T. gondii causes a high disease burden in humans and is a source of economic losses to livestock industries18,19. The increased seroprevalence in T. gondii in the Chinese human population together with a notable increase in number of immune-compromised patients suffering cancer and HIV make this opportunistic parasitic disease an important public health challenge to China10,20. The aims of our study were to determine the seroprevalence of T. gondii in pregnant women and in main meat-producing animals from different regions of China and to examine the potential link between the seroprevalence in humans and livestock.

A total of 72 publications on pregnant women and 200 publications on livestock were included in the dataset. The selected eligible studies for pregnant women covered all seven regions of China. However, data gaps were identified for cattle and small ruminant from Southern China and limited eligible studies were found in ducks, goose and donkeys. These data gaps called for the use of a hierarchical model in which the fitted national (logit-transformed) seroprevalence and the fitted between-region variance could be used to estimate the seroprevalence for regions where no data were available. In all of the eligible publications, seroprevalence data were reported without correction for test sensitivity and specificity. Correctly determining disease status largely depends on the sensitivity and specificity of the serological test. The chance of having a false result can be considerable and the prevalence of test positives may deviate from prevalence of truly infected individuals21. For that reason, data on test characteristics were additionally collected from literature. In our study, most of the selected studies dealing with the T. gondii IgG seroprevalence in pregnant women and many of the studies on livestock used kits with unknown Se and Sp. Moreover, different values of Se and Sp were reported in literature for the same kit to detect T. gondii antibodies in animals. This variation may be due to different characteristics of the reference population (e.g. different levels of exposure to additional pathogens or other biological confounders) and the sampling strategies used in the validation procedures22. Thus, it is inappropriate to assume that the test characteristics are constant over populations23. Therefore a Bayesian approach to estimate the true seroprevalence of T. gondii infection was used. In this approach, prior information about test characteristics was incorporated into the analysis as random variables described using probability distributions in the modelling process. They are therefore not fixed, constant values over different populations. Because insufficient convergence occurred from the initial runs of the model, we used truncated beta distributions for the priors of Se and Sp (Table 3) assuming that the values of Se and Sp of used kits were at least larger than 0.1. After truncation of the distribution of priors, the models for both pregnant women and livestock showed good convergence. In general, the Bayesian hierarchical model estimates for T. gondii true seroprevalence in pregnant women and livestock were similar to the non-modelled apparent seroprevalence but with wider 95% posterior probability intervals. In our opinion, the seroprevalences based on the Bayesian hierarchical model provide the most appropriate estimates of seroprevalence, as regional variation and information on test characteristics are taken into account. The uncertainty present due to the use of insufficiently validated diagnostic kits remains unnoticed when apparent prevalences are reported, but is reflected in the wide posterior probability intervals from the Bayesian hierarchical model. Moreover, the Bayesian hierarchical model allowed us to impute seroprevalence estimates for regions that lacked data.

The true seroprevalence from the Bayesian hierarchical model in Chinese pregnant women obtained from this study ranged from 2.4% to 5.0% in all seven regions of China. Even though the results were low compared to some countries24, this also means that the majority of pregnant women in China are susceptible to a primary infection and their babies to congenital toxoplasmosis. The true seroprevalence was also lower than the overall seroprevalence in Chinese cancer patients reported from a systematic review (21%)25. This is however not a surprise, as cancer patients are generally older than pregnant women and thus have experienced more time at risk of infection.

The results of true seroprevalence for livestock showed that T. gondii infection is wide spread in meat-producing animals in different regions of China. The median of the true seroprevalences from seven regions of China in pigs (24%) was significantly higher than in cattle (9.5%), but it was not significantly higher than in chickens (20%) and small ruminants (20%). In addition, results showed that the regional variation of true seropevalences in chickens (from 11% to 24%) was strongly correlated with variation in small ruminants (Spearman correlation = 0.86, p = 0.01). Chickens are considered good indicators of T. gondii contamination in the environment, as they become infected mostly by ingesting T. gondii oocysts-contaminated soil26. Therefore, regional variability may indicate variation in environmental contamination with oocysts. In China, sheep is one of the major grazing livestock and they are grazing rotationally by following a predetermined range and routine in pastures27. The outdoor access of these animals means that, similarly to chickens, environmental contamination with oocysts is also major risk of infection small ruminants, which may explain the correlation between regional variations of seroprevalence in these species. However, seroprevalence is also strongly associated with farming system with the seroprevalence of T. gondii infection higher in outdoor farming systems than in indoor farming systems28,29,30. In addition, the age of animals, number of cats present in the farm, and feed source are considered as important risk factors associated with T. gondii seroprevalence31,32. Farming system and exposure to risk factors are likely to also vary by region, and may be correlated for the different species (e.g. in regions with a lot of backyard poultry, backyard farming may also be more common for small ruminants). Therefore, to better understand regional variability in seroprevalence it is important to collect and analyse data taking into account exposure to potential risk factors that are related to T. gondii infection in future studies. This type of information was lacking from most of the publications included in the review.

With the exception of cattle and horses, the risk of human T. gondii infection via undercooked meat likely increases with a higher seroprevalence in the animal species. Nonetheless, no strong regional relationship between the true seroprevalence in livestock and pregnant women was found. This may be due to the limited data points in our analysis (7 regions). More importantly, the total meat consumption volume and species-specific preparation habits play crucial roles for the relative attribution of different meat-producing animals on a population level33. In China, pork is the dominant type of meat consumed by the whole population, except for some religious groups, followed by poultry, beef and lamb, the average annual consumption volumes in 2015 were 20.1, 8.4, 1.6 and 1.2 kg respectively34. The highest seroprevalence and total amount of consumption make pork a good potential source of human infections. Additionally, people living in Yunnan, Guizhou and Sichuan provinces eat raw or undercooked pork and beef in their tradition, and the seroprevalence in the ethnic groups from these provinces were found higher than the general population35. In our study, the true seroprevalence in pregnant women from the same region was found to be one of the highest 4.8% (1.7–14%). Due to the diversification of food sources and preparation habits among different regions and ethnic groups, the risk of human infection can vary accordingly. To determine the risk of humans to become infected via the different meat-producing animals, information on prevalence in livestock and meat consumption needs to be combined in a quantitative risk assessment36.

In conclusion, the seroprevalence and geographical distribution of T. gondii infection in pregnant women and meat-producing animals in China were systematically reviewed and summarized. The results obtained from Bayesian hierarchical models showed that T. gondii seroprevalence ranged from 2.4% to 5.0% in pregnant women, pigs (20–33%) and chickens (11–24%) had higher true seroprevalence than small ruminants (15–24%) and cattle (6.8–12%). Studies to better evaluate the performance of kits are needed to get more accurate estimates of T. gondii seroprevalence in humans and animals. More detailed insight in the geographical distribution of T. gondii prevalence in humans and livestock animals can be helpful for making effective intervention strategies to reduce the burden of this disease in the Chinese population. However, the risk of meatborne T. gondii infection in humans is not only depending on the prevalence in meat-producing animals but also on consumed volumes and food preparation habits. Therefore the results obtained from this study should be used to determine meatborne toxoplasmosis risk by using a quantitative microbial risk assessment of T. gondii infection in China.