Toxoplasma gondii infection and cerebral toxoplasmosis in HIV-infected patients

Future Microbiology

Volumn 4, Issue 10, 2009, Pages 1363-1379

  Pereira Chioccola, Vera Lucia ^a   Vidal, José Ernesto ^b,c   Su, Chunlei ^d  

^a INSTITUTO ADOLFO LUTZ   (Brazil)

^b INSTITUTO DE INFECTOLOGIA EMÍLIO RIBAS   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF TENNESSEE   (United States)

Author keywords

AIDS; Cerebral toxoplasmosis; Diagnosis; Genotyping; Review; Toxoplasma gondii

Indexed keywords

ANTIPARASITIC AGENT; ANTIRETROVIRUS AGENT; ATOVAQUONE; AZITHROMYCIN; CLINDAMYCIN; CLINDAMYCIN PLUS PYRIMETHAMINE; CLOTRIMAZOLE; FOLINIC ACID; PARASITE ANTIGEN; PYRIMETHAMINE; PYRIMETHAMINE SULFADIAZINE; SULFADIAZINE; UNCLASSIFIED DRUG;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; BLOOD TOXICITY; CLINICAL TRIAL; COMPUTER ASSISTED TOMOGRAPHY; DIAGNOSTIC PROCEDURE; GENETIC VARIABILITY; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RECONSTITUTION INFLAMMATORY SYNDROME; IMMUNE RESPONSE; IMMUNOLOGICAL PROCEDURES; LIFE CYCLE; LOADING DRUG DOSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARASITE TRANSMISSION; PRIMARY PREVENTION; PRIORITY JOURNAL; REVIEW; SECONDARY PREVENTION; TOXOPLASMA GONDII; TOXOPLASMOSIS; UNSPECIFIED SIDE EFFECT; VERTICAL TRANSMISSION;

AIDS-RELATED OPPORTUNISTIC INFECTIONS; ANIMALS; BIOMEDICAL RESEARCH; GENETIC VARIATION; HIV INFECTIONS; HUMANS; TOXOPLASMA; TOXOPLASMOSIS, CEREBRAL;

TOXOPLASMA GONDII;

EID: 74749098839     PISSN: 17460913     EISSN: None     Source Type: Journal    
DOI: 10.2217/fmb.09.89     Document Type: Review

References (190)

1. Montoya JG, Liesenfeld O: Toxoplasmosis. Lancet 363(12), 1965-1976 (2004).
2. Dubey JP: Advances in the life cycle of Toxoplasma gondii. Int. J. Parasitol. 7, 1019-1024 (1998).
3. Dubey JP: History of the discovery of the life cycle of Toxoplasma gondii. Int. J. Parasitol. 39(8), 877-882 (2009).
4. Dubey JP: The history of Toxoplasma gondii - the first 100 years. J. Eukaryot. Microbiol. 55(6), 467-475 (2008).
5. Frenkel JK: Toxoplasma in and around us. Biol. Sci. 23, 343-352 (1973).
6. Cook AJ, Gilbert RE, Buffolano W et al.: Sources of Toxoplasma infection in pregnant women: European multicentre case-control study. BMJ 321, 142-147 (2000).
7. Remington JS, McLeod R, Thulliez P et al.: Toxoplasmosis. In: Infectious Diseases of the Fetus and Newborn Infant (5th Edition). Remington JS, Klein J (Eds). WB Saunders, PA, USA, 205-346 (2001).
8. Dubey JP, Gamble HR, Hill D et al.: High prevalence of viable Toxoplasma gondii infection in market weight pigs from a farm in Massachusetts. J. Parasitol. 88, 1234-1238 (2002).
9. Santos TR, Costa AJ, Toniollo GH et al.: Prevalence of anti-Toxoplasma gondii antibodies in dairy cattle, dogs, and humans from the Jauru micro-region, Mato Grosso state, Brazil. Vet. Parasitol. 161(3-4), 324-326 (2009).
10. Glasner PD, Silveira C, Kruszon-Moran D et al.: An unusually high prevalence of ocular toxoplasmosis in southern Brazil. Am. J. Ophthalmol. 114, 136-144 (1992).
11. Hill D, Dubey JP: Toxoplasma gondii: transmission, diagnosis and prevention. Clin. Microbiol. Infect. 8, 634-640 (2002).
12. Castagnini M, Bernazzali S, Ginanneschi C et al.: Fatal disseminated toxoplasmosis in a cardiac transplantation with seropositive match for Toxoplasma: should prophylaxis be extended? Transpl. Immunol. 18(2), 193-197 (2007).
13. Derouin F, Pelloux H, ESCMID Study Group on Clinical Parasitology: Prevention of toxoplasmosis in transplant patients. Clin. Microbiol. Infect. 14(12), 1089-1101 (2008). ■■ Provides an excellent overview of genetic characterization of Toxoplasma gondii strains around the world.
14. Ware PL, Kasper LH: Strain-specific antigens of Toxoplasma gondii. Infect. Immun. 55, 778-783 (1987).
15. Bohne W, Gross U, Hasemann J: Differentiation between mouse-virulent and avirulent strains of Toxoplasma gondii by monoclonal antibody recognizing a 27-kilodalton antigen. J. Clin. Microbiol. 31, 1641-1643 (1993).
16. Dardé ML, Bouteille B, Pestre-Alexandre M: Differenciation iso-enzymatique de 7 souches de Toxoplasma gondii par isoelectrofocalisation en gel de polyacrylamide. Bull. Soc. Fr. Parasitol. 5, 33-39 (1987).
17. Darde ML, Bouteille B, Pastre-Alexandre M: Isoenzyme analysis of 35 T. gondii isolates and the biological and epidemiological implications. J. Parasitol. 78, 786-794 (1992).
18. Asai T, Miura S, Sibley LD et al.: Biochemical and molecular characterization of nucleoside triphosphate hydrolase isoenzymes from the parasitic protozoan Toxoplasma gondii. J. Biol. Chem. 270, 11297-11391 (1995).
19. Darde ML: Biodiversity in Toxoplasma gondii. Curr. Top. Microbiol. Immunol. 219, 27-41 (1996).
20. Blackston CR, Dubey JP, Dotson E et al.: High-resolution typing of Toxoplasma gondii using microsatellite loci. J. Parasitol. 87, 1472-1475 (2001).
21. Ajzenberg D, Banuls AL, Su C et al.: Genetic diversity, clonality and sexuality in Toxoplasma gondii. Int. J. Parasitol. 34, 1185-1196 (2004).
22. Ajzenberg D, Banuls AL, Tibayerenc M et al.: Microsatellite ana lysis of Toxoplasma gondii shows considerable polymorphism structured into two main clonal groups. Int. J. Parasitol. 32, 27-38 (2002).
23. Lehmann T, Graham DH, Dahl ER et al.: Variation in the structure of Toxoplasma gondii and the roles of selfing, drift, and epistatic selection in maintaining linkage disequilibria. Infect. Genet. Evol. 4, 107-114 (2004).
24. Sibley LD, Boothroyd CJ: Virulent strains of T. gondii comprise a single clonal lineage. Nature 359, 82-85 (1992).
25. Howe DK, Sibley LD: T. gondii comprises three clonal lineages: correlation of parasite genotype with human disease. J. Infect. Dis. 172, 1561-1566 (1995).
26. Su C, Zhang X, Dubey JP: 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 (2006).
27. Pena HFJ, Gennari SM, Dubey JP et al.: Population structure and mouse-virulence of Toxoplasma gondii in Brazil. Int. J. Parasitol. 38, 561-569 (2008).
28. Dubey JP, Su C: Population biology of Toxoplasma gondii: what's out and where did they come from. Mem. Inst. Oswaldo Cruz 104(2), 190-195 (2009).
29. Fazaeli A, Carter PE, Pennington TH: Intergenic spacer (IGS) polymorphism: a new genetic marker for differentiation of Toxoplasma gondii strains and Neospora caninum. J. Parasitol. 86, 716-723 (2000).
30. Khan A, Jordan C, Muccioli C et al.: Genetic divergence of Toxoplasma gondii strains associated with ocular toxoplasmosis, Brazil. Emerg. Infect. Dis. 12, 942-949 (2006).
31. Khan A, Fux B, Su C et al.: Recent transcontinental sweep of Toxoplasma gondii driven by a single monomorphic chromosome. PNAS 104, 14872-14877 (2007).
32. Velmurugan GV, Dubey JP, Su C: Genotyping studies of Toxoplasma gondii isolates from Africa revealed that the archetypal clonal lineages predominate as in North America and Europe. Vet. Parasitol. 17, 155 (3-4), 314-318 (2008).
33. Grigg ME, Ganatra J, Boothroyd JC et al.: Unusual abundance of atypical strains associated with human ocular toxoplasmosis. J. Infect. Dis. 184(5), 633-639 (2001).
34. Howe KD, Honore S, Derouin F, Sibley LD: Determination of genotypes of Toxoplasma gondii strains isolated from patients with toxoplasmosis. J. Clin. Microbiol. 35, 1411-1414 (1997).
35. Khan A, Su C, German M et al.: Genotyping of Toxoplasma gondii strains from immunocompromised patients reveals high prevalence of type I strains. J. Clin. Microbiol. 43, 5881-5887 (2005).
36. Mordue DG, Monroy F, La Regina M et al.: Acute toxoplasmosis leads to lethal overproduction of Th1 cytokines. J. Immunol. 167, 4574-4584 (2001).
37. Dubey JP, Graham DH, Blackston CR et al.: Biological and genetic characterization of Toxoplasma gondii isolates from chickens (Gallus domesticus) from São Paulo, Brazil: unexpected findings. Int. J. Parasitol. 32, 99-105 (2002).
38. Dubey JP, Navarro IT, Sreekumar C et al.: Toxoplasma gondii infections in cats from Parana, Brazil: seroprevalence, tissue distribution, and biologic and genetic characterization of isolates. J. Parasitol. 90, 721-726 (2004).
39. Zakimi S, Kyan H, Oshiro M et al.: Genetic characterization of GRA6 genes from Toxoplasma gondii from pigs in Okinawa, Japan. J. Vet. Med. Sci. 68, 1105-1107 (2006).
40. Dubey JP, Sundar N, Gennari SM et al.: 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. Vet. Parasitol. 143, 182-188 (2007).
41. Belfort-Neto R, Nussenblatt V, Rizzo L et al.: High prevalence of unusual genotypes of Toxoplasma gondii infection in pork meat samples from Erechim, southern Brazil. An. Acad. Bras. Cien. 79, 111-114 (2007).
42. Ajzenberg D, Cogne N, Paris L et al.: Genotype of 86 Toxoplasma gondii isolates associated with human congenital toxoplasmosis, and correlation with clinical findings. J. Infect. Dis. 186, 684-689 (2002).
43. Nowakowska D, Colon I, Remington JS et al.: 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 (2006).
44. Vallochi A, Muccioli C, Martins M et al.: The genotype of strains causing ocular toxoplasmosis in humans in Brazil. Am. J. Ophthalmol. 139, 350-351 (2005).
45. Fuentes I, Rubio JM, Ramirez C et al.: Genotype characterization of Toxoplasma gondii strains associated with human toxoplasmosis in Spain: direct ana lysis from clinical samples. J. Clin. Microbiol. 39, 1566-1570 (2001).
46. Gallego C, Saavedra-Matiz C, Gómez-Marín JE: direct genotyping of animal and human isolates of Toxoplasma gondii from Colombia (South America). Acta Trop. 97, 161-167 (2006).
47. Ferreira IMR, Vidal JE, Costa-Silva TA et al.: Toxoplasma gondii: genotyping of strains from Brazilian AIDS patients with cerebral toxoplasmosis by multilocus PCR-RFLP markers. Exp. Parasitol. 118, 221-227 (2008).
48. Dardé ML: Genetic ana lysis of the diversity in Toxoplasma gondii. Ann. Ist. Super. Sanità 40, 57-63 (2004).
49. Lindstrom I, Kaddu-Mulindwa DH, Kironde F et al.: Prevalence of latent and reactivated Toxoplasma gondii parasites in HIV-patients from Uganda. Acta Trop. 100(3), 218-222 (2006).
50. Su C, Evans D, Cole R et al.: Recent expansion of Toxoplasma through enhanced oral transmission. Science 299, 414-416 (2003).
51. Sibley LD, Ajioka JW: Population structure of Toxoplasma gondii: clonal expansion driven by infrequent recombination and selective sweeps. Annu. Rev. Microbiol. 62, 329-351 (2008).
52. Dardé ML, Villena I, Pinon JM et al.: Severe toxoplasmosis caused by a Toxoplasma gondii strain with a new isotype acquired in French Guyana. J. Clin. Microbiol. 36, 324 (1998).
53. Ferreira AM, Vitor RWA, Gazzinelli RT et al.: Genetic ana lysis of natural recombinant Brazilian Toxoplasma gondii strains by multilocus PCR-RFLP. Infect. Genet. Evol. 6, 22-31 (2006).
54. Dubey JP, Gomez-Marin JE, Bedoya A et al.: Genetic and biologic characteristics of Toxoplasma gondii isolates in chickens from Colombia, South America. Vet. Parasitol. 134, 67-72 (2005).
55. Dubey JP, Velmurugan GV, Chockalingan A et al.: Genetic diversity of Toxoplasma gondii isolates from chickens from Brazil. Vet. Parasitol. 157, 299-305 (2008).
56. Lehmann PL, Marcet DH, Graham ER et al.: Globalization and the population structure of Toxoplasma gondii. Proc. Natl Acad. Sci. USA 103, 11423-11428 (2006).
57. Carme B, Bissuel F, Ajzenberg D et al.: Severe acquired toxoplasmosis in immunocompetent adult patients in French Guyana. J. Clin. Microbiol. 40, 4037-4044 (2002).
58. Vidal JE, Colombo FA, de Oliveira AC et al.: PCR assay using cerebrospinal fluid for diagnosis of cerebral toxoplasmosis in Brazilian AIDS patients. J. Clin. Microbiol. 42, 4765-4768 (2004).
59. Colombo FA, Vidal JE, de Oliveira AC et al.: Diagnosis of cerebral toxoplasmosis in AIDS patients in Brazil: importance of molecular and immunological methods using peripheral blood samples. J. Clin. Microbiol. 43, 5044-5047 (2005).
60. Vidal JE, Hernandez AV, Penalva de Oliveira AC et al.: Cerebral toxoplasmosis in HIV-positive patients in Brazil: clinical features and predictors of treatment response in the HAART era. AIDS Patient Care STDs 19, 840-848 (2005). ■ Provides a comprehensive review of the T. gondii antigens and host defenses.
61. Suzuki Y, Wong SY, Grumet FC et al.: Evidence for genetic regulation of susceptibility to toxoplasmic encephalitis in AIDS patients. J. Infect. Dis. 173, 265-268 (1996).
62. de Sorrentino AH, López R, Motta P et al.: HLA class II involvement in HIV-associated toxoplasmic encephalitis development. Clin. Immunol. 115(2), 133-137 (2005).
63. Dobrowolski JM, Sibley LD: Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84, 933-939 (1996).
64. Carruthers VB: Host cell invasion by the opportunistic pathogen Toxoplasma gondii. Acta Trop. 81, 111-122 (2002).
65. Zhou XW, Kafsack BFC, Cole RN et al.: The opportunistic pathogen Toxoplasma gondii deploys a diverse legion of invasion and survival proteins. J. Biol. Chem. 280, 34233-34244 (2005).
66. Duquesne V, Auriault C, Darcy F et al.: Protection of nude rats against Toxoplasma infection by excreted-secreted antigenspecific helper T-cells. Infect. Immun. 58, 2120-2126 (1990).
67. Tilley M, Fichera ME, Jerome ME et al.: Toxoplasma gondii sporozoites from a transient parasitophorous vacuole that is impermeable and contains only a subset of dense granule proteins. Infect. Immun. 65, 4598-4605 (1997).
68. Cesbron-Delauw MF, Capron A: Excreted-secreted antigens of Toxoplasma gondii: their origin and role in the host-parasite interaction. Res. Immunol. 144, 41-44 (1993).
69. Prigione I, Facchetti P, Lecordier L et al.: T cell clones raised from chronically infected healthy humans by stimulation with Toxoplasma gondii excretory-secretory antigens cross-react with live tachyzoites: characterization of the fine antigenic specificity of the clones and implications for vaccine development. J. Immunol. 7, 3741-3748 (2000).
70. Zenner L, Estaquier J, Darcy F et al.: Protective immunity in the rat model of congenital toxoplasmosis and the potential vaccinal role of excreted-secreted antigens (ESA). Parasite Immunol. 21, 261-272 (1999).
71. Costa-Silva TA, Meira CS, Ferreira IMR et al.: Evaluation of immunization with tachyzoite excreted-secreted proteins in a novel susceptible mouse model (A/Sn) for Toxoplasma gondii. Exp. Parasitol. 120, 227-234 (2008).
72. Rachinel N, Buzoni-Gatel D, Dutta C et al.: The induction of acute ileitis by a single microbial antigen of Toxoplasma gondii. J. Immunol. 173, 2725-2735 (2004).
73. Prince JB, Auer KL, Huskinson J et al.: Cloning, expression, and cDNA sequence of surface antigen P22 from Toxoplasma gondii. Mol. Biochem. Parasitol. 43, 97-106 (1990).
74. Cesbron-Delauw MF, Guy B, Torpier G et al.: Molecular characterization of a 23-kilodalton major antigen secreted by Toxoplasma gondii. Proc. Natl Acad. Sci. USA 86, 7537-7541 (1989).
75. Mevelec MN, Chardes T, Mercereau-Puijalon O et al.: Molecular cloning of GRA4, a Toxoplasma gondii dense granule protein, recognized by mucosal IgA antibodies. Mol. Biochem. Parasitol. 56, 227-238 (1992).
76. Mercier C, Lecordier L, Darcy F et al.: Molecular characterization of a dense granule antigen (Gra 2) associated with the network of the parasitophorous vacuole in Toxoplasma gondii. Mol. Biochem. Parasitol. 58, 71-82 (1993).
77. Fischer HG, Stachelhaus S, Sahm M et al.: GRA7, an excretory 29 kDa Toxoplasma gondii dense granule antigen released by infected host cells. Mol. Biochem. Parasitol. 91, 251-262 (1998).
78. Meira CS, Costa-Silva TA, Vidal JE et al.: Use of the serum reactivity against Toxoplasma gondii excreted-secreted antigen in cerebral toxoplasmosis diagnosis in HIV-infected patients. J. Med. Microbiol. 57, 845-850 (2008).
79. Suzuki Y, Conley FK, Remington JS: Importance of endogenous IFN-γ for the prevention of toxoplasmic encephalitis in mice. J. Immunol. 143, 2045-2050 (1989).
80. + T lymphocytes is required to reactivate chronic infection with Toxoplasma gondii. J. Immunol. 149(1), 175-180 (1992).
81. Denkers EY, Gazzinelli RT: Regulation and function of T-cell-mediated immunity during Toxoplasma gondii infection. Clin. Microbiol. Rev. 11(4), 569-588 (1998).
82. Yap G, Pesin M, Sher A: IL-12 is required for the maintenance of IFN-γ production in T cells mediating chronic resistance to the intracellular pathogen, Toxoplasma gondii. J. Immunol. 165, 628-631(2000).
83. Denkers EY: From cells to signaling cascades: manipulation of innate immunity by Toxoplasma gondii. FEMS Immunol. Med. Microbiol. 39(3), 193-203 (2003).
84. Khan IA, Matsuura T, Kasper LH: Interleukin-12 enhances murine survival against acute toxoplasmosis Infect. Immun. 62(5), 1639-1642 (1994).
85. Schlüter D, Kaefer N, Hof H et al.: Expression pattern and cellular origin of cytokines in the normal and Toxoplasma gondii-infected murine brain. Am. J. Pathol. 150, 1021-1035 (1997).
86. Schlüter D, Kwok LY, Lütjen S et al.: Both lymphotoxin-α and TNF are crucial for control of Toxoplasma gondii in the central nervous system. J. Immunol. 170(12), 6172-6182 (2003). ■■ Described the several analytical approaches, methods and tools for cerebral toxoplasmosis diagnosis in AIDS.
87. Elbez-Rubinstein A, Ajzenberg D, Dardé ML et al.: Congenital toxoplasmosis and reinfection during pregnancy: case report, strain characterization, experimental model of reinfection, and review. J. Infect. Dis. 199, 280-285 (2009).
88. Luft BJ, Chua A: Central nervous system toxoplasmosis in HIV: pathogenesis, diagnosis, and therapy. Curr. Infect. Dis. 2, 358-362 (2000).
89. Korman AJ, Boss JM, Spies T et al.: Genetic complexity expression of human class II histocompatibility antigens. Immunol. Rev. 85, 45-86 (1995).
90. Kaslow RA, McNicholl JM: Genetic determinants of HIV-1 infection and its manifestations. Proc. Assoc. Am. Physicians 111, 299-307 (1999).
91. Price P, Keane NM, Stone SF et al.: French, MHC haplotypes affect the expression of opportunistic infections in HIV patients. Hum. Immunol. 62, 154-164 (2001).
92. Kaslow RA, Carrington M, Apple R et al.: Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat. Med. 2, 410-412 (1996).
93. Rodrigues MV, Demarco ALG, Donadi EA et al.: HLA class I profile in patients with AIDS and Toxoplasma gondii chorioretinitis. Invest. Ophthalmol. Vis. Sci. 45, E-1672 (2004).
94. Castro Figueiredo JF, de Lourdes Veronese RM, Costa Passos AD et al.: HLA typing in patients with AIDS and neurotoxoplasmosis. Presented at: XIII International AIDs Conference. Durban, South Africa, 9-14 July, 2000 (Abstract MoPeB2141).
95. Sorrentino AH, López R, Motta P et al.: HLA class II involvement in HIV-associated toxoplasmic encephalitis development. Clin. Immunol. 115, 133-137 (2005).
96. Cintra JR, Pereira-Chioccola VL, de Mattos CCB et al.: Haplótipos HLA-DR na suscetibilidade e resistência à toxoplasmose cerebral em pacientes com AIDS. Rev. Patol. Trop. 38(2), 62 (2009).
97. Portegies P, Solod L, Cinque P et al.: Guidelines for the diagnosis and management of neurological complications of HIV infection. Eur. J. Neurol. 11, 297-304 (2004).
98. Guimarães M: Temporal trends in AIDSassociated opportunistic infections in Brazil, 1980-1999. Cad. Saúde Pública. 16(Suppl. 1), 21-36 (2000).
99. Abgrall S, Rabaud C, Costagliola D et al.: Incidence and risk factors for toxoplasmic encephalitis in human immunodeficiency virus-infected patients before and during the highly active antiretroviral therapy. Clin. Infect. Dis. 53, 1747-1755 (2001).
100. Gaspar G, Monereo A, Barros C et al.: Incidence of first episodes of HIV: opportunistic diseases and its changes over time in the period 1987-2001 in the COMESEM Cohort Study. Presented at: 14th International AIDS Conference. Barcelona, Spain, 7-12 July 2002 (Abstract ThPeC7458).
101. Antinori A, Ammassari A, De Luca A et al.: Diagnosis of AIDS-related focal brain lesions: a decision-making ana lysis based on clinical and neuroradiologic characteristics combined with polymerase chain reaction assays in CSF. Neurology 48, 687-694 (1997).
102. Vidal JE, de Oliveira AC, Fink MC et al.: AIDS-related progressive multifocal leukoencephalopathy: a retrospective study in a referral center in São Paulo, Brazil. Rev. Inst. Med. Trop. Sao Paulo 50, 209-212 (2008).
103. Manzardo C, Del Mar Ortega M, Sued O, Garcia F, Moreno A, Miro JM: Central nervous system opportunistic infections in developed countries in the highly active antiretroviral therapy era. Neurovirology 11(Suppl. 3), 72-82 (2005).
104. Harrison MJ, McArthur JC: Opportuistic infections - parasites. In: Clinical Neurology and Neurosurgery Monographs. Harrison MJ, McArthur JC (Eds). Churchill Livingstone, Edinburgh, Scotland, 171-181 (1995).
105. Dal Pan GJ, McArthur JC: Neuroepidemiology of HIV infection. Neurol. Clin. 14, 359-382 (1996).
106. Bahia-Oliveira LM, Jones JL, Azevedo-Silva J et al.: Highly endemic, waterborne toxoplasmosis in north Rio de Janeiro State, Brazil. Emerg. Infect. Dis. 9, 55-62 (2003).
107. Mamidi A, DeSimone JA, Pomerantz RJ: Central nervous system infections in individuals with HIV-1 infection. J. Neurovirol. 8, 158-167 (2002).
108. Vidal JE, Dauar RF, de Oliveira AC: Utility of brain biopsy in patients with acquired immunodeficiency syndrome before and after introduction of highly active antiretroviral therapy. Neurosurgery 63, E1209 (2008).
109. Trujillo JR, Jaramillo-Rangel G, Ortega-Martinez M et al.: International NeuroAIDS: prospects of HIV-1 associated neurological complications. Cell Res. 15, 962-969 (2005).
110. Vidal JE, Hernández AV, Penalva de Oliveira AC et al.: Cerebral tuberculomas in AIDS patients: a forgotten diagnosis? Arq. Neuropsiquiatr. 62(3B), 793-796 (2004).
111. Vidal JE, de Oliveira AC, Leite AG et al.: Tuberculous brain abscess in AIDS patients: report of three cases and literature review. Int. J. Infect. Dis. 9, 201-207 (2005).
112. Bretagne S, Costa JM, Foulet F et al.: Prospective study of Toxoplasma reactivation by polymerase chain reaction in allogenic stem-cell transplant recipient. Transpl. Infect. Dis. 2, 127-132 (2000).
113. Bastien P: Molecular diagnosis of toxoplasmosis. Trans. R. Soc. Trop. Med. Hyg. 96(Suppl. 1), S205-S215 (2002).
114. Skiest DJ: Focal neurological disease in patients with acquired immunodeficiency syndrome. Clin. Infect. Dis. 34, 103-115 (2002).
115. Collazos J: Opportunistic infections of the CNS in patients with AIDS. CNS Drugs 17, 869-887 (2003).
116. Moulignier A: HIV and the central nervous system. Rev. Neurol. (Paris) 162(1), 22-42 (2006).
117. Remington JS, Thulliez P, Montoya JG: Recent developments for diagnosis of toxoplasmosis. J. Clin. Microbiol. 42 (3), 941-945 (2004).
118. Raffi F, Aboulker JP, Michelet C et al.: A prospective study of criteria for the diagnosis of toxoplasmic encephalitis in 186 AIDS patients. The BIOTOXO Study Group. AIDS 11(2), 177-184 (1997).
119. Mechain B, Garin YJ, Robert-Gangneux F et al.: Lack of utility of specific immunoglobulin G antibody avidity for serodiagnosis of reactivated toxoplasmosis in immunocompromised patients. Clin. Diagn. Lab. Immunol. 7, 703-705 (2000).
120. Luft BJ, Remington JS: Toxoplasmic encephalitis in AIDS. Clin. Infect. Dis. 15, 211-222 (1992).
121. Sadler M, Brink NS, Gazzard BG: Management of intracerebral lesions in patients with HIV: a retrospective study with discussion of diagnostic problems. QJM 91(3), 205-217 (1998).
122. Contini C: Clinical and diagnostic management of toxoplasmosis in the immunocompromised patient. Parassitologia 50(1-2), 45-50 (2008).
123. Derouin F, Leport C, Pueyo S et al.: Predictive value of Toxoplasma gondii antibody titres on the occurrence of toxoplasmic encephalitis in HIV-infected patients. AIDS 10, 1521-1527 (1996).
124. Hellerbrand C, Goebel FD, Disko R: High predictive value of Toxoplasma gondii IgG antibody levels in HIV-infected patients for diagnosis of cerebral toxoplasmosis. Eur. J. Clin. Microbiol. Infect. Dis. 15, 869-872 (1996).
125. Antinori A, Larussa D, Cingolani A et al.: Prevalence, associated factors, and prognostic determinants of AIDS-related toxoplasmic encephalitis in the era of advanced highly active antiretroviral therapy. HIV/AIDS 39, 1681-1691 (2004).
126. Pietkiewicz H, Hiszczynska-Sawicka E, Kur J et al.: Usefulness of Toxoplasma gondii-specific recombinant antigens in serodiagnosis of human toxoplasmosis. J. Clin. Microbiol. 42, 1779-1781 (2004).
127. Hiszczynska-Sawicka E, Kur J, Pietkiewicz H et al.: Efficient production of the Toxoplasma gondii GRA6, p35 and SAG2 recombinant antigens and their applications in the serodiagnosis of toxoplasmosis. Acta Parasitol. 50, 249-254 (2005).
128. Pfrepper KI, Enders G, Gohl M et al.: Seroreactivity to and avidity for recombinant antigens in toxoplasmosis. Clin. Diagn. Lab. Immunol. 12(8), 977-982 (2005).
129. Beghetto E, Spadoni A, Bruno L et al.: Chimeric antigens of Toxoplasma gondii: toward standardization of toxoplasmosis serodiagnosis using recombinant products. J. Clin. Microbiol. 44(6), 2133-2140 (2006).
130. Holec L, Gasior A, Brillowska-Dabrowska A et al.: Toxoplasma gondii: enzyme-linked immunosorbent assay using different fragments of recombinant microneme protein 1 (MIC1) for detection of immunoglobulin G antibodies. Exp. Parasitol. 119(1), 1-6 (2008).
131. Carruthers VB, Sibley LD: Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur. J. Cell Biol. 73, 114-123 (1997).
132. Dubremetz JF: Host cell invasion by Toxoplasma gondii. Trends Microbiol. 6, 27-30 (1998).
133. Cerede O, Dubremetz JF, Soete M et al.: Synergistic role of micronemal proteins in Toxoplasma gondii virulence. J. Exp. Med. 201, 453-463 (2005).
134. Zeman A, McLean B, Keir G et al.: The significance of serum oligoclonal bands in neurological diseases. J. Neurol. Neurosurg. Psych. 56(1), 32-35 (1993).
135. Potasman I, Resnick L, Benjamin J et al.: Intrathecal production of antibodies against Toxoplasma gondii in patients with toxoplasmic encephalitis and the acquired immunodeficiency syndrome AIDS. Ann. Int. Med. 108, 49-51 (1988).
136. Contini C, Fainardi E, Cultrera R et al.: Advanced laboratory techniques for diagnosing Toxoplasma gondii encephalitis in AIDS patients: significance of intrathecal production and comparison with PCR and ECL western blotting. J. Neuroimmunol. 92, 29-37 (1998).
137. Dupouy-Camet J, de Souza SL, Maslo C et al.: Detection of Toxoplasma gondii in venous blood from AIDS patients by polymerase chain reaction. J. Clin. Microbiol. 31, 1866-1869 (1993).
138. Dupon M, Cazenave J, Pellegrin JL et al.: Detection of Toxoplasma gondii by PCR and tissue culture in cerebrospinal fluid and blood of human immunodeficiency virusseropositive patients. J. Clin. Microbiol. 33, 2421-2426 (1995).
139. Cingolani A, De Luca A, Ammassari A et al.: PCR detection of Toxoplasma gondii DNA in CSF for the differential diagnosis of AIDS-related focal brain lesions. J. Med. Microbiol. 45, 472-476 (1996).
140. Montoya JG, Parmley S, Liesenfeld O et al.: Use of the polymerase chain reaction for diagnosis of ocular toxoplasmosis. Ophthalmology 106, 1554-1563 (1999).
141. Jones CD, Okhravi N, Adamson P et al.: Comparison of PCR detection methods for B1, P30, and 18S rDNA genes of Toxoplasma gondii in aqueous humor. Invest. Ophthalmol. Vis. Sci. 41, 634-644 (2000).
142. Julander I, Matin C, Lappalainen M et al.: Polymerase chain reaction for diagnosis of cerebral toxoplasmosis in cerebrospinal fluid in HIV-positive patients. Scand. J. Infect. Dis. 33, 538-541 (2001).
143. Romand S, Wallon M, Franck J et al.: Prenatal diagnosis using polymerase chain reaction on amniotic fluid for congenital toxoplasmosis. Obstet. Gynecol. 97, 296-300 (2001).
144. Mele A, Paterson PJ, Prentice HG et al.: Toxoplasmosis in bone marrow transplantation: a report of two cases and systematic review of the literature. Bone Marrow Transplant. 29, 691-698 (2002).
145. Chabbert E, Lachaud L, Crobu L et al.: Comparison of two widely used PCR primer systems for detection of Toxoplasma in amniotic fluid, blood and tissues. J. Clin. Microbiol. 42, 1719-1722 (2004).
146. Edvinsson B, Lundquist J, Ljungman P et al.: A prospective study of diagnosis of Toxoplasma gondii infection after bone marrow transplantation. APMIS 116(5), 345-351 (2008).
147. Novati R, Castagna A, Morisca G et al.: Polymerase chain reaction for Toxoplasma gondii DNA in the cerebrospinal fluid of AIDS patients with focal brain lesions. AIDS 8, 1691-1694 (1994).
148. Pelloux H, Dupouy-Camet J, Derouin F et al.: A multicentre prospective study for the polymerase chain reaction detection of Toxoplasma gondii DNA in blood samples from 186 AIDS patients with suspected toxoplasmic encephalitis. AIDS 11, 1888-1890 (1997).
149. Priya J, Calderón MM, Gilman RH et al.: Optimization and evaluation of a PCR assay for detecting toxoplasmic encephalitis in patients with AIDS. J. Clin. Microbiol. 40, 4499-4503 (2002).
150. Bastien P, Procop GW, Reischl U: Quantitative real-time PCR is not more sensitive than "conventional" PCR. J. Clin. Microbiol. 46(6), 1897-1900 (2008).
151. Hierl T, Reischl U, Lang P et al.: Preliminary evaluation of one conventional nested and two real-time PCR assays for the detection of Toxoplasma gondii in immunocompromised patient. J. Med. Microbiol. 53, 629-632 (2004).
152. Apfalter P, Reischl U, Hammerschlag MR: In-house nucleic acid amplification assays in research: how much quality control is needed before one can rely upon the results? J. Clin. Microbiol. 43, 5835-5841 (2005).
153. Bretagne S: Molecular diagnostics in clinical parasitology and mycology: limits of the current polymerase chain reaction (PCR) assays and interest of the real-time PCR assays. Clin. Microbiol. Infect. 9, 505-511 (2003).
154. Gianotti N, Cinque P, Castagna A et al.: Diagnosis of toxoplasmic encephalitis in HIV-infected patients. AIDS 11, 1529-1530 (1997).
155. Lee CN, Cavanagh HM, Lo ST et al.: Human papillomavirus infection in non-neoplastic uterine cervical disease in Hong Kong. Br. J. Biomed. Sci. 58, 85-91 (2001).
156. Burg JL, Perelman D, Kasper LH et al.: Molecular ana lysis of the gene encoding the major surface antigen of Toxoplasma gondii. J. Immunol. 141, 3584-3591 (1988).
157. Burg JL, Grover CM, Pouletty P et al.: Direct and sensitive detection of a pathogenic protozoan, Toxoplasma gondii, by polymerase chain reaction. J. Clin. Microbiol. 27, 1787-1792 (1989).
158. Homan WL, Vercammenb M, De Braekeleer J et al.: 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 (2000).
159. Kupferschmidt O, Krüger D, Held TK et al.: Quantitative detection of Toxoplasma gondii DNA in human body fluids by TaqMan polymerase chain reaction. Clin. Microbiol. Infect. 7(3), 120-124 (2001).
160. Reischl U, Bretagne S, Krüger D et al.: Comparison of two DNA targets for the diagnosis of toxoplasmosis by real-time PCR using fluorescence resonance energy transfer hybridization probes. BMC Infect. Dis. 3, 7-9 (2003).
161. Contini C, Seraceni S, Cultrera R et al.: Evaluation of a real-time PCR-based assay using the light cycler system for detection of Toxoplasma gondii bradyzoite genes in blood specimens from patients with toxoplasmic retinochoroiditis. Int. J. Parasitol. 35, 275-283 (2005).
162. Switaj K, Master A, Skrzypczak M et al.: Recent trends in molecular diagnostics for Toxoplasma gondii infections. Clin. Microbiol. Infect. 11, 170-176 (2005).
163. Calderaro A, Piccolo G, Gorrini C et al.: Comparison between two real-time PCR assays and a nested-PCR for the detection of Toxoplasma gondii. Acta Biomed. 77, 75-80 (2006).
164. Grover CM, Thulliez P, Remington JS et al.: Rapid prenatal diagnosis of congenital Toxoplasma infection by using polymerase chain reaction and amniotic fluid. J. Clin. Microbiol. 28, 2297-2301 (1990).
165. Cassaing S, Bessières MH, Berry A et al.: Comparison between two amplification sets for molecular diagnosis of toxoplasmosis by real-time PCR. J. Clin. Microbiol. 44, 720-724 (2006).
166. Costa JM, Pautas C, Ernault P et al.: Real-time PCR for diagnosis and follow-up of Toxoplasma reactivation after allogeneic stem cell transplantation using fluorescence resonance energy transfer hybridization probes. J. Clin. Microbiol. 38, 2929-2932 (2000).
167. Edvinsson B, Lappalainen M, Evengard B et al.: Real-time PCR targeting a 529-bp repeat element for diagnosis of toxoplasmosis. Clin. Microbiol. Infect. 12, 131-136 (2006).
168. Jalal S, Nord CE, Lappalainen M et al.: Rapid and sensitive diagnosis of Toxoplasma gondii infections by PCR. Clin. Microbiol. Infect. 10, 937-939 (2004).
169. Mesquita RT, Pereira-Chioccola VL: Molecular diagnosis of cerebral toxoplasmosis: comparison of markers for use in PCR for Toxoplasma gondii determination. Abstract book of Toxoplasma Centennial Congress. 33 (2008).
170. Mesquita RT, Ziegler AP, Kawarabayashi M et al.: Avaliação da PCR em tempo real no diagnóstico molecular da toxoplasmose cerebral. Rev. Brasil. Med. Trop. 42, 149 (2009).
171. Okay TS, Yamamoto L, Oliveira LC et al.: Significant performance variation among PCR systems in diagnosing congenital toxoplasmosis in São Paulo, Brazil: ana lysis of 467 amniotic fluid samples. Clinics 64, 171-176 (2009).
172. Dannemann B, McCutchan JA, Israelski D et al.: Treatment of toxoplasmic encephalitis in patients with AIDS. A randomized trial comparing pyrimethamine plus clindamycin to pyrimethamine plus sulfadiazine. The California Collaborative Treatment Group. Ann. Intern. Med. 116 (1), 33-43 (1992).
173. Katlama C, Mouthon B, Gourdon D et al.: Atovaquone as long-term suppressive therapy for toxoplasmic encephalitis in patients with AIDS and multiple drug intolerance. Atovaquone Expanded Access Group. AIDS 10(10), 1107-1112 (1996).
174. Torre D, Casari S, Speranza F et al.: Randomized trial of trimethoprimsulfamethoxazole versus pyrimethamine-sulfadiazine for therapy of toxoplasmic encephalitis in patients with AIDS. Italian Collaborative Study Group. Antimicrob. Agents Chemother. 42, 1346-1349 (1998).
175. Dedicoat M, Livesley N: Management of toxoplasmic encephalitis in HIV-infected adults (with an emphasis on resource-poor settings). Cochrane Database Syst. Rev. 19(3), CD005420 (2006).
176. Canessa A, Del Bono V, De Leo P, Piersantelli N, Terragna A: Cotrimoxazole therapy of Toxoplasma gondii encephalitis in AIDS patients. Eur. J. Clin. Microbiol. Infect. Dis. 11, 125-130 (1992).
177. Francis P, Patel VB, Bill PL, Bhigjee AI: Oral trimethoprim- sulfamethoxazole in the treatment of cerebral toxoplasmosis in AIDS patients - a prospective study. S. Afr. Med. J. 94, 51-53 (2004).
178. Arens J, Barnes K, Crowley N, Maartens G: Treating AIDS associated cerebral toxoplasmosis: pyrimethamine plus sulfadiazine compared with cotrimoxazole, and outcome with adjunctive glucocorticoids. S. Afr. Med. J. 97, 956-958 (2007).
179. Béraud G, Pierre-François S, Foltzer A et al.: Cotrimoxazole for treatment of cerebral toxoplasmosis: an observational cohort study during 1994-2006. Am. J. Trop. Med. Hyg. 80, 583-587 (2009).
180. CDC: Guidelines for prevention and treatment of opportunistic infections in HIV-infected adults and adolescents. Recommendations from CDC, the National Institutes of Health, and the HIV Medicine Association of the Infectious Diseases Society of America. MMWR 58(No. RR-4), 1-207 (2009).
181. Jordan MK, Burstein AH, Rock-Kress D et al.: Plasma pharmacokinetics of sulfadiazine administered twice daily versus four times daily are similar in human immunodeficiency virus-infected patients. Antimicrob. Agents Chemother. 48, 635-637 (2004).
182. Duval X, Pajot O, Le Moing V et al.: Maintenance therapy with cotrimoxazole for toxoplasmic encephalitis in the era of highly active antiretroviral therapy. AIDS 18, 1342-1344 (2004).
183. Pfeffer G, Prout A, Hooge J, Maguire J: Biopsy-proven immune reconstitution syndrome in a patient with AIDS and cerebral toxoplasmosis. Neurology 73, 321-322 (2009).
184. Sundar N, Cole RA, Thomas NJ et al.: Genetic diversity among sea otter isolates of Toxoplasma gondii. Vet. Parasitol. 151, 125-132 (2008).
185. Prestrud KW, Sbakk KA, Mørk T et al.: Direct high-resolution genotyping of Toxoplasma gondii in arctic foxes (Vulpes lagopus) in the remote arctic Svalbard archipelago reveals widespread clonal type II lineage. Vet. Parasitol. 158, 121-128 (2008).
186. Peyron F, Lobry JR, Musset K et al.: Serotyping of Toxoplasma gondii in chronically infected pregnant women: predominance of type II in Europe and types I and III in Colombia (South America). Microb. Infect. 8, 2333-2340 (2006).
187. Kong JT, Grigg ME, Uyetake L et al.: Serotyping of Toxoplasma gondii infections in humans using synthetic peptides. J. Infect. Dis. 187, 1484-1495 (2003).
188. Frenkel JF, Vidal JE: Toxoplasmose. In: Tratado de Infectologia (4th Edition). Veronesi R, Focaccia R (Eds). Atheneu, São Paulo, Brazil (2010) (In Press).
189. Dubey JP: Toxoplasma gondii. In: Medical Microbiology (5th Edition). Baron SR, Peake C, James DA et al. (Eds). The University of Texas, TX, USA (1996). www.ncbi.nlm.nih.gov/bookshelf/br. fcgi?book=mmed ■■ Exceptionally useful as an overview of T. gondii studies.
190. ToxoDB: the Toxoplasma gondii genome resource. www.toxodb.org/toxo/home.jsp.