predictors of hpv vaccination uptake: a longitudinal study among parents
TRANSCRIPT
Predictors of HPV vaccination uptake a longitudinalstudy among parents
R Hofman1 P van Empelen2 J H Richardus13 I M C M de Kok1H J de Koning1 M van Ballegooijen1 and I J Korfage1
1Department of Public Health Erasmus University Medical Centre 3000 CA Rotterdam the Netherlands 2Department of
Health Promotion TNO Quality of Life 2333 AL Leiden the Netherlands and 3Municipal Public Health Service
Rotterdam-Rijnmond 3011 EN Rotterdam the Netherlands
Correspondence to R Hofman Email rhofmanerasmusmcnl
Received on February 25 2013 accepted on August 15 2013
Abstract
To assess among parents longitudinal predictorsof human papillomavirus (HPV) vaccination
uptake for their daughters random samples of
parents were identified via municipal services
and sent baseline questionnaires in June 2009
and follow-up questionnaires in November 2011
after their uptake decision Hierarchical logistic
regression analysis was used to assess whether
demographic characteristics and affective andsocial cognitive factors predicted uptake at
follow-up Response rates of the baseline and
follow-up questionnaire were 298 (1762
5918) and 743 (7931067) respectively
Uptake was predicted by a later (2011) versus
earlier (2010) decision about uptake as HPV vac-
cination implementation [odds ratio (OR) 248
95 confidence interval (CI) 111ndash552] antici-pated regret about no uptake (OR 143 95 CI
108ndash189) and intention (OR 261 95 CI
147ndash461) There was an interaction between
ambivalence and attitude (OR 168 95 CI
114ndash247) parents with a positive attitude and
a high ambivalence toward vaccination were
more likely to have their daughter vaccinated
than parents with a positive attitude and a lowambivalence An informed choice about uptake
(57 correct items) was made by 44 In conclu-
sion uptake was predicted by intention a later
(2011) versus earlier (2010) decision and by
anticipated regret about no uptake Decisions
regarding new vaccines are difficult to make
we recommend a well-balanced implementation
process
Introduction
In Europe 60 000 women are diagnosed with cer-
vical cancer annually [1] Cervical cancer can only
develop in the presence of infection with high-risk
human papillomavirus (HPV) [2 3] Two vaccines
are available which protect against HPV 16
and 18 which together cause about 70 of cer-
vical cancers [4] Preferably the HPV vaccine
is given prior to the initiation of sexual activity
because the degree of protection is reduced after
HPV infection and the incidence of HPV infection
is highest in the first few months after sexual
debut [5 6]
In November 2008 the Dutch National
Immunization Program (NIP) which is free of
charge and voluntary was extended with HPV
vaccinations for 12-year-old girls The effective-
ness of the NIP depends on the availability of
high-quality vaccines and acceptance by parents
[7] Although childhood vaccination is well-ac-
cepted among parents in the Netherlands with a
95 vaccination rate [8] uptake rates of the HPV
vaccine are much lower (58 in 2010) [9] In the
Netherlands 12-year-old girls are legally entitled
to make their own decision about uptake In prac-
tice however parents play a considerable role
in the decision making about the uptake of HPV
vaccinations [10 11]
HEALTH EDUCATION RESEARCH Vol29 no1 2014
Pages 83ndash96
Advance Access published 16 September 2013
The Author 2013 Published by Oxford University Press All rights reservedFor permissions please email journalspermissionsoupcom
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This study aims to elucidate which psychosocial
factors of parents predict intended and actual HPV
vaccination uptake Previous studies examining
(HPV) vaccination behavior [12ndash14] have generally
relied on psychosocial concepts derived from the
Theory of Planned Behavior (TPB) [15] and the
Health Belief Model (HBM) [16] Both models are
useful in explaining HPV vaccination uptake The
TPB proposes that the most proximal determinant of
behavior is intention which in turn is guided by
three constructs attitudes toward the behavior (ie
the evaluation of advantages and disadvantages of a
behavior) social norms (perceived approval or sup-
port of others) and perceived behavioral control
(perceived ease of performing a behavior) In ac-
cordance with the TPB the HBM suggests that be-
havior is the result of the evaluation of advantages
and disadvantages of a behavior However the
HBM suggests that an important prerequisite of
such an evaluation is the perceived severity and per-
sonal susceptibility of acquiring an illness
Although these models are useful in explaining
behavior toward vaccination including HPV vac-
cination these models generally neglect more af-
fective components that are likely to influence the
decision about and actual uptake of HPV vaccin-
ation [17] Such affective factors may explain the
vaccination behavior beyond the more cognitive
predictors [18] In focus group discussions on de-
cisions to vaccinate against HPV among parents of
HPV vaccination eligible girls factors that played
a role were the perceived lack of knowledge about
HPV vaccination (risk) the felt ambivalence about
the decision to vaccinate (simultaneous positive
and negative evaluations of an attitude object)
[19 20] (dis)trust in authorities perceived paren-
tal responsibility and the anticipation of regret of
(not) acting [21] These findings underpin obser-
vations that the first HPV vaccination campaigns
were met with (parental) concerns about the reli-
ability of the vaccine Therefore in this study we
assessed whether HPV vaccination uptake was
predicted by anticipated regret [22] (dis)trust in
health authorities [23] ambivalence social norm
intention knowledge andor perceived severity
and risk of cervical cancer In addition to studying
predictors of HPV vaccination uptake changes in
parental knowledge attitudes and ambivalence
were explored both before and after their decision
about uptake
Methods
Respondents
Questionnaires were sent to parents who had not
yet made the decision to have their daughter vac-
cinated against HPV but had to decide within
3ndash15 months when their daughters became 12
years of age In the Netherlands all girls receive
an invitation to get vaccinated with the bivalent
HPV vaccine (free of cost) in the year they turn
12 years of age
Procedure
Random samples of parents were identified via four
municipal health services spread throughout the
Netherlands These municipal services hold the
addresses of all girls eligible for HPV vaccination
in their region The Dutch vaccination program
offers one opportunity to get vaccinated against
HPV ie at age 12 years The baseline questionnaire
and an information letter were sent by mail to 5918
parents in June 2009 (the information letter was ad-
dressed to both parents) Parents could return the
completed questionnaire in a self-addressed enve-
lope The questionnaire was pilot tested to check
for face validity and for problems in interpretation
(nfrac14 10)
In the baseline questionnaire we asked parents if
they were willing to complete a follow-up question-
naire after the uptake decision After the baseline
questionnaires were sent the Mexican flu (H1N1
virus) outbreak in the summer of 2009 led to
the implementation of an H1N1 vaccination pro-
gram Therefore the HPV vaccination programs
were postponed until March 2010 and March
2011 Those who consented to complete a follow-
up questionnaire received this questionnaire in
November 2011
The study was approved by the Medical Ethics
Committee of the Erasmus MC Rotterdam
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Baseline questionnaire
Factors derived from HBM
Perceived risk and severity One single item
assessed parentsrsquo perceived risk of their daughter
getting cervical cancer if she was vaccinated and
one additional item assessed the perceived severity
if their daughter would get cervical cancer Both risk
and severity items (adapted from Weinstein [24])
were measured on an 11-point Likert scale
with higher scores indicating a higher risk or
severity [24]
Factors derived from TPB
Attitudes toward HPV vaccination Attitude
was assessed using nine items on a 5-point Likert
scale phrased as lsquoI think having my daughter getting
vaccinated against cervical cancer is rsquo (eg badndash
good unimportantndashimportant unwisendashwise harm-
fulndashbeneficial adapted from Marteau et al [25] and
van den Bergh [26]) The total score was calculated
as the mean of the nine items (Cronbachrsquos frac14 094)
Intention Parentsrsquo intention to have their
daughter vaccinated against cervical cancer was as-
sessed with the question lsquoI want to have my daugh-
ter vaccinated against cervical cancerrsquo response
options [definitely not probably not not sure
(yet) probably definitely
Parental subjective norms Social norms were
examined using eight items on a 5-point Likert scale
measuring the perceived beliefs about and desire to
comply with family partner general practitioner
and friends about vaccinating onersquos daughter against
HPV (Cronbachrsquos frac14 082) (adapted from Tiro
et al [27]) Parentsrsquo normative belief was assessed
using a question about what percentage of other par-
ents the respondents thought would want the vaccin-
ation for their 12-year-old daughters (11 options
ranging from 0 to 100) (adapted from Marlow
et al [28])
Complementary factors
HPV knowledge We developed a knowledge
scale with items about HPV HPV vaccination and
cervical cancer consisting of four truefalsedonrsquot
know items (eg lsquoThe HPV vaccination will
decrease the risk of cervical cancerrsquo) and three mul-
tiple choice questions with 3 or 4 response options
[eg lsquoWhat is the protection rate of the HPV vac-
cinersquo (response options 55 70 85 100)]
A total score was calculated by summing the correct
responses (score range 0ndash7)
Decisional evaluation The subscales satisfac-
tion-uncertainty (eg lsquoI am satisfied with my deci-
sionrsquo Cronbachrsquos frac14 080) and informed choice
(eg lsquoI made a well-informed choicersquo Cronbachrsquos
frac14 079) from the Decision Evaluation Scales [29]
were included to assess how respondents evaluated
their decision about having their daughter vacci-
nated or not Both scales consisted of five items
and responses were on a 5-point Likert scale
(1frac14 strongly disagree 5frac14 strongly agree)
Parental responsibility To asses parental re-
sponsibility we used the subscale lsquobasic needs ndash
health carersquo of the Perceptions of Parental Role
Scales [30] consisting of seven items (eg
lsquoArrange for child to see dentist for routine checkuprsquo)
on a 5-point Likert scale (1frac14 not at all important
5frac14 very important) Cronbachrsquos frac14 073
Anticipated regret and worry To measure
anticipated regret and worry we adapted two
items from Korfage et al [31] measured on a 7-
point Likert scale lsquoIf I donrsquot have my daughter vac-
cinated against cervical cancer then I would regret
thisthen I would worryrsquo (1frac14 definitely not 7frac14 def-
initely) The total score was calculated as the mean
of the two items (Cronbachrsquos frac14 082)
Ambivalence Ambivalence was measured
using two items regarding positive and negative
thoughts about HPV vaccination (adapted from
Kaplan [19]) lsquoConsidering only the positive things
about HPV vaccination and ignoring the negative
things then what do you think of HPV vaccinationrsquo
(response options not at all positive slightly posi-
tive quite positive extremely positive) and vice
versa for negative thoughts Total ambivalence
was calculated as half the sum of the positive and
negative judgments minus the absolute difference
between the two [32]
Trust We developed two items to assess trust in
the NIP and the HPV vaccine on a 6-point Likert
scale (1frac14 none 6frac14 a lot)
Predictors of HPV vaccination uptake
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Reasons for vaccinating Parentsrsquo reasons to
have or not to have their daughter vaccinated were
assessed using 11 pre-defined items for lsquovacci-
natingrsquo 17 items for lsquonot vaccinatingrsquo and an
option to write down additional reasons
Parental characteristics We assessed sex
marital status educational level job status ethnicity
and religion of the parents Female respondents were
asked about their perceived risk of getting cervical
cancer themselves (11-point Likert scale) (adapted
from Marlow et al [24]) and if they had ever had an
abnormal Pap smear result
Follow-up questionnaire
In the follow-up questionnaire we again assessed
knowledge attitude toward HPV vaccination deci-
sional evaluation social norms (without compliance
items because compliance will logically not change
over time) ambivalence risk perception and sever-
ity and trust In addition vaccination uptake was
assessed
An informed choice to participate or not [33 34]
ie a choice based on relevant knowledge consistent
with the decision makerrsquos values and behaviorally
implemented [25] was calculated using knowledge
(at follow-up) attitude (at baseline) and uptake As
there is no standard cut-off to measure sufficient
decision relevant knowledge we presented rates of
informed decisions for 3 4 5 and 6 correct items
(out of 7) As an example results with the cut-off
level of five correct items are fully displayed An
informed choice to have onersquos daughter vaccinated
is characterized by sufficient decision relevant
knowledge a positive attitude toward HPV vaccin-
ation (score gt3) and having onersquos daughter vacci-
nated An informed choice not to have onersquos
daughter vaccinated is characterized by sufficient
decision relevant knowledge a negative attitude to-
ward HPV vaccination (score lt3) and not having
onersquos daughter vaccinated An attitude score of
3 was defined as neutral
Data analyses
The significance of mean and frequency differences
between the baseline and follow-up group was
assessed with the MannndashWhitney U-test and V2 stat-
istics Pearson correlations were calculated to ana-
lyze associations between parent characteristics and
social cognitive factors To determine significant
predictors of uptake (yesno) measured at follow-
up (T2) multiple hierarchical logistic regression
analyses were performed with various factors
measured at baseline as independent variables In
Model 1 demographic characteristics were entered
because these were considered more distal and non-
modifiable predictors In Model 2a parent charac-
teristics were added Model 2b consisted of demo-
graphic characteristics and social cognitive factors
In Model 3 we entered demographic characteristics
parent characteristics social cognitive factors and
an interaction term of attitude ambivalence
Finally in Model 4 intention was added Intention
was added only in the last model because of its high
correlation with other predictors We aimed to show
significant predictors with and without intention in
the model The procedure recommended by Aiken
and West [35] was used to determine whether
ambivalence moderated the relationship between at-
titude and uptake and the unstandardized regression
coefficients were examined for attitude at different
levels of ambivalence (ie the mean ambivalence
score 1 SD above the mean and 1 SD below the
mean) [35] To compare predictors of uptake and
intention the regression analysis of Model 3 was
repeated with intention as the dependent variable
(ordinal logistic regression analyses)
To assess the impact of the time gap between
baseline and follow-up on changes in attitude and
ambivalence two linear regression analyses were
performed with change scores between the baseline
and follow-up measurement Variables that showed
a significant (Plt 005) change over time were
included First we used attitude as the dependent
variable Independent variables were knowledge in-
formed choice (subscale of the Decision Evaluation
Scales [29]) ambivalence toward HPV vaccination
social norm and trust in the vaccine Second we
used ambivalence toward HPV vaccination as the
dependent variable Independent variables were
knowledge informed choice social norm and trust
in the vaccine
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McNemarrsquos test was used to assess the signifi-
cance of the difference in correct responses to the
knowledge items between baseline and follow-up
Results
Respondents
The response rate of the baseline questionnaire was
298 (17625918) A total of 1067 respondents
were willing to complete the follow-up question-
naire of which 793 responded (743) (Fig 1)
At baseline the mean age of those who completed
both questionnaires was 43 years Most respondents
were female (baseline 933 follow-up 937)
had an intermediate (baseline 479 follow-
up 467) or high educational level (baseline
40 follow-up 450) and were born in the
Netherlands (baseline 910 follow-up 938)
In the follow-up group 652 (822) daughters
had been vaccinated against HPV The subgroup
that completed the follow-up assessment differed
significantly from those who did not on six charac-
teristics (Table I)
5918 questionnaires were distributed among parents with a daughter aged 10-11years not yet invited for vaccination (June 2009)
37 not eligible- 31 daughters already had HPV vaccination- 4 completed only 1 or 2 questions- 2 daughters completed the questionnaire
1725 questionnaires were eligible baseline measurement
Those willing to complete the follow-up questionnaire were sent a questionnaire n=1067 (Nov 2011)
7931067 (743) questionnaires completed at follow-up
274 questionnaires not returned
4156 were not returned
1762 (298) questionnaires werereturned
658 were not willing to complete the follow-up questionnaire
Bas
elin
eF
ollo
w-u
p
Fig 1 Flow diagram of numbers of questionnaires at baseline and at follow-up
Predictors of HPV vaccination uptake
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Table I Characteristics of the respondents (parents)
Total baseline
group (nfrac14 1725)
Subgroup that completed
follow-up assessment (nfrac14 793)
Characteristics Mean (SD) Mean (SD) P-value
Age at baseline (years) 428 (417) 430 (405) 0015
range 29ndash59 32ndash58
Children
Age (years) 133 (342) 133 (321)
Age range 0ndash34 0ndash34
Number of girls 17 (078) 17 (074)
Number of boys 09 (077) 09 (076)
n () n ()
Marital status 0372
Marriedcohabiting 1477 (872) 693 (894)
Partner but living alone 34 (20) 16 (21)
No partner 165 (97) 66 (85)
Sex 0233
Female 1596 (933) 743 (937)
Educational level lt0001
Low 200 (121) 64 (83)
Intermediate 789 (479) 358 (467)
High 658 (400) 345 (450)
Job status 0270
Paid job 1268 (786) 617 (816)
Housewife or houseman or unpaid job or student 295 (183) 119 (157)
No job 51 (32) 20 (26)
Net income per month (euros) lt0001
lt1500 161 (105) 45 (61)
1500ndash3000 584 (382) 267 (364)
3000ndash4500 488 (320) 264 (360)
gt4500 294 (193) 157 (214)
Country of birth lt0001
The Netherlands 1550 (910) 740 (938)
Turkey Morocco 37 (22) 6 (08)
Suriname Aruba Netherlands Antilles 16 (09) 4 (05)
Other 100 (59) 39 (49)
Country of birth of both parents 0002
The Netherlands 1459 (885) 703 (894)
Turkey Morocco 44 (27) 9 (11)
Suriname Aruba Netherlands Antilles 19 (12) 5 (06)
Other 126 (76) 69 (88)
Religion 0590
None 960 (570) 450 (579)
Christian 611 (363) 290 (373)
Muslim 57 (34) 13 (17)
Other 54 (32) 24 (31)
Decision about HPV vaccination uptake
In 2010 - 555 (715)
In 2011 - 221 (285)
(continued)
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Predictors of HPV vaccination uptake
Pearsonrsquos correlations showed that most associ-
ations between the predictors were positive
(Table II) Table III presents the results of the hier-
archical logistic regression analyses to predict
HPV vaccination uptake The first model in which
HPV vaccination uptake was regressed on demo-
graphic factors showed that uptake at follow-up
was significantly predicted by religion and the
year the decision about uptake was made (2011
versus 2010) (pseudo R2frac14 006) Specifically
those respondents without a religious affiliation
and those who had to decide in 2011 were more
likely to have their daughter vaccinated In Model
2a parent characteristics were added this model
explained an additional 29 variance HPV vaccin-
ation was more likely for parents with a higher edu-
cational level having no religious affiliation
decision about uptake in 2011 and higher trust in
the NIP and the vaccine In Model 2b (demographic
characteristics and social cognitive factors) signifi-
cant predictors were year of decision about uptake
(2011 versus 2010) a positive attitude toward HPV
vaccination social norm and anticipated regret and
worry about no uptake (pseudo R2frac14 053) In Model
3 (including all predictors except intention) vaccin-
ation was more likely for parents who had to decide
in 2011 ambivalence toward HPV vaccination
(under the condition that attitude is equal to 0) and
higher anticipated regret and worry about no uptake
The interaction term of attitude ambivalence was
also significant (pseudo R2frac14 057) In Model 4
(including all predictors) significant predictors of
uptake were the year the decision about uptake
was made (2011 versus 2010) a higher intention
ambivalence toward HPV vaccination (under the
condition that attitude is equal to 0) and the inter-
action term of attitude ambivalence
The significant interaction term attitude am-
bivalence showed that the predictive validity of at-
titude improved as scores of ambivalence increased
from low (bfrac14 089 Pfrac14 00238) to moderate
(bfrac14 144 Pfrac14 0001) and from moderate
(bfrac14 144 Pfrac14 0001) to high (bfrac14 198 Plt 0001)
Associations of HPV vaccination intention
Alternatively we performed an ordinal logistic re-
gression analysis with intention (instead of uptake)
as dependent variable (data not shown) This ana-
lysis showed that a higher intention was associated
with a positive attitude toward HPV vaccination
[odds ratio (OR) 1953 95 confidence interval
(CI) 1032ndash3693] (under the condition that am-
bivalence is frac140) ambivalence toward HPV vaccin-
ation (OR 239 95 CI 110ndash518) (under the
condition that attitude is frac140) trust in the vaccine
(OR 162 95 CI 116ndash227) anticipated regret
and worry about no uptake (OR 159 95 CI
Table I Continued
Total baseline
group (nfrac14 1725)
Subgroup that completed
follow-up assessment (nfrac14 793)
Characteristics Mean (SD) Mean (SD) P-value
If female abnormal Pap smear result 0103
Yes 185 (117) 98 (132)
No 1351 (856) 634 (853)
Never had a Pap smear taken 42 (27) 11 (15)
Daughter vaccinated against DPTPa and MMRb 0038
Yes 1654 (959) 778 (981)
Daughter vaccinated against HPV
Yes - 652 (831)
The subgroup that completed the follow-up assessment differed significantly from the baseline group on six characteristicsaDPTP refers to diphtheria pertussis tetanus and poliomyelitisbMMR refers to measles mumps and rubella
Predictors of HPV vaccination uptake
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Tab
leII
M
eans
standard
dev
iati
ons
(SD
)and
Pea
rsonrsquos
corr
elati
on
bet
wee
nth
epre
dic
tors
at
base
line
(nfrac14
793)
Mea
n(S
D)
12
34
56
78
910
11
12
1
Par
enta
lre
sponsi
bil
ity
45
0(0
46)
2
Tru
stin
NIP
48
6(0
67)
00
4
3
Tru
stin
vac
cine
43
1(0
92)
00
605
4
4
Per
ceiv
edsu
scep
tibil
ity
of
moth
erto
cerv
ical
cance
r
49
7(1
74)
00
500
100
2
5
Inte
nti
on
38
9(1
07)
00
304
8
07
3
00
5
6
Am
biv
alen
ce17
1(1
07)
00
7
02
0
02
6
00
1
02
9
7
Att
itude
tow
ard
HP
V
vac
cinat
ion
37
3(1
44)
00
9
05
1
07
7
00
508
4
03
3
8
Soci
alnorm
61
0(1
03
1)
01
5
03
3
05
1
00
706
1
01
8
06
4
9
Norm
ativ
ebel
ief
71
2(1
57)
00
501
9
03
3
00
103
3
00
9
03
4
03
7
10
Know
ledge
43
2(1
49)
00
9
01
0
00
300
300
3
00
700
200
3
00
3
11
Per
ceiv
edsu
scep
tibil
ity
of
dau
ghte
rif
vac
cinat
ed
toce
rvic
alca
nce
r
37
3(1
44)
00
6
02
3
03
0
04
1
02
6
00
3
03
1
02
3
02
3
00
1
12
Per
ceiv
edse
ver
ity
of
cerv
ical
cance
r
106
0(0
93)
02
5
00
400
500
300
500
400
600
700
9
01
2
00
1
13
Anti
cipat
edre
gre
tan
d
worr
yab
out
no
upta
ke
49
2(1
56)
02
3
03
8
06
2
01
1
06
9
01
9
07
1
05
3
03
6
00
6
02
3
02
0
Sm
all
effe
ctsi
ze
rgt
01
0
med
ium
effe
ctsi
ze
03
0lt
rlt
05
0
larg
eef
fect
size
rgt
05
0
Plt
00
5
Plt
00
1
R Hofman et al
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Tab
leII
IH
iera
rchic
al
logis
tic
regre
ssio
nanaly
ses
wit
hupta
ke(y
esn
o)
as
dep
enden
tva
riable
all
vari
able
sare
report
edby
pare
nts
at
base
line
Univ
aria
te
Model
1
(nfrac14
708)
Model
2a
(nfrac14
644)
Model
2b
(nfrac14
617)
Model
3
(nfrac14
572)
Model
4
(nfrac14
569)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
Dem
ogra
ph
icch
ara
cter
isti
cs
Age
of
par
ents
(yea
rs)
10
2(0
98ndash10
7)
10
1(0
96ndash10
6)
10
3(0
96ndash10
9)
10
2(0
95ndash11
0)
10
2(0
94ndash11
1)
10
1(0
93ndash10
9)
Educa
tional
level
11
5(1
00ndash13
4)
11
7(0
99ndash13
7)
12
5(1
00ndash15
4)
12
0(0
93ndash15
5)
12
7(0
96ndash17
0)
13
3(0
99ndash17
8)
No
reli
gio
us
affi
liat
ion
17
3(1
19ndash25
3)
16
3(1
09ndash24
2)
17
3(1
07ndash28
1)
11
2(0
63ndash20
0)
11
9(0
63ndash22
5)
11
6(0
60ndash22
3)
Dec
isio
nab
out
upta
ke
2011
(vs
2010)
20
8(1
28ndash33
6)
26
8(1
57ndash45
3)
26
9(1
42ndash51
0)
24
5(1
20ndash50
1)
24
8(1
11ndash55
2)
26
0(1
16ndash58
0)
Pare
nt
chara
cter
isti
cs
No
abnorm
alsm
ear
exper
ience
10
2(0
58ndash17
8)
09
4(0
45ndash19
5)
07
0(0
26ndash18
8)
06
8(0
24ndash19
5)
Par
enta
lre
sponsi
bil
ity
12
3(0
83ndash18
4)
15
3(0
91ndash25
9)
15
5(0
76ndash31
8)
18
6(0
90ndash38
3)
Tru
stin
NIP
35
4(2
61ndash48
1)
18
2(1
21ndash27
4)
14
0(0
86ndash23
0)
13
3(0
79ndash22
4)
Tru
stin
vac
cine
36
4(2
85ndash46
4)
34
1(2
49ndash46
8)
12
3(0
69ndash18
3)
09
9(0
59ndash16
7)
Per
ceiv
edsu
scep
tibil
ity
of
moth
erto
cerv
ical
cance
r
10
4(0
93ndash11
6)
10
3(0
88ndash12
1)
09
7(0
77ndash12
2)
09
6(0
76ndash12
2)
Soci
al
cogn
itiv
efa
ctors
Inte
nti
on
45
9(3
56ndash59
2)
26
1(1
47ndash46
1)
Am
biv
alen
ceto
war
dH
PV
vac
cinat
ion
08
2(0
69ndash09
2)
10
7(0
79ndash14
5)
02
7(0
08ndash08
7)
02
2(0
07ndash07
1)
Posi
tive
atti
tude
tow
ard
HP
Vvac
cinat
ion
57
3(4
26ndash77
1)
34
3(2
01ndash58
4)
17
0(0
69ndash42
1)
08
9(0
34ndash23
6)
Soci
alnorm
12
1(1
16ndash12
6)
10
7(1
01ndash11
3)
10
5(0
99ndash11
1)
10
3(0
97ndash10
9)
Norm
ativ
ebel
ief
14
4(1
28ndash16
3)
09
9(0
81ndash12
1)
10
3(0
83ndash12
9)
10
3(0
81ndash12
9)
Know
ledge
10
8(0
95ndash12
2)
09
5(0
87ndash10
4)
09
3(0
76ndash11
3)
09
5(0
78ndash11
7)
Per
ceiv
edsu
scep
tibil
ity
of
dau
ghte
rif
vac
cinat
ed
toce
rvic
alca
nce
r
06
5(0
57ndash07
4)
08
6(0
70ndash10
5)
08
9(0
69ndash11
4)
08
8(0
68ndash11
4)
Per
ceiv
edse
ver
ity
of
cerv
ical
cance
r
12
2(1
03ndash14
6)
10
8(0
81ndash14
2)
10
6(0
78ndash14
4)
10
8(0
79ndash14
8)
Anti
cipat
edre
gre
tan
d
worr
yab
out
no
upta
ke
22
3(1
93ndash25
8)
14
3(1
11ndash18
4)
14
3(1
08ndash18
9)
12
4(0
92ndash16
7)
Am
biv
alen
ce
atti
tude
inte
ract
ion
16
8(1
14ndash24
7)
17
9(1
22ndash26
2)
R2
00
603
505
305
705
9
Plt
00
5Plt
00
1an
dPlt
00
01
Predictors of HPV vaccination uptake
91
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nloaded from
132ndash192) and social norm (OR 107 95 CI
104ndash110) A lower uptake intention was asso-
ciated with a higher educational level (OR 083
95 CI 070ndash099) and a higher perceived parental
responsibility for their daughterrsquos health (OR 048
95 CI 030ndash075) The interaction term of atti-
tude ambivalence was significant (OR 073
95 CI 059ndash090)
Impact of time
Favorable changes in attitudes toward HPV uptake
over time were significantly related to an increase in
trust in the vaccine (OR 145 95 CI 136ndash153)
and social norm (OR 122 95 CI 115ndash128) over
time and a decrease in ambivalence toward HPV
vaccination (OR 094 95 CI 091ndash098) A de-
crease in ambivalence toward HPV vaccination
over time was significantly related to an increase
in feeling informed about HPV vaccination (OR
079 95 CI 069ndash091) and an increase in trust
in the vaccine (OR 088 95 CI 077ndash099) over
time
Informed decision making
Overall knowledge levels about the degreeduration
of protection were low at baseline and at follow-up
(33ndash43 correct answers) Percentages of correct
responses to five knowledge items increased signifi-
cantly at follow-up (Table IV) When five (out of
seven) correct items were defined as sufficient deci-
sion relevant knowledge then nfrac14 338 (439) of
the respondents made an informed choice about
uptake When four correct items were considered
sufficient then nfrac14 437 (657) of the respondents
made an informed choice about uptake (Table V)
Reasons for vaccinating or not
Main reasons as reported by parents at baseline to
have their daughter vaccinated include feeling re-
sponsible for her health (nfrac14 947 549) a family
history of cancer (nfrac14 128 74) anticipating
regret in case their daughter gets cervical cancer
(nfrac14 103 60) and other (nfrac14 547 317) Main
reasons as reported by parents at baseline not to have
their daughter vaccinated include that consequences
Table IV Knowledge items as completed by those who responded to the baseline and follow-up questionnaire (nfrac14 793)
Correct responses
Baseline
measurement
Follow-up
measurement
Significance level for
difference between
baseline and follow-up
n () n () P-value
Item (truefalse)
HPV causes cervical cancer (true) 496 (625) 479 (604) 0336
A condom protects 100 against HPV (false) 464 (585) 518 (653) 0001
The HPV vaccination will decrease the risk of cervical
cancer (true)
673 (849) 726 (916) lt0001
Vaccination in combination with having a smear taken is
more protective than only vaccination (true)
521 (657) 598 (754) lt0001
Item (multiple choice)
How is HPV transmitted (through blood oxygen sexual
contact)
699 (881) 730 (921) 0006
What is the protection rate of the HPV vaccine (55 70
85 100)
286 (361) 337 (425) 0005
What is the protection duration of a complete vaccination
against cervical cancer (at least 6 (8 at follow-up) years
at least 30 years lifetime)
289 (364) 262 (330) 0094
Correct answers are shaded
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nloaded from
of vaccinating are unpredictable (497 288) fear
of serious side-effects (nfrac14 401 232) and too
little information about the vaccine being available
(nfrac14 125 72)
Discussion
In this study among parents we assessed longitu-
dinal predictors of HPV vaccination uptake of their
daughters Uptake was predicted by intention a later
(2011) versus earlier (2010) decision about uptake
and anticipated regret and worry in case of abstain-
ing from HPV vaccination Ambivalence toward
HPV vaccination at baseline moderated the attitude
(baseline) uptake (follow-up) relationship with the
attitudendashuptake relationship being stronger at higher
ambivalence levels
HPV vaccination was most strongly predicted by
intention which fits the TPB model and was also
reported in an earlier study on predictors of HPV
vaccination uptake [22] In turn HPV vaccination
intention was positively associated with educational
level perceived parental responsibility for onersquos
daughterrsquos health trust in the vaccine the belief
that according to significant others their daughter
should be vaccinated and the motivation to comply
with that (social norm) and anticipated regret and
worry (which also predicted uptake) The relation-
ship found between intention and uptake and
between intention and social norm is consistent
with the TPB model and with another study [22]
which also confirms the association we found
between anticipated regretworry and uptake and
anticipated regretworry and intention The factors
lsquoperceived susceptibilityrsquo and lsquoseverityrsquo of cancer
of the HBM were not associated with intention or
uptake which confirms the results of an earlier study
[22 36]
A possible explanation for the positive effect on
uptake of having to decide later (2011) versus earlier
(2010) might be the amount of time that passed be-
tween the baseline questionnaire (2009) when an
intensive societal debate involving politics phys-
icians media parents and girls about HPV vaccin-
ation was ongoing and the actual decision about
uptake of vaccination In 2011 this debate probably
had less impact on the uptake decision than in 2010
Also after millions of girls worldwide had been
vaccinated and no serious side-effects had been
reported parents who had to decide later versus
earlier probably felt more reassured about the
vaccinersquos safety
This study shows that ambivalence moderated the
attitudendashuptake relationship Parents with a positive
attitude and a high level of ambivalence toward
HPV vaccination were more likely to have their
daughter vaccinated than parents with a positive at-
titude and a low level of ambivalence This finding
might be explained in two ways First ambivalence
is characterized as being subjectively uncomfortable
and people may be motivated to resolve the conflict-
ing evaluations that they hold [37] for example
by searching for information Second earlier
studies found that ambivalent people processed
pro-attitudinal messages to a greater extent than
counter-attitudinal messages probably because
pro-attitudinal messages are more likely to reduce
ambivalence [38 39] Taking these two mechanisms
together it is likely that in our study ambivalent
parents with a positive attitude toward HPV vaccin-
ation processed lsquopositiversquo messages about HPV vac-
cination to a greater extent than lsquonegativersquo messages
and were therefore more likely to have their
Table V Informed decision at follow-up (nfrac14 770)
Daughter
vaccinated
(nfrac14 640)
Daughter not
vaccinated
(nfrac14 130)
n () n ()
Positive attitude
Five or more correct items 280 (364) 14 (18)
Less than five correct items 246 (319) 16 (21)
Negative attitude
Five or more correct items 51 (66) 58 (75)
Less than five correct items 32 (42) 34 (44)
Knowledge was measured with seven items at follow-upInformed decision rate for cut-off at three correct items761 [(504 + 82)770] four correct items 657[(437 + 69)770] five correct items 439 [(280 + 58)770]six correct items 187 [(117 + 27)770] Due to missingitems analyses were based on nfrac14 770 respondents instead ofnfrac14 793 Informed choice (as defined) is shaded
Predictors of HPV vaccination uptake
93
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nloaded from
daughter vaccinated In other words parents who
had both positive attitudes and were ambivalent to-
ward HPV vaccination became even more positive
because they elaborated only information in favor of
HPV vaccination This may imply that this lsquobiasedrsquo
information processing has a negative impact on
informed decision making although parents will
have gained more knowledge during their efforts
to resolve their ambivalence
Assessing decisional factors related to HPV vac-
cination both before and after the decision-making
process about uptake provided a unique opportun-
ity to determine changes in those factors over time
As uptake was predicted by intention and intention
was highly correlated with attitude (rfrac14 084) (at
baseline) we think it is relevant to show which
factors are important for changes in attitude over
time Our results show that a more positive attitude
toward HPV vaccination over time was associated
with an increase in trust in the vaccine and in
social norm over time and a decrease in ambiva-
lence toward HPV vaccination over time This
latter factor was related to an increase in feeling
informed about HPV vaccination and an increase
in trust in the vaccine over time In summary over
time parents felt better informed became less am-
bivalent and had more trust in the vaccine These
results are in accordance with our finding that
girls who had to decide with their parents whether
or not to be vaccinated in 2011 were more likely
to be vaccinated than those who had to decide
in 2010
An important finding is that knowledge about the
duration of protection was low at both baseline and
follow-up For instance about 65 of the parents
thought that protection lasts 30 years or even life-
long As the duration of protection is still unknown
it is important that parents and girls know that
booster vaccinations might be needed in the future
When we applied a cut-off of four or five correct
knowledge items (out of seven) then the rates
of informed choice about uptake were not high
66 and 44 respectively However this finding
should be interpreted with caution because the
time period between the assessment of knowledge
and the last vaccination out of three shots was
1 month (decision in 2011) or 14 months (decision
in 2010) In educational material it should be clearly
stated what is known and not yet known about HPV
vaccination
Study strengths include the longitudinal design
as recommended by authors of a cross-sectional
study [40] the high (absolute) number of respond-
ents of the baseline (nfrac14 1725) and follow-up ques-
tionnaires (nfrac14 793) and the high response rate of the
follow-up questionnaire (74)
Limitations
A limitation was the low response rate of the base-
line questionnaire (30) which might be due to the
length of the questionnaire Our sample may there-
fore not be representative of the general population
as few parents had a low educational level Also
demographic characteristics of the follow-up group
were slightly different from those of the baseline
group with more parents being better educated
and well-off at follow-up These parents might pos-
sibly be more likely than those in the wider popula-
tion to seek to reduce high ambivalence by
searching information allowing them to respond
positively to the vaccine invitationmdashrather than do
nothing
Conclusion
In conclusion this study shows that intention a later
versus earlier decision about uptake and anticipated
regretworry about abstaining from vaccination
were predictors of uptake Anticipated regret was a
common predictor of intention and uptake and thus
an important factor in the decision-making process
about HPV vaccination In turn predictors of inten-
tion like social norm and trust in the vaccine are
also important when deciding about HPV vaccin-
ation Over time parents felt better informed
became less ambivalent and had more trust in the
vaccine
Practice implications
This study shows the usefulness of including affect-
ive factors in studies examining HPV vaccination
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nloaded from
behavior as anticipated regret trust in the vaccine
and ambivalence were found to play a role in the
decision making about uptake However it is also
important that parents are enabled to base their
decision about HPV vaccination of their daughter
on decision relevant knowledge As these results
suggest that people need sufficient time to decide
about the uptake of a new vaccine we recommend
a well-balanced stepwise process of implementa-
tion that is let parents first become aware of the
link between HPV and cervical cancer then provide
them with balanced information about all the
knowns and also the unknowns of HPV vaccination
and then finally offer them the opportunity to have
their daughter vaccinated As two-third of parents
wrongly thought that protection lasts 30 years or
even lifelong educational material should clearly
state that booster vaccinations might be needed in
the future
Acknowledgements
The authors thank the Dutch Cancer Society for
financial support and the participants for their
contribution to the study
Funding
The Dutch Cancer Society [EMCR 2008-3992
EMCR 2009-4561]
Conflict of interest statement
None declared
References
1 Karim-Kos HE de Vries E Soerjomataram I et al Recenttrends of cancer in Europe a combined approach of inci-dence survival and mortality for 17 cancer sites since the1990s Eur J Cancer 2008 44 1345ndash89
2 Bosch FX Lorincz A Munoz N et al The causal relationbetween human papillomavirus and cervical cancer J ClinPathol 2002 55 244ndash65
3 Walboomers JM Jacobs MV Manos MM et al Humanpapillomavirus is a necessary cause of invasive cervicalcancer worldwide J Pathol 1999 189 12ndash9
4 Munoz N Bosch FX Castellsague X et al Against whichhuman papillomavirus types shall we vaccinate and screenThe international perspective Int J Cancer 2004 111278ndash85
5 Koutsky LA Holmes KK Critchlow CW et al A cohortstudy of the risk of cervical intraepithelial neoplasia grade2 or 3 in relation to papillomavirus infection N Engl J Med1992 327 1272ndash8
6 Woodman CB Collins S Winter H et al Natural history ofcervical human papillomavirus infection in young women alongitudinal cohort study Lancet 2001 357 1831ndash6
7 Boot HJ Wallenburg I de Melker HE et al Assessing theintroduction of universal human papillomavirus vaccinationfor preadolescent girls in The Netherlands Vaccine 2007 256245ndash56
8 van Lier EA Oomen PJ Oostenbrug MWM et alImmunization coverage National ImmunizationProgramme in the Netherlands Year of report 2009[Vaccinatiegraad Rijksvaccinatieprogramma NederlandVerslagjaar 2009] Bilthoven RIVM 2009
9 Zwakhals SLN van Lier EA van HPV (cohort 1997) bymunicipality 2012 [HPV (cohort 1997) per gemeente2012] In Dutch National Atlas of Public HealthBilthoven RIVM 2012 (httpwwwzorgatlasnlpreventievaccinaties-en-screeninghpv-cohort-1997-vaccinatiegraad-per-gemeente-2012 accessed 2 September 2013)
10 Brabin L Roberts SA Stretch R et al A survey of adolescentexperiences of human papillomavirus vaccination in theManchester study Br J cancer 2009 101 1502ndash4
11 Brabin L Roberts SA Kitchener HC A semi-qualitativestudy of attitudes to vaccinating adolescents against humanpapillomavirus without parental consent BMC PublicHealth 2007 7 20
12 Brewer NT Fazekas KI Predictors of HPV vaccine accept-ability A theory-informed systematic review Prev Med2007 45 107ndash14
13 Kahn JA Rosenthal SL Jin Y et al Rates of human papillo-mavirus vaccination attitudes about vaccination and humanpapillomavirus prevalence in young women Obstet Gynecol2008 111 1103ndash10
14 Askelson NM Campo S Lowe JB et al Using the theoryof planned behavior to predict mothersrsquo intentions to vaccin-ate their daughters against HPV J Sch Nurs 2010 26194ndash202
15 Ajzen I The theory of Planned Behavior Organ Behav HumDecis Process 1991 50 179ndash211
16 Becker MH The health belief model and personal healthbehavior Health Edu Monogr 1974 2 324ndash508
17 Chapman GB Coups EJ Emotions and preventive healthbehavior worry regret and influenza vaccination HealthPsychol 2006 25 82ndash90
18 Paulussen TG Hoekstra F Lanting CI et al Determinants ofDutch parentsrsquo decisions to vaccinate their child Vaccine2006 24 644ndash51
19 Kaplan KJ On the ambivalence-indifference problem inattitude theory and measurement A suggested modificationof the semantic differential technique Psychol Bull 1972 77361ndash372
20 Dormandy E Hankins M Marteau TM Attitudes and uptakeof a screening test The moderating role of ambivalencePsychol Health 2006 21 499ndash511
Predictors of HPV vaccination uptake
95
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
21 Hofman R van Empelen P Vogel I et al Parental decisionalstrategies regarding HPV vaccination prior to media debatesa focus-group study J Health Commun 2013 18 866ndash80
22 Brewer NT Gottlieb SL Reiter PL et al Longitudinal pre-dictors of human papillomavirus vaccine initiation amongadolescent girls in a high-risk geographic area Sex TransmDis 2011 38 197ndash204
23 Marlow LA Waller J Wardle J Trust and experience aspredictors of HPV vaccine acceptance Hum Vaccin 20073 171ndash5
24 Weinstein ND Perceived probability perceived severityand health-protective behavior Health Psychol 2000 1965ndash74
25 Marteau TM Dormandy E Michie S A measure of informedchoice Health Expect 2001 4 99ndash108
26 van den Berg M Timmermans DR Ten Kate LP et al Arepregnant women making informed choices about prenatalscreening Genet Med 2005 7 332ndash8
27 Tiro JA Diamond PM Perz CA et al Validation of scalesmeasuring attitudes and norms related to mammographyscreening in women veterans Health Psychol 2005 24555ndash66
28 Marlow LAV Waller J Wardle J Parental attitudes to pre-pubertal HPV vaccination Vaccine 2007 25 1945ndash52
29 Stalmeier PF Roosmalen MS Verhoef LC et al Thedecision evaluation scales Patient Educ Couns 2005 57286ndash93
30 Gilbert LA Hanson GR Perceptions of parental role respon-sibilities among working people Development of a compre-hensive measure J Marriage Fam 1983 45 203ndash12
31 Korfage IJ van Ballegooijen M Wauben B et al Informedchoice on Pap smear still limited by lack of knowledge on the
meaning of false-positive or false-negative test resultsPatient Educ Couns 2011 85 214ndash8
32 Thompson MM Zanna MP The conflicted individual per-sonality-based and domain specific antecedents of ambiva-lent social attitudes J Pers 1995 63 259ndash88
33 General Medical Council Seeking Patientsrsquo Consent TheEthical Considerations London GMC 1998
34 Minister of Health Letter about screening [Kaderbriefscreening] PGZP 2848440 Ministry of Health Welfareand Sports The Hague 2008
35 Aiken LS West RR Multiple Regression Testing andInterpreting Interactions Newbury Park CA Sage 1991
36 Krawczyk AL Perez S Lau E et al Human papillomavirusvaccination intentions and uptake in college women HealthPsychol 2012 31 685ndash93
37 Newby-Clark IR McGregor I Zanna MP Thinking andcaring about cognitive inconsistency when and for whomdoes attitudinal ambivalence feel uncomfortable J Pers SocPsychol 2002 82 157ndash66
38 Nordgren LF van Harreveld F van der Pligt J Ambivalencediscomfort and motivated information processing J ExperSoc Psychol 2006 42 252ndash8
39 Clark JK Wegener DT Fabrigar LR Attitudinal ambiva-lence and message-based persuasion motivated processingof proattitudinal information and avoidance of counterattitu-dinal information Pers Soc Psychol Bull 2008 34 565ndash77
40 van Keulen HM Otten W Ruiter RA et al Determinants ofHPV vaccination intentions among Dutch girls and theirmothers a cross-sectional study BMC Public Health 201313 111
R Hofman et al
96
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oronto Library on O
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Dow
nloaded from
This study aims to elucidate which psychosocial
factors of parents predict intended and actual HPV
vaccination uptake Previous studies examining
(HPV) vaccination behavior [12ndash14] have generally
relied on psychosocial concepts derived from the
Theory of Planned Behavior (TPB) [15] and the
Health Belief Model (HBM) [16] Both models are
useful in explaining HPV vaccination uptake The
TPB proposes that the most proximal determinant of
behavior is intention which in turn is guided by
three constructs attitudes toward the behavior (ie
the evaluation of advantages and disadvantages of a
behavior) social norms (perceived approval or sup-
port of others) and perceived behavioral control
(perceived ease of performing a behavior) In ac-
cordance with the TPB the HBM suggests that be-
havior is the result of the evaluation of advantages
and disadvantages of a behavior However the
HBM suggests that an important prerequisite of
such an evaluation is the perceived severity and per-
sonal susceptibility of acquiring an illness
Although these models are useful in explaining
behavior toward vaccination including HPV vac-
cination these models generally neglect more af-
fective components that are likely to influence the
decision about and actual uptake of HPV vaccin-
ation [17] Such affective factors may explain the
vaccination behavior beyond the more cognitive
predictors [18] In focus group discussions on de-
cisions to vaccinate against HPV among parents of
HPV vaccination eligible girls factors that played
a role were the perceived lack of knowledge about
HPV vaccination (risk) the felt ambivalence about
the decision to vaccinate (simultaneous positive
and negative evaluations of an attitude object)
[19 20] (dis)trust in authorities perceived paren-
tal responsibility and the anticipation of regret of
(not) acting [21] These findings underpin obser-
vations that the first HPV vaccination campaigns
were met with (parental) concerns about the reli-
ability of the vaccine Therefore in this study we
assessed whether HPV vaccination uptake was
predicted by anticipated regret [22] (dis)trust in
health authorities [23] ambivalence social norm
intention knowledge andor perceived severity
and risk of cervical cancer In addition to studying
predictors of HPV vaccination uptake changes in
parental knowledge attitudes and ambivalence
were explored both before and after their decision
about uptake
Methods
Respondents
Questionnaires were sent to parents who had not
yet made the decision to have their daughter vac-
cinated against HPV but had to decide within
3ndash15 months when their daughters became 12
years of age In the Netherlands all girls receive
an invitation to get vaccinated with the bivalent
HPV vaccine (free of cost) in the year they turn
12 years of age
Procedure
Random samples of parents were identified via four
municipal health services spread throughout the
Netherlands These municipal services hold the
addresses of all girls eligible for HPV vaccination
in their region The Dutch vaccination program
offers one opportunity to get vaccinated against
HPV ie at age 12 years The baseline questionnaire
and an information letter were sent by mail to 5918
parents in June 2009 (the information letter was ad-
dressed to both parents) Parents could return the
completed questionnaire in a self-addressed enve-
lope The questionnaire was pilot tested to check
for face validity and for problems in interpretation
(nfrac14 10)
In the baseline questionnaire we asked parents if
they were willing to complete a follow-up question-
naire after the uptake decision After the baseline
questionnaires were sent the Mexican flu (H1N1
virus) outbreak in the summer of 2009 led to
the implementation of an H1N1 vaccination pro-
gram Therefore the HPV vaccination programs
were postponed until March 2010 and March
2011 Those who consented to complete a follow-
up questionnaire received this questionnaire in
November 2011
The study was approved by the Medical Ethics
Committee of the Erasmus MC Rotterdam
R Hofman et al
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Baseline questionnaire
Factors derived from HBM
Perceived risk and severity One single item
assessed parentsrsquo perceived risk of their daughter
getting cervical cancer if she was vaccinated and
one additional item assessed the perceived severity
if their daughter would get cervical cancer Both risk
and severity items (adapted from Weinstein [24])
were measured on an 11-point Likert scale
with higher scores indicating a higher risk or
severity [24]
Factors derived from TPB
Attitudes toward HPV vaccination Attitude
was assessed using nine items on a 5-point Likert
scale phrased as lsquoI think having my daughter getting
vaccinated against cervical cancer is rsquo (eg badndash
good unimportantndashimportant unwisendashwise harm-
fulndashbeneficial adapted from Marteau et al [25] and
van den Bergh [26]) The total score was calculated
as the mean of the nine items (Cronbachrsquos frac14 094)
Intention Parentsrsquo intention to have their
daughter vaccinated against cervical cancer was as-
sessed with the question lsquoI want to have my daugh-
ter vaccinated against cervical cancerrsquo response
options [definitely not probably not not sure
(yet) probably definitely
Parental subjective norms Social norms were
examined using eight items on a 5-point Likert scale
measuring the perceived beliefs about and desire to
comply with family partner general practitioner
and friends about vaccinating onersquos daughter against
HPV (Cronbachrsquos frac14 082) (adapted from Tiro
et al [27]) Parentsrsquo normative belief was assessed
using a question about what percentage of other par-
ents the respondents thought would want the vaccin-
ation for their 12-year-old daughters (11 options
ranging from 0 to 100) (adapted from Marlow
et al [28])
Complementary factors
HPV knowledge We developed a knowledge
scale with items about HPV HPV vaccination and
cervical cancer consisting of four truefalsedonrsquot
know items (eg lsquoThe HPV vaccination will
decrease the risk of cervical cancerrsquo) and three mul-
tiple choice questions with 3 or 4 response options
[eg lsquoWhat is the protection rate of the HPV vac-
cinersquo (response options 55 70 85 100)]
A total score was calculated by summing the correct
responses (score range 0ndash7)
Decisional evaluation The subscales satisfac-
tion-uncertainty (eg lsquoI am satisfied with my deci-
sionrsquo Cronbachrsquos frac14 080) and informed choice
(eg lsquoI made a well-informed choicersquo Cronbachrsquos
frac14 079) from the Decision Evaluation Scales [29]
were included to assess how respondents evaluated
their decision about having their daughter vacci-
nated or not Both scales consisted of five items
and responses were on a 5-point Likert scale
(1frac14 strongly disagree 5frac14 strongly agree)
Parental responsibility To asses parental re-
sponsibility we used the subscale lsquobasic needs ndash
health carersquo of the Perceptions of Parental Role
Scales [30] consisting of seven items (eg
lsquoArrange for child to see dentist for routine checkuprsquo)
on a 5-point Likert scale (1frac14 not at all important
5frac14 very important) Cronbachrsquos frac14 073
Anticipated regret and worry To measure
anticipated regret and worry we adapted two
items from Korfage et al [31] measured on a 7-
point Likert scale lsquoIf I donrsquot have my daughter vac-
cinated against cervical cancer then I would regret
thisthen I would worryrsquo (1frac14 definitely not 7frac14 def-
initely) The total score was calculated as the mean
of the two items (Cronbachrsquos frac14 082)
Ambivalence Ambivalence was measured
using two items regarding positive and negative
thoughts about HPV vaccination (adapted from
Kaplan [19]) lsquoConsidering only the positive things
about HPV vaccination and ignoring the negative
things then what do you think of HPV vaccinationrsquo
(response options not at all positive slightly posi-
tive quite positive extremely positive) and vice
versa for negative thoughts Total ambivalence
was calculated as half the sum of the positive and
negative judgments minus the absolute difference
between the two [32]
Trust We developed two items to assess trust in
the NIP and the HPV vaccine on a 6-point Likert
scale (1frac14 none 6frac14 a lot)
Predictors of HPV vaccination uptake
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Reasons for vaccinating Parentsrsquo reasons to
have or not to have their daughter vaccinated were
assessed using 11 pre-defined items for lsquovacci-
natingrsquo 17 items for lsquonot vaccinatingrsquo and an
option to write down additional reasons
Parental characteristics We assessed sex
marital status educational level job status ethnicity
and religion of the parents Female respondents were
asked about their perceived risk of getting cervical
cancer themselves (11-point Likert scale) (adapted
from Marlow et al [24]) and if they had ever had an
abnormal Pap smear result
Follow-up questionnaire
In the follow-up questionnaire we again assessed
knowledge attitude toward HPV vaccination deci-
sional evaluation social norms (without compliance
items because compliance will logically not change
over time) ambivalence risk perception and sever-
ity and trust In addition vaccination uptake was
assessed
An informed choice to participate or not [33 34]
ie a choice based on relevant knowledge consistent
with the decision makerrsquos values and behaviorally
implemented [25] was calculated using knowledge
(at follow-up) attitude (at baseline) and uptake As
there is no standard cut-off to measure sufficient
decision relevant knowledge we presented rates of
informed decisions for 3 4 5 and 6 correct items
(out of 7) As an example results with the cut-off
level of five correct items are fully displayed An
informed choice to have onersquos daughter vaccinated
is characterized by sufficient decision relevant
knowledge a positive attitude toward HPV vaccin-
ation (score gt3) and having onersquos daughter vacci-
nated An informed choice not to have onersquos
daughter vaccinated is characterized by sufficient
decision relevant knowledge a negative attitude to-
ward HPV vaccination (score lt3) and not having
onersquos daughter vaccinated An attitude score of
3 was defined as neutral
Data analyses
The significance of mean and frequency differences
between the baseline and follow-up group was
assessed with the MannndashWhitney U-test and V2 stat-
istics Pearson correlations were calculated to ana-
lyze associations between parent characteristics and
social cognitive factors To determine significant
predictors of uptake (yesno) measured at follow-
up (T2) multiple hierarchical logistic regression
analyses were performed with various factors
measured at baseline as independent variables In
Model 1 demographic characteristics were entered
because these were considered more distal and non-
modifiable predictors In Model 2a parent charac-
teristics were added Model 2b consisted of demo-
graphic characteristics and social cognitive factors
In Model 3 we entered demographic characteristics
parent characteristics social cognitive factors and
an interaction term of attitude ambivalence
Finally in Model 4 intention was added Intention
was added only in the last model because of its high
correlation with other predictors We aimed to show
significant predictors with and without intention in
the model The procedure recommended by Aiken
and West [35] was used to determine whether
ambivalence moderated the relationship between at-
titude and uptake and the unstandardized regression
coefficients were examined for attitude at different
levels of ambivalence (ie the mean ambivalence
score 1 SD above the mean and 1 SD below the
mean) [35] To compare predictors of uptake and
intention the regression analysis of Model 3 was
repeated with intention as the dependent variable
(ordinal logistic regression analyses)
To assess the impact of the time gap between
baseline and follow-up on changes in attitude and
ambivalence two linear regression analyses were
performed with change scores between the baseline
and follow-up measurement Variables that showed
a significant (Plt 005) change over time were
included First we used attitude as the dependent
variable Independent variables were knowledge in-
formed choice (subscale of the Decision Evaluation
Scales [29]) ambivalence toward HPV vaccination
social norm and trust in the vaccine Second we
used ambivalence toward HPV vaccination as the
dependent variable Independent variables were
knowledge informed choice social norm and trust
in the vaccine
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McNemarrsquos test was used to assess the signifi-
cance of the difference in correct responses to the
knowledge items between baseline and follow-up
Results
Respondents
The response rate of the baseline questionnaire was
298 (17625918) A total of 1067 respondents
were willing to complete the follow-up question-
naire of which 793 responded (743) (Fig 1)
At baseline the mean age of those who completed
both questionnaires was 43 years Most respondents
were female (baseline 933 follow-up 937)
had an intermediate (baseline 479 follow-
up 467) or high educational level (baseline
40 follow-up 450) and were born in the
Netherlands (baseline 910 follow-up 938)
In the follow-up group 652 (822) daughters
had been vaccinated against HPV The subgroup
that completed the follow-up assessment differed
significantly from those who did not on six charac-
teristics (Table I)
5918 questionnaires were distributed among parents with a daughter aged 10-11years not yet invited for vaccination (June 2009)
37 not eligible- 31 daughters already had HPV vaccination- 4 completed only 1 or 2 questions- 2 daughters completed the questionnaire
1725 questionnaires were eligible baseline measurement
Those willing to complete the follow-up questionnaire were sent a questionnaire n=1067 (Nov 2011)
7931067 (743) questionnaires completed at follow-up
274 questionnaires not returned
4156 were not returned
1762 (298) questionnaires werereturned
658 were not willing to complete the follow-up questionnaire
Bas
elin
eF
ollo
w-u
p
Fig 1 Flow diagram of numbers of questionnaires at baseline and at follow-up
Predictors of HPV vaccination uptake
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Table I Characteristics of the respondents (parents)
Total baseline
group (nfrac14 1725)
Subgroup that completed
follow-up assessment (nfrac14 793)
Characteristics Mean (SD) Mean (SD) P-value
Age at baseline (years) 428 (417) 430 (405) 0015
range 29ndash59 32ndash58
Children
Age (years) 133 (342) 133 (321)
Age range 0ndash34 0ndash34
Number of girls 17 (078) 17 (074)
Number of boys 09 (077) 09 (076)
n () n ()
Marital status 0372
Marriedcohabiting 1477 (872) 693 (894)
Partner but living alone 34 (20) 16 (21)
No partner 165 (97) 66 (85)
Sex 0233
Female 1596 (933) 743 (937)
Educational level lt0001
Low 200 (121) 64 (83)
Intermediate 789 (479) 358 (467)
High 658 (400) 345 (450)
Job status 0270
Paid job 1268 (786) 617 (816)
Housewife or houseman or unpaid job or student 295 (183) 119 (157)
No job 51 (32) 20 (26)
Net income per month (euros) lt0001
lt1500 161 (105) 45 (61)
1500ndash3000 584 (382) 267 (364)
3000ndash4500 488 (320) 264 (360)
gt4500 294 (193) 157 (214)
Country of birth lt0001
The Netherlands 1550 (910) 740 (938)
Turkey Morocco 37 (22) 6 (08)
Suriname Aruba Netherlands Antilles 16 (09) 4 (05)
Other 100 (59) 39 (49)
Country of birth of both parents 0002
The Netherlands 1459 (885) 703 (894)
Turkey Morocco 44 (27) 9 (11)
Suriname Aruba Netherlands Antilles 19 (12) 5 (06)
Other 126 (76) 69 (88)
Religion 0590
None 960 (570) 450 (579)
Christian 611 (363) 290 (373)
Muslim 57 (34) 13 (17)
Other 54 (32) 24 (31)
Decision about HPV vaccination uptake
In 2010 - 555 (715)
In 2011 - 221 (285)
(continued)
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Predictors of HPV vaccination uptake
Pearsonrsquos correlations showed that most associ-
ations between the predictors were positive
(Table II) Table III presents the results of the hier-
archical logistic regression analyses to predict
HPV vaccination uptake The first model in which
HPV vaccination uptake was regressed on demo-
graphic factors showed that uptake at follow-up
was significantly predicted by religion and the
year the decision about uptake was made (2011
versus 2010) (pseudo R2frac14 006) Specifically
those respondents without a religious affiliation
and those who had to decide in 2011 were more
likely to have their daughter vaccinated In Model
2a parent characteristics were added this model
explained an additional 29 variance HPV vaccin-
ation was more likely for parents with a higher edu-
cational level having no religious affiliation
decision about uptake in 2011 and higher trust in
the NIP and the vaccine In Model 2b (demographic
characteristics and social cognitive factors) signifi-
cant predictors were year of decision about uptake
(2011 versus 2010) a positive attitude toward HPV
vaccination social norm and anticipated regret and
worry about no uptake (pseudo R2frac14 053) In Model
3 (including all predictors except intention) vaccin-
ation was more likely for parents who had to decide
in 2011 ambivalence toward HPV vaccination
(under the condition that attitude is equal to 0) and
higher anticipated regret and worry about no uptake
The interaction term of attitude ambivalence was
also significant (pseudo R2frac14 057) In Model 4
(including all predictors) significant predictors of
uptake were the year the decision about uptake
was made (2011 versus 2010) a higher intention
ambivalence toward HPV vaccination (under the
condition that attitude is equal to 0) and the inter-
action term of attitude ambivalence
The significant interaction term attitude am-
bivalence showed that the predictive validity of at-
titude improved as scores of ambivalence increased
from low (bfrac14 089 Pfrac14 00238) to moderate
(bfrac14 144 Pfrac14 0001) and from moderate
(bfrac14 144 Pfrac14 0001) to high (bfrac14 198 Plt 0001)
Associations of HPV vaccination intention
Alternatively we performed an ordinal logistic re-
gression analysis with intention (instead of uptake)
as dependent variable (data not shown) This ana-
lysis showed that a higher intention was associated
with a positive attitude toward HPV vaccination
[odds ratio (OR) 1953 95 confidence interval
(CI) 1032ndash3693] (under the condition that am-
bivalence is frac140) ambivalence toward HPV vaccin-
ation (OR 239 95 CI 110ndash518) (under the
condition that attitude is frac140) trust in the vaccine
(OR 162 95 CI 116ndash227) anticipated regret
and worry about no uptake (OR 159 95 CI
Table I Continued
Total baseline
group (nfrac14 1725)
Subgroup that completed
follow-up assessment (nfrac14 793)
Characteristics Mean (SD) Mean (SD) P-value
If female abnormal Pap smear result 0103
Yes 185 (117) 98 (132)
No 1351 (856) 634 (853)
Never had a Pap smear taken 42 (27) 11 (15)
Daughter vaccinated against DPTPa and MMRb 0038
Yes 1654 (959) 778 (981)
Daughter vaccinated against HPV
Yes - 652 (831)
The subgroup that completed the follow-up assessment differed significantly from the baseline group on six characteristicsaDPTP refers to diphtheria pertussis tetanus and poliomyelitisbMMR refers to measles mumps and rubella
Predictors of HPV vaccination uptake
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Tab
leII
M
eans
standard
dev
iati
ons
(SD
)and
Pea
rsonrsquos
corr
elati
on
bet
wee
nth
epre
dic
tors
at
base
line
(nfrac14
793)
Mea
n(S
D)
12
34
56
78
910
11
12
1
Par
enta
lre
sponsi
bil
ity
45
0(0
46)
2
Tru
stin
NIP
48
6(0
67)
00
4
3
Tru
stin
vac
cine
43
1(0
92)
00
605
4
4
Per
ceiv
edsu
scep
tibil
ity
of
moth
erto
cerv
ical
cance
r
49
7(1
74)
00
500
100
2
5
Inte
nti
on
38
9(1
07)
00
304
8
07
3
00
5
6
Am
biv
alen
ce17
1(1
07)
00
7
02
0
02
6
00
1
02
9
7
Att
itude
tow
ard
HP
V
vac
cinat
ion
37
3(1
44)
00
9
05
1
07
7
00
508
4
03
3
8
Soci
alnorm
61
0(1
03
1)
01
5
03
3
05
1
00
706
1
01
8
06
4
9
Norm
ativ
ebel
ief
71
2(1
57)
00
501
9
03
3
00
103
3
00
9
03
4
03
7
10
Know
ledge
43
2(1
49)
00
9
01
0
00
300
300
3
00
700
200
3
00
3
11
Per
ceiv
edsu
scep
tibil
ity
of
dau
ghte
rif
vac
cinat
ed
toce
rvic
alca
nce
r
37
3(1
44)
00
6
02
3
03
0
04
1
02
6
00
3
03
1
02
3
02
3
00
1
12
Per
ceiv
edse
ver
ity
of
cerv
ical
cance
r
106
0(0
93)
02
5
00
400
500
300
500
400
600
700
9
01
2
00
1
13
Anti
cipat
edre
gre
tan
d
worr
yab
out
no
upta
ke
49
2(1
56)
02
3
03
8
06
2
01
1
06
9
01
9
07
1
05
3
03
6
00
6
02
3
02
0
Sm
all
effe
ctsi
ze
rgt
01
0
med
ium
effe
ctsi
ze
03
0lt
rlt
05
0
larg
eef
fect
size
rgt
05
0
Plt
00
5
Plt
00
1
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Tab
leII
IH
iera
rchic
al
logis
tic
regre
ssio
nanaly
ses
wit
hupta
ke(y
esn
o)
as
dep
enden
tva
riable
all
vari
able
sare
report
edby
pare
nts
at
base
line
Univ
aria
te
Model
1
(nfrac14
708)
Model
2a
(nfrac14
644)
Model
2b
(nfrac14
617)
Model
3
(nfrac14
572)
Model
4
(nfrac14
569)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
Dem
ogra
ph
icch
ara
cter
isti
cs
Age
of
par
ents
(yea
rs)
10
2(0
98ndash10
7)
10
1(0
96ndash10
6)
10
3(0
96ndash10
9)
10
2(0
95ndash11
0)
10
2(0
94ndash11
1)
10
1(0
93ndash10
9)
Educa
tional
level
11
5(1
00ndash13
4)
11
7(0
99ndash13
7)
12
5(1
00ndash15
4)
12
0(0
93ndash15
5)
12
7(0
96ndash17
0)
13
3(0
99ndash17
8)
No
reli
gio
us
affi
liat
ion
17
3(1
19ndash25
3)
16
3(1
09ndash24
2)
17
3(1
07ndash28
1)
11
2(0
63ndash20
0)
11
9(0
63ndash22
5)
11
6(0
60ndash22
3)
Dec
isio
nab
out
upta
ke
2011
(vs
2010)
20
8(1
28ndash33
6)
26
8(1
57ndash45
3)
26
9(1
42ndash51
0)
24
5(1
20ndash50
1)
24
8(1
11ndash55
2)
26
0(1
16ndash58
0)
Pare
nt
chara
cter
isti
cs
No
abnorm
alsm
ear
exper
ience
10
2(0
58ndash17
8)
09
4(0
45ndash19
5)
07
0(0
26ndash18
8)
06
8(0
24ndash19
5)
Par
enta
lre
sponsi
bil
ity
12
3(0
83ndash18
4)
15
3(0
91ndash25
9)
15
5(0
76ndash31
8)
18
6(0
90ndash38
3)
Tru
stin
NIP
35
4(2
61ndash48
1)
18
2(1
21ndash27
4)
14
0(0
86ndash23
0)
13
3(0
79ndash22
4)
Tru
stin
vac
cine
36
4(2
85ndash46
4)
34
1(2
49ndash46
8)
12
3(0
69ndash18
3)
09
9(0
59ndash16
7)
Per
ceiv
edsu
scep
tibil
ity
of
moth
erto
cerv
ical
cance
r
10
4(0
93ndash11
6)
10
3(0
88ndash12
1)
09
7(0
77ndash12
2)
09
6(0
76ndash12
2)
Soci
al
cogn
itiv
efa
ctors
Inte
nti
on
45
9(3
56ndash59
2)
26
1(1
47ndash46
1)
Am
biv
alen
ceto
war
dH
PV
vac
cinat
ion
08
2(0
69ndash09
2)
10
7(0
79ndash14
5)
02
7(0
08ndash08
7)
02
2(0
07ndash07
1)
Posi
tive
atti
tude
tow
ard
HP
Vvac
cinat
ion
57
3(4
26ndash77
1)
34
3(2
01ndash58
4)
17
0(0
69ndash42
1)
08
9(0
34ndash23
6)
Soci
alnorm
12
1(1
16ndash12
6)
10
7(1
01ndash11
3)
10
5(0
99ndash11
1)
10
3(0
97ndash10
9)
Norm
ativ
ebel
ief
14
4(1
28ndash16
3)
09
9(0
81ndash12
1)
10
3(0
83ndash12
9)
10
3(0
81ndash12
9)
Know
ledge
10
8(0
95ndash12
2)
09
5(0
87ndash10
4)
09
3(0
76ndash11
3)
09
5(0
78ndash11
7)
Per
ceiv
edsu
scep
tibil
ity
of
dau
ghte
rif
vac
cinat
ed
toce
rvic
alca
nce
r
06
5(0
57ndash07
4)
08
6(0
70ndash10
5)
08
9(0
69ndash11
4)
08
8(0
68ndash11
4)
Per
ceiv
edse
ver
ity
of
cerv
ical
cance
r
12
2(1
03ndash14
6)
10
8(0
81ndash14
2)
10
6(0
78ndash14
4)
10
8(0
79ndash14
8)
Anti
cipat
edre
gre
tan
d
worr
yab
out
no
upta
ke
22
3(1
93ndash25
8)
14
3(1
11ndash18
4)
14
3(1
08ndash18
9)
12
4(0
92ndash16
7)
Am
biv
alen
ce
atti
tude
inte
ract
ion
16
8(1
14ndash24
7)
17
9(1
22ndash26
2)
R2
00
603
505
305
705
9
Plt
00
5Plt
00
1an
dPlt
00
01
Predictors of HPV vaccination uptake
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nloaded from
132ndash192) and social norm (OR 107 95 CI
104ndash110) A lower uptake intention was asso-
ciated with a higher educational level (OR 083
95 CI 070ndash099) and a higher perceived parental
responsibility for their daughterrsquos health (OR 048
95 CI 030ndash075) The interaction term of atti-
tude ambivalence was significant (OR 073
95 CI 059ndash090)
Impact of time
Favorable changes in attitudes toward HPV uptake
over time were significantly related to an increase in
trust in the vaccine (OR 145 95 CI 136ndash153)
and social norm (OR 122 95 CI 115ndash128) over
time and a decrease in ambivalence toward HPV
vaccination (OR 094 95 CI 091ndash098) A de-
crease in ambivalence toward HPV vaccination
over time was significantly related to an increase
in feeling informed about HPV vaccination (OR
079 95 CI 069ndash091) and an increase in trust
in the vaccine (OR 088 95 CI 077ndash099) over
time
Informed decision making
Overall knowledge levels about the degreeduration
of protection were low at baseline and at follow-up
(33ndash43 correct answers) Percentages of correct
responses to five knowledge items increased signifi-
cantly at follow-up (Table IV) When five (out of
seven) correct items were defined as sufficient deci-
sion relevant knowledge then nfrac14 338 (439) of
the respondents made an informed choice about
uptake When four correct items were considered
sufficient then nfrac14 437 (657) of the respondents
made an informed choice about uptake (Table V)
Reasons for vaccinating or not
Main reasons as reported by parents at baseline to
have their daughter vaccinated include feeling re-
sponsible for her health (nfrac14 947 549) a family
history of cancer (nfrac14 128 74) anticipating
regret in case their daughter gets cervical cancer
(nfrac14 103 60) and other (nfrac14 547 317) Main
reasons as reported by parents at baseline not to have
their daughter vaccinated include that consequences
Table IV Knowledge items as completed by those who responded to the baseline and follow-up questionnaire (nfrac14 793)
Correct responses
Baseline
measurement
Follow-up
measurement
Significance level for
difference between
baseline and follow-up
n () n () P-value
Item (truefalse)
HPV causes cervical cancer (true) 496 (625) 479 (604) 0336
A condom protects 100 against HPV (false) 464 (585) 518 (653) 0001
The HPV vaccination will decrease the risk of cervical
cancer (true)
673 (849) 726 (916) lt0001
Vaccination in combination with having a smear taken is
more protective than only vaccination (true)
521 (657) 598 (754) lt0001
Item (multiple choice)
How is HPV transmitted (through blood oxygen sexual
contact)
699 (881) 730 (921) 0006
What is the protection rate of the HPV vaccine (55 70
85 100)
286 (361) 337 (425) 0005
What is the protection duration of a complete vaccination
against cervical cancer (at least 6 (8 at follow-up) years
at least 30 years lifetime)
289 (364) 262 (330) 0094
Correct answers are shaded
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nloaded from
of vaccinating are unpredictable (497 288) fear
of serious side-effects (nfrac14 401 232) and too
little information about the vaccine being available
(nfrac14 125 72)
Discussion
In this study among parents we assessed longitu-
dinal predictors of HPV vaccination uptake of their
daughters Uptake was predicted by intention a later
(2011) versus earlier (2010) decision about uptake
and anticipated regret and worry in case of abstain-
ing from HPV vaccination Ambivalence toward
HPV vaccination at baseline moderated the attitude
(baseline) uptake (follow-up) relationship with the
attitudendashuptake relationship being stronger at higher
ambivalence levels
HPV vaccination was most strongly predicted by
intention which fits the TPB model and was also
reported in an earlier study on predictors of HPV
vaccination uptake [22] In turn HPV vaccination
intention was positively associated with educational
level perceived parental responsibility for onersquos
daughterrsquos health trust in the vaccine the belief
that according to significant others their daughter
should be vaccinated and the motivation to comply
with that (social norm) and anticipated regret and
worry (which also predicted uptake) The relation-
ship found between intention and uptake and
between intention and social norm is consistent
with the TPB model and with another study [22]
which also confirms the association we found
between anticipated regretworry and uptake and
anticipated regretworry and intention The factors
lsquoperceived susceptibilityrsquo and lsquoseverityrsquo of cancer
of the HBM were not associated with intention or
uptake which confirms the results of an earlier study
[22 36]
A possible explanation for the positive effect on
uptake of having to decide later (2011) versus earlier
(2010) might be the amount of time that passed be-
tween the baseline questionnaire (2009) when an
intensive societal debate involving politics phys-
icians media parents and girls about HPV vaccin-
ation was ongoing and the actual decision about
uptake of vaccination In 2011 this debate probably
had less impact on the uptake decision than in 2010
Also after millions of girls worldwide had been
vaccinated and no serious side-effects had been
reported parents who had to decide later versus
earlier probably felt more reassured about the
vaccinersquos safety
This study shows that ambivalence moderated the
attitudendashuptake relationship Parents with a positive
attitude and a high level of ambivalence toward
HPV vaccination were more likely to have their
daughter vaccinated than parents with a positive at-
titude and a low level of ambivalence This finding
might be explained in two ways First ambivalence
is characterized as being subjectively uncomfortable
and people may be motivated to resolve the conflict-
ing evaluations that they hold [37] for example
by searching for information Second earlier
studies found that ambivalent people processed
pro-attitudinal messages to a greater extent than
counter-attitudinal messages probably because
pro-attitudinal messages are more likely to reduce
ambivalence [38 39] Taking these two mechanisms
together it is likely that in our study ambivalent
parents with a positive attitude toward HPV vaccin-
ation processed lsquopositiversquo messages about HPV vac-
cination to a greater extent than lsquonegativersquo messages
and were therefore more likely to have their
Table V Informed decision at follow-up (nfrac14 770)
Daughter
vaccinated
(nfrac14 640)
Daughter not
vaccinated
(nfrac14 130)
n () n ()
Positive attitude
Five or more correct items 280 (364) 14 (18)
Less than five correct items 246 (319) 16 (21)
Negative attitude
Five or more correct items 51 (66) 58 (75)
Less than five correct items 32 (42) 34 (44)
Knowledge was measured with seven items at follow-upInformed decision rate for cut-off at three correct items761 [(504 + 82)770] four correct items 657[(437 + 69)770] five correct items 439 [(280 + 58)770]six correct items 187 [(117 + 27)770] Due to missingitems analyses were based on nfrac14 770 respondents instead ofnfrac14 793 Informed choice (as defined) is shaded
Predictors of HPV vaccination uptake
93
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daughter vaccinated In other words parents who
had both positive attitudes and were ambivalent to-
ward HPV vaccination became even more positive
because they elaborated only information in favor of
HPV vaccination This may imply that this lsquobiasedrsquo
information processing has a negative impact on
informed decision making although parents will
have gained more knowledge during their efforts
to resolve their ambivalence
Assessing decisional factors related to HPV vac-
cination both before and after the decision-making
process about uptake provided a unique opportun-
ity to determine changes in those factors over time
As uptake was predicted by intention and intention
was highly correlated with attitude (rfrac14 084) (at
baseline) we think it is relevant to show which
factors are important for changes in attitude over
time Our results show that a more positive attitude
toward HPV vaccination over time was associated
with an increase in trust in the vaccine and in
social norm over time and a decrease in ambiva-
lence toward HPV vaccination over time This
latter factor was related to an increase in feeling
informed about HPV vaccination and an increase
in trust in the vaccine over time In summary over
time parents felt better informed became less am-
bivalent and had more trust in the vaccine These
results are in accordance with our finding that
girls who had to decide with their parents whether
or not to be vaccinated in 2011 were more likely
to be vaccinated than those who had to decide
in 2010
An important finding is that knowledge about the
duration of protection was low at both baseline and
follow-up For instance about 65 of the parents
thought that protection lasts 30 years or even life-
long As the duration of protection is still unknown
it is important that parents and girls know that
booster vaccinations might be needed in the future
When we applied a cut-off of four or five correct
knowledge items (out of seven) then the rates
of informed choice about uptake were not high
66 and 44 respectively However this finding
should be interpreted with caution because the
time period between the assessment of knowledge
and the last vaccination out of three shots was
1 month (decision in 2011) or 14 months (decision
in 2010) In educational material it should be clearly
stated what is known and not yet known about HPV
vaccination
Study strengths include the longitudinal design
as recommended by authors of a cross-sectional
study [40] the high (absolute) number of respond-
ents of the baseline (nfrac14 1725) and follow-up ques-
tionnaires (nfrac14 793) and the high response rate of the
follow-up questionnaire (74)
Limitations
A limitation was the low response rate of the base-
line questionnaire (30) which might be due to the
length of the questionnaire Our sample may there-
fore not be representative of the general population
as few parents had a low educational level Also
demographic characteristics of the follow-up group
were slightly different from those of the baseline
group with more parents being better educated
and well-off at follow-up These parents might pos-
sibly be more likely than those in the wider popula-
tion to seek to reduce high ambivalence by
searching information allowing them to respond
positively to the vaccine invitationmdashrather than do
nothing
Conclusion
In conclusion this study shows that intention a later
versus earlier decision about uptake and anticipated
regretworry about abstaining from vaccination
were predictors of uptake Anticipated regret was a
common predictor of intention and uptake and thus
an important factor in the decision-making process
about HPV vaccination In turn predictors of inten-
tion like social norm and trust in the vaccine are
also important when deciding about HPV vaccin-
ation Over time parents felt better informed
became less ambivalent and had more trust in the
vaccine
Practice implications
This study shows the usefulness of including affect-
ive factors in studies examining HPV vaccination
R Hofman et al
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nloaded from
behavior as anticipated regret trust in the vaccine
and ambivalence were found to play a role in the
decision making about uptake However it is also
important that parents are enabled to base their
decision about HPV vaccination of their daughter
on decision relevant knowledge As these results
suggest that people need sufficient time to decide
about the uptake of a new vaccine we recommend
a well-balanced stepwise process of implementa-
tion that is let parents first become aware of the
link between HPV and cervical cancer then provide
them with balanced information about all the
knowns and also the unknowns of HPV vaccination
and then finally offer them the opportunity to have
their daughter vaccinated As two-third of parents
wrongly thought that protection lasts 30 years or
even lifelong educational material should clearly
state that booster vaccinations might be needed in
the future
Acknowledgements
The authors thank the Dutch Cancer Society for
financial support and the participants for their
contribution to the study
Funding
The Dutch Cancer Society [EMCR 2008-3992
EMCR 2009-4561]
Conflict of interest statement
None declared
References
1 Karim-Kos HE de Vries E Soerjomataram I et al Recenttrends of cancer in Europe a combined approach of inci-dence survival and mortality for 17 cancer sites since the1990s Eur J Cancer 2008 44 1345ndash89
2 Bosch FX Lorincz A Munoz N et al The causal relationbetween human papillomavirus and cervical cancer J ClinPathol 2002 55 244ndash65
3 Walboomers JM Jacobs MV Manos MM et al Humanpapillomavirus is a necessary cause of invasive cervicalcancer worldwide J Pathol 1999 189 12ndash9
4 Munoz N Bosch FX Castellsague X et al Against whichhuman papillomavirus types shall we vaccinate and screenThe international perspective Int J Cancer 2004 111278ndash85
5 Koutsky LA Holmes KK Critchlow CW et al A cohortstudy of the risk of cervical intraepithelial neoplasia grade2 or 3 in relation to papillomavirus infection N Engl J Med1992 327 1272ndash8
6 Woodman CB Collins S Winter H et al Natural history ofcervical human papillomavirus infection in young women alongitudinal cohort study Lancet 2001 357 1831ndash6
7 Boot HJ Wallenburg I de Melker HE et al Assessing theintroduction of universal human papillomavirus vaccinationfor preadolescent girls in The Netherlands Vaccine 2007 256245ndash56
8 van Lier EA Oomen PJ Oostenbrug MWM et alImmunization coverage National ImmunizationProgramme in the Netherlands Year of report 2009[Vaccinatiegraad Rijksvaccinatieprogramma NederlandVerslagjaar 2009] Bilthoven RIVM 2009
9 Zwakhals SLN van Lier EA van HPV (cohort 1997) bymunicipality 2012 [HPV (cohort 1997) per gemeente2012] In Dutch National Atlas of Public HealthBilthoven RIVM 2012 (httpwwwzorgatlasnlpreventievaccinaties-en-screeninghpv-cohort-1997-vaccinatiegraad-per-gemeente-2012 accessed 2 September 2013)
10 Brabin L Roberts SA Stretch R et al A survey of adolescentexperiences of human papillomavirus vaccination in theManchester study Br J cancer 2009 101 1502ndash4
11 Brabin L Roberts SA Kitchener HC A semi-qualitativestudy of attitudes to vaccinating adolescents against humanpapillomavirus without parental consent BMC PublicHealth 2007 7 20
12 Brewer NT Fazekas KI Predictors of HPV vaccine accept-ability A theory-informed systematic review Prev Med2007 45 107ndash14
13 Kahn JA Rosenthal SL Jin Y et al Rates of human papillo-mavirus vaccination attitudes about vaccination and humanpapillomavirus prevalence in young women Obstet Gynecol2008 111 1103ndash10
14 Askelson NM Campo S Lowe JB et al Using the theoryof planned behavior to predict mothersrsquo intentions to vaccin-ate their daughters against HPV J Sch Nurs 2010 26194ndash202
15 Ajzen I The theory of Planned Behavior Organ Behav HumDecis Process 1991 50 179ndash211
16 Becker MH The health belief model and personal healthbehavior Health Edu Monogr 1974 2 324ndash508
17 Chapman GB Coups EJ Emotions and preventive healthbehavior worry regret and influenza vaccination HealthPsychol 2006 25 82ndash90
18 Paulussen TG Hoekstra F Lanting CI et al Determinants ofDutch parentsrsquo decisions to vaccinate their child Vaccine2006 24 644ndash51
19 Kaplan KJ On the ambivalence-indifference problem inattitude theory and measurement A suggested modificationof the semantic differential technique Psychol Bull 1972 77361ndash372
20 Dormandy E Hankins M Marteau TM Attitudes and uptakeof a screening test The moderating role of ambivalencePsychol Health 2006 21 499ndash511
Predictors of HPV vaccination uptake
95
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
21 Hofman R van Empelen P Vogel I et al Parental decisionalstrategies regarding HPV vaccination prior to media debatesa focus-group study J Health Commun 2013 18 866ndash80
22 Brewer NT Gottlieb SL Reiter PL et al Longitudinal pre-dictors of human papillomavirus vaccine initiation amongadolescent girls in a high-risk geographic area Sex TransmDis 2011 38 197ndash204
23 Marlow LA Waller J Wardle J Trust and experience aspredictors of HPV vaccine acceptance Hum Vaccin 20073 171ndash5
24 Weinstein ND Perceived probability perceived severityand health-protective behavior Health Psychol 2000 1965ndash74
25 Marteau TM Dormandy E Michie S A measure of informedchoice Health Expect 2001 4 99ndash108
26 van den Berg M Timmermans DR Ten Kate LP et al Arepregnant women making informed choices about prenatalscreening Genet Med 2005 7 332ndash8
27 Tiro JA Diamond PM Perz CA et al Validation of scalesmeasuring attitudes and norms related to mammographyscreening in women veterans Health Psychol 2005 24555ndash66
28 Marlow LAV Waller J Wardle J Parental attitudes to pre-pubertal HPV vaccination Vaccine 2007 25 1945ndash52
29 Stalmeier PF Roosmalen MS Verhoef LC et al Thedecision evaluation scales Patient Educ Couns 2005 57286ndash93
30 Gilbert LA Hanson GR Perceptions of parental role respon-sibilities among working people Development of a compre-hensive measure J Marriage Fam 1983 45 203ndash12
31 Korfage IJ van Ballegooijen M Wauben B et al Informedchoice on Pap smear still limited by lack of knowledge on the
meaning of false-positive or false-negative test resultsPatient Educ Couns 2011 85 214ndash8
32 Thompson MM Zanna MP The conflicted individual per-sonality-based and domain specific antecedents of ambiva-lent social attitudes J Pers 1995 63 259ndash88
33 General Medical Council Seeking Patientsrsquo Consent TheEthical Considerations London GMC 1998
34 Minister of Health Letter about screening [Kaderbriefscreening] PGZP 2848440 Ministry of Health Welfareand Sports The Hague 2008
35 Aiken LS West RR Multiple Regression Testing andInterpreting Interactions Newbury Park CA Sage 1991
36 Krawczyk AL Perez S Lau E et al Human papillomavirusvaccination intentions and uptake in college women HealthPsychol 2012 31 685ndash93
37 Newby-Clark IR McGregor I Zanna MP Thinking andcaring about cognitive inconsistency when and for whomdoes attitudinal ambivalence feel uncomfortable J Pers SocPsychol 2002 82 157ndash66
38 Nordgren LF van Harreveld F van der Pligt J Ambivalencediscomfort and motivated information processing J ExperSoc Psychol 2006 42 252ndash8
39 Clark JK Wegener DT Fabrigar LR Attitudinal ambiva-lence and message-based persuasion motivated processingof proattitudinal information and avoidance of counterattitu-dinal information Pers Soc Psychol Bull 2008 34 565ndash77
40 van Keulen HM Otten W Ruiter RA et al Determinants ofHPV vaccination intentions among Dutch girls and theirmothers a cross-sectional study BMC Public Health 201313 111
R Hofman et al
96
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Baseline questionnaire
Factors derived from HBM
Perceived risk and severity One single item
assessed parentsrsquo perceived risk of their daughter
getting cervical cancer if she was vaccinated and
one additional item assessed the perceived severity
if their daughter would get cervical cancer Both risk
and severity items (adapted from Weinstein [24])
were measured on an 11-point Likert scale
with higher scores indicating a higher risk or
severity [24]
Factors derived from TPB
Attitudes toward HPV vaccination Attitude
was assessed using nine items on a 5-point Likert
scale phrased as lsquoI think having my daughter getting
vaccinated against cervical cancer is rsquo (eg badndash
good unimportantndashimportant unwisendashwise harm-
fulndashbeneficial adapted from Marteau et al [25] and
van den Bergh [26]) The total score was calculated
as the mean of the nine items (Cronbachrsquos frac14 094)
Intention Parentsrsquo intention to have their
daughter vaccinated against cervical cancer was as-
sessed with the question lsquoI want to have my daugh-
ter vaccinated against cervical cancerrsquo response
options [definitely not probably not not sure
(yet) probably definitely
Parental subjective norms Social norms were
examined using eight items on a 5-point Likert scale
measuring the perceived beliefs about and desire to
comply with family partner general practitioner
and friends about vaccinating onersquos daughter against
HPV (Cronbachrsquos frac14 082) (adapted from Tiro
et al [27]) Parentsrsquo normative belief was assessed
using a question about what percentage of other par-
ents the respondents thought would want the vaccin-
ation for their 12-year-old daughters (11 options
ranging from 0 to 100) (adapted from Marlow
et al [28])
Complementary factors
HPV knowledge We developed a knowledge
scale with items about HPV HPV vaccination and
cervical cancer consisting of four truefalsedonrsquot
know items (eg lsquoThe HPV vaccination will
decrease the risk of cervical cancerrsquo) and three mul-
tiple choice questions with 3 or 4 response options
[eg lsquoWhat is the protection rate of the HPV vac-
cinersquo (response options 55 70 85 100)]
A total score was calculated by summing the correct
responses (score range 0ndash7)
Decisional evaluation The subscales satisfac-
tion-uncertainty (eg lsquoI am satisfied with my deci-
sionrsquo Cronbachrsquos frac14 080) and informed choice
(eg lsquoI made a well-informed choicersquo Cronbachrsquos
frac14 079) from the Decision Evaluation Scales [29]
were included to assess how respondents evaluated
their decision about having their daughter vacci-
nated or not Both scales consisted of five items
and responses were on a 5-point Likert scale
(1frac14 strongly disagree 5frac14 strongly agree)
Parental responsibility To asses parental re-
sponsibility we used the subscale lsquobasic needs ndash
health carersquo of the Perceptions of Parental Role
Scales [30] consisting of seven items (eg
lsquoArrange for child to see dentist for routine checkuprsquo)
on a 5-point Likert scale (1frac14 not at all important
5frac14 very important) Cronbachrsquos frac14 073
Anticipated regret and worry To measure
anticipated regret and worry we adapted two
items from Korfage et al [31] measured on a 7-
point Likert scale lsquoIf I donrsquot have my daughter vac-
cinated against cervical cancer then I would regret
thisthen I would worryrsquo (1frac14 definitely not 7frac14 def-
initely) The total score was calculated as the mean
of the two items (Cronbachrsquos frac14 082)
Ambivalence Ambivalence was measured
using two items regarding positive and negative
thoughts about HPV vaccination (adapted from
Kaplan [19]) lsquoConsidering only the positive things
about HPV vaccination and ignoring the negative
things then what do you think of HPV vaccinationrsquo
(response options not at all positive slightly posi-
tive quite positive extremely positive) and vice
versa for negative thoughts Total ambivalence
was calculated as half the sum of the positive and
negative judgments minus the absolute difference
between the two [32]
Trust We developed two items to assess trust in
the NIP and the HPV vaccine on a 6-point Likert
scale (1frac14 none 6frac14 a lot)
Predictors of HPV vaccination uptake
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Reasons for vaccinating Parentsrsquo reasons to
have or not to have their daughter vaccinated were
assessed using 11 pre-defined items for lsquovacci-
natingrsquo 17 items for lsquonot vaccinatingrsquo and an
option to write down additional reasons
Parental characteristics We assessed sex
marital status educational level job status ethnicity
and religion of the parents Female respondents were
asked about their perceived risk of getting cervical
cancer themselves (11-point Likert scale) (adapted
from Marlow et al [24]) and if they had ever had an
abnormal Pap smear result
Follow-up questionnaire
In the follow-up questionnaire we again assessed
knowledge attitude toward HPV vaccination deci-
sional evaluation social norms (without compliance
items because compliance will logically not change
over time) ambivalence risk perception and sever-
ity and trust In addition vaccination uptake was
assessed
An informed choice to participate or not [33 34]
ie a choice based on relevant knowledge consistent
with the decision makerrsquos values and behaviorally
implemented [25] was calculated using knowledge
(at follow-up) attitude (at baseline) and uptake As
there is no standard cut-off to measure sufficient
decision relevant knowledge we presented rates of
informed decisions for 3 4 5 and 6 correct items
(out of 7) As an example results with the cut-off
level of five correct items are fully displayed An
informed choice to have onersquos daughter vaccinated
is characterized by sufficient decision relevant
knowledge a positive attitude toward HPV vaccin-
ation (score gt3) and having onersquos daughter vacci-
nated An informed choice not to have onersquos
daughter vaccinated is characterized by sufficient
decision relevant knowledge a negative attitude to-
ward HPV vaccination (score lt3) and not having
onersquos daughter vaccinated An attitude score of
3 was defined as neutral
Data analyses
The significance of mean and frequency differences
between the baseline and follow-up group was
assessed with the MannndashWhitney U-test and V2 stat-
istics Pearson correlations were calculated to ana-
lyze associations between parent characteristics and
social cognitive factors To determine significant
predictors of uptake (yesno) measured at follow-
up (T2) multiple hierarchical logistic regression
analyses were performed with various factors
measured at baseline as independent variables In
Model 1 demographic characteristics were entered
because these were considered more distal and non-
modifiable predictors In Model 2a parent charac-
teristics were added Model 2b consisted of demo-
graphic characteristics and social cognitive factors
In Model 3 we entered demographic characteristics
parent characteristics social cognitive factors and
an interaction term of attitude ambivalence
Finally in Model 4 intention was added Intention
was added only in the last model because of its high
correlation with other predictors We aimed to show
significant predictors with and without intention in
the model The procedure recommended by Aiken
and West [35] was used to determine whether
ambivalence moderated the relationship between at-
titude and uptake and the unstandardized regression
coefficients were examined for attitude at different
levels of ambivalence (ie the mean ambivalence
score 1 SD above the mean and 1 SD below the
mean) [35] To compare predictors of uptake and
intention the regression analysis of Model 3 was
repeated with intention as the dependent variable
(ordinal logistic regression analyses)
To assess the impact of the time gap between
baseline and follow-up on changes in attitude and
ambivalence two linear regression analyses were
performed with change scores between the baseline
and follow-up measurement Variables that showed
a significant (Plt 005) change over time were
included First we used attitude as the dependent
variable Independent variables were knowledge in-
formed choice (subscale of the Decision Evaluation
Scales [29]) ambivalence toward HPV vaccination
social norm and trust in the vaccine Second we
used ambivalence toward HPV vaccination as the
dependent variable Independent variables were
knowledge informed choice social norm and trust
in the vaccine
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McNemarrsquos test was used to assess the signifi-
cance of the difference in correct responses to the
knowledge items between baseline and follow-up
Results
Respondents
The response rate of the baseline questionnaire was
298 (17625918) A total of 1067 respondents
were willing to complete the follow-up question-
naire of which 793 responded (743) (Fig 1)
At baseline the mean age of those who completed
both questionnaires was 43 years Most respondents
were female (baseline 933 follow-up 937)
had an intermediate (baseline 479 follow-
up 467) or high educational level (baseline
40 follow-up 450) and were born in the
Netherlands (baseline 910 follow-up 938)
In the follow-up group 652 (822) daughters
had been vaccinated against HPV The subgroup
that completed the follow-up assessment differed
significantly from those who did not on six charac-
teristics (Table I)
5918 questionnaires were distributed among parents with a daughter aged 10-11years not yet invited for vaccination (June 2009)
37 not eligible- 31 daughters already had HPV vaccination- 4 completed only 1 or 2 questions- 2 daughters completed the questionnaire
1725 questionnaires were eligible baseline measurement
Those willing to complete the follow-up questionnaire were sent a questionnaire n=1067 (Nov 2011)
7931067 (743) questionnaires completed at follow-up
274 questionnaires not returned
4156 were not returned
1762 (298) questionnaires werereturned
658 were not willing to complete the follow-up questionnaire
Bas
elin
eF
ollo
w-u
p
Fig 1 Flow diagram of numbers of questionnaires at baseline and at follow-up
Predictors of HPV vaccination uptake
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Table I Characteristics of the respondents (parents)
Total baseline
group (nfrac14 1725)
Subgroup that completed
follow-up assessment (nfrac14 793)
Characteristics Mean (SD) Mean (SD) P-value
Age at baseline (years) 428 (417) 430 (405) 0015
range 29ndash59 32ndash58
Children
Age (years) 133 (342) 133 (321)
Age range 0ndash34 0ndash34
Number of girls 17 (078) 17 (074)
Number of boys 09 (077) 09 (076)
n () n ()
Marital status 0372
Marriedcohabiting 1477 (872) 693 (894)
Partner but living alone 34 (20) 16 (21)
No partner 165 (97) 66 (85)
Sex 0233
Female 1596 (933) 743 (937)
Educational level lt0001
Low 200 (121) 64 (83)
Intermediate 789 (479) 358 (467)
High 658 (400) 345 (450)
Job status 0270
Paid job 1268 (786) 617 (816)
Housewife or houseman or unpaid job or student 295 (183) 119 (157)
No job 51 (32) 20 (26)
Net income per month (euros) lt0001
lt1500 161 (105) 45 (61)
1500ndash3000 584 (382) 267 (364)
3000ndash4500 488 (320) 264 (360)
gt4500 294 (193) 157 (214)
Country of birth lt0001
The Netherlands 1550 (910) 740 (938)
Turkey Morocco 37 (22) 6 (08)
Suriname Aruba Netherlands Antilles 16 (09) 4 (05)
Other 100 (59) 39 (49)
Country of birth of both parents 0002
The Netherlands 1459 (885) 703 (894)
Turkey Morocco 44 (27) 9 (11)
Suriname Aruba Netherlands Antilles 19 (12) 5 (06)
Other 126 (76) 69 (88)
Religion 0590
None 960 (570) 450 (579)
Christian 611 (363) 290 (373)
Muslim 57 (34) 13 (17)
Other 54 (32) 24 (31)
Decision about HPV vaccination uptake
In 2010 - 555 (715)
In 2011 - 221 (285)
(continued)
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Predictors of HPV vaccination uptake
Pearsonrsquos correlations showed that most associ-
ations between the predictors were positive
(Table II) Table III presents the results of the hier-
archical logistic regression analyses to predict
HPV vaccination uptake The first model in which
HPV vaccination uptake was regressed on demo-
graphic factors showed that uptake at follow-up
was significantly predicted by religion and the
year the decision about uptake was made (2011
versus 2010) (pseudo R2frac14 006) Specifically
those respondents without a religious affiliation
and those who had to decide in 2011 were more
likely to have their daughter vaccinated In Model
2a parent characteristics were added this model
explained an additional 29 variance HPV vaccin-
ation was more likely for parents with a higher edu-
cational level having no religious affiliation
decision about uptake in 2011 and higher trust in
the NIP and the vaccine In Model 2b (demographic
characteristics and social cognitive factors) signifi-
cant predictors were year of decision about uptake
(2011 versus 2010) a positive attitude toward HPV
vaccination social norm and anticipated regret and
worry about no uptake (pseudo R2frac14 053) In Model
3 (including all predictors except intention) vaccin-
ation was more likely for parents who had to decide
in 2011 ambivalence toward HPV vaccination
(under the condition that attitude is equal to 0) and
higher anticipated regret and worry about no uptake
The interaction term of attitude ambivalence was
also significant (pseudo R2frac14 057) In Model 4
(including all predictors) significant predictors of
uptake were the year the decision about uptake
was made (2011 versus 2010) a higher intention
ambivalence toward HPV vaccination (under the
condition that attitude is equal to 0) and the inter-
action term of attitude ambivalence
The significant interaction term attitude am-
bivalence showed that the predictive validity of at-
titude improved as scores of ambivalence increased
from low (bfrac14 089 Pfrac14 00238) to moderate
(bfrac14 144 Pfrac14 0001) and from moderate
(bfrac14 144 Pfrac14 0001) to high (bfrac14 198 Plt 0001)
Associations of HPV vaccination intention
Alternatively we performed an ordinal logistic re-
gression analysis with intention (instead of uptake)
as dependent variable (data not shown) This ana-
lysis showed that a higher intention was associated
with a positive attitude toward HPV vaccination
[odds ratio (OR) 1953 95 confidence interval
(CI) 1032ndash3693] (under the condition that am-
bivalence is frac140) ambivalence toward HPV vaccin-
ation (OR 239 95 CI 110ndash518) (under the
condition that attitude is frac140) trust in the vaccine
(OR 162 95 CI 116ndash227) anticipated regret
and worry about no uptake (OR 159 95 CI
Table I Continued
Total baseline
group (nfrac14 1725)
Subgroup that completed
follow-up assessment (nfrac14 793)
Characteristics Mean (SD) Mean (SD) P-value
If female abnormal Pap smear result 0103
Yes 185 (117) 98 (132)
No 1351 (856) 634 (853)
Never had a Pap smear taken 42 (27) 11 (15)
Daughter vaccinated against DPTPa and MMRb 0038
Yes 1654 (959) 778 (981)
Daughter vaccinated against HPV
Yes - 652 (831)
The subgroup that completed the follow-up assessment differed significantly from the baseline group on six characteristicsaDPTP refers to diphtheria pertussis tetanus and poliomyelitisbMMR refers to measles mumps and rubella
Predictors of HPV vaccination uptake
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Tab
leII
M
eans
standard
dev
iati
ons
(SD
)and
Pea
rsonrsquos
corr
elati
on
bet
wee
nth
epre
dic
tors
at
base
line
(nfrac14
793)
Mea
n(S
D)
12
34
56
78
910
11
12
1
Par
enta
lre
sponsi
bil
ity
45
0(0
46)
2
Tru
stin
NIP
48
6(0
67)
00
4
3
Tru
stin
vac
cine
43
1(0
92)
00
605
4
4
Per
ceiv
edsu
scep
tibil
ity
of
moth
erto
cerv
ical
cance
r
49
7(1
74)
00
500
100
2
5
Inte
nti
on
38
9(1
07)
00
304
8
07
3
00
5
6
Am
biv
alen
ce17
1(1
07)
00
7
02
0
02
6
00
1
02
9
7
Att
itude
tow
ard
HP
V
vac
cinat
ion
37
3(1
44)
00
9
05
1
07
7
00
508
4
03
3
8
Soci
alnorm
61
0(1
03
1)
01
5
03
3
05
1
00
706
1
01
8
06
4
9
Norm
ativ
ebel
ief
71
2(1
57)
00
501
9
03
3
00
103
3
00
9
03
4
03
7
10
Know
ledge
43
2(1
49)
00
9
01
0
00
300
300
3
00
700
200
3
00
3
11
Per
ceiv
edsu
scep
tibil
ity
of
dau
ghte
rif
vac
cinat
ed
toce
rvic
alca
nce
r
37
3(1
44)
00
6
02
3
03
0
04
1
02
6
00
3
03
1
02
3
02
3
00
1
12
Per
ceiv
edse
ver
ity
of
cerv
ical
cance
r
106
0(0
93)
02
5
00
400
500
300
500
400
600
700
9
01
2
00
1
13
Anti
cipat
edre
gre
tan
d
worr
yab
out
no
upta
ke
49
2(1
56)
02
3
03
8
06
2
01
1
06
9
01
9
07
1
05
3
03
6
00
6
02
3
02
0
Sm
all
effe
ctsi
ze
rgt
01
0
med
ium
effe
ctsi
ze
03
0lt
rlt
05
0
larg
eef
fect
size
rgt
05
0
Plt
00
5
Plt
00
1
R Hofman et al
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Dow
nloaded from
Tab
leII
IH
iera
rchic
al
logis
tic
regre
ssio
nanaly
ses
wit
hupta
ke(y
esn
o)
as
dep
enden
tva
riable
all
vari
able
sare
report
edby
pare
nts
at
base
line
Univ
aria
te
Model
1
(nfrac14
708)
Model
2a
(nfrac14
644)
Model
2b
(nfrac14
617)
Model
3
(nfrac14
572)
Model
4
(nfrac14
569)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
Dem
ogra
ph
icch
ara
cter
isti
cs
Age
of
par
ents
(yea
rs)
10
2(0
98ndash10
7)
10
1(0
96ndash10
6)
10
3(0
96ndash10
9)
10
2(0
95ndash11
0)
10
2(0
94ndash11
1)
10
1(0
93ndash10
9)
Educa
tional
level
11
5(1
00ndash13
4)
11
7(0
99ndash13
7)
12
5(1
00ndash15
4)
12
0(0
93ndash15
5)
12
7(0
96ndash17
0)
13
3(0
99ndash17
8)
No
reli
gio
us
affi
liat
ion
17
3(1
19ndash25
3)
16
3(1
09ndash24
2)
17
3(1
07ndash28
1)
11
2(0
63ndash20
0)
11
9(0
63ndash22
5)
11
6(0
60ndash22
3)
Dec
isio
nab
out
upta
ke
2011
(vs
2010)
20
8(1
28ndash33
6)
26
8(1
57ndash45
3)
26
9(1
42ndash51
0)
24
5(1
20ndash50
1)
24
8(1
11ndash55
2)
26
0(1
16ndash58
0)
Pare
nt
chara
cter
isti
cs
No
abnorm
alsm
ear
exper
ience
10
2(0
58ndash17
8)
09
4(0
45ndash19
5)
07
0(0
26ndash18
8)
06
8(0
24ndash19
5)
Par
enta
lre
sponsi
bil
ity
12
3(0
83ndash18
4)
15
3(0
91ndash25
9)
15
5(0
76ndash31
8)
18
6(0
90ndash38
3)
Tru
stin
NIP
35
4(2
61ndash48
1)
18
2(1
21ndash27
4)
14
0(0
86ndash23
0)
13
3(0
79ndash22
4)
Tru
stin
vac
cine
36
4(2
85ndash46
4)
34
1(2
49ndash46
8)
12
3(0
69ndash18
3)
09
9(0
59ndash16
7)
Per
ceiv
edsu
scep
tibil
ity
of
moth
erto
cerv
ical
cance
r
10
4(0
93ndash11
6)
10
3(0
88ndash12
1)
09
7(0
77ndash12
2)
09
6(0
76ndash12
2)
Soci
al
cogn
itiv
efa
ctors
Inte
nti
on
45
9(3
56ndash59
2)
26
1(1
47ndash46
1)
Am
biv
alen
ceto
war
dH
PV
vac
cinat
ion
08
2(0
69ndash09
2)
10
7(0
79ndash14
5)
02
7(0
08ndash08
7)
02
2(0
07ndash07
1)
Posi
tive
atti
tude
tow
ard
HP
Vvac
cinat
ion
57
3(4
26ndash77
1)
34
3(2
01ndash58
4)
17
0(0
69ndash42
1)
08
9(0
34ndash23
6)
Soci
alnorm
12
1(1
16ndash12
6)
10
7(1
01ndash11
3)
10
5(0
99ndash11
1)
10
3(0
97ndash10
9)
Norm
ativ
ebel
ief
14
4(1
28ndash16
3)
09
9(0
81ndash12
1)
10
3(0
83ndash12
9)
10
3(0
81ndash12
9)
Know
ledge
10
8(0
95ndash12
2)
09
5(0
87ndash10
4)
09
3(0
76ndash11
3)
09
5(0
78ndash11
7)
Per
ceiv
edsu
scep
tibil
ity
of
dau
ghte
rif
vac
cinat
ed
toce
rvic
alca
nce
r
06
5(0
57ndash07
4)
08
6(0
70ndash10
5)
08
9(0
69ndash11
4)
08
8(0
68ndash11
4)
Per
ceiv
edse
ver
ity
of
cerv
ical
cance
r
12
2(1
03ndash14
6)
10
8(0
81ndash14
2)
10
6(0
78ndash14
4)
10
8(0
79ndash14
8)
Anti
cipat
edre
gre
tan
d
worr
yab
out
no
upta
ke
22
3(1
93ndash25
8)
14
3(1
11ndash18
4)
14
3(1
08ndash18
9)
12
4(0
92ndash16
7)
Am
biv
alen
ce
atti
tude
inte
ract
ion
16
8(1
14ndash24
7)
17
9(1
22ndash26
2)
R2
00
603
505
305
705
9
Plt
00
5Plt
00
1an
dPlt
00
01
Predictors of HPV vaccination uptake
91
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nloaded from
132ndash192) and social norm (OR 107 95 CI
104ndash110) A lower uptake intention was asso-
ciated with a higher educational level (OR 083
95 CI 070ndash099) and a higher perceived parental
responsibility for their daughterrsquos health (OR 048
95 CI 030ndash075) The interaction term of atti-
tude ambivalence was significant (OR 073
95 CI 059ndash090)
Impact of time
Favorable changes in attitudes toward HPV uptake
over time were significantly related to an increase in
trust in the vaccine (OR 145 95 CI 136ndash153)
and social norm (OR 122 95 CI 115ndash128) over
time and a decrease in ambivalence toward HPV
vaccination (OR 094 95 CI 091ndash098) A de-
crease in ambivalence toward HPV vaccination
over time was significantly related to an increase
in feeling informed about HPV vaccination (OR
079 95 CI 069ndash091) and an increase in trust
in the vaccine (OR 088 95 CI 077ndash099) over
time
Informed decision making
Overall knowledge levels about the degreeduration
of protection were low at baseline and at follow-up
(33ndash43 correct answers) Percentages of correct
responses to five knowledge items increased signifi-
cantly at follow-up (Table IV) When five (out of
seven) correct items were defined as sufficient deci-
sion relevant knowledge then nfrac14 338 (439) of
the respondents made an informed choice about
uptake When four correct items were considered
sufficient then nfrac14 437 (657) of the respondents
made an informed choice about uptake (Table V)
Reasons for vaccinating or not
Main reasons as reported by parents at baseline to
have their daughter vaccinated include feeling re-
sponsible for her health (nfrac14 947 549) a family
history of cancer (nfrac14 128 74) anticipating
regret in case their daughter gets cervical cancer
(nfrac14 103 60) and other (nfrac14 547 317) Main
reasons as reported by parents at baseline not to have
their daughter vaccinated include that consequences
Table IV Knowledge items as completed by those who responded to the baseline and follow-up questionnaire (nfrac14 793)
Correct responses
Baseline
measurement
Follow-up
measurement
Significance level for
difference between
baseline and follow-up
n () n () P-value
Item (truefalse)
HPV causes cervical cancer (true) 496 (625) 479 (604) 0336
A condom protects 100 against HPV (false) 464 (585) 518 (653) 0001
The HPV vaccination will decrease the risk of cervical
cancer (true)
673 (849) 726 (916) lt0001
Vaccination in combination with having a smear taken is
more protective than only vaccination (true)
521 (657) 598 (754) lt0001
Item (multiple choice)
How is HPV transmitted (through blood oxygen sexual
contact)
699 (881) 730 (921) 0006
What is the protection rate of the HPV vaccine (55 70
85 100)
286 (361) 337 (425) 0005
What is the protection duration of a complete vaccination
against cervical cancer (at least 6 (8 at follow-up) years
at least 30 years lifetime)
289 (364) 262 (330) 0094
Correct answers are shaded
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nloaded from
of vaccinating are unpredictable (497 288) fear
of serious side-effects (nfrac14 401 232) and too
little information about the vaccine being available
(nfrac14 125 72)
Discussion
In this study among parents we assessed longitu-
dinal predictors of HPV vaccination uptake of their
daughters Uptake was predicted by intention a later
(2011) versus earlier (2010) decision about uptake
and anticipated regret and worry in case of abstain-
ing from HPV vaccination Ambivalence toward
HPV vaccination at baseline moderated the attitude
(baseline) uptake (follow-up) relationship with the
attitudendashuptake relationship being stronger at higher
ambivalence levels
HPV vaccination was most strongly predicted by
intention which fits the TPB model and was also
reported in an earlier study on predictors of HPV
vaccination uptake [22] In turn HPV vaccination
intention was positively associated with educational
level perceived parental responsibility for onersquos
daughterrsquos health trust in the vaccine the belief
that according to significant others their daughter
should be vaccinated and the motivation to comply
with that (social norm) and anticipated regret and
worry (which also predicted uptake) The relation-
ship found between intention and uptake and
between intention and social norm is consistent
with the TPB model and with another study [22]
which also confirms the association we found
between anticipated regretworry and uptake and
anticipated regretworry and intention The factors
lsquoperceived susceptibilityrsquo and lsquoseverityrsquo of cancer
of the HBM were not associated with intention or
uptake which confirms the results of an earlier study
[22 36]
A possible explanation for the positive effect on
uptake of having to decide later (2011) versus earlier
(2010) might be the amount of time that passed be-
tween the baseline questionnaire (2009) when an
intensive societal debate involving politics phys-
icians media parents and girls about HPV vaccin-
ation was ongoing and the actual decision about
uptake of vaccination In 2011 this debate probably
had less impact on the uptake decision than in 2010
Also after millions of girls worldwide had been
vaccinated and no serious side-effects had been
reported parents who had to decide later versus
earlier probably felt more reassured about the
vaccinersquos safety
This study shows that ambivalence moderated the
attitudendashuptake relationship Parents with a positive
attitude and a high level of ambivalence toward
HPV vaccination were more likely to have their
daughter vaccinated than parents with a positive at-
titude and a low level of ambivalence This finding
might be explained in two ways First ambivalence
is characterized as being subjectively uncomfortable
and people may be motivated to resolve the conflict-
ing evaluations that they hold [37] for example
by searching for information Second earlier
studies found that ambivalent people processed
pro-attitudinal messages to a greater extent than
counter-attitudinal messages probably because
pro-attitudinal messages are more likely to reduce
ambivalence [38 39] Taking these two mechanisms
together it is likely that in our study ambivalent
parents with a positive attitude toward HPV vaccin-
ation processed lsquopositiversquo messages about HPV vac-
cination to a greater extent than lsquonegativersquo messages
and were therefore more likely to have their
Table V Informed decision at follow-up (nfrac14 770)
Daughter
vaccinated
(nfrac14 640)
Daughter not
vaccinated
(nfrac14 130)
n () n ()
Positive attitude
Five or more correct items 280 (364) 14 (18)
Less than five correct items 246 (319) 16 (21)
Negative attitude
Five or more correct items 51 (66) 58 (75)
Less than five correct items 32 (42) 34 (44)
Knowledge was measured with seven items at follow-upInformed decision rate for cut-off at three correct items761 [(504 + 82)770] four correct items 657[(437 + 69)770] five correct items 439 [(280 + 58)770]six correct items 187 [(117 + 27)770] Due to missingitems analyses were based on nfrac14 770 respondents instead ofnfrac14 793 Informed choice (as defined) is shaded
Predictors of HPV vaccination uptake
93
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nloaded from
daughter vaccinated In other words parents who
had both positive attitudes and were ambivalent to-
ward HPV vaccination became even more positive
because they elaborated only information in favor of
HPV vaccination This may imply that this lsquobiasedrsquo
information processing has a negative impact on
informed decision making although parents will
have gained more knowledge during their efforts
to resolve their ambivalence
Assessing decisional factors related to HPV vac-
cination both before and after the decision-making
process about uptake provided a unique opportun-
ity to determine changes in those factors over time
As uptake was predicted by intention and intention
was highly correlated with attitude (rfrac14 084) (at
baseline) we think it is relevant to show which
factors are important for changes in attitude over
time Our results show that a more positive attitude
toward HPV vaccination over time was associated
with an increase in trust in the vaccine and in
social norm over time and a decrease in ambiva-
lence toward HPV vaccination over time This
latter factor was related to an increase in feeling
informed about HPV vaccination and an increase
in trust in the vaccine over time In summary over
time parents felt better informed became less am-
bivalent and had more trust in the vaccine These
results are in accordance with our finding that
girls who had to decide with their parents whether
or not to be vaccinated in 2011 were more likely
to be vaccinated than those who had to decide
in 2010
An important finding is that knowledge about the
duration of protection was low at both baseline and
follow-up For instance about 65 of the parents
thought that protection lasts 30 years or even life-
long As the duration of protection is still unknown
it is important that parents and girls know that
booster vaccinations might be needed in the future
When we applied a cut-off of four or five correct
knowledge items (out of seven) then the rates
of informed choice about uptake were not high
66 and 44 respectively However this finding
should be interpreted with caution because the
time period between the assessment of knowledge
and the last vaccination out of three shots was
1 month (decision in 2011) or 14 months (decision
in 2010) In educational material it should be clearly
stated what is known and not yet known about HPV
vaccination
Study strengths include the longitudinal design
as recommended by authors of a cross-sectional
study [40] the high (absolute) number of respond-
ents of the baseline (nfrac14 1725) and follow-up ques-
tionnaires (nfrac14 793) and the high response rate of the
follow-up questionnaire (74)
Limitations
A limitation was the low response rate of the base-
line questionnaire (30) which might be due to the
length of the questionnaire Our sample may there-
fore not be representative of the general population
as few parents had a low educational level Also
demographic characteristics of the follow-up group
were slightly different from those of the baseline
group with more parents being better educated
and well-off at follow-up These parents might pos-
sibly be more likely than those in the wider popula-
tion to seek to reduce high ambivalence by
searching information allowing them to respond
positively to the vaccine invitationmdashrather than do
nothing
Conclusion
In conclusion this study shows that intention a later
versus earlier decision about uptake and anticipated
regretworry about abstaining from vaccination
were predictors of uptake Anticipated regret was a
common predictor of intention and uptake and thus
an important factor in the decision-making process
about HPV vaccination In turn predictors of inten-
tion like social norm and trust in the vaccine are
also important when deciding about HPV vaccin-
ation Over time parents felt better informed
became less ambivalent and had more trust in the
vaccine
Practice implications
This study shows the usefulness of including affect-
ive factors in studies examining HPV vaccination
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nloaded from
behavior as anticipated regret trust in the vaccine
and ambivalence were found to play a role in the
decision making about uptake However it is also
important that parents are enabled to base their
decision about HPV vaccination of their daughter
on decision relevant knowledge As these results
suggest that people need sufficient time to decide
about the uptake of a new vaccine we recommend
a well-balanced stepwise process of implementa-
tion that is let parents first become aware of the
link between HPV and cervical cancer then provide
them with balanced information about all the
knowns and also the unknowns of HPV vaccination
and then finally offer them the opportunity to have
their daughter vaccinated As two-third of parents
wrongly thought that protection lasts 30 years or
even lifelong educational material should clearly
state that booster vaccinations might be needed in
the future
Acknowledgements
The authors thank the Dutch Cancer Society for
financial support and the participants for their
contribution to the study
Funding
The Dutch Cancer Society [EMCR 2008-3992
EMCR 2009-4561]
Conflict of interest statement
None declared
References
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2 Bosch FX Lorincz A Munoz N et al The causal relationbetween human papillomavirus and cervical cancer J ClinPathol 2002 55 244ndash65
3 Walboomers JM Jacobs MV Manos MM et al Humanpapillomavirus is a necessary cause of invasive cervicalcancer worldwide J Pathol 1999 189 12ndash9
4 Munoz N Bosch FX Castellsague X et al Against whichhuman papillomavirus types shall we vaccinate and screenThe international perspective Int J Cancer 2004 111278ndash85
5 Koutsky LA Holmes KK Critchlow CW et al A cohortstudy of the risk of cervical intraepithelial neoplasia grade2 or 3 in relation to papillomavirus infection N Engl J Med1992 327 1272ndash8
6 Woodman CB Collins S Winter H et al Natural history ofcervical human papillomavirus infection in young women alongitudinal cohort study Lancet 2001 357 1831ndash6
7 Boot HJ Wallenburg I de Melker HE et al Assessing theintroduction of universal human papillomavirus vaccinationfor preadolescent girls in The Netherlands Vaccine 2007 256245ndash56
8 van Lier EA Oomen PJ Oostenbrug MWM et alImmunization coverage National ImmunizationProgramme in the Netherlands Year of report 2009[Vaccinatiegraad Rijksvaccinatieprogramma NederlandVerslagjaar 2009] Bilthoven RIVM 2009
9 Zwakhals SLN van Lier EA van HPV (cohort 1997) bymunicipality 2012 [HPV (cohort 1997) per gemeente2012] In Dutch National Atlas of Public HealthBilthoven RIVM 2012 (httpwwwzorgatlasnlpreventievaccinaties-en-screeninghpv-cohort-1997-vaccinatiegraad-per-gemeente-2012 accessed 2 September 2013)
10 Brabin L Roberts SA Stretch R et al A survey of adolescentexperiences of human papillomavirus vaccination in theManchester study Br J cancer 2009 101 1502ndash4
11 Brabin L Roberts SA Kitchener HC A semi-qualitativestudy of attitudes to vaccinating adolescents against humanpapillomavirus without parental consent BMC PublicHealth 2007 7 20
12 Brewer NT Fazekas KI Predictors of HPV vaccine accept-ability A theory-informed systematic review Prev Med2007 45 107ndash14
13 Kahn JA Rosenthal SL Jin Y et al Rates of human papillo-mavirus vaccination attitudes about vaccination and humanpapillomavirus prevalence in young women Obstet Gynecol2008 111 1103ndash10
14 Askelson NM Campo S Lowe JB et al Using the theoryof planned behavior to predict mothersrsquo intentions to vaccin-ate their daughters against HPV J Sch Nurs 2010 26194ndash202
15 Ajzen I The theory of Planned Behavior Organ Behav HumDecis Process 1991 50 179ndash211
16 Becker MH The health belief model and personal healthbehavior Health Edu Monogr 1974 2 324ndash508
17 Chapman GB Coups EJ Emotions and preventive healthbehavior worry regret and influenza vaccination HealthPsychol 2006 25 82ndash90
18 Paulussen TG Hoekstra F Lanting CI et al Determinants ofDutch parentsrsquo decisions to vaccinate their child Vaccine2006 24 644ndash51
19 Kaplan KJ On the ambivalence-indifference problem inattitude theory and measurement A suggested modificationof the semantic differential technique Psychol Bull 1972 77361ndash372
20 Dormandy E Hankins M Marteau TM Attitudes and uptakeof a screening test The moderating role of ambivalencePsychol Health 2006 21 499ndash511
Predictors of HPV vaccination uptake
95
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
21 Hofman R van Empelen P Vogel I et al Parental decisionalstrategies regarding HPV vaccination prior to media debatesa focus-group study J Health Commun 2013 18 866ndash80
22 Brewer NT Gottlieb SL Reiter PL et al Longitudinal pre-dictors of human papillomavirus vaccine initiation amongadolescent girls in a high-risk geographic area Sex TransmDis 2011 38 197ndash204
23 Marlow LA Waller J Wardle J Trust and experience aspredictors of HPV vaccine acceptance Hum Vaccin 20073 171ndash5
24 Weinstein ND Perceived probability perceived severityand health-protective behavior Health Psychol 2000 1965ndash74
25 Marteau TM Dormandy E Michie S A measure of informedchoice Health Expect 2001 4 99ndash108
26 van den Berg M Timmermans DR Ten Kate LP et al Arepregnant women making informed choices about prenatalscreening Genet Med 2005 7 332ndash8
27 Tiro JA Diamond PM Perz CA et al Validation of scalesmeasuring attitudes and norms related to mammographyscreening in women veterans Health Psychol 2005 24555ndash66
28 Marlow LAV Waller J Wardle J Parental attitudes to pre-pubertal HPV vaccination Vaccine 2007 25 1945ndash52
29 Stalmeier PF Roosmalen MS Verhoef LC et al Thedecision evaluation scales Patient Educ Couns 2005 57286ndash93
30 Gilbert LA Hanson GR Perceptions of parental role respon-sibilities among working people Development of a compre-hensive measure J Marriage Fam 1983 45 203ndash12
31 Korfage IJ van Ballegooijen M Wauben B et al Informedchoice on Pap smear still limited by lack of knowledge on the
meaning of false-positive or false-negative test resultsPatient Educ Couns 2011 85 214ndash8
32 Thompson MM Zanna MP The conflicted individual per-sonality-based and domain specific antecedents of ambiva-lent social attitudes J Pers 1995 63 259ndash88
33 General Medical Council Seeking Patientsrsquo Consent TheEthical Considerations London GMC 1998
34 Minister of Health Letter about screening [Kaderbriefscreening] PGZP 2848440 Ministry of Health Welfareand Sports The Hague 2008
35 Aiken LS West RR Multiple Regression Testing andInterpreting Interactions Newbury Park CA Sage 1991
36 Krawczyk AL Perez S Lau E et al Human papillomavirusvaccination intentions and uptake in college women HealthPsychol 2012 31 685ndash93
37 Newby-Clark IR McGregor I Zanna MP Thinking andcaring about cognitive inconsistency when and for whomdoes attitudinal ambivalence feel uncomfortable J Pers SocPsychol 2002 82 157ndash66
38 Nordgren LF van Harreveld F van der Pligt J Ambivalencediscomfort and motivated information processing J ExperSoc Psychol 2006 42 252ndash8
39 Clark JK Wegener DT Fabrigar LR Attitudinal ambiva-lence and message-based persuasion motivated processingof proattitudinal information and avoidance of counterattitu-dinal information Pers Soc Psychol Bull 2008 34 565ndash77
40 van Keulen HM Otten W Ruiter RA et al Determinants ofHPV vaccination intentions among Dutch girls and theirmothers a cross-sectional study BMC Public Health 201313 111
R Hofman et al
96
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Reasons for vaccinating Parentsrsquo reasons to
have or not to have their daughter vaccinated were
assessed using 11 pre-defined items for lsquovacci-
natingrsquo 17 items for lsquonot vaccinatingrsquo and an
option to write down additional reasons
Parental characteristics We assessed sex
marital status educational level job status ethnicity
and religion of the parents Female respondents were
asked about their perceived risk of getting cervical
cancer themselves (11-point Likert scale) (adapted
from Marlow et al [24]) and if they had ever had an
abnormal Pap smear result
Follow-up questionnaire
In the follow-up questionnaire we again assessed
knowledge attitude toward HPV vaccination deci-
sional evaluation social norms (without compliance
items because compliance will logically not change
over time) ambivalence risk perception and sever-
ity and trust In addition vaccination uptake was
assessed
An informed choice to participate or not [33 34]
ie a choice based on relevant knowledge consistent
with the decision makerrsquos values and behaviorally
implemented [25] was calculated using knowledge
(at follow-up) attitude (at baseline) and uptake As
there is no standard cut-off to measure sufficient
decision relevant knowledge we presented rates of
informed decisions for 3 4 5 and 6 correct items
(out of 7) As an example results with the cut-off
level of five correct items are fully displayed An
informed choice to have onersquos daughter vaccinated
is characterized by sufficient decision relevant
knowledge a positive attitude toward HPV vaccin-
ation (score gt3) and having onersquos daughter vacci-
nated An informed choice not to have onersquos
daughter vaccinated is characterized by sufficient
decision relevant knowledge a negative attitude to-
ward HPV vaccination (score lt3) and not having
onersquos daughter vaccinated An attitude score of
3 was defined as neutral
Data analyses
The significance of mean and frequency differences
between the baseline and follow-up group was
assessed with the MannndashWhitney U-test and V2 stat-
istics Pearson correlations were calculated to ana-
lyze associations between parent characteristics and
social cognitive factors To determine significant
predictors of uptake (yesno) measured at follow-
up (T2) multiple hierarchical logistic regression
analyses were performed with various factors
measured at baseline as independent variables In
Model 1 demographic characteristics were entered
because these were considered more distal and non-
modifiable predictors In Model 2a parent charac-
teristics were added Model 2b consisted of demo-
graphic characteristics and social cognitive factors
In Model 3 we entered demographic characteristics
parent characteristics social cognitive factors and
an interaction term of attitude ambivalence
Finally in Model 4 intention was added Intention
was added only in the last model because of its high
correlation with other predictors We aimed to show
significant predictors with and without intention in
the model The procedure recommended by Aiken
and West [35] was used to determine whether
ambivalence moderated the relationship between at-
titude and uptake and the unstandardized regression
coefficients were examined for attitude at different
levels of ambivalence (ie the mean ambivalence
score 1 SD above the mean and 1 SD below the
mean) [35] To compare predictors of uptake and
intention the regression analysis of Model 3 was
repeated with intention as the dependent variable
(ordinal logistic regression analyses)
To assess the impact of the time gap between
baseline and follow-up on changes in attitude and
ambivalence two linear regression analyses were
performed with change scores between the baseline
and follow-up measurement Variables that showed
a significant (Plt 005) change over time were
included First we used attitude as the dependent
variable Independent variables were knowledge in-
formed choice (subscale of the Decision Evaluation
Scales [29]) ambivalence toward HPV vaccination
social norm and trust in the vaccine Second we
used ambivalence toward HPV vaccination as the
dependent variable Independent variables were
knowledge informed choice social norm and trust
in the vaccine
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McNemarrsquos test was used to assess the signifi-
cance of the difference in correct responses to the
knowledge items between baseline and follow-up
Results
Respondents
The response rate of the baseline questionnaire was
298 (17625918) A total of 1067 respondents
were willing to complete the follow-up question-
naire of which 793 responded (743) (Fig 1)
At baseline the mean age of those who completed
both questionnaires was 43 years Most respondents
were female (baseline 933 follow-up 937)
had an intermediate (baseline 479 follow-
up 467) or high educational level (baseline
40 follow-up 450) and were born in the
Netherlands (baseline 910 follow-up 938)
In the follow-up group 652 (822) daughters
had been vaccinated against HPV The subgroup
that completed the follow-up assessment differed
significantly from those who did not on six charac-
teristics (Table I)
5918 questionnaires were distributed among parents with a daughter aged 10-11years not yet invited for vaccination (June 2009)
37 not eligible- 31 daughters already had HPV vaccination- 4 completed only 1 or 2 questions- 2 daughters completed the questionnaire
1725 questionnaires were eligible baseline measurement
Those willing to complete the follow-up questionnaire were sent a questionnaire n=1067 (Nov 2011)
7931067 (743) questionnaires completed at follow-up
274 questionnaires not returned
4156 were not returned
1762 (298) questionnaires werereturned
658 were not willing to complete the follow-up questionnaire
Bas
elin
eF
ollo
w-u
p
Fig 1 Flow diagram of numbers of questionnaires at baseline and at follow-up
Predictors of HPV vaccination uptake
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Table I Characteristics of the respondents (parents)
Total baseline
group (nfrac14 1725)
Subgroup that completed
follow-up assessment (nfrac14 793)
Characteristics Mean (SD) Mean (SD) P-value
Age at baseline (years) 428 (417) 430 (405) 0015
range 29ndash59 32ndash58
Children
Age (years) 133 (342) 133 (321)
Age range 0ndash34 0ndash34
Number of girls 17 (078) 17 (074)
Number of boys 09 (077) 09 (076)
n () n ()
Marital status 0372
Marriedcohabiting 1477 (872) 693 (894)
Partner but living alone 34 (20) 16 (21)
No partner 165 (97) 66 (85)
Sex 0233
Female 1596 (933) 743 (937)
Educational level lt0001
Low 200 (121) 64 (83)
Intermediate 789 (479) 358 (467)
High 658 (400) 345 (450)
Job status 0270
Paid job 1268 (786) 617 (816)
Housewife or houseman or unpaid job or student 295 (183) 119 (157)
No job 51 (32) 20 (26)
Net income per month (euros) lt0001
lt1500 161 (105) 45 (61)
1500ndash3000 584 (382) 267 (364)
3000ndash4500 488 (320) 264 (360)
gt4500 294 (193) 157 (214)
Country of birth lt0001
The Netherlands 1550 (910) 740 (938)
Turkey Morocco 37 (22) 6 (08)
Suriname Aruba Netherlands Antilles 16 (09) 4 (05)
Other 100 (59) 39 (49)
Country of birth of both parents 0002
The Netherlands 1459 (885) 703 (894)
Turkey Morocco 44 (27) 9 (11)
Suriname Aruba Netherlands Antilles 19 (12) 5 (06)
Other 126 (76) 69 (88)
Religion 0590
None 960 (570) 450 (579)
Christian 611 (363) 290 (373)
Muslim 57 (34) 13 (17)
Other 54 (32) 24 (31)
Decision about HPV vaccination uptake
In 2010 - 555 (715)
In 2011 - 221 (285)
(continued)
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Predictors of HPV vaccination uptake
Pearsonrsquos correlations showed that most associ-
ations between the predictors were positive
(Table II) Table III presents the results of the hier-
archical logistic regression analyses to predict
HPV vaccination uptake The first model in which
HPV vaccination uptake was regressed on demo-
graphic factors showed that uptake at follow-up
was significantly predicted by religion and the
year the decision about uptake was made (2011
versus 2010) (pseudo R2frac14 006) Specifically
those respondents without a religious affiliation
and those who had to decide in 2011 were more
likely to have their daughter vaccinated In Model
2a parent characteristics were added this model
explained an additional 29 variance HPV vaccin-
ation was more likely for parents with a higher edu-
cational level having no religious affiliation
decision about uptake in 2011 and higher trust in
the NIP and the vaccine In Model 2b (demographic
characteristics and social cognitive factors) signifi-
cant predictors were year of decision about uptake
(2011 versus 2010) a positive attitude toward HPV
vaccination social norm and anticipated regret and
worry about no uptake (pseudo R2frac14 053) In Model
3 (including all predictors except intention) vaccin-
ation was more likely for parents who had to decide
in 2011 ambivalence toward HPV vaccination
(under the condition that attitude is equal to 0) and
higher anticipated regret and worry about no uptake
The interaction term of attitude ambivalence was
also significant (pseudo R2frac14 057) In Model 4
(including all predictors) significant predictors of
uptake were the year the decision about uptake
was made (2011 versus 2010) a higher intention
ambivalence toward HPV vaccination (under the
condition that attitude is equal to 0) and the inter-
action term of attitude ambivalence
The significant interaction term attitude am-
bivalence showed that the predictive validity of at-
titude improved as scores of ambivalence increased
from low (bfrac14 089 Pfrac14 00238) to moderate
(bfrac14 144 Pfrac14 0001) and from moderate
(bfrac14 144 Pfrac14 0001) to high (bfrac14 198 Plt 0001)
Associations of HPV vaccination intention
Alternatively we performed an ordinal logistic re-
gression analysis with intention (instead of uptake)
as dependent variable (data not shown) This ana-
lysis showed that a higher intention was associated
with a positive attitude toward HPV vaccination
[odds ratio (OR) 1953 95 confidence interval
(CI) 1032ndash3693] (under the condition that am-
bivalence is frac140) ambivalence toward HPV vaccin-
ation (OR 239 95 CI 110ndash518) (under the
condition that attitude is frac140) trust in the vaccine
(OR 162 95 CI 116ndash227) anticipated regret
and worry about no uptake (OR 159 95 CI
Table I Continued
Total baseline
group (nfrac14 1725)
Subgroup that completed
follow-up assessment (nfrac14 793)
Characteristics Mean (SD) Mean (SD) P-value
If female abnormal Pap smear result 0103
Yes 185 (117) 98 (132)
No 1351 (856) 634 (853)
Never had a Pap smear taken 42 (27) 11 (15)
Daughter vaccinated against DPTPa and MMRb 0038
Yes 1654 (959) 778 (981)
Daughter vaccinated against HPV
Yes - 652 (831)
The subgroup that completed the follow-up assessment differed significantly from the baseline group on six characteristicsaDPTP refers to diphtheria pertussis tetanus and poliomyelitisbMMR refers to measles mumps and rubella
Predictors of HPV vaccination uptake
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Tab
leII
M
eans
standard
dev
iati
ons
(SD
)and
Pea
rsonrsquos
corr
elati
on
bet
wee
nth
epre
dic
tors
at
base
line
(nfrac14
793)
Mea
n(S
D)
12
34
56
78
910
11
12
1
Par
enta
lre
sponsi
bil
ity
45
0(0
46)
2
Tru
stin
NIP
48
6(0
67)
00
4
3
Tru
stin
vac
cine
43
1(0
92)
00
605
4
4
Per
ceiv
edsu
scep
tibil
ity
of
moth
erto
cerv
ical
cance
r
49
7(1
74)
00
500
100
2
5
Inte
nti
on
38
9(1
07)
00
304
8
07
3
00
5
6
Am
biv
alen
ce17
1(1
07)
00
7
02
0
02
6
00
1
02
9
7
Att
itude
tow
ard
HP
V
vac
cinat
ion
37
3(1
44)
00
9
05
1
07
7
00
508
4
03
3
8
Soci
alnorm
61
0(1
03
1)
01
5
03
3
05
1
00
706
1
01
8
06
4
9
Norm
ativ
ebel
ief
71
2(1
57)
00
501
9
03
3
00
103
3
00
9
03
4
03
7
10
Know
ledge
43
2(1
49)
00
9
01
0
00
300
300
3
00
700
200
3
00
3
11
Per
ceiv
edsu
scep
tibil
ity
of
dau
ghte
rif
vac
cinat
ed
toce
rvic
alca
nce
r
37
3(1
44)
00
6
02
3
03
0
04
1
02
6
00
3
03
1
02
3
02
3
00
1
12
Per
ceiv
edse
ver
ity
of
cerv
ical
cance
r
106
0(0
93)
02
5
00
400
500
300
500
400
600
700
9
01
2
00
1
13
Anti
cipat
edre
gre
tan
d
worr
yab
out
no
upta
ke
49
2(1
56)
02
3
03
8
06
2
01
1
06
9
01
9
07
1
05
3
03
6
00
6
02
3
02
0
Sm
all
effe
ctsi
ze
rgt
01
0
med
ium
effe
ctsi
ze
03
0lt
rlt
05
0
larg
eef
fect
size
rgt
05
0
Plt
00
5
Plt
00
1
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Tab
leII
IH
iera
rchic
al
logis
tic
regre
ssio
nanaly
ses
wit
hupta
ke(y
esn
o)
as
dep
enden
tva
riable
all
vari
able
sare
report
edby
pare
nts
at
base
line
Univ
aria
te
Model
1
(nfrac14
708)
Model
2a
(nfrac14
644)
Model
2b
(nfrac14
617)
Model
3
(nfrac14
572)
Model
4
(nfrac14
569)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
Dem
ogra
ph
icch
ara
cter
isti
cs
Age
of
par
ents
(yea
rs)
10
2(0
98ndash10
7)
10
1(0
96ndash10
6)
10
3(0
96ndash10
9)
10
2(0
95ndash11
0)
10
2(0
94ndash11
1)
10
1(0
93ndash10
9)
Educa
tional
level
11
5(1
00ndash13
4)
11
7(0
99ndash13
7)
12
5(1
00ndash15
4)
12
0(0
93ndash15
5)
12
7(0
96ndash17
0)
13
3(0
99ndash17
8)
No
reli
gio
us
affi
liat
ion
17
3(1
19ndash25
3)
16
3(1
09ndash24
2)
17
3(1
07ndash28
1)
11
2(0
63ndash20
0)
11
9(0
63ndash22
5)
11
6(0
60ndash22
3)
Dec
isio
nab
out
upta
ke
2011
(vs
2010)
20
8(1
28ndash33
6)
26
8(1
57ndash45
3)
26
9(1
42ndash51
0)
24
5(1
20ndash50
1)
24
8(1
11ndash55
2)
26
0(1
16ndash58
0)
Pare
nt
chara
cter
isti
cs
No
abnorm
alsm
ear
exper
ience
10
2(0
58ndash17
8)
09
4(0
45ndash19
5)
07
0(0
26ndash18
8)
06
8(0
24ndash19
5)
Par
enta
lre
sponsi
bil
ity
12
3(0
83ndash18
4)
15
3(0
91ndash25
9)
15
5(0
76ndash31
8)
18
6(0
90ndash38
3)
Tru
stin
NIP
35
4(2
61ndash48
1)
18
2(1
21ndash27
4)
14
0(0
86ndash23
0)
13
3(0
79ndash22
4)
Tru
stin
vac
cine
36
4(2
85ndash46
4)
34
1(2
49ndash46
8)
12
3(0
69ndash18
3)
09
9(0
59ndash16
7)
Per
ceiv
edsu
scep
tibil
ity
of
moth
erto
cerv
ical
cance
r
10
4(0
93ndash11
6)
10
3(0
88ndash12
1)
09
7(0
77ndash12
2)
09
6(0
76ndash12
2)
Soci
al
cogn
itiv
efa
ctors
Inte
nti
on
45
9(3
56ndash59
2)
26
1(1
47ndash46
1)
Am
biv
alen
ceto
war
dH
PV
vac
cinat
ion
08
2(0
69ndash09
2)
10
7(0
79ndash14
5)
02
7(0
08ndash08
7)
02
2(0
07ndash07
1)
Posi
tive
atti
tude
tow
ard
HP
Vvac
cinat
ion
57
3(4
26ndash77
1)
34
3(2
01ndash58
4)
17
0(0
69ndash42
1)
08
9(0
34ndash23
6)
Soci
alnorm
12
1(1
16ndash12
6)
10
7(1
01ndash11
3)
10
5(0
99ndash11
1)
10
3(0
97ndash10
9)
Norm
ativ
ebel
ief
14
4(1
28ndash16
3)
09
9(0
81ndash12
1)
10
3(0
83ndash12
9)
10
3(0
81ndash12
9)
Know
ledge
10
8(0
95ndash12
2)
09
5(0
87ndash10
4)
09
3(0
76ndash11
3)
09
5(0
78ndash11
7)
Per
ceiv
edsu
scep
tibil
ity
of
dau
ghte
rif
vac
cinat
ed
toce
rvic
alca
nce
r
06
5(0
57ndash07
4)
08
6(0
70ndash10
5)
08
9(0
69ndash11
4)
08
8(0
68ndash11
4)
Per
ceiv
edse
ver
ity
of
cerv
ical
cance
r
12
2(1
03ndash14
6)
10
8(0
81ndash14
2)
10
6(0
78ndash14
4)
10
8(0
79ndash14
8)
Anti
cipat
edre
gre
tan
d
worr
yab
out
no
upta
ke
22
3(1
93ndash25
8)
14
3(1
11ndash18
4)
14
3(1
08ndash18
9)
12
4(0
92ndash16
7)
Am
biv
alen
ce
atti
tude
inte
ract
ion
16
8(1
14ndash24
7)
17
9(1
22ndash26
2)
R2
00
603
505
305
705
9
Plt
00
5Plt
00
1an
dPlt
00
01
Predictors of HPV vaccination uptake
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132ndash192) and social norm (OR 107 95 CI
104ndash110) A lower uptake intention was asso-
ciated with a higher educational level (OR 083
95 CI 070ndash099) and a higher perceived parental
responsibility for their daughterrsquos health (OR 048
95 CI 030ndash075) The interaction term of atti-
tude ambivalence was significant (OR 073
95 CI 059ndash090)
Impact of time
Favorable changes in attitudes toward HPV uptake
over time were significantly related to an increase in
trust in the vaccine (OR 145 95 CI 136ndash153)
and social norm (OR 122 95 CI 115ndash128) over
time and a decrease in ambivalence toward HPV
vaccination (OR 094 95 CI 091ndash098) A de-
crease in ambivalence toward HPV vaccination
over time was significantly related to an increase
in feeling informed about HPV vaccination (OR
079 95 CI 069ndash091) and an increase in trust
in the vaccine (OR 088 95 CI 077ndash099) over
time
Informed decision making
Overall knowledge levels about the degreeduration
of protection were low at baseline and at follow-up
(33ndash43 correct answers) Percentages of correct
responses to five knowledge items increased signifi-
cantly at follow-up (Table IV) When five (out of
seven) correct items were defined as sufficient deci-
sion relevant knowledge then nfrac14 338 (439) of
the respondents made an informed choice about
uptake When four correct items were considered
sufficient then nfrac14 437 (657) of the respondents
made an informed choice about uptake (Table V)
Reasons for vaccinating or not
Main reasons as reported by parents at baseline to
have their daughter vaccinated include feeling re-
sponsible for her health (nfrac14 947 549) a family
history of cancer (nfrac14 128 74) anticipating
regret in case their daughter gets cervical cancer
(nfrac14 103 60) and other (nfrac14 547 317) Main
reasons as reported by parents at baseline not to have
their daughter vaccinated include that consequences
Table IV Knowledge items as completed by those who responded to the baseline and follow-up questionnaire (nfrac14 793)
Correct responses
Baseline
measurement
Follow-up
measurement
Significance level for
difference between
baseline and follow-up
n () n () P-value
Item (truefalse)
HPV causes cervical cancer (true) 496 (625) 479 (604) 0336
A condom protects 100 against HPV (false) 464 (585) 518 (653) 0001
The HPV vaccination will decrease the risk of cervical
cancer (true)
673 (849) 726 (916) lt0001
Vaccination in combination with having a smear taken is
more protective than only vaccination (true)
521 (657) 598 (754) lt0001
Item (multiple choice)
How is HPV transmitted (through blood oxygen sexual
contact)
699 (881) 730 (921) 0006
What is the protection rate of the HPV vaccine (55 70
85 100)
286 (361) 337 (425) 0005
What is the protection duration of a complete vaccination
against cervical cancer (at least 6 (8 at follow-up) years
at least 30 years lifetime)
289 (364) 262 (330) 0094
Correct answers are shaded
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nloaded from
of vaccinating are unpredictable (497 288) fear
of serious side-effects (nfrac14 401 232) and too
little information about the vaccine being available
(nfrac14 125 72)
Discussion
In this study among parents we assessed longitu-
dinal predictors of HPV vaccination uptake of their
daughters Uptake was predicted by intention a later
(2011) versus earlier (2010) decision about uptake
and anticipated regret and worry in case of abstain-
ing from HPV vaccination Ambivalence toward
HPV vaccination at baseline moderated the attitude
(baseline) uptake (follow-up) relationship with the
attitudendashuptake relationship being stronger at higher
ambivalence levels
HPV vaccination was most strongly predicted by
intention which fits the TPB model and was also
reported in an earlier study on predictors of HPV
vaccination uptake [22] In turn HPV vaccination
intention was positively associated with educational
level perceived parental responsibility for onersquos
daughterrsquos health trust in the vaccine the belief
that according to significant others their daughter
should be vaccinated and the motivation to comply
with that (social norm) and anticipated regret and
worry (which also predicted uptake) The relation-
ship found between intention and uptake and
between intention and social norm is consistent
with the TPB model and with another study [22]
which also confirms the association we found
between anticipated regretworry and uptake and
anticipated regretworry and intention The factors
lsquoperceived susceptibilityrsquo and lsquoseverityrsquo of cancer
of the HBM were not associated with intention or
uptake which confirms the results of an earlier study
[22 36]
A possible explanation for the positive effect on
uptake of having to decide later (2011) versus earlier
(2010) might be the amount of time that passed be-
tween the baseline questionnaire (2009) when an
intensive societal debate involving politics phys-
icians media parents and girls about HPV vaccin-
ation was ongoing and the actual decision about
uptake of vaccination In 2011 this debate probably
had less impact on the uptake decision than in 2010
Also after millions of girls worldwide had been
vaccinated and no serious side-effects had been
reported parents who had to decide later versus
earlier probably felt more reassured about the
vaccinersquos safety
This study shows that ambivalence moderated the
attitudendashuptake relationship Parents with a positive
attitude and a high level of ambivalence toward
HPV vaccination were more likely to have their
daughter vaccinated than parents with a positive at-
titude and a low level of ambivalence This finding
might be explained in two ways First ambivalence
is characterized as being subjectively uncomfortable
and people may be motivated to resolve the conflict-
ing evaluations that they hold [37] for example
by searching for information Second earlier
studies found that ambivalent people processed
pro-attitudinal messages to a greater extent than
counter-attitudinal messages probably because
pro-attitudinal messages are more likely to reduce
ambivalence [38 39] Taking these two mechanisms
together it is likely that in our study ambivalent
parents with a positive attitude toward HPV vaccin-
ation processed lsquopositiversquo messages about HPV vac-
cination to a greater extent than lsquonegativersquo messages
and were therefore more likely to have their
Table V Informed decision at follow-up (nfrac14 770)
Daughter
vaccinated
(nfrac14 640)
Daughter not
vaccinated
(nfrac14 130)
n () n ()
Positive attitude
Five or more correct items 280 (364) 14 (18)
Less than five correct items 246 (319) 16 (21)
Negative attitude
Five or more correct items 51 (66) 58 (75)
Less than five correct items 32 (42) 34 (44)
Knowledge was measured with seven items at follow-upInformed decision rate for cut-off at three correct items761 [(504 + 82)770] four correct items 657[(437 + 69)770] five correct items 439 [(280 + 58)770]six correct items 187 [(117 + 27)770] Due to missingitems analyses were based on nfrac14 770 respondents instead ofnfrac14 793 Informed choice (as defined) is shaded
Predictors of HPV vaccination uptake
93
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Dow
nloaded from
daughter vaccinated In other words parents who
had both positive attitudes and were ambivalent to-
ward HPV vaccination became even more positive
because they elaborated only information in favor of
HPV vaccination This may imply that this lsquobiasedrsquo
information processing has a negative impact on
informed decision making although parents will
have gained more knowledge during their efforts
to resolve their ambivalence
Assessing decisional factors related to HPV vac-
cination both before and after the decision-making
process about uptake provided a unique opportun-
ity to determine changes in those factors over time
As uptake was predicted by intention and intention
was highly correlated with attitude (rfrac14 084) (at
baseline) we think it is relevant to show which
factors are important for changes in attitude over
time Our results show that a more positive attitude
toward HPV vaccination over time was associated
with an increase in trust in the vaccine and in
social norm over time and a decrease in ambiva-
lence toward HPV vaccination over time This
latter factor was related to an increase in feeling
informed about HPV vaccination and an increase
in trust in the vaccine over time In summary over
time parents felt better informed became less am-
bivalent and had more trust in the vaccine These
results are in accordance with our finding that
girls who had to decide with their parents whether
or not to be vaccinated in 2011 were more likely
to be vaccinated than those who had to decide
in 2010
An important finding is that knowledge about the
duration of protection was low at both baseline and
follow-up For instance about 65 of the parents
thought that protection lasts 30 years or even life-
long As the duration of protection is still unknown
it is important that parents and girls know that
booster vaccinations might be needed in the future
When we applied a cut-off of four or five correct
knowledge items (out of seven) then the rates
of informed choice about uptake were not high
66 and 44 respectively However this finding
should be interpreted with caution because the
time period between the assessment of knowledge
and the last vaccination out of three shots was
1 month (decision in 2011) or 14 months (decision
in 2010) In educational material it should be clearly
stated what is known and not yet known about HPV
vaccination
Study strengths include the longitudinal design
as recommended by authors of a cross-sectional
study [40] the high (absolute) number of respond-
ents of the baseline (nfrac14 1725) and follow-up ques-
tionnaires (nfrac14 793) and the high response rate of the
follow-up questionnaire (74)
Limitations
A limitation was the low response rate of the base-
line questionnaire (30) which might be due to the
length of the questionnaire Our sample may there-
fore not be representative of the general population
as few parents had a low educational level Also
demographic characteristics of the follow-up group
were slightly different from those of the baseline
group with more parents being better educated
and well-off at follow-up These parents might pos-
sibly be more likely than those in the wider popula-
tion to seek to reduce high ambivalence by
searching information allowing them to respond
positively to the vaccine invitationmdashrather than do
nothing
Conclusion
In conclusion this study shows that intention a later
versus earlier decision about uptake and anticipated
regretworry about abstaining from vaccination
were predictors of uptake Anticipated regret was a
common predictor of intention and uptake and thus
an important factor in the decision-making process
about HPV vaccination In turn predictors of inten-
tion like social norm and trust in the vaccine are
also important when deciding about HPV vaccin-
ation Over time parents felt better informed
became less ambivalent and had more trust in the
vaccine
Practice implications
This study shows the usefulness of including affect-
ive factors in studies examining HPV vaccination
R Hofman et al
94
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Dow
nloaded from
behavior as anticipated regret trust in the vaccine
and ambivalence were found to play a role in the
decision making about uptake However it is also
important that parents are enabled to base their
decision about HPV vaccination of their daughter
on decision relevant knowledge As these results
suggest that people need sufficient time to decide
about the uptake of a new vaccine we recommend
a well-balanced stepwise process of implementa-
tion that is let parents first become aware of the
link between HPV and cervical cancer then provide
them with balanced information about all the
knowns and also the unknowns of HPV vaccination
and then finally offer them the opportunity to have
their daughter vaccinated As two-third of parents
wrongly thought that protection lasts 30 years or
even lifelong educational material should clearly
state that booster vaccinations might be needed in
the future
Acknowledgements
The authors thank the Dutch Cancer Society for
financial support and the participants for their
contribution to the study
Funding
The Dutch Cancer Society [EMCR 2008-3992
EMCR 2009-4561]
Conflict of interest statement
None declared
References
1 Karim-Kos HE de Vries E Soerjomataram I et al Recenttrends of cancer in Europe a combined approach of inci-dence survival and mortality for 17 cancer sites since the1990s Eur J Cancer 2008 44 1345ndash89
2 Bosch FX Lorincz A Munoz N et al The causal relationbetween human papillomavirus and cervical cancer J ClinPathol 2002 55 244ndash65
3 Walboomers JM Jacobs MV Manos MM et al Humanpapillomavirus is a necessary cause of invasive cervicalcancer worldwide J Pathol 1999 189 12ndash9
4 Munoz N Bosch FX Castellsague X et al Against whichhuman papillomavirus types shall we vaccinate and screenThe international perspective Int J Cancer 2004 111278ndash85
5 Koutsky LA Holmes KK Critchlow CW et al A cohortstudy of the risk of cervical intraepithelial neoplasia grade2 or 3 in relation to papillomavirus infection N Engl J Med1992 327 1272ndash8
6 Woodman CB Collins S Winter H et al Natural history ofcervical human papillomavirus infection in young women alongitudinal cohort study Lancet 2001 357 1831ndash6
7 Boot HJ Wallenburg I de Melker HE et al Assessing theintroduction of universal human papillomavirus vaccinationfor preadolescent girls in The Netherlands Vaccine 2007 256245ndash56
8 van Lier EA Oomen PJ Oostenbrug MWM et alImmunization coverage National ImmunizationProgramme in the Netherlands Year of report 2009[Vaccinatiegraad Rijksvaccinatieprogramma NederlandVerslagjaar 2009] Bilthoven RIVM 2009
9 Zwakhals SLN van Lier EA van HPV (cohort 1997) bymunicipality 2012 [HPV (cohort 1997) per gemeente2012] In Dutch National Atlas of Public HealthBilthoven RIVM 2012 (httpwwwzorgatlasnlpreventievaccinaties-en-screeninghpv-cohort-1997-vaccinatiegraad-per-gemeente-2012 accessed 2 September 2013)
10 Brabin L Roberts SA Stretch R et al A survey of adolescentexperiences of human papillomavirus vaccination in theManchester study Br J cancer 2009 101 1502ndash4
11 Brabin L Roberts SA Kitchener HC A semi-qualitativestudy of attitudes to vaccinating adolescents against humanpapillomavirus without parental consent BMC PublicHealth 2007 7 20
12 Brewer NT Fazekas KI Predictors of HPV vaccine accept-ability A theory-informed systematic review Prev Med2007 45 107ndash14
13 Kahn JA Rosenthal SL Jin Y et al Rates of human papillo-mavirus vaccination attitudes about vaccination and humanpapillomavirus prevalence in young women Obstet Gynecol2008 111 1103ndash10
14 Askelson NM Campo S Lowe JB et al Using the theoryof planned behavior to predict mothersrsquo intentions to vaccin-ate their daughters against HPV J Sch Nurs 2010 26194ndash202
15 Ajzen I The theory of Planned Behavior Organ Behav HumDecis Process 1991 50 179ndash211
16 Becker MH The health belief model and personal healthbehavior Health Edu Monogr 1974 2 324ndash508
17 Chapman GB Coups EJ Emotions and preventive healthbehavior worry regret and influenza vaccination HealthPsychol 2006 25 82ndash90
18 Paulussen TG Hoekstra F Lanting CI et al Determinants ofDutch parentsrsquo decisions to vaccinate their child Vaccine2006 24 644ndash51
19 Kaplan KJ On the ambivalence-indifference problem inattitude theory and measurement A suggested modificationof the semantic differential technique Psychol Bull 1972 77361ndash372
20 Dormandy E Hankins M Marteau TM Attitudes and uptakeof a screening test The moderating role of ambivalencePsychol Health 2006 21 499ndash511
Predictors of HPV vaccination uptake
95
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
21 Hofman R van Empelen P Vogel I et al Parental decisionalstrategies regarding HPV vaccination prior to media debatesa focus-group study J Health Commun 2013 18 866ndash80
22 Brewer NT Gottlieb SL Reiter PL et al Longitudinal pre-dictors of human papillomavirus vaccine initiation amongadolescent girls in a high-risk geographic area Sex TransmDis 2011 38 197ndash204
23 Marlow LA Waller J Wardle J Trust and experience aspredictors of HPV vaccine acceptance Hum Vaccin 20073 171ndash5
24 Weinstein ND Perceived probability perceived severityand health-protective behavior Health Psychol 2000 1965ndash74
25 Marteau TM Dormandy E Michie S A measure of informedchoice Health Expect 2001 4 99ndash108
26 van den Berg M Timmermans DR Ten Kate LP et al Arepregnant women making informed choices about prenatalscreening Genet Med 2005 7 332ndash8
27 Tiro JA Diamond PM Perz CA et al Validation of scalesmeasuring attitudes and norms related to mammographyscreening in women veterans Health Psychol 2005 24555ndash66
28 Marlow LAV Waller J Wardle J Parental attitudes to pre-pubertal HPV vaccination Vaccine 2007 25 1945ndash52
29 Stalmeier PF Roosmalen MS Verhoef LC et al Thedecision evaluation scales Patient Educ Couns 2005 57286ndash93
30 Gilbert LA Hanson GR Perceptions of parental role respon-sibilities among working people Development of a compre-hensive measure J Marriage Fam 1983 45 203ndash12
31 Korfage IJ van Ballegooijen M Wauben B et al Informedchoice on Pap smear still limited by lack of knowledge on the
meaning of false-positive or false-negative test resultsPatient Educ Couns 2011 85 214ndash8
32 Thompson MM Zanna MP The conflicted individual per-sonality-based and domain specific antecedents of ambiva-lent social attitudes J Pers 1995 63 259ndash88
33 General Medical Council Seeking Patientsrsquo Consent TheEthical Considerations London GMC 1998
34 Minister of Health Letter about screening [Kaderbriefscreening] PGZP 2848440 Ministry of Health Welfareand Sports The Hague 2008
35 Aiken LS West RR Multiple Regression Testing andInterpreting Interactions Newbury Park CA Sage 1991
36 Krawczyk AL Perez S Lau E et al Human papillomavirusvaccination intentions and uptake in college women HealthPsychol 2012 31 685ndash93
37 Newby-Clark IR McGregor I Zanna MP Thinking andcaring about cognitive inconsistency when and for whomdoes attitudinal ambivalence feel uncomfortable J Pers SocPsychol 2002 82 157ndash66
38 Nordgren LF van Harreveld F van der Pligt J Ambivalencediscomfort and motivated information processing J ExperSoc Psychol 2006 42 252ndash8
39 Clark JK Wegener DT Fabrigar LR Attitudinal ambiva-lence and message-based persuasion motivated processingof proattitudinal information and avoidance of counterattitu-dinal information Pers Soc Psychol Bull 2008 34 565ndash77
40 van Keulen HM Otten W Ruiter RA et al Determinants ofHPV vaccination intentions among Dutch girls and theirmothers a cross-sectional study BMC Public Health 201313 111
R Hofman et al
96
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nloaded from
McNemarrsquos test was used to assess the signifi-
cance of the difference in correct responses to the
knowledge items between baseline and follow-up
Results
Respondents
The response rate of the baseline questionnaire was
298 (17625918) A total of 1067 respondents
were willing to complete the follow-up question-
naire of which 793 responded (743) (Fig 1)
At baseline the mean age of those who completed
both questionnaires was 43 years Most respondents
were female (baseline 933 follow-up 937)
had an intermediate (baseline 479 follow-
up 467) or high educational level (baseline
40 follow-up 450) and were born in the
Netherlands (baseline 910 follow-up 938)
In the follow-up group 652 (822) daughters
had been vaccinated against HPV The subgroup
that completed the follow-up assessment differed
significantly from those who did not on six charac-
teristics (Table I)
5918 questionnaires were distributed among parents with a daughter aged 10-11years not yet invited for vaccination (June 2009)
37 not eligible- 31 daughters already had HPV vaccination- 4 completed only 1 or 2 questions- 2 daughters completed the questionnaire
1725 questionnaires were eligible baseline measurement
Those willing to complete the follow-up questionnaire were sent a questionnaire n=1067 (Nov 2011)
7931067 (743) questionnaires completed at follow-up
274 questionnaires not returned
4156 were not returned
1762 (298) questionnaires werereturned
658 were not willing to complete the follow-up questionnaire
Bas
elin
eF
ollo
w-u
p
Fig 1 Flow diagram of numbers of questionnaires at baseline and at follow-up
Predictors of HPV vaccination uptake
87
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Table I Characteristics of the respondents (parents)
Total baseline
group (nfrac14 1725)
Subgroup that completed
follow-up assessment (nfrac14 793)
Characteristics Mean (SD) Mean (SD) P-value
Age at baseline (years) 428 (417) 430 (405) 0015
range 29ndash59 32ndash58
Children
Age (years) 133 (342) 133 (321)
Age range 0ndash34 0ndash34
Number of girls 17 (078) 17 (074)
Number of boys 09 (077) 09 (076)
n () n ()
Marital status 0372
Marriedcohabiting 1477 (872) 693 (894)
Partner but living alone 34 (20) 16 (21)
No partner 165 (97) 66 (85)
Sex 0233
Female 1596 (933) 743 (937)
Educational level lt0001
Low 200 (121) 64 (83)
Intermediate 789 (479) 358 (467)
High 658 (400) 345 (450)
Job status 0270
Paid job 1268 (786) 617 (816)
Housewife or houseman or unpaid job or student 295 (183) 119 (157)
No job 51 (32) 20 (26)
Net income per month (euros) lt0001
lt1500 161 (105) 45 (61)
1500ndash3000 584 (382) 267 (364)
3000ndash4500 488 (320) 264 (360)
gt4500 294 (193) 157 (214)
Country of birth lt0001
The Netherlands 1550 (910) 740 (938)
Turkey Morocco 37 (22) 6 (08)
Suriname Aruba Netherlands Antilles 16 (09) 4 (05)
Other 100 (59) 39 (49)
Country of birth of both parents 0002
The Netherlands 1459 (885) 703 (894)
Turkey Morocco 44 (27) 9 (11)
Suriname Aruba Netherlands Antilles 19 (12) 5 (06)
Other 126 (76) 69 (88)
Religion 0590
None 960 (570) 450 (579)
Christian 611 (363) 290 (373)
Muslim 57 (34) 13 (17)
Other 54 (32) 24 (31)
Decision about HPV vaccination uptake
In 2010 - 555 (715)
In 2011 - 221 (285)
(continued)
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Predictors of HPV vaccination uptake
Pearsonrsquos correlations showed that most associ-
ations between the predictors were positive
(Table II) Table III presents the results of the hier-
archical logistic regression analyses to predict
HPV vaccination uptake The first model in which
HPV vaccination uptake was regressed on demo-
graphic factors showed that uptake at follow-up
was significantly predicted by religion and the
year the decision about uptake was made (2011
versus 2010) (pseudo R2frac14 006) Specifically
those respondents without a religious affiliation
and those who had to decide in 2011 were more
likely to have their daughter vaccinated In Model
2a parent characteristics were added this model
explained an additional 29 variance HPV vaccin-
ation was more likely for parents with a higher edu-
cational level having no religious affiliation
decision about uptake in 2011 and higher trust in
the NIP and the vaccine In Model 2b (demographic
characteristics and social cognitive factors) signifi-
cant predictors were year of decision about uptake
(2011 versus 2010) a positive attitude toward HPV
vaccination social norm and anticipated regret and
worry about no uptake (pseudo R2frac14 053) In Model
3 (including all predictors except intention) vaccin-
ation was more likely for parents who had to decide
in 2011 ambivalence toward HPV vaccination
(under the condition that attitude is equal to 0) and
higher anticipated regret and worry about no uptake
The interaction term of attitude ambivalence was
also significant (pseudo R2frac14 057) In Model 4
(including all predictors) significant predictors of
uptake were the year the decision about uptake
was made (2011 versus 2010) a higher intention
ambivalence toward HPV vaccination (under the
condition that attitude is equal to 0) and the inter-
action term of attitude ambivalence
The significant interaction term attitude am-
bivalence showed that the predictive validity of at-
titude improved as scores of ambivalence increased
from low (bfrac14 089 Pfrac14 00238) to moderate
(bfrac14 144 Pfrac14 0001) and from moderate
(bfrac14 144 Pfrac14 0001) to high (bfrac14 198 Plt 0001)
Associations of HPV vaccination intention
Alternatively we performed an ordinal logistic re-
gression analysis with intention (instead of uptake)
as dependent variable (data not shown) This ana-
lysis showed that a higher intention was associated
with a positive attitude toward HPV vaccination
[odds ratio (OR) 1953 95 confidence interval
(CI) 1032ndash3693] (under the condition that am-
bivalence is frac140) ambivalence toward HPV vaccin-
ation (OR 239 95 CI 110ndash518) (under the
condition that attitude is frac140) trust in the vaccine
(OR 162 95 CI 116ndash227) anticipated regret
and worry about no uptake (OR 159 95 CI
Table I Continued
Total baseline
group (nfrac14 1725)
Subgroup that completed
follow-up assessment (nfrac14 793)
Characteristics Mean (SD) Mean (SD) P-value
If female abnormal Pap smear result 0103
Yes 185 (117) 98 (132)
No 1351 (856) 634 (853)
Never had a Pap smear taken 42 (27) 11 (15)
Daughter vaccinated against DPTPa and MMRb 0038
Yes 1654 (959) 778 (981)
Daughter vaccinated against HPV
Yes - 652 (831)
The subgroup that completed the follow-up assessment differed significantly from the baseline group on six characteristicsaDPTP refers to diphtheria pertussis tetanus and poliomyelitisbMMR refers to measles mumps and rubella
Predictors of HPV vaccination uptake
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Tab
leII
M
eans
standard
dev
iati
ons
(SD
)and
Pea
rsonrsquos
corr
elati
on
bet
wee
nth
epre
dic
tors
at
base
line
(nfrac14
793)
Mea
n(S
D)
12
34
56
78
910
11
12
1
Par
enta
lre
sponsi
bil
ity
45
0(0
46)
2
Tru
stin
NIP
48
6(0
67)
00
4
3
Tru
stin
vac
cine
43
1(0
92)
00
605
4
4
Per
ceiv
edsu
scep
tibil
ity
of
moth
erto
cerv
ical
cance
r
49
7(1
74)
00
500
100
2
5
Inte
nti
on
38
9(1
07)
00
304
8
07
3
00
5
6
Am
biv
alen
ce17
1(1
07)
00
7
02
0
02
6
00
1
02
9
7
Att
itude
tow
ard
HP
V
vac
cinat
ion
37
3(1
44)
00
9
05
1
07
7
00
508
4
03
3
8
Soci
alnorm
61
0(1
03
1)
01
5
03
3
05
1
00
706
1
01
8
06
4
9
Norm
ativ
ebel
ief
71
2(1
57)
00
501
9
03
3
00
103
3
00
9
03
4
03
7
10
Know
ledge
43
2(1
49)
00
9
01
0
00
300
300
3
00
700
200
3
00
3
11
Per
ceiv
edsu
scep
tibil
ity
of
dau
ghte
rif
vac
cinat
ed
toce
rvic
alca
nce
r
37
3(1
44)
00
6
02
3
03
0
04
1
02
6
00
3
03
1
02
3
02
3
00
1
12
Per
ceiv
edse
ver
ity
of
cerv
ical
cance
r
106
0(0
93)
02
5
00
400
500
300
500
400
600
700
9
01
2
00
1
13
Anti
cipat
edre
gre
tan
d
worr
yab
out
no
upta
ke
49
2(1
56)
02
3
03
8
06
2
01
1
06
9
01
9
07
1
05
3
03
6
00
6
02
3
02
0
Sm
all
effe
ctsi
ze
rgt
01
0
med
ium
effe
ctsi
ze
03
0lt
rlt
05
0
larg
eef
fect
size
rgt
05
0
Plt
00
5
Plt
00
1
R Hofman et al
90
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nloaded from
Tab
leII
IH
iera
rchic
al
logis
tic
regre
ssio
nanaly
ses
wit
hupta
ke(y
esn
o)
as
dep
enden
tva
riable
all
vari
able
sare
report
edby
pare
nts
at
base
line
Univ
aria
te
Model
1
(nfrac14
708)
Model
2a
(nfrac14
644)
Model
2b
(nfrac14
617)
Model
3
(nfrac14
572)
Model
4
(nfrac14
569)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
Dem
ogra
ph
icch
ara
cter
isti
cs
Age
of
par
ents
(yea
rs)
10
2(0
98ndash10
7)
10
1(0
96ndash10
6)
10
3(0
96ndash10
9)
10
2(0
95ndash11
0)
10
2(0
94ndash11
1)
10
1(0
93ndash10
9)
Educa
tional
level
11
5(1
00ndash13
4)
11
7(0
99ndash13
7)
12
5(1
00ndash15
4)
12
0(0
93ndash15
5)
12
7(0
96ndash17
0)
13
3(0
99ndash17
8)
No
reli
gio
us
affi
liat
ion
17
3(1
19ndash25
3)
16
3(1
09ndash24
2)
17
3(1
07ndash28
1)
11
2(0
63ndash20
0)
11
9(0
63ndash22
5)
11
6(0
60ndash22
3)
Dec
isio
nab
out
upta
ke
2011
(vs
2010)
20
8(1
28ndash33
6)
26
8(1
57ndash45
3)
26
9(1
42ndash51
0)
24
5(1
20ndash50
1)
24
8(1
11ndash55
2)
26
0(1
16ndash58
0)
Pare
nt
chara
cter
isti
cs
No
abnorm
alsm
ear
exper
ience
10
2(0
58ndash17
8)
09
4(0
45ndash19
5)
07
0(0
26ndash18
8)
06
8(0
24ndash19
5)
Par
enta
lre
sponsi
bil
ity
12
3(0
83ndash18
4)
15
3(0
91ndash25
9)
15
5(0
76ndash31
8)
18
6(0
90ndash38
3)
Tru
stin
NIP
35
4(2
61ndash48
1)
18
2(1
21ndash27
4)
14
0(0
86ndash23
0)
13
3(0
79ndash22
4)
Tru
stin
vac
cine
36
4(2
85ndash46
4)
34
1(2
49ndash46
8)
12
3(0
69ndash18
3)
09
9(0
59ndash16
7)
Per
ceiv
edsu
scep
tibil
ity
of
moth
erto
cerv
ical
cance
r
10
4(0
93ndash11
6)
10
3(0
88ndash12
1)
09
7(0
77ndash12
2)
09
6(0
76ndash12
2)
Soci
al
cogn
itiv
efa
ctors
Inte
nti
on
45
9(3
56ndash59
2)
26
1(1
47ndash46
1)
Am
biv
alen
ceto
war
dH
PV
vac
cinat
ion
08
2(0
69ndash09
2)
10
7(0
79ndash14
5)
02
7(0
08ndash08
7)
02
2(0
07ndash07
1)
Posi
tive
atti
tude
tow
ard
HP
Vvac
cinat
ion
57
3(4
26ndash77
1)
34
3(2
01ndash58
4)
17
0(0
69ndash42
1)
08
9(0
34ndash23
6)
Soci
alnorm
12
1(1
16ndash12
6)
10
7(1
01ndash11
3)
10
5(0
99ndash11
1)
10
3(0
97ndash10
9)
Norm
ativ
ebel
ief
14
4(1
28ndash16
3)
09
9(0
81ndash12
1)
10
3(0
83ndash12
9)
10
3(0
81ndash12
9)
Know
ledge
10
8(0
95ndash12
2)
09
5(0
87ndash10
4)
09
3(0
76ndash11
3)
09
5(0
78ndash11
7)
Per
ceiv
edsu
scep
tibil
ity
of
dau
ghte
rif
vac
cinat
ed
toce
rvic
alca
nce
r
06
5(0
57ndash07
4)
08
6(0
70ndash10
5)
08
9(0
69ndash11
4)
08
8(0
68ndash11
4)
Per
ceiv
edse
ver
ity
of
cerv
ical
cance
r
12
2(1
03ndash14
6)
10
8(0
81ndash14
2)
10
6(0
78ndash14
4)
10
8(0
79ndash14
8)
Anti
cipat
edre
gre
tan
d
worr
yab
out
no
upta
ke
22
3(1
93ndash25
8)
14
3(1
11ndash18
4)
14
3(1
08ndash18
9)
12
4(0
92ndash16
7)
Am
biv
alen
ce
atti
tude
inte
ract
ion
16
8(1
14ndash24
7)
17
9(1
22ndash26
2)
R2
00
603
505
305
705
9
Plt
00
5Plt
00
1an
dPlt
00
01
Predictors of HPV vaccination uptake
91
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nloaded from
132ndash192) and social norm (OR 107 95 CI
104ndash110) A lower uptake intention was asso-
ciated with a higher educational level (OR 083
95 CI 070ndash099) and a higher perceived parental
responsibility for their daughterrsquos health (OR 048
95 CI 030ndash075) The interaction term of atti-
tude ambivalence was significant (OR 073
95 CI 059ndash090)
Impact of time
Favorable changes in attitudes toward HPV uptake
over time were significantly related to an increase in
trust in the vaccine (OR 145 95 CI 136ndash153)
and social norm (OR 122 95 CI 115ndash128) over
time and a decrease in ambivalence toward HPV
vaccination (OR 094 95 CI 091ndash098) A de-
crease in ambivalence toward HPV vaccination
over time was significantly related to an increase
in feeling informed about HPV vaccination (OR
079 95 CI 069ndash091) and an increase in trust
in the vaccine (OR 088 95 CI 077ndash099) over
time
Informed decision making
Overall knowledge levels about the degreeduration
of protection were low at baseline and at follow-up
(33ndash43 correct answers) Percentages of correct
responses to five knowledge items increased signifi-
cantly at follow-up (Table IV) When five (out of
seven) correct items were defined as sufficient deci-
sion relevant knowledge then nfrac14 338 (439) of
the respondents made an informed choice about
uptake When four correct items were considered
sufficient then nfrac14 437 (657) of the respondents
made an informed choice about uptake (Table V)
Reasons for vaccinating or not
Main reasons as reported by parents at baseline to
have their daughter vaccinated include feeling re-
sponsible for her health (nfrac14 947 549) a family
history of cancer (nfrac14 128 74) anticipating
regret in case their daughter gets cervical cancer
(nfrac14 103 60) and other (nfrac14 547 317) Main
reasons as reported by parents at baseline not to have
their daughter vaccinated include that consequences
Table IV Knowledge items as completed by those who responded to the baseline and follow-up questionnaire (nfrac14 793)
Correct responses
Baseline
measurement
Follow-up
measurement
Significance level for
difference between
baseline and follow-up
n () n () P-value
Item (truefalse)
HPV causes cervical cancer (true) 496 (625) 479 (604) 0336
A condom protects 100 against HPV (false) 464 (585) 518 (653) 0001
The HPV vaccination will decrease the risk of cervical
cancer (true)
673 (849) 726 (916) lt0001
Vaccination in combination with having a smear taken is
more protective than only vaccination (true)
521 (657) 598 (754) lt0001
Item (multiple choice)
How is HPV transmitted (through blood oxygen sexual
contact)
699 (881) 730 (921) 0006
What is the protection rate of the HPV vaccine (55 70
85 100)
286 (361) 337 (425) 0005
What is the protection duration of a complete vaccination
against cervical cancer (at least 6 (8 at follow-up) years
at least 30 years lifetime)
289 (364) 262 (330) 0094
Correct answers are shaded
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nloaded from
of vaccinating are unpredictable (497 288) fear
of serious side-effects (nfrac14 401 232) and too
little information about the vaccine being available
(nfrac14 125 72)
Discussion
In this study among parents we assessed longitu-
dinal predictors of HPV vaccination uptake of their
daughters Uptake was predicted by intention a later
(2011) versus earlier (2010) decision about uptake
and anticipated regret and worry in case of abstain-
ing from HPV vaccination Ambivalence toward
HPV vaccination at baseline moderated the attitude
(baseline) uptake (follow-up) relationship with the
attitudendashuptake relationship being stronger at higher
ambivalence levels
HPV vaccination was most strongly predicted by
intention which fits the TPB model and was also
reported in an earlier study on predictors of HPV
vaccination uptake [22] In turn HPV vaccination
intention was positively associated with educational
level perceived parental responsibility for onersquos
daughterrsquos health trust in the vaccine the belief
that according to significant others their daughter
should be vaccinated and the motivation to comply
with that (social norm) and anticipated regret and
worry (which also predicted uptake) The relation-
ship found between intention and uptake and
between intention and social norm is consistent
with the TPB model and with another study [22]
which also confirms the association we found
between anticipated regretworry and uptake and
anticipated regretworry and intention The factors
lsquoperceived susceptibilityrsquo and lsquoseverityrsquo of cancer
of the HBM were not associated with intention or
uptake which confirms the results of an earlier study
[22 36]
A possible explanation for the positive effect on
uptake of having to decide later (2011) versus earlier
(2010) might be the amount of time that passed be-
tween the baseline questionnaire (2009) when an
intensive societal debate involving politics phys-
icians media parents and girls about HPV vaccin-
ation was ongoing and the actual decision about
uptake of vaccination In 2011 this debate probably
had less impact on the uptake decision than in 2010
Also after millions of girls worldwide had been
vaccinated and no serious side-effects had been
reported parents who had to decide later versus
earlier probably felt more reassured about the
vaccinersquos safety
This study shows that ambivalence moderated the
attitudendashuptake relationship Parents with a positive
attitude and a high level of ambivalence toward
HPV vaccination were more likely to have their
daughter vaccinated than parents with a positive at-
titude and a low level of ambivalence This finding
might be explained in two ways First ambivalence
is characterized as being subjectively uncomfortable
and people may be motivated to resolve the conflict-
ing evaluations that they hold [37] for example
by searching for information Second earlier
studies found that ambivalent people processed
pro-attitudinal messages to a greater extent than
counter-attitudinal messages probably because
pro-attitudinal messages are more likely to reduce
ambivalence [38 39] Taking these two mechanisms
together it is likely that in our study ambivalent
parents with a positive attitude toward HPV vaccin-
ation processed lsquopositiversquo messages about HPV vac-
cination to a greater extent than lsquonegativersquo messages
and were therefore more likely to have their
Table V Informed decision at follow-up (nfrac14 770)
Daughter
vaccinated
(nfrac14 640)
Daughter not
vaccinated
(nfrac14 130)
n () n ()
Positive attitude
Five or more correct items 280 (364) 14 (18)
Less than five correct items 246 (319) 16 (21)
Negative attitude
Five or more correct items 51 (66) 58 (75)
Less than five correct items 32 (42) 34 (44)
Knowledge was measured with seven items at follow-upInformed decision rate for cut-off at three correct items761 [(504 + 82)770] four correct items 657[(437 + 69)770] five correct items 439 [(280 + 58)770]six correct items 187 [(117 + 27)770] Due to missingitems analyses were based on nfrac14 770 respondents instead ofnfrac14 793 Informed choice (as defined) is shaded
Predictors of HPV vaccination uptake
93
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nloaded from
daughter vaccinated In other words parents who
had both positive attitudes and were ambivalent to-
ward HPV vaccination became even more positive
because they elaborated only information in favor of
HPV vaccination This may imply that this lsquobiasedrsquo
information processing has a negative impact on
informed decision making although parents will
have gained more knowledge during their efforts
to resolve their ambivalence
Assessing decisional factors related to HPV vac-
cination both before and after the decision-making
process about uptake provided a unique opportun-
ity to determine changes in those factors over time
As uptake was predicted by intention and intention
was highly correlated with attitude (rfrac14 084) (at
baseline) we think it is relevant to show which
factors are important for changes in attitude over
time Our results show that a more positive attitude
toward HPV vaccination over time was associated
with an increase in trust in the vaccine and in
social norm over time and a decrease in ambiva-
lence toward HPV vaccination over time This
latter factor was related to an increase in feeling
informed about HPV vaccination and an increase
in trust in the vaccine over time In summary over
time parents felt better informed became less am-
bivalent and had more trust in the vaccine These
results are in accordance with our finding that
girls who had to decide with their parents whether
or not to be vaccinated in 2011 were more likely
to be vaccinated than those who had to decide
in 2010
An important finding is that knowledge about the
duration of protection was low at both baseline and
follow-up For instance about 65 of the parents
thought that protection lasts 30 years or even life-
long As the duration of protection is still unknown
it is important that parents and girls know that
booster vaccinations might be needed in the future
When we applied a cut-off of four or five correct
knowledge items (out of seven) then the rates
of informed choice about uptake were not high
66 and 44 respectively However this finding
should be interpreted with caution because the
time period between the assessment of knowledge
and the last vaccination out of three shots was
1 month (decision in 2011) or 14 months (decision
in 2010) In educational material it should be clearly
stated what is known and not yet known about HPV
vaccination
Study strengths include the longitudinal design
as recommended by authors of a cross-sectional
study [40] the high (absolute) number of respond-
ents of the baseline (nfrac14 1725) and follow-up ques-
tionnaires (nfrac14 793) and the high response rate of the
follow-up questionnaire (74)
Limitations
A limitation was the low response rate of the base-
line questionnaire (30) which might be due to the
length of the questionnaire Our sample may there-
fore not be representative of the general population
as few parents had a low educational level Also
demographic characteristics of the follow-up group
were slightly different from those of the baseline
group with more parents being better educated
and well-off at follow-up These parents might pos-
sibly be more likely than those in the wider popula-
tion to seek to reduce high ambivalence by
searching information allowing them to respond
positively to the vaccine invitationmdashrather than do
nothing
Conclusion
In conclusion this study shows that intention a later
versus earlier decision about uptake and anticipated
regretworry about abstaining from vaccination
were predictors of uptake Anticipated regret was a
common predictor of intention and uptake and thus
an important factor in the decision-making process
about HPV vaccination In turn predictors of inten-
tion like social norm and trust in the vaccine are
also important when deciding about HPV vaccin-
ation Over time parents felt better informed
became less ambivalent and had more trust in the
vaccine
Practice implications
This study shows the usefulness of including affect-
ive factors in studies examining HPV vaccination
R Hofman et al
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nloaded from
behavior as anticipated regret trust in the vaccine
and ambivalence were found to play a role in the
decision making about uptake However it is also
important that parents are enabled to base their
decision about HPV vaccination of their daughter
on decision relevant knowledge As these results
suggest that people need sufficient time to decide
about the uptake of a new vaccine we recommend
a well-balanced stepwise process of implementa-
tion that is let parents first become aware of the
link between HPV and cervical cancer then provide
them with balanced information about all the
knowns and also the unknowns of HPV vaccination
and then finally offer them the opportunity to have
their daughter vaccinated As two-third of parents
wrongly thought that protection lasts 30 years or
even lifelong educational material should clearly
state that booster vaccinations might be needed in
the future
Acknowledgements
The authors thank the Dutch Cancer Society for
financial support and the participants for their
contribution to the study
Funding
The Dutch Cancer Society [EMCR 2008-3992
EMCR 2009-4561]
Conflict of interest statement
None declared
References
1 Karim-Kos HE de Vries E Soerjomataram I et al Recenttrends of cancer in Europe a combined approach of inci-dence survival and mortality for 17 cancer sites since the1990s Eur J Cancer 2008 44 1345ndash89
2 Bosch FX Lorincz A Munoz N et al The causal relationbetween human papillomavirus and cervical cancer J ClinPathol 2002 55 244ndash65
3 Walboomers JM Jacobs MV Manos MM et al Humanpapillomavirus is a necessary cause of invasive cervicalcancer worldwide J Pathol 1999 189 12ndash9
4 Munoz N Bosch FX Castellsague X et al Against whichhuman papillomavirus types shall we vaccinate and screenThe international perspective Int J Cancer 2004 111278ndash85
5 Koutsky LA Holmes KK Critchlow CW et al A cohortstudy of the risk of cervical intraepithelial neoplasia grade2 or 3 in relation to papillomavirus infection N Engl J Med1992 327 1272ndash8
6 Woodman CB Collins S Winter H et al Natural history ofcervical human papillomavirus infection in young women alongitudinal cohort study Lancet 2001 357 1831ndash6
7 Boot HJ Wallenburg I de Melker HE et al Assessing theintroduction of universal human papillomavirus vaccinationfor preadolescent girls in The Netherlands Vaccine 2007 256245ndash56
8 van Lier EA Oomen PJ Oostenbrug MWM et alImmunization coverage National ImmunizationProgramme in the Netherlands Year of report 2009[Vaccinatiegraad Rijksvaccinatieprogramma NederlandVerslagjaar 2009] Bilthoven RIVM 2009
9 Zwakhals SLN van Lier EA van HPV (cohort 1997) bymunicipality 2012 [HPV (cohort 1997) per gemeente2012] In Dutch National Atlas of Public HealthBilthoven RIVM 2012 (httpwwwzorgatlasnlpreventievaccinaties-en-screeninghpv-cohort-1997-vaccinatiegraad-per-gemeente-2012 accessed 2 September 2013)
10 Brabin L Roberts SA Stretch R et al A survey of adolescentexperiences of human papillomavirus vaccination in theManchester study Br J cancer 2009 101 1502ndash4
11 Brabin L Roberts SA Kitchener HC A semi-qualitativestudy of attitudes to vaccinating adolescents against humanpapillomavirus without parental consent BMC PublicHealth 2007 7 20
12 Brewer NT Fazekas KI Predictors of HPV vaccine accept-ability A theory-informed systematic review Prev Med2007 45 107ndash14
13 Kahn JA Rosenthal SL Jin Y et al Rates of human papillo-mavirus vaccination attitudes about vaccination and humanpapillomavirus prevalence in young women Obstet Gynecol2008 111 1103ndash10
14 Askelson NM Campo S Lowe JB et al Using the theoryof planned behavior to predict mothersrsquo intentions to vaccin-ate their daughters against HPV J Sch Nurs 2010 26194ndash202
15 Ajzen I The theory of Planned Behavior Organ Behav HumDecis Process 1991 50 179ndash211
16 Becker MH The health belief model and personal healthbehavior Health Edu Monogr 1974 2 324ndash508
17 Chapman GB Coups EJ Emotions and preventive healthbehavior worry regret and influenza vaccination HealthPsychol 2006 25 82ndash90
18 Paulussen TG Hoekstra F Lanting CI et al Determinants ofDutch parentsrsquo decisions to vaccinate their child Vaccine2006 24 644ndash51
19 Kaplan KJ On the ambivalence-indifference problem inattitude theory and measurement A suggested modificationof the semantic differential technique Psychol Bull 1972 77361ndash372
20 Dormandy E Hankins M Marteau TM Attitudes and uptakeof a screening test The moderating role of ambivalencePsychol Health 2006 21 499ndash511
Predictors of HPV vaccination uptake
95
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
21 Hofman R van Empelen P Vogel I et al Parental decisionalstrategies regarding HPV vaccination prior to media debatesa focus-group study J Health Commun 2013 18 866ndash80
22 Brewer NT Gottlieb SL Reiter PL et al Longitudinal pre-dictors of human papillomavirus vaccine initiation amongadolescent girls in a high-risk geographic area Sex TransmDis 2011 38 197ndash204
23 Marlow LA Waller J Wardle J Trust and experience aspredictors of HPV vaccine acceptance Hum Vaccin 20073 171ndash5
24 Weinstein ND Perceived probability perceived severityand health-protective behavior Health Psychol 2000 1965ndash74
25 Marteau TM Dormandy E Michie S A measure of informedchoice Health Expect 2001 4 99ndash108
26 van den Berg M Timmermans DR Ten Kate LP et al Arepregnant women making informed choices about prenatalscreening Genet Med 2005 7 332ndash8
27 Tiro JA Diamond PM Perz CA et al Validation of scalesmeasuring attitudes and norms related to mammographyscreening in women veterans Health Psychol 2005 24555ndash66
28 Marlow LAV Waller J Wardle J Parental attitudes to pre-pubertal HPV vaccination Vaccine 2007 25 1945ndash52
29 Stalmeier PF Roosmalen MS Verhoef LC et al Thedecision evaluation scales Patient Educ Couns 2005 57286ndash93
30 Gilbert LA Hanson GR Perceptions of parental role respon-sibilities among working people Development of a compre-hensive measure J Marriage Fam 1983 45 203ndash12
31 Korfage IJ van Ballegooijen M Wauben B et al Informedchoice on Pap smear still limited by lack of knowledge on the
meaning of false-positive or false-negative test resultsPatient Educ Couns 2011 85 214ndash8
32 Thompson MM Zanna MP The conflicted individual per-sonality-based and domain specific antecedents of ambiva-lent social attitudes J Pers 1995 63 259ndash88
33 General Medical Council Seeking Patientsrsquo Consent TheEthical Considerations London GMC 1998
34 Minister of Health Letter about screening [Kaderbriefscreening] PGZP 2848440 Ministry of Health Welfareand Sports The Hague 2008
35 Aiken LS West RR Multiple Regression Testing andInterpreting Interactions Newbury Park CA Sage 1991
36 Krawczyk AL Perez S Lau E et al Human papillomavirusvaccination intentions and uptake in college women HealthPsychol 2012 31 685ndash93
37 Newby-Clark IR McGregor I Zanna MP Thinking andcaring about cognitive inconsistency when and for whomdoes attitudinal ambivalence feel uncomfortable J Pers SocPsychol 2002 82 157ndash66
38 Nordgren LF van Harreveld F van der Pligt J Ambivalencediscomfort and motivated information processing J ExperSoc Psychol 2006 42 252ndash8
39 Clark JK Wegener DT Fabrigar LR Attitudinal ambiva-lence and message-based persuasion motivated processingof proattitudinal information and avoidance of counterattitu-dinal information Pers Soc Psychol Bull 2008 34 565ndash77
40 van Keulen HM Otten W Ruiter RA et al Determinants ofHPV vaccination intentions among Dutch girls and theirmothers a cross-sectional study BMC Public Health 201313 111
R Hofman et al
96
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nloaded from
Table I Characteristics of the respondents (parents)
Total baseline
group (nfrac14 1725)
Subgroup that completed
follow-up assessment (nfrac14 793)
Characteristics Mean (SD) Mean (SD) P-value
Age at baseline (years) 428 (417) 430 (405) 0015
range 29ndash59 32ndash58
Children
Age (years) 133 (342) 133 (321)
Age range 0ndash34 0ndash34
Number of girls 17 (078) 17 (074)
Number of boys 09 (077) 09 (076)
n () n ()
Marital status 0372
Marriedcohabiting 1477 (872) 693 (894)
Partner but living alone 34 (20) 16 (21)
No partner 165 (97) 66 (85)
Sex 0233
Female 1596 (933) 743 (937)
Educational level lt0001
Low 200 (121) 64 (83)
Intermediate 789 (479) 358 (467)
High 658 (400) 345 (450)
Job status 0270
Paid job 1268 (786) 617 (816)
Housewife or houseman or unpaid job or student 295 (183) 119 (157)
No job 51 (32) 20 (26)
Net income per month (euros) lt0001
lt1500 161 (105) 45 (61)
1500ndash3000 584 (382) 267 (364)
3000ndash4500 488 (320) 264 (360)
gt4500 294 (193) 157 (214)
Country of birth lt0001
The Netherlands 1550 (910) 740 (938)
Turkey Morocco 37 (22) 6 (08)
Suriname Aruba Netherlands Antilles 16 (09) 4 (05)
Other 100 (59) 39 (49)
Country of birth of both parents 0002
The Netherlands 1459 (885) 703 (894)
Turkey Morocco 44 (27) 9 (11)
Suriname Aruba Netherlands Antilles 19 (12) 5 (06)
Other 126 (76) 69 (88)
Religion 0590
None 960 (570) 450 (579)
Christian 611 (363) 290 (373)
Muslim 57 (34) 13 (17)
Other 54 (32) 24 (31)
Decision about HPV vaccination uptake
In 2010 - 555 (715)
In 2011 - 221 (285)
(continued)
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Predictors of HPV vaccination uptake
Pearsonrsquos correlations showed that most associ-
ations between the predictors were positive
(Table II) Table III presents the results of the hier-
archical logistic regression analyses to predict
HPV vaccination uptake The first model in which
HPV vaccination uptake was regressed on demo-
graphic factors showed that uptake at follow-up
was significantly predicted by religion and the
year the decision about uptake was made (2011
versus 2010) (pseudo R2frac14 006) Specifically
those respondents without a religious affiliation
and those who had to decide in 2011 were more
likely to have their daughter vaccinated In Model
2a parent characteristics were added this model
explained an additional 29 variance HPV vaccin-
ation was more likely for parents with a higher edu-
cational level having no religious affiliation
decision about uptake in 2011 and higher trust in
the NIP and the vaccine In Model 2b (demographic
characteristics and social cognitive factors) signifi-
cant predictors were year of decision about uptake
(2011 versus 2010) a positive attitude toward HPV
vaccination social norm and anticipated regret and
worry about no uptake (pseudo R2frac14 053) In Model
3 (including all predictors except intention) vaccin-
ation was more likely for parents who had to decide
in 2011 ambivalence toward HPV vaccination
(under the condition that attitude is equal to 0) and
higher anticipated regret and worry about no uptake
The interaction term of attitude ambivalence was
also significant (pseudo R2frac14 057) In Model 4
(including all predictors) significant predictors of
uptake were the year the decision about uptake
was made (2011 versus 2010) a higher intention
ambivalence toward HPV vaccination (under the
condition that attitude is equal to 0) and the inter-
action term of attitude ambivalence
The significant interaction term attitude am-
bivalence showed that the predictive validity of at-
titude improved as scores of ambivalence increased
from low (bfrac14 089 Pfrac14 00238) to moderate
(bfrac14 144 Pfrac14 0001) and from moderate
(bfrac14 144 Pfrac14 0001) to high (bfrac14 198 Plt 0001)
Associations of HPV vaccination intention
Alternatively we performed an ordinal logistic re-
gression analysis with intention (instead of uptake)
as dependent variable (data not shown) This ana-
lysis showed that a higher intention was associated
with a positive attitude toward HPV vaccination
[odds ratio (OR) 1953 95 confidence interval
(CI) 1032ndash3693] (under the condition that am-
bivalence is frac140) ambivalence toward HPV vaccin-
ation (OR 239 95 CI 110ndash518) (under the
condition that attitude is frac140) trust in the vaccine
(OR 162 95 CI 116ndash227) anticipated regret
and worry about no uptake (OR 159 95 CI
Table I Continued
Total baseline
group (nfrac14 1725)
Subgroup that completed
follow-up assessment (nfrac14 793)
Characteristics Mean (SD) Mean (SD) P-value
If female abnormal Pap smear result 0103
Yes 185 (117) 98 (132)
No 1351 (856) 634 (853)
Never had a Pap smear taken 42 (27) 11 (15)
Daughter vaccinated against DPTPa and MMRb 0038
Yes 1654 (959) 778 (981)
Daughter vaccinated against HPV
Yes - 652 (831)
The subgroup that completed the follow-up assessment differed significantly from the baseline group on six characteristicsaDPTP refers to diphtheria pertussis tetanus and poliomyelitisbMMR refers to measles mumps and rubella
Predictors of HPV vaccination uptake
89
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Tab
leII
M
eans
standard
dev
iati
ons
(SD
)and
Pea
rsonrsquos
corr
elati
on
bet
wee
nth
epre
dic
tors
at
base
line
(nfrac14
793)
Mea
n(S
D)
12
34
56
78
910
11
12
1
Par
enta
lre
sponsi
bil
ity
45
0(0
46)
2
Tru
stin
NIP
48
6(0
67)
00
4
3
Tru
stin
vac
cine
43
1(0
92)
00
605
4
4
Per
ceiv
edsu
scep
tibil
ity
of
moth
erto
cerv
ical
cance
r
49
7(1
74)
00
500
100
2
5
Inte
nti
on
38
9(1
07)
00
304
8
07
3
00
5
6
Am
biv
alen
ce17
1(1
07)
00
7
02
0
02
6
00
1
02
9
7
Att
itude
tow
ard
HP
V
vac
cinat
ion
37
3(1
44)
00
9
05
1
07
7
00
508
4
03
3
8
Soci
alnorm
61
0(1
03
1)
01
5
03
3
05
1
00
706
1
01
8
06
4
9
Norm
ativ
ebel
ief
71
2(1
57)
00
501
9
03
3
00
103
3
00
9
03
4
03
7
10
Know
ledge
43
2(1
49)
00
9
01
0
00
300
300
3
00
700
200
3
00
3
11
Per
ceiv
edsu
scep
tibil
ity
of
dau
ghte
rif
vac
cinat
ed
toce
rvic
alca
nce
r
37
3(1
44)
00
6
02
3
03
0
04
1
02
6
00
3
03
1
02
3
02
3
00
1
12
Per
ceiv
edse
ver
ity
of
cerv
ical
cance
r
106
0(0
93)
02
5
00
400
500
300
500
400
600
700
9
01
2
00
1
13
Anti
cipat
edre
gre
tan
d
worr
yab
out
no
upta
ke
49
2(1
56)
02
3
03
8
06
2
01
1
06
9
01
9
07
1
05
3
03
6
00
6
02
3
02
0
Sm
all
effe
ctsi
ze
rgt
01
0
med
ium
effe
ctsi
ze
03
0lt
rlt
05
0
larg
eef
fect
size
rgt
05
0
Plt
00
5
Plt
00
1
R Hofman et al
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Tab
leII
IH
iera
rchic
al
logis
tic
regre
ssio
nanaly
ses
wit
hupta
ke(y
esn
o)
as
dep
enden
tva
riable
all
vari
able
sare
report
edby
pare
nts
at
base
line
Univ
aria
te
Model
1
(nfrac14
708)
Model
2a
(nfrac14
644)
Model
2b
(nfrac14
617)
Model
3
(nfrac14
572)
Model
4
(nfrac14
569)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
Dem
ogra
ph
icch
ara
cter
isti
cs
Age
of
par
ents
(yea
rs)
10
2(0
98ndash10
7)
10
1(0
96ndash10
6)
10
3(0
96ndash10
9)
10
2(0
95ndash11
0)
10
2(0
94ndash11
1)
10
1(0
93ndash10
9)
Educa
tional
level
11
5(1
00ndash13
4)
11
7(0
99ndash13
7)
12
5(1
00ndash15
4)
12
0(0
93ndash15
5)
12
7(0
96ndash17
0)
13
3(0
99ndash17
8)
No
reli
gio
us
affi
liat
ion
17
3(1
19ndash25
3)
16
3(1
09ndash24
2)
17
3(1
07ndash28
1)
11
2(0
63ndash20
0)
11
9(0
63ndash22
5)
11
6(0
60ndash22
3)
Dec
isio
nab
out
upta
ke
2011
(vs
2010)
20
8(1
28ndash33
6)
26
8(1
57ndash45
3)
26
9(1
42ndash51
0)
24
5(1
20ndash50
1)
24
8(1
11ndash55
2)
26
0(1
16ndash58
0)
Pare
nt
chara
cter
isti
cs
No
abnorm
alsm
ear
exper
ience
10
2(0
58ndash17
8)
09
4(0
45ndash19
5)
07
0(0
26ndash18
8)
06
8(0
24ndash19
5)
Par
enta
lre
sponsi
bil
ity
12
3(0
83ndash18
4)
15
3(0
91ndash25
9)
15
5(0
76ndash31
8)
18
6(0
90ndash38
3)
Tru
stin
NIP
35
4(2
61ndash48
1)
18
2(1
21ndash27
4)
14
0(0
86ndash23
0)
13
3(0
79ndash22
4)
Tru
stin
vac
cine
36
4(2
85ndash46
4)
34
1(2
49ndash46
8)
12
3(0
69ndash18
3)
09
9(0
59ndash16
7)
Per
ceiv
edsu
scep
tibil
ity
of
moth
erto
cerv
ical
cance
r
10
4(0
93ndash11
6)
10
3(0
88ndash12
1)
09
7(0
77ndash12
2)
09
6(0
76ndash12
2)
Soci
al
cogn
itiv
efa
ctors
Inte
nti
on
45
9(3
56ndash59
2)
26
1(1
47ndash46
1)
Am
biv
alen
ceto
war
dH
PV
vac
cinat
ion
08
2(0
69ndash09
2)
10
7(0
79ndash14
5)
02
7(0
08ndash08
7)
02
2(0
07ndash07
1)
Posi
tive
atti
tude
tow
ard
HP
Vvac
cinat
ion
57
3(4
26ndash77
1)
34
3(2
01ndash58
4)
17
0(0
69ndash42
1)
08
9(0
34ndash23
6)
Soci
alnorm
12
1(1
16ndash12
6)
10
7(1
01ndash11
3)
10
5(0
99ndash11
1)
10
3(0
97ndash10
9)
Norm
ativ
ebel
ief
14
4(1
28ndash16
3)
09
9(0
81ndash12
1)
10
3(0
83ndash12
9)
10
3(0
81ndash12
9)
Know
ledge
10
8(0
95ndash12
2)
09
5(0
87ndash10
4)
09
3(0
76ndash11
3)
09
5(0
78ndash11
7)
Per
ceiv
edsu
scep
tibil
ity
of
dau
ghte
rif
vac
cinat
ed
toce
rvic
alca
nce
r
06
5(0
57ndash07
4)
08
6(0
70ndash10
5)
08
9(0
69ndash11
4)
08
8(0
68ndash11
4)
Per
ceiv
edse
ver
ity
of
cerv
ical
cance
r
12
2(1
03ndash14
6)
10
8(0
81ndash14
2)
10
6(0
78ndash14
4)
10
8(0
79ndash14
8)
Anti
cipat
edre
gre
tan
d
worr
yab
out
no
upta
ke
22
3(1
93ndash25
8)
14
3(1
11ndash18
4)
14
3(1
08ndash18
9)
12
4(0
92ndash16
7)
Am
biv
alen
ce
atti
tude
inte
ract
ion
16
8(1
14ndash24
7)
17
9(1
22ndash26
2)
R2
00
603
505
305
705
9
Plt
00
5Plt
00
1an
dPlt
00
01
Predictors of HPV vaccination uptake
91
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nloaded from
132ndash192) and social norm (OR 107 95 CI
104ndash110) A lower uptake intention was asso-
ciated with a higher educational level (OR 083
95 CI 070ndash099) and a higher perceived parental
responsibility for their daughterrsquos health (OR 048
95 CI 030ndash075) The interaction term of atti-
tude ambivalence was significant (OR 073
95 CI 059ndash090)
Impact of time
Favorable changes in attitudes toward HPV uptake
over time were significantly related to an increase in
trust in the vaccine (OR 145 95 CI 136ndash153)
and social norm (OR 122 95 CI 115ndash128) over
time and a decrease in ambivalence toward HPV
vaccination (OR 094 95 CI 091ndash098) A de-
crease in ambivalence toward HPV vaccination
over time was significantly related to an increase
in feeling informed about HPV vaccination (OR
079 95 CI 069ndash091) and an increase in trust
in the vaccine (OR 088 95 CI 077ndash099) over
time
Informed decision making
Overall knowledge levels about the degreeduration
of protection were low at baseline and at follow-up
(33ndash43 correct answers) Percentages of correct
responses to five knowledge items increased signifi-
cantly at follow-up (Table IV) When five (out of
seven) correct items were defined as sufficient deci-
sion relevant knowledge then nfrac14 338 (439) of
the respondents made an informed choice about
uptake When four correct items were considered
sufficient then nfrac14 437 (657) of the respondents
made an informed choice about uptake (Table V)
Reasons for vaccinating or not
Main reasons as reported by parents at baseline to
have their daughter vaccinated include feeling re-
sponsible for her health (nfrac14 947 549) a family
history of cancer (nfrac14 128 74) anticipating
regret in case their daughter gets cervical cancer
(nfrac14 103 60) and other (nfrac14 547 317) Main
reasons as reported by parents at baseline not to have
their daughter vaccinated include that consequences
Table IV Knowledge items as completed by those who responded to the baseline and follow-up questionnaire (nfrac14 793)
Correct responses
Baseline
measurement
Follow-up
measurement
Significance level for
difference between
baseline and follow-up
n () n () P-value
Item (truefalse)
HPV causes cervical cancer (true) 496 (625) 479 (604) 0336
A condom protects 100 against HPV (false) 464 (585) 518 (653) 0001
The HPV vaccination will decrease the risk of cervical
cancer (true)
673 (849) 726 (916) lt0001
Vaccination in combination with having a smear taken is
more protective than only vaccination (true)
521 (657) 598 (754) lt0001
Item (multiple choice)
How is HPV transmitted (through blood oxygen sexual
contact)
699 (881) 730 (921) 0006
What is the protection rate of the HPV vaccine (55 70
85 100)
286 (361) 337 (425) 0005
What is the protection duration of a complete vaccination
against cervical cancer (at least 6 (8 at follow-up) years
at least 30 years lifetime)
289 (364) 262 (330) 0094
Correct answers are shaded
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nloaded from
of vaccinating are unpredictable (497 288) fear
of serious side-effects (nfrac14 401 232) and too
little information about the vaccine being available
(nfrac14 125 72)
Discussion
In this study among parents we assessed longitu-
dinal predictors of HPV vaccination uptake of their
daughters Uptake was predicted by intention a later
(2011) versus earlier (2010) decision about uptake
and anticipated regret and worry in case of abstain-
ing from HPV vaccination Ambivalence toward
HPV vaccination at baseline moderated the attitude
(baseline) uptake (follow-up) relationship with the
attitudendashuptake relationship being stronger at higher
ambivalence levels
HPV vaccination was most strongly predicted by
intention which fits the TPB model and was also
reported in an earlier study on predictors of HPV
vaccination uptake [22] In turn HPV vaccination
intention was positively associated with educational
level perceived parental responsibility for onersquos
daughterrsquos health trust in the vaccine the belief
that according to significant others their daughter
should be vaccinated and the motivation to comply
with that (social norm) and anticipated regret and
worry (which also predicted uptake) The relation-
ship found between intention and uptake and
between intention and social norm is consistent
with the TPB model and with another study [22]
which also confirms the association we found
between anticipated regretworry and uptake and
anticipated regretworry and intention The factors
lsquoperceived susceptibilityrsquo and lsquoseverityrsquo of cancer
of the HBM were not associated with intention or
uptake which confirms the results of an earlier study
[22 36]
A possible explanation for the positive effect on
uptake of having to decide later (2011) versus earlier
(2010) might be the amount of time that passed be-
tween the baseline questionnaire (2009) when an
intensive societal debate involving politics phys-
icians media parents and girls about HPV vaccin-
ation was ongoing and the actual decision about
uptake of vaccination In 2011 this debate probably
had less impact on the uptake decision than in 2010
Also after millions of girls worldwide had been
vaccinated and no serious side-effects had been
reported parents who had to decide later versus
earlier probably felt more reassured about the
vaccinersquos safety
This study shows that ambivalence moderated the
attitudendashuptake relationship Parents with a positive
attitude and a high level of ambivalence toward
HPV vaccination were more likely to have their
daughter vaccinated than parents with a positive at-
titude and a low level of ambivalence This finding
might be explained in two ways First ambivalence
is characterized as being subjectively uncomfortable
and people may be motivated to resolve the conflict-
ing evaluations that they hold [37] for example
by searching for information Second earlier
studies found that ambivalent people processed
pro-attitudinal messages to a greater extent than
counter-attitudinal messages probably because
pro-attitudinal messages are more likely to reduce
ambivalence [38 39] Taking these two mechanisms
together it is likely that in our study ambivalent
parents with a positive attitude toward HPV vaccin-
ation processed lsquopositiversquo messages about HPV vac-
cination to a greater extent than lsquonegativersquo messages
and were therefore more likely to have their
Table V Informed decision at follow-up (nfrac14 770)
Daughter
vaccinated
(nfrac14 640)
Daughter not
vaccinated
(nfrac14 130)
n () n ()
Positive attitude
Five or more correct items 280 (364) 14 (18)
Less than five correct items 246 (319) 16 (21)
Negative attitude
Five or more correct items 51 (66) 58 (75)
Less than five correct items 32 (42) 34 (44)
Knowledge was measured with seven items at follow-upInformed decision rate for cut-off at three correct items761 [(504 + 82)770] four correct items 657[(437 + 69)770] five correct items 439 [(280 + 58)770]six correct items 187 [(117 + 27)770] Due to missingitems analyses were based on nfrac14 770 respondents instead ofnfrac14 793 Informed choice (as defined) is shaded
Predictors of HPV vaccination uptake
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Dow
nloaded from
daughter vaccinated In other words parents who
had both positive attitudes and were ambivalent to-
ward HPV vaccination became even more positive
because they elaborated only information in favor of
HPV vaccination This may imply that this lsquobiasedrsquo
information processing has a negative impact on
informed decision making although parents will
have gained more knowledge during their efforts
to resolve their ambivalence
Assessing decisional factors related to HPV vac-
cination both before and after the decision-making
process about uptake provided a unique opportun-
ity to determine changes in those factors over time
As uptake was predicted by intention and intention
was highly correlated with attitude (rfrac14 084) (at
baseline) we think it is relevant to show which
factors are important for changes in attitude over
time Our results show that a more positive attitude
toward HPV vaccination over time was associated
with an increase in trust in the vaccine and in
social norm over time and a decrease in ambiva-
lence toward HPV vaccination over time This
latter factor was related to an increase in feeling
informed about HPV vaccination and an increase
in trust in the vaccine over time In summary over
time parents felt better informed became less am-
bivalent and had more trust in the vaccine These
results are in accordance with our finding that
girls who had to decide with their parents whether
or not to be vaccinated in 2011 were more likely
to be vaccinated than those who had to decide
in 2010
An important finding is that knowledge about the
duration of protection was low at both baseline and
follow-up For instance about 65 of the parents
thought that protection lasts 30 years or even life-
long As the duration of protection is still unknown
it is important that parents and girls know that
booster vaccinations might be needed in the future
When we applied a cut-off of four or five correct
knowledge items (out of seven) then the rates
of informed choice about uptake were not high
66 and 44 respectively However this finding
should be interpreted with caution because the
time period between the assessment of knowledge
and the last vaccination out of three shots was
1 month (decision in 2011) or 14 months (decision
in 2010) In educational material it should be clearly
stated what is known and not yet known about HPV
vaccination
Study strengths include the longitudinal design
as recommended by authors of a cross-sectional
study [40] the high (absolute) number of respond-
ents of the baseline (nfrac14 1725) and follow-up ques-
tionnaires (nfrac14 793) and the high response rate of the
follow-up questionnaire (74)
Limitations
A limitation was the low response rate of the base-
line questionnaire (30) which might be due to the
length of the questionnaire Our sample may there-
fore not be representative of the general population
as few parents had a low educational level Also
demographic characteristics of the follow-up group
were slightly different from those of the baseline
group with more parents being better educated
and well-off at follow-up These parents might pos-
sibly be more likely than those in the wider popula-
tion to seek to reduce high ambivalence by
searching information allowing them to respond
positively to the vaccine invitationmdashrather than do
nothing
Conclusion
In conclusion this study shows that intention a later
versus earlier decision about uptake and anticipated
regretworry about abstaining from vaccination
were predictors of uptake Anticipated regret was a
common predictor of intention and uptake and thus
an important factor in the decision-making process
about HPV vaccination In turn predictors of inten-
tion like social norm and trust in the vaccine are
also important when deciding about HPV vaccin-
ation Over time parents felt better informed
became less ambivalent and had more trust in the
vaccine
Practice implications
This study shows the usefulness of including affect-
ive factors in studies examining HPV vaccination
R Hofman et al
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nloaded from
behavior as anticipated regret trust in the vaccine
and ambivalence were found to play a role in the
decision making about uptake However it is also
important that parents are enabled to base their
decision about HPV vaccination of their daughter
on decision relevant knowledge As these results
suggest that people need sufficient time to decide
about the uptake of a new vaccine we recommend
a well-balanced stepwise process of implementa-
tion that is let parents first become aware of the
link between HPV and cervical cancer then provide
them with balanced information about all the
knowns and also the unknowns of HPV vaccination
and then finally offer them the opportunity to have
their daughter vaccinated As two-third of parents
wrongly thought that protection lasts 30 years or
even lifelong educational material should clearly
state that booster vaccinations might be needed in
the future
Acknowledgements
The authors thank the Dutch Cancer Society for
financial support and the participants for their
contribution to the study
Funding
The Dutch Cancer Society [EMCR 2008-3992
EMCR 2009-4561]
Conflict of interest statement
None declared
References
1 Karim-Kos HE de Vries E Soerjomataram I et al Recenttrends of cancer in Europe a combined approach of inci-dence survival and mortality for 17 cancer sites since the1990s Eur J Cancer 2008 44 1345ndash89
2 Bosch FX Lorincz A Munoz N et al The causal relationbetween human papillomavirus and cervical cancer J ClinPathol 2002 55 244ndash65
3 Walboomers JM Jacobs MV Manos MM et al Humanpapillomavirus is a necessary cause of invasive cervicalcancer worldwide J Pathol 1999 189 12ndash9
4 Munoz N Bosch FX Castellsague X et al Against whichhuman papillomavirus types shall we vaccinate and screenThe international perspective Int J Cancer 2004 111278ndash85
5 Koutsky LA Holmes KK Critchlow CW et al A cohortstudy of the risk of cervical intraepithelial neoplasia grade2 or 3 in relation to papillomavirus infection N Engl J Med1992 327 1272ndash8
6 Woodman CB Collins S Winter H et al Natural history ofcervical human papillomavirus infection in young women alongitudinal cohort study Lancet 2001 357 1831ndash6
7 Boot HJ Wallenburg I de Melker HE et al Assessing theintroduction of universal human papillomavirus vaccinationfor preadolescent girls in The Netherlands Vaccine 2007 256245ndash56
8 van Lier EA Oomen PJ Oostenbrug MWM et alImmunization coverage National ImmunizationProgramme in the Netherlands Year of report 2009[Vaccinatiegraad Rijksvaccinatieprogramma NederlandVerslagjaar 2009] Bilthoven RIVM 2009
9 Zwakhals SLN van Lier EA van HPV (cohort 1997) bymunicipality 2012 [HPV (cohort 1997) per gemeente2012] In Dutch National Atlas of Public HealthBilthoven RIVM 2012 (httpwwwzorgatlasnlpreventievaccinaties-en-screeninghpv-cohort-1997-vaccinatiegraad-per-gemeente-2012 accessed 2 September 2013)
10 Brabin L Roberts SA Stretch R et al A survey of adolescentexperiences of human papillomavirus vaccination in theManchester study Br J cancer 2009 101 1502ndash4
11 Brabin L Roberts SA Kitchener HC A semi-qualitativestudy of attitudes to vaccinating adolescents against humanpapillomavirus without parental consent BMC PublicHealth 2007 7 20
12 Brewer NT Fazekas KI Predictors of HPV vaccine accept-ability A theory-informed systematic review Prev Med2007 45 107ndash14
13 Kahn JA Rosenthal SL Jin Y et al Rates of human papillo-mavirus vaccination attitudes about vaccination and humanpapillomavirus prevalence in young women Obstet Gynecol2008 111 1103ndash10
14 Askelson NM Campo S Lowe JB et al Using the theoryof planned behavior to predict mothersrsquo intentions to vaccin-ate their daughters against HPV J Sch Nurs 2010 26194ndash202
15 Ajzen I The theory of Planned Behavior Organ Behav HumDecis Process 1991 50 179ndash211
16 Becker MH The health belief model and personal healthbehavior Health Edu Monogr 1974 2 324ndash508
17 Chapman GB Coups EJ Emotions and preventive healthbehavior worry regret and influenza vaccination HealthPsychol 2006 25 82ndash90
18 Paulussen TG Hoekstra F Lanting CI et al Determinants ofDutch parentsrsquo decisions to vaccinate their child Vaccine2006 24 644ndash51
19 Kaplan KJ On the ambivalence-indifference problem inattitude theory and measurement A suggested modificationof the semantic differential technique Psychol Bull 1972 77361ndash372
20 Dormandy E Hankins M Marteau TM Attitudes and uptakeof a screening test The moderating role of ambivalencePsychol Health 2006 21 499ndash511
Predictors of HPV vaccination uptake
95
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
21 Hofman R van Empelen P Vogel I et al Parental decisionalstrategies regarding HPV vaccination prior to media debatesa focus-group study J Health Commun 2013 18 866ndash80
22 Brewer NT Gottlieb SL Reiter PL et al Longitudinal pre-dictors of human papillomavirus vaccine initiation amongadolescent girls in a high-risk geographic area Sex TransmDis 2011 38 197ndash204
23 Marlow LA Waller J Wardle J Trust and experience aspredictors of HPV vaccine acceptance Hum Vaccin 20073 171ndash5
24 Weinstein ND Perceived probability perceived severityand health-protective behavior Health Psychol 2000 1965ndash74
25 Marteau TM Dormandy E Michie S A measure of informedchoice Health Expect 2001 4 99ndash108
26 van den Berg M Timmermans DR Ten Kate LP et al Arepregnant women making informed choices about prenatalscreening Genet Med 2005 7 332ndash8
27 Tiro JA Diamond PM Perz CA et al Validation of scalesmeasuring attitudes and norms related to mammographyscreening in women veterans Health Psychol 2005 24555ndash66
28 Marlow LAV Waller J Wardle J Parental attitudes to pre-pubertal HPV vaccination Vaccine 2007 25 1945ndash52
29 Stalmeier PF Roosmalen MS Verhoef LC et al Thedecision evaluation scales Patient Educ Couns 2005 57286ndash93
30 Gilbert LA Hanson GR Perceptions of parental role respon-sibilities among working people Development of a compre-hensive measure J Marriage Fam 1983 45 203ndash12
31 Korfage IJ van Ballegooijen M Wauben B et al Informedchoice on Pap smear still limited by lack of knowledge on the
meaning of false-positive or false-negative test resultsPatient Educ Couns 2011 85 214ndash8
32 Thompson MM Zanna MP The conflicted individual per-sonality-based and domain specific antecedents of ambiva-lent social attitudes J Pers 1995 63 259ndash88
33 General Medical Council Seeking Patientsrsquo Consent TheEthical Considerations London GMC 1998
34 Minister of Health Letter about screening [Kaderbriefscreening] PGZP 2848440 Ministry of Health Welfareand Sports The Hague 2008
35 Aiken LS West RR Multiple Regression Testing andInterpreting Interactions Newbury Park CA Sage 1991
36 Krawczyk AL Perez S Lau E et al Human papillomavirusvaccination intentions and uptake in college women HealthPsychol 2012 31 685ndash93
37 Newby-Clark IR McGregor I Zanna MP Thinking andcaring about cognitive inconsistency when and for whomdoes attitudinal ambivalence feel uncomfortable J Pers SocPsychol 2002 82 157ndash66
38 Nordgren LF van Harreveld F van der Pligt J Ambivalencediscomfort and motivated information processing J ExperSoc Psychol 2006 42 252ndash8
39 Clark JK Wegener DT Fabrigar LR Attitudinal ambiva-lence and message-based persuasion motivated processingof proattitudinal information and avoidance of counterattitu-dinal information Pers Soc Psychol Bull 2008 34 565ndash77
40 van Keulen HM Otten W Ruiter RA et al Determinants ofHPV vaccination intentions among Dutch girls and theirmothers a cross-sectional study BMC Public Health 201313 111
R Hofman et al
96
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oronto Library on O
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nloaded from
Predictors of HPV vaccination uptake
Pearsonrsquos correlations showed that most associ-
ations between the predictors were positive
(Table II) Table III presents the results of the hier-
archical logistic regression analyses to predict
HPV vaccination uptake The first model in which
HPV vaccination uptake was regressed on demo-
graphic factors showed that uptake at follow-up
was significantly predicted by religion and the
year the decision about uptake was made (2011
versus 2010) (pseudo R2frac14 006) Specifically
those respondents without a religious affiliation
and those who had to decide in 2011 were more
likely to have their daughter vaccinated In Model
2a parent characteristics were added this model
explained an additional 29 variance HPV vaccin-
ation was more likely for parents with a higher edu-
cational level having no religious affiliation
decision about uptake in 2011 and higher trust in
the NIP and the vaccine In Model 2b (demographic
characteristics and social cognitive factors) signifi-
cant predictors were year of decision about uptake
(2011 versus 2010) a positive attitude toward HPV
vaccination social norm and anticipated regret and
worry about no uptake (pseudo R2frac14 053) In Model
3 (including all predictors except intention) vaccin-
ation was more likely for parents who had to decide
in 2011 ambivalence toward HPV vaccination
(under the condition that attitude is equal to 0) and
higher anticipated regret and worry about no uptake
The interaction term of attitude ambivalence was
also significant (pseudo R2frac14 057) In Model 4
(including all predictors) significant predictors of
uptake were the year the decision about uptake
was made (2011 versus 2010) a higher intention
ambivalence toward HPV vaccination (under the
condition that attitude is equal to 0) and the inter-
action term of attitude ambivalence
The significant interaction term attitude am-
bivalence showed that the predictive validity of at-
titude improved as scores of ambivalence increased
from low (bfrac14 089 Pfrac14 00238) to moderate
(bfrac14 144 Pfrac14 0001) and from moderate
(bfrac14 144 Pfrac14 0001) to high (bfrac14 198 Plt 0001)
Associations of HPV vaccination intention
Alternatively we performed an ordinal logistic re-
gression analysis with intention (instead of uptake)
as dependent variable (data not shown) This ana-
lysis showed that a higher intention was associated
with a positive attitude toward HPV vaccination
[odds ratio (OR) 1953 95 confidence interval
(CI) 1032ndash3693] (under the condition that am-
bivalence is frac140) ambivalence toward HPV vaccin-
ation (OR 239 95 CI 110ndash518) (under the
condition that attitude is frac140) trust in the vaccine
(OR 162 95 CI 116ndash227) anticipated regret
and worry about no uptake (OR 159 95 CI
Table I Continued
Total baseline
group (nfrac14 1725)
Subgroup that completed
follow-up assessment (nfrac14 793)
Characteristics Mean (SD) Mean (SD) P-value
If female abnormal Pap smear result 0103
Yes 185 (117) 98 (132)
No 1351 (856) 634 (853)
Never had a Pap smear taken 42 (27) 11 (15)
Daughter vaccinated against DPTPa and MMRb 0038
Yes 1654 (959) 778 (981)
Daughter vaccinated against HPV
Yes - 652 (831)
The subgroup that completed the follow-up assessment differed significantly from the baseline group on six characteristicsaDPTP refers to diphtheria pertussis tetanus and poliomyelitisbMMR refers to measles mumps and rubella
Predictors of HPV vaccination uptake
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Tab
leII
M
eans
standard
dev
iati
ons
(SD
)and
Pea
rsonrsquos
corr
elati
on
bet
wee
nth
epre
dic
tors
at
base
line
(nfrac14
793)
Mea
n(S
D)
12
34
56
78
910
11
12
1
Par
enta
lre
sponsi
bil
ity
45
0(0
46)
2
Tru
stin
NIP
48
6(0
67)
00
4
3
Tru
stin
vac
cine
43
1(0
92)
00
605
4
4
Per
ceiv
edsu
scep
tibil
ity
of
moth
erto
cerv
ical
cance
r
49
7(1
74)
00
500
100
2
5
Inte
nti
on
38
9(1
07)
00
304
8
07
3
00
5
6
Am
biv
alen
ce17
1(1
07)
00
7
02
0
02
6
00
1
02
9
7
Att
itude
tow
ard
HP
V
vac
cinat
ion
37
3(1
44)
00
9
05
1
07
7
00
508
4
03
3
8
Soci
alnorm
61
0(1
03
1)
01
5
03
3
05
1
00
706
1
01
8
06
4
9
Norm
ativ
ebel
ief
71
2(1
57)
00
501
9
03
3
00
103
3
00
9
03
4
03
7
10
Know
ledge
43
2(1
49)
00
9
01
0
00
300
300
3
00
700
200
3
00
3
11
Per
ceiv
edsu
scep
tibil
ity
of
dau
ghte
rif
vac
cinat
ed
toce
rvic
alca
nce
r
37
3(1
44)
00
6
02
3
03
0
04
1
02
6
00
3
03
1
02
3
02
3
00
1
12
Per
ceiv
edse
ver
ity
of
cerv
ical
cance
r
106
0(0
93)
02
5
00
400
500
300
500
400
600
700
9
01
2
00
1
13
Anti
cipat
edre
gre
tan
d
worr
yab
out
no
upta
ke
49
2(1
56)
02
3
03
8
06
2
01
1
06
9
01
9
07
1
05
3
03
6
00
6
02
3
02
0
Sm
all
effe
ctsi
ze
rgt
01
0
med
ium
effe
ctsi
ze
03
0lt
rlt
05
0
larg
eef
fect
size
rgt
05
0
Plt
00
5
Plt
00
1
R Hofman et al
90
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nloaded from
Tab
leII
IH
iera
rchic
al
logis
tic
regre
ssio
nanaly
ses
wit
hupta
ke(y
esn
o)
as
dep
enden
tva
riable
all
vari
able
sare
report
edby
pare
nts
at
base
line
Univ
aria
te
Model
1
(nfrac14
708)
Model
2a
(nfrac14
644)
Model
2b
(nfrac14
617)
Model
3
(nfrac14
572)
Model
4
(nfrac14
569)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
Dem
ogra
ph
icch
ara
cter
isti
cs
Age
of
par
ents
(yea
rs)
10
2(0
98ndash10
7)
10
1(0
96ndash10
6)
10
3(0
96ndash10
9)
10
2(0
95ndash11
0)
10
2(0
94ndash11
1)
10
1(0
93ndash10
9)
Educa
tional
level
11
5(1
00ndash13
4)
11
7(0
99ndash13
7)
12
5(1
00ndash15
4)
12
0(0
93ndash15
5)
12
7(0
96ndash17
0)
13
3(0
99ndash17
8)
No
reli
gio
us
affi
liat
ion
17
3(1
19ndash25
3)
16
3(1
09ndash24
2)
17
3(1
07ndash28
1)
11
2(0
63ndash20
0)
11
9(0
63ndash22
5)
11
6(0
60ndash22
3)
Dec
isio
nab
out
upta
ke
2011
(vs
2010)
20
8(1
28ndash33
6)
26
8(1
57ndash45
3)
26
9(1
42ndash51
0)
24
5(1
20ndash50
1)
24
8(1
11ndash55
2)
26
0(1
16ndash58
0)
Pare
nt
chara
cter
isti
cs
No
abnorm
alsm
ear
exper
ience
10
2(0
58ndash17
8)
09
4(0
45ndash19
5)
07
0(0
26ndash18
8)
06
8(0
24ndash19
5)
Par
enta
lre
sponsi
bil
ity
12
3(0
83ndash18
4)
15
3(0
91ndash25
9)
15
5(0
76ndash31
8)
18
6(0
90ndash38
3)
Tru
stin
NIP
35
4(2
61ndash48
1)
18
2(1
21ndash27
4)
14
0(0
86ndash23
0)
13
3(0
79ndash22
4)
Tru
stin
vac
cine
36
4(2
85ndash46
4)
34
1(2
49ndash46
8)
12
3(0
69ndash18
3)
09
9(0
59ndash16
7)
Per
ceiv
edsu
scep
tibil
ity
of
moth
erto
cerv
ical
cance
r
10
4(0
93ndash11
6)
10
3(0
88ndash12
1)
09
7(0
77ndash12
2)
09
6(0
76ndash12
2)
Soci
al
cogn
itiv
efa
ctors
Inte
nti
on
45
9(3
56ndash59
2)
26
1(1
47ndash46
1)
Am
biv
alen
ceto
war
dH
PV
vac
cinat
ion
08
2(0
69ndash09
2)
10
7(0
79ndash14
5)
02
7(0
08ndash08
7)
02
2(0
07ndash07
1)
Posi
tive
atti
tude
tow
ard
HP
Vvac
cinat
ion
57
3(4
26ndash77
1)
34
3(2
01ndash58
4)
17
0(0
69ndash42
1)
08
9(0
34ndash23
6)
Soci
alnorm
12
1(1
16ndash12
6)
10
7(1
01ndash11
3)
10
5(0
99ndash11
1)
10
3(0
97ndash10
9)
Norm
ativ
ebel
ief
14
4(1
28ndash16
3)
09
9(0
81ndash12
1)
10
3(0
83ndash12
9)
10
3(0
81ndash12
9)
Know
ledge
10
8(0
95ndash12
2)
09
5(0
87ndash10
4)
09
3(0
76ndash11
3)
09
5(0
78ndash11
7)
Per
ceiv
edsu
scep
tibil
ity
of
dau
ghte
rif
vac
cinat
ed
toce
rvic
alca
nce
r
06
5(0
57ndash07
4)
08
6(0
70ndash10
5)
08
9(0
69ndash11
4)
08
8(0
68ndash11
4)
Per
ceiv
edse
ver
ity
of
cerv
ical
cance
r
12
2(1
03ndash14
6)
10
8(0
81ndash14
2)
10
6(0
78ndash14
4)
10
8(0
79ndash14
8)
Anti
cipat
edre
gre
tan
d
worr
yab
out
no
upta
ke
22
3(1
93ndash25
8)
14
3(1
11ndash18
4)
14
3(1
08ndash18
9)
12
4(0
92ndash16
7)
Am
biv
alen
ce
atti
tude
inte
ract
ion
16
8(1
14ndash24
7)
17
9(1
22ndash26
2)
R2
00
603
505
305
705
9
Plt
00
5Plt
00
1an
dPlt
00
01
Predictors of HPV vaccination uptake
91
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nloaded from
132ndash192) and social norm (OR 107 95 CI
104ndash110) A lower uptake intention was asso-
ciated with a higher educational level (OR 083
95 CI 070ndash099) and a higher perceived parental
responsibility for their daughterrsquos health (OR 048
95 CI 030ndash075) The interaction term of atti-
tude ambivalence was significant (OR 073
95 CI 059ndash090)
Impact of time
Favorable changes in attitudes toward HPV uptake
over time were significantly related to an increase in
trust in the vaccine (OR 145 95 CI 136ndash153)
and social norm (OR 122 95 CI 115ndash128) over
time and a decrease in ambivalence toward HPV
vaccination (OR 094 95 CI 091ndash098) A de-
crease in ambivalence toward HPV vaccination
over time was significantly related to an increase
in feeling informed about HPV vaccination (OR
079 95 CI 069ndash091) and an increase in trust
in the vaccine (OR 088 95 CI 077ndash099) over
time
Informed decision making
Overall knowledge levels about the degreeduration
of protection were low at baseline and at follow-up
(33ndash43 correct answers) Percentages of correct
responses to five knowledge items increased signifi-
cantly at follow-up (Table IV) When five (out of
seven) correct items were defined as sufficient deci-
sion relevant knowledge then nfrac14 338 (439) of
the respondents made an informed choice about
uptake When four correct items were considered
sufficient then nfrac14 437 (657) of the respondents
made an informed choice about uptake (Table V)
Reasons for vaccinating or not
Main reasons as reported by parents at baseline to
have their daughter vaccinated include feeling re-
sponsible for her health (nfrac14 947 549) a family
history of cancer (nfrac14 128 74) anticipating
regret in case their daughter gets cervical cancer
(nfrac14 103 60) and other (nfrac14 547 317) Main
reasons as reported by parents at baseline not to have
their daughter vaccinated include that consequences
Table IV Knowledge items as completed by those who responded to the baseline and follow-up questionnaire (nfrac14 793)
Correct responses
Baseline
measurement
Follow-up
measurement
Significance level for
difference between
baseline and follow-up
n () n () P-value
Item (truefalse)
HPV causes cervical cancer (true) 496 (625) 479 (604) 0336
A condom protects 100 against HPV (false) 464 (585) 518 (653) 0001
The HPV vaccination will decrease the risk of cervical
cancer (true)
673 (849) 726 (916) lt0001
Vaccination in combination with having a smear taken is
more protective than only vaccination (true)
521 (657) 598 (754) lt0001
Item (multiple choice)
How is HPV transmitted (through blood oxygen sexual
contact)
699 (881) 730 (921) 0006
What is the protection rate of the HPV vaccine (55 70
85 100)
286 (361) 337 (425) 0005
What is the protection duration of a complete vaccination
against cervical cancer (at least 6 (8 at follow-up) years
at least 30 years lifetime)
289 (364) 262 (330) 0094
Correct answers are shaded
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nloaded from
of vaccinating are unpredictable (497 288) fear
of serious side-effects (nfrac14 401 232) and too
little information about the vaccine being available
(nfrac14 125 72)
Discussion
In this study among parents we assessed longitu-
dinal predictors of HPV vaccination uptake of their
daughters Uptake was predicted by intention a later
(2011) versus earlier (2010) decision about uptake
and anticipated regret and worry in case of abstain-
ing from HPV vaccination Ambivalence toward
HPV vaccination at baseline moderated the attitude
(baseline) uptake (follow-up) relationship with the
attitudendashuptake relationship being stronger at higher
ambivalence levels
HPV vaccination was most strongly predicted by
intention which fits the TPB model and was also
reported in an earlier study on predictors of HPV
vaccination uptake [22] In turn HPV vaccination
intention was positively associated with educational
level perceived parental responsibility for onersquos
daughterrsquos health trust in the vaccine the belief
that according to significant others their daughter
should be vaccinated and the motivation to comply
with that (social norm) and anticipated regret and
worry (which also predicted uptake) The relation-
ship found between intention and uptake and
between intention and social norm is consistent
with the TPB model and with another study [22]
which also confirms the association we found
between anticipated regretworry and uptake and
anticipated regretworry and intention The factors
lsquoperceived susceptibilityrsquo and lsquoseverityrsquo of cancer
of the HBM were not associated with intention or
uptake which confirms the results of an earlier study
[22 36]
A possible explanation for the positive effect on
uptake of having to decide later (2011) versus earlier
(2010) might be the amount of time that passed be-
tween the baseline questionnaire (2009) when an
intensive societal debate involving politics phys-
icians media parents and girls about HPV vaccin-
ation was ongoing and the actual decision about
uptake of vaccination In 2011 this debate probably
had less impact on the uptake decision than in 2010
Also after millions of girls worldwide had been
vaccinated and no serious side-effects had been
reported parents who had to decide later versus
earlier probably felt more reassured about the
vaccinersquos safety
This study shows that ambivalence moderated the
attitudendashuptake relationship Parents with a positive
attitude and a high level of ambivalence toward
HPV vaccination were more likely to have their
daughter vaccinated than parents with a positive at-
titude and a low level of ambivalence This finding
might be explained in two ways First ambivalence
is characterized as being subjectively uncomfortable
and people may be motivated to resolve the conflict-
ing evaluations that they hold [37] for example
by searching for information Second earlier
studies found that ambivalent people processed
pro-attitudinal messages to a greater extent than
counter-attitudinal messages probably because
pro-attitudinal messages are more likely to reduce
ambivalence [38 39] Taking these two mechanisms
together it is likely that in our study ambivalent
parents with a positive attitude toward HPV vaccin-
ation processed lsquopositiversquo messages about HPV vac-
cination to a greater extent than lsquonegativersquo messages
and were therefore more likely to have their
Table V Informed decision at follow-up (nfrac14 770)
Daughter
vaccinated
(nfrac14 640)
Daughter not
vaccinated
(nfrac14 130)
n () n ()
Positive attitude
Five or more correct items 280 (364) 14 (18)
Less than five correct items 246 (319) 16 (21)
Negative attitude
Five or more correct items 51 (66) 58 (75)
Less than five correct items 32 (42) 34 (44)
Knowledge was measured with seven items at follow-upInformed decision rate for cut-off at three correct items761 [(504 + 82)770] four correct items 657[(437 + 69)770] five correct items 439 [(280 + 58)770]six correct items 187 [(117 + 27)770] Due to missingitems analyses were based on nfrac14 770 respondents instead ofnfrac14 793 Informed choice (as defined) is shaded
Predictors of HPV vaccination uptake
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nloaded from
daughter vaccinated In other words parents who
had both positive attitudes and were ambivalent to-
ward HPV vaccination became even more positive
because they elaborated only information in favor of
HPV vaccination This may imply that this lsquobiasedrsquo
information processing has a negative impact on
informed decision making although parents will
have gained more knowledge during their efforts
to resolve their ambivalence
Assessing decisional factors related to HPV vac-
cination both before and after the decision-making
process about uptake provided a unique opportun-
ity to determine changes in those factors over time
As uptake was predicted by intention and intention
was highly correlated with attitude (rfrac14 084) (at
baseline) we think it is relevant to show which
factors are important for changes in attitude over
time Our results show that a more positive attitude
toward HPV vaccination over time was associated
with an increase in trust in the vaccine and in
social norm over time and a decrease in ambiva-
lence toward HPV vaccination over time This
latter factor was related to an increase in feeling
informed about HPV vaccination and an increase
in trust in the vaccine over time In summary over
time parents felt better informed became less am-
bivalent and had more trust in the vaccine These
results are in accordance with our finding that
girls who had to decide with their parents whether
or not to be vaccinated in 2011 were more likely
to be vaccinated than those who had to decide
in 2010
An important finding is that knowledge about the
duration of protection was low at both baseline and
follow-up For instance about 65 of the parents
thought that protection lasts 30 years or even life-
long As the duration of protection is still unknown
it is important that parents and girls know that
booster vaccinations might be needed in the future
When we applied a cut-off of four or five correct
knowledge items (out of seven) then the rates
of informed choice about uptake were not high
66 and 44 respectively However this finding
should be interpreted with caution because the
time period between the assessment of knowledge
and the last vaccination out of three shots was
1 month (decision in 2011) or 14 months (decision
in 2010) In educational material it should be clearly
stated what is known and not yet known about HPV
vaccination
Study strengths include the longitudinal design
as recommended by authors of a cross-sectional
study [40] the high (absolute) number of respond-
ents of the baseline (nfrac14 1725) and follow-up ques-
tionnaires (nfrac14 793) and the high response rate of the
follow-up questionnaire (74)
Limitations
A limitation was the low response rate of the base-
line questionnaire (30) which might be due to the
length of the questionnaire Our sample may there-
fore not be representative of the general population
as few parents had a low educational level Also
demographic characteristics of the follow-up group
were slightly different from those of the baseline
group with more parents being better educated
and well-off at follow-up These parents might pos-
sibly be more likely than those in the wider popula-
tion to seek to reduce high ambivalence by
searching information allowing them to respond
positively to the vaccine invitationmdashrather than do
nothing
Conclusion
In conclusion this study shows that intention a later
versus earlier decision about uptake and anticipated
regretworry about abstaining from vaccination
were predictors of uptake Anticipated regret was a
common predictor of intention and uptake and thus
an important factor in the decision-making process
about HPV vaccination In turn predictors of inten-
tion like social norm and trust in the vaccine are
also important when deciding about HPV vaccin-
ation Over time parents felt better informed
became less ambivalent and had more trust in the
vaccine
Practice implications
This study shows the usefulness of including affect-
ive factors in studies examining HPV vaccination
R Hofman et al
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nloaded from
behavior as anticipated regret trust in the vaccine
and ambivalence were found to play a role in the
decision making about uptake However it is also
important that parents are enabled to base their
decision about HPV vaccination of their daughter
on decision relevant knowledge As these results
suggest that people need sufficient time to decide
about the uptake of a new vaccine we recommend
a well-balanced stepwise process of implementa-
tion that is let parents first become aware of the
link between HPV and cervical cancer then provide
them with balanced information about all the
knowns and also the unknowns of HPV vaccination
and then finally offer them the opportunity to have
their daughter vaccinated As two-third of parents
wrongly thought that protection lasts 30 years or
even lifelong educational material should clearly
state that booster vaccinations might be needed in
the future
Acknowledgements
The authors thank the Dutch Cancer Society for
financial support and the participants for their
contribution to the study
Funding
The Dutch Cancer Society [EMCR 2008-3992
EMCR 2009-4561]
Conflict of interest statement
None declared
References
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2 Bosch FX Lorincz A Munoz N et al The causal relationbetween human papillomavirus and cervical cancer J ClinPathol 2002 55 244ndash65
3 Walboomers JM Jacobs MV Manos MM et al Humanpapillomavirus is a necessary cause of invasive cervicalcancer worldwide J Pathol 1999 189 12ndash9
4 Munoz N Bosch FX Castellsague X et al Against whichhuman papillomavirus types shall we vaccinate and screenThe international perspective Int J Cancer 2004 111278ndash85
5 Koutsky LA Holmes KK Critchlow CW et al A cohortstudy of the risk of cervical intraepithelial neoplasia grade2 or 3 in relation to papillomavirus infection N Engl J Med1992 327 1272ndash8
6 Woodman CB Collins S Winter H et al Natural history ofcervical human papillomavirus infection in young women alongitudinal cohort study Lancet 2001 357 1831ndash6
7 Boot HJ Wallenburg I de Melker HE et al Assessing theintroduction of universal human papillomavirus vaccinationfor preadolescent girls in The Netherlands Vaccine 2007 256245ndash56
8 van Lier EA Oomen PJ Oostenbrug MWM et alImmunization coverage National ImmunizationProgramme in the Netherlands Year of report 2009[Vaccinatiegraad Rijksvaccinatieprogramma NederlandVerslagjaar 2009] Bilthoven RIVM 2009
9 Zwakhals SLN van Lier EA van HPV (cohort 1997) bymunicipality 2012 [HPV (cohort 1997) per gemeente2012] In Dutch National Atlas of Public HealthBilthoven RIVM 2012 (httpwwwzorgatlasnlpreventievaccinaties-en-screeninghpv-cohort-1997-vaccinatiegraad-per-gemeente-2012 accessed 2 September 2013)
10 Brabin L Roberts SA Stretch R et al A survey of adolescentexperiences of human papillomavirus vaccination in theManchester study Br J cancer 2009 101 1502ndash4
11 Brabin L Roberts SA Kitchener HC A semi-qualitativestudy of attitudes to vaccinating adolescents against humanpapillomavirus without parental consent BMC PublicHealth 2007 7 20
12 Brewer NT Fazekas KI Predictors of HPV vaccine accept-ability A theory-informed systematic review Prev Med2007 45 107ndash14
13 Kahn JA Rosenthal SL Jin Y et al Rates of human papillo-mavirus vaccination attitudes about vaccination and humanpapillomavirus prevalence in young women Obstet Gynecol2008 111 1103ndash10
14 Askelson NM Campo S Lowe JB et al Using the theoryof planned behavior to predict mothersrsquo intentions to vaccin-ate their daughters against HPV J Sch Nurs 2010 26194ndash202
15 Ajzen I The theory of Planned Behavior Organ Behav HumDecis Process 1991 50 179ndash211
16 Becker MH The health belief model and personal healthbehavior Health Edu Monogr 1974 2 324ndash508
17 Chapman GB Coups EJ Emotions and preventive healthbehavior worry regret and influenza vaccination HealthPsychol 2006 25 82ndash90
18 Paulussen TG Hoekstra F Lanting CI et al Determinants ofDutch parentsrsquo decisions to vaccinate their child Vaccine2006 24 644ndash51
19 Kaplan KJ On the ambivalence-indifference problem inattitude theory and measurement A suggested modificationof the semantic differential technique Psychol Bull 1972 77361ndash372
20 Dormandy E Hankins M Marteau TM Attitudes and uptakeof a screening test The moderating role of ambivalencePsychol Health 2006 21 499ndash511
Predictors of HPV vaccination uptake
95
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
21 Hofman R van Empelen P Vogel I et al Parental decisionalstrategies regarding HPV vaccination prior to media debatesa focus-group study J Health Commun 2013 18 866ndash80
22 Brewer NT Gottlieb SL Reiter PL et al Longitudinal pre-dictors of human papillomavirus vaccine initiation amongadolescent girls in a high-risk geographic area Sex TransmDis 2011 38 197ndash204
23 Marlow LA Waller J Wardle J Trust and experience aspredictors of HPV vaccine acceptance Hum Vaccin 20073 171ndash5
24 Weinstein ND Perceived probability perceived severityand health-protective behavior Health Psychol 2000 1965ndash74
25 Marteau TM Dormandy E Michie S A measure of informedchoice Health Expect 2001 4 99ndash108
26 van den Berg M Timmermans DR Ten Kate LP et al Arepregnant women making informed choices about prenatalscreening Genet Med 2005 7 332ndash8
27 Tiro JA Diamond PM Perz CA et al Validation of scalesmeasuring attitudes and norms related to mammographyscreening in women veterans Health Psychol 2005 24555ndash66
28 Marlow LAV Waller J Wardle J Parental attitudes to pre-pubertal HPV vaccination Vaccine 2007 25 1945ndash52
29 Stalmeier PF Roosmalen MS Verhoef LC et al Thedecision evaluation scales Patient Educ Couns 2005 57286ndash93
30 Gilbert LA Hanson GR Perceptions of parental role respon-sibilities among working people Development of a compre-hensive measure J Marriage Fam 1983 45 203ndash12
31 Korfage IJ van Ballegooijen M Wauben B et al Informedchoice on Pap smear still limited by lack of knowledge on the
meaning of false-positive or false-negative test resultsPatient Educ Couns 2011 85 214ndash8
32 Thompson MM Zanna MP The conflicted individual per-sonality-based and domain specific antecedents of ambiva-lent social attitudes J Pers 1995 63 259ndash88
33 General Medical Council Seeking Patientsrsquo Consent TheEthical Considerations London GMC 1998
34 Minister of Health Letter about screening [Kaderbriefscreening] PGZP 2848440 Ministry of Health Welfareand Sports The Hague 2008
35 Aiken LS West RR Multiple Regression Testing andInterpreting Interactions Newbury Park CA Sage 1991
36 Krawczyk AL Perez S Lau E et al Human papillomavirusvaccination intentions and uptake in college women HealthPsychol 2012 31 685ndash93
37 Newby-Clark IR McGregor I Zanna MP Thinking andcaring about cognitive inconsistency when and for whomdoes attitudinal ambivalence feel uncomfortable J Pers SocPsychol 2002 82 157ndash66
38 Nordgren LF van Harreveld F van der Pligt J Ambivalencediscomfort and motivated information processing J ExperSoc Psychol 2006 42 252ndash8
39 Clark JK Wegener DT Fabrigar LR Attitudinal ambiva-lence and message-based persuasion motivated processingof proattitudinal information and avoidance of counterattitu-dinal information Pers Soc Psychol Bull 2008 34 565ndash77
40 van Keulen HM Otten W Ruiter RA et al Determinants ofHPV vaccination intentions among Dutch girls and theirmothers a cross-sectional study BMC Public Health 201313 111
R Hofman et al
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Tab
leII
M
eans
standard
dev
iati
ons
(SD
)and
Pea
rsonrsquos
corr
elati
on
bet
wee
nth
epre
dic
tors
at
base
line
(nfrac14
793)
Mea
n(S
D)
12
34
56
78
910
11
12
1
Par
enta
lre
sponsi
bil
ity
45
0(0
46)
2
Tru
stin
NIP
48
6(0
67)
00
4
3
Tru
stin
vac
cine
43
1(0
92)
00
605
4
4
Per
ceiv
edsu
scep
tibil
ity
of
moth
erto
cerv
ical
cance
r
49
7(1
74)
00
500
100
2
5
Inte
nti
on
38
9(1
07)
00
304
8
07
3
00
5
6
Am
biv
alen
ce17
1(1
07)
00
7
02
0
02
6
00
1
02
9
7
Att
itude
tow
ard
HP
V
vac
cinat
ion
37
3(1
44)
00
9
05
1
07
7
00
508
4
03
3
8
Soci
alnorm
61
0(1
03
1)
01
5
03
3
05
1
00
706
1
01
8
06
4
9
Norm
ativ
ebel
ief
71
2(1
57)
00
501
9
03
3
00
103
3
00
9
03
4
03
7
10
Know
ledge
43
2(1
49)
00
9
01
0
00
300
300
3
00
700
200
3
00
3
11
Per
ceiv
edsu
scep
tibil
ity
of
dau
ghte
rif
vac
cinat
ed
toce
rvic
alca
nce
r
37
3(1
44)
00
6
02
3
03
0
04
1
02
6
00
3
03
1
02
3
02
3
00
1
12
Per
ceiv
edse
ver
ity
of
cerv
ical
cance
r
106
0(0
93)
02
5
00
400
500
300
500
400
600
700
9
01
2
00
1
13
Anti
cipat
edre
gre
tan
d
worr
yab
out
no
upta
ke
49
2(1
56)
02
3
03
8
06
2
01
1
06
9
01
9
07
1
05
3
03
6
00
6
02
3
02
0
Sm
all
effe
ctsi
ze
rgt
01
0
med
ium
effe
ctsi
ze
03
0lt
rlt
05
0
larg
eef
fect
size
rgt
05
0
Plt
00
5
Plt
00
1
R Hofman et al
90
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Dow
nloaded from
Tab
leII
IH
iera
rchic
al
logis
tic
regre
ssio
nanaly
ses
wit
hupta
ke(y
esn
o)
as
dep
enden
tva
riable
all
vari
able
sare
report
edby
pare
nts
at
base
line
Univ
aria
te
Model
1
(nfrac14
708)
Model
2a
(nfrac14
644)
Model
2b
(nfrac14
617)
Model
3
(nfrac14
572)
Model
4
(nfrac14
569)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
Dem
ogra
ph
icch
ara
cter
isti
cs
Age
of
par
ents
(yea
rs)
10
2(0
98ndash10
7)
10
1(0
96ndash10
6)
10
3(0
96ndash10
9)
10
2(0
95ndash11
0)
10
2(0
94ndash11
1)
10
1(0
93ndash10
9)
Educa
tional
level
11
5(1
00ndash13
4)
11
7(0
99ndash13
7)
12
5(1
00ndash15
4)
12
0(0
93ndash15
5)
12
7(0
96ndash17
0)
13
3(0
99ndash17
8)
No
reli
gio
us
affi
liat
ion
17
3(1
19ndash25
3)
16
3(1
09ndash24
2)
17
3(1
07ndash28
1)
11
2(0
63ndash20
0)
11
9(0
63ndash22
5)
11
6(0
60ndash22
3)
Dec
isio
nab
out
upta
ke
2011
(vs
2010)
20
8(1
28ndash33
6)
26
8(1
57ndash45
3)
26
9(1
42ndash51
0)
24
5(1
20ndash50
1)
24
8(1
11ndash55
2)
26
0(1
16ndash58
0)
Pare
nt
chara
cter
isti
cs
No
abnorm
alsm
ear
exper
ience
10
2(0
58ndash17
8)
09
4(0
45ndash19
5)
07
0(0
26ndash18
8)
06
8(0
24ndash19
5)
Par
enta
lre
sponsi
bil
ity
12
3(0
83ndash18
4)
15
3(0
91ndash25
9)
15
5(0
76ndash31
8)
18
6(0
90ndash38
3)
Tru
stin
NIP
35
4(2
61ndash48
1)
18
2(1
21ndash27
4)
14
0(0
86ndash23
0)
13
3(0
79ndash22
4)
Tru
stin
vac
cine
36
4(2
85ndash46
4)
34
1(2
49ndash46
8)
12
3(0
69ndash18
3)
09
9(0
59ndash16
7)
Per
ceiv
edsu
scep
tibil
ity
of
moth
erto
cerv
ical
cance
r
10
4(0
93ndash11
6)
10
3(0
88ndash12
1)
09
7(0
77ndash12
2)
09
6(0
76ndash12
2)
Soci
al
cogn
itiv
efa
ctors
Inte
nti
on
45
9(3
56ndash59
2)
26
1(1
47ndash46
1)
Am
biv
alen
ceto
war
dH
PV
vac
cinat
ion
08
2(0
69ndash09
2)
10
7(0
79ndash14
5)
02
7(0
08ndash08
7)
02
2(0
07ndash07
1)
Posi
tive
atti
tude
tow
ard
HP
Vvac
cinat
ion
57
3(4
26ndash77
1)
34
3(2
01ndash58
4)
17
0(0
69ndash42
1)
08
9(0
34ndash23
6)
Soci
alnorm
12
1(1
16ndash12
6)
10
7(1
01ndash11
3)
10
5(0
99ndash11
1)
10
3(0
97ndash10
9)
Norm
ativ
ebel
ief
14
4(1
28ndash16
3)
09
9(0
81ndash12
1)
10
3(0
83ndash12
9)
10
3(0
81ndash12
9)
Know
ledge
10
8(0
95ndash12
2)
09
5(0
87ndash10
4)
09
3(0
76ndash11
3)
09
5(0
78ndash11
7)
Per
ceiv
edsu
scep
tibil
ity
of
dau
ghte
rif
vac
cinat
ed
toce
rvic
alca
nce
r
06
5(0
57ndash07
4)
08
6(0
70ndash10
5)
08
9(0
69ndash11
4)
08
8(0
68ndash11
4)
Per
ceiv
edse
ver
ity
of
cerv
ical
cance
r
12
2(1
03ndash14
6)
10
8(0
81ndash14
2)
10
6(0
78ndash14
4)
10
8(0
79ndash14
8)
Anti
cipat
edre
gre
tan
d
worr
yab
out
no
upta
ke
22
3(1
93ndash25
8)
14
3(1
11ndash18
4)
14
3(1
08ndash18
9)
12
4(0
92ndash16
7)
Am
biv
alen
ce
atti
tude
inte
ract
ion
16
8(1
14ndash24
7)
17
9(1
22ndash26
2)
R2
00
603
505
305
705
9
Plt
00
5Plt
00
1an
dPlt
00
01
Predictors of HPV vaccination uptake
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nloaded from
132ndash192) and social norm (OR 107 95 CI
104ndash110) A lower uptake intention was asso-
ciated with a higher educational level (OR 083
95 CI 070ndash099) and a higher perceived parental
responsibility for their daughterrsquos health (OR 048
95 CI 030ndash075) The interaction term of atti-
tude ambivalence was significant (OR 073
95 CI 059ndash090)
Impact of time
Favorable changes in attitudes toward HPV uptake
over time were significantly related to an increase in
trust in the vaccine (OR 145 95 CI 136ndash153)
and social norm (OR 122 95 CI 115ndash128) over
time and a decrease in ambivalence toward HPV
vaccination (OR 094 95 CI 091ndash098) A de-
crease in ambivalence toward HPV vaccination
over time was significantly related to an increase
in feeling informed about HPV vaccination (OR
079 95 CI 069ndash091) and an increase in trust
in the vaccine (OR 088 95 CI 077ndash099) over
time
Informed decision making
Overall knowledge levels about the degreeduration
of protection were low at baseline and at follow-up
(33ndash43 correct answers) Percentages of correct
responses to five knowledge items increased signifi-
cantly at follow-up (Table IV) When five (out of
seven) correct items were defined as sufficient deci-
sion relevant knowledge then nfrac14 338 (439) of
the respondents made an informed choice about
uptake When four correct items were considered
sufficient then nfrac14 437 (657) of the respondents
made an informed choice about uptake (Table V)
Reasons for vaccinating or not
Main reasons as reported by parents at baseline to
have their daughter vaccinated include feeling re-
sponsible for her health (nfrac14 947 549) a family
history of cancer (nfrac14 128 74) anticipating
regret in case their daughter gets cervical cancer
(nfrac14 103 60) and other (nfrac14 547 317) Main
reasons as reported by parents at baseline not to have
their daughter vaccinated include that consequences
Table IV Knowledge items as completed by those who responded to the baseline and follow-up questionnaire (nfrac14 793)
Correct responses
Baseline
measurement
Follow-up
measurement
Significance level for
difference between
baseline and follow-up
n () n () P-value
Item (truefalse)
HPV causes cervical cancer (true) 496 (625) 479 (604) 0336
A condom protects 100 against HPV (false) 464 (585) 518 (653) 0001
The HPV vaccination will decrease the risk of cervical
cancer (true)
673 (849) 726 (916) lt0001
Vaccination in combination with having a smear taken is
more protective than only vaccination (true)
521 (657) 598 (754) lt0001
Item (multiple choice)
How is HPV transmitted (through blood oxygen sexual
contact)
699 (881) 730 (921) 0006
What is the protection rate of the HPV vaccine (55 70
85 100)
286 (361) 337 (425) 0005
What is the protection duration of a complete vaccination
against cervical cancer (at least 6 (8 at follow-up) years
at least 30 years lifetime)
289 (364) 262 (330) 0094
Correct answers are shaded
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nloaded from
of vaccinating are unpredictable (497 288) fear
of serious side-effects (nfrac14 401 232) and too
little information about the vaccine being available
(nfrac14 125 72)
Discussion
In this study among parents we assessed longitu-
dinal predictors of HPV vaccination uptake of their
daughters Uptake was predicted by intention a later
(2011) versus earlier (2010) decision about uptake
and anticipated regret and worry in case of abstain-
ing from HPV vaccination Ambivalence toward
HPV vaccination at baseline moderated the attitude
(baseline) uptake (follow-up) relationship with the
attitudendashuptake relationship being stronger at higher
ambivalence levels
HPV vaccination was most strongly predicted by
intention which fits the TPB model and was also
reported in an earlier study on predictors of HPV
vaccination uptake [22] In turn HPV vaccination
intention was positively associated with educational
level perceived parental responsibility for onersquos
daughterrsquos health trust in the vaccine the belief
that according to significant others their daughter
should be vaccinated and the motivation to comply
with that (social norm) and anticipated regret and
worry (which also predicted uptake) The relation-
ship found between intention and uptake and
between intention and social norm is consistent
with the TPB model and with another study [22]
which also confirms the association we found
between anticipated regretworry and uptake and
anticipated regretworry and intention The factors
lsquoperceived susceptibilityrsquo and lsquoseverityrsquo of cancer
of the HBM were not associated with intention or
uptake which confirms the results of an earlier study
[22 36]
A possible explanation for the positive effect on
uptake of having to decide later (2011) versus earlier
(2010) might be the amount of time that passed be-
tween the baseline questionnaire (2009) when an
intensive societal debate involving politics phys-
icians media parents and girls about HPV vaccin-
ation was ongoing and the actual decision about
uptake of vaccination In 2011 this debate probably
had less impact on the uptake decision than in 2010
Also after millions of girls worldwide had been
vaccinated and no serious side-effects had been
reported parents who had to decide later versus
earlier probably felt more reassured about the
vaccinersquos safety
This study shows that ambivalence moderated the
attitudendashuptake relationship Parents with a positive
attitude and a high level of ambivalence toward
HPV vaccination were more likely to have their
daughter vaccinated than parents with a positive at-
titude and a low level of ambivalence This finding
might be explained in two ways First ambivalence
is characterized as being subjectively uncomfortable
and people may be motivated to resolve the conflict-
ing evaluations that they hold [37] for example
by searching for information Second earlier
studies found that ambivalent people processed
pro-attitudinal messages to a greater extent than
counter-attitudinal messages probably because
pro-attitudinal messages are more likely to reduce
ambivalence [38 39] Taking these two mechanisms
together it is likely that in our study ambivalent
parents with a positive attitude toward HPV vaccin-
ation processed lsquopositiversquo messages about HPV vac-
cination to a greater extent than lsquonegativersquo messages
and were therefore more likely to have their
Table V Informed decision at follow-up (nfrac14 770)
Daughter
vaccinated
(nfrac14 640)
Daughter not
vaccinated
(nfrac14 130)
n () n ()
Positive attitude
Five or more correct items 280 (364) 14 (18)
Less than five correct items 246 (319) 16 (21)
Negative attitude
Five or more correct items 51 (66) 58 (75)
Less than five correct items 32 (42) 34 (44)
Knowledge was measured with seven items at follow-upInformed decision rate for cut-off at three correct items761 [(504 + 82)770] four correct items 657[(437 + 69)770] five correct items 439 [(280 + 58)770]six correct items 187 [(117 + 27)770] Due to missingitems analyses were based on nfrac14 770 respondents instead ofnfrac14 793 Informed choice (as defined) is shaded
Predictors of HPV vaccination uptake
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nloaded from
daughter vaccinated In other words parents who
had both positive attitudes and were ambivalent to-
ward HPV vaccination became even more positive
because they elaborated only information in favor of
HPV vaccination This may imply that this lsquobiasedrsquo
information processing has a negative impact on
informed decision making although parents will
have gained more knowledge during their efforts
to resolve their ambivalence
Assessing decisional factors related to HPV vac-
cination both before and after the decision-making
process about uptake provided a unique opportun-
ity to determine changes in those factors over time
As uptake was predicted by intention and intention
was highly correlated with attitude (rfrac14 084) (at
baseline) we think it is relevant to show which
factors are important for changes in attitude over
time Our results show that a more positive attitude
toward HPV vaccination over time was associated
with an increase in trust in the vaccine and in
social norm over time and a decrease in ambiva-
lence toward HPV vaccination over time This
latter factor was related to an increase in feeling
informed about HPV vaccination and an increase
in trust in the vaccine over time In summary over
time parents felt better informed became less am-
bivalent and had more trust in the vaccine These
results are in accordance with our finding that
girls who had to decide with their parents whether
or not to be vaccinated in 2011 were more likely
to be vaccinated than those who had to decide
in 2010
An important finding is that knowledge about the
duration of protection was low at both baseline and
follow-up For instance about 65 of the parents
thought that protection lasts 30 years or even life-
long As the duration of protection is still unknown
it is important that parents and girls know that
booster vaccinations might be needed in the future
When we applied a cut-off of four or five correct
knowledge items (out of seven) then the rates
of informed choice about uptake were not high
66 and 44 respectively However this finding
should be interpreted with caution because the
time period between the assessment of knowledge
and the last vaccination out of three shots was
1 month (decision in 2011) or 14 months (decision
in 2010) In educational material it should be clearly
stated what is known and not yet known about HPV
vaccination
Study strengths include the longitudinal design
as recommended by authors of a cross-sectional
study [40] the high (absolute) number of respond-
ents of the baseline (nfrac14 1725) and follow-up ques-
tionnaires (nfrac14 793) and the high response rate of the
follow-up questionnaire (74)
Limitations
A limitation was the low response rate of the base-
line questionnaire (30) which might be due to the
length of the questionnaire Our sample may there-
fore not be representative of the general population
as few parents had a low educational level Also
demographic characteristics of the follow-up group
were slightly different from those of the baseline
group with more parents being better educated
and well-off at follow-up These parents might pos-
sibly be more likely than those in the wider popula-
tion to seek to reduce high ambivalence by
searching information allowing them to respond
positively to the vaccine invitationmdashrather than do
nothing
Conclusion
In conclusion this study shows that intention a later
versus earlier decision about uptake and anticipated
regretworry about abstaining from vaccination
were predictors of uptake Anticipated regret was a
common predictor of intention and uptake and thus
an important factor in the decision-making process
about HPV vaccination In turn predictors of inten-
tion like social norm and trust in the vaccine are
also important when deciding about HPV vaccin-
ation Over time parents felt better informed
became less ambivalent and had more trust in the
vaccine
Practice implications
This study shows the usefulness of including affect-
ive factors in studies examining HPV vaccination
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nloaded from
behavior as anticipated regret trust in the vaccine
and ambivalence were found to play a role in the
decision making about uptake However it is also
important that parents are enabled to base their
decision about HPV vaccination of their daughter
on decision relevant knowledge As these results
suggest that people need sufficient time to decide
about the uptake of a new vaccine we recommend
a well-balanced stepwise process of implementa-
tion that is let parents first become aware of the
link between HPV and cervical cancer then provide
them with balanced information about all the
knowns and also the unknowns of HPV vaccination
and then finally offer them the opportunity to have
their daughter vaccinated As two-third of parents
wrongly thought that protection lasts 30 years or
even lifelong educational material should clearly
state that booster vaccinations might be needed in
the future
Acknowledgements
The authors thank the Dutch Cancer Society for
financial support and the participants for their
contribution to the study
Funding
The Dutch Cancer Society [EMCR 2008-3992
EMCR 2009-4561]
Conflict of interest statement
None declared
References
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2 Bosch FX Lorincz A Munoz N et al The causal relationbetween human papillomavirus and cervical cancer J ClinPathol 2002 55 244ndash65
3 Walboomers JM Jacobs MV Manos MM et al Humanpapillomavirus is a necessary cause of invasive cervicalcancer worldwide J Pathol 1999 189 12ndash9
4 Munoz N Bosch FX Castellsague X et al Against whichhuman papillomavirus types shall we vaccinate and screenThe international perspective Int J Cancer 2004 111278ndash85
5 Koutsky LA Holmes KK Critchlow CW et al A cohortstudy of the risk of cervical intraepithelial neoplasia grade2 or 3 in relation to papillomavirus infection N Engl J Med1992 327 1272ndash8
6 Woodman CB Collins S Winter H et al Natural history ofcervical human papillomavirus infection in young women alongitudinal cohort study Lancet 2001 357 1831ndash6
7 Boot HJ Wallenburg I de Melker HE et al Assessing theintroduction of universal human papillomavirus vaccinationfor preadolescent girls in The Netherlands Vaccine 2007 256245ndash56
8 van Lier EA Oomen PJ Oostenbrug MWM et alImmunization coverage National ImmunizationProgramme in the Netherlands Year of report 2009[Vaccinatiegraad Rijksvaccinatieprogramma NederlandVerslagjaar 2009] Bilthoven RIVM 2009
9 Zwakhals SLN van Lier EA van HPV (cohort 1997) bymunicipality 2012 [HPV (cohort 1997) per gemeente2012] In Dutch National Atlas of Public HealthBilthoven RIVM 2012 (httpwwwzorgatlasnlpreventievaccinaties-en-screeninghpv-cohort-1997-vaccinatiegraad-per-gemeente-2012 accessed 2 September 2013)
10 Brabin L Roberts SA Stretch R et al A survey of adolescentexperiences of human papillomavirus vaccination in theManchester study Br J cancer 2009 101 1502ndash4
11 Brabin L Roberts SA Kitchener HC A semi-qualitativestudy of attitudes to vaccinating adolescents against humanpapillomavirus without parental consent BMC PublicHealth 2007 7 20
12 Brewer NT Fazekas KI Predictors of HPV vaccine accept-ability A theory-informed systematic review Prev Med2007 45 107ndash14
13 Kahn JA Rosenthal SL Jin Y et al Rates of human papillo-mavirus vaccination attitudes about vaccination and humanpapillomavirus prevalence in young women Obstet Gynecol2008 111 1103ndash10
14 Askelson NM Campo S Lowe JB et al Using the theoryof planned behavior to predict mothersrsquo intentions to vaccin-ate their daughters against HPV J Sch Nurs 2010 26194ndash202
15 Ajzen I The theory of Planned Behavior Organ Behav HumDecis Process 1991 50 179ndash211
16 Becker MH The health belief model and personal healthbehavior Health Edu Monogr 1974 2 324ndash508
17 Chapman GB Coups EJ Emotions and preventive healthbehavior worry regret and influenza vaccination HealthPsychol 2006 25 82ndash90
18 Paulussen TG Hoekstra F Lanting CI et al Determinants ofDutch parentsrsquo decisions to vaccinate their child Vaccine2006 24 644ndash51
19 Kaplan KJ On the ambivalence-indifference problem inattitude theory and measurement A suggested modificationof the semantic differential technique Psychol Bull 1972 77361ndash372
20 Dormandy E Hankins M Marteau TM Attitudes and uptakeof a screening test The moderating role of ambivalencePsychol Health 2006 21 499ndash511
Predictors of HPV vaccination uptake
95
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
21 Hofman R van Empelen P Vogel I et al Parental decisionalstrategies regarding HPV vaccination prior to media debatesa focus-group study J Health Commun 2013 18 866ndash80
22 Brewer NT Gottlieb SL Reiter PL et al Longitudinal pre-dictors of human papillomavirus vaccine initiation amongadolescent girls in a high-risk geographic area Sex TransmDis 2011 38 197ndash204
23 Marlow LA Waller J Wardle J Trust and experience aspredictors of HPV vaccine acceptance Hum Vaccin 20073 171ndash5
24 Weinstein ND Perceived probability perceived severityand health-protective behavior Health Psychol 2000 1965ndash74
25 Marteau TM Dormandy E Michie S A measure of informedchoice Health Expect 2001 4 99ndash108
26 van den Berg M Timmermans DR Ten Kate LP et al Arepregnant women making informed choices about prenatalscreening Genet Med 2005 7 332ndash8
27 Tiro JA Diamond PM Perz CA et al Validation of scalesmeasuring attitudes and norms related to mammographyscreening in women veterans Health Psychol 2005 24555ndash66
28 Marlow LAV Waller J Wardle J Parental attitudes to pre-pubertal HPV vaccination Vaccine 2007 25 1945ndash52
29 Stalmeier PF Roosmalen MS Verhoef LC et al Thedecision evaluation scales Patient Educ Couns 2005 57286ndash93
30 Gilbert LA Hanson GR Perceptions of parental role respon-sibilities among working people Development of a compre-hensive measure J Marriage Fam 1983 45 203ndash12
31 Korfage IJ van Ballegooijen M Wauben B et al Informedchoice on Pap smear still limited by lack of knowledge on the
meaning of false-positive or false-negative test resultsPatient Educ Couns 2011 85 214ndash8
32 Thompson MM Zanna MP The conflicted individual per-sonality-based and domain specific antecedents of ambiva-lent social attitudes J Pers 1995 63 259ndash88
33 General Medical Council Seeking Patientsrsquo Consent TheEthical Considerations London GMC 1998
34 Minister of Health Letter about screening [Kaderbriefscreening] PGZP 2848440 Ministry of Health Welfareand Sports The Hague 2008
35 Aiken LS West RR Multiple Regression Testing andInterpreting Interactions Newbury Park CA Sage 1991
36 Krawczyk AL Perez S Lau E et al Human papillomavirusvaccination intentions and uptake in college women HealthPsychol 2012 31 685ndash93
37 Newby-Clark IR McGregor I Zanna MP Thinking andcaring about cognitive inconsistency when and for whomdoes attitudinal ambivalence feel uncomfortable J Pers SocPsychol 2002 82 157ndash66
38 Nordgren LF van Harreveld F van der Pligt J Ambivalencediscomfort and motivated information processing J ExperSoc Psychol 2006 42 252ndash8
39 Clark JK Wegener DT Fabrigar LR Attitudinal ambiva-lence and message-based persuasion motivated processingof proattitudinal information and avoidance of counterattitu-dinal information Pers Soc Psychol Bull 2008 34 565ndash77
40 van Keulen HM Otten W Ruiter RA et al Determinants ofHPV vaccination intentions among Dutch girls and theirmothers a cross-sectional study BMC Public Health 201313 111
R Hofman et al
96
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nloaded from
Tab
leII
IH
iera
rchic
al
logis
tic
regre
ssio
nanaly
ses
wit
hupta
ke(y
esn
o)
as
dep
enden
tva
riable
all
vari
able
sare
report
edby
pare
nts
at
base
line
Univ
aria
te
Model
1
(nfrac14
708)
Model
2a
(nfrac14
644)
Model
2b
(nfrac14
617)
Model
3
(nfrac14
572)
Model
4
(nfrac14
569)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
OR
(95
CI)
Dem
ogra
ph
icch
ara
cter
isti
cs
Age
of
par
ents
(yea
rs)
10
2(0
98ndash10
7)
10
1(0
96ndash10
6)
10
3(0
96ndash10
9)
10
2(0
95ndash11
0)
10
2(0
94ndash11
1)
10
1(0
93ndash10
9)
Educa
tional
level
11
5(1
00ndash13
4)
11
7(0
99ndash13
7)
12
5(1
00ndash15
4)
12
0(0
93ndash15
5)
12
7(0
96ndash17
0)
13
3(0
99ndash17
8)
No
reli
gio
us
affi
liat
ion
17
3(1
19ndash25
3)
16
3(1
09ndash24
2)
17
3(1
07ndash28
1)
11
2(0
63ndash20
0)
11
9(0
63ndash22
5)
11
6(0
60ndash22
3)
Dec
isio
nab
out
upta
ke
2011
(vs
2010)
20
8(1
28ndash33
6)
26
8(1
57ndash45
3)
26
9(1
42ndash51
0)
24
5(1
20ndash50
1)
24
8(1
11ndash55
2)
26
0(1
16ndash58
0)
Pare
nt
chara
cter
isti
cs
No
abnorm
alsm
ear
exper
ience
10
2(0
58ndash17
8)
09
4(0
45ndash19
5)
07
0(0
26ndash18
8)
06
8(0
24ndash19
5)
Par
enta
lre
sponsi
bil
ity
12
3(0
83ndash18
4)
15
3(0
91ndash25
9)
15
5(0
76ndash31
8)
18
6(0
90ndash38
3)
Tru
stin
NIP
35
4(2
61ndash48
1)
18
2(1
21ndash27
4)
14
0(0
86ndash23
0)
13
3(0
79ndash22
4)
Tru
stin
vac
cine
36
4(2
85ndash46
4)
34
1(2
49ndash46
8)
12
3(0
69ndash18
3)
09
9(0
59ndash16
7)
Per
ceiv
edsu
scep
tibil
ity
of
moth
erto
cerv
ical
cance
r
10
4(0
93ndash11
6)
10
3(0
88ndash12
1)
09
7(0
77ndash12
2)
09
6(0
76ndash12
2)
Soci
al
cogn
itiv
efa
ctors
Inte
nti
on
45
9(3
56ndash59
2)
26
1(1
47ndash46
1)
Am
biv
alen
ceto
war
dH
PV
vac
cinat
ion
08
2(0
69ndash09
2)
10
7(0
79ndash14
5)
02
7(0
08ndash08
7)
02
2(0
07ndash07
1)
Posi
tive
atti
tude
tow
ard
HP
Vvac
cinat
ion
57
3(4
26ndash77
1)
34
3(2
01ndash58
4)
17
0(0
69ndash42
1)
08
9(0
34ndash23
6)
Soci
alnorm
12
1(1
16ndash12
6)
10
7(1
01ndash11
3)
10
5(0
99ndash11
1)
10
3(0
97ndash10
9)
Norm
ativ
ebel
ief
14
4(1
28ndash16
3)
09
9(0
81ndash12
1)
10
3(0
83ndash12
9)
10
3(0
81ndash12
9)
Know
ledge
10
8(0
95ndash12
2)
09
5(0
87ndash10
4)
09
3(0
76ndash11
3)
09
5(0
78ndash11
7)
Per
ceiv
edsu
scep
tibil
ity
of
dau
ghte
rif
vac
cinat
ed
toce
rvic
alca
nce
r
06
5(0
57ndash07
4)
08
6(0
70ndash10
5)
08
9(0
69ndash11
4)
08
8(0
68ndash11
4)
Per
ceiv
edse
ver
ity
of
cerv
ical
cance
r
12
2(1
03ndash14
6)
10
8(0
81ndash14
2)
10
6(0
78ndash14
4)
10
8(0
79ndash14
8)
Anti
cipat
edre
gre
tan
d
worr
yab
out
no
upta
ke
22
3(1
93ndash25
8)
14
3(1
11ndash18
4)
14
3(1
08ndash18
9)
12
4(0
92ndash16
7)
Am
biv
alen
ce
atti
tude
inte
ract
ion
16
8(1
14ndash24
7)
17
9(1
22ndash26
2)
R2
00
603
505
305
705
9
Plt
00
5Plt
00
1an
dPlt
00
01
Predictors of HPV vaccination uptake
91
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Dow
nloaded from
132ndash192) and social norm (OR 107 95 CI
104ndash110) A lower uptake intention was asso-
ciated with a higher educational level (OR 083
95 CI 070ndash099) and a higher perceived parental
responsibility for their daughterrsquos health (OR 048
95 CI 030ndash075) The interaction term of atti-
tude ambivalence was significant (OR 073
95 CI 059ndash090)
Impact of time
Favorable changes in attitudes toward HPV uptake
over time were significantly related to an increase in
trust in the vaccine (OR 145 95 CI 136ndash153)
and social norm (OR 122 95 CI 115ndash128) over
time and a decrease in ambivalence toward HPV
vaccination (OR 094 95 CI 091ndash098) A de-
crease in ambivalence toward HPV vaccination
over time was significantly related to an increase
in feeling informed about HPV vaccination (OR
079 95 CI 069ndash091) and an increase in trust
in the vaccine (OR 088 95 CI 077ndash099) over
time
Informed decision making
Overall knowledge levels about the degreeduration
of protection were low at baseline and at follow-up
(33ndash43 correct answers) Percentages of correct
responses to five knowledge items increased signifi-
cantly at follow-up (Table IV) When five (out of
seven) correct items were defined as sufficient deci-
sion relevant knowledge then nfrac14 338 (439) of
the respondents made an informed choice about
uptake When four correct items were considered
sufficient then nfrac14 437 (657) of the respondents
made an informed choice about uptake (Table V)
Reasons for vaccinating or not
Main reasons as reported by parents at baseline to
have their daughter vaccinated include feeling re-
sponsible for her health (nfrac14 947 549) a family
history of cancer (nfrac14 128 74) anticipating
regret in case their daughter gets cervical cancer
(nfrac14 103 60) and other (nfrac14 547 317) Main
reasons as reported by parents at baseline not to have
their daughter vaccinated include that consequences
Table IV Knowledge items as completed by those who responded to the baseline and follow-up questionnaire (nfrac14 793)
Correct responses
Baseline
measurement
Follow-up
measurement
Significance level for
difference between
baseline and follow-up
n () n () P-value
Item (truefalse)
HPV causes cervical cancer (true) 496 (625) 479 (604) 0336
A condom protects 100 against HPV (false) 464 (585) 518 (653) 0001
The HPV vaccination will decrease the risk of cervical
cancer (true)
673 (849) 726 (916) lt0001
Vaccination in combination with having a smear taken is
more protective than only vaccination (true)
521 (657) 598 (754) lt0001
Item (multiple choice)
How is HPV transmitted (through blood oxygen sexual
contact)
699 (881) 730 (921) 0006
What is the protection rate of the HPV vaccine (55 70
85 100)
286 (361) 337 (425) 0005
What is the protection duration of a complete vaccination
against cervical cancer (at least 6 (8 at follow-up) years
at least 30 years lifetime)
289 (364) 262 (330) 0094
Correct answers are shaded
R Hofman et al
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Dow
nloaded from
of vaccinating are unpredictable (497 288) fear
of serious side-effects (nfrac14 401 232) and too
little information about the vaccine being available
(nfrac14 125 72)
Discussion
In this study among parents we assessed longitu-
dinal predictors of HPV vaccination uptake of their
daughters Uptake was predicted by intention a later
(2011) versus earlier (2010) decision about uptake
and anticipated regret and worry in case of abstain-
ing from HPV vaccination Ambivalence toward
HPV vaccination at baseline moderated the attitude
(baseline) uptake (follow-up) relationship with the
attitudendashuptake relationship being stronger at higher
ambivalence levels
HPV vaccination was most strongly predicted by
intention which fits the TPB model and was also
reported in an earlier study on predictors of HPV
vaccination uptake [22] In turn HPV vaccination
intention was positively associated with educational
level perceived parental responsibility for onersquos
daughterrsquos health trust in the vaccine the belief
that according to significant others their daughter
should be vaccinated and the motivation to comply
with that (social norm) and anticipated regret and
worry (which also predicted uptake) The relation-
ship found between intention and uptake and
between intention and social norm is consistent
with the TPB model and with another study [22]
which also confirms the association we found
between anticipated regretworry and uptake and
anticipated regretworry and intention The factors
lsquoperceived susceptibilityrsquo and lsquoseverityrsquo of cancer
of the HBM were not associated with intention or
uptake which confirms the results of an earlier study
[22 36]
A possible explanation for the positive effect on
uptake of having to decide later (2011) versus earlier
(2010) might be the amount of time that passed be-
tween the baseline questionnaire (2009) when an
intensive societal debate involving politics phys-
icians media parents and girls about HPV vaccin-
ation was ongoing and the actual decision about
uptake of vaccination In 2011 this debate probably
had less impact on the uptake decision than in 2010
Also after millions of girls worldwide had been
vaccinated and no serious side-effects had been
reported parents who had to decide later versus
earlier probably felt more reassured about the
vaccinersquos safety
This study shows that ambivalence moderated the
attitudendashuptake relationship Parents with a positive
attitude and a high level of ambivalence toward
HPV vaccination were more likely to have their
daughter vaccinated than parents with a positive at-
titude and a low level of ambivalence This finding
might be explained in two ways First ambivalence
is characterized as being subjectively uncomfortable
and people may be motivated to resolve the conflict-
ing evaluations that they hold [37] for example
by searching for information Second earlier
studies found that ambivalent people processed
pro-attitudinal messages to a greater extent than
counter-attitudinal messages probably because
pro-attitudinal messages are more likely to reduce
ambivalence [38 39] Taking these two mechanisms
together it is likely that in our study ambivalent
parents with a positive attitude toward HPV vaccin-
ation processed lsquopositiversquo messages about HPV vac-
cination to a greater extent than lsquonegativersquo messages
and were therefore more likely to have their
Table V Informed decision at follow-up (nfrac14 770)
Daughter
vaccinated
(nfrac14 640)
Daughter not
vaccinated
(nfrac14 130)
n () n ()
Positive attitude
Five or more correct items 280 (364) 14 (18)
Less than five correct items 246 (319) 16 (21)
Negative attitude
Five or more correct items 51 (66) 58 (75)
Less than five correct items 32 (42) 34 (44)
Knowledge was measured with seven items at follow-upInformed decision rate for cut-off at three correct items761 [(504 + 82)770] four correct items 657[(437 + 69)770] five correct items 439 [(280 + 58)770]six correct items 187 [(117 + 27)770] Due to missingitems analyses were based on nfrac14 770 respondents instead ofnfrac14 793 Informed choice (as defined) is shaded
Predictors of HPV vaccination uptake
93
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Dow
nloaded from
daughter vaccinated In other words parents who
had both positive attitudes and were ambivalent to-
ward HPV vaccination became even more positive
because they elaborated only information in favor of
HPV vaccination This may imply that this lsquobiasedrsquo
information processing has a negative impact on
informed decision making although parents will
have gained more knowledge during their efforts
to resolve their ambivalence
Assessing decisional factors related to HPV vac-
cination both before and after the decision-making
process about uptake provided a unique opportun-
ity to determine changes in those factors over time
As uptake was predicted by intention and intention
was highly correlated with attitude (rfrac14 084) (at
baseline) we think it is relevant to show which
factors are important for changes in attitude over
time Our results show that a more positive attitude
toward HPV vaccination over time was associated
with an increase in trust in the vaccine and in
social norm over time and a decrease in ambiva-
lence toward HPV vaccination over time This
latter factor was related to an increase in feeling
informed about HPV vaccination and an increase
in trust in the vaccine over time In summary over
time parents felt better informed became less am-
bivalent and had more trust in the vaccine These
results are in accordance with our finding that
girls who had to decide with their parents whether
or not to be vaccinated in 2011 were more likely
to be vaccinated than those who had to decide
in 2010
An important finding is that knowledge about the
duration of protection was low at both baseline and
follow-up For instance about 65 of the parents
thought that protection lasts 30 years or even life-
long As the duration of protection is still unknown
it is important that parents and girls know that
booster vaccinations might be needed in the future
When we applied a cut-off of four or five correct
knowledge items (out of seven) then the rates
of informed choice about uptake were not high
66 and 44 respectively However this finding
should be interpreted with caution because the
time period between the assessment of knowledge
and the last vaccination out of three shots was
1 month (decision in 2011) or 14 months (decision
in 2010) In educational material it should be clearly
stated what is known and not yet known about HPV
vaccination
Study strengths include the longitudinal design
as recommended by authors of a cross-sectional
study [40] the high (absolute) number of respond-
ents of the baseline (nfrac14 1725) and follow-up ques-
tionnaires (nfrac14 793) and the high response rate of the
follow-up questionnaire (74)
Limitations
A limitation was the low response rate of the base-
line questionnaire (30) which might be due to the
length of the questionnaire Our sample may there-
fore not be representative of the general population
as few parents had a low educational level Also
demographic characteristics of the follow-up group
were slightly different from those of the baseline
group with more parents being better educated
and well-off at follow-up These parents might pos-
sibly be more likely than those in the wider popula-
tion to seek to reduce high ambivalence by
searching information allowing them to respond
positively to the vaccine invitationmdashrather than do
nothing
Conclusion
In conclusion this study shows that intention a later
versus earlier decision about uptake and anticipated
regretworry about abstaining from vaccination
were predictors of uptake Anticipated regret was a
common predictor of intention and uptake and thus
an important factor in the decision-making process
about HPV vaccination In turn predictors of inten-
tion like social norm and trust in the vaccine are
also important when deciding about HPV vaccin-
ation Over time parents felt better informed
became less ambivalent and had more trust in the
vaccine
Practice implications
This study shows the usefulness of including affect-
ive factors in studies examining HPV vaccination
R Hofman et al
94
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nloaded from
behavior as anticipated regret trust in the vaccine
and ambivalence were found to play a role in the
decision making about uptake However it is also
important that parents are enabled to base their
decision about HPV vaccination of their daughter
on decision relevant knowledge As these results
suggest that people need sufficient time to decide
about the uptake of a new vaccine we recommend
a well-balanced stepwise process of implementa-
tion that is let parents first become aware of the
link between HPV and cervical cancer then provide
them with balanced information about all the
knowns and also the unknowns of HPV vaccination
and then finally offer them the opportunity to have
their daughter vaccinated As two-third of parents
wrongly thought that protection lasts 30 years or
even lifelong educational material should clearly
state that booster vaccinations might be needed in
the future
Acknowledgements
The authors thank the Dutch Cancer Society for
financial support and the participants for their
contribution to the study
Funding
The Dutch Cancer Society [EMCR 2008-3992
EMCR 2009-4561]
Conflict of interest statement
None declared
References
1 Karim-Kos HE de Vries E Soerjomataram I et al Recenttrends of cancer in Europe a combined approach of inci-dence survival and mortality for 17 cancer sites since the1990s Eur J Cancer 2008 44 1345ndash89
2 Bosch FX Lorincz A Munoz N et al The causal relationbetween human papillomavirus and cervical cancer J ClinPathol 2002 55 244ndash65
3 Walboomers JM Jacobs MV Manos MM et al Humanpapillomavirus is a necessary cause of invasive cervicalcancer worldwide J Pathol 1999 189 12ndash9
4 Munoz N Bosch FX Castellsague X et al Against whichhuman papillomavirus types shall we vaccinate and screenThe international perspective Int J Cancer 2004 111278ndash85
5 Koutsky LA Holmes KK Critchlow CW et al A cohortstudy of the risk of cervical intraepithelial neoplasia grade2 or 3 in relation to papillomavirus infection N Engl J Med1992 327 1272ndash8
6 Woodman CB Collins S Winter H et al Natural history ofcervical human papillomavirus infection in young women alongitudinal cohort study Lancet 2001 357 1831ndash6
7 Boot HJ Wallenburg I de Melker HE et al Assessing theintroduction of universal human papillomavirus vaccinationfor preadolescent girls in The Netherlands Vaccine 2007 256245ndash56
8 van Lier EA Oomen PJ Oostenbrug MWM et alImmunization coverage National ImmunizationProgramme in the Netherlands Year of report 2009[Vaccinatiegraad Rijksvaccinatieprogramma NederlandVerslagjaar 2009] Bilthoven RIVM 2009
9 Zwakhals SLN van Lier EA van HPV (cohort 1997) bymunicipality 2012 [HPV (cohort 1997) per gemeente2012] In Dutch National Atlas of Public HealthBilthoven RIVM 2012 (httpwwwzorgatlasnlpreventievaccinaties-en-screeninghpv-cohort-1997-vaccinatiegraad-per-gemeente-2012 accessed 2 September 2013)
10 Brabin L Roberts SA Stretch R et al A survey of adolescentexperiences of human papillomavirus vaccination in theManchester study Br J cancer 2009 101 1502ndash4
11 Brabin L Roberts SA Kitchener HC A semi-qualitativestudy of attitudes to vaccinating adolescents against humanpapillomavirus without parental consent BMC PublicHealth 2007 7 20
12 Brewer NT Fazekas KI Predictors of HPV vaccine accept-ability A theory-informed systematic review Prev Med2007 45 107ndash14
13 Kahn JA Rosenthal SL Jin Y et al Rates of human papillo-mavirus vaccination attitudes about vaccination and humanpapillomavirus prevalence in young women Obstet Gynecol2008 111 1103ndash10
14 Askelson NM Campo S Lowe JB et al Using the theoryof planned behavior to predict mothersrsquo intentions to vaccin-ate their daughters against HPV J Sch Nurs 2010 26194ndash202
15 Ajzen I The theory of Planned Behavior Organ Behav HumDecis Process 1991 50 179ndash211
16 Becker MH The health belief model and personal healthbehavior Health Edu Monogr 1974 2 324ndash508
17 Chapman GB Coups EJ Emotions and preventive healthbehavior worry regret and influenza vaccination HealthPsychol 2006 25 82ndash90
18 Paulussen TG Hoekstra F Lanting CI et al Determinants ofDutch parentsrsquo decisions to vaccinate their child Vaccine2006 24 644ndash51
19 Kaplan KJ On the ambivalence-indifference problem inattitude theory and measurement A suggested modificationof the semantic differential technique Psychol Bull 1972 77361ndash372
20 Dormandy E Hankins M Marteau TM Attitudes and uptakeof a screening test The moderating role of ambivalencePsychol Health 2006 21 499ndash511
Predictors of HPV vaccination uptake
95
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
21 Hofman R van Empelen P Vogel I et al Parental decisionalstrategies regarding HPV vaccination prior to media debatesa focus-group study J Health Commun 2013 18 866ndash80
22 Brewer NT Gottlieb SL Reiter PL et al Longitudinal pre-dictors of human papillomavirus vaccine initiation amongadolescent girls in a high-risk geographic area Sex TransmDis 2011 38 197ndash204
23 Marlow LA Waller J Wardle J Trust and experience aspredictors of HPV vaccine acceptance Hum Vaccin 20073 171ndash5
24 Weinstein ND Perceived probability perceived severityand health-protective behavior Health Psychol 2000 1965ndash74
25 Marteau TM Dormandy E Michie S A measure of informedchoice Health Expect 2001 4 99ndash108
26 van den Berg M Timmermans DR Ten Kate LP et al Arepregnant women making informed choices about prenatalscreening Genet Med 2005 7 332ndash8
27 Tiro JA Diamond PM Perz CA et al Validation of scalesmeasuring attitudes and norms related to mammographyscreening in women veterans Health Psychol 2005 24555ndash66
28 Marlow LAV Waller J Wardle J Parental attitudes to pre-pubertal HPV vaccination Vaccine 2007 25 1945ndash52
29 Stalmeier PF Roosmalen MS Verhoef LC et al Thedecision evaluation scales Patient Educ Couns 2005 57286ndash93
30 Gilbert LA Hanson GR Perceptions of parental role respon-sibilities among working people Development of a compre-hensive measure J Marriage Fam 1983 45 203ndash12
31 Korfage IJ van Ballegooijen M Wauben B et al Informedchoice on Pap smear still limited by lack of knowledge on the
meaning of false-positive or false-negative test resultsPatient Educ Couns 2011 85 214ndash8
32 Thompson MM Zanna MP The conflicted individual per-sonality-based and domain specific antecedents of ambiva-lent social attitudes J Pers 1995 63 259ndash88
33 General Medical Council Seeking Patientsrsquo Consent TheEthical Considerations London GMC 1998
34 Minister of Health Letter about screening [Kaderbriefscreening] PGZP 2848440 Ministry of Health Welfareand Sports The Hague 2008
35 Aiken LS West RR Multiple Regression Testing andInterpreting Interactions Newbury Park CA Sage 1991
36 Krawczyk AL Perez S Lau E et al Human papillomavirusvaccination intentions and uptake in college women HealthPsychol 2012 31 685ndash93
37 Newby-Clark IR McGregor I Zanna MP Thinking andcaring about cognitive inconsistency when and for whomdoes attitudinal ambivalence feel uncomfortable J Pers SocPsychol 2002 82 157ndash66
38 Nordgren LF van Harreveld F van der Pligt J Ambivalencediscomfort and motivated information processing J ExperSoc Psychol 2006 42 252ndash8
39 Clark JK Wegener DT Fabrigar LR Attitudinal ambiva-lence and message-based persuasion motivated processingof proattitudinal information and avoidance of counterattitu-dinal information Pers Soc Psychol Bull 2008 34 565ndash77
40 van Keulen HM Otten W Ruiter RA et al Determinants ofHPV vaccination intentions among Dutch girls and theirmothers a cross-sectional study BMC Public Health 201313 111
R Hofman et al
96
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oronto Library on O
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Dow
nloaded from
132ndash192) and social norm (OR 107 95 CI
104ndash110) A lower uptake intention was asso-
ciated with a higher educational level (OR 083
95 CI 070ndash099) and a higher perceived parental
responsibility for their daughterrsquos health (OR 048
95 CI 030ndash075) The interaction term of atti-
tude ambivalence was significant (OR 073
95 CI 059ndash090)
Impact of time
Favorable changes in attitudes toward HPV uptake
over time were significantly related to an increase in
trust in the vaccine (OR 145 95 CI 136ndash153)
and social norm (OR 122 95 CI 115ndash128) over
time and a decrease in ambivalence toward HPV
vaccination (OR 094 95 CI 091ndash098) A de-
crease in ambivalence toward HPV vaccination
over time was significantly related to an increase
in feeling informed about HPV vaccination (OR
079 95 CI 069ndash091) and an increase in trust
in the vaccine (OR 088 95 CI 077ndash099) over
time
Informed decision making
Overall knowledge levels about the degreeduration
of protection were low at baseline and at follow-up
(33ndash43 correct answers) Percentages of correct
responses to five knowledge items increased signifi-
cantly at follow-up (Table IV) When five (out of
seven) correct items were defined as sufficient deci-
sion relevant knowledge then nfrac14 338 (439) of
the respondents made an informed choice about
uptake When four correct items were considered
sufficient then nfrac14 437 (657) of the respondents
made an informed choice about uptake (Table V)
Reasons for vaccinating or not
Main reasons as reported by parents at baseline to
have their daughter vaccinated include feeling re-
sponsible for her health (nfrac14 947 549) a family
history of cancer (nfrac14 128 74) anticipating
regret in case their daughter gets cervical cancer
(nfrac14 103 60) and other (nfrac14 547 317) Main
reasons as reported by parents at baseline not to have
their daughter vaccinated include that consequences
Table IV Knowledge items as completed by those who responded to the baseline and follow-up questionnaire (nfrac14 793)
Correct responses
Baseline
measurement
Follow-up
measurement
Significance level for
difference between
baseline and follow-up
n () n () P-value
Item (truefalse)
HPV causes cervical cancer (true) 496 (625) 479 (604) 0336
A condom protects 100 against HPV (false) 464 (585) 518 (653) 0001
The HPV vaccination will decrease the risk of cervical
cancer (true)
673 (849) 726 (916) lt0001
Vaccination in combination with having a smear taken is
more protective than only vaccination (true)
521 (657) 598 (754) lt0001
Item (multiple choice)
How is HPV transmitted (through blood oxygen sexual
contact)
699 (881) 730 (921) 0006
What is the protection rate of the HPV vaccine (55 70
85 100)
286 (361) 337 (425) 0005
What is the protection duration of a complete vaccination
against cervical cancer (at least 6 (8 at follow-up) years
at least 30 years lifetime)
289 (364) 262 (330) 0094
Correct answers are shaded
R Hofman et al
92
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
of vaccinating are unpredictable (497 288) fear
of serious side-effects (nfrac14 401 232) and too
little information about the vaccine being available
(nfrac14 125 72)
Discussion
In this study among parents we assessed longitu-
dinal predictors of HPV vaccination uptake of their
daughters Uptake was predicted by intention a later
(2011) versus earlier (2010) decision about uptake
and anticipated regret and worry in case of abstain-
ing from HPV vaccination Ambivalence toward
HPV vaccination at baseline moderated the attitude
(baseline) uptake (follow-up) relationship with the
attitudendashuptake relationship being stronger at higher
ambivalence levels
HPV vaccination was most strongly predicted by
intention which fits the TPB model and was also
reported in an earlier study on predictors of HPV
vaccination uptake [22] In turn HPV vaccination
intention was positively associated with educational
level perceived parental responsibility for onersquos
daughterrsquos health trust in the vaccine the belief
that according to significant others their daughter
should be vaccinated and the motivation to comply
with that (social norm) and anticipated regret and
worry (which also predicted uptake) The relation-
ship found between intention and uptake and
between intention and social norm is consistent
with the TPB model and with another study [22]
which also confirms the association we found
between anticipated regretworry and uptake and
anticipated regretworry and intention The factors
lsquoperceived susceptibilityrsquo and lsquoseverityrsquo of cancer
of the HBM were not associated with intention or
uptake which confirms the results of an earlier study
[22 36]
A possible explanation for the positive effect on
uptake of having to decide later (2011) versus earlier
(2010) might be the amount of time that passed be-
tween the baseline questionnaire (2009) when an
intensive societal debate involving politics phys-
icians media parents and girls about HPV vaccin-
ation was ongoing and the actual decision about
uptake of vaccination In 2011 this debate probably
had less impact on the uptake decision than in 2010
Also after millions of girls worldwide had been
vaccinated and no serious side-effects had been
reported parents who had to decide later versus
earlier probably felt more reassured about the
vaccinersquos safety
This study shows that ambivalence moderated the
attitudendashuptake relationship Parents with a positive
attitude and a high level of ambivalence toward
HPV vaccination were more likely to have their
daughter vaccinated than parents with a positive at-
titude and a low level of ambivalence This finding
might be explained in two ways First ambivalence
is characterized as being subjectively uncomfortable
and people may be motivated to resolve the conflict-
ing evaluations that they hold [37] for example
by searching for information Second earlier
studies found that ambivalent people processed
pro-attitudinal messages to a greater extent than
counter-attitudinal messages probably because
pro-attitudinal messages are more likely to reduce
ambivalence [38 39] Taking these two mechanisms
together it is likely that in our study ambivalent
parents with a positive attitude toward HPV vaccin-
ation processed lsquopositiversquo messages about HPV vac-
cination to a greater extent than lsquonegativersquo messages
and were therefore more likely to have their
Table V Informed decision at follow-up (nfrac14 770)
Daughter
vaccinated
(nfrac14 640)
Daughter not
vaccinated
(nfrac14 130)
n () n ()
Positive attitude
Five or more correct items 280 (364) 14 (18)
Less than five correct items 246 (319) 16 (21)
Negative attitude
Five or more correct items 51 (66) 58 (75)
Less than five correct items 32 (42) 34 (44)
Knowledge was measured with seven items at follow-upInformed decision rate for cut-off at three correct items761 [(504 + 82)770] four correct items 657[(437 + 69)770] five correct items 439 [(280 + 58)770]six correct items 187 [(117 + 27)770] Due to missingitems analyses were based on nfrac14 770 respondents instead ofnfrac14 793 Informed choice (as defined) is shaded
Predictors of HPV vaccination uptake
93
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
daughter vaccinated In other words parents who
had both positive attitudes and were ambivalent to-
ward HPV vaccination became even more positive
because they elaborated only information in favor of
HPV vaccination This may imply that this lsquobiasedrsquo
information processing has a negative impact on
informed decision making although parents will
have gained more knowledge during their efforts
to resolve their ambivalence
Assessing decisional factors related to HPV vac-
cination both before and after the decision-making
process about uptake provided a unique opportun-
ity to determine changes in those factors over time
As uptake was predicted by intention and intention
was highly correlated with attitude (rfrac14 084) (at
baseline) we think it is relevant to show which
factors are important for changes in attitude over
time Our results show that a more positive attitude
toward HPV vaccination over time was associated
with an increase in trust in the vaccine and in
social norm over time and a decrease in ambiva-
lence toward HPV vaccination over time This
latter factor was related to an increase in feeling
informed about HPV vaccination and an increase
in trust in the vaccine over time In summary over
time parents felt better informed became less am-
bivalent and had more trust in the vaccine These
results are in accordance with our finding that
girls who had to decide with their parents whether
or not to be vaccinated in 2011 were more likely
to be vaccinated than those who had to decide
in 2010
An important finding is that knowledge about the
duration of protection was low at both baseline and
follow-up For instance about 65 of the parents
thought that protection lasts 30 years or even life-
long As the duration of protection is still unknown
it is important that parents and girls know that
booster vaccinations might be needed in the future
When we applied a cut-off of four or five correct
knowledge items (out of seven) then the rates
of informed choice about uptake were not high
66 and 44 respectively However this finding
should be interpreted with caution because the
time period between the assessment of knowledge
and the last vaccination out of three shots was
1 month (decision in 2011) or 14 months (decision
in 2010) In educational material it should be clearly
stated what is known and not yet known about HPV
vaccination
Study strengths include the longitudinal design
as recommended by authors of a cross-sectional
study [40] the high (absolute) number of respond-
ents of the baseline (nfrac14 1725) and follow-up ques-
tionnaires (nfrac14 793) and the high response rate of the
follow-up questionnaire (74)
Limitations
A limitation was the low response rate of the base-
line questionnaire (30) which might be due to the
length of the questionnaire Our sample may there-
fore not be representative of the general population
as few parents had a low educational level Also
demographic characteristics of the follow-up group
were slightly different from those of the baseline
group with more parents being better educated
and well-off at follow-up These parents might pos-
sibly be more likely than those in the wider popula-
tion to seek to reduce high ambivalence by
searching information allowing them to respond
positively to the vaccine invitationmdashrather than do
nothing
Conclusion
In conclusion this study shows that intention a later
versus earlier decision about uptake and anticipated
regretworry about abstaining from vaccination
were predictors of uptake Anticipated regret was a
common predictor of intention and uptake and thus
an important factor in the decision-making process
about HPV vaccination In turn predictors of inten-
tion like social norm and trust in the vaccine are
also important when deciding about HPV vaccin-
ation Over time parents felt better informed
became less ambivalent and had more trust in the
vaccine
Practice implications
This study shows the usefulness of including affect-
ive factors in studies examining HPV vaccination
R Hofman et al
94
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
behavior as anticipated regret trust in the vaccine
and ambivalence were found to play a role in the
decision making about uptake However it is also
important that parents are enabled to base their
decision about HPV vaccination of their daughter
on decision relevant knowledge As these results
suggest that people need sufficient time to decide
about the uptake of a new vaccine we recommend
a well-balanced stepwise process of implementa-
tion that is let parents first become aware of the
link between HPV and cervical cancer then provide
them with balanced information about all the
knowns and also the unknowns of HPV vaccination
and then finally offer them the opportunity to have
their daughter vaccinated As two-third of parents
wrongly thought that protection lasts 30 years or
even lifelong educational material should clearly
state that booster vaccinations might be needed in
the future
Acknowledgements
The authors thank the Dutch Cancer Society for
financial support and the participants for their
contribution to the study
Funding
The Dutch Cancer Society [EMCR 2008-3992
EMCR 2009-4561]
Conflict of interest statement
None declared
References
1 Karim-Kos HE de Vries E Soerjomataram I et al Recenttrends of cancer in Europe a combined approach of inci-dence survival and mortality for 17 cancer sites since the1990s Eur J Cancer 2008 44 1345ndash89
2 Bosch FX Lorincz A Munoz N et al The causal relationbetween human papillomavirus and cervical cancer J ClinPathol 2002 55 244ndash65
3 Walboomers JM Jacobs MV Manos MM et al Humanpapillomavirus is a necessary cause of invasive cervicalcancer worldwide J Pathol 1999 189 12ndash9
4 Munoz N Bosch FX Castellsague X et al Against whichhuman papillomavirus types shall we vaccinate and screenThe international perspective Int J Cancer 2004 111278ndash85
5 Koutsky LA Holmes KK Critchlow CW et al A cohortstudy of the risk of cervical intraepithelial neoplasia grade2 or 3 in relation to papillomavirus infection N Engl J Med1992 327 1272ndash8
6 Woodman CB Collins S Winter H et al Natural history ofcervical human papillomavirus infection in young women alongitudinal cohort study Lancet 2001 357 1831ndash6
7 Boot HJ Wallenburg I de Melker HE et al Assessing theintroduction of universal human papillomavirus vaccinationfor preadolescent girls in The Netherlands Vaccine 2007 256245ndash56
8 van Lier EA Oomen PJ Oostenbrug MWM et alImmunization coverage National ImmunizationProgramme in the Netherlands Year of report 2009[Vaccinatiegraad Rijksvaccinatieprogramma NederlandVerslagjaar 2009] Bilthoven RIVM 2009
9 Zwakhals SLN van Lier EA van HPV (cohort 1997) bymunicipality 2012 [HPV (cohort 1997) per gemeente2012] In Dutch National Atlas of Public HealthBilthoven RIVM 2012 (httpwwwzorgatlasnlpreventievaccinaties-en-screeninghpv-cohort-1997-vaccinatiegraad-per-gemeente-2012 accessed 2 September 2013)
10 Brabin L Roberts SA Stretch R et al A survey of adolescentexperiences of human papillomavirus vaccination in theManchester study Br J cancer 2009 101 1502ndash4
11 Brabin L Roberts SA Kitchener HC A semi-qualitativestudy of attitudes to vaccinating adolescents against humanpapillomavirus without parental consent BMC PublicHealth 2007 7 20
12 Brewer NT Fazekas KI Predictors of HPV vaccine accept-ability A theory-informed systematic review Prev Med2007 45 107ndash14
13 Kahn JA Rosenthal SL Jin Y et al Rates of human papillo-mavirus vaccination attitudes about vaccination and humanpapillomavirus prevalence in young women Obstet Gynecol2008 111 1103ndash10
14 Askelson NM Campo S Lowe JB et al Using the theoryof planned behavior to predict mothersrsquo intentions to vaccin-ate their daughters against HPV J Sch Nurs 2010 26194ndash202
15 Ajzen I The theory of Planned Behavior Organ Behav HumDecis Process 1991 50 179ndash211
16 Becker MH The health belief model and personal healthbehavior Health Edu Monogr 1974 2 324ndash508
17 Chapman GB Coups EJ Emotions and preventive healthbehavior worry regret and influenza vaccination HealthPsychol 2006 25 82ndash90
18 Paulussen TG Hoekstra F Lanting CI et al Determinants ofDutch parentsrsquo decisions to vaccinate their child Vaccine2006 24 644ndash51
19 Kaplan KJ On the ambivalence-indifference problem inattitude theory and measurement A suggested modificationof the semantic differential technique Psychol Bull 1972 77361ndash372
20 Dormandy E Hankins M Marteau TM Attitudes and uptakeof a screening test The moderating role of ambivalencePsychol Health 2006 21 499ndash511
Predictors of HPV vaccination uptake
95
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
21 Hofman R van Empelen P Vogel I et al Parental decisionalstrategies regarding HPV vaccination prior to media debatesa focus-group study J Health Commun 2013 18 866ndash80
22 Brewer NT Gottlieb SL Reiter PL et al Longitudinal pre-dictors of human papillomavirus vaccine initiation amongadolescent girls in a high-risk geographic area Sex TransmDis 2011 38 197ndash204
23 Marlow LA Waller J Wardle J Trust and experience aspredictors of HPV vaccine acceptance Hum Vaccin 20073 171ndash5
24 Weinstein ND Perceived probability perceived severityand health-protective behavior Health Psychol 2000 1965ndash74
25 Marteau TM Dormandy E Michie S A measure of informedchoice Health Expect 2001 4 99ndash108
26 van den Berg M Timmermans DR Ten Kate LP et al Arepregnant women making informed choices about prenatalscreening Genet Med 2005 7 332ndash8
27 Tiro JA Diamond PM Perz CA et al Validation of scalesmeasuring attitudes and norms related to mammographyscreening in women veterans Health Psychol 2005 24555ndash66
28 Marlow LAV Waller J Wardle J Parental attitudes to pre-pubertal HPV vaccination Vaccine 2007 25 1945ndash52
29 Stalmeier PF Roosmalen MS Verhoef LC et al Thedecision evaluation scales Patient Educ Couns 2005 57286ndash93
30 Gilbert LA Hanson GR Perceptions of parental role respon-sibilities among working people Development of a compre-hensive measure J Marriage Fam 1983 45 203ndash12
31 Korfage IJ van Ballegooijen M Wauben B et al Informedchoice on Pap smear still limited by lack of knowledge on the
meaning of false-positive or false-negative test resultsPatient Educ Couns 2011 85 214ndash8
32 Thompson MM Zanna MP The conflicted individual per-sonality-based and domain specific antecedents of ambiva-lent social attitudes J Pers 1995 63 259ndash88
33 General Medical Council Seeking Patientsrsquo Consent TheEthical Considerations London GMC 1998
34 Minister of Health Letter about screening [Kaderbriefscreening] PGZP 2848440 Ministry of Health Welfareand Sports The Hague 2008
35 Aiken LS West RR Multiple Regression Testing andInterpreting Interactions Newbury Park CA Sage 1991
36 Krawczyk AL Perez S Lau E et al Human papillomavirusvaccination intentions and uptake in college women HealthPsychol 2012 31 685ndash93
37 Newby-Clark IR McGregor I Zanna MP Thinking andcaring about cognitive inconsistency when and for whomdoes attitudinal ambivalence feel uncomfortable J Pers SocPsychol 2002 82 157ndash66
38 Nordgren LF van Harreveld F van der Pligt J Ambivalencediscomfort and motivated information processing J ExperSoc Psychol 2006 42 252ndash8
39 Clark JK Wegener DT Fabrigar LR Attitudinal ambiva-lence and message-based persuasion motivated processingof proattitudinal information and avoidance of counterattitu-dinal information Pers Soc Psychol Bull 2008 34 565ndash77
40 van Keulen HM Otten W Ruiter RA et al Determinants ofHPV vaccination intentions among Dutch girls and theirmothers a cross-sectional study BMC Public Health 201313 111
R Hofman et al
96
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
of vaccinating are unpredictable (497 288) fear
of serious side-effects (nfrac14 401 232) and too
little information about the vaccine being available
(nfrac14 125 72)
Discussion
In this study among parents we assessed longitu-
dinal predictors of HPV vaccination uptake of their
daughters Uptake was predicted by intention a later
(2011) versus earlier (2010) decision about uptake
and anticipated regret and worry in case of abstain-
ing from HPV vaccination Ambivalence toward
HPV vaccination at baseline moderated the attitude
(baseline) uptake (follow-up) relationship with the
attitudendashuptake relationship being stronger at higher
ambivalence levels
HPV vaccination was most strongly predicted by
intention which fits the TPB model and was also
reported in an earlier study on predictors of HPV
vaccination uptake [22] In turn HPV vaccination
intention was positively associated with educational
level perceived parental responsibility for onersquos
daughterrsquos health trust in the vaccine the belief
that according to significant others their daughter
should be vaccinated and the motivation to comply
with that (social norm) and anticipated regret and
worry (which also predicted uptake) The relation-
ship found between intention and uptake and
between intention and social norm is consistent
with the TPB model and with another study [22]
which also confirms the association we found
between anticipated regretworry and uptake and
anticipated regretworry and intention The factors
lsquoperceived susceptibilityrsquo and lsquoseverityrsquo of cancer
of the HBM were not associated with intention or
uptake which confirms the results of an earlier study
[22 36]
A possible explanation for the positive effect on
uptake of having to decide later (2011) versus earlier
(2010) might be the amount of time that passed be-
tween the baseline questionnaire (2009) when an
intensive societal debate involving politics phys-
icians media parents and girls about HPV vaccin-
ation was ongoing and the actual decision about
uptake of vaccination In 2011 this debate probably
had less impact on the uptake decision than in 2010
Also after millions of girls worldwide had been
vaccinated and no serious side-effects had been
reported parents who had to decide later versus
earlier probably felt more reassured about the
vaccinersquos safety
This study shows that ambivalence moderated the
attitudendashuptake relationship Parents with a positive
attitude and a high level of ambivalence toward
HPV vaccination were more likely to have their
daughter vaccinated than parents with a positive at-
titude and a low level of ambivalence This finding
might be explained in two ways First ambivalence
is characterized as being subjectively uncomfortable
and people may be motivated to resolve the conflict-
ing evaluations that they hold [37] for example
by searching for information Second earlier
studies found that ambivalent people processed
pro-attitudinal messages to a greater extent than
counter-attitudinal messages probably because
pro-attitudinal messages are more likely to reduce
ambivalence [38 39] Taking these two mechanisms
together it is likely that in our study ambivalent
parents with a positive attitude toward HPV vaccin-
ation processed lsquopositiversquo messages about HPV vac-
cination to a greater extent than lsquonegativersquo messages
and were therefore more likely to have their
Table V Informed decision at follow-up (nfrac14 770)
Daughter
vaccinated
(nfrac14 640)
Daughter not
vaccinated
(nfrac14 130)
n () n ()
Positive attitude
Five or more correct items 280 (364) 14 (18)
Less than five correct items 246 (319) 16 (21)
Negative attitude
Five or more correct items 51 (66) 58 (75)
Less than five correct items 32 (42) 34 (44)
Knowledge was measured with seven items at follow-upInformed decision rate for cut-off at three correct items761 [(504 + 82)770] four correct items 657[(437 + 69)770] five correct items 439 [(280 + 58)770]six correct items 187 [(117 + 27)770] Due to missingitems analyses were based on nfrac14 770 respondents instead ofnfrac14 793 Informed choice (as defined) is shaded
Predictors of HPV vaccination uptake
93
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
daughter vaccinated In other words parents who
had both positive attitudes and were ambivalent to-
ward HPV vaccination became even more positive
because they elaborated only information in favor of
HPV vaccination This may imply that this lsquobiasedrsquo
information processing has a negative impact on
informed decision making although parents will
have gained more knowledge during their efforts
to resolve their ambivalence
Assessing decisional factors related to HPV vac-
cination both before and after the decision-making
process about uptake provided a unique opportun-
ity to determine changes in those factors over time
As uptake was predicted by intention and intention
was highly correlated with attitude (rfrac14 084) (at
baseline) we think it is relevant to show which
factors are important for changes in attitude over
time Our results show that a more positive attitude
toward HPV vaccination over time was associated
with an increase in trust in the vaccine and in
social norm over time and a decrease in ambiva-
lence toward HPV vaccination over time This
latter factor was related to an increase in feeling
informed about HPV vaccination and an increase
in trust in the vaccine over time In summary over
time parents felt better informed became less am-
bivalent and had more trust in the vaccine These
results are in accordance with our finding that
girls who had to decide with their parents whether
or not to be vaccinated in 2011 were more likely
to be vaccinated than those who had to decide
in 2010
An important finding is that knowledge about the
duration of protection was low at both baseline and
follow-up For instance about 65 of the parents
thought that protection lasts 30 years or even life-
long As the duration of protection is still unknown
it is important that parents and girls know that
booster vaccinations might be needed in the future
When we applied a cut-off of four or five correct
knowledge items (out of seven) then the rates
of informed choice about uptake were not high
66 and 44 respectively However this finding
should be interpreted with caution because the
time period between the assessment of knowledge
and the last vaccination out of three shots was
1 month (decision in 2011) or 14 months (decision
in 2010) In educational material it should be clearly
stated what is known and not yet known about HPV
vaccination
Study strengths include the longitudinal design
as recommended by authors of a cross-sectional
study [40] the high (absolute) number of respond-
ents of the baseline (nfrac14 1725) and follow-up ques-
tionnaires (nfrac14 793) and the high response rate of the
follow-up questionnaire (74)
Limitations
A limitation was the low response rate of the base-
line questionnaire (30) which might be due to the
length of the questionnaire Our sample may there-
fore not be representative of the general population
as few parents had a low educational level Also
demographic characteristics of the follow-up group
were slightly different from those of the baseline
group with more parents being better educated
and well-off at follow-up These parents might pos-
sibly be more likely than those in the wider popula-
tion to seek to reduce high ambivalence by
searching information allowing them to respond
positively to the vaccine invitationmdashrather than do
nothing
Conclusion
In conclusion this study shows that intention a later
versus earlier decision about uptake and anticipated
regretworry about abstaining from vaccination
were predictors of uptake Anticipated regret was a
common predictor of intention and uptake and thus
an important factor in the decision-making process
about HPV vaccination In turn predictors of inten-
tion like social norm and trust in the vaccine are
also important when deciding about HPV vaccin-
ation Over time parents felt better informed
became less ambivalent and had more trust in the
vaccine
Practice implications
This study shows the usefulness of including affect-
ive factors in studies examining HPV vaccination
R Hofman et al
94
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
behavior as anticipated regret trust in the vaccine
and ambivalence were found to play a role in the
decision making about uptake However it is also
important that parents are enabled to base their
decision about HPV vaccination of their daughter
on decision relevant knowledge As these results
suggest that people need sufficient time to decide
about the uptake of a new vaccine we recommend
a well-balanced stepwise process of implementa-
tion that is let parents first become aware of the
link between HPV and cervical cancer then provide
them with balanced information about all the
knowns and also the unknowns of HPV vaccination
and then finally offer them the opportunity to have
their daughter vaccinated As two-third of parents
wrongly thought that protection lasts 30 years or
even lifelong educational material should clearly
state that booster vaccinations might be needed in
the future
Acknowledgements
The authors thank the Dutch Cancer Society for
financial support and the participants for their
contribution to the study
Funding
The Dutch Cancer Society [EMCR 2008-3992
EMCR 2009-4561]
Conflict of interest statement
None declared
References
1 Karim-Kos HE de Vries E Soerjomataram I et al Recenttrends of cancer in Europe a combined approach of inci-dence survival and mortality for 17 cancer sites since the1990s Eur J Cancer 2008 44 1345ndash89
2 Bosch FX Lorincz A Munoz N et al The causal relationbetween human papillomavirus and cervical cancer J ClinPathol 2002 55 244ndash65
3 Walboomers JM Jacobs MV Manos MM et al Humanpapillomavirus is a necessary cause of invasive cervicalcancer worldwide J Pathol 1999 189 12ndash9
4 Munoz N Bosch FX Castellsague X et al Against whichhuman papillomavirus types shall we vaccinate and screenThe international perspective Int J Cancer 2004 111278ndash85
5 Koutsky LA Holmes KK Critchlow CW et al A cohortstudy of the risk of cervical intraepithelial neoplasia grade2 or 3 in relation to papillomavirus infection N Engl J Med1992 327 1272ndash8
6 Woodman CB Collins S Winter H et al Natural history ofcervical human papillomavirus infection in young women alongitudinal cohort study Lancet 2001 357 1831ndash6
7 Boot HJ Wallenburg I de Melker HE et al Assessing theintroduction of universal human papillomavirus vaccinationfor preadolescent girls in The Netherlands Vaccine 2007 256245ndash56
8 van Lier EA Oomen PJ Oostenbrug MWM et alImmunization coverage National ImmunizationProgramme in the Netherlands Year of report 2009[Vaccinatiegraad Rijksvaccinatieprogramma NederlandVerslagjaar 2009] Bilthoven RIVM 2009
9 Zwakhals SLN van Lier EA van HPV (cohort 1997) bymunicipality 2012 [HPV (cohort 1997) per gemeente2012] In Dutch National Atlas of Public HealthBilthoven RIVM 2012 (httpwwwzorgatlasnlpreventievaccinaties-en-screeninghpv-cohort-1997-vaccinatiegraad-per-gemeente-2012 accessed 2 September 2013)
10 Brabin L Roberts SA Stretch R et al A survey of adolescentexperiences of human papillomavirus vaccination in theManchester study Br J cancer 2009 101 1502ndash4
11 Brabin L Roberts SA Kitchener HC A semi-qualitativestudy of attitudes to vaccinating adolescents against humanpapillomavirus without parental consent BMC PublicHealth 2007 7 20
12 Brewer NT Fazekas KI Predictors of HPV vaccine accept-ability A theory-informed systematic review Prev Med2007 45 107ndash14
13 Kahn JA Rosenthal SL Jin Y et al Rates of human papillo-mavirus vaccination attitudes about vaccination and humanpapillomavirus prevalence in young women Obstet Gynecol2008 111 1103ndash10
14 Askelson NM Campo S Lowe JB et al Using the theoryof planned behavior to predict mothersrsquo intentions to vaccin-ate their daughters against HPV J Sch Nurs 2010 26194ndash202
15 Ajzen I The theory of Planned Behavior Organ Behav HumDecis Process 1991 50 179ndash211
16 Becker MH The health belief model and personal healthbehavior Health Edu Monogr 1974 2 324ndash508
17 Chapman GB Coups EJ Emotions and preventive healthbehavior worry regret and influenza vaccination HealthPsychol 2006 25 82ndash90
18 Paulussen TG Hoekstra F Lanting CI et al Determinants ofDutch parentsrsquo decisions to vaccinate their child Vaccine2006 24 644ndash51
19 Kaplan KJ On the ambivalence-indifference problem inattitude theory and measurement A suggested modificationof the semantic differential technique Psychol Bull 1972 77361ndash372
20 Dormandy E Hankins M Marteau TM Attitudes and uptakeof a screening test The moderating role of ambivalencePsychol Health 2006 21 499ndash511
Predictors of HPV vaccination uptake
95
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
21 Hofman R van Empelen P Vogel I et al Parental decisionalstrategies regarding HPV vaccination prior to media debatesa focus-group study J Health Commun 2013 18 866ndash80
22 Brewer NT Gottlieb SL Reiter PL et al Longitudinal pre-dictors of human papillomavirus vaccine initiation amongadolescent girls in a high-risk geographic area Sex TransmDis 2011 38 197ndash204
23 Marlow LA Waller J Wardle J Trust and experience aspredictors of HPV vaccine acceptance Hum Vaccin 20073 171ndash5
24 Weinstein ND Perceived probability perceived severityand health-protective behavior Health Psychol 2000 1965ndash74
25 Marteau TM Dormandy E Michie S A measure of informedchoice Health Expect 2001 4 99ndash108
26 van den Berg M Timmermans DR Ten Kate LP et al Arepregnant women making informed choices about prenatalscreening Genet Med 2005 7 332ndash8
27 Tiro JA Diamond PM Perz CA et al Validation of scalesmeasuring attitudes and norms related to mammographyscreening in women veterans Health Psychol 2005 24555ndash66
28 Marlow LAV Waller J Wardle J Parental attitudes to pre-pubertal HPV vaccination Vaccine 2007 25 1945ndash52
29 Stalmeier PF Roosmalen MS Verhoef LC et al Thedecision evaluation scales Patient Educ Couns 2005 57286ndash93
30 Gilbert LA Hanson GR Perceptions of parental role respon-sibilities among working people Development of a compre-hensive measure J Marriage Fam 1983 45 203ndash12
31 Korfage IJ van Ballegooijen M Wauben B et al Informedchoice on Pap smear still limited by lack of knowledge on the
meaning of false-positive or false-negative test resultsPatient Educ Couns 2011 85 214ndash8
32 Thompson MM Zanna MP The conflicted individual per-sonality-based and domain specific antecedents of ambiva-lent social attitudes J Pers 1995 63 259ndash88
33 General Medical Council Seeking Patientsrsquo Consent TheEthical Considerations London GMC 1998
34 Minister of Health Letter about screening [Kaderbriefscreening] PGZP 2848440 Ministry of Health Welfareand Sports The Hague 2008
35 Aiken LS West RR Multiple Regression Testing andInterpreting Interactions Newbury Park CA Sage 1991
36 Krawczyk AL Perez S Lau E et al Human papillomavirusvaccination intentions and uptake in college women HealthPsychol 2012 31 685ndash93
37 Newby-Clark IR McGregor I Zanna MP Thinking andcaring about cognitive inconsistency when and for whomdoes attitudinal ambivalence feel uncomfortable J Pers SocPsychol 2002 82 157ndash66
38 Nordgren LF van Harreveld F van der Pligt J Ambivalencediscomfort and motivated information processing J ExperSoc Psychol 2006 42 252ndash8
39 Clark JK Wegener DT Fabrigar LR Attitudinal ambiva-lence and message-based persuasion motivated processingof proattitudinal information and avoidance of counterattitu-dinal information Pers Soc Psychol Bull 2008 34 565ndash77
40 van Keulen HM Otten W Ruiter RA et al Determinants ofHPV vaccination intentions among Dutch girls and theirmothers a cross-sectional study BMC Public Health 201313 111
R Hofman et al
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nloaded from
daughter vaccinated In other words parents who
had both positive attitudes and were ambivalent to-
ward HPV vaccination became even more positive
because they elaborated only information in favor of
HPV vaccination This may imply that this lsquobiasedrsquo
information processing has a negative impact on
informed decision making although parents will
have gained more knowledge during their efforts
to resolve their ambivalence
Assessing decisional factors related to HPV vac-
cination both before and after the decision-making
process about uptake provided a unique opportun-
ity to determine changes in those factors over time
As uptake was predicted by intention and intention
was highly correlated with attitude (rfrac14 084) (at
baseline) we think it is relevant to show which
factors are important for changes in attitude over
time Our results show that a more positive attitude
toward HPV vaccination over time was associated
with an increase in trust in the vaccine and in
social norm over time and a decrease in ambiva-
lence toward HPV vaccination over time This
latter factor was related to an increase in feeling
informed about HPV vaccination and an increase
in trust in the vaccine over time In summary over
time parents felt better informed became less am-
bivalent and had more trust in the vaccine These
results are in accordance with our finding that
girls who had to decide with their parents whether
or not to be vaccinated in 2011 were more likely
to be vaccinated than those who had to decide
in 2010
An important finding is that knowledge about the
duration of protection was low at both baseline and
follow-up For instance about 65 of the parents
thought that protection lasts 30 years or even life-
long As the duration of protection is still unknown
it is important that parents and girls know that
booster vaccinations might be needed in the future
When we applied a cut-off of four or five correct
knowledge items (out of seven) then the rates
of informed choice about uptake were not high
66 and 44 respectively However this finding
should be interpreted with caution because the
time period between the assessment of knowledge
and the last vaccination out of three shots was
1 month (decision in 2011) or 14 months (decision
in 2010) In educational material it should be clearly
stated what is known and not yet known about HPV
vaccination
Study strengths include the longitudinal design
as recommended by authors of a cross-sectional
study [40] the high (absolute) number of respond-
ents of the baseline (nfrac14 1725) and follow-up ques-
tionnaires (nfrac14 793) and the high response rate of the
follow-up questionnaire (74)
Limitations
A limitation was the low response rate of the base-
line questionnaire (30) which might be due to the
length of the questionnaire Our sample may there-
fore not be representative of the general population
as few parents had a low educational level Also
demographic characteristics of the follow-up group
were slightly different from those of the baseline
group with more parents being better educated
and well-off at follow-up These parents might pos-
sibly be more likely than those in the wider popula-
tion to seek to reduce high ambivalence by
searching information allowing them to respond
positively to the vaccine invitationmdashrather than do
nothing
Conclusion
In conclusion this study shows that intention a later
versus earlier decision about uptake and anticipated
regretworry about abstaining from vaccination
were predictors of uptake Anticipated regret was a
common predictor of intention and uptake and thus
an important factor in the decision-making process
about HPV vaccination In turn predictors of inten-
tion like social norm and trust in the vaccine are
also important when deciding about HPV vaccin-
ation Over time parents felt better informed
became less ambivalent and had more trust in the
vaccine
Practice implications
This study shows the usefulness of including affect-
ive factors in studies examining HPV vaccination
R Hofman et al
94
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nloaded from
behavior as anticipated regret trust in the vaccine
and ambivalence were found to play a role in the
decision making about uptake However it is also
important that parents are enabled to base their
decision about HPV vaccination of their daughter
on decision relevant knowledge As these results
suggest that people need sufficient time to decide
about the uptake of a new vaccine we recommend
a well-balanced stepwise process of implementa-
tion that is let parents first become aware of the
link between HPV and cervical cancer then provide
them with balanced information about all the
knowns and also the unknowns of HPV vaccination
and then finally offer them the opportunity to have
their daughter vaccinated As two-third of parents
wrongly thought that protection lasts 30 years or
even lifelong educational material should clearly
state that booster vaccinations might be needed in
the future
Acknowledgements
The authors thank the Dutch Cancer Society for
financial support and the participants for their
contribution to the study
Funding
The Dutch Cancer Society [EMCR 2008-3992
EMCR 2009-4561]
Conflict of interest statement
None declared
References
1 Karim-Kos HE de Vries E Soerjomataram I et al Recenttrends of cancer in Europe a combined approach of inci-dence survival and mortality for 17 cancer sites since the1990s Eur J Cancer 2008 44 1345ndash89
2 Bosch FX Lorincz A Munoz N et al The causal relationbetween human papillomavirus and cervical cancer J ClinPathol 2002 55 244ndash65
3 Walboomers JM Jacobs MV Manos MM et al Humanpapillomavirus is a necessary cause of invasive cervicalcancer worldwide J Pathol 1999 189 12ndash9
4 Munoz N Bosch FX Castellsague X et al Against whichhuman papillomavirus types shall we vaccinate and screenThe international perspective Int J Cancer 2004 111278ndash85
5 Koutsky LA Holmes KK Critchlow CW et al A cohortstudy of the risk of cervical intraepithelial neoplasia grade2 or 3 in relation to papillomavirus infection N Engl J Med1992 327 1272ndash8
6 Woodman CB Collins S Winter H et al Natural history ofcervical human papillomavirus infection in young women alongitudinal cohort study Lancet 2001 357 1831ndash6
7 Boot HJ Wallenburg I de Melker HE et al Assessing theintroduction of universal human papillomavirus vaccinationfor preadolescent girls in The Netherlands Vaccine 2007 256245ndash56
8 van Lier EA Oomen PJ Oostenbrug MWM et alImmunization coverage National ImmunizationProgramme in the Netherlands Year of report 2009[Vaccinatiegraad Rijksvaccinatieprogramma NederlandVerslagjaar 2009] Bilthoven RIVM 2009
9 Zwakhals SLN van Lier EA van HPV (cohort 1997) bymunicipality 2012 [HPV (cohort 1997) per gemeente2012] In Dutch National Atlas of Public HealthBilthoven RIVM 2012 (httpwwwzorgatlasnlpreventievaccinaties-en-screeninghpv-cohort-1997-vaccinatiegraad-per-gemeente-2012 accessed 2 September 2013)
10 Brabin L Roberts SA Stretch R et al A survey of adolescentexperiences of human papillomavirus vaccination in theManchester study Br J cancer 2009 101 1502ndash4
11 Brabin L Roberts SA Kitchener HC A semi-qualitativestudy of attitudes to vaccinating adolescents against humanpapillomavirus without parental consent BMC PublicHealth 2007 7 20
12 Brewer NT Fazekas KI Predictors of HPV vaccine accept-ability A theory-informed systematic review Prev Med2007 45 107ndash14
13 Kahn JA Rosenthal SL Jin Y et al Rates of human papillo-mavirus vaccination attitudes about vaccination and humanpapillomavirus prevalence in young women Obstet Gynecol2008 111 1103ndash10
14 Askelson NM Campo S Lowe JB et al Using the theoryof planned behavior to predict mothersrsquo intentions to vaccin-ate their daughters against HPV J Sch Nurs 2010 26194ndash202
15 Ajzen I The theory of Planned Behavior Organ Behav HumDecis Process 1991 50 179ndash211
16 Becker MH The health belief model and personal healthbehavior Health Edu Monogr 1974 2 324ndash508
17 Chapman GB Coups EJ Emotions and preventive healthbehavior worry regret and influenza vaccination HealthPsychol 2006 25 82ndash90
18 Paulussen TG Hoekstra F Lanting CI et al Determinants ofDutch parentsrsquo decisions to vaccinate their child Vaccine2006 24 644ndash51
19 Kaplan KJ On the ambivalence-indifference problem inattitude theory and measurement A suggested modificationof the semantic differential technique Psychol Bull 1972 77361ndash372
20 Dormandy E Hankins M Marteau TM Attitudes and uptakeof a screening test The moderating role of ambivalencePsychol Health 2006 21 499ndash511
Predictors of HPV vaccination uptake
95
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
21 Hofman R van Empelen P Vogel I et al Parental decisionalstrategies regarding HPV vaccination prior to media debatesa focus-group study J Health Commun 2013 18 866ndash80
22 Brewer NT Gottlieb SL Reiter PL et al Longitudinal pre-dictors of human papillomavirus vaccine initiation amongadolescent girls in a high-risk geographic area Sex TransmDis 2011 38 197ndash204
23 Marlow LA Waller J Wardle J Trust and experience aspredictors of HPV vaccine acceptance Hum Vaccin 20073 171ndash5
24 Weinstein ND Perceived probability perceived severityand health-protective behavior Health Psychol 2000 1965ndash74
25 Marteau TM Dormandy E Michie S A measure of informedchoice Health Expect 2001 4 99ndash108
26 van den Berg M Timmermans DR Ten Kate LP et al Arepregnant women making informed choices about prenatalscreening Genet Med 2005 7 332ndash8
27 Tiro JA Diamond PM Perz CA et al Validation of scalesmeasuring attitudes and norms related to mammographyscreening in women veterans Health Psychol 2005 24555ndash66
28 Marlow LAV Waller J Wardle J Parental attitudes to pre-pubertal HPV vaccination Vaccine 2007 25 1945ndash52
29 Stalmeier PF Roosmalen MS Verhoef LC et al Thedecision evaluation scales Patient Educ Couns 2005 57286ndash93
30 Gilbert LA Hanson GR Perceptions of parental role respon-sibilities among working people Development of a compre-hensive measure J Marriage Fam 1983 45 203ndash12
31 Korfage IJ van Ballegooijen M Wauben B et al Informedchoice on Pap smear still limited by lack of knowledge on the
meaning of false-positive or false-negative test resultsPatient Educ Couns 2011 85 214ndash8
32 Thompson MM Zanna MP The conflicted individual per-sonality-based and domain specific antecedents of ambiva-lent social attitudes J Pers 1995 63 259ndash88
33 General Medical Council Seeking Patientsrsquo Consent TheEthical Considerations London GMC 1998
34 Minister of Health Letter about screening [Kaderbriefscreening] PGZP 2848440 Ministry of Health Welfareand Sports The Hague 2008
35 Aiken LS West RR Multiple Regression Testing andInterpreting Interactions Newbury Park CA Sage 1991
36 Krawczyk AL Perez S Lau E et al Human papillomavirusvaccination intentions and uptake in college women HealthPsychol 2012 31 685ndash93
37 Newby-Clark IR McGregor I Zanna MP Thinking andcaring about cognitive inconsistency when and for whomdoes attitudinal ambivalence feel uncomfortable J Pers SocPsychol 2002 82 157ndash66
38 Nordgren LF van Harreveld F van der Pligt J Ambivalencediscomfort and motivated information processing J ExperSoc Psychol 2006 42 252ndash8
39 Clark JK Wegener DT Fabrigar LR Attitudinal ambiva-lence and message-based persuasion motivated processingof proattitudinal information and avoidance of counterattitu-dinal information Pers Soc Psychol Bull 2008 34 565ndash77
40 van Keulen HM Otten W Ruiter RA et al Determinants ofHPV vaccination intentions among Dutch girls and theirmothers a cross-sectional study BMC Public Health 201313 111
R Hofman et al
96
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
behavior as anticipated regret trust in the vaccine
and ambivalence were found to play a role in the
decision making about uptake However it is also
important that parents are enabled to base their
decision about HPV vaccination of their daughter
on decision relevant knowledge As these results
suggest that people need sufficient time to decide
about the uptake of a new vaccine we recommend
a well-balanced stepwise process of implementa-
tion that is let parents first become aware of the
link between HPV and cervical cancer then provide
them with balanced information about all the
knowns and also the unknowns of HPV vaccination
and then finally offer them the opportunity to have
their daughter vaccinated As two-third of parents
wrongly thought that protection lasts 30 years or
even lifelong educational material should clearly
state that booster vaccinations might be needed in
the future
Acknowledgements
The authors thank the Dutch Cancer Society for
financial support and the participants for their
contribution to the study
Funding
The Dutch Cancer Society [EMCR 2008-3992
EMCR 2009-4561]
Conflict of interest statement
None declared
References
1 Karim-Kos HE de Vries E Soerjomataram I et al Recenttrends of cancer in Europe a combined approach of inci-dence survival and mortality for 17 cancer sites since the1990s Eur J Cancer 2008 44 1345ndash89
2 Bosch FX Lorincz A Munoz N et al The causal relationbetween human papillomavirus and cervical cancer J ClinPathol 2002 55 244ndash65
3 Walboomers JM Jacobs MV Manos MM et al Humanpapillomavirus is a necessary cause of invasive cervicalcancer worldwide J Pathol 1999 189 12ndash9
4 Munoz N Bosch FX Castellsague X et al Against whichhuman papillomavirus types shall we vaccinate and screenThe international perspective Int J Cancer 2004 111278ndash85
5 Koutsky LA Holmes KK Critchlow CW et al A cohortstudy of the risk of cervical intraepithelial neoplasia grade2 or 3 in relation to papillomavirus infection N Engl J Med1992 327 1272ndash8
6 Woodman CB Collins S Winter H et al Natural history ofcervical human papillomavirus infection in young women alongitudinal cohort study Lancet 2001 357 1831ndash6
7 Boot HJ Wallenburg I de Melker HE et al Assessing theintroduction of universal human papillomavirus vaccinationfor preadolescent girls in The Netherlands Vaccine 2007 256245ndash56
8 van Lier EA Oomen PJ Oostenbrug MWM et alImmunization coverage National ImmunizationProgramme in the Netherlands Year of report 2009[Vaccinatiegraad Rijksvaccinatieprogramma NederlandVerslagjaar 2009] Bilthoven RIVM 2009
9 Zwakhals SLN van Lier EA van HPV (cohort 1997) bymunicipality 2012 [HPV (cohort 1997) per gemeente2012] In Dutch National Atlas of Public HealthBilthoven RIVM 2012 (httpwwwzorgatlasnlpreventievaccinaties-en-screeninghpv-cohort-1997-vaccinatiegraad-per-gemeente-2012 accessed 2 September 2013)
10 Brabin L Roberts SA Stretch R et al A survey of adolescentexperiences of human papillomavirus vaccination in theManchester study Br J cancer 2009 101 1502ndash4
11 Brabin L Roberts SA Kitchener HC A semi-qualitativestudy of attitudes to vaccinating adolescents against humanpapillomavirus without parental consent BMC PublicHealth 2007 7 20
12 Brewer NT Fazekas KI Predictors of HPV vaccine accept-ability A theory-informed systematic review Prev Med2007 45 107ndash14
13 Kahn JA Rosenthal SL Jin Y et al Rates of human papillo-mavirus vaccination attitudes about vaccination and humanpapillomavirus prevalence in young women Obstet Gynecol2008 111 1103ndash10
14 Askelson NM Campo S Lowe JB et al Using the theoryof planned behavior to predict mothersrsquo intentions to vaccin-ate their daughters against HPV J Sch Nurs 2010 26194ndash202
15 Ajzen I The theory of Planned Behavior Organ Behav HumDecis Process 1991 50 179ndash211
16 Becker MH The health belief model and personal healthbehavior Health Edu Monogr 1974 2 324ndash508
17 Chapman GB Coups EJ Emotions and preventive healthbehavior worry regret and influenza vaccination HealthPsychol 2006 25 82ndash90
18 Paulussen TG Hoekstra F Lanting CI et al Determinants ofDutch parentsrsquo decisions to vaccinate their child Vaccine2006 24 644ndash51
19 Kaplan KJ On the ambivalence-indifference problem inattitude theory and measurement A suggested modificationof the semantic differential technique Psychol Bull 1972 77361ndash372
20 Dormandy E Hankins M Marteau TM Attitudes and uptakeof a screening test The moderating role of ambivalencePsychol Health 2006 21 499ndash511
Predictors of HPV vaccination uptake
95
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
21 Hofman R van Empelen P Vogel I et al Parental decisionalstrategies regarding HPV vaccination prior to media debatesa focus-group study J Health Commun 2013 18 866ndash80
22 Brewer NT Gottlieb SL Reiter PL et al Longitudinal pre-dictors of human papillomavirus vaccine initiation amongadolescent girls in a high-risk geographic area Sex TransmDis 2011 38 197ndash204
23 Marlow LA Waller J Wardle J Trust and experience aspredictors of HPV vaccine acceptance Hum Vaccin 20073 171ndash5
24 Weinstein ND Perceived probability perceived severityand health-protective behavior Health Psychol 2000 1965ndash74
25 Marteau TM Dormandy E Michie S A measure of informedchoice Health Expect 2001 4 99ndash108
26 van den Berg M Timmermans DR Ten Kate LP et al Arepregnant women making informed choices about prenatalscreening Genet Med 2005 7 332ndash8
27 Tiro JA Diamond PM Perz CA et al Validation of scalesmeasuring attitudes and norms related to mammographyscreening in women veterans Health Psychol 2005 24555ndash66
28 Marlow LAV Waller J Wardle J Parental attitudes to pre-pubertal HPV vaccination Vaccine 2007 25 1945ndash52
29 Stalmeier PF Roosmalen MS Verhoef LC et al Thedecision evaluation scales Patient Educ Couns 2005 57286ndash93
30 Gilbert LA Hanson GR Perceptions of parental role respon-sibilities among working people Development of a compre-hensive measure J Marriage Fam 1983 45 203ndash12
31 Korfage IJ van Ballegooijen M Wauben B et al Informedchoice on Pap smear still limited by lack of knowledge on the
meaning of false-positive or false-negative test resultsPatient Educ Couns 2011 85 214ndash8
32 Thompson MM Zanna MP The conflicted individual per-sonality-based and domain specific antecedents of ambiva-lent social attitudes J Pers 1995 63 259ndash88
33 General Medical Council Seeking Patientsrsquo Consent TheEthical Considerations London GMC 1998
34 Minister of Health Letter about screening [Kaderbriefscreening] PGZP 2848440 Ministry of Health Welfareand Sports The Hague 2008
35 Aiken LS West RR Multiple Regression Testing andInterpreting Interactions Newbury Park CA Sage 1991
36 Krawczyk AL Perez S Lau E et al Human papillomavirusvaccination intentions and uptake in college women HealthPsychol 2012 31 685ndash93
37 Newby-Clark IR McGregor I Zanna MP Thinking andcaring about cognitive inconsistency when and for whomdoes attitudinal ambivalence feel uncomfortable J Pers SocPsychol 2002 82 157ndash66
38 Nordgren LF van Harreveld F van der Pligt J Ambivalencediscomfort and motivated information processing J ExperSoc Psychol 2006 42 252ndash8
39 Clark JK Wegener DT Fabrigar LR Attitudinal ambiva-lence and message-based persuasion motivated processingof proattitudinal information and avoidance of counterattitu-dinal information Pers Soc Psychol Bull 2008 34 565ndash77
40 van Keulen HM Otten W Ruiter RA et al Determinants ofHPV vaccination intentions among Dutch girls and theirmothers a cross-sectional study BMC Public Health 201313 111
R Hofman et al
96
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from
21 Hofman R van Empelen P Vogel I et al Parental decisionalstrategies regarding HPV vaccination prior to media debatesa focus-group study J Health Commun 2013 18 866ndash80
22 Brewer NT Gottlieb SL Reiter PL et al Longitudinal pre-dictors of human papillomavirus vaccine initiation amongadolescent girls in a high-risk geographic area Sex TransmDis 2011 38 197ndash204
23 Marlow LA Waller J Wardle J Trust and experience aspredictors of HPV vaccine acceptance Hum Vaccin 20073 171ndash5
24 Weinstein ND Perceived probability perceived severityand health-protective behavior Health Psychol 2000 1965ndash74
25 Marteau TM Dormandy E Michie S A measure of informedchoice Health Expect 2001 4 99ndash108
26 van den Berg M Timmermans DR Ten Kate LP et al Arepregnant women making informed choices about prenatalscreening Genet Med 2005 7 332ndash8
27 Tiro JA Diamond PM Perz CA et al Validation of scalesmeasuring attitudes and norms related to mammographyscreening in women veterans Health Psychol 2005 24555ndash66
28 Marlow LAV Waller J Wardle J Parental attitudes to pre-pubertal HPV vaccination Vaccine 2007 25 1945ndash52
29 Stalmeier PF Roosmalen MS Verhoef LC et al Thedecision evaluation scales Patient Educ Couns 2005 57286ndash93
30 Gilbert LA Hanson GR Perceptions of parental role respon-sibilities among working people Development of a compre-hensive measure J Marriage Fam 1983 45 203ndash12
31 Korfage IJ van Ballegooijen M Wauben B et al Informedchoice on Pap smear still limited by lack of knowledge on the
meaning of false-positive or false-negative test resultsPatient Educ Couns 2011 85 214ndash8
32 Thompson MM Zanna MP The conflicted individual per-sonality-based and domain specific antecedents of ambiva-lent social attitudes J Pers 1995 63 259ndash88
33 General Medical Council Seeking Patientsrsquo Consent TheEthical Considerations London GMC 1998
34 Minister of Health Letter about screening [Kaderbriefscreening] PGZP 2848440 Ministry of Health Welfareand Sports The Hague 2008
35 Aiken LS West RR Multiple Regression Testing andInterpreting Interactions Newbury Park CA Sage 1991
36 Krawczyk AL Perez S Lau E et al Human papillomavirusvaccination intentions and uptake in college women HealthPsychol 2012 31 685ndash93
37 Newby-Clark IR McGregor I Zanna MP Thinking andcaring about cognitive inconsistency when and for whomdoes attitudinal ambivalence feel uncomfortable J Pers SocPsychol 2002 82 157ndash66
38 Nordgren LF van Harreveld F van der Pligt J Ambivalencediscomfort and motivated information processing J ExperSoc Psychol 2006 42 252ndash8
39 Clark JK Wegener DT Fabrigar LR Attitudinal ambiva-lence and message-based persuasion motivated processingof proattitudinal information and avoidance of counterattitu-dinal information Pers Soc Psychol Bull 2008 34 565ndash77
40 van Keulen HM Otten W Ruiter RA et al Determinants ofHPV vaccination intentions among Dutch girls and theirmothers a cross-sectional study BMC Public Health 201313 111
R Hofman et al
96
at University of T
oronto Library on O
ctober 2 2014httpheroxfordjournalsorg
Dow
nloaded from