Primary HPV DNA based cervical cancer screening at 25 years: Views of young Australian women aged 16–28 years

Journal of Clinical Virology 76 (2016) S74–S80

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Primary HPV DNA based cervical cancer screening at 25 years: Views of young Australian women aged 16–28 years Yasmin Jayasinghe a,b,c,∗ , Cheryl Rangiah d , Alexandra Gorelik e , Gina Ogilvie f , John D. Wark g,h , Stefanie Hartley i,k , Suzanne M. Garland a,i,j,k a

Department of Obstetrics & Gynaecology, University of Melbourne, Royal Women’s Hospital, Victoria, Australia Dysplasia Unit, Royal Women’s Hospital, Victoria, Australia c Department of Gynaecology, Royal Children’s Hospital, Victoria, Australia d Western Health, Victoria, Australia e Melbourne EpiCentre, Royal Melbourne Hospital, University of Melbourne, Victoria Australia f Clinical Prevention Services, BC Centre for Disease Control, University of British Columbia, Vancouver, Canada g Bone and Mineral Medicine, Royal Melbourne Hospital, Parkville, Australia h Faculty of Medicine, Dentistry and Health Sciences, University of Melbourne, Victoria, Australia i Women’s Centre for Infectious Disease, Royal Women’s Hospital, Victoria, Australia j Murdoch Childrens Research Institute, Australia k Department of Microbiology, Royal Children’s Hospital, Australia b

a r t i c l e

i n f o

Article history: Received 15 August 2015 Received in revised form 15 October 2015 Accepted 31 October 2015 Keywords: Cervical screening Young women Young Female Health Initiative (YFHI) HPV testing Cervical cancer Theory of planned behavior Renew

a b s t r a c t Background: Revised Australian guidelines have been announced under the Renew® program to commence screening at 25 years of age with HPV testing in 5-yearly intervals, in 2017. We conducted a study of young Victorian women to assess attitudes towards a change in cervical screening practice. Methods: An online survey was conducted of young women aged 16–28 years enrolled in the Young Female Health Initiative (YFHI) study at the Royal Women’s Hospital, Melbourne, to assess attitudes towards delaying the age of cervical screening, widening screening intervals and screening with HPV DNA testing, prior to the announcement of the renewal. Results: Of 149 respondents (response rate 75%), mean age was 23.2 (range 16–27) years. Most (85/131, 65%) were concerned about delaying the age of cervical screening until 25 years. The majority (79% (106/135) were willing to undertake primary screening with HPV testing, whilst 66% (88/133) were willing to undertake HPV testing from 25 years, only 34% (45/132) were willing to undertake such screening every five years. Those willing to change screening practice were more likely to perceive that people important to them would expect them to do so; to have been vaccinated; and to value the importance of national guidelines (p ≤ 0.05). While 69% (95/136) of participants indicated that a positive HPV test would be a source of worry, 76% (103/136) reported they would not feel ashamed about it. Conclusion: Targeted health campaigns are needed to address the concerns of young women prior to the introduction of new cervical screening guidelines in 2017. © 2015 Elsevier B.V. All rights reserved.

1. Introduction For over two decades the organised National Cervical Screening Program (NCSP) in Australia has recommended Papanicolaou (Pap) testing bienially from 18 years, or two years after the onset of sexual activity, whichever occurs later [1]. The three-year screening par-

∗ Corresponding author at: Department of Obstetrics and Gynaecology, University of Melbourne, Royal Women’s Hospital, Corner of Grattan and Flemington Rd., Parkville, 3052 Victoria, Australia. Fax: +61 3 8345 3702. E-mail address: [email protected] (Y. Jayasinghe). http://dx.doi.org/10.1016/j.jcv.2015.10.026 1386-6532/© 2015 Elsevier B.V. All rights reserved.

ticipation rate is 70.3%, resulting in a halving of the incidence and mortality of cervical cancer (to 6.9 and 1.8 per 100 000 women/year in 2011–2012, respectively) since the introduction of the organized NCSP in 1991 [2]. New guidelines were announced under the Renew® program with recommendations to utilize human papillomavirus (HPV) testing from age 25 at 5-yearly screening intervals from 2017 [3]. This stems from a multitude of factors including the high three-dose HPV vaccination coverage in our target population of school-aged females (73% across all socioeconomic groups) [4]; with the resultant decline in high grade abnormalities in vaccinated women [5]. Furthermore it is due to an improved understanding of

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HPV-related disease [6,7] including the infrequent occurrence of invasive cervical cancer in younger women [2]; the desire to avoid investigation and treatments with potential for obstetric harm, for cervical dysplasia which may otherwise naturally regress [6,8]; and the data suggesting minimal impact on cervical cancer incidence in women ≤25 years despite screening [7]. Currently delayed cervical cytology screening is underway in the United Kingdom (to 25 years) and the United States (to 21 years) [9,10]. However newer technology (HPV testing) has demonstrated greater sensitivity for detection of cervical intraepithelial neoplasia 2 or more (CIN 2+) compared to cytology alone [11], and a higher negative predictive value of CIN3+ of over 96% [12]. Thus a longer duration of protection can be expected. The Swedescreen study has demonstrated that 5-yearly HPV testing is as sensitive for CIN2+ as three-yearly cytology [13]. Population studies from the Netherlands (where 5-yearly HPV testing is used in primary screening) demonstrates improved protection against CIN3 and cervical cancer compared to cytology [14]. It is estimated that under-screening contributes to around 60–80% of cervical cancers in countries with screening programmes [15,16]. During this era of change, it is important, that women understand and comply with cervical screening recommendations. However, linkage between the Victorian Cervical Cytology Registry in Australia, and the National HPV Vaccination Program Register for 2009–2011, demonstrates lower three-year screening participation in vaccinated compared to unvaccinated women: 21.7% lower (54.2% versus 75.9% respectively) for 25–29 year olds; and 55.7% lower (21.4% versus 77.1% respectively) in the 30–34 year old age group [17]. It is unclear how Australian women will respond to further policy changes regarding cervical screening. Delaying screening and

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widening screening intervals have resulted in increased cervical screening non-attendance both in screen-eligible women in the United States [18], and in England [19]. The primary objective of the study was to identify whether young Australian women in the state of Victoria who were recruited via Facebook were willing to delay cervical screening until 25 years, undergo HPV testing instead of Pap screening and extend the screening interval to 5-yearly. Predictive factors and barriers for undertaking such changes were also assessed and could inform educational messages as the Renew is implemented. 2. Materials and methods 2.1. Participants Women aged 16–28 years were recruited through the Young Female Health Initiative (YFHI) study at the Royal Women’s Hospital, Melbourne, prior to the announcement to the Australian community of the future cervical screening guideline changes [3]. YFHI evaluates interactions between key health domains in young Victorian women. Women are recruited through the social network site Facebook, a novel method as previously published [12]. Briefly, Facebook users who clicked on a YFHI advertisement, were directed to a secure study website (www.yfhi.org) and invited to express interest. Respondents were telephoned to assess eligibility. Those <18 years underwent a mature minor assessment by the researcher, or invited to obtain parental/guardian consent [20]. Females aged 16–25 years, residing in Victoria and willing to complete online health modules were included in the original YFHI cohort in 2010, with the oldest participants now 28 years of age. Women were excluded if they did not consent or were perceived to have inadequate understanding of the purpose and procedures of the study.

Table 1 Summary of key questionnaire domains.a Screening concept

Scale itemsb

• • • • •

• I would be willing to have an HPV test to screen for cervical cancer instead of a Pap smear • I would be willing to have an HPV test to screen for cervical cancer every [year] or [3 years] or [5 years] or [10 years] instead of a Pap smear every two years • I am concerned about delaying the age of cervical screening until 25 years of age. • Having an HPV test to screen for cervical cancer [from age 25] [and every year/ 3 years/ 5 years/10 years] instead of a Pap smear every 2 years would be: Accurate/ Safe/ Protect my health/ Acceptable • I would be willing to have an HPV test to screen for cervical cancer from age 25 and every five years thereafter, instead of a Pap smear every two years, after becoming sexually active: (responses from 1 strongly disagree to 7 strongly agree)

Attitudes and intention towards HPV testing instead of cytology Attitudes towards HPV testing at widening screening intervals Attitudes towards delaying cervical screening until 25 years Attitudes towards HPV testing from age 25 at widening screening intervals The primary endpoint was defined as a response to the statement:

• Subjective norms: direct

• If national guidelines recommended having an HPV test to screen for cervical cancer instead of a Pap smear, most people who are important to me would think I should/expect me to have an HPV test instead of a Pap smear • I would feel under social pressure to have an HPV test to screen for cervical cancer instead of a Pap smear

• Subjective norms: indirect

• If national guidelines recommended having an HPV test to screen for cervical cancer instead of a Pap smear my parents /general practitioner (GP) /gynaecologist /teachers /religious leader/ friends/ partner/ role models would think I should have an HPV test to screen for cervical cancer instead of a Pap smear • What my parents/ GP/ gynaecologist/ teachers/ religious leader/ friends/ partner/ role models think is important to me

• Perceived behavioural control

• I am confident I could have an HPV test to screen for cervical cancer instead of a Pap smear: Disagree/Agree • For me to have an HPV test instead of a Pap smear would be: Easy/Difficult • Whether or not I would have an HPV test of a Pap smear would be entirely up to me: Disagree/Agree • How much control would you have over whether you had an HPV test to screen for cervical cancer instead of a Pap smear? No Control/Complete Control

a b

Table is not the complete survey. Results were dichotomized ≤4 and >4 from a 7 point likert scale.

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Women were invited into this sub-study if they had consented to further research, and had completed the module on sexual and reproductive health. This module included questions on knowledge of HPV, the HPV vaccine, HPV vaccination status and Pap screening status; results of which have been previously published [21–23]. 2.2. Procedure In February 2014, 199 women who met the inclusion criteria were emailed invitations to complete an online questionnaire via Survey Monkey (www.surveymonkey.com). Two reminders were sent at the beginning and end of March, 2014. Data collection concluded on the 16th of April 2014. Renewal guidelines were announced on April 28th 2014. Women were compensated for their time with $10 gift vouchers. 2.3. Materials The questionnaire for took 20 min to complete, and assessed women’s intentions to undergo HPV testing at extended intervals from age 25 years (Table 1). Questions were adapted from Ogilvie et al. [24], and based on the theory of planned behaviour (TPB), which has been widely validated to assess health-related behaviours [25]. The TPB assesses three predictors of intention

to perform a health behaviour: (i) attitudes towards a behaviour, (its perceived value and utility); (ii) the influence of subjective norms (the individual’s belief of what people important to them, or external factors such as guideline recommendations about that behaviour,); and (iii) perceived behavioural control (the individuals perception of their ability to control the behavior related to self-efficacy or perceived control of environmental constraints on behaviour) [25]. The survey assessed women’s knowledge of current cervical screening practice in Australia. Then, women were provided with background information on cervical screening; including information on HPV, its aetiological role in cervical cancer, the rationale of HPV testing from age 25 and extended screening intervals. Women’s attitudes towards potential new cervical screening guidelines were then assessed (Table 1). The survey items that predicted behavioural intentions were assessed using seven point Likert scales. As we did not specify that ‘4 on the Likert scale was neutral, a cross tabulation was undertaken between the ‘importance of national guidelines’ to the participants and ‘willingness to undertake revised screening at age 25 years, with HPV testing every five years’. Of those that answered ‘4 for the first question, 100% answered that they were unwilling to undertake screening; therefore ‘4 was regarded as ‘unwilling’ to change screening practice. Survey responses were dichotomised,

Table 2 Bivariate comparisons of demographic characteristics between women willing and not willing to undergo cervical screening in accordance with new guidelines. Variable Intention to screen Age

Category 16–20 21–24 25–28

Willing to screen >4, n (%)a

Not willing to screen; ≤4, n (%)a

n = 45((34.1) 6 (13.3) 28 (62.2) 11 (24.4)

n = 87((65.9) 17 (19.6) 50 (57.5) 20 (23.0)

p-value (Fisher’s exact) 0.67

Education


1 (2.2) 18 (40.0) 26 (57.8)

2 (2.3) 31 (35.6) 54 (62.1)

0.89

Country of Birth

Australia Overseas

38 (84.4) 7 (15.6)

80 (92.0) 7 (8.1)

0.18

Locality

Metropolitan Rural

40 (88.9) 5 (11.1)

72 (82.8) 15 (17.2)

0.35

SEIFA decileb

<5 5-8 >8

4 (8.9) 23 (51.1) 18 (40.0)

13 (14.9) 42 (48.3) 32 (36.8)

0.64

HPV Vaccinationc

Unvaccinated Partial Complete Unsure

1 (2.2) 3 (6.7) 35 (77.8) 6 (13.3)

12 (13.8) 6 (6.9) 57 (65.5) 12 (13.8)

0.03

AFSI (years)d

Never sexually active <16 16–20 21–24 Prefer not to answer

8 (17.8) 10 (22.2) 21 (46.7) 5 (11.1) 1 (2.2)

11 (12.6) 15 (17.2) 58 (66.7) 3 (3.5) 0 (0.00)

0.10

Sexual partnerse

0–1 2–5 6–10 >10

11 (24.4) 14 (31.1) 6 (13.3) 14 (31.1)

24 (27.6) 29 (33.3) 14 (16.1) 20 (23.0)

0.79

Pap smear history

Had Pap smear Never had Pap Unsure

23 (52.3) 20 (45.5) 1 (2.3)

55 (64.7) 30 (35.3) 0 (0.00)

0.18

Age of first Papf

18–21 22–25

23 (48.9) 24 (51.1)

19 (61.3) 12 (38.7)

0.28

a Results were dichotomised with women who answered ≤4 on a seven point Likert scale coded as willing to screen and women who answered >4 as not willing to screen with HPV testing from 25 years every five years. b Socioeconomic index for area based on postal/zip code. Deciles are the rankings within Victoria from lowest to highest 1–10. c Self-reported HPV vaccination status, analysis included unvaccinated women compared to those who had at least one dose, those unsure were excluded. d Age of first sexual intercourse (years). e lifetime number of male sexual partners. f Age of first Pap smear (years), n = 78 as 78 indicated they had undertaken a Pap smear.

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Table 3 Attitudes regarding HPV testing according to intention to change cervical screening practice (bivariate analysis). Willing to screen;n (%)a

Attitude

Not willing to screen; n (%)a

p-Value (Fisher’s exact)

HPV testing is: “Accurate” “Safe” “Likely to protect my health” “Acceptable”

n = 45 31(68.9) 38 (84.4) 34 (75.6) 33 (73.3)

n = 87 45 (51.7) 61 (70.1) 55 (63.2) 54 (62.1)

0.07 0.09 0.2 0.2

Self- collected HPV tests are: “Accurate” “Safe” “Likely to protect my health” “Acceptable”willingness to undertake self-collected HPV tests

n = 44 28 (63.6) 37 (84.1) 33 (75.0) 36 (81.8)39 (88.6)

n = 87 36 (41.4) 51 (58.6) 47 (54.0) 49 (56.3)65 (74.7)

0.02 0.003 0.02 0.004

a Results were dichotomised with women who answered ≤4 on a seven point Likert scale coded as willing to screen and women who answered >4 as not willing to screen with HPV testing from 25 years every five years.

with women who responded ≤4 coded as not willing to perform the health-related behaviour and women who responded >4 coded as willing to perform the health-related behaviour. This also allowed comparison between similar studies [24]. Participants’ demographic data were obtained from the YFHI database. HPV vaccination status was self-reported and recoded as unvaccinated (no doses of HPV vaccine received), partial (1–2 doses of HPV vaccine received) or complete (3 doses of HPV vaccination received). Results were analysed using STATA version 13.0 (StataCorp LP, College Station, TX, USA). Categorical variables were compared using Fisher’s exact tests. Odd ratios were calculated to investigate significant predictors (delaying age of onset of screening to 25 years, screening with an HPV test, widening the screening interval). A two sided p value of less that 5% (p ≤ 0.05) was taken as statistically significant.

3. Results Of the 271 participants in the YFHI database 199 were eligible for participation. Of the 159 respondents, 2 declined, 8 were excluded (there were 2 duplicate responses; and 6 logged on but did not complete any questions). The participation rate was 75% (149/199) of whom 24 partially completed the questionnaire beyond demographics and 125 completed the entire questionnaire. Demographic characteristics are provided as supplementary data

(Table S1). Mean age was 23.2 years (standard deviation [SD] = 2.1, range 16–27 years). Of 132 respondents who answered the question, 34.1% were willing to screen with HPV testing from age 25, at 5-yearly intervals. Unvaccinated women were less willing to adopt new screening practices (1/13, 7.7%), than women who had received at least one dose of the HPV vaccine (38/101, 37.6%) (p = 0.03). Otherwise there were no other significant differences in demographic characteristics or sexual health history between the groups (Table 2). On bivariate analysis, women willing to screen according to new recommendations did not have greater awareness of current cervical screening guidelines (40/45, 88.9% versus 65/87, 74.7%, p = 0.07) or of pending changes to guidelines (38/45, 84.4% versus 72/87, 82.8%, p = 1.0). However, they were more likely to value national guideline recommendations (44/45, 97.8% versus 69/87, 79.3%, p = 0.003). In both groups, beliefs of those that were valued highly in this realm were those of their gynecologist (90.2%), GP’s (88.6%), partners (86.5%), parents (72.0%), friends (69.7%), role models (58.3%); with religious leaders and teachers having less influence (≤6.1%). Those willing to change practice were more likely to feel that people important to them would expect them to screen according to new recommendations (34/45, 75.6% versus 48/87, 55.2% in those unwilling, p = 0.02). Social pressure to adhere to guidelines was felt amongst 32% (42/138) of participants, with no difference between those who were willing or unwilling to change screening practice (p = 0.5). Perceived behavioural control did not influence willingness to screen, with participants feeling that get-

Table 4 Effect of delayed age and extended screening intervals on women’s intentions to screen. Screening modality

Screening interval

(%) Willing to screen of total n (%)

Comparisons between screening intervals

Odds ratio (95% confidence interval);

HPV testing alone

N/Aa

106/135 (78.5)

N/Aa

N/Aa

HPV testing at extended screening intervals

Yearly

92/135 (68.2)

3 early vs yearly 5 yearly vs yearly 10 yearly vs yearly

0.7 (0.4–1.2); 0.2 (0.1–0.4); 0.05 (0.03–0.1);

3 Yearly

82/135 (60.7)

5 Yearly

41/134 (30.6)

5 yearly vs 3 yearly 10 yearly vs 3 yearly 10 yearly vs 5 yearly

0.3 (0.2–0.5); 0.08 (0.04–0.1); 0.3 (0.1–0.5);

10 Yearly

14/134 (10.5)

N/Aa

N/Aa

Yearly

88/133 (66.2)

3 yearly vs yearly 5 yearly vs yearly 10 yearly vs yearly

0.8 (0.5–1.4); 0.3 (0.2–0.5); 0.07 (0.03–0.1);

3 Yearly

81/132 (61.4)

5 Yearly

45/132 (34.1)

5 yearly vs 3 yearly 10 yearly vs 3 yearly 10 yearly vs 5 yearly

0.3 (0.2–0.6); 0.08 (0.04–0.16); 0.2 (0.1–0.5);

10 Yearly

15/132 (11.4)

N/Aa

N/Aa

HPV testing from age 25 years at extended screening intervals

a

Not applicable.

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ting an HPV test rather than a Pap smear would be easy (87.1% [115/132], p = 0.9), their choice (81.5% [110/135], p = 0.6); and under their control (83.7% [113/135], p = 0.9). Attitudinal scores relating to HPV testing did not influence willingness to screen with renewed guidelines (p > 0.05) (Table 4). Most women (79.4%, 104/131) expressed interested in obtaining selfcollected samples for HPV testing, with no significant difference between those willing to change screening practice and those not. However, those unwilling, were more likely to have concerns about self-collected testing (Table 3). Most women (78.5%) were willing to utilise HPV testing as a screening tool instead of Pap testing. Around 68% were willing to undertake HPV testing annually, with no significant difference accepting HPV screening from 25 years annually (66%) (p = 0.7) (Table 4). This number decreased significantly when screening intervals were extended, with 34.1% willing to undertake HPV testing from 25 years, at 5 year intervals. Of 131 participants, 64.9% (n = 85) were concerned about delaying the age of cervical screening until 25 years, 68.7 % (n = 90) thought cervical cancer could be missed, and 58.0% (n = 76) thought that changes in screening being implemented were to reduce governmental costs. Women not willing to screen with HPV testing from 25 years at 5-yearly intervals, were significantly more likely to express concern about delayed age of cervical screening compared to those who were willing (74.7%, 65/87 versus 45.5%, 20/44, p = 0.002). Factors predictive of concern included a self-reported past history of Pap abnormality (OR 5.5 [1.2–50.9]; p = 0.02); family history of cervical cancer (OR 4.3 [0.9–40.8]; p = 0.04); family history of any cancer (OR 3.7 [1.5–9.6], p < 0.01); a fear that cancer will be missed (OR 15.5, [5.8–42.4], p < 0.01) and a belief that less frequent screening is being implemented to reduce costs (OR 7.3, [3.0–17.7], p < 0.01). Reasons reported for not being concerned about the delayed aged of screening included having received HPV vaccination (61.1%, n = 80); while 21.4% (n = 28) felt that being in exclusively same-sex relationships was also reassuring. Sixty percent of participants (n = 79) estimated that there was a <1% risk of developing cervical cancer by 25 years in someone who was vaccinated at 11–13 years; however, only 31.3% (n = 41) believed it to be <1% in someone who was unvaccinated. With delayed onset of screening 59.5% of participants (n = 78) indicated that they would still have yearly sexually transmitted infection checkups; and 65.7% (n = 86) felt that they would be self-motivated to begin cervical screening at 25 years. Of 136 participants, 69.9% (n = 95) indicated that being diagnosed with an HPV infection will be a source of worry; however, 75.7% (n = 103) reported not feeling ashamed about it. Most (75.7%, n = 103) felt their partners would be understanding. Participants indicated greatest comfort sharing a positive HPV result with a healthcare professional (91.2%, n = 124), followed by their partner (77.2%, n = 105), a close friend (73.5%, n = 100) and family member (58.8%, n = 80). Participants reported that appropriate sources for receiving information on changes in cervical screening guidelines could be (in decreasing order), the internet (95/136, 69.9%), television (90/136, 66.2%), Facebook (72/136, 52.9%), radio (64/136, 47.1%), popular magazines (43/136, 31.6%) and YouTube (28/136, 20.6%).

4. Discussion With the recent announcement of the Renewal® program, Australia is on the cusp of revised cervical screening resulting in a major change for Australian women [3]. In this study, 78.5% of participants were willing to utilise HPV testing as a primary screening tool, which may be an overestimate compared to the general population. The YFHI cohort is similar to

the target population of young Australian women living in Victoria women with regards to ethnicity, geographic region, Indigenous status, socioeconomic level and HPV vaccination status; however they are more likely to be tertiary educated and slightly older [4,26]. A study of 314 women aged 16–70 attending Australian Family Planning clinics demonstrated increased psychosocial morbidity when allocated to HPV triage versus conventional cytology, however by 12 months this effect had reversed [27]. Stigma around disclosing positive HPV results may affect acceptance of the test [28]. Our study demonstrated that over 75% of participants believed their partners would understand. This is consistent with past studies of this cohort which have demonstrated high knowledge of HPV and endorsement of HPV vaccination [21,22]. However, approximately one third of participants did foresee difficulties in disclosing a positive HPV result to their partners and concerns may be even higher in an older or less well educated population. Our results are similar to a study of 981 Canadian women aged 25–64 years, where 84.2% were accepting of HPV testing as primary screening tool; however this dropped to 54.2% with a screening interval of 4 years [24]. Similarly our study demonstrated that women’s willingness to screen with HPV testing decreased significantly with extended intervals, with only 34.1% accepting of 5-yearly intervals. Traditionally, Australian women have favoured shorter cervical cytology screening intervals (50% preferring annual screening, 40% biennial) for peace of mind [29]. However in a recent survey of Victorian women up to age 69 years on Pap screening demonstrated that around 49% would embrace three-yearly screening if it were the recommendation (24%), if the evidence supported it (13%), and if it were recommended by a health professional (6%) [30]. Self-sampling for HPV is being evaluated in Australia for underscreened women [31]. However those not willing to change screening practice had significantly lower attitudinal scores regarding self-sampling in our study, highlighting the importance of education underscoring its safety. Notably, those not willing to adopt new screening practices are likely a different group to lapsed screeners, as the former appear more concerned with their cervical cancer risk with delayed onset and less frequent screening [30]. Past studies of lapsed screeners from the United Kingdom, and Italy have demonstrated that self-sampling increases participation rates, and appropriate follow-up [32,33]. Similarly it has demonstrated good levels of acceptability by women in the African American community, and Hispanic women in Puerto Rico [34,35]. Willingness to adopt new screening practice was associated with self-reported HPV vaccination. A previous validation study reported in our population noted that concordance with HPV vaccination registry data and self-report was 82% for those that actually received three doses [22]. It is a concern if unvaccinated women become under-screeners. However Australian reports have demonstrated the opposite, with reduced participation in screening in those vaccinated compared to those not vaccinated [17]. This may suggest misperceptions about the degree of protection provided by the vaccine, as demonstrated in a previous study of this cohort, where 96% aware of the vaccine understood further screening was required but only 66% understood the vaccine was partially protective against cervical cancer [22]. Participants perceived that increased vigilance was required for unvaccinated women. Only 30% of participants estimated the risk of cervical cancer by 25 years to be less than 1% in someone who was unvaccinated. The misconception that less frequent screening is mainly offered for financial reasons has been previously demonstrated [24]. This needs to be dispelled by the evidence allowing screening to occur safely at extended intervals [14], translating to protective reproductive health benefits [36]. Women willing to change screening practice were more likely to report the influence of direct and indirect subjective norms on their

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decision to screen, consistent with previous reports [24]. These findings reiterate the importance of education efforts extended to include healthcare practitioners, peers and family who play an integral role in influencing women’s decisions to take up new screening practices. It would be useful to assess the interaction between knowledge of cervical cancer risk from 25 to 30 years and intention to screen at 25 years. Furthermore young women should be made aware that sensitivity of HPV testing for CIN2+ after five years is around 86%, not 100% [13], hence follow-up is important. Furthermore reduced specificity of testing means that partial genotyping, cytology and colposcopic follow-up may be required [3] Gaps in such knowledge may useful for inclusion in targeted education efforts. 5. Conclusion While this was a relatively small study, it is the first Australian study to assess the acceptability to young women of transitioning from Pap testing to primary HPV testing from age 25 at 5-yearly intervals, and on women’s intentions to attend cervical screening. While acceptance of HPV testing was high, widening the interval reduced willingness to adopt the screening changes. Targeted education of both vaccinated and unvaccinated women regarding the evidence-based nature of these changes prior to the introduction of the new cervical screening guidelines is required. Funding None. Competing interests None declared. YJ has received scholarship funding from the Cancer Council Victoria, Royal Australian and New Zealand College of Obstetricians and Gynaecologists, and Royal Australasian Chapter of Sexual Health Medicine (Novartis Scholarship) and grant funding from the Victorian Cancer Agency and Victorian Comprehensive Cancer Network for unrelated projects. SG has received grant support from CSL Bio, Merck and GlaxoSmithKline to conduct HPV vaccine studies (VIVIANNE) trial. SG is a member of the Merck Global Advisory Board as well as the Merck Scientific Advisory Committee for HPV (unpaid position). Ethical approval Ethics approval was obtained from the Human Research and Ethics Committees at the Royal Women’s Hospital in January, 2014 for this sub-study (HREC 11/14). Author contributions Conception and design of the study: YJ, CR, GO, SH, SG, AG, JW. Acquisition of data: CR, SH, YJ. Analysis and interpretation of data: YJ, CR, AG, SH, JW,SG, GO. Drafting the article or revising it critically for important intellectual content: all authors. Final approval of the version to be submitted: all authors.. Acknowledgement We would like to thank the YFHI study participants for their contribution.

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Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.jcv.2015.10.026. References [1] National Health Medical Research Council, Screening to Prevent Cervical Cancer: Guidelines for Management of Asymptomatic Women with Screen Detected Abnormalities, Australian Government, Canberra, 2006. [2] Australian Institute of Health and Welfare, Cervical Screening in Australia 2012–2013, AIHW, Canberra, 2015. [3] Australian Government National Cervical Screening Program.: Department of Health, 2014. Available from: www.cancerscreening.gov.au/internet/ screening/publishing.nsf/Content/overview-of-the-renewal [cited 22.04.15]. [4] B. Barbaro, J.M. Brotherton, Assessing HPV vaccine coverage in Australia by geography and socioeconomic status: are we protecting those most at risk? Aust. N. Z. J. Public Health 38 (5) (2014) 419–423. [5] D.M. Gertig, J.M. Brotherton, A.C. Budd, K. Drennan, G. Chappell, A.M. Saville, Impact of a population-based HPV vaccination program on cervical abnormalities: a data linkage study, BMC Med. 11 (2013) 227. [6] C.B. Woodman, S. Collins, H. Winter, A. Bailey, J. Ellis, P. Prior, et al., Natural history of cervical human papillomavirus infection in young women: a longitudinal cohort study, Lancet 357 (9271) (2001) 1831–1836. [7] P. Sasieni, A. Castanon, J. Cuzick, Effectiveness of cervical screening with age: population based case-control study of prospectively recorded data, BMJ 339 (2009) b2968. [8] M. Kyrgiou, G. Koliopoulos, P. Martin-Hirsch, M. Arbyn, W. Prendiville, E. Paraskevaidis, Obstetric outcomes after conservative treatment for intraepithelial or early invasive cervical lesions: systematic review and meta-analysis, Lancet 367 (9509) (2006) 489–498. [9] National Health Service. NHS Cervical Screening Program. (accessed April 2007). [10] American College of Obstetricians & Gynecologists, ACOG committee opinion number 463: cervical cancer in adolescents: screening, evaluation, and management, Obstet. Gynecol. 116 (2) (2010) 469–472. [11] G.S. Ogilvie, M. Krajden, D.J. van Niekerk, R.E. Martin, T.G. Ehlen, K. Ceballos, et al., Primary cervical cancer screening with HPV testing compared with liquid-based cytology: results of round 1 of a randomised controlled trial—the HPV FOCAL Study, Br. J. Cancer 107 (12) (2012) 1917–1924. [12] S. Cotton, L. Sharp, J. Little, M. Cruickshank, R. Seth, L. Smart, et al., The role of human papillomavirus testing in the management of women with low-grade abnormalities: multicentre randomised controlled trial, BJOG 117 (6) (2010) 645–659. [13] K.M. Elfstrom, V. Smelov, A.L. Johansson, C. Eklund, P. Naucler, L. Arnheim-Dahlstrom, et al., Long term duration of protective effect for HPV negative women: follow-up of primary HPV screening randomised controlled trial, BMJ 348 (2014) g130. [14] D.C. Rijkaart, J. Berkhof, L. Rozendaal, K. van, F.J. emenade, N.W. Bulkmans, D.A. Heideman, et al., Human papillomavirus testing for the detection of high-grade cervical intraepithelial neoplasia and cancer: final results of the POBASCAM randomised controlled trial, Lancet Oncol. 13 (1) (2012) 78–88. [15] Victorian Cervical Cytology Registry Statistical Report, VCCR, Melbourne, 2013. [16] H. Sancho-Garnier, C. Tamalet, P. Halfon, F.X. Leandri, L. Le Retraite, K. Djoufelkit, et al., HPV self-sampling or the Pap-smear: a randomized study among cervical screening nonattenders from lower socioeconomic groups in France, Int. J. Cancer 133 (11) (2013) 2681–2687. [17] A.C. Budd, J.M. Brotherton, D.M. Gertig, T. Chau, K.T. Drennan, M. Saville, Cervical screening rates for women vaccinated against human papillomavirus, Med. J. Aust. 201 (5) (2014) 279–282. [18] Centre for Disease Control and Prevention, Cervical cancer screening among women aged 18–30 years- United States, 2000–2010, Morb. Mortal. Wkly. Rep. (MMWR) 61 (51) (2013) 1038–1042. [19] R. Albrow, H. Kitchener, N. Gupta, M. Desai, Cervical screening in England: the past, present, and future, Cancer Cytopathol. 120 (2) (2012) 87–96. [20] Y. Jayasinghe, Y. Fenner, J.D. Wark, S.N. Tabrizi, E.E. Moore, A. Fletcher, et al. (Eds.) Recruitment of mature minors into sexual health research using the social networking site Facebook. 17th World Congress on Pediatric & Adolescent Gynecology, Hong Kong, 2013. [21] B. Gunasekaran, Y. Jayasinghe, Y. Fenner, E.E. Moore, J.D. Wark, A. Fletcher, et al., Knowledge of human papillomavirus and cervical cancer among young women recruited using a social networking site, Sex. Transm. Infect. 89 (4) (2013) 327–329. [22] B. Gunasekaran, Y. Jayasinghe, J.M. Brotherton, Y. Fenner, E.E. Moore, J.D. Wark, et al., Asking about human papillomavirus vaccination and the usefulness of registry validation: a study of young women recruited using Facebook, Vaccine 33 (6) (2015) 826–831. [23] N. Ahmed, Y. Jayasinghe, J.D. Wark, Y. Fenner, E.E. Moore, S.N. Tabrizi, et al., Attitudes to Chlamydia screening elicited using the social networking site Facebook for subject recruitment, Sex. Health 10 (3) (2013) 224–228. [24] G.S. Ogilvie, L.W. Smith, N. van, D.J. iekerk, F. Khurshed, M. Krajden, M. Saraiya, et al., Women’s intentions to receive cervical cancer screening with primary human papillomavirus testing, Int. J. Cancer 133 (12) (2013) 2934–2943.

S80

Y. Jayasinghe et al. / Journal of Clinical Virology 76 (2016) S74–S80

[25] C.J. Armitage, M. Conner, Efficacy of the theory of planned behaviour: a meta-analytic review, Br. J. Soc. Psychol. 40 (pt. 4) (2001) 471–499. [26] Y. Fenner, S.M. Garland, E.E. Moore, Y. Jayasinghe, A. Fletcher, S.N. Tabrizi, et al., Web-based recruiting for health research using a social networking site: an exploratory study, J. Med. Internet Res. 14 (1) (2012) e20. [27] K.J. McCaffery, L. Irwig, R. Turner, S.F. Chan, P. Macaskill, M. Lewicka, et al., Psychosocial outcomes of three triage methods for the management of borderline abnormal cervical smears: an open randomised trial, BMJ 340 (2010) b4491. [28] M. Hendry, D. Pasterfield, R. Lewis, A. Clements, S. Damery, R.D. Neal, et al., Are women ready for the new cervical screening protocol in England? A systematic review and qualitative synthesis of views about human papillomavirus testing, Br. J. Cancer 107 (2) (2012) 243–254. [29] M. Dieng, L. Trevena, R.M. Turner, M. Wadolowski, K. McCaffery, What Australian women want and when they want it: cervical screening testing preferences, decision-making styles and information needs, Health Expect. 16 (2) (2013) 177–188. [30] K. Scalzo, R. Mullins, The recommended interval for cervical cancer screening: victorian women’s attitudes to an extended interval, Aust. N. Z. J. Public Health 39 (2) (2015) 153–156. [31] F. Sultana, D.R. English, J.A. Simpson, J.M. Brotherton, K. Drennan, R. Mullins, et al., Rationale and design of the iPap trial: a randomized controlled trial of home-based HPV self-sampling for improving participation in cervical

[32]

[33]

[34]

[35]

[36]

screening by never- and under-screened women in Australia, BMC Cancer 14 (2014) 207. A. Szarewski, L. Cadman, D. Mesher, J. Austin, L. Ashdown-Barr, R. Edwards, et al., HPV self-sampling as an alternative strategy in non-attenders for cervical screening—a randomised controlled trial, Br. J. Cancer 104 (6) (2011) 915–920. R. Giorgi, P. ossi, L.M. Marsili, L. Camilloni, A. Iossa, A. Lattanzi, C. Sani, et al., The effect of self-sampled HPV testing on participation to cervical cancer screening in Italy: a randomised controlled trial (ISRCTN96071600), Br. J. Cancer 104 (2) (2011) 248–254. A.P. Ortiz, N. Alejandro, C.M. Perez, Y. Otero, M. Soto-Salgado, J.M. Palefsky, et al., Acceptability of cervical and anal HPV self-sampling in a sample of Hispanic women in Puerto Rico, Puerto Rico Health Sci. J. 31 (4) (2012) 205–212. I.C. Scarinci, A. G. Litton, I. C. Garces-Palacio, E.E. Partridge, P. E. Castle, Acceptability and usability of self-collected sampling for HPV testing among African-American women living in the Mississippi Delta. Women’s health issues: official publication of the Jacobs Institute of Women’s Health. 2013, 23(2), e123–e130. L. Sadler, A. Saftlas, W. Wang, M. Exeter, J. Whittaker, L. McCowan, Treatment for cervical intraepithelial neoplasia and risk of preterm delivery, JAMA 291 (17) (2004) 2100–2106.