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RESEARCH ARTICLE

Physicians’ Use of Evidence-Based Strategies


to Increase Adult Vaccination Uptake
Laura P. Hurley, MD, MPH,1,2 Megan C. Lindley, MPH,3 Mandy A. Allison, MD, MPH,1,4
Sean T. O’Leary, MD, MPH,1,4 Lori A. Crane, PhD, MPH,1,5 Michaela Brtnikova, PhD, MPH,1,4
Brenda L. Beaty, MSPH,1 Allison Kempe, MD, MPH1,4

Introduction: This study assesses the following among primary care physicians: (1) the use of evi-
dence-based strategies to improve adult vaccination rates, (2) the number of strategies employed
simultaneously, and (3) characteristics associated with assessing adult vaccinations at each visit.

Methods: An internet and mail survey was administered between December 2015 and January
2016 on primary care physicians designed to be representative of the American College of Physi-
cians and American Academy of Family Physicians memberships. Data analysis was conducted in
2019.

Results: The response rate was 66% (617 of 935); 94% reported using electronic health records.
Standing orders (84%) and electronic provider reminders at a visit (61%) were the most common
strategies reported for influenza vaccine. Electronic provider reminders at a visit (53%) and record-
ing a vaccination in an immunization registry (32%) were the most common strategies reported for
all noninfluenza vaccines. Most physicians reported using 2 or more strategies, although this was
more common for influenza (74%) than for noninfluenza (62%) vaccines. In multivariable analysis,
physicians who reported assessing adult vaccinations at every patient visit were more likely to work
in practices where decisions about purchasing and handling vaccines were made at a larger system
level (RR=1.20, 95% CI=1.04,1.40), and they reported using electronic provider reminders
(RR=1.38, 95% CI=1.15, 1.69) and standing orders (RR=1.45, 95% CI=1.21, 1.75) for all nonin-
fluenza adult vaccines.
Conclusions: Several strategies are being used to increase adult vaccination, particularly for the
influenza vaccine. Investment in implementing standing orders and electronic clinical decision sup-
port for all routine adult vaccinations could help facilitate assessment of adult vaccinations at each
visit and potentially improve adult vaccination rates.
Am J Prev Med 2020;59(3):e95−e103. © 2020 American Journal of Preventive Medicine. Published by Elsevier
Inc. All rights reserved.

INTRODUCTION From the 1Adult and Child Consortium for Health Outcomes Research
and Delivery Science, University of Colorado Anschutz Medical Campus

M
any adults in the U.S. do not receive rou- and Children’s Hospital Colorado, Aurora, Colorado; 2Division of General
tinely recommended vaccinations. To give 2 Internal Medicine, Denver Health, Denver, Colorado; 3National Center
examples, as of 2017, the U.S was falling well for Immunization and Respiratory Diseases, Centers for Disease Control
short of meeting the Healthy People 2020 goals of vacci- and Prevention, Atlanta, Georgia; 4Department of Pediatrics Children’s
Hospital Colorado, Aurora, Colorado; and 5Department of Community
nating 70% of adults annually against seasonal influenza and Behavioral Health, University of Colorado Anschutz Medical Cam-
and 90% of adults aged ≥65 years against pneumococcal pus, Aurora, Colorado
disease, with only 45% and 69% of adults receiving these Address correspondence to: Laura P. Hurley, MD, MPH, Denver
vaccines, respectively.1,2 The Centers for Disease Control Health, 301 W 6th Avenue, MC3251, Denver CO 80204. E-mail:
laura.hurley@dhha.org.
and Prevention and Immunization Action Coalition 0749-3797/$36.00
believe that broader implementation of evidence-based https://doi.org/10.1016/j.amepre.2020.03.020

© 2020 American Journal of Preventive Medicine. Published by Elsevier Inc. All rights Am J Prev Med 2020;59(3):e95−e103 e95
reserved.
e96 Hurley et al / Am J Prev Med 2020;59(3):e95−e103
strategies to improve vaccination rates might address networks intended to be representative of the American College
this problem2,3 and could act synergistically with the of Physicians and the American Academy of Family Physician
current standards for adult immunization3 calling for memberships.11,12 These physician networks are similar to physi-
every provider who sees adult patients to assess, recom- cians randomly sampled from the American Medical Association
Masterfile with respect to demographics and attitudes regarding
mend, and administer or refer for needed vaccines at vaccines.11 Census location for each physician is determined on
every visit in order to increase rates of vaccination. the basis of self-reported ZIP code, which is then matched with
Several evidence-based strategies are recommended the most recent census location results. The human subjects
by the U.S. Community Preventive Services Task Force.4 review board at the University of Colorado Anschutz Medical
Five examples include: Campus approved this study as exempt research.

1. Client reminder/recall; Measures


2. Assessment and feedback where vaccine providers are The survey assessed the use of the following 5 evidence-based
given information about their performance on deliv- strategies: (1) client reminder/recall, (2) standing orders, (3)
ering a vaccine or vaccines to a patient population; assessment and feedback, (4) the use of an IIS to assess and record
3. Provider reminders to deliver vaccines at the time of a vaccinations, and (5) provider reminders in the form of electronic
clinical decision support. Physicians were asked about evidence-
visit;
based strategies used for influenza and noninfluenza vaccinations
4. Use of immunization information systems (IISs); and separately, as there may be different approaches for an annually
5. Standing orders4 to permit nonphysician staff to pre- recommended vaccine versus other routinely recommended vac-
scribe and administer vaccinations. cines. The response options for whether a strategy was being used
for influenza vaccination were yes or no, whereas for the other
routine vaccinations, the response options were yes for all, yes for
IISs are confidential, population-based, computerized some, or no. The survey was pretested by a physician advisory
databases that record all immunization doses adminis- board and piloted among a national sample of primary care physi-
tered by participating vaccine providers to people resid- cians.
ing within a given geopolitical area.5 On the basis of physician preference, the survey was sent over
Little is known about provider use of these strategies the internet or through U.S. mail. The internet group was sent an
in adult care. Previous studies, primarily focusing on initial e-mail with up to 8 e-mail reminders, and the U.S mail
group was sent an initial mailing and up to 2 additional
one strategy at a time, have indicated that client
reminders. Nonrespondents in the internet group were also sent
reminder/recall,6 standing orders,7,8 and IISs9,10 are up to 2 surveys by post in case of problems with e-mail correspon-
underutilized. No prior studies have quantified the use dence. The mail protocol was patterned on Dillman’s tailored
of evidence-based strategies to improve vaccinations design method.13 The survey was administered from December
more comprehensively both in terms of the breadth of 2015 to January 2016.
strategies utilized and the vaccinations targeted.
The objectives of this study are to assess the following Statistical Analysis
among primary care physicians, including general Analyses were conducted from April to October 2019. Results
internists and family physicians: were similar by specialty and, so, are presented together. Respond-
ents and nonrespondents were compared on all available charac-
1. The use of evidence-based strategies to improve adult teristics using t-tests, chi-square tests, and Wilcoxon tests, as
vaccination rates; appropriate. In quantifying the number of evidence-based strate-
gies a physician used, it was counted as 1 strategy if a physician
2. The number of strategies being employed simulta- reminded all patients or just high-risk groups to be vaccinated, if
neously; and a physician received lists of all patients or just high-risk groups
3. The characteristics associated with assessing adult needing a vaccine, and if a physician used an IIS to assess or docu-
vaccination status at each visit, which is one of the ment vaccination information. Multivariable regression was con-
proposed standards for adult immunization for all ducted where the dependent variable was assessing vaccination
healthcare professionals.3 status at every visit, including acute care. Independent variables
included physician’s age, sex, practice specialty, number of pro-
viders in practice, practice location (urban or rural) and setting,
region, decision-making capacity regarding the purchasing and
METHODS handling of vaccines, and reported use of evidence-based strate-
gies to improve noninfluenza routinely recommended adult
Study Population vaccines.
The Vaccine Policy Collaborative Initiative, a survey entity to Respondents were excluded from the multivariable model if
assess physician practice and attitudes about vaccines and vaccine they did not answer the outcome variable question, if they
policy, in collaboration with the Centers for Disease Control and reported not using an electronic health record (EHR), and if they
Prevention designed and conducted a survey among physician answered fewer than 6 of the 8 questions that were asked about

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Hurley et al / Am J Prev Med 2020;59(3):e95−e103 e97
using evidence-based methods. Because the outcome was com- physicians from private practices or practicing in the
mon, log-binomial (SAS PROC GENMOD) was used to generate South were less likely to respond, whereas physicians
RRs instead of ORs because ORs overestimate effect size for com- from the Midwest or larger practices were more likely to
mon outcomes. A cut off of p<0.25 was used in bivariate analysis respond. These data are very similar to national esti-
for including variables in the model. A backward elimination pro-
cedure was used, in which the least significant predictor in the
mates of practice setting for primary care physicians.14
model was eliminated sequentially. At each step, estimates were A total of 15 respondents reported not administering
checked to ensure that other variables were not affected by drop- adult vaccinations and were excluded from further anal-
ping the least significant variable. The final model retained only ysis, leaving a final sample of 602 physicians.
variables that were significant at p<0.05. All analyses were per- Standing orders and provider reminders at the time of
formed using SAS, version 9.4. the visit in the form of electronic clinical decision sup-
port were the most common strategies reported for sea-
RESULTS sonal influenza vaccination (Table 2). The use of an
The overall response rate was 66% (617 of 935); 64% electronic clinical decision support system and recording
(293 of 455) for family physicians and 68% (324 of 480) vaccinations in an IIS were the most common strategies
for general internists. Characteristics of respondents and reported for all noninfluenza vaccinations. More
nonrespondents are shown in Table 1. Respondents and physicians reported using reminder/recall and standing
nonrespondents did not differ by census location (urban, orders for influenza than for noninfluenza routinely rec-
suburban, or rural). Male and older physicians and ommended vaccines. Five percent of physicians reported

Table 1. Demographic and Practice Characteristics of Survey Respondents, U.S., 2016

Characteristic Respondents(n=617) Nonrespondents(n=318) p-value


Age of provider, years, mean (SD) 53.5 (8.6) 55.3 (8.3) 0.003
Male, % 54 63 0.01
Specialty
FP 47 51 0.32
GIM 53 49
Region, %a
Midwest 27 22 0.03
Northeast 18 20
South 31 40
West 23 19
Location of practice, %a
Urban 47 45 0.68
Suburban 48 50
Rural 5 6
Practice setting, %a
Private practice 71 79 0.02
Hospital/clinic 22 14
HMO 6 7
Number of providers in your practice, median (IQR) 6 (3‒12) 5 (2‒10) 0.002b
Decisions are made about purchasing and handling vaccines, %
Independently 55 63 0.02
At a larger system level 45 37
Physicians providing vaccines to adults, % 98 N/A
When do you or when does someone in your practice usually assess
an adult patient’s vaccination status?
Initial visit 90 N/A
Annual visit 95
Every visit 56
Practice uses an EMR/EHR, % 94 N/A
Note: Boldface indicates statistical significance p<0.05 between respondents and nonrespondents.
a
Percentages may not add to 100% owing to rounding.
b
Wilcoxon test used.
EHR, electronic health record; EMR, electronic medical record; FP, family physicians; GIM, general internists; N/A, not applicable.

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Table 2. Physician Reported Use of Strategies to Improve Adult Vaccination, U.S. 2016, n=602

Some of the None of the


All noninfluenza noninfluenza noninfluenza
routinely routinely routinely
Influenza recommended recommended recommended
Evidence-based strategy vaccine (%) adult vaccines (%) adult vaccines (%) adult vaccines (%)
Strategies to increase patient demand
for vaccine
Written, telephone, or e-mail 23 9 11 80
vaccination reminders are sent to all
adult patients in the practice who
are due for vaccine(s)a
Written, telephone, or e-mail 23 10 13 77
vaccination reminders are sent to
subgroups of high-risk adult patients
in the practice who are due for
vaccine(s)a
Strategies directed at the provider or
healthcare system
Standing orders (i.e., nonphysician 84 16 41 43
staff use a protocol to prescribe and
deliver vaccinations to patients)
Physicians are provided a list 16 12 8 80
showing them when all of their adult
patients are due or overdue for
vaccination(s)b
Physicians are provided a list 16 10 9 81
showing them when subgroups of
high-risk adult patients in the
practice are due for vaccination(s)b
A state or regional IIS is used to 26 25 8 67
assess an adult patient’s
vaccination status
A state or regional IIS is used to 32 32 3 64
record vaccination(s) an adult
patient receives in your practice
An electronic clinical decision 61 53 12 36
support system is used to help
determine if an adult patient needs
a vaccine(s) at the time of the visitc
a
Client reminder/recall.
b
Assessment and feedback.
c
Provider reminder.
IIS, Immunization Information System

not using any strategies to increase rates for both rou- where decisions about purchasing and handling of vac-
tinely administered influenza and noninfluenza vaccina- cines were made at a larger system level (RR=1.20, 95%
tions (data not shown). CI=1.04, 1.40), and they reported using electronic clini-
Seventy-four percent and 62% of the respondents cal decision support (RR=1.38, 95% CI=1.15, 1.69) and
reported employing 2 or more strategies to increase standing orders (RR=1.45, 95% CI=1.21, 1.75) for all
influenza and noninfluenza vaccination rates, respec- noninfluenza adult vaccines.
tively (Figure 1). Almost 20% of the respondents
reported using 4 or more strategies for both influenza
and noninfluenza vaccinations.
DISCUSSION
The results of the multivariable analysis are presented This is one of the few studies to assess physicians’ use of
in Table 3. A total of 74 respondents were not included evidence-based strategies to improve adult vaccination,
in the model as they did not meet prespecified criteria. including influenza and other adult vaccines. The vast
Physicians who reported assessing adult vaccination sta- majority of physicians reported using standing orders to
tus at each visit were more likely to work in practices help deliver influenza vaccine to their adult patients.

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Hurley et al / Am J Prev Med 2020;59(3):e95−e103 e99

Figure 1. Reported number of strategiesa used to improve influenza and noninfluenza adult vaccine rates, U.S., 2016, n=602.b
a
Strategies included client reminder/recall, standing orders, assessment and feedback, use of an IIS to assess and/or record vaccinations, and pro-
vider reminders.
b
Percentages may not add to 100% owing to rounding.
IIS, Immunization Information System.

Slightly more than half of the physicians reported using consistency of using standing orders and credited physi-
electronic provider reminders at the time of visit for cians only for using standing orders if they were used
influenza and all other routinely recommended adult consistently. This present study investigated whether
vaccines. Most of the physicians reported using at least 2 standing orders were used and therefore likely obtained
strategies to aid adult vaccination efforts, but many a less conservative estimate of standing order use. Stand-
reported not using certain evidence-based strategies, ing order use for the noninfluenza vaccines was not as
including IISs. extensive as for influenza vaccine in this study, with 57%
Few previous studies have reported physicians’ use of using standing orders for some or all noninfluenza vac-
evidence-based strategies to improve adult vaccination. cines. This is possibly because many noninfluenza vac-
A national survey of primary care physicians sampled cine recommendations for adults are risk-based (e.g.,
from the American Medical Association Masterfile and hepatitis B vaccine and pneumococcal for adults aged 19
conducted in 2009 found that 23% of physicians used −64 years) or have different preferred venues of vaccina-
standing orders for both influenza and pneumococcal tion (medical home versus the pharmacy) on the basis of
vaccine and 20% used them for influenza vaccine only; insurance coverage (e.g., zoster vaccine being covered by
the use of standing orders for other routinely recom- Medicare Part D for Medicare beneficiaries), making it
mended vaccines was not assessed.7 In this study, 84% of more difficult to implement a standing order.
the respondents reported using standing orders for influ- This study showed similarly low rates of IIS use for
enza, quadruple of what was previously observed. A assessing and recording adult vaccination information
notable difference between this study and that of Albert compared with a survey that focused on IIS use among
and colleagues7 is that the latter investigated the pediatricians, family physicians, and general internists

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Table 3. Characteristics of Physicians Who Reported Assessing Adult Vaccination Status at Each Visit (n=528)

Assess adult vaccination status at every visit


Bivariate
Variable No(n=230) Yes(n=298) p-value RR (95% CI)
Age of provider, years, mean (SD) 53.2 (9.0) 53.0 (8.3) 0.79
Sex
Female 45% (103) 48% (144) 0.42
Male 55% (127) 52% (154)
Practice specialty
FP 48% (111) 45% (134) 0.45
GIM 52% (119) 55% (164)
Practice setting
University/hospital/public/other 17% (38) 26% (77) 0.002
HMO 4% (10) 9% (26)
Private practice 79% (182) 65% (195)
Census location
Rural 6% (13) 4% (13) 0.15
Urban‒non-inner city 52% (120) 45% (134)
Urban-inner city 42% (97) 51% (151)
Region
Midwest 26% (59) 29% (86) 0.23
Northeast 18% (41) 18% (53)
South 36% (83) 28% (84)
West 20% (47) 25% (75)
Number of providers in your practice, median (IQR) 6.0 (3.0‒12.5) 7.0 (4.0‒15.0) 0.009a
Decisions are made about purchasing and handling
of vaccines
Independently 60% (136) 46% (135) 0.001 Ref
At a larger system level 40% (92) 54% (161) 1.20 (1.04, 1.40)
A state or regional IIS is used to assess an adult
patient’s vaccination status
Yes, for all noninfluenza adult vaccines 24% (55) 28% (81) 0.26
Yes, for some noninfluenza adult vaccines 10% (23) 7% (19)
No 65% (148) 66% (191)
A state or regional IIS is used to record vaccination(s)
an adult patient receives in your practice
Yes, for all noninfluenza adult vaccines 33% (72) 34% (101) 0.39
Yes, for some noninfluenza adult vaccines 5% (11) 3% (8)
No 62% (137) 63% (187)
An electronic clinical decision support system is
used to help determine if an adult patient needs a
vaccine(s) at the time of the visit
Yes, for all noninfluenza adult vaccines 45% (100) 64% (189) <0.001 1.38 (1.15, 1.69)
Yes, for some noninfluenza adult vaccines 14% (31) 12% (34) 1.09 (0.80, 1.43)
No 42% (93) 24% (71) Ref
Written, telephone, or e-mail vaccination reminders
are sent to all adult patients in the practice who are
due for vaccine(s)
Yes, for all noninfluenza adult vaccines 4% (8) 14% (40) <0.001
Yes, for some noninfluenza adult vaccines 10% (22) 12% (36)
No 87% (198) 74% (218)
Written, telephone, or e-mail vaccination reminders
are sent to subgroups of high-risk adult patients in
the practice who are due for vaccine(s)
Yes, for all noninfluenza adult vaccines 6% (14) 14% (39) 0.017

(continued on next page)

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Hurley et al / Am J Prev Med 2020;59(3):e95−e103 e101

Table 3. Characteristics of Physicians Who Reported Assessing Adult Vaccination Status at Each Visit (n=528) (continued)

Assess adult vaccination status at every visit


Bivariate
Variable No(n=230) Yes(n=298) p-value RR (95% CI)
Yes, for some noninfluenza adult vaccines 13% (29) 15% (43)
No 81% (183) 72% (210)
Physicians are provided a list showing them when all
of their adult patients are due or overdue for
vaccination(s)
Yes, for all noninfluenza adult vaccines 6% (13) 16% (47) <0.001
Yes, for some noninfluenza adult vaccines 7% (17) 9% (25)
No 87% (197) 75% (218)
Physicians are provided a list showing them when
subgroups of high-risk adult patients in the practice
are due for vaccination(s)
Yes, for all noninfluenza adult vaccines 5% (11) 14% (41) 0.002
Yes, for some noninfluenza adult vaccines 9% (21) 10% (29)
No 86% (196) 76% (221)
Standing orders (i.e., nonphysician staff use a
protocol to prescribe and deliver vaccinations to
patients)
Yes, for all noninfluenza adult vaccines 10% (24) 22% (65) <0.001 1.45 (1.2, 1.75)
Yes, for some noninfluenza adult vaccines 39% (90) 43% (126) 1.19 (1.00, 1.42)
No 50% (115) 35% (104) Ref
Note: Boldface indicates statistical significance (p<0.05).
a
Wilcoxon test used.
FP, family physicians; GIM, general internists; IIS, Immunization Information System.

using the same methodology.10 It also expands on earlier demonstrating the efficacy of these strategies is now dec-
literature because questions were asked about types of ades old, and the healthcare landscape has changed dra-
vaccines for which the IIS is used. There were no differ- matically with the wide adoption of EHRs. In 2012,
ences in the use of IISs for influenza and noninfluenza recognizing the importance of provider’s recommenda-
vaccines despite an IIS being a potentially useful tool to tion and offer of vaccine at the same visit18,19 and want-
identify vaccines delivered outside the medical home— ing to provide a pathway for improving adult
as often occurs for influenza vaccine15—given that many vaccination rates, the National Vaccine Advisory Com-
EHRs are not yet linked to IIS. mittee published Standards for Adult Immunization
Very few physicians reported using client reminder/ Practice.3 One of the recommended standards is to
recall systems either for all patients or for high-risk incorporate immunization needs assessment into every
patients, but approximately twice the number of physi- clinical encounter.3 The multivariable analysis offers a
cians reported using these systems for influenza than for window into what strategies might be most useful to
noninfluenza vaccines. Previous work has demonstrated adhere to this standard. Using standing orders and elec-
that client reminder/recall has been underused for pedi- tronic clinical decision support were both associated
atric (16% of pediatricians reporting usage)16 and ado- with checking adult vaccination status at each visit. Pre-
lescent patients (24% of pediatricians and 18% of family vious work has demonstrated the impact of provider
physicians reporting usage)17 in national studies; the use reminders (a proxy for electronic clinical decision sup-
of client reminder/recall among general internists has port) in that they alone can independently increase vac-
not been previously documented. There were no data to cinations for influenza, pneumococcal polysaccharide,
compare with this study’s data regarding the use of and hepatitis B in high-risk adults, whereas other strate-
assessment and feedback and electronic provider gies must be combined to improve vaccination rates.20
reminders for adult vaccination. Similarly, EHR prompts have specifically been shown to
Most physicians in this study were using at least 2 improve human papillomavirus vaccination in adoles-
strategies, and nearly 20% were using 4 or more, suggest- cents and young adults21 and hepatitis B vaccination ini-
ing that despite low national rates, there is a substantial tiation and completion in diabetic patients aged 19
effort going into vaccinating adults. Most of the evidence −59 years.22 Physicians from systems where decisions

September 2020
e102 Hurley et al / Am J Prev Med 2020;59(3):e95−e103
about purchasing and handling of vaccines are made at a This publication was supported by Cooperative Agreement
larger system level may have been more likely to assess Number 1 U01 IP000849-02, funded by the Centers for Dis-
vaccinations at each visit because these systems may use ease Control and Prevention.
robust EHRs with technical capabilities to develop the LPH conceptualized and designed the study, contributed to
the data collection instrument design, and drafted the initial
programming required to build standing orders and pro- and final manuscript. AK, MAA, STOL, MCL, and LAC conceptu-
vider alerts into electronic medical records to support alized and designed the study, designed the data collection
adult vaccination efforts. This practice may also reflect instrument, and reviewed and revised the manuscript. BLB con-
greater motivation within these systems to seek pay- tributed to the study design, carried out the initial and further
ments by insurance companies for improving quality analyses, and reviewed and revised the manuscript. MB con-
metrics. tributed to the study design and data collection instrument
design, coordinated and supervised all data collection, and
reviewed and revised the manuscript. All authors approved the
Limitations final manuscript as submitted and agree to be accountable for
This study has both strengths and limitations. The sur- all aspects of the work.
vey methodology results in nationally representative No financial disclosures were reported by the authors of this
samples of primary care physicians who care for adults paper.
in the U.S., and the response rate was high. Physicians
who are male, older, and from smaller, private practices
where decisions are made independently or those prac-
ticing in the South are somewhat under-represented in REFERENCES
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