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Previous Article | Next Article 
Clinical and Diagnostic Laboratory Immunology, July 1999, p. 514-518, Vol. 6, No. 4
1071-412X/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Immunoglobulin G Avidity in Diagnosis of
Toxoplasmic Lymphadenopathy and Ocular Toxoplasmosis
Malgorzata
Paul*
Department of Medical Microbiology, Institute
of Microbiology and Infectious Diseases, University of Medical
Sciences, Pozna
, Poland
Received 15 September 1998/Returned for modification 14 January
1999/Accepted 15 March 1999
 |
ABSTRACT |
Traditional serological techniques have some limitations in
evaluating the duration of Toxoplasma gondii infection in
pregnant women, patients with lymphadenopathy, and older children
suspected of having congenital toxoplasmosis. In these three groups of
patients, two variants of T. gondii immunoglobulin G (IgG)
avidity tests were used: an EIA Kit (Labsystems) and a noncommercial
enzyme-linked immunosorbent assay specially elaborated in the
laboratory. The avidity of specific IgG in sera from 23 patients with a
known recently acquired infection (mainly pregnant women) was low (less than 30%), whereas that in sera from 19 patients with toxoplasmic lymphadenopathy of 3 weeks to 6 months in duration (mean, 8.3 weeks)
covered a large range (between 0.2 and 57.8%; mean, 25.7%); high
avidity results were observed for 10 of 19 patients (52.6%). The large
range of IgG avidity in patients with toxoplasmic lymphadenopathy suggests various durations of infection in these patients, with a
tendency for a chronic phase of toxoplasmosis. According to the avidity
marker, five patients with lymphadenopathy for less than 3 months did
not have a recent Toxoplasma infection. In 6 of 19 patients
with lymphadenopathy (31.6%), low IgG avidity values persisted until 5 months after the first serological examination. In all four patients
with a documented chronic course of Toxoplasma infection (6 months to 8 years after the first positive serology), high IgG avidity
values were observed. Among sera from 10 children and young
immunocompetent adults suspected of having ocular reactivation of
congenital toxoplasmosis, all had high IgG avidity values (over 40%),
suggesting congenitally acquired ocular infection rather than
noncongenital infection. In conclusion, the avidity of IgG is a
valuable marker of recent toxoplasmosis in pregnant women, suggests the
duration of invasion in patients with lymphadenopathy, and may be
helpful for differentiation between reactivation of congenital
infection and recently acquired ocular toxoplasmosis in immunocompetent
patients. A low IgG avidity does not always identify a recent case of
toxoplasmosis, but a high IgG avidity can exclude primary infections of
less than 5 months' duration.
| |
INTRODUCTION |
In Poland, where the rate of
seropositivity for Toxoplasma gondii in the adult population
is about 60% (24), the differential diagnosis between
recent and chronic infections may be important for a clinician.
Clinical symptoms, if any, are of limited value in evaluation of the
duration of T. gondii infection (9, 21).
Lymphadenopathy may occur at different times after the initial T. gondii infection, persist, and/or recur for various times
independently of the specific antiparasitic treatment. Differentiation
between congenital and acquired ocular toxoplasmosis is difficult when
some fresh lesions are visible only without retinochoroidal scans
(5, 8).
Traditional immunodiagnostic techniques also have some limitations in
evaluations of the timing of T. gondii infection. High or
increasing titers of specific immunoglobulin G (IgG) antibodies, especially if they are detected by two different techniques, are helpful in the differentiation of recent and late infections (3, 4, 23). However, in patients with reactivation of chronic Toxoplasma infection, a significant rise in the IgG antibody
titer is not always observed, especially in older children or
adolescents with ocular manifestations of congenital toxoplasmosis.
Interpretation of the patterns of other immunoglobulins also has some
limitations. For example, IgM antibodies can be present some years
after the initial infection (residual IgM) (2, 20).
Similarly, specific IgA antibodies can be detected as late as 45 months
after a documented seroconversion (6), during a 2-year
observation period after their initial detection (18), or in
the 8 months after the start of lymphadenopathy (21).
Specific IgE antibodies are usually synthesized in a recent stage of
infection, but they can also be detected up to 7 months after the onset
of clinical symptoms (21).
The measurement of the avidity of anti-T. gondii-specific
IgG antibodies for the differentiation of recent and late infections was introduced some time ago but was used mainly with pregnant women to
evaluate the risk of congenital toxoplasmosis (9, 13, 17).
This study has been undertaken to observe the maturation of the
specific IgG avidity in the course of T. gondii
lymphadenopathy and to differentiate the recently acquired
retinochoroidal lesions from reactivated ones in patients with
congenital toxoplasmosis.
| |
MATERIALS AND METHODS |
Patients.
In 1995 and 1996, sera from 56 patients were
examined in the Clinic of Parasitic and Tropical Diseases in
Pozna, Poland. Forty-six patients had acquired toxoplasmosis and
had various stages of infection. Ten patients with ocular toxoplasmosis
were either children or adolescents with active, fresh foci of the retinochoroiditis type alone (n = 4) or foci that were
situated close to the old pigmented lesion and that were strongly
suspected of being a reactivation of congenital toxoplasmosis
(n = 6). The patients were divided into four groups
depending on the clinical expression of toxoplasmosis, duration of
symptoms, and the kinetics of specific IgG and IgM antibodies (Table
1).
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TABLE 1.
Classification of the 56 patients with acquired or
congenital toxoplasmosis according to duration of infection,
clinical expression, and results of conventional serological tests
|
|
Serological tests. (i) Detection of specific IgG and IgM
antibodies.
IgG antibodies to T. gondii were detected
by an automatic assay (VIDAS TOXO IgG; VITEK system, bioMérieux,
Marcy-l'Étoile, France), which is based on an enzyme-linked
immunofluorescence assay, and an indirect immunofluorescence assay.
Specific IgM titers were measured by VIDAS TOXO IgM, IgM immunosorbent
agglutination assay, and an indirect immunofluorescence assay as
described previously (1, 25, 26).
(ii) Toxoplasma-specific IgG avidity tests.
IgG
avidity was determined (i) with the Toxoplasma gondii IgG
avidity EIA Kit (Labsystems, Helsinki, Finland) and (ii) by a
noncommercial enzyme-linked immunosorbent assay (ELISA; avidity ELISA)
elaborated in 1996 in the Clinic of Parasitic and Tropical Diseases in
Pozna, Poland.
For use of the Toxoplasma gondii IgG avidity EIA Kit
(Labsystems), each serum sample was examined in increasing serial
dilutions (1:50, 1:200, 1:800, 1:3,200, 1:12,800) in a separate row of
titration plate wells coated with T. gondii antigen
(inactivated tachyzoites from mouse peritoneal fluid) at a volume of
100 µl. The four highest dilutions (starting from 1:200) were placed
in wells A to D, respectively, and the four lowest dilutions (starting
from 1:50) were placed in wells E to H, respectively. After 60 min of
incubation at 37°C, wells A to D were washed with phosphate-buffered
saline (PBS)-Tween and wells E to H were washed with 6 M urea in
PBS-Tween (three times for 5 min each time), with 150 µl of the
washing solution used per well. After the washing step, 100 µl of
sheep anti-human IgG alkaline phosphatase conjugate diluted 1:10 in PBS
was added to the wells, and the plate was left for 60 min at 37°C.
After incubation, all wells were washed in PBS-Tween and 100 µl of
p-nitrophenyl phosphate (5 mg of p-nitrophenyl
phosphate/2.5 ml) in 1.01 M diethanolamine buffer (pH 9.9) containing
0.5 mM MgCl2 was then added as a substrate solution to each
well. After 30 min of incubation in the dark at 37°C, the reaction
was stopped by the addition of 100 µl of 1 M NaOH per well and
thorough mixing. The optical density (OD) at 405 nm was measured
against a blank substrate with an automatic spectrophotometer
(Multiscan PLUS; Labsystems).
One-low avidity sample and one-high avidity sample were used as
controls for the assay.
Two titration curves, the first obtained from a traditional PBS-Tween
washing and the second obtained from a washing with urea solution, were
drawn on millimeter paper for each patient's sample. The distances
between the OD of the curve obtained from washing with PBS-Tween and
the OD of the curve obtained from avidity washing were measured at a
cutoff of 0.2, and the results (percent avidity) were read according to
the table included by the manufacturer (curve-shift method).
Values of less than 15% indicated low avidity, values of between 15 and 30% were considered borderline avidity, and values higher than
30% were considered high avidity.
For the noncommercial avidity ELISA, anti-T. gondii-specific
IgG antibodies were first detected by indirect ELISA in order to
establish the final dilution of each serum that crossed the cutoff line
(OD of 0.4). The final dilution for each patient's sample, defined
during multiple preliminary experiments, was then selected for IgG
avidity determination (final dilution method) (19).
The wells of flat-bottom polystyrene microtiter plates (Kartell,
Noviglio, Italy) were coated with T. gondii antigen, the contents of each well were diluted 1:200 in 50 mM carbonate-bicarbonate buffer (pH 9.6) at a volume of 100 µl per well, and the plates were
incubated overnight at 4°C.
A soluble antigen of T. gondii was prepared from lyophilized
tachyzoites of the RH strain of T. gondii
(bioMérieux). The toxoplasmas were lysed with distilled water
(5 × 108 tachyzoites in 1 ml of distilled water) and
were then disrupted by six successive freeze-thaw cycles
(7). This suspension, consisting of membranous and
cytoplasmic antigens, was used for the ELISA.
In the saturation step, which was aimed at the binding of uncoated
antigenic sites, the wells were covered with 2% bovine serum albumin
(BSA; FR-5, Sigma) in PBS containing 0.05% Tween 20 (PBS-Tween [pH
7.4]), and the plates were incubated for 60 min at room temperature
(RT). After three washes with PBS-Tween, 100 µl of the final dilution
of each serum sample in 1% BSA-PBS-Tween was added to two separate
wells in different plates. After 60 min of incubation at 37°C, the
first plate was washed three times with PBS-Tween and the other plate
was washed three times with a modified PBS-Tween buffer containing 6 M
urea and a fourth time with a traditional PBS-Tween. Alkaline
peroxidase-conjugated (Jackson ImmunoResearch Laboratories, Inc., West
Grove, Pa.) rabbit anti-human IgG antibody (heavy and light chains) was
diluted 1:20,000 in 1% BSA-PBS-Tween at a volume of 100 µl and was
added to the wells, and both plates were left for 60 min at RT. After
incubation, the plates were washed three times with PBS-Tween and
3,3',5,5'-tetramethylbenzidine (TMB; 1-mg TMB tablets; Sigma) dissolved
in substrate solution containing 0.15 M citrate buffer, and 0.02%
H2O2 (1 mg of TMB/ml) was added to each well at
a volume of 100 µl. The plates were then incubated for 20 min in the
dark at RT. The reaction was stopped by the addition of 50 µl of 2 M
H2SO4 to the wells. The OD values at 450 nm
were measured by using an automatic spectrophotometer (Multiscan PLUS; Labsystems).
The results were expressed as percent avidity, calculated as a ratio
between the OD for the sample washed with urea solution and the OD for
the sample washed with a standard PBS-Tween buffer (14).
Values of greater than 40% indicated a high avidity of specific IgG,
values of between 31 and 40% were considered borderline avidity, and
30% indicated low avidity.
Twenty-five serum samples from seronegative healthy patients (as
determined with the VIDAS TOXO IgG and VIDAS TOXO IgM Kits) were used
as a control group. The cutoff point for IgG ELISA was calculated as
the mean OD value for seronegative controls plus 2 standard deviations
(cutoff of 0.4).
Statistical analysis of results.
Statistical analysis of the
results was done with the Microsoft Excel (version 7.0) program for
evaluation of the 
2 test, Student's t test,
and the nonparametric Fisher exact test for small numbers and some
general statistical functions such as arithmetic mean, median, standard
deviation, and coefficient of variance.
| |
RESULTS |
Results obtained with commercial Toxoplasma gondii IgG
avidity EIA Kit (Labsystems).
The Labsystems kit was used to test
18 serum samples from 18 patients with various stages of acquired
toxoplasmosis. The results are presented in Fig.
1. Nine patients had recent toxoplasmosis of 2 to 6 weeks' duration (mean, 4.2 weeks), five patients had lymphadenopathy of 2 to 4 months' duration (mean, 2.6 months), and
four patients had chronic toxoplasmosis of 6 months' to 8 years'
duration (mean, 13 months).
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FIG. 1.
Results of IgG avidity for 18 patients with acquired
toxoplasmosis examined by using the Toxoplasma gondii IgG
avidity EIA Kit (Labsystems).
|
|
Sera from all nine patients with recent toxoplasmosis had low avidity
values (<15%), i.e., between 1.0 and 13.4% (mean, 6.3% ± 4.5%).
Five patients with lymphadenopathy and subacute toxoplasmosis had a
wider range of IgG avidity (6.0 to 50%; mean, 25.0% ± 16.9%); four
patients had high or borderline results (>15%). All four patients
with chronic toxoplasmosis had high avidity values (over 30%, i.e.,
from 33.0 to 87.1%; mean, 64.3% ± 27.2%). The mean avidity values
for low- and high-avidity controls of the test were 2.3 and 71.9%, respectively.
The increase in IgG avidity with the duration of toxoplasmosis is
presented in Fig. 1, and its statistical significance was confirmed by
the Fisher test for small numbers (P = 0.01).
Results of noncommercial avidity ELISA.
The original
noncommercial avidity ELISA was used to test 71 serum samples from 52 patients with various stages of acquired T. gondii infection
and ocular toxoplasmosis of unknown origin: acquired or congenital. The
results are presented in Fig. 2.
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FIG. 2.
Results of IgG avidity for 71 serum samples from 52 patients with recent infection, toxoplasmic lymphadenopathy, or ocular
reactivation of congenital toxoplasmosis by a noncommercial ELISA.
|
|
For sera from 23 patients with seroconversion or in the early stage of
T. gondii infection (less than 8 weeks after an initial infection), IgG avidity values were low (between 0.1 and 35.3%; mean,
13.2% ± 13.3%).
For sera from 19 patients with toxoplasmic lymphadenitis who were
examined for the first time 3 weeks to 6 months (mean, 8.3 weeks) after
their lymphadenopathy occurred, the range of IgG avidity was wide
(between 0.2 and 57.8%; mean, 25.7% ± 16.6%); a low IgG avidity
(<30%) was observed for sera from 9 patients (47.4%). The positive
correlation between an increasing IgG avidity value and a longer
duration of lymphadenopathy was statistically significant (P = 0.02). Upon reexamination of sera from these 19 patients after 5 months, IgG avidity results were between 6.6 and 59.8% (mean, 41.5% ± 17.5%), with a dominance of values over 40% for 13 patients
(68.4%). The results are presented at Fig. 3. For all patients, over the 5 months of
observation an increase in the IgG avidity values of from 1.7 to 52.4%
(mean, 17.3%) was observed. A lower increase was observed for patients
with lymphadenopathy of 
3 months' duration (P = 0.01). The positive predictive value of high avidity results at
the first examination in relation to the results at the reexamination 5 months later was 100% for 10 patients. The positive predictive value
of low avidity results at the reexamination in relation to the results
at the first serological examination 5 months earlier was
100% for six patients.
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FIG. 3.
Maturation of IgG avidity in 19 patients depending on
the duration of lymphadenopathy. Paired sera from individual patients
are connected by lines. I and II, first and second examinations,
respectively.
|
|
Sera from all 10 patients with ocular toxoplasmosis showed high avidity
results (between 40.7 and 86.8%; mean, 52.8% ± 15.0%). This fact
suggests a congenital origin of the eye lesions, which were reactivated
10 to 24 years (median, 16.5 years) after birth.
In summary, the IgG avidity statistically correlated with the duration
of T. gondii infection (P = 0.001). IgG
avidity values increased with time after the initial infection; the
best correlation was observed (P = 0.0001) between low
avidity and recent toxoplasmosis of less than 8 weeks' duration.
| |
DISCUSSION |
The determination of IgG avidity started in the 1980s in the
diagnosis of rubella, hepatitis C, and other viral infections (10,
12, 28). In pregnant women with antibodies to the rubella virus,
the measurement of IgG avidity was used to differentiate subclinical
primary infections characterized by low avidity from reinfections
characterized by high avidity and thus to evaluate the risk of
congenital rubella for the fetus (22, 27). Later, the
avidity test was introduced to differentiate recent and chronic T. gondii infections in pregnant women (9, 14, 17,
19). The value of using an avidity test to evaluate the risk of
congenital toxoplasmosis has been confirmed by the present study with
20 pregnant women who were close to seroconversion for toxoplasmosis and who had low avidity values.
For the 19 patients with toxoplasmic lymphadenopathy, the avidity
values covered a wide range by both commercial and noncommercial avidity assays. However, the distribution of avidity values had a
tendency to cluster for patients with similar durations of infections, as established by the kinetics of the IgG and IgM antibodies. On the
contrary, sera from patients with similar durations of lymphadenopathy
showed different patterns of increases in IgG avidity (Fig. 3).
The wide range of avidity values suggests that, at least in some
patients, lymphadenopathy may not be related to the early, acute stage
of infection only, as proposed by Koci
cka (15) and
Kocicka et al. (16), but may be a clinical sign that
occurs in patients with an advanced course of infection; one cannot
exclude the possibility that this is provoked by a superinfection. This suggestion is also supported by an observation that three patients with
lymphadenopathy of more than 3 months' duration had high avidity
values, which was similar to the case for seven of 16 patients with
lymphadenopathy of less than 3 months' duration. These results
indicate that lymphadenopathy of 3 months' duration may not be a
valuable clinical marker of a recent stage of infection (Fig. 3).
The duration of low avidity values in patients with lymphadenopathy is
not well defined. Holliman et al. (11) suggested that low
IgG avidity occurs during less than 3 months of lymphadenopathy. Lecolier and Pucheu (19) observed patients whose sera had a low IgG avidity for as long as 20 weeks after the acquisition of
infection. In the present study, low IgG avidity values were still
observed 5 months after the first serological examination in 6 of 19 patients with lymphadenopathy (31.6%). In conclusion, one can accept
the fact that although a high IgG avidity value strongly excludes a
recent infection, that is, one that was acquired during the previous 5 months, a low avidity is not a safe marker of an early stage of infection.
So far the avidity test has not been used for the differentiation of
primary and reactivated chronic infections. Holliman et al.
(11) showed no significant difference between avidity values
in human immunodeficiency virus-positive patients with toxoplasmic
encephalitis and those without clinical signs of reactivation; IgG
avidity was high (>50%) in both groups. Among other infectious diseases, in patients with rubella reinfection, high IgG avidity levels
were always detected (22, 27). These observations suggest that in patients with reactivated infection or reinfection, the IgG
avidity values remain high and constant, similar to those in the
chronic stage of infection.
For patients with ocular toxoplasmosis an avidity test may be important
for the differentiation of the fresh lesions in recently acquired
toxoplasmosis resulting from systemic parasitemia from the lesions that
occur in children and/or adolescents due to a reactivation of
congenital toxoplasmosis that was not previously diagnosed. In 10 patients examined in the present study, the high values of the IgG
avidity favor a congenital origin of ocular toxoplasmosis; a
reactivation of chronic acquired infection in immunocompetent patients
is less likely.
In summary, the IgG avidity test is a valuable diagnostic method for
differentiation of a recent infection and a chronic infection, especially in patients with lymphadenopathy, and confirmation of the
congenital origin of toxoplasmosis in older children with active
retinochoroidal lesions. Therefore, low IgG avidity values are not
sufficient to identify an acute case of toxoplasmosis, but high avidity
results can exclude a primary infection acquired during the previous 5 months.
| |
ACKNOWLEDGMENTS |
I thank Zbigniew S. Pawlowski from the University of Medical
Sciences in Pozna, Poland, for kind help during the study and the preparation of the manuscript.
This work was supported by The Polish-American Research Program Maria
Sk
odowska-Curie Joint Fund II (grant MZ-HHS-134/93).
| |
FOOTNOTES |
*
Mailing address: Department of Medical Microbiology,
Institute of Microbiology and Infectious Diseases, Karol Marcinkowski University of Medical Sciences, Wieniawskiego 3, 61-712 Pozna, Poland. Phone: (48) 61 853 64 77. Fax: (48) 61 847 74 90. E-mail: mpaul{at}eucalyptus.usoms.poznan.pl.
| |
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Clinical and Diagnostic Laboratory Immunology, July 1999, p. 514-518, Vol. 6, No. 4
1071-412X/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
