National Antimicrobial Resistance Monitoring System: Two Decades of Advancing Public Health Through Integrated Surveillance of Antimicrobial Resistance

Abstract Drug-resistant bacterial infections pose a serious and growing public health threat globally. In this review, we describe the role of the National Antimicrobial Resistance Monitoring System (NARMS) in providing data that help address the resistance problem and show how such a program can have broad positive impacts on public health. NARMS was formed two decades ago to help assess the consequences to human health arising from the use of antimicrobial drugs in food animal production in the United States. A collaboration among the Centers for Disease Control and Prevention, the U.S. Food and Drug Administration, the United States Department of Agriculture, and state and local health departments, NARMS uses an integrated “One Health” approach to monitor antimicrobial resistance in enteric bacteria from humans, retail meat, and food animals. NARMS has adapted to changing needs and threats by expanding surveillance catchment areas, examining new isolate sources, adding bacteria, adjusting sampling schemes, and modifying antimicrobial agents tested. NARMS data are not only essential for ensuring that antimicrobial drugs approved for food animals are used in ways that are safe for human health but they also help address broader food safety priorities. NARMS surveillance, applied research studies, and outbreak isolate testing provide data on the emergence of drug-resistant enteric bacteria; genetic mechanisms underlying resistance; movement of bacterial populations among humans, food, and food animals; and sources and outcomes of resistant and susceptible infections. These data can be used to guide and evaluate the impact of science-based policies, regulatory actions, antimicrobial stewardship initiatives, and other public health efforts aimed at preserving drug effectiveness, improving patient outcomes, and preventing infections. Many improvements have been made to NARMS over time and the program will continue to adapt to address emerging resistance threats, changes in clinical diagnostic practices, and new technologies, such as whole genome sequencing.

[1]  S. Ladely,et al.  Colistin Resistance mcr-1-Gene-Bearing Escherichia coli Strain from the United States , 2016, Genome Announcements.

[2]  P. McDermott,et al.  Characterization of blaCMY plasmids and their possible role in source attribution of Salmonella enterica serotype Typhimurium infections. , 2014, Foodborne pathogens and disease.

[3]  P. Fedorka-Cray,et al.  First report of vatB and vgaB from Enterococcus gallinarum in the USA. , 2008, International journal of antimicrobial agents.

[4]  J. Powers,et al.  Fluoroquinolone-resistant Campylobacter species and the withdrawal of fluoroquinolones from use in poultry: a public health success story. , 2007, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[5]  N. Marano,et al.  Fluoroquinolone-resistant Campylobacter infections: eating poultry outside of the home and foreign travel are risk factors. , 2004, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[6]  T. Barrett,et al.  Hospitalization and Antimicrobial Resistance in Salmonella Outbreaks, 1984–2002 , 2005, Emerging infectious diseases.

[7]  Rian,et al.  QUINOLONE-RESISTANT CAMPYLOBACTER JEJUNI INFECTIONS IN MINNESOTA , 1992 – 1998 , 2022 .

[8]  B. Tolar,et al.  Nationwide outbreak of multidrug-resistant Salmonella Heidelberg infections associated with ground turkey: United States, 2011 , 2015, Epidemiology and Infection.

[9]  J. Whichard,et al.  Quinolone-resistant Salmonella enterica serotype Enteritidis infections associated with international travel. , 2014, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[10]  B. Tolar,et al.  Identification and Characterization of Multidrug-Resistant Salmonella enterica Serotype Albert Isolates in the United States , 2022 .

[11]  G. Agga,et al.  Occurrence of Antimicrobial-Resistant Escherichia coli and Salmonella enterica in the Beef Cattle Production and Processing Continuum , 2014, Applied and Environmental Microbiology.

[12]  E. Barzilay,et al.  Increase in resistance to ceftriaxone and nonsusceptibility to ciprofloxacin and decrease in multidrug resistance among Salmonella strains, United States, 1996-2009. , 2013, Foodborne pathogens and disease.

[13]  Shaohua Zhao,et al.  MRSA and multidrug-resistant Staphylococcus aureus in U.S. retail meats, 2010-2011. , 2017, Food microbiology.

[14]  T. Crume,et al.  Highly resistant Salmonella Newport-MDRAmpC transmitted through the domestic US food supply: a FoodNet case-control study of sporadic Salmonella Newport infections, 2002-2003. , 2006, The Journal of infectious diseases.

[15]  J. Folster,et al.  Outbreak of Salmonella Heidelberg Infections Linked to a Single Poultry Producer — 13 States, 2012–2013 , 2013, MMWR. Morbidity and mortality weekly report.

[16]  S. M. García,et al.  2014: , 2020, A Party for Lazarus.

[17]  J. Folster,et al.  Emergence of Plasmid-Mediated Quinolone Resistance among Non-Typhi Salmonella enterica Isolates from Humans in the United States , 2009, Antimicrobial Agents and Chemotherapy.

[18]  F. Aarestrup,et al.  Development of a standardized susceptibility test for campylobacter with quality-control ranges for ciprofloxacin, doxycycline, erythromycin, gentamicin, and meropenem. , 2004, Microbial drug resistance.

[19]  T. Jones,et al.  Foodborne Diseases Active Surveillance Network—2 Decades of Achievements, 1996–2015 , 2015, Emerging infectious diseases.

[20]  Edward Topp,et al.  The scourge of antibiotic resistance: the important role of the environment. , 2013, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[21]  T. Jones,et al.  Antimicrobial-resistant nontyphoidal Salmonella is associated with excess bloodstream infections and hospitalizations. , 2005, The Journal of infectious diseases.

[22]  J. Folster,et al.  Reduced azithromycin susceptibility in Shigella sonnei, United States. , 2010, Microbial drug resistance.

[23]  IwamotoMartha,et al.  Ceftriaxone-Resistant Nontyphoidal Salmonella from Humans, Retail Meats, and Food Animals in the United States, 1996-2013. , 2017 .

[24]  P. McDermott,et al.  Characterization of extended-spectrum cephalosporin-resistant Salmonella enterica serovar Heidelberg isolated from food animals, retail meat, and humans in the United States 2009. , 2012, Foodborne pathogens and disease.

[25]  S. Greene,et al.  Distribution of multidrug-resistant human isolates of MDR-ACSSuT Salmonella Typhimurium and MDR-AmpC Salmonella Newport in the United States, 2003-2005. , 2008, Foodborne pathogens and disease.

[26]  A. Petersen,et al.  Development of a Pefloxacin Disk Diffusion Method for Detection of Fluoroquinolone-Resistant Salmonella enterica , 2015, Journal of Clinical Microbiology.

[27]  S. Solomon,et al.  Antibiotic resistance threats in the United States: stepping back from the brink. , 2014, American family physician.

[28]  T. Jones,et al.  Antimicrobial Resistance among Campylobacter Strains, United States, 1997–2001 , 2004, Emerging infectious diseases.

[29]  Jianzhong Shen,et al.  Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. , 2015, The Lancet. Infectious diseases.

[30]  Caroline Smith DeWaal,et al.  World Health Organization Ranking of Antimicrobials According to Their Importance in Human Medicine: A Critical Step for Developing Risk Management Strategies to Control Antimicrobial Resistance From Food Animal Production. , 2016, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[31]  P. McDermott,et al.  The National Antimicrobial Resistance Monitoring System: Two Decades of Vigilance , 2017 .

[32]  David H Lloyd,et al.  Reservoirs of antimicrobial resistance in pet animals. , 2007, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[33]  S. Levy,et al.  Food Animals and Antimicrobials: Impacts on Human Health , 2011, Clinical Microbiology Reviews.

[34]  J. Bono,et al.  Complete Genome Sequence of a Colistin Resistance Gene (mcr-1)-Bearing Isolate of Escherichia coli from the United States , 2016, Genome Announcements.

[35]  A. Sapkota,et al.  Aquaculture practices and potential human health risks: current knowledge and future priorities. , 2008, Environment international.

[36]  Shaohua Zhao,et al.  Whole-Genome Sequencing for Detecting Antimicrobial Resistance in Nontyphoidal Salmonella , 2016, Antimicrobial Agents and Chemotherapy.

[37]  N. Marano,et al.  Prolonged diarrhea due to ciprofloxacin-resistant campylobacter infection. , 2004, The Journal of infectious diseases.

[38]  Ashraf A. Khan,et al.  Isolation and Characterization of Antimicrobial-Resistant Nontyphoidal Salmonella enterica Serovars from Imported Food Products. , 2016, Journal of food protection.

[39]  T. Barrett,et al.  Emergence of Multidrug-Resistant Salmonella enterica Serotype Newport Infections Resistant to Expanded-Spectrum Cephalosporins in the United States , 2003 .

[40]  Samir N. Patel,et al.  Methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria; approved guideline , 2006 .

[41]  Henk C den Bakker,et al.  Genomic Epidemiology: Whole-Genome-Sequencing-Powered Surveillance and Outbreak Investigation of Foodborne Bacterial Pathogens. , 2016, Annual review of food science and technology.

[42]  P. McDermott,et al.  Role of Efflux Pumps and Topoisomerase Mutations in Fluoroquinolone Resistance in Campylobacter jejuni and Campylobacter coli , 2005, Antimicrobial Agents and Chemotherapy.

[43]  P. Fedorka-Cray,et al.  Attribution of Salmonella enterica serotype Hadar infections using antimicrobial resistance data from two points in the food supply system , 2016, Epidemiology and Infection.

[44]  Ronald N. Jones,et al.  Broth Microdilution Susceptibility Testing of Campylobacter jejuni and the Determination of Quality Control Ranges for Fourteen Antimicrobial Agents , 2005, Journal of Clinical Microbiology.

[45]  M. Ferraro Performance standards for antimicrobial susceptibility testing , 2001 .

[46]  P. Fedorka-Cray,et al.  Prevalence of streptogramin resistance in enterococci from animals: identification of vatD from animal sources in the USA. , 2007, International journal of antimicrobial agents.

[47]  Shaohua Zhao,et al.  WGS accurately predicts antimicrobial resistance in Escherichia coli. , 2015, The Journal of antimicrobial chemotherapy.

[48]  J. Folster,et al.  Identification of the Aminoglycoside Resistance Determinants armA and rmtC among Non-Typhi Salmonella Isolates from Humans in the United States , 2009, Antimicrobial Agents and Chemotherapy.

[49]  P. McDermott,et al.  Identification and Expression of CephamycinaseblaCMY Genes in Escherichia coliand Salmonella Isolates from Food Animals and Ground Meat , 2001, Antimicrobial Agents and Chemotherapy.

[50]  P. McDermott,et al.  Whole-Genome Sequencing Analysis Accurately Predicts Antimicrobial Resistance Phenotypes in Campylobacter spp , 2015, Applied and Environmental Microbiology.

[51]  L. Hutwagner,et al.  Prior antimicrobial agent use increases the risk of sporadic infections with multidrug-resistant Salmonella enterica serotype Typhimurium: a FoodNet case-control study, 1996-1997. , 2004, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[52]  A. Robicsek,et al.  Plasmid-mediated quinolone resistance in non-Typhi serotypes of Salmonella enterica. , 2006, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[53]  D. Vugia,et al.  Clinical outcomes of nalidixic acid, ceftriaxone, and multidrug-resistant nontyphoidal salmonella infections compared with pansusceptible infections in FoodNet sites, 2006-2008. , 2014, Foodborne pathogens and disease.

[54]  Arti Kapi The evolving threat of antimicrobial resistance: Options for action , 2014 .

[55]  S. Ladely,et al.  High-level aminoglycoside resistant enterococci isolated from swine , 2004, Epidemiology and Infection.

[56]  J. Hughes,et al.  Antimicrobial Resistance, Food Safety, and One Health: The Need for Convergence. , 2016, Annual review of food science and technology.

[57]  J. Besser,et al.  Quinolone-ResistantCampylobacter jejuniInfections in Minnesota, 1992–1998 , 1999 .

[58]  Jennifer E. Stevenson,et al.  Human Salmonella and Concurrent Decreased Susceptibility to Quinolones and Extended-Spectrum Cephalosporins , 2007, Emerging infectious diseases.

[59]  S. Ladely,et al.  23S rRNA gene mutations contributing to macrolide resistance in Campylobacter jejuni and Campylobacter coli. , 2009, Foodborne pathogens and disease.

[60]  M. Tobin-D'Angelo,et al.  Infection with Pathogens Transmitted Commonly Through Food and the Effect of Increasing Use of Culture-Independent Diagnostic Tests on Surveillance--Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 2012-2015. , 2016, MMWR. Morbidity and mortality weekly report.

[61]  M. F. Wenberg,et al.  Foodborne Diseases Active Surveillance Network (FoodNet) , 1998 .

[62]  Nadine Oosmanally,et al.  Bacterial Enteric Infections Detected by Culture-Independent Diagnostic Tests — FoodNet, United States, 2012–2014 , 2015, MMWR. Morbidity and mortality weekly report.

[63]  J. B. Turpin,et al.  Development of a DNA microarray to detect antimicrobial resistance genes identified in the National Center for Biotechnology Information database. , 2010, Microbial drug resistance.

[64]  Hattie E. Webb,et al.  Carbapenem-Resistant Bacteria Recovered from Faeces of Dairy Cattle in the High Plains Region of the USA , 2016, PloS one.

[65]  P. McDermott,et al.  Novel gentamicin resistance genes in Campylobacter isolated from humans and retail meats in the USA. , 2015, The Journal of antimicrobial chemotherapy.