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ANIMAL PRODUCTS |
Department of Animal Sciences, Auburn University, Auburn, AL 36849
Abstract
Duroc-cross pigs (n = 25) were assigned to one of three experimental finishing diets containing 0 (control), 40,000 (40), or 80,000 (80) IU of supplemental vitamin D3/kg of feed (as-fed basis)to test the effects of vitamin D3 on pork quality traits. Experimental diets were fed for 44 or 51 d before slaughter, and days on feed were blocked in the experimental design. A trend existed for pigs receiving the highest concentration of vitamin D3 supplementation to have a lower (P = 0.08) ADG (0.77 kg/d) compared with pigs fed either the 40-diet (0.88 kg/d) or control (0.92 kg/d). Diet did not (P > 0.10) affect backfat thickness measured along the midline, 10th-rib fat depth, longissimus muscle area, muscle score, or hot carcass weights. Longissimus pH, measured at 0.5, 1, 2, 3, 4, and 24 h postmortem, was higher (P < 0.05) for pigs on the 80-diet than those fed the control diet. Longissimus muscle color, measured at 24 h postmortem, from pigs fed either the 40- or 80-diet were darker (lower L* values; P < 0.05) than those fed the control diet. Objective longissimus color scores were higher (P < 0.01), and firmness/wetness scores lower (P < 0.05), for pigs on the 80-diet as compared to those on the 40-diet or control diet. The diet had no (P > 0.10) effect on Warner-Bratzler shear force values; percentage of cook loss; or trained sensory panel evaluations for tenderness, juiciness, and flavor. Feeding the 80-diet increased (P < 0.05) plasma vitamin D3 and calcium after 2, 4, and 6 wk on feed compared with the control diet. Vitamin D3 and 25-hydroxy vitamin D3 concentrations in the longissimus muscle increased (P = 0.001) with increasing vitamin D3 levels in the diet; however, muscle calcium concentrations and fiber type were not (P > 0.30) affected by diet. These results indicate that feeding supranutritional levels of vitamin D3 for at least 44 d improves pork color and increases pH, but may retard growth if fed at 80,000 IU/kg of feed.
Key Words: Calcium • Fiber Type • Pig • Pork • Quality • Vitamin D3
Introduction
Physiological factors, such as pH decline and glycolytic potential, are closely related to vital pork quality traits, such as color and water-holding capacity (Huff-Lonergan et al., 2002
). Muscle fiber types have also been correlated with similar pork quality traits (Kerth et al. 2001). Because the biggest difference in muscle fiber histology is found in the predominant metabolic enzyme activity, fiber types tend to be either oxidative or glycolytic in nature. The muscles having fibers with mostly glycolytic metabolism would be the most susceptible to differences in lactate production, and, therefore, pH decline and the resulting differences in color and water-holding ability.
It has been reported that a calcineurin pathway responds preferentially to sustained, low-amplitude elevations of calcium (Timmerman et al., 1996) and has been shown to increase the expression of genes linked to slow-twitch oxidative muscle fibers in mice (Chin et al., 1998). Increasing the population of slow-twitch muscle fibers would shift muscle metabolism to become more oxidative. By increasing oxidative metabolism, and decreasing glycolytic metabolism, the rate and extent of pH decline should be decreased, thus improving pork color and water-holding ability.
Swanek et al. (1999) and Montgomery et al. (2000; 2002) have shown that feeding very high concentrations of vitamin D3 to cattle results in increased levels of plasma and muscle calcium. It is reasonable to hypothesize, therefore, that feeding pigs high concentrations of vitamin D3 over a period of 6 wk would increase plasma and cellular calcium concentrations, as well as activate slow-twitch oxidative muscle fiber expression. Therefore, the objective of this study was to test the effects of feeding pigs diets containing 0, 40,000, or 80,000 IU of supplemental vitamin D3/kg of feed for 44 to 51 d on pork color, pH, water-holding capacity, and muscle fiber type.
Materials and Methods
Animals.
Twenty-five Duroc x Yorkshire barrows and gilts were randomly assigned to one of three experimental treatment groups and in accordance with an approved institutional animal care and use protocol. The experimental diets were of fortified corn and soybean meal and formulated to meet or exceed NRC (1998) recommendations for finishing swine. Based on our preliminary, unpublished data and the data of Enright et al. (1998), experimental concentrations of vitamin D3 were determined, and vitamin D3 was added to supply 0 (control), 40,000 (40), or 80,000 (80) IU of supplemental vitamin D3/kg of feed (as-fed basis), and fed for either 44 or 51 d before slaughter. Each diet was assigned to a pen of four or five pigs with duplicate pens of each treatment diet. Pigs were weighed, and feed disappearance was determined weekly to calculate ADG. Blood was collected by jugular vein puncture from four randomly selected pigs per pen at the onset of the experiment, and the same pigs were sampled every other week until slaughter, when blood samples were collected from all pigs during exsanguination. Blood samples were collected in heparinized tubes, and plasma was separated and stored at -80°C until analysis. Pigs were slaughtered at the Auburn University Lambert Meat Laboratory when they reached an average live weight of 102 kg using common harvest techniques, and carcasses were chilled for 24 h at 2°C. Longissimus muscle (LM) pH and temperature was measured at the last rib at 0.5, 1, 2, 3, 4, and 24 h after stunning using a portable pH meter (model IQ150 pH/mv/Temperature System, IQ Scientific Instruments, Inc., San Diego, CA) connected to a stainless probe (model PH07-ss, IQ Scientific Instruments, Inc., San Diego, CA).
Carcass Measurements and Evaluation.
After a 24-h chilling period, carcasses were ribbed between the 10th and 11th ribs. Backfat depth was measured along the midline at the first and last ribs, as well as the last lumbar vertebrae, and one-half the distance across the longissimus muscle at the 10th rib. Visual muscle score (1 = thin, 2 = average, and 3 = thick), carcass length, and LM area measurements were also recorded. Lean color (1 = pale gray to 5 = dark purplish-red), firmness (1 = very soft to 5 = very firm), and marbling (1 = devoid to practically devoid to 5 = moderately abundant or greater) scores were assigned to the LM at the 10th-rib interface by trained and experienced personnel according to NPPC (1991) guidelines. Longissimus muscle at the 10th rib was also evaluated for objective color measurements with a Hunter Miniscan XE Plus (Hunter Associates Laboratory, Inc., Reston, VA) for L*, a*, and b* values. The Miniscan utilized illuminant D65, a 10° viewing angle, and a 35-mm viewing area, and was calibrated according to manufacturer’s recommendations using a black glass plate and a white tile.
A section of the LM was removed from the 4th to 10th ribs. Starting at the posterior (10th rib), six 2.5-cm-thick chops were cut, and two chops were designated for sensory evaluation, two for shear force determination, one for water-holding capacity, and one for drip loss measurement. Samples for water-holding capacity and drip loss were analyzed on fresh, postrigor LM collected during carcass fabrication, whereas chops allocated for sensory and shear evaluation were vacuum-packaged and frozen 24 h postmortem at -20°C for later analyses.
Drip Loss and Water-Holding Capacity.
Samples for drip loss and water-holding capacity were analyzed without freezing on the day of fabrication. Chops used for drip loss were trimmed free of fat and connective tissue, weighed, placed in a plastic bag, and suspended on a hook at 4°C for 8 d. Chops were weighed after 8 d of storage, and drip loss was calculated as the percentage of weight lost from the original weight. Percentage free water was determined using the Carver press method (Grau and Hamm, 1953).
Warner-Bratzler Shear Force (WBSF), Sensory Evaluation, and Cooking Loss.
Chops were thawed in vacuum-package bags at 4°C for 24 h, removed from packages, weighed, and cooked on a clam-shell grill (model 25300 type ST09 grill, Hamilton Beach/Proctor Silex, Inc., Racine, WI) for 4.5 min to an internal temperature of 71°C according to the procedure outlined by Kerth et al. (2003). Chops for WBSF were removed from the grill, weighed, and stored at 4°C for 24 h on a pan covered with polyvinylchloride film. Three 1.3-cm-diameter cores were taken from each chop parallel with the orientation of muscle fibers, and sheared once perpendicular to the length of the core using a Warner-Bratzler shear machine (model 1955; G-R Electric Manufacturing Co., Manhattan, KS). Peak force for each core was recorded, and six cores/pig were averaged for statistical analysis (AMSA, 1995).
Sensory evaluation of LM chops was conducted according to guidelines set by AMSA (1995 using a six-person trained sensory panel made up of meat science faculty and graduate students. Chops were prepared and cooked as described for WBSF evaluation. After cooking, chops were cut into 1cm x 1cm x cooked-chop-thickness cubes, and held in metal double-stack poachers filled with sand and placed in a warming oven for a minimal period of time prior to evaluation. Each panelist was given two pieces to evaluate on an 8-point scale for initial and sustained tenderness, initial and sustained juiciness, flavor intensity, and pork flavor (1 = extremely dry, extremely tough, extremely bland, and extremely uncharacteristic to 8 = extremely tender, extremely juicy, extremely intense, and extremely characteristic). Cook loss was measured as the percentage of precooked weight lost during cooking, and averaged across the two chops from each pig.
Calcium.
Blood was collected in heparinized tubes and centrifuged for 10 min at 1,000 x g. Plasma was removed, frozen at -80°C, packaged in dry ice, and sent to Auburn University College of Veterinary Medicine Clinical Pathology laboratory for analysis using a commercially prepared kit (Roche Diagnostics Corp., Indianapolis, IN) for determination of plasma calcium using the cresophthaline complexone method. Muscle samples were frozen in liquid nitrogen, packaged in dry ice, and sent to the Alabama C.S.R. Veterinary Diagnostic Laboratory for analysis using the AOAC (1995) method.
Vitamin D3, 25-Hydroxy Vitamin D3, and 1,25-Dihydroxy Vitamin D3.
Plasma and LM samples were frozen at -80°C, and sent to the USDA, ARS National Animal Disease Center (Ames, IA) for vitamin D3, 25-hydroxy vitamin D3, and 1,25-dihydroxy vitamin D3 analyses. Vitamin D3 and its metabolites were quantified by the method described by Montgomery et al. (2000), a modification of the method used by Horst et al. (1981).
Glycolytic Potential.
Longissimus muscle samples were taken at approximately 30 min postmortem from the 10th rib (left side of carcass), frozen in liquid nitrogen, and held at -80°C until analysis. Glycolytic potential was determined using the method of Monin and Sellier (1985) as described by Lonergan et al. (2001). Duplicate 0.5-g samples were homogenized in 2.5 mL of cold perchloric acid (0.6 N) held in an ice water bath using a Tissue Tearor (model 985370; Biospec Products, Inc., Bartlesville, OK). Duplicate 200-µL samples were hydrolyzed with amyloglucosidase at 40°C for 120 min. Incubation was stopped by the addition of 1 mL of 0.6 N perchloric acid, and samples were centrifuged for 10 min at 1,000 x g. Clarified samples were used to determine total micromolar glucosyl units (free glucose, glucose-6-phosphate, and glucose from glycogen) using the glucose-hexokinase assay kit (Sigma Chemical Co., St. Louis, MO). Duplicate 1-g samples were extracted in 0.7 N perchloric acid for the determination of lactate using a lactate kit (Sigma Chemical Co.). Glycolytic potential was calculated as [2 x (glycogen + glucose + glucose-6-phosphate)] + lactate (Monin and Sellier, 1985).
Histochemical Analysis.
Longissimus muscle samples, taken from the last rib (left side of carcass) at approximately 30 min postmortem, were cut into 0.5- x 0.5- x 1.5-cm pieces and affixed to a 2- x 2-cm piece of thin cork board using tissue freezing media. The orientation of the muscle fibers was perpendicular to the flat surface of the cork. Affixed samples were frozen in 2-methyl butane submersed in liquid nitrogen, placed in plastic bags, and stored at -80°C, until analysis.
Muscle samples were transported on dry ice, placed in a Reichert Jung Frigicut 2800N (Leica Microsystems, Wetzlar, German) cryostat set at -20°C and allowed to equilibrate for at least 15 min. Slides were prepared by slicing samples perpendicular to the direction of the muscle fibers in 14-µm slices, and muscle sections then were stained for acid-stable ATPase activity according to the methods of Solomon and Dunn (1988).
Microscopic photographs were taken with a Nikon Eclipse E800 (Nikon USA, Inc., Melville, NY) microscope fitted with a 100-W mercury lamp illumination source, a polarizer, dark-field condenser, and a Nikon (model F100; Nikon USA, Inc.) camera. The microscope and camera were linked to a video monitor and a computer equipped with Spot graphics program (Diagnostic Instruments, Inc., Sterling Heights, MI). Images were saved as tiff (uncompressed) files and printed on Hewlett Packard high-quality photo paper using an HP Deskjet 648C. Muscle fibers were classified as ß-red, 
-red, or -white, and reported as a percentage of the total number of muscle fibers counted (at least 500 muscle fibers per animal).
Statistical Analysis.
The effect of vitamin D3 was determined by analysis of variance for a randomized complete block design using the GLM procedure of SAS (SAS Inst. Inc., Cary, NC) with individual pig as the experimental unit. Because the time on feed was not part of the original objective, day of slaughter served as the block to remove any variation caused by an extra 7 d on test. When differences (P < 0.05) were detected, means were separated using Fisher’s protected LSD. Plasma calcium, plasma vitamin D3 and its metabolites, and pH were analyzed as repeated measures using the block x diet interaction as the error term for the diet effect, and the residual variance as the error term for time and diet x time interaction effects.
Results
Carcass Traits and pH.
Feeding pigs supplemental vitamin D3 tended to decrease (P = 0.08) ADG compared to the control diet (Table 1). Supplemental vitamin D3 did not (P > 0.28) affect hot carcass weight or fat thickness measured at the first rib, 10th rib, last rib, last lumbar vertebrae, or LM area. Carcass muscle scores were lower (P < 0.05) for pigs fed the 80-diet compared to those fed the 40-diet or the control diet. Feeding pigs the 80-diet increased (P < 0.05) longissimus pH compared to pigs fed the control or 40-diets when averaged across all times postmortem (Figure 1).
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). Feeding the 80-diet also increased (P < 0.01) plasma vitamin D3 compared to the 40-diet. The same effect was found after 4, 6, and 7 wk of supplementation. The 25-hydroxy vitamin D (25OHD) concentration increased (P < 0.01) in plasma of pigs fed the 40-diet compared to the control diet after 4 or 6 wk of vitamin D3 supplementation, and feeding the 80-diet also increased (P < 0.01) plasma 25OHD compared to the 40-diet at both 4 and 6 wk (Figure 3). After 7 wk of supplementation, plasma 25OHD concentration was higher (P < 0.05) in pigs fed the 80-diet compared to the control diet, but pigs fed the 40-diet did not (P > 0.05) differ from those fed the control diet or the 80-diet. Plasma calcium concentration did not (P > 0.10) differ among the three diets at 0, 2, or 4 wk; however, after 6 or 7 wk of supplementation, pigs fed the 80-diet had a higher (P < 0.05) plasma calcium concentration than pigs receiving the 40 or control diets (Figure 4).
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). Percentage drip loss after 8 d of storage tended to be lower (P = 0.06) in muscle from pigs that had been fed supplemental vitamin D3. The LM from pigs fed the 80-diet was darker (lower L* values; P = 0.02) than the LM of control-fed pigs. Subjective color scores and firmness/wetness scores for pigs fed the 80-diet were higher (P < 0.05) than those fed the 40-diet or control diet.
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). The other metabolite of vitamin D3, 1,25-dihydroxy vitamin D3, was not detected in muscle or blood samples (data not shown). This is not uncommon considering its relatively low concentration in blood and muscle. No (P > 0.10) differences were found among diets for calcium concentration, total glycosyl units, or lactate in muscle samples, yet supranutritional concentrations of vitamin D3 did tend to increase (P < 0.06) the glycolytic potential of the LM. Supplementation of diets with vitamin D3, however, did not (P > 0.3) affect the percentage of red, white, or intermediate muscle fibers in the LM.
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. Vitamin D3 supplementation did not (P > 0.26) affect cook loss percentage; WBSF values; or trained sensory panel scores for tenderness, juiciness, and flavor.
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The objective of this study was to feed supplemental vitamin D3 to increase cellular calcium and activate the calcineurin pathway, which would subsequently promote red oxidative muscle fiber types and improve pork quality. Chin et al. (1998) demonstrated that changing the calcineurin activity for 6 wk caused a change in muscle fiber histology in mice. Although plasma calcium was increased in the present experiment, its effect on muscle metabolism and fiber type was difficult to determine because the elevation in plasma calcium did not occur until the sixth week of the trial. Plasma calcium concentration for pigs fed the 80-diet was elevated approximately 20%, but only for 1 wk before slaughter. This may explain why no differences were observed in muscle fiber histology among pigs fed control, 40-, or 80-diets. Feeding high concentrations of vitamin D3 for longer periods of time may be needed to alter muscle fiber histology. Chin et al. (1998) reported that inhibiting calcineurin in mice, by injecting cyclosporin, for 6 wk altered muscle fiber type (as measured by metabolic activity). It is likely, in the present study, that we did not affect the calcineurin pathway and, therefore, found no effect on muscle fiber type because of the short duration in elevated muscle calcium levels.
Researchers have shown that feeding supranutritional levels of vitamin D3 ranging from 0.5 x 106 to 7.5 x 106 IU/d to steers caused an increase in plasma calcium concentration, which peaks after 6 d of administration (Montgomery et al., 2000, 2002). In the present study, an increase in plasma calcium concentration was not found until the sixth week of treatment. The reason for the difference in response time is most likely attributable to the difference in the metabolism of vitamin D3 between the two species, as well as the level being fed.
Enright et al. (1998) fed low, moderate, and high concentrations (331, 55,031, and 176,000 IU/kg of diet, respectively) of vitamin D3 to finishing pigs for 10 d before slaughter. While plasma calcium was elevated in both the moderate and high treatment groups, vitamin D3 treatment significantly reduced ADG and ADFI. Given the results presented by Enright et al. (1998), it is not surprising that the 80-diet level tended to depress ADG in the present study.
Montgomery et al. (2002) found that feeding steers at least 0.5 x 106 IU of vitamin D3/d increased muscle pH measured at 24 h postmortem. It was suggested that the increased pH was a result of increased cellular calcium and increased oxidative muscle metabolism (Montgomery et al., 2002). A similar affect was found in the present study, in which the highest concentration of vitamin supplementation increased longissimus pH. It is a plausible assumption that if feed intake was reduced by feeding high levels of vitamin D3, muscle glycogen reserves may be reduced; however, in contrast to this assumption, the glycolytic potential tended to be higher in pigs fed the 80-diet when compared to pigs fed the control diet. In fact, Davis et al. (1990), reported that the activity of glyoxylate cycle enzymes, which are used to convert lipid to carbohydrate, were stimulated in animals treated with vitamin D. The result in these chicks would be an increase in the substrate for glycolysis and an increase in glycolytic potential, similar to the findings of the present study. Therefore, an increase in lactate would be expected in postmortem muscle, and the muscle pH should be lower, contrary to the results reported in this paper.
Huff-Lonergan et al. (2002) found that glycolytic potential is very highly, and negatively, correlated with ultimate pH. This antagonistic relationship between glycolytic potential and ultimate pH did not exist in the present study, which affirms the work of van Laack and Kauffman (1999), who did not find glycolytic potential to be the limiting factor in lactate production. According to Scopes (1974), ultimate pH is determined by substrate concentration, and other possible limiting factors, such as AMP deaminase and glycogen phosphorylase. If glycogen potential is increased by elevating muscle vitamin D levels, it seems possible that a buffering effect may be present that inhibits higher lactate concentrations from lowering pH.
A change in muscle fiber type expression and an increase in oxidative metabolism were not detected in the present study, but factors contributing to overall pork quality were improved. The results of this study are in agreement with those of Enright et al. (1998) and Wiegand et al. (2002), who observed that feeding moderate to high concentrations of vitamin D3 for 7 or 10 d preceding slaughter increased subjective color and firmness scores, while decreasing L* values. Similarly, results of the present study indicated that L* values were reduced, and subjective color and firmness scores were increased, by feeding pigs diets containing 80,000 IU/kg of feed. Thus, feeding high concentrations of vitamin D3 to pigs improves pork quality, but the mechanism(s) responsible for these improvements are not clear.
Implications
Supplementing pork finishing diets with at least 40,000 IU/kg of feed for 44 d can be used to improve pork quality by slowing the pH decline in postmortem muscle. This increase in pH is in contrast to an apparent increase in glycolytic activity of muscle from these pigs. Longer feeding times may be required to increase muscle calcium concentrations sufficiently to improve pork tenderness. Additionally, growth rate may be decreased if vitamin D3 is fed at 80,000 IU/kg of feed.
Footnotes
1 Brand names are necessary to report factually on available data; however, Auburn University does not guarantee nor warrant the standard of the product, and the use of the name implies no approval of the product to the exclusion of others that might also be suitable. Special thanks go to R. Horst (USDA-ARS, Ames, IA) and G. D’Andrea (Auburn Veterinary Diagnostic Laboratory) for their assistance in analyses of blood and muscle. 
2 Correspondence: 209 Upchurch Hall (phone: 334-844-1503; fax: 334-844-1519; e-mail: ckerth{at}acesag.auburn.edu).
Received for publication May 2, 2003. Accepted for publication September 2, 2003.
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