Skip to main content

Advertisement

Log in

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

  • Short Communication
  • Published:
Parasitology Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

References

  • 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]

  • 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 7:166–171

    Article  PubMed  Google Scholar 

  • 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 10:155

    Article  PubMed  PubMed Central  Google Scholar 

  • Arthur DR (1963) British ticks. Butterworths, London

    Google Scholar 

  • Balashov YS (1997) Distribution of ixodid ticks (Acarina, Ixodidae) over landscapes within their ranges. Entomol Rev 77:625–637 [In Russian]

    Google Scholar 

  • 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 87:32–48

    Article  CAS  PubMed  Google Scholar 

  • 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 10:1040–1055

    Article  CAS  PubMed  Google Scholar 

  • 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)

  • 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):301–317

  • 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 93:307–317

    Article  CAS  PubMed  Google Scholar 

  • Eichler W (1968) Kritische Liste mitteleuropäischer Zeckenarten. Angew Parasitol 9:88–97 [In German]

  • Fedorov VG (1968) Ixodoidea ticks on humans in western Siberia. Med Parazitol 37:615–616 (NAMRU-3 translation 390)

  • Feider Z (1965) Fauna of the Peoples Republic of Romania. Suprafamily Ixodoidea. Ticks. Ed. Acad. Rep. Pop. Romane, Bucharest [In Romanian]

  • Filippova NA (1977) Ixodid ticks (Ixodinae). Fauna USSR New Series, 4:1–316 [In Russian]

  • Frangoulidis D, Meyer H, Kahlhofer C, Splettstoesser WD (2012) ‘Real-time’ PCR-based detection of Coxiella burnetii using conventional techniques. FEMS Immunol Med Microbiol 64:134–136

    Article  CAS  PubMed  Google Scholar 

  • Fujita H, Watanabe Y (1994) Ehrlichial organisms isolated from Ixodes ovatus ticks and field rodents in Japan. Ann Rep Oharahosp 37:13–17

    Google Scholar 

  • Georgescu M (1968) Contributions to the study of ixodids from Romanian caves. Lucr Inst Speol Emil Racovita 7:187–195 [In Romanian]

    Google Scholar 

  • 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]

    Article  CAS  PubMed  Google Scholar 

  • Hillyard PD (1996) Ticks of north-west Europe. Linnaean Society, London

    Google Scholar 

  • Inokuma H, Parola P, Raoult D, Brouqui P (2001b) Molecular survey of Ehrlichia infection in ticks from animals in Yamaguchi Prefecture, Japan. Vet Parasitol 99:335–339

    Article  CAS  PubMed  Google Scholar 

  • 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 63:815–817

    Article  CAS  PubMed  Google Scholar 

  • Karbowiak G, Wieczorek M, Borowsk Z, Wita I (2007) The new locality of Ixodes apronophorus Schulze, 1924 in Biebrza National Park, Poland. Wiad Parazytol 53:343–345

    PubMed  Google Scholar 

  • Kharitonova NN, Leonov YA (1986) Omsk hemorrhagic fever: ecology of the agent and epizootiology. Am J Trop Med Hyg 35:1318

    Article  Google Scholar 

  • 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 51:1958–1961

    Article  PubMed  PubMed Central  Google Scholar 

  • Lvov DK (1988) Omsk hemorrhagic fever. In: Monath, T.P. The arboviruses: epidemiology and ecology. CRC Press, Inc., Boca Raton, FL 3:205–216

  • 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 84:478–484

    Article  CAS  PubMed  Google Scholar 

  • 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 13:338–341

    Article  CAS  PubMed  Google Scholar 

  • 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):183–206

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Negrobov VP, Borodin VS (1964) Einige seltene Zeckenfunde im mittleren Teil der DDR. Angew Parasitol 5:107–111 [In German]

    Google Scholar 

  • Newson RM, Holmes RG (1968) Some ectoparasites of the coypu (Myocastor coypus) in eastern England. J Anim Ecol 37:471–481

    Article  Google Scholar 

  • Nosek J, Sixl W (1972) Central-European ticks (Ixodoidea): key for determination. Mitt Abt Zool Landesmus Joanneum 1:61–92

    Google Scholar 

  • 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 6:103–113

    Article  PubMed  Google Scholar 

  • Petney TN, Pfäffle MP, Skuballa JD (2012) An annotated checklist of the ticks (Acari:Ixodida) of Germany. Syst Appl Acarol 17:115–170

    Google Scholar 

  • Randolph SE (1995) Quantifying parameters in the transmission of Babesia microti by the tick Ixodes trianguliceps amongst voles (Myodes glareolus). Parasitology 110:287–295

    Article  PubMed  Google Scholar 

  • 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 27:136–145

    Article  CAS  PubMed  Google Scholar 

  • Siuda K (1993) Kleszcze (Acari: Ixodida) Polski. II.Systematyka iroz mieszczenie. Monografie Parazytologiczne vol. 12. Polish Parasitological Society,Warsaw [In Polish]

  • Siuda K, Majszyk A, Nowak M (2006) Ticks (Acari: Ixodida) parsitizing birds (Aves) in Poland. Biol Lett 43:147–151

    Google Scholar 

  • Siuda K, Szczesniak-Zarzycka Dulkiewicz J, Derylo A (1982) Data on knowledge of the tick fauna (Ixodides) of the mammals in Poland. Wiad Parazytol 28:63–67

    Google Scholar 

  • 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 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 41:5492–5499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):368–374

    Article  Google Scholar 

Download references

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

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

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lidia Chitimia-Dobler.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Section Editor: Domenico Otranto

Electronic supplementary material

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)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Andersson, M.O., Radbea, G., Frangoulidis, D. et al. New records and host associations of the tick Ixodes apronophorus and the first detection of Ehrlichia sp. HF in Romania. Parasitol Res 117, 1285–1289 (2018). https://doi.org/10.1007/s00436-018-5800-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-018-5800-3

Keywords

Navigation