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Review
. 2017 Feb 9;2(2):CD003543.
doi: 10.1002/14651858.CD003543.pub4.

Interventions to improve antibiotic prescribing practices for hospital inpatients

Peter Davey  1 , Charis A Marwick  2 , Claire L Scott  3 , Esmita Charani  4 , Kirsty McNeil  5 , Erwin Brown  6 , Ian M Gould  7 , Craig R Ramsay  8 , Susan Michie  9
Affiliations
Review

Interventions to improve antibiotic prescribing practices for hospital inpatients

Peter Davey et al. Cochrane Database Syst Rev. .

Abstract

Background: Antibiotic resistance is a major public health problem. Infections caused by multidrug-resistant bacteria are associated with prolonged hospital stay and death compared with infections caused by susceptible bacteria. Appropriate antibiotic use in hospitals should ensure effective treatment of patients with infection and reduce unnecessary prescriptions. We updated this systematic review to evaluate the impact of interventions to improve antibiotic prescribing to hospital inpatients.

Objectives: To estimate the effectiveness and safety of interventions to improve antibiotic prescribing to hospital inpatients and to investigate the effect of two intervention functions: restriction and enablement.

Search methods: We searched the Cochrane Central Register of Controlled Trials (CENTRAL) (the Cochrane Library), MEDLINE, and Embase. We searched for additional studies using the bibliographies of included articles and personal files. The last search from which records were evaluated and any studies identified incorporated into the review was January 2015.

Selection criteria: We included randomised controlled trials (RCTs) and non-randomised studies (NRS). We included three non-randomised study designs to measure behavioural and clinical outcomes and analyse variation in the effects: non- randomised trials (NRT), controlled before-after (CBA) studies and interrupted time series (ITS) studies. For this update we also included three additional NRS designs (case control, cohort, and qualitative studies) to identify unintended consequences. Interventions included any professional or structural interventions as defined by the Cochrane Effective Practice and Organisation of Care Group. We defined restriction as 'using rules to reduce the opportunity to engage in the target behaviour (or increase the target behaviour by reducing the opportunity to engage in competing behaviours)'. We defined enablement as 'increasing means/reducing barriers to increase capability or opportunity'. The main comparison was between intervention and no intervention.

Data collection and analysis: Two review authors extracted data and assessed study risk of bias. We performed meta-analysis and meta-regression of RCTs and meta-regression of ITS studies. We classified behaviour change functions for all interventions in the review, including those studies in the previously published versions. We analysed dichotomous data with a risk difference (RD). We assessed certainty of evidence with GRADE criteria.

Main results: This review includes 221 studies (58 RCTs, and 163 NRS). Most studies were from North America (96) or Europe (87). The remaining studies were from Asia (19), South America (8), Australia (8), and the East Asia (3). Although 62% of RCTs were at a high risk of bias, the results for the main review outcomes were similar when we restricted the analysis to studies at low risk of bias.More hospital inpatients were treated according to antibiotic prescribing policy with the intervention compared with no intervention based on 29 RCTs of predominantly enablement interventions (RD 15%, 95% confidence interval (CI) 14% to 16%; 23,394 participants; high-certainty evidence). This represents an increase from 43% to 58% .There were high levels of heterogeneity of effect size but the direction consistently favoured intervention.The duration of antibiotic treatment decreased by 1.95 days (95% CI 2.22 to 1.67; 14 RCTs; 3318 participants; high-certainty evidence) from 11.0 days. Information from non-randomised studies showed interventions to be associated with improvement in prescribing according to antibiotic policy in routine clinical practice, with 70% of interventions being hospital-wide compared with 31% for RCTs. The risk of death was similar between intervention and control groups (11% in both arms), indicating that antibiotic use can likely be reduced without adversely affecting mortality (RD 0%, 95% CI -1% to 0%; 28 RCTs; 15,827 participants; moderate-certainty evidence). Antibiotic stewardship interventions probably reduce length of stay by 1.12 days (95% CI 0.7 to 1.54 days; 15 RCTs; 3834 participants; moderate-certainty evidence). One RCT and six NRS raised concerns that restrictive interventions may lead to delay in treatment and negative professional culture because of breakdown in communication and trust between infection specialists and clinical teams (low-certainty evidence).Both enablement and restriction were independently associated with increased compliance with antibiotic policies, and enablement enhanced the effect of restrictive interventions (high-certainty evidence). Enabling interventions that included feedback were probably more effective than those that did not (moderate-certainty evidence).There was very low-certainty evidence about the effect of the interventions on reducing Clostridium difficile infections (median -48.6%, interquartile range -80.7% to -19.2%; 7 studies). This was also the case for resistant gram-negative bacteria (median -12.9%, interquartile range -35.3% to 25.2%; 11 studies) and resistant gram-positive bacteria (median -19.3%, interquartile range -50.1% to +23.1%; 9 studies). There was too much variance in microbial outcomes to reliably assess the effect of change in antibiotic use. Heterogeneity of intervention effect on prescribing outcomesWe analysed effect modifiers in 29 RCTs and 91 ITS studies. Enablement and restriction were independently associated with a larger effect size (high-certainty evidence). Feedback was included in 4 (17%) of 23 RCTs and 20 (47%) of 43 ITS studies of enabling interventions and was associated with greater intervention effect. Enablement was included in 13 (45%) of 29 ITS studies with restrictive interventions and enhanced intervention effect.

Authors' conclusions: We found high-certainty evidence that interventions are effective in increasing compliance with antibiotic policy and reducing duration of antibiotic treatment. Lower use of antibiotics probably does not increase mortality and likely reduces length of stay. Additional trials comparing antibiotic stewardship with no intervention are unlikely to change our conclusions. Enablement consistently increased the effect of interventions, including those with a restrictive component. Although feedback further increased intervention effect, it was used in only a minority of enabling interventions. Interventions were successful in safely reducing unnecessary antibiotic use in hospitals, despite the fact that the majority did not use the most effective behaviour change techniques. Consequently, effective dissemination of our findings could have considerable health service and policy impact. Future research should instead focus on targeting treatment and assessing other measures of patient safety, assess different stewardship interventions, and explore the barriers and facilitators to implementation. More research is required on unintended consequences of restrictive interventions.

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Conflict of interest statement

Peter Davey is an author of four of the included studies. Charis Marwick is an author of two of the included studies. Ian Gould is an author of one of the included studies. Craig Ramsay is an author of one of the included studies. Other review authors completed data extractions for these studies. The institutions of the following authors received funding from the Chief Scientist Office that helped to support the conduct of this review: Peter Davey, Charis Marwick, Esmita Charani.

Peter Davey, none other than as indicated above. Charis Marwick, none other than as indicated above. Claire Scott, none other than as indicated above. Esmita Charani, none other than as indicated above. Kirsty McNeil, none other than as indicated above. Susan Michie, none other than as indicated above. Erwin Brown, none other than as indicated above. Ian Gould, none other than as indicated above. Craig Ramsay, none other than as indicated above.

Figures

1
1
Figure 1 Study flow diagram.
2
2
Risk of bias graph: review authors' judgements about each risk of bias item presented as percentages across all included studies. Blank sections in this graph are due to use of different ROB criteria for CBA, NRT and RCT versus ITS studies
3
3
Forest plot of comparison: 1 Prescribing: RCTs of all interventions to reduce unnecessary prescribing, outcome: 1.1 Dichotomous outcomes, increase in desired practice.
4
4
Forest plot of comparison: 1 Effectiveness: Prescribing outcomes from RCTs of interventions to reduce unnecessary antibiotic use, outcome: 1.4 Continuous outcomes, duration of all antibiotic treatment (days).
5
5
Forest plot of comparison: 2 Adverse effects: Clinical outcomes from RCTs of interventions to reduce unnecessary antibiotic use, outcome: 2.1 Mortality, all RCTs.
6
6
Forest plot of comparison: 2 Adverse effects: Clinical outcomes from RCTs of interventions to reduce unnecessary antibiotic use, outcome: 2.4 Length of stay, all RCTs.
7
7
Meta‐regression by effect modifier for 29 RCTs. A positive value for Beta indicates enhanced intervention effect. One RCT had both enabling and restrictive components in the intervention (Strom 2010).
8
8
Forest plot of comparison 5: RCTs of enablement with and without feedback, outcome: 5.1 Enablement plus feedback.
9
9
Forest plot of comparison 5: RCTs of enablement with and without feedback, outcome: 5.2 Enablement without feedback.
10
10
Meta‐regression by effect modifiers of intervention for 91 ITS studies. Outcome is effect on prescribing six months' postintervention. There are 16 studies with both enabling and restricting intervention components (Figure 11).
11
11
Meta‐regression of prescribing outcome by effect modifiers for 29 ITS studies of interventions that included restriction.
12
12
Meta‐regression by effect modifier for 43 ITS studies of interventions that included enablement but not restriction. Outcome is effect on prescribing six months' postintervention. Note that four studies with feedback were not included in this analysis because they also included restriction.
13
13
Meta‐regression by effect modifiers for 34 microbial outcomes 12 months' postintervention from 26 ITS studies. The bars show the results for unadjusted versus adjusted analyses, the comparison for unplanned interventions is with planned interventions in both the unadjusted and adjusted analysis. CDI: Clostridium difficile infection
 GPC: infection with antibiotic‐resistant gram‐positive cocci
 GNB: infection with antibiotic‐resistant gram‐negative bacteria Other infection control: 'Yes' means there were changes to infection control processes during the study period.
14
14
Meta‐regression by effect modifiers for 20 microbial outcomes 12 months' postintervention from 14 ITS studies of planned interventions that provided details about other infection control changes or interventions. CDI: Clostridium difficile infection
 GPC: infection with antibiotic‐resistant gram‐positive cocci
 GNB: infection with antibiotic‐resistant gram‐negative bacteria Other infection control: 'Yes' means there were changes to infection control processes during the study period.
1.1
1.1. Analysis
Comparison 1 Effectiveness: Prescribing outcomes from RCTs of interventions to reduce unnecessary antibiotic use, Outcome 1 Dichotomous outcomes, increase in desired practice.
1.2
1.2. Analysis
Comparison 1 Effectiveness: Prescribing outcomes from RCTs of interventions to reduce unnecessary antibiotic use, Outcome 2 Dichotomous outcomes, all RCTs with results of cluster RCTs adjusted by inflation factor.
1.3
1.3. Analysis
Comparison 1 Effectiveness: Prescribing outcomes from RCTs of interventions to reduce unnecessary antibiotic use, Outcome 3 Dichotomous outcomes, low or medium 'Risk of bias' studies only.
1.4
1.4. Analysis
Comparison 1 Effectiveness: Prescribing outcomes from RCTs of interventions to reduce unnecessary antibiotic use, Outcome 4 Continuous outcomes, duration of all antibiotic treatment (days).
1.5
1.5. Analysis
Comparison 1 Effectiveness: Prescribing outcomes from RCTs of interventions to reduce unnecessary antibiotic use, Outcome 5 Continuous outcomes, duration of all antibiotic treatment with results of cluster RCTs adjusted by inflation factor.
1.6
1.6. Analysis
Comparison 1 Effectiveness: Prescribing outcomes from RCTs of interventions to reduce unnecessary antibiotic use, Outcome 6 Continuous outcomes, low or medium 'Risk of bias' studies only.
1.7
1.7. Analysis
Comparison 1 Effectiveness: Prescribing outcomes from RCTs of interventions to reduce unnecessary antibiotic use, Outcome 7 Continuous outcome, consumption of targeted antibiotic only, standardised mean reduction (original outcome cost, days or DDD).
2.1
2.1. Analysis
Comparison 2 Adverse effects: Clinical outcomes from RCTs of interventions to reduce unnecessary antibiotic use, Outcome 1 Mortality, all RCTs.
2.2
2.2. Analysis
Comparison 2 Adverse effects: Clinical outcomes from RCTs of interventions to reduce unnecessary antibiotic use, Outcome 2 Mortality, all RCTs with results of cluster RCTs adjusted by inflation factor.
2.3
2.3. Analysis
Comparison 2 Adverse effects: Clinical outcomes from RCTs of interventions to reduce unnecessary antibiotic use, Outcome 3 Mortality, low or medium 'Risk of bias' RCTs.
2.4
2.4. Analysis
Comparison 2 Adverse effects: Clinical outcomes from RCTs of interventions to reduce unnecessary antibiotic use, Outcome 4 Length of stay, all RCTs.
2.5
2.5. Analysis
Comparison 2 Adverse effects: Clinical outcomes from RCTs of interventions to reduce unnecessary antibiotic use, Outcome 5 Length of stay, all RCTs with results of cluster RCTs adjusted by inflation factor.
2.6
2.6. Analysis
Comparison 2 Adverse effects: Clinical outcomes from RCTs of interventions to reduce unnecessary antibiotic use, Outcome 6 Length of stay, low or medium 'Risk of bias' RCTs only.
3.1
3.1. Analysis
Comparison 3 Adverse effects: Clinical outcomes of interventions targeting antibiotic choice, Outcome 1 Mortality for trial patients.
3.2
3.2. Analysis
Comparison 3 Adverse effects: Clinical outcomes of interventions targeting antibiotic choice, Outcome 2 Length of stay for trial patients.
4.1
4.1. Analysis
Comparison 4 Adverse effects: Clinical outcomes of interventions targeting antibiotic exposure, Outcome 1 Mortality for trial patients.
4.2
4.2. Analysis
Comparison 4 Adverse effects: Clinical outcomes of interventions targeting antibiotic exposure, Outcome 2 Length of stay for trial patients.
5.1
5.1. Analysis
Comparison 5 Modifiers of intended effect: Comparison of enabling interventions with and without feedback, Outcome 1 Enablement with feedback.
5.2
5.2. Analysis
Comparison 5 Modifiers of intended effect: Comparison of enabling interventions with and without feedback, Outcome 2 Enablement without feedback.
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    1. Champs C, Franchineau P, Gourgand JM, Loriette Y, Gaulme J, Sirot J. Clinical and bacteriological survey after change in aminoglycoside treatment to control an epidemic of Enterobacter cloacae. Journal of Hospital Infection 1994;28(3):219‐29. - PubMed
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    1. Elligsen M, Walker SAN, Pinto R, Simor A, Mubareka S, Rachlis A, et al. Audit and feedback to reduce broad‐spectrum antibiotic use among intensive care unit patients: a controlled interrupted time series analysis. Infection Control and Hospital Epidemiology 2012;33:354‐61. - PubMed
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    1. Fine MJ, Stone RA, Lave JR, Hough LJ, Obrosky DS, Mor MK, et al. Implementation of an evidence‐based guideline to reduce duration of intravenous antibiotic therapy and length of stay for patients hospitalized with community‐acquired pneumonia: a randomized controlled trial. American Journal of Medicine 2003;115(5):343‐51. - PubMed
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    1. Fowler S, Webber A, Cooper BS, Phimister A, Price K, Carter Y, et al. Successful use of feedback to improve antibiotic prescribing and reduce Clostridium difficile infection: a controlled interrupted time series. Journal of Antimicrobial Chemotherapy 2007;59:990‐5. - PubMed
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Poehling 2006 {published data only}
    1. Poehling KA, Zhu Y, Tang YW, Edwards K. Accuracy and impact of a point‐of‐care rapid influenza test in young children with respiratory illnesses. Archives of Pediatrics & Adolescent Medicine 2006;160:713‐8. - PubMed
Popovski 2015 {published data only}
    1. Popovski Z, Mercuri M, Main C, Sne N, Walsh K, Sung M, et al. Multifaceted intervention to optimize antibiotic use for intra‐abdominal infections. Journal of Antimicrobial Chemotherapy 2015;70:1226‐9. - PubMed
Price 2010 {published and unpublished data}
    1. Price J, Cheek E, Lippett S, Cubbon M, Gerding DN, Sambol SP, et al. Impact of an intervention to control Clostridium difficile infection on hospital‐ and community‐onset disease; an interrupted time series analysis. Clinical Microbiology & Infection 2010;16:1297‐302. - PubMed
Pulcini 2011 {published and unpublished data}
    1. Pulcini C, Defres S, Aggarwal I, Nathwani D, Davey P. Design of a 'day 3 bundle' to improve the reassessment of inpatient empirical antibiotic prescriptions. Journal of Antimicrobial Chemotherapy 2008;61(6):1384‐8. doi: 10.1093/jac/dkn113.. - PubMed
    1. Pulcini C, Dellamonica J, Bernardin G, Molinari N, Sotto A. Impact of an intervention designed to improve the documentation of the reassessment of antibiotic therapies in an intensive care unit. Medecine et Maladies Infectieuses 2011;41:546‐52. - PubMed
Qu 2012 {published data only}
    1. Qu R, Ji Y, Ling Y, Ye CY, Yang SM, Liu YY, et al. Procalcitonin is a good tool to guide duration of antibiotic therapy in patients with severe acute pancreatitis. A randomized prospective single‐center controlled trial. Saudi Medical Journal 2012;33:382‐7. - PubMed
Rattanaumpawan 2010 {published data only}
    1. Rattanaumpawan P, Sutha P, Thamlikitkul V. Effectiveness of drug use evaluation and antibiotic authorization on patients' clinical outcomes, antibiotic consumption, and antibiotic expenditures. American Journal of Infection Control 2010;38:38‐43. - PubMed
Rattanaumpawan 2011 {published data only}
    1. Rattanaumpawan P, Morales KH, Binkley S, Synnestvedt M, Weiner MG, Gasink LB, et al. Impact of antimicrobial stewardship programme changes on unnecessary double anaerobic coverage therapy. Journal of Antimicrobial Chemotherapy 2011;66:2655‐8. - PMC - PubMed
Richards 2003 {published data only}
    1. Richards MJ, Robertson MB, Dartnell JG, Duarte MM, Jones NR, Kerr DA, et al. Impact of a web‐based antimicrobial approval system on broad‐spectrum cephalosporin use at a teaching hospital. Medical Journal of Australia 2003;178:386‐90. - PubMed
Richardson 2000 {published data only}
    1. Richardson LP, Wiseman SW, Melani PN, Lyons MJ, Kauffman CA. Effectiveness of a vancomycin restriction policy in changing the prescribing patterns of house staff. Microbial Drug Resistance 2000;6(4):327‐30. - PubMed
Ross 2014 {published data only}
    1. Ross RK, Hersh AL, Kronman MP, Newland JG, Metjian TA, Localio AR, et al. Impact of Infectious Diseases Society of America/Pediatric Infectious Diseases Society guidelines on treatment of community‐acquired pneumonia in hospitalized children. Clinical Infectious Diseases: an official publication of the Infectious Diseases Society of America 2014;58:834‐8. - PMC - PubMed
Saizy‐Callaert 2003 {published data only}
    1. Saizy‐Callaert S, Causse R, Furhman C, Paih MF, Thebault A, Chouaid C. Impact of a multidisciplinary approach to the control of antibiotic prescription in a general hospital. Journal of Hospital Infection 2003;53(3):177‐82. - PubMed
Salama 1996 {published data only}
    1. Salama S, Rotstein C, Mandell L. A multidisciplinary hospital‐based antimicrobial use program: impact on hospital pharmacy expenditures and drug use. Canadian Journal of Infectious Diseases 1996;7:104‐9. - PMC - PubMed
Schnoor 2010 {published data only (unpublished sought but not used)}
    1. Schnoor M, Meyer T, Suttorp N, Raspe H, Welte T, Schafer T, et al. Development and evaluation of an implementation strategy for the German guideline on community‐acquired pneumonia. Quality & Safety in Health Care 2010;19:498‐502. - PubMed
Schouten 2007 {published data only}
    1. Schouten JA, Hulscher MEJL, Trap‐Liefers J, Akkermans RP, Kullberg BJ, Grol RPTM, et al. Tailored interventions to improve antibiotic use for lower respiratory tract infections in hospitals: a cluster‐randomized, controlled trial. Clinical Infectious Diseases 2007;44:931‐41. - PubMed
Schroeder 2009 {published data only}
    1. Schroeder S, Hochreiter M, Koehler T, Schweiger AM, Bein B, Keck FS, et al. Procalcitonin (PCT)‐guided algorithm reduces length of antibiotic treatment in surgical intensive care patients with severe sepsis: results of a prospective randomized study. Langenbeck's Archives of Surgery/Deutsche Gesellschaft fur Chirurgie 2009;394:221‐6. - PubMed
Schuetz 2009 {published data only}
    1. Schuetz P, Batschwaroff M, Dusemund F, Albrich W, Burgi U, Maurer M, et al. Effectiveness of a procalcitonin algorithm to guide antibiotic therapy in respiratory tract infections outside of study conditions: a post‐study survey. European Journal of Clinical Microbiology & Infectious Diseases 2010;29:269‐77. - PubMed
    1. Schuetz P, Christ‐Crain M, Albrich W, Zimmerli W, Mueller B, Pro Hosp Study Group. Guidance of antibiotic therapy with procalcitonin in lower respiratory tract infections: insights into the ProHOSP study. Virulence 2010;1:88‐92. - PubMed
    1. Schuetz P, Christ‐Crain M, Thomann R, Falconnier C, Wolbers M, Widmer I, et al. Effect of procalcitonin‐based guidelines vs standard guidelines on antibiotic use in lower respiratory tract infections: the ProHOSP randomized controlled trial. JAMA 2009;302:1059‐66. - PubMed
Schwann 2011 {published data only}
    1. Schwann NM, Bretz KA, Eid S, Burger T, Fry D, Ackler F, et al. Point‐of‐care electronic prompts: an effective means of increasing compliance, demonstrating quality, and improving outcome. Anesthesia & Analgesia 2011;113:869‐76. - PubMed
Schwartz 2007 {published data only}
    1. Schwartz DN, Abiad H, DeMarais PL, Armeanu E, Trick WE, Wang Y, et al. An educational intervention to improve antimicrobial use in a hospital‐based long‐term care facility. Journal of the American Geriatrics Society 2007;55:1236‐42. - PubMed
Senn 2004 {published data only}
    1. Senn L, Burnand B, Francioli P, Zanetti G. Improving appropriateness of antibiotic therapy: randomized trial of an intervention to foster reassessment of prescription after 3 days. Journal of Antimicrobial Chemotherapy 2004;53(6):1062‐7. - PubMed
Shehabi 2014 {published data only}
    1. Shehabi Y, Sterba M, Garrett PM, Rachakonda KS, Stephens D, Harrigan P, et al. Procalcitonin algorithm in critically ill adults with undifferentiated infection or suspected sepsis. A randomized controlled trial. American Journal of Respiratory and Critical Care Medicine 2014;190:1102‐10. - PubMed
Shen 2011 {published data only}
    1. Shen J, Sun Q, Zhou X, Wei Y, Qi Y, Zhu J, et al. Pharmacist interventions on antibiotic use in inpatients with respiratory tract infections in a Chinese hospital. International Journal of Clinical Pharmacy 2011;33:929‐33. - PubMed
Shojania 1998 {published data only}
    1. Shojania KG, Yokoe D, Platt R, Fiskio J, Ma'luf N, Bates DW. Reducing vancomycin use utilizing a computer guideline: results of a randomized controlled trial. Journal of the American Medical Informatics Association 1998;5(6):554‐62. - PMC - PubMed
Singh 2000 {published data only}
    1. Singh N, Rogers P, Atwood CW, Wagener MM, Yu VL. Short‐course empiric antibiotic therapy for patients with pulmonary infiltrates in the intensive care unit. A proposed solution for indiscriminate antibiotic prescription. American Journal of Respiratory and Critical Care Medicine 2000;162(2 Pt 1):505‐11. - PubMed
Sirinavin 1998 {published data only}
    1. Sirinavin S, Suvanakoot P, Sathapatayavongs B, Malatham K. Effect of antibiotic order form guiding rational use of expensive drugs on cost containment. Southeast Asian Journal of Tropical Medicine and Public Health 1998;29(3):636‐42. - PubMed
Skaer 1993 {published data only}
    1. Skaer TL, Sclar DA, Won JKH, Markowski DJ. Effect of academic detailing on the utilization of intravenous antimicrobial therapy. Current Therapeutic Research 1993;53(4):349‐55.
Skrlin 2011 {published data only}
    1. Skrlin J, Bacic Vrca V, Marusic S, Ciric‐Crncec M, Mayer L. Impact of ceftriaxone de‐restriction on the occurrence of ESBL‐positive bacterial strains and antibiotic consumption. Journal of Chemotherapy 2011;23:341‐4. - PubMed
Solomon 2001 {published data only}
    1. Solomon DH, Houten L, Glynn RJ, Baden L, Curtis K, Schrager H, et al. Academic detailing to improve use of broad‐spectrum antibiotics at an academic medical center. Archives of Internal Medicine 2001;161(15):1897‐902. - PubMed
Standiford 2012 {published data only}
    1. Standiford HC, Chan S, Tripoli M, Weekes E, Forrest GN. Antimicrobial stewardship at a large tertiary care academic medical center: cost analysis before, during, and after a 7‐year program. Infection Control and Hospital Epidemiology 2012;33:338‐45. - PubMed
Stevenson 1988 {published data only}
    1. Hampson JP, Corkhill JE, Murray A, Griffiths LR, Smith JC, Bartzokas CA. Potential financial benefits of a local antibiotic policy. Pharmaceutical Journal 1988;241:660‐2.
    1. Stevenson RC, Blackman SC, Williams CL, Bartzokas CA. Measuring the saving attributable to an antibiotic prescribing policy. Journal of Hospital Infection 1988;11:16‐25. - PubMed
Stocker 2010 {published data only}
    1. Stocker M, Fontana M, Helou S, Wegscheider K, Berger TM. Use of procalcitonin‐guided decision‐making to shorten antibiotic therapy in suspected neonatal early‐onset sepsis: prospective randomized intervention trial. Neonatology 2010;97:165‐74. - PubMed
Stolz 2007 {published data only}
    1. Stolz D, Christ‐Crain M, Bingisser R, Leuppi J, Miedinger D, Muller C, et al. Antibiotic treatment of exacerbations of COPD: a randomized, controlled trial comparing procalcitonin‐guidance with standard therapy. Chest 2007;131:9‐19. - PubMed
Stolz 2009 {published data only}
    1. Stolz D, Smyrnios N, Eggimann P, Pargger H, Thakkar N, Siegemund M, et al. Procalcitonin for reduced antibiotic exposure in ventilator‐associated pneumonia: a randomised study. European Respiratory Journal 2009;34:1364‐75. - PubMed
Strom 2010 {published data only}
    1. Strom BL, Schinnar R, Aberra F, Bilker W, Hennessy S, Leonard CE, et al. Unintended effects of a computerized physician order entry nearly hard‐stop alert to prevent a drug interaction: a randomized controlled trial. Archives of Internal Medicine 2010;170:1578. - PubMed
Sun 2011 {published data only}
    1. Sun TB, Chao SF, Chang BS, Chen TY, Gao PY, Shyr MH. Quality Improvements of antimicrobial prophylaxis in coronary artery bypass grafting. Journal of Surgical Research 2011;167:329‐35. - PubMed
Suwangool 1991 {published data only}
    1. Suwangool P, Moola‐Or P, Waiwatana A, Sitthi‐amorn C, Israsena S, Hanvanich M. Effect of a selective restriction policy on antibiotic expenditure and use: an institutional model. Journal of the Medical Association of Thailand 1991;74:272‐5. - PubMed
Talpaert 2011 {published data only}
    1. Talpaert MJ, Rao GG, Cooper BS, Wade P. Impact of guidelines and enhanced antibiotic stewardship on reducing broad‐spectrum antibiotic usage and its effect on incidence of Clostridium difficile infection. Journal of Antimicrobial Chemotherapy 2011;66:2168‐74. - PubMed
Tangdén 2011 {published data only}
    1. Tängdén T, Eriksson BM, Melhus A, Svennblad B, Cars O. Radical reduction of cephalosporin use at a tertiary hospital after educational antibiotic intervention during an outbreak of extended‐spectrum beta‐lactamase‐producing Klebsiella pneumoniae. Journal of Antimicrobial Chemotherapy 2011;66:1161‐7. - PubMed
Toltzis 1998 {published data only}
    1. Toltzis P, Yamashita T, Vilt L, Green M, Morrissey A, Spinner‐Block S, et al. Antibiotic restriction does not alter endemic colonization with resistant gram‐negative rods in a pediatric intensive care unit. Critical Care Medicine 1998;26(11):1893‐9. - PubMed
Toltzis 2002 {published data only}
    1. Toltzis P, Dul MJ, Hoyen C, Salvator A, Walsh M, Zetts L, et al. The effect of antibiotic rotation on colonization with antibiotic‐resistant bacilli in a neonatal intensive care unit. Pediatrics 2002;110:707‐11. - PubMed
Toltzis 2014 {published data only}
    1. Toltzis P, O'Riordan M, Cunningham DJ, Ryckman FC, Bracke TM, Olivea J, et al. A statewide collaborative to reduce pediatric surgical site infections. Pediatrics 2014;134:e1174‐80. - PubMed
Trenholme 1989 {published data only}
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Uçkay 2009 {published data only}
    1. Uçkay I, Vernaz‐Hegi N, Harbarth S, Stern R, Legout L, Vauthey L, et al. Activity and impact on antibiotic use and costs of a dedicated infectious diseases consultant on a septic orthopaedic unit. Journal of Infection 2009;58:205‐12. - PubMed
Valiquette 2007 {published data only}
    1. Valiquette L, Cossette B, Garant M‐P, Diab H, Pépin J. Impact of a reduction in the use of high‐risk antibiotics on the course of an epidemic of Clostridium difficile‐associated disease caused by the hypervirulent NAP1/027 strain. Clinical Infectious Diseases 2007;45:S112‐21. - PubMed
van Hees 2008 {published data only}
    1. Hees BC, Ruiter E, Wiltink EH, Jongh BM, Tersmette M. Optimizing use of ciprofloxacin: a prospective intervention study. Journal of Antimicrobial Chemotherapy 2008;61:210‐3. - PubMed
Van Kasteren 2005 {published data only}
    1. Mannien J, Kasteren ME, Nagelkerke NJ, Gyssens IC, Kullberg BJ, Wille JC, et al. Effect of optimized antibiotic prophylaxis on the incidence of surgical site infection. Infection Control & Hospital Epidemiology 2006;27:1340‐6. - PubMed
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Volpe 2012 {published data only}
    1. Volpe D, Harrison S, Damian F, Rachh P, Kahlon PS, Morrissey L, et al. Improving timeliness of antibiotic delivery for patients with fever and suspected neutropenia in a pediatric emergency department. Pediatrics 2012;130:e201‐10. - PubMed
Walker 1998 {published data only}
    1. Walker SE. Physicians' acceptance of a preformatted pharmacy intervention chart note in a community hospital antibiotic step down program. Journal of Pharmacy Technology 1998;14:141‐5.
Wang 2014 {published data only}
    1. Wang HY, Chiu CH, Huang CT, Cheng CW, Lin YJ, Hsu YJ, et al. Blood culture‐guided de‐escalation of empirical antimicrobial regimen for critical patients in an online antimicrobial stewardship programme. International Journal of Antimicrobial Agents 2014;44(6):520‐7. - PubMed
Wax 2007 {published data only}
    1. Wax DB, Beilin Y, Levin M, Chadha N, Krol M, Reich DL. The effect of an interactive visual reminder in an anesthesia information management system on timeliness of prophylactic antibiotic administration. Anesthesia & Analgesia 2007;104:1462‐6. - PubMed
Weinberg 2001 {published data only}
    1. Weinberg M, Fuentes JM, Ruiz A I, Lozano FW, Angel E, Gaitan H, et al. Reducing infections among women undergoing cesarean section in Colombia by means of continuous quality improvement methods. Archives of Internal Medicine 2001;161(19):2357‐65. - PubMed
Weiner 2009 {published data only}
    1. Weiner SG, Brown SF, Goetz JD, Webber CA. Weekly E‐mail reminders influence emergency physician behavior: a case study using the Joint Commission and Centers for Medicare and Medicaid Services Pneumonia Guidelines. Academic Emergency Medicine 2009;16:626‐31. - PubMed
Weiss 2013 {published data only}
    1. Weiss CH, Dibardino D, Rho J, Sung N, Collander B, Wunderink RG. A clinical trial comparing physician prompting with an unprompted automated electronic checklist to reduce empirical antibiotic utilization. Critical Care Medicine 2013;41:2563‐9. - PMC - PubMed
    1. Weiss CH, Persell SD, Wunderink RG, Baker DW. Empiric antibiotic, mechanical ventilation, and central venous catheter duration as potential factors mediating the effect of a checklist prompting intervention on mortality: an exploratory analysis. BMC Health Services Research 2012;12:198. [DOI: 10.1186/1472-6963-12-198] - DOI - PMC - PubMed
Welker 2008 {published data only}
    1. Welker JA, Huston M, McCue JD. Antibiotic timing and errors in diagnosing pneumonia. Archives of Internal Medicine 2008;168:351‐6. - PubMed
Wenisch 2014 {published data only}
    1. Wenisch JM, Equiluz‐Bruck S, Fudel M, Reiter I, Schmid A, Singer E, et al. Decreasing Clostridium difficile infections by an antimicrobial stewardship program that reduces moxifloxacin use. Antimicrobial Agents and Chemotherapy 2014;58 (9):5079‐83. - PMC - PubMed
Willemsen 2010 {published data only}
    1. Willemsen I, Cooper B, Buitenen C, Winters M, Andriesse G, Kluytmans J. Improving quinolone use in hospitals by using a bundle of interventions in an interrupted time series analysis. Antimicrobial Agents and Chemotherapy 2010;54:3763‐9. - PMC - PubMed
Wilson 1991 {published data only}
    1. Wilson J, Gordon A, French S, Aslam M. The effectiveness of prescribers newsletters in influencing hospital drug expenditure. Hospital Pharmacy Practice 1991;1:33‐8.
Winters 2010 {published data only}
    1. Winters BD, Thiemann DR, Brotman DJ. Impact of a restrictive antimicrobial policy on the process and timing of antimicrobial administration. Journal of Hospital Medicine 2010;5:E41‐5. - PubMed
Wishaupt 2011 {published data only}
    1. Wishaupt JO, Russcher A, Smeets LC, Versteegh FG, Hartwig NG. Clinical impact of RT‐PCR for pediatric acute respiratory infections: a controlled clinical trial. Pediatrics 2011;128:e1113‐20. - PubMed
Woodward 1987 {published data only}
    1. Woodward RS, Medoff G, Smith MD, Gray JLI. Antibiotic cost savings from formulary restrictions and physician monitoring in a medical‐school‐affiliated hospital. American Journal of Medicine 1987;83(5):817‐23. - PubMed
Wyatt 1998 {published data only}
    1. Wyatt JC, Paterson‐Brown S, Johanson R, Altman DG, Bradburn MJ, Fisk NM. Randomised trial of educational visits to enhance use of systematic reviews in 25 obstetric units. BMJ 1998;317(7165):1041‐6. - PMC - PubMed
Yealy 2005 {published data only}
    1. Hsu DJ, Stone RA, Obrosky DS, Yealy DM, Meehan TP, Fine JM, et al. Predictors of timely antibiotic administration for patients hospitalized with community‐acquired pneumonia from the cluster‐randomized EDCAP trial. American Journal of the Medical Sciences 2010;339:307‐13. - PMC - PubMed
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Yeo 2012 {published data only}
    1. Yeo CL, Chan DSG, Earnest A, Wu TS, Yeoh SF, Lim R, et al. Prospective audit and feedback on antibiotic prescription in an adult hematology‐oncology unit in Singapore. European Journal of Clinical Microbiology & Infectious Diseases 2012;31:583‐90. - PubMed
Yong 2010 {published data only}
    1. Yong MK, Buising KL, Cheng AC, Thursky KA. Improved susceptibility of Gram‐negative bacteria in an intensive care unit following implementation of a computerized antibiotic decision support system. Journal of Antimicrobial Chemotherapy 2010;65:1062‐9. - PubMed
Yoon 2014 {published data only}
    1. Yoon YK, Yang KS, Lee SE, Kim HJ, Sohn JW, Kim MJ. Effects of Group 1 versus Group 2 carbapenems on the susceptibility of Acinetobacter baumannii to carbapenems: A before and after intervention study of carbapenem‐use stewardship. PLoS ONE 2014;9(6):e99101. - PMC - PubMed
Young 1985 {published data only}
    1. Young EJ, Sewell CM, Koza MA, Clarridge JE. Antibiotic resistance patterns during aminoglycoside restriction. American Journal of Medical Science 1985;290(6):223‐7. - PubMed
Yu 2014 {published data only}
    1. Yu K, Rho J, Morcos M, Nomura J, Kaplan D, Sakamoto K, et al. Evaluation of dedicated infectious diseases pharmacists on antimicrobial stewardship teams. American Journal of Health‐System Pharmacy 2014;71:1019‐28. - PubMed
Zanetti 2003 {published data only}
    1. Zanetti G, Flanagan HL Jr, Cohn LH, Giardina R, Platt R. Improvement of intraoperative antibiotic prophylaxis in prolonged cardiac surgery by automated alerts in the operating room. Infection Control and Hospital Epidemiology 2003;24:13‐6. - PubMed

References to studies excluded from this review

Ahronheim 2000 {published data only}
    1. Ahronheim JC, Morrison RS, Morris J, Baskin S, Meier DE. Palliative care in advanced dementia: a randomized controlled trial and descriptive analysis. Journal of Palliative Medicine 2000; Vol. 3, issue 3:265‐73. - PubMed
Bruno‐Murtha 2005 {published data only}
    1. Bruno‐Murtha LA, Brusch J, Bor D, Li W, Zucker D. A pilot study of antibiotic cycling in the community hospital setting. Infection Control and Hospital Epidemiology 2005;26:81‐7. - PubMed
Burke 1997 {published data only}
    1. Burke CE, Piper J, Holloway W. Order form for restricting vancomycin prescribing. American Journal of Health‐System Pharmacy 1997;54(16):1893, 1897. - PubMed
Cook 2006 {published data only}
    1. Cook PP, Catrou P, Gooch M, Holbert D. Effect of reduction in ciprofloxacin use on prevalence of meticillin‐resistant Staphylococcus aureus rates within individual units of a tertiary care hospital. Journal of Hospital Infection 2006;64:348‐51. - PubMed
Crist 1987 {published data only}
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Cunningham 2008 {published data only}
    1. Cunningham TR, Geller ES, Clarke SW. Impact of electronic prescribing in a hospital setting: a process‐focused evaluation. International Journal of Medical Informatics 2008;77:546‐54. - PubMed
Dellinger 2005 {published data only}
    1. Dellinger EP, Hausmann SM, Bratzler DW, Johnson RM, Daniel DM, Bunt KM, et al. Hospitals collaborate to decrease surgical site infections. American Journal of Surgery 2005;190(1):9‐15. - PubMed
Destache 1990 {published data only}
    1. Destache CJ, Meyer SK, Bittner MJ, Hermann KG. Impact of a clinical pharmacokinetic service on patients treated with aminoglycosides: a cost‐benefit analysis. Therapeutic Drug Monitoring 1990;12(5):419‐26. - PubMed
Ehrenkranz 1992 {published data only}
    1. Ehrenkranz NJ, Nerenberg DE, Shultz JM, Slater KC. Intervention to discontinue parenteral antimicrobial therapy in patients hospitalized with pulmonary infections: effect on shortening patient stay. Infection Control and Hospital Epidemiology 1992;13(1):21‐32. - PubMed
Ehrenkranz 1993 {published data only}
    1. Ehrenkranz NJ, Nerenberg DE, Slater KC, Shultz JM. Intervention to discontinue parenteral antimicrobial therapy in hospitalized patients with urinary tract infection, skin and soft tissue infection, or no evident infection. Infection Control and Hospital Epidemiology 1993;14(9):517‐22. - PubMed
Evans 1994 {published data only}
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Foy 2004 {published data only}
    1. Foy R, Penney GC, Grimshaw JM, Ramsay CR, Walker AE, Maclennan G, et al. A randomised controlled trial of a tailored multifaceted strategy to promote implementation of a clinical guideline on induced abortion care. BJOG: An International Journal of Obstetrics & Gynaecology 2004;111:726‐33. - PubMed
Garcia‐San Miguel 2014 {published data only}
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Gerding 1991 {published data only}
    1. Gerding DN, Larson TA, Hughes RA, Weiler M, Shanholtzer C, Peterson LR. Aminoglycoside resistance and aminoglycoside usage: ten years of experience in one hospital. Antimicrobial Agents and Chemotherapy 1991;35(7):1284‐90. - PMC - PubMed
Kolar 1999 {published data only}
    1. Kolar M, Latal T. Implementation of a practical antibiotic policy in the Czech Republic. Infection Control and Hospital Epidemiology 1999;20(6):440‐3. - PubMed
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Lan 2003 {published data only}
    1. Lan CK, Hsueh PR, Wong WW, Fung CP, Lau YT, Yeung JY, et al. Association of antibiotic utilization measures and reduced incidence of infections with extended‐spectrum beta‐lactamase‐producing organisms. Journal of Microbiology, Immunology, and Infection 2003;36(3):182‐6. - PubMed
Lee 2004 {published data only}
    1. Lee SO, Lee ES, Park SY, Kim SY, Seo YH, Cho YK. Reduced use of third‐generation cephalosporins decreases the acquisition of extended‐spectrum beta‐lactamase‐producing Klebsiella pneumoniae. Infection Control and Hospital Epidemiology 2004;25(10):832‐7. - PubMed
MacCosbe 1985 {published data only}
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Marrie 2000 {published data only}
    1. Marrie TJ, Lau CY, Wheeler SL, Wong CJ, Vandervoort MK, Feagan BG. A controlled trial of a critical pathway for treatment of community‐acquired pneumonia. CAPITAL Study Investigators. Community‐Acquired Pneumonia Intervention Trial Assessing Levofloxacin. JAMA 2000;283(6):749‐55. - PubMed
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Martin 2005 {published data only}
    1. Martin C, Ofotokun I, Rapp R, Empey K, Armitstead J, Pomeroy C, et al. Results of an antimicrobial control program at a university hospital. American Journal of Health‐System Pharmacy 2005;62(7):732‐8. - PubMed
McGregor 2006 {published data only}
    1. McGregor JC, Weekes E, Forrest GN, Standiford HC, Perencevich EN, Furuno JP, et al. Impact of a computerized clinical decision support system on reducing inappropriate antimicrobial use: a randomized controlled trial. Journal of the American Medical Informatics Association 2006;13(4):378‐84. - PMC - PubMed
Nagao 2010 {published data only}
    1. Nagao M, Iinuma Y, Saito T, Matsumura Y, Shirano M, Matsushima A, et al. Close cooperation between infectious disease physicians and attending physicians can result in better management and outcome for patients with Staphylococcus aureus bacteraemia. Clinical Microbiology & Infection 2010;16:1783‐8. - PubMed
Naughton 2001 {published data only}
    1. Naughton BJ, Mylotte JM, Ramadan F, Karuza J, Priore RL. Antibiotic use, hospital admissions, and mortality before and after implementing guidelines for nursing home‐acquired pneumonia. Journal of the American Geriatrics Society 2001;49:1020‐4. - PubMed
Pastel 1992 {published data only}
    1. Pastel DA, Chang S, Nessim S, Shane R, Morgan MA. Department of pharmacy‐initiated program for streamlining empirical antibiotic therapy. Hospital Pharmacy 1992;27(7):596‐603, 614. - PubMed
Ronning 1998 {published data only}
    1. Ronning OM, Guldvog B. Stroke unit versus general medical wards, II: neurological deficits and activities of daily living: a quasi‐randomized controlled trial. Stroke 1998;29(3):586‐90. - PubMed
Sanazaro 1978 {published data only}
    1. Sanazaro PJ, Worth RM. Concurrent quality assurance in hospital care. Report of a study by private initiative in PSRO. New England Journal of Medicine 1978; Vol. 298, issue 21:1171‐7. - PubMed
Takahashi 2010 {published data only}
    1. Takahashi Y, Takesue Y, Nakajima K, Ichiki K, Wada Y, Tsuchida T, et al. Implementation of a hospital‐wide project for appropriate antimicrobial prophylaxis. Journal of Infection and Chemotherapy 2010;16:418‐23. - PubMed
Thomas 2002 {published data only}
    1. Thomas AR, Cieslak PR, Strausbaugh LJ, Fleming DW. Effectiveness of pharmacy policies designed to limit inappropriate vancomycin use: a population‐based assessment. Infection Control and Hospital Epidemiology 2002;23(11):683‐8. - PubMed
Tiley 2003 {published data only}
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References to other published versions of this review

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