J. Anim Sci. 2008. 86:2971-2978. doi:10.2527/jas.2008-0888
© 2008 American Society of Animal Science
Effect of chromium source on tissue concentration of chromium in pigs1,2
M. D. Lindemann*,3,
G. L. Cromwell*,
H. J. Monegue* and
K. W. Purser
,4
* University of Kentucky, Lexington 40546; and
Prince Agri Products Inc., Quincy, IL 62306
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Abstract
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The concentration of Cr in several tissues in response to high-level, short-term supplementation was used to determine the relative bioavailability among 4 organic Cr sources and to assess the relative safety of high levels of supplementation. Crossbred pigs (n = 40; mean BW = 48.1 ± 0.9 kg) were allotted to 5 diets: a control diet with no added Cr, or 5,000 µg/kg of Cr from Cr tripicolinate (CrTP), Cr propionate (CrPrp), Cr methionine (CrMet), or Cr yeast (CrY). Twenty gilts were housed individually and barrows were housed in pairs. Average duration of feeding before slaughter was 75 d. For the total experiment, pigs fed the unsupplemented diet had less ADG than pigs fed CrY (P < 0.05). Serum clinical chemistry values, obtained during the final week of the experiment, demonstrated few effects with no responses that would raise concern about metabolic changes in response to the Cr sources. The effects of the forms of Cr fed on carcass measurements and meat quality were also minimal. All Cr sources reduced cooler shrink (P < 0.05) and most resulted in some meat color change on d 1 postslaughter. For tissue Cr content, 4 of 5 tissues (bone, kidney, liver, and ovary) were increased (P < 0.05) in Cr content by supplementation with CrTP and CrMet, whereas only 2 tissues (bone and kidney) were increased (P < 0.05) by CrY, and none were increased by CrPrp. In all tissues of response, CrTP exceeded CrMet and CrMet exceeded CrY. Comparing the relative increase in tissue Cr for all responsive tissues (bone, kidney, liver, and ovary) gave a range of responses, for which the mean bioavailability relative to CrTP across tissues was 13.1% for CrPrp (0.2 to 19.0%), 50.5% for CrMet (36.2 to 79.1%), and 22.8% for CrY (2.5 to 47.9%). In summation, these results show very clear Cr effects on multiple tissues, which is conclusive evidence of absorption and deposition. The lack of a negative response in growth performance, carcass measures, and clinical chemistry at the increased quantities used herein provides assurance that normal quantities of addition are extremely safe.
Key Words: bioavailability • chromium • pig • tissue
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INTRODUCTION
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General interest in supplemental Cr for pigs began when chromium tripicolinate (CrTP) addition resulted in carcass improvements in finishing pigs (Page et al., 1993
). This was followed by a demonstration of increased litter size in reproducing sows with CrTP supplementation (Lindemann et al., 1995). Much research with many forms of Cr for many species in a variety of situations has followed (Lindemann, 2007).
A variety of organic forms of Cr is now available worldwide. As with all minerals, different forms would be expected to have different bioavailabilities. The relative bioavailability of the different forms will affect the ultimate tissue supply of the mineral and, consequently, will influence both potential biological response(s) and economics of mineral supply. However, measuring the relative bioavailability of trace elements can be difficult because whole-animal responses generally are not responsive enough to allow clear statistical evaluation and interpretation, and discriminating methods of assessment (e.g., using radiolabeled compounds) that might allow clear statistical differentiation among sources are very costly. Another method that has been used with some trace minerals to address this problem is to evaluate tissue concentrations of a mineral in response to high-level, short-term supplementation (Ammerman, 1995).
This study utilized that methodology to evaluate the relative bioavailability of various organic Cr forms by comparing the concentrations of Cr in selected tissues of pigs when fed 5,000 µg/kg of supplemental Cr. The 5,000-µg/kg concentration is 25 times greater than the concentration currently permitted in the United States by the Food and Drug Administration for Cr products available on the market. This serves not only as a useful concentration for this bioavailability research, but also allows assessment of potential safety and toxicity issues.
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MATERIALS AND METHODS
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The experiment was conducted under protocols approved by the Institutional Animal Care and Use Committee of the University of Kentucky.
Crossbred pigs [n = 40; 20 barrows and 20 gilts; Hampshire x (Landrace x Yorkshire)] with a mean BW of 48.1 ± 0.87 kg (range: 42.6 to 54.4 kg) and mean age of 87 d (range: 82 to 90 d) were blocked by sex and BW, and pigs were randomly assigned within block to 1 of 5 dietary treatment groups until slaughter. Gilts were penned singly and barrows as pairs in partly slatted pens that measured 1.2 x 4.3 m. This resulted in 2 replicates of barrows and 4 replicates of gilts. The diets (Table 1) were a control diet with no added Cr (CONT) or that same diet with 5,000 µg/kg of Cr (as-fed basis) from CrTP (Prince Agri Products Inc., Quincy, IL), Cr propionate (CrPrp; Kemin, Des Moines, IA), Cr methionine (CrMet; Zinpro Corp., Eden Prairie, MN), or Cr yeast (CrY; Alltech Inc., Nicholasville, KY). The sources of Cr were digested in HCl/HNO3/H2O and were assayed for Cr and Ca content by inductively coupled plasma (ICP) mass spectrometry (4300 DV ICP-OES, Perkin Elmer, Norwalk, CT) to determine the appropriate inclusion rates. Because some Cr supplements used a limestone carrier, supplements were also analyzed for Ca to make appropriate adjustments in the dietary concentration of Ca. Samples of all diets were taken at the time of mixing. The samples were composited for each diet phase and analyzed for total Cr by the same method used for Cr in the Cr sources. Diets were also analyzed for Mn and Zn by flame atomic absorption spectrophotometry (Thermoelemental, SOLAAR M5, Thermo Electron Corp., Verona, WI) according to a modification of the AOAC procedure (method 927.02; AOAC, 1995). Diets were formulated to meet or exceed all nutrient requirement estimates (NRC, 1998). Pigs had ad libitum access to both feed and water at all times except for the period associated with blood sampling.
Blood sampling for serum clinical chemistry analysis occurred on all pigs during the week of slaughter. Feeders were removed from pens at 1500 h, and fasting blood samples (10 mL) were obtained from the anterior vena cava the next morning between 0700 and 0830 h; time variation among samples within individual replicates was less than 40 min. The collected blood samples were kept on ice for approximately 1 to 2 h, and serum was obtained by centrifugation of the blood at 800 x g and 4°C for 20 min. Serum samples were stored at –20°C until assayed. For examination of the effects of the treatments on carcass measurements and to obtain tissue samples, pigs were electrically stunned and then killed by exsanguination. Carcasses were dehaired, eviscerated, weighed (HCW), split longitudinally, and washed before they were chilled at 1°C for 24 h. Dressing percentage was calculated as HCW divided by slaughter weight. Cold carcass weight was taken before further processing. Cooler shrink was subsequently calculated as the difference between HCW and cold carcass weight divided by HCW and expressed as a percentage. The right side of the carcass was split at the 10th-rib and the LM was traced to determine 10th rib backfat thickness (three-fourths of the distance from the midline to the end of the LM) and LM area (LMA). Carcass length was measured as the distance from first rib to the aitch bone. Subjective measures of color (1 = pale pinkish gray to white; 6 = dark purplish red) were evaluated on the 11th-rib face according to NPB (2000) by a person trained in meat quality evaluation. At slaughter, front feet for metacarpal bones, kidney, liver, LM, and ovary (in gilts) were harvested. Because concentrations of Cr fed were not approved for use in food-producing animals, carcasses of all animals fed supplemental Cr were disposed of as offal.
Meat quality measurements were assessed on LM samples. Objective color was measured using a color meter (Minolta Chroma Meter CR-310, Minolta Co., Ramsey, NJ) with a pulse xenon arc lamp (D65) with a 50-mm aperture size that was calibrated each day using a standard white tile and used to examine CIE L*, a*, and b* color values, where L* values are a measure of lightness (greater value indicates a lighter color); a* values are a measure of redness (greater value indicates a redder color); and b* values are a measure of yellowness (greater value indicates a yellower color). Color measurements were taken immediately after each LM was cut and then repeated after 5 d in a simulated retail display.
Tissue samples were frozen until being shipped to a laboratory (Trace Elements Laboratory, London Health Sciences Centre, London, Ontario, Canada) for Cr analysis. A portion of each tissue (about 0.1 g) was digested in 0.5 mL of concentrated, ultrapure HNO3 at 100°C for 15 min. The digest was then diluted to 10 mL and assayed by ICP (Finnigan Element 1 High Resolution ICP Mass Spectrometer, Bremen, Germany) against aqueous standards. The detection limit for the assayed minerals was 0.0001 µg/g. National Institute of Standards and Technology (Gaithersburg, MD) reference samples for egg powder, bovine muscle, and bovine liver were sent with the tissue samples to validate the assay sensitivity for Cr, Mn, and Zn. The reference values (µg/g; mean ± 95% confidence interval) for Cr, Mn, and Zn were 0.37 ± 0.18, 1.78 ± 0.38, and 67.5 ± 7.6, respectively, for the egg powder, and 0.071 ± 0.038, 0.37 ± 0.09, and 142 ± 14, respectively, for the bovine muscle; for the bovine liver, there was no Cr value listed, and the values for Mn and Zn were 9.9 ± 0.8, and 123 ± 8, respectively. The Cr, Mn, and Zn contents analyzed by the laboratory were 0.348, 1.82, and 77.4, respectively, for the egg powder; 0.077, 0.413, and 132, respectively, for the bovine muscle; and 0.111, 9.4, and 113, respectively, for the bovine liver. Serum samples were analyzed for routine clinical chemistry profiles at the University of Kentucky Clinical Laboratories (Beckman Coulter Synchron LX 20 Pro Chemistry Analyzer, Beckman Coulter Inc., Brea, CA). The LX 20 is a rapid (1,440 tests/h), random access, open reagent chemistry analyzer. The test menu exceeds 80 methods, and the analyzer uses a variety of measurement principles (e.g., spectrophotometric, conductimetric, electrochemical).
The pen served as the experimental unit for statistical analysis. The data were subjected to ANOVA using the GLM procedures (SAS Institute Inc., Cary, NC) as a randomized block design. The model included terms for treatment and block. Treatment means were separated with the PDIFF command and were considered different at P < 0.05.
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RESULTS AND DISCUSSION
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The prestudy analysis of the Cr sources for Cr and Ca, respectively, resulted in the following: CrTP, 410 ppm and 38.3%; CrPrp, 510 ppm and 38.5%; CrMet, 1,040 ppm and 36.3%; and CrY, 1,099 ppm and 0.18%. Analysis of total dietary Cr less that determined in the basal diet yielded a dietary inclusion rate ranging from 92 to 100% of the expected concentration of 5,000 µg/kg for all Cr sources (CrTP, 4,709 ppm; CrPrp, 4,988 ppm; CrMet, 4,695 ppm; and CrY, 4,594 ppm); the basal diet had a mean Cr content of 2,075 ppm. Average duration of feeding for this experiment was 75 d (range: 68 to 82 d for the various BW blocks).
The effect of the high concentration of Cr on growth is presented in Table 2. There were no consistent patterns in the individual period responses. For the total experimental period, pigs fed the unsupplemented diet had numerically less ADG than all Cr treatments, thus providing no indication of negative potential of the Cr sources. For the total period, there was an increase in ADG (P < 0.05) for pigs fed CrY compared with pigs fed the CONT diet. Studies with broilers examining concentrations of 800 µg/kg of Cr as CrTP (Kim et al., 1996a) and 2,400 µg/kg of Cr as CrTP (Kim et al., 1996b) have also shown no adverse effect on growth performance. In fact, the broiler studies actually demonstrated a reduction in mortality with greater quantities of supplementation. In the present study, there was no mortality. Thus, animal well-being, as assessed by growth and livability, was not affected in the present study.
Clinical chemistry values (Table 3) for samples obtained from pigs the week of slaughter demonstrated some responses to the forms of Cr. Of the 16 response criteria presented, only 7 had differences (P < 0.05) among the dietary treatments. For 4 of those 7 response criteria, the differences existed among the Cr sources but not between pigs fed any of the Cr sources and those fed the unsupplemented control diet. Two of the 3 responses in which the control differed from a Cr source were serum K and total CO2. The third response in which a treatment differed from the control was alkaline phosphatase.
Blood urea nitrogen and creatinine values can be used clinically to screen for gross renal dysfunction (Kaneko, 1989). Increased values can occur when about 75% of nephrons become dysfunctional and glomerular filtration rate is affected; decreased levels of dysfunction, however, may not be detectable. In the present study, no treatment values differed from control values.
No treatment values differed from control values for blood glucose concentrations. It should be noted that these are fasting values. Studies have demonstrated that all of these Cr products (Amoikon et al., 1995; Fakler et al., 1999; Guan et al., 2000; Matthews et al., 2001) can change glucose concentrations in other situations. The products do affect either insulin or glucose values when a specific challenge (e.g., an in vivo glucose tolerance test or an in vivo insulin challenge test) is imposed.
Electrolyte and acid-base alterations may be mutually affected in situations of fluid and electrolyte imbalance (Kaneko, 1989). As previously noted, 2 of the 3 response criteria in which the control differed from a Cr source were serum K and total CO2. For both of these, however, the control value was intermediate among the various Cr sources. An interesting aspect among the electrolyte and acid-base. related measures was that all Na values were below the reference range, all K values were at the high end of the reference range, and Cl values were at the extreme low end of the reference range. Thus, the population dynamics of these pigs relative to those from which the reference range was established seem to be greater than any inter-treatment dynamics. This is also related to the reference values used; all of these values would be within the reference value ranges presented by Kaneko (1989).
Clinical enzymology [e.g., measuring alanine aminotransferase (ALT; EC number 2.6.1.2), aspartate aminotransferase (AST; EC number 2.6.1.1), and alkaline phosphatase (AP; EC number 3.1.3.1)] is useful for assessing metabolic responses related to some diseases as well as evaluating cellular membrane integrity (Kaneko, 1989). Elevation of serum enzymes may indicate leakage of an enzyme from a particular organ or induction of enzyme synthesis for a variety of reasons. The AP concentrations are elevated in situations of bone or liver disease, but because they originate from multiple tissues (bone, kidney, placenta, and liver), they are often measured in conjunction with other enzymes. The enzyme ALT is used to assess hepatic health in several species, whereas AST level is a good marker of soft tissue damage but not organ-specific damage. In the present study, there were no differences between the control and treatment samples in AST or ALP. One Cr product differed from the controls for serum AP, but all values were well within the standard reference range.
Serum bilirubin is correlated to its production from heme turnover, with much of the heme catabolism occurring in spleen and liver (Kaneko, 1989). Serum concentrations may be elevated in a variety of hepatobiliary maladies or species-specific diseases. The major site of serum protein synthesis is the liver, and thus, total serum protein is an indicator of hepatic synthesis. Cholesterol is a naturally occurring steroid that is predominantly synthesized in the liver, and it has been implicated in vascular disease. Cholesterol also has diagnostic value for situations such as hypothyroidism (Kaneko, 1989). None of these estimators of hepatic activity in pigs fed various Cr sources deviated from the values observed in control pigs.
With regard to the serum clinical chemistry values, the results primarily demonstrated no numerically large effects (orders of magnitude) of feeding a very large dose of Cr (25 times the Food and Drug Administration-permitted supplementation concentrations for those products approved in the United States). Serum values observed were within published normal ranges (Merck, 2005), which is evidence of the safety of this mineral. Anderson et al. (1997) fed up to 100 ppm of Cr from Cr chloride and CrTP (a concentration 20 times that fed in the present study to rats for 20 wk, almost twice the current length of supplementation) and observed no differences between controls or rats fed 100 ppm of either source in glucose, cholesterol, triacylglycerides, ALT, AST, blood urea N, and total protein.
The effects of the forms of Cr fed on carcass measurements and meat quality are provided in Table 4. Although there were no Cr form effects on dressing percentage, there was a uniform response on cooler shrink, with all Cr forms resulting in less shrink (P < 0.05) than that observed in control animal carcasses, which would indicate better water-holding capacity of the meat. There were also Cr responses in color measures. The L* scores did not differ statistically; however, all values for Cr-fed pigs were numerically less on both d 1 and 5, indicating a darker color. The a* scores indicated a meat that was less red on d 1 in pigs fed CrTP or CrY compared with those fed the control diet (P < 0.05); these same treatment pigs had muscle that was less yellow (a lower b* measure) on d 1, which was also observed in pigs fed CrMet. Statistically significant differences observed on d 1 were no longer present by d 5. It should be emphasized that these pigs were supplemented with 5,000 µg/kg of Cr from the various sources, but a maximum of 200 µg/kg is permitted in the United States (and for only 2 of the sources evaluated); thus, allowable supplementation rates may not elicit the same responses. Meat quality effects related to supplementation of 200 µg/kg of CrPrp have been evaluated in barrows (Matthews et al., 2003) and gilts (Matthews et al., 2005), but the results have not been uniform or consistent.
Results for the tissue mineral analyses (the primary objective of the experiment) are provided in Table 5. Values for 2 other minerals in addition to Cr are provided. The values for Mn and Zn were obtained simply to determine if there were associated effects on some of the divalent cations. The mean diet assay for Mn was 54.1 ppm (ranging from 53.8 to 54.6 ppm across the 5 diets) and for Zn was 154.9 ppm (ranging from 152.1 to 159.7 ppm across the 5 diets); thus, the diets were uniform in their contents of these 2 minerals.
There were generally few effects of Cr form on Mn and Zn, but bone Zn was uniformly reduced (P < 0.05) by 9 to 16% with this high level of supplementation. The physiological effects of this change are unknown, and the reduction was not observed in the other tissues. With regard to Cr, tissue results with rats (Anderson et al., 1996) indicate that kidney Cr concentration is greatest. In the present study, kidney had the greatest Cr concentration among tissues that showed a statistically significant response. Although the greatest numerical values were observed in the loin tissue, there were no statistically significant differences possibly because of the great assay variation. Although kidney may have exhibited the greatest significant response value (especially in CrTP-fed pigs), it should be noted that bone and muscle constitute a greater portion of BW and would provide greater total storage for subsequent use. Bone was, in fact, a consistently affected tissue with several forms of Cr showing elevated concentrations compared with the unsupplemented control. The largest relative increase in tissue Cr concentration was in the ovary. Both CrTP (12-fold response) and Cr Met (6-fold response) increased (P < 0.05) ovary Cr and the magnitude of this response was greater than that observed in bone. This may be related to improvements in reproductive performance that have been observed with CrTP (Lindemann et al., 1995, 2004; Hagen et al., 2000) and may indicate areas for further research. The concentrations of tissue Cr for kidney, liver, and ovary in this study are only marginally greater (<5%) than those observed by Lindemann et al. (2004) in sows fed 600 to 1,000 µg/kg of Cr from a study with multiple concentrations of CrTP supplementation for 3 parities. With regard to other species, Chang et al. (1992) failed to demonstrate any increases in muscle, fat, liver, or kidney Cr when steers were supplemented with 200 µg/kg of Cr from Cr yeast (a different product than the CrY product used in this experiment) for 138 d. Anderson et al. (1997) did observe linear increases in liver and kidney Cr in rats when CrTP was supplemented at 0, 5, 25, 50, or 100 ppm of Cr for 20 wk. Another study by Anderson et al. (1996) evaluated 9 Cr sources fed at 5,000 µg/kg to rats for 3 wk. The study demonstrated clear differences among Cr sources in Cr concentrations in various tissues, with the greatest Cr concentration found in the kidney. Consistent with the present study, muscle Cr was not affected. Of the 5 tissues that were affected, CrTP resulted in the greatest concentrations in liver, lung, and heart, essentially tied with Cr dinicotinic acid diglycine cysteine glutamic acid in spleen, and second to Cr dinicotinic acid diglycine cysteine glutamic acid in kidney. The other forms evaluated in our study (CrPrp, CrMet, and CrY) with pigs were not evaluated by Anderson et al. (1996).
In the present work, Cr content was increased (P < 0.05) in 4 of 5 tissues by CrTP and CrMet, whereas it was increased (P < 0.05) in only 2 of 5 tissues by CrY. Chromium content was not increased in any tissue by CrPrp. In all instances where statistically significant differences were observed, CrTP exceeded CrMet (4 times numerically and 3 times significantly), and in both instances, CrMet exceeded CrY numerically. Because 4 tissues had statistically significant increases in Cr content and all of those tissues had numerical increases for all Cr sources (with a uniform ranking of Cr sources), these tissues were used to assess relative bio-availability among Cr sources. Because CrTP yielded the greatest numerical Cr content for all tissues, it was set as the standard to which the other forms were compared (Table 6). For example, bone Cr was increased by 67.9 ng/g with CrTP and by 53.7 ng/g with CrMet; the increase for CrMet relative to CrTP was then 79.1% (53.7/67.9 x 100). Using this same procedure for all Cr forms for all responsive tissues (bone, kidney, liver, and ovary) gave a range of responses for which the mean bioavailability relative to CrTP across tissues was 13.1% for CrPrp (0.4 to 26.8%), 50.5% for CrMet (36.2 to 79.1%), and 22.8% for CrY (2.5 to 47.9%).
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Table 6. Effect of Cr source on tissue Cr concentration relative to that of Cr tripicolinate (CrTP)-fed pigs (DM basis)1
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In summary, the lack of negative response in growth performance, carcass measures, and clinical chemistry of Cr at the high concentration used herein provides great assurance that normal levels of addition are safe. This is consistent with rat studies (Anderson et al., 1997) in which evaluations at levels of 100 ppm of Cr (20 times the concentration used in this experiment) from CrCl3 or CrTP have also been without adverse effect. Chromium has been listed for many years as the least toxicity concern (less than all other minerals that are supplemented to animal diets; AAFCO, 2001), and the present results are consistent with that thought for any of the sources evaluated. These results show very clear Cr effects on multiple tissues, which is conclusive evidence of absorption and deposition. Not all forms affected tissue Cr concentration equally. This, too, is consistent with rat studies that indicate tissue/form dependency on deposition (Anderson et al., 1996). The results show obvious differences in tissue concentration of organic Cr from the different sources.
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Footnotes
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1 This manuscript is based on research supported in part by the Kentucky Agric. Exp. Stn. and Prince Agri Products Inc.; it is published by the Kentucky Agric. Exp. Stn. as paper No. 07-07-140. 
2 Appreciation is expressed to Akey Inc. (Lewisburg, OH) for the vitamin premix used in the experiments and to the following individuals from the University of Kentucky: B. R. Patton and W. L. Graham for assistance in the care of pigs, N. Inocencio in laboratory analysis, D. Higginbotham for help in diet preparation, and C. Armstrong for meat quality measures.
4 Current address: Delacon USA Inc., Quincy, IL 62305.
3 Corresponding author: merlin.lindemann{at}uky.edu
Received for publication January 21, 2008.
Accepted for publication June 23, 2008.
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LITERATURE CITED
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AAFCO. 2001. Official Publication. Assoc. Am. Feed Control Off. Inc., St. Louis. MO.
Ammerman, C. B. 1995. Methods for estimation of mineral bioavailability. Pages 83–94 in Bioavailability of Nutrients for Animals. C. B. Ammerman, D. H. Baker, and A. J. Lewis, ed. Academic Press, San Diego, CA.
Amoikon, E. K., J. M. Fernandez, L. L. Southern, D. L. Thompson Jr., T. L. Ward, and B. M. Olcott. 1995. Effect of chromium tripicolinate on growth, glucose tolerance, insulin sensitivity, plasma metabolites, and growth hormone in pigs. J. Anim. Sci. 73:1123–1130.[Abstract]
Anderson, R. A., N. A. Bryden, and M. M. Polansky. 1997. Lack of toxicity of chromium chloride and chromium picolinate in rats. J. Am. Coll. Nutr. 16:273–279.[Abstract]
Anderson, R. A., N. A. Bryden, M. M. Polansky, and K. Gautschi. 1996. Dietary chromium effects on tissue chromium concentrations and chromium absorption in rats. J. Trace Elem. Exp. Med. 9:11–25.[CrossRef]
AOAC. 1995. Official Methods of Analysis. 16th ed. 3rd rev. Suppl. Mar. 1997. Assoc. Off. Anal. Chem., Arlington, VA.
Chang, X., D. N. Mowat, and G. A. Spiers. 1992. Carcass characteristics and tissue-mineral contents of steers fed supplemental chromium. Can. J. Anim. Sci. 72:663–669.
Fakler, T. M., T. L. Ward, E. B. Kegley, M. T. Socha, A. B. Johnson, and C. V. Maxwell. 1999. Metabolic effects of dietary chromium-L-methionine in growing pigs. Page 110 in Proc. 10th Int. Symp. Trace Elements in Man and Animal. Evian, France. (Abstr.)
Guan, X., J. J. Matte, P. K. Ku, J. L. Snow, J. L. Burton, and N. L. Trottier. 2000. High chromium yeast supplementation improves glucose tolerance in pigs by decreasing hepatic extraction of insulin. J. Nutr. 130:1274–1279.[Abstract/Free Full Text]
Hagen, C. D., M. D. Lindemann, and K. W. Purser. 2000. Effect of dietary chromium tripicolinate on productivity of sows under commercial conditions. Swine Health Prod. 8:59–63.
Kaneko, J. J. 1989. Reference values for blood gas and electrolyte determinations. Page 564 in Clinical Biochemistry of Domestic Animals. 4th ed. J. J. Kaneko, ed. Academic Press, San Diego, CA.
Kim, Y. H., I. K. Han, Y. J. Choi, I. S. Shin, B. J. Chae, and T. H. Kang. 1996a. Effects of dietary levels of chromium picolinate on growth performance, carcass quality and serum traits in broiler chicks. Asian-australas. J. Anim. Sci. 9:341–347.
Kim, Y. H., I. Han, I. Shin, B. J. Chae, and T. H. Kang. 1996b. Effect of dietary excessive chromium picolinate on growth performance, nutrient utilizability and serum traits in broiler chicks. Asian-australas. J. Anim. Sci. 9:349–354.
Lindemann, M. D. 2007. Use of chromium as an animal feed supplement. Pages 85–118 in The Nutritional Biochemistry of Chromium(III). J. B. Vincent, ed. Elsevier Press, Amsterdam, the Netherlands.
Lindemann, M. D., S. D. Carter, L. I. Chiba, C. R. Dove, F. M. Lemieux, and L. L. Southern. 2004. A regional evaluation of chromium tripicolinate supplementation of diets fed to reproducing sows. J. Anim. Sci. 82:2972–2977.[Abstract/Free Full Text]
Lindemann, M. D., C. M. Wood, A. F. Harper, E. T. Kornegay, and R. A. Anderson. 1995. Dietary chromium picolinate additions improve gain:feed and carcass characteristics in growing-finishing pigs and increase litter size in reproducing sows. J. Anim. Sci. 73:457–465.[Abstract]
Matthews, J. O., A. C. Guzik, F. M. LeMieux, L. L. Southern, and T. D. Bidner. 2005. Effects of chromium propionate on growth, carcass traits, and pork quality of growing-finishing pigs. J. Anim. Sci. 83:858–862.[Abstract/Free Full Text]
Matthews, J. O., A. D. Higbie, L. L. Southern, D. F. Coombs, T. D. Bidner, and R. L. Odgaard. 2003. Effect of chromium propionate and metabolizable energy on growth, carcass traits, and pork quality of growing-finishing pigs. J. Anim. Sci. 81:191–196.[Abstract/Free Full Text]
Matthews, J. O., L. L. Southern, J. M. Fernandez, J. E. Pontif, T. D. Bidner, and R. L. Odgaard. 2001. Effect of chromium picolinate and chromium propionate on glucose and insulin kinetics of growing barrows and on growth and carcass traits of growing-finishing barrows. J. Anim. Sci. 79:2172–2178.[Abstract/Free Full Text]
Merck. 2005. Reference guides, Table 7. Serum biochemical reference ranges. Pages 2586–2587 in The Merck Veterinary Manual. 9th ed. Merck & Co. Inc., Whitehouse Station, NJ.
NPB. 2000. Pork Composition and Quality Assessment Procedures. E. P. Berg, ed. National Pork Board, Des Moines, IA.
NRC. 1998. Nutrient Requirements of Swine. 10th rev. ed. Natl. Acad. Press, Washington, DC.
Page, T. G., L. L. Southern, T. L. Ward, and D. L. Thompson Jr. 1993. Effect of chromium picolinate on growth and serum and carcass traits of growing-finishing pigs. J. Anim. Sci. 71:656–662.[Abstract]
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Abstract
INTRODUCTION
