Abstract
Toxoplasma gondii is an important food-borne zoonotic protozoan parasite, which can infect endothermic animals, including pigs. However, data on T. gondii in slaughter pigs in Shaanxi Province were still lacking. To detect the seroprevalence and analyze the risk factors of T. gondii infection in slaughter pigs in Shaanxi Province, Northwestern China, a total of 784 serum samples were collected from four administrative regions and detected by indirect hemagglutination test for T. gondii infection. Antibodies to T. gondii were found in 19.9% (156/784) slaughter pigs. Moreover, the seropositive rate was different among rearing systems (31% in nonintensive pig farms and 6.7% in intensive pig farms), genders (19.8% in male and 20.0% in female), and regions (ranging from 6.7% in Shenmu to 38.2% in Zhouzhi). Rearing system and region were identified as risk factors for T. gondii infection. These results showed that T. gondii is highly prevalent in slaughter pigs in Shaanxi Province, and it could cause a serious risk to public health. This study provided fundamental information for the prevention and control of T. gondii infection in slaughter pigs in China.
Introduction
T
China is one of the largest producers of pigs in the world, and Shaanxi Province is an important pork producer in China with an annual pork production about 1 million tons. The seroprevalence of T. gondii in pigs has been surveyed in many provinces in China (Zou et al. 2009, Yu et al. 2011, Wu et al. 2012a, 2012b, Li et al. 2015, Xu et al. 2015, You et al. 2015, Sun 2016). Nevertheless, the data about the seroprevalence of T. gondii from slaughter pigs in Shaanxi Province are still lacking. Besides, reports about T. gondii infection in people around Shaanxi Province indicated that the locals and people in adjacent areas are under a severe threat by this pathogen (Yu et al. 2007, Liu et al. 2008, Yang et al. 2012, Zhang and Cheng 2012, Wang et al. 2015). And these data also highlighted the effect of T. gondii on animals and the impact of infected pork on human. Pet keepers, butchers, and other people who might contact animals frequently have a much higher chance of exposure to T. gondii infection (Yu et al. 2007). Therefore, epidemical investigation is necessary to develop prevention and control guidelines. So, as a supplementary, seroprevalence of T. goodii infection in slaughter pigs in Shaanxi Province, Northwestern China, was reported in this study.
Materials and Methods
Ethics statement
This study was approved by the Ethics Committee of the College of Veterinary Medicine, Northwest A&F University before its implementation. All pig blood samples were collected after slaughter without causing any additional discomfort to them.
The collection of blood samples
A total of 784 blood samples were collected in Shaanxi Province, Northwestern China, from November 2015 to April 2016. Samples in Shenmu, Xi'an, Chenggu, and Zhouzhi were collected from 300 (238 from intensively raised and 62 from nonintensively raised), 58 (37 from intensively raised and 21 from nonintensively raised), 138 (59 from intensively raised and 79 from nonintensively raised), and 288 (24 from intensively raised and 264 from nonintensively raised) slaughter pigs, respectively. Approximately 1.5 mL blood samples were collected from slaughter pigs, respectively, by autoclaved 1.5 mL centrifuge tubes, centrifuged at 2000 g for 5 min to obtain sera and then stored at −20°C.
Serological examination
Antibodies to T. gondii were detected in sera by an indirect hemagglutination (IHA) test using a commercially available kit (Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province, China) according to the manufacturer's instructions. In brief, sera were added into 96-well V-bottomed polystryrene plates and diluted in 1:4, 1:16, and 1:64, then the plates were shaken for 2 min followed by incubating them at 37°C for 2 h. The sample was considered positive when erythrocytes agglutinated in all the three wells at different dilutions, and positive and negative controls were included in each test.
Statistical analysis
Statistical analyses of T. gondii seroprevalence in slaughter pigs from different administrative regions, genders, and rearing systems were performed by chi-squared test and the binary logistic regression, using SPSS for Windows (Release 20.0 standard version; IBM SPSS, Inc., Chicago, IL). Differences were considered statistically significant and extremely significant when p < 0.05 and p < 0.01, respectively.
Results and Discussion
Antibodies to T. gondii were found in 156 of 784 slaughter pigs by IHA at a cutoff value of 1:64. The overall seroprevalence was 19.9%, which was higher than that reported in Jilin Province (Xu et al. 2015) but lower than that in Chongqing, Tibet, or Sichuan Province (Shu et al. 2011, Wu et al. 2012a, 2012b). Such difference might be caused by different climates, rearing systems, sanitary conditions, and animal welfares. Of course, the contribution of cats and rodents to Toxoplasma infection also could not be ignored (Weigel et al. 1995, Kijlstra et al. 2008). In addition, our study also showed that slaughter pigs from Zhouzhi County had the highest prevalence (Table 1), probably because of worse environment conditions, welfares, and comparatively more chance to come into contact with cats, rodents, and other sources of infection, which might contribute significantly to the transmission of T. gondii.
Nonintensive pig farm, including semi-intensive pig farm and free-range raising.
CI, confidence interval; OR, odds ratio.
In addition, differences of T. gondii seroprevalence were discovered among rearing systems (nonintensive pig farms: 31.0%; intensive pig farms: 6.7%), genders (male: 19.8%; female: 20.0%), and regions (ranging from 6.7% in Shenmu to 38.2% in Zhouzhi) (Table 1) in this study. Besides, the seroprevalence in nonintensive pig farms (31.0%) was much higher than in intensive pig farms (6.7%) (odds ratio [OR] = 7.02, 95% confidence interval [CI] = 3.94–9.92, p = 0.000). And the seroprevalence in Zhouzhi County (38.2%) (OR = 8.65, 95% CI = 5.18–14.44, p = 0.000) and Chenggu County (15.9%) (OR = 2.66, 95% CI = 1.40–5.05, p = 0.003) was much higher than that in Shenmu County, respectively. The differences of them were both extremely significant. However, the difference of the seroprevalence between Xi'an and Shenmu was nonsignificant (OR = 1.04, 95% CI = 0.34–3.154, p = 0.949) (Table 1).
These results indicated that all factors investigated in this study except sex affected the prevalence of infection. This conclusion was in accordance with previous studies (Villari et al. 2009, Gebremedhin 2014, Zheng et al. 2016a, 2016b) in pigs, sheep, farmed minks, and farmed raccoon dogs. This result might indicate that gender was not a risk factor for T. gondii infection in slaughter pigs. However, region was revealed as an important risk factor for T. gondii infection in slaughter pigs (p < 0.01). Obviously, there are different climates, temperature, humidity, and other geographical conditions in different geographical locations. And these elements may contribute to T. gondii transmission. Remarkably, rearing system (p < 0.01) was considered as a significant risk factor in this study. A different rearing system means a different chance to be exposed to T. gondii, because all things slaughter pigs contacted including food and water may contain T. gondii tissue cysts or oocysts.
Unfortunately, we did not subdivide the risk factors, because we could not get more information about the slaughter pigs from which we collected samples. Thus, the significance of more specific elements including water, food, and other things the pigs contacted should be investigated in further studies to improve the data of risk factors of T. gondii infection in slaughter pigs.
Conclusion
A 19.9% seroprevalence of T. gondii infection in slaughter pigs in Northwestern China was discovered in this study. Rearing system and region were revealed as the significant risk factors for slaughter pig infection with T. gondii. These results indicated that T. gondii is highly prevalent in slaughter pigs in Northwestern China, and the infected pork is extremely likely to be an important risk factor for public health. This study provided fundamental data for the prevention and control of T. gondii infection in slaughter pigs in China.
Footnotes
Acknowledgments
This study was partly supported by the international cooperation project of Ministry of Science and Technology (2015DFG31870), Project of Science and Technology Department of Qinghai Province (2016-ZJ-754), and Program for Changjiang Scholars and Innovative Research Team in University, MOE (IRT13074). The authors are grateful to people who assisted in collecting pig blood samples in the four investigated regions and to other people who participated in this work.
Author Disclosure Statement
No competing financial interests exist.
