Meat quality and lipid profiles in crossbred lambs finished on clover-rich pastures

Meat Science 90 (2012) 733–738

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Meat quality and lipid profiles in crossbred lambs finished on clover-rich pastures P.B. Faria a, M.C. Bressan a, b,⁎, J.O. Vieira a, J. Vicente-Neto a, c, S.P.B. Ferrão a, d, F.C. Rosa a, e, .M. Monteiro f, M.G. Cardoso a, L.T. Gama b, g a

Universidade Federal de Lavras, CEP 37200-000, Minas Gerais, Brazil L-INIA, Instituto Nacional de Recursos Biológicos, 2005-048 Vale de Santarém, Portugal Instituto Federal de Educação, Cáceres, CEP 78200-000, Mato Grosso, Brazil d Universidade Estadual do Sudoeste da Bahia, Itapetinga, CEP 45700-000, Bahia, Brazil e Universidade Federal do Tocantins, CEP 77809-470, Tocantins, Brazil f Embrapa Pecuária Sul, Bagé, CEP 96401-970, Rio Grande do Sul, Brazil g CIISA, Faculdade de Medicina Veterinária, Universidade Técnica de Lisboa 1300-477, Portugal b c

a r t i c l e

i n f o

Article history: Received 21 January 2011 Received in revised form 27 August 2011 Accepted 2 November 2011 Keywords: Fatty acids Meat quality Pasture finishing Sheep

a b s t r a c t Meat quality traits were compared in Texel x Polwarth and Texel x Corriedale ram lambs, with live weight of 25 kg, finished on pastures rich in white clover. The two crossbred groups showed similar results (P > 0.05) for pH, moisture, protein, meat color, individual SFA and total SFA. Fat content was higher and cholesterol lower in Texel x Polwarth lambs (P b 0.05), which also had higher amounts of MUFA (P b 0.05) and lower levels of total PUFA and n− 6 PUFA (P b 0.01). Differences in meat quality among the two crossbred groups were minor, and possibly not perceptible from the consumer standpoint. However, both groups of lambs produced lean meat with high amounts of PUFA (>16%), possibly due to the ingestion of white clover in the finishing period. Overall, these results indicate that a differentiated product can be obtained in these conditions, with higher nutritional value than conventional lamb meat. © 2011 Elsevier Ltd. Open access under the Elsevier OA license.

1. Introduction Until a few years ago, sheep farms in the southern region of Brazil aimed to produce wool and the more widespread breeds were Polwarth (also known as Ideal), Corriedale, Romney Marsh and Merino (Viana & Silveira, 2009). However, with the textile industry evolution and the popularity of synthetic fibers, many breeders decided to use crossbreeding with mutton breeds, to obtain heavier lambs in a shorter period of time. These animals are usually raised until slaughter under extensive systems with subtropical native pastures, characterized by high forage availability in the spring–summer and low forage productivity in the autumn–winter (Bandinelli et al., 2005). An interesting alternative adopted to improve pasture-feeding is the introduction of winter forages of the genera Lolium (ryegrass), Festuca (fescue), Lotus (trefoil), Trifolium (clovers) and Medicago (alfalfa) (Pereira et al., 2008). In this region, forages are usually based on mixed intercropping of grass and legume species, which provide a higher dry-matter yield, with better quality (Olivo et al., 2009), given their higher digestibility and nitrogen content (Fontaneli & Freire, 1991). Compared to native pastures, these forage associations provide a higher output of lamb

⁎ Corresponding author at: L-INIA, Instituto Nacional de Recursos Biológicos, 2005048 Vale de Santarém, Portugal. Tel.: + 351 243767382; fax: + 351 243767307. E-mail address: [email protected] (M.C. Bressan). 0309-1740 © 2011 Elsevier Ltd. Open access under the Elsevier OA license. doi:10.1016/j.meatsci.2011.11.004

per hectare (Assann et al., 2004; Selaive-Villarroel, Silveira, & Oliveira, 1997). Among the mixed intercropping pastures, those based on white clover are especially popular in this area, resulting in drymatter yields of about 2000 to 3000 kg/ha (Fontaneli & Freire, 1991). Carcass and meat quality of wool-type or dual purpose lambs vs. meat lambs have been evaluated in Brazil (Bonagurio, Pérez, Furusho-Garcia, Bressan, & Lemos, 2003; Rota et al., 2004; Souza et al., 2004), but their lipid profiles have not been studied under the pasture conditions which prevail in subtropical climates. Research reports with beef cattle indicate that diet has a major impact upon the deposition of IMF, as well as on the concentration of SFA and PUFA (De Smet, Raes, & Demeyer, 2004), and that genetic differences exist regarding the activity of enzymes involved in fatty acid synthesis, such as Δ 9 desaturase (which converts SFA into cis-9 MUFA), elongase (which converts C16:0 into C18:0) and Δ 4, Δ 5 and Δ 6 desaturase (which convert C18 PUFA into C20-C22 PUFA) (Bressan et al., 2011; Malau-Aduli, Siebert, Bottema, & Pitchford, 1998; Warren et al., 2008; Wood et al., 2008). The health implications of fat quantity and quality in human diets were reviewed by Valsta, Tapanainen, and Mannisto (2005). In general, it is accepted that increasing the level of n−3 FA in the diet reduces the risk of heart problems and arteriosclerosis, while CLA isomers have anticarcinogenic and antiatherogenic properties (Belury, 2002). Therefore, a major challenge for lamb producing systems worldwide is to find ways to decrease the proportion of SFA and increase the amount of n−3 PUFA and CLA in meat (Wood et al., 2008).

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The interaction between animals, environmental factors and man may be reflected in the existence of production systems with unique characteristics, which may result in meats with specific and differentiated attributes. Often, these can receive specific distinguishing labels which result in an added-value that can represent an important contribution to the sustainability of production systems (Bernués, Olaizola, & Corcoran, 2003). The objective of this work was to investigate meat quality in two groups of crossbred lambs (Texel x Polwarth and Texel x Corriedale) finished on clover-rich pastures, including proximate composition, lipid profiles and cholesterol content. 2. Material and methods Humane animal care and handling procedures were followed throughout the raising and finishing periods and at slaughter, according to the guidelines of State of São Paulo (Brazil) law number 11977/2005. 2.1. Animals, production systems, transport and slaughter The study was carried out in the Embrapa Pecuária Sul Experimental Center, located in Bagé, State of Rio Grande do Sul, Brazil, which has a subtropical climate with average annual temperature of 17.5 °C. For several years, this Center has carried out a comparison of the productive performances of Texel, Romney Marsh, Corriedale, Polwarth and Merino sheep, both as pure and crossbred animals (Oliveira, Osório, & Monteiro, 1996; Osório, Oliveira, Osório, Jardim, & Pimentel, 2002; Rota et al., 2004). In the framework of this experiment, about 30 Corriedale and 30 Polwarth ewes were group-mated with Texel rams. Of the progeny born, 10 Texel x Polwarth and 10 Texel x Corriedale crossbred ram lambs were randomly selected for this experiment. Lambs were kept with their mothers on extensive grazing until weaning at 70 days of age. At this point they were moved into cultivated pastures predominantly composed of birdsfoot trefoil (Lotus corniculatus L.), white clover (Trifolium repens L.) and ryegrass (Lolium multiflorum Lam.), with a stocking rate of about 17 lambs/ha. Animals received mineral salt ad libitum and an antihelmintic treatment, and were kept on pasture-finishing for 110 days. When lambs reached a mean live weight of 25 kg at about 6 months of age, they were transported to a commercial abattoir located about 15 km from the farm. They were slaughtered after 16 h of resting, according to official procedures, with electrical stunning, and carcasses were chilled at 2 °C for 24 h. 2.2. Sample collection and laboratory analyses Meat pH was measured in triplicate in the M. longissimus thoracis at 24 hours post mortem, by inserting a glass electrode attached to a portable pH meter M 1120x (Mettler-Toledo International Inc., Columbus, EUA), approximately 2.5 cm into the muscle. Samples of the M. longissimus lumborum were collected, individually vacuumpackaged, frozen at − 35 °C, stored at −20 °C until further analyses. After approximately 30 days of frozen storage, muscle samples were thawed at 4 °C for 24 h, trimmed of subcutaneous fat and surface connective tissue. Three slices with a thickness of 12 mm were obtained by sectioning the M. longissimus lumborum perpendicular to the muscle fibers. After 30 min of blooming at 4 °C, color coordinates L*, a* and b* were obtained with a CR-300b colorimeter (Minolta Camera Co., Ltd., Osaka, Japan), D65 illuminant and 10° observer. Three color measurements were obtained from each slice and the mean of the nine measurements per animal was used for further analyses. Chroma (C*) and hue angle (H*) values were calculated as C* = ((a*) 2 + (b*)2)0,5 and H* = arctan (b*/a*). Meat samples for chemical analyses were minced in a commercial mixer-blender until a homogeneous mass was obtained, and the analyses were carried out in triplicate. Protein was estimated by the

method of Kjeldahl and IMF by Soxhlet (AOAC, 1995). Moisture was determined in an oven at 105 °C until a constant weight was reached, and ash concentration was determined on the residue of samples after drying for 12 h at 550 °C. The proximate composition components were expressed as percentages of fresh meat weight. For the analysis of cholesterol and fatty acids (FA), lipids were extracted according to procedures described by Folch, Lees, and Stanley (1957). Cholesterol was quantified by colorimetry, with a modification of the method of Bohac, Rhee, Cross, and Ono (1988), as described by Bragagnolo and Rodriguez-Amaya (2001), and the results were expressed in mg/100 g of meat. The preparation of FA methyl esters was carried out according to Hartman and Lago (1973). Briefly, FA were saponified with a methanolic NaOH solution and methylated under acidic conditions by adding a solution of ammonia chloride, methanol and sulphuric acid. The FA methyl esters were submitted to gas liquid chromatography on a GC-17A model chromatographer (Shimadzu Corporation, Kyoto, Japan), equipped with a flame ionization detector and a 30 m capillary column of polyethylene glycol (DB-WAX, 30 m × 0.25 mm × 0.20 µm), with oven temperature and other chromatograph settings programmed as described by Vicente-Neto et al. (2010). A 1:5 split injection ratio was used and nitrogen was used as the carrier gas, at a constant flow rate of 1 mL/min. The identification of FA was performed by comparison with the retention time of the FA methyl ester standard PUFA 2 (Supelco Inc., Bellefonte, PA, USA), constituted by a mixture of 14 FA. Individual FA were expressed as percentage of total identified FA, and then grouped as saturated (SFA), monounsaturated (MUFA) and polyunsaturated (PUFA) fatty acids. The estimated activities of Δ 9 desaturase and FA elongase were evaluated according to Kazala et al. (1999) and Malau-Aduli et al. (1998), as follows: C16 desaturase activity index= 100 [(C16:1 cis-9)/(C16:1 cis-9+ C16:0)], C18 desaturase activity index = 100 [(C18:1 cis-9)/(C18:1 cis-9 + C18:0)], C16 to C18 elongase activity index= 100 [(C18:0 + C18:1 cis-9)/(C16:0 + C16:1 cis-9+ C18:0 + C18:1 cis-9)], and C16 to C14 thioesterase activity index = 100 [(C16:0)/(C16:0 + C14:0)]. 2.3. Statistical analyses Animals were considered the experiment unit for all the variables analyzed. The GLM procedure of SAS (SAS Institute, 2004) was used in analyses of variance, to study the effects of type of cross on the response variables evaluated. With the design followed in our study, differences between the two crossbred groups of lambs essentially reflect differences between ewe breeds (Polwarth vs. Corriedale) in both direct and maternal effects, assuming that the heterosis realized is the same when either one of the two ewe breeds is mated with Texel. The response variables analyzed were moisture, protein, fat, ash, cholesterol, pH, color coordinates (L*, a* and b*), H* and C* values, individual fatty acids, sums of groups of fatty acids, functions of groups of fatty acids, nutritional ratios, and indexes of desaturase, elongase and thioesterase activity. Correlations between chemical components and FA concentrations were obtained with the CORR procedure of SAS (SAS Institute, 2004). 3. Results The longissimus lumborum samples of Texel x Polwarth lambs showed higher (P = 0.043) fat content (by 0.30 percentage points) and lower (P = 0.044) cholesterol levels (by 5.72 mg/100 g), when compared to Texel x Corriedale lambs (Table 1). All the other chemical composition variables, as well as pH, color coordinates, C* and H* values did not differ between genetic groups (P > 0.05), even though moisture and the L* coordinate approached significance (P ≃ 0.06). The predominant FA found in intramuscular fat were, in descending order, C18:1 cis-9 (39.54%, pooled across the two crossbred groups), C16:0 (18.84%), C18:0 (17.73%), C18:2n-6 (7.33%), C20:4n-6 (4.50%)

P.B. Faria et al. / Meat Science 90 (2012) 733–738 Table 1 Least squares means by genetic group, standard error (SE) and significance (P - value) for physico-chemical characteristics in M. longissimus lumborum of Texel*Polwarth and Texel*Corriedale crossbred lambs. Variable

Texel*Polwarth (n = 10)

Texel*Corriedale (n = 10)

SE

Significance (P - value)

Moisture (%) Protein (%) IMF (%) Ash (%) Cholesterol (mg/100 g) pH L* a* b* C* H

77.14 20.80 1.39 1.09 73.05 5.61 41.47 9.86 6.83 12.00 34.68

77.90 20.97 1.10 1.13 78.77 5.66 39.62 10.33 7.08 12.61 33.24

0.264 0.205 0.093 0.046 1.873 0.045 0.654 0.274 0.398 0.286 1.824

0.057 0.575 0.043 0.518 0.044 0.520 0.062 0.237 0.655 0.139 0.865

and C20:5n-3 (2.23%). The majority of the individual FA showed similar (P > 0.05) deposition between the two crosses studied here (Table 2), with the exception of C16:1 cis-9 (P = 0.012) and C18:1 cis-9 (P = 0.035), which were higher in Texel x Polwarth lambs, and of C18:2n-6 (P = 0.001), C22:4n-6 (P = 0.050) and C22:5n-3 (P = 0.018), which were higher in Texel x Corriedale. When groups of FA were considered, the means for total SFA (P = 0.194) and n−3 PUFA (P = 0.090) were similar for both crosses, while total MUFA were higher in samples of Texel x Polwarth lambs (P = 0.014), and total PUFA (P = 0.008) and n−6 PUFA (P = 0.004) were higher in Texel x Corriedale. The higher levels of total PUFA found in meat from Texel x Corriedale lambs determined a higher P/ S ratio when compared to Texel x Polwarth lambs, with means higher by 0.12 units (P = 0.016). The same happened to the n− 6/n−3 ratio, which was higher for Texel x Corriedale by 0.52 units (P = 0.046). The estimated activity of Δ 9 desaturase (C16) and Δ 9 desaturase (C18) indexes, was similar for the two crossbred groups (P = 0.083 and P = 0.936, respectively), indicating that the activity of stearoylCoA desaturase, responsible for the modification of the C16:0/C16:1 cis-9 and C18:0/C18:1 cis-9 pairs was similar for Texel x Polwarth and Texel x Corriedale crossbred lambs. Furthermore, the estimated activity of elongase, measured by the C16 to C18 elongase activity index, and the estimated activity of thioesterase, determined by the C16 to C14 thioesterase index, did not differ among crosses (P = 0.336 and P = 0.504, respectively).

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Table 2 Least squares means by genetic group, standard error (SE) and significance (P-value) for individual fatty acids (% of total fatty acids), sum of groups of fatty acids, functions of groups of fatty acids, nutritional relevant ratios and desaturase, elongase and thioesterase indexes in M. longissimus lumborum of Texel*Polwarth and Texel*Corriedale crossbred lambs. Variable

Texel*Polwarth (n = 10)

Texel*Corriedale (n = 8)

Significance (P-value)

Individual fatty acids C14:0 C16:0 C18:0 C16:1 cis-9 C18:1 cis-9 C20:1 cis-9 C18:2 n-6 C18:3 n-6 C18:3 n-3 C20:4 n-6 C20:5 n-3 C22:4 n-6 C22:5 n-3 C22:6 n-3

2.07 ± 0.13 19.02 ± 0.33 18.30 ± 0.55 2.77 ± 0.09 40.69 ± 0.66 0.30 ± 0.03 6.28 ± 0.34 0.10 ± 0.01 1.78 ± 0.13 4.02 ± 0.32 2.03 ± 0.17 0.16 ± 0.01 2.12 ± 0.09 0.37 ± 0.02

2.18 ± 0.15 18.67 ± 0.37 17.16 ± 0.61 2.41 ± 0.09 38.39 ± 0.74 0.32 ± 0.03 8.39 ± 0.38 0.08 ± 0.01 1.94 ± 0.14 4.98 ± 0.36 2.44 ± 0.19 0.20 ± 0.02 2.46 ± 0.10 0.37 ± 0.02

0.600 0.492 0.183 0.012 0.035 0.607 0.001 0.142 0.432 0.061 0.122 0.050 0.018 0.910

Sum SFA a MUFA PUFAc n-6 d n-3 e

39.39 ± 0.68 43.45 ± 0.64 16.86 ± 0.89 10.56 ± 0.62 6.30 ± 0.34

38.01 ± 0.76 41.12 ± 0.72 20.87 ± 0.99 13.66 ± 0.69 7.21 ± 0.38

0.194 0.014 0.008 0.004 0.090

0.43 ± 0.03 1.67 ± 0.07

0.55 ± 0.04 1.92 ± 0.09

0.016 0.046

12.75 ± 0.48 69.01 ± 0.76 73.01 ± 0.35 90.18 ± 0.61

11.43 ± 0.53 69.10 ± 0.85 72.48 ± 0.39 89.55 ± 0.68

0.083 0.936 0.336 0.504

b

Ratios P/Sf n-6/n-3

g

Indexes Δ9 desaturase (C16) Δ9 desaturase (C18) Elongasej Thioesterase k

h i

a

4. Discussion

Sum of SFA (C14:0 + C16:0 + C18:0). Sum of MUFA (C16:1 cis-9 + C18:1 cis-9 + C20:1 cis-9). Sum of PUFA (C18:2n-6 + C18:3n-6 + C18:3n-3 + C20:4n-6 + C20:5n-3 + C22:4n6 + C22:5n-3 + C22:6n-3). d Sum of PUFA of the n-6 series (C18:2n-6 + C18:3n-6 + C20:4n-6 + C22:4n-6). e Sum of PUFA of the n-3 series (C18:3n-3 + C20:5n-3 + C22:5n-3 + C22:6n-3). f Ratio P/S (C18:2n-6 + C18:3n-3)/(C14:0 + C16:0 + C18:0). g Ratio n-6/n-3 (Σn-6/Σn-3). h Index of C16 desaturase activity = 100 [(C16:1 cis-9)/(C16:1 cis-9 + C16:0)]. i Index of C18 desaturase activity = 100 [(C18:1 cis-9)/(C18:1 cis-9 + C18:0)]. j Index of C16 to C18 elongase activity = 100 [(C18:0 + C18:1 cis-9)/(C16:0 + C16:1 cis-9 + C18:0 + C18:1 cis-9)]. k Index of C16 to C14 thioesterase activity = 100 [(C16:0)/(C16:0 + C14:0)].

In most species, fat content is the meat component showing higher variability (Williams et al., 1983), depending on the balance between diet energy content and metabolic requirements, associated to the genetic characteristics of the animal (Cartwright, 1970; Kvame, Brenøe, & Vangen, 2006). Even though the mean intramuscular fat level was low overall (b1.5%), Texel x Polwarth lambs showed higher amounts of fat than those of the Texel x Corriedale group. This suggests that there are differences between groups concerning the distribution of adipose and muscle tissues, with Texel x Corriedale animals presenting leaner carcasses, which could be a consequence of Corriedale being a dual purpose breed, whereas Polwarth is a wool-type sheep. Furthermore, it is generally assumed that breed differences in intramuscular fat are largely due to variability in maturity stage, such that, when compared at the same weight, breeds with larger mature size tend to be leaner than breeds with smaller mature size (Cartwright, 1970; Kvame et al., 2006). Pasture-finished ruminants usually have lower glycogen storage at slaughter and, therefore, higher ultimate pH, than those finished with grain. Nevertheless, the mean values found in our study (pH b 5.8) suggest that the pasture-finished lambs were in good

welfare conditions before slaughter (Muchenje et al., 2009), producing meat with a pH which is considered adequate for proper maintenance of shelf-life (Mach, Bach, Velarde, & Devant, 2008). In our study, the two crossbred groups did not differ in meat color, suggesting that they are similar concerning the morphology of muscle fibers, post mortem glycolytic reactions and pigment ratios. This is in contrast with the results of Bonagurio et al. (2003) with Santa Inês and Santa Inês x Texel crossbred lambs, and of Souza et al. (2004) with Santa Inês x Ile-de-France and Santa Inês x Bergamácia crossbred lambs, who found higher lightness and lower redness in the longissimus muscles from meat type animals. The details of cholesterol metabolism in ruminants are not fully elucidated, in spite of the extensive knowledge existent in other species (Viturro et al., 2009). In cattle, there is no linear association between serum and tissue cholesterol concentrations (Wheeler, Davis, Stoecker, & Harmon, 1987), but the degree of marbling may be positively related with cholesterol content (Rhee, Dutson, Smith, Hostetier, & Reiser, 1982). In our study, the leaner Texel x Corriedale lambs presented higher mean cholesterol levels than Texel x

b c

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Polwarth lambs, suggesting that the wool-type Corriedale crossbred lambs tend to have higher amounts of cholesterol when compared with meat-type crossbred animals. The regulation of the isoprenoid biosynthetic pathway, known to be complex in all eukaryotic organisms, has numerous points of regulation that act to control the overall flux through the pathway as well as the relative flux through various branches of the pathway (DimsterDenk et al., 1999). The major fatty acid in mammalian adipose triglycerides is C18:1 cis-9, which is used for phospholipids and cholesteryl ester synthesis (Nakamura & Nara, 2004). In our work, a negative correlation between the content of meat in cholesterol and C18:0 was found (r= −0.45, P = 0.06, data not shown), indicating that an increased meat deposition of cholesterol is associated with a lower deposition of C18:0 in muscle. These results further suggest that C18:0, which is one of the final products of FA synthesis, either was desaturated into C18:1 cis-9, which participates in cholesterol synthesis, or that it acted as a modulator of cholesterol synthesis. In sheep, the total amount of PUFA usually ranges between 4.6 and 16.3% (Fisher et al., 2000; Lee, Evans, Nute, Richardson, & Scollan, 2009). In general, C18:2n-6 is the more abundant PUFA, with percentages ranging from 1.8 to 12.9% (Díaz et al., 2005; Fisher et al., 2000; Juárez et al., 2009; Santos-Silva, Bessa, & Mendes, 2003). Ruminants finished on pasture tend to show higher amounts of PUFA than those finished with grain (Bressan et al., 2011), due to a higher ingestion of C18 PUFA in the diet. However, the total amount of PUFA found in our work is quite high (P/S ratio greater than 0.40), possibly more than would to be justified only by an increased intake of C18 PUFA. Some reports (Dewhurst, Delaby, Moloney, Boland, & Lewis, 2009; Díaz et al., 2005) describe a higher content of C18:2n-6 and C18:3n-3 in milk and meat of ruminants grazing red or white clover legumes, when compared to milk and meat of animals fed with grasses and other legumes. It is believed that, in red clover-rich diets the fermentation and biohydrogenation in the rumen are different from those obtained with perennial ryegrass (Lourenço, Van Ranst, Vlaeminck, De Smet, & Fievez, 2008) due to the inhibition of proteolysis and lipolysis by the plant enzyme polyphenol oxidase, which is present in clover. This enzyme converts phenols into quinones, which bind with proteins and reduce the occurrence of proteolysis and lipolysis in the rumen (Lee, Parfitt, Scollan, & Minchin, 2007; Van Ranst, Lee, & Fievez, 2010). Consequently, a higher proportion of the unsaturated fatty acids of the ingested feed passes the rumen to be absorbed in the intestine, such that a higher transfer rate of PUFA from feed to ruminant products is observed with clover-rich diets (Lee, Harris, Dewhurst, Merry, & Scollan, 2003). In our work, the total and individual SFA (C14:0, C16:0, and C18:0) were similar for the two crosses considered, while total MUFA and the cis-9 MUFA (C16 and C18) were higher for Texel x Polwarth than for Texel x Corriedale samples. Also, Texel x Polwarth muscle samples showed higher fat content, and it is known that the amount of SFA usually increases when fat deposition is higher (De Smet et al., 2004). In our work, a similar relationship was observed, with a correlation between C16:0 and fat content of r = 0.58 (P b 0.01, data not shown). In cattle, there is evidence of genetic variation in the FA composition of adipose tissue triacylglycerols, with breed differences observed in studies comparing Jersey and Limousin (Malau-Aduli et al., 1998), Holstein and Japanese Black (Zembayashi, Nishimura, Lunt, & Smith, 1995) and Brahman and Hereford (Huerta-Leidenz et al., 1993). However, in the phospholipid fraction, the total amount of SFA, MUFA, and PUFA does not differ among crossbred groups (Malau-Aduli et al., 1998), because certain amounts of unsaturated fatty acids are required to maintain the physical properties of the cell at body temperature of mammals (Nakamura & Nara, 2004). On the other hand, animals with genetic predisposition for fat deposition show higher MUFA concentrations in intramuscular fat than other breeds studied (Zembayashi et al., 1995), such that Wagyu crossbred cattle typically display a MUFA to SFA ratio of 1.5:1 or greater

(Middleton et al., 1998). In our work, a positive correlation between C18:1 cis-9 and intramuscular fat was also observed (r = 0.59, P = 0.01, data not shown), and it can be argued that the greater amount of cis-9 MUFA found in Texel x Polwarth lambs could be associated with a higher expression of Δ 9 desaturase (Stearoyl-CoA desaturase, the enzyme responsible for the conversion of C14:0, C16:0, and C18:0 to their cis-9 monounsaturated counterpart) as has been shown in cattle (Bressan et al., 2011). However, our crude estimates of Δ 9 desaturase activity, obtained by product-substrate ratios (Kazala et al., 1999), did not differ significantly among the two crosses, even though they were close to significance for C16 Δ 9 desaturase (P = 0.083). Nevertheless, it must be recognized that the activity of Δ9 desaturase estimated this way is just an approximation, as it is assumed that the SFA present in intramuscular fat arise just from de novo synthesis, and the possibility of uptake of exogenous SFA (pre-formed FA and the ones arising from diet that go through re-esterification to form triacylglycerol from glycerol, mono or diacylglycerol) is ignored. Overall, there was some indication that the activity of Δ9 desaturase was higher for Texel x Polwarth lambs, mostly substantiated as increased deposition of MUFA. High amounts of PUFA were described by Díaz et al. (2005) in meat from Uruguayan light and heavy lambs, with intramuscular fat around 3% and 6% and total PUFA of about 14% and 10%, respectively. In our work, the means for PUFA were higher, possibly due to the lower amount of intramuscular fat (De Smet et al., 2004), which was about one-third to one-fifth of that found in light and heavy lambs by Díaz et al. (2005). The lower amounts of fat found in Texel x Polwarth and Texel x Corriedale lambs may be the result of the higher deposition of n−3 and n−6 PUFA series, which inhibit the activity of Δ 9 desaturase (Kim, Miyazaki, & Ntambi, 2002; Ntambi, 1999) and repress the expression of enzymes involved in the de novo synthesis (fatty acid synthase complex). In our work, the restrictive effect of PUFA on Δ 9 desaturase activity may be inferred from the relationship observed between C18:2n-6 and C18:1 cis-9 (r = − 0.78, P b 0.01, data not shown), while the repression of the fatty acid synthase complex is suggested by the relationship between C18:2n6 and C16:0 (r = − 0.51, P = 0.04, data not shown). The higher deposition of total PUFA in Texel x Corriedale lambs was largely due to increased amounts of total n−6 PUFA, which resulted from a higher deposition of C18:2n-6 (2% higher). On the other hand, the total amount of n-3 PUFA was not different for the two crossbred groups and, when individual FA were considered, only C22:5n-3 showed differences between crosses. In the metabolism of n−6 and n− 3 PUFA series, the desaturation and elongation reactions are mediated by Δ 4, Δ 5, Δ 6 desaturase and elongase enzymes, resulting in the synthesis of highly unsaturated FA, which are esterified into phospholipids that are constituents of cellular membranes and contribute to membrane fluidity (Nakamura & Nara, 2004), and precursors of regulating molecules called eicosanoids (prostaglandins, thromboxanes and leukotrienes). The Δ 4, Δ 5, Δ 6 desaturase and elongase enzymes are shared by the biosynthetic pathways of n−6 and n−3 PUFA, even though, in this metabolism, preference is given to n−3 over n−6 FA precursors in mammalian tissues (Chapkin, 2008). Consequently, the similar deposition of n-3 PUFA between Texel x Polwarth and Texel x Corriedale lambs suggest that there was similarity in substrate (C18:3n-3) availability in the two crossbred groups, but the higher deposition of C22:5n-3 in Texel x Corriedale lambs suggests a lower activity of Δ 4 desaturase while the higher deposition of C18:2n-6 is an indicator of lower Δ 6 desaturase activity. Considering the recommendations of the World Health Organization (World Health Organization, 2003) regarding human diets, both Texel x Polwarth and Texel x Corriedale lamb meats meet the daily recommended intake of fat, cholesterol, SFA, PUFA and n−3 FA, as well as the nutritional recommendation for a n−6/n−3 PUFA ratio b4:1 and a P/S ratio >0.4 (Enser et al., 2001).

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5. Conclusions Overall, the two crossbred groups of lambs had similar meat quality characteristics, and it is likely that differences between meat originating from Texel x Polwarth and Texel x Corriedale are too small to be detected from the consumer standpoint. Meat produced by both crossbred types was lean (fat content b 1.4%) and with a high content of total PUFA (>16% of the total fatty acids), which is thought to be a consequence of the inclusion of white clover in pasture-finishing. These results indicate that a differentiated type of lamb meat can be obtained under this production system, with a higher nutritional value than that obtained in conventional systems. As a consequence, the recognition and labeling of this meat, possibly as a Protected Geographical Indication or a Protected Designation of Origin, could provide an added-value product which would be important for a better sustainability of farming in southern Brazil. Acknowledgments This work was funded by the Brazilian institutions: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), Universidade Federal de Lavras (UFLA), and the Portuguese Institutions: Instituto Nacional de Recursos Biológicos (INRB) and Fundação para a Ciência e Tecnologia (FCT). Individual grants to P. B. Faria, J. O. Vieira, J. Vicente-Neto and S. P. B. Ferrão are acknowledged. The authors wish to thank the Federal Inspection Service of Brazil for facilitating this research. References AOAC (1995). Official methods of analysis (16th ed.). Washington, DC: Association of Official Analytical Chemists. Assann, A. L., Pelissari, A., Moraes, A., Assmann, T. S., Oliveira, E. B., & Sandini, I. (2004). Produção de gado de corte e acúmulo de matéria seca em sistema de integração lavoura-pecuária em presença e ausência de trevo-branco e nitrogênio. Revista Brasileira Zootecnia, 33, 37–44. Bandinelli, D. G., Gatiboni, L. C., Trindade, J. P. P., Quadros, F. L. F., Kaminski, J., Flores, J. P. C., et al. (2005). Composição florística de pastagem natural afetada por fontes de fósforo, calagem e introdução de espécies forrageiras de estação fria. Ciência Rural, 35(1), 84–91. Belury, M. A. (2002). Dietary conjugated linoleic acid in health: Physiological effects and mechanisms of action. Annual Review of Nutrition, 22, 505–531. Bernués, A., Olaizola, A., & Corcoran, K. (2003). Labelling information demanded by European consumers and relationships with purchasing motives, quality and safety of meat. Meat Science, 65, 1095–1106. Bohac, C. E., Rhee, K. S., Cross, H. R., & Ono, K. (1988). Assessment of methodologies for colorimetric cholesterol assay of meats. Journal of Food Science, 53, 1642–1645. Bonagurio, S., Pérez, J. R. O., Furusho-Garcia, I. F., Bressan, M. C., & Lemos, A. L. S. C. (2003). Qualidade da carne de cordeiros Santa Inês puros e mestiços com Texel abatidos com diferentes pesos. Revista Brasileira de Zootecnia, 32, 1981–1991 (S.2). Bragagnolo, N., & Rodriguez-Amaya, D. B. (2001). Determinação de colesterol em carne: comparação de um método colorimétrico e um método por cromatografia líquida de alta eficiência. Revista do Instituto Adolfo Lutz, 22, 1–13. Bressan, M. C., Rossato, L. V., Rodrigues, E. C., Alves, S. P., Bessa, R. J. B., Ramos, E. M., et al. (2011). Genotype x environment interactions for fatty acid profiles in Bos indicus and Bos taurus finished on either pasture or grain. Journal of Animal Science, 89, 221–232. Cartwright, T. C. (1970). Selection criteria for beef cattle for the future. Journal of Animal Science, 30, 706–711. Chapkin, R. S. (2008). Reappraisal of the essential fatty acids. In C. K. Chow (Ed.), Fatty acids in food and their health implications (pp. 675–692). (3. ed.). Boca Raton, FL, USA: CRC Press. De Smet, S., Raes, K., & Demeyer, D. (2004). Meat fatty acid composition as affected by fatness and genetic factors: A review. Animal Research, 53, 81–98. Dewhurst, R. J., Delaby, L., Moloney, A., Boland, T., & Lewis, E. (2009). Nutritive value of forage legumes used for grazing and silage. Irish Journal of Agricultural and Food Research, 48, 167–187. Díaz, M. T., Álvarez, I., De la Fuente, J., Sañudo, C., Campo, M. M., Oliver, M. A., et al. (2005). Fatty acid composition of meat from typical lamb production systems of Spain, United Kingdom, Germany and Uruguay. Meat Science, 71, 256–263. Dimster-Denk, D., Rine, J., Phillips, J., Scherer, S., Cundiff, P., DeBord, K., et al. (1999). Comprehensive evaluation of isoprenoid biosynthesis regulation in Saccharomyces cerevisiae utilizing the Genome Reproter Matrix™. Journal of Lipid Research, 40, 850–860.

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