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Genetic correlations among fatty acid compositions in different sites of fat tissues, meat production, and meat quality traits in Duroc pigs

K. Suzuki^*,1, M. Ishida, H. Kadowaki, T. Shibata, H. Uchida and A. Nishida^*

^* Graduate School of Agricultural Science, Tohoku University, 1-1 Tsutsumidori-Amamiyamachi, Aoba-ku, Sendai, Miyagi Prefecture 981-8555, Japan; and Miyagi Agricultural College, Hatatate, Taihaku-ku, Sendai-shi, Miyagi Prefecture 982-0215, Japan; and Miyagi Prefecture Animal Industry Experiment Station, Hiwatashi 1, Iwadeyama-cho, Tamatsukuri-gun, Miyagi Prefecture 989-6445, Japan

	Abstract

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This study estimated genetic parameters for fatty acids of different sites of fat tissue, meat production, and meat quality traits of Duroc pigs selected during 7 generations for ADG, LM area, backfat thickness (BF), and intramuscular fat (IMF). For this study, 394 barrows and 153 gilts were slaughtered at 105 kg of BW. High heritabilities for C18:0 of outer and inner subcutaneous fat tissue were estimated, respectively, as 0.54 and 0.51; those of intermuscular and intramuscular fat were 0.40 and 0.51, respectively. Genetic and phenotypic correlations of ADG and BF with saturated fatty acids of outer and inner subcutaneous fat were positive, but those with C16:1 and C18:2 were negative, and those with C18:1 were nearly zero. Genetic and phenotypic correlations between LM area and respective fatty acids showed opposite results. Respective genetic and phenotypic correlations of melting points with C18:0 and C18:1 were positive and high, and negative and high, respectively. Genetic correlations between cooking loss and SFA (C14:0, C16:0, and C18:0) of IMF were positive and moderate: 0.56, 0.47, and 0.47, respectively. On the other hand, monosaturated fatty acid of C18:1 was highly and negatively correlated with cooking loss (–0.61). Moreover, high genetic correlation between meat color (pork color standard and lightness) and fatty acid compositions of IMF suggest that the SFA (C14:0, C16:0, and C18:0) were correlated genetically with meat lightness and that unsaturated fatty acid compositions (C18:1 and C18:2) were correlated with meat darkness. Results of this study suggest that the fatty acid composition of adipose tissue is correlated genetically with meat production and meat quality traits.

Key Words: Duroc pig • fatty acid • genetic parameter • meat quality • selection

	INTRODUCTION

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION IMPLICATIONS LITERATURE CITED

 
Fatty acid composition and melting point of fatty tissue not only determine the quality of fatty tissue of a carcass, but they also influence the eating quality of meat. It is especially important to improve fat quality in Japan: its residents chiefly consume pork as fresh meat. The quality of accumulated fat is determined according to its fatty acid composition. There is large variation in the melting point of specific fatty acids. For that reason, variation in fatty acid composition has an important effect on firmness or softness of meat fat. This effect is especially true for subcutaneous and intermuscular fat, but it also applies to intramuscular fat (IMF, Wood et al., 2004). Cameron et al. (2000) indicated that neutral lipid PUFA were negatively correlated with pork flavor, flavor preference, and overall acceptability. Monounsaturated fatty acids (C16:1, C18:1) were positively correlated with pork flavor, flavor preference, and overall acceptability. Numerous studies have reported fatty acid compositions of lipids of different muscles and different adipose tissue depots (Rule et al., 1995). Nevertheless, very few reports describe estimates of genetic parameters of fatty acid composition. Especially, it is interesting to know how the fatty acid composition of the IMF is correlated genetically to meat quality traits. Suzuki et al. (2005b) reported selection over 7 generations for meat production traits and IMF fat in the loin. Intramuscular fat increased and some meat qualities changed with selection (Suzuki et al., 2005a). Therefore, the current study is intended to estimate genetic parameters of the fatty acid composition of fatty tissue and meat production and meat quality traits.

	MATERIALS AND METHODS

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Animals and Performance Testing Procedures
The research protocols followed the guidance book for performance test of meat production of pigs in Japan. Duroc pigs used in this experiment were of a line that was selected through 7 generations at the Miyagi Prefecture Animal Industry Experiment Station from 1995 to 2001. Details of the selection method were described previously by Suzuki et al. (2005b). Selection criteria traits were the following: ADG from 30 kg to 105 kg of BW; LM area (LMA), and backfat thickness (BF) at 105 kg of BW measured using ultrasound technology; and IMF measured in slaughtered sib pigs.

The average population of each generation was 15.6 boars and 44.5 gilts. Gilts farrowed only once, and boars were retained for use during one 4- to 6-wk breeding period. Thereby, a new generation was obtained each year. Pigs were weaned at 4 wk. At 8 wk, 1 to 2 male piglets (total of 50 piglets) and 2 to 4 female piglets (total of 100 piglets) from each litter were selected as candidates for boars and gilts based on their respective BW at 8 wk. At that time, about 80 piglets in all, composed of mainly boars and some gilts from each litter, were selected for full sib testing in each generation. This first stage of selection was conducted within litters. Boars for full sib tests were subsequently castrated. Performance tests began when the BW reached 30 kg; testing ended at 105 kg. Backfat thickness and LMA were measured on 105-kg animals on the left side at the position of half of body length using an ultrasound (B-mode) color scanning scope (SR-100, Kaijo Corp., Tokyo, Japan). Computer software (Sanken Corp., Tokyo, Japan) determined LMA.

Pigs were provided ad libitum access to a specially ordered formula feed (15% CP, 78% TDN, 0.76% lysine content, on a DM basis) during the testing periods from 30 to 105 kg of BW. The mixing ratio of this feed was specially ordered for the present experiment and was used constantly during 7 generations. Pigs had free access to water. Boars were reared individually in performance testing pens. Gilts and barrows were reared in growing pens, with group feeding in a concrete-floored building with 8 pigs per pen, which allowed 1.2 m² of floor area per pig.

Selection Method
The objective of this selection experiment was to produce a Duroc line to be used as terminal sires to improve meat production and meat quality traits. Subsequently, these Duroc boars will be supplied to pork producers as commercial terminal sires. Because of the limited accommodation ability of the facilities, selection was conducted without a control line. First and second generations of selection were performed using an index selection method based on relative desired gains (Yamada et al., 1975). Traits that were selected for were ADG, LMA, BF, and IMF. Genetic and phenotypic parameters used to derive selection criteria were obtained, respectively, from performance test data of the first and second generations. Respective means of ADG, LMA, BF, and IMF at the first generation were 865 g, 36.1 cm², 2.34 cm, and 4.3%. Relative desired gains were established, respectively, as 135 g, 3.9 cm², –0.54 cm, and 0.7% for ADG, LMA, BF, and IMF. Consequently, the selection index equation was I = 0.038ADG + 1.38LMA – 15.10BF + 12.63IMF – 56.68.

Selection was made within sire families for boars and within litters for gilts at the first generation to avoid rapid loss of genetic diversity from the population. Breeding values of ADG, LMA, BF, and IMF were estimated from the third generation onward by multiple-trait, animal model BLUP. Breeding values were calculated using the PEST3.1 program (Groeneveld, 1990) after estimating genetic parameters using the VCE4.25 program (Neumaier and Groeneveld, 1998), with the models including generation and sex as fixed effects and random effects of individual additive genetic effect and error. Relative economic weights of selection traits were calculated from the relative desired gains, which were established for ADG, LMA, BF, and IMF from performance test data of the first generation, as described previously. Aggregate breeding values were calculated by multiplying the relative economic weights by the estimated breeding value of each trait; then the selection was executed. Relative economic weights of selection traits were calculated from the relative desired gain.

The relative desired gains of ADG, LMA, BF, and IMF were established from performance test data of the first generation, as described before. However, the breeding goals changed to 1,000 g, 40 cm², 2.0 cm, and 5.0% for ADG, LMA, BF, and IMF, respectively. Therefore, relative desired gain were 135 g, 3.9 cm², –0.34 cm, and 0.7%, respectively, because improvement of the IMF cannot be expected when the BF is thinned too much. When the IMF breeding goal is assumed to be 6%, the weight to IMF becomes too high. Therefore, the respective economic weights were assumed to be 0.076, – 0.391, – 10.850, and 3.753 for ADG, LMA, BF, and IMF, respectively.

However, the genetic parameters estimated at the third generation differed from those of the fifth and seventh generations. The relative economic weights obtained using these parameters were also different. Then, the relative economic weights obtained at the third generation were used for the third and fourth generation, and those at the fifth generation were used for the fifth generation and afterward. The aggregate breeding values were calculated by multiplying the relative economic weights by the estimated breeding value of each trait; then selection was executed. Approximately 15 boars and 50 gilts were selected at each generation. Inbreeding coefficients for individual pigs were computed for each generation. Based on inbreeding information, all mating was planned to minimize the rate of increase in inbreeding.

Carcass Dissection and Meat Quality Measurement
Pigs for full-sib tests (barrows and gilts) were slaughtered using manual, low voltage (200 V) electrical stunning 24 h after feed removal with free access to water. Processed, dressed carcasses were placed in a refrigerator as soon as possible. Carcasses were placed in a conventional chiller at 4°C for 24 h. Subsequently, for measuring meat quality in the LM, a 7- to 10-cm-long piece of the loin (2 thoracic vertebrae sections cranial to the last rib) was taken from the left half of each pig carcass. At that time, pork color was measured using the pork color standard (PCS; 1 = light to 6 = dark; Nakai et al., 1975). Then, the chops were moved to a laboratory to measure meat quality traits.

External loin adipose tissue was removed. The meat was cut vertically along the length of the loin. The sliced meat (about 50 g) was hung by wire in the specimen case. Drip loss was determined by weighing sliced meat stored at 4°C in the refrigerator after 24 h; it was calculated as a percentage of the original weight of the sliced meat. Lightness (L*) was measured using a spectrophotometer (CM-2002, Minolta Co., Ltd., Tokyo, Japan) after cutting and blooming for more than 15 min; pH was also measured. The remaining loin meat section was cut into 2 along the muscle fiber and was used to analyze cooking loss, tenderness, and pliability. Two pieces (2 x 2 x 5 cm) of meat were cut from each, then weighed and packaged in polyethylene bags. They were vacuum-packaged and heated in a warm bath at 70°C for 30 min. Then, after cooling at room temperature, moisture on the meat was wiped off, and the meat weight was measured again. Cooking loss was determined by measuring drippings as a percentage of the original meat weight. Furthermore, 2 cooked pieces per animal were cut to 1 x 1 x 5 cm. Tenderness (kg of force/cm²) was measured using a Tensipresser (TTP-50BXII, Taketomo Electric Corp., Tokyo, Japan) developed by Nakai et al. (1992). This machine was developed to evaluate meat tenderness accurately using an up and down motion to imitate chewing action. Two minced loin meat samples of about 20 g were analyzed using the Soxhlet method to determine IMF.

Fatty Acid Composition Analysis and Melting Point Measurement
The longissimus thoracis muscle and adipose tissue samples from the 11th thoracic vertebrae were collected from the left side of the carcass. Approximately 30 g of LM samples were homogenized in 40 mL of chloroform:methanol (2:1, vol/vol) extract solution; the emulsion was filtered into a separatory funnel. This operation was repeated 3 times. The residue was immersed in 40 mL of the extract solution overnight and then filtered.

The filtrate was added to the same separatory funnel. Adding 30 mL of physiological saline performed fractionation. Then the funnel was shaken vigorously and kept motionless until the 2 phases were separated completely. The lower chloroform phase was collected into a flask with 5 g of unhydrated sodium sulfate and was left overnight. The content was filtered, then evaporated in vacuo using a rotary evaporator at 40°C; the weight of the contents was recorded as total lipids. The lipids were then dissolved with 10 mL of chloroform, and an aliquot was transferred into a test tube with a screw cap and stored under refrigeration. Approximately 3 g of inner and outer subcutaneous and intermuscular fat samples were also obtained from the same thoracic vertebrae as the LM samples. Extraction and methylation processes were done using the same procedures as those described for muscle samples.

One milliliter of the lipid fraction was placed into a test tube with a screw top on a heatblock set at 50°C; the solvent was evaporated by nitrogen flow. Before heating at 100°C for 3 h, 5% sulfuric acid-methanol (2 mL) was added to the mixture. After cooling, 1 mL of petroleum ether and 5 mL of physiological saline were added to the test tube. The test tube was shaken vigorously, then allowed to separate. The petroleum ether phase was subjected to gas chromatography. A Hitachi G-3000 gas chromatography apparatus (Tokyo, Japan) was employed to analyze fatty acids. The apparatus was equipped with a flame ionization detector and fitted with a 0.3 mm x 30 m glass column packed with DB-WAX. Respective temperatures for the flame ionization detector and the column were constant and set at 300 and 210°C. Nitrogen carrier gas was used at a rate of 30 mL/min. Subcutaneous fat was separated into outer and inner layers; their respective melting points were measured using the rising melting point method. Melting points were recorded according to the capillary tube method (AOAC, 1975).

Statistical Analysis
Selection traits of ADG, LMA, BF, and IMF, and respective fatty acid compositions and melting points were used to estimate genetic parameters.

The following multiple-trait animal model was used for analyses to estimate genetic parameters:

where Y_ijklm = observation for traits i, µ_i = common constant for trait i, and G_ij = fixed effect of selection generation j for trait i.

The selection generation effect included the genetic effect of selection and the environmental effect at each generation: S_ik = fixed effect of sex k for trait i, a_il = random additive genetic effect of animal _l for trait i, and e_ijkll = random residual effect for trait i.

Seven generations of pedigree information of 1,642 animals with data of 152 ancestors born before the fourth generation (total of 1,794 animals) were included in these analyses. The VCE4.25 program (Neumaier and Groeneveld, 1998) was used to estimate (co)variance components and their respective SE, heritabilities, and genetic and residual correlations. The GLM procedure of SAS (SAS Inst. Inc., Cary, NC) was used to analyze fatty acid composition data, accounting for fixed effects of generation, sex, site and sex x site interaction, and to test significance.

	RESULTS

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Table 1 lists the least-squares means of fatty acid compositions and melting points for the 4 sites and 2 sexes. Results of ANOVA in the fatty acid composition and melting point indicated that the site effect was significant for all fatty acids and that melting points and the effects of sex were also significant in C16:0, C18:0, and C18:2. Saturated fatty acids, such as C16:0 (P < 0.001) and C18:0 (P = 0.003), are more abundant in inner-layer than in outer-layer subcutaneous fat. Conversely, unsaturated fatty acids of C18:1 and C18:2 are less (P < 0.001) abundant in inner-layer fat than in outer-layer subcutaneous fat. Consequently, the melting point of inner-layer subcutaneous fat is greater (P < 0.001) than that of outer-layer subcutaneous fat. The fatty acid compositions of intermuscular fat and inner-layer subcutaneous fat have a similar ratio. In addition, IMF has more (P < 0.001) monounsaturated fatty acids of C16:1 and C18:1, and less (P < 0.001) PUFA of C18:2 than other fat sites.

Heritability estimates of selection traits and fatty acids are listed respectively in Tables 2 and 3. Respective heritabilities of C18:0 are the greatest in the outer and inner layer subcutaneous fats: 0.54 and 0.51, respectively. Either high (0.51) or moderate (0.40) heritability was estimated for intermuscular and intramuscu lar fat. High heritability for C16:0 (0.79) was estimated for intermuscular fat, but heritability estimates were high or moderate in other tissues. Heritability estimates for C16:1 (0.20 to 0.36), C18:1 (0.26 to 0.44), and C18:2 (0.32 for 0.44), for respective fatty tissues, were moderate. Moreover, high heritabilities (0.56 and 0.61) were estimated for melting points of outer-layer and inner-layer subcutaneous fat (Table 3).

Table 6 shows genetic and phenotypic correlations between the fatty-acid composition of intramuscular fat and meat quality traits. All phenotypic correlations among meat quality traits and intramuscular fatty acids were low. Genetic correlations between cooking loss and SFA of C14:0, C16:0, and C18:0 were respectively positive and moderate: 0.56, 0.47, and 0.47. In contrast, monosaturated fatty acid of C18:1 was highly and negatively correlated with cooking loss (–0.61). Moreover, a high genetic correlation between meat color [PCS and lightness (L*)] and fatty acid compositions suggests that the SFA (C14:0, C16:0, and C18:0) were correlated genetically with meat lightness; moreover, PUFA compositions (C18:2) were associated with meat darkness.

	DISCUSSION

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Heritability Estimates for Respective Fatty Acids
Few reports have addressed genetic parameter estimates of fatty acids of fatty tissues in swine. Sellier (1998) reported mean heritability estimates of 0.51 (0.42 to 0.57) for stearic acids (C18:0) and 0.57 (0.47 to 0.70) for linoleic acid (C18:2) of subcutaneous fat. Moreover, Fernandez et al. (2003) reported heritability estimates of fatty acids of intramuscular fat analyzed using near-infrared spectroscopy. They estimated 0.41 for stearic acid (C18:0) as the greatest heritability and 0.31, 0.31, and 0.29, respectively, for C16:0, C18:1, and C18:2. Cameron et al. (2000) pointed out that the influence of feed content is stronger than the genetic effect on the fatty acid composition of intramuscular fat. In the present experiment, the feed mixing ratio was specially ordered, and the feed composition given to each generation appears to be constant. Because raw materials of formula feed are produced each year, the feed composition is inferred to differ among generations. However, when genetic parameters were estimated, the generation effect was corrected because generation was considered as a fixed effect. The high heritability for C18:0 of intramuscular fat and other main fatty acids of subcutaneous fat estimated in this study suggest the possibility of genetic improvement of fatty acid compositions of fatty tissues. A high value was estimated for melting-point heritability, but melting-point heritability estimates have not been reported previously.

Differences of Fatty Acids Among Fatty Tissue
Cameron and Enser (1991) reported that phenotypic correlations of major fatty acids between intramuscular fat and the inner backfat layer were positive and variable in magnitude (0.19 to 0.54), to the same degree as in the current study (0.25 to 0.42). Especially, genetic correlations of C18:2 were considerably low between intramuscular fat and other fatty tissues (inner-layer and outer-layer subcutaneous fat, intermuscular fat). Intramuscular fat contains more phospholipids; furthermore, the percentage of C18:2 was lower than that of subcutaneous fatty tissue. In the current study, the percentage of C18:2 of intramuscular fat was half that of inner and outer layer subcutaneous fat and intermuscular fat (Table 1). That fact suggests that genetic control of fatty acid accumulation is different for subcutaneous fat and intramuscular fat.

Genetic Correlation Between Fatty Acids and Meat Production Traits
Positive phenotypic correlation of BF with SFA and negative phenotypic correlation of BF with PUFA, and positive phenotypic correlations of BF with C18:1 were reported as 0.09 by Cameron et al. (1990). They were reported as 0.09 at last lib and 0.22 at average by Piedrafita et al. (2001). Moreover, Piedrafita et al. (2001) reported positive phenotypic correlation of LMA with C18:2 and negative phenotypic correlation with C18:1. Similar tendencies of genetic and phenotypic correlation among ADG, LMA, and BF and SFA (C16:0, C18:0) and PUFA (C18:2) were confirmed in the current study. However, genetic and phenotypic correlations among BF, LMA, and C18:1 of outer-layer and inner-layer subcutaneous fat were different in sign from those of previous reports. A previous study (Suzuki et al., 2003) examined meat of Berkshire, Duroc, and crossbred pigs sired by BF and C18:1 of inner and outer subcutaneous fat. As was concluded therein, the reason for that different correlation might be the difference in the genetic breed background between reported examinations. Furthermore, the genetic correlation between IMF content and each fatty acid of inner subcutaneous fat tissue was very low in this study. Fernandez et al. (2003) also estimated that the genetic correlations between IMF content and the main fatty acids (C16:0, C18:0, C18:1, and C18:2) were nearly zero (genetic correlation range: –0.06 to 0.09).

The composition ratio of fatty acids influences the melting point. Wood et al. (1978) pointed out that the concentration of C18:0 was the primary determinant of the melting point of subcutaneous fat, particularly in pigs with concentrations of C18:2 between 100 to 150 mg/g. Furthermore, Cameron et al. (1990) reported that, with concentrations of C18:2 above 150 mg/g, the fat firmness and melting point were determined primarily by C16:0 and C18:2 concentrations, rather than by the concentration of C18:0. Respective concentrations of C18:2 in outer and inner subcutaneous fat were 10.86 and 9.89% in the current study. Consequently, the respective genetic correlations of C18:2 with melting points of inner and outer subcutaneous fat tissue were –0.20 and –0.07. Moreover, the influence of C18:0 was positive and high and C18:1 was negative and high in both subcutaneous fats in the present result. These results suggest that the degree of C18:2 concentration affects the correlation of other fatty acids with the melting point. Lea and Swoboda (1970) suggested that the monounsaturated:saturated fatty acid ratio (C16:1 + C18:1: C16:0 + C18:0) might be a measure of fat firmness and melting point. Genetic and phenotypic correlations between the melting point and the monounsaturated:saturated fatty acid ratio were estimated, respectively, as –0.71 and –0.47 in outer subcutaneous fat, and –0.93 and –0.54 in inner subcutaneous fat (not listed in table). The values were same as the correlation of melting point with C18:1.

Prediction of changes of fatty acids as a correlated response to selection for production traits is more important than execution of direct selection for fatty acid compositions of respective adipose tissues. Two reasons for this are: 1) fatty acid composition is not a single trait—it remains unclear which and how many fatty acids or derived parameters should be included as criteria in a breeding program; and 2) measuring fatty acid compositions of numerous animals for breeding value estimation is not possible at a reasonable cost (De Smet et al., 2004). However, a single gene is responsible for the synthesis of all MUFA (i.e., stearoyl-CoA desaturase). A selection strategy that makes this gene a target might be effective. Nevertheless, it is important to measure the fatty acid composition as a correlated response to selection. For instance, Estany et al. (2002) reported the correlated response in carcass, meat, and fat quality traits to selection for litter size. That study concluded that selection might ensex compositional changes in intramuscular fat toward a lower content of PUFA. In addition, Cameron et al. (2000) reported that selection for high lean growth reduces IMF and saturated and monounsaturated fatty acids and increases PUFA in total fats. Generally, a greater carcass lean:fat ratio is genetically associated with lower lipid or low stearic acid content and softer fat as well as with greater moisture or linoleic acid content of fat depots (Sellier, 1998).

Genetic Correlation Between Fatty Acids and Meat Quality Traits
Apparently, the melting point of fat raises according to the saturation level of the increasing fatty acid composition; the whiteness of fat consequently increases the meat lightness. Although opposite genetic correlations between PCS or L* and saturated and polyunsaturated fatty acids were predicted, genetic correlations of C16:1 or C18:1 and PCS or L* showed similar negativity. When monosaturated fatty acids increase, the melting points fall and the fat does not bloom at cooler temperatures to the same extent as SFA. Biological reasons explaining the genetic correlation of cooking loss with fatty acids is unclear. Further research should examine genetic correlations between fatty acid composition and this meat quality trait.

	IMPLICATIONS

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION IMPLICATIONS LITERATURE CITED

 
Results obtained in this study suggest that the fatty acid composition of adipose tissue is correlated genetically with meat production and meat quality traits. The change in the fatty acid composition of the adipose tissue is a correlated response to selection for the production traits and meat quality traits that influence the eating quality of meat. Therefore, when selection for meat production and meat quality traits is executed, we must devote due attention to the correlated response of fatty acid composition of adipose tissues.

¹ Corresponding author: k1suzuki{at}bios.tohoku.ac.jp

Received for publication November 12, 2005. Accepted for publication March 14, 2006.

	LITERATURE CITED

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION IMPLICATIONS LITERATURE CITED

 


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