Serological screening and toxoplasmosis exposure factors among pregnant women in the Democratic Republic of Sao Tome and Principe

Abstract

The seroprevalence of Toxoplasma gondii infection among pregnant women in the Democratic Republic of Sao Tome and Principe (DRSTP) from November 2003 to March 2004 was determined by detection of serum anti-T. gondii antibodies. A short questionnaire interview for pregnant women was performed to investigate risk factors associated with T. gondii infection, including consumption of raw meat or unwashed vegetables, drinking unboiled water and keeping pets (cats and dogs). The overall seroprevalence of T. gondii infection was high (75.2%; 375/499). The older age group of > or =35 years had a significantly higher seroprevalence (85.7%; 54/63) than that of the younger age group of 15-25 years (70.4%; 178/253) (odds ratio 2.5, 95% CI 1.2-5.4; P=0.01). No significant difference in the seroprevalence of T. gondii infection was found between the pregnant women with and without exposure to the risk factors studied. However, among pregnant women with high antibody titers of > or =1:1024, it seemed likely that continual contact with pets and consumption of oocyst-contaminated water or raw unwashed vegetables rather than tissue cysts in meat was the primary route of infection. The incidence of congenital toxoplasmosis in unborn babies should be intensively monitored in the DRSTP.

Full text

Transactions of the Royal Society of Tropical Medicine and Hygiene (2007) 101, 134—139
available at www.sciencedirect.com
journal homepage: www.elsevierhealth.com/journals/trst
Serological screening and toxoplasmosis exposure
factors among pregnant women in the Democratic
Republic of Sao Tome and Principe
Chien-Ching Hunga, Chia-Kwung Fanb,∗, Kua-Eyre Suc, Fung-Chang Sung d,
Hung-Yi Chioue, Vilfrido Gilf, Maria da Conceicao dos Reis Ferreirag,
Jose Manuel de Carvalhoh, Claudina Cruzf, Yu-Kuan Linb, Lian-Fen Tsengi,
Ke-Yun Sao e, Wen-Cheun Changi, Hung-Shue Lanc, Shing-Hsien Choui
aDepartment of Internal Medicine, National Taiwan University Hospital and National Taiwan University College of Medicine,
Taipei, Taiwan
bDepartment of Parasitology, Taipei Medical University College of Medicine, Taipei, Taiwan
cDepartment of Parasitology, National Taiwan University College of Medicine, Taipei, Taiwan
dInstitute of Environmental Health, China Medical University, Taichung, Taiwan
eDepartment of Public Health, College of Public Health, Taipei Medical University, Taipei, Taiwan
fMinistry of Hygiene, Democratic Republic of Sao Tome and Principe
gCenter of Epidemiology, Democratic Republic of Sao Tome and Principe
hNational Center for Health Care of Women and Children, Democratic Republic of Sao Tome and Principe
iMedical Mission of Taiwan in the Democratic Republic of Sao Tome and Principe
Received 23 January 2006; received in revised form 12 April 2006; accepted 12 April 2006
Available online 17 November 2006
KEYWORDS
Toxoplasma gondii;
Protozoan antibodies;
Seroprevalence;
Latex agglutination
test;
Risk factors;
Sao Tome and
Principe
Summary The seroprevalence of Toxoplasma gondii infection among pregnant women in the
Democratic Republic of Sao Tome and Principe (DRSTP) from November 2003 to March 2004 was
determined by detection of serum anti-T. gondii antibodies. A short questionnaire interview
for pregnant women was performed to investigate risk factors associated with T. gondii infec-
tion, including consumption of raw meat or unwashed vegetables, drinking unboiled water and
keeping pets (cats and dogs). The overall seroprevalence of T. gondii infection was high (75.2%;
375/499). The older age group of ≥35 years had a significantly higher seroprevalence (85.7%;
54/63) than that of the younger age group of 15—25 years (70.4%; 178/253) (odds ratio 2.5,
95% CI 1.2—5.4; P= 0.01). No significant difference in the seroprevalence of T. gondii infection
was found between the pregnant women with and without exposure to the risk factors studied.
However, among pregnant women with high antibody titers of ≥1:1024, it seemed likely that
∗Corresponding author. Tel.: +886 2 27395092; fax: +886 2 27395092.
E-mail address: tedfan@tmu.edu.tw (C.-K. Fan).
0035-9203/$ — see front matter © 2006 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.trstmh.2006.04.012

Toxoplasma infection among pregnant women 135
continual contact with pets and consumption of oocyst-contaminated water or raw unwashed
vegetables rather than tissue cysts in meat was the primary route of infection. The incidence of
congenital toxoplasmosis in unborn babies should be intensively monitored in the DRSTP.
© 2006 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights
reserved.
1. Introduction
Toxoplasma gondii is a protozoan parasite that is endemic
worldwide and is a major opportunistic pathogen in immuno-
compromised hosts. Infection is mainly acquired by ingestion
of food, water or soil that is contaminated with oocysts
shed by cats, or by eating undercooked or raw meat con-
taining tissue cysts (Fayer et al., 2004). Primary infection
is usually subclinical, but in severely immunocompromised
patients it may be life-threatening, i.e. encephalitis, or the
greater threat of a latent infection is increasingly likely due
to reactivation as immune function decreases (Montoya and
Liesenfeld, 2004). Newly acquired T. gondii infection in a
pregnant woman can be transmitted to the fetus and may
cause cognitive impairment, blindness, epilepsy and death.
Although congenital toxoplasmosis may be asymptomatic at
birth, ocular problems may manifest later in life (Montoya
and Liesenfeld, 2004). For the diagnosis of T. gondii infec-
tion, detection of the organism itself is confirmative but
very difficult. Thus, most clinical laboratories use serologi-
cal tests to detect antibodies against T. gondii, such as the
latex agglutination (LA) test, ELISA and indirect fluorescent
antibody test. The LA test has been widely used to screen
for T. gondii infection because of its high specificity and high
sensitivity (Fan et al., 2001, 2002, 2003, 2006; Fleck, 1989;
Woldemichael et al., 1998).
In developed countries, congenital toxoplasmosis affects
between 1 and 10 in 10 000 newborn babies (Allain et al.,
1998; Gilbert and Peckham, 2001). In Brazil, the incidence
of congenital toxoplasmosis was estimated approximately to
be 1 in 4800 newborn babies (Neto et al., 2000). Effective
prevention of congenital toxoplasmosis depends on avoid-
ance of infection during pregnancy (Boyer et al., 2005).
Serological screening for T. gondii antibodies should there-
fore be done in pregnant women because absence of IgG
antibodies before or early in pregnancy allows identification
of women at risk of acquiring the infection (Montoya and
Liesenfeld, 2004). In Europe, the prevalence of Toxoplasma
infection among pregnant women ranges from 7.7 to 45.0%
(Allain et al., 1998; Jenum et al., 1998; Logar et al., 1995).
In Africa, few reports concerning the seroprevalence of T.
gondii infection in pregnant women in Western and Eastern
Africa countries are available, e.g. 78% (273/352) in Nigeria,
53.6% (113/211) in Benin (Onadeko et al., 1992; Rodier et
al., 1995); the status of T. gondii infection among pregnant
women in the Democratic Republic of Sao Tome and Principe
(DRSTP) is unknown to date.
Our previous study in the DRSTP indicated that the sero-
prevalence of T. gondii infection among pre-schoolchildren
aged under 5 years was fairly high (21.49%, 26/121), and
it seemed that consumption of oocysts shed from domestic
or stray cats, contaminated soil or water was a possible
route of infection for children (Fan et al., 2006). To
determine the risk factors for toxoplasmosis exposure, a
seroepidemiological survey of T. gondii infection among
pregnant women in Sao Tome Island of the DRSTP using
the LA test was conducted from November 2003 to March
2004. Additionally, a questionnaire interview to determine
personal details, including each study individual’s history
of exposure to risk factors associated with infection, was
included.
2. Materials and methods
2.1. Study population and subject selection
The DRSTP consists of the two islands of Sao Tome and
Principe and a number of smaller islets in the Gulf of Guinea.
Sao Tome lies approximately 180 miles from the coast of
Gabon and is crossed by the equator at its southern tip. The
climate is tropical with two rainy seasons. The total num-
ber of inhabitants of the DRSTP is estimated to be 160 000,
and the total number of inhabitants of Sao Tome Island is
approximately 150 000.
Pregnant women (mean age±SD: 25.4 ±6.4 years) who
visited the National Center for Health Care of Women and
Children on Sao Tome Island were invited to participate in
the present study after giving their oral informed consent.
Serum samples were obtained by venipuncture and were
kept at −20 ◦C at the Medical Mission of Taiwan in the
DRSTP until use.
2.2. Ethical approval
Ethical approval for the study was obtained from the Min-
istry of Hygiene of the Democratic Republic of Sao Tome and
Principe.
2.3. Serological detection of Toxoplasma gondii
infection by latex agglutination test
Sera obtained from pregnant women during their first
trimester (Gilbert and Peckham, 2001) were screened for
T. gondii antibodies using the Toxoplasma latex agglutina-
tion test (TOXO Test-MT, Eiken Co. Ltd, Tokyo, Japan) by
following the manufacturer’s instructions. Titers of ≥32 (i.e.
1:32 to 1:2048) were regarded as positive (Fan et al., 2001,
2006). Compared to the Sabin-Feldman test, the sensitiv-
ity and specificity of TOXO Test-MT were 96.3% and 97.1%,
respectively (Woldemichael et al., 1998).
2.4. Questionnaire interview on Toxoplasma
gondii infection
A short questionnaire interview for pregnant women was
carried out to obtain details of factors associated with T.
gondii infection, including age, residential district, history

136 C.-C. Hung et al.
of eating raw meat or unwashed vegetables, drinking
unboiled water and keeping pets including cats and/or dogs.
2.5. Statistical analysis
The subjects were categorized into three age groups (15—25
years; 25—35 years; ≥35 years). Statistical analysis was per-
formed using SAS software (SAS Institute Inc., Cary, NC,
USA). The increasing trends of age-specific seropositive
rates were tested for statistical significance using the ␹2
test for trends. Risk factor (RF) assessment between preg-
nant women with and without histories of exposure to eating
raw meat, unwashed vegetables, drinking unboiled water or
keeping pets was tested for statistical significance; if the
difference was insignificant, further RF assessment was per-
formed among seropositive pregnant women with high LA
titers to find the possible source of T. gondii infection. Crude
odds ratios with their 95% CIs were estimated by means of
multiple logistic regression analysis. The statistical signifi-
cance of differences in variables associated with seroposi-
tivity for T. gondii infection among comparison groups was
examined by testing the statistical significance of regression
coefficients. P-values <0.05 were considered to be signifi-
cant.
3. Results
Of the 499 serum samples studied, 375 (75.2%) were positive
for Toxoplasma antibodies and the seroprevalence increased
with age (Table 1). Interestingly, 61.3% (230/375) of the
pregnant women had high LA titers of ≥1:1024. The seroposi-
tivity for T. gondii infection in those women with and without
histories of eating raw meat or unwashed vegetables, drink-
ing unboiled water or keeping pets is shown in Table 1.
Further analysis of the questionnaire data revealed that,
of the 230 pregnant women with an LA titer of ≥1:1024,
1.0% (2/204) had a history of eating raw meat compared to
38.4% (76/198) for keeping pets, 72.6% (148/204) for eat-
ing unwashed vegetables and 89.4% (186/208) for drinking
unboiled water (Table 1).
Multiple logistic regression analysis revealed that women
aged 25—35 years and ≥35 years had a higher risk for T.
gondii infection when compared to those aged 15—25 years
(P= 0.07, P= 0.01, respectively) (Table 1). Those who had
histories of eating raw meat (P= 0.24) or unwashed vegeta-
bles (P= 0.21), drinking unboiled water (P= 0.91) or keeping
pets (P= 0.34) had higher Toxoplasma seroprevalence when
compared with those without such a history. However, 230
pregnant women with an LA titer of ≥1:1024 with a his-
tory of keeping pets, eating unwashed vegetables or drink-
ing unboiled water had a higher risk for T. gondii infection
when compared to those with a history of eating raw meat
(P< 0.001).
4. Discussion
The present study indicates that the overall seroprevalence
of T. gondii infection among pregnant women in DRSTP is
high (75.2%, 375/499), and is significantly higher than that
of pregnant women in Taiwan (10.2%, 183/1796; Yu, 1985)
and Korea (4.3%, 39/899; Ryu et al., 1996) in Asia, Nor-
way (10.9%, 3907/35 940; Jenum et al., 1998) and Slove-
nia (45.0%, 9430/20 953; Logar et al., 1995) in Europe, and
Benin (53.6%, 113/211; Rodier et al., 1995) in Eastern Africa,
whereas it is similar to that of pregnant women in Nigeria
(78.0%, 273/352; Onadeko et al., 1992) in Western Africa.
The discrepant seroprevalence between countries might be
explained by differences in socio-economic status and food
habits, e.g. Asian pregnant women consumed well-cooked
food and clean water (Ryu et al., 1996; Yu, 1985), while
consumption of inadequately cooked or cured meat was fre-
quently found among pregnant European women (Cook et
al., 2000). However, contact with an environment contam-
inated by cat feces was the primary source of infection for
pregnant Nigerian women (Onadeko et al., 1992).
High LA titers of anti-Toxoplasma antibodies might be
regarded as either acute infection (Kook et al., 1999; Mackie
et al., 1971) or reinfections (Onadeko et al., 1992). In
the present study, most of the seropositive women (61.3%,
230/375) had high Toxoplasma LA titers (≥1:1024). If these
women were to be infected with T. gondii during the first
trimester, it could be very harmful to the fetus because
after maternal acquisition of T. gondii for the first time dur-
ing gestation, the parasite will enter the fetal circulation by
infection of the placenta. This may result in severe congeni-
tal toxoplasmosis and can result in death of the fetus in utero
and spontaneous abortion (Montoya and Liesenfeld, 2004).
However, in this study it was regrettable that sera IgM or IgG
avidity were not examined and thus it was unclear whether
the seropositive cases with high LA titers had been infected
in the past 6 months.
Alternatively, reinfections may occur frequently due to
continual exposure to the risk factors; consumption of
uncooked foods, water or keeping pets including dogs and
cats was commonly found among DRSTP pregnant women
with high LA titers thus resulting in relatively high antibody
titers being maintained in this population. They might also
have been exposed to the risk factors since childhood. This
possibility is supported by the finding that T. gondii infection
was fairly prevalent in DRSTP pre-schoolchildren aged <5
years (Fan et al., 2006). Another explanation is that DRSTP
women on farms spend more time exposed to T. gondii, since
they carry out activities related to farming and thus have a
higher probability of coming into contact with oocysts.
On the other hand, among the study women, 24.8%
(124/499) did not present specific antibodies against T.
gondii, so this group of women was highly likely to be suscep-
tible to first infection during pregnancy and possible occur-
rence of congenital transmission due to dietary conditions
and contact with environments contaminated by oocysts.
Therefore, there was an urgent need for them to avoid
being infected by T. gondii to decrease risks of transplacen-
tal transmission during gestation (Montoya and Liesenfeld,
2004).
In the present study, although no significant difference
in seroprevalence of T. gondii infection was found between
the pregnant women with and without histories of expo-
sure to the risk factors considered, high seropositive rates
in both groups suggest that they were equally at risk
of being infected. Nevertheless, consumption of oocyst-
contaminated water, vegetables or soil rather than tissue
cysts in meats was the primary route of infection for the

Toxoplasma infection among pregnant women 137
Table 1 Seroprevalence, latex agglutination (LA) titer, and crude odds ratios (OR) with 95% CIs for various risk factors associated with seropositivity of Toxoplasma gondii
antibody among pregnant women in the Democratic Republic of Sao Tome and Principe
Variable No. tested No. positive (%) LA titer OR 95% CI P-value
1:32 1:64 1:128 1:256 1:512 1:1024 1:2048
Age group (years)
15—25 253 178 (70.4) 3 6 15 16 24 44 70 Ref. — —
25—35 183 143 (78.1) 2 5 8 15 23 35 55 1.5 1.0—2.3 0.07
≥35 63 54 (85.7) 3 4 5 10 6 6 20 2.5 1.2—5.4 0.01
Risk factors
Eating raw meat
No 436 327(75.0) —————— —Ref.— —
Yes 42 28(66.7) —————— —0.70.3—1.3 0.24
Eating unwashed vegetables
No 115 91(79.1) —————— —Ref.— —
Yes 367 269(73.3) —————— —0.70.4—1.2 0.21
Drinking unboiled water
No 71 53(74.7) —————— —Ref.— —
Yes 423 313(74.5) —————— —1.00.5—1.7 0.91
Keeping pets
No 271 205(75.7) —————— —Ref.— —
Yes 176 126(71.6) —————— —0.80.5—1.3 0.34
Risk factor assessment among pregnant women with LA titer of ≥1:1024
Eating raw meat 204 2 (1.0) 0 00001 1Ref.— —
Keeping pets 198 76 (38.4) 0 000024 5262.9 15.2—260.8 <0.001
Eating unwashed vegetables 204 148 (72.6) 0 000058 90266.9 64.1—1111.3 <0.001
Drinking unboiled water 208 186 (89.4) 0 000064122853.9 198.1—3681.3 <0.001
Total 499 375 (75.2) 8 15 28 41 53 85 145 — — —
Ref.: referent.

138 C.-C. Hung et al.
seropositive pregnant women. This assumption was sup-
ported by the fact that drinking unboiled water, eating
unwashed vegetables, or keeping pets had relatively higher
risks than eating undercooked meats in the acquisition of
T. gondii infection as revealed by analyzing questionnaire
data among pregnant women with high LA titers of ≥1:1024.
Meat consumption in the DRSTP people is infrequent due to
economic problems (Fan et al., 2006), and given the abun-
dance of cats (both domestic and stray) (Fan et al., 2006)
and the suitable climatic conditions for sporulation of Toxo-
plasma oocysts in tropical regions (Frenkel et al., 1975), it
seems likely that exposure to environments and foods con-
taminated by oocysts shed from cat’s feces is one of the
most important factors associated with Toxoplasma. This sit-
uation is similar to that in Nigeria where contact with cat
feces was the primary source of infection among pregnant
women (Onadeko et al., 1992).
The findings of increasing seropositivity rates of toxo-
plasmosis with age among pregnant women were similar to
those seen in studies conducted in various countries (Hill
and Dubey, 2002; Morris and Croxson, 2004; Petersson et
al., 2000). A possible explanation for this might be their
longer exposure to the risk factors related to T. gondii
infection.
In conclusion, our study demonstrates that Toxoplasma
infection is highly prevalent in pregnant women in the
DRSTP. Our findings suggest that improvements in hygiene
and sanitation are urgently needed to lower the risk of
Toxoplasma infection in the DRSTP, and further attention
should be paid to whether a high incidence of congen-
ital toxoplasmosis is present in newborn infants in the
DRSTP.
Conflicts of interest statement
The authors have no conflicts of interest concerning the work
reported in this paper.
Acknowledgements
The authors are grateful to the Ministries of Foreign Affairs
and Hygiene of the Democratic Republic of Sao Tome and
Principe. The authors also thank the Ministry of Foreign
Affairs and the Department of Health, Taiwan, for their sup-
port of this investigation.
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