1887
Research Open Access
Like 0

Abstract

Background

Lyme borreliosis (LB) is the most common tick-borne disease (TBD) in France. Forestry workers are at high risk of TBD because of frequent exposure to tick bites.

Aim

We aimed to estimate the seroprevalence of sensu lato and tick-borne encephalitis virus (TBEV) antibodies among forestry workers in northern France. We compared seroprevalence by geographical area and assessed factors associated with seropositivity.

Methods

Between 2019 and 2020, we conducted a randomised cross-sectional seroprevalence survey. sl seropositivity was defined as positive ELISA and positive or equivocal result in western blot. Seropositivity for TBEV was defined as positive result from two ELISA tests, confirmed by serum neutralisation. We calculated weighted seroprevalence and adjusted prevalence ratios to determine association between potential risk factors and seropositivity.

Results

A total of 1,778 forestry workers participated. Seroprevalence for sl was 15.5% (95% confidence interval (CI): 13.9–17.3), 3.5 times higher in the eastern regions than in the western and increased with seniority and with weekly time in a forest environment. Seroprevalence was 2.5 times higher in forestry workers reporting a tick bite during past years and reporting usually not removing ticks rapidly. Seroprevalence for TBEV was 0.14% (95% CI: 0.05–0.42).

Conclusion

We assessed for the first time seroprevalence of sl and TBEV antibodies among forestry workers in northern France. These results will be used, together with data on LB and tick-borne encephalitis (TBE) incidence and on exposure to tick-bites, to target prevention programmes.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2023.28.32.2200961
2023-08-10
2024-11-22
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2023.28.32.2200961
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/28/32/eurosurv-28-32-2.html?itemId=/content/10.2807/1560-7917.ES.2023.28.32.2200961&mimeType=html&fmt=ahah

References

  1. Stanek G, Wormser GP, Gray J, Strle F. Lyme borreliosis. Lancet. 2012;379(9814):461-73.  https://doi.org/10.1016/S0140-6736(11)60103-7  PMID: 21903253 
  2. Ruzek D, Avšič Županc T, Borde J, Chrdle A, Eyer L, Karganova G, et al. Tick-borne encephalitis in Europe and Russia: Review of pathogenesis, clinical features, therapy, and vaccines. Antiviral Res. 2019;164:23-51.  https://doi.org/10.1016/j.antiviral.2019.01.014  PMID: 30710567 
  3. Boulanger N, Boyer P, Talagrand-Reboul E, Hansmann Y. Ticks and tick-borne diseases. Med Mal Infect. 2019;49(2):87-97.  https://doi.org/10.1016/j.medmal.2019.01.007  PMID: 30736991 
  4. Réseau Sentinelles. Bilan d'activité 2020 - Surveillance de la borréliose de Lyme. [Activity report 2020 – Surveillance of Lyme borreliosis]. Paris: Medicine Sorbonne Université. UMR-S 1136; 2021. 87-94 p. French. Available from: https://www.sentiweb.fr/document/5361
  5. Septfons A, Goronflot T, Jaulhac B, Roussel V, De Martino S, Guerreiro S, et al. Epidemiology of Lyme borreliosis through two surveillance systems: the national Sentinelles GP network and the national hospital discharge database, France, 2005 to 2016. Euro Surveill. 2019;24(11):1800134.  https://doi.org/10.2807/1560-7917.ES.2019.24.11.1800134  PMID: 30892181 
  6. Vourc’h G, Abrial D, Bord S, Jacquot M, Masséglia S, Poux V, et al. Mapping human risk of infection with Borrelia burgdorferi sensu lato, the agent of Lyme borreliosis, in a periurban forest in France. Ticks Tick Borne Dis. 2016;7(5):644-52.  https://doi.org/10.1016/j.ttbdis.2016.02.008  PMID: 26897396 
  7. Cotté V, Bonnet S, Cote M, Vayssier-Taussat M. Prevalence of five pathogenic agents in questing Ixodes ricinus ticks from western France. Vector Borne Zoonotic Dis. 2010;10(8):723-30.  https://doi.org/10.1089/vbz.2009.0066  PMID: 20020814 
  8. Boulanger N, Zilliox L, Goldstein V, Boyer P, Napolitano DBJ. Surveillance du vecteur de la borréliose de Lyme, Ixodes ricinus, en Alsace de 2013 à 2016. Bull Epidemiol Hebd (Paris). 2018:19-20.
  9. Ferquel E, Garnier M, Marie J, Bernède-Bauduin C, Baranton G, Pérez-Eid C, et al. Prevalence of Borrelia burgdorferi sensu lato and Anaplasmataceae members in Ixodes ricinus ticks in Alsace, a focus of Lyme borreliosis endemicity in France. Appl Environ Microbiol. 2006;72(4):3074-8.  https://doi.org/10.1128/AEM.72.4.3074-3078.2006  PMID: 16598024 
  10. Beytout J, George JC, Malaval J, Garnier M, Beytout M, Baranton G, et al. Lyme borreliosis incidence in two French departments: correlation with infection of Ixodes ricinus ticks by Borrelia burgdorferi sensu lato. Vector Borne Zoonotic Dis. 2007;7(4):507-17.  https://doi.org/10.1089/vbz.2006.0633  PMID: 17979533 
  11. Jenkins VA, Silbernagl G, Baer LR, Hoet B. The epidemiology of infectious diseases in Europe in 2020 versus 2017-2019 and the rise of tick-borne encephalitis (1995-2020). Ticks Tick Borne Dis. 2022;13(5):101972.  https://doi.org/10.1016/j.ttbdis.2022.101972  PMID: 35662067 
  12. Dekker M, Laverman GD, de Vries A, Reimerink J, Geeraedts F. Emergence of tick-borne encephalitis (TBE) in the Netherlands. Ticks Tick Borne Dis. 2019;10(1):176-9.  https://doi.org/10.1016/j.ttbdis.2018.10.008  PMID: 30385073 
  13. Heinz FX, Stiasny K, Holzmann H, Kundi M, Sixl W, Wenk M, et al. Emergence of tick-borne encephalitis in new endemic areas in Austria: 42 years of surveillance. Euro Surveill. 2015;20(13):21077.  https://doi.org/10.2807/1560-7917.ES2015.20.13.21077  PMID: 25860391 
  14. Botelho-Nevers E, Gagneux-Brunon A, Velay A, Guerbois-Galla M, Grard G, Bretagne C, et al. Tick-borne encephalitis in Auvergne-Rhône-Alpes region, France, 2017-2018. Emerg Infect Dis. 2019;25(10):1944-8.  https://doi.org/10.3201/eid2510.181923  PMID: 31538929 
  15. Santé publique France. Foyer de cas d’encéphalite à tiques liés à la consommation de fromage de chèvre au lait cru dans l’Ain. [Outbreak of tick-borne encephalitis associated with consumption of cheese of raw goat milk in Ain]. Saint-Maurice: Santé publique France; 22 June 2020. French. Available from: https://www.santepubliquefrance.fr/les-actualites/2020/foyer-de-cas-d-encephalite-a-tiques-lies-a-la-consommation-de-fromage-de-chevre-au-lait-cru-dans-l-ain.-point-au-19-juin-2020#:~:text=formulaire%20ci%2Ddessous-,Foyer%20de%20cas%20d%27enc%C3%A9phalite%20%C3%A0%20tiques%20li%C3%A9s%20%C3%A0%20la,entre%20avril%20et%20mai%202020
  16. Richard S, Oppliger A. Zoonotic occupational diseases in forestry workers - Lyme borreliosis, tularemia and leptospirosis in Europe. Ann Agric Environ Med. 2015;22(1):43-50.  https://doi.org/10.5604/12321966.1141368  PMID: 25780827 
  17. Piacentino JD, Schwartz BS. Occupational risk of Lyme disease: an epidemiological review. Occup Environ Med. 2002;59(2):75-84.  https://doi.org/10.1136/oem.59.2.75  PMID: 11850549 
  18. Magnavita N, Capitanelli I, Ilesanmi O, Chirico F. Occupational Lyme disease: a systematic review and meta-analysis. Diagnostics (Basel). 2022;12(2):296.  https://doi.org/10.3390/diagnostics12020296  PMID: 35204387 
  19. Schielein L, Tizek L, Biedermann T, Zink A. Tick bites in different professions and regions: pooled cross-sectional study in the focus area Bavaria, Germany. BMC Public Health. 2022;22(1):234.  https://doi.org/10.1186/s12889-021-12456-3  PMID: 35120477 
  20. Rigaud E, Jaulhac B, Garcia-Bonnet N, Hunfeld KP, Féménia F, Huet D, et al. Seroprevalence of seven pathogens transmitted by the Ixodes ricinus tick in forestry workers in France. Clin Microbiol Infect. 2016;22(8):735.e1-9.  https://doi.org/10.1016/j.cmi.2016.05.014  PMID: 27237545 
  21. Zhioua E, Rodhain F, Binet P, Perez-Eid C. Prevalence of antibodies to Borrelia burgdorferi in forestry workers of Ile de France, France. Eur J Epidemiol. 1997;13(8):959-62.  https://doi.org/10.1023/A:1007465305193  PMID: 9476828 
  22. Eltinge J, Yansaneh I. Diagnostics for formation of nonresponse adjustment cells, with an application to income nonresponse in the U.S. consumer expenditure survey. Surv Methodol. 1997;23:33-40.
  23. Deville J, Särndal C, Sautory O. Generalized raking procedures in survey sampling. J Am Stat Assoc. 1993;88(423):1013-20.  https://doi.org/10.1080/01621459.1993.10476369 
  24. Velay A, Solis M, Barth H, Sohn V, Moncollin A, Neeb A, et al. Comparison of six commercial tick-borne encephalitis IgM and IgG ELISA kits and the molecular characterization of their antigenic design. Diagn Microbiol Infect Dis. 2018;90(4):286-92.  https://doi.org/10.1016/j.diagmicrobio.2017.12.012  PMID: 29366629 
  25. Beck C, Desprès P, Paulous S, Vanhomwegen J, Lowenski S, Nowotny N, et al. A high-performance multiplex Immunoassay for serodiagnosis of flavivirus-associated neurological diseases in horses. BioMed Res Int. 2015;2015:678084.  https://doi.org/10.1155/2015/678084  PMID: 26457301 
  26. The American Association for Public Opinion Research (AAPOR). Standard definitions: final dispositions of case codes and outcome rates for surveys. Alexandria: AAPOR; 2016. Available from: https://aapor.org/standards-and-ethics/standard-definitions/
  27. Septfons A, Figoni J, Gautier A, Soullier N, de Valk H, Desenclos JC. Increased awareness and knowledge of Lyme Borreliosis and tick bite prevention among the general population in France: 2016 and 2019 health barometer survey. BMC Public Health. 2021;21(1):1808.  https://doi.org/10.1186/s12889-021-11850-1  PMID: 34620144 
  28. Dong Y, Zhou G, Cao W, Xu X, Zhang Y, Ji Z, et al. Global seroprevalence and sociodemographic characteristics of Borrelia burgdorferi sensu lato in human populations: a systematic review and meta-analysis. BMJ Glob Health. 2022;7(6):e007744.  https://doi.org/10.1136/bmjgh-2021-007744  PMID: 35697507 
  29. Wilking H, Fingerle V, Klier C, Thamm M, Stark K. Antibodies against Borrelia burgdorferi sensu lato among adults, Germany, 2008-2011. Emerg Infect Dis. 2015;21(1):107-10.  https://doi.org/10.3201/eid2101.140009  PMID: 25531140 
  30. De Keukeleire M, Robert A, Luyasu V, Kabamba B, Vanwambeke SO. Seroprevalence of Borrelia burgdorferi in Belgian forestry workers and associated risk factors. Parasit Vectors. 2018;11(1):277.  https://doi.org/10.1186/s13071-018-2860-2  PMID: 29716647 
  31. van Beek J, Sajanti E, Helve O, Ollgren J, Virtanen MJ, Rissanen H, et al. Population-based Borrelia burgdorferi sensu lato seroprevalence and associated risk factors in Finland. Ticks Tick Borne Dis. 2018;9(2):275-80.  https://doi.org/10.1016/j.ttbdis.2017.10.018  PMID: 29153461 
  32. Glatz M, Golestani M, Kerl H, Müllegger RR. Clinical relevance of different IgG and IgM serum antibody responses to Borrelia burgdorferi after antibiotic therapy for erythema migrans: long-term follow-up study of 113 patients. Arch Dermatol. 2006;142(7):862-8.  https://doi.org/10.1001/archderm.142.7.862  PMID: 16847202 
  33. Kalish RA, McHugh G, Granquist J, Shea B, Ruthazer R, Steere AC. Persistence of immunoglobulin M or immunoglobulin G antibody responses to Borrelia burgdorferi 10-20 years after active Lyme disease. Clin Infect Dis. 2001;33(6):780-5.  https://doi.org/10.1086/322669  PMID: 11512082 
  34. Aguero-Rosenfeld ME, Nowakowski J, Bittker S, Cooper D, Nadelman RB, Wormser GP. Evolution of the serologic response to Borrelia burgdorferi in treated patients with culture-confirmed erythema migrans. J Clin Microbiol. 1996;34(1):1-9.  https://doi.org/10.1128/jcm.34.1.1-9.1996  PMID: 8748261 
  35. Bournez L, Umhang G, Moinet M, Richomme C, Demerson JM, Caillot C, et al. Tick-borne encephalitis virus: seasonal and annual variation of epidemiological parameters related to nymph-to-larva transmission and exposure of small mammals. Pathogens. 2020;9(7):518.  https://doi.org/10.3390/pathogens9070518  PMID: 32605114 
  36. Gonzalez G, Bournez L, Moraes RA, Marine D, Galon C, Vorimore F, et al. A One-Health approach to investigating an outbreak of alimentary tick-borne encephalitis in a non-endemic area in France (Ain, eastern France): a longitudinal serological study in livestock, detection in ticks, and the first tick-borne encephalitis virus isolation and molecular characterisation. Front Microbiol. 2022;13:863725.  https://doi.org/10.3389/fmicb.2022.863725  PMID: 35479640 
  37. Süss J. Tick-borne encephalitis 2010: epidemiology, risk areas, and virus strains in Europe and Asia-an overview. Ticks Tick Borne Dis. 2011;2(1):2-15.  https://doi.org/10.1016/j.ttbdis.2010.10.007  PMID: 21771531 
  38. Voyiatzaki C, Papailia SI, Venetikou MS, Pouris J, Tsoumani ME, Papageorgiou EG. Climate changes exacerbate the spread of Ixodes ricinus and the occurrence of Lyme borreliosis and tick-borne encephalitis in Europe-how climate models are used as a risk assessment approach for tick-borne diseases. Int J Environ Res Public Health. 2022;19(11):6516.  https://doi.org/10.3390/ijerph19116516  PMID: 35682098 
  39. Heinz FX, Stiasny K, Holzmann H, Grgic-Vitek M, Kriz B, Essl A, et al. Vaccination and tick-borne encephalitis, central Europe. Emerg Infect Dis. 2013;19(1):69-76.  https://doi.org/10.3201/eid1901.120458  PMID: 23259984 
/content/10.2807/1560-7917.ES.2023.28.32.2200961
Loading

Data & Media loading...

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