International Journal for Parasitology 39 (2009) 1385–1394

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International Journal for Parasitology

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Toxoplasmosis snapshots: Global status of Toxoplasma gondii seroprevalence

and implications for pregnancy and congenital toxoplasmosis
Georgios Pappas a,b,*, Nikos Roussos a, Matthew E. Falagas a,c,d
a
Alfa Institute of Biomedical Sciences (AIBS), Athens, Greece
b
Institute of Continuing Medical Education of Ioannina, Greece
c
Department of Medicine, Henry Dunant Hospital, Athens, Greece
d
Department of Medicine, Tufts University School of Medicine, Boston, MA, USA

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

Article history: Toxoplasma gondii’s importance for humans refers mainly to primary infection during pregnancy, result-
Received 17 February 2009 ing in abortion/stillbirth or congenital toxoplasmosis. The authors sought to evaluate the current global
Received in revised form 22 April 2009 status of T. gondii seroprevalence and its correlations with risk factors, environmental and socioeco-
Accepted 23 April 2009
nomic parameters. Literature published during the last decade on toxoplasmosis seroprevalence, in
women who were pregnant or of childbearing age, was retrieved. A total of 99 studies were eligible;
a further 36 studies offered seroprevalence data from regions/countries for which no data on preg-
Keywords:
nancy/childbearing age were available. Foci of high prevalence exist in Latin America, parts of East-
Toxoplasmosis
Pregnancy
ern/Central Europe, the Middle East, parts of south-east Asia and Africa. Regional seroprevalence
Seroprevalence variations relate to individual subpopulations’ religious and socioeconomic practices. A trend towards
lower seroprevalence is observed in many European countries and the United States of America
(USA). There is no obvious climate-related gradient, excluding North and Latin America. Immigration
has affected local prevalence in certain countries. We further sought to recognise specific risk factors
related to seropositivity; however, such risk factors are not reported systematically. Population aware-
ness may affect recognition of said risks. Global toxoplasmosis seroprevalence is continuingly evolving,
subject to regional socioeconomic parameters and population habits. Awareness of these seroprevalence
trends, particularly in the case of women of childbearing age, may allow proper public health policies to
be enforced, targeting in particular seronegative women of childbearing age in high seroprevalence
areas.
Ó 2009 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.

1. Introduction
Toxoplasma gondii is an obligate intracellular protozoan able to
infect different species (Tenter et al., 2000). Sexual forms of the
parasite are found in the intestinal epithelium of definitive hosts
such as domestic cats: therein they transform into oocysts which
are subsequently shed in the environment. Oocysts, remarkably
stable environmentally, are transmitted to other hosts through
inadvertent ingestion. Humans acquire T. gondii through ingestion
of undercooked meat, contact with feline faeces and rarely through
drinking contaminated water or through transplantation of a con-
taminated organ (Hill and Dubey, 2002).
Human toxoplasmosis is usually subclinical or resembles a min-
or viral illness (Montoya and Liesenfeld, 2004). It is nevertheless
the most common food-borne parasitic infection requiring hospi-
* Corresponding author. Address: Institute of Continuing Medical Education of
Ioannina, H. Trikoupi 10, 45333 Ioannina, Greece. Tel./fax: +30 26510 28289.
E-mail address: gpele@otenet.gr (G. Pappas).
talisation (Vaillant et al., 2005) and the third most common cause
of hospitalisation due to food-borne infection overall (Mead et al.,
1999). Furthermore the parasite’s bradyzoites can persist inside
human cells for protracted periods and latent infection may be
reactivated, typically in the case of AIDS where T. gondii reactiva-
tion causes severe encephalitis (Porter and Sande, 1992).
Primary infection during pregnancy may cause spontaneous
abortion or stillbirth. A newborn exposed to T. gondii in utero
may develop congenital toxoplasmosis with major ocular and
neurological consequences. The disease burden of congenital
toxoplasmosis, as represented by disability-adjusted life years
(DALY), is the highest among all food-borne pathogens (Havelaar
et al., 2007).
Due to its long-term complications and the fact that T. gondii is
omnipresent, epidemiological studies on its seroprevalence help
shape health policies in individual countries. The purpose of this
is to collectively evaluate available epidemiological data on the
worldwide seroprevalence of T. gondii, particularly focusing on
pregnant women or women of childbearing age (15–45 years).

0020-7519/$36.00 Ó 2009 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.ijpara.2009.04.003
1386 G. Pappas et al. / International Journal for Parasitology 39 (2009) 1385–1394
2. Materials and methods
A literature search was initially performed in PubMed (http://
www.ncbi.nlm.nih.gov/sites/entrez?db=pubmed) and Scopus
(www.scopus.com) databases using as keywords the terms ‘‘sero-
prevalence OR seropositivity” AND ‘‘toxoplasma OR toxoplasmo-
sis”. We subsequently searched these databases and a general
search engine (Google, http://www.google.com) using the terms
‘‘Toxoplasma OR Toxoplasmosis” and individual country names,
for all countries (e.g. ‘‘toxoplasmosis AND Afghanistan”, and so
on). We additionally searched the SciELO (scientific electronic li-
brary online, www.scielo.br) database with the keyword toxoplas-
mosis, for hitherto unretrieved relevant Latin American literature.
A further search was performed in the references of the initially re-
trieved articles. We also searched abstract books of last decade’s
international infectious disease congresses for additional studies,
including the Infectious Diseases Society of America’s annual meet-
ings (http://www.idsociety.org/Content.aspx?id=1900), the Inter-
national Congress of Infectious Diseases (http://www.isid.org),
and the European Congress of Clinical Microbiology and Infectious
Diseases (http://www.blackwellpublishing.com/eccmid18).
We selected articles published during the last decade, i.e. after
January 1, 1999 and registered until December 30, 2008 (when a
final search was re-performed), irrespective of the date of retrieval
of the contained data. Available literature on the subject published
prior to 1999 has been summarised in a relevant review, published
in 2000 (Tenter et al., 2000). For countries for which no recent data
were available, relevant data search was extended until 1990, in
order to create a global view of T. gondii seroprevalence. Articles
written in languages other than English, Greek, Spanish, French
or Italian were translated by a native speaker of the individual
language.
Included studies reported seroprevalence rates either in women
of childbearing age or pregnant, or in the general population or a
representative sample of it. Studies focusing on specific target
groups (for example HIV-positive patients or slaughterhouse work-
ers or children or psychiatric patients) were excluded. We also ex-
cluded studies focusing on a specific sub-group of pregnancy,
Fig. 1. Global status of Toxoplasma gondii seroprevalence. Dark red equals prevalence above 60%, light red equals 40–60%, yellow 20–40%, blue 10–20% and green equals
prevalence <10%. White equals absence of data. Data as described in tables and text (Section 3).
women with bad obstetric history, since their results cannot be
reliably translated to general prevalence rates. For a study to be in-
cluded, the minimum number of patients was preset as 100, in or-
der to minimise undue sampling biases into prevalence estimates.
2.1. Statistical analysis
Confidence intervals (CIs) for seroprevalence rates in each indi-
vidual study were either derived from the relevant study, or esti-
mated using the freely available online Sample Size Calculator
(Creative Research Systems, http://www.surveysystem.com/
sscalc.htm). When CIs were not available from an individual study,
we calculated 95% CIs using the available sample size and percent-
ages, and presumed that the population from which the sample
size was derived was too large (or unknown) to exert any signifi-
cance on 95% CIs.
3. Results
Fig. 1 depicts the current global T. gondii seroprevalence status,
according to the data retrieved and subsequently analysed and
discussed.
3.1. North and Latin America
Numerous studies derive from Latin America, in particular Bra-
zil; data for USA are derived from the nationwide NHANES study
(Jones et al., 2007), while limited information is available for Can-
ada (Table 1). The majority of studies emerging from Latin Ameri-
can countries show significantly high seropositivity rates; the only
exception is a large-sample study from Brasilia (Cabral et al.,
2008): one can presume that Brazil’s capital may exhibit a different
socioeconomic structure compared to the rest of the country since
it is a city recently built in order to serve as a federal centre. Sero-
prevalence studies in general population samples in Amerindians
have shown even higher prevalence rates and potential correla-
tions with sanitary practices and eating/drinking habits (the use
of well water or the consumption of rodents or monkeys) (Boia
 G. Pappas et al. / International Journal for Parasitology 39 (2009) 1385–1394 1387

Table 1
Toxoplasmosis seroprevalence in the Americas – females of reproductive age or pregnant.

Country (reference) Region Sample size (absolute Seroprevalence in % Comments – risk factors identified
number) (95% confidence
intervals)
Argentina (Marquez and Etcheverry, 2003) La Plata– Buenos Aires Pregnant (1,007) 48.7 (45.6–51.8) 1992 rate was 65.7%
Argentina (Rickard et al., 1999) Buenos Aires Pregnant (650) 53.4 (49.6–57.2)
Brazil (Lago et al., 2009) Southern (Rio Grande do Pregnant (2,421) 67 (65.1–68.9)
Sul)
Brazil (Porto et al., 2008) Recife Pregnant (503) 77.5 (73.9–81.1) School attendance only risk factor
Brazil (Carellos et al., 2008) Minas Gerais Pregnant (420) 61.2 (56.5–65.9)
Brazil (Cabral et al., 2008) Brasilia Childbearing age (37,961) 7.3 (7.0–7.6)
Brazil (Reis et al., 2006) Porto Alegre Pregnant (10,468) 61.1 (60.2–62.0)
Brazil (Spalding et al., 2005) Southern (Rio Grande do Pregnant (2,126) 74.5 (72.7–76.3) Contact with soil, consumption of
Sul) poorly cooked meat, contact with
rodents/cats
Brazil (Avelino et al., 2004) Goiania Childbearing age (2,242) 51.2 (49.1–53.3)
Brazil (Olbrich Neto and Meira, 2004) Botucatu, Sao Paulo Pregnant (478) 60 (55.6–64.4)
Brazil (Leao et al., 2004) Mato Grosso Pregnant (205) 70.6 (64.4–76.8)
Brazil (Varella et al., 2003) Porto Alegre Pregnant (1,261) 59.8 (57.1–62.5) Inverse relation to educational level
Brazil (Reiche et al., 2000) Parana Pregnant (1,559) 67 (64.7–69.3)
Brazil (Rey and Ramalho, 1999) Fortaleza Pregnant (186) 71.3 (64.8–77.8)
Colombia (Rosso et al., 2008) Cali Pregnant (955) 48.7 (45.5–51.9) Increase compared with 1980s
Colombia (Castro et al., 2008) Villavicencio Pregnant (300) 63.5 (60.3–66.7) Contact with felines as risk factor
Colombia (Barrera et al., 2002) Bogota Pregnant (637) 47 (43.1–50.9)
Costa Rica (Zapata et al., 2005) Central Valley 20–40 year old (283) 55 (49.2–60.8) Increased prevalence in rural origin
and low socioeconomic status
Cuba (Martinez et al., 2005) Havana–Lisa Pregnant (160) 44 (36.3–51.7)
Cuba (Sanchez-Gutierrez et al., 2003) Havana and Pinar del Rio Pregnant (1,210) 61.8 (59.1–64.5)
Cuba (Acosta-Bas et al., 2001) Marianao–Havana Pregnant (207) 60.3 (53.6–67.0)
Grenada (Asthana et al., 2006) Nationwide Pregnant (534) 57 (52.8–61.2)
Mexico (Alvarado-Esquivel et al., 2006) Durango Pregnant (343) 6.1 (3.6–8.6)
Trinidad and Tobago (Ramsewak et al.,, 2008) 2/3 island hospitals Pregnant (450) 42.9 (38.3–47.5)
United States (Jones et al., 2007) Nationwide Childbearing age (>6,000a) 11 (10.2–11.8) 7.7 for US-born, 28.1 for foreign-born
Venezuela (Triolo-Mieses and Traviezo-Valles, Lara State Pregnant (446) 38 (33.5–42.5)
2006)
a
Estimate.

et al., 2008). The overall climate conditions of the rainforest region
might also allow for the protracted environmental survival of the
parasite’s oocysts (de la Rosa et al., 1999). There are no seropreva-
lence data for French Guyana, which has recently been the host of
an aggressive disease outbreak in immunocompetent patients
(Bossi and Bricaire, 2004). High seroprevalence rates can be pro-
jected for Guatemala, according to results from a study in children
showing seroprevalence of 37.8% by the age of 10 years (Jones
et al., 2005). An older nationwide general population study in Chile
showed relatively lower seroprevalence (36.9% overall) (Contreras
et al., 1996). Older nationwide studies in Mexico (Velasco-Castre-
jon et al., 1992) exhibited in general a north–south seroprevalence
gradient: rates in south Mexico were similar to the rest of Latin
America. Recent data though are available only from the north-
centre state of Durango, where current seroprevalence estimates
are significantly lower than in the recent past (6.1% compared with
19.2% in the aforementioned nationwide study). Even if this lower
seroprevalence trend is projected in the rate of the recent past for
the southern states, the overall rate would remain high in these
states. Seroprevalence in the USA is significantly decreased,
according to the two most recent NHANES studies (Jones et al.,
2007). Prevalence is higher in African–Americans and Mexican–
Americans, particularly in those not born in the USA (one can pre-
sume that the lower rates observed in USA-born Mexican–Ameri-
cans correlate with the environmental conditions of the southern
USA states, where the majority of them reside: these are similar
to those observed in the north Mexican states and may not allow
for protracted T. gondii environmental survival). The relationship
of toxoplasmosis seropositivity to socioeconomic status has led
some experts to propose a generalised intervention through mass
screening for congenital toxoplasmosis (Hotez, 2008). Recent gen-
eral population data from Toronto, Canada, report seropositivity of
16.8–18.6% (Shuhaiber et al., 2003). Inuits comprise a population
with significant seroprevalence. A recent study in a Canadian–Inuit
population showed prevalence of 59.8% (Messier et al., 2009) and
these rates (in the past reproduced also in Alaskan residents) have
been related to consumption of seal and caribou meat.
3.2. Europe
European studies on toxoplasmosis seroprevalence in preg-
nancy or in females of childbearing age do not homogenously de-
pict the general European seroprevalence status, with certain
countries such as Greece being over-represented, while available
data for some of the Western/Central European regions are mini-
mal (Table 2). A West–East gradient may exist according to avail-
able data. Conclusions may not easily be drawn, however, due to
different individual country policies towards toxoplasmosis
screening. A recent review (Benard et al., 2008) showed that epide-
miologic surveillance for congenital toxoplasmosis is limited
throughout Europe: only two countries have such a nationwide
surveillance program (France and Germany); Austria has a similar
program, while Denmark’s program recently stopped. This review
emerged from the EUROTOXO project, a coalition of scientists
cooperating on all aspects of congenital toxoplasmosis (http://
eurotoxo.isped.u-bordeux2.fr). Another obstacle in interpreting re-
sults of some of the studies is the gradual change in the sampled
population due to immigration, particularly from Eastern Europe,
as observed in certain areas of Greece and Spain. Trends towards
lower seroprevalence are observed in certain countries together
with a trend towards localisation of increased seroprevalence rates
in rural areas. The prime example of minimal available data is
France, synonymous to toxoplasmosis seropositivity in all text-
books: a study on risk factors for toxoplasmosis during pregnancy
1388 G. Pappas et al. / International Journal for Parasitology 39 (2009) 1385–1394

Table 2
Toxoplasmosis seroprevalence in Europe – females of reproductive age or pregnant.

Country (reference) Region Sample size Seroprevalence in % Comments – risk factors identified
(absolute number) (95% confidence
intervals)
Belgium (Breugelmans et al., 2004) Brussels Pregnant (16,541) 48.7 (47.9–49.5) Minor prevalence decrease compared with
the 1980s
Croatia (Punda-Polic et al., 2000) Split Childbearing age (1,109) 38.1 (35.2–41.0)
Czech Republic (Kankova and Flegr Prague Pregnant (1,053) 19.8 (17.4–22.2)
(2007))
Denmark (Lebech et al., 1999) Copenhagen Pregnant (89,873) 27.8 (27.5–28.1)
Germany (Fiedler et al., 1999) Western Pregnant (not specified) 63.2
Pomerania
Greece (Kansouzidou et al., 2008) Northern Greece Childbearing age (273) 21.2 (16.4–26.0)
Greece (Baka et al., 2006) Athens Pregnant (1,466) 20.1 (18.1–22.1)
Greece (Diza et al., 2005) Northern Greece Childbearing age (about 150-estimate) 20 (13.6–26.4) Gradual prevalence decrease compared with
previous decades
Greece (Glynou et al., 2005) Athens Childbearing age (3,016) 25.4 (23.9–26.9)
Significant difference in prevalence between
Greeks (12.2) and immigrants (45.1)
Greece (Antoniou et al., 2004) Crete Pregnant (5,532) 29.4 (28.2–30.6)
Greece (Mela et al., 2004) Thrace Childbearing age (318) 22 (17.5–26.5)
Prevalence 15% in Greek orthodox, 31% in
Muslims, 29% in Greek-Soviet immigrants
Greece (Alexandrou et al., 2002) Athens Pregnant (2,794) 24.1 (22.5–25.7)
Similar prevalence in Greeks and Eastern
Europe immigrants
Greece (Farsaraki et al., 2002) Crete Childbearing age (8,100) 36.4 (35.4–37.4)
Ireland (Ferguson et al., 2008) Nationwide Pregnant (20,252) 24.6 (24.0–25.2) Prevalence varying by county, range 19.9
(Dublin) to 41.3 (Longford)
Italy (Masini et al., 2008) Rome Pregnant (1,345) 19.8 (17.7–21.9)
Italy (De Paschale et al., 2008) Legnano– Pregnant (3,426) 22.7 (21.3–24.1)
Lombardy
Italy (Beccara et al., 2005) Verona Pregnant (1801) 17.5 (15.8–19.2)
Italy (Ricci et al., 2003) Rome Pregnant (8,061) 34.4 (33.4–35.4)
Italy (Russo et al., 1999) Catania Pregnant (9,029) 23 (22.1–23.9)
Netherlands (Kortbeek et al., 2004) Nationwide Childbearing age (selected from 7,521 35.2 (32.9–38.6) Significantly decreased compared with
samples) previous decade
Poland (Nowakowska et al., 2006) Lodz Pregnant (4,916) 41.3 (39.9–42.7) Gradual decrease in the study period (1998–
2003)
Poland (Niemiec et al., 2002) Warsaw Pregnant (2,016) 35.8 (33.7–37.9)
Poland (Paul et al., 2001) Poznan Pregnant (2,656) 43.7 (41.8–45.6) Prevalence increased in rural origin
Romania (Olariu et al., 2008) Timisoara Childbearing age (328) 57.6 (52.3–62.9)
Prevalence increased in rural origin
Serbia (Bobic et al., 2007) Nationwide Childbearing age (765) 33 (29.7–36.3) Major decrease compared during the early
1990s – prevalence was 86% in 1988 – risk
factors were contact with soil and
undercooked beef
Slovakia (Studenicova et al., 2008) Bratislava Pregnant (656) 22.1 (18.9–25.3) Contact with soil, suburban residence were
risk factors
Slovenia (Logar et al., 2002) Nationwide Pregnant (21,270) 34 (33.4–34.6) Decrease compared with previous reports
Spain (Bartolome Alvarez et al., Albacete Pregnant (2,623) 21 (19.4–22.6) Significant difference in prevalence between
2008) Spanish (16%) and immigrants (51%)
Spain (Gutierrez-Zufiaurre et al., Salamanca Pregnant (2,929) 18.8 (17.4–20.2)
2004)
Spain (Munoz Batet et al., 2004) Barcelona Pregnant (16,362) 28.6 (27.9–29.3)
Spain (Pujol-Rique et al., 2000) Barcelona Childbearing age (7,090) 43.8 (42.7–44.9) Decreasing prevalence during the 1990s
Sweden (Evengard et al., 2001) Stockholm and Pregnant (40,978) 18 (17.6–18.4) 14% for Stockholm, 25.7% for Skane
Skane
Switzerland (Zufferey et al., 2007) Lausanne and Childbearing age (1,000) 8.2 (6.5–9.9)
Geneva
Switzerland (Signorell et al., 2006) Basel Pregnant (not specified) 35 Significant prevalence decrease for 1999
compared with the 1980s
United Kingdom (Nash et al., 2005) East Kent Pregnant (1,897) 9.1 (7.8–10.4) Prevalence related to rural or continental
childhood residence

estimated a seroprevalence in pregnancy of 59% for 1995 (Baril
et al., 1999). Some conclusions can be indirectly drawn from inci-
dence data, such as those reported by the European Food Safety
Authority (EFSA) (European Food Safety Authority, 2007) which
showed a decreasing incidence overall (0.84/105 for 2005, com-
pared with 1.7/105 in 1995), with a predominance of reported
cases from Lithuania, Czech Republic and Slovakia. High seroprev-
alence rates in the general population were also reported for an-
other Baltic country, Estonia, where prevalence was above 50%
in a population sample that included women of reproductive
age. In the same study (Birgisdottir et al., 2006), general popula-
tion prevalence was significantly lower for Sweden (23%) and
even lower for Iceland (9.8%). An older study from Denmark re-
ported low prevalence rates in pregnancy for Faroe Islands and
Greenland: the rates were similar to those of Iceland, a country
geographically closer to Greenland and Faroe, compared with
their federal administration, Denmark (Lebech et al., 1993).
Regarding information emerging from older studies, not included
 G. Pappas et al. / International Journal for Parasitology 39 (2009) 1385–1394 1389

in Table 2, one should note the low seroprevalence of Norway,
with a north to south gradient of 6–13% (Jenum et al., 1998), a
gradual decrease of seropositivity in Austria (still 42% though in
1997) (Moese and Vander-Moese, 1998), a stable high prevalence
in Hungary (almost 60% for the mid-1990s) (Szenasi et al., 1997),
and a south–north gradient in Portugal (Angelo, 2003) possibly
related to enhanced disease awareness in the south of the country
(Machado et al., 2006).
3.3. Asia and Oceania
Regarding studies on toxoplasmosis seroprevalence in women
who are pregnant or of childbearing age originating from Asia
and Oceania, once more there is an over-representation of certain
countries such as Iran, while information from other, geographi-
cally larger, countries may be limited (Table 3). There exists no
obvious gradient in toxoplasmosis seroprevalence in Asia. High-
prevalence foci exist in the Middle East including Turkey, Iran, Iraq
and Kuwait. A general population study in Eastern Saudi Arabia
showed a lower prevalence, reaching 25% (Al-Qurashi et al.,
2001), similar to pregnant women in Bahrain (Tabbara and Saleh,
2005), and to the general population prevalence observed in Qatar
(Abu-Madi et al., 2008). In the latter study, the authors raised their
concern regarding the relationship of seroprevalence and the feline
population of Doha, the Qatar capital: it is estimated that 2 million
cats live in Qatar. What is surprising, however, is that the preva-
lence rates in neighbouring countries are much higher, and Qatar,
too many cats or not, actually exhibits a low regional seropreva-
lence. Another high seroprevalence region, partly at least, is
south-east Asia, with high rates in Indonesia and Malaysia but sig-
nificantly lower rates in Thailand or Vietnam. This variation may
be observed in regions of the same country. In the Philippines a
general population study (Kawashima et al., 2000) demonstrated
prevalence ranged from 11.1% in Manila to >60% in Mindoro. The
phenomenon of mixed racial populations may explain some of
the observed differences. A general population study in Northern

Table 3
Toxoplasmosis seroprevalence in Asia and Oceania – females of reproductive age or pregnant.

Country (reference) Region Sample size Seroprevalence in % Comments – risk factors identified
(absolute number) (95% confidence
intervals)
Australia (Karunajeewa et al., Melbourne Pregnant (308) 23 (18.3–26.7)
2001)
Bahrain (Tabbara and Saleh, 2005) Manama Childbearing age (3,499) 22.3 (20.9–23.7)
China (Liu et al., 2009) Changchun Pregnant (235) 10.6 (6.7–14.5)
India (Borkakoty et al., 2007) Assam Pregnant (180) 41.6 (34.4–48.8)
India (Singh and Pandit, 2004) New Delhi Pregnant (180) 45 (37.7–52.3)
India (Akoijam et al., 2002) New Delhi Pregnant (503) 41.7 (37.4–46.0)
India 1999 (Kaur et al., 1999) New Delhi Pregnant (120) 11.6 (5.9–17.3)
Indonesia (Terazawa et al., 2003) Jakarta Childbearing age (20– >60%
39 years) (399)
Iran (Abdi et al., 2008) Ilam Pregnant (553) 44.8 (40.7–48.9)
Iran (Fallah et al., 2008) Hamadan Pregnant (576) 33.5 (29.7–37.3) Related to consumption of undercooked meat
and raw vegetables
Iran (Pashazadeh et al., 2008) Tabriz Pregnant (197) 29.4 (23.0–35.8)
Iran (Saeedi et al., 2007) Gorgan Pregnant (300) 48.3 (42.7–53.9) Related to household felines
Iran (Youssefi et al., 2007) Babol Childbearing age (241) 63.9 (57.8–70.0)
Iran (Sagha and Daryani, 2004) Arabia City Childbearing age (504) 34.7 (30.5–38.9)
Iran (Taravati and Sadegkhalili, Urmia Childbearing age (300) 32.8 (27.5–38.1)
2003)
Iraq (Mahdi and Sharief, 2002) Basrah Pregnant (254) 49.2 (43.1–55.3) Related to poor socioeconomic status and
contact with soil
Jordan (Jumaian, 2005) Amman Pregnant (280) 47.1 (41.3–52.9)
Korea, South (Han et al., 2008) Daejeon Pregnant (351) 3.7 (1.7–5.7) Related to consumption of undercooked meat
Korea, South (Song et al., 2005) Suwon Pregnant (5,175) 0.8 (0.6–1.0
approximately)
Kuwait (Iqbal et al., 2003) Kuwait Pregnant (225) 45.7 (39.2–52.2)
Malaysia (Nissapatorn et al., Kuala Lumpur Pregnant (200) 49 (42.1–55.9) Prevalence significantly higher in Malays
2003) (55.7%) and Indians (55.3%) compared to
Chinese (19.4%) – no correlations to any risk
factor – incidence increasing compared to past
reports (Nissapatorn and Abdullah, 2004)?
New Caledonia (Breurec et al., Regional Pregnant (2,416) 56.7 (54.7–58.7) Prevalence significantly higher in North-east
2004) (79.1%), and Melanesian origin (62.1%)
New Zealand (Morris and Auckland Pregnant (500) 35.4 (31.2–39.6)
Croxson, 2004)
Singapore (Wong et al., 2000) Singapore Pregnant (120) 17.2 (10.5–23.9)
Taiwan (Lin et al., 2008) Mid-Taiwan Pregnant (426) 31 (26.6–35.4) Prevalence lower in immigrants (18.2%) than
natives (40.6) – related to consumption of
undercooked pork, contact with soil and felines
Thailand (Tantivanich et al., 2001) Bangkok Pregnant (200) 21.5 (15.8–27.2)
Thailand (Wanachiwanawin et al., Bangkok Pregnant (831) 5.3 (3.8–6.8) Significantly low compared with prevalence in
2001) HIV-positive pregnant (53.7%)
Thailand (Sukthana et al., 2000) Nationwide Pregnant (1,200) 13.2 (11.3–15.1) Related to consumption of undercooked meat
and household felines
Turkey (Ocak et al., 2007) Hatay Province Pregnant (1,652) 52.6 (50.2–55)
Turkey (Ertug et al., 2005) Aydin Pregnant (389) 30.1 (25.5–34.7)
Turkey (Harma et al., 2004) Southeastern Anatolia– Pregnant (1,149) 60.4 (57.6–63.2) Increased prevalence presumably related to
Sanliurfa eating habits (raw meatball consumption)
Vietnam (Buchy et al., 2003) Nha Trang Pregnant (300) 11.2 (7.6–14.8)
1390 G. Pappas et al. / International Journal for Parasitology 39 (2009) 1385–1394
Thailand showed variations according to origin, with Chinese ori-
gin coinciding with low prevalence, but also differences between
individual aboriginal populations, ranging from 9.1% to 37.9% (for
the Yau aborigines) (Fan et al., 2003). Similarly, a study on migrant
workers in Malaysia also showed major ethnic differences (Chan
et al., 2008): the highest prevalence was noted in Nepalese work-
ers; the majority of the other migrant ethnic groups exhibited low-
er rates compared with the seroprevalence observed in those of
Malaysian origin. Differences in daily practices and ethnic habits
probably account for these differences. Malaysians, for example,
are known to have cats as pets. Migration, however, is not a phe-
nomenon limited to population circulation in neighbouring coun-
tries; it can also be transcontinental, carrying seroprevalence
variations to a broadly different environment. There are no data
available for Cambodia and Laos, while the neighbouring Vietnam
exhibits low prevalence rates; yet a study on congenital toxoplas-
mosis in Massachusetts, USA (Jara et al., 2001) showed that congen-
ital toxoplasmosis was significantly more common in children
whose mothers were born in these two countries: as will be dis-
cussed later, this may actually translate to low seroprevalence and
thus increased risk, but may also translate to increased environmen-
tal protozoan presence, and thus increased seroprevalence overall.
Older nationwide studies from Asia that also merit mention,
confirm that China exhibits one of the lowest prevalence rates
worldwide, being below 1% in the province of Shangdong (Chen
et al., 2005). Provincial data from Thailand have also shown varia-
tion, with prevalence in the Khon Kaen province in the north-east-
ern Thailand being extremely low (2% – interestingly an area with
a high HIV-prevalence) (Sukthana et al., 2000). A recent provincial
general population study in India also showed varying seropreva-
lence rates, ranging from 9.4% in Rajasthan to 48.2% in Kerala (Dhu-
mne et al., 2007). High prevalence was noted in Nepalese pregnant
women in a study chronologically marginally excluded from Table
3 (prevalence 55.4% (Rai et al., 1998), similar to that of the general
population reported in other older studies from this country).
Regarding Oceania, New Zealand data confirm a decrease in
prevalence rates compared with past studies (Cursons et al., 1982).
3.4. Africa
Compared with the numerous studies performed in the early
1990s in Africa, limited follow-up exists, even for the general pop-
ulation (Table 4). Apart from these studies, recent general popula-
tion data showed prevalence rates of 57.9% for Egypt (Hussein
et al., 2001), 58.4% for Tunisia (Bouratbine et al., 2001), 20.8% for
Nigeria (Uneke et al., 2005), and 21% for Mali in a blood-donor
sample (Maiga et al., 2001). The Nigerian study identified con-
sumption of rodents and contact with soil as seropositivity risk fac-
tors. Older studies in pregnant women or women of childbearing
age in Africa have been summarised previously (Tenter et al.,
2000) and have been utilised for individual countries in Fig. 1 when
no recent data were available. Of these, the studies that were per-
Table 4
Toxoplasmosis seroprevalence in Africa – females of reproductive age or pregnant.
Country (reference) Region Sample size (absolute number)
Burkina Faso (Simpore et al., 2006) Ouagadougou Pregnant (336)
Ivory Coast (Adou-Bryn et al., 2004) Abidjan Childbearing age (1,025)
Morocco (El Mansouri et al., 2007) Rabat Pregnant (2,456)
Sao Tome and Principe Nationwide Pregnant (499)
(Hung et al. (2007)
Sudan (Elnahas et al., 2003) Khartoum Pregnant (487)
and Omdurman
formed during the 1990s showed prevalence rates of 53.6% in Be-
nin (Rodier et al., 1995), 71.2% in Gabon (Nabias et al., 1998),
83.5% in Madagascar (Lelong et al., 1995) and 40.2% in Senegal
(Faye et al., 1998).
4. Discussion
In the present study, we aimed to summarise recent global
trends of toxoplasmosis seroprevalence. Of the numerous regional
studies included, some offer extended and reliable information
about certain countries, being nationwide or utilising large, repre-
sentative samples; on the other hand, for some countries the avail-
able information may be limited and of questionable reliability. The
absence of adequate data can be considered more significant for
countries where HIV is endemic, since HIV-seropositive individuals
have emerged as an important high-risk group for toxoplasmosis.
Does seroprevalence mean anything? It is a measure of the
accumulated exposure during a person’s lifetime in a particular so-
cial setting. One may thus treat the seropositivity rate as a quanti-
tative measure (although inherently inaccurate, still the only one
available) of the relative protection for a woman of this population
against primary infection during pregnancy. In settings with low
general population seroprevalence, the potential for a particular
woman to be infected is consequently low, but if she is infected
during pregnancy it will most likely be her primary infection, at
risk for abortion or congenital toxoplasmosis. On the other hand,
in settings with high general population seroprevalence, the
chances of a particular woman acquiring a primary infection dur-
ing pregnancy are low because she has most likely already been ex-
posed to T. gondii. However if she has not been exposed to the
parasite until childbearing age, the chances of her having a primary
infection during pregnancy are high. Obviously, surveillance with a
simple blood test early in pregnancy would benefit most non-im-
mune females living in a high-prevalence setting. The cumulative
results of this study underline that seroprevalence rates are evolv-
ing through time in a varying manner: a general trend towards
lower rates is observed in the Western world, but concern should
be raised by the potential effect of the increasing influx of
immigrants from developing, T. gondii endemic countries, in the
industrialised world. A typical example of the latter is the afore-
mentioned risk for congenital toxoplasmosis in the USA, related
to mothers being born in south-east Asia. Since humans are a
dead-end host for T. gondii this variation may not continue to sub-
sequent generations. On the other hand, immigration is also a dy-
namic phenomenon, the peak of which may not have been reached
yet; thus, continuing population influx may continuously alter
local seroprevalence rates in the developed world in the future.
General environmental conditions that theoretically allow for T.
gondii survival and thus increased human exposure and seroprev-
alence (hotter and moister climates) do not always apply; a typical
example is the varying seropositivity rates in south-east Asian
countries. Recognition of a rural predominance of seropositivity,
Seroprevalence in % Comments – risk factors identified
(95% confidence intervals)
25.3 (20.7–29.9) Prevalence slightly higher in HIV-positive
pregnant (28.5%) compared with
HIV-negative (20.2%)
60 (57.0–63.0)
50.6 (48.6–52.6) Related to contact with soil and lack of
knowledge on the disease
75.2 (71.4–79.0)
34.1 (29.9–38.3) Related to consumption of undercooked meat
 G. Pappas et al. / International Journal for Parasitology 39 (2009) 1385–1394
depicted in numerous studies in Tables 1–4, is not surprising, how-
ever it raises concerns. A rural population, due to its inferior socio-
economic status (in general or compared to the urban population
of a given country), may have worse access to the health sector
and may further exhibit an inferior level of health literacy, as ob-
served in certain other zoonoses with rural predominance.
The aim of the present study was to collect data from as many
areas of origin as possible. In order to achieve the widest geograph-
ical representation possible, selection criteria were not stringent,
limited mainly to excluding studies with less than 100 partici-
pants. There are numerous drawbacks to applying such a selection
process. In order for one to ensure that results are representative of
the actual seropositivity rates for the specific region where the
study was undertaken, one would expect a sophisticated study de-
sign and a systematic selection process of a large population sam-
ple, whereas many studies here only focus on a limited number of
women of reproductive age; hence the large confidence intervals
observed for some studies’ results. These studies should be viewed
cautiously since they may not accurately represent the seropositiv-
ity status of their respective areas. Furthermore, there is an ab-
sence of data about the sampled population in many of the
studies from Tables 1–4, and one can support that there may be
a risk of over-representation of those with most access to health
services, or (in the other direction) of over-representation of indi-
viduals considered as high-risk. Another troubling issue in collec-
tively evaluating what seroprevalence rates tell us is the
difference in diagnostic methods used. Seroprevalence rates may
vary widely, even doubling, according to the selected method’s
sensitivity, as was noted in studies incorporating more than one
diagnostic assay. The use of a different assay, however, does not ac-
count for most of the regional variations observed through time.
IgM seropositivity constituted a significant part of the overall sero-
positivity (noted in the respective ‘‘comments” column of the rel-
evant tables) in an extremely limited number of studies. One
could also support that if we were to meta-analyse these results,
most studies would be deemed ineligible; yet such meta-analysis
would be aim-less: all the included studies are essentially toxo-
plasmosis snapshots in a particular space and time. As snapshots,
they tell you a lot about the background (the specific population),
but the image may be blurred (inadequate selection criteria).
Only a few studies systematically evaluated risk factors for T.
gondii seropositivity and the results, as shown when available in
the last column of Tables 1–4, vary. A surprisingly absent risk fac-
tor in most studies is contact with cats. A European attempt by the
EUROTOXO project (Leroy and Hadjichristodoulou, 2005) to evalu-
ate risk factors found only limited data with contradicting results;
only one study was multi-national (Cook et al., 2000). This study
identified as major risk factors the consumption of undercooked
lamb or game meat and travel outside the developed world, while
contact with soil was a less significant risk factor and consumption
of undercooked pork and contact with cats did not significantly in-
crease risk. A possible explanation for the absence of risk in contact
with cats has been offered in another study evaluating health liter-
acy of pregnant women regarding toxoplasmosis (Jones et al.,
2003). In this study, the majority of the participants related
T. gondii acquisition to contact with cats, but only 30% was aware
of the risk imposed by eating undercooked meat. Thus pregnant
women may take the necessary precautions regarding contact with
pet cats during pregnancy and downplay the role of this contact in
T. gondii transmission. Whether health literacy is of a similar level
in the developing world (and whether it is feasible to be) is another
matter altogether.
Toxoplasma gondii seroprevalence is evolving worldwide, sub-
ject to complex environmental, socioeconomic and health-related
practices. Given the severe complications it can cause in newborns,
it is imperative that its distribution must be thoroughly surveyed.
1391
The differences in prevalence rates among the various countries
may help clarify the risk factors involved, as well as determine
the optimal health policies to be adopted by each state.
Acknowledgments
We are indebted to the anonymous reviewers for their insight-
ful comments that have significantly shaped this manuscript.
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