Toxoplasma gondii in backyard pigs: seroepidemiology and mouse bioassay
-
Erika Fernanda Torres Samico-Fernandes
,
Marcela Fernanda Torres Samico-Fernandes
Abstract
The aim of this study was to evaluate the occurrence of Toxoplasma gondii in backyard pigs destined for human consumption in Pernambuco state, Brazil. Blood and tissue samples (liver, heart, brain, lung and diaphragm) were collected from 224 pigs from legal slaughterhouses and tested for T. gondii infection. Antibodies to T. gondii were found in the sera of 37.9% (85/224) by using the immunofluorescence antibody test (cut-off – 1:64). Tissue samples from seropositive pigs were bioassayed in mice. Tissue samples from seropositive pigs and from mice of the bioassay were submitted to histopathology, immunohistochemistry, polymerase chain reaction (PCR) and sequencing; 14.1% of pig tissue samples and 27.7% of bioassayed mouse samples were positive for T. gondii DNA, but all pig and mouse tissues were negative in histopathology analysis and immunochemistry. By using a risk assessment questionnaire, there was significant difference (p<0.001) in seroprevalence of 21.2% (reproducer) and 3.1% (finishing pig). These data serve as indicative of the sanitary conditions and risk of T. gondii infection for backyard pigs. Preventive measures must be implemented by health services to avoid toxoplasmosis human cases due to ingestion of pig meat.
Conflict of interest statement The authors declare that no competing interests exist.
Acknowledgements
The authors would like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and the Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE) for their financial support for this project (APQ 1492-5.05/12).
References
Berger-Schoch A., Herrmann D., Schares G., Müller N., Bernet D., Doherr M., et al. 2010. Incidence and genotypes of Toxoplasma gondii in the muscle of sheep, cattle and pigs in Switzerland. Veterinary Parasitology, 1, 290–97. 10.1016/j.vetpar.2010.11.046Search in Google Scholar
Bezerra R.A., Carvalho F.S., Guimarães L.A., Rocha D.S., Maciel B.M., Wenceslau A.A., et al. 2012. Genetic characterization of Toxoplasma gondii isolation from pigs intended for human consumption in Brazil. Veterinary Parasitology, 189, 153–61. org/10.1016/j.vetpar.2012.04.036Search in Google Scholar
Cademartori B.G., Santos L.M.J.F., Oliveira A.F.C., Quevedo A.P., Oliveira A.P.A., Ramos T.S., et al. 2014. Isolation and pathogenicity of Toxoplasma gondii in naturally infected (rustic farm) pigs in southern Brazil. Veterinary Parasitology, 203, 207–21. 10.1016/j.vetpar.2014.02.009Search in Google Scholar
Camargo M.E. 1974. Introduction to immunofluorescence technique. Revista Brasileira de Patologia Clínica, 10, 143–171(In Portuguese)Search in Google Scholar
Demar M., Ajzenberg D., Maubon D., Djossou F., Panchoe D., Punwasi W., et al. 2007. Fatal outbreak of human toxoplasmosis along the Maroni River: epidemiological, clinical and parasitological aspects, Clinical Infectious Diseases, 45:88–95. 10.1086/521246Search in Google Scholar
Dubey J.P. Long-term persistence of Toxoplasma gondii in tissues of pigs inoculated with T. gondii oocysts and effect of freezing on viability of tissue cysts in pork. 1988. American Journal Veterinary Research, 49, 910–3. PMID:3400928Search in Google Scholar
Dubey J.P., Weigel R.M., Siegel A.M., Thulliezt P., Kitron U.D., Mitchell M.A., et al. 1995. Sources and reservoirs of Toxoplasma gondii infection on 47 swine farms in Illinois. Journal Parasitology, 81, 723–29. PubMed: 747286210.2307/3283961Search in Google Scholar
Dubey J.P. Refinement of pepsin digestion method for isolation of Toxoplasma gondii from infected tissues. 1998. Veterinary Parasitology, 74, 75–77. 10.1016/S0304-4017(97)00135-0Search in Google Scholar
Dubey J.P., Hill D.E., Jones J.L., Hightower A.W., Kirkland E., Roberts J.M., et al. 2005. Prevalence of viable Toxoplasma gondii in beef, chicken, and pork from retail meat stores in the United States: risk assessment to consumers. Journal Parasitology, 91, 1082–93. org/10.1645/GE-683.1Search in Google Scholar
Dubey, JP. 2009. Toxoplasmosis in pigs – The last 20 years. Veterinary Parasitology, 164, 89–103. org/10.1016/j.vetpar.2009.05.018Search in Google Scholar
Dubey JP. (Ed.) 2010. Toxoplasmosis of animals and humans. Second Edition. Florida, (CRC Press). pp.336Search in Google Scholar
Dubey, J.P., Lago, E.G., Gennari, S.M., Su, C., Jones, J.L., 2012. Toxoplasmosis in humans and animals in Brazil: high prevalence, high burden of disease, and epidemiology. Parasitology. 139, 1375–142410.1017/S0031182012000765Search in Google Scholar PubMed
Feitosa T.F., Vilela V.L.R., Melo L.R.B., Neto J.L.A., Souto D.V.O., Morais D.F., et al. 2014. Toxoplasma gondii and Neospora caninum in slaughtered pigs from Northeast, Brazil. Veterinary Parasitology, 202:305– 09. 10.1016/j.vetpar.2014.03.015Search in Google Scholar PubMed
Fernandes E.F.T.S., Fernandes M.F.T.S., Kim P.C.P., DE Albuquerque P.P.F., Neto O.L.S., Santos A.S., et al. 2012. Study of Toxoplasma gondii in slaughtered swine in the state of Pernambuco, Brazil. Journal Parasitology, 98:690–91. 10.1645/GE-3032.1Search in Google Scholar
Galiza G.J.N., Tochetto C., Rosa F.B., Panziera W., Silva T.M., Caprioli R.A., et al. 2014. Usage of three immunohistochemical methods in the detection of aspergillosis and zygomycosis in animals. Pesquisa Veterinária Brasileira, 34, 637–42. org/10.1590/S0100-736X2014000700005Search in Google Scholar
Homan W.L., Vercammen M., De Braekeleer J., Verschueren H. 2000. Identification of a 200 – to 300-fold repetitive 529 bp DNA fragment in Toxoplasma gondii, and its use for diagnostic and quantitative PCR. International Journal Parasitology, 30, 69–75. org/10.1016/S0020-7519(99)00170-8Search in Google Scholar
Landis J.R., Koch G.G. 1977. The measurement of observer agreement for categorical data. Biometrics, 33, 159–7410.2307/2529310Search in Google Scholar
Luna L.G. (Ed.). 1968. Manual of histologic staining methods of the armed forces institute of pathology. New York, (McGraw-Hill Book Company). (In Portuguese)Search in Google Scholar
Oliveira P.A., Oliveira F.C., Faria L.M.J., Cademartori B.G., Pereira C.M., Coelho A.C.B., et al. 2014. Patogenicidade e virulência de Toxoplasma gondii isolado de suínos de criação artesanal no sul do Brasil. Pesquisa Veterinária Brasileira, 34, 1186–90. org/10.1590/S0100-736X2014001200007Search in Google Scholar
Piassa F.R., Araújo J.B., Rosa R.C., Mattei R.J., Silva R.C., Langoni H., et al. 2010. Prevalence and risk factors for Toxoplasma gondii infection in certified and non-certified pig breeding farms in the Toledo microregion, PR, Brazil. Revista Brasileira Parasitologia Veterinária, 19, 152–56. org/10.1590/S1984-29612010000300005Search in Google Scholar
Silva A.V., Da Silva R.C., Zamprogna T.O. 2010. Toxoplasma gondii in pigs with emphasis on the Brazilian contribution. Scince Medical, 20: 120–130. (In Portuguese)Search in Google Scholar
Swierzy I.J., Muhammad M., Kroll J., Abelmann A., Tenter A.M., Luder C.G. 2014. Toxoplasma gondii within skeletal muscle cells: a critical interplay for food-borne parasite transmission. International Journal Parasitology, 44, 91–8. 10.1016/j.ijpara.2013.10.001Search in Google Scholar PubMed
Torgerson P.R., Silva N.R., Fevre E.M., Kasuga F., Rokni M.B., Zhou X.N., et al. 2014. The global burden of foodborne parasitic diseases: an update. Trends Parasitology, 30, 20–6. 10.1016/j.pt.2013.11.002Search in Google Scholar PubMed
Thrusfield M.V. (Ed.). 2004. Veterinary Epidemiology. Second Edition. São Paulo, (Roca), pp. 556. (In Portuguese)10.1002/9781118280249Search in Google Scholar
© 2017 W. Stefański Institute of Parasitology, PAS
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- New record of Steinernema arenarium (Artyukhovsky) (Rhabditida: Steinernematidae) from Ukraine and a note on its distribution
- Isolation and molecular characterization of a Naegleria strain from a recreational water fountain in Tenerife, Canary Islands, Spain
- PCR denaturing gradient gel electrophoresis as a useful method to identify of intestinal bacteria flora in Haemaphysalis flava ticks
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- Amoebicidal activity of α-bisabolol, the main sesquiterpene in chamomile (Matricaria recutita L.) essential oil against the trophozoite stage of Acanthamoeba castellani Neff
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