MAJOR ARTICLE

Congenital Toxoplasmosis and Reinfection during

Pregnancy: Case Report, Strain Characterization,
Experimental Model of Reinfection, and Review
Annie Elbez-Rubinstein,1 Daniel Ajzenberg,3,4 Marie-Laure Dard,3,4 Robert Cohen,2 Aurlien Dumtre,4 Hlne Yera,5
Emmanuelle Gondon,1 Jean-Claude Janaud,1 and Philippe Thulliez5
1

Service de Nonatologie and 2Laboratoire de Bactriologie, Hpital Intercommunal de Crteil, Crteil, 3Centre National de Rfrence
Toxoplasmose/Toxoplasma Biological Resource Center, Centre Hospitalier-Universitaire Dupuytren, and 4Laboratoire de Parasitologie-Mycologie, EA
3174-NETEC, Facult de Mdecine, Universit de Limoges, Limoges, and 5Institut de Puriculture de Paris, Paris, France

After primary maternal infection by Toxoplasma gondii

during gestation, the parasite may enter the fetal circulation by infection of the placenta. Placental transmission is less frequent when infection is acquired before
the tenth week of pregnancy and is very rare when infection is acquired before conception. Without treatment,
the incidence of fetal infection is 10%15% for acquisition during the first trimester, 30% for the second trimester, and 60% for the third trimester [1]. Early maternal infection (during the first and second trimester) may
result in severe congenital toxoplasmosis, including fetal
death and spontaneous abortion. By contrast, late maternal infection (during the third trimester) usually re-

Received 19 May 2008; accepted 18 August 2008; electronically published 20

November 2008.
Potential conflicts of interest: none reported.
Presented in part: VIII International Congress on Toxoplasmosis, Porticcio,
Corsica, France, 2731 May 2005 (abstract 26).
Financial support: Centre National de Rfrence (CNR) Toxoplasmose (06-SMIP-40-23); Toxoplasma Biological Resource Center.
Reprints or correspondence: Dr. Daniel Ajzenberg, Centre National de Rfrence
(CNR) Toxoplasmose, Laboratoire de Parasitologie et de Mycologie, Centre
Hospitalier-Universitaire Dupuytren, 2 avenue Martin Luther King, 87042 Limoges,
France (ajz@unilim.fr).
The Journal of Infectious Diseases 2009; 199:280 5
2008 by the Infectious Diseases Society of America. All rights reserved.
0022-1899/2009/19902-0017$15.00
DOI: 10.1086/595793

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Elbez-Rubinstein et al.

sults in subclinical toxoplasmosis in newborns. In these

cases, infection initially goes unnoticed, but these babies
can develop chorioretinitis during later life [2]. Acute
infection is followed by the formation of cysts in chronic
infection and is associated with an immune response
that usually confers protection against reinfection. This
chronic infection is characterized by stable titers of specific IgG. In immunocompetent mothers who have been
immunized against toxoplasmosis before conception,
immune mechanisms prevent transmission of the infection to their fetuses. We report a case of life-threatening,
disseminated congenital toxoplasmosis in an infant
born to an immunocompetent mother who had been
immunized against toxoplasmosis before conception.
We also isolated and characterized the strain that caused
the infection.
SUBJECTS, MATERIALS, AND METHODS
A 31-year-old woman, native to France, gave birth at
term to a 3050 g baby by cesarean delivery (this method
of delievery was decided on as a result of dystocia). It was
her second child, and the results of serological testing
during her previous pregnancy were consistent with a
past Toxoplasma infection. Several hours after birth, the

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We present a case of disseminated congenital toxoplasmosis in a newborn born to a mother who had been immunized against toxoplasmosis before conception. The mother was reinfected, likely by ingestion of imported raw
horse meat during pregnancy. This clinical presentation is exceptional in France and raised the possibility of
infection by a highly virulent Toxoplasma strain. The strain responsible was isolated from the peripheral blood of
the newborn, and when genotyped with microsatellite markers, it exhibited an atypical genotype, one which is
very uncommon in Europe but had been described in South America. We tested the hypothesis of a reinfection
with a different genotype by using an experimental mouse model, which confirmed that acquired immunity
against European Toxoplasma strains may not protect against reinfection by atypical strains acquired during
travel outside Europe or by eating imported meat.

Table 1.

Results of serological testing for mother and child infected with Toxoplasma.
IgG

Patient, date
Mother
2 May 2001
19 February 2002
25 March 2002
4 June 2002
27 June 2002
10 September 2002
Child, born on 27 June 2002
4 July 2002
1 April 2003
3 September 2003

Dye test,
IU/mL

ELISA,
IU/mL

HS or AC/HS
agglutination, IU/mL

IgG
avidity

IgM
ISAGA

IgA
ISAGA

4
4
4
...
1600
3200

3
3
3
31
524
...

2
2
2
...
100/800
400/1600

...
0.48
...
...
0.48
...

0
0
0
...
0
0

...
0
0
...
10
12

400
10
400

...
...
...

100
2
200

...
...
...

12
0
0

...
0
0

child presented hypotonia, liver and splenic enlargement, petechial purpura, and thrombocytopenia (platelet count, 17,000
platelets/L). Sepsis investigations ruled out a bacterial infection (blood culture results and C-reactive protein remained negative) and viral infection due to cytomegalovirus, herpes simplex
viruses 1 and 2, and echovirus. The following day, the baby became polypneic and hypoxic, requiring nasal oxygen therapy,
despite receipt of wide-spectrum antibiotic therapy (ampicillin,
gentamycin, and cefotaxime). A pulmonary radiograph showed
an alveolar syndrome. The results of a pulmonary computed
tomography (CT) scan and cardiac ultrasound were normal.
The diagnosis of congenital toxoplasmosis was suggested by
the ophthalmologist, who found multiple foci of chorioretinitis
on both eyes. The inflammation was moderate but involved the
macula in the right eye. The diagnosis was confirmed by analysis
of the newborns blood 8 days after birth: a polymerase chain
reaction (PCR) assay with a direct amplification of the Toxoplasma B1 gene was positive, and T. gondii was isolated by inoculation into mice. PCR of cerebrospinal fluid samples was negative. Specific IgM antibody synthesis in serum from the
newborn was demonstrated with an immunosorbent agglutination assay (ISAGA) (table 1). The results of an electroencephalogram, cranial radiograph, and ultrasound were normal, but a
cerebral CT scan showed diffuse microcalcifications. Treatment
with a combination of pyrimethamine, sulfadiazine, and folinic
acid began 6 days after birth and was continued throughout the
first year of life. After 1 week of treatment, hypotonia and thrombopenia disappeared. Pulmonary signs lasted for 12 days, and
chorioretinitis stabilized without the use of steroids. The last
cranial ultrasound showed no ventricular enlargement and only
1 calcification.

Fourteen months of follow-up serological testing showed a

decrease in specific IgG titer followed by a rebound after discontinuation of therapy at 1 year of age (table 1). After 5 years of
clinical follow-up, the childs neurological examination results
were normal, and the child was performing satisfactorily in
school. Ophthalmologic examination shows a large scar in the
right macula. The visual acuity is 2/10 in the right eye and 10/10
in the left eye; she wears corrective glasses and needs an orthoptic
aid.
Maternal clinical and laboratory data. The results of tests
for Toxoplasma antibodies performed in May 2001, before the
beginning of the pregnancy (October 2001), were consistent
with past infection (i.e., the results showed the presence of specific IgG antibodies in the dye test without detectable IgM). Serological results remained unchanged until 4 June 2002, at 32
weeks of pregnancy, when an increase in IgG titer was observed
and confirmed 3 weeks later by further testing (table 1).
The mother recalled severe asthenia, general dizziness, headache, and abdominal pain occurring on June 11. She had eaten
raw horse meat several times in May and June. Tests for underlying immunosuppression in the mother had negative results,
including complete phenotypes of circulating T lymphocytes,
functional testing of T lymphocytes, and serological testing for
HIV. The mother had had autoimmune thyroiditis (Hashimoto
disease) for years, and the level of antithyroglobulin antibodies
was high at the time of birth, signaling active thyroiditis.
Strain characterization. T. gondii was isolated from the
newborns peripheral blood 8 days after birth by mouse inoculation. The strain, called IPP-2002-URB, was virulent for mice at
the time of isolation: all inoculated mice died 9 days after inoculation. The results of genotyping this strain with 5 microsatel-

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NOTE. Thresholds of positivity were 2 IU/mL for the dye test and agglutination test with formalin-fixed tachyzoites
(HS antigen) and 3 IU/mL for ELISA (AxSym; Abbott); an AC/HS ratio (differential agglutination of acetone [AC]fixed vs.
HS-fixed tachyzoites) 4 indicated a nonacute pattern. An IgG avidity result 0.3 (Vidas; BioMrieux) was interpreted as
high avidity. An IgM immunosorbent agglutination assay (ISAGA) index from 3 to 12 was interpreted as positive for
infants, and an IgA ISAGA index from 9 to 12 was interpreted as positive for adults.

DISCUSSION
In relatively few cases, congenital toxoplasmosis results from reactivation of a latent infection in pregnant women with altered
immune status, such as that resulting from systemic lupus erythematosus or hematological malignancies [6] and HIV infection [79]. Some case reports involved congenital toxoplasmosis
transmitted from immunocompetent mothers infected before
conception, but clinical and serological data permitted researchers to date the occurrence of the primary infection to a few
months before the onset of pregnancy. Lymphadenopathy was
the most frequent clinical presentation, and it occurred 1 [10], 2
[6, 11, 12], or 3 months [13] before conception. In one case [14],
a flu-like syndrome was reported by the mother 2 months before
conception, whereas in another case [15], the recent infection
was asymptomatic and could be identified only by serological
data. In all these immunocompetent patients, the delayed transplacental transmission of Toxoplasma was explained by a persistent or recurrent parasitemia over a prolonged period.
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Table 2. Detection of experimentally induced mixed infections

in mouse brains by microscopic cyst examination and microsatellite analysis.

Reinfection delay,
mouse number
1 month after
initial infection
1
2
3
4
5
6
4 months after
initial infection
1
2
3
4
5
6

Number of cysts
in brain, PRU--Gal/
IPP-2002-URB

Microsatellite
B17 alleles,
334 bp (PRU--Gal)/
352 bp (IPP-2002-URB)

614/0
343/4
290/6
372/6
180/3
Not donea

/
/
/
/
/
Not donea

229/1
203/2
419/4
93/4
100/2
142/23

/
/
/
/
/
/

NOTE. Mice were initially infected with a transfected type II strain

(PRU-- Gal) and reinfected either 1 or 4 months later with IPP-2002-URB.
a

Because of death 12 days after reinfection.

To our knowledge, the case described in the present article is

the sixth case of congenital toxoplasmosis as a consequence of
maternal parasitemia following reinfection in an immunocompetent woman who had previous test results consistent with past
toxoplasmic infection (table 3) that has been reported in the
literature during the past 3 decades [16 20] . Our case is the first
in which the Toxoplasma strain likely to be the origin of reinfection was isolated. In all 6 cases, the serological data collected
before or at the beginning of the pregnancy ruled out a recent
infection before conception (i.e., the presence of IgG and absence of IgM). Reinfection with another strain during pregnancy
was a plausible explanation, with serological reactivation observed in the mother during gestation or at birth: increased titers
of IgG were observed in all cases, the appearance of IgA was
documented for 5 cases (IgA data was not reported for patient 5),
and the absence of IgM was documented for all cases except
patient 2 (for whom data showed the appearance of IgM at week
28 of amenorrhea). For 2 cases (patients 2 and 6 [the present
case]), a flu-like syndrome consistent with an acute toxoplasmosis had been reported by the mother before the observed serological reactivation during pregnancy. To support the hypothesis of maternal reinfection during pregnancy, the authors of all 6
case reports documented the absence of any underlying immunodeficiency in the mothers. In the case we describe, the mother
had active Hashimoto thyroiditis. In this autoimmune disease, a
defect in a subpopulation of NK immune cells has been described [21]. As NK cells are critical for the initiation of an im-

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lite markers have been described elsewhere [3]; it exhibited an

atypical genotype, one different from the 3 archetypal lineages of
T. gondii designated as types I, II, and III.
Experimental model of reinfection. To test the hypothesis
of reinfection, we created an experimental model of reinfection
by IPP-2002-URB in mice chronically infected by a type II strain
of T. gondii, PRU. We used a transfected PRU strain (PRU
galactosidase [PRU--Gal]) that expresses Escherichia coli
-galactosidase [4]. When submitted to X-gal staining, cysts of
the transfected strain (PRU--Gal) appear blue, whereas those
of the nontransfected strain (IPP-2002-URB) are not colored,
which permits these 2 strains to be microscopically differentiated. Furthermore, these 2 strains can be distinguished by PCR
assay by use of 1 microsatellite marker, B17, because the (TC)n
dinucleotide tandem repeat of this marker is repeated 16 times in
IPP-2002-URB and 7 times in archetypal type II strains such as
PRU or ME49 [3]. The length polymorphism of these 2 different
alleles (334 bp for PRU and 352 bp for IPP-2002-URB) can be
detected by automated capillary electrophoresis by use of an
ABI310 genetic analyzer and GeneScan software (Applied Biosystems), as described elsewhere [5]. Twelve mice were chronically infected by oral ingestion of PRU--Gal (20 cysts). Oral
reinfection with 20 cysts of IPP-2002-URB was performed on 2
groups of 6 mice, at 1 and 4 months, respectively, after primary
infection. Six weeks after reinfection, the brains of the mice were
submitted to X-gal staining and microsatellite analysis with the
B17 marker. By microscopic examination of each brain suspension, we identified reinfection in 4 of 5 mice in the 1-month
group and 6 of 6 mice in the 4-month group (table 2). By microsatellite analysis, the 2 genotypes were detected in 4 of 5 reinfected mice in the 1-month group and 5 of 6 reinfected mice in
the 4-month group (table 2).

Table 3. Reported cases of congenital toxoplasmosis transmitted from immunized mothers who experienced reinfection during
pregnancy, from literature of the past 3 decades.
Maternal data
Patient
1

Childs
clinical data

Clinical
None

Chorioretinitis at 3 weeks,
no other abnormalities
at 13 months

None

Disseminated
toxoplasmosis at birth,
favorable outcome
Disseminated
toxoplasmosis at birth;
decreased visual acuity
in right eye and normal
psychomotor
development at 5 years

None

NOTE.

Resident of France;
contact with a kitten
early in pregnancy
Resident of France;
contact with kittens in
eighteenth week of
pregnancy
Resident of France, born
in Haiti; lived in French
Guiana for 7 years
Born in Brazil, resident of
Switzerland for 6 years;
travel to and contact
with kittens in Brazil in
fifth month of
pregnancy
Born in Angola, resident
of France for 2 years

Flu-like syndrome at 19
weeks

None

Flu-like syndrome at 33
weeks

Native resident of France;

raw horse meat
consumption between
weeks 27 and 32 of
pregnancy

Serological

Year,
source

IgA, IgM, and an

increase in IgG at 11
weeks of pregnancy
IgA, IgM, and an
increase in IgG at 28
weeks of pregnancy

1991 [16]

IgA, IgM, and an

increase in IgG 1 month
after delivery
IgA, IgM, and an
increase in IgG at
delivery

NR [18]

IgA NR, IgM, and an

increase in IgG in eighth
month of pregnancy
IgA, IgM, and an
increase in IgG between
weeks 32 and 35 of
pregnancy

NR [20]

1992 [17]

2002 [19]

2002, present case

NR, not reported.

munological intestinal response against T. gondii [22], it cannot

be ruled out that this underlying disease could have favored oral
reinfection.
The immune response of the mother might be overwhelmed when reinfection occurs as the result of a massive
inoculum [16], a different infectious stage (oocyst vs. cysts)
[17], or a strain with a different genetic background [20]. In
the 6 cases of reinfection during pregnancy presented in table
3, epidemiological risk factors were present, such as contact
with kittens (patients 1, 2, and 4), consumption of imported
raw meat (horse meat was consumed by patient 6, described
here), birthplace and residence, or travel abroad (patient 4
could have been exposed in Brazil and patients 3 and 5 in
France after primary infection in Haiti and/or French Guiana
and Angola, respectively).
All 6 cases of congenital toxoplasmosis after maternal reinfection were diagnosed because the newborns were symptomatic.
In 3 cases (patients 2, 3, and 4), the clinical diagnosis was revealed by typical toxoplasmic chorioretinitis. In the 3 other cases
(patients 1, 5 and 6), the clinical presentation was more severe,
with a disseminated toxoplasmosis leading to spontaneous abortion in patient 1, cardiac abnormalities in the offspring of patient
5, and a bacterial sepsis-like infection in the infant described in
this article, which is very uncommon in congenital toxoplasmo-

sis [23]. These severe and unusual clinical presentations might

be explained by an infection during pregnancy due to a highly
virulent strain. In our case, the Toxoplasma strain (IPP-2002URB) was isolated from the peripheral blood of the newborn,
which traduces the high capacity for dissemination of this strain.
Furthermore, the genetic analysis of the strain showed an atypical genotype that is very uncommon in France, where 96% of
congenital toxoplasmosis is due to a single genotype, type II [24].
Conversely, type II strains seem rare outside Europe and North
America. In South America, Toxoplasma strains are genetically
more diverse, with many different genotypes described mainly
in Brazil and the Guianas [3, 2527]. These atypical South American strains, initially called exotic strains, belong to several
haplogroups that are endemic to South America [28, 29]. Because a large amount of the horse meat eaten in France is imported from South America (Argentina, Uruguay, and Brazil), it
is likely that the infecting strain in the case presented here originated from these countries, where similar atypical genotypes
had already been described [3]. Even if there is still no evidence
for a correlation between atypical strains and severe toxoplasmosis, disseminated cases in immunocompetent patients in
French Guiana or Suriname [25, 30] and congenital toxoplasmosis [24] are more often associated with atypical genotypes of
T. gondii.

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Spontaneous abortion at
12 weeks of gestation,
growth retardation
Strabismus and
chorioretinitis at 9
months, no other
complications at 3 years
Cataract and chorioretinitis
at one month

Epidemiological

Acknowledgments
We would like to thank our colleagues M. Robin and H. Vrillon from the
maternity ward of Saint Maurice Hospital for providing serological results

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for the mother and Anne Dao and Jean-Franois Dubremetz for providing us
the transfected strain PRU -Gal.

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The results of our experimental model confirmed reinfection

by the atypical strain IPP-2002-URB in mice chronically infected
by a type II strain of T. gondii. This experimental model had
already been used to demonstrate the possibility of reinfection in
mice by different T. gondii strains (type II challenged by type I or
III) [4, 31, 32]. The definitive proof of reinfection in our patient
would require the isolation and identification of the initial infecting strain, which would be nearly impossible to obtain. The
only alternative would be serotyping [33, 34], with results showing different serotypes in the mother before and after serological
reactivation, and in the newborn. Serotyping was attempted in
this case, but was unsuccessful for the mother before reactivation
because titers of anti-Toxoplasma antibodies were too low.
In France and probably elsewhere in Europe, congenital
toxoplasmosis following maternal reinfection during pregnancy
is exceptional. In these countries, past immunity usually protects
against reinfection because generally only 1 genotype (type II)
circulates in humans and in the environment [35, 36], and as a
consequence, there is a very low probability of reinfection with
different genotypes. However, in other areas, such as South
America, where the genetic diversity of Toxoplasma is higher,
reinfection with different genotypes is likely to occur more frequently. For instance, in Brazil, where cases of reinfection have
been described for acquired toxoplasmosis [37], congenital
toxoplasmosis due to reinfection during pregnancy might not be
so exceptional. Thus, we assume that pregnant women from Europe who have been immunized against type II strains but are
traveling in tropical areas or eat imported meat during pregnancy are at risk of reinfection by atypical strains. Conversely, as
reported in this review (see patients 3 and 5 in table 3), women
born in Africa or South America, and likely immunized against
atypical Toxoplasma strains before conception, could also be at
risk of reinfection by a type II strain when they migrate to European countries.
In conclusion, cases of reinfection with T. gondii involving an
immunocompetent pregnant woman are exceptional but show
that the presence of residual IgG-specific antibodies is not always
synonymous with protection against a new Toxoplasma infection. To our knowledge, the case described here is the first in
which the T. gondii strain involved in reinfection was isolated,
characterized, and studied in an experimental mouse model that
suggested immunity against a type II strain may not be protective against a reinfection with a different genotype, especially if it
is atypical. Because there is increasing evidence that Toxoplasma
strains are genetically more diverse outside Europe, health-care
providers in Europe should be aware of this possibility when
pregnant women travel abroad or eat imported meat.

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