Introduction

Each year in the United States (U.S.), an estimated 35,900 people are diagnosed with a Human Papillomavirus (HPV)-related cancer [1]. An estimated 90% of these cases could be prevented by HPV vaccination [1]. However, a 2020 U.S. nationally representative survey found that only 75% of adolescents aged 13–17 received at least 1 dose of the HPV vaccine, only 59% were fully vaccinated, and vaccination rates were lower among male compared to female adolescents [2]. Furthermore, from 2015 to 2018, there was a 79% increase in the percentage of parents who cited safety concerns as a primary reason to refuse initiation of the HPV vaccine for their adolescents [3]. In the general population, HPV knowledge is relatively limited, particularly surrounding its association with cancer as upwards of 77% of people were unaware of the links between HPV and anal, penile, and oral cancers [4].

Improving HPV vaccination rates is a U.S. public health priority. Previous studies have found that physicians may hesitate to mention HPV vaccinations out of fear that patients will refuse the vaccine as well as inadequate time during visits to sufficiently explain the benefits of vaccination [5]. However, evidence suggests that when physicians do take the time to discuss the merits of the HPV vaccine, they may positively encourage their patients to receive the vaccine [6,7]. Among 18–26 year olds, trust in the clinician and clinician recommendation were major factors influencing vaccination decisions [6]. In a study of college students, clinician recommendation to receive the HPV vaccine resulted in participants being nearly five times more likely to be vaccinated [7].

Patient eligibility for the HPV vaccine has expanded since U.S. Food and Drug Administration (FDA) approval in 2006. While the vaccine was initially aimed at adolescent and pre-teen girls, recommendation has expanded to now include both male and female patients, starting as young as age 9 and extending through age 45. Current guidelines recommend patients aged 11–12 receive 2 doses and patients aged 15–26 receive 3 vaccine doses [1]. Patients aged 27–45 are advised to engage in shared decision making with their providers to determine whether vaccination against HPV is appropriate based on individual risk factors and values.

While the link between HPV and cervical cancer is widely-known, HPV is also responsible for oropharyngeal, anal, penile, vulvar, and vaginal cancers, which account for over two-thirds of annual HPV-related cancers [1]. Previous studies of medical students have found that many, 59.7% of students, were not aware of the connection between HPV and these other cancers [8,9]. Given the power of clinician recommendation and knowledgeable explanation of the risks and benefits of HPV vaccination, medical education about HPV vaccination is imperative to ensure vaccination rates meet the public health need.

Previous studies have found knowledge of HPV and HPV vaccination increased as medical students progressed through training [8,10]. Medical students who had personally received the HPV vaccine also reported significantly greater willingness to vaccinate adolescents before ages 15–16, as well as greater willingness to discuss vaccination during visits [11]. However, much of this research was conducted prior to expansion of indications for HPV-vaccination beyond adolescent and pre-teen girls. Continued investigation is needed to assess current medical students’ knowledge of HPV vaccination with the ultimate goals of continuing to increase HPV vaccination rates and decrease the incidence of HPV-related cancers.

Furthermore, most of the previous research on medical students’ HPV vaccine knowledge was conducted with allopathic medical students. However, osteopathic and allopathic medical students differ in their medical school curricula and clinical experiences. Both types of students learn scientific, evidence-based practices and treatments at four-year medical training programs that are examined by the same state licensing boards (but using different exams). That said, osteopathic medical practice centers holistic medicine and musculoskeletal manipulative medicine techniques, while allopathic medicine focuses primarily on symptom alleviation and disease treatment through pharmaceutical interventions [12]. Osteopathic medical education places a specific emphasis on preventive medicine and health promotion, such as vaccinations.

The goals of the current study were to address the following, specific research questions: 1) What are the specific knowledge gaps among medical students regarding U.S. Center for Disease Control (CDC) HPV vaccinations guidelines?; 2) What are the demographic and academic correlates of knowledge of HPV vaccination guidelines?; and 3) Are there specific knowledge deficits that remain among medical students in their final year of training?

Methods

Results

A total of 1,592 students indicated interest in participating in this study. Of these interested students, 808 completed the study (response rate = 50.8%). We removed 90 due to incomplete responses. This left a final analytic sample of 718.

Demographics

The largest proportion of the participants in this study were in their first year of training (n = 204, 28.4%) and approximately half were in allopathic medical education programs (n = 382, 53.2%). Over half of participants were White (n = 416, 57.9%), most were heterosexual (n = 604, 84.1%), and approximately two-thirds were cisgender women (n = 450, 62.7%). Regionally, the greatest number of participants were training in the Midwestern U.S. (n = 361, 50.3%). Full demographic information is provided in Table 1. The mean age of participants was 26.3 years (SD = 3.25). Comparison of demographics between allopathic and osteopathic student groups is presented in S1 Table. We also compared demographics of the sample responding to the survey to the demographics of medical students nationally to ensure representation without identifying major discrepancies (S2 Table).

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Table 1. Sample demographics (N = 718).

https://doi.org/10.1371/journal.pone.0280287.t001

Specific cancer diagnoses

Participants were asked to indicate which cancers HPV could cause from a provided list of 12 different cancers- the correct answers were cervical, vaginal/vulvar, anal, and penile cancers (Fig 1). We found that 92.8% of participants correctly indicated that HPV could be a causative etiology for cervical cancer (n = 666). However, we found that lower percentages of participants correctly indicated HPV could be causative for vaginal/vulvar cancer (67.7%, n = 486), anal cancer (63.4%, n = 455), and penile cancer (53.9%, n = 387). We found that 10.7% (n = 77) of participants indicated HPV was a causative etiology for testicular cancer and 10.0% (n = 72) indicated this for colorectal cancer, both of which were incorrect.

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Fig 1. Specific cancer associations with HPV.

Percentage of respondents indicating an association between HPV and each cancer type. Those indicated with an asterisk have a well-documented relationship with HPV. Labels for each bar indicate the number of participants indicating a relationship between HPV and the listed malignancy.

https://doi.org/10.1371/journal.pone.0280287.g001

Multiple choice items

A greater percentage of students in the clinical-phase of training correctly answered six of the eight multiple choice items (Table 2). Specifically, greater percentages of clinical-phase students correctly identified the age at which patients are no longer indicated to receive the HPV vaccine (>45 years; 65.2% vs. 55.6%, χ²[1, N = 718] = 7.05, p = .008), that three HPV vaccine doses were needed to confer protection for a 16 year old patient (88.3% vs. 67.9%, χ²[1, N = 718] = 54.6, p < .001), and that a patient should also be considered for the Hepatitis A vaccine (84.9% vs. 78.6%, χ²[1, N = 718] = 4.54, p = .03) in addition to the HPV vaccine.

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Table 2. Individual item analyses.

https://doi.org/10.1371/journal.pone.0280287.t002

In addition, a greater percentage of clinical-phase students correctly responded that women who have received the HPV vaccine still require pap-smears (98.8% vs. 96.4%, χ²[1, N = 718] = 4.62, p = .03), that the HPV vaccine does not protect against all strains of HPV (98.5% vs. 91.3%, χ²[1, N = 718] = 17.5, p < .001), and that HPV serology is not required prior to receiving the HPV vaccine (88.3% vs. 64.4%, χ²[1, N = 718] = 41.3, p < .001).

Knowledge comparisons

In the univariate ANOVA analyses (Table 3) we found that knowledge of HPV differed based on a participant’s year in training (F[3,714] = 32.6, p < .001). Students in the first year of training reported the lowest knowledge percentage compared to all other years (all p < .001; M = 74.3% [72.6–76.0]) as compared to those in the second (79.4% [77.6–81.3]), third (84.2% [82.6–85.7]) and fourth years (M = 84.6% [82.9–86.2]) of training). We also found that knowledge of the HPV vaccine differed based on the participants’ gender identity (F[2,717] = 3.61, p = .03). Cisgender women (M = 81.8% [80.0–82.2]) reported higher knowledge of the HPV vaccine compared to cisgender men (M = 78.7% [77.1–80.2], p = .03). In the bivariate comparison of knowledge between allopathic (M = 81.3% [80.1–82.5]) and osteopathic (M = 79.0% [77.6–80.4]) medical students, we found that allopathic students reported a higher average knowledge score (t[716] = 2.53, p = .01).

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Table 3. HPV knowledge assessment scores.

https://doi.org/10.1371/journal.pone.0280287.t003

In the adjusted analyses, the effect of participants’ year in training was maintained (F[3,713] = 32.4, p < .001). First-year students reported lower knowledge compared to all other years (all p < .001). The effect of participant gender identity was also maintained (F[2,713] = 5.57, p < .001) with cisgender women reporting higher knowledge compared to cisgender men. No additional effects of demographic or training characteristics were identified on HPV knowledge (Table 3).

Discussion

HPV-associated cancers continue to cause mortality and morbidity in the U.S. despite wide availability of effective prevention with the HPV vaccine. Clinicians play a key role in ensuring that HPV vaccination reaches all eligible patients [14]. Medical education about the HPV vaccine is crucial so medical students can identify vaccine candidates, educate their patients about the risks and benefits, and respond to patient questions. To the best of our knowledge, this is the first multi-regional and multi-institutional study of both allopathic and osteopathic medical students’ knowledge of HPV vaccination guidelines. The current findings may be used to improve medical education about HPV-associated cancers and HPV vaccination.

Most participants (92.8%) correctly identified the connection between HPV and cervical cancer. However, smaller percentages correctly identified the link between HPV and vaginal/vulvar, anal, and penile cancers, echoing previous work [8,9]. Importantly, this previous study grouped penile and vaginal/vulvar cancer as genital cancers whereas we separated these two diagnoses. In our study, two-thirds of students linked HPV to vaginal/vulvar cancers, whereas just over half linked HPV to penile cancers. This suggests difficulty identifying HPV-related cancers in the male genital tract that both reflects the predominant societal narrative that so closely links HPV to women’s health and suggests need for concentrated educational efforts that focus specifically on HPV and anal/penile cancers [15,16].

The burden of HPV infection and HPV-related disease among men who have sex with men (MSM) remains disproportionate, and recent work has found that HPV vaccination was more common among MSM who were using HIV PrEP compared to those who were not [17]. While this is encouraging, it suggests there is a significant need to broadly improve HPV vaccination among all patients who are at risk, not just those who are already engage in preventive sexual healthcare. Research conducted among heterosexual patients found only 11.5% had received one dose of the HPV vaccination, underscoring the importance of education to broadly improve uptake of the HPV vaccine [18].

Broadly, knowledge of HPV vaccination guidelines improved with increasing years of training as second, third, and fourth-year medical students performed better than first-year students. This trend in increasing knowledge is intuitive given the progressive concentration on clinical medicine as training progresses, and these results are consistent with those from prior studies [8,10]. We found that the only questions without difference between year of training were those answered incorrectly by most students in either group. Specifically, we found that fewer than half (33.0%) of the students in this study, even those in the clinical years of training (36.6%), correctly identified patients could begin receiving the HPV vaccine at age 9. Additionally, only 48.1% of participants, including 48.0% of those in clinical training, were correct in identifying three HPV vaccine doses conferred full protection for a 16-year-old patient. The persistence of incorrect knowledge in this later phase of training suggests the need for additional training about eligibility for the HPV vaccine.

These knowledge gaps thus present an opportunity for educational intervention [19–21]. There is a demonstrable benefit that increased training among first- and second-year medical students can improve comfort and knowledge in counseling on HPV vaccination [22,23]. A follow-up study to the workshop curricula that was implemented by Evans et al. demonstrated that a year and a half later, these students retained their knowledge and continued to better advocate for the vaccine than their peers who did not participate in the workshop, and these students were also able to integrate their knowledge into increasing HPV vaccination rates in student-run free clinics [22,24].

We found several interesting demographic trends. Greater HPV knowledge was demonstrated among cisgender women as compared to cisgender men, without difference based on sexual orientation, region, or type of training. Women remain more likely to have received the HPV vaccine, and this first-hand experience is related to their greater current knowledge and future discussions of the vaccine with patients [11]. To standardize provider knowledge and to ensure that all students possess a similar foundation of knowledge related to HPV vaccination, school-wide initiatives are necessary. Even a single lecture by an expert can improve attitudes with HPV vaccination, especially in students who themselves did not have it [24–26]. Other curricula have had similar success, including a role-playing workshop conducted with 28 medical students and residents that showed improved participant knowledge, comfort, and confidence discussing the HPV vaccine [21,27,28].

Conclusion

Increased knowledge about HPV-related cancers and HPV vaccination as well as confidence discussing the HPV vaccine can positively impact its uptake and continue to decrease the prevalence of HPV-related cancers. This begins with giving medical students a strong foundation on the effects of HPV infection, the benefits of vaccination, and when/to whom it should be administered. While many studies have focused on the general knowledge base of medical students in specific regions and at specific institutions, we demonstrate multi-regional osteopathic and allopathic knowledge of HPV vaccination rationale and guidelines, highlighting the gaps in knowledge where educational interventions are needed. We found deficits in medical students’ ability to link HPV to vaginal, vulvar, anal, and especially penile cancers, including markedly decreased knowledge in the pre-clinical years. The focus of future work should now shift to the development and implementation of curricular interventions. Students could greatly benefit from lectures and workshops dedicated specifically to non-cervical HPV-related cancers and how to discuss the HPV vaccine with patients. With a new cohort of physicians prepared to address HPV vaccination, we may more successfully decrease the prevalence of deaths from cancers preventable with the HPV vaccine.

Supporting information

Acknowledgments

The authors would like to thank all of the University administrators who assisted with distribution of study information as well as all of the students who took the time to participate in this study.