The European Journal of Contraception and Reproductive Health Care, 2014; 19: 86–92

Sexual experiences in relation to HPV vaccination status in female high school students in Sweden Magdalena Mattebo∗,†1, Nathalie Gr ün‡1, Andreas Rosenblad†, Margareta Larsson∗, Elisabet Häggström-Nordin∗,#, Tina Dalianis‡ and Tanja Tydén¶ ∗Department

of Women’s and Children’s Health, Uppsala University, Uppsala, †Centre of Clinical Research Västerås, Uppsala University, Central Hospital,Västerås, ‡ Department of Oncology-Pathology, Karolinska Institutet, Stockholm, #School of Health, Care and Social Welfare, Mälardalen University, Västerås, and ¶Department of Public Health and Caring Sciences, Uppsala University, Uppsala, Sweden ............................................................................................................................................................................................................

ABSTRACT

Objectives To investigate sexual experiences, sexually transmitted infections (STIs) and use of condoms in relation to human papillomavirus (HPV)-vaccination status in female high school students. Methods In 2013, 355 female students with a median age of 18 years from randomly selected high schools in Sweden answered a classroom questionnaire on sexual experiences and HPV-vaccination status. Results In total 227/348 (65%) of the women reported having received at least one HPV vaccine dose. Median age at first intercourse was 15 and 16 years respectively, in the 141/227 (62%) vaccinated after, and the 86/227 (38%) vaccinated before their sexual debut. There were no differences between the HPV-vaccinated and non-vaccinated groups regarding condom use, STIs, and experiences of oral and anal sex, or friendswith-benefit relationships. However, having had sexual intercourse and ‘one-night stands’ were more common in the vaccinated group (both p ⬍ 0.05). Conclusion Many students (62%) were vaccinated against HPV, with two-thirds after their sexual debut. There were no differences in condom use and STIs, and only a few differences in sexual experiences between the HPV-vaccinated and non-vaccinated groups. Initiating HPV vaccination before sexual debut is important, as is information about the link between HPV, sexual behaviour and cancer.

K E Y WO R D S

Adolescents; HPV; HPV vaccine; Sexual experiences; Sexual behaviour; Survey research; Sweden

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1These two authors contributed equally to this study. Correspondence: Nathalie Grün, Department of Oncology-Pathology, Karolinska Institutet, Karolinska University Hospital, 171 76 Stockholm, Sweden. Tel: ⫹ 46 8 51776583. E-mail: [email protected]

© 2014 The European Society of Contraception and Reproductive Health DOI: 10.3109/13625187.2013.878021

Sexual experiences in female high school students

I N T RO D U C T I O N

In Sweden, human papilloma virus (HPV) vaccination with the quadrivalent vaccine is now free of charge for 10- to 12-year-old girls within the schoolbased vaccination programme and, in most counties, as catch-up vaccination for girls up to 18 years of age. Similar vaccination programmes are now in place in many western countries1. Yet the introduction of the HPV vaccine has been somewhat controversial in various parts of the world. More specifically, concerns have been raised on whether sexual behaviour can be affected, due to a false sense of security, as a result of being vaccinated against a sexually transmitted infection (STI)2. There is thus a need to follow the present development with the gradual introduction of public HPV vaccination, and possibly related changes in sexual conduct. In Sweden, there is a relatively liberal attitude towards sex outside of a stable relationship and the numbers of sexual partners and casual sexual intercourses without using a condom have increased, as has the number of STIs and teenage abortions3–7. Also likely attributable to changes in sexual behaviour is the recent dramatic rise in incidence of HPVpositive oropharyngeal squamous cell carcinoma, affecting mainly the tonsils and the base of the tongue, and exemplified by a seven-fold increase in HPVpositive tonsillar cancer between 1970 and 2007 in the Stockholm region8,9. Similar trends are noted in other Western countries, resulting in an increased threat by the virus classically associated with cervical and anogenital cancers10,11. In this context in Sweden, HPV-vaccination of young women was gradually introduced in 2006, and by 2007 the cost was reduced for teenage girls; however, it was not until 2012 that HPV vaccination became free of charge within the school vaccination programme, with an uptake of 79% during the first year12. The quadrivalent vaccine accounted for 99% of all vaccine doses13. Initial interviews with young vaccinated women showed that fear of cancer, support from the mothers and mothers’ sponsorship of costs initiated HPV vaccination14. Despite having been vaccinated, many young women were unaware of the relation between sexual behaviour, HPV, and cervical cancer14. However, it was shown that educational intervention in first-year high school students improved knowledge about HPV, although

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attitudes towards HPV vaccination, Pap-smear testing and condom use were harder to influence15. Both Canadian and Swedish investigators observed that parents who were concerned about the potential impact of the HPV vaccine on sexual practices were less likely to have their daughters vaccinated in a school-based vaccination programme2,16. To assess how the situation evolved since the introduction of HPV vaccination, we gathered information on sexual experiences, STIs and use of condoms in relation to HPV-vaccination status among female high school students in Sweden.

METHODS

Population and sampling This study was part of a longitudinal project initiated in 2011 which involved first-year high school students in randomly selected classes in two municipalities in mid-Sweden17. In the second data collection, which took place between January and March 2013, we gathered data from 355 female students, now 17 to 21 years old (median age: 18 years). Of the 355 participants, 338 answered the questionnaire in the classroom setting and an additional 17 absent students (mainly due to an influenza epidemic) replied to a postal questionnaire. A subsample of the participants (n ⫽ 160), also provided a mouthwash sample for oral HPV testing18. The Regional Ethical Review Board in Uppsala, Sweden, (Dnr. 2010/369), approved the research.

Instrument and procedure The questionnaire comprised 48 multiple-choice questions. Relevant questions here were those related to sexual experiences and HPV-vaccination status. Most students were familiar with the procedure, presented previously17. The questionnaire, placed in an envelope, was collected by the first author and colleagues, who were present in the classroom during the proceedings. As a token of gratitude, the students (irrespective of participation or not) received a gift bag with candy, condoms and a lottery ticket. Cards from the local Youth Clinic were also offered, if anybody wanted counselling, along with pamphlets with information on HPV and HPV-vaccination.

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Statistical analysis The data were transferred into the IBM Statistical Packages of Social Sciences, SPSS 20. Descriptive statistics were used and differences in sexual experiences, condom use and STIs between HPV-vaccinated girls and non-vaccinated girls were analysed with Fisher’s exact test and the Chi-squared test. A p-value below 0.05 was considered significant.

R E S U LT S

Characterisation of the participants and their sexual experiences In all, 355 young women participated, but not all answered all questions. In total, 348/355 (98%) reported HPV-vaccination status; 266/319 (80%) stated that they had had sexual intercourse (vaginal coitus); and 260/347 (75%) mentioned experience of oral sex (Table 1 and data not shown). Experience of anal

sex, having friends-with-benefit relationships (i.e., having sex with a friend, either once or more regularly, but without further commitment or economic or other compensation), or one-night stands were less common and reported by 26 to 36% of the respondents. Finally 5% had experience of group sex. Sexual experiences, contraception and STIs in relation to HPV-vaccination status When asked about HPV-vaccination status, 227/ 348 (65%) of the women reported having received at least one dose of the vaccine, but only 86 (38%) of the vaccinated women appeared to have been vaccinated before their sexarche (first vaginal intercourse). Median age at first coitus was 15 years for those vaccinated after their sexual debut, as compared to a median age of 16 years for the women vaccinated before their sexarche (data not shown). Data with regard to sexual experiences, condom use at specific time points, having friends-with-benefit relationships

Table 1 Sexual experiences and condom use by human papillomavirus (HPV)-vaccination status in the 2013 cohort. HPV-vaccinated Items Experience of intercourse Used condom during intercourse First time Last time Experience of receiving oral sex Used protection∗∗∗ when receiving oral sex First time Last time Experience of performing oral sex Used protection∗∗∗ when performing oral sex First time Last time Experience of anal sex Used condom during anal sex First time Last time Experience of group sex Ever had a friends-with-benefits relationship Had one night stand

Yes (n ⫽ 227) n∗(%)

No (n ⫽ 121) n∗(%)

p-value∗∗

181 (84)

83 (70)

0.005

116 (61) 27 (14) 175 (77)

51 (58) 13 (15) 85 (71)

0.79 1 0.15

3 (2) 2 (1) 172 (76)

0 (0) 1 (1) 83 (69)

0.55 1 0.16

11 (6) 3 (2) 58 (26)

5 (6) 2 (2) 29 (24)

1 0.66 0.80

21 20 12 70 92

10 9 5 33 35

1 0.65 0.80 0.54 0.046

(32) (33) (5) (32) (41)

(30) (27) (4) (28) (29)

∗n indicates the number of individuals answering ‘Yes’ to the specific question. ∗∗Fisher’s exact test. ∗∗∗‘Protection’ is referring to the use of condom or dental dam.

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and ‘one night stands’ are shown separately for HPVvaccinated and non-vaccinated individuals in Table 1. There were no significant differences concerning experience of oral and anal sex, or regarding condom use (Table 1). Answering ‘Yes’ when asked about experience of sexual intercourse (vaginal coitus) and ‘one night stands’ were, however, more common in the HPV-vaccinated group (p ⫽ 0.005 and p ⫽ 0.046, respectively; Table 1). There were no significant differences in STIs between the two groups. The most commonly reported STI was Chlamydia (n ⫽ 26; with 18/227 [8%] in the vaccinated- and 8/120 [7%] in the nonvaccinated group). Other STIs were condylomata acuminata (n ⫽ 9), with 6/227 (3%) in the vaccinated group and 3/117 (3%) in the non-vaccinated group, and genital herpes (n ⫽ 1), with 1/222 (0.4%) in the vaccinated group and 0/181 (0%) in the nonvaccinated group. There were no reported cases of syphilis or gonorrhoea. Sexual experiences in a subgroup of young women with a positive oral HPV sample A subgroup of the young women (n ⫽ 160) donated a mouthwash sample that was tested for the presence of HPV-DNA and five (3%) of these had HPV-positive samples. The procedure of HPV analysis is described elsewhere18. All five young women had various sexual experiences (Table 2). However, possibly because of their small number, there were no statistically significant differences between them and the other 155 women. DISCUSSION

Findings We investigated sexual experiences, use of condoms and STIs in female high school students in relation to HPV-vaccination status, and found no significant differences with the exception of experience of vaginal coitus and ‘one night stands’ being more common in the vaccinated group. We also examined the sexual experiences of five young women with an oral HPV infection (for details see Nordfors et al. 201318). These girls seemed to have had their sexual debut at an earlier age and appeared to be more sexually experienced, but differences between these girls and the others who had also given a mouthwash sample that

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was tested for the presence of HPV-DNA, were not statistically significant. Strengths and weaknesses of the study The strengths of this study were that it was performed during a limited time period, in 13 high schools among women in randomly selected classes representing a wide range of study programmes, and included youths with different backgrounds. Moreover, during data collection in classrooms the response rate was high (around 99%) with only two students declining to participate. Furthermore, one of the authors (MM) distributed all the questionnaires and was present in the classroom during data collection enabling participants to ask any questions related to the study. There are, however, some limitations. Due to an influenza epidemic the questionnaire was distributed by regular mail to absent students, and only 17 women replied; this could have introduced a bias as those replying might have differed from absentees who did not. We have no data on the latter. However, the 17 girls who responded by post represented only 5% of the total cohort. In addition, the reliability of the answers should always be considered when using a self-report questionnaire. Questions about sexual experiences are sensitive and some students may have stated more or less experience than they actually had. Recall bias was also a risk especially when the students were asked to recall events that happened several years ago. The participants mentioned their name on the questionnaire and, even though their identity was deleted before analysis, this may have intimidated some respondents. Our findings in relation to those of other studies Few studies have examined sexual experiences in relation to HPV vaccination. Of note, we were able to show that being HPV-vaccinated neither influenced the decision of whether or not to use a condom during sex, nor increased the risk of contracting STIs. This result is in line with findings of another study, which showed no differences in sexual experiences depending on HPV status19. This is of great importance since concerns have been expressed that HPV vaccination may influence sexual behaviour in general, and prevention of STIs in particular20,21.

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90 Yes No Yes 14 No No Yes 14 No No Yes 17 No No No No No

No No Yes 15 No No Yes No answer No answer No answer No Yes No



2 2–5 Yes, 2 doses No Yes 15

No No Yes 15

Yes 14

2–5 No

STI, sexually transmitted infection. ∗‘Protection’ is referring to the use of condom or dental dam.

Total number of sexual partners Vaccinated against HPV Vaccinated against HPV before sexual debut Ever had intercourse Age at first intercourse Used condom during intercourse First time Last time Ever performed oral sex Age when first performed oral sex Used protection∗ when performing oral sex First time Last time Ever received oral sex Age when first receiving oral sex Used protection when receiving oral sex First time Last time Ever had anal sex Age when first having anal sex Used condom when having anal sex First time Last time Ever had an STI Ever had a friend-with-benefits Relationship Ever had group sex

1

Yes

– – Yes, Chlamydia Yes

No No No –

No No Yes 15

No No Yes 15

6–10 Yes, 3 doses No Yes 14

3

Individual

Table 2 Sexual experiences and condom use in the five women with an oral human papillomavirus (HPV) infection.

No

– – No No

No No No –

No No Yes 16

Yes No Yes 16

2–5 Yes, 3 doses No Yes 15

4

Yes

No No Yes, Chlamydia Yes

No No Yes 14

No No Yes 14

No No Yes 14

⬎ 10 Yes, 3 doses No Yes 14

5

Sexual experiences in female high school students Mattebo et al.

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None of the women in our study were vaccinated within the school-based vaccination programme, since it had not yet started when they were 12 years of age. Only 38% of the women had been vaccinated before their sexual debut.We do not have any information about why this group had opted for vaccination. Our findings thus need to be confirmed in further studies and among girls who have been part of the school-based vaccination programme and preferably vaccinated before their sexual debut. While the HPV vaccine is being marketed as protective against cervical cancer, it may also prevent HPV-positive oropharyngeal cancer, but this has yet to be established. A subsample of the participants in this study provided a mouthwash sample, and the analysis of these samples revealed that only five girls (3%) had detectable oral HPV; none of these girls were vaccinated prior to their first experience of oral sex18. Since they were so few it was not possible to analyse differences in sexual experiences between those who had an HPV-positive mouthwash and those who had not, so further studies are needed to follow oral and genital HPV-prevalence in the population over time. Nevertheless, our findings highlight the importance of providing, whenever possible, correct, repeated information and counselling about the link between sexual behaviour and STI risk. Midwives, physicians and school nurses who regularly meet young women and men are key resources in this respect.Youth Clinic visits, health interviews with the school nurse or HPV-vaccination appointments are all useful opportunities. A message that needs to be repeated is that condom use and limiting the number of casual partners have been shown to be protective measures, and that secondary prevention, such as PAP smear tests, still is important, despite immunisation.22 Relevance of the findings: Implications for clinicians and policymakers Understanding the attitudes and behavioural patterns of young adults is essential in tailoring sexual education with a view to improving their future sexual and reproductive health. However, sexuality education given in schools is not the only source of information for young Swedes. The sexualised content of popular media affects the opinions and behaviour of youths17,23–26. Contraception is rarely discussed or displayed in sexualised media or in pornographic material; thus, it is important to emphasise

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the value of sexual education and youth-friendly counselling as a counterweight to these media forms. Future research In sum, many of the female students were vaccinated against HPV after their sexual debut, but there were no differences in condom use and STIs, and only few differences in sexual experiences between the HPV-vaccinated and non-vaccinated groups. Initiating HPV vaccination before sexual debut is important. Whether or not HPV vaccination influences one’s sexual experiences needs to be further investigated, among other vaccinated cohorts. In Sweden, this should be followed up in the future in high school students who received their HPV vaccine within the context of the school-based programme. CONCLUSION

Two-thirds (65%) of the women were vaccinated against HPV, but vaccination had taken place after the first sexual intercourse for most. Sexual intercourse and ‘one-night stands’ were more common in the HPV-vaccinated group, but there were no differences between HPVvaccinated and non-vaccinated women in condom use, STIs or other sexual experiences. Information and counselling about STIs, especially regarding cause and effect of HPV infection, remain important, as does initiating HPV vaccination before sexual debut. AC K N OW L E D G E M E N T S

Many thanks to Andreas Ährlund-Richter, Cecilia Nordfors and Torbjörn Ramqvist for their helpful comments. Declaration of interest: The authors report no conflict of interest. The authors alone are responsible for the content and the writing of the paper. This work was made possible by funding from the Swedish Research Council K2011-56X-15282-07-06, the Swedish Cancer Foundation 120417 and 120535, the Stockholm Cancer Foundation 121043, Karolinska Institutet 2013fobi37387, the Stockholm City Council 520007, the Medical Faculty of Uppsala University 2012/1609, Uppsala-Örebro Regional Research Council RFR 312791, the European Society of Contraception and Reproductive Health, and ALF-funds.

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Sexual experiences in relation to HPV vaccination status in female high school students in Sweden.

To investigate sexual experiences, sexually transmitted infections (STIs) and use of condoms in relation to human papillomavirus (HPV)-vaccination sta...
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