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Original article
Austral J. Vet. Sci.
Vol 54, 45-53 (2022)
DOI: 10.4067/S0719-81322022000200045

Non-O157 Shiga toxin-producing Escherichia coli with potential harmful profiles to humans are isolated from the faeces of calves in Uruguay

1 Departamento de Microbiología, Instituto de Investigaciones Biológicas Clemente Estable,. Avenida Italia 3318. CP: 11600. Montevideo, Uruguay.
2 Programa de Microbiología y Micología, Instituto de Ciencias Biomédicas, Facultad de Medicina, Universidad de Chile, Santiago, Chile.
3 Plataforma de Investigación en Salud Animal. Instituto Nacional de Investigación Agropecuaria (INIA), Estación Experimental INIA La Estanzuela. Ruta 50, Km 11. CP: 70000. Colonia, Uruguay
4 Departamento de Bacteriología y Virología, Instituto de Higiene, Facultad de Medicina, Universidad de la República. Avenida Alfredo Navarro 3051. CP: 11600. Montevideo, Uruguay.
5 Programa de Microbiología y Micología, Instituto de Ciencias Biomédicas, Facultad de Medicina, Universidad de Chile, Santiago, Chile; Instituto Milenio de Inmunología e Inmunoterapia, Facultad de Medicina, Universidad de Chile, Santiago, Chile.
Keywords: Non-O157 STEC Shiga toxin subtypes antimicrobial resistance

Submitted: 2021-10-12

Accepted: 2021-12-30

Published: 2022-06-13

*Corresponding author:
aumpierrez@iibce.edu.uy

How to Cite

Umpiérrez, A., Ernst, D., Cardozo, A., Torres, A., Fernández, M., Fraga, M., Vignoli, R., Bado, I., Vidal, R., & Zunino, P. (2022). Non-O157 Shiga toxin-producing Escherichia coli with potential harmful profiles to humans are isolated from the faeces of calves in Uruguay. Austral Journal of Veterinary Sciences, 54(2), 45–53. https://doi.org/10.4067/S0719-81322022000200045

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Copyright (c) 2022 Ana Umpiérrez, Déborah Ernst, Andrea Cardozo, Alexia Torres, Magalí Fernández, Martín Fraga, Rafael Vignoli, Inés Bado, Roberto Vidal, Pablo Zunino

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This work is licensed under a Creative Commons Attribution 4.0 International License.

Abstract

Shiga toxin-producing Escherichia coli (STEC) infections are responsible for acute illnesses and deaths in humans. Cattle and humans are exposed to STEC through faeces and contaminated food and water. The big six and O157 STEC serogroups are important food and water-borne human pathogens. Additionally, Stx1a, Stx2a and Stx2c subtypes are highly associated with the haemolytic uremic syndrome. This study aimed to determine Shiga toxin-subtypes, the presence of antigen 43 families, the genotypic and phenotypic antimicrobial susceptibility profiles, O-serogrouping, phylotypes and phylogenetic relatedness of STEC of calf origin. Sixteen STEC isolates from calf origin were analysed. PCR was performed to determine Stx subtypes, serogroups, the presence of ag43 I and II and phylotypes. The antimicrobial profile was evaluated and the presence of PMQR and fosfomycin genes was determined by PCR. The clonal relatedness of STEC was studied by PFGE. The genotypes stx1a+c, stx1a+, stx1a+/stx2e+, stx1a+c/stx2e and stx2a were detected. Ag43 II was the most prevalent among subfamilies. STEC isolates were serotyped as O103 (n=5) and O111 (n=6). Fifty per cent of the isolates were classified as B1 phylogroup, 4/16 as E, 1/16 as C, and 1/16 as F. Non-O157 STEC isolates showed a high level of diversity, independent of the geographical and farm-origin. Isolates were resistant to ampicillin, ciprofloxacin, gentamicin, and fosfomycin-trometamol. The gene fosA7 was detected in 1 isolate. The virulence profiles, including Shiga toxin-subtypes and serogroups, denote the potential harm of non-O157 STEC isolates to humans. We also confirmed that circulating non-O157 STEC from cattle present genetic heterogeneity and are susceptible to antibiotics.

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References

  1. Amézquita-López, B.A., Quiñones, B., Soto-Beltrán, M., Lee, B.G., Yambao, J.C., Lugo-Melchor, O.Y., Chaidez, C. (2016). Antimicrobial resistance profiles of Shiga toxin-producing Escherichia coli O157 and Non-O157 recovered from domestic farm animals in rural communities in Northwestern Mexico. Antimicrob Resist Infect Control, 05, 01.
  2. Bai, X., Fu, S., Zhang, J., Fan, R., Xu, Y., Sun, H., He, X., Xu, J., Xiong, Y. (2018). Identification and pathogenomic analysis of an Escherichia coli strain producing a novel Shiga toxin 2 subtype. Sci Rep, 08, 6756.
  3. Balbin, M.M., Hull, D., Guest, C., Nichols, L., Dunn, R., Hull, D., Siddhartha, T. (2020). Antimicrobial resistance and virulence factors profile of Salmonella spp. and Escherichia coli isolated from different environments exposed to anthropogenic activity. J Glob Antimicrob Resist, 22, 578-583.
  4. Bettelheim, K., Goldwater P. 2014. Serotypes of Non-O157 Shigatoxigenic Escherichia coli (STEC). Adv Microb, 04, 377-389.
  5. Beutin, L., Krüger, U., Krause, G., Miko, A., Martin, A., Strauch, E. (2008). Evaluation of major types of Shiga toxin 2E-producing Escherichia coli bacteria present in food, pigs, and the environment as potential pathogens for humans. Appl Environ Microbiol, 74, 4806-4816.
  6. Bibbal, D., Loukiadis, E., Kérourédan, M., Ferré, F., Dilasser, F., Peytavin de Garam, C., Cartier, P., Oswald, E., Gay, E., Auvray, F., Brugère, H. (2015). Prevalence of carriage of Shiga toxin-producing Escherichia coli serotypes O157:H7, O26:H11, O103:H2, O111:H8, and O145:H28 among slaughtered adult cattle in France. Appl Environ Microbiol, 81, 1397-1405.
  7. Blanco, M., Padola, N.L., Krüger, A., Sanz, M.E., Blanco, J.E., González, E.A., Ghizlane, D., Azucena, M., Bernárdez, M.I., Etcheverría, A.I., Arroyo, G.H., Lucchesi, P.M.A., Parma, A.E., Blanco, J. (2004). Virulence genes and intimin types of Shiga-toxin-producing Escherichia coli isolated from cattle and beef products in Argentina. Int Microbiol, 7, 269-276.
  8. Bumunang, E.W., McAllister, T.A., Zaheer, R., Polo, R.O., Stanford, K., King, R., Niu, Y.D., Ateba, C.N. (2019). Characterization of Non-O157 Escherichia coli from Cattle Faecal Samples in the North-West Province of South Africa. Microorganisms, 7, 272.
  9. Cap, M., Carbonari, C.C., D’Astek, B.A., Zolezzi, G., Deza, N., Palladino, M.P., Masana, M., Chinen, I., Rivas, M. (2019). Frequency, characterization and genotypic analysis of Shiga toxin-producing Escherichia coli in beef slaughterhouses of Argentina. Rev Argent Microbiol, 51, 32-38.
  10. Carter, M.Q., Brandl, M.T., Kudva, I.T., Katani, R., Moreau, M.R., Kapur, V. (2017). Conditional Function of Autoaggregative Protein Cah and Common cah Mutations in Shiga Toxin-Producing Escherichia coli. Appl Environ Microbiol, 84, e01739-17.
  11. Cernicchiaro, N., Cull, C.A., Paddock, Z.D., Shi, X., Bai, J., Nagaraja, T.G., Renter, D.G. (2013). Prevalence of Shiga Toxin–Producing Escherichia coli and Associated Virulence Genes in Feces of Commercial Feedlot Cattle. Foodborne Pathog Dis, 10, 835-841.
  12. Clermont, O., Christenson, J.K., Denamur, E., Gordon, D.M. (2013). The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep, 5, 58-65.
  13. Clinical and Laboratory Standards Institute, CLSI. (2017). Performance Standards for Antimicrobial Susceptibility Testing. CLSI supplement M100.
  14. Cóppola, N., Freire, B., Umpiérrez, A., Cordeiro, N.F., Ávila, P., Trenchi, G., Castro, G., Casaux, M.L., Fraga, M., Zunino, P., Bado, I., Vignoli, R. (2020). Transferable resistance to highest priority critically important antibiotics for human health in Escherichia coli strains obtained from livestock feces in Uruguay. Front Vet Sci, 7, 588919.
  15. Daly, R.F., & Hill, N.T. (2016). Characterizing the Role of Animal Exposures in Cryptosporidiosis and Shiga Toxin-producing Escherichia coli Infections: South Dakota, 2012. Zoonoses Public Health, 63, 467-476.
  16. EFSA BIOHAZ Panel. (2020). Pathogenicity assessment of Shiga toxin‐producing Escherichia coli (STEC) and the public health risk posed by contamination of food with STEC. EFSA Journal 18, e05967.
  17. Fan, R., Shao, K., Yang, X., Bai, X., Fu, S., Sun, H., Xu, Y., Wang, H., Li, Q., Hu, B., Zhang, J., Xiong, Y. (2019). High prevalence of non-O157 Shiga toxin-producing Escherichia coli in beef cattle detected by combining four selective agars. BMC Microbiol, 19, 213.
  18. Gadea, M.dP., Deza, N., Mota, M.I., Carbonari, C., Robatto, M., D`Astek, B., Balseiro, V., Bazet, C., Rügnitz, E., Livrelli, V., Schelotto, F., Rivas, M., Varela, G. (2012). Two cases of urinary tract infection caused by Shiga toxin-producing Escherichia coli O157:H7 strains. Rev Argent Microbiol, 44, 94-96.
  19. García-Fulgueiras, V., Caiata, L., Bado, I., Giachetto, G., Robino, L. (2021). Antibiotic susceptibility and fosfomycin resistance characterization in a cohort of children older than 6 years of age with urinary tract infection. Rev Argent Microbiol, S0325-7541(21)00055-9.
  20. Gyles, J.M., & Fairbrother, F.C.L. (2010). Escherichia coli. En: Gyles CL, Prescott JF, Songer JG, Thoen CO, editors. Pathogenesis of Bacterial Infections in Animals, Wiley-Blackwell, Pp 276–308.
  21. Jajarmi, M., Imanifooladi, A.A., Badouei, M.A., Ahmadi, A. (2017). Virulence genes, Shiga toxin subtypes, major O-serogroups, and phylogenetic background of Shiga toxin-producing Escherichia coli strains isolated from cattle in Iran. Microb Pathog, 109, 274-279.
  22. Kintz, E., Brainard, J., Hooper, L., Hunter, P. (2017). Transmission pathways for sporadic Shiga-toxin producing E. coli infections: A systematic review and meta-analysis. Int J Hyg Environ Health, 220, 57-67.
  23. Kjaergaard, K., Schembri, M.A., Hasman, H., Klemm, P. (2000). Antigen 43 from Escherichia coli induces inter- and intraspecies cell aggregation and changes in colony morphology of Pseudomonas fluorescens. J Bacteriol, 182, 4789-4796.
  24. Majowicz, S.E., Scallan, E., Jones-Bitton, A., Sargeant, J.M., Stapleton, J., Angulo, F.J., Yeung, D.H., Krik, M.D. (2014). Global incidence of human Shiga toxin-producing Escherichia coli infections and deaths: a systematic review and knowledge synthesis. Foodborne Pathog Dis, 1, 447-455.
  25. Marshall, B.M., & Levy, S.B. (2011). Food Animals and Antimicrobials: Impacts on Human Health. Clin Microbiol Rev 24, 718-733.
  26. Matheus-Guimarães, C., Gonçalves, E.M., Guth, B.E.C. (2014). Interactions of O157 and non-O157 Shiga toxin-producing Escherichia coli (STEC) recovered from bovine hide and carcass with human cells and abiotic surfaces. Foodborne Pathog Dis, 11, 248-255.
  27. Mir, R.A., & Kudva, I.T. (2019). Antibiotic-resistant Shiga toxin-producing Escherichia coli: An overview of prevalence and intervention strategies. Zoonoses Public Health, 66, 1-13.
  28. Montero, D.A., Velasco, J., Del Canto, F., Puente, J.L., Padola, N.L., Rasko, D.A., Farfán, M., Salazar, J.C., Vidal, R. (2017). Locus of Adhesion and Autoaggregation (LAA), a pathogenicity island present in emerging Shiga Toxin-producing Escherichia coli strains. Sci Rep, 7, 7011.
  29. Mora, A., Blanco, J.E., Blanco, M., Alonso, M.P., Dhabi, G., Echeita, A., González, E.A., Bernárdez, M.I., Blanco, J. (2005). Antimicrobial resistance of Shiga toxin (verotoxin)-producing Escherichia coli O157:H7 and non-O157 strains isolated from humans, cattle, sheep and food in Spain. Res Microbiol, 156, 793-806.
  30. Paddock, Z., Shi, X., Bai, J., Nagaraja, T.G. (2012). Applicability of a multiplex PCR to detect O26, O45, O103, O111, O121, O145, and O157 serogroups of Escherichia coli in cattle feces. Vet Microbiol, 156, 381-388.
  31. Patel, J.B. (2014). Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fourth Informational Supplement.
  32. Pérez, L., Apezteguía, L., Piñeyrúa, C., Dabezies, A., Bianco, M.N., Schelotto, F., Varela, G. (2014). Hemolytic uremic syndrome with mild renal involvement due to Shiga toxin-producing Escherichia coli (STEC) O145 strain. Rev Argent Microbiol, 46, 103-106.
  33. Rehman, M.A., Yin, X., Persaud-Lachhman, M.G., Diarra, M.S. (2017). First Detection of a Fosfomycin Resistance Gene, fosA7, in Salmonella enterica Serovar Heidelberg Isolated from Broiler Chickens. Antimicrob Agents Chemother, 61.
  34. Rivas, M., Chinen, I., Miliwebsky, E., Masana, M. (2014). Risk Factors for Shiga Toxin-Producing Escherichia coli-Associated Human Diseases. Microbiol Spectr, 2.
  35. Rivelli Zea, S.M., Padola, N.L., Etcheverría, A.I, Florentín, M., Acuña, P., Rodríguez, F., Colello, R., Guillén Fretes, R.M. (2020). Caracterización molecular de aislamientos de Escherichia coli productores de toxina Shiga obtenidos en 2 establecimientos ganaderos del Paraguay. Rev Argent Microbiol, 52, 131-135.
  36. Sapountzis, P., Segura, A., Desvaux, M., & Forano, E. (2020). An Overview of the Elusive Passenger in the Gastrointestinal Tract of Cattle: The Shiga Toxin Producing Escherichia coli. Microorganisms, 8, 877.
  37. Scheutz, F., Teel, L.D., Beutin, L., Piérard, D., Buvens, G., Karch, H., Mellmann, A., Caprioli, A., Tozzoli, R., Morabito, S., Strockbine, N.A., Melton-Celsa, A.R., Sanchez, M., Persson, S., O'Brien, A.D. (2012). Multicenter evaluation of a sequence-based protocol for subtyping Shiga toxins and standardizing Stx nomenclature. J Clin Microbiol, 50, 2951-2963.
  38. Scheutz, F. (2014). Taxonomy Meets Public Health: The Case of Shiga Toxin-Producing Escherichia coli. Microbiol Spectr, 2.
  39. Schroeder, C.M., Meng, J., Zhao, S., DebRoy, C., Torcolini, J., Zhao, C., McDermott, P.F., Wagner, D.D., Walker, R.D., White, D.G. (2002). Antimicrobial resistance of Escherichia coli O26, O103, O111, O128, and O145 from animals and humans. Emerg Infect Dis, 8, 1409-1414.
  40. Seija, V., Medina Presentado, J.C., Bado, I., Papa Ezdra, R., Batista, N., Gutiérrez, C., Guirado, M., Vidal, M., Nin, M., Vignoli, R. (2015). Sepsis caused by New Delhi metallo-β-lactamase (blaNDM-1) and qnrD-producing Morganella morganii, treated successfully with fosfomycin and meropenem: case report and literature review. Int J Infect Dis, 30, 20-26.
  41. Shridhar, P.B., Siepker, C., Noll, L.W., Shi, X., Nagaraja, T.G., Bai, J. (2017). Shiga Toxin Subtypes of Non-O157 Escherichia coli Serogroups Isolated from Cattle Feces. Front Cell Infect Microbiol, 7.
  42. Tenaillon, O., Skurnik, D., Picard, B., Denamur, E. (2010). The population genetics of commensal Escherichia coli. Nat Rev Microbiol, 8, 207-217.
  43. Thomas, K.M., McCann, M.S., Collery, M.M., Logan, A., Whyte, P., McDowell, D.A., Duffy, G. (2012). Tracking verocytotoxigenic Escherichia coli O157, O26, O111, O103 and O145 in Irish cattle. Int J Food Microbiol 153, 288-296.
  44. Torres, A.G., Amaral, M.M., Bentancor, L., Galli, L., Goldstein, J., Krüger, A., Rojas-López, M. (2018). Recent Advances in Shiga Toxin-Producing Research in Latin America. Microorganisms, 6.
  45. Umpiérrez, A., Bado, I., Oliver, M., Acquistapace, S., Etcheverría, A.L., Padola, N.L., Vignoli, R., Zunino, P. (2017). Zoonotic Potential and Antibiotic Resistance of Escherichia coli in Neonatal Calves in Uruguay. Microbes Environ, 32, 275-282.
  46. Umpiérrez, A., Ernst, D., Fernández, M., Oliver, M., Casaux, M.L., Caffarena, R.D., Schild, C., Giannitti, F., Fraga, M., Zunino, P. (2021). Virulence genes of Escherichia coli in diarrheic and healthy calves. Rev Argent Microbiol, 53, 34-38.
  47. Varela, G., Chinen, I., Gadea, M.P., Miliwebsky, E., Mota, M.I., González, S., González, G., Gugliada, M.J., Carbonari, C.C., Algorta, G., Bernadá, M., Sabelli, R., Pardo, L., Rivas, M., Schelotto, F. (2008). Detección y caracterización de Escherichia coli productor de toxina Shiga a partir de casos clínicos y de alimentos en Uruguay. Rev Argent Microbiol, 40, 93–100.
  48. World Health Organization & WHO Advisory Group on Integrated Surveillance of Antimicrobial Resistance (‎AGISAR). (2017). Critically important antimicrobials for human medicine: ranking of antimicrobial agents for risk management of antimicrobial resistance due to non-human use, 5th rev. World Health Organization. https://apps.who.int/iris/handle/10665/255027.
  49. Yang, X., Bai, X., Zhang, J., Sun, H., Fu, S., Fan, R., He, X., Scheutz, F., Matussek, A. (2020a). Escherichia coli strains producing a novel Shiga toxin 2 subtype circulate in China. Int J Med Microbiol, 310, 151377.
  50. Yang, X., Sun, H., Fan, R., Fu, S., Zhang, J., Matussek, A., Xiong, Y., Bai, X. (2020b). Genetic diversity of the intimin gene (eae) in non-O157 Shiga toxin-producing Escherichia coli strains in China. Sci Rep, 10, 3275.

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