Introduction

Nearly a decade after the introduction of the human papillomavirus (HPV) vaccine, prevalence of genital HPV among US adults ages 18–59 is still 45.2% in men and 39.9% in women [1]. The American Cancer Society expects 12,820 new diagnosed cases of invasive cervical cancer in 2017; virtually all of these cancers will be caused by HPV infection [2]. Although HPV is most commonly associated with cervical cancer, the CDC estimates that 31,500 cases of HPV-related cancers occur annually, including cancers of the cervix, vagina, vulva, penis, anus, rectum, and oropharynx [3]. The HPV vaccine is highly effective in preventing HPV infection, but tepid uptake has prevented maximal benefit in the US.

HPV vaccination rates in the US have steadily improved since Food and Drug Administration (FDA) approval in 2006 but remain substantially below target. In 2016, only about 60% of adolescents ages 13–17 had received one dose of the HPV vaccine, and only 43% had received all required doses [4]. Comparatively, 88% of adolescents had received the recommended tetanus, diphtheria, and pertussis (Tdap) vaccine [4]. This disparity in coverage was even more striking between males and females; at every age between 13 and 17, females were more likely to have received the HPV vaccine than their male peers, and only 38% of 13-17-year-old males received all required doses compared to 50% of females [4].

HPV vaccine messaging has negatively impacted its initial uptake in the US. Based on a systematic review, communication barriers have included general lack of HPV vaccination information/awareness and initial framing of the HPV vaccine as a vaccine against an STD (HPV) that is recommended for females [5]. Early marketing focused on the prevention of HPV as a sexually transmitted infection, raising concerns about sexual promiscuity [6, 7]. Furthermore, the HPV vaccine was first FDA-approved in the US exclusively for girls with a focus on cervical cancer prevention, which may have contributed to the gender disparity in vaccination rates [4]. Cervical cancer only accounts for about one third of all HPV-related cancers, and about 40% of all HPV-related cancers occur in males [8]. In 2016, the CDC recommended a 2-dose schedule (rather than the previous 3-dose schedule) for adolescents who initiate the vaccination series at ages 9–14 years, which may result in higher completion rates among adolescents.

Effective HPV vaccine messaging remains an important strategy to increase vaccine uptake, especially in South Carolina (SC) where HPV vaccination rates are below the national average [4]. Since 2006, the CDC has improved messaging on a national level, emphasizing the ubiquity of HPV, the HPV vaccine as a cancer-prevention measure, and the importance of the vaccine for all adolescents [9]. However, low vaccination rates in SC suggest that healthcare professionals and advocates need to operationalize these messages and maximize their effectiveness within the state.

In 2014, the National Cancer Institute selected 18 sites, including the MUSC Hollings Cancer Center, to carry out environmental scans to evaluate barriers, facilitators, and potential strategies for improving state-level HPV vaccination rates [10]. Our environmental scan consisted of interviews with state leaders, regional community focus groups, and focus groups with primary care practices. The current report describes communication strategies recommended for improving HPV vaccination rates in SC that emerged from interviews with state leaders.

Methods

Design

This analysis reports on recommended messengers, messages, and messaging strategies for increasing HPV vaccination in SC. Thirty-four key informant interviews were conducted with state leaders from organizations whose roles had potential to address HPV vaccination policies and practices. This analysis was designed to gather feedback from the perspective of state leaders, a stakeholder group that may have considerable insight into best practices for public health messaging that may be relevant to HPV vaccination, but for whom little has been published. On average, interviews lasted for 40 min (range 30–60 min). After each interview, participants completed a self-administered demographic survey. Participants were not compensated. The MUSC IRB reviewed the study protocol and deemed the primary purpose to be program evaluation, obviating need for IRB approval.

Participants and Setting

Stakeholders were recruited via purposive sampling to identify leaders from organizations with potential to address statewide HPV vaccination policies and practices. Participants were recruited via three email invitations, followed by two phone calls to non-respondents. Contact attempts were spaced about 2 weeks apart. The state leaders who participated in interviews represented organizations that included large insurers, healthcare provider organizations, public health, state quality improvement collaboratives, K-12 schools, universities, non-profits and grassroot organizations that target cancer prevention and adolescent health, and state legislators. Among organizations invited to participate in interviews, all completed the interviews except for two legislators who were known as HPV vaccination opponents and one state university that did not reply to our invitation requests. Most interviews were conducted in person, but three were done by phone based upon stakeholder preference.

Data Collection, Management, and Analysis

The primary data source was the key informant interviews. The semi-structured interview guide was developed by investigators with expertise in qualitative research, program evaluation, HPV, and cancer control and was pilot tested with two cancer control professionals prior to use, which helped to streamline and ensure neutral presentation of questions. The interview guide assessed best practices for improving HPV vaccination in SC. Generic questions included (a) stakeholder perceptions about HPV vaccination; (b) barriers, facilitators, and best practices for improving HPV vaccination; and (c) key partnerships and discussions needed for optimizing HPV vaccination rates. Each of the questions was carefully written to be neutral to minimize potential response bias. For example, to inquire about stakeholders’ perceptions about HPV vaccination, we asked “What are your thoughts about HPV vaccination in South Carolina.” Similarly, to ask about barriers to HPV vaccination, we asked “What are the barriers to HPV vaccination in our state?” with subsequent questions to follow up on each barrier listed by the participant. This same type of question framing was used for each of the questions on the interview guide.

Each interview was audiotaped and transcribed. Transcripts were reviewed by a second person for accuracy. A thematic content analysis approach was utilized [11]. Two investigators independently reviewed a sample of interview transcripts to develop a codebook for structuring formal data analysis. Transcripts were coded, with emerging codes added to the codebook as needed. Preliminary results were shared with the research team for review and discussion. This iterative process was used to maximize valid interpretations of the interview data.

Results

Among the 34 key informants who participated in interviews, 73.5% were female, 82.4% were white, and 85.3% had a graduate degree or above; 38% were under the age of 45, 53.0% were 45–64, and 8.8% were 65 or older. Among these individuals who represented their state-level organizations, 14.7% represented the public health department, 14.7% physician associations, 2.9% pharmacy organizations, 8.8% insurers, 8.8% QI collaboratives, 2.9% department of education, 2.9% school nurses association, 11.8% university school health programs, 8.8% state legislators, 17.6% grassroots cancer prevention organizations, and 5.9% adolescent health organizations. Of note, we interviewed all individuals in the state who we were aware of that had led state-level HPV vaccination efforts (n = 5), such as grassroots community engagement, pediatric quality improvement initiatives, and legislative efforts to make the HPV vaccine mandatory for middle school and/or to require education about the vaccine in middle schools. Themes emerged from the interviews centered on the identification of optimal HPV vaccination messengers, messages, and messaging strategies.

HPV Vaccine Messengers

As presented in Table 1, identifying appropriate messengers emerged as a central concern among most participants who agreed that information about HPV vaccination needs to come from the right source to be the most effective. One participant stated, “It’s your messenger as much as your message,” and this sentiment was echoed throughout the interviews. Participants recommended utilizing messengers in three categories: national and state health organizations, community-based organizations, and peers.

Table 1 HPV vaccine messengers
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National and State Health Organizations

Participants identified individuals representing state and national health agencies who could serve as messengers, such as American Academy of Pediatrics, CDC, Cervical Cancer-Free SC, SC Department of Health and Environmental Control, MUSC Hollings Cancer Center, SC Academy of Family Physicians, SC Medical Association, and health insurers. Multiple participants stressed the value of public endorsements or “stamps of approval” from leaders representing these entities to lend a sense of expertise and authority to HPV vaccine messaging. Participants also identified familiarity and respect as important factors in the credibility of spokespersons and recommended local health professionals, such as primary care providers and school nurses as messengers who may be most effective in communicating HPV information and increasing vaccine uptake.

Community-Based Organizations

Other trusted community-based authorities may also serve as messengers, and many participants suggested partnering with local Parent Teacher Associations and faith-based and community organizations. Leaders in these organizations offer a valuable platform for disseminating information and may be seen as more trustworthy than sources from outside the community; “If that message is coming from someone seen as a physician or an outsider then it is often times not that well received.” To further bridge the gap between a trusted local authority and an outside medical authority, one participant suggested utilizing healthcare-related student organizations or medical students from a local university to emphasize education and show support, stating: “That educational component needs to be involved and so do the younger people, maybe even medical students. They came to our hearings for Smoke-free Charleston in their white coats and it was a really great appearance.”

Peers

Several participants identified peers as important messengers who, along with community and medical authorities, may encourage vaccine uptake. Adolescents who hear about the HPV vaccine from friends may be more likely to advocate for the vaccine for themselves, and parents may be similarly likely to take advice from other parents. One participant reported, “Parents put some stock in their doctor generally speaking, but parent to parent communication has been critical for us.” Peer-to-peer interaction was also identified as a means of promoting the HPV vaccine among healthcare providers. One participant suggested utilizing messengers within the same profession to promote the vaccine among peers, because “nurses don’t want to hear from doctors about how to do their job.”

HPV Vaccine Messages

As described in Table 2, participants identified six HPV vaccination messages and communication strategies that may be instrumental in increasing uptake: focusing on cancer prevention instead of sexual transmission, highlighting the high risk for acquiring HPV, comparing HPV-related cancers to other cancers, appealing to parents’ moral obligation to protect their children, emphasizing the need for both boys and girls to be vaccinated, integrating the HPV vaccine into the routine schedule of adolescent vaccination, and tailoring messages to ethnic and cultural groups.

Table 2 HPV vaccine messages
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Focus on Cancer Instead of Sexual Transmission

Concern among the general population about sex and sexual activity is a significant barrier in receiving the HPV vaccine. Perhaps the most popular topic related to HPV vaccine messages was the need to distance HPV from sexual activity and focus on cancer prevention: “As a global comment in South Carolina, the HPV vaccine is tied to sex. It is not tied to cancer prevention. That’s a messaging problem.” Multiple participants reiterated this sentiment and suggested that sexual activity and transmission have played too large a role in prior messaging efforts, distracting the public from the purpose of vaccination and discouraging parents from participating. One participant asserted, “we need to focus on the cancer angle and not on sexual activity. CDC put too much focus on sexual transmission.”

To avoid predominant cultural perceptions about the vaccine and sexual activity, several participants offered specific recommendations to approach the issue. One participant suggested opening a conversation with wary parents by first acknowledging their child is not sexually active, “because of the outstanding parents they are, we know that they would want their children to be protected in case they do become sexually active.” Another, more tongue-in-cheek response suggested extraordinary denial about adolescents and sex: “If we change the message to preventing cancer, this would resonate more than focusing on the sexual part. We are in the Bible Belt. There is no sex going on.” Another participant recommended circumnavigating sexual transmission by focusing on less explicit forms of transmission, such as kissing. “It would be more palatable for a parent to think they need to protect their child from a kissing exposure.” In every case, participants who recommended decreasing focus on sexual transmission also recommended simultaneously increasing awareness of the causal link between HPV and cancer, “it needs to get out there this is not a sex vaccine; it is a cancer vaccine.”

Compare Cervical Cancer to Other Cancers

To educate the public about the risks of HPV, multiple participants recommended comparing cervical cancer to other more widely known forms of cancer. Breast cancer was the most popular comparison, and one participant stated, “Cervical pre-cancer is a very common problem that occurs more often than breast cancer. Just most of the time we catch it. But do you really want your daughter to be the one that we catch with cancer? And lastly, cervical cancer is devastating and life threatening and still happens.” Another participant drew attention to the unique nature of the HPV vaccine, pointing out that other cancers are not associated with an identifiable, preventable virus: “If you had the opportunity to vaccinate your child against breast cancer you would take it in a minute (…) this is the only vaccine that is available for preventing cancer.”

Appeal to Moral Responsibility

In addition to minimizing the association between sex and HPV, another common theme was an appeal to parents’ sense of duty and moral responsibility for the well-being of their children. A majority of participants posed some version of a rhetorical question asking why anyone would neglect their child’s health and presented HPV vaccination as a moral imperative. One participant said, “Same as with other diseases, the chance is very low to get cervical cancer, but do you want your child to be the one that gets cervical cancer?” Another simply asked, “Why would you not protect your child?”

Emphasize Vaccine Uptake Among Males

Another messaging issue specific to this vaccine concerns gender; multiple participants recommended explicitly addressing males and their risks for HPV-related cancers. Two participants pointed to pervasive misperceptions about HPV being a problem that only affects females and mentioned personal examples of peers who were unaware of when or why boys should be vaccinated. One participant commented, “Some of the allies we work with to promote HPV vaccination had no idea that boys could get it and that it could cause cancers in boys. This message needs to be shared.”

Routinize HPV Vaccines

Some participants suggested it would be beneficial to normalize the HPV vaccine as one of the many standard childhood vaccines, not as an extra or optional vaccine. One participant explained that treating HPV just like MMR and DTAP, “gives it more strength and credibility,” elevating the seriousness of HPV and encouraging more people to receive the vaccine. Including the HPV vaccine in the battery of normal adolescent vaccines may also motivate parents to comply with vaccination recommendations. One participant cited experiences with providers who choose not to treat children who do not have all the recommended vaccines: “That typically ends the conversation, and many choose to get vaccinated.”

Indirect Cost-Savings of Preventing Cancer

Some participants pointed out that, as a preventive measure, the HPV vaccine can reduce overall healthcare costs by reducing the need for cancer diagnostics and treatment. This may be an important point to discuss with “key stakeholder leaders” who may be interested in the benefits of the vaccine from a financial perspective.

Targeted Messaging

Though a less common topic, some participants provided recommendations for targeted messaging. Some participants identified increased need for sensitivity and consideration regarding messaging to specific populations, such as ethnic/cultural groups and religious communities. According to one participant, an effective strategy included identifying the most effective messengers within different cultural groups, such as elders/authority figures in the Native American community or men in the Hispanic community. Recommendations regarding religious communities included framing the vaccine as a gift from God, as well as distancing HPV messaging from sexual activity. Conversely, one participant suggested that messages directed to the African American community may not need to be as cautious regarding sexual transmission of HPV, stating, “because HIV has hit the African American community so hard, that stigma has kind of gone away.” Two participants also identified the need to evaluate educational materials for use with bilingual and low-literacy populations, emphasizing readability at a third-grade level.

HPV Messaging Strategies

As presented in Table 3, participants identified several general messaging strategies to increase HPV vaccine uptake. Most frequently, participants recommended communicating messages across multiple media (e.g., traditional and new media), consulting with public health and marketing experts, and utilizing personal stories and scientific data to increase credibility and present consistent messages.

Table 3 HPV vaccine messaging strategies
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Communicate Across Multiple Media

Participants suggested using social and entertainment media such as YouTube and Facebook to relay messages. Another participant recommended entertainment events, such as live performances, fairs, and farmers’ markets to promote HPV education, saying “Out of our university’s sexual health office, we often do unrelated social events first to break the stigma instead of just pushing the vaccine. Students may come to the event because they want to see a competitive dance show but there is also educational information to raise awareness. It draws in people who may not otherwise come to the event.” Similarly, another participant pointed to a study that showed an increase in subjects’ knowledge about HPV after encountering educational materials in fraternity/sorority meetings and primary care clinics.

Consult with Experts

To maximize the impact of messages across multiple media platforms, many participants suggested collaborating with experts, such as marketing and social media professionals. Public health experts were also identified as resources to help craft the most effective messages, which should be clear and concise. One participant recommended, “identify the very best message and stick with it across time and communities.”

Share Personal Stories

Several participants stressed the value of personal stories in communicating HPV risks and making messages more personally relatable. Since first-hand experiences may resonate on a more personal level, stories from cancer survivors, parents who have already vaccinated their children and peers who have received the vaccine were identified as potential vignettes to include in vaccine messages. One participant, referencing the case of a mother of two who was recently diagnosed with cervical cancer, stated, “I think it would be great for someone like her to say ‘I had cervical cancer, and I would have loved to have known about the vaccine.’” Another participant stated that this strategy would provide “a powerful perspective to see how people who have already gone through cancer feel about getting a vaccine that can prevent another cancer.” Another participant referenced an example of how personal stories from public figures can raise awareness and influence legislators. “That’s an unfortunate truth about how the politics work. Only when a conservative legislator who had colorectal cancer made connections with the legislature and got into advocating for colorectal cancer prevention and screening very forcefully, then we had colorectal cancer funding again in South Carolina.”

Present Scientific Data

To further boost credibility, several participants suggested that messages should incorporate reliable scientific data. Several participants advocated disseminating sound research data to decrease skepticism about the HPV vaccine’s efficacy, safety, and necessity: “There is the statistical data about how many people have been vaccinated; how safe it is; how it has been even more effective than we thought it would be. That’s a story that is not getting enough press. The fact that 60% of girls have gotten the vaccine is remarkable. Anytime you can tell a positive story, it needs to be told.” Another participant suggested that outcome data from Australia, where the HPV vaccine has been in use longer than in the US, could be “an important tool for educating providers.” Participants advocated for use of scientifically accurate data not only to promote the HPV vaccine, but also to combat misconceptions and “ensure we are debunking the myths that are perpetuated.” Some of the myths participants identified that should be addressed included the (disproven) belief that vaccines may cause autism, or that the HPV vaccine encourages promiscuity. Data may reassure concerned parents, and one participant offered “The HPV vaccine shows no evidence that it increases sexual activity or contraction of other STDs.”

Discussion

Although HPV vaccination communication remains widespread, ineffective messages are a barrier to vaccine uptake [5]. Interview participants recommended a strategic comprehensive approach to HPV vaccine messaging. Many suggestions aligned with recent CDC health communication recommendations, which include working with partners such as Cervical Cancer-Free America and presenting the HPV vaccine to parents as cancer prevention [12]. The most recommended trusted messengers included healthcare organizations and providers, patient and parent peers, and local public figures. Findings elaborated extant research showing the success of peer-to-peer messaging [13] and the synergistic effectiveness of combining expert and peer narratives [14].

Participants recommended crafting messages that appeal to parents’ moral responsibility to protect children against cancer. This finding resonates with a recent study which reported moral values, such as purity and liberty were associated with vaccine hesitancy [15]. Messages that emphasize HPV vaccination as a parental responsibility and personal choice may influence vaccine-hesitant parents. Participants also identified HPV’s link to sexual activity as a significant problem with previous messages, particularly in SC which has a large Christian population. Innovative messages may address the ubiquity of HPV and share growing evidence that HPV may be transmitted independent of sexual activity via skin to skin contact [16]. Participants also recommended disseminating CDC messages that emphasize cancer prevention and the risks of HPV. Messages that improve knowledge about transmission and prevention of HPV may improve vaccine uptake [17,18,19]. Other HPV-specific messages included promoting male vaccination and routinizing the HPV vaccine series. Many of these suggestions align with constructs from behavioral models such as the Health Belief Model and Social Cognitive Theory [20], such as conveying high risk for HPV infection, severity of illness (cancer) associated with HPV disease, cue to action that it is parents’ responsibility to protect children from known risks, and normalizing HPV vaccination as standard practice.

Recommended messaging strategies for increasing vaccine uptake included utilizing personal stories from cancer survivors and parents who have vaccinated their children. Audience-generated messages offer an effective strategy in health communication campaigns [21]. Participants also suggested employing narratives to emphasize how common cervical pre-cancer remains among women. According to the CDC, over 300,000 US women experience invasive testing and treatment for cervical pre-cancer that can result in mental and physical harms, such as cervical instability leading to preterm birth. Participants also recommended a culturally tailored messaging approach. This finding builds on extant research highlighting the role of racial disparities and sociocultural values on HPV vaccination decision-making [22, 23]. Stakeholders also described the need to utilize credible experts to deliver scientific data to emphasize safety and efficacy and communicate across multiple media platforms to engage a wider audience. Participants also recommended seeking advice from media experts regarding the most effective strategies. These recommendations for messaging strategies provide a blueprint for developing a media campaign supported by Communication Theory [20], which describes the need to develop media campaigns that rely upon optimal messengers and message platforms, with message targeting at the group level and tailoring at the individual level as needed to reach intended audiences with appropriate messages.

To date, there is limited evidence to evaluate the effect of HPV vaccination awareness campaigns on HPV vaccination rates. Findings from a recent national environmental scan suggest that many awareness campaigns have been conducted, but rigorous evaluation of these campaigns is limited [24]. Evaluations most commonly reported HPV vaccination process measures (e.g., web/phone traffic, provider use of educational materials, HPV vaccine awareness), and among two studies that evaluated actual HPV vaccination rates, results were mixed [24]. A recent HPV vaccination campaign conducted in Ireland provides insight into how one country implemented rapid and effective communication strategies for improving HPV vaccination rates [25]. An evaluation was first conducted to assess the underlying reasons for low vaccination rates, which was followed by a national HPV vaccination campaign. An HPV vaccination alliance was formed with 35+ organizational partners working in health, women’s rights, child welfare, and the public, followed by a media campaign widely supported by members of the alliance and senior politicians. As part of a multi-level approach, HPV vaccine print and online materials were revised and short videos were created, which were housed on a WHO-accredited website, a comprehensive provider training program was implemented, and unvaccinated girls were offered another opportunity for vaccination. Over the campaign period, first dose HPV vaccination rates for girls increased from 50% in 2016–17 to 62% in 2017–18 [25]. These findings suggest thoughtful baseline evaluation, coupled with subsequent coordinated multi-level strategies to address identified vaccination barriers may rapidly yield robust improvements in HPV vaccination uptake.

Our interviews relied on expert opinions from professionals from numerous organizations in SC, but it is possible that informants were not entirely impartial representing their respective organizations. This evaluation may have also benefitted from interviews with HPV vaccination opponents who could offer a more complete picture of barriers to vaccine uptake. Unfortunately, SC legislators who had opposed state vaccine legislation declined to participate in interviews.

This study provides robust insight from SC leaders whose roles afford them opportunity to influence HPV vaccination policy and practice in a state where HPV vaccination rates are among the lowest in the country. While the study was conducted in SC, a state where HPV vaccination rates have been historically low, the results were strikingly similar to what has been reported nationally, suggesting these results may be generalizable to other states in the US. To increase HPV vaccine uptake, health professionals and advocates will need to disseminate effective messages both at the state and grassroots community level. This scan identified three elements of effective messages: 1) appropriate messengers, 2) factual messages about HPV and the vaccine with a focus on overcoming misunderstanding about the vaccine’s purpose and target groups, and 3) strategic communication to ensure effectiveness and reach of messages to the intended audience.