Skip to main content

Advertisement

Log in

Increased incidence of Lyme borreliosis in southern Sweden following mild winters and during warm, humid summers

  • Article
  • Published:
European Journal of Clinical Microbiology and Infectious Diseases Aims and scope Submit manuscript

Abstract

The aim of the present study was to investigate the long-term incidence rate of Lyme borreliosis and, additionally, to determine whether a correlation exists between climatic factors and summer-season variations in the incidence of Lyme borreliosis. Climatic variability acts directly on tick population dynamics and indirectly on human exposure to Lyme borreliosis spirochetes. In this study, conducted in primary healthcare clinics in southeastern Sweden, electronic patient records from 1997–2003 were searched for those that fulfilled the criteria for erythema migrans. Using a multilevel Poisson regression model, the influence of various climatic factors on the summer-season variations in the incidence of erythema migrans were studied. The mean annual incidence rate was 464 cases of erythema migrans per 100,000 inhabitants. The incidence was significantly higher in women than in men, 505 and 423 cases per 100,000 inhabitants, respectively (p<0.001). The summer-season variations in the erythema migrans incidence rate correlated with the monthly mean summer temperatures (incidence rate ratio 1.12; p<0.001), the number of winter days with temperatures below 0°C (incidence rate ratio 0.97; p<0.001), the monthly mean summer precipitation (incidence rate ratio 0.92; p<0.05), and the number of summer days with relative humidity above 86% (incidence rate ratio 1.04; p<0.05). In conclusion, Lyme borreliosis is highly endemic in southeastern Sweden. The climate in this area, which is favourable not only for human tick exposure but also for the abundance of host-seeking ticks, influences the summer-season variations in the incidence of Lyme borreliosis.

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

Similar content being viewed by others

References

  1. Mejlon HA, Jaenson TG (1993) Seasonal prevalence of Borrelia burgdorferi in Ixodes ricinus in different vegetation types in Sweden. Scand J Infect Dis 25:449–456

    Article  PubMed  CAS  Google Scholar 

  2. Berglund J, Eitrem R, Ornstein K, Lindberg A, Rignér Å, Elmrud H, Carlsson M, Runehagen A, Svanborg C, Norrby R (1995) An epidemiological study of Lyme disease in southern Sweden. N Engl J Med 333:1319–1324

    Article  PubMed  CAS  Google Scholar 

  3. Ornstein K, Berglund J, Nilsson I, Norrby R, Bergström S (2001) Characterization of Lyme borreliosis isolates from patients with erythema migrans and neuroborreliosis in southern Sweden. J Clin Microbiol 39:1294–1298

    Article  PubMed  CAS  Google Scholar 

  4. Carlsson SA, Granlund H, Jansson C, Nyman D, Wahlberg P (2003) Characteristics of erythema migrans in Borrelia afzelii and Borrelia garinii infections. Scand J Infect Dis 35:31–33

    Article  PubMed  Google Scholar 

  5. Berglund J (1998) Kraftig ökning av antalet patienter behandlade för borreliainfektion 1997 jämfört med 1992. Smittskydd 6:70

    Google Scholar 

  6. Jensen PM, Hansen H, Frandsen F (2000) Spatial risk assessment for Lyme borreliosis in Denmark. Scand J Infect Dis 32:545–550

    Article  PubMed  CAS  Google Scholar 

  7. Robertson JN, Gray JS, Stewart P (2000) Tick bite and Lyme borreliosis risk at a recreational site in England. Eur J Epidemiol 16:647–652

    Article  PubMed  CAS  Google Scholar 

  8. O’Connell S, Granström M, Gray JS, Stanek G (1998) Epidemiology of European Lyme borreliosis. Zentralbl Bakteriol 287:229–240

    PubMed  CAS  Google Scholar 

  9. Randolph SE (2001) The shifting landscape of tick-borne encephalitis and Lyme borreliosis in Europe. Philos Trans R Soc Lond B Biol Sci 356:1045–1056

    PubMed  CAS  Google Scholar 

  10. Gray JS, Kahl O, Robertson JN, Daniel M, Estrada-Pena A, Gettinby G (1998) Lyme borreliosis habitat assessment. Zentralbl Bakteriol 287:211–228

    CAS  Google Scholar 

  11. van Es RP, Gettinby G, Hillerton JE (1999) Models of temporal variation in questing activity in individuals of Ixodes ricinus (Acari: Ixodidae). Exp Appl Acarol 23:977–986

    Article  Google Scholar 

  12. Jensen PM (2000) Host-seeking activity of Ixodes ricinus ticks based on daily consecutive flagging samples. Exp Appl Acarol 24:695–708

    Article  PubMed  CAS  Google Scholar 

  13. Perret JL, Guigoz E, Rais O, Gern L (2000) Influence of saturation deficit and temperature on Ixodes ricinus tick questing activity in a Lyme borreliosis-endemic area (Switzerland). Parasitol Res 86:554–557

    Article  PubMed  CAS  Google Scholar 

  14. Lindgren E, Gustafson R (2001) Tick-borne encephalitis in Sweden and climate change. Lancet 358:16–18

    Article  PubMed  CAS  Google Scholar 

  15. Lindgren E, Tälleklint L, Polfeldt T (2000) Impact of climatic change on the northern latitude limit and population density of the disease-transmitting European tick Ixodes ricinus. Environ Health Perspect 108:119–123

    Article  PubMed  CAS  Google Scholar 

  16. Randolph SE, Storey K (1999) Impact of microclimate on immature tick-rodent host interactions (Acari: Ixodidae): implications for parasite transmission. J Med Entomol 36:741–748

    PubMed  CAS  Google Scholar 

  17. Gray JS (1984) Studies on the dynamics of active populations of the sheep tick, Ixodes ricinus L. in Co. Wicklow, Ireland. Acarologia 25:167–178

    PubMed  CAS  Google Scholar 

  18. Gray JS (1980) Studies on the activity of the Ixodes ricinus in relation to the epidemiology of babesiosis in Co. Meath, Ireland. Br Vet J 136:427–436

    PubMed  CAS  Google Scholar 

  19. MacLeod J (1936) Ixodes ricinus in relation to its physical environment. IV. An analysis of the ecological complexes controlling distribution and activities. Parasitology 28:298–319

    Google Scholar 

  20. Gray JS, Turley T, Strickland KL (1978) Studies on the ecology of sheep tick, Ixodes ricinus, in Co. Wicklow, Ireland. Ir Vet J 32:25–34

    Google Scholar 

  21. Mejlon HA (1997) Diel activity of Ixodes ricinus Acari: Ixodidae at two locations near Stockholm, Sweden. Exp Appl Acarol 21:247–255

    Article  PubMed  CAS  Google Scholar 

  22. Knülle W, Rudolph D (1982) Humidity relations and water balance of ticks. In: Obenchain FD, Galun R (eds) Physiology of ticks. Pergamon, Oxford, UK, pp 43–70

    Google Scholar 

  23. Centers for Disease Control and Prevention (1990) Case definitions for public health surveillance. MMWR Morb Mortal Wkly Rep 39(RR–13):19–21

    Google Scholar 

  24. Goldstein H (2003) Multilevel statistical models, 3rd edn. Hodder Arnold, London, pp 95–125

    Google Scholar 

  25. Rasbash J, Steele F, Browne W, Prosser B (2000) A user's guide to MLwiN. Centre for Multilevel Modelling, Institute of Education, University of London, London, UK. http://multilevel.ioe.ac.uk/download/userman20.pdf. Accessed November 2004

    Google Scholar 

  26. Rogers DJ, Randolph S, Lindsay S, Thomas C (2001) Vector-borne diseases and climate change. In: Department of Health (ed) Health effects of climate change in the UK. Available at http://www.doh.gov.uk/airpollution/climatechange02/

  27. Department for Environment, Food and Rural Affairs, UK (2003) Review of UK climate change indicators. http://www.nbu.ac.uk/iccuk/reportjune2003/Jan2004.htm. pp 1–67. Accessed January 2004

  28. Kaiser R (1995) Tick borne encephalitis in southern Germany. Lancet 345:463

    Article  PubMed  CAS  Google Scholar 

  29. Randolph SE, Green RM, Hoodles AN, Peacey MF (2002) An empirical quantitative framework for the seasonal population dynamics of the tick Ixodes ricinus. Int J Parasitol 32:979–989

    Article  PubMed  Google Scholar 

  30. Stjernberg L, Berglund J (2002) Risk of acquiring tick bites in south-eastern Sweden. Scand J Infect Dis 34:840–844

    Article  PubMed  Google Scholar 

  31. Orloski KA, Hayes EB, Campbell GL, Dennis DT (2000) Surveillance for Lyme disease—United States, 1992-1998. MMWR Surveill Summ 49:1–11

    CAS  Google Scholar 

  32. Chow CC, Evans AS, Noonan-Toly CM, White D, Johnson GS, Marks SJ, Caldwell MC, Hayes FB (2003) Lyme disease trends—Dutchess County, New York, 1992–2000. Mt Sinai J Med 70:207–213

    PubMed  Google Scholar 

  33. Dhôte R, Basse-Guerineau AL, Beaumesnil V, Christoforov B, Assous MV (2001) Full spectrum of clinical, serological and epidemiological features of complicated forms of Lyme borreliosis in the Paris, France, area. Eur J Clin Microbiol Infect Dis 19:809–815

    Google Scholar 

  34. Weber K, Puznik A, Becker T (1983) Erythema migrans-Krankheit. Beitrag zur Klinik und Beziehung zur Lyme-Krankheit. Dtsch Med Wochenschr 109:1182–1190

    Article  Google Scholar 

  35. Åsbrink E, Olsson I, Hovmark A (1986) Clinical manifestations of erythema chronicum migrans Afzelius in Sweden. A study of 231 patients. Zentral Bakteriol Mikrobiol Hyg [A] 263:229–236

    Google Scholar 

  36. Steere AC, Bartenhagen NH, Craft JE, Hutchinson GJ, Newman JH, Rahn DW, Sigal LH, Spieler PN, Stenn KN, Malawista SE (1983) The early clinical manifestations of Lyme disease. Ann Intern Med 99:76–82

    PubMed  CAS  Google Scholar 

  37. Berger B (1984) Erythema chronicum migrans of Lyme disease. Arch Dermatol 120:1017–1021

    Article  PubMed  CAS  Google Scholar 

  38. Widhe M (2003) Immune responses in human Lyme borreliosis. Cytokines and IgG subclasses in relation to clinical outcome. Linköping University Medical Dissertations, no 778. Linköping University, Linköping, Sweden

    Google Scholar 

Download references

Acknowledgements

This study was funded by grants from the county councils of Blekinge and Skåne. We thank Hans Alexandersson and Marcus Flarup at the Swedish Meteorological and Hydrological Institute for providing us with climate information and Desirée Clemedtsson at the Clinic for Infectious and Skin Diseases at the County Hospital in Karlskrona and the primary healthcare system administrators at the healthcare centres in the Blekinge County for providing us with electronic patient records.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. Bennet.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bennet, L., Halling, A. & Berglund, J. Increased incidence of Lyme borreliosis in southern Sweden following mild winters and during warm, humid summers. Eur J Clin Microbiol Infect Dis 25, 426–432 (2006). https://doi.org/10.1007/s10096-006-0167-2

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-006-0167-2

Keywords

Navigation