The U.S. Food and Drug Administration has released a new interim report that measures antimicrobial resistance in Salmonella isolated from raw retail meat and poultry collected through the National Antimicrobial Resistance Monitoring System (NARMS).
The 2014-2015 Retail Meat Interim Report contains data from January 2014 – June 2015. It focuses only on Salmonella, a major pathogen of concern in foodborne disease outbreaks. Information includes serotype distribution, prevalence by food source and state, selected resistance patterns, and a list of all the identified antimicrobial resistance genes. To provide data in a timelier manner, the FDA intends to issue retail meat interim reports twice per year. In this report FDA also includes, for the first time, whole-genome sequencing data for Salmonella as a new component of routine NARMS surveillance practices and has placed all the isolate-level data on its website.
NARMS was established in 1996 as a partnership between the FDA, the Centers for Disease Control and Prevention, and the U.S. Department of Agriculture to track antibiotic resistance in foodborne bacteria for drugs that are considered important in human medicine, including whether they are multidrug resistant (resistant to three or more classes of antibiotics). NARMS is critically important for monitoring trends in antimicrobial resistance among foodborne bacteria collected from humans, retail meats and food animals. In particular, it assists the FDA in making data-driven decisions on the approval of safe and effective antimicrobial drugs for animals.
The retail meat arm of the NARMS program collects samples of grocery store chicken, ground turkey, ground beef and pork chops, and tests for non-typhoidal Salmonella, Campylobacter, Escherichia coli and Enterococcus, to determine whether such bacteria are resistant to various antibiotics used in human and veterinary medicine. Enterococcus and most E. coli are not considered major foodborne pathogens but are included because they are helpful in understanding how resistance occurs and spreads.
Consumers can help protect themselves from foodborne bacteria, including antibiotic-resistant bacteria, by following four basic food safety tips: clean, separate, cook, chill. Learn more at http://www.foodsafety.gov/keep/basics/.
2014-2015 Retail Meat Interim Report
In many important categories, encouraging improvements found in 2011 continued to be evident in the latest data.
The prevalence of Salmonella in retail poultry is at its lowest level since testing began in 2002. In ground turkey, the prevalence of Salmonella has declined from a high of 19% in 2008 to 6% in 2014. In retail chicken over the same time period, it has dropped from 15% to 9%.
Salmonella resistance to ceftriaxone (an important antibiotic used to treat seriously ill patients) from chicken sources continued to decline steadily from a high of 38% in retail chicken meats in 2009 to 18% in 2014, and 5% during the first half of 2015. In ground turkey isolates, ceftriaxone resistance was detected in 7% of 2014 isolates and 4% of 2015 isolates collected through June, which represents an 80% decline since 2011 when resistance peaked at 22%.
Fluoroquinolones like ciprofloxacin are classified as critically important for the treatment of Salmonella infections. Ciprofloxacin resistance was absent in Salmonella from poultry and beef, although a single isolate was found in pork.
All Salmonella from retail meats were susceptible to azithromycin, another important antibiotic recommended for the treatment of Salmonella and other intestinal pathogens.
Multidrug resistance in Salmonella continued to show a downward drift in chicken and turkey from 2011 levels of 45% and 50%, respectively, to 20% and 36% in June 2015.
Findings of Concern
FDA identified the first instance of ciprofloxacin resistance in an isolate from retail pork, and identified the genes associated with this resistance for future tracking (see below).
One ceftriaxone-resistant retail chicken isolate from 2014 had the extended-spectrum β-lactamase (ESBL) gene blaCTX-M-65. This is the first time this important class of resistance gene was detected in the U.S. This ESBL gene causes resistance to β-lactam antibiotics, including third generation cephalosporins, resulting in fewer treatment options for infected patients.
While only three isolates of Salmonella serotype Dublin were recovered from meats (ground beef) in 2014, they exhibited extensive resistance patterns as in the past, showing resistance to 9-12 of 14 drugs tested.
Whole Genome Sequencing
Whole genome sequencing (WGS) has ushered in a new age in infectious disease science, with the power to greatly enhance diagnosis, tracking and treatment. Because WGS has become an inexpensive and rapid tool for characterizing bacteria, it has the potential to replace a number of long-standing laboratory methods such as biochemical tests to identify species, and the subtyping methods of serotyping and pulsed-field gel electrophoresis, each of which requires specialized training and separate lab processes. Whole genome sequence data are published for all 271 retail meat isolates from 2014 and 114 Salmonella isolated in the first half of 2015. All of the WGS data for NARMS isolates are now publicly available in GenBank bioproject PRJNA290865.
WGS data can be used to predict antimicrobial resistance for a number of bacteria, including the foodborne pathogens Salmonella, Campylobacter, and E. coli. In addition, WGS data reveal the range of genes causing resistance to a particular antibiotic. FDA has included comprehensive genetic data for the first time in a NARMS report, listing the antimicrobial resistance genes and resistance-associated mutations for Salmonella. Some notable findings from WGS in this report include:
WGS helped identify antibiotic resistant genes in the form of diverse quinolone resistance mechanisms. In addition to two isolates with well-known DNA gyrase mutations associated with quinolone resistance, two isolates possessed the plasmid-mediated qnr genes, one with qnrS and one with qnrB. This analysis revealed that the single ciprofloxacin-resistant isolate from pork carried the qnrS gene. The presence of such plasmid-associated resistance genes is of particular concern due to the potential for transmissibility to other strains of Salmonella. This appears to be the first report of qnr genes present in retail meat Salmonella isolated in the United States. Despite these findings, Salmonella largely remained susceptible to ciprofloxacin and other first line human clinical therapies, including azithromycin, during 2014 and the first half of 2015.
As noted above, 2014 was the first year FDA found a blaCTX-M-65 ESBL in Salmonella from a retail meat sample in the United States. This was identified by WGS and was seen in a single isolate. Studies are ongoing to see if this finding points to a broader distribution of this important trait in Salmonella from other sources.
The WGS data has allowed FDA, for the first time, to understand the mechanisms underlying each of the resistance phenotypes observed, and how they differ by source. For instance, the predominant β-lactamases in ground turkey and pork chop isolates were blaTEM enzymes, whereas in retail chicken and ground beef isolates, blaCMY were more prevalent.blaCMY genes are generally associated with more extended activity, and confer resistance to third-generation cephalosporins, important drugs in the treatment of Salmonella infections. The tetA gene predominated among tetracycline resistant isolates from retail chicken, ground turkey, and ground beef isolates, while in pork chop isolates tetB was most common. Additional genetic information over multiple years will be necessary to determine whether these differences are stable over time and may be used to help determine the source of resistant infections in isolates recovered from humans.
All the isolate-level data, including links to the WGS data, can be found at