Abstract
Human papillomavirus (HPV) is a common sexually transmitted infection. Binge drinkers often engage in HIV/HPV co-infection high-risk behaviors. We examined the association between binge drinking, HIV/HPV co-infection risk, HIV testing and HPV vaccination among young adults. Data from the 2017 Behavioral Risk Factor Surveillance System survey were examined. Participants (N=430/450,016; 0.11%) were HPV vaccine-eligible young adults ages 18-26 years. Multivariable logistic regression examined the association between binge drinking in the past 30 days, HIV/HPV co-infection high-risk risk behaviors, HIV testing, and HPV vaccination (initiated/completed, unvaccinated) among young adults. Respondents were primarily cisgender (99.8%), non-Hispanic White (41.4%), employed (46.2%) or student (35.4%), and insured (68.2%). Most did not binge drink (55.2%). The majority did not engage in HIV/HPV co-infection high-risk risk behaviors (78.2%). More than one-half had never been tested for HIV (59%) nor vaccinated against HPV (60.6%). Although binge drinkers (44.8%) were significantly more likely to engage in HIV/HPV co-infection high-risk behaviors (OR=2.1;95%CI:1.0-4.5), binge drinking was not positively associated with HIV testing (OR=0.98;95%CI:0.63-1.53). After adjusting for demographics and HIV/HPV co-infection high-risk behaviors, one (aOR=2.71; 95% CI: 1.11-6.65) and two episodes (aOR=3.05; 95% CI: 1.26-7.41) of binge drinking in the past 30 days were significantly associated with HPV vaccination uptake. Positive associations between HPV vaccination and participants having an HIV test in 2017 (aOR=3.86;95%CI:1.42-10.55) and before 2017 (aOR=2.62;95%CI:1.23-5.56) were also statistically significant. Because young adult binge drinkers are more likely to engage in HIV/HPV co-infection high-risk behaviors, promoting HPV vaccination and HIV testing are important public health objectives.
Keywords: Behavior Risk Factor Surveillance System (BRFSS), Human Papilloma Virus (HPV), Human Immunodeficiency Virus (HIV), HPV Vaccination, Binge drinking, HIV testing, HIV risk behaviors, Alcohol, Young Adults
INTRODUCTION
Annually, the Human Papilloma Virus (HPV) affects approximately 14 million individuals in the United States (U.S.), making it the most prevalent sexually transmitted infection (STI) (Center for Disease Control and Prevention, 2013; Satterwhite et al., 2013). Those between ages 15 to 24, in particular, account for 50% of all new STI cases each year (Markowitz et al., 2014; Shannon & Klausner, 2018). Although majority of HPV-related illnesses are low-grade lesions (e.g. genital warts) or resolve to virus-free, asymptomatic states (Gargano et al., 2017), persistence of oncogenic HPV subtypes in the human epithelium increases the risk for cancer development (Oh et al., 2015). Specifically, persistent infection with high-risk (HR) subtypes of HPV is primarily responsible for the development of cervical cancer (Bosch, Lorincz, Muñoz, Meijer, & Shah, 2002; Oh et al., 2015). Other malignancies associated with persistent HR-HPV include penile (de Sousa, Isaura Danielli Borges et al., 2015), head and neck cancers (Chen, Sun, & Jiang, 2016; Gillison et al., 2000), as well as, anal, vulvar, vaginal cancers (De Vuyst, Clifford, Nascimento, Madeleine, & Franceschi, 2009). These carcinogenic processes occur mostly as a result of the oncogenic proteins E6 and E7 of HR-HPV which include HPV 16 and HPV 18 (Chen et al., 2016). Accordingly, the World Health Organization describes HPV types 16 and 18 as the cause for 70% of cervical cancers (World Health Organization, 2019). Moreover, the occurrence of HPV-related cancers, especially in the oropharynx and anus, continue to rise significantly despite a reduction in cancer mortalities caused by most etiologies (Jemal et al., 2013). Consequently, the HPV vaccine is currently recommended by the Center for Disease Control and Prevention’s (CDC) Advisory Committee on Immunization Practices (ACIP) as part of the vaccination schedule for boys ages 13 to 21 and girls 11 to 26 years old (Centers for Disease Control and Prevention, 2011).
Alcohol consumption severely impairs normal functioning of the immune system, which is the body’s defense mechanism against infectious agents (Cook, 1998; Molina, Happel, Zhang, Kolls, & Nelson, 2010; Szabo, 1997). As a result, acute and/or chronic abuse of alcohol increase susceptibility to and severity of infectious diseases, such as the HPV infection. A prospective U.S. study observed that men who self-reported high levels of alcohol consumption per day had significantly higher prevalence of HPV infections compared to men who consumed lower levels of alcohol (P< 0.001) (Schabath et al., 2015). Additionally, the association between alcohol use and HPV-related endpoints among other study populations (e.g. sexually active college women, uncircumcised Danish men) has been well documented in scientific literature (Ho, Bierman, Beardsley, Chang, & Burk, 1998; Nielsen et al., 2013). What is less frequently examined, however, are the links between alcohol use and HR-HPV persistence (Oh et al., 2015). Among the currently published literature, women who recently used alcohol had a higher risk of developing continuous cervical HPV positivity for 3 consecutive years [odds ratio (OR) 2.49, 95% confidence interval (CI) 1.32–4.71] (Oh et al., 2015). Similarly, a 12-year retrospective study found that advanced cancer stage among young patients suffering from oral squamous cell cancers (OSCC), was significantly associated with alcohol consumption, as well as tobacco use (P=0.001) (Hellen-Bandeira-de-Pontes Santos et al., 2016).
High-risk sexual behaviors, such as trading sex for money or drugs, engaging in sex with multiple partners and/or without a condom, and unprotected anal intercourse, as well as injection drug use, could potentially lead to acquiring the Human Immunodeficiency Virus (HIV) infection and other STIs (Cooperman, Arnsten, & Klein, 2007; Jenness et al., 2011; Ramirez-Valles, Garcia, Campbell, Diaz, & Heckathorn, 2008). These HIV risk behaviors have been shown to be significantly associated with high-risk drinking behaviors, such as binge drinking (≥ 5 drinks for men, or ≥ 4 drinks for women, on any one occasion in the past 30 days) (Wen, Balluz, & Town, 2012). For instance, 18- to 64-year old binge drinkers are twice as likely to report HIV risky behaviors compared to their non-binge drinking counterparts (Wen et al., 2012). The clustering of these specific risk factors - binge drinking, unsafe sexual practices, and HIV/STI infections - has been thoroughly reported in several scientific studies (Chersich, M. F. et al., 2007; Chersich, Matthew F., Bosire, King’ola, Temmerman, & Luchters, 2014; Chiao, Morisky, Rosenberg, Ksobiech, & Malow, 2006).
Current Investigation
To date, limited research has examined individual-level characteristics associated with HPV vaccine uptake (e.g., female gender and self-reported HIV testing) (Bass, Leader, Shwarz, Greener, & Patterson, 2015). Interestingly, some studies have shown a positive association between binge drinking and HIV testing (Bass et al., 2015); however, little is known about why this association might occur and whether an association exists between binge drinking and HPV vaccination status. The primary objective of our study, therefore, was to examine the association between HPV vaccination uptake and binge drinking among young adults. We also explored among this population the association between HPV vaccination uptake and HIV testing, as well as risky behaviors for HIV/HPV co-infection.
METHODS
Data Source
Secondary data from the 2017 Behavioral Risk Factor Surveillance System (BRFSS) survey were explored. BRFSS is a U.S. population-based interviewer-administered telephone survey that is conducted annually. Data are collected about health-related risk behaviors, chronic health conditions, and use of preventive services. Participants are selected via random-digit-dialed landline and cell phone numbers and include adults aged 18+ years who reside in the 50 states, District of Columbia (DC), and two U.S. territories (i.e., Guam, Puerto Rico). The 2017 BRFSS includes data that were collected from N = 450,016 survey respondents (Centers for Disease Control and Prevention, 2017).
Study Design & Participants
Herein, we explored a subsample of the N = 450,016 survey respondents who completed the 2017 BRFSS survey. The subsample for this investigation represented the 430 (0.10%) survey respondents who were heterosexual females aged 18-26 years (n = 260), lesbian females aged 18-26 years (n = 35), heterosexual males aged 18-21 years (n = 107), or gay or bisexual males aged 18-26 years (n = 28). These respondents were specifically selected since adult HPV vaccinations are recommended by the ACIP for (a) all females aged 18-26 years, (b) heterosexual males aged 18-21 years, and (c) gay or bisexual males aged 18-26 years (Petrosky et al., 2015).
Variables
HPV vaccination.
Two items were used to measure HPV vaccination. The first question asked whether the participant ever had an HPV vaccination. For participants who had been vaccinated, a follow-up question asked how many doses of the HPV vaccine the participant received. In order to prevent HPV infections and other HPV-related endpoints, including cancers, ACIP recommends that adults and special populations get three doses of the HPV vaccine for maximum effectiveness (Petrosky et al., 2015), although only two doses are recommended for average risk adolescents ages 9 through age 14 years (Meites, 2016). Therefore, we combined these two variables to create a dichotomous HPV vaccination variable with the following levels: unvaccinated (0 doses), initiated (1-2 doses) / completed (3 doses), which is consistent with one of the four ways that the National Immunization Survey measures HPV vaccine coverage (defined as receipt of at least 1 dose) among adolescents (Centers for Disease Control and Prevention, 2015). This HPV vaccination variable was our primary outcome variable of interest.
Binge drinking.
BRFSS used the National Institute on Alcohol Abuse and Alcoholism’s (NIAAA) 2004 gender-based definition of binge drinking (i.e., males having five or more drinks on one occasion, females having four or more drinks on one occasion). In the current study, this variable was used as both a continuous variable (i.e., number of days binge drank within the past 30 days) and to create a dichotomous variable (yes/no) establishing whether binge drinking occurred in the last month. We used the continuous variable to create a 4-level ordinal variable by recoding frequency of binge drinking as 0, 1, 2, or 3+ times.
HIV/HPV co-infection high-risk behaviors.
A single item was used to measure risk of acquiring or transmitting HIV infection. This question assessed whether (within the past year) the participant engaged in high-risk HIV infection behaviors, including injection drug use and/or high-risk sexual behaviors (i.e. having a sexually transmitted disease, exchanging sex for money/drugs, and unprotected anal sex). Participants did not have to specify which HIV infection high-risk behavior(s) they engaged in, just whether they had engaged in any of these behaviors within the past year.
HIV testing.
To reduce the spread of HIV, the CDC recommends routine HIV testing among adolescents, adults and pregnant women (Centers for Disease Control and Prevention, 2019). Two items were used to measure HIV testing. First, participants were asked if they had ever had an HIV test. Participants who had an HIV test were next asked the month and year of their last HIV test, which did not include any HIV testing that was done as part of a blood donation. We combined these two variables to create a new variable that distinguished HIV testing that was done in 2017, before 2017, or never.
Covariates.
A composite variable was created by combining sexual orientation, sex, and age to describe the sample based on ACIP’s HPV different vaccination eligibility guidelines for heterosexual versus gay or bisexual males. The following four categories were created: (1) heterosexual females aged 18-26 years, (2) lesbian females aged 18-26 years, (3) heterosexual males aged 18-21 years, and (4) gay or bisexual males aged 18-26 years. Other variables that were used to describe the sample characteristics were: gender identity (cisgender, transgender or gender nonconforming), race/ethnicity, marital status, education, occupation, health insurance, smoking status, BMI, and U.S. Census region or territory).
Data Analysis
Stata/SE 15.1 (College Station, Texas, USA) was used to calculate crude and adjusted odds ratios, which were obtained by performing simple and multivariable logistic regression analysis on the weighted BRFSS data. A SVYSET statement was used to account for the complex survey design of the BRFSS data, in which an iterative proportional fitting or raking sampling method is used to weight the data using age, sex, categories of ethnicity, geographic regions within states, marital status, education level, home ownership, and type of phone ownership based on the five-year American Community Survey PUMS data set (2012-2016) (Centers for Disease Control and Prevention, n.d; U.S. Census Bureau, 2019).
HPV vaccination (outcome) was modeled as initiated/completed versus unvaccinated (referent). Our logistic regression model used a 4-level ordinal measure of frequency of binge drinking (referent=0). Covariates were added to the models one-by-one using a forward stepwise process in which only variables that changed the odds ratio for our exposure variable (i.e., binge drinking) by more than 10% were kept in the model as a potential confounder of the relationship between binge drinking and HPV vaccination. Race/ethnicity, geographical location, and health insurance were forced into the model because these are known predictors of HPV vaccination. (Bastani et al., 2011; Pourat & Jones, 2012). The statistical significance of each covariate in the final models was determined based on the 95% confidence intervals not including a value of 1.0, and also a P value < 0.05.
RESULTS
Participants’ Demographics
Participants’ characteristics and HPV vaccination uptake are represented in Table 1. Respondents were mostly cisgender (99.8%), non-Hispanic White (41.4%), unmarried (74.7%), educated with at least a GED or some college degree (78.9%), insured (68.2%), nonsmoking (71.1%), had neither received the HPV vaccine (60.6%) nor been tested for HIV in their lifetime (59%). Participants described their sexual orientation as heterosexual females (61.1%), lesbians (7.9%), gay/bisexual males (4.8%) and heterosexual males (26.4%). Almost half of all respondents (44.8%) described having one or more self-reported episodes of binge drinking within the past 30 days; while an estimated 21.8% engaged in high-risk HIV behaviors such as injection drug use, exchange of sex for money/drugs, and unprotected anal sex. Overall, a greater proportion of participants were unvaccinated (61%) compared to those who had initiated (21%) or completed (18%) the HPV vaccine. Fewer than half of those unvaccinated were not binge drinkers (36.2%), did not engage in high-risk HIV behaviors (48.9%), had never been tested for HIV (42.1%), and were unmarried (46.3%).
Table 1:
Total sample (N=430) | Initiated (1-2 doses) N=90, 21% |
Completed (3 doses) N=79, 18% |
Unvaccinated (0 doses) N=261, 61% |
|||||
---|---|---|---|---|---|---|---|---|
Characteristics | n | (%) | n | (%) | n | (%) | n | (%) |
No. times binge drinking, past 30 days a | ||||||||
None | 237 | 55.2 | 39 | 9.0 | 43 | 9.9 | 155 | 36.2 |
1 | 86 | 20.2 | 30 | 7.0 | 21 | 4.8 | 36 | 8.4 |
2 | 46 | 10.8 | 13 | 2.9 | 7 | 1.6 | 28 | 6.4 |
3 or more times | 61 | 13.8 | 10 | 2.2 | 10 | 2.2 | 42 | 9.6 |
HIV/HPV co-infection risk behavior, past year b | ||||||||
High | 96 | 21.8 | 26 | 6.1 | 18 | 4.0 | 52 | 11.7 |
Low | 334 | 78.2 | 64 | 15.0 | 61 | 14.3 | 209 | 48.9 |
Year of most recent HIV test | ||||||||
2017 | 53 | 14.9 | 17 | 4.6 | 12 | 3.5 | 24 | 6.8 |
Before 2017 | 117 | 26.1 | 35 | 7.7 | 30 | 6.8 | 52 | 11.6 |
Never | 260 | 59.0 | 39 | 8.8 | 36 | 8.1 | 185 | 42.1 |
Sexual orientation, sex (age, years) c | ||||||||
Heterosexual, female (18-26) | 260 | 61.1 | 80 | 18.7 | 57 | 13.4 | 123 | 29.0 |
Lesbian, female (18-26) | 35 | 7.9 | 7 | 1.5 | 13 | 3.0 | 15 | 3.4 |
Heterosexual, male (18-21) | 107 | 26.4 | 2 | 0.5 | 7 | 1.6 | 98 | 24.3 |
Gay or bisexual, male (18-26) | 28 | 4.8 | 2 | 0.4 | 3 | 0.5 | 23 | 3.9 |
Gender identity | ||||||||
Cisgender | 428 | 99.8 | 90 | 21.1 | 79 | 18.3 | 259 | 60.4 |
Transgender or gender nonconforming | 2 | 0.2 | 0 | 0.0 | 0 | 0.0 | 2 | 0.2 |
Race/ethnicity | ||||||||
Non-Hispanic White | 220 | 41.4 | 57 | 10.7 | 33 | 6.3 | 130 | 24.4 |
Non-Hispanic Black/African American | 78 | 17.7 | 12 | 2.7 | 14 | 3.1 | 52 | 11.9 |
Non-Hispanic Other | 16 | 3.4 | 6 | 1.3 | 2 | 0.4 | 8 | 1.7 |
Non-Hispanic Multiple Races | 17 | 3.0 | 1 | 0.2 | 11 | 1.9 | 5 | 0.9 |
Hispanic | 99 | 34.5 | 16 | 6.3 | 20 | 6.6 | 63 | 21.6 |
Marital status | ||||||||
Married | 96 | 25.3 | 21 | 5.5 | 21 | 5.5 | 54 | 14.3 |
Unmarried | 334 | 74.7 | 69 | 15.5 | 59 | 12.9 | 206 | 46.3 |
Education | ||||||||
Less than grade 12 | 26 | 6.1 | 2 | 0.5 | 4 | 0.9 | 20 | 4.7 |
Grade 12 or GED | 140 | 32.5 | 14 | 3.3 | 29 | 6.7 | 97 | 22.5 |
Some college | 198 | 46.4 | 33 | 7.8 | 38 | 9.0 | 127 | 29.7 |
College or higher | 66 | 15.0 | 41 | 9.4 | 8 | 1.8 | 17 | 3.8 |
Occupation | ||||||||
Student | 151 | 35.4 | 36 | 8.5 | 27 | 6.5 | 88 | 20.5 |
Non-student | 279 | 64.6 | 55 | 12.6 | 51 | 11.8 | 173 | 40.1 |
Smoking status | ||||||||
Current smoker | 78 | 21.4 | 17 | 4.4 | 17 | 4.8 | 44 | 12.11 |
Former smoker | 29 | 7.5 | 2 | 0.5 | 4 | 1.0 | 23 | 6.0 |
Non-smoker | 323 | 71.1 | 73 | 16.1 | 57 | 12.5 | 193 | 42.4 |
BMI | ||||||||
Underweight | 16 | 3.9 | 2 | 0.6 | 10 | 2.3 | 4 | 1.0 |
Normal | 226 | 53.9 | 56 | 13.4 | 25 | 5.9 | 145 | 34.7 |
Overweight | 90 | 19.8 | 20 | 4.4 | 17 | 3.7 | 53 | 11.8 |
Obese | 98 | 22.4 | 12 | 2.7 | 28 | 6.5 | 58 | 13.2 |
Health insurance | ||||||||
Insured | 344 | 68.2 | 85 | 17.0 | 67 | 13.2 | 192 | 38.0 |
Uninsured | 86 | 31.8 | 11 | 4.0 | 14 | 5.2 | 61 | 22.6 |
Unweighted;
weighted;
adjusted model included sexual orientation/sex, race/ethnicity, and education
Males ≥ 5, females ≥ 4;
used injection drugs, treated for a sexually transmitted infection, exchanged sex for money or drugs, had unprotected anal sex, and/or had four or more sex partners in the past year;
based on 2017 HPV vaccination guidelines;
Abbreviations: OR (odds ratio); aOR (adjusted odds ratio); CI (confidence interval).
Data Source: 2017 Behavioral Risk Factor Surveillance System
Predictors of HPV Vaccination Uptake
Table 2 depicts crude odds ratio (OR), adjusted odds ratio (aOR) and predictors for HPV vaccine uptake among participants. After adjusting for age, sex, race/ethnicity, education etc., individuals who identified as Non-Hispanic Multiple race, were significantly more likely to initiate and/or complete HPV vaccination doses than other races/ethnicities (aOR=5.18;95%CI: 1.13-23.65). Concurrently, acquiring “college or higher” education among respondents, was associated with a greater likelihood of HPV vaccine uptake (aOR=3.96;95%CI: 1.57-9.96). On the contrary, heterosexual males (aOR=0.14;95%CI:0.05-0.62) and gay/bisexual males (aOR=0.18;95%CI:0.05-0.62) were less likely to have received the HPV vaccine. Participants’ marital status was not found to be significantly associated with HPV vaccination uptake.
Table 2:
Characteristics | OR (95% CI) | aOR (95% CI) * |
---|---|---|
No. times binge drinking, past 30 days a | ||
None | Ref | Ref |
1 | 2.70 (1.15-6.36) | 2.71 (1.11-6.65) |
2 | 1.32 (0.50-3.51) | 3.05 (1.26-7.41) |
3 or more times | 0.84 (0.36-1.97) | 0.80 (0.25-2.59) |
HIV/HPV co-infection risk behavior, past year b | ||
High | 1.43 (0.67-3.04) | --- |
Low | Ref | --- |
Year of most recent HIV test | ||
2017 | 2.94 (1.11-7.78) | 3.86 (1.42-10.55) |
Before 2017 | 3.12 (1.54-6.30) | 2.62 (1.23-5.56) |
Never | Ref | Ref |
Sexual orientation, sex (age, years)c | ||
Heterosexual, female (18-26) | Ref | Ref |
Lesbian, female (18-26) | 1.21 (0.41-3.63) | 1.39 (0.40-4.84) |
Heterosexual, male (18-21) | 0.08 (0.03-0.17) | 0.14 (0.05-0.35) |
Gay or bisexual, male (18-26) | 0.19 (0.06-0.63) | 0.18 (0.05-0.62) |
Race/ethnicity | ||
Non-Hispanic White | Ref | Ref |
Non-Hispanic Black/African American | 0.70 (0.32-1.50) | 0.79 (0.32-1.97) |
Non-Hispanic Other | 1.47 (0.03-7.15) | 2.31 (0.51-10.57) |
Non-Hispanic Multiple Races | 3.42 (0.63-18.56) | 5.18 (1.13-23.65) |
Hispanic | 0.86 (0.40-1.83) | 1.04 (0.45-2.39) |
Marital status | ||
Married | 1.26 (0.58-2.74) | --- |
Unmarried | Ref | --- |
Education | ||
Less than grade 12 | 0.54 (0.16-1.82) | 0.63 (0.17-2.34) |
Grade 12 or GED | 0.79 (0.36-1.76) | 0.74 (0.33-1.65) |
College or higher | 5.15 (2.36-11.25) | 3.96 (1.57-9.96) |
Some college | Ref | Ref |
Occupation | ||
Student | 1.2 (0.63-2.27) | --- |
Non-student | Ref | --- |
Smoking status | ||
Current smoker | 1.13 (0.47-2.69) | 1.51 (0.58-3.91) |
Former smoker | 0.37 (0.12-1.12) | 1.13 (0.32-4.07) |
Non-smoker | Ref | Ref |
BMI | ||
Normal | Ref | Ref |
Underweight | 5.50 (0.99-30.45) | 7.86 (0.92-67.40) |
Overweight | 1.24 (0.57-2.72) | 1.49 (0.66-3.36) |
Obese | 1.25 (0.58-2.73) | 0.90 (0.39-2.08) |
Health insurance | ||
Insured | Ref | Ref |
Uninsured | 0.51 (0.23-1.15) | 0.78 (0.34-1.78) |
Model adjusted for sexual orientation/sex, race/ethnicity, and education.
Males ≥ 5, females ≥ 4;
used injection drugs, treated for a sexually transmitted infection, exchanged sex for money or drugs, had unprotected anal sex, and/or had four or more sex partners in the past year;
based on 2017 HPV vaccination guidelines;
Abbreviations: OR (odds ratio); aOR (adjusted odds ratio); CI (confidence interval).
Data Source: 2017 Behavioral Risk Factor Surveillance System
In this study, participants’ HIV testing in 2017 (aOR=3.86;95%CI:1.42-10.55); before 2017 (aOR=2.62;95%CI:1.23-5.56); binge drinking i.e. 1 episode (aOR=2.71;95%CI:1.11-6.65) and 2 episodes (aOR=3.05;95%CI:1.26-7.41) within 30 days of self-report, were strong predictors for HPV vaccination uptake. HIV risky behavior was not found to be strongly linked with receiving at least one dose of the HPV vaccine. While binge drinking (44.8%) more than doubled the likelihood of participating in HIV risk behaviors (OR=2.1;95%CI:l.0-4.5), it was not found to be predictive participants’ self-report of HIV testing (OR=0.98;95%CI:0.63-1.53).
DISCUSSION
This large-scale population-based study examined HPV vaccine uptake among a subsample of 430 respondents aged 18-26 years residing in 50 states, DC, and two US territories (i.e., Guam, Puerto Rico). Overall, approximately two out of every three respondents had not received the HPV vaccine. In addition, males (both heterosexual and gay) were least likely to be vaccinated. Binge drinking was found to be significantly associated with HIV risk behaviors; while respondents reporting 1 and 2 episodes in the past 30-days were more likely to have initiated or received the HPV vaccine, compared to those engaging in 3 or more episodes of binge drinking.
Despite ACIP’s recommendations for routine use of the quadrivalent HPV vaccine for boys ages 13 to 21 and girls 11 to 26 years old, HPV vaccine uptake remains sub-optimal. For instance, a minority of our sample (39%) reported coverage of at least one dose of HPV vaccine. Parents’ concerns on vaccine safety, belief that adolescents could engage in risky sexual behaviors, financial cost and multiple doctor’s visits are some of the reasons responsible for poor vaccine uptake (Holman et al., 2014; Quinn, Vadaparampil, Johns, Alexander, & Giuliano, 2014). Given the high-risk sexual health behaviors reported among individuals aged 15-24 years (Markowitz et al., 2014; Shannon & Klausner, 2018), the college/university represents the ideal setting to promote catch-up vaccinations among a significant proportion of young individuals who have neither completed nor initiated the 3-dose HPV immunization schedule. In addition to relatively low HPV vaccinations rates, almost two-thirds (59%) of study participants stated they had never been tested for HIV in their lifetime. Despite rigorous campaign efforts to mitigate spread of HIV in the U.S., more than a quarter (30%) of new infections are transmitted by individuals oblivious to their HIV infectious state (Skarbinski et al., 2015). Infected individuals who have undergone medical testing to determine their disease state demonstrate lower transmission risk behaviors compared to those with an unknown disease state (Hall, Holtgrave, & Maulsby, 2012). Moreover, higher prevalence of HIV/AIDS diagnosis has been reported among young adults (Rangel, Gavin, Reed, Fowler, & Lee, 2006). Thus, further exploration is warranted on why individuals choose to refrain from getting tested for HIV.
Effective intervention approaches, which incorporate immunization, screening, early diagnosis and effective treatment, are crucial to control and prevent the transmission of HIV and/or HPV infections (Wallace, McLellan-Lemal, Harris, Townsend, & Miller, 2011). Novel strategies, which improve catch-up vaccination rates and increase HIV testing among college students, should be implemented. For instance, schools with mandatory insurance coverage could roll out campaigns outlining access, affordability, and efficacy of vaccinations and screenings to increase adoption rates. Colleges/universities could also promote effective messaging strategies that utilize videos, leaflets, and monthly reminders (Richman, Maddy, Torres, & Goldberg, 2016), as well as, provide disease information and resources on students’ health websites (Fontenot, Fantasia, Sutherland, & Lee-St John, 2016).
In this population-based study, heterosexual and gay/bisexual males were less likely to have received the HPV vaccine. This finding is consistent with previous studies which cite low HPV coverage among young men (Reagan-Steiner, 2016). This is disconcerting given that heterosexual (15%) and gay (60%) males, as well as, gay men living with HIV (95%), disproportionately suffer from anogenital HPV infections (Newman, Logie, Doukas, & Asakura, 2013). Concurrently, average lifetime probability of acquiring the HPV infection with at least one sexual partner of the opposite sex in men exceeds that of their female counterparts (Chesson, Dunne, Hariri, & Markowitz, 2014). The prophylactic administration of the HPV vaccine among men is proven to be effective, safe and able to significantly minimize disease burdens occurring from HPV infections (i.e. anogenital warts), as well as, persistent infections and HPV-associated cancers (i.e. oropharyngeal, anal and penile cancers). Conversely, the vaccine is able to control spread of HPV infection from affected men to their respective sexual partners through herd immunity (Centers for Disease Control and Prevention, 2011; Giuliano et al., 2011). Therefore, the implementation of targeted health promotion campaigns may be warranted. Lessons learned from social marketing campaigns designed to increased HIV and STI testing among high-risk groups, such as men who have sex with men, may be influential in the development and evaluation of these future programs (Guy et al., 2009; Wei et al., 2011; Wilkinson et al., 2016).
Similar to previous investigations (Wen et al., 2012), respondents engaging in binge drinking in the past 30-days were more likely to participate in HIV risk behaviors (i.e. injection drugs use, exchange of sex for money/drugs, and unprotected anal sex). Along with increased HIV risk behaviors, binge drinkers have been found to have elevated blood pressure and cholesterol values (Abramson, Lewis, & Murrah, 2010; Piano, Burke, Kang, & Phillips, 2018; Wellman et al., 2016); increased risk of suicide and self-inflicted harm (Brewer & Swahn, 2005); permanent disabilities and deaths occurring from drunk driving, violence, homicide and other forms of trauma (Courtney & Polich, 2009; Dawson, Li, & Grant, 2008); as well as, reduced cognitive processing and impulse control (Kuntsche, Kuntsche, Thrul, & Gmel, 2017). Among our sample, binge drinkers i.e. having 1 and 2 episodes were more likely to have initiated and/or received the HPV vaccine. Though seemingly counterintuitive, the co-occurrence of HPV vaccine uptake and HIV risky behaviors among binge drinkers has been previously documented in scientific literature (Bednarczyk, Birkhead, Morse, Doleyres, & McNutt, 2011). Additional, more explanatory, research should seek to further explore and unpack this association.
There were a number of limitations in this study that should be considered in unison with our results. Given the secondary nature of our data, these limitations are inherited from the BRFSS survey. Specifically, measurement variables for this study were self-reported. Collecting information on intimate and sensitive topics, such as HIV risk behaviors may be subject to recall bias, response bias, and social desirability bias. Secondly, sample sizes for some sub-categories (i.e., “underweight”) were found to be relatively small and as depicted by wide confidence intervals. Despite this limitation, this study provided strong evidence for other important variables. Additionally, HIV risk behavior was assessed using a single general item, which ultimately may not capture the entire scope of these behaviors. Similarly, the BRFSS does not obtain information on participants’ HIV status, or their intent to initiate or complete the 3-dose HPV vaccination schedule. Nevertheless, this large-scale nationally representative study has provided valid, reliable estimates on HPV, HIV and binge drinking prevalence among young adults aged 18-26 years in the U.S. This study also highlighted key implications for promoting HPV vaccination and HIV testing particularly among at-risk young adult binge drinkers.
HIGHLIGHTS.
Approximately, two-thirds of respondents had neither been tested for HIV (59%) nor received the HPV vaccine (60.6%).
Heterosexual (aOR=0.14;95%CI:0.05-0.62) and gay/bisexual males (aOR=0.18;95%CI:0.05-0.62) less likely to receive vaccine.
Binge drinkers were more likely to engage in HIV/HPV co-infection high-risk behaviors (OR=2.1;95%CI:1.0-4.5).
Participant’s HIV testing was a strong predictor for HPV vaccination uptake.
Acknowledgments
FUNDING:
Research reported in this publication was supported by the National Cancer Institute of the National Institutes of Health under award number K01CA175239.
The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Cancer Institute, National Institutes of Health, Department of Health and Human Services, or the United States Government.
Footnotes
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CONFLICT OF INTEREST DISCLOSURE:
The authors declare that there are no conflicts of interests
REFERENCES
- Abramson JL, Lewis C, & Murrah NV (2010). Relationship of self-reported alcohol consumption to ambulatory blood pressure in a sample of healthy adults. American Journal of Hypertension, 23(9), 994–999. [DOI] [PubMed] [Google Scholar]
- Bass SB, Leader A, Shwarz M, Greener J, & Patterson F (2015). Correlates to human papillomavirus vaccination status and willingness to vaccinate in Low-Income Philadelphia high school students. Journal of School Health, 85(8), 527–535. [DOI] [PubMed] [Google Scholar]
- Bastani R, Glenn BA, Tsui J, Chang LC, Marchand EJ, Taylor VM, & Singhal R (2011). Understanding suboptimal human papillomavirus vaccine uptake among ethnic minority girls. Cancer Epidemiology and Prevention Biomarkers, 20(7), 1463–1472. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bednarczyk RA, Birkhead GS, Morse DL, Doleyres H, & McNutt L (2011). Human papillomavirus vaccine uptake and barriers: Association with perceived risk, actual risk and race/ethnicity among female students at a new york state university, 2010. Vaccine, 29(17), 3138–3143. [DOI] [PubMed] [Google Scholar]
- Bosch FX, Lorincz A, Muñoz N, Meijer C, & Shah KV (2002). The causal relation between human papillomavirus and cervical cancer. Journal of Clinical Pathology, 55(4), 244–265. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brewer RD, & Swahn ΜH (2005). Binge drinking and violence. Jama, 294(5), 616–618. [DOI] [PubMed] [Google Scholar]
- Center for Disease Control and Prevention. (2013). Incidence, prevalence, and cost of sexually transmitted infections in the united states - CDC fact sheet. Retrieved from https://www.cdc.gov/std/stats/STI-Estimates-Fact-Sheet-Feb-2013.pdf
- Centers for Disease Control and Prevention. (2011). Recommendations on the use of quadrivalent human papillomavirus vaccine in males--advisory committee on immunization practices (ACIP), 2011. MMWR.Morbidity and Mortality Weekly Report, 60(50), 1705. [PubMed] [Google Scholar]
- Centers for Disease Control and Prevention. (2015). NIS-teen data - adolescents/teens (13-17 years): (adolescents/teens) NIS-teen data (timeframe for household interviews). Retrieved from https://www.cdc.gov/vaccines/imz-managers/coverage/nis/teen/index.html
- Centers for Disease Control and Prevention. (2017). 2017 behavioral risk factor surveillance system: Questionnaire, survey data and documentation. Retrieved from https://www.cdc.gov/brfss/index.html
- Centers for Disease Control and Prevention. (2019). HIV testing. Retrieved from https://www.cdc.gov/hiv/testing/index.html
- Centers for Disease Control and Prevention. (n.d). Weighting the BRFSS data. Retrieved from https://www.cdc.gov/brfss/annual_data/2017/pdf/weighting-2017-508.pdf
- Chen X, Sun K, & Jiang W (2016). Absence of high-risk HPV 16 and 18 in chinese patients with oral squamous cell carcinoma and oral potentially malignant disorders. Virology Journal, 13(1), 81. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chersich MF, Luchters S, Malonza IM, Mwarogo P, King’Ola N, & Temmerman M (2007). Heavy episodic drinking among kenyan female sex workers is associated with unsafe sex, sexual violence and sexually transmitted infections. International Journal of STD & AIDS, 18(11), 764–769. [DOI] [PubMed] [Google Scholar]
- Chersich MF, Bosire W, King’ola N, Temmerman M, & Luchters S (2014). Effects of hazardous and harmful alcohol use on HIV incidence and sexual behaviour: A cohort study of kenyan female sex workers. Globalization and Health, 10(1), 22. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chesson HW, Dunne EF, Hariri S, & Markowitz LE (2014). The estimated lifetime probability of acquiring human papillomavirus in the united states. Sexually Transmitted Diseases, 41(11), 660–664. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chiao C, Morisky DE, Rosenberg R, Ksobiech K, & Malow R (2006). The relationship between HIV Sexually transmitted infection risk and alcohol use during commercial sex episodes: Results from the study of female commercial sex workers in the Philippines. Substance use & Misuse, 41(10-12), 1509–1533. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cook RT (1998). Alcohol abuse, alcoholism, and damage to the immune system—a review. Alcoholism: Clinical and Experimental Research, 22(9), 1927–1942. [PubMed] [Google Scholar]
- Cooperman NA, Arnsten JH, & Klein RS (2007). Current sexual activity and risky sexual behavior in older men with or at risk for HIV infection. AIDS Education & Prevention, 19(4), 321–333. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Courtney KE, & Polich J (2009). Binge drinking in young adults: Data, definitions, and determinants. Psychological Bulletin, 135(1), 142. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dawson DA, Li T, & Grant BF (2008). A prospective study of risk drinking: At risk for what? Drug and Alcohol Dependence, 95(1-2), 62–72. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Sousa Isaura Danielli Borges, Vidal FCB, Vidal João Paulo Castello Branco, de Mello George Castro Figueira, Nascimento Maria do Desterro Soares Brandão, & Brito LMO (2015). Prevalence of human papillomavirus in penile malignant tumors: Viral genotyping and clinical aspects. BMC Urology, 15(1), 13. [DOI] [PMC free article] [PubMed] [Google Scholar]
- De Vuyst H, Clifford GM, Nascimento MC, Madeleine ΜM, & Franceschi S (2009). Prevalence and type distribution of human papillomavirus in carcinoma and intraepithelial neoplasia of the vulva, vagina and anus: A meta-analysis. International Journal of Cancer, 124(7), 1626–1636. [DOI] [PubMed] [Google Scholar]
- Fontenot HB, Fantasia HC, Sutherland MA, & Lee-St John T (2016). HPV and HPV vaccine information among a national sample of college and university websites. Journal of the American Association of Nurse Practitioners, 28(4), 218–223. [DOI] [PubMed] [Google Scholar]
- Gargano JW, Unger ER, Liu G, Steinau M, Meites E, Dunne E, & Markowitz LE (2017). Prevalence of genital human papillomavirus in males, united states, 2013–2014. The Journal of Infectious Diseases, 215(7), 1070–1079. [DOI] [PubMed] [Google Scholar]
- Gillison ML, Koch WM, Capone RB, Spafford M, Westra WH, Wu L, … Symer DE (2000). Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. Journal of the National Cancer Institute, 92(9), 709–720. [DOI] [PubMed] [Google Scholar]
- Giuliano AR, Palefsky JM, Goldstone S, Moreira ED Jr, Penny ΜE, Aranda C, … Hillman R (2011). Efficacy of quadrivalent HPV vaccine against HPV infection and disease in males. New England Journal of Medicine, 364(5), 401–411. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Guy R, Goller J, Leslie D, Thorpe R, Grierson J, Batrouney C, … Ginige S (2009). No increase in HIV or sexually transmissible infection testing following a social marketing campaign among men who have sex with men. Journal of Epidemiology & Community Health, 63(5), 391–396. [DOI] [PubMed] [Google Scholar]
- Hall HI, Holtgrave DR, & Maulsby C (2012). HIV transmission rates from persons living with HIV who are aware and unaware of their infection. Aids, 26(7), 893–896. [DOI] [PubMed] [Google Scholar]
- Hellen-Bandeira-de-Pontes Santos T, dos Santos K, Paz A, Cavalcanti Y, Cassiano-Francisco-Weege Nonaka G, & Godoy PA (2016). Clinical findings and risk factors to oral squamous cell carcinoma in young patients: A 12-year retrospective analysis. Medicina Oral, Patologia Oral Y Cirngia Bncal, 21(2), e151. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ho GY, Bierman R, Beardsley L, Chang CJ, & Burk RD (1998). Natural history of cervicovaginal papillomavirus infection in young women. New England Journal of Medicine, 338(7), 423–428. [DOI] [PubMed] [Google Scholar]
- Holman DM, Benard V, Roland KB, Watson M, Liddon N, & Stokley S (2014). Barriers to human papillomavirus vaccination among US adolescents: A systematic review of the literature. JAMA Pediatrics, 168(1), 76–82. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jemal A, Simard EP, Dorell C, Noone A, Markowitz LE, Kohler B, … Saslow D (2013). Annual report to the nation on the status of cancer, 1975–2009, featuring the burden and trends in human papillomavirus (HPV)-associated cancers and HPV vaccination coverage levels. JNCI: Journal of the National Cancer Institute, 105(3), 175–201. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jenness SM, Kobrak P, Wendel T, Neaigus A, Murrill CS, & Hagan H (2011). Patterns of exchange sex and HIV infection in high-risk heterosexual men and women. Journal of Urban Health, 88(2), 329–341. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kuntsche E, Kuntsche S, Thrul J, & Gmel G (2017). Binge drinking: Health impact, prevalence, correlates and interventions. Psychology & Health, 32(8), 976–1017. [DOI] [PubMed] [Google Scholar]
- Markowitz LE, Dunne EF, Saraiya M, Chesson HW, Curtis CR, Gee J, … Linger ER (2014). Human papillomavirus vaccination: Recommendations of the advisory committee on immunization practices (ACIP). Morbidity and Mortality Weekly Report: Recommendations and Reports, 63(5), 1–30. [PubMed] [Google Scholar]
- Meites E (2016). Use of a 2-dose schedule for human papillomavirus vaccination—updated recommendations of the advisory committee on immunization practices. MMWR.Morbidity and Mortality Weekly Report, 65 [DOI] [PubMed] [Google Scholar]
- Molina PE, Happel KI, Zhang P, Rolls JK, & Nelson S (2010). Focus on: Alcohol and the immune system. Alcohol Research & Health, 33(1-2), 97. [PMC free article] [PubMed] [Google Scholar]
- Newman PA, Logie CH, Doukas N, & Asakura K (2013). HPV vaccine acceptability among men: A systematic review and meta-analysis. Sex Transm Infect, 89(7), 568–574. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nielsen A, Munk C, Jorgensen HO, Winther JF, Van Den Brule A, & Kjaer SK (2013). Multiple-type human papillomavirus infection in younger uncircumcised men. International Journal of STD & AIDS, 24(2), 128–133. [DOI] [PubMed] [Google Scholar]
- Oh HY, Kim MK, Seo S, Lee DO, Chung YK, Lim MC, … Park S (2015). Alcohol consumption and persistent infection of high-risk human papillomavirus. Epidemiology & Infection, 143(7), 1442–1450. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Petrosky E, Bocchini JA Jr, Hariri S, Chesson H, Curtis CR, Saraiya M, … Markowitz LE (2015). Use of 9-valent human papillomavirus (HPV) vaccine: Updated HPV vaccination recommendations of the advisory committee on immunization practices. MMWR.Morbidity and Mortality Weekly Report, 64(11), 300. [PMC free article] [PubMed] [Google Scholar]
- Piano MR, Burke L, Kang M, & Phillips SA (2018). Effects of repeated binge drinking on blood pressure levels and other cardiovascular health metrics in young adults: National health and nutrition examination survey, 2011-2014. Journal of the American Heart Association, 7(13), e008733. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pourat N, & Jones JM (2012). Role of insurance, income, and affordability in human papillomavirus vaccination. The American Journal of Managed Care, 18(6), 320–330. [PubMed] [Google Scholar]
- Quinn GP, Vadaparampil ST, Johns T, Alexander KA, & Giuliano AR (2014). Adolescent sexual activity and cancer risk: Physicians’ duty to inform? Current Medical Research and Opinion, 30(9), 1827–1831. [DOI] [PubMed] [Google Scholar]
- Ramirez-Valles J, Garcia D, Campbell RT, Diaz RM, & Heckathorn DD (2008). HIV infection, sexual risk behavior, and substance use among latino gay and bisexual men and transgender persons. American Journal of Public Health, 98(6), 1036–1042. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rangel MC, Gavin L, Reed C, Fowler MG, & Lee LM (2006). Epidemiology of HIV and AIDS among adolescents and young adults in the united states. Journal of Adolescent Health, 39(2), 156–163. [DOI] [PubMed] [Google Scholar]
- Reagan-Steiner S (2016). National, regional, state, and selected local area vaccination coverage among adolescents aged 13–17 years—United states, 2015. MMWR.Morbidity and Mortality Weekly Report, 65 [DOI] [PubMed] [Google Scholar]
- Richman AR, Maddy L, Torres E, & Goldberg EJ (2016). A randomized intervention study to evaluate whether electronic messaging can increase human papillomavirus vaccine completion and knowledge among college students. Journal of American College Health, 64(4), 269–278. [DOI] [PubMed] [Google Scholar]
- Satterwhite CL, Torrone E, Meites E, Dunne EF, Mahajan R, Ocfemia MCB, … Weinstock H (2013). Sexually transmitted infections among US women and men: Prevalence and incidence estimates, 2008. Sexually Transmitted Diseases, 40(3), 187–193. [DOI] [PubMed] [Google Scholar]
- Schabath MB, Thompson ZJ, Egan KM, Torres BN, Nguyen A, Papenfuss MR, … Giuliano AR (2015). Alcohol consumption and prevalence of human papillomavirus (HPV) infection among US men in the HPV in men (HIM) study. Sex Transm Infect, 91(1), 61–67. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shannon CL, & Klausner JD (2018). The growing epidemic of sexually transmitted infections in adolescents: A neglected population. Current Opinion in Pediatrics, 30(1), 137–143. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Skarbinski J, Rosenberg E, Paz-Bailey G, Hall HI, Rose CE, Viall AH, … Mermin JH (2015). Human immunodeficiency virus transmission at each step of the care continuum in the united states. JAMA Internal Medicine, 175(4), 588–596. [DOI] [PubMed] [Google Scholar]
- Szabo G (1997). Alcohol’s contribution to compromised immunity. Alcohol Health and Research World, 21, 30–41. [PMC free article] [PubMed] [Google Scholar]
- U.S. Census Bureau. (2019). 2012-2016 american community survey (ACS): PUMS data. Retrieved from https://www.census.gov/programs-surveys/acs/data/pums.html
- Wallace SA, McLellan-Lemal E, Harris MJ, Townsend TG, & Miller KS (2011). Why take an HIV test? concerns, benefits, and strategies to promote HIV testing among low-income heterosexual african american young adults. Health Education & Behavior, 38(5), 462–470. [DOI] [PubMed] [Google Scholar]
- Wei C, Herrick A, Raymond HF, Anglemyer A, Gerbase A, & Noar SM (2011). Social marketing interventions to increase HIV/STI testing uptake among men who have sex with men and male-to-female transgender women. Cochrane Database of Systematic Reviews, (9) [DOI] [PubMed] [Google Scholar]
- Wellman RJ, Vaughn JA, Sylvestre M, O’Loughlin EK, Dugas EN, & O’Loughlin JL (2016). Relationships between current and past binge drinking and systolic blood pressure in young adults. Journal of Adolescent Health, 58(3), 352–357. [DOI] [PubMed] [Google Scholar]
- Wen X, Balluz L, & Town M (2012). Prevalence of HIV risk behaviors between binge drinkers and non-binge drinkers aged 18-to 64-years in US, 2008. Journal of Community Health, 37(1), 72–79. [DOI] [PubMed] [Google Scholar]
- Wilkinson AL, Pedrana AE, El-Hayek C, Vella AM, Asselin J, Batrouney C, … Stoove M (2016). The impact of a social marketing campaign on HIV and sexually transmissible infection testing among men who have sex with men in australia. Sexually Transmitted Diseases, 43(1), 49–56. [DOI] [PubMed] [Google Scholar]
- World Health Organization. (2019). Human papillomavirus (HPV) and cervical cancer. Retrieved from https://www.who.int/news-room/fact-sheets/detail/human-papillomavirus-(hpv)-and-cervical-cancer