Immunisation of children with asthma with H1N1 influenza A vaccine and the attitudes of the parents

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Vaccine
32
(2014)
2275–2280
Contents
lists
available
at
ScienceDirect
Vaccine
j
our
na
l
ho
me
page:
www.elsevier.com/locate/vaccine
What
a
pandemic
teaches
us
about
vaccination
attitudes
of
parents
of
children
with
asthma
Betul
Buyuktiryakia,
Ozge
Uysal
Soyerb,
Mustafa
Erkocogluc,
Ayse
Doganb,
Dilek
Azkurc,
Can
Naci
Kocabasc,
Yildiz
Dallarb,
Ayfer
Tuncera,
Bulent
Enis
Sekerela,∗
aHacettepe
University,
School
of
Medicine,
Pediatric
Allergy
and
Asthma
Unit,
Ankara,
Turkey
bMinistry
of
Health,
Ankara
Education
and
Research
Hospital,
Ankara,
Turkey
cMinistry
of
Health,
Ankara
Hematology
and
Oncology
Education
and
Research
Hospital,
Pediatric
Allergy
Clinic,
Ankara,
Turkey
a
r
t
i
c
l
e
i
n
f
o
Article
history:
Received
16
October
2013
Received
in
revised
form
17
January
2014
Accepted
26
February
2014
Available
online
12
March
2014
Keywords:
Asthma
Attitude
Influenza
A/H1N1
Survey
Vaccine
a
b
s
t
r
a
c
t
Background:
During
the
recent
pandemic,
Influenza
A/H1N1
vaccine
uptake
remained
far
below
the
tar-
geted
rates.
Associated
factors
regarding
vaccine
refusal
in
the
general
population
have
been
reported
in
many
studies,
however
the
reasons
behind
refusals
for
asthmatic
children
have
not
yet
been
identi-
fied.
We
aimed
to
investigate
Influenza
A/H1N1
virus
vaccine
acceptance
for
children
with
asthma,
to
determine
the
attitudes
and
beliefs
of
parents
concerning
Influenza
A/H1N1
disease
and
vaccine
and
to
identify
the
association
of
asthma
control
parameters
with
vaccination.
Methods:
The
parents
of
asthmatic
children
aged
6–18
years
participated
in
a
cross-sectional
survey
study
in
three
pediatric
allergy
outpatient
clinics.
The
survey
measured
demographic
factors,
asthma
control
parameters,
vaccination
rates,
and
beliefs
and
attitudes
regarding
Influenza
A/H1N1
vaccine.
Results:
Of
the
625
asthmatic
children,
16.8%
(n
=
105)
were
immunized
with
Influenza
A/H1N1
and
45.7%
(n
=
286)
with
seasonal
influenza
vaccine.
Educational
background
of
parents
(p
<
0.001
and
p
=
0.002,
for
father’s
and
mother’s
educational
level,
respectively),
previous
vaccination
with
seasonal
influenza
(p
<
0.001),
and
having
a
family
member
vaccinated
against
Influenza
A/H1N1
(p
<
0.001)
had
a
significant
influence
on
vaccine
acceptance,
while
fear
of
side
effects
(88.6%)
was
the
major
parental
reason
for
refusing
the
vaccine.
Asthma
control
parameters
had
no
influence
on
uptake
of
the
vaccine.
Physician
recommendation
(84.8%)
was
important
in
the
decision-making
process
for
immunization.
The
statement
“Children
with
asthma
should
receive
swine
flu
vaccine”
increased
the
likelihood
of
being
vaccinated
[OR:
2.160,
(95%CI
1.135–4.111),
p
=
0.019].
Conclusion:
Although
asthmatic
children
are
considered
to
be
a
high-priority
group
for
Influenza
A/H1N1
vaccination,
we
found
low
uptake
of
vaccine
among
our
patients.
Beliefs
and
attitudes
rather
than
asthma
control
parameters
influenced
parental
decisions
for
immunization.
Understanding
the
underlying
deter-
minants
for
refusing
the
vaccine
will
help
to
improve
vaccine
campaigns
in
advance
of
a
future
outbreak.
©
2014
Elsevier
Ltd.
All
rights
reserved.
1.
Introduction
The
pandemic
of
Influenza
A/H1N1
virus
established
a
major
challenge
to
health
care
providers
globally
in
2009.
In
May
2009,
the
first
laboratory-confirmed
case
of
Influenza
A/H1N1
virus
infec-
tion
was
reported
in
Turkey,
and
thereafter
10,700
patients
were
hospitalized
due
to
the
virus.
During
the
pandemic,
656
patients
∗Corresponding
author.
Tel.:
+90
312
305
1700;
fax:
+90
312
311
2357.
E-mail
address:
b
sekerel@yahoo.com
(B.E.
Sekerel).
with
Influenza
A/H1N1
virus
infection
died,
two
thirds
of
whom
had
chronic
diseases
or
were
pregnant
[1].
The
Ministry
of
Health
of
Turkey
launched
a
vaccination
cam-
paign
as
a
component
of
an
action
plan
against
Influenza
A/H1N1
virus
according
to
the
suggestion
of
the
World
Health
Organization.
Individuals
most
susceptible
to
Influenza
A/H1N1
virus
infection,
such
as
pregnant
women,
persons
between
the
ages
of
6
months
to
24
years
of
age
and
patients
with
chronic
health
disorders
or
com-
promised
immune
systems
were
prioritized
to
receive
Influenza
A/H1N1
vaccine
[2].
Vaccination
was
offered
free
of
charge
to
the
public
and
was
carried
out
in
family
health
centers
and
govern-
ment
hospitals.
The
Ministry
of
Health
of
Turkey
made
plans
to
http://dx.doi.org/10.1016/j.vaccine.2014.02.076
0264-410X/©
2014
Elsevier
Ltd.
All
rights
reserved.

Author's personal copy
2276
B.
Buyuktiryaki
et
al.
/
Vaccine
32
(2014)
2275–2280
order
43
million
doses
of
Influenza
A/H1N1
virus
vaccine
[3]
but
purchased
6
million
doses.
Three
million
doses
of
Influenza
A/H1N1
virus
vaccine
were
administered
to
the
public,
which
was
far
below
the
expected
immunization
rate
[1].
Immunization
of
certain
risk
groups
is
an
important
issue
of
preventive
health
care
for
decreasing
mortality
and
morbidity.
Patients
with
asthma
were
advised
to
receive
Influenza
A/H1N1
virus
vaccine
during
the
pandemic
since
they
were
considered
to
be
high-priority
group
[4].
Though
the
safety
and
effectiveness
of
the
vaccine
were
reported
[5,6],
Influenza
A/H1N1
virus
vac-
cine
uptake
was
low
worldwide.
In
the
USA,
20.3%
of
population
received
the
vaccine,
29.4%
of
whom
were
between
6
months
and
18
years
old
[7].
Nearly
one
tenth
of
individuals
living
in
France
were
immunized
against
Influenza
A/H1N1
virus
during
the
pan-
demic
[8].
In
England,
37.1%
of
the
patients
in
risk
groups,
including
pregnant
women,
accepted
to
be
vaccinated
[9].
However,
findings
from
these
studies
did
not
reveal
information
about
the
vaccina-
tion
status
of
specific
risk
groups,
including
children
with
asthma,
nor
about
the
barriers
and
motives
for
uptake
of
the
vaccine.
The
aims
of
this
study
were
to
estimate
Influenza
A/H1N1
virus
vaccine
acceptance
for
children
with
asthma,
to
determine
attitudes
and
beliefs
of
parents
about
Influenza
A/H1N1
disease
and
vaccine
and
to
identify
factors
influencing
vaccine
refusal.
2.
Methods
2.1.
Subjects
This
study
was
conducted
from
1
April
to
30
July
2010,
after
termination
of
the
Influenza
A/H1N1
immunization
campaign.
We
invited
parents
of
all
children
with
asthma
aged
6–18
years
old
admitted
to
our
outpatient
allergy–asthma
clinics.
The
parents
were
so
willingly
to
participate
in
the
study
that
only
three
par-
ents
refused
to
participate
and
eight
parents
did
not
give
back
the
questionnaires
to
their
physicians.
All
three
parents
stated
the
same
reason
for
refusal:
“lack
of
time”.
We
performed
the
study
in
three
centers
(one
university
hospital,
two
education
and
research
hospitals).
While
all
these
clinics
serve
as
referral
centers
for
their
specific
regions,
patients
may
also
be
admitted
upon
request;
thus
they
function
both
as
primary
and
tertiary
health
care
services.
In
these
allergy–asthma
departments,
the
patients
are
followed
by
pediatric
asthma
specialists
so
that
we
have
no
suspicious
about
disease
diagnosis.
The
diagnosis
of
asthma
was
based
on
the
crite-
ria
of
The
Global
Initiative
for
Asthma
(GINA)
guideline
defined
as
a
history
of
intermittent
wheezing
and/or
reversible
airway
obstruc-
tion
with
at
least
a
12%
improvement
in
forced
expiratory
volume
in
1
s
(FEV1)
following
salbutamol
inhalation
[10].
2.2.
Questionnaire
We
administered
a
survey
concerning
demographic
factors
(age,
gender,
age
at
asthma
diagnosis,
parents’
education
level,
family
history
for
atopic
diseases,
smoke
exposure
and
monthly
income)
and
asthma
control
parameters
(scheduled
and
unsched-
uled
healthcare
resource
usage
and
admittance
to
an
emergency
unit
in
the
last
year
due
to
asthma,
ever
having
hospitalization
or
within
the
last
year
because
of
asthma).
The
parents
were
asked
whether
their
child
was
vaccinated
against
seasonal
flu
both
in
the
current
and
any
previous
influenza
seasons.
The
parents
also
answered
questions
concerning;
-
Perception
and
knowledge
about
Influenza
A/H1N1
virus
infec-
tion
and
the
impact
of
infection
on
children
with
asthma.
-
Knowledge
about
the
indications
for
Influenza
A/H1N1
virus
vac-
cine.
-
Potential
benefits
of
immunization
with
Influenza
A/H1N1
virus
vaccine
(decreased
risk
of
infection,
decreased
risk
and
severity
of
asthma
exacerbations).
-
Anyone
in
the
household
who
was
vaccinated
against
Influenza
A/H1N1
virus.
-
Reasons
for
acceptance
of
Influenza
A/H1N1
virus
vaccine.
-
Reasons
for
refusing
immunization
with
Influenza
A/H1N1
virus
vaccine.
Responses
to
most
survey
items
were
evaluated
using
a
5-point
Likert
scale
from
“strongly
agree”
to
“strongly
disagree”.
The
physicians
noted
some
information
related
to
the
patient’s
asthma,
such
as
asthma
severity,
atopy,
medications,
other
atopic
diseases,
lung
function
tests,
and
asthma
control
in
the
last
four
weeks.
Participation
was
on
a
voluntary
base.
2.3.
Analysis
We
performed
statistical
analyses
with
the
SPSS
15
package
program
(SPSS,
Inc,
Chicago,
IL,
USA).
The
Kolmogorov–Smirnov
test
was
used
to
test
the
normal
distribution
of
data.
Differ-
ences
between
the
groups
were
compared
by
Student’s
t
or
Mann–Whitney
U
test
or
chi-square
as
appropriate.
A
sample
size
of
603
patients
achieved
80%
power
to
detect
the
difference
between
the
vaccinated
and
unvaccinated
groups
for
the
variables
(NCSS/PASS
2006
Software).
We
used
multivariate
logistic
regres-
sion
to
model
the
odds
of
being
unvaccinated
versus
vaccinated.
Dependent
variables
were
dichotomized:
the
answers
“strongly
agree”
and
“agree”
versus
all
others.
Variables
that
were
associ-
ated
with
the
outcomes
in
the
univariate
analysis
at
a
p
value
of
less
than
0.25
were
entered
in
the
multivariate
logistic
regression
models
using
the
stepwise
selection
criteria
(backward
elimination
procedure).
The
results
of
multivariate
logistic
regression
analysis
were
expressed
as
odds
ratios
(ORs)
and
95%
confidence
intervals
(CIs).
A
value
of
p
≤
0.05
was
considered
statistically
significant.
3.
Results
Overall,
a
total
of
625
parents
participated
in
the
study
after
the
Influenza
A/H1N1
immunization
campaign.
During
the
2009–2010
influenza
season,
105
children
with
asthma
(16.8%)
were
immu-
nized
with
Influenza
A/H1N1
vaccine
and
286
(45.7%)
children
with
seasonal
influenza
vaccine
(Table
1).
Patients
who
declared
that
they
received
the
Influenza
A/H1N1
vaccine
had
an
asthma
diagno-
sis
at
an
earlier
age
[5
(2.3–7)
vs.
6
(3–8)
years,
p
=
0.018]
and
with
longer
duration
of
asthma
follow
up
[4
(2–7)
vs.
3
(1.5–5)
years,
p
=
0.010].
Although
asthma
control
parameters
within
the
last
year,
including
unscheduled
health
care
or
emergency
department
visit,
or
hospitalization
due
to
asthma,
did
not
differ
between
the
groups;
higher
educational
level
of
the
parents,
being
vaccinated
against
seasonal
influenza
ever
and/or
in
the
current
year,
and
having
a
family
member
vaccinated
against
Influenza
A/H1N1
did
have
a
positive
impact
on
being
vaccinated
with
Influenza
A/H1N1
vaccine
(Table
1).
The
important
correlates
of
being
vaccinated
with
Influenza
A/H1N1
vaccine
are
also
the
different
knowledge,
attitudes
and
beliefs
of
parents
about
Influenza
A/H1N1
vaccine
and
disease
(Fig.
1).
The
parents
who
agreed
to
have
their
children
immunized
were
concerned
about
Influenza
A/H1N1
disease
severity
both
in
healthy
and
asthmatic
children.
In
addition,
they
affirmed
more
fre-
quently
that
the
Influenza
A/H1N1
vaccine
was
safe
(35.2%
vs.
6.2%,
p
<
0.001)
and
easy
to
find
(61%
vs.
37.5%,
p
<
0.001).
Nearly
half
of
the
patients
(47.6%)
who
were
immunized
against
Influenza
A/H1N1
experienced
an
adverse
event
attributed
to
the
vaccine;
malaise
(19%),
fever
(15.2%),
rhinorrhea
(12.4%),
headache

Author's personal copy
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et
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/
Vaccine
32
(2014)
2275–2280
2277
Table
1
Demographic
characteristics.
H1N1
vaccine
(+)
(n
=
105)
H1N1
vaccine
(−)
(n
=
520)
p
Age
(year)
10.3
(8.1–12.3)
9.9
(7.8–12.1)
>0.05*
Gender
(M)
(%) 61
59.6
>0.05†
Age
at
diagnosis
(year)
5
(2.3–7)
6
(3–8)
0.018*
Follow-up
duration
(year)
4
(2–7)
3
(1.5–5)
0.010*
Family
history
for
atopic
disease
(%)
26.7
27.3
>0.05†
Mother’s
education
level
(high
school–univ.)
(%)
46.7
31.3
0.002†
Father’s
education
level
(high
school–univ)
(%)
69.5
44
<0.001†
Atopy
(%)
42.9
53.8
0.040*
FEV1%
94
(85.8–102) 95
(86–105) >0.05*
School
absenteeism
in
last
year
due
to
asthma
(%)
85.7
78.5
<0.05*
Unscheduled
visit/last
year
(≥1)
(%)
52.4
52.3
>0.05*
Emergency
room
visit/last
year
(≥1)
(%)
37.1
28.8
>0.05*
Hospitalization/last
year
≥1(%)
14.3
13.1
>0.05*
Hospitalization/lifetime
≥1(%)
48.6
37.7
0.014*
Monthly
income
≥500
Euro
(%)
63.8
45.9
0.001*
Asthma
severity
(%)
Mild
intermittent
43.8
48.8
>0.05*
Mild
persistant 33.3
32.3
Moderate
persistant
20
15.4
Severe
persistant
2.9
3.3
Seasonal
influenza
vaccination/lifetime
(≥1)
(%)
82.9
64.2
<0.001†
Seasonal
influenza
vaccination/current
year
(%)
65.7
41.7
<0.001†
Vaccinated
another
family
member
(%)
57.1
5.8
<0.001†
*Mann–Whitney
U
test.
†Chi
square.
(10.5%),
cough
(7.6%),
increase
in
need
for
a
short-acting
bron-
chodilator
(5.7%),
or
wheezing
(1.9%).
None
of
the
side
effects
were
severe
or
long
lasting
as
reported
by
the
parents.
The
major
rationales
for
Influenza
A/H1N1
vaccine
acceptance
were
the
child’s
illness
(asthma)
(81%),
recommendation
of
being
vaccinated
(53.3%)
and
fear
of
being
infected
with
Influenza
A/H1N1
of
the
child
(31.4%).
The
recommendation
of
immunization
was
carried
out
by
physicians
(84.8%),
media
(22.9%),
teachers
(11.4%),
nurses
(5.7%),
pharmacists
(3.8%)
and
friends
(2.9%).
The
most
important
parental
reason
for
declining
Influenza
A/H1N1
vacci-
nation
was
fear
of
side
effects
(88.6%).
The
influence
of
politicians
and
media
on
vaccine
decliners
were
prominent
(25.2%
and
24.9%).
The
negative
suggestions
of
friends,
physicians
and
healthcare
providers
about
the
vaccine
further
contributed
to
denial
of
the
vaccine
(Table
2).
Logistic
regression
analysis
revealed
the
determinants
of
Influenza
A/H1N1
vaccine
acceptance
(Table
3).
The
agreement
of
parents
with
the
statement
“Children
with
asthma
should
receive
swine
flu
vaccine”
increased
the
likelihood
of
being
vac-
cinated
[OR:
2.160,
(95%CI
1.135–4.111),
p
=
0.019].
The
odds
ratio
of
being
vaccinated
was
3.941
for
children
whose
parents
reported
“Swine
flu
vaccine
was
safe”
(95%CI
1.919–8.092,
p
<
0.001).
The
61.0%
35.2%
36.2%
56.2%
61.0%
56.2%
74.3%
42.9%
80.0%
66.7%
64.8%
80.0%
62.9%
37.5%
6.2%
14.2%
28.1%
19.0%
28.1%
16.9%
13.3%
65.4%
63.3%
53.6%
59.4%
49.2%
0.0%
20.0%
40.0%
60.0%
80.0%
100.0%
Swine fl
u vaccine is easy to find†
Swine fl
u vaccine is saf
e†
Swine fl
u vaccinaon decr
eas
es schoo
l absente
eism†
Swine fl
u vaccinaon decr
eas
es severity of asthma aack
s†
Swine fl
u vaccinaon decr
eas
es incide
nce of asthma aack
s†
Children wit
h severe asthma should get
a swine flu vaccine†
All asthmac children sh
ould receive a swine flu vaccine†
All child
ren sh
ould receive a swine flu vaccine†
Asthmac c
hildren ma
y be more
vulnerable to s
wine flu than health
y children
Swine fl
u ma
y c
ause hospit
alizaon
Swine fl
u ma
y cau
se an asthma aack*
Swine fl
u i
s a serious diseas
e in asthmac children†
Swine flu is a serious disease in healthy children*
unvaccinated
vaccinated
Knowledge
Beli
efs
Fig.
1.
Parental
knowledge,
beliefs
and
attitudes
concerning
Influenza
A/H1N1
disease
and
vaccination. *p
≤
0.05 †p
≤
0.001.

Author's personal copy
2278
B.
Buyuktiryaki
et
al.
/
Vaccine
32
(2014)
2275–2280
Table
2
Reasons
for
refusing
Influenza
A/H1N1
vaccination.
%
I
had
the
fear
of
side
effects
88.6
Politicians
recommended
not
to
do 25.2
Media
recommended
not
to
do
24.9
My
friends
recommended
not
to
do
18.3
I
have
no
knowledge
about
the
necessity.
13.1
Physicians
recommended
not
to
do
12.3
Healthcare
provider
recommended
not
to
do
6.7
Pharmaceutics
offered
not
to
do
4.2
Previously
had
swine
flu 5
immunization
of
another
family
member
with
Influenza
A/H1N1
vaccine
increased
the
odds
of
being
vaccinated
[OR:
15.018
(95%CI
8.364–26.964),
p
<
0.001]
(Table
3).
4.
Discussion
We
investigated
for
the
first
time
the
parameters
that
influenced
Influenza
A/H1N1
vaccine
uptake
rates
along
with
the
attitudes
and
beliefs
of
parents
related
to
vaccination
in
children
with
asthma.
We
also
considered
the
relation
of
asthma
control
parameters
with
the
acceptance
of
the
vaccine.
Asthma
was
the
most
common
comorbidity
in
hospitalized
patients
with
H1N1
Influenza
A
infection
[11]
and
an
increased
sus-
ceptibility
for
Influenza
A/H1N1
infection
has
been
demonstrated
in
asthmatic
children
[12].
With
regard
to
these
facts,
patients
with
asthma
have
been
targeted
as
a
high-risk
group
for
vaccination
[4].
However,
the
topic
whether
the
influenza
vaccination
should
be
advocated
to
all
asthmatic
children
is
still
controversial
[13,14]
on
account
of
the
studies
demonstrating
no
clear
benefit
of
influenza
vaccination
in
asthmatic
children
and
the
potential
of
influenza
vaccine
to
cause
a
worsening
of
asthma.
Despite
this
ongoing
debate,
vigorous
effects
have
been
expanded
on
vaccination
cam-
paigns.
Nevertheless,
overall
uptake
of
the
vaccine
worldwide
did
not
reach
the
expected
rates,
neither
in
the
general
population
nor
in
recommended
groups
[8,15–17].
The
underlying
reasons
for
declining
the
Influenza
A/H1N1
vaccine
have
been
investigated
in
many
studies;
however,
none
of
these
studies
have
elucidated
influ-
encing
factors
for
children
with
asthma.
From
this
standpoint,
our
results
contribute
to
the
literature
as
being
unique
data
regarding
this
issue.
We
showed
that
just
16.8%
of
children
with
asthma
were
immu-
nized
with
Influenza
A/H1N1
vaccine.
This
was
lower
compared
with
a
study
reporting
a
45%
prevalence
of
intention
to
receive
Influenza
A/H1N1
vaccine,
which
was
conducted
with
children
and
adults
with
asthma.
Hence,
the
actual
rate
for
vaccine
uptake
remains
unknown
[18].
Given
the
higher
percentage
of
vaccination
in
children
who
have
low
age
of
onset
and
long
follow-up
duration
might
conceivably
represent
their
parents
being
more
conscious
about
disease
progress
and
the
complications
on
account
of
dealing
with
the
disease
for
a
long
period
of
time.
We
also
demonstrated
that
parents
with
a
higher
educational
level
were
more
likely
to
have
their
children
vaccinated.
This
is
compatible
with
previous
studies
in
which
a
correlation
between
being
more
educated
and
vaccine
uptake
has
been
shown
[19–21].
The
opportunity
for
more
effective
and
profound
dialogue
between
these
parents
and
health
care
professionals
about
the
risks
and
benefits
of
vaccination
and
also
the
tendency
of
the
more
educated
parents
to
rely
on
expert
explanations
rather
than
non-scientific
data
may
partly
explain
this
relation.
Since
the
vaccine
was
administered
free
of
charge
for
all
citizens,
accessibility
could
not
be
a
reason
for
this
difference.
Nev-
ertheless,
there
are
some
studies
that
have
revealed
no
effect
of
education
level
on
vaccination
[22,23].
Considering
the
triggering
role
of
viral
respiratory
tract
infec-
tions
in
asthma
exacerbations
[24]
and
the
association
with
loss
of
asthma
control
[12],
we
expected
that
uncontrolled
asthmatic
chil-
dren
would
have
higher
vaccination
rates
and
their
parents
would
be
more
prone
to
get
their
children
vaccinated.
Unfortunately,
we
could
not
identify
any
influence
of
asthma
control
parameters
on
vaccination
rates.
Presumably,
insufficient
awareness
of
the
par-
ents
related
to
their
child’s
disease
status
may
be
the
reason
for
this
discrepancy,
and
if
this
is
the
case,
it
should
show
that
there
are
still
gaps
in
asthma
education
of
the
parents.
Additionally,
our
result
is
also
in
line
with
the
recent
study
by
Soyer
et
al.
[25]
that
showed
no
influence
of
asthma
control
parameters
on
seasonal
influenza
immunization
uptake.
It
is
obvious
from
our
results
that
the
knowledge,
beliefs,
and
attitudes
of
parents
concerning
the
Influenza
A/H1N1
vaccine
had
an
effect
on
accepting
or
declining
the
vaccination.
The
parents
were
more
prone
to
have
their
child
immunized
if
they
believed
that
the
disease
was
severe
and
the
vaccine
safe.
Similarly,
the
association
between
perceived
severity
of
a
disease
and
vaccination
behavior
was
shown
in
another
study
[26].
The
positive
influence
of
having
a
family
member
vaccinated
against
Influenza
A/H1N1
suggests
the
propensity
of
individuals
for
vaccination.
Our
find-
ings
are
in
agreement
with
a
study
that
the
parents
who
thought
Influenza
A/H1N1
infection
might
become
severe
were
keener
to
accept
vaccination
for
their
children,
and
persons
who
had
a
family
member
who
was
vaccinated
were
more
likely
to
accept
vaccination
[27].
We
observed
that
recommendations
of
physicians
were
indeed
very
effective
in
the
decision-making
process
for
vaccination.
Since
our
study
group
consisted
of
chronically
ill
patients,
it
is
possible
that
numerous
encounters
with
physicians
may
have
positively
affected
the
parents’
trust
in
health
care
staff
and
their
advices.
Gaygisiz
et
al.
demonstrated
that
chronically
ill
persons
followed
the
recommendations
of
physicians
more
than
healthy
individuals
on
the
subject
of
Influenza
A/H1N1
immunization
[28].
In
addition,
the
positive
effect
of
physicians
on
peoples’
and
parents’
attitudes
regarding
vaccination
against
seasonal
or
pandemic
influenza
vac-
cination
has
also
been
demonstrated
in
other
studies
[21,23,29,30].
Taken
together,
the
leadership
role
of
health
care
professionals
cannot
be
underestimated
in
vaccination
programs
and
they
should
participate
more
in
the
encouragement
of
their
patients
Table
3
Logistic
regression
analysis
for
being
vaccinated.
Univariate
Multivariate
OR
95%
CI
p
OR
95%
CI
p
Mother’s
education
(high
school/university)
1.916
1.252–2.934
0.003
–
–
–
Father’s
education
(high
school/university)
2.899
1.848–4.547
<0.001
2.121
1.226–3.668
0.007
Hospitalization
≥1
(lifetime)
1.691
1.108–2.580
0.015
–
–
–
Monthly
income
≥500
Euro
2.082
1.349–3.213
0.001
–
–
–
All
asthmatic
children
should
receive
swine
flu
vaccine
2.185
1.349–3.538
0.001
2.160
1.135–4.111
0.019
Swine
flu
vaccine
is
safe
8.298
4.851–14.195
<0.001
3.941
1.919–8.092
<0.001
Vaccinated
another
family
member
21.733
12.740–37.076
<0.001
15.018
8.364–26.964
<0.001
Seasonal
influenza
vaccination
(current
year)
2.676
1.725–4.151
<0.001
2.528
1.462–4.373
0.001

Author's personal copy
B.
Buyuktiryaki
et
al.
/
Vaccine
32
(2014)
2275–2280
2279
particularly
when
deciding
to
receive
a
novel
vaccine
in
order
to
achieve
high
uptake
rates.
In
keeping
with
previous
studies
[19,31,32],
ever
having
been
vaccinated
against
seasonal
influenza
and/or
in
the
current
year
had
a
positive
impact
on
Influenza
A/H1N1
immunization
which
reflects
the
motivation
and
compliance
for
receiving
the
vaccine.
Strikingly,
however,
the
acceptance
of
seasonal
influenza
vaccine
was
roughly
three-fold
higher
than
Influenza
A/H1N1
vaccination
among
the
asthmatic
children.
Hence,
this
raised
the
question
why
they
were
unwillingly
to
accept
Influenza
A/H1N1
vaccine.
When
we
analyzed
our
results,
the
most
cited
reason
for
refusal
of
the
vaccine
was
the
fear
of
side
effects,
while
the
influence
of
media
and
politicians
was
also
remarkable.
The
association
with
lower
acceptance
of
vaccination
and
fear
of
side
effects
was
pointed
out
in
many
studies,
consistent
with
our
observation
[21,32–36].
In
contradistinction
to
seasonal
influenza
vaccination,
the
Influenza
A/H1N1
vaccine
has
been
excessively
questioned.
After
the
release
of
the
vaccine,
the
media
was
more
interested
in
the
vaccine
rather
than
the
disease
itself.
It
has
been
demonstrated
that
mass
media
is
the
main
information
source
for
most
people
[37].
There-
fore,
unfavorable
news
about
the
vaccine
covered
in
the
media
might
inevitably
affect
the
perceptions
of
individuals
adversely,
as
revealed
in
recent
studies
[16,35,36].
In
our
country,
concerns
about
vaccine
safety,
including
adjuvants
(squalene),
preservatives
(thiomersal)
besides
the
beliefs
of
rapid
development
and
inad-
equate
testing
of
the
novel
vaccine,
could
have
led
to
confusion
and
increased
the
reluctance
of
vaccination.
In
addition,
conflicting
statements
of
politicians
may
have
been
amplified
the
mistrust
about
vaccine
safety.
Hence,
during
pandemics
we
propose
that
the
media
should
pay
more
attention
to
conveying
information
based
on
scientific
evidence.
Of
note,
we
should
state
that
despite
high
rates
of
fear
of
side
effects
in
our
study
group,
the
parents
whose
children
were
vaccinated
did
not
report
any
serious
events
due
to
vaccination.
This
is
the
first
study
carried
out
on
children
with
asthma
regarding
parents’
beliefs
and
attitudes
toward
Influenza
A/H1N1
vaccination
and
it
included
three
tertiary
referral
hospitals.
We
can
assume
this
sampling
is
representative
of
parents
of
chil-
dren
with
asthma
in
Ankara,
however
as
a
limitation
we
cannot
generalize
the
results
for
whole
asthmatic
children
and
adult
populations.
In
conclusion,
in
spite
of
an
underlying
chronic
illness,
the
rate
of
Influenza
A/H1N1
vaccine
uptake
for
children
with
asthma
was
not
higher
than
the
rates
reported
in
other
population
studies.
Parental
beliefs
and
attitudes
along
with
recommendations
of
physicians
were
more
influential
on
decision-making
for
immunization
rather
than
asthma
control
parameters.
Importantly,
fear
of
side
effects
was
detected
as
a
major
barrier
for
parents
to
accept
the
novel
vac-
cine.
Our
results
suggest
that
success
of
vaccine
campaigns
depends
on
providing
unambiguous
information
and
also
reliance
on
the
safety
and
efficacy
of
the
vaccine
for
patients
and
parents.
We
do
hope
that
the
lessons
learned
from
the
last
pandemic
will
guide
us
in
developing
new
vaccination
strategies
for
future
outbreaks
in
collaboration
with
health
care
providers,
politicians
and
mass
media.
Authors’
contributions
•SBE
had
primary
responsibility
for
protocol
development,
out-
come
assessment
and
data
analysis,
and
prepared
the
article
with
BB
and
OUS.
•BB
and
OUS
participated
in
the
development
of
the
protocol
and
the
analytic
framework
for
the
study,
performed
statistical
anal-
yses,
prepared
the
article,
and
had
primary
responsibility
for
patient
screening.
•EM,
DA,
AD,
KCN,
DY,
and
TA
supervised
the
design
and
execution
of
the
study,
contributed
to
the
preparation
of
the
article,
and
helped
with
patient
screening.
•All
authors
approved
the
manuscript.
Conflict
of
interest
statement
The
authors
report
no
conflicts
of
interest.
References
[1]
The
Ministry
of
Health
of
Turkey.
A
H1N1
hakkında
basın
ac¸
ıklaması.
The
Ministry
of
Health
of
Turkey;
2010.
http://www.grip.gov.tr/
index.php?option=com
content&view=article&id=868:12082010-tarihli-
acklama&catid=113:basin-duyurulari&Itemid=540
[last
accessed
01.09.
2013].
[2]
Centers
for
Disease
Control
and
Prevention.
H1N1
vaccination
rec-
ommendations.
Centers
for
Disease
Control
and
Prevention;
2009.
http://www.cdc.gov/h1n1flu/vaccination/acip.htm
[last
accessed
01.09.2013].
[3]
The
Ministry
of
Health
of
Turkey.
Eyüp
Can:As¸
ı
Hakkında
Sa˘
glık
Bakanı’na
19
soru,
http://www.istanbulhaber.com.tr/haber/bakanrecep-akdaga-19-
domuz-gribi-sorusu-19469.htm
[last
accessed
01.08.2013].
[4]
Rank
MA,
Li
JT.
Clinical
pearls
for
preventing,
diagnosing,
and
treating
sea-
sonal
and
2009
H1N1
influenza
infection
in
patients
with
asthma.
J
Allergy
Clin
Immunol
2009;124:1123–6.
[5]
Wu
J,
Xu
F,
Lu
L,
Lu
M,
Miao
L,
Gao
T,
et
al.
Safety
and
effectiveness
of
a
2009
H1N1
vaccine
in
Beijing.
N
Engl
J
Med
2010;363:2416–23.
[6]
Busse
WW,
Peters
SP,
Fenton
MJ,
Mitchell
H,
Bleecker
ER,
Castro
M,
et
al.
Vac-
cination
of
patients
with
mild
and
severe
asthma
with
a
2009
pandemic
H1N1
influenza
virus
vaccine.
J
Allergy
Clin
Immunol
2011;127:130–7.
[7]
Centers
for
Disease
C.
Prevention.
Interim
results:
Influenza
A/H1N1
2009
monovalent
vaccination
coverage—United
States,
October–December
2009.
MMWR
Morb
Mortal
Wkly
Rep,
59.
Centers
for
Disease
C;
2010.
p.
44–8.
[8]
Bone
A,
Guthmann
JP,
Nicolau
J,
Levy-Bruhl
D.
Population
and
risk
group
uptake
of
H1N1
influenza
vaccine
in
mainland
France
2009–2010:
results
of
a
national
vaccination
campaign.
Vaccine
2010;28:8157–61.
[9]
Department
of
Health.
Pandemic
H1N1
vaccine
uptake
fig-
ures
for
England
by
SHA
and
PCT.
Department
of
Health;
2010.
http://webarchive.nationalarchives.gov.uk/20130107105354/http://www.
dh.gov.uk/prod
consum
dh/groups/dh
digitalassets/@dh/@en/@ps/documents/
digitalasset/dh
114211.pdf
[last
accessed
01.09.2013].
[10]
Global
Initiative
for
Asthma
(GINA).
Global
strategy
for
asthma
management
and
prevention.
Available
from
www.ginaasthma.org
[last
accessed
July
2013].
[11]
Jain
S,
Kamimoto
L,
Bramley
AM,
Schmitz
AM,
Benoit
SR,
Louie
J,
et
al.
Hospital-
ized
patients
with
2009
H1N1
influenza
in
the
United
States,
April–June
2009.
N
Engl
J
Med
2009;361:1935–44.
[12]
Kloepfer
KM,
Olenec
JP,
Lee
WM,
Liu
G,
Vrtis
RF,
Roberg
KA,
et
al.
Increased
H1N1
infection
rate
in
children
with
asthma.
Am
J
Respir
Crit
Care
Med
2012;185:1275–9.
[13]
Cates
CJ,
Rowe
BH.
Vaccines
for
preventing
influenza
in
people
with
asthma.
Cochrane
Database
Syst
Rev
2013;2:CD000364.
[14]
Patria
MF,
Tenconi
R,
Esposito
S.
Efficacy
and
safety
of
influenza
vaccination
in
children
with
asthma.
Expert
Rev
Vaccines
2012;11:461–8.
[15]
Brown
JR,
Goebel
LJ,
Neitch
SM,
Tweel
HK,
Mufson
MA.
Barriers
to
vaccinating
the
elderly
with
H1N1
vaccine.
Am
J
Med
Sci
2011;342:24–6.
[16]
Nougairede
A,
Lagier
JC,
Ninove
L,
Sartor
C,
Badiaga
S,
Botelho
E,
et
al.
Likely
correlation
between
sources
of
information
and
acceptability
of
A/H1N1
swine-
origin
influenza
virus
vaccine
in
Marseille,
France.
PLoS
One
2010;5:e11292.
[17]
Ozer
A,
Arikan
DC,
Kirecci
E,
Ekerbicer
HC.
Status
of
pandemic
influenza
vac-
cination
and
factors
affecting
it
in
pregnant
women
in
Kahramanmaras,
an
eastern
Mediterranean
city
of
Turkey.
PLoS
One
2010;5:e14177.
[18]
Leo
HL,
Clark
SJ,
Butchart
AT,
Singer
DC,
Clark
NM,
Davis
MM.
2009
seasonal
and
H1N1
influenza
vaccination
compliance
in
asthmatic
children
and
adults.
J
Allergy
Clin
Immunol
2010;126:166–8.
[19]
Galarce
EM,
Minsky
S,
Viswanath
K.
Socioeconomic
status,
demograph-
ics,
beliefs
and
A(H1N1)
vaccine
uptake
in
the
United
States.
Vaccine
2011;29:5284–9.
[20]
Rubin
GJ,
Amlot
R,
Page
L,
Wessely
S.
Public
perceptions,
anxiety,
and
behaviour
change
in
relation
to
the
swine
flu
outbreak:
cross
sectional
telephone
survey.
BMJ
2009;339:b2651.
[21]
Akis
S,
Velipasaoglu
S,
Camurdan
AD,
Beyazova
U,
Sahin
F.
Factors
associated
with
parental
acceptance
and
refusal
of
pandemic
influenza
A/H1N1
vaccine
in
Turkey.
Eur
J
Pediatr
2011;170:1165–72.
[22]
Velan
B,
Kaplan
G,
Ziv
A,
Boyko
V,
Lerner-Geva
L.
Major
motives
in
non-
acceptance
of
A/H1N1
flu
vaccination:
the
weight
of
rational
assessment.
Vaccine
2011;29:1173–9.
[23]
Frew
PM,
Hixson
B,
del
Rio
C,
Esteves-Jaramillo
A,
Omer
SB.
Acceptance
of
pan-
demic
2009
Influenza
A/H1N1
vaccine
in
a
minority
population:
determinants
and
potential
points
of
intervention.
Pediatrics
2011;127(Suppl
1):S113–9.
[24]
Busse
WW,
Lemanske
Jr
RF,
Gern
JE.
Role
of
viral
respiratory
infections
in
asthma
and
asthma
exacerbations.
Lancet
2010;376:826–34.

Author's personal copy
2280
B.
Buyuktiryaki
et
al.
/
Vaccine
32
(2014)
2275–2280
[25]
Soyer
OU,
Hudaverdiyev
S,
Civelek
E,
Isik
E,
Karabulut
E,
Kocabas
C,
et
al.
Parental
perspectives
on
influenza
vaccination
in
children
with
asthma.
Pediatr
Pulmonol
2011;46:139–44.
[26]
Setbon
M,
Raude
J.
Factors
in
vaccination
intention
against
the
pandemic
influenza
A/H1N1.
Eur
J
Public
Health
2010;20:490–4.
[27]
Eastwood
K,
Durrheim
DN,
Jones
A,
Butler
M.
Acceptance
of
pandemic
(H1N1)
2009
influenza
vaccination
by
the
Australian
public.
Med
J
Aust
2010;192:33–6.
[28]
Gaygisiz
U,
Gaygisiz
E,
Ozkan
T,
Lajunen
T.
Why
were
Turks
unwilling
to
accept
the
A/H1N1
influenza-pandemic
vaccination?
People’s
beliefs
and
perceptions
about
the
swine
flu
outbreak
and
vaccine
in
the
later
stage
of
the
epidemic.
Vaccine
2010;29:329–33.
[29]
Chor
JS,
Ngai
KL,
Goggins
WB,
Wong
MC,
Wong
SY,
Lee
N,
et
al.
Willingness
of
Hong
Kong
healthcare
workers
to
accept
pre-pandemic
influenza
vaccination
at
different
WHO
alert
levels:
two
questionnaire
surveys.
BMJ
2009;339:b3391.
[30]
Merrill
RM,
Kelley
TA,
Cox
E,
Layman
AB,
Layton
BJ,
Lindsay
R.
Factors
and
barriers
influencing
influenza
vaccination
among
students
at
Brigham
Young
University.
Med
Sci
Monit
2010;16:PH29–34.
[31]
Seale
H,
Heywood
AE,
McLaws
ML,
Ward
KF,
Lowbridge
CP,
Van
D,
et
al.
Why
do
I
need
it?
I
am
not
at
risk!
Public
perceptions
towards
the
pandemic
(H1N1)
2009
vaccine.
BMC
Infect
Dis
2010;10:99.
[32]
Raude
J,
Caille-Brillet
AL,
Setbon
M.
The
2009
pandemic
H1N1
influenza
vac-
cination
in
France:
who
accepted
to
receive
the
vaccine
and
why?
PLoS
Curr
2010;2:RRN1188.
[33]
Sypsa
V,
Livanios
T,
Psichogiou
M,
Malliori
M,
Tsiodras
S,
Nikolakopoulos
I,
et
al.
Public
perceptions
in
relation
to
intention
to
receive
pan-
demic
influenza
vaccination
in
a
random
population
sample:
evidence
from
a
cross-sectional
telephone
survey.
Euro
Surveill
2009;1:4,
pii:
19437.
[34]
Corace
K,
Prematunge
C,
McCarthy
A,
Nair
RC,
Roth
V,
Hayes
T,
et
al.
Predicting
influenza
vaccination
uptake
among
health
care
workers:
what
are
the
key
motivators?
Am
J
Infect
Control
2013;41:679–84.
[35]
Bish
A,
Yardley
L,
Nicoll
A,
Michie
S.
Factors
associated
with
uptake
of
vaccination
against
pandemic
influenza:
a
systematic
review.
Vaccine
2011;29:6472–84.
[36]
Bults
M,
Beaujean
DJ,
Richardus
JH,
van
Steenbergen
JE,
Voeten
HA.
Pandemic
Influenza
A/H1N1
vaccination
in
The
Netherlands:
parental
reasoning
underlying
child
vaccination
choices.
Vaccine
2011;29:
6226–35.
[37]
Tozzi
AE,
Gesualdo
F,
Romano
M,
Caione
D.
Parental
attitude
toward
influenza
A(H1N1)v
vaccination
in
Italy.
Vaccine
2009;27:6807.