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METABOLISM AND NUTRITION |
* CIIS – Faculdade de Medicina Veterinária, Pólo Universitário do Alto da Ajuda, Avenida da Universidade Técnica, 1300-477 Lisbon, Portugal; and Estação Zootécnica Nacional, Instituto Nacional de Investigação Agrária e das Pescas, Fonte Boa, 2005-048 Vale de Santarém, Portugal
1 Corresponding author: cafontes{at}fmv.utl.pt
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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-linolenic acid (18:3n-3), respectively. In spring the levels of eicosapentaenoic acid (20:5n-3) in breast meat were significantly greater in birds consuming pastures, which suggests greater conversion of -linolenic acid into eicosapentaenoic acid in these birds. Finally, when compared with meat from slower-growing genotypes obtained under the conventional European free-range production systems with slaughtering at d 81, meat from birds of the Ross genotype raised intensively and slaughtered at d 35 seemed to have greater nutritional quality.
Key Words: free-range broiler • pasture intake • fatty acid profile • polyunsaturated fatty acid • saturated fatty acid
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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Poultry meat has been considered one of the main sources of PUFA, in particular n-3 PUFA, for human diets (Howe et al., 2006; Sioen et al., 2006). It has been shown that the content of poultry meat in n-3 fatty acids, particularly in -linolenic acid (ALA; 18:3n-3), can be readily improved by increasing the levels of n-3 PUFA in poultry diets through the incorporation of vegetable oils (López-Ferrer et al., 1999, 2001a) or oily fish by-products (Hulan et al., 1988; López-Ferrer et al., 2001b). However, a decrease in flavor quality has been reported for these products due to overall greater susceptibility to lipid oxidation in meat (Manilla and Husvéth, 1999; Bou et al., 2001). It is well known that green pastures are a good source of ALA, and pasture consumption in ruminants leads to greater contents of this fatty acid in meat while decreasing the n-6/n-3 fatty acid ratio (Wood and Enser, 1997; O’Sullivan et al., 2004). Free-range chickens are expected to consume variable amounts of forages, although the pasture contribution to alter fatty acid profiles in chicken meat has yet to be evaluated. In addition, although pasture is a poor source of EPA and DHA, it is presently unknown if birds are able to use pasture ALA as a precursor for the synthesis and deposition of these 2 essential fatty acids in broiler meat. Moreover, pastures are a good source of tocopherols and tocotrienols, natural diterpenes with vitamin E activity, which is the primary lipid-soluble antioxidant in biological systems (Kerry et al., 2000). Tocotrienols are also known to help lower plasma cholesterol levels (Qureshi et al., 1997). Antioxidant supplementation of feed is an efficient method for increasing meat oxidative stability (Maraschiello et al., 1999), although the various vitamin E forms are known to have different antioxidant potencies (Bourgeois, 1992). The contribution of grass vitamin E homologues for the oxidative stability of meat from free-range chicken has yet to be established. Finally, meat provides from one-third to one-half of the recommended daily cholesterol intake (300 mg, World Health Organization), which seems to be directly associated with a greater risk of hypercholesterolemia (Chizzolini et al., 1999). Nevertheless, the influence of pasture intake in cholesterol levels in free-range chicken is unknown.
Consumer interest in organic and natural poultry products is increasing in Western societies. In Europe, free-range broiler production systems use slow-growing meat birds with a production period of at least 81 d (European Union, 1991; Fanatico et al., 2005). The birds are housed in conventional housing but are allowed free access to the outdoors during the day and are fed ad libitum with diets containing more than 70% of cereals. Pasture consumption under this system is likely to be low because birds tend to rapidly spoil the small surplus of grass found in the vicinity of the buildings. In addition to the production system, the bird’s genotype, size, and age may affect meat fatty acid profiles (Rymer and Givens, 2005). Therefore, research is needed to evaluate the impact of these factors in the fatty acid profile of meat from free-range broilers compared with meat from conventionally grown birds.
To assess the impact of pasture intake on bird performance and meat quality, floorless portable pens were used to produce broilers of a slow-growing genotype from d 28 to 56 on legume-based pastures. Data presented in the companion paper show that pasture intake promotes boiler performance without affecting the sensorial attributes of meat (Ponte et al., 2007). The objective of the research reported here was to investigate the effect of pasture consumption on fatty acid composition, cholesterol, and vitamin E compounds of meat from free-range chickens. In addition, the cholesterol content and the profiles of fatty acids and vitamin E homologues in meat of broilers originated on free-range and conventional production systems will be characterized.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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Birds, Diets, and Management
Two experiments were conducted in the spring and autumn of 2003 in Herdade dos Esquerdos (039° 07.18' North, 007° 29.36' West, 318 m above sea level), Vaiamonte, Portugal, using the same trial design. In the spring experiment, the average of the daily mean temperature was 13.7°C (mean of highest temperature, 20.0°C, and of the minimum, 7.3°C) with 6 d of rain and total precipitation of 86.4 mm. In the autumn trial, the average of the daily mean temperature was 12.3°C (mean of highest temperature, 17.8°C, and of the minimum, 6.9°C) with 9 d of rain and total precipitation of 128.7 mm. For each experiment, one hundred twenty 28-d-old RedBro Cou Nu x RedBro M males, vaccinated against Marek disease, were divided into 12 floorless portable outdoor pens (10 birds per pen/replicate), equalizing both the mean and variance of BW. Before the start of the experiment, from d 0 to 28, birds were raised in battery brooders in a temperature-controlled room under standard brooding practices and were fed ad libitum with a typical maize-soybean diet. At d 28, birds were moved to the pastured pens described below, in which they were maintained for an additional 28 d until slaughtered at d 56. The portable pens measured 1.7 m x 1.5 m x 0.5 m (0.255 m2 per bird) and allowed birds to directly contact the legume-based pastures, promoting pasture intake. Water and a cereal-based feed were available ad libitum throughout the experiments and were provided in 2 automatic drinking nipples and an individual hanging tube feeder, respectively. The composition of the cereal-based feed used in these studies, which was formulated to contain adequate nutrient levels as defined by NRC (1994), is presented in Table 1
. Approximately one-third of the top area of the pen was covered with transparent whitewashed plastic to protect against harsh climatic conditions.
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On the day of slaughter for birds in the spring experiment, 24 carcasses of 35-d-old Ross commercial broilers (meat of this treatment is referred to herein as Ross) raised under the conventional system and slaughtered at the same commercial processing plant were acquired for further comparison with the field experimental meats. In addition, 24 carcasses of 81-d-old RedBro Cou Nu x RedBro M raised under the European free-range system (meat of this treatment is referred to herein as Lab) were obtained to allow comparison of the biochemical properties of the Ross and Lab meats. The Ross and Lab birds were randomly selected from birds originating from 4 different conventional or free-range farms, respectively, with a total of 6 birds slaughtered per farm. Birds of the Ross and Lab treatments were fed ad libitum with typical maize-soybean diets, although the precise composition of the feeds is unknown. The Ross and Lab treatments represented poultry meats available for consumers in the market. Carcasses were stored in a cool chamber at 0 to 4°C for 24 h. After carcass measurements, skinless breast meat samples (approximately 10 g) were collected for determining total lipids, fatty acid composition, and total cholesterol and vitamin E compounds. The samples were ground using a food processor (3 x 5 s), vacuum packed, and stored at –80°C until required.
Determination of Total Lipids
Meat samples were lyophilized (–60°C and 2.0 hPa) to constant weight using a Edwards Modulyo lyophilizer (Edwards High Vacuum International, Norfolk, UK), stored dessicated at room temperature, and analyzed within 2 wk. For total lipid determination, intramuscular fat was extracted from the lyophilized samples (0.25 g) as described by Alfaia et al. (2006). Total lipids were measured gravimetrically, in duplicate, by weighing the fatty residue obtained after solvent evaporation.
Determination of Fatty Acid Composition
Intramuscular fat of lyophilized samples (0.25 g), cereal-based feed, or pasture (0.10 g of DM) were first dissolved in 1 mL of dry toluene. Then, fatty acids were converted to FAME by base-catalyzed transesterification with sodium methoxide for 2 h at 30°C. Fatty acid composition was determined by gas chromatography of FAME, performed with a Varian 3800 gas chromatograph (Varian Inc, Walnut Creek, CA) equipped with a flame-ionization detector and an OmegaWax 250 capillary column (30 m x 0.25 mm i.d., 0.25-µm film thickness, Supelco, Bellefonte, PA). The chromatographic conditions were as follows: injector temperature, 250°C; detector temperature, 280°C; helium was used as carrier gas; and the split ratio was 1:20. The gas chromatograph oven temperature was programmed to start at 150°C (maintained for 15 min) followed by a 3°C/min increase to 220°C (maintained for 20 min). Identification was accomplished by comparing the retention times of peaks from samples with those of FAME standard mixtures. Quantification of FAME was based on the internal standard technique, using nonadecanoic acid (19:0) as internal standard and on the conversion to relative peak areas to weight percentage, using the corrected response factor of each fatty acid (European Committee for Standardization, 1990). Fatty acids were expressed as gravimetric contents (mg/g of muscle) or as a percentage of the sum of identified fatty acids (% wt/wt).
Quantification of Total Cholesterol, Tocopherols, and Tocotrienols
The simultaneous determination of total cholesterol, β-carotene, tocopherols, and tocotrienols was performed as described by Prates et al. (2006). The method involved a direct saponification of the fresh meat (0.75 g), high-energy feed, or pasture (0.10 g of DM), a single n-hexane extraction, and analysis of the extracted compounds by normal-phase HPLC, using fluorescence (tocopherols and tocotrienols) and UV-visible photodiode array (cholesterol and β-carotene) detections in tandem. The contents of total cholesterol, β-carotene, tocopherols, and tocotrienols were calculated in duplicate for each sample based on the external standard technique from a standard curve of peak area vs. compound concentration.
Statistical Analysis
Statistical analysis was conducted by ANOVA using SAS with the GLM procedure (SAS Institute, 2004). The model used for analyzing data of the pasture experiment included the effect of treatment, the effect of season, and the interaction between treatment and season. The experimental unit considered was the pen. The significance for main effects of season and interaction were presented but the treatment effect was replaced by 2 orthogonal contrasts. The first contrast (NP vs. pasture) compared the biochemical parameters of meat from birds with no access to pasture (NP) with meat from birds that had access to pasture. The second contrast (TrP vs. TsP) compared the biochemical parameters of meat from birds with access to the white clover based pasture with meat from birds with access to the subterranean clover based pasture. The linear model used in the experiment of commercial broilers included only the effect of the type of commercial production (Lab and Ross). In this specific case, the experimental unit considered was the farm. Unless otherwise stated, differences were considered significant when P < 0.05.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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Fatty Acid Composition and Cholesterol, β-Carotene, Tocopherol, and Tocotrienol Contents of Pastures and Cereal-Based Feed
The fatty acid composition of the cereal-based feed and both pastures is presented in Table 2. Total fatty acids were greater in the cereal-based feed, intermediate in pastures from autumn, and lowest in pastures from spring. As expected, linoleic acid (LA; 18:2n-6) was the major fatty acid in the cereal-based diet, whereas ALA was predominant in the legume-based pastures, especially in the autumn. Palmitic acid (16:0) was relatively abundant in the various feeds, although at greater levels in the pasture relative to cereal-based feed. In contrast, the cereal-based feed contained greater percentages of oleic acid (18:1n-9) when compared with all pastures. There were no major differences in the fatty acid profile of the TsP or TrP, although in the autumn. both pastures had a greater proportion of ALA. In addition, EPA and DHA were negligible in all feeds analyzed (data not shown). Finally, the 4 pastures presented LA/ALA ratios of <0.40, whereas the cereal-based feed had an LA/ALA ratio of 16.7.
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. Although 
-tocopherol was coeluted with a minor proportion of β-tocotrienol and, specifically in the cereal-based feed, 
-tocotrienol, a complete profile of vitamin E compounds was obtained. The - and -tocopherols were the most abundant vitamin E homologues in the cereal-based diet, in agreement with the exogenous supplementation of -tocopherol to the cereal-based feed, whereas -tocopherol and -tocotrienol were predominant in the legume-based pastures. It is well known that tocotrienols have different antioxidant potencies and biological activities compared with tocopherols; therefore, the determination of all vitamin E molecules in feed is critical. In addition, the pastures presented significant levels of β-carotene, although the cereal-based feed showed undetectable levels of this lipid-soluble antioxidant provitamin.
Effect of Pasture Intake on Fatty Acid Composition, Cholesterol, Tocopherols, and Tocotrienols of Meat from Free-Range Broilers
Data referring to the fatty acid composition of breast meat from free-range broilers fed ad libitum on a cereal-based diet and allowed grazing on TsP or TrP during spring and autumn are presented in Table 3. The predominant fatty acids in chicken meats of all treatments were palmitic and stearic (18:0) acids as SFA, oleic acid as mono-unsaturated fatty acid (MUFA), and LA and arachidonic acid (20:4n-6) as PUFA. Oleic and palmitic acids were the most abundant fatty acids in the various meats under analysis. Pasture consumption had little effect on the fatty acid profile of broiler meats. This is not completely unexpected, because the levels of pasture intake (in terms of DM) in birds with access to the legume-based pastures were low (Ponte et al., 2007). In addition, pasture intake did not reduce the amount of cereal-based diet consumed but rather increased it. Although pastures presented LA/ALA ratios <0.40, meat from free-range broilers had a much greater n-6/n-3 ratio (11.3 to 12.9) that was not affected by pasture intake (Table 3). It is known that ALA present in pasture is in the esterified form in structural lipids, including galactolipids from chloroplasts (Gurr, 1984). Therefore, it is possible that the broiler digestive system may not be able to digest structural lipids or may lack the required galactolipase activity to free ALA from galactolipids. Although consumption of both pastures did not affect the percentages of the major represented fatty acids (P > 0.05), intake of TrP reduced (P < 0.01) the percentage of LA in broiler meat. This effect could be due to the reduced proportion of LA in the pastures and to slightly greater intakes observed in birds foraging on TrP (data not shown). Interestingly, a seasonal effect (P < 0.001) was observed on the content of LA, with greater percentages of the fatty acid being observed in broiler meat from the autumn experiment.
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Pasture intake had no effect (P > 0.05) on the total cholesterol concentration in meat (Table 3). In contrast, meat glycerol lipids (or nonsterol lipids) were lower in birds with access to pastures when compared with those without access to pasture. However, all chicken meats were lean based on the Food Advisory Committee (1990) criteria (<5% fat), and depict median contents of total cholesterol (0.49 to 0.51 mg/g) compared with those reviewed by Chizzolini et al. (1999) for beef. -Tocopherol, which co-eluted in these meats with small amounts of -tocotrienol, was the major vitamin E homologue detected in breast meats (Table 4). In addition, small contents of -tocopherol (which coeluted with a minor proportion of β-tocotrienol), β-tocopherol, and -tocotrienol were also identified. In contrast, although the pastures presented detectable levels of -tocopherol (0.53 to 1.00 µg/g of DM) and -tocotrienol (2.30 to 7.71 µg/g of DM), these diterpenes were not detected in any of the meat samples analyzed. The prevalence of -tocopherol in meat is well known and is due to the more than 10-fold preference of the tocopherol-binding protein for -tocopherol, relative to -homologues, which are the most common vitamin E molecules in plant foods (Decker et al., 2000). Finally, the levels of vitamin E compounds in meat were not affected (P > 0.05) by pasture intake, although seasonal variation (P < 0.001) in the levels of β- and -tocopherols was observed (Table 4). In addition, although the pastures presented significant levels of β-carotene (2.96 to 21.4 µg/g of DM), this lipid-soluble anti-oxidant provitamin was not detected in any of the meat samples analyzed, which may be due to their lower fat content.
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confirm that there are considerable differences in the fatty acid profiles of the 2 meats under analysis. In both meats, the predominant fatty acid was palmitic acid, followed by oleic acid. However, these 2 fatty acids were more represented in meat from the free-range broilers. As expected, in both meats the precursor of the n-6 fatty acid family (LA) predominates in relation to the precursor of the n-3 family (ALA), although both PUFA were present in greater percentages in meat from the fast-growing genotype. Although EPA and 20:3n-3 were predominant in meat from the conventional broilers, DHA was more abundant in meat from the commercial free-range birds. In relation to the long-chain n-6 fatty acids, arachidonic acid predominated in meat from the slower-growing genotype, whereas 22:4n-6 was more abundant in breast meat from the Ross genotype. The SFA (P < 0.001) and MUFA (P < 0.01) contents of meat from the free-range broilers were greater compared with meat from the fast-growing genotype, as shown in Table 5. Accordingly, fast-growing birds yielded breast meat with greater percentages (P < 0.001) of PUFA. However, the n-6/n-3 ratio was not different between the 2 meats, although the fast-growing genotype yielded breast meat with greater percentages (P < 0.01) of both n-6 and n-3 fatty acids (Table 5). Taken together, these data suggest that slower-growing genotypes raised under free-range production systems may not originate meat with greater nutritional quality. Here, it was shown that meat from intensively grown birds slaughtered at d 35 presented greater levels of PUFA and n-3 fatty acids compared with the commercial free-range broilers.
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). Cholesterol is an important molecule that has roles in membrane structure as well as being a precursor for the synthesis of molecules such as steroid hormones, vitamin D, and bile acids. Cholesterol can be obtained directly from the diet, or it can be synthesized in cells from 2-carbon acetate groups of acetyl-CoA. Because the synthetic pathway is under feedback control from dietary cholesterol, the percentage of cholesterol arising from de novo biosynthesis depends upon the amount of cholesterol in the diet. Even when cholesterol intake is very low, de novo biosynthesis will enable the production of the cholesterol required to supply the large variety of biological processes in which this molecule is involved. Therefore, although our data suggested that fast-growing and younger birds had greater levels of cholesterol, it is unknown if these results were the consequence of high cholesterol levels in the diet or result from the influence of genotype per se. Finally, -tocopherol, which coeluted with small amounts of -tocotrienol, was present at similar levels (P > 0.05) in both meats and was the most abundant compound with vitamin E activity, in accordance with the putative supplementation of the broiler diets with significant and similar levels of exogenous -tocopherol acetate (Table 6). In addition, small amounts of -tocopherol, which coeluted with minor amounts of β-tocotrienol, β-tocopherol, and -tocotrienol, were also determined. In contrast, the diterpenes -tocopherol and -tocotrienol were not detected in any of the meat samples analyzed. There were no significant differences (P > 0.05) for the minor vitamin E compounds between Lab and Ross meats, with the exception of -tocopherol, which was greater (P < 0.001) in Ross meat.
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ACKNOWLEDGMENTS |
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Received for publication April 10, 2007. Accepted for publication September 8, 2007.
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