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Volume 18, Number 5—May 2012

Antimicrobial Drug Resistance in Escherichia coli from Humans and Food Animals, United States, 1950–2002

Daniel A. Tadesse, Shaohua Zhao, Emily Tong, Sherry Ayers, Aparna Singh, Mary J. Bartholomew, and Patrick F. McDermottComments to Author 
Author affiliations: Food and Drug Administration, Laurel, Maryland, USA (D.A. Tadesse, S. Zhao, E. Tong, S. Ayers, A. Singh, P.F. McDermott); Food and Drug Administration, Rockville, Maryland, USA (M.J. Bartholomew)

Main Article

Table 2

Antimicrobial drug resistance phenotypes of Escherichia coli isolates from different sources, United States, 1950–2002*

Drug class Drug Resistance breakpoint, µg/mL % Resistance
Timeline for clinical use of drugs (reference)
Overall, n = 1,729 Human, n = 983 Cattle, n = 323 Chickens, n = 138 Pigs, n = 285
Penicillins AMP >32 24.1 16.5 35 34.1 33.3 1961 (17)
β-lactam/β-lactamase inhibitor combinations AUG >32 5.6 2.4 12.7 7.3 7.4 1984 (17)
Cephems CEP >32 12.9 8.8 20.1 12.3 19.3 1964 (18)
FOX >32 4.4 1.5 9.3 5.1 8.4 1977 (19)
TIO >8 2.3 0.1 7.4 1.5 4.2 1988 (FDA Green Book)†
AXO >4 2.4 0.1 7.7 1.5 4.6 1984 (FDA Orange Book)‡
Phenicols CHL >32 8.1 3.7 18 8.7 11.9 1947 (17)
Aminoglycosides GEN >16 6.7 0.1 16.1 16.7 14 1963 (17)
KAN >64 19.3 5.7 39.9 29.7 37.5 1957 (17)
STR§ >64 34.2 15.3 61.3 58 57.2 1943 (17)
Quinolones CIP >4 0.4 0 1.9 0.7 0 1987 (17)
NAL >32 1.7 1 3.7 1.5 1.8 1962 (19)
Tetracyclines TET >16 40.9 18 71.2 68.8 72.3 1948 (17)
Folate pathway inhibitors SUL >512 36.2 19.9 61 60.9 52.6 1936 (19)
TMP/SMX >4 7 2.2 16.1 13.8 9.8 1968 (19)

*AMP, ampicillin; AUG, amoxicillin/clavulanic acid; CEP, cephalothin; FOX, cefoxitin; TIO, ceftiofur; FDA, Food and Drug Administration; AXO, ceftriaxone; CHL, chloramphenicol; GEN, gentamicin; KAN, kanamycin; STR, streptomycin; CIP, ciprofloxacin; NAL, nalidixic acid; TET, tetracycline; SUL, sulfonamide; TMP/SMX, trimethoprim/sulfamethoxazole.
§No Clinical and Laboratory Standards Institute breakpoint. The National Antimicrobials Resistance Monitoring System breakpoint was used.

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  1. Aarestrup  FM, Wegener  HC, Collignon  P. Resistance in bacteria of the food chain: epidemiology and control strategies. Expert Rev Anti Infect Ther. 2008;6:73350. DOIPubMedGoogle Scholar
  2. Walsh  CT. Antibiotics: actions, origins, resistance. Washington (DC): American Society for Microbiology Press; 2003.
  3. Levy  SB, Marshall  B. Antibacterial resistance worldwide: causes, challenges and responses. Nat Med. 2004;10(Suppl):S1229. DOIPubMedGoogle Scholar
  4. von Baum  H, Marre  R. Antimicrobial resistance of Escherichia coli and therapeutic implications. Int J Med Microbiol. 2005;295:50311. DOIPubMedGoogle Scholar
  5. Sodha  SV, Lynch  M, Wannemuehler  K, Leeper  M, Malavet  M, Schaffzin  J, Multistate outbreak of Escherichia coli O157:H7 infections associated with a national fast-food chain, 2006: a study incorporating epidemiological and food source traceback results. Epidemiol Infect. 2011;139:30916. DOIPubMedGoogle Scholar
  6. Taur  Y, Smith  MA. Adherence to the Infectious Diseases Society of America guidelines in the treatment of uncomplicated urinary tract infection. Clin Infect Dis. 2007;44:76974. DOIPubMedGoogle Scholar
  7. Igarashi  T, Inatomi  J, Wake  A, Takamizawa  M, Katayama  H, Iwata  T. Failure of prediarrheal antibiotics to prevent hemolytic uremic syndrome in serologically proven Escherichia coli O157:H7 gastrointestinal infection. J Pediatr. 1999;135:7689. DOIPubMedGoogle Scholar
  8. Erb  A, Stürmer  T, Marre  R, Brenner  H. Prevalence of antibiotic resistance in Escherichia coli: overview of geographical, temporal, and methodological variations. Eur J Clin Microbiol Infect Dis. 2007;26:8390. DOIPubMedGoogle Scholar
  9. Womack  NA, Kabera  CM, Tong  EA, Jones  S, Gaines  S, Bartholomew  M, ; The NARMS Working Group. The use of Escherichia coli as a sentinel for antimicrobial resistance in Salmonella. In: Abstracts of the National Foundation for Infectious Diseases Annual Conference on Antimicrobial Resistance, Bethesda, Maryland, February 1–3, 2010. Bethesda (MD): The Foundation; 2010. Abstract no. P12.
  10. US Food and Drug Administration. National antimicrobial resistance monitoring system –enteric bacteria (NARMS): 2008 executive report. Rockville (MD); 2010 [cited 2012 Feb 13].
  11. Atkinson  BA, Lorian  V. Antimicrobial agent susceptibility patterns of bacteria in hospitals from 1971 to 1982. J Clin Microbiol. 1984;20:7916.PubMedGoogle Scholar
  12. Blaettler  L, Mertz  D, Frei  R, Elzi  L, Widmer  AF, Battegay  M, Secular trend and risk factors for antimicrobial resistance in Escherichia coli isolates in Switzerland 1997–2007. Infection. 2009;37:5349. DOIPubMedGoogle Scholar
  13. Kronvall  G. Antimicrobial resistance 1979–2009 at Karolinska Hospital, Sweden: normalized resistance interpretation during a 30-year follow-up on Staphylococcus aureus and Escherichia coli resistance development. APMIS. 2010;118:62139. DOIPubMedGoogle Scholar
  14. McEwen  SA, Fedorka-Cray  P. Antimicrobial use and resistance in animals. Clin Infect Dis. 2002;34(Suppl 3):S93106. DOIPubMedGoogle Scholar
  15. Jensen  VF, Jakobsen  L, Emborg  H, Seyfarth  AM, Hammerum  AM. Correlation between apramycin and gentamicin use in pigs and an increase reservoir of gentamicin-resistant Escherichia coli. J Antimicrob Chemother. 2006;58:1017. DOIPubMedGoogle Scholar
  16. National Committee for Clinical Laboratory Standards. Performance standards for antimicrobial susceptibility testing; 12th informational supplement. M100–S20. Wayne (PA): The Committee; 2010.
  17. Guilfoile  P. 2006. Antibiotic resistant bacteria. Northborough (MA): Chelsea House Publishers; 2006.
  18. Kunin  CM, Atuk  N. Excretion of cephaloridine and cephalothin in patients with renal impairment. N Engl J Med. 1966;274:6546. DOIPubMedGoogle Scholar
  19. Bryskier  A. Historical review of antibacterial chemotherapy. In: Bryskier A, editor. Antimicrobial agents: antibacterials and antifungals. Washington (DC): American Society for Microbiology Press; 2005. p. 1–11.
  20. Sen  PK. Estimates of the regression coefficient based on Kendall’s tau. J Am Stat Assoc. 1968;63:137989. DOIGoogle Scholar
  21. Salmi  T, Määttä  A, Anttila  P, Ruoho-Airola  T, Amnell  T. Detecting trends of annual values of atmospheric pollutants by the Mann–Kendall test and Sen’s slope estimates: the Excel template application Helsinki: MAKESENS. Helsinki: Finnish Meteorological Institute; 2002.
  22. Enne  VI, Livermore  DM, Stephens  P, Hall  LM. Persistence of sulphonamide resistance in Escherichia coli in the UK despite national prescribing restriction. Lancet. 2001;357:13258. DOIPubMedGoogle Scholar
  23. Kozak  GK, Pearl  DL, Parkman  J, Reid-Smith  RJ, Deckert  A, Boerlin  P. Distribution of sulfonamide resistance genes in Escherichia coli and Salmonella isolates from swine and chickens at abattoirs in Ontario and Québec, Canada. Appl Environ Microbiol. 2009;75:59996001. DOIPubMedGoogle Scholar
  24. Zhao  S, White  DG, McDermott  PF, Friedman  S, English  L, Ayers  S, Identification and expression of cephamycinase bla (CMY) genes in Escherichia coli and Salmonella isolates from food animals and ground meat. Antimicrob Agents Chemother. 2001;45:364750. DOIPubMedGoogle Scholar
  25. Bean  DC, Livermore  DM, Papa  I, Hall  LM. Resistance among Escherichia coli to sulphonamides and other antimicrobials now little used in man. J Antimicrob Chemother. 2005;56:9624. DOIPubMedGoogle Scholar
  26. Bean  DC, Livermore  DM, Hall  LM. Plasmids imparting sulfonamide resistance in Escherichia coli: implications for persistence. Antimicrob Agents Chemother. 2009;53:108893. DOIPubMedGoogle Scholar
  27. Wu  S, Dalsgaard  A, Hammerum  AM, Porsbo  LJ, Jensen  LB. Prevalence and characterization of plasmids carrying sulfonamide resistance genes among Escherichia coli from pigs, pig carcasses and human. Acta Vet Scand. 2010;52:47. DOIPubMedGoogle Scholar
  28. Enne  VI, Bennett  PM, Livermore  DM, Hall  LM. Enhancement of host fitness by the sul2-coding plasmid p9123 in the absence of selective pressure. J Antimicrob Chemother. 2004;53:95863. DOIPubMedGoogle Scholar
  29. Langlois  BE, Cromwell  GL, Stahly  TS, Dawson  KA, Hays  VW. Antibiotic resistance of fecal coliforms after long-term withdrawal of therapeutic and subtherapeutic antibiotic use in a swine herd. Appl Environ Microbiol. 1983;46:14334.PubMedGoogle Scholar
  30. Roberts  MC. Update on acquired tetracycline resistance genes. FEMS Microbiol Lett. 2005;245:195203. DOIPubMedGoogle Scholar
  31. Schroeder  CM, Zhao  C, DebRoy  C, Torcolini  J, Zhao  S, White  DG, Antimicrobial resistance of Escherichia coli O157 isolated from humans, cattle, swine, and food. Appl Environ Microbiol. 2002;68:57681. DOIPubMedGoogle Scholar
  32. Bischoff  KM, White  DG, Hume  ME, Poole  TL, Nisbet  DJ. The chloramphenicol resistance gene cmlA is disseminated on transferable plasmids that confer multiple-drug resistance in swine Escherichia coli. FEMS Microbiol Lett. 2005;243:28591. DOIPubMedGoogle Scholar
  33. White  DG, Hudson  C, Maurer  JJ, Ayers  S, Zhao  S, Lee  MD, Characterization of chloramphenicol and florfenicol resistance in Escherichia coli associated with bovine diarrhea. J Clin Microbiol. 2000;38:45938.PubMedGoogle Scholar
  34. Schwarz  S, Kehrenberg  C, Doublet  B, Cloeckaert  A. Molecular basis of bacterial resistance to chloramphenicol and florfenicol. FEMS Microbiol Rev. 2004;28:51942. DOIPubMedGoogle Scholar
  35. Cannon  M, Harford  S, Davies  J. A comparative study on the inhibitory actions of chloramphenicol, thiamphenicol and some fluorinated derivatives. J Antimicrob Chemother. 1990;26:30717. DOIPubMedGoogle Scholar
  36. Harada  K, Asai  T, Kojima  A, Ishihara  K, Takahashi  T. Role of coresistance in the development of resistance to chloramphenicol in Escherichia coli isolated from sick cattle and pigs. Am J Vet Res. 2006;67:2305. DOIPubMedGoogle Scholar
  37. US Food and Drug Administration. 2009 summary report on antimicrobials sold or distributed for use in food-producing animals. December 9, 2010. Rockville, MD [cited 2011Feb 23].
  38. Yates  CM, Pearce  MC, Woolhouse  ME, Amyes  SG. High frequency transfer and horizontal spread of apramycin resistance in calf faecal Escherichia coli. J Antimicrob Chemother. 2004;54:5347. DOIPubMedGoogle Scholar
  39. Burton  PJ, Thornsberry  C, Cheung  YY, Watts  JL, Yancey  RJ. Interpretive criteria for antimicrobial susceptibility testing of ceftiofur against bacteria associated with swine respiratory disease. J Vet Diagn Invest. 1996;8:4648. DOIPubMedGoogle Scholar
  40. 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;45:271622. DOIPubMedGoogle Scholar

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