Candidatus Neoehrlichia mikurensis and Anaplasma phagocytophilum in natural rodent and tick communities in Southern Hungary

Ticks and Tick-borne Diseases

Volumn 6, Issue 2, 2015, Pages 111-116

  Szekeres, Sándor ^a   Claudia Coipan, Elena ^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

Anaplasma phagocytophilum; Candidatus neoehrlichia mikurensis; Hungary; Prevalence; Rodent; Tick

Indexed keywords

ALCOHOL; BACTERIAL DNA; HEAT SHOCK PROTEIN; MAJOR SURFACE PROTEIN 2; PROTEIN; UNCLASSIFIED DRUG;

ANAPLASMA PHAGOCYTOPHILUM; ANIMAL TISSUE; APODEMUS AGRARIUS; APODEMUS FLAVICOLLIS; ARTICLE; BACTERIAL INFECTION; BACTERIUM DETECTION; CANDIDATUS NEOEHRLICHIA MIKURENSIS; CANDIDATUS NEOEHRLICHIA MIKURENSIS INFECTION; CONTROLLED STUDY; DNA EXTRACTION; ECTOPARASITE; FEMALE; GENE; GROEL GENE; HUMAN GRANULOCYTIC ANAPLASMOSIS; HUNGARY; IXODES RICINUS; LIFE CYCLE STAGE; MALE; MICROTUS ARVALIS; MUS MUSCULUS; MYODES GLAREOLUS; NONHUMAN; NYMPH; PATHOPHYSIOLOGY; PREVALENCE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RICKETTSIALES; RODENT; SKIN; SPECIES DIFFERENTIATION; SPLEEN; TICK; TICK INFESTATION; TISSUE PRESERVATION; VEGETATION; ANAPLASMATACEAE; ANAPLASMATACEAE INFECTIONS; ANIMAL; EHRLICHIOSIS; GENETICS; HUMAN; ISOLATION AND PURIFICATION; IXODIDAE; MICROBIOLOGY; PARASITE VECTOR; VETERINARY;

ANAPLASMA PHAGOCYTOPHILUM; APODEMUS AGRARIUS; APODEMUS FLAVICOLLIS; CANDIDATUS NEOEHRLICHIA MIKURENSIS; DERMACENTOR RETICULATUS; HAEMAPHYSALIS CONCINNA; IXODES RICINUS; IXODIDA; MAMMALIA; MICROTUS ARVALIS; MUS MUSCULUS; RODENTIA;

ANAPLASMA PHAGOCYTOPHILUM; ANAPLASMATACEAE; ANAPLASMATACEAE INFECTIONS; ANIMALS; ARACHNID VECTORS; DNA, BACTERIAL; EHRLICHIOSIS; FEMALE; HUMANS; HUNGARY; IXODIDAE; MALE; PREVALENCE; RODENTIA;

EID: 84922008642     PISSN: 1877959X     EISSN: 18779603     Source Type: Journal    
DOI: 10.1016/j.ttbdis.2014.10.004     Document Type: Article

References (38)

1. Aulagnier S., Haffner P., Mitchell-Jones A., Moutou F., Zima J. Mammals of Europe, North Africa and the Middle East 2008, A & C Black Publishers Ltd, London.
2. Blaňarová L., Stanko M., Carpi G., Miklisová D., Víchová B., Mošanský L., Bona M., Derdáková M. Distinct Anaplasma phagocytophilum genotypes associated with Ixodes trianguliceps ticks and rodents in Central Europe. Ticks Tick. Borne. Dis. 2014, 5:928-938. 10.1016/j.ttbdis.2014.07.012.
3. Bown K.J., Begon M., Bennett M., Birtles R.J., Burthe S., Lambin X., Telfer S., Woldehiwet Z., Ogden N.H. 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, 6:404-410.
4. 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, 5:245-251. 10.1016/j.ttbdis.2013.11.007.
5. Cisarovsky G., Schmid-Hempel P. Few colonies of the host Bombus terrestris disproportionately affect the genetic diversity of its parasite, Crithidia bombi. Infect. Genet. Evol. 2014, 21:192-197. 10.1016/j.meegid.2013.11.010.
6. Courtney J.W., Kostelnik L.M., Zeidner N.S., Massung R.F. Multiplex real-time PCR for detection of Anaplasma phagocytophilum and Borrelia burgdorferi multiplex real-time PCR for detection of Anaplasma phagocytophilum and Borrelia burgdorferi. J. Clin. Microbiol. 2004, 42:3164-3168. 10.1128/JCM.42.7.3164.
7. Derdáková M., Václav R., Pangrácova-Blaňárová L., Selyemová D., Koči J., Walder G., Spitalská E. Candidatus Neoehrlichia mikurensis and its co-circulation with Anaplasma phagocytophilum in Ixodes ricinus ticks across ecologically different habitats of Central Europe. Parasit. Vectors 2014, 7:160. 10.1186/1756-3305-7-160.
8. 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, 3:90-94. 10.1016/j.ttbdis.2012.01.002.
9. Földvári G., Jahfari S., Rigó K., Jablonszky M., Szekeres S., Majoros G., Tóth M., Molnár V., Coipan E.C., Sprong H. Candidatus Neoehrlichia mikurensis and Anaplasma phagocytophilum in Urban Hedgehogs. Emerg. Infect. Dis. 2014, 20:496-498.
10. Földvári G., Rigó K., Jablonszky M., Biró N., Majoros G., Molnár V., Tóth M. Ticks and the city: ectoparasites of the Northern white-breasted hedgehog (Erinaceus roumanicus) in an urban park. Ticks Tick. Borne. Dis. 2011, 2:231-234. 10.1016/j.ttbdis.2011.09.001.
11. Grankvist A., Andersson P.-O., Mattsson M., Sender M., Vaht K., Höper L., Sakiniene E., Trysberg E., Stenson M., Fehr J., Pekova S., Bogdan C., Bloemberg G.C.W. Infections with the tick-borne bacterium Candidatus Neoehrlichia mikurensis mimic non-infectious conditions in patients with B cell malignancies or autoimmune diseases. Clin. Infect. Dis. 2014, 58:1716-1722.
12. Guy E.C., Stanek G. Detection of Borrelia burgdorferi in patients with Lyme disease by the polymerase chain reaction. J. Clin. Pathol. 1991, 44:610-611.
13. Hillyard P. Ticks of North-West Europe 1996, Field Studies Council, Shrewsbury.
14. Hornok S., Meli M.L., Gönczi E., Hofmann-Lehmann R. First evidence of Candidatus Neoehrlichia mikurensis in Hungary. Parasit. Vectors 2013, 6:267. 10.1186/1756-3305-6-267.
15. 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. 10.1186/1756-3305-5-8.
16. Jahfari S., Coipan E., Fonville M., Docters van Leeuwen A., Hengeveld P., Heylen D., Heyman P., van Maanen C., Butler C., Földvári G., Szekeres S., van Duijvendijk G., Tack W., Rijks J., van der Giessen J., Takken W., van Wieren S., Takumi K., Sprong H. Circulation of four Anaplasma phagocytophilum ecotypes in Europe. Parasit. Vectors 2014, 7:365.
17. Jahfari S., Fonville M., Hengeveld P., Reusken C., Scholte E.-J., Takken W., Heyman P., Medlock J., Heylen D., Kleve J., Sprong H. Prevalence of Neoehrlichia mikurensis in ticks and rodents from North-west Europe. Parasit. Vectors 2012, 5:74. 10.1186/1756-3305-5-74.
18. Kawahara M., Rikihisa Y., Isogai E., Takahashi M., Misumi H., Suto C., Shibata S., Zhang C., Tsuji M. Ultrastructure and phylogenetic analysis of "Candidatus Neoehrlichia mikurensis" in the family Anaplasmataceae, isolated from wild rats and found in Ixodes ovatus ticks. Int. J. Syst. Evol. Microbiol. 2004, 54:1837-1843. 10.1099/ijs.0.63260-0.
19. Khanakah G., Kocianová E., Vyrosteková V., Rehácek J., Kundi M., Stanek G. Seasonal variations in detecting Borrelia burgdorferi sensu lato in rodents from north eastern Austria. Wien. Klin. Wochenschr. 2006, 118:754-758. 10.1007/s00508-006-0730-y.
20. Kiffner C., Vor T., Hagedorn P., Niedrig M., Rühe F. Factors affecting patterns of tick parasitism on forest rodents in tick-borne encephalitis risk areas, Germany. Parasitol. Res. 2011, 108:323-335. 10.1007/s00436-010-2065-x.
21. Li H., Jiang J., Liu W., Zheng Y., Huo Q., Tang K., Zuo S., Liu K., Jiang B., Yang H., Cao W. Human infection with Candidatus Neoehrlichia mikurensis, China. Emerg. Infect. Dis. 2012, 18:10-13. 10.3201/eid1810.1205942012.
22. Medlock J.M., Hansford K.M., Bormane A., Derdakova M., Estrada-Peña A., George J.-C., Golovljova I., Jaenson T.G.T., Jensen J.-K., Jensen P.M., Kazimirova M., Oteo J.a, Papa A., Pfister K., Plantard O., Randolph S.E., Rizzoli A., Santos-Silva M.M., Sprong H., Vial L., Hendrickx G., Zeller H., Van Bortel W. Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasit. Vectors 2013, 6:1. 10.1186/1756-3305-6-1.
23. Nosek J., Sixl W. Central-European Ticks (Ixodoidea). Key for Determination 1972, D. Jahrbuch (Ed.).
24. Oliver J.H., Lin T., Gao L., Clark K.L., Banks C.W., Durden L.A., James A.M., Chandler F.W. An enzootic transmission cycle of Lyme borreliosis spirochetes in the southeastern United States. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:11642-11645. 10.1073/pnas.1434553100.
25. Pekova S., Vydra J., Kabickova H., Frankova S., Haugvicova R., Mazal O., Cmejla R., Hardekopf D.W., Jancuskova T., Kozak T. Candidatus Neoehrlichia mikurensis infection identified in 2 hematooncologic patients: benefit of molecular techniques for rare pathogen detection. Diagn. Microbiol. Infect. Dis. 2011, 69:266-270. 10.1016/j.diagmicrobio.2010.10.004.
26. Rigó K., Gyuranecz M., Tóth A.G., Földvári G. Detection of Borrelia burgdorferi Sensu Lato and Anaplasma phagocytophilum in small mammals and ectoparasites in Hungary. Vector Borne Zoonotic Dis. 2011, 11:1499-1501. 10.1089/vbz.2011.0608.
27. Rizzoli A., Silaghi C., Obiegala A., Rudolf I., Hubalek Z., Foldvari G., Plantard O., Vayssier-Taussat M., Bonnet S., Spitalska E., Kazimirova M. Ixodes ricinus and its transmitted pathogens in urban and peri-urban areas in Europe: new hazards and relevance for public health. Front. Public Health 2014, 2:251. 10.3389/fpubh.2014.00251.
28. Rózsa L., Reiczigel J., Majoros G. Quantifying parasites in samples of hosts. J. Parasitol. 2000, 86:228-232. 10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO; 2.
29. Schouls L., van de Pol I., Rijpkema S., Schot C. Detection and identification of Ehrlichia Borrelia burgdorferi Sensu Lato, and Bartonella Species in Dutch Ixodes ricinus Ticks. J. Clin. Microbiol. 1999, 37:2215-2222.
30. 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. 10.1186/1756-3305-5-285.
31. Stuen S., Granquist E.G., Silaghi C. Anaplasma phagocytophilum - a widespread multi-host pathogen with highly adaptive strategies. Front. Cell. Infect. Microbiol. 2013, 3:31. 10.3389/fcimb.2013.00031.
32. The R Development Core Team R□: A Language and Environment for Statistical Computing 2010.
33. Tijsse-Klasen E., Koopmans M.P.G., Sprong H. Tick-borne pathogen - reversed and conventional discovery of disease. Front. Public Health 2014, 2. 10.3389/fpubh.2014.00073.
34. Tomanović S., Chochlakis D., Radulović Z., Milutinović M., Cakić S., Mihaljica D., Tselentis Y., Psaroulaki A. Analysis of pathogen co-occurrence in host-seeking adult hard ticks from Serbia. Exp. Appl. Acarol. 2013, 59:367-376. 10.1007/s10493-012-9597-y.
35. Víchová B., Majláthová V., Nováková M., Stanko M., Hviščová I., Pangrácová L., Chrudimský T., Čurlík J., Petko B. Anaplasma infections in ticks and reservoir host from Slovakia. Infect. Genet. Evol. 2014, 22:265-272. 10.1016/j.meegid.2013.06.003.
36. Víchová B., Majlathova V., Novakova M., Straka M., Petko B. First molecular detection of Anaplasma phagocytophilum in European Brown Bear (Ursus arctos). Vector-borne Zoonotic Dis. 2010, 10:543-545.
37. Wirtgen M., Nahayo a., Linden a., Losson B., Garigliany M., Desmecht D. Detection of Anaplasma phagocytophilum in Dermacentor reticulatus ticks. Vet. Rec. 2011, 168:195. 10.1136/vr.d1053.
38. Yabsley M.J., Murphy S.M., Luttrell M.P., Wilcox B.R., Howerth E.W., Munderloh U.G. Characterization of "Candidatus Neoehrlichia lotoris" (family Anaplasmataceae) from raccoons (Procyon lotor). Int. J. Syst. Evol. Microbiol. 2008, 58:2794-2798. 10.1099/ijs.0.65836-0.