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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
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
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
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
Butland R, Coulson I (1985) Pulmonary eosinophilia associated with cutaneous larva migrans. Thorax 40:76–77
Capuano DM, Rocha GM (2005) Environmental contamination by Toxocara sp. eggs in Ribeirao Preto, Sao Paulo State, Brazil. Rev Inst Med Trop Sao Paulo 47:223–226
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
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
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
Dantas-Torres F (2008b) Canine vector-borne diseases in Brazil. Parasit Vectors 1:1–17
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
Eckert J, Friedhoff KT, Zahner H, Deplazes P (2008) Lehrbuch der Parasitologie für die Tiermedizin. Enke, Stuttgart
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
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
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
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
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
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
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
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
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
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
Inpankaew T, Traub R, Thompson RC, Sukthana Y (2007) Canine parasitic zoonoses in Bangkok temples. Southeast Asian J Trop Med Public Health 38:247–255
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
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
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
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
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
Lemos CH, Oliveira CR (1985) Infestaçäo humana pelo Dipylidium caninum [Human infection with Dipylidium caninum]. Rev Soc Bras Med Trop 18:267–268
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
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
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
Mehlhorn H, Armstrong PM (2001) Encyclopedic reference of parasitology: diseases, treatment, therapy. Springer, Berlin, Heidelberg
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
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
Moriello KA (2003) Zoonotic skin diseases of dogs and cats. Anim Health Res Rev 4:157–168. doi.10.1079/AHRR200355
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
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
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
Palm HW (2004) The trypanorhyncha diesing, 1863. PKSPL-IPB Press, Bogor
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
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
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
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
Ramos-E-Silva M, De Moura Castro Jacques C (2002) Leishmaniasis and other dermatozoonoses in Brazil. Clin Dermatol 20:122–134
Riemann F (1988) Nematoda. In: Higgins RP, Thiel H (eds) Introduction to the study of meiofauna. Smithsonian Institution Press, Washington, pp 293–301
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
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
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
Stevenson AF (2004) Market development reports, pet food report. GAIN Report–BR4602Brazil: 11
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
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
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 67:539–545
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
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
Wehrend A (2007) Neonatologie beim Hund: von der Geburt bis zum Absetzen. Schlütersche Verlagsgesellschaft, Hannover
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
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
Zander CD (1997) Parasit-Wirt-Beziehungen: Einführung in die ökologische Parasitologie. Springer, Berlin, Heidelberg
Acknowledgments
We thank the Centro de Control de Zoonoses/Uberlândia and the Universidade Federal do Ceará/Fortaleza for the help and support. JH is research fellow from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/Brazil). LA received a scholarship from FUNCAP/Brazil (Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico). This study was supported by a “Projeto Universal” grant from CNPq. The present study was financially supported by the research funding programme “Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz” (LOEWE) of Hesse's Ministry of Higher Education, Research and the Arts.
Declaration
We declare that the conducted study comply with the Brazilian laws.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Heukelbach, J., Frank, R., Ariza, L. et al. High prevalence of intestinal infections and ectoparasites in dogs, Minas Gerais State (southeast Brazil). Parasitol Res 111, 1913–1921 (2012). https://doi.org/10.1007/s00436-012-3037-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-012-3037-0