First Report of Toxoplasma gondii Prevalence in Tibetan Pigs in Tibet,China

Introduction

T oxoplasma gondii is an important intracellular protozoan parasite of zoonotic significance, affecting humans and animals worldwide (Tenter et al. 2000; Montoya and Liesenfeld 2004; Dubey 2009, 2010; Jittapalapong et al. 2011; Vujanić et al. 2011; Zhou et al. 2011; Elmore et al. 2012). In the People's Republic of China, it is estimated that approximately 7.9% of the population has been exposed to T. gondii, with an increasing incidence in recent years (Zhou et al. 2011). Generally, T. gondii infection in humans is asymptomatic (Dubey 2010), but primary infection in pregnant women may cause severe disease with vertical transmission to the fetus, leading to abortion, encephalitis, mental retardation, and blindness (Cook et al. 2000). More importantly, T. gondii infection can be fatal in immunocompromised patients, such as AIDS patients and organ transplant recipients (Montoya and Liesenfeld 2004).

The parasite can also severely threaten the health of pigs, and clinical signs in pigs vary from symptomless infections to death. Sow reproductive performance may also be affected, leading to heavy economic losses to the swine industry (Dubey 2009). Pig meat is an important foodstuff worldwide, and humans can acquire infections with T. gondii by ingesting undercooked pig meat containing tissue cysts. Surveys of seroprevalence of T. gondii infection in pigs have been reported throughout the world (Dubey 2009, 2010; Garcia-Bocanegra et al. 2010; Holec-Gasior et al. 2010), and there have also been surveys of T. gondii infection in pigs in several provinces of China in recent years (Suo et al. 2006; Zou et al. 2009; Huang et al. 2010; Zhou et al. 2010).

Tibetan pigs are mainly distributed in the Qinghai-Tibetan Plateau, and usually feed on wild plants outdoors. The typical characteristics of the Tibetan pig is its powerful musculature, and the fact that its entire body is covered by hard black hair (Li and Luo 1993; Zheng 1998). Tibetan pig meat is a sought-after delicacy, which is high in protein, with a tender texture, and rich in amino acids, and thus is an important source of protein for Tibetans. However, little is known about the prevalence of T. gondii in Tibetan pigs in Tibet. In view of this background, the objective of this survey was to estimate the seroprevalence of T. gondii infection in Tibetan pigs.

Materials and Methods

Results and Discussion

Table 1 shows the seroprevalence of T. gondii in 427 Tibetan pigs, with an overall prevalence of 22.72% (97/427). The distribution of seropositives was as follows: 26.36% (29/110) in the slaughter pigs, 23.58% (25/106) in the fattening pigs, 21.37% (28/131) in the growing pigs, and 21.13% (15/71) in the piglets. No seropositive pigs were detected among breeding boars and sows, possibly due to the limited serum samples. Antibodies (≥1:25) were found in 97 of 427 (22.72%) Tibetan pigs with MAT titers of 1:25 in 18, 1:50 in 10, 1:100 in 1, 1:200 in 28, 1:400 in 13, 1:800 in 9, and 1:1600 or higher in 18.

The overall T. gondii seroprevalence in Tibetan pigs in Nyingchi prefecture, Tibet, was lower than that reported in pigs in southern China's subtropical Hainan and Guangdong Provinces (Suo et al. 2006; Zhou et al. 2010). This is possibly related to different climate conditions in these areas. The average annual temperatures in Hainan, Guangdong, and Nyingchi are 23.8°C, 22.3°C, and 8.7°C, respectively, and the climate in Hainan and Guangdong Provinces is warmer and more humid than in Nyingchi prefecture. T. gondii oocysts are more prone to become infective and survive longer in warmer and more humid environments (Dubey 2010). Slaughter pigs had the highest T. gondii seroprevalence, compared with the seroprevalence in the fattening pigs, growing pigs, and piglets, possibly due to difference in their ages, although the difference was not statistically significant (p≥0.05, data not shown). Although the average annual temperature in Nyingchi prefecture is low, Tibetan pigs are usually raised in an outdoor environment and so have more potential contacts with felids and rodents, which are more common than in some other parts of China; they also are more likely to ingest food or water contaminated with T. gondii oocysts excreted by infected felids.

Previous investigations have shown that dietary habits play an important role in T. gondii infection in China (Zhou et al. 2011). T. gondii seroprevalence was higher in some ethnic groups who eat raw or undercooked meat (Zhou et al. 2011). Although the T. gondii seroprevalance in Tibetans in Nyingchi prefecture is not yet known, indigenous people in this area like to eat roast pork derived from Tibetan pigs, and this may result in a high T. gondii prevalence in Tibetans in this area.

In this study, we used the MAT for the detection of T. gondii seroprevalence in Tibetan pigs because of its high sensitivity and specificity for the diagnosis of latent toxoplasmosis compared to other serological tests (Dubey et al. 1995b). Previous studies have shown that the MAT is a specific technique for measuring T. gondii antibodies in pigs, and no cross-reaction was found when using the MAT for testing serum samples of T. gondii-negative pigs infected with other parasites and viruses (Dubey 1997, 2009, 2010).

In conclusion, the results of the present survey demonstrate that T. gondii is prevalent in Tibetan pigs, indicating the widespread contamination of the environment by T. gondii oocysts in Nyingchi, Tibet. This poses a significant public health risk in Tibet because T. gondii is an important zoonotic parasite, and the meat of Tibetan pigs is an important part of the Tibetan diet. Therefore, measures should be taken to prevent cat feces from contaminating the environment in Tibet. The results also provide foundational data for executing integrated strategies and measures to control toxoplasmosis in humans and animals in Tibet.