Parasitology Research

, Volume 111, Issue 5, pp 1913–1921 | Cite as

High prevalence of intestinal infections and ectoparasites in dogs, Minas Gerais State (southeast Brazil)

  • Jörg Heukelbach
  • Raphael Frank
  • Liana Ariza
  • Íris de Sousa Lopes
  • Alcides de Assis e Silva
  • Ana Cláudia Borges
  • Jean Ezequiel Limongi
  • Carlos Henrique Morais de Alencar
  • Sven Klimpel
Original Paper

Abstract

In the present study, 155 dogs euthanized by the Zoonotic Disease Unit of Uberlândia in Minas Gerais State (Southeast Brazil) were autopsied. Ectoparasites were collected, and the intestinal content of dogs was systematically examined for the presence of helminthic parasites. In total, we isolated 5,155 metazoan parasites of eight species (three intestinal helminth species, five ectoparasite species). The cestode Dipylidium caninum was present in 57 dogs (36.8 %), the nematodes Ancylostoma caninum in 30 (19.4 %) and Toxocara canis in 24 (15.5 %), respectively. Among the ectoparasites, 139 (89.7 %) dogs were infested with Rhipicephalus sanguineus, 115 (74.2 %) with Ctenocephalides felis, 5 (3.2 %) with Tunga penetrans and one specimen (0.7 %) with Amblyomma cajennense, while myiasis was found in one dog (0.7 %). In logistic regression analysis, young age (adjusted odds ratio 5.74; 95 % confidence interval 1.18–27.85) and male sex (3.60; 1.24–10.40) were significantly associated with toxocariasis, and crossbreed dogs (8.20; 1.52–44.31), with dipylidiasis. Male (2.23; 1.12–4.43) and crossbreed dogs (5.17; 1.17–22.83) had also a significant higher number of concomitant parasitoses. Spatial distribution of dogs by neighbourhood identified high-risk areas. Our systematic study shows that dogs in Uberlândia carry a high number of parasites which may cause zoonotic diseases in humans; therefore, further specific evidence-based intervention measures are needed.

References

  1. Alderete J, Jacob C, Pastorino AC, Elefant GR, Castro APM, Fomin ABF, Chieffi PP (2003) Prevalence of Toxocara infection in schoolchildren from the Butantã region, São Paulo, Brazil. Mem Inst Oswaldo Cruz 98:593–597. doi:10.1590/S0074-02762003000500002 PubMedCrossRefGoogle Scholar
  2. Anaruma Filho F, Chieffi PP, Correa CRS, Camargo ED, Silveira EP, Aranha JJB, Ribeiro MCSA (2002) Human toxocariasis: a seroepidemiological survey in the municipality of Campinas (SP), Brazil. Rev Inst Med Trop Sao Paulo 44:303–307. doi:10.1590/S0036-46652002000600002 PubMedCrossRefGoogle Scholar
  3. Blazius RD, Emerick S, Prophiro JS, Romão PRT, Silva OS (2005) Occurrence of protozoa and helminthes in faecal samples of stray dogs from Itapema City, Santa Catarina. Rev Soc Bras Med Trop 38:73–74. doi:10.1590/S0037-86822005000100018 PubMedCrossRefGoogle Scholar
  4. Butland R, Coulson I (1985) Pulmonary eosinophilia associated with cutaneous larva migrans. Thorax 40:76–77PubMedCrossRefGoogle Scholar
  5. Capuano DM, Rocha GM (2005) Environmental contamination by Toxocara sp. eggs in Ribeirao Preto, Sao Paulo State, Brazil. Rev Inst Med Trop Sao Paulo 47:223–226PubMedCrossRefGoogle Scholar
  6. Caumes E, Carrière J, Guermonprez G, Bricaire F, Danis M, Gentilini M (1995) Dermatoses associated with travel to tropical countries: a prospective study of the diagnosis and management of 269 patients presenting to a tropical disease unit. Clin Infect Dis 20:542–548. doi:10.1093/clinids/20.3.542 PubMedCrossRefGoogle Scholar
  7. Dalimi A, Sattari A, Motamedi G (2006) A study on intestinal helminthes of dogs, foxes and jackals in the western part of Iran. Vet Parasitol 142:129–133. doi:10.1016/j.vetpar.2006.06.024 PubMedCrossRefGoogle Scholar
  8. Dantas-Torres F (2008a) The brown dog tick, Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae): From taxonomy to control. Vet Parasitol 152:173–185. doi:10.1016/j.vetpar.2007.12.030 PubMedCrossRefGoogle Scholar
  9. Dantas-Torres F (2008b) Canine vector-borne diseases in Brazil. Parasit Vectors 1:1–17CrossRefGoogle Scholar
  10. Duh D, Tozon N, Petrovec M, Strasek K, Avsic-Zupanc T (2004) Canine babesiosis in Slovenia: molecular evidence of Babesia canis canis and Babesia canis vogeli. Vet Res 35:363–368. doi:10.1051/vetres:2004018 PubMedCrossRefGoogle Scholar
  11. Eckert J, Friedhoff KT, Zahner H, Deplazes P (2008) Lehrbuch der Parasitologie für die Tiermedizin. Enke, StuttgartGoogle Scholar
  12. Eguia-Aguilar P, Cruz-Reyes A, Martinez-Maya JJ (2005) Ecological analysis and description of the intestinal helminths present in dogs in Mexico City. Vet Parasitol 127:139–146. doi:10.1016/j.vetpar.2004.10.004 PubMedCrossRefGoogle Scholar
  13. Földvári G, Hell E, Farkas R (2005) Babesia canis canis in dogs from Hungary: detection by PCR and sequencing. Vet Parasitol 127:221–226. doi:10.1016/j.vetpar.2004.10.016 PubMedCrossRefGoogle Scholar
  14. Gilot B, Laforge M, Pichot J, Raoult D (1990) Relationships between the Rhipicephalus sanguineus complex ecology and Mediterranean spotted fever epidemiology in France. Eur J Epidemiol 6:357–362. doi:10.1007/BF00151708 PubMedCrossRefGoogle Scholar
  15. Glaser C, Lewis P, Wong S (2000) Pet-, animal-, and vector-borne infections. Pediatr Rev 21:219–232. doi:10.1542/pir.21-7-219 Google Scholar
  16. Heukelbach J, Costa A, Wilcke T, Mencke N, Feldmeier H (2004a) The animal reservoir of Tunga penetrans in severely affected communities of north-east Brazil. Med Vet Entomol 18:329–335. doi:10.1111/j.0269-283X.2004.00532.x PubMedCrossRefGoogle Scholar
  17. Heukelbach J, Feldmeier H (2008) Epidemiological and clinical characteristics of hookworm-related cutaneous larva migrans. Lancet Infect Dis 8:302–309. doi:10.1016/S1473-3099(08)70098-7 PubMedCrossRefGoogle Scholar
  18. Heukelbach J, Gomide M, Araújo F Jr, Pinto NSR, Santana RD, Brito JRM, Feldmeier H (2007) Cutaneous larva migrans and tungiasis in international travelers exiting Brazil: an airport survey. J Travel Med 14:374–380. doi:10.1111/j.1708-8305.2007.00156.x PubMedCrossRefGoogle Scholar
  19. Heukelbach J, Hengge UR (2009) Bed bugs, leeches and hookworm larvae in the skin. Clin Dermatol 27:285–290. doi:10.1016/j.clindermatol.2008.10.008 PubMedCrossRefGoogle Scholar
  20. Heukelbach J, Wilcke T, Feldmeier H (2004b) Cutaneous larva migrans (creeping eruption) in an urban slum in Brazil. Int J Dermatol 43:511–515. doi:10.1111/j.1365-4632.2004.02152.x PubMedCrossRefGoogle Scholar
  21. Heukelbach J, Wilcke T, Winter B, Feldmeier H (2005) Epidemiology and morbidity of scabies and pediculosis capitis in resource-poor communities in Brazil. Br J Dermatol 15:150–156. doi:10.1111/j.1365-2133.2005.06591.x CrossRefGoogle Scholar
  22. Inpankaew T, Traub R, Thompson RC, Sukthana Y (2007) Canine parasitic zoonoses in Bangkok temples. Southeast Asian J Trop Med Public Health 38:247–255PubMedGoogle Scholar
  23. Katagiri S, Oliveira-Sequeira TC (2008) Prevalence of dog intestinal parasites and risk perception of zoonotic infection by dog owners in Sao Paulo State, Brazil. Zoonoses Public Hlth 55:406–413. doi:10.1111/j.1863-2378.2008.01163.x CrossRefGoogle Scholar
  24. Keller N, Jacobson LS, Nel M, Clerq M, Thompson PN, Schoeman JP (2004) Prevalence and risk factors of hypoglycemia in virulent canine babesiosis. J Vet Intern Med 18:265–270. doi:10.1111/j.1939-1676.2004.tb02544.x PubMedCrossRefGoogle Scholar
  25. Klimpel S, Förster M, Schmahl G (2007a) Parasite fauna of the bank vole (Clethrionomys glareolus) in an urban region of Germany: reservoir host of zoonotic metazoan parasites? Parasitol Res 102:69–75. doi:10.1007/s00436-007-0725-2 PubMedCrossRefGoogle Scholar
  26. Klimpel S, Förster M, Schmahl G (2007b) Parasites of two abundant sympatric rodent species in relation to host phylogeny and ecology. Parasitol Res 100:867–875. doi:10.1007/s00436-006-0368-8 PubMedCrossRefGoogle Scholar
  27. Klimpel S, Heukelbach J, Pothmann D, Rückert S (2010) Gastrointestinal and ectoparasites from urban stray dogs in Fortaleza (Brazil): high infection risk for humans? Parasitol Res 107:713–719. doi:10.1007/s00436-010-1926-7 PubMedCrossRefGoogle Scholar
  28. Lemos CH, Oliveira CR (1985) Infestaçäo humana pelo Dipylidium caninum [Human infection with Dipylidium caninum]. Rev Soc Bras Med Trop 18:267–268Google Scholar
  29. Mantovani E, Costa I, Gauditano G, Bonoldi V, Higuchi M, Yoshinari N (2007) Description of Lyme disease-like syndrome in Brazil: is it a new tick borne disease or Lyme disease variation? Braz J Med Biol Res 40:443–456. doi:10.1590/S0100-879X2006005000082 PubMedCrossRefGoogle Scholar
  30. Matjila P, Penzhorn B, Bekker C, Nijhof A, Jongejan F (2004) Confirmation of occurrence of Babesia canis vogeli in domestic dogs in South Africa. Vet Parasitol 122:119–125. doi:10.1016/j.vetpar.2004.03.019 PubMedCrossRefGoogle Scholar
  31. Matjila TP, Nijhof AM, Taoufik A, Houwers D, Teske E, Penzhorn BL, Lange T, Jongejan F (2005) Autochthonous canine babesiosis in The Netherlands. Vet Parasitol 131:23–29. doi:10.1016/j.vetpar.2005.04.020 PubMedCrossRefGoogle Scholar
  32. Mehlhorn H, Armstrong PM (2001) Encyclopedic reference of parasitology: diseases, treatment, therapy. Springer, Berlin, HeidelbergCrossRefGoogle Scholar
  33. Minnaar WN, Krecek RC, Fourie LJ (2002) Helminths in dogs from a peri-urban resource-limited community in Free State Province, South Africa. Vet Parasitol 107:343–349. doi:10.1016/S0304-4017(02)00155-3 PubMedCrossRefGoogle Scholar
  34. Miraglia del Giudice M, De Luca M, Capristo C (2002) Probiotics and atopic dermatitis. A new strategy in atopic dermatitis. Dig Liver Dis 34:68–71. doi:10.1016/S1590-8658(02)80169-4 CrossRefGoogle Scholar
  35. Moriello KA (2003) Zoonotic skin diseases of dogs and cats. Anim Health Res Rev 4:157–168. doi.10.1079/AHRR200355 Google Scholar
  36. O'Dwyer LH, Massard CL, de Souza JC Pereira (2001) Hepatozoon canis infection associated with dog ticks of rural areas of Rio de Janeiro State, Brazil. Vet Parasitol 94:143–150. doi:10.1016/S0304-4017(00)00378-2 PubMedCrossRefGoogle Scholar
  37. Okoye IC, Obiezue NR, Okorie CE, Ofoezie IE (2011) Epidemiology of intestinal helminth parasites in stray dogs from markets in south-eastern Nigeria. J Helminthol 85:415–420. doi:10.1017/S0022149X10000738 PubMedCrossRefGoogle Scholar
  38. Oliveira-Sequeira T, Amarante A, Ferrari T, Nunes L (2002) Prevalence of intestinal parasites in dogs from São Paulo State, Brazil. Vet Parasitol 103:19–27. doi:10.1016/S0304-4017(01)00575-1 PubMedCrossRefGoogle Scholar
  39. Palm HW (2004) The trypanorhyncha diesing, 1863. PKSPL-IPB Press, BogorGoogle Scholar
  40. Pedersen AB, Altizer S, Poss M, Cunningham AA, Nunn CL (2005) Patterns of host specificity and transmission among parasites of wild primates. Int J Parasitol 35:647–657. doi:10.1016/j.ijpara.2005.01.005 Google Scholar
  41. Pinter A, Horta MC, Pacheco RC, Moraes-Filho J, Labruna MB (2008) Serosurvey of Rickettsia spp. in dogs and humans from an endemic area for Brazilian spotted fever in the State of São Paulo. Brazil Cad Saude Publica 24:247–252. doi:10.1590/S0102-311X2008000200003 CrossRefGoogle Scholar
  42. Pugh RE (1987) Effects on the development of Dipylidium caninum and on the host reaction to this parasite in the adult flea (Ctenocephalides felis felis). Parasitol Res 73:171–177. doi:10.1007/BF00536475 PubMedCrossRefGoogle Scholar
  43. Ramirez-Barrios RA, Barboza-Mena G, Munoz J, Angulo-Cubillan F, Hernandez E, Gonzalez F, Escalona F (2004) Prevalence of intestinal parasites in dogs under veterinary care in Maracaibo, Venezuela. Vet Parasitol 121:11–20. doi:10.1016/j.vetpar.2004.02.024 PubMedCrossRefGoogle Scholar
  44. Ramos-E-Silva M, De Moura Castro Jacques C (2002) Leishmaniasis and other dermatozoonoses in Brazil. Clin Dermatol 20:122–134PubMedCrossRefGoogle Scholar
  45. Riemann F (1988) Nematoda. In: Higgins RP, Thiel H (eds) Introduction to the study of meiofauna. Smithsonian Institution Press, Washington, pp 293–301Google Scholar
  46. Rodriguez-Vivas RI, Gutierrez-Ruiz E, Bolio-Gonzalez ME, Ruiz-Pina H, Ortega-Pacheco A, Reyes-Novelo E, Manrique-Saide P, Aranda-Cirerol F, Lugo-Perez JA (2011) An epidemiological study of intestinal parasites of dogs from Yucatan, Mexico, and their risk to public health. Vector Borne Zoonotic Dis 11:1141–1144. doi:10.1089/vbz.2010.0232 PubMedCrossRefGoogle Scholar
  47. Salb AL, Barkema HW, Elkin BT, Thompson RCA, Whiteside DP, Black SR, Dubey JP, Kutz SJ (2008) Dogs as sources and sentinels of parasites in humans and wildlife, northern Canada. Emerg Infect Dis 14:60–63. doi:10.3201/eid1401.071113 Google Scholar
  48. Sowemimo OA (2009) The prevalence and intensity of gastrointestinal parasites of dogs in Ile-Ife, Nigeria. J Helminthol 83:27–31. doi:10.1017/S0022149X08067229 PubMedCrossRefGoogle Scholar
  49. Stevenson AF (2004) Market development reports, pet food report. GAIN Report–BR4602Brazil: 11Google Scholar
  50. Stoye M (1973) Untersuchungen über die möglichkeit pränataler und galaktogener infektionen mit Ancylostoma caninum Ercolani 1859 (Ancylostomidae) beim Hund. Zbl Vet Med B 20:1–39. doi:10.1111/j.1439-0450.1973.tb01098.x CrossRefGoogle Scholar
  51. Szabó M, De Souza L, Olegário M, Ferreira F, De Albuquerque Pajuaba Neto A (2010) Ticks (Acari: Ixodidae) on dogs from Uberlândia, Minas Gerais, Brazil. Transbound Emerg Dis 57:72–74. doi:10.1111/j.1865-1682.2010.01111.x PubMedCrossRefGoogle Scholar
  52. Traub RJ, Robertson ID, Irwin PJ, Mencke N, Thompson RCAA (2002) The role of dogs in transmission of gastrointestinal parasites in a remote tea-growing community in northeastern India. Am J Trop Med Hyg 67:539–545Google Scholar
  53. Traub RJ, Robertson ID, Irwin PJ, Mencke N, Thompson R (2005) Canine gastrointestinal parasitic zoonoses in India. Trends Parasitol 21:42–48. doi:10.1016/j.pt.2004.10.011 PubMedCrossRefGoogle Scholar
  54. 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 4:1–9. doi:10.1186/1746-6148-4-49 CrossRefGoogle Scholar
  55. Wehrend A (2007) Neonatologie beim Hund: von der Geburt bis zum Absetzen. Schlütersche Verlagsgesellschaft, HannoverGoogle Scholar
  56. Wilcke T, Heukelbach J, Moura RCS, Kerr-Pontes LRS, Feldmeier H (2002) High prevalence of tungiasis in a poor neighbourhood in Fortaleza, Northeast Brazil. Acta Trop 83:255–258. doi:10.1016/S0001-706X(02)00133-X PubMedCrossRefGoogle Scholar
  57. Xhaxhiu D, Kusi I, Rapti D, Kondi E, Postoli R, Rinaldi L, Dimitrova ZM, Visser M, Knaus M, Rehbein S (2011) Principal intestinal parasites of dogs in Tirana, Albania. Parasitol Res 108:341–353. doi:10.1007/s00436-010-2067-8 PubMedCrossRefGoogle Scholar
  58. Zander CD (1997) Parasit-Wirt-Beziehungen: Einführung in die ökologische Parasitologie. Springer, Berlin, HeidelbergGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Jörg Heukelbach
    • 1
    • 2
  • Raphael Frank
    • 3
  • Liana Ariza
    • 1
  • Íris de Sousa Lopes
    • 4
  • Alcides de Assis e Silva
    • 4
  • Ana Cláudia Borges
    • 4
  • Jean Ezequiel Limongi
    • 4
  • Carlos Henrique Morais de Alencar
    • 1
  • Sven Klimpel
    • 3
  1. 1.Department of Community Health, School of MedicineFederal University of CearáFortalezaBrazil
  2. 2.Anton Breinl Centre for Tropical Medicine and Public Health, School of Public Health, Tropical Medicine and Rehabilitation SciencesJames Cook UniversityTownsvilleAustralia
  3. 3.Biodiversity and Climate Research Centre (BiK-F), Medical Biodiversity and Parasitology, Senckenberg Gesellschaft für Naturforschung (SGN), Institute for Ecology, Evolution and DiversityGoethe-University (GO)Frankfurt am MainGermany
  4. 4.Department of Public HealthCentre of Control of Zoonotic DiseaseUberlândiaBrazil

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