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ANIMAL PRODUCTION |
* Department of Animal and Dairy Science, University of Georgia, Athens 30602-2771 and
and
Department of Animal Science, University of Missouri, Columbia 65211-5300
Abstract
Thirty-six Angus x Hereford heifers (365 kg) were used to determine effects of dietary lipid supplementation from two sources during the final 32 or 60 d of feeding on serum and adipose tissue leptin concentrations, animal performance, and carcass characteristics. Following an initial feeding period of 56 d, heifers were fed one of three diets in a 3 x 2 factorial arrangement: 1) basal diet, 2) basal diet plus 4% (DM basis) corn oil, or 3) basal diet plus 2% (DM basis) rumen-protected conjugated linoleic acid (a mixture of Ca-salts of palm oil fatty acids with 31% conjugated linoleic acid). Jugular blood samples were collected at 28-d intervals (d 28 to 118) and serum subsequently harvested for leptin quantification via RIA. Real-time ultrasound measurements were collected at 28-d intervals across time on feed. At slaughter, samples were obtained from various adipose depots. Data were analyzed with dietary treatment, length of supplementation, adipose depot (when appropriate), and all two- and three-way (when appropriate) interactions in the repeated measures model. Measures of feedlot performance, including ADG, DMI, and gain:feed did not differ (P > 0.23) with dietary treatment or supplementation length. Heifers supplemented with corn oil tended (P < 0.07) to have higher marbling scores following 32 d of treatment than those supplemented with rumen-protected conjugated linoleic acid, with controls intermediate. Quality grade and hot carcass weight did not differ (P > 0.15) with treatment or length of supplementation. Leptin concentrations were higher (P < 0.05) from d 57 to 118 on feed than the initial period (d 0 to 56) of dietary adaptation when all animals received the basal diet. Circulating leptin concentrations were not affected by dietary treatment. However, leptin concentrations in adipose tissues were greater (P < 0.05) for heifers supplemented with corn oil than either control or rumen-protected conjugated linoleic acid diets, which did not differ. Compared with adipose tissues from rumen-protected conjugated linoleic acid-supplemented animals, tissues from heifers fed corn oil contained 68% greater leptin concentration. Correlations between performance, carcass traits, and serum leptin concentrations were low. Serum leptin concentrations across time on feed were not associated with carcass and performance data, including ADG, DMI, and gain:feed. Based on these data, concentrations of leptin are not related to indices of feedlot performance and carcass quality in beef cattle.
Key Words: Beef • Conjugated Linoleic Acid • Leptin
Introduction
During ruminal biohydrogenation of dietary unsaturated lipids, unique fatty acid intermediates termed conjugated linoleic acid (CLA) and trans-vaccenic acid are produced in addition to saturated end products (Bauman et al., 1999
, Enser et al., 1999; Scollan et al., 2001). Conjugated linoleic acid refers simply to the positional and geometric isomers of linoleic acid. In particular, the cis-9, trans-11 and trans-10, cis-12 CLA isomers have been shown to possess anticarcinogenic (Ha et al., 1987) and repartitioning properties (Wiegand et al., 2001; Yamasaki et al., 2003), respectively. Ruminant milk and meat products represent the largest natural source of CLA. Research in dairy cattle has shown that supplementing CLA salts or vegetable oils increases the cis-9, trans-11 CLA isomer in milk fat (Kelly et al., 1998; Enser et al., 1999; Corl et al., 2001). Additionally, research in lactating dairy cattle (Chouinard et al., 1999; Baumgard et al., 2001) as well as lactating sows (Bee, 2000) has shown that supplementing CLA in diets alters lipid metabolism and results in depressed milk fat synthesis.
Leptin, a 16-kDa protein synthesized and secreted by adipocytes, functions to regulate energy homeostasis and serves as a circulating signal of adiposity through coordination with neuroendocrine function (Houseknecht et al., 1998; Barb et al., 2002). Circulating leptin concentrations are well correlated with adiposity as well as adipocyte size for animals in a state of positive energy balance (Houseknecht et al., 1998). However, research as to how dietary manipulations may alter circulating leptin concentrations or carcass characteristics is limited, particularly in ruminant animals consuming high-concentrate diets. The objective of this study was to determine the effects of supplemental corn oil, composed predominantly of linoleic acid, or rumen-protected CLA on serum and adipose tissue leptin concentrations, animal performance, and carcass traits in feedlot beef cattle.
Materials and Methods
Animals and Diets
Thirty-six Angus x Hereford heifers (365 ± 60 kg) obtained from the Northwest Georgia Experiment Station in Calhoun were used in a completely randomized design to determine the effect of lipid source on leptin levels. Treatment effects on circulating leptin concentration were evaluated in a 3 x 2 factorial arrangement with three diets (control, 4% corn oil, or 2% rumen-protected CLA salt) fed for the last 32 or 60 d before slaughter, corresponding to a time on feed of 89 or 118 d. Following an initial feeding period of 56 d (basal diet), heifers were fed one of three dietary treatments (DM basis): 1) basal diet containing 88% concentrate and 12% grass hay (CON); 2) basal diet plus 4% corn oil (OIL); or 3) basal diet plus 2% rumen-protected CLA salt (RPCLA), containing 31% CLA-60. The RPCLA supplement was composed of a mixture of Ca-salts of palm oil fatty acids and CLA, which contained 22.1% palmitate, 4.8% stearate, 27.4% oleate, 7.1% linoleate, and 31% CLA (27.2% cis-9, trans-11; 32.8% trans-10, cis-12; 10.6% trans-8, cis-10; 18.95% cis-11, trans-13; and 10.5% various trans, trans conjugated linoleic acid isomers). Rumen-protected CLA salt was generously provided by Agribrands Purina Canada, Inc. (Ontario, Canada). Animal handling procedures for this study were approved by the University of Georgia Animal Care and Use Committee. The study was conducted from January to May.
Ingredient and chemical composition of the three diets are shown in Table 1. Dietary treatments were formulated to be isonitrogenous; as supplemental lipid was included, an equal proportion of concentrate was removed. Synovex-H implants (20 mg of estradiol benzoate and 200 mg of testosterone; Ft. Dodge Animal Health, Ft. Dodge, IA) were administered to all animals at trial initiation. Melengesterol acetate (Pharmacia, Kalamazoo, MI) was fed throughout the trial at 0.45 mg•heifer-1•d-1. Rumensin-80 (Elanco Animal Health, Greenfield, IN) was fed throughout the trial at 250 mg of monensin activity•heifer-1•d-1.
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Real-Time Ultrasound Data
Real-time ultrasound measures were collected across time on feed to assess s.c. fat thickness and longissimus muscle area (LMA). Transverse scans for fat thickness and LMA prediction were obtained at the interface between the 12th and 13th rib by a certified technician using an Aloka 500-V ultrasonograph (Corometrics Medical Systems, Wallingford, CT) equipped with a 17-cm, 3.5-MHz linear probe. Beef Information Manager software, Version 3.0 (Critical Vision, Inc., Atlanta, GA) was used for image interpretation.
Serum Sampling
Blood samples were obtained by jugular venipuncture directly into collection tubes containing no anticoagulant on d 28, 56, 89, and 118 of the trial; samples were collected at 0800 before feeding. Blood samples from fasted animals were obtained at slaughter. Samples were stored on ice before transport to the laboratory. Samples were stored overnight at 4°C, centrifuged at 1,600 x g, and serum harvested. Aliquots were stored at -80°C for subsequent leptin quantification.
Leptin Assays
Following trial completion, serum samples were shipped on dry ice to the University of Missouri, Columbia, for leptin analysis. Serum leptin concentrations were determined by RIA according to Delavaud et al. (2000). Assays were performed in duplicate aliquots of 200 µL with inter- and intraassay coefficients of variation of less than or equal to 10%.
Carcass Data
Heifers were randomly allotted to dietary treatments (12 heifers/treatment) at trial initiation. After 90 d on feed (32 d of supplementation), heifers (six heifers/treatment) that had 1.27 cm or greater s.c. fat thickness were slaughtered. The remaining heifers (six heifers/treatment) were fed the treatment diets to reach a similar s.c. fat thickness end point (
1.27 cm), which required an additional 28 d on the dietary treatments, and then slaughtered. This approach allowed us to attain the same compositional end point for each supplementation length in order to ascertain the true effects of dietary supplementation. It is well documented (Mendell et al., 1997; Duckett et al., 1993) that differences in compositional end points influence animal production and carcass quality. Animals were transported to the University of Georgia’s Meat Science and Technology Center (Athens, GA) following overnight feed withdrawal, and fasted live animal weights were recorded before slaughter.
Subcutaneous adipose tissue samples were removed from the 12th rib and perianal region of the left side of carcasses before chilling and immediately frozen at -20°C for subsequent leptin analyses. Hot carcass weights were recorded following trimming. Following a 48-h chilling period, carcass measurements—including, adjusted fat thickness; LMA; marbling score; percentage of kidney, pelvic, and heart fat (KPH); skeletal maturity; and USDA quality and yield grades—were determined by five trained evaluators. Rib sections were obtained from right sides and 2.54-cm-thick steaks removed, trimmed, and frozen at -20°C for subsequent determination of intramuscular leptin amounts.
Protein Assays and SDS-PAGE
Adipose tissue samples from (animals fed treatment diets for 60 d only) s.c. and perianal depots as well as i.m. lipid dissected from sections of longissimus muscle were homogenized in 1x lysis buffer (60 nmol/L Tris, pH 6.8, and 10 g/L SDS) with a ratio of 2:1 of tissue weight and centrifuged at 1,600 x g for 15 min at 4°C to remove insolubles. Total protein concentration of sample lysates was determined using a Bio-Rad DC protein assay kit (Bio-Rad Laboratories, Hercules, CA). Adipose tissue extracts containing 30 µg of total protein were diluted in SDS-sample buffer and subjected to SDS-PAGE under reducing conditions according to method of Laemmli (1970) in 15% polyacrylamide gels. Prepared tissue proteins, prestained molecular weight protein marker (Bio-Rad), and leptin standard (Sigma Chemical Co., St. Louis, MO) were loaded onto gels, and electrophoresis was conducted for 35 min at 200 V. Protein bands were visualized using GelCode SilverSnap Stain kit (Pierce, Rockford, IL). Gel images were obtained and densitometry calculations performed using an Alpha Innotek Imager (San Leandro, CA); densitometry measures were standardized based upon the inclusion of the leptin standard.
Statistical Analysis
Data were analyzed using the GLM procedure of SAS (SAS Inst. Inc., Cary, NC), with individual heifer serving as the experimental unit. Performance, serum leptin, and ultrasound data for each animal were analyzed using the repeated measures analysis of the GLM model of SAS. Differences due to dietary treatment (CON, OIL, and RPCLA), length of lipid supplementation (32 vs. 60 d), and the two-way interaction were tested with the between-subjects error term. Differences due to time on feed (28, 56, 89, or 118 d) and all possible interactions that included time on feed were tested using the within-subjects error term. For carcass data, the model included the effects of dietary treatment, supplementation length, and the two-way interaction. For leptin adipose tissue concentrations, the model included the effects of dietary treatment, adipose depot (i.m., perianal, and s.c.), and the two-way interaction. Differences were separated using least squares means procedure of SAS. Agreement between carcass and ultrasound variables was determined using the regression procedure of SAS. Pearson correlation analysis was used to analyze the relationship between serum leptin concentration and independent variables. Significance was determined at P 
0.05; differences of P > 0.05 to P 0.10 are discussed as trends.
Results and Discussion
Performance data for feedlot heifers are presented in Table 2. All interactions between dietary treatment and length of supplementation for animal performance were nonsignificant, which demonstrate that the effects observed for dietary treatments are consistent across supplementation length. Inclusion of RPCLA increased (P < 0.05) ADG from d 57 to 89 of treatment compared with OIL or CON treatments. Daily gains were similar between animals fed treatment diets from d 90 to 118. In contrast, Gassman et al. (2000) reported that rumen-protected CLA supplementation decreased ADG by 25%. Feed intake did not differ by dietary treatment, length of lipid supplementation, or the two-way interaction. Gassman et al. (2000) reported reductions in feed intake when 2.5% rumen-protected CLA was supplemented to feedlot cattle diets. Gain efficiency (gain:feed) was improved (P < 0.05) for RPCLA from d 57 to 89 on feed compared to either OIL or CON treatments, which were similar. However, gain efficiency (gain:feed) as well as ADG were lower for all animals from d 90 to 118, with no differences between dietary treatments. Gassman et al. (2000) observed no differences in gain efficiency values between control and rumen-protected CLA salt that was supplemented feedlot cattle. Similarly, Garcia et al. (2003) fed 5% whole sunflower seed containing approximately 70% linoleic acid and observed no differences in the live weight, ADG, or carcass weight of beef heifers compared to those fed no dietary lipid supplement.
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), swine (Thiel-Cooper et al., 2001; Wiegand et al., 2001), and dairy cattle (Chouinard et al., 1999; Baumgard et al., 2001) has demonstrated that CLA supplementation improves animal performance, reduces animal adiposity, and alters lipid metabolism. Although several positional and structural isomers of CLA exist, two in particular have been implicated as biologically active. The cis-9, trans-11 isomer has anticarcinogenic effects (Ha et al., 1987), whereas the trans-10, cis-12 CLA isomer possesses repartitioning properties that result in reduced body fatness (Yamasaki et al., 2000; Rahman et al., 2001). Wiegand et al. (2001) showed that CLA supplementation in swine increased gain:feed ratio compared to control animals, with no differences in ADG observed between treatments. Results from this study and Gassman et al. (2000) indicate that feeding rumen-protected CLA salt does not affect animal performance in beef cattle to the same extent reported for swine (Thiel-Cooper et al., 2001; Wiegand et al., 2001) and laboratory animals (Azain et al., 2000).
Figure 1 depicts changes in subcutaneous fat thickness (FT) across time on feed. Dietary treatment did not alter ultrasound measures of FT across time on feed. Subcutaneous FT increased (P < 0.05) in a linear manner for heifers fed supplemental lipid for 32 d (FT cm = 0.7637 + 0.0091 x time on feed, d; r2 = 0.5958) or 60 d (FT cm = 0.5338 + 0.0087 x time on feed, d; r2 = 0.7461) before slaughter. The rate of subcutaneous FT deposition reported in this study is similar to that reported by Nash et al. (2000) for Limousin x Angus heifers. Heifers utilized in the current trial were backgrounded on pasture for 112 d and were heavier at the onset of the study than those used in Nash et al (2000). Ultrasound LMA measures across time on feed are shown in Figure 2. Supplementing feedlot diets with corn oil or rumen-protected CLA salt did not alter ultrasound LMA measurements. Longissimus muscle area increased in a linear manner (32-d LMA, cm2 = 53.98 + 0.20 x time on feed, d; r2 = 0.44 and 60-d LMA, cm2 = 52.25 + 0.19 x time on feed, d; r2 = 0.64) across time on feed. The rate of increase in LMA is similar to rates reported by Nash et al. (2000) as well as May et al. (1992) for Angus x Hereford steers.
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; Minton et al., 1998) have indicated that circulating leptin concentrations may indicate ultimate carcass composition in beef cattle.
Carcass characteristics did not differ by length of supplementation (Table 3). Hot carcass weight, dressing percentage, s.c. fat thickness, longissimus muscle area, percentage KPH, yield grade, and quality grade were similar across time on treatment and among diets. Azain et al. (2000) observed reduced peritoneal and parametrial fat pad weights in Sprague-Dawley rats fed 0.25 or 0.5% CLA, which were attributed to decreased cell size rather than cell number. Similarly, subcutaneous as well as intramuscular lipid was reduced in barrows fed 0.12 to 1.0% CLA (Thiel-Cooper et al., 2001). Wiegand et al. (2001) also observed decreased backfat thickness in barrows fed 0.75% dietary CLA. Isomers of CLA containing a trans-10 bond have been implicated as being those responsible for such repartitioning effects. Reductions in milk fat synthesis in lactating dairy cattle observed by Baumgard et al. (2001) were associated with increasing doses of abomasal trans-10, cis-12 CLA infusions. Gassman et al. (2000) additionally reported a numeric decrease in s.c. fat thickness measurements as the percentage of CLA fed increased. However, in that study, Continental-cross steers were fed CLA an average of 133 d.
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). Gassman et al. (2000) reported lower marbling scores in feedlot cattle when 2.5% rumen-protected CLA was fed. Andrae et al. (2001) reported that marbling scores increased in steers fed high-oil corn compared to traditional corn varieties. Carcasses from heifers fed for 32 d tended (P = 0.10) to have greater marbling scores than those fed for 60 d. Research has previously shown that i.m. lipid deposition occurs in a nonlinear manner across time on feed in cattle. In Angus x Hereford steers, i.m. fat percentage doubled between d 84 and 112 on feed, with no changes occurring in additional days on feed (Duckett et al., 1993). In this study, feeding an additional 28 d did not improve marbling scores. Carcass values were determined using a value-based marketing grid with no differences observed between dietary treatments (Table 3). However, carcasses from heifers fed supplemental corn oil were valued, on average, at approximately $30 and $18 greater than those from CON or RPCLA-treated animals, respectively.
Circulating leptin concentrations did not differ by dietary treatment at any time during the trial (data not shown). Serum leptin levels were lower (P < 0.05) for heifers during the first half of the feeding period (d 0 to 59; 12.22 ng/mL serum) than the last half (d 60 to 118; 13.89 ng/mL serum). These mean values are high, reflecting good body condition scores at trial initiation as well as the propensity for females to have higher circulating leptin levels compared to males (Chow and Phoon, 2003). As the heifers increased in adiposity over the finishing period (see Figure 1), as expected, a concomitant increase in serum leptin concentration was observed. Similarly, Garcia et al. (2003) reported no dietary effects on serum concentrations of leptin in beef heifers fed linoleic acid-rich diets. Baumgard et al. (2002) also reported no differences in plasma leptin concentrations when late-lactation dairy cattle received abomasal infusions of either cis-9, trans-11 or trans-10, cis-12 CLA isomers.
Conjugated linoleic acid supplementation has been linked to reductions in circulating leptin concentrations in humans (Medina et al., 2000) and laboratory animals (Yamasaki et al., 2000; Rahman et al., 2001). However, Cha and Jones (1998) demonstrated that feeding fish oil or safflower oil to Sprague-Dawley rats resulted in leptin values 60% higher than those animals fed beef tallow. Similarly, feeding corn oil to rats (Iritani et al., 2000) increased plasma leptin concentrations and upregulated leptin mRNA expression compared to feeding fat-free diets.
Although no dietary effects on circulating leptin concentration were observed, a treatment effect was established at the tissue level. The effect of dietary treatment on adipose tissue leptin concentration is shown in Figure 3. Heifers fed supplemental corn oil had 68% higher (P < 0.01) concentrations (µg leptin/µg protein in adipose tissue) of leptin in adipose depots compared to RPCLA and CON animals. An example of a 15% silver-stained SDS-PAGE image is illustrated in Figure 4.
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; Gottschling-Zeller et al., 1999). Additionally, Rosenbaum et al. (2001) showed that leptin expression was higher in subcutaneous compared with visceral adipose tissue in women. In laboratory animals, epididymal and retroperitoneal adipose tissues express higher leptin mRNA levels than inguinal depots (Villafuerte et al., 2000; Zhang et al., 2001). In cattle, the opposite has been observed, with visceral adipocytes displaying greater leptin tissue expression than subcutaneous adipocytes (Chilliard et al., 2001; Ren et al., 2002).
Circulating leptin concentration is associated with animal adiposity and has been suggested as a factor for correlation with carcass characteristics. Geary et al. (2003) reported positive correlations between serum leptin concentrations and marbling score (r = 0.35 and 0.50), fat depth (r = 0.34 and 0.46), KPH (r = 0.42 and 0.46), and quality grade (r = 0.36 and 0.39) in two differing genetic lines of beef cattle. In this study, serum leptin concentrations were not well correlated with either performance (ADG, DMI, and gain:feed) or carcass characteristics. However, there was a trend (P < 0.08) for a low yet positive correlation (r = 0.30) between the rate of leptin increase across time on feed and carcass marbling score. Similarly, the rate of increase in serum leptin concentration for animals fed dietary treatments for 60 d tended (P < 0.06) to be negatively correlated with total gain (r = -0.45) as well as gain:feed (r = -0.44). However, serum leptin concentrations for heifers supplemented 60 d were positively associated (r = 0.47, P < 0.05) with dressing percent. Additionally, the percentage of KPH fat was positively associated (r = 0.50, P < 0.05) with the rate of increase in serum leptin concentrations across time on feed for heifers supplemented a total of 60 d before slaughter.
Others have reported circulating leptin concentrations to be well correlated with measures of fatness in sheep (Daniel et al., 2002) as well as cattle (Ehrhardt et al., 2000). In fed ewes, Daniel et al. (2002) reported high correlation between fat thickness and mean plasma leptin concentrations (r = 0.72, P < 0.02). Similarly, plasma leptin concentration was highly related to carcass fat (r = 0.91, P < 0.001) in calves receiving milk replacer to 105-kg body weight (Ehrhardt et al., 2000). Ehrhardt et al. (2000) also evaluated the relationship between circulating leptin concentration and fatness indicated by the assignment of body condition score in dairy cattle during late lactation (r = 0.37, P < 0.01). Kawakita et al. (2001) additionally reported backfat thickness (r = 0.28) as well as marbling score (r = 0.39) to be positively correlated with the rate of increase in serum leptin concentrations in Wagyu steers.
Implications
Supplemental lipid as rumen-protected conjugated linoleic acid or linoleate-rich corn oil added to feedlot cattle diets did not alter animal performance, fat, or muscle accretion as measured by real-time ultrasound, carcass measurements, or mean serum leptin concentrations. The addition of corn oil to feedlot diets improved marbling scores and increased leptin content in all adipose tissues. Serum leptin concentrations were not highly associated with carcass quality or performance data.
Footnotes
1 Supported in part by Cattlemen’s Beef Board and National Cattlemen’s Beef Association. 
2 Correspondence: 206 Edgar L. Rhodes Center for Animal and Dairy Science (phone: 706-542-0942; fax: 706-542-0399; e-mail: sduckett{at}uga.edu).
Received for publication May 28, 2003. Accepted for publication October 28, 2003.
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