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Expression of blaA and blaB and Susceptibility to Penicillins and Cephalosporins in Yersinia enterocolitica from Different Foods

Year 2020, Volume: 79 Issue: 2, 83 - 88, 25.12.2020

Abstract

Objective: Yersinia enterocolitica which is an important foodborne pathogen causing illness in humans is an extremely heterogeneous species consisting of different subtypes. It has the intrinsic resistance to β-lactam antibiotics because of the production of β-lactamases, BlaA and BlaB. Y. enterocolitica exhibits variable susceptibilities to β-lactams.
Materials and Methods: The expression of the blaA and blaB genes by polymerase chain reaction, and the susceptibility to some β-lactams including penicillins and cephalosporins using the broth microdilution and disk diffusion methods were determined. A total of 18 Y. enterocolitica isolates were examined.
Results: Overall, 33.3% of these isolates carried the blaA and blaB genes, all of which were recovered from chicken meat. The wide range of MIC for ampicillin (≤ 2-128 µg/mL) and ceftazidime (≤ 0.0625-2 µg/mL) was also observed. Of the Y. enterocolitica isolates, 55.6% were resistant to ampicillin (≥ 32 µg/mL) while the remaining isolates (44.4%) were susceptible to ampicillin (≤ 8 µg/mL). All isolates were susceptible to ceftazidime at the concentration tested. According to the disk diffusion test, 55.6% and 33.3% of the isolates were resistant to ticarcillin and cefoxitin, respectively. No resistance to piperacillin and ceftriaxone was found.
Conclusion: The results showed that the presence of the blaA and blaB genes and intrinsic resistance against penicillins and cephalosporins were variable among Y. enterocolitica food isolates. Furthermore, the blaA and blaB genes were expressed in most of the resistant isolates to β-lactams, which may indicate the contribution of the genes to the drug resistance.

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References

  • 1. Carniel E, Autenrieth I, Cornelis G, Fukushima H, Guinet F, Isberg R, et al. Y. enterocolitica and Y. pseudotuberculosis. Dworkin M, Falkow S, Rosenberg E, Schleifer, KH, Stackebrandt E, editors. The Prokaryotes. New York, NY: Springer; 2006.p.270-398.
  • 2. Sharma S, Mittal S, Mallik S, Virdi JS. Molecular characterization of β-lactamase genes blaA and blaB of Yersinia enterocolitica biovar 1A. FEMS Microbiol Lett 2006; 257: 319-27.
  • 3. Bhunia AK. Foodborne Microbial Pathogens: Mechanisms and Pathogenesis. New York, NY: Springer; 2008.
  • 4. Logue CM, Sheridan JJ, Wauters G, McDowell DA, Blair IS. Yersinia spp. and numbers, with particular reference to Y. enterocolitica bio/serotypes, occurring on Irish meat and meat products, and the influence of alkali treatment on their isolation. Int J Food Microbiol 1996; 33: 257-74.
  • 5. Capita R, Calleja CA, Prieto M, Fernandez MDCG, Moreno B. Incidence and pathogenicity of Yersinia spp. isolates from poultry in Spain. Food Microbiol 2002; 19: 295-301.
  • 6. Soltan-Dallal MM, Tabarraie A, MoezArdalan K. Comparison of four methods for isolation of Yersinia enterocolitica from raw and pasteurized milk from northern Iran. Int J Food Microbiol 2004; 94: 87-91.
  • 7. Van Damme I, Berkvens D, Botteldoorn N, Dierick K, Wits J, Pochet B, et al. Evaluation of the ISO 10273:2003 method for the isolation of human pathogenic Yersinia enterocolitica from pig carcasses and minced meat. Food Microbiol 2013; 36: 170-5.
  • 8. Martins BTF, Botelho CV, Silva DAL, Lanna FGPA, Grossi JL, Campos-Galvao MEM, et al. Yersinia enterocolitica in a Brazilian pork production chain: Tracking of contamination routes, virulence and antimicrobial resistance. Int J Food Microbiol 2018; 276: 5-9.
  • 9. Ray B. Fundamental Food Microbiology. 3rd ed. Boca Raton, Florida: CRC Press; 2004.
  • 10. Preston MA, Brown S, Borczyk AA, Riley G, Krishnan C. Antimicrobial susceptibility of pathogenic Yersinia enterocolitica isolated in Canada from 1972 to 1990. Antimicrob Agents Chemother 1994; 38: 2121-4.
  • 11. Crowe M, Ashford K, Ispahani P. Clinical features and antibiotic treatment of septic arthritis and osteomyelitis due to Yersinia enterocolitica. J Med Microbiol 1996; 45:
  • 12. Stock I. Natural susceptibility of Yersinia enterocolitica-like species to β-lactam antibiotics. Rev Med Microbiol 2004; 15: 81-92.
  • 13. Fabrega A, Vila J. Yersinia enterocolitica: pathogenesis, virulence and antimicrobial resistance. Enferm Infecc Microbiol Clin 2012; 30: 24-32.
  • 14. Cornelis G, Abraham EP. β- lactamases from Yersinia enterocolitica. J Gen Microbiol 1975; 87: 273-84.
  • 15. Pham JN, Bell SM, Lanzarone JYM. A study of the β-lactamases of 100 clinical isolates of Yersinia enterocolitica. J Antimicrob Chemother 1991; 28: 19-24.
  • 16. Sharma S, Ramnani P, Virdi JS. Detection and assay of β-lactamases in clinical and non-clinical strains of Yersinia enterocolitica biovar 1A. J Antimicrob Chemother 2004; 54: 401-5.
  • 17. Livermore DM. β- Lactamases in laboratory and clinical resistance. Clin Microbiol 1995; 8: 557-84.
  • 18. Stock I, Heisig P, Wiedemann B. Expression of β-lactamases in Yersinia enterocolitica strains of biovars 2, 4 and 5. J Med Microbiol 1999; 48: 1023-7.
  • 19. Stock I, Heisig P, Wiedemann B. β-lactamase expression in Yersinia enterocolitica biovars 1A, 1B, and 3. J Med Microbiol 2000; 49: 403-8.
  • 20. Bent ZW, Young GM. Contribution of BlaA and BlaB β-lactamases to antibiotic susceptibility of Yersinia enterocolitica Biovar 1B. Antimicrob Agents Chemother 2010; 54: 4000-2.
  • 21. Singhal N, Srivastava A, Kumar M, Virdi JS. Structural variabilities in β-lactamase (blaA) of different biovars of Yersinia enterocolitica: implications for β-lactam antibiotic and β-lactamase inhibitor susceptibilities. PloS One 2015; 10(4): e0123564.
  • 22. Neubauer H, Hensel A, Aleksic S, Meyer H. Identification of Yersinia enterocolitica within the genus Yersinia. Syst Appl Microbiol 2000; 23: 58-62.
  • 23. Bottone EJ, Bercovier H, Mollaret HH. Genus XLI. Yersinia. Garrity GM, Brenner DJ, Krieg NR, Staley JT, editors. Bergey’s manual of systematic bacteriology. New York, NY: Springer; 2005. p. 838-48.
  • 24. Ausubel FM, Kingston RE, Brent R, Moore DD, Seidman J, Smith JA, et al. editors. Current protocols in molecular biology. New York, NY: Greene Publishing Associates & Wiley Interscience; 1991.
  • 25. Meyer C, Stolle A, Fredriksson-Ahomaa M. Comparison of broth microdilution and disk diffusion test for antimicrobial resistance testing in Yersinia enterocolitica 4/O:3 strains. Microb Drug Resist 2011; 17: 479-84.
  • 26. International Standard. Susceptibility testing of infectious agents and evaluation of performance of antimicrobial susceptibility test devices-Part 1: Broth micro-dilution reference method for testing the in vitro activity of antimicrobial agents against rapidly growing aerobic bacteria involved in infectious diseases. Geneva, Switzerland; ISO 20776-1: 2019.
  • 27. Clinical and Laboratory Standards Institute (CLSI), Performance standards for Antimicrobial Susceptibility Testing; Twenty-sixth Edition, in, Wayne, PA, USA, 2016.
  • 28. Ye Q, Wu Q, Hu H, Zhang J, Huang H. Prevalence and characterization of Yersinia enterocolitica isolated from retail foods in China. Food Control 2016; 61: 20-7.
  • 29. Kot B, Piechota M, Jakubiak K. Virulence genes and antibiotic resistance of Yersinia enterocolitica strains isolated from children. EJBR 2017; 7: 366-73.
  • 30. Singhal N, Kumar M, Virdi JS. Molecular analysis of β-Lactamase genes to understand their differential expression in strains of Yersinia enterocolitica biotype 1A. Sci Rep 2014; 4:5270.
  • 31. Pham JN, Bell SM, Martin L, Carniel E. The β-lactamases and β-lactam antibiotic susceptibility of Yersinia enterocolitica. J Antimicrob Chemother 2000; 46: 951-7.
  • 32. Mittal S, Mallik S, Sharma S, Virdi JS. Characteristics of β-lactamases and their genes (blaA and blaB) in Yersinia intermedia and Y. frederiksenii. BMC Microbiol 2007; 7:25.
  • 33. Fabrega A, Balleste-Delpierre C, Vila J. Antimicrobial resistance in Yersinia enterocolitica. Chen C-Y, Yan X, Jackson CR, editors. Antimicrobial Resistance and Food Safety; 2015.p.77-104.
  • 34. Peng Z, Zou M, Li M, Liu D, Guan W, Hao Q, et al. Prevalence, antimicrobial resistance and phylogenetic characterization of Yersinia enterocolitica in retail poultry meat and swine feces in parts of China. Food Control 2018; 93: 121-8.
  • 35. Kwaga J, Iversen JO. In vitro antimicrobial susceptibilities of Yersinia enterocolitica and related species isolated from slaughtered pigs and pork products. Antimicrob Agents Chemother 1990; 34: 2423-5.
  • 36. Verbikova V, Borilova G, Babak V, Moravkova M. Prevalence, characterization and antimicrobial susceptibility of Yersinia enterocolitica and other Yersinia species found in fruits and vegetables from the European Union. Food Control 2018; 85: 161-7.
  • 37. Bonke R, Wacheck S, Stuber E, Meyer C, Martlbauer E, Fredriksson-Ahomaa M. Antimicrobial susceptibility and distribution of β-lactamase A (blaA) and β-lactamase B (blaB) genes in enteropathogenic Yersinia species. Microb Drug Resist 2011; 17: 575-81.
  • 38. Abdel-Haq NM, Papadopol R, Asmar BI, Brown WJ. Antibiotic susceptibilities of Yersinia enterocolitica recovered from children over a 12-year period. Int J Antimicrob Agents 2006; 27: 449-52.
  • 39. Weiner M. ERIC-based differentiation and antimicrobial susceptibility of Yersinia enterocolitica O:9 isolated from animals serologically positive and negative for brucellosis. Bull Vet Inst Pulawy 2013; 57: 493-8.
  • 40. Frazao MR, Andrade LN, Darini ALC, Falcao JP. Antimicrobial resistance and plasmid replicons in Yersinia enterocolitica strains isolated in Brazil in 30 years. Braz J Infect Dis 2017; 21: 477-80.
  • 41. Ye Q, Wu Q, Hu H, Zhang J, Huang H. Prevalence, antimicrobial resistance and genetic diversity of Yersinia enterocolitica isolated from retail frozen foods in China. FEMS Microbiol Lett 2015; 362: 1-7.
  • 42. Baumgartner A, Kuffer M, Suter D, Jemni T, Rohner P. Antimicrobial resistance of Yersinia enterocolitica strains from human patients, pigs and retail pork in Switzerland. Int J Food Microbiol 2007; 115: 110-4.
  • 43. Bonardi S, Bassi L, Brindani F, D’Incau M, Barco L, Carra E, et al. Prevalence, characterization and antimicrobial susceptibility of Salmonella enterica and Yersinia enterocolitica in pigs at slaughter in Italy. Int J Food Microbiol 2013; 163: 248-57.
Year 2020, Volume: 79 Issue: 2, 83 - 88, 25.12.2020

Abstract

References

  • 1. Carniel E, Autenrieth I, Cornelis G, Fukushima H, Guinet F, Isberg R, et al. Y. enterocolitica and Y. pseudotuberculosis. Dworkin M, Falkow S, Rosenberg E, Schleifer, KH, Stackebrandt E, editors. The Prokaryotes. New York, NY: Springer; 2006.p.270-398.
  • 2. Sharma S, Mittal S, Mallik S, Virdi JS. Molecular characterization of β-lactamase genes blaA and blaB of Yersinia enterocolitica biovar 1A. FEMS Microbiol Lett 2006; 257: 319-27.
  • 3. Bhunia AK. Foodborne Microbial Pathogens: Mechanisms and Pathogenesis. New York, NY: Springer; 2008.
  • 4. Logue CM, Sheridan JJ, Wauters G, McDowell DA, Blair IS. Yersinia spp. and numbers, with particular reference to Y. enterocolitica bio/serotypes, occurring on Irish meat and meat products, and the influence of alkali treatment on their isolation. Int J Food Microbiol 1996; 33: 257-74.
  • 5. Capita R, Calleja CA, Prieto M, Fernandez MDCG, Moreno B. Incidence and pathogenicity of Yersinia spp. isolates from poultry in Spain. Food Microbiol 2002; 19: 295-301.
  • 6. Soltan-Dallal MM, Tabarraie A, MoezArdalan K. Comparison of four methods for isolation of Yersinia enterocolitica from raw and pasteurized milk from northern Iran. Int J Food Microbiol 2004; 94: 87-91.
  • 7. Van Damme I, Berkvens D, Botteldoorn N, Dierick K, Wits J, Pochet B, et al. Evaluation of the ISO 10273:2003 method for the isolation of human pathogenic Yersinia enterocolitica from pig carcasses and minced meat. Food Microbiol 2013; 36: 170-5.
  • 8. Martins BTF, Botelho CV, Silva DAL, Lanna FGPA, Grossi JL, Campos-Galvao MEM, et al. Yersinia enterocolitica in a Brazilian pork production chain: Tracking of contamination routes, virulence and antimicrobial resistance. Int J Food Microbiol 2018; 276: 5-9.
  • 9. Ray B. Fundamental Food Microbiology. 3rd ed. Boca Raton, Florida: CRC Press; 2004.
  • 10. Preston MA, Brown S, Borczyk AA, Riley G, Krishnan C. Antimicrobial susceptibility of pathogenic Yersinia enterocolitica isolated in Canada from 1972 to 1990. Antimicrob Agents Chemother 1994; 38: 2121-4.
  • 11. Crowe M, Ashford K, Ispahani P. Clinical features and antibiotic treatment of septic arthritis and osteomyelitis due to Yersinia enterocolitica. J Med Microbiol 1996; 45:
  • 12. Stock I. Natural susceptibility of Yersinia enterocolitica-like species to β-lactam antibiotics. Rev Med Microbiol 2004; 15: 81-92.
  • 13. Fabrega A, Vila J. Yersinia enterocolitica: pathogenesis, virulence and antimicrobial resistance. Enferm Infecc Microbiol Clin 2012; 30: 24-32.
  • 14. Cornelis G, Abraham EP. β- lactamases from Yersinia enterocolitica. J Gen Microbiol 1975; 87: 273-84.
  • 15. Pham JN, Bell SM, Lanzarone JYM. A study of the β-lactamases of 100 clinical isolates of Yersinia enterocolitica. J Antimicrob Chemother 1991; 28: 19-24.
  • 16. Sharma S, Ramnani P, Virdi JS. Detection and assay of β-lactamases in clinical and non-clinical strains of Yersinia enterocolitica biovar 1A. J Antimicrob Chemother 2004; 54: 401-5.
  • 17. Livermore DM. β- Lactamases in laboratory and clinical resistance. Clin Microbiol 1995; 8: 557-84.
  • 18. Stock I, Heisig P, Wiedemann B. Expression of β-lactamases in Yersinia enterocolitica strains of biovars 2, 4 and 5. J Med Microbiol 1999; 48: 1023-7.
  • 19. Stock I, Heisig P, Wiedemann B. β-lactamase expression in Yersinia enterocolitica biovars 1A, 1B, and 3. J Med Microbiol 2000; 49: 403-8.
  • 20. Bent ZW, Young GM. Contribution of BlaA and BlaB β-lactamases to antibiotic susceptibility of Yersinia enterocolitica Biovar 1B. Antimicrob Agents Chemother 2010; 54: 4000-2.
  • 21. Singhal N, Srivastava A, Kumar M, Virdi JS. Structural variabilities in β-lactamase (blaA) of different biovars of Yersinia enterocolitica: implications for β-lactam antibiotic and β-lactamase inhibitor susceptibilities. PloS One 2015; 10(4): e0123564.
  • 22. Neubauer H, Hensel A, Aleksic S, Meyer H. Identification of Yersinia enterocolitica within the genus Yersinia. Syst Appl Microbiol 2000; 23: 58-62.
  • 23. Bottone EJ, Bercovier H, Mollaret HH. Genus XLI. Yersinia. Garrity GM, Brenner DJ, Krieg NR, Staley JT, editors. Bergey’s manual of systematic bacteriology. New York, NY: Springer; 2005. p. 838-48.
  • 24. Ausubel FM, Kingston RE, Brent R, Moore DD, Seidman J, Smith JA, et al. editors. Current protocols in molecular biology. New York, NY: Greene Publishing Associates & Wiley Interscience; 1991.
  • 25. Meyer C, Stolle A, Fredriksson-Ahomaa M. Comparison of broth microdilution and disk diffusion test for antimicrobial resistance testing in Yersinia enterocolitica 4/O:3 strains. Microb Drug Resist 2011; 17: 479-84.
  • 26. International Standard. Susceptibility testing of infectious agents and evaluation of performance of antimicrobial susceptibility test devices-Part 1: Broth micro-dilution reference method for testing the in vitro activity of antimicrobial agents against rapidly growing aerobic bacteria involved in infectious diseases. Geneva, Switzerland; ISO 20776-1: 2019.
  • 27. Clinical and Laboratory Standards Institute (CLSI), Performance standards for Antimicrobial Susceptibility Testing; Twenty-sixth Edition, in, Wayne, PA, USA, 2016.
  • 28. Ye Q, Wu Q, Hu H, Zhang J, Huang H. Prevalence and characterization of Yersinia enterocolitica isolated from retail foods in China. Food Control 2016; 61: 20-7.
  • 29. Kot B, Piechota M, Jakubiak K. Virulence genes and antibiotic resistance of Yersinia enterocolitica strains isolated from children. EJBR 2017; 7: 366-73.
  • 30. Singhal N, Kumar M, Virdi JS. Molecular analysis of β-Lactamase genes to understand their differential expression in strains of Yersinia enterocolitica biotype 1A. Sci Rep 2014; 4:5270.
  • 31. Pham JN, Bell SM, Martin L, Carniel E. The β-lactamases and β-lactam antibiotic susceptibility of Yersinia enterocolitica. J Antimicrob Chemother 2000; 46: 951-7.
  • 32. Mittal S, Mallik S, Sharma S, Virdi JS. Characteristics of β-lactamases and their genes (blaA and blaB) in Yersinia intermedia and Y. frederiksenii. BMC Microbiol 2007; 7:25.
  • 33. Fabrega A, Balleste-Delpierre C, Vila J. Antimicrobial resistance in Yersinia enterocolitica. Chen C-Y, Yan X, Jackson CR, editors. Antimicrobial Resistance and Food Safety; 2015.p.77-104.
  • 34. Peng Z, Zou M, Li M, Liu D, Guan W, Hao Q, et al. Prevalence, antimicrobial resistance and phylogenetic characterization of Yersinia enterocolitica in retail poultry meat and swine feces in parts of China. Food Control 2018; 93: 121-8.
  • 35. Kwaga J, Iversen JO. In vitro antimicrobial susceptibilities of Yersinia enterocolitica and related species isolated from slaughtered pigs and pork products. Antimicrob Agents Chemother 1990; 34: 2423-5.
  • 36. Verbikova V, Borilova G, Babak V, Moravkova M. Prevalence, characterization and antimicrobial susceptibility of Yersinia enterocolitica and other Yersinia species found in fruits and vegetables from the European Union. Food Control 2018; 85: 161-7.
  • 37. Bonke R, Wacheck S, Stuber E, Meyer C, Martlbauer E, Fredriksson-Ahomaa M. Antimicrobial susceptibility and distribution of β-lactamase A (blaA) and β-lactamase B (blaB) genes in enteropathogenic Yersinia species. Microb Drug Resist 2011; 17: 575-81.
  • 38. Abdel-Haq NM, Papadopol R, Asmar BI, Brown WJ. Antibiotic susceptibilities of Yersinia enterocolitica recovered from children over a 12-year period. Int J Antimicrob Agents 2006; 27: 449-52.
  • 39. Weiner M. ERIC-based differentiation and antimicrobial susceptibility of Yersinia enterocolitica O:9 isolated from animals serologically positive and negative for brucellosis. Bull Vet Inst Pulawy 2013; 57: 493-8.
  • 40. Frazao MR, Andrade LN, Darini ALC, Falcao JP. Antimicrobial resistance and plasmid replicons in Yersinia enterocolitica strains isolated in Brazil in 30 years. Braz J Infect Dis 2017; 21: 477-80.
  • 41. Ye Q, Wu Q, Hu H, Zhang J, Huang H. Prevalence, antimicrobial resistance and genetic diversity of Yersinia enterocolitica isolated from retail frozen foods in China. FEMS Microbiol Lett 2015; 362: 1-7.
  • 42. Baumgartner A, Kuffer M, Suter D, Jemni T, Rohner P. Antimicrobial resistance of Yersinia enterocolitica strains from human patients, pigs and retail pork in Switzerland. Int J Food Microbiol 2007; 115: 110-4.
  • 43. Bonardi S, Bassi L, Brindani F, D’Incau M, Barco L, Carra E, et al. Prevalence, characterization and antimicrobial susceptibility of Salmonella enterica and Yersinia enterocolitica in pigs at slaughter in Italy. Int J Food Microbiol 2013; 163: 248-57.
There are 43 citations in total.

Details

Primary Language English
Journal Section Research Articles
Authors

Fatma Ozdemır This is me 0000-0002-4804-936X

Seza Arslan This is me 0000-0002-2478-6875

Hafize Gizem Erturk This is me 0000-0001-8151-5185

Publication Date December 25, 2020
Submission Date May 8, 2020
Published in Issue Year 2020 Volume: 79 Issue: 2

Cite

AMA Ozdemır F, Arslan S, Erturk HG. Expression of blaA and blaB and Susceptibility to Penicillins and Cephalosporins in Yersinia enterocolitica from Different Foods. Eur J Biol. December 2020;79(2):83-88.