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Effects of breed, sex, and halothane genotype on fatty acid composition of pork longissimus muscle¹

S. Zhang^*, T. J. Knight, K. J. Stalder^,2, R. N. Goodwin, S. M. Lonergan and D. C. Beitz

^* Department of Biochemistry, Biophysics, and Molecular Biology, and and Department of Animal Science, Iowa State University, Ames 50010

	Abstract

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The objective of this study was to estimate the effects of breed, sex, and halothane genotype on fatty acid composition and several fatty acid indices of lipid extracted from porcine LM. Purebred Yorkshire (n = 436), Duroc (n = 353), Hampshire (n = 218), Spotted (n = 187), Chester White (n = 173), Poland China (n = 124), Berkshire (n = 256), and Landrace (n = 187) pigs (n = 1,934; 1,128 barrows and 806 gilts) from 1991, 1992, 1994, and 2001 National Barrow Show Sire Progeny Tests were used. Pigs were classified as the HAL-1843 normal (NN) genotype (n = 1,718) or the HAL-1843 carrier (Nn) genotype (n = 216). For statistical analysis, a mixed model was used that included fixed effects of breed, sex, halothane genotype, test, slaughter date, interaction of breed x sex, and random effects of sire and dam within breed. Breed significantly affected the concentration of individual fatty acids, total lipid content, and the values of several fatty acid indices of LM. Duroc pigs had the greatest (P < 0.01) content of total SFA. Total MUFA concentration in Poland China pigs was greater (P < 0.05) than in all other breeds except the Spotted (P > 0.05). The concentrations of total PUFA were greater (P < 0.01) in Hampshire, Landrace, and Yorkshire pigs compared with those of other breeds. Significant sex differences for individual fatty acids were detected. Compared with gilts, barrows had greater (P < 0.01) concentrations of SFA and MUFA but lower (P < 0.01) total PUFA. Halothane genotype was a significant source of variation for the percentages of some fatty acids. Pigs with the carrier (Nn) genotype had lower concentrations of SFA (P < 0.05) and MUFA (P < 0.01) but a greater concentration of PUFA (P < 0.01) compared with NN pigs. There were significant negative correlations between total lipid content and individual PUFA and significant positive correlations between lipid concentration and most individual SFA and MUFA. In conclusion, the results suggest that breed and sex are important sources of variation for fatty acid composition of LM.

Key Words: breed • fatty acid • halothane genotype • longissimus muscle • pig • sex

	INTRODUCTION

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION IMPLICATIONS LITERATURE CITED

 
Meat fatty acid composition is of great interest because of its implications for human health. High intake of SFA causes elevated plasma cholesterol, which contributes to cardiovascular disease (Bronte-Stewart et al., 1956). In contrast, PUFA and MUFA increase hepatic low-density lipoprotein receptor activity, thereby decreasing the circulating concentration of LDL-cholesterol (Woollett et al., 1992; Rudel et al., 1995). Nutritional concern about dietary fat, especially SFA, has stimulated the production of leaner pigs in the past 2 decades. However, low content of intramuscular fat (IMF) is believed to negatively impact pork flavor (De-Vol et al., 1988). Manipulation of the fatty acid composition of IMF, therefore, plays an important role in producing healthier pork without compromising consumer acceptable palatability.

Fatty acid composition of IMF in pigs is affected by environmental factors, such as diet, and by genetic factors, such as breed, sex, and halothane genotype (De-Smet et al., 2004). Numerous studies have shown that fatty acid composition of pig muscle and adipose tissue can be changed through modified feeding strategies (Gatlin et al., 2002, Kouba et al., 2003; Nürnberg et al., 2005). In contrast, the effects of genetic factors, especially breed and halothane genotype, have received less attention (Piedrafita et al., 2001; Wood et al., 2004; LoFiego et al., 2005). This study is the first to investigate the effects of breed on fatty acid composition using pigs of all of the 8 major swine breeds in the United States when fed similar diets. Determining the extent to which genetic factors affect the variation of fatty acid composition will provide breeders a tool to modify the fatty acid composition of pork and minimize the negative consequences for pork quality.

The objective of this study was to determine the influence of breed, sex, and halothane genotype on the fatty acid composition of LM lipids of purebred pigs fed the same diets.

	MATERIALS AND METHODS

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Animals
Animal care and use approval was not obtained for this study because the data were from an existing database. In brief, the following procedures were used to generate the data within the database.

Pigs (n = 1,934) of 8 purebred breeds from the 1991, 1992, 1994, and 2001 National Barrow Show Sire Progeny Test program (George A. Hormel and Co., Austin, MN) were used in the current study. The breeds were Yorkshire (n = 436), Duroc (n = 353), Hampshire (n = 218), Spotted (n = 187), Chester White (n = 173), Poland China (n = 124), Berkshire (n = 256), and Landrace (n = 187). Pigs were delivered to the Northwest Iowa Testing Station (New Hampton, IA) at approximately 8 wk of age and were penned by breed, sire group, and weight in a solid-concrete-floored, open-front building and given 1.4 m² of pen space per pig. Pigs within contemporary groups were fed the same diets. The diets of all pigs consisted of ground shelled corn, soybean meal, and supplements, which met or exceeded NRC (1988, 1998) requirements for all phases throughout these grow-finish studies. Additionally, incorporation of contemporary group within the statistical model used to evaluate these data accounts for dietary differences across contemporary groups. Halothane genotypes of the pigs were determined using the HAL-1843 test described by Fujii et al. (1991). Distribution of the breeds by year, sex, and HAL-1843 genotype is shown in Table 1. Pigs were weighed weekly and transported to George A. Hormel Company for slaughter at a BW of approximately 103 kg.

Fatty Acid Analysis
Total lipids were extracted from the LM samples using a chloroform and methanol (2:1, vol:vol) mixture (Folch et al., 1957). The lipids were methylated directly with acetyl chloride and methanol according to Lepage and Roy (1986). Fatty acid methyl esters (FAME) were quantified by a gas chromatograph (model 3400, Varian, Palo Alto, CA) equipped with a Supelco SP-2380 column (30 m long x 0.25 mm i.d. x 0.20 µm film thickness) and a flame ionization detector. The column began at a temperature of 100°C and was ramped to 170°C at a rate of 2°C/min, followed by an increase to 180°C at 0.5°C/min and to 250°C at 10°C/min. The total running time was 62 min. The temperature of the injector was programmed to increase from a beginning temperature of 68°C to a final temperature of 250°C at a rate of 250°C/min. The detector was maintained at 220°C.

Peaks of FAME were identified by comparing the retention time with the commercially available FAME standards (Nu-Chek-Prep Inc., Elysian, MN). The fatty acid compositions were calculated using the peak areas and expressed on a weight percentage basis. The activities of 9-desaturase and elongase were estimated by relating the percentage of product to the percentage of precursor (Pan et al., 1995; Okada et al., 2005). Specifically, the 9-desaturase (16) index was calculated as 100 times the ratio of the palmitoleic acid (C16:1) percentage to the sum of C16:1 and palmitic acid (C16:0). The 9-desaturase (18) index was calculated as 100 times the ratio of oleic acid (C18:1) to the sum of C18:1 and stearic acid (C18:0). The 9-desaturase (16+18) index was calculated as 100 times the ratio of the sum of C16:1 and C18:1 to the sum of C16:1, C16:0, C18:1, and C18:0. The elongase index was calculated as the ratio of C18:0 to C16:0. The thioesterase index was calculated as the ratio of C16:0 to myristic acid (C14:0). The index of atherogenicity (IA) was calculated according to Ulbricht and Southgate (1991).

Statistical Analysis
Least squares means (±SE) were determined using a mixed linear model (PROC MIXED, SAS Inst. Inc., Cary, NC) that included the fixed effects of breed, sex, halothane genotype, test, slaughter date (contemporary group), the interaction of breed x sex, and random effects of sire and dam within breed. Means were compared using pairwise t-tests (PDIFF option of SAS) and declared to be different at P < 0.05. Residual correlation coefficients between the traits were calculated using a fixed effects model with breed, sex, halothane genotype, test, slaughter date, and the interaction between breed x sex in a multivariate ANOVA in PROC GLM of SAS.

	RESULTS AND DISCUSSION

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Breed Effects
Breed was a significant source of variation for the percentage of individual fatty acids and the content of total lipids (Table 2). The concentration of each fatty acid in LM of Duroc pigs differed from that of Yorkshire and Landrace pigs (P < 0.05). Similarly, the percentage of each fatty acid differed between Chester White and Yorkshire pigs (P < 0.05). No significant fatty acid percentage differences were observed between Yorkshire and Landrace pigs. The lipid content of LM was greatest in Duroc pigs (P < 0.01). Berkshire pigs had the second greatest (P < 0.05) concentration of lipid but did not differ (P > 0.05) from Poland China pigs. In contrast, Yorkshire, Landrace, and Hampshire pigs had the lowest lipid content (P < 0.01). It has been shown that Duroc pigs have greater lipid content than Berkshire (Suzuki et al., 2003) and Landrace pigs (Lo et al., 1992). Similarly, Wood et al. (2004) reported that IMF content was relatively high and backfat lipid content was relatively low in Duroc pigs, whereas marbling and backfat lipid contents were high in Berkshire pigs. Newcom et al. (2004) reported that Duroc and Chester White pigs had the greatest IMF, whereas Landrace and Yorkshire pigs had the lowest IMF, which were not different from Hampshire and Poland China pigs.

Breed was a significant source of variation for both the thioesterase and elongase indices (Table 3). Landrace, Yorkshire, Hampshire, and Spotted pigs had a greater thioesterase index than Duroc and Chester White pigs (P < 0.05). Thioesterase in the fatty acid synthase complex is responsible for terminating the cycles of fatty acid synthesis and release of the newly synthesized fatty acid. Both C14-acyl ACP and C16-acyl ACP are substrates for thioesterase, even though C16:0 is the major product. The ratio of C16:0 to C14:0 was utilized to reflect the selective cleavage of thioesterase on C14-acyl ACP or C16-acyl ACP; the greater the thioesterase index, the less cleavage of C14-acyl ACP. The elongase index was greater (P < 0.05) in Landrace, Yorkshire, and Duroc than in the other breeds. The elongation of fatty acids occurs in the mitochondria and microsomal membranes, but the predominant site for elongation is the endoplasmic reticulum membrane. Generally, the mitochondrial elongation system uses fatty acyl CoA substrates in the range of C10-C14, whereas microsomal elongases act on C16 and longer fatty acids (Harwood, 1994). In the current study, the ratio of C18:0 to C16:0 was used to represent the enzyme activity of elongase on C16:0.

Berkshire pigs had the greatest percentage of C16:1, whereas Yorkshire and Landrace had the lowest concentrations of C16:1 (P < 0.05; Table 2). Oleic acid (C18:1) content was greater (P < 0.01) in Poland China, Spotted, Chester White, and Duroc pigs than that in Berkshire, Yorkshire, Landrace, and Hampshire. In addition, Poland China pigs had greater concentration of C18:1 (P < 0.05) than did Chester White and Duroc pigs. Because C18:1 is a major component of the total lipid, approximately 45% of the total fatty acids, the trend for differences in total MUFA content was similar to that of C18:1. The concentration of total MUFA was greater in Poland China (P < 0.05) than in all other breeds except Spotted. Our results were consistent with those of Mason et al. (2005), who found that Landrace pigs had lower C16:1 and C18:1 in LM than did Duroc pigs. Loins from Duroc pigs had greater content of lipid than did loins from Landrace, Berkshire, and Hampshire pigs. The increase in IMF content is in large part attributed to the increase in neutral lipid content, but not phospholipid (PL) content (Fernandez et al., 1999; Wood et al., 2004). Consequently, the percentage of tri-acylglycerol (TAG) in total lipid tended to be greater with increasing IMF content. Oleic acid makes up approximately 40% of total fatty acid content of TAG, whereas it makes up only about 10% of total fatty acid content of PL (Wood et al., 2004). It is possible that the greater content of TAG in LM of Duroc pigs can be attributed, at least in part, to the greater concentration of C18:1 in total lipid of Duroc pigs compared with Landrace, Berkshire, and Hampshire pigs.

The concentration of linoleic acid (C18:2) was greatest in Hampshire pigs (P < 0.05; Table 2). Yorkshire and Landrace pigs had the second greatest (P < 0.01) content of C18:2. The content of C18:2 in Duroc pigs was lower (P < 0.01) than that of all other breeds except Poland China (P > 0.05; Table 2). Linoleic acid cannot be synthesized in vivo in pigs and, therefore, exclusively reflects dietary intake. The concentration of C18:2 was negatively correlated with the lipid content with an overall correlation of –0.68 (P < 0.01). This correlation occurs because pigs with less IMF content tend to have lower de novo fatty acid synthesis and, consequently, have greater concentration of dietary fatty acids incorporated into their tissues (Wood et al., 1989). In the current study, pigs from breeds with less lipid content in LM, such as Hampshire, Yorkshire, and Landrace, had greater concentration of C18:2, whereas pigs from breeds with greater lipid content in LM had lower concentration of C18:2 (Table 2). These results indicate that the differences in C18:2 content observed in the current study may be the result of differences in lipid content of LM among breeds, which might be attributed further to differences in amount of de novo fatty acid synthesis among breeds. Similarly, arachidonic acid (C20:4) and total PUFA concentrations were greater (P < 0.01) in Hampshire, Yorkshire, and Landrace than in the other breeds (Table 2). These results were consistent with those of Cameron and Enser (1991), which showed that Duroc pigs had greater concentration of total SFA and MUFA and lower content of PUFA in lipid of their LM than did Landrace pigs.

Of the SFA, including C14:0, C16:0, and C18:0, dietary C14:0 is considered to have the most harmful cardiovascular effect on humans, with almost 4 times the effect of C16:0 (Hegsted et al., 1965; Keys et al., 1974), whereas C18:0 is believed to be neutral in effect (Bonanome and Grundy, 1988). The ratio of total PUFA to SFA (P:S ratio) has been widely used as a lipid quality indicator in relation to atherogenicity. However, the IA developed by Ulbricht and Southgate (1991) is considered to be a better atherogenicity measure of dietary lipids because it includes MUFA and places more weight on C14:0 (Kinsella et al., 1990; Ulbricht and Southgate, 1991). In the current study, Hampshire pigs had the greatest and Landrace and Yorkshire had the second greatest P:S ratio (Table 2), whereas the P:S ratio for the Duroc pigs was the lowest. The IA of LM from Hampshire pigs (IA = 0.46) was lower (P < 0.05) than that of all other breeds except the Spotted. In contrast, Duroc pigs had the greatest IA, which was 17% greater than that of Hampshire pigs (P < 0.05). Chester White, Berkshire, and Poland China pigs had the same P:S ratio, but their IA differed significantly from each other (Table 2). The P:S ratio of Spotted pigs was lower than that of Yorkshire, Landrace, and Hampshire pigs, but the IA of Spotted pigs did not differ from that of these 3 breeds (Table 2). Leszczynski et al. (1992) found that the P:S ratio of lipid in LM increased 25 or 54% in the pigs fed a 10 or 20% extruded full-fat soybean (FFS) diet for 6 wk compared with pigs fed a corn-soybean meal diet. However, the atherogenic indices calculated from their data were 0.48, 0.46, and 0.48 for 10% FFS, 20% FFS, and control groups, respectively, which were very similar. These results suggest that the assessment of lipid quality depends on the selection of indicators.

Sex Effects
Sex was a highly significant source of variation for the percentage of each individual fatty acid (Table 3). The concentrations of C14:0, C16:0, C18:0, C16:1, and C18:1 were greater (P < 0.01) in barrows than in gilts. In contrast, the percentages of 18:2 and 20:4 were greater (P < 0.01) in gilts than in barrows. Consequently, barrows had greater (P < 0.01) total SFA and MUFA than gilts, whereas gilts had 21% more (P < 0.01) total PUFA than barrows (Table 3). The P:S ratio was 26% greater (P < 0.01) in gilts than in barrows. Gilts also had a smaller (P < 0.01) IA than barrows. The indices of ⁹-desaturase, thioesterase, and elongase did not differ between the 2 sex groups (P < 0.05), indicating similar enzyme activities in barrows and gilts. The effects of sex were different in the 8 breeds, as indicated by significant breed x sex interactions for the percentages of C16:0, C16:1, C18:0, C18:2, and C20:4, total SFA, MUFA, and PUFA, IA, and P:S ratio.

The sex effect results from the current study were consistent with those of Nürnberg et al. (2005), who reported that barrows had greater SFA and lower PUFA than gilts in total lipid of LM. A previous study of the fatty acid composition of longissimus muscle showed significant effects of sex on several fatty acids (Leszczynski et al., 1992). Warnants et al. (1999) reported that barrows had greater concentration of C16:0, C18:0, and total SFA in backfat and greater content of C16:0 in the total lipid of IMF than gilts. In agreement with previous studies (Leszczynski et al., 1992; Warnants et al., 1996), barrows have greater IMF content than gilts. The PL content of LM in barrows is similar to that of gilts, and the difference in IMF content between barrows and gilts is likely attributable to the difference in the content of TAG (Warnants et al., 1996). The IMF of barrows, therefore, contains more TAG than that of gilts. Because the fatty acid composition of TAG differs greatly from that of PL, the differences in fatty acid composition of LM between gilts and barrows observed in the current study are in part the result of differences in TAG content.

Halothane Genotype Effects
Table 4 shows the fatty acid composition of LM by halothane genotype. All 3 HAL-1843 genotypes, NN, Nn, and HAL-1843 positive (nn), were detected in the test pigs. However, there were so few nn pigs that they were dropped from the current study. Halothane genotype was a significant source of variation for the percentages of some, but not all, fatty acids. Pigs with NN genotype had more 16:0 and 18:1 and less 18:2 and 20:4 than did Nn pigs (P < 0.01; Table 4). Consequently, the total SFA and MUFA concentrations and IA were greater (P < 0.05 and P < 0.01, respectively) in NN pigs, whereas the total PUFA concentration and P:S ratio were less (P < 0.01) in Nn pigs. No significant difference in the indices of ⁹ desaturase, thioesterase, and elongase were observed between the 2 HAL 1843 genotypes, indicating similar enzyme activities. Our results were contrary to those of Piedrafita et al. (2001), which suggested that HAL 1843 genotype had significant effects on the percentages of several fatty acids in adipose tissue of NN, Nn, and HAL 1843 positive (nn) pigs, but the mean values for NN and Nn pigs were very similar in their study. Pigs with the NN genotype have greater marbling than pigs with nn (Stalder et al., 1998; Piedrafita et al., 2001) and Nn (Hamilton et al., 2000; Maddock et al., 2002). Our data supported these results by showing that the lipid content was greater (P < 0.01) in NN than in Nn pigs (Table 4).

	IMPLICATIONS

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Per capita pork consumption in the United States decreased by 10% between 1960 and 2003, according to the United States Department of Agriculture, Economic Research Service. Health concerns over fat intake, especially saturated fatty acids, is one of the factors contributing to this decline. Significant breed differences in fatty acid composition of longissimus muscle were observed in the current study. These differences may be sufficient to be exploited through selection to design a more healthful pork product for nutrition-conscious consumers.

	Footnotes

 
¹ This paper of the Iowa Agriculture and Home Economics Experiment Station, Ames, Project No. 3801, was supported by Hatch Act and State of Iowa funds.

² Corresponding author: stalder{at}iastate.edu

Received for publication April 14, 2006. Accepted for publication October 17, 2006.

	LITERATURE CITED

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION IMPLICATIONS LITERATURE CITED

 


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