Skip to main content
Log in

Biochemical identification of bovine spongiform encephalopathies in cattle

  • Original Paper
  • Published:
Acta Neuropathologica Aims and scope Submit manuscript

Abstract

Important changes have occurred in the post-mortem diagnosis of bovine spongiform encephalopathy (BSE) in recent years. We have evaluated a commercially available Western blot method (TeSeE® Wb) as a potential means of confirming BSE. This method was (i) highly sensitive, compared with a biochemical confirmatory Western blot method (AFSSA-Wb) previously used in France and (ii) more sensitive than two routinely used highly sensitive rapid tests (TeSeE® ELISA, HerdCheck® BSE). We show that this high sensitivity is mainly due to the antibody used (Sha31). Interestingly, TeSeE® Wb was also able to diagnose the two currently recognised deviant BSE phenotypes (H-type and L-type or BASE). The initially described molecular features of these atypical forms of BSE were also readily recognised, although sensitivity of the method may be differently affected by the chosen Ab compared with typical BSE. This method is thus of potential interest for future evaluations of BSE confirmatory methods.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Abrial D, Calavas D, Jarrige N, Ducrot C (2005) Spatial heterogeneity of the risk of BSE in France following the ban of meat and bone meal in cattle feed. Prev Vet Med 6:69–82

    Article  Google Scholar 

  2. Baron T, Biacabe AG (2006) Origin of bovine spongiform encephalopathy. Lancet 36:297–298. Author reply 298–299

    Article  Google Scholar 

  3. Baron T, Biacabe AG, Arsac JN, Benestad S, Groschup MH (2006) Atypical transmissible spongiform encephalopathies (TSEs) in ruminants. Vaccine 25:5625–5630

    Article  PubMed  CAS  Google Scholar 

  4. Beekes M, Baldauf E, Cassens S, Diringer H, Keyes P, Scott AC, Wells GA, Brown P, Gibbs CJ Jr, Gajdusek DC (1995) Western blot mapping of disease-specific amyloid in various animal species and humans with transmissible spongiform encephalopathies using a high-yield purification method. J Gen Virol 76(Pt 10):2567–2576

    Article  PubMed  CAS  Google Scholar 

  5. Bencsik AA, Debeer SO, Baron TG (2005) An alternative pretreatment procedure in animal transmissible spongiform encephalopathies diagnosis using PrPsc immunohistochemistry. J Histochem Cytochem 5:1199–1202

    Article  CAS  Google Scholar 

  6. Beringue V, Bencsik A, Le Dur A, Reine F, Lai TL, Chenais N, Tilly G, Biacabe AG, Baron T, Vilotte JL, Laude H (2006) Isolation from cattle of a prion strain distinct from that causing bovine spongiform encephalopathy. PLoS Pathog 2:e112

    Article  PubMed  CAS  Google Scholar 

  7. Biacabe AG, Laplanche JL, Ryder S, Baron T (2004) Distinct molecular phenotypes in bovine prion diseases. EMBO Rep 5:110–115

    Article  PubMed  CAS  Google Scholar 

  8. Biacabe AG, Jacobs JG, Bencsik A, Langeveld JP, Baron T (2007) H-type bovine spongiform encephalopathy: complex molecular features and similarities with human prion diseases. Prion 1:61–68

    PubMed  Google Scholar 

  9. Bird SM (2003) European Union’s rapid TSE testing in adult cattle and sheep: implementation and results in 2001 and 2002. Stat Methods Med Res 1:261–278

    Article  Google Scholar 

  10. Bolton DC, McKinley MP, Prusiner SB (1982) Identification of a protein that purifies with the scrapie prion. Science 21:1309–1311

    Article  Google Scholar 

  11. Brown P, McShane LM, Zanusso G, Detwiler L (2006) On the question of sporadic or atypical bovine spongiform encephalopathy and Creutzfeldt–Jakob Disease. Emerg Inf Dis 12:1816–1821

    Google Scholar 

  12. Bruce ME, Will RG, Ironside JW, McConnell I, Drummond D, Suttie A, McCardle L, Chree A, Hope J, Birkett C, Cousens S, Fraser H, Bostock CJ (1997) Transmissions to mice indicate that ‘new variant’ CJD is caused by the BSE agent. Nature 38:498–501

    Article  CAS  Google Scholar 

  13. Buschmann A, Gretzschel A, Biacabe AG, Schiebel K, Corona C, Hoffmann C, Eiden M, Baron T, Casalone C, Groschup MH (2006) Atypical BSE in Germany-Proof of transmissibility and biochemical characterization. Vet Microbiol 117:103–116

    Article  PubMed  CAS  Google Scholar 

  14. Calavas D, Ducrot C, Baron TG (2004) Past, present and future of bovine spongiform encephalopathy in France. Curr Top Microbiol Immunol 28:51–63

    Google Scholar 

  15. Casalone C, Zanusso G, Acutis P, Ferrari S, Capucci L, Tagliavini F, Monaco S, Caramelli M (2004) Identification of a second bovine amyloidotic spongiform encephalopathy: molecular similarities with sporadic Creutzfeldt–Jakob disease. Proc Natl Acad Sci USA 10:3065–3070

    Article  CAS  Google Scholar 

  16. Chaplin MJ, Barlow N, Ryder S, Simmons MM, Spencer Y, Hughes R, Stack MJ (2002) Evaluation of the effects of controlled autolysis on the immunodetection of PrP(Sc) by immunoblotting and immunohistochemistry from natural cases of scrapie and BSE. Res Vet Sci 7:37–43

    Article  Google Scholar 

  17. Chesebro B, Race R, Wehrly K, Nishio J, Bloom M, Lechner D, Bergstrom S, Robbins K, Mayer L, Keith JM, Garon C, Haase A (1985) Identification of scrapie prion protein-specific mRNA in scrapie-infected and uninfected brain. Nature 31:331–333

    Article  Google Scholar 

  18. Collinge J, Rossor M (1996) A new variant of prion disease. Lancet 34:916–917

    Article  Google Scholar 

  19. Cooley WA, Clark JK, Stack MJ (1998) Comparison of scrapie-associated fibril detection and Western immunoblotting for the diagnosis of natural ovine scrapie. J Comp Pathol 11:41–49

    Article  Google Scholar 

  20. Cooley WA, Clark JK, Ryder SJ, Davis LA, Farrelly SS, Stack MJ (2001) Evaluation of a rapid western immunoblotting procedure for the diagnosis of bovine spongiform encephalopathy (BSE) in the UK. J Comp Pathol 12:64–70

    Article  Google Scholar 

  21. Debeer SO, Baron TG, Bencsik AA (2001) Immunohistochemistry of PrPsc within bovine spongiform encephalopathy brain samples with graded autolysis. J Histochem Cytochem 4:1519–1524

    Google Scholar 

  22. Debeer SO, Baron TG, Bencsik AA (2002) Transmissible spongiform encephalopathy diagnosis using PrPsc immunohistochemistry on fixed but previously frozen brain samples. J Histochem Cytochem 5:611–616

    Google Scholar 

  23. Deslys JP, Comoy E, Hawkins S, Simon S, Schimmel H, Wells G, Grassi J, Moynagh J (2001) Screening slaughtered cattle for BSE. Nature 40:476–478

    Article  Google Scholar 

  24. Deslys JP, Grassi J (2005) [Screening tests for animal TSE: present and future]. Pathol Biol (Paris) 5:221–228

    Google Scholar 

  25. European Commission (1999) The evaluation of tests for the diagnosis of transmissible spongiform encephalopathy in bovines. http://europa.eu.int/comm/food/fs/bse/bse12_en.pdf

  26. European Commission (2002) The evaluation of five rapid tests for the diagnosis of transmissible spongiform encephalopathy in bovines (2nd study). http://europa.eu.int/comm/food/fs/bse/bse42_en.pdf

  27. Farquhar CF, Somerville RA, Ritchie LA (1989) Post-mortem immunodiagnosis of scrapie and bovine spongiform encephalopathy. J Virol Methods 2:215–221

    Article  Google Scholar 

  28. Feraudet C, Morel N, Simon S, Volland H, Frobert Y, Creminon C, Vilette D, Lehmann S, Grassi J (2005) Screening of 145 anti-PrP monoclonal antibodies for their capacity to inhibit PrPSc replication in infected cells. J Biol Chem 28:11247–11258

    Article  CAS  Google Scholar 

  29. Grassi J (2003) Pre-clinical diagnosis of transmissible spongiform encephalopathies using rapid tests. Transfus Clin Biol 1:19–22

    Article  Google Scholar 

  30. Grassi J, Comoy E, Simon S, Creminon C, Frobert Y, Trapmann S, Schimmel H, Hawkins SA, Moynagh J, Deslys JP, Wells GA (2001) Rapid test for the preclinical postmortem diagnosis of BSE in central nervous system tissue. Vet Rec 14:577–582

    Google Scholar 

  31. Haritani M, Spencer YI, Wells GA (1994) Hydrated autoclave pretreatment enhancement of prion protein immunoreactivity in formalin-fixed bovine spongiform encephalopathy-affected brain. Acta Neuropathol (Berl) 8:86–90

    Google Scholar 

  32. Hill AF, Desbruslais M, Joiner S, Sidle KC, Gowland I, Collinge J, Doey LJ, Lantos P (1997) The same prion strain causes vCJD and BSE. Nature 38:448–450

    Article  CAS  Google Scholar 

  33. Jacobs JG, Langeveld JP, Biacabe AG, Acutis PL, Polak MP, Gavier-Widen D, Buschmann A, Caramelli M, Casalone C, Mazza M, Groschup M, Erkens JH, Davidse A, van Zijderveld FG, Baron T (2007) Molecular discrimination of atypical bovine spongiform encephalopathy strains from a geographical region spanning a wide area in europe. J Clin Microbiol 4:1821–1829

    Article  CAS  Google Scholar 

  34. Katz JB, Pedersen JC, Jenny AL, Taylor WD (1992) Assessment of western immunoblotting for the confirmatory diagnosis of ovine scrapie and bovine spongiform encephalopathy (BSE). J Vet Diagn Invest 4:447–449

    PubMed  CAS  Google Scholar 

  35. Madec JY, Groschup MH, Buschmann A, Belli P, Calavas D, Baron T (1998) Sensitivity of the Western blot detection of prion protein PrPres in natural sheep scrapie. J Virol Methods 7:169–177

    Article  Google Scholar 

  36. Madec JY, Belli P, Calavas D, Baron T (2000) Efficiency of Western blotting for the specific immunodetection of proteinase K-resistant prion protein in BSE diagnosis in France. Vet Rec 14:74–76

    Google Scholar 

  37. Oesch B, Westaway D, Walchli M, McKinley MP, Kent SB, Aebersold R, Barry RA, Tempst P, Teplow DB, Hood LE, Prusiner SB, Weissmann C (1985) A cellular gene encodes scrapie PrP 27–30 protein. Cell 4:735–746

    Article  Google Scholar 

  38. OIE (2004) Bovine Spogiform Encephalopathy, Manual of Diagnostic tests and Vaccines for Terrestrial Animals. Office International des Epizooties update 23.07.2004

  39. Richt JA, kunkle RA, Alt D, Nicholson EM, Hamir AN, Czub S, Kluge J, Davis AJ, Hall SM (2007) Identification and characterization of two bovine spongiform encephalopathy cases diagnosed in the United States. J Vet Diagn Invest 19:142–154

    PubMed  Google Scholar 

  40. Schaller O, Fatzer R, Stack M, Clark J, Cooley W, Biffiger K, Egli S, Doherr M, Vandevelde M, Heim D, Oesch B, Moser M (1999) Validation of a western immunoblotting procedure for bovine PrP(Sc) detection and its use as a rapid surveillance method for the diagnosis of bovine spongiform encephalopathy (BSE). Acta Neuropathol (Berl) 9:437–443

    Article  Google Scholar 

  41. Seuberlich T (2006) Spongiform encephalopathy in a miniature zebu. Emerg Infect Dis 1:1950–1953

    Google Scholar 

  42. Supervie V, Costagliola D (2004) The unrecognised French BSE epidemic. Vet Res 3:349–362

    Article  Google Scholar 

  43. Supervie V, Costagliola D (2006) How was the French BSE epidemic underestimated? C R Biol 32:106–116

    Google Scholar 

  44. van Keulen LJ, Schreuder BE, Meloen RH, Poelen-van den Berg M, Mooij-Harkes G, Vromans ME, Langeveld JP (1995) Immunohistochemical detection and localization of prion protein in brain tissue of sheep with natural scrapie. Vet Pathol 3:299–308

    Article  Google Scholar 

  45. Vidal E, Marquez M, Ordonez M, Raeber AJ, Struckmeyer T, Oesch B, Siso S, Pumarola M (2005) Comparative study of the PrPBSE distribution in brains from BSE field cases using rapid tests. J Virol Methods 12:24–32

    Google Scholar 

  46. Vidal E, Marquez M, Tortosa R, Costa C, Serafin A, Pumarola M (2006) Immunohistochemical approach to the pathogenesis of bovine spongiform encephalopathy in its early stages. J Virol Methods 13:15–29

    Article  CAS  Google Scholar 

  47. Wells GA, Scott AC, Johnson CT, Gunning RF, Hancock RD, Jeffrey M, Dawson M, Bradley R (1987) A novel progressive spongiform encephalopathy in cattle. Vet Rec 12:419–420

    Google Scholar 

  48. Wells GA, Hancock RD, Cooley WA, Richards MS, Higgins RJ, David GP (1989) Bovine spongiform encephalopathy: diagnostic significance of vacuolar changes in selected nuclei of the medulla oblongata. Vet Rec 12:521–524

    Google Scholar 

  49. Wells GA, Spencer YI, Haritani M (1994) Configurations and topographic distribution of PrP in the central nervous system in bovine spongiform encephalopathy: an immunohistochemical study. Ann N Y Acad Sci 72:350–352

    Article  Google Scholar 

  50. Will RG, Ironside JW, Zeidler M, Cousens SN, Estibeiro K, Alperovitch A, Poser S, Pocchiari M, Hofman A, Smith PG (1996) A new variant of Creutzfeldt–Jakob disease in the UK. Lancet 34:921–925

    Article  Google Scholar 

  51. Yamakawa Y, Hagiwara K, Nohtomi K, Nakamura Y, Nishijima M, Higuchi Y, Sato Y, Sata T (2003) Atypical proteinase K-resistant prion protein (PrPres) observed in an apparently healthy 23-month-old Holstein steer. Jpn J Infect Dis 5:221–221

    Google Scholar 

Download references

Acknowledgments

The authors are grateful to J-M. Bilheude for his technical support and helpful discussions. We also wish to thank M. Lavoine for her excellent technical assistance. This work was partly supported by NEUROPRION European network of excellence (EUROSTRAINS project).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thierry Baron.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Arsac, JN., Biacabe, AG., Nicollo, J. et al. Biochemical identification of bovine spongiform encephalopathies in cattle. Acta Neuropathol 114, 509–516 (2007). https://doi.org/10.1007/s00401-007-0270-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00401-007-0270-1

Keywords

Navigation