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Rickettsia spp. in Dermacentor marginatus ticks: analysis of the host-vector-pathogen interactions in a northern Mediterranean area

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Abstract

In this work, we have analyzed the key features of Rickettsia spp. maintenance in Dermacentor marginatus ticks in four regions of the northern Mediterranean area, where extensive investigations are currently lacking. For this purpose, 380 adult D. marginatus ticks were collected from vegetation and wild ungulates during a 3-year study. A host-vector-pathogen interaction approach was applied to investigate the key components of the disease systems and evaluate their respective weight in the intensity of infection in natural foci. A high variability in the R. slovaca infection rate among sampling sites was observed, whereas R. raoultii was sporadically present and at low infection rates. Dermacentor marginatus presence was confirmed in all the investigated regions. The local wild boar population showed a strong association with adult D. marginatus ticks. The results of this investigation suggest that wild boars not only maintain D. marginatus populations by feeding adult ticks, but may also have a potential role in the eco-epidemiology of rickettsioses, as carriers of rickettsiae-infected ticks. The public health implications of these results are discussed.

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References

  • Angelakis E, Pulcini C, Waton J, Imbert P, Socolovschi C, Edouard S, Dellamonica P, Raoult D (2010) Scalp eschar and neck lymphadenopathy caused by Bartonella henselae after tick bite. Clin Infect Dis 50:549–551

    Article  PubMed  Google Scholar 

  • Azad AF, Beard CB (1998) Rickettsial pathogens and their arthropod vectors. Emerg Infect Dis 4:179–186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benini R (1989) La popolazione di Cinghiale (Sus scrofa L.) dell’isola d’Elba e sua distribuzione in rapporto ai diversi tipi vegetazionali. Tesi di laurea in “Scienze forestali”, Facoltà di Agraria. Università degli Studi di Firenze, A.A. 1988–1989

  • Borsotti G, Arcamone E (1984) Il Cinghiale nel Livornese. Fascicolo tratto dagli Uffici del Museo Provinciale di Storia Naturale di Livorno, 30 settembre 1984

  • Briedermann L (1971) Ermittlungen zur Aktivitätperiodik des Mitteleuropaischen Wildschweines (Sus. scrofa L.). Zool Garten N F Leipzig 40:302–327. (as cited in: Andersson A, Äänismaa R, Huusko J, Jensen P (2011) Behaviour of European wild boars (Sus scrofa) in connection with farrowing in an enclosure. Mamm Biol 76(3):332–338

  • Burgdorfer W (1985) Transovarial transmission: an effective ecological means for the survival of tickborne spotted fever group Rickettsiae, Ann. N.Y. Acad. Sci. 265–271

  • Hasle G, Bjune GA, Røed KH (2009) Transport of ticks by migratory passerine birds to norway. J Parasitol. doi:10.1645/GE-2146.1

    PubMed  Google Scholar 

  • Hoogstraal H, Aeschilimann A (1982) Tick-host specificity. Mitt Schweiz Entomol Ges 55:5–32

    Google Scholar 

  • Inokuma H, Yoshizaki Y, Shimada Y, Sakata Y, Okuda M, Onishi T (2003) Epidemiological survey of Babesia species in Japan performed with specimens from ticks collected from dogs and detection of new Babesia DNA closely related to Babesia odocoilei and Babesia divergens DNA. J Clin Microbiol 41:3494–3498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keskin A, Erciyas-Yavuz K (2016) A Preliminary Investigation on Ticks (Acari: Ixodidae) Infesting Birds in Kizilirmak Delta, Turkey. J Med Entomol 53(1):217–220

    Article  Google Scholar 

  • Kiszewski AE, Matuschka F-R, Spielman A (2001) MSSIT. Annu Rev Entomol 46(1):167–182

    Article  CAS  PubMed  Google Scholar 

  • Labruna MB (2009) Ecology of Rickettsia in South America. Ann N Y Acad Sci 2009(1166):156–166

    Article  Google Scholar 

  • Magdaş C, Magdaş VA, Mihalca AD, Baciu H, Gherman CM, Ştefănuţ CL, Lefkaditis M, Cozma V (2015) Laboratory development of Dermacentor marginatus ticks (Acari: Ixodidae) at two temperatures. Exp Appl Acarol 67(2):309–315. doi:10.1007/s10493-015-9942-z

    Article  PubMed  Google Scholar 

  • Manilla G (1998) Fauna d’Italia. Acari: Ixodida. Edizioni Calderini, Bologna

    Google Scholar 

  • Márquez FJ (2008) Spotted fever group Rickettsia in ticks from southeastern Spain natural parks. Exp Appl Acarol. doi:10.1007/s10493-008-9181-7

    PubMed  Google Scholar 

  • Martello E, Selmi M, Ragagli C, Ambrogi C, Stella MC, Mannelli A, Tomassone L (2013) Rickettsia slovaca in immature Dermacentor marginatus and tissues from Apodemus spp. in the northern Apennines, Italy. Ticks Tick Borne Dis 4:518–521

    Article  PubMed  Google Scholar 

  • Masala G, Chisu V, Satta G, Socolovschi C, Raoult D, Parola P (2012) Rickettsia slovaca from Dermacentor marginatus ticks in Sardinia, Italy. Ticks Tick Borne Dis 3(5–6):393–395. doi:10.1016/j.ttbdis.2012.10.007

    Article  PubMed  Google Scholar 

  • Merhej V, Raoult D (2011) Rickettsial evolution in the light of comparative genomics. Biol Rev Camb Philos Soc 86:379–405

    Article  PubMed  Google Scholar 

  • Niebylski ML, Peacock MG, Schwan TG (1999) Lethal effect of Rickettsia rickettsii on its tick vector (Dermatocentor andersoni). Appl Environ Microbiol 65:773–778

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nosek J (1972) The ecology and public health importance of Dermacentor marginatus and D. reticulatus ticks in Central Europe. Folia Parasitol (Praha) 19:93–102

    CAS  Google Scholar 

  • Otranto D, Dantas-Torres F, Giannelli A, Latrofa MS, Cascio A, Cazzin S, Ravagnan S, Montarsi F, Zanzani SA, Manfredi MT, Capelli G (2014) Ticks infesting humans in Italy and associated pathogens. Parasite Vectors 7:328

    Article  Google Scholar 

  • Parola P, Paddock CD, Raoult D (2005) Tick-borne rickettsioses around the world: emerging diseases challenging old concepts. Clin Microbiol Rev 18:719–756

    Article  PubMed  PubMed Central  Google Scholar 

  • Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T, Yazid Abdad M, Stenos J, Bitam I, Fournier PE, Raoult D (2014) Update on tick-borne Rickettsioses around the world: a geographic approach. Clin Microbiol Rev 26(4):657–702

    Article  Google Scholar 

  • Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644

    Article  Google Scholar 

  • Perlman SJ, Hunter MS, Zchori-Fein E (2006) The emerging diversity of Rickettsia. Proc Biol Sci 273:2097–2106

    Article  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Regnery RL, Spruill CL, Plikaytis BD (1991) Genotypic identification of rickettsiae and estimation of intra species sequence divergence for portions of two rickettsial genes. J Bacteriol 173:1576–1589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rehácek J (1989) Ecological relationships between ticks and Rickettsiae. Eur J Epidemiol 5:407–413

    Article  PubMed  Google Scholar 

  • Rehácek J, Liebisch A, Urvölgyi J, Kovacova E (1977) Rickettsiae of the spotted fever group isolated from Dermacentor marginatus ticks in south Germany. Zentralbl Bakteriol [Orig A] 239:275–281

    Google Scholar 

  • Roux V, Raoult D (2000) Phylogenetic analysis of the members of the genus Rickettsia using the gene encoding the outer-membrane protein rOmpB (ompB). Int J Syst Evol Microbiol 50:1449–1455

    Article  CAS  PubMed  Google Scholar 

  • Rubel F, Brugger K, Pfeffer M, Chitimia-Dobler L, Didyk YM, Leverenz S et al (2016) Geographical distribution of Dermacentor marginatus and Dermacentor reticulatus in Europe. Ticks Tick Borne Dis 7:224–233

    Article  PubMed  Google Scholar 

  • Samoylenko I, Shpynov S, Raoult D, Rudakov N, Fournier PE (2009) Evaluation of Dermacentor species naturally infected with Rickettsia raoultii. Clin Microbiol Infect 15(Suppl 2):305–306

    Article  PubMed  Google Scholar 

  • Selmi M, Bertolotti L, Tomassone L, Mannelli A (2008) Rickettsia slovaca in Dermacentor marginatus and tick-borne lymphadenopathy, Tuscany, Italy. Emerg Infect Dis 14:817–820

    Article  PubMed  PubMed Central  Google Scholar 

  • Selmi M, Martello E, Bertolotti L, Bisanzio D, Tomassone L (2009) Rickettsia slovaca and Rickettsia raoultii in Dermacentor marginatus ticks collected on wild boars in Tuscany, Italy. J Med Entomol 46:1490–1493

    Article  PubMed  Google Scholar 

  • Socolovschi C, Mediannikov O, Raoult D, Parola P (2009) The relationship between spotted fever group Rickettsiae and Ixodid ticks. Vet Res 40(2):34

    Article  PubMed  PubMed Central  Google Scholar 

  • Špitalská E, Štefanidesová K, Kocianová E, Boldiš V (2012) Rickettsia slovaca and Rickettsia raoultii in Dermacentor marginatus and Dermacentor reticulatus ticks from Slovak Republic. Exp Appl Acarol 57:189–197

    Article  PubMed  Google Scholar 

  • Uspensky I (2014) Tick pests and vectors (Acari: Ixodoidea) in European towns: Introduction, persistence and management. Tick Borne Dis 5:41–47

    Article  Google Scholar 

  • Yesilbag K, Aydin L, Dincer E, Alpay G, Girisgin AO, Tuncer P, Ozkul A (2013) Tick survey and detection of Crimean-Congo hemorrhagic fever virus in tick species from a non-endemic area, South Marmara region, Turkey. Exp Appl Acarol 60:253–261

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We wish to thank Francesca Giannini and Silvia Contu for the coordination of the hunting teams and for their assistance in collecting specimens. In particular, the authors thank Walter Mignone, head of the local branch of IZSPLV in Imperia, Italy, for his invaluable support and advice. We are also grateful to Alessandro Mannelli and Gianluca Fichi for the inspiring conversations on the topic. This study was supported by the EU-funded projects “Réseau transfrontalier de démoustication et de lutte anti-vectorielle” (REDLAV) and “Réseau durable transfrontalier de démoustication et de lutte anti-vectorielle” (REDLAV 2.1), under the Programmes Interreg Italie-France Maritime 2007–2013 and 2014–2020.

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Correspondence to Marco Selmi.

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Selmi, M., Ballardini, M., Salvato, L. et al. Rickettsia spp. in Dermacentor marginatus ticks: analysis of the host-vector-pathogen interactions in a northern Mediterranean area. Exp Appl Acarol 72, 79–91 (2017). https://doi.org/10.1007/s10493-017-0132-z

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