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DELAYED PRESCRIBING: PROMOTING ANTIBIOTIC STEWARDSHIP

ABSTRACT
Background: According to the Centers for Disease Control, (CDC, 2018) at least thirty
percent of outpatient antibiotics are unnecessary. A retrospective 2018 study by Incze, M.A.,
Redberg, R.F. and Katz, M. found forty nine percent of antibiotic prescriptions in the urgent care
setting were for inappropriate diagnosis. The aim of this study was to educate providers on one
method of reducing antibiotic prescriptions and incorporate new patient instructions into the
electronic health record. Participants included physicians associates and nurse practitioners.
Methods: The Quality improvement approach of Plan Do Study Act was utilized for this
project. A literature review was completed to study methods of antibiotic stewardship. The
electronic health record system was queried for delayed prescribing discharge instructions.
Informal discussions among providers revealed absence of a cohesive approach to reducing
unnecessary prescriptions for antibiotics.
Interventions: A PowerPoint was emailed to all providers on the use of delayed
prescribing for antibiotics along with a Likert-Scale survey on provider perceptions of
implementation. New instructions for patients on delayed prescribing of antibiotics was added to
the existing electronic health record system. For a period of 30 days the number of times
delayed prescribing instructions sheets were printed for patients was monitored along with the
number of patients seen at each location. The provider survey was also reviewed.
Results: Provider survey demonstrated favorable attitudes toward antibiotic stewardship.
The delayed prescribing instruction set was utilized twenty-seven times over the thirty-day
period. There were 2,579 patient encounters during the study for a 0.9% utilization rate.

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Conclusions: This was a new process in the clinic where the study was completed and
though the utilization was low there was favorable consensus among providers on the value of
antibiotic stewardship. There are many opportunities going forward including tracking diagnosis
codes along with antibiotic prescriptions and following up to determine how many delayed
prescriptions were filled. This research can provide a starting point for any outpatient facility
looking to decrease rates of antibiotic prescribing.
Keywords: antibiotic stewardship, outpatient, urgent care, delayed prescribing
Definition of Terms
Antibiotic Stewardship: proper antibiotic selection and treatment duration to allow current
antibiotics to remain effective and decrease antibiotic resistance (CDC,2021).
Health Care Provider: Any individual who is specially trained to diagnose and treat disease.
This includes but is not limited to nurse practitioners, physician associates and physicians.

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INTRODUCTION
Antimicrobial resistance seems a nebulous threat which will likely never cause real harm,
similar to a pandemic. COVID-19 has proven these threats can come to fruition, and therefore,
need to be addressed. Along with a worldwide pandemic, antibiotic resistance was named as one
of the top ten threats to global health by the World Health Organization in 2019 (World Health
Organization, 2019). The most concerning problems with antimicrobial resistance are the global
impact, high financial and personal costs, and lack of new antibiotics in production. This issue
has solutions which require commitments from both
healthcare and the general population.
Bacteria are amazingly durable and have been creating their own form of resistance long
before antibiotics were developed. It is estimated bacteria have been developing resistance for
both survival and extermination of competitors for the last 2.5 billion years. In 2016, researchers
uncovered bacteria in an isolated cave at Carlsbad Caverns in New Mexico which were resistant
to every antibiotic in production despite never having had human interaction (Spellburg, 2016).
Antibiotic resistance is found in humans, crops and animals and it occurs globally. Worldwide
resistance patterns of streptococcus pneumoniae, the most common cause of otitis media, to
macrolide antibiotics range from 8-34%. Every antibiotic in existence today is linked to a
worldwide resistance pattern by at least one bacterium (Center for Disease Dynamics
Economics and Policy, 2020).
Data from the United States reveals a similar trend of antibiotic resistance (Center for
Disease Dynamics Economics and Policy, 2020). When combined with high antibiotic
prescribing rates, the US faces severe risks of sequelae related to antibiotic resistance. Each year

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approximately 3 million Americans are infected with an antibiotic resistant organism and over
30,000 of them do not survive (Centers for Disease Control, 2020). The 2019 Antibiotic
Resistance Threats Report from the CDC cites C. Difficile infections occurred in 228,000 people
in the United States and resulted in over 12,000 deaths in 2017. These patterns extend to all
regions with southern parts of the United States experiencing the highest resistance rates
(Johnston, Thorpe, Jacob, & Murphy, 2019). The local antibiogram for the study site shows
steady rise in e. coli resistance to multiple antibiotics over the course of the last fifteen years
(Appendix A).
The cost burden is estimated at over 2 billion dollars annually in the United States
(University of Minnesota, 2018). In a 2019 study, researchers performed a meta-analysis in
which they calculated additional cost as an average of $1400 per infection. The authors noted a
two-fold increase in resistant infections from 2002-2014, the authors attributed the increase to
antibiotic overuse in both the inpatient and outpatient settings (Johnston, Thorpe, Jacob, &
Murphy, 2019). The burden on patients is less often studied, but factors such as missed days of
work, decreased productivity and expense of additional treatments should be included.
Further evidence of the seriousness of antibiotic resistance is the amount of resources
appropriated by the federal government in the United States. In 2014 through an Executive
Order, the CDC created the United States National Action Plan for Combating Antibiotic
Resistant Bacteria (CARB). This plan was expanded on and awarded 160 million dollars of
additional funding in 2020. Along with this funding came a new timeline and objectives to span
over the next five years. An overview of the five tenets of this program include: slowing
emergence of resistant bacteria, strengthen surveillance efforts, develop rapid detection test for

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resistant bacteria, accelerate the development of new antibiotics and improve international
collaboration on antibiotic resistance (Centers for Disease Control, 2020).
In 2019, the World Health Organization published a report on the state of antibiotic
development. The outlook showed a scarcity of new antibiotics and those in development with
little improvement over existing antibiotics. At the time of the report only fifty new antibiotics
were in development and these were predominately reformulations or combinations of existing
antibiotics. Cited in the report as primary reasons new formulations of antibiotics are lacking
were difficulties in finding new binding sites on targeted bacteria, lack of specificity in testing
for resistant organisms and unfavorable private sector funding. (World Health Organization,
2019).
Healthcare providers play a key role in combating antimicrobial resistance. The CDC has
outlined an antibiotic stewardship guide which provides a formula to keeping antibiotics
effective as long as possible. Education for patients and communities is a key component to
preventing antibiotic resistance. Primary care providers are uniquely positioned to provide
education to patients about appropriate use of antibiotics, methods to decrease spread of
infections and vaccine education and promotion. Healthcare providers in turn, have a
responsibility to be current on treatment guidelines, know how to screen for resistant infections
and to use antibiotics judiciously (Centers for Disease Control, 2021).

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LITERATURE REVIEW
Review of literature for this study began with a review of the recommendations from the
CDC’s report on the Core Elements of Outpatient Antibiotic Stewardship. The four main
elements of this campaign are; commitment, action for policy and practice, tracking and
reporting, education and expertise (Sanchez, Fleming-Dutra, Roberts, & Hicks, 2016). Of these,
the report was further investigated for actions for practice, delayed prescribing was one of the
methods identified in the report and became the focus of this study. The literature was reviewed
utilizing EBSCO Host and the following databases; CINAHL Complete, Cochrane Registry of
Systematic Review, Healthsource-Nursing/Academic Edition and MEDLINE complete. The
keywords used were; Delayed Prescribing with “AND” modifier for Antibiotics. This search
returned 163 results. Limits were added for peer-reviewed and articles within last seven years
which returned 71 results. The literature was further narrowed to exclude and results which were
commentaries, omitted delayed prescribing or were secondary or tertiary observations, after
these 13 articles remained.
The literature was further reviewed for themes regarding delayed prescribing of
antibiotics. The existing research demonstrated that delayed prescribing is effective in decreasing
antibiotic use and much of the effectiveness is relying on the interactions between the patients
and the prescribers. The majority of the existing research was done on upper respiratory
infections as these account for a large percentage of antibiotic prescribing. These infections are
often viral in nature and self -limiting in an otherwise healthy person and yet account for over
fifty percent of the outpatient antibiotic prescription (De la Poza Abad, et al., 2016). The
reviews included were global as this is a worldwide issue.

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There exist an abundance of research demonstrating the effectiveness of delayed
prescribing as a tool for decreasing inappropriate antibiotic use. Little et. al. 2014 studied four
different delayed prescription strategies by reviewing symptom severity and duration. In the
outpatient setting they demonstrated that no matter which method was used the rate of antibiotic
use was decreased by forty percent. Little and his colleagues noted the only difference was
patients who were given immediate antibiotic prescriptions demonstrated a higher belief in the
effectiveness of antibiotics. Similar results were replicated by Moore et. al. 2017 in the
DECARTES (Decision Rule for the Symptoms and Complications of Acute Red Throat in
Everyday practice) prospective cohort study out of the UK. This study found similarities in
symptom severity and relief in the delayed versus immediate anabatic prescribing groups and
that delayed prescribing resulted in fewer overall Antibiotic prescriptions filled. In a Cochrane
Systematic Review meta-analysis from the (Spurling, Del Mar, Dooley, Foxlee, & Farley, 2017)
which included 11 studies and over 3000 participants the findings were again that delayed
prescribing resulted in lower antibiotic use than immediate prescribing. This meta-analysis also
demonstrated specifically for a diagnosis of cough that the clinical outcomes were identical for
patients who received antibiotics versus those who did not. Findings were again replicated in this
study out of Spain in which patients were given no antibiotic, delayed prescription, return for
prescription or immediate antibiotic showed lowest antibiotic consumption with no prescription
and second lowest consumption with delayed prescription (De la Poza Abad, et al., 2016).
Ghebrehewet et. al. 2020 performed another study similar to De la Poza et. al. and again
replicated the same results of delayed prescribing resulting in lower antibiotic consumption with
similar clinical outcomes. One large cohort study out of the UK and Wales with 1.8 million
chart reviews did demonstrate some contradictory findings with a higher percentage of patients

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receiving delayed prescriptions experiencing complications which required hospitalization. Of
note this finding varied across the age groups in the study. The authors of the study
recommended a risk stratification process for patients who would receive delayed prescribing
versus immediate prescribing for upper respiratory infections (Van Staa, et al., 2020).
Overwhelming the evidence points towards delayed prescribing as a way to decrease overall
antibiotic use with minimal risk for complications.
In the review of the literature there is research concerning parent and patient perceptions
and experiences of delayed prescribing. A 2019 study with a cross sectional survey of 347
patrons at pharmacies demonstrated some respondents felt antibiotics would work on viral
infections and that they were effective for the common cold. This shows an opportunity exist for
public education about the role of antibiotic therapy (Seipel, Prohaska, Ruisinger, & Melton,
2019). In 2015 Mangione et. al. completed a cross sectional survey study in a pediatric setting in
Seattle WA. In this study they surveyed providers in parents after children were seen with a
diagnosis of upper respiratory infection. Their findings were the parents who had the highest
satisfaction ratings had received instructions on treatment for symptoms for their child and
discouragement from using antibiotic therapy for viral respiratory infections. When only
antibiotics were discouraged the satisfaction scores were lower. These findings show an
opportunity for education of the public on the role of antibiotic therapy and on symptom
management for viral infections.
Provider perceptions and education also play a role in the use of delayed prescribing for
antibiotics. In a 2016 study providers were more competent utilizing delayed prescribing after
they had received communication skills for discussing this strategy with patience, electronic
health record prompts and feedback on their prescribing habits (Vervloet, et al., 2016). Link et.
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al. 2016 utilized provider training exclusively on delayed prescribing with pretest and posttest
after 60-minute in person educational sessions. They then measured antibiotic prescribing rates
the two months prior and two months post after the education. The study found significant
decreases in antibiotic prescribing rates specifically for acute uncomplicated bronchitis. A 2016
qualitative study with semi-structured phone number use of 32 general practitioners revealed
patterns of perception about delayed prescribing. The findings were request for more consistency
in delayed prescribing strategies, increase in formal training on antibiotic stewardship and
feedback to providers on prescribing habits (Ryves, et al., 2016).Another qualitative study out of
Australia of primary care providers and pharmacists revealed further similarities on attitudes
towards delayed prescribing. The providers in this study reported the use of delayed prescribing
would be dependent upon the patient they were seeing and the patient stated expectations. The
pharmacist echoed this sentiment stating they would fill a delayed prescription early if the patient
insisted (Sargent, McCullough, Del Mar, & Lowe, 2017). A final qualitative study again out of
Australia, which has a high antibiotic prescribing rate overall, involved primary care trainees and
their supervisors. This study found that the supervisors use of delayed prescribing and attitudes
towards impacted the trainees use of this method. These findings also uncovered the supervisory
providers were better at-risk stratification in regards to which patients would be best suited for
delayed prescribing (Dallas, et al., 2020).
The review of literature shows delayed prescribing is an effective strategy at decreasing
overall antibiotic use. It is also multifactorial and has many players. The appropriate use is
dependent on the severity of illness, the receptiveness of the patient, the approach of the provider
and the reinforcement of the community pharmacist. There is great opportunity for additional
research in this area.
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METHODOLOGY
This project was conducted to measure the effectiveness of provider education to increase
the utilization of delayed prescribing as a method of antibiotic stewardship. Providers were
educated about delayed prescribing via a PowerPoint presentation and surveyed (Appendix C) on
their perceptions of this intervention. The medical records of all patients were queried to
uncover how often delayed prescribing was utilized after provider education.
Research design. This study was an evidenced based practice improvement project
utilizing the plan-do-study-act model to see if a new practice of delayed prescribing of antibiotics
would be utilized by advanced practice providers in an urgent care setting after they received
education and new patient instructions (Appendix B) were added to the electronic health record
system. In addition to an educational PowerPoint, which the providers self-reviewed, they also
completed a short survey on their perceptions of antibiotic stewardship and delayed prescribing.
A retrospective chart review was completed thirty days after provider training to see how often
patients were given delayed prescribing instructions with their antibiotic prescription.
Population and Location. This project was completed at three urgent care settings in
rural northwestern Pennsylvania. There were no exclusions for providers and seven chose to
participate. Exclusions for retrospective chart review were patients who were seen for physical
exams only.
Intervention, data collection and measurement. Providers at the three urgent care
locations provided email addresses to receive the delayed prescribing educational PowerPoint
presentation and Survey conducted on Survey Monkey. Upon completion of the PowerPoint and
Survey by the providers new patient instructions were added to the existing list of discharge
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instructions in the electronic health record. The patient instructions utilized were from the
CDC’s Antibiotic Stewardship for the Outpatient setting initiative (CDC, 2019). Reminder cards
were also place at each provider’s computer while the data was being collected. For thirty days
after education was completed the patient records were reviewed and a tally was completed of
how many times providers opted to chose the newly added delayed prescribing instructions for
patients upon discharge. This number was divided by the total number of patients seen to
determine a percentage of utilization.
Analysis. The provider surveys were evaluated to determine overall perceptions of
delayed prescribing and likelihood for providers to utilize. The retrospective chart reviews
provided data on frequency of use of the new patient instructions on delayed prescribing.
Ethical Considerations. This project was approved by IRB at Edinboro University. This
study was exempt from individual consent as no identifying information for patients was
collected and only the researcher had access to patient records. Deidentified data was housed on
a secure laptop. One cause of concern was patients being advised not to take antibiotics when
they were really necessary and could potentially delay needed treatment.

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RESULTS
This project was conducted to survey provider perceptions of delayed prescribing and
evaluate effectiveness of provider education in implementation of a new delayed prescribing
process to increase antibiotic stewardship. The first objective was an evaluation of the providers
knowledge and attitudes toward antibiotic stewardship and delayed prescribing. The second
objective was to evaluate use of new patient discharge instructions in the retrospective review of
the electronic health record after provider education was completed. The study included nine
advanced practice providers and reviewed 2,579 electronic charts over a thirty-day period.
Description of Study Sample Characteristics
Among the nine advanced practice providers who agreed to participate were seven
physician associates (PA’s) and two were nurse practitioners NPs). The range of years of
practice was three to seventeen. All participants practice in an urgent care group in rural
Northwestern Pennsylvania with three locations. The retrospective chart reviews were
completed over a thirty-day period from October to November of 2019. Patient visits for
physical exams relating to CDL licenses, driver’s licenses and school sports participation were
eliminated from the reviews as these patients would not have been prescribed antibiotics.
Research Questions
A. What are provider perceptions of antibiotic stewardship?
B. Will providers choose to utilize delayed prescribing as an antibiotic stewardship strategy
after education and addition of new patient discharge instructions in the electronic health
record?

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A survey with multiple choice and Likert Scale items was included as a link at the end of the
educational PowerPoint. Seven participants selected to view the survey and six opted to
complete it. The survey consisted of six questions and the first was asked if they would
participate in the survey to which six answered yes. Four participants reported currently using
delayed prescribing in their practice for question number two. Questions three through six were
Likert Style and detailed further overview of provider knowledge and attitude about delayed
prescribing and are detailed in the graphs below. Survey results demonstrated participants were
aware antibiotic resistance is a concern in healthcare and many currently practiced a form of
delayed prescribing. There was a positive trend toward using delayed prescribing by the
participants and most reported this method would be easy to incorporate.

Q 3. Antibiotic resistance is a
significant problem in healthcare

Q 4. Delayed prescribing is useful
method for promoting antibiotic
stewardship

3
3

2
2

STRONGLY AGREE

AGREE

0

0

0

NEITHER AGREE
OR DISAGREE

DISAGREE

STRONGLY
DISAGREE

STRONGLY AGREE

0

0

DISAGREE

STRONGLY
DISAGREE

3

3

1

1

1
0
AGREE

0
NEITHER AGREE
OR DISAGREE

Q. 6 I will be incorporating delayed
prescribing into my practice

Q. 5 Delayed prescribing will be easy
to incorporate into my practice

STRONGLY AGREE

AGREE

NEITHER AGREE
OR DISAGREE

1

0
DISAGREE

STRONGLY
DISAGREE

STRONGLY AGREE

AGREE

NEITHER AGREE
OR DISAGREE

0

0

DISAGREE

STRONGLY
DISAGREE

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The retrospective chart review focused on identifying which patients were provided
delayed prescribing instruction upon discharge. Prior to this study the electronic health record
was lacking formal delayed prescribing instructions. The data collected was limited to which
charts contained the new delayed prescribing instructions. Over a thirty-day period 2,957 charts
were reviewed for the three urgent care locations. Twenty-seven charts contained the new
instructions on delayed prescribing for a rate of utilization of 0.9%.

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DISCUSSION
This study was undertaken to evaluate provider perceptions of antibiotic stewardship
using delayed prescribing, to give provider education on delayed prescribing, and add
standardized patient instructions into the existing electronic health record. Prior to this project,
antibiotic stewardship had not been formally discussed in this practice setting and there were no
evidenced based, standardized patient instructions for use. Urgent Care Centers are desirable
setting for antibiotic stewardship initiatives as many patients per year seek care for episodic
illness at Urgent Care Centers.
Overall, the providers who agreed to be surveyed were aware of the need for antibiotic
stewardship and viewed delayed prescribing as a favorable method for the treatment of mild,
episodic illness which would be easy to implements. There was utilization of the new delayed
prescribing instructions sheets over the thirty days of chart reviews. Prior to this project the
electronic health record was lacking standardized, evidenced based instructions on delayed
prescribing. This addition was completed at no cost and provided immediate impact for better
antibiotic stewardship practices.
Limitations: This study’s first limitation was the size. Nine participants were recruited
and of those only five completed the survey. Future studies would be better served to include more
participants from outpatient settings such as primary care offices, emergency rooms and other
urgent care settings. A larger cohort would give additional perspectives for the survey too.
The second limitation was not analyzing provider and practice antibiotic prescribing trends
before and after intervention. Improvements for further research studies would be to measure
provider and practice antibiotic prescribing trends. Evaluation of practice antibiotic prescribing
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rates ahead of time would allow the intervention to occur before a period of historically high rates
of antibiotic prescribing Another beneficial measurement would be trending individual antibiotic
prescribing habits before the intervention and after. This information should be shared with each
provider with only their data identified and other provider’s data de-identified but still provided
for comparison. This data could include antibiotic prescribing habits regionally with diagnosis
included. This would give providers insight into their antibiotic prescribing habits compared to
their peers and would likely have more impact.
A third limitation was not including diagnosis and symptom data from the retrospective
chart review. To increase the effectiveness of this study patient diagnosis and symptom severity
and duration should have been included in the data. This would have allowed the researcher to
see the most common diagnosis and symptoms associated with antibiotic prescribing. This should
be shared with the participants as de-identified information to have increased impact on prescribing
habits. This could also prompt a discussion of which diagnosis and symptoms are consistent with
viral versus bacterial infections.
Oversight in failing to notifying local pharmacies of this study was the final limitation.
Local pharmacist could have been made aware of this research study and supported the initiative
when patients came to fill prescriptions. This intervention could also have included follow up with
the patient pharmacy listed in the electronic health record to see how many delayed prescriptions
were filled. Further follow up could have been completed with patients to see what prompted them
to fill their prescription.
Implications for Further Research Antibiotic stewardship is an important area of
research and initiatives to target prescribers is effective at increasing strategies to prevent

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unnecessary antibiotic use. This is especially important in the outpatient setting. This study with
the modifications identified in the limitations section would be easily replicated and have greater
impact. A future study should include practice trends and be implemented prior to a historically
high antibiotic use timeframe. It should provide data to the individual prescribers on their patterns
of antibiotic use compared to their peers. Patient data collected should include diagnosis and
duration along with severity of symptoms. A thorough review for the effectiveness of delayed
prescribing interventions would include follow up on number of prescriptions filled. Finally, the
data should be reviewed with the participants after completion of the study.
Conclusion Further studies with additional details need to be conducted on antibiotic
stewardship strategies as this issue is only growing. The outpatient setting remains the ideal place
to implement strategies to decrease antibiotic use as it is where most antibiotics are prescribed. By
decreasing unnecessary antibiotic use we can realize a multitude of benefits including; maintain
the effectiveness of our current antibiotics, decreasing adverse drug effects due to antibiotics and
realize a cost savings by prevention of the adverse drug effects. This remains a very important
initiative and it is multifaceted which provides many opportunities for research and education for
both prescribers of antibiotics and the patients who take them.

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Appendix A
Local Hospital Antibiogram

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Appendix B
Delayed Prescribing Patient Instructions

What is Delayed Prescribing?
WAIT. DO NOT FILL YOUR PRESCRIPTION JUST YET.
Your healthcare professional believes your illness may resolve on its own.
First, follow your healthcare professional’s recommendations to help you feel better without antibiotics.
Continue to monitor your symptoms over the next few days.
o
o
o
o
o

Rest.
Drink extra water and fluids.
Use a cool mist vaporizer or saline nasal spray to relieve congestion.
For sore throat in adults and older children, try ice chips, sore throat spray or lozenges.
Use honey to relieve cough. Do not give honey to infants younger than 1 year.

If you do not feel better in _______ days / hours or feel worse, go ahead and fill your prescription.
If you feel better, you do not need the antibiotic, and do not have to risk the side effects.

Waiting to see if you really need an antibiotic can help you take antibiotics only when needed. When
antibiotics aren’t needed, they won’t help you and the side effects could still hurt you. Common side
effects of antibiotics can include rash, dizziness, nausea, diarrhea and yeast infections.
Antibiotics save lives, and when a patient needs antibiotics, the benefits outweigh the risks of side
effects. You can protect yourself and others by learning when antibiotics are and are not needed.
To learn more about antibiotic prescribing and use, visit www.cdc.gov/antibiotic-use.

CDC, 2018

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DELAYED PRESCRIBING: PROMOTING ANTIBIOTIC STEWARDSHIP

Appendix C
Provider Survey Questions
Survey Post Education

Survey Post Education

1. Will you participate in this survey?
2. Do you currently use delayed prescribing for antibiotics in your practice?
For the following please rank:
1=strongly disagree
2=disagree
3=neutral
4=agree
5=strongly agree

3. Antibiotic resistance is a significant problem in healthcare

4. Delayed prescribing is useful method for promoting antibiotic stewardship

5. Delayed prescribing will be easy to incorporate into my practice

6. I will be incorporating delayed prescribing into my practice.

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