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Prevalence of antimicrobial resistance and integrons in extended-spectrum β-lactamases producing Escherichia coli isolated from Nakdong and Gumho river

낙동강과 금호강에서 분리된 광범위 베타 락탐 분해효소 생성 Escherichia coli 내 항균제 내성 및 integrons의 분포

  • Cho, Jae-Keun (Metropolitan Health & Environmental Research Institute) ;
  • Kim, Hwan-Deuk (Metropolitan Health & Environmental Research Institute) ;
  • Kwon, Soon-Hyo (Metropolitan Health & Environmental Research Institute) ;
  • Kim, Jin-Hyun (Gyeongbuk Veterinary Service Laboratory) ;
  • Jang, Sung-Il (Metropolitan Health & Environmental Research Institute) ;
  • Park, Choi-Kyu (College of Veterinary Medicine, Kyungpook National University) ;
  • Kim, Ki-Seuk (College of Veterinary Medicine, Kyungpook National University)
  • 조재근 (대구광역시보건환경연구원) ;
  • 김환득 (대구광역시보건환경연구원) ;
  • 권순효 (대구광역시보건환경연구원) ;
  • 김진현 (경상북도가축위생시험소) ;
  • 장성일 (대구광역시보건환경연구원) ;
  • 박최규 (경북대학교 수의과대학) ;
  • 김기석 (경북대학교 수의과대학)
  • Received : 2014.01.02
  • Accepted : 2014.03.04
  • Published : 2014.03.30

Abstract

This study was conducted to investigate the antimicrobial resistance, presence of ${\beta}$-lactamase genes and integrons in 83 ESBL-producing Escherichia coli isolated from Nakdong river and Geumho river in Daegu. Among the ${\beta}$-lactam antimicrobials, all isolates were resistant to ampicillin, cephalothin, cefamandole and cefotaxime, followed by piperacillin (98.8%), ampicillin/sulbactam (86.7%), aztreonam (60.2%) and cefepime (59.0%), whereas resistance to piperacillin/tazobacram, ticarcillin/clavulanic acid and cefoxitin was less than 30%. Many of the ESBL-producing Escherichia coli were also resistant to non-${\beta}$-lactams antimicrobials such as nalidixic acid (83.1%), sulfonamides (72.3%), ciprofloxacin (62.7%) and gentamicin (38.6%). All isolates showed resistance to seven or more antimicrobial agents. The most frequently detected gene was $bla_{TEM+CTX-M}$ (49.4%), followed by $bla_{CTX-M}$ (27.7%), $bla_{TEM}$ (6.0%) and $bla_{OXA}$ (1.2%). But $bla_{SHV}$ was not found. Class 1 integrons were found in 61.4% (51 isolates) of isolates, however, class 2 and 3 integrons were not detected. The results showed water from Nakdong river and Geumho river is contaminated with ESBL-producing E. coli isolates. These results suggest the need for further investigation of antibiotic resistant bacteria to prevent public health impacts in the water environment.

Keywords

References

  1. Ash RJ, Mauck B, Morgan M. 2002. Antibiotic resistance of gramnegative bacteria in rivers, United States. Emerg Infect Dis 8: 713-716. https://doi.org/10.3201/eid0807.010264
  2. Bauer AW, Kirby WM, Sherris JC, Turck M. 1966. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45: 493-496.
  3. Baquero F, Martinez JL, Canton R. 2008. Antibiotics and antibiotic resistance in water environments. Curr Opin Biotechnol 19: 260-265. https://doi.org/10.1016/j.copbio.2008.05.006
  4. Belaaouaj A, Lapoumeroulie C, Canica MM, Vedel G, Nevot P, Krishnamoorthy R, Paul G. 1994. Nucleotide sequences of the genes coding for the TEM-like beta-lactamases IRT-1 and IRT-2 (formerly called TRI-1 and TRI-2). FEMS Microbiol Lett 120: 75-80.
  5. Bradford PA. 2001. Extended-spectrum $\beta$-lactamases in the 21st century: Characterization, epidemiology, and detection of this important resistance threat. Clin Microbiol Rev 14: 933-951. https://doi.org/10.1128/CMR.14.4.933-951.2001
  6. Cambray G, Guerout A, Mazel D. 2010. Integrons. Annu Rev Gen 44: 141-166. https://doi.org/10.1146/annurev-genet-102209-163504
  7. Chen H, Shu W, Chang X, Chen JA, Guo Y, Tan Y. 2010. The profile of antibiotics resistance and integrons of extended- spectrum beta-lactamase producing thermotolerant coliforms isolated from the Yangtze River basin in Chongqing. Environ Pollut 158: 2459-2464. https://doi.org/10.1016/j.envpol.2010.03.023
  8. Chen B, Zheng W, Yu Y, Huang W, Zheng S, Zhang Y, Guan X, Zhuang Y, Chen N, Topp E. 2011. Class 1 integrons, selected virulence genes, and antibiotic resistance in Escherichia coli isolates from the Minjiang River, Fujian Province, China. Appl Environ Microbiol 77: 148-155. https://doi.org/10.1128/AEM.01676-10
  9. Cho JK, Sung MS, Kim JH, Kim KS. 2011. Detection of CTX-M and TEM type extended-spectrum $\beta$-lactamases in Escherichia coli isolated from livestocks in Korea. Kor J Vet Serv 34: 37-43. https://doi.org/10.7853/kjvs.2011.34.1.037
  10. CLSI. Clinical and Laboratory Standards Institute. 2012. Performance standards for antimicrobial susceptibility testing; Twenty-second informational supplement. M100-S22. Wayne, Pa, USA.
  11. Cocchi S, Grasselli E, Gutacker M, Benagli C, Convert M, Piffaretti JC. 2007. Distribution and characterization of integrons in Escherichia coli strains of animal and human origin. FEMS Immunol Med Microbiol 50: 126-132. https://doi.org/10.1111/j.1574-695X.2007.00242.x
  12. Coque TM, Oliver A, Perez-Diaz JC, Baquero F, Canton R. 2002. Genes encoding TEM-4, SHV-2, and CTX-M-10 extended- spectrum beta-lactamases are carried by multiple Klebsiella pneumoniae clones in a single hospital (Madrid, 1989 to 2000). Antimicrob Agents Chemother 46: 500-510. https://doi.org/10.1128/AAC.46.2.500-510.2002
  13. Dhanji H, Murphy NM, Akhigbe C, Doumith M, Hope R, Livermore DM, Woodford N. 2011. Isolation of fluoroquinolone- resistant O25b:H4-ST131 Escherichia coli with CTX-M-14 extended-spectrum $\beta$-lactamase from UK river water. J Antimicrob Chemother 66: 512-516. https://doi.org/10.1093/jac/dkq472
  14. Ferreira da Silva M, Vaz-Moreira I, Gonzalez-Pajuelo M, Nunes OC, Manaia CM. 2007. Antimicrobial resistance patterns in Enterobacteriaceae isolated from an urban wastewater treatment plant. FEMS Microbiol Ecol 60: 166-176. https://doi.org/10.1111/j.1574-6941.2006.00268.x
  15. Goldstein C, Lee MD, Sanchez S, Hudson C, Phillips B, Register B, Grady M, Liebert C, Summers AO, White DG, Maurer JJ. 2001. Incidence of class 1 and 2 integrases in clinical and commensal bacteria from livestock, companion animals, and exotics. Antimicrob Agents Chemother 45: 723-726. https://doi.org/10.1128/AAC.45.3.723-726.2001
  16. Jang J, Suh YS, Di DY, Unno T, Sadowsky MJ, Hur HG. 2013. Pathogenic Escherichia coli strains producing extended spectrum $\beta$-lactamases in the Yeongsan river basin of South Korea. Environ Sci Technol 47: 1128-1136. https://doi.org/10.1021/es303577u
  17. Jeong SH, Bae IK, Lee JH, Sohn SG, Kang GH, Jeon GJ, Kim YH, Jeong BC, Lee SH. 2004. Molecular characterization of extended-spectrum beta-lactamases produced by clinical isolates of Klebsiella pneumoniae and Escherichia coli from a Korean nationwide survey. J Clin Microbiol 42: 2902-2906. https://doi.org/10.1128/JCM.42.7.2902-2906.2004
  18. Kang HY, Jeong YS, Oh JY, Tae SH, Choi CH, Moon DC, Lee WK, Lee YC, Seol SY, Cho DT, Lee JC. 2005. Characterization of antimicrobial resistance and class 1 integrons found in Escherichia coli isolates from humans and animals in Korea. J Antimicrob Chemother 55: 639-644. https://doi.org/10.1093/jac/dki076
  19. Kim J, Kang HY, Lee Y. 2008. The identification of CTX-M-14, TEM-52, and CMY-1 enzymes in Escherichia coli isolated from the Han River in Korea. J Microbiol 46: 478-481. https://doi.org/10.1007/s12275-008-0150-y
  20. Kim JH, Zheng XH, Cho JK, Sung MS, Kim KS. 2012. Prevalence and characterization of extended-spectrum $\beta$-lactamase among Escherichia coli isolated from Geumho river in Korea. J Pure and Appl Microb 6: 989-1000.
  21. Laroche E, Pawlak B, Berthe T, Skurnik D, Petit F. 2009. Occurrence of antibiotic resistance and class 1, 2 and 3 integrons in Escherichia coli isolated from a densely populated estuary (Seine, France). FEMS Microbiol Ecol 68: 118-130. https://doi.org/10.1111/j.1574-6941.2009.00655.x
  22. Lee HG, Kim HJ, Kim GD. 2007. Typing of $\beta$-Lactamase of Escherichia coli and Klebsiella pneumoniae isolated from rivers in Busan, Korea. Kor J Microbiol 43: 116-123.
  23. Lee S, Park YJ, Kim M, Lee HK, Han K, Kang CS, Kang MW. 2005. Prevalence of Ambler class A and D beta-lactamases among clinical isolates of Pseudomonas aeruginosa in Korea. J Antimicrob Chemother 56: 122-127. https://doi.org/10.1093/jac/dki160
  24. Lee SG, Jeong SH, Lee H, Kim CK, Lee Y, Koh E, Chong Y, Lee K. 2009. Spread of CTX-M- type extended-spectrum beta-lactamases among bloodstream isolates of Escherichia coli and Klebsiella pneumoniae from a Korean hospital. Diagn Microbiol Infect Dis 63: 76-80. https://doi.org/10.1016/j.diagmicrobio.2008.09.002
  25. Lim SK, Lee HS, Nam HM, Jung SC, Bae YC. 2009. CTX-M-type beta-lactamase in Escherichia coli isolated from sick animals in Korea. Microb Drug Resist 15: 139-142. https://doi.org/10.1089/mdr.2009.0901
  26. Lu SY, Zhang YL, Geng SN, Li TY, Ye ZM, Zhang DS, Zou F, Zhou HW. 2010. High diversity of extended-spectrum beta-lactamase-producing bacteria in an urban river sediment habitat. Appl Environ Microbiol 76: 5972-5976. https://doi.org/10.1128/AEM.00711-10
  27. Machado E, Ferreira J, Novais A, Peixe L, Canton R, Baquero F, Coque TM. 2007. Preservation of integron types among Enterobacteriaceae producing extended-spectrum beta-lactamases in a Spanish hospital over a 15-year period (1988 to 2003). Antimicrob Agents Chemother 51: 2201-2204. https://doi.org/10.1128/AAC.01389-06
  28. Martinez JL 2009. Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ Pollut 157: 2893-2902. https://doi.org/10.1016/j.envpol.2009.05.051
  29. Mazel D, Dychinco B, Webb VA, Davies J. 2000. Antibiotic resistance in the ECOR collection: integrons and identification of a novel aad gene. Antimicrob Agents Chemother 44: 1568- 1574. https://doi.org/10.1128/AAC.44.6.1568-1574.2000
  30. Mukherjee S, Chakraborty R. 2006. Incidence of class 1 integrons in multiple antibiotic-resistant Gram-negative copiotrophic bacteria from the River Torsa in India. Res Microbiol 157: 220-226. https://doi.org/10.1016/j.resmic.2005.08.003
  31. Oliver A, Perez-Vazquez M, Martinez-Ferrer M, Baquero F, De Rafael L, Canton R. 1999. Ampicillin-sulbactam and amoxicillin-clavulanate susceptibility testing of Escherichia coli isolates with different beta-lactam resistance phenotypes. Antimicrob Agents Chemother 43: 862-867.
  32. Paterson DL, Bonomo RA. 2005. Extended-spectrum beta-lactamases: a clinical update. Clin Microbiol Rev 18: 657-686. https://doi.org/10.1128/CMR.18.4.657-686.2005
  33. Peak N, Knapp CW, Yang RK, Hanfelt MM, Smith MS, Aga DS, Graham DW. 2007. Abundance of six tetracycline resistance genes in wastewater lagoons at cattle feedlots with different antibiotic use strategies. Environ Microbiol 9: 143-151. https://doi.org/10.1111/j.1462-2920.2006.01123.x
  34. Pitout JD. Thomson KS, Hanson ND, Ehrhardt AF, Moland ES, Sanders CC. 1998. beta-lactamases responsible for resistance to expanded-spectrum cephalosporins in Klebsiella pneumoniae, Escherichia coli, and Proteus mirabilis isolates recovered in South Africa. Antimicrob Agents Chemother 42: 1350-1354.
  35. Reinthaler FF, Feierl G, Galler H, Haas D, Leitner E, Mascher F, Melkes A, Posch J, Winter I, Zarfel G, Marth E. 2010. ESBL-producing Escherichia coli in Austrian sewage sludge. Water Res 44: 1981-1985. https://doi.org/10.1016/j.watres.2009.11.052
  36. Roe MT, Vega E, Pillai SD. 2003. Antimicrobial resistance markers of class 1 and class 2 integron- bearing Escherichia coli from irrigation water and sediments. Emerg Infect Dis 9: 822-826. https://doi.org/10.3201/eid0907.020529
  37. Rosenberg SM. 2001. Evolving responsively: adaptive mutation. Nat Rev Genet 2: 504-515.
  38. Rosser SJ, Young HK. 1999. Identification and characterization of class 1 integrons in bacteria from an aquatic environment. J Antimicrob Chemother 44: 11-18.
  39. Steward CD, Rasheed JK, Hubert SK, Biddle JW, Raney PM, Anderson GJ, Williams PP, Brittain KL, Oliver A, McGowan JE Jr, Tenover FC. 2001. Characterization of clinical isolates of Klebsiella pneumoniae from 19 laboratories using the National Committee for Clinical Laboratory Standards extended-spectrum beta-lactamase detection methods. J Clin Microbiol 39: 2864-2872. https://doi.org/10.1128/JCM.39.8.2864-2872.2001
  40. Su HC, Ying GG, Tao R, Zhang RQ, Zhao JL, Liu YS. 2012. Class 1 and 2 integrons, sul resistance genes and antibiotic resistance in Escherichia coli isolated from Dongjiang River, South China. Environ Pollut 169: 42-49. https://doi.org/10.1016/j.envpol.2012.05.007
  41. Takasu H, Suzuki S, Reungsang A, Pham HV. 2011. Fluoroquinolone (FQ) contamination does not correlate with occurrence of FQ-resistant bacteria in aquatic environments of Vietnam and Thailand. Microbes Environ 26: 135-143. https://doi.org/10.1264/jsme2.ME10204
  42. Yu HS, Lee JC, Kang HY, Ro DW, Chung JY, Jeong YS, Tae SH, Choi CH, Lee EY, Seol SY, Lee YC, Cho DT. 2003. Changes in gene cassettes of class 1 integrons among Escherichia coli isolates from urine specimens collected in Korea during the last two decades. J Clin Microbiol 41: 5429-5433. https://doi.org/10.1128/JCM.41.12.5429-5433.2003
  43. Weldhagen GF, Poirel L, Nordmann P. 2003. Ambler class A extended- spectrum beta-lactamases in Pseudomonas aeruginosa: novel developments and clinical impact. Antimicrob Agents Chemother 47: 2385-2392. https://doi.org/10.1128/AAC.47.8.2385-2392.2003