Histopathological findings of infections caused by canine distemper virus, Trypanosoma cruzi, and other parasites in two free-ranging White-nosed Coatis Nasua narica (Carnivora: Procyonidae) from Costa Rica

Main Article Content

Jorge Rojas-Jiménez
https://orcid.org/0000-0002-5664-6359
Juan A. Morales-Acuña
Milena Argüello-Sáenz
https://orcid.org/0000-0001-9156-5936
Silvia E. Acevedo-González
https://orcid.org/0000-0001-5238-194X
Michael J. Yabsley
https://orcid.org/0000-0003-2452-5015
Andrea Urbina-Villalobos
https://orcid.org/0000-0002-9001-761X

Abstract

Canine distemper virus (CDV) causes systemic infections and immunosuppression in carnivores, which subsequently makes animals highly susceptible to opportunistic infections.  Although Trypanosoma cruzi infects procyonids, chagasic myocarditis in Coatis has not been reported in Central America.  The aim of this study was to report the histopathological findings caused by canine distemper virus, T. cruzi, and other parasites in two free-ranging White-nosed Coatis Nasua narica found dead in a national park on the Pacific coast of Costa Rica.  Heart, lung, tongue, liver, brain and spleen samples were subjected to macroscopic and microscopic examination.  A mononuclear meningoencephalitis associated with intra-nuclear eosinophilic inclusion bodies consistent with canine distemper virus was observed in nervous tissue.  Myocarditis and associated nests of amastigotes of T. cruzi were observed during microscopic examination in cardiac tissue, and in muscle from the tongue of both animals. Molecular analysis confirmed T. cruzi in formalin-fixed paraffin embedded cardiac tissues.  The myocardial damage caused by the opportunistic infection due to T. cruzi in these individuals could be the result of a severe compromised immunological status associated to the CDV infection, and subsequent opportunistic polyparasitism described herein.  To the authors knowledge this is the first report of chagasic myocarditis in free-ranging coatis from Central America. 


 

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[1]
Rojas-Jiménez, J., Morales-Acuña, J.A., Argüello-Sáenz, M., Acevedo-González, S.E., Yabsley, M.J. and Urbina-Villalobos, A. 2021. Histopathological findings of infections caused by canine distemper virus, Trypanosoma cruzi, and other parasites in two free-ranging White-nosed Coatis Nasua narica (Carnivora: Procyonidae) from Costa Rica. Journal of Threatened Taxa. 13, 1 (Jan. 2021), 17521–17528. DOI:https://doi.org/10.11609/jott.5907.13.1.17521-17528.
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Short Communications

References

Alves, F.M., J.S. de Lima, F.L. Rocha, H.M. Herrera, G.de.M. Mourão & A.M. Jansen (2016). Complexity and multi-factoriality of Trypanosoma cruzi sylvatic cycle in coatis, Nasua nasua (Procyonidae), and triatomine bugs in the Brazilian Pantanal. Parasites & Vectors 9(1): 378. https://doi.org/10.1186/s13071-016-1649-4

Alves, F.M., N. Olifiers, R.D.C. Bianchi, A.C. Duarte, P.M.T. Cotias, P.S. D’Andrea, M.E. Gompper, G.de.M. Mourão, H.M. Herrera & A.M. Jansen (2011). Modulating variables of Trypanosoma cruzi and Trypanosoma evansi transmission in free-ranging coati (Nasua nasua) from the Brazilian Pantanal Region. Vector-Borne and Zoonotic Diseases 11(7): 835–841. https://doi.org/10.1089/vbz.2010.0096

Anderson, R.C., A.G. Chabaud & S. Willmott (Eds.) (2009). Keys to the Nematode Parasites of Vertebrates. Archival Volume. CAB International, Wallingford, UK, 463pp.

Araujo Carreira, J.C., A.M. Jansen, M.P. Deane & H.L. Lenzi (1996). Histopathological study of experimental and natural infections by Trypanosoma cruzi in Didelphis marsupialis. Memorias Do Instituto Oswaldo Cruz 91(5): 609–618. https://doi.org/10.1590/S0074-02761996000500012

Avendaño, R., F. Barrueta, S. Soto-Fournier, M. Chavarría, O. Monge, G.A. Gutiérrez-Espeleta & A. Chaves (2016). Canine Distemper Virus in Wild Felids of Costa Rica. Journal of Wildlife Diseases 52(2): 373–377. https://doi.org/10.7589/2015-02-041

Barr, S.C., K.A. Gossett & T.R. Klei (1991). Clinical, clinicopathologic, and parasitologic observations of trypanosomiasis in dogs infected with North American Trypanosoma cruzi isolates. American Journal of Veterinary Research 52(6): 954–960.

Barrera, Y.K., J.M. Guevara, P.X. Pavía, M. Montilla, R.S. Nicholls, E. Parra & C.J. Puerta (2008). Evaluación de las pruebas de PCR TcH2AF-R y S35-S36 para la detección de Trypanosoma cruzi en tejido cardiaco de ratón. Biomedica 28: 616–626. https://doi.org/10.7705/biomedica.v28i4.68

Calvopiña, M., D. Romero, B. Castañeda, Y. Hashiguchi & H. Sugiyama (2014). Current status of Paragonimus and paragonimiasis in Ecuador. Memorias Do Instituto Oswaldo Cruz 109(7): 849–855. https://doi.org/10.1590/0074-0276140042

Chinchilla, M. (1966). Hallazgo de dos nuevos reservorios de la Enfermedad de Chagas en Costa Rica. Acta Médica Costarricense 9(3): 165–166.

Cuarón, A.D., K. Helgen, F. Reid, J. Pino & J.F. González-Maya (2016). Nasua narica. The IUCN Red List of Threatened Species 2016: e.T41683A45216060. https://doi.org/10.2305/IUCN.UK.2016-1.RLTS.T41683A45216060.en

Curtis-Robles, R., B.C. Lewis & S.A. Hamer (2016). High Trypanosoma cruzi infection prevalence associated with minimal cardiac pathology among wild carnivores in central Texas. International Journal for Parasitology: Parasites and Wildlife 5: 117–123. https://doi.org/10.1016/j.ijppaw.2016.04.001

de Lima, J.S., F.L. Rocha, F.M. Alves, E.S. Lorosa, A.M. Jansen & G.de.M. Mourão (2015). Infestation of arboreal nests of coatis by triatomine species, vectors of Trypanosoma cruzi, in a large Neotropical wetland. Journal of Vector Ecology 40(2): 379–385. https://doi.org/10.1111/jvec.12177

Deem, S.L., L.H. Spelman, R.A. Yates & R.J. Montali (2000). Canine Distemper in Terrestrial Carnivores: a Review. Journal of Zoo and Wildlife Medicine 31(4): 441–451. https://doi.org/10.1638/1042-7260(2000)031[0441:CDITCA]2.0.CO;2

Dorn, P.L., A.G. McClure, M.D. Gallaspy, E. Waleckx, A.S. Woods, M.C. Monroy & L. Stevens (2017). The diversity of the Chagas parasite, Trypanosoma cruzi, infecting the main Central American vector, Triatoma dimidiata, from Mexico to Colombia. PLoS Neglected Tropical Diseases 11(9): 1–15. https://doi.org/10.1371/journal.pntd.0005878

Duarte Moraes, M.F., M.X. da Silva, P.C. Magalhães-Matos, A.C.A. de Albuquerque, J.H. Tebaldi, L.A. Mathias & E.G. Lux Hoppe (2017). Filarial nematodes with zoonotic potential in ring-tailed coatis (Nasua nasua Linnaeus, 1766, Carnivora: Procyonidae) and domestic dogs from Iguaçu National Park, Brazil. Veterinary Parasitology: Regional Studies and Reports 8: 1–9. https://doi.org/10.1016/j.vprsr.2017.01.003

Dubey, J.P., J.A. Morales, D. Leandro & B.M. Rosenthal (2008). Molecular Phylogeny Implicates New World Opossums (Didelphidae) as the Definitive Hosts of Sarcocystis ramphastosi, a Parasite of the Keel-billed Toucan (Ramphastos sulfuratus). Acta Protozoologica 47: 55–61.

Ferrer, E. (2015). Técnicas Moleculares para el diagnóstico de la Enfermedad de Chagas. Saber, Universidad de Oriente, Venezuela. 27(3): 359–371.

Furtado, M.M., E.M.K. Hayashi, S.D. Allendorf, C.J. Coelho, A.T. de Almeida Jácomo, J. Megid, J.D. Ramos-Filho, L. Silveira, N. Mundim-Tôrres & J.S. Ferreira Neto (2016). Exposure of Free-Ranging Wild Carnivores and Domestic Dogs to Canine Distemper Virus and Parvovirus in the Cerrado of Central Brazil. EcoHealth 13: 549–557. https://doi.org/10.1007/s10393-016-1146-4

Hass, C.C. & D. Valenzuela (2002). Anti-predator benefits of group living in white-nosed coatis (Nasua narica). Behavioral Ecology and Sociobiology 51: 570–578. https://doi.org/10.1007/s00265-002-0463-5

Hernández-Chea, R., A.E. Jiménez-Rocha, R. Castro, D. Blair & G. Dolz (2017). Morphological and molecular characterization of the metacercaria of Paragonimus caliensis, as a separate species from P. mexicanus in Costa Rica. Parasitology International 66(2): 126–133. https://doi.org/10.1016/j.parint.2016.12.006

Herrera, L. (2010). Una revisión sobre reservorios de Trypanosoma (Schizotrypanum) cruzi (Chagas, 1909), agente etiológico de la Enfermedad de Chagas. Boletín de Malariología y Salud Ambiental 50(1): 1–14.

Hutter, S.E., K. Brugger, V.H. Sancho Vargas, R. González, O. Aguilar, B. León, A. Tichy, C.L. Firth & F. Rubel (2016). Rabies in Costa Rica: Documentation of the Surveillance Program and the Endemic Situation from 1985 to 2014. Vector-Borne and Zoonotic Diseases 16(5): 334–341. https://doi.org/10.1089/vbz.2015.1906

Kapil, S. & T.J. Yeary (2011). Canine Distemper Spillover in Domestic Dogs from Urban Wildlife. Veterinary Clinics: Small Animal Practice 41(6): 1069–1086. https://doi.org/10.1016/j.cvsm.2011.08.005

Kubiski, S. V., S. Sisó, M.E. Church, A.N. Cartoceti, B. Barr & P.A. Pesavento (2016). Unusual Necrotizing Encephalitis in Raccoons and Skunks Concurrently Infected With Canine Distemper Virus and Sarcocystis sp. Veterinary Pathology 53(3): 674–676. https://doi.org/10.1177/0300985815603430

Lainson, R. (1965). Parasitological studies in British Honduras. Annals of Tropical Medicine and Parasitology 59(1): 37–42. https://doi.org/10.1080/00034983.1965.11686279

Martinez-Gutierrez, M. & J. Ruiz-Saenz (2016). Diversity of susceptible hosts in canine distemper virus infection: a systematic review and data synthesis. BMC Veterinary Research 12(1): 1–11. https://doi.org/10.1186/s12917-016-0702-z

Martínez-Hernández, F., O. López-Díaz, R. Bello-Bedoy, G. Villalobos, C.I. Muñoz-García, R. Alejandre-Aguilar, A. Córdoba-Aguilar, A.E. Gutiérrez-Cabrera, G. Suzán, C. Villanueva-García, L.M. Gama-Campillo, M.T. Díaz-Negrete & E. Rendón-Franco (2016). Possible Differences in the Effects of Trypanosoma cruzi on Blood Cells and Serum Protein of Two Wildlife Reservoirs. Vector-Borne and Zoonotic Diseases 16(11): 709–716. https://doi.org/10.1089/vbz.2016.1986

Mehrkens, L.R., L.A. Shender, M.J. Yabsley, B.C. Shock, F.A. Chinchilla, J. Suarez & K.V.K. Gilardi (2013). White-Nosed Coatis (Nasua narica) Are a Potential Reservoir of Trypanosoma cruzi and Other Potentially Zoonotic Pathogens in Monteverde, Costa Rica. Journal of Wildlife Diseases 49(4): 1014–1018. https://doi.org/10.7589/2013-01-005

Mena-Marín, A.L., R. Zeledón, J.A. Morales, M. Pereira & A. Urbina (2012). Influencia del sexo en la susceptibilidad de ratones Swiss a Trypanosoma cruzi. Boletín de Malariología y Salud Ambiental 52(2): 233–244.

Michelazzo, M.deM.Z., T.E.S. de Oliveira, N.E. Viana, W. de Moraes, Z.S. Cubas & S.A. Headley (2020). Immunohistochemical evidence of canine morbillivirus (canine distemper) infection in coatis (Nasua nasua) from Southern Brazil. Transboundary and Emerging Diseases 00: 1–7. https://doi.org/10.1111/tbed.13456

Montenegro, V.M., M.C. Bonilla, D. Kaminsky, J.J. Romero-Zúñiga, S. Siebert & F. Krämer (2017). Serological detection of antibodies to Anaplasma spp., Borrelia burgdorferi sensu lato and Ehrlichia canis and of Dirofilaria immitis antigen in dogs from Costa Rica. Veterinary Parasitology 236: 97–107. https://doi.org/10.1016/j.vetpar.2017.02.009

Morales, E.A., P. Mayor, M. Bowler, E. Aysanoa, E.S. Pérez-Velez, J. Pérez, J.A. Ventocilla, G.C. Baldeviano & A.G. Lescano (2017). Prevalence of Trypanosoma cruzi and Other Trypanosomatids in Frequently-Hunted Wild Mammals from the Peruvian Amazon. American Journal of Tropical Medicine and Hygiene 97(5): 1482–1485. https://doi.org/10.4269/ajtmh.17-0028

Origgi, F.C., P. Plattet, U. Sattler, N. Robert, J. Casaubon, F. Mavrot, M. Pewsner, N. Wu, S. Giovannini, A. Oevermann, M.H. Stoffel, V. Gaschen, H. Segner & M.P. Ryser-Degiorgis (2012). Emergence of Canine Distemper Virus Strains With Modified Molecular Signature and Enhanced Neuronal Tropism Leading to High Mortality in Wild Carnivores. Veterinary Pathology 49(6): 913–929. https://doi.org/10.1177/0300985812436743

Rentería-Solís, Z., C. Förster, A. Aue, U. Wittstatt, G. Wibbelt & M. König (2014). Canine distemper outbreak in raccoons suggests pathogen interspecies transmission amongst alien and native carnivores in urban areas from Germany. Veterinary Microbiology 174: 50–59. https://doi.org/10.1016/j.vetmic.2014.08.034

Rocha, F.L., A.L.R. Roque, J.S. de Lima, C.C. Cheida, F.G. Lemos, F.C. de Azevedo, R. Corassa-Arrais, D. Bilac, H. Miraglia-Herrera, G.de.M. Mourão & A.M. Jansen (2013). Trypanosoma cruzi Infection in Neotropical Wild Carnivores (Mammalia: Carnivora): At the Top of the T. cruzi Transmission Chain. PLoS ONE 8(7): e67463. https://doi.org/10.1371/journal.pone.0067463

Roellig, D.M., A.E. Ellis & M.J. Yabsley (2009). Genetically different isolates of Trypanosoma cruzi elicit different infection dynamics in raccoons (Procyon lotor) and Virginia opossums (Didelphis virginiana). International Journal for Parasitology 39: 1603–1610. https://doi.org/10.1016/j.ijpara.2009.06.007

Santoro, M., A. Alfaro-Alarcón, V. Veneziano, A. Cerrone, M.S. Latrofa, D. Otranto, I. Hagnauer, M. Jiménez & G. Galiero (2016). The White-nosed Coati (Nasua narica) is a naturally susceptible definitive host for the zoonotic nematode Angiostrongylus costaricensis in Costa Rica. Veterinary Parasitology 228: 93–95. https://doi.org/10.1016/j.vetpar.2016.08.017

Schofield, C.J. (2000). Trypanosoma cruzi - The Vector-parasite Paradox. Memórias Do Instituto Oswaldo Cruz 95(4): 535–544.

Taques, I.I.G.G., T.O. Morgado, Í.A. Braga, R.C.R. Paz, S.H.R. Corrêa, J.T.T. Fritzen, A.A. Alfieri & D.M. Aguiar (2018). Antibodies against canine distemper virus, parvovirus and Ehrlichia spp. in wild captive carnivores in midwestern Brazil. Brazilian Journal of Veterinary Research 38(8): 1681–1684. https://doi.org/10.1590/1678-5150-pvb-5333

Vallejo, G.A., F. Guhl, E. Chiari & A.M. Macedo (1999). Species specific detection of Trypanosoma cruzi and Trypanosoma rangeli in vector and mammalian hosts by polymerase chain reaction amplification of kinetoplast minicircle DNA. Acta Tropica 72: 203–212. https://doi.org/10.1016/S0001-706X(98)00085-0

Vallejo, G.A., Y. Suárez, J.L. Olaya, S.A. Gutierrez & J.C. Carranza (2015). Trypanosoma rangeli: un protozoo infectivo y no patógeno para el humano que contribuye al entendimiento de la transmisión vectorial y la infección por Trypanosoma cruzi, agente causal de la enfermedad de Chagas. Revista de La Academia Colombiana de Ciencias Exactas, Físicas y Naturales 39(150): 111–122. https://doi.org/10.18257/raccefyn.143

Vezzani, D., D.F. Eiras & C. Wisnivesky (2006). Dirofilariasis in Argentina: Historical review and first report of Dirofilaria immitis in a natural mosquito population. Veterinary Parasitology 136: 259–273. https://doi.org/10.1016/j.vetpar.2005.10.026

Wainwright, M. (2007). The Mammals of Costa Rica: A Natural History and Field Guide. Zona Tropical, Comstock Publishing Associates, Cornell University Press, Ithaca, New York, 454pp.