Clinical Microbiology and Infection xxx (xxxx) xxx

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Clinical Microbiology and Infection

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Systematic review

Global prevalence of latent toxoplasmosis in pregnant women: a

systematic review and meta-analysis
A. Rostami 1, 2, *, S.M. Riahi 3, H.R. Gamble 4, Y. Fakhri 5, M. Nourollahpour Shiadeh 6,
M. Danesh 6, H. Behniafar 7, S. Paktinat 8, M. Foroutan 9, A.H. Mokdad 10, P.J. Hotez 11,
R.B. Gasser 12
1)
Infectious Diseases and Tropical Medicine Research Centre, Health Research Institute, Babol University of Medical Sciences, Babol, Iran
2)
Immunoregulation Research Centre, Health Research Institute, Babol University of Medical Sciences, Babol, Iran
3)
Social Determinants of Health Research Centre, Department of Epidemiology and Biostatistics, Faculty of Health, Birjand University of Medical Sciences,
Birjand, Iran
4)
National Academy of Sciences, Washington, DC, USA
5)
Department of Environmental Health Engineering, Student Research Committee, School of Public Health, Shahid Beheshti University of Medical Sciences,
Tehran, Iran
6)
Sexual and Reproductive Health Research Centre, Mazandaran University of Medical Sciences, Sari, Iran
7)
Department of Basic Sciences, Medical Faculty of Sarab, Sarab, Iran
8)
Department of Biology and Anatomical Sciences, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
9)
Department of Parasitology, Abadan Faculty of Medical Sciences, Abadan, Iran
10)
Institute for Health Metrics and Evaluation, University of Washington, Seattle, WA, USA
11)
Texas Children's Hospital Center for Vaccine Development, Department of Pediatrics and Molecular Virology & Microbiology, National School of Tropical
Medicine, Baylor College of Medicine, Houston, TX, USA
12)
Department of Veterinary Biosciences, Melbourne Veterinary School, The University of Melbourne, Parkville, Victoria, Australia

a r t i c l e i n f o a b s t r a c t

Article history: Background: Toxoplasma gondii infection, if acquired as an acute infection during pregnancy, can have
Received 31 August 2019 substantial adverse effects on mothers, fetuses and newborns. Latent toxoplasmosis also causes a variety
Received in revised form of pathologies and has been linked to adverse effects on pregnancy.
11 December 2019
Objective: Here, we present results of a comprehensive systematic review and meta-analysis of the
Accepted 8 January 2020
Available online xxx
global prevalence of latent toxoplasmosis in pregnant women.
Data source: We searched PubMed, EMBASE, Web of Science, SciELO and Scopus databases for relevant
Editor: M. Leeflang studies that were published between 1 January 1988 and 20 July 2019.
Study eligibility criteria: All population-based, cross-sectional and longitudinal studies reporting the
Keywords: prevalence of latent toxoplasmosis in healthy pregnant women were considered for inclusion.
Global prevalence Participants: Pregnant women who were tested for prevalence of latent toxoplasmosis.
Latent toxoplasmosis Interventions: There were no interventions.
Meta-analysis Method: We used a random effects model to calculate pooled prevalence estimates with 95% confidence
Pregnant women
intervals (CIs). We grouped prevalence data according to the geographic regions defined by the World
Systematic review
Health Organization (WHO). Multiple subgroup and meta-regression analyses were performed.
Results: In total, 311 studies with 320 relevant data sets representing 1 148 677 pregnant women from 91
countries were eligible for inclusion in the meta-analysis. The global prevalence of latent toxoplasmosis in
pregnant women was estimated at 33.8% (95% CI, 31.8e35.9%; 345 870/1 148 677). South America had the
highest pooled prevalence (56.2%; 50.5e62.8%) of latent toxoplasmosis in pregnant women, whereas the
Western Pacific region had the lowest prevalence (11.8%; 8.1e16.0%). A significantly higher prevalence of latent
toxoplasmosis was associated with countries with low income and low human development indices (p < 0.001).
Conclusion: Our results indicate a high level of latent toxoplasmosis in pregnant women, especially in
some low- and middle-income countries of Africa and South America, although the local prevalence
varied markedly. These results suggest a need for improved prevention and control efforts to reduce the
health risks to women and newborns. A. Rostami, Clin Microbiol Infect 2020;▪:1
© 2020 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All
rights reserved.

* Corresponding author. A. Rostami, Infectious Diseases and Tropical Medicine Research Centre, Health Research Institute, Babol University of Medical Sciences, Babol. Iran.
E-mail addresses: alirostami1984@gmail.com, a.rostami@mubabol.ac.ir (A. Rostami).

https://doi.org/10.1016/j.cmi.2020.01.008
1198-743X/© 2020 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All rights reserved.

Please cite this article as: Rostami A et al., Global prevalence of latent toxoplasmosis in pregnant women: a systematic review and meta-analysis,
Clinical Microbiology and Infection, https://doi.org/10.1016/j.cmi.2020.01.008
2 A. Rostami et al. / Clinical Microbiology and Infection xxx (xxxx) xxx
Introduction
Toxoplasmosis, caused by Toxoplasma gondii, an obligate
intracellular protozoan parasite, is one of the most important
infectious diseases during pregnancy. Congenital toxoplas-
mosis, resulting from acute infection in pregnant women, is
responsible for a disease burden of 1.2 million disability-
adjusted life years (DALYS) annually, although it is often
overlooked in obstetrics and gynaecology clinics [1,2]. A recent
global meta-analysis using strict criteria (diagnosis based on
seroconversion and low IgG avidity) showed that the
overall prevalence of acute Toxoplasma infection in pregnant
women is estimated at 0.6% (95% CI 0.4e0.7%) and indicated
that annually ~201 600 children are born with congenital
toxoplasmosis [3].
Congenital infection can result in abortion/stillbirth, hydro-
cephaly/microcephaly and ocular/neurological complications in
childhood or early adulthood [4,5]. Although the majority of
congenital infections occur when pregnant women are infected
during pregnancy, it can also occur via reactivation of a previously
acquired T. gondii infection, classified as latent [6,7]. Unless the
immune system is suppressed, a specific antibody against T. gondii
from a previously acquired infection prevents re-activation of a
latent infection [2,8]. Thus, knowledge of the prevalence of latent
infection in pregnant women can contribute to a better under-
standing of the risk to, and the overall exposure rate of, pregnant
women.
A growing body of literature indicates that latent Toxoplasma
infection is responsible for many neuropathological effects [9].
Studies have indicated that latent toxoplasmosis can result in
psychiatric disorders (anxiety, schizophrenia spectrum disorders,
depression, self-directed violence and/or suicidal behaviour), pre-
eclampsia, decreased weight, autoimmune thyroid diseases, and
secondary infertility [10e18]. In pregnant women, latent toxo-
plasmosis has been associated with slower fetal development,
longer pregnancies and slower development of postnatal motor
skills [19].
T. gondii infection is diagnosed primarily using serological
techniques, and, in recent years, several laboratory methods
have been developed to differentiate between acute and latent
toxoplasmosis. While there has been a large number of
seroepidemiological studies [20e25], there are knowledge gaps
regarding the prevalence of latent toxoplasmosis in many
countries, and its overall global status is unknown. Considering
the potential long-term complications and the public health
importance of latent toxoplasmosis, a comprehensive under-
standing of the global prevalence of latent toxoplasmosis
in pregnant women could help shape health policies for in-
ternational bodies, such as the World Health Organization
(WHO), and in individual countries. To address this need, we
designed a systematic review and meta-analysis to assess the
worldwide prevalence of latent toxoplasmosis in pregnant
women.
Methods
Search strategy and selection criteria
We used the methodology recommended by the Preferred
Reporting Items for Systematic Reviews and Meta-Analyses
(PRISMA) guidelines [26], and systematically searched five in-
ternational electronic databases (PubMed, EMBASE, Web of
Science, SciELO and Scopus) for relevant, peer-reviewed arti-
cles published between 1 January 1988 and 20 July 2019,
Please cite this article as: Rostami A et al., Global prevalence of latent toxoplasmosis in pregnant women: a systematic review and meta-analysis,
Clinical Microbiology and Infection, https://doi.org/10.1016/j.cmi.2020.01.008
without geographic and language limitations. A seropositivity
(IgG positive) rate for latent toxoplasmosis in pregnant women
was considered as the main outcome of interest. We began by
systematically searching the databases with medical subject
headings (MeSH) terms such as ‘Toxoplasma’, ‘toxoplasmosis’,
‘seroepidemiology’, ‘seroprevalence’, ‘pregnancy’ and ‘pregnant
women’ alone or combined together with the Boolean opera-
tors ‘OR’ and/or ‘AND’ (Fig. S1). For some countries (e.g., the
USA and Canada) that lacked adequate data, we also searched
databases for articles published before 1988. Following the
initial search, relevant citations were recorded based on titles
and/or abstracts, and abstracts were saved in a separate word
file for further evaluation. After excluding duplicate records,
articles potentially eligible for inclusion were downloaded
through online resources. The full texts of articles were inde-
pendently reviewed by four trained investigators (M.F., H.B.,
S.P. and A.R.) to assess final eligibility. The articles selected
were scrutinized carefully, and contradictions were obviated
through discussion, achieving a consensus. The full-text articles
selected were also examined to identify additional articles not
detected via the web search. A protocol for inclusion of eligible
peer-reviewed publications was defined by the research team.
All population-based, cross-sectional and longitudinal studies
published in peer-reviewed journals and reporting the preva-
lence of latent toxoplasmosis in healthy pregnant women were
considered for inclusion. We excluded studies if they clearly
were not representative of healthy pregnant women (e.g.,
HIV þ patients, psychiatric women, women with a history of
challenging or high-risk pregnancies and/or other complica-
tions); were not associated with a full-text article or report;
were performed in non-pregnant women at child bearing age;
were caseecontrol studies; did not include serological data;
were comparative studies of diagnostic methods; had a sample
size of <100; or were reviews, systematic reviews or meta-
analyses. Moreover, we excluded articles if their data sets
overlapped with those of other articles included. These strict
inclusion/exclusion criteria were employed in this systematic
review and meta-analysis, and all papers included had to fulfil
the inclusion criteria.
Data extraction and quality assessment
Data extraction was performed by four investigators in
duplicate (M.F., H.B., M.D. and M.N.S.). Two authors (M.F. and
H.B.) extracted the required data, and the others (M.D. and
M.N.S.) independently verified these data. Any conflict of
opinion was resolved by the lead investigator (A.R.). Following
the review of full texts of articles, a specific form (designed by
A.R. and M.F.) in Microsoft Excel (version 2016; Microsoft
Corporation, Redmond, WA) was used to extract from each
paper all relevant data and information, including study char-
acteristics (the first author's last name, year of publication,
country, city, the WHO region [27], income level [28] and
human development index (HDI) [29] of the area or region
studied as well as the type of serological methods used) and
participant characteristics (the number of participants, and the
details of serological test results (IgG serum antibodies)). If
multiple diagnostic methods were used in a study, we
extracted and appraised the results for the method that
showed the highest seroprevalence. Moreover, we extracted
data based on sample size for distinct age groups (if available).
Since some studies categorized participants into groups of <20,
20e30 or >30 years of age and others into groups of
<25, 26e35, >36 years of age, we extracted data for both of
 A. Rostami et al. / Clinical Microbiology and Infection xxx (xxxx) xxx
these age groupings and performed two subgroup analyses. A
quality assessment of the studies included was performed
using the JBI (Joanna Briggs Institute) Prevalence Critical
Appraisal Tool [30]. Each individual study (article) was ranked
according to ten criteria (collection of a representative sample,
appropriate method for recruitment of participants, sample
size, setting description, subject description, outcome mea-
surement, reliable measurements, data analysis, subpopulation
analysis and adjustment for confounders). For each study, the
total number of ‘yes’ answers was counted; the high number
of ‘yes’ answers suggested a low risk of bias in the present
study.
Meta-analysis
To estimate the pooled prevalence of latent toxoplasmosis
in pregnant women, we used a DerSimonianeLaird random-
effects model. We estimated the pooled prevalence at a 95%
confidence interval (CI) for each study that was eligible for
inclusion. For this purpose, we used a metaprop command in
Stata software. Prevalence rates from raw cell counts were
pooled using a FreemaneTukey double arcsine transformation,
and CIs for individual studies were calculated. We stratified the
studies by geographical region as defined by WHO, and the
pooled prevalence was estimated for each of the seven regions.
Heterogeneity was calculated using an I2 index to estimate the
percentage of variation across the included studies; I2 values of
<25%, 25e50% and >50% were defined as low, moderate and
high heterogeneities, respectively [31]. To address the sources
of heterogeneity, meta-regression and subgroup analyses were
performed using the following variables: (1) WHO region; (2)
publication year; (3) sample size and (4) income level and HDI
of countries. All analyses were carried out with Stata statistical
Fig. 1. Flow diagram showing the search and selection methodology used, which follows PRISMA guidelines.
Please cite this article as: Rostami A et al., Global prevalence of latent toxoplasmosis in pregnant women: a systematic review and meta-analysis,
Clinical Microbiology and Infection, https://doi.org/10.1016/j.cmi.2020.01.008
3
software (v.13 Stata Corp., College Station, TX, USA); for all
statistical tests, the significance level was considered to
be < 0.05.
Results
From 15 946 studies retrieved using our search terms, we
identified 311 studies containing 320 relevant data sets eligible
for data extraction and meta-analysis (Fig. 1). These studies
were from 91 countries, representing all seven WHO regions;
30 countries were from Europe (727 757 pregnant women), 18
from Africa (18 836 pregnant women), 15 from the Eastern
Mediterranean region (89 382 pregnant women), seven from
North America (143 839 pregnant women), four from South
America (92 760 pregnant women), nine from the Western
Pacific region (63 496 pregnant women) and eight from South-
East Asia (12 607 pregnant women). Countries with the most
studies were Iran (n ¼ 28), Brazil (27), Turkey (18), China (17),
Saudi Arabia (14) and India (12). The majority of selected
studies used a cross-sectional design and employed the
enzyme-linked immunosorbent assay (ELISA) to measure levels
of anti-T. gondii IgG serum antibodies. Other studies used the
immunofluorescence assay (IFA), the modified agglutination
test (MAT), the chemiluminescent microparticle immunological
assay (CMIA), the microparticle enzyme immunoassay (MEIA),
the enzyme-linked fluorescent assay technique (ELFA), the la-
tex agglutination test (LAT) or the SabineFeldman Dye test
(SFT) for the detection of anti-Toxoplasma serum antibody
(IgG). With respect to risk of bias, 259 and 52 studies had low
and moderate risks of bias, respectively. No study had a high
risk of bias. The references, main study characteristics and
seropositivity rates for pregnant women reported in these 311
studies are given in Table S1.
4 A. Rostami et al. / Clinical Microbiology and Infection xxx (xxxx) xxx

Table 1
Global, regional and national pooled prevalence of latent toxoplasmosis among pregnant women (results from 306 studies performed in 91 countries)

WHO regions/country Number Number Number Pooled prevalence (95% CI) Weight (%) Heterogeneity
datasets of pregnant of pregnant
I2 (%)
(305 studies) women women with
screened latent
(total) toxoplasmosis
(IgG seropositive)

Global 320 1 148 677 345 870 33.8 (31.8e35.9) 100 99.8
South Americas 37 92 760 49 749 56.2 (50.5e62.8) 11.6 99.8
Brazil 27 62 244 38 436 61.2 (58.2e64.1) 8.6 97.8
Colombia 6 3996 2121 50.6 (43.3-57.9) 1.89 95.4
Venezuela 2 853 306 35.8 (32.6e39.0) 0.6 99.9
Argentina 2 25 667 8886 33.7 (33.1e34.3) 0.6 99.6
African region 43 18 836 9402 48.7 (41.5e55.9) 13.5 99.0
Ethiopia 10 2956 1757 65.0 (45.5e82.2) 3.1 99.2
Nigeria 5 1592 568 36.3 (30.7e42.1) 1.6 82.5
Ghana 3 452 334 74.3 (48.2e93.5) 0.9 97.1
Burkina Faso 3 834 220 25.7 (20.2e31.6) 0.9 71.9
Senegal 3 1749 640 34.4 (25.6e43.9) 0.9 90.8
Tanzania 3 1453 506 35.0 (30.6e39.5) 0.9 64.1
Benin 2 494 198 39.8 (35.5e44.2) 0.6 98.9
Gabon 2 1813 1027 56.7 (54.4e59.0) 0.6 99.9
Algeria 2 1171 522 44.4 (41.5e47.2) 0.6 98.9
Cameroon 2 302 225 74.6 (69.5e79.4) 0.6 86.0
Rwanda 1 384 37 9.6 (6.9e13.0) 0.3 NA
Zambia 1 411 24 5.8 (3.8e8.6) 0.3 NA
Angola 1 300 76 25.3 (20.5e30.7) 0.3 NA
Congo 1 781 627 80.3 (77.3e83.0) 0.3 NA
Mozambique 1 150 28 18.7 (12.8e25.8) 0.3 NA
Sao Tome and Principe 1 499 375 75.2 (71.1e78.9) 0.3 NA
Madagascar 1 599 500 83.5 (80.3e86.4) 0.3 NA
Republic of the Congo 1 2897 1738 60.0 (58.2e61.8) 0.3 NA
Eastern Mediterranean 77 89 382 33 313 35.1 (31.5e35.6) 24.2 99.1
Iran 28 12 724 3939 32.2 (25.7e39.0) 8.8 98.5
Saudi Arabia 14 12 389 2799 29.6 (20.5e39.6) 4.4 99.1
Egypt 8 1760 827 45.9 (33.6e58.5) 2.5 96.3
Yemen 4 1794 690 37.2 (25.3e49.9) 1.3 96.7
Pakistan 4 1825 404 22.8 (10.3e38.5) 1.3 98.1
Morocco 4 7193 3216 45.8 (39.4e52.1) 0.3 95.8
Sudan 3 838 269 30.5 (21.7e40.0) 0.9 86.5
Tunisia 3 44 987 18 017 44.1 (38.2e50.1) 1.0 97.8
Iraq 2 475 153 32.2 (28.0e36.5) 0.6 99.4
Libya 2 730 317 43.4 (39.8e47.0) 0.6 99.5
Lebanon 1 2456 2029 82.6 (81.1e84.1) 0.3 NA
Palestine 1 204 57 27.9 (21.9e34.6) 0.3 NA
Kuwait 1 224 119 53.1 (46.4e59.8) 0.3 NA
Jordan 1 280 133 47.5 (41.5e53.5) 0.3 NA
United Arab Emirates 1 1503 344 22.9 (20.8e25.1) 0.3 NA
European region 84 727 757 217 150 31.2 (28.4e34.0) 26.8 99.8
Turkey 18 136 011 38 463 35.8 (30.3e41.6) 5.7 99.7
Italy 8 36 308 10 613 29.7 (22.9e36.9) 2.6 99.5
Spain 8 39 406 10 103 23.6 (19.8e27.6) 2.5 98.6
Poland 6 19 253 8066 45.2 (41.0e49.5) 1.9 96.8
United Kingdom 5 26 205 3118 12.3 (7.6e17.9) 1.6 99.3
France 4 58 861 26 120 44.6 (37.7e51.7) 1.3 99.7
Austria 3 167 032 52 734 31.6 (31.3e31.8) 1.0 0.0
Sweden 3 47 728 8486 16.8 (14.9e18.8) 1.0 92.2
Romania 3 1335 566 41.1 (34.8e47.5) 0.9 80.0
Norway 2 37 862 4086 10.8 (10.5e11.1) 0.6 99.9
Slovenia 2 42 223 16 581 39.2 (38.7e39.7) 0.6 90.0
Croatia 2 1060 305 28.7 (26.1e31.5) 0.6 1.9
Russia 2 10 189 1984 19.4 (18.7e20.2) 0.6 90.0
Belgium 2 7333 3924 53.5 (52.4e54.7) 0.6 1.9
Portugal 1 155 34 21.9 (15.7e29.3) 0.3 NA
Germany 1 5402 1856 34.4 (33.1e35.6) 0.3 NA
Cyprus 1 23 076 4129 17.9 (17.4e18.4) 0.3 NA
Kosovo 1 334 97 29.0 (24.2e34.2) 0.3 NA
Macedonia 1 235 48 20.4 (15.5e26.2) 0.3 NA
Albania 1 496 241 48.6 (44.1e53.1) 0.3 NA
Greece 1 5532 1628 29.4 (28.2e30.6) 0.3 NA
Netherlands 1 500 154 30.8 (26.8e35.1) 0.3 NA
Czech Republic 1 3392 1187 35.0 (33.4e36.6) 0.3 NA
Hungary 1 17 735 11 490 64.8 (64.1e65.5) 0.3 NA
Denmark 1 5402 1478 27.4 (26.2e28.6) 0.3 NA
Switzerland 1 9059 4172 46.1 (45.0e47.1) 0.3 NA
Finland 1 16 733 1378 19.0 (18.4e19.6) 0.3 NA

Please cite this article as: Rostami A et al., Global prevalence of latent toxoplasmosis in pregnant women: a systematic review and meta-analysis,
Clinical Microbiology and Infection, https://doi.org/10.1016/j.cmi.2020.01.008
 A. Rostami et al. / Clinical Microbiology and Infection xxx (xxxx) xxx 5

Table 1 (continued )

WHO regions/country Number Number Number Pooled prevalence (95% CI) Weight (%) Heterogeneity
datasets of pregnant of pregnant
I2 (%)
(305 studies) women women with
screened latent
(total) toxoplasmosis
(IgG seropositive)

Israel 1 213 45 21.1 (15.8e27.2) 0.3 NA

Scotland 1 5909 998 16.9 (15.9e17.9) 0.3 NA
Serbia 1 2778 1266 45.6 (43.7e47.4) 0.3 NA
North America 15 143 839 24 933 28.2 (16.6e41.5) 4.8 99.5
USA 5 133 476 19 094 18.9 (6.4e36.0) 1.6 99.9
Mexico 3 1120 78 6.9 (5.5e8.5) 0.9 0.0
Canada 2 1925 938 48.6 (46.3e50.8) 0.6 99.9
Cuba 2 5897 4186 71.0 (69.8e72.2) 0.6 99.9
Grenada 1 534 304 56.9 (52.6e61.2) 0.3 NA
Caribbean islands 1 437 174 39.8 (35.2e44.6) 0.3 NA
Trinidad and Tobago 1 450 159 35.3 (30.9e39.9) 0.3 NA
South-East Asian Region 30 12 607 3123 23.4 (18.7e28.4) 9.3 97.6
India 12 4614 1473 26.5 (19.1e34.7) 3.7 97.1
Thailand 9 5101 852 17.3 (11.7e23.7) 2.8 96.8
Bangladesh 3 1053 288 27.8 (18.3e38.4) 0.9 91.3
Sri Lanka 2 829 196 23.0 (20.2e26.0) 0.6 99.7
Myanmar 1 215 66 30.7 (24.6e37.3) 0.3 NA
Singapore 1 120 21 17.5 (11.2e25.5) 0.3 NA
Nepal 1 345 191 55.4 (49.9e60.7) 0.3 NA
Indonesia 1 330 36 10.9 (7.8e14.8) 0.3 NA
Western Pacific Region 34 63 496 8200 11.8 (8.1e16.0) 10.8 99.6
China 17 38 565 3368 9.4 (6.4e12.9) 5.4 99.1
Taiwan 4 1233 204 13.3 (4.3e26.0) 1.2 96.7
South-Korea 3 6425 94 2.7 (0.5e6.6) 1.0 96.5
Vietnam 3 1095 74 6.8 (3.7e10.8) 0.9 82.0
Malaysia 2 500 187 37.3 (33.1e41.6) 0.6 99.9
Australia 2 10 515 3616 34.3 (33.4e35.3) 0.6 99.9
Japan 1 4466 459 10.3 (9.4e11.2) 0.3 NA
New Zealand 1 500 163 32.6 (28.5e36.9) 0.3 NA
Papua New Guinea 1 197 35 17.8 (12.7e23.8) 0.3 NA

WHO regions are sorted according to prevalence rates. Countries are sorted according to number of studies included. NA, not applicable.

We estimated the prevalence of latent toxoplasmosis in
pregnant women from 91 countries by random-effects meta-
analysis. The worldwide prevalence of latent toxoplasmosis in
healthy pregnant women (1 148 677 participants) reported in the
311 studies was estimated to be 33.8% (95% CI, 31.8e35.9%;
345 870/1 148 677); the heterogeneity among studies was sub-
stantial (I2 ¼ 99.8%, p < 0.001; Table 1). The highest prevalence
rates of latent toxoplasmosis in pregnant women in WHO regions
were 56.2% (50.5e62.8%) in South America and 48.7%
(41.5e55.9%) in Africa; the lowest prevalence rate, 11.8%
(8.1e16.0%), was found in the Western Pacific region. The pooled
prevalence rates for latent toxoplasmosis in pregnant women in
other WHO regions were 35.1% (31.5e35.6%) in the Eastern
Mediterranean region, 31.2% (28.4e34.0%) in Europe, 28.2%
(16.6e41.5%) in North America and 23.4% (18.7e28.4%) in South-
East Asia. The heterogeneity assessment results and the preva-
lence rates for individual countries are given in Fig. 2 and Table 1.
Fig. 3 shows a geographic information system (GIS) map sum-
marizing the prevalence of latent toxoplasmosis in pregnant
women for individual countries.
In subgroup analyses, by income level and HDI, we observed
substantial differences in prevalence rates among countries. The
pooled prevalence rates of latent toxoplasmosis in pregnant
women in countries with low, lower-middle, upper-middle and
high levels of income were 50.6% (40.5e60.6%), 33.3% (29.9e36.7%),
35.8% (31.9e39.7%) and 27.2% (24.2e30.4%), respectively. The
pooled prevalence rates of latent toxoplasmosis in pregnant
women in countries with low, moderate, high and very high levels
of HDI were 42.4% (35.0e49.9%), 35.0% (29.3e40.9%), 35.3%
(31.7e39.0%) and 27.8% (24.9e30.8%), respectively. An analysis over
six time periods (<1995, 1995e2000, 2001e2005, 2006e2010,
2011e2015 and 2016e2019) showed that latent toxoplasmosis
prevalence was slightly higher after 2005 than other periods
(Table 2).
We estimated the pooled prevalence rates of latent toxoplas-
mosis for pregnant women in different age groups. Depending on
the study, pregnant women were grouped into three age groups in
two distinct ways: <20, 20e30 or >30 years of age; or <25, 26e35,
>36 years of age. Hence, we estimated the prevalence rates for
these distinct age groupings. The pooled prevalence rates of latent
toxoplasmosis in pregnant women of <20, 20e30 and > 30 years of
age were 29.0% (24.0e34.3%), 35.7% (30.0e41.5%) and 41.4%
(35.0e47.9%), respectively. The pooled prevalence rates of latent
toxoplasmosis among pregnant women of <25, 26e35, and
>36 years of age were 30.9% (23.3e39.1%), 35.7% (26.8e45.0%) and
43.0% (33.7e52.6%), respectively. Based on subgroup analysis by
risk of bias, prevalence rates were 31.8e36.3% (mean: 34.0%) in
studies containing seven to ten items with ‘yes’ answers and
29.4e36.4% (mean: 32.8%) in studies containing four to six items
with ‘yes’ answers (Table 2).
We also investigated temporal and sociodemographic effects on
prevalence of latent toxoplasmosis. Meta-regression indicated a
non-significant increase in prevalence over time (coefficient
(C) ¼ 0.0009; p 0.49). There was a non-statistically significant
decreasing trend in prevalence of latent toxoplasmosis with
increasing sample size (C ¼ e008; p 0.26). With respect to socio-
demographic parameters, we identified a significant decreasing
trend in prevalence in countries with increasing per capita income
(C ¼ e2.85e-06; p < 0.0001) and HDI levels (C ¼ e0.0036;
p < 0.0001) (Fig. 4).

Please cite this article as: Rostami A et al., Global prevalence of latent toxoplasmosis in pregnant women: a systematic review and meta-analysis,
Clinical Microbiology and Infection, https://doi.org/10.1016/j.cmi.2020.01.008
6 A. Rostami et al. / Clinical Microbiology and Infection xxx (xxxx) xxx

Fig. 2. Forest plot of the prevalence of latent toxoplasmosis in pregnant women by WHO region and globally. ES, estimated prevalence of latent toxoplasmosis for WHO regions and
individual countries.

Please cite this article as: Rostami A et al., Global prevalence of latent toxoplasmosis in pregnant women: a systematic review and meta-analysis,
Clinical Microbiology and Infection, https://doi.org/10.1016/j.cmi.2020.01.008
 A. Rostami et al. / Clinical Microbiology and Infection xxx (xxxx) xxx 7

Fig. 3. Prevalence of latent toxoplasmosis in pregnant women in different countries using geographic information system (GIS).

Table 2
Prevalence of Latent Toxoplasma infection in pregnant women according to a priori defined subgroups

Variable/subgroups Number Number Number Pooled prevalence (95% CI) Heterogeneity

studies of pregnant of pregnant
I2 (%)
women screened women with
(total) latent
toxoplasmosis
(IgG seropositive)

Income
Low 26 11 501 6201 50.6 (40.5e60.6) 99.1
Lower middle 62 68 165 25 834 33.3 (29.9e36.7) 98.3
Upper middle 136 291 312 102 103 35.8 (31.9e39.7) 99.8
High 96 777 699 211 732 27.2 (24.2e30.4) 99.8
HDI
Low 40 17 129 7837 42.4 (35.0e49.9) 99.0
Medium 45 19 148 7056 35.0 (29.3-40.9) 98.6
High 137 248 621 99 726 35.3 (31.7e39.0) 99.8
Very high 98 863 779 231 251 27.8 (24.9e30.8) 99.9
Year
<1995 18 178 750 34 034 32.8 (23.6e42.7) 99.9
1995e2000 37 150 570 48 541 32.3 (24.8e40.0) 99.9
2001e2005 29 116 376 30 466 31.2 (25.6e37.2) 99.7
2005e2010 61 168 714 73 011 38.3 (33.5e43.2) 99.7
2011e2015 95 278 126 77 858 34.9 (31.3e38.5) 99.7
2016e2019 80 286 141 81 960 31.2 (28.4e33.9) 99.5
Sample size
<500 163 46 233 16 336 34.3 (31.1e37.5) 98.2
500e1000 48 34 734 14 088 39.7 (33.5e46.5) 99.3
1000e2000 28 40 998 12 352 28.2 (20.6e36.5) 99.7
2000e4000 27 76 396 26 954 36.0 (27.7e44.7) 99.8
>4000 54 950 316 276 140 29.3 (24.9e33.8) 99.9
Risk of bias (total number of item with ‘yes’ answers per study)
7e10 268 1 088 267 322 404 34.0 (31.8e36.3) 99.8
4e6 52 60 410 23 466 32.8 (29.4e36.4) 99.7
Method
ELISA 230 670 612 201 919 32.0 (29.8e34.3) 99.7
IFAT 17 49 413 20 058 46.0 (40.7e51.4) 99.0
LAT 11 9438 2497 50.2 (29.9e70.5) 99.7
ELFA 11 26 111 9942 53.5 (41.1e65.7) 99.7
MEIA 10 41 196 16 143 40.6 (20.7e62.2) 99.9
IHA 9 104 175 9545 22.4 (13.8e32.3) 99.5
CMIA 8 10 015 4036 38.1 (30.6e46.0) 99.3
DAT 4 14 658 4231 13.9 (4.5e27.5) 99.6
MAT 3 892 248 29.0 (18.5e40.7) 99.2
IIFT 3 168 858 54 227 45.7 (37.8e53.8) 99.9
Other (CLIA, CFT, VIDAS, 14 53 309 22 988 27.8 (16.0e41.4) 99.9
SFT, ISAGA, LFIA, IFFT,
LFIA, ECLIA, DT
(continued on next page)

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8 A. Rostami et al. / Clinical Microbiology and Infection xxx (xxxx) xxx

Table 2 (continued )

Variable/subgroups Number Number Number Pooled prevalence (95% CI) Heterogeneity

studies of pregnant of pregnant
I2 (%)
women screened women with
(total) latent
toxoplasmosis
(IgG seropositive)

Age 1
<25 33 6663 2300 30.9 (23.3e39.1) 97.9
26e35 33 11 803 4665 35.7 (26.8e45.0) 99.0
>36 28 3134 1243 43.0 (33.7e52.6) 96.0
Age 2
<20 52 6798 1872 29.0 (24.0e34.3) 94.4
20e30 56 44 502 10 317 35.7 (30.0e41.5) 99.2
>30 56 24 708 6203 41.4 (35.0e47.9) 98.6

Abbreviations: CFT, complement fixation test; CLIA, chemiluminescent immunoassay; DT, dye test; ELISA, enzyme-linked immunosorbent assay; ECLIA, electro-
chemiluminescence immunoassay; IIFT, Indirect Immunofluorescence Test; IFA, immunofluorescence assay; IHA, indirect haemagglutination assay; ISAGA, immunosorbent
agglutination assay; MAT, modified agglutination test; EIAs, enzyme immunoassays; IAT, immunosorbent agglutination test; CMIA, chemiluminescent microparticle
immunological assay; ELFA, enzyme-linked fluorescent assay technique; LAT, latex agglutination test; SFT, Sabin-Feldman test; MEIA, microparticle enzyme immunoassay;
LFIA, Lateral flow immunoassay assay; DAT, direct agglutination test.

Fig. 4. Ecological linear meta-regression analyses of the prevalence of latent Toxoplasma infection in pregnant women according to (A) time period (1988e2019), showing a non-
statistically significant upward trend in prevalence in more recent years; (B) sample size, showing a non-statistically significant downward trend in prevalence with increasing
sample size; (C) a country's income level, showing a statistically significant downward trend in prevalence in countries with higher income levels; (D) human development index
(HDI), showing a statistically significant downward trend in prevalence in countries with higher HDIs.

Discussion studies published after 2010. Therefore, we believe that the

The results of this meta-analysis confirm that, worldwide, and
during the time period of this study, approximately one-third
(33.6%) of pregnant women were seropositive for latent toxo-
plasmosis. More than 74% of data sets analysed here were from
prevalence rate reported here is representative of actual preva-
lence worldwide. We showed variation by region and other factors
associated with the prevalence of latent toxoplasmosis. Examining
the root causes of this variation, especially in areas or countries
with similar characteristics, would be useful in the formulation of

Please cite this article as: Rostami A et al., Global prevalence of latent toxoplasmosis in pregnant women: a systematic review and meta-analysis,
Clinical Microbiology and Infection, https://doi.org/10.1016/j.cmi.2020.01.008
 A. Rostami et al. / Clinical Microbiology and Infection xxx (xxxx) xxx
improved public health policies. That is, if two countries had
similar profiles, but significantly different prevalence rates, there
might be lessons that could be learned and applied to reduce the
burden of latent toxoplasmosis. Therefore, a multinational
approach to examine these variations and their drivers is needed
to inform action.
Our findings corroborate a general assumption that nearly one-
third of humans have been exposed to T. gondii [32]. For the studies
included, the prevalence rates of latent toxoplasmosis ranged from
0.7% in South Korea (Western Pacific region) to 92% in Ghana (Af-
rican region). We observed the highest prevalence rates in the
South American (56.2%) and African (48.7%) regions, and the lowest
prevalence in the Western Pacific region (11.8%). Prevalence rates in
countries located in the Eastern Mediterranean, European, North
American and South-East Asian regions were 35.1%, 31.2%, 28.2%
and 23.7%, respectively, showing considerable variation among
WHO -regions, and even among studies within the same region
(Table 1). Differences in the prevalence of latent toxoplasmosis in
pregnant women among the different WHO geographical regions
will require additional epidemiological investigations and further
studies related to the social determinants of disease. It is likely that
they may be attributed to variation in levels of public health and
sanitary services, economic status, different cultural and social
conditions, and differences in climate. For example, some African
countries where the prevalence rates were highest, including
Madagascar, Ghana, Cameroon and Congo, exhibit extreme poverty,
low income levels and low HDIs, which are associated with inad-
equate sanitary services. Specific reasons for high prevalence rates
of latent toxoplasmosis in some African and South American
countries could include (1) a relatively large numbers of cats and
diverse T. gondii genotypes in these areas; (2) a lack of control
measures for stray cats living in urban and peri-urban areas; and (3)
high levels of contamination of the environment (e.g., soil and
water) and/or food with T. gondii oocysts [33,34]. In contrast,
countries in the Western Pacific region, including South Korea
(2.7%), China (9.4%) and Japan (10.3%), with higher levels of income,
may attribute lower prevalence rates due to better control mea-
sures for stray cats, better environmental hygiene, and may also
reflect a lower consumption of undercooked meat [35]. Our results
regarding disparities among countries with varying economic sta-
tus are supported by previous studies showing high burden of
congenital toxoplasmosis and acute Toxoplasma infection in preg-
nant women in low-income countries [1,3]. Similarly, in a recent
meta-analysis study, Wang et al. [36] reported a higher burden of
T. gondii infection in HIV þ patients living in countries with lower
income levels versus high income countries. In accordance with
this reasoning, our analyses showed that pregnant women in areas
with lower income levels and HDIs are at greater risk for exposure
to T. gondii. However, some other nations with relatively high levels
of poverty, such as India, Bangladesh and Pakistan in South Asia, did
not exhibit particularly high rates of Toxoplasma exposure. This
could be explained by the fact that there are more vegetarians in
these countries and that the consumption of raw or semi-cooked
meat is raredmost people consume well-cooked meat [3]. Like-
wise, an explanation for a relatively low prevalence of latent
toxoplasmosis in countries in the Western Pacific region might be
due to high proportion of marine food (fish and etc.) and lower
consumption of raw or undercooked meat in the daily diet of
people in these countries [37], while moderate to high prevalence
rates of latent toxoplasmosis in European, North America and
Middle East regions could be explained by the fact that under-
cooked meat, such as lamb or kebab, are popular foods in these
regions [3,9].
Other factors explaining variation of latent toxoplasmosis
prevalence in different countries or even within the same country
Please cite this article as: Rostami A et al., Global prevalence of latent toxoplasmosis in pregnant women: a systematic review and meta-analysis,
Clinical Microbiology and Infection, https://doi.org/10.1016/j.cmi.2020.01.008
9
could be different environmental and climate parameters. Epide-
miological studies in Latin/Caribbean countries revealed a high
burden of T. gondii infection in stray cats [38e40], suggesting that
the environment may be heavily contaminated with oocysts [41],
which in turn can lead to contamination of vegetables and
contamination of the hands of people in contact with soil. More-
over, the high prevalence rates of toxoplasmosis found in Cuba and
Brazil could possibly be related to a tropical climate, along with
cultural and culinary habits.
Many factors enter into the influence of climate. For example, a
study in Colombia [33] showed that altitude and mean temperature
were not significantly correlated with geographical differences in
incidence, but that mean annual precipitation was. Other studies
have shown that the incidence risk of Toxoplasma infection in cats
or marine mammals relates to mean precipitation [34], and a recent
global meta-regression analysis indicated significant and non-
significant decreasing trends of acute Toxoplasma infection in
pregnant women with increasing geographical latitude and annual
precipitation, respectively [35]. Clearly, precipitation, moisture and
temperature play an important role in survival, sporulation and
infectivity of T. gondii oocysts in water and soil [36,37] and have a
significant effect on the prevalence of Toxoplasma infection in a
particular geographical area. In the future, it would interesting to
develop a multisectoral model, potentially based on poverty, meat
consumption and climate, for the prediction of toxoplasmosis
prevalence rates.
Our study did not examine variation within individual coun-
tries due to a limited availability of studies for many regions.
However, one would expect significant variation among regions
or communities within individual countries (especially large
countries or countries with a wide range of climatic and eco-
nomic disparities). Understanding the variation in prevalence
among regions of a country could help in assessing risk factors
and developing improved programs and policies to reduce the
burden of latent toxoplasmosis. Therefore, we believe that our
results may help to support future modelling and risk map
analyses.
In subgroup analyses, our findings indicated an increasing
prevalence rate with increasing age, which is in accordance with
some previously published results [9,42e45]. One explanation
could be that, assuming risk is constant over time, older women
have had a longer period of time for exposure to, or infection with
Toxoplasma. On that basis, it might be of interest to examine the risk
of young mothers acquiring first-time infection during pregnancy
in areas where the overall community prevalence (IgG antibody)
for toxoplasmosis is high. Since anti-T. gondii antibodies persist for a
long time (usually for life) [46], increasing seroprevalence with age
is a result of exposure over time [47e49]. In addition, our results
showed an increasing trend in prevalence rate over the time period
of a study, although it was statistically non-significant (p 0.64).
Likely explanations for this increasing trend might include an
increasing tendency of world population to eat undercooked meats,
fast food (hamburgers, sausages and other) and/or an increasing
close relationships with pet cats. Another possible explanation for
an increased prevalence rate in recent years might an increased
sensitivity and/or decreased specificity (increased ‘background’) of
serological tests.
This systematic review has a number of strengths and
limitations. By including 311 studies from 91 countries repre-
senting all seven WHO regions in the meta-analysis, we were
able to estimate the prevalence of latent toxoplasmosis in
pregnant women using a large sample size (n ¼ 1 148 677
participants), thereby increasing the reliability of the estimates.
It should be noted that, although most studies recruited
randomly selected participants, some studies might have
10 A. Rostami et al. / Clinical Microbiology and Infection xxx (xxxx) xxx
employed distinct methods of sampling which may have
confounded results for respective regions or countries. We took
into account the effects of study-level factors, including
geographical and sociodemographic variables, on the preva-
lence of latent toxoplasmosis by subgroup and meta-regression
analyses. Limitations for this study are similar to our previous
meta-analyses on the global status of infectious diseases
[48,50,51]. Some important limitations include publications
which may have been missed (mainly due to publication in
national journals), and little or no data for some important
countries or regions. We expect that the prevalence of latent
toxoplasmosis in pregnant women in countries without data or
with a single study would be similar to the pooled prevalence
established for the same region, but this might not be the case.
Other important limitations are the existence of substantial
heterogeneity among studies, which is recognized as common
or expected in global prevalence investigations [52e54]. We
attempted to define a source of heterogeneity, but did not find
it. The high level of heterogeneity is consistent across all WHO-
regions. The usual process to deal with heterogeneity is to look
for mediating variables. We tried to do so, and tested effects of
geographical regions, sociodemographic parameters, diagnostic
methods, over time and sample size, but without success. This
issue remains to be solved through future research. We
accepted individual authors' definitions of cut-off values for
test positivity in diagnostic methods, and this could be a
source of heterogeneity in the seroprevalence analysis. Another
issue is that different diagnostic methods were used in distinct
studies. Bioassays (in mice or cats) are considered a reference
standard for the definitive diagnosis of Toxoplasma infection,
but are usually not used for the diagnosis of Toxoplasma
infection or toxoplasmosis in humans. Serological assays are
predominantly employed for epidemiological surveys. As there
is variation in the sensitivity and specificity (and, thus, positive
and negative predictive values) among distinct assays, sero-
logical results might not represent true prevalence rates. Thus,
seroprevalence rates reported in the present study are
apparent prevalence rates for Toxoplasma infection.
Despite the above limitations, these data on the prevalence of
latent T. gondii infection in pregnant women should assist health
policy makers in prioritizing programs and interventions that
improve public health and minimize adverse outcomes. The Sus-
tainable Development Goal of the United Nations calls for reducing
newborn, child and maternal mortalities by ending preventable
deaths before 2030. Therefore, it is important to better understand
the risk factors and drivers of latent toxoplasmosis, in order to
improve maternal health. Clearly, many of the risk factors could be
addressed by improved hygiene and health education. In-
terventions to improve maternal health, through improved
knowledge of potential risk factors, including nutritional sources
and contact with cats, could help to reduce the risk of health
problems arising from both primary and latent infections with
T. gondii.
Transparency declaration
There was no specific funding source for this study. The authors
declare that there are no conflicts of interest.
Role of funding source
No external funding was received for this study. The corre-
sponding author had access to the data in the study and had final
responsibility for the decision to submit for publication.
Please cite this article as: Rostami A et al., Global prevalence of latent toxoplasmosis in pregnant women: a systematic review and meta-analysis,
Clinical Microbiology and Infection, https://doi.org/10.1016/j.cmi.2020.01.008
Acknowledgements
RBG's research program is presently supported through funds
from the National Health and Medical Research Council (NHMRC)
of Australia, the Australian Research Council (ARC), Yourgene
Health, Melbourne Water Corporation and The University of
Melbourne.
Appendix A. Supplementary data
Supplementary data to this article can be found online at
https://doi.org/10.1016/j.cmi.2020.01.008.
Author contributions
A.R., S. M.R, H.R.G. and R.B.G conceived the study. M.N.S, M.D.,
H.B., S.P., M.F., conducted the searches and collected data. A.R.,
S.M.R. and Y.F. analysed and interpreted the data sets. A.R., H.R.G.
and R.B.G drafted and edited the manuscript. R.B.G, A.H.M and P.J.H.
critically reviewed and revised the paper. All authors commented
on, or edited drafts and approved the final version of the
manuscript.
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