Health care providers’ perspectives on county-level barriers and facilitators to HPV vaccination: A socio-ecological approach (2022–2023)

ABSTRACT

In Indiana, HPV vaccine series completion is 59.6%. Using a socio-ecological model (SEM) approach, this study investigates county health department providers’ perspectives on improving vaccine initiation and completion among adolescents in Indiana. We conducted semi-structured interviews to explore health department providers’ opinions on barriers and facilitators of HPV vaccine series initiation and completion amongst parents of adolescents. Thematic analysis was then conducted on the transcribed interviews. Interviews were conducted with 24 county health department providers across Indiana with 54.2% (n = 13) holding a Vaccine Coordinator position. Perceived barriers to initiation at the individual level included the parents’ lack of education regarding the HPV vaccine and the importance of prevention. Interpersonally, misinformation and busy schedules for both the parents and adolescents hindered initiation and completion. Further, the presentation of the vaccine by the clinic could affect initiation and completion rates (both positively and negatively). Organizationally, having reminder systems regarding follow-up appointments was a facilitator to completion. Community-level barriers included a lack of providers, transportation, and language issues, but flexible scheduling options were a facilitator. Policy barriers included HPV not being a school-required vaccine. Participants provided valuable insight into perceptions of the HPV vaccine and the barriers and facilitators to HPV vaccine series initiation and completion in Indiana. Barriers to series completion included lack of information and conflicting schedules. Facilitators of series completion included reminder systems and flexible vaccination scheduling options. Interventions that include these facilitators can be developed to improve completion.

Introduction

Human papillomavirus (HPV) infection has been causally linked to multiple forms of cancer, including cervical, anal, vaginal, penile, and oropharyngeal cancers, as well as genital warts and recurrent respiratory papillomatosis (RRP)^1,2 and is spread through skin-to-skin contact.³ HPV DNA has also been found in 98.8% of cervical cancer in situ cases, and 90.6% of invasive cervical cancer cases.⁴ Approximately 37,800 cases of cancer annually within the United States can be attributed to HPV.¹

HPV vaccination is both safe and effective at preventing infection and disease. While there are several different HPV vaccines used globally, Gardasil®9 is the only vaccine that is currently available within the United States.⁵ This vaccine prevents infection from 9 different strains of HPV, responsible for most HPV-caused cancers, genital warts, and RRP. Research suggests that up to 90% of cervical and anal cancers caused by HPV can be prevented by the HPV vaccine, and is more efficacious when administered prior to potential contact with the virus.^1,5,6 Consequently, experts recommend that children begin the series as early as 9 years old. If the series is started before the child’s 15th birthday, there are 2 doses of the vaccine recommended for complete coverage (administered 6–12 months apart); if the series is started at age 15 years or older, 3 doses are required.⁵ The American Academy of Pediatrics (AAP), the American Academy of Family Physicians (AAFP), and the Advisory Committee on Immunization Practices (ACIP) continue to recommend a 2-dose regimen for those under age 15 years.^7,8 Since the vaccine’s introduction in the United States in 2006, there has been an 88% reduction in infections with oncogenic HPV types in adolescent girls and an 81% reduction in young adult women.⁵

Given that HPV largely continues to be a multi-series vaccination, rates are often reported in terms of series initiation (i.e., the individual has received at least one dose of the vaccine) and series completion (i.e., the individual has received all recommended doses of the vaccine). In 2022, when this study was implemented, 76.0% (95% CI: 74.7–77.3) of adolescents between 13–17 years in the United States had initiated the series and 62.6% (95% CI: 61.1–64.0) had completed the series.⁹ This completion rate is well-below the 80% coverage goal identified by Healthy People 2030.¹⁰

Rates vary drastically by state, often due to differences in policies related to the vaccine. A few states and jurisdictions, most notably, Rhode Island and Puerto Rico, require HPV vaccination for entry into school and consequently have higher initiation and completion rates.¹¹ In Indiana, where HPV is not a school required vaccine, 75.5% (95% CI: 68.4–81.4) had initiated the series but only 59.6% (95% CI: 52.2–66.6) had completed the series in 2022.⁹ Insurance coverage is also associated with vaccination rates. In 2022, vaccination initiation ranged from 71.8% to 77.2% amongst insured adolescents but was 58.3% among uninsured adolescents.^11,12

In addition, rates can also vary due to various social determinants of health. These determinants can be embedded in the Social Ecological Model (SEM), which looks at behavior across multiple levels of influence, postulating that the individual and environment have a reciprocal relationship.¹³ The environment is comprised of multiple levels that spans the individual, interpersonal, community, organizational, and policy environments.^14,15 This model emphasizes that individuals develop as a consequence of their varying relationships in each level of the SEM. The SEM has been previously utilized to further vaccine research as it helps researchers understand the complexity of vaccine decision making.^16,17 In our previous quantitative work examining HPV vaccine initiation across counties in Indiana, we found a number of social determinants of health that were correlated with this behavior, including individual issues, like income and insurance status, and community level issues, like access to primary care and rurality.¹⁸

To further this work and illuminate how various SEM factors may affect series completion, this study aims to qualitatively evaluate the barriers and facilitators health care providers at county health departments, many of whom hold vaccine coordinator positions, perceive that parents of adolescents encounter for HPV vaccine series initiation and completion across counties in Indiana. Health care providers at county health departments were sampled due to the wide range of HPV vaccine-eligible populations they serve, their presence in every county, as well as the ease of sampling due to contact information shared by the Indiana Department of Health. Utilizing this framework, we hope to develop solutions to increase HPV vaccine series initiation and completion in Indiana.

Methods

Approvals

This study was reviewed and approved as exempt by the Institutional Review Board at Indiana University. Written informed consent was obtained from participants via e-mail prior to the interview.

Recruitment and procedure

We conducted one-time interviews with 24 health care providers affiliated with county health departments in Indiana. Contact lists were obtained through the Indiana Department of Health, through their Vaccine for Children’s program list. Participants were purposefully recruited from counties with the highest and the lowest HPV series completion rates based on data from Indiana’s immunization registry to better represent perceived barriers and facilitators in the state of Indiana. The interviews were conducted between August 2022 and July 2023 and took place via Zoom (Zoom Communications, Inc., San Jose, CA, USA). Each interview lasted an average of 26 min (range: 16–48). The Zoom audio was recorded, and interviews were professionally transcribed. Vaccine coordinators and related health care professionals were recruited into the study due to their unique positionality in interacting with various members of the health care team, parents, and adolescents.

Interviews were conducted by the female first-author (RAK) who was a Master of Public Health student at the time. She was trained by all members of the research team (MLK, GDZ, KJH) on the research protocol and conducting qualitative research, including a mock-interview with MLK and KJH, prior to interview commencement. The interviewer (first author) followed a semi-structured interview protocol that addressed all five levels of the SEM. The interviewer entered participants’ responses to closed-ended items and took notes on participants’ responses to open-ended items into an electronic form during the interview. The interview protocol was developed based on the expertise of the research team and previous work on this topic.^16–18 Each interview was also audio-recorded and later professionally transcribed. A quality check was done by the first and last authors, who compared the transcript to the audio recording in places when deemed necessary. Interviews began with explaining the purpose and goals of the study. Closed-ended questions included assessing the estimated average number of 11–18‑year-old patients the practice sees each week, the doses of HPV vaccine administered over the past month in the clinic, and more. Open-ended questions inquired about parents’ reasons for not returning for subsequent doses, patient-provider communication, clinic-level attributes that facilitated series completion, and perceptions of policy and practice issues at the county and state level that may facilitate or hinder series completion.

The original aim of this study was to focus on HPV vaccine series completion specifically but given the intertwined nature of series initiation and completion, participants reported barriers to both initiation and completion despite the first author’s efforts to redirect the conversation back to completion. Participants were then given a pseudonym, using “HCP” to label them as a health care provider and a number that corresponded with the order of the participant IDs assigned to them.

Analytic strategy

Data analysis was led by the first and last author and followed the thematic analysis approach and reporting standards outlined by Braun & Clarke.¹⁹ An iterative discussion process to identify salient themes as outlined by this approach was followed here. Both authors read the transcripts line-by-line to familiarize themselves with the data and independently used an inductive coding approach using coding notes and analytic memos. The authors then met to discuss and compare initial findings and develop a final codebook. The authors’ initially intended to stratify results based on counties with higher vs. lower completion rates. However, based on closer review of the thematic analysis, there was significant overlap in themes across both high and low vaccinating counties, thus the results were collapsed to present a singular analysis.

The first author returned to the transcripts and, using Dedoose (SocioCultural Research Consultants, LLC, Los Angeles, CA, USA) software, thoroughly coded every transcript using the established coding categories. The authors met a final time to discuss the coded transcripts and discuss overall themes, including how findings were aligned with the SEM and the clear distinction between barriers and facilitators. A summary of the quantitative answers is provided in Table 1 and described under Participant Characteristics.

Table 1.

Characteristics of the sample.

	Full Sample (n = 24) (n, %)
Age in years (Median, (IQR))	44 (36.5–51.5)
Gender
Male	0 (0.0%)
Female	24 (100.0%)
Race/Ethnicity
White	23 (95.8%)
Black or African American	1 (4.2%)
Role in Practicea
Physician (MD/DO)	1 (4.2%)
Nurse (RN)	7 (29.2%)
Nurse (LPN)	3 (12.5%)
Public Health Nurse (PHN)	9 (37.5%)
Administrator	1 (4.2%)
Vaccine Coordinator	13 (54.2%)
Other	14 (58.3%)
Number of Primary Care Providers
None	5 (20.8%)
1–2	15 (62.5%)
3–5	3 (12.5%)
6–10	1 (4.2%)
More than 10	0 (0.0%)
Geographic Location
Rural	15 (62.5%)
Suburban	5 (20.8%)
Urban	4 (16.7%)
Estimated Average Number of 11–18 years Old Patients (Per Week)b
Less than 25 patients 11–17 years old	12 (50.0%)
25–49 patients 11–17 years old	10 (41.7%)
50 or more patients 11–17 years old	2 (8.3%)
Doses Administered (Past Month)b,d
0–15 HPV vaccine doses	11 (45.8%)
15–19 HPV vaccine doses	3 (12.5%)
20–29 HPV vaccine doses	5 (20.8%)
30 or more HPV vaccine doses	4 (16.7%)
Don’t Know	1 (4.2%)
Insurance Coverage (Majority of Patients)c
Private	10 (41.7%)
Public	2 (8.3%)
Uninsured	4 (16.7%)
VFC Eligible	18 (75.0%)
Reminder Systems
Yes	18 (75.0%)
No	6 (25.0%)

^aThe percentages add up to over 100% because participants could have held multiple positions simultaneously.

^bThis was self-reported and is not a reflection of verified data.

^cParticipants could have reported multiple answers.

^dWe made a minor error in the questionnaire by allowing an overlap between the “0–15” and “15–19” categories; we do not believe it affected the results.

Research suggests that qualitative studies of this nature typically reach saturation of themes in under 25 interviews²⁰; this was consistent with our research where thematic saturation was reached with 24 participants. The first author began to observe thematic saturation during interview 18, whereupon she discussed this with the research team. Then, the decision was made to complete all scheduled interviews but to not recruit any new participants. This observation was validated during the coding of the transcripts, which was done in a random order, where very few new codes were generated during the last few transcripts.

Results

Participant characteristics

A total of 383 health care providers were contacted via e-mail to take part in this study. Health care providers were organized by county; once at least one participant from a county agreed to take part in this study, no other participants from that county were contacted in an attempt to maximize county representation. Of these, 27 participants said they were interested; ultimately, a total of 24 participants aged 18 or older took part in virtual interviews through Zoom. The final sample size was partially constrained by participation interest, however, as the first author was conducting the interviews and beginning to note thematic saturation, the research team made the decision cease recruitment into the study. Participants were represented from counties across Indiana, and were not clustered in one geographic region of Indiana. All of the participants were female (n = 24, 100.0%) and the majority were White (n = 23, 95.8%), and most reported holding a formal Vaccine Coordinator role (n = 13, 54.2%), though it is important to note that many providers interviewed simultaneously held multiple roles. The majority of practices had 1–2 Primary Care Providers (PCPs) (n = 15, 62.5%), were located in rural geographic locations (n = 15, 62.5%), saw less than 25 patients between the ages of 11 and 17 years old per week (n = 12, 50.0%), and saw patients with VFC eligibility (n = 18, 75.0%,). Nearly half administered between 0–15 HPV vaccine doses in the last month (n = 11, 45.8%). Other participant characteristics are described in Table 1.

Overall organization of themes into the SEM

We present the findings based on the five levels of the SEM: individual, interpersonal, organizational, community, and policy. A more thorough representation of the quotes is presented in Table 2. A visual representation of the emerging themes has been described in Figure 1. As aforementioned, while our interview questions were specifically focused on vaccine series completion, many participants spoke generally about HPV vaccine initiation as well, with many healthcare providers failing to distinguish their thoughts between completion and initiation. As these topics are all interrelated to our study purpose, we wanted to honor their perspectives and broadened the scope of this paper and included these findings as well. Across interviews, while the participants in the study certainly had a wide variety of experiences and information, there were no contradicting themes brought up by health care providers.

Table 2.

Additional exemplar quotes.

SEM Level	Key Theme	Quotes
Individual	Importance of Prevention	“So, those are like the parents and/or grandparents of the children that are ready for the HPV vaccines. And, so they’re going through these [colonoscopies] in order to keep themselves safe. I think those people, then, that are completing the screenings have a better understanding of the cancers that affect – you know, the anal cancers and female cancers, they’re going to the doctor and being educated. And I think they are now trying to, you know, take that to their families. They want that protection for their next generation, or the generation after that. And, if it’s a simple thing that we can do, like, a screening thing is simple and easy, you know, a screening.” (HCP08).
	Knowledge Regarding Vaccine	“[…] we have some people who are like, ‘definitely not, don’t want to do it,’ and, you know, we have to go through that conversation of why and just educating them on, you know, cervical cancer rates, and other cancer rates that the vast improvement or the, you know, the drastic drop that we’ve seen in cancer rates with the advent of the HPV vaccine. And just how important it is, and how much it can protect and, you know, the benefit just so outweighs the risk.” (HCP14). “So, maybe they come in the first time and they get the first HPV, not really understanding what the vaccine is. They’re out in the community and someone is bashing HPV vaccine for numerous reasons. Most of those are uneducated talk that is happening, but someone buys into that uneducated talk and they feel like they shouldn’t go ahead with the rest of the series.” (HCP15).
	Lack of Sexual Activity	“I think just lack of knowledge and denial that intercourse and growing adolescents, they don’t want to admit… they correlate that with sexual intercourse, HPV, or an STI. So, automatically it’s like they shudder at the thought that maybe their kid may one day have intercourse.” (HCP20).
Interpersonal Level	Trusted Messengers	“A lot of times parents are very trusting of their physician, so another mode that we often talk about is if physicians, namely pediatricians, would recommend this vaccine in their practice when they’re getting their… whether it’s a sports physical or just their annual checkups, it would be helpful because, you know, who does a parent trust more than anyone? Usually their physician.” (HCP15). “[…] mostly just providing that education and really presenting it in a way where you’re listening to what they’re saying as well and taking their feelings into consideration, and not trying to just hardline facts, ‘here you go,’ but like make it a conversation.” (HCP14)
	Busy Schedules	“I would have to say the timing of that third vaccine causes an issue. Yeah, that would be the biggest obstacle, is the timing of the doses.” (HCP15)
	Transient Populations	“[…] another problem is people change their phone numbers a lot. So, when we’re relying on text messages sent to their phones, we have to have a good working phone number.” (HCP06) “In our community we have a lot of people who relocate a lot. So, whenever we try to do any mailings of any type, it’s not uncommon to get them returned. We have a lot of immigrants right now, and it’s just hard to keep track of them.” (HCP06) “It’s transient in the sense of they move a lot, and they change phone numbers a lot. So, it’s very hard for us to find them, get a hold of them, to send them a reminder that says hey this is due.” (HCP17).
	Social Media, Misinformation, & Distrust	“You know, again, with the misinformation, if they’ve read anything on the internet… yeah, if they’ve read anything on the internet, especially from the anti-vax perspective, or if they start doing research and depending on what sources they’re looking at, they may decide not to come back [for subsequent doses of the vaccine].” (HCP11). “I think that oftentimes, you know, parents have maybe heard something from, like I said, family, friends, possibly some misinformation that’s out there, you know, social media, or just news media, whatever that might be. And, you know, if you’re misinformed and you don’t understand the value of it, you don’t understand the risk vs. benefit of it, and you don’t have anybody telling you any different, then it makes sense to me that you’re going to be hesitant.” (HCP14). “I think that it’s their kind of disinformation that kind of spreads like wildfire, and I think that they’ve gotten, like I said, really good at kind of appealing to your emotions. And, so, I think looking at that aspect, because I think social media and just how fast a meme or a post can spread and can be shared by hundreds of thousands, if not millions, of people … it’s interesting because I think that when people say ‘I did my research,’ unfortunately I think that a huge component of it is, ‘I saw it on the Internet.’” (HCP17).
	Framing	“[…] if practitioners don’t have kind of the same unified message about when to give HPV, how to give HPV, why give HPV, then now you kind of have this extra hesitancy and this extra kind of, I don’t know the word to use […]. Or, how come your doctor said that it was important and mine said it wasn’t? You know what I mean? And, so, like getting everyone in this town to give a unified message, I think that would be helpful” (HCP17). “I do a lot of preaching that it’s cancer-preventing. That’s the route I go in saying that it’s just as beneficial; I mean it’s a little more beneficial for girls, but I say it’s beneficial for boys because, you know, the throat cancer and the anal cancer and everything. That’s the only thing that I can see, to me, that if I can keep my child from getting cancer, I’m going to do everything I can. So that’s the area, kind of the route we go and hit really hard, that it’s a cancer-preventing shot.” (HCP05).
Organizational Level	Reminder Systems	“[…] we get a list of the students who are behind on their vaccinations based on the School Cares, or, I can’t remember what it’s called for the school nurses. But they generate and send us a report of those students who are behind on their vaccinations. And we have a clerk that is our school liaison, and it’s through the school-liaison grant, and she reaches out, whether it be a phone call or a letter or a postcard, to the family.” (HCP15). “Yes, they get a postcard two weeks prior to appointment. They get a phone call the night before or the Friday before reminding them of their appointment, and they get an appointment card when they leave.” (HCP16). “No [we do not have a reminder system], we try to reschedule them back here and make an appointment so we know they have an appointment and they come back.” (HCP05).
Community Level	Clinics	“So, at least on average I guess I would say once per semester as a minimum. But we’re trying to get some other clinics scheduled and do more than that, but that’s our main minimum.” (HCP21). “we’re really trying to, we’re also getting a mobile, like, clinic bus. So, picture an Amazon delivery truck but retro-fitted to be able to give vaccines out of and STDs test out of.” (HCP17).
	Barriers to Access	“one thing might be because we are a rural, I don’t want to say poor county, but maybe those counties with higher rates that are bumping the average have the tools to get reminder recalls out, to host more community events, to do the types of things that we don’t.” (HCP02). “here in our town if someone didn’t have transportation, that might be an issue because we don’t have any public transportation or anything here in our area.” (HCP23)
Public Policy Level	School Based Clinics	“I think we try to overcome that by going into the schools and setting up multiple clinics a year in each school system so that if they do need three doses because they didn’t start it until, you know, after age fifteen, we can get into the schools three times within that school year to get them completed.” (HCP15). “[…] we hired some school nurse liaisons, and they have gone out to the schools, and they’ve gone over shot records, and basically, they’ve actually worked and gotten our rates higher.” (HCP13). “it’s our school clinics, our school clinics outreach program that we get into the schools, we give them access to the vaccinations while they’re in school instead of parents having to bring them in to a provider to get the vaccine. So, I think it’s all about providing that vaccine the easiest way possible to the students.” (HCP15).
	Two vs. Three Vaccines	“When they first made the switch that adolescents under fourteen would get by with two doses instead of three, a lot more parents were picking up on the idea because they don’t like their kid getting three shots and having to make two more return trips.” (HCP16). “I definitely think it is, and I do tell people that. They’re like, ‘Oh, maybe we’ll wait.” I’m like, you know, if you wait, if you wait too long, you’re going to have to get three of them.” And if someone needs convincing, that usually does it.” (HCP24).
	School Requirements	“Or, because it’s not required [by the school], they’re not getting reminders from their school nurses and, you know, it’s one more thing that they have to do, in their mind unnecessarily.” (HCP20). “‘well, no, school said they only need, they need this tetanus, diphtheria…’ so then I have to explain, ‘Yeah, that’s the Tdap, it’s all-in-one, but they also need this HPV.’ ‘Well, why didn’t school tell me?’ So, then I have to get into, it’s not a school-required vaccine. Well, when we’re at that timeframe, they only want school-required vaccines. ‘No, we’ll just do the ones that are required for school today.’” (HCP18).

Figure 1.

Visual representation of the overall organization of themes into the SEM.

Individual level

Importance of prevention

Overall multiple participants acknowledged that if a parent is willing to engage in preventative behaviors for themselves, they are more likely to extend that to their child as well: “[…] it’s the overall general mind-set of prevention is the best treatment, best cure.” (HCP15). Other participants explicitly commented on how engagement with preventative services may not be limited to procedures such as colonoscopies for colorectal cancer screening but also to other forms of prevention, such as vaccines, which is important to initiation. The importance of prevention was not isolated to the parent–child dyad, but the culture of prevention could also be generational.

Knowledge regarding vaccine

Many participants reported that parents often lacked a concrete understanding of what the HPV vaccine was, which contributed to their hesitancy surrounding the vaccine which impacted vaccine initiation. One participant reported that, “[…] we have some people who are like, ‘definitely not, don’t want to do it,’ and, you know, we have to go through […] the drastic drop that we’ve seen in cancer rates with the advent of the HPV vaccine.” (HCP14). Participants reported that just having this educating conversation is often sufficient and parents choose to both initiate and complete the series for their child. However, another participant shared an anecdote elucidating how the community may impact HPV vaccine series completion. Specifically sharing how parents may choose to get the first dose of the vaccine, but are then influenced by external sources to not complete the series.

Lack of sexual activity

Another prominent barrier identified by some providers is denial from parents that their child is likely to one day engage in sexual intercourse. There is a lack of awareness that the HPV vaccine is more effective if administered prior to sexual debut or contact, which has shaped official recommendations. When parents focus primarily on HPV vaccination as prevention of a sexually transmitted infection, and less on the devastating cancers that can be prevented, parents may fear they are encouraging sexual behavior and/or aren’t open to it because their child is not currently having sex: “[…] when you start talking about the HPV vaccine, some parents will immediately stop the conversation and say, ‘we’re not getting that, my child is not sexually active.’” (HCP11). This belief also speaks to vaccine literacy issues, as all prophylactic vaccines should be given prior to exposure to the pathogen.

However, not all sexual contact is consensual and non-consensual sexual intercourse can also lead to the transmission of the virus. This was brought up as a counterpoint by one of the participants when she encountered a parent who didn’t want to complete the series as they thought it was unnecessary due to their child’s lack of current sexual activity: “I was like, ‘so, if they get raped, that’s their fault?’ They didn’t say that much more to me after that.” (HCP16), emphasizing that prevention in all scenarios is key.

Interpersonal level

Trusted messengers

Parents often rely on the advice of their provider in order to make health decisions. Participants reflected that having their physician or nurse advocate for vaccination may help increase rates – of both HPV series initiation and completion. This conversation may be initiated by the parents, “I feel like they’re more comfortable to ask [the nurse], like, ‘what would you do,’ and they trust [the nurse] a little more.” (HCP01) or by their physicians, “[…] who does a parent trust more than anyone? Usually their physician.” (HCP15). Participants also noted the importance of being sensitive to parents’ feelings while simultaneously trying to educate them.

Busy schedules

One of the biggest barriers to HPV vaccine series completion may be the intersection between it being a multi-series vaccine with doses spaced over multiple months and the busy schedules of parents: “I’d say probably 60% have not come back because it’s six months out and they just get sidetracked and forget all about it.” (HCP16).

Transient populations

Similarly, another barrier identified was losing people to follow-up. This can be something as simple as a change in contact information: “[…] another problem is people change their phone numbers a lot.” (HCP06), something bigger such as relocating, or even a combination of both.

Social media/misinformation/distrust

Another major barrier that providers mentioned was misinformation – especially through the internet, social media, and interactions with the community. Through the internet, a variety of perspectives are available regarding the HPV vaccine. Regardless of the scientific reliability of the source, many parents may read the information and choose not to continue the series, “[…] if they’ve read anything on the internet, especially from the anti-vax perspective, or if they start doing research and depending on what sources they’re looking at, they may decide not to come back [for subsequent doses of the vaccine].” (HCP11).

Sometimes receiving information from loved ones such as friends or family makes parents more inclined to trust them and choose not to initiate or complete the series. Another participant commented on how disinformation is able to persuade parents, the domino effect that it has on parents, and most importantly, how quickly the disinformation is able to spread through the internet and social media.

Framing

The way that the vaccine was verbally presented to parents by the health care staff could impact HPV vaccine series initiation. It is important to note that initiation impacts completion. One vaccine coordinator implied if the vaccine is not presented in a consistent manner by different health care workers, they may choose not to begin the series – affecting vaccine initiation.

Further, some providers reported that the HPV vaccine not being a required vaccine for schools in Indiana has led to the belief that it is not an important vaccine. While health care providers are truthful about the distinction between required and recommended, “We don’t certainly lie if they ask us if it’s required. We do get that sometimes, then we educate them on the cancer and why it’s good, you know, and we don’t misconstrue any information and say it’s required.” (HCP20), they also actively try to educate parents on how this vaccine can prevent cancer using reputable sources, such as the American Cancer Society. Some providers reported appealing to the ethos of the parents when describing how this vaccine can prevent cancer, presenting it in a way that is consistent with parents’ motivation to protect their child and that this has improved both initiation and completion.

Organizational level

Reminder systems

Many health care providers reported that having appropriate reminder systems in place have facilitated the completion of the HPV vaccine series, especially because it addresses the difficulty remembering that HPV is a multi-series vaccine spread out over months. Many participants reported their clinics having a multi-faceted reminder system with two or more components included in them. These could include calling, texting, e-mail, and physical mail.

Based on the county and the resources available to them, some vaccine coordinators have gotten more creative with their reminder systems and are able to reach a greater range of people – including individuals who are not current patients in their practice. In certain cases, the reminder systems are integrated within the school system and providers perceive this as an effective way of ensuring children are up-to-date on all vaccines – including the HPV vaccine.

Some counties do not have a reminder system in place and simply schedule their next appointment and hope that parents follow through with the appointment. Later in the interview this participant did comment on how this may be one of the reasons for the low series completion rates in their county.

Community level

Clinics

At the community level, increasing access to the vaccine has been reported to be very important. Often time constraints based on parents’ busy schedules and limited clinic hours means that it is difficult to find time for multiple formal appointments to complete the series. Consequently, participants have found that including the HPV vaccine at community events and clinics has helped with series completion: “[…] we take whatever we’re doing, any back-to-school events, we take HPV vaccine with us.” (HCP11). Some providers also commented on how flexible scheduling options such as extended/weekend hours as well as walk-in appointments are beneficial to both the initiation and completion of the vaccine series.

Barriers to access

Some of the community‑level barriers to series initiation and completion fall under access. One of the barriers to access is a language barrier, and participants reported that having someone on their team to serve as an interpreter has helped with both initiation and completion rates: “She calls most of our Hispanic individuals because she is Spanish-speaking. So, it helps break down that language barrier. And she reaches out to them via phone.” (HCP15).

Another barrier was transportation – especially in rural counties. Consequently, providers reported that having clinics (either community-based or school-based) has helped more children to be up-to-date with their vaccines, “I think going out to the schools, I think that helps a lot because you can catch some kiddos that maybe don’t have transportation to come in.” (HCP24).

Insurance may also play an important role in both series initiation and completion. As one participant stated, “[…] if you look at our county compared to some of the other ones, like I said I think just the access to care, the insurance, I think that plays a big role.” (HCP11). Many families may also struggle with access because they are not aware of programs that provide certain vaccines regardless of insurance status.

Public policy level

School & community based clinics

As aforementioned, clinics could be community- or school-based. The availability of school-based clinics is dependent on multiple factors, including timing, approval from the school board and/or school administration, and whether mobile clinics can come into the community. Some counties have outreach programs, enabling going into schools to offer various vaccinations, and others conduct frequent formal vaccination clinics within the schools, “We do school-based clinics after school has started. We do […] sixteen in the spring, and […], six in the fall […].” (HCP16).

Some counties have reported having access to grants to hire school liaisons to carry out this important work of going into schools to administer vaccines and have reported seeing an increase in HPV vaccine series completion rates, along with an increase in rates for other vaccines. Some of the reasons why these school-based interventions for increasing vaccination rates may be effective is because it increases access and convenience to the vaccine.

Two vs. three vaccines

Participants have also commented on how the need for multiple doses has hindered series completion – with many participants emphasizing that getting the vaccine earlier ensures that their child would only need to take 2 doses rather than 3. This was reported to be an effective “bargaining tool” (HCP02) because it meant less trips for parents and their children, and their children have to take less shots. The effectiveness of this for initiation and completion was especially noted when the directive from the Advisory Committee on Immunization Practices (ACIP) recommended a two-dose schedule for children who initiate the vaccination series prior to age 15 and a three-dose schedule for children initiating the vaccination series following their 15^th birthday.

School requirements

Lastly, participants reported that some parents choose to prioritize school-required vaccines and given that HPV does not fall under that category, they do not make it a priority: “[…] a lot of times parents are like, ‘well, it’s not required for school so I’m not going to make it a priority.’” (HCP11). Participants further described how often the lack of prioritization is because not completing the series does not lead to any immediate negative consequences.

Discussion

HPV vaccination is most efficacious when the series has been completed. Therefore, our objective was to qualitatively analyze interviews with health care providers in Indiana to uncover some important barriers and facilitators that impact the rate of HPV vaccine series completion. While a majority of work regarding HPV vaccination has focused on increasing series initiation, this study initially aimed to focus on series completion to fill an important gap in the literature. The use of semi-structured interviews also provided flexibility to collect as much relevant information as possible, broadening the scope of this investigation to both series initiation and completion. A lack of education regarding the vaccine, misinformation (further perpetuated by social media), and the presentation of the HPV vaccination emerged as reported barriers to series initiation. Prominent barriers to series completion included busy schedules and limited clinic hours, though these could also be barriers to initiation. Facilitators to series initiation included an emphasis on a two-dose schedule particularly for encouraging initiation prior to age 15 years. Reminder systems, flexible scheduling options (such as extended and weekend hours), and community or school-based vaccination clinics were reported to be major facilitators to series completion.

At an individual level, a key facilitator to initiation identified is the individuals’ emphasis on the importance of prevention. Vaccine coordinators reported that parents’ regular engagement in preventive care for themselves (i.e., pap smears, mammograms, or colonoscopies) may make them more willing to engage in preventative services for their child as well. This is consistent with other research that found that maternal preventative care utilization is associated with their willingness to vaccinate their daughters for HPV.^21,22

Misinformation as a barrier to vaccination has been reported in other literature as well. This is a phenomenon that affects all vaccines. Effective vaccination programs in the U.S. have significantly reduced the incidence of many diseases that historically were responsible for widespread suffering and death. As a result of these successes, some parents may underestimate the dangers of vaccine-preventable disease, and focus, instead, on the negligible risks associated with vaccination.²³ In our study, one provider commented on how it made sense to them how misinformation caused the vaccine hesitancy, sharing that if the parent does not understand the value of the vaccine or the risk vs. benefit, it is natural to be wary and choose to avoid starting it or prioritizing completion.

One study also suggested that awareness of safety concerns can occur after series initiation as well and can hinder series completion.²⁴ This was not brought up by the participants in our study, though one participant alluded to parents choosing not to return with their child for subsequent doses due to the experience of negative side effects after the first dose of the series. Increasing the awareness of the safety and side effects of the HPV vaccine for cancer prevention is key to helping increase uptake.

Further, another study reports that conversations with a general practitioner had the greatest impact on a parent’s decision to vaccinate their child.²⁵ A national cross-sectional study reported that the most frequent reason for the lack of parental intention for series completion was the “lack of recommendation from their health care provider”; “safety concerns,” “lack of knowledge” and “not needed or not necessary” were other reasons cited in the top five most common reasons for choosing not to complete the series.²⁶ This was echoed by multiple providers in our study as they pushed for consistent and purposeful messaging from the entire health care team regarding this vaccine. Our study suggested that the way that providers engage in discussions surrounding the HPV vaccine may impact parental perception regarding vaccination. Another study found that parents being told that their child is “due for the vaccine” or that “the vaccine was important” were two of the least effective, or worst reasons to initiate vaccination against HPV; being told that it can “prevent some types of cancer” and that it has “lasting benefits” ranked as some of the best reasons.²⁷ This finding was consistent across parents with both high and low levels of vaccine confidence. Consequently, consistent specific messaging would be beneficial to both series initiation and completion rather than utilizing generic language.^28,29 Interestingly in our study, many providers placed heavy emphasis on children being due for the vaccine, often sandwiching it between other vaccines, thereby emphasizing that, like tetanus, diphtheria, and pertussis (Tdap) and meningococcal ACWY (MenACWY), which are required for middle-school entry in Indiana, HPV vaccine is also a routine part of the vaccination schedule. The way that providers frame vaccines can impact whether parents believe the vaccine is necessary for their child – especially since some parents remain unaware of the importance of the vaccine in preventing cancers in males.³⁰ As a result, health care providers are a key demographic that need to be mobilized to help fight against vaccine hesitancy and misinformation.

One of themes that arose through this analysis is the unique positionality of reminder systems to serve as both barriers and facilitators to HPV vaccine series completion. Across individual provider accounts, providers who described robust reminder systems often credited those systems for their higher series completion rates. For counties with reminder systems in place, most reported utilizing phone calls, text messaging, e-mails, physical mail, or a combination of those. One county reported going as far as to do billboards and advertisement campaigns. The importance of reminder systems has been previously reported in the literature with one study reporting that 89% of parents that initiated but did not complete the series, did intend to complete the series but did not because they were either not reminded by clinics or they experienced other logistical barriers.³¹ In our study, some counties lamented that while they understood the importance of reminder systems, there was a lack of resources to develop a comprehensive system. In lieu of a reminder system they try to reschedule parents so there is an appointment on their calendars, encouraging them to come back.

Additionally, having expanded clinic hours and utilizing school-based clinics was instrumental to facilitating series completion. Parents in our study and others have reported that competing priorities and the busy schedules of both the adolescent and the parent make series completion difficult.³¹ Some coordinators reported that school liaisons or school-based clinics have helped with series completion. These results are echoed in a randomized clinical trial where schools that had a school-based vaccine clinic (3 times a year to align with the HPV vaccine schedule) saw large increases in multiple adolescent vaccines and the largest increase in the HPV vaccine.³² The results of this study and the anecdotal evidence presented in the current study suggests that the development of school-based clinics is a feasible way to improve vaccination rates. Another study that focused on increasing education regarding the HPV vaccine found that the majority of parents (97%) and school staff members (85%) were in support of school-based clinics.³³

Lastly, we would be remiss if we didn’t comment on the impact that the COVID-19 pandemic had on HPV vaccine series completion. Importantly, all interviews for this present study were conducted after the primary period of the pandemic. While we chose not to directly report COVID-19 related barriers and facilitators to the HPV vaccine in our results, many commented on how the pandemic influenced all vaccines – not just the HPV vaccine – and outlined how COVID-19 has added a layer of mistrust between the public and federal and state health agencies. Further that while all vaccine rates have been negatively impacted, given that HPV is an optional vaccine, it has been particularly affected.

The results of our study have several important implications. First, health care teams play an integral role in HPV vaccination series completion through the dissemination of accurate information and actively combating vaccine misinformation through purposeful and consistent messaging. Second, taking steps to address various barriers to access (language, transportation, and limited clinic hours) can help to expand the reach of the HPV vaccination and help parents initiate and complete the series for their child. Lastly, utilizing funding to create comprehensive reminder systems can help to increase completion rates.

The present study had several limitations and results should be interpreted with caution. The sample that made up our study was limited to those that replied to the e-mails sent by the first author. However, counties without a centralized e-mail address or lack of staff to monitor e-mails and/or participate in this may not have been represented in this study. Further, with the majority of our participants being female and White, it is possible that themes prominent to minority populations and other demographic groups may not have been identified. For example, culturally specific barriers that may impact HPV vaccination series initiation and/or completion could not be identified. Further, barriers and facilitators that may be tied to race and structural racism are likely to be underrepresented or mischaracterized. Characteristic of the study design, there is the chance for recall bias through the interviews. Our study was purposefully limited to counties with the highest and lowest HPV series completion rates in the state of Indiana. Expanding this to the whole state of Indiana, other US regions, or to other global healthcare systems can allow for the identification of other barriers and facilitators to HPV vaccine series completion that can inform the development of expanded interventions.

Conclusion

As with all qualitative research, the results reported should be interpreted with caution and may not be generalizable to HPV vaccination experiences in other states and counties. Regardless, the results of this study may be a helpful starting point for decision-making in similar settings. This study examined the perspectives of health care providers affiliated with county health departments in the state of Indiana regarding HPV vaccine series initiation and completion amongst adolescents. Using the SEM as a guiding framework, this study contributes to our understanding of the major barriers and facilitators to HPV vaccination series initiation and completion at each level that included: the importance of prevention, school-based clinics, provider recommendations, and reminder systems. Future work should build off these identified barriers to increase knowledge regarding the importance of the vaccine for boys and girls alike, invest in comprehensive reminder systems, and develop policies to address underlying demographic disparities that lead to lower HPV series completion rates.

Biographies

Rida A. Khatri was a Master of Public Health student during the completion of this project. She is currently attending the University of Wisconsin Madison as a PhD student in Epidemiology. Her research interests include social and lifestyle determinants of screening preventable cancers, cancer risk, and cancer mortality – especially in minoritized populations.

Gregory D. Zimet is clinical psychologist, consultant, and Professor Emeritus of Pediatrics and Psychiatry at Indiana University School of Medicine. His research focuses on psychosocial/behavioral issues associated with acceptance of biomedical approaches to the diagnosis and prevention of infections and disease.

Monica L. Kasting is an Associate Professor in the Department of Public Health at Purdue University. She has a PhD in epidemiology and completed a postdoctoral fellowship at the Moffitt Cancer Center. The overarching theme of Dr. Kasting’s interdisciplinary research program centers on improving preventive health behaviors and care delivery. She seeks to understand health behaviors as they relate to cancer prevention and address barriers to engaging in those healthy behaviors.

Katharine J. Head is an Associate Professor in the Department of Communication Studies at Indiana University. Her research focuses on health communication, and much of her scholarship has focused on how individuals communicate about vaccines and cancer screenings in the public and clinical contexts.

Funding Statement

This research was supported by the Investigator Studies Program of Merck Sharp & Dohme Corp [MISP #60560] administered through Indiana University.

Disclosure statement

RAK has no relevant financial or non-financial interests to disclose. GDZ has served as an external advisory board member for Pfizer, Moderna, and Sanofi, and as a consultant to Merck and Pfizer; has received investigator-initiated research funding from Merck administered through Indiana University; and serves as an unpaid member of the Board of Directors for the Unity Consortium, a nonprofit organization that supports adolescent and young adult health through vaccination. MLK has served as a consultant to Merck and has received investigator-initiated research funding from Merck, administered through Purdue University. KJH has received investigator-initiated research funding from Merck administered through Indiana University and serves as an unpaid board member for the Indiana Immunization Coalition.

Data availability statement

We are happy to provide study materials, including the interview guide, if interested researchers contact the first author.