Abstract
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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
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. https://doi.org/10.1086/650172
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. https://doi.org/10.4269/ajtmh.2011.10-0355
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. https://doi.org/10.1016/j.ttbdis.2017.04.005
Brites-Neto J, Duarte KMR, Martins TF (2015) Tick-borne infections in human and animal population worldwide. Vet world 8:301–315. https://doi.org/10.14202/vetworld.2015.301-315
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. https://doi.org/10.3201/eid1905.121169
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. https://doi.org/10.1016/j.ttbdis.2016.12.007
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. https://doi.org/10.1016/j.ttbdis.2018.02.008
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. https://doi.org/10.1016/j.ttbdis.2012.10.003
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: https://doi.org/10.1128/genomeA.00157-16
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
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 48:839–849
Germanakis A, Chochlakis D, Angelakis E, Tselentis Y, Psaroulaki A (2013) Rickettsia aeschlimannii infection in a man, Greece. Emerging Infect Dis 19:1176–1177. https://doi.org/10.3201/eid1907.130232
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95–98
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. https://doi.org/10.3201/eid1309.060186
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. https://doi.org/10.3389/fcimb.2017.00114
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. https://doi.org/10.1093/bioinformatics/btm404
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. https://doi.org/10.1007/s15010-016-0921-z
Manilla G (1998) Acari, Ixodida. Fauna d’Italia 36. Edizioni Calderini, Bologna
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. https://doi.org/10.1016/j.ttbdis.2012.10.006
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. https://doi.org/10.1016/j.ttbdis.2012.10.007
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. https://doi.org/10.1099/ijs.0.64952-0
Merhej V, Angelakis E, Socolovschi C, Raoult D (2014) Genotyping, evolution and epidemiological findings of Rickettsia species. Infect Genet Evol 25:122–137. https://doi.org/10.1016/j.meegid.2014.03.014
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. https://doi.org/10.3201/eid1507.081449
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. https://doi.org/10.1128/CMR.00032-13
Portillo A, Santibáñez S, García-Álvarez L, Palomar AM, Oteo JA (2015) Rickettsioses in Europe. Microbes Infect 17:834–838. https://doi.org/10.1016/j.micinf.2015.09.009
Pretorius A-M, Birtles RJ (2002) Rickettsia aeschlimannii: a new pathogenic spotted fever group rickettsia, South Africa. Emerging Infect Dis 8:874. https://doi.org/10.3201/eid0805.020199
Raoult D, Fournier P-E, Abboud P, Caron F (2002) First documented human Rickettsia aeschlimannii infection. Emerging Infect Dis 8:748–749. https://doi.org/10.3201/eid0807.010480
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 50:1449–5145
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 47:252–261
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. https://doi.org/10.1007/s10493-006-9008-3
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. https://doi.org/10.1099/jmm.0.021543-0
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. https://doi.org/10.1093/molbev/mst197
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 22:4673–4680
Vitale G, Mansuelo S, Rolain J-M, Raoult D (2006) Rickettsia massiliae human isolation. Emerging Infect Dis 12:174–175. https://doi.org/10.3201/eid1201.050850
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. https://doi.org/10.1186/1756-3305-7-318
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
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.
Additional information
Section Editor: Boris R. Krasnov
Rights and permissions
About this article
Cite this article
Chisu, V., Foxi, C. & Masala, G. First molecular detection of the human pathogen Rickettsia raoultii and other spotted fever group rickettsiae in Ixodid ticks from wild and domestic mammals. Parasitol Res 117, 3421–3429 (2018). https://doi.org/10.1007/s00436-018-6036-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-018-6036-y