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Low birth weight is associated with enlarged muscle fiber area and impaired meat tenderness of the longissimus muscle in pigs^1,2

F. Gondret^*,3, L. Lefaucheur^*, H. Juin, I. Louveau^* and B. Lebret^*

^* Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherches-Systèmes d’Elevage, Nutrition Animale et Humaine, F-35590 Saint-Gilles, France; and and Laboratoire d’Analyses Sensorielles, Domaine du Magneraud, BP52, F-17700 Surgères, France

	Abstract

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The objective of this study was to determine the relationships between birth-weight-associated modifications in histological or chemical muscle characteristics and meat quality traits in pigs. At 68 d of age, Pietrain x (Large White x Landrace) female littermates were allocated into 2 groups on the basis of low birth weight (LW = 1.05 ± 0.04 kg; n = 15) or high birth weight (HW = 1.89 ± 0.02 kg; n = 15). Pigs were reared in individual pens with free access to a standard diet up to slaughter at approximately 112 kg of BW. During the growing-finishing period, LW and HW pigs had a similar daily feed consumption, whereas G:F was lower (P = 0.009) for LW pigs than for HW littermates. At final BW, LW pigs were 12 d older (P < 0.001) than HW littermates. Estimated lean meat content, relative proportions of loin and ham in the carcass, and weights of LM and semitendinosus muscle (SM) were decreased (P < 0.05) in LW pigs compared with HW pigs. Conversely, the LW pigs exhibited a fatter carcass, greater activity levels of fatty acid synthase and malic enzyme in backfat (n = 15 per group), and enlarged subcutaneous adipocytes (n = 8 per group) compared with the HW pigs. Similarly, lipid content was increased by 25% (P = 0.009), and mean adipocyte diameter was 12% greater (P = 0.008) in the SM from LW pigs compared with that from HW pigs, whereas lipid content did not vary in the LM of either group. Mean myofiber cross-sectional areas were 14% greater in the LM (P = 0.045) and the SM (P = 0.062) of LW pigs than of HW pigs. Conversely, the total number of myofibers was less (P = 0.003) in the SM of LW vs. HW pigs. There were no differences between groups for glycolytic potential at slaughter and rate and extent of postmortem pH decline in both muscles, as well as for LM drip losses. A trained sensory test panel judged the roast loin meat to be less tender (P = 0.002) in LW pigs relative to HW pigs. Scores for juiciness, flavor, flouriness, and fibrousness of meat did not differ between groups. Overall, negative but somewhat low correlation coefficients were found between LM tenderness score and ultimate pH (r = –0.36; P = 0.06) and between LM tenderness and mean cross-sectional area of myofibers (r = –0.34; P = 0.07). This study demonstrates a lower tenderness of meat from pigs that had a LW, partly as a result of their enlarged myofibers at market weight.

Key Words: birth weight • collagen • lipid • meat quality • muscle fiber • pig

	INTRODUCTION

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION IMPLICATIONS LITERATURE CITED

 
Pig birth weight and within-litter variation are important risk factors for preweaning mortality (Roehe and Kalm, 2000). Small piglets at birth also require a greater number of days than larger littermates to reach market weight (Wolter et al., 2002; Le Cozler et al., 2004). Nonetheless, the possibility that birth weight irreversibly affects postnatal fat and/or muscle development, and ultimately meat quality, remains rather controversial (Bee, 2004; Poore and Fowden, 2004; Gondret et al., 2005b) because of interfering factors such as competition between piglets and subsequent differences in feeding levels (Powell and Aberle, 1980). Low-birth-weight pigs exhibit a lower total number of muscle fibers than heavier littermates, a characteristic definitively fixed before birth (Wigmore and Stickland, 1983), but have larger myofibers at market BW (Kühn et al., 2002; Gondret et al., 2005b). However, some reports did not find consistent variation in total fiber number in relation to birth weight (Dwyer et al., 1993). Whether histological modifications influence meat quality traits in low-birth-weight pigs remains unknown. Lengerken et al. (1997) indicated that muscles with a low fiber number but large fibers are prone to rapid postmortem pH decline and high drip losses, two factors known to alter meat tenderness. Maltin et al. (1997), however, did not show any relationship between myofiber cross-sectional area and meat tenderness in different pig populations. Finally, other muscle characteristics such as lipid content, amount and heat-solubility of collagen, or muscle fiber typology may differ according to birth weight and influence the perception of meat quality (Lebret et al., 1999).

The objectives of this study were to determine the influences of birth BW on adipose tissue and muscle development and the consequences on eating quality when pigs were reared and fed individually during the growing-finishing period.

	MATERIALS AND METHODS

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION IMPLICATIONS LITERATURE CITED

 
Experimental Design
The experiment was conducted at the experimental unit of INRA (UMR SENAH, F-35590 Saint-Gilles, France). Thirteen litters from cross-bred (Large White x Landrace) sows and pure Pietrain boars, all free of the halothane-sensitive allele at the HAL/RYR1 locus, were used. A total of 6 successive replicates were needed to obtain the required number of animals. The mean litter size was 14.8 ± 0.3 piglets born alive. Birth weight of piglets born alive ranged from 0.60 to 2.20 kg (mean ± SEM, 1.46 ± 0.03 kg). None of the experimental piglets was cross-fostered. The piglets were weaned at 27.6 ± 0.2 d of age and penned by litter in the nursery. They had free access to a starter diet (20% CP, 6.6% fat, and 2.40 Mcal of NE/kg; as-fed basis) from 15 d until approximately 42 d and to a piglet diet (19.1% CP, 2.7% fat, and 2.30 Mcal of NE/kg; as-fed basis) until the age of approximately 77 d. At 68.2 ± 0.3 d of age (end of the postweaning period), a total of 30 females were assigned within litter (1 or 2 pairs of piglets per litter) to 1 of the 2 following groups on the basis of low birth weight (LW = 0.75 to 1.25 kg at birth; n = 15) or high birth weight (HW = 1.75 to 2.05 kg at birth; n = 15). Runts, defined as having a birth weight 2.5 SD below the mean weight of their respective littermates, were excluded from this study. Growing-finishing animals were reared in individual pens in the same room. They had free access to a growing diet (17.6% CP, 3.9% fat, and 2.32 Mcal of NE/kg; as-fed basis) until slaughter. They were weighed at birth, weaning, end of nursing, and then weekly up to slaughter at 111.8 ± 0.8 kg. Feed distribution and removal were recorded weekly during the growing-finishing period for the calculation of G:F. Pigs were slaughtered after an overnight fast by electrical stunning and exsanguination in compliance with the French national regulations applied in slaughterhouses.

Insulin Concentration
Blood was collected on heparin immediately after slaughter. Plasma was prepared by low-speed centrifugation (2,500 x g for 10 min) and stored at –20°C. Plasma insulin concentrations were measured by RIA as previously described (Prunier et al., 1993). All samples were analyzed in duplicate within a single assay.

Carcass Composition
Just after slaughter, the hot carcass and perirenal fat were weighed. Backfat depth (mean of the measurements between third and fourth lumbar vertebra and third and fourth last rib levels) and muscle depth (between the third and fourth last rib level) were measured using a Fat-O-Meter (SFK, Herlev, Denmark) to estimate lean meat content (Daumas and Dhorne, 1997). At 24 h postmortem, weights of dissectible backfat, ham, loin, shoulder, and belly wholesale cuts from the left side of the carcass were recorded and expressed as relative percentage of cold left-side weight. The entire LM was dissected from the loin piece and weighed.

Tissue Sampling and Meat Quality Indicators
Immediately after slaughter, an adipose tissue sample containing the upper and middle layers was removed from backfat (first lumbar vertebra). Pooled slices from the two layers were frozen in liquid N₂ and stored at –70°C until analyses of lipogenic enzymes. A sample also was restrained on flat stick, frozen in liquid N₂, and used for histological analysis.

Just after animal slaughtering (approximately 20 min postmortem), the LM at the last rib level and the whole semitendinosus muscle (SM) containing the outer and inner parts were excised from the right side of the carcass. Samples from LM were immediately prepared on flat sticks to keep initial length before histological examinations. Determination of the glycolytic potential also was performed on these samples. The whole SM was first weighed and transversally sectioned in its mid part. Samples devoted to measuring histological characteristics and glycolytic potential were taken immediately from the distal portion in the central zone of the transverse section, restrained on flat sticks, and frozen in liquid N₂. The proximal portion of the SM was placed always in the same position on a flat stick and stored at 4°C for 24 h to let the muscle reach rigor mortis and then relax. The muscle was then frozen at –20°C before measuring its transverse section. This procedure was necessary to get an accurate estimation of the muscle cross-sectional area in a steady state (not contracting muscle) and to avoid cold shortening during freezing at –20°C. Samples of each muscle were also taken 30 min after slaughter and immediately frozen in liquid N₂ for further determination of pH (pH₁) after tissue thawing and homogenization in iodoacetate using a combined glass electrode (Ingold, Mettler Toledo, Switzerland) and a portable pH meter (Knick, Berlin, Germany).

At 1 d postmortem, backfat layers were minced, freeze-dried, pulverized, and stored at –20°C under vacuum for lipid content determination. One slice of SM (midbelly) from the left carcass side and one slice of LM from the right carcass side (consecutively to the last sampling) also were taken. Immediately after sampling, color was measured using a Minolta Chroma Meter CR-300 (Osaka, Japan) set to the Commission Inter-nationale de l’Eclairage (CIE) color scale of lightness (L*), redness (a*), and yellowness (b*). Measurements were determined in triplicate at one point of the slice. The ultimate pH (pH₂₄) was measured in situ on the same samples using the same apparatus just described. Muscle slices were then minced, freeze-dried, pulverized, vacuum-packed, and stored at –20°C until chemical determinations. Three other slices (approximately 100 g) were removed from the LM consecutively to the last sampling (third, fourth, and fifth last ribs) for determination of drip loss after 2 and 4 d postmortem using the plastic bag method (Honikel, 1998). Finally, the loin piece (0.5 to 0.7 kg) was taken from the lumbar region of the right carcass side, trimmed from external fat, and kept for 3 subsequent days at 4°C. Samples were then deboned, keeping muscles and adipose tissue next to the LM in place. Color (L*, a*, b*) was measured immediately on the cut surface of the resulting roasts. Samples were then vacuum-packed and stored at –20°C until sensory tests.

Lipogenesis
Samples of backfat (approximately 0.6 g) were homogenized in 2.5 mL of ice-cold 0.25 M sucrose solution containing 1 mM dithiothreitol, 1 mM EDTA, and protease inhibitors (Bazin and Ferré, 2001). The mixture was centrifuged at 100,000 x g at 4°C for 1 h, and the cytosolic supernatant fraction was collected and stored at –75°C. Activities of cytosolic enzymes controlling a key step of fatty acid synthesis [fatty acid synthase (FAS); EC 2.3.1.85] or providing reduced NAD phosphate for lipogenesis [malic enzyme (MAL); EC 1.1.1.40] were assessed spectrophotometrically (Bazin and Ferré, 2001). In all assays, enzymes were maximally activated by the substrate provided in excess and cofactors, so that the activity represented the maximum potential of the enzymes under optimal conditions. Reactions were linear with respect to time over the period of the assay (10 min). One unit of activity was defined as the amount of enzyme that catalyzed the oxidation of 1 nmol NAD phosphate (FAS) or produced 1 nmol nucleotide (MAL) per minute and per gram of fresh tissue.

Expression levels of genes involved in lipogenesis were determined by real-time quantitative PCR using ABI PRISM 7000 SDS thermal cycler apparatus (Applied Biosystems, Foster City, CA). Total RNA was first extracted from adipose tissue samples according to the guanidiniumthiocyanate method (Chomczynski and Sacchi, 1987) with minor modifications (Louveau et al., 1991). The first strand was synthesized from total DNase-treated RNA using random hexamers and murine Moloney leukemia virus reverse transcriptase according to the manufacturer’s instructions (Applied Biosystems). Primers were designed from porcine sequences using Primer Express software (Applied Biosystems). The following primers were retained for FAS (forward primer 5'-AGCCTAACTCCTCGCTGCAAT-3', reverse primer 5'-TCCTTGGAACCGTCTGTGTTC-3'), MAL (forward primer 5'-TGGTGACTGATGGAGAACGTATTC-3', reverse primer 5'-CAGGATGACAGGCAGACATTCTT-3'), and the transcription factor sterol regulatory-element binding protein [forward primer 5'-CGGACGGCTCACAATGC-3', reverse primer 5'-GCAAGACGGCGGATTTATTC-3', (SREBP-1)]. The quantification of a target gene by real-time PCR normalized to an endogenous reference (18S) in pigs has been previously described (Louveau and Gondret, 2004). Briefly, PCR reactions were performed starting with 50 ng of first-strand cDNA and 500 nM of both sense and anti-sense primers in a final volume of 25 µL using SYBR Green I PCR core reagents (Applied Biosystems). Forty cycles of amplifications were performed using an annealing temperature of 59°C for each gene. Endogenous 18S ribosomal RNA amplifications were performed according to the manufacturer’s instructions (Human 18S rRNA predeveloped TaqMan kit, Applied Biosystems). Absence of contamination from either genomic DNA amplification or primer-dimer formation was ensured using controls without reverse transcriptase or with no DNA template or reverse transcriptase. A melting curve analysis also was performed, which resulted in expected single-product specific melting temperature. Cycle threshold values are means of triplicate measurements for each gene.

Histological Analysis
Total cross-sectional area of SM was measured using a programmable planimeter (Kontron; AMO 3, France) to estimate the total number of myofibers. This measurement was not relevant in the LM because myofibers are not parallel to the longitudinal axis of the muscle. Cross-sectional area (CSA) and number of myofibers were determined from transverse 14-µm-thick cross-sections that were cut in a cryostat (2800 Frigocut; Reichert-Jung, Francheville, France) and treated with azorubin to stain myofibers red. Mean CSA was determined in 3 randomly selected fields after interfiber network extraction using a macro program developed on an image analysis system (Optimas 6.5; Media Cybernetics, Silver Spring, MD). In SM, myofibers were counted over 5 randomly selected fields of known size (1.01 mm²; 200 to 300 fibers) using a projection microscope (Visopan Reichert, Vienna, Austria). The total fiber number of SM was estimated by extrapolation from the number of fibers counted over the selected fields and from the muscle cross-sectional area.

In backfat and in SM, adipocyte diameters were measured on 12-µm-thick serial cross-sections (5 sections per sample, 50-µm interval each) in a randomly chosen sample subset (n = 8 per group). Because of the lack of differences in lipid content between treatment groups, this measurement was not performed in the LM. As previously described (Gondret and Lebret, 2002), cross-sections were fixed for 10 min in 0.1 M phosphate buffer (pH 7.4) containing 2.5% (vol/vol) glutaraldehyde (25% Aqueous solution, Sigma, St. Louis, MO). They were then rinsed in distilled water and stained for 4 min in isopropanol containing 0.5% oil red O, rinsed in distilled water, and counter-stained in an aqueous solution of crystal violet. Visible adipocytes were reproduced on transparent plastic sheets using the projection microscope described earlier and digitized with a CCD camera. A macro program was developed on Optimas to measure individual adipocyte areas. Mean diameter (µm) was then calculated from about 200 adipocytes per section in each sample.

Chemical Composition
Dry matter was determined from the weight of minced tissues before and after freeze-drying. Freeze-dried tissues (approximately 250 mg for muscle and 100 mg for backfat) were homogenized for estimation of fat content, using the total lipid extraction procedure outlined by Folch et al. (1957). For the determination of total collagen content, freeze-dried powdered muscle samples (approximately 150 mg) were hydrolyzed in 6 N HCl for 18 h at 110°C. After removing HCl, the amount of hydroxyproline was determined by spectrophotometric methods (Bergman and Loxley, 1963), and a factor of 7.14 was used to convert hydroxyproline to collagen. Heat-labile collagen was estimated using the procedure of Hill (1966). Briefly, a powered muscle sample (approximately 300 mg) was homogenized in a solution containing 147 mM NaCl, 4 mM KCl, and 2.2 mM CaCl₂. The resulting homogenate was heated at 77°C for 1 h and then centrifuged for 30 min at 1,000 x g. The amount of hydroxyproline was determined in the supernatant fraction following the methods described above. Heat-stable collagen was obtained by the difference between total and heat-labile collagen. Results are the means of triplicates. All traits were expressed as milligrams per gram of fresh tissue. Glycolytic potential was determined according to Monin and Sellier (1985). After homogenization of muscle (approximately 1 g) into 10 mL of perchloric acid (0.55 M), metabolites were determined by enzymatic methods adapted on an automatic spectrophotometric analyzer (Cobas Mira Roche, Basel, Switzerland) using commercially available kits (glucose HK, ABX Diagnostics kit, Montpellier, France; lactate PAP, Biomerieux, Marcy l’Etoile, France). Glycolytic potential was expressed in micromoles of lactate equivalent per gram of fresh tissue.

Sensory Test Analyses
The vacuum-packed loins were transported in a cold environment (–20°C) to the sensory analyses laboratory (INRA Le Magneraud, F-17700 Surgères, France). One or two roasts from each birth group were thawed at 4°C during 48 h before testing. Roasts (600 g) were then cooked in an oven by dry heat for 10 min at 250°C and then by humid heat at 100°C to a core temperature of 80°C (±2°C). They were cut into 1-cm-thick slices before three rectangular samples were taken in the middle of each slice. A descriptive test was carried out by a selected and trained sensory panel consisting of 12 members. Thirteen sessions were organized to serve 1 or 2 roast samples from each experimental birth group. Three preliminary sessions on nonexperimental pork were performed. Tenderness, juiciness, perception of muscle fibers during mastication (fibrousness), flour sensation after mastication (flouriness), global flavor, and pork specific flavor were scored on a continuous scale from 0 (absent) to 10 (high).

Statistics
Data were analyzed by variance analysis using the Mixed procedure of SAS (SAS Inst., Inc., Cary, NC) with birth weight group (2 levels) and replicate (6 levels) as main effects. For sensory traits, the model included the main effects of birth weight group, panel member, session, and their interactions. Overall Pearson correlation coefficients were calculated between LM composition at slaughter, pH values or drip losses, and meat quality traits. Finally, stepwise regression analysis was performed with meat tenderness as the dependent variable and pre- and postmortem muscle characteristics as independent variables. Only variables meeting the 0.10 significance level were retained for entry into the stepwise regression model. Data are presented as arithmetic means by birth group.

	RESULTS

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Pig Performance and Fat Deposition
Mean BW in LW group was 56% of that in HW group at the day of birth. Compared with larger littermates, the LW pigs grew slower during suckling, nursing, and growing-finishing periods (Table 1); however, individual birth weight did not correlate (P = 0.11) with ADG during the growing-finishing period (i.e., from 10 wk until slaughter; data not shown). Consequently, LW pigs needed 12 d more than HW pigs to reach the same final BW (Table 1). There was no significant difference between groups for the daily feed consumption during the growing-finishing period. In contrast, the G:F was lower (P < 0.01) in LW than in HW pigs. Fasting insulin concentration in plasma did not differ between the 2 groups. Backfat thickness at slaughter was increased by 21% (P < 0.01) in the LW pigs compared with the HW pigs, whereas estimated lean meat content was decreased by 2 percentage points (P < 0.01) in LW pigs. Data obtained by physical separation of the chilled carcass substantiated these observations (Table 1); LW pigs had a 29% greater backfat yield, a greater proportion of belly, but slightly lower proportions of loin and ham (–4% on average; P < 0.04) compared with HW pigs.

Meat Quality Traits
Glycolytic potential and the rate (pH₁) and extent (pH₂₄) of postmortem pH decline in both muscles did not differ between groups (Table 4). Drip losses in LM were similar in both groups. Meat L* value assessed at 1 d postmortem was slightly greater (P < 0.05) for the LW than for the HW pigs, whereas meat a* and b* values did not differ between groups. After aging for 4 d, LM color did not differ between groups. Roast loin from LW pigs showed a lower score for tenderness compared with that from HW pigs (P < 0.01), whereas scores for other sensory quality traits under study did not differ between the two groups.

	DISCUSSION

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The data presented herein substantiate previous findings showing that light pigs at birth exhibit lower postnatal growth rates compared with heavy littermates (Powell and Aberle, 1980; Gondret et al., 2005b). Fetal undernutrition is considered the main reason for LW (Roeder and Chow, 1972) and is generally associated with low milk consumption during sucking because of competition among littermates (Campbell and Dunkin, 1982). In the current study, there was no difference in feed intake during the last growing period from 10 wk (approximately 25 kg) onward, suggesting that fetal undernutrition did not affect the appetite of LW pigs. In contrast, G:F was clearly lower for LW than for HW pigs, which might be explained by an inadequate digestion and/or nutrient use as a consequence of early undernutrition (Roeder and Chow, 1972). After weaning, inconsistent effects of birth weight and/or weaning BW on daily feed consumption and feed efficiency have been previously reported in pigs (Powell and Aberle, 1980; Wolter and Ellis, 2001; Wolter et al., 2002). The timing and degree of early undernutrition and the composition of postnatal diets might be important for subsequent feeding behavior (Breier et al., 2001).

The low weight at birth resulted unambiguously in greater carcass fatness at market weight and increased lipid contents in backfat and SM. As reported in fetal-growth-restricted rats as adults (Jones and Friedman, 1982), enlarged adipocyte diameters were observed in adipose tissues and skeletal muscle from LW pigs compared with HW pigs. Powell and Aberle (1981), however, mentioned a greater proportion of small adipocytes in runt piglets compared with larger littermates as indicative of prolonged adipocyte hyperplasia. We suggest that these variations in fat content and cellularity in relation to birth BW were instead related to differences in lipogenic enzyme activities than to differences in duration of fat accumulation and/or in physiological maturity between pigs. Indeed, with increased lipogenic enzyme activities at least in backfat, LW pigs likely exhibited a greater potential for fatty acid synthesis than HW pigs. Fatty acid synthase is subjected to tight hormonal and nutritional control primarily at the transcriptional level with SREBP-1 as the key upregulating factor of lipogenic gene transcription (Brown and Goldstein, 1997); however, glucose is increasingly recognized as an important regulator of FAS mRNA stability (Semenkovich, 1997). In the current study, the increase in activities in LW compared with HW pigs, despite no major changes in mRNA levels, may involve differences in glucose metabolism between the two groups. Indeed, Poore and Fowden (2002) have reported that low-birth-weight female pigs presented a poor glucose tolerance compared with high-birth-weight littermates at slaughter, despite similar insulin plasma concentrations in both groups (current results; Poore and Fowden, 2004). Altogether, our findings agree with the results of previous studies showing a greater body fatness in low-birth-weight piglets offered free access to diets during growth (Kühn et al., 2002; Poore and Fowden, 2004) or reared on an adjusted daily feed allowance (Bee, 2004). Our results also support the growing number of epidemiological studies suggesting that poor nutrition during fetal life and LW can affect predispositions to adult health outcomes, including body mass index and obesity (Breier et al., 2001; Rogers, 2005). Nonetheless, the full expression of lipogenic potential and fat growth in small piglets may be prevented in animals that are not fed ad libitum during postnatal period because of restricted feeding and/or feed competition among animals (Powell and Aberle, 1980; Wolter et al., 2002; Gondret et al., 2005b).

The second main finding of this study was that enlarged cross-sectional area of myofibers in pigs having a low rather than a high weight at birth was paralleled by a lower sensory score for meat tenderness. Differences in muscle histological characteristics between LW and HW pigs were somewhat expected. Indeed, other studies have previously shown that mean myofiber diameters were either larger or tended to be larger in the SM and/or LM muscle of pigs that were small at birth compared with heavier littermates, at a constant market BW (Handel and Stickland, 1987; Bee, 2004; Gondret et al., 2005b) or at the same age (Kühn et al., 2002). Because of intrafascicularly terminating fibers, the histological method used to assess the total fiber number likely underestimated the actual number of fibers in the muscle; however, pigs of both groups were compared at the same BW and thereby likely displayed the same muscle lengths. Therefore, underestimation of total fiber number would have been similar in the 2 groups. Collectively, our results confirm that LW pigs other than runts exhibited fewer fibers than heavier littermates, at least in the SM. This finding is consistent with several studies showing a deceased number of muscle fibers in small piglets relative to larger littermates as a response to selection for birth weight (Handel and Stickland, 1988; Kühn et al., 2002; Gondret et al., 2005b), weight at 5 wk (Dwyer and Stickland, 1991), or carcass weight at the same age (Nissen et al., 2004). Indeed, it is largely admitted that different levels of nutrition received in utero are a major cause of intralitter variation in total fiber number (Dwyer et al., 1994), which seems to be irreversible because total fiber number is set before birth in pigs (Wigmore and Stickland, 1983). Our results also support the assumption that the postnatal hypertrophy of the individual fibers is greater when there is a lower number of fibers in the muscle (Rehfeldt et al., 2000).

The negative relationship evidenced here between myofiber diameter and taste-panel tenderness score agrees with previous results obtained between fiber size and sensory or instrumentally measured tenderness in pork (Carpenter et al., 1963; Ryu and Kim, 2005); however, other reports have not mentioned any significant relationship between these traits (Henckel et al., 1997; Maltin et al., 1997). Enlarged myofiber CSA combined with a lower total number of fibers in pig muscle have been previously suggested to decrease pH₁ and to increase drip loss during meat postmortem aging (Lengerken et al., 1997), but Lengerken et al. included halothane-positive pigs, which exhibit an allele directly assigned to accelerate the rate of postmortem pH fall and drip loss (Monin et al., 1999). Therefore, the increased myofiber CSA observed in halothane-positive pigs (Essen-Gustavsson et al., 1992) may not be directly related to their frequently inferior meat quality. Considering halothane-negative pigs, we did not observe any differences in muscle glycolytic potential at slaughter, pH values, and/or drip losses between LW and HW pigs, despite variations between birth groups in myofiber number and size. Similarly, Nissen et al. (2004) did not observe any difference in meat drip loss among littermates differing in carcass weight at the same age, despite a lower fiber number in the lightest pigs. Contrary to the findings of others (Huff-Lonergan et al., 2002; Hamilton et al., 2003), we did not detect any relationships between glycolytic potential at slaughter and tenderness of pork loin. Nonetheless, we observed a negative association between tenderness and pH₂₄, which agrees with the findings of Fernandez and Tornberg (1992) for the same range of pH values. For the same range of pH values, negative relationships between tenderness and ultimate pH also were noted by Göransson et al. (1992), whereas Hovenier et al. (1993) showed no relation between these two traits. Aside from variations in genotype and/or storage time (van Laack et al., 2001), the controversies among studies could also arise from quadratic rather than from linear relationships between muscle components and sensory attributes, as suggested by Fernandez and Tornberg (1992) for pork and Purchas (1990) for beef, with likely threshold values for some of these traits.

We did not anticipate finding a greater amount of heat-stable collagen in the LM of LW pigs, leading to a tendency for a slightly higher content in total collagen compared with HW littermates at market BW. Several investigations have shown that intramuscular collagen content relative to myofibrillar protein content decreases during normal growth in pigs (Gondret et al., 2005a). In agreement with our results, collagen content per gram of muscle has been reported to be greater in lambs exhibiting a slow compared with a high growth rate, consecutively to different feeding levels (Sylvestre et al., 2002). Differences observed in total collagen content at slaughter for LW pigs relative to HW littermates also may have a fetal origin that continued postnatally. In support of this suggestion, Karunaratne et al. (2005) recently observed increased levels of type I collagen within skeletal muscle of the lightest pig littermate compared with its largest littermate during late fetal life; however, we have no explanation for such a birth weight effect in the LM muscle without any significant variation in SM muscle. Finally, muscle collagen heat-solubility decreases with growth, providing large differences in age ranges (Lebret et al., 1998). Thus, the lack of any birth weight effect on collagen heat-solubility may be related to the small difference in age between LW and HW pigs at market BW. Interestingly, the amounts of collagen fractions in LM did not correlate with taste panel scores. Similarly, other researchers did not find any significant correlation coefficients in pork meat between total amount of collagen and tenderness (Carpenter et al., 1963; Hovenier et al., 1993; Candek-Potokar et al., 1998) or between collagen heat-solubility and variation in texture (DeVol et al., 1988; Avery et al., 1996).

Altogether, chemical and histological characteristics of LM accounted for only one-third of the variance in loin tenderness in the present experiment. Categorizing littermates in lightest, middle, and heaviest weight at final BW as indicative of differences in birth BW and postnatal growth rates, Nissen et al. (2004) calculated the lowest muscle deposition rate in the lightest pigs. In addition, when comparing pigs fed restrictively from weaning to slaughter, ad libitum during the same period, or undergoing a compensatory growth, Therkildsen et al. (2004) observed that improved growth rate was related to greater values of both muscle protein synthesis and protein degradation in vitro and thereby to a greater muscle protein turnover. Therefore, it seems reasonable to speculate that LW pigs displayed a lower protein turnover relative to HW pigs, which might have resulted in a decrease in the amount and/or activity of proteolytic enzymes such as calpain and cathepsins (Kristensen et al., 2002) in LW pigs that negatively affected final meat tenderness.

	IMPLICATIONS

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION IMPLICATIONS LITERATURE CITED

 
Free access to feed during the growing-finishing period favored fat deposition in pigs that exhibited a light weight at birth, resulting in a fatter carcass at market weight and increased lipid content of the semitendinosus muscle in low-birth-weight pigs relative to their heavy littermates. Furthermore, this study reinforces previous evidence for larger myofiber mean cross-sectional areas in pigs having been small at birth compared with larger littermates at slaughter body weight. For the first time, we found that pigs with small birth weights had altered loin tenderness, which may be attributed, at least in part, to enlarged myofibers. Fiber number is fixed before birth in pigs, and fiber hypertrophy is accelerated in muscle with a low number of fibers. Therefore, manipulations of maternal nutrition during gestation and/or genetic selection on litter homogeneity may be useful strategies to improve pork quality.

	Footnotes

 
¹ The authors acknowledge F. Pontrucher, P. Ecolan, N. Bonhomme, and C. Trefeu for sample preparation and analyses; R. Delaunay, B. Duteil, C. Homo, and H. Demay for animal care; M. Alix, J. F. Rouaud, and J. Liger for animal slaughtering and carcass evaluation; and K. Méteau for expert management of sensory analyses.

² Preliminary results were presented during European meeting of COST ACTION 925 (F. Gondret, L. Lefaucheur, I. Louveau, and B. Lebret. 2005. The long-term influences of birth weight on muscle characteristics and eating meat quality in pigs individually reared and fed during fattening. Arch. Tierz. Dummerstorf. 48:68–73).

³ Corresponding author: Florence.Gondret{at}rennes.inra.fr

Received for publication May 20, 2005. Accepted for publication August 21, 2005.

	LITERATURE CITED

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION IMPLICATIONS LITERATURE CITED

 


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