Diagnosis of toxoplasmosis and typing of Toxoplasma gondii

Parasites and Vectors

Volumn 8, Issue 1, 2015, Pages

  Liu, Quan ^a,b   Wang, Ze Dong ^b   Huang, Si Yang ^a,c   Zhu, Xing Quan ^a,c  

^a Lanzhou Veterinary Research Institute   (China)

^b BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^c YANGZHOU UNIVERSITY   (China)

Author keywords

Diagnosis; Genetic characterization; Genotyping; Serotyping; Toxoplasma gondii; Toxoplasmosis

Indexed keywords

DNA; DYE; NUCLEIC ACID; POLYPEPTIDE;

AGGLUTINATION TEST; BIOASSAY; COMPUTER ASSISTED TOMOGRAPHY; DIAGNOSTIC ACCURACY; ECHOGRAPHY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; GENOTYPE; HIGH RESOLUTION MELTING ANALYSIS; IMMUNOAFFINITY CHROMATOGRAPHY; IMMUNOSORBENT AGGLUTINATION ASSAY; INDIRECT AGGLUTINATION TEST; LATEX AGGLUTINATION TEST; LOOP MEDIATED ISOTHERMAL AMPLIFICATION; MICROSATELLITE MARKER; MODIFIED AGGLUTINATION TEST; MOLECULAR DIAGNOSIS; MOLECULAR TYPING; MULTILOCUS SEQUENCE TYPING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PIEZOELECTRIC IMMUNOAGGLUTINATION ASSAY; POLYMERASE CHAIN REACTION; RANDOM AMPLIFIED POLYMORPHIC DNA; REVIEW; SEROLOGY; SEROTYPING; TACHYZOITE; TOXOPLASMOSIS; WESTERN BLOTTING; ANIMAL; CLASSIFICATION; DIAGNOSTIC TEST; GENETICS; HUMAN; IMMUNOLOGY; ISOLATION AND PURIFICATION; PARASITOLOGY; PROCEDURES; TOXOPLASMA;

ANIMALIA; PROTOZOA; TOXOPLASMA GONDII;

ANIMALS; DIAGNOSTIC TESTS, ROUTINE; HUMANS; TOXOPLASMA; TOXOPLASMOSIS;

EID: 84930618712     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/s13071-015-0902-6     Document Type: Review

References (200)

1. Liu Q, Singla LD, Zhou H. Vaccines against Toxoplasma gondii: status, challenges and future directions. Hum Vacc Immunother. 2012;8:1305-8.
2. Moncada PA, Montoya JG. Toxoplasmosis in the fetus and newborn: an update on prevalence, diagnosis and treatment. Expert Rev Anti Infect Ther. 2012;10:815-28.
3. Dubey JP. The history of Toxoplasma gondii-the first 100 years. J Eukaryot Microbiol. 2008;55:467-75.
4. Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: from animals to humans. Int J Parasitol. 2000;30:1217-58.
5. Paul M. Immunoglobulin G avidity in diagnosis of toxoplasmic lymphadenopathy and ocular toxoplasmosis. Clin Diagn Lab Immun. 1999;6:514-18.
6. Cuomo G, D'Abrosca V, Rizzo V, Nardiello S, La Montagna G, Gaeta GB, et al. Severe polymyositis due to Toxoplasma gondii in an adult immunocompetent patient: a case report and review of the literature. Infection. 2013;41:859-62.
7. Neves Ede S, Kropf A, Bueno WF, Bonna IC, Curi AL, Amendoeira MR, et al. Disseminated toxoplasmosis: an atypical presentation in an immunocompetent patient. Trop Doct. 2011;41:59-60.
8. Carme B, Bissuel F, Ajzenberg D, Bouyne R, Aznar C, Demar M, et al. Severe acquired toxoplasmosis in immunocompetent adult patients in French Guiana. J Clin Microbiol. 2002;40:4037-44.
9. Candolfi E, de Blay F, Rey D, Christmann D, Treisser A, Pauli G, et al. A parasitologically proven case of Toxoplasma pneumonia in an immunocompetent pregnant woman. J Infection. 1993;26:79-81.
10. Abhilash KP, Roshine MK, Vandana K, Varghese GM. A probable case of acquired toxoplasmosis presenting as pyrexia of unknown origin in an immunocompetent individual. Int J Infect Dis. 2013;17:e1067-8.
11. Eza DE, Lucas SB. Fulminant toxoplasmosis causing fatal pneumonitis and myocarditis. HIV Med. 2006;7:415-20.
12. Saadatnia G, Golkar M. A review on human toxoplasmosis. Scand J Infect Dis. 2012;44:805-14.
13. Hermanns B, Brunn A, Schwarz ER, Sachweh JS, Seipelt I, Schroder JM, et al. Fulminant toxoplasmosis in a heart transplant recipient. Pathol Res Pract. 2001;197:211-5.
14. Georgiev VS. Management of toxoplasmosis. Drugs. 1994;48:179-88.
15. Montoya JG, Liesenfeld O. Toxoplasmosis. Lancet. 2004;363:1965-76.
16. Howe DK, Sibley LD. Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. J Infect Dis. 1995;172:1561-6.
17. Shwab EK, Zhu XQ, Majumdar D, Pena HF, Gennari SM, Dubey JP, et al. Geographical patterns of Toxoplasma gondii genetic diversity revealed by multilocus PCR-RFLP genotyping. Parasitology. 2014;141:453-61.
18. Su C, Shwab EK, Zhou P, Zhu XQ, Dubey JP. Moving towards an integrated approach to molecular detection and identification of Toxoplasma gondii. Parasitology. 2010;137:1-11.
19. Bossi P, Bricaire F. Severe acute disseminated toxoplasmosis. Lancet. 2004;364:579.
20. Grigg ME, Ganatra J, Boothroyd JC, Margolis TP. Unusual abundance of atypical strains associated with human ocular toxoplasmosis. J Infect Dis. 2001;184:633-9.
21. Sibley LD, Boothroyd JC. Virulent strains of Toxoplasma gondii comprise a single clonal lineage. Nature. 1992;359:82-5.
22. Boothroyd JC, Grigg ME. Population biology of Toxoplasma gondii and its relevance to human infection: do different strains cause different disease? Curr Opin Microbiol. 2002;5:438-42.
23. Kotresha D, Noordin R. Recombinant proteins in the diagnosis of toxoplasmosis. APMIS. 2010;118:529-42.
24. Bastien P. Molecular diagnosis of toxoplasmosis. T Roy Soc Trop Med Hyg. 2002;96:S205-15.
25. Switaj K, Master A, Skrzypczak M, Zaborowski P. Recent trends in molecular diagnostics for Toxoplasma gondii infections. Clin Microbiol Infect. 2005;11:170-6.
26. da Silva PC, Shiraishi CS, Silva AV, Goncalves GF, Sant'Ana Dde M, Araujo EJ. Toxoplasma gondii: a morphometric analysis of the wall and epithelial cells of pigs intestine. Exp Parasitol. 2010;125:380-3.
27. Gordon SM, Gal AA, Hertzler GL, Bryan JA, Perlino C, Kanter KR. Diagnosis of pulmonary toxoplasmosis by bronchoalveolar lavage in cardiac transplant recipients. Diagn Cytopathol. 1993;9:650-4.
28. Dubey JP, Carpenter JL. Histologically confirmed clinical toxoplasmosis in cats: 100 cases (1952-1990). J Am Vet Med Assoc. 1993;203:1556-66.
29. Hutchison WM, Pittilo RM, Ball SJ, Siim JC. Toxoplasma gondii: scanning electron microscope studies on the small intestine of infected and uninfected cats. Acta Pathol Microbiol Scand B. 1979;87:393-5.
30. Sims TA, Hay J, Talbot IC. An electron microscope and immunohistochemical study of the intracellular location of Toxoplasma tissue cysts within the brains of mice with congenital toxoplasmosis. British J Exp Pathol. 1989;70:317-25.
31. Dubey JP, Darrington C, Tiao N, Ferreira LR, Choudhary S, Molla B, et al. Isolation of viable Toxoplasma gondii from tissues and feces of cats from Addis Ababa, Ethiopia. J Parasitol. 2013;99:56-8.
32. Dubey JP, Graham DH, De Young RW, Dahl E, Eberhard ML, Nace EK, et al. Molecular and biologic characteristics of Toxoplasma gondii isolates from wildlife in the United States. J Parasitol. 2004;90:67-71.
33. Sabin AB, Feldman HA. Dyes as microchemical indicators of a new immunity phenomenon affecting a protozoon parasite (Toxoplasma). Science. 1948;108:660-3.
34. Reiter-Owona I, Petersen E, Joynson D, Aspock H, Darde ML, Disko R, et al. The past and present role of the Sabin-Feldman dye test in the serodiagnosis of toxoplasmosis. Bull World Health Organ. 1999;77:929-35.
35. Dubey JP, Desmonts G, McDonald C, Walls KW. Serologic evaluation of cattle inoculated with Toxoplasma gondii: comparison of Sabin-Feldman dye test and other agglutination tests. Am J Vet Res. 1985;46:1085-8.
36. Dubey JP, Ruff MD, Camargo ME, Shen SK, Wilkins GL, Kwok OC, et al. Serologic and parasitologic responses of domestic chickens after oral inoculation with Toxoplasma gondii oocysts. Am J Vet Res. 1993;54:1668-72.
37. Ashburn D, Chatterton JM, Evans R, Joss AW, Ho-Yen DO. Success in the toxoplasma dye test. J Infection. 2001;42:16-9.
38. Udonsom R, Buddhirongawatr R, Sukthana Y. Is Sabin-Feldman dye test using T. gondii tachyzoites from animal inoculation still the best method for detecting Toxoplasma gondii antibodies. Southeast Asian J Trop Med Public Health. 2010;41:1059-64.
39. Desmonts G, Remington JS. Direct agglutination test for diagnosis of Toxoplasma infection: method for increasing sensitivity and specificity. J Clin Microbiol. 1980;11:562-8.
40. Fulton JD, Turk JL. Direct agglutination test for Toxoplasma gondii. Lancet. 1959;2:1068-9.
41. Macri G, Sala M, Linder AM, Pettirossi N, Scarpulla M. Comparison of indirect fluorescent antibody test and modified agglutination test for detecting Toxoplasma gondii immunoglobulin G antibodies in dog and cat. Parasitol Res. 2009;105:35-40.
42. Zhu C, Cui L, Zhang L. Comparison of a commercial ELISA with the modified agglutination test for detection of Toxoplasma gondii antibodies in sera of naturally infected dogs and cats. Iran J Parasitol. 2012;7:89-95.
43. Montoya JG, Berry A, Rosso F, Remington JS. The differential agglutination test as a diagnostic aid in cases of toxoplasmic lymphadenitis. J Clin Microbiol. 2007;45(5):1463-8.
44. Villena I, Durand B, Aubert D, Blaga R, Geers R, Thomas M, et al. New strategy for the survey of Toxoplasma gondii in meat for human consumption. Vet Parasitol. 2012;183:203-8.
45. Mazumder P, Chuang HY, Wentz MW, Wiedbrauk DL. Latex agglutination test for detection of antibodies to Toxoplasma gondii. J Clin Microbiol. 1988;26:2444-6.
46. Oncel T, Vural G, Babur C, Kilic S. Detection of toxoplasmosis gondii seropositivity in sheep in Yalova by Sabin Feldman dye test and latex agglutination test. Turkiye Parazitol Derg. 2005;29:10-2.
47. Holliman RE, Barker KF, Johnson JD. Selective antenatal screening for toxoplasmosis and the latex agglutination test. Epidemiol Infect. 1990;105:409-14.
48. Sato K, Ise Y, Iida T, Suzuki T, Shimada K, Nishioka K. Detection of toxoplasma IgM antibody by passive latex agglutination reaction. J Immunol Methods. 1987;101:183-91.
49. Cambiaso CL, Galanti LM, Leautaud P, Masson PL. Latex agglutination assay of human immunoglobulin M antitoxoplasma antibodies which uses enzymatically treated antigen-coated particles. J Clin Microbiol. 1992;30:882-8.
50. Dubey JP. Toxoplasmosis of Animals and Humans, vol. 313. Boca Raton: CRC Press; 2010.
51. Eissa MH, Abdel Salam AM, Antonious SN, Abdel Gafar AR, Morsy TA. Comparative study of the Sabin-Feldman dye test and the indirect haemagglutination test in serodiagnosis of toxoplasmosis. J Egypt Soc Parasitol. 1990;20:729-35.
52. Balfour AH, Bridges JB, Harford JP. An evaluation of the ToxHA test for the detection of antibodies to Toxoplasma gondii in human serum. J Clin Pathol. 1980;33:644-7.
53. Caruana LB. A study of variation in the indirect hemagglutination antibody test for toxoplasmosis. Am J Med Technol. 1980;46:386-91.
54. Yamamoto YI, Hoshino-Shimizu S, Camargo ME. A novel IgM-indirect hemagglutination test for the serodiagnosis of acute toxoplasmosis. J Clin Lab Anal. 1991;5:127-32.
55. Arthur MJ, Blewett DA. IFAT detection of IgG specific to toxoplasma in thoracic fluids from aborted lambs: evaluation on routine diagnostic submissions. Vet Rec. 1988;122:29-31.
56. Sucilathangam G, Palaniappan N, Sreekumar C, Anna T. IgG-indirect fluorescent antibody technique to detect seroprevalence of Toxoplasma gondii in immunocompetent and immunodeficient patients in southern districts of Tamil Nadu. Indian J Med Microbiol. 2010;28:354-7.
57. Rodrigues IM, Castro AM, Gomes MB, Amaral WN, Avelino MM. Congenital toxoplasmosis: evaluation of serological methods for the detection of anti-Toxoplasma gondii IgM and IgA antibodies. Mem Inst Oswaldo Cruz. 2009;104:434-40.
58. Miller MA, Gardner IA, Packham A, Mazet JK, Hanni KD, Jessup D, et al. Evaluation of an indirect fluorescent antibody test (IFAT) for demonstration of antibodies to Toxoplasma gondii in the sea otter (Enhydra lutris). J Parasitol. 2002;88:594-9.
59. dos Santos TR, Nunes CM, Luvizotto MC, de Moura AB, Lopes WD, da Costa AJ, et al. Detection of Toxoplasma gondii oocysts in environmental samples from public schools. Vet Parasitol. 2010;171:53-7.
60. Shaapan RM, El-Nawawi FA, Tawfik MA. Sensitivity and specificity of various serological tests for the detection of Toxoplasma gondii infection in naturally infected sheep. Vet Parasitol. 2008;153:359-62.
61. Filice G, Meroni V, Carnevale G, Olliaro P, Carosi G. Comparison of ELISA and indirect immunofluorescence in the detection of IgG and IgM antitoxoplasma antibodies. Boll Ist Sieroter Milan. 1983;62:445-50.
62. Tomasi JP, Schlit AF, Stadtsbaeder S. Rapid double-sandwich enzyme-linked immunosorbent assay for detection of human immunoglobulin M anti-Toxoplasma gondii antibodies. J Clin Microbiol. 1986;24:849-50.
63. Obwaller A, Hassl A, Picher O, Aspock H. An enzyme-linked immunosorbent assay with whole trophozoites of Toxoplasma gondii from serum-free tissue culture for detection of specific antibodies. Parasitol Res. 1995;81:361-4.
64. Lau YL, Fong MY, Idris MM, Ching XT. Cloning and expression of Toxoplasma gondii dense granule antigen 2 (GRA2) gene by Pichia pastoris. Southeast Asian J Trop Med Public Health. 2012;43:10-6.
65. Thiruvengadam G, Init I, Fong MY, Lau YL. Optimization of the expression of surface antigen SAG1/2 of Toxoplasma gondii in the yeast Pichia pastoris. Trop Biomed. 2011;28:506-13.
66. Chang PY, Fong MY, Nissapatorn V, Lau YL. Evaluation of Pichia pastoris-expressed recombinant rhoptry protein 2 of Toxoplasma gondii for its application in diagnosis of toxoplasmosis. Am J Trop Med Hyg. 2011;85:485-9.
67. Wang Z, Ge W, Li J, Song M, Sun H, Wei F, et al. Production and evaluation of recombinant granule antigen protein GRA7 for serodiagnosis of Toxoplasma gondii infection in cattle. Foodborne Pathog Dis. 2014;11:734-9.
68. Wang Z, Ge W, Huang SY, Li J, Zhu XQ, Liu Q. Evaluation of recombinant granule antigens GRA1 and GRA7 for serodiagnosis of Toxoplasma gondii infection in dogs. BMC Vet Res. 2014;10:158.
69. Li S, Galvan G, Araujo FG, Suzuki Y, Remington JS, Parmley S. Serodiagnosis of recently acquired Toxoplasma gondii infection using an enzyme-linked immunosorbent assay with a combination of recombinant antigens. Clin Diagn Lab Immun. 2000;7(5):781-7.
70. Aubert D, Maine GT, Villena I, Hunt JC, Howard L, Sheu M, et al. Recombinant antigens to detect Toxoplasma gondii-specific immunoglobulin G and immunoglobulin M in human sera by enzyme immunoassay. J Clin Microbiol. 2000;38:1144-50.
71. Pfrepper KI, Enders G, Gohl M, Krczal D, Hlobil H, Wassenberg D, et al. Seroreactivity to and avidity for recombinant antigens in toxoplasmosis. Clin Diagn Lab Immun. 2005;12:977-82.
72. Hill D, Coss C, Dubey JP, Wroblewski K, Sautter M, Hosten T, et al. Identification of a sporozoite-specific antigen from Toxoplasma gondii. J Parasitol. 2011;97:328-37.
73. Suzuki Y, Ramirez R, Press C, Li S, Parmley S, Thulliez P, et al. Detection of immunoglobulin M antibodies to P35 antigen of Toxoplasma gondii for serodiagnosis of recently acquired infection in pregnant women. J Clin Microbiol. 2000;38:3967-70.
74. Lu B, Wu S, Shi Y, Zhang R, Zou L, Gao S, et al. Toxoplasma gondii: expression pattern and detection of infection using full-length recombinant P35 antigen. Exp Parasitol. 2006;113:83-90.
75. Dautu G, Ueno A, Miranda A, Mwanyumba S, Munyaka B, Carmen G, et al. Toxoplasma gondii: detection of MIC10 antigen in sera of experimentally infected mice. Exp Parasitol. 2008;118:362-71.
76. Pappas MG, Lunde MN, Hajkowski R, McMahon J. Determination of IgM and IgG antibodies to Toxoplasma using the IFA test, ELISA, and Dot-ELISA procedures. Vet Parasitol. 1986;20:31-42.
77. Jafar Pour Azami S, Keshavarz H, Rezaian M, Mohebali M, Shojaee S. Rapid detection of Toxoplasma gondii antigen in experimentally infected mice by Dot- ELISA. Iran J Parasitol. 2011;6:28-33.
78. Youssef MM, el-Ganayni GA, el-Shazly AM. The efficacy of IHAT, IFAT and Dot-ELISA in serodiagnosis of toxoplasmosis in complicated pregnancies. J Egypt Soc Parasitol. 1992;22:343-7.
79. Desmonts G, Naot Y, Remington JS. Immunoglobulin M-immunosorbent agglutination assay for diagnosis of infectious diseases: diagnosis of acute congenital and acquired Toxoplasma infections. J Clin Microbiol. 1981;14:486-91.
80. Remington JS, Eimstad WM, Araujo FG. Detection of immunoglobulin M antibodies with antigen-tagged latex particles in an immunosorbent assay. J Clin Microbiol. 1983;17:939-41.
81. Thobhani S, Attree S, Boyd R, Kumarswami N, Noble J, Szymanski M, et al. Bioconjugation and characterisation of gold colloid-labelled proteins. J Immunol Methods. 2010;356:60-9.
82. Goni P, Martin B, Villacampa M, Garcia A, Seral C, Castillo FJ, et al. Evaluation of an immunochromatographic dip strip test for simultaneous detection of Cryptosporidium spp, Giardia duodenalis, and Entamoeba histolytica antigens in human faecal samples. Eur J Clin Microbiol. 2012;31:2077-82.
83. Wang YH, Li XR, Wang GX, Yin H, Cai XP, Fu BQ, et al. Development of an immunochromatographic strip for the rapid detection of Toxoplasma gondii circulating antigens. Parasitol Int. 2011;60:105-7.
84. Huang X, Xuan X, Hirata H, Yokoyama N, Xu L, Suzuki N, et al. Rapid immunochromatographic test using recombinant SAG2 for detection of antibodies against Toxoplasma gondii in cats. J Clin Microbiol. 2004;42:351-3.
85. Terkawi MA, Kameyama K, Rasul NH, Xuan X, Nishikawa Y. Development of an immunochromatographic assay based on dense granule protein 7 for serological detection of Toxoplasma gondii infection. Clin Vacc Immunol. 2013;20:596-601.
86. Suleiman AA, Guilbault GG. Recent developments in piezoelectric immunosensors: a review. Analyst. 1994;119:2279-82.
87. Cabral-Miranda G, de Jesus JR, Oliveira PR, Britto GS, Pontes-de-Carvalho LC, Dutra RF, et al. Detection of parasite antigens in Leishmania infantum-infected spleen tissue by monoclonal antibody-, piezoelectric-based immunosensors. J Parasitol. 2014;100:73-8.
88. Wang S, Yin T, Zeng S, Che H, Yang F, Chen X, et al. A piezoelectric immunosensor using hybrid self-assembled monolayers for detection of Schistosoma japonicum. PLoS One. 2012;7:e30779.
89. Xu S, Mutharasan R. Rapid and sensitive detection of Giardia lamblia using a piezoelectric cantilever biosensor in finished and source waters. Environ Sci Technol. 2010;44:1736-41.
90. Wang H, Lei C, Li J, Wu Z, Shen G, Yu R. A piezoelectric immunoagglutination assay for Toxoplasma gondii antibodies using gold nanoparticles. Biosens Bioelectron. 2004;19:701-9.
91. Stroehle A, Schmid K, Heinzer I, Naguleswaran A, Hemphill A. Performance of a Western immunoblot assay to detect specific anti-Toxoplasma gondii IgG antibodies in human saliva. J Parasitol. 2005;91:561-3.
92. Villard O, Filisetti D, Roch-Deries F, Garweg J, Flament J, Candolfi E. Comparison of enzyme-linked immunosorbent assay, immunoblotting, and PCR for diagnosis of toxoplasmic chorioretinitis. J Clin Microbiol. 2003;41:3537-41.
93. Robert-Gangneux F, Commerce V, Tourte-Schaefer C, Dupouy-Camet J. Performance of a Western blot assay to compare mother and newborn anti-Toxoplasma antibodies for the early neonatal diagnosis of congenital toxoplasmosis. Eur J Clin Microbiol. 1999;18:648-54.
94. Bobic B, Sibalic D, Djurkovic-Djakovic O. High levels of IgM antibodies specific for Toxoplasma gondii in pregnancy 12 years after primary Toxoplasma infection. Case report. Gynecol Obstet Investig. 1991;31(3):182-4.
95. Gorgievski-Hrisoho M, Germann D, Matter L. Diagnostic implications of kinetics of immunoglobulin M and A antibody responses to Toxoplasma gondii. J Clin Microbiol. 1996;34:1506-11.
96. Meek B, Diepersloot RJ, van Gool T, Speijer D, Peek R. IgM recognition of recombinant Toxoplasma gondii antigens by sera of acutely or latently infected humans. Diagn Microbiol Infect Dis. 2003;45:45-52.
97. Gutierrez J, Rodriguez M, Piedrola G, del Carmen MM. Detection of IgA and low-avidity IgG antibodies for the diagnosis of recent active toxoplasmosis. Clin Microbiol Infect. 1997;3:658-62.
98. Hedman K, Lappalainen M, Seppaia I, Makela O. Recent primary Toxoplasma infection indicated by a low avidity of specific IgG. J Infect Dis. 1989;159:736-40.
99. de Ory F, Casas I, Domingo CJ, Echevarria J. Application of fluoroimmunoassay to the identification of low avidity specific IgG against pathogenic human viruses and Toxoplasma gondii. Clin Diagn Virol. 1995;3:323-32.
100. Ashburn D, Joss AW, Pennington TH, Ho-Yen DO. Do IgA, IgE, and IgG avidity tests have any value in the diagnosis of Toxoplasma infection in pregnancy? J Clin Pathol. 1998;51:312-5.
101. Ali-Heydari S, Keshavarz H, Shojaee S, Mohebali M. Diagnosis of antigenic markers of acute toxoplasmosis by IgG avidity immunoblotting. Parasite. 2013;20:18.
102. Deshpande PS, Kotresha D, Noordin R, Yunus MH, Saadatnia G, Golkar M, et al. IgG avidity Western blot using Toxoplasma gondii rGRA-7 cloned from nucleotides 39-711 for serodiagnosis of acute toxoplasmosis. Rev Inst Med Trop Sao Paulo. 2013;55:79-83.
103. Rossi CL. A simple, rapid enzyme-linked immunosorbent assay for evaluating immunoglobin G antibody avidity in toxoplasmosis. Diagn Microbiol Infect Dis. 1998;30:25-30.
104. Cozon GJ, Ferrandiz J, Nebhi H, Wallon M, Peyron F. Estimation of the avidity of immunoglobulin G for routine diagnosis of chronic Toxoplasma gondii infection in pregnant women. Eur J Clin Microbiol. 1998;17:32-6.
105. Buffolano W, Lappalainen M, Hedman L, Ciccimarra F, Del Pezzo M, Rescaldani R, et al. Delayed maturation of IgG avidity in congenital toxoplasmosis. Eur J Clin Microbiol. 2004;23:825-30.
106. Meroni V, Genco F, Tinelli C, Lanzarini P, Bollani L, Stronati M, et al. Spiramycin treatment of Toxoplasma gondii infection in pregnant women impairs the production and the avidity maturation of T. gondii-specific immunoglobulin G antibodies. Clin Vacc Immunol. 2009;16:1517-20.
107. Lefevre-Pettazzoni M, Bissery A, Wallon M, Cozon G, Peyron F, Rabilloud M. Impact of spiramycin treatment and gestational age on maturation of Toxoplasma gondii immunoglobulin G avidity in pregnant women. Clin Vacc Immunol. 2007;14:239-43.
108. Lefevre-Pettazzoni M, Le Cam S, Wallon M, Peyron F. Delayed maturation of immunoglobulin G avidity: implication for the diagnosis of toxoplasmosis in pregnant women. Eur J Clin Microbiol. 2006;25(11):687-93.
109. Bonyadi MR, Bastani P. Modification and evaluation of avidity IgG testing for differentiating of Toxoplasma gondii infection in early stage of pregnancy. Cell J. 2013;15:238-43.
110. Virkola K, Lappalainen M, Valanne L, Koskiniemi M. Radiological signs in newborns exposed to primary Toxoplasma infection in utero. Pediatr Radiol. 1997;27:133-8.
111. Blaakaer J. Ultrasonic diagnosis of fetal ascites and toxoplasmosis. Acta Obst Gyn Scan. 1986;65:653-4.
112. Vutova K, Peicheva Z, Popova A, Markova V, Mincheva N, Todorov T. Congenital toxoplasmosis: eye manifestations in infants and children. Ann Trop Paediatr. 2002;22:213-8.
113. Porter SB, Sande MA. Toxoplasmosis of the central nervous system in the acquired immunodeficiency syndrome. New Engl J Med. 1992;327:1643-8.
114. Alenghat JP, Morris JH, Kido DK, Rumbaugh CL. Computed tomography in opportunistic cerebral toxoplasmosis: report of two cases. Comput Tomogr. 1981;5:231-7.
115. Collins AT, Cromwell LD. Computed tomography in the evaluation of congenital cerebral toxoplasmosis. J Comput Assist Tomo. 1980;4(3):326-9.
116. Foulon W, Naessens A, Mahler T, de Waele M, de Catte L, de Meuter F. Prenatal diagnosis of congenital toxoplasmosis. Obstet Gynecol. 1990;76:769-72.
117. Abboud P, Harika G, Saniez D, Gabriel R, Bednarczyk L, Chemla C, et al. Ultrasonic signs of fetal toxoplasmosis. Review of the literature. J Gynecol Obstet Biol Reprod. 1995;24:733-8.
118. Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, et al. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988;239:487-91.
119. Burg JL, Grover CM, Pouletty P, Boothroyd JC. Direct and sensitive detection of a pathogenic protozoan, Toxoplasma gondii, by polymerase chain reaction. J Clin Microbiol. 1989;27:1787-92.
120. Khalifa K-S, Roth A, Roth B, Arasteh KN, Janitschke K. Value of PCR for evaluating occurrence of parasitemia in immunocompromised patients with cerebral and extracerebral toxoplasmosis. J Clin Microbiol. 1994;32:2813-9.
121. Hohlfeld P, Daffos F, Costa JM, Thulliez P, Forestier F, Vidaud M. Prenatal diagnosis of congenital toxoplasmosis with a polymerase-chain-reaction test on amniotic fluid. New Engl J Med. 1994;331:695-9.
122. Parmley SF, Goebel FD, Remington JS. Detection of Toxoplasma gondii in cerebrospinal fluid from AIDS patients by polymerase chain reaction. J Clin Microbiol. 1992;30:3000-2.
123. Ho-Yen DO, Joss AW, Balfour AH, Smyth ET, Baird D, Chatterton JM. Use of the polymerase chain reaction to detect Toxoplasma gondii in human blood samples. J Clin Pathol. 1992;45:910-3.
124. Lamoril J, Molina JM, de Gouvello A, Garin YJ, Deybach JC, Modai J, et al. Detection by PCR of Toxoplasma gondii in blood in the diagnosis of cerebral toxoplasmosis in patients with AIDS. J Clin Pathol. 1996;49:89-92.
125. Homan WL, Vercammen M, De Braekeleer J, Verschueren H. 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. 2000;30:69-75.
126. Reischl U, Bretagne S, Kruger D, Ernault P, Costa JM. Comparison of two DNA targets for the diagnosis of Toxoplasmosis by real-time PCR using fluorescence resonance energy transfer hybridization probes. BMC Infect Dis. 2003;3:7.
127. Hurtado A, Aduriz G, Moreno B, Barandika J, Garcia-Perez AL. Single tube nested PCR for the detection of Toxoplasma gondii in fetal tissues from naturally aborted ewes. Vet Parasitol. 2001;102:17-27.
128. Jauregui LH, Higgins J, Zarlenga D, Dubey JP, Lunney JK. Development of a real-time PCR assay for detection of Toxoplasma gondii in pig and mouse tissues. J Clin Microbiol. 2001;39:2065-71.
129. Calderaro A, Piccolo G, Gorrini C, Peruzzi S, Zerbini L, Bommezzadri S, et al. Comparison between two real-time PCR assays and a nested-PCR for the detection of Toxoplasma gondii. Acta Biomed. 2006;77:75-80.
130. Fallahi S, Kazemi B, SJ S t, Bandehpour M, Lasjerdi Z, Taghipour N, et al. Comparison of the RE and B1 gene for detection of Toxoplasma gondii infection in children with cancer. Parasitol Int. 2014;63:37-41.
131. Jones CD, Okhravi N, Adamson P, Tasker S, Lightman S. Comparison of PCR detection methods for B1, P30, and 18S rDNA genes of T. gondii in aqueous humor. Invest Ophth Vis Sci. 2000;41:634-44.
132. Emrich T, Karl G. Nonradioactive detection of telomerase activity using a PCR-ELISA-based telomeric repeat amplification protocol. Methods Mol Biol. 2002;191:147-58.
133. Martinez E, Carmelo E, Alonso R, Ortega A, Pinero J, del Castillo A, et al. Development of a rapid polymerase chain reaction-ELISA assay using polystyrene beads for the detection of Toxoplasma gondii DNA. Lett Appl Microbiol. 2003;36:30-4.
134. Kompalic-Cristo A, Frotta C, Suarez-Mutis M, Fernandes O, Britto C. Evaluation of a real-time PCR assay based on the repetitive B1 gene for the detection of Toxoplasma gondii in human peripheral blood. Parasitol Res. 2007;101:619-25.
135. Nogui FL, Mattas S, Turcato Junior G, Lewi DS. Neurotoxoplasmosis diagnosis for HIV-1 patients by real-time PCR of cerebrospinal fluid. Braz J Infect Dis. 2009;13:18-23.
136. Dworkin LL, Gibler TM, Van Gelder RN. Real-time quantitative polymerase chain reaction diagnosis of infectious posterior uveitis. Arch Ophthalmol. 2002;120:1534-9.
137. Kasper DC, Sadeghi K, Prusa AR, Reischer GH, Kratochwill K, Forster-Waldl E, et al. Quantitative real-time polymerase chain reaction for the accurate detection of Toxoplasma gondii in amniotic fluid. Diagn Micr Infect Dis. 2009;63:10-5.
138. Menotti J, Vilela G, Romand S, Garin YJ, Ades L, Gluckman E, et al. Comparison of PCR-enzyme-linked immunosorbent assay and real-time PCR assay for diagnosis of an unusual case of cerebral toxoplasmosis in a stem cell transplant recipient. J Clin Microbiol. 2003;41:5313-6.
139. Teixeira LE, Kanunfre KA, Shimokawa PT, Targa LS, Rodrigues JC, Domingues W, et al. The performance of four molecular methods for the laboratory diagnosis of congenital toxoplasmosis in amniotic fluid samples. Rev Soc Bras Med Trol. 2013;46:584-8.
140. Bretagne S, Costa JM. Towards a nucleic acid-based diagnosis in clinical parasitology and mycology. Clin Chim Acta. 2006;363:221-8.
141. Opsteegh M, Langelaar M, Sprong H, den Hartog L, De Craeye S, Bokken G, et al. Direct detection and genotyping of Toxoplasma gondii in meat samples using magnetic capture and PCR. Int J Food Microbiol. 2010;139:193-201.
142. Jurankova J, Basso W, Neumayerova H, Balaz V, Janova E, Sidler X, et al. Brain is the predilection site of Toxoplasma gondii in experimentally inoculated pigs as revealed by magnetic capture and real-time PCR. Food Microbiol. 2014;38:167-70.
143. Jurankova J, Opsteegh M, Neumayerova H, Kovarcik K, Frencova A, Balaz V, et al. Quantification of Toxoplasma gondii in tissue samples of experimentally infected goats by magnetic capture and real-time PCR. Vet Parasitol. 2013;193:95-9.
144. Notomi T, Okayama H, Masubuchi H, Yonekawa T, Watanabe K, Amino N, et al. Loop-mediated isothermal amplification of DNA. Nucleic Acids Res. 2000;28:e63.
145. Wang Y, Wang G, Zhang D, Yin H, Wang M. Detection of acute toxoplasmosis in pigs using loop-mediated isothermal amplification and quantitative PCR. Korean J Parasitol. 2013;51:573-7.
146. Lin Z, Zhang Y, Zhang H, Zhou Y, Cao J, Zhou J. Comparison of loop-mediated isothermal amplification (LAMP) and real-time PCR method targeting a 529-bp repeat element for diagnosis of toxoplasmosis. Vet Parasitol. 2012;185:296-300.
147. Lau YL, Meganathan P, Sonaimuthu P, Thiruvengadam G, Nissapatorn V, Chen Y. Specific, sensitive, and rapid diagnosis of active toxoplasmosis by a loop-mediated isothermal amplification method using blood samples from patients. J Clin Microbiol. 2010;48:3698-702.
148. Cao L, Cheng R, Yao L, Yuan S, Yao X. Establishment and application of a loop-mediated isothermal amplification method for simple, specific, sensitive and rapid detection of Toxoplasma gondii. J Vet Med Sci. 2014;76:9-14.
149. Zhang H, Thekisoe OM, Aboge GO, Kyan H, Yamagishi J, Inoue N, et al. Toxoplasma gondii: sensitive and rapid detection of infection by loop-mediated isothermal amplification (LAMP) method. Exp Parasitol. 2009;122:47-50.
150. Hu X, Pan CW, Li YF, Wang H, Tan F. Urine sample used for detection of Toxoplasma gondii infection by loop-mediated isothermal amplification (LAMP). Folia Parasit. 2012;59:21-6.
151. Sotiriadou I, Karanis P. Evaluation of loop-mediated isothermal amplification for detection of Toxoplasma gondii in water samples and comparative findings by polymerase chain reaction and immunofluorescence test (IFT). Diagn Micr Infec Dis. 2008;62:357-65.
152. Qu D, Zhou H, Han J, Tao S, Zheng B, Chi N, et al. Development of reverse transcription loop-mediated isothermal amplification (RT-LAMP) as a diagnostic tool of Toxoplasma gondii in pork. Vet Parasitol. 2013;192:98-103.
153. Mikita K, Maeda T, Ono T, Miyahira Y, Asai T, Kawana A. The utility of cerebrospinal fluid for the molecular diagnosis of toxoplasmic encephalitis. Diagn Micr Infec Dis. 2013;75:155-9.
154. Krasteva D, Toubiana M, Hartati S, Kusumawati A, Dubremetz JF, Widada JS. Development of loop-mediated isothermal amplification (LAMP) as a diagnostic tool of toxoplasmosis. Vet Parasitol. 2009;162:327-31.
155. Gallas-Lindemann C, Sotiriadou I, Mahmoodi MR, Karanis P. Detection of Toxoplasma gondii oocysts in different water resources by loop mediated isothermal amplification (LAMP). Acta Trop. 2013;125:231-6.
156. Ajzenberg D, Collinet F, Mercier A, Vignoles P, Darde ML. Genotyping of Toxoplasma gondii isolates with 15 microsatellite markers in a single multiplex PCR assay. J Clin Microbiol. 2010;48:4641-5.
157. Li M, Mo XW, Wang L, Chen H, Luo QL, Wen HQ, et al. Phylogeny and virulence divergency analyses of Toxoplasma gondii isolates from China. Parasit Vectors. 2014;7:133.
158. Ajzenberg D, Banuls AL, Tibayrenc M, Darde ML. Microsatellite analysis of Toxoplasma gondii shows considerable polymorphism structured into two main clonal groups. Int J Parasitol. 2002;32:27-38.
159. Blackston CR, Dubey JP, Dotson E, Su C, Thulliez P, Sibley D, et al. High-resolution typing of Toxoplasma gondii using microsatellite loci. J Parasitol. 2001;87(6):1472-5.
160. Quan JH, Kim TY, Choi IU, Lee YH. Genotyping of a Korean isolate of Toxoplasma gondii by multilocus PCR-RFLP and microsatellite analysis. Korean J Parasitol. 2008;46:105-8.
161. Dumetre A, Ajzenberg D, Rozette L, Mercier A, Darde ML. Toxoplasma gondii infection in sheep from Haute-Vienne, France: seroprevalence and isolate genotyping by microsatellite analysis. Vet Parasitol. 2006;142:376-9.
162. Khan A, Jordan C, Muccioli C, Vallochi AL, Rizzo LV, Belfort Jr R, et al. Genetic divergence of Toxoplasma gondii strains associated with ocular toxoplasmosis, Brazil. Emerg Infect Dis. 2006;12:942-9.
163. Khan A, Fux B, Su C, Dubey JP, Darde ML, Ajioka JW, et al. Recent transcontinental sweep of Toxoplasma gondii driven by a single monomorphic chromosome. Proc Natl Acad Sci U S A. 2007;104:14872-7.
164. Ajzenberg D, Cogne N, Paris L, Bessieres MH, Thulliez P, Filisetti D, et al. Genotype of 86 Toxoplasma gondii isolates associated with human congenital toxoplasmosis, and correlation with clinical findings. J Infect Dis. 2002;186:684-9.
165. Lehmann T, Marcet PL, Graham DH, Dahl ER, Dubey JP. Globalization and the population structure of Toxoplasma gondii. Proc Natl Acad Sci U S A. 2006;103:11423-8.
166. Khan A, Taylor S, Su C, Mackey AJ, Boyle J, Cole R, et al. Composite genome map and recombination parameters derived from three archetypal lineages of Toxoplasma gondii. Nucleic Acids Res. 2005;33:2980-92.
167. Khan A, Su C, German M, Storch GA, Clifford DB, Sibley LD. Genotyping of Toxoplasma gondii strains from immunocompromised patients reveals high prevalence of type I strains. J Clin Microbiol. 2005;43:5881-7.
168. 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. 2006;36:841-8.
169. Ferreira IM, Vidal JE, Costa-Silva TA, Meira CS, Hiramoto RM, de Oliveira AC P, et al. Toxoplasma gondii: genotyping of strains from Brazilian AIDS patients with cerebral toxoplasmosis by multilocus PCR-RFLP markers. Exp Parasitol. 2008;118:221-7.
170. Dubey JP, Sundar N, Gennari SM, Minervino AH, Farias NA, Ruas JL, 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. 2007;143:182-8.
171. Zhou Y, Zhang H, Cao J, Gong H, Zhou J. Isolation and genotyping of Toxoplasma gondii from domestic rabbits in China to reveal the prevalence of type III strains. Vet Parasitol. 2013;193:270-6.
172. Su C, Khan A, Zhou P, Majumdar D, Ajzenberg D, Darde ML, et al. Globally diverse Toxoplasma gondii isolates comprise six major clades originating from a small number of distinct ancestral lineages. Proc Natl Acad Sci U S A. 2012;109:5844-9.
173. Huang SY, Cong W, Zhou P, Zhou DH, Wu SM, Xu MJ, et al. First report of genotyping of Toxoplasma gondii isolates from wild birds in China. J Parasitol. 2012;98:681-2.
174. Zhou P, Sun XT, Yin CC, Yang JF, Yuan ZG, Yan HK, et al. Genetic characterization of Toxoplasma gondii isolates from pigs in southwestern China. J Parasitol. 2011;97:1193-5.
175. Zhou P, Zhang H, Lin RQ, Zhang DL, Song HQ, Su C, et al. Genetic characterization of Toxoplasma gondii isolates from China. Parasitol Int. 2009;58:193-5.
176. Dubey JP, Zhu XQ, Sundar N, Zhang H, Kwok OC, Su C. Genetic and biologic characterization of Toxoplasma gondii isolates of cats from China. Vet Parasitol. 2007;145:352-6.
177. Guo ZG, Gross U, Johnson AM. Toxoplasma gondii virulence markers identified by random amplified polymorphic DNA polymerase chain reaction. Parasitol Res. 1997;83:458-63.
178. Guo ZG, Johnson AM. Genetic characterization of Toxoplasma gondii strains by random amplified polymorphic DNA polymerase chain reaction. Parasitology. 1995;111:127-32.
179. Ferreira Ade M, Vitor RW, Carneiro AC, Brandao GP, Melo MN. Genetic variability of Brazilian Toxoplasma gondii strains detected by random amplified polymorphic DNA-polymerase chain reaction (RAPD-PCR) and simple sequence repeat anchored-PCR (SSR-PCR). Infect Genet Evol. 2004;4:131-42.
180. Arif IA, Bakir MA, Khan HA, Al Farhan AH, Al Homaidan AA, Bahkali AH, et al. A brief review of molecular techniques to assess plant diversity. Inter J Mol Sci. 2010;11(5):2079-96.
181. Jex AR, Smith HV, Monis PT, Campbell BE, Gasser RB. Cryptosporidium-biotechnological advances in the detection, diagnosis and analysis of genetic variation. Biotechnol Adv. 2008;26:304-17.
182. Costa JM, Cabaret O, Moukoury S, Bretagne S. Genotyping of the protozoan pathogen Toxoplasma gondii using high-resolution melting analysis of the repeated B1 gene. J Microbiol Methods. 2011;86:357-63.
183. Costa JM, Alanio A, Moukoury S, Clairet V, Debruyne M, Poveda JD, et al. Direct genotyping of Toxoplasma gondii from amniotic fluids based on B1 gene polymorphism using minisequencing analysis. BMC Infect Dis. 2013;13:552.
184. Kong JT, Grigg ME, Uyetake L, Parmley S, Boothroyd JC. Serotyping of Toxoplasma gondii infections in humans using synthetic peptides. J Infect Dis. 2003;187:1484-95.
185. Xiao J, Buka SL, Cannon TD, Suzuki Y, Viscidi RP, Torrey EF, et al. Serological pattern consistent with infection with type I Toxoplasma gondii in mothers and risk of psychosis among adult offspring. Microbes Infect. 2009;11:1011-8.
186. Sousa S, Ajzenberg D, Marle M, Aubert D, Villena I, da Costa JC, et al. Selection of polymorphic peptides from GRA6 and GRA7 sequences of Toxoplasma gondii strains to be used in serotyping. Clin Vacc Immunol. 2009;16:1158-69.
187. Sousa S, Canada N, Correia da Costa JM, Darde ML. Serotyping of naturally Toxoplasma gondii infected meat-producing animals. Vet Parasitol. 2010;169:24-8.
188. Sousa S, Ajzenberg D, Vilanova M, Costa J, Darde ML. Use of GRA6-derived synthetic polymorphic peptides in an immunoenzymatic assay to serotype Toxoplasma gondii in human serum samples collected from three continents. Clin Vacc Immunol. 2008;15:1380-6.
189. Peyron F, Lobry JR, Musset K, Ferrandiz J, Gomez-Marin JE, Petersen E, 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). Microbes Infect. 2006;8:2333-40.
190. Maksimov P, Zerweck J, Dubey JP, Pantchev N, Frey CF, Maksimov A, et al. Serotyping of Toxoplasma gondii in cats (Felis domesticus) reveals predominance of type II infections in Germany. PLoS One. 2013;8:e80213.
191. Maksimov P, Zerweck J, Maksimov A, Hotop A, Gross U, Spekker K, et al. Analysis of clonal type-specific antibody reactions in Toxoplasma gondii seropositive humans from Germany by peptide-microarray. PLoS One. 2012;7:e34212.
192. Turunen H, Vuorio KA, Leinikki PO. Determination of IgG, IgM and IgA antibody responses in human toxoplasmosis by enzyme-linked immunosorbent assay (ELISA). Scand J Infect Dis. 1983;15:307-11.
193. Li S, Maine G, Suzuki Y, Araujo FG, Galvan G, Remington JS, et al. Serodiagnosis of recently acquired Toxoplasma gondii infection with a recombinant antigen. J Clin Microbiol. 2000;38:179-84.
194. Chandramukhi A. Diagnosis of neurotoxoplasmosis by antibody detection in cerebrospinal (CSF) fluid using latex agglutination test and ELISA. J Commun Dis. 2004;36:153-8.
195. Trees AJ, Crozier SJ, Buxton D, Blewett DA. Serodiagnosis of ovine toxoplasmosis: an assessment of the latex agglutination test and the value of IgM specific titres after experimental oocyst-induced infections. Res Vet Sci. 1989;46:67-72.
196. Rilling V, Dietz K, Krczal D, Knotek F, Enders G. Evaluation of a commercial IgG/IgM Western blot assay for early postnatal diagnosis of congenital toxoplasmosis. Eur J Clin Microbiol. 2003;22:174-80.
197. Cresti S, Ciacci C, Donati E, Giordano I, Tordini G, Barberi A. Evaluation of PCR methods for 5S-rDNA and p30 genes to detect Toxoplasma gondii in blood and other clinical samples. New Microbiol. 2001;24:171-4.
198. Yu H, Huang B, Zhuo X, Chen X, Du A. Evaluation of a real-time PCR assay based on the single-copy SAG1 gene for the detection of Toxoplasma gondii. Vet Parasitol. 2013;197:670-3.
199. Wahab T, Edvinsson B, Palm D, Lindh J. Comparison of the AF146527 and B1 repeated elements, two real-time PCR targets used for detection of Toxoplasma gondii. J Clin Microbiol. 2010;48:591-2.
200. Kong QM, Lu SH, Tong QB, Lou D, Chen R, Zheng B, et al. Loop-mediated isothermal amplification (LAMP): early detection of Toxoplasma gondii infection in mice. Parasite Vector. 2012;5:2.