Professional Documents
Culture Documents
G Model
JVAC 14625 1–16
Vaccine
journal homepage: www.elsevier.com/locate/vaccine
1 Review
11 a r t i c l e i n f o a b s t r a c t
12
13 Article history: Background and objective: Two human papillomavirus vaccines were licenced in 2006/2007 for cervical
14 Received 9 May 2013 cancer prevention. National vaccination programmes for schoolgirls were subsequently introduced in
15 Received in revised form 22 August 2013 some European countries, North America and Australia. To understand factors influencing vaccine uptake
16 Accepted 28 August 2013
and to inform the development of appropriate UK educational materials, we aimed to synthesise evidence
Available online xxx
of girls’ and parents’ information needs, views and preferences regarding HPV vaccination.
17
Design: Systematic review and mixed method synthesis of qualitative and survey data.
18 Keywords:
Data sources: 12 electronic databases; bibliographies of included studies 1980 to August 2011.
19 Human papillomavirus
20 Vaccination
Review methods: Two reviewers independently screened papers and appraised study quality. Studies were
21 Cervical cancer synthesised collaboratively using framework methods for qualitative data, and survey results integrated
22 Systematic review where they supported, contrasted or added to the themes identified.
Results: Twenty-eight qualitative studies and 44 surveys were included. Where vaccination was offered,
uptake was high. Intention to decline was related to a preference for vaccinating later to avoid appearing to
condone early sexual activity, concerns about vaccine safety and low perception of risk of HPV infection.
Knowledge was poor and there were many misconceptions; participants tried to assess the potential
benefits and harms of vaccination but struggled to interpret limited information about HPV in the context
of existing knowledge about sexually transmitted infections and cancer.
Conclusion Many girls and their parents have limited understanding to an extent that impinges on their
ability to make informed choices about HPV vaccination and could impact on future uptake of cervical
screening. This is a considerable challenge to those who design and provide information, but getting the
messages right for this programme could help in developing patient information about other HPV related
cancers.
© 2013 Published by Elsevier Ltd.
23 Contents
24 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
25 2. Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
26 3. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
27 3.1. Summary of included studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
28 3.2. Study quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
29 3.3. Emergent themes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
30 3.3.1. Trying to decide on HPV vaccination – unanswered questions and concerns . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
31 3.3.2. The benefits, harms and misconceptions of HPV vaccination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Please cite this article in press as: Hendry M, et al. “HPV? Never heard of it!”: A systematic review of girls’ and parents’ information needs, views
and preferences about human papillomavirus vaccination. Vaccine (2013), http://dx.doi.org/10.1016/j.vaccine.2013.08.091
ARTICLE IN PRESS
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JVAC 14625 1–16
3.3.3. The perceived need for vaccination was affected by participants’ interpretation, or misinterpretation, of their own or their
children’s risk of HPV infection Confusion about the best method of HPV prevention was a barrier to vaccine acceptance . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
4. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
4.1. Summary of main findings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
4.2. How this study fits in . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
4.3. Study strengths and limitations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
4.4. Implications for research, and UK policy and practice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Appendix A. Supplementary data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
33Q3 Sexually transmitted human papillomavirus (HPV) types 16 and counts as data from qualitative studies [10]; we considered authors’ 83
34 18 account for 70% of cervical cancers. Two vaccines (Gardasil® findings to be syntheses of entire primary data-sets, of which 84
35 and Cervarix TM ), licenced in 2006 and 2007 respectively, were quotations were illustrative examples. Studies were synthesised 85
36 recommended for girls and young women aged 9–26 years. Both collaboratively using the framework approach [11]. Data were 86
37 are effective against HPV types 16 and 18 (Gardasil® additionally repeatedly read to achieve familiarity, themes were identified and 87
38 protects against HPV types 6 and 11, implicated in genital warts), organised into categories, reviewed and refined until both review- 88
39 and are recommended for large-scale use in national immunisa- ers agreed on the validity of the thematic framework. Data were 89
40 tion programmes [1]. Vaccination programmes typically target girls then coded, the framework applied and again reviewed and refined 90
41 aged 11–13 (i.e. before the age of likely sexual debut and there- until consensus was reached [12]. We first identified themes in the 91
42 fore exposure to HPV viruses) to provide maximum protection [2]. qualitative studies, as the best source of rich data that was most 92
43 Their success is dependent on high uptake, which is likely to be likely to illuminate people’s opinions, perceptions, attitudes and 93
44 influenced by people’s views, perceptions and understanding of experiences in relation to HPV vaccination. We organised the sur- 94
45 HPV infection and the principles of vaccination. This presents a vey data in a summary table and, in keeping with the principle of 95
46 challenge to those who provide information to explain these com- data saturation [13], we compared the survey results with the qual- 96
47 plex issues with sufficient clarity [3]. In this systematic review itative results and looked for evidence that supported, contrasted 97
48 of the international literature, we aimed to synthesise qualitative with or added new themes, which was then integrated into the 98
49 and quantitative evidence of people’s information needs, views and mixed methods synthesis. 99
were from the USA, UK and Australia. Two were from Malaysia, two 108
59 The review was conducted using methodology reported in the
from India and one from Hong Kong. Forty-four surveys [42–85] 109
60 NHS Centre for Reviews and Dissemination (CRD) report 4, [5] sup-
were included; Again the majority were from North America (23), 110
61 plemented by Harden’s recommendations for systematic reviews
twelve from Western Europe and one from Australia. The remain- 111
62 of qualitative studies [6]. We also adhered to guidance on meth-
der (9) were from Malaysia, Hong Kong, Brazil, Vietnam, South 112
63 ods for conducting and reporting systematic reviews in the PRISMA
Korea, Thailand, Taiwan and El Salvador. Study characteristics are 113
64 statement, where it could be applied to mixed method reviews [7].
described in Tables 2 and 3. 114
65 We searched 12 electronic databases including MEDLINE,
66 EMBASE, CINAHL and PsycINFO using thesaurus terms and key-
67Q4 words relating to HPV and vaccination or testing (Appendix 1). 3.2. Study quality 115
70 ducted in June 2009, updated in August 2011; and limited to 1980 to be of good to moderately good standard (Table 4). Approxi- 117
71 onwards when relevant papers began to appear. Two (out of four) mately a third of the surveys were well conducted and five of these 118
72 reviewers (MH, RL, DP and RA) independently screened titles and had a sample size greater than 600 respondents and a response 119
73 abstracts for relevance, assessed the relevant papers against the rate greater than 70%; the remaining studies varied in quality from 120
74 inclusion criteria, and considered study quality. Differences were moderately good to poor (Table 5). 121
79 Pettigrew and Roberts [9]. Details of the qualitative studies were tive data. Text in italics is quoted verbatim from the qualitative 124
80 extracted into pre-defined forms. The authors’ findings were studies in order to illustrate the themes and subthemes. Girls 125
Please cite this article in press as: Hendry M, et al. “HPV? Never heard of it!”: A systematic review of girls’ and parents’ information needs, views
and preferences about human papillomavirus vaccination. Vaccine (2013), http://dx.doi.org/10.1016/j.vaccine.2013.08.091
ARTICLE IN PRESS
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JVAC 14625 1–16
Table 1
Inclusion and exclusion criteria for studies of HPV vaccination.
Inclusion Exclusion
Population Any participants who could be involved in HPV vaccination including Studies where the study population is not appropriate to the
parents of children aged 9–15, young women up to the age of 26 (i.e. intervention, e.g. adults over the age of 26, unless questions relate to
those for whom the vaccine is licenced), healthcare professionals third parties who would be eligible for the intervention
Intervention HPV vaccination in clinical trials or in clinical practice Hypothetical vaccination for STIs
Outcomes People’s views of HPV vaccination, such as their understanding, Studies that assess participants’ knowledge and/or behaviour, not their
attitude, perception, acceptability, concerns and information needs views
Studies that look at participant characteristics that influence the
uptake of HPV vaccination, e.g. smoking, social class, not their views
Study design Any study design used to elicit qualitative or quantitative data relating
to participants’ views on HPV vaccination
Reporting Studies must be reported in sufficient detail for meaningful Studies with insufficient detail, e.g. available only as abstracts
data-extraction
Studies included
(n = 89*)
(104 arcles)
Qualitave Surveys
studies (n = 44*)
(n = 28*) (52 arcles)
(33 arcles)
Fig. 1. PRISMA flowchart. *Some studies were reported in more than one publication.
Please cite this article in press as: Hendry M, et al. “HPV? Never heard of it!”: A systematic review of girls’ and parents’ information needs, views
and preferences about human papillomavirus vaccination. Vaccine (2013), http://dx.doi.org/10.1016/j.vaccine.2013.08.091
4
Table 2
Summary of qualitative studies investigating views and attitudes towards HPV vaccination.
Study, location Data collection method and date Participant details Analysis Type of data collected or relevant questions asked
Al Naggar, 2010 Face to face interviews January 30 unvaccinated female students aged 19–26 years recruited Thematic analysis Current level of HPV knowledge, mode of transmission,
Shah Alam, Malaysia 2010 from a variety of university faculties. 20% were married. 60% causes of cervical cancer, reasons for/against
were from urban areas. 50% Malay, 23% Indian, 20% Chinese vaccination
Bair, 2008 Face to face interviews 40 Latina mothers aged 24–40 with unvaccinated daughters Thematic content General knowledge of HPV and HPV vaccine, factors
Indiana, USA November 2004–March 2005 aged 7–14 years recruited in an urban paediatric care clinic. analysis influencing acceptance/refusal of HPV vaccine
95% reported religion was very important to them. 60% <high
school education
Bernard, 2011 Focus groups and face to face 130 vaccinated girls aged 12–16; 38 parents; 10 teachers; 7 Constant comparative Attitudes towards HPV vaccine, the decision making
Sydney, Australia interviews vaccination nurses purposively sampled from Catholic, method process, knowledge and understanding, experience of
Date not reported independent and state schools vaccination, discussion with family and friends,
questions and concerns
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Cooper Robbins, 2010 Focus groups and interviews 130 vaccinated and vaccine declined adolescent girls in year Thematic analysis Necessity of vaccination, vaccine and Pap smear
NSW, Australia Date not reported 7 or 9/10 purposively sampled from 9 Catholic, state and connection, myths and rumours, need for more
independent schools, and 38 parents information
Dempsey, 2009 Telephone survey 52 mothers of vaccinated and vaccine declined daughters Thematic analysis Acceptance of HPV vaccine, factors influencing
Michigan, USA January–April 2007 aged 11–17, recruited in University family medicine or decision, perceived risk of HPV, vaccine safety
paediatric clinics. 37% declined vaccination. 90% had college
education or higher
Table 2 (Continued)
Study, location Data collection method and date Participant details Analysis Type of data collected or relevant questions asked
Marlow, 2009 Face to face interviews 20 Black and Asian mothers, born in the UK were recruited Framework analysis Attitudes to HPV vaccination, concerns about
UK April–August 2008 (method not reported). 8 Christian, 6 Muslim, 4 Hindu. 75% vaccination, barriers to acceptance of vaccine, social
were home-owners, 95% car-owners. 50% were influences on opinion of vaccine
degree-educated, 85% were employed
Mays, 2004 Face to face interviews 34 parents of children aged 8–17 recruited from 2 paediatric Thematic analysis Attitudes towards HPV vaccine, decision making
Indiana, USA January–June 2000 primary care sites (1 urban, low income; 1 rural, narrative, likelihood of immunising their children,
middle-class). 85% were mothers. 71% white, 29% African rationale for decision
American. 50% college educated
McClelland, 2006 Face to face interviews 14 unvaccinated men and women aged 18–23, recruited by Thematic analysis Knowledge of, and attitudes towards HPV vaccine, the
Melbourne, Australia Date not reported snowballing. 50% female. 43% Catholic, 14% Anglican; 43% link between HPV and cervical cancer, knowledge of
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had no religion. 43% were in relationships. 50% had tertiary clinical trials of HPV vaccine, factors influencing
education vaccine acceptance
Noakes, 2006 Focus groups 27 (±2) parents of boys and girls aged 8–10 were recruited Not reported Knowledge of HPV, attitudes towards sexually
London and Nottingham, UK August–September 2005 (method not reported), excluding outright rejecters of the transmitted nature of HPV, timing of vaccination,
immunisation programme. Exact numbers and demographic barriers to acceptance of HPV vaccine
data not reported
5
6
Table 3
Summary of quantitative studies investigating views and attitudes towards HPV vaccination.
Study, Country Setting Data collection method, date Participant details Summary of relevant questions Brief Summary of Key Results
and response rate
Allen, 2009 Private university On-line questionnaire 2007 1897 female students Age not Perceived benefits of and barriers 93% had heard of HPV and 87% of HPV
New England, USA 40% RR reported 78% white 47% to HPV vaccination; peers receipt vaccination. 65% had had or were planning to
sexually active of vaccine (social norms); have the vaccine; 15% were undecided. There
perception of significant others’ was a strong correlation between social and
approval (subjective norms) subjective norms and later stages of adoption
Askelson, 2010a Rural mid-west state Postal questionnaire Date not 217 mothers of 9–15 year-old Attitudes, subjective norms, and 48% intended to vaccinate their daughters;
Iowa, USA reported 25% RR daughters; 63% college perceived behavioural control; mothers indicated a high perceived
graduates; most had income mothers’ perception of risk to their behavioural control. Most perceived their
≥$50,000 and health insurance
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daughters, vaccine promotion of daughters had a low risk of infection; almost
sexual activity all strongly agreed that the vaccine would have
no impact on their daughter’s sexual activity
Askelson, 2010b Rural mid-west state Postal questionnaire 207 primary care physicians. Intention to vaccinate against HPV, 87% intended to vaccinate female patients and
Iowa, USA March–April 2007 25% RR 79% participated in the Vaccine correct age for delivery of vaccine, mean age preferred was 11 years
for Children programme attitudes (social norms; perceived (recommended) but the range was 6–21 years.
behavioural control), barriers to Intention to vaccinate was driven by subjective
Table 3 (Continued)
Study, Country Setting Data collection method, date Participant details Summary of relevant questions Brief Summary of Key Results
and response rate
Chow, 2010 10 randomly selected In-home, interview. Date not 1617 women with daughters Knowledge about of cervical 98% of women had heard of cervical cancer but
Korea, Taiwan, districts within 4 Asian reported. RR not reported. aged 10–26 who had access to cancer, HPV, vaccination, and <10% had knowledge of HPV and 65% were not
Thailand and Malaysia capital cities. In-office, interview. Date not HPV vaccination and could perceived risk. Factors associated aware of HPV vaccination. 88% thought
reported. RR not reported. afford it. 480 physicians who with vaccine acceptance. daughters’ at low risk of cervical cancer. 83% of
had prescribed or administered Knowledge about of cervical women would be most influenced to vaccinate
HPV vaccine within the last cancer, HPV, vaccination, and by doctors’ recommendations. 48% of
month perceived risk. Factors associated physicians were not confident in discussing
with vaccine recommendation HPV related issues and wanted more
information or training. Only 56% had initiated
conversations with patients about HPV
vaccination and only 2/3 of these were
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comfortable in doing so
Dahlstrom, 2009 The Swedish Population Postal invitation to online 13,946 parents, 11,187 of girls Perception and concerns about HP 76% would accept vaccination; 63% even if not
Nationwide Sweden Register questionnaire and 2759 of boys aged 12–15 V vaccination and correlations of free. 70% preferred vaccination at ≥15 years.
January–May 2007 70% RR years. 87% Swedish, 87% acceptance and willingness to pay 54% of girls’ parents wanted vaccination for
employed for it. Preferred age of vaccination boys. Prior awareness of HPV increased
and vaccination need for boys acceptance; safety concerns decreased it. Well
educated/unemployed less willing to pay
7
8
Table 3 (Continued)
Study, Country Setting Data collection method, date Participant details Summary of relevant questions Brief Summary of Key Results
and response rate
Duval, 2009 Provincial nursing Postal questionnaire 946 nurses. 68% involved in Knowledge about HPV and 85% would recommend HPV vaccines; 93% if
Provinces: NS, QC, ON, associations 2007 53% RR vaccine administration. 58% in vaccination. Intention to free. 91% thought vaccination should be before
BC Canada practice for ≥ 20 years recommend HPV vaccination, sexual debut but 82% also thought all sexually
appropriate age and acceptability active women should be vaccinated.46%
to parents. Impact on screening expected the frequency of screening to be
frequency reduced for vaccinated women
Fang, 2010 Subset of Health Postal questionnaire 1383 individuals who had a Acceptability of HPV vaccination 58% would have a daughter aged 11–12 years
Nationwide USA Information National 2007 RR unclear (<40%) female child aged less than 18 for a daughter aged 11–12 years old vaccinated. Reasons for saying no were lack
Trends Survey years in their household of knowledge (48%), safety concerns (20%);
child not sexually active (9%) or too young
(3%); doctor hasn’t recommended it (6%); more
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research needed (3%)
Feemster, 2008 Paediatric network On-line questionnaire 105 paediatric clinicians 76% HPV knowledge, endorsement of 78% would recommend HPV vaccine to 11–12
Philadelphia, USA affiliated to a metropolitan December 2006–February female 86% white HPV vaccines, attitudes about HPV year old girls Vaccine safety and efficacy
children’s hospital 2007 59% RR vaccination and intention to concerns were barriers to recommendation;
recommend for 11–12 year old parental concerns or concerns about sexuality
girls were not
Study, Country Setting Data collection method, date Participant details Summary of relevant questions Brief Summary of Key Results
and response rate
Jensen, 2009 University database of Postal questionnaire. 204 healthcare professionals: Intentions to recommend HPV 95% were willing to recommend HPV
Wisconsin USA physicians in Dane County. September 2006 39%RR 91% physicians, 9% nurse vaccination to male and female vaccination, 67% to female patients only. 58%
practitioners. 45% urban, 38% patients were very comfortable vaccinating 10–14
suburban, 12% rural year-olds, 76% 15–18 year-olds and 75% >18
year-olds
Kahn, 2009 Primary care membership Email invitation and online 1122 primary care physicians. HPV knowledge, barriers to HPV 44% wanted more information about HPV. 49%
Texas, USA of the American Medical questionnaire 64.% white, 55% male vaccines, reasons for and against always recommended HPV vaccination to girls;
Association September–November 2008 mandated HPV vaccination, 68% were likely to recommend it to boys; 42%
14.4% RR intention to recommend the HPV agreed with mandated vaccination. Barriers
vaccine to boys were parental refusal or inadequate insurance
coverage
Kang, 2010 16 colleges located across Paper q’naire self-completed in 1359 female Korean college Intentions to be vaccinated, 64% wanted to know more about the vaccine
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Nationwide South Korea class students aged 18–32 years. concerns about vaccine, but 78% thought it was too expensive.
Korea April–June 2008 87% RR 26% Christian, 13% Catholic. vaccination and unsafe sexual Intention to be vaccinated was higher when
1.3% HPV vaccinated behaviour recommended by a physician
Lenselink, 2008 17 urban primary schools Postal invitation and telephone 356 parents with children aged Knowledge of the risk factors for 30% of parents had heard of HPV, 14% of
Nijmegan Netherlands interview 10–12 years. 91% mothers, 51% cervical cancer, the transmission of parents understood its relationship with
Date not reported 31% RR. had higher education HPV, its relationship with cervical cervical cancer. 6% had heard of HPV
cancer and the acceptance of HPV vaccination 88% would accept vaccination of
9
10
Study, Country Setting Data collection method, date Participant details Summary of relevant questions Brief Summary of Key Results
and response rate
Podolsky, 2009 Waiting rooms in 2 Self- or 148 Latina mothers in New Knowledge about HPV and 88% New York and 30% Salvadoran women had
El Salvador and USA hospitals in disadvantaged researcher-administered in York, 160 in San Vicente, of acceptability of HPV vaccination, heard of HPV. 68% NY and 88% Salvadoran
communities clinic children aged 8–18. 53% which was available in New York, women would accept vaccination for their
Date not reported 95% RR ≤elementary education but not in El Salvador daughter; 59% and 88% for sons. The most
common reason given for refusing the vaccine
was lack of knowledge (41%)
Riedesel, 2005 Membership of the Postal questionnaire 145 physicians (58% in HPV knowledge, attitudes to HPV Important factors were thought to be long
Nationwide USA American Academy of Date not reported 16% RR urban/suburban practice) vaccination and intention to lasting immunity (96%), few side effects (95%)
Family Physicians Mean age 44 59% male administer vaccine recommendation by professional bodies (98%)
and cost (90%). Barriers were parental
concerns about vaccine safety (73%), risky
behaviour (49%) and vaccination against STIs
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Rosenthal, 2008 A university-based primary Self complete survey, method 153 female carers of 11–17 Perceptions of HPV related disease 44% had been offered vaccination, 60% of
Texas, USA care clinic not reported year-old girls. Aged 27–77 39% severity, susceptibility and barriers whom had accepted. 57% agreed HPV
April 2007–January 2008 83% African-American, 34% White, to vaccination, whether vaccination would be safe, 75% that it could
RR 78% > high school vaccination had been offered and, protect against cervical cancer and genital
if so, reasons for acceptance/refusal warts. 11% against vaccination per se, 9%
thought cost too high, 18% thought daughter
126 described as “unvaccinated” had not been offered vaccination (yet); A few parents believed that the HPV vaccine should be offered to 185
127 girls who had been offered the vaccination and refused it are adolescents when they can take part in the decision whether to be 186
128 described as “vaccine declined”. immunised. (parents of unvaccinated children, USA) [33] 187
Many participants voiced specific concerns that HPV vaccines given 188
129 3.3.1. Trying to decide on HPV vaccination – unanswered to 11 year olds would not prevent infection late in adolescence. 189
130 questions and concerns (healthcare professionals, USA) [22] 190
131 3.3.1.1. Knowledge was poor and there were misconceptions.
132 Although acceptability and uptake of the vaccine, where offered, 3.3.1.4. Participants questioned the rationale for not vaccinating 191
133 were high, people’s level of knowledge was poor. A common boys. A majority of healthcare professionals supported vaccinat- 192
134 thread that permeated their narratives related to unanswered ing boys [69] [69,76,80,81] and parents also thought it important 193
135 questions, concerns and misconceptions [14–16,20,25,26,38]. Par- [24,32,33,41,69]. Some reasoned that this would prevent trans- 194
136 ticipants struggled to make sense of the limited information mission to girls [32,33] and others that it would emphasise boys’ 195
137 available to them and understand how it fitted in with their exist- responsibilities with regard to sex and sexual health [32]. Target- 196
138 ing knowledge of vaccination, cervical cancer, viral infections and ing girls with the vaccine was seen to stigmatise them [24]. Support 197
139 STIs [16,17,20,26]. for male vaccination was evident in four surveys of parents where 198
140 The majority of participants had never heard of HPV. (female stu- a majority of 54–88% were in favour [52,71,75,77]. 199
141 dents, unvaccinated, Malaysia) [14] [About two thirds] of participants reported that they would be 200
142 Typically, participants knew very little about HPV infection and its equally likely to give the HPV vaccine to girls and boys; the pri- 201
143 transmission...Around half the girls were aware that HPV infection mary rationale given was that vaccinating boys should protect girls 202
144 could lead to the development of cervical cancer, but there was also by preventing HPV transmission. (healthcare professionals, USA) 203
145 some confusion about whether cancer could actually be prevented. [23] 204
146 (girls, vaccinated, vaccine declined and undecided) [20] Another topic that emerged was that only girls were being blamed 205
for HPV by targeting the vaccine only towards young girls. (health- 206
147 3.3.1.2. Poor information was a barrier to acceptance. Lack of care providers, community leaders, parents and women eligible 207
148 information was cited in several surveys of parents and young for vaccine) [24] 208
149 women; up to 55% said it was a barrier to vaccine acceptance Most parents thought that the HPV vaccine should be given to boys 209
150 [47,52,60,70,77,79,83,85]. Many participants expressed dissatis- and girls, even though the vaccine has less direct benefit for boys. 210
151 faction with the information available to them and stressed the Most parents felt that immunising boys was important to protect 211
152 importance to both girls and parents that they had sufficient future partners and to reduce disease transmission. (parents of 212
153 clear and understandable information to enable them to make an unvaccinated children, USA) [33] 213
154 informed decision about vaccination [18,19,28,30,38,40,41]. Some
155 girls described how having more knowledge might help them be
3.3.2. The benefits, harms and misconceptions of HPV vaccination 214
156 less confused and more positive about the vaccination experience
3.3.2.1. Cancer prevention was the most important influence in vac- 215
157 [16].
cine acceptability. An obvious benefit of the vaccine was seen to 216
158 Three of the 10 parents who declined the vaccines said they had be cervical cancer prevention [20–22]; some participants knew of, 217
159 insufficient information with which to make an informed decision. or had nursed, people who had died of cancer, sometimes after 218
160 HPV elicited responses of being unfamiliar with the disease and/or a prolonged illness, and were motivated by the desire to protect 219
161 being uniformed about its prevalence or threat to teens. (parents themselves and their loved ones from cancer [28,35]. 220
163 Many girls described how an understanding of why they were and having seen “the trauma they have been through” had decided 222
164 being vaccinated and the benefits of HPV vaccination would help to that the benefits of preventing HPV infection outweighed the risk 223
165 reduce their fear...Nurses agreed the lack of information played a of possible long-term side effects. (NHS school nurses, UK) [35] 224
168 3.3.1.3. Limited understanding about the young age of vaccination number of UK mothers, the erroneous assumption that HPV vac- 227
169 was a barrier to some parents. Parents appeared not to under- cination obviated the necessity for cervical screening appeared to 228
170 stand the reason for targeting HPV vaccination programmes at be a major factor in giving consent for their daughters’ vaccina- 229
171 pre-pubertal girls before sexual debut (i.e. to prevent the most tion [19,39]. This sentiment was supported in one survey of 684 230
172 cases of cervical cancer for a given public expenditure) and ques- mothers also from UK, 70% of whom said they would be glad if HPV 231
173 tioned the need for vaccinating their daughters at such a young vaccination meant an end to cervical screening [73]. 232
174 age [17,29,34,40]. They reasoned that their child was not ready and . . .there were also girls that were certain that Pap smears were now 233
175 would not be sexually active for many years to come, by which unnecessary. . .Parents on the other hand, were more likely to think 234
176 time the effect of the vaccine may have worn off [22,26,41]. Older that girls who had been vaccinated still needed to have Pap smears, 235
177 girls were thought more able to understand the implications of although some were unsure. A few parents stated that they had 236
178 HPV vaccination and therefore to participate in the consent process not heard anything about Pap smear guidelines after vaccination. 237
179 [15,18,33]. (girls, vaccinated and vaccine declined, and parents, Australia) 238
180 There was confusion as to why the vaccination programme has [17] 239
181 been targeted at their age group. The majority of participants did It became clear that some parents had made the decision about 240
182 not understand that this was because the vaccine is most effective whether their daughter would receive the HPV vaccine based on 241
183 when administered before any sexual activity. (girls, vaccinated, misconceptions about the need for cervical screening in the future. 242
184 UK) [34] Several parents had believed that the vaccine would eliminate 243
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and preferences about human papillomavirus vaccination. Vaccine (2013), http://dx.doi.org/10.1016/j.vaccine.2013.08.091
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244 the need for cervical screening. (girls, vaccinated and vaccine surveys [45,47,52,60,61,67,73,74,78–80,84–86,88]; where about 304
245 declined, and parents) [19] three quarters of mothers and young women expressed such wor- 305
246 3.3.2.3. Trusting existing cancer prevention methods was a barrier of the vaccine [20,28,33], although others were suspicious of the 307
247 to acceptance. However, some participants did not see vaccina- medical establishment and pharmaceutical companies [24,37]. 308
257 3.3.2.4. A minority of parents and some physicians had reservations Some ethnic minority participants had concerns relating to the 318
258 about a vaccination for a sexually transmitted infection. Resistance to content of the vaccine and perceived biological differences between 319
259 HPV vaccination was largely related to HPV as a sexually transmit- different racial groups that might provoke or exacerbate side- 320
260 ted infection. The provision of HPV vaccination was seen by some as effects [29,41]. 321
268 sexually active and this could be out of the parents’ control and the black Caribbean mothers was the effect of biological differences 328
269 potentially at a relatively young age [25,32,40]. across ethnic groups and difference in disease risk, with examples 329
given of sickle cell anaemia or increased risk of diabetes. (Black and 330
270 Muslim respondents were more uneasy about this issue. Several...
Asian mothers, UK) [29] 331
271 feared that the vaccine will encourage children to engage in sex-
272 ual activity sooner than they would otherwise. (women and girls,
273 unvaccinated, Malaysia [41] 3.3.2.6. Some girls were afraid of having injections. In both quali- 332
278 Although physician recommendation was acknowledged as adversely affected vaccination uptake. 338
286 However in two surveys of physicians [51,53] the majority were participants’ interpretation, or misinterpretation, of their own or 344
287 confident in discussing HPV vaccination with patients; whilst in their children’s risk of HPV infection Confusion about the best 345
288 two more [78,81], only a minority said parental concern about pro- method of HPV prevention was a barrier to vaccine acceptance 346
289 moting sexual behaviour was a barrier to vaccination uptake. Participants in some studies, interpreting HPV infection in the 347
context of other STIs, did not see the need for vaccination because 348
290 Participants’ decision narratives that indicated vaccine accep-
they erroneously assumed that HPV could be managed by preven- 349
291 tance included discussion with health care providers who explicitly
tive tactics such as condom use [20,21,30,32,40]. Others preferred 350
292 encouraged and recommended HPV vaccination. (female students,
to advocate abstinence or monogamy [20,21,29], but some failed 351
293 some vaccinated, USA) [21]
to recognise that having a number of partners consecutively might 352
294 . . .physician related barriers to recommending HPV vac- present a risk [21]. 353
298 3.3.2.5. Concern about vaccine safety was a barrier to acceptance. Responses reflected the false belief, in many cases, that monogamy 357
299 Participants worried about vaccine safety [21,24,28,29,34,38,40], was protective. . . vaccination was only considered when events 358
300 and voiced fears of the possible consequences of having a new occurred, such as breaking up, which then prompted consideration 359
301 vaccine [24,29,40], particularly relating to adverse effects on fer- of the vaccine. Women acknowledged the potential for HPV vul- 360
302 tility [24,28], and the lack of research into its long term effects nerability because of having multiple partners, or after breaking up 361
303 [24,38]. Concerns about vaccine safety were also evident in with their partner. Participants never acknowledged the possibility 362
Please cite this article in press as: Hendry M, et al. “HPV? Never heard of it!”: A systematic review of girls’ and parents’ information needs, views
and preferences about human papillomavirus vaccination. Vaccine (2013), http://dx.doi.org/10.1016/j.vaccine.2013.08.091
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363 of serial monogamy as a transmission mode. (female students, Monogamous relationships were perceived to be safe regardless of 423
364 some vaccinated) [21] women’s or their partners’ previous sexual history. Some moth- 424
ers could not imagine their daughters becoming sexually active for 425
365 3.3.3.1. Misperception of risk of acquiring an HPV infection could be many years and therefore saw no urgency for vaccination. 426
390 Mothers declining the vaccine perceived their daughters to be at low education about HPV. It is also important as the findings can inform 447
391 risk for HPV-primarily because they did not believe their daughter the broadening of HPV vaccination programmes, as other cancers 448
392 was likely to be sexually active currently or in the near future. These are attributed to HPV viruses, for example, oropharangeal and anal 449
393 mothers lacked a sense of urgency about the need for vaccination cancers. 450
394 before the onset of sexual activity. (mothers of vaccinated and Our review was comprehensive; however it was limited by the 451
395 vaccine declined daughters) [18] scope of the primary studies. Only seven out of 28 qualitative stud- 452
was scarcely a mention of genital warts and none at all of other 459
401 4. Discussion cancers (e.g. ano-genital, head and neck) that could be prevented 460
402 4.1. Summary of main findings in views between ethnic groups; the Marlow review [93] focussed 462
403 Overall the acceptability of HPV vaccination was high. How- research in this area, though there was some evidence that religion 464
404 ever, people had insufficient knowledge and understanding about was an important factor in acceptability but socioeconomic status 465
405 HPV vaccination and a poor grasp of the facts was revealed, with was not. 466
406 participants struggling to interpret limited information in the con- Study populations were heterogeneous in terms of geog- 467
407 text of existing knowledge, impacting on the ability to make raphy, culture, health system and time (i.e. before or after 468
408 informed choices. This lack of understanding permeated all our vaccination programmes). However, since most of the studies 469
409 findings. were set in high-income countries, the review is well placed 470
410 Participants tried to weigh the benefits of HPV vaccination to inform UK vaccination campaign materials. The majority of 471
411 against the possible harms; as well as the clear benefit of cer- studies were conducted in the context of an expectation of 472
412 vical cancer prevention, some participants erroneously perceived vaccination being offered as part of a national programme. In 473
413 a benefit that vaccination would avoid the need for cervical this context, there was no discernible difference in responses 474
414 screening. Others saw no “added value” of vaccination in addi- between those who were making an actual versus a future vaccine 475
415 tion to what they perceived as a tried and tested screening choice. 476
416 programme. Potential harms were perceived to be the encourage- We did not report in detail the impact of vaccine cost, although 477
417 ment of early or promiscuous sexual activity and adverse vaccine it was mentioned by participants in many studies, because it did 478
418 effects, with some girls expressing fear of the vaccination process not impact on people’s views about the vaccine itself or its accept- 479
419 itself. ability. However we acknowledge cost as a major barrier to vaccine 480
420 The risk of HPV infection was interpreted in the context of uptake for some. Socio-economically marginalised women suffer a 481
421 other STIs and it was assumed that only the sexually promiscu- disproportionately large burden of cervical cancer; for HPV vacci- 482
422 ous were at high risk, and that condoms would be fully protective. nation to provide a public health solution in developing economies 483
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and preferences about human papillomavirus vaccination. Vaccine (2013), http://dx.doi.org/10.1016/j.vaccine.2013.08.091
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484 cheaper vaccines as well as improved health education and screen- 5. Conclusions 547
and their parents are poorly informed, have limited understanding 549
486 4.4. Implications for research, and UK policy and practice and many unanswered questions, which impinges on their ability 550
to make informed choices about HPV vaccination and could impact 551
487 Our most striking finding was the lack of knowledge and under- on future uptake of cervical screening. 552
488 standing among the public though, given the complexity of HPV
489 related issues, this is not wholly surprising. More worrying perhaps Acknowledgements 553
490 is that UK general practitioners and practice nurses are concerned
491 about the adequacy of information given in schools and their own We acknowledge the contributions of Sue Wilson, Theresa 554
492 ability to explain and manage conflicts between parents and chil- Marteau, Kirsten McCaffery and the late Joan Austoker to study 555
493 dren [100]. Sound information that can be readily understood by design, and thank Sally Warmington, Annie Hendry, Ellen Richards, 556
494 parents and girls, and straightforwardly delivered in school and pri- Barbara France and the staff of John Spalding Library, Wrexham 557
495 mary care settings is needed. Consideration also needs to be given Medical Institute for their help. 558
496 to the information needs of ethnic minorities to ensure information This review is part of the multi-method HPV Core Messages 559
497 that is relevant to those groups. project, funded by Cancer Research UK (Ref. C1273/A9479) to 560
498 In England the first tranche of vaccinated young women will inform the development of evidence-based informational material 561
499 be eligible to enter the cervical screening programme in 2016. for use in the context of HPV vaccination and testing programmes. 562
500 In light of the evident uncertainty about the need for vaccinated
501 women to participate in cervical screening, this should empha-
Appendix A. Supplementary data 563
502 sised in the information relating to both vaccination and screening
503 programmes, and the screening behaviour of vaccinated women
Supplementary data associated with this article can be 564
504 should be monitored.
found, in the online version, at http://dx.doi.org/10.1016/ 565
505 Furthermore, given the increased incidence of HPV-related
j.vaccine.2013.08.091. 566
506 cancers, public concern regarding vaccination of boys is an addi-
507 tional relevant factor for increasing pressure to vaccinate both
508 genders in the UK. Newman et al. [98] conducted a systematic References 567
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and preferences about human papillomavirus vaccination. Vaccine (2013), http://dx.doi.org/10.1016/j.vaccine.2013.08.091