PEDIATRICS Vol. 122 No. 1 July 2008, pp. 1-7 (doi:10.1542/10.1542/peds.2007-2515)
ARTICLE |
Behavior in Early Adolescence and Risk of Human Papillomavirus Infection as a Young Adult: Results From a Population-Based Study
a Department of General Pediatrics, University of Michigan, Ann Arbor, Michigan
b Department of Epidemiology, University of Washington, Seattle, Washington
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONREFERENCES |
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OBJECTIVE. The goal of this study was to determine the utility of a risk factor-based approach to human papillomavirus catch-up vaccination.
METHODS. Data from waves I and III of the National Longitudinal Study of Adolescent Health were examined to determine the association between adolescent characteristics and future human papillomavirus infection. Analysis was restricted to 3181 female subjects who were >12 years of age when risk factors were assessed in wave I (1994–1995) and who underwent human papillomavirus testing as young adults in wave III (2001–2002). The main outcome of interest was a positive test result for 
1 of 4 human papillomavirus types (human papillomavirus-6, -11, -16, or -18) targeted by the human papillomavirus vaccine currently available in the United States. Separate analyses were performed for sexually active and virginal adolescents. Poststratification sampling weights were used to generate nationally representative estimates.
RESULTS. Although nearly one half (43%) of the female adolescents were sexually active in wave I, adolescent sexual activity status was not associated with future detection of vaccine-specific human papillomavirus infection. Furthermore, for both virginal and sexually active adolescents, none of the assessed risk factors was associated with increased odds of future vaccine-specific human papillomavirus infection in multivariate models. Similar results were obtained when all high-risk human papillomavirus types were assessed as the outcome measure.
CONCLUSIONS. Behavioral risk factors assessed during adolescence are inadequate predictors of future infection with vaccine-type human papillomavirus. A risk factor-based approach to human papillomavirus catch-up vaccination is unlikely to be an effective implementation strategy.
Key Words: human papillomavirus • vaccine • risk factors • adolescent
Abbreviations: HPV—human papillomavirus • CI—confidence interval • Add Health—National Longitudinal Study of Adolescent Health
In June 2006, the US Food and Drug Administration licensed the first vaccine against human papillomavirus (HPV) for use in girls and women 9 to 26 years of age.1 This tetravalent vaccine is highly effective in preventing infection and clinical sequelae resulting from HPV-6, -11, -16, and -18.2–5 These 4 HPV types are thought to account for 
70% of cases of cervical cancer and >90% of cases of genital warts.6–8 Widespread uptake of this vaccine is expected to have a significant impact in reducing the incidence of these diseases.
After licensure, the Advisory Committee on Immunization Practices recommended that the HPV vaccine be universally provided to all 11- to 12-year-old girls. Comprehensive "catch-up" immunization of older adolescents and young adults not previously vaccinated against HPV was also advised.9 However, with a list price of $120 per dose ($96 per dose under the Vaccines for Children Program),10 the high cost raises concerns that financial constraints may hinder universal accessibility of this vaccine. Barriers include high up-front costs to stock the vaccine, low levels of reimbursement from private insurers, and inconsistent coverage by governmental programs for HPV vaccination of older adolescents and young adults.11 Indeed, a recent report suggested that many states are struggling to provide this vaccine to all eligible girls and women.12
Immunization of all girls and women entitled to the vaccine would undoubtedly provide the most-comprehensive protection against HPV infection. However, because financial barriers might make this strategy difficult to implement, some have suggested that individual-level risk factors could be used to "target" HPV catch-up vaccination preferentially to girls and women at highest risk for acquiring HPV. Although previous studies of sexually active adolescents and young adults identified specific sexual partnership, behavioral, and sociodemographic characteristics associated with increased risk for HPV infection,13–16 a limitation of many of those studies was that they identified women with current HPV infection and analyzed potential risk factors for infection retrospectively. Few studies have evaluated the ability of specific risk factors to predict future HPV infection prospectively; this is an important distinction, given that HPV vaccines must be provided before vaccine type-specific infection to be effective. Furthermore, no studies have evaluated the characteristics of virginal girls that predict acquisition of HPV infection after sexual debut.
The National Longitudinal Study of Adolescent Health (Add Health) provides an opportunity to determine whether specific adolescent characteristics are risk factors predictive of future HPV infection among young adults. Using these data, we tested 2 hypotheses, that is, (1) among sexually active girls and women, the risk factors identified retrospectively in other studies as being associated with current HPV infection also would be predictive of future HPV infection and, (2) among virgins, risk factors associated with the future acquisition of other sexually transmitted diseases and/or with engagement in high-risk sexual behaviors would be predictive of future HPV infection. Because our interest was in potentially developing a clinical risk assessment scoring tool that could be used to triage young women for HPV vaccination, we focused our analysis specifically on the evaluation of risk factors that could be assessed easily in a typical outpatient clinical encounter.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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Data Source
Data for this analysis were derived from Add Health. A detailed description of Add Health survey and data collection procedures was reported previously.17,18 Briefly, Add Health is a longitudinal study of adolescents enrolled in grades 7 to 12 that evaluates how social factors and health-related behaviors influence health outcomes. Add Health uses a stratified, school-based, sampling strategy to provide nationally representative estimates.
Data collection for Add Health occurred in 3 "waves" over a period of 6 years. Approximately 90 000 students completed in-school surveys as part of wave I (1994–1995). Of these, a subsample (n = 20 745) also underwent an extensive in-home survey that evaluated adolescents’ behaviors, attitudes, relationships, and sociodemographic characteristics. Additional in-home surveys occurred in wave II (1996) and wave III (2001–2002) for all wave I in-home participants who could be identified (wave II, n = 14 738; wave III, n = 15 197). In addition, 12 966 participants in wave III provided a urine sample for testing for a variety of sexually transmitted diseases. Our analysis used data from waves I and III. All Add Health activities were approved by the University of North Carolina at Chapel Hill institutional review board. Additional approvals for these specific analyses were provided by institutional review boards at the University of Michigan and the University of Washington.
Study Sample
Type-specific, urine-based, HPV testing was performed in wave III for a nationally representative subsample of 3483 girls who were sexually active.14 Details of the HPV testing protocol and HPV test targeting procedures were described previously.14,19 For these analyses, we used data for 3196 of these girls who had nonmissing cross-sectional sampling weights and were >12 years of age in wave I. Children who were 
12 years of age in wave I (n = 80) were excluded from our analysis because they would not be eligible for catch-up HPV immunization, defined by the Advisory Committee on Immunization Practices guidelines for this vaccine as occurring for children 13 years of age.9 Although overall estimates of HPV prevalence are based on data for these 3196 women, we used data for only 3181 women for analyses stratified according to sexual activity, excluding an additional 15 women for whom sexual activity information was missing.
Measures
The primary outcome measure was positive test results in wave III for any of the 4 HPV types (HPV-6, -11, -16, and -18) included in the currently licensed HPV vaccine. Because additional HPV types may be incorporated in future iterations of HPV vaccines, we also assessed positive test results for an expanded panel of HPV types that included HPV-6, HPV-11, and "high-risk" HPV types (HPV-16, -18, -26, -31, -33, -35, -39, -45, -51, -52, -53, -56, -58, -59, -64, -66, -67, -68, -69, -73, and -82) as a secondary outcome.
Adolescent risk factors to be assessed were identified by searching the published literature. For sexually active adolescents, we considered risk factors that were associated with either cervical HPV-related disease or HPV infection.13–16 For adolescents who were not sexually active, we considered risk factors associated with future sexually transmitted disease acquisition and/or eventual engagement in high-risk sexual behaviors,18,20–24 because there were no published studies on risk factors among virgins for future HPV infection. Because we were interested in potentially developing a risk assessment tool that could be used in outpatient settings to target HPV catch-up vaccination, we limited the number of risk factors to be evaluated and focused specifically on factors that could be easily assessed during a typical clinical encounter. Expert consensus was used to select the final list of risk factors included in our analysis.
Adolescent sexual activity status was determined by using wave I data and was defined by a positive response to the question, "Have you ever had sexual intercourse?" or by reports of ever having a sex partner. For sexually active adolescents, 5 risk factors were assessed, that is, (1) high lifetime number of sex partners, defined as having >1 partner, including both romantic and "nonromantic" relationships (defined in the Add Health protocol); (2) history of ever having a significantly older male sex partner, defined as having a male sex partner >2 years older than the respondent, including both romantic and nonromantic relationships; (3) new sex partner within the past year, defined by calculating the time interval between the interview date and the initiation of sexual activity with either romantic or nonromantic partners; (4) history of illegal drug use, defined as having ever used cocaine, inhalants, other illegal drugs ("LSD, PCP, ecstasy, mushrooms, speed, ice, heroin, or pills"), or injectable drugs; and (5) history of sex while impaired by drinking, defined as have ever gotten "into a sexual situation that you later regretted because you had been drinking."
For virginal adolescents, 6 risk factors were assessed, that is, (1) history of ever having an older partner, defined as having a male romantic or nonromantic partner >2 years older than the respondent; (2) history of school problems/delinquency, defined as self-report of ever having been suspended or expelled from school or having a positive response to select items from the Add Health delinquency scale; (3) low high school grade point average, defined as a grade point average of <3.0 using the average of self-reported grades for English, math, social studies, and science; (4) lack of perceived parental disapproval of sex, defined by not having a response of strongly disapprove or disapprove to the question, "How would your [mother/father] feel about your having sex at this time in your life?" or by not having a response of strongly agree or agree to the question, "If you had sexual intercourse, it would upset your [mother/father]"; (5) regular use of cigarettes/alcohol, defined by an affirmative response to any of the following: ever having "smoked cigarettes regularly, that is, at least 1 cigarette every day for 30 days," trying to quit smoking cigarettes in the past 6 months, drinking on at least 2 or 3 days per month in the past 12 months, drinking 5 drinks at least 3 times in the past 12 months, or getting into trouble at school, getting into trouble with parents or friends, getting into fights, getting into a sexual situation, or getting sick because of drinking; and (6) history of illegal drug use, defined as described above for sexually active adolescents.
Four sociodemographic variables also were evaluated. These included age (categorized as 13-15 years or 16 years) and grade (categorical) in school at the time of the wave I interview, race (white, black, or other), and Hispanic ethnicity.
Statistical Methods
Separate analyses were performed for sexually active and virginal adolescents, as defined by their self-reported sexual activity status in wave I. Bivariate associations were assessed by using Pearson's design-based 
2 tests. Multivariate logistic regression models assessed the independent association between adolescent risk factors and HPV positivity, with adjustment for sociodemographic variables. Logistic models included all of the risk factors and sociodemographic variables identified a priori as potentially important predictors of HPV infection. A subanalysis restricted to subjects who were between the ages of 18 and 21 years in wave III was also performed, to focus more specifically on capturing both persistent and transient HPV infections that had not yet had time to clear. All analyses were conducted by using Stata 8 software (Stata Corp, College Station, TX) and were weighted to account for the cluster sampling design of Add Health and to generate nationally representative estimates.
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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Of the 3181 female subjects included in our analysis, 43% of the sample (weighted estimate; 95% confidence interval [CI]: 39%–48%) reported being sexually active in wave I of the study. These sexually active adolescents tended to be older and in a higher grade in school and were more likely to be black, compared with those who had not yet initiated sexual activity in wave I. HPV prevalence levels were similar in the 2 groups (Table 1).
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In wave III, 9.0% (95% CI: 7.6%–10.4%) of the study sample tested positive for
1 of the 4 HPV types found in the currently licensed HPV vaccine (HPV-6, -11, -16, and -18). Less than 1% of women tested positive for 2 or 3 of these HPV types simultaneously, and no women tested positive for all 4 HPV vaccine types. Fifty-three percent of the subjects who tested positive for HPV in wave III were virgins in wave I. When an expanded panel of HPV, composed of HPV-6, HPV-11, and all high-risk HPV types, was considered, the prevalence of infection was 20.6% (95% CI: 18.6%–22.6%). The overall prevalence of HPV infection in the sample, when all HPV types were considered, was 26.2% (95% CI: 23.9%–28.5%). Bivariate analyses demonstrated that there was no significant association between adolescent sexual activity status and detection of vaccine-type HPV as a young adult (Table 2). Among virginal adolescents, none of the risk factors assessed was associated with increased odds of testing positive for vaccine-type HPV as a young adult, although a history of illegal drug use was associated with decreased odds of testing positive for vaccine-type HPV as a young adult. Among sexually active adolescents, only a history of having sex while impaired by alcohol was significantly associated with increased odds of testing positive for vaccine-type HPV as a young adult. When the outcome measure was expanded to include all high-risk HPV types, none of the factors evaluated for virgins or for sexually active adolescents was associated with high-risk HPV infection as a young adult (data not shown).
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A similar pattern of adolescent risk factors and young-adult infection with vaccine-specific HPV types was found with multivariate logistic regression analysis (Table 3). As in the bivariate analyses, among virgins, having a history of illegal drug use was associated with decreased odds of young-adult HPV infection (Table 3). In the multivariate model, the association of vaccine-type HPV with having sex while impaired by drinking (among sexually active adolescents) remained elevated, but the statistical significance was borderline (odds ratio: 1.82; 95% CI: 0.94–3.54; P = .08). When the analysis was expanded to include all high-risk HPV, none of the factors evaluated for virgins or for sexually active adolescents was associated with high-risk HPV infection (data not shown).
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The vast majority of HPV infections are transient, becoming undetectable with molecular assays after a period of 4 to 18 months.25–28 Because of this, cross-sectional analyses of HPV prevalence may miss women with previous transient infections who demonstrate negative HPV results at the time of testing. To evaluate the potential impact of this length-biased sampling, we performed a subgroup analysis restricted to the youngest women (18–21 years of age) tested for HPV in wave III, because the infections among these women would more likely represent new-onset, transient HPV infections, compared with those detected in older women with more sexual experience. Analyses restricted to this subgroup also demonstrated no association between adolescent risk factors and positive test results for HPV vaccine types (data not shown).
We were interested in understanding whether the observed general lack of association between adolescent risk factors and young-adult HPV infection could be explained on the basis of "reclassification" of study subjects from low-risk categories for a given variable during adolescence (in wave I) to the higher-risk category for that variable during young adulthood (in wave III). To explore this, we determined the proportion of study subjects who changed their risk classification between waves I and III. For sexually active adolescents, this type of analysis was permissible for 4 of the risk factors, that is, having an older sex partner, having a high lifetime number of sex partners, having sex while impaired by alcohol, and illegal drug use. Of the subjects who did not have an older sex partner in wave I, nearly 73% reported an older sex partner by wave III. Similarly, 69% of subjects who had a low lifetime number of sex partners in wave I (defined as 1 partner) were reclassified as having a high lifetime number of sex partners in wave III (defined as >3 sex partners). For the variables of having sex while impaired by alcohol and illegal drug use, a smaller but still substantial proportion of subjects moved from the low-risk category to the high-risk category between waves I and III (10% for having sex while impaired by alcohol and 28% for illegal drug use). In bivariate analyses, only reclassification to the higher-risk category for illegal drug use was associated with increased risk of vaccine-specific HPV (7.9% of nonreclassified subjects and 14.5% of reclassified subjects tested positive for HPV; P = .0080). For virginal adolescents, this type of analysis was permissible for only 2 risk factors, namely, having an older partner and illegal drug use. Sixty-seven percent of subjects who did not have a significantly older romantic partner in wave I reported this in wave III. For illegal drug use, 28% of subjects moved to the higher-risk category by wave III. Among these, only reclassification to the higher-risk category for having an older partner was associated in bivariate analyses with increased risk of vaccine-specific HPV (3.3% of nonreclassified subjects and 11.2% of reclassified subjects tested positive for HPV; P < .0001).
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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Our study used population-based, longitudinal data to evaluate the association between potential behavioral risk factors occurring during adolescence and infection with vaccine-type HPV (HPV-6, -11, -16, and/or -18) as a young adult. None of the risk factors we evaluated, including sexual activity status during adolescence, seemed to predict adequately future acquisition of these 4 HPV types. A similar lack of association occurred when we expanded our outcome measure to include positive test results for HPV-6, HPV-11, or any of the high-risk HPV types. Our results therefore imply that using risk factors to target specific adolescents for HPV catch-up vaccination is not a practical strategy for implementation of the currently available vaccine or future HPV vaccines that may provide protection against additional HPV types. Instead, our findings underscore the need for comprehensive catch-up vaccination of all eligible women, as recommended by the Advisory Committee on Immunization Practices.9
Historically, attempts to target vaccination to specific high-risk populations have had mixed success as an implementation strategy. For example, multiple policies aimed at selective vaccination of individuals at high risk against hepatitis B did little to affect the overall population incidence of this virus,29 which eventually led to adoption of a universal vaccination approach.30,31 Conversely, a targeted approach to hepatitis A vaccination was so successful that infection rates in the targeted populations declined below those seen in populations for which vaccination was not recommended.32 HPV infection differs from other vaccine-preventable diseases because it is nearly ubiquitous in the sexually active population; estimates suggest that >80% of the US population will have had previous infections by the age of 50 years.33 Furthermore, even among young women who report a single sex partner, rates of HPV infection are high.34 This high prevalence and incidence make it difficult to define high-risk groups for vaccination, a conclusion underscored by our finding that, for many of the risk factors assessed, individuals frequently moved from low-risk categories to higher-risk categories as they aged and movement to the higher risk classification did not consistently predict HPV infection. We think that these findings, combined with the fact that none of the adolescent characteristics we assessed (including adolescent sexual activity status) was associated with increased odds of HPV infection, support the idea that essentially all individuals who become sexually active are at risk of eventually acquiring this infection.
One notable finding from our study was the statistically significantly decreased odds of vaccine-type HPV infection among virgins who reported a previous history of illegal drug use. This association is the opposite of what would be expected and may represent a spurious finding related to the relatively small number of study participants with this risk factor (Table 2). Alternatively, because the Add Health sample was derived by using a school-based sampling strategy, it is possible that adolescents who used illegal drugs but were able to maintain school attendance had behaviors, beliefs, or peer support influences that placed them at decreased risk for HPV infection. A similar association might not have been observed if users of illegal drug who had dropped out of school were included in the sample.
HPV infection generally occurs shortly after sexual debut.35 For most women, infections clear spontaneously, becoming undetectable with molecular assays after 18 months.25–28 In these analyses, assessment of adolescent risk factors for HPV infection occurred 6 years before the HPV testing was performed. Because we did not have information on HPV status before wave III, it is likely that the number of women classified in our analysis as testing negative for HPV (implying that there had been no previous infection with HPV and that HPV vaccination would be protective) is inflated, which could bias our results. In an attempt to circumvent this limitation, we performed a subanalysis specifically among the youngest women (18–21 years of age) tested for HPV in wave III, because younger women generally have less sexual experience and therefore are more likely to have incident initial HPV infections captured at the time of testing in wave III. The absence of association between adolescent risk factors and young-adult HPV infection in this subanalysis supports our conclusion that risk factor assessment during adolescence would be of limited value for predicting future HPV infection and should not be used as a vaccine-targeting strategy.
An additional limitation of our study was that HPV testing and typing for Add Health were performed with urine specimens. Urine-based polymerase chain reaction assays for HPV detection are less sensitive than assays performed with cervical swab specimens,36–38 which suggests that some cases of prevalent HPV infection were missed. Nevertheless, this noninvasive sampling technique permitted the assessment of early risk factors for later acquisition of HPV infection in a nationally representative, population-based sample, strengthening the generalizability of our results.
Given that a risk factor-based approach does not seem to be a reasonable option for implementing HPV catch-up vaccination, alternative solutions to meet the financial demands of universal HPV catch-up vaccination must be developed. Vaccination programs already seem to be struggling to provide this vaccine,12 and the situation is likely to become critical if vaccine licensure is expanded to include older women and men, as is anticipated.9 A bivalent HPV (HPV-16 and -18) vaccine is currently in late-stage clinical trials and is expected to enter the US marketplace in the near future.39 This may drive down the price of HPV vaccines in the future, potentially alleviating some of the financial pressures currently being encountered. However, even if the price of the HPV vaccine decreases significantly, the expected addition of other vaccines to the recommended immunization schedule indicates that a long-term plan to ensure ongoing universal access to all recommended vaccines needs to be developed.
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ACKNOWLEDGMENTS |
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This research uses data from Add Health, a program project designed by J. Richard Udry, Peter S. Bearman, and Kathleen Mullan Harris and funded by grant P01 HD31921 from the National Institute of Child Health and Human Development, with cooperative funding from 17 other agencies. This work was supported in part by the 2007 Ambulatory Pediatric Association Young Investigators grant program.
Special acknowledgment goes to Ronald R. Rindfuss and Barbara Entwisle for assistance in the original study design.
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FOOTNOTES |
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Accepted Oct 16, 2007.
Address correspondence to Amanda F. Dempsey, MD, PhD, MPH, Child Health Evaluation and Research Unit, University of Michigan, 300 North Ingalls Building, Room 6E08, Ann Arbor, MI 48109-0456. E-mail: adempsey{at}umich.edu
Financial Disclosure: The University of Washington receives funds from Merck for Dr Koutsky to conduct HPV vaccine trials.
Persons interested in obtaining data files from Add Health should contact Add Health, Carolina Population Center, 123 W. Franklin St, Chapel Hill, NC 27516-2545.
| What's Known on This Subject Little is known about the association between adolescent behavioral risk factors and future HPV infection.
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| What This Study Adds This study is the first to evaluate the prospective association between behavioral risk factors during adolescence and future HPV infection.
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PEDIATRICS (ISSN 1098-4275). ©2008 by the American Academy of Pediatrics
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