Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-19T19:27:00.378Z Has data issue: false hasContentIssue false

Molecular identification of Ancylostoma species from dogs and an assessment of zoonotic risk in low-income households, São Paulo State, Brazil

Published online by Cambridge University Press:  11 January 2016

A.P. Oliveira-Arbex
Affiliation:
UNESP – Universidade Estadual Paulista, Departamento de Parasitologia, Instituto de Biociências, CEP: 18618-970, Botucatu, São Paulo, Brazil
E.B. David
Affiliation:
UNESP – Universidade Estadual Paulista, Departamento de Parasitologia, Instituto de Biociências, CEP: 18618-970, Botucatu, São Paulo, Brazil
T.C.G. Oliveira-Sequeira
Affiliation:
UNESP – Universidade Estadual Paulista, Departamento de Parasitologia, Instituto de Biociências, CEP: 18618-970, Botucatu, São Paulo, Brazil
S. Katagiri
Affiliation:
UFS – Universidade Federal de Sergipe, Departamento de Morfologia, Centro de Ciências Biológicas e da Saúde, CEP 49000-000, São Cristovão, Aracaju, Sergipe, Brazil
S.T. Coradi
Affiliation:
USC – Universidade do Sagrado Coração, Departamento de Ciências Biológicas e da Saúde, CEP 17011160, Bauru, São Paulo, Brazil
S. Guimarães*
Affiliation:
UNESP – Universidade Estadual Paulista, Departamento de Parasitologia, Instituto de Biociências, CEP: 18618-970, Botucatu, São Paulo, Brazil

Abstract

Hookworm infection stands out for its worldwide distribution and for its veterinary and public health relevance. Based on copromicroscopic examinations and polymerase chain reaction (PCR) amplification of the ITS1–5.8S–ITS2 region, we assessed, respectively, the prevalence of intestinal parasites and the identification of canine hookworm species in faeces recovered from 278 dogs living in households of an inland municipality of São Paulo State, Brazil. Intestinal parasites were found in 67.3% of dogs and hookworm infection was found at the highest prevalence rate (56.6%), followed by Toxocara canis (11.9%), Isospora spp. (11.9%), Giardia spp. (5.8%), Sarcocystis spp. (4.0%), ‘Hammondia-like’ (1.4%), Dipylidium caninum (1.1%) and Trichuris vulpis (0.7%). Of 158 samples positive for hookworm eggs, 106 (67.1%) were amplified by PCR and, of those, 88 (55.7%) were successfully sequenced for species identification. Single infections with Ancylostoma caninum and Ancylostoma braziliense were recorded in 61.4% and 12.5%, respectively, and mixed infections were found in 26.1%. The nucleotide sequences of both species showed high identity rates (98–100%) when compared with reference sequences. Although A. caninum was the most prevalent hookworm in the dogs assessed, the occurrence of both A. caninum and A. braziliense in single and/or mixed infections poses a potential risk for the local population in a low-income area, especially children, to acquire cutaneous larva migrans (CLM).

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bowman, D.D., Montgomery, S.P., Zajac, A.M., Eberhard, M.L. & Kazacos, K.R. (2010) Hookworms of dogs and cats as agents of cutaneous larva migrans. Trends in Parasitology 26, 6267.CrossRefGoogle ScholarPubMed
Cardoso, A.S., Costa, I.M.H., Figueiredo, C., Castro, A. & Conceição, M.A.P. (2014) The occurrence of zoonotic parasites in rural dog populations from northern Portugal. Journal of Helminthology 88, 203209.CrossRefGoogle ScholarPubMed
Coelho, W.M.D., Amarante, A.F.T., Apolinário, J.D.C., Coelho, N.M.D. & Bresciani, K.D.S. (2011) Occurrence Ancylostoma in dogs, cats and public places from Andradina city, São Paulo state, Brazil. Revista do Instituto de Medicina Tropical de Sao Paulo 53, 181184.CrossRefGoogle ScholarPubMed
David, E.B., Coradi, S.T., Oliveira-Sequeira, T.C.G., Ribolla, P.E.M., Katagiri, S. & Guimarães, S. (2011) Diagnosis of Giardia infections by PCR-based methods in children of an endemic area. Journal of Venomous Animals and Toxins including Tropical Diseases 17, 209215.CrossRefGoogle Scholar
Fontanarrosa, M.F., Vezzani, D., Basabe, J. & Eiras, D.F. (2006) An epidemiological study of gastrointestinal parasites of dogs from Southern Greater Buenos Aires (Argentina): age, gender, breed, mixed infections, and seasonal and spatial patterns. Veterinary Parasitology 136, 283295.CrossRefGoogle Scholar
Garcia, L.S. (2001) Diagnostic medical parasitology. 4th edn. 1092 pp. Washington, DC, ASM Press.Google Scholar
Gingrich, E.N., Scorza, A.V., Clifford, E.L., Olea-Popelka, F.J. & Lappin, M.R. (2010) Intestinal parasites of dogs on the Galapagos Islands. Veterinary Parasitology 169, 404407.CrossRefGoogle ScholarPubMed
Heukelbach, J. & Feldmeier, H. (2008) Epidemiological and clinical characteristics of hookworm related cutaneous larva migrans. Lancet Infectious Diseases 8, 302309.CrossRefGoogle ScholarPubMed
Heukelbach, J., Frank, R., Ariza, L., Lopes, I.S., Silva, A.D.A., Borges, A.C., Limongi, J.E., De Alencar, C.H.M. & Klimpel, S. (2012) High prevalence of intestinal infections and ectoparasites in dogs, Minas Gerais State (southeast Brazil). Parasitology Research 111, 19131921.CrossRefGoogle Scholar
Katagiri, S. & Oliveira-Sequeira, T.C.G. (2008) Prevalence of dog intestinal parasites and risk perception of zoonotic infection by dog owners in Sao Paulo State, Brazil. Zoonoses Public Health 55, 406413.CrossRefGoogle ScholarPubMed
Klimpel, S., Heukelbach, J., Pothmann, D. & Rückert, S. (2010) Gastrointestinal and ectoparasites from urban stray dogs in Fortaleza (Brazil): high infection risk for humans? Parasitology Research 107, 713719.CrossRefGoogle ScholarPubMed
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J., & Higgins, D.G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 29472948.CrossRefGoogle ScholarPubMed
La Sala, L.F., Leiboff, A., Burgos, J.M. & Costamagna, S.R. (2015) Spatial distribution of canine zoonotic enteroparasites in Bahía Blanca, Argentina. Revista Argentina de Microbiologia 47, 1724.CrossRefGoogle ScholarPubMed
Lesshafft, H., Schuster, A., Reichert, F., Talhari, S., Ignatius, R. & Feldmeier, H. (2012) Knowledge, attitudes, perceptions, and practices regarding cutaneous larva migrans in deprived communities in Manaus, Brazil. Journal of Infection in Developing Countries 6, 422429.CrossRefGoogle ScholarPubMed
Liotta, J.L., Koompapong, K.N., Yaros, J.P., Prullage, J. & Bowman, D.D. (2012) Prevalence of Ancylostoma braziliense in cats in three northern counties of Florida, United States. Journal of Parasitology 98, 10321033.CrossRefGoogle ScholarPubMed
Little, S.E., Johnson, E.M., Lewis, D., Jaklitsch, R.P., Payton, M.E., Blagburn, B.L., Bowman, D.D., Moroff, S., Tams, T., Rich, L. & Aucoin, D. (2009) Prevalence of intestinal parasites in pet dogs in the United States. Veterinary Parasitology 166, 4452.CrossRefGoogle ScholarPubMed
Mahdy, M.A., Lim, Y.A., Ngui, R., Fatimah, M., Choy, S.H., Yap, N.J., Al-Mekhlafi, H.M., Ibrahim, J. & Surin, J. (2012) Prevalence and zoonotic potential of canine hookworms in Malaysia. Parasites & Vectors 5, 88.CrossRefGoogle ScholarPubMed
Mandarino-Pereira, A., Souza, F.S., Lopes, C.W.G. & Pereira, M.J.S. (2010) Prevalence of parasites in soil and dog feces according to diagnostic tests. Veterinary Parasitology 170, 176181.CrossRefGoogle ScholarPubMed
Marques, J.P., Guimarães, C.D.R., Boas, A.V., Carnaúba, P.U. & Moraes, J. (2012) Contamination of public parks and squares from Guarulhos (São Paulo State, Brazil) by Toxocara spp. and Ancylostoma spp. Revista do Instituto de Medicina Tropical de Sao Paulo 54, 267271.CrossRefGoogle Scholar
Ngui, R., Lim, Y.A., Traub, R., Mahmud, R. & Mistam, M.S. (2012) Epidemiological and genetic data supporting the transmission of Ancylostoma ceylanicum among human and domestic animals. PLoS Neglected Tropical Diseases 6, 17.CrossRefGoogle ScholarPubMed
Palmer, C.S., Traub, R.J., Robertson, I.D., Hobbs, R.P., Elliot, A., While, L., Rees, R. & Thompson, R.C.A. (2007) The veterinary and public health significance of hookworm in dogs and cats in Australia and the status of A. ceylanicum . Veterinary Parasitology 145, 304313.CrossRefGoogle Scholar
Riggio, F., Mannella, R., Ariti, G. & Perrucci, S. (2013) Intestinal and lung parasites in owned dogs and cats from central Italy. Veterinary Parasitology 193, 7884.CrossRefGoogle ScholarPubMed
Scorza, A.V., Duncan, C., Miles, L. & Lappin, M.R. (2011) Prevalence of selected zoonotic and vector borne agents in dogs and cats in Costa Rica. Veterinary Parasitology 183, 178183.CrossRefGoogle ScholarPubMed
Soriano, S.V., Pierangeli, N.B., Roccia, I., Bergagna, H.F.J., Lazzarini, L.E., Celescinco, A., Saiz, M.S., Kossman, A., Contreras, A.P., Arias, C. & Basualdo, J.A. (2010) A wide diversity of zoonotic intestinal parasites infects urban and rural dogs in Neuquén, Patagonia, Argentina. Veterinary Parasitology 167, 8185.CrossRefGoogle Scholar
Sprenger, L.K., Green, K.T. & Molento, M.B. (2014) Geohelminth contamination of public areas and epidemiological risk factors in Curitiba, Brazil. Revista Brasileira de Parasitologia Veterinária 23, 6973.CrossRefGoogle ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28 27312739.CrossRefGoogle ScholarPubMed
Traub, R.J., Robertson, I.D., Irwin, P., Mencke, N. & Thompson, R.C.A. (2004a) Application of a species specific PCR-RFLP to identify Ancylostoma eggs directly from canine faeces. Veterinary Parasitology 123, 245255.CrossRefGoogle ScholarPubMed
Traub, R.J., Robertson, I.D., Irwin, P., Mencke, N. & Thompson, R.C.A. (2004b) The prevalence, intensities and risk factors associated with geohelminth infection in tea-growing communities of Assam, India. Tropical Medicine and International Health 9, 688701.CrossRefGoogle ScholarPubMed
Traub, R.J., Robertson, I.D., Irwin, P.J., Mencke, N. & Thompson, R.C.A. (2005) Canine gastrointestinal parasitic zoonoses in India. Trends in Parasitology 21, 4248.CrossRefGoogle ScholarPubMed
Traub, R.J., Inpankaew, T., Sutthikornchai, C., Sukthana, Y. & Thompson, R.C.A. (2008) PCR-based coprodiagnostic tools reveal dogs as reservoirs of zoonotic ancylostomiasis caused by Ancylostoma ceylanicum in temple communities in Bangkok. Veterinary Parasitology 155, 6773.CrossRefGoogle ScholarPubMed
Traversa, D., Frangipane di Regalbono, A., Di Cesare, A., La Torre, F., Drake, J. & Pietrobelli, M. (2014) Environmental contamination by canine geohelminths. Parasites & Vectors 7, 67.CrossRefGoogle ScholarPubMed