Hostname: page-component-76fb5796d-vfjqv Total loading time: 0 Render date: 2024-04-25T16:27:57.427Z Has data issue: false hasContentIssue false

Rhipicephalus turanicus, a new vector of Hepatozoon canis

Published online by Cambridge University Press:  21 December 2016

ALESSIO GIANNELLI
Affiliation:
Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, Valenzano, Bari, Italy
RICCARDO PAOLO LIA
Affiliation:
Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, Valenzano, Bari, Italy
GIADA ANNOSCIA
Affiliation:
Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, Valenzano, Bari, Italy
CANIO BUONAVOGLIA
Affiliation:
Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, Valenzano, Bari, Italy
ELEONORA LORUSSO
Affiliation:
Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, Valenzano, Bari, Italy
FILIPE DANTAS-TORRES
Affiliation:
Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, Valenzano, Bari, Italy Departamento de Imunologia, Centro de Pesquisas Aggeu Magalhães (Fiocruz-PE), Recife, Pernambuco, Brazil
GAD BANETH
Affiliation:
School of Veterinary Medicine, Hebrew University, Rehovot, Israel
DOMENICO OTRANTO*
Affiliation:
Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, Valenzano, Bari, Italy
*
*Corresponding author: Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, Valenzano, Bari, Italy. E-mail: domenico.otranto@uniba.it

Summary

The distribution of Hepatozoon canis mainly encompasses areas where its main tick vector, Rhipicephalus sanguineus sensu lato, is present. However, the detection of this pathogen in dogs, foxes and golden jackals well outside the areas inhabited by this tick species reinforced the hypothesis that additional ixodids are involved in the life cycle and transmission of this protozoon. The present study provides, for the first time, data supporting the sporogonic development of H. canis in specimens of Rhipicephalus turanicus collected from a naturally infected fox from southern Italy. The epidemiological role of R. turanicus as a vector of H. canis is discussed, along with information on the potential use of cell cultures for the experimental infection with H. canis sporozoites. The in vitro infection of canine leucocytes by sporozoites from ticks is proposed as a potential tool for future in-depth studies on the biology of H. canis.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aktas, M. (2014). A survey of ixodid tick species and molecular identification of tick-borne pathogens. Veterinary Parasitology 200, 276283.CrossRefGoogle ScholarPubMed
Alencar, N. X., Kohayagawa, A., Santarém, V. A. (1997). Hepatozoon canis infection of wild carnivores in Brazil. Veterinary Parasitology 70, 279282.Google Scholar
Ball, G. H., Chao, J. (1973). The complete development of the sporogonous stages of Hepatozoon rarefaciens cultured in a Culex pipiens cell line. Journal of Parasitology 59, 513515.Google Scholar
Baneth, G. (2011). Perspectives on canine and feline hepatozoonosis. Veterinary Parasitology 181, 311.Google Scholar
Baneth, G., Samish, M., Shkap, V. (2007). Life cycle of Hepatozoon canis (Apicomplexa: Adeleorina: Hepatozoidae) in the tick Rhipicephalus sanguineus and domestic dog (Canis familiaris). Journal of Parasitology 93, 283299.CrossRefGoogle ScholarPubMed
Çetinkaya, H., Matur, E., Akyazi, İ., Ekiz, E. E., Aydin, L., Toparlak, M. (2016). Serological and molecular investigation of Ehrlichia spp. and Anaplasma spp. in ticks and blood of dogs, in the Thrace Region of Turkey. Ticks and Tick Borne Diseases 7, 706714.Google Scholar
Chochlakis, D., Ioannou, I., Papadopoulos, B., Tselentis, Y., Psaroulaki, A. (2014). Rhipicephalus turanicus: from low numbers to complete establishment in Cyprus. Its possible role as a bridge-vector. Parasites and Vectors 7 (Suppl. 1), P11.Google Scholar
Dantas-Torres, F., Latrofa, M. S., Annoscia, G., Giannelli, A., Parisi, A., Otranto, D. (2013). Morphological and genetic diversity of Rhipicephalus sanguineus sensu lato from the New and Old Worlds. Parasites and Vectors 6, 213.Google Scholar
de Miranda, R. L., de Castro, J. R., Olegário, M. M., Beletti, M. E., Mundim, A. V., O'Dwyer, L. H., Eyal, O., Talmi-Frank, D., Cury, M. C., Baneth, G. (2011). Oocysts of Hepatozoon canis in Rhipicephalus (Boophilus) microplus collected from a naturally infected dog. Veterinary Parasitology 177, 392396.Google Scholar
De Tommasi, A. S., Giannelli, A., de Caprariis, D., Ramos, R. A., Di Paola, G., Crescenzo, G., Dantas-Torres, F., Baneth, G., Otranto, D. (2014). Failure of imidocarb dipropionate and toltrazuril/emodepside plus clindamycin in treating Hepatozoon canis infection. Veterinary Parasitology 200, 242245.Google Scholar
Demoner, L. C., Rubini, A. S., Paduan Kdos, S., Metzger, B., de Paula Antunes, J. M., Martins, T. F., Mathias, M. I., O'Dwyer, L. H. (2013). Investigation of tick vectors of Hepatozoon canis in Brazil. Ticks and Tick Borne Diseases 4, 542546.Google Scholar
Duscher, G. G., Kübber-Heiss, A., Richter, B., Suchentrunk, F. (2013). A golden jackal (Canis aureus) from Austria bearing Hepatozoon canis – import due to immigration into a non-endemic area? Ticks and Tick Borne Diseases 4, 133137.Google Scholar
Duscher, G. G., Leschnik, M., Fuehrer, H. P., Joachim, A. (2014). Wildlife reservoirs for vector-borne canine, feline and zoonotic infections in Austria. International Journal for Parasitology: Parasites and Wildlife 4, 8896.Google Scholar
Farkas, R., Solymosi, N., Takács, N., Hornyák, Á., Hornok, S., Nachum-Biala, Y., Baneth, G. (2014). First molecular evidence of Hepatozoon canis infection in red foxes and golden jackals from Hungary. Parasites and Vectors 7, 303.Google Scholar
Ferguson, L. V., Kirk Hillier, N., Smith, T. G. (2012). Influence of Hepatozoon parasites on host-seeking and host-choice behaviour of the mosquitoes Culex territans and Culex pipiens . International Journal for Parasitology: Parasites and Wildlife 2, 6976.Google Scholar
Gabrielli, S., Kumlien, S., Calderini, P., Brozzi, A., Iori, A., Cancrini, G. (2010). The first report of Hepatozoon canis identified in Vulpes vulpes and ticks from Italy. Vector Borne Zoonotic Diseases 10, 855859.Google Scholar
Giannelli, A., Ramos, R. A., Dantas-Torres, F., Mencke, N., Baneth, G., Otranto, D. (2013 a). Experimental evidence against transmission of Hepatozoon canis by Ixodes ricinus . Ticks and Tick Borne Diseases 4, 391394.Google Scholar
Giannelli, A., Ramos, R. A., Di Paola, G., Mencke, N., Dantas-Torres, F., Baneth, G., Otranto, D. (2013 b). Transstadial transmission of Hepatozoon canis from larvae to nymphs of Rhipicephalus sanguineus . Veterinary Parasitology 196, 15.Google Scholar
Hamšíková, Z., Silaghi, C., Rudolf, I., Venclíková, K., Mahríková, L., Slovák, M., Mendel, J., Blažejová, H., Berthová, L., Kocianová, E., Hubálek, Z., Schnittger, L., Kazimírová, M. (2016). Molecular detection and phylogenetic analysis of Hepatozoon spp. in questing Ixodes ricinus ticks and rodents from Slovakia and Czech Republic. Parasitology Research 115, 3897–3890.Google Scholar
Hendrick, L. D., Fayer, R. (1973). Development of Hepatozoon griseisciuri in Cultured Squirrel Cells. Journal of Protozoology 2, 550554.CrossRefGoogle Scholar
Hodžić, A., Alić, A., Fuehrer, H. P., Harl, J., Wille-Piazzai, W., Duscher, G. G. (2015). A molecular survey of vector-borne pathogens in red foxes (Vulpes vulpes) from Bosnia and Herzegovina. Parasites and Vectors 8, 88.Google Scholar
Hodžić, A., Alić, A., Prašović, S., Otranto, D., Baneth, G., Duscher, G. G. (2016). Hepatozoon silvestris sp. nov.: morphological and molecular characterization of a new Hepatozoon species (Adeleorina: Hepatozoidae) from the European wild cat (Felis silvestris silvestris). Parasitology. doi: https://doi.org/10.1017/S0031182016002316.Google Scholar
Hornok, S., Tánczos, B., Fernández de Mera, I. G., de la Fuente, J., Hofmann-Lehmann, R., Farkas, R. (2013). High prevalence of Hepatozoon-infection among shepherd dogs in a region considered to be free of Rhipicephalus sanguineus . Veterinary Parasitology 196, 189193.Google Scholar
Inokuma, H., Okuda, M., Ohno, K., Shimoda, K., Onishi, T. (2002). Analysis of the 18S rRNA gene sequence of a Hepatozoon detected in two Japanese dogs. Veterinary Parasitology 106, 265271. PubMed PMID: 12062514.Google Scholar
Kamani, J., Baneth, G., Mumcuoglu, K. Y., Waziri, N. E., Eyal, O., Guthmann, Y., Harrus, S. (2013). Molecular detection and characterization of tick-borne pathogens in dogs and ticks from Nigeria. PLoS Neglected Tropical Diseases 7, e2108.Google Scholar
Kelly, P., Marabini, L., Dutlow, K., Zhang, J., Loftis, A., Wang, C. (2014). Molecular detection of tick-borne pathogens in captive wild felids, Zimbabwe. Parasites and Vectors 7, 514.Google Scholar
Latrofa, M. S., Dantas-Torres, F., Giannelli, A., Otranto, D. (2014). Molecular detection of tick-borne pathogens in Rhipicephalus sanguineus group ticks. Ticks and Tick Borne Diseases 5, 943946.Google Scholar
Majláthová, V., Hurníková, Z., Majláth, I., Petko, B. (2007). Hepatozoon canis infection in Slovakia: imported or autochthonous? Vector Borne Zoonotic Diseases 7, 199202.Google Scholar
Manilla, G. (1998). Fauna d'Italia, Acari-Ixodida. Edizioni Calderini, Bologna, Italy.Google Scholar
Matjila, P. T., Leisewitz, A. L., Jongejan, F., Bertschinger, H. J., Penzhorn, B. L. (2008). Molecular detection of Babesia rossi and Hepatozoon sp. in African wild dogs (Lycaon pictus) in South Africa. Veterinary Parasitology 157, 123127.CrossRefGoogle ScholarPubMed
McCully, R. M., Basson, P. A., Bigalke, R. D., De Vos, V., Young, E. (1975). Observations on naturally acquired hepatozoonosis of wild carnivores and dogs in the Republic of South Africa. Onderstepoort Journal of Veterinary Research 42, 117133.Google Scholar
Millán, J., Proboste, T., Fernández de Mera, I. G., Chirife, A. D., de la Fuente, J., Altet, L. (2016). Molecular detection of vector-borne pathogens in wild and domestic carnivores and their ticks at the human–wildlife interface. Ticks and Tick Borne Diseases 7, 284290.Google Scholar
Mitková, B., Hrazdilová, K., Steinbauer, V., D'Amico, G., Mihalca, A. D., Modrý, D. (2016). Autochthonous Hepatozoon infection in hunting dogs and foxes from the Czech Republic. Parasitology Research 115, 41674171.Google Scholar
Murata, T., Inoue, M., Taura, Y., Nakama, S., Abe, H., Fujisaki, K. (1995). Detection of Hepatozoon canis oocyst from ticks collected from the infected dogs. Journal of Veterinary Medical Sciences 57, 111122.Google Scholar
Najm, N. A., Meyer-Kayser, E., Hoffmann, L., Pfister, K., Silaghi, C. (2014). Hepatozoon canis in German red foxes (Vulpes vulpes) and their ticks: molecular characterization and the phylogenetic relationship to other Hepatozoon spp. Parasitology Research 113, 26792685.Google Scholar
Nijhof, A. M., Bodaan, C., Postigo, M., Nieuwenhuijs, H., Opsteegh, M., Franssen, L., Jebbink, F., Jongejan, F. (2007). Ticks and associated pathogens collected from domestic animals in the Netherlands. Vector Borne Zoonotic Diseases 7, 585595.Google Scholar
Otranto, D., Cantacessi, C., Dantas-Torres, F., Brianti, E., Pfeffer, M., Genchi, C., Guberti, V., Capelli, G., Deplazes, P. (2015 a). The role of wild canids and felids in spreading parasites to dogs and cats in Europe. Part II: helminths and arthropods. Veterinary Parasitology 213, 2437.Google Scholar
Otranto, D., Cantacessi, C., Pfeffer, M., Dantas-Torres, F., Brianti, E., Deplazes, P., Genchi, C., Guberti, V., Capelli, G. (2015 b). The role of wild canids and felids in spreading parasites to dogs and cats in Europe. Part I: protozoa and tick-borne agents. Veterinary Parasitology 213, 1223.Google Scholar
Passos, L. M. (2012). In vitro cultivation of Anaplasma marginale and A. phagocytophilum in tick cell lines: a review. Revista Brasileira Parasitologia Veterinaria 21, 8186.Google Scholar
Ramos, R. A., Giannelli, A., Carbone, D., Baneth, G., Dantas-Torres, F., Otranto, D. (2014). Occurrence of Hepatozoon canis and Cercopithifilaria bainae in an off-host population of Rhipicephalus sanguineus sensu lato ticks. Ticks and Tick Borne Diseases 5, 311314.Google Scholar
Redington, B. C., Jachowski, L. A. (1971). Syngamy and sporogony of Hepatozoon griseisciuri Clark, 1958 (Sporozoa: Haemogregarinidae), in its natural vector, Haemogamasus reidi Ewing, 1925 (Acari: Mesostigmata). Journal of Parasitology 57, 953960.Google Scholar
Rubini, A. S., Paduan, K. S., Martins, T. F., Labruna, M. B., O'Dwyer, L. H. (2009). Acquisition and transmission of Hepatozoon canis (Apicomplexa: Hepatozoidae) by the tick Amblyomma ovale (Acari: Ixodidae). Veterinary Parasitology 164, 324327.Google Scholar
Sixl, W. (1972). Drie weitere Zeckenarten in Osterreich. Mitteilungen der Abteilung fir Zoologischen des Landesmuseums joanneum 1, 5152.Google Scholar
Smith, T. G. (1996). The genus Hepatozoon (Apicomplexa: Adeleina). Journal of Parasitology 82, 565585.Google Scholar
Tolnai, Z., Sréter-Lancz, Z., Sréter, T. (2015). Spatial distribution of Anaplasma phagocytophilum and Hepatozoon canis in red foxes (Vulpes vulpes) in Hungary. Ticks and Tick Borne Diseases 6, 645648.Google Scholar
Toma, L., Khoury, C., Bianchi, R., Severini, F., Mancini, F., Ciervo, A., Ricci, D., Fausto, A. M., Quarchioni, E., Di Luca, M. (2015). Preliminary investigation on tick fauna in the neighbourhood of Tarquinia, Lazio, Italy. Annali dell'Istituto Superiore di Sanità 51, 6770.Google Scholar
Uspensky, I. (2014). Tick pests and vectors (Acari: Ixodoidea) in European towns: introduction, persistence and management. Ticks and Tick Borne Diseases 5, 4147.Google Scholar
Walker, J. B., Keirans, J. E., Horak, I. G. (2000). The Genus Rhipicephalus (Acari, Ixodidae): A Guide to the Brown Ticks of the World. Cambridge University Press, Cambridge, UK.Google Scholar
Waner, T., Keysary, A., Eremeeva, M. E., Din, A. B., Mumcuoglu, K. Y., King, R., Atiya-Nasagi, Y. (2014). Rickettsia africae and Candidatus Rickettsia barbariae in ticks in Israel. American Journal of Tropical Medicine and Hygiene 90, 920922.Google Scholar
Williams, B. M., Berentsen, A., Shock, B. C., Teixiera, M., Dunbar, M. R., Becker, M. S., Yabsley, M. J. (2014). Prevalence and diversity of Babesia, Hepatozoon, Ehrlichia, and Bartonella in wild and domestic carnivores from Zambia, Africa. Parasitology Research 113, 911918.Google Scholar