J. Anim Sci. 2008. 86:173-179. doi:10.2527/jas.2006-814
© 2008 American Society of Animal Science
Bioavailability of copper from copper glycinate in steers fed high dietary sulfur and molybdenum1,2
S. L. Hansen*,
P. Schlegel
,
L. R. Legleiter*,
K. E. Lloyd* and
J. W. Spears*,3
* Department of Animal Science, North Carolina State University, Raleigh 27695; and
Pancosma, S.A., Geneva, Switzerland
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Abstract
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Sixty Angus (n = 29) and Angus-Sim-mental cross (n = 31) steers, averaging 9 mo of age and 277 kg of initial BW, were used in a 148-d study to determine the bioavailability of copper glycinate (CuGly) relative to feed-grade copper sulfate (CuSO4) when supplemented to diets high in S and Mo. Steers were blocked by weight within breed and randomly assigned to 1 of 5 treatments: 1) control (no supplemental Cu), 2) 5 mg of Cu/kg of DM from CuSO4, 3) 10 mg of Cu/kg of DM from CuSO4, 4) 5 mg of Cu/kg of DM from CuGly, and 5) 10 mg of Cu/kg of DM from CuGly. Steers were individually fed a corn silage-based diet (analyzed 8.2 mg of Cu/kg of DM), and supplemented with 2 mg of Mo/kg of diet DM and 0.15% S for 120 d (phase 1). Steers were then supplemented with 6 mg of Mo/kg of diet DM and 0.15% S for an additional 28 d (phase 2). Average daily gain and G:F were improved by Cu supplementation regardless of source (P = 0.01). Final ceruloplasmin, plasma Cu, and liver Cu values were greater (P < 0.05) in steers fed supplemental Cu compared with controls. Plasma Cu, liver Cu, and ceruloplasmin values were greater (P < 0.05) in steers supplemented with 10 mg of Cu/kg of DM vs. those supplemented with 5 mg of Cu/kg of DM. Based on multiple linear regression of final plasma Cu, liver Cu, and ceruloplasmin values on dietary Cu intake in phase 1 (2 mg of Mo/kg of DM), bioavailability of Cu from CuGly relative to CuSO4 (100%) was 140 (P = 0.10), 131 (P = 0.12), and 140% (P = 0.01), respectively. Relative bio-availability of Cu from CuGly was greater than from CuSO4 (P = 0.01; 144, 150, and 157%, based on plasma Cu, liver Cu, and ceruloplasmin, respectively) after supplementation of 6 mg of Mo/kg of DM for 28 d. Results of this study suggest that Cu from CuGly may be more available than CuSO4 when supplemented to diets high in S and Mo.
Key Words: bioavailability • cattle • copper glycinate • copper sulfate • growth
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INTRODUCTION
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As an essential component of several enzymes, Cu functions in numerous physiological processes (Underwood and Suttle, 1999
). Deficiencies in Cu are found around the world, and low Cu incorporation into enzymes may cause Cu deficiency signs such as retarded growth and hair depigmentation (NRC, 1996). Bioavailability of Cu from ruminant diets is depressed by the presence of antagonists such as Mo, S, and Fe (Spears, 2003). Formation of ruminal thiomolybdates in the presence of high dietary Mo and S can impair not only absorption but also systemic metabolism of Cu (Underwood and Suttle, 1999). Considerable research has focused on identification of Cu sources that are more bioavailable in the presence of Cu antagonists. Certain organic Cu sources that are complexed or chelated to various ligands may be more bioavailable to cattle than traditionally fed inorganic Cu sulfate (CuSO4). Copper lysine (Ward et al., 1993; Pott et al., 1994; Rabiansky et al., 1999) and Cu proteinate (Kincaid et al., 1986; Wittenberg et al., 1990; Ward et al., 1996) have been evaluated in a number of studies with ruminants. Results obtained with these organic sources have been variable, with some studies indicating greater Cu bioavailability and others finding similar bioavailability, relative to CuSO4. Copper glycinate is a chelated Cu source which, to our knowledge, has not been evaluated as a source of dietary Cu for cattle.
The current study was conducted to determine the bioavailability of copper glycinate (CuGly) relative to CuSO4 in steers fed diets high in Mo and S. The CuGly used in this present study was an organic form of Cu bound to the amino acid glycine in a crystalline form with the following chemical formula: [Cu(C2H5- NO2)(H2O)2(SO4)]n.
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MATERIALS AND METHODS
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Animals and Experimental Design
Experimental procedures were reviewed and approved by the North Carolina State University Animal Care and Use Committee.
Sixty Angus (n = 29) and Angus x Simmental (n = 31) steers, approximately 9 mo of age and 277 ± 6.8 kg of initial BW, were used in this study. Before initiation of the study, steers were vaccinated for infectious bovine rhinotracheitis, bovine viral diarrhea (I and II), parainfluenza-3, bovine respiratory syncytial virus (Titanium 5, AgriLabs, St. Joseph, MO) and Clostridial organisms (Vision 7, Intervet, Millsboro, DE). Steers were also treated for internal and external parasites (Bovimec, Virbac, Fort Worth, TX). Steers were housed in a covered facility with slatted floors, and individually fed via electronic feeders (American Calan, Northwood, NH). Steers were stratified by BW within a breed, placed in 1 of 5 pens, and randomly assigned to treatments within pen.
Treatments consisted of: 1) control (no supplemental Cu), 2) 5 mg of Cu/kg of DM from CuSO4, 3) 10 mg of Cu/kg of DM from CuSO4, 4) 5 mg of Cu/kg of DM from CuGly, or 5) 10 mg of Cu/kg of DM from CuGly. The CuSO4 · 5H2O originated from Eastern Minerals (Henderson, NC) and the CuGly {chemical formula: [Cu(C2H5NO2)(H2O)2(SO4)]n; B-TRAXIM 2C} originated from Pancosma S.A. (Le Grand-Saconnex, Geneva, Switzerland). Steers were fed a corn silage-based diet (analyzed at 8.2 mg of Cu/kg of DM), supplemented with 2 mg of Mo/kg of DM and 0.15% S for 120 d (phase 1). To further challenge the bioavailability of the CuGly in the presence of antagonists, supplemental Mo was increased to 6 mg of Mo/kg of DM for an additional 28 d at the end of phase 1 (phase 2). Diets were formulated to meet or exceed all NRC requirements (1996), with the exception of Cu. Ingredient and chemical composition of the control diet is shown in Table 1. Concentrations of supplemental Cu, based on laboratory analysis, are presented in Table 2. Steers were fed once daily, with feed amounts based on what they would consume in a 24-h period. Initial and final BW for the 148-d study were the average of BW measured on 2 consecutive days. Interim steer BW were recorded at 28-d intervals. Jugular blood samples were collected 2 h postfeeding on d 0, 28, 56, 84, 112, and 148 for analysis of plasma Cu and ceruloplasmin. Liver biopsy samples were obtained, as described by Engle and Spears (2000), on d 0, 117, and 148 for Cu determination.
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Table 2. Supplemental dietary Cu concentrations based on analysis of corn supplements that provided Cu treatments to steers fed diets high in Mo and S
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Analytical Procedures
Blood was collected in heparinized vacuum tubes designed for trace mineral analysis (Becton Dickinson, Rutherford, NJ), transferred on ice to the laboratory, and centrifuged at 1,200 x g for 20 min at 20 ° C. Plasma was removed and immediately analyzed for ceruloplasmin activity and then stored at – 20 ° C until analyzed for Cu concentration. Ceruloplasmin activity of fresh plasma was determined as described by Houchin (1958) using a spectrophotometer (Spectronic 1001, Bausch and Lomb, Rochester, NY). Before analysis for Cu, plasma samples were prepared by diluting 1:3 (vol/vol) with 5% nitric acid and centrifuging for 20 min at 1,200 x g at 25 ° C. Feed and liver samples were prepared for Cu analysis by wet ashing using microwave digestion (Mars 5, CEM Corp., Matthews, NC) as described by Gengelbach et al. (1994). Copper content of plasma, feed, and liver samples was determined by flame atomic absorption spectroscopy (Shimadzu Scientific Instruments, Kyoto, Japan).
Statistical Analysis
Statistical analysis of performance data was performed by ANOVA for a completely randomized design using the GLM procedure (SAS Inst. Inc, Cary, NC). Liver Cu, plasma Cu, and ceruloplasmin data were analyzed as repeated measures with individual animals serving as the experimental unit. Covariate analyses using d 0 values were performed on liver and plasma Cu data. The model included the fixed effects of breed, treatment, time, and all related interactions. When a treatment x time interaction was observed, data were analyzed by sampling day. Interactions that were not significant (P 
0.05) for the measurement of interest were removed from the model. When treatment was significant (P < 0.10), differences among means were separated using single df orthogonal contrasts. The comparisons made included: control vs. supplemental Cu, 5 mg of Cu/kg of DM vs. 10 mg of Cu/kg of DM, 5 mg of Cu/kg of DM from CuGly vs. 5 mg of Cu/kg of DM from CuSO4, and 10 mg of Cu/kg of DM from CuGly vs. 10 mg of Cu/kg of DM from CuSO4. Relative bioavailability of CuGly was determined, using CuSO4 as the standard source, by means of multiple linear regression and the slope-ratio method. Dependent variables (plasma Cu, plasma ce-ruloplasmin, and liver Cu) were regressed on total supplemental Cu intake for the 120-d period (phase 1) or 148-d period (phase 2). Liver Cu data were log10 transformed to account for heterogeneity of variances. As suggested by Littell et al. (1997), assumptions for the slope-ratio assay were checked for validity. Regressions using plasma Cu data required the addition of an X0 indicator variable to the model statement to meet the requirement for equality of intercepts for each Cu source. Regressions using liver Cu and ceruloplasmin data met assumptions for the slope-ratio assay procedure and did not require adjustment factors.
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RESULTS AND DISCUSSION
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Initial liver Cu concentrations averaged 255 mg of Cu/kg of DM and were similar among treatments (Table 3). Liver Cu concentrations had decreased (P < 0.01) greatly in all treatment groups by d 117. The dramatic decrease in liver Cu following Mo supplementation is consistent with previous studies (Humphries et al., 1983; Ward et al., 1996). Liver Cu concentrations were lower (P < 0.01) in controls compared with Cu-supplemented steers on d 117 and 148. Steers supplemented with 10 mg of Cu/kg of DM also had greater (P < 0.01) liver Cu concentrations than those supplemented with 5 mg of Cu/kg of DM on d 117 and 148. Liver Cu values of 25 mg/kg of DM or less may be indicative of a marginal deficiency (Wikse et al., 1992). Control steers as well as those receiving 5 mg of supplemental Cu/kg of DM had liver Cu values below this level by d 117. Increasing supplemental Mo from 2 to 6 mg/kg of DM for 28 d did not significantly reduce liver Cu concentrations compared with values observed on d 117. Copper stored in the liver is believed to be bound primarily to metallothionein (Bremner, 1987). This pool of liver Cu can decrease greatly when intestinal absorption of Cu is inadequate, as observed in the current study as well as previous studies. However, once liver Cu concentrations reach relatively low concentrations, a greater percentage of liver Cu is present in cuproenzymes, and this fraction of liver Cu decreases at a much slower rate even during prolonged periods of Cu deficiency (Ward and Spears, 1997). Source of Cu did not significantly affect liver Cu.
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Table 3. Effect of Cu level (from copper sulfate of copper glycinate) on Cu indices in steers fed diets high in Mo and S1
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Plasma Cu was affected by time and by a time x treatment interaction (P < 0.01; Table 3
). Copper source did not significantly affect plasma Cu concentrations. Dietary Cu did not affect plasma Cu concentrations on d 28. By d 56 (P < 0.05) and at subsequent sampling dates (P < 0.01), plasma Cu was lower in controls compared with Cu-supplemented steers. Steers supplemented with 10 mg of Cu/kg of DM had greater (P < 0.01) plasma Cu levels than those fed 5 mg of Cu/kg of DM on d 148, but not at the earlier sampling dates. It has been previously demonstrated that supplementation of Mo to a diet low in Cu causes a reduction in plasma Cu (Wittenberg et al., 1990; Ward et al., 1996). Plasma Cu values for steers fed the control diet were below 0.5 mg/L by d 84 of the study, suggesting that steers were at least marginally deficient in Cu by this time (Underwood and Suttle, 1999). The addition of either 5 or 10 mg of Cu/kg of DM prevented marginal Cu deficiency, based on plasma Cu concentrations. Plasma Cu concentrations reflect intestinal absorption of Cu as well as mobilization of stored Cu from the liver. These results suggest that absorption of Cu in steers supplemented with 5 mg of Cu/kg of DM was sufficient to maintain plasma Cu concentrations in the normal range, despite liver Cu concentrations by d 117 that probably allowed minimal release of stored Cu into the blood. Claypool et al. (1975) found no correlation between plasma and liver Cu concentrations in cattle with liver Cu concentrations above 40 mg of Cu/kg of DM. However, liver Cu concentrations below 40 mg of Cu/kg of DM were associated with plasma Cu concentrations below 0.5 mg/L in this study (Claypool et al., 1975), indicating that liver stores were inadequate to maintain normal plasma Cu values.
Ceruloplasmin is a copper metalloprotein that contains a large percentage of the Cu found in plasma. Plasma ceruloplasmin activity was consistent with the pattern displayed by plasma Cu during the course of the study, and was affected by a time x treatment interaction (P < 0.01). Ceruloplasmin activity values from d 56 through the end of the study (d 148) were lower (P < 0.01) in control steers than in those supplemented with Cu (Table 3). Final ceruloplasmin activity values were greater (P < 0.01) in steers supplemented with 10 mg of Cu/kg of DM compared with those supplemented with 5 mg of Cu/kg of DM. Steers supplemented with 10 mg of Cu/kg of DM from CuGly had greater (P < 0.05; 19.0 vs. 14.6 mg/L) ceruloplasmin activity on d 148 than steers fed a similar concentration of Cu from CuSO4.
Bioavailability of CuGly relative to CuSO4 was estimated from plasma Cu, ceruloplasmin, and liver Cu concentrations measured at the end of the 2 phases of Mo supplementation by means of multiple linear regression and the slope-ratio method. Dependent variables were regressed on total supplemental Cu intake for the 120-d period (phase 1) or 148-d period (phase 2). Based on laboratory analysis of diets, steers receiving 5 and 10 mg of Cu/kg of DM from CuSO4 consumed an average of 46.8 and 107.1 mg of supplemental Cu/d, respectively. Those steers receiving supplemental Cu from CuGly at a level of 5 and 10 mg of Cu/kg of DM consumed an average of 47.1 and 89.8 mg of supplemental Cu/d, respectively. Slopes and estimated relative bioavailability of Cu are reported in Table 4. Compared with CuSO4 (100%) at the end of phase 1, relative bioavailability of Cu from CuGly was 140 (P = 0.10), 140 (P = 0.01), and 131% (P = 0.12), based on slope ratios for plasma Cu, plasma ceruloplasmin, and liver Cu, respectively. Following the 28-d period of increased Mo supplementation (phase 2; 6 mg of Mo/kg of DM) slopes further separated and bioavailability was greater (P < 0.01) from CuGly when compared with CuSO4. Bioavailability of Cu from CuGly relative to CuSO4 at the end of phase 2 was 144, 157, and 150%, based on plasma Cu, ceruloplasmin, and liver Cu, respectively (Figures 1 and 2). Although the slopes differed between Cu sources, the linear regression lines (Figures 1 and 2) suggest that the differences in slope could at least partially be accounted for by greater predicted Cu intakes for steers fed 10 mg of Cu/kg of DM from CuSO4 than for those fed 10 mg of Cu/kg of DM from CuGly. Despite this concern, the data suggest that Cu from CuGly may be more bioavailable to cattle fed diets high in Mo and S compared with CuSO4.
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Table 4. Estimated relative bioavailability of Cu sources in steers fed diets high in Mo and S, based on multiple linear regression of Cu indices on total supplemental Cu intake (g)1
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Figure 1. Relative bioavailability of copper glycinate (CuGly) vs. copper sulfate (CuSul) as determined by multiple linear regression of phase 2 liver Cu concentrations on total supplemental intake of Cu (g). The data represented are log transformed and adjusted for initial liver Cu values.
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Figure 2. Relative bioavailability of copper glycinate (CuGly) vs. copper sulfate (CuSul) as determined by multiple linear regression of phase 2 plasma Cu on total supplemental intake of Cu (g). Represented data are adjusted for d 0 values and forced through a common intercept in order to meet validity requirements for the regression analysis.
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High dietary concentrations of Mo and S reduce Cu bioavailability in ruminants. In the rumen, molybdate can react with sulfide produced by ruminal microorganisms, resulting in the formation of thiomolybdates (Suttle, 1991). Thiomolybdates can form insoluble complexes with Cu, resulting in reduced Cu absorption. Independent of dietary Mo, S can decrease Cu absorption, possibly via the formation of insoluble Cu sulfide in the rumen (Spears, 2003). Organically bound Cu sources may prevent or at least reduce the adverse effects of antagonists such as Mo and S on Cu absorption. The data indicate that the CuGly source used in this study is more bioavailable than CuSO4 in cattle fed diets high in Mo and S. Results obtained in previous studies comparing the bioavailability of organic Cu sources to inorganic CuSO4 have been highly variable. Ward et al. (1993) found that bioavailability of Cu from CuSO4 and Cu lysine was similar in steers fed high dietary Mo and S. Similarly, Rabiansky et al. (1999) reported comparable results between CuSO4 and Cu lysine when fed to heifers. However, apparent absorption and retention of Cu was greater in steers fed Cu lysine compared with those given CuSO4 following stress, induced by ACTH administration and feed and water restriction (Nockels et al., 1993). Steers supplemented with 20 mg of Cu/kg of DM from a Cu AA complex had greater plasma and liver Cu concentrations than steers given a similar concentration of Cu from CuSO4 (Dorton et al., 2003). However, differences in liver and plasma Cu concentrations were not demonstrated when these 2 Cu sources were supplemented at 10 mg of Cu/kg of DM (Dorton et al., 2003). In cattle fed diets high in Mo, Cu proteinate was more bioavailable than CuSO4 in some studies (Kincaid et al., 1986; Ward et al., 1996) but not in others (Wittenberg et al., 1990).
Copper supplementation, regardless of source and concentration, improved (P < 0.01) ADG and G:F of steers compared with controls (Table 5). Spears et al. (2004) also found that Cu supplementation to a control diet high in Mo and S increased gain and G:F in growing steers. In the current study, DMI also tended (P = 0.09) to be greater in Cu-supplemented steers compared with control steers. Performance of steers did not differ (P > 0.05) among those supplemented with 5 or 10 mg of supplemental Cu/kg of DM, despite the differences observed in Cu status of the steers.
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Table 5. Effect of source and level of supplemental Cu (from copper sulfate or copper glycinate) on growth characteristics of steers fed diets high in Mo and S1
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In summary, Cu from the CuGly complex tended to be more bioavailable than CuSO4 when fed to steers receiving diets supplemented with 2 mg of Mo/kg of DM. When supplemental Mo was increased from 2 to 6 mg of Mo/kg of DM, bioavailability of Cu was greater from CuGly than from CuSO4.
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Footnotes
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1 Use of trade names in this publication does not imply endorsement by the North Carolina Agric. Research Service or criticism of similar products not mentioned. 
2 Appreciation is extended to G. Shaeffer, J. Dickerson, and J. Woodlief for their assistance in sampling and animal care.
3 Corresponding author: Jerry_Spears{at}ncsu.edu
Received for publication December 13, 2006.
Accepted for publication September 26, 2007.
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LITERATURE CITED
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Ward, J. D., J. W. Spears, and E. B. Kegley. 1993. Effect of copper level and source (copper lysine vs. copper sulfate) on copper status, performance, and immune response in growing steers fed diets with or without supplemental molybdenum and sulfur. J. Anim. Sci. 71:2748–2755.[Abstract]
Ward, J. D., J. W. Spears, and E. B. Kegley. 1996. Bioavailability of copper proteinate and copper carbonate relative to copper sulfate in cattle. J. Dairy Sci. 79:127–132.[Abstract]
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Abstract
INTRODUCTION
