J. Anim Sci. 2008. 86:390-396. doi:10.2527/jas.2006-671
© 2008 American Society of Animal Science
The effect of dietary copper supplementation on fatty acid profile and oxidative stability of adipose depots in Boer x Spanish goats1
K. A. Cummins*,2,
S. G. Solaiman
and
W. G. Bergen*
* Department of Animal Sciences, Auburn University, Auburn, AL 36849; and
Department of Agriculture and Environmental Sciences, Tuskegee University, Tuskegee, AL 36088
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Abstract
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A feeding trial was designed to examine the effects of copper sulfate pentahydrate (CuSO4.5H2O) on the fatty acid composition and oxidative stability in muscle and adipose tissues of Boer x Spanish goat kids. Fifteen (n = 5 per treatment) goats were fed 0, 100, or 200 mg of supplemental Cu per day as copper sulfate for 98 d. The animals were slaughtered, and LM, s.c. adipose from the sternal region, and mesenteric adipose tissues were collected. Total lipids were extracted with chloroform:methanol (2:1), methylated and isolated via GLC from all tissues. The subsequent peaks were then positively identified by mass spectrometry. Thiobarbituric acid-reactive substances were measured also. In s.c. adipose, dietary Cu significantly decreased C14:0 (P = 0.03) and C16:0 (P = 0.01). In muscle, C15:0 (P = 0.03) was linearly increased by Cu. Dietary Cu supplementation did not influence oxidative stability in goat muscle or s.c. adipose. Copper supplementation at 200 mg/d resulted in a significant increase in malondialdehyde in mesenteric adipose (P = 0.01) compared with the 0 or 100 mg/d groups. These results indicate that lipid composition may differ from depot to depot and that depending on the depot, dietary Cu seems to elicit a variable response on the fatty acid composition.
Key Words: copper • diet • goat • lipid
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INTRODUCTION
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A required trace mineral for ruminant species (Becker et al., 1931
; Underwood and Suttle, 1999), Cu forms part of a number of enzymes called cupro-enzymes. Widely used as a defaunating and growth-promoting agent, Cu may also alter lipid metabolism in animals (Pesti and Bakalli, 1996; Engle et al., 2000a,b; Hill et al., 2000). Animal studies indicate that dietary Cu may alter the fatty acid profiles in various tissues (Ho and Elliot, 1974; Dove, 1993; Morales et al., 2000). Long-term Cu supplementation to diets marginal in Cu decreased backfat depth and increased LM area in steers (Ward and Spears, 1997). Supplementation of Cu at 10 to 40 mg of Cu/kg of DM decreased backfat and increased the concentration of unsaturated fatty acids in the LM of finishing steers (Engle et al., 1999). In beef cattle, dietary Cu supplementation modulated the fatty acid composition of the LM by increasing the concentration of PUFA (Engle et al., 2000a,b).
Expression of as many as 12 genes involved in lipid, fatty acid, and sterol metabolism may be affected by dietary Cu (Svensson et al., 2003). More specifically, dietary Cu increased the expression of genes involved in low-density lipoprotein uptake and de novo cholesterol biosynthesis, which is consistent with data obtained from other animal studies (Engle et al., 2000b; Morales et al., 2000). However, in a study conducted with steers, supplemental Cu had no detectable effect on lipid or cholesterol metabolism (Engle and Spears, 2001), and data in goats showed a quadratic response in carcass lipid content with increasing levels of Cu (Solaiman et al., 2006). Limited data is available on the effect of dietary Cu on lipid content of goat carcasses. The objective of this research was to determine the effect of different levels of dietary Cu supplementation on the fatty acid profiles and the oxidative stability in the LM, the mesenteric adipose (MA) depot, and the s.c. adipose (SA) depot of Boer x Spanish goat kids.
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MATERIALS AND METHODS
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Animals
All animal procedures described herein were approved by both the Auburn University and Tuskegee University Animal Care and Use Committees.
In this experiment, 15 Boer x Spanish goat kids (average BW 21.3 ± 0.7 kg and age 4 to 5 mo) were utilized. On arrival, and 2 wk into the experiment, all animals were dewormed with Cydectin (moxidectin; Fort Dodge Animal Health, Fort Dodge, IA), vaccinated with Clostridium perfringens type C and D-Tetani Bacterin-Toxoid (Bayer Corp., Animal Health, Shawnee Mission, KS), and dusted for external parasites with CoRal 1% dust (Dale Alley Co., St. Joseph, MO). The animals were castrated and injected with Liquamycin LA-200 (Pfizer Animal Health, Exton, PA) by a licensed veterinarian. Gradual adjustment to the 70:30 grain:hay diet took place over the 30-d quarantine period, at which time the experimental treatments were begun. The animals were housed at Tuskegee University, and the slaughter and sampling were done at Auburn University.
Diets
All animals received a commercial pellet (Nutrena Feed Division, Minneapolis, MN) and 30% bahiagrass hay (chopped to 4 to 5 cm in length) on a DM basis (Table 1). Copper sulfate pentahydrate (CuSO4.5H2O) was supplemented at 0, 100, or 200 mg/d of Cu in porcine gelatin capsules (Torpac #13, Torpac Inc., Fairfield, NJ). Supplemental Cu was administered with a balling gun once a day before the morning feeding. Control goats received an empty gelatin capsule as a placebo.
The amount of feed offered was determined based on the NRC (1981) recommendations to assure adequate protein and energy intake for maintenance, 150 g/d of BW gain, and a 10% refusal. Fresh grain and hay were available ad libitum. Daily feed intakes were recorded by measuring feed offered minus feed refused. Refusals (grain plus hay) were collected daily before feeding (0800), and feed offered was adjusted weekly. When the feed refusal was more than 10%, the feed offered was decreased, and when the feed refusal was less than 5%, the feed offered was increased. Animals had ad libitum access to water throughout the study (except during BW measurements). The water contained 0.7 ppm Zn; other minerals were undetectable.
Experimental Design
A completely randomized design was used, in which animals were assigned to 1 of 3 experimental treatments. Animals were housed in individual raised mesh floor-type pens, measuring 1.8 x 2.1 m. The experiment consisted of a 2-wk adjustment period, which followed the 30-d quarantine, followed by 10 wk of performance measurement. Animals continued on supplemental Cu until slaughter at 14 wk after initiation of the supplemental Cu intake. General health parameters were observed daily, including feed intake, general behavior, diarrhea, and signs of respiratory illness. Body weights were obtained every 2 wk on 2 consecutive days. Body weight was recorded after 4 h of feed and water restriction.
Collection of Tissues
On the day of slaughter, tissue samples from LM, MA, and SA were collected immediately after stunning of the animal, followed by exsanguination, and flash-frozen in liquid N. These samples were then placed on dry ice and transported to a –80°C freezer, where they were kept until further processing.
Analytical Procedures
Fatty Acid Isolation and Derivation of Methyl Esters.
The LM was dissected, and any visible external fat was removed. Representative subsamples of approximately 2.5 g total were taken for lipid extraction using a 2:1 solution of chloroform:methanol, according to the procedure described by Folch et al. (1957). Both MA and SA tissues were pulverized while frozen using a mortar and pestle, and then representative subsamples of approximately 0.1 g total were taken for lipid extraction using the chloroform:methanol solution, as described for muscle. The lipid fraction was dried under N2, and fatty acid methyl ester derivatives were prepared by methylation of the fatty acids using the trifluoroboride (Sigma, St. Louis, MO) method described by Morrison and Smith (1964).
Gas Chromatography-Mass Spectrometry.
Gas chromatography was carried out with a Hewlett Packard 5890 gas chromatograph equipped with a mass spectrometry mass detector, using a high-polarity Heliflex AT-silar capillary column (30 m x 0.32 mm i.d. x 0.25 µm) with a stationary phase of 5% phenyl:95% methylpolysiloxane (Alltech Associates Inc., Deerfield, IL). The temperature was held at 50°C for 2 min, then increased from 50 to 180°C at 10°C/min, and then increased from 180 to 240°C at 5°C/min. The temperature of the injector and detector were maintained at 250 and 180°C, respectively. The carrier gas was He (40 cm/s), and the split ratio was 1:50. Mass spectrometry was performed on a MicroMass mass spectrometer connected to a Mass-Lynx data system (Water’s Corp., Milford, MA). Electron ionization mass spectra were recorded at an ionization energy of 70 eV. Peak detection and area integration were achieved by using the Mass-Lynx software equipped with the Sowitzki-Golay integration (Water’s Corp.).
Fatty acid identification was obtained through comparing the linear retention time and mass spectra at the apex of a particular peak to those of the standards and confirmed by using the NIST mass spectra library version 2.0 (NIST, 2005). Mixtures of fatty acid methyl esters (Alltech Associates Inc.) were used as standards. The standards were chosen as suitable for mass spectrometry but contained an incomplete range of positional isomers for C18:2 fatty acids.
Thiobarbituric Acid Determination.
Malondialdehyde (MDA), a secondary oxidation product of thiobarbituric acid, was measured according to the method described by Grau et al. (2000) and modified by Galobart et al. (2001) using third derivative spectrophotometry with some modifications. A 1.5-g sample (in duplicate) of frozen tissue was pulverized with a stainless steel mortar and pestle and then weighed into a 25-mL screw-capped centrifuge tube, and 5 mL of 0.8% butylated hydroxytoluene in hexane was immediately added. Before homogenization, 8 mL of 5% aqueous trichloroacetic acid was added to the tube. The mixture was mixed for 40 s, the top hexane layer was discarded, and the bottom aqueous layer was filtered through filter paper (Fisher brand No. 1, Fisher Scientific, Suwanee, GA). The volume was increased to 10 mL with 5% trichloroacetic acid. After filtration, 2 x 3 mL aliquots were transferred to another tube and mixed with 2 mL of 0.8% thiobarbituric acid. The mixture was incubated at 70°C in a water bath under gentle agitation for 30 min, after which it was cooled in an ice bath for 7 min. After the tube was tempered for 45 min at room temperature, the reaction mixture was used for third-order derivative spectrophotometry. Tetraethoxypropane (Sigma) was used as the MDA precursor in the standard curve. The height of the third-order derivative peak that appeared at approximately 521.5 nm was used for calculation of the MDA concentration in the examined extract on the basis of slope and intercept data of the computed least squares fit of a freshly prepared standard curve.
Statistical Analyses
The experiment was a completely randomized design with goat as the experimental unit and Cu intake as the treatment. The data were analyzed by 1-way ANOVA using the GLM procedure (SAS Inst. Inc., Cary, NC). Treatment means were compared using linear and quadratic orthogonal contrasts. The significance level was established at P < 0.05. The model was as follows: Y =µ+ C + 
, where µ= the overall mean; C = the effect due to Cu intake; and = the error term.
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RESULTS
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This experiment was part of a study examining the effects of dietary Cu supplementation to Boer x Spanish goat kids. Results from the other 2 parts of this study include production data (Hopkins, 2002) and data on rumen fermentation (Craig, 2003).
Fifteen positively identifiable fatty acids were detected (Table 2) in the LM samples. No changes (P > 0.1) in the fatty acid composition were detected across treatments with the exception of C15:0, pentadecanoic acid, which increased (P = 0.03) linearly with increasing dietary Cu. The unidentified fatty acid isomers ranged from 8.33 to 11.01% of the mass of detected fatty acids across treatments.
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Table 2. The effect of dietary Cu on the fatty acid composition (mass percentage) of LM of Boer x Spanish goat kids
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Fifteen positively identifiable fatty acids (Table 3) were detected in SA samples. There was a linear decrease in percentage for both C14:0 (P = 0.03) and C16:0 (P = 0.01) with increasing Cu in the diet. A quadratic trend was observed for C17:0, with the greatest concentrations observed in goats given 100 mg of Cu/d (P = 0.09). Unidentified isomers of fatty acids ranged from 9.37 to 16.84% of the mass of detected fatty acids across treatments.
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Table 3. The effect of dietary Cu on the fatty acid composition (mass percentage) in the s.c. adipose tissue of Boer x Spanish goat kids
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Sixteen positively identifiable fatty acids (Table 4) were detected in MA samples. No differences (P > 0.05) in percentage were detected among treatments for the known FA. Unidentified isomers of fatty acids ranged from 4.24 to 9.19% of the mass of detected fatty acids across treatments.
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Table 4. The effect of dietary Cu on the fatty acid composition (mass percentage) in mesenteric adipose tissue of Boer x Spanish goat kids
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There was no effect (P > 0.05) of high dietary Cu on the oxidative stability of both LM and SA tissue (Table 5). However, increasing dietary Cu resulted in a linear increase in the formation of MDA in the MA tissue (P = 0.01).
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Table 5. The effect of dietary Cu on the oxidative stability of goat tissue measured as thiobarbituric acid reactive substances (ng of malondialdehyde/g of tissue)
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DISCUSSION
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The objectives of this study were to examine the effects of different levels of dietary Cu supplementation on the fatty acid composition and oxidative stability of muscle and adipose tissues from Boer x Spanish goat kids. The effect of Cu varied with tissue examined.
In LM, there was an increase in C15:0 with increasing dietary Cu (P = 0.03). Although C15:0 was not reported in steers (Engle and Spears, 2001), C15:0 has previously been detected in goat LM (Banskalieva et al., 2000). The isomers of pentadecanoic acid (C15:0) comprise a large proportion of rumen microbial fatty acids, and distinct differences in the pattern of the branch-chain C15:0 isomers are inherent to dietary components fermented (Vlaeminck et al., 2004). Increasing dietary Cu may change the proportions of different classes of microbes leaving the rumen, which may elicit differences in the microbial fatty acid profiles.
Dietary Cu supplementation altered the fatty acid composition of SA, decreasing C14:0 (P = 0.03) and C16:0 (P = 0.01) with increasing dietary Cu. These fatty acids can be viewed as markers for lipogenesis (Murray et al., 1996). In SA, high dietary Cu supplementation may decrease de novo fatty acid synthesis. This is in agreement with results from gene-expression studies. In intact rats, Cu deficiency increased hepatic fatty acid synthetase mRNA (Wilson et al., 1997), and in studies with poultry livers, high levels of dietary Cu (180 mg/kg DM diet) decreased fatty acid synthetase activity (Konjufca et al., 1997).
There were no changes in identifiable fatty acids with increasing dietary Cu in MA. Conjugated linoleic acid refers to a class of positional and geometric conjugated diene isomers of linoleic acid that elicit a variety of physiological effects (Pariza et al., 2000). All known isomers of linoleic acid appear to be produced via the biohydrogenation pathway in the rumen (Wallace et al., 2007). Under certain dietary conditions in the rumen, the conversion of cis-9, cis-12 C18:2 to trans-11 C18:1 and subsequently to stearic acid (C18:0) can occur. During this process, the cis-9, trans-11 and trans-10, cis-12 CLA isomers are produced to various extents. The trans-10, cis-12 CLA isomer has been shown to be a causative factor in bovine milk fat depression (Bauman and Griinari, 2003). Research in goats confirmed the presence of CLA in MA but did not list the specific isomers encountered (Banskalieva et al., 2000). Engle et al. (2001) demonstrated that Cu supplementation in dairy cows at 10 or 40 mg of Cu/kg of DM decreased the C18 dienes and the cis isomers of C18:1 in milk in a linear fashion. It appears that dietary Cu elicits a variable response in fatty acid synthesis and deposition, depending on the specific tissue. Differences in gene expression and metabolism that may affect these observed differences await further studies.
Traditionally, adipose tissue was seen only as a depot for energy storage. However, recent discoveries on the physiological effects of specific fatty acids and their isomers indicates lipid may be involved in a much more intricate molecular regulatory system than was originally recognized (Pariza et al., 2000; Arab, 2003). In addition, ruminant adipose tissues are the primary site of de novo fatty acid synthesis (Bergen and Mersmann, 2005), and a role of adipose tissues in endocrine functions is increasingly recognized (Ronti et al., 2006). Therefore, the idea of examining minor fatty acids has some merit. A total of 77, 68, and 45 peaks were observed above the noise line in MA, SA, and LM, respectively (data not shown). In MA, the fatty acid methyl esters used as standards only represented about 94% (mass basis) of the total compounds detected. For SA, the standards represented 88% of lipids detected and 91% in LM. Statistical analysis of the unidentified peaks, assuming peaks with the same retention time and mass were the same in different samples, indicated differences (P < 0.05) with dietary Cu supplementation for 1 unknown in SA and 8 in MA (data not shown). None of the unidentified peaks were observed to be statistically different due to dietary Cu treatment (all P > 0.1) in LM. Other studies have primarily reported data related to the major compounds (Banskalieva et al., 2000; Morales et al., 2000; Engle et al., 2001), and occasionally, unknown peaks that fell outside the scope of the predetermined standards have been mentioned (Engle and Spears, 2001). The lack of data on fatty acid composition of ruminant tissue for minor fatty acid constituents, and from goats in particular, makes it very difficult to compare these results to those of others. However, the results obtained indicate that fatty acids present in small amounts in tissue can be altered by dietary Cu supplementation. These fatty acids cannot be positively identified due to a lack of standards, but their presence indicates that the analysis of adipose tissue fatty acid composition solely by GLC without the use of mass spectrophotometry does not identify all the changes resulting from the dietary treatment.
Dietary Cu did not elicit a difference in the oxidative stability of goat muscle or s.c. adipose. The absolute values of MDA detected in MA were lower than those detected in LM and SA. However, results from this study demonstrate that dietary Cu supplementation significantly decreased (P = 0.01) the oxidative stability in MA. Previous studies conducted with cooked broiler leg meat showed reduced oxidation values upon removal of Cu from the diet (Ruiz et al., 2000). Depending on depot, Cu may elicit a variable response on the oxidative stability of goat tissue.
Only 3 identified fatty acids were significantly affected by dietary Cu supplementation. Only C15:0 was increased, and C14:0 and C16:0 were decreased. Supplementation of dietary Cu in goats resulted in a significant decrease in the oxidative stability of MA tissue, but not in other tissues examined. In addition, there were several putative lipids in 2 of the tissues examined that were altered by dietary Cu supplementation that were not positively identified. These compounds generally accounted for less than 5% of the lipid in each tissue. Dietary Cu supplementation appears to have variable effects on de novo fatty acid synthesis and lipid deposition in adipose of different tissues.
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Footnotes
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1 Supported by the Alabama Agricultural Experiment Station and Upchurch Fund for Excellence, Department of Animal Sciences. 
2 Corresponding author: cummika{at}auburn.edu
Received for publication October 6, 2006.
Accepted for publication November 6, 2007.
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Abstract
INTRODUCTION
