The seroprevalence and distribution of Toxoplasma gondii in pigs in China from 2000 to 2023: a systematic review and meta-analysis

Abstract

Toxoplasma gondii (T. gondii) is a globally distributed parasite that can infect a diversity of warm-blooded animals, including swine and humans. Infection in swine poses a considerable threat to food safety and public health. The aim of this meta-analysis was to estimate the seroprevalence of T. gondii infection in the swine population in China from 2000 to 2023 and to examine potential factors associated with infection. A total of 112 studies were included, collectively involving 145,152 swine samples originating from 26 provinces. The pooled seroprevalence was 26.0% (95% CI: 23.3%–28.7%). Stratified analysis based on diagnostic methods revealed that studies using the indirect hemagglutination assay (IHA) reported a seroprevalence of 19.7% (95% CI: 17.2%–22.2%), whereas those utilizing the enzyme-linked immunosorbent assay (ELISA) reported a higher seroprevalence of 35.5% (95% CI: 29.1%–41.8%). Geographical analysis indicated higher seroprevalence in the South Central and Southwest regions, whereas the East and Northwest areas reported the lowest seroprevalence. Chongqing Province reported the highest seroprevalence, reaching 44.9% (95% CI: 43.4%–46.0%), followed by Xinjiang, Hainan, and Guizhou, whereas the lowest was observed in Shandong Province (3.5%, 95% CI: 1.7%–6.1%). These findings provide important epidemiological evidence that can inform strategies for the prevention and control of T. gondii infection in swine populations, with a focus on high-risk populations and geographical areas. This imperative contributes substantially to the improvement of both food safety and public health.

Keywords

Seroprevalence / Distribution / Toxoplasma gondii / Pigs / Systematic review

References

[1] AbdelbasetAE, AbushahbaMFN, IgarashiM. Toxoplasma gondii in humans and animals in Japan: An epidemiological overview. Parasitology International, 2022, 87 ArticleID: 102533

[2] Bin, Zheng, Yin Zhikui, Li Jinna, Yao Zhijun, Wang Shuai, Ren Hongbin, and Zhang Haizhu. 2017. Analysis of Toxoplasma gondii infection and risk factors in pigs in Xinxiang area, Henan Province, Progress in Veterinary Medicine, 38: 117–19. https://doi.org/10.16437/j.cnki.1007-5038.2017.06.026

[3] BacciC, VismarraA, MangiaC, BonardiS, BruiniI, GenchiM, KramerL, BrindaniF. Detection of Toxoplasma gondii in free-range, organic pigs in Italy using serological and molecular methods. International Journal of Food Microbiology, 2015, 202: 54-56

[4] BaiMJ, ZouY, ElsheikhaHM, MaJG, ZhengWB, ZhaoQ, ZhangXX, ZhuXQ. Toxoplasma gondiiInfection in farmed wild boars (sus scrofa) in three cities of northeast China. Foodborne Pathogens and Disease, 2017, 14: 379-385

[5] Bin, Xu, Zhang Xialan, Zeng Zheng, Feng Chao, Su Bing, and He Qin. 2013. Serological investigation and analysis of pig toxoplasmosis in Chongqing area, Chinese Veterinary Science, 43: 98–102. https://doi.org/10.16656/j.issn.1673-4696.2013.01.018

[6] Bingchao, Meng, Wang Jiaming, Zhou Shenghuai, and Dong Baoyu. 2016. Serological investigation of pig toxoplasmosis in Qiannan Prefecture, Animal Husbandry & Veterinary Medicine, 48: 151–52. S

[7] Boshu, Liu, Wang Qiongqiu, Li Yongbin, Guo Jianxin, Liu Jiasheng, and Zhou Xiaowu. 2006. Serological investigation of pig toxoplasmosis in Honghe Prefecture, Yunnan Journal of Animal Science and Veterinary Medicine, 12–13. https://doi.org/10.3969/j.issn.1005-1341.2006.04.007

[8] Bucai, Zhang. 2015. Seroepidemiological investigation of Toxoplasma gondii in pigs in Taizhou area and study on the efficacy of traditional Chinese medicine in treating acute infection of Toxoplasma gondii in mice, Yangzhou University.

[9] Buxton, D. 1998. Protozoan infections (Toxoplasma gondii, Neospora caninum and Sarcocystis spp.) in sheep and goats: recent advances, Vet Res, 29: 289–310. https://pubmed.ncbi.nlm.nih.gov/9689743/

[10] Caigejia, Zhang Jun, Wang Jinwen, Wang Xiaohong, and Li Xin. 2019. Serological investigation and analysis of porcine toxoplasmosis in Hainan, Qinghai Province, Journal of Livestock Ecology, 0: 69–71.

[11] Cairen, Jinan. 2015. Serological Epidemic Investigation of Porcine Toxoplasma gondii Infection in Shengduo County, Qinghai Province, Heilongjiang animal science and veterinary medicine, 110–11. https://doi.org/10.13881/j.cnki.hljxmsy.2015.1283

[12] Caiying, Chen. 2008. Epidemiological investigation of toxoplasmosis in livestock in Datong County, Qinghai Journal of Animal Husbandry and Veterinary Medicine, 23.

[13] ChangQC, ZhengX, QiuJH, WangCR, ZhuXQ. Seroprevalence of Toxoplasma gondii infection in fattening pigs in Northeast China. Journal of Parasitology, 2013, 99: 544-545

[14] Chenghong, Lei, Guo Fuli, Wang Yili, Bao Zhenzhong, and Cai Yuanqing. 2013. Serological investigation of toxoplasmosis in pigs, dogs, and chickens in Urumqi region, Xinjiang Animal Husbandry, 28–30. https://doi.org/10.16795/j.cnki.xjxmy.2013.11.009

[15] ChengminWang, HongxuanHe, JianhuaQin, SixinYao, LirongWang, LiyanLiu, ChaofengNiu, MingchaoGao. Epidemiological investigation of pig and sheep toxoplasmosis in the suburbs of Xinxiang City. Henan Province, Chinese Journal of Parasitology and Parasitic Diseases, 2005, 23: 31

[16] Chunxue, Sun, Xia Binbin, Zhang Li, and Li Hailong. 2018. Seroepidemiological investigation of Toxoplasma gondii in border areas of Yunnan Province, Heilongjiang animal science and veterinary medicine, 100–01. https://doi.org/10.13881/j.cnki.hljxmsy.2017.12.0278

[17] Cuiqin, Huang, He Qian, and Zheng Xintian. 2018. Comparative analysis of three ELISA kits for detecting porcine toxoplasmosis, Heilongjiang animal science and veterinary medicine, 0: 49–53. https://doi.org/10.13881/j.cnki.hljxmsy.2017.07.0090

[18] Cunfu, Gao, Kang Guiying, Qin Jianhua, and Gu Xiaolong. 2005. Detection of serum antibodies against toxoplasmosis in pigs and cows in Hebei Province, Chinese Journal of Animal Quarantine, 39. https://doi.org/10.3969/j.issn.1005-944X.2005.09.025

[19] Dai, Dai. 2014. Investigation of Toxoplasma gondii infection in pigs in Yushu Prefecture, Qinghai Province, Contemporary Livestock and Poultry Breeding Industry, 53–54. https://doi.org/10.14070/j.cnki.15-1150.2014.08.129

[20] De BerardinisA, PaludiD, PennisiL, VergaraA. Toxoplasma gondii, a Foodborne Pathogen in the Swine Production Chain from a European Perspective. Foodborne Pathogens and Disease, 2017, 14: 637-648

[21] DengH, DevleesschauwerB, LiuM, LiJ, WuY, van der GiessenJWB, OpsteeghM. Seroprevalence of Toxoplasma gondii in pregnant women and livestock in the mainland of China: A systematic review and hierarchical meta-analysis. Science and Reports, 2018, 8: 6218

[22] DonghuaGu, HanlinLi. Serological detection of porcine toxoplasmosis. Shandong Animal Husbandry and Veterinary Medicine, 2014, 35: 53-54

[23] DubeyJP. History of the discovery of the life cycle of Toxoplasma gondii. International Journal for Parasitology, 2009, 39: 877-882

[24] DubeyJP, Cerqueira-CézarCK, MurataFHA, KwokOCH, HillD, YangY, SuC. All about Toxoplasma gondii infections in pigs: 2009–2020. Veterinary Parasitology, 2020, 288 ArticleID: 109185

[25] Elsheikha, H. M., C. M. Marra, and X. Q. Zhu. 2021. Epidemiology, pathophysiology, diagnosis, and management of cerebral toxoplasmosis, Clin Microbiol Rev, 34. https://doi.org/10.1128/CMR.00115-19

[26] Facheng, Jiang, Jiang Suojun, Chen Shuxia, and Sun Hao. 2013. Serological investigation of porcine toxoplasmosis in Huaian city, Shanghai Animal Husbandry and Veterinary Medicine, 47+49. https://doi.org/10.3969/j.issn.1000-7725.2013.02.024

[27] FangpingXiao, BoYu, KaizhiShi, YuekaiYang, Yang MaoshengXu, Hongzhong, and Ren Rongqing. . Serological investigation and analysis of pig toxoplasmosis in Guiyang area. Animal Husbandry & Veterinary Medicine, 2014, 46: 86-88

[28] ForoutanM, FakhriY, RiahiSM, EbrahimpourS, NamroodiS, TaghipourA, SpotinA, GambleHR, RostamiA. The global seroprevalence of Toxoplasma gondii in pigs: A systematic review and meta-analysis. Veterinary Parasitology, 2019, 269: 42-52

[29] Gedai. 2010. Epidemiological investigation of toxoplasmosis in fern ma pig in the high cold and damp areas of Gannan, Journal of Animal Science and Veterinary Medicine, 55–56.

[30] GongQL, LiJ, LiD, TianT, LengX, LiJM, ShiK, ZhangNZ, DuR, ZhaoQ. Seroprevalence of Toxoplasma gondii in cattle in China from 2010 to 2019: A systematic review and meta-analysis. Acta Tropica, 2020, 211 ArticleID: 105439

[31] Gongga, Puqiong, Luosang Awang, Mima, and Sorangs bead. 2013. Serological investigation of toxoplasma gondii in Tibetan pigs in some regions of Tibet, Chinese Animal Husbandry and Veterinary Medicine, 29: 126+58.

[32] Guangyu, Liao, Liu Cheng, Xiao Jianhua, Chen Minghai, Li Yangyu, and Chen Mingfeng. 2016. Serological investigation of porcine toxoplasmosis in Yongzhou, Hunan Province, Animal Husbandry and Veterinary Science and Technology Information, 22–23. https://doi.org/10.3969/J.ISSN.1671-6027.2016.07.012

[33] Guili, Lu, Wang Wen, Chen Weidong, Wang Ping, Shaylan Kaiza, Cheng Jin, and Xia Jun. 2014. https://doi.org/10.16437/j.cnki.1007-5038.2014.07.025

[34] Guiling, Mu. 2009. Diagnosis and epidemiological investigation of porcine toxoplasmosis in Yanqing County, Chinese Academy of Agricultural Sciences.

[35] HaiboYu. The current situation and prospects of the Chinese pig industry. Sichuan Anim Vet Sci, 2015, 42: 19-20

[36] HaixiaWang. Serological investigation of pig toxoplasmosis in Huangzhong County. Chinese Journal of Animal Quarantine, 2012, 29: 44-45

[37] HaiyanWang, QingeRen, FuchunKan, YangZhou, ChangshenNing, LongxianZhang. Investigation of Toxoplasma gondii infection in some areas of Henan Province and vaccination test of pig derived strains on mice. Chinese Journal of Zoonoses, 2008, 24: 930-932

[38] HerreroL, GraciaMJ, Pérez-ArquilluéC, LázaroR, HerreraM, HerreraA, BayarriS. Toxoplasma gondii: Pig seroprevalence, associated risk factors and viability in fresh pork meat. Veterinary Parasitology, 2016, 224: 52-59

[39] HeyunSun. Serological investigation of swine toxoplasmosis in Xinyang City. Henan Province, Progress in Veterinary Medicine, 2016, 37: 123-125

[40] Hua, Zheng, Zhai Shaoqin, Zhou Xue, and Xu Dengfeng. 2009. Serological investigation of pig toxoplasmosis in Rongchang area, Shanghai Animal Husbandry and Veterinary Medicine, 39–40. https://doi.org/10.3969/j.issn.1000-7725.2009.06.019

[41] HuangCQ, LinYY, DaiAL, LiXH, YangXY, YuanZG, ZhuXQ. Seroprevalence of Toxoplasma gondii infection in breeding sows in Western Fujian Province. China, Trop Anim Health Prod, 2010, 42: 115-118

[42] Huilan, Liu. 2014. Serological investigation of toxoplasmosis in pigs, cattle, and sheep in Wuping County, Fujian Animal Husbandry and Veterinary Medicine, 36: 16–18. CNKI:SUN:FJCY.0.2014–02–008

[43] JiangHH, ZhangWB, ZhaoL, ZhouDH, SongHQ, XuCM, DengSZ, ZhuXQ. Seroprevalence of Toxoplasma gondii infection in pigs in Jiangxi Province. Southeastern China, Foodborne Pathog Dis, 2014, 11: 362-365

[44] Jianqiang, Han, Sun Xiutao, Li Bing, Duan Gang, and Zou Fengcai. 2011. Serological investigation of pig toxoplasmosis in Yuxi City, Yunnan Province, Heilongjiang animal science and veterinary medicine, 102–03. https://doi.org/10.13881/j.cnki.hljxmsy.2011.07.048

[45] JibinZhu. Investigation of Toxoplasma gondii infection in pigs in Hebei Province. Journal of Hebei North University, 2006, 22: 46-48

[46] Jingqing, Liu, Zhang Liang, and Yuan Tao. 2010. Seroepidemiological investigation and analysis of porcine toxoplasmosis, Veterinary Guide, 25–26. https://doi.org/10.3969/j.issn.1673-8586.2010.04.012

[47] JinlongShao. Serological investigation and analysis of toxoplasmosis in some pig farms in Xiamen. Fujian Animal Husbandry and Veterinary Medicine, 2017, 39: 12-13

[48] Jinshui, Tong. 2014. Serological investigation and analysis of Toxoplasma gondii in pig farms in Longyan City, Fujian Agriculture And Forestry University.

[49] Jinzhou, You, Zhang Ruizhen, Qiu Jianlong, Xie Min, and Hu Lingying. 2015. Epidemiological investigation report on swine toxoplasmosis in Fujian Province, Contemporary Animal Husbandry, 22–23. CNKI:SUN:DDXM.0.2015–06–017

[50] JunWang, JunjuanShan, WenshengJiang, ZhiqiangLuo, Zheng ChaofengGu, Xi, and Zhou Huaping. . Serological investigation and analysis of pig toxoplasmosis in the third agricultural division. Chinese Journal of Animal Quarantine, 2011, 28: 62-63

[51] Junwei, Liu, Jiang Jinqing, Li Xuehua, Si Hongying, and Gu Qiaoling. 2010. Serological investigation and analysis of Toxoplasma gondii infection in pigs awaiting slaughter in Xinxiang City, Modern Agricultural Sciences and Technology, 294+96. https://doi.org/10.3969/j.issn.1007-5739.2010.18.182

[52] Kaichao, Hu. 2020. Detection and analysis of serum antibodies against porcine toxoplasmosis in some areas of Pingdingshan City, Rural Science and Technology, 111–12. https://doi.org/10.19345/j.cnki.1674-7909.2020.21.056

[53] Kouguan, Ye, Fan Feng, Cui Hongping, and Zhou Qingxin. 2004. Serological investigation of Toxoplasma gondii infection in commercial slaughtered pigs in Wuxi area, Livestock and poultry industry, 43. https://doi.org/10.19567/j.cnki.1008-0414.2004.05.022

[54] Kun, Liu. 2013a. Serological investigation and analysis of pig toxoplasmosis in Xinyang area, Henan Agricultural Science, 42: 166–68. https://doi.org/10.15933/j.cnki.1004-3268.2013.05.042

[55] Kun, Wang. 2013b. Investigation on the infection of toxoplasma gondii in some animals in fujian province and study on the genotypes of Toxoplasma gondii from pigs, Fujian Agriculture And Forestry University.

[56] LeiZhou. Summary of pig toxoplasmosis. Foreign Zootechnics: Pig and Poultry, 2021, 41: 103-105

[57] LiYN, NieX, PengQY, MuXQ, ZhangM, TianMY, S. J. Min. Seroprevalence and Genotype of Toxoplasma Gondii in Pigs, Dogs and Cats from Guizhou Province, Southwest China, Parasit Vectors, 2015, 8: 214

[58] Lifei, Du, Li Jie, Ren Huibo, Qiu Meizhen, Wang Hui, Yang Jun, and Zhou Wangping. 2018. Infection of Toxoplasma gondii in some pig farms in Hunan Province and its impact on production performance, Heilongjiang animal science and veterinary medicine, 95–97+100. https://doi.org/10.13881/j.cnki.hljxmsy.2017.09.0038

[59] LijunLiu, YimingTian, JianZhang, XiaoboZhao, JieLin. Serological Investigation of Porcine Toxoplasmosis in Dazhou City. Animal Health in China, 2015, 17: 72-74

[60] LimonG, BeauvaisW, DadiosN, VillenaI, CockleC, BlagaR, GuitianJ. Cross-Sectional Study of Toxoplasma gondii Infection in Pig Farms in England. Foodborne Pathogens and Disease, 2017, 14: 269-281

[61] Lin, Wang, Zhao Ge, Zhao Jianmei, Gao Yubin, Yan Shikang, Li Yuehua, Liu Na, Zhang Qingqing, Huang Xiumei, Liu Junhui, and Wang Junwei. 2020. Detection of Trichinella spiralis and Toxoplasma gondii in slaughtered pigs in some regions of China in 2019, Chinese Journal of Animal Quarantine, 37: 1–4+22. CNKI:SUN:ZGDW.0.2020–05–001

[62] LiuX, LiuC, LiuY, JinH, ZhaoY, ChenJ, YangM, LiuQ. Seroprevalence of Toxoplasma gondii infection in slaughtered pigs and cattle in Liaoning Province, northeastern China. Journal of Parasitology, 2012, 98: 440-441

[63] LiyaLiu, PingWang, JieWang, KaizaShaylan, YinghongJin, GuiliLu. Monitoring and analysis of Toxoplasma gondii antibodies in large-scale pig farms in some areas of Xinjiang. Progress in Veterinary Medicine, 2016, 37: 130-132

[64] Lizhong, Hua, Wei Debao, Wang Jia, Xiong Qiyan, Feng Zhixin, Liu Maojun, Wang Li, and Shao Guoqing. 2016. Serological investigation of porcine Toxoplasma gondii in Northeast and North China, Chinese Journal of Preventive Veterinary Medicine, 38: 124–27+41. https://doi.org/10.3969/j.issn.1008-0589.2016.02.09

[65] Longbai, Wang, Zhou Lunjiang, Wei Hong, Che Yongliang, Chen Shaoying, and Zhuang Xiangsheng. 2007. Epidemiological investigation of swine toxoplasmosis in Fujian Province, Journal of Animal Science and Veterinary Medicine, 4–5. https://doi.org/10.3969/j.issn.1004-6704.2007.03.002

[66] Meijing, Zhang. 2022. Investigation report on the infection of Toxoplasma gondii in pigs in Miyun area, Animal husbandry environment, 29–30.

[67] MengKong. Serological Investigation of Animal Toxoplasmosis in Some Areas of Jiangsu Province and Establishment of Artificial Disease Models of Swine Toxoplasmosis. Nanjing Agricultural University, 2009

[68] MinLiu, BaoyunWan, JianhongWei, FanfanShu, JianfaYang, FengcaiZou. Serological investigation of toxoplasmosis in Tibetan pigs in Yunnan. Chinas Livestock and Poultry Breeding Industry, 2011, 7: 111-112

[69] MontoyaJG, LiesenfeldO. Toxoplasmosis. Lancet, 2004, 363: 1965-1976

[70] Na, Yang, Xing Mengen, Wang Dawei, Li Hongkui, Li Dechen, and Wu Yuanhua. 2017. Detection and analysis of serum antibodies against porcine Toxoplasma gondii in Liaoning Province, Progress in Veterinary Medicine, 38: 125–28. https://doi.org/10.16437/j.cnki.1007-5038.2017.04.026

[71] Na, Yang, Ding Yingying, Li Jiaqi, Li Chenghuan, Wu Anhe, Xing Mengen, Wang Dawei, Guo Xiaogai, and Wu Yuanhua. 2019. Investigation on the current situation of porcine Toxoplasma gondii infection and analysis of infection factors in Liaoning Province, Journal of Shenyang Agricultural University, 50: 476–80. CNKI:SUN:SYNY.0.2019–04–014

[72] NieLB, GongQL, WangQ, ZhangR, ShiJF, YangY, LiJM, ZhuXQ, ShiK, DuR. Prevalence of Toxoplasma gondii infection in chickens in China during 1993–2021: A systematic review and meta-analysis. Parasitology Research, 2022, 121: 287-301

[73] NiningHong, DexingQian, DengxiangZhang, YingHua, TaoLi, LongzhongRan, HairongTian, XiaLiu, TiandeYu. Serological Investigation of Porcine Toxoplasmosis in Guizhou Province. Chinese Journal of Animal Infectious Diseases, 2010, 18: 68-70

[74] OlsenA, BergR, TagelM, MustK, DeksneG, EnemarkHL, AlbanL, JohansenMV, NielsenHV, SandbergM, et al.. Seroprevalence of Toxoplasma gondii in domestic pigs, sheep, cattle, wild boars, and moose in the Nordic-Baltic region: A systematic review and meta-analysis. Parasite Epidemiol Control, 2019, 5, e00100

[75] PageMJ, McKenzieJE, BossuytPM, BoutronI, HoffmannTC, MulrowCD, ShamseerL, TetzlaffJM, AklEA, BrennanSE, et al.. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ, 2021, 372, n71

[76] PappasG, RoussosN, FalagasME. Toxoplasmosis snapshots: Global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. International Journal for Parasitology, 2009, 39: 1385-1394

[77] Peng, Yan, Shang Xuedong, Tian Zhongyuan, and Hua Lizhong. 2020. Serological investigation of Toxoplasma gondii infection in large-scale pig farms in Zhejiang and Hebei provinces, Modern Animal Husbandry and Veterinary Medicine, 50–53. CNKI:SUN:LNXM.0.2020–01–014

[78] Pig production and pork production have returned in 2021, China. 2022. Northern animal husbandry, 6.

[79] Qijun, Tan, Li Yan, Nie Kui, Zeng Zheng, and Yang Zelin. 2008. Seroepidemiological investigation of Toxoplasma gondii in pigs in Chongqing area, Progress in Veterinary Medicine, 109–10+15. https://doi.org/10.16437/j.cnki.1007-5038.2008.07.005

[80] Qin, Zhang. 2016. Serological investigation of Toxoplasma gondii in some regions of China, Anhui Agricultural University. CNKI:CDMD:2.1016.258420

[81] Qingna, Wen, Guo Yanhua, Yang Jufeng, Shen Hong, and Du Yingchun. 2015. Serological investigation of porcine Toxoplasma gondii infection in Henan Province, Chinese Journal of Veterinary Medicine, 51: 44–45. CNKI:SUN:ZSYZ.0.2015–04–015.

[82] Rahman, M., B. Devriendt, I. Gisbert Algaba, B. Verhaegen, P. Dorny, K. Dierick, and E. Cox. 2019. QuilA-Adjuvanted T. gondii lysate antigens trigger robust antibody and IFNγ(+) T-Cell responses in pigs leading to reduction in parasite DNA in tissues upon challenge infection, Front Immunol, 10: 2223. https://doi.org/10.3389/fimmu.2019.02223

[83] RentongWang Epidemiological investigation of swine toxoplasmosis in Lushunkou District, 2020 Dalian City Shenyang Agricultural University

[84] RuiYang, PeizhenLi, XupengYue, Xia QiangDu, YanxinLianfeng, Lu, YeLiao, JinjinGuo. Meta-analysis on the prevalence of Toxoplasma gondii and the relationship with reproductive disorder in male population in China. Chinese Journal of Zoonozoology, 2016, 32: 810-818

[85] Sanke, Yu, Lin Qing, Liu Yongqing, and Wang Xuyu. 2000. Serological investigation of porcine Toxoplasmosis in Yangling district, Shaanxi Province, Progress in Veterinary Medicine, 57–59. CNKI:SUN:DYJZ.0.2000–02–014

[86] ShaominJiang, YapingChen, TianqiWang. Serological Investigation and Analysis of Swine Toxoplasmosis in Yichuan County. Journal of Animal Science and Veterinary Medicine, 2009, 28: 35-36

[87] SuYJ, MaZD, QiaoX, WangPT, KangYT, YangNA, JiaW, ZhaoZJ. Geospatial epidemiology of Toxoplasma gondii infection in livestock, pets, and humans in China, 1984–2020. Parasitology Research, 2022, 121: 743-750

[88] TaoQ, WangZ, FengH, FangR, NieH, HuM, ZhouY, ZhaoJ. Seroprevalence and risk factors for Toxoplasma gondii infection on pig farms in central China. Journal of Parasitology, 2011, 97: 262-264

[89] Tao, Jiang, He Huishi, Zhao Nianbiao, Han Youyuan, and Zhao Junlong. 2007. Serological investigation of Toxoplasma gondii infection in some pig farms in Hubei Province, Hubei Journal of Animal and Veterinary Sciences, 22+25. https://doi.org/10.16733/j.cnki.issn1007-273x.2007.06.010

[90] Tianqi, Wang, Dong Faming, Pan Yaoqian, Zhang Ling, and Fang Jiapei. 2006. Serological investigation and analysis of pig toxoplasmosis in Luoyang area, Hubei Journal of Animal and Veterinary Sciences, 29–30. https://doi.org/10.16733/j.cnki.issn1007-273x.2006.09.016

[91] TorgersonPR, MastroiacovoP. The global burden of congenital toxoplasmosis: A systematic review. Bulletin of the World Health Organization, 2013, 91: 501-508

[92] WangD, LiuY, JiangT, ZhangG, YuanG, HeJ, SuC, YangN. Seroprevalence and genotypes of Toxoplasma gondii isolated from pigs intended for human consumption in Liaoning province, northeastern China. Parasites & Vectors, 2016, 9: 248

[93] WangYG, GuiBZ, LiRC, WangGP, GeM, LiuGH. Seroprevalence and Risk Factors of Toxoplasma gondii Infection in Growth Stages of Pigs in Hunan Province. Subtropical China, Vector Borne Zoonotic Dis, 2019, 19: 945-949

[94] WangW, GongQL, LiMH, WeiXY, ChenY, JiangJ, NiHB, LyuC, WangCR. The prevalence of Toxoplasma gondii in sheep in China: A systematic review and meta-analysis. Research in Veterinary Science, 2021, 138: 19-29

[95] WangqiangShi Investigation and Analysis on the Infection Status of Pig Intestinal Parasites and Toxoplasma gondii in Large Scale Farms in Dafeng District, 2018 Yancheng City Yangzhou University

[96] Weitao, Xie, Qiao Songlin, Liang Yue, Hao Huifang, Deng Ruiguang, Zhang Longxian, Li Xiangrui, and Zhang Gaiping. 2019. Seroepidemiological survey of Toxoplasma gondii in large-scale pig farms in Henan Province from 2017 to 2018, Chinese Journal of Veterinary Medicine, 39: 2179–83+89. https://doi.org/10.16303/j.cnki.1005-4545.2019.11.15

[97] Wenxun, Gao, Li Kun, Han Zhaoqing, Wang Xiaoqiang, Wang Lei, Zhang Hui, Lan Yanfang, Liu Xinyu, and Li Jiakui. 2016. Report on serum detection of Toxoplasma gondii in Tibetan pigs in some areas of Tibet, Hubei Animal Husbandry and Veterinary Medicine, 37: 5–6. https://doi.org/10.16733/j.cnki.issn1007-273x.2016.03.001

[98] WuD, LvR, SunX, ShuF, ZhouZ, NieK, DuanG, ZouF. Seroprevalence of Toxoplasma gondii antibodies from slaughter pigs in Chongqing. China, Trop Anim Health Prod, 2012, 44: 685-687

[99] WuF, WangYL, YangZ, LiXL, LiZR, LinQ. Seroprevalence and Risk Factors of Toxoplasma gondii in Slaughter Pigs in Shaanxi Province. Northwestern China, Vector Borne Zoonotic Dis, 2017, 17: 517-519

[100] Wenyu, Jia, Wei Yuming, and Qian Zhenbo. 2017. Epidemiological and serological investigation of major swine epidemic diseases in Zhangye City, Journal of Animal Science and Veterinary Medicine, 36: 73–75+78.

[101] Xia, Xue, Li Kaihang, Deng Bo, and Sun Quanyun. 2009. Serological investigation of toxoplasmosis in large-scale pig farms in Shanghai, Progress in Veterinary Medicine, 30: 28–31. https://doi.org/10.16437/j.cnki.1007-5038.2009.03.022

[102] Xiangyan, Ren. 2022. Investigation on the occult infection of Toxoplasma gondii in some coastal areas of Shandong Province, Shandong Animal Husbandry and Veterinary Medicine, 43: 16–17+20. https://doi.org/10.3969/j.issn.1007-1733.2022.07.006

[103] Xianpeng, Zhang, Li Yue, Wen Qingping, and Lai Xiaoxian. 2006. Serological investigation of 5 pig diseases in Dongguan city, Progress in Veterinary Medicine, 111–12. https://doi.org/10.16437/j.cnki.1007-5038.2006.01.031

[104] Xiaodong, Shao, Yuan Lin, Zhai Kai, Qian Weifeng, Yan Wenchao, and Wang Tianqi. 2014. Seroepidemiological investigation and PCR detection of porcine toxoplasmosis in Luoyang area, Heilongjiang animal science and veterinary medicine, 0: 75–77. https://doi.org/10.13881/j.cnki.hljxmsy.2014.0737

[105] Xiaolan, Li, Bu Yuming, Xie Ping, and Hu Shijun. 2010. Serological investigation of toxoplasmosis in some pig farms in Sichuan province, Contemporary Livestock and Poultry Breeding Industry, 17–19. https://doi.org/10.14070/j.cnki.151150.2010.01.015

[106] Xiaowei, Yang, and Zhao Guangwei. 2015. Investigation and analysis of Toxoplasma gondii infection in pigs at different feeding stages in Chongqing area, Chinese Journal of Veterinary Medicine, 51: 44–45. CNKI:SUN:ZSYZ.0.2015–02–015

[107] Xiaoyun, Mi, Bayncha Khan, and Li Wenchao. 2007. Serological investigation of toxoplasmosis in pigs, cattle, and sheep in Xinjiang, Chinese Journal of Veterinary Parasitology, 22–24.

[108] Xingping, Cao. 2000. Serological investigation of toxoplasmosis in pigs and cattle, Contemporary Animal Husbandry, 21–22.

[109] Xiuyong, Ou, Long Zongkang, Peng Yihui, Qian Dexing, and Long Wenbo. 2003. Epidemiological investigation of pig toxoplasmosis in Sansui County, Guizhou Province, Chinese Journal of Veterinary Parasitology, 37–56. https://doi.org/10.3969/j.issn.1674-6422.2003.01.011

[110] XuY, LiRC, LiuGH, CongW, ZhangXX, YuXL, ZhuXQ. Seroprevalence of Toxoplasma gondii infection in sows in Hunan province, China. The Scientific World Journal, 2014, 2014, 347908

[111] Xu, P., Y. N. Cai, X. Leng, J. Wang, W. Ma, G. D. Mu, J. Jiang, X. Y. Liu, Z. D. Wang, Q. Zhao, and G. L. Yang. 2015. Seroprevalence of Toxoplasma gondii infection in pigs in Jilin Province, Northeastern China, Trop Biomed, 32: 116–20. PMID: 25801260. https://pubmed.ncbi.nlm.nih.gov/25801260/

[112] XueyuanChao, QuanhuiGuo. Serological investigation of pig toxoplasmosis in Ledu, Qinghai. Chinese Journal of Veterinary Medicine, 2008, 44: 40

[113] Xufeng, Suo, Liu Jianjie, Wang Dalin, Gu Pin, Li Bisi, Wang Meiyan, and Wu Lianyu. 2006. Seroepidemiological investigation of toxoplasmosis in pig farms in Hainan Province, Journal of Pig Breeding, 36–37.

[114] Yangsha, Yin, Li Guiyun, Wu Yongyin, Dong Baoyu, Wang Jiaming, and Meng Bingchao. 2015. Serological investigation of pig toxoplasmosis in Qiannan Prefecture, Contemporary Animal Husbandry, 81–82.

[115] Yanhong, Qiu, and Lin Qing. 2007. Serological investigation and analysis of toxoplasmosis in some pig farms in Fuzhou City, Journal of Pig Breeding, 62–63. https://doi.org/10.3969/j.issn.1002-1957.2007.04.032

[116] Yanqiu, Zhu, and Yang Desheng. 2005. Seroepidemiological investigation and analysis of porcine Toxoplasmosis, Journal of Pig Breeding, 22–24. https://doi.org/10.3969/j.issn.1002-1957.2005.04.012

[117] Yijuan, Fu. 2003. Detection of serum antibodies against toxoplasmosis in pigs, cattle, and sheep in Qinghai Province, China Veterinary Science and Technology, 33: 68–69. https://doi.org/10.16656/j.issn.1673-4696.2003.09.026

[118] Ying, Li, Li Zengkui, Kang Ming, Li Yongjian, and Fu Jianchao. 2010. Serological investigation of pig toxoplasmosis in Huzhu County, Heilongjiang animal science and veterinary medicine, 75–76. https://doi.org/10.13881/j.cnki.hljxmsy.2010.16.028

[119] Yizhi, Mao, Wang Xingqun, Zhao Fuwei, Wu Botao, Chen Nengqiao, and Xu Quanzhong. 2013. Serological investigation of 7 epidemic diseases in some large-scale pig farms in Zunyi City, Anhui Agricultural Science, 41: 5366+69. https://doi.org/10.13989/j.cnki.0517-6611.2013.12.160

[120] YongjuanKuang. Investigation and Control of Swine Toxoplasmosis in Shenzhen City. China Veterinary Science and Technology, 2002, 32: 37-38

[121] YongjunChen, WangquanJiang Wei, YingchunLiu, ZhenyuJing, YenaYan. Epidemiological investigation of Toxoplasma gondii in pigs in Shanghai. Chinese Journal of Animal Infectious Diseases, 2010, 18: 54-58

[122] Yongmin, Liao. 2020. Serological investigation and analysis of swine Toxoplasmosis in Miluo city, Hunan Province from 2017 to 2019, Journal of Pig Breeding, 105–06

[123] Yongsen, Dong, Pan Yingqing, Fan Xiulan, Zhang Guocang, and Liu Xiuqing. 2010. Seroepidemiological investigation of porcine Toxoplasmosis in Qinghai Province, Heilongjiang animal science and veterinary medicine, 83–84. https://doi.org/10.13881/j.cnki.hljxmsy.2010.24.023

[124] YuHJ, ZhangZ, LiuZ, QuDF, ZhangDF, ZhangHL, ZhouQJ, DuAF. Seroprevalence of Toxoplasma gondii infection in pigs. Zhejiang Province, China, J Parasitol, 2011, 97: 748-749

[125] YunJiang, LiangxianWu. Serological investigation of Toxoplasma gondii infection in some pig farms in Xinluo District. Longyan City, Fujian Animal Husbandry and Veterinary Medicine, 2011, 33: 6-7

[126] Yutong, Wu, Xiao Fangping, and Xie Lili. 2015. Analysis of serological detection methods for porcine toxoplasmosis in Guiyang area, Veterinary Guide, 0: 54–55. https://doi.org/10.3969/j.issn.1673-8586.2015.10.049

[127] Yuxian, Su. 2019. Serological investigation and analysis of Toxoplasma gondii in some pig farms in Pingdingshan City, Henan Province, Journal of Pig Breeding, 125–26. https://doi.org/10.13257/j.cnki.21-1104/s.2019.02.048

[128] Zechuan, Cai, Li Fuhuang, Hu Ping, Guan Wenyi, Li Changjun, and Cao Pujun. 2017. Serological investigation and analysis of toxoplasma gondii infection in some pig farms in the suburbs of Beijing, Heilongjiang animal science and veterinary medicine, 103–04. https://doi.org/10.13881/j.cnki.hljxmsy.2017.0684

[129] ZhangXX, ZhaoQ, ShiCW, YangWT, JiangYL, WeiZT, WangCF, YangGL. Seroprevalence and associated risk factors for Toxoplasma gondii infection in the Korean. Manchu, Mongol and Han Ethnic Groups in Eastern and Northeastern China, Epidemiol Infect, 2016, 144: 2018-2024

[130] ZhangXX, RenWX, TanQD, HouG, FeiYC, ZhaoLJ, ZhaoQ, SunD. Meta-analysis of Toxoplasma gondii in pigs intended for human consumption in Mainland China. Acta Tropica, 2019, 198, ArticleID: 105081

[131] ZhangY, GongH, MiR, HuangY, HanX, XiaL, LiS, JiaH, ZhangX, SunT, WangX, ChenZ. Seroprevalence of Toxoplasma gondii infection in slaughter pigs in Shanghai, China. Parasitology International, 2020, 76 ArticleID: 102094

[132] ZhangL, WangX, LiuM, FengG, ZengY, WangR, XieZ. The epidemiology and disease burden of congenital TORCH infections among hospitalized children in China: A national cross-sectional study. PLoS Neglected Tropical Diseases, 2022, 16, e0010861

[133] ZhangY, MiR, XieJ, JiaH, LingH, ZhangX, LuoL, GongH, HanX, HuangY, ZengZ, ChenZ. Seroprevalence and the Risk Factor of Toxoplasma gondii Infection to Slaughter Pigs in Chongqing. China, Vector Borne Zoonotic Dis, 2022, 22: 238-243

[134] ZhenboYang, DiaolanMo, HuicongHuang. Epidemiological investigation and analysis of Toxoplasma gondii in pigs in Dongguan from 2010 to 2016. Rural Economy and Technology, 2017, 28: 44-45

[135] ZhengmaoXu, UrnaMing, MengliLiu, QianlinChen, KhanBayncha. Serological detection of porcine toxoplasmosis in Bazhou region. Xinjiang, Animal Husbandry & Veterinary Medicine, 2016, 48: 114-115

[136] ZhenyingLin, TianfangWang, PingZhou, CaiqingLuo, ShoushengQiu, HuaquanZhang. Serological investigation of toxoplasmosis in some pig farms in Longyan area. Fujian Animal Husbandry and Veterinary Medicine, 2008, 30: 7-8

[137] Zhongju, Xiang, Duan Yonglan, Yue Xinjun, and Chen Pengju. 2011. Serological investigation of porcine Toxoplasmosis in some areas of Anhui Province, Hunan Agricultural Sciences, 134–35+38. https://doi.org/10.16498/j.cnki.hnnykx.2011.17.044

[138] Zhongxing, Zhao, Fan Feng, Zhou Yonghua, and Liu Xiaobing. 2003. Serological investigation of toxoplasma gondii infection in pigs in Wuxi area, Chinese Journal of Schistosomiasis Control, 417–21. https://doi.org/10.16250/j.32.1374.2003.06.009

[139] ZhouDH, LiangR, YinCC, ZhaoFR, YuanZG, LinRQ, SongHQ, ZhuXQ. Seroprevalence of Toxoplasma gondii in pigs from southern China. Journal of Parasitology, 2010, 96: 673-674

[140] ZhouP, ChenZ, LiHL, ZhengH, HeS, LinRQ, ZhuXQ. Toxoplasma gondii infection in humans in China. Parasites & Vectors, 2011, 4: 165

[141] ZouFC, SunXT, XieYJ, LiB, ZhaoGH, DuanG, ZhuXQ. Seroprevalence of Toxoplasma gondii in pigs in southwestern China. Parasitology International, 2009, 58: 306-307

[142] Zuhong, Deng, Yang Jianfa, Sun Xiutao, Xie Yinjie, Zhao Guohong, Duan Gang, and Zou Fengcai. 2010. Serological investigation of pig toxoplasmosis, Chinese Animal Husbandry and Veterinary Medicine, 225–26.

Funding

Key Technologies Research and Development Program(2022YFE0114400)

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