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ANIMAL PRODUCTS |
Kansas State University, Manhattan 66506
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Abstract |
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 Top Abstract INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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Key Words: fatty acid • lamb • lipid • meat quality • vitamin A
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INTRODUCTION |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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).
Recently, the relationship between vitamin A intake and marbling development has been investigated. Increased marbling scores and chemically extractable intramuscular fat (IMF) have been demonstrated in cattle (Oka et al., 1998; Nade et al., 2003; Kruk et al., 2004) and swine (D’Souza et al., 2003) fed either no or very low supplemental levels of vitamin A. Furthermore, marbling scores have been negatively correlated with concentrations of vitamin A (retinol) in cattle blood (Oka et al., 1998; Adachi et al., 1999) and liver (Oka et al., 1998; Chae et al., 2003). Preadipocyte differentiation has been either suppressed or completely inhibited in the presence of retinoids in cultured porcine (Brandebourg and Hu, 2005), bovine (Ohyama et al., 1998), and ovine (Torii et al., 1995) stromal-vascular cells. Several authors have theorized that vitamin A and its metabolites inhibit preadipocyte differentiation by activating retinoic acid receptors and downregulating the expression of peroxisome proliferator-activated receptor-
, a marker of preadipocyte differentiation (Xue et al., 1996; Brandebourg and Hu, 2005).
To minimize economic risks and to conduct a study of shorter duration, we used lambs as a "model species" to evaluate the effects of high and low vitamin A diets on growth performance, carcass traits, and lipid composition of market lambs by using a combination of backgrounding (BG) and finishing (FN) periods. Specifically, in this study we sought to determine the relationships between vitamin A status and the content and composition of fatty acids (FA) in serum, liver, and carcass fat depots.
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MATERIALS AND METHODS |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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Forty crossbred wethers (Rambouillet x Finn ewes mated to Suffolk x Hampshire rams) were purchased at approximately 90 d of age (BW = 29 kg) from a single source and weaned on the day of purchase. Lambs had ad libitum access to creep feed from birth to weaning, which was on the day of purchase. The lambs were vaccinated and treated for internal parasites prior to weaning.
Experimental Design and Treatments
A completely random design with a 2 x 2 factorial treatment structure was used for this research. There were 4 pens (2 per treatment), each with either 10 or 11 lambs, during the 56-d BG period. During the 56-d FN period, 8 pens (2 per treatment) each contained either 5 or 6 lambs. This was accomplished by constructing a fence through the middle of each pen on the last day of BG, thus doubling the number of pens. Consequently, pen size and the number of animals per pen were halved for the FN period. However, this method allowed the stocking rate and the amount of pen space per animal to remain the same throughout the experiment. Lambs were weighed prior to assignment of treatments, and initial pen weights were balanced by stratifying weights onto treatment. Lambs were randomly assigned to 1 of 2 BG treatments: high vitamin A or low vitamin A. After 56 d on the BG diets, a similar method of stratifying animal weight onto treatment created 4 treatment combinations for the combined feeding periods: high vitamin A during the BG and FN periods (HH); high vitamin A during the BG period, then low vitamin A during the FN period (HL); low vitamin A during the BG period and high vitamin A during the FN period (LH); or low vitamin A during the BG and FN periods (LL).
Diets
To examine the effect of level of vitamin A intake during the growing phase in lambs, a 56-d BG period was included in this study immediately preceding the 56-d FN period. Diets were mixed at the Kansas State University feed mill (Table 1), and the lambs were adjusted to a basal diet for 14 d prior to initiation of the trial. The same diet formulation was used for the BG and FN periods. Intake was restricted to produce an average daily gain of 0.22 kg/head per d during the BG period, which was approximately half of the estimated ad libitum growth rate potential. During the FN period, which was initiated on d 57, the lambs had ad libitum access to feed. Lambs were adjusted to ad libitum access to feed by increasing the amount of feed offered each day, in increments determined at the discretion of trained personnel, to a level such that, at the end of a feeding event, some feed was left in the bunk. This stepping-up process was complete after approximately 4 d; thereafter, management was used to determine the appropriate amount of feed to be offered in each bunk daily, such that all of the feed was consumed each day. A free-choice mineral containing no vitamin A (Vita-Ferm Custom Sheep Mineral, Biozyme Inc., St. Joseph, MO) was provided throughout the experiment.
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Sample Collection
Lambs were weighed every 14 d, and blood was collected every 28 d to document the onset and extent of the differences among treatments in vitamin A concentrations in circulation. Blood samples were also used to evaluate changes in circulating FA during the experiment. Blood was collected via jugular venipuncture into 10-mL red-topped, nonheparinized tubes (Kendall, Monoject, 16 x 100 mm, Tyco Healthcare Group LP, Mansfield, MA). Blood sampling was conducted in a dimly lighted room, and care was taken to avoid exposing the tubes to light. Filled tubes were immediately placed on ice. When sampling was completed, blood tubes were returned to the laboratory and allowed to cool in a dark refrigerator at 4°C for 24 h. The tubes were then centrifuged (Beckman Coulter, Fullerton, CA) for 25 min at 2,200 x g and 4°C. Serum was pipetted into two 5-mL plastic tubes under UV-filtered light and frozen at –27°C for no longer than 90 d before vitamin A analyses were conducted.
Lambs were weighed off-test on d 112 and were slaughtered at the Kansas State University abattoir over 2 consecutive days by using humane procedures. Liver samples were collected from the caudate lobe, quick-frozen in liquid nitrogen, and then stored at –27°C for no more than 90 d until chemical analyses were conducted. Carcasses were allowed to chill for 24 h before ribbing between the 12th and 13th ribs. Marbling scores were determined by 3 experienced evaluators by using the marbling score system for USDA Beef Quality Grading and marbling picture standards. The USDA Lamb Quality Grade standards use "flank fat streaking," which is a subjective system with no reference points. Backfat thickness was measured midway over the LM and then adjusted subjectively for body wall thickness. Sections (2.54 cm thick) of the longissimus thoracis (LT) muscle and overlying subcutaneous fat were removed and stored at –27°C before chemical analyses.
Vitamin A Determination
Blood serum and liver were analyzed for vitamin A content by HPLC according to the methods described by Barua and Olson (1998). Retinyl acetate was obtained from the Department of Human Nutrition at Kansas State University and used as the internal standard. Because retinol constituted nearly 85% of the detected retinoids in our samples, vitamin A content was interpreted as the total of retinol esters present in each sample. Likewise, retinol is metabolized to a number of metabolites, namely, retinoic acid (Barua and Olson, 1998). Analyses were conducted under yellow light to minimize the deterioration of retinol. The mobile phase contained methanol with the flow rate set at 1.0 mL/min. The reverse phase was measured by using a 25-cm C-18 column. Vitamin A data were interpreted with chromatography software (Gold Chromatography Data System Version 1.6, licensed to Beckman Coulter, Fullerton, CA) by using a 320-nm spectrum with a 4-nm band. All analyses were conducted in duplicate, and the mean was reported as the value for each sample.
FA Analysis
Blood serum, liver from the caudate lobe, and a section of the LT obtained at the 12th- to 13th-rib juncture were analyzed for lipid content and FA profiles with a Shimadzu GC-17A (Shimadzu, Kyoto, Japan) gas chromatograph (GC). After 500-µL samples were freeze-dried overnight, 1 mL of benzene, containing the internal standard (1,000 µg/mL, methyl-13:0), was added and the tubes were vortexed to break up the pellet. Then, 4 mL of boron trifluoride:methanol reagent (Supelco B1252, Supelco Inc., Bellefonte, PA) was added and the tubes were mixed gently. The tubes were incubated at 60°C for 60 min. Tubes were cooled at room temperature, and 4 mL of ddH2O and 1 mL of hexane were then added and mixed vigorously. The tubes were centrifuged at 1,000 x g for 5 min, and the upper layer (1 to 2 mL) from each was transferred to a GC vial. Samples were injected at 260°C through a Supelco SP-2560 capillary column and detected at 260°C. The detector temperature was 260°C and the final oven temperature was 240°C, which was held for 15 min. Column flow rate was set at 1.1 mL/min, with a split ratio of 48:1. A Supelco 37 FA methyl ester mix was used as the external standard. All GC analyses were run in duplicate. Individual FA were expressed as the proportion of sample weight for liver and muscle, and as a proportion of the total FA content for serum.
Statistical Analyses
A completely random design with a 2 x 2 factorial arrangement of treatments was used. There were 2 pens per treatment, with either 10 or 11 lambs and either 5 or 6 lambs per pen for the BG and FN periods, respectively. The data were analyzed by using the MIXED procedure (SAS Institute, 2002). Differences in serum retinoids and FA measured over time were analyzed with the MIXED procedure by using a repeated-measures model with an unstructured covariance, which allowed us to determine the best correlation model. The model contained vitamin A status as the main effects for the BG and FN periods and their interaction. Additionally, Pearson correlation coefficients (PROC CORR of SAS) were determined for serum retinol, marbling score, percentage of IMF in the LT, back-fat thickness, liver FA concentration, and serum FA content. Paired t-tests were used to compare individual FA components in serum, muscle, backfat, and liver.
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RESULTS AND DISCUSSION |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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Liver is the primary storage site for vitamin A, and its depletion from the liver is critical in establishing divergent treatment effects (Goodman, 1984). Serum levels of retinol were used as an indicator of vitamin A status in the liver because a significant logarithmic relationship between serum and liver concentrations of vitamin A has been demonstrated in lambs (May et al. 1987) and in steers (r = 0.77, P < 0.01; Oka et al., 1998). Serum retinol was not different (P > 0.10) between lambs from the high and low vitamin A BG treatments on any sampling day during the BG period (18, 21, and 24 vs. 17, 20, and 18 µg/dL of serum on d 0, 28, and 56 for the high and low vitamin A treatments, respectively; Figure 1). Serum levels differed (P < 0.10) by d 84 between the HH and LL lambs (25 vs. 15 µg/dL, respectively; Figure 2). This difference remained throughout the rest of the experiment. Divergence in serum levels of retinol is often delayed, and levels in blood sometimes rise when dietary vitamin A sources are removed and hepatic stores are mobilized (McDowell, 1989). Thus, disappearance of vitamin A from the blood tends to take longer in animals with greater stores of hepatic vitamin A, and hepatic stores are generally greater in animals with high dietary intake of vitamin A or in older animals that may have accumulated significant reserves (Riggs, 1940). There were no differences in serum retinol (P > 0.10) between the HL and LH lambs throughout the FN period. Because liver is the primary storage site, vitamin A was not measured in fat depots.
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Average initial BW was 28.8 kg for all lambs (Table 2) and BW were not different (P > 0.10) among treatments. Although a divergence in circulating vitamin A was achieved by d 56, no negative effects on growth performance among treatments were detected (P > 0.10) for the BG, FN, or combined feeding periods. Average final BW for all treatments was 60.9 kg (Table 2). Average daily gain for all treatments was 0.28 kg/head over the entire experimental period and did not differ among treatments (P > 0.10) for the BG, FN, or combined feeding periods. These findings are consistent with those of May et al. (1987), who reported no significant linear or quadratic effects of vitamin A levels for live weight gain, feed intake, or feed efficiency when lambs received vitamin A supplementation ranging from 2 to 64 µg/kg of BW per d for 16 wk. Bruns and Webb (1990) reported similar growth rates between vitamin A-deficient and vitamin A-sufficient lambs during initial feeding, but decreased growth performance in vitamin A-deficient lambs during later stages of growth. A similar pattern of growth performance was reported by Oka et al. (1998) in cattle fed high or low vitamin A diets. However, feeding less than half the NRC recommended level of vitamin A to Angus cross steers for 168 d did not reduce DMI, ADG, or G:F (Gorocica-Buenfil et al., 2005). However, retinoic acid, a form of vitamin A, regulates growth hormone gene expression (Bedo et al., 1989) and has increased growth rates of cattle (Perry et al., 1968). Several factors, including the extent and duration of depletion, chronological age, phase of growth, species, and other environmental conditions, likely contribute to the discrepancies in growth performance reported in these studies. Research is warranted to describe how vitamin A depletion over time affects the growth performance of ruminants in US livestock production systems.
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Several investigators in countries supplying Asian beef markets have associated serum retinol content with beef carcass marbling scores. Oka et al. (1998) reported a correlation between serum vitamin A concentration and beef marbling score (Japanese scale) of –0.38 (P < 0.05). Similarly, Adachi et al. (1999) demonstrated a negative correlation between vitamin A level in cattle blood and marbling score. Currently, little information is available on the relationship between serum retinol status and marbling development in US lamb and beef production. In our study, however, serum retinol concentration was positively correlated with, and a moderate predictor of, marbling score (r = 0.30; P = 0.07) and total extractable lipids (r = 0.31; P = 0.06) in lamb carcasses.
Results from the Japanese studies likely differed partially because of feeding cattle much longer and feeding to older chronological ages than is deemed ideal in most US beef production systems. Depletion of dietary vitamin A for extended periods in the Japanese studies would likely have caused greater depletion of liver stores, thus increasing the correlation between serum vitamin A and marbling score in these studies. Our data oppose the findings of Oka et al. (1998) and Adachi et al. (1999) and tend not to support those of Pyatt et al. (2005), who studied the effects of dietary vitamin A level on marbling development in a US beef production model. We were surprised by our findings and suggest that the relationship between serum levels of vitamin A and marbling deposition in lambs is different from that reported in cattle. The mechanism by which this relationship may be opposite in sheep is not clear, although differences in fat levels contained in the liver and IMF storage depots suggest a preferential effect related to blood retinol. These fat differences are reported herein.
Serum FA Concentration
Concentration of FA in serum increased with time throughout the BG period in both treatments (Figure 3). On the last day of BG (d 56), serum FA had increased to 831 and 820 µg/g for the high and low vitamin A treatments, respectively. Interestingly, serum FA concentration peaked on d 56 in all treatments, and then decreased (P < 0.01) in all treatments 28 d into the FN period (d 84; Figure 4). Following the decrease in serum FA midway through the FN period (d 84), serum FA concentration increased in all treatments for the remainder of the FN period. Serum FA concentrations were not different (P > 0.10) by treatment on the last day of the FN period. The magnitude of FA decline (d 56 to 84) was considerably greater (P < 0.05) in the HL and LH treatments. The reason for the decrease in these 2 treatments is not clear; however, the stress of comingling lambs from different BG treatments with those in the new FN treatments and the establishment of new social hierarchies early in the FN period may be partly responsible. Lambs that were switched from high to low, or low to high vitamin A treatments were also presented with more new pen mates than lambs remaining on the same treatment through the BG and FN periods. Additionally, all of the lambs endured extremely hot days during the FN period, which may have affected FA circulation and storage. These data are supported by Oka et al. (1998), who reported no differences in serum FA concentrations of Japanese Black steers fed diets containing high or low vitamin A, despite differences in the FA content of liver and muscle. Adachi et al. (1999) found no differences in nonesterified FA in serum of Japanese Black steers finished on diets containing either high or low levels of vitamin A.
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). The correlation of serum FA on the last day of the trial with 12th-rib backfat depth was –0.36 (P = 0.03), whereas it was –0.33 (P = 0.04) with marbling score and –0.38 (P = 0.01) with percentage of IMF in the LT. These data indicate a negative relationship between serum FA and fat deposition at 2 distinct anatomical locations, suggesting that serum FA content may be useful in predicting total FA content in the various tissues. Because of the moderate correlations reported here, more research would be useful in characterizing the relationship between serum and tissue FA concentrations as affected by vitamin A status. Currently, there are no published data describing the effects of vitamin A level on serum or tissue FA content in lambs.
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Backfat Thickness.
Because the genetic composition and live weights were similar, carcass weights and loin eye area were not considered in the analysis. Fat depth was measured midway over the LT at the 12th rib and then adjusted for differences in thickness of the body wall. Average fat thickness was 0.71 cm for all treatments (Table 2
). Carcasses from HL and LH treatments tended to be fatter (P = 0.08) than those from the LL and HH treatments. Fat thickness is an important consideration here, because similar studies involving beef cattle have reported that dietary vitamin A content may influence marbling deposition in the LM without increasing backfat thickness (Oka et al., 1998; Gorocica-Buenfil et al., 2005). Determination of feeding practices such as these, which have the potential to increase marbling without increasing deposition of backfat, are desirable for livestock producers, processors, and consumers.
Marbling Scores.
It is common practice in the United States to grow cattle, and sometimes lambs, on forage-based diets for several months (i.e., BG) before finishing on high-energy grain diets. When BG is done on lush spring pastures, these animals are likely consuming 100,000 to 300,000 IU/kg of vitamin A in forage (Pyatt and Berger, 2005). Large amounts of vitamin A may become stored in liver and fat tissues during this period. The effect of high vitamin A intake, either from BG on lush green pastures or from high supplemental intake during the FN period, may be detrimental to carcass marbling deposition. Consequently, to examine these effects in lambs, a BG period was included in our study immediately preceding the FN period. Average marbling score for all treatments was 484 degrees (i.e., Small84). Lambs fed high vitamin A diets during the FN period tended to have greater (P < 0.10) marbling scores than those fed low vitamin A diets (Table 2). The HH and LH treatments produced carcasses containing Modest degrees of marbling (514 and 519 degrees, respectively), whereas carcasses from lambs fed the HL and LL diets contained Small degrees of marbling (445 and 459 degrees, respectively). Marbling scores were greater (P < 0.05) in HH and LH lambs than in HL lambs and LL lambs (514 and 519 vs. 445 and 459 marbling degrees, respectively; Table 2). These data suggest that feeding high vitamin A diets to lambs for 56 d prior to slaughter will increase marbling scores. Interestingly, when Japanese Black steers were fed either low or high vitamin A diets after 23 mo of age and slaughtered at 33 mo, there were no differences in marbling score when using the Japanese scale. However, when steers were placed on high or low vitamin A diets beginning at 15 mo of age and slaughtered at 31 mo, marbling scores were greater in cattle fed low vitamin A diets (Oka et al., 1998). When Angus steers (12 mo of age) were fed either high or low vitamin A diets for 10 mo, there were no differences in marbling scores when either the Australian or USDA grading system was used (Kruk et al., 2004). Similarly, Pyatt et al. (2005) found no difference (P > 0.05) in marbling score or the percentage of carcasses grading low or premium Choice between Angus x Simmental steers and heifers fed either low or high vitamin A (3.3x NRC) diets. Gorocica-Buenfil et al. (2005) reported a trend for a 10% increase in marbling scores and percentage of carcasses graded USDA Choice from beef steers that were provided no supplemental vitamin A for 168 d vs. those provided 2,700 IU of vitamin A/kg of dietary DM (P = 0.11 for marbling score and P = 0.13 for percentage of Choice). Vitamin A effects on cattle marbling scores are not consistent and generally contradict our findings in lambs. Clearly, the effects of age and time on feed are important considerations in depleting vitamin A and altering marbling deposition. These effects should be considered further in lambs to clarify the potential for high or low vitamin A diets to affect marbling deposition in different species of livestock.
Tissue FA Concentration
FA Concentration in the LT.
Content of FA in the LT provided an objective measure of IMF deposition to evaluate the effects of vitamin A treatment. This is arguably the most important determination made in this study because of our interest in extrapolating these differences to potential USDA Quality Grade differences in cattle that might be observed when cattle are treated similarly (i.e., no supplemental vitamin A and high vitamin A). The percentage of IMF in the LT was assessed by GC, and was intended to substantiate the marbling scores by using an objective method. Percentage of IMF is reported as total FA as a proportion of the LT sample weight (Table 2 and Figure 5). The results of our study in lambs contradict the findings from similar research conducted with cattle. In general, feeding lambs low levels of vitamin A decreased IMF, feeding high levels increased IMF, and feeding high and low levels in BG and FN combinations resulted in intermediate IMF, regardless of the combination (HL or LH). Lambs from the LL treatment produced carcasses with the lowest percentage of IMF and were different (P < 0.05) from the HH treatment (3.1 vs. 3.9% IMF for LL and HH, respectively). The HL and LH treatments produced carcasses containing intermediate IMF (3.5 and 3.4% IMF, respectively) compared with the LL or HH treatments and were not different compared with the LH and HL treatments (P > 0.10). Furthermore, this relationship suggests that a linear model may explain the relationship between vitamin A status and marbling deposition in lambs.
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). When Large White x Landrace x Duroc finisher gilts were fed diets containing no supplemental vitamin A, they had greater (P = 0.002) IMF content in the LM than supplemented gilts (D’Souza et al., 2003). Research reports describing the relationship between dietary vitamin A intake and IMF accumulation in the LT are inconsistent, and further investigation is warranted to mitigate these discrepancies.
FA Composition of the LT.
Changes in unsaturated FA were of particular interest because increased concentrations of these FA in human diets have been associated with a reduction of certain cancers and the risk of heart diseases, such as coronary artery disease (Simopoulos, 1991). There were no differences (P > 0.10) in the unsaturated FA content in s.c. fat deposited over the LT among the 4 treatments, which includes all monounsaturated and polyunsaturated FA that were detected by GC. Therefore, these data are not shown. Oleic acid (18:1n-9 cis) was greater (P < 0.02) in the LT of carcasses from the HH lambs compared with LL lambs (Table 4). This increase accounts for more than half of the increase in total FA observed in the HH carcasses. Interestingly, this advantage in IMF deposition in HH lambs did not come in the form of linoleic acid, which has been shown to be of potential benefit to human health (Scollan et al., 2006). Rather, linoleic acid was the lowest in HH lambs and greatest in concentration in IMF from LL lambs (6.4 vs. 7.8% for HH and LL, respectively; P < 0.05). In retrospect, assays of desaturase enzyme activities would have strengthened our understanding of this relationship and may have explained how vitamin A affects the activity of these enzymes in vivo. Concentrations of oleic and linoleic acids from the LT of both crossover treatments (HL and LH) were intermediate, substantiating the likelihood of a linear relationship between dietary vitamin A status and content of unsaturated FA in lamb loin meat. These data suggest that feeding diets high in vitamin A for at least 112 d will increase the concentration of monounsaturated fat, but will decrease the amount of polyunsaturated fat in the LT. This feeding protocol may help characterize lamb meat as a source of heart-healthy protein. This result contradicts the findings of Daniel et al. (2004), who fed growing lambs vitamin A for 21 d and increased levels of palmitoleic and oleic acids in liver and adipose tissues, and concluded that manipulation of dietary vitamin A was not a suitable method of increasing unsaturated fat content in lamb meat. It is questionable whether feeding either high or low levels of vitamin A for only 21 d in the study by Daniel et al. (2004) was enough time to create significant changes in tissue FA concentrations.
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and Figure 5). Lambs from the LL treatment had a lower (P < 0.01) concentration of liver FA than those in other treatments (3.4 vs. 3.7, 3.8, and 3.6 for the LL, HH, HL, and LH treatments, respectively). Although total FA content from the liver of HL lambs was numerically the greatest, it was not different from the HH or LH treatments (P > 0.10). Nonetheless, this trend of greater FA in HH lambs and lower FA in the liver of LL lambs is consistent with the FA profiles of the LT muscle. Coupled with the greater FA content of LL and lower FA content of HH serum of these lambs, vitamin A appears to be interacting with the mechanism of uptake of long-chain FA from blood and subsequent storage.
FA Composition in the Liver.
Although lamb liver from the HH and HL treatments contained more total FA (P < 0.02) than liver from the LL treatment, the concentration of monounsaturated FA was greater in the LL treatment. Both isomers of oleic acid were greater (P < 0.05) in the liver from LL lambs than HH lambs (Table 5). The cis isomer contributed more to the total FA content and was greater in LH and LL than in the other treatments (P < 0.02). By contrast, the cis isomer for IMF was greatest in the HH treatment. High vitamin A caused increased monounsaturation as fat became stored as marbling, compared with those FA stored in the liver. The mechanisms responsible for differences in FA saturation by storage depot are likely related to the desaturase enzymes, but the means by which they can be regulated at different depots in vivo remains unclear. The concentration of linoleic acid was not different in the liver tissue (P > 0.20). In our study, there is no clear relationship between the levels of linoleic acid in the liver and IMF depots.
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1 Corresponding author: mdikeman{at}ksu.edu
Received for publication March 19, 2007. Accepted for publication July 11, 2007.
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LITERATURE CITED |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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. Mol. Cell. Biol. 16:1567–1575.This article has been cited by other articles:
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  A. Arana, J. A. Mendizabal, M. Alzon, B. Soret, and A. Purroy The effect of vitamin A supplementation on postnatal adipose tissue development of lambs J Anim Sci, December 1, 2008; 86(12): 3393 - 3400. [Abstract] [Full Text] [PDF]
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