Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter January 17, 2018

Molecular and serological investigation of infectious diseases in captive and free-range crab-eating fox (Cerdocyon thous – Linnaeus, 1776) from northeastern Brazil

Jonatas C. Almeida, Renata P.B. Melo, Pomy C.P. Kim, Neurisvan R. Guerra, Leucio C. Alves, Diego F. Costa, Clebert José Alves, Wagnner J.N. Porto and Rinaldo A. Mota
From the journal Acta Parasitologica

Abstract

The aim of this study was to detect DNA and antibodies anti-Leishmania spp., Neospora caninum and Toxoplasma gondii in captive and free-range crab-eating fox (Cerdocyon thous) from northeastern Brazil. Twenty-five crab-eating foxes from different states of northeastern Brazil were sampled by this study. Blood samples were collected by cephalic or jugular vein punctures. The whole blood was submitted to PCR, and the sera samples to the serological analysis as follows: MAT for T. gondii, NAT for N. caninum, and ELISA for L. chagasi. The frequence of antibodies anti-T. gondii was 50% and 29.41% for free-range and captive wild canids, respectively. The frequence of antibodies anti-N. caninum observed by this study was 62.50% and 23.52% for free-range and captive wild canids, respectively. The frequence of antibodies anti-L. chagasi was 4.0% for captive wild canids. Co-infections cases were identified as follows: one captive wild canid seropositive for T. gondii and L. chagasi and two free-range animals seropositive for T. gondii and N. caninum. All PCR assays performed were negative for the pathogens analyzed. This study describes the presence of antibodies anti-T. gondii, N. caninum e L. chagasi in wild canids from northeastern Brazil and highlights the necessity of further studies on infectious diseases in free-range and captive wild canids.

References

Almeida A.P., Souza T.D., Marcili A., Labruna M.B., 2013. Novel Ehrlichia and Hepatozoon agents infecting the crabeating fox (Cerdocyon thous) in southeastern Brazil. Journal of Medical Entomology, 50, 640–646. PMID: 2380246110.1603/ME12272Search in Google Scholar

Almeida Curi N.H., Araújo A.S., Campos F.S., Lobato Z.I.P., Gennari S.M., Marvulo M.F.V., Silva J.C.R., Talamoni S.A., 2010. Wild canids, domestic dogs and their pathogens in Southeast Brazil: Disease threats for canid conservation. Biodiversity and Conservation, 19, 3513–3524. 10.1007/s10531-010-9911-0Search in Google Scholar

Almeida Curi N.H., Coelho C.M., Campos Cordeiro Malta M., Magni E.M., Sábato M.A., Araújo A.S., Lobato Z.I., Santos J.L., Santos H.A., Ragozo A.A., Souza S.L., 2012. Pathogens of wild maned wolves (Chrysocyon brachyurus) in Brazil. Journal of Wildlife Diseases, 48, 1052–1056. 10.7589/2011-10-304Search in Google Scholar PubMed

André M.R., Adania C.H., Teixeira R.H., Silva K.F., Jusi M.M., Machado S.T., Bortolli C.P., Falcade M., Sousa L., Alegretti S.M., Felippe P.A., Machado R.Z., 2010. Antibodies to Toxoplasma gondii and Neospora caninum in captive neotropical and exotic wild canids and felids. Journal of Parasitology, 96, 1007–1009. 10.1645/GE-2502.1Search in Google Scholar

Ashford R.W., 2000. The leishmaniases as emerging and reemerging zoonoses. International Journal for Parasitology, 30, 1269–1281. 10.1016/S0020-7519(00)00136-3Search in Google Scholar PubMed

Buxton D., Maley S.W., Pastoret P.P., Brochier B., Innes E.A., 1997. Examination of red fox (Vulpes vulpes) from Belgium for antibody to Neospora caninum and Toxoplasma gondii. Veterinary Record, 141, 308–309. PMID: 933047710.1136/vr.141.12.308Search in Google Scholar

Buxton D., Maley S.W., Wright S., Thomson K.M., Rae A.G., Innes E.A., 1998. The pathogenesis of experimental neosporosis in pregnant sheep. Journal of Comparative Pathology, 118. 267–279. PMID: 965180410.1016/S0021-9975(07)80003-XSearch in Google Scholar PubMed

Cañón-Franco W.A., Bergamaschi D.P., Labruna M.B., Camargo L. M.A., Souza S.L.P., Silva J.C.R., Pinter A., Dubey J.P., Gennari S.M., 2003. Prevalence of antibodies to Neospora caninum in dogs from Amazon, Brasil. Veterinary Parasitology, 115, 71–74. 10.1016/S0304-4017(03)00131-6Search in Google Scholar

Carnieli P.Jr., Castilho J.G., Fahl W.O., Véras N.M., Carrieri M. L., Kotait I., 2009. Molecular characterization of Rabies Virus isolates from dogs and crab-eating foxes in Northeastern Brazil. Virus Research, 141, 81–89. 10.1016/j.virusres.2008.12.015Search in Google Scholar PubMed

Carvalho M.R., Lima B.S., Marinho-Júnior J.F., Silva F.J., Valença H.F., Almeida F.de. A, Silva A.L., Brandão-Filho S.P., 2007. Phlebotomine sandfly species from an American visceral leishmaniasis area in the Northern Rainforest region of Pernambuco State, Brazil. Cadernos de Saúde Pública, 23, 1227–1232. 10.1590/S0102-311X2007000500024Search in Google Scholar PubMed

Catenacci L.S., Griese J., Silva R.C., Langoni H., 2010. Toxoplasma gondii and Leishmania spp. infection in captive crab-eating foxes, Cerdocyon thous (Carnivora, Canidae) from Brazil. Veterinary Parasitology, 169, 190–192. 10.1016/j.vetpar.2009.12.019Search in Google Scholar PubMed

Cortes S., Rolão N., Ramada J., Campino L., 2004. PCR as a rapid and sensitive tool in the diagnosis of human and canine leishmaniasis using Leishmania donovani s.l.-specific kinetoplastid primers. Transactions of the Royal Society of Tropical Medicine and Hygiene, 98, 12–17. PMID: 1470283410.1016/S0035-9203(03)00002-6Search in Google Scholar

Courtenay O., Santana E.W., Johnson P.J., Vasconcelos I.A., Vasconcelos A.W., 1996. Visceral leishmaniasis in the hoary zorro Dusicyon vetulus: a case of mistaken identity. Transactions of the Royal Society of Tropical Medicine and Hygiene, 90, 498–502. PMID: 894425410.1016/S0035-9203(96)90293-XSearch in Google Scholar PubMed

Courtenay O., Quinnell R.J., Garcez L.M., Shaw J.J., Dye C., 2002. Infectiousness in a cohort of Brazilian dogs: why culling fails to control visceral leishmaniasis in areas of high transmission. Journal of Infectious Diseases, 186, 1314–1320. 10.1086/344312Search in Google Scholar PubMed

Curi N.H., Miranda I., Talamoni S.A., 2006. Serologic evidence of Leishmania infection in free-ranging wild and domestic canids around a Brazilian National Park. Memórias do Instituto Oswaldo Cruz, 101, 99–101. 10.1590/S007402762006000100019Search in Google Scholar PubMed

Daszak P., Cunningham A.A., Hyatt A.D., 2000. Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science, 287, 443-449. 10.1126/science.287.5452.443Search in Google Scholar PubMed

Desmonts G., Remington J.S., 1980. Direct agglutination test for diagnosis of Toxoplasma infection: method for increasing sensitivity and specificity. Journal of Clinical Microbiology, 11, 562–568. PMCID: PMC27346110.1128/jcm.11.6.562-568.1980Search in Google Scholar PubMed PubMed Central

Dorneles E.M.S., Pellegrin A.O., Péres I.A.H.F.S., Mathias L.A., Mourão G., Bianchi R.C., Olifiers N., Rocha F.L., Lage A.P., 2014. Serology for brucellosis in free-ranging crab-eating foxes (Cerdocyon thous) and brown-nosed coatis (Nasua nasua) from Brazilian Pantanal. Ciência Rural, 44, 2193-2196. http://dx.doi.org/10.1590/0103-8478cr2013116710.1590/0103-8478cr20131167Search in Google Scholar

Dubey J.P., Jenkins M.C., Ferreira L.R., Choudhary S., Verma S.K., Kwok O.C., 2014. Isolation of viable Neospora caninum from brains of wild gray wolves (Canis lupus). Veterinary Parasitology, 201, 150–153. 10.1016/j.vetpar.2013.12.032Search in Google Scholar PubMed

Ferroglio E., Bosio F., Trisciuoglio A., Zanet S., 2014. Toxoplasma gondii in sympatric wild herbivores and carnivores: epidemiology of infection in the Western Alps. Parasite and Vectors, 7, 1:196. 10.1186/1756-3305-7-196Search in Google Scholar PubMed PubMed Central

Figueiredo F.B., Gremiao I.D., Pereira S.A., Fedulo L.P., Menezes R.C., Balthazar D.A., 2008. First report of natural infection of a bush dog (Speothos venaticus) with Leishmania (Leishmania) chagasi in Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene, 102, 200–201. 10.1016/j.trstmh.2007.10.001Search in Google Scholar PubMed

Fornazari F., Langoni H., 2014. Principais zoonoses em mamíferos selvagens. Veterinária e Zootecnia, 21, 10–24Search in Google Scholar

Gennari S.M., Canón-Franco W.A., Yai L.E.O., Souza S.L.P., Santos L.C., Farias N.A.R., Ruas J., Rossi F.W., Gomes A.A.B., 2004. Seroprevalence of Toxoplasma gondii antibodies from wild canids from Brazil. Veterinary Parasitology, 121, 337–340. 10.1016/j.vetpar.2004.02.023Search in Google Scholar PubMed

Hamilton C.M., Gray R., Wright S. E., Gangadharan B., Laurenson K., Innes E.A., 2005. Prevalence of antibodies to Toxoplasma gondii and Neospora caninum in red foxes (Vulpes vulpes) from around the U.K. Veterinary Parasitology, 130, 169–173. 10.1016/j.vetpar.2005.03.020Search in Google Scholar

Holsback L., Cardoso M.J., Fagnani R., Patelli T.H., 2013. Natural infection by endoparasites among free-living wild animals. Brazilian Journal of Veterinary Parasitology, 22, 302–306. 10.1590/S1984-29612013005000018Search in Google Scholar

Hurtado A., Aduriz G., Moreno B., Barandika J., García-Pérez A.L., 2001. Single tube nested PCR for the detection of Toxoplasma gondii in fetal tissues from naturally aborted ewes. Veterinary Parasitology, 102, 17–27. 10.1016/S0304-4017(01)00526-XSearch in Google Scholar PubMed

Jakubek E.B., Brojer C., Regnersen C., Uggla A., Schares G., Bjorkman C., 2001. Seroprevalences of Toxoplasma gondii and Neospora caninum in Swedish red foxes (Vulpes vulpes). Veterinary Parasitology, 102, 167–172. 10.1016/S03044017(01)00513-1Search in Google Scholar PubMed

Jusi M.M., Starke-Buzetti W.A., Oliveira T.M., Tenório M.S., Sousa L.O., Machado R.Z., 2011. Molecular and sorological detection of Leishmania sp. in captive wild animals from Ilha Solteira, SP, Brazil. Revista Brasileira de Parasitologia Veterinária, 20, 219–222. 10.1590/S1984-29612011000300008Search in Google Scholar

King A., Varughese P., De Serres G., Tipples G.A., Waters J., 2004. Measles elimination in Canada. Journal of Infectious Diseases, S236. 10.1086/378499Search in Google Scholar PubMed

Liu Q., Wang Z.D., Huang S.Y., Zhu X.Q., 2015. Diagnosis of toxoplasmosis and typing of Toxoplasma gondii. Parasite and Vectors, 8, 292. 10.1186/s13071-015-0902-6Search in Google Scholar PubMed PubMed Central

Lombardi M.C., Turchetti A.P., Tinoco H.P., Pessanha A.T., Soave S.A., Malta M.C.C., Paixão T.A., Santos R.L., 2014. Diagnosis of Leishmania infantum infection by Polymerase Chain Reaction in wild mammals. Pesquisa Veterinária Brasileira, 34, 1243–1246. 10.1590/S0100-736X2014001200017Search in Google Scholar

Mattos B.C., Patrício L.L.F., Plugge N.F.R., Lange R.R., Richartz R.R.T.B., Locatelli-Dittrich R., 2008. Soroprevaléncia de anticorpos anti-Neospora caninum e anti-Toxoplasma gondii em canídeos selvagens cativos. Revista Brasileira Parasitologia Veterinária, 17, 267–272. PMID: 20059860Search in Google Scholar

McAllister M., Wills R.A., McGuire A.M., Jolley W.R., Tranas J.D., Williams E.S., Lindsay D.S., Björkman C., Belden E.L., 1999. Ingestion of Neospora caninum tissue cysts by Mustela species. International Journal for Parasitology, 29, 1531–1536. PMID: 1060843910.1016/S0020-7519(99)00098-3Search in Google Scholar PubMed

Melo C.B., Leite R.C., Leite F.S.C., Leite R.C., 2002. Serological surveillance on South American wild canids for Neospora caninum. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 54, 444–447. 10.1590/S0102-09352002000400018Search in Google Scholar

Morse S.S. (Ed.). 1994. Emerging Viruses, Oxford University Press, USA, pp. 352Search in Google Scholar

Nascimento C.O., Silva M.L., Kim P.C.P, Gomes A.A., Gomes A.L., Maia R.C., Almeida J.C., Mota R.A. 2015. Occurrence of Neospora caninum and Toxoplasma gondii DNA in brain tissue from hoary foxes (Pseudalopex vetulus) in Brazil. Acta Tropica, 146, 60–65. 10.1016/j.actatropica.2015.02.016Search in Google Scholar PubMed

OIE – World Organisation for Animal Health. (Ed.) 2010. Training Manual on Wildlife Diseases and Surveillance, Office International des epizooties, FR, pp. 56Search in Google Scholar

Piantedosi D., Veneziano V., Di Muccio T., Manzillo F.V., Fiorentino E., Scalone A., Neola B., Di Prisco F., D’Alessio N., Gradoni L., Oliva G., Gramiccia M., 2016. Epidemiological survey on Leishmania infection in red foxes (Vulpes vulpes) and hunting dogs sharing the same rural area in Southern Italy. Acta Parasitologica, 61, 769–775. 10.1515/ap-2016-0106Search in Google Scholar PubMed

Proença L.M., Silva J.C.R., Galera P.D., Lion M.B., Marinho-Filho J.S., Ragozo A.M.A., Gennari S.M., Dubey J.P., Vasconcellos S.A., Souza G.O., Pinheiro-Junior J.W., Santana V.L.A., França G.L., Rodrigues F.H.G., 2013. Serologic survey of infectious diseases in populations of maned wolf (Chrysocyon brachyurus) and crab-eating fox (Cerdocyon thous) from Águas Emendadas Ecological Station, Brazil. Journal of Zoo and Wildlife Medicine, 44, 152–155. 10.1638/1042-7260-44.1.152Search in Google Scholar PubMed

Regidor-Cerrillo J., Arranz-Solís D., Benavides J., Gómez-Bautista M., Castro-Hermida J.A., Mezo M., Pérez V., Ortega-Mora L.M., González-Warleta M., 2014. Neospora caninum infection during early pregnancy in cattle: how they isolate influences infection dynamics, clinical outcome and peripheral and local immune responses. Veterinary Research, 45, 10. 10.1186/1297-9716-45-10Search in Google Scholar PubMed PubMed Central

Rodrigues T.C.S., Santos A.L.Q., Lima-Ribeiro A.M.C., Lemos F.G., Azevedo F.C., Arrais R.C., Gomes D.O., Tavares T.C.F., 2015. Occurrence of antibodies against Leptospira spp. in free-ranging wild canids from the Brazilian savanna. Pesquisa Veterinária Brasileira, 35, 734–740. 10.1590/S0100-736X2015000800005Search in Google Scholar

Romand S., Thulliez P., Dubey J.P., 1998. Direct agglutination test for serologic diagnose of Neospora caninum. Parasitology Research, 84, 50–53. PMID: 949142610.1007/s004360050355Search in Google Scholar PubMed

Ruas J.L., Muller G., Farias N.A.R., Gallina T., Lucas A.S., Pappen F.G., Sinkoc A.L., Brum J.G.W., 2008. Helminths of Pampas fox Pseudalopex gymnocercus (Fischer, 1814) and of Crabeating fox Cerdocyon thous (Linnaeus, 1766) in the Southern of the State of Rio Grande do Sul, Brazil. Brazilian Journal of Veterinary Parasitology, 17, 87–92. http://dx.doi.org/10.1590/S1984-2961200800020000510.1590/S1984-29612008000200005Search in Google Scholar PubMed

Santos J.L.C., Magalhães N.B., Santos H.A., Ribeiro R.R., Guimarães M.P., 2012. Parasites of domestic and wild canids in the region of Serra do Cipó National Park, Brazil. Revista Brasileira de Parasitologia Veterinária, 21, 270–277. 10.1590/S1984-29612012000300016Search in Google Scholar

Şuteu O., Mihalca A.D., Paştiu A.I., Györke A., Matei I.A., Ionică A., Balea A., Oltean M., D’Amico G., Sikó S.B., Ionescu D., Gherman C.M., Cozma V., 2014. Red foxes (Vulpes vulpes) in Romania are carriers of Toxoplasma gondii but not Neospora caninum. Journal of Wildlife Diseases, 50, 713–716. 10.7589/2013-07-167Search in Google Scholar PubMed

Taylor L.H., Latham S.M., Woolhouse M.E., 2001. Risk factors for human disease emergence. Philosophical Transactions of the Royal Society B: Biological Sciences, 356, 983–989. 10.1098/rstb.2001.0888Search in Google Scholar PubMed PubMed Central

Tenório M.S., Sousa L.O., Paixão M.S., Alves M.F., Paulan S.C., Lima F.L., Jusi M.M., Tasca K.I., Machado R.Z., Starke-Buzetti W.A., 2011. Visceral leishmaniasis in a captive crabeating fox Cerdocyon thous. Journal of Zoo and Wildlife Medicine, 42, 608–616. 10.1638/2010-0245.1Search in Google Scholar PubMed

Vitaliano S.N., Silva D.A.O., Mineo T.W.P., Ferreira R.A., Bevilacqua E., Mineo J.R., 2004. Seroprevalence of Toxoplasma gondii and Neospora caninum in captive maned wolves (Chrysocyon brachyurus) from southeastern and midwestern regions of Brazil. Veterinary Parasitology, 122, 253–260. 10.1016/j.vetpar.2004.04.004Search in Google Scholar PubMed

Zarnke R.L., Dubey J.P., Kwok O.C., Ver Hoef J.M., 2000. Serologic survey for Toxoplasma gondii in selected wildlife species from Alaska. Journal of Wildlife Diseases, 36, 219–224. 10.7589/0090-3558-36.2.219Search in Google Scholar PubMed

Zimpel C.K., Grazziotin A.L., Barros-Filho I.R., Guimaraes A.M.S., Santos L.C., Moraes W., Cubas Z.S., Oliveira M.J., Pituco E.M., Lara M.C.C.S.H., Villalobos E.M.C., Silva L.M.P., Cunha E.M.S., Castro V., Biondo A.W., 2015. Occurrence of antibodies anti-Toxoplasma gondii, Neospora caninum and Leptospira interrogans in a captive deer herd in Southern Brazil. Brazilian Journal of Veterinary Parasitology, 24, 482–487. 10.1590/S1984-29612015065Search in Google Scholar PubMed

Williams E.S., Yuill T., Artois M., Fischer J., Haigh S.A., 2002. Emerging infectious diseases in wildlife. Revue Scientifique Et Technique, 21, 139–157. PMID: 1197462510.20506/rst.21.1.1327Search in Google Scholar PubMed

Woolhouse M.E.J., Taylor L.H., Haydon D.T., 2001. Population biology of multi-host pathogens. Science, 292, 1109–1112. 10.1126/science.1059026Search in Google Scholar PubMed

Woolhouse M.E.J., Gowtage-Sequeria S., 2005. Host Range and Emerging and Reemerging Pathogens. Emerging Infectious Diseases, 11, 1842–1847. 10.3201/eid1112.050997Search in Google Scholar PubMed PubMed Central

Received: 2017-3-19
Revised: 2017-10-31
Accepted: 2017-11-20
Published Online: 2018-1-17
Published in Print: 2018-3-26

© 2018 W. Stefański Institute of Parasitology, PAS