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A review of the “mysterious” wasting disease in swedish moose (Alces alces L.) related to molybdenosis and disturbances in copper metabolism

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Abstract

The main purpose of this article is to review the previously published data on so-called “moose sickness” in the light of two case studies presented here. Molybdenosis and Mo-induced disturbances of Cu metabolism in moose are characterized by numerous severe lesions caused by reduced activity of Cu-containing enzymes such as ceruloplasmin, superoxide dismutase in blood, and myocardial cytochrome c oxidase. Consequences of such metabolic disturbances (e.g. glucose intolerance, insulin resistance, and noninsulin-dependent diabetes mellitus) were first reported in moose in 2000. This was corroborated by the detection of furosine, pentosidine, and Ne-(carboxymethyl)-lysine in blood plasma and the kidney, indicating long-term hyperglycemia. Increased concentrations of insulin, glucose, and urea and reduced levels of phosphate, T4, and Mg in blood were also seen. Recently, a similar toxic endocrinopathy was reported in sheep treated therapeutically with thiomolybdates because of chronic Cu toxicosis. Two case reports illustrate the difficulty of diagnosing Mo-related disturbances of Cu metabolism in moose, as analyses of Cu and Mo have not proved entirely reliable because of interaction, accumulation, and the short biological half-life of Mo. The increased bioavailability of Mo is most probably the result of increased pH in the soil, caused, for example, by liming, making Mo accessible in forage plants consumed by moose. The etiology underlying the Swedish moose disease has been difficult to determine because of the complex clinical signs and unspecific pathological findings. However, a combination of clinical chemistry, trace element analysis, and biochemistry correlated with the pathological findings has corroborated molybdenosis and Mo-induced disturbances of Cu metabolism as the probable etiological factor. Alternative etiologies suggested for the moose disease, such as viral infection, starvation because of overpopulation, and/or shortage of forage as well as senescence and phytotoxic substances, are discussed.

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References

  1. C. Rehbinder, E. Gimeno, K. Belák, et al., A bovine viral diarrhoea/mucosal disease-like syndrome in moose (Alces alces L.): investigations on the central nervous system, Vet. Rec. 129, 552–554 (1991).

    PubMed  CAS  Google Scholar 

  2. M. Stéen, A. Frank, M. Bergsten, and C. Rehbinder, En ny sjukdomsbild hos älg. [A new pathological pattern of moose disease]. Svensk Veterinärtidn. 41, 73–77 (1989) (in Swedish).

    Google Scholar 

  3. M. Stéen, R. Diaz, and E. Faber, An erosive/ulcerative alimentary disease of undetermined aetiology in Swedish moose (Alces alces L.), Rangifer 13, 149–156 (1993).

    Google Scholar 

  4. A. Frank, “Mysterious” moose disease in Sweden; similarities to copper deficiency and/or molybdenosis in cattle and sheep. Biochemical background of clinical signs and organ lesions, Sci. Total Environ. 209, 17–26 (1998).

    Article  PubMed  CAS  Google Scholar 

  5. Swedish Environmental Protection Agency, Swedish Liming 1989, Report No. 3606 (1989) (Svensk Kalkning, SNV Rapport 3606), Swedish Environmental Protection Agency, Stockholm, (1989), (in Swedish).

    Google Scholar 

  6. M. Simonsson, M. Merza, and M. Stéen, Virology concerning the project “Älvsborgssjukan hos älg”. Evaluation of virus as possible causative agent of Älvsborgssjukan, a moose wasting syndrome (MWS), in particular the study of a putative retrovirus associated with Älvsborgssjukan. Final Report, Swedish EPA. Stockholm (1999) (in Swedish).

    Google Scholar 

  7. E. Broman, K. Wallin, M. Stéen, and G. Cederlund, A wasting syndrome in Swedish moose (Alces alces): background and current hypotheses, Ambio 31, 409–416 (2002).

    Article  PubMed  Google Scholar 

  8. G. Ericsson and K. Wallin, Age-specific moose (Alces alces) mortality in a predator free environment: evidence for senescence in females, Ecoscience 8, 157–163 (2001).

    Google Scholar 

  9. G. Ericsson, K. Wallin, J. P. Ball, and M. Broberg, Age-related reproductive effort and senescence in free ranging moose, Alces alces, Ecology 82, 1613–1620 (2001).

    Google Scholar 

  10. K. Sunnerheim-Sjöberg and P.-G. Knutsson, Platyphylloside: metabolism and digestibility reduction in vitro, J. Chem. Ecol. 21, 1339–1340 (1995).

    Article  Google Scholar 

  11. A. Frank, V. Galgan, and L. R. Petersson, Secondary copper deficiency, chromium deficiency and trace element imbalance in the moose (Alces alces L.): effect of anthropogenic activity, Ambio 23, 315–317 (1994).

    Google Scholar 

  12. A. Frank, Bly-och kadmiumhalt in lever och njure från älg samt koncentrationer av kobolt, koppar, mangan och zink i älglever. Rapport till SNV. 1989-01-30. (Lead and cadmium contents in liver and kidneys from the moose (Alces alces L.) and hepatic concentrations of cobalt, copper, manganese and zinc. Sample collection comprising Sweden in 1982. Report to the Swedish EPA (1989) (in Swedish).

  13. A. Frank and V. Galgan, The moose (Alces alces L.), a fast and sensitive monitor of environmental changes, in Environmental Biomonitoring, K. S. Subramanian and G. V. Iyengar, eds., ACS Symposium Series No. 654, American Chemical Society, Washington, DC, pp. 57–64 (1997).

    Google Scholar 

  14. A. Frank, In search for biomonitors for cadmium: cadmium content of wild Swedish fauna during 1973–1976, Sci. Total Environ. 57, 57–65 (1986).

    Article  PubMed  CAS  Google Scholar 

  15. A. Frank, R. Danielsson, and B. Jones, The “mysterious” disease in Swedish moose. Concentrations of trace elements in liver and kidneys and clinical chemistry. Comparison with experimental molybdenosis and copper deficiency in the goat, Sci. Total Environ. 249, 107–122 (2000a).

    Article  PubMed  CAS  Google Scholar 

  16. A. Frank, D. R. Sell, R. Danielsson, J. F. Fogarty, and V. M. Monnier, A syndrome of molybdenosis, copper deficiency, and type 2 diabetes in the moose population of south west Sweden, Sci. Total Environ. 249, 123–131 (2000b).

    Article  PubMed  CAS  Google Scholar 

  17. A. Frank, M. Anke, and R. Danielsson, Experimental copper and chromium deficiency and additional molybdenum supplementation in goats. I. Feed consumption and weight development, Sci. Total Environ. 249, 133–142 (2000c).

    Article  PubMed  CAS  Google Scholar 

  18. A. Frank, R. Danielsson, and B. Jones, Experimental copper and chromium deficiency and additional molybdenum supplementation in goats. II. Concentrations of trace and minor elements in liver, kidneys and ribs, haematology and clinical chemistry, Sci. Total Environ. 249, 143–170 (2000d).

    Article  PubMed  CAS  Google Scholar 

  19. A. Frank, R. Wibom, and R. Danielsson, Myocardial cytochrome c oxidase activity in the Swedish moose (Alces alces L.) affected by molybdenosis, Sci. Total Environ. 290, 121–129 (2002).

    Article  PubMed  CAS  Google Scholar 

  20. A. Frank, Metallanalyser av älgorgan från Jönköpings län insamlade under hösten 1993. Utvärdering och jämförelse med 1982 års värden. Rapport till Länstyrelsen i Jönköping län, 1996-06-18. [Metal analysis of moose organs from the county of Jönköping collected in 1993. Evaluation and comparison with the reference values from 1982. Report to the County Council of Jönköping (1996) (in Swedish)].

  21. D. C. Blood and O. M. Radostits, Starvation, inanition (malnutrition). Copper deficiency, in Veterinary Medicine: A Textbook on the Diseases of Cattle, Sheep, Pigs, Goats and Horses, 7th ed., Baillière-Tindall, London, pp. 78–79 (1989).

    Google Scholar 

  22. D. C. Blood and O. M. Radostits, Starvation, inanition (malnutrition). Copper deficiency, in Veterinary Medicine: A Textbook on the Diseases of Cattle, Sheep, Pigs, Goats and Horses, 7th ed., Baillière-Tindall, London, pp. 1160–1173 (1989).

    Google Scholar 

  23. J. J. Strain, Newer aspects of micronutrients in chronic disease: copper, Proc. Nutr. Soc. 3, 583–598 (1994).

    Article  Google Scholar 

  24. A. Holmäng and P. Björntorp, The effects of testosterone on insulin sensitivity in male rats, Acta Physiol. Scand. 146, 505–510 (1992).

    PubMed  Google Scholar 

  25. S. Kumagai, A. Holmäng, and P. Björntorp, The effects of oestrogen and progesterone on insulin sensitivity in female rat, Acta Physiol. Scand. 149, 91–97 (1993).

    Article  PubMed  CAS  Google Scholar 

  26. S. Haywood, Z. Dincer, J. Holding, and N. M. Parry, Metal (molybdenum, copper) accumulation and retention in brain, pituitary and other organs of ammonium tetrathiomolybdate-treated sheep, Br. J. Nutr. 79, 329–331 (1998).

    Article  PubMed  CAS  Google Scholar 

  27. S. Haywood, Z. Dincer, B. Jasani, and M. J. Loughran, Molybdenum-associated pituitary endocrinopathy in sheep treated with ammonium tetrathiomolybdate, J. Comp. Pathol. 130, 21–31 (2004).

    Article  PubMed  CAS  Google Scholar 

  28. M. Phillippo, W. R. Humphries, I. Bremner, T. Atkinson, and G. Henderson, Molybdenum-induced infertility in cattle, in Proceedings of the Fifth International Symposium on Trace Elements in Man and Animals—TEMA 5, C. F. Mills, I. Bremner, and J. K. Chesters, eds., Commonwealth Agricultural Bureaux, Farnham Royal, Slough, England, pp. 176–180 (1985).

    Google Scholar 

  29. M. Phillippo, W. R. Humphries, T. Atkinson, G. D. Henderson, and P. H. Garthwaite, The effect of dietary molybdenum and iron on copper status, puberty, fertility and oestrous cycles in cattle, J. Agric. Sci. (Cambridge) 109, 321–334 (1987b).

    CAS  Google Scholar 

  30. L. Igarza, M. Agostini, D. Becú-Villalobos, and N. Auza, Efectos de la molibdenosis sobre hormona luterinizante, folículo estimulante y estradiol en ratas. [Effects of molybdenosis on luteinizing hormone, follicle stimulating and estradiol hormones in rats.] Arch. Med. Vet. 28, 101–106 (1996) (in Spanish, summary in English).

    CAS  Google Scholar 

  31. M. Phillippo, W. R. Humphries, and P. H. Garthwaite, The effect of dietary molybdenum and iron on copper status and growth in cattle, J. Agric. Sci. (Cambridge) 109, 315–320 (1987).

    CAS  Google Scholar 

  32. T. Kronevi, B. Holmberg, and K. Borg, Lens lesions in the elk, Acta Vet. Scand. 18, 159–167 (1977).

    PubMed  CAS  Google Scholar 

  33. T. Kuiken, B. Grahn, and G. Wobeser, Pathology of ocular lesions in free-living moose (Alces alces) from Saskatchewan, J. Wildl. Dis. 33, 87–94 (1997).

    PubMed  CAS  Google Scholar 

  34. H. Aupperle, H.-A. Schoon, and A. Frank, Experimental copper deficiency, chromium deficiency and additional molybdenum supplementation in goats—pathological findings, Acta Vet. Scand. 43, 311–322 (2001).

    Article  Google Scholar 

  35. M. Anke, Die Bedeutung der Spurenelemente für die Fauna. Kupfer, in Spurenelemente in der Umwelt, 2nd ed., H. J. Fiedler und H. J. Rösler, eds., Gustav Fischer Verlag, Stuttgart, p. 226 (1993). [The importance of trace elements for the fauna. Copper, in Trace Elements in the Environment, 2nd ed., Gustav Fischer Verlag, Stuttgart, p. 226 (1993).

    Google Scholar 

  36. N. F. Suttle, The role of comparative pathology in the study of copper and cobalt deficiencies in ruminants, J. Comp. Pathol. 99, 241–249 (1988).

    Article  PubMed  CAS  Google Scholar 

  37. N. F. Suttle, Trace element disorders, in Bovine Medicine: Diseases and Husbandry of Cattle, A. H. Andrews, R. W. Blowey, H. Boyed, and R. G. Eddy, eds., Blackwell Scientific, London, pp. 263–265 (1992).

    Google Scholar 

  38. C. F. Mills and G. K. Davis, Molybdenum, in Trace Elements in Human and Animal Nutrition, W. Mertz, ed., Academic, San Diego, CA, Vol. 1, pp. 429–457 (1987).

    Google Scholar 

  39. W. R. Humphries, M. Phillippo, B. W. Young, and I. Bremner, The influence of dietary iron and molybdenum on copper metabolism in calves, Br. J. Nutr. 49, 77–86 (1983).

    Article  PubMed  CAS  Google Scholar 

  40. G. K. Davis and W. Mertz, Copper, in Trace Elements in Human and Animal Nutrition, W. Mertz, ed., Academic, San Diego, CA, Vol. 1, pp. 301–364 (1987).

    Google Scholar 

  41. M. C. Linder, Biochemistry of copper, in Biochemistry of the Elements, E. Frieden, ed., Plenum, New York, Vol. 10 (1991).

    Google Scholar 

  42. G. K. Davis, The influence of copper on the metabolism of phosphorus and molybdenum, in Copper Metabolism, A Symposium on Animal, Plant, and Soil Relationships, W. D. McElroy and B. Glass, eds., Johns Hopkins Press, Baltimore, MD, pp. 216–229 (1950).

    Google Scholar 

  43. J. Christensen, P. Fischer, S. Knudsen, H. Surensen, and O. Venge, A syndrome of hereditary tyrosinemia in mink, Can. J. Comp. Med. 43, 333–340 (1979).

    PubMed  CAS  Google Scholar 

  44. S. E. Sanford, Tyrosinemia II (pseudodistemper) in mink, Can. Vet. J. 29, 298–299 (1988).

    PubMed  CAS  Google Scholar 

  45. R. Wibom, personal communication (2001).

  46. A. A. Mylroie, A. Boseman, and J. Kyle, Pancreatic superoxide dismutase activity in copper-depleted rat, in Trace Elements in Man and Environment (TEMA 6), L. S. Hurley, C. L. Keen, B. Lönnerdal, and R. B. Rucker, eds., Plenum, New York, pp. 381–382 (1988).

    Google Scholar 

  47. A. A. Mylroie, A. Boseman, and J. Kyle, Further studies on the effects of dietary copper deficiency on rat pancreas. Trace Substances in Environmental Health, XXII Proc., pp. 419–428 (1988).

  48. F. J. Schweigert, S. Uehlein-Harrel, G. v. Hegel, and H. Wiesner, Vitamin A (retinol and retinyl esters), α-tocopherol and lipid levels in plasma of captive wild mammals and birds, J. Vet. Med. A 38, 35–42 (1991).

    Article  CAS  Google Scholar 

  49. V. Galgan and A. Frank, Survey of bioavailable selenium in Sweden with the moose (Alces alces L.) as monitoring animal. Sci. Total Environ. 172, 37–45 (1995).

    Article  PubMed  CAS  Google Scholar 

  50. A. K. Sharma and N. S. Parihar, Pathology of experimental molybdenosis in goats, Ind. J. Anim. Sci. 64, 114–119 (1994).

    Google Scholar 

  51. A. K. Sharma and N. S. Parihar, Clinicopathology of induced molybdenum toxicity in young goats. Int. J. Anim. Sci. 64, 120–125 (1994b).

    CAS  Google Scholar 

  52. B. Ytrehus, H. Skagemo, G. Stuve, T. Sievertsen, K. Handeland, and T. Vikøren, Osteoporosis, bone mineralization, and status of selected trace elements in two populations of moose calves in Norway, J. Wildl. Dis. 35, 204–211 (1999).

    PubMed  CAS  Google Scholar 

  53. T. M. O'Hara, G. Caroll, P. Barboza, et al. Mineral and heavy metal status as related to a mortality event and poor recruitment in a moose population in Alaska, J. Wildl. Dis. 37, 509–522 (2001).

    PubMed  Google Scholar 

  54. R. P. Brockman, Concentration of copper in livers of Saskatchewan cattle at slaughter Can. Vet. J. 18, 168–170 (1977).

    PubMed  CAS  Google Scholar 

  55. S. R. Gooneratne, W. T. Buckley, and D. A. Christensen, Review of copper deficiency and metabolism in ruminants, Can. J. Anim. Sci. 69, 819–845 (1989).

    Article  Google Scholar 

  56. D. A. Christensen, Trace mineral deficiency in ruminants problems in western Canada, Proceedings of the Western Nutrition Conference (1980).

  57. E. Funseth, U. Lindh, L. Wesslén, G. Friman, and N. G. Ilbäck, Trace element changes in the myocardium during Coxsackievirus B3 myocarditis in the mouse, Biol. Trace Element Res. 76, 149–160 (2000).

    Article  CAS  Google Scholar 

  58. Å. Pehrson, Effekter av kalkning på mineralhalter i älgbetesväxter. Rapport 5. Hjortviltgruppen. Grimsö. SLU. 1996-08-20. [Liming effects on mineral concentrations in moose forage. Grimsö Wildlife Research Station, pp. 26 (1996) (in Swedish)].

  59. Workshop EU. Improvements of Trace Elements in Plant Matrices, Brussels, 29–31 May 1994, Sci. Total Environ. 176, 1–3 (1995).

    Article  Google Scholar 

  60. F. MacNaeidhe, Procedures and precautions used in sampling techniques and analysis of trace elements in plant matrices, Sci. Total Environ. 176, 25–31 (1995).

    Article  CAS  Google Scholar 

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  1. Department of Clinical Chemistry, Faculty of Veterinary Medicine and Animal Sciences, Swedish University of Agricultural Sciences, Box 7038, SE-750 07, Uppsala, Sweden

    Adrian Frank

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Frank, A. A review of the “mysterious” wasting disease in swedish moose (Alces alces L.) related to molybdenosis and disturbances in copper metabolism. Biol Trace Elem Res 102, 143–159 (2004). https://doi.org/10.1385/BTER:102:1-3:143

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