Abstract
Introduction
In the United States, most antibiotics are prescribed in ambulatory settings. Human factors engineering, which explores interactions between people and the place where they work, has successfully improved quality of care. However, human factors engineering models have not been explored to frame what is known about ambulatory antibiotic stewardship (AS) interventions and barriers and facilitators to their implementation.
Methods
We conducted a systematic review and searched OVID MEDLINE, Embase, Scopus, Web of Science, and CINAHL to identify controlled interventions and qualitative studies of ambulatory AS and determine whether and how they incorporated principles from a human factors engineering model, the Systems Engineering Initiative for Patient Safety 2.0 model. This model describes how a work system (ambulatory clinic) contributes to a process (antibiotic prescribing) that leads to outcomes. The work system consists of 5 components – tools and technology, organization, person, tasks, and environment – within an external environment.
Results
Of 1288 abstracts initially identified, 42 quantitative studies and 17 qualitative studies met inclusion criteria. Effective interventions focused on tools and technology (e.g., clinical decision support, point-of-care testing), the person (e.g., clinician education), organization (e.g., audit and feedback, academic detailing), tasks (e.g., delayed antibiotic prescribing), the environment (e.g., commitment posters), and the external environment (media campaigns). Studies have not focused on clinic-wide approaches to AS.
Conclusions
A human factors engineering approach suggests that investigating the role of the clinic’s processes or physical layout, or external pressures’ role in antibiotic prescribing may be a promising way to improve ambulatory AS.
INTRODUCTION
Antibiotic resistance is increasing worldwide, largely driven by excessive antibiotic use.1–3 In the United States, antibiotic resistance contributes to 23,000 deaths annually and $20 billion in excess healthcare costs.4 Antibiotic stewardship (AS) minimizes the development of resistance as well as the risk of harm from antibiotic-associated adverse events by ensuring that only patients who need antibiotics get them, and that each patient who needs antibiotics receives the right antibiotic at the right time at the right dose for the right duration.5
While implementation of hospital-based AS teams have been recommended for a decade,6 the majority of human antibiotic expenditures (62%) and use occur in the ambulatory setting.7 At least 30% of these prescriptions are inappropriate.8 Reducing inappropriate ambulatory antibiotic prescribing is essential to decreasing antibiotic resistance.9,10
Human factors engineering is the “scientific discipline concerned with understanding interactions among humans and other elements of a system.”11,12 According to a healthcare-specific human factors engineering model, the Systems Engineering Initiative in Patient Safety (SEIPS 2.0) model,13 the characteristics of a workplace (e.g., an ambulatory clinic) interact in a work system (comprised of person(s), tools and technologies, the organization, tasks, and the physical environment, within a larger external environment); this work system impacts processes such as antibiotic prescribing, which influence outcomes.13
While human factors engineering approaches have been occasionally used in ambulatory clinics to improve patient safety and quality of care,14–18 human factors engineering approaches and models have not been applied to understanding ambulatory AS. We performed a systematic review because human factors engineering approaches describing the clinic’s work system could explain influences on antibiotic prescribing and lead to more effective AS interventions. For example, human factors engineering could explain how clinic characteristics such as the ease with which clinicians adapt the electronic health record (EHR) could enhance the intervention’s success. We used the SEIPS 2.0 model13 to frame what is known about effective ambulatory AS interventions, and identify barriers and facilitators to successful implementation of ambulatory AS interventions.
METHODS
Literature Search and Inclusion Criteria
We included quantitative studies to learn whether ambulatory AS interventions were efficacious and qualitative studies to describe barriers and facilitators to AS. We defined ambulatory settings as outpatient practices or offices in which patients came and left on their own (excluding dentistry and emergency medicine practices). We searched the OVID MEDLINE, Embase, Scopus, Web of Science, and CINAHL databases through November 7th, 2016 using a predetermined set of search terms (Appendix). We identified additional titles from the Cochrane database as well as from the citations in identified articles. Citation titles and abstracts were screened independently by two reviewers (S.C.K. and P.D.T.), and full texts were retrieved for all potentially relevant studies. Duplicate studies were removed.
Studies were limited to English-language human studies of antibiotic prescribing interventions or qualitative studies seeking to understand antibiotic prescribing practices. Quantitative and qualitative studies were assessed by two reviewers (S.C.K. and P.D.T.) to determine if they evaluated AS interventions conducted in ambulatory clinics. We considered AS interventions any intervention that sought to improve the appropriate use of antibiotics in an ambulatory clinic. We included studies that measured the application of an intervention targeting antibiotic prescriptions, described the factors that influence antibiotic prescribing, or explained the process of implementing approaches to improve antibiotic prescribing. For quantitative studies, we a priori only included studies with rigorous designs: randomized controlled trials (RCTs) or quasi-experimental studies using stepped wedge or interrupted time-series approaches. Qualitative studies were included if they described the context in which antibiotic prescribing decisions were made, or the context, barriers, or facilitators of AS interventions. Any disagreements about study inclusion were discussed until consensus was achieved.
SEIPS 2.0 Model and Data Extraction
Data for studies meeting inclusion criteria were abstracted using components of the SEIPS 2.0 work system model.13,19 The SEIPS 2.0 work system includes five components—(1) person(s), (2) tools and technologies, (3) organization, (4) tasks, and (5) physical environment—within a wider external environment. The work system centers around the person(s), including healthcare professionals and the patient and family and their individual characteristics (e.g., age, education, etc.) and connections between individuals (e.g., a patient-clinician relationship).13 Tools and technologies include objects that people use to do work, such as information technologies, educational materials, medical devices, testing equipment, and physical tools. Organization refers to the structures that organize clinic time, space, resources, and activities, including staff member roles. Tasks are specific actions (e.g., placing an electronic order), and have qualities such as difficulty, complexity, ambiguity, variety, and sequence. The physical environment includes the clinic’s physical space. The work system lies within a larger external regulatory and cultural environment, including societal, economic, and policy forces that impact a clinic.13
We used these work system components to organize aspects of the interventions and the context of AS, and to understand which processes and outcomes were addressed by AS interventions. Our aim in using this approach was to identify how aspects of the clinic work system could affect AS intervention successes. We evaluated identified sources and recorded study design and aspects of the studies that could be interpreted in the context of the SEIPS 2.0 model. We also described how measures and outcomes of the studies could be interpreted in the context of the SEIPS 2.0 work system.
RESULTS
Search Results
The search identified 1288 abstracts (Figure 1). Four additional studies meeting inclusion criteria identified through knowledge of the literature were added based on their relevance to the work. Ultimately, 42 quantitative and 17 qualitative articles met the eligibility criteria, with one study considered both quantitative and qualitative.19 Fourteen of the quantitative studies were RCTs,20–33 one was a randomized crossover trial,34 two were pragmatic RCTs,35,36 14 were cluster randomized trials,37–48 two were pragmatic cluster-randomized trials,49,50 and nine were quasiexperimental interrupted time-series studies.19,51–58
Figure 1.

Flow chart demonstrating inclusion of articles in the review. Rigorously designed quantitative studies of ambulatory antibiotic stewardship interventions (randomized controlled trials and quasi-experimental studies with stepped wedge and interrupted time-series approaches) as well as qualitative studies describing barriers and facilitators to ambulatory antibiotic stewardship were included. Databases were searched through November 7th, 2016, with additional titles added based on knowledge of the literature and relevance to the work.
Of the qualitative studies, three were follow-up studies to prior quantitative work19,59,60 (one of which had been described in the quantitative review).19,38 Eight used semi-structured interviews61–68 and one used focus groups.72 One combined interviews and focus groups69 and two involved surveys.70,71 A single study focused on written physician self-reflection, prompting them to review the medical charts of patients.72 Finally, one study used a “think-aloud” approach where physicians commented on their inner thought processes.73
AS Interventions and the SEIPS 2.0 Work System13
Table 1, Appendix Table 1, and Figure 2 describe how aspects of included studies fit into components of the clinic work system.13 [Insert Table 1]. Appendix Table 2 describes the processes and outcomes used in each included study.
Table 1.
Aspects of ambulatory antimicrobial stewardship interventions as applied to components of the ambulatory work system, SEIPS 2.0.13 Studies described include rigorously designed quantitative and qualitative studies describing antibiotic stewardship interventions and the context around antibiotic prescribing decisions, included through November 7, 2016.
| Tools / Technology Components |
Person(s) Components | Organizational Components | Task Components | Physical Environment Components |
External Environment Components |
|---|---|---|---|---|---|
|
|
|
|
|
Abbreviations: SEIPS: Systems Engineering In Patient Safety; PCP: primary care provider; CDSS: clinical decision support system; POC: point of care; ARI: acute respiratory infection; EHR: electronic health record; CDC: Centers for Disease Control and Prevention; GP: general practitioner; CRP: C-reactive protein; ID: infectious diseases; PCR: polymerase chain reaction
Figure 2.

Legend: Adaptation of the Systems Engineering Initiative for Patient Safety (SEIPS) 2.0 model of the healthcare work system to approaches taken in the literature to improve antibiotic stewardship in the ambulatory setting.
Tools and Technology
Tools and technologies include objects and technologies that people use to do work. AS interventions incorporating tools and technologies included clinical decision support systems (CDSS), interventions based in EHRs, educational tools (e.g., newsletters, booklets, videotapes, etc.), AS messaging tools (e.g., magnets, lapel pins, etc.), and point-of-care (POC) testing.
CDSS tools and other EHR-based interventions were frequent and often effective. Highlighting several CDSS tools, a CDSS incorporated into an EHR encounter template decreased acute respiratory infection (ARI) antibiotic prescriptions from 43% to 38% (versus 40% to 39% in control groups).41 An RCT of a computerized patient flow manager with evidence-based prompts decreased antibiotic prescriptions for acute otitis media by 34%.32,74
EHR-based tools have incorporated behavioral interventions. In a 2x2x2 randomized factorial study comparing accountable justification (providing a written explanation for prescribing non-indicated antibiotics) and suggested alternatives (pop-up messages with education and non-antibiotic alternatives), the suggested alternatives arm was associated with decreased antibiotic prescriptions for ARIs.20 In a larger cluster-randomized trial, suggested alternatives did not decrease antibiotic prescription, but accountable justification decreased inappropriate antibiotic prescribing (23% to 5%).43
However, the context in which electronic tools were deployed impacted their implementation. Factors associated with unsuccessful incorporation of CDSS tools and EHR technologies into clinics included non-intuitive tools, need for additional software,51 computers not being available in examination rooms, and slow internet connectivity.19 CDSS tools needed to be used to have an effect: in a cluster-randomized trial, EHR-integrated CDSS did not impact antibiotic prescribing, but the CDSS was used in only 6% of intervention clinic visits.75
The effect of educational tools was mixed. Educational booklets (e.g., on self-care for respiratory infections, potential harms of antibiotics, and other topics) were developed with the goals of assisting patients with understanding harms associated with unnecessary antibiotic use and supporting clinicians with antibiotic prescribing.59,66 As a broader intervention including physician feedback, mailing brochures to parents of children successfully decreased community-wide antibiotic use by 4.6% among those aged 2-4 years and by 6.7% among those aged 4-5 years.42 However, in another study involving mailed patient and clinician education, antibiotic use did not decrease.55 In addition, in a trial of patient educational materials including a letter from the medical director along with pamphlets compared (1) materials mailed to patients and to office practices, (2) pamphlets mailed to offices only, and (3) usual care on antibiotic prescription for acute bronchitis.56 Only the full intervention sites showed a decline in antibiotic prescriptions for acute bronchitis visits, from 74% to 48%.56
Evidence was similarly mixed regarding the impact of multi-faceted educational tool bundles. In a cluster-randomized trial in 16 Massachusetts communities, clinicians were given tools with AS messages (i.e., stickers, lapel pins, otoscope insufflators), bimonthly newsletters regarding AS, and prescription pads with written recommendations for symptomatic treatment of viral ARIs.46,53 Parents of young children were also mailed brochures and advertisements were placed in child care centers and pharmacies.46 While there was no difference in ARI antibiotic prescribing in children <2 years, a 5% decrease in children 2-3 years and a 7% decrease in children 4-5 years was observed.46 In an additional cluster-randomized trial, a multifaceted intervention (educational information at pharmacies and clinics, patient mailings, clinic posters, refrigerator magnets, flip charts, patient-initiated chart documentation tools, and CDSS tools) resulted in a decrease in antibiotic prescriptions among children <6 years.37 Another multifaceted intervention (CDSS, clinician education, audit and feedback, and patient education brochures) also led to decreases in the percentage of adolescents and adults prescribed antibiotics for ARIs at CDSS sites (decreased 12%) versus control sites (increased 1%) with no impact on 30-day return visits.40
Interventions involving tools for patient and family education were not always successful. An intervention including mailed information and guideline distribution did not decrease antibiotic use among elderly patients with ARIs.57 Meanwhile, providing patients with an educational pamphlet and videotape of their pediatricians did not decrease the number of viral ARI visits, antibiotic prescriptions for acute otitis media or sinusitis, or total antibiotic prescriptions.27 Patient characteristics such as older age and the need to open the pamphlet or view the videotapes may have made these interventions less effective.
Other studies focused on POC testing as a tool. C-reactive protein (CRP) POC testing, which may perform better than clinical symptoms and signs in predicting the diagnosis of pneumonia52 but decreases clinician confidence in reducing antibiotic prescribing and decreases patient satisfaction.59 In a study of POC CRP testing availability, antibiotic prescription improved,49 but on follow-up 2-3 years later, POC CRP testing was only performed in 4% of eligible patient visits.50 POC tests have also been criticized for their short shelf life, need for quality control testing, and difficulties linking the test result to the EHR.76 These factors may have made the tools more difficult to incorporate into practice and limited their effectiveness.
Person
The person component of the SEIPS 2.0 work system describes individual characteristics and relationships between individuals. However, characteristics and perspectives of other clinic staff members such as medical assistants, nurses, and front desk staff were not described.
Patients and Families
Patient factors like symptoms and comorbidities influence whether a clinician would prescribe antibiotics.19,61,66 Patient and family factors such as education, knowledge of antibiotics, or trust in their physician decreased requests for antibiotics.35,67,70
Clinicians
Clinician training, particularly focusing on communication training, problem-solving strategies, and peer-review, was also studied. In an RCT, French general practitioners were randomized to a day-long seminar focusing on problem-solving strategies after all attended a two-day seminar on evidence-based ARI management.29 The intervention group sustained a decrease in the proportion of antibiotics prescribed over 30 months.29 General practitioners who attended a training session or received in-office instruction along with clinician-specific feedback increased adherence to community-acquired pneumonia guidelines.45 A workshop including peer-reviews of transcripts of interactions with standardized patients reduced antibiotic prescriptions from 54% to 27%,49 sustained for 2-3 years.50
Clinician and Patient Relationships
Relationships between individuals are an important part of the ambulatory work system.13 Some physicians think that patients want antibiotics,61 and prescribe antibiotics to meet perceived patient expectations.68 Physicians may also believe that patients want something (i.e., an antibiotic prescription) in exchange for taking off work and paying co-pays.63
Organization
The organization refers to the structures and roles that organize a clinic. Characteristics of the clinic, roles of clinic members, and the larger organizations in which clinics operate were explored through investigating roles of clinic team members, comparing clinicians to peers, and learning how clinic structures allow clinician education or improve communication.
Few studies involved changing roles of non-clinician staff members to impact AS. Only one study included a non-clinician staff member in an educational intervention, and the role of this person was not specified.51 In a qualitative study, clinicians suggested using nurses to perform pre-visit triage and education.71 In POC testing interventions, participants found that it was unclear which staff members to train in POC testing, as various organizational roles performed the test in different clinics.76,77
Audit and feedback interventions, where clinicians are compared to others, have had success.20,48 In a Canadian RCT where clinicians were mailed educational information or prescribing feedback, the feedback group was more likely to use first-line antibiotic prescriptions.21 In a cluster-randomized trial, comparing clinicians with top performers (those who seldom prescribe antibiotics inappropriately) decreased inappropriate prescriptions from 20% to 4%.43 In a RCT, antibiotic use decreased among providers who received a letter from England’s Chief Medical Officer saying they were prescribing more antibiotics than 80% of local practices.22 An RCT found that the combination of clinician education and audit and feedback decreased antibiotic prescribing overall and broad-spectrum prescribing in particular.38
However, audit and feedback may not be universally successful. In the above RCT,38 after the termination of audit and feedback, prescribing of broad-spectrum antibiotics returned to a level above baseline.39 In a follow-up qualitative study, some clinicians expressed skepticism and discounted the reports.60 Furthermore, in a recent RCT of high-prescribing physicians across Switzerland, receiving letters and an online log-in code with information about antibiotic prescribing did not impact antibiotic prescribing over two years.36 Only 11% of physicians in the intervention group viewed their prescribing data.36 Similarly, a cluster-randomized trial of an audit and feedback dashboard led to no difference in antibiotic prescribing for ARI visits,78 but only 28% of intervention-group physicians used the dashboard. These clinicians had a lower ARI antibiotic prescribing rate (42% vs 50%).78
Organizational structures could pose barriers to AS. Clinic visits were often too brief to discuss guidelines with patients.63,69 If patients saw multiple clinicians in a practice with different prescribing practices, patients may expect to receive antibiotics.63,69 Many clinics did not have protected time for group education.63 However, in practices where physicians discussed AS guidelines, outcomes improved.52,46
If clinics had protected time for group education, academic detailing, where an expert visits a practice to discuss AS,51,64 was successful.55 In a study comparing (1) office-based patient education, (2) office- and home-based patient and clinician education (practice profiling, setting clinic goals, and academic detailing) and (3) usual care, full intervention sites had a substantial decline in antibiotic prescriptions for acute bronchitis (74% to 48%), while the control and limited intervention sites did not.56
Tasks
Tasks describe specific actions and their characteristics. Clinicians pick particular words when describing physical exam findings to patients or perform a thorough physical exam to explain to patients why they were not prescribing antibiotics.61,66,73
In delayed prescription strategies, the clinician gives the patient a prescription and leaves it up to the patient whether to fill it after a specified time or with worsened symptoms. Patients with acute uncomplicated ARIs were randomized to (1) deciding to fill the prescription after two days, (2) returning to the clinic after two days for a prescription, (3) no prescription, or (4) immediate prescription.35 Patient satisfaction was similar in all groups, and antibiotic use and belief in antibiotic effectiveness was lower in all groups compared to the immediate prescription group.35
Physical Environment
The physical environment refers to the clinic’s layout. Most physical environment-based interventions used posters.24,38,46,59,60 By themselves, posters about avoiding antibiotics for “chest colds” did not decrease antibiotic prescription for acute bronchitis.56 However, visible signed commitments about avoiding unnecessary antibiotics decreased unnecessary antibiotic prescribing by up to 20%.31 Studies did not discuss optimizing the placement of these posters.37,45,46,53,56,57
External Environment
The larger external environment includes guidelines and societal, economic, and policy forces that impact a clinic. External guidelines were not always used because they were sometimes difficult to locate,63,64,72 too long,64 or not seen as relevant.64 Some physicians did not trust guidelines, wondering whether they were intended to save money instead of improving care.64
Media campaigns reinforced what clinicians conveyed.66 A Colorado-wide campaign of billboards, bus signs, radio advertisements, and newspaper op-eds decreased population-wide antibiotic dispenses.53,57 Advertisements in child care centers and pharmacies also reduced antibiotic use.46 In another community-level study, interventions including news releases, community meetings, and presentations at health fairs decreased antibiotic prescriptions.37 In an Italian study, region-wide campaign materials (posters, brochures, and local media advertisements) and a doctor and pharmacist newsletter decreased antibiotic prescribing 4%.58
DISCUSSION
Human factors engineering approaches have only recently been used in ambulatory clinics to describe defects in testing,14 apply new EHR technologies,15,18 and improve clinic workflows.16,17 Our review is the first to incorporate a human factors engineering approach to understanding ambulatory AS.
In the SEIPS 2.0 work system, tools and technologies refer to objects and technologies. Tools and technologies used in ambulatory AS interventions have included CDSS and EHR-based interventions, educational materials, and POC testing. CDSS and EHR-based and educational materials improved AS but only if they were used. POC tools such as CRP testing impacted AS, but many clinicians stopped using the POC tests over time. Human factors engineering would suggest that to make these tools more effective researchers should make them easier to use.
The person component of the work system includes individual characteristics and relationships between individuals. In particular, clinician communication training had a sustained positive impact on AS, and interventions aimed at educating patients and families also showed a positive impact on AS. However, while clinicians have mentioned the potential impact of other members of the healthcare team, characteristics of other healthcare team members have not been studied. Human factors engineering would suggest that the role of other members of the healthcare team in AS interventions should be studied, and these team members should be engaged.
Few studies focused on the organization component of the work system model, or the structures and roles that organize a clinic. Audit and feedback and academic detailing had a positive impact on AS. However, we know little about the role of non-clinicians in AS. Engagement of the entire ambulatory team has the potential to send a consistent message about appropriate antibiotic prescribing.68 Human factors engineering would suggest research exploring the roles of clinic staff and clinic flow in an intervention’s effectiveness.
Similarly, few interventions focused on the work system component of tasks, or specific actions and their characteristics, although delayed prescription strategies were promising. Few interventions focused on the impact of the physical environment of the clinic on antibiotic prescription. However, clinic posters with signed commitments advocating AS positively impacted AS. Human factors engineering would suggest an investigation into the role of the location of clinic posters and other elements of the physical environment, as well as qualities of tasks related to antibiotic prescription, on AS interventions.
Finally, the work system occurs within the external regulatory and cultural environment. Several interventions incorporated the external environment, showing that media-based interventions could improve AS at a community level, and showing that external guidelines needed to be accessible to clinicians and trusted by clinicians. The role of the external environment in the form of external pressures on AS interventions such as patient satisfaction-based reimbursement has not been fully examined and should be a focus of future research.
Our review has several limitations. We only included well-controlled quantitative studies and may have missed other domains if they were only targeted in uncontrolled studies. We did not assess for publication bias. Finally, our findings are more applicable to ARIs, the focus of most studies, as we were unable to identify many high-quality studies that implemented AS for other conditions (e.g., urinary tract infections, cellulitis, etc.).
Evidence-based AS interventions impact different portions of the ambulatory work system, and using a human factors engineering approach may facilitate the intervention’s success. However, interventions did not typically engage all clinic staff in the implementation, a model that has led to successes in patient safety and quality improvement.79–84 Few interventions have accounted for physical environment or task characteristics in implementing interventions. Future work in ambulatory AS should address the entire work system in which the intervention is implemented. Such work system interventions, if rigorously evaluated, may have greater potential than isolated interventions to improve the effectiveness of ambulatory AS.
Supplementary Material
Acknowledgments
We gratefully acknowledge the support of Maria Trusky, MLS, for her assistance in extracting the articles. We also appreciate the assistance of Kathleen Speck, MPH, for assistance in formatting the tables.
Funding statement: This work was supported by the Agency for Healthcare Research and Quality (AHRQ) (HHSP233201500020I/HHSP23337003T). The findings and conclusions in this document are those of the authors, who are responsible for its content, and do not necessarily represent the views of AHRQ. No statement in this report should be construed as an official position of AHRQ or of the U.S. Department of Health and Human Services. SCK receives funding from the National Center for Advancing Translational Sciences/Johns Hopkins Institute for Clinical and Translational research, KL2 Award KL2TR001077.
Footnotes
Conflicting and Competing Interests: None reported
Note to NIH – Please include: The published version of this article can be accessed on the Journal of the American Board of Family Medicine website at: http://jabfm.org/content/31/3/417.full
Contributor Information
Sara C. Keller, Assistant Professor, Division of Infectious Diseases, Johns Hopkins University School of Medicine, Baltimore, MD.
Pranita D. Tamma, Assistant Professor, Division of Infectious Diseases, Johns Hopkins University School of Medicine, Baltimore, MD.
Sara E. Cosgrove, Professor, Division of Infectious Diseases, Johns Hopkins University School of Medicine, Baltimore, MD.
Melissa A. Miller, Medical Officer, Division of Healthcare-Associated Infections, Agency for Healthcare Research and Quality, Rockville, MD.
Heather Sateia, Instructor, Division of General Internal Medicine, Johns Hopkins University School of Medicine, Baltimore, MD.
Julie Szymczak, Assistant Professor, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA.
Ayse P. Gurses, Associate Professor, Armstrong Institute of Patient Safety and Quality, Johns Hopkins University School of Medicine, Baltimore, MD.
Jeffrey A. Linder, Professor, Division of General Internal Medicine and Geriatrics, Northwestern University Feinberg School of Medicine, Chicago, IL.
References
- 1.Pakyz A, Powell JP, Harpe SE, Johnson C, Edmond M, Polk RE. Diversity of antimicrobial use and resistance in 42 hospitals in the United States. Pharmacotherapy. 2008;28(7):906–12. doi: 10.1592/phco.28.7.906. [DOI] [PubMed] [Google Scholar]
- 2.Pakyz AL, MacDougall C, Oinonen M, Polk RE. Trends in antibacterial use in US academic health centers: 2002 to 2006. Arch Intern Med. 2008;168(20):2254–60. doi: 10.1001/archinte.168.20.2254. [DOI] [PubMed] [Google Scholar]
- 3.Adriaenssens N, Coenen S, Muller A, Vankerckhoven V, Goossens H, Group EP European Surveillance of Antimicrobial Consumption (ESAC): outpatient systemic antimycotic and antifungal use in Europe. J Antimicrob Chemother. 2010;65(4):769–74. doi: 10.1093/jac/dkq023. [DOI] [PubMed] [Google Scholar]
- 4.Centers for Disease Control and Prevention. Antibiotic resistance threats in the United States, 2013. 2013 http://www.cdc.gov/drugresistance/threat-report-2013/ (accessed September 28, 2017).
- 5.The White House. National Action Plan for Combating Antibiotic-Resistant Bacteria. 2015 [Google Scholar]
- 6.Dellit TH, Owens RC, McGowan JE, Jr, 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. 2007;44(2):159–77. doi: 10.1086/510393. [DOI] [PubMed] [Google Scholar]
- 7.Suda KJ, Hicks LA, Roberts RM, Hunkler RJ, Danziger LH. A national evaluation of antibiotic expenditures by healthcare setting in the United States, 2009. J Antimicrob Chemother. 2013;68(3):715–8. doi: 10.1093/jac/dks445. [DOI] [PubMed] [Google Scholar]
- 8.Fleming-Dutra KE, Hersh AL, Shapiro DJ, et al. Prevalence of inappropriate antibiotic prescriptions among US ambulatory care visits, 2010-2011. JAMA. 2016;315(17):1864–73. doi: 10.1001/jama.2016.4151. [DOI] [PubMed] [Google Scholar]
- 9.Nicolle LE, Bradley S, Colgan R, et al. Infectious Diseases Society of America guidelines for the diagnosis and treatment of asymptomatic bacteriuria in adults. Clin Infect Dis. 2005;40(5):643–54. doi: 10.1086/427507. [DOI] [PubMed] [Google Scholar]
- 10.Chow AW, Benninger MS, Brook I, et al. IDSA clinical practice guideline for acute bacterial rhinosinusitis in children and adults. Clin Infect Dis. 2012;54(8):e72–e112. doi: 10.1093/cid/cir1043. [DOI] [PubMed] [Google Scholar]
- 11.Gurses AP, Ozok AA, Pronovost PJ. Time to accelerate integration of human factors and ergonomics in patient safety. BMJ Qual Saf. 2012;21(4):347–51. doi: 10.1136/bmjqs-2011-000421. [DOI] [PubMed] [Google Scholar]
- 12.International Ergonomics Association. Definition and domains of ergonomics. 2017 http://www.iea.cc/whats/ (accessed September 28 2017).
- 13.Holden RJ, Carayon P, Gurses AP, et al. SEIPS 20: a human factors framework for studying and improving the work of healthcare professionals and patients. Ergonomics. 2013;56(11):1669–86. doi: 10.1080/00140139.2013.838643. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Elder NC, McEwen TR, Flach JM, Gallimore JJ. Creating Safety in the Testing Process in Primary Care Offices. In: Henriksen K, Battles JB, Keyes MA, Grady ML, editors. Advances in Patient Safety: New Directions and Alternative Approaches (Vol 2: Culture and Redesign) Rockville MD: 2008. [Google Scholar]
- 15.Asan O. Providers’ perceived facilitators and barriers to EHR screen sharing in outpatient settings. Appl Ergon. 2017;58:301–7. doi: 10.1016/j.apergo.2016.07.005. [DOI] [PubMed] [Google Scholar]
- 16.Patterson ES, Lowry SZ, Ramaiah M, et al. Improving Clinical Workflow in Ambulatory Care: Implemented Recommendations in an Innovation Prototype for the Veteran’s Health Administration. EGEMS (Wash DC) 2015;3(2):1149. doi: 10.13063/2327-9214.1149. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Saleem JJ, Adams S, Frankel RM, Doebbeling BN, Patterson ES. Efficiency strategies for facilitating computerized clinical documentation in ambulatory care. Stud Health Technol Inform. 2013;192:13–7. [PubMed] [Google Scholar]
- 18.van Stiphout F, Zwart-van Rijkom JE, Maggio LA, et al. Task analysis of information technology-mediated medication management in outpatient care. Br J Clin Pharmacol. 2015;80(3):415–24. doi: 10.1111/bcp.12625. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Donabedian A. The quality of care. How can it be assessed? JAMA. 1988;260(12):1743–8. doi: 10.1001/jama.260.12.1743. [DOI] [PubMed] [Google Scholar]
- 20.Litvin CB, Ornstein SM, Wessell AM, Nemeth LS, Nietert PJ. Adoption of a clinical decision support system to promote judicious use of antibiotics for acute respiratory infections in primary care. Int J Med Inform. 2012;81(8):521–6. doi: 10.1016/j.ijmedinf.2012.03.002. [DOI] [PubMed] [Google Scholar]
- 21.Persell SD, Doctor JN, Friedberg MW, et al. Behavioral interventions to reduce inappropriate antibiotic prescribing: a randomized pilot trial. BMC Infect Dis. 2016;16:373. doi: 10.1186/s12879-016-1715-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Hux JE, Melady MP, DeBoer D. Confidential prescriber feedback and education to improve antibiotic use in primary care: a controlled trial. CMAJ. 1999;161(4):388–92. [PMC free article] [PubMed] [Google Scholar]
- 23.Hallsworth M, Chadborn T, Sallis A, et al. Provision of social norm feedback to high prescribers of antibiotics in general practice: a pragmatic national randomised controlled trial. Lancet. 2016;387(10029):1743–52. doi: 10.1016/S0140-6736(16)00215-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Strykowski DF, Nielsen AB, Llor C, Siersma V, Bjerrum L. An intervention with access to C-reactive protein rapid test reduces antibiotic overprescribing in acute exacerbations of chronic bronchitis and COPD. Fam Pract. 2015;32(4):395–400. doi: 10.1093/fampra/cmv020. [DOI] [PubMed] [Google Scholar]
- 25.Foxman B, Valdez RB, Lohr KN, Goldberg GA, Newhouse JP, Brook RH. The effect of cost sharing on the use of antibiotics in ambulatory care: results from a population-based randomized controlled trial. J Chronic Dis. 1987;40(5):429–37. doi: 10.1016/0021-9681(87)90176-7. [DOI] [PubMed] [Google Scholar]
- 26.Long W, Deng X, Zhang Y, Lu G, Xie J, Tang J. Procalcitonin guidance for reduction of antibiotic use in low-risk outpatients with community-acquired pneumonia. Respirology. 2011;16(5):819–24. doi: 10.1111/j.1440-1843.2011.01978.x. [DOI] [PubMed] [Google Scholar]
- 27.Arakaki RY, Strazzula L, Woo E, Kroshinsky D. The impact of dermatology consultation on diagnostic accuracy and antibiotic use among patients with suspected cellulitis seen at outpatient internal medicine offices: a randomized clinical trial. JAMA Dermatol. 2014;150(10):1056–61. doi: 10.1001/jamadermatol.2014.1085. [DOI] [PubMed] [Google Scholar]
- 28.Taylor JA, Kwan-Gett TS, McMahon EM., Jr Effectiveness of a parental educational intervention in reducing antibiotic use in children: a randomized controlled trial. Pediatr Infect Dis J. 2005;24(6):489–93. doi: 10.1097/01.inf.0000164706.91337.5d. [DOI] [PubMed] [Google Scholar]
- 29.Torres FA, Pasarelli I, Cutri A, Ossorio MF, Ferrero F. Impact assessment of a decision rule for using antibiotics in pneumonia: a randomized trial. Pediatr Pulmonol. 2014;49(7):701–6. doi: 10.1002/ppul.22849. [DOI] [PubMed] [Google Scholar]
- 30.Le Corvoisier P, Renard V, Roudot-Thoraval F, et al. Long-term effects of an educational seminar on antibiotic prescribing by GPs: a randomised controlled trial. Br J Gen Pract. 2013;63(612):e455–64. doi: 10.3399/bjgp13X669176. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Meeker D, Knight TK, Friedberg MW, et al. Nudging guideline-concordant antibiotic prescribing: a randomized clinical trial. JAMA Intern Med. 2014;174(3):425–31. doi: 10.1001/jamainternmed.2013.14191. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.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. doi: 10.1186/1741-7015-9-44. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Christakis DA, Zimmerman FJ, Wright JA, Garrison MM, Rivara FP, Davis RL. A randomized controlled trial of point-of-care evidence to improve the antibiotic prescribing practices for otitis media in children. Pediatrics. 2001;107(2):E15. doi: 10.1542/peds.107.2.e15. [DOI] [PubMed] [Google Scholar]
- 34.Christakis DA, Wright JA, Taylor JA, Zimmerman FJ. Association between parental satisfaction and antibiotic prescription for children with cough and cold symptoms. Pediatr Infect Dis J. 2005;24(9):774–7. doi: 10.1097/01.inf.0000176616.11643.17. [DOI] [PubMed] [Google Scholar]
- 35.Dahler-Eriksen BS, Lauritzen T, Lassen JF, Lund ED, Brandslund I. Near-patient test for C-reactive protein in general practice: assessment of clinical, organizational, and economic outcomes. Clin Chem. 1999;45(4):478–85. [PubMed] [Google Scholar]
- 36.de la Poza Abad M, Mas Dalmau G, Moreno Bakedano M, et al. Prescription strategies in acute uncomplicated respiratory infections: a randomized clinical trial. JAMA Intern Med. 2016;176(1):21–9. doi: 10.1001/jamainternmed.2015.7088. [DOI] [PubMed] [Google Scholar]
- 37.Hemkens LG, Saccilotto R, Reyes SL, et al. Personalized prescription feedback using routinely collected cata to reduce antibiotic use in primary care: a randomized clinical trial. JAMA Intern Med. 2017;177(2):176–83. doi: 10.1001/jamainternmed.2016.8040. [DOI] [PubMed] [Google Scholar]
- 38.Samore MH, Bateman K, Alder SC, et al. Clinical decision support and appropriateness of antimicrobial prescribing: a randomized trial. JAMA. 2005;294(18):2305–14. doi: 10.1001/jama.294.18.2305. [DOI] [PubMed] [Google Scholar]
- 39.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(22):2345–52. doi: 10.1001/jama.2013.6287. [DOI] [PubMed] [Google Scholar]
- 40.Gerber JS, Prasad PA, Fiks AG, et al. Durability of benefits of an outpatient antimicrobial stewardship intervention after discontinuation of audit and feedback. JAMA. 2014;312(23):2569–70. doi: 10.1001/jama.2014.14042. [DOI] [PubMed] [Google Scholar]
- 41.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(4):267–73. doi: 10.1001/jamainternmed.2013.1589. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Jenkins TC, Irwin A, Coombs L, et al. Effects of clinical pathways for common outpatient infections on antibiotic prescribing. Am J Med. 2013;126(4):327–35e12. doi: 10.1016/j.amjmed.2012.10.027. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43.Finkelstein JA, Davis RL, Dowell SF, et al. Reducing antibiotic use in children: a randomized trial in 12 practices. Pediatrics. 2001;108(1):1–7. doi: 10.1542/peds.108.1.1. [DOI] [PubMed] [Google Scholar]
- 44.Meeker D, Linder JA, Fox CR, et al. Effect of behavioral interventions on inappropriate antibiotic prescribing among primary care practices: a randomized clinical trial. JAMA. 2016;315(6):562–70. doi: 10.1001/jama.2016.0275. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.Yang L, Liu C, Wang L, Yin X, Zhang X. Public reporting improves antibiotic prescribing for upper respiratory tract infections in primary care: a matched-pair cluster-randomized trial in China. Health Res Policy Syst. 2014;12:61. doi: 10.1186/1478-4505-12-61. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46.Schnoor M, Meyer T, Suttorp N, et al. Development and evaluation of an implementation strategy for the German guideline on community-acquired pneumonia. Qual Saf Health Care. 2010;19(6):498–502. doi: 10.1136/qshc.2008.029629. [DOI] [PubMed] [Google Scholar]
- 47.Finkelstein JA, Huang SS, Kleinman K, et al. Impact of a 16-community trial to promote judicious antibiotic use in Massachusetts. Pediatrics. 2008;121(1):e15–23. doi: 10.1542/peds.2007-0819. [DOI] [PubMed] [Google Scholar]
- 48.Huang SS, Rifas-Shiman SL, Kleinman K, et al. Parental knowledge about antibiotic use: results of a cluster-randomized, multicommunity intervention. Pediatrics. 2007;119(4):698–706. doi: 10.1542/peds.2006-2600. [DOI] [PubMed] [Google Scholar]
- 49.Vervloet M, Meulepas MA, Cals JW, Eimers M, van der Hoek LS, van Dijk L. Reducing antibiotic prescriptions for respiratory tract infections in family practice: results of a cluster randomized controlled trial evaluating a multifaceted peer-group-based intervention. NPJ Prim Care Respir Med. 2016;26:15083. doi: 10.1038/npjpcrm.2015.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50.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(4):231–40. doi: 10.14236/jhi.v17i4.742. [DOI] [PubMed] [Google Scholar]
- 51.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):e311–9. [PubMed] [Google Scholar]
- 52.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. doi: 10.1136/bmj.b1374. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 53.Cals JW, de Bock L, Beckers PJ, et al. Enhanced communication 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(2):157–64. doi: 10.1370/afm.1477. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 54.Mainous AG, 3rd, Lambourne CA, Nietert PJ. Impact of a clinical decision support system on antibiotic prescribing for acute respiratory infections in primary care: quasi-experimental trial. J Am Med Inform Assoc. 2013;20(2):317–24. doi: 10.1136/amiajnl-2011-000701. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55.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(2):325–9. doi: 10.1007/s11096-012-9606-6. [DOI] [PubMed] [Google Scholar]
- 56.Gonzales R, Corbett KK, Wong S, et al. “Get smart Colorado”: Impact of a mass media campaign to improve community antibiotic use. Medical Care. 2008;46(6):597–605. doi: 10.1097/MLR.0b013e3181653d2e. [DOI] [PubMed] [Google Scholar]
- 57.Hurlimann D, Limacher A, Schabel M, et al. Improvement of antibiotic prescription in outpatient care: a cluster-randomized intervention study using a sentinel surveillance network of physicians. J Antimicrob Chemother. 2015;70(2):602–8. doi: 10.1093/jac/dku394. [DOI] [PubMed] [Google Scholar]
- 58.Vinnard C, Linkin DR, Localio AR, et al. Effectiveness of interventions in reducing antibiotic use for upper respiratory infections in ambulatory care practices. Pop Health Mgmt. 2013;16(1):22–7. doi: 10.1089/pop.2012.0025. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59.Gonzales R, Steiner JF, Lum A, Barrett PH., Jr Decreasing antibiotic use in ambulatory practice: impact of a multidimensional intervention on the treatment of uncomplicated acute bronchitis in adults. JAMA. 1999;281(16):1512–9. doi: 10.1001/jama.281.16.1512. [DOI] [PubMed] [Google Scholar]
- 60.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(1):39–45. doi: 10.1111/j.1532-5415.2004.52008.x. [DOI] [PubMed] [Google Scholar]
- 61.Formoso G, Paltrinieri B, Marata AM, et al. Feasibility and effectiveness of a low cost campaign on antibiotic prescribing in Italy: community level, controlled, non-randomised trial. BMJ. 2013;347:f5391. doi: 10.1136/bmj.f5391. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 62.Yardley L, Douglas E, Anthierens S, et al. Evaluation of a web-based intervention to reduce antibiotic prescribing for LRTI in six European countries: quantitative process analysis of the GRACE/INTRO randomised controlled trial. Implement Sci. 2013;8:134. doi: 10.1186/1748-5908-8-134. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 63.Szymczak JE, Feemster KA, Zaoutis TE, Gerber JS. Pediatrician perceptions of an outpatient antimicrobial stewardship intervention. Infect Control Hosp Epidemiol. 2014;35(Suppl 3):S69–78. doi: 10.1086/677826. [DOI] [PubMed] [Google Scholar]
- 64.Mustafa M, Wood F, Butler CC, Elwyn G. Managing expectations of antibiotics for upper respiratory tract infections: a qualitative study. Ann Fam Med. 2014;12(1):29–36. doi: 10.1370/afm.1583. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 65.Grondal H, Hedin K, Strandberg EL, Andre M, Brorsson A. Near-patient tests and the clinical gaze in decision-making of Swedish GPs not following current guidelines for sore throat - a qualitative interview study. BMC Fam Pract. 2015;16:81. doi: 10.1186/s12875-015-0285-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 66.Munoz-Plaza CE, Parry C, Hahn EE, et al. Integrating qualitative research methods into care improvement efforts within a learning health system: addressing antibiotic overuse. Health Res Policy Syst. 2016;14(1):63. doi: 10.1186/s12961-016-0122-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 67.Tonkin-Crine S, Yardley L, Coenen S, et al. Strategies to promote prudent antibiotic use: exploring the views of professionals who develop and implement guidelines and interventions. Fam Pract. 2013;30(1):88–95. doi: 10.1093/fampra/cms043. [DOI] [PubMed] [Google Scholar]
- 68.Wood F, Phillips C, Brookes-Howell L, et al. Primary care clinicians’ perceptions of antibiotic resistance: a multi-country qualitative interview study. J Antimicrob Chemother. 2013;68(1):237–43. doi: 10.1093/jac/dks338. [DOI] [PubMed] [Google Scholar]
- 69.Mauffrey V, Kivits J, Pulcini C, Boivin JM. Perception of acceptable antibiotic stewardship strategies in outpatient settings. Med Mal Infect. 2016;46(6):285–93. doi: 10.1016/j.medmal.2016.06.006. [DOI] [PubMed] [Google Scholar]
- 70.Ronnerstrand B, Andersson Sundell K. Trust, reciprocity and collective action to fight antibiotic resistance. An experimental approach. Soc Sci Med. 2015;142:249–55. doi: 10.1016/j.socscimed.2015.08.032. [DOI] [PubMed] [Google Scholar]
- 71.Dempsey PP, Businger AC, Whaley LE, Gagne JJ, Linder JA. Primary care clinicians’ perceptions about antibiotic prescribing for acute bronchitis: a qualitative study. BMC Fam Pract. 2014;15:194. doi: 10.1186/s12875-014-0194-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 72.Huddy JR, Ni MZ, Barlow J, Majeed A, Hanna GB. Point-of-care C reactive protein for the diagnosis of lower respiratory tract infection in NHS primary care: a qualitative study of barriers and facilitators to adoption. BMJ Open. 2016;6(3):e009959. doi: 10.1136/bmjopen-2015-009959. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 73.Rowbotham S, Chisholm A, Moschogianis S, et al. Challenges to nurse prescribers of a no-antibiotic prescribing strategy for managing self-limiting respiratory tract infections. J Adv Nurs. 2012;68(12):2622–32. doi: 10.1111/j.1365-2648.2012.05960.x. [DOI] [PubMed] [Google Scholar]
- 74.Kuzujanakis M, Kleinman K, Rifas-Shiman S, Finkelstein JA. Correlates of parental antibiotic knowledge, demand, and reported use. Ambul Pediatr. 2003;3(4):203–10. doi: 10.1367/1539-4409(2003)003<0203:copakd>2.0.co;2. [DOI] [PubMed] [Google Scholar]
- 75.Ackerman SL, Gonzales R, Stahl MS, Metlay JP. One size does not fit all: evaluating an intervention to reduce antibiotic prescribing for acute bronchitis. BMC Health Serv Res. 2013;13:462. doi: 10.1186/1472-6963-13-462. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 76.Murphy M, Bradley CP, Byrne S. Antibiotic prescribing in primary care, adherence to guidelines and unnecessary prescribing—an Irish perspective. BMC Fam Pract. 2012;13:43. doi: 10.1186/1471-2296-13-43. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 77.Anthierens S, Tonkin-Crine S, Douglas E, et al. General practitioners’ views on the acceptability and applicability of a web-based intervention to reduce antibiotic prescribing for acute cough in multiple European countries: a qualitative study prior to a randomised trial. BMC Fam Pract. 2012;13:101. doi: 10.1186/1471-2296-13-101. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 78.Gurses AP, Seidl KL, Vaidya V, et al. Systems ambiguity and guideline compliance: a qualitative study of how intensive care units follow evidence-based guidelines to reduce healthcare-associated infections. Qual Saf Health Care. 2008;17(5):351–9. doi: 10.1136/qshc.2006.021709. [DOI] [PubMed] [Google Scholar]
- 79.Pronovost PJ, Berenholtz SM, Goeschel CA, et al. Creating high reliability in health care organizations. Health Serv Res. 2006;41(4 Pt 2):1599–617. doi: 10.1111/j.1475-6773.2006.00567.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 80.Timmel J, Kent PS, Holzmueller CG, Paine L, Schulick RD, Pronovost PJ. Impact of the Comprehensive Unit-based Safety Program (CUSP) on safety culture in a surgical inpatient unit. Jt Comm J Qual Patient Saf. 2010;36(6):252–60. doi: 10.1016/s1553-7250(10)36040-5. [DOI] [PubMed] [Google Scholar]
- 81.Simpson KR, Knox GE, Martin M, George C, Watson SR. Michigan Health & Hospital Association Keystone Obstetrics: a statewide collaborative for perinatal patient safety in Michigan. Jt Comm J Qual Patient Saf. 2011;37(12):544–52. doi: 10.1016/s1553-7250(11)37070-5. [DOI] [PubMed] [Google Scholar]
- 82.Wick EC, Hobson DB, Bennett JL, et al. Implementation of a surgical comprehensive unit-based safety program to reduce surgical site infections. J Am Coll Surg. 2012;215(2):193–200. doi: 10.1016/j.jamcollsurg.2012.03.017. [DOI] [PubMed] [Google Scholar]
- 83.Ali KJ, Farley DO, Speck K, Catanzaro M, Wicker KG, Berenholtz SM. Measurement of implementation components and contextual factors in a two-state healthcare quality initiative to reduce ventilator-associated pneumonia. Infect Control Hosp Epidemiol. 2014;35(Suppl 3):S116–23. doi: 10.1086/677832. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 84.Hsu YJ, Marsteller JA. Influence of the Comprehensive Unit-based Safety Program in ICUs: Evidence From the Keystone ICU Project. Am J Med Qual. 2016;31(4):349–57. doi: 10.1177/1062860615571963. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
