Transactions of the Royal Society of Tropical Medicine and Hygiene (2009) 103, 162—166

available at www.sciencedirect.com

journal homepage: www.elsevierhealth.com/journals/trst

Toxoplasma gondii infection in pregnant

women in China
Quan Liu a,∗, Feng Wei b, Shengyan Gao a,b, Li Jiang a,b, Hai Lian a,
Bao Yuan a, Ziguo Yuan a, Zhiping Xia a, Bin Liu d,
Xianghong Xu c, Xing-Quan Zhu e,∗

a
Laboratory of Parasitology, Veterinary Institute, Academy of Military Medical Sciences, 1068 Qinglong Road,
Changchun 130062, China
b
College of Life Science, Jilin Agricultural University, Changchun 130118, China
c
Teaching Center of Basic Courses, Jilin University, Changchun 130062, China
d
The 208th Hospital of PLA, Changchun 130062, China
e
Department of Parasitology, College of Veterinary Medicine, South China Agricultural University, 483 Wushan Street,
Tianhe District, Guangzhou 510642, Guangdong Province, China

Received 27 June 2007; received in revised form 16 July 2008; accepted 16 July 2008
Available online 25 September 2008

KEYWORDS Summary Infection with Toxoplasma gondii is common and usually asymptomatic, but it can
have serious consequences in pregnant women if passed to the developing fetus. The aims
Toxoplasma gondii;
of this study were to determine the prevalence of toxoplasmosis in pregnant women and to
Pregnant women;
identify the possible risk factors associated with T. gondii infection in China. Of a sample of
Epidemiology;
235 pregnant women in Changchun, China, 25 (10.6%) were found by ELISA to be positive for
Prevalence;
IgG and none (0%) for IgM. Major risk factors were found by bivariate and multivariate analysis
Risk factors;
to include eating raw or undercooked meat, unwashed raw vegetables or fruit, contact with
China
cats, living in rural areas, and low educational standards. In order to lower congenital infection,
pregnant women need to be informed about the risk factors for toxoplasmosis.
© 2008 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights
reserved.

1. Introduction

Toxoplasma gondii, an obligate intracellular protozoan par-

∗ Corresponding authors. Tel.: +86 431 86985910;
fax: +86 431 86985910.
E-mail addresses: liuquan1973@hotmail.com (Q. Liu),
xingquanzh@scau.edu.cn (X.-Q. Zhu).
asite, is capable of infecting a variety of mammals. Humans
can be infected by consuming undercooked or raw meat
(e.g. pork, lamb) containing tachyzoites or bradyzoites,
or through food, water or unwashed vegetables contam-
inated with oocysts excreted by cats.1 Women infected

0035-9203/$ — see front matter © 2008 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.trstmh.2008.07.008
Toxoplasmosis in pregnant women in China 163

with T. gondii before pregnancy usually do not transmit
it to the fetus; however, if infection occurs during preg-
nancy, the pathogen will be transmitted transplacentally
to the fetus. Toxoplasmosis in fetuses and neonates may
present in various ways, from hydrocephalus, chorioretini-
tis and intracranial calcifications to hepatosplenomegaly,
thrombocytopenia, microcephaly, convulsions, fever and
small-for-gestational-age size at birth. Nevertheless, most
infected neonates are asymptomatic at birth. Risk of
congenital toxoplasmosis is somewhat lower if infection
occurs during the first trimester of pregnancy than in
the third, but the severity of congenital infection is
substantially higher, and primary infection acquired dur-
ing pregnancy may cause severe damage to the fetus.2
Therefore, toxoplasmosis is a major public health prob-
lem.
Prevalence of T. gondii infection in pregnant women
varies substantially among different countries. For exam-
ple, prevalences in pregnant women were from 38% to 71%
in some Europe countries.3,4 In Asian countries, a low preva-
lence of infection was found in Korean and Vietnamese
women (0.8% and 11.2%, respectively), but prevalences of
41.8% to 55.4% have been found in India, Malaysia and
Nepal.5 Toxoplasma gondii infects the Chinese population
with an average incidence of 7.9%, but with considerable
variation among the different regions.6 However, there is
limited epidemiological information on T. gondii infection
in pregnant Chinese women. We therefore performed this
study to determine the prevalence of infection and to iden-
tify associated risk factors.
2. Materials and methods
2.1. Subjects
Two hundred and thirty-five pregnant women, who attended
general hospitals for antenatal care for the first time or
second time in 2006 at the general hospitals in Changchun
(the capital and largest city of Jilin Province, located at
the northeast of China), gave verbal consent to be included
in the study. The pregnant women were 21—38 years old
(mean age 25.3 ± 5.6; Kolmogorov—Smirnov one sample
test, P = 0.56). The women were interviewed using a stan-
dard questionnaire including questions about their clinical
and behavioural characteristics. On the same day, blood

Table 1 Bivariate analysis of risk factors associated with Toxoplasma gondii infection in pregnant women

Risk factor No. tested (n = 235) Positive (%) Odds ratio (95% CI) P-valuea

Degree of meat cooking

Raw or undercooked 152 14.5 4.51 (1.27—15.49) 0.01
Well done 83 3.6
Unwashed raw vegetable or fruit consumption
Yes 27 22.2 2.8 (1.03—8.17) 0.038
No 208 9.1
Contact with catsb
Yes 184 13.0 7.5 (0.99—56.83) 0.023
No 51 2.0
Gardening or agriculture
Yes 124 10.4 1.72 (0.75—3.94) 0.935
No 111 10.8
Residence area
Rural 142 12.7 1.78 (0.71—4.44) 0.211
Urban 93 7.5
Number of pregnancies
1 159 8.8 0.57 (0.25—1.32) 0.069
>1 76 6.3
Housing conditions
Bad 99 14.1 1.87 (0.81—4.31) 0.137
Regular 136 8.08
Time of pregnancy (weeks)
<8 108 15.7 1.68 (0.51—5.57) 0.05
8—12 54 9.3 3.74 (1.13—12.41) 0.06
>12 63 4.8
Educational level
No education 45 28.6 4.67 (1.90—11.47) 0.001
Educated 190 7.9
a Fisher’s exact was used.
b Cat in home or neighborhood or cleaning cat feces.
164 Q. Liu et al.

samples were taken from the women under sterile condi-
tions, and the sera were separated and stored at −20 ◦ C
until further testing.
2.2. Serological technique
ELISA was used for determination of T. gondii IgG and IgM
antibodies. The ELISA kits were provided by Beijing Modern
Golden Biotechnology Co. Ltd, Beijing, China. The procedure
was performed according to the manufacturer’s instruc-
tions.
2.3. Statistical analysis
3. Results
3.1. Prevalence of Toxoplasma gondii infection in
pregnant women
Out of the 235 pregnant women studied, 25 were found to be
positive for T. gondii IgG antibodies and none were positive
for T. gondii IgM antibodies. Therefore, we found a 10.6%
prevalence of latent T. gondii infection and 0% prevalence
of acute T. gondii infection in our study.
3.2. Risk factors associated with Toxoplasma
gondii infection in pregnant women

All data were processed and analyzed by SPSS 13.0 Data
Editor (SPSS Inc., Chicago, IL, USA). Bivariate and mul-
tivariate analyses were used to assess the risk factors
associated with T. gondii infection. Variables were included
in the multivariate analysis if they had a P-value < 0.3 in
the bivariate analysis. Adjusted odds ratios (OR) and 95%
CIs were calculated by multivariate analysis using a multi-
ple, unconditional logistic regression model. The results in
comparisons between groups were considered different if
P < 0.05.
In the bivariate analysis, four variables were identified
as possible risk factors associated with T. gondii infection
(Table 1): (i) eating raw or undercooked meat (P = 0.01); (ii)
eating unwashed raw vegetable or fruit (P = 0.038); (iii) con-
tact with cats (P = 0.023); (iv) educational level (P < 0.001).
The other clinical and behavioural characteristics of the
women studied did not show any likely association with T.
gondii infection.
Logistic regression was used to investigate the associa-
tion of risk factors and T. gondii infection at the individual

Table 2 Multivariate analysis of risk factors associated with Toxoplasma gondii infection in pregnant women

Risk factora Adjusted odds ratiob 95% CI P-value

Degree of meat cooking

Raw or undercooked 5.69 1.14—16.23 0.008
Well done 1
Unwashed raw vegetable or fruit consumption
Yes 3.85 1.06—9.63 0.015
No 1
Contact with cats
Yes 8.23 0.85—57.63 0.001
No 1
Residence area
Rural 4.81 0.54—4.64 0.006
Urban 1
Number of pregnancies
1 1.63 0.23—2.41 0.238
>1 1
Housing conditions
Bad 1.46 0.42—4.98 0.546
Regular 1
Time of pregnancy (weeks)
<8 1.25 0.38—6.21 0.064
8—12 2.93 1.06—13.52 0.083
>12 1
Educational level
No education 4.93 1.02—12.65 0.044
Educated 1
a The variables included were those with a P-value <0.3 obtained in the bivariate analysis.
b Adjusted by number of pregnancies, gardening or agriculture, housing conditions, and the rest of characteristics included in this table.
Toxoplasmosis in pregnant women in China
level (Table 2). The analysis revealed that eating raw or
undercooked meat, eating unwashed raw vegetable or fruit,
contact with cats, living in rural areas and no education were
independently associated with the risk of T. gondii infection.
The other factors such as number of pregnancies, housing
conditions and time of pregnancy did not have an increased
risk for T. gondii infection.
4. Discussion
In recent years, rural residents and urban migrants have
gained access to the health care system due to the
improved socio-economic situation in China. Although this
study was performed in hospitals, and participants were
not selected from the general population, the samples in
our hospital-based study almost represented the general
population due to the common antenatal care in hospi-
tal.
The 10.6% prevalence of latent T. gondii infection in preg-
nant women of Changchun, China, is much lower than in
other countries which range from 20% to 74.5%,7 but this fig-
ure is consistent with the low overall prevalence of T. gondii
in China. A study performed in the seaside city of Dalian,
China, where people frequently eat raw or undercooked sea
food, showed that 23.66% of pregnant women were posi-
tive for T. gondii antibodies.8 Our figure, however, is higher
than those reported from elsewhere in China. For example,
a 5.42% prevalence in pregnant women was found in the
northwest of China,9 6.75% in Hubei10 and 4.5% in Jiangsu.11
The higher figure in the northeast might be explained by the
habit of eating raw vegetables there.
Our study highlights potential risk factors for T. gondii
infection in pregnant women in China. Consumption of
undercooked/raw meat, and contact with cats, are well-
established risk factors12 that contribute to T. gondii
infection even in healthy populations. In our study, the ORs
for T. gondii infection in pregnant women consuming raw or
undercooked meat, and having contact with cats, and those
consuming thoroughly cooked meat, with no cat contact,
were 5.69 (95% CI 1.14—16.23) and 8.23 (95% CI 0.85—57.63),
respectively. Our findings emphasize the need to avoid con-
suming undercooked/raw meat, and of detecting T. gondii
antibodies in cats.
Oocysts are often buried in soil with cat feces, and soil
contact is universal and difficult to avoid.13,14 This may
explain the higher frequency of infection in pregnant women
living in houses with soil floors, and consuming unwashed raw
vegetables/fruit. The ORs were 3.85 (95% CI 1.06—9.63) for
pregnant women consuming unwashed raw vegetables/fruit
and 4.81 (95% CI 0.54—4.64) for pregnant women living
in rural areas. Our findings suggest that soil contact is a
potential target for preventive strategies against toxoplas-
mosis.
The association between a low level of education and T.
gondii infection has been reported previously.15 We found
that pregnant women who had not attended school were at
higher risk of T. gondii infection than those who had (OR 4.93
[95% CI 1.02—12.65]). Health education has been proved a
cost-effective intervention. For example, even brief educa-
tion of pregnant women helps to improve some congenital
toxoplasmosis preventive behavior, and health education
165
was associated with a 63% reduction in T. gondii infection in
Belgium.16 In addition, researchers working in Poland found
that toxoplasmosis-related education of pregnant women
doubled their knowledge of the disease and resulted in sig-
nificant prevention within 4 years.17 It is therefore essential
that Chinese women entering their childbearing years be
taught to avoid undercooked meat, cat feces, and contam-
inated soil and food.
Authors’ contributions: QL designed the study; SG, LJ, HL,
ZY and BL carried out interviews and recruited participants;
FW, SG and ZY carried out laboratory assessments; QL, BY,
XX and ZX analyzed and interpreted the data; QL and FW
drafted the manuscript. All authors reviewed and approved
the final manuscript. QL and XQZ are guarantors of the
paper.
Acknowledgements: We thank the study participants. We
also thank Prof. J.B. Campbell (Department of Medical
Genetics and Microbiology, University of Toronto) and Dr
Hai Lan (Veterinary Institute, Academy of Military Medical
Sciences) for critically reviewing the paper.
Funding: Director Foundation of Veterinary Institute,
Academy of Military Medical Science in Changchun, China
(Approved No. 200504) and National Basic Research Program
of China (Approved No. 2007CB116301).
Conflicts of interest: None declared.
Ethical approval: Science and Ethics Committee, Veterinary
Institute, Academy of Military Medical Sciences, Changchun,
Jilin Province, China (Approved No. 2006021).
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