Isolation and genotyping of Toxoplasma gondii from Ugandan chickens reveals frequent multiple infections

Parasitology

Volumn 135, Issue 1, 2008, Pages 39-45

  Lindstrom I ^a   Sundar, N ^b   Lindh, J ^c   Kironde, F ^d   Kabasa, J D ^d   Kwok, O C H ^b   Dubey, J P ^b   Smith, J E ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^d MAKERERE UNIVERSITY   (Uganda)

Author keywords

Bioassay; Chickens; Genotyping; Seroprevalence; Toxoplasma gondii; Uganda

Indexed keywords

ANTIBODY;

ANIMAL TISSUE; ARTICLE; CHICKEN; CONTROLLED STUDY; GENE LOCUS; GENETIC POLYMORPHISM; GENOTYPE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE ISOLATION; POLYMERASE CHAIN REACTION; PREVALENCE; PRIORITY JOURNAL; SUPERINFECTION; TOXOPLASMA GONDII; UGANDA; VIRULENCE;

ANIMALS; ANTIBODIES, PROTOZOAN; BASE SEQUENCE; CATS; CHICKENS; DNA, PROTOZOAN; FEMALE; GENOTYPE; MICE; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; POULTRY DISEASES; PREVALENCE; TOXOPLASMA; TOXOPLASMOSIS, ANIMAL; UGANDA;

ANIMALIA; GALLUS GALLUS; MUS; TOXOPLASMA GONDII;

EID: 37249017651     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182007003654     Document Type: Article

References (53)

1. Ajzenberg, D., Banuls, A. L., Tibayrenc, M. and Darde, M. L. (2002). Microsatellite analysis of Toxoplasma gondii shows considerable polymorphism structured into two main clonal groups. International Journal for Parasitology 32, 27-38.
2. Ajzenberg, D., Banuls, A. L., Su, C., Dumetre, A., Demar, M., Carme, B. and Darde, M. L. (2004). Genetic diversity, clonality and sexuality in Toxoplasma gondii. International Journal for Parasitology 34, 1185-1196.
3. Araujo, F., Slifer, T. and Kim, S. (1997). Chronic infection with Toxoplasma gondii does not prevent acute disease or colonization of the brain with tissue cysts following reinfection with different strains of the parasite. The Journal of Parasitology 83, 521-522.
4. Aspinall, T. V., Guy, E. C., Roberts, K. E., Joynson, D. H., Hyde, J. E. and Sims, P. F. (2003). Molecular evidence for multiple Toxoplasma gondii infections in individual patients in England and Wales: public health implications. International Journal for Parasitology 33, 97-103.
5. Bowry, T. R., Camargo, M. E. and Kinyanjui, M. (1986). Sero-epidemiology of Toxoplasma gondii infection in young children in Nairobi, Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 439-441.
6. Carme, B., Bissuel, F., Ajzenberg, D., Bouyne, R., Aznar, C., Demar, M., Bichat, S., Louvel, D., Bourbigot, A. M., Peneau, C., Neron, P. and Darde, M. L. (2002). Severe acquired toxoplasmosis in immunocompetent adult patients in French Guiana. Journal of Clinical Microbiology 40, 4037-4044.
7. Carme, B. and Demar-Pierre, M. (2006). [Toxoplasmosis in French Guiana. Atypical (neo-)tropical features of a cosmopolitan parasitosis]. Medecine Tropical 66, 495-503.
8. Dao, A., Fortier, B., Soete, M., Plenat, F. and Dubremetz, J. F. (2001). Successful reinfection of chronically infected mice by a different Toxoplasma gondii genotype. International Journal for Parasitology 31, 63-65.
9. Dubey, J. P., Miller, N. L. and Frenkel, J. K. (1970). The Toxoplasma gondii oocyst from cat feces. Journal of Experimental Medicine 132, 636-662.
10. Dubey, J. P. and Desmonts, G. (1987). Serological responses of equids fed Toxoplasma gondii oocysts. Equine Veterinary Journal 19, 337-339.
11. Dubey, J. P. and Beattie, C. P. (1988). Toxoplasmosis of Animals and Man. CRC Press, Boca Raton, FL, USA.
12. Dubey, J. P. (1995). Duration of immunity to shedding of Toxoplasma gondii oocysts by cats. The Journal of Parasitology 81, 410-415.
13. Dubey, J. P. (1998). Re-examination of resistance of Toxoplasma gondii tachyzoites and bradyzoites to pepsin and trypsin digestion. Parasitology 116, 43-50.
14. Dubey, J. P., Venturini, M. C., Venturini, L., Piscopo, M., Graham, D. H., Dahl, E., Sreekumar, C., Vianna, M. C. and Lehmann, T. (2003a). Isolation and genotyping of Toxoplasma gondii from free-ranging chickens from Argentina. The Journal of Parasitology 89, 1063-1064.
15. 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. (2003b). Isolation and molecular characterization of Toxoplasma gondii from chickens and ducks from Egypt. Veterinary Parasitology 114, 89-95.
16. Dubey, J. P., Graham, D. H., Dahl, E., Sreekumar, C., Lehmann, T., Davis, M. F. and Morishita, T. Y. (2003c). Toxoplasma gondii isolates from free-ranging chickens from the United States. The Journal of Parasitology 89, 1060-1062.
17. Dubey, J. P., Graham, D. H., Silva, D. S., Lehmann, T. and Bahia-Oliveira, L. M. G. (2003d). Toxoplasma gondii isolates of free-ranging chickens from Rio de Janeiro, Brazil: mouse mortality, genotype, and oocyst shedding by cats. The Journal of Parasitology 89, 851-853.
18. 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. (2003e). Characterization of Toxoplasma gondii isolates from free range chickens from Paraná, Brazil. Veterinary Parasitology 117, 229-234.
19. 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. (2004a). High prevalence of Toxoplasma gondii in a commercial flock of chickens in Israel, and public health implications of free-range farming. Veterinary Parasitology 121, 317-322.
20. Dubey, J. P., Levy, M., Sreekumar, C., Kwok, O. C. H., Shen, S. K., Dahl, E., Thulliez, P. and Lehmann, T. (2004b). Tissue distribution and molecular characterization of chicken isolates of Toxoplasma gondii from Peru. The Journal of Parasitology 90, 1015-1018.
21. Dubey, J. P., Morales, E. S. and Lehmann, T. (2004c). Isolation and genotyping of Toxoplasma gondii from free-ranging chickens from Mexico. The Journal of Parasitology 90, 411-413.
22. 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. (2005a). First biologic and genetic characterization of Toxoplasma gondii isolates from chickens from Africa (Democratic Republic of Congo, Mali, Burkina Faso, and Kenya). The Journal of Parasitology 91, 69-72.
23. Dubey, J. P., Edelhofer, R., Marcet, P., Vianna, M. C. B., Kwok, O. C. H. and Lehmann, T. (2005b). Genetic and biologic characteristics of Toxoplasma gondii infections in free range chickens from Austria. Veterinary Parasitology 133, 299-306.
24. Dubey, J. P., Rajapakse, R. P. V. J., Ekanayake, D. K., Sreekumar, C. and Lehmann, T. (2005c). Isolation and molecular characterization of Toxoplasma gondii from chickens from Sri Lanka. The Journal of Parasitology 92, 1480-1482.
25. 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. and Lehmann, T. (2005d). Isolation, tissue distribution, and molecular characterization of Toxoplasma gondii from chickens in Grenada, West Indies. The Journal of Parasitology 91, 557-560.
26. 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. (2005e). Genetic and biologic characteristics of Toxoplasma gondii isolates in free-range chickens from Colombia, South America. Veterinary Parasitology 134, 67-72.
27. Dubey, J. P., Lopez, B., Alveraz, M., Mendoza, C. and Lehmann, T. (2005f). Isolation, tissue distribution, and molecular characterization of Toxoplasma gondii from free-range chickens from Guatemala. The Journal of Parasitology 91, 955-957.
28. Dubey, J. P., Marcet, P. L. and Lehmann, T. (2005g). Characterization of Toxoplasma gondii isolates from free-range chickens in Argentina. The Journal of Parasitology 91, 1335-1339.
29. Dubey, J. P., Lenhart, A., Castillo, C. E., Alvarez, L., Marcet, P., Sreekumar, C. and Lehmann, T. (2005h). Toxoplasma gondii infections in chickens from Venezuela: isolation, tissue distribution, and molecular characterization. The Journal of Parasitology 91, 1332-1334.
30. Dubey, J. P., Patitucci, A. N., Su, C., Sundar, N., Kwok, O. C. and Shen, S. K. (2006a). Characterization of Toxoplasma gondii isolates in free-range chickens from Chile, South America. Veterinary Parasitology 140, 76-82.
31. Dubey, J. P., Vianna, M. C. B., Sousa, S., Canada, N., Meireles, C. S., Correia da Costa, J. M., Marcet, P. L., Lehmann, T., Dardé, M. L. and Thulliez, F. D. (2006b). Characterization of Toxoplasma gondii isolates in free-range chickens from Portugal. The Journal of Parasitology 92, 184-186.
32. Dubey, J. P., Sundar, N., Pineda, N., Kyvsgaard, N. C., Luna, L. A., Rimbaud, E., Oliveira, J. B., Kwok, O. C., Qi, Y. and Su, C. (2006c). Biologic and genetic characteristics of Toxoplasma gondii isolates in free-range chickens from Nicaragua, Central America. Veterinary Parasitology 142, 47-53.
33. Dubey, J. P., Su, C., Oliveira, J., Morales, J. A., Bolaños, R. V., Sundar, N., Kwok, O. C. H. and Shen, S. K. (2006d). Biologic and genetic characteristics of Toxoplasma gondii isolates in free-range chickens from Costa Rica, Central America. Veterinary Parasitology 139, 29-36.
34. Dubey, J. P., Webb, D. M., Sundar, N., Velmurugan, G. V., Bandini, L. M., Kwok, O. C. and Su, C. (2007a). 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, 207-212.
35. Dubey, J. P., Cortés-Vecino, J. A., Vargas-Duarte, J. J., Sundar, N., Velmurugan, G. V., Bandini, L. M., Polo, L. J., Zambrano, L., Mora, L. E., Kwok, O. C., Smith, T. and Su, C. (2007b). Prevalence of Toxoplasma gondii in dogs from Colombia, South America and genetic characterization of T. gondii isolates. Veterinary Parasitology 145, 45-50.
36. Dubey, J. P., Rajapakse, R. P., Wijesundera, R. R., Sundar, N., Velmurugan, G. V., Kwok, O. C. and Su, C. (2007c). Prevalence of Toxoplasma gondii in dogs from Sri Lanka and genetic characterization of the parasite isolates. Veterinary Parasitology 146, 341-346.
37. Dubey, J. P., Sundar, N., Gennari, S. M., Minervino, A. H., Farias, N. A., Ruas, J. L., dos Santos, T. R., Cavalcante, G. T., Kwok, O. C. and Su, C. (2007d). Biologic and genetic comparison of Toxoplasma gondii isolates in free-range chickens from the northern Para state and the southern state Rio Grande do Sul, Brazil revealed highly diverse and distinct parasite populations. Veterinary Parasitology 143, 182-188.
38. Dubey, J. P., Zhu, X. Q., Sundar, N., Zhang, H., Kwok, O. C. and Su, C. (2007e). Genetic and biologic characterization of Toxoplasma gondii isolates of cats from China. Veterinary Parasitology 145, 352-356.
39. Fuentes, I., Rubio, J. M., Ramirez, C. and Alvar, J. (2001). Genotypic characterization of Toxoplasma gondii strains associated with human toxoplasmosis in Spain: direct analysis from clinical samples. Journal of Clinical Microbiology 39, 1566-1570.
40. Fux, B., Nawas, J., Khan, A., Gill, D. B., Su, C. and Sibley, L. D. (2007). Toxoplasma gondii strains defective in oral transmission are also defective in developmental stage differentiation. Infection and Immunity 75, 2580-2590.
41. Grigg, M. E., Ganatra, J., Boothroyd, J. C. and Margolis, T. P. (2001). Unusual abundance of atypical strains associated with human ocular toxoplasmosis. The Journal of Infectious Diseases 184, 633-639.
42. Hill, D. E., Chirukandoth, S. and Dubey, J. P. (2005). Biology and epidemiology of Toxoplasma gondii in man and animals. Animal Health Research Reviews 6, 41-61.
43. Honore, S., Couvelard, A., Garin, Y. J., Bedel, C., Henin, D., Darde, M. L. and Derouin, F. (2000). [Genotyping of Toxoplasma gondii strains from immunocompromised patients]. Pathologie-biologie (Paris) 48, 541-547.
44. Howe, D. K., Honore, S., Derouin, F. and Sibley, L. D. (1997). Determination of genotypes of Toxoplasma gondii strains isolated from patients with toxoplasmosis. Journal of Clinical Microbiology 35, 1411-1414.
45. Howe, D. K. and Sibley, L. D. (1995). Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. The Journal of Infectious Diseases 172, 1561-1566.
46. Khan, A., Jordan, C., Muccioli, C., Vallochi, A. L., Rizzo, L. V., Belfort, R. Jr., Vitor, R. W., Silveira, C. and Sibley, L. D. (2006). Genetic divergence of Toxoplasma gondii strains associated with ocular toxoplasmosis, Brazil. Emerging Infectious Diseases 12, 942-949.
47. Khan, A., Su, C., German, M., Storch, G. A., Clifford, D. B. and Sibley, L. D. (2005). Genotyping of Toxoplasma gondii strains from immunocompromised patients reveals high prevalence of type I strains. Journal of Clinical Microbiology 43, 5881-5887.
48. 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, USA 103, 11423-11428.
49. Lindström, I., Kaddu-Mulindwa, D. H., Kironde, F. and Lindh, J. (2006). Prevalence of latent and reactivated Toxoplasma gondii parasites in HIV-patients from Uganda. Acta Tropica 100, 218-222.
50. Sibley, L. D. and Boothroyd, J. C. (1992). Virulent strains of Toxoplasma gondii comprise a single clonal lineage. Nature, London 359, 82-85.
51. Sreekumar, C., Graham, D. H., Dahl, E., Lehmann, T., Raman, M., Bhalerao, D. P., Vianna, M. C. B. and Dubey, J. P. (2003). Genotyping of Toxoplasma gondii isolates from chickens from India. Veterinary Parasitology 118, 187-194.
52. Wanyenya, I., Muyanja, C. and Nasinyama, G. W. (2004). Kitchen practices used in handling broiler chickens and survival of Campylobacter spp. on cutting surfaces in Kampala, Uganda. Journal of Food Protection 67, 1957-1960.
53. World Health Organization (2006). Sub-Saharan Africa 2006 AIDS Epidemic Update. http://www.who.int/hiv/mediacentre/04- Sub_Saharan_Africa_2006_EpiUpdate_eng.pdf.