.87**  14.73  17.61  15.50  15.14  2.69  0.010  <0.001  0.155  C20:4n-6  5.93  5.29  5.48  6.24  5.47  6.63  4.29  6.48  6.74  1.51  0.212  <0.001  0.424  C18:3n-3  0.37  0.37  0.25  0.33  0.38  0.33  0.64  0.36  0.01  0.06  0.752  <0.001  0.960  C20:5n-3  1.63  1.81  1.52  1.83  1.65  1.77  1.40  1.80  1.94  0.15  0.571  <0.001  0.424  C22:6n-3  13.34ns  11.17*  11.93†  14.27ns  12.42ns  13.89  8.60  14.90  15.10  7.31  0.044  <0.001  0.739  SFA  37.74  36.63  37.43  37.35  36.29  37.70  37.89  36.55  37.13  3.44  0.498  0.065  0.148  MUFA  25.36  27.04  27.04  23.90  26.76  24.86  29.48  24.30  23.69  8.85  0.106  <0.001  0.305  PUFA  36.90  36.33  35.54  38.76  36.95  37.44  32.69  39.07  39.19  6.26  0.141  <0.001  0.872  Total n-6  21.56ns  22.98**  21.84ns  22.32†  22.49*  21.46  22.03  22.16  22.15  0.97  0.021  0.884  0.153  Total n-3  15.34ns  13.35*  13.70*  16.43ns  14.45ns  15.98  10.65  16.99  17.04  7.55  0.0612  <0.001  0.736  n-6/n-3  1.51  2.01  1.77  1.46  1.77  1.42  2.29  1.33  1.36  0.33  0.262  <0.001  0.727  1Treatments consisted of basal diet without antioxidant supplement (Control); basal diet added 200 ppm alpha-tocopherol acetate (E-200); basal diet added turmeric oleoresin to provide 20 ppm (CUR-20), 40 ppm (CUR-40), 60 ppm (CUR-60), and 80 ppm (CUR-80) curcuminoids. 2The difference was tested with alpha = 0.10. Data of some detectable fatty ≤ 0.4% for all treatments are not shown (C15:0, C23:0, C20:2n-6). The label expressed the difference from the treatments to positive control (E-200) within each type of fatty acid by Dunnett's Test, where “ns,” “†,” “*,” or “**” means no significance (P > 0.1), tending significance (0.05 < P ≤ 0.1), significance (P ≤ 0.05), or high significance (P ≤ 0.01), respectively. View Large The proportion of FA, in particular n-3 PUFA in the thigh meat (Table 7), showed almost no meaningful changes caused by either the E-200 or curcuminoids treatments. The contents of FA in the thigh meat of the present study agreed with those reported by Daneshyar et al. (2011). To the best of our knowledge, the present study has provided the first observations on the FA contents of the meat of slow-growing chickens fed a combination of curcumin removed turmeric oleoresin and tuna oil. The combination of curcumin and long-chain n-3 PUFA might have had synergetic effects, causing a decrease in the accumulation of fat in the tissue (Forman et al., 1997) noting the effects of curcumin or long-chain n-3 PUFA on FA metabolism reported recently (Kang et al., 2013; Fan et al., 2016; Thota et al., 2016). Table 7. Fatty acid profile (g/100 g total FA) of thigh meat of the chickens. Item  Treatment (Diet)1  Time  SEM  P-value    Control  CUR-20  CUR-40  CUR-60  CUR-80  E-200  1st Month  2nd Month  3rd Month    Diet  Time  Diet × Time  C14:0  1.42  1.50  1.49  1.49  1.45  1.47  1.52  1.43  1.46  0.02  0.926  0.089  0.638  C16:0  22.17  21.56  21.86  21.74  22.15  21.96  22.09  21.88  21.52  2.60  0.983  0.480  0.566  C18:0  8.90  8.28  8.95  8.75  8.15  9.70  8.50  9.42  8.39  1.29  0.302  <0.001  0.450  C22:0  0.22  0.24  0.25  0.22  0.25  0.29  0.24  0.18  0.30  0.90  0.832  0.011  0.119  C16:1  3.16  2.87  3.08  2.97  3.57  2.63  3.14  2.73  3.24  0.44  0.354  0.001  0.135  C17:1  0.47  0.51  0.49  0.30  0.34  0.71  0.26  0.62  0.54  0.13  0.180  0.008  0.061  C18:1n-9  28.31  28.61  28.76  28.34  29.86  27.45  28.68  28.05  28.98  2.24  0.088  0.091  0.637  C20:1  0.53  0.54  0.47  0.47  0.46  0.43  0.69  0.06  0.71  0.01  0.222  <0.001  0.399  C18:2n-6  22.35  23.56  22.57  23.33  22.30  22.37  23.10  22.28  22.99  1.84  0.448  0.011  0.192  C18:3n-6  0.10  0.11  0.08  0.06  0.09  0.14  0.20  0.08  0.00  0.01  0.536  <0.001  0.417  C20:4n-6  2.75  2.47  2.54  2.63  2.20  2.95  2.28  2.91  2.63  0.35  0.404  0.001  0.557  C18:3n-3  0.35  0.34  0.37  0.35  0.36  0.36  0.25  0.65  0.14  0.04  0.991  <0.001  0.999  C20:5n-3  1.37  1.47  1.34  1.40  1.34  1.30  1.39  1.32  1.42  0.05  0.687  0.266  0.755  C22:6n-3  6.70  6.83  6.69  6.60  6.36  6.95  6.71  6.73  6.69  1.63  0.954  0.995  0.549  SFA  33.41  32.28  33.17  32.87  32.72  34.08  33.02  33.66  32.30  4.79  0.788  0.057  0.573  MUFA  32.69  32.77  33.02  32.30  34.45  31.41  32.99  31.75  33.62  4.03  0.247  0.001  0.656  PUFA  33.90  34.95  33.81  34.83  32.83  34.51  33.99  34.57  34.03  5.26  0.455  0.568  0.521  Total n-6  25.41  26.30  25.40  26.46  24.77  25.90  25.60  25.85  25.85  2.46  0.419  0.801  0.441  Total n-3  8.52  8.65  8.41  8.37  8.06  8.61  8.37  8.67  8.22  1.74  0.929  0.528  0.437  n-6/n-3  3.03  3.11  3.06  3.20  3.16  3.08  3.11  3.05  3.19  0.22  0.971  0.602  0.467  Item  Treatment (Diet)1  Time  SEM  P-value    Control  CUR-20  CUR-40  CUR-60  CUR-80  E-200  1st Month  2nd Month  3rd Month    Diet  Time  Diet × Time  C14:0  1.42  1.50  1.49  1.49  1.45  1.47  1.52  1.43  1.46  0.02  0.926  0.089  0.638  C16:0  22.17  21.56  21.86  21.74  22.15  21.96  22.09  21.88  21.52  2.60  0.983  0.480  0.566  C18:0  8.90  8.28  8.95  8.75  8.15  9.70  8.50  9.42  8.39  1.29  0.302  <0.001  0.450  C22:0  0.22  0.24  0.25  0.22  0.25  0.29  0.24  0.18  0.30  0.90  0.832  0.011  0.119  C16:1  3.16  2.87  3.08  2.97  3.57  2.63  3.14  2.73  3.24  0.44  0.354  0.001  0.135  C17:1  0.47  0.51  0.49  0.30  0.34  0.71  0.26  0.62  0.54  0.13  0.180  0.008  0.061  C18:1n-9  28.31  28.61  28.76  28.34  29.86  27.45  28.68  28.05  28.98  2.24  0.088  0.091  0.637  C20:1  0.53  0.54  0.47  0.47  0.46  0.43  0.69  0.06  0.71  0.01  0.222  <0.001  0.399  C18:2n-6  22.35  23.56  22.57  23.33  22.30  22.37  23.10  22.28  22.99  1.84  0.448  0.011  0.192  C18:3n-6  0.10  0.11  0.08  0.06  0.09  0.14  0.20  0.08  0.00  0.01  0.536  <0.001  0.417  C20:4n-6  2.75  2.47  2.54  2.63  2.20  2.95  2.28  2.91  2.63  0.35  0.404  0.001  0.557  C18:3n-3  0.35  0.34  0.37  0.35  0.36  0.36  0.25  0.65  0.14  0.04  0.991  <0.001  0.999  C20:5n-3  1.37  1.47  1.34  1.40  1.34  1.30  1.39  1.32  1.42  0.05  0.687  0.266  0.755  C22:6n-3  6.70  6.83  6.69  6.60  6.36  6.95  6.71  6.73  6.69  1.63  0.954  0.995  0.549  SFA  33.41  32.28  33.17  32.87  32.72  34.08  33.02  33.66  32.30  4.79  0.788  0.057  0.573  MUFA  32.69  32.77  33.02  32.30  34.45  31.41  32.99  31.75  33.62  4.03  0.247  0.001  0.656  PUFA  33.90  34.95  33.81  34.83  32.83  34.51  33.99  34.57  34.03  5.26  0.455  0.568  0.521  Total n-6  25.41  26.30  25.40  26.46  24.77  25.90  25.60  25.85  25.85  2.46  0.419  0.801  0.441  Total n-3  8.52  8.65  8.41  8.37  8.06  8.61  8.37  8.67  8.22  1.74  0.929  0.528  0.437  n-6/n-3  3.03  3.11  3.06  3.20  3.16  3.08  3.11  3.05  3.19  0.22  0.971  0.602  0.467  1Treatments consisted of basal diet without antioxidant supplement (Control); basal diet added 200 ppm alpha-tocopherol acetate (E-200); basal diet added turmeric oleoresin to provide 20 ppm (CUR-20), 40 ppm (CUR-40), 60 ppm (CUR-60), and 80 ppm (CUR-80) curcuminoids. Data of some detectable fatty ≤ 0.50% for all treatments are not shown (C15:0, C24:1, C20:2n-6). View Large Regarding the TBARS values in the breast and thigh meat, the individual treatments did not affect the proportion of total n-3 PUFA during the period of frozen storage. The proportions of C18:3n-3 (α-linolenic acid), C20:5n-3 (EPA), and DHA in the breast meat increased (P < 0.001) during the 3 mo of storage at −20°C. The higher proportions of EPA and DHA found in the frozen breast meat agreed with Zymon et al. (2007) who also found a tendency towards higher contents of EPA and DHA in frozen veal stored for 3 mo at −18°C. A study comparing slow-growing chickens (a similar breed to that in the present study) with commercial broilers has revealed that the PUFA content (mg/g) of the breast and thigh meat of the “Korat Meat Chicken” increased, while that of the broilers decreased after 8 mo of frozen storage (Jirawat Yongsawatdigul, SUT, Nakhon Ratchasima, personal communication). This could suggest that there were certain changes during frozen storage rather than autoxidation and hydrolysis. In the present study, no changes occurred in the EPA or DHA content of the thigh meat during 3 mo of frozen storage. Horbanczuk et al. (2015) showed that the DHA and total PUFA content of meat from ostriches fed 4 or 8% linseed oil decreased, especially between 61 to 120 d of frozen storage at −20°C, but the FA profile of the meat was not influenced up to 60 d, with different muscles having varied responses. In conclusion, dietary supplementation with curcuminoids in the form of the curcumin removed turmeric oleoresin showed positive effects on FCR, breast fillet weight, and the yellowness of the chicken skin. The curcuminoids exhibited antioxidant and pro-antioxidant effects that were not dose dependent. The present study has shown that a suitable level of curcuminoids for supplementing the diets of slow-growing chickens was 60 mg/kg. Further studies are needed to investigate how to enhance the bioavailability of the oleoresin at the molecular level. This would help to determine the activity of curcuminoids on the antioxidative defense system and on the accumulation of n-3 PUFA by combining curcuminoids and n-3 PUFA in the chicken diet. ACKNOWLEDGEMENTS We gratefully acknowledge the mainly financial support of The Thailand Research Fund (TRF) and the Suranaree University of Technology (SUT) under the project “Establishment of “Korat Meat Chicken” Strain for Small and Micro Community Enterprise Production.” We also highly appreciate the “PhD Scholarship for ASEAN Countries” program of SUT for partly financially supporting this research. REFERENCES Abou-Elkhair R., Ahmed H. A., Selim S.. 2014. 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Effect of freezing and frozen storage on fatty acid profile of calves' meat. Pol. J. Food Nutr. Sci.  57: 647– 650. © 2017 Poultry Science Association Inc. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Poultry Science Oxford University Press

Supplementation with curcuminoids and tuna oil influenced skin yellowness, carcass composition, oxidation status, and meat fatty acids of slow-growing chickens

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Oxford University Press
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© 2017 Poultry Science Association Inc.
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0032-5791
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Abstract

Abstract The present study aimed to determine the effects of dietary curcuminoids combined with tuna oil on the growth performance, meat quality, thiobarbituric acid reactive substances (TBARS) values in the plasma and raw meat, and fatty acid profile of chicken meat. A total of 480 21-day-old mixed-sex slow-growing chickens was assigned to a completely randomized design model with 6 treatments and 4 replicates (pens) per treatment. The basal diet based on corn-soybean and 4% tuna oil was used as the negative control. The experimental diets comprised the basal diet supplemented with curcumin removed turmeric oleoresin to provide 20, 40, 60, or 80 mg/kg curcuminoids (CUR-20, CUR-40, CUR-60, and CUR-80, respectively) or dl-α-tocopheryl acetate at 200 ppm as the positive control (E-200). Finally, the vacuum-packed carcasses were stored frozen at −20°C for 3 mo to examine the effect of curcuminoids on changes in the TBARS values and fatty acid composition of the breast and thigh meat. Increasing the levels of curcuminoids tended to improve the feed conversion ratio (linear, P = 0.065) and significantly increased the proportion of breast fillet (linear, P = 0.037) and the yellowness of the skin of both the breast (linear, P = 0.016) and the thigh (linear, P = 0.023). The curcuminoids exhibited antioxidant properties, but their effect was not dose dependent. The CUR-20 and CUR-40 treatments increased the linoleic acid content but decreased the C22:6n-3 (DHA) content of the breast meat. The CUR-60 treatment inhibited oxidation (measured by TBARS) in the chicken meat similarly to dl-α-tocopheryl acetate but had no effect on the proportion of DHA in the breast or thigh meat. Auto-oxidation occurred in the breast meat but not in the thigh meat during the 3 mo of frozen storage. The present study showed that a suitable level of curcuminoids in the diet of slow-growing chickens was 60 mg/kg. INTRODUCTION Meat enriched with n-3 polyunsaturated fatty acids (PUFA) makes it more susceptible to lipid oxidation (Cortinas et al., 2004), which causes deterioration in the flavor, color, texture, and nutritive value of the meat and the production of toxic compounds (Kanner, 1994). Therefore, antioxidants are used in poultry feed to limit the rate of oxidation in the bird itself, and in the subsequent poultry products (Leeson, 2012). Antioxidants from natural sources are usually considered “generally recognized as safe” (GRAS) and so can be suitable alternatives to synthetic antioxidants. The antioxidant properties of curcumin and its derivatives have been studied extensively (Masuda et al., 1999; Barclay et al., 2000; Fujisawa et al., 2004). Curcumin can help to stabilize free radicals (Barzegar and Moosavi-Movahedi, 2011) and increase the activities of antioxidant enzymes (Aggarwal, 2010). Its derivatives, demethoxycurcumin and bisdemethoxycurcumin, also have antioxidant effects (Chattopadhyay et al., 2004). Therefore, it is hypothesized that curcuminoids could prevent oxidation in meat enriched with n-3 PUFA. Dietary turmeric powder in broiler diets has been shown to decrease the content of triglycerides and saturated fatty acids (SFA) in thigh meat (Daneshyar et al., 2011). Combining with curcuminoids and long-chain n-3 PUFA might have synergetic effects and enhance the accumulation of C22:6n-3 (DHA) in chicken meat. Therefore, it can be hypothesized that a combination of curcuminoids and tuna oil, rich in DHA, can protect chicken meat from lipid oxidation and influence its fatty acid (FA) profile. To the best of our knowledge, there have been no studies on the effect of supplementing the diet of slow-growing chickens with different levels of curcuminoids from curcumin removed turmeric oleoresin combined with tuna oil. Such a study could be a model for types of slow-growing chickens in various countries to produce value-added chicken meat with high n-3 PUFA, and so improve the competitiveness of small- and medium-sized farms. Therefore, the present study aims to determine the effects of dietary curcuminoids combined with tuna oil on the growth performance, carcass yield, skin color, and drip loss of chicken meat, the levels of thiobarbituric acid reactive substances (TBARS) in the plasma and raw chicken meat, and the FA profile of chicken meat. It also aims to evaluate the oxidative inhibition property of curcuminoids on TBARS values and the FA composition of meat during 3 mo of frozen storage at −20°C. MATERIALS AND METHODS Birds, Experimental Design, and Diets All procedures used in the present study were approved by the Ethics Committee on Animal Use of the Suranaree University of Technology (SUT). The study used a type of Thai indigenous crossbred chicken, the “Korat meat chicken” (male Lueng Hang Khao and female SUT line). Four-hundred-eighty one-day-old mixed-sex chicks were housed and cared for following the SUT farm guidelines. The chicks were fed a corn-soybean meal based diet (21% CP and 3,100 kcal ME/kg) from d 1 to 21. On d 21, the chicks, with an average BW of 289.05 ± 6.66 g, were randomly allotted to 6 experimental diets with 4 replications of 20 birds each in a completely randomized design. The study lasted for 63 d, from d 22 to 84. The chicks were fed ad libitum throughout the experimental period. For all treatments, the birds were reared in floor pens (8 birds/m2) in an open-sided house. The basal ration (Table 1), containing 2% crude rice bran oil (RBO; Thai Ruam Jai Korat Co. Ltd., Nakhon Ratchasima, Thailand) and 4% tuna oil (TO; feed grade; T. C. Union Agrotech Co. Ltd., Bangkok, Thailand), was used as the negative control diet. The positive control diet (E-200) was the basal ration supplemented with dl-α-tocopheryl acetate [Zagro (Thailand) Co. Ltd., Pathum Thani, Thailand] at 200 mg/kg. The other treatment diets, CUR-20, CUR-40, CUR-60, and CUR-80, comprised the basal ration with added curcumin removed turmeric oleoresin (Government Pharmaceutical Organization, Bangkok, Thailand) to provide diets with 20, 40, 60, or 80 mg/kg curcuminoids, respectively. The total curcuminoids content of the curcumin removed turmeric oleoresin was 21.6 ± 0.62% by weight. Table 1. Ingredients and nutrient composition of the basal diets (as-fed basis). Items  Grower   Finisher    (d 22 to 42)  (d 43 to 84)   Soybean meal (44% CP)   33.55   26.55   Corn (8% CP)   50.36   51.50   De-oil rice bran   6.11   12.48   Tuna oil   4.00   4.00   Rice bran oil   2.00   2.00   DL-Methionine   0.25   0.19   L-Lysine   0.13   0.10   L-Threonine   0.10   0.06   Salt   0.35   0.28   CaCO3   1.57   1.42   Monocalcium phosphate (21% P)   1.08   0.92   Premix1   0.50   0.50  Calculated nutrients level (% unless stated otherwise)   ME (kcal/kg)   3100   3100   CP   19.0   17.0   Digestible lysine   1.00   0.85   Digestible methionine   0.51   0.43   Digestible Met + Cys   0.76   0.65   Digestible threonine   0.69   0.58   Calcium   0.90   0.80   Available phosphorus   0.35   0.30  Analyzed nutrient level (%)   Total lipid2 (%)   7.30   7.74  Fatty acid profile (% of total fatty acid)   Saturated fatty acids   31.98   30.33   Monounsaturated fatty acids   32.93   32.56   Polyunsaturated fatty acids   35.09   37.11   n-6   26.58   26.89   n-3   8.51   10.22   n-6/n-3   3.12   2.63  Items  Grower   Finisher    (d 22 to 42)  (d 43 to 84)   Soybean meal (44% CP)   33.55   26.55   Corn (8% CP)   50.36   51.50   De-oil rice bran   6.11   12.48   Tuna oil   4.00   4.00   Rice bran oil   2.00   2.00   DL-Methionine   0.25   0.19   L-Lysine   0.13   0.10   L-Threonine   0.10   0.06   Salt   0.35   0.28   CaCO3   1.57   1.42   Monocalcium phosphate (21% P)   1.08   0.92   Premix1   0.50   0.50  Calculated nutrients level (% unless stated otherwise)   ME (kcal/kg)   3100   3100   CP   19.0   17.0   Digestible lysine   1.00   0.85   Digestible methionine   0.51   0.43   Digestible Met + Cys   0.76   0.65   Digestible threonine   0.69   0.58   Calcium   0.90   0.80   Available phosphorus   0.35   0.30  Analyzed nutrient level (%)   Total lipid2 (%)   7.30   7.74  Fatty acid profile (% of total fatty acid)   Saturated fatty acids   31.98   30.33   Monounsaturated fatty acids   32.93   32.56   Polyunsaturated fatty acids   35.09   37.11   n-6   26.58   26.89   n-3   8.51   10.22   n-6/n-3   3.12   2.63  1Premix (0.5%) provided the following per kilogram of diet: 15,000 IU of vitamin A; 3000 IU of vitamin D3; 25 IU of vitamin E; 5 mg of vitamin K3; 2 mg of vitamin B1; 7 mg of vitamin B2; 4 mg of vitamin B6; 25 μg of vitamin B12; 11.04 mg of pantothenic acid; 35 mg of nicotinic acid; 1 mg of folic acid; 15 μg of biotin; 250 mg of choline chloride; 1.6 mg of Cu; 60 mg of Mn; 45 mg of Zn; 80 mg of Fe; 0.4 mg of I; 0.15 mg of Se. 2Extracted by chloroform: methanol (2:1 vol/vol). View Large Sampling and Storage Conditions On d 84, chickens whose weight was within 10% of the mean of the experimental unit were transported to the university slaughterhouse, where they were stunned using electricity, bled, scalded, de-feathered by machine, then manually eviscerated. The carcasses were washed with clean water, weighed, then cooled in a chill room (4°C, 24 h) before cutting into portions. The carcass composition of 48 birds (one male and one female per experimental unit) was measured. After chilling, samples of breast and thigh meat were used to evaluate skin color and drip loss. A total of 144 birds was harvested (3 males and 3 females per pen), then the whole carcasses were vacuum-packed and chilled for 24 h at 4°C, followed by freezing at −20°C and 15, 60, or 90 d of frozen storage. Before analysis, the carcasses were thawed in ice-slurry, followed by manually separating the breast and thigh meat (without skin). The chilled breast and thigh meat were chopped then blended individually immediately after separation. The individually minced meat samples were used to determine the TBARS levels and FA composition. Measurements and Chemical Analysis Growth Performance and Carcass Composition The BW and feed intake per pen were monitored each wk to allow the ADG, ADFI, and feed conversion ratio (FCR) values to be calculated. The occurrence of mortality also was recorded. The abdominal fat was considered as the fat extending within the ischium, surrounding the cloaca, and adjacent to the abdominal muscles. The dressed weight and weight of abdominal fat were then calculated as a proportion of the live BW of the chicken. The weight of the breast fillet, thigh, and drumstick were expressed as a percentage of the chilled carcass weight. Skin Color Measurement The skin color was measured using a Hunter Lab ColorQuest XE spectrophotometer with QC Software (Reston, VA) calibrated against black and white reference tiles. The L* (lightness), a* (redness), and b* (yellowness) values were obtained by an illuminant/observer D65/10°. The measurements were made through the transparent packaging material. Three random readings were taken from the sample surface then averaged for statistical analysis. Drip Loss of Meat. Pieces of breast and thigh muscles from the same location were cut to a shape of 1.5 × 3.0 × 0.5 cm. The samples were suspended inside a chilled storage room at 4°C for 24 h using airtight containers. The drip loss was expressed as a percentage of the initial weight. Plasma TBARS Measurement Blood samples were collected from 8 chickens per treatment (one male and one female per pen) into EDTA-treated tubes, then gently shaken and kept and handled on wet ice. The plasma was separated by centrifuging the blood samples at 1,000 × g for 10 min at 4°C, then transferred to 1.5-mL microcentrifuge tubes and stored at −80°C. The TBARS values of the EDTA-treated plasma were measured using the modified method of Grotto et al. (2007). A standard curve for 1,1,3,3-tetramethoxypropane (Sigma-Aldrich Pte Ltd., Singapore) was used, and the concentration was expressed as nmol MDA/mL solution. The TBARS values were then determined using a Bio-Rad Benchmark Plus Microplate Reader (Bio-Rad Laboratories Inc., Hercules, CA). Meat TBARS Measurement The TBARS values of duplicate 5-g samples of the raw chicken meat were measured following the protocol of Leick et al. (2010). The samples, blanks, and standards were read at 530 nm using a Bio-Rad Benchmark Plus Microplate Reader. Meat Fatty Acid Profile The lipids were extracted from approximately 5 g of each muscle sample using 90 mL of chloroform: methanol (2:1, vol/vol) (Folch et al., 1957). After between 20 and 25 mg of the extracted fat had been methylated (Metcalfe et al., 1966), the FA methyl esters were analyzed using gas chromatography (Hewlett-Packard 7890A; Agilent Technologies, Santa Clara, CA) using a capillary column (SP 2560, Supelco Inc., Bellefonte, PA, 100 m × 0.25 mm i.d., 0.20-μm film thickness) and a flame ionization detector. The carrier gas was helium at a flow rate of 0.95 mL/min. The temperatures of the injector and detector were 260°C. The initial column temperature was 70°C, which was then raised to 175°C at a rate of 13°C/min, then finally to 240°C at a rate of 4°C/min. Statistical Analysis The mean values from each pen were used as the experimental unit for all analyses. Analysis of variance was performed using the GLM procedure of SAS University Edition (SAS Institute Inc., Cary, NC). The data from the FA profiles and the TBARS contents of the chicken meat during storage were analyzed by the PROC MIXED and REPEATED procedures in SAS. Orthogonal polynomial contrasts were used to test the linear and quadratic effects of increasing the levels of curcuminoids (0, 20, 40, 60, and 80 mg/kg) in the diet. The differences between the means of the curcuminoids-treated and control groups were tested by orthogonal contrast, while Dunnett's test was used to compare the effects of each curcuminoids level with the positive controls. Overall differences between treatment means were considered to be significant at P ≤ 0.05, with a tendency toward significance being declared at 0.05 < P ≤ 0.1. Data were expressed as the mean ± SEM, representing the pooled SEM for the model. RESULTS AND DISCUSSION Growth Performance and Carcass Yield The mortality of chickens observed in the negative control, CUR-60, and CUR-80 treatments were 2.50, 3.75, and 2.50%, respectively. The dietary treatments had no effect on the final BW or ADG of the chickens compared with the control treatments (Table 2). Increasing the level of curcuminoids tended to improve the overall FCR linearly (P = 0.065 by orthogonal polynomial contrast). Table 2. Growth performance of slow-growing chickens fed experimental diets.1 Treatment2  BW d 21 (kg/b)  BW d 84 (kg/b)  ADG (g/b/d)  ADFI (g/b/d)  FCR  Control  0.27  1.79  24.13  70.99  2.94  CUR-20  0.27  1.75  23.48  68.26  2.91  CUR-40  0.28  1.80  24.23  70.91  2.93  CUR-60  0.27  1.79  24.11  69.37  2.88  CUR-80  0.27  1.77  23.71  67.24  2.84  E-200  0.27  1.78  23.89  68.12  2.85  SEM  0.01  0.05  0.84  2.11  0.08  P-value  0.889  0.781  0.793  0.103  0.307  Contrast3 for the effect of different levels of curcuminoids  Linear  0.651  0.840  0.880  0.091  0.065  Quadratic  0.582  0.774  0.820  0.485  0.591  Treatment2  BW d 21 (kg/b)  BW d 84 (kg/b)  ADG (g/b/d)  ADFI (g/b/d)  FCR  Control  0.27  1.79  24.13  70.99  2.94  CUR-20  0.27  1.75  23.48  68.26  2.91  CUR-40  0.28  1.80  24.23  70.91  2.93  CUR-60  0.27  1.79  24.11  69.37  2.88  CUR-80  0.27  1.77  23.71  67.24  2.84  E-200  0.27  1.78  23.89  68.12  2.85  SEM  0.01  0.05  0.84  2.11  0.08  P-value  0.889  0.781  0.793  0.103  0.307  Contrast3 for the effect of different levels of curcuminoids  Linear  0.651  0.840  0.880  0.091  0.065  Quadratic  0.582  0.774  0.820  0.485  0.591  1Each mean of growth performance represents values from 4 replicates (20 birds/replicate). 2Treatments consisted of basal diet without antioxidant supplement (Control); basal diet added 200 ppm alpha-tocopherol acetate (E-200); basal diet added turmeric oleoresin to provide 20 ppm (CUR-20), 40 ppm (CUR-40), 60 ppm (CUR-60), and 80 ppm (CUR-80) curcuminoids. 3 3P-values were obtained by orthogonal polynomial contrasts to test the effect of different levels of curcuminoids (0, 20, 40, 60, or 80 ppm), excluding positive control (E-200). View Large The growth performance in the present study was in line with that reported elsewhere (Emadi and Kermanshahi, 2006; Mehala and Moorthy, 2008; Rahmatnejad et al., 2009). The tendency of improving the FCR in the present study agreed with Rajput et al. (2013b) who demonstrated that supplementing the diet with 200 mg/kg pure curcumin improved the feed efficiency of broiler chickens. The dressing percentage was not significantly affected by the different diet treatments (Table 3) agreeing with the findings of Abou-Elkhair et al. (2014). The present study showed a linear effect (P = 0.039; by polynomial contrast) of the different levels of curcuminoids in the diet on the amount of abdominal fat. Nouzarian et al. (2011) supplemented the diet of broiler chickens with turmeric powder (38.28 mg/kg curcumin content) and found a statistically significant decrease in the amount of abdominal fat while Rajput et al. (2013a) using 150 mg/kg pure curcumin in the diet of broiler chickens showed no similar effect. These inconsistent results may have been caused by the different forms of the supplements, and the amount of abdominal fat might have been influenced by the turmeric oils or by the synergetic effects of the oil and curcuminoids rather than by the pure curcumin itself, as reported by Honda et al. (2006). The percentage of breast fillet increased linearly (P = 0.037) with increasing levels of curcuminoids. Such an improvement partly agreed with the findings of Wang et al. (2015) who found that dietary supplementation with turmeric rhizome extract at 300 mg/kg increased the breast-to-carcass weight ratio of broilers. Table 3. Carcass composition of slow-growing chickens fed experimental diets.1 Treatment2  Dressing (%)  Breast fillet4 (%)  Thigh4 (%)  Drumstick4 (%)  Abdominal fat (%)  Control  68.61  16.09  17.43  16.28  0.41  CUR-20  68.28  16.38  17.05  16.18  0.75  CUR-40  67.73  17.09  17.61  15.86  0.66  CUR-60  69.35  17.49  17.42  15.59  0.87  CUR-80  68.17  16.79  17.42  15.74  0.88  E-200  68.19  16.82  16.76  16.01  0.72  SEM  1.19  0.69  0.71  0.56  0.30  P-value  0.535  0.694  0.577  0.513  0.312  Contrast3 for the effect of different levels of curcuminoids  Linear  0.928  0.037  0.776  0.066  0.039  Quadratic  0.846  0.100  0.985  0.579  0.525  Treatment2  Dressing (%)  Breast fillet4 (%)  Thigh4 (%)  Drumstick4 (%)  Abdominal fat (%)  Control  68.61  16.09  17.43  16.28  0.41  CUR-20  68.28  16.38  17.05  16.18  0.75  CUR-40  67.73  17.09  17.61  15.86  0.66  CUR-60  69.35  17.49  17.42  15.59  0.87  CUR-80  68.17  16.79  17.42  15.74  0.88  E-200  68.19  16.82  16.76  16.01  0.72  SEM  1.19  0.69  0.71  0.56  0.30  P-value  0.535  0.694  0.577  0.513  0.312  Contrast3 for the effect of different levels of curcuminoids  Linear  0.928  0.037  0.776  0.066  0.039  Quadratic  0.846  0.100  0.985  0.579  0.525  1Carcass composition represents values from 4 replicates (2 samples/replicate). 2Treatments consisted of basal diet without antioxidant supplement (Control); basal diet added 200 ppm alpha-tocopherol acetate (E-200); basal diet added turmeric oleoresin to provide 20 ppm (CUR-20), 40 ppm (CUR-40), 60 ppm (CUR-60), and 80 ppm (CUR-80) curcuminoids. 3P-values were obtained by orthogonal polynomial contrasts to test the effect of different levels of curcuminoids (0, 20, 40, 60, or 80 ppm), excluding positive control (E-200). 4Expressed as percentage of chilled carcass weight. View Large Skin Color Supplementation with curcuminoids was expected to increase the yellowness of chicken skin because in certain regions of the world consumers prefer such a trait. In the present study, the yellowness values (b*) of the breast and thigh skin increased linearly (P = 0.016 and 0.023, respectively) with increasing levels of dietary curcuminoids (Table 4). However, the L* and a* values of the skin showed no similar effect. In the present study, the effect of curcuminoids on the skin color of chickens was similar to the effect of marigold flower extract (lutein) (Wang et al., 2017). Table 4. Skin color of the breast and thigh of slow-growing chickens fed experimental diets.1 Treatment2  Breast skin  Thigh skin    L*  a*  b*  L*  a*  b*  Control  69.92  4.62  10.01  70.83  3.07  6.19  CUR-20  68.54  4.46  10.00  70.75  3.55  7.3  CUR-40  68.87  4.33  10.71  70.52  3.58  8.12  CUR-60  68.36  4.98  11.56  70.44  3.88  8.52  CUR-80  69.42  4.60  11.59  70.12  3.87  8.76  E-200  70.54  4.27  10.18  69.95  3.62  7.56  SEM  1.15  0.65  1.17  1.95  0.63  1.58  P-value  0.104  0.682  0.206  0.985  0.510  0.268  Contrast3 for the effect of different levels of curcuminoids  Linear  0.479  0.621  0.016  0.612  0.084  0.023  Quadratic  0.051  0.774  0.919  0.936  0.570  0.480  Treatment2  Breast skin  Thigh skin    L*  a*  b*  L*  a*  b*  Control  69.92  4.62  10.01  70.83  3.07  6.19  CUR-20  68.54  4.46  10.00  70.75  3.55  7.3  CUR-40  68.87  4.33  10.71  70.52  3.58  8.12  CUR-60  68.36  4.98  11.56  70.44  3.88  8.52  CUR-80  69.42  4.60  11.59  70.12  3.87  8.76  E-200  70.54  4.27  10.18  69.95  3.62  7.56  SEM  1.15  0.65  1.17  1.95  0.63  1.58  P-value  0.104  0.682  0.206  0.985  0.510  0.268  Contrast3 for the effect of different levels of curcuminoids  Linear  0.479  0.621  0.016  0.612  0.084  0.023  Quadratic  0.051  0.774  0.919  0.936  0.570  0.480  1Each mean represents values from 4 replicates (2 samples/replicate). 2Treatments consisted of basal diet without antioxidant supplement (Control); basal diet added 200 ppm alpha-tocopherol acetate (E-200); basal diet added turmeric oleoresin to provide 20 ppm (CUR-20), 40 ppm (CUR-40), 60 ppm (CUR-60), and 80 ppm (CUR-80) curcuminoids. 3P-values were obtained by orthogonal polynomial contrasts to test the effect of different levels of curcuminoids (0, 20, 40, 60, or 80 ppm), excluding positive control (E-200). View Large Drip Loss of the Meat The drip losses from the breast meat showed no significant differences between treatments (Figure 1), but those from the thigh meat of the antioxidant-treated groups tended to be lower (P = 0.06) than those from the control treatment. Increasing the levels of curcuminoids produced a linear effect (P = 0.035) on the drip loss from the thigh meat but had no effect on the breast meat. The higher fat content of the thigh meat might have resulted in the higher accumulation of curcuminoids or its metabolites in the muscle. The drip loss results agreed with those of Wang et al. (2015) because the oxidative defense system of muscle has a direct effect on water-holding capacity (Huff-Lonergan and Lonergan, 2005). Curcuminoids might have the potential to inhibit oxidation in membrane lipids, as suggested by Menon and Sudheer (2007), resulting in the increased integrity of the muscle cell membrane so that water entrapped in the meat can be retained. The results of the present study partly agreed with Zhang et al. (2015) who supplemented broiler diets with 50, 100, and 200 mg/kg curcumin. Figure 1. View largeDownload slide Drip loss (Mean ± SEM; n = 4/treatment; 2 samples/replicate) of the breast and thigh meat. Increasing level of curcuminoids linearly (P = 0.035) decreased the drip loss of thigh meat. Solid line represents for breast meat and dotted line for thigh meat. Figure 1. View largeDownload slide Drip loss (Mean ± SEM; n = 4/treatment; 2 samples/replicate) of the breast and thigh meat. Increasing level of curcuminoids linearly (P = 0.035) decreased the drip loss of thigh meat. Solid line represents for breast meat and dotted line for thigh meat. TBARS Value of Plasma and Meat There were no significant differences between the mean plasma TBARS levels (Figure 2) for treatments in which the basal ration was supplemented with either dl-α-tocopheryl acetate or different levels of curcuminoids and those for the control treatment. In the present study, the TBARS values in the plasma differed from those found by Akhavan-Salamat and Ghasemi (2016) using dietary 0.2% turmeric powder under heat stress conditions and those by Hosseini-Vashan et al. (2012) using 0.4 and 0.8% turmeric powder under normal conditions from d 0 to 28 and under heat stress conditions thereafter. In particular, the plasma TBARS levels from the E-200, CUR-40, and CUR-80 treatments were lower than the control treatment by 7.37, 9.41, and 10.03%, respectively. For the curcuminoids treatments, the pattern of the plasma TBARS levels corresponded with that of the drip loss from the breast and thigh meat, confirming the antioxidant effect of dietary curcuminoids on the chicken meat. Figure 2. View largeDownload slide Plasma TBARS (Mean ± SEM; n = 4/treatment; 2 samples/replicate) of chickens. Figure 2. View largeDownload slide Plasma TBARS (Mean ± SEM; n = 4/treatment; 2 samples/replicate) of chickens. The TBARS levels in the chicken meat exhibited significant differences (P < 0.01) between treatments and meat type (Table 5). The TBARS levels in the breast and thigh meat both shared the same trend, with the lowest value from the E-200 treatment. In the present study, the TBARS values from the frozen samples were measured during the 3-month storage period from different carcasses. There was no interaction between the dietary treatment and frozen storage time, implying that, in the present study, dietary curcuminoids could not protect the breast and thigh meat from oxidation during frozen storage. Indeed, the difference between the curcuminoids group and the negative control was not statistically significant (by orthogonal contrast). Table 5. TBARS value of the breast and thigh meat of slow-growing chickens fed experimental diets.1 Items    Breast  Thigh  Treatment (diet)2  Control    0.22ns  0.37ns  CUR-20    0.22†  0.36ns  CUR-40    0.31**  0.62**  CUR-60    0.19ns  0.43†  CUR-80    0.25*  0.55**  E-200    0.15  0.17  Time  1st Month    0.26  0.42  2nd Month    0.23  0.40  3rd Month    0.18  0.44  SEM    0.01  0.04  P-value  Diet  0.002  0.006    Time  0.003  0.664    Diet × Time  0.697  0.139  Items    Breast  Thigh  Treatment (diet)2  Control    0.22ns  0.37ns  CUR-20    0.22†  0.36ns  CUR-40    0.31**  0.62**  CUR-60    0.19ns  0.43†  CUR-80    0.25*  0.55**  E-200    0.15  0.17  Time  1st Month    0.26  0.42  2nd Month    0.23  0.40  3rd Month    0.18  0.44  SEM    0.01  0.04  P-value  Diet  0.002  0.006    Time  0.003  0.664    Diet × Time  0.697  0.139  1 1Each mean represents values from 4 replicates (2 samples/replicate/month). 2 2Treatments consisted of basal diet without antioxidant supplement (Control); basal diet added 200 ppm alpha-tocopherol acetate (E-200); basal diet added turmeric oleoresin to provide 20 ppm (CUR-20), 40 ppm (CUR-40), 60 ppm (CUR-60), and 80 ppm (CUR-80) curcuminoids. The label expressed the difference from the treatments to positive control (E-200) within each type of meat by Dunnett's Test, where “ns,” “†,” “*,” or “**” means no significance (P > 0.1), tending significance (0.05 < P ≤ 0.1), significance (P ≤ 0.05), or highly significance (P ≤ 0.01), respectively. View Large Increasing the supplementation with curcuminoids caused no dose-dependent response, as reported recently (Daneshyar, 2012; Zhang et al., 2015). The TBARS values in the meat exhibited the opposite pattern to that in the plasma. Lower plasma TBARS values were found in meat from the CUR-40 and CUR-80 treatments compared with those from the CUR-20 and CUR-60 treatments but the TBARS values in the breast and thigh meat were reversed. Under certain conditions, curcumin can exhibit pro-oxidant properties (Kelly et al., 2001; Galati et al., 2002), depending on its concentration and the presence of metal ions, but the mechanism in vivo has not been clearly determined (Joe et al., 2004). In the present study, it could be suggested that curcuminoids might switch from providing anti-oxidative activity in the living birds to become a pro-oxidative agent in the postmortem aging process. The changes in TBARS values during frozen storage (−20°C) are shown in Table 5. There was a significant difference (P < 0.05) in the TBARS values from the breast meat over the 3 mo of frozen storage, while that of the thigh meat showed no significant difference. The pattern of TBARS values in the thigh meat agreed with that found by Botsoglou et al. (2003) who found that the MDA values, measured in the breast and thigh muscles of chickens fed 6.06% soybean oil, stayed relatively constant up to mo 6 then rapidly increased thereafter up to 9 mo of frozen storage. Flavia et al. (2014) also found that the TBARS values of poultry fat did not differ significantly from d 1 until d 90 during frozen storage at −18°C. To evaluate the extent of lipid oxidation, the TBARS value is often used. However, lipid oxidation is a dynamic process, and the TBARS value of meat is likely to increase during storage, reach a peak, then decline (Larick and Parker, 2001). In the present study, a steady decrease in the TBARS values of the breast meat suggested that a significant breakdown of hydroperoxides occurred before the first measurement had been made. The difference in the influence of antioxidant between the breast and thigh meat in the present study agreed with results from Delles et al. (2016) who suggested that dietary antioxidants can ameliorate meat quality of broilers fed oxidized oil, and that this effect was more pronounced in the thigh than in the breast muscle. In the present study, the proportion of total PUFA, especially n-3 PUFA, was higher in the breast meat than in the thigh meat, probably because more antioxidant had been incorporated into the thigh meat, as reported by Botsoglou et al. (2003). Fatty Acid Profile of the Breast and Thigh Meat Supplementation with curcuminoids showed remarkable effects on certain FA in the breast meat (Table 6). The CUR-20 treatment led to the highest proportions of C18:2n-6 (linoleic acid) and total n-6 PUFA, significantly higher (P < 0.01) than those from the E-200 treatment. The CUR-40 treatment tended to increase (P < 0.10) the proportion of C18:1n-9 (oleic acid) compared with the E-200 treatment. A study by Daneshyar et al. (2011) determined that supplementation with 0.75% turmeric powder caused a significant decrease in the total SFA of thigh meat. Curcumin also was shown to inhibit the microsomal Δ5 and Δ6 desaturases of rat liver (Shimizu et al., 1992). Therefore, curcumin is likely to be involved in the regulation of the biosynthesis of PUFA in chicken. In fact, the linoleic acid content, constituting approximately 25% of total FA in the diets, accumulated in the breast meat of the curcuminoids groups significantly (P < 0.05) more than in the breast meat from the E-200 treatment. Supplementing with 20 mg/kg curcuminoids exhibited a larger down-regulation effect on FA synthesis than the other curcuminoids treatment levels by inhibiting the synthesis of longer chain PUFA in breast meat, which exhibited the highest content of linoleic acid and lowest proportion of DHA compared with either the control or the E-200 diet. The CUR-40 and CUR-60 treatments led to proportions of linoleic acid and DHA in the breast meat similar to those of the control. The CUR-60 treatment can therefore be used to provide the best response in terms of DHA content in the breast meat. Table 6. Fatty acid profile (g/100 g total FA) of the breast meat of the chickens. Items  Treatment (Diet)1  Time  SEM  P-value    Control  CUR-20  CUR-40  CUR-60  CUR-80  E-200  1st Month  2nd Month  3rd Month    Diet  Time  Diet × Time  C14:0  0.88  1.14  1.03  0.83  0.95  0.93  1.15  0.82  0.91  0.09  0.282  0.003  0.290  C16:0  23.91  23.28  24.01  23.80  23.15  23.83  25.21  22.52  23.25  1.29  0.547  <0.001  0.569  C18:0  11.70  11.14  11.43  11.36  11.12  11.86  10.26  11.81  12.22  1.64  0.753  <0.001  0.124  C20:0  0.31  0.25  0.23  0.41  0.23  0.28  0.50  0.36  0.00  0.08  0.699  <0.001  0.402  C22:0  0.51  0.40  0.41  0.62  0.44  0.49  0.31  0.42  0.69  0.08  0.250  <0.001  0.951  C16:1  1.18  1.32  1.51  1.24  1.47  1.14  1.71  1.19  1.04  0.31  0.540  0.003  0.043  C17:1  0.90  0.86  0.67  0.88  0.63  1.00  0.20  1.20  1.07  0.33  0.596  <0.001  0.795  C18:1n-9  23.15ns  24.47†  24.68†  21.57ns  24.33ns  22.56  27.22  21.79  21.37  6.56  0.0592  <0.001  0.589  C20:1  0.07  0.27  0.12  0.16  0.21  0.05  0.28  0.02  0.15  0.04  0.302  0.001  0.137  C18:2n-6  15.23ns  17.53**  16.28*  15.92†  16.87**  14.73  17.61  15.50  15.14  2.69  0.010  <0.001  0.155  C20:4n-6  5.93  5.29  5.48  6.24  5.47  6.63  4.29  6.48  6.74  1.51  0.212  <0.001  0.424  C18:3n-3  0.37  0.37  0.25  0.33  0.38  0.33  0.64  0.36  0.01  0.06  0.752  <0.001  0.960  C20:5n-3  1.63  1.81  1.52  1.83  1.65  1.77  1.40  1.80  1.94  0.15  0.571  <0.001  0.424  C22:6n-3  13.34ns  11.17*  11.93†  14.27ns  12.42ns  13.89  8.60  14.90  15.10  7.31  0.044  <0.001  0.739  SFA  37.74  36.63  37.43  37.35  36.29  37.70  37.89  36.55  37.13  3.44  0.498  0.065  0.148  MUFA  25.36  27.04  27.04  23.90  26.76  24.86  29.48  24.30  23.69  8.85  0.106  <0.001  0.305  PUFA  36.90  36.33  35.54  38.76  36.95  37.44  32.69  39.07  39.19  6.26  0.141  <0.001  0.872  Total n-6  21.56ns  22.98**  21.84ns  22.32†  22.49*  21.46  22.03  22.16  22.15  0.97  0.021  0.884  0.153  Total n-3  15.34ns  13.35*  13.70*  16.43ns  14.45ns  15.98  10.65  16.99  17.04  7.55  0.0612  <0.001  0.736  n-6/n-3  1.51  2.01  1.77  1.46  1.77  1.42  2.29  1.33  1.36  0.33  0.262  <0.001  0.727  Items  Treatment (Diet)1  Time  SEM  P-value    Control  CUR-20  CUR-40  CUR-60  CUR-80  E-200  1st Month  2nd Month  3rd Month    Diet  Time  Diet × Time  C14:0  0.88  1.14  1.03  0.83  0.95  0.93  1.15  0.82  0.91  0.09  0.282  0.003  0.290  C16:0  23.91  23.28  24.01  23.80  23.15  23.83  25.21  22.52  23.25  1.29  0.547  <0.001  0.569  C18:0  11.70  11.14  11.43  11.36  11.12  11.86  10.26  11.81  12.22  1.64  0.753  <0.001  0.124  C20:0  0.31  0.25  0.23  0.41  0.23  0.28  0.50  0.36  0.00  0.08  0.699  <0.001  0.402  C22:0  0.51  0.40  0.41  0.62  0.44  0.49  0.31  0.42  0.69  0.08  0.250  <0.001  0.951  C16:1  1.18  1.32  1.51  1.24  1.47  1.14  1.71  1.19  1.04  0.31  0.540  0.003  0.043  C17:1  0.90  0.86  0.67  0.88  0.63  1.00  0.20  1.20  1.07  0.33  0.596  <0.001  0.795  C18:1n-9  23.15ns  24.47†  24.68†  21.57ns  24.33ns  22.56  27.22  21.79  21.37  6.56  0.0592  <0.001  0.589  C20:1  0.07  0.27  0.12  0.16  0.21  0.05  0.28  0.02  0.15  0.04  0.302  0.001  0.137  C18:2n-6  15.23ns  17.53**  16.28*  15.92†  16.87**  14.73  17.61  15.50  15.14  2.69  0.010  <0.001  0.155  C20:4n-6  5.93  5.29  5.48  6.24  5.47  6.63  4.29  6.48  6.74  1.51  0.212  <0.001  0.424  C18:3n-3  0.37  0.37  0.25  0.33  0.38  0.33  0.64  0.36  0.01  0.06  0.752  <0.001  0.960  C20:5n-3  1.63  1.81  1.52  1.83  1.65  1.77  1.40  1.80  1.94  0.15  0.571  <0.001  0.424  C22:6n-3  13.34ns  11.17*  11.93†  14.27ns  12.42ns  13.89  8.60  14.90  15.10  7.31  0.044  <0.001  0.739  SFA  37.74  36.63  37.43  37.35  36.29  37.70  37.89  36.55  37.13  3.44  0.498  0.065  0.148  MUFA  25.36  27.04  27.04  23.90  26.76  24.86  29.48  24.30  23.69  8.85  0.106  <0.001  0.305  PUFA  36.90  36.33  35.54  38.76  36.95  37.44  32.69  39.07  39.19  6.26  0.141  <0.001  0.872  Total n-6  21.56ns  22.98**  21.84ns  22.32†  22.49*  21.46  22.03  22.16  22.15  0.97  0.021  0.884  0.153  Total n-3  15.34ns  13.35*  13.70*  16.43ns  14.45ns  15.98  10.65  16.99  17.04  7.55  0.0612  <0.001  0.736  n-6/n-3  1.51  2.01  1.77  1.46  1.77  1.42  2.29  1.33  1.36  0.33  0.262  <0.001  0.727  1Treatments consisted of basal diet without antioxidant supplement (Control); basal diet added 200 ppm alpha-tocopherol acetate (E-200); basal diet added turmeric oleoresin to provide 20 ppm (CUR-20), 40 ppm (CUR-40), 60 ppm (CUR-60), and 80 ppm (CUR-80) curcuminoids. 2The difference was tested with alpha = 0.10. Data of some detectable fatty ≤ 0.4% for all treatments are not shown (C15:0, C23:0, C20:2n-6). The label expressed the difference from the treatments to positive control (E-200) within each type of fatty acid by Dunnett's Test, where “ns,” “†,” “*,” or “**” means no significance (P > 0.1), tending significance (0.05 < P ≤ 0.1), significance (P ≤ 0.05), or high significance (P ≤ 0.01), respectively. View Large The proportion of FA, in particular n-3 PUFA in the thigh meat (Table 7), showed almost no meaningful changes caused by either the E-200 or curcuminoids treatments. The contents of FA in the thigh meat of the present study agreed with those reported by Daneshyar et al. (2011). To the best of our knowledge, the present study has provided the first observations on the FA contents of the meat of slow-growing chickens fed a combination of curcumin removed turmeric oleoresin and tuna oil. The combination of curcumin and long-chain n-3 PUFA might have had synergetic effects, causing a decrease in the accumulation of fat in the tissue (Forman et al., 1997) noting the effects of curcumin or long-chain n-3 PUFA on FA metabolism reported recently (Kang et al., 2013; Fan et al., 2016; Thota et al., 2016). Table 7. Fatty acid profile (g/100 g total FA) of thigh meat of the chickens. Item  Treatment (Diet)1  Time  SEM  P-value    Control  CUR-20  CUR-40  CUR-60  CUR-80  E-200  1st Month  2nd Month  3rd Month    Diet  Time  Diet × Time  C14:0  1.42  1.50  1.49  1.49  1.45  1.47  1.52  1.43  1.46  0.02  0.926  0.089  0.638  C16:0  22.17  21.56  21.86  21.74  22.15  21.96  22.09  21.88  21.52  2.60  0.983  0.480  0.566  C18:0  8.90  8.28  8.95  8.75  8.15  9.70  8.50  9.42  8.39  1.29  0.302  <0.001  0.450  C22:0  0.22  0.24  0.25  0.22  0.25  0.29  0.24  0.18  0.30  0.90  0.832  0.011  0.119  C16:1  3.16  2.87  3.08  2.97  3.57  2.63  3.14  2.73  3.24  0.44  0.354  0.001  0.135  C17:1  0.47  0.51  0.49  0.30  0.34  0.71  0.26  0.62  0.54  0.13  0.180  0.008  0.061  C18:1n-9  28.31  28.61  28.76  28.34  29.86  27.45  28.68  28.05  28.98  2.24  0.088  0.091  0.637  C20:1  0.53  0.54  0.47  0.47  0.46  0.43  0.69  0.06  0.71  0.01  0.222  <0.001  0.399  C18:2n-6  22.35  23.56  22.57  23.33  22.30  22.37  23.10  22.28  22.99  1.84  0.448  0.011  0.192  C18:3n-6  0.10  0.11  0.08  0.06  0.09  0.14  0.20  0.08  0.00  0.01  0.536  <0.001  0.417  C20:4n-6  2.75  2.47  2.54  2.63  2.20  2.95  2.28  2.91  2.63  0.35  0.404  0.001  0.557  C18:3n-3  0.35  0.34  0.37  0.35  0.36  0.36  0.25  0.65  0.14  0.04  0.991  <0.001  0.999  C20:5n-3  1.37  1.47  1.34  1.40  1.34  1.30  1.39  1.32  1.42  0.05  0.687  0.266  0.755  C22:6n-3  6.70  6.83  6.69  6.60  6.36  6.95  6.71  6.73  6.69  1.63  0.954  0.995  0.549  SFA  33.41  32.28  33.17  32.87  32.72  34.08  33.02  33.66  32.30  4.79  0.788  0.057  0.573  MUFA  32.69  32.77  33.02  32.30  34.45  31.41  32.99  31.75  33.62  4.03  0.247  0.001  0.656  PUFA  33.90  34.95  33.81  34.83  32.83  34.51  33.99  34.57  34.03  5.26  0.455  0.568  0.521  Total n-6  25.41  26.30  25.40  26.46  24.77  25.90  25.60  25.85  25.85  2.46  0.419  0.801  0.441  Total n-3  8.52  8.65  8.41  8.37  8.06  8.61  8.37  8.67  8.22  1.74  0.929  0.528  0.437  n-6/n-3  3.03  3.11  3.06  3.20  3.16  3.08  3.11  3.05  3.19  0.22  0.971  0.602  0.467  Item  Treatment (Diet)1  Time  SEM  P-value    Control  CUR-20  CUR-40  CUR-60  CUR-80  E-200  1st Month  2nd Month  3rd Month    Diet  Time  Diet × Time  C14:0  1.42  1.50  1.49  1.49  1.45  1.47  1.52  1.43  1.46  0.02  0.926  0.089  0.638  C16:0  22.17  21.56  21.86  21.74  22.15  21.96  22.09  21.88  21.52  2.60  0.983  0.480  0.566  C18:0  8.90  8.28  8.95  8.75  8.15  9.70  8.50  9.42  8.39  1.29  0.302  <0.001  0.450  C22:0  0.22  0.24  0.25  0.22  0.25  0.29  0.24  0.18  0.30  0.90  0.832  0.011  0.119  C16:1  3.16  2.87  3.08  2.97  3.57  2.63  3.14  2.73  3.24  0.44  0.354  0.001  0.135  C17:1  0.47  0.51  0.49  0.30  0.34  0.71  0.26  0.62  0.54  0.13  0.180  0.008  0.061  C18:1n-9  28.31  28.61  28.76  28.34  29.86  27.45  28.68  28.05  28.98  2.24  0.088  0.091  0.637  C20:1  0.53  0.54  0.47  0.47  0.46  0.43  0.69  0.06  0.71  0.01  0.222  <0.001  0.399  C18:2n-6  22.35  23.56  22.57  23.33  22.30  22.37  23.10  22.28  22.99  1.84  0.448  0.011  0.192  C18:3n-6  0.10  0.11  0.08  0.06  0.09  0.14  0.20  0.08  0.00  0.01  0.536  <0.001  0.417  C20:4n-6  2.75  2.47  2.54  2.63  2.20  2.95  2.28  2.91  2.63  0.35  0.404  0.001  0.557  C18:3n-3  0.35  0.34  0.37  0.35  0.36  0.36  0.25  0.65  0.14  0.04  0.991  <0.001  0.999  C20:5n-3  1.37  1.47  1.34  1.40  1.34  1.30  1.39  1.32  1.42  0.05  0.687  0.266  0.755  C22:6n-3  6.70  6.83  6.69  6.60  6.36  6.95  6.71  6.73  6.69  1.63  0.954  0.995  0.549  SFA  33.41  32.28  33.17  32.87  32.72  34.08  33.02  33.66  32.30  4.79  0.788  0.057  0.573  MUFA  32.69  32.77  33.02  32.30  34.45  31.41  32.99  31.75  33.62  4.03  0.247  0.001  0.656  PUFA  33.90  34.95  33.81  34.83  32.83  34.51  33.99  34.57  34.03  5.26  0.455  0.568  0.521  Total n-6  25.41  26.30  25.40  26.46  24.77  25.90  25.60  25.85  25.85  2.46  0.419  0.801  0.441  Total n-3  8.52  8.65  8.41  8.37  8.06  8.61  8.37  8.67  8.22  1.74  0.929  0.528  0.437  n-6/n-3  3.03  3.11  3.06  3.20  3.16  3.08  3.11  3.05  3.19  0.22  0.971  0.602  0.467  1Treatments consisted of basal diet without antioxidant supplement (Control); basal diet added 200 ppm alpha-tocopherol acetate (E-200); basal diet added turmeric oleoresin to provide 20 ppm (CUR-20), 40 ppm (CUR-40), 60 ppm (CUR-60), and 80 ppm (CUR-80) curcuminoids. Data of some detectable fatty ≤ 0.50% for all treatments are not shown (C15:0, C24:1, C20:2n-6). View Large Regarding the TBARS values in the breast and thigh meat, the individual treatments did not affect the proportion of total n-3 PUFA during the period of frozen storage. The proportions of C18:3n-3 (α-linolenic acid), C20:5n-3 (EPA), and DHA in the breast meat increased (P < 0.001) during the 3 mo of storage at −20°C. The higher proportions of EPA and DHA found in the frozen breast meat agreed with Zymon et al. (2007) who also found a tendency towards higher contents of EPA and DHA in frozen veal stored for 3 mo at −18°C. A study comparing slow-growing chickens (a similar breed to that in the present study) with commercial broilers has revealed that the PUFA content (mg/g) of the breast and thigh meat of the “Korat Meat Chicken” increased, while that of the broilers decreased after 8 mo of frozen storage (Jirawat Yongsawatdigul, SUT, Nakhon Ratchasima, personal communication). This could suggest that there were certain changes during frozen storage rather than autoxidation and hydrolysis. In the present study, no changes occurred in the EPA or DHA content of the thigh meat during 3 mo of frozen storage. Horbanczuk et al. (2015) showed that the DHA and total PUFA content of meat from ostriches fed 4 or 8% linseed oil decreased, especially between 61 to 120 d of frozen storage at −20°C, but the FA profile of the meat was not influenced up to 60 d, with different muscles having varied responses. In conclusion, dietary supplementation with curcuminoids in the form of the curcumin removed turmeric oleoresin showed positive effects on FCR, breast fillet weight, and the yellowness of the chicken skin. The curcuminoids exhibited antioxidant and pro-antioxidant effects that were not dose dependent. The present study has shown that a suitable level of curcuminoids for supplementing the diets of slow-growing chickens was 60 mg/kg. 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Poultry ScienceOxford University Press

Published: Mar 1, 2018

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