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  1. The National Antimicrobial Resistance Monitoring System

2016-2017 NARMS Integrated Summary

NARMS Update

About NARMS

The National Antimicrobial Resistance Monitoring System (NARMS) is a national public health surveillance system that monitors foodborne bacteria to determine if they are resistant to various antibiotics used in human and veterinary medicine. NARMS is composed of the FDA, CDC, and USDA as partner agencies.

The NARMS program helps promote and protect public health by providing information about emerging bacterial resistance, how resistant infections differ from susceptible infections, and the impact of interventions designed to limit the spread of resistance. NARMS data are used by FDA to make regulatory decisions designed to preserve the effectiveness of antibiotics for humans and animals.

What’s changed?

The reports

Historically, NARMS has published Integrated Reports annually (or biannually) to highlight antimicrobial resistance patterns in bacteria isolated from humans (by CDC), raw retail meats including chicken, ground turkey, ground beef, and pork chops (by FDA), and animals at slaughter including chickens, turkeys, cattle, and swine (by USDA). Starting this year with the release of 2016-2017 data, NARMS is publishing a NARMS Integrated Summary, instead of the long-form Integrated Report. The Integrated Summary is a bulleted list of the most important takeaways for the reporting year. Online interactive data displays are still be available on FDA’s website.

This 2016-2017 Integrated Summary is the first time NARMS has included data on animal pathogens from a pilot study with FDA's Veterinary Laboratory Response and Investigation Network (Vet-LIRN). In addition, this summary is the first time that NARMS will provide genomic information for Campylobacter and E. coli retail meat and food animal isolates. Up to this point, this information was only available for Salmonella.

Antimicrobials on susceptibility testing panel

In 2016, a carbapenem, meropenem was added onto the gram-negative panel used in antimicrobial susceptibility testing of Salmonella and E. coli isolated from NARMS sources. The meropenem breakpoint set by the Clinical and Laboratory Standards Institute (CLSI) is >=4 µg/ml. In addition, ceftiofur was removed from the gram-negative panel and the drug range for azithromycin was shifted to 0.5-32 µg/ml.

Acknowledgements

NARMS is possible only because of the dedicated effort of many people across Federal, State, and academic institutions. A complete list of NARMS partners can be found in the supplemental material.

The NARMS Steering Committee consists of the following people:

U.S. Food and Drug Administration
Patrick McDermott
Heather Tate
Olgica Ceric

U.S. Centers for Disease Control and Prevention
Cindy Friedman
Jean Whichard

U.S. Department of Agriculture - Food Safety Inspection Service
Uday Dessai
Gamola Fortenberry
Sheryl Shaw

U.S. Department of Agriculture - Agricultural Research Service
Kim Cook
Roxann Motroni

Background

NARMS generates a large dataset on bacteria from 14 distinct sources (see Table 1 below). This summary focuses on antimicrobial resistance to drug classes that are most important to human medicine (generally, first- or second-line treatments), multidrug resistance, and specific co-resistance profiles of epidemiological importance.

Salmonella and Campylobacter are the leading bacterial causes of foodborne illness in the United States. Nontyphoidal serotypes of Salmonella enterica can be present in intestinal tracts of a wide range of animals including wildlife, livestock, and domestic pets. The bacterium spreads through the fecal-oral route, mainly by contact with contaminated foods of animal origin, or less frequently by contact with animals or animal contaminated produce. Similarly, Campylobacter is commonly present in the gut flora of food-producing animals such as chickens, turkeys, swine, cattle, and sheep. 

Public health significance: Salmonella is estimated to cause over 1.2 million illnesses and 120 deaths, and Campylobacter is estimated to cause over 1.3 million illnesses and 120 deaths each year (Scallan et al., 2011).

Generic Escherichia coli and Enterococcus isolates also are tested for antimicrobial susceptibility. These are cultured from animal samples at slaughter and from retail meats. Testing these organisms indicates resistance to antimicrobials that are active against gram-negative and gram-positive bacteria. For more information about these four bacterial organisms, visit the NARMS webpage. 

This summary presents consolidated information from the four data types that form the NARMS system:

  1. Human clinical isolates 
  2. Food-producing animal isolates from cecal (intestinal) samples at slaughter 
  3. Samples collected at slaughter as part of Pathogen Reduction/Hazard Analysis Critical Control Point (PR/HACCP) testing 
  4. Raw retail meats (chicken, ground turkey, ground beef, and pork chops) collected at retail outlets in 18 states. 

The samples were collected from the sources in Table 1 below.

Table 1: Data sources for 2016-2017 NARMS Integrated Summary

Human Chickens Turkeys Cattle Swine
Clinical illness Retail Chickens
PR/HACCP
Cecal
Retail Ground Turkey
PR/HACCP
Cecal
Retail Ground Beef
PR/HACCP
Cecal Beef
Cecal Dairy
Retail Pork Chops
Cecal Market Swine
Cecal Sows

2016-2017 Highlights

Salmonella

Ceftriaxone

  • Ceftriaxone resistance in nontyphoidal Salmonella (henceforth referred to as Salmonella) from humans remains low, with an increase from 2.8% in 2015 to 3.4% in 2017. For most food and animal Salmonella isolates, ceftriaxone resistance declined or remained stable at around 11%. However, in isolates from chicken samples collected routinely at slaughter as part of Pathogen Reduction/Hazard Analysis Critical and Control Point (PR/HACCP) testing, ceftriaxone resistance increased from 6.5% in 2015 to 9.3% 2017, and in cecal isolates from turkeys it increased from 8% to 12% during the same time period. Infantis was the predominant ceftriaxone-resistant serotype among Salmonella from humans, all chicken sources, retail turkey meat and PR/HACCP turkey samples tested. 

Ciprofloxacin

  • The percentage of Salmonella isolates from humans and poultry sources with decreased susceptibility to ciprofloxacin (DSC; minimum inhibitory concentration ≥0.12 µg/mL) continued to increase.  Since 2013, DSC has more than doubled in isolates from humans, reaching over 8% in 2017.  DSC has increased from <1% to 9% in isolates from retail chicken meat, 14% in isolates from routinely sampled chickens, and 18% in isolates from chicken ceca. Among retail turkey meat and routine turkey samples, DSC has increased from <1% to ~6%. The rise in DSC among isolates from humans was largely due to Salmonella Enteritidis and may be related to international travel (1). The increase in DSC among poultry isolates was due to the increase in multidrug resistant (MDR) Infantis that exhibited DSC. Transmissible plasmid-mediated quinolone resistance (PMQR) genes continued to be identified among DSC isolates from humans, retail meats, and animal sources.

Azithromycin/Carbapenem

  • Although azithromycin resistance (MIC of ≥32 μg/mL) among Salmonella isolates from humans was rare, an increase was seen in 2017. During 2011–2016, only 26 Salmonella (0.2%) isolates were resistant to azithromycin. However, in 2017 alone, 26 (1.1%) azithromycin-resistant isolates were identified. Newport was the most common serotype, accounting for 35% (9/26) of azithromycin resistant isolates in 2017. Salmonella from food and animal samples collected between 2015 and 2017 did not have azithromycin resistance. 
  • Salmonella isolates from humans, retail meats, and animals did not show carbapenem resistance (meropenem testing became routine in 2016). 

MDR

  • Multidrug resistance (MDR) is defined as resistance to three or more antimicrobial classes. In humans, MDR Salmonella has remained at approximately 10% over the last 10 years. In 2017, the most common MDR serotype in humans was I 4,[5],12:i:-,  accounting for 25% of MDR Salmonella isolates. Approximately 80% of MDR I 4,[5],12:i- isolates had combined resistance to ampicillin, streptomycin, sulfisoxazole, and tetracycline (ASSuT).
  • During 2015–2017, there was a substantial increase in MDR Salmonella recovered from routinely sampled chickens (9.5% to 18%) and chicken cecal samples (15% to 25%). This increase was largely driven by the rise in MDR Salmonella Infantis isolates.  MDR continued to decline in Salmonella from turkey sources during the same time period. The majority of MDR isolates in turkey were serotypes Infantis, Reading, and I 4,[5],12:i:-.  

Campylobacter

  • During 2015–2017, the proportion of macrolide-resistant (azithromycin or erythromycin) C. jejuni isolates from humans and chickens remained at ≤3%. Macrolide resistance among C. coli isolates from humans declined from 13% to 7% during the same time period. Macrolide resistance among C. coli isolates from routine and cecal chicken samples declined in 2016 but increased in 2017. Among cecal samples, macrolide resistance was found most often in C. coli isolates from market swine. 
  • The proportion of ciprofloxacin-resistant C. jejuni isolates from humans increased from 25% in 2015 to approximately 28% in 2017. Among C. coli isolates from humans, ciprofloxacin resistance in 2017 was nearly 40%, similar to rates in 2015.  In 2017, there was no significant change in ciprofloxacin resistance among C. jejuni and C. coli isolated from chickens as compared to 2015. Among all animal sources of Campylobacter tested in 2017, beef cattle cecal samples yielded the highest levels of ciprofloxacin resistance (69% in C. coli).

MDR

  • During 2015–2017, MDR among C. coli isolated from cecal samples either decreased or remained stable for all commodities except beef cattle, where MDR increased from 7% to 15%, and dairy cattle, where MDR increased from 4% to 11%. Among C. jejuni from cecal samples, MDR remained below 3% (in commodities with at least 10 C. jejuni isolates tested) 

E. coli

  • During 2015–2017, ceftriaxone-resistant E. coli continued to decline or remained below 5% in all animal sources except retail pork chops and market swine cecal samples, where it increased to 4.4% (from 1.2%) and 6.3% (from 2.7%), respectively.
  • During 2015–2017, azithromycin resistance was not detected in E. coli from retail meat samples. Among cecal samples from all animal sources, E. coli isolates with azithromycin resistance has remained below 3%. 
  • Among cecal samples from all food animals, MDR E. coli either decreased or remained stable, except in market swine (which showed an increase from 24% in 2015 to 27% in 2017) and sows (which showed an increase from 13% in 2015 to 16% in 2017).

Enterococcus

  • Since testing began in 2013, Enterococcal species that predominate in beef cattle ceca had increased resistance to macrolides. From 2013 to 2017, resistance to tylosin increased from 6.3% to 18% and resistance to erythromycin increased from 2.1% to 13%. The top 3 Enterococcal species that account for the greatest proportion of resistance to macrolides were Enterococcus hirae, durans and gallinarum
  • Between 2013 and 2017 there was an increase in chloramphenicol resistance among E. faecalis from market swine ceca (from 15% to 23%) and retail pork (from 2.1% to 5.5%). Chloramphenicol resistance in sow ceca declined from 21% to 8.5% during the same time period.
  • Since cecal testing began in 2013, there has been a decrease in gentamicin-resistant E. faecalis among turkeys (from 39% to 23%), chickens (from 46% to 17%) and sows (from 17% to 1.4%). While there was a decrease in gentamicin-resistant E. faecalis from retail chicken meat (from 24% to 13%), no significant decrease was observed in isolates from ground turkey or pork chops.
  • During 2015–2017, MDR E. faecalis decreased or remained stable among cecal samples from all commodities except market swine and sows, where MDR increased from 55% to 60%. During the same time period, E. faecium isolates from beef cattle also showed an increase (9.3% to 14%) in MDR.

Colistin

  • Although isolates were not tested for susceptibility to colistin, the genomes of all Salmonella and selected E. coli isolates were examined for the presence of transmissible colistin resistance genes (mcr-1 through mcr-9).  The mcr-1 gene was found in nine Salmonella isolates and one pathogenic E. coli O157 isolate collected from humans during 2016–2017. All ten patients traveled internationally before their illnesses began. One isolate was identified through routine NARMS surveillance and the remaining nine isolates underwent whole genome sequencing at state health departments. During 2016–2017 there were no Salmonella nor E. coli isolates from food animals or retail meats that harbored mcr-1 through mcr-8 resistance genes.  However, a newly discovered colistin resistance gene, mcr-9.1 (2), was found in several isolates from humans and all retail meat and food animal sources.  Further work is underway to fully characterize the gene and its potential to confer clinical resistance.

References

  1. O’Donnell AT, et al. Quinolone-resistant Salmonella enterica serotype Enteritidis infections associated with international travel. Clin Infect Dis. 2014 Nov 1:59(9):e139-141.
  2. Carroll, LM et al. Identification of Novel Mobilized Colistin Resistance Gene mcr-9 in a Multidrug-Resistant, Colistin-Susceptible Salmonella enterica Serotype Typhimurium Isolate. MBio. 2019 May 7; 10(3).

Percent of Animal and Food Samples Positive for Bacteria

These interactive data displays must be accessed in a web browser at NARMS Now: Integrated Data.

2017 Animal Pathogen AMR data

Background

Vet-LIRN: In late 2010, FDA initiated a program, the Veterinary Laboratory Investigation and Response Network (Vet-LIRN), to collaborate with veterinary diagnostic laboratories to build laboratory capacity for routine and emergency response. The overall goal for FDA is for the 40 participating laboratories to be ready, willing, and able to help investigate potential problems with animal feed and animal drugs by providing a rapid response to reports of animal injury.  Recent activities include developing and validating new laboratory testing methods, investigating possible contamination events such as excess Vitamin D in animal feed, and exploring the potential relationship between Dilated Cardiomyopathy and certain grain free or high legume content pet foods. 

Vet-LIRN laboratories are also participating in the national initiative to Combat Antibiotic Resistant Bacteria (CARB) by collecting veterinary pathogens for antimicrobial susceptibility testing and sequencing. This program has provided a wealth of information to FDA, with the ultimate goal of detecting emerging issues and of fostering antimicrobial stewardship in veterinary settings. 

The Network provides FDA with critical laboratory testing data from experts around the country, evaluating animal diagnostic samples, not the typical food matrices. Cooperative agreements fund the network and enable these laboratories to serve as first responders in case investigations and emergency response activities when the ability to quickly track down and isolate a dangerous pathogen or chemical adulterant is critical.  

More information about Vet-LIRN.

About the data

Isolates were collected by a network of 20 Vet-LIRN veterinary diagnostic laboratories (“Source laboratories”). Source laboratories collected the first four isolates each month, from each of the three selected pathogens, Escherichia coli and Staphylococcus pseudintermedius in dogs and Salmonella enterica from any host. 

Source laboratories serotyped all Salmonella isolates either in-house or by referral to the USDA National Veterinary Services Laboratory. Laboratories were instructed to select only one isolate per client submission. Isolate species were determined by either analytical profile index (API), matrix assisted laser desorption/ionization time of flight (MALDI-TOF) mass spectrometry, polymerase chain reaction (PCR), Sensititre, Vitek, or biochemical identification.

To view Vet-LIRN’s companion animal data visit: 2017 Animal Pathogen AMR Data.

NARMS Integrated Data Displays

Supplemental Materials

Suggested Citation

The National Antimicrobial Resistance Monitoring System: NARMS Integrated Report, 2016-2017. Laurel, MD: U.S. Department of Health and Human Services, FDA, 2019.