1887
  1. Home
  2. Eurosurveillance
  3. Volume 28, Issue 50, 14/Dec/2023
  4. Article
Surveillance Open Access
Like 0
Download

Abstract

Background

Prion diseases are rare, fatal disorders that have repeatedly raised public health concerns since the early 1990s. An active prion disease surveillance network providing national level data was implemented in France in 1992.

Aim

We aimed to describe the epidemiology of sporadic, genetic and infectious forms of prion diseases in France since surveillance implementation.

Methods

We included all suspected cases notified from January 1992 to December 2016, and cases who died during the period with a definite or probable prion disease diagnosis according to EuroCJD criteria. Demographic, clinical, genetic, neuropathological and biochemical data were collected.

Results

In total, 25,676 suspected cases were notified and 2,907 were diagnosed as prion diseases, including 2,510 (86%) with sporadic Creutzfeldt–Jakob disease (sCJD), 240 (8%) genetic and 157 (6%) with infectious prion disease. Suspected cases and sCJD cases increased over time. Younger sCJD patients (≤ 50 years) showed phenotypes related to a distinct molecular subtype distribution vs those above 50 years. Compared to other European countries, France has had a higher number of cases with iatrogenic CJD after growth hormone treatment and variant CJD (vCJD) linked to bovine spongiform encephalopathy (second after the United Kingdom), but numbers slowly decreased over time.

Conclusion

We observed a decrease of CJD infectious forms, demonstrating the effectiveness of measures to limit human exposure to exogenous prions. However, active surveillance is needed regarding uncertainties about future occurrences of vCJD, possible zoonotic potential of chronic wasting diseases in cervids and increasing trends of sCJD observed in France and other countries.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2023.28.50.2300101
2023-12-14
2024-04-28
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2023.28.50.2300101
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/28/50/eurosurv-28-50-2.html?itemId=/content/10.2807/1560-7917.ES.2023.28.50.2300101&mimeType=html&fmt=ahah

References

  1. Prusiner SB. Novel proteinaceous infectious particles cause scrapie. Science. 1982;216(4542):136-44.  https://doi.org/10.1126/science.6801762  PMID: 6801762 
  2. Atkinson CJ, Zhang K, Munn AL, Wiegmans A, Wei MQ. Prion protein scrapie and the normal cellular prion protein. Prion. 2016;10(1):63-82.  https://doi.org/10.1080/19336896.2015.1110293  PMID: 26645475 
  3. Aguzzi A, Sigurdson C, Heikenwaelder M. Molecular mechanisms of prion pathogenesis. Annu Rev Pathol. 2008;3(1):11-40.  https://doi.org/10.1146/annurev.pathmechdis.3.121806.154326  PMID: 18233951 
  4. Minikel EV, Vallabh SM, Lek M, Estrada K, Samocha KE, Sathirapongsasuti JF, et al. Quantifying prion disease penetrance using large population control cohorts. Sci Transl Med. 2016;8(322):322ra9.  https://doi.org/10.1126/scitranslmed.aad5169  PMID: 26791950 
  5. National CJD Research and Surveillance Unit. Creutzfeldt-Jakob Disease Surveillance in the UK. 28th Annual Report 2019. Edinburgh: National CJD Research and Surveillance Unit; 2109. Available from: http://www.cjd.ed.ac.uk/sites/default/files/Report28.pdf
  6. Brandel JP, Peckeu L, Haïk S. The French surveillance network of Creutzfeldt-Jakob disease. Epidemiological data in France and worldwide. Transfus Clin Biol. 2013;20(4):395-7.  https://doi.org/10.1016/j.tracli.2013.02.029  PMID: 23587616 
  7. Chen C, Dong XP. Epidemiological characteristics of human prion diseases. Infect Dis Poverty. 2016;5(1):47.  https://doi.org/10.1186/s40249-016-0143-8  PMID: 27251305 
  8. Creutzfeldt-Jakob Disease International Surveillance Network. CJD surveillance data 1993-2020. Edinburgh: University of Edinburgh. [Accessed: 9 Feb 2023]. Available from: https://www.eurocjd.ed.ac.uk/data
  9. Parchi P, Giese A, Capellari S, Brown P, Schulz-Schaeffer W, Windl O, et al. Classification of sporadic Creutzfeldt-Jakob disease based on molecular and phenotypic analysis of 300 subjects. Ann Neurol. 1999;46(2):224-33.  https://doi.org/10.1002/1531-8249(199908)46:2<224::AID-ANA12>3.0.CO;2-W  PMID: 10443888 
  10. Bateman D, Hilton D, Love S, Zeidler M, Beck J, Collinge J. Sporadic Creutzfeldt-Jakob disease in a 18-year-old in the UK. Lancet. 1995;346(8983):1155-6.  https://doi.org/10.1016/S0140-6736(95)91828-0  PMID: 7475612 
  11. Britton TC, al-Sarraj S, Shaw C, Campbell T, Collinge J. Sporadic Creutzfeldt-Jakob disease in a 16-year-old in the UK. Lancet. 1995;346(8983):1155.  https://doi.org/10.1016/S0140-6736(95)91827-2  PMID: 7475611 
  12. Chazot G, Broussolle E, Lapras Cl, Blättler T, Aguzzi A, Kopp N. New variant of Creutzfeldt-Jakob disease in a 26-year-old French man. Lancet. 1996;347(9009):1181.  https://doi.org/10.1016/S0140-6736(96)90638-8  PMID: 8609775 
  13. Collinge J, Sidle KC, Meads J, Ironside J, Hill AF. Molecular analysis of prion strain variation and the aetiology of ‘new variant’ CJD. Nature. 1996;383(6602):685-90.  https://doi.org/10.1038/383685a0  PMID: 8878476 
  14. Will RG, Ironside JW, Zeidler M, Cousens SN, Estibeiro K, Alperovitch A, et al. A new variant of Creutzfeldt-Jakob disease in the UK. Lancet. 1996;347(9006):921-5.  https://doi.org/10.1016/S0140-6736(96)91412-9  PMID: 8598754 
  15. Lasmézas CI, Deslys JP, Demaimay R, Adjou KT, Lamoury F, Dormont D, et al. BSE transmission to macaques. Nature. 1996;381(6585):743-4.  https://doi.org/10.1038/381743a0  PMID: 8657276 
  16. Hill AF, Desbruslais M, Joiner S, Sidle KC, Gowland I, Collinge J, et al. The same prion strain causes vCJD and BSE. Nature. 1997;389(6650):448-50, 526.  https://doi.org/10.1038/38925  PMID: 9333232 
  17. Brandel JP, Heath CA, Head MW, Levavasseur E, Knight R, Laplanche JL, et al. Variant Creutzfeldt-Jakob disease in France and the United Kingdom: Evidence for the same agent strain. Ann Neurol. 2009;65(3):249-56.  https://doi.org/10.1002/ana.21583  PMID: 19334063 
  18. Kobayashi A, Kitamoto T, Mizusawa H. Iatrogenic Creutzfeldt-Jakob disease. Handb Clin Neurol. 2018;153:207-18.  https://doi.org/10.1016/B978-0-444-63945-5.00012-X  PMID: 29887137 
  19. Rudge P, Jaunmuktane Z, Adlard P, Bjurstrom N, Caine D, Lowe J, et al. Iatrogenic CJD due to pituitary-derived growth hormone with genetically determined incubation times of up to 40 years. Brain. 2015;138(Pt 11):3386-99.  https://doi.org/10.1093/brain/awv235  PMID: 26268531 
  20. Brandel JP, Preece M, Brown P, Croes E, Laplanche JL, Agid Y, et al. Distribution of codon 129 genotype in human growth hormone-treated CJD patients in France and the UK. Lancet. 2003;362(9378):128-30.  https://doi.org/10.1016/S0140-6736(03)13867-6  PMID: 12867116 
  21. Prusiner SB. Prion diseases and the BSE crisis. Science. 1997;278(5336):245-51.  https://doi.org/10.1126/science.278.5336.245  PMID: 9323196 
  22. Brown P, Brandel JP, Preece M, Sato T. Iatrogenic Creutzfeldt-Jakob disease: the waning of an era. Neurology. 2006;67(3):389-93.  https://doi.org/10.1212/01.wnl.0000231528.65069.3f  PMID: 16855204 
  23. European Centre for Disease Prevention and Control (ECDC). European Creutzfeldt-Jakob Disease Surveillance Network (EuroCJD). Stockholm: ECDC. [Accessed: 9 Feb 2023]. Available from: https://www.ecdc.europa.eu/en/about-ecdc/what-we-do/partners-and-networks/disease-and-laboratory-networks/european-creutzfeldt
  24. Peoc’h K, Manivet P, Beaudry P, Attane F, Besson G, Hannequin D, et al. Identification of three novel mutations (E196K, V203I, E211Q) in the prion protein gene (PRNP) in inherited prion diseases with Creutzfeldt-Jakob disease phenotype. Hum Mutat. 2000;15(5):482.  https://doi.org/10.1002/(SICI)1098-1004(200005)15:5<482::AID-HUMU16>3.0.CO;2-1  PMID: 10790216 
  25. Levavasseur E, Laffont-Proust I, Morain E, Faucheux BA, Privat N, Peoc’h K, et al. Regulating factors of PrP glycosylation in Creutzfeldt-Jakob disease--implications for the dissemination and the diagnosis of human prion strains. PLoS One. 2008;3(7):e2786.  https://doi.org/10.1371/journal.pone.0002786  PMID: 18665216 
  26. Creutzfeldt-Jakob Disease International Surveillance Network. Diagnostic criteria for surveillance of CJD from 1 January 2017. Edinburgh: University of Edinburgh. [Accessed: 9 Feb 2023]. Available from: https://www.eurocjd.ed.ac.uk/node/833
  27. Alperovitch A, Zerr I, Pocchiari M, Mitrova E, de Pedro Cuesta J, Hegyi I, et al. Codon 129 prion protein genotype and sporadic Creutzfeldt-Jakob disease. Lancet. 1999;353(9165):1673-4.  https://doi.org/10.1016/S0140-6736(99)01342-2  PMID: 10335789 
  28. Saba R, Booth SA. The genetics of susceptibility to variant Creutzfeldt-Jakob disease. Public Health Genomics. 2013;16(1-2):17-24.  https://doi.org/10.1159/000345203  PMID: 23548713 
  29. Pocchiari M, Puopolo M, Croes EA, Budka H, Gelpi E, Collins S, et al. Predictors of survival in sporadic Creutzfeldt-Jakob disease and other human transmissible spongiform encephalopathies. Brain. 2004;127(Pt 10):2348-59.  https://doi.org/10.1093/brain/awh249  PMID: 15361416 
  30. Parchi P, Saverioni D. Molecular pathology, classification, and diagnosis of sporadic human prion disease variants. Folia Neuropathol. 2012;50(1):20-45. PMID: 22505361 
  31. Parchi P, Capellari S, Chen SG, Petersen RB, Gambetti P, Kopp N, et al. Typing prion isoforms. Nature. 1997;386(6622):232-4.  https://doi.org/10.1038/386232a0  PMID: 9069279 
  32. Bougard D, Brandel JP, Bélondrade M, Béringue V, Segarra C, Fleury H, et al. Detection of prions in the plasma of presymptomatic and symptomatic patients with variant Creutzfeldt-Jakob disease. Sci Transl Med. 2016;8(370):370ra182.  https://doi.org/10.1126/scitranslmed.aag1257  PMID: 28003547 
  33. Peckeu L, Brandel JP, Welaratne A, Costagliola D, Haïk S. Susceptibility to Creutzfeldt-Jakob disease after human growth hormone treatment in France. Neurology. 2018;91(8):e724-31.  https://doi.org/10.1212/WNL.0000000000006028  PMID: 30045957 
  34. Ladogana A, Kovacs GG. Genetic Creutzfeldt-Jakob disease. Handb Clin Neurol. 2018;153:219-42.  https://doi.org/10.1016/B978-0-444-63945-5.00013-1  PMID: 29887139 
  35. Masters CL, Harris JO, Gajdusek DC, Gibbs CJ Jr, Bernoulli C, Asher DM. Creutzfeldt-Jakob disease: patterns of worldwide occurrence and the significance of familial and sporadic clustering. Ann Neurol. 1979;5(2):177-88.  https://doi.org/10.1002/ana.410050212  PMID: 371520 
  36. Watson N, Brandel JP, Green A, Hermann P, Ladogana A, Lindsay T, et al. The importance of ongoing international surveillance for Creutzfeldt-Jakob disease. Nat Rev Neurol. 2021;17(6):362-79.  https://doi.org/10.1038/s41582-021-00488-7  PMID: 33972773 
  37. Brown P, Brandel JP, Sato T, Nakamura Y, MacKenzie J, Will RG, et al. Iatrogenic Creutzfeldt-Jakob disease, final assessment. Emerg Infect Dis. 2012;18(6):901-7.  https://doi.org/10.3201/eid1806.120116  PMID: 22607808 
  38. Uttley L, Carroll C, Wong R, Hilton DA, Stevenson M. Creutzfeldt-Jakob disease: a systematic review of global incidence, prevalence, infectivity, and incubation. Lancet Infect Dis. 2020;20(1):e2-10.  https://doi.org/10.1016/S1473-3099(19)30615-2  PMID: 31876504 
  39. Klug GM, Wand H, Simpson M, Boyd A, Law M, Masters CL, et al. Intensity of human prion disease surveillance predicts observed disease incidence. J Neurol Neurosurg Psychiatry. 2013;84(12):1372-7.  https://doi.org/10.1136/jnnp-2012-304820  PMID: 23965290 
  40. Denouel A, Brandel JP, Seilhean D, Laplanche JL, Elbaz A, Haik S. The role of environmental factors on sporadic Creutzfeldt-Jakob disease mortality: evidence from an age-period-cohort analysis. Eur J Epidemiol. 2023;38(7):757-64.  https://doi.org/10.1007/s10654-023-01004-5  PMID: 37191829 
  41. Laplanche JL, Delasnerie-Lauprêtre N, Brandel JP, Chatelain J, Beaudry P, Alpérovitch A, et al. Molecular genetics of prion diseases in France. Neurology. 1994;44(12):2347-51.  https://doi.org/10.1212/WNL.44.12.2347  PMID: 7991124 
  42. Palmer MS, Dryden AJ, Hughes JT, Collinge J. Homozygous prion protein genotype predisposes to sporadic Creutzfeldt-Jakob disease. Nature. 1991;352(6333):340-2.  https://doi.org/10.1038/352340a0  PMID: 1677164 
  43. Parchi P, de Boni L, Saverioni D, Cohen ML, Ferrer I, Gambetti P, et al. Consensus classification of human prion disease histotypes allows reliable identification of molecular subtypes: an inter-rater study among surveillance centres in Europe and USA. Acta Neuropathol. 2012;124(4):517-29.  https://doi.org/10.1007/s00401-012-1002-8  PMID: 22744790 
  44. Haïk S, Brandel JP. Biochemical and strain properties of CJD prions: complexity versus simplicity. J Neurochem. 2011;119(2):251-61.  https://doi.org/10.1111/j.1471-4159.2011.07399.x  PMID: 21790605 
  45. Gelpi E, Baiardi S, Nos C, Dellavalle S, Aldecoa I, Ruiz-Garcia R, et al. Sporadic Creutzfeldt-Jakob disease VM1: phenotypic and molecular characterization of a novel subtype of human prion disease. Acta Neuropathol Commun. 2022;10(1):114.  https://doi.org/10.1186/s40478-022-01415-7  PMID: 35978418 
  46. Peckeu L, Brandel JP, Welaratne A, Amar E, Costagliola D, Haïk S. Factors influencing the incubation of an infectious form of Creutzfeldt-Jakob Disease. Clin Infect Dis. 2020;70(7):1487-90. PMID: 31351441 
  47. Brandel JP, Vlaicu MB, Culeux A, Belondrade M, Bougard D, Grznarova K, et al. Variant Creutzfeldt-Jakob disease diagnosed 7.5 years after occupational exposure. N Engl J Med. 2020;383(1):83-5.  https://doi.org/10.1056/NEJMc2000687  PMID: 32609989 
  48. Mok T, Jaunmuktane Z, Joiner S, Campbell T, Morgan C, Wakerley B, et al. Variant Creutzfeldt-Jakob disease in a patient with heterozygosity at PRNP codon 129. N Engl J Med. 2017;376(3):292-4.  https://doi.org/10.1056/NEJMc1610003  PMID: 28099827 
  49. Tranulis MA, Gavier-Widén D, Våge J, Nöremark M, Korpenfelt SL, Hautaniemi M, et al. Chronic wasting disease in Europe: new strains on the horizon. Acta Vet Scand. 2021;63(1):48.  https://doi.org/10.1186/s13028-021-00606-x  PMID: 34823556 
  50. Hannaoui S, Zemlyankina I, Chang SC, Arifin MI, Béringue V, McKenzie D, et al. Transmission of cervid prions to humanized mice demonstrates the zoonotic potential of CWD. Acta Neuropathol. 2022;144(4):767-84.  https://doi.org/10.1007/s00401-022-02482-9  PMID: 35996016 
  51. Anderson CA, Bosque P, Filley CM, Arciniegas DB, Kleinschmidt-Demasters BK, Pape WJ, et al. Colorado surveillance program for chronic wasting disease transmission to humans: lessons from 2 highly suspicious but negative cases. Arch Neurol. 2007;64(3):439-41.  https://doi.org/10.1001/archneur.64.3.439  PMID: 17353391 
  52. Rodriguez MM, Peoc’h K, Haïk S, Bouchet C, Vernengo L, Mañana G, et al. A novel mutation (G114V) in the prion protein gene in a family with inherited prion disease. Neurology. 2005;64(8):1455-7.  https://doi.org/10.1212/01.WNL.0000158618.39527.93  PMID: 15851745 
  53. Chen B, Zhang S, Xiao Y, Wu Y, Tang W, Yan L, et al. Genetic Creutzfeldt-Jakob disease shows fatal family insomnia phenotype. Prion. 2021;15(1):177-82.  https://doi.org/10.1080/19336896.2021.1968291  PMID: 34486485 
  54. Chapman J, Arlazoroff A, Goldfarb LG, Cervenakova L, Neufeld MY, Werber E, et al. Fatal insomnia in a case of familial Creutzfeldt-Jakob disease with the codon 200(Lys) mutation. Neurology. 1996;46(3):758-61.  https://doi.org/10.1212/WNL.46.3.758  PMID: 8618678 
  55. Taratuto AL, Piccardo P, Reich EG, Chen SG, Sevlever G, Schultz M, et al. Insomnia associated with thalamic involvement in E200K Creutzfeldt-Jakob disease. Neurology. 2002;58(3):362-7.  https://doi.org/10.1212/WNL.58.3.362  PMID: 11839833 
Prospective 25-year surveillance of prion diseases in France, 1992 to 2016: a slow waning of epidemics and an increase in observed sporadic forms
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Ang%C3%A9line+Denouel&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Denouel Angéline</a>, <a href="/search?value1=Jean-Philippe+Brandel&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Brandel Jean-Philippe</a>, <a href="/search?value1=Laur%C3%A8ne+Peckeu-Abboud&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Peckeu-Abboud Laurène</a>, <a href="/search?value1=Danielle+Seilhean&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Seilhean Danielle</a>, <a href="/search?value1=Elodie+Bouaziz-Amar&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bouaziz-Amar Elodie</a>, <a href="/search?value1=Isabelle+Quadrio&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Quadrio Isabelle</a>, <a href="/search?value1=Jean-Baptiste+Oudart&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Oudart Jean-Baptiste</a>, <a href="/search?value1=Sylvain+Lehmann&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Lehmann Sylvain</a>, <a href="/search?value1=Pantxika+Bellecave&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bellecave Pantxika</a>, <a href="/search?value1=Jean-Louis+Laplanche&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Laplanche Jean-Louis</a>, <a href="/search?value1=St%C3%A9phane+Haik&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Haik Stéphane</a></span>. Prospective 25-year surveillance of prion diseases in France, 1992 to 2016: a slow waning of epidemics and an increase in observed sporadic forms. <a href="/content/ecdc">Euro Surveill.</a> 2023;28(50):pii=2300101. <a href="https://doi.org/10.2807/1560-7917.ES.2023.28.50.2300101" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2023.28.50.2300101</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 09 Feb 2023;&nbsp;&nbsp; <span class="generated">Accepted</span>: 01 Jun 2023 </span> </p>
/content/10.2807/1560-7917.ES.2023.28.50.2300101
/content/10.2807/1560-7917.ES.2023.28.50.2300101
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
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