Folia Parasitologica 65:008 (2018) | DOI: 10.14411/fp.2018.008
Molecular screening for bacterial pathogens in ticks (Ixodes ricinus) collected on migratory birds captured in northern Italy
- 1 Pediatric Clinical Research Center Romeo ed Enrica Invernizzi, University of Milano, Italy;
- 2 University of South Bohemia, Faculty of Science, České Budějovice, Czech Republic;
- 3 Department of Bioscience, University of Milano, Italy;
- 4 Department of Agricultural and Environmental Sciences, University of Milano, Italy;
- 5 Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emila Romagna, Pavia, Italy;
- 6 Department of Biology and Biotechnology, University of Pavia, Italy
Migratory birds have an important role in transporting ticks and associated tick-borne pathogens over long distances. In this study, 2,793 migratory birds were captured by nets in a ringing station, located in northern Italy, and checked for the presence of ticks. Two-hundred and fifty-one ticks were identified as nymphs and larvae of Ixodes ricinus (Linnaeus, 1758) and they were PCR-screened for the presence of bacteria belonging to Borrelia burgdorferi sensu lato, Rickettsia spp., Francisella tularensis and Coxiella burnetii. Four species of Borrelia (B. garinii, B. afzelii, B. valaisiana and B. lusitaniae) and three species of Rickettsia (R. monacensis, R. helvetica and Candidatus Rickettsia mendelii) were detected in 74 (30%) and 25 (10%) respectively out of 251 ticks examined. Co-infection with Borrelia spp. and Rickettsia spp. in the same tick sample was encountered in 7 (7%) out of the 99 infected ticks. We report for the first time the presence of Candidatus Rickettsia mendelii in I. ricinus collected on birds in Italy. This study, besides confirming the role of birds in dispersal of I. ricinus, highlights an important route by which tick-borne pathogens might spread across different countries and from natural environments towards urbanised areas.
Keywords: Migratory birds, tick-borne pathogens, Borrelia spp., Candidatus Rickettsia mendelii, molecular characterisation
Received: August 9, 2017; Accepted: May 28, 2018; Published online: June 15, 2018 Show citation
| ACS | AIP | APA | ASA | Harvard | Chicago | Chicago Notes | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
References
- Berri M., Laroucau K., Rodolakis A. 2000: The detection of Coxiella burnetii from ovine genital swabs, milk and fecal samples by the use of a single touchdown polymerase chain reaction. Vet. Microbiol. 72: 285-293.
Go to original source...
Go to PubMed... - Biernat B., Stańczak J., Michalik J., Sikora B., Cieniuch S. 2016: Rickettsia helvetica and R. monacensis infections in immature Ixodes ricinus ticks derived from sylvatic passerine birds in west-central Poland. Parasitol. Res. 115: 3469-3477.
Go to original source...
Go to PubMed... - Chu C.Y., Jiang B.G., Liu W., Zhao Q.M., Wu X.M., Zhang P.H., Zhan L., Yang H., Cao W.C. 2008: Presence of pathogenic Borrelia burgdorferi sensu lato in ticks and rodents in Zhejiang, south-east China. J. Med. Microbiol. 57: 980-985.
Go to original source...
Go to PubMed... - Corrain R., Drigo M., Fenati M., Menandro M.L., Mondin A., Pasotto D., Martini M. 2012: Study on ticks and tick-borne zoonoses in public parks in Italy. Zoonoses Publ. Hlth. 59: 468-476.
Go to original source...
Go to PubMed... - Dantas-Torres F. 2015: Climate change, biodiversity, ticks and tick-borne diseases: the butterfly effect. Int. J. Parasitol. Parasites Wildl. 4: 452-461.
Go to original source...
Go to PubMed... - Dubska L., Literak I., Kocianova E., Taragelova V., Sverakova V., Sychra O., Hromadko M. 2011: Synanthropic birds influence the distribution of Borrelia species: analysis of Ixodes ricinus ticks feeding on passerine birds. Appl. Environ. Microbiol. 77: 1115-1117.
Go to original source...
Go to PubMed... - Ebani V.V., Bertelloni F., Mani P. 2016: Molecular survey on zoonotic tick-borne bacteria and chlamydiae in feral pigeons (Columba livia domestica). Asian Pac. J. Trop. Med. 9: 324-327.
Go to original source...
Go to PubMed... - Elfving K., Olsen B., Bergström S., Waldenström J., Lundkvist A., Sjöstedt A., Mejlon H., Nilsson K. 2010: Dissemination of spotted fever rickettsia agents in Europe by migrating birds. PLoS ONE 5: 8572.
Go to original source... - Forsman M., Sandström G., Sjöstedt A. 1994: Analysis of 16S ribosomal DNA sequences of Francisella strains and utilisation for determination of the phylogeny of the genus and for identification of strains by PCR. Int. J. Syst. Bacteriol. 44: 38-46.
Go to original source...
Go to PubMed... - Galdikaitė E., Banaitytė A., Paulauskas A., Radzijevskaja J., Golovljova I. 2013: Investigation of genetic diversity of Ixodes ricinus based on four microsatellite loci. Biologija 59: 201-212.
Go to original source... - Gryczyńska A., Welc-Falęciak R. 2016: Long-term study of the prevalence of Borrelia burgdorferi s.l. infection in ticks (Ixodes ricinus) feeding on blackbirds (Turdus merula) in NE Poland. Exp. Appl. Acarol. 70: 381-394.
Go to original source...
Go to PubMed... - Hajduskova E., Literak I., Papousek I., Costa F.B., Novakova M., Labruna M.B., Zdrazilova-Dubska L. 2016: 'Candidatus Rickettsia mendelii', a novel basal group rickettsia detected in Ixodes ricinus ticks in the Czech Republic. Ticks Tick Borne Dis. 7: 482-486.
Go to original source...
Go to PubMed... - Hamer S.A., Goldberg T.L., Kitron U.D., Brawn J.D., Anderson T.K., Loss S.R., Walker E.D., Hamer G.L. 2012: Wild birds and urban ecology of ticks and tick-borne pathogens, Chicago, Illinois, USA, 2005-2010. Emerg. Infect. Dis. 18: 1589-1595.
Go to original source...
Go to PubMed... - Hansford K.M., Fonville M., Gillingham E.L., Coipan E.C., Pietzsch M.E., Krawczyk A.I., Vaux A.G., Cull B., Sprong H., Medlock J.M. 2017: Ticks and Borrelia in urban and peri-urban green space habitats in a city in southern England. Ticks Tick Borne Dis. 8: 353-361.
Go to original source...
Go to PubMed... - Heylen D.J., Sprong H., Krawczyk A., Van Houtte N., Genné D., Gomez-Chamorro A., van Oers K., Voordouw M.J. 2017: Inefficient co-feeding transmission of Borrelia afzelii in two common European songbirds. Sci. Rep. 7: 39596.
Go to original source...
Go to PubMed... - Hornok S., Kováts D., Csörgő T., Meli M.L., Gönczi E., Hadnagy Z., Takács N., Farkas R., Hofmann-Lehmann R. 2014: Birds as potential reservoirs of tick-borne pathogens: first evidence of bacteraemia with Rickettsia helvetica. Parasit. Vectors 7: 128.
Go to original source...
Go to PubMed... - Klaus C., Gethmann J., Hoffmann B., Ziegler U., Heller M., Beer M. 2016: Tick infestation in birds and prevalence of pathogens in ticks collected from different places in Germany. Parasitol. Res. 115: 2729-2740.
Go to original source...
Go to PubMed... - Kowalec M., Szewczyk T., Welc-Falęciak R., Siński E., Karbowiak G., Bajer A. 2017: Ticks and the city - are there any differences between city parks and natural forests in terms of tick abundance and prevalence of spirochaetes? Parasit. Vectors 10: 573.
Go to original source...
Go to PubMed... - Labruna M.B., McBride J.W., Bouyer D.H., Camargo L.M., Camargo E.P., Walker D.H. 2004: Molecular evidence for spotted fever group Rickettsia species in the tick Amblyomma longirostre in Brazil. J. Med. Entomol. 41: 533-537.
Go to original source...
Go to PubMed... - Lado P., Nava S., Labruna M.B., Szabo M.P.J., Durden L.A., Bermudez S., Montagna M., Sánchez Quirós A.C., Beati L. 2016. Amblyomma parvum Aragão, 1908 (Acari: Ixodidae): Phylogeography and systematic considerations. Ticks Tick Borne Dis. 7: 817-827.
Go to original source...
Go to PubMed... - Lindeborg M., Barboutis C., Ehrenborg C., Fransson T., Jaenson T.G., Lindgren P.E., Lundkvist A., Nyström F., Salaneck E., Waldenström J., Olsen B. 2012: Migratory birds, ticks, and Crimean-Congo hemorrhagic fever virus. Emerg. Infect. Dis. 18: 2095-2097.
Go to original source...
Go to PubMed... - Manilla G. 1998: Acari Ixodida. Fauna d'Italia, Vol. 36. Calderini, Bologna, 280 pp.
- Marconi R.T., Garon C.F. 1992: Development of polymerase chain reaction primer sets for diagnosis of Lyme disease and for species-specific identification of Lyme disease isolates by 16S rRNA signature nucleotide analysis. J. Clin. Microbiol. 30: 2830-2834.
Go to original source...
Go to PubMed... - Margos G., Vollmer S.A., Cornet M., Garnier M., Fingerle V., Wilske B., Bormane A., Vitorino L., Collares-Pereira M., Drancourt M., Kurtenbach K. 2009: A new Borrelia species defined by multilocus sequence analysis of housekeeping genes. Appl. Environ. Microbiol. 75: 5410-5416.
Go to original source...
Go to PubMed... - Mehlhorn H., Mehlhorn T., Müller M., Vogt M., Rissland J. 2015. Tick survey for prevalent pathogens in peri-urban recreation sites in Saarland and Rhineland-Palatinate (Germany). Parasitol. Res. 115: 1167-1172.
Go to original source... - Michalik J., Wodecka B., Skoracki M., Sikora B., Stańczak J. 2008: Prevalence of avian-associated Borrelia burgdorferi s.l. genospecies in Ixodes ricinus ticks collected from blackbirds (Turdus merula) and song thrushes (T. philomelos). Int. J. Med. Microbiol. 298: 129-138.
Go to original source... - Nilsson K., Lindquist O., Påhlson C. 1999: Association of Rickettsia helvetica with chronic perimyocarditis in sudden cardiac death. Lancet. 354: 1169-1173.
Go to original source...
Go to PubMed... - Nilsson K., Wallménius K., Hartwig S., Norlander T., Påhlson C. 2014: Bell's palsy and sudden deafness associated with Rickettsia spp. infection in Sweden. A retrospective and prospective serological survey including PCR findings. Eur. J. Neurol. 21: 206-214
Go to original source...
Go to PubMed... - Olivieri E., Gazzonis A.L., Zanzani S.A., Veronesi F., Manfredi M.T. 2017: Seasonal dynamics of adult Dermacentor reticulatus in a peri-urban park in southern Europe. Ticks Tick Borne Dis. 8: 772-779.
Go to original source...
Go to PubMed... - Paduraru O.A., Buffet J.P., Cote M., Bonnet S., Moutailler S., Paduraru V., Femenia F., Eloit M., Savuta G., Vayssier-Taussat M. 2012: Zoonotic transmission of pathogens by Ixodes ricinus ticks, Romania. Emerg. Infect. Dis. 18: 2089-2090.
Go to original source...
Go to PubMed... - Parola P., Paddock C.D., Socolovschi C., Labruna M.B., Mediannikov O., Kernif T., Abdad M.Y., Stenos J., Bitam I., Fournier P.E., Raoult D. 2013: Update on tick-borne rickettsioses around the world: a geographic approach. Clin. Microbiol. Rev. 26: 657-702.
Go to original source...
Go to PubMed... - Paul R.E.L., Cote M., Le Naour E., Bonnet S.I. 2016: Environmental factors influencing tick densities over seven years in a French suburban forest. Parasite. Vector. 9: 309.
Go to original source...
Go to PubMed... - Pistone D., Pajoro M., Fabbi M., Vicari N., Marone P., Genchi C., Novati S., Sassera S., Epis S., Bandi C. 2010: Lyme Borreliosis, Po River Valley, Italy. Emerg. Infect. Dis. 16: 1289-1291.
Go to original source...
Go to PubMed... - Porretta D., Mastrantonio V., Mona S., Epis S., Montagna M., Sassera D., Bandi C., Urbanelli S. 2013: The integration of multiple independent data reveals an unusual response to Pleistocene climatic changes in the hard tick Ixodes ricinus. Mol. Ecol. 22: 1666-1682.
Go to original source...
Go to PubMed... - R Core team. 2017: R: A language and environment for statistical computing. R Foundation for Statistical computing, Vienna, Austria, www.r-project.org.
- Reiczigel J. 2003: Confidence intervals for the binomial parameter: some new considerations. Stat. Med. 22: 611-621.
Go to original source...
Go to PubMed... - Rizzoli A., Silaghi C., Obiegala A., Rudolf I., Hubálek Z., Földvári G., Plantard O., Vayssier-Taussat M., Bonnet S., ©pitalská E., Kazimírová M. 2014: Ixodes ricinus and its transmitted pathogens in urban and peri-urban areas in Europe: new hazards and relevance for public health. Front. Publ. Hlth. 2: 251.
Go to original source...
Go to PubMed... - Rollend L., Fish D., Childs J.E. 2013: Transovarial transmission of Borrelia spirochetes by Ixodes scapularis: a summary of the literature and recent observations. Ticks Tick Borne Dis. 4: 46-51.
Go to original source...
Go to PubMed... - Roux V., Fournier P.E., Raoult D. 1996: Differentiation of spotted fever group rickettsiae by sequencing and analysis of restriction fragment length polymorphism of PCR-amplified DNA of the gene encoding the protein rOmpA. J. Clin. Microbiol. 34: 2058-2065.
Go to original source...
Go to PubMed... - Røed K.H., Kvie K.S., Hasle G., Gilbert L., Leinaas H.P. 2016: Phylogenetic lineages and postglacial dispersal dynamics characterise the genetic structure of the tick, Ixodes ricinus, in Northwest Europe. PLoS ONE. 11: 0167450.
Go to original source... - Toma L., Mancini F., Di Luca M., Cecere J.G., Bianchi R., Khoury C., Quarchioni E., Manzia F., Rezza G., Ciervo A. 2014: Detection of microbial agents in ticks collected from migratory birds in central Italy. Vector Borne Zoonotic Dis. 14: 199-205.
Go to original source...
Go to PubMed... - Voordouw M.J. 2015: Co-feeding transmission in Lyme disease pathogens. Parasitology 142: 290-302.
Go to original source...
Go to PubMed... - Wallménius K., Barboutis C., Fransson T., Jaenson T.G., Lindgren P.E., Nyström F., Olsen B., Salaneck E., Nilsson K. 2014: Spotted fever Rickettsia species in Hyalomma and Ixodes ticks infesting migratory birds in the European Mediterranean area. Parasit. Vectors. 7: 318.
Go to original source...
Go to PubMed... - Wallménius K., Barboutis C., Fransson T., Jaenson T.G., Lindgren P.E., Nyström F., Olsen B., Salaneck E., Nilsson K. 2014: Spotted fever Rickettsia species in Hyalomma and Ixodes ticks infesting migratory birds in the European Mediterranean area. Parasit. Vectors. 7: 318.
Go to original source...
Go to PubMed...


