Fatty acid profile, oxidative stability, and sensory properties of breast meat from turkeys fed diets with a different n-6/n-3 PUFA ratio
Abstract
The objective of this study was to determine the effect of diets with a different n-6/n-3 PUFAs ratio (7.31, 4.43, and 0.99), resulting from the addition of different dietary oils: soybean, rapeseed, and linseed (diets S, R, and L, respectively), on the fatty acid (FA) profile, oxidative status, and sensory properties of turkey breast meat. After 15 wk of feeding, breast meat yield and chemical properties of the meat were similar in all groups. Raw breast meat of R turkeys had a significantly higher content of all-trans-retinol and α-tocopherol, compared with S and L. The physicochemical properties of breast meat, including pH, color, drip loss, and cooking loss, did not differ significantly. Cooked meat samples differed significantly with respect to the concentrations of oleic acid, linoleic acid (S and R>L), and linolenic acid (S and R<L). Compared with S and R, breast meat of L turkeys was characterized by higher concentrations of total PUFAs (35.1 vs. 30.1 and 29.3%), a significantly lower n-6/n-3 PUFAs ratio (1.51 vs. 5.43 and 5.07%) and a higher thiobarbituric acid reactive substances content (TBARS; 31.9 vs. 26.4 and 26.7 nmol/g). After 4 months of deep-freeze storage the n-6/n-3 PUFAs ratio did not deteriorate. It may be concluded that replacing soybean oil with linseed oil, but not with rapeseed oil, increased the proportion of PUFAs in the total FAs pool and improved the n-6/n-3 PUFAs ratio, yet it also adversely affected the sensory properties and oxidative stability of meat. Both raw and stored breast meat from L turkeys was susceptible to oxidative changes, as manifested by the significantly higher TBARS concentrations (17.07 and 81.06) compared with those of the S group (10.91 and 53.00 nmol/g, respectively).
Practical applications: Studies investigating the possibility of increasing the health benefits of poultry meat have been performed mostly on broilers, while the problem remains poorly researched in turkeys. Our findings show that linseed oil, in contrast to rapeseed oil, is a good source of PUFAs, in particular n-3 PUFAs, that can be effectively transferred from feed to carcass lipids. However, desirable changes in the fatty acid profile are accompanied by increased susceptibility to lipid oxidation and deterioration of the sensory properties of meat. Thus, the linseed oil content of turkey diets should be reduced, or diets supplemented with linseed oil should be fed for shorter periods of time to alleviate the negative effects of linseed oil on the sensory attributes and oxidative status of meat.
Abbreviations:
BW, body weight; FA, fatty acid; TBARS, thiobarbituric acid reactive substances
Introduction
Modification of the fatty acid (FA) composition of animal products, aimed at improving the n-6/n-3 PUFA ratio in the human diet, is an important consideration in the production of health-promoting foods 1. Research results show that the consumption of PUFAs, especially n-3 PUFAs plays an important role in cardiovascular disease prevention 2, and that changes in the FA profile of livestock diets lead to changes in the blood FA composition in consumers of animal products, comparable to those noted under the Cretan diet 3. In developed countries, the major sources of n-3 PUFAs are meat and meat products 4, including poultry products which account for over 40% of the total meat consumption 5. Therefore, numerous attempts have been made to supplement diets for broiler chickens and laying hens with vegetable oils with an increased n-3 PUFA content 6, 7.
In modern dietary trends, consumption of turkey meat is indicated as an adequate source of essential FAs with a low content of total lipids. However, the n-3 PUFA content can be considered too low to achieve a healthy n-6/n-3 PUFA ratio when birds are fed on standard diets. Poultry diets are often enriched with fats and high-fat feed components for economic reasons, since an increase in metabolizable energy (ME) concentrations in diets to approximately 12–13 MJ of ME/kg of feed helps fast-growing birds reach their full genetic potential 8.
Early studies used fish oil 9, 10 as the source of n-3 PUFA, while recent studies have used vegetable oil or seeds 11-14 containing linolenic acid (ALA; C18:3 n-3) to enrich meat with PUFA, particularly with n-3 PUFA. Vegetable sources of n-3 PUFAs seem to be efficient sources in terms of the modification of fat composition, especially dietary flaxseed oil has been found to be effective in increasing the n-3 PUFA content of poultry meat 13-17. The physicochemical properties and the FA profile of fat added to poultry diets affect the bodily functions of birds as well as carcass abdominal fat content 18, the lipid composition of meat 19, sensory attributes, and the oxidative stability of lipid fractions 20. Meat with high content of unsaturated FAs can be more susceptible to oxidation 14, 21-24. Lipid oxidation in cooked meat shows a significant linear increase as PUFA concentrations in raw meat increase 14, and the values of lipid oxidation indices in meat are higher if birds are fed vegetable oils instead of animal fats 25. The effect of dietary oils containing a high proportion of n-3 PUFA on the FA composition and meat quality has been studied in chicken, with inconsistent findings. The oxidative stability of stored chicken meat decreases when broilers are fed soybean oil or linseed oil as a substitute for animal fats 24, 26. In some cases 11, 27, no effects on meat quality parameters were observed, but in other 10, adverse effects on odor and flavor/taste of meat were detected. Data regarding modifications of muscle lipid composition in young turkeys and the shelf-life of the resulting turkey meat products are scant and insufficient.
Therefore, the objective of this study was to determine the effect of altering the FA profile (including the n-6/n-3 PUFA ratio) of turkey breast muscles by replacing soybean oil with rapeseed oil or linseed oil in turkey diets on the oxidative status and sensory properties of turkey breast meat.
Materials and methods
Birds and housing
The experiment was carried out at the Research Laboratory of the Department of Poultry Science, University of Warmia and Mazury in Olsztyn, according to the guidelines of the Local Animal Experimentation Ethics Committee. A total of 625 one-day-old heavy-type Large White BIG-6 female turkeys, sexed at a local commercial hatchery, were randomly assigned to three feeding groups (14 replications). The turkeys were kept in pens (15 birds per pen, 4 m2) on litter in a building with a controlled environment, equipped with central heating. The poults were vaccinated against turkey rhinotracheitis (TRT) by spray application at 1 day of age. The initial body weight (BW) of 1-day-old poults was 61 g.
The temperature and lighting program was consistent with the recommendations of Aviagen, Inc. 28. The brooder temperature was set at 35°C, and it was gradually decreased as needed. RT was set at 28°C on the day of placement, and it was subsequently reduced by 2°C per week. A visual inspection of all birds was performed on a daily basis. Temperature and humidity were monitored daily at 8.00 a.m. and 3.00 p.m. The following lighting program was adopted: 24 h light with an intensity of 100 lx in the first 72 h, followed by 18 h light per day until day 14, and 16 h light per day until the end of the growing period. Light intensity was reduced to 5 lx between 3 and 7 days, and it was gradually increased to 15 lx as of week 5. The birds had free access to feed and water. The trial was conducted to 105 days of age.
Diets
Commercially available soybean oil, rapeseed oil, and linseed oil (from Grodzisk Wlk. Co., Poland) were used in this experiment (dietary S, R, and L groups, respectively). Feed mixtures were prepared in the Agrocentrum feed mill in Kaleczyn, Poland. The diets were isoenergetic and isonitrogenous, and they were formulated using least-cost linear programming software to meet the nutrient requirements of turkeys, as recommended by British United Turkeys Ltd. 29. The amount of oils in the diets was increased from 2% in the first 4 wk of feeding to 6% at the final stage of feeding (from 14 to 15 wk) as described in the work of Jankowski et al. 30 where the performance trial was presented and discussed. All diets were equally supplemented with vitamin E (dl-α-tocopheryl acetate) and selenium (sodium selenite) at amount 54 and 0.3 mg/kg of diets, respectively. Vitamin A (all-trans-retinol acetate) was supplied at amount 15 000 IU/kg of diet.
The addition of different vegetable oils to experimental diets changed their FA profiles (Table 1). The most pronounced differences in the FA profile between groups S, R, and L were found for the following four FAs: C16, C18:1cis 9, C18:2, and C18:3. Diet S, compared with diets R and L, had the highest content of palmitic and linoleic acids: 12.6% versus 9.88% and 10.1%, and 49.7% versus 33.0% and 30.3%, respectively. Diet R, in comparison with diets S and L, had the highest concentrations of oleic acid (41.4% vs. 23.1% and 21.7%, respectively). Diet L, compared with diets S and R, was characterized by the highest content of linolenic acid (30.6% vs. 7.02% and 7.96%, respectively). In comparison with diet S, diet R had a lower proportion of SFAs (13.9% vs. 17.4%) and PUFAs (40.9% vs. 56.8%), particularly n-6 PUFAs, in the total FA pool (33.0% vs. 49.7%). In diet L, the proportions of n-6 and n-3 PUFAs were similar (30.3% and 30.6%, respectively). The n-6/n-3 PUFA ratio in diet L (0.99) was over sevenfold and fourfold lower than in diets S (7.31) and R (4.43), respectively.
| Fatty acid | Experimental group | ||
|---|---|---|---|
| S | R | L | |
| C14 Myristic | 0.20 | 0.26 | 0.35 |
| C15 Pentadecanoic | 0.04 | 0.04 | 0.05 |
| C16 Palmitic | 12.6 | 9.88 | 10.1 |
| C16:1 Palmitoleic | 0.26 | 0.25 | 0.24 |
| C17 Margaric | 0.11 | 0.09 | 0.10 |
| C17:1 Margaroleic | 0.06 | 0.06 | 0.06 |
| C18:0 Stearic | 3.62 | 2.80 | 3.86 |
| C18:1 cis 9 Oleic | 23.1 | 41.4 | 21.7 |
| C18:1 cis 11 Elaidic | 1.71 | 2.10 | 1.43 |
| C18:2 Linoleic | 49.7 | 33.0 | 30.3 |
| C18:3 Linolenic | 7.02 | 7.96 | 30.6 |
| C20:0 Arachidic | 0.48 | 0.52 | 0.41 |
| C20:1 Gondoic | 0.68 | 1.02 | 0.42 |
| C22:0 Behenic | 0.38 | 0.30 | 0.24 |
| C22:1 Erucic | 0.00 | 0.29 | 0.00 |
| SFA | 17.4 | 13.9 | 15.1 |
| UFA | 82.6 | 86.1 | 84.9 |
| MUFA | 25.8 | 45.2 | 24.0 |
| PUFA | 56.8 | 40.9 | 60.9 |
| n-6 PUFA | 49.7 | 33.0 | 30.3 |
| n-3 PUFA | 7.02 | 7.96 | 30.6 |
| n-6/n-3 PUFA ratio | 7.31 | 4.43 | 0.99 |
Sample collection
After 15 wk of feeding, eight birds representing an average BW of each group (24 birds in total) were slaughtered at a processing plant, 8 h after feed withdrawal. The birds were electrically stunned (400 mA; 350 Hz), and they were hung on a shackle line and exsanguinated by a unilateral neck cut severing the right carotid artery and jugular vein. After a 3-min bleeding period, the birds were scalded at 61°C for 60 s, defeathered in a rotary drum picker for 25 s, and manually eviscerated. Following evisceration, whole carcasses were air pre-chilled at 12°C for 30 min, air chilled and stored at 4°C, and then hand-deboned on a cone at 24 h postmortem. At the time of deboning (24 h postmortem), the right pectoralis major subsamples were used to determine meat color and drip loss. The left pectoralis major subsamples were used to determine pH values at 1 and 24 h postmortem, and weight loss during cooking (24 h postmortem). The remaining meat from the left breast muscles was vacuum-packaged, frozen at −20°C, and stored for further analysis (chemical composition, all-trans-retinol and α-tocopherol content, FA profile, sensory properties, lipid oxidation). The FA profile and changes in the oxidative stability of lipids were determined in raw, cooked, and freeze-stored (−20°C, 4 months) breast meat samples.
Analysis
The pH of breast muscles was measured at 1 and 24 h postmortem (pH-meter, Testo 206–pH2 model, Testo AG, Lenzkirch, Germany).
Meat color was determined on breast muscle samples by the optical reflection method, in the CIELAB system 31 with L* (lightness, lower values indicate a darker color), a* (redness, higher positive values indicate a higher contribution of redness), and b* (yellowness, higher values indicate a higher contribution of yellowness), using a MiniScan XE Plus color difference meter (Hunter Associates Laboratory, Inc., Reston, VA, USA). The average of three readings taken from the cross-section of the right breast muscle free from color defects, bruising, and hemorrhages was recorded.
To determine drip loss, breasts samples were weighed, stored in plastic bags (4°C), and weighed again after 48 h of cold storage. Drip loss was calculated as: (drip loss/initial muscle weight) × 100. To estimate cooking losses, breast samples were weighed (wtm), cooked in a microwave oven (12 min, 480 W), and weighed again (wtc). Cooking loss was calculated as (wtm − wtc)/wtm × 100.
Approximately 1 wk after slaughter, the content of dry matter, ash, crude protein, and fat of meat samples was determined in triplicate, using AOAC 32 methods 934.01, 942.05, 976.05, and 920.39, respectively.
The content of α-tocopherol in meat samples was determined by HPLC (Shimadzu, Japan), as described by Rettenmaier and Schüep 33. The external standard used was all-rac-α-tocopherol (Sigma, Switzerland).Vitamin A was assayed by HPLC according to Cuesta Sanz and Castro Santa-Cruz 34. The obtained values were expressed as micrograms per gram of meat (µg/g).
For FA analysis, minced feed and meat samples were extracted with a mixture of chloroform and methanol (2:1 v/v), as described by Folch et al. 35, esterified by the method of Peisker 36, and subjected to a gas chromatographic analysis using a 6890 N gas chromatograph (Agilent Technologies, Inc., Palo Alto, USA) equipped with a FID. Column (capillary, 0.32 mm × 30 m), injector and detector temperatures were 180, 225, and 250°C, respectively. The flow rate of helium carrier gas was 0.7 cm3/min. FAs were identified based on their retention times, and were expressed as a percentage of the sum of identified FAs (% w/w). All analyses were performed in duplicate. Based on the performed analyses, the content of saturated fatty acids (SFA), MUFA, and PUFA as well as the n-6/n-3 PUFA ratio were determined.
Approximately 1 wk after slaughter, a sensory analysis of breast meat was conducted at the Department of Commodity Science and Animal Raw Material Processing, University of Warmia and Mazury. Meat samples were cooked in a steam-convection oven (BECK FCV 4 EDS, GmbH, Jagsthausen, Germany) for 30 min, until the minimum temperature of 75°C was reached inside the muscle. After cooking the meat samples were evaluated by a team of seven trained panelists, based on a 9-point hedonic scale (1 – extremely dislike, 9 – extremely like), according to ISO 4121 37.
Changes in the oxidative stability of lipids were determined using the method proposed by Draper and Hadley 38, based on the thiobarbituric acid reactive substances (TBARS) content of meat. Absorbance was measured with a Specord 40 spectrophotometer (Analityk Jena AG), and TBARS levels were expressed as nmol of malondialdehyde (MDA) per g of meat.
Statistical analysis
The STATISTICA software package version 8.0 39 was used to determine whether variables differed among treatment groups. One-way ANOVA was applied to assess the effects of the inclusion of different types of dietary vegetable oils on the parameters analyzed in the study, except for the assessment of changes in breast meat FA profile during 4-month storage. In the latter case, two-way ANOVA was performed to determine the effects of the type of dietary oil (soybean, rapeseed, and linseed), the treatment applied (raw or stored meat), and the interaction between these two factors (D × S) 40. When the ANOVA indicated significant treatment effects, means were separated using Duncan's multiple range test. In the Tables, results are presented as mean values with pooled standard errors. Data were checked for normality before the statistical analysis was performed. Differences were considered to be significant at p ≤ 0.05.
Results
Chemical composition and physicochemical properties of raw breast meat
Breast meat yield was similar in all groups, and it exceeded 22% of the total BW (Table 2). No significant differences were found in the content of dry matter, fat, protein, and ash in breast meat between groups. The physicochemical properties of breast meat, including pH, color, drip loss, and cooking loss, did not differ significantly between groups. Raw breast meat of group R turkeys had a significantly higher content of all-trans-retinol and α-tocopherol (p = 0.015 and p = 0.029, respectively), compared with groups S and L (Fig. 1).
| Experimental groupa) | SEM | p-value | |||
|---|---|---|---|---|---|
| S | R | L | |||
| Relative weight (% BW) | 22.7 | 22.4 | 22.1 | 0.208 | 0.531 |
| Chemical composition (%) | |||||
| Dry matter | 26.3 | 26.7 | 26.2 | 0.027 | 0. 104 |
| Fat | 0.79 | 0.81 | 0.70 | 0.033 | 0.364 |
| Protein | 23.7 | 23.7 | 23.6 | 0.065 | 0.699 |
| Ash | 1.19 | 1.19 | 1.18 | 0.005 | 0.724 |
| Meat pH | |||||
| After 1 h | 5.84 | 5.81 | 5.81 | 0.009 | 0.331 |
| After 24 h | 5.92 | 5.88 | 5.88 | 0.020 | 0.672 |
| Color | |||||
| Minolta lightness, L* | 54.7 | 53.9 | 53.5 | 0.645 | 0.755 |
| Minolta redness, a* | 5.8 | 5.4 | 5.0 | 0.307 | 0.581 |
| Minolta yellowness, b* | 11.7 | 12.7 | 11.4 | 0.502 | 0.560 |
| Drip loss (%) | 1.42 | 1.89 | 1.87 | 0.162 | 0.419 |
| Cooking loss (%) | 18.2 | 19.2 | 18.9 | 0.365 | 0.510 |
- a) Data represent mean values of eight samples per treatment.
Retinol and α-tocopherol content (µg/g) of raw breast meat in turkeys at 105 days of age fed diets containing soybean oil, rapeseed oil, and linseed oil (dietary S, R, and L groups, respectively). Data represent mean values of eight samples per treatment. (a,b) Means within a column with different letters differ (p<0.05).
Fatty acid profile and sensory properties of cooked breast meat
The FA composition of cooked breast meat from turkeys fed diets with different oil types is presented in Table 3. Significant differences were reported for oleic acid (S and R>L, p>0.001), linoleic acid (S and R>L, p<0.001) and linolenic acid (S and R<L, p>0.001). The inclusion of dietary linseed oil significantly increased the percentage of eicosapentaenoic acid and decreased the concentration of gondoic acid (in both cases p<0.001 vs. the other groups). A significantly higher content of myristic acid and gondoic acid in the FA profile followed the dietary inclusion of rapeseed oil, in comparison with groups S and L. The major FA proportion, including MUFA and PUFA of cooked breast meat from groups S and L were similar, despite significant differences in the FA profile of both diets. Compared with groups S and R, breast meat from group L turkeys was characterize by a lower proportion of MUFA (p>0.001) and a higher proportion of PUFA (p<0.001) in the total FA pool. A closer analysis revealed that meat from group L turkeys had a lower n-6 PUFA content and a higher n-3 PUFA content (p>0.001 vs. groups S and R). The n-6/n-3 PUFA ratio in the meat of group L turkeys was over threefold lower (p>0.001), in comparison with groups S and R (1.51 vs. 5.43 and 5.07, respectively). The TBARS content of cooked breast meat was significantly (p = 0.004) higher in group L than in groups S and R (31.9 vs. 26.4 and 26.7, respectively). The results of a sensory evaluation of meat are illustrated in Fig. 2. Meat from turkeys fed a diet supplemented with soybean oil (group S) received the highest scores for sensory properties. Sensory scores were significantly lower in group R (6.73 vs. 7.87, p<0.001), and lowest in group L (4.07, p>0.001).
| Fatty acid | Experimental groupa) | SEM | p-value | ||
|---|---|---|---|---|---|
| S | R | L | |||
| C14 Myristic | 0.62b | 0.73a | 0.58b | 0.018 | 0.001 |
| C14:1 Myristoleic | 0.16 | 0.18 | 0.17 | 0.007 | 0.313 |
| C15 Pentadecanoic | 0.16 | 0.15 | 0.16 | 0.007 | 0.177 |
| C16 Palmitic | 23.6 | 22.7 | 23.1 | 0.205 | 0.224 |
| C16:1 Palmitoleic | 3.24 | 2.84 | 3.27 | 0.219 | 0.698 |
| C17 Margaric | 0.18 | 0.19 | 0.19 | 0.006 | 0.942 |
| C17:1 Margaroleic | 0.12 | 0.13 | 0.14 | 0.010 | 0.784 |
| C18:0 Stearic | 8.64 | 8.54 | 9.66 | 0.221 | 0.063 |
| C18:1 CIS9 Oleic | 30.1a | 31.8a | 25.4b | 0.696 | <0.001 |
| C18:1 CIS11 Elaidic | 2.54b | 2.77a | 1.88c | 0.094 | >0.001 |
| Total C18:1 | 32.7a | 34.5a | 27.2b | 0.776 | >0.001 |
| C18:2 Linoleic | 22.5a | 21.5a | 19.4b | 0.382 | <0.001 |
| C18:3 Linolenic | 4.11b | 4.05b | 12.4a | 0.884 | >0.001 |
| C20:0 Arachidic | 0.14 | 0.15 | 0.14 | 0.005 | 0.624 |
| C20:1 Gondoic | 0.41b | 0.48a | 0.25c | 0.022 | >0.001 |
| C20:2 Eicosadienoic | 0.28 | 0.28 | 0.37 | 0.039 | 0.667 |
| C20:4 Arachidonic | 2.61a | 2.70a | 1.47b | 0.191 | 0.007 |
| C20:5 Eicosapentaenoic | 0.27b | 0.35b | 0.97a | 0.083 | >0.001 |
| C22:6 Docosahexaenoic | 0.26 | 0.40 | 0.51 | 0.046 | 0.075 |
| SFA | 33.3 | 32.5 | 33.8 | 0.320 | 0.248 |
| UFA | 66.6 | 67.5 | 66.2 | 0.320 | 0.248 |
| MUFA | 36.6a | 38.2a | 31.1b | 0.867 | >0.001 |
| PUFA | 30.1b | 29.3b | 35.1a | 0.712 | <0.001 |
| n-6 PUFA | 25.1a | 24.2a | 20.9b | 0.541 | >0.001 |
| n-3 PUFA | 4.64b | 4.80b | 13.8a | 0.970 | >0.001 |
| n-6/n-3 PUFA ratio | 5.43a | 5.07a | 1.51b | 0.401 | >0.001 |
| TBARS [nmol/g] | 26.4b | 26.7b | 31.9a | 0.814 | 0.004 |
- a) Data represent mean values of 8 samples per treatment. a–cMeans with different superscripts within the same line differ significantly (p<0.05).
Sensory properties of cooked breast meat in turkeys fed diets containing soybean oil, rapeseed oil, and linseed oil (dietary S, R, and L groups, respectively). Nine point hedonic scale (1 – extremly dislike, 9 – extremly like). Data represent mean values of eight samples per treatment. (a–c) Means within a column with different letters differ (p<0.05).
Effect of storage conditions on the fatty acid profile and TBARS content of breast meat
Storage conditions affected the percentage content of all acids in the FA profile, except for linolenic acid (Table 4). In comparison with raw breast meat, regardless of oil type, meat storage for 4 months at −20°C significantly decreased MUFA content and significantly increased PUFA content, including n-6 and n-3 PUFA (p<0.001). Two-way ANOVA revealed that meat storage significantly reduced SFA concentrations and increased the total UFA content of meat from turkeys fed diets supplemented with soybean oil and linseed oil, while such changes in the FA profile were not reported for rapeseed oil. In the latter case, storage did not affect the percentages of SFA and UFA in the FA profile. A significant interaction between the two main factors was also observed with respect to the n-6/n-3 PUFA ratio in the breast meat of turkeys. In group S (raw and frozen meat), storage at −20°C significantly decreased the n-6/n-3 PUFA ratio, but such changes were not observed in breast meat samples collected in groups R and L. The MUFA and PUFA proportion, and n-6/n-3 PUFA ratio of stored breast meat from groups S and L were similar, despite significant differences in the FA profile of raw meat. The TBARS content of raw meat from group S turkeys was significantly lower (p>0.001) than in the other groups (Fig. 3). In frozen meat, a significantly (p>0.001) higher TBARS content was noted in group L versus groups S and R.
| Fatty acid | C14-C18:0 | ∑C18:1a) | C18:2 | C18:3 | ∑C20b) | C20:4 | C20:5 | C22:6 | SFA | UFA | MUFA | PUFA | ∑n-6 | ∑n-3 | n-6/n-3 ratio |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Group | |||||||||||||||
| SR | 36.3a | 33.7 | 22.3 | 3.79b | 0.90 | 2.48 | 0.32 | 0.27c | 32.9a | 67.1c | 37.6 | 29.4 | 24.8 | 4.39 | 5.71a |
| SF | 32.2c | 33.3 | 23.9 | 4.65b | 1.15 | 3.12 | 0.35 | 0.45b | 29.0bc | 71.0ab | 37.0 | 34.0 | 27.0 | 5.74 | 4.73b |
| RR | 34.1b | 38.0 | 20.6 | 3.91b | 1.00 | 1.94 | 0.25 | 0.23c | 30.3b | 69.7b | 42.5 | 27.2 | 22.5 | 4.39 | 5.13b |
| RF | 31.8c | 35.3 | 22.6 | 4.36b | 1.23 | 2.90 | 0.39 | 0.48b | 28.9bc | 71.1ab | 38.8 | 32.3 | 25.5 | 5.54 | 4.63b |
| LR | 34.0b | 28.3 | 19.7 | 15.6a | 0.59 | 0.93 | 0.63 | 0.26c | 30.2b | 69.8b | 32.5 | 37.3 | 20.7 | 16.47 | 1.26c |
| LF | 32.4c | 26.6 | 19.9 | 15.2a | 0.83 | 1.54 | 1.18 | 0.67a | 29.0c | 71.0a | 30.4 | 40.6 | 21.4 | 17.3 | 1.24c |
| SEM | 0.281 | 0.656 | 0.301 | 0.839 | 0.036 | 0.144 | 0.056 | 0.030 | 0.258 | 0.258 | 0.716 | 0.758 | 0.427 | 0.897 | 0.292 |
| p-value | 0.008 | 0.242 | 0.095 | 0.042 | 0.907 | 0.665 | 0.721 | 0.040 | <0.001 | <0.001 | 0.292 | 0.497 | 0.155 | 0.656 | 0.017 |
| Oil | |||||||||||||||
| S | 33.9a | 33.5b | 23.2a | 4.28b | 1.04b | 2.85a | 0.34b | 0.37b | 30.7a | 69.3b | 37.3b | 32.0b | 26.1a | 5.16b | 5.15a |
| R | 32.7b | 36.4a | 21.8b | 4.19b | 1.14a | 2.53a | 0.34b | 0.38b | 29.5b | 70.5a | 40.2a | 30.3c | 24.4b | 5.10b | 4.82b |
| L | 33.1b | 27.3c | 19.8c | 15.3a | 0.73c | 1.28b | 0.94a | 0.49a | 29.5b | 70.5a | 31.3c | 39.2a | 21.1c | 17.0a | 1.25c |
| p-value | 0.007 | <0.001 | <0.001 | <0.001 | <0.001 | <0.001 | <0.001 | 0.031 | <0.001 | <0.001 | <0.001 | <0.001 | <0.001 | <0.001 | <0.001 |
| Treatment | |||||||||||||||
| Raw | 34.8a | 33.0a | 20.9b | 7.99 | 0.82b | 1.77b | 0.41b | 0.25b | 31.2a | 68.8b | 37.3a | 31.6b | 22.7b | 8.65b | 3.97a |
| Frozen | 32.1b | 31.7b | 22.1a | 8.06 | 1.07a | 2.53a | 0.65a | 0.53a | 29.0b | 71.0a | 35.4b | 35.6a | 24.7a | 9.53a | 3.53b |
| p-value | <0.001 | 0.005 | 0.001 | 0.153 | <0.001 | <0.001 | <0.001 | <0.001 | <0.001 | <0.001 | 0.011 | <0.001 | <0.001 | <0.001 | <0.001 |
- a) C18:1 CIS9 and C18:1 CIS11.
- b) C20:1, C20:2, and C20:3.
TBARS concentrations (nmol/g) in raw and freeze-stored breast meat in turkeys fed diets containing soybean oil, rapeseed oil and linseed oil (dietary S, R, and L groups, respectively). Data represent mean values of eight samples per treatment. (a,b) Means within a column with different letters differ (p<0.05).
Discussion
In the present study, we analyzed the effect of modified lipid composition of turkey diets on the chemical composition and quality of breast meat. The inclusion of different vegetable oils (soybean, rapeseed, and linseed) in diets caused changes in their FA profile.
In soybean oil, linoleic acid accounts for over 50% of the total FA pool, while linolenic acid content is relatively low (<10%) 18, 19, 41. Rapeseed oil has a very high oleic acid content and a proportionally lower linoleic acid content 20, 42. Linseed oil, compared with soybean oil, contains substantially less linoleic acid and significantly more linolenic acid 15, 18, 41. Rapeseed oil, in comparison with linseed oil, has an over twofold higher oleic acid content, a similar linoleic acid content, and a much lower linolenic acid content 16, 24.
The diet with soybean oil had higher concentrations of palmitic, stearic, and linoleic acids, the diet with rapeseed oil had a higher oleic acid content, and the diet with linseed oil had higher levels of linolenic acid, which corroborates the findings of other authors. The replacement of soybean oil with rapeseed oil decreased the proportion of PUFAs, including n-6 PUFAs in the total FA pool, leading to a decrease in the n-6/n-3 PUFA ratio from 7.31 to 4.43. Diet supplementation with linseed oil increased the proportion of n-3 PUFAs, thus decreasing the n-6/n-3 PUFA ratio to 0.99. In other experiments, the n-6/n-3 PUFA ratio was 6.04–9.63 in diets with soybean oil 19, 41, 3.77 in diets with rapeseed oil 24, and 1.20–2.07 in diets with linseed oil 19, 24, 41.
Results of many experiments indicate that n-3 PUFA-enriched diets increase the deposition of these FAs in muscles 21-24, 43. Rapeseed oil is also considered a good source of n-3 PUFA which expected to increase the diet and meat content of n-3 PUFAs 9, 42. In the present study, rapeseed oil used as a substitute for soyabean oil contributed to a significant increase in the total pool of unsaturated fatty acids (UFAs) in lipids of raw breast meat, mostly due to an increase in the concentrations of monounsaturated C18 FAs (oleic and elaidic). As a result, total PUFAs level was lower, and a decrease in the proportion of n-6 PUFAs significantly improved the n-6/n-3 PUFA ratio (5.13), compared with turkeys receiving soyabean oil (5.71). However, the MUFA and PUFA proportion, and n-6/n-3 PUFA ratio of cooked and stored breast meat of turkeys fed diets with soyabean oil and rapeseed oil were similar, despite significant differences in the FA profile of both diets. The changes in the FA profile, noted in the present experiment, correspond to those observed by other authors in chickens 9, 26, 44 and turkeys 45 fed rapeseed oil-supplemented diets. In comparison with the cited studies, in the present experiment the proportion of total PUFAs was lower and the n-6/n-3 PUFA ratio was similar (above 5) in raw meat. With regard to numerous indicators, including the concentrations of MUFAs and n-6 and n-3 PUFAs, our results are consistent with the findings reported for broilers fed diets supplemented with rapeseed oil by Lopez-Ferrer et al. 9 and confirmed by Salamatdoustnobar et al. 44.
Numerous studies involving chickens show that linseed (or flaxseed oil) is a valuable source of n-3 PUFAs that can be effectively transferred from feed to carcass lipids 9, 13, 15, 16, 24. Similar results were obtained in the present study of growing turkeys. Diet supplementation with linseed oil significantly increased the proportion of n-3 PUFA in the FA profile of cooked meat. In comparison with turkeys fed soybean oil, the proportion of n-3 PUFAs increased from 4.64 to 13.8%, and the n-6/n-3 PUFA ratio decreased from 5.43 to 1.51.
A lower dietary n-6/n-3 PUFA ratio provides health benefits to consumers. In typical Western diets, the n-6/n-3 PUFA ratio is high, ranging between 10:1 and 30:1 46, while it should remain in the 1:1–1:4 range 47. The ideal dietary n-6/n-3 PUFA ratio, recommended by an international panel of lipids experts, is approximately 2:1 48. In the present experiment, the ideal n-6/n-3 PUFA ratio was achieved in cooked breast meat from turkeys fed a linseed oil-supplemented diet. A statistical comparison of the FA composition of unprocessed and cooked breast muscles has not been provided, as ample authors did not observe differences in the FA profile of raw and cooked poultry edible meat when it was cooked at lower temperatures, to 80–90°C 23, 49. In the present experiment, turkey breast meat was cooked at 75°C, and the data obtained confirmed the above observations. It has been reported that cooking at low temperatures can cause fat losses of similar magnitude in all families of FAs, while more aggressive thermal processes may cause harsh PUFA losses which can be observed in an altered FA profile 23.
In the present experiment, no significant differences were found in the breast meat yield and chemical or physicochemical properties of raw breast meat between groups. Similarly, Crespo and Esteve-Garcia 15 and Cortinas et al. 14 observed that breast meat yields of chicken were not modified by dietary PUFA level. In study by Ebeid et al. 43, no differences were also found in the content of dry matter, total protein, and crude ash in the breast muscles. Contrary to the present findings, Crespo and Esteve-Garcia 50 found that different dietary fats had a significant effect on the ash content of thigh- and breast muscle.
The content of intramuscular fat plays an important role in meat quality (flavor and juiciness) of chickens. Some authors 9, 15, 24 showed that the dietary PUFA level does not influence intramuscular lipid content of breast. The lack of effect of fat source on crude fat can be related to the moderate enrichment of muscles, because Ajuyah et al. 51 found a higher fat content in breast with increasing levels of PUFA in the diet. By contrast, others 23, 52 found lower lipid content of breast muscle of chickens fed diets enriched with polyunsaturated oils. The concentrations of the above components in the whole carcass of chickens fed diets supplemented with different vegetable oils did not differ significantly 18. The breast muscle content of the carcass and the chemical composition of breast muscles, determined in the present study, agree with the results cited above.
The analyzed physicochemical properties of meat, including pH, color, drip loss, and cooking loss, were similar regardless of total PUFA and n-3 PUFA levels in experimental diets and breast meat. Similarly in study Qi et al. 53 no differences were found in pH ultimate and drip loss of breast muscle due to dietary n-6/n-3 PUFA. Results of some studies indicate that dietary lipid source or n-6/n-3 PUFA ratio did not influence the functional properties of raw chicken meat while it modified its color characterized in scale L*, a*, and b*. For example, Bianchi et al. 54 reported that dietary use of vegetable oils produced darker and a higher yellowness of breast meat than animal fats. Meat color is one of the first characteristics noted by customers, especially in boneless products and is also an indicator of meat quality. In study by Qi et al. 53, there was a strong impact of decreasing n-6/n-3 on the color of breast muscle in chicken. L* values increased significantly when n-6/n-3 ratio decreased from 10:1 to 5:1. In addition a* values progressively decreased as the diets contained increasing n-3 content, up to the 5:1 and 2.5:1 n-6/n-3. The changes in b* were also significant but the pattern was almost the reverse of changes in a* values.
Water-holding capacity is an important attribute of meat quality and can be measured by drip loss. If water-holding capacity is poor, whole meat and further-processed products will lack juiciness. In a different experiment, enriching broiler meat with n-3 PUFAs from flaxseed reduced the ultimate pH of breast meat, decreased L* values (meat became lighter in color), and increased drip loss and cooking loss 6. Such changes were not observed in the breast meat of turkeys.
In the present experiment, the substitution of rapeseed oil for soybean oil increased the concentrations of all-trans-retinol and α-tocopherol in the breast meat of turkeys, which could be due to the different content of retinol and α-tocopherol in the analyzed oils or to the effect of different PUFA concentrations in diets on the retention of both vitamin forms in the tissues of turkeys. In a different study 55, soybean oil and linseed oil differed considerably with respect to α-tocopherol equivalents (146 and 46 mg/kg, respectively), which resulted in significant differences in α-tocopherol concentrations in the breast meat of broiler chickens. A decrease in the α-tocopherol content of breast meat was noted in an experiment in which linseed oil was substituted for soybean oil in broiler diets 22. In a study by Jensen et al. 56, the use of oxidized oil contributed to a nearly twofold decrease in the α-tocopherol content of broiler breast and thigh meat. Barroeta 57 demonstrated that the α-tocopherol content of chicken meat decreases as the dietary PUFA level increases.
The increase in the TBARS content of cooked breast meat from turkeys fed diets containing linseed oil, noted in the present study, was accompanied by a higher proportion PUFA in the total FA pool. In other experiments, an increase in PUFA levels in meat was followed by an increase in the concentrations of lipid oxidation products (measured as TBARS content) or cholesterol oxidation products, both in raw meat 20, 23 and heat-processed meat 55. Hydrothermal treatment promotes lipid oxidation in meat 38. As demonstrated by Cortinas et al. 23, TBARS values in cooked meat were 12-fold higher than in raw meat. In a different experiment, the supplementation of broiler chicken diets with linseed oil as a substitute for soybean oil resulted in a twofold increase in the TBARS content of cooked meat 55.
It is well known that lipid oxidation is a major cause of quality deterioration in meat and meat products and can give rise to rancidity and the formation of undesirable odors and flavors, which affect the functional, sensory, and nutritive values of meat products. Shear force, which measures the textural integrity, is an objective measurement, inversely related to the tenderness of meat; lower shear force indicates greater tenderness. Lopez-Ferrer et al. 10, 11, using diets supplemented with fish oil or linseed oil (n-6/n-3 ranging from 0.57 to 7.48) found no significant effects on the objective parameters (tenderness, juiciness, and grill losses) of broiler meat quality. However, other authors showed that decreasing dietary n-6/n-3 from 20:1 to 10:1 or 5:1 significantly increased shear force values of chicken meat 53. The results of sensory evaluation of boiled breast meat showed that the smell, taste, and other indices in the meat of chickens fed rapeseed oil and fish oil were not different 26. In the present experiment, the results of a sensory evaluation revealed that breast meat from turkeys fed diets supplemented with soybean oil and rapeseed oil was marked by the highest level of sensory properties. In both cases, the average score remained in the 8.0–6.0 range, i.e., between the like very much and like slightly categories. Similar sensory scores were reported by other authors 6, 58. The inclusion of linseed oil in turkey diets significantly decreased the overall sensory properties of breast meat. The average sensory score for the breast meat of group L turkeys (4.07) was below the neither like nor dislike category, and it was only slightly lower than the consumer acceptability scores for meat from chickens fed a similar diet in a study by Bou et al. 59.
In the present experiment, no undesirable changes in the n-6/n-3 PUFA ratio were noted in turkey breast meat stored for 4 months at −20°C. However, the proportion of PUFA in the FA profile significantly increased in frozen meat at the expense of SFA and MUFA, which could have consequences for the oxidative stability of meat and the formation of ROS (ROS). The increased PUFA content through storage and, at the same time, the highest concentrations of PUFA, in particular n-3 PUFA, in the meat of group L indicate that the meat of turkeys fed a diet containing linseed oil was most prone to oxidative changes. The scant experimental data available in the literature suggest that the FA profile of meat tissue lipids undergoes relatively small changes during freeze-storage. After 6-month storage, a numeric decrease in total SFA and an increase in total UFAs was noted in meat from conventionally fed chickens 60 and chickens fed diets supplemented with 0.8% fish oil 26. In a different study, the proportion of linoleic acid, AA, eicosadienoic acid, and doccosahexaenoic acid decreased significantly in turkey breast meat stored for 12 months 61.
In our study, the TBARS content of turkey breast meat increased significantly over 4-month storage, approximately 4.8- to 4.9-fold in groups S and L, and 3.4-fold in group R, compared with raw meat. The above agrees with the interaction effects in two-way ANOVA (see Table 4 and the Results Section), pointing to changes in SFA and UFA concentrations in the dietary treatments with soybean oil and linseed oil, but not with rapeseed oil. According to other authors, increased PUFA concentrations in meat are correlated with increased levels of lipid oxidation products during storage 21, 22, 24, 55. In a study by Du et al. 21, after 7-day storage at 4°C, TBARS values increased threefold in control meat samples and almost fivefold in meat with an increased CLA content. Rahimi et al. 24 reported that adding flaxseed and canola seed to broiler chicken diets increased MDA concentrations in meat, in comparison with tallow-supplemented diets. In other experiments, the addition of linseed oil to broiler chicken diets increased the TBARS content of frozen-stored breast meat, compared with chickens fed soybean oil 55 or sunflower oil 22. As expected, in our study the highest TBARS content of cooked and frozen breast meat was noted in group L. It is well known that higher n-3 PUFA deposition in muscles is accompanied by increased ROS formation (as confirmed by the TBA assay). It has also been reported that ROS formation could lead to enhanced glycolysis and accumulation of lactic acid 62. In our experiment, pH values determined at 1 and 24 h post mortem were similar in all groups. According to some authors, dietary vitamin E supplementation may prevent ROS formation and protect n-3 PUFAs in meat samples 6. In the current study, vitamin E concentration in experimental diets (54 mg) was insufficient to prevent n-3 PUFA oxidation in turkey breast muscles. Consequently, the low vitamin E content and high n-3 PUFA levels could have enhanced ROS formation in the breast muscles of turkeys fed a diet with linseed oil.
Conclusions
The current study showed that enriching turkey diets with selected vegetable oils, in particular linseed oil, is an easy way to produce breast meat with a nutritionally desired n-6/n-3 PUFA ratio. However, dietary linseed oil had a negative effect on the sensory properties and oxidation susceptibility of turkey meat. We assume that better results could be achieved via the concomitant dietary addition of linseed oil and the appropriate level of an antioxidant, e.g., selenium, vitamin E, or α-lipoic acid. Therefore, further studies are required to fully utilize the functional ingredients and health benefits offered by linseed oil rich in n-3 PUFA.
Acknowledgements
Research was realized within the project “BIOFOOD – innovative, functional products of animal origin no. POIG.01.01.02-014-090/09 co-financed by the European Union from the European Regional Development Fund within the Innovative Economy Operational Programme 2007–2013.”
The authors certify that they have no affiliation with, or functional involvement in, any organization or entity with a direct financial interest in the subject matter or materials discussed in the manuscript.
The authors have declared no conflict of interest.
