Genetic diversity of Toxoplasma gondii in animals and humans

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 364, Issue 1530, 2009, Pages 2749-2761

  David Sibley, L ^a   Khan, Asis ^a   Ajioka, James W ^b   Rosenthal, Benjamin M ^c  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Clonality; Pathogenesis; Population genetics; Recombination; Toxoplasmosis

Indexed keywords

DISEASE TRANSMISSION; GENETIC VARIATION; HOST-PARASITE INTERACTION; PARASITOLOGY; PATHOGENICITY; PROTOZOAN; PUBLIC HEALTH; RECOMBINATION; SEXUAL MATURITY; ZOOGEOGRAPHY;

EURASIA; EUROPE; NORTH AMERICA; SOUTH AMERICA;

ANIMALIA; TOXOPLASMA GONDII; VERTEBRATA;

ANIMAL; CELL CLONE; DISEASE TRANSMISSION; GENETIC VARIABILITY; GENETICS; HUMAN; IMMUNOLOGY; PARASITOLOGY; PHYLOGENY; PREVALENCE; REVIEW; TOXOPLASMA; TOXOPLASMOSIS; ZOONOSIS;

ANIMALS; CLONE CELLS; GENETIC VARIATION; HUMANS; PHYLOGENY; PREVALENCE; TOXOPLASMA; TOXOPLASMOSIS, ANIMAL; ZOONOSES;

EID: 70349311821     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2009.0087     Document Type: Review

References (137)

1. Ajioka, J. A. et al. 1998 Gene discovery by EST sequencing in Toxoplasma gondii reveals sequences restricted to the Apicomplexa. Gen. Res. 8, 18-28.
2. Ajzenberg, D., Bañuls, A. L., Tibayrenc, M. & Dardé, M. L. 2002a Microsatellite analysis of Toxoplasma gondii shows considerable polymorphism structured into two main clonal groups. Int. J. Parasitol. 32, 27-38. (doi:10.1016/ S0020-7519(01)00301-0)
3. Ajzenberg, D., Cogné, N., Paris, L., Bessieres, M. H., Thulliez, P., Fillisetti, D., Pelloux, H., Marty, P. & Dardé, M. L. 2002b Genotype of 86 Toxoplasma gondii isolates associated with human congenital toxoplasmosis and correlation with clinical findings. J. Infect. Dis. 186, 684-689. (doi: 10.1086/342663)
4. Ajzenberg, D., Bañuls, A. L., Su, C., Dumètre, A., Demar, M., Carme, B. & Dardé, M. L. 2004 Genetic diversity, clonality and sexuality in Toxoplasma gondii. Int. J. Parasitol. 34, 1185-1196. (doi:10.1016/j.ijpara.2004. 06.007)
5. Arnaud-Haond, S., Duarte, C. M., Altberto, F. & Serrão, E. A. 2007 Standardizing methods to address clonality in population studies. Mol. Ecol. 16, 5115-5139.
6. Aspinall, T V., Mariee, D., Hyde, J. E. & Sims, P. F. G. 2002 Prevalence of Toxoplasma gondii in commercial meat products as monitored by polymerase chain reaction-food for thought. Int. J. Parasitol. 32, 1193-1199. (doi:10.1016/ S0020-7519(02)00070-x)
7. Bahia-Oliveira, L. M., Jones, J. L., Azevedo-Silva, J., Alves, C. C., Orefice, F. & Addiss, D. G. 2003 Highly endemic, waterborne toxoplasmosis in north Rio de Janeiro state, Brazil. Emerg. Infect. Dis. 9, 55-62.
8. Barragan, A. & Sibley, L. D. 2003 Migration of Toxoplasma gondii across biological barriers. Trends Microbiol. 11, 426-430. (doi:10.1016/S0966- 842X(03) 00205-1)
9. Benenson, M. W., Takafuji, E. T., Lemon, S. M., Greenup, R. L. & Sulzer, A. J. 1982 Oocyst-transmitted toxoplasmosis associated with ingestion of contaminated water. N. Engl. J. Med 307, 666-669.
10. Bowie, W. R., King, A. S., Werker, D. H., Issac-Renton, J. L., Eng, S. B. & Marion, S. A. 1997 Outbreak of toxoplasmosis associated with municipal drinking water. The BC Toxoplasma investigation team. Lancet 19, 173-177. (doi:10.1016/S0140-6736(96)11105-3)
11. Boyle, J. P., Rajasekar, B., Saeij, J. P. J., Ajioka, J. W., Berriman, M., Paulsen, I., Sibley, L. D., White, M. & Boothroyd, J. C. 2006 Just one cross appears capable of dramatically altering the population biology of a eukaryotic pathogen like Toxoplasma gondii. Proc. Natl Acad. Sci. USA 103, 10 514-10 519. (doi:10.1073/pnas. 0510319103)
12. Burg, J. L., Grover, C. M., Pouletty, P. & Boothroyd, J. C. 1989 Direct and sensitive detection of a pathogenic protozoan, Toxoplasma gondii, by polymerase chain reaction. J. Clin. Microbiol. 27, 1787-1792.
13. Buxton, D., Maley, S. W., Wright, S. E., Rodger, S., Bartley, P. & Innes, E. A. 2007 Ovine toxoplasmosis: transmission, clinical outcome and control. Parassitologia 49, 219-221.
14. Carme, B. et al. 2002 Severe acquired toxoplasmsis in immunocompetent adult patients in French Guiana. J. Clin. Microbiol. 40, 4037-4044. (doi:10.1128/JCM.40.11. 4037-4044.2002)
15. Choi, W., Nam, H., Kwak, N., Huh, W., Kim, Y., Kang, M., Cho, S. & Dubey, J. P. 1997 Foodborne outbreaks of human toxoplasmosis. J. Infect. Dis. 175, 1280-1282. (doi: 10.1086/593702)
16. Cornelissen, A. W. C. A. & Overdulve, J. P. 1985 Sex determination and sex differentiation in coccidia: gametogony and oocyst production after monoclonal infection of cats with free-living and intermediate host stages of Isospora (Toxoplasma) gondii. Parassitologia 90, 35-44. (doi: 10. 1017/S003118200004899X)
17. Dardé, M. L., Bouteille, B. & Pestre-Alexandre, M. 1988 Isoenzymic characterization of seven strains of Toxoplasma gondii by isoelectrofocusing in Polyacrylamide gels. Am. J. Trop. Med. Hyg. 39, 551-558.
18. Dardé, M. L., Bouteille, B. & Pestre-Alexandre, M. 1992 Isoenzyme analysis of 35 Toxoplasma gondii isolates and the biological and epidemiological implications. J. Parasitol. 78, 786-794. (doi: 10.2307/3283305)
19. Dardé, M. L., Villena, I., Pinon, J. M. & Beguinot, I. 1998 Severe toxoplasmosis caused by a Toxoplasma gondii strain with a new isotype acquired in French Guyana. J. Clin. Microbiol. 36, 324.
20. Dawson, D. 2005 Foodborne protozoan parasites. Int. J. Food Microbiol. 103, 207-227. (doi:10.1016/ j.ijfoodmicro.2004.12.032)
21. de Moura, L. et al. 2006 Waterborne toxoplasmosis, Brazil, from field to gene. Emerg. Infect. Dis. 12, 326-329.
22. Devada, K., Anandan, R. & Dubey, J. 1998 Serologic prevalence of Toxoplasma gondii in chickens in Madras, India. J. Parasitol. 84, 621-622. (doi: 10.2307/3284735)
23. Driscoll, C. A. et al. 2007 The near eastern origin of cat domestication. Science 317, 519-523. (doi:10.1126/ science. 1139518)
24. Dubey, J. P. 1977 Toxoplasma, Hammondia, Besniotia, Sarcocystis, and other tissue cyst-forming coccidia of man and animals. In Parasitic protozoa (ed. J. P. Kreier), pp. 101-237. New York, NY: Academic Press.
25. Dubey, J. P. 1997a Bradyzoite-induced murine toxoplasmosis: stage conversion pathogenesis, and tissue cyst formation in mice fed bradyzoites of different strains of Toxoplasma gondii. J. Eukaryot. Microbiol. 44, 592-602.
26. Dubey, J. P. 1997b Tissue cyst tropism in Toxoplasma gondii: a comparison of tissue cyst formation in organs of cats, and rodents fed oocysts. Parasitolgy 115, 15-20. (doi: 10.1017/S0031182097008949)
27. Dubey, J. P. 1998a Refinement of pepsin digestion method for isolation of Toxoplasma gondii from infected tissues. Vet. Parastiol. 74, 75-77. (doi:10.1016/S03044017(97)00135-0)
28. Dubey, J. P. 1998b Toxoplasma gondii oocyst survival under defined temperatures. J. Parasitol. 84, 862-865. (doi:10. 2307/3284606)
29. 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. J. Parasitol. 87, 215-219.
30. Dubey, J. P. 2007 The life cycle of Toxoplasma gondii. In Toxoplasma: molecular and cellular biology (eds J. W Ajioka & D. Soldati), pp. 3-16. Norfolk, VA: Horizon Biosciene. (doi: 10.1017/S0031182097008949)
31. Dubey, J. P. & Beattie, C. P. 1988 Toxoplasmosis of animals and man. Boca Raton, FL: CRC Press.
32. Dubey, J. P. & Desmonts, G. 1987 Serological responses of equids fed Toxoplasma gondii oocysts. Equine Vet. J. 19, 337-339.
33. Dubey, J. P. & Frenkel, J. F 1972 Cyst-induced toxoplasmosis in cats. J. Protozool. 19, 155-177.
34. Dubey, J. P. & Frenkel, J. K. 1976 Feline toxoplasmosis from acutely infected mice and the development of Toxoplasma cysts. J. Protozool. 23, 537-546.
35. Dubey, J. P. & Thulliez, P. 1993 Persistence of tissue cysts in edible tissues of cattle fed Toxoplasma gondii oocysts. Am. J. Vet. Res. 54, 270-273.
36. Dubey, J. P., Swan, G. V & Frenkel, J. K. 1972 A simplified method for isolation of Toxoplasma gondii from the feces of cats. J. Parasitol. 58, 1005-1006. (doi:10.2307/3286603)
37. Dubey, J. P., Lunney, J. K., Shen, S. K., Kwok, O. C. H., Ashford, D. A. & Thulliez, P. 1996 Infectivity of low numbers of Toxoplasma gondii oocysts to pigs. J. Parasitol. 82, 438-443. (doi:10.2307/3284082)
38. Dubey, J. P., Speer, C. A., Shen, S. K., Kwok, O. C. H. & Blixt, J. A. 1997 Oocyst-induced murine Toxoplasmosis: life cycle, pathogenicity, and stage conversion in mice fed Toxoplasma gondii oocysts. J. Parasitol. 83, 870-882. (doi: 10.2307/3284282)
39. Dubey, J. P., Lindsay, D. S. & Speer, C. A. 1998 Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clin. Microbiol. Rev. 11, 267-299.
40. Dubey, J. P., Gamble, H. R, Hill, D. E., Sreekumar, C., Romand, S. & Thulliez, P. 2002 High prevalence of viable Toxoplasma gondii infection in market weight pigs from a farm in Massachusetts. J. Parasitol. 88, 1234-1238.
41. Dubey, J. P., Graham, D. H., Dahl, E., Hilali, M., El-Ghaysh, A., Streekumar, C., Kwok, O. C. H., Shen, S. K. & Lehmann, T. 2003a Isolation and molecular characterization of Toxoplasma gondii from chickens and ducks from Egypt. Vet. Parasitol. 114, 89-95.
42. Dubey, J. P., Graham, D. H., Dahl, E., Sreekumar, C., Lehmann, T., Davis, M. F. & Morishita, T. Y. 2003b Toxoplasma gondii isolates from free-ranging chickens from the United States. J. Parasitol. 89, 1060-1062. (doi:10.1645/GE-124R)
43. Dubey, J. P. et al. 2005a Genetic and biologic characteristics of Toxoplasma gondii isolates in free-range chickens from Colombia, South America. Vet. Parasitol. 134, 67-72. (doi:10.1016/j.vetpar.2005.07.013)
44. Dubey, J. P. et al. 2005b Prevalence of viable Toxoplasma gondii in beef, chicken, and pork from retail meat stores in the United States: risk assessment to consumer. J. Parasitol. 91, 1082-1093. (doi:10.1645/GE-683.1)
45. Dubey, J. P., Gennari, S. M., Labuna, M. B., Camargo, L. M. A., Vianna, M. C. B. & Marcet, P. L. 2006a Characterization of Toxoplasma gondii isolates from freerange chickens from Amazon, Brazil. J. Parasitol. 92, 36-40. (doi:10.1645/GE-655R.1)
46. Dubey, J. P., Patitucci, A. N., Su, C., Sundar, N., Kwok, O. C. H. & Shen, S. K. 2006b Characterization of Toxoplasma gondii isolates in free-range chickens from Chile, South America. Vet. Parasitol. 140, 76-82. (doi:10.1016/ j.vetpar.2006.03.023)
47. Dubey, J. P., Su, C. L., Oliveira, J. B., Morales, J. A., Bolanos, R. V., Sundar, N., Kwok, O. C. H. & Shen, S. K. 2006c Biologic and genetic characteristics of Toxoplasma gondii isolates in free-range chickens from Costa Rica, Central America. Vet. Parasitol. 139, 29-36. (doi:10.1016/j.vetpar.2006. 02.031)
48. Dubey, J. P. et al. 2006a Biologic and genetic characteristics of Toxoplasma gondii isolates in free-rage chickens from Nicaragua, Central America. Vet. Parasitol. 142, 47-53. (doi:10.1016/j.vetpar.2006.06.016)
49. Dubey, J. P., Zhu, X. Q., Sundar, N., Zhang, H., Kwok, O. C. & Su, C. 2007 Genetic and biologic characterization of Toxoplasma gondii isolates of cats from China. Vet. Parasitol. 145, 352-356. (doi:10.1016/j.vetpar.2006. 12.016)
50. Dubey, J. P. et al. 2008a Endemic toxoplasmosis in pigs on a farm in Maryland: isolation and genetic characterization of Toxoplasma gondii. J. Parastiol. 94, 36-41. (doi: 10. 1645/GE-1312.1)
51. Dubey, J. P., Quirk, T., Pitt, J. A., Sundar, N., Velmurugan, G. V., Kwok, O. C., Leclar, D., Hill, R & Su, C. 2008b Isolation and genetic characterization of Toxoplasma gondii from raccoons (Procyon lotor), cats (Felis domesticus), striped skunk (Mephitis mephitis), black bear (Ursus americanus), and cougar (Puma concolor) from Canada. J. Parasitol. 94,42-45. (doi:10.1645/GE-1349.1)
52. Dubey, J. P., Sundar, N., Hill, D., Velmurugan, G. V., Bandini, L. A., Kwok, O. C., Majumdar, D. & Su, C. 2008c High prevalence and abundant atypical genotypes of Toxoplasma gondii isolated from lambs destined for human consumption in the USA. Int. J. Parasitol. 38, 999-1006. (doi:10.1016/j.ijpara. 2007.11.012)
53. Dubey, J. P., Sundar, N., Nolden, C. A., Samuel, M. D., Velmurugan, G. V., Mandini, L. A., Kwok, O. C., Bodenstein, B. & Su, C. 2008d Characteristics of Toxoplasma gondii from raccoons (Procyon btor), coyotes (Canis latrans), striped skunks (Mephitis mephitis) in Wisconsin identified several atypical genotypes. J. Parasitol. 93, 1524-1527. (doi:10.1645/GE-1245.1)
54. El-Massry, A., Mahdy, O. A., El-Ghaysh, A. & Dubey, J. P. 2000 Prevalence of Toxoplasma gondii antibodies in sera of turkeys, chickens, and ducks from Egypt. J. Parasitol. 86, 627-628.
55. Falush, D., Stephens, M. & Pritchard, J. K. 2003 Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567-1587.
56. Fazaeli, A., Carter, P. E., Dardé, M. L. & Pennington, T. H. 2000 Molecular typing of Toxoplasma gondii strains by GRA6 gene sequence analysis. Int. J. Parasitol. 30, 637-642. (doi: 10.1016/S0020-7519(00)00036-9)
57. Ferguson, D. J. P., Hutchison, W. M. & Pettersen, E. 1989 Tissue cyst rupture in mice chronically infected with Toxoplasma gondii. Parasitol. Res. 75, 599-603. (doi:10. 1007/BF00930955)
58. Ferreira, A. M., Martins, M. S. & Vitor, R. W 2001 Virulence for BALB/c mice and antigenic diversity of eight Toxoplasma gondii strains isolated from animals and humans in Brazil. Parasite 8, 99-105.
59. Ferreira Ade, M., Vitor, R. W., Carneiro, A. C., Brandão, G. P. & Melo, M. N. 2004 Genetic variability of Brazilian Toxoplasma gondii strains detected by random amplified polymorphic DNA-polymerase chain reaction (RAPDPCR) and simple sequence repeat anchored-PCR (SSR-PCR). Infect. Genet. Evol. 4, 131-142. (doi:10. 1016/j.meegid.2004.03.002)
60. Ferreira, A. M., Vitor, R. W., Gazzinelli, R. T. & Melo, M. N. 2006 Genetic analysis of natural recombinant Brazilian Toxoplasma gondii strains by multilocus PCR-RFLP. Infect. Genet. Evol. 6, 22-31. (doi:10.1016/j.meegid. 2004.12.004)
61. Ferreira, I. M., Idal, J. E., Costa-Silva, T. A., Meira, C. S., Hiramoto, R. M., Penalva de Oliveira, A. C. & PereiraChioccola, V. L. 2008 Toxoplasma gondii: genotyping of strains from Brazilian AIDS patients with cerebral toxoplasmosis by multilocus PCR-RFLP markers. Exp. Parasitol. 118, 221-217. (doi:10.1016/j.exppara.2007. 08.006)
62. Frenkel, J. K. 1973 Toxoplasma in and around us. Bioscience 23, 343-352. (doi:10.2307/1296513)
63. Frenkel, J. K. & Escajadillo, A. 1987 Cyst rupture as a pathogenic mechanism of toxoplasmic encephalitis. Am. J. Trop. Med. Hyg. 36, 517-522.
64. Frenkel, J. K. & Smith, D. D. 1982 Immunization of cats against shedding of Toxoplasma oocysts. J. Parasitol. 68, 744-748. (doi:10.2307/3280978)
65. Frenkel, J. K., Ruiz, A. & Chinchilla, M. 1975 Soil survival of Toxoplasma oocysts in Kansas and Costa Rica. Am. J. Trop. Med. Hyg. 24, 439-443.
66. Frenkel, J. K., Lindsay, D. S., Parker, B. B. & Dobesh, M. 2003 Dogs as possible mechanical carriers of Toxoplama, and their fur as a source of infection of young children. Int. J. Infect. Dis. 7, 292-293. (doi:10.1016/S12019712(03)90112-3)
67. Gamble, H. R., Brady, R. C. & Dubey, J. P. 1999 Prevalence of Toxoplasma gondii infection in domestic pigs in the New England states. Vet. Parasitol. 82, 129-136. (doi:10.1016/ S0304-4017(99)00004-7)
68. Grigg, M. E. & Boothroyd, J. C. 2001 Rapid identification of virulent type I strains of the protozoan parasite Toxoplasma gondii by PCR-restriction fragment length polymorphism analysis of the Bl gene. J. Clin. Microbiol. 39, 398-400. (doi:10.1128/JCM.39.1.398400.2001)
69. Grigg, M. E., Bonnefoy, S., Hehl, A. B., Suzuki, Y. & Boothroyd, J. C. 2001a Success and virulence in Toxoplasma as the result of sexual recombination between two distinct ancestries. Science 294, 161-165. (doi:10. 1126/science.1061888)
70. Grigg, M. E., Ganatra, J., Boothroyd, J. C. & Margolis, T. P. 20016 Unusual abundance of atypical strains associated with human ocular toxoplasmosis. J. Infect. Dis. 184, 633-639. (doi:10.1086/322800)
71. Grover, C. M., Thulliez, P., Remington, J. S. & Boothroyd, J. C. 1990 Rapid prenatal diagnosis of congenital Toxoplasma infection by using polymerase chain reaction and amniotic fluid. J. Clin. Microbiol. 28, 2297-2301.
72. Guo, Z. G. & Johnson, A. M. 1995 Genetic characterization of Toxoplasma gondii strains by random amplified polymorphic DNA polymerase chain reaction. Parasitology 111, 127-132. (doi:10.1017/S0031182000064866)
73. Hall, S., Ryan, K. A. & Buxton, D. 2001 The epidemiology of toxoplasma infection. In Toxoplasmosis: a comprehensive clinical guide (eds D. H. Joynson & T J. Wreghitt), pp. 58-124. Cambridge, UK: Cambridge University Press.
74. Hide, G. et al. 2007 Does vertical transmission contribute to the prevalence of toxoplasmosis? Parassitobgia 49, 223-226.
75. Hill, D., Chirukandoth, S. & Dubey, J. P. 2005 Biology and epidemiology of Toxoplasma gondii in man and animals. Anim. Health Res. Rev. 6, 41-61. (doi:10.1079/ AHR2005100)
76. Holland, G. N. 2003 Ocular toxoplasmosis: a global reassessment. Part I: epidemiology and course of disease. Am. J. Ophthalmol. 136, 973-988. (doi:10.1016/j.ajo. 2003.09.040)
77. Holland, G. N. 2004 Ocular toxoplasmosis: a global reassessment. Part II: disease manifestations and management. Am. J. Ophthalmol. 137, 1-17. (doi:10.1016/ S0002-9394(03)01319-9)
78. 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. Int. J. Parasitol. 30, 69-75. (doi:10.1016/S00207519(99)00170-8)
79. Honoré, S., Couvelard, A., Garin, Y J., Bedel, C., Hénin, D., Dardé, M. L. & Derouin, F. 2000 Genotyping of Toxoplasma gondii strains from immunocompromised patients. Pathol. Biol. (Paris) 48, 541-547.
80. Howe, D. K. & Sibley, L. D. 1995 Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. J. Infect. Dis. 112, 1561-1566.
81. Howe, D. K., Summers, B. C. & Sibley, L. D. 1996 Acute virulence in mice is associated with markers on chromosome VIII in Toxoplasma gondii. Infect. Immun. 64, 5193-5198.
82. Howe, D. K., Honoré, S., Derouin, F. & Sibley, L. D. 1997 Determination of genotypes of Toxoplasma gondii strains isolated from patients with toxoplasmosis. J. Clin. Microbiol. 35, 1411-1414.
83. Ho-Yen, D. O. 2001 Infection in the immunocompetent. In Toxoplasmosis: a comprehensive clinical guide (eds D. H. M. Joynson & T. G. Wreghitt). Cambridge, UK: Cambridge University Press.
84. Jauregui, L. H., Higgins, J., Zarlenga, D., Dubey, J. P. & Lunney, J. K. 2001 Development of a real-time PCR assay for detection of Toxoplasma gondii in pig and mouse tissues. J. Clin. Microbiol. 39, 2065-2071. (doi:10.1128/JCM.39.6.2065-2071.2001)
85. Johnson, W. E., Eizirik, E., Pecon-Slattery, J., Murphy, W. J., Auntunes, A., Teeling, E. & O'Brien, S. J. 2006 The late miocene radiation of modern Felidae: a genetic assessment. Science 311, 73-77. (doi:10.1126/science. 1122277)
86. Jones, C. D., Okhravi, N., Adamson, P., Tasker, S. & Lightman, S. 2000 Comparison of PCR detection methods for Bl, P30, and 18S rDNA genes of T. gondii in aqueous humor. Invest. Ophthalmol. Vis. Sci. 41, 634-644.
87. Jones, J. L., Kruszon-Moran, D., Wilson, M., McQuillan, G., Navin, T. & McAuley, J. B. 2001 Toxoplasma gondii infection in the United States: seroprevalence and risk factors. Am. J. Epidemiol. 154, 357-365. (doi:10.1093/ aje/154.4.357)
88. Jones, J. L., Muccioli, C., Belfort Jr, R., Holland, G. N., Roberts, J. M. & Silveira, C. 2006 Recently acquired Toxoplasma gondii infection, Brazil. Emerg. Infect. Dis. 12, 582-587.
89. Joynson, D. H. & Wreghitt, T. J. 2001 Toxoplasmosis: a comprehensive clinical guide. Cambridge, UK: Cambridge University Press.
90. Khan, A., Su, C., German, M., Storch, G. A., Clifford, D. & Sibley, L. D. 2005a Genotyping of Toxoplasma gondii strains from immunocompromised patients reveals high prevalence of type I strains. J. Clin. Microbiol. 43, 5881-5887. (doi:10.1128/JCM.43.12.5881-5887. 2005)
91. Khan, A. et al. 2005b; Composite genome map and recombination parameters derived from three archetypal lineages of Toxoplasma gondii. Nucleic Acids Res. 33, 2980-2992. (doi:10.1093/nar/gki604)
92. Khan, A. et al. 2006a Common inheritance of chromosome Ia associated with clonal expansion of Toxoplasma gondii. Gen. Res. 16, 1119-1125. (doi:10.1101/gr. 5318106)
93. Khan, A., Jordan, C., Muccioli, C., Vallochi, A. L., Rizzo, L. V., Belfort Jr, R., Vitor, R. W., Silveira, C. & Sibley, L. D. 2006b Genetic divergence of Toxoplasma gondii strains associated with ocular toxoplasmosis Brazil. Emerg. Infect. Dis. 12, 942-949. (doi:10.3201/eidl206.060025)
94. Khan, A., Fux, B., Su, C., Dubey, J. P., Darde, M. L., Ajioka, J. W., Rosenthal, B. M. & Sibley, L. D. 2007 Recent transcontinental sweep of Toxoplasma gondii driven by a single monomorphic chromosome. Proc. Natl. Acad. Sci. USA 104, 14872-14877. (doi:10.1073/ pnas.0702356104)
95. Khan, A., Taylor, S., Ajioka, J. W., Rosenthal, B. M. & Sibley, L. D. 2009 Selection at a single locus leads to widespread expansion of Toxoplasma gondii lineages that are virulence in mice. PLoS Genet. 5, e1000404. (doi:10.1371/journal.pgen.1000404)
96. Kong, J. T., Grigg, M. E., Uyetake, L., Parmley, S. F & Boothroyd, J. C. 2003 Serotyping of Toxoplasma gondii infections in humans using synthetic peptides. J. Infect. Dis. 187, 1484-1495. (doi:10.1086/374647)
97. Lehmann, T., Marcet, P. L., Graham, D. H., Dahl, E. R. & Dubey, J. P. 2006 Globalization and the population structure of Toxoplasma gondii. Proc. Natl Acad. Sci. USA 103, 11423-11428. (doi:10.1073/pnas. 0601438103)
98. Li, L. et al. 2003 Gene discovery in the Apicomplexa as revealed by EST sequencing and assembly of a comparative gene database. Gen. Res. 13, 443-454. (doi:10.1101/gr.693203)
99. Lindstrom, I., Sundar, N., Lindh, J., Kironde, F., Kabasa, J. D., Kwok, O. C., Dubey, J. P. & Smith, J. E. 2008 Isolation and genotyping of Toxoplasma gondii from Ugandan chickens reveals frequent multiple infections. Parasitology 135,39-45. (doi:10.1017/S0031182007003654)
100. Marchall, L. G., Webb, S. D., Sepkoski Jr, J. J. & Raup, D. M. 1982 Mammalian evolution and the great American interchange. Science 215, 1351-1257. (doi:10.1126/science. 215.4538.1351)
101. McCabe, R. E. 2001 Antitoxoplasma chemotherapy. In Toxoplasmosis: a comprehensive clinical guide (eds D. H. M. Joynson & T. G. Wreghitt), pp. 319-359. Cambridge, UK: Cambridge University Press.
102. McLeod, R. et al. 2000 The child with congenital toxoplasmosis. Curr. Clin. Top. Infect. Dis. 20, 189-208.
103. Mead, P. S., Slutsker, L., Dietz, V., McCaig, L. F., Bresee, J. S., Shapiro, C., Griffin, P. M. & Tauxe, R. V. 1999 Food-related illness and death in the United States. Emerg. Infect. Dis. 5, 607-625.
104. Miller, M. A. et al. 2004 An unusual genotype of Toxoplasma gondii is common in California sea otters (Enhydra lutris nerds) and is a cause of mortality. Int. J. Parasitol. 34, 275-284. (doi:10.1016/j.ijpara.2003.12.008)
105. Mondragon, R., Howe, D. K., Dubey, J. P. & Sibley, L. D. 1998 Genotypic analysis of Toxoplasma gondii isolates in pigs. J. Parasitol. 84, 639-641. (doi:10.2307/ 3284743)
106. Mordue, D. G., Monroy, F., La Regina, M., Dinarello, C. A. & Sibley, L. D. 2001 Acute toxoplasmosis leads to lethal overproduction of Th1 cytokines. J. Immunol. 167, 4574-4584.
107. Morrissette, N. S. & Sibley, L. D. 2002 Cytoskeleton of apicomplexan parasites. Microbiol. Mol. Biol. Rev. 66, 21-38. (doi:10.1128/MMBR66.1.21-38. 2002)
108. Nowakowska, D., Colon, I., Remington, J. S., Grigg, M. E., Golab, E., Wilczynski, J. & Sibley, L. D. 2006 Genotyping of Toxoplasma gondii by multiplex PCR and peptide-based serological testing of samples from infants in Poland diagnosed with congenital toxoplasmosis. J. Clin. Microbiol. 44, 1382-1389. (doi:10.1128/JCM. 44.4.1382-1389.2006)
109. Owen, M. R. & Trees, A. J. 1999 Genotyping of Toxoplasma gondii associated with abortion in sheep. J. Parasitol. 85, 382-384. (doi:10.2307/3285654)
110. Pena, H. F., Gennari, S. M., Dubey, J. P. & Su, C. 2008 Population structure and mouse-virulence of Toxoplasma gondii in Brazil. Int. J. Parasitol. 38, 561-569. (doi:10. 1016/j.ijpara.2007.09.004)
111. Pfefferkorn, E. R., Pfefferkorn, L. C. & Colby, E. D. 1977 Development of gametes and oocysts in cats fed cysts derived from cloned trophozoites of Toxoplasma gondii. J. Parasitol. 63, 158-159. (doi:10.2307/3280129)
112. Romer, A. S. & Parsons, T S. 1977 The vertebrate body. Toronto, ON: W.B. Saunders.
113. Rosenthal, B. M. 2009 How has agriculture influenced the geography and genetics of animal parasites? Trends Parasitol. 25, 67-70. (doi:10.1016/j.pt. 2008. 10.004)
114. Saeij, J. P. J., Boyle, J. P., Coller, S., Taylor, S., Sibley, L. D., Brooke-Powell, E. T., Ajioka, J. W. & Boothroyd, J. C. 2006 Polymorphic secreted kinases are key virulence factors in toxoplasmosis. Science 314, 1780-1783. (doi:10. 1126/science.1133690)
115. Sibley, L. D. & Boothroyd, J. C. 1992 Virulent strains of Toxoplasma gondii comprise a single clonal lineage. Nature (Lond.) 359, 82-85. (doi:10.1038/359082a0)
116. Sibley, L. D., Charron, A. J., Hakansson, S. & Mordue, D. G. 2007 Invasion and intracellular survival by Toxoplasma. In Protozoans in macrophages (eds E. Y. Denkers & R. T. Gazzibelli), pp. 16-24. Austin, TX: Landes Bioscience.
117. Silveira, C., Belfort Jr, R., Muccioli, C., Abreu, M. T., Martins, M. C., Victora, C., Nussenblatt, R. B. & Holland, G. N. 2001 A follow-up study of Toxoplasma gondii infection in southern Brazil. Am. J. Ophthalmol. 131, 351-354. (doi:10.1016/S00029394(00)00830-8)
118. Smith, J. M., Smith, N. H., O'Rouke, M. & Spratt, B. G. 1993 How clonal are bacteria? Proc. Natl Acad. Sci. USA 90, 4384-4388. (doi: 10.1073/pnas.90.10.4384)
119. Sreekumar, C., Graham, D. H., Dahl, E., Lehmann, T., Raman, M., Bhalerao, D. P., Vianna, M. C. B. & Dubey, J. P. 2003 Genotyping of Toxoplasma gondii isolates from chickens from India. Vet. Parasitol. 118, 187-194. (doi:10.1016/j.vetpar.2003.10.018)
120. Su, C., Evans, D., Cole, R H., Kissinger, J. C., Ajioka, J. W & Sibley, L. D. 2003a Recent expansion of Toxoplasma through enhanced oral transmission. Science 299, 414-416. (doi:10.1126/science.1078035)
121. Su, C., Hott, C., Brownstein, B. H. & Sibley, L. D. 2003b Typing single nucleotide polymorphisms in Toxoplasma gondii by allele-specific primer extension and microarray detection. Methods Mol. Biol. Parasite Genomics Protoc. 270, 249-262. (doi:10.1385/1-59259793-9:249)
122. Su, C., Zhang, X. & Dubey, J. P. 2006 Genotyping of Toxoplasma gondii by multilocus PCR-RFLP markers: a high resolution and simple method for identification of parasites. Int. J. Parasitol. 36, 841-848. (doi:10.1016/ j.ijpara.2006.03.003)
123. Sundar, N., Cole, R. A., Thomas, N. J., Majumdar, D., Dubey, J. P. & Su, C. 2008 Genetic diversity among sea otter isolates of Toxoplasma gondii. Vet. Parasitol. 151, 125-132. (doi:10.1016/j.vetpar.2007.11.012)
124. Suzuki, Y & Joh, K. 1994 Effect of the strain of Toxoplasma gondii on the development of toxoplasmic encephalitis in mice treated with antibody to interferon-gamma. Parasitol. Res. 80, 125-130. (doi: 10. 1007/BF00933779)
125. Suzuki, Y., Conley, F. K. & Remington, J. S. 1989 Differences in virulence and development of encephalitis during chronic infection vary with the strain of Toxoplasma gondii. J. Infect. Dis. 159, 790-794.
126. Swofford, D. L. 2002 PAUP*: Phylogenetic analysis using parsimony (*andother methods). Sunderland, UK: Sinauer Associates.
127. Taylor, S. et al. 2006 A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii. Science 314, 1776-1780. (doi:10.1126/ science. 1133643)
128. Templeton, A. R., Crandall, K. A. & Sing, C. F. 1992 A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. Genetics 132, 619-633.
129. Tibayrenc, M. & Ayala, F. J. 1991 Towards a population genetics of microorganisms: the clonal theory of parasitic protozoa. Parasitol. Today 7, 228-235. (doi:10.1016/ 0169-4758(91)90234-F)
130. Tibayrenc, M., Kjellberg, F & Ayala, F. J. 1990 A clonal theory of parasitic protozoa: the population structures of Entamoeba, Giardia, Leishmania, Naegleria, Plasmodium, Trichomonas, and Trypanosoma and their medical and taxonomie consequences. Proc. Natl Acad. Sci. USA 87, 2414-2418. (doi:10.1073/pnas.87.7.2414)
131. Tibayrenc, M., Kjellberg, F., Araud, J., Oury, B., Breniere, S. F., Dardé, M. L. & Ayala, F J. 1991 Are eukaryotic microorganisms clonal or sexual? A population genetics vantage. Proc. Natl Acad. Sci. USA 88, 5129-5133. (doi:10.1073/pnas.88.12.5129)
132. Tibayrenc, M., Neubauer, K., Barnabe, C., Guerrini, F., Skarecky, D. & Ayala, F J. 1993 Genetic characterization of six parasitic protozoa: parity between random-primer DNA typing and multilocus enzyme electrophoresis. Proc. Natl Acad. Sci. 90, 1335-1339. (doi:10.1073/ pnas.90.4.1335)
133. Torrey, E. F., Bartko, J. J., Lun, Z. R & Yolken, R. H. 2007 Antibodies to Toxoplasma gondii in patients with schizophrenia: a meta-analysis. Schizophr. Bull. 33, 719-736. (doi: 10.1093/schbul/sb1050)
134. Velmurugan, G. V., Dubey, J. P. & Su, C. 2008 Genotyping studies of Toxoplasma gondii isolates from Africa revealed that the archetypal clonal lineages predominate as in North America and Europe. Vet. Parastiol. 155, 314-318. (doi:10.1016/j.vetpar.2008.04.021)
135. Vyas, A., Kim, K. S., Giacomini, N., Boothoryd, J. C. & Sapolsky, R. M. 2007 Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc. Natl Acad. Sci. USA 104, 6442-6447. (doi:10.1073/pnas.0608310104)
136. Webster, J. P. 2001 Rats, cats, people and parasites: the impact of latent toxoplasmosis on behavior. Microbes Infect. 3, 1037-1045. (doi:10.1016/S1286-4579(01) 01459-9)
137. Wong, S. & Remington, J. S. 1994 Toxoplasmosis in pregnancy. Clin. Infect. Dis. 18, 853-862.