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- Introduction
- Copper Content of Commercial Dog Foods and Hepatic Copper Concentrations in Dogs
- Copper Metabolism
- Hepatic Injury Association With Copper Accumulation
- Histologic Patterns of Copper-Mediated Hepatic Injury
- Treatment of Dogs With Pathological Hepatic Copper Accumulation
- Potential Causes of Pathological Hepatic Copper Accumulation
- Determining Dietary Copper Requirements and Tolerability
- Summary of Evidence for Reconsidering Dietary Copper Recommendations for Dogs
- Conclusions
- Acknowledgments
- Footnotes
- Abbreviations
- References
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Su LC, Owen CA, Zollman PE, et al. A defect of biliary excretion of copper in copper-laden Bedlington Terriers. Am J Physiol 1982;243:G231–G236.
-
2.
Su LC, Ravanshad S, Owen CA, et al. A comparison of copper-loading disease in Bedlington Terriers and Wilson's disease in humans. Am J Physiol 1982;243:G226–G230.
-
3.
Thornburg LP. A perspective on copper and liver disease in the dog. J Vet Diagn Invest 2000;12:101–110.
-
4.
Johnston AN, Center SA, McDonough SP, et al. Hepatic copper concentrations in Labrador Retrievers with and without chronic hepatitis: 72 cases (1980–2010). J Am Vet Med Assoc 2013;242:372–380.
-
5.
Gagné JW, Wakshlag JJ, Center SA, et al. Evaluation of calcium, phosphorus, and selected trace mineral status in commercially available dry foods formulated for dogs. J Am Vet Med Assoc 2013;243:658–666.
-
6.
Fieten H, Hooijer-Nouwens BD, Biourge VC, et al. Association of dietary copper and zinc levels with hepatic copper and zinc concentration in Labrador Retrievers. J Vet Intern Med 2012;26:1274–1280.
-
7.
Strickland JM, Buchweitz JP, Smedley RC, et al. Hepatic copper concentrations in 546 dogs (1982–2015). J Vet Intern Med 2018;32:1943–1950.
-
8.
Association of American Feed Control Officials. 2019 official publication. Oxford, Ind: Association of American Feed Control Officials, 2019.
-
9.
National Research Council. Minerals. In: Beitz DC, ed. Nutrient requirements of dogs and cats. Washington, DC: National Academies Press, 2006;145–192.
-
10.
Baker DH. Cupric oxide should not be used as a copper supplement for either animals or humans. J Nutr 1999;129:2278–2279.
-
11.
Flinn FB, Inouye JM. Some physiological aspects of copper in the organism. J Biol Chem 1929;84:101–114.
-
12.
Meyer AE, Eggreet C. Iron and copper in liver and liver extracts. J Biol Chem 1932;99:265–270.
-
13.
Beck AB. The copper content of the liver and blood of some vertebrates. Aust J Zool 1956;4:1–18.
-
14.
Gumbrell RC. Suspected copper deficiency in a group of full sib Samoyed dogs. N Z Vet J 1972;20:238–240.
-
15.
Keen CL, Lonnerdal B, Fisher GL. Age related variations in hepatic iron, copper, zinc and selenium concentrations in Beagles. Am J Vet Res 1981;42:1884–1887.
-
16.
Thornburg LP, Shaw D, Dolan M, et al. Hereditary copper toxicosis in West Highland White Terriers. Vet Pathol 1986;23:148–154.
-
17.
Zentek J, Meyer H. Investigations on copper deficiency in growing dogs. J Nutr 1991;121:S83–S84.
-
18.
Sternlieb I, Twedt DC, Johnson GF, et al. Inherited copper toxicity of the liver in Bedlington Terriers. Proc R Soc Med 1977;70(suppl 3):8–9.
-
19.
Twedt DC, Sternlieb I, Gilbertson SR. Clinical, morphologic and chemical studies on copper toxicosis of Bedlington Terriers. J Am Vet Med Assoc 1979;175:269–275.
-
20.
Ludwig J, Owen CA Jr, Barham SS, et al. The liver in the inherited copper disease of Bedlington Terriers. Lab Invest 1980;43:82–87.
-
21.
Hunt DM, Wake SA, Mercer JF, et al. A study of the role of metallothionein in the inherited copper toxicosis of dogs. Biochem J 1986;236:409–415.
-
22.
Miller AJ, Center SA, Randolph JF, et al. Disparities in hepatic copper concentrations determined by atomic absorption spectroscopy, inductively coupled plasma mass spectrometry, and digital image analysis of rhodanine-stained sections in dogs. J Am Vet Med Assoc 2021;258:395–406.
-
23.
Center SA, McDonough SP, Bogdanovic L. Digital image analysis of rhodanine-stained liver biopsy specimens for calculation of hepatic copper concentrations in dogs. Am J Vet Res 2013;74:1474–1480.
-
24.
Kim BE, Nevitt T, Thiele DJ. Mechanisms for copper acquisition, distribution and regulation. Nat Chem Biol 2008;4:176–185.
-
25.
Gaetke LM, Chow-Johnson HS, Chow CK. Copper: toxicological relevance and mechanisms. Arch Toxicol 2014;88:1929–1938.
-
26.
Gaetke LM, Chow CK. Copper toxicity: oxidative stress and antioxidant nutrients. Toxicology 2003;189:147–163.
-
27.
Wapnir RA. Copper absorption and bioavailability. Am J Clin Nutr 1998;67(suppl 5):1054S–1060S.
-
28.
Baker ZN, Cobine PA, Leary SC. The mitochondrion: a central architect of copper homeostasis. Metallomics 2017;9:1501–1512.
-
29.
Zischka H, Lichtmannegger J. Pathological mitochondrial copper overload in livers of Wilson's disease patients and related animal models. Ann N Y Acad Sci 2014;1315:6–15.
-
30.
Yuan L, Kaplowitz N. Glutathione in liver diseases and hepatotoxicity. Mol Aspects Med 2009;30:29–41.
-
31.
Sokol RJ, Devereaux MW, O'Brien K, et al. Abnormal hepatic mitochondrial respiration and cytochrome C oxidase activity in rats with long-term copper overload. Gastroenterology 1993;105:178–187.
-
32.
Nagasaka H, Takayanagi M, Tsukahara H. Childrens' toxicology from bench to bed—liver injury (3): oxidative stress and antioxidant systems in liver of patients with Wilson disease. J Toxicol Sci 2009;34:SP229–SP236.
-
33.
Jing M, Liu Y, Song W, et al. Oxidative damage induced by copper in mouse primary hepatocytes by single-cell analysis. Environ Sci Pollut Res Int 2016;23:1335–1343.
-
34.
Sokol RJ, Devereaux M, Mierau GW, et al. Oxidant injury to hepatic mitochondrial lipids in rats with dietary copper overload. Modification by vitamin E deficiency. Gastroenterology 1990;99:1061–1071.
-
35.
Hill TL, Breitschwerdt EB, Cecere T, et al. Concurrent hepatic copper toxicosis and Fanconi's syndrome in a dog. J Vet Intern Med 2008;22:219–222.
-
36.
Appleman EH, Cianciolo R, Mosenco AS, et al. Transient acquired Fanconi syndrome associated with copper storage hepatopathy in 3 dogs. J Vet Intern Med 2008;22:1038–1042.
-
37.
Langlois DK, Smedley RC, Schall WD, et al. Acquired proximal renal tubular dysfunction in 9 Labrador Retrievers with copper-associated hepatitis (2006–2012). J Vet Intern Med 2013;27:491–499.
-
38.
Webster CRL, Center SA, Cullen JM, et al. ACVIM consensus statement on the diagnosis and treatment of chronic hepatitis in dogs. J Vet Intern Med 2019;33:1173–1200.
-
39.
Fieten H, Biourge VC, Watson AL, et al. Dietary management of Labrador Retrievers with subclinical hepatic copper accumulation. J Vet Intern Med 2015;29:822–827.
-
40.
van De Sluis B, Rothuizen J, Pearson PL, et al. Identification of a new copper metabolism gene by positional cloning in a purebred dog population. Hum Mol Genet 2002;11:165–173.
-
41.
Klomp AE, van de Sluis B, Klomp LW, et al. The ubiquitously expressed MURR1 protein is absent in canine copper toxicosis. J Hepatol 2003;39:703–709.
-
42.
Schilsky ML. Wilson disease: diagnosis, treatment, and follow-up. Clin Liver Dis 2017;21:755–767.
-
43.
Fieten H, Gill Y, Martin AJ, et al. The Menkes and Wilson disease genes counteract in copper toxicosis in Labrador Retrievers: a new canine model for copper-metabolism disorders. Dis Model Mech 2016;9:25–38.
-
44.
Pindar S, Ramirez C. Predicting copper toxicosis: relationship between the ATP7A and ATP7B gene mutations and hepatic copper quantification in dogs. Hum Genet 2019;138:541–546.
-
45.
Wu X, Mandigers PJJ, Watson AL, et al. Association of the canine ATP7A and ATP7B with hepatic copper accumulation in Doberman dogs. J Vet Intern Med 2019;33:1646–1652.
-
46.
Haywood S, Boursnell M, Loughran MJ, et al. Copper toxicosis in non-COMMD1 Bedlington Terriers is associated with metal transport gene ABCA12. J Trace Elem Med Biol 2016;35:83–89.
-
47.
Hurwitz BM, Center SA, Randolph JF, et al. Presumed primary and secondary hepatic copper accumulation in cats. J Am Vet Med Assoc 2014;244:68–77.
-
48.
Azumi N. Copper and liver injury—experimental studies on the dogs with biliary obstruction and copper loading. Hokkaido Igaku Zasshi 1982;57:331–349.
-
49.
Spee B, Arends B, van den Ingh TSGAM, et al. Copper metabolism and oxidative stress in chronic inflammatory and cholestatic liver diseases in dogs. J Vet Intern Med 2006;20:1085–1092.
-
50.
Requirements of vitamin A, iron, folate, and vitamin B12. Report of a Joint FAO/WHO Expert Consultation. Rome: Food and Agriculture Organization of the United Nations, 1988.
-
51.
Milne DB. Assessment of copper nutritional status. Clin Chem 1994;40:1479–1484.
-
52.
Lönnerdal B. Bioavailability of copper. Am J Clin Nutr 1996;63:821S–829S.
-
53.
Olivares M, Uauy R. Limits of metabolic tolerance to copper and biological basis for present recommendations and regulations. Am J Clin Nutr 1996;63:846S–852S.
-
54.
Taylor AA, Tsuji JS, Garry MR, et al. Critical review of exposure and effects: implications for setting regulatory health criteria for ingested copper. Environ Manage 2020;65:131–159.
-
55.
AAFCO methods for substantiating nutritional adequacy of dog and cat foods. Proposed revisions edited per comments for 2014 Official Publication. Available at: www.aafco.org/Portals/0/SiteContent/Regulatory/Committees/Pet-Food/Reports/Pet_Food_Report_2013_Midyear-Proposed_Revisions_to_AAFCO_Nutrient_Profiles.pdf. Accessed Oct 26, 2020.
-
56.
Hoffmann G, Jones PG, Biourge V, et al. Dietary management of hepatic copper accumulation in Labrador Retrievers. J Vet Intern Med 2009;23:957–963.
-
57.
Fieten H, Biourge VC, Watson AL, et al. Nutritional management of inherited copper-associated hepatitis in the Labrador Retriever. Vet J 2014;199:429–433.
-
58.
Laflamme DP, Allen SW, Huber TL. Apparent dietary protein requirement of dogs with portosystemic shunt. Am J Vet Res 1993;54:719–723.
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Is it time to reconsider current guidelines for copper content in commercial dog foods?
Sharon A. Center
DVM
Sharon A. Center
From the Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853.
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Keith P. Richter
DVM
Keith P. Richter
Veterinary Specialty Hospital of San Diego, San Diego, CA 92121.
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David C. Twedt
DVM
David C. Twedt
Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO 80521.
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Joseph J. Wakshlag
DVM, PhD
Joseph J. Wakshlag
From the Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853.
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Penny J. Watson
VetMD
Penny J. Watson
Department of Veterinary Medicine, University of Cambridge, Cambridge CB3 0ES, England.
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Cynthia R. L. Webster
DVM
Cynthia R. L. Webster
Department of Clinical Sciences, Cummings School of Veterinary Medicine, Tufts University, North Grafton, MA 01536.
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- Introduction
- Copper Content of Commercial Dog Foods and Hepatic Copper Concentrations in Dogs
- Copper Metabolism
- Hepatic Injury Association With Copper Accumulation
- Histologic Patterns of Copper-Mediated Hepatic Injury
- Treatment of Dogs With Pathological Hepatic Copper Accumulation
- Potential Causes of Pathological Hepatic Copper Accumulation
- Determining Dietary Copper Requirements and Tolerability
- Summary of Evidence for Reconsidering Dietary Copper Recommendations for Dogs
- Conclusions
- Acknowledgments
- Footnotes
- Abbreviations
- References
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Su LC, Owen CA, Zollman PE, et al. A defect of biliary excretion of copper in copper-laden Bedlington Terriers. Am J Physiol 1982;243:G231–G236.
-
2.
Su LC, Ravanshad S, Owen CA, et al. A comparison of copper-loading disease in Bedlington Terriers and Wilson's disease in humans. Am J Physiol 1982;243:G226–G230.
-
3.
Thornburg LP. A perspective on copper and liver disease in the dog. J Vet Diagn Invest 2000;12:101–110.
-
4.
Johnston AN, Center SA, McDonough SP, et al. Hepatic copper concentrations in Labrador Retrievers with and without chronic hepatitis: 72 cases (1980–2010). J Am Vet Med Assoc 2013;242:372–380.
-
5.
Gagné JW, Wakshlag JJ, Center SA, et al. Evaluation of calcium, phosphorus, and selected trace mineral status in commercially available dry foods formulated for dogs. J Am Vet Med Assoc 2013;243:658–666.
-
6.
Fieten H, Hooijer-Nouwens BD, Biourge VC, et al. Association of dietary copper and zinc levels with hepatic copper and zinc concentration in Labrador Retrievers. J Vet Intern Med 2012;26:1274–1280.
-
7.
Strickland JM, Buchweitz JP, Smedley RC, et al. Hepatic copper concentrations in 546 dogs (1982–2015). J Vet Intern Med 2018;32:1943–1950.
-
8.
Association of American Feed Control Officials. 2019 official publication. Oxford, Ind: Association of American Feed Control Officials, 2019.
-
9.
National Research Council. Minerals. In: Beitz DC, ed. Nutrient requirements of dogs and cats. Washington, DC: National Academies Press, 2006;145–192.
-
10.
Baker DH. Cupric oxide should not be used as a copper supplement for either animals or humans. J Nutr 1999;129:2278–2279.
-
11.
Flinn FB, Inouye JM. Some physiological aspects of copper in the organism. J Biol Chem 1929;84:101–114.
-
12.
Meyer AE, Eggreet C. Iron and copper in liver and liver extracts. J Biol Chem 1932;99:265–270.
-
13.
Beck AB. The copper content of the liver and blood of some vertebrates. Aust J Zool 1956;4:1–18.
-
14.
Gumbrell RC. Suspected copper deficiency in a group of full sib Samoyed dogs. N Z Vet J 1972;20:238–240.
-
15.
Keen CL, Lonnerdal B, Fisher GL. Age related variations in hepatic iron, copper, zinc and selenium concentrations in Beagles. Am J Vet Res 1981;42:1884–1887.
-
16.
Thornburg LP, Shaw D, Dolan M, et al. Hereditary copper toxicosis in West Highland White Terriers. Vet Pathol 1986;23:148–154.
-
17.
Zentek J, Meyer H. Investigations on copper deficiency in growing dogs. J Nutr 1991;121:S83–S84.
-
18.
Sternlieb I, Twedt DC, Johnson GF, et al. Inherited copper toxicity of the liver in Bedlington Terriers. Proc R Soc Med 1977;70(suppl 3):8–9.
-
19.
Twedt DC, Sternlieb I, Gilbertson SR. Clinical, morphologic and chemical studies on copper toxicosis of Bedlington Terriers. J Am Vet Med Assoc 1979;175:269–275.
-
20.
Ludwig J, Owen CA Jr, Barham SS, et al. The liver in the inherited copper disease of Bedlington Terriers. Lab Invest 1980;43:82–87.
-
21.
Hunt DM, Wake SA, Mercer JF, et al. A study of the role of metallothionein in the inherited copper toxicosis of dogs. Biochem J 1986;236:409–415.
-
22.
Miller AJ, Center SA, Randolph JF, et al. Disparities in hepatic copper concentrations determined by atomic absorption spectroscopy, inductively coupled plasma mass spectrometry, and digital image analysis of rhodanine-stained sections in dogs. J Am Vet Med Assoc 2021;258:395–406.
-
23.
Center SA, McDonough SP, Bogdanovic L. Digital image analysis of rhodanine-stained liver biopsy specimens for calculation of hepatic copper concentrations in dogs. Am J Vet Res 2013;74:1474–1480.
-
24.
Kim BE, Nevitt T, Thiele DJ. Mechanisms for copper acquisition, distribution and regulation. Nat Chem Biol 2008;4:176–185.
-
25.
Gaetke LM, Chow-Johnson HS, Chow CK. Copper: toxicological relevance and mechanisms. Arch Toxicol 2014;88:1929–1938.
-
26.
Gaetke LM, Chow CK. Copper toxicity: oxidative stress and antioxidant nutrients. Toxicology 2003;189:147–163.
-
27.
Wapnir RA. Copper absorption and bioavailability. Am J Clin Nutr 1998;67(suppl 5):1054S–1060S.
-
28.
Baker ZN, Cobine PA, Leary SC. The mitochondrion: a central architect of copper homeostasis. Metallomics 2017;9:1501–1512.
-
29.
Zischka H, Lichtmannegger J. Pathological mitochondrial copper overload in livers of Wilson's disease patients and related animal models. Ann N Y Acad Sci 2014;1315:6–15.
-
30.
Yuan L, Kaplowitz N. Glutathione in liver diseases and hepatotoxicity. Mol Aspects Med 2009;30:29–41.
-
31.
Sokol RJ, Devereaux MW, O'Brien K, et al. Abnormal hepatic mitochondrial respiration and cytochrome C oxidase activity in rats with long-term copper overload. Gastroenterology 1993;105:178–187.
-
32.
Nagasaka H, Takayanagi M, Tsukahara H. Childrens' toxicology from bench to bed—liver injury (3): oxidative stress and antioxidant systems in liver of patients with Wilson disease. J Toxicol Sci 2009;34:SP229–SP236.
-
33.
Jing M, Liu Y, Song W, et al. Oxidative damage induced by copper in mouse primary hepatocytes by single-cell analysis. Environ Sci Pollut Res Int 2016;23:1335–1343.
-
34.
Sokol RJ, Devereaux M, Mierau GW, et al. Oxidant injury to hepatic mitochondrial lipids in rats with dietary copper overload. Modification by vitamin E deficiency. Gastroenterology 1990;99:1061–1071.
-
35.
Hill TL, Breitschwerdt EB, Cecere T, et al. Concurrent hepatic copper toxicosis and Fanconi's syndrome in a dog. J Vet Intern Med 2008;22:219–222.
-
36.
Appleman EH, Cianciolo R, Mosenco AS, et al. Transient acquired Fanconi syndrome associated with copper storage hepatopathy in 3 dogs. J Vet Intern Med 2008;22:1038–1042.
-
37.
Langlois DK, Smedley RC, Schall WD, et al. Acquired proximal renal tubular dysfunction in 9 Labrador Retrievers with copper-associated hepatitis (2006–2012). J Vet Intern Med 2013;27:491–499.
-
38.
Webster CRL, Center SA, Cullen JM, et al. ACVIM consensus statement on the diagnosis and treatment of chronic hepatitis in dogs. J Vet Intern Med 2019;33:1173–1200.
-
39.
Fieten H, Biourge VC, Watson AL, et al. Dietary management of Labrador Retrievers with subclinical hepatic copper accumulation. J Vet Intern Med 2015;29:822–827.
-
40.
van De Sluis B, Rothuizen J, Pearson PL, et al. Identification of a new copper metabolism gene by positional cloning in a purebred dog population. Hum Mol Genet 2002;11:165–173.
-
41.
Klomp AE, van de Sluis B, Klomp LW, et al. The ubiquitously expressed MURR1 protein is absent in canine copper toxicosis. J Hepatol 2003;39:703–709.
-
42.
Schilsky ML. Wilson disease: diagnosis, treatment, and follow-up. Clin Liver Dis 2017;21:755–767.
-
43.
Fieten H, Gill Y, Martin AJ, et al. The Menkes and Wilson disease genes counteract in copper toxicosis in Labrador Retrievers: a new canine model for copper-metabolism disorders. Dis Model Mech 2016;9:25–38.
-
44.
Pindar S, Ramirez C. Predicting copper toxicosis: relationship between the ATP7A and ATP7B gene mutations and hepatic copper quantification in dogs. Hum Genet 2019;138:541–546.
-
45.
Wu X, Mandigers PJJ, Watson AL, et al. Association of the canine ATP7A and ATP7B with hepatic copper accumulation in Doberman dogs. J Vet Intern Med 2019;33:1646–1652.
-
46.
Haywood S, Boursnell M, Loughran MJ, et al. Copper toxicosis in non-COMMD1 Bedlington Terriers is associated with metal transport gene ABCA12. J Trace Elem Med Biol 2016;35:83–89.
-
47.
Hurwitz BM, Center SA, Randolph JF, et al. Presumed primary and secondary hepatic copper accumulation in cats. J Am Vet Med Assoc 2014;244:68–77.
-
48.
Azumi N. Copper and liver injury—experimental studies on the dogs with biliary obstruction and copper loading. Hokkaido Igaku Zasshi 1982;57:331–349.
-
49.
Spee B, Arends B, van den Ingh TSGAM, et al. Copper metabolism and oxidative stress in chronic inflammatory and cholestatic liver diseases in dogs. J Vet Intern Med 2006;20:1085–1092.
-
50.
Requirements of vitamin A, iron, folate, and vitamin B12. Report of a Joint FAO/WHO Expert Consultation. Rome: Food and Agriculture Organization of the United Nations, 1988.
-
51.
Milne DB. Assessment of copper nutritional status. Clin Chem 1994;40:1479–1484.
-
52.
Lönnerdal B. Bioavailability of copper. Am J Clin Nutr 1996;63:821S–829S.
-
53.
Olivares M, Uauy R. Limits of metabolic tolerance to copper and biological basis for present recommendations and regulations. Am J Clin Nutr 1996;63:846S–852S.
-
54.
Taylor AA, Tsuji JS, Garry MR, et al. Critical review of exposure and effects: implications for setting regulatory health criteria for ingested copper. Environ Manage 2020;65:131–159.
-
55.
AAFCO methods for substantiating nutritional adequacy of dog and cat foods. Proposed revisions edited per comments for 2014 Official Publication. Available at: www.aafco.org/Portals/0/SiteContent/Regulatory/Committees/Pet-Food/Reports/Pet_Food_Report_2013_Midyear-Proposed_Revisions_to_AAFCO_Nutrient_Profiles.pdf. Accessed Oct 26, 2020.
-
56.
Hoffmann G, Jones PG, Biourge V, et al. Dietary management of hepatic copper accumulation in Labrador Retrievers. J Vet Intern Med 2009;23:957–963.
-
57.
Fieten H, Biourge VC, Watson AL, et al. Nutritional management of inherited copper-associated hepatitis in the Labrador Retriever. Vet J 2014;199:429–433.
-
58.
Laflamme DP, Allen SW, Huber TL. Apparent dietary protein requirement of dogs with portosystemic shunt. Am J Vet Res 1993;54:719–723.
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