Abstract
This study aimed to assess the literacy of Human Papillomavirus (HPV) and its vaccine between genders in young adults in an Asian urban community. The secondary aim was to identify factors associated with the acceptability of HPV vaccine among unvaccinated males. A self-administered e-survey was distributed via convenience sampling over 3 months in 2022 in Singapore. Demographic data and literacy on HPV and HPV vaccine were collected from young adults aged 15–24 years through a secured electronic platform. Chi-square or Fisher’s exact test was used to examine the association between acceptability of vaccine uptake and literacy of HPV and HPV vaccine. 591 youths comprising of 236 (40%) males and 355 (60%) females completed the survey. HPV vaccination uptake rate was low in males (11.4%) but high in females (80%). Both genders had low awareness on the ability of HPV to infect males (50%) and majority (80%) were unaware of the benefits of HPV vaccine to males. Among unvaccinated males, 82.5% accepted the recommendation of providing males with HPV vaccination, and 72.7% were acceptable towards taking up the vaccine. The main barriers to vaccination were cost (78.9%) and inconvenience (52.2%), while lifelong immunity (67.5%) and government health policies (67%) were identified as enablers. Young adults had low literacy on HPV’s ability to infect males and the benefits of HPV vaccine to both genders. Its uptake in males would depend on their acceptance of the HPV vaccine, cost, administration convenience and duration of its immunity post-vaccination.
Introduction
Human papillomavirus (HPV) is transmitted through vagina, oral and anal sexual intercourse and affects both genders. 1 Males are the main source of HPV transmission, although infected females can also transmit the infection to males. 2 HPV causes 70% of cervical cancer, 70% of oropharyngeal cancer, and 90% of anus cancer which can be attributed to type 16/18. 3 Approximately 40% of HPV-related cancer occurs in males, 4 and contributes to 10% of HPV-related deaths. 5 Besides cancer, HPV-related genital warts are also observed with an incidence of 1%. 6 The annual cost for managing HPV-related diseases ranges from USD 790 million in United States of America (USA) to €31 million (∼USD 34.1 million) in Sweden, which averages out to be approximately USD 2.45 and USD 3.74 per inhabitant respectively.7,8 In Singapore, HPV-related diseases incur treatment cost averaging SGD 3.3 million (∼USD 2.4 million) per year. 9
HPV vaccination is the main prevention to HPV infection and becomes more pertinent due to increasing number of diverse sexual orientations. 10 In a lifetime, 58% of people have an average of two to nine sexual partners, which increases their risk of contracting HPV infection. 11 HPV vaccines can protect individuals from HPV-related cancers and genital warts. 1 There are three types of HPV vaccine – Bivalent, Quadrivalent and Nonavalent. Bivalent Cervarix™ protects against type 16/18, which causes cervical cancer. On top of HPV 16/18, quadrivalent Gardasil 4™ covers type 6/11 which causes genital warts. In addition to the former four strains, nonavalent Gardasil 9™ includes five more types (31/33/45/52/58) that are considered intermediate for causing cancer. 12
With the rising incidence of HPV-related anal and oropharyngeal cancer to approximately one per 100,000 males, 13 early HPV vaccination in males can potentially reduce HPV-related cancers in both genders, genital warts, and their associated healthcare cost. In Australia, the National HPV immunization strategy was implemented in 2013 to all youths (both males and females) aged 12–13 years old, 14 with 80% being fully vaccinated by Gardasil 9™. 15 A study by Taira et al. found that HPV vaccination for males resulted in about 2.2% reduction of cervical cancer cases in females. 16 The implementation of the immunization strategy correlates with a decline in the incidence of cervical cancer, dropping from 7.4 to 6.6 per 100,000 females between 2012 and 2017. 17 However, some countries such as Singapore and Thailand only provide females with HPV vaccination in their national immunization programme to solely target on cervical cancer prevention. 18 In Singapore, females aged 13–14 years old are provided with free Cervarix™ vaccination in school under the National School-based HPV programme. 19 It is not mandatory and requires parental consent, but more than 90% took up the vaccine since the inauguration of the programme in 2019. 20
Singapore launched “Healthier-SG” in July 2023, a new national healthcare programme advocating preventive health across its 5.7 million Asian population, regardless of gender and ethnicity. 21 Vaccinating males, who represent half of the local population, with HPV vaccine such as Gardasil can effectively protect their sexual partners, irrespective of gender, from HPV infection. High HPV vaccination rate will enhance the local herd immunity, leading to a healthier population with reduced risk of HPV infection and its associated consequences.
Awareness and acceptability to be vaccinated against HPV are determinants of the vaccine uptake rate in the community, as alluded by the high HPV vaccine uptake rate among young females due to its structured HPV vaccination programme in local schools. 22 Assessing the literacy of HPV and its vaccine, including factors influencing their decision-making to receive the vaccine among youths, will facilitate the design of an optimal HPV vaccination programme for males. 23 This study aimed to assess the literacy of HPV and its vaccine between genders among young adults in an Asian urban community. The secondary aim was to identify factors influencing the acceptability of receiving the HPV vaccine among unvaccinated male participants. We hypothesize that young males lack knowledge on HPV and its vaccine which affects their acceptability of receiving the HPV vaccine.
Materials and methods
Study design
A cross sectional study using a self-designed web-based questionnaire was conducted between September to November 2022. HPV infection has been associated with perceived perverse sexual behavior and social stigma in neighboring Malaysia with a similar Asian population. 24 To avoid concerns from HPV-related stigma, recruitment was performed through an anonymized e-survey.
The study included youths aged 15–24 years, who are the target recipients of the HPV vaccine. A user acceptance test was performed on the e-survey prior to recruitment, with six eligible youth participants to ensure the questionnaire was clear and understandable, with 100% acceptance rate. Youths who were unable to read and understand English were excluded from the study. The survey was distributed via convenience sampling using social media, messaging application such as WhatsApp™, and word of mouth. Participants were recruited by scanning the QR code or survey link provided which redirected them to fill in the questionnaire. FORMSG, a local secured online platform was used for data collection. 25 The purpose of the study was explained to the participants before starting the survey, with confidentiality of participants ensured. Participation in the survey implied consent. All data collected was stored and maintained on a password-locked computer only accessible to the research team members.
Sample size
According to Chowdhury et al., 43.2% of people have good knowledge on HPV. Using 97% confidence interval and 5% precision, the minimum sample size required is 463 using sample size for proportion. 26 With an estimated of 44% response rate for internet survey according to Meng-Jia, 27 the survey was sent out to at least 1052 individuals.
Questionnaire
The survey consisted of 29 questions comprising six sections: demographics (3 questions), literacy on HPV and HPV vaccine (10 questions), acceptability of HPV vaccine recommendation (3 questions), side effects of HPV vaccine (7 questions), HPV vaccine uptake (5 questions) and number of e-survey distributed (1 question). Questions were either ranked on a five-point Likert scale (Strongly Agree, Agree, Neutral, Disagree and Strongly Disagree) or in multiple choice format. The main variable of interest (dependent variable) was acceptability of HPV vaccination, obtained from the question “I am willing to be vaccinated” under the “HPV vaccine uptake” section. Participants who answered Strongly Agree and Agree were classified as those willing to be vaccinated against HPV infection. Views towards HPV vaccine recommendation was measured from the question “HPV vaccine should be recommended for young male in Singapore”. Demographics and questions related to literacy of HPV and HPV vaccine were added as independent variables. Response rate was tabulated via asking participants on the number of e-surveys they have distributed.
Ethical review statement
Ethics approval was obtained from the approval authority in an institution of higher learning in Singapore prior to the commencement of the study. The e-survey was performed in accordance with relevant regulations and guidelines.
Statistical analyses
Frequencies and percentages were presented for categorical data such as demographics and literacy on HPV and HPV vaccine. Chi-squared test was used to test for association between age group, ethnicity with respect to gender. Additionally, Chi-squared or Fisher’s exact test was used to test for association between gender and literacy on HPV and HPV vaccine in addition to HPV information source. To identify the factors influencing acceptability to uptake HPV vaccine among the unvaccinated males, significant factors (p ≤ .05) from bivariate analysis were included in the multivariable binomial logistic regression model as potential confounders. Odds ratio and their confidence interval were presented for factors associated with acceptability to uptake the HPV vaccine. All analysis were carried out on R version 3.5.2 and Rstudio with tidyverse library. Statistical significance was set at p ≤ .05.
Results
Demographics and vaccination rate of the study population
Demographics, characteristics and literacy of HPV and HPV vaccine among youths (N = 591).
* Percentages may not sum up to 100% due to rounding off.
Approximately half of the participants had been vaccinated against HPV (52.6%). HPV vaccination rate stood at 11.4% and 80% for males and females respectively, with significantly more HPV vaccinated females (p < .001). Among unvaccinated participants, 79% of females and 72.7% of males were acceptable towards receiving the HPV vaccine.
Literacy of HPV and HPV vaccination in males and females
Participants had low literacy on the ability of HPV to infect males (48.9%) and high literacy on the ability of HPV to infect females (78.8%). A significant percentage of female agreed that HPV can infect females (p < .001) and are aware of the availability of HPV vaccine (p < .001). The overall literacy on HPV vaccine ranges from 20.3% to 75.6%, with males having lower literacy compared to females. Females had significantly higher awareness that HPV vaccine is given to females (p < .001) and reduces risk of cervical cancer (p < .001). However, majority of the male and female participants were unaware of the benefits of HPV vaccine to males, specifically HPV vaccine reduces genital warts (78.0%) and anal cancer (79.7%) in males. Despite the low awareness on the benefits to males, approximately 66% for both genders thought that HPV vaccination should be recommended for young males. The results are summarized by frequency and percentages as shown in Table 1.
HPV vaccination information source in males and females
The primary source of information for HPV vaccination were briefings and talks in school (53.3%) followed by family (21.7%). Social media (21.3%), mainstream media (18.8%) and friends (14.4%) were the least common source of information. Chi-square test revealed that gender was significantly associated with briefings or talks in school (p < .001) and family (p < .001).
Predictors for acceptability of HPV vaccination in unvaccinated males
Acceptability of HPV vaccination for unvaccinated male youths in logistic regression (N = 209).
* Percentages may not sum up to 100% due to rounding off.
Bivariate analysis showed that unvaccinated males who were aware that HPV can infect males were more acceptable to receive the HPV vaccine (p = .002). However, it was not significant in multivariable logistic regression. Multivariable logistic regression revealed that unvaccinated males were more acceptable to receive the HPV vaccine if they were agreeable on its recommendation [OR = 1.19; 95% CI = 1.19–5.94; p = .018]. Although not statistically significant, unvaccinated males who were aware that HPV vaccine can be given to males [OR = 2.45; 95% CI = 0.92–7.09; p = .082] were more acceptable to receive the HPV vaccine. Demographic, willingness to pay for vaccine and other factors on awareness of HPV and its vaccine were not statistically significant.
Barriers and enablers for HPV vaccination in unvaccinated youths
Figure 1 summarizes the responses to potential barriers for HPV vaccination. Majority of unvaccinated males (78.9%) cited cost of HPV vaccine as a concern. This was followed by inconvenience of receiving the vaccine (52.2%) and side effects of the vaccine (50.7%). Stigma around the vaccine was of least concern (17.7%) and was not associated with awareness on the availability of HPV vaccine (p = .370). Figure 2 shows the responses to potential enablers for HPV vaccination. To increase uptake of HPV vaccination, participants reported lifelong immunity (67.5%) and governmental health policy (67%) as the two most effective factors. For unvaccinated females, cost of HPV vaccine (69.0%) was listed as the main barrier for HPV vaccination, while parental advice (70.4%) was the most influential factor to influence their willingness. Barriers of HPV vaccination in unvaccinated males. Enablers of HPV vaccination in unvaccinated males.
Discussion
This study assessed the literacy on HPV and its vaccine between genders among local youths. 78.8% of participants agreed that HPV can infect females, but only 48.9% agreed that males can be infected. Males were less aware that HPV can infect females (61% for males and 91% for females). These findings reflect that both genders lack knowledge that HPV can infect males, and males lack knowledge that HPV can infect females. Participants also were less cognizant that HPV vaccine could be administered in males (63.5%), prevent genital warts (78.0%) and anal cancer (79.7%). The finding was consistent with an earlier study that identified poor literacy of HPV and HPV-related cancer in males. 28 While females knew that HPV vaccine could prevent cervical cancer, few were aware of its protection against genital warts (23.4%) and anal cancer (21.1%). Hence educational talks through local school health service and media should expound the additional benefits of the HPV vaccine beyond mitigating cervical cancer.
Unvaccinated males who agree to the recommendation of HPV vaccination were 1.2 times more likely to accept the HPV vaccine (p = .018) (Table 2). Considering that 89% of them were not vaccinated and over half had limited literacy in HPV and its vaccine, improving HPV literacy of males might improve uptake of its vaccine. A study conducted among university students revealed that HPV knowledge scores was higher in the vaccinated. 29 As parental consent would also be required for HPV vaccination, improving the literacy of parents on HPV and HPV vaccine is equally important. A qualitative study reported that mothers had low awareness on the risk of HPV-related cancers and benefits of HPV vaccination. 30 Such finding may hinder parents from providing consent for their sons to receive the vaccine.
Despite high acceptability among unvaccinated males (72.7%) on their HPV vaccination, cost (78.9%) and inconvenience (52.2%) of HPV vaccination were identified as the primary barriers. Participants identified health policy recommended by policymakers (67.0%) and lifelong immunity of HPV vaccine (67.5%) as key factors to influence their HPV vaccine uptake. 18% of unvaccinated males would only take up the HPV vaccine if it was provided for free. If males had to pay for the vaccination, majority in our study (93%) were only willing to pay up to SGD 250. In Singapore, HPV vaccination is not included for males in the National vaccination program. In addition, males are also required to visit a clinic to receive the vaccine at their own time, and pay for the multi-dose vaccination ranging from USD 183 to USD 584 (1 USD = 1.37 SGD).
The recipients of the vaccine should be provided with information of the length of its immunity post-immunization. Literature reveals that antibody levels against HPV remains relatively stable in a 10-year period after the three-dose HPV vaccine regimen. 31 Besides immunity, the HPV vaccine has also proven its safety profile with serious adverse events such as anaphylaxis occurring in 1.7 per million doses. 32 Such information could be relayed and reassure youths on the benefits of long-term immunity of HPV vaccine and the low risk of serious adverse events.
Results of this study indicated that 17.7% of unvaccinated males perceived stigma towards HPV vaccine, although it did not significantly influence their acceptance to uptake. A study in Canada revealed that HPV-related stigma was associated with lack of awareness on the availability of HPV vaccine for males. 33 However, in this study, there was no significant difference between both factors. Nonetheless, it is important to address HPV vaccine-related stigma given its relation to promiscuous sexual behavior discovered in a Malaysian study. 34 Efforts could be focused on correcting misconceptions that HPV vaccination in males does not necessarily imply an increase in their number of sexual partners and that vaccination is not a means to encourage such behavior.
Only 22.0% and 20.3% of youths were aware that HPV vaccine can prevent genital warts and anal cancer respectively. As preventive health takes precedence in Healthier-SG, it becomes pertinent to educate and address concerns of youths on HPV and its vaccine. Although briefings and talks in schools were the main source for HPV education (53.3%), significantly fewer males (22.9%) compared to females (73.5%) attended the talks. Information on HPV vaccine preventing anal cancer and genital warts, plus knowledge on the three different types of HPV vaccine and their strain coverage should be covered in such education talks. Besides talks in school, social media can also be used as a platform for dissemination of information. Few participants reported receiving HPV-related information from social media (18.2% for males and 23.4% for females). A study in the USA reported that social media usage led to increased awareness of HPV and HPV vaccine. 35 Given that all youths own a smartphone, 36 schools could utilize social media to serve as trusted channels for HPV information and address queries that might arise, minimizing the potential risk of misinformation.
Strengths and limitations
This study provides perspectives of HPV and its vaccination among the local young adults which will have relevance and implications to the new national preventive health programme. Nonetheless, it also has its limitations. Convenience sampling is susceptible to selection bias, but the electronic survey format mitigated potential social stigma and opened the study access to participants across all local educational institutes and include those who are working or enlisted in the mandatory military service. Majority of the participants in the survey was Chinese, which limited findings from the minority groups, but this study was not intended to stratify the participants based on ethnicity.
Conclusion
Females had higher literacy on both HPV and its vaccine compared to males. There was low awareness that HPV can infect males, and the benefits of the vaccine for males, regardless of gender. Literacy was a key factor to males being agreeable towards HPV vaccine recommendation. Both males and females need to be educated on the various HPV vaccines available, and their benefits on anal cancer and genital warts. Cost and duration of immunity can influence choice of taking up the vaccination.
Availability of data statement
The data that supports the findings of this study are available from the corresponding author upon reasonable request.
Footnotes
Acknowledgments
The authors would like to thank Dr Wee Juan Dee for his guidance to the students and administrative support to obtain IRB approval.
Author contributions
Conceptualization, NC and DX; methodology, NC and DX; data curation, XY, RK and ZT; formal analysis, DX; writing—original draft preparation, DX and QH; writing—review and editing; QH and NC. All authors have read and agreed to the published version of the manuscript.
Declaration of conflicting interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) received no financial support for the research, authorship, and/or publication of this article.
Ethical approval
Ethical approval for this study was obtained from Institutional Review Board, Hwa Chong Institution.
Informed Consent
Implied consent was obtained from all subjects before the study. Written informed consent was not obtained because the study utilizes an anonymized e-survey for recruitment.
