Seroprevalence of Toxoplasma gondii in Beef Cattle and Dairy Cattle in Northeast China

Introduction

T oxoplasma gondii is an obligate intracellular protozoan parasite affecting almost all species of warm-blooded animals and humans worldwide (Tenter et al., 2000; Dubey, 2010). T. gondii infection is usually asymptomatic, but infection occurring in pregnant animals or humans may cause early embryonic death and resorption, fetal death and mummification, abortion, stillbirth, and neonatal death (Cook et al., 2000; Morley, et al., 2005; Dubey, 2010). Toxoplasmosis is considered an important foodborne parasitic zoonosis (Zhou et al., 2008). Humans can get infected with T. gondii by ingestion of raw beef, although this transmission is not considered important because cattle are considered a poor host for T. gondii (Dubey, 2010).

Numerous serologic surveys on the prevalence of T. gondii in beef cattle and dairy cattle have been carried out in other countries (Bekele and Kasali, 1989; Samad et al., 1993; Klun et al., 2006; Bártová et al., 2009; Inpankaew et al., 2010; Schoonman et al., 2010; Frazão-Teixeira and de Oliveira, 2011; Shahiduzzaman et al., 2011). Several surveys have shown that T. gondii infection in beef cattle and dairy cattle was common in other provinces of China (Mo et al., 1993; Cao 2000; Gu et al., 2005; Mi et al., 2007), but there have been no reports of T. gondii infection in beef cattle and dairy cattle in Heilongjiang Province, northeastern China. Heilongjiang Province is one of the most important producers of milk and beef in China, having the largest number of beef cattle and dairy cattle, and producing about one-sixth of both milk and beef in the whole nation.

In view of this background, the objective of the present investigation was to estimate the seroprevalence of T. gondii in beef cattle and dairy cattle in Heilongjiang Province, northeastern China, which would provide a baseline dataset for the prevention and control of T. gondii infection in beef cattle and dairy cattle in this province, and for assessing the potential risk for human infection.

Methods

Results

In the present investigation, 46 out of 1803 serum samples (2.6%) were positive for T. gondii using IHA test (Table 1), with the following distributions: 1.2% in intensively raised beef cattle, 1.6% in intensively raised dairy cattle, 3.6% in semi-intensively raised beef cattle, and 3.3% in semi-intensively raised dairy cattle (Table 2). The overall seroprevalence in beef cattle was 3.0%, and in dairy cattle it was 2.3%. Antibodies to T. gondii in beef cattle and dairy cattle populations varied from 0 to 5.3% among different regions of Heilongjiang Province (Table 1). The seroprevalence of T. gondii in adult beef cattle, adult dairy cattle, beef calves, and dairy calves were 3.1%, 2.3%, 2.8%, and 2.1%, respectively (Table 2). In male beef cattle, the seroprevalence of T. gondii was 2.5%, and it was 3.4% in females (Table 2).

Discussion

Our previous surveys showed that the seroprevalence of Neospora caninum infection in dairy cattle in Heilongjiang Province was high (14.6%) (Wang et al., 2010), but there had been no survey of T. gondii infection in beef cattle and dairy cattle in this unique northeast province. The surveys of T. gondii infection in beef cattle and dairy cattle have been conducted in many countries, and the seroprevalence in beef cattle was 76.3% in Serbia (Klun et al., 2006), 47.7% in Brazil (Frazão-Teixeira and de Oliveira, 2011), 16.1% in Bangladesh (Samad et al., 1993), 12% in Bangladesh (Shahiduzzaman et al., 2011), 8.4% in West Indies (Chikweto et al., 2011), 6.6% in Ethiopia (Bekele and Kasali, 1989), and 3.3% in Tanzania (Schoonman et al., 2010). The seroprevalence in dairy cattle was 51.5% in Brazil (Frazão-Teixeira and de Oliveira, 2011) and 9.4% in Thailand (Inpankaew et al., 2010). In the present study, the seroprevalences of T. gondii in beef cattle and dairy cattle were 3.0% and 2.3%, respectively, which was lower than that reported in other countries mentioned above. These seroprevalences were also lower than that reported in Guangxi (beef cattle, 80.0%; dairy cattle, 50.9%), Xinjiang (beef cattle, 31.9%), Anhui (dairy cattle, 11.5%), and Yunnan Provinces (4.4%) in China (Cao et al., 2000; Mo et al., 1993; Gu et al., 2005; Mi et al., 2007). The seroprevalence of T. gondii infection is variable, and is dependent on living customs, traditions and life styles of the inhabitants, weather conditions, age of the animals, and husbandry practices (Smith, 1991). In addition, the prevalence of T. gondii in animals and humans is related to oocysts excreted by cats, which become infectious to humans and animals after sporulation (Dubey, 2010).

The present investigation used IHA to detect antibodies to T. gondii in the serum samples of beef cattle and dairy cattle because IHA is considered a simple, sensitive, and specific assay for the detection of antibodies to T. gondii in animal serum samples (Dubey et al., 1995; Zou et al., 2009; Wang et al., 2011). A comparative study of sensitivity and specificity of several serologic tests revealed that IHA has the highest specificity based on the isolation of viable T. gondii (Dubey et al., 1995). The IHA Kit we used in the present investigation has been marketed in China for many years and widely used in serological surveys of T. gondii infection in animals (Zou et al., 2009; Wang et al., 2011).

There are three likely reasons for such a low prevalence of T. gondii in beef cattle and dairy cattle in Heilongjiang Province. First, the oocysts of T. gondii excreted by infected cats can hardly become infective under the low temperature in the long winter season of nearly 6 months per year, so infection is less common in cold climates than in warm climates. Second, the slaughter conditions of domestic animals (such as cattle, sheep, goats, and pigs) are very strict in Heilongjiang Province, so the only definitive host cats are not easily to contract T. gondii from slaughtered animals. Third, the seroprevalence of T. gondii in cats is low (2.8%) in Heilongjiang Province (authors' unpublished data), which was lower than that reported in northeastern Portugal (Lopes et al., 2008).

The present survey showed that the seroprevalence of T. gondii in adult beef cattle and dairy cattle were slightly higher than in calves (Table 2), although the difference was not statistically significant (p>0.05). This result is similar to that reported by Klun et al. (2006), and a similar association had also been observed in other related species such as sheep and goats (Ramzan et al., 2009; Wang et al., 2011). The increase in seroprevalence with age could be attributed to the fact that as animals grow older, they have had a longer time period to potentially be exposed.

The present survey showed that the seroprevalence of T. gondii in female beef cattle was slightly higher than in male beef cattle (Table 2), although the difference was not statistically significant (p>0.05). Our result is similar to that reported by Klun et al. (2006), but it is not consistent with that reported by Samad et al. (1993), who indicated that female Zebu cattle had lower prevalence than male Zebu cattle.

Beef cattle and dairy cattle are raised intensively in large farms ( >500) or semi-intensively by individual families (<50) in Heilongjiang Province. The present survey indicated that the prevalence of T. gondii in beef cattle and dairy cattle raised intensively was lower than that in beef cattle and dairy cattle raised semi-intensively (Table 2). Our findings are consistent with that reported in other countries (Klun et al., 2006; Frazão-Teixeira and de Oliveira, 2011), and a similar association was also observed in other related species such as pig, sheep, and goats (Bártová and Sedlák, 2011; Wang et al., 2011). This difference is likely due to the variation in the two raising systems. The beef cattle and dairy cattle raised intensively are caged and thus have less chance to contact or ingest the oocysts of T. gondii excreted by infective cats.

Humans can also be infected by T. gondii by ingesting tissue cysts in undercooked meat, food or drink contaminated with oocysts, or oocysts from the environment accidentally, or by vertical transmission from mother to fetus via tachyzoites in the circulation (Dubey, 2010). Some studies have proven that consuming undercooked or raw meat is an important source of T. gondii infection for humans (Klun et al., 2006; Lopes et al., 2010). Despite the lower seroprevalence of T. gondii in beef cattle and dairy cattle in Heilongjiang Province, consumption of undercooked or raw “Pan-Fried Beef Skewer” and “Raw beef” is a risk factor for human infection with T. gondii in Heilongjiang Province.

In conclusion, the present survey revealed the occurrence of T. gondii in beef cattle and dairy cattle in Heilongjiang Province, northeast China, which has significance for animal health and poses a public health concern in this area. Integrated control strategies and efficient management measures should be implemented to prevent and control T. gondii infection in beef cattle and dairy cattle in this area.