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Parasitology Research

, Volume 117, Issue 4, pp 1285–1289 | Cite as

New records and host associations of the tick Ixodes apronophorus and the first detection of Ehrlichia sp. HF in Romania

  • Martin O. Andersson
  • Gabriel Radbea
  • Dimitrios Frangoulidis
  • Herbert Tomaso
  • Franz Rubel
  • Santiago Nava
  • Lidia Chitimia-Dobler
Short Communication

Abstract

Ixodes (Ixodes) apronophorus is a neglected tick species and its geographical distribution, host associations, and role as a disease vector are not well known. We collected I. apronophorus from several locations in Romania. Morphological identification of ticks was confirmed by analysis of 16S rDNA and 12S rDNA gene sequences. We report new host associations of I. apronophorus, which was collected from dogs, foxes, and a hare—all new hosts for this tick species in Romania. Furthermore, we report for the first time occurrence of Ehrlichia sp. HF in I. apronophorus. Ehrlichia sp. HF was identified by sequencing a part of the 16S rDNA gene and was found in 16% (3/19) of the tested ticks. Ehrlichia sp. HF has not been previously reported in Eastern Europe and seems to have a much larger geographic distribution than previously known. Currently, it is unknown whether I. apronophorus is a competent vector for Ehrlichia sp. HF, or if the findings in this study represent infection in the hosts, namely dogs and fox.

Keywords

Ixodes apronophorus Ehrlichia sp. HF Dogs Romania 

Notes

Acknowledgements

We thank Professor Martin Pfeffer for valuable comments on the manuscript and Byrgit Hofmann for excellent technical assistance. We thank Michael Levin for the help in language.

Funding information

This work was funded by the German Center of Infection Research (DZIF) (LCD) and by the Royal Swedish Academy of Agriculture and Forestry (MOA).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

436_2018_5800_MOESM1_ESM.png (1.5 mb)
ESM 1 Supplementary map Ixodes apronophorus ditribution in Romania: red dots – new finding, yellow dot – Feider (1965); blue dot – Mihalca et al. (2012) and Ehrlichia sp. HF locations in Romania represented by white stars (PNG 1525 kb)

References

  1. Aeschlimann A, Büttiker W, Wiehl PA, Eichenberger G, Immler R, Weiss N (1970) Présence d’Ixodes trianguliceps (Birula, 1895) et d’Ixodes apronophorus (Schulze, 1924) en Suisse (Ixodoidea, Ixodidae). Rev Suisse Zool 77:527–535 [In French]Google Scholar
  2. Al-Deeb MA, Frangoulidis D, Walter MC, Kömpf D, Fischer SF, Petney T, Muzaffar SB (2016) Coxiella-like endosymbiont in argasid ticks (Ornithodoros muesebecki) from a Socotra Cormorant colony in Umm Al Quwain, United Arab Emirates. Ticks Tick Borne Dis 7:166–171CrossRefPubMedGoogle Scholar
  3. Andersson MO, Tolf C, Tamba P, Stefanache M, Waldenström J, Dobler G, Chitimia-Dobler L (2017) Canine tick-borne diseases in pet dogs from Romania. Parasit Vectors 10:155CrossRefPubMedPubMedCentralGoogle Scholar
  4. Arthur DR (1963) British ticks. Butterworths, LondonGoogle Scholar
  5. Balashov YS (1997) Distribution of ixodid ticks (Acarina, Ixodidae) over landscapes within their ranges. Entomol Rev 77:625–637 [In Russian]Google Scholar
  6. Beati L, Keirans JE (2001) Analysis of the systematic relationships among ticks of the genera Rhipicephalus and Boophilus (Acari: Ixodidae) based on mitochondrial 12S ribosomal DNA gene sequences and morphological characters. J Parasitol 87:32–48CrossRefPubMedGoogle Scholar
  7. Charrel RN, Attoui H, Butenko AM, Clegg JC, Deubel V, Frolova TV, Gould EA, Gritsun TS, Heinz FX, Labuda M, Lashkevich VA, Loktev V, Lundkvist A, Lvov DV, Mandl CW, Niedrig M, Papa A, Petrov VS, Plyusnin A, Randolph S, Süss J, Zlobin VI, de Lamballerie X (2004) Tick-borne virus diseases of human interest in Europe. Clin Microbiol Infect 10:1040–1055CrossRefPubMedGoogle Scholar
  8. Chitimia-Dobler L, Rieß R, Kahl O, Wölfel S, Dobler G, Nava N, Estrada-Peña A (2017) Ixodes inopinatus—occurring also outside the Mediterranean region. Ticks Tick Borne Dis (in press)Google Scholar
  9. Coipan EC, Vladimirescu AF, Ciolpan O, Teodorescu I (2011) Tick species (Acari: Ixodoidea) distribution, seasonality and host associations in Romania. Travaux du Muséum National d’Histoire Naturelle Grigore Antipa (2):301–317Google Scholar
  10. Criado-Fornelio A, Martinez-Marcos A, Buling-Sarana A, Barba-Carretero JC (2003) Presence of Mycoplasma haemofelis, Mycoplasma haemominutum and piroplasmids in cats from southern Europe: a molecular study. Vet Microbiol 93:307–317CrossRefPubMedGoogle Scholar
  11. Eichler W (1968) Kritische Liste mitteleuropäischer Zeckenarten. Angew Parasitol 9:88–97 [In German]Google Scholar
  12. Fedorov VG (1968) Ixodoidea ticks on humans in western Siberia. Med Parazitol 37:615–616 (NAMRU-3 translation 390)Google Scholar
  13. Feider Z (1965) Fauna of the Peoples Republic of Romania. Suprafamily Ixodoidea. Ticks. Ed. Acad. Rep. Pop. Romane, Bucharest [In Romanian]Google Scholar
  14. Filippova NA (1977) Ixodid ticks (Ixodinae). Fauna USSR New Series, 4:1–316 [In Russian]Google Scholar
  15. Frangoulidis D, Meyer H, Kahlhofer C, Splettstoesser WD (2012) ‘Real-time’ PCR-based detection of Coxiella burnetii using conventional techniques. FEMS Immunol Med Microbiol 64:134–136CrossRefPubMedGoogle Scholar
  16. Fujita H, Watanabe Y (1994) Ehrlichial organisms isolated from Ixodes ovatus ticks and field rodents in Japan. Ann Rep Oharahosp 37:13–17Google Scholar
  17. Georgescu M (1968) Contributions to the study of ixodids from Romanian caves. Lucr Inst Speol Emil Racovita 7:187–195 [In Romanian]Google Scholar
  18. Gilot B, Moncada E, Pautou G (1976) Presence en France d’Ixodes apronophorus (Schulze, 1924). Ixodoidea-Ixodidae. Ann Parasitol Hum Comp 51:601–603 [In French]CrossRefPubMedGoogle Scholar
  19. Hillyard PD (1996) Ticks of north-west Europe. Linnaean Society, LondonGoogle Scholar
  20. Inokuma H, Parola P, Raoult D, Brouqui P (2001b) Molecular survey of Ehrlichia infection in ticks from animals in Yamaguchi Prefecture, Japan. Vet Parasitol 99:335–339CrossRefPubMedGoogle Scholar
  21. Inokuma H, Ohno K, Onishi T, Raoult D, Brouqui P (2001a) Detection of ehrlichial infection by PCR in dogs from Yamaguchi and Okinawa Prefectures, Japan. J Vet Med Sci 63:815–817CrossRefPubMedGoogle Scholar
  22. Karbowiak G, Wieczorek M, Borowsk Z, Wita I (2007) The new locality of Ixodes apronophorus Schulze, 1924 in Biebrza National Park, Poland. Wiad Parazytol 53:343–345PubMedGoogle Scholar
  23. Kharitonova NN, Leonov YA (1986) Omsk hemorrhagic fever: ecology of the agent and epizootiology. Am J Trop Med Hyg 35:1318CrossRefGoogle Scholar
  24. Krücken J, Schreiber C, Maaz D, Kohn M, Demeler J, Beck S, Schein E, Richter D, Matuschka F, Pachnicke S, Krieger K, Kohn B, von Samson-Himmelstjerna G (2013) A novel high-resolution melt PCR assay discriminates Anaplasma phagocytophilum and “ Candidatus Neoehrlichia mikurensis”. J Clin Microbiol 51:1958–1961CrossRefPubMedPubMedCentralGoogle Scholar
  25. Lvov DK (1988) Omsk hemorrhagic fever. In: Monath, T.P. The arboviruses: epidemiology and ecology. CRC Press, Inc., Boca Raton, FL 3:205–216Google Scholar
  26. Mangold AJ, Bargues MD, Mas-Coma S (1998) Mitochondrial 16S rRNA sequences and phylogenetic relationships of Rhipicephalus and other tick genera among Metastriata (Acari: Ixodidae). Parasitol Res 84:478–484CrossRefPubMedGoogle Scholar
  27. Marumoto K, Joncour G, Lamanda P, Inokuma H, Brouqui P (2007) Detection of Anaplasma phagocytophilum and Ehrlichia sp. HF strains in Ixodes ricinus in Brittany, France. Clin Microbiol Infect 13:338–341CrossRefPubMedGoogle Scholar
  28. Mihalca AD, Dumitrache MO, Magdaş C, Gherman CM, Domşa C, Mircean V, Ghira IV, Pocora V, Ionescu DT, Barabási S, Cozma V, Sándor AD (2012) Synopsis of the hard ticks (Acari: Ixodidae) of Romania with update on host associations and geographical distribution. Exp Appl Acarol 58(2):183–206CrossRefPubMedGoogle Scholar
  29. Mironescu I (1966) A new Ixodid for the fauna of our country, parasitic on birds. An St Univ Al I Cuza Iasi Biol 12:61–65 [In Romanian]Google Scholar
  30. Negrobov VP, Borodin VS (1964) Einige seltene Zeckenfunde im mittleren Teil der DDR. Angew Parasitol 5:107–111 [In German]Google Scholar
  31. Newson RM, Holmes RG (1968) Some ectoparasites of the coypu (Myocastor coypus) in eastern England. J Anim Ecol 37:471–481CrossRefGoogle Scholar
  32. Nosek J, Sixl W (1972) Central-European ticks (Ixodoidea): key for determination. Mitt Abt Zool Landesmus Joanneum 1:61–92Google Scholar
  33. Ornstein K, Barbour AG (2006) A reverse transcriptase–polymerase chain reaction assay of Borrelia burgdorferi 16S rRNA for highly sensitive quantification of pathogen load in a vector. Vector-Borne Zoonotic Dis 6:103–113CrossRefPubMedGoogle Scholar
  34. Petney TN, Pfäffle MP, Skuballa JD (2012) An annotated checklist of the ticks (Acari:Ixodida) of Germany. Syst Appl Acarol 17:115–170Google Scholar
  35. Randolph SE (1995) Quantifying parameters in the transmission of Babesia microti by the tick Ixodes trianguliceps amongst voles (Myodes glareolus). Parasitology 110:287–295CrossRefPubMedGoogle Scholar
  36. Schwaiger M, Cassinotti P (2003) Development of a quantitative real-time RT-PCR assay with internal control for the laboratory detection of tick borne encephalitis virus (TBEV) RNA. J Clin Virol 27:136–145CrossRefPubMedGoogle Scholar
  37. Siuda K (1993) Kleszcze (Acari: Ixodida) Polski. II.Systematyka iroz mieszczenie. Monografie Parazytologiczne vol. 12. Polish Parasitological Society,Warsaw [In Polish]Google Scholar
  38. Siuda K, Majszyk A, Nowak M (2006) Ticks (Acari: Ixodida) parsitizing birds (Aves) in Poland. Biol Lett 43:147–151Google Scholar
  39. Siuda K, Szczesniak-Zarzycka Dulkiewicz J, Derylo A (1982) Data on knowledge of the tick fauna (Ixodides) of the mammals in Poland. Wiad Parazytol 28:63–67Google Scholar
  40. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likely-hood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  41. Versage JL, Severin DDM, Chu MC, Petersen JM (2003) Development of a multitarget real-time TaqMan PCR assay for enhanced detection of Francisella tularensis in complex specimens. J Clin Microbiol 41:5492–5499CrossRefPubMedPubMedCentralGoogle Scholar
  42. Wölfel R, Essbauer S, Dobler G (2008) Diagnostics of tick-borne rickettsioses in Germany: a modern concept for a neglected disease. Int J Med Microbiol 298(S1):368–374CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Martin O. Andersson
    • 1
  • Gabriel Radbea
    • 2
  • Dimitrios Frangoulidis
    • 3
    • 4
  • Herbert Tomaso
    • 5
  • Franz Rubel
    • 6
  • Santiago Nava
    • 7
  • Lidia Chitimia-Dobler
    • 3
    • 4
    • 8
  1. 1.Center for Ecology and Evolution in Microbial Model Systems (EEMiS)Linnaeus UniversityKalmarSweden
  2. 2.Sal-Vet Private Veterinary ClinicsTimisoaraRomania
  3. 3.Bundeswehr Institute of MicrobiologyMunichGermany
  4. 4.German Center of Infection Research (DZIF) Partner MunichMunichGermany
  5. 5.Friedrich-Loeffler-Institut, Institute of Bacterial Infections and ZoonosesJenaGermany
  6. 6.Institute for Veterinary Public HealthUniversity of Veterinary Medicine ViennaViennaAustria
  7. 7.Estación Experimental Agropecuaria Rafaela, and Consejo Nacional de Investigaciones Científicas y TécnicasInstituto Nacional de Tecnología AgropecuariaBuenos AiresArgentina
  8. 8.Institute for Diagnosis and Animal HealthBucharestRomania

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