Abstract
Ticks are vectors for a variety of human and animal pathogens (bacteria, protozoa and viruses). In order to investigate the pathogens carried by ticks in Greece, a total of 179 adult ticks (114 female and 65 male) were collected from domestic animals (sheep, goats and dogs) from 14 prefectures of six regions of Greece. Among them, 40 were Dermacentor marginatus, 25 Haemaphysalis parva, 22 H. sulcata, one H. punctata, 13 Ixodes gibbosus, 77 Rhipicephalus sanguineus s.l. and one R. bursa. All ticks were tested for the presence of DNA of Anaplasma spp., Babesia spp., Coxiella burnetii, Rickettsia spp. and Theileria spp. The collected ticks were examined by PCR and reverse line blot (RLB) assay. A prevalence of 20.1% for Anaplasma spp., 15.6% for Babesia spp. (identifying B. bigemina, B. divergens, B. ovis and B. crassa), 17.9% for C. burnetii, 15.1% for Rickettsia spp., and 21.2% for Theileria spp. (identifying T. annulata, T. buffeli/orientalis, T. ovis and T. lestoquardi) was found. The results of this study demonstrate the variety of tick-borne pathogens of animal and human importance circulating in Greece, and that awareness is needed to minimize the risk of infection, especially among farmers and pet owners.
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References
Atkinson SF, Sarkar S, Aviña A, Schuermann JA, Williamson P (2012) Modelling spatial concordance between Rocky Mountain spotted fever disease incidence and habitat probability of its vector Dermacentor variabilis (American dog tick). Geospat Health 7:91–100. https://doi.org/10.4081/gh.2012.108
Babalis T, Tselentis Y, Roux V, Psaroulaki A, Raoult D (1994) Isolation and identification of a rickettsial strain related to Rickettsia massiliae in Greek ticks. Am J Trop Med Hyg 50:365–372. https://doi.org/10.4269/ajtmh.1994.50.365
Bonnet S, de la Fuente J, Nicollet P, Liu X, Madani N, Blanchard B, Maingourd C, Alongi A, Torina A, Fernández de Mera IG, Vicente J, George JC, Vayssier-Taussat M, Joncour G (2013) Prevalence of tick-borne pathogens in adult Dermacentor spp. ticks from nine collection sites in France. Vector Borne Zoonotic Dis 13:226–236. https://doi.org/10.1089/vbz.2011.0933
Chaligiannis I, Musella V, Rinaldi L, Cringoli G, de la Fuente J, Papa A, Sotiraki S (2016) Species diversity and spatial distribution of ixodid ticks on small ruminants in Greece. Parasitol Res 115:4673–4680. https://doi.org/10.1007/s00436-016-5259-z
Chochlakis D, Psaroulaki A, Kokkini S, Kostanatis S, Arkalati E, Karagrannaki E, Tsiatis K, Tselentis Y, Gikas A (2009) First evidence of Anaplasma infection in Crete, Greece. Report of six human cases. Clin Microbiol Infect 15:8–9. https://doi.org/10.1111/j.1469-0691.2008.02695.x
Estrada-Pena A, Bouattour A, Camicas J, Walker A (2004) Ticks of domestic animals in the Mediterranean region: a guide to identification of species. University of Zaragoza, Spain
Germanakis A, Chochlakis D, Angelakis E, Tselentis Y, Psaroulaki A (2013) Rickettsia aeschlimannii infection in a man, Greece. Emerg Infect Dis 19:1176–1177. https://doi.org/10.3201/eid1907.130232
Giadinis ND, Chochlakis D, Ioannou I, Kritsepi-Konstantinou M, Papadopoulos E, Psaroulaki A, Karatzias H (2011) Haemorrhagic diathesis in a ram with Anaplasma phagocytophilum infection. J Comp Pathol 144:82–85. https://doi.org/10.1016/j.jcpa.2010.04.011
Giadinis N, Katsoulos P, Chochlakis D, Tselentis Y, Ntais P, Lafi S, Karatzias H, Psaroulaki A (2015) Serological investigation for West Nile virus, Anaplasma ovis and Leishmania infantum in Greek cattle. Vet Ital 51:205–209. https://doi.org/10.12834/VetIt.174.523.4
Gonzalez-Barrio D, Velasco Avila AL, Boadella M, Beltran-Beck B, Barasona JA, Santos JPV, Queiros J, García-Pérez AL, Barral M, Ruiz-Fons F (2015) Host and environmental factors modulate the exposure of free ranging and farmed red deer (Cervus elaphus) to Coxiella burnetii. Appl Environ Microbiol 81:6223–6231. https://doi.org/10.1128/AEM.01433-15
Gray J, Zintl A, Hildebrandt A, Hunfeld KP, Weiss L (2010) Zoonotic babesiosis: overview of the disease and novel aspects of pathogen identity. Ticks Tick Borne Dis 1:3–10. https://doi.org/10.1016/j.ttbdis.2009.11.003
Kachrimanidou M, Papa A, Choclakis D, Pavlidou V, Psaroulaki A (2011) Molecular evidence for Anaplasma phagocytophilum in Ixodes ricinus ticks from Greece. Vector Borne Zoonotic Dis 11:1391–1393. https://doi.org/10.1089/vbz.2010.0251
Kokkini S, Kofteridis D, Psaroulaki A, Sipsas N, Tsiodras S, Giannitsiotiand E, Gikas A (2009) Q fever endocarditis in Greece: report of five cases. Clin Microbiol Infect 2:136–137. https://doi.org/10.1111/j.1469-0691.2008.02639.x
Kostopoulou V, Chochlakis D, Kanta C, Katsanou A, Rossiou K, Rammos A, Papadopoulos SF, Katsarou T, Tselentis Y, Psaroulaki A, Boukas C (2016) A case of human infection by Rickettsia slovaca in Greece. Jpn J Infect Dis 69:335–337
Latrofa MS, Angelou A, Giannelli A, Annoscia G, Ravagnan S, Dantas-Torres F, Capelli G, Halos L, Beugnet F, Papadopoulos E, Otranto D (2017) Ticks and associated pathogens in dogs from Greece. Parasit Vectors 10:301. https://doi.org/10.1186/s13071-017-2225-2
Maurin M, Raoult D (1999) Q fever. Clin Microbiol Rev 12:518–553
Ogo NI, Fernandez de Mera IG, Galindo RC, Okubanjo OO, Inuwa HM, Agbede RIS, Torina A, Alongi A, Vicente J, Gortazar C, de la Fuente J (2012) Molecular identification of tick-borne pathogens in Nigerian ticks. Vet Parasitol 187:572–577. https://doi.org/10.1016/j.vetpar.2012.01.029
Papa A, Chaligiannis I, Xanthopoulou K, Papaioakim M, Papanastasiou S, Sotiraki S (2011) Ticks parasitizing humans in Greece. Vector Borne Zoonotic Dis 11:539–542. https://doi.org/10.1089/vbz.2010.0036
Papa A, Xanthopoulou K, Kotriotsiou T, Papaioakim M, Sotiraki S, Chaligiannis I, Maltezos E (2016) Rickettsia species in human-parasitizing ticks in Greece. Trans R Soc Trop Med Hyg 110:299–304. https://doi.org/10.1093/trstmh/trw022
Papa A, Tsioka K, Kontana A, Papadopoulos C, Giadinis N (2017) Bacterial pathogens and endosymbionts in ticks. Ticks Tick Borne Dis 8:31–35. https://doi.org/10.1016/j.ttbdis.2016.09.011
Papadopoulos B, Morel PC, Aeschlimann A (1996a) Ticks of domestic animals in the Macedonia region of Greece. Vet Parasitol 63:25–40
Papadopoulos B, Brossard M, Perié NM (1996b) Piroplasms of domestic animals in the Macedonia region of Greece. 2. Piroplasms of cattle. Vet Parasitol 63:57–66
Papadopoulos B, Brossard M, Perié NM (1996c) Piroplasms of domestic animals in the Macedonia region of Greece. 3. Piroplasms of small ruminants. Vet Parasitol 63:67–74
Papazahariadou MG, Papadopoulos EG, Himonas CA (1995) Seasonal activity of ixodid ticks on goats in northern Greece. Vet Rec 136:585–588. https://doi.org/10.1136/vr.136.23.585
Papazahariadou MG, Saridomichelakis MN, Koutinas AF, Papadopoulos EG, Leontides L (2003) Tick infestation of dogs in Thessaloniki, northern Greece. Med Vet Entomol 17:110–113. https://doi.org/10.1046/j.1365-2915.2003.00404.x
Pavlidou V, Gerou S, Kahrimanidou M, Papa A (2008) Ticks infesting domestic animals in northern Greece. Exp Appl Acarol 45:195–198. https://doi.org/10.1007/s10493-008-9167-5
Perez-Eid C (2007) Les tiques. Identification, biologie, importance médicale et vétérinaire. TEC & DOC Lavoisier, Paris
Psaroulaki A, Spyridaki I, Ioannidis A, Babalis T, Gikas A, Tselentis Y (2003) First isolation and identification of Rickettsia conorii from ticks collected in the region of Fokida in Central Greece. J Clin Microbiol 41:3317–3319. https://doi.org/10.1128/JCM.41.7.3317-3319
Psaroulaki A, Germanakis A, Gikas A, Scoulica E, Tselentis Y (2005a) Simultaneous detection of Rickettsia mongolotimonae in a patient and in a tick in Greece. J Clin Microbiol 43:3558–3559. https://doi.org/10.1128/JCM.43.7.3558-3559
Psaroulaki A, Germanakis A, Gikas A, Scoulica E, Tselentis Y (2005b) First isolation and genotypic identification of Rickettsia conorii Malish 7 from a patient in Greece. Eur J Clin Microbiol Infect Dis 24:297–298. https://doi.org/10.1007/s10096-005-1304-z
Psaroulaki A, Ragiadakou D, Kouris G, Papadopoulos B, Chaniotis B, Tselentis Y (2006) Ticks, tick-borne rickettsiae, and Coxiella burnetii in the Greek Island of Cephalonia. Ann N Y Acad Sci 1078:389–399. https://doi.org/10.1196/annals.1374.077
Ruiz-Fons F, Fernández de Mera IG, Acevedo P, Höfle U, Vicente J, de la Fuente J, Gortazar C (2006) Ticks (Acari: Ixodidae) parasitizing Iberian red deer (Cervus elaphus hispanicus) and European wild boar (Sus scrofa) from Spain: geographical and temporal distribution. Vet Parasitol 140:133–142. https://doi.org/10.1016/j.vetpar.2006.03.033
Uilenberg G (2001) Babesiosis. In: Service MW (ed) Encyclopedia of arthropod-transmitted infectious of man and domesticated animals. CABI Publishing, Wallingford, pp 53–60
Acknowledgements
The authors gratefully acknowledge all the veterinarians who contributed in the study by providing the samples. This study was financially supported by the State Scholarship Foundation IKY, NSRF 2007–2013. IGFM is funded from the Own Research Program by University of Castilla-La Mancha.
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Chaligiannis, Ι., Fernández de Mera, I.G., Papa, A. et al. Molecular identification of tick-borne pathogens in ticks collected from dogs and small ruminants from Greece. Exp Appl Acarol 74, 443–453 (2018). https://doi.org/10.1007/s10493-018-0237-z
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DOI: https://doi.org/10.1007/s10493-018-0237-z