First Molecular Identification of Zoonotic Babesia odocoilei in Ticks from Romania
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sample Collection
2.2. DNA Extraction
2.3. Molecular Analysis of Ticks for Babesia spp.
2.4. Conventional PCR
3. Results
3.1. Tick Infestation of Wild Boars
3.2. Molecular Detection of Babesia spp. in Ticks
3.3. Sequencing Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Heyman, P.; Cochez, C.; Hofhuis, A.; van der Giessen, J.; Sprong, H.; Porter, S.R.; Losson, B.; Saegerman, C.; Donoso Mantke, O.; Niedrig, M.; et al. A clear and present danger: Tick-borne diseases in Europe. Expert Rev. Anti. Ther. 2010, 8, 33–50. [Google Scholar] [CrossRef] [PubMed]
- Randolph, S.E. Evidence that climate change has caused “emergence” of tickborne diseases in Europe? Int. J. Med. Microbiol. 2004, 293, 5–15. [Google Scholar] [PubMed]
- Kjemtrup, A.; Conrad, P.A. Human babesiosis: An emerging tick-borne disease. Int. J. Parasitol. 2000, 30, 1323–1337. [Google Scholar] [CrossRef]
- Schnittger, L.; Rodriguez, A.E.; Florin-Christensen, M.; Morrison, D.A. Babesia: A world emerging. Infect. Genet. Evol. 2012, 12, 1788–1809. [Google Scholar] [CrossRef]
- Yabsley, M.J.; Shock, B.C. Natural history of Zoonotic Babesia: Role of wildlife reservoirs. Int. J. Parasitol. Parasites Wildl. 2013, 2, 18–31. [Google Scholar] [CrossRef]
- Harvell, D.; Altizer, S.; Cattadori, I.M.; Harrington, L.; Weil, E. Climate change and wildlife diseases: When does the host matter the most? Ecology 2009, 4, 912–920. [Google Scholar] [CrossRef]
- Medlock, J.M.; Hansford, K.M.; Bormane, A.; Derdakova, M.; Estrada-Pena, A.; George, J.C.; Golovljova, I.; Jaenson, T.G.T.; Jensen, J.K.; Kazimirova, M.; et al. Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasit. Vectors 2013, 6, 1. [Google Scholar] [CrossRef]
- Fanelli, A. A historical review of Babesia spp. associated with deer in Europe: Babesia divergens/Babesia divergens-like, Babesia capreoli, Babesia venatorum, Babesia cf. odocoilei. Vet Parasitol. 2021, 294, 109433. [Google Scholar] [CrossRef] [PubMed]
- Babes, V. Sur l’hemoglobinurie bacterienne du boeuf. C.R. Hebd. Seances Acad. Sci. Ser. D Sci. Nat. 1888, 107, 692–694. [Google Scholar]
- Levine, N.D. Progress in taxonomy of the Apicomplexan protozoa. J. Protozool. 1998, 35, 518–520. [Google Scholar] [CrossRef]
- Homer, M.J.; Aguilar-Delfin, I.; Telford, S.R.; Krause, P.J.; Persing, D.H. Babesiosis. Clin. Microbiol. Rev. 2000, 13, 451–469. [Google Scholar] [CrossRef]
- Hunfeld, K.P.; Hildebrandt, A.; Gray, J.S. Babesiosis: Recent insights into an ancient disease. Int. J. Parasitol. 2008, 38, 1219–1237. [Google Scholar] [CrossRef] [PubMed]
- Krause, P.J. Human babesiosis. Int. J. Parasitol. 2019, 49, 165–174. [Google Scholar] [CrossRef]
- Gunders, A.E. Piroplasmal sporozoites in the argasid Ornithodoros erraticus (Lucas). Experientia 1977, 33, 892–893. [Google Scholar] [CrossRef] [PubMed]
- Gray, J.S.; Estrada-Pena, A.; Zintl, A. Vectors of babesiosis. Annu. Rev. Entomol. 2019, 64, 149–165. [Google Scholar] [CrossRef]
- Øines, Ø.; Radzijevskaja, J.; Paulauskas, A.; Rosef, O. Prevalence and diversity of Babesia spp. in questing Ixodes ricinus ticks from Norway. Parasit. Vectors 2012, 5, 156. [Google Scholar] [CrossRef]
- Hildebrandt, A.; Gray, J.S.; Hunfeld, K.P. Human Babesiosis in Europe: What clinicians need to know. Infection 2013, 41, 1057–1072. [Google Scholar] [CrossRef] [PubMed]
- Stuen, S.; Pettersen, K.S.; Granquist, E.G.; Bergstrom, K.; Bown, K.J.; Birtles, R.J. Anaplasma phagocytophilum variants in sympatric red deer (Cervus elaphus) and sheep in southern Norway. Ticks Tick-Borne Dis. 2013, 4, 197–201. [Google Scholar] [CrossRef]
- Hornok, S.; Szekeres, S.; Horváth, G.; Takács, N.; Bekő, K.; Kontschán, J.; Gyuranecz, M.; Tóth, B.; Sándor, A.D.; Juhász, A.; et al. Diversity of tick species and associated pathogens on peri-urban wild boars—First report of the zoonotic Babesia cf. crassa from Hungary. Ticks Tick-Borne Dis. 2022, 13, 101936. [Google Scholar] [CrossRef]
- Emerson, H.R.; Wright, W.T. The isolation of a Babesia in white-tailed deer. Bull. Wildl. Dis. Assoc. 1968, 4, 142–143. [Google Scholar] [CrossRef]
- Emerson, H.R.; Wright, W.T. Correction. J. Wildl. Dis. 1970, 6, 519. [Google Scholar] [CrossRef]
- Holman, P.J.; Madeley, J.; Craig, T.M.; Allsopp, B.A.; Allsopp, M.T.; Petrini, K.R.; Waghela, S.D.; Wagner, G.G. Antigenic, phenotypic and molecular characterization confirms Babesia odocoilei isolated from three cervids. J. Wildl. Dis. 2000, 36, 518–530. [Google Scholar] [CrossRef]
- Skrabalo, Z.; Deanovic, Z. Piroplasmosis in man: Report on a case. Doc. Med. Geogr. Trop. 1957, 9, 11–16. [Google Scholar] [PubMed]
- Mørch, K.; Holmaas, G.; Frolander, P.S.; Kristoffersen, E.K. Severe human Babesia divergens infection in Norway. Int. J. Infect. Dis. 2014, 33, 37–38. [Google Scholar] [CrossRef]
- Public Health Authority of the Slovak Republic. Available online: http://www.uvzsr.sk/en/ (accessed on 14 February 2025).
- Herwaldt, B.L.; Linden, J.V.; Bosserman, E.; Young, C.; Olkowska, D.; Wilson, M. Transfusion-associated babesiosis in the United States: A description of cases. Ann. Intern. Med. 2011, 155, 509–519. [Google Scholar] [CrossRef] [PubMed]
- Linden, J.V.; Prusinski, M.A.; Crowder, L.A.; Tonnetti, L.; Stramer, S.L.; Kessler, D.A.; White, J.; Shaz, B.; Olkowska, D. Transfusion-transmitted and community-acquired babesiosis in New York, 2004 to 2015. Transfusion 2018, 58, 660–668. [Google Scholar] [CrossRef]
- Karshima, S.N.; Karshima, M.N.; Ahmed, M.I. Global meta-analysis on Babesia infections in human population: Prevalence, distribution and species diversity. Pathog. Global Health 2022, 116, 220–235. [Google Scholar] [CrossRef] [PubMed]
- Chang, D.; Hossain, M.; Hossain, M.A. Severe babesiosis masquerading as thrombotic thrombocytopenic purpura: A case report. Cureus 2019, 11, e4459. [Google Scholar] [CrossRef]
- Krause, P.J.; Gewurz, B.E.; Hill, D.; Marty, F.M.; Vannier, E.; Foppa, I.M.; Furman, R.R.; Neuhaus, E.; Skowron, G.; Gupta, S.; et al. Persistent and relapsing babesiosis in immunocompromised patients. Clin. Infect. Dis. 2008, 46, 370–376. [Google Scholar] [CrossRef]
- González, L.M.; Castro, E.; Lobo, C.A.; Richart, A.; Ramiro, R.; González-Camacho, F.; Luque, D.; Velasco, A.C.; Montero, E. First report of Babesia divergens infection in an HIV patient. Int. J. Infect. Dis. 2015, 33, 202–204. [Google Scholar] [CrossRef]
- Estrada-Peña, A.; Mihalca, A.; Petney, T. Ticks of Europe and North Africa: A Guide to Species Identification; Springer: Cham, Switzerland, 2017. [Google Scholar]
- MapChart. Available online: https://www.mapchart.net/romania.html (accessed on 18 February 2025).
- Stańczak, J.; Cieniuch, S.; Lass, A.; Biernat, B.; Racewicz, M. Detection and quantification of Anaplasma phagocytophilum and Babesia spp. in Ixodes ricinus ticks from urban and rural environment, northern Poland, by real-time polymerase chain reaction. Exp. Appl. Acarol. 2015, 66, 63–81. [Google Scholar] [CrossRef] [PubMed]
- Giubega, S.; Ilie, M.S.; Morariu, S.; Imre, M.; Dreghiciu, C.; Rugea, T.; Ivascu, S.; Simion, G.; Dărăbuș, G. Molecular Investigations of Babesia caballi from Clinically Healthy Horses in Southwestern Romania. Vet. Sci. 2024, 11, 600. [Google Scholar] [CrossRef] [PubMed]
- BlastBasic Local Alignment Search Tool, National Center for Biotechnology Information. Available online: https://blast.ncbi.nlm.nih.gov (accessed on 14 March 2025).
- Wikipedia. Available online: https://ro.wikipedia.org/wiki/Jude%C8%9Bul_Timi%C8%99 (accessed on 7 May 2025).
- Zintl, A.; Finnerty, E.J.; Murphy, T.M.; de Waal, T.; Gray, J.S. Babesias of red deer (Cervus elaphus) in Ireland. Vet. Res. 2011, 42, 7. [Google Scholar] [CrossRef] [PubMed]
- Wiegmann, L.; Silaghi, C.; Obiegala, A.; Karnath, C.; Langer, S.; Ternes, K.; Kämmerling, J.; Osmann, C.; Pfeffer, M. Occurrence of Babesia species in captive reindeer (Rangifer tarandus) in Germany. Vet. Parasitol. 2015, 211, 16–22. [Google Scholar] [CrossRef]
- Hamšíková, Z.; Kazimírová, M.; Haruštiaková, D.; Mahríková, L.; Slovák, M.; Berthová, L.; Kocianová, E.; Schnittger, L. Babesia spp. in ticks and wildlife in different habitat types of Slovakia. Parasit. Vectors 2016, 9, 292. [Google Scholar] [CrossRef]
- Duh, D.; Petrovec, M.; Avsic-Zupanc, T. Diversity of Babesia infecting European sheep ticks (Ixodes ricinus). J. Clin. Microbiol. 2001, 39, 3395–3397. [Google Scholar] [CrossRef]
- Gandy, S.; Medlock, J.; Cull, B.; Smith, R.; Gibney, Z.; Sewgobind, S.; Parekh, I.; Harding, S.; Johnson, N.; Hansford, K. Detection of Babesia species in questing Ixodes ricinus ticks in England and Wales. Ticks Tick-Borne Dis. 2024, 15, 102291. [Google Scholar] [CrossRef]
- Puraite, I.; Rosef, O.; Radzijevskaja, J.; Lipatova, I.; Paulauskas, A. The first detection of species of Babesia Starcovici, 1893 in moose, Alces alces (Linnaeus), in Norway. Folia Parasitol. 2016, 63, 1–5. [Google Scholar] [CrossRef]
- Schoelkopf, L.; Hutchinson, C.E.; Bendele, K.G.; Goff, W.L.; Willette, M.; Rasmussen, J.M.; Holman, P.J. New ruminant hosts and wider geographic range identified for Babesia odocoilei (Emerson and Wright 1970). J. Wildl. Dis. 2005, 41, 683–690. [Google Scholar] [CrossRef]
- Bartlett, S.L.; Abou-Madi, N.; Messick, J.B.; Birkenheuer, A. Diagnosis and treatment of Babesia odocoilei in captive reindeer (Rangifer tarandus tarandus) and recognition of three novel host species. J. Zoo Wildl. Med. 2009, 40, 152–159. [Google Scholar] [CrossRef]
- Smith, R.P., Jr.; Elias, S.P.; Borelli, T.J.; Missaghi, B.; York, B.J.; Kessler, R.A.; Lubelczyk, C.B.; Lacombe, E.H.; Hayes, C.M.; Coulter, M.S.; et al. Human babesiosis, Maine, USA, 1995–2011. Emerg. Infect. Dis. 2014, 20, 1727–1730. [Google Scholar] [CrossRef] [PubMed]
- Steiner, F.E.; Pinger, R.R.; Vann, C.N.; Abley, M.J.; Sullivan, B.; Grindle, N.; Clay, K.; Fuqua, C. Detection of Anaplasma phagocytophilum and Babesia odocoilei DNA in Ixodes scapularis (Acari: Ixodidae) collected in Indiana. J. Med. Entomol. 2006, 43, 437–442. [Google Scholar] [CrossRef]
- Steiner, F.E.; Pinger, R.R.; Vann, C.N.; Grindle, N.; Civetello, D.; Clay, K.; Fuqua, C. Infection and co-infection rates of Anaplasma phagocytophilum variant, Babesia spp., Borrelia burgdorferi, and rickettsial endosymbiont in Ixodes scapularis (Acari: Ixodidae) from sites in Indiana, Maine, Pennsylvania, and Wisconsin. J. Med. Entomol. 2008, 45, 289–297. [Google Scholar] [CrossRef] [PubMed]
- Waldrup, K.A.; Kocan, A.A.; Qureshi, T.; Baggett, D.; Wagner, G.G. Serological prevalence and isolation of Babesia odocoilei among white-tailed deer (Odocoileus virginianus) in Texas and Oklahoma. J. Wild. Dis. 1989, 25, 194–201. [Google Scholar] [CrossRef]
- Andersson, M.O.; Tolf, C.; Tamba, P.; Stefanache, M.; Radbea, G.; Rubel, F.; Waldenström, J.; Dobler, G.; Chițimia-Dobler, L. Babesia, Theileria, and Hepatozoon species in ticks infesting animal hosts in Romania. Parasitol. Res. 2017, 116, 2291–2297. [Google Scholar] [CrossRef]
- Paduraru, O.A.; Buffet, J.P.; Cote, M.; Bonnet, S.; Moutailler, S.; Paduraru, V.; Femenia, F.; Eloit, M.; Savuta, G.; Vayssier-Taussat, M. Zoonotic transmission of pathogens by Ixodes ricinus. Emerg. Infect. Dis. 2012, 18, 2089–2090. [Google Scholar] [CrossRef] [PubMed]
- Ionita, M.; Mitrea, I.L.; Pfister, K.; Hamel, D.; Silaghi, C. Molecular evidence for bacterial and protozoan pathogens in hard ticks from Romania. Vet. Parasitol. 2013, 196, 71–76. [Google Scholar] [CrossRef]
- Drews, S.J.; Kjemtrup, A.M.; Krause, P.J.; Lambert, G.; Leiby, D.A.; Lewin, A.; O’Brien, S.F.; Renaud, C.; Tonnetti, L.; Bloch, E.M. Transfusion-transmitted Babesia spp.: A changing landscape of epidemiology, regulation, and risk mitigation. J. Clin. Microbiol. 2023, 61, e0126822. [Google Scholar] [CrossRef]
Epidemiological Factors | No. of Ticks |
---|---|
County | |
Timiș | 10 |
Caraș Severin | 5 |
Hunedoara | 7 |
Alba | 5 |
Sibiu | 6 |
Mureș | 8 |
Gender | |
Male | 9 |
Female | 32 |
Stage of development | |
Adult | 41/41 |
Larvae | 0/41 |
Nymph | 0/41 |
Species | |
I. ricinus | 8 |
D. reticulatus | 13 |
D. marginatus | 16 |
H. concinna | 1 |
H. erinacei | 2 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Dreghiciu, I.C.; Hoffman, D.; Dumitru, S.; Oprescu, I.; Imre, M.; Florea, T.; Plesko, A.; Iorgoni, V.; Morariu, S.; Dărăbuș, G.; et al. First Molecular Identification of Zoonotic Babesia odocoilei in Ticks from Romania. Microorganisms 2025, 13, 1182. https://doi.org/10.3390/microorganisms13061182
Dreghiciu IC, Hoffman D, Dumitru S, Oprescu I, Imre M, Florea T, Plesko A, Iorgoni V, Morariu S, Dărăbuș G, et al. First Molecular Identification of Zoonotic Babesia odocoilei in Ticks from Romania. Microorganisms. 2025; 13(6):1182. https://doi.org/10.3390/microorganisms13061182
Chicago/Turabian StyleDreghiciu, Ioan Cristian, Diana Hoffman, Simona Dumitru, Ion Oprescu, Mirela Imre, Tiana Florea, Anamaria Plesko, Vlad Iorgoni, Sorin Morariu, Gheorghe Dărăbuș, and et al. 2025. "First Molecular Identification of Zoonotic Babesia odocoilei in Ticks from Romania" Microorganisms 13, no. 6: 1182. https://doi.org/10.3390/microorganisms13061182
APA StyleDreghiciu, I. C., Hoffman, D., Dumitru, S., Oprescu, I., Imre, M., Florea, T., Plesko, A., Iorgoni, V., Morariu, S., Dărăbuș, G., & Ilie, M. S. (2025). First Molecular Identification of Zoonotic Babesia odocoilei in Ticks from Romania. Microorganisms, 13(6), 1182. https://doi.org/10.3390/microorganisms13061182