Occurrence of Babesia Species and Co-Infection with Hepatozoon canis in Symptomatic Dogs and in Their Ticks in Eastern Romania
Abstract
:1. Introduction
2. Results
2.1. Dogs
2.2. Ticks
3. Discussion
4. Materials and Methods
4.1. Study Design and Samples Collection
4.2. DNA Extraction, PCR Amplification and Sequencing
4.3. Statistical Analysis
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Acknowledgments
Conflicts of Interest
References
- Dantas-Torres, F.; Chomel, B.B.; Otranto, D. Ticks and tick-borne diseases: A one health perspective. Trends Parasitol. 2012, 28, 437–446. [Google Scholar] [CrossRef]
- Baneth, G.; Bourdeau, P.; Bourdoiseau, G.; Bowman, D.; Breitschwerdt, E.; Capelli, G.; Cardoso, L.; Dantas-Torres, F.; Day, M.; Dedet, J.-P.; et al. Vector-Borne Diseases—constant challenge for practicing veterinarians: Recommendations from the CVBD World Forum. Parasites Vectors 2012, 5, 55. [Google Scholar] [CrossRef] [Green Version]
- Banović, P.; Díaz-Sánchez, A.A.; Galon, C.; Foucault-Simonin, A.; Simin, V.; Mijatović, D.; Papić, L.; Wu-Chuang, A.; Obregón, D.; Moutailler, S.; et al. A one health approach to study the circulation of tick-borne pathogens: A preliminary study. One Health 2021, 13, 100270. [Google Scholar] [CrossRef] [PubMed]
- Otranto, D.; Dantas-Torres, F.; Weigl, S.; Latrofa, M.S.; Stanneck, D.; Decaprariis, D.; Capelli, G.; Baneth, G. Diagnosis of Hepatozoon canis in young dogs by cytology and PCR. Parasites Vectors 2011, 4, 55. [Google Scholar] [CrossRef] [Green Version]
- Hamel, D.; Silaghi, C.; Lescai, D.; Pfister, K. Epidemiological aspects on vector-borne infections in stray and pet dogs from Romania and Hungary with focus on Babesia spp. Parasitol. Res. 2011, 110, 1537–1545. [Google Scholar] [CrossRef] [PubMed]
- Imre, M.; Farkas, R.; Ilie, M.; Imre, K.; Hotea, I.; Morariu, S.; Morar, D.; Dărăbuş, G. Seroprevalence of Babesia canis infection in clinically healthy dogs from Western Romania. J. Parasitol. 2013, 99, 161–163. [Google Scholar] [CrossRef]
- Solano-Gallego, L.; Sainz, Á.; Roura, X.; Peña, A.E.; Miró, G. A review of canine babesiosis: The European perspective. Parasites Vectors 2016, 9, 1–18. [Google Scholar] [CrossRef] [Green Version]
- Andersson, M.O.; Tolf, C.; Tamba, P.; Stefanache, M.; Waldenström, J.; Dobler, G.; Chitimia-Dobler, L. Canine tick-borne diseases in pet dogs from Romania. Parasites Vectors 2017, 10, 155. [Google Scholar] [CrossRef] [Green Version]
- Leica, L.; Mitrea, I.L.; Ionita, M. Clinical occurrence of canine babesiosis in the coastal area of the Black Sea (Dobrogea) in southeastern Romania and associated epidemiological implications. J. Parasitol. 2019, 105, 491–496. [Google Scholar] [CrossRef] [PubMed]
- Cimpan, A.A.; Nachum-Biala, Y.; Ben-Shitrit, B.; Miron, L.; Baneth, G. Epidemiological study of canine babesiosis and hepatozoonosis in the South of Romania. Acta Parasitol. 2020, 65, 669–678. [Google Scholar] [CrossRef] [PubMed]
- Penzhorn, B.L. Don’t let sleeping dogs lie: Unravelling the identity and taxonomy of babesia canis, babesia rossi and babesia vogeli. Parasites Vectors 2020, 13, 1–9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dantas-Torres, F. The brown dog tick, Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae): From taxonomy to control. Vet. Parasitol. 2008, 152, 173–185. [Google Scholar] [CrossRef] [PubMed]
- Foldvari, G.; Široký, P.; Szekeres, S.; Majoros, G.; Sprong, H. Dermacentor reticulatus: A vector on the rise. Parasites Vectors 2016, 9, 1–29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rizzoli, A.; Silaghi, C.; Obiegala, A.; Rudolf, I.; Hubálek, Z.; Földvári, G.; Plantard, O.; Vayssier-Taussat, M.; Bonnet, S.; Spitalská, E.; et al. Ixodes ricinus and its transmitted pathogens in urban and peri-urban areas in Europe: New hazards and relevance for public health. Front. Public Health 2014, 1, 251. [Google Scholar] [CrossRef]
- Gray, J.S.; Estrada-Peña, A.; Zintl, A. Vectors of Babesiosis. Annu. Rev. Èntomol. 2019, 64, 149–165. [Google Scholar] [CrossRef] [PubMed]
- Greene, C.E. Feline enteric viral infections. In Infectious Diseases of the Dog and Cat, 4th ed.; Elsevier/Sounders: St. Lousis, MO, USA, 2012; pp. 771–784. [Google Scholar]
- Levi, M.M.; Nachum-Biala, Y.; King, R.; Baneth, G. A survey of Babesia spp. and Hepatozoon spp. in wild canids in Israel. Parasites Vectors 2018, 11, 150. [Google Scholar] [CrossRef] [PubMed]
- 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] [PubMed]
- Kraje, A.C. Canine haemobartonellosis and babesiosis. Compend. Contin. Educ. Pract. Vet. 2001, 23, 310–318. [Google Scholar]
- Ullal, T.; Birkenheuer, A.; Vaden, S. Azotemia and proteinuria in dogs infected with Babesia gibsoni. J. Am. Anim. Hosp. Assoc. 2018, 54, 156–160. [Google Scholar] [CrossRef] [PubMed]
- Irwin, P.J. Canine babesiosis: From molecular taxonomy to control. Parasites Vectors 2009, 2, 1–9. [Google Scholar] [CrossRef] [Green Version]
- Solano-Gallego, L.; Baneth, G. Babesiosis in dogs and cats—Expanding parasitological and clinical spectra. Veter. Parasitol. 2011, 181, 48–60. [Google Scholar] [CrossRef]
- Lempereur, L.; Beck, R.; Fonseca, I.; Marques, C.; Duarte, A.; Santos, M.; Zúquete, S.; Gomes, J.; Walder, G.; Domingos, A.; et al. Guidelines for the detection of Babesia and Theileria Parasites. Vector Borne Zoonotic Dis. 2017, 17, 51–65. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Galán, A.; Mayer, I.; Rafaj, R.B.; Bendelja, K.; Sušić, V.; Cerón, J.J.; Mrljak, V. MCP-1, KC-like and IL-8 as critical mediators of pathogenesis caused by Babesia canis. PLoS ONE 2018, 13, e0190474. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Böhm, M.; Leisewitz, A.L.; Thompson, P.N.; Schoeman, J.P. Capillary and venous Babesia canis rossi parasitaemias and their association with outcome of infection and circulatory compromise. Veter. Parasitol. 2006, 141, 18–29. [Google Scholar] [CrossRef] [PubMed]
- Leisewitz, A.; Goddard, A.; De Gier, J.; Van Engelshoven, J.; Clift, S.; Thompson, P.; Schoeman, J.P. Disease severity and blood cytokine concentrations in dogs with natural Babesia rossi infection. Parasite Immunol. 2019, 41, e12630. [Google Scholar] [CrossRef]
- Baneth, G.; Nachum-Biala, Y.; Birkenheuer, A.J.; Schreeg, M.E.; Prince, H.; Florin-Christensen, M.; Schnittger, L.; Aroch, I. A new piroplasmid species infecting dogs: Morphological and molecular characterization and pathogeny of Babesia negevi n. sp. Parasites Vectors 2020, 13, 1–13. [Google Scholar] [CrossRef]
- Little, S.E.; Allen, K.E.; Johnson, E.M.; Panciera, R.J.; Reichard, M.V.; Ewing, S.A. New developments in canine hepatozoonosis in North America: A review. Parasites Vectors 2009, 2, 1–4. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Roopali, B.; Mahadappa, P.; Satheesha, S.P.; Sandeep, H.; Kasaralikar, V.; Patil, N.A. Acute hepatozoonosis in dogs: A case report. J. Parasit. Dis. 2017, 41, 747–749. [Google Scholar] [CrossRef]
- Baneth, G. Perspectives on canine and feline hepatozoonosis. Veter Parasitol. 2011, 181, 3–11. [Google Scholar] [CrossRef]
- Imre, M.; Farkas, R.; Ilie, M.S.; Imre, K.; Dărăbuş, G. Survey of babesiosis in symptomatic dogs from Romania: Occurrence of Babesia gibsoni associated with breed. Ticks Tick-Borne Dis. 2013, 4, 500–502. [Google Scholar] [CrossRef]
- Ionita, M.; Mitrea, I.L.; Pfister, K.; Hamel, D.; Buzatu, C.M.; Silaghi, C. Canine babesiosis in Romania due to Babesia canis and Babesia vogeli: A molecular approach. Parasitol. Res. 2011, 110, 1659–1664. [Google Scholar] [CrossRef] [PubMed]
- Imre, M.; Dudu, A.; Ilie, M.S.; Morariu, S.; Imre, K.; Dărăbuş, G. Molecular Survey of Hepatozoon canis in Red Foxes (Vulpes vulpes) from Romania. J. Parasitol. 2015, 101, 490–491. [Google Scholar] [CrossRef]
- Andersson, M.; Turcitu, M.A.; Stefanache, M.; Tamba, P.; Barbuceanu, F.; Chitimia, L. First evidence of Anaplasma platys and Hepatozoon canis co-infection in a dog from Romania—A case report. Ticks Tick Borne Dis. 2013, 4, 317–319. [Google Scholar] [CrossRef]
- Ilie, M.S.; Darabus, G.; Imre, M.; Imre, K.; Hotea, I.; Sorescu, I. Survey of canine babesiosis in Banat area. Bull. UASVM Vet. Medicine. 2010, 67, 125–130. [Google Scholar]
- Ionita, M.; Mitrea, I.L.; Pfister, K.; Hamel, D.; Silaghi, C. Molecular evidence for bacterial and protozoan pathogens in hard ticks from Romania. Veter. Parasitol. 2013, 196, 71–76. [Google Scholar] [CrossRef]
- Solano-Gallego, L.; Trotta, M.; Carli, E.; Carcy, B.; Caldin, M.; Furlanello, T. Babesia canis canis and Babesia canis vogeli clinicopathological findings and DNA detection by means of PCR-RFLP in blood from Italian dogs suspected of tick-borne disease. Veter. Parasitol. 2008, 157, 211–221. [Google Scholar] [CrossRef]
- Máthé, A.; Dobos-Kovács, M.; Voros, K. Histological and ultrastructural studies of renal lesions in Babesia canis infected dogs treated with imidocarb. Acta Veter. Hung. 2007, 55, 511–523. [Google Scholar] [CrossRef]
- Guo, H.; Sevinc, F.; Ceylan, O.; Sevinc, M.; Ince, E.; Gao, Y.; Moumouni, P.F.A.; Liu, M.; Efstratiou, A.; Wang, G.; et al. A PCR survey of vector-borne pathogens in different dog populations from Turkey. Acta Parasitol. 2017, 62, 533–540. [Google Scholar] [CrossRef] [PubMed]
- Gabrielli, S.; Otašević, S.; Ignjatović, A.; Savic, S.; Fraulo, M.; Arsić-Arsenijević, V.; Momčilović, S.; Cancrini, G. Canine Babesioses in Noninvestigated Areas of Serbia. Vector-Borne Zoonotic Dis. 2015, 15, 535–538. [Google Scholar] [CrossRef]
- Barutzki, D.; Reule, M.; Scheunemann, R.; Heile, C.; Schein, E. Die Babesiose des Hundes. Dtsch. Tierärzteblatt 2007, 3, 284–293. [Google Scholar]
- Nijhof, A.M.; Bodaan, C.; Postigo, M.; Nieuwenhuijs, H.; Opsteegh, M.; Franssen, L.; Jebbink, F.; Jongejan, F. Ticks and Associated Pathogens Collected from Domestic Animals in the Netherlands. Vector Borne Zoonotic Dis. 2007, 7, 585–596. [Google Scholar] [CrossRef]
- Sréter, T.; Széll, Z.; Varga, I. Spatial distribution of Dermacentor reticulatus and Ixodes ricinus in Hungary: Evidence for change? Veter. Parasitol. 2005, 128, 347–351. [Google Scholar] [CrossRef]
- Heile, C.; Heydorn, A.O.; Schein, E. Dermacentor reticulatus (Fabricius, 1794)—Verbreitung, Biologie und Vektor von Babesia canis in Deutschland. Berl. Münch. Tierärztl. Wochenschr. 2006, 119, 330–334. [Google Scholar]
- Hamel, D.; Röhrig, E.; Pfister, K. Canine vector-borne disease in travelled dogs in Germany—A retrospective evaluation of laboratory data from the years 2004–2008. Veter. Parasitol. 2011, 181, 31–36. [Google Scholar] [CrossRef] [PubMed]
- Diakou, A.; Di Cesare, A.; Morelli, S.; Colombo, M.; Halos, L.; Simonato, G.; Tamvakis, A.; Beugnet, F.; Paoletti, B.; Traversa, D. Endoparasites and vector-borne pathogens in dogs from Greek islands: Pathogen distribution and zoonotic implications. PLoS Negl. Trop. Dis. 2019, 13, e0007003. [Google Scholar] [CrossRef] [Green Version]
- Mihalca, A.D.; Dumitrache, M.O.; Magdas, C.; Gherman, C.M.; Domsa, C.; Mircean, V.; Ghira, I.V.; Pocora, V.; Ionescu, D.T.; Baraba, S. Synopsis of the hard ticks (Acari: Ixodidae) of Romania with update on host associations and geographical distribution. Exp. Appl. Acarol. 2012, 58, 183–206. [Google Scholar] [CrossRef]
- Tudor, P.; Braslasu, D.E.; Fernoaga, C. Study on natural infestation with hard ticks on dogs in Bucharest. Sci. Work. —Univ. Agron. Sci. Vet. Med. Buchar. Ser. C Vet. Med. 2010, 56, 172–179. [Google Scholar]
- Ioniţă, M.; Mitrea, I.L. Observations on the life cycle of the brown dog tick (Rhipicephalus sanguineus Latreille 1806, Acari: Ix-odidae), in the Buchraest’s environment conditions. Sci. Parasitol. 2003, 4, 167–171. [Google Scholar]
- Ioniţă, M.; Mitrea, I.L.; Buzatu, M.C.; Dascalu, L. Seasonal dynamics of tick (Acari: Ixodidae) populations in different areas of Romania and the associated risks of tick-borne diseases. In Proceedings of the XIIth International Congress of Parasitology (ICOPA), Melbourne, Australia, 15–20 August 2010; p. 665. [Google Scholar]
- Bratuleanu, B.E.; Temmam, S.; Chrétien, D.; Regnault, B.; Pérot, P.; Bouchier, C.; Bigot, T.; Savuța, G.; Eloit, M. The virome of Rhipicephalus, Dermacentor and Haemaphysalis ticks from Eastern Romania includes novel viruses with potential relevance for public health. Transbound. Emerg. Dis. 2021, 1–17. [Google Scholar] [CrossRef]
- Najm, N.-A.; Meyer-Kayser, E.; Hoffmann, L.; Pfister, K.; Silaghi, C. Hepatozoon canis in German red foxes (Vulpes vulpes) and their ticks: Molecular characterization and the phylogenetic relationship to other Hepatozoon spp. Parasitol. Res. 2014, 113, 2679–2685. [Google Scholar] [CrossRef] [PubMed]
- Reye, A.L.; Hübschen, J.M.; Sausy, A.; Muller, C.P. Prevalence and Seasonality of Tick-Borne Pathogens in Questing Ixodes ricinus Ticks from Luxembourg. Appl. Environ. Microbiol. 2010, 76, 2923–2931. [Google Scholar] [CrossRef] [Green Version]
- Namina, A.; Capligina, V.; Seleznova, M.; Krumins, R.; Aleinikova, D.; Kivrane, A.; Akopjana, S.; Lazovska, M.; Berzina, I.; Ranka, R. Tick-borne pathogens in ticks collected from dogs, Latvia, 2011–2016. BMC Veter. Res. 2019, 15, 1–10. [Google Scholar] [CrossRef]
- Giannelli, A.; Ramos, R.A.N.; Dantas-Torres, F.; Mencke, N.; Baneth, G.; Otranto, D. Experimental evidence against transmission of Hepatozoon canis by Ixodes ricinus. Ticks Tick-Borne Dis. 2013, 4, 391–394. [Google Scholar] [CrossRef] [PubMed]
- Potkonjak, A.; Gutiérrez, R.; Savic, S.; Vračar, V.; Nachum-Biala, Y.; Jurišić, A.; Kleinerman, G.; Rojas, A.; Petrović, A.; Baneth, G.; et al. Molecular detection of emerging tick-borne pathogens in Vojvodina, Serbia. Ticks Tick-Borne Dis. 2016, 7, 199–203. [Google Scholar] [CrossRef] [PubMed]
- Chitimia-Dobler, L.; Langguth, J.; Pfeffer, M.; Kattner, S.; Küpper, T.; Friese, D.; Dobler, G.; Guglielmone, A.A. Genetic analysis of ticks parasites of dogs in Africa north of the Sahara based on mitochondrial DNA sequences. Vet. Parasitol. 2017, 239, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Miterpáková, M.; Komjáti-Nagyová, M.; Hurníková, Z.; Víchová, B. Retrospective molecular study on canine hepatozoonosis in Slovakia—Does really infection risk for dogs exist? Ticks Tick Borne Dis. 2017, 8, 567–573. [Google Scholar] [CrossRef] [PubMed]
- Baneth, G.; Samish, M.; Shkap, V. Life cycle of Hepatozoon canis (Apicomplexa: Adeleorina: Hepatozoidae) in the tick Rhipicephalus sanguineus and domestic dog (Canis familiaris). J. Parasitol. 2007, 93, 283–299. [Google Scholar] [CrossRef]
- Christophers, S.R. The sexual life cycle of Leucocytozoon canis in the tick. Sci. Mem. Off. Med. Sanit. Dep. Gov. India 1907, 28, 1–11. [Google Scholar]
- Galay, R.L.; Manalo, A.A.L.; Dolores, S.L.D.; Aguilarm, I.P.M.; Sandalo, K.A.C.; Cruz, K.B.; Divina, B.P.; Andoh, M.; Masatani, T.; Tanaka, T. Molecular detection of tick-borne pathogens in canine population and Rhipicephalus sanguineus (sensu lato) ticks from southern Metro Manila and Laguna, Philippines. Parasites Vectors 2018, 11, 643. [Google Scholar] [CrossRef]
- Bouattour, A.; Chabchoub, A.; Hajjaji, I.; M’ghirbi, Y. Hepatozoon canis and Babesia vogeli infections of dogs in Tunisia. Vet. Parasitol. Reg. Stud. Rep. 2021, 23, 100512. [Google Scholar]
- Juasook, A.; Siriporn, B.; Nopphakhun, N.; Phetpoang, P.; Khamyang, S. Molecular detection of tick-borne pathogens in infected dogs associated with Rhipicephalus sanguineus tick infestation in Thailand. Vet. World 2021, 14, 1631–1637. [Google Scholar] [CrossRef] [PubMed]
- Baneth, G.; Thamsborg, S.M.; Otranto, D.; Guillo, J.; Blaga, R.; Deplazes, P.; Solano-Gallego, L. Major parasitic zoonoses associated with dogs and cats in Europe. J. Comp. Pathol. 2016, 155, 54–74. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Otranto, D. Arthropod-borne pathogens of dogs and cats: From pathways and times of transmission to disease control. Vet. Parasitol. 2018, 15, 68–77. [Google Scholar] [CrossRef]
- Colombo, M.; Morelli, S.; Simonato, G.; Di Cesare, A.; Veronesi, F.; Frangipane Di Regalbono, A.; Grassi, L.; Russi, I.; Tiscar, P.G.; Morganti, G.; et al. Exposure to major vector-borne diseases in dogs subjected to different preventative regimens in endemic areas of Italy. Pathogens 2021, 10, 507. [Google Scholar] [CrossRef]
- Morelli, S.; Diakou, A.; Traversa, D.; Di Gennaro, E.; Simonato, G.; Colombo, M.; Dimzas, D.; Grillini, M.; Frangipane Di Regalbono, A.; Beugnet, F.; et al. First record of Hepatozoon spp. in domestic cats in Greece. Ticks Tick Borne Dis. 2021, 12, 101580. [Google Scholar] [CrossRef]
- Viljoen, S.; O’Riain, M.J.; Penzhorn, B.L.; Drouilly, M.; Vorster, I.; Bishop, J.M. Black-backed jackals (Canis mesomelas) from semi-arid rangelands in South Africa harbour Hepatozoon canis and a Theileria species but apparently not Babesia rossi. Vet. Parasitol. Reg. Stud. Reports. 2021, 24, 100559. [Google Scholar] [PubMed]
- Angelescu, A. The Golden Jackal: Origin, Morphoanatomy, Eco-Etholgy, Management; MMC: Bucharest, Romania, 2004. [Google Scholar]
- Papp, C.R.; Banea, O.C.; Szekely-Sitea, A.I. Applied ecology and management aspects related to the golden jackal specific ecological system in Romania. Acta Musei Maramorosiensis 2014, 9, 275–292. [Google Scholar]
- Ionică, A.M.; Matei, I.A.; D’Amico, G.; Daskalaki, A.A.; Juránková, J.; Ionescu, D.T.; Mihalca, A.D.; Modrý, D.; Gherman, C.M. Role of golden jackals (Canis aureus) as natural reservoirs of Dirofilaria spp. in Romania. Parasites Vectors 2016, 28, 240. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arnold, J.; Humer, A.; Heltai, M.; Murariu, D.; Spassov, N.; Hackländer, K. Current status and distribution of golden jackals (Canis aureus L., 1758) in Europe. Mammal. Rev. 2012, 42, 1–11. [Google Scholar] [CrossRef]
- Trouwborst, A.; Krofel, M.; Linnell, J.D.C. Legal implications of range expansions in a terrestrial carnivore: The case of the golden jackal (Canis aureus) in Europe. Biodivers. Conserv. 2015, 24, 2593–2610. [Google Scholar] [CrossRef] [Green Version]
- Vasiliu, G. Verzeichnis der Säugetiere Rumäniens (Enumera ia mamiferelor din România). Säugetierkd Mitt. München 1961, 9, 56–68. [Google Scholar]
- Birkenheuer, A.J.; Buch, J.; Beall, M.J.; Braff, J.; Chandrashekar, R. Global distribution of canine Babesia species identified by a commercial diagnostic laboratory. Vet. Parasitol. Reg. Stud. Rep. 2020, 22, 100471. [Google Scholar] [CrossRef]
- Estrada-Pena, A.; Bouattour, A.; Camicas, J.L.; Walker, A.R. Ticks of Domestic Animals in the Mediterranean Region: A guide to The Identification of Species, 1st ed.; University of Zaragoza: Zaragoza, Spain, 2004. [Google Scholar]
- Dantas-Torres, F.; Latrofa, M.S.; Annoscia, G.; Giannelli, A.; Parisi, A.; Otranto, D. Morphological and genetic diversity of Rhipicephalus sanguineus sensu lato from the New and Old Worlds. Parasites Vectors 2013, 6, 213. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marchiondo, A.A.; Holdsworth, P.A.; Green, P.; Blagburn, B.L.; Jacobs, D.E. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) guidelines for evaluating the efficacy of parasiticides for the treatment, prevention and control of flea and tick infestation on dogs and cats. Vet. Parasitol. 2007, 145, 332–344. [Google Scholar]
- Bajer, A.; Dwużnik, D.; Tołkacz, K.; Alsarraf, M.; Mierzejewska, E.J. Comparison of the detection efficiency of haemoparasite DNA in blood and faecal samples—The way to eco-epidemiological studies. Ann. Agric. Environ. Med. 2019, 26, 538–543. [Google Scholar] [CrossRef] [PubMed]
- Inokuma, H.; Okuda, M.; Ohno, K.; Shimoda, K.; Onishi, T. Analysis of the 18S rRNA gene sequence of a Hepatozoon detected in two Japanese dogs. Vet. Parasitol. 2002, 106, 265–271. [Google Scholar] [CrossRef]
- Kramer, V.; Randolph, M.; Hui, L.; Irwin, W.; Gutierrez, A.; Duc, J. Detection of the agents of human ehrlichioses in Ixodid ticks from California. Am. J. Trop. Med. Hyg. 1999, 60, 62–65. [Google Scholar] [CrossRef] [Green Version]
- Zanet, S.; Battisti, E.; Pepe, P.; Ciuca, L.; Colombo, L.; Trisciuoglio, A.; Ferroglio, E.; Cringoli, G.; Rinaldi, L.; Maurelli, M.P. Tick-borne pathogens in Ixodidae ticks collected from privately-owned dogs in Italy: A country-wide molecular survey. BMC Vet. Res. 2020, 7, 16–46. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Far, D.; Takács, N.; Gyurkovszky, M.; Solymosi, N.; Farkas, R. Ticks and tick-borne infections of dogs in two Jordanian shelters. Vector Borne Zoonotic Dis. 2021, 21, 573–578. [Google Scholar] [CrossRef] [PubMed]
Variable | Babesial Prevalence (95% CI) |
---|---|
Gender Males Females | 52.2% (41.5–62.7) 47.8% (37.2–58.5) |
Age categories (years) Puppies (>1) 1–3 4–6 7–10 >10 | 5.6% (2.1–13.1) 58.9% (48.0–69.0) 13.3% (7.4–22.5) 10% (4.9–18.6) 12.2% (6.6–21.2) |
Dog breeds Cross-breed Peking German Sheperd Akita Beagle Caucasian Sheperd Bullmastiff Bull terrier Boxer | 52.2% (41.5–62.8) 14.4% (8.2–23.8) 10% (4.9–18.6) 2.2% (0.4–8.6) 5.6% (2.1–13.1) 4.4% (1.4–11.6) 1.1% (0.1–6.9) 3.3% (0.9–10.1) 6.7% (2.7–14.5) |
Lifestyle Outdoors Indoors | 74.4% (63.9–82.8) 25.6% (17.2–36.0) |
Tick infestation history | 100% (94.9–99.9) |
Dogs With ticks Without ticks | 16.7% (9.9–26.3) 83.3% (73.7–90.0) |
Babesiosis Acute Mild | 61.1% (50.2–71.0) 38.9% (28.9–49.8) |
Total dogs analysed (90) | 100% (94.9–99.9) |
Species | No. of Ticks (Females/Males/Nymphs/Larvae) | No. Pools (Females/Males/Nymphs/Larvae) | Pathogen Species |
---|---|---|---|
Ixodes ricinus | 112 (73/38/1/0) | 64 (45/19/1/0) | * B. canis (n = 55) * H. canis (n = 15) * B. microti-like piroplasm (n = 1) |
Dermacentor reticulatus | 67 (39/28/0/0) | 33 (20/13/0/0) | B. canis (n = 33) |
Rhipicephalus sanguineus group | 3 (1/0/1/1) | 3 (1/0/1/1) | B. vogeli (n = 3) |
Samples Collection | Laboratory Analyses |
---|---|
Blood samples from symptomatic dogs (no. = 90) and collection of ticks (no. = 58 ticks present on 15 dogs) | Quick Romanowsky stained-thin blood smear [23] for detection of intra-erythrocytic piroplasms DNA extraction, PCR amplification and sequencing [79,80] for Babesia spp. and H. canis Morphological identification of the ticks [76,77] |
124 ticks collected from the coat of other 23 dogs previously diagnosed with babesiosis by stained blood smears | Morphological identification of the ticks [76,77] |
Total number of tick sub-samples (no. = 100) | DNA extraction, PCR amplification and sequencing [79,80] for Babesia spp. and H. canis |
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Ciuca, L.; Martinescu, G.; Miron, L.D.; Roman, C.; Acatrinei, D.; Cringoli, G.; Rinaldi, L.; Maurelli, M.P. Occurrence of Babesia Species and Co-Infection with Hepatozoon canis in Symptomatic Dogs and in Their Ticks in Eastern Romania. Pathogens 2021, 10, 1339. https://doi.org/10.3390/pathogens10101339
Ciuca L, Martinescu G, Miron LD, Roman C, Acatrinei D, Cringoli G, Rinaldi L, Maurelli MP. Occurrence of Babesia Species and Co-Infection with Hepatozoon canis in Symptomatic Dogs and in Their Ticks in Eastern Romania. Pathogens. 2021; 10(10):1339. https://doi.org/10.3390/pathogens10101339
Chicago/Turabian StyleCiuca, Lavinia, Gabriela Martinescu, Liviu Dan Miron, Constantin Roman, Dumitru Acatrinei, Giuseppe Cringoli, Laura Rinaldi, and Maria Paola Maurelli. 2021. "Occurrence of Babesia Species and Co-Infection with Hepatozoon canis in Symptomatic Dogs and in Their Ticks in Eastern Romania" Pathogens 10, no. 10: 1339. https://doi.org/10.3390/pathogens10101339
APA StyleCiuca, L., Martinescu, G., Miron, L. D., Roman, C., Acatrinei, D., Cringoli, G., Rinaldi, L., & Maurelli, M. P. (2021). Occurrence of Babesia Species and Co-Infection with Hepatozoon canis in Symptomatic Dogs and in Their Ticks in Eastern Romania. Pathogens, 10(10), 1339. https://doi.org/10.3390/pathogens10101339