Original Articles

Molecular characterization and antimicrobial resistance of Yersinia enterocolitica isolated from raw chicken meat in Iran: polymerase chain reaction ribotyping insights

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Received: 14 May 2025
Accepted: 8 August 2025
Published: 12 January 2026
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Yersinia enterocolitica is a well-known foodborne pathogen that is widely distributed among domestic and wild animals. This study aimed to determine the prevalence of Y. enterocolitica in raw chicken meat and to characterize the isolates in terms of bio/serotypes, virulence factors, antimicrobial sensitivity, and genetic diversity. In 2021-2023, a total of 622 raw chicken meat samples were collected, from which Y. enterocolitica strains were isolated and confirmed by 16S rRNA detection. Biotype and serotype were identified using biochemical assays and agglutination methods, respectively. Six virulence-associated genes were examined using polymerase chain reaction (PCR). Antimicrobial susceptibility was assessed via the disk diffusion, and molecular typing was conducted by PCR ribotyping. The overall prevalence of Y. enterocolitica was 9.3%. A significant relationship was found between seasonal variation and prevalence (p=0.0001). Bio/serotypes 1A/O:8, 1A/O:5, 1A/O:NI, 1B/O:8, and 1B/O:NI were identified, with most isolates belonging to 1A/O:NI and 1A/O:8. A significant relationship was also observed between seasons and biotype distribution (p=0.031). In biotype 1B, the most frequent virulence genes were ystA, myfA, virF, ail, and inv, whereas biotype 1A predominantly harbored ystB and inv. All isolates were susceptible to 14 antibiotics. Ceftazidime and ampicillin resistance, however, was 100%. Notably, there were also notable levels of resistance to trimethoprim-sulfamethoxazole and nitrofurantoin. Pathogenic strains (IRT1 and IRT2) were grouped independently from non-pathogenic strains (IRT3) using PCR ribotyping. The detection of highly pathogenic Y. enterocolitica (1B/O:8) in Iran may pose a serious public health concern.

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Aghamohammad S, Gholami M, Dabiri H, Rahimzadeh G, Souod N, Goudarzi H, Sardari S, Mohammadzadeh A, 2015. Distribution and antimicrobial resistance profile of Yersinia species isolated from chicken and beef meat. Int J Enteric Pathog 3:1-5. DOI: https://doi.org/10.17795/ijep29009
Aladhadh M, 2023. A review of modern methods for the detection of foodborne pathogens. Microorganisms 11:1111. DOI: https://doi.org/10.3390/microorganisms11051111
Arsić M, Vićić I, Petrović M, Dmitrić M, Karabasil N, 2023. Yersinia enterocolitica and control measures for reducing risks in the pork production chain. Meat Technol 64:237-41. DOI: https://doi.org/10.18485/meattech.2023.64.2.43
Bari ML, Hossain MA, Isshiki K, Ukuku D, 2011. Behavior of Yersinia enterocolitica in foods. J Pathog 2011:420732. DOI: https://doi.org/10.4061/2011/420732
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: https://doi.org/10.4315/0362-028X-73.10.1785
Bottone EJ, 1999. Yersinia enterocolitica: overview and epidemiologic correlates. Microbes Infect 1:323-33. DOI: https://doi.org/10.1016/S1286-4579(99)80028-8
Capita R, Alonso-Calleja C, Prieto M, del Camino Garcı́a-Fernández MA, Moreno B, 2002. Incidence and pathogenicity of Yersinia spp. isolates from poultry in Spain. Food Microbiol 19:295-301. DOI: https://doi.org/10.1006/fmic.2002.0492
Chen F, Jiang F, Ma J, Alghamdi MA, Zhu Y, Yong JWH, 2024. Intersecting planetary health: Exploring the impacts of environmental stressors on wildlife and human health. Ecotoxicol Environ Saf 283:116848. DOI: https://doi.org/10.1016/j.ecoenv.2024.116848
Clinical and Laboratory Standards Institute, 2023. Performance standards for antimicrobial susceptibility testing (33rd ed., CLSI supplement M100).
EFSA, ECDC, 2024. The European Union One Health 2023 zoonoses report. EFSA Journal 22, e9106. DOI: https://doi.org/10.2903/j.efsa.2024.9106
Estrada CSL, del Carmen Velázquez L, Escudero ME, Favier GI, Lazarte V, de Guzmán AMS, 2011. Pulsed field, PCR ribotyping and multiplex PCR analysis of Yersinia enterocolitica strains isolated from meat food in San Luis Argentina. Food Microbiol 28:21-8. DOI: https://doi.org/10.1016/j.fm.2010.07.026
Fàbrega A, Vila J, 2012. Yersinia enterocolitica: pathogenesis, virulence and antimicrobial resistance. Enferm Infecc Microbiol Clin 30:24-32.
Fazlara A, Zarei M, Mavalizadeh A, 2016. Survey on contamination to yersinia entrocolotica in cow milk distributed in ahvaz area and evaluation of antibiotic resistance of isolates. J Food Microbiol 3:11-23.
Fewtrell L, Kaufmann RB, Kay D, Enanoria W, Haller L, Colford JM, 2005. Water, sanitation, and hygiene interventions to reduce diarrhoea in less developed countries: a systematic review and meta-analysis. Lancet Infect Dis 5:42-52. DOI: https://doi.org/10.1016/S1473-3099(04)01253-8
Gkouletsos T, Patas K, Lambrinidis G, Neubauer H, Sprague L, Ioannidis A, Chatzipanagiotou S, 2019. Antimicrobial resistance of Yersinia enterocolitica and presence of plasmid pYV virulence genes in human and animal isolates. New Microbes New Infect 32:100604. DOI: https://doi.org/10.1016/j.nmni.2019.100604
Gupta, V., Gulati, P., Bhagat, N., Dhar, M., Virdi, J., 2015. Detection of Yersinia enterocolitica in food: an overview. Eur J Clin Microbiol Infect Dis 34:641-50. DOI: https://doi.org/10.1007/s10096-014-2276-7
Hanifian S, Khani S, 2012. Prevalence of virulent Yersinia enterocolitica in bulk raw milk and retail cheese in northern-west of Iran. Int J Food Microbiol 155:89-92. DOI: https://doi.org/10.1016/j.ijfoodmicro.2012.01.012
Hassanzadeh P, Limoee EG, Gharajalar SN, 2022. Molecular detection, biotyping and serotyping of Yersinia enterocolitica isolated from chicken livers in Tabriz. Comp Immunol Microbiol Infect Dis 83:101777. DOI: https://doi.org/10.1016/j.cimid.2022.101777
Huang S, Li Y, Hong C, Jin Y, Li S, Xu X, Xia Y, Zhang L, Lou Y, Guan W, 2023. Whole-genome sequencing-based analysis of antimicrobial resistance, virulence factors, and genetic diversity in Yersinia isolated in Wenzhou, China 2020. Mol Phylogenet Evol 188:107903. DOI: https://doi.org/10.1016/j.ympev.2023.107903
Łada P, Kończyk-Kmiecik K, Bancerz-Kisiel A, 2023. Isolation, characterization and antimicrobial resistance of Yersinia enterocolitica from Polish cattle and their carcasses. BMC Vet Res 19:143. DOI: https://doi.org/10.1186/s12917-023-03700-6
Lü Z, Su X, Chen J, Qin M, Sheng H, Zhang Q, Zhang J, Yang J, Cui S, Li F, 2022. Prevalence, bio-serotype, antibiotic susceptibility and genotype of Yersinia enterocolitica and other Yersinia species isolated from retail and processed meats in Shaanxi Province, China. LWT 168:113962. DOI: https://doi.org/10.1016/j.lwt.2022.113962
Mahdavi S, Farshchian MR, Amini K, Abbasi M, Rad MG, Ebadi AR, 2012. Survey of Yersinia enterocolitica contamination in distributed broiler meats in Tabriz City, Iran. African J Microbiol Res 6:3019-23.
Mahmoud RA, Sadat A, Younis G, 2023. Insight into the prevalence of the planktonic and biofilm-producing Yersiniaa enterocolitica in poultry meat in Egypt. Egypt J Vet Sci 54:703-13. DOI: https://doi.org/10.21608/ejvs.2023.200752.1481
Mastrodonato AC, Favier GI, Lucero Estrada CS, Vidal R, Escudero ME, 2018. Bioserotypes, virulence genes, antimicrobial susceptibility and genomic diversity of Yersinia enterocolitica isolates from Argentina and Chile. J Food Saf 38:e12491. DOI: https://doi.org/10.1111/jfs.12491
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: https://doi.org/10.3382/japr.2012-00549
Pakharukova N, Roy S, Tuittila M, Rahman MM, Paavilainen S, Ingars AK, Skaldin M, Lamminmäki U, Härd T, Teneberg S, 2016. Structural basis for Myf and Psa fimbriae‐mediated tropism of pathogenic strains of Yersinia for host tissues. Mol Microbiol 102:593-610. DOI: https://doi.org/10.1111/mmi.13481
Park MS, Park KH, Bahk GJ, 2018. Interrelationships between multiple climatic factors and incidence of foodborne diseases. Int J Environ Res Public Health 15:2482. DOI: https://doi.org/10.3390/ijerph15112482
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: https://doi.org/10.1016/j.foodcont.2018.05.048
Peruzy MF, Murru N, Perugini AG, Capuano F, Delibato E, Mercogliano R, Korkeala H, Proroga YTR, 2017. Evaluation of virulence genes in Yersinia enterocolitica strains using SYBR Green real-time PCR. Food Microbiol 65:231-5. DOI: https://doi.org/10.1016/j.fm.2017.03.004
Rahimi E, Sepehri S, Dehkordi FS, Shaygan S, Momtaz H, 2014. Prevalence of Yersinia species in traditional and commercial dairy products in Isfahan Province, Iran. Jundishapur J Microbiol 7:e9249. DOI: https://doi.org/10.5812/jjm.9249
Silva CC, Ribeiro SC, 2024. Microorganisms and their importance in the food industry: safety, quality and health properties. Foods 13:1452. DOI: https://doi.org/10.3390/foods13101452
Sirghani K, Zeinali T, Jamshidi A, 2018. Detection of Yersinia enterocolitica in retail chicken meat, Mashhad, Iran. J Pathog 2018:1286216. DOI: https://doi.org/10.1155/2018/1286216
Soltan Dallal M, Khorramizadeh M, MoezArdalan K, 2006. Occurrence of enteropathogenic bacteria in children under 5 years with diarrhoea in south Tehran. East Mediterr Health J 12:792-7.
Soltan Dallal MM, Sharifi Yazdi MK, Monadi Sefidan A, Hassanpour G, Sharifi Yazdi S, Haghighat Khajavi S, Vahedi S, Abrichamchian Langaroudi SM, Pourmoradian M, Molla Agha Mirzaei H, 2022. Biotyping of Yersinia enterocolitica Isolates from children with diarrhea and chicken meat in Tehran, Iran (2016-17). J Gorgan Univ Med Sci 24:94-9.
Virdi JS, Sachdeva P, 2005. Molecular heterogeneity in Yersinia enterocolitica and ‘Y. enterocolitica-like’species—implications for epidemiology, typing and taxonomy. FEMS Immunol Med Microbiol 45:1-10. DOI: https://doi.org/10.1016/j.femsim.2005.03.006
Wang X, Cui Z, Wang H, Tang L, Yang J, Gu L, Jin D, Luo L, Qiu H, Xiao Y, 2010. Pathogenic strains of Yersinia enterocolitica isolated from domestic dogs (Canis familiaris) belonging to farmers are of the same subtype as pathogenic Y. enterocolitica strains isolated from humans and may be a source of human infection in Jiangsu Province, China. J Clin Microbiol 48:1604-10. DOI: https://doi.org/10.1128/JCM.01789-09
Ye Q, Wu Q, Hu H, Zhang J, Huang H, 2015. Prevalence, antimicrobial resistance and genetic diversity of Yersinia enterocolitica isolated from retail frozen foods in China. FEMS Microbiol Lett 362:fnv197. DOI: https://doi.org/10.1093/femsle/fnv197
Zadernowska A, Chajęcka-Wierzchowska W, Łaniewska-Trokenheim Ł, 2014. Yersinia enterocolitica: a dangerous, but often ignored, foodborne pathogen. Food Rev Int 30:53-70.

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1.
Molecular characterization and antimicrobial resistance of Yersinia enterocolitica isolated from raw chicken meat in Iran: polymerase chain reaction ribotyping insights. Ital J Food Safety [Internet]. 2026 Jan. 12 [cited 2026 Jan. 23];. Available from: https://www.pagepressjournals.org/ijfs/article/view/13983