Human Papillomavirus Vaccination Knowledge, Barriers, and Recommendations among Healthcare Provider Groups in the Western United States

Abstract

Introduction:

This study compared human papillomavirus (HPV) vaccination occurrences on the same day as provider recommendations at clinics in the Western United States stratified by healthcare provider groups. In addition, the relationships between provider groups’ perceived challenges associated with HPV vaccination, HPV vaccination knowledge, HPV recommendation practices, and same-day HPV vaccinations and recommendations are described.

Method:

Eligible participants included pediatric healthcare providers and staff with influence on patient/parental-level decisions regarding HPV vaccination. Participants filled out a 40-question survey.

Results:

Results for study participants (N=99) showed providers reported a higher number of challenges limiting HPV vaccination, higher HPV vaccination knowledge, and more favorable HPV vaccination recommendation practices compared to other health care team members (OTM) suggesting providers may have a better overall understanding of the HPV vaccination climate than OTMs.

Discussion:

Clinics should examine OTMs’ training, expectations, and opportunities to increase the frequency and strength of HPV vaccination recommendations to adolescent patients and parents.

Background

In the United States (US), more than 24,900 women and 19,100 men are diagnosed with human papillomavirus (HPV) associated cancers annually (Centers for Disease Control and Prevention, 2019). HPV is a sexually transmitted infection that can cause cervical, anal, penile, vagile, vulvar, genital warts, and oropharyngeal cancers. Over the past decade, HPV vaccinations have emerged as a safe, effective way to prevent HPV infection and subsequent related cancers (Landis et al., 2018). Furthermore, the vaccine can protect against 70% of cervical cancers, 90% of genital warts, and approximately 70% of HPV-attributable oropharyngeal cancers. Despite the HPV vaccine availability in the United States (US) and its strong recommendations by the Centers for Disease Control and Prevention (CDC), uptake remains low among females and males of eligible age (Reveal, 2016).

Between 2018 and 2019, HPV vaccination rates improved among US teens and adolescents. Not only did the first dose HPV vaccination rate improve for both males and females, but also the second and third dose HPV vaccination rate; however, this is likely due to state and national organizations supporting a two-dose HPV series rather than a three-dose series (Elam-Evans et al., 2020). Unfortunately, these improvements in vaccination coverage are limited in non-metropolitan or rural areas. Historically, the lowest HPV vaccination rates in the US are in rural areas of the Western US, also called the Mountain West (MW) regions—encompassing 11 states: Washington, Oregon, California, Idaho, Wyoming, Montana, Nevada, Utah, Colorado, Arizona, and New Mexico. In terms of national HPV up-to-date (UTD) rates, Wyoming, Utah, Idaho, Montana, Nevada and New Mexico are all under the national average of 54.2% (UTD) among all adolescents. UTD means those with ≥3 doses, and those with 2 doses when the first HPV vaccine dose was initiated before age 15 years and time between the first and second dose was at least 5 months minus 4 days. Among all the MW states, HPV vaccine completion rates for ages 13–15 years are below the Healthy People 2020 goal of 80% (Elam-Evans et al., 2020).

Previous research has established that a strong healthcare provider recommendation is an important factor associated with HPV vaccination uptake (Allen et al., 2010; Reiter et al., 2009; Rosenthal et al., 2011; Ylitalo et al., 2013; McRee et al., 2014). Much attention has been focused on examining ways to mitigate patient and parental disparities related to HPV vaccination, particularly in rural areas like much of the MW region; these disparities include low health insurance coverage, low-income, low education attainment, low health literacy, low knowledge and trust in vaccinations, geographical barriers to healthcare, and limited provider networks leading to lack of privacy (Newcomer et al., 2020; Peterson et al., 2020; Williams et al., 2020; Vanderpool et al., 2019; Walker et al., 2017; Head et al., 2013; Blumling et al., 2013; Yabroff et al., 2005; Casey et al., 2001; Shell & Tudiver, 2004; Hart et al., 2005). However, healthcare providers face a number of barriers to recommending HPV vaccine as well such as, feeling uncomfortable discussing sexual health issues with parents and adolescents (Daley et al., 2010; Vadaparampil et al., 2011) and avoiding lengthy or confrontational conversations about vaccination (Daley et al., 2010; Hughes et al., 2011). Likewise, other research has centered on the need for increasing provider knowledge of HPV and HPV vaccination guidelines (Bertowitz et al., 2015; Topazian et al., 2019) and improving provider communication (Holman et al., 2014).

In our survey study, we sought to compare whether the HPV vaccination typically occurs on the same day as the clinic-delivered recommendation at MW clinics stratified by healthcare provider and staff groups. In addition, we described the relationships between different provider groups’ perceived challenges associated with HPV vaccination, HPV vaccination knowledge, HPV recommendation practices, and same-day HPV vaccination and recommendation.

Methods

Sample and Setting

To be eligible for participation in this survey study, participants had to be pediatric healthcare providers and staff in a position to impact patient/parental-level decisions regarding HPV vaccination. Participants were divided into two groups: 1) clinicians, which included medical doctors, residents, physician assistants (PA), and nurse practitioners, and 2) other healthcare team members (OTM), which included nurses, medical assistants (MA), clinic staff, administrators, and stakeholders. Stakeholder was defined as those from professions related to community health (e.g. community health worker).

This study engaged several partners who aided in the recruitment process: (1) the Intermountain West HPV Vaccination Coalition, a group of health practitioners, health researchers, community members, and other stakeholders interested in increasing the HPV vaccination rates in the MW; the High Sierra Area Health Education Center an organization in Nevada interested in developing community-academic partnerships and develop future leaders in healthcare; and (3) community healthcare clinics and small medical centers. Recruitment methods largely included purposive sampling. Each identified participant’s eligibility was confirmed, and informed consent was obtained before taking the survey.

Participants from ten clinics in five MW states—Montana (n=24), Colorado (n=32), Utah (n=22), Nevada (n=5), and Arizona (n=16)—completed the survey between January and June 2019. To obtain a more representative sample of the MW, we oversampled rural clinics. Participants received a $25 gift card for completing our survey and participating in a related focus group. Participating clinics received a stipend for their time and support in recruiting participants. Before study activities began, the study was submitted to and approved by the University of Utah’s Institutional Review Board and all methods were performed in accordance with the relevant guidelines and regulations.

Measures

The researchers administered paper surveys which included 40 questions. The survey included demographic questions, a perceived challenges subscale, a knowledge subscale, a recommendation practices subscale, and a same-day HPV vaccination question (primary outcome). The demographic portion included three participant-level questions (e.g. gender, race, and Hispanic ethnicity) and two employment questions (e.g. clinic location and provider type). We used the zip code for each clinic to identify the rural-urban status of each clinic. The 2010 Rural-Urban Commuting Area codes were used to classify areas based on population and direction of primary commuting flows (United States Department of Agriculture, 2010). For this study, large rural, small rural, and isolated clinic locations were grouped into a single rural category.

Next, the survey included items to assess 16 perceived challenges related to administering the HPV vaccine such as, “Our clinic does not stock the vaccine”, “Lack of time during the clinic visit to administer the vaccine”, and “We do not use the electronic health record to track the HPV vaccine status of patients”. This list of challenges was drawn from published literature and the researchers’ expertise and experiences (Newcomer et al., 2020; Peterson et al., 2020; Williams et al., 2020; Vanderpool et al., 2019; Walker et al., 2017; Head et al., 2013; Blumling et al., 2013; Yabroff et al., 2005; Casey et al., 2001; Shell & Tudiver, 2004; Hart et al., 2005; Daley et al., 2010; Vadaparampil et al., 2011; Hughes et al., 2011; Bertowitz et al., 2015; Topazian et al., 2019; Holman et al., 2014). A total score for challenges was calculated for each participant by adding up the number of challenges selected. Each response was given a score of one meaning the minimum obtainable score was 0 and the maximum score was 16.

Then, items on the survey assessed knowledge regarding the HPV vaccine using 15 items created by the researchers. Some example items included, “The HPV vaccine leads to long lasting immunity” and “HPV vaccination is highly effective at preventing cervical cancer precursors.” Eight questions had responses on a five-point Likert scale (1 = “Strongly disagree”, 2 = “Disagree”, 3 = “Neither agree nor disagree”, 4 = “Agree”, 5 = “Strongly agree”) and seven questions were graded responses on a three-point scale (−1 = Incorrect answer, 0 = Don’t know, 1 = Correct answer). However, one three-point scale question, “Offering the HPV vaccine provides an opportunity to discuss sexuality issues with your patients,” was excluded in the calculation since the question is not easily determined to be correct or incorrect. Hence the total score for knowledge was calculated by adding up scores of 14 items and the minimum obtainable score was 2 and the maximum score was 46.

Finally, the survey assessed HPV vaccine recommendation practices using three items, including “How often do you recommend the HPV vaccine to boys and girls at 11–12 years of age?”, “How often do you assume the child will get the HPV vaccine as part of the regularly scheduled adolescent vaccines?”, and “How often do you recommend that patients get the vaccine on the same day you recommended it?”. These items had responses on five-point Likert scale (0 = “N/A”, 1 = “Rarely/Never”, 2 = “Sometimes”, 3 = “Usually”, 4 = “Almost always”). The total score for recommendation practices was calculated by adding up responses for the three items; hence, the minimum obtainable score was 0 and the maximum score was 12. The last question asked about the study’s primary outcome, “How often do your patients get the HPV vaccine the same day after you recommend it?” The responses were based on a five-point Likert scale (0 = “N/A”, 1 = “Rarely/Never”, 2 = “Sometimes”, 3 = “Usually”, 4 = “Almost always”) and was separately calculated with the minimum obtainable score was 0 and the maximum score was 4.

Data Analysis

All data were stratified by participant group, either clinician or OTM. Fisher’s exact tests were used to assess demographic variable differences by group. Total scores for challenges, knowledge, and recommendation practices were presented as means and 95% confidence intervals (CIs), and Wilcoxon rank-sum tests were performed to assess differences between the two groups. Odds ratios and 95% CIs were estimated using logistic regression models to compare clinicians with OTMs for each recommendation practice item and our primary outcome. Pearson correlation coefficients were used to examine the correlational relationships between the perceived challenges subscale, knowledge subscale, recommendation practices subscale, and same-day HPV vaccination question. Statistical significance was set at p<0.05. Data were analyzed using SAS, software version 9.4 (SAS Institute, Cary, North Carolina).

Results

The sample analyzed for this study (N=99) was mostly female (clinicians: 63.6%; OTM: 92.2%), with a higher proportion of female OTMs compared to clinicians (p=0.0023; see table 1). Although the majority of the sample was non-Hispanic, there was a higher proportion of Hispanic OTMs (36.4%) compared to Hispanic clinicians (9.1%; p=0.0167). A higher proportion of clinicians were from rural clinic locations (77.3%) compared to OTMs (50.6%; p=0.0301). More PAs completed the survey (9.1%) than other clinician profession categories; and the most common OTMs profession categories to complete the survey included nurses (26.3%), other healthcare professions (22.2%), and MAs (21.2%). It is also important to note that no meaningful differences were found between rural and urban subgroups on demographics or survey responses. Due to the purposive recruitment methods used, a response rate was incalculable. Based on estimates from study partners, however, our study had a high response rate estimated to be 90%−95%.

Table 1.

Demographic characteristics by provider type.

	Overall, N=99	Clinician, n=22	OTM*, n=77	p-valuea
Gender, n(%)				0.0023
Male	14 (14.1%)	8 (36.4%)	6 (7.8%)
Female	85 (85.9%)	14 (63.6%)	71 (92.2%)
Race, n(%)				1.0000
White	91 (91.9%)	20 (90.9%)	71 (92.2%)
Other	8 (8.1%)	2 (9.1%)	6 (7.8%)
Hispanic, n(%)b				0.0167
Yes	30 (30.3%)	2 (9.1%)	28 (36.4%)
No	68 (68.7%)	20 (90.9%)	48 (62.3%)
n/a	1 (1.0%)	-	1 (1.3%)
Clinic location, n(%)c				0.0301
Rural	56 (56.6%)	17 (77.3%)	39 (50.6%)
Urban	43 (43.4%)	5 (22.7%)	38 (49.4%)
Provider Type, n(%)d
Medical Doctor	7 (7.1%)	7 (31.8%)	-	n/a
Physician Assistant	9 (9.1%)	9 (40.9%)	-
Nurse Practitioner	6 (6.1%)	6 (27.3%)	-
Nurse	26 (26.3%)	-	26 (33.8%)
Medical Assistant	21 (21.2%)	-	21 (27.3%)
Clinic staff	6 (6.1%)	-	6 (7.8%)
Administrator	2 (2%)	-	2 (2.6%)
Other	22 (22.2%)	-	22 (28.6%)

^*Other Health Care Team Members (OTM)

^aFishers Exact Test for Count Data

^bMissing value omitted from test

^cUnited States Department of Agriculture. (2010). Rural-Urban Commuting Areas Codes (RUCA). https://www.ers.usda.gov/topics/rural-economy-population/rural-classifications/

^dOther: healthcare students, behavioral health, Certified Professional Coder, Licensed Family and Marriage Therapist

Table 2 shows that clinicians scored higher on all sub-scales. Clinicians reported a higher number of challenges that limit HPV vaccination (1.95; 95%CI: 1.47–2.44) compared to OTMs (1.06; 95%CI: 0.70–1.43; p=0.0002). Clinicians also reported higher overall knowledge scores about HPV vaccination (39.82; 95%CI: 38.13–41.50) compared to OTMs (32.48; 95%CI: 30.55–34.41; p<0.0001); and clinicians reported higher HPV recommendation practice scores (10.55; 95%CI: 9.81–11.28) compared to OTMs (6.79; 95%CI: 5.66–7.92; p=0.0030). Lastly, clinicians reported a higher tendency for patients to get the HPV vaccination the same day of a recommendation (2.50; 95%CI: 2.07–2.93) compared to OTMs (1.69; 95%CI: 1.35–2.02; p=0.0287).

Table 2.

Summary table for average scores (challenges, knowledge, and recommendation practices) by provider type.

	Clinician, n=22	OTM*, n=77	p-value a
	Mean (95%CI)
Number of challenges that limits HPV vaccination	1.95 (1.47 – 2.44)	1.06 (0.70 – 1.43)	0.0002
Overall knowledge score about HPV vaccination b	39.82 (38.13–41.50)	32.48 (30.55–34.41)	<0.0001
HPV recommendation practices c	10.55 (9.81 – 11.28)	6.79 (5.66 – 7.92)	0.0030
Tendency patients get HPV vaccination the same day of provider recommendation d	2.50 (2.07 – 2.93)	1.69 (1.35 – 2.02)	0.0287

^*Other Health Care Team Members (OTM)

^aWilcoxon rank sum test

^bHigher score indicates higher knowledge about HPV vaccination. Maximum score 46.

^cHigher score indicates higher recommendation practices for the HPV vaccination. Maximum score 12.

^dHigher score indicates higher frequency of HPV vaccination the same day after recommendation. Maximum score 4.

The odds of the HPV vaccine ‘almost always’ being recommended to boys and girls at 1–12 years of age was 3.31 higher (95%CI: 1.11–9.88) for clinicians compared to OTMs (see table 3). Likewise, the odds that the provider ‘almost always’ recommends that the vaccine be administered the same day it is recommended was 3.55 higher (95%CI: 1.29–9.72) compared to OTMs. Other comparisons of recommendation practices and response level were statistically insignificant between the two groups. After adjusting for sex, ethnicity, and rurality, the inference did not change but the 95% CI became wider due to limited sample size (data not shown).

Table 3.

Comparison of HPV vaccination recommendation practices among clinicians vs. OTM^*.

Questions	Response	Crude OR (95%CI)
How often do you recommend the HPV vaccine to boys and girls at 1–12 years of age?	Rarely/Never	−
	Sometimes	7.60 (0.66–88.12)
	Usually	0.86 (0.22–3.35)
	Almost always	3.31 (1.11–9.88)
How often do you assume the child will get the HPV vaccine as part of the regularly scheduled adolescent vaccines?	Rarely/Never	−
	Sometimes	1.20 (0.35–4.19)
	Usually	1.75 (0.64–4.80)
	Almost always	2.38 (0.89–6.34)
How often do you recommend that patients get the vaccine at the same day you recommended it?	Rarely/Never	3.62 (0.22–60.33)
	Sometimes	−
	Usually	1.85 (0.61–5.61)
	Almost always	3.55 (1.29–9.72)
How often do your patients get the HPV vaccine the same day after you recommended it?	Rarely/Never	0.69 (0.08–6.20)
	Sometimes	2.64 (0.96–7.27)
	Usually	1.75 (0.64–4.80)
	Almost always	1.19 (0.29–4.85)

^*Other Health Care Team Members (OTM)

Overall, the correlations tested were not particularly strong but were statistically significant as shown in table 4. The reported number of challenges that limit HPV vaccination were significantly correlated with recommendation practices (p=0.0011) and same-day HPV vaccination (p=0.0313). Likewise, HPV vaccination knowledge scores are significantly correlated with recommendation practices (p<0.0001) and same-day HPV vaccination (p<0.0001). Recommendation practices and same-day HPV vaccination were also significantly correlated (p<0.0001). These relationships were largely driven by the OTMs. A sub-group analysis reveals that these significance levels do not convey when examining clinicians only, but do when examining OTMs only.

Table 4.

Correlations among number of challenges, knowledge, recommendation practices, and same-day HPV vaccination.

Variables	Correlation a	p-value
Overall (Clinicians and OTMs*):
Number of challenges vs. Recommendation practices	0.32	0.0011
Number of challenges vs. Same-day HPV vaccination	0.22	0.0313
Knowledge vs. Recommendation practice	0.53	<0.0001
Knowledge vs. Same-day HPV vaccination	0.45	<0.0001
Recommendation practices vs. Same-day HPV vaccination	0.83	<0.0001
Clinicians:
Number of challenges vs. Recommendation practices	0.17	0.4417
Number of challenges vs. Same-day HPV vaccination	−0.07	0.7637
Knowledge vs. Recommendation practice	0.32	0.1575
Knowledge vs. Same-day HPV vaccination	0.08	0.7300
Recommendation practices vs. Same-day HPV vaccination	0.39	0.0741
OTMs:
Number of challenges vs. Recommendation practices	0.26	0.0200
Number of challenges vs. Same-day HPV vaccination	0.19	0.1043
Knowledge vs. Recommendation practice	0.45	<0.0001
Knowledge vs. Same-day HPV vaccination	0.42	0.0002
Recommendation practices vs Same-day HPV vaccination	0.85	<0.0001

^*Other Health Care Team Members (OTM)

^aPearson correlation coefficient

Discussion

Our study found that providers reported a higher number of challenges that limit HPV vaccination compared to OTMs. This could be that clinicians are simply more aware of the aggregate challenges related to this topic. Over the last two decades, adolescent and young adult HPV vaccination guidelines have been clarified and strengthened by the top professional agencies and committees, such as the Advisory Committee on Immunization Practices approving a two-dose schedule (Meites et al., 2016) and extending the age for vaccination (Meites et al., 2019). However, doctors may still have their own reservations about the vaccine or know that some patients/parents may be misinformed. Despite health communication campaigns, segments of the US population are anti-vaccination or hold misconceptions about HPV vaccination (Nyhan et al., 2014; Blasi et al., 2015; Mohanty et al., 2018). As a result, this potential dissonance in professional recommendations and lay beliefs may lead some clinicians to more easily identify directly related challenges and other indirect barriers, such as time and budget constraints, compared to other OTMs.

Providers also reported higher knowledge scores suggesting that clinicians may have a better overall understanding of the HPV vaccination climate than OTMs. This finding is supported by Roberts et al.’s findings that knowledge about vaccinations differ among staff members in a healthcare clinic (Roberts et al., 2020). While increasing OTMs knowledge is a common intervention and is useful in increasing vaccine uptake, researchers or interventionists should not interpret increases in OTMs’ reported challenges after an educational effort as a negative outcome. In fact, our results support that knowledge and identifying challenges may be beneficial in improving recommendation practices and uptake rates. Nevertheless, it is unclear from our survey if the barriers identified by clinicians or OTMs are perceived to be surmountable. Some challenges may be perceived as easy to overcome while others are difficult or impossible to work around.

In regards to recommendation practices, we found that clinicians, as compared to OTMs, more often recommend the HPV vaccine to boys and girls at 11–12 years of age and recommend that patients get the vaccine that day. This could be due to a number of different factors such as, clinic flow, recommendations typically coming from clinicians, and/or education. It may be beneficial for clinics to examine OTMs’ training, expectations, and opportunities to make HPV vaccination recommendations to patients and parents to increase uptake rates.

Interestingly, clinicians and OTMs did not differ on the assumption that a child will get the HPV vaccine as part of the regularly scheduled adolescent vaccines. This suggests that clinicians and OTMs may hold similar thoughts and assumptions regarding their patients and the HPV vaccine. Likewise, clinicians and OTMs did not differ on how often patients get the HPV vaccine the same day it is recommended meaning that the healthcare provider type is not a differentiating factor in patients’/parents’ ultimate decision to vaccinate. Finally, we did confirm the positive association between strong recommendation practices and same-day HPV vaccination, which was largely driven by OTMs. Thus, OTMs do have an impact on patients’/parents’ decisions to vaccinate and reevaluating OTMs’ roles regarding HPV vaccination recommendation could be an important strategy for improving HPV vaccine uptake in the MW. Our research suggests that although both clinicians and OTMs are not consistently providing strong recommendations for same-day vaccination, they do understand the importance of doing so. It may be beneficial for clinics to take a “whole-office” approach to vaccination recommendations by including all clinic staff in intentional trainings to increase the number of strong recommendations to vaccinate and same-day vaccinations, as well as including all clinic staff in discussions to set key performance indicators for the clinic to improve vaccination rates.

Limitations

Our study should not be overgeneralized as it was a relatively modest sample in the MW region and was oversampled for rural provider participation. Other regions of the US or countries should conduct studies to understand unique cultural, political, or societal factors that impact HPV vaccination in their respective populations. Our survey was limited as it did not examine specific challenges, assess particular knowledge strengths/deficits, or ask follow-up questions regarding recommendation practices. The survey was also voluntary meaning self-selection bias is a possibility, although it was anonymous; and all items were self-reported which could have resulted in social desirability bias. This bias may help explain why we found no meaningful differences between rural and urban providers. More research on a larger, representative sample would undoubtedly be beneficial in understanding the vaccination climate in the MW.

Conclusion

As other researchers have emphasized, increasing HPV vaccination in any part of the US will require a multi-faceted approach (Askelson et al., 2019; Head et al., 2018). By assessing HPV vaccination challenges, knowledge, and recommendation practices, we were able to identify potential interventions to improve HPV vaccination in MW clinics. More broadly, we hope that the results of this survey provide information regarding gaps in HPV vaccination efforts and reveal opportunities for improving clinical practice and patient outcomes.

Our study found that clinicians reported a higher number of challenges that limit HPV vaccination, higher HPV vaccination knowledge, and more favorable HPV vaccination recommendation practices compared to OTMs, which may suggest clinicians have a better overall understanding of the HPV vaccination climate than OTMs. However, clinicians and OTMs did not differ on how often patients get the HPV vaccine the same day it is recommended suggesting that the healthcare provider type is not a differentiating factor in patients’/parents’ ultimate decision to vaccinate. Finally, we did confirm the relationship between healthcare providers’ strong recommendation practices and same-day HPV vaccination. In conclusion, it may be beneficial for clinics to examine OTMs’ training, expectations, and opportunities to increase the frequency and strength of HPV vaccination recommendations to adolescent patients and parents. All clinics, but especially those with lower HPV vaccination rates, should include both clinicians and OTMs in a “whole-office” approach to vaccination recommendations.

List of Abbreviations

CDC

Centers for Disease Control and Prevention

CI

confidence interval

HPV

human papillomavirus

MA

medical assistant

MW

Mountain West

OTM

other healthcare team members

PA

physician assistants

US

United States

UTD

up-to-date