Prevalence and Antimicrobial Resistance of Enterococci Isolated from Retail Meats in the United States, 2002 to 2014

Abstract

Bacteria of the genus Enterococcus are important human pathogens that are frequently resistant to a number of clinically important antibiotics. They are also used as markers of animal fecal contamination of human foods and are employed as sentinel organisms for tracking trends in resistance to antimicrobials with Gram-positive activity. As part of the National Antimicrobial Resistance Monitoring System (NARMS), we evaluated several retail meat commodities for the presence of enterococci from 2002 to 2014, and we found 92.0% to be contaminated. The majority of isolates were either Enterococcus faecalis (64.0%) or Enterococcus faecium (28.6%), and the antimicrobial resistance of each isolate was assessed by broth microdilution. The resistance prevalences for several drugs, including erythromycin and gentamicin, were significantly higher among poultry isolates, compared to retail beef or pork isolates. None of the isolates was resistant to the clinically important human drug vancomycin, only 1 isolate was resistant to linezolid, and resistance to tigecycline was below 1%. In contrast, a majority of both E. faecalis (67.5%) and E. faecium (53.7%) isolates were resistant to tetracycline. Overall, the robust NARMS testing system employed consistent sampling practices and methods throughout the testing period, with the only significant trend in resistance prevalence being decreased E. faecium resistance to penicillin. These data provide excellent baseline levels of resistance that can be used to measure future changes in resistance prevalence that may result from alterations in the use of antimicrobials in food animal production.IMPORTANCE Enterococci, including E. faecalis and E. faecium, are present in the guts of food-producing animals and are used as a measure of fecal contamination of meat. We used the large consistent sampling methods of NARMS to assess the prevalence of Enterococcus strains isolated from retail meats, and we found over 90% of meats to be contaminated with enterococci. We also assessed the resistance of the Enterococcus strains, commonly used as a measure of resistance to agents with Gram-positive activity, in foods. Resistance prevalence was over 25% for some antimicrobials and sample sources but was less than 1% for several of the most important therapeutic agents used in human medicine.

Keywords: Enterococcus; antimicrobial resistance; retail meats.

FIG 1

Prevalence of Enterococcus from various sources. (A) Frequency of isolation of any Enterococcus strain from different retail meat commodities. (B) Prevalence of E. faecalis and E. faecium among all enterococci for each of the retail meat commodities.

FIG 2

Comparison of resistance prevalences for E. faecalis and E. faecium for 11 antimicrobials. Drugs tested but not depicted (vancomycin, tigecycline, chloramphenicol, and linezolid) had resistance prevalence of less than 1% for both bacterial species. Quinupristin-dalfopristin resistance is not reported for E. faecalis due to the intrinsic resistance of E. faecalis. Error bars depict 95% confidence intervals for resistance prevalence. Differences in resistance prevalence between E. faecalis and E. faecium had chi-square P values of <0.0001 for all drugs depicted except streptomycin (P = 0.3026) and erythromycin (P = 0.005). GEN, gentamicin; KAN, kanamycin; STR, streptomycin; DAP, daptomycin; ERY, erythromycin; TYL, tylosin; NIT, nitrofurantoin; PEN, penicillin; CIP, ciprofloxacin; QDA, quinupristin-dalfopristin; TET, tetracycline.

FIG 3

Trends in antimicrobial resistance over time. Prevalences of resistance to selected antimicrobials over the years are depicted for E. faecalis (A) and E. faecium (B). GEN, gentamicin; KAN, kanamycin; STR, streptomycin; ERY, erythromycin; TET, tetracycline; PEN, penicillin.