Changes in patterns of antimicrobial susceptibility and class 1 integron carriage among Escherichia coli isolates

Kang, Sang-Gyun;Lee, Deog-Yong;Shin, Sung-Jae;Ahn, Jeong-Min;Yoo, Han-Sang

  • Published : 20050900

Abstract

The worldwide use of antimicrobials in different fields has created enormous pressure for the selection of resistance among opportunistic bacterial pathogen. One hundred four E. coli isolates were collected and identified from swine with diarrhea in Korea during the period of 2002. The isolates showed highly resistant to streptomycin (99.0%), tetracycline (97.1%), neomycin (91.3%)and carbenicillin (84.6%)in antimicrobial susceptibility test. Moreover, all of the isolates showed multiple antimicrobial resistant to more than 3, and 85%of them were resistant to more than 7 of total 14 antimicrobial agents. In comparison with isolates in 1998, resistance to antimicrobialswas more frequent among the isolates in 2002. Presence of class 1 integrons was investigated through amplification of the gene with PCR, and could be classified 8 groups by pattern of 4 different amplicons. Class 1 integrons were observed in 67 strains (64.2%)of E. coli from swine in Korea. One and 1.6 kbp of amplicons were revealed to contain aadA1 and aadB-aadA1 gene cassettes respectively. Two kbp of amplicon had three different gene cassettes, dhfrXII-orfF-aadA2, and 3.0 kbp of amplicon includes aadB-cmlA1 gene cassettes.

Keywords

References

  1. Aarestrup FM, Seyfarth AM, Emborg H, Pedersen K, Hendriksen RS, Bager F. Effect of abolishment on the use of antimicrobial agents for growth promotion on occurrence of antimicrobial resistance in fecal enterococci from food animals in Denmark. Antimicrob Agents Chemother 2001, 45, 2054-2059 https://doi.org/10.1128/AAC.45.7.2054-2059.2001
  2. Adrian PV, Thomson CJ, Klugman KP, Amyes SGB. New gene cassettes for trimethoprim resistance, dfr13, and streptomycin-spectinomycin resistance, aadA4, inserted on a class 1 integron. Antimicrob Agents Chemother 2000, 44, 355-361 https://doi.org/10.1128/AAC.44.2.355-361.2000
  3. Altschul AF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990, 215, 403-410
  4. Amita S, Chowdhury R, Thungapathra M, Ramanurthy T, Nair GB, Ghosh A. Class 1 integrons and SXT elements in E1 tor strains isolated before and after 1992 Vibrio cholerae O139 outbreak, Calcutta, India. Emerg Infect Dis 2003, 9, 500-501 https://doi.org/10.3201/eid0904.020317
  5. Bischoff KM, White DG, McDermott PF, Zohao S, Gaines S, Maurer JJ, Nisbet DJ. Characterization of chloramphenicol resistance in $\beta$-hemolytic Escherichia coli associated with diarrhea in neonatal swine. J Clin Microbiol 2002, 40, 389-394 https://doi.org/10.1128/JCM.40.2.389-394.2002
  6. Chandler M, Claverys JP. Genome diversity: soureces and forces. Curr Opin Microbiol 2001, 4, 547-549 https://doi.org/10.1016/S1369-5274(00)00249-6
  7. Chung ME, Yeo SG. Distribution of antimicrobial resistances and properties of R-plasmids in E. coli isolated from pigs. Korean J Vet Res, 1994, 34, 759-768
  8. Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals; approved standard. 2nd ed. CLSI document M31-A2. CLSI, Wayne, 2002
  9. Deshpande L, Pfaller MA, Jones RN. In vitro activity of ceftiofur tested against clinical isolates of Escherichia coli and Klebsiella pneumoniae including extended spectrum $\beta$-lactamase producing strains. Int J Antimicrob Agents 2000, 15, 271-275 https://doi.org/10.1016/S0924-8579(00)00184-9
  10. Gilmore A. Chloramphenicol and the politics of health. Can Med Assoc J 1986, 134, 423-435
  11. Guerra B, Soto S, Cal S, Mendoza C. Antimicrobial resistance and spread of class 1 integrons among Salmonella serotypes. Antimicrob Agents Chemother 2000, 44, 2166-2169 https://doi.org/10.1128/AAC.44.8.2166-2169.2000
  12. Hall RM, Collis CM. Mobile gene cassettes and integrons: capture and spread of genes by site-specific recombination. Mol Microbiol 1995, 15, 593-600 https://doi.org/10.1111/j.1365-2958.1995.tb02368.x
  13. Ham HJ, Min KS, Chae CH. Antibiotics susceptibility and biochemical characterization of Escherichia coli associated with diarrhea from preweaning piglets. Korean J Vet Res 1997, 37, 773-777
  14. Hanau-Bercot B, Casin IPI, Collatz E. An intrinsic control element for translational initiation in class 1 integrons. Mol Microbiol 2002, 44, 119-130 https://doi.org/10.1046/j.1365-2958.2002.02843.x
  15. Heikkila E, Skurnik M, Sundstrom L, Huovinen P. A novel dihydrofolate reductase cassette inserted in an integron borne on a Tn21-like element. Antimicrob Agents Chemother 1993, 37, 1297-1304 https://doi.org/10.1128/AAC.37.6.1297
  16. Huovinen P, Sundstrom L, Swedberc G, Skold O. Trimethoprim and sulfonamide resistance. Antimicrob Agents Chemother 1995, 39, 279-289 https://doi.org/10.1128/AAC.39.2.279
  17. Jones CS, Osborne DJ, Stanley J. Enterobacterial tetracycline resistance in relation to plasmid incompatibility. Mol Cell Probes 1992, 6, 313-317 https://doi.org/10.1016/0890-8508(92)90007-K
  18. Kim BW, Rhee JC, Kim DS. The in vitro drug resistance of Escherichia coli Isolated from piglets, calves, lamb and goats with diarrhea. Korean J Vet Res 1979, 19, 121-126
  19. Kim JM, Jean NS, Kim JJ, Jean YH, Lee HS, Kweon CH, Woo SR, Lee HC, Park JM, Kim JH, Rhee JC. Antimicrobial drug susceptibility and treatment efficacy in mice against Escherichia coli and Salmonella spp isolated from feces of diarrheal animals. Korean J Vet Res 1997, 37, 389-403
  20. Kwon HJ, Kim TE, Cho SH, Seol JG, Kim BJ, Hyun JW, Park KY, Kim SJ, Yoo HS. Distribution and characterization of class 1 integrons in Salmonella enterica serotype Galinarum biotype Gallinarum. Vet Microbiol 2002, 89, 303-309 https://doi.org/10.1016/S0378-1135(02)00257-2
  21. Lanz R, Kuhnert P, Boerlin P. Antimicrobial resistance and resistance gene determinants in clinical Escherichia coli from different animal species in Switzerland. Vet Microbiol 2003, 91, 73-84 https://doi.org/10.1016/S0378-1135(02)00263-8
  22. Levesque C, Piché L, Larose C, Roy PH. PCR mapping of integrons several novel combinations of resistance genes. Antimicrob Agents Chemother 1995, 39, 185-195 https://doi.org/10.1128/AAC.39.1.185
  23. Mazel D, Davies J. Antibiotic resistance in microbes. Cell Mol Life Sci 1999, 56, 742-754 https://doi.org/10.1007/s000180050021
  24. McDermott PF, Barry AL, Jones RN, Stein GE, Thornsberry C, Wu CC, Walker RD. Standardization of broth microdilution and disk diffusion susceptibility tests for Actinobacillus pleuropneumoniae and Haemophilus somnus: quality control standards for ceftiofur, enrofloxacin, florfenicol, gentamicin, penicillin, tetracycline, tilmicosin, and trimethoprimsulfamethoxazole. J Clin Microbiol 2001, 39, 4283-4287 https://doi.org/10.1128/JCM.39.12.4283-4287.2001
  25. Nijsten R, London N, van den Bogaard A, Stobberingh E. Antibiotic resistance among Escherichia coli isolated from faecal samples of pig farmers and pigs. J Antimicrob Chemother 1996, 37, 1131-1140 https://doi.org/10.1093/jac/37.6.1131
  26. Park JY, Shin NR, Park YH, Yoo HS. Characteristics of Escherichia coli isolated from piglets with diarrhea; antimicrobial susceptibility, genotypes of enterotoxins and pili and plasmid profiles. Korean J Vet Res 2000, 40, 301-310
  27. Recchia GD, Hall RM. Gene cassette: a new class of mobile element. Microbiology 1995, 141, 3015-3027 https://doi.org/10.1099/13500872-141-12-3015
  28. Rosser SJ, Young HK. Identification and characterization of class 1 integrons in bacteria from an aquatic environment. J Antimicrob Chemother 1999, 44, 11-18
  29. Rowe-Magnus DA, Mazel D. Integron: natural tools for bacterial genome evolution. Curr Opin Microbiol 2001, 4, 565-569 https://doi.org/10.1016/S1369-5274(00)00252-6
  30. Salmon SA, Watts JL, Case CA, Hoffman LJ, Wegener HC, Yancey RJ. Comparison of MICs of ceftiofur and other antimicrobial agents against bacterial pathogens of swine from the United States, Canada, and Denmark. J Clin Microbiol 1995, 33, 2435-2444
  31. Sanchez S, Stevenson MAM, Hudson CR, Maier M, Buffington T, Dam Q, Maurer JJ. Characterization of multidrug-resistant Escherichia coli isolates associated with nosocomial infections in dogs. J Clin Microbiol 2002, 40, 3586-3595 https://doi.org/10.1128/JCM.40.10.3586-3595.2002
  32. Sandvang D. Novel streptomycin and spectinomycin resistance gene as a gene cassette within a class 1 integron isolated from Escherichia coli. Antimicrob Agents Chemother 1999, 43, 3036-3038
  33. Schmidt AS, Bruun MS, Dalsgaard I, Larsen JL. Incidence, distribution, and spread of tetracycline resistance determinants and integron-associated antibiotic resistance genes among motile Aeromonads from a fish farming environment. Appl Environ Microbiol 2001, 67, 5675-5682 https://doi.org/10.1128/AEM.67.12.5675-5682.2001
  34. Sengelov G, Halling-Sorensen B, Aarestrup FM. Susceptibility of Escherichia coli and Enterococcus faecium isolated from pigs and broiler chickens to tetracycline degradation products and distribution of tetracycline resistance determinants in E. coli from food animals. Vet Microbiol 2003, 95, 91-101 https://doi.org/10.1016/S0378-1135(03)00123-8
  35. Williams JB. Drug efflux as a mechanism of resistance. Br J Biomed Sci 1996, 53, 290-293
  36. Winokur PL, Vonstein DL, Hoffman LJ, Uhlenhopp EK, Doern GV. Evidence for transfer of CMY-2 AmpC $\beta$-lactamase plasmids between Escherichia coli and Salmonella isolates from food animals and humans. Antimicrob Agents Chemother 2001, 45, 2716-2722 https://doi.org/10.1128/AAC.45.10.2716-2722.2001
  37. Zhao S, White DG, McDermott PF, Friedman S, English L, Ayers S, Meng J, Maurer JJ, Holland R, Walker RD. Identification and expression of cephamycinase $bla_{CMY}$ genes in Escherichia coli and Salmonella isolates from food animals and ground meat. Antimicrob Agents Chemother 2001, 45, 3647-3650 https://doi.org/10.1128/AAC.45.12.3647-3650.2001