Toxoplasma gondii in pork & pork products – too much on our plate?

Main Article Content

Ivana Klun
https://orcid.org/0000-0001-7976-3104
Olgica Djurkovic-Djakovic
https://orcid.org/0000-0001-7521-8598

Abstract

Background. The constant growth of the global population has led to increasing food production, which has been particularly evident in the production of pork in recent years. In 2015, the number of pigs surpassed one billion, and in 2018 a record high of 120 million tonnes of pork was produced worldwide. In spite of the expansion and dominance of specialized industrial farming in developed countries, Toxoplasma gondii infection in pigs as a source of human infection remains an issue in traditional small-scale farming. The disease burden of toxoplasmosis is estimated to be the highest of all parasitic infections and even higher than that of salmonellosis and campylobacteriosis.
Scope and Approach. This paper reviews the latest research on T. gondii-contaminated pork and pork products, published in the past decade. As current methods do not allow for practical and cost-effective detection of T. gondii at slaughter, efforts towards safe meat have focused on the detection of the parasite in pork and ready-to-eat pork products and on post-harvest mitigation measures.
Key Findings and Conclusions. In contrast to recommendations for preventing Trichinella infection, there are no globally applicable standardised and validated inactivation procedures for rendering T. gondii infected pork/pork products safe for consumers. Moreover, there are no EU regulations in place for the prevention of T. gondii infection by consumption of pork and pork products. Recommended actions, both at the producer and consumer levels, include post-harvest processing such as cooking, freezing, and proper salting/curing.

Downloads

Download data is not yet available.

Article Details

How to Cite
Klun, I., & Djurkovic-Djakovic, O. (2021). Toxoplasma gondii in pork & pork products – too much on our plate?. Veterinarski Glasnik, 75(1), 42-56. https://doi.org/10.2298/VETGL200720010K
Section
Mini Review

References

Abdulmawjood A., Rosa S., Taubert A., Bauer C., Failing K., Zahner H., Bülte M. 2014. Investigation of persistence of infectious Toxoplasma gondii in raw sausages using in-house developed and validated real time-PCR. Meat Science, 97(4):542-547. https://doi.org/10.1016/j.meatsci.2014.03.008.

Alves B. F., Oliveira S., Soares H. S., Pena H. F. J., Conte-Junior C. A., Gennari S. M. 2019. Isolation of viable Toxoplasma gondii from organs and Brazilian commercial meat cuts of experimentally infected pigs. Parasitology Research, 118(4):1331-1335. https://doi.org/10.1007/s00436-019-06229-6.

Alves B. F., Gennari S. M., Oliveira S., Soares H. S., Conte-Junior C. A., Dubey J. P., Amaku M., Jesus Pena H. F. 2020. The impact of dry ageing vacuum-packed pork on the viability of Toxoplasma gondii tissue cysts. Food Microbiology, 86:103331. https://doi.org/10.1016/j.fm.2019.103331.

Batz M. B., Hoffmann S., Morris J. G. Jr. 2012. Ranking the disease burden of 14 pathogens in food sources in the United States using attribution data from outbreak investigations and expert elicitation. Journal of Food Protection, 75(7):1278-1291. https://doi.org/10.4315/0362-028X.JFP-11-418.

Bayarri S., Gracia M. J., Lázaro R., Pérez-Arquillué C., Barberán M., Herrera A. 2010. Determination of the viability of Toxoplasma gondii in cured ham using bioassay: influence of technological processing and food safety implications. Journal of Food Protection, 73(12):2239-2243. https://doi.org/10.4315/0362-028x-73.12.2239.

Bayarri S., Gracia M. J., Pérez-Arquillué C., Lázaro R., Herrera A. 2012. Toxoplasma gondii in commercially available pork meat and cured ham: a contribution to risk assessment for consumers. Journal of Food Protection, 75(3):597-600. https://doi.org/10.4315/0362-028X.JFP-11-350.

Bobić B., Jevremović I., Marinković J., Šibalić D., Djurković-Djaković O. 1998. Risk factors for Toxoplasma infection in a reproductive age female population in the area of Belgrade, Yugoslavia. European Journal of Epidemiology, 14(6):605-610. https://doi.org/10.1023/a:1007461225944.

Bobić B., Nikolić A., Klun I., Vujanić M., Djurković-Djaković O. 2007. Undercooked meat consumption remains the major risk factor for Toxoplasma infection in Serbia. Parassitologia, 49(4):227-230.

Bouwknegt M., Devleesschauwer B., Graham H., Robertson L. J., van der Giessen J. W. B. and the Euro-FBP workshop participants. 2018. Prioritisation of food-borne parasites in Europe, 2016. Eurosurveillance, 23(9):pii=17-00161. https://doi.org/10.2807/1560-7917.ES.2018.23.9.17-00161.

Cademartori B. G., Santos L. M. J. F., Oliveira F. C., Quevedo P., Oliveira P. A., Ramos T. S., Rocha A. S. R., Ruas J. L., Farias N. A. R. 2014. Isolation and pathogenicity of Toxoplasma gondii in naturally infected (rustic farm) pigs in Southern Brazil. Veterinary Parasitology, 203(1-2):207-211. https://doi.org/10.1016/j.vetpar.2014.02.009. Epub 2014 Feb 18.

Condoleo R., Rinaldi L., Sette S., Mezher Z. 2018. Risk assessment of human toxoplasmosis associated with the consumption of pork meat in Italy. Risk Analysis, 38(6):1202-1222. https://doi.org/10.1111/risa.12934.

Cook A. J., Gilbert R. E., Buffolano W., Zufferey J., Petersen E., Jenum P. A., Foulon W., Semprini A. E., Dunn D. T. 2000. Sources of Toxoplasma infection in pregnant women: European multicentre case-control study. European Research Network on Congenital Toxoplasmosis. The British Medical Journal,‎ 321(7254):142-147. https://doi.org/10.1136/bmj.321.7254.142.

Costa D. F., Fowler F., Silveira C., Junqueira Nóbrega M., Junqueira Nobrega H. A., Nascimento H., Rizzo L. V., Commodaro A. G., Belfort R. Jr. 2018. Prevalence of Toxoplasma gondii DNA in processed pork meat. Foodborne Pathogens and Disease, 15(11):734-736. https://doi.org/10.1089/fpd.2018.2438.

Cubas-Atienzar A. I., Hide G., Jiménez-Coello M., Ortega-Pacheco A., Smith J. E. 2018. Genotyping of Toxoplasma gondii from pigs in Yucatan, Mexico. Veterinary Parasitology: Regional Studies and Reports, 14:191-199. https://doi.org/10.1016/j.vprsr.2018.10.009.

FAO. 2019. Food Outlook - Biannual Report on Global Food Markets – November 2019. Rome. ISBN: 978-92-5-131932-1.

FAO/WHO [Food and Agriculture Organization of the United Nations/World Health Organization]. 2014. Multicriteria-based ranking for risk management of food-borne parasites. Microbiological Risk Assessment Series No. 23. Rome. pp. 14-22. ISBN: 978-92-5-108199-0.

Deng H., Swart A., Bonačić Marinović A. A., van der Giessen J. W. B., Opsteegh M. 2020. The effect of salting on Toxoplasma gondii viability evaluated and implemented in a quantitative risk assessment of meat-borne human infection. International Journal of Food Microbiology, 314:108380. https://doi.org/10.1016/j.ijfoodmicro.2019.108380.

Djokić V., Blaga R., Aubert D., Durand B., Perret C., Geers R., Ducry T., Vallee I., Djurković-Djaković O., Mzabi A., Villena I., Boireau P. 2016. Toxoplasma gondii infection in pork produced in France. Parasitology, 143(5):557-567. https://doi.org/10.1017/S0031182015001870.

Djurković-Djaković O., Bobić B., Klun I., Nikolić A., Dupouy-Camet J. 2013. Pork as a source of human parasitic infection. Clinical Microbiology and Infection, 19(7):586-594. https://doi.org/10.1111/1469-0691.12162.

Dubey J. P. 1974. Effect of freezing on the infectivity of Toxoplasma cysts in cats. Journal of the American Veterinary Medical Association, 165:534-536.

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(6):910-913.

Dubey J. P. 1998. Advances in the life cycle of Toxoplasma gondii. International Journal of Parasitology 28(7):1019-1024. https://doi.org/10.1016/s0020-7519(98)00023-x.

Dubey J. P. 2001. Oocyst shedding by cats fed isolated bradyzoites and comparison of infectivity of bradyzoites of the VEG strain Toxoplasma gondii to cats and mice. Journal of Parasitology, 87(1):215-219. https://doi.org/10.1645/0022-3395(2001)087[0215:OSBCFI]2.0.CO;2.

Dubey J. P. 2009. Toxoplasmosis in pigs – the last 20 years. Veterinary Parasitology, 164(2-4):89-103. https://doi.org/10.1016/j.vetpar.2009.05.018.

Dubey J. P. 2010. Toxoplasmosis of Animals and Humans (Second edition), CRC Press, Boca Taylor & Francis Group, Boca Raton, London, New York. ISBN: 978-1-4200-9236-3.

Dubey JP, Murrell KD, Fayer R, Schad GA. 1986. Distribution of Toxoplasma gondii tissue cysts in commercial cuts of pork. Journal of the American Veterinary Medical Association, 188(9):1035-1037.

Dubey J. P., Kotula A. W., Sharar A., Andrews C. D., Lindsay D. S. 1990. Effect of high temperature on infectivity of Toxoplasma gondii tissue cysts in pork. Journal of Parasitology, 76(2):201-204.

Dubey J. P., Hill D. E., Sundar N., Velmurugan G. V., Bandini L. A., Kwok O. C., Pierce V., Kelly K., Dulin M., Thulliez P., Iwueke C., Su C. 2008. Endemic toxoplasmosis in pigs on a farm in Maryland: isolation and genetic characterization of Toxoplasma gondii. Journal of Parasitology, 94(1):36-41. https://doi.org/10.1645/GE-1312.1.

Dubey J. P., Hill D. E., Rozeboom D. W., Rajendran C., Choudhary S., Ferreira L. R., Kwok O. C. H., Su C. 2012. High prevalence and genotypes of Toxoplasma gondii isolated from organic pigs in Northern USA. Veterinary Parasitology, 188(1-2):14-18. https://doi.org/10.1016/j.vetpar.2012.03.008.

Foroutan M., Fakhri Y., Riahi S. M., Ebrahimpour S., Namroodi S., Taghipour A., Spotin A., Gamble H. R., Rostami A. 2019. The global seroprevalence of Toxoplasma gondii in pigs: A systematic review and meta-analysis. Veterinary Parasitology, 269:42-52. https://doi.org/10.1016/j.vetpar.2019.04.012.

Franco-Hernandez E. N., Acosta A., Cortés-Vecino J., Gómez-Marín J. E. 2016. Survey for Toxoplasma gondii by PCR detection in meat for human consumption in Colombia. Parasitology Research, 115(2):691-695. https://doi.org/10.1007/s00436-015-4790-7.

Fredericks J., Hawkins-Cooper D. S., Hill D. E., Luchansky J., Porto-Fett A., Gamble H. R., Fournet V. M., Urban J. F., Holley R., Dubey J. P. 2019. Low salt exposure results in inactivation of Toxoplasma gondii bradyzoites during formulation of dry cured ready-to-eat pork sausage. Food and Waterborne Parasitology, 15:e00047. https://doi.org/10.1016/j.fawpar.2019.e00047.

Fredericks J., Hawkins-Cooper D. S., Hill D. E., Luchansky J. B., Porto-Fett A. C. S., Shoyer B. A., Fournet V. M., Urban J. F., Dubey J. P. 2020. Inactivation of Toxoplasma gondii bradyzoites after salt exposure during preparation of dry-cured hams. Journal of Food Protection, 83(6):1038-1042. https://doi.org/10.4315/0362-028X.JFP-19-461.

Galván-Ramirez M. L., Madriz Elisondo A. L., Rico Torres C. P., Luna-Pastén H., Rodríguez Pérez L. R., Rincón-Sánchez A. R., Franco R., Salazar-Montes A., Correa D. 2010. Frequency of Toxoplasma gondii in pork meat in Ocotlán, Jalisco, Mexico. Journal of Food Protection, 73(6):1121-1123. doi: https://doi.org/10.4315/0362-028x-73.6.1121.

Genchi M., Vismarra A., Mangia C., Faccini S., Vicari N., Rigamonti S., Prati P., Marino A. M., Kramer L., Fabbi M. 2017. Lack of viable parasites in cured ‘Parma Ham’ (PDO), following experimental Toxoplasma gondii infection of pigs. Food Microbiology, 66:157-164. https://doi.org/10.1016/j.fm.2017.04.007.

Gisbert Algaba I., Geerts M., Jennes M., Coucke W., Opsteegh M., Cox E., Dorny P., Dierick K., De Craeye S. 2017. A more sensitive, efficient and ISO 17025 validated Magnetic Capture real time PCR method for the detection of archetypal Toxoplasma gondii strains in meat. International Journal of Parasitology, 47(13):875-884. https://doi.org/10.1016/j.ijpara.2017.05.005.

Gisbert Algaba I., Verhaegen B., Jennes M., Rahman M., Coucke W., Cox E., Dorny P., Dierick K., De Craeye S. 2018. Pork as a source of transmission of Toxoplasma gondii to humans: a parasite burden study in pig tissues after infection with different strains of Toxoplasma gondii as a function of time and different parasite stages. International Journal of Parasitology, 48(7):555-560. https://doi.org/10.1016/j.ijpara.2017.12.009.

Gomez-Samblas M., Vílchez S., Racero J. C., Fuentes M. V., Osuna A. 2015. Quantification and viability assays of Toxoplasma gondii in commercial “Serrano” ham samples using magnetic capture real-time qPCR and bioassay techniques. Food Microbiology, 46:107-113. https://doi.org/10.1016/j.fm.2014.07.003.

Gomez-Samblas M., Vilchez S., Racero J. C., Fuentes M. V., Osuna A. 2016. Toxoplasma gondii detection and viability assays in ham legs and shoulders from experimentally infected pigs. Food Microbiology, 58:112-120. https://doi.org/10.1016/j.fm.2016.04.005.

Guo M., Dubey J. P., Hill D., Buchanan R. L., Gamble H. R., Jones J. L., Pradhan A. K. 2015. Prevalence and risk factors for Toxoplasma gondii infection in meat animals and meat products destined for human consumption. Journal of Food Protection, 78(2):457-476. https://doi.org/10.4315/0362-028X.JFP-14-328.

Hernández-Cortazar I. B., Acosta-Viana K. Y., Guzmán-Marin E., Ortega-Pacheco A., de Jesus Torres-Acosta J. F., Jimenez-Coello M. 2016. Presence of Toxoplasma gondii in pork intended for human consumption in tropical Southern Mexico. Foodborne Pathogens and Disease, 13(12):695-699. https://doi.org/10.1089/fpd.2016.2165.

Herrero L., Gracia M. J., Pérez-Arquillué C., Lázaro R., Herrera M., Herrera A., Bayarri S. 2016. Toxoplasma gondii: Pig seroprevalence, associated risk factors and viability in fresh pork meat. Veterinary Parasitology, 224:52-59. https://doi.org/10.1016/j.vetpar.2016.05.010.

Herrero L., Gracia M. J., Pérez-Arquillué C., Lázaro R., Herrera A., Bayarri S. 2017. Toxoplasma gondii in raw and dry-cured ham: The influence of the curing process. Food Microbiology, 65:213-220. https://doi.org/10.1016/j.fm.2017.02.010.

Hill D. E., Sreekumar C., Gamble H. R., Dubey J. P. 2004. Effect of commonly used enhancement solutions on the viability of Toxoplasma gondii tissue cysts in pork loin. Journal of Food Protection, 67(10):2230-2233. https://doi.org/10.4315/0362-028x-67.10.2230.

Hill D. E., Luchansky J., Porto-Fett A., Gamble H. R., Fournet V. M., Hawkins-Cooper D. S., Urban J. F., Gajadhar A. A., Holley R., Juneja V. K., Dubey J. P. 2018. Rapid inactivation of Toxoplasma gondii bradyzoites during formulation of dry cured ready-to-eat pork sausage. Food and Waterborne Parasitology, 12:e00029. https://doi.org/10.1016/j.fawpar.2018.e00029.

Iqbal A., Janecko N., Pollari F., Dixon B. 2018. Prevalence and molecular characterization of Toxoplasma gondii DNA in retail fresh meats in Canada. Food and Waterborne Parasitology, 13:e00031. https://doi.org/10.1016/j.fawpar.2018.e00031.

Kapperud G., Jenum P. A., Stray-Pedersen B., Melby K. K., Eskild A., Eng J. 1996. Risk factors for Toxoplasma gondii infection in pregnancy. Results of a prospective case-control study in Norway. The American Journal of Epidemiology, 144(4):405-412. https://doi.org/10.1093/oxfordjournals.aje.a008942.

Klun I., Vujanić M., Yera H., Nikolić A., Ivović V., Bobić B., Bradonjić S., Dupouy-Camet J., Djurković-Djaković O. 2011. Toxoplasma gondii infection in slaughter pigs in Serbia: seroprevalence and demonstration of parasites in blood. Veterinary Research, 42(1):17. https://doi.org/10.1186/1297-9716-42-17.

Kortbeek L. M., Hofhuis A., Nijhuis C. D. M., Havelaar A. H. 2009. Congenital toxoplasmosis and DALYs in the Netherlands. Memórias do Instituto Oswaldo Cruz, 104(2):370-373. https://doi.org/10.1590/S0074-02762009000200034.

Kuruca Lj., Klun I., Uzelac A., Nikolić A., Bobić B., Simin S., Lalošević V., Lalošević D., Djurković-Djaković O. 2017. Detection of Toxoplasma gondii in naturally infected domestic pigs in Northern Serbia. Parasitology Research, 116(11):3117-3123. https://doi.org/1010.1007/s00436-017-5623-7.

Li X., Babol J., Wallby A., Lundström K. 2013. Meat quality, microbiological status and consumer preference of beef gluteus medius aged in a dry ageing bag or vacuum. Meat Science, 95(2):229-234. https://doi.org/10.1016/j.meatsci.2013.05.009.

Li X., Babol J., Bredie W. L., Nielsen B., Tománková J., Lundström K. 2014. A comparative study of beef quality after ageing longissimus muscle using a dry ageing bag, traditional dry ageing or vacuum package ageing. Meat Science, 97(4):433-442. https://doi.org/10.1016/j.meatsci.2014.03.014.

Miura A. C., de Barros L. D., Ferreira F. P., Ferreira Neto J. M. , Sicupira Franco P. M. L., Su C., Vidotto O., Garcia J. L. 2019. Genotyping of Toxoplasma gondii isolated from pigs for human consumption. Parasitology Research, 118(5):1593-1599. https://doi.org/10.1007/s00436-019-06274-1.

Opsteegh M., Langelaar M., Sprong H., den Hartog L., De Craeye S., Bokken G., Ajzenberg D., Kijlstra A., van der Giessen J. 2010. Direct detection and genotyping of Toxoplasma gondii in meat samples using magnetic capture and PCR. International Journal of Food Microbiology, 139(3):193-201. https://doi.org/10.1016/j.ijfoodmicro.2010.02.027.

Opsteegh M., Prickaerts S., Frankena K., Evers E. G. 2011. A quantitative microbial risk assessment for meatborne Toxoplasma gondii infection in The Netherlands. International Journal of Food Microbiology, 150(2-3):103-114. https://doi.org/10.1016/j.ijfoodmicro.2011.07.022.

Opsteegh M., Schares G. and van der Giessen J. on behalf of the consortium. 2016. Relationship between seroprevalence in the main livestock species and presence of Toxoplasma gondii in meat (GP/EFSA/BIOHAZ/2013/01). An extensive literature review. Final report. EFSA supporting publication, 2016:EN-996, 294 pp. https://doi.org/10.2903/sp.efsa.2016.EN-996

Paraboni M. L. R., Costa D. F., Silveira C., Gava R., Pereira-Chioccola V. L., Belfort R. Jr., Commodaro A. G. 2020. A new strain of Toxoplasma gondii circulating in Southern Brazil. Journal of Parasitic Diseases, 44(1):248-252. https://doi.org/10.1007/s12639-019-01155-x.

Paştiu A. I., Cozma-Petruț A., Mercier A., Balea A., Galal L., Mircean V., Pusta D. L., Bogdan L., Györke A. 2019. Prevalence and genetic characterization of Toxoplasma gondii in naturally infected backyard pigs intended for familial consumption in Romania. Parasites & Vectors, 12(1):586. https://doi.org/10.1186/s13071-019-3842-8.

Plaza J., Dámek F., Villena I., Innes E.A., Katzer F., Hamilton C. M. 2020. Detection of Toxoplasma gondii in retail meat samples in Scotland. Food and Waterborne Parasitology, 20:e00086. https://doi.org/10.1016/j.fawpar.2020.e00086.

Rani S., Cerqueira-Cézar C. K., Murata F. H. A., Sadler M., Kwok O. C. H., Pradhan A. K., Hill D. E., Urban J. F. Jr., Dubey J. P. 2019. Toxoplasma gondii tissue cyst formation and density of tissue cysts in shoulders of pigs 7 and 14 days after feeding infected mice tissues. Veterinary Parasitology, 269:13-15. https://doi.org/10.1016/j.vetpar.2019.04.004.

Robert-Gangneux F., Dardé M. L. 2012. Epidemiology of and diagnostic strategies for toxoplasmosis. Clinical Microbiology Reviews, 25(2):264-296. https://doi.org/10.1128/CMR.05013-11.

Scallan E., Hoekstra R. M., Angulo F. J., Tauxe R. V., Widdowson M. A., Roy S. L., Jones J. L., Griffin P. M. 2011. Foodborne illness acquired in the United States – major pathogens. Emerging Infectious Diseases, 17(1):7-15. https://doi.org/10.3201/eid1701.p11101.

Scharff R. 2020. Food attribution and economic cost estimates for meat- and poultry-related illnesses. Journal of Food Protection, 83(6):959-967. https://doi.org/10.4315/JFP-19-548.

Sroka J., Bilska-Zając E., Wójcik-Fatla A., Zając V., Dutkiewicz J., Karamon J., Piotrowska W., Cencek T. 2019. Detection and molecular characteristics of Toxoplasma gondii DNA in retail raw meat products in Poland. Foodborne Pathogens and Disease, 16(3):195-204. https://doi.org/10.1089/fpd.2018.2537.

Vergara A., Marangi M., Caradonna T., Pennisi L., Paludi D., Papini R., Ianieri A., Giangaspero A., Normanno G. 2018. Toxoplasma gondii lineages circulating in slaughtered industrial pigs and potential risk for consumers. Journal of Food Protection, 81(8):1373-1378. https://doi.org/10.4315/0362-028X.JFP-17-496.

Vitale M., Tumino G., Partanna S., La Chiusa S., Mancuso G., Giglia M. L., Presti V. D. 2014. Impact of traditional practices on food safety: a case of acute toxoplasmosis related to the consumption of contaminated raw pork sausage in Italy. Journal of Food Protection, 77(4):643-646. https://doi.org/10.4315/0362-028X.JFP-13-285.

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 genotypes of Toxoplasma gondii in pork from retail meat stores in Eastern China. International Journal of Food Microbiology, 157(3):393-397. https://doi.org/10.1016/j.ijfoodmicro.2012.06.011.