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An effective human papillomavirus vaccination policy will reduce infection- and malignancy-related morbidity and mortality

      Executive Summary

      Twelve human papillomaviruses (HPVs) are classified as strong human carcinogens, commonly referred to as high-risk HPVs (hrHPVs), and are responsible for nearly all cervical malignancies and 40% to 50% of all vaginal and vulvar cancers in women (
      • Bouvard V.
      • Baan R.
      • Straif K.
      • Grosse Y.
      • Secretan B.
      • El Ghissassi F.
      • et al.
      A review of human carcinogens—Part B: Biological agents.
      ,
      • International Agency for Research on Cancer
      Preamble: IARC Monographs on the Evaluation of Carcinogenic Risks to Humans.
      ,
      International Agency for Research on Cancer (IARC) Working Group on Evaluation of Carcinogenic Risks to Humans
      IARC Monographs on the Evaluation of Carcinogenic Risks to Humans.
      ). Together these hrHPVs are the cause of ≥75% of anal and perianal cancers in male and female adults (
      • Bosch F.X.
      • de Sanjose S.
      Chapter 1: Human papillomavirus and cervical cancer—burden and assessment of causality.
      ,
      • Clifford G.M.
      • Smith J.S.
      • Plummer M.
      • Munoz N.
      • Franceschi S.
      Human papillomavirus types in invasive cervical cancer worldwide: A meta-analysis.
      ,
      • Munoz N.
      Human papillomavirus and cancer: The epidemiological evidence.
      ,
      • Walboomers J.M.
      • Jacobs M.V.
      • Manos M.M.
      • Bosch F.X.
      • Kummer J.A.
      • Shah K.V.
      • et al.
      Human papillomavirus is a necessary cause of invasive cervical cancer worldwide.
      ). Currently approved HPV vaccines are safe and highly efficacious in preventing HPV16- and HPV18-caused precancers. They also provide >70% protection against all cervical cancers, most vulvar and vaginal HPV cancers, and >75% of anal cancers (
      • Dillner J.
      • Kjaer S.K.
      • Wheeler C.M.
      • Sigurdsson K.
      • Iversen O.E.
      • Hernandez-Avila M.
      • et al.
      Four year efficacy of prophylactic human papillomavirus quadrivalent vaccine against low grade cervical, vulvar, and vaginal intraepithelial neoplasia and anogenital warts: randomised controlled trial.
      ,
      • Garland S.M.
      • Hernandez-Avila M.
      • Wheeler C.M.
      • Perez G.
      • Harper D.M.
      • Leodolter S.
      • et al.
      Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases.
      ,
      • Harper D.M.
      • Franco E.L.
      • Wheeler C.
      • Ferris D.G.
      • Jenkins D.
      • Schuind A.
      • et al.
      Efficacy of a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and 18 in young women: A randomised controlled trial.
      ,
      • Joura E.
      • Bautista O.
      • Luxembourg A.
      A 9-valent HPV vaccine in women.
      ,
      • Joura E.A.
      • Pils S.
      Vaccines against human papillomavirus infections: Protection against cancer, genital warts or both?.
      ). The Academy supports the acceleration of HPV Vaccine Uptake in the US communities, consistent with recommendations by the 2012 to 2013 President's Cancer Panel recommendations and Healthy People 2020 goals (IID-11.4, 11.5) (

      Healthy People 2020. Immunization and Infectious Diseases: IID-11 Increase routine vaccination coverage levels for adolescents. In U.S. Department of Health and Human Services Office of Disease Prevention and Health Promotion. Washington, DC.

      ,
      • Rimer B.K.
      • Harper H.
      • Witte O.N.
      ).

      Background

      Worldwide, 12 HPVs are classified as strong human carcinogens by the American Cancer Association and the International Agency for Research on Cancer, which is a World Health Organization intergovernmental agency (
      • Bouvard V.
      • Baan R.
      • Straif K.
      • Grosse Y.
      • Secretan B.
      • El Ghissassi F.
      • et al.
      A review of human carcinogens—Part B: Biological agents.
      ,
      • International Agency for Research on Cancer
      Preamble: IARC Monographs on the Evaluation of Carcinogenic Risks to Humans.
      ,
      International Agency for Research on Cancer (IARC) Working Group on Evaluation of Carcinogenic Risks to Humans
      IARC Monographs on the Evaluation of Carcinogenic Risks to Humans.
      ). These HPVs include HPV types 16 and 18, and are responsible for nearly all cervical malignancies and 40% to 50% of vaginal and vulvar cancers in women, along with 75% of anal and perianal cancers in male and female adults (
      • Bosch F.X.
      • de Sanjose S.
      Chapter 1: Human papillomavirus and cervical cancer—burden and assessment of causality.
      ,
      • Bouvard V.
      • Baan R.
      • Straif K.
      • Grosse Y.
      • Secretan B.
      • El Ghissassi F.
      • et al.
      A review of human carcinogens—Part B: Biological agents.
      ,
      • Clifford G.M.
      • Smith J.S.
      • Plummer M.
      • Munoz N.
      • Franceschi S.
      Human papillomavirus types in invasive cervical cancer worldwide: A meta-analysis.
      ,
      • International Agency for Research on Cancer
      Preamble: IARC Monographs on the Evaluation of Carcinogenic Risks to Humans.
      ,
      International Agency for Research on Cancer (IARC) Working Group on Evaluation of Carcinogenic Risks to Humans
      IARC Monographs on the Evaluation of Carcinogenic Risks to Humans.
      ,
      • Munoz N.
      Human papillomavirus and cancer: The epidemiological evidence.
      ,
      • Walboomers J.M.
      • Jacobs M.V.
      • Manos M.M.
      • Bosch F.X.
      • Kummer J.A.
      • Shah K.V.
      • et al.
      Human papillomavirus is a necessary cause of invasive cervical cancer worldwide.
      ). HPVs are transmitted by direct skin-to-skin contact (
      • Giuliano A.R.
      • Nyitray A.G.
      • Kreimer A.R.
      • Pierce Campbell C.M.
      • Goodman M.T.
      • Sudenga S.L.
      • et al.
      EUROGIN 2014 roadmap: Differences in human papillomavirus infection natural history, transmission and human papillomavirus-related cancer incidence by gender and anatomic site of infection.
      ,
      • Stanley M.
      Pathology and epidemiology of HPV infection in females.
      ). Most genital infections are commonly acquired during adolescence and young adulthood and cleared within 2 years of infection (
      • Giuliano A.R.
      • Nyitray A.G.
      • Kreimer A.R.
      • Pierce Campbell C.M.
      • Goodman M.T.
      • Sudenga S.L.
      • et al.
      EUROGIN 2014 roadmap: Differences in human papillomavirus infection natural history, transmission and human papillomavirus-related cancer incidence by gender and anatomic site of infection.
      ). However, HPV infections are painless, without symptoms, and some infections become persistent and undetected over years, with several developing into cancers that affect middle-age and older adults. Signs of malignancy, such as unexplained postcoital bleeding, occur late in the natural history of disease.
      HPV vaccines are safe and prevent personally and publicly costly human cancers. Three Food and Drug Administration (FDA)-approved HPV prevention vaccines are approved for administration, and each is shown to be safe and highly efficacious in preventing HPV16- and HPV18-caused precancers: Cervarix (HPV2), Gardasil (HPV4), and Gardasil-9 (HPV9) (
      • Harper D.M.
      • DeMars L.R.
      HPV vaccines—A review of the first decade.
      ). All three provide more than 70% protection against all cervical cancers, most vulvar and vaginal HPV cancers, and more than 75% of anal cancers (
      • Dillner J.
      • Kjaer S.K.
      • Wheeler C.M.
      • Sigurdsson K.
      • Iversen O.E.
      • Hernandez-Avila M.
      • et al.
      Four year efficacy of prophylactic human papillomavirus quadrivalent vaccine against low grade cervical, vulvar, and vaginal intraepithelial neoplasia and anogenital warts: randomised controlled trial.
      ,
      • Garland S.M.
      • Hernandez-Avila M.
      • Wheeler C.M.
      • Perez G.
      • Harper D.M.
      • Leodolter S.
      • et al.
      Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases.
      ,
      • Harper D.M.
      • Franco E.L.
      • Wheeler C.
      • Ferris D.G.
      • Jenkins D.
      • Schuind A.
      • et al.
      Efficacy of a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and 18 in young women: A randomised controlled trial.
      ,
      • Joura E.
      • Bautista O.
      • Luxembourg A.
      A 9-valent HPV vaccine in women.
      ,
      • Joura E.A.
      • Pils S.
      Vaccines against human papillomavirus infections: Protection against cancer, genital warts or both?.
      ). However, the HPV9 vaccine also prevents five additional HPVs infections that are responsible for nearly 20% of cervical cancers worldwide: HPV31, 33, 45, 52, and 58 (
      • Zhai L.
      Tumban E. Gardasil-9: A global survey of projected efficacy.
      ). Lastly, HPV4 and HPV9 vaccines also protect against HPV6 and 11 (
      • Zhai L.
      Tumban E. Gardasil-9: A global survey of projected efficacy.
      ). These two HPVs cause warty abnormalities that seldom, if ever, cause cancer. However, these warty abnormalities cause distress among affected individuals and inflate cancer-screening costs caused by perturbations they induce in Pap test cervical cancer-screening programs that are employed nationally (
      • Dillner J.
      • Kjaer S.K.
      • Wheeler C.M.
      • Sigurdsson K.
      • Iversen O.E.
      • Hernandez-Avila M.
      • et al.
      Four year efficacy of prophylactic human papillomavirus quadrivalent vaccine against low grade cervical, vulvar, and vaginal intraepithelial neoplasia and anogenital warts: randomised controlled trial.
      ,
      • Garland S.M.
      • Hernandez-Avila M.
      • Wheeler C.M.
      • Perez G.
      • Harper D.M.
      • Leodolter S.
      • et al.
      Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases.
      ,
      • Joura E.
      • Bautista O.
      • Luxembourg A.
      A 9-valent HPV vaccine in women.
      ,
      • Joura E.A.
      • Pils S.
      Vaccines against human papillomavirus infections: Protection against cancer, genital warts or both?.
      ).
      The greatest population protection and health-care savings will be realized when all eligible children under 13 years of age complete HPV2, HPV4, or HPV9 vaccine on schedule (
      • Jit M.
      • Brisson M.
      • Laprise J.F.
      • Choi Y.H.
      Comparison of two dose and three dose human papillomavirus vaccine schedules: Cost effectiveness analysis based on transmission model.
      ,
      • Jit M.
      • Laprise J.F.
      • Choi Y.H.
      • Brisson M.
      Fewer than three doses of HPV vaccine.
      ,
      • Laprise J.F.
      • Markowitz L.E.
      • Chesson H.W.
      • Drolet M.
      • Brisson M.
      Comparison of 2-dose and 3-dose 9-valent human papillomavirus vaccine schedules in the United States: A cost-effectiveness analysis.
      ). The HPV vaccines are composed of laboratory-manufactured proteins and contain no active agent, making children without allergies to constituents, such as yeast, eligible for vaccination. Data suggest the cost per quality-adjusted life-year gained through HPV vaccination of 12-year-old girls, using three doses of HPV2, HPV4, or HPV9 to existing cervical cancer screening practices, ranges from $3,906 to $14,723 (
      • Chesson H.W.
      • Ekwueme D.U.
      • Saraiya M.
      • Markowitz L.E.
      Cost-effectiveness of human papillomavirus vaccination in the United States.
      ,
      • Chesson H.W.
      • Forhan S.E.
      • Gottlieb S.L.
      • Markowitz L.E.
      The potential health and economic benefits of preventing recurrent respiratory papillomatosis through quadrivalent human papillomavirus vaccination.
      ). Newly recommended two-dose vaccine strategies are more cost-effective, with equivalent population outcomes for cervical cancer screening practices, depending upon the duration of vaccine effectiveness (
      • Chesson H.W.
      • Ekwueme D.U.
      • Saraiya M.
      • Markowitz L.E.
      Cost-effectiveness of human papillomavirus vaccination in the United States.
      ,
      • Chesson H.W.
      • Forhan S.E.
      • Gottlieb S.L.
      • Markowitz L.E.
      The potential health and economic benefits of preventing recurrent respiratory papillomatosis through quadrivalent human papillomavirus vaccination.
      ,
      • Laprise J.F.
      • Markowitz L.E.
      • Chesson H.W.
      • Drolet M.
      • Brisson M.
      Comparison of 2-dose and 3-dose 9-valent human papillomavirus vaccine schedules in the United States: A cost-effectiveness analysis.
      ).
      All three vaccines are recommended for children 11 to 12 years of age and may be administered safely to children as young as 9 years of age. HPV vaccines are safe and effective and are recommended for 13- to 26-year-olds as a catch-up vaccination schedule. HPV2, HPV4, and HPV9 vaccines provide effective protection when two doses are administered over 6 to 12 months for 9- to 14-year-olds (
      • Jit M.
      • Brisson M.
      • Laprise J.F.
      • Choi Y.H.
      Comparison of two dose and three dose human papillomavirus vaccine schedules: Cost effectiveness analysis based on transmission model.
      ,
      • Jit M.
      • Laprise J.F.
      • Choi Y.H.
      • Brisson M.
      Fewer than three doses of HPV vaccine.
      ,
      • Laprise J.F.
      • Markowitz L.E.
      • Chesson H.W.
      • Drolet M.
      • Brisson M.
      Comparison of 2-dose and 3-dose 9-valent human papillomavirus vaccine schedules in the United States: A cost-effectiveness analysis.
      ,
      • Meites E.
      • Kempe A.
      • Markowitz L.E.
      Use of a 2-dose schedule for human papillomavirus vaccination-updated recommendations of the advisory committee on immunization practices.
      ). For 15- to 26-year-olds, HPV2, HPV4, and HPV9 vaccines are each given as three doses over 6 months (
      • Petrosky E.
      • Bocchini Jr., J.A.
      • Hariri S.
      • Chesson H.
      • Curtis C.R.
      • Saraiya M.
      • et al.
      Use of 9-valent human papillomavirus (HPV) vaccine: Updated HPV vaccination recommendations of the Advisory Committee on Immunization Practices.
      ). There is no on-label recommended use for HPV vaccines in adults aged 27 years and older. In 2013, population-based data showed only 57.3% of girls and 34.6% of boys aged 13 to 17 years received at least one dose; however, among those receiving at least one dose, 70.4% and 48.3% of similar-aged girls and boys completed the three-dose series in 2013 (
      • Elam-Evans L.D.
      • Yankey D.
      • Jeyarajah J.
      • Singleton J.A.
      • Curtis R.C.
      • MacNeil J.
      • et al.
      National, regional, state, and selected local area vaccination coverage among adolescents aged 13-17 years—United States, 2013.
      ,
      • Stokley S.
      • Jeyarajah J.
      • Yankey D.
      • Cano M.
      • Gee J.
      • Roark J.
      • et al.
      Human papillomavirus vaccination coverage among adolescents, 2007-2013, and postlicensure vaccine safety monitoring, 2006-2014—United States.
      ).
      HPVs that cause cancers can be reduced significantly in the population when we vaccinate youth using effective vaccines. Recent adjusted analyses show that even with modest HPV vaccine coverage, the prevalence of vaccine-specific HPVs was reduced to nearly 1.5- to 2.8-fold among 14- to 24-year-olds between 2009 and 2012 alone (
      • Markowitz L.E.
      • Liu G.
      • Hariri S.
      • Steinau M.
      • Dunne E.F.
      • Unger E.R.
      Prevalence of HPV after introduction of the vaccination program in the United States.
      ). Nonetheless, these data are worrisome also; specifically, the 14- to 24-year old vaccinated girls were more often white than were the 14- to 24-year old unvaccinated girls (
      • Markowitz L.E.
      • Liu G.
      • Hariri S.
      • Steinau M.
      • Dunne E.F.
      • Unger E.R.
      Prevalence of HPV after introduction of the vaccination program in the United States.
      ). If these disparities remain, we should expect even greater cancer disparities related to race among middle- and older-age women beginning in 2040. In essence, merely preventing cancer in one group translates into greater gaps across groups.

      Responses and Policy Options

      Universal vaccine coverage to prevent cancers in adulthood is the goal of domestic and international HPV vaccine campaigns. Responsible policy and planning efforts will promote vaccination that prevents human suffering and reduces U.S. expenditures. For example, reduced costs to consumers will promote vaccination, as addressed by U.S. FDA approvals and the Centers for Disease Control and Prevention (CDC)'s Advisory Committee on Immunization Practices (ACIP) recommendations to adopt HPV vaccination as a standard of care. Both the U.S. Department of Health and Human Services (HHS) and the Health Resources and Services Administration support the Vaccines for Children (VFC) Program and the National Vaccine Injury Compensation Program that buttress vaccination programs that are administered at state and at local levels. VFC provides no-cost vaccine for uninsured, underinsured, and special-population children (e.g., American Indian and Alaska Natives) aged 18 years and younger. VFC approval sets the standard for most private insurance carriers to provide coverage under the Affordable Care Act (
      • Compilation of Patient Protection and Affordable Care Act
      Office of the Legislative Counsel.
      ). National immunization survey data show 62.8%, 52.2%, and 41.9% of 13-17 year olds girls had completed at least one, two, or three HPV-vaccine doses in 2015 (
      • Reagan-Steiner S.
      • Yankey D.
      • Jeyarajah J.
      • Elam-Evans L.D.
      • Curtis C.R.
      • MacNeil J.
      • et al.
      National, regional, state, and selected local area vaccination coverage among adolescents aged 13-17 years—United States, 2015.
      ). Completion rates for 2015 are up 3% to 6% over 2014 levels. (
      • Reagan-Steiner S.
      • Yankey D.
      • Jeyarajah J.
      • Elam-Evans L.D.
      • Curtis C.R.
      • MacNeil J.
      • et al.
      National, regional, state, and selected local area vaccination coverage among adolescents aged 13-17 years—United States, 2015.
      ). Similarly aged boys showed 49.8%, 39.0%, and 28.1% completed greater than one, two, and three HPV vaccine doses in 2015, up 19% to 30% over 2014 estimates (
      • Reagan-Steiner S.
      • Yankey D.
      • Jeyarajah J.
      • Elam-Evans L.D.
      • Curtis C.R.
      • MacNeil J.
      • et al.
      National, regional, state, and selected local area vaccination coverage among adolescents aged 13-17 years—United States, 2015.
      ). Nonetheless, funding alone cannot account for less than optimal, although increasing, rates of population coverage for HPV vaccine (
      • Reagan-Steiner S.
      • Yankey D.
      • Jeyarajah J.
      • Elam-Evans L.D.
      • Curtis C.R.
      • MacNeil J.
      • et al.
      National, regional, state, and selected local area vaccination coverage among adolescents aged 13-17 years—United States, 2015.
      ,
      • Whitney C.G.
      • Zhou F.
      • Singleton J.
      • Schuchat A.
      Centers for Disease C, Prevention
      Benefits from immunization during the vaccines for children program era—United States, 1994-2013.
      ).

       Guideline Interpretation Opportunities

      Clear, easily interpreted guidelines are essential to both provider and parent adherence. Evidence has accumulated at a rapid pace and recommendations have changed significantly across products, age groups, sex, and time beginning with domestic licensing in 2006. For example, between 2015 and 2016, HPV vaccination recommendations changed significantly. In 2015, VFC Resolution 2/01-01 recommended HPV vaccines varied for boys and girls <19 years of age; however, rules were modified in mid-2016 to advise two- and three-dose regimens for HPV2, HPV4, and HPV9 administered to all 9- to 14-year-olds and 15- to 18-year-olds, respectively (VFC Resolution 10/16-2) (
      • Advisory Committee on Immunization Practices, Vaccines for Children Program
      Vaccines to prevent human papillomavirus.
      ). Newly evolving evidence shows drug labeling for use, including dose and dispensation, influences risk for errors made by both prescribers and patients (
      • Cochran G.L.
      • Klepser D.G.
      • Morien M.
      • Lomelin D.
      • Schainost R.
      • Lander L.
      From physician intent to the pharmacy label: Prevalence and description of discrepancies from a cross-sectional evaluation of electronic prescriptions.
      ,
      • Wolf M.S.
      • Davis T.C.
      • Curtis L.M.
      • Bailey S.C.
      • Knox J.P.
      • Bergeron A.
      • et al.
      A patient-centered prescription drug label to promote appropriate medication use and adherence.
      ,
      • Yin H.S.
      • Parker R.M.
      • Sanders L.M.
      • Dreyer B.P.
      • Mendelsohn A.
      • Bailey S.
      • et al.
      Effect of medication label units of measure on parent choice of dosing tool: A randomized experiment.
      ). As with other medications, the most simplified evidence-based recommendations may promote greater adherence over older guidance that provided different recommendations for one vaccine type over another, and for male over female populations.

       Provider Strategies

      Although high-quality recommendations for HPV vaccination show greater uptake and follow-through than low-quality or no recommendation, most HPV vaccine utilization research focuses on provider recommendations. For example, survey data show parents who perceive receiving high-quality recommendations for HPV vaccine show greater uptake and completion for age-eligible youth. Among 1,495 parents of 11- to 17-year-old boys and girls, 63% and 86%, respectively, stated their providers characterized HPV vaccination as very or extremely important and preventive for cancer (
      • Gilkey M.B.
      • Calo W.A.
      • Moss J.L.
      • Shah P.D.
      • Marciniak M.W.
      • Brewer N.T.
      Provider communication and HPV vaccination: The impact of recommendation quality.
      ). Any recommendation improved HPV vaccine initiation over no recommendation: 9.3- and 4.1-fold higher odds for high-quality and low-quality recommendations (p < .05), respectively. However, only high-quality recommendations improved three-dose completion (
      • Gilkey M.B.
      • Calo W.A.
      • Moss J.L.
      • Shah P.D.
      • Marciniak M.W.
      • Brewer N.T.
      Provider communication and HPV vaccination: The impact of recommendation quality.
      ). Overreliance on any single strategy, including the quality of provider recommendations, will delay and possibly thwart efforts to reach the Healthy People 2020 target of 80% completion of the two- or three-dose vaccine series. Provider opinions have varied over time, region, and personal beliefs, such as in early and late vaccine adopters (
      • Gilkey M.B.
      • Calo W.A.
      • Moss J.L.
      • Shah P.D.
      • Marciniak M.W.
      • Brewer N.T.
      Provider communication and HPV vaccination: The impact of recommendation quality.
      ,
      • Kahn J.A.
      • Cooper H.P.
      • Vadaparampil S.T.
      • Pence B.C.
      • Weinberg A.D.
      • LoCoco S.J.
      • et al.
      Human papillomavirus vaccine recommendations and agreement with mandated human papillomavirus vaccination for 11-to-12-year-old girls: a statewide survey of Texas physicians.
      ). Few public service announcements promote the use of HPV vaccine to prevent cancer, and more importantly, parents, children, and young adults live in communities composed of a wide variety of frequented businesses and settings as compared to health-care providers whom they visit (comparatively) infrequently.
      Novel approaches that combine skilled providers, prevention, and business approaches may promote cost-effective vaccination delivery programs that can be promulgated across the globe. For example, public-private partnerships between pharmacies and public school districts may increase access using business models already developed for licensed pharmacists, nurse practitioners, and registered nurses (
      • Brewer N.T.
      • Chung J.K.
      • Baker H.M.
      • Rothholz M.C.
      • Smith J.S.
      Pharmacist authority to provide HPV vaccine: novel partners in cervical cancer prevention.
      ). Accordingly, evidence-based programs that incentivize novel approaches to safe, on-time, cost-effective vaccine delivery should be trialed and implemented nationwide.

       School- and Community-Based Strategies

      Worldwide, school-based vaccination is associated with successful HPV-vaccine uptake. School settings are frequented by 9- to 18-year-old youth, making vaccination easily accessible to children, especially when parents work. In the United States, school vaccination programs represent unfunded mandates in most settings. New strategies for school-based vaccination will improve adherence to administration guidelines for both mandated and nonmandated vaccines. For acute communicable diseases, such as measles, mumps, and rubella, absenteeism and large outbreaks could be prevented using school-based vaccinations. For HPV vaccines, school-based programs would provide multiple opportunities, especially across the 9- to 14-year age range, for parents to initiate vaccination, lending choice without the penalty of missed work needed for provider-based vaccination programs. A variety of novel approaches might be tested; for example, contemporary pharmacies practice using a distribution-based business model. Pharmacists are empowered to vaccinate adults in 80% of U.S. states and territories, and although they are less frequently authorized to immunize minors, model legislation and policies for vaccinating youth have been tested. For example, only 24% to 31% of states regulate and allow pharmacist-administered vaccine administration to minors, including HPV vaccines (
      • Brewer N.T.
      • Chung J.K.
      • Baker H.M.
      • Rothholz M.C.
      • Smith J.S.
      Pharmacist authority to provide HPV vaccine: novel partners in cervical cancer prevention.
      ).

       International Strategies

      Strategies that provide varied options, including routine prescription by providers and access for vaccine delivery, have increased uptake. Australia, the United Kingdom, Scotland, and Brazil report real and model-driven data that suggest significant and cost-effective cancer and precancer prevention can be realized through well-planned and well-executed vaccination programs in economically developed and developing settings (
      • Barbaro B.
      • Brotherton J.M.
      Assessing HPV vaccine coverage in Australia by geography and socioeconomic status: Are we protecting those most at risk?.
      ,
      • Cameron R.L.
      • Kavanagh K.
      • Pan J.
      • Love J.
      • Cuschieri K.
      • Robertson C.
      • et al.
      Human papillomavirus prevalence and herd immunity after introduction of vaccination program, Scotland, 2009-2013.
      ,
      • Clifford G.M.
      • Smith J.S.
      • Plummer M.
      • Munoz N.
      • Franceschi S.
      Human papillomavirus types in invasive cervical cancer worldwide: A meta-analysis.
      ,
      • Fregnani J.H.
      • Carvalho A.L.
      • Eluf-Neto J.
      • Ribeiro Kde C.
      • Kuil Lde M.
      • da Silva T.A.
      • et al.
      A school-based human papillomavirus vaccination program in Barretos, Brazil: Final results of a demonstrative study.
      ,
      • Jemal A.
      • Simard E.P.
      • Dorell C.
      • Noone A.-M.
      • Markowitz L.E.
      • Kohler B.
      • et al.
      Annual Report to the Nation on the Status of Cancer, 1975–2009, Featuring the Burden and Trends in Human Papillomavirus (HPV)-Associated Cancers and HPV Vaccination Coverage Levels.
      ,
      • Lin A.
      • Ong K.J.
      • Hobbelen P.
      • King E.
      • Mesher D.
      • Edmunds W.J.
      • et al.
      Impact and cost-effectiveness of selective human papillomavirus vaccination of men who have sex with men.
      ,
      • Novaes H.M.
      • de Soarez P.C.
      • Silva G.A.
      • Ayres A.
      • Itria A.
      • Rama C.H.
      • et al.
      Cost-effectiveness analysis of introducing universal human papillomavirus vaccination of girls aged 11 years into the National Immunization Program in Brazil.
      ,
      • Rimer B.K.
      • Harper H.
      • Witte O.N.
      ,
      • Smith K.
      • Bazini-Barakat N.
      A public health nursing practice model: Melding public health principles with the nursing process.
      ,
      • White J.
      • Sukamal D.
      Annual HPV vaccine coverage in England in 2010/11: Human papillomavirus (HPV) vaccine coverage monitoring programme 2010/2011.
      ). Realized benefits can be obtained, even in settings showing some implementation heterogeneity. For example, Australian school-based programs in some states show differences in HPV vaccination policies that are more locally driven by legislative and public health system differences (
      • Jemal A.
      • Simard E.P.
      • Dorell C.
      • Noone A.-M.
      • Markowitz L.E.
      • Kohler B.
      • et al.
      Annual Report to the Nation on the Status of Cancer, 1975–2009, Featuring the Burden and Trends in Human Papillomavirus (HPV)-Associated Cancers and HPV Vaccination Coverage Levels.
      ). Some U.S. data for influenza vaccination suggest collaborations between public schools and local health departments can result in successful vaccination campaigns (
      • Klaiman T.
      • O'Connell K.
      • Stoto M.A.
      Learning from successful school-based vaccination clinics during 2009 pH1N1.
      ). Simply said, it may be equally important to develop overall goals for large groups (e.g., nations) that promote some variations across communities. For example, Australia has strongly supported states and territories in purchasing vaccines for school-based programs and vaccine delivery (
      • Jemal A.
      • Simard E.P.
      • Dorell C.
      • Noone A.-M.
      • Markowitz L.E.
      • Kohler B.
      • et al.
      Annual Report to the Nation on the Status of Cancer, 1975–2009, Featuring the Burden and Trends in Human Papillomavirus (HPV)-Associated Cancers and HPV Vaccination Coverage Levels.
      ). The United Kingdom supported a rigorous school-based vaccine delivery program to enhance access for underrepresented groups (
      • Batista Ferrer H.
      • Trotter C.L.
      • Hickman M.
      • Audrey S.
      Barriers and facilitators to uptake of the school-based HPV vaccination programme in an ethnically diverse group of young women.
      ). In Brazil, 97% of children completed three doses of HPV vaccine through focused school-based vaccination programs (
      • Fregnani J.H.
      • Carvalho A.L.
      • Eluf-Neto J.
      • Ribeiro Kde C.
      • Kuil Lde M.
      • da Silva T.A.
      • et al.
      A school-based human papillomavirus vaccination program in Barretos, Brazil: Final results of a demonstrative study.
      ). Overall, school-based vaccine programs improve vaccine coverage and lower family burden for access for HPV and other vaccines.

      The Academy's Position

      The American Academy of Nursing has long supported the use of vaccines to reduce the incidence of disease, particularly for vulnerable populations. The Academy supports the acceleration of HPV Vaccine Uptake in U.S. communities, consistent with recommendations by the 2012 to 2013 President's Cancer Panel recommendations and Healthy People 2020 goals (IID-11.4, 11.5) (

      Healthy People 2020. Immunization and Infectious Diseases: IID-11 Increase routine vaccination coverage levels for adolescents. In U.S. Department of Health and Human Services Office of Disease Prevention and Health Promotion. Washington, DC.

      ,
      • Rimer B.K.
      • Harper H.
      • Witte O.N.
      ).
      The American Academy of Nursing supports the clearest, most concise, and easy-to-follow recommendations be crafted by health-care and communication experts to guide messaging to professionals and the public. These communications should employ a variety of media for dissemination (
      • Smith K.
      • Bazini-Barakat N.
      A public health nursing practice model: Melding public health principles with the nursing process.
      ). Additionally, the Academy supports ongoing evaluation of programmatic approaches to guiding vaccination programs (
      • Smith K.
      • Bazini-Barakat N.
      A public health nursing practice model: Melding public health principles with the nursing process.
      ).
      The American Academy of Nursing supports efforts to increase HPV vaccination completion rates in 9- to 26-year-olds to decrease HPV-related morbidity among young and middle-age adults, and cancer-related mortality among middle-age and older male and female adults.
      The Academy will collaborate with other nursing organizations, the CDC, including ACIP, FDA, HHS, National Cancer Institute, National Institute of Allergy and Infectious Diseases, the President's Cancer Panel, National Institute for Nursing Research, as well as other clinician and consumer organizations, to support a more robust and workable HPV prevention strategy.

      Recommendations

      Health-care providers at every level should increase opportunities to initiate HPV vaccination in the clinical setting and the community. For example, physicians, nurse practitioners, and physician's assistants should be encouraged to introduce standing order policies for HPV vaccination.
      Pharmaceutical professional organizations should create portals for safe and effective vaccine delivery in community-based pharmacies.
      The HHS, in partnership with the National Association of School Nurses, and pharmaceutical professional organizations should develop new strategies for consistent and flexible delivery of vaccines for children in schools through new and novel approaches. HHS should support state funded block grants that allow the U.S. Department of Education to distribute to community schools. Additionally, HHS should encourage partnerships with private sector pharmaceutical businesses to bring vaccine programs into schools.
      The HHS, CDC, state Departments of Public Health, and professional societies should collaborate to enhance and promote adherence to vaccination reporting systems that link all clinic- and community-based vaccination administration sites to electronic medical records and centralized records to promote proper administration.
      The U.S. Congress and the Center for Medicare and Medicaid Services should establish national standards for vaccine reimbursement, including administration fees, for administration of HPV vaccinations both in and out of existing health-care coverage networks.
      The HHS, CDC, state Departments of Public Health, and professional societies should develop linguistically appropriate, culturally competent, and accurate vaccination messaging geared toward social media dissemination that is aimed at increasing acceptability of HPV vaccines by parents, youth, and other community members.
      The HHS, CDC, National Institutes of Health, state and local Departments of Public Health, and professional societies should develop, trial, and implement evidence-based community and systems level population-based interventions that increase adherence to HPV vaccination recommendations and improve acceptability in American communities.

      Acknowledgments

      Academy Expert Panels: Emerging Infectious Diseases Expert Panel (Kaye Bender); Women's Health Expert Panel (Diana Taylor; Versie Johnson-Mallard); Primary Care Expert Panel (Patricia Vanhook); Child, Adolescent and Family Expert Panel (Cindy Greenberg; Judith Vessey); Health Behavior Expert Panel (Marjorie McCullagh); and Bioethics Expert Panel (Lucia Wocial).

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