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Lessons from the Past: Metabolic Bone Disease in Historical Captive Primates

Abstract

Primate welfare in captivity has significantly improved over the last century as a result of the advances made in providing an adequate diet and environment. The skeletal collections of museums provide evidence of this shift in captive care, because metabolic disease caused by dietary deficiency or inappropriate surroundings can cause deformation to the hard tissues. The Royal College of Surgeons of England (RCS) holds a collection of 1507 nonhuman primate skulls in its Odontological Collection, the majority donated before the mid-20th century from various sources. We observed a recurring gross pathology in 51 of these skulls, noted in museum records as captive animals. In all cases, general bone thickening with decreased bone density is the main feature and involves primarily the bones of the maxillofacial region and mandible. We performed computed tomography scanning on a subsample of these skulls to investigate these pathological features further. We compared the RCS historical collections and a more recent captive primate collection at the National Museum of Scotland. The findings suggest that a metabolic bone disease is the causative agent, with osteomalacia the likely diagnosis. Osteomalacia typically occurs due to malnutrition and/or insufficient ultraviolet light exposure and in this case reflects the inadequacy of zoo primate management during the late 19th and early 20th centuries. Developments have since been made in captive animal welfare as a result of improvements in nutrition and environment. Metabolic bone disease in primate captivity can be regarded as a lesson from the past.

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References

  1. Barker, M. J. M., & Herbert, R. T. (1972). Diseases of the Skeleton. In R. N. T-W-Fienes (Ed.), Pathology of simian primates (pp. 433–519). Basel: S. Karger.

    Chapter  Google Scholar 

  2. Bernard, J. B. (1997). Vitamin D and ultraviolet radiation: Meeting lighting needs for captive animals. In Nutrition Advisory Group handbook fact sheet 002. http://nagonline.net/wp-content/uploads/2014/01/NAG-FS002-97-Vit-D-JONI-FEB-24-2002-MODIFiED.pdf (Accessed June 17, 2013).

  3. Brooks, H., & Blair, W. R. (1904). Eighth annual report of the New York Zoological Society for 1903. New York: Crow Press.

    Google Scholar 

  4. Chesney, R. W. (1984). Metabolic bone diseases. Pediatrics in Review, 5(8), 227–237.

    Article  Google Scholar 

  5. Cousins, D. (2008). Possible goundou in gorillas. Gorilla Journal, 37, 22–24

  6. Favus, M. J. (2008). Primer on the metabolic bone diseases and disorders of mineral metabolism, 4th ed. Philadelphia: American Society for Bone and Mineral Research.

  7. Fidgett, A. L., & Dierenfeld, E. S. (2007). Minerals and stork nutrition. In M. E. Fowler & R. E. Miller (Eds.), Zoo and wild animal medicine: Current therapy (6th ed.). St. Louis, MO: Saunders (Elsevier).

    Google Scholar 

  8. Gartner, L. M., & Greer, F. R. (2003). Prevention of rickets and vitamin D deficiency: New guidelines for vitamin D intake. Pediatrics, 111, 908–910.

    Article  PubMed  Google Scholar 

  9. Gillespie, D., Frye, F. L., Stockham, S. L., & Fredeking, T. (2001). Blood values in wild and captive Komodo dragons (Varanus komodoensis). Zoo Biology, 19, 495–509.

    Article  Google Scholar 

  10. Gonzalez-Reimers, E. (2007). Quantitative computerized tomography for the diagnosis of osteopenia in prehistoric skeletal remains. Journal of Archaeological Science, 34(4), 554–561.

    Article  Google Scholar 

  11. Guillery, P. (1993). The buildings of London Zoo. London: Royal Commission on the Historical Monuments of England.

  12. Hamerton, A. E. (1929). Report on the deaths occurring in the Society's Gardens during the Year 1928. Proceedings Zoological Society of London – Yearbook, 99(1), 49–59.

    Article  Google Scholar 

  13. Hamerton, A. E. (1931). Report on the deaths occurring in the Society’s gardens during the year 1930. Proceedings Zoological Society of London – Yearbook, 101(2), 527–555.

    Article  Google Scholar 

  14. Hamerton, A. E. (1934). Report on deaths occurring in the Society’s gardens during the year 1933. Proceedings Zoological Society of London – Yearbook, 104(2), 389–422.

    Article  Google Scholar 

  15. Hamerton, A. E. (1936). Report on the deaths occurring in the Society’s gardens during the year 1935. Proceedings Zoological Society of London – Yearbook, 106, 659–686.

    Article  Google Scholar 

  16. Hatt, J. M., & Sainsbury, A. W. (1998). Unusual case of metabolic bone disease in a common marmoset (Callithrix jacchus). Veterinary Record, 143, 78–80.

    Article  CAS  PubMed  Google Scholar 

  17. Hosey, G., Melf, V., & Pankhurst, S. (2009). Zoo animals: Behaviour, management and welfare. Oxford: Oxford University Press.

    Google Scholar 

  18. Jones, T. C., Hunt, R. D., & King, N. W. (1997). Veterinary pathology (6th ed.). Baltimore: Williams & Wilkins.

    Google Scholar 

  19. Joslin, J. O. (2003). Other primates excluding great apes. In M. E. Fowler & R. E. Miller (Eds.), Zoo and wild animal medicine (5th ed.). Philadelphia: Saunders.

    Google Scholar 

  20. Lagravere, M. O., Carey, J., Ben-Zvi, M., Packota, G. V., & Major, P. W. (2008). Effect of object location on the density measurement and Hounsfield conversion in a NewTom 3G cone beam computed tomography unit. Dentomaxillofacial Radiology, 37, 305–308.

    Article  CAS  PubMed  Google Scholar 

  21. Mah, P., Reeves, T. E., & McDavid, W. D. (2010). Deriving Hounsfield units using grey levels in cone beam computed tomography. Dentomaxillofacial Radiology, 39, 323–335.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. O’Regan, H. J., & Kitchener, A. C. (2005). The effects of captivity on the morphology of captive, domesticated and feral mammals. Mammal Review, 35, 215–230.

    Article  Google Scholar 

  23. Plesker, R., & Zwerger, C. (2002). Rickets, osteomalacia and osteoporosis in an indoor non-human primate facility. Primate Report, 62, 69–78.

    Google Scholar 

  24. Plimmer, H. G. (1910). Report on the deaths which occurred in the Zoological Gardens during 1909. Proceedings of the Zoological Society of London, 80, 131–136.

    Article  Google Scholar 

  25. Poole, K. E. S. (2006). Osteoporosis and its management. British Medical Journal, 333(7581), 1251–1256.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Rees, P. A. (2011). An introduction to zoo biology and management. Chichester: Wiley-Blackwell.

    Book  Google Scholar 

  27. Ruch, T. C. (1959). Diseases of laboratory primates. Philadelphia and London: Saunders.

    Google Scholar 

  28. Santora, L., & Skolbekken, J. A. (2011). From brittle bones to standard deviations: The historical development of osteoporosis in the late twentieth century. Science, Technology & Human Values, 36(4), 497–521.

    Article  Google Scholar 

  29. Sclater, P. L. (1870). Guide to the gardens of the Zoological Society of London (24th ed.). London: Bradbury, Evans and Co.

    Google Scholar 

  30. Seidlova-Wuttke, D. (2008). Orchidectomized (orx) marmoset (Callithrix jacchus) as a model to study the development of osteopenia/osteoporosis. American Journal of Primatology, 70(3), 294–300.

    Article  PubMed  Google Scholar 

  31. Sutton, J. B. (1884). Observations on rickets in captive and wild animals. Journal of Anatomy, 18, 363–387.

    Google Scholar 

  32. Theiler, A. (1934). Osteodystrophic disease of domesticated animals. Veterinary Journal, 90, 159–175.

    CAS  Google Scholar 

  33. Ullrey, D. E. (2003). Metabolic bone diseases. In M. E. Fowler & R. E. Miller (Eds.), Zoo and wild animal medicine: Current therapy (5th ed., pp. 749–756). Philadelphia: Elsevier (Saunders).

    Google Scholar 

  34. Vieth, R. (1999). Vitamin D supplementation, 25 hydroxyvitamin D concentrations, and safety. The American Journal of Clinical Nutrition, 69(5), 842–856.

    CAS  PubMed  Google Scholar 

  35. Wallace, M. P. (2000). Retaining natural behaviour in captivity for re-introduction programmes. In L. M. Gosling & W. J. Sutherland (Eds.), Behaviour and Conservation, Cambridge University Press: Cambridge.

  36. Williams, V. C., Lucas, J., Babcock, M. A., Gutmann, D. H., Korf, B., & Maria, B. L. (2009). Neurofibromatosis type 1 revisited. Pediatrics, 123, 124–133.

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank the following people and organizations for their contribution to this study: Dr. Andrew Kitchener (National Museum of Scotland), Dr. Sam Alberti, John Carr (Royal College of Surgeons of England), Cavendish Imaging, and the Faculty of Dental Surgery for their support. We also extend our sincere gratitude to the editor and our reviewers for their invaluable comments and suggestions.

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Correspondence to Milly Farrell.

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Farrell, M., Rando, C. & Garrod, B. Lessons from the Past: Metabolic Bone Disease in Historical Captive Primates. Int J Primatol 36, 398–411 (2015). https://doi.org/10.1007/s10764-015-9831-7

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Keywords

  • Captivity
  • Museum collections
  • Osteomalacia
  • Zoos