https://orcid.org/0000-0001-9163-8103
ABSTRACT
Objectives
We compared HPV vaccine initiation and completion of heterosexual with lesbian and bisexual (LB) women.
Methods
We aggregated National Health and Nutrition Examination Survey data from 2009 to 2016 for 3,017 women aged 18 to 34 y in the United States. HPV vaccine initiation was defined as reported receipt of ≥1 dose of the vaccine and completion as receipt of the three recommended doses. Weighted percentages and multivariable logistic regression models were used to examine differences in HPV vaccine initiation and completion between heterosexual and LB women.
Results
Approximately 12% of respondents self-identified as LB women. Overall, a higher percentage of respondents (26%) had initiated the HPV vaccine than completed the three vaccine doses (17%). In the bivariate analysis, LB women had higher initiation ([35% of LB women versus 25% heterosexual]; p = .0012) and completion rates ([24% of LB women versus 17% heterosexual]; p = .0052) than heterosexual women. After adjusting for covariates, compared to heterosexual women, LB women were 60% (aOR = 1.60, 95% CI: 1.16–2.19) more likely to initiate and 63% (aOR = 1.63, 95% CI: 1.12–2.37) more likely to complete the HPV vaccine.
Conclusions
Although LB women had higher likelihood of HPV vaccine initiation and completion compared with heterosexual women, their HPV vaccine uptake was well below the Healthy People 2020 target (80%). Understanding differences in the drivers of vaccine uptake in the LB population may inform strategies that would further increase HPV vaccine uptake toward achieving the 80% completion target.
Introduction
Human papillomavirus (HPV) is spread via skin-to-skin contact and infects cutaneous and mucosal epithelial cells in many areas of the body and comprises over 150 subtypes.Citation1 An estimated 80–90% of sexually active people will acquire HPV in their lifetime.Citation2 Among women aged 15 to 59 y, approximately 14million new cases of sexually transmitted infections are attributable to HPV each year.Citation3 For most people exposed, the virus is harmless and the body naturally clears the infection. However, for some, certain strains of the HPV infection are associated with cervical, anal, oropharyngeal, vaginal, vulvar, and penile cancersCitation4-6 and second primary cancers.Citation7–9 Specifically, HPV accounts for about 44,000 HPV-associated cancers per year: about 25,000 among women, and about 19,000 among men.Citation10
The Advisory Committee on Immunization Practices recommends routine HPV vaccination for adolescents between 11 and 12 y of age.Citation11 Catch-up vaccination is also recommended for both males and females aged 13–26 y and shared clinical decision-making through age 45.Citation11 Despite the availability, safety, and efficacy of the HPV vaccines,Citation12 uptake has been suboptimal compared to other routine vaccinations in adolescents. In 2017, 65.5% of adolescents aged 13–17 y received at least one dose of HPV vaccine (68.6% for girls and 62.6% for boys) and 48.6% complete the series (53.1% for girls and 44.3% for boys).Citation13 These rates fall short of the Healthy People 2020 goal of 80% completion of the three-dose vaccine among males and females 13–15 y olds.Citation14 For young adults aged 18–26 y, this uptake is even lower, with national initiation rates of 40% for women and only 8% for men.Citation15 Data from the 2013–2015 National Health Interview Survey data reported HPV vaccine initiation was 51.6% among bisexual females and 40.2% for heterosexual females.Citation16
Sexual minority women (i.e., lesbians and bisexuals, LB) are an often-overlooked group despite their risk for HPV infection. Sexual minority women are at increased risk of HPV infection and cervical cancer from current or prior sexual partners, both female and male.Citation17–19 Previous studies report that about 30% of LBs have had a history of genital HPV infections compared with 23% of heterosexual women,Citation20 and about 12% have had a history of genital warts vs. 7% of heterosexual women.Citation21 Moreover, sexual minority women may be at a higher risk for cervical cancer than heterosexual women because sexual minority women are less likely to receive Papanicolaou (Pap) smear screening,Citation22,Citation23 and experience more sexual violence.Citation24,Citation25 With a differential prevalence of HPV infection among sexual minority versus heterosexual women but lower prevalence of regular Pap test use, HPV vaccination among sexual minorities should be an important strategy for preventing HPV-related disease. Therefore, the aim of this study was to compare HPV vaccine initiation and completion between heterosexual and LB women using the National Health and Nutrition Examination Survey (NHANES) data from 2009 to 2016 which is a probability sampling design to provide national estimates of various health outcomes.
Methods
Data collection
We utilized publicly available data from the NHANES, pooled from 2009 to 2016 for 3,017 women aged 18 to 34 y. The censored upper age was selected because these women would have been eligible to have received the HPV vaccine at some point after it was licensed in the U.S. in 2006. The NHANES is a nationally representative cross-sectional survey of United States adults and children that assesses health and nutritional status by using in-home interviews and physical examinations. Starting in 1999, the NHANES surveys about 5000 new persons annually. Combining data across several years provides adequate sample size for hard-to-reach populations such as sexual minority women. Survey response rates for the NHANES-examined sample ranged from 71% to 80% for the 6-y period.Citation26 More details regarding the NHANES design and sampling strategies are described elsewhere.Citation27 This study did not require ethical approval from an institution review board since we used publicly available datasets.
Measures
HPV vaccination was assessed with the question “Human Papillomavirus (HPV) vaccine is given to prevent cervical cancer in girls and women. There are two HPV vaccines available called Cervarix and Gardasil. It is given in 3 separate doses over a 6 month period. How many doses have you received?” We defined HPV vaccine initiation as reported receipt of at least one dose of the vaccine. HPV vaccine completion was defined as reported receipt of three recommended doses. We used 3-dose as completion since the 2-dose vaccination series was not recommended until 2016 when the survey had already been conducted. Those who answered, “don’t know” (n = 101) were included in the “No” initiation/completion group. In addition, a sensitivity analysis was performed where the “don’t know” group were excluded.
The main independent variable for our study was sexual orientation. In NHANES, gender was assessed with the question “What is the gender of the respondent? Male or Female”. Sexual orientation for females aged 18–59 y was then assessed using the sexual orientation question: “Do you think of yourself as … heterosexual or straight (that is, sexually attracted only to men); homosexual or lesbian (that is, sexually attracted only to women); bisexual (that is, sexually attracted to men and women); something else; or you’re not sure?” For the present study, we defined LB as women who self-identified either as lesbian, bisexual, or something else/not sure. Reported sexual orientation was then dichotomized as heterosexual versus LB. We also conducted a sensitivity analysis which excluded women who answered something else/not sure. The following covariates based on a literature review were included in the model: participants’ age, race/ethnicity (non-Hispanic White, non-Hispanic Black, Hispanic, and other race – including multiracial), marital status (married/other), education (high school diploma or less, some college or 2-y degree, and 4-y college graduate or higher), and annual household income (≤$24 999, 25 000 USD to 54 999 USD, 55 000 USD to 99 999 USD, and 100 000+ USD).Citation28,Citation29 HPV vaccine initiation and completion rates have been shown to vary significantly by rural-urban residence; however, we were unable to adjust for rural-urban status because NHANES do not have Metropolitan Statistical Area (MSA) status or Rural-Urban Continuum (RUC) codes.
Statistical analysis
Analysis was conducted between January and March 2019. We analyzed data by using SAS version 9.4 survey procedures (SAS Institute, Cary, NC), incorporating both the design information and weights as specified in the NHANES Analytic and Reporting Guidelines. The survey procedures, which incorporate survey-sampling weights to account for the complex sampling design of NHANES, provide representative estimates of the United States population. We compared demographic characteristics by sexual orientation using chi-square test for proportions and the student t-test for continuous variables. Weighted multivariable logistic regression models were used to examine differences in HPV vaccine initiation and completion. All variables were included in the multivariable models regardless of their association with the outcome variable.
To examine the effect of potential recall bias, we conducted three separate sensitivity analyses where we excluded women (n = 101) who answered don’t know/refuse to the HPV vaccination question (model 1); excluded women (n = 82) who answered something else/don’t know to the sexual orientation question (model 2); and treated the something else/don’t know as a category in the sexual orientation variable (Model 3). Weighted multivariable logistic regression models (a total of six) were used to examine differences in HPV vaccine initiation and completion for each model above. All tests were two sided, and an alpha of <0.05 or confidence intervals that exclude one were considered statistically significant.
Results
Of the 7129 women aged 18–34 y old, 3041 answered the sexual orientation question. Among the 3041 women, we excluded 24 who refused to answer the question, resulting in 3017 women being included in the study. shows the characteristics of the study population overall and by sexual orientation. All percentages presented shown are weighted. The average age was 25.3 (SD = 5.0) y and approximately 377 (11.7%) women self-identified as LB. Overall, 25.9% of the women had initiated the HPV vaccine, and the initiation rate among LB women was significantly higher than heterosexual women (34.6% of LB women versus 24.8% of heterosexual women, p = .0012). Overall vaccine completion rate was 17.4%, and similarly the rate among LB women was significantly higher than heterosexual women (24.1% of LB women versus 16.5% of heterosexual, p = .0052). Heterosexual women were more likely to be married (p < .0001) and earn higher income (p < .0001) than their LB counterparts.
Table 1. Characteristics of adult women aged 18–34 by sexual orientation, NHANES (2009–2016)
presents the crude and adjusted odds of HPV vaccine initiation and completion based on sexual orientation. In the crude model, LB women were more likely to initiate (aOR = 1.61, 95% CI: 1.20–2.15) and complete (aOR = 1.61, 95% CI: 1.15–2.24) the HPV vaccine than heterosexual women. After adjusting for potential confounders, the results remained similar. Compared to heterosexual women, LB women were 60% more likely to initiate (aOR = 1.60, 95% CI: 1.16–2.19) and 63% more likely to complete (aOR = 1.63, 95% CI: 1.12–2.37) the HPV vaccine. In the adjusted model, a 1-y increase in age was associated with lower odds of initiating (aOR = 0.82, 95% CI: 0.80–0.85) and completing (aOR = 0.86, 95% CI: 0.83–0.89) the HPV vaccination. Women who were not married were more likely to initiate (aOR = 1.34, 95% CI: 1.02, 1.75) and complete (aOR = 1.61, 95% CI: 1.17, 2.22) the HPV vaccine compared to those that were married. The likelihood of initiating and completing the HPV vaccine declined steadily across education levels and was lowest for those with high school diploma or less compared to those with college degree or higher.
Table 2. Weighted multivariable logistic regression models for HPV vaccine uptake among young adult women, NHANES (2009–2016) aged 18–34 y
The sensitivity analyses are presented in . Overall, the findings from the sensitivity analyses were similar to that of the main analyses. In model 1 where we excluded women who answered don’t know/refuse to the HPV vaccination question, LB women were more likely to initiate (aOR = 1.59, 95% CI: 1.15–2.19) and complete (aOR = 1.63, 95% CI: 1.12–2.37) the HPV vaccine than heterosexual women. Similarly, in model 2 where we excluded women who answered something else/don’t know to the sexual orientation question, LB women were more likely to initiate (aOR = 1.75, 95% CI: 1.24–2.48) and complete (aOR = 1.76, 95% CI: 1.17–2.64) the HPV vaccine than heterosexual women. Finally, in model 3 where we treated the something else/don’t know as a category in the sexual orientation variable, compared to heterosexual women, LB women were more likely to initiate (aOR = 1.76, 95% CI: 1.24–2.48) and complete (aOR = 1.76, 95% CI: 1.17–2.64) the HPV vaccine. There were no differences between women who answered something else/don’t know and heterosexual women.
Table 3. Weighted multivariable logistic regression models for HPV vaccine uptake among young adult women, NHANES (2009–2016) aged 18–34 y [Sensitivity Analyses]
Discussion
Cancer risk and outcomes among LBs is an important public health concern, as formalized in multiple position statements (e.g. American Society of Clinical Oncology) and designation as a priority population by the National Institutes of Health.Citation30,Citation31 In this study, we investigated the association between sexual orientation and HPV vaccine uptake among young adult women aged 18–34 y using a national sample. The vaccination rate overall was low with only 1-in-4 having initiated the vaccine and about 1-in-5 having completed the vaccine dose. After adjusting for covariates, our study showed that LB women were 60% and 63% more likely to initiate and complete the HPV vaccine, respectively, compared to heterosexual women.
This study found that HPV vaccination rate (both initiation and completion) was very low in both LB (35%, 25%) and heterosexual (24%, 17%) women even though it was higher in LB women. The initiation rate for LB was slightly higher than what Agénor et al.Citation29 reported (22.5%) but less than the 45% reported by McRee et al.Citation32 In addition, the completion rate in our study was less than what was reported by McRee et al. (32%).Citation32 It should be noted that McRee et al.Citation32 used data from 543 LB and bisexual women ages 18–26 during Fall 2013 and Agenor et al.Citation29 used the 2006–2010 National Survey of Family Growth data for 3,253 women and girls aged 15–25 y. Our findings show that vaccination rates have been increasing compared to Agenor et al.Citation29 study, which is expected. It is hard to explain how the vaccination rates in McRee et al.Citation32 were much higher than what we found in our study. These vaccination rates are far below the Healthy People 2020 goal of achieving 80% vaccination rates. After adjusting for covariates, we found that adult LB women were still more likely to initiate and complete the vaccine than their heterosexual peers. Interestingly, several studies have shown that LB women compared to heterosexual women are significantly less likely to receive a regular Pap smear screening, which is the most important screening tool for the detection of precancerous cervical abnormalities.Citation11,Citation12 Therefore, HPV vaccination holds great promise and importance for the primary prevention of HPV-associated diseases in LB women.
There are several explanations for the higher HPV vaccination uptake observed among LB women. LB women are more likely to have a sexual encounter at an early age, have more male and female partners, and experience more sexual violence than their heterosexual peers.Citation16,Citation17,Citation33 Therefore, LB women might experience more sexual and reproductive health risks, which may encourage them to initiate and complete HPV vaccination as a preventive measure. In addition, the assertion that LB women have more sexual partners may influence health-care providers to recommend the HPV vaccine to this group.Citation33 Furthermore, previous studies and the current one have found that unmarried women are more likely to initiate and complete the HPV vaccination. Also, in our study, LB women were less likely to be married than heterosexual peers. This could, therefore, explain why they were more likely to initiate and complete the vaccine compared with heterosexual women.
Implications
With LB women at increased risk of HPV infection,Citation17–19 and having lower prevalence of Pap test use thereby having a higher risk of cervical cancer,Citation11,Citation12,Citation34 improving HPV vaccine uptake is paramount for preventing HPV-related disease. Effective policy interventions such as increasing coverage for HPV vaccination and implementing opt-out provisions in schools could help increase vaccine uptake in adolescents and young adults,Citation35 irrespective of sexual minority status. Future HPV prevention strategies should be enhanced due to the effect of vaccination on the cost-effectiveness of existing cervical screening programs. Regardless of sexual orientation identity, health-care providers should counsel women and offer HPV vaccination to every individual who meets age guideline since provider recommendationCitation36 is the main predictor of vaccine uptake. Furthermore, the 2010 Affordable Care Act (ACA)’s policy of increasing access to preventive services for HPV vaccine coverage without cost sharing for individuals aged 19–25 has affected the likelihood of initiating and completing the HPV vaccine among young adult women, increasing it by 7.7 and 5.8 percentage points, respectively.Citation37 A couple of studies have observed that 1 dose of the HPV vaccine may gain similar protection against HPV infection compared with those who received additional doses. There should be more clinical trials in the future to evaluate the efficacy of a single-dose regime compared with 2 or 3 doses.Citation38,Citation39
Limitations
The study does have some limitations. Our study combined LB and bisexual women into one group, which precludes assessing differences between those sexual minority subgroups among women. We were unable to distinguish between these groups due to the small sample sizes. Second, the use of self-reported measures of HPV vaccine initiation and completion, as well as sexual minority status, could have introduced misclassification due to recall bias. However, previous studies have shown that recall and electronic medical records for HPV vaccine are comparable.Citation40 There was also a high non-response rate for the sexual orientation question which could have affected findings. But the survey weights generated by NHANES do account for non-response bias; therefore, we assume this effect will be minimized. Third, there could be a risk of social desirability bias which could affect our findings. Fourth, there is the potential of clustering of both individual-level and contextual factors that logistic regressions are unable to account for. This could lead to the underestimation of standard errors of regression coefficients, leading to an overestimation of observed effect sizes. However, this bias is minimized due to the fact that we accounted for the complex survey design used for NHANES which adjusts for oversampling, stratification, and clustering. Lastly, although we assessed and controlled for a limited number of factors that are reported in NHANES, the potential for residual confounding remains. For example, there was no information on provider recommendation, which has been shown to positively improve vaccination rates, Citation36 nor rural-urban status of participants.
Conclusions
This study indicates that LB women are more likely to both initiate and complete the HPV vaccine than heterosexuals. Continued inclusion of sexual minority status on national surveys will allow for a more nuanced comparison of this population including sexual minority subpopulations compared to heterosexuals. Further research to understand the factors that increase uptake by LB women can aid in improving uptake in this sexual minority population and thus among all women irrespective of the sexual orientation.
Acknowledgments
Portion of this work was presented at the Ninth Annual AACR Conference on the Science of Cancer Health Disparities in Racial/Ethnic Minorities and the Medically Under-served, Fort Lauderdale, FL.
Authors would like to acknowledge Ms. Erika Juhlin for her technical assistance and for proofreading this manuscript.
Disclosure statement
All authors have no conflict of interest to declare.
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