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Detection of Leishmania Infantum in red foxes (Vulpes vulpes) in Central Greece

Published online by Cambridge University Press:  24 September 2015

STELIOS KARAYIANNIS
Affiliation:
Stelios Karagiannis, Ktiniatriki Epe, Vasilikon 25, Lamia, Greece
PANTELIS NTAIS
Affiliation:
Laboratory of Clinical Bacteriology, Parasitology, Zoonoses and Geographical Medicine, Faculty of Medicine, University of Crete, Greece
IPPOKRATIS MESSARITAKIS
Affiliation:
Laboratory of Clinical Bacteriology, Parasitology, Zoonoses and Geographical Medicine, Faculty of Medicine, University of Crete, Greece
NIKOLAOS TSIRIGOTAKIS
Affiliation:
Laboratory of Clinical Bacteriology, Parasitology, Zoonoses and Geographical Medicine, Faculty of Medicine, University of Crete, Greece
EMMANOUIL DOKIANAKIS
Affiliation:
Laboratory of Clinical Bacteriology, Parasitology, Zoonoses and Geographical Medicine, Faculty of Medicine, University of Crete, Greece
MARIA ANTONIOU*
Affiliation:
Laboratory of Clinical Bacteriology, Parasitology, Zoonoses and Geographical Medicine, Faculty of Medicine, University of Crete, Greece
*
*Corresponding author. University of Crete, Medical School, Voutes 710 03, Heraklion, Crete, Greece. E-mail: [email protected]

Summary

This is the first record of Leishmania detection in foxes in Greece. Spleen, lymph nodes, bone marrow and blood samples were collected from 47 red foxes (Vulpes vulpes) found dead or captured, narcotized and freed after bleeding, from November 2009 to 2011, in Fthiotida prefecture, central Greece. This is an endemic for canine leishmaniasis area with several human visceral leishmaniasis cases. The samples were tested for Leishmania infantum and Leishmania tropica by molecular methods (polymerase chain reaction (PCR) and restriction fragment length polymorphism) and serology (indirect immunofluorescent antibody test; when blood samples were available). Leishmania infantum DNA was detected in 28 animals (59·5%). PCR positivity was related to animal age, sex, weight, characteristics of the area trapped, presence of leishmaniasis symptoms and presence of endo- and ecto-parasites. The results were related to dog seropositivity obtained earlier in the area. The findings support the hypothesis that this wild canid may serve as a reservoir for Leishmania in areas where the sandfly vectors are found. In the prefectures of Larisa and Magnisia, adjacent to Fthiotida, Phlebotomus perfiliewi and Phlebotomus tobbi (known vectors of L. infantum) have been reported.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Abranches, P., Conceiçao-Silva, F. M. and Silva-Pereira, M. C. (1984). Kala-azar in Portugal. V. The sylvatic cycle in the enzootic endemic focus of Arrabida. American Journal of Tropical Medicine and Hygiene 87, 197200.Google Scholar
Beck, A., Beck, R., Kusak, J., Gudan, A., Martinkovic, F., Artukovic, B., Hohsteter, M., Huber, D., Marinculic, A. and Grabarevic, Z. (2008). A case of visceral leishmaniosis in a gray wolf (Canis lupus) from Croatia. Journal of Wildlife Diseases 44, 451456.Google Scholar
Bettini, S., Pozio, E. and Gradoni, L. (1980). Leishmaniasis in Tuscany (Italy): (II) Leishmania form wild Rodentia and Carnivora in a human and canine leishmaniasis focus. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 7783.CrossRefGoogle Scholar
Christodoulou, V., Antoniou, M., Ntais, P., Messaritakis, I., Ivovic, V., Dedet, J. P., Pratlong, F., Dvorak, V. and Tselentis, Y. (2012). Re-emergence of visceral and cutaneous leishmaniasis in the Greek Island of Crete. Vector-Borne and Zoonotic Diseases 12, 214222.Google ScholarPubMed
Cirović, D., Chochlakis, D., Tomanović, S., Sukara, R., Penezić, A., Tselentis, Y. and Psaroulaki, A. (2014). Presence of Leishmania and Brucella species in the golden jackal Canis aureus in Serbia. BioMed Research International 2014, 728516.CrossRefGoogle ScholarPubMed
Courtenay, O., Macdonald, D. W., Lainson, R., Shaw, J. J. and Dye, C. (1994). Epidemiology of canine leishmaniasis: a comparative serological study of dogs and foxes in Amazon Brazil. Parasitology 109, 273279.Google ScholarPubMed
Criado-Fornelio, A., Gutierrez-Garcia, L., Rodriguez-Caabeiro, F., Reus-Garcia, E., Roldan-Soriano, M. A. and Diaz-Sanchez, M. A. (2000). A parasitological survey of wild red foxes (Vulpes vulpes) from the province of Guadalajara, Spain. Veterinary Parasitology 92, 245251.CrossRefGoogle ScholarPubMed
Deane, M. P. and Deane, L. M. (1954). Infecção experimental do Phlebotomus longipalpis em raposa (Lycolopex vetulus), naturalmente parasitada pela Leishmania donovani . O Hospital 46, 651653.Google Scholar
Dipineto, L., Manna, L., Baiano, A., Gala, M., Fioretti, A., Gravino, A. E. and Menna, L. F. (2007). Presence of Leishmania infantum in Red Foxes (Vulpes vulpes) in Southern Italy. Journal of Wildlife Diseases 43, 518520.CrossRefGoogle ScholarPubMed
Dolev, A. (2006). Modeling the spatial dynamics of rabies in canid vectors using a realistic landscape: a tool for optimizing the spatial scattering of oral rabies vaccination . Dissertation. The Ben-Gurion University of the Negev, Beer Sheba, Israel.Google Scholar
Gramiccia, M., Maazoun, R., Lanotte, G., Rioux, J. A., le Blancq, S., Evans, D. A., Peters, W., Bettini, S., Gradoni, L. and Pozio, E. (1982). [Enzymatic typing of 11 strains of Leishmania isolated in mainland Italy from the visceral murine, canine and vulpine forms. Demonstration of an enzymatic variant in the fox (Vulpes vulpes) and the dog]. [Article in French]. Annales De Parasitologie Humaine Et Comparee 57, 527531.Google Scholar
Hervás, J., Méndez, A., Carrasco, L. and Gómez-Villamandos, J. C. (1996). Pathological study of visceral leishmaniasis in a jackal (Canis aureus). Veterinary Record 139, 293295.CrossRefGoogle Scholar
Ivovic, V., Patakakis, M., Tselentis, Y. and Chaniotis, B. (2007). Faunistic study of sandflies in Greece. Medical and Veterinary Entomology 21, 121124.Google ScholarPubMed
Jacobson, R. L., Eisenberger, C. L., Svobodova, M., Baneth, G., Sztern, J., Carvalho, J., Nasereddin, A., El Fari, M., Shalom, U., Volf, P., Votypka, J., Dedet, J. P., Pratlong, F., Schonian, G., Schnur, L. F., Jaffe, C. L. and Warburg, A. (2003). Outbreak of cutaneous leishmaniasis in northern Israel. Journal of Infectious Diseases 188, 10651073.Google ScholarPubMed
Lainson, R., Shaw, J. J., Silveira, F. T. and Braga, R. R. (1987). American visceral leishmaniasis: on the origin of Leishmania (Leishmania) chagasi . Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 517.CrossRefGoogle ScholarPubMed
Lainson, R., Dye, C., Shaw, J. J., Macdonald, D., Courtenay, O., Souza, A. A. and Silveira, F. T. (1990). Amazonian visceral leishmaniasis: distribution of the vector Lutzomyia longipalpis (Lutz & Neiva) in relation to the fox Cerdocyon thous (L.) and the efficiency of this reservoir host as a source of infection. Memorias do Instituto Oswaldo Cruz 85, 135137.CrossRefGoogle Scholar
Mancianti, F., Mignone, W. and Galastri, F. (1994). Serologic survey for leishmaniasis in free-living red foxes (Vulpes vulpes) in Italy. Journal of Wildlife Diseases 30, 454456.CrossRefGoogle ScholarPubMed
Minodier, P., Piarroux, R., Gambarelli, F., Joblet, C. and Dumon, H. (1997). Rapid identification of causative species in patients with Old World leishmaniasis. Journal of Clinical Microbiology 35, 25512555.CrossRefGoogle ScholarPubMed
Mohebali, M., Hajjaran, H., Hamzavi, Y., Mobedi, I., Arshi, S., Zarei, Z., Akhoundi, B., Naeini, K. M., Avizeh, R. and Fakhar, M. (2005). Epidemiological aspects of canine visceral leishmaniosis in the Islamic Republic of Iran. Veterinary Parasitology 129, 243251.CrossRefGoogle ScholarPubMed
Musabekov, K. S., Novak, M. D. and Farisova, O. M. (1997). The jackal, a potential source of leishmaniasis in southern and south-eastern Kazakhstan. Izvestiya Rossiiskoi Akademii Nauk – Seriya Biologicheskaya 4, 8687.Google Scholar
Ntais, P., Sifaki-Pistola, D., Christodoulou, V., Messaritakis, I., Pratlong, F., Poupalos, G. and Antoniou, M. (2013). Leishmaniases in Greece. American Journal of Tropical Medicine and Hygiene 89, 906915.CrossRefGoogle ScholarPubMed
Rhajaoui, M., Nasereddin, A., Fellah, H., Azmi, K., Amarir, F., Al-Jawabreh, A., Ereqat, S., Planer, J. and Abdeen, Z. (2007). New clinicoepidemiologic profile of cutaneous leishmaniasis, Morocco. Emerging Infectious Diseases 13, 13581360.CrossRefGoogle ScholarPubMed
Rioux, J. A., Albaret, J. L., Houin, R., Dedet, J. P. and Lanotte, G. (1968). Ecologie des leishmanioses dans le sud de la France. 2. Les reservoirs selvatiques. Infestation spontanee de renard (Vulpes vulpes L.). Annales De Parasitologie Humaine Et Comparee 43, 421428.CrossRefGoogle Scholar
Sastre, N., Francino, O., Ramirez, O., Ensenat, C., Sanchez, A. and Altet, A. (2008). Detection of Leishmania infantum in captive wolves from Southwestern Europe. Veterinary Parasitology 158, 117120.CrossRefGoogle ScholarPubMed
Schönian, G., Nasereddin, A., Dinse, N., Schweynoch, C., Schallig, H. D., Presber, W. and Jaffe, C. L. (2003). PCR diagnosis and characterization of Leishmania in local and imported clinical samples. Diagnostic Microbiology and Infectious Disease 47, 349358.CrossRefGoogle ScholarPubMed
Sobrino, R., Ferroglio, E., Oleaga, A., Romano, A., Millan, J., Revilla, M., Arnal, M., Trisciuoglio, M. C. and Gortazar, C. (2008). Characterization of widespread canine leishmaniasis among wild carnivores from Spain. Veterinary Parasitology 155, 198203.Google ScholarPubMed
Sukker, F. (1984). Epidemiology and control of visceral leishmaniasis in Iraq. Bull End Dis Iraq 26, 1326.Google Scholar
Talmi-Frank, D., Kedem-Vaanunu, N., King, R., Bar-Gal, G. K., Edery, N., Jaffe, C. L. and Baneth, G. (2010). Leishmania tropica infection in golden jackals and red foxes, Israel. Emerging Infectious Diseases 16, 19731975.Google ScholarPubMed
Verin, R., Poli, A., Ariti, G., Nardoni, S., Fanucchi, M. B. and Mancianti, F. (2010). Detection of Leishmania infantum DNA in tissues of free-ranging red foxes (Vulpes vulpes) in Central Italy. European Journal of Wildlife Research 56, 689692.Google Scholar
Xanthopoulou, K., Anagnostou, V., Ivović, V., Djurkovic-Djakovic, O., Rogozi, E., Sotiraki, S. and Papa, A. (2011). Distribution of sandflies (Diptera, Psychodidae) in two Ionian Islands and northern Greece. Vector-Borne and Zoonotic Diseases 11, 15911594.CrossRefGoogle ScholarPubMed