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Comparative analysis of the VIDAS Toxo IgG IV assay in the detection of antibodies to Toxoplasma gondii
Diagnostic Microbiology and Infectious Disease 53 (2005) 79 – 81 www.elsevier.com/locate/diagmicrobio
Comparative analysis of the VIDAS Toxo IgG IV assay in the detection of antibodies to Toxoplasma gondii B Nathalie Roux-Buissona, He´le`ne Fricker-Hidalgoa,T, Agne`s Foussadierb, Dominique Rollandb, Anne-Sophie Suchel-Jambonb, Marie-Pierre Brenier-Pincharta, Herve´ Pellouxa a
Service de Parasitologie-Mycologie, Centre Hospitalier Universitaire, BP217, 38043 Grenoble, France b Recherche et De´veloppement, bioMe´rieux, Chemin de l’Orme, 69280 Marcy l’Etoile, France Received 4 January 2005; accepted 21 April 2005
Abstract A new serological test, Vidas Toxo IgG IV, has been developed with antigens obtained from tachyzoites cultured on cells. Vidas Toxo IgG IV replaces Vidas Toxo IgG II by offering a more standardized antigenic production and a lower number of indeterminate results while retaining equivalent sensitivity and specificity. D 2005 Elsevier Inc. All rights reserved. Keywords: Toxoplasma gondii; Vidas Toxo IgG IV; Toxoplasmosis; Antigens
1. Introduction
2. Materials and methods
A new version of the serological test Vidas Toxo IgG has been recently developed with antigens obtained from tachyzoites cultured on cells and not on mice. To avoid the use of laboratory animals, in vitro maintenance on cell culture is used to obtain tachyzoites for antigen preparation. Affinity-purified P30-enriched fraction of Toxoplasma gondii antigens was prepared for a new immunoenzymatic test developed by bioMe´rieux, Vidas Toxo IgG IV, which would replace Vidas Toxo IgG II. The aim of our study is to evaluate Vidas Toxo IgG IV’s sensitivity, specificity, and ability to swiftly detect IgG antibodies and to compare its performance with 3 other techniques: Vidas Toxo IgG II (bioMe´rieux), Toxo IgG Axsym (Abbott), and indirect immunofluorescence assay (IFA).
The study related to 656 sera, obtained from the Parasitology–Mycology Laboratory at Grenoble hospital. Of the 656 sera, 596 sera were obtained from the routine activity of the laboratory and consisted of sera from pregnant women, newborns, immunocompetent and immunocompromised patients, and 60 sequential sera were obtained from 20 pregnant women showing seroconversion (3 sera per patient). Vidas Toxo IgG IV, marketed by bioMe´rieux (69280 Marcy l’Etoile/France), is an automated assay for the Vidas system. The antigens were of membrane and cytoplasmic origin (RH Sabin strain). T. gondii tachyzoites is obtained from in vitro cell culture. After lysis, affinity chromatography is performed to obtain P30-enriched fraction as previously described (Santoro et al., 1985). The other techniques were Vidas Toxo IgG IV (Pelloux et al., 1993), Toxo IgG Axsym (Abbott Laboratories, Diagnostics Division, Abbott Park, IL) (Goubet et al., 1999), and IFA (Ambroise-Thomas et al., 1996). When the IgG detection result of a technique was discrepant with that of the other tests, dye test was performed by Dr P. Thulliez (Institut de Pue´riculture, Paris, France) (Reiter-Owona et al., 1999). For each serum, the biologic interpretation (presence or absence of IgG) considered results obtained with Vidas Toxo IgG II, Toxo IgG Axsym, and IFA. The interpretation was easy when all
B
The results included in this article were previously presented in a French national congress: poster: Fricker-Hidalgo, H., Roux-Buisson, N., Foussadier, A., Rolland, D., Suchel-Jambon, A.S., Brenier-Pinchart, M.P., Pelloux, H. Un nouveau test ELISA, Vidas Toxo IgG IV: e´valuation par rapport a` trois autres techniques se´rologiques, Congre`s de la Socie´te´ Franc¸aise de Parasitologie, Maisons-Alfort, France, 16 –18 de´cembre 2003. T Corresponding author. Tel.: +33-4-76765490; fax: +33-4-76765660. E-mail address: [email protected] (H. Fricker-Hidalgo). 0732-8893/$ – see front matter D 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.diagmicrobio.2005.04.005
80
N. Roux-Buisson et al. / Diagnostic Microbiology and Infectious Disease 53 (2005) 79 – 81
Table 1 Resolved sensitivities, specificities, and positive and negative predictive values of the immunoassay systems evaluated Test systems
a
Sensitivity (%)
Vidas Toxo IgG IV 98.67 Vidas Toxo IgG II 98.13 Toxo IgG Axsym 100.00 IFA 93.04
Specificity (%) 99.44 99.72 98.89 99.45
b
Positive Negative predictive predictive valuec (%) valued (%) 99.11 99.53 98.25 99.07
99.16 98.91 100.00 95.79
a
Sensitivity = true-positive/(true-positive + false-negative). Specificity = true-negative/(true-negative + false-positive). c Positive predictive value = true-positive/(true-positive + falsepositive). d Negative predictive value = true-negative/(true-negative + falsenegative). b
3 techniques showed similar results. Any serum showing a discrepancy or indeterminate result with a technique was retested with the considered technique and the dye test (Reiter-Owona et al., 1999). The results of the dye test allowed to classify the sera as positive or negative IgG. The sensitivities, the specificities, and the positive and negative predictive values of each technique were calculated in reference to the classification of sera (Table 1) and were compared using the McNemar test (Schwartz, 1986). 3. Results Three hundred sixty-six sera out of 596 routine laboratory sera were considered as negative for anti-T. gondii IgG and 230 as positive. Dye test was performed on 57 sera. The overall consistency between the various methods was 97.68% (548/561) and was between 96.74% and 99.12%, when the assays were compared in pairs. Vidas Toxo IgG IV and II and Toxo IgG Axsym showed statistically equivalent sensitivity and specificity (Table 1). IFA showed an equivalent specificity at 99.45% but a statistically significant lower sensitivity (93.04%) than Toxo IgG Axsym (100%), Vidas Toxo IgG IV (98.67%), and Vidas Toxo IgG II (98.13%). Sixteen false-negative results were observed with IFA (Table 2). Vidas Toxo IgG IV showed 13/596 (2.18%) indeterminate results, similar to Toxo IgG Axsym and less than Vidas Toxo IgG II (19/596, 3.18%) (Table 2). The ability to detect IgG antibodies earlier than other assays was evaluated on 60 sera obtained from 20 seroconverted women (3 sera per patient). When we analyzed the results of the second serum of the 20 patients, the number of positive results was 8 with Vidas Toxo IgG IV, 9 with Vidas Toxo IgG II, 16 with Toxo IgG Axsym, and 17 with IFA. The number of positive results of the third serum was 17 with Vidas Toxo IgG IV, 17 with Vidas Toxo IgG II, 20 with Toxo IgG Axsym, and 20 with IFA. Thus, IgG appeared often earlier with IFA and Toxo IgG Axsym than with Vidas Toxo IgG II and IV.
4. Discussion The main interest of Vidas Toxo IgG IV lies in the preparation of the antigen, produced on cell culture and not on mice as with Vidas Toxo IgG II. It makes preparation easier and more reproducible, and the sensitivity and specificity of Vidas Toxo IgG IV were equivalent to Vidas Toxo IgG II. In a previous study (Goubet et al., 1999) evaluating Vidas Toxo IgG II, Toxo IgG Axsym, and IFA, the consistencies were equivalent to those found in this study. Similar sensitivity and specificity values for Vidas Toxo IgG II have been reported by other authors (De Champs et al., 1997; Hofgartner et al., 1997; Pelloux et al., 1993). Cimon et al. (1998) found a specificity of 95.6% for Toxo IgG Axsym in low antibody titers in pregnant women. The lower sensitivity of IFA compared with Toxo IgG Axsym and Vidas Toxo IgG IV may be related to the lack of antigen affinity purification and the sometimesdelicate microscope reading at the threshold dilution. In practice, IFA is used in our laboratory in combination with another method with different antibody kinetics, and it contributes to the dating of the seroconversion. For Vidas Toxo IgG IV and II, Toxo IgG Axsym, and IFA, we found 13 of 23 false-negative results and 7 of 9 false-positive results relating to immunocompromised patients. This is in line with the fact that serological methods are often not sufficient in the follow-up of immunocompromised patients (Arnold et al., 1997; Botterel et al., 2002). In seroconversion cases, Vidas Toxo IgG II and IV showed extremely similar antibody kinetics, but IgG appeared often earlier with IFA and Toxo IgG Axsym than with Vidas Toxo IgG II and IV. However, the detection of seroconversion is mainly based on the appearance of IgM, even if the final diagnosis of toxoplasmic seroconversion determined by the appearance of a specific IgG. In conclusion, Vidas Toxo IgG IV replaces Vidas Toxo IgG II by offering more standardized antigenic production and a lower number of indeterminate results while retaining equivalent high sensitivity and specificity. Table 2 Consistency and discrepancies among the 4 immunoassay systems for Toxoplasma IgG antibody detection in 596 sera Test systems TrueTrueFalseFalseIndeterminate positivea negativea positivea negativea resultb Vidas Toxo IgG IV Vidas Toxo IgG II Toxo IgG Axsym IFA a
223
355
2
3
13
210
362
1
4
19
224
355
4
0
13
214
364
2
16
0
The sera were classified as positive or negative IgG according to the results of Vidas Toxo IgG II, Toxo IgG Axsym, and IFA when all 3 techniques showed similar results and according to the result of dye test in cases of discrepancy or indeterminate results with other techniques. b The indeterminate result of Vidas Toxo IgG IV was from 2 to 5 IU/mL; Vidas Toxo IgG II, 4 –7 IU/mL; Toxo IgG Axsym IV, 2 IU/mL.
N. Roux-Buisson et al. / Diagnostic Microbiology and Infectious Disease 53 (2005) 79 – 81
Acknowledgments The authors thank Drs Thuillez and Romand for their contributions, E. Issartel, C. Barois, C. Mur, and G. Gervasi for their technical assistance, N. Falchero for the statistic analysis, and C. Dupuy and S. Gaymard for rereading the manuscript. References Ambroise-Thomas P, Garin JP, Rigaud A (1966) Ame´lioration de la technique d’immunofluorescence par l’emploi de contre-colorants. Application a` la toxoplasmose. Presse Med 74:2215 – 2216. Arnold SJ, Kinney MC, McCormick MS, Dummer S, Scott MA (1997) Disseminated toxoplasmosis: Unusual presentations in the immunocompromised host. Arch Pathol Lab Med 121:869 – 873. Botterel F, Ichai P, Feray C, Bouree P, Saliba F, Tur Raspa R, Samuel D, Romand S (2002) Disseminated toxoplasmosis, resulting from infection of allograft, after orthotopic liver transplantation: Usefulness of quantitative PCR. J Clin Microbiol 40:1648 – 1650. Cimon B, Marty P, Morin O, Bessieres MH, Marx-Chemla C, GayAndrieu F, Thulliez P (1998) Specificity of low anti-Toxoplasma IgG titers with IMx and AxSYM Toxo IgG assays. Diagn Microbiol Infect Dis 32:65 – 67.
81
De Champs C, Pelloux H, Cambon M, Fricker-Hidalgo H, Goullier-Fleuret A, Ambroise-Thomas P (1997) Evaluation of the second generation IMx Toxo IgG antibody assay for detection of antibodies to Toxoplasma gondii in human sera. J Clin Lab Anal 11:214 – 219. Goubet S, Pelloux H, Fricker-Hidalgo H, Goullier-Fleuret A, AmbroiseThomas P (1999) Se´rodiagnostic de la toxoplasmose: Comparaison de la trousse Elisa AxsymR (Abbott) avec la trousse Vidas (bioMe´rieux), l’immunofluorescence indirecte et l’Isaga. Ann Biol Clin 57:481 – 484. Hofgartner WT, Swanzy SR, Bacina RM, Condon J, Gupta M, Matlock PE, Bergeron DL, Plorde JJ, Fritsche TR (1997) Detection of immunoglobulin G (IgG) and IgM antibodies to Toxoplasma gondii: Evaluation of four commercial immunoassay systems. J Clin Microbiol 35:3313 – 3315. Pelloux H, Ciapa P, Goullier-Fleuret A, Ambroise-Thomas P (1993) Evaluation du syste`me Vidas pour le diagnostic se´rologique de la toxoplasmose. Ann Biol Clin 50:875 – 878. Reiter-Owona I, Petersen E, Joynson D, Aspock H, Darde ML, Disko R, Dreazen O, Dumon H, Grillo R, Gross U, Hayde M, Holliman R, Ho-Yen DO, Janitschke K, Jenum PA, Naser K, Olszewski M, Thulliez P, Seitz HM (1999) The past and present role of the Sabin-Feldman dye test in the serodiagnosis of toxoplasmosis. Bull World Health Organ 77:929 – 935. Santoro F, Afchain D, Pierce R, Cesbron JY, Ovlaque G, Capron A (1985) Serodiagnosis of toxoplasma infection using a purified parasite protein (P30). Clin Exp Immunol 62:262 – 269. Schwartz D (1986) Me´thodes statistiques a` l’usage des me´decins et des biologistes. Paris7 Flammarion Me´decine-Sciences.
Comparative analysis of the VIDAS Toxo IgG IV assay in the detection of antibodies to Toxoplasma gondii B Nathalie Roux-Buissona, He´le`ne Fricker-Hidalgoa,T, Agne`s Foussadierb, Dominique Rollandb, Anne-Sophie Suchel-Jambonb, Marie-Pierre Brenier-Pincharta, Herve´ Pellouxa a
Service de Parasitologie-Mycologie, Centre Hospitalier Universitaire, BP217, 38043 Grenoble, France b Recherche et De´veloppement, bioMe´rieux, Chemin de l’Orme, 69280 Marcy l’Etoile, France Received 4 January 2005; accepted 21 April 2005
Abstract A new serological test, Vidas Toxo IgG IV, has been developed with antigens obtained from tachyzoites cultured on cells. Vidas Toxo IgG IV replaces Vidas Toxo IgG II by offering a more standardized antigenic production and a lower number of indeterminate results while retaining equivalent sensitivity and specificity. D 2005 Elsevier Inc. All rights reserved. Keywords: Toxoplasma gondii; Vidas Toxo IgG IV; Toxoplasmosis; Antigens
1. Introduction
2. Materials and methods
A new version of the serological test Vidas Toxo IgG has been recently developed with antigens obtained from tachyzoites cultured on cells and not on mice. To avoid the use of laboratory animals, in vitro maintenance on cell culture is used to obtain tachyzoites for antigen preparation. Affinity-purified P30-enriched fraction of Toxoplasma gondii antigens was prepared for a new immunoenzymatic test developed by bioMe´rieux, Vidas Toxo IgG IV, which would replace Vidas Toxo IgG II. The aim of our study is to evaluate Vidas Toxo IgG IV’s sensitivity, specificity, and ability to swiftly detect IgG antibodies and to compare its performance with 3 other techniques: Vidas Toxo IgG II (bioMe´rieux), Toxo IgG Axsym (Abbott), and indirect immunofluorescence assay (IFA).
The study related to 656 sera, obtained from the Parasitology–Mycology Laboratory at Grenoble hospital. Of the 656 sera, 596 sera were obtained from the routine activity of the laboratory and consisted of sera from pregnant women, newborns, immunocompetent and immunocompromised patients, and 60 sequential sera were obtained from 20 pregnant women showing seroconversion (3 sera per patient). Vidas Toxo IgG IV, marketed by bioMe´rieux (69280 Marcy l’Etoile/France), is an automated assay for the Vidas system. The antigens were of membrane and cytoplasmic origin (RH Sabin strain). T. gondii tachyzoites is obtained from in vitro cell culture. After lysis, affinity chromatography is performed to obtain P30-enriched fraction as previously described (Santoro et al., 1985). The other techniques were Vidas Toxo IgG IV (Pelloux et al., 1993), Toxo IgG Axsym (Abbott Laboratories, Diagnostics Division, Abbott Park, IL) (Goubet et al., 1999), and IFA (Ambroise-Thomas et al., 1996). When the IgG detection result of a technique was discrepant with that of the other tests, dye test was performed by Dr P. Thulliez (Institut de Pue´riculture, Paris, France) (Reiter-Owona et al., 1999). For each serum, the biologic interpretation (presence or absence of IgG) considered results obtained with Vidas Toxo IgG II, Toxo IgG Axsym, and IFA. The interpretation was easy when all
B
The results included in this article were previously presented in a French national congress: poster: Fricker-Hidalgo, H., Roux-Buisson, N., Foussadier, A., Rolland, D., Suchel-Jambon, A.S., Brenier-Pinchart, M.P., Pelloux, H. Un nouveau test ELISA, Vidas Toxo IgG IV: e´valuation par rapport a` trois autres techniques se´rologiques, Congre`s de la Socie´te´ Franc¸aise de Parasitologie, Maisons-Alfort, France, 16 –18 de´cembre 2003. T Corresponding author. Tel.: +33-4-76765490; fax: +33-4-76765660. E-mail address: [email protected] (H. Fricker-Hidalgo). 0732-8893/$ – see front matter D 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.diagmicrobio.2005.04.005
80
N. Roux-Buisson et al. / Diagnostic Microbiology and Infectious Disease 53 (2005) 79 – 81
Table 1 Resolved sensitivities, specificities, and positive and negative predictive values of the immunoassay systems evaluated Test systems
a
Sensitivity (%)
Vidas Toxo IgG IV 98.67 Vidas Toxo IgG II 98.13 Toxo IgG Axsym 100.00 IFA 93.04
Specificity (%) 99.44 99.72 98.89 99.45
b
Positive Negative predictive predictive valuec (%) valued (%) 99.11 99.53 98.25 99.07
99.16 98.91 100.00 95.79
a
Sensitivity = true-positive/(true-positive + false-negative). Specificity = true-negative/(true-negative + false-positive). c Positive predictive value = true-positive/(true-positive + falsepositive). d Negative predictive value = true-negative/(true-negative + falsenegative). b
3 techniques showed similar results. Any serum showing a discrepancy or indeterminate result with a technique was retested with the considered technique and the dye test (Reiter-Owona et al., 1999). The results of the dye test allowed to classify the sera as positive or negative IgG. The sensitivities, the specificities, and the positive and negative predictive values of each technique were calculated in reference to the classification of sera (Table 1) and were compared using the McNemar test (Schwartz, 1986). 3. Results Three hundred sixty-six sera out of 596 routine laboratory sera were considered as negative for anti-T. gondii IgG and 230 as positive. Dye test was performed on 57 sera. The overall consistency between the various methods was 97.68% (548/561) and was between 96.74% and 99.12%, when the assays were compared in pairs. Vidas Toxo IgG IV and II and Toxo IgG Axsym showed statistically equivalent sensitivity and specificity (Table 1). IFA showed an equivalent specificity at 99.45% but a statistically significant lower sensitivity (93.04%) than Toxo IgG Axsym (100%), Vidas Toxo IgG IV (98.67%), and Vidas Toxo IgG II (98.13%). Sixteen false-negative results were observed with IFA (Table 2). Vidas Toxo IgG IV showed 13/596 (2.18%) indeterminate results, similar to Toxo IgG Axsym and less than Vidas Toxo IgG II (19/596, 3.18%) (Table 2). The ability to detect IgG antibodies earlier than other assays was evaluated on 60 sera obtained from 20 seroconverted women (3 sera per patient). When we analyzed the results of the second serum of the 20 patients, the number of positive results was 8 with Vidas Toxo IgG IV, 9 with Vidas Toxo IgG II, 16 with Toxo IgG Axsym, and 17 with IFA. The number of positive results of the third serum was 17 with Vidas Toxo IgG IV, 17 with Vidas Toxo IgG II, 20 with Toxo IgG Axsym, and 20 with IFA. Thus, IgG appeared often earlier with IFA and Toxo IgG Axsym than with Vidas Toxo IgG II and IV.
4. Discussion The main interest of Vidas Toxo IgG IV lies in the preparation of the antigen, produced on cell culture and not on mice as with Vidas Toxo IgG II. It makes preparation easier and more reproducible, and the sensitivity and specificity of Vidas Toxo IgG IV were equivalent to Vidas Toxo IgG II. In a previous study (Goubet et al., 1999) evaluating Vidas Toxo IgG II, Toxo IgG Axsym, and IFA, the consistencies were equivalent to those found in this study. Similar sensitivity and specificity values for Vidas Toxo IgG II have been reported by other authors (De Champs et al., 1997; Hofgartner et al., 1997; Pelloux et al., 1993). Cimon et al. (1998) found a specificity of 95.6% for Toxo IgG Axsym in low antibody titers in pregnant women. The lower sensitivity of IFA compared with Toxo IgG Axsym and Vidas Toxo IgG IV may be related to the lack of antigen affinity purification and the sometimesdelicate microscope reading at the threshold dilution. In practice, IFA is used in our laboratory in combination with another method with different antibody kinetics, and it contributes to the dating of the seroconversion. For Vidas Toxo IgG IV and II, Toxo IgG Axsym, and IFA, we found 13 of 23 false-negative results and 7 of 9 false-positive results relating to immunocompromised patients. This is in line with the fact that serological methods are often not sufficient in the follow-up of immunocompromised patients (Arnold et al., 1997; Botterel et al., 2002). In seroconversion cases, Vidas Toxo IgG II and IV showed extremely similar antibody kinetics, but IgG appeared often earlier with IFA and Toxo IgG Axsym than with Vidas Toxo IgG II and IV. However, the detection of seroconversion is mainly based on the appearance of IgM, even if the final diagnosis of toxoplasmic seroconversion determined by the appearance of a specific IgG. In conclusion, Vidas Toxo IgG IV replaces Vidas Toxo IgG II by offering more standardized antigenic production and a lower number of indeterminate results while retaining equivalent high sensitivity and specificity. Table 2 Consistency and discrepancies among the 4 immunoassay systems for Toxoplasma IgG antibody detection in 596 sera Test systems TrueTrueFalseFalseIndeterminate positivea negativea positivea negativea resultb Vidas Toxo IgG IV Vidas Toxo IgG II Toxo IgG Axsym IFA a
223
355
2
3
13
210
362
1
4
19
224
355
4
0
13
214
364
2
16
0
The sera were classified as positive or negative IgG according to the results of Vidas Toxo IgG II, Toxo IgG Axsym, and IFA when all 3 techniques showed similar results and according to the result of dye test in cases of discrepancy or indeterminate results with other techniques. b The indeterminate result of Vidas Toxo IgG IV was from 2 to 5 IU/mL; Vidas Toxo IgG II, 4 –7 IU/mL; Toxo IgG Axsym IV, 2 IU/mL.
N. Roux-Buisson et al. / Diagnostic Microbiology and Infectious Disease 53 (2005) 79 – 81
Acknowledgments The authors thank Drs Thuillez and Romand for their contributions, E. Issartel, C. Barois, C. Mur, and G. Gervasi for their technical assistance, N. Falchero for the statistic analysis, and C. Dupuy and S. Gaymard for rereading the manuscript. References Ambroise-Thomas P, Garin JP, Rigaud A (1966) Ame´lioration de la technique d’immunofluorescence par l’emploi de contre-colorants. Application a` la toxoplasmose. Presse Med 74:2215 – 2216. Arnold SJ, Kinney MC, McCormick MS, Dummer S, Scott MA (1997) Disseminated toxoplasmosis: Unusual presentations in the immunocompromised host. Arch Pathol Lab Med 121:869 – 873. Botterel F, Ichai P, Feray C, Bouree P, Saliba F, Tur Raspa R, Samuel D, Romand S (2002) Disseminated toxoplasmosis, resulting from infection of allograft, after orthotopic liver transplantation: Usefulness of quantitative PCR. J Clin Microbiol 40:1648 – 1650. Cimon B, Marty P, Morin O, Bessieres MH, Marx-Chemla C, GayAndrieu F, Thulliez P (1998) Specificity of low anti-Toxoplasma IgG titers with IMx and AxSYM Toxo IgG assays. Diagn Microbiol Infect Dis 32:65 – 67.
81
De Champs C, Pelloux H, Cambon M, Fricker-Hidalgo H, Goullier-Fleuret A, Ambroise-Thomas P (1997) Evaluation of the second generation IMx Toxo IgG antibody assay for detection of antibodies to Toxoplasma gondii in human sera. J Clin Lab Anal 11:214 – 219. Goubet S, Pelloux H, Fricker-Hidalgo H, Goullier-Fleuret A, AmbroiseThomas P (1999) Se´rodiagnostic de la toxoplasmose: Comparaison de la trousse Elisa AxsymR (Abbott) avec la trousse Vidas (bioMe´rieux), l’immunofluorescence indirecte et l’Isaga. Ann Biol Clin 57:481 – 484. Hofgartner WT, Swanzy SR, Bacina RM, Condon J, Gupta M, Matlock PE, Bergeron DL, Plorde JJ, Fritsche TR (1997) Detection of immunoglobulin G (IgG) and IgM antibodies to Toxoplasma gondii: Evaluation of four commercial immunoassay systems. J Clin Microbiol 35:3313 – 3315. Pelloux H, Ciapa P, Goullier-Fleuret A, Ambroise-Thomas P (1993) Evaluation du syste`me Vidas pour le diagnostic se´rologique de la toxoplasmose. Ann Biol Clin 50:875 – 878. Reiter-Owona I, Petersen E, Joynson D, Aspock H, Darde ML, Disko R, Dreazen O, Dumon H, Grillo R, Gross U, Hayde M, Holliman R, Ho-Yen DO, Janitschke K, Jenum PA, Naser K, Olszewski M, Thulliez P, Seitz HM (1999) The past and present role of the Sabin-Feldman dye test in the serodiagnosis of toxoplasmosis. Bull World Health Organ 77:929 – 935. Santoro F, Afchain D, Pierce R, Cesbron JY, Ovlaque G, Capron A (1985) Serodiagnosis of toxoplasma infection using a purified parasite protein (P30). Clin Exp Immunol 62:262 – 269. Schwartz D (1986) Me´thodes statistiques a` l’usage des me´decins et des biologistes. Paris7 Flammarion Me´decine-Sciences.