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Assessing the Effectiveness of Web-Based Modules on Human Papillomavirus Among Dental and Dental Hygiene Students

Literature suggests that deficiencies among dental professional students in both knowledge and awareness of human papillomavirus (HPV) and its association with oropharyngeal cancers (OPC), as well as its risk factors implicating the prevalence of HPV, may be due to the lack of HPV-related education during professional schooling. The aim of this study was to assess the effectiveness of an online learning tool to educate dental and dental hygiene students about HPV and its association with OPC, rapidly evolving disease patterns, and dental professionals’ role in HPV-associated OPC prevention efforts. A three-section online learning module was developed to improve dental professionals’ comfort levels with, and knowledge of, HPV. The participants were recruited to participate in surveys before and after the intervention. Descriptive statistics and chi-square analysis were computed to study the effectiveness of the modules in improving the knowledge of students about this topic. Pre-intervention survey participants totaled 142, and 107 participants answered the post-intervention survey. The majority of the study participants had some baseline understanding of HPV prior to accessing the modules. After reviewing the modules, there was a statistically significant increase in the proportion of respondents who identified OPC (p = 0.01), vaginal cancer (0.02), vulvar cancer (0.04), and penile cancer (0.01) as associated with HPV. A gap in the understanding of HPV vaccine–eligible groups was noted in almost half of the participants; while most participants could correctly identify that boys and girls aged 9–12 years were eligible to get the vaccine, the gap in knowledge in this regard was related to “25-year-old with an abnormal pap result.” Due to the evolving nature of this topic, there is a need to find new and effective methods of disseminating HPV-related information among the existing and future dental workforce.


Introduction
Persistent, high-risk human papillomavirus (HPV) infections are associated with most oropharyngeal, cervical, and anal cancers in the USA.
[1] Data obtained from cancer registries of diagnosed patients between 1995 and 2005 show that approximately 72% of oropharyngeal cancers (OPC) are caused by HPV, [2,3] and the rates of HPV-associated OPC have progressively surpassed those of cervical cancer in the USA. [3][4][5] Even though the incidence of HPV-associated OPC continues to increase and pose a significant threat to public health, most of these cancers are now preventable through HPV vaccination.
The HPV vaccine is a primary prevention tool which has been proven to be safe and effective in protecting against the most common HPV strains, including the high-risk types 16 and 18 that cause 80% of cancers. [6,7] However, the US rates of HPV vaccine administration and coverage remain low. [8][9][10] According to National Immunization Surveys (NIS) data, only 61.4% of females and 56% of males aged 13-17 in the USA have received all of the recommended doses of the HPV vaccine as of 2020. [11] This continues to represent an unmet need and poses a public health threat.
Both the American Dental Association (ADA) and the American Association for Pediatric Dentistry (AAPD) have issued policy statements that endorse dental professionals' role in the promotion of HPV vaccines to prevent OPC in dental care settings. [12,13] Studies conducted in the past couple of years indicate that, post availing educational opportunities on this topic, several oral health care providers felt more comfortable educating their patients about HPV and HPV vaccinations [14][15][16][17] Because dental providers perform oral cancer screenings and routinely see their patients on a bi-annual/annual basis for preventive care, [18] point-of-care opportunities to educate about HPV can be effectively conducted in dental care settings. Beyond education, dental providers frequently administer local anesthetic injections for oral procedures, and several states now allow dentists to administer the COVID-19 and influenza vaccines. Such developments make the increased access of HPV vaccination in the dental setting seem closer to reality. [19][20][21][22] Increasing access to care by including dentists in HPV immunization practices may improve HPV completion rates while minimizing health disparities related to factors such as gender, racial and ethnic minority backgrounds, and geographic location. [23,24] Few studies have assessed the knowledge, awareness, and acceptance of vaccine administration and its implications with HPV-OPC among dental and dental hygiene students. [25][26][27] In addition, current deficiencies in both knowledge and awareness may be due to the lack of HPV-related education during school. [28][29][30] Recent evidence suggests that providing HPV-specific educational resources may improve both knowledge and likelihood of recommending HPV immunization in patient care. [31][32][33] This study builds upon this very important and timely topic from existing literature. Due to the unprecedented challenges of uncertainty and adaptation of the COVID-19 pandemic, remote education has found its own niche, rendering online modules as a useful tool for distance learning especially when in-person settings are restricted. As such, with this study we aimed to assess the effectiveness of a novel web-based learning tool to educate dental and dental hygiene students about HPV and its association with OPC, as well as current preventative strategies for HPV-associated cancers that are both adaptable and pertinent to the evolving global environment and dental workforce.

Study Modules
We developed a three-section, web-based, learning module for dental and dental hygiene students focused on improving comfort levels with, and knowledge of, HPV.
The first section of the module consisted of flash cards that included information about HPV viral strains, HPVrelated disease prevalence and epidemiological trends, HPV relationship to OPCs, and the current Advisory Committee on Immunization Practices (ACIP) recommendations for HPV vaccination. [34] The second section consisted of a pre-recorded presentations describing the role of oral health providers in HPV vaccine promotion and practical information on integrating HPV prevention into patient care. The last section of the module included patient-facing educational materials from professional organizations such as the ADA and AAPD for use in dental practices.
Descriptive 24-item pre-survey and 18-item post-survey questionnaires were used to assess the knowledge levels of the participants. The surveys were internally validated among the research investigators on the project, along with feedback from subject matter experts. These surveys included questions on HPV-associated cancer awareness, knowledge of risk factors for HPV-associated OPC, HPV vaccine recommendations, and student's attitude and comfort levels in discussing HPV with patients. The surveys were administered using Google forms and were connected to the modules' webpage. Details of the surveys can be found under Appendices I and II.
The Institutional Review Board at the Indiana University School of Dentistry approved this study as exempt (Protocol # 2,009,006,645).

Data Collection
Between November 2020 and July 2021, all modules were shared with the class listservs for dental and dental hygiene students at the Indiana University-Dental Public Health, dental residents at Harvard School of Dental Medicine, Boston University School of Dental Medicine, and University of California, San Francisco School of Dentistry. The survey and module links were shared first in November 2020 and reminder emails were sent out thrice to all participants (every 2 months). Participation was voluntary and all participants provided consent electronically. The participants who completed both pre-and post-surveys were provided with $5 Amazon gift certificates.

Data Analysis
Descriptive statistics were used to summarize demographic information, including age, gender, and race/ethnicity. Frequency, percentage calculation, and the chi-square test were computed to compare the respondents' answers for pre-and post-intervention questionnaires. All p values were considered statistically significant at p < 0.05. We also used descriptive statistics to synopsize the usefulness of the modules. SPSS version 22 for Windows was used.

Participants' Distribution
The pre-and post-intervention surveys had a total of 142 and 107 respondents, respectively. Most respondents were dental students (68.3%; n = 97); females (71.8%; n = 102); and between 18 and 30 years of age (74.6%; n = 106). Details on the demographic breakdown of the participants can be found in Table 1.

Baseline Understanding of HPV Infection (Pre-survey Responses)
Most of the study participants had some previous knowledge of HPV prior to accessing the modules, as shown in the presurvey analysis ( Table 2). 94.4% (n = 134) of the respondents correctly identified HPV infections as not "rare" and 93.7% (n = 133) noted HPV as a sexually transmitted infection. Although it was not statistically significant, the percentage of respondents who correctly answered the above questions increased after reviewing the modules. (The percentages of correct responses on the post-survey for the above questions were 98.1% (n = 105) and 95.3% (n = 102) respectively.)

Comparison of Pre-and Post-survey Responses
A statistically significant increase in correct responses was observed following the intervention for several questions, such as: "Do you think that an HPV infection would go away on its own without treatment?" (p = 0.002); "Which of the following cancers may be caused by HPV" (p = 0.003); "What percent of sexually active women and men are infected with HPV" (p = 0.001); and "Which of these do you think the HPV vaccine can reduce or prevent" (p = 0.001) ( Table 2). When compared to the pre-educational intervention survey, a greater proportion of respondents could correctly identify that HPV infection was the main cause of genital warts during the post-survey, but it was not statistically significant (73.2% vs. 84.1%; p = 0.296).
When asked about the type of cancers caused by HPV, 90.8% of the participants on the pre-survey and 95.3% on the post-survey correctly indicated cervical cancers (Table 3). There was a statistically significant improved knowledge postintervention for other HPV-associated cancers: OPC (p = 0.01), vaginal (0.02), vulvar (0.04), and penile (0.01). The number of participants who correctly identified diseases that could be prevented by HPV vaccine also increased post-intervention (32.4% vs. 54.2%; p = 0.001). There was a statistically significant decrease in the number of students who incorrectly responded that chlamydia infections were caused by HPV (p = 0.05). The percent of correct responses decreased for some (78.2% vs. 72.9%) for the question "if someone has HPV, they will develop cancer at some point," but it was not statistically significant. The responses to the question on ACIP's HPV vaccine recommendation were not statistically significant; almost half of the respondents (N = 65; 45.8% vs. N = 50; 46.7%) could not correctly identify a one vaccine-eligible group (previously unvaccinated 25-year-old women with abnormal pap smear). However, most respondents could correctly indicate other vaccine-eligible groups, such as "girls and boys 9-11 years of age" (girls aged 9-12 years: 85.2% vs. 85%, p = 0.97; boys aged 9-12 years: 74.6% vs. 82.25, p = 0.15). There was a statistically significant (p = 0.012) increase in respondents who reported feeling a little (35.2% vs. 39.3%) or very comfortable (40.8% vs. 52.3%) in talking to their patient about HPV. There was a statistically significant increase in respondents who felt "a little comfortable" administering the HPV vaccine if they had adequate training and reimbursement (22.5% vs. 30.8%, p = 0.05).

Usefulness of the Modules
More than 90% of study participants thought the information provided in the modules was valuable and 47% of the participants found the information to be new (Fig. 1). Importantly, 95% of study participants reported the information provided in the modules was easy to understand.

Discussion
Our study assessed the effectiveness of web-based learning modules on HPV among dental students, dental residents, and dental hygiene students. Following the online educational intervention, there was an increase in knowledge about topics such as prevalence of HPV infections, HPVassociated cancers, and diseases that could be prevented with the HPV vaccine. Most participants correctly identified that HPV is a common sexually transmitted infection Several studies in the past have highlighted the importance of having an educational intervention on HPV for oral health providers to improve their knowledge and attitude toward HPV-associated cancer prevention and vaccination efforts. [28,[34][35][36][37][38][39] Yet, a recent study indicates dental hygiene programs, regardless of institutional setting, provide less than 2 h of HPV didactic content and clinical application  [40]. Unlike other studies that reported an obvious lack in dental students' knowledge of both HPV pathogenesis and the HPV vaccine, [41] we found that most students had good, though basic, understanding of HPV and the cancers associated with it, even prior to accessing the modules. Studies also suggest that HPV literacy among providers plays a vital role in improving patient education and OPC prevention. [26,42,43] Deficits in students' knowledge about this topic as observed in our study necessitate the importance of including and expanding on this topic in dental curriculums. Such curriculum content could have substantial impacts in OPC prevention, as our study's respondents reported a significant increase in comfort levels in talking to patient about HPV following the intervention.
The online educational intervention utilized in our study was designed to provide relevant and current information on HPV in a concise and accessible manner. It was found to be of value and was easily understood by most of the study participants. The limitation of this study included the cross-sectional study design with a relatively small and heterogenous (dental students vs. dental residents) sample size, so the generalizability of the study results is limited. This could also explain why the knowledge of certain topics may be higher in our study participants as compared to other studies. It is important to note how variation by school location and level/type of education setting (e.g., students versus residents, dental programs vs. dental hygiene programs) can potentially confound not only knowledge findings but also findings related to level of comfort in talking about the topic as well.
Sampling error is another potential limitation as the choice of participants to take part in the study might have been influenced by their previous knowledge on oral cancer and HPV and their interest in the topic. Moreover, not all participants completed both questionnaires, which limited the measurement of efficacy of the intervention.
There may be different ways to introduce HPV-related educational opportunities for the existing and future dental care workforce. One approach may be to include more specific information about HPV in relevant courses in dental school curricula, and continuing education courses for practicing dental professionals could be another. Because large-scale changes to dental curricula may not parallel the evolving role of dentists in vaccine administration, it is important to find other effective methods of disseminating HPV-related information, to prepare the existing and future dental workforce.