FEATURES

Journal of the American Pharmacists Association xxx (2017) 1e10

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SPECIAL FEATURES
Outpatient antibiotic stewardship: Interventions and
opportunities
Erica L. Dobson*, Michael E. Klepser, Jason M. Pogue, Matthew J. Labreche,
Alex J. Adams, Timothy P. Gauthier, R. Brigg Turner, Christy P. Su, David M. Jacobs,
Katie J. Suda, on behalf of SIDP Community Pharmacy Antimicrobial Stewardship
Task Force

a r t i c l e i n f o a b s t r a c t

Article history: Improving the use of antibiotics across the continuum of care is a national priority. Data
Received 18 November 2016 outlining the misuse of antibiotics in the outpatient setting justify the expansion of antibiotic
Received in revised form stewardship programs (ASPs) into this health care setting; however, best practices for
7 March 2017
outpatient antibiotic stewardship (AS) are not yet defined. In a companion article, we focused
Accepted 31 March 2017
on recommendations to overcome challenges related to the implementation of an outpatient
ASP (e.g., building the AS team and defining program metrics). In this document, we outline AS
interventions that have demonstrated success and highlight opportunities to enhance AS in
the outpatient arena. This article summarizes examples of point-of-care testing, policies and
interventions, and education strategies to improve antibiotic use that can be used in the
outpatient setting.
© 2017 American Pharmacists Association®. Published by Elsevier Inc. All rights reserved.

One of the first hospital antibiotic stewardship programs
(ASPs) in the United States was initiated in the late 1970s,
when a team of infectious diseases physicians and pharmacists
implemented a prospective audit and feedback strategy at
Hartford Hospital in Connecticut.1 Since that time, ASPs have
been formally defined2 and have produced mounting evidence
that the use of interventions in acute care results in judicious
prescribing and improvement in patient outcomes.3 Antibiotic
overuse and misuse is not unique to the hospital setting, and
recent federal policy provides the impetus to implement ASPs
across all health care settings. In recognition of the need to
expand the fight against drug-resistant pathogens, the White
House issued Executive Order 13676: Combating Antibiotic-
Resistant Bacteria in September 2014.4 One facet of the order
was the call for defining and establishing antibiotic steward-
ship (AS) across the continuum of care, including, but not
limited to, office-based practices and outpatient settings.4 In
response to the executive order, the National Strategy and
Disclosures: The views expressed in this article are those of the authors and
do not necessarily reflect the position or policy of the U.S. Department of
Veterans Affairs or the U.S. government.
* Correspondence: Erica L. Dobson, PharmD, 601 Elmwood Ave, Box 638,
Rochester, NY 14642.
E-mail address: Erica_Dobson@urmc.rochester.edu (E.L. Dobson).
National Action Plan for Combating Antibiotic-Resistant Bac-
teria were published in 2014 and 2015, respectively.5,6 These
documents were intended to serve as a roadmap for meeting
the challenge presented by antibiotic-resistant bacteria. The
action plan outlined numerous objectives and milestones
aimed at increasing outpatient AS (Table 1).5
Presently, there is limited guidance available for AS teams
that are forming or expanding into the outpatient practice
setting. The factors that drive antibiotic misuse or over-
prescribing in the outpatient setting may be different from
those in the hospital, including perceived patient and parent
or caregiver expectations for antibiotics, diagnostic uncer-
tainty, prescriber time pressures, and patient satisfaction.7 To
address these unique circumstances, stewardship in-
terventions that have been suggested to improve outpatient
antibiotic prescribing patterns differ somewhat from those in
the inpatient setting. Optimal intervention components are
difficult to identify given the paucity of comparable data in this
setting; however, experts agree that a multifaceted approach
is necessary to improve antibiotic use.8-10 The Centers for
Disease Control and Prevention (CDC) recently released the
Core Elements of Outpatient Antibiotic Stewardship in an
attempt to consolidate evidence-based practices and adapt
best practices across other clinical settings.11 When planning a
new outpatient AS initiative, the AS team should select

http://dx.doi.org/10.1016/j.japh.2017.03.014
1544-3191/© 2017 American Pharmacists Association®. Published by Elsevier Inc. All rights reserved.
FEATURES
E.L. Dobson et al. / Journal of the American Pharmacists Association xxx (2017) 1e10

Table 1
Objectives and select milestones outlined in the National Action Plan for Combating Antibiotic-Resistant Bacteria specific to outpatient antibiotic stewardship5
 Sub-Objective 1.1.1A: Strengthen antibiotic stewardship in inpatient, outpatient, and long-term care settings by expanding existing programs, developing
new ones, and monitoring progress and efficacy.
Within 3 years:
B The Centers for Disease Control and Prevention (CDC), Centers for Medicare and Medicaid Services (CMS), the Agency for Healthcare Research and

Quality, and other partners will issue guidance on antibiotic stewardship and best practices for ambulatory surgery centers, dialysis centers, nursing
homes, other long-term care facilities, doctors’ offices and other outpatient settings, pharmacies, emergency departments, and medical departments at
correctional facilities.
 Sub-Objective 1.1.1B: Strengthen educational programs that inform physicians, veterinarians, members of the agricultural industry, and the public about
good antibiotic stewardship.
Within 3 years:
B CMS will expand the Physician Quality Reporting System (PQRS) to include quality measures that discourage inappropriate antibiotic use to treat

non-bacterial infections, such as respiratory tract infections.

 Sub-Objective 1.1.3: Implement annual reporting of antibiotic use in inpatient and outpatient settings and identify geographic variations or variations at
the provider or patient level that can help to guide interventions.
Within 1 year:
B CDC will report outpatient prescribing rates for 2011 and 2012 and use the data to target and prioritize intervention efforts.

B CDC will establish a benchmark (in terms of prescriptions per population) for reduction in antibiotic use.

Within 3 years:
B Starting in 2016, CDC will issue yearly reports on progress in meeting the national target of 50% reduction in inappropriate use of antibiotics in

outpatient settings, as well as on overall trends in antibiotic prescribing.

B The U.S. Department of Defense (DOD) will establish goals for reducing antibiotic use in DOD facilities that provide outpatient care for military

personnel and their families.

B DOD will centralize reporting of outpatient antibiotic use and issue annual summary reports.

 Sub-Objective 2.1.1: Create a regional public health laboratory network that uses standardized testing platforms to expand the availability of reference
testing services, characterize emerging resistance patterns and bacterial strains obtained from outbreaks and other sources, and facilitate rapid data
analysis and dissemination of information.
 Sub-Objective 2.1.2: Link data generated by the regional public health laboratory network to existing public health surveillance networks so that antibiotic
susceptibility testing data are immediately available to local, state, and federal public health authorities as they detect and investigate outbreaks, and to
veterinary diagnostic and food safety laboratory databases and surveillance systems, as needed.
 Sub-Objective 2.2.1: Enhance reporting infrastructure and provide incentives for reporting (e.g., require reporting of antibiotic-resistance data to National
Healthcare Safety Network as part of the CMS Hospital Inpatient Quality Reporting Program).
 Sub-Objective 2.2.2: Add electronic reporting of antibiotic use and resistance data in a standard file format to the Stage 3 Meaningful Use certification
program for electronic health record systems.
 Sub-Objective 2.2.3: Expand the activities and scope of the Emerging Infections Program to include monitoring of additional urgent and serious bacterial
threats and evaluating at-risk populations across community and health care settings.
 Objective 3.1: Develop and validate new diagnosticsdincluding tests that rapidly distinguish between viral and bacterial pathogens and tests that detect
antibiotic-resistancedthat can be implemented in a wide range of settings.
 Objective 3.2: Expand the availability and use of diagnostics to improve treatment of antibiotic-resistant bacteria, enhance infection control, and facilitate
outbreak detection and response in health care and community settings.

interventions and education strategies that will be practical
and effective for achieving established ASP objectives.
This article describes evidence-based opportunities and
interventions for developing and expanding AS initiatives into
the outpatient practice setting. For the purposes of this article,
the outpatient practice setting will encompass ambulatory
care clinics, physician offices, convenient care clinics, urgent
care clinics, and community pharmacies. Although emergency
departments, nursing homes, and long-term care facilities
may be considered outpatient practice sites and some of the
concepts discussed herein may be applicable to these settings,
these venues also offer unique opportunities and present
challenges that may not be addressed.
Identifying stewardship targets
Traditionally, AS initiatives have tended to focus on activ-
ities under a limited organizational umbrella. However,
collaboration among clinics, health systems, laboratories,
public health, community pharmacies, and other stakeholders
may optimize an outpatient AS program and provide new
models for achieving outpatient AS objectives. Although
outpatient ASPs could certainly have a focus within a partic-
ular health system, they have the potential to reach much
further. To realize their full potential, outpatient ASPs should
strive to engage a broader cohort of partners, including clinics,
community pharmacies, and hospitals. Furthermore, outpa-
tient AS initiatives can take on numerous forms; however, at
the most basic level, all interventions are designed to affect a
process on the patient-infection continuum (Table 2).12
When implementing a new AS initiative or expanding an
existing ASP, the AS team should perform an evidence-based
assessment of antibiotic prescribing for infectious diseases
syndromes and identify barriers to optimal management
across the patient-infection continuum. This exercise will aid
in identifying areas of opportunity for AS initiatives and
prioritizing interventions. Once priorities and opportunities
have been recognized, AS strategies that have documented
success in improving antibiotic overprescribing should be
implemented (Table 3).10,13 ASP leaders will need to discern
the elements of ASPs that are both critical to the success of the
AS initiative, but also feasible in the diverse outpatient setting.
Most data in the outpatient arena evaluate interventions to
curb unnecessary prescribing for acute respiratory tract in-
fections (RTIs), and this infectious syndrome has been an
obvious and critical target for intervention given the docu-
mented gross overuse of antibiotics to treat acute bronchitis
and other RTIs that are primarily viral in nature.14

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Antibiotic stewardship in the outpatient setting

Table 2
The patient-infection continuum

Patient care segment Opportunity for action Rationale

Need to seek care
Decision to prescribe antibiotics and agent
selection
Dispensing of an antibiotic
Post-encounter care
Abbreviations used: POC, point of care.
 Immunization programs  If a physician visit for an infection is avoided,
 Patient education then there is not a risk for an antibiotic to be
 Preventive medicine and wellness initiatives prescribed.
 Postdischarge bridge calls
 Use of POC diagnostics  Improve the selection of antibiotics
 Clinic use
 Pharmacy use
 Prescriber audit and feedback
 Peer comparison
 Prescriber education, behavioral intervention
 Practice updates
 Development of practice guidelines
 Prescribing tools
▪ Suggested alternatives
▪ Accountable justification
 Development of regional and local
antibiograms of outpatient isolates
 Development of outpatient or practice
formularies
 Development of allergy assessment and
penicillin skin testing program or referral
 Pharmacist education  Improve the appropriateness of antibiotic use
 Encourage prescriber inclusion of ICD-10
code or diagnosis and duration on the pre-
scription to allow pharmacist verification of
the appropriateness of the agent, dose, and
duration
 Telephone follow-up 24e48 hours after the  Decrease rates of antibiotic overuse
initial encounter  Improve patient safety
 Allow for better use of delayed prescribing
 Safety net regarding the decision not to use
antibiotics or on the appropriateness and
safety of the agent prescribed

Interventions tailored to problems of antibiotic overuse and Audit and feedback

resistance must include other common outpatient infectious
diseases (e.g., otitis media, skin or soft tissue infections, and
asymptomatic bacteriuria), specific pathogens, or specific
antibiotic agents.
Recently, CDC in collaboration with a panel of national
experts described outpatient prescribing rates for 2010-2011
to understand the breadth of unnecessary antibiotics pre-
scribed to adults and children in the United States.15 These
data can serve as an important starting point for novel
outpatient ASPs or as an area for enhancement for existing
ones. In this analysis, the investigators estimated that 30% of
outpatient antibiotic prescriptions were unnecessary.15 These
data can be used to target and prioritize AS intervention efforts
while also providing a benchmark for reduction in antibiotic
prescriptions. Collectively, acute RTIs (e.g., sinusitis, otitis
media, pharyngitis, bronchitis and bronchiolitis, upper respi-
ratory infections, asthma and allergy, influenza, and pneu-
monia) accounted for 44% of outpatient antibiotic
prescriptions, with half of these prescriptions estimated to be
unnecessary.15 This finding supports an infectious diseases
syndromeespecific approach to AS in the outpatient setting,
particularly in clinics, emergency departments, and hospital
outpatient departments (Table 4) and suggests that acute RTIs
can serve as an important starting target disease state for ASPs.
In what follows, we review select examples of outpatient AS
interventions for which data exist to support implementation.
Program metrics should be disseminated to stakeholders,
team members, and prescribers to identify need or motivation
for changes in prescribing patterns. Clinical practices may
consider adding antibiotic use metrics (matched to AS initia-
tives) as a clinical metric to any existing or planned customized
measurement dashboards16 or other methods used to provide
feedback to providers. For quality improvement purposes,
prescribing metrics can be compared with peer performance
in a practice site, network, or region, or with established
benchmarks and can be outlined by high-priority condition.
Peer comparison and positive reinforcement to top performers
is a strategy that has demonstrated the ability to reduce un-
necessary antibiotic prescribing for acute RTIs.17
Continuously providing prescribers access to real time
antibiotic use metrics allows clinicians and the ASP to track
changes in prescribing practices of an individual or group of
prescribers. Alternatively, antibiotic prescribing summaries
may be provided at specified intervals. When combined with
clinician education, quarterly provider feedback demonstrated
a nearly 50% relative reduction in broad-spectrum antibiotic
prescribing rates for bacterial infections (e.g., sinusitis, strep-
tococcal pharyngitis, and pneumonia) encountered in the
outpatient environment.18 Following cessation of this inter-
vention, broad-spectrum prescribing reverted back toward
baseline, suggesting that antibiotic use feedback strategies

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E.L. Dobson et al. / Journal of the American Pharmacists Association xxx (2017) 1e10
Table 3
Antibiotic stewardship interventions with demonstrated success in the
outpatient setting10
 Additional testing to aid in diagnostic certainty (e.g., point-of-care
tests for group A streptococcus or influenza, viral polymerase chain
reaction, procalcitonin, C-reactive protein)
 Audit and feedback
 Clinical decision support tools
 Communication training for prescribers
 Delayed prescribing strategies
 Evidence-based guidelines
 Patient education
 Provider education
 Provider pledge to practice antibiotic stewardship
need to be sustained to maintain optimal prescribing habits.19
In addition, once targets of use have been met, the effectiveness
of these strategies may become stagnant.20
Education
A comprehensive education plan is imperative to the suc-
cess of any planned AS activity and is necessary for adoption of
changes in practice.2 Education in the outpatient setting will
need to be directed at prescribers, pharmacists, and other
health professionals, as well as patients and other members of
the community. Given that the audience is likely to be scat-
tered across different clinics, pharmacies, or other venues,
educational methods (e.g., formal or informal didactic pre-
sentations, webinars, workshops, case review, posters, news-
letters, brochures, electronic health record (EHRs) alerts, or
direct person-to-person communication) selected for use will
need to be varied. The AS team must develop the education
plan in tandem with targeted AS initiatives and have a plan for
who to educate, how to educate, when to educate, and
appropriate intervals for re-education as needed. ASPs should
be visible to the end users, and educational materials should
be easily accessible. Education alone is an insufficient stew-
ardship strategy and should be combined with a correspond-
ing AS intervention (e.g., audit and feedback, clinical decision
support, delayed prescribing, public display of provider pledge
to practice antibiotic stewardship).21 Without a plan for
continual educational efforts, the beneficial effects of educa-
tion on antibiotic prescribing are likely to diminish over time.
Educational resources
Educational programs target health care providers and the
general community. They should encompass a number of
topics ranging from treatment guideline updates to the ben-
efits of vaccination and wellness programs on antibiotic
avoidance. It is important that the educational objectives of
the AS team be consistent with the targeted AS initiative. To
facilitate the development of educational content, there are
several reputable Web-based resources available; some pro-
vide shortened summaries of national evidence-based guide-
lines, Web-based learning modules, or health care consumer
education materials that can be downloaded for use with little
or no alteration.
In the United States, the “CDC Get Smart: Know When
Antibiotics Work” national campaign (http://www.cdc.gov/
getsmart/community/index.html) provides evidence-based
4
Table 4
Syndrome-specific interventions for acute respiratory tract infections in the
outpatient8
Infectious diseases syndrome Recommended national goal
for a reduction in antibiotic
prescribing
Sinusitis Age 0e19 years: 9%
Age 20e65 years: 51%
65 years and older: 16%
Nonsuppurative otitis media All ages: 100%
Suppurative otitis media Age 0e19 years: 10%
Age 20e64 years: 33%
Pharyngitis 0e19 years: 34%
20e64 years: 75%
Viral upper respiratory infections All ages: 100%
Bronchitis All ages: 100%
Asthma and allergy All ages: 100%
Influenza All ages: 100%
Viral pneumonia All ages: 100%
Nonviral pneumonia All ages: 0%
resources for common infectious diseases and educational
courses designed by experts in the field. In addition, the
website contains brochures, posters, fact sheets, and letters
that can be distributed to patients and placed in clinics or
pharmacies. State and local health departments have imple-
mented community-based AS educational campaigns and re-
sources; these tools typically focus on the lack of efficacy of
antibiotics in treating common viral illnesses or prevention of
Clostridium difficile infections (CDIs). In the United Kingdom,
the TARGET Antibiotics Toolkit (http://www.rcgp.org.uk/
clinical-and-research/toolkits/target-antibiotics-toolkit.aspx)
was designed as a resource by the Antimicrobial Stewardship
in Primary Care (ASPIC) collaboration to optimize antibiotic
prescribing in the primary care setting. E-learning modules,
patient education leaflets, auditing toolkits, self-assessment
checklists, and additional resources are provided on the
ASPIC webpage, which is publically accessible.
Clinician education
Efforts to improve antibiotic use and selection for specific
infections must include those responsible for prescribing and
dispensing antibiotics. Many studies have used passive
educational techniques, such as lecturing, continuing educa-
tion, and seminars, as the principle intervention or as a sup-
plement to other interventions.22-32 While education is often
delivered only once, several studies delivered education mul-
tiple times24,28 including 1 study that held bimonthly ses-
sions.27 The academic detailing model has demonstrated
effectiveness in reducing the number of antibiotic pre-
scriptions and in improving antibiotic selection.33-36 The aca-
demic detailing model involves one-on-one education by
clinical specialists (including pharmacists, nurses, or physi-
cians) to help clinicians provide evidence-based care to their
patients.37 This method primarily involves educational
outreach, generally in a frontline clinician’s office, where in-
formation is provided interactively. This allows the educator to
understand where the clinician is coming from in terms of
knowledge, attitudes, and behavior. The educator will then
modify the presentation to address the personal learning op-
portunities to keep the practitioner engaged. The one-on-one

Antibiotic stewardship in the outpatient setting
visit ends with specific practice-changing recommendations.
Pharmacists or other health care providers can participate in
the academic detailing training series developed by the Na-
tional Resource Center for Academic Detailing (http://www.
narcad.org/training-series.html).
Communication training for prescribers has also been
shown to decrease unnecessary antibiotic prescribing.10,38 This
strategy can be used to address factors that drive antibiotic
misuse, specifically perceived patient or parent or caregiver
expectations for antibiotics and patient satisfaction.39 Con-
trary to the belief of many clinicians, patient satisfaction is less
associated with the receipt of an antibiotic and more depen-
dent on the quality of communication provided during an
encounter. The message should focus on why an antibiotic is or
is not needed, nonantibiotic treatment options, and contin-
gency planning. Incorporating positive (offer symptomatic
treatment options) and negative (explain why antibiotics are
not needed) treatment recommendations during the patient
encounter has demonstrated an 85% reduction in the risk of
antibiotic prescribing for viral RTIs, while improving patient
satisfaction scores.40 Shared decision making is another
example of a communication approach that has demonstrated
reductions in antibiotic use for acute RTIs, without reducing
patient satisfaction. In this process, the patient and prescriber
make health care decisions together after reviewing patient
expectations, options for management, and the benefits and
risks. In a recent analysis, this approach led to a 38% reduction
in antibiotic prescribing compared to usual care without
reducing patient satisfaction.41
Patient education
Traditionally the main objective of patient education in the
outpatient setting has been to decrease patient perception of
the need for an antibiotic in viral illnesses when they are not
indicated, such as in acute RTIs.42 This continues to be an
important objective for patient education in this setting,
although with the continued development of AS interventions
focused on a particular infection or syndrome, more specific
educational messages are necessary. There are multiple pa-
tient education delivery methods that can be considered:
mailing or distributing brochures and informational pam-
phlets,33,36,38,43 displaying pamphlets and posters in
clinics27,32,36 and pharmacies,27,32 providing hyperlinks in the
EHRs for printing and distributing at the point of care,44 or
public presentations to community groups.32 These types of
patient education are intended to supplement key AS in-
terventions, and are unlikely to affect antibiotic use outcomes
alone. Educational efforts to improve antibiotic use in outpa-
tient settings should be coordinated to target health pro-
fessionals and consumers across a variety of venues.
Additional patient education efforts should target the pa-
tients’ need and decision to seek care (Table 2). Programs to
promote wellness, vaccinations, and community pharmacy-
based disease management can help to reduce unnecessary
office visits and therefore reduce the risk of receipt of an
antibiotic prescription.12,15 Community pharmacies should
incorporate patient education on optimal antibiotic use into
direct-to-consumer advertising and onsite direct-to-patient
educational initiatives.
FEATURES
Computerized decision support and electronic health
records
EHRs45 and computerized order entry have become critical
instruments in the rapidly changing health care environment.
The availability of clinical decision support (CDS) can be
invaluable to the busy outpatient prescriber who is limited by
the nature of the encounter, often lacks real-time access to
specialists, and may not have the opportunity to change a
prescription once it is written. CDS tools developed from EHRs
offer an opportunity to assist with AS at the point of pre-
scribing to include electronic alerts, antibiotic order sets, and
cascading questions to guide antibiotic selection, dose, and
duration for a particular infection or patient.46 Having CDS
tools available at the point of prescribing, such as accountable
justification for nonrecommended antibiotic prescribing, is a
useful strategy to ensure guideline-concordant antibiotic
prescribing. EHRs also provide data that can be aggregated to
conduct electronic surveillance of antibiotic prescribing prac-
tices and to assess the impact of the ASP.18,47-49 The AS team
should place emphasis on the design and use of CDS tools that
will prompt the prescriber to optimize antibiotic use, selec-
tion, dose, and duration (or no antibiotic) based on clinically
relevant factors such as prescribing indication, available
microbiology culture results and susceptibilities, antibiotic
allergies, drug-drug interactions, renal function, medical his-
tory, and cost or insurance coverage. Other examples of CDS
tools include embedding clinical guidelines into the health
record (or easy Web-based access, laminated cards, posters,
etc.), real-time community or facility antibiograms, or the use
of branching logic to guide decisions. Regardless of the CDS
mechanism, prescribers need to be educated before and dur-
ing the implementation to optimize its uptake and utility.
Studies evaluating the impact of CDS tools on antibiotic use in
the outpatient setting have primarily focused on acute RTIs
and have generally demonstrated a favorable reduction in
antibiotic prescribing.10,44,50-55 In one instance, implementa-
tion of a clinical pathway-based intervention in combination
with a peer champion and patient education resulted in a
significant decrease in overall antibiotic (14.4% relative
reduction; P <0.001) prescribing for acute RTIs that are not
pneumonia.55
It is important to anticipate challenges and barriers asso-
ciated with CDS tools when considering implementation.
Providers are unlikely to use a CDS tool if it will interrupt
workflow, its function is inflexible, or it introduces time
pressure in the context of the medical encounter.56 New CDS
tools should be designed or implemented with the assistance
of information technology (IT), infectious diseases specialists,
and frontline providers with the opportunity for testing and
refinement before and after its introduction into clinical
practice. The development and maintenance of CDS tools
within the EHR is labor intensive and requires ongoing dedi-
cated resources.
Outpatient clinic practices should develop policies
requiring providers to specify the indication and duration of
antibiotic therapy on prescriptions. The EHR can be used to
support this policy by mandating these entry fields during
electronic prescribing, and the data can be collected for pro-
cess measures as metrics for AS. The AS team should identify
and work with IT to extract meaningful outcome and
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E.L. Dobson et al. / Journal of the American Pharmacists Association xxx (2017) 1e10
performance measures from the EHR to inform AS. EHR ven-
dors should support AS tools for use in the outpatient
settingdfor example, by creating AS platforms that are specific
to outpatient prescribing.56
Delayed prescribing
Delayed prescribing, also referred to as watchful waiting, is
an effective strategy that can be implemented for mild acute
otitis media57 and acute RTIs.58-60 This strategy reduces anti-
biotic use by requesting that patients delay filling their pre-
scription by 24-48 hours, postdating the prescription or
contacting the patient after the encounter to determine
whether an antibiotic is necessary considering lack of symp-
tom improvement. For practices that use electronic prescrib-
ing, postdating the prescription is often not feasible; rather,
the provider can add a note to the prescription such as “fill in 2
days if not better” in the signature field.44 Delayed prescribing
is one approach that can be used to address overprescribing
related to patient pressure for antibiotics and concerns often
relayed by providers that patient satisfaction scores may suffer
if antibiotics are not prescribed.39 When using this approach, it
should be noted that patients may feel uncomfortable deciding
on their own when the prescription should be filled. Therefore,
to improve the effectiveness of this approach, a member of the
AS team should contact the patient or their caregiver at a
specified time to assess the need to fill the prescription for the
antibiotic.
Guideline implementation
Clinical experts on the AS team should review, implement,
and maintain community-wide or health system-specific
antibiotic use guidelines for common outpatient infectious
diseases. These guidelines should take into account local pre-
scribing trends, resistance patterns, and antibiotic cost. In a
systematic review, Drekonja et al.10 identified that the use of
prescribing guidelines are associated with improved antibiotic
outcomes (e.g., reduced overall use or improved agent selec-
tion) in the outpatient setting. Guidance on when and how to
use antibiotics needs to be accessible, short, easy-to-read, and
widely promoted.
In response to a significant increase in the incidence of CDI
in the province of Que bec, Canada, an educational program
targeted to physicians and pharmacists was launched to
reduce outpatient antibiotic prescriptions for common
outpatient infections.61 The guidelines were available on the
Internet and were heavily promoted in a widespread educa-
tional campaign. One year following the dissemination and
promotion of the guidelines, the number of antibiotic pre-
scriptions in Quebec per 1000 residents was reduced with an
associated decrease in prescription costs. Combining the
dissemination of user-friendly guidelines with an active pro-
motion and educational campaign demonstrated sustained
reductions in antibiotic prescribing out to 36 months.
One of the advantages to the implementation of treat-
ment guidelines is the opportunity to provide a community-
wide best practice document designed by disease state
experts. The goal is to drive optimal antibiotic use by
disseminating this information to the frontline provider,
such as a primary care provider or community pharmacist.
6
The dissemination of guidelines on a large scale has proved
difficult to implement in the outpatient setting.25 This can
be overcome with attentiveness to factors that are deemed
critical to success,21,61 such as interdisciplinary guideline
development, engagement of peer champions, incorporating
recommendations into CDS, and facilitating implementation
through audit and feedback strategies similar to the inpa-
tient setting.2,21
Point-of-care testing
Improved use of point-of-care (POC) diagnostics in outpa-
tient practice has been identified as a means to promote AS in
this setting.62-65 POC testing for infectious diseases in com-
munity pharmacies and ambulatory care settings represents
an ideal opportunity to enhance AS by influencing the decision
to use and select an antibiotic. POC tests paired with a
physician-pharmacist collaborative practice agreement (CPA)
can benefit patients by offering access to care and initiation of
therapy in a timely manner while concurrently reducing dis-
ease transmission within the population.66
There are approximately 60,000 community pharmacies in
the United States, and 95% of all Americans live within 5 miles
of a pharmacy.67,68 In addition, pharmacies are open nights
and weekends, when many other care settings are closed.
Thus, community pharmacists are a highly accessible health
professional in most communities. A recent analysis revealed
that 10,838 community pharmacies possessed a Clinical Lab-
oratories Improvement Act (CLIA) certificate of waiver
enabling them to perform POC tests.69 Although this varies by
state, community pharmacies are an opportunity to expand
access to POC testing for infectious diseases.
If allowed by state regulations, implementation of
pharmacy-based, collaborative disease management programs
that incorporate CLIA-waived POC testing should be
explored.62,70 These programs can target various diseases such
as influenza, group A streptococcus (GAS) pharyngitis, human
immunodeficiency virus,26 and hepatitis C virus. Programs
could focus on either identifying infected patients and linking
them to care or providing care under CPAs or via telemedicine.
Either way, the focus should be to identify patients with a
disease of interest, provide timely treatment with recom-
mended antimicrobial agents, provide supportive care when
antibiotics are not indicated, and share information among
practitioners. Successful collaborative disease state manage-
ment models for influenza and acute pharyngitis have been
described.63-65,71 Pharmacists, physicians, and public health
officials should seek opportunities to replicate and expand
CPAs for AS where permissible. Although CLIA-waived POC
tests are simple to perform, their integration into successful
disease management programs is not always straightforward.
Therefore, we recommend that individuals seeking to develop
and implement collaborative disease management programs
that incorporate CLIA-waived POC tests receive appropriate
training through a certificate program (e.g., National Associa-
tion of Chain Drug Stores; http://nacds.learnercommunity.
com).
Although numerous CLIA-waived POC tests for infectious
agents have been approved for use in the United States, rela-
tively few examples have described how their use can enhance

Antibiotic stewardship in the outpatient setting
AS activities. Some of these experiences are summarized as
follows.
Influenza management model
Seasonal influenza is responsible for the hospitalization of
more than 200,000 people in the United States annually with
an associated mortality of 3000-49,000.72,73 Although the
influenza vaccine can reduce the probability of acquiring
influenza, prompt treatment with antivirals can help to lessen
symptoms and prevent serious complications. To be optimally
effective, antiviral treatment should be initiated within 2 days
of the onset of symptoms.74 Community pharmacists repre-
sent an early opportunity to intervene in the course of disease.
POC testing for influenza in a community pharmacy could
provide early diagnosis to facilitate the prescribing of antivi-
rals, potentially eliminating the need for empiric antibacterial
prescriptions when positive.
Klepser et al.65 described their experience implementing a
collaborative disease management model for patients with
influenza-like illness. This model was studied in 55 commu-
nity pharmacies in 3 states. According to the algorithm, pa-
tients with influenza-like illness were screened to determine
whether the use of a CLIA-waived rapid influenza diagnostic
test was appropriate. Eleven percent of patients had a positive
influenza test result and offered a prescription for oseltamivir
under a CPA. No individuals received an antibiotic. These
findings indicated improved rates of antiviral use when indi-
cated and a significant reduction in unnecessary antibiotic use
compared with published data.75,76
Pharyngitis management model
Acute pharyngitis accounts for more than 18 million office
visits annually throughout the world and more than 7 million
visits to pediatricians each year in the United States.77 GAS is
the most common bacterial cause of pharyngitis, accounting
for 5%-18% and 20%-37% of cases of pharyngitis among adults
and children, respectively.78-83 Most cases of pharyngitis are of
viral origin.39 Therefore, it is disturbing that despite the rela-
tively low frequency with which GAS is identified as the
causative pathogen in cases of adult pharyngitis, data continue
to show that antibiotics are prescribed for 60%-72% of en-
counters.15,84 This suggests that more than half of antibiotics
prescribed for adult pharyngitis are unnecessary.
Because it can be difficult to distinguish between viral and
bacterial causes of pharyngitis, guidelines for the diagnosis
and management of GAS pharyngitis support the use of a rapid
antigen detection test (RADT) to direct treatment de-
cisions.39,78,85 Among adults, neither U.S. or European guide-
lines recommend follow-up culture for negative RADT tests.
Among children, however, the guidelines are split with respect
to their recommendations regarding follow-up culture. How-
ever, data continue to document the low rates with which
acute rheumatic fever and other complications occur among
children and POC tests continue to improve with respect to
reliability.86,87 Numerous CLIA-waived POC tests for the
detection of GAS are available in the United States. These tests
are typically antigen detection tests that yield results in as
little as 5 minutes. Although considerable variability exists
among tests, the overall sensitivity and specificity are high
FEATURES
(86% and 96%, respectively). Newer CLIA-waived tests for GAS
use molecular technologies and have higher performance
characteristics.87
A multicenter, pharmacy-based pharyngitis management
program63 conducted GAS RADT in adult patients with signs
and symptoms consistent with pharyngitis (as determined by
calculation of a Centor score). Of the 273 adult patients
screened, only 17.6% had a positive test result and received
antibiotics per a CPA. Patients with negative test results were
recommended over-the-counter products to manage symp-
toms. No negative outcomes were noted among those who did
not receive an antibiotic. This represents an absolute reduction
in antibiotic prescribing of approximately 40% over historical
rates of antibiotic prescribing. Thornley et al.71 reported
similar findings in a comparable pharmacy-based study.
Similar reductions in antibiotic prescription rates were also
identified with the use of GAS RADT in pediatric patients being
seen in the emergency department.88 The use of GAS RADT and
modification of prescriber behavior in response to results to
reduce unnecessary prescribing of antibiotics for pharyngitis
not caused by GAS can be a possible strategy as part of
outpatient AS.8,39,78
Recommendations
The National Action Plan for Combating Antibiotic-Resistant
Bacteria includes actions that will advance AS and intensify
educational programs directed at optimal antibiotic use prac-
tices in all health care settings, including outpatient settings.
U.S. governmental agencies (e.g., CDC, Agency for Healthcare
Research and Quality, Centers for Medicare and Medicaid)
have recently provided guidance on core elements for outpa-
tient AS,1 and implemented reporting of antibiotic prescribing
rates at the population level,89 and they will continue to
expand quality measures for optimal antibiotic use. We have
provided recommendations for implementing and assessing
outcomes for outpatient ASP in Table 5.
The National Action Plan set a goal of reducing inappro-
priate antibiotic prescribing by 50% in the outpatient setting
by the year 2020.5 Although accomplishing a 50% reduction in
antibiotic prescribing seems daunting, data on outpatient AS
initiatives and community pharmacy-based disease manage-
ment programs have shown that this goal is safely achievable.
We support the goal of minimally reducing antibiotic pre-
scribing by 50% by 2020. This said, it may be reasonable to
establish disease state-specific targets for reducing antibiotic
use (Table 4). We endorse the use of the CDC Core Elements for
Outpatient Antibiotic Stewardship (commitment, action for
policy and practice, tracking and reporting, and education and
expertise) as a framework for clinicians and facilities to begin
to work toward this goal.11
Presently, data regarding comprehensive ASPs are lacking
in the outpatient setting. If widespread engagements in AS
efforts in the outpatient sector are accomplished and antibiotic
use patterns optimized, it will result in improved public health
and patient safety. Detection of antibiotic prescribing rates is a
sensitive and reasonable parameter to use to measure the re-
sults of AS efforts. Systematic reviews evaluating the impact of
outpatient AS interventions on prescribing have consistently
shown improvement in antibiotic prescribing practices,10,90-92
with one review demonstrating a 9.7% reduction in the
7
FEATURES
E.L. Dobson et al. / Journal of the American Pharmacists Association xxx (2017) 1e10
Table 5
Recommendations for implementing and measuring the impact of outpatient
antibiotic stewardship programs
Implementation
 Use Centers for Disease Control and Prevention Core Elements as a
road map.
 Develop a comprehensive community strategy to realize maximal
benefits.
 Use a multifaceted approach targeting all 4 phases of the patient-
infection continuum.
Outcomes
 Use an assessment of quantity and appropriateness of antibiotic
prescribing as the primary outcome.
 Short-termdGlobal and disease-specific targets of antibiotic
prescription reductions to measure effectiveness of interventions
 Long termdImprovement in inpatient antibiotic use for
community-acquired infections, declining incidence of outpatient
and inpatient drug-resistant pathogens, and decreased antibiotic-
associated complications (e.g., adverse drug reactions, community-
associated C. difficile)
proportion of patients receiving antibiotics at 6 months.90
Pharmacy-based management models of acute pharyngitis
have demonstrated more than a 50% reduction in inappro-
priate antibiotic prescriptions.63 Owing to the intertwined
relationship between outpatient and inpatient antibiotic use,
susceptibility profiles, and adverse events, it is likely that all
these parameters will be influenced by reducing outpatient
antibiotic use. However, the impact that outpatient AS has on
these patient and microbial outcomes is not well character-
ized. A reduction in the rate of outpatient antibiotic prescrib-
ing by 10% may reduce community-associated C. difficile
infections (CA-CDI) by 17%.93 Experience with a multifaceted
intervention that combined the use of guidelines, education,
and feedback to reduce prescribing rates for specific antibiotics
associated with a high CA-CDI risk demonstrated a 55.5%
reduction in prescribing of these agents 24 months following
intervention.94
A need for AS in the outpatient setting has been recognized
for decades, but its implementation has proved difficult. Un-
like the inpatient setting, financial incentives for the devel-
opment of AS are not realized and the infrastructure to
develop an AS team is often lacking in this diverse setting. The
overall success of outpatient AS will largely depend on part-
nerships with inpatient AS teams, local or state health de-
partments, and other external stakeholders with common
objectives. This support will help to leverage AS policies,
provide education or training across the state or region, and
support the AS collaborative to target specific antibiotic over-
use and misuse issues. Unique strategies to overcome some of
the challenges in the outpatient setting require further
research; some examples include the use of electronic
consultation or telemedicine to extend expertise in managing
infectious diseases95 and a coordinated approach to AS in the
outpatient setting.96
Conclusion
Antibiotic resistance is a complex public health crisis. No
single intervention will prevent the spread of antibiotic
resistance or improve the use and safety of today’s antibiotics.
Progress requires a comprehensive plan tailored to the needs
in the community, individual practices, or health system with a
8
commitment from prescribers to use antibiotics judiciously in
clinical practice. With the federal mandate to decrease anti-
biotic resistance, many of the historical barriers to imple-
mentation of AS across the continuum of care will disentangle
through strategies outlined in the National Action Plan. In the
meantime, AS activities in the outpatient setting should
continue to progress, with an emphasis on expansion of stra-
tegies that have demonstrated effectiveness, piloting of inno-
vative models that can be researched and implemented on a
broader scale, and the development of coordinated efforts
among teams of health professionals and stakeholders to
establish widespread AS practices.
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Erica L. Dobson, PharmD, Department of Pharmacy, University of Rochester
Medical Center, Rochester, NY
Michael E. Klepser, PharmD, Ferris State University College of Pharmacy,
Kalamazoo, MI
Jason M. Pogue, PharmD, Department of Pharmacy Services, Sinai-Grace Hospi-
tal; Detroit Medical Center and Wayne State University School of Medicine,
Detroit, MI
Matthew J. Labreche, PharmD, MSc, Highland Hospital, Oakland, CA
Alex J. Adams, PharmD, MPH, Idaho State Board of Pharmacy, Boise, ID; at the
time of study, National Association of Chain Drug Stores, Arlington, VA
Timothy P. Gauthier, PharmD, Miami Veterans Affairs Healthcare System,
Miami, FL
R. Brigg Turner, PharmD, Pacific University, School of Pharmacy, Hillsboro, OR
Christy P. Su, PharmD, Memorial Hermann Greater Heights Hospital,
Houston, TX
David M. Jacobs, PharmD, University at Buffalo School of Pharmacy and Phar-
maceutical Sciences, Buffalo, NY
Katie J. Suda, PharmD, U.S. Department of Veterans Affairs, Center of Innovation
of Complex Chronic Healthcare, Edward Hines Jr. VA Hospital; University of
Illinois at Chicago College of Pharmacy, Chicago, IL