Background

Inappropriate antimicrobial use is common in the outpatient setting but often goes unaddressed by stewardship education. Residents might benefit from directed stewardship education.

Objective

We conducted a needs assessment of resident knowledge, attitudes, and behaviors regarding antibiotic use and stewardship in outpatient continuity clinics.

Methods

Internal medicine (IM) residents with continuity clinic at Minneapolis Veterans Affairs Health Care System were eligible. Antimicrobial prescriptions and number of visits were extracted from the Computerized Patient Record System (July 1, 2017–March 31, 2018). Antimicrobial rate (prescriptions per 1000 visits) was calculated for each resident. Results from a resident survey that included demographics, attitudes, and case-based multiple-choice knowledge questions were linked by unique identifier to antimicrobial rate.

Results

Prescription and visit data were available for 37 residents. Mean monthly antimicrobial rate was 51 prescriptions per 1000 visits (range 8–239). Surveys were completed by 19 residents (51%). Respondents were 32% female, 32% interns, and 11% international medical graduates. An online resource was most commonly used for prescribing guidance, whereas lectures and small group sessions for residents were rated as the most helpful educational modalities. Many respondents reported being unprepared to perform basic tasks related to antimicrobial stewardship. Median percentage correct was 57% of case-based knowledge questions (interquartile range 50%–71%).

Conclusions

Antimicrobial rates among IM residents at a VA outpatient continuity clinic are low and vary by provider. Residents agree with key antimicrobial stewardship concepts but lack preparation in tasks related to antimicrobial stewardship. Knowledge regarding antimicrobial prescribing was low.

The US Centers for Disease Control and Prevention estimates that 50% of outpatient antimicrobial prescriptions are inappropriate and 30% are completely unnecessary.1  The overuse of antimicrobials is an avoidable contributor to antimicrobial resistance,2  health care costs,3  and adverse drug events such as clostridioides difficile infection, allergy, kidney failure, and death.47  Antimicrobial stewardship is a crucial response to antimicrobial overprescribing and its deleterious effects. Stewardship began in the acute setting, but 80% of inappropriate antimicrobial prescribing occurs outpatient.8  Optimal outpatient stewardship is largely undefined.9  Inpatient stewardship directed at family medicine and internal medicine (IM) resident physicians improved guideline-concordant prescribing10 ; however, no studies have described similar outpatient programs. IM residents in the United States have reported a high degree of prescribing autonomy,11  making them a key target for stewardship education.

Antimicrobial stewardship training focused on IM residents is currently limited but relates directly to the Accreditation Council for Graduate Medical Education Milestones.12  Training focused on clinical knowledge (milestone 6) necessary for antimicrobial stewardship is lacking; one study across multiple residency and fellowship programs found less than 1% of learning topics were related to antimicrobial stewardship except in infectious diseases programs.13  Similarly, 22% of residents from multiple specialties reported no antimicrobial education within the last year.14  Several studies using case-based quizzes showed that resident knowledge was poor, with 28% to 60% responding correctly.1416  Additionally, 90% of residents reported desiring more antimicrobial education, and 67% desired feedback on their own prescribing.14 

Due to the gap in antimicrobial stewardship education directed to resident physicians, we undertook this study. This pilot study describes needs assessment of outpatient antimicrobial stewardship training for IM residents as preparation for educational interventions to manage patients (milestone 3), monitor self-practice (milestone 12), improve systems (milestone 10), and learn via feedback (milestone 15).12  We assessed a priori the correlation between level of training, site of training, and percentage correct on knowledge questions with antibiotic prescribing.

All University of Minnesota IM resident physicians with outpatient continuity clinic at the Minneapolis Veterans Affairs Health Care System (MVAHCS) as of July 2017 were eligible for enrollment (n = 37). Continuity clinic at MVAHCS involves a half day of scheduled appointments (no same-day appointments) with access to point-of-care antimicrobial decision support software tied to order entry.

The MVAHCS Institutional Review Board approved the survey as minimal-risk research and exempted prescription monitoring as quality improvement.

All outpatient resident antimicrobial prescriptions were extracted from the Computerized Patient Record System (CPRS) at MVAHCS with those outside of continuity clinic excluded from analysis. Prescriptions were deidentified and recorded monthly. Continuity clinic visits were extracted from CPRS. Antimicrobial rate was calculated as prescriptions per 1000 patient visits averaged over the 9 months of the study. Verbal informed consent was obtained for a paper survey with a unique identifier to link responses with individual prescribing data. Two survey reminder emails were sent.

Measurement Instrument

Survey questions (provided as online supplemental material) were developed with permission from a subset of 75 questions in a published unvalidated study.16  Twenty-one questions covered demographics (n = 5), attitudes (n = 5), and stewardship knowledge (n = 11). Attitude questions, unaltered from the previous survey, rated 39 statements regarding antimicrobial stewardship, terminology, and educational resources via 5-point Likert scales. Knowledge questions were brief clinical vignettes with multiple choice answers designed based on Infectious Diseases Society of America guidelines when available17,18  to span antimicrobial stewardship concepts such as spectrum of activity, de-escalation of empiric antimicrobials, and effective use of laboratory testing. These questions were reviewed by 4 infectious disease specialists, an infectious disease fellow, and an epidemiologist involved in statewide antimicrobial stewardship initiatives who provided feedback, modified, and came to consensus on the final survey items. The survey was pretested with several chief residents to determine administration time and clarify ambiguous wording.

Statistical Analysis

Responses were characterized by descriptive statistics. Correlations between antibiotic prescribing rate, percentage correct, and demographic variables were chosen a priori, with a P value of .05 considered to be significant, and calculated using Pearson's correlation coefficients in SAS 9.4 (SAS Institute Inc, Cary, NC).

All 37 IM residents at the site participated from July 1, 2017 to March 31, 2018. Mean antibiotic prescribing rate was 51 of 1000 patient visits (range 8 to 239). During 3604 patient visits, 182 individual antimicrobials were prescribed. Residents saw 1 to 6 patients per half-day session. On average, each resident prescribed 5 antimicrobials during the 9-month period. The most common antibiotics prescribed were doxycycline (n = 41), acyclovir (n = 15), then amoxicillin, azithromycin, and valacyclovir (n = 12 each). The median duration for antimicrobials was 10 days, and the mode was 5.

Nineteen of 37 residents responded to the survey (51%). Mean age was 30 years (range 26–35). There were 6 female respondents (32%). Respondents were in postgraduate year 1 (32%, 6 of 19), 2 (26%, 5 of 19), and 3 (42%, 8 of 19). Two respondents completed medical school internationally (11%, 2 of 19). Respondent attitudes are presented in the Figure. Forty-seven percent of respondents (9 of 19) felt they could easily explain the term “antimicrobial stewardship,” while 53% (10 of 19) reported a general sense of what the term meant.

Figure

Attitudes Toward Antimicrobial Stewardship

Note: All numbers displayed are percentages of respondents (n = 19).

Figure

Attitudes Toward Antimicrobial Stewardship

Note: All numbers displayed are percentages of respondents (n = 19).

Close modal

Of 11 knowledge questions, the median percentage correct was 57% (interquartile range 50%–71%). Variation in correct answers to individual questions was high. All respondents answered 2 questions (PO to IV conversion and perioperative antibiotics) correctly. There was one correct response to a question assessing guideline-concordant vancomycin use. Knowledge of mechanisms of resistance to antimicrobials was low (21%–47% correct).

Advancing level of training did not correlate with antimicrobial prescribing rates. Interestingly, increased training level correlated with decreased percentage correct on knowledge questions (P = .010). Site of medical school training had no correlation with antimicrobial rate or percentage correct on knowledge questions. Antimicrobial prescribing rates did not correlate with percentage correct on knowledge questions.

Antimicrobial prescribing rates varied widely among resident physicians; however, on average, antimicrobial prescription rate was 51 per 1000 patient visits. No previous studies have found such a low prescribing rate. An appropriate rate of prescribing in resident clinic is unknown. A study of outpatient general IM clinics found that nationally the antibiotic prescription rate is 506 per 1000 patient visits.1  A 1-day continuity clinic on a fixed day may not be a common place for patients to present with acute infections, due to availability of same-day walk-in clinics and the emergency department at MVAHCS. Antimicrobial prescription rates are likely affected by a multitude of variables, but in our study did not correlate with level of training, medical school site, or knowledge. However, our small numbers may not provide enough power to detect these correlations.

Assessing knowledge, attitudes, and prescribing rates was the first step toward an educational program for IM residents to begin outpatient antimicrobial stewardship education at MVAHCS. We found that IM residents have low knowledge, agree with antimicrobial stewardship concepts, and desire additional knowledge. Low knowledge (61% correct) is consistent with other studies of resident knowledge, which reported scores of 28%–60%.1416  Correct responses varied by topic, with topics such as mechanisms of antibiotic resistance presenting challenges for many respondents. These apparent knowledge gaps provide targets for further educational interventions. Possible interventions include small group skills sessions, academic detailing, and prospective audit and feedback.

Limitations of this study include the small sample of participants from a single site over a short time period. Survey data were obtained through self-report and also based on an unvalidated survey adapted from a previously published 75-question survey instrument.16  Our population and clinic type limits application of this study to other clinic settings, which may be more heterogeneous and have more acute infectious visits (no walk-in or same-day appointments available). Resident physicians work with multiple attending physicians who may also influence resident prescribing.

Antimicrobial prescribing in an IM resident VA clinic was variable and lower than expected. Although residents agree with many antimicrobial stewardship concepts, they feel unprepared for specific tasks. Knowledge regarding antimicrobial prescribing was similar to other studies at 61% correct.

1
Fleming-Dutra
KE,
Hersh
AL,
Shapiro
DJ,
Bartoces
M,
Enns
EA,
File
TM
Jr,
et al.
Prevalence of inappropriate antibiotic prescriptions among US ambulatory care visits, 2010–2011
.
JAMA
.
2016
;
315
(
17
):
1864
1873
. doi:.
2
Lipsitch
M,
Samore
MH.
Antimicrobial use and antimicrobial resistance: a population perspective
.
Emerg Infect Dis
.
2002
;
8
(
4
):
347
354
. doi:.
3
Michaelidis
CI,
Fine
MJ,
Lin
CJ,
Linder
JA,
Nowalk
MP,
Shields
RK,
et al.
The hidden societal cost of antibiotic resistance per antibiotic prescribed in the United States: an exploratory analysis
.
BMC Infect Dis
.
2016
;
16
(
1
):
655
. doi:.
4
Tamma
PD,
Avdic
E,
Li
DX,
Dzintars
K,
Cosgrove
SE.
Association of adverse events with antibiotic use in hospitalized patients
.
JAMA Intern Med
.
2017
;
177
(
9
):
1308
1315
. doi:.
5
Cunha
BA.
Antibiotic side effects
.
Med Clin North Am
.
2001
;
85
(
1
):
149
185
. doi:.
6
Luther
MK,
Timbrook
TT,
Caffrey
AR,
Dosa
D,
Lodise
TP,
LaPlante
KL.
Vancomycin plus piperacillin-tazobactam and acute kidney injury in adults: a systematic review and meta-analysis
.
Crit Care Med
.
2018
;
46
(
1
):
12
20
. doi:.
7
Chou
HW,
Wang
JL,
Chang
CH,
Lai
CL,
Lai
MS,
Chan
KA.
Risks of cardiac arrhythmia and mortality among patients using new-generation macrolides, fluoroquinolones, and beta-lactam/beta-lactamase inhibitors: a Taiwanese nationwide study
.
Clin Infect Dis
.
2015
;
60
(
4
):
566
577
. doi:.
8
Sanchez
GV,
Fleming-Dutra
KE,
Roberts
RM,
Hicks
LA.
Core elements of outpatient antibiotic stewardship
.
MMWR Recomm Rep
.
2016
;
65
(
6
):
1
12
. doi:.
9
Drekonja
DM,
Filice
GA,
Greer
N,
Olson
A,
MacDonald
R,
Rutks
I,
et al.
Antimicrobial stewardship in outpatient settings: a systematic review
.
Infect Control Hosp Epidemiol
.
2015
;
36
(
2
):
142
152
. doi:.
10
VanLangen
KM,
Dumkow
LE,
Axford
KL,
Havlichek
DH,
Baker
JJ,
Drobish
IC,
et al.
Evaluation of a multifaceted approach to antimicrobial stewardship education methods for medical residents
.
Infect Control Hosp Epidemiol
.
2019
;
40
(
11
):
1236
1241
. doi:.
11
Laake
AM,
Bernabe
G,
Peterson
J,
Liappis
AP.
Internal medicine resident perspectives regarding broad-spectrum antibiotic usage
.
Open Forum Infect Dis.
2017
;
4(2):ofx060.
doi:.
12
The Accreditation Council for Graduate Medical Education, The American Board of Internal Medicine
.
The Internal Medicine Milestone Project
. ,
2020
.
13
Rawson
TM,
Butters
TP,
Moore
LS,
Castro-Sanchez
E,
Cooke
FJ,
Holmes
AH.
Exploring the coverage of antimicrobial stewardship across UK clinical postgraduate training curricula
.
J Antimicrob Chemother
.
2016
;
71
(
11
):
3284
3292
. doi:.
14
Srinivasan
A,
Song
X,
Richards
A,
Sinkowitz-Cochran
R,
Cardo
D,
Rand
C.
A survey of knowledge, attitudes, and beliefs of house staff physicians from various specialties concerning antimicrobial use and resistance
.
Arch Intern Med
.
2004
;
164
(
13
):
1451
1456
. doi:.
15
Drekonja
DM,
Abbo
LM,
Kuskowski
MA,
Gnadt
C,
Shukla
B,
Johnson
JR.
A survey of resident physicians' knowledge regarding urine testing and subsequent antimicrobial treatment
.
Am J Infect Control
.
2013
;
41
(
10
):
892
896
. doi:.
16
Abbo
L,
Sinkowitz-Cochran
R,
Smith
L,
Ariza-Heredia
E,
Gómez-Marín
O,
Srinivasan
A,
et al.
Faculty and resident physicians' attitudes, perceptions, and knowledge about antimicrobial use and resistance
.
Infect Control Hosp Epidemiol
.
2011
;
32
(
7
):
714
718
. doi:.
17
Rybak
MJ,
Lomaestro
BM,
Rotschafer
JC,
Moellering
RC,
Craig
WA,
Billeter
M,
et al.
Vancomycin therapeutic guidelines: a summary of consensus recommendations from the infectious diseases Society of America, the American Society of Health-System Pharmacists, and the Society of Infectious Diseases Pharmacists
.
Clin Infect Dis
.
2009
;
49
(
3
):
325
327
. doi:.
18
Shulman
ST,
Bisno
AL,
Clegg
HW,
Gerber
MA,
Kaplan
EL,
Lee
G,
et al.
Clinical practice guideline for the diagnosis and management of group A streptococcal pharyngitis: 2012 update by the Infectious Diseases Society of America
.
Clin Infect Dis
.
2012
;
55
(
10
):
1279
1282
. doi:.

Author notes

Editor's Note: The online version of this article contains the survey used in the study.

Funding: This project was funded by the National Institutes of Health T32AI055433 award and the resources of the Minneapolis VA Health Care System.

Competing Interests

Conflict of interest: The authors declare they have no competing interests.

These data were previously presented partially as a poster at the St Jude/Pediatric Infectious Disease Society Research Conference, Memphis, Tennessee, March 13–14, 2020.

The authors would like to thank Dr. Ruth Lynfield for her support with study design, Amy Gravely for her support with statistical analysis, and Anders Westanmo for his support with extraction of antimicrobial prescriptions.

Supplementary data