Hostname: page-component-76fb5796d-r6qrq Total loading time: 0 Render date: 2024-04-26T14:14:04.869Z Has data issue: false hasContentIssue false

Validation of the modified agglutination test for the detection of Toxoplasma gondii in free-range chickens by using cat and mouse bioassay

Published online by Cambridge University Press:  02 December 2015

J. P. DUBEY*
Affiliation:
U. S. Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Animal Parasitic Diseases Laboratory, Building 1001, Beltsville, Maryland 20705-2350, USA
E. LAURIN
Affiliation:
Department of Health Management, Atlantic Veterinary College, 550 University Ave. Charlottetown, Prince Edward Island, C1A 4P3, Canada
O. C. H. KWOWK
Affiliation:
U. S. Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Animal Parasitic Diseases Laboratory, Building 1001, Beltsville, Maryland 20705-2350, USA
*
*Corresponding author. USDA, ARS, APDL, BARC-East, Building 1001, Beltsville, Maryland 20705, USA. E-mail: jitender.dubey@ars.usda.gov

Summary

The modified agglutination test (MAT) is one of the most commonly used tests for the detection of antibodies to Toxoplasma gondii in animal and human sera. The objective of the present study was to evaluate the diagnostic accuracy of the MAT and bioassay in free-range/backyard (FR) chickens (Gallus domesticus). Previously-published T. gondii test results from 2066 chickens from 19 countries were compiled for the present study. The frequency of isolation of T. gondii increased for MAT titres between 1:5 and 1:160, and ranged from 61 to 75% for antibody titres of 1:160, 1:320, and ⩾1:640. Twenty-three cats fed pooled hearts from a total of 802 FR seronegative (MAT, <1:5) chickens from several countries did not excrete oocysts, indicating a high negative predictive value of MAT because FR chickens would have been exposed to many microbes; cats are the most sensitive indicators of T. gondii infection in tissues and can excrete millions of oocysts after ingesting even a few bradyzoites. Of the 29 cats in this study, six cats, fed hearts pooled from 15–122 FR chickens, excreted oocysts; but these identifications were likely related to misidentification or prozone. Results of the present study support the validity of MAT for the detection of T. gondii infection in chickens.

Type
Research Article
Creative Commons
Parts of this are a work of the U.S. Government and not subject to copyright protection in the United States.
Copyright
Copyright © Cambridge University Press 2015

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

REFERENCES

Casartelli-Alves, L., Boechat, V. C., Macedo-Couto, R., Ferreira, L. C., Nicolau, J. L., Neves, L. B., Millar, P. R., Vicente, R. T., Oliveira, R. V. C., Muniz, A. G., Bonna, I. C. F., Amendoeira, M. R. R., Silva, R. C., Langoni, H., Schubach, T. M. P. and Menezes, R. C. (2014). Sensitivity and specificity of serological tests, histopathology and immunohistochemistry for detection of Toxoplasma gondii infection in domestic chickens. Veterinary Parasitology 204, 346351.CrossRefGoogle ScholarPubMed
da Silva, D. S., Bahia-Oliveira, L. M. G., Shen, S. K., Kwok, O. C. H., Lehmann, T. and Dubey, J. P. (2003). Prevalence of Toxoplasma gondii in chickens from an area in southern Brazil highly endemic to humans. Journal of Parasitology 89, 394396.CrossRefGoogle ScholarPubMed
Dubey, J. P. (2001). Oocyst shedding by cats fed isolated bradyzoites and comparison of infectivity of bradyzoites of the VEG strain Toxoplasma gondii to cats and mice. Journal of Parasitology 87, 215219.CrossRefGoogle ScholarPubMed
Dubey, J. P. (2010 a). Toxoplasmosis of Animals and Humans, 2nd Edn, pp. 1313. CRC Press, Boca Raton, Florida.Google Scholar
Dubey, J. P. (2010 b). Toxoplasma gondii infections in chickens (Gallus domesticus): prevalence, clinical disease, diagnosis, and public health significance. Zoonoses and Public Health 57, 6073.CrossRefGoogle ScholarPubMed
Dubey, J. P. and Desmonts, G. (1987). Serological responses of equids fed Toxoplasma gondii oocysts. Equine Veterinary Journal 19, 337339.Google Scholar
Dubey, J. P., Ruff, M. D., Camargo, M. E., Shen, S. K., Wilkins, G. L., Kwok, O. C. H. and Thulliez, P. (1993). Serologic and parasitologic responses of domestic chickens after oral inoculation with Toxoplasma gondii oocysts. American Journal of Veterinary Research 54, 16681672.Google Scholar
Dubey, J. P., Thulliez, P. and Powell, E. C. (1995). Toxoplasma gondii in Iowa sows: comparison of antibody titers to isolation of T. gondii by bioassays in mice and cats. Journal of Parasitology 81, 4853.Google Scholar
Dubey, J. P., Graham, D. H., Blackston, C. R., Lehmann, T., Gennari, S. M., Ragozo, A. M. A., Nishi, S. M., Shen, S. K., Kwok, O. C. H., Hill, D. E. and Thulliez, P. (2002). Biological and genetic characterisation of Toxoplasma gondii isolates from chickens (Gallus domesticus) from São Paulo, Brazil: unexpected findings. International Journal for Parasitology 32, 99105.Google Scholar
Dubey, J. P., Graham, D. H., Silva, D. S., Lehmann, T. and Bahia-Oliveira, L. M. G. (2003 a). Toxoplasma gondii isolates of free-ranging chickens from Rio de Janeiro, Brazil: mouse mortality, genotype, and oocyst shedding by cats. Journal of Parasitology 89, 851853.CrossRefGoogle Scholar
Dubey, J. P., Graham, D. H., Dahl, E., Hilali, M., El-Ghaysh, A., Sreekumar, C., Kwok, O. C. H., Shen, S. K. and Lehmann, T. (2003 b). Isolation and molecular characterization of Toxoplasma gondii from chickens and ducks from Egypt. Veterinary Parasitology 114, 8995.Google Scholar
Dubey, J. P., Graham, D. H., Dahl, E., Sreekumar, C., Lehmann, T., Davis, M. F. and Morishita, T. Y. (2003 c). Toxoplasma gondii isolates from free-ranging chickens from the United States. Journal of Parasitology 89, 10601062.Google Scholar
Dubey, J. P., Navarro, I. T., Graham, D. H., Dahl, E., Freire, R. L., Prudencio, L. B., Sreekumar, C., Vianna, M. C. and Lehmann, T. (2003 d). Characterization of Toxoplasma gondii isolates from free range chickens from Paraná, Brazil. Veterinary Parasitology 117, 229234.CrossRefGoogle ScholarPubMed
Dubey, J. P., Venturini, M. C., Venturini, L., Piscopo, M., Graham, D. H., Dahl, E., Sreekumar, C., Vianna, M. C. and Lehmann, T. (2003 e). Isolation and genotyping of Toxoplasma gondii from free-ranging chickens from Argentina. Journal of Parasitology 89, 10631064.Google Scholar
Dubey, J. P., Levy, M., Sreekumar, C., Kwok, O. C. H., Shen, S. K., Dahl, E., Thulliez, P. and Lehmann, T. (2004 a). Tissue distribution and molecular characterization of chicken isolates of Toxoplasma gondii from Peru. Journal of Parasitology 90, 10151018.Google Scholar
Dubey, J. P., Morales, E. S. and Lehmann, T. (2004 b). Isolation and genotyping of Toxoplasma gondii from free-ranging chickens from Mexico. Journal of Parasitology 90, 411413.Google Scholar
Dubey, J. P., Salant, H., Sreekumar, C., Dahl, E., Vianna, M. C. B., Shen, S. K., Kwok, O. C. H., Spira, D., Hamburger, J. and Lehmann, T. (2004 c). High prevalence of Toxoplasma gondii in a commercial flock of chickens in Israel, and public health implications of free-range farming. Veterinary Parasitology 121, 317322.CrossRefGoogle Scholar
Dubey, J. P., Bhaiyat, M. I., de Allie, C., Macpherson, C. N. L., Sharma, R. N., Sreekumar, C., Vianna, M. C. B., Shen, S. K., Kwok, O. C. H., Miska, K. B., Hill, D. E. and Lehmann, T. (2005 a). Isolation, tissue distribution, and molecular characterization of Toxoplasma gondii from chickens in Grenada, West Indies. Journal of Parasitology 91, 557560.Google Scholar
Dubey, J. P., Edelhofer, R., Marcet, P., Vianna, M. C. B., Kwok, O. C. H. and Lehmann, T. (2005 b). Genetic and biologic characteristics of Toxoplasma gondii infections in free-range chickens from Austria. Veterinary Parasitology 133, 299306.Google Scholar
Dubey, J. P., Gomez-Marin, J. E., Bedoya, A., Lora, F., Vianna, M. C. B., Hill, D., Kwok, O. C. H., Shen, S. K., Marcet, P. L. and Lehmann, T. (2005 c). Genetic and biologic characteristics of Toxoplasma gondii isolates in free-range chickens from Colombia, South America. Veterinary Parasitology 134, 6772.Google Scholar
Dubey, J. P., Hill, D. E., Jones, J. L., Hightower, A. W., Kirkland, E., Roberts, J. M., Marcet, P. L., Lehmann, T., Vianna, M. C. B., Miska, K., Sreekumar, C., Kwok, O. C. H., Shen, S. K. and Gamble, H. R. (2005 d). Prevalence of viable Toxoplasma gondii in beef, chicken, and pork from retail meat stores in the United States: risk assessment to consumers. Journal of Parasitology 91, 10821093.Google Scholar
Dubey, J. P., Karhemere, S., Dahl, E., Sreekumar, C., Diabaté, A., Dabiré, K. R., Vianna, M. C. B., Kwok, O. C. H. and Lehmann, T. (2005 e). First biologic and genetic characterization of Toxoplasma gondii isolates from chickens from Africa (Democratic Republic of Congo, Mali, Burkina Faso, and Kenya). Journal of Parasitology 91, 6972.Google Scholar
Dubey, J. P., Lenhart, A., Castillo, C. E., Alvarez, L., Marcet, P., Sreekumar, C. and Lehmann, T. (2005 f). Toxoplasma gondii infections in chickens from Venezuela: isolation, tissue distribution, and molecular characterization. Journal of Parasitology 91, 13321334.Google Scholar
Dubey, J. P., Marcet, P. L. and Lehmann, T. (2005 g). Characterization of Toxoplasma gondii isolates from free-range chickens in Argentina. Journal of Parasitology 91, 13351339.Google Scholar
Dubey, J. P., Rajapakse, R. P. V. J., Ekanayake, D. K., Sreekumar, C. and Lehmann, T. (2005 h). Isolation and molecular characterization of Toxoplasma gondii from chickens from Sri Lanka. Journal of Parasitology 91, 14801482.Google Scholar
Dubey, J. P., Gennari, S. M., Labruna, M. B., Camargo, L. M. A., Vianna, M. C. B., Marcet, P. L. and Lehmann, T. (2006 a). Characterization of Toxoplasma gondii isolates in free-range chickens from Amazon, Brazil. Journal of Parasitology 92, 3640.CrossRefGoogle ScholarPubMed
Dubey, J. P., Patitucci, A. N., Su, C., Sundar, N., Kwok, O. C. H. and Shen, S. K. (2006 b). Characterization of Toxoplasma gondii isolates in free-range chickens from Chile, South America. Veterinary Parasitology 140, 7682.Google Scholar
Dubey, J. P., Su, C., Oliveira, J., Morales, J. A., Bolaños, R. V., Sundar, N., Kwok, O. C. H. and Shen, S. K. (2006 c). Biologic and genetic characteristics of Toxoplasma gondii isolates in free-range chickens from Costa Rica, Central America. Veterinary Parasitology 139, 2936.Google Scholar
Dubey, J. P., Sundar, N., Pineda, N., Kyvsgaard, N. C., Luna, L. A., Rimbaud, E., Oliveira, J. B., Kwok, O. C. H., Qi, Y. and Su, C. (2006 d). Biologic and genetic characteristics of Toxoplasma gondii isolates in free-range chickens from Nicaragua, Central America. Veterinary Parasitology 142, 4753.Google Scholar
Dubey, J. P., Vianna, M. C. B., Sousa, S., Canada, N., Meireles, S., Correia da Costa, J. M., Marcet, P. L., Lehmann, T., Dardé, M. L. and Thulliez, P. (2006 e). Characterization of Toxoplasma gondii isolates in free-range chickens from Portugal. Journal of Parasitology 92, 184186.Google Scholar
Dubey, J. P., Webb, D. M., Sundar, N., Velmurugan, G. V., Bandini, L. A., Kwok, O. C. H. and Su, C. (2007). Endemic avian toxoplasmosis on a farm in Illinois: clinical disease, diagnosis, biologic and genetic characteristics of Toxoplasma gondii isolates from chickens (Gallus domesticus), and a goose (Anser anser). Veterinary Parasitology 148, 207212.Google Scholar
Dubey, J. P., Huong, L. T. T., Lawson, B. W. L., Subekti, D. T., Tassi, P., Cabaj, W., Sundar, N., Velmurugan, G. V., Kwok, O. C. H. and Su, C. (2008). Seroprevalence and isolation of Toxoplasma gondii from free-range chickens in Ghana, Indonesia, Italy, Poland, and Vietnam. Journal of Parasitology 94, 6871.CrossRefGoogle ScholarPubMed
Dubey, J. P., Rajendran, C., Costa, D. G. C., Ferreira, L. R., Kwok, O. C. H., Qu, D., Su, C., Varvulo, M. F. V., Alves, L. C., Mota, R. A. and Silva, J. C. R. (2010). New Toxoplasma gondii genotypes isolated from free-range chickens from the Fernando de Noronha, Brazil: unexpected findings. Journal of Parasitology 96, 709712.Google Scholar
Dubey, J. P., Lago, E. G., Gennari, S. M., Su, C. and Jones, J. L. (2012). Toxoplasmosis in humans and animals in Brazil: high prevalence, high burden of disease, and epidemiology. Parasitology 139, 13751424.Google Scholar
Dubey, J. P., Lehmann, T., Lautner, F., Kwok, O. C. H. and Gamble, H. R. (2015). Toxoplasmosis in sentinel chickens (Gallus domesticus) in New England farms: seroconversion, distribution of tissue cysts in brain, heart, and skeletal muscle by bioassay in mice and cats. Veterinary Parasitology. In press.Google Scholar
Lehmann, T., Marcet, P. L., Graham, D. H., Dahl, E. R. and Dubey, J. P. (2006). Globalization and the population structure of Toxoplasma gondii . Proceedings of the National Academy of Sciences of the United States of America 103, 1142311428.CrossRefGoogle ScholarPubMed
Ruiz, A. and Frenkel, J. K. (1980). Intermediate and transport hosts of Toxoplasma gondii in Costa Rica. American Journal of Tropical Medicine and Hygiene 29, 11611166.Google Scholar
Shwab, E. K., Zhu, X. Q., Majumdar, D., Pena, H. F. J., Gennari, S. M., Dubey, J. P. and Su, C. (2014). Geographical patterns of Toxoplasma gondii genetic diversity revealed by multilocus PCR-RFLP genotyping. Parasitology 141, 453461.Google Scholar