Are Apodemus spp. mice and Myodes glareolus reservoirs for Borrelia miyamotoi, Candidatus Neoehrlichia mikurensis, Rickettsia helvetica, R. monacensis and Anaplasma phagocytophilum?

Ticks and Tick-borne Diseases

Volumn 5, Issue 3, 2014, Pages 245-251

  Burri, C ^a   Schumann, O ^a   Schumann, C ^a   Gern, L ^a  

^a Institut de Biologie   (Switzerland)

Author keywords

Anaplasma phagocytophilum; Borrelia miyamotoi; Candidatus Neoehrlichia mikurensis; Rickettsia helvetica; Rickettsia monacensis; Rodents; Xenodiagnosis

Indexed keywords

ANAPLASMA PHAGOCYTOPHILUM; ANAPLASMATACEAE; ANAPLASMATACEAE INFECTION; APODEMUS FLAVICOLLIS; APODEMUS SYLVATICUS; ARTICLE; BACTERIAL GENE; BACTERIAL TRANSMISSION; BACTERIUM DETECTION; BORRELIA; BORRELIA AFZELII; BORRELIA INFECTION; BORRELIA MIYAMOTOI; DISEASE CARRIER; GENE SEQUENCE; HUMAN GRANULOCYTIC ANAPLASMOSIS; INFECTION RATE; IXODES RICINUS; LARVA; MIXED INFECTION; MOLTING; MYODES GLAREOLUS; NEOEHRLICHIA MIKURENSIS; NEOEHRLICHIA MIKURENSIS INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; P66 GENE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REPRODUCTIVE SUCCESS; RICKETTSIA HELVETICA; RICKETTSIA MONACENSIS; RICKETTSIACEAE INFECTION; SWITZERLAND; TICK INFESTATION; XENODIAGNOSIS; ANAPLASMATACEAE INFECTIONS; ANIMAL; ARVICOLINAE; BORRELIA INFECTIONS; CHEMISTRY; DNA SEQUENCE; EHRLICHIOSIS; FEMALE; GENETICS; ISOLATION AND PURIFICATION; IXODES; MICROBIOLOGY; MOLECULAR GENETICS; MURINAE; PARASITE VECTOR; RICKETTSIA; RICKETTSIA INFECTIONS; VETERINARY;

ANAPLASMA PHAGOCYTOPHILUM; APODEMUS; BORRELIA; BORRELIA AFZELII; BORRELIA BURGDORFERI GROUP; BORRELIA MIYAMOTOI; CANDIDATUS NEOEHRLICHIA MIKURENSIS; IXODES RICINUS; IXODIDA; MAMMALIA; MUS; RICKETTSIA; RICKETTSIA HELVETICA; RICKETTSIA MONACENSIS; RODENTIA; SPIROCHAETES; TICK-BORNE ENCEPHALITIS VIRUS;

BACTERIAL DNA;

ANAPLASMA PHAGOCYTOPHILUM; ANAPLASMATACEAE; ANAPLASMATACEAE INFECTIONS; ANIMALS; ARACHNID VECTORS; ARVICOLINAE; BASE SEQUENCE; BORRELIA; BORRELIA INFECTIONS; COINFECTION; DISEASE RESERVOIRS; DNA, BACTERIAL; EHRLICHIOSIS; FEMALE; IXODES; MOLECULAR SEQUENCE DATA; MURINAE; RICKETTSIA; RICKETTSIA INFECTIONS; SEQUENCE ANALYSIS, DNA; SWITZERLAND;

EID: 84897419725     PISSN: 1877959X     EISSN: 18779603     Source Type: Journal    
DOI: 10.1016/j.ttbdis.2013.11.007     Document Type: Article

References (71)

1. Alekseev A.N., Dubinina H.V., Van de Pol I., Schouls L.M. Identification of Ehrlichia spp. and Borrelia burgdorferi in Ixodes ticks in the Baltic regions of Russia. J. Clin. Microbiol. 2001, 39:2237-2242.
2. Andersson M., Raberg L. Wild rodents and novel human pathogen Candidatus Neoehrlichia mikurensis, southern Sweden. Emerg. Infect. Dis. 2011, 17:1716-1718.
3. Beati L., Péter O., Burgdorfer W., Aeschlimann A., Raoult D. Confirmation that Rickettsia helvetica sp. nov. is a distinct species of the spotted fever group of Rickettsiae. Int. J. Syst. Bacteriol. 1993, 43:521-526.
4. Bekker C.P., de Vos S., Taoufik A., Sparagano O.A., Jongejan F. Simultaneous detection of Anaplasma and Ehrlichia species in ruminants and detection of Ehrlichia ruminantium in Amblyomma variegatum ticks by reverse line blot hybridization. Vet. Microbiol. 2002, 89:223-238.
5. Bellet-Edimo R., Betschart B., Gern L. Frequency and efficiency of transovarial and subsequent transstadial transmissions of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks. Bull. Soc. Neuch. Sci. Nat. 2005, 128:117-125.
6. Beninati T., Piccolo G., Rizzoli A., Genchi C., Bandi C. Anaplasmataceae in wild rodents and roe deer from Trento Province (northern Italy). Eur. J. Clin. Microbiol. Infect. Dis. 2006, 25:677-678.
7. Bown K.J., Begon M., Bennett M., Woldehiwet Z., Ogden N.H. Seasonal dynamics of Anaplasma phagocytophila in a rodent-tick (Ixodes trianguliceps) system, United Kingdom. Emerg. Infect. Dis. 2003, 9:63-70.
8. Bown K.J., Lambin X., Ogden N.H., Petrovec M., Shaw S.E., Woldehiwet Z., Birtles R.J. High resolution genetic fingerprinting of European strains of Anaplasma phagocytophilum by use of multilocus variable-number tandem-repeat analysis. J. Clin. Microbiol. 2007, 45:1771-1776.
9. Bown K.J., Lambin X., Ogden N.H., Begon M., Telford G., Woldehiwet Z., Birtles R.J. Delineating Anaplasma phagocytophilum ecotypes in coexisting, discrete enzootic cycles. Emerg. Infect. Dis. 2009, 15:1948-1954.
10. Bunikis J., Barbour A.G. Third Borrelia species in white-footed mice. Emerg. Infect. Dis. 2005, 11:1150-1151.
11. Burgdorfer W., Aeschlimann A., Péter O., Hayes S.F., Philip R.N. Ixodes ricinus: vector of a hitherto undescribed spotted fever group agent in Switzerland. Acta Trop. 1979, 36:357-367.
12. Burri C., Morán Cadenas F., Douet V., Moret J., Gern L. Ixodes ricinus density and infection prevalence of Borrelia burgdorferi sensu lato along a North-facing altitudinal gradient in the Rhone Valley (Switzerland). Vector Borne Zoonotic Dis. 2007, 7:50-58.
13. Burri C., Dupasquier C., Bastic V., Gern L. Pathogens of emerging tick-borne diseases, Anaplasma phagocytophilum, Rickettsia spp., and Babesia spp., in Ixodes ticks collected from rodents at four sites in Switzerland (Canton of Bern). Vector Borne Zoonotic Dis. 2011, 11:939-944.
14. Cotty A. Clé de détermination des Ixodidae et Amblyommidae de Suisse. 1985, University Neuchâtel, Switzerland, Ph.D. thesis.
15. Courtney J.W., Kostelnik L.M., Zeidner N.S., Massung R.F. Multiplex real-time PCR for detection of Anaplasma phagocytophilum and Borrelia burgdorferi. J. Clin. Microbiol. 2004, 42:3164-3168.
16. De Sousa R., Lopes de Carvalho I., Santos A.S., Bernardes C., Milhano N., Jesus J., Menezes D., Nuncio M.S. Role of the lizard Teira dugesii as a potential host for Ixodes ricinus tick-borne pathogens. Appl. Environ. Microbiol. 2012, 78:3767-3769.
17. Diniz P.P., Schulz B.S., Hartmann K., Breitschwerdt E.B. Candidatus Neoehrlichia mikurensis infection in a dog from Germany. J. Clin. Microbiol. 2011, 49:2059-2062.
18. Fehr J.S., Bloemberg G.V., Ritter C., Hombach M., Lüscher T.F., Weber R., Keller P.M. Septicemia caused by tick-borne bacterial pathogen Candidatus Neoehrlichia mikurensis. Emerg. Infect. Dis. 2010, 16:1127-1129.
19. Fomenko N.V., Livanova N.N., Borgoiakov V., Kozlova I.V., Shulaikina I.V., Pukhovskaia N.M., Tokarevich K.N., Livanov S.G., Doroshchenko E.K., Ivanov L.I. Detection of Borrelia miyamotoi in ticks Ixodes persulcatus from Russia. Parazitologiia 2010, 44:201-211.
20. Fraenkel C.J., Garpmo U., Berglund J. Determination of novel Borrelia genospecies in Swedish Ixodes ricinus ticks. J. Clin. Microbiol. 2002, 40:3308-3312.
21. 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, 45:804-810.
22. 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.
23. Gern L., Humair F. Ecology of Borrelia burgdorferi sensu lato in Europe. Lyme Borreliosis: Biology, Epidemiology and Control 2002, 149-174. CAB International, Oxon, United Kingdom. J. Gray, O. Kahl, R.S. Lane, G. Stanek (Eds.).
24. Gern L., Douet V., López Z., Rais O., Morán Cadenas F. Diversity of Borrelia genospecies in Ixodes ricinus ticks in a Lyme borreliosis endemic area in Switzerland identified by using new probes for reverse line blotting. Ticks Tick-borne Dis. 2010, 1:23-29.
25. Graf G.F. Copulation, nutrition et ponte chez Ixodes ricinus L. (Ixodoidea: Ixodidae), 1ère partie. Bull. Soc. Entomol. Suisse 1978, 51:89-97.
26. 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, 368:240-245.
27. Hamer S.A., Tsao J.I., Walker E.D., Hickling G.J. Invasion of the Lyme disease vector Ixodes scapularis: implications for Borrelia burgdorferi endemicity. EcoHealth 2010, 7:47-63.
28. 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. Parasite Vector 2012, 5:231.
29. Humair P.F., Rais O., Gern L. Transmission of Borrelia afzelii from Apodemus mice and Clethrionomys voles to Ixodes ricinus ticks: differential transmission pattern and overwintering maintenance. Parasitology 1999, 118:33-42.
30. Jado I., Escudero R., Gil H., Jimenez-Alonso M.I., Sousa R., Garcia-Perez A.L., Rodriguez-Vargas M., Lobo B., Anda P. Molecular method for identification of Rickettsia species in clinical and environmental samples. J. Clin. Microbiol. 2006, 44:4572-4576.
31. 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. Parasite Vector 2012, 5:74.
32. Kahl O., Gern L., Eisen L., Lane R.S. Ecological research on Borrelia burgdorferi sensu lato: terminology and some methodological pitfalls. Lyme Borreliosis: Biology, Epidemiology and Control 2002, 29-46. CAB International, Oxon, United Kingdom. J. Gray, O. Kahl, R.S. Lane, G. Stanek (Eds.).
33. Karan' L.S., Koliasnikova N.M., Toporkova M.G., Makhneva M.A., Nadezhdina M.V., Esaulkova A.Iu., Romanenko V.V., Arumova E.A., Platonov A.E., Maleev V.V. Usage of real-time polymerase chain reaction for diagnostics of different tick-borne infections. Zh. Mikrobiol. Epidemiol. Immunobiol. 2010, 3:72-77. (in Russian).
34. 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. Sys. Evol. Microbiol. 2004, 54:1837-1843.
35. Li H., Jiang J.F., Liu W., Zheng Y.C., Huo Q.B., Tang K., Zuo S.Y., Liu K., Jiang B.G., Yang H., Cao W.C. Human infection with Candidatus Neoehrlichia mikurensis, China. Emerg. Infect. Dis. 2012, 18:1636-1639.
36. Lommano E., Bertaiola L., Dupasquier C., Gern L. Infections and co-infections of questing Ixodes ricinus ticks by emerging zoonotic pathogens in Western Switzerland. Appl. Environ. Microbiol. 2012, 78:4606-4612.
37. Maurer F.P., Keller P.M., Beuret C., Joha C., Achermann Y., Gubler J., Bircher D., Karrer U., Fehr J., Zimmerli L., Bloemberg G.V. Close geographic association of human neoehrlichiosis and tick populations carrying Candidatus Neoehrlichia mikurensis in eastern Switzerland. J. Clin. Microbiol. 2013, 51:169-176.
38. Movila A., Toderas I., Uspenskaia I., Conovalov J. Molecular detection of tick-borne pathogens in Ixodes ricinus from Moldova collected in 1960. Ticks Tick Borne Dis. 2013, 4:359-361.
39. 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, 43:120-123.
40. Naitou H., Kawaguchi D., Nishimura Y., Inayoshi M., Kawamori F., Masuzawa T., Hiroi M., Kurashige H., Kawabata H., Fujita H., Ohashi N. Molecular identification of Ehrlichia species and Candidatus Neoehrlichia mikurensis from ticks and wild rodents in Shizuoka and Nagano Prefectures, Japan. Microbiol. Immunol. 2006, 50:45-51.
41. Nilsson K., Lindquist O., Pahlson C. Association of Rickettsia helvetica with chronic perimyocarditis in sudden cardiac death. Lancet 1999, 354:1169-1173.
42. Nilsson K., Lindquist O., Pahlson C. Rickettsia helvetica in patient with meningitis, Sweden, 2006. Emerg. Infect. Dis. 2010, 16:490-492.
43. Overzier E., Pfister K., Herb I., Mahling M., Bock G., Silaghi C. Detection of tick-borne pathogens in roe deer (Capreolus capreolus), in questing ticks (Ixodes ricinus), and in ticks infesting roe deer in southern Germany. Ticks Tick Borne Dis. 2013, 13:559-564.
44. Pérez D., Kneubühler Y., Rais O., Gern L. Seasonality of Ixodes ricinus ticks on vegetation and on rodents and Borrelia burgdorferi sensu lato genospecies diversity in two Lyme borreliosis-endemic areas in Switzerland. Vector Borne Zoonotic Dis. 2012, 12:633-644.
45. Péter O. Contribution à la connaissance de l'écologie de la Rickettsie suisse transmise par la tique Ixodes ricinus L., 1758 (Ph.D. thesis) 1984, University of Neuchâtel, Switzerland.
46. Piesman J., Gern L. Lyme borreliosis in Europe and North America. Parasitology 2004, 129(Suppl.):S191-S220.
47. 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, 17:1816-1823.
48. Poupon M.A., Lommano E., Humair P.F., Douet V., Rais O., Schaad M., Jenni L., Gern L. Prevalence of Borrelia burgdorferi sensu lato in ticks collected from migratory birds in Switzerland. Appl. Environ. Microbiol. 2006, 72:976-979.
49. R Development Core Team R: A Language and Environment for Statistical Computing 2012, R Foundation for Statistical Computing, Vienna, Austria.
50. Rar V., Golovljova I. Anaplasma, Ehrlichia, and "Candidatus Neoehrlichia mikurensis" bacteria: pathogenicity, biodiversity, and molecular genetic characteristics, a review. Infect. Genet. Evol. 2011, 11:1842-1846.
51. Richter D., Matuschka F.-R. Elimination of Lyme disease spirochetes from ticks feeding on domestic ruminants. Appl. Environ. Microbiol. 2010, 76:7650-7652.
52. Richter D., Schlee D.B., Matuschka F.-R. Relapsing fever-like spirochetes infecting European vector tick of Lyme disease agent. Emerg. Infect. Dis. 2003, 9:697-701.
53. Rijpkema S.G., Molkenboer M.J., Schouls L.M., Jongejan F., Schellekens J.F. Simultaneous detection and genotyping of three genomic groups of Borrelia burgdorferi sensu lato in Dutch Ixodes ricinus ticks by characterization of the amplified intergenic spacer region between 5S and 23S rRNA genes. J. Clin. Microbiol. 1995, 33:3091-3095.
54. Rollend L., Fish D., Childs J.E. Transovarial transmission of Borrelia spirochetes by Ixodes scapularis: a summary of the literature and recent observations. Ticks Tick Borne Dis. 2013, 4:46-51.
55. 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.
56. Sanogo Y.O., Parola P., Shpynov S., Camicas J.L., Brouqui P., Caruso G., Raoult D. Genetic diversity of bacterial agents detected in ticks removed from asymptomatic patients in northeastern Italy. Ann. N. Y. Acad. Sci. 2003, 990:182-190.
57. Schex S., Dobler G., Riehm J., Müller J., Essbauer S. Rickettsia spp. in wild small mammals in Lower Bavaria, South-Eastern Germany. Vector Borne Zoonotic Dis. 2011, 11:493-502.
58. Schouls L.M., Van De Pol I., Rijpkema S.G., Schot C.S. Detection and identification of Ehrlichia, Borrelia burgdorferi sensu lato, and Bartonella species in Dutch Ixodes ricinus ticks. J. Clin. Microbiol. 1999, 37:2215-2222.
59. Scoles G.A., Papero M., Beati L., Fish D. A relapsing fever group spirochete transmitted by Ixodes scapularis ticks. Vector Borne Zoonotic Dis. 2001, 1:21-34.
60. Scott M.C., Rosen M.E., Hamer S.A., Baker E., Edwards H., Crowder C., Tsao J.I., Hickling G.J. High-prevalence Borrelia miyamotoi infection among wild turkeys (Meleagris gallopavo) in Tennessee. J. Med. Entomol. 2010, 47:1238-1242.
61. 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. Parasite Vector 2012, 5:285.
62. Simser J.A., Palmer A.T., Fingerle V., Wilske B., Kurtti T.J., Munderloh U.G. Rickettsia monacensis sp. nov., a spotted fever group Rickettsia, from ticks (Ixodes ricinus) collected in a European city park. Appl. Environ. Microbiol. 2002, 68:4559-4566.
63. Speck S., Perseke L., Petney T., Skuballa J., Pfäffle M., Taraschewski H., Bunnell T., Essbauer S., Dobler G. Detection of Rickettsia helvetica in ticks collected from European hedgehogs (Erinaceus europaeus, Linnaeus, 1758). Ticks Tick Borne Dis. 2013, 4:222-226.
64. Sprong H., Wielinga P.R., Fonville M., Reusken C., Brandenburg A.H., Borgsteede F., Gaasenbeek C., van der Giessen J.W. Ixodes ricinus ticks are reservoir hosts for Rickettsia helvetica and potentially carry flea-borne Rickettsia species. Parasite Vector 2009, 2:41.
65. Stuen S., Granquist E., Silaghi C. Anaplasma phagocytophilum - a widespread multi-host pathogen with highly adaptive strategies. Front. Cell. Infect. Microbiol. 2013, 3:31.
66. Taylor K.R., Takano A., Konnai S., Shimozuru M., Kawabata H., Tsubota T. Borrelia miyamotoi infections among wild rodents show age and month independence and correlation with Ixodes persulcatus larval attachment in Hokkaido, Japan. Vector Borne Zoonotic Dis. 2013, 13:92-97.
67. Vayssier-Taussat M., Le Rhun D., Buffet J.P., Maaoui N., Galan M., Guivier E., Charbonnel N., Cosson J.F. Candidatus Neoehrlichia mikurensis in bank voles, France. Emerg. Infect. Dis. 2012, 18:2063-2065.
68. von Loewenich F.D., Geissdörfer W., Disqué C., Matten J., Schett G., Sakka S.G., Bogdan C. Detection of Candidatus Neoehrlichia mikurensis in two patients with severe febrile illnesses: evidence for a European sequence variant. J. Clin. Microbiol. 2010, 48:2630-2635.
69. Welinder-Olsson C., Kjellin E., Vaht K., Jacobsson S., Wennerås C. First case of human Candidatus Neoehrlichia mikurensis infection in a febrile patient with chronic lymphocytic leukemia. J. Clin. Microbiol. 2010, 48:1956-1959.
70. Wilhelmsson P., Fryland L., Borjesson 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.
71. Wodecka B. Significance of red deer (Cervus elaphus) in the ecology of Borrelia burgdorferi sensu lato. Wiad. Parazytol. 2007, 53:231-237.