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DOI: 10.1055/a-2054-0270
Digital Antimicrobial Stewardship Decision Support to Improve Antimicrobial Management
Funding U.S. Department of Health and Human Services; National Institutes of Health; U.S. National Library of Medicine; NLM Institutional Training grant number: T15LM007092-30.
- Abstract
- Background and Significance
- Objective
- Methods
- Results
- Discussion
- Conclusion
- Clinical Relevance Statement
- Multiple-Choice Questions
- References
Abstract
Objectives We sought to create a digital application to support clinicians in empiric and pathogen-directed antibiotic ordering based on local susceptibility patterns and evidence-based treatment durations, thereby promoting antimicrobial stewardship.
Methods We formed a multidisciplinary team that met bimonthly from 2017 to 2018 to design and construct a web-based antimicrobial stewardship platform called Antibiogram + . We used an iterative and agile technical development process with frequent feedback from clinicians.
Results Antibiogram+ is an online tool, accessible via the electronic health record and hospital intranet, which offers institutional antibiotic susceptibilities for major pathogens, recommendations for empiric antibiotic selection and treatment durations for common pediatric conditions, antimicrobial dosing and monitoring guidance, and links to other internal clinical decision support resources. The tool was accessed 11,823 times with 492 average monthly views during the first 2 years after release. Compared with use of a preexisting print antibiogram and dosing card, pediatric residents more frequently reported “often” being sure of antibiotic dosing with Antibiogram+ (58 vs. 15%, p < 0.01). Respondents also reported improved confidence in choice of antibiotic, but this finding did not reach statistical significance (55 vs. 35%, p = 0.26).
Conclusion We report the successful development of a digital antimicrobial stewardship platform with consistent rates of access during the first 2 years following release and improved provider comfort with antibiotic management.
Keywords
microbial sensitivity tests - antimicrobial stewardship - clinical decision support systemsBackground and Significance
Antimicrobial resistance is widely recognized as a global public health threat.[1] In the United States, antibiotic-resistant organisms cause 2.8 million infections and more than 35,000 deaths each year.[2] Antimicrobial stewardship programs (ASPs) perform systematic interventions to promote effective and judicious antimicrobial use, including establishing policies to foster best practices and developing guidelines, order sets, and other tools to support evidence-based clinical decision-making. Through these actions, ASPs facilitate appropriate antimicrobial selection (i.e., choosing the narrowest-spectrum and safest drug active against the targeted pathogen[s]), dosing, duration, and monitoring, which in turn optimizes clinical outcomes while minimizing antimicrobial-associated adverse effects and development of resistance.[3] [4] [5] [6] [7]
Clinicians commonly manage moderate-to-severe infections by initiating an empiric antimicrobial regimen to cover the most likely pathogens while awaiting microbiological data.[6] [8] Once organisms have been identified and antibiotic susceptibilities are available, antimicrobials are typically de-escalated to a targeted regimen as appropriate.[6] [8] To delineate this process and highlight moments in care to promote antimicrobial stewardship, the Agency for Healthcare Research and Quality (AHRQ) developed the Four Moments of Antibiotic Decision Making[9] [10]:
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Does my patient have an infection that requires antibiotics?
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Have I ordered appropriate cultures before starting antibiotics? What empiric therapy should I initiate?
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A day or more has passed. Can I stop antibiotics? Can I narrow therapy or change from intravenous (IV) to oral therapy?
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What duration of antibiotic therapy is needed for my patient's diagnosis?
An effective clinical decision support tool should aid the clinician in all Four Moments of Antibiotic Decision Making.
Selecting empiric antimicrobial therapy can be challenging as it requires synthesizing knowledge of likely pathogens, severity of illness, clinical trajectory, and underlying patient risk factors.[10] [11] [12] Local antibiograms aggregate susceptibility data for bacterial pathogens over a period of time and guide optimal antibiotic selection.[13] [14] However, antibiograms do not include information about relative frequencies of causative agents of different infectious diseases, making them the most straightforward to use when a pathogen has been identified, but final susceptibility results are still pending.[15] Other forms of clinical decision support have been shown to improve antimicrobial prescribing practices.[16] [17] [18] Effective antimicrobial stewardship requires decision support both in empiric selection based on likely pathogens for a given syndrome and in tailoring regimens once the pathogen is known.
At our institution, the ASP has historically provided a paper reference to prescribers colloquially known as the “Green Card” (referred to hereafter as the print antibiogram) that includes the hospital-wide antibiogram, together with dosing and monitoring recommendations for frequently used antimicrobials and duration recommendations for common pediatric infectious diseases. This reference card is updated annually and distributed to all prescribers, including medical trainees at the start of training. The print antibiogram does not include information about relative frequencies of causative agents or recommendations for empiric antimicrobial regimens for various syndromes. However, clinical pathways that provide complementary guidance on management of some infectious diseases are available in PDF format in a centralized library, accessible via the electronic health record (EHR), the hospital intranet homepage, and a mobile application.
Objective
Our objective was to develop and deploy a web-based integrated clinical decision support platform that we named Antibiogram+ to help frontline clinicians to manage antimicrobials in accordance with our institutional antibiogram and clinical pathways, national guidelines, and available pediatric evidence.
Methods
Setting
The study was conducted at the Boston Children's Hospital (BCH) in Boston, Massachusetts, United States, an urban, tertiary care pediatric hospital with 404 licensed beds during the study period. The Innovation and Digital Health Accelerator (IDHA) program at BCH facilitates and accelerates software and digital innovations from within the hospital system, through provision of competitive internal grants and partnership on information technology development. Proposals from hospital staff are vetted by a team of clinicians, researchers, business specialists, engineers, and legal experts. The most promising ideas are granted in-kind support to accelerate the idea toward internal use or commercialization.
At the time of this study, the BCH ASP consisted of a Medical Director (1.0 FTE, infectious-diseases trained), Antimicrobial Stewardship Pharmacist (0.5 FTE, infectious-diseases trained), and data analyst (0.5 FTE).
BCH uses a business intelligence application (MicroStrategy, Tysons Corner, Virginia, United States) to consolidate enterprise-wide susceptibility data. Each spring, the Infectious Diseases Diagnostic Laboratory (IDDL) compiles susceptibility data from the preceding calendar year for selected common bacterial pathogens and antibiotics to create an annual antibiogram. Organisms are only included if data are available for approximately 30 isolates; for some less frequently isolated bacteria, data from the prior 2 years are combined to achieve this minimum sample. The ASP reviews the antibiogram for accuracy and to assess resistance trends. The IDDL and ASP adhere to the Clinical and Laboratory Standards Institute (CLSI) guidelines.
Design of the Antibiogram+ Clinical Decision Support Platform
Antibiogram+ was iteratively developed as a collaboration between the clinical and IDHA technical teams. Two clinicians (a general pediatrics resident and an infectious diseases attending) recognized the need for improved accessibility of antimicrobial stewardship decision support. After review of available applications and an informal literature review, they did not find a suitable and customizable application and therefore applied to the IDHA for a grant to support internal development. The grant provided in-kind engineering, design/user interface, and project manager support. Development started in Spring 2017, and the application launched in Fall 2018.
Our team consisted of a project manager, four clinicians (two general pediatrics residents, an infectious diseases attending, and an emergency medicine attending), a senior engineer, and two additional engineers. The project manager had specific prior experience leading commercialization initiatives in multiple industries, and her primary role at the IDHA was development and execution of grant-funded innovations. The senior engineer had prior experience as a health care application architect; his primary role at the IDHA consisted of technical advising. The two additional engineers both had computer programming and user-centered design experience.
We followed the standard IDHA project accelerator workflow, which uses agile process development. The medical and technical teams met initially to explore possible solutions to meet clinical needs. The technical team met daily to iteratively build and refine visual and technical aspects of the application. The project manager and technical lead used Jira software (Atlassian) to track development progress and plan for next steps. The developers presented wireframe designs, followed by prototypes and then working versions of the tool for clinical feedback on at least a monthly basis or more frequently as needed.
Creating Empiric Antibiotic Recommendations
An expert panel, consisting of the Antimicrobial Stewardship Pharmacist and Medical Director of Antimicrobial Stewardship plus three other pediatric infectious diseases physicians, developed antibiotic recommendations based on national and local guidelines, current literature, and hospital antimicrobial susceptibility data. Common pediatric infections were included based on the experience of the panel. Recommendations were reviewed and supported by the Division of Infectious Diseases and Antimicrobial Subcommittee of the BCH Pharmacy and Therapeutics Committee.
Usability and Pilot Testing
At later stages of development, feedback on format and usability was elicited from clinicians who had expressed interest in the project. After development, the platform underwent rigorous pilot testing prior for usability testing and feedback before ultimate broad implementation. We invited a diverse group of frontline ordering clinicians to participate since they were most likely to use the tool. Focus group sessions were informal and consisted of a brief demonstration of the application and an opportunity for free user exploration. Changes based on user feedback were integrated into the final version of Antibiogram + .
User Surveys
We surveyed pediatric residents pre- and postimplementation to evaluate perceptions of Antibiogram+ and its impact on clinical practice. We chose to focus on residents because they are frontline clinicians who frequently make antibiotic management decisions.
Process measures included perceived accessibility and usability of Antibiogram+ compared with the print antibiogram and number of session uses per month. Outcome measures included perceived usefulness of Antibiogram+ and confidence with deciding on empiric antibiotics, antibiotic dosage, and treatment duration using Antibiogram+ compared with the print antibiogram. Answer options for questions about ease of use, frequency of use, and confidence used a 4-point Likert scale. Multiple-choice and free-text answer options were used to collect other feedback about barriers to use and suggestions for improvement of Antibiogram + . The survey was reviewed and revised by two faculty members with expertise in survey design (who were not involved in the design or development of Antibiogram + ) and another with expertise in antimicrobial stewardship.
The surveys were distributed using REDCap (Research Electronic Data Capture).[19] The presurvey was distributed 6 weeks prior to implementation of Antibiogram + , whereas the postsurvey was released 2 weeks after implementation. Each survey was kept open for 1 month. Both the pre-and postsurveys were sent out via email to all pediatric residents with three reminder emails. The postsurvey instructions specified that only residents who had used Antibiogram+ for patient care should complete the survey. Survey responses were collected anonymously, but pre- and postimplementation surveys were paired for respondents who completed both.
Data Analysis
We used Google Analytics (Alphabet Inc, Mountain View, California, United States) to collect anonymous usage statistics for Antibiogram + , consisting of frequency of access of the various parts of the platform. We analyzed pre- and postimplementation survey responses and summarized them using descriptive statistics. We compared pre- and postimplementation results using the Fisher's exact test. A p-value < 0.05 was considered statistically significant. We used RStudio 7 (Posit, Boston, Massachusetts, United States) for all analyses.
Results
Antibiogram+ Front-End Description
Antibiogram+ is available to all clinicians via a direct link from the EHR toolbar, as well as from a “quick link” on the institutional intranet home page. The application's landing page provides four menu options: Antibiotic Susceptibilities, Antibiotic Recommendations, Dosing Quick References, and Resource Materials. Users can also search for a specific pathogen, drug, or clinical syndrome, yielding results that link to the relevant Antibiotic Susceptibilities, Dosing Quick References, and Antibiotic Recommendations pages ([Figs 1] [2] [3]). All Antibiogram+ content is managed by the Medical Director of the ASP and Antimicrobial Stewardship Pharmacist, who update the antibiogram annually and revise or amend other content as needed.






Antibiotic Susceptibilities displays the digital antibiogram for common bacterial pathogens and antibiotics ([Fig. 1]). The webpage design follows standard antibiogram formatting with pathogens listed vertically and antibiotics listed horizontally. The default view shows all pathogens and antibiotics, but to highlight data for pathogen–antibiotic combinations of interest, the user can select one or more individual pathogens and/or antibiotics on the antibiogram itself or using the Bug-Drugs Filter. The number of isolates assessed for each pathogen–antibiotic combination is listed. Each cell displays the percentage of isolates susceptible to a given antibiotic and is shaded according to that percent susceptibility, with darker cells representing greater susceptibility; inherent resistance is denoted with an “R” and gray shading. A dash and absence of shading indicate that the antibiotic is not typically tested for the organism. A legend at the top of the antibiogram defines these notations and formatting conventions.
Antibiotic Recommendations ([Fig. 2]) features treatment recommendations for common community- and hospital-acquired infectious diseases, organized by organ system. The page for each syndrome identifies the most common pathogens, displays their susceptibility patterns, and suggests appropriate empiric therapy (first-line regimens, as well as second- and third-line recommendations for patients with antibiotic allergies) and treatment durations ([Fig. 2]). Also provided are comments and alerts about relevant clinical pathways and order sets, guidance on using additional or alternative antibiotics in specific clinical scenarios, and criteria for requesting Infectious Diseases consultation.
Dosing Quick Reference ([Fig. 3]) provides dosing by route and indication and therapeutic drug monitoring guidance for common antimicrobials. The cost of each drug is indicated using a scale of 1 to 4 dollar signs that is defined in a legend at the top of the page. Clinically relevant comments and alerts are displayed: Examples include the need for dose adjustment with renal dysfunction or preference for use of the enteral formulation.
Resource Materials offers links to the ASP's internal website, which includes further clinical guidance, profiles of ASP team members, and information on current and past initiatives.
A navigation menu within each section of the application offers access to the other sections, as well as a Feedback button that links to a brief form for submitting technical or clinical comments or questions.
Antibiogram+ Back-End Description
Antibiogram+ is a Google site (Alphabet Inc., Mountain View, California, United States) backed by a database that contains the hospital antibiogram and other content securely within the network. There is no login required to use Antibiogram + , but only users on the hospital network can access the site. Administrator logins are provided to the ASP team, who are able to modify most content without the need for an application engineer.
Antibiogram+ Implementation
Antibiogram+ was made available on October 3, 2018. Prior to launch, we publicized the platform via an internal electronic newsletter and notified residents and advanced practice providers about it via email.
Usage Logs
During the 2 years after release, Antibiogram+ was accessed 11,823 times with similar proportions of views for susceptibility data, dosing, and empiric antibiotic recommendations. In the 2 years after release, there were 492 average monthly views with usage increasing over time ([Fig. 4]). There were 480 average monthly views in the first 12 months after implementation and 506 average monthly views in the second 12 months after implementation. Slightly less than 10% of users left the site after only viewing the landing page. About 30% of users used the “typed search” function to search from the landing page. Approximately 20% used the Antibiotic Recommendations page to find empiric antibiotic recommendations by body system ([Fig. 2]); the most frequently viewed diagnosis was inpatient uncomplicated community-acquired pneumonia ([Fig. 5]).




Survey Results
Forty-six (30%) of 151 eligible pediatric residents responded to the preimplementation survey and 31 (20%) responded to both the pre- and postimplementation surveys. Preimplementation, 63% of respondents reported that the main barrier to use of the print antibiogram was not having the resource with them when needed. Over 90% of postsurvey respondents indicated that they felt Antibiogram+ was very or somewhat useful and very or somewhat easy to use.
Respondents reported referring more frequently to Antibiogram+ than the print antibiogram for antimicrobial dosing (26 vs. 2% referred to it at least weekly, p < 0.01). Respondents similarly reported referring more frequently to treatment duration recommendations using Antibiogram+ (26 vs. 4% referred to it at least weekly, p = 0.03) than the print antibiogram ([Fig. 6]). Furthermore, they more often referred to the antibiogram within Antibiogram+ than to the print version (45 vs. 24% referred to it at least weekly), but this did not reach statistical significance (p = 0.25).


Compared with preimplementation, respondents were more likely postimplementation to report that they were “often” sure when selecting the correct antibiotic dose (39 vs. 15%, p < 0.01, [Fig. 7]). They were also more likely to report “often” being sure of which empiric antibiotic to select (55 vs. 35%), but this difference was not statistically significant ([Fig. 7], p = 0.26).


Discussion
We report the successful development and implementation of Antibiogram + , a web-based antimicrobial stewardship decision support platform. Our application is comprehensive and designed to aid clinicians at each of the Four Moments of Antibiotic Decision Making: when to initiate antibiotics, which antibiotics to use, whether and how to narrow antibiotics, and what duration of therapy to use.[9] [10] We offer an example use case: when pediatric residents admit a patient with a suspected urinary tract infection (UTI), they could first refer to Antibiogram+ for guidance on which empiric antibiotic regimen to initiate. The Antibiotic Recommendations section provides information on the most common UTI pathogens, their typical susceptibility patterns, and recommended first- and second-line regimens, whereas the Dosing Quick Reference section offers indication-specific dosages and guidance on renal dose adjustments and therapeutic drug monitoring. Once a pathogen has been identified on urine culture, they could refer to the Antibiotic Susceptibilities section to ensure that the empiric regimen is likely to provide adequate coverage pending susceptibility results. Finally, as the patient is approaching discharge, they can again refer to Antibiogram+ for enteral antibiotic dosages and UTI treatment duration recommendations.
Tallman et al reported poor resident ability to select an appropriate empiric antibiotic for case vignettes of a postsurgical abdominal infection (49% selected an appropriate regimen) and recurrent pyelonephritis (77% selected an appropriate regimen). While 90% of respondents were aware of the hospital antibiogram, only 44% knew how to access it.[20] Our survey data indicate that after implementation of Antibiogram + , residents more often consulted the institutional antibiogram and felt more confident in choosing appropriate empiric antibiotics, dosing, and treatment durations.
Usage data demonstrated excellent uptake by clinicians, which increased throughout the first 2 years of measurement. Self-report from resident surveys confirmed increased use and confidence in selection of empiric antibiotics, antibiotic dosing, and treatment durations compared with the preexisting print reference. Our findings suggest that similar digital tools could serve as an effective means to facilitate antimicrobial stewardship at the point of care delivery.
Untapped Potential of Antibiograms as Clinical Decision Support Tools
Although the CLSI released consensus guidelines for the analysis and presentation of antimicrobial resistance data (M39) in 2007, their recommendations did not focus on maximizing provider utilization or recommend the best medium for distributing this information.[21] [22] Typically, antibiograms are available via hospital website or pocket card. A perceived lack of easy access to the resource may lead to reduced utilization.[23] Frontline prescribers frequently do not know how to access antibiograms or find access inconvenient (75% of low utilizers).[24] Survey data have indicated that house officers, attending physicians, and nurse practitioners across multiple specialties and practice settings express low rates (≤50%) of institutional antibiogram use, instead favoring publicly available general resources such as UpToDate or The Sanford Guide.[20] [24] [25] [26] These resources lack antibiotic recommendations tailored to susceptibility patterns at the regional or institutional level. As such, we believe that enhancing functionality and accessibility of the antibiogram and integrating it with broader clinical decision support is critical for improving antimicrobial stewardship.
Antibiogram+ Design and Accessibility Informed Usability Design Choices
To optimize end user experience and encourage clinician use of decision support tools, ease of access and an intuitive design are critical. We believe that ease of access to Antibiogram+ and the intuitive navigation it provides to needed information were critical to its success. The application is available from the menu bar in the EHR so that it is plainly visible to all clinicians (i.e., users are not required to click a dropdown menu to reveal its location). Moreover, the application layout was chosen to minimize the number of clicks required to get to clinical guidance. As an example, to navigate from the chart of a patient with a newly diagnosed UTI to recommendations for management, only three clicks are needed to reach the Antibiotic Recommendations section of Antibiogram + .
For the antibiogram, we designed a color shading scheme that correlated with degree of susceptibility, in contrast with the more commonly used green (susceptible)–yellow (intermediate susceptibility)/red (resistant) approach, thereby incorporating more nuance into the visual depiction of antibiotic susceptibility. The green–yellow–red scheme is simple but assumes a one-size-fits-all risk tolerance for potential antibiotic resistance, when in fact this may be vary based on individual patient factors such as underlying immunocompromised state or severity of illness.
While Antibiogram+ can fully replace the previous print reference in terms of functionality, the print antibiogram is still available for clinicians who prefer to use a nondigital pocket resource in addition to a web-based resource. The ASP distributes the print reference to clinical teams and keeps a supply, available to any staff member who would like a copy, at the hospital's central pharmacy.
Comparison of Antibiogram+ with Other Digital Applications
Antibiogram+ showed strong uptake with over 11,000 sessions in the first 2 years after implementation, which compares with Simpao et al, who described the development of an e-antibiogram, updated monthly, that automates the process of compiling hospital-wide antibiogram data, stratifies laboratory data by source, and is available to clinicians via an EHR link.[27] They reported over 4,000 sessions in the first year following release, with a notable increase over time.
There are many mobile apps that offer similar content to promote antimicrobial stewardship. Examples include Microguide, the Stewardship Assist (Sanford Guide), and Firstline (formerly Spectrum).[28] [29] [30] A review of ASP applications as of 2020 showed widely variable average monthly uses, ranging from 21 to 1,953 per month across seven different studies.[31] The group reporting the highest monthly use rate made their application available on smartphone, tablet, and desktop. Of note, 21% of Antibiogram+ unique sessions were accessed via smartphone. These findings suggest that making Antibiogram+ available as a smartphone app accessible outside of the hospital network may further improve utilization. In addition, Antibiogram+ could be made even more useful and appealing if more tightly integrated with the hospital electronic formulary and clinical pathways via direct bidirectional links.
Limitations
Our study has several limitations. The study setting is a freestanding children's hospital with a large pediatric residency program, potentially limiting generalizability to other practice settings. Our survey had an overall low-response rate for both the pre- and postsurveys, which may have limited the representativeness of the responses. Furthermore, it is possible that residents interested in clinical decision support, clinical informatics, or antimicrobial stewardship were more likely to complete the survey, thus biasing the responses. We only surveyed pediatric residents but not advanced practice providers or attending physicians and thus cannot comment on perceptions of Antibiogram+ among these clinician groups. Because we were unable to link users' Antibiogram+ access to their subsequent antibiotic prescriptions, we were unable to directly evaluate improved adherence with local guidelines. Our use of surveys inherently relied on self-report and thus may have been less accurate in evaluating the impact of Antibiogram+ compared with direct assessment of clinical decisions. Finally, empiric antibiotic recommendations necessarily depend on local susceptibility patterns, which vary by institution. That the antibiogram and empiric antibiotic recommendations within Antibiogram+ are based on local susceptibility data is a strength, but to implement our platform or similar applications, other institutions would need engagement with local infectious diseases and antimicrobial stewardship representatives, potentially limiting applicability if this expertise is not available.
Conclusion
We describe the successful implementation of a digital antimicrobial stewardship platform that intuitively integrates the institutional antibiogram, recommendations for empiric antibiotic selection and treatment durations, and antimicrobial dosing guidance. We used an agile design process with frequent clinical feedback that enabled rapid and effective development. Our application achieved excellent uptake by clinicians, and survey responses showed improvement in clinician use over a preexisting print resource and increased confidence in antibiotic management.
Clinical Relevance Statement
Choosing the appropriate antimicrobial regimen when caring for patients with infectious diseases is of utmost importance. This decision is a complex one that requires not just consideration of the patient's condition and clinical trajectory, but also familiarity with institutional and local resistance patterns and knowledge of local and national evidence-based guidelines. Digital antimicrobial stewardship applications represent an untapped potential source to integrate these key resources and support clinicians in making decisions for optimal antimicrobial management.
Multiple-Choice Questions
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Which of the following is one of the Four Moments of Antibiotic Decision Making according to the AHRQ?[9] [10]
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Does my patient have an infection that requires antibiotics?
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Which is the most cost-effective antibiotic choice for my patient's condition?
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What dose frequency should I prescribe for my patient's antibiotics?
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Which two antibiotics will have the most synergistic effect when treating my patient's infection?
Correct Answer: The correct answer is option a. According to the AHRQ the Four Moments of Antibiotic Decision Making are[9] [10]:
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Does my patient have an infection that requires antibiotics?
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Have I ordered appropriate cultures before starting antibiotics? What empiric therapy should I initiate?
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A day or more has passed. Can I stop antibiotics? Can I narrow therapy or change from IV to oral therapy?
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What duration of antibiotic therapy is needed for my patient's diagnosis?
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Which of the following describes agile project methodology?
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Performing extensive documentation to make postimplementation support as easy as possible
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Avoiding a change to the project plan or description unless strictly necessary
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Avoiding presentation of unfinished or partially finished deliverables, only interfacing with the customer once a fully working tool that supports all desired functionality has been created
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Delivering software frequently to allow an iterative development cycle with frequent customer input
Correct Answer: The correct answer is option d. One of the 12 principles of the Agile Manifesto is an emphasis on early and frequent software delivery to maximize customer input and satisfaction.[32]
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Conflict of Interest
None declared.
Acknowledgments
We would like to acknowledge the Boston Children's Hospital Innovation and Digital Health Accelerator team for the provision of both project management and technical time and expertise. This project would not have been possible without their generous support.
Protection of Human and Animal Subjects
The Boston Children's Hospital Institutional Review Board reviewed and approved this study.
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References
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Address for correspondence
Publikationsverlauf
Eingereicht: 19. Dezember 2022
Angenommen: 12. März 2023
Accepted Manuscript online:
14. März 2023
Artikel online veröffentlicht:
31. Mai 2023
© 2023. Thieme. All rights reserved.
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References
- 1 Walker B, Barrett S, Polasky S. et al. Environment. Looming global-scale failures and missing institutions. Science 2009; 325 (5946): 1345-1346
- 2 Centers for Disease Control and Prevention (U.S.). Antibiotic Resistance Threats in the United States, 2019. Centers for Disease Control and Prevention (U.S.); 2019.
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