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Journal of Integrative Agriculture  2015, Vol. 14 Issue (9): 1838-1844    DOI: 10.1016/S2095-3119(15)61044-9
Animal Science · Veterinary Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Investigation on the co-infections of Toxoplasma gondii with PRRSV, CSFV or PCV-2 in swine in part of China
 Wang Shuai, ZHang Meng, LIU Xin-chao, LIn Tao, Yang Han-chun, YUan Shi-shan, ZHao guang-wei, Ia Hassan, Yan Ruo-feng, Song Xiao-kai, XU Li-xin, LI Xiang-rui
1、College of Veterinary Medicine, Nanjing Agricultural University, Nanjing 210095, P.R.China
2、Key Laboratory of Animal Epidemiology and Zoonosis, Ministry of Agriculture/State Key Laboratory of Agrobiotechnology, Collegeof  Veterinary Medicine, China Agricultural University, Beijing 100193, P.R.China
3、Department of Swine Infectious Diseases, Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences,Shanghai 200241, P.R.China
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摘要  The objective of the present investigation was to estimate the prevalence of Toxoplasma gondii infection and co-infection with porcine reproductive and respiratory syndrome virus (PRRSV), classical swine fever virus (CSFV) and porcine circovirus type 2 (PCV-2) in pigs in China. A total of 372 tissues or serum samples collected from pigs distributed in 9 provinces/ municipalities of China during the period from February 2011 to November 2012 were assayed for T. gondii antigens and antibodies using enzyme linked immunosorbent assay (ELISA) technique, while the PCR was designed for the detection of the PRRSV, CSFV and PCV-2, respectively. The total positive rate of T. gondii, PRSSV, CSFV and PCV-2 was 9.14% (34/372), 50.00% (186/372), 37.10% (138/372) and 3.23% (12/372), respectively. Among the 34 T. gondii positive samples, 26 samples were simultaneously infected with T. gondii and viruses, while the remaining eight samples were infected with T. gondii alone. In addition, the co-infection rate of T. gondii with PRSSV, T. gondii with PRSSV and CSFV, T. gondii with PRSSV and PCV-2, T. gondii with CSFV and PCV-2, T. gondii with PRSSV, CSFV and PCV-2 was 1.61% (6/372), 4.03% (15/372), 0.27% (1/372), 0.27% (1/372) and 0.81% (3/372), respectively. The results of the present survey revealed that PRRSV and CSFV were the common pathogens co-existing with porcine toxoplasmosis in China, and both of them could increase the chances of T. gondii infection in pig. This is the first report of T. gondii co-infections with viruses in pigs. It is very important to understand the interactions of parasite and virus, and can be used as reference data for the control and prevention of co-infections of T. gondii and viruses in pigs.

Abstract  The objective of the present investigation was to estimate the prevalence of Toxoplasma gondii infection and co-infection with porcine reproductive and respiratory syndrome virus (PRRSV), classical swine fever virus (CSFV) and porcine circovirus type 2 (PCV-2) in pigs in China. A total of 372 tissues or serum samples collected from pigs distributed in 9 provinces/ municipalities of China during the period from February 2011 to November 2012 were assayed for T. gondii antigens and antibodies using enzyme linked immunosorbent assay (ELISA) technique, while the PCR was designed for the detection of the PRRSV, CSFV and PCV-2, respectively. The total positive rate of T. gondii, PRSSV, CSFV and PCV-2 was 9.14% (34/372), 50.00% (186/372), 37.10% (138/372) and 3.23% (12/372), respectively. Among the 34 T. gondii positive samples, 26 samples were simultaneously infected with T. gondii and viruses, while the remaining eight samples were infected with T. gondii alone. In addition, the co-infection rate of T. gondii with PRSSV, T. gondii with PRSSV and CSFV, T. gondii with PRSSV and PCV-2, T. gondii with CSFV and PCV-2, T. gondii with PRSSV, CSFV and PCV-2 was 1.61% (6/372), 4.03% (15/372), 0.27% (1/372), 0.27% (1/372) and 0.81% (3/372), respectively. The results of the present survey revealed that PRRSV and CSFV were the common pathogens co-existing with porcine toxoplasmosis in China, and both of them could increase the chances of T. gondii infection in pig. This is the first report of T. gondii co-infections with viruses in pigs. It is very important to understand the interactions of parasite and virus, and can be used as reference data for the control and prevention of co-infections of T. gondii and viruses in pigs.
Keywords:  Toxoplasma gondii       coinfection       PRRSV       CSFV       PCV-2       pig  
Received: 16 January 2015   Accepted:
Fund: 

This work was supported by the Special Fund for Public Welfare Industry of Ministry of Agriculture of China (200903036- 04) and the Priority Academic Program Development of Jiangsu Higher Education Institutions, China (PAPD).

Corresponding Authors:  LI Xiang-rui, Tel/Fax: +86-25-84399000,E-mail: lixiangrui@njau.edu.cn     E-mail:  lixiangrui@njau.edu.cn
About author:  WANG Shuai, Tel: +86-25-84395904, E-mail: tongbaiws1003@163.com;

Cite this article: 

Wang Shuai, ZHang Meng, LIU Xin-chao, LIn Tao, Yang Han-chun, YUan Shi-shan, ZHao guang-wei, Ia Hassan, Yan Ruo-feng, Song Xiao-kai, XU Li-xin, LI Xiang-rui. 2015. Investigation on the co-infections of Toxoplasma gondii with PRRSV, CSFV or PCV-2 in swine in part of China. Journal of Integrative Agriculture, 14(9): 1838-1844.

Chang Q C, Zheng X, Qiu J H, Wang C R, Zhu X Q. 2013.Seroprevalence of Toxoplasma gondii infection in fatteningpigs in northeast China. Journal of Parasitology, 99,544-545

Diao Y X, Ding J B, Jiang S J, Cui Z Z, Chen B L. 2005. PCRdetection of PCV-2 and PRRSV in porcine pleuropneumoniasamples. Acta Microbiologica Sinica, 45, 397-400 (inChinese)

Drew T W. 2000. A review of evidence for immunosuppressiondue to porcine reproductive and respiratory syndrome virus.Veterinary Research, 31, 27-39

Dubey J P. 2010. Toxoplasma gondii infections in chickens(Gallus domesticus): Prevalence, clinical disease, diagnosisand public health significance. Zoonoses and Public Health,57, 60-73

Dubey J P, Urban Jr J F, Davis S W. 1991. Protective immunityto toxoplasmosis in pigs vaccinated with a nonpersistentstrain of Toxoplasma gondii. American Journal of VeterinaryResearch, 52, 1316-1319

Ge X, Wang F, Guo X, Yang H. 2012. Porcine circovirus type2 and its associated diseases in China. Virus Research,164, 100-106

Green L E, Morgan K L. 1991. Toxoplasma abortion in a Guineapig. Veterinary Research, 129, 266-267

Heaslip A T, Nishi M, Stein B, Hu K. 2011. The motility of ahuman parasite, Toxoplasma gondii, is regulated by a novellysine methyltransferase. PLoS Pathogens, 7. doi, 10.1371/journal.ppat.1002201Huang C Q, Lin Y Y, Dai A L, Li X H, Yang X Y, Yuan Z G, Zhu XQ. 2010. Seroprevalence of Toxoplasma gondii infection inbreeding sows in Western Fujian Province, China. TropicalAnimal Health and Production, 42, 115-118

Jiang Y, Shang H, Xu H, Zhu L, Chen W, Zhao L, Fang L.2010. Simultaneous detection of porcine circovirus type 2,classical swine fever virus, porcine parvovirus and porcinereproductive and respiratory syndrome virus in pigs bymultiplex polymerase chain reaction. The VeterinaryJournal, 183, 172-175

Jungersen G, Bille-Hansen V, Jensen L, Lind P. 2001.Transplacental transmission of Toxoplasma gondii inminipigs infected with strains of different virulence. Journalof Parasitology, 87, 108-113

Kim J H, Kang K I, Kang W C, Sohn H J, Jean Y H, Park B K,Kim Y, Kim D Y. 2009. Porcine abortion outbreak associatedwith Toxoplasma gondii in Jeju Island, Korea. Journal ofVeterinary Science, 10, 147-151

Lange A, Blome S, Moennig V, Greiser-Wilke I. 2011.Pathogenesis of classical swine fever-similarities to viralhaemorrhagic fevers: A review. Berliner und MunchenerTierarztliche Wochenschrift, 124, 36-47

Lang H W, Zhang G C, Wu F Q, Zhang C G. 2000. Detection ofserum antibody against postweaning multisystemic wastingsyndrome in pigs. Chinese Journal of Veterinary Scienceand Technology, 30, 3-5 (in Chinese)

Li B, Fang L, Guo X, Gao J, Song T, Bi J, He K, Chen H, XiaoS. 2011. Epidemiology and evolutionary characteristicsof the porcine reproductive and respiratory syndromevirus in China between 2006 and 2010. Journal of ClinicalMicrobiology, 49, 3175-3183

Li B, Zhong N, Peng W, Shang L, Jin H, Liu Q. 2012.Seroprevalence of Toxoplasma gondii infection in dogsin Sichuan Province, southwestern China. Journal ofParasitology, 98, 209-210

Liao R B, Zhao H C, Li W T, Xiao W, Liu Y Y, Liu X L, Li Q,Wang L, He Q G. 2011. Epidemiological investigation ofporcine circovirus diseases. Swine Production, 1, 81-82(in Chinese)

Lin T, Li X, Yao H, Wei Z, Liu R, Deng Y, Zhai S, Li W, Sun L,Long J. 2013. Phylogenetic diversity of classical swine fevervirus (csfv) field isolates from outbreaks in China between2008 and 2011. Asian Journal of Animal & VeterinaryAdvances, 8, 449-460

Moennig V, Floegel-Niesmann G, Greiser-Wilke I. 2003. Clinicalsigns and epidemiology of classical swine fever: A review of new knowledge. The Veterinary Journal, 165, 11-20

Renukaradhya G J, Alekseev K, Jung K, Fang Y, Saif L J.2010. Porcine reproductive and respiratory syndrome virusinducedimmunosuppression exacerbates the inflammatoryresponse to porcine respiratory coronavirus in pigs. ViralImmunology, 23, 457-466

Shang Y, Wang G, Tian H, Yin S, Du P, Wu J, Chen Y, YangS, Jin Y, Zhang K, Liu X. 2012. Molecular epidemiologicalinvestigation of porcine reproductive and respiratorysyndrome virus in Northwest China from 2007 to 2010.Virus Genes, 45, 90-97

Tao Q, Wang Z, Feng H, Fang R, Nie H, Hu M, Zhou Y, ZhaoJ. 2011. Seroprevalence and risk factors for Toxoplasmagondii infection on pig farms in central China. Journal ofParasitology, 97, 262-264

Tu C, Lu Z, Li H, Yu X, Liu X, Li Y, Zhang H, Yin Z. 2001.Phylogenetic comparison of classical swine fever virus inChina. Virus Research, 81, 29-37

Wang H, Wang T, Luo Q, Huo X, Wang L, Liu T, Xu X, Wang Y,Lu F, Lun Z, Yu L, Shen J. 2012. Prevalence and genotypesof Toxoplasma gondii in pork from retail meat stores inEastern China. International Journal of Food Microbiology,157, 393-397

Wu D, Lv R, Sun X, Shu F, Zhou Z, Nie K, Duan G, Zou F.2012. Seroprevalence of Toxoplasma gondii antibodiesfrom slaughter pigs in Chongqing, China. Tropical AnimalHealth and Production, 44, 685-687

Xie J, Cui T, Cui J, Chen Y, Zhang M, Zhou P, Deng S, SuS, Zhang G. 2014. Epidemiological and evolutionarycharacteristics of the PRRSV in Southern China from 2010to 2013. Microbial Pathogenesis, 75, 7-15

Yao W S, Fan X Z, Wang Q, Ning Y B. 2011. Epidemic statusand proposals for prevention and control of classical swinefever in China. Chinese Journal of Veterinary Drug, 45,44-47 (in Chinese)

Yu H J, Zhang Z, Liu Z, Qu D F, Zhang D F, Zhang H L, ZhouQ J, Du A F. 2011. Seroprevalence of Toxoplasma gondiiinfection in pigs, in Zhejiang Province, China. Journal ofParasitology, 97, 748-749

Zhang J, Zhuang J, Liu C, Wang X, Yuan S. 2009. Molecularepidemiology analysis on porcine circovirus type 2 in someregions of China in 2007. Scientia Agricultura Sinica, 42,2949-2957 (in Chinese)

Zhao G, Shen B, Xie Q, Xu L X, Yan R F, Song X K, HassanI A, Li X R. 2012. Detection of Toxoplasma gondii in freerangechickens in China based on circulating antigens andantibodies. Veterinary Parasitology, 185, 72-77

Zhou D H, Liang R, Yin C C, Zhao F R, Yuan Z G, Lin R Q,Song H Q, Zhu X Q. 2010. Seroprevalence of Toxoplasmagondii in pigs from southern China. Journal of Parasitology,96, 673-674
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