Prevalence and genetic variability of Anaplasma phagocytophilum in wild rodents from the Italian alps

. 2017 Jun 14 ; 10 (1) : 293. [epub] 20170614

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid28615038
Odkazy

PubMed 28615038
PubMed Central PMC5471728
DOI 10.1186/s13071-017-2221-6
PII: 10.1186/s13071-017-2221-6
Knihovny.cz E-zdroje

BACKGROUND: Human granulocytic anaplasmosis is a zoonotic bacterial disease with increasing relevance for public health in Europe. The understanding of its sylvatic cycle and identification of competent reservoir hosts are essential for improving disease risk models and planning preventative measures. RESULTS: In 2012 we collected single ear biopsy punches from 964 live-trapped rodents in the Province of Trento, Italy. Genetic screening for Anaplasma phagocytophilum (AP) was carried out by PCR amplification of a fragment of the 16S rRNA gene. Fifty-two (5.4%) samples tested positive: 49/245 (20%) from the bank vole (Myodes glareolus) and 3/685 (0.4%) samples collected from the yellow-necked mouse (Apodemus flavicollis). From these 52 positive samples, we generated 38 groEL and 39 msp4 sequences. Phylogenetic analysis confirmed the existence of a distinct rodent strain of AP. CONCLUSIONS: Our results confirm the circulation of a specific strain of AP in rodents in our study area; moreover, they provide further evidence of the marginal role of A. flavicollis compared to M. glareolus as a reservoir host for this pathogen.

Zobrazit více v PubMed

Jahfari S, Coipan EC, Fonville M, van Leeuwen AD, Hengeveld P, Heylen D, et al. Circulation of four Anaplasma phagocytophilum ecotypes in Europe. Parasit Vectors. 2014;7:365. doi: 10.1186/1756-3305-7-365. PubMed DOI PMC

Rizzoli A, Silaghi C, Obiegala A, Rudolf I, Hubálek Z, Földvári 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 Health. 2014;2:251. doi: 10.3389/fpubh.2014.00251. PubMed DOI PMC

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;74:7118–7125. doi: 10.1128/AEM.00625-08. PubMed DOI PMC

Stuen S, Granquist EG, Silaghi C. Anaplasma phagocytophilum - a widespread multi host pathogen with highly adaptive strategies. Front Cell Infect Microbiol. 2013;3:31. PubMed PMC

Dumler JS, Choi KS, Garcia-Garcia JC, Barat NS, Scorpio DG, Garyu JW, et al. Human granulocytic anaplasmosis and Anaplasma phagocytophilum. Emerg Infect Dis. 2005;11:1828–1834. doi: 10.3201/eid1112.050898. PubMed DOI PMC

Dugat T, Lagrée AC, Maillard R, Boulouis HJ, Haddad N. Opening the black box of Anaplasma phagocytophilum diversity: current situation and future perspective. Front Cell Infect Microbiol. 2015;5:61. doi: 10.3389/fcimb.2015.00061. PubMed DOI PMC

Ismail N, Bloch KC, Mc Bride JW. Human ehrlichiosis and anaplasmosis. Clin lab med. 2010;30:261–292. doi: 10.1016/j.cll.2009.10.004. PubMed DOI PMC

Piccolin G, Benedetti G, Doglioni C, Lorenzato C, Mancuso S, Papa N, et al. A study of the presence of Borrelia burgdorferi, Anaplasma (previously Ehrlichia) phagocytophilum, Rickettsia and Babesia in Ixodes ricinus collected within the territory of Belluno. Italy Vector Borne Zoonotic Dis. 2006;6:24–31. doi: 10.1089/vbz.2006.6.24. PubMed DOI

Cinco M, Padovan D, Murgia R, Maroli M, Frusteri L, Heldtander M, et al. Coexistence of Ehrlichia phagocytophila and Borrelia burgdorferi sensu lato in Ixodes ricinus ticks from Italy as determined by 16S rRNA gene sequencing. J Clin Microbiol. 1997;35:3365–3366. PubMed PMC

Kauffmann M, Rehbein S, Hamel D, Lutz W, Heddergott M, Pfister K, et al. Anaplasma phagocytophilum and Babesia spp. in roe deer (Capreolus capreolus), fallow deer (Dama dama) and mouflon (Ovis musimon) in Germany. Mol Cell Probes. 2017;31:46-54. PubMed

Carrade DD, Foley JE, Borjesson DL, Sykes JE. Canine granulocytic anaplasmosis: a review. J Vet Intern Med. 2009;23:1129–41. PubMed

Stuen S. Anaplasma phagocytophilum (Formerly Ehrlichia phagocitophila) infection in sheep and wild ruminants in Norway. A study on clinical manifestation, distribution and persistence. PhD thesis, Norwegian School of Veterinarian Science, Oslo. 2003.

Bjöersdorff A, Bergstrom S, Massung RF, Haemig PD, Olsen B. Erlichia-infected ticks on migrating birds. Emerg Infect Dis. 2001;7:877–879. doi: 10.3201/eid0705.017517. PubMed DOI PMC

Sparagano O, George D, Giangaspero A, Špitalská E. Arthropods and associated arthropod-borne diseases transmitted by migrating birds. The case of ticks and tick borne pathogens. Vet Parasitol. 2015;213:61–6. PubMed

Kiffner C, Vor T, Hagedorn P, Niedrig M, Ruhe F. Factors affecting patterns of tick parasitism on forest rodents in tick borne encephalitis risk areas, Germany. Parasitol Res. 2011;108:323–35. PubMed PMC

Bown KJ, Lambin X, Ogden NH, Begon M, Telford G, Woldehiwet Z, et al. Delineating Anaplasma phagocytophilum ecotypes in coexisting, discrete enzootic cycles. Emerg Infect Dis. 2009;15:1948–1954. doi: 10.3201/eid1512.090178. PubMed DOI PMC

Blaňarová L, Stanko M, Carpi G, Miklisová D, Víchová B, Mošanský L, et al. Distinct Anaplasma phagocytophilum genotypes associated with Ixodes trianguliceps ticks and rodents in Central Europe. Ticks Tick Borne Dis. 2014;5:928–938. doi: 10.1016/j.ttbdis.2014.07.012. PubMed DOI

Baráková I, Derdáková M, Carpi G, Rosso F, Collini M, Tagliapietra V, et al. Genetic and ecologic variability among Anaplasma phagocytophilum strains, northern Italy. Emerg Infect Dis. 2014;6:1082–1085. doi: 10.3201/eid2006.131023. PubMed DOI PMC

Dumler JS. The biological basis of sever outcomes in Anaplasma phagocytophilum infection. FEMS Immunol med Microbiol. 2012;64:13–20. doi: 10.1111/j.1574-695X.2011.00909.x. PubMed DOI PMC

Adams DA, Jajosky RA, Ajani U, Kriseman J, Sharp P, Onweh DH, et al. Summary of notifiable diseases - United States, 2012. MMWR Morb Mortal Wkly Rep. 2014;61:1–121. PubMed

Zhang L, Liu H, Xu B, Zhang Z, Jin Y, Li W, et al. Rural residents in China are at increased risk of exposure to tick-borne pathogens Anaplasma phagocytophilum and Ehrlichia chaffeensis. Biomed Res Int. 2014;2014:313867. PubMed PMC

Courtney JW, Dryden LR, Montgomery J, Schneider BS, Smith G, Massung RF. Molecular characterization of Anaplasma phagocytophilum and Borrelia burgdorferi in Ixodes scapularis ticks from Pennsylvania. J Clin Microbiol. 2003;41:1569–1573. doi: 10.1128/JCM.41.4.1569-1573.2003. PubMed DOI PMC

Reichard MV, Roman RM, Kocan KM, Blouin EF, de la Fuente J, Snider TA, et al. Inoculation of white-tailed deer (Odocoileus virginianus) with Ap-V1 or NY-18 strains of Anaplasma phagocytophilum and microscopic demonstration of Ap-V1 in Ixodes scapularis adults that acquired infection from deer as nymphs. Vector Borne Zoonotic Dis. 2009;9:565–568. doi: 10.1089/vbz.2008.0106. PubMed DOI

Massung RF, Priestley RA, Miller NJ, Mather TN, Ml L. Inability of a variant strain of Anaplasma phagocytophilum to infect mice. J Infect Dis. 2003;188:1757–1763. doi: 10.1086/379725. PubMed DOI

Liz JS, Anderes L, Sumner JW, Massung RF, Gern L, Rutti B, et al. PCR detection of granulocytic ehrlichiae in Ixodes ricinus ticks and wild small mammals in western Switzerland. J Clin Microbiol. 2000;38:1002–1007. PubMed PMC

Bown KJ, Begon M, Bennett M, Woldehiwet Z, Ogden NH. Seasonal dynamics of Anaplasma phagocytophila in a rodent-tick (Ixodes trianguliceps) system, United Kingdom. Emerg Infect Dis. 2003;9:63–70. doi: 10.3201/eid0901.020169. PubMed DOI PMC

Chastagner A, Moinet M, Perez G, Roy E, McCoy KD, Plantard O, et al. Prevalence of Anaplasma phagocytophilum in small rodents in France. Ticks TickBorne Dis. 2016;7:988–991. doi: 10.1016/j.ttbdis.2016.05.005. PubMed DOI

Kallio ER, Begon M, Birtles RJ, Bown KJ, Koskela E, Mappes T, et al. First report of Anaplasma phagocytophilum and Babesia microti in rodents in Finland. Vector Borne Zoonotic Dis. 2014;14:389–393. doi: 10.1089/vbz.2013.1383. PubMed DOI PMC

Torre I, Arrizabalaga A. Habitat preference of the bank vole Myodes glareolus in a Mediterranean mountain range. Acta Theriol. 2008;53:241–250. doi: 10.1007/BF03193120. DOI

Michielin V. Il sistema acqua suolo. In: Rapporto sullo stato dell’ambiente 2003. Provincia Autonoma di Trento, Trento 2003; 112.

Obiegala A, Pfeffer M, Pfister K, Tiedemann T, Thiel C, Balling A, et al. Candidatus Neoehrlichia mikurensis and Anaplasma phagocytophilum: prevalences and investigations on a new transmission path in small mammals and ixodid ticks. Parasit Vectors. 2014;7:563. PubMed PMC

Svitálková Z, Haruštiaková D, Mahríková L, Berthová L, Slovák M, Kocianová E, et al. Anaplasma phagocytophilum prevalence in ticks and rodents in an urban and natural habitat in south-western Slovakia. Parasit Vectors. 2015;8:276. doi: 10.1186/s13071-015-0880-8. PubMed DOI PMC

Sinsky RJ, Piesman J. Ear punch biopsy method for detection and isolation of Borrelia burgdorferi from rodents. J Clin Microbiol. 1989;27(8):1723–1727. PubMed PMC

Massung RF, Priestley RA, Levin ML. Transmission route efficacy and kinetics of Anaplasma phagocytophilum infection in the white-footed mouse, Peromyscus leucopus. Vector Borne Zoonotic Dis. 2004;4:310–318. doi: 10.1089/vbz.2004.4.310. PubMed DOI

Randolph SE, Miklisoá D, Lysy J, Rogers DJ, Labuda M. Incidence from coincidence: patterns of tick infestations on rodents facilitate transmission of tick-borne encephalitis virus. Parasitology. 1999;118:177–186. doi: 10.1017/S0031182098003643. PubMed DOI

Humair PF, 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. doi: 10.1017/S0031182098003564. PubMed DOI

Michalik J, Hofman T, Buczek A, Skoracki M, Sikora B. Borrelia burgdorferi s.l.in Ixodes ricinus (Acari: Ixodidae) ticks collected from vegetation and small rodents in recreational areas of the city of Poznań. J Med Entomol. 2003;40:690–7. PubMed

Paulauskas A, Radzijevskaja J, Rosef O, Turcinaviciene J, Ambrasiene D. Infestation of mice and voles with Ixodes ricinus ticks in Lithuania and Norway. Est J Ecol. 2009;58:112–125. doi: 10.3176/eco.2009.2.05. DOI

Gray J, Kirstein F, Robertson J. Borrelia burgdorferi sensu lato in Ixodes ricinus ticks and rodents in a recreational park in south-western Ireland. Exp Appl Acarol. 1999;23:717–729. doi: 10.1023/A:1006233700194. PubMed DOI

Hanincova K, Schafer S, Etti S, Sewell H, Taragelova V, Ziak D, et al. Association of Borrelia afzelii with rodents in Europe. Parasitology. 2003;126:11–20. doi: 10.1017/S0031182002002548. PubMed DOI

Siński E, Pawelczyk A, Baker A, Behnke J. Abundance of wild rodents, ticks and environmental risk of Lyme borreliosis: a longitudinal study in an area of Mazury Lakes district of Poland. Ann Agric Environ Med. 2006;13:295–300. PubMed

Estrada-Peña A, Osácar JJ, Pichon B, Gray JS. Host and pathogen detection for immature stages of Ixodes ricinus (Acari:Ixodidae) in north-Central Spain. Exp Appl Acarol. 2005;37:257. doi: 10.1007/s10493-005-3271-6. PubMed DOI

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. doi: 10.1016/j.ttbdis.2013.11.007. PubMed DOI

Krücken J, Schreiber C, Maaz D, Kohn M, Demeler J, Beck S, et al. A novel high-resolution melt PCR assay discriminates Anaplasma phagocytophilum and “Candidatus Neoehrlichia mikurensis”. J Clin Microbiol. 2013;51:1958–1961. doi: 10.1128/JCM.00284-13. PubMed DOI PMC

Randolph SE. Patterns of distribution of the tick Ixodes trianguliceps Birula on its hosts. J Anim Ecol. 1975;44:451–474. doi: 10.2307/3606. DOI

Mysterud A, Byrkjeland R, Qviller L, Viljugrein H. The generalist tick Ixodes ricinus and the specialist tick Ixodes trianguliceps on shrews and rodents in a northern forest ecosystem - a role of body size even among small hosts. Parasit Vectors. 2015;16:639. PubMed PMC

Turner AK, Beldomenico PM, Bown K, Burthe SJ, Jackson JA, Lambin X, et al. Host-parasite biology in the real world: the field voles of Kielder. Parasitology. 2014;141:997–1017. doi: 10.1017/S0031182014000171. PubMed DOI PMC

Michaux JR, Kinet S, Filippucci MG, Libois R, Besnard A, Catzfelis F. Molecular identification of three sympatric species of wood mice (Apodemus sylvaticus, A. flavicollis, A. alpicola) in western Europe (Muridae, Rodentia) Mol Ecol Notes. 2001;1:260–263. doi: 10.1046/j.1471-8278.2001.00100.x. DOI

Massung RF, Levin ML, Munderloh UG, Silverman DJ, Lynch MJ, Gaywee JK. Isolation and propagation of the Ap-variant 1 strain of Anaplasma phagocytophilum in a tick cell line. Jour Clin Microbiol. 2007;45:2138–2143. doi: 10.1128/JCM.00478-07. PubMed DOI PMC

De la Fuente J, Massung RF, Wong SJ, Chu FK, Lutz H, Meli M, et al. Sequence analysis of the msp4 gene of Anaplasma phagocytophilum strains. J Clin Microbiol. 2005;43:1309–1317. doi: 10.1128/JCM.43.3.1309-1317.2005. PubMed DOI PMC

Carpi G, Bertolotti L, Pecchioli E, Cagnacci F, Rizzoli A. Anaplasma phagocytophilum groEL gene heterogeneity in Ixodes ricinus larvae feeding on roe deer in northeastern Italy. Vector Borne Zoonotic Dis. 2009;9:179–184. doi: 10.1089/vbz.2008.0068. PubMed DOI

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. doi: 10.1093/molbev/mst197. PubMed DOI PMC

Harris JW, Stocker H. Handbook of mathematics and computational Science. New York: Springer-Verlag; 1998. Maximum Likelihood Method; p. 824.

Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993;10:512–526. PubMed

Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985;39:783–791. doi: 10.1111/j.1558-5646.1985.tb00420.x. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace