Original Study Human Papillomavirus Vaccination and Sexual Behavior in Young Women Mary B. Rysavy BA 1, Jessica D.K. Kresowik MD 1, Dawei Liu PhD 2, Lindsay Mains MD 1, Megan Lessard MPH 2, Ginny L. Ryan MD, MA 1,* 1 2
Department of Obstetrics and Gynecology, Carver College of Medicine, University of Iowa, Iowa City, IA Department of Biostatistics, College of Public Health, University of Iowa, Iowa City, IA
a b s t r a c t Study Objective: To compare sexual attitudes and behaviors of young women who have received or declined the HPV vaccine. Design: Cross-sectional survey. Setting: Obstetrics and gynecology and pediatrics clinics at a large, Midwestern, academic health center. Participants: 223 young women (ages 13-24): 153 who had received HPV vaccination and 70 with no prior HPV vaccination. Main Outcome Measures: Sexual behaviors; attitudes toward sexual activity. Results: Vaccinated young women were slightly but significantly younger than unvaccinated (mean age 19.2 vs 20.0). Both groups showed a large percentage of participants engaging in high-risk sexual behavior (75% vs 77%). The mean age at sexual debut was not significantly different between the groups (16.8 vs 17.0) nor was the average number of sexual partners (6.6 for both). Unvaccinated participants were more likely to have been pregnant (20% vs 8.6%, P 5 .016), although this difference was not significant in multivariate analysis CI [0.9025.177]. Specific questions regarding high-risk sexual behaviors and attitudes revealed no significant differences between the groups. Conclusion: We found that sexual behaviors, including high-risk behaviors, were similar between young women who had and had not received HPV vaccination. Our findings provide no support for suggestions that the vaccine is associated with increased sexual activity. Importantly, we found that young women in our population are sexually active at a young age and are engaged in high-risk behaviors, affirming the importance of early vaccination. Key Words: HPV vaccine, Sexual behavior, Young women
Introduction
Human papillomavirus (HPV) is the most common sexually transmitted infection worldwide and is wellknown for its oncogenic properties.1 Specifically, HPV subtypes 16 and 18 are known to cause nearly 70% of all invasive cervical cancers and 35% of oral cavity and oropharyngeal squamous cell carcinomas.2,3 Although there is no known cure for persistent HPV infection, 2 vaccines have been developed which protect against the 16 and 18 subtypes: Cervarix (GlaxoSmithKline) and Gardasil (Merck). The Gardasil vaccine also protects against HPV subtypes 6 and 11, which are known to cause genital warts.4 For the vaccines to be most effective, the complete series of 3 injections must be administered prior to sexual debut.5 Despite current recommendations for HPV vaccination of all young women at age 11 or 12, vaccine coverage among young women remained under 50% in the US in 2010.6 One proposed reason for low coverage has been the persistence of negative attitudes toward the vaccine, including parental concerns related to the moral connotations of vaccinating adolescent women against a sexually transmitted disease.
The authors indicate no conflicts of interest. Financial support: American College of Obstetricians and Gynecologist/Merck and Company Inc. Research Award. * Address correspondence to: Ginny L. Ryan, MD, MA, University of Iowa Carver College of Medicine, Department of Obstetrics & Gynecology, 200 Hawkins Dr, 31332 PFP, Iowa City, IA 52242; Phone: (319) 384-9170; fax: (319) 384-9367 E-mail address: [email protected] (G.L. Ryan).
Following the approval of the first HPV vaccine in 2006, debate ensued in both the scientific literature and the popular media over whether vaccination against a sexually transmitted infection would cause sexual “disinhibition,” or an increase in sexual activity, in vaccinated youth.7e9 Early studies showed that parental concern about the possibility of sexual disinhibition from the vaccine was a barrier to vaccine uptake.10 In the past few years, several studies have attempted to address linkages between the HPV vaccine and sexual behavior. Generally, we know that young women in the United States tend to become sexually active in their midteenage years.11 An initial study of the idea that HPV vaccination could cause sexual disinhibition used other vaccines as a model to predict disinhibition behaviors after vaccination. This study found that vaccination could possibly cause a reduction in protective behaviors, but likely would not lead to increased risk-taking.12 A 2012 study, one of the first to look at specific sexual behaviors in young women receiving the HPV vaccination, reported no association between having been vaccinated and an increase in risky sexual behavior.13 Another recent study looked at use of healthcare for sexual health indicators and found that vaccinated young women were no more likely to be treated for a sexually transmitted infection (STI) or to become pregnant than if they had not received the vaccine.14 The purpose of our study was to compare the sexual behaviors and attitudes of young women who had received the HPV vaccine against those who had not. We
1083-3188/$ - see front matter Ó 2014 North American Society for Pediatric and Adolescent Gynecology. Published by Elsevier Inc. http://dx.doi.org/10.1016/j.jpag.2013.08.009
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hypothesized that vaccination status would not predict sexual behavior and differences in attitudes towards sex. Materials and Methods
Young women aged 13-23 y were recruited at the University of Iowa Hospitals and Clinics during 2009-2011. A convenience sample of participants was recruited from the general pediatrics, general obstetrics and gynecology, and pediatric/adolescent gynecology clinics. Age-eligible women were approached in clinic by a research assistant and asked if they would be willing to fill out an online survey related to their sexual knowledge and behavior. If willing to participate, each young woman spoke privately with a research assistant who explained the survey and obtained informed consent. For minor participants, assent was obtained from the participant and informed consent was obtained from an accompanying parent. Young women under age 17 who were not accompanied by a parent or guardian could not sign an informed consent and were excluded from participation. All other women within the age range were eligible to participate. Although we do not have data on patients who declined to participate, recruiters reported that a large majority of those approached agreed to participate. When private insurance does not cover the cost of the vaccine, the HPV vaccine is provided free of charge to all young women in Iowa via a statewide vaccination program. A survey instrument was partially modeled after surveys published by Mathematica Policy Research, Inc, which were designed to evaluate abstinence education programs and their impact on sexual attitudes and behavior in teens.15 Some questions were also modeled after surveys published by the National Study of Adolescent Health (Add Health).16 Our resultant survey queried basic demographic information and participants' prior education and current sexual and HPV-related knowledge. The second section of the survey, which is the focus of this paper, addressed participants' attitudes toward sex and their sexual behaviors (including oral, vaginal, and anal intercourse). More specifically, if a participant endorsed a sexual behavior, she was asked the age at which this was first done as well as total number of partners for this behavior. Young women who had previously received the HPV vaccine answered 3 additional questions regarding their attitudes and behavior related to having been vaccinated. All study participants were told that if a question did not apply to them, they could leave the answer space blank. Study patients were compensated for their participation. The survey instrument and study protocols were approved by the University of Iowa Institutional Review Board and Human Subjects Office. Following completion of the survey, question responses were compiled using Microsoft Access 2007 (Microsoft Corp., Redmond, WA) and data analysis was performed using SAS 9.3 (SAS Institute Inc, Cary, NC). Analyses were performed to examine associations between HPV vaccination status and demographic data, sexual attitudes and sexual behaviors. In order to evaluate high-risk behaviors, a composite high-risk behavior score was first assessed using as a
measure any behavior that could expose the participant to HPV (ie, anal, vaginal or oral intercourse). Johnson et al reported increased risk for HPV infection in women who had sex before age 16 and had greater than 2 sexual partners17 so we further analyzed our groups looking at each potentially risky sexual behavior based on age at first participation and number of partners. We also separately examined condom usage, pregnancy, and sexually transmitted disease diagnosis as indicators of high-risk sexual behavior. Univariate analyses were performed on demographic, sexual behavior, and sexual attitude variables using Pearson chi-square or Fisher exact test for the categorical variables and the 2-sample t-test for continuous variables; P-values are reported. Additionally, multivariate logistic regression was performed to examine the effects on sexual attitudes and behaviors of differences in the baseline demographics of our study groups. The analysis presented here is part of a larger study in which power analysis was based on the ability to detect a change in attitudes and behavior over time between the 2 study groups using follow-up surveys. Results
A total of 223 young women were enrolled in the study between 2009 and 2011 (Table 1). The average age was slightly but significantly higher in the unvaccinated group (20.1 vs 19.2, P 5 .044), and the average number of participants still in school was lower in the unvaccinated group (64.7% vs 79.3%, P 5 .021). There was a tendency for the vaccinated group to include more white women than the unvaccinated group, though this was not statistically significant (P 5 .052). Religious differences between the 2 groups were not significant. In comparing sexual behaviors between vaccinated and unvaccinated participants, a high percentage of both groups was found to engage in high-risk sexual behaviors, with
Table 1 Demographics of Participants Who Received or Did Not Receive the HPV Vaccine Variable
Age (y) Race/Ethnicity Asian Black Hispanic White Other Religion Catholic Protestant Other Student Grade in School 7th-8th 9th-12th 13th-16th
Vaccinated Group (n 5 153)
Unvaccinated Group (n 5 70)
19.2 2.8
20.1 2.9
1 5 3 139 5
(1) (3) (2) (91) (3)
2 2 7 56 2
(3) (3) (10) (82) (3)
57 55 40 119
(38) (36) (26) (79)
20 25 23 44
(29) (37) (34) (65)
P
.044 .052
.405
5 (4) 47 (34) 88 (63)
.021 .593
3 (5) 16 (27) 41 (68)
HPV, human papillomavirus vaccine Multivariate logistic regression that controlled for age, student-status, and race did not reveal any significant differences in behaviors or attitudes between the two groups. Data are mean SD or count and frequency: n (%).
M.B. Rysavy et al. / J Pediatr Adolesc Gynecol 27 (2014) 67e71
virtually no significant differences between the groups (Table 2). In looking at the composite high-risk behaviors, which included any behaviors placing participants at risk for HPV infection, 75% of vaccinated and 77% of unvaccinated participants engaged in at least 1 of these behaviors. In both groups, a low percentage of participants used condoms in all sexual encounters (20% vs 25%, not significant). When examining each high-risk behavior individually to consider the age of beginning participation and number of partners, we saw similar behavioral profiles in each activity from both groups. Through univariate analysis, a significant difference was seen in only 1 variable: unvaccinated participants were more likely to have been pregnant (20% vs 8.6%, P 5 .016); however, after performing multivariate logistic regression, this difference was no longer significant.
Table 2 Summary of Sexual Behaviors by Vaccination Group Variable
Vaccinated Group (n 5 153)
Composite high-risk behaviors* 115 (75) Vaginal intercourse Age at first vaginal intercourse !16 23 (24) $16 74 (76) Average age 16.8 2 Number of partners Lifetime O2 59 (63) Lifetime # 2 35 (37) Average number of partners 6.6 7.5 Condom use Used condom all of the time 19 (19) Used condom less than all of the time 80 (81) Anal intercourse Age at first anal intercourse !16 2 (7) $16 27 (93) Number of partners 1 22 (76) $2 7 (24) Oral intercourse Age at first oral intercourse !16 32 (33) $16 66 (67) Number of partners Lifetime O2 48 (52) Lifetime # 2 44 (48) y Pregnancy/sexually transmitted infections Pregnancyz 13 (9) Chlamydia 8 (5) Gonorrhea 3 (2) Genital herpes 5 (3) Syphilis 1 (1) Crabs 1 (1) HIV 2 (1) Genital Warts 4 (3) HPV 14 (9) Trichomoniasis 1 (1) Hepatitis B 1 (1)
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Attitudes toward sexual behavior were not significantly different between groups. For example, 58% of vaccinated young women and 50% of unvaccinated young women affirmed a belief that it is appropriate for dating teens to have sex. Only 5% and 7% of the groups believed that having sex helps a young woman become popular and only 6% and 4% believed that having sex would gain a young woman more respect from her partner. 31% and 29% of each group believed that it was not a problem for teens to have sex as long as they did not become pregnant. Participants in the vaccinated group also answered additional questions about their attitudes towards sexual behavior in relation to having been vaccinated. Only 27% of the vaccinated young women reported getting vaccinated because they felt their sexual behaviors put them at risk for HPV. In addition, a small number (7.5%) felt that the vaccine protected them from all sexually transmitted infections. Discussion
Unvaccinated Group (n 5 70)
P
54 (77)
.749 .768
11 (22) 40 (78) 17 2 28 (57) 21 (43) 6.6 8.8
.665 .513
.968 .407
13 (25) 39 (75) .337 2 (17) 10 (24) .105 6 (50) 6 (50) .295 10 (24) 32 (76) .593 24 (57) 18 (43) 14 3 0 1 0 0 0 1 5 0 0
(20) (4) (0) (1.5) (0) (0) (0) (1) (2) (0) (0)
.016 .763 .242 .435 .501 .501 .339 .575 .618 .498 .496
Data are mean SD or frequency in counts [n (%)]. Data n values reflect number of participant responses to each particular variable; if a participant did not respond to a specific query (e.g. had not participated in anal intercourse, thus had no response to number of partners), she was not included in the analysis. * Composite high-risk behaviors refers to ever participating in behaviors that would risk HPV infection, including anal, vaginal, or oral intercourse. y Numbers reflect participants who reported a positive diagnosis of any of the listed conditions. z Value was not significant after analysis with multivariate logistic regression. OR 2.16, CI 0.902d5.177.
We found that sexual behaviors, including high-risk behaviors, are similar among young women who have and have not received the HPV vaccine. Our findings provide no support for suggestions that the vaccine is associated with increased sexual activity. The suggestion that HPV vaccination would encourage increased sexual activity in vaccinated adolescents was first expressed in the popular media before the FDA had even approved its use. Conservative political groups and abstinence-only education supporters opposed the vaccine because they believed it would condone sexual activity before marriage.18 Such groups believed vaccination would disinhibit young women's sexual desires and lead them to believe they were protected from all HPV strains and other sexually transmitted infections.19 Following the release of the first HPV vaccine, a letter in the Journal of Adolescent Health proposed that “Vaccination might actually increase the notion among adolescents that condoms are no more necessary, and that it is safe to have multiple sexual partners.” The letter cited as precedent experiments with an HIV vaccine that led to behavioral disinhibition.20 Discussion of the behavioral effects of the vaccine on adolescents has continued, even as the vaccine has become widely accepted around the country. Beyond the public debate on the matter, many parents have also expressed worry that the vaccine might cause their daughters to increase their sexual activity,21 which has resulted in a barrier to routine vaccination. An early study examining beliefs about vaccination against a STI showed that 24% of parents who did not want to vaccinate their children believed it would make their child more likely to have sex.22 With education and more widespread use, parental acceptance of the vaccine has increased.23,24 Still, a recent study showed that these beliefs continue: Though current parents are less likely to believe that HPV vaccination would cause young women to be more likely to have sex, older and more conservative parents d 16% of parents in the study d still believed that sexual disinhibition may occur if their daughters are vaccinated.25 Some physicians have even shared concerns of vaccination causing sexual disinhibition. At the 2005 meeting of
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the Advisory Committee on Immunization Practices, 11% of the 294 pediatricians present said that they were worried the vaccine might encourage risky sexual behavior in adolescent patients.18 A 2007 survey of factors influencing pediatricians in their intent to recommend the HPV vaccine again reported that physicians themselves were worried that the vaccine could have an impact on sexual behavior. One physician quote was presented as a summary belief: “administering this [vaccine] may encourage [adolescents] to engage in more risky behavior.”26 Our study does not support the claim that HPV vaccination is associated with increased sexual activity in young women. This should help to reduce concerns from parents, physicians, and other concerned groups. Prior studies that have examined the relationship between sexual behaviors and the HPV vaccine have yielded varying results. Regarding vaccine uptake, several studies have suggested that vaccine initiation is higher in adolescents who have already had sex.27e29 One study found that among young rural Appalachian women, those engaging in risky behaviors were more likely to refuse the vaccine.30 These studies highlight variations in sexual attitudes based on the study population. Several reports published after the completion of our study found that HPV vaccination was not a significant predictor of sexual behavior; one found that vaccinated young women were more likely to have positive attitudes toward maintaining safe sexual health,31 another reported that vaccinated young women were more likely to use condoms than unvaccinated,13 and another recent report showed that vaccinated adolescents were no more likely to become pregnant or be treated for an STI than unvaccinated youth.14 Current or past pregnancy was the only predictor of sexual behavior that we found in univariate analysis, and this was no longer significant when we controlled for the higher age of participants in the unvaccinated group. Women were more likely to have become pregnant as they got older, regardless of vaccine use. Unlike the aforementioned reports,13,27e31 we found no difference between vaccinated and unvaccinated young women in their use of condoms or in their sexual attitudes. In fact, young women who had already received the vaccine did not recognize that they needed to be vaccinated based on previous risky behaviors, even when they admitted to already engaging in sexual behavior that put them at risk for HPV infection. Sexual attitudes have been found to predict sexual behaviors in teens,32 and declared attitudes about sexual behaviors and risk-taking often reflect actual and future behavior.33 As such, the lack of difference between vaccinated young women and unvaccinated young women in our study again fails to support notions that having been vaccinated for HPV would encourage sexual activity. Even though our study did not follow young women longitudinally after vaccination, it appears unlikely from the similarity in sexual attitudes that sexual behaviors will differ between the 2 groups over time. Notably, we observed that young women in our study reported becoming sexually active in their mid-teenage years, which affirms the importance of early HPV vaccination. Our data shows an average age at sexual debut of approximately 17, with 66% of all subjects reaching sexual
debut by age 17. This finding is similar to CDC data that only 27% of 15 to 17-year-olds had reached sexual debut, while 64% of 18-19 year olds had already had sexual intercourse.34 Strengths of our study include being one of a few studies to empirically examine the relationship between HPV vaccination and sexual behavior, and a survey design that looked at this issue using survey questions regarding both behaviors and attitudes about sex. Although the average age in our study was higher than the age at which most young women now receive the HPV vaccine, we corrected for the older age of participants by representing high-risk activity with variables that would not change with time, such as age of sexual debut. We also performed multivariate regression to control for age and found no changes in our conclusion. A weakness of our study was that data were self-reported and subject to reporting bias. As with all studies of this nature, we assume honesty in responses, but cannot guarantee it. Data suggests that adolescents in the age groups we studied tend to report their sexual behaviors honestly in clinical surveys.35 Studies have also reported increased honesty when adolescents use computer-assisted interview technology, as the participants in our study did, in lieu of paper surveys or personal interviews.36 Another potential weakness was a reliance on non-objective measures of sexual activity in this study. While we originally planned to use chlamydia testing as an objective measure, assessment of chlamydia infection could not contribute meaningfully to our conclusions due to low prevalence of sexually transmitted disease in our population. On a related note, because we studied a largely Caucasian population with a low STI prevalence rate, our results may not be widely applicable to a more diverse population or one with a higher STI prevalence. Further research on this topic should prospectively monitor young women immediately following vaccination to observe any changes that might be more closely and temporally related to receiving the vaccine. Our findings did not support the notion that young women who are vaccinated for HPV would be more sexually active than unvaccinated young women. Importantly, young women are engaging in sexual behaviors that put them at risk for HPV at young ages and they need to be vaccinated early in order to provide the best possible protection against cervical cancer. Additionally, the attitudes toward vaccination in the participants who had already received the vaccine suggest that, even though they were already engaging in behaviors that put them at risk for HPV, they did not recognize themselves as needing the vaccine based on those behaviors. This suggests that the encouragement of vaccination from parents and physicians may be extremely important. We believe this study should support parents in their decision to vaccinate and should encourage physicians to recommend the vaccine to early adolescents and their parents, given age of sexual debut and frequency of risky behavior. References 1. Hathaway JK: HPV: diagnosis, prevention, and treatment. Clin Obstet Gynecol 2012; 55:671 2. Clifford GM, Smith JS, Plummer M, et al: Human papillomavirus types in invasive cervical cancer worldwide: a meta-analysis. Br J Cancer 2003; 88:63
M.B. Rysavy et al. / J Pediatr Adolesc Gynecol 27 (2014) 67e71 3. Jayaprakash V, Reid M, Hatton E, et al: Human papillomavirus types 16 and 18 in epithelial dysplasia of oral cavity and oropharynx: a meta-analysis, 1985-2010. Oral Oncol 2011; 47:1048 4. U.S. Food and Drug Administration: Vaccines, Blood & Biologics. Human Papillomavirus Vaccine. Available: http://www.fda.gov/BiologicsBloodVaccines/ Vaccines/ApprovedProducts/ucm172678.htm. Accessed July 27, 2012 5. Centers for Disease Control and Prevention: FDA licensure of bivalent human papillomavirus vaccine (HPV2, Cervarix) for use in females and updated HPV vaccination recommendations from the Advisory Committee on Immunization Practices (ACIP). MMWR Morb Mortal Wkly Rep 2010; 59:626 6. Centers for Disease Control and Prevention: National and state vaccination coverage among adolescents aged 13 through 17 yearseUnited States, 2010. MMWR Morb Mortal Wkly Rep 2011; 60:1117 7. Charo RA: Politics, parents, and prophylaxisemandating HPV vaccination in the United States. N Engl J Med 2007; 356:1905 8. Forster A, Wardle J, Stephenson J, et al: Passport to promiscuity or lifesaver: press coverage of HPV vaccination and risky sexual behavior. J Health Commun 2010; 15:205 9. Specter M: The Bush Administration's War on the Laboratory. New Yorker 2006 March 13;58 10. Brewer NT, Fazekas KI: Predictors of HPV vaccine acceptability: a theory-informed, systematic review. Prev Med 2007; 45:107 11. Santelli J, Ott MA, Lyon M, et al: Abstinence and abstinence-only education: a review of US policies and programs. J Adolesc Health 2006; 38:72 12. Brewer NT, Cuite CL, Herrington JE, et al: Risk compensation and vaccination: can getting vaccinated cause people to engage in risky behaviors? Ann Behav Med 2007; 34:95 13. Liddon NC, Leichliter JS, Markowitz LE: Human papillomavirus vaccine and sexual behavior among adolescent and young women. Am J Prev Med 2012; 42:44 14. Bednarczyk RA, Davis R, Ault K, et al: Sexual activity-related outcomes after human papillomavirus vaccination of 11- to 12-year-olds. Pediatrics 2012; 130:798 15. Trenholm C, Devaney B, Fortson K, et al: Impacts of abstinence education on teen sexual activity, risk of pregnancy, and risk of sexually transmitted diseases. J Policy Anal Manage 2008; 27:255 16. Udry JR, Bearman PS, Harris KM: The National Study of Adolescent Health (Add Health): Study Design. 2003. Available: http://www.cpc.unc.edu/projects/ addhealth/design. Accessed June 9, 2008 17. Johnson AM, Mercer CH, Beddows S, et al: Epidemiology of, and behavioural risk factors for, sexually transmitted human papillomavirus infection in men and women in Britain. Sex Transm Infect 2012; 88:212 18. Stein R: Cervical cancer vaccine gets injected with a social issue. Washington Post 2005 Oct 31. Sec A:3. 19. Gibbs N: Defusing the war over the promiscuity vaccine. Time 2006 Jun 21. Available: http://content.time.com/time/nation/article/0,8599,1206813,00.html. Accessed June 11, 2012
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20. Kapoor S: The HPV vaccine and behavioral disinhibition. J Adolesc Health 2008; 42:105 21. Chan SS, Cheung TH, Lo WK, et al: Women's attitudes on human papillomavirus vaccination to their daughters. J Adolesc Health 2007; 41:204 22. Davis K, Dickman ED, Ferris D, et al: Human papillomavirus vaccine acceptability among parents of 10 to15-year-old adolescents. J Low Genit Tract Dis 2004; 8:188 23. Constantine NA, Jerman P: Acceptance of human papillomavirus vaccination among Californian parents of daughters: a representative statewide analysis. J Adolesc Health 2007; 40:108 24. Ogilvie G, Anderson M, Marra F, et al: A population-based evaluation of a publicly funded, school-based HPV vaccine program in British Columbia, Canada: parental factors associated with HPV vaccine receipt. PLoS Med 2010; 7: e1000270 25. Schuler CL, Reiter PL, Smith JS, et al: Human papillomavirus vaccine and behavioural disinhibition. Sex Transm Infect 2011; 87:349 26. Kahn JA, Rosenthal SL, Tissot AM, et al: Factors influencing pediatricians' intention to recommend human papillomavirus vaccines. Ambul Pediatr 2007; 7:367 27. Taylor LD, Hariri S, Sternberg M, et al: Human papillomavirus vaccine coverage in the United States, National Health and Nutrition Examination Survey, 2007-2008. Prev Med 2011; 52:398 28. Keenan K, Hipwell A, Stepp S: Race and sexual behavior predict uptake of the human papillomavirus vaccine. Health Psychol 2012; 31:31 29. Crosby R, Schoenberg N, Hopenhayn C, et al: Correlates of intent to be vaccinated against human papillomavirus: an exploratory study of collegeaged women. Sex Health 2007; 4:71 30. Mills LA, Vanderpool RC, Crosby RA: Sexually related behaviors as predictors of HPV vaccination among young rural women. J Womens Health (Larchmt) 2011; 20:1909 31. Mather T, McCaffery K, Juraskova I: Does HPV vaccination affect women's attitudes to cervical cancer screening and safe sexual behaviour? Vaccine 2012; 30:3196 32. Lee FA, Lewis RK, Kirk CM: Sexual attitudes and behaviors among adolescents. J Prev Interv Community 2011; 39:277 33. Burack R: Teenage sexual behavior: attitudes towards and declared sexual activity. Br J Fam Plann 1999; 24:145 34. Centers for Disease Control and Prevention: Sexual experience and contraceptive use among female teens - United States, 1995, 2002, and 2006-2010. MMWR Morb Mortal Wkly Rep 2012; 61:864 35. Siegel DM, Aten MJ, Roghmann KJ: Self-reported honesty among middle and high school students responding to a sexual behavior questionnaire. J Adolesc Health 1998; 23:20 36. Turner CF, Ku L, Rogers SM, et al: Adolescent sexual behavior, drug use, and violence: increased reporting with computer survey technology. Science 1998; 280(5365):867
Department of Obstetrics and Gynecology, Carver College of Medicine, University of Iowa, Iowa City, IA Department of Biostatistics, College of Public Health, University of Iowa, Iowa City, IA
a b s t r a c t Study Objective: To compare sexual attitudes and behaviors of young women who have received or declined the HPV vaccine. Design: Cross-sectional survey. Setting: Obstetrics and gynecology and pediatrics clinics at a large, Midwestern, academic health center. Participants: 223 young women (ages 13-24): 153 who had received HPV vaccination and 70 with no prior HPV vaccination. Main Outcome Measures: Sexual behaviors; attitudes toward sexual activity. Results: Vaccinated young women were slightly but significantly younger than unvaccinated (mean age 19.2 vs 20.0). Both groups showed a large percentage of participants engaging in high-risk sexual behavior (75% vs 77%). The mean age at sexual debut was not significantly different between the groups (16.8 vs 17.0) nor was the average number of sexual partners (6.6 for both). Unvaccinated participants were more likely to have been pregnant (20% vs 8.6%, P 5 .016), although this difference was not significant in multivariate analysis CI [0.9025.177]. Specific questions regarding high-risk sexual behaviors and attitudes revealed no significant differences between the groups. Conclusion: We found that sexual behaviors, including high-risk behaviors, were similar between young women who had and had not received HPV vaccination. Our findings provide no support for suggestions that the vaccine is associated with increased sexual activity. Importantly, we found that young women in our population are sexually active at a young age and are engaged in high-risk behaviors, affirming the importance of early vaccination. Key Words: HPV vaccine, Sexual behavior, Young women
Introduction
Human papillomavirus (HPV) is the most common sexually transmitted infection worldwide and is wellknown for its oncogenic properties.1 Specifically, HPV subtypes 16 and 18 are known to cause nearly 70% of all invasive cervical cancers and 35% of oral cavity and oropharyngeal squamous cell carcinomas.2,3 Although there is no known cure for persistent HPV infection, 2 vaccines have been developed which protect against the 16 and 18 subtypes: Cervarix (GlaxoSmithKline) and Gardasil (Merck). The Gardasil vaccine also protects against HPV subtypes 6 and 11, which are known to cause genital warts.4 For the vaccines to be most effective, the complete series of 3 injections must be administered prior to sexual debut.5 Despite current recommendations for HPV vaccination of all young women at age 11 or 12, vaccine coverage among young women remained under 50% in the US in 2010.6 One proposed reason for low coverage has been the persistence of negative attitudes toward the vaccine, including parental concerns related to the moral connotations of vaccinating adolescent women against a sexually transmitted disease.
The authors indicate no conflicts of interest. Financial support: American College of Obstetricians and Gynecologist/Merck and Company Inc. Research Award. * Address correspondence to: Ginny L. Ryan, MD, MA, University of Iowa Carver College of Medicine, Department of Obstetrics & Gynecology, 200 Hawkins Dr, 31332 PFP, Iowa City, IA 52242; Phone: (319) 384-9170; fax: (319) 384-9367 E-mail address: [email protected] (G.L. Ryan).
Following the approval of the first HPV vaccine in 2006, debate ensued in both the scientific literature and the popular media over whether vaccination against a sexually transmitted infection would cause sexual “disinhibition,” or an increase in sexual activity, in vaccinated youth.7e9 Early studies showed that parental concern about the possibility of sexual disinhibition from the vaccine was a barrier to vaccine uptake.10 In the past few years, several studies have attempted to address linkages between the HPV vaccine and sexual behavior. Generally, we know that young women in the United States tend to become sexually active in their midteenage years.11 An initial study of the idea that HPV vaccination could cause sexual disinhibition used other vaccines as a model to predict disinhibition behaviors after vaccination. This study found that vaccination could possibly cause a reduction in protective behaviors, but likely would not lead to increased risk-taking.12 A 2012 study, one of the first to look at specific sexual behaviors in young women receiving the HPV vaccination, reported no association between having been vaccinated and an increase in risky sexual behavior.13 Another recent study looked at use of healthcare for sexual health indicators and found that vaccinated young women were no more likely to be treated for a sexually transmitted infection (STI) or to become pregnant than if they had not received the vaccine.14 The purpose of our study was to compare the sexual behaviors and attitudes of young women who had received the HPV vaccine against those who had not. We
1083-3188/$ - see front matter Ó 2014 North American Society for Pediatric and Adolescent Gynecology. Published by Elsevier Inc. http://dx.doi.org/10.1016/j.jpag.2013.08.009
68
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hypothesized that vaccination status would not predict sexual behavior and differences in attitudes towards sex. Materials and Methods
Young women aged 13-23 y were recruited at the University of Iowa Hospitals and Clinics during 2009-2011. A convenience sample of participants was recruited from the general pediatrics, general obstetrics and gynecology, and pediatric/adolescent gynecology clinics. Age-eligible women were approached in clinic by a research assistant and asked if they would be willing to fill out an online survey related to their sexual knowledge and behavior. If willing to participate, each young woman spoke privately with a research assistant who explained the survey and obtained informed consent. For minor participants, assent was obtained from the participant and informed consent was obtained from an accompanying parent. Young women under age 17 who were not accompanied by a parent or guardian could not sign an informed consent and were excluded from participation. All other women within the age range were eligible to participate. Although we do not have data on patients who declined to participate, recruiters reported that a large majority of those approached agreed to participate. When private insurance does not cover the cost of the vaccine, the HPV vaccine is provided free of charge to all young women in Iowa via a statewide vaccination program. A survey instrument was partially modeled after surveys published by Mathematica Policy Research, Inc, which were designed to evaluate abstinence education programs and their impact on sexual attitudes and behavior in teens.15 Some questions were also modeled after surveys published by the National Study of Adolescent Health (Add Health).16 Our resultant survey queried basic demographic information and participants' prior education and current sexual and HPV-related knowledge. The second section of the survey, which is the focus of this paper, addressed participants' attitudes toward sex and their sexual behaviors (including oral, vaginal, and anal intercourse). More specifically, if a participant endorsed a sexual behavior, she was asked the age at which this was first done as well as total number of partners for this behavior. Young women who had previously received the HPV vaccine answered 3 additional questions regarding their attitudes and behavior related to having been vaccinated. All study participants were told that if a question did not apply to them, they could leave the answer space blank. Study patients were compensated for their participation. The survey instrument and study protocols were approved by the University of Iowa Institutional Review Board and Human Subjects Office. Following completion of the survey, question responses were compiled using Microsoft Access 2007 (Microsoft Corp., Redmond, WA) and data analysis was performed using SAS 9.3 (SAS Institute Inc, Cary, NC). Analyses were performed to examine associations between HPV vaccination status and demographic data, sexual attitudes and sexual behaviors. In order to evaluate high-risk behaviors, a composite high-risk behavior score was first assessed using as a
measure any behavior that could expose the participant to HPV (ie, anal, vaginal or oral intercourse). Johnson et al reported increased risk for HPV infection in women who had sex before age 16 and had greater than 2 sexual partners17 so we further analyzed our groups looking at each potentially risky sexual behavior based on age at first participation and number of partners. We also separately examined condom usage, pregnancy, and sexually transmitted disease diagnosis as indicators of high-risk sexual behavior. Univariate analyses were performed on demographic, sexual behavior, and sexual attitude variables using Pearson chi-square or Fisher exact test for the categorical variables and the 2-sample t-test for continuous variables; P-values are reported. Additionally, multivariate logistic regression was performed to examine the effects on sexual attitudes and behaviors of differences in the baseline demographics of our study groups. The analysis presented here is part of a larger study in which power analysis was based on the ability to detect a change in attitudes and behavior over time between the 2 study groups using follow-up surveys. Results
A total of 223 young women were enrolled in the study between 2009 and 2011 (Table 1). The average age was slightly but significantly higher in the unvaccinated group (20.1 vs 19.2, P 5 .044), and the average number of participants still in school was lower in the unvaccinated group (64.7% vs 79.3%, P 5 .021). There was a tendency for the vaccinated group to include more white women than the unvaccinated group, though this was not statistically significant (P 5 .052). Religious differences between the 2 groups were not significant. In comparing sexual behaviors between vaccinated and unvaccinated participants, a high percentage of both groups was found to engage in high-risk sexual behaviors, with
Table 1 Demographics of Participants Who Received or Did Not Receive the HPV Vaccine Variable
Age (y) Race/Ethnicity Asian Black Hispanic White Other Religion Catholic Protestant Other Student Grade in School 7th-8th 9th-12th 13th-16th
Vaccinated Group (n 5 153)
Unvaccinated Group (n 5 70)
19.2 2.8
20.1 2.9
1 5 3 139 5
(1) (3) (2) (91) (3)
2 2 7 56 2
(3) (3) (10) (82) (3)
57 55 40 119
(38) (36) (26) (79)
20 25 23 44
(29) (37) (34) (65)
P
.044 .052
.405
5 (4) 47 (34) 88 (63)
.021 .593
3 (5) 16 (27) 41 (68)
HPV, human papillomavirus vaccine Multivariate logistic regression that controlled for age, student-status, and race did not reveal any significant differences in behaviors or attitudes between the two groups. Data are mean SD or count and frequency: n (%).
M.B. Rysavy et al. / J Pediatr Adolesc Gynecol 27 (2014) 67e71
virtually no significant differences between the groups (Table 2). In looking at the composite high-risk behaviors, which included any behaviors placing participants at risk for HPV infection, 75% of vaccinated and 77% of unvaccinated participants engaged in at least 1 of these behaviors. In both groups, a low percentage of participants used condoms in all sexual encounters (20% vs 25%, not significant). When examining each high-risk behavior individually to consider the age of beginning participation and number of partners, we saw similar behavioral profiles in each activity from both groups. Through univariate analysis, a significant difference was seen in only 1 variable: unvaccinated participants were more likely to have been pregnant (20% vs 8.6%, P 5 .016); however, after performing multivariate logistic regression, this difference was no longer significant.
Table 2 Summary of Sexual Behaviors by Vaccination Group Variable
Vaccinated Group (n 5 153)
Composite high-risk behaviors* 115 (75) Vaginal intercourse Age at first vaginal intercourse !16 23 (24) $16 74 (76) Average age 16.8 2 Number of partners Lifetime O2 59 (63) Lifetime # 2 35 (37) Average number of partners 6.6 7.5 Condom use Used condom all of the time 19 (19) Used condom less than all of the time 80 (81) Anal intercourse Age at first anal intercourse !16 2 (7) $16 27 (93) Number of partners 1 22 (76) $2 7 (24) Oral intercourse Age at first oral intercourse !16 32 (33) $16 66 (67) Number of partners Lifetime O2 48 (52) Lifetime # 2 44 (48) y Pregnancy/sexually transmitted infections Pregnancyz 13 (9) Chlamydia 8 (5) Gonorrhea 3 (2) Genital herpes 5 (3) Syphilis 1 (1) Crabs 1 (1) HIV 2 (1) Genital Warts 4 (3) HPV 14 (9) Trichomoniasis 1 (1) Hepatitis B 1 (1)
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Attitudes toward sexual behavior were not significantly different between groups. For example, 58% of vaccinated young women and 50% of unvaccinated young women affirmed a belief that it is appropriate for dating teens to have sex. Only 5% and 7% of the groups believed that having sex helps a young woman become popular and only 6% and 4% believed that having sex would gain a young woman more respect from her partner. 31% and 29% of each group believed that it was not a problem for teens to have sex as long as they did not become pregnant. Participants in the vaccinated group also answered additional questions about their attitudes towards sexual behavior in relation to having been vaccinated. Only 27% of the vaccinated young women reported getting vaccinated because they felt their sexual behaviors put them at risk for HPV. In addition, a small number (7.5%) felt that the vaccine protected them from all sexually transmitted infections. Discussion
Unvaccinated Group (n 5 70)
P
54 (77)
.749 .768
11 (22) 40 (78) 17 2 28 (57) 21 (43) 6.6 8.8
.665 .513
.968 .407
13 (25) 39 (75) .337 2 (17) 10 (24) .105 6 (50) 6 (50) .295 10 (24) 32 (76) .593 24 (57) 18 (43) 14 3 0 1 0 0 0 1 5 0 0
(20) (4) (0) (1.5) (0) (0) (0) (1) (2) (0) (0)
.016 .763 .242 .435 .501 .501 .339 .575 .618 .498 .496
Data are mean SD or frequency in counts [n (%)]. Data n values reflect number of participant responses to each particular variable; if a participant did not respond to a specific query (e.g. had not participated in anal intercourse, thus had no response to number of partners), she was not included in the analysis. * Composite high-risk behaviors refers to ever participating in behaviors that would risk HPV infection, including anal, vaginal, or oral intercourse. y Numbers reflect participants who reported a positive diagnosis of any of the listed conditions. z Value was not significant after analysis with multivariate logistic regression. OR 2.16, CI 0.902d5.177.
We found that sexual behaviors, including high-risk behaviors, are similar among young women who have and have not received the HPV vaccine. Our findings provide no support for suggestions that the vaccine is associated with increased sexual activity. The suggestion that HPV vaccination would encourage increased sexual activity in vaccinated adolescents was first expressed in the popular media before the FDA had even approved its use. Conservative political groups and abstinence-only education supporters opposed the vaccine because they believed it would condone sexual activity before marriage.18 Such groups believed vaccination would disinhibit young women's sexual desires and lead them to believe they were protected from all HPV strains and other sexually transmitted infections.19 Following the release of the first HPV vaccine, a letter in the Journal of Adolescent Health proposed that “Vaccination might actually increase the notion among adolescents that condoms are no more necessary, and that it is safe to have multiple sexual partners.” The letter cited as precedent experiments with an HIV vaccine that led to behavioral disinhibition.20 Discussion of the behavioral effects of the vaccine on adolescents has continued, even as the vaccine has become widely accepted around the country. Beyond the public debate on the matter, many parents have also expressed worry that the vaccine might cause their daughters to increase their sexual activity,21 which has resulted in a barrier to routine vaccination. An early study examining beliefs about vaccination against a STI showed that 24% of parents who did not want to vaccinate their children believed it would make their child more likely to have sex.22 With education and more widespread use, parental acceptance of the vaccine has increased.23,24 Still, a recent study showed that these beliefs continue: Though current parents are less likely to believe that HPV vaccination would cause young women to be more likely to have sex, older and more conservative parents d 16% of parents in the study d still believed that sexual disinhibition may occur if their daughters are vaccinated.25 Some physicians have even shared concerns of vaccination causing sexual disinhibition. At the 2005 meeting of
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the Advisory Committee on Immunization Practices, 11% of the 294 pediatricians present said that they were worried the vaccine might encourage risky sexual behavior in adolescent patients.18 A 2007 survey of factors influencing pediatricians in their intent to recommend the HPV vaccine again reported that physicians themselves were worried that the vaccine could have an impact on sexual behavior. One physician quote was presented as a summary belief: “administering this [vaccine] may encourage [adolescents] to engage in more risky behavior.”26 Our study does not support the claim that HPV vaccination is associated with increased sexual activity in young women. This should help to reduce concerns from parents, physicians, and other concerned groups. Prior studies that have examined the relationship between sexual behaviors and the HPV vaccine have yielded varying results. Regarding vaccine uptake, several studies have suggested that vaccine initiation is higher in adolescents who have already had sex.27e29 One study found that among young rural Appalachian women, those engaging in risky behaviors were more likely to refuse the vaccine.30 These studies highlight variations in sexual attitudes based on the study population. Several reports published after the completion of our study found that HPV vaccination was not a significant predictor of sexual behavior; one found that vaccinated young women were more likely to have positive attitudes toward maintaining safe sexual health,31 another reported that vaccinated young women were more likely to use condoms than unvaccinated,13 and another recent report showed that vaccinated adolescents were no more likely to become pregnant or be treated for an STI than unvaccinated youth.14 Current or past pregnancy was the only predictor of sexual behavior that we found in univariate analysis, and this was no longer significant when we controlled for the higher age of participants in the unvaccinated group. Women were more likely to have become pregnant as they got older, regardless of vaccine use. Unlike the aforementioned reports,13,27e31 we found no difference between vaccinated and unvaccinated young women in their use of condoms or in their sexual attitudes. In fact, young women who had already received the vaccine did not recognize that they needed to be vaccinated based on previous risky behaviors, even when they admitted to already engaging in sexual behavior that put them at risk for HPV infection. Sexual attitudes have been found to predict sexual behaviors in teens,32 and declared attitudes about sexual behaviors and risk-taking often reflect actual and future behavior.33 As such, the lack of difference between vaccinated young women and unvaccinated young women in our study again fails to support notions that having been vaccinated for HPV would encourage sexual activity. Even though our study did not follow young women longitudinally after vaccination, it appears unlikely from the similarity in sexual attitudes that sexual behaviors will differ between the 2 groups over time. Notably, we observed that young women in our study reported becoming sexually active in their mid-teenage years, which affirms the importance of early HPV vaccination. Our data shows an average age at sexual debut of approximately 17, with 66% of all subjects reaching sexual
debut by age 17. This finding is similar to CDC data that only 27% of 15 to 17-year-olds had reached sexual debut, while 64% of 18-19 year olds had already had sexual intercourse.34 Strengths of our study include being one of a few studies to empirically examine the relationship between HPV vaccination and sexual behavior, and a survey design that looked at this issue using survey questions regarding both behaviors and attitudes about sex. Although the average age in our study was higher than the age at which most young women now receive the HPV vaccine, we corrected for the older age of participants by representing high-risk activity with variables that would not change with time, such as age of sexual debut. We also performed multivariate regression to control for age and found no changes in our conclusion. A weakness of our study was that data were self-reported and subject to reporting bias. As with all studies of this nature, we assume honesty in responses, but cannot guarantee it. Data suggests that adolescents in the age groups we studied tend to report their sexual behaviors honestly in clinical surveys.35 Studies have also reported increased honesty when adolescents use computer-assisted interview technology, as the participants in our study did, in lieu of paper surveys or personal interviews.36 Another potential weakness was a reliance on non-objective measures of sexual activity in this study. While we originally planned to use chlamydia testing as an objective measure, assessment of chlamydia infection could not contribute meaningfully to our conclusions due to low prevalence of sexually transmitted disease in our population. On a related note, because we studied a largely Caucasian population with a low STI prevalence rate, our results may not be widely applicable to a more diverse population or one with a higher STI prevalence. Further research on this topic should prospectively monitor young women immediately following vaccination to observe any changes that might be more closely and temporally related to receiving the vaccine. Our findings did not support the notion that young women who are vaccinated for HPV would be more sexually active than unvaccinated young women. Importantly, young women are engaging in sexual behaviors that put them at risk for HPV at young ages and they need to be vaccinated early in order to provide the best possible protection against cervical cancer. Additionally, the attitudes toward vaccination in the participants who had already received the vaccine suggest that, even though they were already engaging in behaviors that put them at risk for HPV, they did not recognize themselves as needing the vaccine based on those behaviors. This suggests that the encouragement of vaccination from parents and physicians may be extremely important. We believe this study should support parents in their decision to vaccinate and should encourage physicians to recommend the vaccine to early adolescents and their parents, given age of sexual debut and frequency of risky behavior. References 1. Hathaway JK: HPV: diagnosis, prevention, and treatment. Clin Obstet Gynecol 2012; 55:671 2. Clifford GM, Smith JS, Plummer M, et al: Human papillomavirus types in invasive cervical cancer worldwide: a meta-analysis. Br J Cancer 2003; 88:63
M.B. Rysavy et al. / J Pediatr Adolesc Gynecol 27 (2014) 67e71 3. Jayaprakash V, Reid M, Hatton E, et al: Human papillomavirus types 16 and 18 in epithelial dysplasia of oral cavity and oropharynx: a meta-analysis, 1985-2010. Oral Oncol 2011; 47:1048 4. U.S. Food and Drug Administration: Vaccines, Blood & Biologics. Human Papillomavirus Vaccine. Available: http://www.fda.gov/BiologicsBloodVaccines/ Vaccines/ApprovedProducts/ucm172678.htm. Accessed July 27, 2012 5. Centers for Disease Control and Prevention: FDA licensure of bivalent human papillomavirus vaccine (HPV2, Cervarix) for use in females and updated HPV vaccination recommendations from the Advisory Committee on Immunization Practices (ACIP). MMWR Morb Mortal Wkly Rep 2010; 59:626 6. Centers for Disease Control and Prevention: National and state vaccination coverage among adolescents aged 13 through 17 yearseUnited States, 2010. MMWR Morb Mortal Wkly Rep 2011; 60:1117 7. Charo RA: Politics, parents, and prophylaxisemandating HPV vaccination in the United States. N Engl J Med 2007; 356:1905 8. Forster A, Wardle J, Stephenson J, et al: Passport to promiscuity or lifesaver: press coverage of HPV vaccination and risky sexual behavior. J Health Commun 2010; 15:205 9. Specter M: The Bush Administration's War on the Laboratory. New Yorker 2006 March 13;58 10. Brewer NT, Fazekas KI: Predictors of HPV vaccine acceptability: a theory-informed, systematic review. Prev Med 2007; 45:107 11. Santelli J, Ott MA, Lyon M, et al: Abstinence and abstinence-only education: a review of US policies and programs. J Adolesc Health 2006; 38:72 12. Brewer NT, Cuite CL, Herrington JE, et al: Risk compensation and vaccination: can getting vaccinated cause people to engage in risky behaviors? Ann Behav Med 2007; 34:95 13. Liddon NC, Leichliter JS, Markowitz LE: Human papillomavirus vaccine and sexual behavior among adolescent and young women. Am J Prev Med 2012; 42:44 14. Bednarczyk RA, Davis R, Ault K, et al: Sexual activity-related outcomes after human papillomavirus vaccination of 11- to 12-year-olds. Pediatrics 2012; 130:798 15. Trenholm C, Devaney B, Fortson K, et al: Impacts of abstinence education on teen sexual activity, risk of pregnancy, and risk of sexually transmitted diseases. J Policy Anal Manage 2008; 27:255 16. Udry JR, Bearman PS, Harris KM: The National Study of Adolescent Health (Add Health): Study Design. 2003. Available: http://www.cpc.unc.edu/projects/ addhealth/design. Accessed June 9, 2008 17. Johnson AM, Mercer CH, Beddows S, et al: Epidemiology of, and behavioural risk factors for, sexually transmitted human papillomavirus infection in men and women in Britain. Sex Transm Infect 2012; 88:212 18. Stein R: Cervical cancer vaccine gets injected with a social issue. Washington Post 2005 Oct 31. Sec A:3. 19. Gibbs N: Defusing the war over the promiscuity vaccine. Time 2006 Jun 21. Available: http://content.time.com/time/nation/article/0,8599,1206813,00.html. Accessed June 11, 2012
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20. Kapoor S: The HPV vaccine and behavioral disinhibition. J Adolesc Health 2008; 42:105 21. Chan SS, Cheung TH, Lo WK, et al: Women's attitudes on human papillomavirus vaccination to their daughters. J Adolesc Health 2007; 41:204 22. Davis K, Dickman ED, Ferris D, et al: Human papillomavirus vaccine acceptability among parents of 10 to15-year-old adolescents. J Low Genit Tract Dis 2004; 8:188 23. Constantine NA, Jerman P: Acceptance of human papillomavirus vaccination among Californian parents of daughters: a representative statewide analysis. J Adolesc Health 2007; 40:108 24. Ogilvie G, Anderson M, Marra F, et al: A population-based evaluation of a publicly funded, school-based HPV vaccine program in British Columbia, Canada: parental factors associated with HPV vaccine receipt. PLoS Med 2010; 7: e1000270 25. Schuler CL, Reiter PL, Smith JS, et al: Human papillomavirus vaccine and behavioural disinhibition. Sex Transm Infect 2011; 87:349 26. Kahn JA, Rosenthal SL, Tissot AM, et al: Factors influencing pediatricians' intention to recommend human papillomavirus vaccines. Ambul Pediatr 2007; 7:367 27. Taylor LD, Hariri S, Sternberg M, et al: Human papillomavirus vaccine coverage in the United States, National Health and Nutrition Examination Survey, 2007-2008. Prev Med 2011; 52:398 28. Keenan K, Hipwell A, Stepp S: Race and sexual behavior predict uptake of the human papillomavirus vaccine. Health Psychol 2012; 31:31 29. Crosby R, Schoenberg N, Hopenhayn C, et al: Correlates of intent to be vaccinated against human papillomavirus: an exploratory study of collegeaged women. Sex Health 2007; 4:71 30. Mills LA, Vanderpool RC, Crosby RA: Sexually related behaviors as predictors of HPV vaccination among young rural women. J Womens Health (Larchmt) 2011; 20:1909 31. Mather T, McCaffery K, Juraskova I: Does HPV vaccination affect women's attitudes to cervical cancer screening and safe sexual behaviour? Vaccine 2012; 30:3196 32. Lee FA, Lewis RK, Kirk CM: Sexual attitudes and behaviors among adolescents. J Prev Interv Community 2011; 39:277 33. Burack R: Teenage sexual behavior: attitudes towards and declared sexual activity. Br J Fam Plann 1999; 24:145 34. Centers for Disease Control and Prevention: Sexual experience and contraceptive use among female teens - United States, 1995, 2002, and 2006-2010. MMWR Morb Mortal Wkly Rep 2012; 61:864 35. Siegel DM, Aten MJ, Roghmann KJ: Self-reported honesty among middle and high school students responding to a sexual behavior questionnaire. J Adolesc Health 1998; 23:20 36. Turner CF, Ku L, Rogers SM, et al: Adolescent sexual behavior, drug use, and violence: increased reporting with computer survey technology. Science 1998; 280(5365):867
