Occurrence of Borrelia burgdorferi s.l. in different genera of mosquitoes (Culicidae) in Central Europe

Ticks and Tick-borne Diseases

Volumn 7, Issue 2, 2016, Pages 256-263

  Melaun, Christian ^a   Zotzmann, Sina ^a   Santaella, Vanesa Garcia ^a   Werblow, Antje ^a   Zumkowski Xylander, Helga ^b   Kraiczy, Peter ^c   Klimpel, Sven ^a  

^a GOETHE UNIVERSITY   (Germany)

^b SENCKENBERG MUSEUM OF NATURAL HISTORY GÖRLITZ   (Germany)

^c UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

Borrelia burgdorferi complex; Culicidae; Lyme borreliosis; Mosquitoes; Spirochetes

Indexed keywords

BACTERIAL DNA; FLAGELLIN; OUTER SURFACE PROTEIN A; SUBUNIT B OF FLAGELLIN; UNCLASSIFIED DRUG; BACTERIAL VACCINE; FLAB FLAGELLIN; LIPOPROTEIN; MEMBRANE ANTIGEN; OUTER MEMBRANE PROTEIN;

ADULT; AEDES; ARTICLE; BACTERIAL GENE; BACTERIAL TRANSMISSION; BACTERIUM IDENTIFICATION; BORRELIA AFZELII; BORRELIA BAVARIENSIS; BORRELIA BURGDORFERI; BORRELIA GARINII; CENTRAL EUROPE; CONTROLLED STUDY; CULEX; CULISETA; EMBRYO; EUROPE; FEMALE; FLAB GENE; GERMANY; LARVA; MOSQUITO; NONHUMAN; NUCLEOTIDE SEQUENCE; OCHLEROTATUS; OSPA GENE; PRIORITY JOURNAL; ANIMAL; BORRELIA; DNA SEQUENCE; GENETICS; GEOGRAPHY; INSECT VECTOR; ISOLATION AND PURIFICATION; LYME DISEASE; MICROBIOLOGY; TRANSMISSION;

ANIMALS; ANTIGENS, SURFACE; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL VACCINES; BORRELIA; BORRELIA BURGDORFERI; CULICIDAE; FEMALE; FLAGELLIN; GEOGRAPHY; GERMANY; INSECT VECTORS; LARVA; LIPOPROTEINS; LYME DISEASE; SEQUENCE ANALYSIS, DNA;

EID: 84958927610     PISSN: 1877959X     EISSN: 18779603     Source Type: Journal    
DOI: 10.1016/j.ttbdis.2015.10.018     Document Type: Article

References (58)

1. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
2. Becker N., Petric D., Zgomba M., Boase C., Dahl C., Lane J., Kaiser A. Mosquitoes and Their Control 2010, Kluwer Academic/Plenum, New York, NY.
3. Bigl S., Müller L., Pönitz G., Mickel C., Klapper B.M. Untersuchungen zur Epidemiologie der Borreliose im Freistaat Sachsen 1997 Verbreitung von Borrelia burgdorferi in Zecken. Bundesgesundheitsbln Gesundh. Gesundh. 1999, 42:219-225.
4. Bingsohn L., Beckert A., Zehner R., Kuch U., Oehme R., Kraiczy P., Amendt J. Prevalences of tick-borne encephalitis virus and Borrelia burgdorferi sensu lato in Ixodes ricinus populations of the Rhine-Main region, Germany. Ticks Tick Borne Dis. 2013, 4:207-213. 10.1016/j.ttbdis.2012.11.012.
5. Casjens S.R., Fraser-Liggett C.M., Mongodin E.F., Qiu W.G., Dunn J.J., Luft B.J., Schutzer S.E. Whole genome sequence of an unusual Borrelia burgdorferi sensu lato isolate. J. Bacteriol. 2011, 193:1489-1490.
6. Cisak E., Wójcik-Fatla A., Stojek N.M., Chmielewska-Badora J., Zwoliński J., Buczek A., Dutkiewicz J. Prevalence of Borrelia burgdorferi genospecies in Ixodes ricinus ticks from Lublin region (Eastern Poland). Ann. Agric. Environ. Med. 2006, 13:301-306.
7. Doby J.M., Anderson J.F., Coutarmanach A., Magnarelli L.A., Martin A. Lyme disease in Canada with possible transmission by an insect. Zbl. Bakt. Hyg. A 1986, 263:488-490.
8. Gern L. Life cycle of Borrelia burgdorferi sensu lato and transmission to humans. Lyme Borreliosis. Curr. Probl. Dermatol. 2009, 37:18-30.
9. Grimm D., Tilly K., Byram R., Stewart P.E., Krum J.G., Bueschel D.M., Schwan T.G., Policastro P.F., Elias A.F., Rosa P.A. Outer-surface protein C of the Lyme disease spirochete: a protein induced in ticks for infection of mammals. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:3142-3147. 10.1073/pnas.0306845101.
10. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999, 41:95-98.
11. Halouzka J. Borreliae in Aedes vexans and hibernating Culex pipiens molestus mosquitoes. Biologia (Bratisl.) 1998, 48:123-124.
12. Halouzka J., Postic D., Hubálek Z. Isolation of the spirochaete Borrelia afzelii from the mosquito Aedes vexans in the Czech Republic. Med. Vet. Entomol. 1998, 12:103-105.
13. Halouzka J., Wilske B., Stünzner D., Sanoge Y.O., Hubálek Z. Isolation of Borrelia afzelii from overwintering Culex pipiens biotype molestus mosquitoes. Infection 1999, 27:275-277.
14. Hård S. Erythema chronicum migrans (Afzelii) associated with mosquito bite. Acta Derm. Venerol. 1966, 46:473-476.
15. Hildebrandt A., Schmidt K.H., Wilske B., Dorn W., Straube E., Fingerle V. Prevalence of four species of Borrelia burgdorferi sensu lato and coinfection with Anaplasma phagocytophila in Ixodes ricinus ticks in central Germany. Eur. J. Microbiol. Infect. Dis. 2003, 22:364-367.
16. Hubalek Z., Halouzka J. Prevalence rates of Borrelia burgdorferi sensu lato in host-seeking Ixodes ricinus ticks in Europe. Parasitol. Res. 1998, 84:167-172.
17. Ivanova L.B., Tomova A., González-Acuña D., Murúa R., Moreno C.X., Hernández C., Cabello J., Cabello C., Daniels T.J., Godfrey H.P., Cabello F.C. Borrelia chilensis, a new member of the Borrelia burgdorferi sensu lato complex that extends the range of this genospecies in the southern hemisphere. Environ. Microbiol. 2014, 16:1069-1080. 10.1111/1462-2920.12310.
18. Ivanova N.V., deWaard J., Hebert P.D.N. An inexpensive, automation-friendly protocol for recovering high quality DNA. Mol. Ecol. Notes 2006, 6:998-1002.
19. Jaffé J. Spirochaeta culicis nov. spec. Arch. F. Protist. 1907, 9:100-107.
20. Kahl O., Gern L., Gray J.S., Guy E.C., Jongejan F., Kirstein F., Kurtenbach K., Rijpkema S.G.T., Stanek G. Detection of Borrelia burgdorferi sensu lato in ticks: immunofluorescence assay versus polymerase chain reaction. Zentralbl. Bacteriol. Microbiol. Hyg. 1998, 287:205-210.
21. Kosik-Bogacka D., Bukowska K., Kuźna-Grygiel W. Detection of Borrelia burgdorferi sensu lato in mosquitoes (Culicidae) in recreation areas of the city of Szczecin. Ann. Agric. Environ. Med. 2002, 9:55-57.
22. Kosik-Bogacka D., Kuźna-Grygiel W., Bukowska K. The prevalence of spirochaete Borrelia burgdorferi sensu lato in ticks Ixodes ricinus and mosquitoes Aëdes spp. within a selected recreational area in the city of Szczecin. Ann. Agric. Environ. Med. 2004, 11:105-108.
23. Kosik-Bogacka D., Kuźna-Grygiel W., Górnik K. Borrelia burgdorferi sensu lato infection in mosquitoes from Szczecin area. Folia Biol. 2006, 54:55-59.
24. Kosik-Bogacka D., Kuźna-Grygiel W., Jamborowska M. Ticks and mosquitoes as vectors of Borrelia burgdorferi s.l. in the forested areas of Szczecin. Folia Biol. 2007, 55:143-146.
25. Kurtenbach K., De Michelis S., Sewell H.S., Etti S., Schäfer S.M., Hails R., Collares-Pereira M., Santos-Reis M., Haninçová K., Labuda M., Bormane A., Donaghy M. Distinct combinations of Borrelia burgdorferi sensu lato genospecies found in individual questing ticks from Europe. Appl. Environ. Microbiol. 2001, 67:4926-4929.
26. Li X., Neelakanta G., Liu X., Beck D.S., Kantor F.S., Fish D., Anderson J.F., Fikrig E. Role of outer surface protein D in the Borrelia burgdorferi life cycle. Infect. Immun. 2007, 75:4237-4244. 10.1128/IAI.00632-07.
27. Luger S.W. Lyme disease transmitted by a biting fly. N. Engl. J. Med. 1990, 322:1752.
28. Lundström J.O., Andersson A.C., Bäckman S., Schäfer M.L., Forsman M., Thelaus J. Transstadial transmission of Francisella tularensis holarctica in mosquitoes, Sweden. Emerg. Infect. Dis. 2011, 17:794-799. 10.3201/eid1705.100426.
29. Maetzel D., Maier W.A., Kampen H. Borrelia burgdorferi infection prevalences in questing Ixodes ricinus ticks (Acari: Ixodidae) in urban and suburban Bonn, western Germany. Parasitol. Res. 2005, 95:5-12.
30. Magnarelli L.A., Anderson J.F., Barbour A.G. The etiologic agent of Lyme disease in deer flies, horse flies and mosqitoes. J. Infect. Dis. 1986, 154:355-358.
31. Magnarelli L.A., Freier J.E., Anderson J.F. Experimental infections of mosquitoes with Borrelia burgdorferi, the etiologic agent of Lyme disease. J. Infect. Dis. 1987, 156:694-695.
32. Magnarelli L.A., Anderson J.F. Ticks and biting insects infected with the etiologic agent of Lyme disease, Borrelia burgdorferi. J. Clin. Microbiol. 1988, 26:1482-1486.
33. Matuschka F.J., Richter D. Mosquitoes and soft ticks cannot transmit Lyme disease spirochetes. Parasitol. Res. 2002, 88:283-284. 10.1007/s00436-001-0584-1.
34. Margos G., Wilske B., Sing A., Hizo-Teufel C., Cao W.C., Chu C., Scholz H., Straubinger R.K., Fingerle V. Borrelia bavariensis sp. nov. is widely distributed in Europe and Asia. Int. J. Syst. Evol. Microbiol. 2013, 63:4284-4288. 10.1099/ijs.0.052001-0.
35. Mohrig W. Die Culiciden Deutschlands. Parasitologische Schriftenreihe 1969, vol. 18. Gustav Fischer Verlag, Jena.
36. Morens D.M., Folkers G.K., Fauci A.S. The challenge of emerging and re-emerging infectious diseases. Nature 2004, 430:242-249.
37. Nejedlá P., Norek A., Vostal K., Žákovska A. What is the percentage of pathogenic Borrelia in spirochaetal findings of mosquito larvae. Ann. Agric. Environ. Med. 2009, 16:273-276.
38. Pal U., Yang X., Chen M., Bockenstedt L.K., Anderson J.F., Flavell R.A., Norgard M.V., Fikrig E. OspC facilitates Borrelia burgdorferi invasion of Ixodes scapularis salivary glands. J. Clin. Invest. 2004, 113:220-230. PMC 311436. PMID 14722614. 10.1172/JCI19894.
39. Pal U., Li X., Wang T., Montgomery R.R., Ramamoorthi N., Desilva A.M., Bao F., Yang X., Pypaert M., Pradhan D., Kantor F.S., Telford S., Anderson J.F., Fikrig E. TROSPA, an Ixodes scapularis receptor for Borrelia burgdorferi. Cell 2004, 119:457-468. 10.1016/j.cell.2004.10.027.
40. Picken R.N. Polymerase chain reaction primers and probes derived from flagellin gene sequences for specific detection of the agents of lyme disease and North American relapsing fever. J. Clin. Microbiol. 1992, 30:99-114.
41. Picken M.M., Picken R.N., Han D., Cheng Y., Strle F. Single-tube nested polymerase chain reaction assay based on flagellin gene sequences for detection of Borrelia burgdorferi sensu lato. Eur. J. Clin. Microbiol. Infect. Dis. 1996, 15:489-498.
42. Rauter C., Hartung T. Prevalence of Borrelia burgdorferi sensu lato genospecies in Ixodes ricinus ticks in Europe: a metaanalysis. Appl. Environ. Microbiol. 2005, 71:7203-7216.
43. Rijpkema S.G., Tazelaar T., Molkenboer M., Noordhoek G., Plantinga G., Schouls L.M., Schellekens J.E. Detection of Borrelia afzelii, Borrelia burgdorferi sensu stricto, Borrelia garinii and group VS116 by PCR in skin biopsies of patients with erythema migrans and acrodermatitis chronica atrophicans. Clin. Microbiol. Infect. 1997, 3:109-116.
44. Rizzoli A., Hauffe H.C., Carpi G., Vourc'h G.I., Neteler M., Rosà R. Lyme borreliosis in Europe. Eur. Surveill. 2011, 16(27). pii=19906.
45. Rudenko N., Golovchenko M., Grubhoffer L., Oliver J.H. Updates on Borrelia burgdorferi sensu lato complex with respect to public health. Ticks Tick Borne Dis. 2011, 2:123-128. 10.1016/j.ttbdis.2011.04.002.
46. Sanogo Y.O., Halouzka J., Hubálek Z., Němec M. Detection of spirochetes in, and isolation from, culicine mosquitoes. Folia Parasitol. 2000, 47:79-80.
47. Schuijt T.J., Hovius J.W., van Burgel N.D., Ramamoorthi N., Fikrig E., van Dam A.P. The tick salivary protein Salp15 inhibits the killing of serum-sensitive Borrelia burgdorferi sensu lato isolates. Infect. Immun. 2008, 76:2888-2894. 10.1128/IAI.00232-08.
48. Schwan T.G., Piesman J. Temporal changes in outer surface proteins A and C of the Lyme disease-associated spirochete, Borrelia burgdorferi, during the chain of infection in ticks and mice. J. Clin. Microbiol. 2000, 38:382-388.
49. Sinton J.A., Shute P.G. Spirochaetal infections of mosquitoes. J. Trop. Med. Hyg. 1939, 42:125-126.
50. Skotarczak B. Why are there several species of Borrelia burgdorferi sensu lato detected in dogs and humans?. Infect. Genet. Evol. 2014, 23:182-188. 10.1016/j.meegid.2014.02.014.
51. Skuballa J., Petney T., Pfäffle M., Oehme R., Hartelt K., Fingerle V., Kimmig P., Taraschewski H. Occurrence of different Borrelia burgdorferi sensu lato genospecies including B. afzelii, B. bavariensis, and B. spielmanii in hedgehogs (Erinaceus spp.) in Europe. Ticks Tick Borne Dis. 2012, 3:8-13. 10.1016/j.ttbdis.2011.09.008.
52. Thelaus J., Andersson A., Broman T., Bäckman S., Granberg M., Karlsson L., Kuoppa K., Larsson E., Lundmark E., Lundström J.O., Mathisen P., Näslund J., Schäfer M., Wahab T., Forsman M. Francisella tularensis subspecies holarctica occurs in Swedish mosquitoes, persists through the developmental stages of laboratory-infected mosquitoes and is transmissible during blood feeding. Microb. Ecol. 2014, 67:96-107. 10.1007/s00248-013-0285-1.
53. Tilly K., Krum J.G., Bestor A., Jewett M.W., Grimm D., Bueschel D., Byram R., Dorward D., Vanraden M.J., Stewart P., Rosa P. Borrelia burgdorferi OspC protein required exclusively in a crucial early stage of mammalian infection. Infect. Immun. 2006, 74:3554-3564. 10.1128/IAI.01950-05.
54. Vennestrøm J., Egholm H., Jensen P.M. Occurrence of multiple infections with different Borrelia burgdorferi genospecies in Danish Ixodes ricinus nymphs. Parasitol. Int. 2008, 57:32-37.
55. Wodecka B., Leońska A., Skotarczak B. A comparative analysis of molecular markers for the detection and identification of Borrelia spirochetes in Ixodes ricinus. J. Med. Microbiol. 2010, 59:309-314. 10.1099/jmm.0.0135.08-0.
56. Žákovska A., Jörkova M., Šerý O., Dendis M. Spirochetes in Culex (C.) pipiens s.l. larvae. Biologia (Bratisl.) 2004, 59:283-287.
57. Žákovska A., Čapková L., Šerý O., Halouzka J., Dendis M. Isolation of Borrelia afzelii from overwintering Culex pipiens biotype molestus mosquitoes. Ann. Agric. Environ. Med. 2006, 13:345-348.
58. Zeman P. Borrelia infection rates in ticks and vectors accompanying human risk acquiring Lyme borreliosis in a highly endemic region in Central Europe. Folia Parasitol. 1998, 45:319-325.