Skip to main content Accessibility help

The Impact of Reducing Antibiotics on the Transmission of Multidrug-Resistant Organisms

  • Sean L. Barnes (a1), Clare Rock (a2), Anthony D. Harris (a3), Sara E. Cosgrove (a2), Daniel J. Morgan (a3) (a4) (a5) and Kerri A. Thom (a3)...



Antibiotic resistance is a major threat to public health. Resistance is largely driven by antibiotic usage, which in many cases is unnecessary and can be improved. The impact of decreasing overall antibiotic usage on resistance is unknown and difficult to assess using standard study designs. The objective of this study was to explore the potential impact of reducing antibiotic usage on the transmission of multidrug-resistant organisms (MDROs).


We used agent-based modeling to simulate interactions between patients and healthcare workers (HCWs) using model inputs informed by the literature. We modeled the effect of antibiotic usage as (1) a microbiome effect, for which antibiotic usage decreases competing bacteria and increases the MDRO transmission probability between patients and HCWs and (2) a mutation effect that designates a proportion of patients who receive antibiotics to subsequently develop a MDRO via genetic mutation.


Intensive care unit


Absolute reduction in overall antibiotic usage by experimental values of 10% and 25%


Reducing antibiotic usage absolutely by 10% (from 75% to 65%) and 25% (from 75% to 50%) reduced acquisition rates of high-prevalence MDROs by 11.2% (P<.001) and 28.3% (P<.001), respectively. We observed similar effect sizes for low-prevalence MDROs.


In a critical care setting, where up to 50% of antibiotic courses may be inappropriate, even a moderate reduction in antibiotic usage can reduce MDRO transmission.

Infect Control Hosp Epidemiol 2017;38:663–669


Corresponding author

Address correspondence to Sean Barnes, 4352 Van Munching Hall, University of Maryland, College Park, MD 20742 ( or Kerri Thom, 685 West Baltimore Street, MSTF 334B, Baltimore, MD 21201 (


Hide All
1. Antibiotic resistance threats in the United States. 2013. antibiotic/antimicrobial resistance. Centers for Disease Control and Prevention website. Published 2013. Accessed January 19, 2017.
2. Tornieporth, NG, Roberts, RB, John, J, Hafner, A, Riley, LW. Risk factors associated with vancomycin-resistant Enterococcus faecium infection or colonization in 145 matched case patients and control patients. Clin Infect Dis Off Publ Infect Dis Soc Am 1996;23:767772.
3. Ling, ML, Tee, YM, Tan, SG, et al. Risk factors for acquisition of carbapenem resistant Enterobacteriaceae in an acute tertiary care hospital in Singapore. Antimicrob Resist Infect Control 2015;4:26.
4. Couderc, C, Jolivet, S, Thiébaut, ACM, et al. Fluoroquinolone use is a risk factor for methicillin-resistant Staphylococcus aureus acquisition in long-term care facilities: a nested case-case-control study. Clin Infect Dis Off Publ Infect Dis Soc Am 2014;59:206215.
5. Dellit, TH, Owens, RC, McGowan, JE, et al. Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship. Clin Infect Dis Off Publ Infect Dis Soc Am 2007;44:159177.
6. Macal, CM, North, MJ. Tutorial on agent-based modelling and simulation. J Simul 2010;4:151162.
7. Uri Wilensky. NetLogo home page. Northwestern University website. Published 2013. Accessed January 19, 2017.
8. Barnes, SL, Morgan, DJ, Harris, AD, Carling, PC, Thom, KA. Preventing the transmission of multidrug-resistant organisms: modeling the relative importance of hand hygiene and environmental cleaning interventions. Infect Control Hosp Epidemiol 2014;35:11561162.
9. Magiorakos, A-P, Srinivasan, A, Carey, RB, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis 2012;18:268281.
10. Climo, MW, Sepkowitz, KA, Zuccotti, G, et al. The effect of daily bathing with chlorhexidine on the acquisition of methicillin-resistant Staphylococcus aureus, vancomycin-resistant Enterococcus, and healthcare-associated bloodstream infections: results of a quasi-experimental multicenter trial. Crit Care Med 2009;37:18581865.
11. Smet, AM, de, Kluytmans, JA, Cooper, BS, et al. Decontamination of the digestive tract and oropharynx in ICU patients. N Engl J Med 2009;360:2031.
12. Reddy, T, Chopra, T, Marchaim, D, et al. Trends in antimicrobial resistance of Acinetobacter baumannii isolates from a metropolitan Detroit health system. Antimicrob Agents Chemother 2010;54:22352238.
13. Huskins, WC, Huckabee, CM, O’Grady, NP, et al. Intervention to reduce transmission of resistant bacteria in intensive care. N Engl J Med 2011;364:14071418.
14. Ziakas, PD, Thapa, R, Rice, LB, Mylonakis, E. Trends and significance of VRE colonization in the ICU: a meta-analysis of published studies. PloS One 2013;8:e75658.
15. Swaminathan, M, Sharma, S, Blash, SP, et al. Prevalence and risk factors for acquisition of carbapenem-resistant Enterobacteriaceae in the setting of endemicity. Infect Control Hosp Epidemiol 2013;34:809817.
16. Harris, AD, Pineles, L, Belton, B, et al. Universal glove and gown use and acquisition of antibiotic-resistant bacteria in the ICU: a randomized trial. JAMA 2013;310:15711580.
17. Dhar, S, Marchaim, D, Tansek, R, et al. Contact precautions: more is not necessarily better. Infect Control Hosp Epidemiol 2014;35:213221.
18. Morgan, DJ, Murthy, R, Munoz-Price, LS, et al. Reconsidering contact precautions for endemic methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococcus . Infect Control Hosp Epidemiol 2015;36:11631172.
19. Render, ML, Kim, HM, Deddens, J, et al. Variation in outcomes in Veterans Affairs intensive care units with a computerized severity measure. Crit Care Med 2005;33:930939.
20. Vasilevskis, EE, Kuzniewicz, MW, Cason, BA, et al. Mortality probability model III and simplified acute physiology score II: assessing their value in predicting length of stay and comparison to APACHE IV. Chest 2009;136:89101.
21. Khan, BA, Hui, KY, Hui, SL, et al. Time-motion analysis of health care workers’ contact with patients and workers’ hand hygiene: open vs closed units. Am J Crit Care Off Publ Am Assoc Crit-Care Nurses 2011;20:e75e79.
22. Morgan, DJ, Pineles, L, Shardell, M, et al. The effect of contact precautions on healthcare worker activity in acute care hospitals. Infect Control Hosp Epidemiol 2013;34:6973.
23. Hornbeck, T, Naylor, D, Segre, AM, Thomas, G, Herman, T, Polgreen, PM. Using sensor networks to study the effect of peripatetic healthcare workers on the spread of hospital-associated infections. J Infect Dis 2012;206:15491557.
24. Erasmus, V, Daha, TJ, Brug, H, et al. Systematic review of studies on compliance with hand hygiene guidelines in hospital care. Infect Control Hosp Epidemiol 2010;31:283294.
25. Girou, E, Loyeau, S, Legrand, P, Oppein, F, Brun-Buisson, C. Efficacy of handrubbing with alcohol based solution versus standard handwashing with antiseptic soap: randomised clinical trial. BMJ 2002;325:362.
26. Lawrence, SJ, Puzniak, LA, Shadel, BN, Gillespie, KN, Kollef, MH, Mundy, LM. Clostridium difficile in the intensive care unit: epidemiology, costs, and colonization pressure. Infect Control Hosp Epidemiol Off J Soc Hosp Epidemiol Am 2007;28:123130.
27. Vincent, JL, Rello, J, Marshall, J, et al. International study of the prevalence and outcomes of infection in intensive care units. JAMA 2009;302:23232329.
28. Candeloro, CL, Kelly, LM, Bohdanowicz, E, Martin, CM, Bombassaro, AM. Antimicrobial use in a critical care unit: a prospective observational study. Int J Pharm Pract 2012;20:164171.
29. Lilly, CM, Zuckerman, IH, Badawi, O, Riker, RR. Benchmark data from more than 240,000 adults that reflect the current practice of critical care in the United States. Chest 2011;140:12321242.
30. Get smart for healthcare. Core elements of hospital antibiotic stewardship programs. Centers for Disease Control and Prevention website. Accessed January 19, 2017.
31. File, TM, Srinivasan, A, Bartlett, JG. Antimicrobial stewardship: importance for patient and public health. Clin Infect Dis Off Publ Infect Dis Soc Am 2014;59:S93S96.
32. Nilholm, H, Holmstrand, L, Ahl, J, et al. An audit-based, infectious disease specialist-guided antimicrobial stewardship program profoundly reduced antibiotic use without negatively affecting patient outcomes. Open Forum Infect Dis 2015;2:ofv042.
33. Malani, AN, Richards, PG, Kapila, S, Otto, MH, Czerwinski, J, Singal, B. Clinical and economic outcomes from a community hospital’s antimicrobial stewardship program. Am J Infect Control 2013;41:145148.
34. Willmann, M, Marschal, M, Hölzl, F, Schröppel, K, Autenrieth, IB, Peter, S. Time series analysis as a tool to predict the impact of antimicrobial restriction in antibiotic stewardship programs using the example of multidrug-resistant Pseudomonas aeruginosa . Antimicrob Agents Chemother 2013;57:17971803.
35. Pelat, C, Kardaś-Słoma, L, Birgand, G, et al. Hand hygiene, cohorting, or antibiotic restriction to control outbreaks of multidrug-resistant Enterobacteriaceae. Infect Control Hosp Epidemiol 2016;37:272280.
36. Dickstein, Y, Geffen, Y, Leibovici, L, Paul, M. Comparison of antibiotic susceptibility patterns of bacterial isolates based on time from hospitalization and culture source: implications for hospital antibiograms. Infect Control Hosp Epidemiol 2016;37:212214.
37. McGregor, JC, Furuno, JP. Optimizing research methods used for the evaluation of antimicrobial stewardship programs. Clin Infect Dis Off Publ Infect Dis Soc Am 2014;59:S185S192.
38. Schechner, V, Temkin, E, Harbarth, S, Carmeli, Y, Schwaber, MJ. Epidemiological interpretation of studies examining the effect of antibiotic usage on resistance. Clin Microbiol Rev 2013;26:289307.
39. Malhotra-Kumar, S, Lammens, C, Coenen, S, Van Herck, K, Goossens, H. Effect of azithromycin and clarithromycin therapy on pharyngeal carriage of macrolide-resistant streptococci in healthy volunteers: a randomised, double-blind, placebo-controlled study. Lancet 2007;369:482490.
40. Hay, AD, Thomas, M, Montgomery, A, et al. The relationship between primary care antibiotic prescribing and bacterial resistance in adults in the community: a controlled observational study using individual patient data. J Antimicrob Chemother 2005;56:146153.
41. Cotter, PD, Stanton, C, Ross, RP, Hill, C. The impact of antibiotics on the gut microbiota as revealed by high-throughput DNA sequencing. Discov Med 2012;13:193199.
42. Drusano, GL, Louie, A, Deziel, M, Gumbo, T. The crisis of resistance: identifying drug exposures to suppress amplification of resistant mutant subpopulations. Clin Infect Dis Off Publ Infect Dis Soc Am 2006;42:525532.
Type Description Title
Supplementary materials

Barnes supplementary material
Barnes supplementary material 1

 Word (717 KB)
717 KB
Supplementary materials

Barnes supplementary material
Barnes supplementary material 2

 PDF (55 KB)
55 KB

The Impact of Reducing Antibiotics on the Transmission of Multidrug-Resistant Organisms

  • Sean L. Barnes (a1), Clare Rock (a2), Anthony D. Harris (a3), Sara E. Cosgrove (a2), Daniel J. Morgan (a3) (a4) (a5) and Kerri A. Thom (a3)...


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed