Eco-epidemiology of Borrelia miyamotoi and Lyme borreliosis spirochetes in a popular hunting and recreational forest area in Hungary

Parasites and Vectors

Volumn 8, Issue 1, 2015, Pages

  Szekeres, Sándor ^a   Coipan, Elena Claudia ^b   Rigó, Krisztina ^a   Majoros, Gábor ^a   Jahfari, Setareh ^b   Sprong, Hein ^b   Földvári, Gábor ^a  

^a SZENT ISTVÁN UNIVERSITY   (Hungary)

^b NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

Author keywords

Apodemus flavicollis; Borrelia burgdorferi sensu lato; Borrelia miyamotoi; Endophilic pathogen cycle; Hungary; Hunters; Ixodes acuminatus; Rodents; Ticks

Indexed keywords

ANIMAL EUTHANASIA; ANIMAL HUNTING; ANIMAL TISSUE; APODEMUS FLAVICOLLIS; ARTHROPOD LARVA; ARTICLE; BACTERIAL GENE; BIOGEOGRAPHIC REGION; BORRELIA; BORRELIA AFZELII; BORRELIA BURGDORFERI; BORRELIA INFECTION; BORRELIA MIYAMOTOI; CONTROLLED STUDY; DERMACENTOR MARGINATUS; DNA SEQUENCE; ECOLOGICAL GENETICS; FEMALE; FLAGELLIN GENE; FOREST; FORESTRY; GENE AMPLIFICATION; GENE IDENTIFICATION; GENE LOCATION; GENE TARGETING; GENETIC EPIDEMIOLOGY; HOST PATHOGEN INTERACTION; HUNGARY; INFECTION RISK; IXODES RICINUS; MALE; MULTIPLEX POLYMERASE CHAIN REACTION; MYODES GLAREOLUS; NONHUMAN; ORGANISM COMMUNITY; PARASITE PREVALENCE; POPULATION CYCLE; QUANTITATIVE STUDY; RAT; REAL TIME POLYMERASE CHAIN REACTION; RECREATION; SEQUENCE HOMOLOGY; SEX DIFFERENCE; SKIN; SPECIES HABITAT; SPLEEN; STRAIN DIFFERENCE; TICK; TISSUE DISTRIBUTION; ANIMAL; CLASSIFICATION; ECOSYSTEM; GENETICS; INSECT VECTOR; ISOLATION AND PURIFICATION; MICROBIOLOGY; PARASITOLOGY; RODENT; TICK INFESTATION; VETERINARY;

APODEMUS; APODEMUS FLAVICOLLIS; BORRELIA BURGDORFERI; BORRELIA BURGDORFERI GROUP; BORRELIA MIYAMOTOI; DERMACENTOR MARGINATUS; IXODES ACUMINATUS; IXODES RICINUS; IXODIDA; MAMMALIA; RODENTIA; SPIROCHAETALES;

ANIMALS; BORRELIA; ECOSYSTEM; FORESTS; HUNGARY; INSECT VECTORS; MULTIPLEX POLYMERASE CHAIN REACTION; REAL-TIME POLYMERASE CHAIN REACTION; RODENTIA; TICK INFESTATIONS; TICKS;

EID: 84934912483     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/s13071-015-0922-2     Document Type: Article

References (55)

1. Silaghi C, Woll D, Mahling M, Pfister K, Pfeffer M. Candidatus Neoehrlichia mikurensis in rodents in an area with sympatric existence of the hard ticks Ixodes ricinus and Dermacentor reticulatus, Germany. Parasit Vectors. 2012;5:285.
2. Ostfeld RS, Levi T, Jolles AE, Martin LB, Hosseini PR, Keesing F. Life History and Demographic Drivers of Reservoir Competence for Three Tick-Borne Zoonotic Pathogens. PLoS One. 2014;9:e107387.
3. Oliver JH, Lin T, Gao L, Clark KL, Banks CW, Durden LA, et al. An enzootic transmission cycle of Lyme borreliosis spirochetes in the southeastern United States. Proc Natl Acad Sci. 2003;100(20):11642-5.
4. Estrada-Peña A, de la Fuente J. The ecology of ticks and epidemiology of tick-borne viral diseases. Antiviral Res. 2014;108:104-28.
5. Rizzoli A, Silaghi C, Obiegala A, Rudolf I, Hubalek Z, Foldvari G, et al. Ixodes ricinus and its transmitted pathogens in urban and peri-urban areas in Europe: new hazards and relevance for public health. Front public Heal. 2014;2:251.
6. Jahfari S, Herremans T, Platonov AE, Kuiper H, Karan LS, Vasilieva O, et al. High seroprevalence of Borrelia miyamotoi antibodies in forestry workers and individuals suspected of human granulocytic anaplasmosis in the Netherlands. New Microbes New Infect. 2014;2:144-9.
7. Lakos A, Igari Z, Solymosi N. Recent lesson from a clinical and seroepidemiological survey: low positive predictive value of Borrelia burgdorferi antibody testing in a high risk population. Adv Med Sci. 2012;57:356-63.
8. Cetin E, Sotoudeh M, Auer H, Stanek G. Paradigm Burgenland: risk of Borrelia burgdorferi sensu lato infection indicated by variable seroprevalence rates in hunters. Wien Klin Wochenschr. 2006;118:677-81.
9. Pugliese A, Beltramo T, Torre D. Seroprevalence study of Tick-borne encephalitis, Borrelia burgdorferi, Dengue and Toscana virus in Turin Province. Cell Biochem Funct. 2007;25:185-8.
10. Nuti M, Serafini DA, Bassetti D, Ghionni A, Russino F, Rombolà P, et al. Ehrlichia Infection in Italy. Emerg Infect Dis. 1998;4:663-5.
11. Kubo N, Arashima Y, Yoshida M, Kawabata M, Nishinarita S, Hayama T, et al. Qestionnaire Surveys of Cases of Tick Bite and Lyme Borreliosis in Hunters in Hokkaido with Reference to Detection of Anti-Borrelia burgdorferi Antibody. Intern Med. 1992;31:1163-8.
12. Nováková M, Víchová B, Majláthová V, Lesnáková A, Pochybová M, Pe'tko B. Fist case of human granulocytic anaplasmosis from Slovakia. Ann Agric Env Med. 2010;17:173-5.
13. Jansen A, La Scola B, Raoult D, Lierz M, Wichmann O, Stark K, et al. Antibodies against Rickettsia spp. in Hunters, Germany. Emerg Infect Dis. 2008;14:1961-3.
14. Platonov AE, Maleev VV, Karan' LS. Relapsing borrelioses fevers: forgotten and new ones. Ter Arkh. 2010;82:74-80.
15. Raoult D, Birtles RJ, Montoya M, Perez E, Tissot-Dupont H, Roux V, et al. Survey of three bacterial louse-associated diseases among rural Andean communities in Peru: prevalence of epidemic typhus, trench fever, and relapsing fever. Clin Infect Dis. 1999;29:434-6.
16. Fukunaga M, Takahashi Y, Tsuruta Y, Matsushita O, Ralph D, McClelland M, et al. 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;45:804-10.
17. Fukunaga M, Koreki Y. The flagellin gene of Borrelia miyamotoi sp. nov. and its phylogenetic relationship among Borrelia species. FEMS Microbiol Lett. 1995;134:255-8.
18. Richter D, Schlee DB, Matuschka F-R. Relapsing fever-like spirochetes infecting European vector tick of Lyme disease agent. Emerg Infect Dis. 2003;9:697-701.
19. Geller J, Nazarova L, Katargina O, Järvekülg L, Fomenko N, Golovljova I. Detection and genetic characterization of relapsing fever spirochete Borrelia miyamotoi in Estonian ticks. PLoS One. 2012;7:e51914.
20. Kiewra D, Stańczak 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;5:892-7.
21. Michelet L, Delannoy S, Devillers E, Umhang G, Aspan A, Juremalm M, et al. High-throughput screening of tick-borne pathogens in Europe. Front Cell Infect Microbiol. 2014;4.
22. 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:in press.
23. Tijsse-Klasen E, Koopmans MPG, Sprong H. Tick-borne pathogen - reversed and conventional discovery of disease. Front Public Heal. 2014;2:73.
24. Platonov AE, Karan LS, Kolyasnikova NM, Makhneva NA, Toporkova MG, Maleev VV, et al. Humans Infected with Relapsing Fever Spirochete Borrelia, Russia. Emerg Infect Dis. 2011;17:1816-23.
25. Krause PJ, Narasimhan S, Wormser GP, Rollend L, Fikrig E, Lepore T, et al. Human Borrelia miyamotoi Infection in the United States. N Engl J Med. 2013;368:291-3.
26. Hovius JWR, de Wever B, Sohne M, Brouwer MC, Coumou J, Wagemakers A, et al. A case of meningoencephalitis by the relapsing fever spirochaete Borrelia miyamotoi in Europe. Lancet. 2013;382:658.
27. Stanek G, Wormser GP, Gray J, Strle F. Lyme borreliosis. Lancet. 2012;379:461-73.
28. Zöldi V, Juhász A, Nagy C, Papp Z, Egyed L. Tick-borne encephalitis and lyme disease in Hungary: the epidemiological situation between 1998 and 2008. Vector Borne Zoonotic Dis. 2013;13:256-65.
29. Lakos A. Lyme borreliosis-experience of the last 25 years in Hungary. Orv Hetil. 2009;150:725-32.
30. Crowder CD, Carolan HE, Rounds MA, Honig V, Mothes B, Haag H, et al. Prevalence of Borrelia miyamotoi in Ixodes Ticks in Europe and the United States. Emerg Infect Dis. 2014;20:1678-82.
31. Cosson J-F, Michelet L, Chotte J, Le Naour E, Cote M, Devillers E, et al. 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.
32. Scoles GA, Papero M, Beati L, Fish D. A Relapsing Fever Group Spirochete Transmitted by Ixodes scapularis Ticks. Vector Borne Zoonotic Dis. 2001;1:21-34.
33. Burri C, Schumann O, Schumann C, Gern L. Are Apodemus spp. mice and Myodes glareolus reservoirs for Borrelia miyamotoi, Candidatus Neoehrlichia mikurensis, Rickettsia helvetica, R. monacensis and Anaplasma phagocytophilum? Ticks Tick Borne Dis. 2014;5:245-51.
34. Szekeres S, Coipan EC, Rigó K, Majoros G, Jahfari S, Sprong H, et al. Candidatus Neoehrlichia mikurensis and Anaplasma phagocytophilum in natural rodent and tick communities in Southern Hungary. Ticks Tick Borne Dis. 2015;6:111-6.
35. Heylen D, Tijsse E, Fonville M, Matthysen E, Sprong H. Transmission dynamics of Borrelia burgdorferi s.l. in a bird tick community. Environ Microbiol. 2013;15:663-73.
36. Coipan EC, Fonville M, Tijsse-Klasen E, van der Giessen JWB, Takken W, Sprong H, et al. Geodemographic analysis of Borrelia burgdorferi sensu lato using the 5S-23S rDNA spacer region. Infect Genet Evol. 2013;17:216-22.
37. The R Development Core Team. R: A Language and Environment for Statistical Computing. Volume 1. 2010.
38. Rózsa L, Reiczigel J, Majoros G. Quantifying parasites in samples of hosts. J Parasitol. 2000;86:228-32.
39. Egyed L, Elo P, Sréter-Lancz Z, Széll Z, Balogh Z, Sréter T. Seasonal activity and tick-borne pathogen infection rates of Ixodes ricinus ticks in Hungary. Ticks Tick Borne Dis. 2012;3:90-4.
40. Földvári G, Rigó K, Majláthová V, Majláth I, Farkas R, Pet'ko B. Detection of Borrelia burgdorferi sensu lato in lizards and their ticks from Hungary. Vector Borne Zoonotic Dis. 2009;9:331-6.
41. Majláthová V, Majláth I, Derdáková M, Víchová B, Petko B. Borrelia lusitaniae and Green Lizards (Lacerta viridis), Karst Region, Slovakia. Emerg Infect Dis. 2006;12:1895-901.
42. Mayer J. The vertebrates of Béda-Karapancsa landscape protection area, South Hungary. Dunántúli Dolg Természetudományi Sor. 1992;6:257-72.
43. Collares-Pereira M, Couceiro S, Franca I, Kurtenbach K, Scha SM, Baptista S, et al. First Isolation of Borrelia lusitaniae from a Human Patient. J Clin Microbiol. 2004;42:1316-8.
44. Rigó K, Gyuranecz M, Tóth AG, Földvári G. Detection of Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum in small mammals and ectoparasites in Hungary. Vector Borne Zoonotic Dis. 2011;11:1499-501.
45. Földvári G, Farkas R, Lakos A. Borrelia spielmanii Erythema Migrans, Hungary. Emerg Infect Dis. 2005;11:2004-5.
46. Bown KJ, Begon M, Bennett M, Birtles RJ, Burthe S, Lambin X, et al. Sympatric Ixodes trianguliceps and Ixodes ricinus Ticks Feeding on Field Voles (Microtus agrestis): Potential for Increased Risk of Anaplasma phagocytophilum in the United Kingdom? Vector-borne Zoonotic Dis. 2006;6:404-10.
47. Bown KJ, Lambin X, Telford GR, Ogden NH, Telfer S, Woldehiwet Z, et al. Relative importance of Ixodes ricinus and Ixodes trianguliceps as vectors for Anaplasma phagocytophilum and Babesia microti in field vole (Microtus agrestis) populations. Appl Environ Microbiol. 2008;74:7118-25.
48. Petney TN, Moser E, Littwin N, Pfäffle M, Senta V, Taraschewski H. Additions to the "Annotated Checklist of the Ticks of Germany": Ixodes acuminatus and Ixodes inopinatus. Syst Appl Acarol Acarol. 2015;20:221-4.
49. Gern L, Rouvinez E, Toutoungi LEG. Transmission cycles of Borrelia burgdorferi sensu lato involving Ixodes ricinus and/or I. hexagonus ticks and the European hedgehog, Erinaceus europaeus, in suburban and urban areas in Switzerland. Folia Parasitol (Praha). 1997;44:309-14.
50. Hillyard P. Ticks of North-West Europe. Shrewsbury: Field Studies Council; 1996.
51. Kahl O, Janetzki C, Gray J, Stein J, Bauch R. Tick infection rates with Borrelia: Ixodes ricinus versus Haemaphysalis concinna and Dermacentor reticulatus in two locations in eastern Germany. Med Vet Entomol. 1992;6:363-6.
52. Gray J, Kahl O, Lane RS, Stanek G. Lyme Borreliosis Biology, Epidemiology and Control. 2002.
53. Földvári G, Rigó K, Lakos A. Transmission of Rickettsia slovaca and Rickettsia raoultii by male Dermacentor marginatus and Dermacentor reticulatus ticks to humans. Diagn Microbiol Infect Dis. 2013;76:387-9.
54. Kurtenbach K, De Michelis S, Etti S, Schäfer SM, Sewell H-S, Brade V, et al. Host association of Borrelia burgdorferi sensu lato-the key role of host complement. Trends Microbiol. 2002;10:74-9.
55. Pacilly FCA, Benning ME, Jacobs F, Leidekker J, Sprong H, Van Wieren SE, et al. Blood feeding on large grazers affects the transmission of Borrelia burgdorferi sensu lato by Ixodes ricinus. Ticks Tick Borne Dis. 2014;5:810-7.