Acta Parasitologica

, Volume 64, Issue 2, pp 352–359 | Cite as

Prevalence of Endoparasites in Urban Stray Dogs from Brazil Diagnosed with Leishmania, with Potential for Human Zoonoses

  • A. M. Saldanha-Elias
  • M. A. Silva
  • V. O. Silva
  • S. L. A. Amorim
  • A. R. Coutinho
  • H. A. Santos
  • R. C. Giunchetti
  • R. W. A. Vitor
  • Stefan M. GeigerEmail author
Original Paper



In tropical environments, abandoned animals can be an important source for human zoonotic infections, such as human visceral leishmaniasis and other vector-borne diseases. Here, we report the frequency of protozoan and helminth intestinal parasites in stray dogs, which might have an implication for human health in urban Brazilian settings.

Material and Methods

We performed necropsies on 93 animals, euthanized due to canine visceral leishmaniasis control program, and examined their intestines looking for the presence of helminths; we determined the parasite load, and the elimination of eggs and cysts of protozoan parasites in fecal samples. Further, we performed serology tests for the detection of specific antibodies against Toxoplasma gondii.


Overall, a high prevalence of intestinal parasites with potential for human zoonoses resulted and only 8.6% of examined intestines remained negative. The most prevalent helminths were Ancylostoma caninum and Dipylidium caninum. For nematodes, high worm burdens were detected for A. caninum and Trichuris vulpis. Additionally, we analyzed worm burdens and quantitative stool examinations, but found no significant association between positive serology for Leishmania infection and intestinal parasite burden. Interestingly, serology for T. gondii infection revealed a prevalence of 33.3% and a positive result was significantly associated with a higher A. caninum adult worm recovery (p = 0.0087).


Our results showed stray dogs living in urban areas are heavily parasitized, which presents a potential risk for humans. Beyond the control of canine visceral leishmaniasis, we propose an improvement of the control program to reduce the risk for other parasitic diseases in dogs and humans.


Stray dogs Visceral canine leishmaniasis Endoparasites Zoonoses 



The authors received financial support for the parasitological exams from the Post-Graduation Program in Parasitology, Federal University of Minas Gerais, Brazil. We would like to thank the staff from the ‘Centro de Controle de Zoonoses’, Municipality of Belo Horizonte for their help and collaboration to obtain the biological samples, especially the veterinarians and technicians involved in the control of canine leishmaniasis. We would like to thank the contributions: Samira Oliveira Silva for grammatical revision of the English language, the Technician from the Toxoplasmosis Sector of UFMG, Rosálida Estevam Nazar Lopes, for the serological analysis, and the graduation students Andréa Cristina Silva de Paula and Francine Lemos Freitas Fontoura for the help in the serological tests.


  1. 1.
    Amouei A, Jahandar H, Daryani A, Sharif M, Sarvi S, Mizani A, Hosseini SA, Sarafrazi M, Siyadatpanah A, Gohardieh S, Bastani R, Gholami S (2018) Carnivores as important reservoirs of intestinal helminthic infections in Mazandaran Province, Northern Iran. Iran J Parasitol 13(2):251–257PubMedPubMedCentralGoogle Scholar
  2. 2.
    Ayinmode AB, Obebe OO, Olayemi E (2016) Prevalence of potentially zoonotic gastrointestinal parasites in canine faeces in Ibadan, Nigeria. Ghana Med J 50(4):201–206CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Ballweber LR, Xiao L, Bowman DD, Kahn G, Cama VA (2010) Giardiasis in dogs and cats: update on epidemiology and public health significance. Trends Parasitol 26:180–189CrossRefPubMedGoogle Scholar
  4. 4.
    Baneth G, Thamsborg SM, Otranto D, Guillot J, Blaga R, Deplazes P, Solano-Gallego L (2016) Major parasitic zoonoses associated with dogs and cats in Europe. J Comp Pathol 155:S54–S74CrossRefPubMedGoogle Scholar
  5. 5.
    Bowman DD, Montgomery SP, Zajac AM, Eberhard ML, Kazacos KR (2010) Hookworms of dogs and cats as agents of cutaneous larva migrans. Trends Parasitol 26:162–167CrossRefPubMedGoogle Scholar
  6. 6.
    Brazilian Ministry of Health (2006) In: Ministério da Saúde—MS (ed) Manual de Vigilância e Controle da Leishmaniose Visceral, Brasília, pp 1–122Google Scholar
  7. 7.
    Brazilian Ministry of Health/Ministry of Agriculture, Farming and Food Supply (2008) Portaria Interministerial n° 1.426. Diário Oficial da União 133:37Google Scholar
  8. 8.
    Bundy DAP, Medley GF (1992) Immuno-epidemiology of human geohelminthiasis: ecological and immunological determinants of worm burden. Parasitology 104:S105–S119CrossRefPubMedGoogle Scholar
  9. 9.
    Chomel BB, Sun B (2011) Zoonoses in the bedroom. Emerg Infect Dis 17:167–172CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Cortez-Aguirre GR, Jiménez-Coello M, Gutiérrez-Blanco E, Ortega-Pacheco A (2018) Stray dog population in a city of Southern Mexico and its impact on the contamination of public areas. Vet Med Int 2018:2381583CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Criado BR, Belda W Jr, Vasconcellos C, Silva CS (2012) Cutaneous larva migrans: a bad souvenir from the vacation. Dermatol Online 18:11Google Scholar
  12. 12.
    Croese J (1998) Hookworm-provoked IgE-mediated pathology: capricious damage or remarkable strategy? Parasitol Today 14(1998):70–72CrossRefPubMedGoogle Scholar
  13. 13.
    Dantas-Torres F (2008) Canine vector borne diseases in Brazil. Parasites Vectors 1:1–25CrossRefGoogle Scholar
  14. 14.
    Dantas-Torres F, Otranto D (2016) Best practices for preventing vector-borne diseases in dogs and humans. Trends Parasitol 32:43–55CrossRefPubMedGoogle Scholar
  15. 15.
    Deplazes P, Van Knapen F, Schweiger A, Overgaauw PA (2011) Role of pet dogs and cats in the transmission of helminthic zoonoses in Europe, with a focus on echinococcosis and toxocarosis. Vet Parasitol 182:41–53CrossRefPubMedGoogle Scholar
  16. 16.
    Dreer MKP, Gonçalves DD, Caetano ICS, Gerônimo E, Menegas PH, Bergo D, Lopes-Mori FMR, Benitez A, Freitas JC, Evers F, Navarro IT, Martins LA (2013) Toxoplasmosis, leptospirosis and brucellosis in stray dogs housed at the shelter in Umuarama municipality, Paraná, Brazil. J Venom Anim Toxins Incl Trop Dis 9:231Google Scholar
  17. 17.
    Etheredge GD, Michael G, Michael P, Muehlenbein MP, Frenkel JK (2004) The roles of cats and dogs in the transmission of Toxoplasma infection in Kuna and Embera children in eastern Panama. Rev Panam Salud Publica 16:176–186CrossRefPubMedGoogle Scholar
  18. 18.
    Feng Y, Xiao L (2011) Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Rev Clin Microbiol 24:110–140CrossRefGoogle Scholar
  19. 19.
    Hoffman WA, Pons JA, Janer JL (1934) Sedimentation concentration method in schistosomiasis mansoni. Puerto Rico J Publ Health 9:283–298Google Scholar
  20. 20.
    Katagiri S, Oliveira-Siqueira TC (2008) Prevalence of dog intestinal parasites and risk perception of zoonotic infection by dog owners in São Paulo State, Brazil. Zoonoses Publ Health 55:406–413CrossRefGoogle Scholar
  21. 21.
    Katz N, Chaves A, Pellegrino J (1972) A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Rev Inst Med Trop São Paulo 14:397–400PubMedGoogle Scholar
  22. 22.
    Keymer AE, Slater AFG (1987) Helminth fecundity: density dependence or statistical illusion? Parasitol Today 3:56–58CrossRefPubMedGoogle Scholar
  23. 23.
    Klimpel S, Heukelbach J, Pothmann D, Rueckert S (2010) Gastrointestinal and ectoparasites from urban stray dogs in Fortaleza (Brazil): high infection risk for humans? Parasitol Res 107:713–719CrossRefPubMedGoogle Scholar
  24. 24.
    Landmann JK, Prociv P (2003) Experimental human hookworm infection with the dog hookworm Ancylostoma caninum. Med J Austral 178:69–71PubMedGoogle Scholar
  25. 25.
    Langoni H, Fornazari F, Silva RC, Monti ET, Villa FB (2013) Prevalence of antibodies against Toxoplasma gondii and Neospora caninum in dogs. Braz J Microbiol 44:1327–1330CrossRefPubMedGoogle Scholar
  26. 26.
    De Liberato C, Berrilli F, Odorizi L, Scarcella R, Barni M, Amoruso C, Scarito A, Di Filippo MM, Carvelli A, Lacoponi F, Scaramozzino P (2017) Parasites in stray dogs from Italy: prevalence, risk factors and management concerns. Acta Parasitol 63(1):27–32CrossRefGoogle Scholar
  27. 27.
    Little SE (2013) Future challenges for parasitology: vector control and one health in the Americas. Vet Parasitol 195:249–255CrossRefPubMedGoogle Scholar
  28. 28.
    Lucio-Forster A, Liotta JA, Yaros JP, Briggs KR, Mohammed HO, Bowman DD (2012) Morphological differentiation of eggs of Ancylostoma caninum, Ancylostoma tubaeforme, and Ancylostoma braziliense from dogs and cats in the United States. J Parasitol 98:1041–1044CrossRefPubMedGoogle Scholar
  29. 29.
    Mallawarachchi CH, Chandrasena N, Wickramasinghe S, Premaratna R, Gunawardane N, Mallawarachchi N, de Silva NR (2018) A preliminary survey of filarial parasites in dogs and cats in Sri Lanka. PLoS One 13(11):e0206633CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Medina-Pinto R, Rodríguez-Vivas R, Bolio-González M (2018) Nematodos intestinales de perros em parques públicos de Yucatán, México. Biomédica 38(1):105–110CrossRefPubMedGoogle Scholar
  31. 31.
    Meireles P, Montiani-Ferreira F, Thomaz-Soccol V (2008) Survey of giardiosis in household and shelter dogs from metropolitan areas of Curitiba, Paraná state, Southern Brazil. Vet Parasitol 152:242–248CrossRefPubMedGoogle Scholar
  32. 32.
    Moskvina TV, Ermolenko AV (2016) Helminth infections in domestic dogs from Russia. Vet World 9(11):1248–1258CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Oguz B, Ozdal N, Kilinc OO, Serdar Deger M (2018) Preliminary studies on the prevalence and genotyping of Echinococcus granulosus infection in stray dogs in Van Province, Turkey. J Vet Res 62(4):497–502CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Oliveira-Arbex AP, David EB, Oliveira-Sequeira TC, Katagiri S, Coradi ST, Guimarães S (2016) Molecular identification of Ancylostoma species from dogs and an assessment of zoonotic risk in low-income households, São Paulo State, Brazil. J Helminthol 11:1–6Google Scholar
  35. 35.
    Oudni-M’rad M, Chaâbane-Banaoues R, M’rad S, Trifa F, Mezhoud H, Babba H (2017) Gastrointestinal parasites of canids, a latent risk to human health in Tunisia. Parasites Vectors 10(1):280CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Paul M, King L, Carlin EP (2010) Zoonoses of people and their pets: a US perspective on significant pet-associated parasitic diseases. Trends Parasitol 26:153–154CrossRefPubMedGoogle Scholar
  37. 37.
    Pennisi MG (2015) Leishmaniosis of companion animals in Europe: an update. Vet Parasitol 208:35–47CrossRefPubMedGoogle Scholar
  38. 38.
    Belo Horizonte City Hall (2007) Relatório final da IX Conferência Municipal de Saúde de Belo Horizonte—Etapa Municipal da 13ª Conferência Nacional de Saúde. Conselho Municipal de Saúde de Belo Horizonte e Secretaria Municipal de Saúde de Belo Horizonte. Accessed 09 Oct 2014
  39. 39.
    Schares G, Pantchev N, Barutzki D, Heydorn AO, Bauer C, Conraths FJ (2005) Oocysts of Neospora caninum, Hammondia heydorni, Toxoplasma gondii and Hammondia hammondi in faeces collected from dogs in Germany. Int J Parasitol 35:1525–1537CrossRefPubMedGoogle Scholar
  40. 40.
    Schnieder T, Laabs E-M, Welz C (2011) Larval development of Toxocara canis in dogs. Vet Parasitol 175:193–206CrossRefPubMedGoogle Scholar
  41. 41.
    Silva DAO, Lobato J, Mineo TWP, Mineo JR (2007) Evaluation of serological tests for the diagnosis of Neospora caninum infection in dogs: optimization of cut off titers and inhibition studies of cross-reactivity with Toxoplasma gondii. Vet Parasitol 143:234–244CrossRefPubMedGoogle Scholar
  42. 42.
    Silva NM, Lourenço EV, Silva DAO, Mineo JR (2002) Optimisation of cut-off titres in Toxoplasma gondii specific ELISA and IFAT in dog sera using immunoreactivity to SAG-1 antigen as a molecular marker of infection. Vet J 163:94–98CrossRefPubMedGoogle Scholar
  43. 43.
    Tenter AM (1999) Current knowledge on the epidemiology of infections with Toxoplasma. Tokai J Exp Clin Med 23:391Google Scholar
  44. 44.
    Traversa D, Di Regalbono AF, Di Cesare A, La Torre F, Drake J, Pietrobelli M (2014) Environmental contamination by canine geohelminths. Parasites Vectors 7:67CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Traversa D (2012) Pet roundworms and hookworms: a continuing need for global worming. Parasites Vectors 5:91CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Ugbomoiko US, Ariza L, Heukelbach J (2008) Parasites of importance for human health in Nigerian dogs: high prevalence and limited knowledge of pet owners. BMC Vet Res 4:49CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    World Health Organization (2012) Research priorities for zoonoses and other marginalized infections. Tech. Rep. Series No. 971Google Scholar
  48. 48.
    World Organization for Animal Health—OIE (2017) One Health “at a glance” 2017. Accessed 10 June 2017

Copyright information

© Witold Stefański Institute of Parasitology, Polish Academy of Sciences 2019

Authors and Affiliations

  • A. M. Saldanha-Elias
    • 1
  • M. A. Silva
    • 2
  • V. O. Silva
    • 1
  • S. L. A. Amorim
    • 1
  • A. R. Coutinho
    • 1
  • H. A. Santos
    • 1
  • R. C. Giunchetti
    • 3
  • R. W. A. Vitor
    • 1
  • Stefan M. Geiger
    • 1
    Email author
  1. 1.Departamento de Parasitologia, Instituto de Ciências BiológicasUniversidade Federal de Minas GeraisBelo HorizonteBrazil
  2. 2.Empresa de Informática e Informação do Município de Belo Horizonte, PRODABELBelo HorizonteBrazil
  3. 3.Departamento de Morfologia, Instituto de Ciências BiológicasUniversidade Federal de Minas GeraisBelo HorizonteBrazil

Personalised recommendations