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Acta Parasitologica

, Volume 61, Issue 4, pp 769–775 | Cite as

Epidemiological survey on Leishmania infection in red foxes (Vulpes vulpes) and hunting dogs sharing the same rural area in Southern Italy

  • Diego Piantedosi
  • Vincenzo Veneziano
  • Trentina Di Muccio
  • Valentina Foglia ManzilloEmail author
  • Eleonora Fiorentino
  • Aldo Scalone
  • Benedetto Neola
  • Francesca Di Prisco
  • Nicola D’Alessio
  • Luigi Gradoni
  • Gaetano Oliva
  • Marina Gramiccia
Article

Abstract

Southern Italy, particularly Campania region, is an area where canine leishmaniasis (CanL) and zoonotic human visceral leishmaniasis (VL) are endemic. The red fox (Vulpes vulpes) has been hypothesized to play a role in occurrence of CanL in Italy but specific studies are poor. The aim of the present survey was to investigate the prevalence of Leishmania infection in dogs and foxes living in the same rural area (Picentini hills). 123 sera from autochthonous fox-hunting dogs were examined by immunofluorescent-antibody test (IFAT) using a cut-off of 1:160. The seroprevalence of dogs examined was 17.9%. Moreover, 48 foxes were examined after having been shooted by hunters or road accidents. Spleen, liver and lymph node samples were analyzed by specific Leishmania nested PCR (n-PCR). 10 foxes were found infected by L. infantum (20.8%) of which 4 animals in spleen, 2 in lymph nodes and 4 both in spleen and lymph nodes. The overall n-PCR positivity was 17.4% for spleen samples and 13.3% for lymph nodes; all liver samples resulted negative. In positive PCR foxes no signs clearly referable to leishmaniasis were recorded at necropsy. The results confirmed the presence of L. infantum infection in red foxes from Southern Italy, with a moderate level of exposure. Because a large proportions of dogs with ascertained progressive leishmaniasis show a prolonged “subpatent condition” during which they are only positive to n-PCR before seroconversion, our results allow to assume that exposure risk in foxes is lower than hunting dogs living in the studied area.

Keywords

Leishmaniasis Italy fox hunting dog 

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References

  1. Adler S., Theodor O. 1932. Investigations on Mediterranean Kala Azar. VI. — Canine Visceral Leishmaniasis. Proceedings of the Royal Society of London B Biological Sciences, 110, 402–412. DOI: 10.1098/rspb.1932.0035CrossRefGoogle Scholar
  2. Alvar J., Vélez I.D., Bern C., Herrero M., Desjeux P., Cano J., Jannin J., den Boer M. 2012. Leishmaniasis worldwide and global estimates of its incidence. World Health Organization Leishmaniasis Control Team. PLoS One, 7(5):e35671. DOI: 10.1371/journal.pone.0035671CrossRefGoogle Scholar
  3. Bongiorno G., Paparcone R., Foglia Manzillo V., Oliva G., Cuisinier A.M., Gradoni L. 2013. Vaccination with LiESP/QA-21 (CaniLeish®) reduces the intensity of infection in Phlebotomus perniciosus fed on Leishmania infantum infected dogs — a preliminary xenodiagnosis study. Veterinary Parasitology, 197, 691–695. DOI: 10.1016/j.vetpar.2013.05.008CrossRefGoogle Scholar
  4. Cardoso L., Cortes H.C.E., Reis A., Rodrigues P., Simôes M., Lopes A.P., Vila-Viçosa M.J., Talmi-Frank D., Eyal O., Solano-Gallego L., Baneth G. 2013. Prevalence of Babesia microti-like infection in red foxes (Vulpes vulpes) from Portugal. Veterinary Parasitology, 19, 90–95. DOI:10.1016/j.vetpar.201212.00CrossRefGoogle Scholar
  5. Cavallini P. 2001. (Ed). La Volpe. In: (Eds. A.M. Simonetta and F. Dessi-Fulgheri) Principi e tecniche di gestione faunisticovenatoria, Greentime Publishing, Bologna, Italy, 330–342 (In Italian)Google Scholar
  6. Courtenay O., Carson C., Calvo-Bado L., Garcez L.M., Quinnell R.J. 2014. Heterogeneities in Leishmania infantum infection: using skin parasite burdens to identify highly infectious dogs. PLoS Neglected Tropical Diseases, 8, e2583. DOI: 10.1371/journal.pntd.0002583CrossRefGoogle Scholar
  7. Criado-Fornelio A., Gutierrez-Garcia L., Rodriguez-Caabeiro F., Reus-Garcia E., Roldan-Soriano M.A., Diaz-Sanchez M.A. 2000. A parasitological survey of wild red foxes (Vulpes vulpes) from the province of Guadalajara, Spain. Veterinary Parasitology, 92, 245–251. DOI: 10.1016/S0304-4017(00)00329-0CrossRefGoogle Scholar
  8. Davoust B., Mary C., Marié J.L. 2014. Detection of Leishmania in red foxes (Vulpes vulpes) from southeastern France using realtime quantitative PCR. Journal of Wildlife Diseases, 50, 130–132. DOI: 10.7589/2013-07-190CrossRefGoogle Scholar
  9. Di Muccio T., Veronesi F., Antognoni M.T., Onofri A., Piergili Fioretti D., Gramiccia M. 2012. Diagnostic value of conjunctival swab sampling associated with nested PCR for different categories of dogs naturally exposed to Leishmania infantum infection. Journal ofClinical Microbiology, 50, 2651–2659. DOI: 10.1128/JCM.00558-12CrossRefGoogle Scholar
  10. Dipineto L., Manna L., Baiano A., Gala M., Fioretti A., Gravino A.E., Menna L.F. 2007. Presence of Leishmania infantum in red foxes (Vulpes vulpes) in southern Italy. Journal of Wildlife Diseases, 43, 518–520. DOI: 10.7589/0090-3558-43.3.518CrossRefGoogle Scholar
  11. Duscher G.G., Leschnik M., Fuehrer H.P., Joachim A. 2015. Wildlife reservoirs for vector-borne canine, feline and zoonotic infections in Austria. International Journal for Parasitology: Parasites and Wildlife, 4, 88–89. DOI: 10.1016/j.ijppaw.2014.12.001PubMedGoogle Scholar
  12. Foglia Manzillo V, Di Muccio T., Cappiello S., Scalone A., Paparcone R., Fiorentino E., Gizzarelli M., Gramiccia M., Gradoni L., Oliva G., 2013. Prospective study on the incidence and progression of clinical signs in naïve dogs naturally infected by Leishmania infantum. PLoS Neglected Tropical Diseases, 7, e225. DOI: 10.1371/journal.pntd.0002225CrossRefGoogle Scholar
  13. Gradoni L., Gramiccia M. 2000. Leishmaniasis. In: OIE manual of standards for diagnostic tests and vaccine. Office International des Epizooties, Paris, France, 2000 pp. 803–812Google Scholar
  14. Gramicciactive analysis of the multi-annual epidemic that occurred from 1989 to 2009. Eurosurveillance, 18(29):pii=20535. DOI: 10.2807/1560-7917.ES2013.18.28.20535Google Scholar
  15. Hodžič A., Alic 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 & Vectors, 8:88. DOI: 10.1186/s13071-015-0692-xCrossRefGoogle Scholar
  16. Karayiannis S., Ntais P., Messaritakis I., Tsirigotakis N., Dokianakis E., Antoniou M. 2015. Detection of Leishmania infantum in red foxes (Vulpes vulpes) in Central Greece. Parasitology, 142, 1574–1578. DOI: 10.1017/S0031182015001158CrossRefGoogle Scholar
  17. Mackenstedt U., Jenkins D., Romig T. 2015. The role of wildlife in the transmission of parasitic zoonoses in peri-urban and urban areas. International Journal for Parasitology: Parasites and Wildlife, 4, 71–79. DOI: 10.1016/j.ijppaw.2015.01.006PubMedGoogle Scholar
  18. Maroli M., Gramiccia M., Gradoni L., Troiani M., Ascione R. 1994. Natural infection of Phlebotomus perniciosus with MON 72 zymodeme of Leishmania infantum in the Campania region of Italy. Acta Tropica, 57, 333–335. DOI:10.1016/0001 - 706X(94)90079-5CrossRefGoogle Scholar
  19. Michel G., Pomares C., Ferrua B., Marty P. 2011. Importance of worldwide asymptomatic carriers of Leishmania infantum (L. chagasi) in human. Acta Tropica, 119, 69–75: DOI: 10.1016/j.actatropica.2011.05.012CrossRefGoogle Scholar
  20. Millán J., Ferroglio E., Solano-Gallego L. 2014. Role of wildlife in the epidemiology of Leishmania infantum infection in Europe. Parasitology Research, 113, 2005–2014: DOI: 10.1007/s00436 - 014-3929-2CrossRefGoogle Scholar
  21. Mohammad N.S.A., Halasa T., Kapel C.M.O. 2014. Infections with cardiopulmonary and intestinal helminths and sacrcoptic mange in red foxes from two different localities in Denmark. Acta Parasitologica, 59, 98–107. DOI: 10.2478/s11686-014-0214-6Google Scholar
  22. Moreno J., Alvar J. 2002. Canine leishmaniasis: epidemiological risk and the experimental model. Trends in Parasitology, 18, 399–405. DOI: 10.1016/S1471-4922(02)02347-4CrossRefGoogle Scholar
  23. Oliva G., Scalone A., Foglia Manzillo V., Gramiccia M., Pagano A., Di Muccio T., Gradoni L. 2006. Incidence and time course of Leishmania infantum infections examined by parasitological, serologic, and nested-PCR techniques in a cohort of naive dogs exposed to three consecutive transmission seasons. Journal of Clinical Microbiology, 44, 1318–1322. DOI: 10.1128/JCM.44.4.1318-1322.2006CrossRefGoogle Scholar
  24. Otranto D., Cantacessi C., Pfeffer M., Dantas-Torres F., Brianti E., Deplazes P., Genchi C., Guberti V., Capelli G. 2015. The role of wild canids and felids in spreading parasite to dogs and cats in Europe. Part I: Protozoa and tick-borne agents. Veterinary Parasitology, 213, 12–23. DOI: 10.1016/j.vetpar.2015.04.022CrossRefGoogle Scholar
  25. Paltrinieri S., Solano-Gallego L., Fondati A., Lubas G., Gradoni L., Castagnaro M., Crotti A., Maroli M., Oliva G., Roura X., Zatelli A., Zini E. 2010. Guidelines for diagnosis and clinical classification of leishmaniasis in dogs. Canine Leishmaniasis Working Group, Italian Society of Veterinarians of Companion Animals. Journal of the American Veterinary Medical Association, 236, 1184–1191. DOI: 10.2460/javma.236.11.1184CrossRefGoogle Scholar
  26. Plummer L., Davison J., Saarma U. 2014. Rapid urbanization of red foxes in Estonia: distribution, behaviour, attacks on domestic animals, and health-risks related to zoonotic diseases. PLoS One, 96(12): e115124. DOI: 10.1371/journal.pone.0115124CrossRefGoogle Scholar
  27. Roulichovà J., Andera M., 2007. Simple method of age determination in red fox, Vulpes vulpes. Folia Zoologica, 56, 440–444Google Scholar
  28. Rosypal A.C., Troy G.C., Zajac A.M., Frank G., Lindsay D.S. 2005. Transplacental transmission of a north american isolate of Leishmania infantum in an experimentally infected beagle. Journal of Parasitology, 91, 970–972. DOI: 10.1645/GE-483R.1CrossRefGoogle Scholar
  29. Quinnell R.J, Courtenay O. 2009. Transmission, reservoir hosts and control of zoonotic visceral leishmaniasis. Parasitology, 136, 1915–1934. DOI: 10.1017/S0031182009991156CrossRefGoogle Scholar
  30. Santoro M., D’Alessio N., Di Prisco F., Neola B., Restucci B., Pagano T.B., Veneziano V. 2015. Angiostrongylus vasorum infection in red foxes (Vulpes vulpes) in southern Italy. Acta Parasitologica, 60, 356–359. DOI: 10.1015/ap-2015-0050CrossRefGoogle Scholar
  31. Scott D.M., Berg M.J., Tolhurst B.A., Chauvenet A.L., Smith G.C., Neaves K., Lochhead J., Baker PJ. Changes in the distribution of red foxes (Vulpes vulpes) in urban areas in Great Britain: findings and limitations of a media-driven nationwide survey. PLoS One, 9, e99059. DOI: 10.1371/journal.pone.0099059.CrossRefGoogle Scholar
  32. Souza T.D., Turchetti A.P., Toshio Fujiwara T., Alves Paixäo T., Lima Santos R. 2014. Visceral leishmaniasis in zoo and wildlife. Veterinary Parasitology, 200, 233-24. DOI: 10.1016/j.vetpar.2013.12.025CrossRefGoogle Scholar
  33. 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, 645–648. DOI: 10.1016/j.ttbdis.2015.05.009CrossRefGoogle Scholar
  34. van Eyes G.J., Schoone G.J., Kroon N.C., Ebeling S.B. 1992. Sequence analysis of small subunit ribosomal RNA genes and its use for detection and identification of Leishmania parasites. Molecular and Biochemical Parasitology, 51, 133–142. DOI: 10.1016/0166-6851(92)90208-2CrossRefGoogle Scholar
  35. Verin R., Polia A., Ariti G., Nardoni S., Fanucchi Bertucelli M., Mancianti F. 2010. Detection of Leishmania infantum DNA in tissue of free-ranging red foxes (Vulpes vulpes) in Central Italy. European Journal of Wildlife Research, 56, 689–692. DOI: 10.1007/s10344-010-0395-8CrossRefGoogle Scholar

Copyright information

© Witold Stefański Institute of Parasitology, Polish Academy of Sciences 2016

Authors and Affiliations

  • Diego Piantedosi
    • 1
  • Vincenzo Veneziano
    • 1
  • Trentina Di Muccio
    • 2
  • Valentina Foglia Manzillo
    • 1
    Email author
  • Eleonora Fiorentino
    • 2
  • Aldo Scalone
    • 2
  • Benedetto Neola
    • 1
  • Francesca Di Prisco
    • 3
  • Nicola D’Alessio
    • 3
  • Luigi Gradoni
    • 2
  • Gaetano Oliva
    • 1
  • Marina Gramiccia
    • 2
  1. 1.Department of Veterinary Medicine and Animal ProductionsUniversity of Naples Federico IINaplesItaly
  2. 2.Unit of Vector-borne Diseases and International Health, MIPIIstituto Superiore di SanitàRomeItaly
  3. 3.Istituto Zooprofilattico del MezzogiornoSezione Diagnostica Provinciale di AvellinoMonteforte IrpinoItaly

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