Improving Influenza Vaccination in

Children With Comorbidities: A

Systematic Review
Daniel A. Norman, MPH, MInfectDis,a,b Rosanne Barnes, PhD,a Rebecca Pavlos, PhD,a Mejbah Bhuiyan, PhD,a
Kefyalew Addis Alene, PhD,a,c Margie Danchin, MBBS, PhD,d,e,f Holly Seale, PhD,g Hannah C. Moore, PhD,a
Christopher C. Blyth, MBBS, PhDa,b,h,i

CONTEXT: Children with

medical comorbidities are at greater risk for severe influenza and poorer abstract
clinical outcomes. Despite recommendations and funding, influenza vaccine coverage remains
inadequate in these children.
We aimed to systematically review literature assessing interventions targeting
OBJECTIVE:
influenza vaccine coverage in children with comorbidities and assess the impact on influenza
vaccine coverage.
DATA SOURCES:PubMed, Scopus, Embase, Cumulative Index to Nursing and Allied Health
Literature, Cochrane Central Register of Controlled Trials, Allied and Complementary Medicine
Database, and Web of Science databases were searched.
STUDY SELECTION: Interventions targeting influenza vaccine coverage in children with medical
comorbidities.
Two reviewers independently screened articles, extracting studies’ methods,
DATA EXTRACTION:
interventions, settings, populations, and results. Four reviewers independently assessed risk
of bias.
RESULTS: From 961 screened articles, 35 met inclusion criteria. Published studies revealed that
influenza vaccine coverage was significantly improved through vaccination reminders and
education directed at either patients’ parents or providers, as well as by vaccination-related
clinic process changes. Interventions improved influenza vaccine coverage by an average 60%,
but no significant differences between intervention types were detected. Significant bias and
study heterogeneity were also identified, limiting confidence in this effect estimate.
LIMITATIONS: A
high risk of bias and overall low quality of evidence limited our capacity to assess
intervention types and methods.
CONCLUSIONS: Interventions were shown to consistently improve influenza vaccine coverage;
however, no significant differences in coverage between different intervention types were
observed. Future well-designed studies evaluating the effectiveness of different intervention
are required to inform future optimal interventions.

a
Wesfarmers Centre of Vaccines and Infectious Diseases, Telethon Kids Institute, Western Australia, Australia; bSchool of Medicine, University of Western Australia, Western Australia,
Australia; cFaculty of Health Sciences, Curtin University, Western Australia, Australia; dDepartment of General Medicine, The Royal Children’s Hospital, Victoria, Australia; eDepartment of
Pediatrics, University of Melbourne, Victoria, Australia; fVaccine Hesitancy, Murdoch Children’s Research Institute, Victoria, Australia; gSchool of Population Health, University of New South
Wales, New South Wales, Australia; hDepartment of Infectious Diseases, Perth Children’s Hospital, Western Australia, Australia; and iDepartment of Microbiology, PathWest Laboratory
Medicine, Western Australia, Australia

To cite: Norman DA, Barnes R, Pavlos R, et al. Improving Influenza Vaccination in Children With Comorbidities: A Systematic Review. Pediatrics. 2021;147(3):
e20201433

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PEDIATRICS Volume 147, number 3, March 2021:e20201433 REVIEW ARTICLE
Influenza remains a substantial cause
of morbidity and mortality in children
despite the widespread availability of
seasonal vaccines.1 Children with
medical comorbidities, including
asthma, immunodeficiency, and
epilepsy, are at increased risk of
severe influenza infections and more
adverse clinical outcomes.2 As
a result, national immunization
programs3–5 recommend and fund
annual influenza vaccination for those
with medical comorbidities.3,6
Despite these efforts, influenza
vaccine coverage in children with
comorbidities remains inadequate.7,8
The reasons for noncompliance with
recommendations are complex and
multifactorial,9 yet interventions
targeting improvement in influenza
coverage in children with medical
comorbidities have been shown to be
efficacious.10
A previous review of interventions
targeting influenza vaccine coverage
in children aged 6 months to 19 years
with comorbidities, published in
2015, concluded that there was
strong evidence for parental letter-
based vaccination appointment
reminders.11 Pooled estimates of the
overall and relative impact of
interventions were not assessed and
the numerous biases of the included
studies were not formally reported.
The review was also limited by the
search strategy restricted to
“influenza AND vaccination OR
immunization OR children AND
asthma OR malignancy OR high risk
AND reminder,” potentially missing
nonreminder type interventions and
other comorbidities.
To design and evaluate effective and
sustainable interventions to improve
influenza vaccine coverage in
children with comorbidities requires
an understanding of the overall and
relative effectiveness of these
interventions and any associated
biases. To this end, we conducted
a systematic review of published
interventions targeting influenza
vaccine coverage in children with
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2 NORMAN et al
medical comorbidities to evaluate
the overall effectiveness and
effectiveness of different
intervention types.
METHODS
The study was designed with the
Preferred Reporting Items for
Systematic Reviews and Meta-
Analyses (PRISMA) guidelines and
checklist12 with registration through
PROSPERO: The International
Prospective Register of Systematic
Reviews (CRD42019090623). We
conducted a narrative review
describing studies’ characteristics,
results, and biases. Where possible,
absolute results of influenza vaccine
coverage were extracted to determine
pooled effect estimates for each
intervention type and study method.
Search Strategy and Data Sources
PubMed, Scopus, Embase,
Cumulative Index to Nursing and
Allied Health Literature, Cochrane
Central Register of Controlled Trials,
Allied and Complementary Medicine,
and Web of Science databases were
searched for articles published in
English from January 1976 to March
2019. The search strategy was
"Influenza vaccination or influenza
immunization or influenza
immunisation) and (reminder or
interventions or best practices or
strategies) and (children or pediatric
or paediatric) and (high-risk or
asthma or neurological or
malignancy or cardiac or
hematological or oncology or
comorbidity or chronic diseases or
medical conditions." This strategy
was designed with free-text search
terms encompassing influenza
vaccination and comorbidities
defined by the Australian,3 US,4 and
UK5 national guidelines with
appropriate terms for intervention
types and methods. Hand searching
of retrieved articles’ bibliographies
was undertaken to identify any
additionally relevant publications.
Ongoing trials were searched
through the National Institutes of
Health’s clinicaltrials.gov Web site.
Two authors (D.A.N. and R.B.) were
responsible for screening of
extracted articles and identification
of potentially eligible studies.
Study Selection
Randomized control trials (RCTs),
cohort, and quasi-experimental
studies undertaken in community,
primary care, and/or hospital settings
were reviewed if they (1) included
children (aged 6 months to 21 years
old) who met medical comorbidity
criteria as per national immunization
guidelines3–5 and (2) evaluated at
least 1 clinical, behavioral, or
structural intervention designed to
improve influenza vaccine coverage in
children with 1 or more
comorbidities. Exclusion criteria of
studies included non–peer reviewed
results, studies from which changes
in influenza vaccination could not be
extracted or separated from non-
influenza vaccination, studies with
influenza vaccination results of
children with comorbidities which
could not be separated from other
populations, and other systematic
reviews of eligible studies
(Supplemental Information). Raw
numbers were extracted, where
possible. When required, the number
of vaccinated patients were calculated
from percentages included in study
reports.
Data Extraction
A data form based on Cochrane’s
“Data Collection Form: Intervention
Review – RCTs and Non-RCTS”13 was
used to ensure standardized
extraction of articles. Data were
extracted by a primary author
(D.A.N.) and independently confirmed
by supplementary authors (R.P., M.B.,
and K.A.A.). When discrepancies were
identified, results were resolved by
the senior author (C.C.B.). The
extraction form included publishing
journal, study methodology,
intervention type, clinical setting,
geographical location, participant
comorbidity type(s), participant age
group, study years, and vaccination
status ascertainment method (ie,
parental report, clinic vaccination
records, and immunization registry
records). Absolute vaccination
numbers, rates, and relevant
statistical testing results (ie, P value
and risk ratios) were extracted from
applicable studies. Studies were
grouped by methodology: (1) RCT
(clustered or individually
randomized), (2) cohort studies
(prospective and retrospective), or
(3) a quasi-experimental study type
including quality improvement (QI)14
or before and after studies.15 QI
studies were classified as such if the
study’s authors identified them as QI
and were approved by a relevant
ethics group or review board as a QI
study. Before and after studies were
defined by their observations of the
study population’s influenza vaccine
coverage taken before an
intervention(s)’ introduction and
after introduction without identifying
as a QI study. Final observations of
vaccine coverage in before and after
studies were used as the
postintervention vaccine coverage
values for quantitative analysis.
Before and after studies did not use
negative control groups but may have
randomly assigned individuals to
different interventions.
Qualitative Data Analysis
Study characteristics and individual
results as well as trends across
studies were assessed. There were 5
intervention categories: (1) parental
reminders (physical or electronic
reminders directed to parents or
guardians about their child(s)’
vaccination status and eligibility), (2)
parental education (information for
parents about influenza infection
risks and vaccination benefits
through counseling by a provider or
written material), (3) provider
reminders (physical or electronic
reminders directed to clinicians
managing children with medical
comorbidities), (4) provider
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PEDIATRICS Volume 147, number 3, March 2021
education (information for clinicians
about influenza infection risks and
vaccination benefits), and (5) clinic
process changes. Clinic process
changes were defined as
interventions that impacted how
patients received influenza
vaccinations in a clinical
environment, the flow of vaccination
resources, vaccination status
recording, and/or reporting within
the study’s setting(s). Such
interventions included introduction
of electronic vaccination records,
interclinic collaboration, and resource
sharing. Studies in which researchers
examined multiple interventions
trialed in the same group(s) were
identified as a multicomponent
intervention, whereas those using the
same intervention in single or
multiple study groups were defined
as single interventions.
Quantitative Data Analysis
Quantitative changes in influenza
vaccination coverage either between
allocated intervention and control
groups (ie, RCTs) or across influenza
seasons (ie, quasi-experimental and
cohort studies) were extracted when
applicable. Where applicable,
absolute and relative changes in
vaccine coverage were directly
extracted from publication or back
calculated when necessary.
Subanalyses were performed to
assess different interventions types,
study designs, and single versus
multicomponent interventions.
Studies in which researchers
evaluated the same intervention(s) in
different populations or different
interventions within same
populations across different time
points were treated as separate data
sets. Changes in influenza vaccine
coverage in an intervention group(s)
compared with a control group or
before and after introduction of an
intervention were estimated by using
risk ratios with 95% confidence
intervals (CIs). Random effect
models16 using the Mantel-Haenszel
method (M-H)17 were used for
pooling of vaccination coverage
changes. Random effect models were
used because of the high level of
methodologic and clinical diversity
between studies and the assumption
of different effects across studies.18
Heterogeneity of quantitative results
was evaluated by using the
standardized t 2 and I2 statistics
describing the proportion of
dispersion across studies due to true
heterogeneity.19
Risk of Bias Analysis
Individual studies’ risk of bias was
assessed with Cochrane’s Grading of
Recommendations Assessment,
Development and Evaluation
(GRADE) tool.20 One primary
reviewer (D.A.N.) examined risk of
bias in all studies, and 3 secondary
reviewers (R.P., K.A.A., and M.B.)
independently reviewed an equal
proportion of the studies. A senior
reviewer (C.C.B.) acted to resolve any
discordant assessments between the
primary and the secondary reviewers.
Studies were assigned to be low risk
if all domains were identified as low
risk, unclear risk if 1 or more
domains were of unclear risk (with
no high-risk scored domains), and
high risk if at least 1 domain was
identified as high risk.
RESULTS
Study Search and Selection
Our initial search identified 961
primary articles, with 6 additional
articles identified by searching
references. No ongoing trials or
intervention studies meeting our
inclusion criteria were identified
through the National Institutes of
Health clinicaltrials.gov Web site.
Once duplicates were removed, 611
unique articles remained. Title and
abstract review excluded a further
442 and 108 articles, respectively.
From the 61 articles remaining for
full-text review, 35 articles met our
inclusion criteria. Sufficient data were
present in 26 of these articles for
3

FIGURE 1
Article extraction flowchart.
quantitative analysis. The reasons for
exclusion after full article review are
listed in Fig 1.
Of the 35 included articles, 33
examined seasonal influenza
vaccination exclusively, 1 evaluated
pandemic H1N1/09 influenza
vaccination21 and 1 examined both
seasonal and pandemic H1N1/09
vaccination.22 There were 5
RCTs23–27 and 4 cohort
studies.10,22,28,29 The remainder,
defined as quasi-experimental
studies, included 20 before and after
intervention studies21,28,30–47 and 6
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4 NORMAN et al
QI studies.48–54 One article included
both a quasi-experimental study and
a cohort study.28
RCTs
All RCTs were singular type
intervention of parental influenza
vaccination reminders: researchers in
4 studies used postal letter
reminders23,24,26,27 and those in 1
evaluated mobile phone text message
reminders (Table 1).25 All studies
were conducted within the United
States between 1992 and 2017. Four
were conducted at pediatric clinics, of
which 3 only targeted asthmatic
patients,23,26,27 and the fourth
included patients with a range of
comorbidity types.25 Dombkowski et
al24 targeted children with different
comorbidity types with reminders
through a statewide immunization
registry. Changes in vaccination
coverage were recorded sufficiently
for each RCT to be included within
the quantitative analysis. All postal
letter interventions revealed
significant improvements in influenza
vaccine coverage for those receiving
reminders compared with their
respective control groups. Statistically
significant low to moderate absolute
increases in influenza vaccine
coverage of 6.5%, 18%, 23%, and
25% were present for their respective
intervention groups of Dombkowski
et al,24 Daley et al,23 Szilagyi et al,27
and Kemper et al26 compared with
their control groups. Conversely, the
intervention group in Hofstetter et
al25 had a lower but not statistically
significant absolute coverage decline
of 7% compared with their control
group.
Cohort Studies
Four cohort studies met the review’s
inclusion criteria, with 2
prospective10,22 and 2 retrospective
evaluations (Table 2).28,29 All had
sufficient results to be included
within the quantitative analysis and
pooled effect estimate. Moore and
Parker29 evaluated the use of a postal
letter for an intervention group
versus verbal reminders in the
control group. Fiks et al28 compared
use of electronic provider reminders
with a provider educational session in
an intervention group versus
a control group who received the
educational session alone. Bay and
Crawford10 tested electronic
reminders delivered through an
online patient portal system with
educational material links, compared
with a standard of care in a single
cohort. Dombkowski et al22 examined
postal letter reminders for a seasonal
and pandemic influenza A/H1N109
 TABLE 1 Characteristics and Results of RCTs
Authors and Setting, Country, and Study Participants Participant Study Vaccination Status Intervention Absolute Effect Size Relative Effect Sizes Study Summary
Publication Study Years (Population) Ages Methodology Ascertainment Type (% of Vaccine (% of Vaccine
Year (Subtype) Coverage) Coverage)
Daley et al23 Pediatric practices, Pediatric asthmatic Not specified Individualized Immunization Parent Absolute influenza Intervention group: Mailed letter influenza
(2004) United States patients: RCT registry records reminder vaccine coverage 42%; control group: vaccination reminders
(2002–2003) intervention group: n and patient increased by 17% 25% to patients’ families
= 920; control group: billing record significantly improved
n = 931 influenza vaccine
uptake in asthmatic
children
Dombkowski et Michigan Children with 2–5 y Individualized Immunization Parent Absolute influenza Intervention group: Children with
al24 (2012) immunization comorbidities (ACIP RCT registry records reminder vaccine coverage 30.8%; control comorbidities were

PEDIATRICS Volume 147, number 3, March 2021

registry, United guidelinesa): n = (ICD-9 codes) increased by 6.5% group: 24.3%; odds 1.39 times more likely
States 3618 ratio of 1.39 (95% to receive an influenza
(2008–2009) CI: 1.13–1.72) vaccine if they
received a mailed
vaccination letter
reminder compared
with those who did not
Hofstetter et Pediatric clinics, Pediatric patients with 11–17 y Individualized Electronic Parent Absolute difference Educational text Nonsignificantly lower
al25 (2017) United States comorbidities (ACIP RCT vaccination reminder in vaccine message group: influenza vaccination
(2014–2015) guidelinesa): records coverage of 7% 56.8%; plain text coverage was seen in
education reminder: between reminder message group: children assigned an
n = 154, plain groups 63.8% (P = .24) education-embedded
reminder: n = 141 vaccination reminder
compared with a plain
reminder
Kemper et al26 Pediatric clinic, Pediatric asthmatic Average of 4.5 Individualized Clinic vaccination Parent Absolute vaccination Intervention group: Pediatric asthmatic
(1993) United States patients: y (no range RCT records reminder coverage was 25% 46%; control group: patients who received
(1991) intervention group: n given) greater in the 21% mailed letter influenza
= 43; control group: intervention group vaccination reminders
n = 53 were significantly
more likely to receive
the seasonal influenza
vaccination

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Szilagyi et al27 Pediatric clinic, Pediatric asthmatic 1–18 y Individualized Clinic vaccination Parent Absolute increase in Intervention group: Mailed influenza
(1992) United States patients: RCT records reminder influenza vaccine 30%; control group: vaccination reminder
(1990–1991) intervention group: n uptake of 23% 7% letters to families
= 63; control group: considerably improved
n = 53 influenza vaccine
uptake
ACIP, Advisory Committee on Immunization Practices; ICD-9, The International Classification of Diseases, Ninth Revision codes for disease diagnoses.
a ACIP guidelines: guidelines on comorbidities that increase individuals’ risks from influenza infection and recommendations for seasonal influenza vaccination.

5
vaccine compared with standard of
care.
All cohort studies were conducted
within the United States and were
published after 2005. Collectively,
cohort studies revealed low to
moderate improvements in influenza
vaccination coverage. Coverage
improvements were significant for all
interventions except that of Fiks et
al,28 who used a provider electronic
reminder revealing only
a nonsignificant increase of 3.4% in
coverage for their intervention group
versus their control group. The
greatest improvement was shown by
Bay and Crawford,10 with a 20.8%
increase in coverage for children
whose families reported receiving
a reminder through reminder
messages and education via an online
patient portal.
Quasi-Experimental Studies
Quasi-experimental studies were the
most varied, with researchers
examining different interventions for
both respiratory and nonrespiratory
comorbidities (Supplemental Table
4). Multicomponent interventions
were only evaluated by using quasi-
experimental studies. QI studies
were only conducted post-2006 and
in the United States, with 60%
targeting patients of pediatric
oncology clinics with
multicomponent interventions.
Before and after studies took place
across a longer time frame, in
Europe, Australia, and North
America, and examined both singular
and multicomponent for a range of
respiratory and nonrespiratory
comorbidities. Appropriate
quantitative results were present in
18 of the included quasi-
experimental studies for inclusion in
the pooled effect estimate. Quasi-
experimental studies had the
greatest range of influenza
vaccination coverage impacts, with
increases from 3.4%28 to 45.5%53
postintervention. Additionally,
a minority of quasi-experimental
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6 NORMAN et al
studies had nonsignificant changes
in vaccination coverage38,41,45,46 or
reported results in which absolute
coverage changes could not be
ascertained.42,48,49,51
Pooled Estimates
From 5 RCTs, 4 cohort studies, and
18 quasi-experimental studies
included within the quantitative
analyses, 33 separate intervention
results had sufficient data for pool
effect estimates (Fig 2).
Researchers in 2 studies examined
3 different telephone-based
parental reminders from different
types of clinicians (ie, pediatric
oncologist and public health
physicians) using before and after
intervention designs in separate
populations; these were considered
as 6 distinct data sets for
quantitative analysis.32,34
Dombkowski et al 22 evaluated the
impact of the same reminder
system for both seasonal and
pandemic influenza vaccinations
programs in 2009. Fiks et al28
conducted both a before and after
study and a prospective cohort
study examining the introduction of
an electronic health record alert.
Rao et al52 evaluated separate
provider reminder and parental
education intervention groups to
a control group within their QI
study.
The effect estimate following
pooling of interventions’
quantitative results revealed an
average increase in influenza vaccine
coverage of 60% (risk ratio: 1.60;
95% CI: 1.47–1.74) across 368 574
participants. Point estimates varied
between intervention types,
singular-component versus
multicomponent intervention, and
study methods; however, the relative
risks of specific intervention types
were not significantly different
(Supplemental Table 5). Likewise,
the effect estimates of different
study methodologies were not
significantly different (Supplemental
Table 6).
Risk of Bias
Substantial heterogeneity was
observed across studies, with the
overall and subgroup analyses all
having I2 scores .75% (Fig 2). 55
Overall, a high level of bias was
observed, with all but 1 study
having a high risk of bias in at least
1 of GRADE’s domains (Table 3).
RCTs had a lower average number
of high-risk bias domains per study
of 1.8 compared with quasi-cohort
and experimental studies with
average scores of 3.25 and 4.03,
respectively.
DISCUSSION
Interventions of vaccination
reminders and influenza vaccination
education targeting either parents or
providers as well as clinic process
changes were all shown to have
effectiveness for improving influenza
vaccine coverage in children with
comorbidities. Numerous biases and
high heterogeneity were observed
across all study types because of
study designs, vaccination status
ascertainment methods, and
outcomes reported. These biases
limited our capacity to determine if
significant differences existed
between intervention types, and the
high level of heterogeneity reduced
confidence in the meta-analysis
results.
RCTs revealed how simple
vaccination reminders targeting
patients’ parents or guardian could
moderately improve influenza
vaccine coverage. Cohort studies
had similarly low to moderate
improvements for influenza
vaccination coverage with parental
reminders. Conversely, researchers
in quasi-experimental studies
examined a variety of intervention
types and moderate-to-high impact
on increasing influenza vaccine
coverage for a diversity of patients.
Unsurprisingly, RCTs had a lower
 TABLE 2 Characteristics and Results of Cohort Studies
Authors and Setting, Country, and Study Participants Participant Study Vaccination Status Intervention Absolute Effect Size Relative Effect Sizes (% Study Summary
Publication Study Years (Population) Ages Methodology Ascertainment Type (Vaccine Coverage %) of Vaccine Coverage)
Year
Bay and Pediatric respiratory Pediatric respiratory Not Retrospective Parental reporting Parent Absolute influenza Intervention: 70.8%; no Families of pediatric
Crawford10 clinic, United disease patients: n = specified cohort study reminder vaccination intervention: 50% respiratory clinic
(2017) States (2015) 107 increased by 20.8% patients who
reported receiving
influenza vaccination
reminders had
significantly higher
influenza vaccine
uptake

PEDIATRICS Volume 147, number 3, March 2021

Dombkowski et Michigan Children with 0.5–18 y Retrospective Immunization Parent Pandemic H1N1 Pandemic H1N1 Children with
al22 (2014) immunization comorbidities (ACIP cohort study registry records reminder vaccine: coverage vaccine: intervention comorbidities were
registry, United guidelinesa): n = (ICD-9 codesb) increase of 2.2%; group: 6.5%, control more likely to receive
States 142 383 seasonal influenza group: 4.3%. both pandemic and
(2009–2010) vaccine: coverage Seasonal influenza seasonal influenza
increase of 2.1% vaccine: intervention vaccines if they
group: 4.8%, control received a mailed
group: 2.7% vaccination letter
compared with those
who did not
Fiks et al28 Pediatric outpatient Pediatric asthmatic 5–18 y Prospective Electronic Provider Absolute improve Intervention group: Electronic medical
(2009) clinics, United patients: intervention cohort studyc vaccination reminder vaccination between before: 45.7%, after: record vaccination
States group baseline year: records coverage difference 51.0%; control reminder prompts
(2006–2007) n = 5329; intervention between group: before: for physicians had
group study year: n = intervention and 46.0%, after: 47.9% minimal impact on
6110; control group control groups of influenza vaccine
baseline year: n = 3.4% uptake
5338; control group
study year: n = 5809
Moore and Pediatric clinics, Pediatric asthmatic 0.5–18 y Prospective Electronic Parent Absolute influenza Letters reminders Influenza vaccination
Parker29 United States patients: letters cohort study vaccination reminder vaccination group: 57.9%, verbal reminders for
(2006) (2004–2005) reminders group: n = records coverage difference reminders group: asthmatic pediatric
114; verbal in intervention 43.8% patients by mailed

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reminders group: n = group = 14.1% letter showed
820 superiority over
verbal reminders by
providers for
influenza vaccine
uptake
ACIP, Advisory Committee on Immunization Practices; ICD-9, International Classification of Diseases, Ninth Revision.
a ACIP guidelines: guidelines on comorbidities that increase individuals’ risks from influenza infection and recommendations for seasonal influenza vaccination.
b ICD-9 codes: International Classification of Diseases, Ninth Revision.
c Fiks et al28 conducted both a before and after evaluation and a prospective cohort study within their population for the 2006–2007 northern hemisphere influenza season.

7
 concerns of not recommending
influenza vaccination to vulnerable
patients.
The high heterogeneity of studies
made identifying discernible trends
across studies methods and results
through meta-analysis difficult. A
narrative synthesis identified a shift
toward multicomponent
interventions, targeting of children
with nonrespiratory comorbidities,
and greater use of information
technologies (ie, electronic medical
records and e-mail or text message
reminders), particularly with more
recent publications (since 2010). This
was likely due to greater use of
multicomponent interventions across
public health, clinical integration of
information technologies, and
recognition of the severe influenza
infection impacts in children with
nonrespiratory comorbidities.
Using quantitative analysis, we found
an average improvement in coverage
by 60% (RR: 1.60 [95% CI:
1.47–1.75]). The high heterogeneity
of studies and strong risk of bias
limited our confidence in this effect
estimate and further subanalyses of
quantitative results. Furthermore, we
could not establish if any single
intervention type or
a multicomponent intervention
showed greater efficacy. Moreover,
differences in point estimates
between different intervention types
FIGURE 2 should be interpreted with caution
Pooled effect estimates and forest plots. a Dombkowski et al22 evaluated both seasonal and pan-
demic A/H1N109 vaccines for the 2009–2010 northern hemisphere influenza season. b Fiks et al28 given overlapping CIs and biases
conducted both a before and after evaluation and a prospective cohort study within their population observed.
for the 2006–2007 northern hemisphere influenza season. c Cecinati et al32 trialed 3 different
variations of parental reminders in 3 distinct populations of pediatric oncology patients and As reported in a previous systematic
therefore results were treated as 3 different before and after studies. d Esposito et al34 trialed 3 review,11 parental letter-based
different variations of parental reminders in 3 distinct populations of pediatric asthmatic patients reminders improve influenza vaccine
and therefore results were treated as 3 different before and after studies. e Rao et al52 evaluated coverage. We additionally identified
both a provider reminder intervention and parental educational tool in distinct populations; as such,
they were treated as 2 separate data sets. df, degrees of freedom. evidence revealing that provider
reminders, educational interventions,
and clinic process changes can also
average number of high risk of bias for intervention design and improve vaccine coverage. We
domains compared with cohort and evaluation provided by cohort and identified a further 17 articles* not
quasi-experimental studies. Future quasi-experimental designs. captured by the previous review11
intervention designers will need to Moreover, researchers in future and excluded 2 that were previously
balance the low bias risk and intervention evaluations should
rigorous design requirements of an implement standards of control * Refs 10, 21, 22, 24, 25, 30, 31, 33, 36–39, 41, 42, 45,
RCT with the capacity and flexibility groups because of the ethical 51–54.

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8 NORMAN et al
TABLE 3 GRADE Risk of Bias Domain Scores
Study and Year
Random Sequence
Generation
Bay and Crawford10
(2016)
Bjornson et al30 (2000)
Britto et al48 (2006)
Britto et al49 (2007)
Camurdan et al31
(2012)
Cecinati et al32 (2010)
Crawford et al33 (2014)
Daley et al23 (2004)
Dombkowski et al24
(2012)
Dombkowski et al22
(2014)
Esposito et al34 (2009)
Fiks et al28 (2009)
Freedman et al50 (2014)
Gaglani et al35 (2001)
Gattis et al36 (2018)
Gregori et al21 (2012)
Hofstetter et al25 (2017)
Huth et al37 (2015)
Kempe et al38 (2014)
Kemper et al26 (1993)
Lin et al39 (2015)
Martin40 (2008)
McCreary41 (2013)
Merckx et al42 (2016)
Moore and Parker29
(2006)
Olshefski et al51 (2018)
Patwardhan et al43
(2011)
Paul et al44 (2006)
Rao et al52 (2018)
Sobota et al53 (2015)
Szilagyi et al27 (1992)
Urkin et al45 (2016)
Walter et al46 (1997)
Wong et al54 (2017)
Zimmerman et al47
(2006)
The score of each risk of bias domain for the listed studies by their respective symbol, with low risk (plus sign), unclear risk (question mark), or high risk (dash).
included (a conference abstract56 and
a systematic review of already
included articles57). In the previous
review, authors claimed that meta-
analysis was inappropriate because of
high heterogeneity between studies.
Although high heterogeneity was
observed, we believe pooled analyses
are important to identify potential
effect sizes. These pooled estimates
are required to inform development
and design appropriately conducted
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PEDIATRICS Volume 147, number 3, March 2021
GRADE Risk of Bias Quality Assessment
Allocation Blinding of Blinding of Incomplete Outcome Selective
Concealment Participants Outcome Data Reporting
and Personnel Assessment
2 2 2 2 2 2
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clinical trials and evaluations because of the increased severity of
assessing the relative benefit of influenza infections in these children
different interventions. and potential negative impacts of
unnecessary interventions in
This is the first attempt to quantify families with high-care needs.
the overall impact on interventions Superiority of multicomponent
designed to improve influenza interventions compared with single
vaccine coverage for children with interventions has been shown in
comorbidities. Optimizing similar contexts for improving
interventions to improve influenza vaccine coverage in high-risk
vaccine use in high-risk pediatric adults58 and human papillomavirus
populations is clinically relevant vaccine use,59 but we were not able
9
to demonstrate superiority in this
context.
Further evaluation of interventions’
costs, feasibility, and acceptance by
clinical staff, patients, and families are
necessary for future optimal
intervention design. Use of negative
control groups within such studies,
particularly populations at high risk
of influenza, needs careful
consideration. Assessing pre-
established “standard of care models”
concurrently with additional
interventions enables researchers to
assess impacts, maintain high
methodology quality and ensure
appropriate patient care.
Our results were primarily limited by
the quality of studies available for
analysis. The relatively high number
of quasi-experimental studies
published compared with RCTs and
well-constructed cohort studies is
reflective of their convenience,
relatively low cost, and ease of
implementation within diverse
populations and settings. The ability
to disaggregate and assess the
relative impact of multicomponent
interventions remains challenging
given the diversity of interventions
and study design. Use of the GRADE
risk of bias evaluation tool was
chosen a priori.20 We were limited in
our capacity to compare the relative
quality of less rigorous study designs,
particularly the quasi-experimental ACKNOWLEDGMENTS
studies. This project constitutes part of
Daniel Norman’s doctor of
philosophy candidature and, as
CONCLUSIONS such, was not directly sponsored or
Interventions targeting influenza funded. Mr Norman’s PhD is funded
vaccination in children with medical by the Commonwealth of Australian’
comorbidities through vaccination research training program PhD
reminders, education targeting scholarship and the Wesfarmers
parents or providers, and clinical Centre for Vaccines and Infectious
process changes improved coverage. Diseases PhD top-up scholarship.
No intervention type was clearly Prof Blyth is supported by
superior. Multicomponent a fellowship from the National
interventions have been used for Health and Medical Research
children with respiratory and Council of Australia. Dr Moore is
nonrespiratory comorbidities, supported by a Telethon Kids
whereas single component Institute Emerging Research Leader
interventions have been used Fellowship. Prof Danchin is
predominately to target children Melbourne University’s David
with respiratory comorbidities. Bickart Clinician Scientist
However, superiority of single or fellowship recipient.
multicomponent interventions for
improving influenza vaccination was
not established. High level of ABBREVIATIONS
methodologic bias, poor quality of CI: confidence interval
evidence, and small study size limit GRADE: Grading of Recommenda-
conclusions that can be drawn from tions Assessment, Devel-
the literature. Future design and opment and Evaluation
evaluation of interventions to M-H: Mantel-Haenszel method
improve influenza vaccine coverage PRISMA: Preferred Reporting
should directly compare Items for Systematic
intervention types using rigorous Reviews and Meta-
study methodologies to optimize Analyses
effectiveness and reduce the QI: quality improvement
influenza disease burden in children RCT: randomized control trial
with medical comorbidities.

Mr Norman conceived and designed the study, led publication review, data extraction, quantitative analysis, qualitative analysis, and risk of bias assessments, and
wrote the manuscript; Prof Blyth oversaw the design of the study, analyses, and manuscript writing; Dr Barnes contributed to the screening of articles, data
extraction, and analysis; Drs Pavlos, Alene, and Bhuiyan contributed to the evaluation of risk of bias for included studies; Dr Moore, Prof Seale, and Prof Danchin
assisted in designing of the review and drafting of the manuscript; and all authors approved the final manuscript as submitted and agree to be accountable for all
aspects of the work.
This trial has been registered with the National Institute for Health Research (https://www.crd.york.ac.uk/prospero/) (identifier PROSPERO CRD42019090623).
DOI: https://doi.org/10.1542/peds.2020-1433
Accepted for publication Dec 1, 2020
Address correspondence to Daniel A. Norman, MPH, MInfectDis, Telethon Kids Institute, Perth Children’s Hospital, 15 Hospital Ave, Nedlands, WA 6009, Australia.
E-mail: daniel.norman@telethonkids.org.au
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
Copyright © 2021 by the American Academy of Pediatrics
FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.

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10 NORMAN et al
FUNDING: No external funding was secured for this study. Prof Blyth is supported by a fellowship from the National Health and Medical Research Council of
Australia. Dr Moore is supported by a Telethon Kids Institute Emerging Research Leader Fellowship. The other authors received no additional funding.
POTENTIAL CONFLICT OF INTEREST: Prof Seale has previously received funding from vaccine manufactures for investigator driven research and for presenting at
workshops. This funding was not associated with this research; the other authors have indicated they have no potential conflicts of interest to disclose.
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13
Improving Influenza Vaccination in Children With Comorbidities: A Systematic
Review
Daniel A. Norman, Rosanne Barnes, Rebecca Pavlos, Mejbah Bhuiyan, Kefyalew
Addis Alene, Margie Danchin, Holly Seale, Hannah C. Moore and Christopher C.
Blyth
Pediatrics 2021;147;
DOI: 10.1542/peds.2020-1433 originally published online February 8, 2021;

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Improving Influenza Vaccination in Children With Comorbidities: A Systematic
Review
Daniel A. Norman, Rosanne Barnes, Rebecca Pavlos, Mejbah Bhuiyan, Kefyalew
Addis Alene, Margie Danchin, Holly Seale, Hannah C. Moore and Christopher C.
Blyth
Pediatrics 2021;147;
DOI: 10.1542/peds.2020-1433 originally published online February 8, 2021;

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