Borrelia miyamotoi is widespread in Ixodes ricinus ticks in southern Norway

Ticks and Tick-borne Diseases

Volumn 6, Issue 4, 2015, Pages 516-521

  Kjelland, Vivian ^a,b   Rollum, Rikke ^a   Korslund, Lars ^a   Slettan, Audun ^a   Tveitnes, Dag ^c  

^a UNIVERSITY OF AGDER   (Norway)

^b Section of Rheumatology   (Norway)

^c STAVANGER UNIVERSITY HOSPITAL   (Norway)

Author keywords

Borrelia miyamotoi; Infection prevalence; Ixodes ricinus ticks; Real time PCR; Sequencing

Indexed keywords

RNA 16S; BACTERIAL DNA;

ADULT; AMPLICON; ARTICLE; BACTERIUM DETECTION; BACTERIUM IDENTIFICATION; BORRELIA; BORRELIA BURGDORFERI; BORRELIA INFECTION; BORRELIA MIYAMOTOI; DISEASE CARRIER; DISEASE TRANSMISSION; GENE AMPLIFICATION; GENE SEQUENCE; GEOGRAPHIC DISTRIBUTION; INFECTION RATE; IXODES RICINUS; LARVA; MIXED INFECTION; NONHUMAN; NORWAY; NUCLEOTIDE SEQUENCE; PREVALENCE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; ANIMAL; CLASSIFICATION; FEMALE; GENETICS; ISOLATION AND PURIFICATION; IXODES; MALE; MICROBIOLOGY; MOLECULAR GENETICS; NYMPH; PHYLOGENY; PHYSIOLOGY;

BORRELIA MIYAMOTOI; IXODES RICINUS; IXODIDA; SPIROCHAETALES;

ANIMALS; BORRELIA; DNA, BACTERIAL; FEMALE; IXODES; MALE; MOLECULAR SEQUENCE DATA; NORWAY; NYMPH; PHYLOGENY;

EID: 84930042187     PISSN: 1877959X     EISSN: 18779603     Source Type: Journal    
DOI: 10.1016/j.ttbdis.2015.04.004     Document Type: Article

References (45)

1. Arthur D.A. British Ticks 1963, Butterworths, London.
2. Balmelli T., Piffaretti J.C. Association between different clinical manifestations of Lyme disease and different species of Borrelia burgdorferi sensu lato. Res. Microbiol. 1995, 146(4):329-340.
3. Barbour A. Borrelia: A Diverse and Ubiquitous Genus of Tick-Borne Pathogens (Vol. 5). 2001, American Society for Microbiology Press, Washington, DC.
4. Barbour A.G., Bunikis J., Travinsky B., Hoen A.G., Diuk-Wasser M.A., Fish D., Tsao J.I. Niche partitioning of Borrelia burgdorferi and Borrelia miyamotoi in the same tick vector and mammalian reservoir species. Am. J. Trop. Med. Hyg. 2009, 81(6):1120-1131. 10.4269/ajtmh.2009.09-0208.
5. Bunikis J., Garpmo U., Tsao J., Berglund J., Fish D., Barbour A.G. Sequence typing reveals extensive strain diversity of the Lyme borreliosis agents Borrelia burgdorferi in North America and Borrelia afzelii in Europe. Microbiology 2004, 150(Pt 6):1741-1755. 10.1099/mic.0.26944-0.
6. Cadavid D., Barbour A.G. Neuroborreliosis during relapsing fever: review of the clinical manifestations, pathology, and treatment of infections in humans and experimental animals. Clin. Infect. Dis. 1998, 26(1):151-164.
7. Centers for Disease Control Prevention (CDC) Three sudden cardiac deaths associated with Lyme carditis - United States, November 2012-July 2013. MMWR 2013, 62(49):993-996.
8. Chowdri H.R., Gugliotta J.L., Berardi V.P., Goethert H.K., Molloy P.J., Sterling S.L., Telford S.R. Borrelia miyamotoi infection presenting as human granulocytic anaplasmosis: a case report. Ann. Intern. Med. 2013, 159(1):21-27. 10.7326/0003-4819-159-1-201307020-00005.
9. Cochez C., Heyman P., Heylen D., Fonville M., Hengeveld P., Takken W., Simons L., Sprong H. The Presence of Borrelia miyamotoi, A Relapsing Fever Spirochaete, in Questing Ixodes ricinus in Belgium and in The Netherlands. Zoonoses Public Health 2014, 10.1111/zph.12154.
10. Cosson J.F., Michelet L., Chotte J., Le Naour E., Cote M., Devillers E., Poulle M.-L., Huet D., Galan M., Geller J., Moutailler S., Vayssier-Taussat M. Genetic characterization of the human relapsing fever spirochete Borrelia miyamotoi in vectors and animal reservoirs of Lyme disease spirochetes in France. Parasit. Vectors 2014, 7:233. 10.1186/1756-3305-7-233.
11. Crowder C.D., Carolan H.E., Rounds M.A., Honig V., Mothes B., Haag H., Nolte O., Luft B.J., Grubhoffer L., Ecker D.J., Schutzer A.E., Eshoo M.W. Prevalence of Borrelia miyamotoi in Ixodes ticks in Europe and the United States. Emerg. Infect. Dis. 2014, 20(10):1678-1682. 10.3201/eid2010.131583.
12. Cutler S.J. Relapsing fever-a forgotten disease revealed. J. Appl. Microbiol. 2010, 108(4):1115-1122. 10.1111/j. 1365-2672.2009.04598.x.
13. Dibernardo A., Cote T., Ogden N.H., Lindsay L.R. The prevalence of Borrelia miyamotoi infection, and co-infections with other Borrelia spp. in Ixodes scapularis ticks collected in Canada. Parasit. Vectors 2014, 7:183. 10.1186/1756-3305-7-183.
14. Fraenkel C.J., Garpmo U., Berglund J. Determination of novel Borrelia genospecies in Swedish Ixodes ricinus ticks. J. Clin. Microbiol. 2002, 40(9):3308-3312.
15. Fukunaga M., Takahashi Y., Tsuruta Y., Matsushita O., Ralph D., McClelland M., Nakao M. Genetic and phenotypic analysis of Borrelia miyamotoi sp. nov., isolated from the ixodid tick Ixodes persulcatus, the vector for Lyme disease in Japan. Int. J. Syst. Bacteriol. 1995, 45(4):804-810.
16. Geller J., Nazarova L., Katargina O., Jarvekulg L., Fomenko N., Golovljova I. Detection and genetic characterization of relapsing fever spirochete Borrelia miyamotoi in Estonian ticks. PLoS ONE 2012, 7(12):e51914. 10.1371/journal.pone.0051914.
17. Gugliotta J.L., Goethert H.K., Berardi V.P., Telford S.R. Meningoencephalitis from Borrelia miyamotoi in an immunocompromised patient. N. Engl. J. Med. 2013, 368(3):240-245. 10.1056/NEJMoa1209039.
18. Hamer S.A., Hickling G.J., Keith R., Sidge J.L., Walker E.D., Tsao J.I. Associations of passerine birds, rabbits, and ticks with Borrelia miyamotoi and Borrelia andersonii in Michigan, U.S.A. Parasit. Vectors 2012, 5:231. 10.1186/1756-3305-5-231.
19. Hansford K.M., Fonville M., Jahfari S., Sprong H., Medlock J.M. Borrelia miyamotoi in host-seeking Ixodes ricinus ticks in England. Epidemiol. Infect. 2014, 1-9. 10.1017/S0950268814001691.
20. Hillyard P.D. Ticks of North-West Europe. Synopsis of the British Fauna (New Series) 1996, Vol. 52. Field Studies Council, Shrewsbury.
21. Hovius J.W., de Wever B., Sohne M., Brouwer M.C., Coumou J., Wagemakers A., Oei A., Knol H., Narasimhan S., Hodiamont C.J., Jahfari S., Pals S.T., Horlings H.M., Fikrig E., Sprong H., van Oers M.H. A case of meningoencephalitis by the relapsing fever spirochaete Borrelia miyamotoi in Europe. Lancet 2013, 382(9892):658. 10.1016/S0140-6736(13)61644-X.
22. Hulinska D., Votypka J., Kriz B., Holinkova N., Novakova J., Hulinsky V. Phenotypic and genotypic analysis of Borrelia spp. isolated from Ixodes ricinus ticks by using electrophoretic chips and real-time polymerase chain reaction. Folia Microbiol. (Praha) 2007, 52(4):315-324.
23. Jore S., Viljugrein H., Hofshagen M., Brun-Hansen H., Kristoffersen A.B., Nygard K., Brun E., Ottesen P., Saevik B.K., Ytrehus B. Multi-source analysis reveals latitudinal and altitudinal shifts in range of Ixodes ricinus at its northern distribution limit. Parasit. Vectors 2011, 4:84. 10.1186/1756-3305-4-84.
24. Kiewra D., Stanczak J., Richter M. Ixodes ricinus ticks (Acari, Ixodidae) as a vector of Borrelia burgdorferi sensu lato and Borrelia miyamotoi in Lower Silesia, Poland-preliminary study. Ticks Tick Borne Dis. 2014, 5(6):892-897. 10.1016/j.ttbdis.2014.07.004.
25. Kjelland V., Stuen S., Skarpaas T., Slettan A. Prevalence and genotypes of Borrelia burgdorferi sensu lato infection in Ixodes ricinus ticks in southern Norway. Scand. J. Infect. Dis. 2010, 42(8):579-585. 10.3109/00365541003716526.
26. Krause P.J., Narasimhan S., Wormser G.P., Rollend L., Fikrig E., Lepore T., Barbour A., Fish D. Human Borrelia miyamotoi infection in the United States. N. Engl. J. Med. 2013, 368(3):291-293. 10.1056/NEJMc1215469.
27. Kurtenbach K., Hanincova K., Tsao J.I., Margos G., Fish D., Ogden N.H. Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nat. Rev. Microbiol. 2006, 4(9):660-669. 10.1038/nrmicro1475.
28. Melkert P.W. Mortality in high risk patients with tick-borne relapsing fever analysed by the Borrelia-index. East Afr. Med. J. 1991, 68(11):875-879.
29. Michelet L., Delannoy S., Devillers E., Umhang G., Aspan A., Juremalm M., Chirico J., van der Wal F.J., Sprong H., Boye Phil T.P., Klitgaard K., Bodker R., Fach P., Moutailler S. High-throughput screening of tick-borne pathogens in Europe. Front. Cell. Infect. Microbiol. 2014, 4:103. 10.3389/fcimb.2014.00103.
30. Mun J., Eisen R.J., Eisen L., Lane R.S. Detection of a Borrelia miyamotoi sensu lato relapsing-fever group spirochete from Ixodes pacificus in California. J. Med. Entomol. 2006, 43(1):120-123.
31. Pichon B., Rogers M., Egan D., Gray J. Blood-meal analysis for the identification of reservoir hosts of tick-borne pathogens in Ireland. Vector Borne Zoonotic Dis. 2005, 5(2):172-180. 10.1089/vbz.2005.5.172.
32. Platonov A.E., Karan L.S., Kolyasnikova N.M., Makhneva N.A., Toporkova M.G., Maleev V.V., Fish D., Krause P.J. Humans infected with relapsing fever spirochete Borrelia miyamotoi, Russia. Emerg. Infect. Dis. 2011, 17(10):1816-1823. 10.3201/eid1710.101474.
33. Randolph S.E. Evidence that climate change has caused 'emergence' of tick-borne diseases in Europe?. Int. J. Med. Microbiol. 2004, 293(Suppl. 37):5-15.
34. Rauter C., Hartung T. Prevalence of Borrelia burgdorferi sensu lato genospecies in Ixodes ricinus ticks in Europe: a metaanalysis. Appl. Environ. Microbiol. 2005, 71(11):7203-7216. 10.1128/AEM.71.11. 7203-7216.2005.
35. Rebaudet S., Parola P. Epidemiology of relapsing fever borreliosis in Europe. FEMS Immunol. Med. Microbiol. 2006, 48(1):11-15. 10.1111/j.1574-95X.2006.00104.x.
36. Richter D., Schlee D.B., Matuschka F.R. Relapsing fever-like spirochetes infecting European vector tick of Lyme disease agent. Emerg. Infect. Dis. 2003, 9(6):697-701. 10.3201/eid0906.020459.
37. Richter D., Debski A., Hubalek Z., Matuschka F.R. Absence of Lyme disease spirochetes in larval Ixodes ricinus ticks. Vector Borne Zoonotic Dis. 2012, 12(1):21-27. 10.1089/vbz.2011.0668.
38. Scoles G.A., Papero M., Beati L., Fish D. A relapsing fever group spirochete transmitted by Ixodes scapularis ticks. Vector Borne Zoonotic Dis. 2001, 1(1):21-34.
39. Stanek G., Wormser G.P., Gray J., Strle F. Lyme borreliosis. Lancet 2012, 379(9814):461-473. 10.1016/S0140-6736(11)60103-7.
40. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 2013, 30:2725-2729.
41. Tsao J.I., Wootton J.T., Bunikis J., Luna M.G., Fish D., Barbour A.G. An ecological approach to preventing human infection: vaccinating wild mouse reservoirs intervenes in the Lyme disease cycle. Proc. Natl. Acad. Sci. U. S. A. 2004, 101(52):18159-18164. 10.1073/pnas.0405763102.
42. Vayssier-Taussat M., Moutailler S., Michelet L., Devillers E., Bonnet S., Cheval J., Hebert C., Eloit M. Next generation sequencing uncovers unexpected bacterial pathogens in ticks in western Europe. PLoS ONE 2013, 8(11):e81439. 10.1371/journal.pone.0081439.
43. Vial L., Diatta G., Tall A., Ba el H., Bouganali H., Durand P., Sokhna C., Rogier C., Renaud F., Trape J.F. Incidence of tick-borne relapsing fever in west Africa: longitudinal study. Lancet 2006, 368(9529):37-43. 10.1016/S0140-6736(06)68968-X.
44. Wilhelmsson P., Fryland L., Borjesson S., Nordgren J., Bergstrom 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(11):4169-4176. 10.1128/JCM. 01061-10.
45. 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 Aland Islands, Finland with different Lyme borreliosis incidences. PLoS ONE 2013, 8(11):e81433. 10.1371/journal.pone.0081433.