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Vaccine 31 (2013) 1051–1056

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Vaccine
journal homepage: www.elsevier.com/locate/vaccine

Knowledge and awareness of HPV and the HPV vaccine among young women in
the first routinely vaccinated cohort in England
Harriet L. Bowyer a , Laura A.V. Marlow a , Sam Hibbitts b , Kevin G. Pollock c , Jo Waller a,∗
a
Cancer Research UK Health Behaviour Research Centre, Research Department of Epidemiology and Public Health, UCL, Gower Street, London, WC1E 6BT, United Kingdom
b
HPV Research Group, Institute of Cancer and Genetics, School of Medicine, Cardiff University, Cardiff, CF14 4XN, United Kingdom
c
Vaccine Preventable Diseases, NHS National Services Scotland, Health Protection Scotland, Cadogan Street, Glasgow, G2 6QE, United Kingdom

a r t i c l e i n f o a b s t r a c t

Article history: A national school-based human papillomavirus (HPV) vaccination programme has been available for
Received 4 October 2012 12–13 year old females in the UK since 2008, offering protection against HPV types 16 and 18, which are
Received in revised form responsible for the majority of cervical cancer. Little is known about HPV knowledge in girls who have
11 December 2012
been offered the vaccine. Girls offered the school-based vaccine in the first routine cohort (n = 1033) were
Accepted 14 December 2012
recruited from 13 schools in London three years post-vaccination. Participants completed a questionnaire
Available online 28 December 2012
about HPV awareness, knowledge about HPV and the vaccine, and demographic characteristics includ-
ing vaccine status. About a fifth of the girls reported they were unaware of the HPV infection. Among
Keywords:
HPV infection
those who reported being aware of HPV (n = 759) knowledge was relatively low. Approximately half of
Knowledge the participants knew that HPV infection causes cervical cancer, condoms can reduce the risk of trans-
Adolescents mission and that cervical screening is needed regardless of vaccination status. These results are helpful
Vaccination in benchmarking HPV-related knowledge in vaccinated girls and could be used in the development of
Cervical cancer appropriate educational messages to accompany the first cervical screening invitation in this cohort in
the future.
© 2012 Elsevier Ltd. All rights reserved.

1. Introduction adult women surveyed were able to recognise HPV infection as a


risk factor for cervical cancer development [13]. Studies assessing
In September 2008, a free national programme was introduced HPV knowledge in young females have generally focused on knowl-
in the UK offering 12–13 year old females a bivalent vaccination that edge prior to the introduction of the HPV vaccine [14], but it is also
protects against the two high-risk types of human papillomavirus important to assess the knowledge of those who have been involved
(HPV) responsible for approximately 70% of cervical cancers [1]. in the vaccination programme, as this could potentially have an
Prior to vaccination all eligible girls are provided with an informa- impact on future behaviours relating to sexual health and cervical
tion leaflet from the Department of Health, sent to their homes by screening attendance. It has been suggested that HPV vaccination
post. The leaflet includes information about the link between HPV could provide a ‘teachable moment’ for parents to discuss sex and
and cervical cancer, the sexually transmitted nature of HPV, the sexual health with their adolescent daughters [15,16]. Equally, it
need for three doses of the vaccine and the need to attend cervi- could provide an opportunity to inform girls about cervical can-
cal screening in the future [2]. Most girls in the first routine cohort cer and the recommendation to attend for screening when they
were offered the vaccine at school (94.2%) within the UK [3]. Uptake are invited (currently at 25 years in England; 20 years in Scotland
rates have been relatively high, with 84% of girls offered the vaccine and Wales). With the time delay between HPV vaccination (12–13
receiving all three doses in 2010/2011 in England [4] and similar years) and cervical screening attendance (20–25 years) it will be
coverage in Scotland and Wales [5,6]. important to reiterate these messages closer to the time of the first
Prior to the introduction of HPV vaccination programmes, screening invitation.
awareness of HPV and its relationship with cervical cancer was low Little is known about HPV knowledge in girls who have been
in a variety of population groups, both in the UK [7–11] and else- offered the vaccine. A small body of qualitative research focusing on
where [12]. Recently published data from the UK showed that a vaccinated cohorts suggests that HPV knowledge is generally low.
year after the start of the programme, fewer than half (46%) of the These studies suggest that girls know little about how the human
papillomavirus is transmitted [17], how to reduce the risk of HPV
infection [18], or about the link between HPV and cervical cancer
∗ Corresponding author. Tel.: +44 0 20 7679 5958; fax: +44 0 20 7679 8354. [17,18]. Furthermore, girls are unclear about the level or duration
E-mail address: j.waller@ucl.ac.uk (J. Waller). of protection the HPV vaccine offers [17–19] and lack knowledge

0264-410X/$ – see front matter © 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.vaccine.2012.12.038
1052 H.L. Bowyer et al. / Vaccine 31 (2013) 1051–1056

about the need for future cervical screening [17]. In one study completion all participants received a debriefing sheet containing
involving 87 girls, just over half were aware of cervical screening further information about HPV.
and the need to attend in the future [18]. While these qualitative Participants were asked about their date of birth, ethnicity and
studies have helped to map the range of girls’ knowledge after the religion. Household income was indexed by self-reported FSME
implementation of HPV vaccination programmes, larger quantita- with individuals classified as ‘eligible’ or ‘not eligible’ for free school
tive studies are needed in order to ascertain knowledge within a meals. Participants’ awareness of HPV was assessed using the ques-
representative sample. Previous studies in the US have shown that tion ‘Before today, had you heard of HPV?’; this question has been
vaccinated and unvaccinated girls have similar levels of knowledge used previously [25]. After a brief description of the vaccine, vac-
about HPV and the HPV vaccine [20,21]. Licht et al. [20] found that cine status was assessed by asking participants to tick a box that
regardless of vaccine status, respondents lacked knowledge about best described them (response options: ‘I have had all 3 doses of the
the link between HPV and genital warts, HPV transmission and the HPV vaccine’; ‘I have had 1 or 2 doses of the HPV vaccine’; ‘I have
fact that HPV infection is as common in men as in women. The only been offered the HPV vaccine but I haven’t had it’; ‘I have not been
statistically significant difference in knowledge by vaccine status offered the HPV vaccine’; ‘I don’t know’). Knowledge of HPV was
was a greater awareness in those individuals who had received at assessed in those who had heard of it using 21 statements about
least one dose of the HPV vaccine, that HPV causes genital warts. HPV and the HPV vaccine and asking participants to rate them as
Caskey et al. [21] found that vaccinated respondents were more ‘true’ or ‘false’ (there was also a ‘don’t know’ option). Items were re-
likely to know that the HPV vaccine protects against cervical can- coded into responses that were ‘correct’, ‘incorrect’ or ‘don’t know’.
cer, and that women who receive the HPV vaccine should continue A total knowledge score was then derived for those with no more
using condoms during sexual intercourse. than five out of 21 items missing (i.e. allowing for approximately
This study aimed to extend this research to the UK, using quan- 25% missing data) by summing the number of correct responses
titative methods to examine knowledge about HPV and the HPV (possible range 0–21). The knowledge measure has been subjected
vaccine, in girls based in London, England, three years after the to rigorous psychometric evaluation in population-based samples
introduction of routine school-based vaccination. [26]. The study was approved by the UCL research ethics committee
(ref: 0630/002).
2. Materials and methods

In September 2011, young women in school Year 11 (aged 15–16 2.1. Analysis
years) were recruited from 13 schools in London, England. These
girls were part of the first cohort to have been offered the HPV vac- We used complex samples chi-square tests, clustering by school,
cine in the NHS school-based vaccination programme in 2008–9. A to examine demographic differences between girls who had heard
sampling frame was created using level of Free School Meal Eli- of HPV and girls who had not, and to examine demographic differ-
gibility (FSME)1 and General Certificate in Secondary Education ences in HPV knowledge. Adjusting for correlation or clustering of
(GCSE) attainment as indicators of socio-economic status (SES). data within schools is needed to obtain unbiased tests of signifi-
Schools were categorised as being above or below the national cance. Analyses were performed using SPSS v20 [27].
average on each of these metrics (23% FSME [23] and 53% GCSE
(pupils attaining 5 A*–C grades including English and Maths [24])).
All government-funded (state) schools with female pupils and 3. Results
reported HPV uptake within 10% of the national average [3] (n = 89)
were entered into the sampling frame.2 Schools in each cell of the 3.1. Sample characteristics
sampling frame were selected at random and contacted until the
target sample of 1000 participants was reached. Out of 89 schools, Over 98% of girls approached agreed to participate in the study
19 (21%) refused to participate (primarily for reasons related to (n = 1033; see Fig. 1). Non-participation was either due to parental
scheduling difficulties) and 13 were included. The schools included (n = 5) or participant (n = 9) refusal to consent. Demographic charac-
in the sample did not differ from the rest of those in the samp- teristics of the sample are shown in Table 1. All participants were 15
ling frame in terms of HPV uptake (2 (1,89) = 1.19, p = .276), FSME or 16 years old. Most were of White or Black ethnicity, were Chris-
(2 (1,89) = 3.63, p = .057) or GCSE attainment (2 (1,89) = 1.19, tian or had no religious affiliation, and free school meal eligibility
p = .276). was 27%, in line with national figures [23].
One week before the study took place, parents of Year 11 girls Individuals who had received at least one dose of the HPV
received an information sheet about the study, which included an vaccine were coded as ‘vaccinated’ (n = 792/1033; 76.6%). This
opt-out form; those that did not return the opt-out form to the included 71.2% who had received all three doses, and 5.4% who
school implied consent. had received 1–2 doses. A small number of girls reported that
Researchers visited the schools on a given day and all girls in they had not been offered the vaccine (n = 28). Of these, six indi-
attendance were invited to complete the questionnaire (see Sup- cated in a subsequent open question that they had in fact refused
plement 1). In each classroom a researcher explained the purposes the vaccine, so these were coded as ‘unvaccinated’ along with 98
and procedures of the study and all participants were given the who responded that they had not been vaccinated (total ‘unvac-
opportunity to read through an information sheet before comple- cinated’ = 10.1% (104/1033)). Twenty-two girls who reported not
ting the questionnaire. The questionnaire was then distributed to having been offered the vaccine,3 100 girls who did not know their
all participants, with consent inferred from completion of the ques- vaccine status and 15 girls with missing data (totalling n = 137)
tionnaire. The questionnaires were completed in silence and upon were excluded from analyses of vaccination status.

1
Children are eligible for free school meals if their parents are entitled to means-
3
tested welfare benefits from the UK government [22]. We excluded these respondents as their answers suggested that they were either
2
School-level data on uptake of HPV vaccine were only available for 162 out of not living in the UK at the time the vaccine was offered, or that their responses were
348 mixed/girls’ schools in London as Primary Care Trusts vary in whether they can unreliable – all 12-13 year old girls in England should have been offered the vaccine
provide this information. in 2008.
H.L. Bowyer et al. / Vaccine 31 (2013) 1051–1056 1053

Offered quesonnaire
(n=1047)

Refused to
parcipate
(parent=5;
parcipant=9)

Completed
quesonnaire (n=1033)

Missing data for


HPV awareness
(n=8)

Awareness analysis
(n=1025)

Aware of HPV (n=819) Unaware of HPV


(n=206)

Missing data for Excluded: >5


knowledge missing items on
items (n=50-66) knowledge
measure (n=60)

Knowledge item Knowledge score


analysis (n=753-769) analysis (n=759)

Fig. 1. Recruitment and sample size for each analysis.

Table 1
Chi-square associations (clustering by school) between demographic factors and awareness of HPV (n = 1025a ).

HPV aware n (row %) HPV unaware n (row %) 2 clustering by school (p-value)

All (n = 1025) 819 (80.0) 206 (20.0)


Age (Mean, SD, t-test) (n = 993) 15.8 (0.3) 15.8 (0.3) 163.21 (.691)

Ethnicity (n = 1015) 7.53 (.247)


White (n = 443) 351 (79.2) 92 (20.8)
Black (n = 244) 201 (82.4) 43 (17.6)
Asian (n = 193) 162 (83.9) 31 (16.1)
Other (n = 135) 98 (72.6) 37 (27.4)
Missing (n = 10) 7 (70.0) 3 (30.0)

Religion (n = 1022) 3.09 (.439)


Christian (n = 478) 388 (81.2) 90 (18.8)
None (n = 277) 212 (76.5) 65 (23.5)
Muslim (n = 199) 163 (81.9) 36 (18.1)
Other (n = 68) 53 (77.9) 15 (22.1)
Missing (n = 3) 3 (100.0) –

Self-reported FSMEb (n = 894) 0.13 (.780)


No (n = 616) 490 (79.5) 126 (20.5)
Yes (n = 278) 224 (80.6) 54 (19.4)
Missing (n = 131) 105 (80.2) 26 (19.8)

Vaccine status (≥1 dose) (n = 890) 12.26 (.017)


Vaccinated (n = 787) 683 (86.8) 104 (13.2)
Unvaccinated (n = 103) 76 (73.8) 27 (26.2)
Missing (n = 135) 60 (44.4) 75 (55.6)
a
Missing data means that the n varies between analyses.
b
Free School Meal Eligibility.
1054 H.L. Bowyer et al. / Vaccine 31 (2013) 1051–1056

Table 2
Responses to knowledge items from sub-sample who had heard of HPV (n = 753–769)a .

Correct na (%) Incorrect na (%) Do not know na (%)

HPV knowledge items


HPV can be passed on during sex 538 (70.3) 36 (4.7) 191 (25.0)
Having many sexual partners increases the risk of getting HPV 480 (63.1) 40 (5.3) 241 (31.7)
Using condoms reduces the risk of getting HPV 440 (57.6) 55 (7.2) 269 (35.2)
HPV can be passed on by genital skin-to-skin contact 423 (55.4) 97 (12.7) 243 (31.8)
HPV can cause cervical cancer 404 (53.1) 46 (6.0) 311 (40.9)
A person could have HPV for many years without knowing it 396 (52.4) 29 (3.8) 331 (43.8)
HPV is rare (F) 269 (35.0) 90 (11.7) 410 (53.3)
There are many types of HPV 238 (31.3) 70 (9.2) 452 (59.5)
Having sex at an early age increases the risk of getting HPV 227 (29.9) 136 (17.9) 397 (52.2)
HPV can be cured with antibiotics (F) 224 (29.6) 84 (11.1) 449 (59.3)
Men cannot get HPV (F) 209 (27.5) 201 (26.5) 349 (46.0)
HPV always has visible signs or symptoms (F) 200 (26.1) 144 (18.8) 423 (55.1)
HPV can cause genital warts 177 (23.2) 68 (8.9) 517 (67.8)
HPV can cause HIV/AIDs (F) 142 (18.7) 170 (22.4) 448 (58.9)
Most sexually active people will get HPV at some point in their lives 132 (17.5) 202 (26.7) 422 (55.8)
HPV usually does not need any treatment 29 (3.8) 449 (59.0) 283 (37.2)

HPV vaccine knowledge items


HPV vaccines require three doses 257 (69.8) 20 (2.6) 208 (27.5)
Girls who have had the HPV vaccine do not need cervical screening (a smear or 399 (52.7) 41 (5.4) 317 (41.9)
Pap test) when they are older (F)
The HPV vaccine offers protection against most cervical cancers 354 (46.9) 42 (5.6) 359 (47.5)
Someone who has had an HPV vaccine cannot develop cervical cancer (F) 269 (35.7) 97 (12.9) 387 (51.4)
The HPV vaccine is most effective if given to people who have never had sex 236 (31.3) 97 (12.8) 422 (55.9)

F = Correct answer is ‘false’. For all other items, correct answer is ‘true’.
a
n varies slightly between items because of missing data.

3.2. Awareness of HPV (2 (1,662) = 0.11, p = .752), or vaccine status (2 (1,708) = 0.001,
p = .974)(see Table 3).
Eight girls had missing data for the question on HPV aware-
ness, leaving a sample of 1025 for analysis. Overall, 819 (80%)
respondents had heard of HPV, while 20% (n = 206) had not (see 4. Discussion
Fig. 1). There were no statistically significant differences between
those who had heard of HPV and those who had not in terms of This study is the first, to our knowledge, to use quantitative
ethnicity (2 (3,1015) = 7.53, p = .247), religion (2 (3,1022) = 3.09, methods to measure awareness and knowledge of HPV in a cohort
p = .439) or self-reported FSME (2 (1,894) = 0.13, p = .780). How- of girls who have been offered the HPV vaccine in the UK. Three
ever, vaccinated participants were statistically significantly more years after being offered the HPV vaccine in school as part of the
likely to have heard of HPV than unvaccinated participants (2 national programme in England, girls in our sample, 77% of whom
(1,890) = 12.26, p = .017). reported having received at least one vaccine dose, demonstrated
low HPV knowledge. A fifth of our respondents reported that they
had not heard of HPV, which may reflect the fact that the vaccine has
been widely publicised as ‘the cervical cancer vaccine’ rather than
3.3. HPV knowledge the HPV vaccine, in the British media [28]. Although HPV and its
link with cervical cancer development are described in the Depart-
Of the 819 participants who were aware of HPV, between 753 ment of Health information materials provided prior to vaccination,
and 769 responded to each of the 21 items assessing knowledge the focus is on cervical cancer prevention [2]. When we asked girls
about HPV and the vaccine (see Table 2). Only three items were who had heard of HPV to respond to true/false statements about
answered correctly by over 60% of respondents – that HPV can HPV and the vaccine, the mean number of correct responses was 8
be passed on during sex (70.3%), that having many sexual part- out of 21. This suggests that our sample overall had low levels of
ners increases the risk of getting HPV (63.1%) and that the vaccine knowledge about HPV and the HPV vaccine, supporting previous
requires three doses (69.8%). For nine of the items, the most fre- studies assessing HPV knowledge among adult women in the UK
quent response was ‘don’t know’. Only half (52.7%) knew that it is [7–11].
not true that girls who have been vaccinated will not need screening Our findings are consistent with previous qualitative and quan-
in the future. titative work demonstrating confusion about HPV infection and
A total knowledge score was calculated for 759 participants the HPV vaccine, uncertainty about protection offered and lack of
with complete data for at least 16 out of 21 items on the knowl- awareness about the need for future cervical screening [17–19].
edge measure (i.e. <25% missing data). The mean total score Information covering these areas was provided in a leaflet pub-
(pro-rated for those with missing data) was 8.30 (SD = 4.77) out lished by the Department of Health [2], but it seems that three years
of a possible score of 21. Participants were divided into ‘high’ on, girls had retained relatively little of the detail. There is some lit-
and ‘low’ knowledge groups using a median split. A total of 430 erature identifying problems with information provision; evidence
(56.7%) were classified as having low knowledge of HPV (0–9 cor- from the US suggests that the information physicians provide about
rect responses) and 329 (43.3%) were classified as having high HPV and the vaccine can be limited [29], and research conducted
knowledge (10–20 correct responses). There were no statisti- in Belgium found that patients seek HPV-related information on
cally significant differences between those with high and those the internet, even after speaking to their health care provider [30].
with low HPV knowledge in terms of ethnicity (2 (3,755) = 7.53, In the school-based programme in the UK, information provision
p = .705), religion (2 (3,756) = 1.24, p = .690), self-reported FSME relies primarily on a written leaflet rather than interactions with
H.L. Bowyer et al. / Vaccine 31 (2013) 1051–1056 1055

Table 3
Chi-square associations (clustering by school) between demographic factors and HPV knowledge (n = 759)a .

n (row %) with low knowledge n (row %) with high knowledge 2 (p-value)

All (n = 759) 430 (56.7) 329 (43.3)

Ethnicity (n = 755) 1.73 (.705)


White 191 (57.2) 143 (42.8)
Black 104 (58.1) 75 (41.9)
Asian 79 (52.0) 73 (48.0)
Other 53 (58.9) 37 (41.1)

Religion (n = 756) 1.24 (.690)


Christian 202 (56.4) 156 (43.6)
None 115 (57.5) 85 (42.5)
Muslim 87 (58.8) 61 (41.2)
Other 25 (50.0) 25 (50.0)

Self-reported FSMEb (n = 662) 0.11 (.752)


No 254 (55.5) 204 (44.5)
Yes 116 (56.9) 88 (43.1)

Vaccine status (n = 708) 0.01 (.974)


Vaccinated 349 (55.0) 286 (45.0)
Unvaccinated 40 (54.8) 33 (45.2)
a
Missing data means that the n varies between analyses.
b
Free School Meal Eligibility.

health professionals, and little is known about what nurses deliv- knowledge about the virus, the vaccine and the need for future
ering the vaccine tell girls as they are being vaccinated. screening. Our study provides a benchmark of knowledge about
It seems surprising, nevertheless, that only half of the respon- HPV and its relationship with cervical cancer development in a vac-
dents were aware that HPV can cause cervical cancer. It is important cinated cohort, which could be used in developing health education
that adolescents understand why they are being offered the HPV materials to support future uptake of the routine cervical screening
vaccine to ensure uptake remains high; research into HPV-related programme.
information provision and communication in the UK would help
assess whether more effective communication prior to, and at the Acknowledgements
point at which the vaccine is offered is necessary. Only half of the
respondents were aware that cervical screening is still necessary This work was carried out as part of a Cancer Research UK project
following vaccination. Cervical screening in England is not offered grant (A13254, PI Professor John Edmunds). We are grateful to the
until 25 years of age and so it may be premature to offer school- schools that worked with us to facilitate data collection and the
aged children information on cervical screening. However, it does girls who took part in the study.
highlight that healthcare providers should be aware of the need to Conflict of interest: All authors declare no conflict of interest that
communicate effectively regarding HPV infection, the HPV vaccine may have influenced this work.
and cervical screening with young women as they approach the Author contributions: JW conceived of the study. HB and JW col-
screening age. It was encouraging to see that almost a quarter of lected the data for the study. HB, LM and JW contributed to the
girls knew that HPV infection could cause genital warts, although analyses of the study and all authors contributed to the interpreta-
our participants had been offered the bivalent vaccine, which does tion of results and the writing of this paper and have approved the
not protect against genital warts. Encouraging schools to discuss final draft.
HPV infection, the HPV vaccine and cervical cancer within personal,
social, health and economic (PHSE) education lessons might be a
Appendix A. Supplementary data
way to integrate knowledge about HPV into broader health-related
issues.
Supplementary data associated with this article can be
The study benefited from a large sample size including girls from
found, in the online version, at http://dx.doi.org/10.1016/j.vaccine.
a range of ethnic and socioeconomic backgrounds, and the use of a
2012.12.038.
validated measure of HPV knowledge. However the study is limited
in that it was carried out in London and so the generalizability of
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