Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 27, Number 6—June 2021
Research

Increased Incidence of Antimicrobial-Resistant Nontyphoidal Salmonella Infections, United States, 2004–2016

Felicita MedallaComments to Author , Weidong Gu, Cindy R. Friedman, Michael Judd, Jason Folster, Patricia M. Griffin, and Robert M. Hoekstra
Author affiliation: Centers for Disease Control and Prevention, Atlanta, Georgia, USA

Main Article

Table 1

Number and percentage of antimicrobial-resistant nontyphoidal Salmonella isolates, by serotype and resistance category, United States, 2004–2016*

Resistance category No. (%) isolates
Enteritidis, n = 5,206 Typhimurium, n = 4,404 Newport, n = 3,140 I 4,[5],12:i:-, n = 1,158 Heidelberg, n = 974 Other fully serotyped, n = 12,878 Not fully serotyped, n = 505 Total nontyphoidal Salmonella, N = 28,265
Any clinically important resistance† 548 (10.5) 1,197 (27.2) 284 (9.0) 389 (33.6) 240 (24.6) 843 (6.5) 45 (8.9) 3,546 (12.5)
Multidrug resistance‡ 114 (2.2) 1,178 (26.7) 271 (8.6) 382 (33.0) 204 (20.9) 727 (5.6) 36 (7.1) 2,912 (10.3)
Amp-only§ 152 (2.9) 897 (20.4) 30 (1.0) 319 (27.5) 120 (12.3) 311 (2.4) 28 (5.5) 1,857 (6.6)
Cef/Amp§¶ 15 (0.3) 212 (4.8) 237 (7.5) 39 (3.4) 116 (11.9) 212 (1.6) 4 (0.8) 835 (3.0)
Cipro§# 381 (7.3) 88 (2.0) 17 (0.5) 31 (2.7) 4 (0.4) 320 (2.5) 13 (2.6) 854 (3.0)

*Amp-only, resistant to ampicillin (MIC >32 µg/mL) but susceptible to ceftriaxone and ciprofloxacin; Cef/Amp, resistant to ceftriaxone (MIC >4 µg/mL) and ampicillin; Cipro, nonsusceptible to ciprofloxacin (MIC >0.12 µg/mL) but susceptible to ceftriaxone; NTS, nontyphoidal Salmonella, which includes isolates serotyped as Enteritidis, Typhimurium, Newport, I 4,[5],12:i:-, and Heidelberg, isolates serotyped as other than those 5, and those not fully serotyped.
†Includes any of the 3 clinically important resistance patterns (i.e., resistant to ceftriaxone, resistant to ampicillin, or nonsusceptible to ciprofloxacin). Isolates might have resistance to other agents tested.
‡Resistant to >3 classes of antimicrobial agents.
§Amp-only, Cef/Amp, and Cipro are mutually exclusive categories of clinically important resistance.
¶Of the 835 isolates with Cef/Amp resistance, 78 (0.3% of all nontyphoidal Salmonella isolates) were nonsusceptible to ciprofloxacin. Of the 78 isolates, 71 (91%) had ciprofloxacin MICs within the intermediate range (i.e., 0.12–0.5) (Appendix Figure 6). These 78 isolates were not included in the Cipro category.
#Of the 854 isolates, 785 (92%) had ciprofloxacin MICs within the intermediate range (Appendix Figure 6).

Main Article

References
  1. Scallan  E, Hoekstra  RM, Angulo  FJ, Tauxe  RV, Widdowson  MA, Roy  SL, et al. Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis. 2011;17:7–15. DOIPubMedGoogle Scholar
  2. Pegues  DA, Miller  SI. Salmonella Species. In: John E. Bennett, Raphael Dolin, Blaser. MJ, eds. Mandell, Douglas, and Bennett’s principles and practice of infectious diseases. Philadelphia: Elsevier Saunders; 2020. p. 2725–36.
  3. Varma  JK, Greene  KD, Ovitt  J, Barrett  TJ, Medalla  F, Angulo  FJ. Hospitalization and antimicrobial resistance in Salmonella outbreaks, 1984-2002. Emerg Infect Dis. 2005;11:943–6. DOIPubMedGoogle Scholar
  4. Krueger  AL, Greene  SA, Barzilay  EJ, Henao  O, Vugia  D, Hanna  S, et al. Clinical outcomes of nalidixic acid, ceftriaxone, and multidrug-resistant nontyphoidal salmonella infections compared with pansusceptible infections in FoodNet sites, 2006-2008. Foodborne Pathog Dis. 2014;11:335–41. DOIPubMedGoogle Scholar
  5. Varma  JK, Molbak  K, Barrett  TJ, Beebe  JL, Jones  TF, Rabatsky-Ehr  T, et al. Antimicrobial-resistant nontyphoidal Salmonella is associated with excess bloodstream infections and hospitalizations. J Infect Dis. 2005;191:554–61. DOIPubMedGoogle Scholar
  6. Crump  JA, Barrett  TJ, Nelson  JT, Angulo  FJ. Reevaluating fluoroquinolone breakpoints for Salmonella enterica serotype Typhi and for non-Typhi salmonellae. Clin Infect Dis. 2003;37:75–81. DOIPubMedGoogle Scholar
  7. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing, 31st edition (M100). Wayne (PA): The Institute; 2021.
  8. Johnson  LR, Gould  LH, Dunn  JR, Berkelman  R, Mahon  BE; Foodnet Travel Working Group. Salmonella infections associated with international travel: a Foodborne Diseases Active Surveillance Network (FoodNet) study. Foodborne Pathog Dis. 2011;8:1031–7. DOIPubMedGoogle Scholar
  9. Dewey-Mattia  D, Manikonda  K, Hall  AJ, Wise  ME, Crowe  SJ; Centers for Disease Control and Prevention. Surveillance for foodborne disease outbreaks—United States, 2009–2015. MMWR Surveill Summ. 2018;67:1–11. DOIPubMedGoogle Scholar
  10. Kozlica  J, Claudet  AL, Solomon  D, Dunn  JR, Carpenter  LR. Waterborne outbreak of Salmonella I 4,[5],12:i:-. Foodborne Pathog Dis. 2010;7:1431–3. DOIPubMedGoogle Scholar
  11. Marder Mph  EP, Griffin  PM, Cieslak  PR, Dunn  J, Hurd  S, Jervis  R, et al.; Centers for Disease Control and Prevention. Preliminary incidence and trends of infections with pathogens transmitted commonly through food—Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 2006–2017. MMWR Morb Mortal Wkly Rep. 2018;67:324–8. DOIPubMedGoogle Scholar
  12. Centers for Disease Control and Prevention. Multistate outbreaks of Salmonella infections linked to contact with live poultry in backyard flocks, 2018 (final update). 2018 Sep 13 [cited 2020 Oct 29]. https://www.cdc.gov/salmonella/backyard-flocks-06-18/index.html
  13. Huang  JY, Patrick  ME, Manners  J, Sapkota  AR, Scherzinger  KJ, Tobin-D’Angelo  M, et al. Association between wetland presence and incidence of Salmonella enterica serotype Javiana infections in selected US sites, 2005-2011. Epidemiol Infect. 2017;145:2991–7. DOIPubMedGoogle Scholar
  14. Dechet  AM, Scallan  E, Gensheimer  K, Hoekstra  R, Gunderman-King  J, Lockett  J, et al.; Multistate Working Group. Outbreak of multidrug-resistant Salmonella enterica serotype Typhimurium Definitive Type 104 infection linked to commercial ground beef, northeastern United States, 2003-2004. Clin Infect Dis. 2006;42:747–52. DOIPubMedGoogle Scholar
  15. Varma  JK, Marcus  R, Stenzel  SA, Hanna  SS, Gettner  S, Anderson  BJ, 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. J Infect Dis. 2006;194:222–30. DOIPubMedGoogle Scholar
  16. Centers for Disease Control and Prevention. National Antimicrobial Resistance Monitoring System for Enteric Bacteria (NARMS): human isolates final report, 2015. Atlanta: The Centers; 2018.
  17. Centers for Disease Control and Prevention. National Salmonella Surveillance [cited 2020 Oct 29]. https://www.cdc.gov/nationalsurveillance/salmonella-surveillance.html
  18. Centers for Disease Control and Prevention. National Antimicrobial Resistance Monitoring System for Enteric Bacteria [cited 2020 Oct 29]. https://www.cdc.gov/narms/reports/index.html
  19. Medalla  F, Hoekstra  RM, Whichard  JM, Barzilay  EJ, Chiller  TM, Joyce  K, et al. Increase in resistance to ceftriaxone and nonsusceptibility to ciprofloxacin and decrease in multidrug resistance among Salmonella strains, United States, 1996-2009. Foodborne Pathog Dis. 2013;10:302–9. DOIPubMedGoogle Scholar
  20. Medalla  F, Gu  W, Mahon  BE, Judd  M, Folster  J, Griffin  PM, et al. Estimated incidence of antimicrobial drug–resistant nontyphoidal Salmonella infections, United States, 2004–2012. Emerg Infect Dis. 2016;23:29–37. DOIPubMedGoogle Scholar
  21. Greene  SK, Stuart  AM, Medalla  FM, Whichard  JM, Hoekstra  RM, Chiller  TM. Distribution of multidrug-resistant human isolates of MDR-ACSSuT Salmonella Typhimurium and MDR-AmpC Salmonella Newport in the United States, 2003-2005. Foodborne Pathog Dis. 2008;5:669–80. DOIPubMedGoogle Scholar
  22. Crim  SM, Chai  SJ, Karp  BE, Judd  MC, Reynolds  J, Swanson  KC, et al. Salmonella enterica serotype Newport infections in the United States, 2004–2013: increased incidence investigated through four surveillance systems. Foodborne Pathog Dis. 2018;15:612–20. DOIPubMedGoogle Scholar
  23. Jones  TF, Ingram  LA, Cieslak  PR, Vugia  DJ, Tobin-D’Angelo  M, Hurd  S, et al. Salmonellosis outcomes differ substantially by serotype. J Infect Dis. 2008;198:109–14. DOIPubMedGoogle Scholar
  24. US Food and Drug Administration. 2018 NARMS update: integrated report summary interactive version [cited 2020 Dec 28]. https://www.fda.gov/animal-veterinary/national-antimicrobial-resistance-monitoring-system/2018-narms-update-integrated-report-summary-interactive-version
  25. US Census Bureau. Population and housing unit estimates [cited 2020 Oct 29]. https://www.census.gov/popest
  26. Gu  W, Medalla  F, Hoekstra  RM. Bayesian hierarchical model of ceftriaxone resistance proportions among Salmonella serotype Heidelberg infections. Spat Spatio-Temporal Epidemiol. 2018;24:19–26. DOIPubMedGoogle Scholar
  27. Lunn  DJ, Thomas  A, Best  N, Spiegelhalter  D. WinBUGS—a Bayesian modelling framework: concepts, structure, and extensibility. Stat Comput. 2000;10:325–37. DOIGoogle Scholar
  28. Lambert  PC, Sutton  AJ, Burton  PR, Abrams  KR, Jones  DR. How vague is vague? A simulation study of the impact of the use of vague prior distributions in MCMC using WinBUGS. Stat Med. 2005;24:2401–28. DOIPubMedGoogle Scholar
  29. Chai  SJ, White  PL, Lathrop  SL, Solghan  SM, Medus  C, McGlinchey  BM, et al. Salmonella enterica serotype Enteritidis: increasing incidence of domestically acquired infections. Clin Infect Dis. 2012;54(Suppl 5):S488–97. DOIPubMedGoogle Scholar
  30. Marcus  R, Varma  JK, Medus  C, Boothe  EJ, Anderson  BJ, Crume  T, et al.; Emerging Infections Program FoodNet Working Group. Re-assessment of risk factors for sporadic Salmonella serotype Enteritidis infections: a case-control study in five FoodNet Sites, 2002-2003. Epidemiol Infect. 2007;135:84–92. DOIPubMedGoogle Scholar
  31. O’Donnell  AT, Vieira  AR, Huang  JY, Whichard  J, Cole  D, Karp  BE. Quinolone-resistant Salmonella enterica serotype Enteritidis infections associated with international travel. Clin Infect Dis. 2014;59:e139–41. DOIPubMedGoogle Scholar
  32. Grass  JE, Kim  S, Huang  JY, Morrison  SM, McCullough  AE, Bennett  C, et al. Quinolone nonsusceptibility among enteric pathogens isolated from international travelers - Foodborne Diseases Active Surveillance Network (FoodNet) and National Antimicrobial Monitoring System (NARMS), 10 United States sites, 2004 - 2014. PLoS One. 2019;14:e0225800. DOIPubMedGoogle Scholar
  33. Harvey  RR, Friedman  CR, Crim  SM, Judd  M, Barrett  KA, Tolar  B, et al. Epidemiology of Salmonella enterica serotype Dublin infections among humans, United States, 1968–2013. Emerg Infect Dis. 2017;23:1493–501. DOIPubMedGoogle Scholar
  34. Elnekave  E, Hong  S, Mather  AE, Boxrud  D, Taylor  AJ, Lappi  V, et al. Salmonella enterica serotype 4,[5],12:i:- in swine in the United States Midwest: an emerging multidrug-resistant clade. Clin Infect Dis. 2018;66:877–85. DOIPubMedGoogle Scholar
  35. Rabatsky-Ehr  T, Whichard  J, Rossiter  S, Holland  B, Stamey  K, Headrick  ML, et al.; NARMS Working Group. Multidrug-resistant strains of Salmonella enterica Typhimurium, United States, 1997-1998. Emerg Infect Dis. 2004;10:795–801. DOIPubMedGoogle Scholar
  36. Leekitcharoenphon  P, Hendriksen  RS, Le Hello  S, Weill  FX, Baggesen  DL, Jun  SR, et al. Global genomic epidemiology of Salmonella enterica Serovar Typhimurium DT104. Appl Environ Microbiol. 2016;82:2516–26. DOIPubMedGoogle Scholar
  37. Centers for Disease Control and Prevention. Multistate outbreak of multidrug-resistant Salmonella I 4,[5],12:i:- and Salmonella Infantis infections linked to pork (final update) [cited 2020 Oct 29]. https://www.cdc.gov/salmonella/pork-08-15/index.html
  38. US Department of Agriculture, National Agricultural Statistics Service. Quarterly hogs and pigs. 2021 Mar 25 [cited 2021 Apr 19]. https://downloads.usda.library.cornell.edu/usda-esmis/files/rj430453j/7p88db205/mw22w1890/hgpg0321.pdf
  39. US Department of Agriculture, Economic Research Service. Factors affecting U.S. pork consumption/LDP-M-130–01. 2005 May [cited 2020 Oct 29]. https://www.ers.usda.gov/webdocs/outlooks/37377/15778_ldpm13001_1_.pdf?v=5280.8
  40. US Department of Commerce. National Travel and Tourism Office. U.S. travel and tourism statistics (U.S. resident outbound) [cited 2020 Oct 29]. https://travel.trade.gov/outreachpages/outbound.general_information.outbound_overview.asp
  41. Threlfall  EJ, Day  M, de Pinna  E, Charlett  A, Goodyear  KL. Assessment of factors contributing to changes in the incidence of antimicrobial drug resistance in Salmonella enterica serotypes Enteritidis and Typhimurium from humans in England and Wales in 2000, 2002 and 2004. Int J Antimicrob Agents. 2006;28:389–95. DOIPubMedGoogle Scholar
  42. Bae  D, Kweon  O, Khan  AA. Isolation and characterization of antimicrobial-resistant nontyphoidal Salmonella enterica serovars from imported food products. J Food Prot. 2016;79:1348–54. DOIPubMedGoogle Scholar
  43. Karp  BE, Campbell  D, Chen  JC, Folster  JP, Friedman  CR. Plasmid-mediated quinolone resistance in human non-typhoidal Salmonella infections: An emerging public health problem in the United States. Zoonoses Public Health. 2018;65:838–49. DOIPubMedGoogle Scholar
  44. Centers for Disease Control and Prevention. Foodborne Diseases Active Surveillance Network (FoodNet): FoodNet 2015 surveillance report (final update). Atlanta: The Centers; 2017.
  45. Scallan  E, Crim  SM, Runkle  A, Henao  OL, Mahon  BE, Hoekstra  RM, et al. Bacterial enteric infections among older adults in the United States: Foodborne Diseases Active Surveillance Network, 1996–2012. Foodborne Pathog Dis. 2015;12:492–9. DOIPubMedGoogle Scholar
  46. Angelo  KM, Reynolds  J, Karp  BE, Hoekstra  RM, Scheel  CM, Friedman  C. Antimicrobial resistance among nontyphoidal Salmonella isolated from blood in the United States, 2003–2013. J Infect Dis. 2016;214:1565–70. DOIPubMedGoogle Scholar
  47. Crump  JA, Medalla  FM, Joyce  KW, Krueger  AL, Hoekstra  RM, Whichard  JM, et al.; Emerging Infections Program NARMS Working Group. Antimicrobial resistance among invasive nontyphoidal Salmonella enterica isolates in the United States: National Antimicrobial Resistance Monitoring System, 1996 to 2007. Antimicrob Agents Chemother. 2011;55:1148–54. DOIPubMedGoogle Scholar
  48. Boore  AL, Hoekstra  RM, Iwamoto  M, Fields  PI, Bishop  RD, Swerdlow  DL. Salmonella enterica infections in the United States and assessment of coefficients of variation: a novel approach to identify epidemiologic characteristics of individual serotypes, 1996–2011. PLoS One. 2015;10:e0145416. DOIPubMedGoogle Scholar
  49. McDermott  PF, Tyson  GH, Kabera  C, Chen  Y, Li  C, Folster  JP, et al. Whole-genome sequencing for detecting antimicrobial resistance in nontyphoidal Salmonella. Antimicrob Agents Chemother. 2016;60:5515–20. DOIPubMedGoogle Scholar
  50. Karp  BE, Tate  H, Plumblee  JR, Dessai  U, Whichard  JM, Thacker  EL, et al. National Antimicrobial Resistance Monitoring System: two decades of advancing public health through integrated surveillance of antimicrobial resistance. Foodborne Pathog Dis. 2017;14:545–57. DOIPubMedGoogle Scholar

Main Article

Page created: April 30, 2021
Page updated: May 18, 2021
Page reviewed: May 18, 2021
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external