The Presence and Antibiotic Resistance of Non-O157 STEC on Lamb Carcasses

Yıl 2024, , 55 - 61, 28.06.2024

Pelin Koçak Kızanlık , Cemil Sahıner , Ergün Ömer Göksoy

https://doi.org/10.53913/aduveterinary.1456133

Öz

There is an increasing trend in the prevalence of Hemolytic Uremic Syndrome (HUS) both in Türkiye and in the world. HUS might be caused by Shiga toxin (Stx)-producing Escherichia coli (STEC) O157 and strains of non-O157 STEC. The feces and fleece of lambs, and non-hygienic conditions present in the lamb slaughtering process are the main sources for STEC contaminations of lamb carcasses. In this study, the prevalence of STEC on lamb carcasses and, as an important global public health issue, the antibiotic resistance profiles of STEC strains isolated were aimed to be determined. The presence of stx was considered as STEC indicator. 16% of the carcasses (8/50) were found to be contaminated by E. coli. The analysis showed that none of the strains isolated were O157 serotype. But, 5 out of 8 strains isolated carried stx1 and stx2 genes so they were identified as non-O157 cytotoxigenic E. coli. Antibiotic resistance profiles of the isolates were determined by using Kirby Bauer method. All of the isolates were found to be resistant at least one antibiotics investigated, and as the most resistance rate found 87.5% of the isolates were resistant to both gentamycin and pefloxacine. In addition, 75% of the isolates were multidrug resistant (MDR), and overall MAR (Multi Antimicrobial Resistant) index of isolates was 0.4. As a result, STEC contamination on lamb carcasses was considered to be a risk for both children and adults for HUS, and high antibiotic resistance of the isolates observed also increased the public health hesitations. Reassessment of the slaughtering process based on the HACCP (Hazard Analysis and Critical Control Points) requirements and taking necessary actions/measures to control cross contaminations are thought to be crucial steps to reduce pathogenic bacteria incidence in food chain.

Anahtar Kelimeler

Antibiotic resistance, lamb carcasses, non-O157 STEC

Kaynakça

• Alharbi, M.G., Al-Hindi, R.R., Esmael, A., Alotibi, I.A., Azhari, S.A., Alseghayer, M.S., & Teklemariam, A.D. (2022). The “big six”: Hidden emerging foodborne bacterial pathogens. Tropical Medicine and Infectious Disease, 7(11), 356. https://doi.org/10.3390/tropicalmed7110356
• Babolhavaeji, K., Shokoohizadeh, L., Yavari, M., Moradi, A., & Alikhani, M.Y. (2021). Prevalence of Shiga toxin-producing Escherichia coli O157 and non-O157 serogroups isolated from fresh raw beef meat samples in an industrial slaughterhouse. International Journal of Microbiology, 2021. https://doi.org/10.1155/2021/1978952
• Berger, M., Aijaz, I., Berger, P., Dobrindt, U., & Koudelka, G. (2019). Transcriptional and translational inhibitors block SOS response and Shiga toxin expression in enterohemorrhagic Escherichia coli. Scientific Reports, 9(1), 18777. https://doi.org/10.1038/s41598-019-55332-2
• Deng, W., Li, Y., Vallance, B.A. & Finlay, B.B. (2001). Locus of enterocyte effacement from Citrobacter rodentium: sequence analysis and evidence for horizontal transfer among attaching and effacing pathogens. Infect Immunity, 69, 6323-6335. https://doi.org/10.1128/iai.69.10.6323-6335.2001
• EFSA & ECDC (European Food Safety Authority & European Centre for Disease Prevention and Control) (2019). The European Union one health 2018 zoonoses report. EFSA Journal, 17(12), e05926.
• EFSA & ECDC (European Food Safety Authority & European Centre for Disease Prevention and Control) (2021). The European Union one health 2020 zoonoses report. EFSA Journal, 19(12), e06971.
• Elabbasy, M.T., Hussein, M.A., Algahtani, F.D., Abd El-Rahman, G.I., Morshdy, A.E., Elkafrawy, I.A., & Adeboye, A.A. (2021). MALDI-TOF MS based typing for rapid screening of multiple antibiotic resistance E. coli and virulent non-O157 shiga toxin-producing E. coli isolated from the slaughterhouse settings and beef carcasses. Foods, 10(4), 820. https://doi.org/10.3390/foods10040820
• Enriquez-Gómez, E., Acosta-Dibarrat, J., Talavera-Rojas, M., Soriano-Vargas, E., Navarro, A., Morales-Espinosa, R., ... & Cal-Pereyra, L. (2023). serotypes, pathotypes, shiga toxin variants and antimicrobial resistance in diarrheagenic escherichia coli ısolated from rectal swabs and sheep carcasses in an abattoir in Mexico. Agriculture, 13(8), 1604. https://doi.org/10.3390/agriculture13081604
• Etcheverría, A.I., Padola, N.L., Sanz, M.E., Polifroni, R., Krüger, A., Passucci, J., ... & Parma, A.E. (2010). Occurrence of Shiga toxinproducing E. coli (STEC) on carcasses and retail beef cuts in the marketing chain of beef in Argentina. Meat Science, 86(2), 418-421. https://doi.org/10.1016/j.meatsci.2010.05.027
• EUCAST (European Committee on Antimicrobial Susceptibility Testing). Breakpoint tables for interpretation of MICs and zone diameters. Version 10.0, 2021.
• Ferhat, L., Chahed, A., Hamrouche, S., Korichi‐Ouar, M., & Hamdi, T.M. (2019). Research and molecular characteristic of Shiga toxin‐producing Escherichia coli isolated from sheep carcasses. Letters in applied microbiology, 68(6), 546-552. https://doi.org/10.1111/lam.13142
• Gencay, Y.E. (2014). Sheep as an important source of E. coli O157/O157: H7 in Turkey. Veterinary Microbiology, 172(3-4), 590-595. https://doi.org/10.1016/j.vetmic.2014.06.014
• Gupta, M. D., Sen, A., Shaha, M., Dutta, A., & Das, A. (2022). Occurrence of Shiga toxin‐producing Escherichia coli carrying antimicrobial resistance genes in sheep on smallholdings in Bangladesh. Veterinary Medicine and Science, 8(6), 2616-2622. https://doi.org/10.1002/vms3.935
• Hauge, S.J., Wahlgren, M., Røtterud, O.J., & Nesbakken, T. (2011). Hot water surface pasteurisation of lamb carcasses: Microbial effects and cost-benefit considerations. International Journal of Food Microbiology, 146(1), 69-75. https://doi.org/10.1016/j.ijfoodmicro.2011.02.003
• ISO (International Organization for Standardization). (2001). ISO 16654: 2001. Microbiology of food and animal feeding stuffs–Horizontal method for the detection of Escherichia coli O157.
• ISO (International Organization for Standardization). (2015). ISO 17604: 2015. Microbiology of the food chain. Carcass sampling for microbiological analysis.
• Jeshveen, S.S., Chai, L.C., Pui, C.F., & Son, R. (2012). Optimization of multiplex PCR conditions for rapid detection of Escherichia coli O157: H7 virulence genes. International Food Research Journal, 19(2), 461-466.
• Kalchayanand, N., Arthur, T.M., Bosilevac, J.M., Brichta-Harhay, D.M., Guerini, M.N., Shackelford, S.D., ... & Koohmaraie, M. (2007). Microbiological characterization of lamb carcasses at commercial processing plants in the United States. Journal of Food Protection, 70(8), 1811-1819. https://doi.org/10.4315/0362-028X-70.8.1811.
• Karama, M., Cenci-Goga, B.T., Malahlela, M., Smith, A.M., Keddy, K.H., El-Ashram, S., ... & Kalake, A. (2019). Virulence characteristics and antimicrobial resistance profiles of shiga toxin-producing Escherichia coli isolates from humans in South Africa: 2006–2013. Toxins, 11(7), 424. https://doi.org/10.3390/toxins11070424.
• Krumperman, P.H. (1983). Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Applied Environmental Microbiology, 46, 165-170. https://doi.org/10.1128/aem.46.1.165-170.1983
• Liu, Y., Li, H., Chen, X., Tong, P., Zhang, Y., Zhu, M., ... & Cai, W. (2022). Characterization of Shiga toxin‐producing Escherichia coli isolated from cattle and sheep in Xinjiang province, China, using wholegenome sequencing. Transboundary and Emerging Diseases, 69(2), 413-422. https://doi.org/10.1111/tbed.13999
• Maluta, R.P., Fairbrother, J.M., Stella, A.E., Rigobelo, E.C., Martinez, R., & de Ávila, F.A. (2014). Potentially pathogenic Escherichia coli in healthy, pasture-raised sheep on farms and at the abattoir in Brazil. Veterinary Microbiology, 169(1-2), 89-95. https://doi.org/10.1016/j.vetmic.2013.12.013
• Mateus, K.A., dos Santos, M.R., de Lima, J., de Bona, L.F., dos Santos, M.S., Korb, A., ... & Kessler, J.D. (2021). Antimicrobial resistance of Escherichia coli isolates from spray‑chilled sheep carcasses during cooling. Revista Colombiana de Ciencias Pecuarias, 34(1), 63-72. https://doi.org/10.17533/udea.rccp.v34n2a04
• McCarthy, S.C., Burgess, C.M., Fanning, S., & Duffy, G. (2021a). An overview of Shiga-toxin producing Escherichia coli carriage and prevalence in the ovine meat production chain. Foodborne Pathogens and Disease, 18(3), 147-168. https://doi.org/10.1089/fpd.2020.2861
• McCarthy, S.C., Macori, G., Duggan, G., Burgess, C.M., Fanning, S., & Duffy, G. (2021b). Prevalence and whole-genome sequencebased analysis of shiga toxin-producing Escherichia coli isolates from the recto-anal junction of slaughter-age Irish sheep. Applied and Environmental Microbiology, 87(24), e01384-21. https://doi.org/10.1128/AEM.01384-21
• Milios, K., Mataragas, M., Pantouvakis, A., Drosinos, E.H., & Zoiopoulos, P.E. (2011). Evaluation of control over the microbiological contamination of carcasses in a lamb carcass dressing process operated with or without pasteurizing treatment. International Journal of Food Microbiology, 146(2), 170-175. https://doi.org/10.1016/j.ijfoodmicro.2011.02.023
• Mir, R.A., & Kudva, I.T. (2019). Antibiotic‐resistant Shiga toxin producing Escherichia coli: An overview of prevalence and intervention strategies. Zoonoses and Public Health, 66(1), 1-13. https://doi.org/10.1111/zph.12533
• Momtaz, H., Dehkordi, F.S., Rahimi, E., Ezadi, H., & Arab, R. (2013). Incidence of Shiga toxin-producing Escherichia coli serogroups in ruminant’s meat. Meat Science, 95(2), 381-388. https://doi.org/10.1016/j.meatsci.2013.04.051
• Mughini-Gras, L., Van Pelt, W., Van der Voort, M., Heck, M., Friesema, I., & Franz, E. (2018). Attribution of human infections with Shiga toxin‐producing Escherichia coli (STEC) to livestock sources and identification of source‐specific risk factors, The Netherlands (2010–2014). Zoonoses and Public Health, 65(1), e8-e22. https://doi.org/10.1111/zph.12403
• Oporto, B., Ocejo, M., Alkorta, M., Marimón, J.M., Montes, M., & Hurtado, A. (2019). Zoonotic approach to Shiga toxin-producing Escherichia coli: integrated analysis of virulence and antimicrobial resistance in ruminants and humans. Epidemiology and Infection, 147, e164. https://doi.org/10.1017/S0950268819000566
• Pan, Y., Hu, B., Bai, X., Yang, X., Cao, L., Liu, Q., ... & Xiong, Y. (2021). Antimicrobial resistance of Non-O157 shiga toxin-producing Escherichia coli isolated from humans and domestic animals. Antibiotics, 10(1), 74. https://doi.org/10.3390/antibiotics10010074
• Parvin, M.S., Talukder, S., Ali, M.Y., Chowdhury, E.H., Rahman, M.T., & Islam, M. T. (2020). Antimicrobial resistance pattern of Escherichia coli isolated from frozen chicken meat in Bangladesh. Pathogens, 9(6), 420. https://doi.org/10.3390/pathogens9060420
• Paton, A.W., & Paton, J.C. (2002). Direct detection and characterization of Shiga toxigenic Escherichia coli by multiplex PCR for stx 1, stx 2, eae, ehxA, and saa. Journal of Clinical Microbiology, 40(1), 271-274. https://doi.org/10.1128/jcm.40.1.271-274.2002
• Quiros, P., & Muniesa, M. (2017). Contribution of cropland to the spread of Shiga toxin phages and the emergence of new Shiga toxin producing strains. Scientific Reports, 7, 7796. https://doi.org/10.1038/s41598-017-08169-6
• Rubab, M., & Oh, D.H. (2021). Molecular detection of antibiotic resistance genes in Shiga toxin-producing E. coli isolated from different sources. Antibiotics, 10(4), 344. https://doi.org/10.3390/antibiotics10040344
• Söderlund, R., Hedenström, I., Nilsson, A., Eriksson, E., & Aspán, A. (2012). Genetically similar strains of Escherichia coli O157: H7 isolated from sheep, cattle and human patients. BMC Veterinary Research, 8, 1-4. https://bmcvetres.biomedcentral.com/articles/10.1186/1746-6148-8-200
• Tarr, P.I., Gordon, C.A., & Chandler, W.L. (2005). Shiga-toxinproducing Escherichia coli and haemolytic uraemic syndrome. The Lancet, 365(9464), 1073-1086. https://doi.org/10.1016/S0140-6736(05)71144-2
• USDA (US Department of Agriculture). (2002). Escherichia coli O157:H7 in Ground Beef: Review of a Draft Risk Assessment. National Academies Press.
• Werber, D., Fruth, A., Buchholz, U., Prager, R., Kramer, M.H., Ammon, A., & Tschäpe, H. (2003). Strong association between Shiga toxinproducing Escherichia coli O157 and virulence genes stx 2 and eae as possible explanation for predominance of serogroup O157 in patients with haemolytic uraemic syndrome. European Journal of Clinical Microbiology and Infectious Diseases, 22, 726-730. https://doi.org/10.1007/s10096-003-1025-0