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Research Paper

Knowledge and awareness of Human Papillomavirus (HPV) and HPV vaccines among Caribbean youth: the case of the Bahamas

ORCID Icon, ORCID Icon, , ORCID Icon & ORCID Icon
Pages 573-580 | Received 23 Apr 2019, Accepted 18 Aug 2019, Published online: 23 Sep 2019

ABSTRACT

There is a high burden of cervical cancer in the Caribbean region, particularly in the Bahamas, yet there are few studies of Human Papillomavirus (HPV) and HPV vaccine in the region. The objective of this study was to assess the knowledge and awareness of HPV and the HPV vaccine among school-aged youth (15–18 years) living in the Bahamas.

Cross-sectional data were obtained from the “Getting to Zero” HIV study in the Bahamas conducted in 2014/2015 (n = 1553). The questionnaire elicited information on knowledge of HPV and HPV vaccines, using previously validated scales. Data analysis included Chi-square tests and Mann Whitney U test.

In this sample of school-aged youth, only 10.7% (146/1364) had ever heard of HPV. With respect to those who were sexually active (n = 685), only 10.7% had ever heard of HPV. For those who had heard of HPV, knowledge of HPV and HPV vaccines was assessed on an HPV Knowledge and HPV Vaccine Knowledge scale, respectively. There was no statistically significant difference in mean HPV knowledge score between males and females, or HPV vaccine knowledge scores, between males and females.

There was a general lack of awareness of HPV and HPV vaccines among school-aged youth in the Bahamas. This is an important gap in the HPV vaccine strategy and cancer prevention, as this is the age at which most people acquire HPV. It emphasizes the importance of developing a careful implementation plan, with an evaluation of knowledge and attitudes, in order to have an effective HPV vaccine uptake.

1. Introduction

Human Papillomaviruses (HPV) cause genital, anal, and oropharyngeal cancers in men and women. In the United States, HPV is responsible for approximately 91% of cervical cancers in women and 90% of anal cancers in men and women.Citation1 In the Caribbean region, cervical cancer accounts for 18% of deaths among women.Citation2 There is a paucity of research on the burden and the distribution of anal cancers in men and women in the Caribbean region, including the Bahamas. Studies in US populations have demonstrated a higher incidence of anal cancer among Black men compared to White and Hispanic men,Citation3,Citation4 particularly among those living with HIV.Citation5,Citation6

Most HPV-associated cancers are preventable as there are safe and effective vaccines available.Citation7 HPV acquisition is common among sexually active individuals,Citation1 and in 2011–2014 its prevalence in the USA was estimated at 42% (45% men, 39.9% women) in the general population but 64.1% (65% men; 63% women) among non-Hispanic Blacks.Citation8 HPV infection is highest among sexually active youth but many will spontaneously clear the infection.Citation9 However, about one in ten will develop genital warts.Citation10 Among women,1.5% of HPV infection will persist and they may develop cervical intraepithelial neoplasia CIN2/3 and invasive cancer.Citation11

In the Bahamas in 2018, the estimated number of new cervical cancer cases diagnosed annually was 29, with an age-standardized incidence (ASI) of 10.9 per 100,000, compared to an ASI of 13.1 per 100,000 for the rest of the world.Citation12 Cervical cancer is the second most common female cancer in the Bahamas among those 15 to 44 years of age.Citation12 Youth in the Bahamas, as in many other areas of the world, become sexually active at an early age. Early sexual debut is a risk factor for cervical cancer,Citation13 perhaps due to longer and/or persistent HPV infection.Citation14 High numbers of sexual partners are known to increase the risk of exposure to HPV and the risk of genital and oropharyngeal cancers.Citation15 Sexually active youth often practice oral sex and while there is no clear evidence independently linking oral sex to oropharyngeal cancers,Citation16 there is evidence that HPV can be transmitted through oral sex.Citation17

Since 2011, HPV vaccine programs for young men and women have become widespread in many countries including some countries in the Caribbean region. However, there are still countries in that region that have not yet implemented HPV vaccine programs.Citation18 The Bahamas introduced its HPV vaccine program in 2015 for 9−12-year-old females and males.Citation19 Since then, the program has been extended to all women under 26 years of age, upon request. A study conducted between 2008 and 2010 among adults in the Bahamas revealed that only 46% of participants had heard of HPV and 35% had heard of the HPV vaccine.Citation20

The current study was conducted in 2014–15, prior to the introduction of an HPV vaccine into the national schedule of the immunization program in the Bahamas.Citation19 At the time of this study, Cervarix and Gardasil had become available in private physicians’ offices for a fee and there were widespread discussions in the media about the future government-funded program.Citation19 This study assesses youth’s understanding of HPV and HPV vaccine at a time when the HPV vaccine strategy was being rolled out – an important factor in HPV vaccine uptake.Citation21 More importantly, for countries that have not yet implemented their HPV Vaccine strategy, this study provides important lessons on the importance of assessing HPV and HPV vaccine knowledge prior to program implementation. It also provides important information for improving HPV vaccine uptake in other jurisdictions, including the US and Canada, where programs are not meeting their targets.Citation22,Citation23

2. Methods

This study is based on a sub-analysis of a larger study on male circumcision, HIV prevention and sexual health among Bahamians. The main study employed a stratified sampling of Bahamian high school students based on school distribution within the Bahamas. This was achieved through the support of the government’s Statistical Division and the Ministries of Health and Education. Ethical approval for the study was obtained from the Bahamas National Research Ethics Board and the Research Ethics Board of the University of Ontario Institute of Technology.

2.1. Recruitment and study administration

The established rapport between the Ministry of Health (MOH), the Bahamas National AIDS Program (NAP) and the Ministry of Education (MOE) was used to facilitate student recruitment through The Focus on Youth Program.Citation24 This program involves working with parents and their children to improve sexual health communication and has a well-established presence throughout the Bahamas.

The Bahamas consists of many islands with 90% of the population and its immigrant diversity residing on the islands of New Providence, Grand Bahama, and Abaco. The sample size was calculated by the Department of Statistics for the main research outcome for male circumcision. Based on the student population in the country, a sample size of 910 was calculated for gathering data for the subset of those 15–17 years of age.

Government public senior high schools were approached in New Providence (n = 7), Abaco (n = 3) and Grand Bahama (n = 2) and all participated. Students were recruited through standard procedures established by the MOE. Following obtaining the Ministry’s permission, each school principal was approached to obtain agreement for recruiting a specific class. Students consent was then obtained before administering the printed questionnaire under exam-like conditions. The original study was not designed for young women but was later modified to include them as was desired by stakeholders. As such, recruitment occurred in more classes than was previously planned to ensure female participation. Students were informed that they could refuse to answer any or all of the questions. An honorarium of a $5 phone card was offered.

2.1.1. Study instrument

The questionnaire elicited information on students’ socio-demographic status including age and sex, sexual behavior and HIV knowledge. As religiosity is an important aspect of Bahamian life, we asked about religious affiliation and frequency of religious service attendance. For this paper, our main instrument included a battery of questions to determine general HPV knowledge and HPV vaccine knowledge.Citation25

The general HPV Knowledge Scale, a 16-item questionnaire and the HPV Vaccine Knowledge Scale, a 7-item questionnaire, developed by Waller et al.,Citation25 were used to measure HPV and HPV vaccine knowledge. Participants were first asked, “Before today, had you ever heard of human papillomavirus?” Those who responded “yes” were asked to complete the HPV Knowledge Scale in a “True/False/don’t know” format. In creating a composite score for HPV knowledge, the scale developers suggested scoring “true” as 1, and “false and don’t know” as 0. As such, the general HPV knowledge score could range from 0 to 16. One of the original scale questions “HPV causes HIV/AIDS” was excluded from this scale since, as suggested by the authors of the scale, its poor performance on the scale may suggest that it may be more informative as an individual item rather than part of the subscale.Citation25,Citation26 As such participants could score between 0 and 15 on the general knowledge scale. Cronbach alpha for the original scale was 0.849 and test–retest reliability value was 0.68.

The HPV Vaccine Knowledge Scale is comprised of 7 items. As above, participants scored 1 for each correct response and 0 for each incorrect or “I don’t know” response. HPV vaccine knowledge score could vary between 0 and 7. Cronbach alpha for the original scale was 0.561 suggesting some heterogeneity of item content, and test–retest reliability value was 0.62 showing fair reliability.Citation25 Based on the developers exploratory principal factor analysis, four items did not load strongly (HPV vaccines require three doses; The HPV vaccines are most effective if given to people who have never had sex; The HPV vaccines offer protection against most cervical cancers; One of the HPV vaccines offers protection against genital warts). However, the developers stated that a follow-up EFA showed that removing items that did not load strongly did little to improve unidimensionality.Citation25

We also asked a series of questions on sexual behavior such as “Have you ever had sex?” “When was the last time you had sex?” “Have you ever had oral sex?” “In the past year, how many different people did you have sex with?” “How old was the last person you had sex with?” to juxtapose HPV and HPV vaccine knowledge against sexual behavior. Sexual intercourse was defined as anal or vaginal intercourse.

2.2. Data analysis

Data analysis included univariate and bivariate analysis in IBM SPSS (version 25). Chi-square tests were done to determine whether there was an association between HPV awareness,main outcome variable, sociodemographic (such as sex, age, place of birth) and sexual characteristics of participants (such as sexual initiation, HIV testing, condom use). Mann Whitney U test was also used to determine differences in HPV knowledge and HPV vaccine knowledge (outcome variables) by sociodemographic and sexual characteristics of the group.

3. Results

There were 1,553 completed questionnaires (100% completion rate). Of these, 797 (51.4%) were males and two individuals did not indicate their sex. As expected, 1287 (84.5%) of the sample resided in New Providence (7 schools), 154 (10.1%) lived in Grand Bahama (2 schools) and 82 (5.3%) lived in Abaco (3 schools). Most students (91.3%) were born in the Bahamas, 1.1% were born in Haiti, 3.6% and 3.0%, were born in the USA and Jamaica, respectively. More than half of the sample (51.2%) reported that they attend religious services frequently (once or more often per week).

With regards to sexual activity (n = 1456), 778 (53.4%) of the sample responded “yes” to ever having sex (42.9% or 298/695 females and 63.1% or 479/759 males). Thirty-eight males and 116 females did not respond to the question “Have you ever had sex”. Fifty-seven (11.2%) of those who reported never having sexual intercourse reported having oral sex.

3.1. Factors associated with ever hearing of HPV

With regards to the question “Before today, had you ever heard of Human Papillomavirus (HPV)?,” 146 (10.7%, 95% CI 9.1%-12.5%) responded “yes” (87/638, 13.6% females; 59/726, 8.1% males), and 1218 (89.3%) responded “no”. There were 188 who did not respond to this question and they were removed from further analyses. As such, 1364 individuals were available for further analysis. shows the characteristics of participants who had heard and had not heard of HPV. Between those who had heard and not heard of HPV, only “ever tested for HIV” (p = .01), “engaging in oral sex” (p = .04) and being female (p < .01) were statistically significant in Chi-Square analyses.

Table 1. Sociodemographic and sexual characteristics of school-aged youth who had heard and not heard of HPV (N = 1364, Chi Sq. test)

3.2. Sexual activity and awareness of HPV

As infection by HPV occurs most frequently through sexual activity, it was important to determine HPV awareness for those who had already initiated sexual activities and responded to the question on HPV awareness (n = 685). Of those who had initiated sex, 10.7% (73/685) had heard of HPV. Of this sexually active group, 23.1% reported sexual activity within the last week; 35.2% had three or more sexual partners in the past year; 57% always used condoms; 71.1% had a most recent sexual partner of their age group; 68.6% had never tested for HIV but of those who tested for HIV, 64% had done so within the last year. In bivariate analysis () being female, testing for HIV, oral sex, recent sexual activity, and frequent condom use, were associated with being aware of HPV (all p < .05).

Table 2. Sexual behavior characteristics of the sample who reported ever having sex by awareness (had heard vs. not heard) of HPV (n = 685, Chi Sq. test)

3.3. HPV general and HPV vaccine knowledge

Individuals who had heard of HPV were asked to respond to a 16-item general HPV knowledge and 7-item HPV vaccine knowledge scale.Citation25 shows the performance of each item on the scale. About 55% of the participants did not know that HPV causes cervical cancer; only 40.7% (50/123) correctly answered that HPV is the cause of genital warts; 38.5% (50/130) correctly stated that HPV is quite common; 43.4% (56/129) correctly responded that it can be passed on through skin to skin contact and 43.1% (56/130) were correct in indicating that men could get HPV. Although 68.2% (88/129) knew that someone could have HPV for many years without knowing it, only 33.6% (44/131) correctly answered that HPV may not have visible sign or symptoms. 77.1% (101/131) knew that having many sexual partners increases the risk of HPV. Only 18.3% knew that HPV cannot cause HIV and 23% were aware that HPV cannot be cured by antibiotics. Less than 10% knew that HPV can sometimes spontaneously clear without treatment.

Table 3. Frequency distribution of knowledge of HPV (N = 146) and HPV vaccine (N = 121) for those who had heard of HPV

As suggested by the authors of the HPV scale, “HPV can cause HIV/AIDS” was removed from the global knowledge scale due to its different psychometric properties and tested as a separate item.Citation25 HPV knowledge (n = 111, 44 males and 67 females) ranged from 0 to 13 (not correctly answering any of the questions to correctly answering 13 of the 15 questions). No participant correctly answered all the 15 questions. A Welch t-test was run to determine if there were differences in HPV knowledge between males and females due to the assumption of homogeneity of variances being violated, as assessed by Levene’s test for equality of variances (p = .01). The HPV knowledge score was not appreciably higher among males (M = 6.77, SD = 4.19) than females (M = 6.48, SD = 3.24). Male mean HPV knowledge score was 0.30, 95% CI [−1.19 to 1.77] higher than female’s mean HPV knowledge score. However, there was no statistically significant differences in mean HPV knowledge score between males and females, t (75.67) = 0.40, p = .069 ().

Table 4. Frequency distribution of HPV general knowledge and vaccine knowledge among school-aged youth. Chi Sq. test

For the item “HPV can cause HIV/AIDS”, there was a similar distribution in selecting the incorrect response for both males and females.

With regards to HPV vaccine knowledge, 121 participants responded to the questions on HPV vaccine (45 males and 76 females). HPV vaccine knowledge ranged from 0 to 6 (not correctly answering any of the questions to correctly answering 6 of the 7 questions). No participant correctly answered all the seven questions. An independent t-test was run to determine if there were differences in the HPV Vaccine Knowledge score between males and females. There was homogeneity of variance as assessed by Levene’s test for equality of variance (p = .40). HPV vaccine knowledge was not appreciably higher in females (Mean score = 1.76, SD = 1.64) compared to males (mean score = 1.69) (SD = 1.62) (). Male HPV vaccine knowledge score was −0.07, 95% CI [−0.68 to 0.53] lower than females. There was no statistically significant difference in mean HPV vaccine knowledge score between males and females, t (119) = −0.242, p = .81.

4. Discussion

Sexual intercourse is the most important risk for HPV infectionCitation15 and as such, it was important to evaluate the sexual behavior and sexual health practices that may put youth at risk for HPV. In this study, a proportionally large number of these youth (42.9% female, 63.1% males) were sexually active with almost a quarter reporting sexual intercourse within the past week and more than one-third reporting having three or more sexual partners within the past year. Multiple sexual partners is a confirmed independent risk factor for HPV related cervical cancerCitation15 and may be a risk factor for HPV-associated oropharyngeal cancers.Citation27 In their meta-analyses, Lui et al. observed a significant increased risk of cervical disease among women with multiple sexual partners.Citation15 As the number of sexual partners increased, the risk of invasive cervical cancer also increased. It was also argued that there may be other factors associated with multiple partners that may increase cancer risk.Citation15

Many in our sample were oral sex experienced, including some who had not had sexual intercourse. Oral sex is a risk factor for some oropharyngeal cancers.Citation27,Citation28 While we did not test these youths’ knowledge of oral sex as an HPV risk, it is likely that few knew of the link with HPV and oral sex. Awareness of HPV acquisition through oral sex has been shown to modify future desire for HPV vaccine uptakeCitation29 and may be an important area to include in the Bahamas school-based health education curricula.

4.1. HPV awareness

Only 10% of the sample reported that they had previously heard of HPV. This was an unexpected result as the study was conducted at a time when there was much discussion in the media about the merits of HPV vaccines, but also about the potential increased sexual compensatory behaviors among adolescent girls.Citation19,Citation30 While we did not ask participants for their source of HPV knowledge, previous research noted that greater media information may have an impact on HPV awareness.Citation31 In an earlier study among adults drawn from mostly clinical settings in the Bahamas, 46% had heard of HPV.Citation20 The setting of that study and the different age group sampled, may in part, explain the differences in knowledge between that study and the current one. However, Bahamian youth are not unique in their low HPV knowledge. In a study conducted in China in 2016–2017, only 15.5% of middle school children had heard of HPV.Citation32 Despite the widespread use of HPV vaccine in Europe, only 29.8% of European boys knew of HPV compared to 51.7% European girls.Citation33 Our results indicate that unfocused information on HPV may not reach the target audience. As such, it may be important to include information on HPV in school-based health education programs.

Young men’s awareness of HPV was lower than that of young women, perhaps because, in 2013, most of the debate on HPV had focused on a female-only HPV vaccine program.Citation34 Further, it was only in December 2014 that Gardasil was approved in the USA for males,Citation35 so males were not included in the knowledge sphere. For some time, the discussion of a male HPV vaccine strategy focused only on men who have sex with men,Citation36 a topic that would not be given much media attention in Caribbean societies. It would be important for future research (such as our follow-up study later in 2019) to determine whether sexuality issues have an impact on current HPV vaccine uptake for young men in the region.

4.2. HPV and HPV vaccine knowledge

Awareness of HPV does not translate into knowledge and understanding of HPV as a risk factor for anogenital and oropharyngeal cancers or genital warts. None of the youth in our study who had heard of HPV were able to correctly answer all the knowledge questions and, in particular, there was a large gap in knowledge of the relationship between HPV and cervical cancer, genital warts and other HPV related infections. This indicates that general information about HPV had not penetrated this youth group, despite US media discussions. Our data demonstrate that the misunderstanding that “men cannot get HPV” was prevalent, an issue seen in other research.Citation37 This may have been because of the previous focus on HPV as a women’s health issue.Citation36 As such, it is imperative that the health promotion programs and the media include men in the rhetoric of HPV prevention.

There was also poor understanding of how HPV is manifested (signs and symptoms of HPV), its relationship to HIV (HPV causes HIV/AIDS) and the general ubiquity of HPV (HPV is very rare). This fragmented information may lead youth (and parents) to consider HPV vaccines as a low priority. Studies oriented to the Health Belief Model have identified that, if HPV is not evaluated as a risk to personal health, it is less likely that individuals will take actions to protect themselves.Citation21,Citation38 Knowledge of the link between HPV and HIV infectionCitation39 and vice versaCitation40 may have an impact on HPV vaccine uptake and should be explored.

A poor understanding of HPV was also prevalent with regards to sexual health. The majority of those who completed the questions on HPV did not know that most sexually active individuals will get HPV during their lifetime; that early sexual debut is associated with increased HPV risk or that HPV causes genital warts. Sexual behaviors are known to be the most important risk factor for HPV.Citation15 Further, it is well established that improved knowledge of HPV and HPV vaccines can lead to improved HPV vaccine uptake.Citation21,Citation23

Youth had poor knowledge of the HPV vaccine, including being unaware of its association with cervical cancer prevention, dosing (at the time of the study, the recommended dosage was 3), and timing. Studies have reported that poor understanding of the HPV vaccine can lead to resistance to vaccine uptake or poor adherence to vaccine dosage.Citation23,Citation41 However, motivated youth may have an influence on their parents’ consenting to the HPV vaccine.Citation42 Since the implementation of the HPV vaccine, many countries have reported poor HPV vaccine uptake which may lead to lower optimal coverage for herd effect.Citation43

In the Bahamas, the HPV vaccine program was implemented after this study was conducted. Initial uptake of the HPV vaccine was poor (personal communication) reflecting our findings of poor knowledge and understanding. It also emphasizes the need for countries in the region who have not yet implemented a program, to create well-designed, multifaceted, intensive educational strategies to maximize HPV vaccine uptake. This education must target youth, educators, health-care providers and parents.Citation44Citation46

5. Limitations

There are several limitations to this study. Unlike the original scale which asked, “Have you ever heard of HPV vaccine?” followed by the scale items, we skipped this question and directly asked about HPV vaccines. Only 40 (3.3%) students who had never heard of HPV responded to this HPV vaccine scale and 97% of the responses were “I don’t know” to the items.

The main instrument measuring HPV knowledge scale test–retest reliability was reported as 0.68,Citation25 suggesting that the measure had low consistency. However, this reliability may be acceptable for this type of non-clinical research study.

As this study is based on data emanating from the male circumcision study, the sampling strategy for that study included only boys. However, due to stakeholder’s interest in knowing young girls’ opinion about male circumcision, the sample strayed from cluster sampling to convenience sampling. We will soon be implementing an HPV follow-up study in the Bahamas, post-vaccine implementation and will determine whether HPV and HPV vaccine knowledge has an impact on the low HPV vaccine uptake.

The survey recruited students from the government (public) senior high schools and did not include those attending private or religion affiliated high schools. As knowledge of sexual health is often poorer among students attending schools that promote abstinence-based sexual education only, it is not believed that including these students would have improved the study’s results.Citation47

6. Conclusion

There was a significant lack of awareness of HPV among school-aged youth in the Bahamas. This is an important gap in the HPV vaccine strategy and cancer prevention, as this is the age at which most people acquire HPV. However, awareness alone does not lead to positive actions toward health.Citation48 The results of the study indicate that, while youth are sexually active, they do not have sufficient knowledge of HPV as a risk for anogenital and oropharyngeal cancers and that there are safe and effective vaccines available. As such, it is important to develop education strategies specifically targeting this age group. There is a need to educate youth that HPV is a risk factor for many cancers and genital warts in both men and women and that men have a role to play in the prevention of HPV transmission. Having an enhanced knowledge of HPV will not only increase HPV vaccine uptake but may support the uptake of preventive measures such as Pap smear testing and condom use. For health officials, it is important to measure HPV and HPV vaccine knowledge as part of HPV prevention program planning.

Acknowledgments

This work was supported by the Canadian Foundation for AIDS Research (CANFAR), Toronto, Ontario, Canada [grant number 4, cycle 24]; and a Canadian Institutes for Health Research New Investigator Award.

The authors thank The Bahamas AIDS Foundation, The Bahamas National AIDS Program, and The UWI School of Clinical Medicine and Research, Nassau, for supporting this study. This study has been presented in part as an oral presentation at the 2018 Caribbean Public Health Conference (CARPHA), St. Kitts, West Indies.

Additional information

Funding

This work was supported by the Canadian Foundation for AIDS Research [4-24];Canadian Institutes of Health Research [New Investigator Award].

References

  • Saraiya M, Unger ER, Thompson TD, Lynch CF, Hernandez BY, Lyu CW, Steinau M, Watson M, Wilkinson EJ, Hopenhayn C, et al. US assessment of HPV types in cancers: implications for current and 9-valent HPV vaccines. JNCI J National Cancer Inst. 2015;107(6):djv086. doi:10.1093/jnci/djv086.
  • Phillips AA, Jacobson JS, Magai C, Consedine N, Horowicz-Mehler NC, Neugut AI. Cancer incidence and mortality in the Caribbean. Cancer Invest. 2007;25(6):476–83. doi:10.1080/07357900701359841.
  • Viens LJ, Henley SJ, Watson M, Markowitz LE, Thomas CC, Thompson TD, Razzaghi H, Saraiya M Human papillomavirus–associated cancers—United States, 2008–2012. MMWR. Morbidity and Mortality Weekly Report 2016:65 doi:10.15585/mmwr.mm6526a1
  • Colón-López V, Ortiz AP, Soto-Salgado M, Torres-Cintrón M, Mercado-Acosta JJ, Suárez E. Anal cancer incidence and mortality in Puerto Rico. P R Health Sci J. 2013;32:76–81.
  • Walsh T, Bertozzi-Villa C, Schneider JA. Systematic review of racial disparities in human papillomavirus–associated anal dysplasia and anal cancer among men who have sex with men. Am J Public Health. 2015;105(4):e34–e45. doi:10.2105/AJPH.2014.302469.
  • Nyitray AG, Fujimoto K, Zhao J, Giuliano AR, Schneider JA, Hwang L-Y. Prevalence of and risk factors for anal human papillomavirus infection in a sample of young, predominantly black men who have sex with men, Houston, Texas. J Infect Dis. 2018;217(5):777–84. doi:10.1093/infdis/jix617.
  • Stokley S, Jeyarajah J, Yankey D, Cano M, Gee J, Roark J, Curtis RC, Markowitz L. Immunization services division NCfI, Respiratory diseases CDC et al. Human papillomavirus vaccination coverage among adolescents, 2007–2013, and postlicensure vaccine safety monitoring, 2006–2014–united states. MMWR. Morb. Mortal. Wkly. Rep. 2014;63:620–24.
  • McQuillan GM, Kruszon-Moran D, Markowitz LE, Unger ER, Paulose-Ram R. Prevalence of HPV in adults aged 18-69: United States. US Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Health Statistics Hyattsville, MD:National Center for Health Statistics. [Accessed 2018 July 25]2011–2014.
  • de Pokomandy A, Rouleau D, Ghattas G, Vezina S, Cote P, Macleod J, Allaire G, Franco Eduardo L, Coutle F. Prevalence, clearance, and incidence of anal human papillomavirus infection in HIV infected men: the hipvirg cohort study. J Infect Dis. 2009;199(7):965–73. doi:10.1086/597207.
  • de Sanjose S, Quint WG, Alemany L, Geraets DT, Klaustermeier JE, Lloveras B, Tous S, Felix A, Bravo LE, Shin HR, et al. Human papillomavirus genotype attribution in invasive cervical cancer: A retrospective cross-sectional worldwide study. Lancet Oncol. 2010;11(11):1048–56. doi:10.1016/S1470-2045(10)70230-8.
  • Stanley M. Pathology and epidemiology of HPV infection in females. Gynecol Oncol. 2010;117(2 Suppl):S5–10. doi:10.1016/j.ygyno.2010.01.024.
  • Bruni L, Barrionuevo-Rosas L, Albero G, Serrano B, Gomez D, Bosch FX, de Santos S, Mena M, Muñoz J. Human papillomavirus and related diseases report: Bahamas. In: Human papillomavirus and related diseases report: Bahamas. ICO/IARC HPV Information Centre; 2017. July 27, [Accessed 2018 February 25].
  • Louie KS, de Sanjose S, Diaz M, Castellsagué X, Herrero R, Meijer CJ, Shah K, Franceschi S, Muñoz N, Bosch FX. Early age at first sexual intercourse and early pregnancy are risk factors for cervical cancer in developing countries. Br J Cancer. 2009;100(7):1191–97. doi:10.1038/sj.bjc.6604974.
  • Chen H-C, Schiffman M, Lin C-Y, Pan M-H, You S-L, Chuang L-C, Hsieh C-Y, Liaw K-L, Hsing AW, Chen C-J, et al. Persistence of type-specific human papillomavirus infection and increased long-term risk of cervical cancer. J Natl Cancer Inst. 2011;103(18):1387–96. doi:10.1093/jnci/djr283.
  • Liu Z-C, Liu W-D, Liu Y-H, Ye X-H, Chen S-D. Multiple sexual partners as a potential independent risk factor for cervical cancer: a meta-analysis of epidemiological studies. Asian Pac J Cancer Prev. 2015;16(9):3893–900. doi:10.7314/apjcp.2015.16.9.3893.
  • Li S, Ni XB, Xu C, Wang XH, Zhang C, Zeng XT. Oral sex and risk of oral cancer: a meta-analysis of observational studies. J Evid Based Med. 2015;8(3):126–33. doi:10.1111/jebm.12159.
  • Antonsson A, Cornford M, Perry S, Davis M, Dunne MP, Whiteman DC. Prevalence and risk factors for oral HPV infection in young Australians. PLoS One. 2014;9(3):e91761. doi:10.1371/journal.pone.0091761.
  • Lewis-Bell K Lessons learned from HPV introduction in the Caribbean. In. https://www.sabin.org/sites/sabin.org/files/karen_lewins.pdf. [Accessed 2019 March 4].
  • Maura M. Government to tackle cervical cancer through introduction of HPV vaccine. In: Govt. To tackle cervical cancer through introduction of HPV vaccine. Nassau (Bahamas); 2013. July 4. [Accessed  2018 July 26].https://www.Eleutheranews.com
  • Halliday D, Butler R, Francis D, Thompson J, Joseph M, Ragin C. Knowledge and attitudes toward HPV and the HPV vaccines in The Bahamas. West Indian Med J. 2013;62(8):(731–737).doi: 10.7727/wimj.2012.318
  • SJ MH K, Watson M, Braunack-Mayer AJ, Reuzel R, Tooher RL. Factors associated with HPV vaccine uptake in teenage girls: a systematic review. Vaccine. 2012;30(24):3546–56. doi:10.1016/j.vaccine.2012.03.063.
  • Bird Y, Obidiya O, Mahmood R, Nwankwo C, Moraros J. Human papillomavirus vaccination uptake in Canada: a systematic review and meta-analysis. Int J Prev Med. 2017;8(71). doi:10.4103/ijpvm.IJPVM_324_16.
  • Loke AY, Kwan ML, Wong YT, Wong AKY. The uptake of human papillomavirus vaccination and its associated factors among adolescents: a systematic review. J Prim Care Community Health. 2017;8(4):349–62. doi:10.1177/2150131917742299.
  • Deveaux L, Lunn S, Mae Bain R, Gomez P, Kelly T, Brathwaite N, Russell-Rolle G, Li X, Stanton B. Focus on youth in the Caribbean: beyond the numbers. J Int Assoc Physicians AIDS Care. 2011;10(5):316–25. (Chicago, Ill.: 2002). doi:10.1177/1545109710397367.
  • Waller J, Ostini R, Marlow LAV, McCaffery K, Zimet G. Validation of a measure of knowledge about human papillomavirus (HPV) using item response theory and classical test theory. Prev Med. 2013;56(1):35–40. doi:10.1016/j.ypmed.2012.10.028.
  • Marlow LAV, Zimet GD, McCaffery KJ, Ostini R, Waller J. Knowledge of human papillomavirus (HPV) and HPV vaccination: an international comparison. Vaccine. 2013;31(5):763–69. doi:10.1016/j.vaccine.2012.11.083.
  • Farsi NJ, El-Zein M, Gaied H, Lee YCA, Hashibe M, Nicolau B, Rousseau MC. Sexual behaviours and head and neck cancer: a systematic review and meta-analysis. Cancer Epidemiol. 2015;39(6):1036–46. doi:10.1016/j.canep.2015.08.010.
  • D’Souza G, Kreimer AR, Viscidi R, Pawlita M, Fakhry C, Koch WM, Westra WH, Gillison ML. Case–control study of human papillomavirus and oropharyngeal cancer. N Engl J Med. 2007;356(19):1944–56. doi:10.1056/NEJMoa065497.
  • Stock ML, Peterson LM, Houlihan AE, Walsh LA. Influence of oral sex and oral cancer information on young adults’ oral sexual-risk cognitions and likelihood of HPV vaccination. J Sex Res. 2013;50(1):95–102. doi:10.1080/00224499.2011.642904.
  • Forster A, Wardle J, Stephenson J, Waller J. Passport to promiscuity or lifesaver: press coverage of HPV vaccination and risky sexual behavior. J Health Commun. 2010;15(2):205–17. doi:10.1080/10810730903528066.
  • Pitts MK, Dyson SJ, Rosenthal DA, Garland SM. Knowledge and awareness of human papillomavirus (HPV): attitudes towards HPV vaccination among a representative sample of women in Victoria, Australia. Sex Health. 2007;4:177–80.
  • Xue L, Hu W, Zhang H, Xie Z, Zhang X, Zhao F, Qiao Y, Gao L, Ma W. Awareness of and willingness to be vaccinated by human papillomavirus vaccine among junior middle school students in Jinan, China. Hum Vaccin Immunother. 2018;14(2):404–11. doi:10.1080/21645515.2017.1393132.
  • Patel H, Jeve YB, Sherman SM, Moss EL. Knowledge of human papillomavirus and the human papillomavirus vaccine in European adolescents: A systematic review. Sex Transm Infect. 2016;92(6):474–79. doi:10.1136/sextrans-2015-052341.
  • Forster AS, Marlow LAV, Wardle J, Stephenson J, Waller J. Interest in having HPV vaccination among adolescent boys in England. Vaccine. 2012;30(30):4505–10. doi:10.1016/j.vaccine.2012.04.066.
  • FDA licensure of quadrivalent human papillomavirus vaccine (HPV4. Gardasil) for use in males and guidance from the Advisory Committee on Immunization Practices (ACIP). JAMA. 2010;304(5):518–19.
  • Daley EM, Vamos CA, Thompson EL, Zimet GD, Rosberger Z, Merrell L, Kline NS. The feminization of HPV: how science, politics, economics and gender norms shaped U.S. HPV vaccine implementation. Papillomavirus Res. 2017;3(142–148). doi:10.1016/j.pvr.2017.04.004.
  • Fontenot HB, Collins Fantasia H, Charyk A, Sutherland MA. Human papillomavirus (HPV) risk factors, vaccination patterns, and vaccine perceptions among a sample of male college students. J Am Coll Health. 2014;62(3):186–92. doi:10.1080/07448481.2013.872649.
  • Patty NJS, van Dijk HM, Wallenburg I, Bal R, Helmerhorst TJM, van Exel J, Cramm JM. To vaccinate or not to vaccinate? Perspectives on HPV vaccination among girls, boys, and parents in the Netherlands: A q-methodological study. BMC Public Health. 2017;17(1):872. doi:10.1186/s12889-017-4879-2.
  • Houlihan CF, Larke NL, Watson-Jones D, Smith-McCune KK, Shiboski S, Gravitt PE, Smith JS, Kuhn L, Wang C, Hayes R. Human papillomavirus infection and increased risk of HIV acquisition. Syst Rev Meta-anal AIDS. 2012;26:2211–22.
  • Looker KJ, Rönn MM, Brock PM, Brisson M, Drolet M, Mayaud P, Boily MC. Evidence of synergistic relationships between hiv and human papillomavirus (HPV): systematic reviews and meta analyses of longitudinal studies of HPV acquisition and clearance by hiv status, and of hiv acquisition by HPV status. J Int AIDS Soc. 2018;21(6):e25110. doi:10.1002/jia2.25110.
  • Holman DM, Benard V, Roland KB, Watson M, Liddon N, Stokley S. Barriers to human papillomavirus vaccination among us adolescents: A systematic review of the literature. JAMA Pediatr. 2014;168(1):76–82. doi:10.1001/jamapediatrics.2013.2752.
  • Batista Ferrer H, Trotter CL, Hickman M, Audrey S. Barriers and facilitators to uptake of the school-based HPV vaccination programme in an ethnically diverse group of young women. J Public Health (Oxf). 2016;38(3):569–77. doi:10.1093/pubmed/fdv073.
  • Brisson M, É B, Drolet M, Bogaards JA, Baussano I, Vänskä S, Jit M, Boily M-C, Smith MA, Berkhof J, et al. Population-level impact, herd immunity, and elimination after human papillomavirus vaccination: A systematic review and meta-analysis of predictions from transmission-dynamic models. Lancet Publ Health. 2016;1(1):e8–e17. doi:10.1016/S2468-2667(16)30001-9.
  • Cunningham MS, Davison C, Aronson KJ. HPV vaccine acceptability in Africa: A systematic review. Prev Med. 2014;69(274–279). doi:10.1016/j.ypmed.2014.08.035.
  • Dempsey AF, Butchart A, Singer D, Clark S, Davis M. Factors associated with parental intentions for male human papillomavirus vaccination: results of a national survey. Sex Transm Dis. 2011;38(8):769–76. 710.1097/OLQ.1090b1013e318211c318248. doi:10.1097/OLQ.0b013e318211c248.
  • Fiks AG, Grundmeier RW, Mayne S, Song L, Feemster K, Karavite D, Hughes CC, Massey J, Keren R, Bell LM, et al. Effectiveness of decision support for families, clinicians, or both on HPV vaccine receipt. Pediatrics. 2013;131(6):1114–24. doi:10.1542/peds.2012-3122.
  • Santelli J, Ott MA, Lyon M, Rogers J, Summers D, Schleifer R. Abstinence and abstinence-only education: A review of u.S. policies and programs. J Adolesc Health. 2006;38(1):72–81. doi:10.1016/j.jadohealth.2005.10.006.
  • Perkins EL, Stennis KB, Taylor Spriggs V, Kwegyir-Afful EA, Prather A. Is knowledge enough? Considering hiv/aids risk behaviors and hiv/aids knowledge with African American women. Int. J. High. Risk. Behav. Addict. 2014;3(3):e15038–e15038. doi:10.5812/ijhrba.15038.