Retrospective study on the prevalence of Yersinia enterocolitica in food collected in Umbria region (central Italy)

Submitted: 8 November 2022
Accepted: 14 December 2022
Published: 8 March 2023
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Yersinia enterocolitica represents one of the main foodborne pathogens in Europe and the evaluation of possible sources of contamination and its prevalence in food is of considerable interest for risk analysis approach. The results of the search for Yersinia enterocolitica in food samples taken in Umbria region (central Italy) were evaluated during the years 2015-2018. Different types of foods were considered, both ready-to-eat (meat products, dairy products, and raw vegetables) and meat preparations to be eaten after cooking. Samples were assayed by molecular screening for the species indicator gene ompF. Screening positives were subjected to isolation and characterization by searching for specific virulence marker genes, including the ail gene responsible for invasiveness and the ystB gene for the production of enterotoxin. The total prevalence of positive samples for Yersinia enterocolitica was 16.86% with a higher percentage of positive samples in meat preparations (19.35%), followed by ready-to-eat vegetables (11.76%). Poultry meat samples had a higher prevalence than pork and beef samples. Neither positive samples were found in meat products and dairy, nor seasonality in positivity was observed. All isolated strains of Yersinia enterocolitica were biotype 1A, with absence of the ail virulence gene but presence of ystB gene. Since the strains isolated from human patients appear to be primarily biotypes that possess the ail marker, future investigations would be needed regarding the real role of biotype 1A in human disease. In this context, attention should certainly be paid to ready-to-eat vegetables and to careful cooking of meat preparations.



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Arden K, Gedye K, AngelinBonnet O, Murphy E, Antic D, 2022. Yersinia enterocolitica in wild and peridomestic rodents within Great Britain, a prevalence study. Zoonoses Public Health 69:537-49. DOI:
Bancerz-Kisiel A, Pieczywek M, Łada P, Szweda W, 2018. The most important virulence markers of Yersinia enterocolitica and their role during infection. Genes 9:235. DOI:
Bolton DJ, Ivory C, McDowell D, 2013. A small study of Yersinia enterocolitica in pigs from birth to carcass and characterisation of porcine and human strains. Food Control 33:521-4. DOI:
Bonardi S, Paris A, Bassi L, Salmi F, Bacci C, Riboldi E, Boni E, D’Incau M, Tagliabue S, Brindani F, 2010. Detection, semiquantitative enumeration, and antimicrobial susceptibility of Yersinia enterocolitica in pork and chicken meats in Italy. J Food Prot 73:1785-92. DOI:
Bonardi S, Le Guern AS, Savin C, Pupillo G, Bolzoni L, Cavalca M, Pongolini S, 2018. Detection, virulence and antimicrobial resistance of Yersinia enterocolitica in bulk tank milk in Italy. Int Dairy J 84:46-53. DOI:
Bottone EJ, 2015. Yersinia enterocolitica: revisitation of an enduring human pathogen. Clin Microbiol News 37:1-8. DOI:
Capita R, Alonso-Calleja C, Prieto M, del Camino Garcı́a-Fernández M, Moreno B, 2002. Incidence and pathogenicity of Yersinia spp. isolates from poultry in Spain. Food Microbiol 19:295-301. DOI:
Centers for Disease Control and Prevention (CDC), 2016. Available from: Accessed on: 31/10/2022.
Cristiano D, Peruzy MF, Aponte M, Mancusi A, Proroga YTR, Capuano F, Murru N, 2021. Comparison of droplet digital PCR vs real-time PCR for Yersinia enterocolitica detection in vegetables. Int J Food Microbiol 354:109321. DOI:
European Center for Disease Prevention and Control (ECDC), 2019. Yersiniosis In: ECDC. Annual epidemiological report for 2018. Stockholm, Sweden. Available from:
European Center for Disease Prevention and Control (ECDC), 2021. Yersiniosis In: ECDC. Annual epidemiological report for 2019. Stockholm, Sweden. Available from:
European Food Safety Authority and European Center for Disease Prevention and Control (EFSA and ECDC), 2021. The European Union One Health 2020 Zoonoses Report. EFSA J 19:e06971. DOI:
Espenhain L, Riess M, Müller L, Colombe S, Ethelberg S, Litrup E, Jernberg C, Kühlmann-Berenzon S, Lindblad M, Hove NK, Torpdahl M, Mörk MJ, 2019. Cross-border outbreak of Yersinia enterocolitica O3 associated with imported fresh spinach, Sweden and Denmark, March 2019. Euro Surveill 24:1900368. DOI:
Ferl M, Mäde D, Braun PG, 2020. Combined molecular biological and microbiological detection of pathogenic Yersinia enterocolitica in spiced ground pork, meat for production of ground pork and raw sausages. J Cons Prot Food Saf 15:27-35. DOI:
Fois F, Piras F, Torpdahl M, Mazza R, Ladu D, Consolati SG, Spanu C, Scarano C, De Santis EP, 2018. Prevalence, bioserotyping and antibiotic resistance of pathogenic Yersinia enterocolitica detected in pigs at slaughter in Sardinia. Int J Food Microbiol 283:1-6. DOI:
Fredriksson-Ahomaa M, Stolle A, Siitonen A, Korkeala H, 2006. Sporadic human Yersinia enterocolitica infections caused by bioserotype 4/O: 3 originate mainly from pigs. J Med Microbiol 55:747-9. DOI:
Fredriksson-Ahomaa M, 2012. Isolation of enteropathogenic Yersinia from non-human sources. Adv Exp Med Biol 954:97–105. DOI:
Garzetti D, Susen R, Fruth A, Tietze E, Heesemann J, Rakin A, 2014. A molecular scheme for Yersinia enterocolitica patho-serotyping derived from genome-wide analysis. Int J Med Microbiol 304:275-83. DOI:
Gruber JF, Morris S, Warren KA, Kline KE, Schroeder B, Dettinger L, Husband B, Pollard K, Davis C, Miller J, Weltman A, Mattioli M, Ray L, Tarr C, Longenberger AH, 2021 Yersinia enterocolitica outbreak associated with pasteurized milk. Foodborne Pathog Dis 18:448-54. DOI:
Guillier L, Fravalo P, Leclercq A, Thébault A, Kooh P, Cadavez V, Gonzales-Barron U, 2021. Risk factors for sporadic Yersinia enterocolitica infections: a systematic review and meta-analysis. Microb Risk Anal 17:100141. DOI:
Le Guern A-S, Martin L, Savin C, Carniel E, 2016. Yersiniosis in France: overview and potential sources of infection. Int J Infect Dis 46:1–7. DOI:
Licciardi C, Primavilla S, Roila R, Lupattelli A, Farneti S, Blasi G, Petruzzelli A, Drigo I, Di Raimo Marrocchi E, 2021. Prevalence, molecular characterization and antimicrobial susceptibility of clostridioides difficile isolated from pig carcasses and pork products in Central Italy. Int J Environ Res Public Health 18:11368. DOI:
Longenberger AH, Gronostaj MP, Yee GY, Johnson LM, Lando JF, Voorhees RE, Waller K, Weltman AC, Moll M, Lyss SB, Cadwell BL, Gladney ML, Ostroff SM, 2014. Yersinia enterocolitica infections associated with improperly pasteurized milk products: southwest Pennsylvania, March–August, 2011. Epidemiol 142:1640-50. DOI:
Mancini ME, Beverelli M, Donatiello A, Didonna A, Dattoli L, Faleo S, Occhiochiuso G, Galante D, Rondinone V, Del Sambro L, Bianco A, Miccolupo A, Goffredo E, 2022. Isolation and characterization of Yersinia enterocolitica from foods in Apulia and Basilicata regions (Italy) by conventional and modern methods. Plos one 17:e0268706. DOI:
Mengal H, Samad A, Asmat MT, Mustafa MZ, Abbas F, Sajjad N, Ishtaq H, Rahim H, Ghilzai D, 2019. The study to evaluate the prevalence of Yersinia species in salad sold and water supplied in Quetta city, Pakistan. Pure Appl Biol 8:1902-8. DOI:
Momtaz H, Rahimian MD, Dehkordi FS, 2013. Identification and characterization of Yersinia enterocolitica isolated from raw chicken meat based on molecular and biological techniques. J Appl Poult Res 22:137-45. DOI:
Özdemir F, Arslan S, 2015. Genotypic and phenotypic virulence characteristics and antimicrobial resistance of Yersinia spp. isolated from meat and milk products. J Food Sci 80:M1306-13. DOI:
Peng Z, Zou M, Li M, Liu D, Guan W, Hao Q, Xu J, Zhang S, Jing H, Li Y, Liu X, Yu D, Yan S, Wang W, Li F, 2018. Prevalence, antimicrobial resistance and phylogenetic characterization of Yersinia enterocolitica in retail poultry meat and swine feces in parts of China. Food Control 93: 121-8. DOI:
Peruzy MF, Aponte M, Proroga YTR, Capuano F, Cristiano D, Delibato E, Houf K, Murru N, 2020. Yersinia enterocolitica detection in pork products: Evaluation of isolation protocols. Food Microbiol 92:103593. DOI:
Piras F, Spanu C, Sanna R, Siddi G, Mocci AM, Demontis M, Meloni MP, Spanu V, De Santis EP, Scarano C, 2021. Detection, virulence genes and antimicrobial resistance of Yersinia enterocolitica in sheep and goat raw milk. Int Dairy J 117:105011. DOI:
Platt-Samoraj A, 2022. Toxigenic Properties of Yersinia enterocolitica biotype 1A. Toxins 14:118. DOI:
Primavilla S, Magistrali CF, Cucco L, Orsini S, Deliberato E, Farneti S, 2017. Characterization of Yersinia enterocolitica isolated from human patients, animal and food during 2003-2016 in Umbria and Marche Region. Proceedings XVIII 18th conference of the World Association of Veterinary Laboratory Diagnosticians (WAVLD), 7-10 June 2017, Sorrento, Italy.
Rastawicki W, Szych J, Rokosz N, Zacharczuk K, Gierczyński R, 2013. Seasonality of Yersinia enterocolitica bioserotype 1B/O: 8 infections in Poland. Epidemiol Infect 141:2039-42. DOI:
Riahi SM, Ahmadi E, Zeinali T, 2021. Global prevalence of Yersinia enterocolitica in cases of gastroenteritis: a systematic review and meta-analysis. Int J Microbiol 2021:1499869. DOI:
Rosner BM, Stark K, Werber D, 2010. Epidemiology of reported Yersinia enterocolitica infections in Germany, 2001-2008. BMC Public Health 10:337. DOI:
Sirghani K, Zeinali T, Jamshidi A, 2018. Detection of Yersinia enterocolitica in retail chicken meat, Mashhad, Iran. J Pathog 19:1286216. DOI:
Stenkova AM, Isaeva MP, Rasskazov VA, 2008. Development of a multiplex PCR for detection of the Yersinia genus with identification of pathogenic species (Y.pestis, Y.pseudotuberculosis, Y.enterocolitica). Mol Gen Mikrobiol Virusol 3:18-23. DOI:
Terentjeva M, Ķibilds J, Meistere I, Gradovska S, Alksne L, Streikiša M, Ošmjana J, Valciņa O, 2022. Virulence determinants and genetic diversity of yersinia species isolated from retail meat. Pathogens 11:37. DOI:
Van Cauteren D, Le Strat Y, Sommen C, Bruyand M, Tourdjman M, Da Silva NJ, Couturier E, Fournet N, de Valk H, Desenclos JC, 2017. Estimated annual numbers of foodborne pathogen–associated illnesses, hospitalizations, and deaths, France, 2008–2013. Emerg Infect Dis 23:1486-92. DOI:
Verbikova V, Borilova G, Babak V, Moravkova M, 2018. Prevalence, characterization and antimicrobial susceptibility of Yersinia enterocolitica and other Yersinia species found in fruits and vegetables from the European Union. Food Control 85:161-7. DOI:
Veronesi F, Ranucci D, Branciari R, Miraglia D, Mammoli R, Piergili Fioretti D, 2011. Seroprevalence and risk factors for Toxoplasma gondii infection on finishing swine reared in the Umbria region, central Italy. Zoonoses Public Health 58:178-84. DOI:
Wang J, Liu M, Wang H, Wu Q, Ding Y, Xu T, Ma G, Zhong Y, Zhang J, Chen M, Xue L, Ye Q, Zheng H, Yang X, Yang R, 2021. Occurrence, molecular characterization, and antimicrobial susceptibility of Yersinia enterocolitica isolated from retail food samples in China. LWT 150:111876. DOI:
Wannet WJ, Reessink M, Brunings HA, Maas HM, 2001. Detection of pathogenic Yersinia enterocolitica by a rapid and sensitive duplex PCR assay. J Clin Microbiol 39:4483-6. DOI:
Zdolec N, Kiš M, 2021. Meat safety from farm to slaughter—risk-based control of Yersinia enterocolitica and Toxoplasma gondii. Processes 9:815. DOI:
ZhiChao C, Feng Z, DaWei G, HongWei C, Jie S, HuaiQi J, 2019. Epidemiological characters of Yersinia enterocolitica in poultry and livestock feces in Lu'an, Anhui. China Trop Med 19:943-6.

How to Cite

Primavilla S, Farneti S, Roila R, Branciari R, Altissimi C, Valiani A, Ranucci D. Retrospective study on the prevalence of <em>Yersinia enterocolitica</em> in food collected in Umbria region (central Italy). Ital J Food Safety [Internet]. 2023 Mar. 8 [cited 2024 Jul. 25];12(1). Available from:

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