Hostname: page-component-848d4c4894-2pzkn Total loading time: 0 Render date: 2024-06-06T04:30:07.371Z Has data issue: false hasContentIssue false

Toxoplasma gondii infection in pork produced in France

Published online by Cambridge University Press:  01 March 2016

V. DJOKIC
Affiliation:
Ecole Nationale Vétérinaire d'Alfort, ANSES, INRA, Université Paris-Est, Laboratoire de santé animale de Maisons-Alfort, UMR BIPAR, Maisons-Alfort, France Institute for Medical Research, National Reference Laboratory for Toxoplasmosis, University of Belgrade, Dr. Subotića 4, P.O. Box 102, Belgrade 11129, Serbia
R. BLAGA
Affiliation:
Ecole Nationale Vétérinaire d'Alfort, ANSES, INRA, Université Paris-Est, Laboratoire de santé animale de Maisons-Alfort, UMR BIPAR, Maisons-Alfort, France
D. AUBERT
Affiliation:
Université Reims Champagne-Ardenne, Laboratoire de Parasitologie-Mycologie, EA 3800, SFR CAP-SANTE, Centre National de Référence de la Toxoplasmose, Centre de Ressources Biologiques Toxoplasma, Hôpital Maison Blanche, Reims, France
B. DURAND
Affiliation:
ANSES, Université Paris-Est, Laboratoire de santé animale de Maisons-Alfort, Epidemiology Unit, Maisons-Alfort, France
C. PERRET
Affiliation:
ANSES, Ecole Nationale Vétérinaire d'Alfort, INRA, Université Paris-Est, Laboratoire de santé animale de Maisons-Alfort, UMR BIPAR, Maisons-Alfort, France
R. GEERS
Affiliation:
Université Reims Champagne-Ardenne, Laboratoire de Parasitologie-Mycologie, EA 3800, SFR CAP-SANTE, Centre National de Référence de la Toxoplasmose, Centre de Ressources Biologiques Toxoplasma, Hôpital Maison Blanche, Reims, France
T. DUCRY
Affiliation:
ANSES, Ecole Nationale Vétérinaire d'Alfort, INRA, Université Paris-Est, Laboratoire de santé animale de Maisons-Alfort, UMR BIPAR, Maisons-Alfort, France
I. VALLEE
Affiliation:
ANSES, Ecole Nationale Vétérinaire d'Alfort, INRA, Université Paris-Est, Laboratoire de santé animale de Maisons-Alfort, UMR BIPAR, Maisons-Alfort, France
O. DJURKOVIC DJAKOVIC
Affiliation:
Institute for Medical Research, National Reference Laboratory for Toxoplasmosis, University of Belgrade, Dr. Subotića 4, P.O. Box 102, Belgrade 11129, Serbia
A. MZABI
Affiliation:
Université Reims Champagne-Ardenne, Laboratoire de Parasitologie-Mycologie, EA 3800, SFR CAP-SANTE, Centre National de Référence de la Toxoplasmose, Centre de Ressources Biologiques Toxoplasma, Hôpital Maison Blanche, Reims, France
I. VILLENA
Affiliation:
Université Reims Champagne-Ardenne, Laboratoire de Parasitologie-Mycologie, EA 3800, SFR CAP-SANTE, Centre National de Référence de la Toxoplasmose, Centre de Ressources Biologiques Toxoplasma, Hôpital Maison Blanche, Reims, France
P. BOIREAU*
Affiliation:
ANSES, Ecole Nationale Vétérinaire d'Alfort, INRA, Université Paris-Est, Laboratoire de santé animale de Maisons-Alfort, UMR BIPAR, Maisons-Alfort, France
*
*Corresponding author: ANSES, Ecole Nationale Vétérinaire d'Alfort, INRA, Université Paris-Est, Laboratoire de santé animale de Maisons-Alfort, UMR BIPAR, Maisons-Alfort, France. E-mail: pascal.boireau@anses.fr

Summary

The aim of this study was to assess the seroprevalence of the Toxoplasma gondii parasite in pork produced in France, and to determine infection risk factors. An innovative survey was designed based on annual numbers of slaughtered pigs from intensive and outdoor farms in France. A total of 1549 samples of cardiac fluids were collected from pig hearts to determine seroprevalence using a Modified Agglutination Test. Of those, 160 hearts were bio-assayed in mice to isolate live parasites. The overall seroprevalence among fattening pigs was 2·9%. The adjusted seroprevalence in pigs from intensive farms was 3·0%; the highest in sows (13·4%); 2·9% in fattening pigs and 2·6% in piglets. Adjusted seroprevalence in fattening animals from outdoor farms was 6·3%. Strains were isolated from 41 animals and all were genotyped by Restriction Fragment Length Polymorphism as type II. Risk-factor analysis showed that the risk of infection was more than three times higher for outdoor pigs, and that sows’ risk was almost five times higher than that of fattening animals. This study provides further evidence of extensive pork infection with T. gondii regardless of breeding systems, indicating that farm conditions are still insufficient to guarantee ‘Toxoplasma-free pork’.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

AFSSA (2005). Toxoplasmose : état des connaissances et évaluation du risque lié à l'alimentation Rapport du groupe de travail “Toxoplasma gondii” de l'Afssa. 318.Google Scholar
Alvarado-Esquivel, C., Romero-Salas, D., Garcia-Vazquez, Z., Crivelli-Diaz, M., Barrientos-Morales, M., Lopez-de-Buen, L. and Dubey, J. P. (2014). Seroprevalence and correlates of Toxoplasma gondii infection in domestic pigs in Veracruz State, Mexico. Tropical Animal Health and Production 46, 705709.Google Scholar
Association BD PORC (2012). Rapport du commissaire aux comptes sur les comptes annuels.Google Scholar
Association BD PORC (2013). Rapport du commissaire aux comptes sur les comptes annuels.Google Scholar
Bartova, E. and Sedlak, K. (2011). Seroprevalence of Toxoplasma gondii and Neospora caninum in slaughtered pigs in the Czech Republic. Parasitology 138, 13691371.Google Scholar
Belfort-Neto, R., Nussenblatt, V., Rizzo, L., Muccioli, C., Silveira, C., Nussenblatt, R., Khan, A., Sibley, L. D. and Belfort, R. Jr. (2007). High prevalence of unusual genotypes of Toxoplasma gondii infection in pork meat samples from Erechim, Southern Brazil. Anais da Academia Brasilieira Ciencias 79, 111114.Google Scholar
Berger-Schoch, A. E., Herrmann, D. C., Schares, G., Muller, N., Bernet, D., Gottstein, B. and Frey, C. F. (2011). Prevalence and genotypes of Toxoplasma gondii in feline faeces (oocysts) and meat from sheep, cattle and pigs in Switzerland. Veterinary Parasitology 177, 290297.CrossRefGoogle ScholarPubMed
Bezerra, R. A., Carvalho, F. S., Guimaraes, L. A., Rocha, D. S., Maciel, B. M., Wenceslau, A. A., Lopes, C. W. and Albuquerque, G. R. (2012). Genetic characterization of Toxoplasma gondii isolates from pigs intended for human consumption in Brazil. Veterinary Parasitology 189, 153161.Google Scholar
Bobic, B., Jevremovic, I., Marinkovic, J., Sibalic, D. and Djurkovic-Djakovic, O. (1998). Risk factors for Toxoplasma infection in a reproductive age female population in the area of Belgrade, Yugoslavia. European Journal of Epidemiology 14, 605610.Google Scholar
Chikweto, A., Kumthekar, S., Tiwari, K., Nyack, B., Deokar, M. S., Stratton, G., Macpherson, C. N., Sharma, R. N. and Dubey, J. P. (2011). Seroprevalence of Toxoplasma gondii in pigs, sheep, goats, and cattle from Grenada and Carriacou, West Indies. Journal of Parasitology 97, 950951.Google Scholar
Cook, A. J., Gilbert, R. E., Buffolano, W., Zufferey, J., Petersen, E., Jenum, P. A., Foulon, W., Semprini, A. E. and Dunn, D. T. (2000). Sources of toxoplasma infection in pregnant women: European multicentre case–control study. European Research Network on Congenital Toxoplasmosis. BMJ 321, 142147.Google Scholar
de Sousa, R. Á., Lemos, J. F., Farias, L. A., Lopes, C. D. and Dos Santos, K. R. (2014). Seroprevalence and risk factors for Toxoplasma gondii infection in pigs in southern Piauí. Revista Brasileira de Parasitologia Veterinária 23, 98100.CrossRefGoogle ScholarPubMed
de Sousa, S., Ajzenberg, D., Canada, N., Freire, L., da Costa, J. M., Darde, M. L., Thulliez, P. and Dubey, J. P. (2006). Biologic and molecular characterization of Toxoplasma gondii isolates from pigs from Portugal. Veterinary Parasitology 135, 133136.CrossRefGoogle ScholarPubMed
Deksne, G. and Kirjusina, M. (2013). Seroprevalence of Toxoplasma gondii in domestic pigs (Sus scrofa domestica) and wild boars (Sus scrofa) in Latvia. Journal of Parasitology 99, 4447.Google Scholar
Dubey, J. P. (1988). Long-term persistence of Toxoplasma gondii in tissues of pigs inoculated with T. gondii oocysts and effect of freezing on viability of tissue cysts in pork. American Journal of Veterinary Research 49, 910913.Google Scholar
Dubey, J. P. (1998). Refinement of pepsin digestion method for isolation of Toxoplasma gondii from infected tissues. Veterinary Parasitology 74, 7577.CrossRefGoogle ScholarPubMed
Dubey, J. P., Kotula, A. W., Sharar, A., Andrews, C. D. and Lindsay, D. S. (1990). Effect of high temperature on infectivity of Toxoplasma gondii tissue cysts in pork. Journal of Parasitology 76, 201204.CrossRefGoogle ScholarPubMed
Dubey, J. P., Lunney, J. K., Shen, S. K., Kwok, O. C., Ashford, D. A. and Thulliez, P. (1996). Infectivity of low numbers of Toxoplasma gondii oocysts to pigs. Journal of Parasitology 82, 438443.Google Scholar
Dubey, J. P., Hill, D. E., Rozeboom, D. W., Rajendran, C., Choudhary, S., Ferreira, L. R., Kwok, O. C. and Su, C. (2012). High prevalence and genotypes of Toxoplasma gondii isolated from organic pigs in northern USA. Veterinary Parasitology 188, 1418.Google Scholar
Edelhofer, R. (1994). Prevalence of antibodies against Toxoplasma gondii in pigs in Austria–an evaluation of data from 1982 and 1992. Parasitology Research 80, 642644.Google Scholar
Esteban-Redondo, I., Maley, S. W., Thomson, K., Nicoll, S., Wright, S., Buxton, D. and Innes, E. A. (1999). Detection of T. gondii in tissues of sheep and cattle following oral infection. Veterinary Parasitology 86, 155171.Google Scholar
Esteves, F., Aguiar, D., Rosado, J., Costa, M. L., de Sousa, B., Antunes, F. and Matos, O. (2014). Toxoplasma gondii prevalence in cats from Lisbon and in pigs from centre and south of Portugal. Veterinary Parasitology 200, 812.CrossRefGoogle ScholarPubMed
Feitosa, T. F., Vilela, V. L., de Melo, L. R., de Almeida Neto, J. L., Souto, D. V., de Morais, D. F., Athayde, A. C., Azevedo, S. S. and Pena, H. F. (2014). Toxoplasma gondii and Neospora caninum in slaughtered pigs from Northeast, Brazil. Veterinary Parasitology 202, 305309.Google Scholar
Forbes, L. B., Parker, S. E. and Gajadhar, A. A. (2012). Performance of commercial ELISA and agglutination test kits for the detection of anti-Toxoplasma gondii antibodies in serum and muscle fluid of swine infected with 100, 300, 500 or 1000 oocysts. Veterinary Parasitology, 190, 362367.Google Scholar
Frey, C., Berger-Schoch, A., Herrmann, D., Schares, G., Muller, N., Bernet, D., Doherr, M. and Gottstein, B. (2012). Incidence and genotypes of Toxoplasma gondii in the muscle of sheep, cattle, pigs as well as in cat feces in Switzerland. Schweizer Archiv für Tierheilkun 154, 251255.Google Scholar
Garcia-Bocanegra, I., Simon-Grife, M., Dubey, J. P., Casal, J., Martin, G. E., Cabezon, O., Perea, A. and Almeria, S. (2010 a). Seroprevalence and risk factors associated with Toxoplasma gondii in domestic pigs from Spain. Parasitology International 59, 421426.CrossRefGoogle ScholarPubMed
Garcia-Bocanegra, I., Simon-Grife, M., Sibila, M., Dubey, J. P., Cabezon, O., Martin, G. and Almeria, S. (2010 b). Duration of maternally derived antibodies in Toxoplasma gondii naturally infected piglets. Veterinary Parasitology 170, 134136.Google Scholar
Halos, L., Thebault, A., Aubert, D., Thomas, M., Perret, C., Geers, R., Alliot, A., Escotte-Binet, S., Ajzenberg, D., Darde, M. L., Durand, B., Boireau, P. and Villena, I. (2010). An innovative survey underlining the significant level of contamination by Toxoplasma gondii of ovine meat consumed in France. International Journal for Parasitology 40, 193200.Google Scholar
Halova, D., Mulcahy, G., Rafter, P., Turcekova, L., Grant, T. and de Waal, T. (2013). Toxoplasma gondii in Ireland: seroprevalence and novel molecular detection method in sheep, pigs, deer and chickens. Zoonoses and Public Health 60, 168173.Google Scholar
Hill, D. E. and Dubey, J. P. (2013). Toxoplasma gondii prevalence in farm animals in the United States. International Journal for Parasitology 43, 107113.CrossRefGoogle ScholarPubMed
Hill, D. E., Benedetto, S. M., Coss, C., McCrary, J. L., Fournet, V. M. and Dubey, J. P. (2006). Effects of time and temperature on the viability of Toxoplasma gondii tissue cysts in enhanced pork loin. Journal of Food Protection 69, 19611965.Google Scholar
Jiang, T., Gong, D., Ma, L. A., Nie, H., Zhou, Y., Yao, B. and Zhao, J. (2008). Evaluation of a recombinant MIC3 based latex agglutination test for the rapid serodiagnosis of Toxoplasma gondii infection in swines. Veterinary Parasitology 158, 5156.Google Scholar
Kijlstra, A., Eissen, O. A., Cornelissen, J., Munniksma, K., Eijck, I. and Kortbeek, T. (2004). Toxoplasma gondii infection in animal-friendly pig production systems. Investigative Ophthalmology and Visual Science 45, 31653169.CrossRefGoogle ScholarPubMed
Klun, I., Djurkovic-Djakovic, O., Katic-Radivojevic, S. and Nikolic, A. (2006). Cross-sectional survey on Toxoplasma gondii infection in cattle, sheep and pigs in Serbia: seroprevalence and risk factors. Veterinary Parasitology 135, 121131.Google Scholar
Klun, I., Vujanic, M., Yera, H., Nikolic, A., Ivovic, V., Bobic, B., Bradonjic, S., Dupouy-Camet, J. and Djurkovic-Djakovic, O. (2011). Toxoplasma gondii infection in slaughter pigs in Serbia: seroprevalence and demonstration of parasites in blood. Veterinary Research 42, 17.CrossRefGoogle ScholarPubMed
Lehmann, T., Graham, D. H., Dahl, E., Sreekumar, C., Launer, F., Corn, J. L., Gamble, H. R. and Dubey, J. P. (2003). Transmission dynamics of Toxoplasma gondii on a pig farm. Infection, Genetics and Evolution 3, 135141.Google Scholar
Li, X., Wang, Y., Yu, F., Li, T. and Zhang, D. (2010). An outbreak of lethal toxoplasmosis in pigs in the Gansu province of China. Journal of Veterinary Diagnostic Investigation 22, 442444.CrossRefGoogle ScholarPubMed
Lindsay, D. S., Collins, M. V., Holliman, D., Flick, G. J. and Dubey, J. P. (2006). Effects of high-pressure processing on Toxoplasma gondii tissue cysts in ground pork. Journal of Parasitology 92, 195196.CrossRefGoogle ScholarPubMed
Lopes, A. P., Dubey, J. P., Neto, F., Rodrigues, A., Martins, T., Rodrigues, M. and Cardoso, L. (2013). Seroprevalence of Toxoplasma gondii infection in cattle, sheep, goats and pigs from the North of Portugal for human consumption. Veterinary Parasitology 193, 266269.Google Scholar
Markovic, M., Ivovic, V., Stajner, T., Djokic, V., Klun, I., Bobic, B., Nikolic, A. and Djurkovic-Djakovic, O. (2014). Evidence for genetic diversity of Toxoplasma gondii in selected intermediate hosts in Serbia. Comparative Immunology Microbiology and Infectious Diseases 37, 173179.Google Scholar
Mondragon, R., Howe, D. K., Dubey, J. P. and Sibley, L. D. (1998). Genotypic analysis of Toxoplasma gondii isolates from pigs. Journal of Parasitology 84, 639641.Google Scholar
Nogareda, F., Le Strat, Y., Villena, I., De Valk, H. and Goulet, V. (2014). Incidence and prevalence of Toxoplasma gondii infection in women in France, 1980–2020: model-based estimation. Epidemiology and Infection 142, 16611670.CrossRefGoogle ScholarPubMed
Pastiu, A. I., Gyorke, A., Blaga, R., Mircean, V., Rosenthal, B. M. and Cozma, V. (2013). In Romania, exposure to Toxoplasma gondii occurs twice as often in swine raised for familial consumption as in hunted wild boar, but occurs rarely, if ever, among fattening pigs raised in confinement. Parasitology Research 112, 24032407.CrossRefGoogle ScholarPubMed
Piassa, F. R., de Araujo, J. B., da Rosa, R. C., Mattei, R. J., da Silva, R. C., Langoni, H. and da Silva, A. V. (2010). Prevalence and risk factors for Toxoplasma gondii infection in certified and non-certified pig breeding farms in the Toledo microregion, PR, Brazil. Revista Brasileira de Parasitologia Veterinaria 19, 152156.Google Scholar
R development Core Team (2010). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing.Google Scholar
Samico Fernandes, E. F., Samico Fernandes, M. F., Kim, P. C., de Albuquerque, P. P., de Souza Neto, O. L., de, S. S. A., de Moraes, E. P., de Morais, E. G. and Mota, R. A. (2012). Prevalence of Toxoplasma gondii in slaughtered pigs in the state of Pernambuco, Brazil. Journal of Parasitology 98, 690691.Google Scholar
Sroka, J., Wojcik-Fatla, A., Szymanska, J., Dutkiewicz, J., Zajac, V. and Zwolinski, J. (2010). The occurrence of Toxoplasma gondii infection in people and animals from rural environment of Lublin region – estimate of potential role of water as a source of infection. Annals of Agricultural and Environmental Medicine 17, 125132.Google Scholar
Schares, G., Vrhovec, M. G., Pantchev, N., Herrmann, D. C. and Conraths, F. J. (2008). Occurrence of Toxoplasma gondii and Hammondia hammondi oocysts in the faeces of cats from Germany and other European countries. Veterinary Parasitology 152, 3445.Google Scholar
Su, C., Shwab, E. K., Zhou, P., Zhu, X. Q. and Dubey, J. P. (2010). Moving towards an integrated approach to molecular detection and identification of Toxoplasma gondii . Parasitology 137, 111.Google Scholar
Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 12171258.Google Scholar
Torrey, E. F. and Yolken, R. H. (2013). Toxoplasma oocysts as a public health problem. Trends in Parasitology 29, 380384.Google Scholar
Turcekova, L., Antolova, D., Reiterova, K. and Spisak, F. (2013). Occurrence and genetic characterization of Toxoplasma gondii in naturally infected pigs. Acta Parasitologica 58, 361366.Google Scholar
van der Giessen, J., Fonville, M., Bouwknegt, M., Langelaar, M. and Vollema, A. (2007). Seroprevalence of Trichinella spiralis and Toxoplasma gondii in pigs from different housing systems in The Netherlands. Veterinary Parasitology, 148, 371374.Google Scholar
Venturini, M. C., Bacigalupe, D., Venturini, L., Rambeaud, M., Basso, W., Unzaga, J. M. and Perfumo, C. J. (2004). Seroprevalence of Toxoplasma gondii in sows from slaughterhouses and in pigs from an indoor and an outdoor farm in Argentina. Veterinary Parasitology 124, 161165.CrossRefGoogle Scholar
Veronesi, F., Ranucci, D., Branciari, R., Miraglia, D., Mammoli, R. and Fioretti, D. P. (2011). Seroprevalence and risk factors for Toxoplasma gondii Infection on finishing swine reared in the Umbria region, central Italy. Zoonoses and Public Health 58, 178184.Google Scholar
Villari, S., Vesco, G., Petersen, E., Crispo, A. and Buffolano, W. (2009). Risk factors for toxoplasmosis in pigs bred in Sicily, Southern Italy. Veterinary Parasitology 161, 18.Google Scholar
Villena, I., Durand, B., Aubert, D., Blaga, R., Geers, R., Thomas, M., Perret, C., Alliot, A., Escotte-Binet, S., Thebault, A., Boireau, P. and Halos, L. (2012). New strategy for the survey of Toxoplasma gondii in meat for human consumption. Veterinary Parasitology 183, 203208.CrossRefGoogle ScholarPubMed
Vujanic, M., Ivovic, V., Kataranovski, M., Nikolic, A., Bobic, B., Klun, I., Villena, I., Kataranovski, D. and Djurkovic-Djakovic, O. (2011). Toxoplasmosis in naturally infected rodents in Belgrade, Serbia. Vector-Borne and Zoonotic.Diseases 11, 12091211.Google Scholar
Wang, H., Wang, T., Luo, Q., Huo, X., Wang, L., Liu, T., Xu, X., Wang, Y., Lu, F., Lun, Z., Yu, L. and Shen, J. (2012). Prevalence and genotypes of Toxoplasma gondii in pork from retail meat stores in Eastern China. International Journal of Food Microbiology 157, 393397.CrossRefGoogle ScholarPubMed
Wu, S. M., Ciren, D., Huang, S. Y., Xu, M. J., Ga, G., Yan, C., Mahmoud, M. S., Zou, F. C. and Zhu, X. Q. (2012). First report of Toxoplasma gondii prevalence in Tibetan pigs in Tibet, China. Vector-Borne and Zoonotic Diseases 12, 654656.CrossRefGoogle ScholarPubMed
Zakimi, S., Kyan, H., Oshiro, M., Sugimoto, C., Xuenan, X. and Fujisaki, K. (2006). Genetic characterization of GRA6 genes from Toxoplasma gondii from pigs in Okinawa, Japan. Journal of Veterinary Medical Sciences 68, 11051107.Google Scholar
Zhou, D. H., Liang, R., Yin, C. C., Zhao, F. R., Yuan, Z. G., Lin, R. Q., Song, H. Q. and Zhu, X. Q. (2010 a). Seroprevalence of Toxoplasma gondii in pigs from southern China. Journal of Parasitology 96, 673674.Google Scholar
Zhou, P., Nie, H., Zhang, L. X., Wang, H. Y., Yin, C. C., Su, C., Zhu, X. Q. and Zhao, J. L. (2010 b). Genetic characterization of Toxoplasma gondii isolates from pigs in China. Journal of Parasitology 96, 10271029.Google Scholar