Parasitology Research

, Volume 117, Issue 11, pp 3421–3429 | Cite as

First molecular detection of the human pathogen Rickettsia raoultii and other spotted fever group rickettsiae in Ixodid ticks from wild and domestic mammals

  • Valentina Chisu
  • Cipriano Foxi
  • Giovanna Masala
Original Paper


Tick-borne rickettsioses are recognized as emerging vector-borne infections capable of infecting both human and animal hosts worldwide. This study focuses on the detection and molecular identification of species belonging to the genus Rickettsia in ticks sampled from human, vegetation, and domestic and wild vertebrates in Sardinia. Ticks were tested by PCR targeting gltA, ompA, and ompB genes, followed by sequencing analysis. The results provide evidences of a great variety of Rickettsia species of the Spotted fever group in Ixodid ticks and allow establishing for the first time the presence of R. raoultii in Rhipicephalus sanguineus s.l. and Dermacentor marginatus ticks in Sardinia island. Rickettsia massiliae was detected on R. sanguineus s.l. and R. aeschlimannii in Hyalomma marginatum and Hy. lusitanicum ticks. In addition, eight D. marginatus ticks were positive for R. slovaca. This study provides further evidence that different Rickettsia species are widespread in Sardinian ticks and that detailed investigations are required to understand the role these tick species play on spotted fever group rickettsiae circulation. More studies will provide new background on molecular epidemiology of zoonotic rickettsiae, the geographical distribution of tick-transmitted rickettsial pathogens, and the involvement of vertebrate hosts in propagation and maintenance of these bacteria in nature.


Ticks Tick-borne rickettsioses Rickettsiosis 


Compliance with ethical standards

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animal were followed. All procedures performed in studies involving human participant were in accordance with the ethical standards of the institutional and/or national ethic committee. A written informed consent was obtained from patients at the time of hospitalization. The Istituto Zooprofilattico Sperimentale of Sardinia was authorized by the ethics committee of the Local Health Authority of Sassari (Comitato di Bioetica, ASL N. 1, Sassari) Prot N. 1136, to analyze human sera following the request of the National Health Service doctors, since 03/26/2013.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. CrossRefGoogle Scholar
  2. 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. CrossRefPubMedGoogle Scholar
  3. Beeler E, Abramowicz KF, Zambrano ML, Sturgeon MM, Khalaf N, Hu R, Dasch GA, Eremeeva ME (2011) A focus of dogs and Rickettsia massiliae-infected Rhipicephalus sanguineus in California. Am J Trop Med Hyg 84:244–249. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Blanda V, Torina A, La Russa F, D'Agostino R, Randazzo K, Scimeca S, Giudice E, Caracappa S, Cascio A, de la Fuente J (2017) A retrospective study of the characterization of Rickettsia species in ticks collected from humans. Ticks Tick Borne Dis 8:610–614. CrossRefPubMedGoogle Scholar
  5. Brites-Neto J, Duarte KMR, Martins TF (2015) Tick-borne infections in human and animal population worldwide. Vet world 8:301–315. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cascio A, Torina A, Valenzise M, Blanda V, Camarda N, Bombaci S, Iaria C, De Luca F, Wasniewska M (2013) Scalp eschar and neck lymphadenopathy caused by Rickettsia massiliae. Emerging Infect Dis 19:836–837. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Chisu V, Leulmi H, Masala G, Piredda M, Foxi C, Parola P (2017) Detection of Rickettsia hoogstraalii, Rickettsia helvetica, Rickettsia massiliae, Rickettsia slovaca and Rickettsia aeschlimannii in ticks from Sardinia, Italy. Ticks Tick Borne Dis 8:347–352. CrossRefPubMedGoogle Scholar
  8. Chisu V, Foxi C, Mannu R, Satta G, Masala G (2018) A five-year survey of tick species and identification of tick-borne bacteria in Sardinia, Italy. Ticks Tick Borne Dis 9:678–681. CrossRefPubMedGoogle Scholar
  9. Demoncheaux J-P, Socolovschi C, Davoust B, Haddad S, Raoult D, Parola P (2012) First detection of Rickettsia aeschlimannii in Hyalomma dromedarii ticks from Tunisia. Ticks Tick Borne Dis 3:398–402. CrossRefPubMedGoogle Scholar
  10. El Karkouri K, Mediannikov O, Robert C, Raoult D, Fournier PE (2016) Genome sequence of the tick-borne pathogen Rickettsia raoultii. Genome Announc 4:. doi:
  11. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. CrossRefGoogle Scholar
  12. Fournier PE, Roux V, Raoult D (1998) Phylogenetic analysis of spotted fever group rickettsiae by study of the outer surface protein rOmpA. Int J Syst Bacteriol 48:839–849CrossRefGoogle Scholar
  13. Germanakis A, Chochlakis D, Angelakis E, Tselentis Y, Psaroulaki A (2013) Rickettsia aeschlimannii infection in a man, Greece. Emerging Infect Dis 19:1176–1177. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95–98Google Scholar
  15. Jado I, Oteo JA, Aldámiz M, Escudero R, Ibarra V, Portu J, Portillo A, Lezaun MJ, García-Amil C, Rodríguez-Moreno I, Anda P (2007) Rickettsia monacensis and human disease, Spain. Emerging Infect Dis 13:1405–1407. CrossRefPubMedPubMedCentralGoogle Scholar
  16. de la Fuente J, Antunes S, Bonnet S, Cabezas-Cruz A, Domingos AG, Estrada-Peña A, Johnson N, Kocan KM, Mansfield KL, Nijhof AM, Papa A, Rudenko N, Villar M, Alberdi P, Torina A, Ayllón N, Vancova M, Golovchenko M, Grubhoffer L, Caracappa S, Fooks AR, Gortazar C, Rego ROM (2017) Tick-pathogen interactions and vector competence: identification of molecular drivers for tick-borne diseases. Front Cell Infect Microbiol 7:114. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. CrossRefPubMedGoogle Scholar
  18. Madeddu G, Fiore V, Mancini F, Caddeo A, Ciervo A, Babudieri S, Masala G, Bagella P, Nunnari G, Rezza G, Mura MS (2016) Mediterranean spotted fever-like illness in Sardinia, Italy: a clinical and microbiological study. Infection 44:733–738. CrossRefPubMedGoogle Scholar
  19. Manilla G (1998) Acari, Ixodida. Fauna d’Italia 36. Edizioni Calderini, BolognaGoogle Scholar
  20. Masala G, Chisu V, Foxi C, Socolovschi C, Raoult D, Parola P (2012a) First detection of Ehrlichia canis in Rhipicephalus bursa ticks in Sardinia, Italy. Ticks Tick Borne Dis 3:396–397. CrossRefPubMedGoogle Scholar
  21. Masala G, Chisu V, Satta G, Socolovschi C, Raoult D, Parola P (2012b) Rickettsia slovaca from Dermacentor marginatus ticks in Sardinia, Italy. Ticks Tick Borne Dis 3:393–395. CrossRefPubMedGoogle Scholar
  22. Mediannikov O, Matsumoto K, Samoylenko I, Drancourt M, Roux V, Rydkina E, Davoust B, Tarasevich I, Brouqui P, Fournier PE (2008) Rickettsia raoultii sp. nov., a spotted fever group rickettsia associated with Dermacentor ticks in Europe and Russia. Int J Syst Evol Microbiol 58:1635–1639. CrossRefPubMedGoogle Scholar
  23. Merhej V, Angelakis E, Socolovschi C, Raoult D (2014) Genotyping, evolution and epidemiological findings of Rickettsia species. Infect Genet Evol 25:122–137. CrossRefPubMedGoogle Scholar
  24. Parola P, Rovery C, Rolain JM, Brouqui P, Davoust B, Raoult D (2009) Rickettsia slovaca and R. raoultii in tick-borne Rickettsioses. Emerging Infect Dis 15:1105–1108. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T, Abdad MY, Stenos J, Bitam I, Fournier PE, Raoult D (2013) Update on tick-borne rickettsioses around the world: a geographic approach. Clin Microbiol Rev 26:657–702. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Portillo A, Santibáñez S, García-Álvarez L, Palomar AM, Oteo JA (2015) Rickettsioses in Europe. Microbes Infect 17:834–838. CrossRefPubMedGoogle Scholar
  27. Pretorius A-M, Birtles RJ (2002) Rickettsia aeschlimannii: a new pathogenic spotted fever group rickettsia, South Africa. Emerging Infect Dis 8:874. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Raoult D, Fournier P-E, Abboud P, Caron F (2002) First documented human Rickettsia aeschlimannii infection. Emerging Infect Dis 8:748–749. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Roux V, Raoult D (2000) Phylogenetic analysis of members of the genus Rickettsia using the gene encoding the outer-membrane protein rOmpB (ompB). Int J Syst Evol Microbiol 50:1449–5145CrossRefGoogle Scholar
  30. Roux V, Rydkina E, Eremeeva M, Raoult D (1997) Citrate synthase gene comparison, a new tool for phylogenetic analysis, and its application for the rickettsiae. Int J Syst Bacteriol 47:252–261CrossRefGoogle Scholar
  31. Santos-Silva MM, Sousa R, Santos AS, Melo P, Encarnação V, Bacellar F (2006) Ticks parasitizing wild birds in Portugal: detection of Rickettsia aeschlimannii, R. helvetica and R. massiliae. Exp Appl Acarol 39:331–338. CrossRefPubMedGoogle Scholar
  32. Satta G, Chisu V, Cabras P, Fois F, Masala G (2011) Pathogens and symbionts in ticks: a survey on tick species distribution and presence of tick-transmitted micro-organisms in Sardinia, Italy. J Med Microbiol 60:63–68. CrossRefPubMedGoogle Scholar
  33. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  35. Vitale G, Mansuelo S, Rolain J-M, Raoult D (2006) Rickettsia massiliae human isolation. Emerging Infect Dis 12:174–175. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Wallménius K, Barboutis C, Fransson T, Jaenson TG, Lindgren PE, 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. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Valentina Chisu
    • 1
  • Cipriano Foxi
    • 1
  • Giovanna Masala
    • 1
  1. 1.Istituto Zooprofilattico Sperimentale della SardegnaSassariItaly

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