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Antimicrobial Stewardship in Outpatient Settings: A Systematic Review

Published online by Cambridge University Press:  22 December 2014

Dimitri M. Drekonja
Department of Medicine, University of Minnesota School of Medicine, Minneapolis, Minnesota Infectious Disease Service, Minneapolis VA Health Care System, Minneapolis, Minnesota
Gregory A. Filice
Department of Medicine, University of Minnesota School of Medicine, Minneapolis, Minnesota Infectious Disease Service, Minneapolis VA Health Care System, Minneapolis, Minnesota
Nancy Greer*
Center for Chronic Disease Outcomes Research, Minneapolis VA Health Care System, Minneapolis, Minnesota
Andrew Olson
Department of Medicine, University of Minnesota School of Medicine, Minneapolis, Minnesota Department of Pediatrics, University of Minnesota School of Medicine, Minneapolis, Minnesota
Roderick MacDonald
Center for Chronic Disease Outcomes Research, Minneapolis VA Health Care System, Minneapolis, Minnesota
Indulis Rutks
Center for Chronic Disease Outcomes Research, Minneapolis VA Health Care System, Minneapolis, Minnesota
Timothy J. Wilt
Department of Medicine, University of Minnesota School of Medicine, Minneapolis, Minnesota Center for Chronic Disease Outcomes Research, Minneapolis VA Health Care System, Minneapolis, Minnesota
Address correspondence to Nancy Greer, PhD, Minneapolis VA Health Care System, One Veterans Drive, Mail Code 111-O, Minneapolis, MN 55417 (



Evaluate the effect of outpatient antimicrobial stewardship programs on prescribing, patient, microbial outcomes, and costs.


Systematic review


Search of MEDLINE (2000 through November 2013), Cochrane Library, and reference lists of relevant studies. We included English language studies with patient populations relevant to the United States (eg, infectious conditions, prescription services) evaluating stewardship programs in outpatient settings and reporting outcomes of interest. Data regarding study characteristics and outcomes were extracted and organized by intervention type.


We identified 50 studies eligible for inclusion, with most (29 of 50; 58%) reporting on respiratory tract infections, followed by multiple/unspecified infections (17 of 50; 34%). We found medium-strength evidence that stewardship programs incorporating communication skills training and laboratory testing are associated with reductions in antimicrobial use, and low-strength evidence that other stewardship interventions are associated with improved prescribing. Patient-centered outcomes, which were infrequently reported, were not adversely affected. Medication costs were generally lower with stewardship interventions, but overall program costs were rarely reported. No studies reported microbial outcomes, and data regarding outpatient settings other than primary care clinics are limited.


Low- to moderate-strength evidence suggests that antimicrobial stewardship programs in outpatient settings improve antimicrobial prescribing without adversely effecting patient outcomes. Effectiveness depends on program type. Most studies were not designed to measure patient or resistance outcomes. Data regarding sustainability and scalability of interventions are limited.

Infect Control Hosp Epidemiol 2014;00(0):1–11

Original Articles
© 2014 by The Society for Healthcare Epidemiology of America. All rights reserved 

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1. Centers for Disease Control and Prevention website. Threat report 2013. Published September 2013. Accessed March 24, 2014.Google Scholar
2. Fairlie, T, Shapiro, DJ, Hersh, AL, Hicks, LA. National trends in visit rates and antibiotic prescribing for adults with acute sinusitis. Arch Intern Med 2012;172:15131514.Google Scholar
3. Smith, SS, Kern, RC, Chandra, RK, Tan, BK, Evans, CT. Variations in antibiotic prescribing of acute rhinosinusitis in United States ambulatory settings. Otolaryngol Head Neck Surg 2013;148:852859.Google Scholar
4. Barnett, ML, Linder, JA. Antibiotic prescribing to adults with sore throat in the United States, 1997–2010. JAMA Intern Med 2014;174:138140.Google Scholar
5. Costelloe, C, Metcalfe, C, Lovering, A, Mant, D, Hay, AD. Effect of antibiotic prescribing in primary care on antimicrobial resistance in individual patients: systematic review and meta-analysis. BMJ 2010;340:c2096.Google Scholar
6. MacDougall, C, Polk, RE. Antimicrobial stewardship programs in health care systems. Clin Microbiol Rev 2005;18:638656.Google Scholar
7. Dellit, TH, Owens, RC, McGowan, JE Jr, Gerding, DN, Weinstein, RA, Burke, JP. 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 2007;44:159177.CrossRefGoogle Scholar
8. Jacob, JT, Gaynes, RP. Emerging trends in antibiotic use in US hospitals: quality, quantification and stewardship. Expert Rev Anti Infect Ther 2010;8:893902.Google Scholar
9. Ohl, CA, Dodds Ashley, ES. Antimicrobial stewardship programs in community hospitals: the evidence base and case studies. Clin Infect Dis 2011;53:S23S28.Google Scholar
10. Ranji, SR, Steinman, MA, Shojania, KG, et al. Antibiotic prescribing behavior. In: Shojania KG, McDonald KM, Wachter RM, Owens DK, editors. Closing the Quality Gap: A Critical Analysis of Quality Improvement Strategies Vol. 4. Technical Review 9 (Prepared by the Stanford University-UCSF Evidence-based Practice Center under Contract No. 290-02-0017). AHRQ Publication No. 04(06)-0051-4 Rockville, MD: Agency for Healthcare Research and Quality. January 2006.Google Scholar
11. Ranji, SR, Steinman, MA, Shojania, KG, Gonzales, R. Intervention to reduce unnecessary antibiotic prescribing: a systematic review and quantitative analysis. Med Care 2008;46:847862.Google Scholar
12. Steinman, MA, Ranji, SR, Shojania, KG, Gonzales, R. Improving antibiotic selection: a systematic review and quantitative analysis of quality improvement strategies. Med Care 2006;44:617628.Google Scholar
13. Davey, P, Brown, E, Fenelon, L, et al. Interventions to improve antibiotic prescribing practices for hospital inpatients. Cochrane Database Syst Rev 2005, Issue 4. Art. No.: CD003543.Google Scholar
14. Arnold, SR, Straus, SE. Interventions to improve antibiotic prescribing practices in ambulatory care. Cochrane Database Syst Rev 2005, Issue 4. Art. No.: CD003539.Google Scholar
15. Suggested risk of bias criteria for EPOC reviews. Effective Practice and Organisation of Care (EPOC) website. Published 2014. Accessed March 24, 2014.Google Scholar
16. Shea, BJ, Grimshaw, JM, Wells, GA, et al. Development of AMSTAR: a measurement tool to assess the methodological quality of systematic reviews. BMC Med Res Methodol 2007;7:10.Google Scholar
17. Owens, DK, Lohr, KN, Atkins, D, et al. AHRQ series paper 5: grading the strength of a body of evidence when comparing medical interventions—Agency for Healthcare Research and Quality and the Effective Health Care Program. J Clin Epidemiol 2010;63:513523.Google Scholar
18. Gerber, JS, Prasad, PA, Fiks, AG, et al. Effect of an outpatient antimicrobial stewardship intervention on broad-spectrum antibiotic prescribing by primary care pediatricians: a randomized trial. JAMA 2013;309:23452352.CrossRefGoogle ScholarPubMed
19. Vinnard, C, Linkin, DR, Localio, AR, et al. Effectiveness of interventions in reducing antibiotic use for upper respiratory infections in ambulatory care practices. Popul Health Manag 2013;16:2227.Google Scholar
20. Finkelstein, JA, Huang, SS, Kleinman, K, et al. Impact of a 16-community trial to promote judicious antibiotic use in Massachusetts. Pediatrics 2008;121:e15e23.Google Scholar
21. Metlay, JP, Camargo, CA, MacKenzie, T, et al. for the IMPAACT Investigators. Cluster-randomized trial to improve antibiotic use for adults with acute respiratory infections treated in emergency departments. Ann Emerg Med 2007;50:221230.Google Scholar
22. Gonzales, R, Sauaia, A, Corbett, KK, et al. Antibiotic treatment of acute respiratory tract infections in the elderly: effect of a multidimensional educational intervention. J Am Geriatr Soc 2004;52:3945.Google Scholar
23. Stewart, J, Pilla, J, Lunn, L. Pilot study for appropriate anti-infective community therapy: effect of a guideline-based strategy to optimize use of antibiotics. Can Fam Physician 2000;46:851859.Google Scholar
24. Linder, JA, Schnipper, JL, Tsurikova, R, et al. Electronic health record feedback to improve antibiotic prescribing for acute respiratory infections. Am J Manag Care 2010;16(12 Suppl HIT):e311e319.Google Scholar
25. Dowell, D, Tian, LH, Stover, JA, et al. Changed in fluoroquinolone use for gonorrhea following publication of revised treatment guidelines. Am J Public Health 2012;102:148155.Google Scholar
26. Weiss, K, Blais, R, Fortin, A, Lantin, S, Gaudet, M. Impact of a multipronged education strategy on antibiotic prescribing in Quebec, Canada. Clin Infectious Dis 2011;53:433439.Google Scholar
27. Worrall, G, Kettle, A, Graham, W, Hutchinson, J. Postdated versus usual delayed antibiotic prescriptions in primary care. Can Fam Physician 2010;56:10321036.Google Scholar
28 Légaré, F, Labrecque, M, Cauchon, M, Castel, J, Turcotte, S, Grimshaw, J. Training family physicians in shared decision-making to reduce the overuse of antibiotics in acute respiratory infections: a cluster randomized trial. CMAJ 2012;184:E726E734.Google Scholar
29. Légaré, F, Labrecque, M, LeBlanc, A, et al. Training family physicians in shared decision making for the use of antibiotics for acute respiratory infections: a pilot clustered randomized controlled trial. Health Expect 2010;14:S96S110.Google Scholar
30. Manns, B, Laupland, K, Tonelli, M, Gao, S, Hemmelgam, B. Evaluating the impact of a novel restricted reimbursement policy for quinolone antibiotics: A time series analysis. BMC Health Serv Res 2012;12:290.Google Scholar
31. Marshall, D, Gough, J, Grootendorst, P, et al. Impact of administrative restrictions on antibiotic use and expenditure in Ontario: time series analysis. J Health Serv Res Policy 2006;11:1320.Google Scholar
32. Gonzales, R, Anderer, T, McCulloch, CE, et al. A cluster randomized trial of decision support strategies for reducing antibiotic use in acute bronchitis. JAMA Intern Med 2013;173:267273.CrossRefGoogle ScholarPubMed
33. Jenkins, TC, Irwin, A, Coombs, L, et al. Effects of clinical pathways for common outpatient infections on antibiotic prescribing. Am J Med 2013;126:327335.Google Scholar
34. McGinn, TG, McCullagh, L, Kannry, J, et al. Efficacy of an evidence-based clinical decision support in primary care practices. A randomized clinical trial. JAMA Intern Med ePub July 29, 2013.Google Scholar
35. Rattinger, GB, Mullins, CD, Zukerman, IH, et al. A sustainable strategy to prevent misuse of antibiotics for acute respiratory infections. PLoS ONE 2012;7:e51147.Google Scholar
36. Linder, JA, Schnipper, JL, Tsurikova, R, et al. Documentation-based clinical decision support to improve antibiotic prescribing for acute respiratory infections in primary care: a cluster randomised controlled trial. Inform Prim Care 2009;17:231240.Google Scholar
37. Worrall, G, Hutchinson, J, Sherman, G, Griffiths, J. Diagnosing streptococcal sore throat in adults: randomized controlled trial of in-office aids. Can Fam Physician 2007;53:666671.Google Scholar
38. Butler, CC, Simpson, SA, Dunstan, F, et al. Effectiveness of multifaceted educational programme to reduce antibiotic dispensing in primary care: practice based randomized controlled trial. BMJ 2012;233:d8173.Google Scholar
39. Llor, C, Cots, JM, López-Valcárcel, BG, et al. Interventions to reduce antibiotic prescription for lower respiratory tract infections: Happy Audit study. Eur Respir J 2012;40:436441.Google Scholar
40. Llor, C, Bjerrum, L, Arranz, J, et al. C-reactive protein testing in patients with acute rhinosinusitis leads to a reduction in antibiotic use. Fam Pract 2012;29:653658.Google Scholar
41. Smeets, HM, Kuyvenhoven, MM, Akkerman, AE, et al. Intervention with educational outreach at large scale to reduce antibiotics for respiratory tract infections: a controlled before and after study. Fam Pract 2009;26:8387.Google Scholar
42. van Driel, ML, Coenen, S, Dirven, K, et al. What is the role of quality circles in strategies to optimize antibiotic prescribing? A pragmatic cluster-randomized controlled trial in primary care. Qual Saf Health Care 2007;16:197202.Google Scholar
43. Varonen, H, Rautakorpi, U-M, Nyberg, S, et al. for the MIKSTRA Collaborative Study Group. Implementing guidelines on acute maxillary sinusitis in general practice—a randomized controlled trial. Fam Pract 2007;24:201206.Google Scholar
44. Little, P, Rumsby, K, Kelly, J, et al. Information leaflet and antibiotic prescribing strategies for acute lower respiratory tract infection: a randomized controlled trial. JAMA 2005;293:30293305.Google Scholar
45. Gjelstad, S, Høye, S, Straand, J, Brekke, M, Dalen, I, Lindbæk, M. Improving antibiotic prescribing in acute respiratory tract infections: cluster randomised trial from Norwegian general practice (prescription peer academic detailing (Rx-PAD) study). BMJ 2013;347:f4403.Google Scholar
46. Naughton, C, Feely, J, Bennett, K. A RCT evaluating the effectiveness and cost-effectiveness of academic detailing versus postal prescribing feedback in changing GP antibiotic prescribing. J Eval Clin Pract 2009;15:807812.Google Scholar
47. Madridejos-Mora, R, Amado-Guirado, E, Pérez-Rodriguez, MT. Effectiveness of the combination of feedback and educational recommendations for improving drug prescription in general practice. Med Care 2004;42:643648.Google Scholar
48. Slekovec, C, Leroy, J, Vernaz-Hegi, N, et al. Impact of a region wide antimicrobial stewardship guideline on urinary tract infection prescription patterns. Int J Clin Pharm 2012;34:325329.Google Scholar
49. Venekamp, RP, Rovers, MM, Verheij, THJ, Bonten, MJM, Sachs, APE. Treatment of acute rhinosinusitis: discrepancy between guideline recommendations and clinical practice. Fam Pract 2012;29:706712.Google Scholar
50. Seager, JM, Howell-Jones, RS, Dunstan, FD, Lewis, MAO, Richmond, S, Thomas, DW. A randomised controlled trial of clinical outreach education to rationalise antibiotic prescribing for acute dental pain in the primary care setting. Br Dent J 2006;201:217222.Google Scholar
51. Martens, JD, Winkens, RAG, van der Weijden, T, de Bruyn, D, Severens, JL. Does a joint development and dissemination of multidisciplinary guidelines improve prescribing behaviour: a pre/post study with concurrent control group and a randomised trial. BMC Health Serv Res 2006;6:145.Google Scholar
52. Little, P, Moore, MV, Turner, S, et al. Effectiveness of five different approaches in management of urinary tract infections: randomised controlled trial. BMJ 2010;340:c199.Google Scholar
53. Little, P, Stuart, B, Francis, N, et al. on behalf of the GRACE consortium. Effects of internet-based training on antibiotic prescribing rates for acute respiratory-tract infections: a multinational cluster, randomised, factorial, controlled trial. Lancet 2013;382:11751182.Google Scholar
54. Cals, JW, Butler, CC, Hopstaken, RM, Hood, K, Dinant, GJ. Effect of point of care testing for C reactive protein and training in communication skills on antibiotic use in lower respiratory tract infections: cluster randomised trial. BMJ 2009;338:b1374.Google Scholar
55. Cals, JW, Ament, AJ, Hood, K, et al. C-reactive protein point of care testing and physician communication skills training for lower respiratory tract infections in general practice: economic evaluation of a cluster randomized trial. J Eval Clin Pract 2011;17:10591069.Google Scholar
56. Cals, JW, deBock, L, Beckers, P-JHW, et al. Enhanced communications skills and C-reactive protein point of care testing for respiratory tract infection: 3.5 year follow-up of a cluster randomized trial. Ann Fam Med 2013;11:157164.Google Scholar
57. Francis, NA, Butler, CC, Hood, K, Simpson, S, Wood, F, Nuttall, J. Effect of using an interactive booklet about childhood respiratory tract infections in primary care consultations on reconsulting and antibiotic prescribing: a cluster randomised controlled trial. BMJ 2009;339:b2885.Google Scholar
58. Altiner, A, Brockmann, S, Sielk, M, Wilm, S, Wegscheider, K, Abholz, H-H. Reducing antibiotic prescriptions for acute cough by motivating GPs to change their attitudes to communication and empowering patients: a cluster-randomized intervention study. J Antimicrob Chemother 2007;60:638644.Google Scholar
59. Martens, JD, van der Weijden, T, Severens, JL, et al. The effect of computer reminders on GPs’ prescribing behaviour: a cluster-randomised trial. Int J Med Inform 2007;76:S403S416.Google Scholar
60. Martens, JD, Werkhoven, MJ, Severens, JL, et al. Effects of a behaviour independent financial incentive on prescribing behaviour of general practitioners. J Eval Clin Pract 2007;13:369373.Google Scholar
61. Little, P, Hobbs, FDR, Moore, M, et al. Clinical score and rapid antigen detection test to guide antibiotic use for sore throats: randomized controlled trial of PRISM (primary care streptococcal management). BMJ 2013;347:f5806.Google Scholar
62. Brittain-Long, R, Westin, J, Olofsson, S, Lindh, M, Andersson, LM. Access to a polymerase chain reaction assay method targeting 13 respiratory viruses can reduce antibiotics: a randomised, controlled trial. BMC Med 2011;9:44.Google Scholar
63. Diederichsen, HZ, Skamling, M, Diederichsen, A, et al. Randomised controlled trial of CRP rapid test as a guide to treatment of respiratory infections in general practice. Scand J Prim Health Care 2000;18:3943.Google Scholar
64. Cals, JW, Schot, MJ, de Jong, SA, Dinant, GJ, Hopstaken, RM. Point-of-care C-reactive protein testing and antibiotic prescribing for respiratory tract infections: a randomized controlled trial. Ann Fam Med 2010;8:124133.Google Scholar
65. Regev-Yochay, G, Raz, M, Dagan, R, et al. Reduction in antibiotic use following a cluster randomized controlled multifaceted intervention: the Israeli judicious antibiotic prescription study. Clin Infectious Dis 2011;53:3341.Google Scholar
66. Esmaily, HM, Silver, I, Shiva, S, et al. Can rational prescribing be improved by an outcome-based educational approach? A randomized trial completed in Iran. J Contin Educ Health Prof 2010;30:1118.Google Scholar
67. Chazan, B, Turjeman, RBZ, Frost, Y, et al. Antibiotic consumption successfully reduced by a community intervention program. Isr Med Assoc J 2007;9:1620.Google Scholar
68. Pagaiya, N, Garner, P. Primary care nurses using guidelines in Thailand: a randomized controlled trial. Trop Med Int Health 2005;10:471477.Google Scholar
69. Takemura, Y, Ebisawa, K, Kakoi, H, et al. Antibiotic selection patterns in acutely febrile new outpatients with or without immediate testing for C reactive protein and leucocyte count. J Clin Pathol 2005;58:729733.Google Scholar
70. Moore, M, Little, P, Rumsby, K, Kelly, J, et al. Effect of antibiotic prescribing strategies and an information leaflet on longer-term reconsultation for acute lower respiratory tract infection. Brit J Gen Pract 2009;59:728734.Google Scholar
71. Schuetz, P, Miller, B, Christ-Crain, M, Stoltz, D, Tamm, M, Bouadma, L. Procalcitonin to initiate or discontinue antibiotics in acute respiratory tract diseases. Cochrane Database Syst Rev 2012, Issue 9. Art. No.: CD007498. DOI: 10.1002/14651858.CD007498.pub2.Google Scholar
72. Aagaard, EM, Gonzales, R, Camargo, CA, et al. Physician champions are key to improving antibiotic prescribing quality. Jt Comm J Qual Patient Saf 2010;36:109116.Google Scholar
73. Stille, CJ, Rifas-Shiman, SL, Kleinman, K, Kotch, JB, Finkelstein, JA. Physician response to a community-level trial promoting judicious antibiotic use. Ann Fam Med 2008;6:206212.Google Scholar
74. Frich, JC, Høye, S, Lindbæk, M, Straand, J. General practitioners and tutors’ experiences with peer group academic detailing: a qualitative study. BMC Fam Pract 2010;11:12.Google Scholar
75. Allaire, A-S, Labrecque, M, Giguere, A, Gagnon, M-P, Légaré, F. What motivates family physicians to participate in training programs in shared decision making? J Contin Educ Health Prof 2012;32:98107.Google Scholar
76. van de Sande-Bruinsma, N, Grundmann, H, et al. for the European Antimicrobial Resistance Surveillance System Group; European Surveillance of Antimicrobial Consumption Project Group. Antimicrobial drug use and resistance in Europe. Emerg Infect Dis 2008;14:17221730.Google Scholar
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