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Experimental and Applied Acarology

, Volume 79, Issue 2, pp 267–278 | Cite as

Prevalence and molecular characterization of Rickettsia spp. in questing ticks from north-western Spain

  • Susana Remesar
  • Pablo DíazEmail author
  • Aránzazu Portillo
  • Sonia Santibáñez
  • Alberto Prieto
  • José M. Díaz-Cao
  • Ceferino M. López
  • Rosario Panadero
  • Gonzalo Fernández
  • Pablo Díez-Baños
  • José A. Oteo
  • Patrocinio Morrondo
Article

Abstract

Tick-borne rickettsioses, most of them belonging to the spotted fever group (SFG), have been recognized as important emerging vector-borne zoonotic diseases. In order to determine the presence of Rickettsia spp. in questing ticks from north-western Spain, 1056 Ixodes ricinus, 19 Dermacentor marginatus, 17 Dermacentor reticulatus and one Ixodes acuminatus were processed. Rickettsia DNA was detected by PCR targeting rOmpA and rOmpB genes. A total of 219 (20.7%) I. ricinus, 19 (100%) D. marginatus and four D. reticulatus (23.5%) were positive. The prevalence was significantly higher in I. ricinus from coastal areas and in winter. Five species were identified: Rickettsia felis, Rickettsia monacensis, Rickettsia raoultii, Rickettsia slovaca and “Candidatus Rickettsia rioja”. Our results reveal a significant presence of some pathogenic Rickettsia species in questing tick populations from this area which involves a noticeable risk of rickettsiosis. As R. raoultii, R. slovaca and “Ca. R. rioja” DNA were identified in I. ricinus, considered an unusual vector for these Rickettsia species, further studies are needed to unravel the role of that tick species in the maintenance and transmission of these three Rickettsia species in north-western Spain.

Keywords

Rickettsia Dermacentor Ixodes Tick-borne diseases Spain Zoonoses 

Notes

Acknowledgements

This research was supported by the Programme for Consolidating and Structuring Competitive Research Groups (GRC2015/003; Xunta de Galicia, Spain) and by a predoctoral grant (European Social Fund, Secretaría Xeral de Universidades, Xunta de Galicia, Spain).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10493_2019_426_MOESM1_ESM.xlsx (82 kb)
Supplementary material 1 (XLSX 81 kb)

References

  1. Barandika JF, Hurtado A, García-Sanmartin J, Juste RA, Anda P, García-Perez AL (2008) Prevalence of tick-borne zoonotic bacteria in questing adult ticks from northern Spain. Vector Borne Zoonotic Dis 8:829–835CrossRefPubMedGoogle Scholar
  2. Boldis V, Spitalska E (2010) Dermacentor marginatus and Ixodes ricinus ticks versus L929 and Vero cell lines in Rickettsia slovaca life cycle evaluated by quantitative real time PCR. Exp Appl Acarol 50:353–359CrossRefPubMedGoogle Scholar
  3. Burri C, Dupasquier C, Bastic V, Gern L (2011) Pathogens of Emerging Tick-Borne Diseases, Anaplasma phagocytophilum, Rickettsia spp., and Babesia spp., in Ixodes ticks collected from rodents at four sites in Switzerland (Canton of Bern). Vector Borne Zoonotic Dis 11:939–944CrossRefPubMedGoogle Scholar
  4. Chmielewski T, Podsiadly E, Karbowiak G, Tylewska-Wierzbanowska S (2009) Rickettsia spp. in ticks, Poland. Emerg Infect Dis 15:486–488CrossRefPubMedPubMedCentralGoogle Scholar
  5. Choi YJ, Lee SH, Park KH, Koh YS, Lee KH, Baik HS et al (2005) Evaluation of PCR-based assay for diagnosis of spotted fever group rickettsiosis in human serum samples. Clin Diagn Lab Immunol 12:759–763PubMedPubMedCentralGoogle Scholar
  6. Dautel H, Dippel C, Oehme R, Hartelt K, Schettler E (2006) Evidence for an increased geographical distribution of Dermacentor reticulatus in Germany and detection of Rickettsia sp. RpA4. Int J Med Microbiol 296:149–156CrossRefPubMedGoogle Scholar
  7. Dobec M, Golubic D, Punda-Polic V, Kaeppeli F, Sievers M (2009) Rickettsia helvetica in Dermacentor reticulatus ticks. Emerg Infect Dis 15:98–100CrossRefPubMedPubMedCentralGoogle Scholar
  8. Dobler G, Wolfel R (2009) Typhus and other rickettsioses emerging infections in Germany. Dtsch Arztebl Int 106:348–354PubMedPubMedCentralGoogle Scholar
  9. Elfving K, Olsen B, Bergstrom S, Waldenstrom J, Lundkvist A, Sjostedt A et al (2010) Dissemination of spotted fever rickettsia agents in Europe by migrating birds. PLoS ONE 5:e8572CrossRefPubMedPubMedCentralGoogle Scholar
  10. Estrada-Peña A, de la Fuente J (2014) Toward a multidisciplinary approach to the study of tick-borne diseases. Front Cell Infect Microbiol 4:118PubMedPubMedCentralGoogle Scholar
  11. Fernández de Mera IG, Ruíz-Fons F, de la Fuente G, Mangold AJ, Gortázar C, de la Fuente J (2013) Spotted fever group rickettsiae in questing ticks, Central Spain. Emerg Infect Dis 19:1163–1165CrossRefPubMedPubMedCentralGoogle Scholar
  12. Floris R, Yurtman AN, Margoni EF, Mignozzi K, Boemo B, Altobelli A et al (2008) Detection and identification of Rickettsia species in the northeast of Italy. Vector Borne Zoonotic Dis 8:777–782CrossRefPubMedGoogle Scholar
  13. Ibarra V, Portillo A, Santibáñez S, Blanco JR, Pérez-Martinez L, Márquez J et al (2005) DEBONEL/TIBOLA—is Rickettsia slovaca the only etiological agent? Rickettsioses: from genome to proteome, pathobiology, and Rickettsiae as an international threat. Ann N Y Acad Sci 1063:346–348CrossRefPubMedGoogle Scholar
  14. Jado I, Oteo JA, Aldámiz M, Gil H, Escudero R, Ibarra V et al (2007) Rickettsia monacensis and human disease, Spain. Emerg Infect Dis 13:1405–1407CrossRefPubMedPubMedCentralGoogle Scholar
  15. Labruna MB, Whitworth T, Bouyer DH, McBride J, Camargo LMA, Camargo EP et al (2004) Rickettsia bellii and Rickettsia amblyommii in Amblyomma ticks from the State of Rondonia, Western Amazon, Brazil. J Med Entomol 41:1073–1081CrossRefPubMedGoogle Scholar
  16. Márquez FJ (2008) Spotted fever group Rickettsia in ticks from southeastern Spain natural parks. Exp Appl Acarol 45:185–194CrossRefPubMedGoogle Scholar
  17. Márquez FJ, Millán J (2009) Rickettsiae in ticks from wild and domestic carnivores of Doñana National Park (Spain) and surrounding area. Clin Microbiol Infect 15:224–226CrossRefPubMedGoogle Scholar
  18. May K, Strube C (2014) Prevalence of Rickettsiales (Anaplasma phagocytophilum and Rickettsia spp.) in hard ticks (Ixodes ricinus) in the city of Hamburg, Germany. Parasitol Res 113:2169–2175CrossRefPubMedGoogle Scholar
  19. Milhano N, Lopes de Carvalho I, Alves AS, Arroube S, Soares J, Rodriguez P, Carolino M, Núncio MS, Piesman J, de Sousa R (2010) Coinfections of Rickettsia slovaca and Rickettsia helvetica with Borrelia lusitaniae in ticks collected in a Safari Park. Portugal. Ticks Tick-borne Dis 1(4):172–177CrossRefPubMedGoogle Scholar
  20. Oteo JA, Portillo A (2012) Tick-borne rickettsioses in Europe. Ticks Tick Borne Dis 3:270–277CrossRefGoogle Scholar
  21. Oteo JA, Ibarra V, Blanco JR, Martínez de Artola V, Márquez FJ, Portillo A, Raoult D, Anda P (2004) Dermacentor-borne necrosis erythema and lymphadenopathy: clinical and epidemiological features of a new tick-borne disease. Clin Microbiol Infect 10(4):327–331CrossRefPubMedGoogle Scholar
  22. Oteo JA, Portillo A, Santibáñez S, Pérez-Martínez L, Blanco JR, Jiménez S et al (2006) Prevalence of spotted fever group Rickettsia species detected in ticks in La Rioja, Spain. Ann N Y Acad Sci 1078:320–323CrossRefPubMedGoogle Scholar
  23. Otranto D, Dantas-Torres F, Giannelli A, Latrofa MS, Cascio A, Cazzin S et al (2014) Ticks infesting humans in Italy and associated pathogens. Parasit Vectors 14:328CrossRefGoogle Scholar
  24. Palomar AM, Portillo A, Mazuelas D, Roncero L, Arizaga J, Crespo A et al (2016) Molecular analysis of Crimean-Congo hemorrhagic fever virus and Rickettsia in Hyalomma marginatum ticks removed from patients (Spain) and birds (Spain and Morocco), 2009–2015. Ticks Tick Borne Dis 7:983–987CrossRefPubMedGoogle Scholar
  25. Parola P (2011) Rickettsia felis: from a rare disease in the USA to a common cause of fever in sub-Saharan Africa. Clin Microbiol Infect 17:996–1000CrossRefPubMedGoogle Scholar
  26. Parola P, Raoult D (2001) Tick-borne bacterial diseases emerging in Europe. Clin Microbiol Infect 7:80–83CrossRefPubMedGoogle Scholar
  27. Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T et al (2013) Update on tick-borne rickettsioses around the world: a geographic approach. Clin Microbiol Rev 26:657–702CrossRefPubMedPubMedCentralGoogle Scholar
  28. Paules CI, Marston HD, Bloom ME, Fauci AS (2018) Tickborne diseases—confronting a growing threat. N Engl J Med 379:701–703CrossRefPubMedGoogle Scholar
  29. Pérez-Eid C (2007) Les tiques. Identification, biologie, importance médicale et vétérinaire. Lavoisier TEC & DOC, ParisGoogle Scholar
  30. Petney TN, Pfäfffie MP, Skuballa JD (2012) An annotated checklist of the ticks (Acari: Ixodida) of Germany. Syst Appl Acarol 17:115–170Google Scholar
  31. Portillo A, Ibarra V, Santibáñez S, Pérez-Martinez L, Blanco JR, Oteo JA (2009) Genetic characterisation of ompA, ompB and gltA genes from Candidatus Rickettsia rioja. Clin Microbiol Infect 15:307–308CrossRefPubMedGoogle Scholar
  32. Portillo A, Santibáñez S, García-Álvarez L, Palomar AM, Oteo JA (2015) Rickettsioses in Europe. Microbes Infect 17:834–838CrossRefPubMedGoogle Scholar
  33. R Core Team (2018) R: A Language and Environment for Statistical Computing. https://www.R-project.org/
  34. Regnery RL, Spruill CL, Plikaytis BD (1991) Genotypic identification of Rickettsiae and estimation of intraspecies sequence divergence for portions of 2 rickettsial genes. J Bacteriol 173:1576–1589CrossRefPubMedPubMedCentralGoogle Scholar
  35. Remesar S, Díaz P, Venzal JM, Pérez-Creo A, Prieto A, Estrada-Peña A et al (2019) Tick species diversity and population dynamics of Ixodes ricinus in Galicia (north-western Spain). Ticks Tick Borne Dis 10:132–137CrossRefPubMedGoogle Scholar
  36. Reye AL, Stegniy V, Mishaeva NP, Velhin S, Hubschen JM, Ignatyev G et al (2013) Prevalence of tick-borne pathogens in Ixodes ricinus and Dermacentor reticulatus ticks from different geographical locations in Belarus. PLoS ONE 8:e54476CrossRefPubMedPubMedCentralGoogle Scholar
  37. Rizzoli A, Silaghi C, Obiegala A, Rudolf I, Hubálek Z, Földvári G et al (2014) Ixodes ricinus and its transmitted pathogens in urban and peri-urban areas in Europe: new hazards and relevance for public health. Front Public Health 1:251Google Scholar
  38. Roux V, Fournier PE, 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 34:2058–2065PubMedPubMedCentralGoogle Scholar
  39. Santibáñez S, Portillo A, Santibáñez P, Palomar AM, Oteo JA (2013) Usefulness of rickettsial PCR assays for the molecular diagnosis of human rickettsioses. Enferm Infecc Microbiol Clin 31:283–288CrossRefPubMedGoogle Scholar
  40. Santibáñez S, Portillo A, Palomar AM, Santibáñez P, Oteo JA (2017) Rickettsia spp. detected in Dermacentor marginatus from DEBONEL/TIBOLA/SENLAT patients. ESCCAR-ASR Joint meeting. International congress on Rickettsiae and other intracellular bacteria. Marseille, France. P1-20Google Scholar
  41. Selmi M, Ballardini M, Salvato L, Ricci E (2017) Rickettsia spp. in Dermacentor marginatus ticks: analysis of the host-vector-pathogen interactions in a northern Mediterranean area. Exp Appl Acarol 72:79–91CrossRefPubMedGoogle Scholar
  42. Silaghi C, Hamel D, Thiel C, Pfister K, Pfeffer M (2011) Spotted Fever Group Rickettsiae in ticks, Germany. Emerg Infect Dis 17:890–892CrossRefPubMedPubMedCentralGoogle Scholar
  43. 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(2):189–197CrossRefPubMedGoogle Scholar
  44. Spitalska E, Boldis V, Derdakova M, Selyemova D, Taragel’ova VR (2014) Rickettsial infection in Ixodes ricinus ticks in urban and natural habitats of Slovakia. Ticks Tick Borne Dis 5:161–165CrossRefPubMedGoogle Scholar
  45. Stanczak J, Biernat B, Racewicz M, Zalewska M, Matyjasek A (2018) Prevalence of different Rickettsia spp. in Ixodes ricinus and Dermacentor reticulatus ticks (Acari: Ixodidae) in north-eastern Poland. Ticks Tick Borne Dis 9:427–434CrossRefPubMedGoogle Scholar
  46. Svehlova A, Berthova L, Sallay B, Boldis V, Sparagano OAE, Spitalska E (2014) Sympatric occurrence of Ixodes ricinus, Dermacentor reticulatus and Haemaphysalis concinna ticks and Rickettsia and Babesia species in Slovakia. Ticks Tick Borne Dis 5:600–605CrossRefPubMedGoogle Scholar
  47. Tijsse-Klasen E, Jameson LJ, Fonville M, Leach S, Sprong H, Medlock JM (2011) First detection of spotted fever group rickettsiae in Ixodes ricinus and Dermacentor reticulatus ticks in the UK. Epidemiol Infect 139:524–529CrossRefPubMedGoogle Scholar
  48. Toledo A, Olmeda AS, Escudero R, Jado I, Valcárcel F, Casado-Nistal MA et al (2009) Tick-borne zoonotic bacteria in tickscollected from Central Spain. Am J Trop Med Hyg 81:67–74CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Susana Remesar
    • 1
  • Pablo Díaz
    • 1
    Email author
  • Aránzazu Portillo
    • 2
  • Sonia Santibáñez
    • 2
  • Alberto Prieto
    • 1
  • José M. Díaz-Cao
    • 1
  • Ceferino M. López
    • 1
  • Rosario Panadero
    • 1
  • Gonzalo Fernández
    • 1
  • Pablo Díez-Baños
    • 1
  • José A. Oteo
    • 2
  • Patrocinio Morrondo
    • 1
  1. 1.Departamento de Patología Animal (Grupo INVESAGA), Facultad de VeterinariaUniversidade de Santiago de CompostelaLugoSpain
  2. 2.Centro de Rickettsiosis y Enfermedades Transmitidas por Artrópodos Vectores (CRETAV), Departamento de Enfermedades Infecciosas, Hospital U. San Pedro-CIBIRLogroñoSpain

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