A review of the factors influencing the development of intermuscular adipose tissue in the growing pig

Meat Science 88 (2011) 213–220

Contents lists available at ScienceDirect

Meat Science j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / m e a t s c i

Review

A review of the factors influencing the development of intermuscular adipose tissue in the growing pig Maryline Kouba a,b,⁎, Pierre Sellier c,d a

INRA, UMR 1079 Systèmes d'Elevage, Nutrition Animale et Humaine, 35590 Saint-Gilles, France Agrocampus Ouest, UMR 1079 Systèmes d'Elevage, Nutrition Animale et Humaine, 35000 Rennes, France, Université Européenne de Bretagne, France c INRA, UMR1313 Génétique Animale et Biologie Intégrative, 78350 Jouy-en-Josas, France d AgroParisTech, UMR1313 Génétique Animale et Biologie Intégrative, 75231 Paris 05, France b

a r t i c l e

i n f o

Article history: Received 17 May 2010 Received in revised form 10 January 2011 Accepted 10 January 2011 Keywords: Pig Intermuscular fat Environmental effects Genetic effects

a b s t r a c t Compared with subcutaneous or abdominal fat depots of pig carcasses, intermuscular fat displays a number of original properties. It cannot be easily removed from fresh or processed meat delivered to consumers and has therefore an influence on consumer acceptability of pork. Particular compositional characteristics of intermuscular fat include low lipid content and small size of adipocytes. How age (or body weight), gender, castration, environmental temperature, feeding restriction, diet composition, as well as genetic factors affect intermuscular fat development and composition are surveyed in this review paper. Up to now, few studies have specifically dealt with the intermuscular compartment of body fat while very abundant information is available on the subcutaneous one. As a general rule, any factor, either genetic or non-genetic, which causes a decrease of whole carcass fat deposition generates a higher relative importance of the intermuscular fraction of total fat as well as an increased degree of unsaturation of constituent fatty acids. © 2011 Elsevier Ltd. All rights reserved.

Contents 1. 2.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Non-genetic factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Development, partition, and composition of pig adipose tissues with age . . . . . . . . . . . . 2.1.1. Development of the different body tissues with age. . . . . . . . . . . . . . . . . . 2.1.2. Changes in cellularity of adipose tissue during pig growth . . . . . . . . . . . . . . 2.1.3. Comparative development of the different adipose tissues during growth . . . . . . . 2.2. Effect of gender and castration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Effect of environmental temperature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4. Effect of exogenous hormones . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.5. Effect of nutrition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.5.1. Food restriction or energy restriction . . . . . . . . . . . . . . . . . . . . . . . . 2.5.2. Dietary protein level . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Genetic factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Breed differences in body fat partition . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Within-breed genetic variation in fat partition and composition . . . . . . . . . . . . . . . . 3.3. Effect of within-population selection for backfat thickness on body fat partition and composition 3.4. Effects of single genes or QTL on body fat partition . . . . . . . . . . . . . . . . . . . . . . 4. Conclusion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . .

213 214 214 214 214 214 215 215 215 216 216 216 216 216 217 217 217 218 218

1. Introduction ⁎ Corresponding author. AGROCAMPUS-OUEST, UMR 1079 SENAH, 65 rue de Saint Brieuc, 35042 Rennes cedex, France. Tel.: + 33 223485367; fax: + 33 223485900. E-mail address: [email protected] (M. Kouba). 0309-1740/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.meatsci.2011.01.003

Reduction of fat deposition has been a major goal in the continuing improvement of pork production for the last five or six decades.

214

M. Kouba, P. Sellier / Meat Science 88 (2011) 213–220

Breeding for leaner pigs has led to a decrease in total carcass fat from 35–45% to less than 20% today for a commercial slaughter pig (Nguyen, McPhee, & Wade, 2004; Tribout et al., 2004). Although the newborn piglet is quite lean with less than 10 g mobilizable fat per kg body weight (Le Dividich et al., 1991), carcass fat increases rapidly with age (Henry, 1977; Mersmann, Allen, Steffen, Brown, & Danielson, 1976; Schinckel, Mahan, Wiseman, & Einstein, 2008). Body fat is deposited in different anatomical locations as subcutaneous, perirenal, intermuscular (between muscles) or intramuscular (within muscle) fat. Among these fat depots, subcutaneous fat accounts for 60 to 70% of total body fat, intermuscular fat for 20 to 35%, and perirenal fat for about 5% (Kouba, Bonneau, & Noblet, 1999; Monziols, Bonneau, Davenel, & Kouba, 2005; Mourot & Kouba, 1995; Wood, Whelehan, Ellis, Smith, & Laird, 1983). The quantitative importance of subcutaneous fat in the pig is the major reason why selection against adiposity has been mainly based on the reduction of subcutaneous fat, another practical reason being that the dorsal part of subcutaneous fat is easy to access for measuring fat depths and thus predicting carcass fatness on the live animal. These various deposits do not have the same importance with regard to carcass and meat quality. Perirenal and subcutaneous fats can be easily trimmed off the lean meat that is delivered to the consumers whereas, in most instances, intermuscular fat cannot be removed. Therefore, intermuscular fat content has a great impact on consumer acceptability of meat commodities containing several muscles, such as pork chops or processed ham slices. The partitioning of the different adipose tissues in the pig carcass is influenced by intrinsic factors such as age (or body weight), gender, genotype, and environmental (extrinsic) factors such as feeding, temperature, castration, use of exogenous hormones. The aim of this paper is to examine the effect of these factors on growth and chemical composition of the intermuscular adipose tissue (and other adipose tissues, for comparison) in the pig. Non-genetic effects and then genetic effects will be considered. 2. Non-genetic factors 2.1. Development, partition, and composition of pig adipose tissues with age 2.1.1. Development of the different body tissues with age Growth and development of porcine lean and fat tissues have extensively been studied, because these traits strongly affect economy of pig production. As shown by McMeekan (1940), muscle and bone develop first, with muscle growing relatively quickly and bone relatively slowly, and when fat formation accelerates during the latter growth stages, rates of muscle and bone deposition decline. These basic features have been verified by numerous authors on modern-type pigs (Davies, 1974; Tess, Dickerson, Nienaber, & Ferrell, 1986; Wagner, Schinckel, Chen, Forrest, & Coe, 1999). 2.1.2. Changes in cellularity of adipose tissue during pig growth According to Anderson and Kauffman (1973), pig adipose tissue development is due to cellular hyperplasia between 7 and 20 kg, to both hyperplasia and hypertrophy between 20 and 70 kg, and to cellular hypertrophy alone above this body weight. So, the increase of fat deposits during pig growth is mainly due to an increase in adipocyte size. 2.1.3. Comparative development of the different adipose tissues during growth A number of studies have thoroughly described the growth of adipose tissues in relation to body weight using the classical allometric approach. They consistently show that the relative growth of intermuscular fat is slower than those of subcutaneous and perirenal fat (Table 1). However, Jones, Richmond, Price, and Berg (1980) found that relative growth coefficients (b) for intermuscular and subcutaneous

depots were similar for the hind quarter, but the intermuscular depot coefficient was slightly higher for the fore quarter. It was also found by Kouba and Bonneau (2009) that growth of intermuscular adipose tissue in relation to carcass weight was similar to that of subcutaneous fat, perirenal fat exhibiting by far the fastest relative growth. Anderson, Kauffman, and Kastenschmidt (1972) compared the lipid content of several adipose tissues in 170 kg body weight pigs and found that intermuscular adipose tissue was the lowest in lipid content and perirenal fat was the highest whereas backfat was intermediate in this respect. This pattern was confirmed by Wood, Buxton, Whittington, and Enser (1986). Duran-Montgé, Realini, Barroeta, Lizardo, and Esteve-Garcia (2008) showed that subcutaneous and flare fat had the highest lipid content, next was intermuscular fat and finally it was intramuscular fat in 100 kg body weight gilts. Recently, Monziols, Bonneau, Davenel, and Kouba (2007) and Kouba and Bonneau (2009) confirmed these results in 115 kg body weight pigs, and in 30, 70 and 110 kg body weight pigs, respectively. Eggert, Grant, and Schinckel (2007) reached the same conclusions for subcutaneous and intermuscular adipose tissues, in all the carcass cuts they examined (boston, ham, loin, and picnic), and for perirenal fat. Moreover, they found a small effect of body weight on lipid content of adipose tissue, when they compared 105 kg, 120 kg and 135 kg body weight pigs. It is indeed known that adipose tissue exhibits a very large enrichment in lipids in the few first weeks of life whereas the augmentation of lipid content is much weaker afterwards (Moody, Enser, Restall, & Lister, 1978). As far as lipogenesis is concerned, Mourot, Kouba, and Peiniau (1995) and Mourot, Kouba, and Bonneau (1996) showed that the activities of acetyl-CoA carboxylase, malic enzyme and glucose-6phosphate dehydrogenase were the lowest in neck subcutaneous adipose tissue, the highest in backfat and leaf fat, and intermediate in ham intermuscular adipose tissue in Large White and Meishan pigs. Mourot and Kouba (1999) compared two intermuscular adipose tissues (in ham and shoulder) in Large White and Meishan pigs. The evolution of lipogenic enzyme activities was very similar in both tissues, with a peak of acetyl-CoA carboxylase activity at 40 kg body weight in Large White pigs, and a peak at 20 kg body weight in Meishan pigs (Table 2). The between-adipose tissue differences in lipid content are mainly related to adipocyte size. Anderson et al. (1972) showed that cell size followed the same pattern as lipid content: perirenal adipose tissue possessed the largest cells and intermuscular adipose tissue the smallest, subcutaneous adipose tissue being intermediate. Lee and Kauffman (1974a;1974b) also showed that smaller adipocytes have greater amounts of water relative to lipid than larger adipocytes. This is consistent with the lower water content of perirenal fat compared with backfat (Sellier, Maignel, & Bidanel, 2010). It has been known for a long time (Dean & Hilditch, 1933) that the unsaturation degree of fat deposits in the pig follows a negative gradient from outside to inside. Monziols et al. (2005), among others, confirmed this feature and found that the degree of unsaturation of intermuscular adipose tissue is lower than that of subcutaneous adipose tissue, but is higher than that of perirenal fat. The lower degree of unsaturation of intermuscular adipose tissue compared to subcutaneous adipose tissue is due to a lower concentration of both mono- and poly-unsaturated fatty acids. These results on intermuscular adipose tissue were recently confirmed by Duran-Montgé et al. (2008). The average compositional and histological characteristics of intermuscular, subcutaneous, and perirenal fats are summarized in Table 3. 2.1.3.1. Relative development of adipose tissues in the cuts. The relative development of subcutaneous and intermuscular adipose tissues in the different primal cuts (belly, ham, loin, and shoulder) has commanded some attention from research workers (Fisher, Green, Whittemore, Wood, & Schofield, 2003; Kempster & Evans, 1979; Kouba & Bonneau,

M. Kouba, P. Sellier / Meat Science 88 (2011) 213–220

215

Table 1 A list of literature estimates for allometric coefficients (b)a of subcutaneous, intermuscular, perirenal, and intramuscular fats in pig carcasses. Period of growth

Independent variable

b for subcutaneous fat

b for intermuscular fat

b for perirenal fat

b for intramuscular fat

Authors

8 to 62 kg live weight 55 to 125 kg live weight 112 to 452 days of age (“low plane of nutrition”) 112 to 165 days of age (“high plane of nutrition”) 15 to 120 kg live weight 30 to 140 kg live weight 35 to 115 kg live weight (Piétrain) 35 to 115 kg live weight (Landrace)

Total side fat Total fat Total fat

1.01 1.01 1.02

0.97 0.87 0.98

1.08 1.24 1.22

0.91

Davies and Pryor (1977) Kempster and Evans (1979) Davies (1983)

Total fat

1.01

0.97

1.37

Davies (1983)

Total fat Total fat Side weight Side weight

1.04 1.00 1.43 1.69

0.91 0.96 1.21 1.234

1.21 1.31

Wood et al. (1983) Kouba and Bonneau (2009) Fisher et al. (2003) Fisher et al. (2003)

a When b = 1, the rate of growth of the fat depot is equal to that of the independent variable, whereas when b b 1 or when b N 1, the rate of growth of the fat depot is slower or faster, respectively, than that of the independent variable.

2009; Mohrmann et al., 2006; Wood et al., 1983). There is however some difficulty in comparing the results of these studies because cutting and dissection methods are very different. Table 4 shows the allometric coefficients for the two adipose tissues in the different carcass cuts. There is some dissimilarity among anatomical locations. In the belly, intermuscular fat grows more rapidly than subcutaneous fat whereas the reverse is observed in the ham. However, unlike subcutaneous adipose tissue, the kinetics of deposition of intermuscular fat does not seem to be homogenous during pig growth. It appears from the results given by Richmond and Berg (1971a) that this adipose tissue develops first in the pig (it represents 18% of total fat in 23 kg body weight pigs, while subcutaneous fat represents 78%), then its development slows down with the increasing live weight, along with an increase in the deposition of subcutaneous adipose tissue (intermuscular fat represents 13% of total fat in 114 kg body weight pigs and subcutaneous fat 84%). The quick development of intermuscular fat in the belly leads to “fat bellies” that are difficult to valorise in traditional French heavy pigs. Hence, further studies are needed for a better understanding of this particular adipose tissue. 2.2. Effect of gender and castration It is well known that there is a strong effect of gender on carcass fatness in the pig. Martin, Fredeen, Weiss, and Carson (1972) showed that boars had substantially less total backfat, perirenal fat, intermuscular and intramuscular fat depots than gilts. However, Fortin, Wood, and Whelehan (1987) found that at the same weight of total side fat (8 · 80 kg), entire males have more intermuscular and less subcutaneous fat than females. Castration is also well known to cause a large increase in pig fatness (Henry, 1977). Many authors showed that carcasses from intact males are markedly leaner than those from castrated males (e. g., Desmoulin, Bonneau, & Bourdon, 1974; Knudson, Hogberg, Merkel, Allen, & Magee, 1985; Martin et al., 1972; Wood & Riley, 1982; Wood et al., 1986). Wood and Riley (1982) also showed that the ratio of intermuscular to subcutaneous fat is higher in boars than in castrates. Lee, Kauffman,

and Grummer (1973) showed that castration of pigs led to an increase in fat deposition mainly due to a stronger hypertrophy of adipocytes. Eggert et al. (2007) showed that lipid content of both subcutaneous and intermuscular adipose tissues was higher in barrows than in gilts, while there was no difference in lipid content of perirenal fat. 2.3. Effect of environmental temperature Regarding environmental temperature, a range of 18 to 21 °C has generally been found to be the most convenient for optimal performance of growing-finishing pigs. Environmental temperature is known to affect body weight gain, voluntary energy intake, heat production, ham composition and adipose tissue characteristics (e. g. degree of unsaturation) in the growing pig (Fuller, Duncan, & Boyne, 1974; Le Dividich, Noblet, & Bikawa, 1987; Lefaucheur et al., 1991). Numerous reports indicate that prolonged exposure to high environmental temperatures, as compared to cold or moderate ones, enhances fat accumulation at internal sites (perirenal fat, viscera), at the expense of external sites such as subcutaneous backfat (Katsumata, Kaji, & Saitoh, 1996; Le Dividich et al., 1987; Lefaucheur et al., 1991). However, Lefaucheur et al. (1991) found no influence of a high environmental temperature on intermuscular fat percentage. 2.4. Effect of exogenous hormones Administration of porcine somatotropin (pST) to finishing pigs reduces voluntary feed intake, improves growth performance (particularly feed efficiency), and results in decreased rates of lipid accretion and total accumulation of adipose tissue mass. Protein accretion is increased concurrently, due to increased muscle growth (Bonneau, 1992; Campbell et al., 1988;1989a;1989b; Etherton et al., 1986). According to Sorensen, Oksbjerg, Agergaard, and Petersen (1996), the

Table 3 Compositional and histological characteristics of subcutaneous, intermuscular, and perirenal fats. Derived from Anderson et al. (1972), Eggert et al. (2007), and Wood et al. (1986). Adipose tissue

Table 2 Lipogenic enzyme activities in various adipose tissues of Large White and Meishan pigs. Derived from Mourot et al. (1995) and Mourot et al. (1996). Lipogenic enzyme

Subcutaneous Subcutaneous Intermuscular Perirenal fat fat fat fat (neck region) (dorsal region)

Acetyl-CoA-carboxylase Malic enzyme Glucose-6-phosphate dehydrogenase

+ + +

+++ +++ +++

++ ++ ++

+++ +++ +++

The number of crosses indicates the relative level of the enzyme activity under consideration in the different adipose tissues.

Trait

Subcutaneous

Intermuscular

Perirenal

Composition Water Lipid Unsaturation degree Fat free dry matter

++ ++ +++ ++

+++ + ++ +++

+ +++ + +

Histology Adipocyte size Number of adipocytes

++ ++

+ +++

+++ +

The number of crosses indicates the relative level of the trait under consideration in the different adipose tissues.

216

M. Kouba, P. Sellier / Meat Science 88 (2011) 213–220

Table 4 Compared allometric coefficients (b) of subcutaneous and intermuscular fats in different pig carcass cuts. Period of growth

Independent variable

Carcass cut

b for subcutaneous fat

b for intermuscular fat

Authors

35 to 115 kg live weight

Total weight of the considered adipose tissue in the side

Total fat in the cut

1.05 0.84 1.01 0.98 1.08 1.21 0.97 1.00 1.07 1.02

1.34 0.90 0.91 0.69 1.30 1.12 1.03 1.00 0.82 0.94

Fisher et al. (2003)

30 to 140 kg live weight

Belly Shoulder Pelvic limb Flank Foreloin Hindloin Belly Shoulder Ham Loin

Kouba and Bonneau (2009)

When b = 1, the rate of growth of the fat depot is equal to that of the independent variable, whereas when b b 1 or when b N 1, the rate of growth of the fat depot is slower or faster, respectively, than that of the independent variable.

decrease of fat deposition rate exhibited by pST-treated pigs is of the same order for intermuscular and subcutaneous fat fractions. Kramer, Bergen, Grant, and Merkel (1993) found that administration of pST to pigs led to a decreased lipid percentage in both intermuscular and subcutaneous adipose tissues. Conversely, Clark, Wander, and Hu (1992) showed that total lipid content was significantly decreased by pST treatment in subcutaneous adipose tissue, but not in intermuscular adipose tissue or Longissimus muscle. Clark et al. (1992) showed that administration of pST led to decreased contents of saturated and monounsaturated fatty acids (expressed as grams of fatty acids per 100 g of wet tissue) in both subcutaneous and intermuscular adipose tissues, but the polyunsaturated fatty acid content was not affected by the treatment. They also found no effect of somatotropin on muscle fatty acid composition whereas Kramer et al. (1993) found a slight effect on this composition, with a decreased proportion of palmitic and stearic acids. Effects of numerous β-adrenergic agonist (β-AA) compounds have been described in the literature, but it appears that no author has examined these effects for intermuscular adipose tissue characteristics. 2.5. Effect of nutrition 2.5.1. Food restriction or energy restriction Kempster and Evans (1979) showed that ad libitum-fed pigs were more mature in terms of body fat partition with more perirenal fat and less intermuscular fat at equal total fat weight, compared to restrictedfed pigs. This result was confirmed by Davies, Pearson, and Carr (1980). However, in the study of Richmond and Berg (1971b), pigs were fed ad libitum a high or a low energy ration, and those fed the high energy ration had a greater percentage of intermuscular fat than did those fed the low energy diet (15.3 vs 14.2%). 2.5.2. Dietary protein level Wood et al. (2004) compared a conventional and a low crude protein diet (20 and 16%, respectively) in entire males from four breeds. There was a breed by diet interaction for intermuscular fat development but not for subcutaneous fat development in the foreloin. The low protein diet led to an increase of intermuscular fat percentage in Large White and Berkshire pigs and, to a lesser extent, in Duroc pigs, whereas there was no significant diet effect on this trait in Tamworth pigs. Low protein diet was associated with a markedly decreased ratio of intermuscular to subcutaneous fat in the Duroc (a breed known for the particularly high value of this ratio, as mentioned later) whereas diet effect was of small magnitude in the three other breeds. 3. Genetic factors 3.1. Breed differences in body fat partition Evaluating differences between breeds raised in the same environment is the easiest way to obtain first indications of genetic

variation for any trait. Over the last decades, a number of breed comparisons have included the partition of fat deposition in the growing pig among the traits studied. As a general rule, when two populations (breeds or crosses) differing in whole carcass fatness are compared, the diminution of intermuscular fat depot in the leanest population is proportionately less important than that of subcutaneous fat depot in this population. This inverse relationship between subcutaneous and intermuscular fractions of total fat is well illustrated by the results obtained by Kouba et al. (1999) in a comparison between five genetic types of pigs, namely Chinese Meishan, Meishan × Large White, Large White, Piétrain, and a “lean” synthetic sire line. This study dealt with a considerable range of variation in global adiposity since the carcass fat percentage of Meishan purebreds was about two-fold that of pigs from the synthetic line. The ratio of intermuscular to subcutaneous fat weight was approximately 0.5 in the synthetic line, 0.3 in Meishan, and around 0.4 in Large White. Certain breeds, however, do not fit exactly into the general pattern consisting of a linear gradient of increasing ratio of intermuscular to subcutaneous fat with decreasing carcass fatness. The Piétrain and, to a lesser extent, the Duroc are the main “outlier” breeds in this respect. Even taking into account that the Piétrain is a lean breed, the ratio of intermuscular to subcutaneous fat appears to be particularly high in the Pietrain (Gispert et al., 2007; Kouba et al., 1999). Carcasses from purebred or crossbred Duroc pigs also exhibit much higher intermuscular fat weights than could be expected from their “medium” overall fatness (Cameron, 1990a; Candek-Potokar, Monin, & Zlender, 2002; Jones et al., 1980; Kolstad, 2001; Smith & Pearson, 1986; Wood et al., 2004). The Hampshire tends to display the same picture as the Duroc (Goenaga & Carden, 1979; Richmond & Berg, 1971b; Smith, Pearson, & Purchas, 1990). Specific breed effects, independent from global carcass fatness, have therefore a substantial impact on intermuscular relative to subcutaneous fat deposition. Moreover, it may be pointed out that such specific breed effects are also true for the relative importance of other sites of fat deposition in the growing pig. For example, the Landrace is known for having a particularly strong propensity to deposit body cavity fat, e.g. perirenal fat (Bout, Girard, Runavot, & Sellier, 1989; Cameron, 1990a; Gispert et al., 2007; Kolstad, 2001). High intramuscular fat levels relative to total fat are exhibited by the Duroc (Cameron, 1990a; Goodwin & Burroughs, 1995) and, to a lesser extent, by the Piétrain (Guéblez, Sellier, Fernandez, & Runavot, 1993; Hartmann, Otten, Kratzmair, Berrer, & Eichinger, 1992). Hence, the particular position of Duroc and Piétrain breeds in terms of body fat partition is encountered for both intramuscular and intermuscular fat deposition. The between-breed variation pattern for compositional traits of fat depots (lipid to water ratio, fatty acid profile) closely follows that for whole carcass fatness. It is well established that breeds with higher carcass fatness exhibit lower proportions of polyunsaturated fatty acids and higher proportions of saturated fatty acids and lipid to water ratios in subcutaneous and internal fat depots. In the breed comparison

M. Kouba, P. Sellier / Meat Science 88 (2011) 213–220

(Piétrain vs German Landrace) performed by Hartmann et al. (1992), the breed difference in total lipid content of adipose tissue was markedly higher in the fat depot richer in lipids (backfat) than in the fat depot poorer in lipids (intermuscular fat). 3.2. Within-breed genetic variation in fat partition and composition In the study carried out by Cameron (1990a) on Duroc and Landrace pigs, heritability (h2) estimates for weight and percentage of intermuscular fat (0.49 and 0.26, respectively) were lower than those for weight and percentage of subcutaneous fat (0.66 and 0.62, respectively). The correlation between the weights, percentages or areas of these two fat depots is close to 0.50 at both phenotypic and genetic levels (Cameron, 1990a; Hermesch, 2008). Heritability estimates reported by Suzuki, Inomata, Katoh, Kadowaki, and Shibata (2009) for several carcass cross sectional fat areas of Duroc pigs agreed with those of Cameron (1990a) with significantly higher values for subcutaneous fat areas (0.56–0.71) than for intermuscular fat areas (0.16–0.41). Estimates of genetic correlations (rA) between ultrasonic backfat thickness and weights, percentages or areas of adipose tissues are 0.8– 0.9 for subcutaneous fat and only 0.5–0.7 for intermuscular fat whereas corresponding phenotypic correlations are of the order of 0.7 and 0.3–0.4, respectively (Cameron, 1990a; Hermesch, 2008; Suzuki et al., 2009). Phenotypic and genetic correlations between weight or cross sectional area of intermuscular fat and intramuscular fat content (Longissimus muscle) range from 0.2 to 0.4 according to Cameron (1990b) and Suzuki et al. (2009) and are therefore of a smaller magnitude than those involving intermuscular and subcutaneous fat weights. Results reported by Newcom, Baas, Schwab, and Stalder (2005) along with those of numerous earlier studies – for review, see Sellier (1998) – have shown that genetic correlations between intramuscular fat content and various subcutaneous fat measurements are also moderate and average around 0.3. Regarding the respective fatty acid profiles of subcutaneous, intermuscular and intramuscular fat depots, Suzuki et al. (2006) found that heritability estimates were moderate to high and grossly similar among depots in Duroc pigs (e.g., 0.40 to 0.54, 0.26 to 0.44, and 0.32 to 0.44 for C18:0, C18:1 and C18:2 concentrations, respectively). Genetic correlations “between” adipose tissues for the concentration of a given fatty acid were higher than 0.4, except for the relationships between intramuscular fat and other adipose tissues for C18:2 content. The genetic association of C18:2 content of intermuscular fat with that of the inner layer of subcutaneous fat (rA = 0.75) was closer than with that of the outer layer of subcutaneous fat (rA = 0.53). Heritability values for fatty acid composition were found by Schwörer, Morel, Prabucki, and Rebsamen (1990) to be comparable among inner and outer layers of backfat, perirenal fat and belly fat. According to Sellier et al. (2010), the genetic correlation ‘between’ backfat and perirenal fat for the coefficient of unsaturation of lipids is less than unity (rA = 0.57 ± 0.05) while being markedly closer than the genetic correlations between coefficients of unsaturation of backfat (or perirenal fat) and muscle lipids (rA ~ 0.15). Considering the network of genetic relationships between homologous quantitative and qualitative characteristics of subcutaneous, intermuscular, perirenal and intramuscular fat depots therefore reinforces the idea that these adipose tissues, though being genetically linked to each other, are not a unique fat deposition trait from a genetic point of view. It appears that intermuscular fat is genetically ‘closer’ to subcutaneous than to intramuscular fat in most of homologous characteristics. 3.3. Effect of within-population selection for backfat thickness on body fat partition and composition Whether classical selection for low ultrasonic backfat thickness affects fat deposition at different body sites, including the intermus-

217

cular level, has been investigated in some experimental studies. The first authors to tackle this question were Wood et al. (1983) who evaluated the partition of fat between subcutaneous, intermuscular and abdominal depots in a Large White line selected primarily for reduced backfat thickness during ten generations, compared with a control line. There was no significant evidence that selection had caused relocation of body fat from subcutaneous to the others sites of fat deposition, but overall responses to selection remained rather small for average backfat thickness (− 3 mm) and carcass fat percentage (−2.7 points). Studying the same genetic material some years later but in a separate experiment based on a different dissection method, Rook, Ellis, Whittemore, and Phillips (1987) reached slightly different conclusions since they found some significant or marginally significant indications of a redistribution of body fat away from subcutaneous and perirenal fat depots and towards the intermuscular fat depot. However, more pronounced modifications of fat partition under the effect of selection were found by Cameron and Curran (1995) in a set of Large White lines divergently selected on lean tissue growth rate or lean tissue feed conversion. The deviation of “lean” lines from “fat” lines averaged 5 points for the percentage of separable fat in the dissected carcass side (trait 1). Whichever divergent lines were compared, the observed line divergence, expressed in phenotypic standard deviation units of the trait, was markedly larger for subcutaneous fat weight than for intermuscular or perirenal fat weights. The percentage of intermuscular fat relatively to total separable fat (trait 2) was therefore augmented, by 4.5 points on average, in the different lean lines compared to their respective fat counterparts. This result is in line with the estimates of genetic parameters reported in the preceding section. Moreover, this withinbreed negative genetic association between traits 1 and 2 appears to be in broad agreement with the across-breed relationship mentioned above. Available results pertaining to the effects of within-breed selection against backfat thickness on chemical composition of fat depots have consistently shown that subcutaneous adipose tissue becomes “softer” due to an increased water to lipid ratio and to a higher degree of unsaturation of lipids, which essentially results from an enrichment in linoleic acid (Scott, Cornelius, & Mersmann, 1981b; Tribout et al., 2004; Wood et al., 1978). These correlative responses to selection are in excellent agreement with the estimates of genetic correlations between carcass fatness and compositional traits of subcutaneous fat (Cameron, 1990b; Sellier et al., 2010). Regarding cellularity of subcutaneous adipose tissue, pigs from the ‘obese’ line studied by Scott, Cornelius, and Mersmann (1981a) had a two-fold higher backfat thickness than pigs from the ‘lean’ line derived from the same Yorkshire–Duroc background, and they approximately exhibited a two-fold greater adipocyte volume with, consequently, fewer cells per gram of tissue. Experimental evidence is lacking about the effects of selection for reduced backfat thickness on the compositional traits of adipose tissues other than the subcutaneous one. Results reported by Cameron and Enser (1991) and Sellier et al. (2010) suggest that the change in fatty acid profile of intramuscular lipids would be limited. In contrast, compositional traits of perirenal fat (except lipid content) would be modified to the same extent as those of subcutaneous backfat (Sellier et al., 2010). 3.4. Effects of single genes or QTL on body fat partition A number of single genes known at the DNA level have been reported as exerting a more or less pronounced influence on fat deposition traits in pigs. Most of them are involved in various pathways of adipogenesis or lipid metabolism whereas some others participate in regulation of appetite and energy intake. Regarding the RYR1/HAL gene, many comparisons between DNAbased halothane genotypes have been carried out since the mid-1990s

218

M. Kouba, P. Sellier / Meat Science 88 (2011) 213–220

for carcass composition traits, including those pertaining to adipose tissue development in growing pigs (e. g., Larzul et al., 1997; Thaller et al., 2000). Only one of these comparisons (Garcia-Macias et al., 1996) specifically considered the intermuscular adipose depot among fatness-related traits. Only NN and Nn genotypes were dealt with in this study and no influence of halothane genotype was found for percentage of intermuscular fat in the carcass as well as for percentages of total, subcutaneous and intramuscular fat. One can also hypothesize that the fatty acid profile of intermuscular fat is essentially unaffected since Garcia-Macias et al. (1996) and Tor et al. (2001) did not find any significant effect of halothane genotype in this respect for subcutaneous fat. Since the establishment of the first pig genome maps in the mid1990s, an impressive amount of research work has been accomplished worldwide for detecting QTL, i.e. chromosomal regions which are shown, with the aid of anonymous genetic markers, to encompass at least one locus influencing the trait under study. Initially, QTL mapping studies dealing with growth and carcass traits were based on F2 crosses between largely divergent populations such as wild boar or Iberian, Berkshire, Chinese Meishan breeds on one side, and usual commercial breeds (Large White, Landrace, Duroc, Piétrain, and Hampshire) on the other side. More recently, resource populations relying on commercial breeds were increasingly used in QTL studies. Microsatellite markers have essentially been used in pig genome-wide scans in the past 15 years, but recourse begins to be made to a new class of markers consisting of single nucleotide polymorphisms (SNP) and allowing a considerably higher density of genome coverage. To the best of our knowledge, no pig QTL mapping study has dealt up to now with traits pertaining to comparative development and chemical composition of intermuscular fat. 4. Conclusion Intermuscular fat cannot be easily trimmed from the meat, and consequently, it is a complete part of the meat that the consumer will purchase. So, a high content of intermuscular fat may negatively affect the acceptability of fresh pork and processed pork products by consumers. Intermuscular fat is a particular fat depot in several respects. Compared with subcutaneous and perirenal fats, its protein content is intermediate, its lipid content is the lowest and these lipids are localized in smaller adipocytes. Its degree of unsaturation is intermediate, being higher than that of perirenal fat but lower than that of subcutaneous fat. The growth rate of intermuscular fat relatively to carcass weight is lower than, or equal to, that of subcutaneous adipose tissue. However, it grows more rapidly than subcutaneous fat in some carcass cuts, in particular in the belly that can become excessively fat in heavy pig production systems. The development of intermuscular adipose tissue seems to be determined at an early stage, before 20 kg of body weight, especially in lean breeds such as Pietrain. Classical selection for increased carcass leanness, essentially based on backfat depth recording, appears to be less successful for reducing intermuscular than for reducing subcutaneous fats in pigs, and that is particularly true in the leanest animals. Among common pig breeds, Pietrain and Duroc exhibit a particularly strong development of intermuscular fat resulting in high values of the ratio of intermuscular to subcutaneous fat. In conclusion, little is known about the genetic and non-genetic control of intermuscular fat development and composition in pigs. Because of its importance in meat acceptability by the consumer, further research is needed for a better knowledge of this particular adipose tissue, in order to find ways to exert a better control of its development. On one hand, comparative transcriptomic profiles of the different adipose tissues, in the line of the approach used by Ferraz et al. (2008), could provide us with novel insights to the physiological character-

ization of these tissues. On the other hand, the availability of a highdensity (~ 50 K) pig SNP chip at an affordable price today opens new avenues for conducting whole-genome association studies in a more efficient way and identifying gene polymorphisms of interest more thoroughly.

References Anderson, D. B., & Kauffman, R. G. (1973). Cellular and enzymatic changes in porcine adipose tissue during growth. Journal of Lipid Research, 14, 160−168. Anderson, D. B., Kauffman, R. G., & Kastenschmidt, L. L. (1972). Lipogenic enzyme activities and cellularity of porcine adipose tissue from various anatomical locations. Journal of Lipid Research, 13, 593−599. Bonneau, M. (1992). Administration de GRF ou de somatotropine chez le porc et les volailles : effets sur les performances, la qualité des viandes et la fonction de reproduction. INRA Productions animales, 5, 257−267. Bout, J., Girard, J. P., Runavot, J. P., & Sellier, P. (1989). Genetic variation in chemical composition of fat depots in pigs. Proceedings 40th Annual Meeting of the European Association for Animal Production (GP3-12), August 1989 27–31, Dublin, Ireland. Cameron, N. D. (1990a). Comparison of Duroc and British Landrace pigs and the estimation of genetic and phenotypic parameters for growth and carcass traits. Animal Production, 50, 141−153. Cameron, N. D. (1990b). Genetic and phenotypic parameters for carcass traits, meat and eating quality traits in pigs. Livestock Production Science, 26, 119−135. Cameron, N. D., & Curran, M. K. (1995). Responses in carcass composition to divergent selection for components of efficient lean growth rate in pigs. Animal Science, 61, 347−359. Cameron, N. D., & Enser, M. B. (1991). Fatty acid composition of lipids in longissimus dorsi muscle of Duroc and British Landrace pigs and its relationships with eating quality. Meat Science, 29, 295−307. Campbell, R. G., Steele, N. C., Caperna, T. J., McMurtry, J. P., Solomon, M. B., & Mitchell, A. D. (1988). Interrelationships between energy intake and endogenous porcine growth hormone administration on the performance, body composition, and protein and energy metabolism of growing pigs weighing 25 to 55 kilograms live weight. Journal of Animal Science, 66, 1643−1655. Campbell, R. G., Steele, N. C., Caperna, T. J., McMurtry, J. P., Solomon, M. B., & Mitchell, A. D. (1989a). Effects of exogenous porcine growth hormone administration between 30 and 60 kilograms on the subsequent and overall performance of pigs grown to 90 kilograms. Journal of Animal Science, 67, 1265−1271. Campbell, R. G., Steele, N. C., Caperna, T. J., McMurtry, J. P., Solomon, M. B., & Mitchell, A. D. (1989b). Interrelationships between sex and exogenous growth hormone administration on performance, body composition, and protein and fat accretion of growing pigs. Journal of Animal Science, 67, 177−186. Candek-Potokar, M., Monin, G., & Zlender, B. (2002). Pork quality, processing, and sensory characteristics of dry-cured hams as influenced by Duroc crossing and sex. Journal of Animal Science, 80, 988−996. Clark, S. L., Wander, R. C., & Hu, C. Y. (1992). The effect of porcine somatotropin supplementation in pigs on the lipid profile of subcutaneous and intermuscular adipose tissue and longissimus muscle. Journal of Animal Science, 70, 3435−3442. Davies, A. S. (1974). A comparison of tissue development in Pietrain and Large White pigs from birth to 64 kg live weight. 1. Growth changes in carcass composition. Animal Production, 19, 367−376. Davies, A. S. (1983). Growth and development of pigs: A reanalysis of the effects of nutrition on body composition. Journal of Agricultural Science, Cambridge, 100, 681−687. Davies, A. S., Pearson, G., & Carr, J. R. (1980). The carcass composition of male, castrated male and female pigs resulting from two levels of feeding. Journal of Agricultural Science, Cambridge, 95, 251−259. Davies, A. S., & Pryor, W. J. (1977). Growth changes in the distribution of dissectable and intramuscular fat in pigs. Journal of Agricultural Science, Cambridge, 89, 257−266. Dean, H. K., & Hilditch, T. P. (1933). The body fats of the pig. III. The influence of body temperature on the composition of depot fats. The Biochemical Journal, 27, 1950−1956. Desmoulin, B., Bonneau, M., & Bourdon, D. (1974). Etude en bilan azoté et composition corporelle des porcs mâles entiers ou castrés de race Large White. Journées de la Recherche Porcine en France, 6, 247−255. Duran-Montgé, P., Realini, C. E., Barroeta, A. C., Lizardo, R., & Esteve-Garcia, E. (2008). Tissue fatty acid composition of pigs fed different fat sources. Animal, 2(12), 1753−1762. Eggert, J. M., Grant, A. L., & Schinckel, A. P. (2007). Factors affecting fat distribution in pork carcasses. The Professional Animal Scientist, 23, 42−53. Etherton, T. D., Wiggins, J. P., Chung, C. S., Evock, C. M., Rebhun, J. F., & Walton, P. E. (1986). Stimulation of pig growth performance by porcine growth hormone and growth hormone-releasing factor. Journal of Animal Science, 63, 1389−1399. Ferraz, A. L. J., Ojeda, A., Lopez-Béjar, M., Fernandes, L. T., Castello, A., Folch, J. M., & Pérez-Enciso, M. (2008). Transcriptome architecture across tissues in the pig. BMC Genomics, 9, 173. Fisher, A. V., Green, D. M., Whittemore, C. T., Wood, J. D., & Schofield, C. P. (2003). Growth of carcass components and its relation with conformation in pigs of three types. Meat Science, 65, 639−650. Fortin, A., Wood, J. D., & Whelehan, O. P. (1987). Breed and sex effects on yje development, distribution of muscle, fat and bone, and the partotition of fat in pigs. Journal of Agricultural Science, 108, 141−153.

M. Kouba, P. Sellier / Meat Science 88 (2011) 213–220 Fuller, M. F., Duncan, W. R. H., & Boyne, A. W. (1974). Effect of environmental temperature on the degree of unsaturation of depot fat of pigs given different amounts of food. Journal of the Science of Food and Agriculture, 25, 205−210. Garcia-Macias, J. A., Gispert, M., Oliver, M. A., Diestre, A., Alonso, P., Munoz-Luna, A., Siggens, K., & Cuthbert-Heavens, D. (1996). The effects of cross, slaughter weight and halothane genotype on leanness and meat and fat quality in pig carcasses. Animal Science, 63, 487−496. Gispert, M., Fonti Furnols, M., Gil, M., Velarde, A., Diestre, A., Carrion, D., Sosnicki, A. A., & Plastow, G. S. (2007). Relationships between carcass quality parameters and genetic types. Meat Science, 77, 397−404. Goenaga, P. R., & Carden, A. E. (1979). A comparison of tissue weight distribution in Landrace, Hampshire and Duroc Jersey pigs. Journal of Agricultural Science, Cambridge, 93, 271−280. Goodwin, R., & Burroughs, S. (1995). Genetic evaluation: Terminal line program results. Des Moines, Iowa, USA: National Pork Producers Council. Guéblez, R., Sellier, P., Fernandez, X., & Runavot, J. P. (1993). Comparaison des caractéristiques physico-chimiques et technologiques des tissus maigre et gras de trois races porcines françaises (Large White, Landrace Français et Piétrain). 1. Caractéristiques du tissu maigre. Journées de la Recherche Porcine en France, 25, 5−12. Hartmann, S., Otten, W., Kratzmair, M., Berrer, A., & Eichinger, H. M. (1992). Effects of breed, halothane genotype and sex on the lipid composition of two skeletal muscles and adipose tissue in swine. Proceedings 38th International Congress of Meat Science and Technology, vol. 2. (pp. 77−80) 23-28 August 1992, Clermont-Ferrand, France. Henry, Y. (1977). Développement morphologique et métabolique du tissu adipeux chez le porc : influence de la sélection, de l'alimentation et du mode d'élevage. Annales de Biologie Animale, Biochimie, Biophysique, 17, 923−952. Hermesch, S. (2008). Genetic relationships between composition of pork bellies and performance, carcase and meat quality traits. Animal, 2, 1178−1185. Jones, S. D. M., Richmond, R. J., Price, M. A., & Berg, R. T. (1980). Effects of breed and sex on the patterns of fat deposition and distribution in swine. Canadian Journal of Animal Science, 60, 223−230. Katsumata, M., Kaji, Y., & Saitoh, M. (1996). Growth and carcass fatness responses of finishing pigs to dietary fat supplementation at a high ambient temperature. Animal Science, 62, 591−598. Kempster, A. J., & Evans, D. G. (1979). The effects of genotype, sex and feeding regimen on pig carcass development. 2. Tissue weight distribution and fat partition between depots. Journal of Agricultural Science Cambridge, 93, 349−358. Knudson, B. K., Hogberg, M. G., Merkel, R. A., Allen, R. E., & Magee, W. T. (1985). Developmental comparisons of boars and barrows: 1. Growth rate, carcass and muscle characteristics. Journal of Animal Science, 61, 789−796. Kolstad, K. (2001). Fat deposition and distribution measured by computer tomography in three genetic groups of pigs. Livestock Production Science, 67, 281−292. Kouba, M., & Bonneau, M. (2009). Compared development of intermuscular and subcutaneous fat in carcass and primal cuts of growing pigs from 30 to 140 kg body weight. Meat Science, 81, 270−274. Kouba, M., Bonneau, M., & Noblet, J. (1999). Relative development of subcutaneous, intermuscular, and kidney fat in growing pigs with different body compositions. Journal of Animal Science, 77, 622−629. Kramer, S. A., Bergen, W. G., Grant, A. L., & Merkel, R. A. (1993). Fatty acid profiles, lipogenesis, and lipolysis in lipid depots in finishing pigs treated with recombinant porcine somatotropin. Journal of Animal Science, 71, 2066−2072. Larzul, C., Le Roy, P., Guéblez, R., Talmant, A., Gogué, J., Sellier, P., & Monin, G. (1997). Effect of halothane genotype (NN, Nn, nn) on growth, carcass and meat quality traits of pigs slaughtered at 95 kg or 125 kg live weight. Journal of Animal Breeding and Genetics, 114, 309−320. Le Dividich, J., Esnault, T., Lynch, B., Hoo-Paris, R., Castex, C., & Peiniau, J. (1991). Effect of colostral fat level on fat deposition and plasma metabolites in the newborn pig. Journal of Animal Science, 69, 2480−2488. Le Dividich, J., Noblet, J., & Bikawa, T. (1987). Effect of environmental temperature and dietary energy concentration on the performance and carcass characteristics of growing-finishing pigs fed to equal rate of gain. Livestock Production Science, 17, 235−246. Lee, Y. B., & Kauffman, R. G. (1974a). Cellular and enzymatic changes with animal growth in porcine intramuscular adipose tissue. Journal of Animal Science, 38, 532−537. Lee, Y. B., & Kauffman, R. G. (1974b). Cellular and lipogenic enzyme activity of porcine intramuscular adipose tissue. Journal of Animal Science, 38, 538−544. Lee, Y. B., Kauffman, R. G., & Grummer, R. H. (1973). Effects of early nutrition on the development of adipose tissue in the pig. II. Weight constant basis. Journal of Animal Science, 37, 1319−1325. Lefaucheur, L., Le Dividich, J., Mourot, J., Monin, G., Ecolan, P., & Krauss, D. (1991). Influence of environmental temperature on growth, muscle and adipose tissue metabolism, and meat quality in swine. Journal of Animal Science, 69, 2844−2854. Martin, A. H., Fredeen, H. T., Weiss, G. M., & Carson, R. B. (1972). Distribution and composition of porcine carcass fat. Journal of Animal Science, 35, 534−541. Acid composition of various tissues. The British Journal of Nutrition, 83, 637−643. McMeekan, C. P. (1940). Growth and development in the pig, with special reference to carcass quality characters. Journal of Agricultural Science, Cambridge, 30, 276−343. Mersmann, H. J., Allen, C. D., Steffen, D. G., Brown, L. G., & Danielson, D. M. (1976). Effect of age, weaning and diet on swine adipose tissue and liver lipogenesis. Journal of Animal Science, 43, 140−150. Mohrmann, M., Roehe, R., Susenbeth, A., Baulain, U., Knap, P. W., Looft, H., Plastow, G. S., & Kalm, E. (2006). Association between body composition of growing pigs determined by magnetic resonance imaging, deuterium dilution technique, and chemical analysis. Meat Science, 72, 518−531.

219

Monziols, M., Bonneau, M., Davenel, A., & Kouba, M. (2005). Tissue distribution in pig carcasses exhibiting large differences in their degree of leanness, with special emphasis on intermuscular fat. Livestock Production Science, 97, 267−274. Monziols, M., Bonneau, M., Davenel, A., & Kouba, M. (2007). Comparison of lipid content and fatty acid composition of intermuscular and subcutaneous adipose tissues in pig carcasses. Meat Science, 76, 54−60. Moody, W. G., Enser, M. B., Restall, D. J., & Lister, D. (1978). Comparison of fat and muscle development in Pietrain and Large White piglets. Journal of Animal Science, 46, 618−633. Mourot, J., & Kouba, M. (1995). Les lipides de la viande de porc. Cahiers de Nutrition et de Diététique, 30, 365−370. Mourot, J., & Kouba, M. (1999). Development of intra- and intermuscular adipose tissue in growing Large White and Meishan pigs. Reproduction, Nutrition, Development, 39, 125−132. Mourot, J., Kouba, M., & Bonneau, M. (1996). Comparative study of in vitro lipogenesis in various adipose tissues in the growing Meishan pig: Comparison with the large White pig (Sus domesticus). Comparative Biochemistry and Physiology, 115B, 383−388. Mourot, J., Kouba, M., & Peiniau, P. (1995). Comparative study of in vitro lipogenesis in various adipose tissues in the growing domestic pig (sus domesticus). Comparative Biochemistry and Physiology, 111B, 379−384. Newcom, D. W., Baas, T. J., Schwab, C. R., & Stalder, K. J. (2005). Genetic and phenotypic relationships between individual subcutaneous backfat layers and percentage of longissimus intramuscular fat in Duroc swine. Journal of Animal Science, 83, 316−323. Nguyen, N. H., McPhee, C. P., & Wade, C. M. (2004). Genetic selection strategies for efficient lean growth in pigs. Pig News and Information, 25, 149N−163N. Richmond, R. J., & Berg, R. T. (1971a). Tissue development in swine as influenced by live-weight, breed, sex and ration. Canadian Journal of Animal Science, 51, 31−39. Richmond, R. J., & Berg, R. T. (1971b). Fat distribution in swine as influenced by liveweight, breed, sex and ration. Canadian Journal of Animal Science, 51, 523−531. Rook, A. J., Ellis, M., Whittemore, C. T., & Phillips, P. (1987). Relationships between whole-body chemical composition, physically dissected carcass parts and backfat measurements in pigs. Animal Production, 44, 263−273. Schinckel, A. P., Mahan, D. C., Wiseman, T. G., & Einstein, M. E. (2008). Growth of protein, moisture, lipid, and ash of two genetic lines of barrows and gilts from twenty to one hundred twenty-five kilograms of body weight. Journal of Animal Science, 86, 460−471. Schwörer, D., Morel, P., Prabucki, A., & Rebsamen, A. (1990). Genetic parameters of intramuscular fat content and fatty acids of pork fat. Proceedings 4th World Congress on Genetics Applied to Livestock Production, vol. 15. (pp. 545−548) 23–27 July 1990, Edinburgh, UK. Scott, R. A., Cornelius, S. G., & Mersmann, H. J. (1981a). Effects of age on lipogenesis and lipolysis in lean and obese swine. Journal of Animal Science, 52, 505−511. Scott, R. A., Cornelius, S. G., & Mersmann, H. J. (1981b). Fatty acid composition of adipose tissue from lean and obese swine. Journal of Animal Science, 53, 977−981. Sellier, P. (1998). Genetics of meat and carcass traits. In M. F. Rothschild, & A. Ruvinski (Eds.), The Genetics of the Pig (pp. 463−510). Wallingford, Oxon, UK: CAB International. Sellier, P., Maignel, L., & Bidanel, J. P. (2010). Genetic parameters for tissue and fatty acid composition of backfat, perirenal fat and longissimus muscle in Large White and Landrace pigs. Animal, 4, 497−504. Smith, W. C., & Pearson, G. (1986). Comparative voluntary feed intakes, growth performance, carcass composition, and meat quality of Large White, Landrace, and Duroc pigs. New Zealand Journal of Experimental Agriculture, 14, 43−50. Smith, W. C., Pearson, G., & Purchas, R. W. (1990). A comparison of the Duroc, Hampshire, Landrace, and Large White as terminal sire breeds of crossbred pigs slaughtered at 85 kg liveweight. 1. Performance and carcass characteristics. New Zealand Journal of Agricultural Research, 33, 89−96. Sorensen, M. T., Oksbjerg, N., Agergaard, N., & Petersen, J. S. (1996). Tissue deposition rates in relation to muscle fibre and fat cell characteristics in lean female pigs (Sus scrofa) following treatment with porcine growth hormone (pGH). Comparative Biochemistry and Physiology Part A, 113, 91−96. Suzuki, K., Inomata, K., Katoh, K., Kadowaki, H., & Shibata, T. (2009). Genetic correlations among carcass cross-sectional fat area ratios, production traits, intramuscular fat, and serum leptin concentration in Duroc pigs. Journal of Animal Science, 87, 2209−2215. Suzuki, K., Ishida, M., Kadowaki, H., Shibata, T., Uchida, H., & Nishida, A. (2006). Genetic correlations among fatty acid compositions in different sites of fat tissues, meat production, and meat quality traits in Duroc pigs. Journal of Animal Science, 84, 2026−2034. Tess, M. W., Dickerson, G. E., Nienaber, J. A., & Ferrell, C. L. (1986). Growth, development and body composition in three genetic stocks of swine. Journal of Animal Science, 62, 968−979. Thaller, G., Dempfle, L., Schlecht, A., Wiedemann, S., Eichinger, H., & Fries, R. (2000). Efect of the MHS locus on growth, carcass and meat quality in F2 crosses between Mangalitza and Pietrain breeds. Archiv fûr Tierzucht, 43, 263−275. Tor, M., Estany, J., Villalba, D., Cubilo, D., Tibau, J., Soler, J., Sanchez, A., & Noguera, J. L. (2001). A within breed comparison of RYR1 pig genotypes for performance, feeding behaviour, and carcass, meat and fat quality traits. Journal of Animal Breeding and Genetics, 118, 417−427. Tribout, T., Caritez, J. C., Gogué, J., Gruand, J., Bouffaud, M., Billon, Y., Péry, C., Griffon, H., Brenot, S., Le Tiran, M. H., Bussières, F., Le Roy, P., & Bidanel, J. P. (2004). Estimation, par utilisation de semence congelée, du progrès génétique réalisé en France entre 1977 et 1998 dans la race porcine Large White: résultats pour quelques caractères de production et de qualité des tissus gras et maigres. Journées de la Recherche Porcine, 36, 275−282.

220

M. Kouba, P. Sellier / Meat Science 88 (2011) 213–220

Wagner, J. R., Schinckel, A. P., Chen, W., Forrest, J. C., & Coe, B. L. (1999). Analysis of body composition changes of swine during growth and development. Journal of Animal Science, 77, 1442−1466. Wood, J. D., Buxton, P. J., Whittington, F. M., & Enser, M. (1986). The chemical composition of fat tissues in the pig: Effects of castration and feeding treatment. Livestock Production Science, 15, 73−82. Wood, J. D., Enser, M. B., MacFie, H. J. H., Smith, W. C., Chadwick, J. P., Ellis, M., & Laird, R. (1978). Fatty acid composition of backfat in Large White pigs selected for low backfat thickness. Meat Science, 2, 289−300.

Wood, J. D., Nute, G. R., Richardson, R. I., Whittington, F. M., Southwood, O., Plastow, G., Mansbridge, R., da Costa, N., & Chang, K. C. (2004). Effects of breed, diet and muscle on fat deposition and eating quality in pigs. Meat Science, 67, 651−667. Wood, J. D., & Riley, J. E. (1982). Comparison of boars and castrates for bacon production. I. Growth data, and carcass and joint composition. Animal Production, 35, 55−63. Wood, J. D., Whelehan, O. P., Ellis, M., Smith, W. C., & Laird, R. (1983). Effects of selection for low backfat thickness in pigs on the sites of tissue deposition in the body. Animal Production, 36, 389−397.