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Sexually Transmitted Diseases:
doi: 10.1097/OLQ.0b013e3182641f1c
Original Study

Prevalence and Risk Factors for Oncogenic Human Papillomavirus Infections in High-Risk Mid-Adult Women

Winer, Rachel L. PhD*; Hughes, James P. PhD; Feng, Qinghua PhD; Xi, Long Fu MD, PhD*‡; Lee, Shu-Kuang MS; O’Reilly, Sandra F. BS*; Kiviat, Nancy B. MD; Koutsky, Laura A. PhD*

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Author Information

From the Departments of *Epidemiology, †Biostatistics, and ‡Pathology, University of Washington, Seattle, WA

Supported by the Developmental Awards Program of the National Institutes of Health NIAID Sexually Transmitted Infections and Topical Microbicide Cooperative Research Centers (STI-TM CRC) grant (AI 31448, to the University of Washington), and by a National Institutes of Health K01 grant (AI 079270, to R.L.W.) L.A.K. has received honoraria from Roche Diagnostics and Dana-Farber Cancer Institute.

Correspondence: Rachel L. Winer, PhD, HPV Research Group, University of Washington, Box 359933, 325 9th Ave, Seattle, WA 98104. E-mail: rlw@u.washington.edu.

Received for publication March 20, 2012, and accepted June 11, 2012.

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Abstract

Background: The epidemiology of high-risk (hr) human papillomavirus (HPV) infections in mid-adult women with new sex partners is undefined.

Methods: We analyzed baseline data from 518 25- to 65-year-old women online daters. Women were mailed questionnaires and kits for self-collecting vaginal specimens for polymerase chain reaction–based hrHPV testing. Risk factors for infection were identified using Poisson regression models to obtain prevalence ratios (PRs).

Results: The prevalence of hrHPV infection was 35.9%. In multivariate analysis restricted to sexually active women, the likelihood of hrHPV infection was associated with abnormal Papanicolaou test history (PR = 1.42, 95% confidence interval [CI]: 1.10–1.84), lifetime number of sex partners >14 (compared with 1–4; PR = 2.13, 95% CI: 1.13–4.02 for 15–24 partners; and PR = 1.91, 95% CI: 1.00–3.64 for ≥25 partners), male partners with ≥1 concurrent partnership (PR = 1.34, 95% CI: 1.05–1.71), and male partners whom the subject met online (PR = 1.39, 95% CI: 1.08–1.79). Age was inversely associated with infection only in women who were sexually inactive (PR = 0.67 per 5-year age difference, adjusted for Papanicolaou history and lifetime number of partners). Compared with sexually inactive women, the likelihood of infection increased with increasing risk level (from low-risk to hr partners; P < 0.0001 by trend test). In multivariate analysis, infection with multiple versus single hrHPV types was inversely associated with ever having been pregnant (PR = 0.64, 95% CI: 0.46–0.90) and recent consistent condom use (PR = 0.56, 95% CI: 0.32–0.97), and positively associated with genital wart history (PR = 1.43, 95% CI: 1.03–1.99).

Conclusions: Measures of both cumulative and recent sexual history were associated with prevalent hrHPV infection in this hr cohort of mid-adult women.

Although much is now known about the acquisition and natural history of human papillomavirus (HPV) infections in sexually active young women, less is known about HPV infections in mid-adult women.1 In particular, the risk of acquiring new high-risk (hr) infections from new sex partners is undefined, and the frequency of reactivating infections that were acquired in adolescence or young adulthood is unknown. Whether mid-adult women are susceptible to acquiring new hrHPV infections from new sex partners has important implications for prophylactic vaccine implementation guidelines in mid-adult women. Prophylactic HPV vaccines are not currently licensed for women >26 years of age in the United States.2 It is debatable whether it would be beneficial or cost-effective to vaccinate mid-adult women, or whether there are certain hr groups that might be targeted for vaccination.2–4

Reflective of the marital status of the general population, the majority of mid-adult female participants in HPV studies have been married or in long-term monogamous relationships with male partners. To our knowledge, no studies of HPV infections have specifically targeted mid-adult women with recent new sex partners. In this study, we specifically recruited 25- to 65-year-old US women who reported recent use of online dating websites (i.e., women likely to report recent new sex partners), targeting women past the recommended age for “catch-up” vaccination through the recommended age for cervical cancer screening cessation. For 1 year, women were longitudinally followed with triannual at-home vaginal self-collections for hrHPV testing and detailed health and sexual behavior questionnaires. In this report, we present the baseline prevalence and predictors of hrHPV infections in this hr cohort of mid-adult women.

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METHODS

Between 2007 and 2010, 25- to 65-year-old women were recruited through the Internet and enrolled into a longitudinal study of genital HPV infections. Recruitment advertisements were posted primarily on Craigslist.org (a community-based Web site offering free classified advertisements in >700 cities worldwide). Advertisements were posted weekly in the “volunteer opportunities” section of 1 city on a rotating basis (37 major US cities were targeted). Advertisements were also posted on University of Washington research volunteer recruitment Web sites and other national Web sites offering free classified advertisements. Advertisements targeted 25- to 65-year-old women who reported using the Internet to search for romantic partners within the previous 12 months. Women who were pregnant, breastfeeding, planning a pregnancy in the next 6 months; hysterectomized; immunocompromized; or reported no history of sex with men were not eligible to participate. In all, 1170 women responding to the recruitment advertisements were screened over the telephone, of whom 832 (71.1%) women were eligible; 743 (63.5% of women screened) returned a mailed consent form and were enrolled (Fig. 1). The protocol was reviewed and approved by the University of Washington institutional review board.

Figure 1
Figure 1
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Every 4 months for up to 1 year, enrolled women were mailed demographic, sexual behavior, and health history questionnaires and materials for self-collecting vaginal samples for HPV DNA testing. Self-collection materials included illustrated instructions, 2 Dacron-tipped swabs (2 sequential self-collected swabs increases sensitivity for HPV detection5), a capped tube containing 1.5 mL of Specimen Transport Medium (Qiagen, Gaithersburg, MD), nitrile gloves, and packing and shipping materials. The kit also contained written instructions to refrain from douching, vaginal intercourse, and the use of vaginal medications or preparations for 48 hours before collecting the vaginal samples, and to collect the samples at least 2 days after the end of the last menses. Women were instructed to complete the questionnaire and collect the samples on the same day, and to return the materials in the provided prepaid standard overnight Federal Express envelope.

Vaginal samples were tested for HPV DNA using polymerase chain reaction (PCR)-based methods. Exfoliated cell samples were digested with 20 μg/mL of protease K at 37°C for 1 hour. DNA was isolated using the QIAamp DNA blood mini column (Qiagen, Inc., Valencia, CA) according to the manufacturer’s protocol. Two microliters of purified DNA (equivalent to 1/250 of each sample) was amplified in 50-μL PCR reaction, and 10 μL of PCR products were dotted onto nylon filters and probed with both a biotin-labeled HPV generic probe and a biotin-labeled β-globin probe. Samples negative for β-globin DNA were deemed insufficient. Specimens determined to be HPV positive by generic probe were typed using the Roche Linear Array HPV genotyping test (Roche Molecular Systems, Inc., Alameda, CA) for 37 HPV types.

The current analyses focused on the baseline visit only. We evaluated risk factors for prevalent hrHPV infection (positive for any of the following types classified as carcinogenic, probably carcinogenic, or possibly carcinogenic: 16/18/26/31/33/35/39/45/51/52/53/56/58/59/66/68/73/82/IS396,7) using Poisson regression models with robust variance estimates to obtain prevalence ratios (PRs). Potential risk factors included demographics, smoking history, women’s health history (e.g., pregnancy history, history of an abnormal Papanicolaou [Pap] test result or genital warts, menopausal status, and hormone use), and cumulative and recent sexual behaviors. Age was divided by 5 and included in the model as a continuous variable to reflect the relative change in the likelihood of hrHPV detection associated with a 5-year difference in age (we evaluated a linear trend using a likelihood ratio test to compare a categorical variable based on 5-year age-groups with the linear model based on age divided by 5; the likelihood ratio test was not significant, indicating a linear trend). Cumulative sexual behavior variables included age at first intercourse with a male partner and lifetime number of male sex partners. Recent sexual behavior variables included characteristics of male sex partners and partnerships in the past 6 months. If multiple partners were reported in the past 6 months, the characteristic was summarized across partners/partnerships (Table 3). Variables found to be statistically significant (P < 0.10) in univariate analyses were entered into multivariate models. Forward stepwise regression was used to construct the final multivariate models, with P < 0.10 used as the criterion for entering and removing variables. Because the final multivariate model included partner/partnership variables restricted to women who reported sex with male partners in the past 6 months, women without recent male sex partners were excluded. Although effect modification by recent sexual activity was not formally explored (owing to a limited number of women reporting no male sex partners in the past 6 months; n = 87), we compared the final multivariate model with a second multivariate model that excluded recent partner/partnership variables to explore whether the magnitude of association between hrHPV infection and any other variables in the model differed between recently sexually active women and the full data set of women who were and were not recently sexually active.

Table 3
Table 3
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Separately, we evaluated a composite variable constructed to characterize additive effects of partner/partnership risk factors on the likelihood of hrHPV detection. Partner or partnership characteristics found to be significantly associated (P < 0.10) with hrHPV detection in the univariate analyses described earlier in the text were selected as risk factors and incorporated into this variable (3 risk factors were selected: report of ≥1 casual male sex partner, report of ≥1 male sex partner with a concurrent partnership, and sex with ≥1 male partner whom the subject met online). The composite variable was categorized as a 5-level variable: (1) not sexually active with a male partner in the past 6 months; or sexually active with male partner(s) who (2) did not have any identified risk factors, or had (3) 1 risk factor, (4) 2 risk factors, (5) or all 3 risk factors. We evaluated potential confounding by variables that were associated with hrHPV detection in the univariate analyses described earlier in the text (excluding individual sexual behavior variables over the past 6 months). Each variable was tested individually with the composite variable; those that changed any of the composite variable point estimates by >10% were considered confounders and retained in the final model.

Finally, among women testing positive for hrHPV, we evaluated whether any of the variables described earlier in the text were predictive of testing positive for multiple hrHPV types versus a single hrHPV type. All variables were tested univariately, and forward stepwise regression was used to construct one final multivariate model, with P < 0.10 used as the criterion for entering and removing variables.

Most analyses were prespecified; we explicitly note post hoc analyses.

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RESULTS

Of 743 enrolled subjects, 526 (70.8%) returned their first self-sampling kit and questionnaire. Five were enrolled before turning 25 years of age and were excluded from all analyses. Three (0.6% of 521) samples were insufficient for HPV testing (Fig. 1). The mean age of the remaining 518 subjects at the time of first sample collection was 35.7 (standard deviation: 9.5) years, and the median reported lifetime number of sex partners was 11 (range: 1–300). Other demographic, health, and sexual behavior characteristics are described in Table 1.

Table 1
Table 1
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The prevalence of hrHPV was 35.9%. In total, 41.4% of all hrHPV-positive samples were positive for multiple hrHPV types (range: 1–7 types), representing 14.9% of all samples tested. The most common hrHPV type detected was HPV-16 (Table 2).

Table 2
Table 2
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In univariate analyses, increasing age was negatively associated with hrHPV positivity. History of an abnormal Pap test result, having ever had a follow-up test or procedure after an abnormal Pap test result, and history of genital warts were all positively associated with hrHPV infection (compared with never having had an abnormal Pap test result, the PR for having ever had a follow-up test or procedure after an abnormal Pap test result [e.g., colposcopy, biopsy, or treatment for a cervical lesion] was similar to the PR for never having had a procedure; therefore, the latter was not entered into the multivariate model). Lifetime number of sex partners was categorized into approximate quintiles a priori; women reporting a lifetime number of sex partners >4 were more likely to be positive than those reporting ≤4 partners. Women reporting having had sex with a male partner in the past 6 months were more likely to be hrHPV positive than those who were not sexually active. Among those who were sexually active in the past 6 months, male partner characteristics associated with an increased likelihood of positivity included casual partners, partners reported to have ≥1 concurrent partnership, and partners whom the subject met online. In the final multivariate model (restricted to women who were sexually active in the past 6 months), a history of an abnormal Pap test result (PR = 1.42, 95% confidence interval [CI]: 1.10–1.84) and a lifetime number of sex partners >14, compared with 1–4 partners (PR for 15–24 partners = 2.13, 95% CI: 1.13–4.02; and PR for >24 partners = 1.91, 95% CI: 1.00–3.64), were both positively associated with hrHPV infection. In addition, reports of partners with ≥1 concurrent partnership (PR = 1.34, 95% CI: 1.05–1.71) and partners whom the subject met online (PR = 1.39, 95% CI: 1.08–1.79) were both positively associated with hrHPV infection (Table 3). When we excluded partner/partnership variables from the multivariate model (expanding the data set to include women reporting no male sex partners in the past 6 months), increasing age was statistically significantly negatively associated with hrHPV positivity (PR = 0.92, 95% CI: 0.86–0.99 for each 5-year age difference, adjusting for history of an abnormal Pap test result and lifetime number of sex partners; risk estimates for the other variables evaluated in multivariate analyses were similar between the restricted and full models). We then stratified the risk estimates for the relationship between age and hrHPV infection by recent sexual activity (a post hoc analysis; Fig. 2); a statistically significant relationship between age and hrHPV positivity was observed among women reporting no male sex partners in the past 6 months (adjusted PR = 0.67, 95% CI: 0.49–0.91 for each 5-year age difference), but not among women who were sexually active in the past 6 months (adjusted PR = 0.96, 95% CI: 0.90–1.03 for each 5-year age difference).

Figure 2
Figure 2
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Compared with women who were not sexually active, those who reported sex with male partners with ≥1 identified risk factor (including partners who were casual, who reported to have ≥1 concurrent partnership, and whom the subject met online) were more likely to be hrHPV positive (Table 4). A linear categorical dose-response effect was observed, as the likelihood of hrHPV positivity increased with increasing level of risk (from no recent sexual activity to partners with all 3 identified risk factors; P < 0.0001 by the test for trend). No confounding by any nonpartner/partnership variables was identified.

Table 4
Table 4
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Among women who were hrHPV positive, women who reported having ever been pregnant (PR = 0.64, 95% CI: 0.46–0.90, adjusted for recent condom use and genital wart history) and women reporting having always used condoms with all male partners in the past 6 months (PR = 0.56, 95% CI: 0.32–0.97, adjusted for pregnancy and genital wart history) were less likely to test positive for multiple hrHPV types than a single hrHPV type. Women with a history of genital warts were more likely to test positive for multiple hrHPV types (PR = 1.43, 95% CI: 1.03–1.99, adjusted for pregnancy history and recent condom use; Table 5). In a post hoc analysis, a negative linear dose-response effect was observed between increasing number of births and likelihood of testing positive for multiple hrHPV types (P = 0.015 by the test for trend, adjusted for recent condom use and genital warts history).

Table 5
Table 5
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DISCUSSION

To our knowledge, this is the first study of HPV infections to specifically target mid-adult women with recent new sex partners (46.5% of women in this online dating cohort reported at least 1 new male sex partner in the past 6 months). The overall prevalence of hrHPV infection in this hr cohort of 25- to 65-year-old women was 36%. Population-based data from the United States show a peak in hrHPV prevalence in the early twenties, followed by an age-related decline (in some non-US populations, a second prevalence peak is observed in older women8). Among women self-sampling for HPV in the 2003–2006 population-based National Health and Nutrition Examination Survey, hrHPV prevalence peaked in women aged 20 to 24 years (43%), and then declined with increasing age, ranging from 31% in 25- to 29-year-old women to 24% in those aged 50 to 59 years (compared with our study, the National Health and Nutrition Examination Survey included 4 additional types classified by the International Agency for Research on Cancer as possibly carcinogenic: 64, 67, 69, and 70).9 In our cohort, the relationship between age and hrHPV prevalence varied according to recent sexual activity with male partners. Although hrHPV prevalence declined with age in sexually inactive women, age was unrelated to hrHPV prevalence in sexually active women.

Measures of both cumulative (e.g., lifetime number of male sex partners and history of an abnormal Pap test result) and recent (e.g., report of recent male sex partners with concurrent partnerships, recent casual male partners, and recent male partners whom the subject met online) risk behavior were associated with an increased likelihood of infection. A dose-response relationship was observed, whereby compared with sexually inactive women, the likelihood of hrHPV positivity increased with increasing level of risk, from low-risk partners to hr partners. Previous studies in average-risk populations of mid-adult women have also reported associations between HPV infection and recent markers of risk behavior (e.g., marital status10–12 and recent new partners11–16) in addition to cumulative risk behaviors (e.g., lifetime number of partners11,14,16). Self-reported sexual behavior can be challenging to interpret, as behaviors may correlate over time. Although we measured some cumulative risk behaviors (e.g., lifetime number of partners), residual confounding by past hr sexual behavior may partially account for the observed associations between recent risk behavior and prevalent infection (e.g., women who choose riskier partners in young adulthood may also be more likely to choose riskier partners in mid-adulthood, and also more likely to harbor persistent or reactivated infections from young adulthood). This could explain our finding that report of recent hr partners (e.g., those with concurrent partners), but not recent new partners, was associated with HPV infection. Nonetheless, a role for new hrHPV acquisition in hr mid-adult women cannot be ruled out.

Women who reported recent sex with a male partner whom they met online were more likely to test positive for hrHPV (but not more or less likely to test positive for multiple vs. single hrHPV types). The literature on the association between seeking sex partners via Internet dating or social networking Web sites and sexually transmitted infection risk has been mixed. Several studies have reported an increased likelihood of hr sexual behaviors associated with online sex seeking or online dating,17–19 but studies linking online dating/sex seeking to sexually transmitted infections have been equivocal.20–22 One study aiming to correlate self-reported history of HPV infection with online sex-seeking behavior reported no association (in either men or women).21 To our knowledge, our study is the first to directly evaluate online dating in relation to current HPV infection, through HPV testing.

In our hr cohort of mid-adult women, coinfection with multiple hrHPV types was common (representing 41% of hrHPV infections) and unrelated to age. In contrast, studies in average-risk populations tend to report an inverse relationship between age and multiple-type HPV infections.23–25 For reasons that are unclear, we identified risk factors for multiple- versus single hr–type infections that differed from those associated with testing hrHPV positive versus negative. Among hrHPV-positive women, those reporting a history of genital warts were more likely to test positive for multiple hrHPV types, whereas those reporting always using condoms with male partners in the past 6 months or past pregnancy were less likely to test positive for multiple hrHPV types (in a post hoc analysis, a linear dose-response relationship was observed between number of births and likelihood of single-type hrHPV infection). Parity and genital wart history may reflect cumulative lifetime sexual risk behavior. The inverse association between parity and multiple-type infection is in agreement with previous reports linking increasing number of births to decreased likelihood of infection with multiple HPV types.26,27 Although consistent condom use has been shown to be protective against newly acquired HPV infection in newly sexually active young women, cross-sectional studies have been equivocal, likely owing to the transient nature of HPV infections and difficulty in establishing a temporal relationship between condom use and HPV infection.28 Although recent condom use was unsurprisingly unrelated to hrHPV positivity in this cohort of hr mid-adult women, the association with multiple- versus single-type infection is of interest. In a randomized trial, Hogewoning et al29 reported that condom use promoted regression of cervical intraepithelial neoplasia and clearance of HPV infection, and postulated that condom use might contribute to lowered HPV viral load and clearance by blocking repetitive transmission of shed HPV virus between partners. Applying this theory to our findings, condom use may have the effect of limiting the number of type-specific infections. With longitudinal data, we will be able to further test this theory by exploring the relationship between condom use and persistent type-specific detection.

Limitations to our study should be noted. Given the self-selected nature of our cohort, the results may not be generalizable to all mid-adult women who seek or have had recent new partners. Women reported higher lifetime numbers of male sex partners than reported in national surveys (for example, the median lifetime number of partners reported by 25- to 44-year-old women in our study was 10 vs. 3.6 in the 2006–2008 National Survey of Family Growth30). Furthermore, in this cross-sectional analysis, we were unable to distinguish between persistent and newly acquired or reactivated infections. In future analyses, we will use longitudinal data from this cohort of hr mid-adult women to identify risk factors for newly detected and persistently detected infections. Such longitudinal data are critical for understanding the natural history of HPV infections in mid-adult women and elucidating the relative contribution of reactivation versus new acquisition associated with new sex partners. Additional studies are needed to further evaluate the carcinogenic progression of infections that are acquired in mid-adulthood. Information on new acquisition, persistence, and progression could be used to further inform decisions surrounding prophylactic HPV vaccination recommendations in mid-adult women.

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