INTRODUCTION
China is home to 1 in 5 people on this planet and yet there are considerable gaps in the global scientific understanding of how infectious diseases in China are viewed in the global perspective. This review aims to focus specifically, on Toxoplasma gondii with respect to pregnant women in whom it has the potential to cause significant disease in the developing fetus and newborns. T. gondii is an obligate intracellular protozoan that belongs to the phylum Apicomplexa and probably infects all warm-blooded animals including humans (Tenter et al. Reference Tenter, Heckeroth and Weiss2000). Humans acquire Toxoplasma infection through consuming raw or undercooked meat, contact with cat feces, ingesting contaminated food or water, vertical transmission across placenta to fetus, or rarely through transplantation of a contaminated organ (Montoya and Liesenfeld, Reference Montoya and Liesenfeld2004). Infection in humans may cause various clinical manifestations. Adults with a normal immune system usually have few symptoms or mild and transient symptoms such as fever, malaise, and lymphadenopathy. Toxoplasmatic encephalitis and disseminated toxoplasmosis have been reported in AIDS, transplant recipients and people with immunodeficiencies due to immunosuppressive therapy or Hodgkin's disease (Luft and Remington, Reference Luft and Remington1992; Weiss and Dubey, Reference Weiss and Dubey2009). Immunocompetent women infected with T. gondii prior to conception have little or no risk of transmitting the infection to their fetus except those who become infected shortly before gestation (Vogel et al. Reference Vogel, Kirisits, Michael, Bach, Hosteter, Boyer, Simpson, Holfels, Hopkins, Mack, Mets, Swisher, Patel, Roizen, Stein, Stein, Withers, Mui, Eqwuaqu, Remington, Dorfman and Mcleaod1996). Vertical transmission occurs in most cases when a mother has a primary infection during pregnancy and this can present itself as either subclinical infection or congenital toxoplasmosis with a wide spectrum of severe manifestation in newborns or relapse later in life (Weiss and Dubey, Reference Weiss and Dubey2009; Hide et al. Reference Hide, Morley, Hughes, Gerwash, Elmahaishi, Elmahaishi, Thomasson, Wright, Williams, Murphy and Smith2009).
The global status of Toxoplasma seroprevalence in pregnant women has recently been summarized and evaluated by Pappas et al. (Reference Pappas, Roussos and Falagas2009). The incidence of congenital toxoplasmosis varies between 1 and 10 per 10 000 live births in western countries: 0·8 /10 000 births in the United States (Guerina et al. Reference Guerina, Hsu, Meissner, Maguire, Lynfield, Stechenberg, Abroms, Pasternack, Hoff, Eaton and Grady1994), 3·4/10 000 in the United Kingdom (Gilbert et al. Reference Gilbert, Tan, Cliffe, Guy and Stanford2006) and 4/10 000 in Denmark (Lebech et al. Reference Lebech, Andersen, Christensen, Hertel, Nielsen, Peitersen, Rechnitzer, Larsen, Nørgaard-Pedersen and Petersen1999). Raw or undercooked meat was found to be the main risk factor in a European multicentre case-control study (Cook et al. Reference Cook, Gilbert, Buffolano, Zufferey, Petersen, Jenum, Foulon, Semprini and Dunn2000) as well as in another study from the United States (Jones et al. Reference Jones, Dargelas, Roberts, Press, Remington and Montoya2009).
With a population of 1·34 billion encapsulated within the world population of 6·8 billion, 1 in 5 people live in China. However, epidemiological knowledge regarding the prevalence and risk of associated maternal Toxoplasma infection is limited in China. The effect of this is to hamper efforts towards global estimation of disease burden, national evaluation of the current situation in China and the formulation of effective health policies nationally and globally. Although studies have been conducted in China, these are typically published in Chinese and consequently are largely inaccessible to the global scientific community whose international scientific language is English. To render this data more accessible, this review aims to gain a collective estimate of the nationwide seroprevalence of T. gondii infection in Chinese pregnant women, to review the prevalence trends, sources of risk and clinical manifestations in mothers and their fetuses/newborns. Thus providing an update on the current status of Toxoplasma prevalence in pregnant women in this major component of the global population.
SEARCH STRATEGY AND SELECTION CRITERIA
The primary search for literature was performed in PubMed and the ISI Web of Knowledge with keywords ‘congenital toxoplasmosis’ OR ‘Toxoplasma infection in pregnant women’ AND ‘China’. A search of JSTOR was conducted for outdated publications. Databases of Chinese publications, CNKI (China National Knowledge Infrastructure, http://www.cnki.net) and Wanfang (http://www.wanfangdata.com.cn), were subsequently searched for more articles with data on nationwide or provincial seroprevalence in China; the keywords for searching were ‘Toxoplasma infection’ AND (pregnant women’ OR ‘pregnancy’). The majority of these latter papers were published in Chinese and, therefore, probably not generally accessible to the English-speaking scientific community. A comprehensive search has been conducted up to December 2010 and relevant articles and book chapters, falling within our specified criteria (see below) both in English and Chinese are referenced.
For seroprevalence data in China, articles that were published in the last 2 decades, i.e. from January 1990 through December 2010, were retrieved. For a study to be included in the discussion, the minimum sample size was selected as 100. Studies that focused on pregnant subpopulations with potentially biased obstetric histories or that employed biased sampling were excluded from our seroprevalence estimations.
SEROPREVALENCE
Seroprevalence in China
The national survey of parasitic disease conducted by the Ministry of Health of China from 2001 to 2004 provides the latest prevalence data of general Toxoplasma infection in China. A seropositivity rate of 7·97% was measured for the general population from a sample of 47 444 people (Xu et al. Reference Xu, Chen, Sun, Cai, Fang, Wang, Liu, Li, Feng and Li2005). This figure is lower than seen in many serological studies elsewhere (Jones et al. Reference Jones, Kruszon-Moran, Sanders-Lewis and Wilson2007). To our knowledge, however, there has been no nationwide epidemiological study or seroprevalence investigation of Toxoplasma infection in Chinese pregnant women. Nevertheless, serological testing for Toxoplasma-induced antibodies has been available to pregnant women for antenatal care or counselling in some hospitals and clinical laboratories in China. In reports of studies we retrieved which were conducted over the last 2 decades, a total of 56 have documented the seropositivity rate of women whose serum samples were collected during pregnancy. These were predominantly tested by ELISA to detect Toxoplasma-specific IgG (Table 1). The studies cover a wide range of districts including 20 of the total of 34 provinces (municipalities) in China.
Table 1. Seroprevalence of Toxoplasma gondii in Chinese pregnant women (data collected from publications from 1990 to 2010)
Note:
Period: during which sera samples were collected from pregnant women, documented in the referred study.
*: the publication year of the study when no specific period is documented in it.
Age: na, the age range of women that attended in the study is not mentioned.
Assay: applied in the study for determination of past infection. IHA: indirect hemaglutination; ELISA: enzyme-linked immunosorbent assay; CLIA: chemiluminescent immunoassay. For the studies applying IHA, a titre of greater than 1:64 is generally considered as positive; for the rest, only one of the 44 studies using ELISA reported a concrete cut-off value of >35I U/ml, highlighted with
† and the only CLIA study reported a cut-off value of >6I U/ml.
TORCH: prenatal testing for infection of Toxoplasma, Rubella, Cytomegalovirus, Herpes simplex; Y=data from TORCH test; N=data from test specifically for Toxoplasma infection.
The reported seroprevalence, ranging from 0·17% (Li et al. Reference Li, Zhang and Yuan2001) to 31·06% (Lin et al. Reference Lin, Liao, Liao, Chen, Kuo and He2008), displays considerable variance among districts, even among studies in the same region (Table 1). Therefore, no single provincial or district survey could reflect the nationwide seroprevalence in pregnant women. Although most of the studies included in this review (43 out of 56) reported seropositivity within the range of 0–10% and nearly half of them (20 of 43) reported rates of lower than 5%. It is notable that the 2 multi-year studies, both with largest sample sizes (1 of 18 127 from Hubei and 1 of 10 939 from Zhejiang), both reported seroprevalence rates around 10% in women during pregnancy (Liu and Yao, Reference Liu and Yao2003; Suo and Yao, Reference Suo and Yao2009). Though ranging widely between 0 and 10%, seroprevalence data from China show a relatively low level compared with seroprevalence reported from other countries (both neighbouring and cross-continental) most of which had prevalences above 10% with some up to 60% and beyond (Pappas et al. Reference Pappas, Roussos and Falagas2009). This low seroprevalence in Chinese pregnant women suggests that there might be only a small proportion of women who are immune to Toxoplasma infection prior to gestation leaving the majority to be susceptible to infection during pregnancy.
Infection has been thought to be more common in warmer and humid areas or at lower altitudes (Elsheikha, Reference Elsheikha2008). So far, however, we found no studies or data that investigate this potential influence on T. gondii seroprevalence in China. It could be a very important project to be carried out as conditions can vary very widely across the large expanse occupied by China. Such results will also be very useful for understanding the true T. gondii infection status of pregnant women and may influence regional healthcare policy.
Seroprevalence trends
Among the studies that had collected samples for more than 5 years, only 1 provided annual data on cases and seroprevalence (Suo and Yao, Reference Suo and Yao2009). Each year from 2001 to 2007, pregnant women in Wuhan were tested for Toxoplasma-specific antibodies in serum by ELISA (IgM and IgG) at the time of their prenatal examination (Table 2) (Suo and Yao, Reference Suo and Yao2009). Overall, the proportions of seropositive mothers (either IgM and IgG positives or IgG only) showed a slightly increasing trend. No significant difference was observed between any individual years except that the prevalence of the IgG-only positives in 2007 were significantly increased when compared with the figures for 2001.
Table 2. The yearly Toxoplasma-specific seropositivity in pregnant women reported from Wuhan during 2001∼2007 by Suo and Yao (Reference Suo and Yao2009)
* The rate showed no significant difference compared with that of any previous studied year.
† The seropositive rate is significantly higher compared with that of 2001, P<0·05.
For the general population in China, T. gondii seropositivity was reported to be 4·86% (n=61 494) from the 1983∼1986 nationwide survey (Cui, Reference Cui1991) and a higher rate of 7·97% (n=47 444) was found in the 2001∼2004 nationwide survey (Xu et al. Reference Xu, Chen, Sun, Cai, Fang, Wang, Liu, Li, Feng and Li2005) showing an upward trend. By comparison, seroprevalence of T. gondii infection in China, either for the general population or for the subgroup of pregnant women, in these Chinese studies has not shown the decreasing trend that has been reported in the USA (Jones et al. Reference Jones, Kruszon-Moran, Sanders-Lewis and Wilson2007) or some other western countries during recent years (Pappas et al. Reference Pappas, Roussos and Falagas2009). The reasons for this will be discussed in a later section of this paper.
SEROLOGICAL DIAGNOSIS OF ACUTE INFECTION DURING PREGNANCY
Women that show seronegativity for Toxoplasma-induced antibodies before or early in pregnancy are at risk of acquiring acute infection and passing it to their fetuses transplacentally. Rarely, transplacental transmission can also occur in chronically infected women who are immunocompromised due to HIV/AIDS or immunosuppressive treatment and experience re-activated infection (Montoya and Remington, Reference Montoya and Remington2008). Most pregnant women do not show obvious symptoms when infected acutely (Boyer et al. Reference Boyer, Holfels, Roizen, Swisher, Mack, Remington, Withers, Meier and Mcleod2005) and, therefore, serological testing is crucial to the diagnosis of acute infection during pregnancy (Montoya and Remington, Reference Montoya and Remington2008).
Immunological testing for IgM seropositivity
For clinical diagnosis, as practiced by most of the Chinese studies included here, seropositivity of IgM is interpreted as a recent or acute infection. This is because Toxoplasma-specific IgM usually develops early during primary infection and generally decreases to below the detection cutoff within months after infection (Jenum and Stray-Pedersen, Reference Jenum and Stray-Pedersen1998). However, T. gondii-specific IgM can sometimes persist for years, giving rise to false-positive diagnoses of acute infection when no additional tests for T. gondii-specific IgG were conducted, prior to conception or in the first trimester, to exclude women already infected before pregnancy (Jenum et al. Reference Jenum, Stray-Pedersen, Melby, Kapperud, Whitelaw, Eskild and Eng1998; Montoya, Reference Montoya2002). Essentially, a positive specific-IgM in a single serum sample can be interpreted as a true-positive result of recent or acute infection, a true-positive result after an infection acquired in the distant past or a false-positive result (Montoya, Reference Montoya2002). The data from studies that only report IgM seropositivity are not valid and, hence, excluded from this discussion of the primary Toxoplasma infection during pregnancy in Chinese women.
Combining immunological testing for IgM, IgG and CAg
Serological evidence of acute infection by Toxoplasma, as described by Lebech et al. (Reference Lebech, Joynson, Seitz, Thulliez, Gilbert, Dutton, Ovlisen and Petersen1996), requires (i) seroconversion, (ii) a significant increase of both specific-IgG titre (>3-fold) and dye test titre (⩾4-fold) and (iii) the presence of specific-IgM and a high IgG titre (dye test result, ⩾300 IU/ml). However, this standard is hardly ever adopted outside of reference laboratories. No one study in our survey has consistently applied this standard to the diagnosis of primary pregnant infection. Studies that combined tests of IgM, IgG and CAg in diagnosis, though limited, are the most informative since they provided data that could be measured against the current Chinese serological standard for diagnosis of acute Toxoplasma infection (established by the Forth National Toxoplasmosis Symposium) (Gan, Reference Gan2001): (i) specific-IgG positivity and a significant increase of specific-IgG titre (⩾4-fold) in 2 weeks, (ii) specific-IgM (IgA) positivity and (iii) detection of CAg. Acute infection can be determined when 2 of the former conditions are met.
We retrieved 9 studies that used these combined seropositivity data (Table 3). As none of these studies have collected follow-up samples to detect the change in specific IgG titre, a serum sample can be assumed to be acutely infected only when both specific IgM and CAg show positivity. The rates of both IgM and CAg positivity (shown in the column of ‘IgM+, CAg +’ in Table 3) are within 0·3% in most studies (6 of 9). The 3 higher outliers (0·5%, 0·84% and 1·2%) demonstrate that there may be some local variation in prevalence. The average seropositivity of IgM combined with CAg is 0·33% throughout the 9 studies. Therefore, around 0·3% of the studied women can be considered to be diagnosed with acute infection during pregnancy according to the national standards currently used in China. This is an estimate of the level of incidence of infection in pregnant women. A comparable incidence (0·19%) was reported from a nationwide prospective study of 35 940 pregnant women in Norway (Jenum et al. Reference Jenum, Stray-Pedersen, Melby, Kapperud, Whitelaw, Eskild and Eng1998) where the seroprevalence of Toxoplasma infection is 10·9% among pregnant women and is approximately comparable to the seroprevalence in Chinese pregnant women estimated from our studies.
Table 3. Seropositivity based on a combination of tests for Toxoplasma-specific IgG, IgM and CAg in pregnant women
Note: IgM+, IgG+, CAg+, refer to the seropositivity in the detection of Toxoplasma-specific IgM, IgG and circulating antigen, respectively; for each row, the seropositivity rate shown in the column ‘IgM+ CAg+’ is derived from the addition of the rate in the column of ‘IgM+, CAg+, IgG−’ and the rate in the column of ‘IgM+, CAg+, IgG+’.
RISK FACTORS
Several potential risk factors associated with Toxoplasma infection have been investigated in Chinese pregnant women. According to a study, from Changchun (in the north of China) in 2008, major risk factors identified by multivariate analysis include eating raw or undercooked meat, unwashed raw vegetables or fruit, contact with cats, living in rural areas and low educational level (Liu et al. Reference Liu, Wei, Gao, Jiang, Lian, Yuan, Yuan, Xia, Liu, Xu and Zhu2009) (Table 4).
Table 4. Risk factors associated with Toxoplasma infection in Chinese pregnant women as reported by Liu et al. (Reference Liu, Wei, Gao, Jiang, Lian, Yuan, Yuan, Xia, Liu, Xu and Zhu2009)
Consumption of raw or undercooked meat
Consumption of raw or undercooked meat was found to be a strong risk factor with an odds ratio (OR) of 5·69 (95% CI: 1·14–16·23) as mentioned in the study by Liu et al. (Reference Liu, Wei, Gao, Jiang, Lian, Yuan, Yuan, Xia, Liu, Xu and Zhu2009) and consistent with the findings from other countries (Kapperud et al. Reference Kapperud, Jenum, Stray-Pedersen, Melby, Eskild and Eng1996; Cook et al. Reference Cook, Gilbert, Buffolano, Zufferey, Petersen, Jenum, Foulon, Semprini and Dunn2000; Jones et al. Reference Jones, Dargelas, Roberts, Press, Remington and Montoya2009). This food-borne feature of T. gondii infection may partially explain the relatively low seroprevalence reported in China as consumption of raw or undercooked meat is not as common in the Chinese daily diet as in some Western diets. With regard to the kinds of meat consumed, Li and Wu (Reference Li and Wu2002) reported that subjects favouring duck and beef were associated with higher seropositivity than those with a preference for other kinds of meat including pork, lamb and chicken. However, such details may vary by region, dependent on local dietary customs. As reported in western countries, undercooked lamb and pork are major dietary risk factors in Norway, with beef and lamb being major factors in France and the United States (Kapperud et al. Reference Kapperud, Jenum, Stray-Pedersen, Melby, Eskild and Eng1996; Cook et al. Reference Cook, Gilbert, Buffolano, Zufferey, Petersen, Jenum, Foulon, Semprini and Dunn2000; Jones et al. Reference Jones, Dargelas, Roberts, Press, Remington and Montoya2009). Poor kitchen hygiene and improper handling of raw meat may also lead to cross-contamination of foods resulting in additional risk beyond meat consumption (Kapperud et al. Reference Kapperud, Jenum, Stray-Pedersen, Melby, Eskild and Eng1996; Cook et al. Reference Cook, Gilbert, Buffolano, Zufferey, Petersen, Jenum, Foulon, Semprini and Dunn2000).
Contact with or ownership of cats or dogs
Contact with cats was found with the highest odds ratio, 8·23 (95% CI 0·85–57·63) in Liu's study (Liu et al. Reference Liu, Wei, Gao, Jiang, Lian, Yuan, Yuan, Xia, Liu, Xu and Zhu2009) (Table 4) although there are discrepancies between this study and the conclusions of some studies from different countries (Kapperud et al. Reference Kapperud, Jenum, Stray-Pedersen, Melby, Eskild and Eng1996; Cook et al. Reference Cook, Gilbert, Buffolano, Zufferey, Petersen, Jenum, Foulon, Semprini and Dunn2000). Occasional contact with or ownership of cats may not necessarily be a risk factor, whereas frequent exposure to feline feces or neglect of preventive measures (i.e. not washing hands or wearing gloves) may increase the risk of infection to an appreciable level. In the latest study from the United States, Jones et al. (Reference Jones, Dargelas, Roberts, Press, Remington and Montoya2009) indentified that having 3 or more kittens increased the risk while having 1 or 2 did not. Pets and livestock kept together with cats are highly exposed to oocysts in the feces of infected cats, thus becoming another potential source of infection by transportation of oocysts into households. Evidence for this is presented by Huang who studied a sample of 2076 pregnant women in Guangxi (Southwest of China) and found a significantly higher seropositivity rate in pregnant women owning dogs compared with those with no dogs in houses (Huang, Reference Huang1996). In a study from Panama, dog contact was observed with a risk ratio even higher than that of the above study. Contact with cat and dog fur contaminated with cat feces was suggested as a vector for transmission to people without careful preventive measures (Frenkel et al. Reference Frenkel, Hassanein, Hassanein, Brown, Thulliez and Quintero-Nunez1995). A recent study in Lanzhou (Northwest China) reinforces this view by demonstration of a high prevalence of Toxoplasma infection in dogs (Wu et al. Reference Wu, Huang, Fu, Liu, Chen, Chen, Yuan, Zhou, Weng, Zhu and Ye2011).
Consumption of unwashed raw vegetables or fruits and farming as an occupation
Widespread infectious oocysts also contribute to a range of potential risk factors for T. gondii infection, including contact with soil, eating unwashed contaminated vegetables and fruits, and drinking unpasteurized milk or untreated surface water. Consumption of unwashed raw vegetables and fruits was found to be associated with Toxoplasma infection during pregnancy (ORs: 3·85; 95% CI: 1·06–9·63) by Liu et al. (Reference Liu, Wei, Gao, Jiang, Lian, Yuan, Yuan, Xia, Liu, Xu and Zhu2009). Gardening or contact with soil has been identified as a risk factor in several case-control studies (Kapperud et al. Reference Kapperud, Jenum, Stray-Pedersen, Melby, Eskild and Eng1996; Cook et al. Reference Cook, Gilbert, Buffolano, Zufferey, Petersen, Jenum, Foulon, Semprini and Dunn2000). In China, farmers are the population with the most frequent contact with soil and also may have significant contact with unpasteurized milk. A recent study, showing high prevalences of infection in dairy goats, suggests a potential risk of a transmission route of Toxoplasma via unpasteurized milk (Zhao et al. Reference Zhao, Zhang, Lei, Shang, Cao, Tian, Li, Xu, Yao, Chen and Zhu2011). Significantly higher seropositivity has been reported in pregnant women working on farms than with other occupations (Yu et al. Reference Yu, Yu, Pan, Zhang and Xing1994; Sun et al. Reference Sun, Liu, Song, Zhang and Ren2006) and being an agricultural worker has been identified as promoting a higher risk of maternal infection in Taiwan (Hu et al. Reference Hu, Chen and Su2006). Therefore, women on farms are suggested to be at an increased risk of Toxoplasma infection during pregnancy.
Living in rural regions
Living in rural or suburban regions is another risk factor for Chinese pregnant women and is supported by most studies that have available residence information of the women (Yu et al. Reference Yu, Yu, Pan, Zhang and Xing1994; He et al. Reference He, Wu and Wang1999; Liu and Li, Reference Liu and Li2001; Wu, Reference Wu2004; Li, Reference Li2007; Xu, Reference Xu2007; Liu et al. Reference Liu, Wei, Gao, Jiang, Lian, Yuan, Yuan, Xia, Liu, Xu and Zhu2009). This is consistent with the higher seroprevalence of Toxoplasma infection recorded in rural areas based on a global perspective (Pappas et al. Reference Pappas, Roussos and Falagas2009). Residence is not a univariate factor; in China rural or suburban residence is generally associated with poorer sanitary facilities, more frequent contact with soil or animals and drinking unpasteurized or unboiled water.
Age and educational level
Two studies also suggest that women in China of lower educational level are more likely to acquire infection during their pregnancy (Sun et al. Reference Sun, Liu, Song, Zhang and Ren2006; Liu et al. Reference Liu, Wei, Gao, Jiang, Lian, Yuan, Yuan, Xia, Liu, Xu and Zhu2009). Liu and coworkers found that pregnant women who had not attended school were at higher risk of infection than women with schooling (Liu et al. Reference Liu, Wei, Gao, Jiang, Lian, Yuan, Yuan, Xia, Liu, Xu and Zhu2009). Even the pregnant women who obtained middle school education showed a significantly higher seroprevalence of Toxoplasma compared to those with higher education (Sun et al. Reference Sun, Liu, Song, Zhang and Ren2006). Both studies suggest health education as an effective intervention of Toxoplasma infection in pregnant women.
Age, on the other hand, is not found to be associated with Toxoplasma infection in Chinese pregnant women (Wu, Reference Wu2004; Sun et al. Reference Sun, Liu, Song, Zhang and Ren2006; Ji et al. Reference Ji, Wang, Wang, Ruan and Sun2007) although the general view is that the prevalence of Toxoplasma infection increases with age (Elsheikha, Reference Elsheikha2008).
MANIFESTATION IN MOTHERS AND FETUS/NEWBORNS
Transplacental transmission can cause miscarriage, stillborn fetuses, neonatal death, or fetal/newborn abnormalities. Pregnant women who are infected with T. gondii usually have absent or only mild symptoms; fever, malaise, extreme fatigue, myalgia, headache and lymphadenopathy were recorded as symptoms in maternal infection (Zhang et al. Reference Zhang, Zhang, Hao, Lv, Fu and Wang1996; Jenum et al. Reference Jenum, Stray-Pedersen, Melby, Kapperud, Whitelaw, Eskild and Eng1998; Boyer et al. Reference Boyer, Holfels, Roizen, Swisher, Mack, Remington, Withers, Meier and Mcleod2005). However, clinical manifestations in infected newborns can be severe, including chorioretinitis, strabismus, blindness, epilepsy, psychomotor or mental retardation, anaemia, jaundice, rash, petechiae of thrombocytopenia, encephalitis, pneumonitis, microcephaly, intracranial calcification, hydrocephalus, diarrhoea, and hypothermia (Remington et al. Reference Remington, Mcleod, Wilson, Desmonts, Remington, Klein, Wilson, Nizet and Maldonado2010). The incidence and severity of congenital infection mainly depend on the onset of maternal infection during pregnancy. Infection acquired in later gestation is more likely to result in vertical transmission; however, severe manifestation is more related to the infection in an early stage of pregnancy (Dunn et al. Reference Dunn, Wallon, Peyron, Petersen, Peckham and Gilbert1999; Montoya and Remington, Reference Montoya and Remington2008).
CONCLUSIONS
Serological data, collectively assembled in our study, show a relatively low prevalence of Toxoplasma infection among pregnant women in most areas of China compared to the global level. Despite the tendency towards lower seroprevalence in many western countries, no such decrease has been observed in the last 20 years in China. A nationwide survey or sophisticated study with large and representative sampling is therefore required imminently to establish an authentic prevalence and incidence of maternal Toxoplasma infection in China on which an efficient health promotion policy can be defined. For individual pregnant women at risk, adequate serum samples and clinical information for confirmation of seroconversion are essential to improve the diagnostic accuracy of primary infection and to facilitate follow-up for cases of maternal infection as well as congenital toxoplasmosis.
Maternal infection and congenital toxoplasmosis can be largely prevented if women and their health-care providers are better educated about Toxoplasma infection and the avoidance of risk. Pregnant women should avoid eating or tasting raw or undercooked meat. Preventive measures are suggested for pet owning, gardening and farming (i.e. wearing gloves and washing hands frequently). Kitchen hygiene should be improved, including avoiding drinking contaminated liquids or consuming inadequately washed vegetables and fruits. Education aimed at prevention is the most accessible and cost-effective method (Elsheikha, Reference Elsheikha2008) especially in China where seroprevalence is low and any screening programmes would be considerably expensive if adopted for large populations of non-immune pregnant women. Once prevention fails and acute infection occurs during pregnancy, treatment should be encouraged to reduce the transmission or the clinical severity of fetal infection. Effective prevention and treatment require the physician to have knowledge about the manifestations and treatment of toxoplasmosis as well as a general public awareness of the risks and consequences of maternal and congenital Toxoplasma infection.
Conflicts of interest
We declare that we have no conflicts of interest.
ACKNOWLEDGEMENTS
This work was supported by grants from National Basic Research Program (973 project, #2010CB530000), the National Special Research Programs for Non-Profit Trades (Agriculture) (Grant No. 200803017), and the Stanley Medical Research Institute (#07R-1002). The authors thank Dr Robert Owen for his critical comments and help with preparation of the manuscript. We also thank the colleagues from our laboratories who provided critical comments and suggestions during the period we were working on the review article.
