1887

Abstract

Transmissible spongiform encephalopathies or prion diseases comprise diseases with different levels of contagiousness under natural conditions. The hypothesis has been raised that the chronic wasting disease (CWD) cases detected in Nordic moose () may be less contagious, or not contagious between live animals under field conditions. This study aims to investigate the epidemiology of CWD cases detected in moose in Norway, Sweden and Finland using surveillance data from 2016 to 2022.

In total, 18 CWD cases were detected in Nordic moose. All moose were positive for prion (PrP) detection in the brain, but negative in lymph nodes, all were old (mean 16 years; range 12–20) and all except one, were female. Age appeared to be a strong risk factor, and the sex difference may be explained by few males reaching high age due to hunting targeting calves, yearlings and males.

The cases were geographically scattered, distributed over 15 municipalities. However, three cases were detected in each of two areas, Selbu in Norway and Arjeplog-Arvidsjaur in Sweden. A Monte Carlo simulation approach was applied to investigate the likelihood of such clustering occurring by chance, given the assumption of a non-contagious disease. The empirical -value for obtaining three cases in one Norwegian municipality was less than 0.05, indicating clustering. However, the moose in Selbu were affected by different CWD strains, and over a 6 year period with intensive surveillance, the apparent prevalence decreased, which would not be expected for an ongoing outbreak of CWD. Likewise, the three cases in Arjeplog-Arvidsjaur could also indicate clustering, but management practices promotes a larger proportion of old females and the detection of the first CWD case contributed to increased awareness and sampling.

The results of our study show that the CWD cases detected so far in Nordic moose have a different epidemiology compared to CWD cases reported from North America and in Norwegian reindeer (). The results support the hypothesis that these cases are less contagious or not contagious between live animals under field conditions. To enable differentiation from other types of CWD, we support the use of sporadic CWD (sCWD) among the names already in use.

Funding
This study was supported by the:
  • Miljødirektoratet (Award 22087484)
    • Principle Award Recipient: ChristerMoe Rolandsen
  • Miljødirektoratet (Award 17070060)
    • Principle Award Recipient: ChristerMoe Rolandsen
  • Veterinærinstituttets (Award 12081)
    • Principle Award Recipient: JørnVåge
  • ICRAD (Award 322907)
    • Principle Award Recipient: Lafond BenestadSylvie
  • Research Council of Norway, NVI Open Access publishing fund (Award OA2023-20)
    • Principle Award Recipient: HoppPetter
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001952
2024-01-24
2024-05-04
Loading full text...

Full text loading...

/deliver/fulltext/jgv/105/1/jgv001952.html?itemId=/content/journal/jgv/10.1099/jgv.0.001952&mimeType=html&fmt=ahah

References

  1. Gambetti P, Cali I. Human sporadic prion diseases. In Zou WQ, Gambetti P. eds Prions and Diseases Cham, Switzerland: Springer; 2023 pp 353–373 [View Article]
    [Google Scholar]
  2. Acín C, Bolea R, Monzón M, Monleón E, Moreno B et al. Classical and atypical scrapie in sheep and goats. Review on the etiology, genetic factors, pathogenesis, diagnosis, and control measures of both diseases. Animals 2021; 11:691 [View Article] [PubMed]
    [Google Scholar]
  3. Fediaevsky A, Tongue SC, Nöremark M, Calavas D, Ru G et al. A descriptive study of the prevalence of atypical and classical scrapie in sheep in 20 European countries. BMC Vet Res 2008; 4:19 [View Article] [PubMed]
    [Google Scholar]
  4. Gallardo MJ, Delgado FO. Animal prion diseases: a review of intraspecies transmission. Open Vet J 2021; 11:707–723 [View Article] [PubMed]
    [Google Scholar]
  5. Hoinville LJ. A review of the epidemiology of scrapie in sheep. Rev Sci Tech 1996; 15:827–852 [View Article] [PubMed]
    [Google Scholar]
  6. Wilesmith JW, Wells GAH, Cranwell MP, Ryan JBM. Bovine spongiform encephalopathy: epidemiological studies. Vet Rec 1988; 123:638–644 [View Article] [PubMed]
    [Google Scholar]
  7. Will RG, Ironside JW, Zeidler M, Cousens SN, Estibeiro K et al. A new variant of Creutzfeldt-Jakob disease in the UK. Lancet 1996; 347:921–925 [View Article] [PubMed]
    [Google Scholar]
  8. European Commission No 999/2001 of the European Parliament and of the Council of 22 May 2001 laying down rules for the prevention, control and eradication of certain transmissible spongiform encephalopathies. Off J Eur Communities 2001; 2001:1–40
    [Google Scholar]
  9. Benestad SL, Sarradin P, Thu B, Schönheit J, Tranulis MA et al. Cases of scrapie with unusual features in Norway and designation of a new type, Nor98. Vet Rec 2003; 153:202–208 [View Article] [PubMed]
    [Google Scholar]
  10. Biacabe AG, Laplanche JL, Ryder S, Baron T. Distinct molecular phenotypes in bovine prion diseases. EMBO Rep 2004; 5:110–114 [View Article] [PubMed]
    [Google Scholar]
  11. Casalone C, Zanusso G, Acutis P, Ferrari S, Capucci L et al. Identification of a second bovine amyloidotic spongiform encephalopathy: molecular similarities with sporadic Creutzfeldt-Jakob disease. Proc Natl Acad Sci U S A 2004; 101:3065–3070 [View Article] [PubMed]
    [Google Scholar]
  12. Greenlee JJ, Smith JD, West Greenlee MH, Nicholson EM. Clinical and pathologic features of H-type bovine spongiform encephalopathy associated with E211K prion protein polymorphism. PLoS One 2012; 7:e38678 [View Article] [PubMed]
    [Google Scholar]
  13. European Food Safety Authority (EFSA) The European Union summary report on surveillance for the presence of transmissible spongiform encephalopathies (TSE) in 2021. EFSA J 2022; 20:e07655 [View Article] [PubMed]
    [Google Scholar]
  14. World Organisation for Animal Health Scrapie. Terrestrial animal health code series vol. Chapter 14.8; 2022 https://www.woah.org/fileadmin/Home/eng/Health_standards/tahc/2023/chapitre_scrapie.pdf
  15. World Organisation for Animal Health Paris: World Organisation for Animal Health; 2023 https://www.woah.org/fileadmin/Home/eng/Health_standards/tahc/2023/chapitre_bse.pdf
  16. Williams ES, Young S. Chronic wasting disease of captive mule deer: a spongiform encephalopathy. J Wildl Dis 1980; 16:89–98 [View Article] [PubMed]
    [Google Scholar]
  17. Benestad SL, Mitchell G, Simmons M, Ytrehus B, Vikøren T. First case of chronic wasting disease in Europe in a Norwegian free-ranging reindeer. Vet Res 2016; 47:88 [View Article] [PubMed]
    [Google Scholar]
  18. Pirisinu L, Tran L, Chiappini B, Vanni I, Di Bari MA et al. Novel type of chronic wasting disease detected in Moose (Alces alces), Norway. Emerg Infect Dis 2018; 24:2210–2218 [View Article] [PubMed]
    [Google Scholar]
  19. European Commission Commission regulation (EU) 2017/1972 of 30 October 2017 amending Annexes I and III to regulation (EC) no 999/2001 of the European Parliament and of the council as regards a surveillance programme for chronic wasting disease in Cervids in Estonia, Finland, Latvia, Lithuania, Poland and Sweden and repealing Commission decision 2007/182/EC. Off J Eur Union 2017; 281:14–20
    [Google Scholar]
  20. Vikøren T, Våge J, Madslien KI, Røed KH, Rolandsen CM et al. First detection of chronic wasting disease in a wild red deer (Cervus elaphus) in Europe. J Wildl Dis 2019; 55:970–972 [View Article] [PubMed]
    [Google Scholar]
  21. Jensen WF, Rea RV, Penner CE, Jason R, Smith JR et al. A review of circumpolar moose populations with emphasis on Eurasian moose distribution and densities. Alces 2020; 56:63–78
    [Google Scholar]
  22. Bunnefeld N, Börger L, van Moorter B, Rolandsen CM, Dettki H et al. A model-driven approach to quantify migration patterns: individual, regional and yearly differences. J Anim Ecol 2011; 80:466–476 [View Article] [PubMed]
    [Google Scholar]
  23. van Moorter B, Singh NJ, Rolandsen CM, Solberg EJ, Dettki H et al. Seasonal release from competition explains partial migration in European moose. Oikos 2021; 130:1548–1561 [View Article]
    [Google Scholar]
  24. Lavsund S, Nygren T, Solberg EJ. Status of moose populations and challenges to moose management in Fennoscandia. Alces 2003; 39:109–130
    [Google Scholar]
  25. Ericsson G, Wallin K. Age-specific moose (Alces alces) mortality in apredator-free environment: evidence for senescence in females. Écoscience 2001; 8:157–163 [View Article]
    [Google Scholar]
  26. Ericsson G, Wallin K, Ball JP, Broberg M. Age-related reproductive effort and senescence in free-ranging moose, Alces alces. Ecology 2001; 82:1613–1620 [View Article]
    [Google Scholar]
  27. Rolandsen CM, Våge J, Hopp P, Benestad SL, Mysterud A et al. Kartlegging av skrantesjuke (CWD) i 2016 og 2017. Rapport: Norsk institutt for naturforskning (NINA)2018; 2016 http://hdl.handle.net/11250/2504005
  28. Koutsoumanis K, Allende A, Alvarez-Ordoñez A, Bolton D et al.EFSA Panel on Biological Hazards Monitoring of chronic wasting disease (CWD) (IV). EFSA J 2023; 21:e07936 [View Article] [PubMed]
    [Google Scholar]
  29. Rolandsen CM, Solberg EJ, Heim M, Holmstrøm F, Solem MI et al. Accuracy and repeatability of moose (Alces alces) age as estimated from dental cement layers. Eur J Wildl Res 2008; 54:6–14 [View Article]
    [Google Scholar]
  30. Veiberg V, Nilsen EB, Rolandsen CM, Heim M, Andersen R et al. The accuracy and precision of age determination by dental cementum annuli in four northern cervids. Eur J Wildl Res 2020; 66: [View Article]
    [Google Scholar]
  31. Moazami-Goudarzi K, Andréoletti O, Vilotte J-L, Béringue V. Review on PRNP genetics and susceptibility to chronic wasting disease of Cervidae. Vet Res 2021; 52:128 [View Article] [PubMed]
    [Google Scholar]
  32. R Core Team R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2022 https://www.R-project.org
  33. North BV, Curtis D, Sham PC. A note on the calculation of empirical P values from Monte Carlo procedures. Am J Hum Genet 2002; 71:439–441 [View Article] [PubMed]
    [Google Scholar]
  34. Lüdecke D. ggeffects: tidy data frames of marginal effects from regression models. J Open Source Softw 2018; 3:772 [View Article]
    [Google Scholar]
  35. Sola D, Tran L, Våge J, Madslien K, Vuong TT et al. Heterogeneity of pathological prion protein accumulation in the brain of moose (Alces alces) from Norway, Sweden and Finland with chronic wasting disease. Vet Res 2023; 54:74 [View Article] [PubMed]
    [Google Scholar]
  36. Mysterud A, Madslien K, Viljugrein H, Vikøren T, Andersen R et al. The demographic pattern of infection with chronic wasting disease in reindeer at an early epidemic stage. Ecosphere 2019; 10:11 [View Article]
    [Google Scholar]
  37. Heisey DM, Osnas EE, Cross PC, Joly DO, Langenberg JA et al. Linking process to pattern: estimating spatiotemporal dynamics of a wildlife epidemic from cross‐sectional data. Ecol Monogr 2010; 80:221–240 [View Article]
    [Google Scholar]
  38. Samuel MD, Storm DJ. Chronic wasting disease in white-tailed deer: infection, mortality, and implications for heterogeneous transmission. Ecology 2016; 97:3195–3205 [View Article] [PubMed]
    [Google Scholar]
  39. Miller MW, Conner MM. Epidemiology of chronic wasting disease in free-ranging mule deer: spatial, temporal, and demographic influences on observed prevalence patterns. J Wildl Dis 2005; 41:275–290 [View Article] [PubMed]
    [Google Scholar]
  40. Rees EE, Merrill EH, Bollinger TK, Hwang YT, Pybus MJ et al. Targeting the detection of chronic wasting disease using the hunter harvest during early phases of an outbreak in Saskatchewan, Canada. Prev Vet Med 2012; 104:149–159 [View Article] [PubMed]
    [Google Scholar]
  41. Rogers W, Brandell EE, Cross PC. Epidemiological differences between sexes affect management efficacy in simulated chronic wasting disease systems. J Appl Ecol 2022; 59:1122–1133 [View Article]
    [Google Scholar]
  42. Rolandsen CM, Våge J, Hopp P, Benestad SL, Viljugrein H et al. Kartlegging av skrantesjuke (CWD) i 2016-2018. Rapport: Norsk institutt for naturforskning (NINA)/Veterinærinstituttet2019; 2019 http://hdl.handle.net/11250/2618282
  43. Rolandsen CM, Våge J, Hopp P, Benestad SL, Viljugrein H et al. Kartlegging og overvåking av skrantesjuke (chronic wasting disease - CWD) 2021. Rapport: Norsk institutt for naturforskning (NINA) og Veterinærinstituttet (VI)2022; 2021 https://hdl.handle.net/11250/3000616
  44. Bian J, Kim S, Kane SJ, Crowell J, Sun JL et al. Adaptive selection of a prion strain conformer corresponding to established North American CWD during propagation of novel emergent Norwegian strains in mice expressing elk or deer prion protein. PLoS Pathog 2021; 17:e1009748 [View Article] [PubMed]
    [Google Scholar]
  45. Nonno R, Di Bari MA, Pirisinu L, D’Agostino C, Vanni I et al. Studies in bank voles reveal strain differences between chronic wasting disease prions from Norway and North America. Proc Natl Acad Sci U S A 2020; 117:31417–31426 [View Article] [PubMed]
    [Google Scholar]
  46. Belsare AV, Millspaugh JJ, Mason JR, Sumners J, Viljugrein H et al. Getting in front of chronic wasting disease: model-informed proactive approach for managing an emerging wildlife disease. Front Vet Sci 2020; 7:608235 [View Article] [PubMed]
    [Google Scholar]
  47. Tranulis MA, Tryland M. The zoonotic potential of chronic wasting disease-a review. Foods 2023; 12:824 [View Article] [PubMed]
    [Google Scholar]
  48. Osnas EE, Heisey DM, Rolley RE, Samuel MD. Spatial and temporal patterns of chronic wasting disease: fine-scale mapping of a wildlife epidemic in Wisconsin. Ecol Appl 2009; 19:1311–1322 [View Article] [PubMed]
    [Google Scholar]
  49. Baeten LA, Powers BE, Jewell JE, Spraker TR, Miller MW. A natural case of chronic wasting disease in a free-ranging moose (Alces alces shirasi). J Wildl Dis 2007; 43:309–314 [View Article] [PubMed]
    [Google Scholar]
  50. Goldmann W, Hunter N, Foster JD, Salbaum JM, Beyreuther K et al. Two alleles of a neural protein gene linked to scrapie in sheep. Proc Natl Acad Sci U S A 1990; 87:2476–2480 [View Article] [PubMed]
    [Google Scholar]
  51. Moum T, Olsaker I, Hopp P, Moldal T, Valheim M et al. Polymorphisms at codons 141 and 154 in the ovine prion protein gene are associated with scrapie Nor98 cases. J Gen Virol 2005; 86:231–235 [View Article] [PubMed]
    [Google Scholar]
  52. Robinson SJ, Samuel MD, Johnson CJ, Adams M, McKenzie DI. Emerging prion disease drives host selection in a wildlife population. Ecol Appl 2012; 22:1050–1059 [View Article] [PubMed]
    [Google Scholar]
  53. Monello RJ, Galloway NL, Powers JG, Madsen-Bouterse SA, Edwards WH et al. Pathogen-mediated selection in free-ranging elk populations infected by chronic wasting disease. Proc Natl Acad Sci U S A 2017; 114:12208–12212 [View Article] [PubMed]
    [Google Scholar]
  54. Wik L, Mikko S, Klingeborn M, Steen M, Simonsson M et al. Polymorphisms and variants in the prion protein sequence of European moose (Alces alces), reindeer (Rangifer tarandus), roe deer (Capreolus capreolus) and fallow deer (Dama dama) in Scandinavia. Prion 2012; 6:256–260 [View Article]
    [Google Scholar]
  55. Güere ME, Våge J, Tharaldsen H, Kvie KS, Bårdsen B-J et al. Chronic wasting disease in Norway-a survey of prion protein gene variation among cervids. Transbound Emerg Dis 2022; 69:e20–e31 [View Article] [PubMed]
    [Google Scholar]
  56. World Organisation for Animal Health Scrapie. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 2022 series vol. Chapter 3.8.11): World Organisation for Animal Health; 2022 https://www.woah.org/fileadmin/Home/eng/Health_standards/tahm/3.08.11_SCRAPIE.pdf
  57. Prince MJ, Bailey JA, Barrowman PR, Bishop KJ, Campbell GR et al. Bovine spongiform encephalopathy. Rev Sci Tech 2003; 22:37–60 [View Article] [PubMed]
    [Google Scholar]
  58. World Organisation for Animal Health Bovine spongiform encephalopathy (version adopted in May 2021). Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 2021 series vol. Chapter 3.4.5): World Organisation for Animal Health; 2021 https://www.woah.org/fileadmin/Home/eng/Health_standards/tahm/3.04.05_BSE.pdf
  59. Argue CK, Ribble C, Lees VW, McLane J, Balachandran A. Epidemiology of an outbreak of chronic wasting disease on elk farms in Saskatchewan. In Canadian Veterinary Journal-Revue Veterinaire Canadienne vol 48 2007 pp 1241–1248
    [Google Scholar]
  60. Monello RJ, Powers JG, Hobbs NT, Spraker TR, Watry MK et al. Survival and population growth of a free‐ranging elk population with a long history of exposure to chronic wasting disease. J Wildl Manag 2014; 78:214–223 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001952
Loading
/content/journal/jgv/10.1099/jgv.0.001952
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error