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

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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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oronto Library on O

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nloaded from