The National Antimicrobial Resistance Monitoring System (NARMS) is a national public health surveillance system that monitors enteric bacteria and select animal pathogens to determine if they are resistant to antimicrobial agents used in human and veterinary medicine. NARMS is a collaboration of agencies within the U.S. Department of Health and Human Services (Food and Drug Administration (FDA) and Centers for Disease Control and Prevention (CDC)) and the U.S. Department of Agriculture (USDA) (Food Safety and Inspection Service (FSIS), Animal and Plant Health Inspection Service, and Agricultural Research Service).
The NARMS program tracks trends in antimicrobial resistance over time, identifies new types and patterns of resistance, and helps measure the impact of interventions designed to limit the spread of resistance. NARMS data are used by FDA in the regulatory review of new animal antimicrobial drugs, and to develop policies on judicious antimicrobial use in animals. To minimize potential consumer exposure to pathogens and antimicrobial resistance thereof, the CDC and FSIS use NARMS information on a case-by-case basis in foodborne illness and outbreak investigations.
What is New in This Report?
A new way to calculate multidrug resistance (MDR)
MDR is defined as resistance to three or more antimicrobial drug classes. In previous annual reports, MDR was calculated using the panel of antimicrobials employed for that testing year. If an antimicrobial agent had been removed from the panel, then it was not included in the MDR calculation in any year. Beginning with this report, antimicrobial agents tested historically are included when calculating MDR up until the year they were removed from the panel. Using this approach, the NARMS year-to-year MDR trend analysis and comparisons will be more consistent with past results.
Retail meat protocol
In 2019, FDA made the following changes to the retail meat testing protocol to increase pathogen recovery:
- Increased ground meats sample size from 25g to 50g
- Incorporated overnight enrichment for isolation of Salmonella
- Reprioritized retail sample collection from pork chops to ground pork
NARMS collects numerous bacterial isolates from 15 distinct human, animal, and food sources (see Table 1 below). This summary report prioritizes antimicrobial resistance in Salmonella, Campylobacter, and antimicrobial drug classes that are (1) most important to human medicine (generally, first- or second-line treatments), (2) multidrug resistant, and (3) specific drug resistance profiles of epidemiological importance.
It is important to note that the changes highlighted in this summary may be influenced by multiple factors and their interactions. These include changes in animal health, antimicrobial use, environmental influences, animal and food production practices, human behavior (such as travel and food-product choices), sampling and laboratory methodologies, and year-to-year variations in serotype distributions.
Salmonella and Campylobacter are the leading bacterial causes of foodborne illness in the United States, and are the main pathogens tracked by NARMS. Campylobacter and nontyphoidal serotypes of Salmonella enterica (henceforth referred to as Salmonella) can be present in the intestinal tracts of a wide range of animals including wildlife, livestock, and domestic pets. Salmonella and Campylobacter exposure in humans occurs primarily through the consumption of contaminated foods. In the United States each year, Salmonella is estimated to cause over 1.35 million illnesses, 26,500 hospitalizations, and 420 deaths, while Campylobacter is estimated to cause over 1.5 million illnesses, 19,500 hospitalizations, and 240 deaths (1). A small fraction of Salmonella and Campylobacter infections are known to result in long-term sequelae such as reactive arthritis and Guillain-Barré syndrome.
Generic Escherichia coli and Enterococcus isolated from NARMS samples are tested for antimicrobial susceptibility. NARMS monitors these bacteria in retail meats and cecal contents from animals to detect both emerging resistance patterns and specific resistance genes affecting drugs with gram-negative and gram-positive activity, respectively. For more information about these four bacterial organisms, visit the NARMS webpage.
This summary represents a consolidated view of the data generated from the four categories of NARMS historic sample sources:
- Human clinical isolates
- Food-producing animal isolates from cecal (intestinal) contents collected at slaughter establishments
- Meat and poultry product samples collected at inspected slaughter and processing establishments (FSIS product verification or exploratory testing)
- Raw meats (chicken, ground turkey, ground beef, and ground pork) collected at retail outlets in 21 states (20 sites)
- Animal clinical isolates
The NARMS samples were collected from the sources listed in Table 1 below.
Table 1: Data sources for 2019 NARMS Integrated Summary
* Previously referred to as Pathogen Reduction/Hazard Analysis Critical Control Point (PR/HACCP) testing or Routine testing. The food products sampled by FSIS at the regulated establishments as part of regulatory PR/HACCP sampling are called “product samples” and those collected by FDA from the retail outlets are called “retail samples”. The “product samples” include chicken (carcass, comminuted and parts), turkeys (carcass and comminuted), beef (beef manufacturing trimmings and ground beef), and pork1 (comminuted and intact/non-intact pork products).
**Beef includes steer, heifers, and beef cows.
2019 Highlights: Human and Food Animal Sources
The majority (78%) of Salmonella from humans were not resistant to any of the antimicrobials tested under NARMS. In humans, the overall level of resistance remains relatively unchanged from 2018, and is in line with other data from 2006-2017, where 76-85% of Salmonella tested were susceptible to all antimicrobials. However, important resistance threats to human and animal health remain. Some of these threats are highlighted in CDC’s 2019 Antibiotic Resistance Threats Report. Resistance to the most important clinical antimicrobial agents is summarized below.
- As in previous years, ceftriaxone resistance in human isolates remained below 4% in 2019.
- Before the emergence of MDR Infantis in 2014, Heidelberg was one of the more common ceftriaxone-resistant serotypes among human isolates. Notably, there were no ceftriaxone-resistant Heidelberg isolates from humans in 2019 in NARMS surveillance.
- Resistance increased in isolates from chicken (retail and product) and beef (product), likely driven by the presence of the blaCTX-M-65 gene in Infantis but declined or remained stable in the rest of the animal sample sources.
- Five Heidelberg isolates from retail meats and food animals (cecal contents and product samples) were resistant to ceftriaxone in 2019. Two of these were from retail chickens, and one each from chicken product, market swine cecal contents, and cattle product samples.
- In humans, from 2018 to 2019, Salmonella with decreased susceptibility to ciprofloxacin (DSC2) increased from 9% to 11%, from 18% to 31% in retail chicken, from 20% to 30% in chicken product samples, from 26% to 32% in chicken cecal contents samples, and from 0% to 14% in retail pork samples.
- In 2019, Enteritidis was the most common serotype among isolates with DSC, accounting for 45% of DSC Salmonella in humans (similar to the 2016 – 2018 data). The second most abundant serotype was Infantis (18%).
- The increase in DSC among poultry isolates was primarily due to the increase in serotype Infantis (which carried a single chromosomal gyrA mutation). DSC among Enteritidis (also carrying chromosomal gyrA mutations) from chicken product samples also increased from 5% in 2018 to 18% in 2019.
- Transmissible quinolone resistance genes qnrB, qnrS, aac(6’)-lb-cr, and oqxA continued to be identified among DSC isolates from humans, retail meats, cecal contents, and product samples. These genes were most common in isolates from swine (cecal contents samples from market swine and sow) and constituted over 95% of DSC.
Decreased susceptibility to azithromycin (DSA3) continued to be uncommon in 2019.
- Salmonella isolates from humans, retail meats, cecal contents, and product samples did not show any resistance to carbapenems.
- Only 1% of human isolates tested exhibited DSA, with serotype Newport comprising the majority (53%) of the isolates.
- In 2019, DSA Salmonella in cecal contents and products were also rare and represented about 1% of isolates in turkey products (1/296), pork products (5/528), market swine cecal contents (6/433), and beef cattle cecal contents (2/225).
- The mph(A) gene was found in many of the sequenced DSA isolates from humans (18/22), cecal contents (2/8), and product samples (1/1). The mph(E) gene was also found in three of the sequenced cecal content samples.
- In 2019, of the sixteen DSA Newport isolates from humans, thirteen (81%) were closely related to an outbreak strain (2) attributed to consumption of beef and dairy products.
Multidrug Resistance (MDR)
- In 2019, MDR Salmonella remained stable at around 10% and I 4,,12:i:- was the most common serotype accounting for 26% of MDR Salmonella.
- Ampicillin and trimethoprim-sulfamethoxazole (TMP-SMX) are now considered second-line drugs to treat Salmonella. In human isolates of Salmonella, resistance to ampicillin has been steadily declining from ~21% in 1996 to ~9% in 2019 while TMP-SMX resistance remained stable at ~3% during that period.
- MDR in Salmonella isolates recovered from chicken product samples between 2018 to 2019 showed an increase from 22% to 29% while isolates from retail chicken increased from 20% to 32%. These increases were largely driven by the rise in MDR Salmonella Infantis isolates. The number of resistance genes in MDR Salmonella Infantis varied, and in some isolates up to ten AMR genes were found (3). In 2019, the percentage of MDR Salmonella recovered from chicken cecal contents samples remained around 32%.
- In turkey product and retail turkey samples MDR Salmonella continued to decline between 2018 (25%) and 2019 (17% and 21%). However, MDR increased from 23% to 31% in Salmonella isolates from turkey cecal contents. The majority of MDR Salmonella isolates from turkey samples were serotypes Reading, Infantis, and Typhimurium.
- Extremely drug-resistant (XDR) is defined as resistance to eight or more antimicrobial drug classes. In 2019, XDR was detected in six human, eleven cattle, two swine, and one chicken isolate. Serotypes involved included: twelve Dublin, two Agona, two Infantis, two Typhimurium, one I 4,,12:i:-, and one Newport.
- Two Salmonella isolates from humans and two from market swine cecal contents exhibited decreased susceptibility to all three first-line antimicrobial agents used for the treatment of complicated or invasive salmonellosis (ceftriaxone, ciprofloxacin, azithromycin). Isolates from humans included serotypes Typhimurium and Infantis, and both isolates from market swine cecal contents were serotype Agona.
MDR Salmonella I 4,,12:i:-
- Since 2010, the percentage of MDR isolates from humans that are serotype I 4,,12:i:- has been steadily increasing (7% in 2010 to 26% in 2019). A similar increase was seen in isolates from swine samples taken between 2013 (7%) and 2019 (35%).
- Approximately 78% of MDR I 4,,12:i:- isolates from humans had combined resistance to ampicillin, streptomycin, sulfisoxazole, and tetracycline (ASSuT) in 2019. Infections with this antimicrobial resistance pattern have been associated with pork consumption in a 2019 outbreak (4).
- Approximately 71% of I 4,,12:i:- isolates from all retail meat sources and 77% from turkey product, market swine cecal contents, and sow cecal contents samples combined also exhibited resistance to ASSuT. One isolate from retail pork was resistant to ASSuT plus ceftriaxone, chloramphenicol, ciprofloxacin, nalidixic acid, gentamicin, and trimethoprim-sulfamethoxazole. To our knowledge, this is the first I 4,,12:i:- isolate from a food source with this MDR pattern in the United States. More information on this isolate can be found on the NARMS Interim Data Updates page.
- Over the past decade, MDR I 4,,12:i:- has become a public health concern in both Europe (5) and the United States (6). The resistance to ceftriaxone and ciprofloxacin in MDR I 4,,12:i:-, is particularly concerning because these antibiotics are routinely used to treat severe Salmonella infections.
- Macrolide-resistant (azithromycin or erythromycin) C. jejuni isolates from humans, and chicken sources (chicken cecal contents, chicken product, and chicken retail samples) remained at or below 3%. Between 2018 and 2019, macrolide-resistant C. coli from humans decreased from 13% to 8% and remained around 4% in both chicken product and chicken cecal contents samples. Among the cecal contents samples, macrolide-resistant C. coli was most common in market swine (26%).
- In humans, the proportion of ciprofloxacin-resistant Campylobacter isolates increased for both C. jejuni (29% in 2018 and 34% in 2019) and C. coli (41% in 2018 to 45% in 2019).
- Ciprofloxacin-resistant C. jejuni isolated from both chicken cecal contents (21% in 2018 to 26% in 2019) and chicken retail samples (20% in 2018 to 22% in 2019) increased compared to the previous year. The highest level of ciprofloxacin resistance was seen in beef cattle cecal contents samples (62% in C. coli) in 2019.
- Additional work is needed to understand why fluoroquinolone resistance is rising in Campylobacter.
- Between 2018 and 2019, ceftriaxone-resistant E. coli increased from 3% to 7% in sow cecal samples and from 4% to 7% in retail pork.
- DSA4 was detected in less than 1% of E. coli isolates. This included E. coli from retail samples (two from pork, one each from chicken and turkey), and cecal contents samples (five from market swine and one from beef cattle). All DSA isolates carried a corresponding mph(A) gene, except for the isolate from retail chicken.
- DSC remained under 8% among E. coli from cecal contents, product, and retail meats. Of the cecal contents and product isolates, 52% (45/86) were associated with gyr or par mutations and twenty-three contained qnr genes. In retail meats, eleven isolates contained qnr resistance genes, and the remaining twenty-five had at least one mutation in the gyr or par genes.
- MDR E. coli either decreased or remained stable in all retail meat, cecal contents, and product samples except for retail pork, where it increased from 16% to 22% from 2018 to 2019. In 2019, three XDR E. coli were isolated from market swine cecal contents, sow cecal contents, and retail pork samples.
- None of the E. coli isolates from retail meats or animal cecal contents samples showed any resistance to carbapenems.
- Since testing began in 2013, erythromycin resistance has increased from 2% to 12% among predominant enterococcal species in beef cattle cecal contents samples. Species E. hirae, E. durans and E. gallinarum accounted for the greatest proportion of macrolide-resistant Enterococcus.
- Since the testing of cecal contents began in 2013, there has been a decrease in gentamicin-resistant E. faecalis among turkeys (39% to 15%) and chickens (46% to 11%). There was a decrease in gentamicin-resistant E. faecalis from retail chicken (24% to 5%) during the same period, and a decrease in gentamicin-resistant E. faecalis from retail turkey (31% in 2017 to 16% in 2019).
- Following the 2016 approval of avilamycin for the prevention of necrotic enteritis associated with Clostridium perfringens in broiler chickens (7), NARMS added avilamycin to the Enterococcus panel in 2018. In 2019, only three avilamycin-resistant isolates (E. faecalis, E. durans, and E. gallinarum) were recovered from chicken cecal contents.
Colistin is considered a drug of last resort for some pan-resistant strains of Enterobacterales. The genomes of all Salmonella and E. coli isolates were examined for the presence of colistin resistance genes, mcr-1 through mcr-8. In general, fewer isolates positive for mcr genes have been reported in the United States5 than in countries where colistin is or has been used in food animal production (8,9). A comprehensive search of genome sequences in National Center for Biotechnology Information (NCBI) revealed the mcr-1 gene in six Salmonella isolates and two pathogenic E. coli (O109:H45 and:H11) isolates collected from humans in 2019. All isolates underwent whole genome sequencing at State health departments. NARMS also performed phenotypic antimicrobial susceptibility testing (AST) on five of eight isolates, confirming colistin resistance. In 2019, none of the Salmonella or E. coli isolates from NARMS cecal contents, product, or retail meat samples harbored any of the mcr-1 through mcr-8 resistance genes.
Antimicrobial Resistance in Animal Pathogens
The FDA’s Veterinary Laboratory Investigation and Response Network (Vet-LIRN) and USDA’s National Animal Health Laboratory Network (NAHLN) collect data on antimicrobial resistance (AMR) in animal pathogens with the goal of increasing antimicrobial stewardship. In 2017 and 2018, respectively, Vet-LIRN and NAHLN began collecting antimicrobial susceptibility data on clinically relevant bacterial isolates from different animal hosts, including companion animal species. The primary goal of both projects is to monitor AMR profiles in animal pathogens routinely isolated by veterinary clinics and diagnostic laboratories across the U.S. By developing a centralized data collection and reporting process across all of these laboratories, data can be monitored for trends in AMR phenotypes and genotypes to identify new or emerging resistance profiles, to help monitor the continued usefulness of antibiotics over time, and to provide information back to our stakeholders regarding these trends.
In 2019, Vet-LIRN continued the AMR monitoring program with thirty “Source” laboratories (25 labs in the U.S. and 5 labs in Canada) to conduct antimicrobial susceptibility testing (AST) of S. pseudintermedius and E. coli from dogs and Salmonella spp. from any animal host. Additional isolates surveyed were: Klebsiella pneumoniae, Pseudomonas aeruginosa, Enterococcus faecalis or faecium, and Streptococcus spp. (canis, equis, suis, zooepidemicus) (across all animal species). Six whole genome sequencing (WGS) laboratories (5 labs in the U.S. and 1 lab in Canada) sequenced a subset of the isolates submitted by their Source labs and uploaded all sequences to the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA). Concurrently, NAHLN continued the NAHLN AMR pilot project, covering the period from January 1, 2019 to December 31, 2019. Twenty-four laboratories provided AST data to the NAHLN. Microbiological data from four livestock species (cattle, swine, poultry, and horses), and two companion animal species (dogs and cats) were included. The bacterial isolates surveyed were E. coli (across all animal species), Salmonella enterica spp. and Mannheimia haemolytica (from cattle), Pasteurella multocida (from poultry), Streptococcus spp. (equis, suis, zooepidemicus) (from swine and horses) and Staphylococcus intermedius group (from dogs and cats). Both networks followed Clinical Laboratory Standards Institute (CLSI) AST testing methods. To view the Joint FDA and USDA Report on Antimicrobial Resistance, visit: 2019 Animal Pathogen AMR Data.
The NARMS collaboration is possible only through 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.
- CDC. Antibiotic Resistance Threats in the United States, 2019. Atlanta, GA: U.S. Department of Health and Human Services, CDC; 2019.
- Plumb ID, et al. Outbreak of Salmonella Newport infections with decreased susceptibility to azithromycin linked to beef obtained in the United States and soft cheese obtained in Mexico, 2018-2019. MMWR. Morbidity and Mortality Weekly Report, 2019 Aug 23: 68(33): 713–717.
- Tyson GH, et al. A multidrug-resistant Salmonella Infantis clone is spreading and recombining in the United States. Microbial Drug Resistance (Larchmont, N.Y.). 2020 Nov 24; doi:10.1089/mdr.2020.0389.
- CDC. Multistate outbreaks of multidrug-resistant Salmonella I 4,,12:i:- and Salmonella Infantis infections linked to pork (Final Update). Atlanta, GA:U.S. Department of Health and Human Services, CDC; 2015.
- EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control). The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2012. EFSA Journal 2014; 12(2):3547, 312 pp. doi:10.2903/j.efsa.2014.3547.
- Medalla F, Gu W, Friedman CR, et al. Increased incidence of antimicrobial-resistant nontyphoidal Salmonella infections, United States, 2004-2016. Emerging Infectious Diseases. 2021;27(6):1662-1672. doi:10.3201/eid2706.204486.
- Zhao, S et al. “Complete genome sequences of two avilamycin-resistant Enterococcus faecium strains isolated from chicken in the United States.” Microbiology Resource Announcements, vol. 8(47) e00957-19. 21 Nov. 2019, doi:10.1128/MRA.00957-19
- Sun J, et al. Towards understanding mcr-like colistin resistance. Trend Microbiol. 2018 Sep;26(9):794-808.
- Nang SC, et al. The rise and spread of mcr plasmid-mediated polymyxin resistance. Crit Rev Microbiol. 2019 Mar;45(2):131-161.
1FSIS Sampling program for exploratory pork - https://www.fsis.usda.gov/science-data/sampling-program/raw-pork-products-exploratory-sampling-program.
2The NARMS program started categorizing Salmonella with resistance to ciprofloxacin at MIC >= 0.12 ug/ml as DSC. Because even small increases in quinolone MICs can negatively impact the response to treatment, the DSC classification which includes Salmonella with lower-level resistance helps to decrease the likelihood of inadvertent ciprofloxacin treatment failures.
3CLSI (Clinical Laboratory Standards Institute) breakpoints for azithromycin are only established for Salmonella ser. Typhi. The azithromycin interpretive standards used for nontyphoidal Salmonella serotypes are NARMS-established breakpoints for resistance monitoring. We refer to nontyphoidal Salmonella isolates with an azithromycin MIC of ≥ 32 µg/mL as having decreased susceptibility to azithromycin (DSA). Similar to DSC, the DSA phenomenon is clinically relevant and important to avoid potential for treatment failure.
4CLSI breakpoints for azithromycin are not established for E. coli. The azithromycin interpretive standards used for E. coli are NARMS-established breakpoints for resistance monitoring. We refer to E. coli isolates with an azithromycin MIC of ≥ 32 µg/mL as having decreased susceptibility to azithromycin (DSA).
5There is a single colistin-containing product approved for use in food animals in the U.S., but it has never been marketed.