Original Article
FOODBORNE PATHOGENS AND DISEASE Volume 0, Number 0, 2014 ª Mary Ann Liebert, Inc. DOI: 10.1089/fpd.2013.1686
Seroprevalence of Toxoplasma gondii Infection in Pigs in Jiangxi Province, Southeastern China Hai-Hai Jiang,1 Wen-Bo Zhang,2 Lei Zhao,1 Dong-Hui Zhou,1 Hui-Qun Song,1 Chang-Man Xu,2 Shun-Zhou Deng,2 and Xing-Quan Zhu1,3
Abstract
Toxoplasma gondii is the causative agent of toxoplasmosis in humans and a wide range of animal species. In the current study, a serological investigation using an indirect hemagglutination (IHA) test was carried out to determine the seroprevalence of T. gondii infection in pigs in Jiangxi Province, southeastern China. A total of 1232 serum samples were collected from pigs in 10 administrative districts in Jiangxi, and specific antibodies were detected in 282 pigs (22.9%) with the titers ‡ 1:64. Positive pigs were found in each administrative district, with prevalence ranging from 5.0% to 46.2%. Age and season were found to be associated with T. gondii infection. Lactating sows (odds ratio [OR] = 15.4, 95% confidence interval [CI] = 6.8–35.2, p < 0.01), pregnant sows (OR = 11.5, 95% CI = 5.3– 24.8, p < 0.01), nonpregnant sows (OR = 13.7, 95% CI = 6.4–29.3, p < 0.01), breeding boars (OR = 9, 95% CI = 3.8– 21.4, p < 0.01), and fattening pigs (OR = 4.9, 95% CI = 2.1–11.7, p < 0.01) all had a greater risk of acquiring infection compared to the weanling pigs. There is a higher risk of infection in the spring (OR = 1.7, 95% CI = 1.1–2.6, p = 0.01) and the summer (OR = 2.1, 95% CI = 1.3–3.2, p < 0.01) than in the winter. This is the first documentation of T. gondii seroprevalence in pigs in Jiangxi Province, which enriches the epidemiological data of T. gondii infection in pigs in China. The results of this study indicate that pigs in Jiangxi Province are frequently exposed to T. gondii, posing a direct threat to the pig industry as well as to public health. Integrated strategies are needed to strengthen future prevention and control of T. gondii infection in pigs in this region.
Public concerns associated with T. gondii clearly show the need for an epidemiological survey in pigs since they are an important source of meat for human consumption. Pigs infected with T. gondii are of veterinary and medical significance because they are potential reservoirs of human toxoplasmosis (Dias et al., 2005; Dubey, 2009). Acute toxoplasmosis including blindness may outbreak if people consume raw pork as previously reported (Choi et al., 1997). Some serologic surveys on the prevalence of T. gondii in pigs have been carried out in other countries recently (Garcı´aBocanegra et al., 2010; Ba´rtova´ and Sedla´k, 2011; Klun et al., 2011). Several studies have shown that T. gondii infection in pigs was common in some regions of China (Zhou et al., 2010; Huang et al., 2010; Tao et al., 2011; Yu et al., 2011). However, there are no data for Jiangxi Province, southeastern China, where the pork production is among the largest in China. Given this background and the zoonotic significance of T. gondii, the objective of the present study was to investigate the seroprevalence of T. gondii infection in pigs in
Introduction
T
oxoplasma gondii is a worldwide zoonotic protozoan parasite that can infect humans and all warm-blooded animals. Domestic cats and other felids, the definitive hosts of this parasite, are able to excrete oocysts into the environment. T. gondii is considered an important foodborne pathogen (Zhou et al., 2008; Davies, 2011). Humans get infected mainly through ingestion of undercooked or raw meat containing tissue cysts or through ingestion of food or water contaminated by oocysts (Dubey, 2004). Approximately 30% of the world population shows seropositivity for T. gondii (Dubey, 2010; Zhou et al., 2011), while in China the prevalence is 7.9% (Xu et al., 2005). Although T. gondii infection is benign in most people, causing few clinical manifestations, blindness and mental retardation may occur in children who were congenitally infected. It can be serious or fatal in immunocompromised individuals such as AIDS patients (Montoya and Liesenfeld, 2004).
1 State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province, China. 2 College of Animal Science and Technology, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China. 3 College of Animal Science and Veterinary Medicine, Heilongjiang Bayi Agricultural University, Daqing, Heilongjiang Province, China.
1
2
JIANG ET AL.
Jiangxi Province, southeastern China. The results are expected to provide basic data for prevention and control programs of T. gondii infection in humans and other animals in this area. Materials and Methods Blood sampling and serum sample preparation
Between January and December 2012, a total of 1232 blood samples were collected from pigs in Jiangxi Province. These pigs were intensively raised in pig farms and came from 10 administrative districts, including Fuzhou, Ganzhou, Ji’an, Jiujiang, Nanchang, Pingxiang, Shangrao, Xinyu, Yichun, and Yingtan. Information concerning geographical location, pig age, and sampling season were recorded. Blood samples were centrifuged at 3000 rpm for 5 min, and sera were collected and transferred to 1.5-mL centrifuge tubes. The obtained serum samples were stored at - 20C until tested for T. gondii antibodies.
Then 25 lL of T. gondii IHA antigen was added into each dilution. The plates were shaken gently for 2 min and incubated at 37C for 2–3 h without shaking. Samples were judged as positive when layers of agglutinated erythrocytes formed in the wells of 1:64 dilutions. The positive and negative control sera provided by the commercial kits were used in each test. Those serum samples that gave doubtful results were re-tested. Statistical analysis
Differences in T. gondii seroprevalence among pigs of different ages and among sampling seasons were analyzed using binary logistic regression in SPSS Version 19 (SPSS Inc., IBM Corp.). The differences in prevalence were considered statistically significant when p < 0.05. Odds ratios (OR) with 95% confidence intervals (CI) based on likelihood ratio statistics were reported. Results
Determination of antibodies to T. gondii
Antibodies to T. gondii were detected by the 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 recommendations. IHA is known as a simple, sensitive, and specific technique for the detection of T. gondii antibodies in animal serum samples (Dubey et al., 1995; Qiu et al., 2012; Miao et al., 2013). In brief, 75 lL of IHA dilution solution and 25 lL of sera (with fourfold serial dilution from 1:4 to 1:256) were added into 96-well 110 V-bottomed polystyrene plates.
In the present study, specific antibodies to T. gondii were detected in 282 of 1232 (22.9%) serum samples by IHA at a dilution of ‡ 1:64. Positive pigs were found in each administrative district of Jiangxi Province, with the prevalence ranging from 5% to 46.2% (Table 1). Seropositive pigs were detected in all age groups. The seroprevalence of T. gondii infection in adult pigs was higher than that in all the younger ones (Table 1); it was the highest in lactating sows (35.5%), followed by nonpregnant sows (32.6%), pregnant sows (29.8%), breeding boars (28.3%), fattening pigs (16.4%), and growing pigs (7.3%). Weanling pigs, however, had the lowest seroprevalence of 3.7%. Lactating sows (OR = 15.4, 95%
Table 1. Seroprevalence of Toxoplasma gondii Infection in Pigs in Jiangxi Province, Southeastern China According to Geographical Location, Age, and Sampling Season Factors Geographical location Fuzhou Ganzhou Ji’an Jiujiang Nanchang Pingxiang Shangrao Xinyu Yichun Yingtan Age Lactating sow (adult female) Pregnant sow (adult female) Nonpregnant sow (adult female) Breeding boar (adult male) Fattening pig (18–23 weeks) Growing pig (11–17 weeks) Weanling pig (4–10 weeks) Sampling season Spring Summer Autumn Winter Total
No. examined
No. positive
Prevalence (%)
13 81 179 65 214 20 182 50 378 50
6 14 37 14 49 1 36 16 101 8
46.2 17.3 20.7 21.5 22.9 5 19.8 32 26.7 16
107 238 334 99 116 124 214
38 71 109 28 19 9 8
35.5 29.8 32.6 28.3 16.4 7.3 3.7
456 285 173 318 1232
113 87 29 53 282
24.8 30.5 16.8 16.7 22.9
TOXOPLASMA SEROPREVALENCE IN PIGS IN JIANGXI, CHINA
CI = 6.8–35.2, p < 0.01), pregnant sows (OR = 11.5, 95% CI = 5.3–24.8, p < 0.01), nonpregnant sows (OR = 13.7, 95% CI = 6.4–29.3, p < 0.01), breeding boars (OR = 9, 95% CI = 3.8–21.4, p < 0.01), and fattening pigs (OR = 4.9, 95% CI = 2.1–11.7, p < 0.01) all had a greater risk of acquiring the infection compared to the weanling pigs, while there was no significant difference in T. gondii seroprevalence between growing pigs (7.3%) and weanling pigs (3.7%) ( p > 0.05). In terms of sampling seasons, pigs faced a greater risk in the spring (OR = 1.7, 95% CI = 1.1–2.6, p = 0.01) and the summer (OR = 2.1, 95% CI = 1.3–3.2, p < 0.01) than in the winter. No significant difference was found in T. gondii seroprevalence between pigs in autumn (16.8%) and winter (16.7%) ( p > 0.05). Discussion
Consumption of undercooked or raw meat or meat products is an important route of human infection with T. gondii (Bobic´ et al., 2007). In China, pork is the most common meat, accounting for 65% of the meat consumption. However, before it is sold and consumed, pork is not required to be inspected for T. gondii contamination by law. The present study, therefore, was aimed to estimate T. gondii seroprevalence in pigs in Jiangxi Province, where pork is mostly consumed. A previous study reported an overall T. gondii seroprevalence of 36% among 551 clinically healthy adult slaughtered pigs in Czech Republic (Ba´rtova´ and Sedla´k, 2011). Garcı´a-Bocanegra et al. detected a 16.6% prevalence in domestic pigs from 100 farms in the 10 main swine production regions in Spain by the modified agglutination test (Garcı´a-Bocanegra et al., 2010), and Klun et al. (2011) reported a low prevalence of T. gondii infection in slaughter pigs (9.2%) in Serbia. In this study, the overall seroprevalence of T. gondii infection in pigs in Jiangxi Province was 22.9%, which was lower than that in the Czech Republic but higher than that detected in Spain and Serbia. Compared with neighboring provinces in China, the overall T. gondii seroprevalence in pigs in Jiangxi Province was higher than that in Fujian Province (14.4%) (Hang et al., 2010), but lower than that in Hubei Province (24.5%) (Tao et al., 2011), Zhejiang Province (53.4%) (Yu et al., 2011), and Guangdong Province (27%) (Zhou et al., 2010). The reasons why T. gondii prevalence varies among different provinces could be manifold. Different regions located in different geographical areas have a different climate and environment, which may influence the presence of T. gondii. The management of pig farms, as well as pig welfare, varies from place to place. Studies vary in the serological tests used may in part account for the prevalence differences among different studies. In the current study, we also found the prevalence variation in pigs of different ages. The prevalence of T. gondii infection in adult pigs was higher than that in all the younger ones, which may be due merely to longer exposure of adult pigs. The T. gondii seroprevalence in pigs varied also according to sampling seasons, with the seroprevalence in the summer being significantly higher than in the winter. Jiangxi has a hot, humid summer, which may be more favorable for the survival of T. gondii oocysts, but a cool, damp winter, which may be less suitable for the presence of T. gondii (Dubey, 2010).
3
According to a serological survey carried out in the city of Nanchang, the capital of Jiangxi Province, T. gondii antibodies were detected in 8% of the examined 1960 people (Chen et al., 2005). Jiangxi’s pork industry produces about 4.5% of all pork produced in China, a large proportion of which is consumed locally. Once the meat of T. gondii–seropositive pigs is put on the market, it may put local people at risk of T. gondii infection if consumed raw or undercooked. This study tested 1232 pig serum samples collected in Jiangxi Province within a single year for T. gondii antibodies, which is a short period of time. Thus our results may not reflect the actual status of T. gondii infection for longer periods of time. However, our findings provide useful information for further studies. Our next efforts would be directed at determining the seroprevalence of T. gondii infection in pigs over several years, as well as in other animal species and humans in this region. In conclusion, the present study is the first report of T. gondii seroprevalence in pigs in Jiangxi Province, southeastern China. The results indicate that pigs in Jiangxi Province are frequently exposed to T. gondii. The seroprevalence of T. gondii infection in pigs in Jiangxi Province poses a risk for human infection and accordingly, is of public health significance. Hence, it is necessary to improve sanitation and management of pig farms to reduce transmission of T. gondii, and to implement routine inspection of T. gondii infection during slaughtering and postslaughter processing of pigs. Acknowledgments
The authors thank Associate Professor Chunlei Su at Department of Microbiology, the University of Tennessee, Knoxville, TN for copyediting and improving the manuscript. Project support was provided by the National Natural Science Foundation of China (Grant Nos. 31230073 and 31172316), and the Science Fund for Creative Research Groups of Gansu Province (Grant No. 1210RJIA006). Disclosure Statement
No competing financial interests exist. References
Ba´rtova´ E, Sedla´k K. Seroprevalence of Toxoplasma gondii and Neospora caninum in slaughtered pigs in the Czech Republic. Parasitology 2011;138:1369–1371. Bobic´ B, Nikolic´ A, Klun I, Vujanic´ M, Djurkovic´-Djakovic´ O. Undercooked meat consumption remains the major risk factor for Toxoplasma infection in Serbia. Parassitologia 2007;49: 227–230. Chen HY, Xiao HM, Zeng XJ, Xiong CH, Ge J, Hu GH. Seroepidemiological survey on the infection of Toxoplasma gondii among population in Nanchang area. Chin J Parasit Dis Con 2005;18:435–437 (in Chinese). Choi WY, Nam HW, Kwak NH, Huh W, Kim YR, Kang MW, Cho SY, Dubey JP. Foodborne outbreaks of human toxoplasmosis. J Infect Dis 1997;175:1280–1282. Davies PR. Intensive swine production and pork safety. Foodborne Pathog Dis 2011;8:189–201. Dias RA, Navarro IT, Ruffolo BB, Bugni FM, Castro MV, Freire RL. Toxoplasma gondii in fresh pork sausage and seroprevalence in butchers from factories in Londrina, Parana´
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State, Brazil. Rev Inst Med Trop Sao Paulo 2005;47:185– 189. Dubey JP. Toxoplasmosis—A waterborne zoonosis. Vet Parasitol 2004;126:57–72. Dubey JP. Toxoplasmosis in pigs—The last 20 years. Vet Parasitol 2009;164:89–103. Dubey JP. Toxoplasmosis of Animals and Humans, 2nd ed. Boca Raton, FL: CRC Press, 2010, pp. 1–313. Dubey JP, Thulliez P, Weigel RM, Andrews CD, Lind P, Powell EC. Sensitivity and specificity of various serologic tests for detection of Toxoplasma gondii infection in naturally infected sows. Am J Vet Res 1995;56:1030–1036. Garcı´a-Bocanegra I, Simon-Grife´ M, Dubey JP, Casal J, Martı´n GE, Cabezo´n O, Perea A, Almerı´a S. Seroprevalence and risk factors associated with Toxoplasma gondii in domestic pigs from Spain. Parasitol Int 2010;59:421–426. Huang CQ, Lin YY, Dai AL, Li XH, Yang XY, Yuan ZG, Zhu XQ. Seroprevalence of Toxoplasma gondii infection in breeding sows in Western Fujian Province, China. Trop Anim Health Prod 2010;42:115–118. Klun I, Vujanic´ M, Year H, Nikolic´ A, Ivovic´ V, Bobic´ B, Bradonjic´ S, Dupouy-Camet J, Djurkovic´-Djakovic´ O. Toxoplasma gondii infection in slaughter pigs in Serbia: Seroprevalence and demonstration of parasites in blood. Vet Res 2011;42:17. Montoya JG, Liesenfeld O. Toxoplasmosis. Lancet 2004;363: 1965–1976. Miao Q, Wang X, She LN, Fan YT, Yuan FZ, Yang JF, Zhu XQ, Zou FC. Seroprevalence of Toxoplasma gondii in horses and donkeys in Yunnan Province, Southwestern China. Parasit Vectors 2013;6:168. Qiu JH, Wang CR, Zhang X, Sheng ZH, Chang QC, Zhao Q, Wu SM, Zou FC, Zhu XQ. Seroprevalence of Toxoplasma gondii in beef cattle and dairy cattle in Northeast China. Foodborne Pathog Dis 2012;9:579–582. Tao Q, Wang Z, Feng H, Fang R, Nie H, Hu M, Zhou Y, Zhao J. Seroprevalence and risk factors for Toxoplasma gondii
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infection on pig farms in central China. J Parasitol 2011; 97:262–264. Xu LQ, Chen YD, Sun FH, Cai L, Fang YY, Wang LP, Liu X, Li LS, Feng Y, Li H. A national survey on current status of the important parasitic diseases in human population. Chin J Parasitol Parasit Dis 2005;23:332–340 (in Chinese). Yu HJ, Zhang Z, Liu Z, Qu DF, Zhang DF, Zhang HL, Zhou QJ, Du AF. Seroprevalence of Toxoplasma gondii infection in pigs in Zhejiang Province, China. J Parasitol 2011;97: 748–749. Zhou DH, Liang R, Yin CC, Zhao FR, Yuan ZG, Lin RQ, Song HQ, Zhu XQ. Seroprevalence of Toxoplasma gondii in pigs from southern China. J Parasitol 2010;96:673–674. Zhou P, Chen N, Zhang RL, Lin RQ, Zhu XQ. Food-borne parasitic zoonoses in China: Perspective for control. Trends Parasitol 2008;24:190–196. Zhou P, Chen ZG, Li HL, Zheng HH, He SY, Lin RQ, Zhu XQ. Toxoplasma gondii infection in humans in China. Parasit Vectors 2011;24:165.
Address correspondence to: Xing-Quan Zhu, PhD State Key Laboratory of Veterinary Etiological Biology Key Laboratory of Veterinary Parasitology of Gansu Province Lanzhou Veterinary Research Institute Chinese Academy of Agricultural Sciences Lanzhou, Gansu Province 730046, China E-mail: [email protected] Shun-Zhou Deng, PhD College of Animal Science and Technology Jiangxi Agricultural University Nanchang, Jiangxi Province 330045, China E-mail: [email protected]
FOODBORNE PATHOGENS AND DISEASE Volume 0, Number 0, 2014 ª Mary Ann Liebert, Inc. DOI: 10.1089/fpd.2013.1686
Seroprevalence of Toxoplasma gondii Infection in Pigs in Jiangxi Province, Southeastern China Hai-Hai Jiang,1 Wen-Bo Zhang,2 Lei Zhao,1 Dong-Hui Zhou,1 Hui-Qun Song,1 Chang-Man Xu,2 Shun-Zhou Deng,2 and Xing-Quan Zhu1,3
Abstract
Toxoplasma gondii is the causative agent of toxoplasmosis in humans and a wide range of animal species. In the current study, a serological investigation using an indirect hemagglutination (IHA) test was carried out to determine the seroprevalence of T. gondii infection in pigs in Jiangxi Province, southeastern China. A total of 1232 serum samples were collected from pigs in 10 administrative districts in Jiangxi, and specific antibodies were detected in 282 pigs (22.9%) with the titers ‡ 1:64. Positive pigs were found in each administrative district, with prevalence ranging from 5.0% to 46.2%. Age and season were found to be associated with T. gondii infection. Lactating sows (odds ratio [OR] = 15.4, 95% confidence interval [CI] = 6.8–35.2, p < 0.01), pregnant sows (OR = 11.5, 95% CI = 5.3– 24.8, p < 0.01), nonpregnant sows (OR = 13.7, 95% CI = 6.4–29.3, p < 0.01), breeding boars (OR = 9, 95% CI = 3.8– 21.4, p < 0.01), and fattening pigs (OR = 4.9, 95% CI = 2.1–11.7, p < 0.01) all had a greater risk of acquiring infection compared to the weanling pigs. There is a higher risk of infection in the spring (OR = 1.7, 95% CI = 1.1–2.6, p = 0.01) and the summer (OR = 2.1, 95% CI = 1.3–3.2, p < 0.01) than in the winter. This is the first documentation of T. gondii seroprevalence in pigs in Jiangxi Province, which enriches the epidemiological data of T. gondii infection in pigs in China. The results of this study indicate that pigs in Jiangxi Province are frequently exposed to T. gondii, posing a direct threat to the pig industry as well as to public health. Integrated strategies are needed to strengthen future prevention and control of T. gondii infection in pigs in this region.
Public concerns associated with T. gondii clearly show the need for an epidemiological survey in pigs since they are an important source of meat for human consumption. Pigs infected with T. gondii are of veterinary and medical significance because they are potential reservoirs of human toxoplasmosis (Dias et al., 2005; Dubey, 2009). Acute toxoplasmosis including blindness may outbreak if people consume raw pork as previously reported (Choi et al., 1997). Some serologic surveys on the prevalence of T. gondii in pigs have been carried out in other countries recently (Garcı´aBocanegra et al., 2010; Ba´rtova´ and Sedla´k, 2011; Klun et al., 2011). Several studies have shown that T. gondii infection in pigs was common in some regions of China (Zhou et al., 2010; Huang et al., 2010; Tao et al., 2011; Yu et al., 2011). However, there are no data for Jiangxi Province, southeastern China, where the pork production is among the largest in China. Given this background and the zoonotic significance of T. gondii, the objective of the present study was to investigate the seroprevalence of T. gondii infection in pigs in
Introduction
T
oxoplasma gondii is a worldwide zoonotic protozoan parasite that can infect humans and all warm-blooded animals. Domestic cats and other felids, the definitive hosts of this parasite, are able to excrete oocysts into the environment. T. gondii is considered an important foodborne pathogen (Zhou et al., 2008; Davies, 2011). Humans get infected mainly through ingestion of undercooked or raw meat containing tissue cysts or through ingestion of food or water contaminated by oocysts (Dubey, 2004). Approximately 30% of the world population shows seropositivity for T. gondii (Dubey, 2010; Zhou et al., 2011), while in China the prevalence is 7.9% (Xu et al., 2005). Although T. gondii infection is benign in most people, causing few clinical manifestations, blindness and mental retardation may occur in children who were congenitally infected. It can be serious or fatal in immunocompromised individuals such as AIDS patients (Montoya and Liesenfeld, 2004).
1 State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province, China. 2 College of Animal Science and Technology, Jiangxi Agricultural University, Nanchang, Jiangxi Province, China. 3 College of Animal Science and Veterinary Medicine, Heilongjiang Bayi Agricultural University, Daqing, Heilongjiang Province, China.
1
2
JIANG ET AL.
Jiangxi Province, southeastern China. The results are expected to provide basic data for prevention and control programs of T. gondii infection in humans and other animals in this area. Materials and Methods Blood sampling and serum sample preparation
Between January and December 2012, a total of 1232 blood samples were collected from pigs in Jiangxi Province. These pigs were intensively raised in pig farms and came from 10 administrative districts, including Fuzhou, Ganzhou, Ji’an, Jiujiang, Nanchang, Pingxiang, Shangrao, Xinyu, Yichun, and Yingtan. Information concerning geographical location, pig age, and sampling season were recorded. Blood samples were centrifuged at 3000 rpm for 5 min, and sera were collected and transferred to 1.5-mL centrifuge tubes. The obtained serum samples were stored at - 20C until tested for T. gondii antibodies.
Then 25 lL of T. gondii IHA antigen was added into each dilution. The plates were shaken gently for 2 min and incubated at 37C for 2–3 h without shaking. Samples were judged as positive when layers of agglutinated erythrocytes formed in the wells of 1:64 dilutions. The positive and negative control sera provided by the commercial kits were used in each test. Those serum samples that gave doubtful results were re-tested. Statistical analysis
Differences in T. gondii seroprevalence among pigs of different ages and among sampling seasons were analyzed using binary logistic regression in SPSS Version 19 (SPSS Inc., IBM Corp.). The differences in prevalence were considered statistically significant when p < 0.05. Odds ratios (OR) with 95% confidence intervals (CI) based on likelihood ratio statistics were reported. Results
Determination of antibodies to T. gondii
Antibodies to T. gondii were detected by the 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 recommendations. IHA is known as a simple, sensitive, and specific technique for the detection of T. gondii antibodies in animal serum samples (Dubey et al., 1995; Qiu et al., 2012; Miao et al., 2013). In brief, 75 lL of IHA dilution solution and 25 lL of sera (with fourfold serial dilution from 1:4 to 1:256) were added into 96-well 110 V-bottomed polystyrene plates.
In the present study, specific antibodies to T. gondii were detected in 282 of 1232 (22.9%) serum samples by IHA at a dilution of ‡ 1:64. Positive pigs were found in each administrative district of Jiangxi Province, with the prevalence ranging from 5% to 46.2% (Table 1). Seropositive pigs were detected in all age groups. The seroprevalence of T. gondii infection in adult pigs was higher than that in all the younger ones (Table 1); it was the highest in lactating sows (35.5%), followed by nonpregnant sows (32.6%), pregnant sows (29.8%), breeding boars (28.3%), fattening pigs (16.4%), and growing pigs (7.3%). Weanling pigs, however, had the lowest seroprevalence of 3.7%. Lactating sows (OR = 15.4, 95%
Table 1. Seroprevalence of Toxoplasma gondii Infection in Pigs in Jiangxi Province, Southeastern China According to Geographical Location, Age, and Sampling Season Factors Geographical location Fuzhou Ganzhou Ji’an Jiujiang Nanchang Pingxiang Shangrao Xinyu Yichun Yingtan Age Lactating sow (adult female) Pregnant sow (adult female) Nonpregnant sow (adult female) Breeding boar (adult male) Fattening pig (18–23 weeks) Growing pig (11–17 weeks) Weanling pig (4–10 weeks) Sampling season Spring Summer Autumn Winter Total
No. examined
No. positive
Prevalence (%)
13 81 179 65 214 20 182 50 378 50
6 14 37 14 49 1 36 16 101 8
46.2 17.3 20.7 21.5 22.9 5 19.8 32 26.7 16
107 238 334 99 116 124 214
38 71 109 28 19 9 8
35.5 29.8 32.6 28.3 16.4 7.3 3.7
456 285 173 318 1232
113 87 29 53 282
24.8 30.5 16.8 16.7 22.9
TOXOPLASMA SEROPREVALENCE IN PIGS IN JIANGXI, CHINA
CI = 6.8–35.2, p < 0.01), pregnant sows (OR = 11.5, 95% CI = 5.3–24.8, p < 0.01), nonpregnant sows (OR = 13.7, 95% CI = 6.4–29.3, p < 0.01), breeding boars (OR = 9, 95% CI = 3.8–21.4, p < 0.01), and fattening pigs (OR = 4.9, 95% CI = 2.1–11.7, p < 0.01) all had a greater risk of acquiring the infection compared to the weanling pigs, while there was no significant difference in T. gondii seroprevalence between growing pigs (7.3%) and weanling pigs (3.7%) ( p > 0.05). In terms of sampling seasons, pigs faced a greater risk in the spring (OR = 1.7, 95% CI = 1.1–2.6, p = 0.01) and the summer (OR = 2.1, 95% CI = 1.3–3.2, p < 0.01) than in the winter. No significant difference was found in T. gondii seroprevalence between pigs in autumn (16.8%) and winter (16.7%) ( p > 0.05). Discussion
Consumption of undercooked or raw meat or meat products is an important route of human infection with T. gondii (Bobic´ et al., 2007). In China, pork is the most common meat, accounting for 65% of the meat consumption. However, before it is sold and consumed, pork is not required to be inspected for T. gondii contamination by law. The present study, therefore, was aimed to estimate T. gondii seroprevalence in pigs in Jiangxi Province, where pork is mostly consumed. A previous study reported an overall T. gondii seroprevalence of 36% among 551 clinically healthy adult slaughtered pigs in Czech Republic (Ba´rtova´ and Sedla´k, 2011). Garcı´a-Bocanegra et al. detected a 16.6% prevalence in domestic pigs from 100 farms in the 10 main swine production regions in Spain by the modified agglutination test (Garcı´a-Bocanegra et al., 2010), and Klun et al. (2011) reported a low prevalence of T. gondii infection in slaughter pigs (9.2%) in Serbia. In this study, the overall seroprevalence of T. gondii infection in pigs in Jiangxi Province was 22.9%, which was lower than that in the Czech Republic but higher than that detected in Spain and Serbia. Compared with neighboring provinces in China, the overall T. gondii seroprevalence in pigs in Jiangxi Province was higher than that in Fujian Province (14.4%) (Hang et al., 2010), but lower than that in Hubei Province (24.5%) (Tao et al., 2011), Zhejiang Province (53.4%) (Yu et al., 2011), and Guangdong Province (27%) (Zhou et al., 2010). The reasons why T. gondii prevalence varies among different provinces could be manifold. Different regions located in different geographical areas have a different climate and environment, which may influence the presence of T. gondii. The management of pig farms, as well as pig welfare, varies from place to place. Studies vary in the serological tests used may in part account for the prevalence differences among different studies. In the current study, we also found the prevalence variation in pigs of different ages. The prevalence of T. gondii infection in adult pigs was higher than that in all the younger ones, which may be due merely to longer exposure of adult pigs. The T. gondii seroprevalence in pigs varied also according to sampling seasons, with the seroprevalence in the summer being significantly higher than in the winter. Jiangxi has a hot, humid summer, which may be more favorable for the survival of T. gondii oocysts, but a cool, damp winter, which may be less suitable for the presence of T. gondii (Dubey, 2010).
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According to a serological survey carried out in the city of Nanchang, the capital of Jiangxi Province, T. gondii antibodies were detected in 8% of the examined 1960 people (Chen et al., 2005). Jiangxi’s pork industry produces about 4.5% of all pork produced in China, a large proportion of which is consumed locally. Once the meat of T. gondii–seropositive pigs is put on the market, it may put local people at risk of T. gondii infection if consumed raw or undercooked. This study tested 1232 pig serum samples collected in Jiangxi Province within a single year for T. gondii antibodies, which is a short period of time. Thus our results may not reflect the actual status of T. gondii infection for longer periods of time. However, our findings provide useful information for further studies. Our next efforts would be directed at determining the seroprevalence of T. gondii infection in pigs over several years, as well as in other animal species and humans in this region. In conclusion, the present study is the first report of T. gondii seroprevalence in pigs in Jiangxi Province, southeastern China. The results indicate that pigs in Jiangxi Province are frequently exposed to T. gondii. The seroprevalence of T. gondii infection in pigs in Jiangxi Province poses a risk for human infection and accordingly, is of public health significance. Hence, it is necessary to improve sanitation and management of pig farms to reduce transmission of T. gondii, and to implement routine inspection of T. gondii infection during slaughtering and postslaughter processing of pigs. Acknowledgments
The authors thank Associate Professor Chunlei Su at Department of Microbiology, the University of Tennessee, Knoxville, TN for copyediting and improving the manuscript. Project support was provided by the National Natural Science Foundation of China (Grant Nos. 31230073 and 31172316), and the Science Fund for Creative Research Groups of Gansu Province (Grant No. 1210RJIA006). Disclosure Statement
No competing financial interests exist. References
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Address correspondence to: Xing-Quan Zhu, PhD State Key Laboratory of Veterinary Etiological Biology Key Laboratory of Veterinary Parasitology of Gansu Province Lanzhou Veterinary Research Institute Chinese Academy of Agricultural Sciences Lanzhou, Gansu Province 730046, China E-mail: [email protected] Shun-Zhou Deng, PhD College of Animal Science and Technology Jiangxi Agricultural University Nanchang, Jiangxi Province 330045, China E-mail: [email protected]
