New insights on severe clinical manifestations and deaths from visceral leishmaniasis in free-living crab-eating foxes (Cerdocyon thous) in Brazil

Authors

DOI:

https://doi.org/10.33448/rsd-v10i16.22869

Keywords:

Crab-eating fox; Leishmaniasis; Parasitic diseases; Neglected tropical disease; Brazil.

Abstract

Visceral leishmaniasis (VL) is a zoonotic and severe neglected tropical disease, with worldwide distribution, that still cause many deaths among dogs and humans. Brazil is the country responsible for about 97% of the cases of leishmaniasis in the Americas and the disease is still considered a serious public health concern. Among wild mammalians, studies demonstrate the involvement of Cerdocyon thous in the biological cycle of Leishmania. Nevertheless, several authors consider the clinical manifestation of the disease to be rare or mild in free-living animals. Herein, we demonstrate the occurrence of severe clinical sings and deaths caused by VL in free-living crab-eating foxes. Three specimens of foxes collected from periurban areas were diagnosed with VL. The animals presented cutaneous, ophthalmological, gastrointestinal, locomotor and hematological alterations, and died after clinical progression. We identified the presence of anti-Leishmania antibodies by immunochromatographic test in all specimens. We also observed intra and extracellular amastigotes in skin cytology and lymph node aspirate. Furthermore, Leishmania infantum DNA was identified in all samples by the polymer chain reaction technique. Additionally, we performed blood count and stool parasitological tests and observed hematological disorders common to VL, such as anemia and lymphopenia. Taken together, our data demonstrate that VL can induce clinical complications and even cause death in C. thous and corroborate that this crab-eating fox is an adequate host for L. infantum.

References

Almeida, J. C., Melo, R. P. B., Kim, P. C. P. et al (2018) Molecular and serological investigation of infectious diseases in captive and free-range crab-eating fox (Cerdocyon thous - Linnaeus, 1776) from northeastern Brazil. Acta Parasitol 63:184–189

Altschul, S. F., et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410

Brandão, E. M. V., et al (2020) Wild and Domestic Canids and Their Interactions in the Transmission Cycles of Trypanosoma Cruzi and Leishmania spp. in an Area of the Brazilian Cerrado. Pathogens 9:818

Cerqueira, E. J. L., et al (2000) Considerações sobre pulgas (Siphonaptera) da raposa Cerdocyon thous (Canidae) da área endêmica de leishmaniose visceral de Jacobina, Bahia, Brasil. Rev Soc Bras Med Trop 33:91–93

Cortes, S., et al (2004) PCR as a rapid and sensitive tool in the diagnosis of human and canine leishmaniasis using Leishmania donovani s.l.-specific kinetoplastid primers. Trans R Soc Trop Med Hyg 98:12–17

Courtenary, O., et al (1996) Visceral leishmaniasis in the hoary zorro Dusicyon vetulus: a case of mistaken identity. Trans R Soc Trop Med Hyg 90:498—502

Courtenay, O., et al (2002) Low infectiousness of a wildlife host of Leishmania infantum: the crab­eating fox is not important for transmission. Parasitology 125:407–414

Dantas-Torres, F. (2007) The role of dogs as reservoirs of Leishmania parasites with emphasis on Leishmania (Leishmania) infantum and Leishmania (Viannia) braziliensis. Vet Parasitol 149:139–146

Dantas-Torres, F., & Brandão-Filho, S. P. (2006) Visceral leishmaniasis in Brazil: revisiting paradigms of epidemiology and control. Rev Inst Med Trop Sao Paulo 48:151–156

Deane, L. M., & Deane, M. P. (1954) Encontro de leishmanias nas vísceras e na pele de uma raposa, em zona endêmica de calazar, nos arredores de Sobral, Ceará. Hospital 45:419–421

Facure, K. G., & Monteiro-Filho, E. L. A. (1996) Feedings habits of the crab-eating fox, Cerdocyon thous (Carnivora, Canidae), in a suburban área of southeastern Brazil. Mammalia 60:147–149

Ferreira, P. R. B., et al (2013) Teste de ELISA indireto para diagnóstico sorológico de leishmaniose visceral em canídeos silvestres. Pesq Vet Bras 33:528–534

Figueiredo, F. B., et al (2008). First report of natural infection of a bush dog (Speothos venaticus) with Leishmania (Leishmania) chagasi in Brasil. Trans R Soc Trop Med Hyg 102:200–201

Fornazari F., & Langoni, H. (2014) Principais zoonoses em mamíferos selvagens. Vet Zootec 21: 10–24

Gomes, M. S. (2006) Carnivora – Canidae (Lobo-guará, Cachorro-do-mato, Raposa-do-campo) In: Cubas ZC (ed) Tratado de Animais Selvagens – Medicina Veterinária. Roca, São Paulo, pp 492–504

Gomes, R. B., et al (2007) Antibodies against Lutzomyia longipalpis saliva in the fox Cerdocyon thous and the sylvatic cycle of Leishmania chagasi. Trans R Soc Trop Med Hyg 101:127–133

Gontijo, C. M. F., & Melo, M. N. (2004). Leishmaniose visceral no Brasil: quadro atual, desafios e perspectivas. Rev Bras Epidemiol. 7:338–349

Hall, T. A. (1999) BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Winows 95/98/NT. Nucl Acid Symp Serie 41:95–98

Hoffman, W. A., Pons, J. A., & Janer, J. L. (1934) The sedimentation concentration methods in Schistosomiases mansoni. PR J Public Health Trop Med 9:283-289

Jorge, R. S. P., Rocha, F. L., May, J. A., & Morayo, R. G. (2010) Occurrence of pathogens in brazilian wild carnivores and its implications for conservation and public health. Oecol Aust 14: 686–710

Juarez, K. M., & Marinho-Filho, J. (2002) Diet, habitat use, and home ranges of sympatric canids in Central Brazil. J. Mammalogy 83:925–933

Jusi, M. M., et al (2011) Molecular and serological detection of Leishmania spp. in captive wild animals from Ilha Solteira, SP, Brazil. Rev Bras Parasitol Vet 20:219–222

Kruse, H., Kirkemo, A., & Handeland, K. (2004) Wildlife as a source of zoonotic infections. Emerg Infect Dis 10:2067–2072

Lainson, R., et al (1990) Amazonian visceral leishmaniais: distribution of the vector Lutzomyia longipalpis (Lutz & Neiva) in relation to the fox Cerdocyon thous (Linn.) and the efficiency of this reservoir host as a source of infection. Mem Inst Oswaldo Cruz 85:135–137

Lainson, R., & Shaw, J. J. (1987) Evolution, classification, and geographical distribution. In: Peters W (ed) The Leishmaniasis in Biology and Medicine. Academic Press, London, pp 1-120

Lainson, R., Shaw, J. J., & Lins, Z. C. (1969) Leishmaniasis in Brazil: IV. The fox, Cerdocyon thous (L) as a reservoir of Leishmania donovani in Pará State, Brazil. Trans R Soc Trop Med Hyg 63:741–745

Lima, V. F. S. (2018) Parasitic agents in wild, synanthropic and domestic animals: clinical epidemiological and public health aspects. Dissertation, Rural Federal University of Pernambuco

Luppi, M. M., et al (2008) Visceral leishmaniasis in captive wild canids in Brazil. Vet Parasitol 155:146–151

Manna, L., Reale, S., Vitale, F., & Gravino, A. E. (2009) Evidence for a relationship between Leishmania load and clinical manifestations. Res Vet Sci 87:76–78

Mattoso, C. R. S., et al (2012) Hematologic, serum biochemistry and urinary values for captive Crab-eating Fox (Cerdocyon thous) in São Paulo state, Brazil. Pesq Vet Bras 32:559–566

Mello, D. A., et al (1988) Cerdocyon thous (L.) (Carnivora, Canidae) naturally infected with Leishmania donovani chagasi (Cunha & Chagas, 1973) in Corumba (Mato Grosso do Sul State, Brazil). Mem Inst Oswaldo Cruz 83:259

Miles, M. A., Povoa, M. M., & Souxa, A. A. (1980) In: Lainson R, Shaw JJ (ed) Some methods for the enzyme characterization of Latin-American Leishmania, with particular reference to Leishmania mexicana amazonensis and subspecies of Leishmania hertigi. Trans R Soc Trop Med Hyg 74:243–252

Nicolato, R. C., et al (2013) Clinical Forms of Canine Visceral Leishmaniasis in Naturally Leishmania infantum–Infected Dogs and Related Myelogram and Hemogram Changes. PLoS ONE 8:1–9

Oliveira, R. L. (2012) Investigation of IgG anti-Leishmania infantum antibodies in free-living and captive foxes (Cerdocyon thous) and in domestic dogs (Canis familiaris) in Conservation Units of the State of Pernambuco. Dissertation, Rural Federal University of Pernambuco

Reithinger, R., Lambson, B. E., Barker, D. C., & Davies, C. R. (2000) Use of PCR to detect Leishmania (Viannia) sp. in dog blood and bone marrow. J Clin Microbiol 38:748–751

Ribeiro, C. J. N., et al (2021) Space-time risk cluster of visceral leishmaniasis in Brazilian endemic region with high social vulnerability: An ecological time series study. PLoS Negl Trop Dis 15:1–20

Ribeiro, C. J. N., et al (2021) Space-time risk cluster of visceral leishmaniasis in Brazilian endemic region with high social vulnerability: An ecological time series study. PLoS Negl Trop Dis 15: 1–20

Rodrigues, A. F. S. F., & Daemon, E. (2004) Ixodídeos e Sifonápteros em Cerdocyon thous (Carnivora, Canidae) procedentes da zona da mata mineira, Brasil. Arq Inst Biol 71:371–372

Roque, A. L. R., & Jansen, A. M. (2014) Wild and synanthropic reservoirs of Leishmania species in the Americas. Int J Parasitol Parasites Wild 3:251–262

Santos, E. F. M. (2019) Bionomy of Migonemyia migonei (Diptera, Psychodidae, Phlebotominae) under experimental conditions. Dissertation, Leonidas and Maria Deane Institute

Santos, J. D. O. (2013) Diversity of intestinal helminths in domestic dogs (Canis familiaris Linnaeus, 1758) and foxes (Cerdocyon thous Linnaeus, 1766) in semi-arid northeastern Brazil and health implications. Dissertation, Fundação Oswaldo Cruz

Silva, E. S., et al (2000) Visceral leishmaniasis in the crab-eating fox (Cerdocyon thous) in south-east Brazil. Vet Rec 147:421–422

Silveira, F. T., et al (1982) Leishmaniasis in Brazil. XVIII. Further evidence incriminating the fox, Cerdocyon thous (L), as a reservoir of Amazonian visceral leishmaniasis. Trans R Soc Trop Med Hyg 76:830–832

Soares, M. R. A., et al (2017) Occurrence of Lutzomyia longipalpis Lutz & Neiva 1912 and Cerdocyon thous Linnaeus 1977, in a visceral leishmaniasis endemic area in Brazil. Acta Trop 174:118–121

Souza, N. P., et al (2010) Leishmania (Leishmania) infantum chagasi em canídeos silvestres mantidos em cativeiro, no Estado de Mato Grosso. Rev Soc Bras Med Trop 43:333–335

Tafuri, W. L., Oliveira, M. R., Melo, M. N., & Tafuri, W. L. (2001) Canine visceral leishmaniosis: a remarkable histopathological picture of one case reported from Brazil. Vet. Parasitol 96: 203–212

Tenório, M. S. (2015) Visceral evaluation of the serology technique for visceral leishmaniasis and Chagas disease in wild animals and molecular identification. Dissertation, State University of São Paulo Julio de Mesquita Filho

Travi, B. L., et al (1998) Leishmania (Leishmania) chagasi: clinical and parasitological observations in experimentally infected Didelphis marsupialis reservoir of new world visceral leishmaniasis. Exp Parasitol 88:73–75

WHO (2020) Leishmaniasis. IOP Publishing PhysicsWeb. https://www.who.int/health-topics/leishmaniasis#tab=tab_1.

Willis, H. H. (1921) Simple levitation methods for direction of hookworm ova. Med J Aust 2:375–376.

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Published

07/12/2021

How to Cite

SILVA, M. A. D. da .; OLIVEIRA, M. R. .; SCHETTINO, S. C. .; SANTOS, I. G. dos .; OLIVEIRA NETO, M. B. .; SILVA, W. S. I. da .; BATISTA, A. I. V.; RAMOS, C. A. do N. .; RAMOS, R. A. N. .; BEZERRA-SANTOS, M. .; LIMA, V. F. S. . New insights on severe clinical manifestations and deaths from visceral leishmaniasis in free-living crab-eating foxes (Cerdocyon thous) in Brazil. Research, Society and Development, [S. l.], v. 10, n. 16, p. e108101622869, 2021. DOI: 10.33448/rsd-v10i16.22869. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/22869. Acesso em: 23 apr. 2024.

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Health Sciences