Practice-, provider- and patient-level facilitators of and barriers to HPV vaccine promotion and uptake in Georgia: a qualitative study of healthcare providers’ perspectives

Abstract

Georgia experiences higher human papillomavirus (HPV)-associated cancer burden and lower HPV vaccine uptake compared with national estimates. Using the P3 model that concomitantly assesses practice-, provider- and patient-level factors influencing health behaviors, we examined facilitators of and barriers to HPV vaccine promotion and uptake in Georgia. In 2018, we conducted six focus groups with 55 providers. Questions focused on multilevel facilitators of and barriers to HPV vaccine promotion and uptake. Our analysis was guided by the P3 model and a deductive coding approach. We found that practice-level influences included organizational priorities of vaccinations, appointment scheduling, immunization registries/records, vaccine availability and coordination with community resources. Provider-level influences included time constraints, role, vaccine knowledge, self-efficacy to discuss HPV vaccine and vaccine confidence. Patient-level influences included trust, experiences with vaccine-preventable diseases, perceived high costs, perceived side effects and concerns with sexual activity. Findings suggest that interventions include incentives to boost vaccine rates and incorporate appointment scheduling technology. An emphasis should be placed on the use of immunization registries, improving across-practice information exchange, and providing education for providers on HPV vaccine. Patient–provider communication and trust emerge as intervention targets. Providers should be trained in addressing patient concerns related to costs, side effects and sexual activity.

Introduction

Human papillomavirus (HPV) is a known cause of several types of cancers, including cervical, oropharyngeal, vulvar, vaginal, penile and anal cancers [1]. From 2008 to 2012, the annual incidence rate of HPV-associated cancers in the United States was 11.7 (13.5 among females and 9.7 among males) per 100 000 persons [2]; in 2015, this rate was 12.1 (13.6 among females and 10.5 among males) per 100 000 persons [3]. The state of Georgia has slightly higher HPV-associated cancer rates compared with US national estimates; from 2008 to 2012, the annual incidence rate for HPV-associated cancers in Georgia was 12.6 (14.3 among females and 10.7 among males) per 100 000 persons [2].

HPV vaccine is a safe and effective method for protection against genital warts and HPV-caused cancers [1]. The 2018 CDC National Immunization Survey (NIS)-Teen showed that the initiation rate for HPV vaccine uptake in Georgia for those aged 13–17 (68.1%) was similar to the national estimate (68.1%) but the completion rate (49.6%) was slightly lower than the national estimate (51.1%) [4]. The 2018 Georgia Adolescent Immunization Survey, which focused on seventh graders, reported rates of 50.6% for initiation and 23.4% for up to date on HPV vaccine uptake [5]. Moreover, a 2016 survey of students at seven colleges and universities in Georgia found lower prevalence of vaccine initiation (43.3% for women and 16.7% for men) [6] compared with nationwide college-aged students (68.9% for women and 42.9% for men) [7].

With a population of 10.6 million, Georgia is diverse in terms of race and ethnicity (32.6% Black, 9.9% Hispanic/Latinos, 4.4% Asians and 10.1% foreign-born) and socioeconomic status (14.3% living in poverty and 15.7% under the age of 65 living without health insurance) [8]. In comparison, the US population as a whole is 13.4% Black, 18.5% Hispanic/Latinos, 5.9% Asians, and 13.5% foreign-born; in addition, 11.8% of US population is living in poverty and 10.0% under the age of 65 is living without insurance [9]. In order to increase HPV vaccine uptake (which could reduce HPV-associated cancer burden) in Georgia, researchers need to account for local contextual determinants and examine state-specific facilitators of and barriers to vaccine promotion.

Little research has targeted these questions in Georgia. A recent systematic review found only five published articles that focused on Georgia-specific facilitators of and barriers to HPV vaccine promotion and uptake [10]. An important finding from this review concerned how HPV vaccination needs and promotion of cervical cancer prevention were lacking significantly or only briefly mentioned in Georgia hospital and county-level community needs assessments [10]. This review also identified state-level initiatives (e.g. the Georgia Comprehensive Cancer Control Plan) aiming to increase adolescent HPV vaccine coverage and encouraging pediatricians’ routine vaccine recommendation (note that, however, missing from the picture is any statewide policy or mandate to educate parents and adolescents about HPV vaccine) [10, 11]. Additionally, the review discussed various barriers to HPV vaccine in Georgia. For example, among Hispanic populations in the state, fears of embarrassment or stigma, lack of knowledge about HPV, cultural acceptability of sexual behavior, low English proficiency, distrust of healthcare and general lack of information were prominent barriers [12, 13]. In rural communities in Georgia, people reported a fear of social judgment for getting HPV vaccine [14]; local culture also exercised impacts on people’s perceptions of risk and access to information and preventive care [15]. These issues merit additional exploration.

Lacking from the current literature, however, is research that focuses on healthcare providers’ perceptions of facilitators of and barriers to HPV vaccine uptake in Georgia. While healthcare providers play a fundamental role in increasing HPV vaccine uptake [16], to our knowledge, currently only one study has examined perspectives of healthcare providers in Georgia on HPV vaccine [13]. This study also focused on providers serving a specific immigrant population in rural areas of the state as opposed to sampling providers from different regions within Georgia. As Georgia experiences a large rural–urban divide in health status [17], it is important for researchers to collect data from providers serving rural as well as urban areas to understand aggregated facilitators and barriers.

Collectively, aforementioned findings highlight the need for additional research incorporating perspectives of providers from different regions of Georgia to understand facilitators of and barriers to HPV vaccine promotion and uptake in the state. Moreover, limited research has leveraged a multilevel theoretical framework that incorporates aspects related to health systems, healthcare providers, and parents and adolescents to explore these facilitators and barriers. Health behaviors and outcomes are not just driven by individual-level factors but are often results of a dynamic interplay between factors at multiple socioecological levels (e.g. individuals' behavioral patterns; the physical, social, cultural and economic contexts; and broader healthcare environment [18–20]).

Our study attempts to fill the abovementioned gaps in the literature by using a multilevel framework to examine facilitators of and barriers to HPV vaccine promotion and uptake in Georgia. The P3 model was designed to examine practice-, provider- and patient-level factors that influence preventive health behaviors (e.g. HPV vaccine uptake) [21]. The model overcomes existing limitations in the literature by accounting for different components of the health system beyond individual-level factors. In this study, we focus on the perspectives of healthcare providers from diverse backgrounds and recruited from five different geographic regions in Georgia.

Methods

Setting and recruitment

Between April and July 2018, we conducted six focus group discussions (FGDs) with 55 healthcare providers throughout the state of Georgia. Healthcare providers came from diverse backgrounds and included physicians, nurses, medical assistants, physician assistants and other practice staff members. The study was approved by the Institutional Review Board at Emory University.

The research team worked closely with community-based organizations (CBOs) (e.g. regional cancer coalitions or immunization coalitions) to set up and recruit for FGDs. Participants were eligible if they worked in a healthcare practice that interacted with adolescent patients, were over 18 years old, and could speak, read, write and understand English. CBO staff members reached out to healthcare practices directly and recruited FGD participants for the study. All participants in the study provided written informed consent. Each participant was offered a $30 gift card as a compensation for participation.

To provide representation throughout the state of Georgia, we conducted at least one focus group in five different geographic regions (Northwest, East, Southeast, South and Southwest ). We expected to reach thematic saturation with six focus groups. Past research on sample sizes for qualitative studies has suggested that four focus groups were sufficient to identify a range of new issues (code saturation) [22] and that 90% of qualitative themes can be discovered within three to six focus groups [23].

Focus group questions

We explored multilevel facilitators of and barriers to HPV vaccine promotion and uptake that healthcare providers observed in their practices. Examples of questions included ‘What are some of the structural or logistical issues that may make recommending HPV vaccine difficult?’; ‘Please explain your level of comfort/level of confidence in discussing HPV vaccine’.; ‘What do you tell your patients and/or their family about the human papillomavirus (HPV)?’ and ‘What do you think are the most significant barriers for adolescents and young adults to receive HPV vaccine?’

Analysis

All FGDs were audio recorded and transcribed verbatim. All transcriptions were stored on a password-protected server with restricted access to only research team members. The research team uploaded all transcribed data from FGDs to MAXQDA 2018 (VERBI GmbH, Berlin, Germany) for analysis. We used a deductive coding approach [24]. Two researchers (M.V. and A.K.) read two transcripts to identify common codes and themes present across the data. We developed a codebook with definitions, inclusion criteria, exclusion criteria, and examples for each code. The two researchers then applied this codebook to the remaining transcripts. Coding results were compared in team meetings and emerging themes were identified and discussed. Using the P3 model [21] as the guiding framework, codes were indexed based on each level of influence (i.e. practice-, provider- and patient-level) and presented by levels of influence in the analysis.

Results

Six FGDs were held with 55 providers. Table I shows sociodemographic characteristics of providers. Table II summarizes perspectives of healthcare providers on key practice-, provider- and patient-level influences on HPV vaccine promotion and uptake in the state of Georgia.

Table I.

Sociodemographic characteristics of focus group participants

Sociodemographic characteristics	N or M	% or SD
Sex
Male	7	12.7%
Female	48	87.3%
Clinical role
Nurse practitioner, nurse, nurse manager or nurse navigator	17	30.9%
Medical assistant or physician’s assistant	4	7.3%
Health educator	1	1.8%
Pharmacist	1	1.8%
Physician	6	10.9%
Practice manager/administrator	3	5.5%
Non-specific office or medical staff	18	32.7%
Other clinical staff	5	9.1%
Region
Northwest	8	14.5%
East	8	14.5%
South	8	14.5%
Southeast	22	40.0%
Southwest	9	16.4%
Years of experience in healthcare (range 0.5–43)a	16.1	10.0

^aData were missing for 23 participants.

Table II.

Summary of practice-, provider- and patient-level influences on HPV vaccine promotion and uptake

Category	Influence
Practice-level influences
Facilitator	Organizational priorities of vaccinations
Facilitator	Scheduling of future HPV vaccine doses for patients
Facilitator and barrier	Georgia Registry of Immunization Transactions and Services and other systems for immunization medical records
Facilitator	Availability of HPV vaccine at healthcare practices
Facilitator	Ability to coordinate with community resources
Provider-level influences
Barrier	Time constraints
Facilitator and barrier	Clinical role (e.g., nurses are more readily available to talk to patients about HPV vaccine compared with physicians)
Facilitator	Knowledge of HPV vaccine
Barrier	Lack of knowledge or low knowledge of HPV vaccine
Facilitator	Self-efficacy to discuss HPV vaccine with patients
Barrier	Lack of self-efficacy to discuss HPV vaccine with patients
Barrier	Lack of confidence in HPV vaccine
Patient-level influences
Facilitator	Patient’s trust in provider
Facilitator	Experiences with vaccine-preventable diseases
Barrier	Lack of experiences with vaccine-preventable diseases
Barrier	Perceived high costs of HPV vaccine
Barrier	Perceived side effects of HPV vaccine
Barrier	Concerns with sexual activity

Practice-level influences

Organizational priorities emerged as a key theme influencing providers’ push for HPV vaccine. A physician explained that his practice strongly prioritized vaccinations: ‘In primary care we are very aggressive with vaccines… [Patients] come for sick visits… annual physical exams… that’s when you do address the vaccines… Every visit, regardless of what they are here for, we check their vaccine status…’ Participants also highlighted the importance of scheduling future HPV vaccine appointments for patients before they left the first vaccination appointment. A nurse shared: ‘Scheduling appropriate appointments and appropriate time frames… we’re pretty good about that because everybody knows every year and up to a year what those regiments at the well child check appointments are’. A physician said, ‘You’re not going to leave without a follow up appointment scheduled… get that on the books, and we have the automated systems for reminders’.

Additionally, participants discussed the utility of the Georgia Registry of Immunization Transactions and Services (GRITS) in helping providers to identify HPV vaccination needs and to recommend HPV vaccine to patients. A medical assistant said, ‘I always pull the GRITS up, and if… I see that this or anything hasn’t been done, I put it in the chart to bring it to my provider’s attention’. A nurse explained: ‘If you have a GRITS account you can just log in there, put in the patient’s name and date of birth, and it’ll pull up everybody’s, I mean all the vaccines they’ve ever received… It gives you a recommended date and the earliest you can receive it’. A medical assistant discussed how GRITS helped identifying patients with vaccination needs: ‘If we had a new patient we would certainly look on to see if they had a GRITS account… If they were coming in for an acute visit we would say we know we are seeing you for this today but… you are recommended to have these vaccines so please schedule a well check’.

A few participants reported encountering issues with GRITS. For example, a clinical supervisor mentioned that ‘GRITS goes down’ and that ‘people don’t enter things [into GRITS] right, if they’re from a different part of Georgia it might not come in right’. Others also echoed that they occasionally encountered incorrect information listed in GRITS. As an alternative to GRITS, some participants said that their practice used the Comprehensive Clinic Assessment Software Application (CoCASA), a software that could be used for internal practice assessment and could generate reports on vaccination coverage. A healthcare administrator mentioned using CoCASA to generate reports, letters and alerts for patients and providers. They stated ‘[CoCASA has] letters in there that get sent to the patients, I mean they have a myriad of things that we can use… I can flag the chart stating that this is what the child needs the next time they comes in… If they’re behind they are going to do what they need to do to get caught back up’. The same participant also mentioned that their practice used their EMR system and GRITS in conjunction with one another.

Finally, some participants also mentioned that the availability of HPV vaccine at healthcare practices as well as the ability to coordinate with community resources was essential to HPV vaccine promotion. For example, a nurse reported: ‘Most of the vaccination we do have it in the refrigerator…If [we] were out of it or something, we [recommend patients] to go to the health department, which is, every county has one…’ A physician said: ‘I think the engagement between the public health department and the provider on the ground, at least for me, I think we’ve seen successful example of that in partnering with my local counterparts…’

Provider-level influences

For providers, time constraints during a visit were mentioned as an important factor limiting their ability to discuss HPV vaccine with their patients. A physician said, ‘Time is definitely a factor. Because they’re here with a sick visit… In that ten minutes we’ve got to address that day’s issue and on the top of it, HPV vaccine. And if they’ve already refused the vaccine, we need more time’. Related to time constraints, compared with physicians, other providers or staff might be more readily available to talk about HPV vaccine with patients. A participant said, ‘And [the doctors are] also not going to take the time to go into a detailed discussion because their goal is to look at what the issue is and move on to the next one… That responsibility [of discussing the vaccine] does fall back on that nurse or that medical office assistant or whomever is available’. A nurse noted, ‘A lot of time the nurse’s recommendation, it goes a lot further than the M.D.s. I have experienced several patients… They don’t know, the doctor did not even tell them’.

Moreover, providers’ knowledge of HPV vaccine and self-efficacy to discuss HPV vaccine with patients frequently came up. Some providers expressed that they were comfortable discussing HPV vaccine with patients. A nurse said, ‘I have no reservation about it… it’s just an everyday thing’. However, for others, a lack of knowledge of HPV vaccine and vaccine recommendation guidelines was a challenge. A clinical supervisor said, ‘One of our doctors, we hired him last year, he said, “I’m just going to be honest with you. They don’t teach us this in residency. They don’t teach us this anywhere, I don’t know my shots at all”.’ Another nurse suggested educating providers about vaccination guidelines: ‘We should train physicians to always be, monitoring for, and applying the current state of knowledge… As long as we’re doing our best to act upon what the evidence would suggest as best practices… So, our thing would be dedicated education initiative… We brought in pharmaceutical representatives and vaccine representatives to come in to educate the faculty as well as staff, in addition to the residents’.

In addition, a few providers mentioned instances where they observed other providers discussing a lack of confidence in HPV vaccine. Provider’s lack of vaccine confidence was a barrier to vaccine recommendation for patients. For example, a participant (healthcare practice staff with non-clinical duties) said, ‘My doctor said that there wasn’t enough research to [recommend HPV vaccine]… He was like, I don’t know about these side effects from it and there isn’t enough research out there for me to really recommend it… it’s up to you but I really can’t recommend it at this time…’

Another physician talked about ‘the onus of education’ that fell on healthcare providers to acquire considerable knowledge of HPV vaccine to address potential questions from patients. He said, ‘the challenge for healthcare providers is that we really have to own the entirety of literature… where as it only takes one comment, one article whatever, to really influence a family member to a very firm point. So unless you’re prepared to go over that specific concern when it’s raised in the room by a family member, you immediately get discounted as a medical provider…’ The same physician reiterated this point later in the discussion, stating, ‘It just takes one encounter where you and your team are not viewed as expert[s] and you are immediately no longer valued in that discussion’. A healthcare company staff member highlighted the importance of being able to address questions from patients about HPV vaccine: ‘It starts with the receptionist, it starts with the front desk, it starts with the person who answers the phone, you know, “my child is getting shots tomorrow, how many are they getting, what are they getting?” I think they need to be somewhat educated on it to be ready to deliver certain answers to questions that parents have or get them to the right person’.

Others brought up resources they utilized to address questions from patients about HPV vaccine. An immunization coordinator said: ‘Somebody has a question or an issue I try to, you know, go to the [Immunization Action Coalition] or CDC and find my counter article and, you know, answer that question or present that issue… give them an opportunity to make an informed decision’.

Patient-level influences

When discussing factors that influenced caregivers’ and patients’ decision to get HPV vaccine, several providers talked about the importance of establishing trust. Trust in providers could be developed through either communication with caregivers and patients or through providers’ actions of vaccinating their own children. For example, a nurse described: ‘I feel that its trust and you give [parents] the information and they say, “Would you give [the vaccine] to your child?” and, and if you say, “Yes”, Then they say, “Let me think about it”’. Another provider said, ‘Having the bedside manner and the skillset to be able to talk to the patient in a way that, or the patient’s family, understands what it is that you’re trying to say and you do it in a way that is not unkind or condescending… It’s important to acknowledge the patients’ feelings because they’re not gonna [get the vaccine] if they don’t trust you’.

In addition, providers also reported that experiences with vaccine-preventable diseases (VPD) were central in influencing attitudes towards vaccination in general and HPV vaccine in particular. For example, a nurse described using personal anecdotes to encourage her patients to pursue HPV vaccine: ‘I’ll also tell them about the young professor that I knew. A man that had throat cancer and didn’t even know it was related to HPV… These are real stories, these are personal, and these are people I know personally…’ In contrast, providers also discussed how a lack of personal experience with VPDs made some patients less likely to believe in vaccine efficacy or the need for vaccination and make providers less likely to give strong recommendations. A nurse shared: ‘Because we in America have been very successful with vaccines, to the point where there are so many diseases that many doctors don’t, they’ve never seen… We’ve been very successful with vaccinating which may be hurting us now’.

Another issue influencing caregivers’ and patients’ HPV vaccine decision-making was perceived high costs. Not all parents were aware of the Vaccine for Children (VFC) program, which covers the costs of vaccinations for children through 18 years of age. When asked whether parents knew about VFC, a nurse said, ‘We have some parents that say, “I didn’t know you can come to the health department and get your vaccines…” I tell them “tell your friends, anyone you know that needs vaccines, and they don’t have insurance”.’

Moreover, many providers brought up challenges in discussing HPV vaccine with caregivers and patients who held negative beliefs about possible side effects of the vaccine. A nurse reported, ‘There was so much negative media coverage about [HPV vaccine] when it first started coming out. Parents are still retaining that mindset… they say… “I don’t trust that vaccine there’s too many side effects”.’ Another nurse described, ‘Sometimes you have parents that don’t want to vaccinate because they’ve read a lot of incorrect studies about how vaccines cause all sorts of different diseases’.

Providers also reiterated another barrier: the perceived approval of sexual initiation if the caregiver approved HPV vaccination. A participant said, ‘And then [parents] go back to the notion where they feel like HPV in particular would be, the vaccine in particular would be permission to go have sex’. This reaction led to certain providers framing discussions of HPV vaccine with caregivers to focus more on cancer prevention instead of sexually transmitted diseases. One participant said, ‘When it comes to the vaccine with me, I do not mention sex at all… It comes up but I try not to make it about sex… I say it’s the only thing we have preventing cancer’.

Discussion

Our study used the P3 model to investigate healthcare providers’ perspectives on facilitators of and barriers to HPV vaccine promotion and uptake in the state of Georgia. At the healthcare practice level, we documented several key influences, such as organizational priorities of vaccinations, ability to schedule future HPV vaccine doses for patients, use of immunization registries and medical records, availability of HPV vaccine at healthcare practices, and ability to coordinate with community resources. At the provider level, important emerging themes included time constraints, provider’s role (e.g. nurses versus physicians), knowledge of HPV vaccine, self-efficacy to discuss HPV vaccine, and HPV vaccine confidence. At the patient level, providers in our study noted issues related to patients’ trust, experiences with HPV vaccine-preventable diseases, perceived high costs, perceived side effects and concerns with adolescent sexual activity.

Regarding clinic-level aspects, our findings are generally consistent with existing literature. For example, two recent qualitative studies of health clinics found that strategic prioritization of HPV vaccination or the presence of pro-HPV vaccination culture was an important factor distinguishing clinics with low versus high HPV vaccine uptake [25, 26]. Additionally, the literature has also documented how the ability of clinics to schedule or pre-book future HPV vaccine doses with appropriate time intervals can play a significant role in promoting vaccine uptake [25, 27, 28]. Future programs and interventions can consider targeting organizational priorities and encouraging pro-HPV vaccination culture through implementing benchmarks and incentives to boost vaccine rates and designating immunization champions in clinics [26, 29]. Technology that allows scheduling follow-up HPV vaccination appointments in the future (for both those who have initiated the vaccine as well as those who delay vaccination) should also be incorporated [30].

Moreover, our study participants discussed the utility of using GRITS to track vaccinations. Other research has examined the utility of state and regional immunization registries in helping providers identify HPV vaccine needs and prevent duplicate vaccinations [27, 31]. We note, however, that our participants also mentioned occasional issues encountered with incorrect information in the registry, highlighting the need to address this issue to avoid missed opportunities for vaccinations. Some providers also reported supplementing GRITS data with their own clinics’ medical records systems. Other research has noted similar practices [32], though studies have also pointed out challenges in linking data between medical records and immunization registries [33]. A recent CDC publication provides information on several standards and best practices for the development and maintenance of immunization registries [34], which can help make immunization registries more accurate and efficient to use. To our knowledge, our study is the first that uncovers the benefits and challenges associated with the use of GRITS and immunization record systems for HPV vaccine in the context of Georgia, which can inform future research and practice with immunization registries in the state.

The discussions around the availability of HPV vaccine at healthcare practices and ability to coordinate with community resources represent important opportunities for outreach and communication. Limited literature has focused on this topic. A few studies have looked at how the high costs of vaccine stocking could dissuade clinics from ordering HPV vaccine [27, 35]. Future hospital and community health needs assessments in Georgia should pay attention to barriers to stocking HPV vaccine at clinics as well as collaborations for promoting HPV vaccination. Improved availability could be achieved through coordination between clinics and resources such as county health departments, pharmacies, or the Vaccines For Children program [27, 28]. It may be beneficial to provide additional information on the Vaccines for Children program (e.g. how the program works and how to become a Vaccines for Children provider) to clinics. We note that Georgia has been experiencing a shortage of physicians, with a 2019 report showing that 9 counties had no physicians, 18 had no family medicine physicians and 60 had no pediatricians [36]. The lack of providers, particularly in rural counties, further highlights the need for coordination.

Regarding provider-level findings, some participants expressed a lack of adequate knowledge of HPV vaccine or self-efficacy to discuss HPV vaccine with patients. Providers can find additional training on these matters through several educational programs, such as the CDC’s continuing education courses on immunization and HPV vaccination [37] or the Georgia Chapter of the American Academy of Pediatrics’ EPIC Immunization Program [38]. Interventions can provide additional education and training on patient–provider communication around the HPV vaccine and incorporate tools such as using ‘presumptive announcement’, [39] scripts for providers, decision aids, fact sheets and motivational interviewing with vaccine-hesitant parents [40–42]. We emphasize that the use of ‘presumptive announcement’ has been shown to increase vaccination initiation among adolescents [41]. The CDC also currently recommends clinicians to adopt ‘same day same way’ approach to HPV vaccination (i.e. recommending HPV vaccination to patients in the same way and on the same day that clinicians recommend other vaccines for adolescents) [43].

Research has also identified common HPV myths that providers can address with vaccine-hesitant patients [44]. Other resources, such as the National HPV Vaccination Roundtable’s clinician and support staff guides, can also be consulted [45]. Additionally, the theme of vaccine confidence came up in focus group discussions, with participants observing occasions when other providers declined to recommend HPV vaccine out of uncertainties about its effectiveness. Providers’ lack of HPV vaccine confidence has been noted in other studies as well [26, 27], but little is known on interventions that can target this problem. Future research needs to study ways in which providers’ vaccine confidence can be addressed through training and education.

While time constraints are an issue commonly experienced in clinics [25, 27, 28], HPV vaccine recommendation rates can still be improved if across-practice communication is well coordinated and the entire clinical team is engaged. If the physician does not have enough time to make a recommendation about HPV vaccine to patients, other staff such as nurses, physician’s assistants, or medical assistants could play a key role in recommending and administering the vaccine [26, 28]. However, we also note that a study with clinics belonging to a federally qualified health center found that, compared with physicians and nurse practitioners, medical assistants or licensed vocational nurses were more likely to express skepticism about vaccine efficacy [26]. Such findings highlight again the need to provide training and education for all clinical staff to ensure adequate knowledge, confidence and understanding of HPV vaccine.

Regarding patient-level influences on HPV vaccine uptake, we identified perceived high costs [46–48], perceived side effects [47–50], and concerns with adolescents’ sexual activity [48, 51]. While the aforementioned systematic review on HPV vaccine in Georgia also documented concerns with adolescents’ sexual activity as one of the prominent barriers, it did not identify issues related to costs and perceived side effects [10]. Caregivers with concerns related to costs should be made aware of the Vaccines for Children program, which covers the cost of vaccinations for children without insurance through 18 years of age. Many states’ Children’s Health Insurance Programs also cover the costs of HPV vaccination [52]. To address concerns regarding perceived side effects or safety, patients can be provided with vaccine safety data from clinical trials in addition to research showing no evidence of vaccinated individuals developing commonly-feared conditions (e.g. autoimmune and neurological conditions) [44]; providers also need training to present these data in a manner that patients can easily understand. Again, providers should be trained to answer questions and concerns that patients or caregivers may have, and materials (e.g. fact sheets) can help with addressing these concerns. Researchers also suggest that, in discussions of vaccine safety, it may be useful to talk about non-vaccination as an active decision and introduce the notion that there are also risks associated with not receiving HPV vaccine [53].

Similarly, vaccine-hesitant caregivers should be introduced to a strong body of evidence showing that no association exists between HPV vaccination and increased sexual activity [54, 55]. In our study, it appears that to avoid parents bringing up concerns about sexual activity, providers framed the discussion around HPV vaccine on cancer prevention as opposed to STI prevention. Research also shows that parents are most receptive or persuaded to get HPV vaccine for their children when providers’ message focuses on the benefits of cancer prevention [56]; thus, this approach may be useful in improving parents’ HPV vaccine uptake for adolescents.

We found that experiences with vaccine-preventable diseases influenced providers’ recommendation of HPV vaccine as well as patients’ attitudes toward HPV vaccine. This topic was not identified in the aforementioned systematic review on HPV vaccine in Georgia. In our review of the literature, we found only one study with providers from federally qualified health centers which documented that compared with White middle-class parents, immigrant parents from low-resource settings were more receptive to HPV vaccination, due to their personal experience with vaccine-preventable diseases and cervical cancer [57]. Future studies should pay attention to the role that experiences with vaccine-preventable diseases play in decision-making and recommendation around HPV vaccine. In particular, given that pediatricians are not likely to see many HPV-related cancers, we need to engage the experiences and perspectives of a wide range of healthcare providers in different specialties and provide information on HPV vaccination through different phases of training. In our study, patients’ trust in healthcare providers came up as an important aspect of HPV vaccine decision-making, which has also been documented in previous literature [46] and highlights the need for creating and sustaining strong patient–provider relationships to achieve higher HPV vaccination coverage.

Strengths and limitations

Strengths of our study include having a large sample of healthcare providers with diverse backgrounds and geographical locations in Georgia. We also use theory (i.e. the P3 model) to guide our analysis. Nevertheless, our study is qualitative and the findings are not meant to be generalized across settings and contexts. While the study sought to understand healthcare providers’ perspectives on facilitators of and barriers to HPV vaccine uptake, we did not assess direct relationships between these perceived facilitators and barriers and clinics’ HPV vaccination rates, which could further elucidate the importance of the documented factors. Additionally, in this analysis, we only assessed providers’ perspectives of patient-level barriers and facilitators as opposed to relying on data directly captured from parents and caregivers.

Conclusions

Our study represents one of the first efforts to examine healthcare providers’ perspectives on facilitators of and barriers to HPV vaccine promotion and uptake in Georgia. We provide several suggestions for how interventions can be developed to address issues specific to the context of Georgia. Effective interventions should incorporate elements addressing each of the levels of the P3 model. Interventions may include incentives to boost vaccine rates and incorporate technology for vaccination appointment scheduling. The use of immunization registries should be encouraged. An additional emphasis should be placed on improving across-practice information exchange and providing education for providers on HPV vaccine knowledge and discussion of HPV vaccine with patients. Patient–provider communication and trust emerge as important intervention targets. Providers should be trained in addressing concerns about HPV vaccine, such as those related to costs, side effects, and sexual activity.

Funding

This research was funded by the National Cancer Institute (NCI) P-30 Supplement funding program under Award Number P30CA138292. Research reported in this publication was supported in part by the Intervention Development, Dissemination and Implementation Developing Shared Resource of Winship Cancer Institute of Emory University and NIH/NCI under Award Number P30CA138292. M.V. is supported by the National Cancer Institute (F31 CA243220, PI: Vu). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Conflict of interest statement

None declared.