A prospective study on the incidence of Borrelia burgdorferi sensu lato infection after a tick bite in Sweden and on the Åland Islands, Finland (2008-2009)

Ticks and Tick-borne Diseases

Volumn 7, Issue 1, 2016, Pages 71-79

  Wilhelmsson, Peter ^a   Fryland, Linda ^a   Lindblom, Pontus ^a   Sjöwall, Johanna ^a   Ahlm, Clas ^b   Berglund, Johan ^c   Haglund, Mats ^d   Henningsson, Anna J ^e   Nolskog, Peter ^f   Nordberg, Marika ^g   Nyberg, Clara ^g   Ornstein, Katharina ^h,i   Nyman, Dag ^g   Ekerfelt, Christina ^a   Forsberg, Pia ^a   Lindgren, Per Eric ^a,e  

^a LINKÖPING UNIVERSITY   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

^c BLEKINGE INSTITUTE OF TECHNOLOGY   (Sweden)

^d KALMAR COUNTY HOSPITAL   (Sweden)

^e RYHOV COUNTY HOSPITAL   (Sweden)

^f SKARABORG HOSPITAL   (Sweden)

^g The Åland Group for Borrelia Research   (Finland)

^h Hässleholm Hospital   (Sweden)

ⁱ LUND UNIVERSITY   (Sweden)

Author keywords

Asymptomatic infection; Bacterial load; Borrelia burgdorferi sensu lato; Lyme borreliosis; Tick bite; Tick feeding

Indexed keywords

ADULT; AGED; ARTHRALGIA; ARTICLE; BORRELIA BURGDORFERI; BORRELIA BURGDORFERI SENSU LATO; COGNITIVE DEFECT; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FATIGUE; FEEDING BEHAVIOR; FEMALE; FEVER; FINLAND; FOLLOW UP; HEADACHE; HUMAN; IMMUNOBLOTTING; INCIDENCE; LOSS OF APPETITE; LYME DISEASE; MALE; MIDDLE AGED; MYALGIA; NAUSEA; NECK PAIN; NONHUMAN; PAIN; PARASITE LOAD; PARESTHESIA; PRIORITY JOURNAL; PROSPECTIVE STUDY; REAL TIME POLYMERASE CHAIN REACTION; RISK FACTOR; SEROCONVERSION; SEROPREVALENCE; SEX DIFFERENCE; SWEDEN; TICK BITE; TICK FEEDING; VERTIGO; WEIGHT REDUCTION; BLOOD; ISLAND (GEOLOGICAL); ISOLATION AND PURIFICATION; TRANSMISSION;

BACTERIUM ANTIBODY;

AGED; ANTIBODIES, BACTERIAL; BORRELIA BURGDORFERI GROUP; FEMALE; FINLAND; HUMANS; ISLANDS; LYME DISEASE; MALE; MIDDLE AGED; SWEDEN; TICK BITES;

EID: 84947487301     PISSN: 1877959X     EISSN: 18779603     Source Type: Journal    
DOI: 10.1016/j.ttbdis.2015.08.009     Document Type: Article

References (46)

1. Berglund J., Eitrem R. Tick-borne borreliosis in the archipelago of southern Sweden. Scand. J. Infect. Dis. 1993, 25:67-72.
2. Berglund J., Eitrem R., Ornstein K., Lindberg A., Ringér A., Elmrud H., Carlsson M., Runehagen A., Svanborg C., Norrby R. An epidemiologic study of Lyme disease in southern Sweden. N. Engl. J. Med. 1995, 333:1319-1327.
3. Boehringer-Ingelheim Drygt 1,3 miljoner svenskar blev bitna av fästing senaste säsongen. SIFO undersökning 2006 2006, (press release).
4. Carlsson S.A., Granlund H., Nyman D., Wahlberg P. IgG seroprevalence of Lyme borreliosis in the population of the Aland Islands in Finland. Scand. J. Infect. Dis. 1998, 30:501-503.
5. Cerar D., Cerar T., Ruzić-Sabljić E., Wormser G.P., Strle F. Subjective symptoms after treatment of early Lyme disease. Am. J. Med. 2010, 123:79-86.
6. Ekerfelt C., Masreliez C., Svenvik M., Ernerudh J., Roberg M., Forsberg P. Antibodies and T-cell reactivity to Borrelia burgdorferi in an asymptomatic population: a study of healthy blood donors in an inland town district in the south-east of Sweden. Scand. J. Infect. Dis. 2001, 33:806-808.
7. Fahrer H., van der Linden S.M., Sauvain M.J., Gern L., Zhioua E., Aeschlimann A. The prevalence and incidence of clinical and asymptomatic Lyme borreliosis in a population at risk. J. Infect. Dis. 1991, 163:305-310.
8. Faulde M.K., Rutenfranz M., Hepke J., Rogge M., Görner A., Keth A. Human tick infestation pattern, tick-bite rate, and associated Borrelia burgdorferi s.l. infection risk during occupational tick exposure at the Seedorf military training area, northwestern Germany. Ticks Tick-Borne Dis. 2014, 5:594-599.
9. Finnish Ministry of Social Affairs and Health Statistical Database 2013, The National Institute for Health and Welfare.
10. Fraser C.G. Reference change values. Clin. Chem. Lab. Med. 2012, 50:807-812.
11. Fryland L., Wilhelmsson P., Lindgren P.-E., Nyman D., Ekerfelt C., Forsberg P. Low risk of developing Borrelia burgdorferi infection in the south-east of Sweden after being bitten by a Borrelia burgdorferi-infected tick. Int. J. Infect. Dis. 2011, 15:e174-e181.
12. Fülöp B., Poggensee G. Epidemiological situation of Lyme borreliosis in Germany: surveillance data from six Eastern German States, 2002 to 2006. Parasitol. Res. 2008, 1(103 Suppl.):S117-S120.
13. Galea S., Tracy M. Participation rates in epidemiologic studies. Ann. Epidemiol. 2007, 17:643-653.
14. Gray J., Stanek G., Kundi M., Kocianova E. Dimensions of engorging Ixodes ricinus as a measure of feeding duration. Int. J. Med. Microbiol. 2005, 295:567-572.
15. Gustafson R., Forsgren M., Gardulf A., Granström M., Svenungsson B. Clinical manifestations and antibody prevalence of Lyme borreliosis and tick-borne encephalitis in Sweden: a study in five endemic areas close to Stockholm. Scand. J. Infect. Dis. 1993, 25:595-603.
16. Hofhuis A., van der Giessen J.W.B., Borgsteede F.H.M., Wielinga P.R., Notermans D.W., van Pelt W. Lyme borreliosis in the Netherlands: strong increase in GP consultations and hospital admissions in past 10 years. Euro Surveill. 2006, 11:E060622.2.
17. Hofhuis A., Herremans T., Notermans D.W., Sprong H., Fonville M., van der Giessen J.W.B., van Pelt W. A prospective study among patients presenting at the general practitioner with a tick bite or erythema migrans in The Netherlands. PLOS ONE 2013, 8:e64361.
18. Hubálek Z. Epidemiology of lyme borreliosis. Curr. Probl. Dermatol. 2009, 37:31-50.
19. Huegli D., Moret J., Rais O., Moosmann Y., Erard P., Malinverni R., Gern L. Prospective study on the incidence of infection by Borrelia burgdorferi sensu lato after a tick bite in a highly endemic area of Switzerland. Ticks Tick-Borne Dis. 2011, 2:129-136.
20. Jaenson T.G.T., Lindgren E. The range of Ixodes ricinus and the risk of contracting Lyme borreliosis will increase northwards when the vegetation period becomes longer. Ticks Tick-Borne Dis. 2011, 2:44-49.
21. Jaenson T.G.T., Jaenson D.G.E., Eisen L., Petersson E., Lindgren E. Changes in the geographical distribution and abundance of the tick Ixodes ricinus during the past 30 years in Sweden. Parasit. Vectors 2012, 5:8.
22. Jones K.L., Muellegger R.R., Means T.K., Lee M., Glickstein L.J., Damle N., Sikand V.K., Luster A.D., Steere A.C. Higher mRNA levels of chemokines and cytokines associated with macrophage activation in erythema migrans skin lesions in patients from the United States than in patients from Austria with Lyme borreliosis. Clin. Infect. Dis. 2008, 46:85-92.
23. Kahl O., Janetzki-Mittmann C., Gray J.S., Jonas R., Stein J., de Boer R. Risk of infection with Borrelia burgdorferi sensu lato for a host in relation to the duration of nymphal Ixodes ricinus feeding and the method of tick removal. Zentralbl. Bakteriol. 1998, 287:41-52.
24. Läkemedelsverket/Medical Products Agency. URL (accessed 13.07.15). https://lakemedelsverket.se/malgrupp/Halso---sjukvard/Behandlings--rekommendationer/Behandlingsrekommendation---listan/Borrelia/.
25. Mannelli A., Bertolotti L., Gern L., Gray J. Ecology of Borrelia burgdorferi sensu lato in Europe: transmission dynamics in multi-host systems, influence of molecular processes and effects of climate change. FEMS Microbiol. Rev. 2012, 36:837-861.
26. Mehnert W.H., Krause G. Surveillance of Lyme borreliosis in Germany, 2002 and 2003. Euro Surveill. 2005, 10:83-85.
27. Meiners T., Hammer B., Göbel U.B., Kahl O. Determining the tick scutal index allows assessment of tick feeding duration and estimation of infection risk with Borrelia burgdorferi sensu lato in a person bitten by an Ixodes ricinus nymph. Int. J. Med. Microbiol. 2006, 296(Suppl. 40):103-107.
28. Nadelman R.B., Nowakowski J., Fish D., Falco R.C., Freeman K., McKenna D., Welch P., Marcus R., Agüero-Rosenfeld M.E., Dennis D.T., Wormser G.P., Tick Bite Study Group Prophylaxis with single-dose doxycycline for the prevention of Lyme disease after an Ixodes scapularis tick bite. N. Engl. J. Med. 2001, 345:79-84.
29. Nahimana I., Gern L., Blanc D.S., Praz G., Francioli P., Péter O. Risk of Borrelia burgdorferi infection in western Switzerland following a tick bite. Eur. J. Clin. Microbiol. Infect. Dis. 2004, 23:603-608.
30. Ornstein K., Barbour A.G. A reverse transcriptase-polymerase chain reaction assay of Borrelia burgdorferi 16S rRNA for highly sensitive quantification of pathogen load in a vector. Vector Borne Zoonotic Dis. 2006, 6:103-112.
31. Piesman J., Mather T.N., Sinsky R.J., Spielman A. Duration of tick attachment and Borrelia burgdorferi transmission. J. Clin. Microbiol. 1987, 25:557-558.
32. Shapiro E.D., Gerber M.A., Holabird N.B., Berg A.T., Feder H.M., Bell G.L., Rys P.N., Persing D.H. A controlled trial of antimicrobial prophylaxis for Lyme disease after deer-tick bites. N. Engl. J. Med. 1992, 327:1769-1773.
33. Sood S.K., Salzman M.B., Johnson B.J., Happ C.M., Feig K., Carmody L., Rubin L.G., Hilton E., Piesman J. Duration of tick attachment as a predictor of the risk of Lyme disease in an area in which Lyme disease is endemic. J. Infect. Dis. 1997, 175:996-999.
34. Stanek G., Reiter M. The expanding Lyme Borrelia complex - clinical significance of genomic species?. Clin. Microbiol. Infect. 2011, 17:487-493.
35. Stanek G., Fingerle V., Hunfeld K.-P., Jaulhac B., Kaiser R., Krause A., Kristoferitsch W., O'Connell S., Ornstein K., Strle F., Gray J. Lyme borreliosis: clinical case definitions for diagnosis and management in Europe. Clin. Microbiol. Infect. 2011, 17:69-79.
36. Steere A.C., Sikand V.K., Schoen R.T., Nowakowski J. Asymptomatic infection with Borrelia burgdorferi. Clin. Infect. Dis. 2003, 37:528-532.
37. Strle F., Nelson J.A., Ruzic-Sabljic E., Cimperman J., Maraspin V., Lotric-Furlan S., Cheng Y., Picken M.M., Trenholme G.M., Picken R.N. European Lyme borreliosis: 231 culture-confirmed cases involving patients with erythema migrans. Clin. Infect. Dis. 1996, 23:61-65.
38. Strle F., Videcnik J., Zorman P., Cimperman J., Lotric-Furlan S., Maraspin V. Clinical and epidemiological findings for patients with erythema migrans. Comparison of cohorts from the years 1993 and 2000. Wien. Klin. Wochenschr. 2002, 114:493-497.
39. Strle K., Drouin E.E., Shen S., Khoury J.E., McHugh G., Ruzic-Sabljic E., Strle F., Steere A.C. Borrelia burgdorferi stimulates macrophages to secrete higher levels of cytokines and chemokines than Borrelia afzelii or Borrelia garinii. J. Infect. Dis. 2009, 200:1936-1943.
40. Strle F., Ružić-Sabljić E., Logar M., Maraspin V., Lotrič-Furlan S., Cimperman J., Ogrinc K., Stupica D., Nadelman R.B., Nowakowski J., Wormser G.P. Comparison of erythema migrans caused by Borrelia burgdorferi and Borrelia garinii. Vector Borne Zoonotic Dis. 2011, 11:1253-1258.
41. Strle F., Wormser G.P., Mead P., Dhaduvai K., Longo M.V., Adenikinju O., Soman S., Tefera Y., Maraspin V., Lotrič-Furlan S., Ogrinc K., Cimperman J., Ružić-Sabljić E., Stupica D. Gender disparity between cutaneous and non-cutaneous manifestations of Lyme borreliosis. PLOS ONE 2013, 8:e64110.
42. Tjernberg I., Krüger G., Eliasson I. C6 peptide ELISA test in the serodiagnosis of Lyme borreliosis in Sweden. Eur. J. Clin. Microbiol. Infect. Dis. 2007, 26:37-42.
43. Tomao P., Ciceroni L., Ovidio M.C.D'., De Rosa M., Vonesch N., Iavicoli S., Signorini S., Ciarrocchi S., Ciufolini M.G., Fiorentini C., Papaleo B. Prevalence and incidence of antibodies to Borrelia burgdorferi and to tick-borne encephalitis virus in agricultural and forestry workers from Tuscany, Italy. Eur. J. Clin. Microbiol. Infect. Dis. 2005, 24:457-463.
44. Wahlberg P. Incidence of tick-bite in man in Aland Islands: reference to the spread of Lyme borreliosis. Scand. J. Infect. Dis. 1990, 22:59-62.
45. Wilhelmsson P., Fryland L., Börjesson S., Nordgren J., Bergström S., Ernerudh J., Forsberg P., Lindgren P.-E. Prevalence and diversity of Borrelia species in ticks that have bitten humans in Sweden. J. Clin. Microbiol. 2010, 48:4169-4176.
46. Wilhelmsson P., Lindblom P., Fryland L., Ernerudh J., Forsberg P., Lindgren P.-E. Prevalence, diversity, and load of Borrelia species in ticks that have fed on humans in regions of Sweden and Åland Islands, Finland with different Lyme borreliosis incidences. PLOS ONE 2013, 8:e81433.