ABSTRACT
Provider recommendation is a primary reason for patient uptake of the human papillomavirus (HPV) vaccine. Most provider-focused educational interventions are focused on physicians, even though nurses are also important sources of vaccine-related information for their patients. This study examined whether a HPV educational intervention could improve nursing students’ HPV knowledge, beliefs, and comfort with counseling. The same lecture on HPV and HPV vaccination was given to both medical and nursing students. To determine the effects of the lecture, students were asked to complete identical pre- and post-lecture tests with questions on demographics, knowledge, attitudes, and comfort with counseling on the HPV vaccine. Pre- and post-lecture test scores were compared between nursing and medical students to assess whether there were differences in pre-lecture test scores and/or changes in post-lecture test scores. On the pre-lecture tests, fewer nursing students responded correctly to knowledge questions, indicated positive attitudes or comfort with counseling about the HPV vaccine compared to medical students. However, similar frequencies of nursing and medical students responded correctly to knowledge questions and indicated a positive attitude, as well as a high comfort level with counseling on the post-lecture tests. Study results show that integrating lectures in a nursing program curriculum could be a feasible way to increase students’ HPV knowledge. Having health-care providers with similar levels of knowledge, attitudes, and comfort with counseling on HPV vaccination is ideal, as all share the responsibility of recommending the vaccine to patients.
Introduction
The Advisory Committee on Immunization Practices (ACIP) recommends routine administration of the human papillomavirus (HPV) vaccine to 11–12 years olds, although it can be given to individuals as young as 9 or as old as 45 years of age.Citation1 Models predicting the long-term impact of HPV vaccination in high-income countries determined that an 80% vaccination coverage of 12-year-old girls and boys over time will generate herd effects strong enough to substantially reduce or even eliminate vaccine-related HPV types in the population.Citation2 Despite these predictions and the availability of a vaccine since 2006,Citation3,Citation4 HPV vaccination rates in the United States (US) remain below 80%. In 2018, the Centers for Disease Control (CDC) estimated that only 51.1% of 13–17 year olds in the US were up to date with the HPV vaccine series, despite there being no cost for the vaccine, as it is covered by the Vaccines For Children program among uninsured patients.Citation5 Barriers to HPV vaccine uptake need to be addressed to achieve higher vaccination rates in the US.
Prior studies which examined reasons cited by parents for deciding to have their child vaccinated against HPV found that the most frequent reason was that their child’s provider recommended it.Citation6,Citation7 In fact, provider recommendation has been found to be the most important factor in awareness of the vaccine among parents and vaccine uptake among patients, regardless of patient race/ethnicity.Citation8–12 Many studies have focused on physician recommendation, but nurses are also an important source of healthcare information as they are increasingly utilized to provide primary healthcare and advice to patients in the US.Citation13 Not only are nurses ubiquitous in the clinical setting and crucial to discussing vaccines with patients before they see a physician or during the vaccination process, nurse practitioners often provide primary care directly to patients in a clinical setting and are able to prescribe the vaccine. Moreover, nurses providing care in schools may play a strong role in promoting HPV vaccination.Citation14–16 However, nurses may not be completely informed about vaccines that they are expected to promote. Focus groups of nurses found that they did not know enough about the flu vaccine to promote it actively, especially among those who did not get it themselves.Citation17 Therefore, informing these professionals about the HPV vaccine and providing them with strategies is an important undertaking.
For any provider to feel comfortable with recommending HPV vaccination to parents of adolescent patients, they must have access to up-to-date information on the vaccine. Our research team found that medical students who attended a single lecture on HPV vaccination increased their baseline knowledge and improved their readiness to counsel.Citation18 Similar results were observed in two other studies that investigated the impact of recently developed educational modules on HPV biology and vaccination for medical students.Citation19,Citation20 This suggests that interventions to increase knowledge about HPV may be appropriate for medical students, especially since their curriculum is set and difficult to change.
It is equally important to develop and test educational interventions on nursing students, as they have a strong influence on patients and their families who often look to them for guidance on care.Citation21 Moreover, past studies have shown that parents view nurses as sources of information on vaccines for children.Citation22,Citation23 While surveys examining baseline knowledge of HPV and vaccination guidelines among nursing students have identified knowledge gaps,Citation24–27 no studies have formally assessed baseline knowledge and readiness to counsel of nursing students before and after an educational intervention.
The purpose of this study was to examine baseline knowledge and attitudes of HPV vaccination among nursing students and determine if the educational intervention we tested on medical students was as effective when incorporated in the curriculum of a Bachelor of Science in Nursing (BSN) program. Pre- and post-test scores of the nursing students were then compared to those of medical students to assess whether there was a difference in baseline scores or changes in scores after attending the educational lecture.
Material and methods
To examine whether short, structured presentations can improve HPV-related knowledge, attitudes, and comfort with counseling among nursing students, we used a quasi-experimental pre-test/post-test design with identical surveys administered to all willing participants before and after the lectures. As our research recently showed that this same intervention improved knowledge, attitudes, and comfort with counseling among medical students,Citation18 we compared responses between nursing students and medical students as well as examined changes in their scores before and after the lecture. Between May 2016 and March 2020, the first author (ABB) conducted a total of 5 presentations on HPV and HPV vaccination to The University of Texas Medical Branch (UTMB) undergraduate nursing students during their pediatrics course and to UTMB medical students 23 times, in smaller groups, during their core clerkship in obstetrics and gynecology. These rotations occurred during the last half of the overall curriculum in both the medical and nursing programs. Although medical students had several more sessions than nursing students due to smaller groups rotating through their clerkships throughout the year, the lectures occurred within the same time period (May 2016-March 2020) for both groups. No student participated in the lecture more than one time. Lectures consisted of 45 minutes of a PowerPoint presentation, with questions following. Each lecture included information that medical practitioners should know, such as dosing schedules, safety, and efficacy of the vaccine. Even though these lectures were part of the required curriculum for both nursing and medical student programs, students were not required to participate in the study. Participants received a small gift, such as a lunch sack or a flash drive valued at ≤ 5, USD as compensation for their time if they completed both study surveys directly preceding and directly after the lecture in the room where it was delivered. All methods described herein were approved by the UTMB Institutional Review Board.
To determine the effect of the presentations on knowledge, beliefs and attitudes, and comfort with counseling about the HPV vaccine, we asked lecture attendees to take a one-page anonymous, voluntary pencil and paper survey with questions about basic demographics, 4 HPV knowledge questions, and 21 questions about attitudes and comfort with counseling patients regarding HPV vaccination immediately before the presentation. Details about the survey were previously published.Citation18 Survey questions were piloted before surveys were administered, and are presented in tables as they were shown in the survey. Responses to knowledge questions were either “true” or “false.” Comfort with counseling and attitude questions consisted of 5 Likert scale response categories: “strongly agree,” “agree,” “neutral,” “disagree,” or “strongly disagree.” Identical post-surveys were administered immediately at the end of the presentation and scored identically to the pre-surveys. Each pre- and post-lecture survey took approximately 5–10 minutes to complete. Unique IDs were used to pair a participant’s pre- and post-lecture survey responses.
Participants’ data were excluded from this study if they did not return both pre- and post-lecture surveys. Other students or professionals may have participated, but we only included survey responses from those who indicated they were either a nursing or medical student, as one of the goals of this study was to determine whether nursing students gained as much benefit from the program as medical students.
For basic demographics, participants responded to questions about their age, gender, race/ethnicity, and whether they had received at least one dose of the HPV vaccine. Knowledge questions were scored as either correct or incorrect. The frequency of correct responses was compared between nursing and medical students for both the pre- and post-lecture surveys to evaluate associations between student training and correct responses.
Items that focused on attitudes and beliefs were evaluated for improvement, which was defined as changing from “neutral,” “disagree,” or “strongly disagree” for each item on the pre-lecture survey to either “agree” or “strongly agree” on the post-lecture survey. Improvement was also defined as those who changed a “disagree” or “strongly disagree” from the pre-lecture survey to “neutral” on the post-lecture survey. Improvement was coded as a 1 and all other possibilities were coded as a 0. One item, “The HPV vaccine should not be offered to patients until they are sexually active,” was reverse coded, with changes to “disagree” or “strongly disagree” considered improvement. Changes from “strongly agree” or “agree” to “neutral” were also coded as improvement on the reverse scored item.
Each question related to comfort with counseling was evaluated for improvement as well. Improvement was considered a change from “neutral,” “disagree,” or “strongly disagree” for each item on the pre-lecture survey to either “agree” or “strongly agree” on the post-lecture survey. Improvement was also defined as those who changed a “disagree” or “strongly disagree” from the pre-lecture survey to “neutral” on the post-lecture survey. Improvement was coded as a 1 and all other possibilities were coded as a 0. The item, “I am uncomfortable recommending a vaccine against sexually transmitted infections,” was reverse coded so that “disagree” or “strongly disagree” were considered improvement. Changes from “strongly agree” or “agree” to “neutral” were also coded as improvement on reverse-scored items. The sub-items associated with the statement, “I need the following to be more comfortable with counseling patients/parents,” were also reverse coded. For the five sub-items that were associated with that statement, a change from “neutral,” “agree,” or “strongly agree” on the pre-lecture survey to “disagree” or “strongly disagree” on the post-lecture survey was considered an improvement. Improvement was coded as a 1 and any other possibilities were coded as a 0.
Statistical analyses
Bivariate comparisons were performed using chi-square tests. These were performed to compare characteristics of medical and nursing students. Chi-square tests were also used to examine the differences in frequency of correct responses to knowledge questions, improvement in attitudes and beliefs, and improvement in comfort with counseling between nursing and medical students. Participants with missing data were included in the study but were excluded from the analyses for the items with missing values. P-values ≤0.05 were considered significant. Percent increase was calculated among nursing students by dividing the difference of correct response frequencies between the pre-lecture survey and post-lecture survey, then dividing by the frequency of correct responses on the pre-lecture survey. Multivariable binary logistic regression analyses were conducted to examine the association of improvement in attitudes and beliefs as well as in comfort with counseling with student type (nursing versus medical) after controlling for HPV vaccination status. We controlled for HPV vaccine status because it is possible that vaccinated students would have a different view on HPV vaccination before and after the lecture compared to unvaccinated students.Citation27–29 Participants with missing HPV vaccination data were excluded from the logistic regression models. All statistical analyses were conducted using SAS software 9.4® (Cary, North Carolina).
Results
Of the 973 presentation attendees, we excluded data on 73 individuals: 40 non-students, 13 with missing information about their student status, 13 medical students who did not complete both surveys, and 7 nursing students who did not complete both surveys. After these exclusions, 900 students (96%) were included in this study. Of those, 512 were medical students and 388 were nursing students. Most participants were younger than 30 years old (93%). Therefore, most were in the age cohort that would have been eligible to receive the vaccine after it was recommended in the US. The rate of self-reported HPV vaccination was 61%, with 49% of the medical students reporting vaccine initiation compared to 76% of the nursing students ().
Table 1. Basic characteristics of students who completed pre- and post-lecture surveys (N = 900)
Knowledge
Overall, more participants answered knowledge questions correctly after the lecture was given (). In particular, a high frequency of nursing students improved their knowledge, with a 176% relative change (342–124 = 218 absolute change) to correct responses for contraindications, 479% relative change (324–56 = 268 absolute change) to correct responses about HPV testing for sexually active women before vaccination, and 146% relative change (366–149 = 217 absolute change) to correct responses for whether dosing needs to be restarted after a 6 month gap. The frequency of nursing students responding correctly to CDC recommended guidelines for patients ≥15 years old was similar to that of medical students in both pre- and post-lecture surveys (p > .05). However, after only 39% of nursing students responded correctly on the pre-lecture survey for recommended dosing of patients ≥15 years old, 67% of nursing students responded correctly after the lecture for the same item. The proportion of nursing students with correct scores at baseline (i.e., pre-lecture) was lower than medical students’ baseline knowledge for: contraindications to HPV vaccination, testing before vaccination, and whether to restart the series if a patient has a gap of greater than 6 months between doses. However, the frequency of correct responses on the post-lecture surveys was similar for all knowledge questions between nursing and medical students.
Table 2. Association between student knowledge and time of test (N = 900)
Comfort with counseling
When comparing the changes in pre- and post-lecture values for comfort with counseling, a similar frequency of nursing students improved between the pre- and the post-lecture surveys compared to medical students for all but five items (). There was a 50% change in the frequency of nursing students who felt more comfortable with counseling patients who came into the clinic with other problems. A higher frequency of nursing students (34.9%) compared to medical students (20.8%) improved their willingness to discuss HPV vaccination when patients come in for other problems (p < .001). Nursing students did not improve their scores as much as medical students on two statements testing comfort with counseling. A large proportion of nursing students (43.2%) still felt they needed additional education to be more comfortable counseling patients about HPV vaccination. Fewer nursing students felt they did not need more safety data on HPV vaccination (p < .01) to be comfortable with counseling patients and parents about HPV vaccination than medical students. More nursing students than medical students increased their comfort in recommending the HPV vaccine to 13–17 year olds (p < .001), with 91% of nursing students feeling comfortable with offering the vaccine to this age group after the lecture compared to 63% before the lecture. Finally, a higher proportion of nursing students disagreed that they were uncomfortable recommending a vaccine against sexually transmitted infections compared to medical students (p < .05).
Table 3. Improvement in comfort with counseling patients on the human papillomavirus (HPV) vaccine after an educational lecture (N = 900)
After controlling for vaccination status, several items for comfort with counseling still showed variations in improvement between nursing and medical students, and one item became significant (). Nursing students had higher odds (OR: 2.17, 95% CI: 1.53–3.07) of changing to “agree” or “strongly agree” than medical students regarding, “willing to discuss HPV vaccination when patients come in for other problems.” However, nursing students were less likely to improve being comfortable with counseling without more education on HPV vaccination and more safety data on HPV vaccination after controlling for HPV vaccination status (OR: 0.45, 95% CI: 0.34–0.62). After the education session, nursing students were more likely to improve their comfort with offering the HPV vaccine to 11–12 year old (OR 1.65, 95% CI: 1.21–2.26) and 13–17 year old patients (OR 2.25, 95% CI: 1.59–2.93) compared to medical students after controlling for HPV vaccination status.
Beliefs and attitude
Improvements in beliefs and attitudes occurred among nursing students, but was not as notable as the increases in comfort with counseling patients. Overall when comparing changes between the pre- and post-lecture tests, nursing students had more positive beliefs and attitudes on HPV vaccination (). Nursing students experienced a strong increase in improved beliefs and attitudes after the lecture, with an 18% increase in those who agreed that the vaccine provides more benefit than harm from pre-lecture to post-lecture survey. Nursing students had more than 3 times the odds of a more informed belief about the HPV vaccine providing more benefits than harm after the brief lecture, even after controlling for HPV vaccination status compared to medical students (OR 3.17, 95% CI: 1.91–5.24). Nursing students had 2 times the odds or more of having a more positive attitudes over medical students for the following items: the HPV vaccine should not be offered to patients until they are sexually active (OR 1.98, 95% CI 1.35–2.89), the HPV vaccine saves lives (OR 2.67, 95% CI: 1.70–4.25), and that they expect to see benefits from HPV vaccination in their patient population (OR 3.00, 95% CI: 1.83–3.33). Finally, nursing students had almost twice the odds of developing a more positive attitude about HPV posing a public health threat compared to medical students (OR 1.98, 95% CI: 1.18–3.33). The stronger improvement seen among nursing students is at least partially due to lower baseline positive attitudes and informed beliefs about the vaccine before the lecture.
Table 4. Changes in beliefs and attitudes among medical and nursing students (N = 900)
Discussion
We found that nursing students had low baseline scores compared to medical students with regard to HPV knowledge. This is in agreement with prior studiesCitation30,Citation31 and has been attributed to variations in program curriculum.Citation30,Citation32 Within programs, students further along in their training had higher levels of HPV knowledge.Citation27,Citation33,Citation34 For example, in countries with 4-year nursing programs, students in their 3rd or 4th year of study gave more correct responses to questions on HPV compared to students in their 1st year.Citation27,Citation33,Citation34 Nursing students were in their 3rd semester of a bachelor’s degree program consisting of 4 semesters when they participated in the lecture. This program requires completion of 60 hours of prerequisite courses before enrollment. The medical students were in their 3rd year of a graduate program and thus had already completed 2 years of health-related education. Thus, it is possible that additional years of education or the material taught in the respective programs are reasons for the differences in baseline knowledge we observed.
In particular, we found that fewer nursing students scored correctly on items related to administration of the vaccine, such as contraindications. These findings agree with those from previous surveys used to determine HPV knowledge among nursing students.Citation25,Citation27,Citation34 While questions testing HPV vaccination knowledge varied, overall results indicated that nursing students were not familiar with HPV vaccination guidelines.Citation25,Citation27,Citation34 For example, more than half of the nursing students in several studies did not know the eligible age range for the vaccineCitation25,Citation27,Citation34 or the number of doses required to complete the vaccine series.Citation27,Citation34 These results demonstrate the importance of including information on HPV vaccination in nursing student curriculum.
We also observed that fewer nursing students reported positive attitudes than medical students before the short lecture. This finding is surprising, as a higher proportion of nursing students received the HPV vaccine and were female, thus in a group that has been more highly targeted for vaccination. However, lower positive attitudes about the HPV vaccine among nursing students agrees with prior studies which have demonstrated that many nurses appear to have more safety concerns about vaccination in general,Citation31,Citation35 and HPV vaccination in particular.Citation35–37 For example, compared to other healthcare professional students, nursing students were the least confident when asked about the link between the measles, mumps, rubella (MMR) vaccine and autism and more felt that the current immunization schedule for children could overwhelm their immune system.Citation31 In a survey on HPV vaccination, more nurses (32.8%) than physicians (20%) felt that side effects were a barrier to vaccine uptake.Citation38 Greater safety concerns over the HPV vaccine may be due to the fact that it is a recently developed vaccine, as nurses or nursing students had lower levels of concern on the safety of vaccines with a longer history of use in the public, such as vaccines for polio.Citation35,Citation37 Thus, educating nurse providers on the safety of HPV vaccination is critical.
In our study, many of the nursing students indicated a much lower comfort level with counseling than medical students prior to the lecture but showed great improvement after the brief intervention. Although they did not end up with scores as high as the medical students, they were very close. This intervention helped close the gap. After the lecture, some nursing students desired additional information on the vaccine and its safety. Although nursing curricula generally include information about vaccinations, this information and opportunities to increase their immunization knowledge and competency could be provided in a variety of ways. Continuing education through professional organizations for nurses could offer opportunities to expand knowledge about the HPV vaccine. Including nursing students or registered nurses in training on vaccination that is regularly offered to medical students or physicians could provide opportunities to increase their knowledge on the topic. In addition, nurses could take an online module to supplement their education as this was successful in addressing deficiencies in several areas of HPV epidemiology and vaccination among school nurses in Missouri.Citation39 In addition to educational lectures, students could be given materials to serve as aids while counseling patients. After attending educational lectures, oral health professionals were given toolkits consisting of brochures, posters, talking-tips sheet, and tear-off pads with information about HPV.Citation40 A majority (67.5%) of the providers felt better prepared and more comfortable talking to their patients about the importance of HPV vaccination in cancer prevention when using the toolkits.
With distance education taking an increased role, it has been questioned whether lectures are effective enough.Citation41 We showed they can play a role. Integrating lectures about HPV into a course or program curriculum could be an easy, effective way to increase HPV knowledge in nursing schools. Nursing students have reported that college courses are a common source of information on HPV.Citation24,Citation32 Students with higher levels of knowledge often have positive attitudes toward vaccination.Citation26,Citation36,Citation42 For example, a study in Italy found that the 63% of nursing students who had heard about HPV infection during their degree program were more likely to know the risks of HPV infection and the benefits of vaccination, which contributed to a positive attitude about the vaccine and willingness to recommend the HPV vaccine to patients in the future.Citation26
An advantage of the intervention we described is that it is appropriate for interprofessional education (IPE), even among those with lower baseline HPV-related knowledge, beliefs, and attitudes. Since patient care often involves multiple healthcare providers, educational programs for these professions have IPE components and many accrediting agencies require them.Citation43 IPE is one way to help promote consistency in patient care. For example, IPE has been successful in training providers how to instruct patients on the proper technique for using an inhaler.Citation44,Citation45 Having health-care providers with similar levels of knowledge, beliefs, and attitudes on HPV vaccination is ideal, as all have the shared responsibility of recommending this vaccine to patients. In fact, parents who received consistent recommendations for HPV vaccination from multiple members of their child’s healthcare team were 2.3 times more likely to initiate HPV vaccination compared to parents who received recommendation from a single member.Citation46
Strengths and limitations
One strength of this study is that it was conducted on a large sample of nursing and medical students. We were able to compare their responses before and after the intervention. However, this study may not be generalizable, as students all attended the same institution. Moreover, we did not assess whether this program had longer-term benefits. The post-lecture survey indicates the immediate reaction to the learning material but does not show long-term retention or effect on attitudes and beliefs. Longitudinal studies that examine the effect of education on HPV vaccination uptake would help identify whether short interventions are adequate to improve uptake and completion, or whether longer more sustained interventions are needed. Further, it would be helpful to know whether interventions conducted during nursing or medical school training are as effective as providing training as part of continuing education, and how using technology to provide training could be effectively utilized. Future studies should include validation of the questions in the instrument beyond piloting among the focus group and evaluate long-term outcomes. This study was conducted as part of a larger effort to vaccinate eligible males and females in Southeast Texas. In addition to educating students, health care providers were educated, and patient navigators were at many clinics that would have hosted medical students for rotations, which may have influenced their knowledge and attitudes about the vaccine differently from nursing students at the university. Further, greater acceptance of the HPV vaccine during the study’s duration may have influenced beliefs and attitudes across time, as well.
Conclusion
Overall, we found that a single lecture could help nursing students improve their knowledge, attitudes and comfort with counseling about the HPV vaccine. It is important to identify easy ways to improve awareness and the practice of nursing providers, as they have a large sphere of influence. They meet with more patients and are trusted by family and friends for health-related information.Citation21,Citation37 Programs aimed at educating nurses could improve HPV vaccination within their communities, as other interventions, such as mandating the HPV vaccine at the state level, are not highly effective at elevating population HPV vaccination rates.Citation47–49 Although increasing legislation to improve HPV vaccine rates may be helpful, patients often feel that getting a recommendation from their health care provider is very important in helping them make decisions about their children’s health care. Therefore, increased education for nurses about controversial vaccines could help prepare them to address questions from patients.
Disclosure of potential conflicts of interest
The authors report no conflicts of interest.
Acknowledgments
Financial support for this study was provided by 3 prevention grants from the Cancer Prevention & Research Institute of Texas (CPRIT PP180012, PP160010, and PP190004, Berenson PD). This study was conducted with the support of the Institute for Translational Sciences at The University of Texas Medical Branch supported in part by a Clinical and Translational Science Award (UL1TR001439) from the National Center for Advancing Translational Sciences (NCATS), National Institutes of Health. The content is solely the responsibility of the authors and does not necessarily represent the official views of CPRIT or NCATS.
Additional information
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References
- Meites E, Szilagyi PG, Chesson HW, Unger ER, Romero JR, Markowitz LE. Human papillomavirus vaccination for adults: updated recommendations of the advisory committee on immunization practices. MMWR Morb Mortal Wkly Rep. 2019;68(32):698–702. doi:10.15585/mmwr.mm6832a3.
- Brisson M, Benard É, Drolet M, Bogaards JA, Baussano I, Vanska 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 Public Health. 2016;1(1):e8–e17. doi:10.1016/S2468-2667(16)30001-9.
- FDA licenses new vaccine for prevention of cervical cancer and other diseases in females caused by human papillomavirus [press release]. US Food and Drug Administration June 8, 2006.
- Markowitz LE, Dunne EF, Saraiya M, Lawson HW, Chesson H, Unger ER. Quadrivalent human papillomavirus vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep. 2007;56(RR–2):1–24.
- Walker TY, Elams-Evans LD, Yankey D, Markowitz LE, Williams CL, Fredua B, Singleton JA, Stokley S. National, regional, state, and selected local area vaccination coverage among adolescents aged 13-17 years - United States, 2018 Centers for Disease Control and Prevention August 23, 2019.
- Dorell C, Yankey D, Kennedy A, Stokley S. Factors that influence parental vaccination decisions for adolescents, 13 to 17 years old: National Immunization Survey-Teen, 2010. Clin Pediatr (Phila). 2013;52(2):162–70. doi:10.1177/0009922812468208.
- Gargano LM, Herbert NL, Painter JE, Sales JM, Morfaw C, Rask K, Murray D, DiClemente RJ, Hughes JM. Impact of a physician recommendation and parental immunization attitudes on receipt or intention to receive adolescent vaccines. Hum Vaccin Immunother. 2013;9(12):2627–33. doi:10.4161/hv.25823.
- Rosenthal SL, Weiss TW, Zimet GD, Ma L, Good MB, Vichnin MD. Predictors of HPV vaccine uptake among women aged 19-26: importance of a physician’s recommendation. Vaccine. 2011;29(5):890–95. doi:10.1016/j.vaccine.2009.12.063.
- Lau M, Lin H, Flores G. Factors associated with human papillomavirus vaccine-series initiation and healthcare provider recommendation in US adolescent females: 2007 National Survey of Children’s Health. Vaccine. 2012;30(20):3112–18. doi:10.1016/j.vaccine.2012.02.034.
- Ylitalo KR, Lee H, Mehta NK. Health care provider recommendation, human papillomavirus vaccination, and race/ethnicity in the US National Immunization Survey. Am J Public Health. 2013;103(1):164–69. doi:10.2105/AJPH.2011.300600.
- Rahman M, Laz TH, McGrath CJ, Berenson AB. Provider recommendation mediates the relationship between parental human papillomavirus (HPV) vaccine awareness and HPV vaccine initiation and completion among 13- to 17-year-old U.S. adolescent children. Clin Pediatr (Phila). 2015;54(4):371–75. doi:10.1177/0009922814551135.
- Gilkey MB, Calo WA, Moss JL, Shah PD, Marciniak MW, Brewer NT. Provider communication and HPV vaccination: the impact of recommendation quality. Vaccine. 2016;34(9):1187–92. doi:10.1016/j.vaccine.2016.01.023.
- Laurant M, van der Biezen M, Wijers N, Watananirun K, Kontopantelis E, van Vught AJ. Nurses as substitutes for doctors in primary care. Cochrane Database Syst Rev. 2018;7(7):CD001271–CD. doi:10.1002/14651858.CD001271.pub3.
- Rosen BL, Ashwood D, Richardson GB. School Nurses’ professional practice in the HPV vaccine decision-making process. J Sch Nurs. 2016;32:138–48. doi:10.1177/1059840515583312.
- Boyce T, Holmes A. Addressing health inequalities in the delivery of the human papillomavirus vaccination programme: examining the role of the school nurse. Plos One. 2012;7:e43416. doi:10.1371/journal.pone.0043416.
- Rosen BL, Goodson P, Thompson B, Wilson KL. School nurses’ knowledge, attitudes, perceptions of role as opinion leader, and professional practice regarding human papillomavirus vaccine for youth. J Sch Health. 2015;85:73–81. doi:10.1111/josh.12229.
- Willis BC, Wortley P. Nurses’ attitudes and beliefs about influenza and the influenza vaccine: A summary of focus groups in Alabama and Michigan. Am J Infect Control. 2007;35:20–24. doi:10.1016/j.ajic.2006.07.009.
- Berenson AB, Hirth JM, Fuchs EL, Chang M, Rupp RE. An educational intervention to improve attitudes regarding HPV vaccination and comfort with counseling among US medical students. Hum Vaccin Immunother. 2019:1–6. doi:10.1080/21645515.2019.1692558.
- Schnaith AM, Evans EM, Vogt C, Tinsay AM, Schmidt TE, Tessier KM, Erickson BK. An innovative medical school curriculum to address human papillomavirus vaccine hesitancy. Vaccine. 2018;36(26):3830–35. doi:10.1016/j.vaccine.2018.05.014.
- Wiley R, Shelal Z, Bernard C, Urbauer D, Toy E, Ramondetta L. Human papillomavirus: from basic science to clinical management for preclinical medical students. MedEdPORTAL. 2018;14(1):10787. doi:10.15766/mep_2374-8265.10787.
- RegisteredNursing.org. The importance of the nurse-patient relationship for patient care 2019 [accessed 2019 July 6]. https://www.registerednursing.org/importance-nurse-patient-relationship-care/.
- Austvoll-Dahlgren A, Helseth S. What informs parents’ decision-making about childhood vaccinations? J Adv Nurs. 2010;66(11):2421–30. doi:10.1111/j.1365-2648.2010.05403.x.
- Hill MC, Cox CL. Influencing factors in MMR immunisation decision making. Br J Nurs. 2013;22(15):893–98. doi:10.12968/bjon.2013.22.15.893.
- Schmotzer GL, Reding KW. Knowledge and beliefs regarding human papillomavirus among college nursing students at a minority-serving institution. J Community Health. 2013;38(6):1106–14. doi:10.1007/s10900-013-9720-y.
- Topan A, Ozturk O, Eroglu H, Bahadir O, Harma M, Harma MI. Knowledge level of working and student nurses on cervical cancer and human papilloma virus vaccines. Asian Pac J Cancer Prev. 2015;16(6):2515–19. doi:10.7314/apjcp.2015.16.6.2515.
- Pelullo CP, Esposito MR, Di Giuseppe G. Human papillomavirus infection and vaccination: knowledge and attitudes among nursing students in Italy. Int J Environ Res Public Health. 2019;16(10):1770. doi:10.3390/ijerph16101770.
- Villanueva S, Mosteiro-Miguens DG, Dominguez-Martis EM, Lopez-Ares D, Novio S. Knowledge, attitudes, and intentions towards human papillomavirus vaccination among nursing students in Spain. Int J Environ Res Public Health. 2019;16(22):4507. doi:10.3390/ijerph16224507.
- Afonso NM, Kavanagh MJ, Swanberg SM, Schulte JM, Wunderlich T, Lucia VC. Will they lead by example? Assessment of vaccination rates and attitudes to human papilloma virus in millennial medical students. BMC Public Health. 2017;17(1):35. doi:10.1186/s12889-016-3969-x.
- Berenson AB, Hirth JM, Fuchs EL. US medical students’ willingness to offer the HPV vaccine by vaccination status. Vaccine. 2017;35(9):1212–15. doi:10.1016/j.vaccine.2017.01.028.
- Pelly LP, Pierrynowski MacDougall DM, Halperin BA, Strang RA, Bowles SK, Baxendale DM, McNeil SA. THE VAXED PROJECT: an Assessment of Immunization Education in Canadian Health Professional Programs. BMC Med Educ. 2010;10(1):86. doi:10.1186/1472-6920-10-86.
- Dybsand LL, Hall KJ, Carson PJ. Immunization attitudes, opinions, and knowledge of healthcare professional students at two Midwestern universities in the United States. BMC Med Educ. 2019;19(1):242. doi:10.1186/s12909-019-1678-8.
- Shetty S, Prabhu S, Shetty V, Shetty AK. Knowledge, attitudes and factors associated with acceptability of human papillomavirus vaccination among undergraduate medical, dental and nursing students in South India. Hum Vaccin Immunother. 2019;15(7–8):1656–65. doi:10.1080/21645515.2019.1565260.
- Cirilo CA, Barbosa AS, Zambrano E. Level of behavior and knowledge concerning human papillomavirus among university students of a nursing college. Rev Soc Bras Med Trop. 2010;43(4):362–66. doi:10.1590/s0037-86822010000400005.
- Bal-Yılmaz H, Koniak-Griffin D. Knowledge, behaviors, and attitudes about human papilloma virus among nursing students in Izmir, Turkey. J Cancer Educ. 2018;33(4):814–20. doi:10.1007/s13187-017-1163-1.
- Wilson R, Zaytseva A, Bocquier A, Nokri A, Fressard L, Chamboredon P, Carbonaro C, Bernardi S, Dubé E, Verger P. Vaccine hesitancy and self-vaccination behaviors among nurses in southeastern France. Vaccine. 2020;38(5):1144–51. doi:10.1016/j.vaccine.2019.11.018.
- Papagiannis D, Rachiotis G, Symvoulakis EK, Daponte A, Grivea IN, Syrogiannopoulos GA, Hadjichristodoulou C. Vaccination against human papillomavirus among 865 female students from the health professions in central Greece: a questionnaire-based cross-sectional study. J Multidiscip Healthc. 2013;6:435–39. doi:10.2147/JMDH.S49558.
- Wilson KL, Avery JS, Slack J. Nursing students’ perceptions and beliefs about immunizations: A descriptive study. Nurse Educ Today. 2020;92:104491. doi:10.1016/j.nedt.2020.104491.
- Cheung T, Lau JTF, Wang JZ, Mo P, Siu CK, Chan RTH, Ho JYS. The acceptability of HPV vaccines and perceptions of vaccination against HPV among physicians and nurses in Hong Kong. Int J Environ Res Public Health. 2019;16(10). doi:10.3390/ijerph16101700.
- Rhodes D, Visker JD, Cox C, Sas A, Banez JC. Effects of an online educational module on school nurses‘ knowledge of HPV vaccination. J Contin Educ Nurs. 2017;48(9):431–36. doi:10.3928/00220124-20170816-10.
- Shukla A, Nyambose J, Vanucci R, Johnson LB, Welch K, Lind E, Villa A. Evaluating the effectiveness of human papillomavirus educational intervention among oral health professionals. J Cancer Educ. 2019;34(5):890–96. doi:10.1007/s13187-018-1391-z.
- Salinas GD, Effectiveness: CME. Utilizing outcomes assessments of 600+ cme programs to evaluate the association between format and effectiveness. J Contin Educ Health Prof. 2015:35. doi:10.1002/chp.21279.
- Dönmez S, Öztürk R, Kısa S, Karaoz Weller B, Zeyneloğlu S. Knowledge and perception of female nursing students about human papillomavirus (HPV), cervical cancer, and attitudes toward HPV vaccination. J Am Coll Health. 2019;67(5):410–17. doi:10.1080/07448481.2018.1484364.
- Sanko J, McKay M, Shekhter I, Motola I, Birnbach DJ. What participants learn, with, from and about each other during inter-professional education encounters: A qualitative analysis. Nurse Educ Today. 2020;88:104386. doi:10.1016/j.nedt.2020.104386.
- Bosnic-Anticevich SZ, Stuart M, Mackson J, Cvetkovski B, Sainsbury E, Armour C, Mavritsakis S, Mendrela G, Travers-Mason P, Williamson M. Development and evaluation of an innovative model of inter-professional education focused on asthma medication use. BMC Med Educ. 2014;14(1):72. doi:10.1186/1472-6920-14-72.
- Basheti IA, Hamadi SA, Reddel HK. Inter-professional education unveiling significant association between asthma knowledge and inhaler technique. Pharm Pract. 2016;14(1):713. doi:10.18549/PharmPract.2016.01.713.
- Fontenot HB, Kornides ML, McRee A-L, Gilkey MB. Importance of a team approach to recommending the human papillomavirus vaccination. J Am Assoc Nurse Pract. 2018;30(7):368–72. doi:10.1097/JXX.0000000000000064.
- Perkins RB, Lin M, Wallington SF, Hanchate AD. Impact of school-entry and education mandates by states on HPV vaccination coverage: analysis of the 2009–2013 National Immunization Survey-Teen. Hum Vaccin Immunother. 2016;12(6):1615–22. doi:10.1080/21645515.2016.1150394.
- Greyson D, Vriesema-Magnuson C, Bettinger JA. Impact of school vaccination mandates on pediatric vaccination coverage: a systematic review. CMAJ Open. 2019;7(3):E524–E36. doi:10.9778/cmajo.20180191.
- Gualano MR, Olivero E, Voglino G, Corezzi M, Rossello P, Vicentini C, Bert F, Siliquini R. Knowledge, attitudes and beliefs towards compulsory vaccination: a systematic review. Hum Vaccin Immunother. 2019;15(4):918–31. doi:10.1080/21645515.2018.1564437.