Environmental Geochemistry and Health

, Volume 31, Issue 1, pp 133–145 | Cite as

Spatial correlation between the prevalence of transmissible spongiform diseases and British soil geochemistry

Original Paper

Abstract

Transmissible spongiform encephalopathies (TSEs) are a group of fatal neurological conditions affecting a number of mammals, including sheep and goats (scrapie), cows (BSE), and humans (Creutzfeldt-Jakob disease). The diseases are widely believed to be caused by the misfolding of the normal prion protein to a pathological isoform, which is thought to act as an infectious agent. Outbreaks of the disease are commonly attributed to contaminated feed and genetic susceptibility. However, the implication of copper and manganese in the pathology of the disease, and its apparent geographical clustering, have prompted suggestions of a link with trace elements in the environment. Nevertheless, studies of soils at regional scales have failed to provide evidence of an environmental risk factor. This study uses geostatistical techniques to investigate the correlations between the distribution of TSE prevalence and soil geochemical variables across the UK according to different spatial scales. A similar spatial pattern in scrapie and BSE occurrence is identified, which may be linked with increasing pH and total organic carbon, and decreasing iodine concentration. However, the pattern also resembles that of the density of dairy farming. Nevertheless, despite the low spatial resolution of the TSE data available for this study, the fact that significant correlations are detected indicates there is a possibility of a link between soil geochemistry, scrapie, and BSE. It is suggested that further investigations of the prevalence of TSE and environmental exposure to trace metals should take into account the factors affecting their bioavailability.

Keywords

Transmissible spongiform diseases Soil geochemistry Scrapie BSE Geostatistics Linear model of coregionalisation Prion 

Notes

Acknowledgements

The funding for this research was provided by the European Commission project FATEPriDE (QLK4-CT2002-02723). The data on TSEs and sheep, cattle, and human populations were obtained from websites maintained by DEFRA, the National CJD Surveillance Unit, the Scottish Executive, the General Register Office for Scotland, and the Office for National Statistics. The geochemical data for Europe were kindly provided by Professor Reijo Salminen of the FORum of European GeoSurveys.

References

  1. Bastian, F. O. (2005). Spiroplasma as a candidate agent for the transmissible spongiform encephalopathies. Journal of Neuropathology and Experimental Neurology, 64, 833–838.CrossRefGoogle Scholar
  2. Brown, D. R., Wong, B. S., Hafiz, F., Clive, C., Haswell, S. J., & Jones, I. M. (1999). Normal prion protein has an activity field like that of superoxide dismutase. Biochemical Journal, 344, 1–5.CrossRefGoogle Scholar
  3. Brown, D. R., Hafiz, F., Glasssmith, L. L., Wong, B. S., Jones, I. M., Clive, C. C., et al. (2000). Consequences of manganese replacement of copper for prion protein function and proteinase resistance. EMBO Journal, 19, 1180–1186.CrossRefGoogle Scholar
  4. Brown, D. R. (2007). FATEPRIDE. SEAC 97/4. Spongiform Encephalopathy Advisory Committee. London. http://www.seac.gov.uk/agenda/agen100507.htm. (Data of last access February 1, 2008.)
  5. Broxmeyer, L. (2004). Is mad cow disease caused by a bacteria? Medical Hypotheses, 63, 731–739.CrossRefGoogle Scholar
  6. Chihota, C. M., Gravenor, M. B., & Baylis, M. (2004). Investigation of trace elements in soil as risk factors in the epidemiology of scrapie. Veterinary Record, 154, 809–813.Google Scholar
  7. DEFRA (2006a). National scrapie plan for Great Britain: scheme brochure. London: Department for Environment, Food and Rural Affairs on behalf of the GB Agriculture Departments.Google Scholar
  8. DEFRA (2006b). BSE: statistics-general statistics for GB as at 3 January 2006. www.defra.gov.uk/animalh/bse/statistics/bse/general.html. Accessed 13 February 2006.
  9. Doherr, M. G., Hett, A. R., Rüfenacht, J., Zurbriggen, A., & Heim, D. (2002). Geographical clustering of cases of bovine spongiform encephalopathy (BSE) born in Switzerland after the feed ban. Veterinary Record, 151, 467–472.Google Scholar
  10. Ebringer, A., Rashid, T., & Wilson, C. (2005). Bovine spongiform encephalopathy, multiple sclerosis, and Creutzfeld-Jakob disease are probably autoimmune diseases evoked by Acinetobacter bacteria. Autoimmunity: concepts and diagnosis at the cutting edge. Annals of the New York Academy of Sciences, 1050, 417–428.CrossRefGoogle Scholar
  11. Georgsson, G., Sigurdarson, S., & Brown, P. (2006). Infectious agent of sheep scrapie may persist in the environment for at least 16 years. Journal of General Virology, 87, 3737–3740.CrossRefGoogle Scholar
  12. Goovaerts, P. (1997). Geostatistics for natural resources evaluation. New York, Oxford: Oxford University Press.Google Scholar
  13. Gordon, I., Abdulla, E. M., Campbell, I. C., & Whatley, S. A. (1998). Phosmet induces up-regulation of surface levels of the cellular prion protein. Neuroreport, 9, 1391–1395.CrossRefGoogle Scholar
  14. Haase, B., Doherr, M. G., Seuberlich, T., Drogemuller, C., Dolf, G., Nicken, P., et al. (2007). PRNP promoter polymorphisms are associated with BSE susceptibility in Swiss and German cattle. BMC Genetics, 8, 15.CrossRefGoogle Scholar
  15. Hesketh, S., Sassoon, J., Knight, R., Hopkins, J., & Brown, D. R. (2007). Elevated manganese levels in blood and central nervous system before onset of clinical signs in scrapie and bovine spongiform encephalopathy. Journal of Animal Science, 85, 1596–1609.CrossRefGoogle Scholar
  16. Imrie, C. E., Korre, A., Munoz-Melendez, G., Thornton, I. & Durucan, S. (2008). Application of factorial kriging analysis to the FOREGS European topsoil geochemistry database. Science of the Total Environment. doi:10.1016/j.scitotenv.2007.12.012.
  17. Isaaks, E. H., & Srivastava, R. M. (1989). Applied geostatistics. New York: Oxford University Press.Google Scholar
  18. Jóhannesson, T., Gudmundsdóttir, K. B., Eiríksson, T., Kristinsson, J., & Sigurdarson, S. (2004). Selenium and GPX activity in blood samples from pregnant and non-pregnant ewes and selenium in hay on scrapie-free, scrapie-prone and scrapie-afflicted farms in Iceland. Icelandic Agricultural Sciences, 16–17, 3–13.Google Scholar
  19. Juling, K., Schwarzenbacher, H., Williams, J. L., & Fries, R. (2006). A major genetic component of BSE susceptibility. BMC Biology, 4, 33.CrossRefGoogle Scholar
  20. Kabata-Pendias, A. (2001). Trace elements in soils and plants, 3rd edn. Florida: CRC Press.Google Scholar
  21. Manuelidis, L. (2007). A 25 nm virion is the likely cause of transmissible spongiform encephalopathies. Journal of Cellular Biochemistry, 100, 897–915.CrossRefGoogle Scholar
  22. McBride, M. B. (2007). Trace metals and sulfur in soils and forage of a chronic wasting disease locus. Environmental Chemistry, 4, 134–139.CrossRefGoogle Scholar
  23. National CJD Surveillance Unit (2005). Creutzfeld-Jakob disease surveillance in the UK: thirteenth annual report 2004. Edinburgh: National CJD Surveillance Unit.Google Scholar
  24. National CJD Surveillance Unit (2007). Creutzfeld-Jakob disease surveillance in the UK: fifteenth annual report 2006. Edinburgh: National CJD Surveillance Unit.Google Scholar
  25. Prusiner, S. B. (1982). Novel proteinaceous infectious particles cause scrapie. Science, 216, 136–144.CrossRefGoogle Scholar
  26. Purdey, M. (1998). High-dose exposure to systemic phosmet insecticide modifies the phosphatidylinositol anchor on the prion protein: the origins of new variant transmissible spongiform encephalopathies? Medical Hypotheses, 50, 91–111.CrossRefGoogle Scholar
  27. Purdey, M. (2000). Ecosystems supporting clusters of sporadic TSEs demonstrate excesses of the radical-generating divalent cation manganese and deficiencies of antioxidant co-factors Co, Se, Fe Zn-does a foreign cation substitution at prion protein’s Cu domain initiate TSE? Medical Hypotheses, 54, 278–306.CrossRefGoogle Scholar
  28. Ragnarsdottir, K. V., & Hawkins, D. P. (2006). Bioavailable copper and manganese in soils from Iceland and their relationship with scrapie occurrence in sheep. Journal of Geochemical Exploration, 88, 228–234.CrossRefGoogle Scholar
  29. Salminen, R., Tarvainen, T., Demetriades, A., Duris, M., Fordyce, F. M., Gregorauskiene, V., et al. (1998). FOREGS geochemical mapping field manual. Espoo: Geological Survey of Finland.Google Scholar
  30. Salminen, R. (Chief-editor), Batista, M. J., Bidovec, M., Demetriades, A., De Vivo, B., De Vos, W., Duris, M., Gilucis, A., Gregorauskiene, V., Halamic, J., Heitzmann, P., Lima, A., Jordan, G., Klaver, G., Klein, P., Lis, J., Locutura, J., Marsina, K., Mazreku, A., O’Connor, P. J., Olsson, S. Ǻ., Ottersen, R. T., Petersell, V., Plant, J. A., Reeder, S., Salpeteur, I., Sandström, H., Siewers, U., Steenfelt, A. & Tarvainen, T. (2005). Geochemical atlas of Europe, Part 1: Background information, methodology and maps. Espoo: Geological Survey of Finland.Google Scholar
  31. Sigurdarson, S. (2000). Scrapie or “rida” in Iceland. Norsk Veterinarisk Tidskift, 112, 408–413 (in Norwegian).Google Scholar
  32. Stevenson, M. A., Morris, R. S., Lawson, A. B., Wilesmith, J. W., Ryan, J. B. M., & Jackson, R. (2005). Area-level risks for BSE in British cattle before and after the July 1998 meat and bone meal feed ban. Preventative Veterinary Medicine, 69, 129–144.CrossRefGoogle Scholar
  33. Tongue, S. C., Pfeiffer, D. U., & Wilesmith, J. W. (2006). Descriptive spatial analysis of scrapie-affected flocks in Great Britain between January 1993 and December 2002. Veterinary Record, 159, 165–170.Google Scholar
  34. Wackernagel, H. (1998). Multivariate geostatistics, 2nd edn. Berlin: Springer-Verlag.Google Scholar
  35. Wong, B. S., Chen, S. G., Colucci, M., Xie, Z., Pan, T., Lui, T., et al. (2001). Aberrant metal binding by prion protein in human prion disease. Journal of Neurochemistry, 78, 1400–1408.CrossRefGoogle Scholar
  36. Zeng, F., Watt, N. T., Walmsley, A. R., & Hooper, N. M. (2003). Tethering the N-terminus of the prion protein compromises the cellular response to oxidative stress. Journal of Neurochemistry, 84, 480–490.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.Department of Earth Science and EngineeringImperial College LondonLondonUK

Personalised recommendations