690
Views
1
CrossRef citations to date
0
Altmetric
Acceptance & Hesitation

Urban and rural healthcare providers’ perspectives on HPV vaccination in Minnesota

, , , , , , , , & show all
Article: 2291859 | Received 16 Sep 2023, Accepted 03 Dec 2023, Published online: 14 Dec 2023

ABSTRACT

Human papillomavirus (HPV) vaccination can dramatically reduce the incidence of HPV-associated cancers. However, HPV vaccination coverage in rural areas is lower than in urban areas, and overall HPV vaccination coverage in the United States remains lower than other adolescent vaccines. We conducted 20 qualitative interviews with adolescent healthcare providers and clinic staff in urban and rural Minnesota and assessed their perspectives on HPV vaccination. Guiding interview topics included: strategies to persuade families to vaccinate their children, the impact of the patient-provider relationship and the clinical environment on vaccination uptake, and provider perceptions of parents’ vaccine attitudes. In thematic analysis, all participants reported using common vaccination strategies, such as framing the HPV vaccine in terms of cancer prevention. The analysis also revealed three themes described as occurring uniquely or more intensely in rural communities than urban communities: the rural value of choice or independence, the spread of misinformation, and close-knit, multifaceted patient-provider relationships in clinical practice. Interventions aimed at increasing HPV vaccination should consider the distinctive circumstances of rural healthcare providers and patients.

Introduction

Human papillomavirus (HPV) is a leading cause of cancer morbidity and mortality in the United States, resulting in approximately 24,809 new cases of cervical, oropharyngeal, and other cancers annually.Citation1 HPV vaccination has dramatically reduced these cancers’ incidence and mortality in areas with high coverage.Citation2 However, HPV vaccination coverage in the United States remains below other adolescent vaccines, particularly in rural areas.Citation3 To explore clinical perspectives on urban-rural HPV vaccination disparities, we interviewed urban and rural adolescent healthcare providers in Minnesota.

Only 65.7% of Minnesota adolescents 13–17 years old were up to date on their HPV vaccinations in 2021, despite coverage over 90% for tetanus, diphtheria, and acellular pertussis (Tdap) and quadrivalent meningococcal (MenACWY) vaccines.Citation4 Coverage is even lower for rural adolescents: from 2015–2019, adolescents aged 13–17 living outside a metropolitan statistical area (MSA) in the United States were thirteen percentage points less likely to be up-to-date on their HPV vaccine series than those living in MSA principal cities.Citation3

Furthermore, general hesitancy toward routine vaccinations may have increased during the COVID-19 pandemic.Citation5 By January 2022, COVID-19 vaccination coverage for adults and children aged ≥5 years was 17% points lower in rural areas than in urban areas.Citation6 If urban-rural inequity in COVID-19 vaccination coverage reflects growing overall vaccine hesitancy in rural areas, the urban-rural disparity in HPV vaccination coverage may widen.

Numerous best practices have been identified for clinics and providers to increase HPV vaccination coverage. Recommended individual-level strategies include having vaccine providers use presumptive language, where vaccines are announced rather than discussed as options to be weighed (e.g., “Today you are due for 3 vaccines: Tdap, HPV, and meningococcal vaccines”),Citation7 and the “sandwich method,” where HPV is presented in a list between other required or more readily accepted adolescent vaccines.Citation8 Clinic-level interventions include training and prompts for both providers and staff to promote vaccines at every opportunityCitation9,Citation10 and reminder/recall mail, e-mail, phone, or texting campaigns to inform parents that their children are due for vaccines.Citation11,Citation12

Beyond specific strategies, numerous studies have found that healthcare providers can influence HPV vaccination decisions. Multiple studies show that a strong provider recommendation is a strong predictor of vaccine uptake,Citation13,Citation14 and patients consistently cite their provider’s recommendation as one of the most influential factors in vaccine decision-making.Citation15 Healthcare providers may also have valuable insight into the values and perspectives contributing to families’ adolescent vaccination choices. To harness this knowledge and gain a stronger understanding of the factors driving low HPV vaccination in the rural Upper Midwest, we conducted 20 semi-structured in-depth interviews with key informants who are urban and rural healthcare providers and clinical staff in Minnesota.

Materials and methods

Design and participants

Clinics that provide adolescent vaccines in Minnesota were identified using the Minnesota Immunization Information Connection (MIIC), Minnesota’s statewide immunization information system (IIS). Participants were included if they 1) provided vaccinations to adolescents (individuals aged 13 to 17 years) and 2) worked in a clinical setting in a rural or urban county as determined by the United States Department of Agriculture Urban Influence Codes (UIC) (Documentation: 2013 Rural-Urban Continuum Codes, 2020). Counties were designated as rural (UIC 6–12) or urban (UIC 1), and all providers working in counties with UIC 2–5 were excluded.

Clinics that served adolescent patients as of November 2021 were extracted from MIIC and sorted by their combined HPV and COVID-19 vaccination coverage levels in MIIC. Vaccination coverage levels were derived by dividing the number of individuals aged 13–17 associated with the clinic who had initiated their HPV and COVID-19 series by the total number of individuals aged 13–17 associated with the clinic. To catalog a variety of experiences, clinics with the lowest combined coverage levels were contacted first, then all clinics on the list were contacted.

Email addresses recorded in MIIC were supplemented with contact information on Minnesota medical licensing and clinic websites. In addition, the Minnesota Chapter of the American Academy of Pediatrics (MNAAP) posted a recruitment advertisement in their e-newsletter. Finally, an advertisement was posted on the Minnesota Department of Health’s Facebook page for 14 days and targeted Facebook users who liked organizations related to adolescent healthcare. Emails were sent using MIIC data from January 2022 through April 2022, and advertisements with MNAAP and Facebook occurred in April 2022. Although we did not verify participants’ recruitment sources, and some participants may have been recruited from multiple strategies, all 20 participants worked for clinics on the initial MIIC recruitment list.

An invitation was emailed to the vaccination coordinator listed for each clinic in MIIC. The study invitation directed providers to a brief REDCap survey that confirmed eligibility (as described above), collected demographic information, and obtained consent to participate in a recorded virtual interview. Consent was affirmed at the beginning of each interview.

Participant recruitment goals were set at ten rural and ten urban participants. These goals were based on expected saturation within a well-defined population, researchers’ previous experience with the population, the anticipated deductive coding strategy, and resource limitations.Citation16 Two individuals initially erroneously categorized as “rural” worked in excluded counties, resulting in two fewer rural providers than anticipated. After excluding these providers, the final cohort included seven rural and 13 urban providers. Through iterative discussions throughout the data collection process, the research team determined that saturation had been met with only seven rural interviews since new interviews of rural providers were no longer providing new data on our themes of interest.

Data collection

Interviews were completed virtually and recorded using Microsoft Teams. Nine participants elected to conduct video interviews, while twelve selected audio only. Five study staff members conducted approximately four interviews each (BC, MD, HL, EP, and AS).

Each interview lasted approximately 20 minutes. An interview guide was developed by study investigators and revised iteratively by interview staff. Probing questions were included to help participants focus on factors they believe influence adolescent vaccination decisions. The final interview guide focused on three major areas. First, providers were asked about their strategies when discussing HPV, COVID-19 and other adolescent vaccines. Then, they were asked to describe the clinical environment’s role in encouraging vaccination. Finally, participants were asked to describe their perceptions of parents’ attitudes toward adolescent vaccination. Participants were encouraged to express their general attitudes about HPV vaccines, COVID-19 vaccines, other adolescent vaccines, and related concepts. Because the study was conducted during a particularly intense period of the COVID-19 pandemic and rollout of new COVID-19 vaccine (winter 2022), we also collected information about COVID-19 vaccines and how perceptions, recommendations, and clinical processes for COVID-19 and HPV vaccines might have related to one another in clinical settings. This project was deemed to be not human subjects research by the institutional review board of the Minnesota Department of Health.

Analysis

All interviews were transcribed and codes were primarily generated inductively, although three deductive codes were designated a priori based on the interview guide: provider strategies, patient-provider relationship, and physical clinic resources. Codes were generated iteratively and by a team of two researchers with supervision from the team’s qualitative expert. The team met to compare coded quotations after separately coding two, then ten, then all interviews. Once concordance was determined to be adequate, thematic analysis was finalized. The thematic analysis included the responses of both urban and rural providers. Because our primary goal was to explore low rural HPV vaccination uptake, we focused the analysis on the challenges and barriers highlighted by rural providers.

Results

Participants were 13 urban and 7 rural healthcare providers working in twelve Minnesota counties. Participants reported a median of 20 years at their current clinic (range: 1 month to 37 years). Participants were primary care providers (physician or physician assistant) (N = 15), nurses (N = 2), epidemiologist (N = 1), pharmacist (N = 1), and clinic manager (N = 1). Of physicians, 3 were pediatricians, 2 were family practitioners, and 10 did not list a specialty. Twelve of 13 (92%) urban and 3 of 7 (43%) rural participants were physicians or physician assistants. Eight (40%) also listed a clinic leadership role, such as manager or chief medical officer. Of 13 participants who provided race and ethnicity information, 11 were non-Hispanic White, one was non-Hispanic Black, and one was “other.” All rural participants who reported race and ethnicity identified as White and non-Hispanic (). Median clinic HPV vaccine initiation coverage was 58.3% in rural providers and 58.4% in urban providers. Quotes included here and in were felt to typify repeated language across the interviews.

Table 1. Participant characteristics.

Table 2. Common provider strategies to introduce HPV vaccines.

Provider strategies

When asked which strategies they use to introduce the HPV vaccine to families, most providers listed similar approaches, which are described in . During individual clinic visits, most described focusing on cancer prevention (rather than sexual transmission), and several mentioned that they encouraged reluctant families to initiate the HPV vaccine series on time by informing them that the vaccine increases to three doses in older patients. Multiple providers mentioned the use of presumptive language and the sandwich method, and most providers recommend the HPV vaccine at age 11 along with the Tdap and MenACWY vaccines. However, one participant mentioned that they preferred to recommend the vaccine at age 12 and combine it with a larger conversation about puberty. A few providers stated they speak directly to adolescent patients about vaccines when parents are hesitant.

Clinic-level strategies included: creating a clinic-wide culture of vaccination that involves unified pro-vaccine messaging from rooming staff, nurses, and physicians and offering vaccines at every clinical encounter. Additionally, two urban providers reported hiring staff and providers who speak the languages and come from the same cultures as their patients.

Participants described similar strategies to discuss vaccines with patients, regardless of rural or urban location. However, rural and urban participants described different experiences for three themes: patient-provider relationships, the value of choice, and misinformation/disinformation (). Finally, both urban and rural participants described the impact of COVID-19 on their adolescent immunization experiences.

Figure 1. Responses of individual participants surrounding three core themes.

Figure 1. Responses of individual participants surrounding three core themes.

Theme 1: patient-provider relationship

Most providers confirmed that a trusting patient-provider relationship is crucial to increasing vaccine acceptance. However, these relationships took different forms for urban and rural participants. For urban providers, connections with patients and their families were long-term and trusting, but ultimately professional:

… you have this trusted mechanic for your car. They’ve never steered you wrong. This time they tell you you need new brake pads. You could pull your car out and go to the guy next door and get his opinion or her opinion, but they’ve never steered you wrong before. You know, you just do it. So, I think people come to see me, they trust me, we’ve been talking for a long time. Their kid is now 12 years old, and let’s say their older kids are much older so they’ve known me for 20 years, and they say, what do I recommend? And I say, this is what we should do. And they just do it. – Urban #19, Physician (Pediatrician), 32 years in role

Conversely, most rural participants described multifaceted bonds with patients. Several described living in the communities where they worked, sending their children to school with their patients, or getting to know whole families by playing multiple roles in small clinics. These close relationships can be an asset to providers:

I usually just address it directly unless I know the patient and know the parents, I should say, and know their take on vaccines. Because like I said, it’s a small town, so my children go to school with most of these kids and we know them outside of the clinic. – Rural #8, Physician, 13 years in role

Relationships of nurses and clinic staff with patients

Nearly all urban (10/13) and rural (5/7) providers mentioned that patients connect easily to nurses and clinic staff. Providers reported that patients’ trust in nurses could be a useful tool ():

We try to get our nursing staff educated too. So at least, you know, when we’re rooming our patients here, our nursing staff are kind of in there bringing up the conversation of vaccines. You know, a lot of times, you know, before I even go into the room, I kind of have an idea, you know, is this patient going to be predisposed to, you know, this vaccine or that vaccine and, you know, maybe where I need to focus my attention on. So, I think that’s been a really good asset, is having our nurses trained in on what we’re vaccinating for and why. – Rural #11, Physician Assistant, 6 years in role

However, a few providers mentioned that they try to keep their vaccine-hesitant nurses and rooming staff from sharing their opinions with patients:

Unfortunately, our medical staff is sometimes not so pro-vaccine themselves. They begrudgingly get COVID-19 vaccines and flu vaccines. So, we definitely don’t want those people talking about it. – Urban #17, Physician (Pediatrician), 18 years in role

Theme 2: choice vs authority

Rural and urban providers noted that some rural residents valued personal choice in their healthcare decisions, particularly in opposition to traditional authority figures, such as urban public health officials or physicians. Some rural providers felt this value interfered with common advice to use presumptive language in vaccine conversations.

A few urban providers mentioned that they found presumptive language to be a helpful tool:

It’ll be mentioned by support staff that, you know, here’s the vaccines your child is due for today, and that’ll be one mention. And then when I get to the vaccine part,… I usually put it in between at that point Tdap and Menveo so it’s just mentioned as the second vaccine required. – Urban #16, Physician (Pediatrician), 30 years in role

However, multiple rural providers mentioned that their patients hold a strong value of personal choice and independence in the face of authority:

I’ve lived rural my whole life. Obviously in school I was in more urban areas. But there is a huge level of, prior to COVID even, a huge level of distrust when it comes to rural people and the city telling them what to do. – Rural #8, Physician, 13 years in role

Perhaps in response to this rural value of choice, both urban and rural participants thought rural providers were less likely to use presumptive language in their vaccine recommendations. Some rural participants felt that discarding presumptive language allowed them to maintain trusting patient relationships and provide better care. However, nearly all rural participants expressed some support for presumptive language and mandates, even while recognizing the importance of maintaining patient relationships and patient choice. At least one urban provider believed that reluctance of rural providers to use presumptive language may partially explain lower coverage in rural areas.

I don’t necessarily want to come off pushy. I know sometimes it’s –it’s almost easier to have better compliance if you just don’t give people a choice. But … I like to really get a knowledge of what my patients come into the clinic with and then, discuss their reasoning behind why they would, take a vaccine or wouldn’t take a vaccine and then, basically try to see if there [are] any myths that we can try to debunk. – Rural #11, Physician Assistant, 6 years in role

I think to me one reason the rural section is less [vaccinated] is that vaccines aren’t necessarily promoted as, this is what your child should get. I think it’s presented to them, this is optional. – Urban #16, Physician (Pediatrician), 30 years in role

Theme 3: misinformation and reasons for vaccine hesitancy

Both urban (11/13) and rural (4/7) providers highlighted the role of misinformation in vaccine hesitancy, particularly in the era of social media ().

I feel like the power of social media is something that’s just roaring, you know, fast and loud. And you know, I think, too, as people tend to access social media, and I’ve seen things out there too, I think just getting good information on there is going to be important. – Rural #11, Physician Assistant, 6 years in role

Some rural providers mentioned that misinformation was especially impactful in smaller communities:

Those people that are way out there on the fringe, you know, in a town of 400,000 or a city of 400,000, yeah, nobody hears it. But when these people are standing up at church meetings in a small town of 3,000 and saying that, it – unfortunately, there is just people that instead of looking at those they trust for every other part of their healthcare and saying, what do you think, they’re listening to these people that are just – have no idea what they’re talking about. – Rural #8, Physician, 13 years in role

Both rural and urban providers mentioned that misinformation fuels a common perception among parents that their children do not need the HPV vaccine because they are not sexually active. Some providers perceived that this belief might be more common in rural areas.

So, you know, we have a lot of very – a much more conservative base, I would say, than, you know, in the [Twin] Cities. So, we have a lot of patients that even before COVID with the HPV, there is still a lot of this, just, misinformation about, well, you’re just giving them this and then it’s okay for them to go screw around, you know, type of mentality. – Rural #8, Physician, 13 years in role

Theme 4: the impact of the COVID-19 pandemic

Both urban and rural participants described dramatic changes in the adolescent vaccine conversation in wake of the COVID-19 pandemic and vaccine rollout. Many providers reported that HPV vaccine hesitancy was not necessarily related to COVID-19 vaccine hesitancy:

So those people who are choosing – who aren’t embracing vaccines in general certainly aren’t going to embrace the COVID vaccine. But there’s a whole lot of people that embrace all other vaccines and just won’t do the COVID vaccine. And that includes HPV. They don’t question the HPV shot. – Rural #7, Physician (Family Medicine), 28 years in role

However, others felt that COVID-19 vaccine hesitancy was spreading to other vaccines, including HPV:

Like I said, I’ve been doing this for 30 years. I do think I felt like HPV rates were increasing. Then COVID hit, and we had a lot of vaccine hesitancy about the COVID vaccine, and that has carried over to HPV in a really negative way. Now all the sudden there’s more hesitancy about that. – Urban #14, Physician (Pediatrician), 29 years in role

According to participants, the three themes differentiating rural and urban HPV vaccine attitudes (choice, misinformation, and the patient-provider relationship) have been heightened during the COVID-19 pandemic.

Highlighting the value of choice, participants reported that more patients feel that they should be doing their own research and making their own choices about vaccines.

Yeah, there’s a little bit more questioning that’s going on. I mean, we’ve had to do some more education than we used to have to do. Which isn’t a bad thing. I mean, it’s a good idea to know what you’re getting and why. But, yeah, it’s different now. The last couple years have been different. – Rural #6, Clinic Manager and Immunization Manager, 2 years in role

Rural participants also reported strong local resistance to COVID-19 vaccine mandates:

All of a sudden once it flipped to mandates, it was, like, angry people, abusive people, people coming in, like, swearing at staff, thrashing at them, like, it just was like a hazard to the immunization clinic to have these folks in there. – Rural #6, Clinic Manager and Immunization Manager, 2 years in role

Participants also reported that vaccine misinformation has increased with the rollout of the COVID-19 vaccine.

Think it’s just because the COVID vaccine is based so much around such a hot topic, and there’s so many conspiracy theories about COVID itself that people’s minds just twist. – Rural #3, Registered Nurse Supervisor, 2 years in role

Some participants also reported that patients’ anger regarding COVID-19 vaccines has strained the patient-provider relationship, which may be particularly taxing in close-knit rural communities.

I’ve been here for quite a while. Like I said, I’m our hospice medical director. So these are people that — I mean, I’ve been in some pretty not pleasant situations taking care of their loved ones and suggesting, hey, we need to do this or we need to do that, and they don’t question it ever. And from the beginning of [the pandemic], there’s just a huge level of distrust … – Rural #8, Physician, 13 years in role

Ultimately, both urban and rural participants reported that the political nature of the COVID-19 pandemic and strong anti-COVID-19 vaccine sentiment kept them from discussing vaccines with their patients. While much of this anger is directed at COVID-19 restrictions overall and mandates, there was additional anger directed specifically at the COVID-19 vaccine, even in settings (such as pediatrics) where COVID-19 vaccines were not likely to be mandatory.

all of a sudden there’s politics involved and some people are believing that, like, if you’re right or left or whatever – they’re the ones that created this vaccine … you hear a lot of just – crazy stories of why people are not getting vaccinated – Rural #2, Pharmacy Manager, 6 years in role

Quite frankly, I haven’t brought [the COVID-19 vaccine] up recently unless someone has asked me about it. Again, trying to preserve my mental health over the last two years. We were — it was pretty rough. – Urban #18, Physician (Pediatrician), 22 years in role

Discussion

This study investigated urban and rural provider strategies and experiences with HPV vaccination in Minnesota. Urban and rural providers generally employed similar strategies to increase vaccination in their clinics, but rural providers identified several unique aspects of working in communities that appeared to make HPV vaccination conversations particularly challenging, including the strong value of choice and harm from misinformation in small communities. Conversely, tight-knit, multi-role patient-provider relationships were both an asset and a challenge to rural providers.

Most providers described similar immunization strategies to those identified in other studies of healthcare providers in Minnesota and throughout the United States.Citation17,Citation18 The rural providers we interviewed were generally aware of evidence-based strategies to improve vaccinations and implemented them whenever possible and previous quantitative work largely corroborates this finding. For example, in a survey of urban and rural providers in Minnesota and Wisconsin, rural providers were more likely than urban providers to have standing orders to administer all recommended adolescent vaccines and provide HPV vaccine information to families before it is due.Citation19 However, some providers we interviewed believe that recommended practices, particularly presumptive language, are at odds with the rural value of choice, and can damage patient-provider relationships.

Most participants highlighted the importance of the patient-provider relationship. Prior studies confirm that this relationship can be a persuasive tool in vaccine conversations in rural clinical settings, but can also be fragile.Citation20–22 Parents cite providers who do not make time to answer vaccine questions as a barrier to vaccination.Citation20

Rural providers also reported a perception that misinformation can be more impactful in small communities compared to urban communities, and described common patient worries about HPV vaccine safety. This finding is also reflected in a previous survey, which found that rural parents were more likely than urban parents to worry that the HPV vaccine might cause lasting harms.Citation23

These findings can be contextualized using the Theory of Planned Behavior.Citation24,Citation25 This model of behavior hypothesizes that individuals’ intentions and subsequent actions are informed by a combination of individual beliefs and subjective norms. Individual beliefs and perceptions of norms can be influenced by personal experiences, demographics, culture knowledge, values, and personality. Common provider strategies such as presumptive language and the sandwich method attempt to shift patient perceptions of community norms, by signaling that the HPV vaccine is uncontroversial and widely accepted in the community. However, in rural settings, personal beliefs in independence and choice – and therefore a prioritization of personal belief over normative perceptions – may conflict with this strategy. Conversely, presumptive language may be an effective strategy to circumvent conversations about patient choice versus provider recommendations. Several providers mentioned a nuanced approach to this dilemma, where they defaulted to a brief, presumptive vaccine discussion, but made space and used their long-term relationships and prior knowledge of their patients to have more open-ended, less authoritarian conversations if needed. Furthermore, widespread misinformation may impact personal beliefs, regardless of the educational efforts (such as a focus on cancer prevention) of providers. Since the beliefs of healthcare providers may be less influential in rural areas that value personal beliefs over authority or social norms, it may be particularly difficult for providers to gain patient trust in these settings using the presumptive approach.

During the 2009 H1N1 influenza pandemic, Danielle Ofri described an “emotional epidemiology” of pandemic immunization campaigns, in which social groups fuel each other’s eagerness for solutions, safety fears, and impatience, resulting in emotional surges that aren’t necessarily caused by the virus itself or scientific progress on the vaccines.Citation26 Vaccine hesitancy has been more common during the COVID-19 vaccine pandemic than the H1N1 pandemic, in part because the H1N1 vaccine was a licensed vaccine product using long-standing methods and there was a lack of mandates except in some healthcare settings based on individual facility decision making. However, the pattern Ofri describe is reflected in the COVID-19 experiences of both urban and rural participants, who were wary of patient vaccine hesitancy and anger over vaccine mandates.

Participants in both urban and rural areas also mentioned that COVID-19 vaccine hesitancy damaged their ability to create a clinical culture of immunization. Vaccine hesitant staff were discouraged from discussing vaccines with patients. In small communities, perceived silencing of hesitant providers by their clinics may harm patient trust and exacerbate the impression that healthcare settings are authoritarian figures in society. Conversely, research has shown benefits of unified, pro-vaccine messaging across the entire clinic staff. More research is needed on how to reconcile these conflicting priorities in rural settings. Further harming clinical pro-vaccine culture, even staff and providers who were enthusiastic about vaccines reported that they were less likely to mention vaccines because of fears of patient anger.

Participants reported that strong emotions about the COVID-19 vaccine enhanced certain differences between urban and rural patients. Specifically, rural patients were more committed to individual choice and self-determination and exposed to more misinformation and disinformation than they had been before the pandemic. Patient-provider relationships frayed because of this growing tension. Thus, it is growing more important to consider the role of unique social norms of rural communities in vaccine hesitancy. To best understand how to address vaccine hesitancy in rural areas, evaluations of provider strategies to improve adolescent vaccination coverage should include rural providers and patients and consider their unique experiences.

Limitations

All participants had positive views on the HPV and COVID vaccines, and many held vaccine-related leadership roles in their clinics. Interview questions were framed to be neutral; however, providers and staff who had negative views may have been less likely to respond to our recruitment efforts. We made several efforts to recruit participants with a diversity of perspectives and experiences with adolescent vaccination, by including nurses and clinic staff as well as primary care providers, and prioritizing recruitment of individuals from clinics with low HPV-vaccination coverage rates. However, individuals with knowledge of vaccination best practices and positive perceptions of vaccines were likely overrepresented, and HPV-vaccination coverage was similar in urban and rural clinics included in our sample. Inclusion of vaccine hesitant providers, particularly among providers who reject certain vaccines but accept others (for example, those who discourage HPV vaccines for religious reasons), may have provided further insight into the perspectives of vaccine hesitant patients and added nuanced insight to how patient concerns can be addressed.

While the inclusion of clinic staff (other than providers such as physicians and physician assistants) provided insight into the clinic-wide vaccine landscape, clinical roles were not equally distributed among urban and rural strata. While nearly all urban participants were physicians or physician assistants, over half of rural participants held other staff roles in their clinics. This discrepancy may partially explain the differences observed between urban and rural participants.

Of providers who reported race and ethnicity information, nearly all (and all rural participants) were White and non-Hispanic. Participants did not reflect the racial and ethnic makeup of urban or rural Minnesota, and we may have missed nuance in the experiences of non-White and/or Hispanic Minnesotan providers.

Because providers were divided into rural and urban strata at the county level, some providers classified as urban may share experiences with rural providers, because they are located at the edge of an urban area and serve suburban and/or rural patients. A more granular definition of rurality may have revealed more nuanced patterns and themes.

These interviews were conducted in the winter of 2022, a time of high COVID-19 incidence and hospitalization fueled by Delta and Omicron variants. This has been noted as an exceptionally difficult time for healthcare providers,Citation27,Citation28 and participant observations may reflect conditions, emotions, and burnout that have since improved. In addition, the uniquely stressful timing may have further discouraged vaccine hesitant or poorly resourced providers from participating. However, we believe the timing of these interviews is also a strength, since the impact of the COVID-19 pandemic on the experiences of healthcare providers may last for years, and research conducted before 2020 may not fully reflect the current vaccine ecosystem.

Conclusion

The providers in this study offered new insights into urban-rural challenges with HPV vaccination. Although both urban and rural providers used similar strategies to persuade hesitant parents to immunize their children, rural providers highlighted that the values of choice and independence and heightened vaccine misinformation make it more difficult to encourage hesitant families to vaccinate their children. Interventions designed to increase HPV vaccination should take the unique cultural values of rural patients into account.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

This work was funded by cooperative agreement 5U01 IP001093 with the U.S. Centers for Disease Control and Prevention (CDC). CDC scientists participated in data interpretation, preparation, review and approval of the manuscript for publication. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the CDC.

References

  • Deshmukh AA, Suk R, Shiels MS, Damgacioglu H, Lin Y-Y, Stier EA, Nyitray AG, Chiao EY, Nemutlu GS, Chhatwal J, et al. Incidence trends and burden of human papillomavirus-associated cancers among women in the United States, 2001-2017. JNCI J Nat Cancer Inst. 2021;113(6):792–8. doi:10.1093/jnci/djaa128.
  • Lei J, Ploner A, Elfström KM, Wang J, Roth A, Fang F, Sundström K, Dillner J, Sparén P. HPV vaccination and the risk of invasive cervical cancer. N Engl J Med. 2020;383(14):1340–1348. doi:10.1056/NEJMoa1917338.
  • Prevention CfDCa. Vaccination coverage among adolescents (13-17 years). Centers for Disease Control and Prevention. [accessed 2023 Apr 6]. https://www.cdc.gov/vaccines/imz-managers/coverage/teenvaxview/data-reports/index.html.
  • Adolescent immunization coverage in Minnesota. Minnesota department of Health. [accessed 2023 Apr 6]. https://www.health.state.mn.us/people/immunize/stats/adol/coverdata.html.
  • He K, Mack WJ, Neely M, Lewis L, Anand V. Parental perspectives on immunizations: impact of the COVID-19 pandemic on childhood vaccine hesitancy. J Community Health. 2022;47:1–14. doi:10.1007/s10900-021-01017-9.
  • Saelee R, Zell E, Murthy BP, Castro-Roman P, Fast H, Meng L, Shaw L, Gibbs-Scharf L, Chorba T, Harris LQ, et al. Disparities in COVID-19 vaccination coverage between urban and rural counties—United States, December 14, 2020–January 31, 2022. Morb Mort Wkly Rep. 2022;71(9):335. doi:10.15585/mmwr.mm7109a2.
  • Jacobson RM, St SJ, Griffin JM, MacLaughlin KL, Finney Rutten LJ. How health care providers should address vaccine hesitancy in the clinical setting: evidence for presumptive language in making a strong recommendation. Hum Vaccin Immunother. 2020;16(9):2131–5. doi:10.1080/21645515.2020.1735226.
  • King AR, Moon T, Agnew G, Bednarczyk RA. Human papillomavirus vaccination in Georgia: evaluating the Georgia HPV work group. J Community Health. 2019;44(3):428–35. doi:10.1007/s10900-018-00598-2.
  • Zimet G, Dixon BE, Xiao S, Tu W, Kulkarni A, Dugan T, Sheley M, Downs SM. Simple and elaborated clinician reminder prompts for human papillomavirus vaccination: a randomized clinical trial. Acad Pediatr. 2018;18(2):S66–S71. doi:10.1016/j.acap.2017.11.002.
  • Fiks AG, Grundmeier RW, Mayne S, Song L, Feemster K, Karavite D, Hughes CC, Massey J, Keren R, Bell LM, et al. Effectiveness of decision support for families, clinicians, or both on HPV vaccine receipt. Pediatrics. 2013;131(6):1114–24. doi:10.1542/peds.2012-3122.
  • Matheson EC, Derouin A, Gagliano M, Thompson JA, Blood-Siegfried J. Increasing HPV vaccination series completion rates via text message reminders. J Pediatr Health Care. 2014;28(4):e35–e9. doi:10.1016/j.pedhc.2013.09.001.
  • Chao C, Preciado M, Slezak J, Xu L. A randomized intervention of reminder letter for human papillomavirus vaccine series completion. J Adolesc Health. 2015;56(1):85–90. doi:10.1016/j.jadohealth.2014.08.014.
  • Holloway GL. Effective HPV vaccination strategies: what does the evidence say? An integrated literature review. J Pediatr Nurs. 2019;44:31–41. doi:10.1016/j.pedn.2018.10.006.
  • P-J L, Yankey D, Jeyarajah J, O’Halloran A, Elam-Evans LD, Smith PJ, Stokley S, Singleton JA, Dunne EF. HPV vaccination coverage of male adolescents in the United States. Pediatrics. 2015;136(5):839–849. doi:10.1542/peds.2015-1631.
  • Oh NL, Biddell CB, Rhodes BE, Brewer NT. Provider communication and HPV vaccine uptake: a meta-analysis and systematic review. Prev Med. 2021;148:106554. doi:10.1016/j.ypmed.2021.106554.
  • Guest G, Bunce A, Johnson L. How many interviews are enough? An experiment with data saturation and variability. Field Method. 2006;18(1):59–82. doi:10.1177/1525822X05279903.
  • Yared N, Malone M, Welo E, Mohammed I, Groene E, Flory M, Basta NE, Horvath KJ, Kulasingam S. Challenges related to human papillomavirus (HPV) vaccine uptake in Minnesota: clinician and stakeholder perspectives. Cancer Cause Control. 2021;32(10):1107–1116. doi:10.1007/s10552-021-01459-5.
  • Gilkey MB, Grabert BK, Malo TL, Hall ME, Brewer NT. Physicians’ rhetorical strategies for motivating HPV vaccination. Soc Sci Med. 2020;266:113441. doi:10.1016/j.socscimed.2020.113441.
  • Goessl CL, Christianson B, Hanson KE, Polter EJ, Olson SC, Boyce TG, Dunn D, Williams CL, Belongia EA, McLean HQ, et al. Human papillomavirus vaccine beliefs and practice characteristics in rural and urban adolescent care providers. BMC Public Health. 2022;22(1):1322. doi:10.1186/s12889-022-13751-3.
  • Thomas M, Kohli V, King D. Barriers to childhood immunization: findings from a needs assessment study. Home Health Care Serv Q. 2004;23(2):19–39. doi:10.1300/J027v23n02_02.
  • Wilson T. Factors influencing the immunization status of children in a rural setting. J Pediatr Health Care. 2000;14(3):117–21. doi:10.1016/S0891-5245(00)70022-8.
  • Mical R, Martin-Velez J, Blackstone T, Derouin A. Vaccine hesitancy in rural pediatric primary care. J Pediatr Health Care. 2021;35(1):16–22. doi:10.1016/j.pedhc.2020.07.003.
  • Boyce TG, Christianson B, Hanson KE, Dunn D, Polter E, VanWormer JJ, Williams CL, Belongia EA, McLean HQ. Factors associated with human papillomavirus and meningococcal vaccination among adolescents living in rural and urban areas. Vaccine. 2022;11:100180. doi:10.1016/j.jvacx.2022.100180.
  • Ajzen I. From intentions to actions: a theory of planned behavior. Action Control. 1985;1:11–39.
  • De Leeuw A, Valois P, Ajzen I, Schmidt P. Using the theory of planned behavior to identify key beliefs underlying pro-environmental behavior in high-school students: implications for educational interventions. J Environ Psychol. 2015;42:128–38. doi:10.1016/j.jenvp.2015.03.005.
  • Ofri D. The emotional epidemiology of H1N1 influenza vaccination. N Engl J Med. 2009;361(27):2594–5. doi:10.1056/NEJMp0911047.
  • Khan NH, Hassan S, Bahader S, Fatima S, Zaidi SMIH, Virk R, Jiang K, Jiang E. How daily obstacles affect frontline healthcare professionals’ mental health during omicron: a daily diary study of handwashing behavior. Int J Env Res Pub He. 2022;19(14):8748. doi:10.3390/ijerph19148748.
  • Swed S, Bohsas H, Alibrahim H, Hafez W, Shoib S, Sawaf B, Rais MA, Aljabali A, Shaheen N, Elsayed M, et al. Health-care provider burnout in Syria during COVID-19 pandemic’s omicron wave. Medicine. 2022;101(50):e32308. doi:10.1097/MD.0000000000032308.