Northeastern U.S. Salmonella Strains from Retail Meat Are More Prevalent and More Resistant to Antimicrobials.

ABSTRACT: Between 2002 and 2017, the National Antimicrobial Resistance Monitoring System (NARMS) recovered 5,803 Salmonella isolates from retail meat samples of chicken parts, ground turkey, pork chops, and ground beef collected in 21 states. NARMS tested these isolates for susceptibility to amoxicillin-clavulanic acid, ampicillin, azithromycin, cefoxitin, ceftiofur, ceftriaxone, chloramphenicol, gentamicin, nalidixic acid, streptomycin, tetracycline, trimethoprim-sulfamethoxazole (cotrimoxazole), sulfisoxazole, and ciprofloxacin. To evaluate possible geographic differences in the prevalence and distribution of antimicrobial-resistant Salmonella, we used a chi-square test of association. We used the U.S. Department of Agriculture Office of Investigation, Enforcement and Audit map for the regional subdivisions. A significant association was found between region, Salmonella prevalence, and Salmonella resistance to all tested antimicrobials except cotrimoxazole, streptomycin, ciprofloxacin, and azithromycin. The Northeast region was the most influential contributor to overall prevalence and resistance to most of the antimicrobials tested, and Salmonella Typhimurium was the serotype driving these associations. Although this work did not elucidate the reasons for differences in prevalence and antimicrobial resistance for Salmonella Typhimurium strains in the Northeast, lack of certain resistance mechanisms in Salmonella strains from other regions was ruled out by analysis of 484 sequences from the 485 isolates resistant to ampicillin, sulfonamides, and tetracycline.

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

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.

MRSA and multidrug-resistant Staphylococcus aureus in U.S. retail meats, 2010-2011.

Methicillin-resistant Staphylococcus aureus (MRSA) has been detected in retail meats, although large-scale studies are scarce. We conducted a one-year survey in 2010-2011 within the framework of the National Antimicrobial Resistance Monitoring System. Among 3520 retail meats collected from eight U.S. states, 982 (27.9%) contained S. aureus and 66 (1.9%) were positive for MRSA. Approximately 10.4% (107/1032) of S. aureus isolates, including 37.2% (29/78) of MRSA, were multidrug-resistant (MDRSA). Turkey had the highest MRSA prevalence (3.5%), followed by pork (1.9%), beef (1.7%), and chicken (0.3%). Whole-genome sequencing was performed for all 66 non-redundant MRSA. Among five multilocus sequence types identified, ST8 (72.7%) and ST5 (22.7%) were most common and livestock-associated MRSA ST398 was assigned to one pork isolate. Eleven spa types were represented, predominately t008 (43.9%) and t2031 (22.7%). All four types of meats harbored t008, whereas t2031 was recovered from turkey only. The majority of MRSA (84.8%) possessed SCCmec IV and 62.1% harbored Panton-Valentine leukocidin. Pulsed-field gel electrophoresis showed that all ST8 MRSA belonged to the predominant human epidemic clone USA300, and others included USA100 and USA200. We conclude that a diverse MRSA population was present in U.S. retail meats, albeit at low prevalence.

Molecular Subtyping and Source Attribution of Campylobacter Isolated from Food Animals.

Campylobacter spp. commonly cause gastrointestinal illness in humans. Poultry meats have long been considered the predominant source of these infections, but few in-depth Campylobacter source attribution studies have been completed. We analyzed more than 1,300 Campylobacter isolates recovered from a number of animal and food sources, including dairy and beef cattle, pigs, poultry, and retail poultry meat, and compared them with Campylobacter isolates recovered from human clinical samples. Each isolate was subtyped using pulsed-field gel electrophoresis (PFGE) with SmaI and queried against the Centers for Disease Control and Prevention PulseNet database to identify human isolates with indistinguishable patterns. Half (49.5%) of the PFGE patterns from poultry animal and retail meat isolates were indistinguishable from patterns of at least one human isolate. Among the isolates from beef and dairy cows, 56.6 and 65.0%, respectively, of their PFGE patterns were indistinguishable from those of human isolates. Only a small portion of the PFGE patterns of Campylobacter isolated from pigs (9.5%) were found to have PFGE patterns in common with human isolates. These data imply that cattle may be larger contributors to Campylobacter infections than previously recognized and help further our understanding of potential sources of human campylobacteriosis.

Temporal patterns of Campylobacter contamination on chicken and their relationship to campylobacteriosis cases in the United States.

The proportion of Campylobacter contaminated food and water samples collected by different surveillance systems often exhibit seasonal patterns. In addition, the incidence of foodborne campylobacteriosis also tends to exhibit strong seasonal patterns. Of the various product classes, the occurrence of Campylobacter contamination can be high on raw poultry products, and chicken is often thought to be one of the leading food vehicles for campylobacteriosis. Two different federal agencies in the United States collected samples of raw chicken products and tested them for the presence of Campylobacter. During the same time period, a consortium of federal and state agencies operated a nationwide surveillance system to monitor cases of campylobacteriosis in the United States. This study uses a common modeling approach to estimate trends and seasonal patterns in both the proportion of raw chicken product samples that test positive for Campylobacter and cases of campylobacteriosis. The results generally support the hypothesis of a weak seasonal increase in the proportion of Campylobacter positive chicken samples in the summer months, though the number of Campylobacter on test-positive samples is slightly lower during this time period. In contrast, campylobacteriosis cases exhibit a strong seasonal pattern that generally precedes increases in contaminated raw chicken. These results suggest that while contaminated chicken products may be responsible for a substantial number of campylobacteriosis cases, they are most likely not the primary driver of the seasonal pattern in human illness.