The most effective and promising population health strategies to advance human papillomavirus vaccination

Abstract

The US is failing to make substantive progress toward improving rates of human papillomavirus vaccine uptake. While the Healthy People 2020 goal for human papillomavirus (HPV) vaccination is 80%, the three-dose completion rate in the US in 2014 for 13- to 17-year-old females is less than 40%, and the rate for males is just above 20%. Experts point to a number of reasons for the poor HPV vaccination rates including parental concerns about safety, necessity, and timing. However, the evidence refuting these concerns is substantial. Efforts focusing on education and communication have not shown promise, but several population health strategies have reminder/recall systems; practice-focused strategies targeting staff, clinicians, and parents; assessment and feedback activities; and school-based HPV vaccination programs.

The US is failing to make substantive progress toward improving rates of human papillomavirus (HPV) vaccine uptake. The Healthy People 2020 goal for HPV vaccination for both males and females is 80%,[1] but the completion rate for the three-dose series in the US in 2014 for 13- to 17-year-old females is only 39.7% and the rate for males is 21.6%.[2] To address this problem, both healthcare organizations and public health services need to adopt evidence-based population health interventions to achieve high levels of vaccination.

The Food and Drug Administration licensed the first HPV vaccine in the US in 2006, and the Advisory Committee on Immunization Practices (ACIP) published its first recommendations in 2007.[3] Figure 1 illustrates the HPV-vaccine timeline in terms of major licensures and recommendations. The ACIP recommended the HPV vaccine in 2007 for females only.[3] Three years later, ACIP permitted one of the then two US-licensed HPV vaccines for use in males [4] and then published a full recommendation for routine use in males on December 23, 2011.[5]

Figure 1.

Key events in human papillomavirus (HPV) vaccination. Advisory Committee on Immunization Practices (ACIP)

Figure 2 illustrates the HPV vaccination trends over time with the flat trend line for females since 2010. Males started much later, and at a much lower point, and have made steady progress each year since 2011.[2] Figure 2 also illustrates how the uptake of HPV has lagged behind other adolescent vaccinations including the tetanus toxoid, reduced diphtheria toxoid and acellular pertussis vaccine, adsorbed (Tdap), and the quadrivalent meningococcal conjugate (MenACWY) vaccines, recommended for routine use only one to two years before the HPV vaccine for females.[2]

Figure 2.

Human papillomavirus (HPV), tetanus toxoid, reduced diphtheria toxoid and acellular pertussis vaccine, adsorbed (Tdap), and quadrivalent meningococcal conjugate (MenACWY) vaccination uptake over time for 13–17 year olds in the US (%). Data from the National Immunization Survey – Teen, CDC.

Of note, as of 2014, among both US females and males 13–17 years of age, disparities exist in HPV vaccination by race, ethnicity, and socioeconomic status.[2] Among females, Hispanics, non-Hispanic blacks, and non-Hispanic American Indian/Alaska Natives all have higher rates of initiation of the HPV vaccine series than whites, as do females below the federal poverty level compared to females above the poverty level. Among males, Hispanics and non-Hispanic blacks have the highest rates of initiation of the HPV vaccine series, as do those males below the federal poverty level. However, while HPV vaccine initiation rates are higher in these populations, completion rates are lower.[2] Language barriers, lack of health insurance, and lower provider rates of recommendation have been identified as key reasons for lower completion rates.[6]

The basis for the failure of HPV vaccine uptake

A lack of clinical care encounters

Experts point to a number of reasons for the poor HPV vaccination rates.[7] One of these is that adolescents have a limited number of clinical care encounters at which to receive the vaccine. In countries like the US and Luxembourg, routine vaccination of school children and adolescents take place primarily in the clinic; this is in contrast to countries like the UK, Canada, and Australia, where routine vaccination takes place in the schools.[8] And, unlike Tdap or MenACWY, the HPV vaccine series calls for three visits over 6 months. While patients need not restart the vaccine series if they do not receive the three doses within certain intervals, one cannot depend upon regular health maintenance visits or annual checkups to obtain the vaccines. Nordin et al. found that one-third of adolescents had no preventive care visits between the ages of 13 and 17, while an additional 40% had only one visit.[9] Fewer than 2% of the adolescents in that study actually followed the annual preventive care visits recommended by the American Academy of Pediatrics’ Bright Futures [10] and the AMA’s Guidelines for Adolescent Preventive Services. [11] Nonpreventive care visits were more common in this age group and ranged from 1 to 1.5 visits per year, and such visits could be used as ‘catch-up’ opportunities to administer needed vaccines. Still, in the one study that reported the incidence of missed opportunities to vaccinate against HPV, even among the visits that do occur for adolescents, the great majority fail to result in HPV vaccination when due.[12]

A lack of an obvious ‘pediatric’ benefit

A second reason for poor HPV vaccination rates is the lack of an obvious ‘pediatric’ benefit, in which an adolescent patient benefits from vaccination in the short term. The problem is not just that most HPV infections go unrecognized and undiagnosed, but rather the development of HPV cancers does not pose an immediate threat for adolescent health. For example, cervical cancer can take up to 10 or more years to develop as the result of persistent infection. This is quite different from other pediatric vaccine-preventable diseases such as meningococcal or rotavirus infections where the infections primarily occur in the pediatric age groups and cause immediate harm. Studies of parents and clinicians as well as adolescents indicate a lack of knowledge and familiarity with HPV infection and their sequelae for which they are asked to complete a three-dose vaccine series.[13–20]

An implication of sexual maturity

The fact that HPV infection is a sexually transmitted disease colors how parents and others view HPV vaccination.[21,22] Parents who expressed no intention to vaccinate against HPV in the coming 12 months frequently cite timing issues with the vaccine and, specifically, that their adolescent was not the appropriate age or was not sexually active.[17] Health professionals and parents have raised concerns that support for the vaccination or even discussion of the vaccine was tantamount to tacit approval of adolescent sexual activity.[23] Less frequently, parents specifically have raised the concern that vaccinating may increase sexual activity.[21,22,24,25] Focus groups have demonstrated that delays in HPV vaccination do result from parental attitudes regarding the risk to their children of sexually transmitted diseases, and concerns about the timing of the vaccine in relationship to sexual activity.[26]

A lack of school requirements

A fourth explanation for poor uptake of the HPV vaccine is that unlike other universally recommended vaccines for children most states do not have school requirements for HPV vaccination. School vaccination requirements, established in the US at the state rather than the federal level, have a significant impact on vaccine uptake in adolescents [27] and resulting vaccine-preventable disease rates.[28–30] Schwartz et al. reported in 2015 that only Virginia and the District of Columbia require the three-dose HPV series, 8 years after the ACIP first recommended routine use.[31] While some point to the relative newness of the vaccine, 8 years following the publication of the ACIP recommendations for the specific vaccines, 37 states (including the District of Columbia) had requirements for hepatitis B, 39 for varicella, 22 for meningococcal, and only 2 for HPV. Rhode Island adopted a requirement after the completion of this analysis.[32]

A politically contentious issue

HPV vaccination has become a contentious political issue since it was first licensed. In a 2007 analysis, Schwartz et al. reviewed the change in public opinion concerning HPV vaccination, which was initially quite positive with the licensure and recommendation, and turned negative following early efforts for states to require the vaccine.[33] These authors point out that the call for such requirements in less than a year’s time of the vaccine’s debut was unusually early as compared to the timetables for other routinely recommended vaccines. Arguing against the requirement, civil libertarians found themselves allied with social conservatives as well as with proponents of the antivaccine movement who claimed safety concerns. The authors also note that Merck aggressively promoted Gardasil before and after licensure and lobbied state legislators and governors in pursuit of the creation of school vaccination requirements.[33] These widely publicized efforts resulted in a negative public reaction.

The staggered rollout of recommendations

The staggered rollout of recommendations likely did not help HPV vaccine uptake (Figure 1). The ACIP recommended the HPV vaccines only for females from 2007 to 2010.[3,34] Thus, adolescents and their parents were taught that the vaccine was only for females for several years. In October 2009, the ACIP approved permissive language for the vaccine in males but did not recommend it.[4] Finally, in December 2011, the ACIP published a new recommendation for the vaccine in males.[5] The CDC cites the restriction to only females as a likely reason why states initially avoided school vaccination requirements for HPV.[35] Furthermore, previous efforts to limit vaccination recommendations to particular risk groups rather than universal vaccination have been shown to impede vaccine uptake among those at risk. In two cases – hepatitis B and influenza vaccination – ACIP moved from risk-based vaccination to universal vaccination in part to overcome the failure of risk-based vaccination.[36–38] In the third case, with a Lyme disease vaccine, the manufacturer stopped the manufacture and sale of the vaccine due to poor uptake.[39,40]

Faulty communication with parents

Problematic clinician-communication skills may play a major role in low HPV vaccine uptake, as suggested by parent responses when asked why they were not vaccinating their teens against HPV. Parents frequently cited a lack of knowledge and the absence of a physician recommendation as the reason for their intent not to vaccinate.[17,18] While the National Immunization Survey-Teen data indicate that clinicians recommend the HPV vaccine at a higher rate than the Tdap or MenACWY vaccines, some have suggested that clinicians are presenting the vaccine as special or different thereby failing to give what parents perceive as strong recommendations.[17,18] As a result, the Director of the Centers for Disease Control and Prevention, Thomas Frieden, MD, MPH, is calling for clinicians to make a strong recommendation for HPV vaccination along with other important vaccines.[41]

Population health interventions to improve HPV vaccination

To fully appreciate effective population health strategies to improve HPV vaccination, it is essential to understand public resistance to uptake and the evidence base negating common concerns. It is also critical to review commonly employed strategies that have not proven successful. In the following sections, we summarize the evidence that counters the common barriers to uptake and summarize failed strategies to HPV promotion as a broad contextual introduction to a brief overview of the state of the art in HPV vaccine uptake strategies and a more lengthy discussion of what population health interventions have to offer HPV vaccination.

What we know: the science behind the concerns

Reasons parents cite for not vaccinating their adolescents against HPV include not only their lack of knowledge or the lack of a clinician’s recommendation but also reasons that scientific study can directly refute. Parents have continuing questions and concerns regarding the need for the vaccine, the safety of the vaccine, and the timing of the vaccination.[17,18] Few cite concerns about access, expense, or vaccine effectiveness.[17,18] In the following sections, we address each of these concerns in light of current literature.

Need

Substantial evidence exists regarding the need for this vaccine. Most sexually active individuals in the US will at one point in their lifetimes become infected with HPV.[42] In England and the US, studies have shown that more than 40% of 15- to 24-year-old women are likely to become infected after 3 years’ time of sexual activity.[43–45] The infections are clinically asymptomatic and persist for 1–2 years even though the overwhelming majority of infected individuals clear the infections.[42] Thus, individuals can spread the infection to others unaware that they themselves are infected. However, depending on the HPV type, perhaps less than 10% of individuals do not clear the infections after 2 years. A fraction of these individuals will go on suffer dysplastic changes that can proceed to frank cancers involving the anogenital or oropharyngeal areas.[43,46] Experts estimate that 26,000 new cases of cancers caused by HPV occur each year in the US, with approximately 17,000 occurring in females and 9000 in males.[47] The vaccine prevents HPV infection and the cancers the HPV infection causes. It has a substantially high effectiveness rate against the strains the vaccine contains.[48] Furthermore, it appears to establish a long-lasting immunity.[49]

Safety

Postlicensure studies have confirmed prelicensure findings of safety [50] and have addressed concerns raised about autoimmune disorders.[51] Using data from Kaiser Permanente of California, Klein et al. examined the postvaccination intervals of nearly 200,000 females who received a dose of HPV vaccine from August 2006 through March 2008 and compared their incidence of hospitalizations and emergency department visits with time since their vaccination.[50] They found associations with same-day syncope and the appearance of skin infections in the first two weeks following vaccination but no new safety concerns. Drawing from the same population, they compared the incidence of new diagnoses of 16 autoimmune diseases identified a priori with matched unvaccinated individuals from the same two managed care organizations.[51] They did not identify any increased risk of autoimmune disease in those that were vaccinated compared to those that were not vaccinated. Vichnin et al. summarized more than 15 postlicensure safety studies of the quadrivalent HPV vaccine in more than 1 million individuals. In those studies, including both active and passive surveillance, serious adverse events occurred no more frequently than background rates.[52] Stillo et al. similarly reviewed postlicensure studies for the quadrivalent form but also added prelicensure studies as well as studies pre- and postlicensure for the bivalent form and reached the same conclusion.[53] Vesikari et al. published their safety and immunogenicity study of a new, nonavalent vaccine comparing it to the licensed, quadrivalent vaccine; the results found the safety profiles the same.[54] In 2015, the ACIP recommended the nonavalent vaccine for routine use along with the bivalent and quadrivalent vaccines, stating no preference.[55]

Timing

The vaccine prevents HPV-infection sequelae through the prevention of infection rather than through some postinfection mechanism. A systematic review of efficacy studies did not support the vaccine’s ability to protect against dysplasia in those previously infected, but some recipients do develop protective immunity before completing the series and intention-to-treat analyses demonstrate substantial value in completing the series among those sexually active and those previously infected with one strain but not another. [56] Thus, to achieve the greatest protection, recipients should complete the series before exposure to the virus. The vaccine is routinely recommended at 11–12 years of age, in part in recognition of the lack of regular clinician encounters through early adolescence,[9] and in part in recognition of the timing of HPV infection. Seventy-four percent of new HPV infections occur among those aged 15–24 years.[57] This relates to the ubiquity of infection and the timing of sexual debut. Twenty-seven percent of US females and 28% of males 15–17 years of age report ever having sexual intercourse.[58] Those percentages increase to 62.7 and 63.9% by 18–19 years of age. As for the concerns that vaccinating against HPV results in earlier sexual debut and increased sexual activity, studies have shown no actual association between HPV vaccination and sexual activity and its sequelae.[59–62]

What won’t work: the failure with education

Concerns with poor HPV vaccination rates have led to calls for improved efforts with patient-and-parent education as well as clinician communication. Research suggests that some communication practices are not effective in increasing vaccine uptake, however. A recent observational study suggested that vaccine communication language that evokes shared decision-making is less effective than use of expectant or presumptive language to vaccinate.[63] Analysis of conversations between clinicians and parents demonstrates that use of expectant or presumptive language (e.g. ‘You are due to have your HPV vaccine today, so the nurse will be in to deliver it’) results in vaccination completion more often than collaborative communication (e.g. ‘Are you interested in having an HPV vaccine today?’).[63] Unfortunately, the presumptive language approach led to less satisfaction for the parents with the visit compared with the shared decision-making approach.[64] Furthermore, while patients express that clinicians’ recommendations matter and that stronger recommendations are more effective than weaker ones in driving HPV vaccination,[65] Henrikson et al. reported the failure of a concerted effort to teach clinicians communication skills to improve the quality of their communication with patients about their vaccine recommendations.[66] This cluster randomized trial evaluating the impact of physician-targeted communication training on vaccine hesitancy in mothers of newborn infants failed to improve maternal vaccine hesitancy and did not improve physician self-efficacy around communicating with parents about vaccination.[66] Limitations of this study include a question of the intensity of the training as well as the effort of the intervention to pursue vaccination through shared decision-making.[67]

For some parents, current communication strategies about vaccination may increase misperceptions or reduce intention to vaccinate. In 2014, Nyhan and colleagues published the results of their study testing the effectiveness of five different forms of communication to address vaccine hesitancy among parents, specifically regarding the MMR vaccine with particular attention to fears that the MMR vaccine may cause autism.[68] They recruited participants through use of a nationally representative online panel and collected data in two waves from online interviews with parents with one or more children aged 17 or under living in their household. In the first wave, participants completed a series of measures to assess their attitudes toward vaccination and to document prior vaccination behavior with their children. In the second wave, participants were randomly assigned to receive one of four different messages about vaccination or a control message and were then asked a series of questions to evaluate misperceptions about MMR, concerns about MMR side effects, and intentions to vaccinate future children. None of the messages increased parents’ intention to vaccinate. Although messages that refuted claims of a link between MMR and autism were successful in reducing misperceptions that vaccines cause autism, among those with the least favorable attitudes toward vaccine, this message actually decreased intention to vaccinate. Participants who received messages containing images of sick children demonstrated an increase in their belief that there is a link between vaccination and autism, and participants who received messages containing a dramatic narrative about an infant in danger of dying from a vaccine-preventable disease showed an increase in beliefs about serious vaccine side effects. Nyhan et al. repeated the effort with the flu vaccine and found similar results.[69] These studies build on prior research demonstrating the failure of attempts to correct political misperceptions and the appearance of what has been termed the backfire effect.[70]

Recognizing the limitations of attempting to influence attitudes by countering misinformation, Horne et al. evaluated the effectiveness of an alternative approach to using scientific information to influence attitudes.[71] Rather than attempting to refute misinformation about vaccination, they aimed to introduce new information about vaccination by focusing on the probability of contracting disease in the absence of vaccination and the ramifications thereof. Adults recruited from a commercial crowd-sourcing effort were randomly assigned to one of three conditions: (1) the disease risk condition, (2) the correcting misinformation about the vaccine/autism link condition, or a (3) control intervention. The participants’ attitudes toward vaccine were assessed before and after the intervention. The authors found that the disease risk intervention led to a positive change in attitudes toward vaccination, even among participants who were initially quite skeptical of vaccines. The authors concluded that educational interventions to illustrate and emphasize the diseases that the vaccines prevent may be more effective in reducing vaccine hesitancy than educational interventions directed to dispel misconceptions about vaccine side effects and risks.[71]

However, a systematic review of a broad range of educational interventions to increase uptake of HPV vaccination showed that most interventions had disappointing results.[72] Fu et al. sought English-language studies of educational interventions designed to improve patient or parental knowledge or attitudes regarding HPV vaccination for eligible patients.[72] They found 33 eligible studies evaluating the impact of parental education, adolescent/young adult education, and comparative message persuasiveness, but, upon review, they found no clearly superior intervention ‘meriting strong recommendation for widespread implementation.’[72] It is clear that unique approaches to addressing the educational gaps associated with HPV vaccination uptake, both in clinical settings and in the general public, may require a multileveled perspective that involves not only patient populations, but also policy decision makers and healthcare professionals and that utilizes an effective population health intervention.[73]

The state of the art with HPV vaccine-uptake strategies

Niccolai and Hansen recently published a systematic review of US comparative-effectiveness studies of practice- and community-based interventions that sought to improve HPV vaccination rates among adolescents 18 years and younger.[74] A total of 14 studies were included in this review evaluating a variety of approaches including reminder/recall systems, clinician-focused interventions, school-located programs and social marketing in diverse populations and geographic locations. The vast majority of studies reported significant improvements in at least one HPV vaccination outcome.

Briss et al.’s systematic review of interventions to improve vaccination rates published in 2000 is in agreement with both the results reported by Niccolai and Hansen and the study by Fu et al. [72] pointing to a greater effectiveness of system-level rather than individual-level intervention.[75] Briss et al.’s systematic reviews of the effectiveness of population-based interventions aimed at improving vaccination coverage found strong evidence for reminder/recall communications, point-of-care reminders, and standing orders for vaccination.

What population health interventions have to offer HPV vaccination

Table 1 briefly summarizes the findings in the literature regarding evidence-based population health approaches that improve HPV vaccination uptake. Of note, in their analysis of the most recent National Immunization Survey-TEEN survey results for HPV vaccine uptake among US adolescents 13–17 years of age, Reagan-Steiner et al. summarized strategies that were adopted in states that demonstrated higher-than-average improvements in vaccine uptake.[2] Specifically, in the vast majority of jurisdictions that showed increased HPV vaccination coverage among females, a combination of strategies was implemented. Effective strategies included immunization reminder/recall systems; practice-focused strategies targeting staff, clinicians, and parents; assessment and feedback activities; and school-based HPV vaccination programs. These and other evidence-based population health interventions to improve HPV vaccination are summarized below.

Table 1.

Evidence-based population health interventions for human papillomavirus vaccination.

Intervention	Description
Reminder/recall systems	Reminders: messages for upcoming or due vaccinations Recalls: messages for past due vaccinations
Standing orders/ Nursing protocols	Policies that permit nurses to treat patients per protocol without clinician orders Overcomes potential barriers in scheduling visits with clinician
Point-of-care reminders	Notifications to clinicians at patient encounter Requires patient to present for care
Audit-and-feedback	Reports on vaccination rates empanelled to a clinician or a practice Reports are not dependent on patient pre-senting for care
School-located immunization	Strategy that utilizes schools as a platform for vaccination delivery Can reduce out-of-pocket costs and elim-inate potential barriers associated with clinic visits

Reminder/recall systems

Reminders refer to messages anticipating a vaccine coming due or currently due, whereas recalls refer to situations when the vaccination is past due. Reminder/recall systems do not depend upon the patient presenting for care and so they overcome the common barriers of lack of adolescent participation in preventive health care [9] and the lack of parental awareness of the vaccine recommendations. [17] Reminder/recall efforts to notify the parent and/ or the adolescent when the HPV vaccine is due or past due have been shown to be effective whether using US mail, telephone, auto dialers, text messaging, or outreach visits.[74,76–82]

Standing orders or nursing protocols

Standing orders or nursing protocols refer to healthcare organization policies that permit nurses to treat patients per protocol without clinician orders. These facilitate relatively easy, efficient, and cost-effective visits as they do not require clinician involvement or assessment. Briss et al. demonstrated the effectiveness of this approach with vaccination.[75] Experts have called for use of standing orders/nursing protocols with adolescent and adult vaccination.[83,84] Dempsey et al. demonstrated acceptability of standing orders/nursing protocols specifically with HPV vaccination among both adolescent and adult patients.[85] The Minnesota Department of Health, among others, publishes up-to-date nursing protocols for vaccinations including HPV vaccination (http://www.health.state.mn.us/divs/idepc/immunize/hcp/protocols/) as does the Immunization Action Coalition (http://www.immunize.org/standing-orders/).

Point-of-care reminders

Point-of-care reminders such as electronic decision support and alerts that notify clinicians that vaccinations or other interventions are due at the time of the clinical encounter with the patient have been shown to be effective with vaccination, in general,[75] and with HPV vaccination, in particular.[74,79,86] Unlike reminder/recalls and standing orders/nursing protocols, point-of-care reminders require the patient to present for care, which is a known limitation among adolescent populations who demonstrate low levels of participation in preventive care services.[9]

Audit and feedback systems

Audit and feedback systems involve systematic reporting of measurements conducted on the clinician’s or the practice’s actual rate of success with a given intervention to the individual clinician or to the practice. Briss et al. showed these systems are generally effective with immunization,[75] and additional studies have demonstrated similar rates of success with HPV vaccination.[74,79,86–88] Depending on how the audit is configured, these systems can capture patients empaneled to a clinician or a practice and measure their vaccination rates regardless of whether the patient presents for care. Utilizing a regional immunization registry can improve the accuracy of the audit and account for vaccines received in settings other than the clinical practice, such as school-located immunization efforts.

School-based HPV vaccination programs

In a 2014 paper published in this journal, Shah et al. extensively reviewed alternative settings for adolescent vaccines such as schools, pharmacies, school health centers, and specialty clinics.[89] Indeed, school-located immunization efforts have been demonstrated to improve HPV vaccination rates in many countries worldwide,[90–92] including Ontario, Canada, with third-dose HPV vaccine uptake rates of 59%;[93,94] Prince Edward Island, Canada, with 82%; [95] England with 76–80%;[96] Brazil with a rate of 85%;[97] Rwanda with a rate of 93%;[98] and Australia with rates as high as 90%.[99,100] While it is true the US routinely relies on clinic-based settings for childhood and adolescent vaccinations, despite some logistical barriers,[101–103] US school-located vaccination programs, in general, have been found to be useful in improving immunization rates among children and adolescents, particularly for new vaccines or vaccines with expanded or new recommendations.[92] Furthermore, published studies provide strong evidence that school-located vaccination programs decrease rates of vaccine-preventable illness and associated morbidity and mortality.[92] In the US, for HPV vaccination, at least one substantive effort, conducted in Guilford County, North Carolina, was quite successful in increasing uptake and completion of the HPV vaccine among middle-school girls attending schools with temporary clinics that provided the HPV vaccine.[104] Furthermore, US parents are generally supportive of HPV vaccination in the schools, although less so than for Tdap, MenACWY, or influenza.[105–107] A frequently encountered barrier to school-located vacci-nation is funding programs through third-party payers.[103,108,109] These barriers, however, can and have been overcome in the US.

Expert commentary

To improve population uptake and completion of the HPV vaccine, adoption of several evidence-based population health strategies is encouraged, including immunization reminder/recall systems, standing orders/nursing protocols for immunization, point-of-care reminders, systematic audit and feedback for clinicians and practices, and school-located HPV vaccination programs. Such population-based strategies have significant potential to improve HPV vaccination coverage. School-located HPV vaccination programs, for example, will directly address one of the barriers to HPV vaccine uptake – the lack of clinical care encounters – by providing a proven alternative source of vaccination for children. Other barriers reviewed above, however, must be carefully addressed. One barrier is that HPV vaccination early on became a politically contentious issue. We must take care to avoid further provocation and polarization when pursuing these population-health strategies. We would advise that the vaccine manufacturers of HPV vaccines not play a principal role in leading for the adoption of these strategies. Furthermore, we would advise against school requirements for the vaccine at this time. Such efforts might further weaken public trust [110] and call school requirements for other routine vaccines into question.[111] Instead, efforts should focus on access combined with education and clear articulation of a strong recommendation and expectation for routine vaccination.

Clinicians thus should treat every clinical encounter as an opportunity to vaccinate, using visits for acute illness, injury, and chronic disease to review and address vaccination. Clinician recommendation is a consistent and strong predictor of use of preventive services, including vaccination.[17,65,112–114] Thus, clinicians must communicate their strong recommendations for the HPV vaccine, adopting effective strategies to understand and address any patient or parental concerns about vaccination. [63,115,116]

Five-year view

Although the HPV vaccine has been available in the US for nearly a decade, uptake has been disappointing and financial, legal, political, and cultural challenges to widespread adoption remain. State-mandated school requirements for vaccination have been shown to increase population vaccine coverage and serve as a foundation of childhood vaccination efforts; however, only two states (Rhode Island and Virginia) and the District of Columbia currently require the HPV vaccine for school entry.[31,117] At this time, over half of the states (29 states) have no laws pertaining to school entry, funding to cover the cost of vaccination, or required public education.[117] Given the current climate and the previous backlash in response to early attempts at state HPV vaccination requirements,[33] rapid proliferation of state mandates for HPV vaccination seems unlikely. If states with current school requirements are able to overcome the opposition and maintain their requirements, they will likely enjoy substantial improvements in their vaccination rates. Within this larger political context, developing outreach to provide the vaccines in schools (whether required or not) could help the US improve its vaccination rates and obtain rates that approximate the HealthyPeople 2020 goals.

In addition to efforts at the state and local levels, clinicians have the opportunity to significantly improve HPV vaccination rates in the next five years. Clinicians throughout the country are increasingly evaluated and reimbursed based on meeting quality metrics and reducing costs of care for assigned populations of patients. Vaccination rates are a key metric in many of these evaluations, and clinicians will need to demonstrate that their patient population is properly vaccinated. As a result, practices have the opportunity to adopt population health interventions that have been shown to be effective at the practice level. The implementation of reminder/recall systems, standing orders/nursing protocols, and point-of-care reminders will enable clinicians to substantially improve HPV vaccination rates within their patient populations.

Key issues.

• The US currently suffers low rates of human papillomavirus (HPV) vaccination.

• Adolescents suffer low access to vaccination (but for not for reasons one would think); they simply do not present for preventive care and rarely utilize other types of health care.

• Natural biases make parents question the vaccine biases based on the basis of the HPV transmission and the timing of the pathology.

• Clinicians have been cited for failing to recommend the vaccine and the same biases that hamper parents may hamper them as well; moreover, they do not have the same access to adolescent patients as they do to infants and preschoolers who more regularly attend clinic care.

• Drawing from past experience, clinicians must adopt population health interventions to improve HPV vaccination rates. Effective interventions include reminder recalls, standing orders/nursing protocols, point-of-care prompts, and audit-and-feedback mechanisms. Finally, clinicians should consider how they can support school-located immunization programs.