Does HPV vaccination affect women's attitudes to cervical cancer screening and safe sexual behaviour?

doi:10.1016/j.vaccine.2012.02.081

Vaccine

Volume 30, Issue 21, 2 May 2012, Pages 3196-3201

https://doi.org/10.1016/j.vaccine.2012.02.081 Get rights and content

Abstract

The Human Papillomavirus (HPV) vaccine has the potential to greatly reduce the incidence of cervical cancer by protecting against HPV infections responsible for 70% of cervical cancer diagnoses. However, preliminary research has indicated that women vaccinated against HPV may be less likely to undergo cervical cancer screening and engage in safe sexual behaviour. The aim of the current study was to investigate whether vaccinated and unvaccinated women differ in their (i) knowledge of cervical screening guidelines, (ii) perceived vulnerability to cervical cancer, (iii) cervical screening intentions and uptake, and (iv) attitudes to and engagement in safe sexual behaviour. Participants were 193 female university students (119 vaccine recipients and 74 vaccine non-recipients) who completed online self-report questionnaires. Of all the assessed outcomes, attitudes to safe sexual behaviour were the only significant findings related to vaccination status (p < .001), such that vaccinated women held more positive attitudes to practicing safe sexual behaviour. Less than 5% of participants correctly identified screening guidelines. These findings do not support previous research concluding vaccination could have a detrimental impact on screening and sexual behaviour. Importantly, results highlight poor awareness of screening guidelines, poor levels of consistent condom use (50%) amongst those sexually active, and low uptake of screening (42%) amongst those eligible to be screened. Further research needs to specifically address young women's gaps in knowledge by developing initiatives promoting cervical screening.

Highlights

► We assessed the attitudes of HPV vaccine recipients and non-recipients. ► Vaccinated women held more positive attitudes to practicing safe sexual behaviour. ► Knowledge of cervical screening guidelines was extremely poor.

Introduction

The Human Papillomavirus (HPV) vaccine inoculates against the strains of HPV that cause 70% of cases of cervical cancer. HPV vaccination followed by regular cervical cancer screening is estimated to reduce lifetime risk of cervical cancer by 94% [1], highlighting that it is the combination of vaccination and screening that provides the best protection against this disease. In 2007, Australia was the first country to introduce a quadrivalent prophylactic HPV vaccine, Gardasil^®, providing a unique opportunity to monitor the impact of vaccination on cervical screening rates. It is recommended that Australian women are screened every two years, starting when they turn 18, or two years after they first have sexual intercourse, whichever comes later. Although this guideline does not differ for women vaccinated with Gardasil^®, between 1996 and 2008 rates of screening in Australia steadily declined, with the most prominent decrease evident amongst women aged 20–25 years old [2]. This age group has the lowest uptake (45%) of cervical screening in Australia [3] despite having the highest detection rates of cervical abnormalities [4]. It is therefore important to determine reasons for the decline in screening, and ensure it is not related to HPV vaccination.

There is a paucity of research regarding the impact of HPV vaccination on the uptake of screening, as the literature has predominantly focussed on factors influencing uptake of the vaccine [5], [6], [7]. The existing Australian research indicates that for a small but important proportion of women, cervical screening is of low priority after vaccination. In a recent qualitative study, the majority of girls aged 12–16 interviewed believed they were fully protected against cervical cancer after receiving the vaccine [8]. Another quantitative study utilising a sample of 159 unvaccinated female university students aged between 18 and 27 found that 19% viewed screening as being of low importance following vaccination [6]. The main limitation of research to date is the lack of direct comparison between vaccinated and unvaccinated women, to determine whether potential complacency towards screening is related to vaccination status.

It is currently unclear whether vaccinated young women are aware of screening guidelines and the continued need to screen. Qualitative studies using focus groups identified that young girls had poor knowledge of specific guidelines for screening commencement and frequency following HPV vaccination [8], [9], [10]. However, these studies assessed girls who would not require screening for several years.

International research has offered more insight into the impact of vaccination on health protective behaviour. In line with Australian findings of Cooper Robbins et al., two UK qualitative studies also identified low awareness that cervical screening is necessary following vaccination, as many girls believed the vaccination offered full protection against cervical cancer [9], [10]. To date, only one quantitative study compared rates of screening of vaccinated and unvaccinated women. This study assessed post-vaccination behaviour in a population based telephone survey of 760 German women aged between 14 and 65 [11]. Contrary to the aforementioned findings, Kuitto and colleagues found that vaccination uptake was positively correlated with participation in cervical screening, suggesting that women choosing to receive the vaccine had a positive attitude to preventative health that may promote uptake of cervical screening. However, 77% of the German participants were aged 27 and older, and therefore were not in the age bracket of interest (20–24 years) of recently vaccinated women via the school based vaccination programme and those for which rates of screening in Australia have been dropping.

More so than complacency to cervical screening, HPV vaccine literature has highlighted parents’ fears that vaccinated girls may engage in more risky sexual behaviour, such as earlier sexual debut, and an increase in unprotected sex and number of partners [12], [13], [14]. However, to date, only one study has directly assessed the potential impact of HPV vaccination on sexual behaviour. This study utilised a sample of unvaccinated adolescents and identified that a small but important proportion of teenage girls (20%) reported that they would be less concerned about protecting their sexual health after HPV vaccination [13].

The current study was designed to address limitations from previous research by utilising a sample of women aged between 18 and 30 in order to:

1.
Investigate whether women who have received the HPV vaccine report
- (a)
  lower perceived vulnerability to cervical cancer
- (b)
  less motivation to undergo regular cervical screening
- (c)
  lower uptake of cervical screening and increased likelihood of engaging in unprotected sexual behaviour, compared to women who have not been vaccinated.
2.
Assess levels of knowledge about cervical screening guidelines among vaccinated and non-vaccinated women.

To our knowledge, this is the first quantitative study to directly compare vaccinated and unvaccinated women's intentions to participate in cervical screening and attitudes to sexual behaviour.

Section snippets

Participants

Participants were female students (18–30 years) enrolled in the Psychology course at the University of Sydney, recruited via an online advertisement. All 1304 female students in the first year Psychology cohort were exposed to the advertisement. The vaccinated group included women who had received at least one dose of the HPV vaccine, and the unvaccinated group involved women who had not received any dose. Of 212 students initially recruited (16% of the eligible cohort), 19 did not complete the

Results

Table 1 provides an overview of the sample demographic characteristics. The mean age of participants was 19 (range 18–30). Over half of the sample (54%) identified as Australian, with the next most common ethnicity being North-East Asian (15%). More than a third of participants (40%) were Christian, and the same proportion reported being non-religious. Just over half of participants (55%) reported being sexually active, although only 32% had been sexually active for two years or more (i.e.

Discussion

Although the HPV vaccine has the potential to reduce the prevalence of cervical cancer, it is important to ensure that vaccination does not have detrimental effects on cervical screening and other health behaviours. In this educated sample, vaccinated women did not differ significantly from unvaccinated women on levels of perceived vulnerability to cervical cancer, intention to undergo cervical screening, uptake of cervical screening or likelihood of engaging in safe sexual behaviour.

References (27)

S.C. Cooper Robbins et al.
Is cancer contagious?: Australian adolescent girls and their parents: making the most of limited information about HPV and HPV vaccination
Vaccine
(2010)
S. Hilton et al.
I thought cancer was one of those random things I didn’t know cancer could be caught: adolescent girls’ understandings and experiences of the HPV programme in the UK
Vaccine
(2011)
D.H. Bernat et al.
Parental support for the human papillomavirus vaccine
Journal of Adolescent Health
(2009)
L.A. Marlow et al.
Mothers’ and adolescents’ beliefs about risk compensation following HPV vaccination
Journal of Adolescent Health
(2009)
N.C. Liddon et al.
Human papillomavirus vaccine and sexual behavior among adolescent and young women
American Journal of Preventive Medicine
(2012)
M. Siahpush et al.
Sociodemographic predictors of pap test receipt, currency and knowledge among Australian women
Preventive Medicine
(2002)
R.A. Breslow et al.
Americans’ knowledge of cancer risk and survival
Preventive Medicine
(1997)
S. Goldie et al.
A comprehensive natural history model of HPV infection and cervical cancer to estimate the clinical impact of a prophylactic HPV-16/18 vaccine
International Journal of Cancer
(2003)
Australian Institute of Health and Welfare
Australia's health 2010
(2010)
Australian Institute of Health and Welfare
Cervical screening in Australia 2008–2009
(2011)

Australian Institute of Health and Welfare

Cervical screening in Australia 2006–2007

(2009)

K. Williams et al.

Attitudes towards human papillomavirus vaccination: a qualitative study of vaccinated and unvaccinated girls aged 17–18 years

Journal of Family Planning and Reproductive Health Care

(2011)

I. Juraskova et al.

HPV vaccine promotion: does referring to both cervical cancer and genital warts affect intended and actual vaccination behaviour?

Womens Health Issues

(2010)

Cited by (49)

Young Danish HPV vaccinated women's knowledge, barriers and facilitators towards cervical cancer screening: A qualitative study
2021, Preventive Medicine Reports
Cervical cancer occurs more often in under-screened women, and participation rates in cervical cancer screening among young women are worryingly low worldwide. In Denmark only about half the women in their twenties participate in cervical cancer screening. 64–80% of women between 20 and 29 have been HPV vaccinated with a vaccine protecting against 70% of all cervical cancers. Thus screening is still an important supplement to HPV vaccination for the next decades.
The aim of this study was to investigate knowledge, facilitators and barriers towards cervical cancer screening among young HPV vaccinated women in Denmark. This qualitative study used an anthropological approach, and data was collected using semi structured focus group interviews as this is an effective method for promoting self-disclosure among participants. Eight focus groups were conducted with participation of 49 HPV vaccinated women aged 20–29 years.
We identified five main themes providing an understanding of the women’s barriers and facilitators towards cervical cancer screening: Lack of knowledge about HPV and cervical cancer, the screening invitation, the GP as gatekeeper, the gynaecological examination and perceived relevance of cervical cancer screening. Former vaccination did not impact the women’s reflection about screening attendance. We argue that systematic information and the attitude and tone of the GP are the primary facilitators for filling the knowledge gap we found among young HPV vaccinated women. As an important gatekeeper, the GP can explain, motivate and remind young women about the importance of a regular Pap smear.
Australian women's cervical cancer screening attendance as a function of screening barriers and facilitators
2019, Social Science and Medicine
Citation Excerpt :
Poor knowledge is also nominated as a key psychological barrier (Islam et al., 2017; McFarland et al., 2016). Several studies have shown that women often have poor knowledge about the purpose and efficacy of screening (Neilson and Jones, 1998; Philips et al., 2003) and the cervical screening guidelines (e.g., correct age to start testing) (Mather et al., 2012), but awareness of cervical cancer screening does not necessarily lead to timely screening (Viens et al., 2016). However, few prior studies have examined the screening barriers and facilitators in regards to women's screening status (i.e., up-to-date vs. overdue for screening).
Cervical cancer screening registry data indicate that 43% of eligible Australian women did not screen in the latest reporting period (2014–2015). However, few prior empirical studies have examined whether the screening barriers and facilitators experienced by women can affect their screening attendance. Such information is required to inform the development of future tailored health promotion strategies.
This study examined whether the cervical cancer screening barriers and facilitators identified by women were related to their screening history, from November 2015 and January 2016. At this time, Australian women typically undertook a Pap test every two years. They were deemed overdue for screening if they have not screened in the past 27 months (i.e., overdue by more than three months).
In this study, a large sample (N = 338) of women were asked about their screening history including screening status (i.e., up-to-date vs. overdue) and prior screening (i.e., never screened vs. screened), and the psychological and practical screening barriers or facilitators they had experienced.
Logistic regression analysis indicated that screening status was related to a greater number of psychological barriers, but not practical barriers or facilitators. In contrast, prior screening was related to more practical and psychological screening barriers and fewer practical facilitators, but not psychological facilitators. Some individual psychological screening barriers (e.g., anxiety, embarrassment), practical barriers (e.g., lack of time) and practical facilitators (e.g., low cost of test) were related to women's screening status and prior screening.
Results suggest that addressing practical cervical cancer screening facilitators (e.g., reminder prompts) and psychological screening barriers may help to optimize screening attendance in women who have never screened or are overdue for cervical cancer screening.
HPV Unvaccinated Status and HPV Sexual Risk Behaviour are Common among Canadian Young Adult Women and Men
2018, Journal of Obstetrics and Gynaecology Canada
The current research focuses on sexual risk behaviour among young adult Canadians who have not been vaccinated against HPV.
Six hundred and forty-six Canadian university undergraduates completed a self-administered survey assessing HPV vaccination status and sexual risk behaviour.
Five hundred and thirty-seven participants (154 men and 383 women aged 17–23) who met eligibility criteria were analyzed. 48.5% (n = 185) of female and 89.6% (n = 138) of male participants had not been vaccinated against HPV. In the unvaccinated cohort, 51.4% (n = 95) of women were coitally experienced, 49.2% (n = 91) reported experience with oral sex, and 6.5% (n = 12) reported experience with receptive anal intercourse. 55.1% (n = 76) of men were coitally experienced, 22.5% (n = 31) of men reported receptive oral sex, and 2.9% (n = 4) of men reported receptive anal intercourse. Using validated sexual risk behaviour cut-offs, we determined that in the female unvaccinated population, the proportion at significantly increased risk for genital warts, cervical, anal, and oropharyngeal cancer was 11.0%, 30.0%, 6.5%, and 49.2% respectively. In the male unvaccinated population, the proportion at significantly elevated risk for genital warts and anal cancer was 27.2% and 2.9% respectively.
Unvaccinated young Canadian women and men commonly engaged in sexual risk behaviours for HPV infection, engaged in sexual risk behaviours at a similar level as their vaccinated counterparts, and a substantial number were at elevated risk of HPV related morbidities at a young age. Findings contribute to an evidence-based case for redoubling efforts to encourage HPV vaccination among unvaccinated young Canadians who are at risk of HPV infection.
Étudier les comportements sexuels à risque des jeunes adultes canadiens non vaccinés contre le VPH.
Six cent quarante-six étudiants au baccalauréat ont répondu à un sondage sur leur statut vaccinal contre le VPH et leurs comportements sexuels à risque.
Nous avons analysé les données des 537 répondants (154 hommes et 383 femmes de 17 à 23 ans) qui répondaient à nos critères d'admissibilité. Au total, 48,5 % (n = 185) des femmes et 89,6 % (n = 138) des hommes n'avaient pas été vaccinés contre le VPH. Parmi les femmes non vaccinées, 51,4 % (n = 95) ont dit avoir eu des relations sexuelles coïtales, 49,2 % (n = 91), des relations buccogénitales et 6,5 % (n = 12), des relations sexuelles anales réceptives. Parmi les hommes non vaccinés, 55,1 % (n = 76) ont dit avoir eu des relations sexuelles coïtales, 22,5 % (n = 31), des relations buccogénitales réceptives et 2,9 % (n = 4), des relations sexuelles anales réceptives. Nous avons déterminé, au moyen de seuils de comportements sexuels à risque validés, que les proportions de femmes non vaccinées présentant un risque significativement accru de verrues génitales, de cancer du col utérin, de cancer anal et de cancer oropharyngien étaient respectivement de 11,0 %, de 30,0 %, de 6,5 % et de 49,2 %. Les proportions d'hommes non vaccinés à risque significatif de verrues génitales et de cancer de l'anus étaient respectivement de 27,2 % et de 2,9 %.
Les jeunes adultes canadiens non vaccinés présentaient sensiblement le même niveau de comportements sexuels à risque d'infection par le VPH que les vaccinés, et bon nombre d'entre eux étaient à haut risque d'être atteint d'une affection liée au VPH à un jeune âge. Les résultats de cette étude s'ajoutent aux données probantes appuyant la promotion de la vaccination chez les jeunes canadiens à risque d'infection par le VPH.
Differences in cervical cancer screening knowledge, practices, and beliefs: An examination of survey responses
2017, Preventive Medicine Reports
Citation Excerpt :
For example, one study found that health-protective behaviors such as diet, exercise, and contraception use clustered together and those who engaged in one pro-health behavior were more likely to engage in another (Fortenberry et al., 1997). Women are generally unaware of screening guidelines (Mather et al., 2012) which have changed four times in the last 30 years (American Cancer Society, 2014). The current CDC recommendations for average risk women state that women should be screened with a Papanicolaou (Pap) test every three years from age 21 to 29.
Among the identified barriers to HPV vaccination is the concern that women may compensate for their reduced susceptibility to cervical cancers by reducing cervical cancer screening. This exploratory study examined the relationship between cervical cancer screening rates and HPV vaccination. We conducted a cross-sectional survey using a convenience sample of women aged 21–35 attending a local minority health fair in July 2015. Data were analyzed in 2015–2016. Outcomes assessed were: receiving a Pap test within the last three years, awareness and comfort with current Pap test recommendations, and knowledge regarding the purpose of a Pap test. A total of 291 women were included in the analyses. Mean age was 28.5 years and 62% were non-Hispanic black. 84% had received a Pap test in the last three years and 33% had received at least one HPV vaccine. Logistic regression results showed that women who had been vaccinated did not have lower odds of having a Pap test in the past three years (OR = 1.32; 95% CI = 0.66–2.65). In an adjusted regression model controlling for age and race, vaccinated women were significantly more likely to have had a Pap test (AOR = 3.06; 95% CI = 1.37–6.83). Yet only 26% of women knew the purpose of a Pap test and the proportion who answered correctly was higher among non-Hispanic white women. Women who have been vaccinated for HPV are more likely to have been screened for cervical cancer. These results suggest areas for more robust studies examining pro-health attitudes, behaviors, and communication regarding vaccination and preventive screening.
Human papillomavirus vaccination and subsequent cervical cancer screening in a large integrated healthcare system
2017, American Journal of Obstetrics and Gynecology
Human papillomavirus vaccination may result in lowered intention to be screened for cervical cancer, potentially leading to gaps in screening coverage and avoidable cervical cancer diagnoses.
The purpose of this study was to examine the association between human papillomavirus vaccination and subsequent cervical cancer screening initiation and adherence to recommended screening intervals to detect gaps in screening coverage and inform future prevention efforts.
A retrospective cohort study was conducted in 2 distinct cohorts of female members of Kaiser Permanente Southern California, which is a large integrated healthcare delivery system. Papanicolaou screening initiation was evaluated in women who reached 21 years from 2010–2013. Adherence to recommended screening intervals was evaluated in women who were 25–30 years old in 2010. All women were observed to the end of 2013 for the evaluation of their screening behaviors. History of human papillomavirus vaccination and Papanicolaou screening were obtained from electronic medical records. Adherence to recommended screening intervals was measured as ≥85% vs <85% of the observed “screening up-to-date” person-time. Multivariable Cox and logistic regression models were used to examine associations between vaccination history and screening initiation and interval adherence. Demographic characteristics, gynecologic health history, healthcare use, and characteristics of women’s primary care providers were included as potential confounders in the analyses.
There were 27,352 and 41,328 women included in the screening initiation and screening interval adherence analyses, respectively. In comparison with unvaccinated women, adjusted hazard ratios (95% confidence intervals [CIs]) for screening initiation among women who had been vaccinated against human papillomavirus were 1.19 (95% CI, 1.11–1.28), 1.44 (95% CI, 1.34–1.53), and 1.57 (95% CI, 1.50–1.65) for 1, 2, and ≥3 doses, respectively. Adjusted odds ratios for screening interval adherence were 0.93 (95% CI, 0.83–1.04), 1.73 (95% CI, 1.52–1.97), and 2.29 (95% CI, 2.05–2.56), for 1, 2, and ≥3 doses, respectively.
Women who had been vaccinated against human papillomavirus in this community-based, integrated healthcare setting were more likely to be screened for cervical cancer than were unvaccinated women. Our findings underscore the need for targeted interventions among unvaccinated women who may be disproportionally affected by cervical cancer, despite the presence of population-based screening programs.
Healthcare providers' beliefs and attitudes regarding risk compensation following HPV vaccination
2016, Papillomavirus Research
Provider recommendation is a significant predictor of HPV vaccine uptake. Prior research suggests that concerns regarding risk compensation could cause some providers to hesitate recommending the HPV vaccine.
During 15–30 min semi-structured interviews in early 2015, 22 U.S. pediatric providers were asked about their beliefs regarding sexual risk compensation and cervical cancer screening following HPV vaccination. Providers were asked if these beliefs result in reservations recommending the vaccine. Interviews were audio-recorded, transcribed, and analyzed using inductive content analysis.
None of the providers believed the HPV vaccine would result in risky sexual behavior. Half indicated it was better to start vaccination early, before sexual activity was a worry. Others noted that patients’ risky behavior decisions happen independently of vaccination. When providers were asked if they were concerned about decreased cervical cancer screening, half said they did not know and some stated they had never thought about it before. The main themes addressed were the significant time lapse between vaccination and screening and that women tend to get over-screened as opposed to under-screened.
Providers were generally in favor of HPV vaccination and do not perceive risk compensation as a barrier to HPV recommendation.

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Does HPV vaccination affect women's attitudes to cervical cancer screening and safe sexual behaviour?

Abstract

Highlights

Introduction

Section snippets

Participants

Results

Discussion

Vaccine

Vaccine

Journal of Adolescent Health

Journal of Adolescent Health

American Journal of Preventive Medicine

Preventive Medicine

Preventive Medicine

A comprehensive natural history model of HPV infection and cervical cancer to estimate the clinical impact of a prophylactic HPV-16/18 vaccine

International Journal of Cancer

Australia's health 2010

Cervical screening in Australia 2008–2009

Cervical screening in Australia 2006–2007

Attitudes towards human papillomavirus vaccination: a qualitative study of vaccinated and unvaccinated girls aged 17–18 years

Journal of Family Planning and Reproductive Health Care

HPV vaccine promotion: does referring to both cervical cancer and genital warts affect intended and actual vaccination behaviour?

Womens Health Issues