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Voluntary School-Based Human Papillomavirus Vaccination: An Efficient and Acceptable Model for Achieving High Vaccine Coverage in Adolescents

      See Related Articles pp. 237, 242, 249, and 305
      Recently published data from large efficacy studies suggest that human papillomavirus (HPV) vaccines can substantially reduce anogenital neoplasia and warts overall when administered to young women with no previous exposure to most high- and low-risk HPV types [
      • Muñoz N.
      • Kjaer S.K.
      • Sigurdsson K.
      • et al.
      Impact of human papillomavirus (HPV)-6/11/16/18 vaccine on All HPV-associated genital diseases in young women.
      ,
      • Paavonen J.
      • Naud P.
      • Salmerón J.
      • et al.
      Efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types (PATRICIA): Final analysis of a double-blind, randomised study in young women.
      ]. These data refer to young women who were naïve to HPV and therefore considered similar to female adolescents before their sexual debut. Most countries have centered HPV vaccination recommendations on this particular age group.
      Mathematical models predict that vaccination of young adolescent females will dramatically reduce HPV infection and associated disease in the population offered vaccination [
      • Garnett G.P.
      Role of herd immunity in determining the effect of vaccines against sexually transmitted disease.
      ,
      • Hughes J.P.
      • Garnett G.P.
      • Koutsky L.
      The theoretical population-level impact of a prophylactic human papilloma virus vaccine.
      ,
      • Taira A.V.
      • Neukermans C.P.
      • Sanders G.D.
      Evaluating human papillomavirus vaccination programs.
      ], and that this is a cost-effective intervention [
      • Goldie S.J.
      • Kohli M.
      • Grima D.
      • et al.
      Projected clinical benefits and cost-effectiveness of a human papillomavirus 16/18 vaccine.
      ]. These studies have generally assumed vaccination uptake to be in the range consistent with previously published data on uptake for adolescent vaccinations offered through school vaccination programs or programs with mandated vaccination for school entry (70%–80%), and have further assumed that lower levels of uptake predict a lesser effect on infection and disease [
      • Smith M.A.
      • Canfell K.
      • Brotherton J.M.L.
      • et al.
      The predicted impact of vaccination on human papillomavirus infections in Australia.
      ]. As several countries have now implemented HPV vaccination programs, the first data on coverage are beginning to emerge. It is concerning, but also intriguing, that there is such a vast range in HPV vaccine coverage across these countries, from very high to very low [
      • Brabin L.
      • Roberts S.A.
      • Stretch R.
      • et al.
      Uptake of first two doses of human papillomavirus vaccine by adolescent schoolgirls in Manchester: Prospective cohort study.
      ,
      • Brotherton J.M.L.
      • Deeks S.L.
      • Campbell-Lloyd S.
      • et al.
      Interim estimates of human papillomavirus vaccination coverage in the school-based program in Australia.
      ,
      • Jain N.
      • Euler G.L.
      • Shefer A.
      • et al.
      Human papillomavirus (HPV) awareness and vaccination initiation among women in the United States, National Immunization Survey—Adult 2007.
      ,
      • Rouzier R.
      • Giordanella J.-P.
      Coverage and compliance of human papillomavirus vaccines in Paris: Demonstration of low compliance with non-school-based approaches.
      ,

      Rosenthal SL, Weiss TW, Zimet GD, et al. Predictors of HPV vaccine uptake among women aged 19–26: Importance of a physician’s recommendation. Vaccine (in press).

      ,

      Wong C, Berkowitz Z, Dorell C, et al. National HPV vaccine uptake among girls 9-17 years old—National Health Interview Survey, United States, 2008. Conference abstract 10768 in “Children’s Health: Climbing to new Heights;” October 2–5, 2010; San Francisco, CA. Available at: http://aap.confex.com/aap/2010/webprogram/Paper10768.html.

      ].
      In this issue of the Journal of Adolescent Health, four articles report on HPV vaccine uptake in female adolescents and explore issues that potentially affect vaccination consent and completion. Rouzier and Giordanella presented HPV vaccine coverage for female adolescents in Paris, France, 1 year after the French government recommended that adolescents be vaccinated (through medical providers) [
      • Rouzier R.
      • Giordanella J.-P.
      Coverage and compliance of human papillomavirus vaccines in Paris: Demonstration of low compliance with non-school-based approaches.
      ]. The reported uptake of 17% (with less than half of these adolescents receiving all three doses) is similar to the low level of uptake (25% for one dose; 11% for all three) previously reported in the United States [

      Wong C, Berkowitz Z, Dorell C, et al. National HPV vaccine uptake among girls 9-17 years old—National Health Interview Survey, United States, 2008. Conference abstract 10768 in “Children’s Health: Climbing to new Heights;” October 2–5, 2010; San Francisco, CA. Available at: http://aap.confex.com/aap/2010/webprogram/Paper10768.html.

      ]. Low vaccination rates were found to have no overall effect on abnormalities detected by the Pap test in a clinic sample from the United States [
      • Gross M.S.
      • Andres R.
      • Soren K.
      Human papillomavirus (HPV) vaccination and pap smear results in adolescent girls—Have we seen a difference?.
      ], whereas in Australia, where uptake is much higher, a reduction in high grade Pap abnormalities among young women was evidenced in the data collected by a state cytology registry [

      Brotherton JML, Fridman M, Saville M, Gertig D. First indication of a possible impact on cervical abnormalities following a national HPV vaccination program, in Victoria, Australia. Conference abstract in “HPV 2010;” July 2–8, 2010; Montreal, Canada. Available at: http://hpv2010.org/main/index.php?option=com_conference&view=presentation&id=1746&conference=1&Itemid=103.

      ]. Rouzier and Giordanella correctly conclude that national policies for HPV vaccination that do not either promote, enforce, or support HPV vaccination recommendations will have suboptimal levels of uptake.
      There are two evidence-based approaches to high vaccine uptake of adolescents at the population level: (1) “strict” school-linked mandates (where attendance in school is contingent on demonstration of a vaccination certificate for mandated vaccines, and exemption is allowed only in certain circumstances), and (2) voluntary on-site school-based mass vaccination. School-related mandates have been successful in achieving high rates of adolescent vaccination in the United States [
      • Orenstein W.A.
      • Hinman A.R.
      The immunization system in the United States—The role of school immunization laws.
      ]. Voluntary school-based vaccination programs have been successful in achieving high rates of adolescent vaccination against hepatitis B in Australia, Canada, and Italy, among other European countries [
      • Skinner S.R.
      • Imberger A.
      • Nolan T.
      • Lester R.
      • Glover S.
      • Bowes G.
      Randomised controlled trial of an educational strategy to increase school-based adolescent hepatitis B vaccination.
      ,
      • Dobson S.
      • Scheifele D.
      • Bell A.
      Assessment of a universal school-based hepatitis B vaccination program.
      ,
      • Stroffolini T.
      • Cialdea L.
      • Tosti M.
      • et al.
      Vaccination campaign against hepatitis B for 12 year old subjects in Italy.
      ], and more recently for HPV vaccination in the United Kingdom, Australia, and Canada [
      • Brabin L.
      • Roberts S.A.
      • Stretch R.
      • et al.
      Uptake of first two doses of human papillomavirus vaccine by adolescent schoolgirls in Manchester: Prospective cohort study.
      ,

      Brotherton JML, Fridman M, Saville M, Gertig D. First indication of a possible impact on cervical abnormalities following a national HPV vaccination program, in Victoria, Australia. Conference abstract in “HPV 2010;” July 2–8, 2010; Montreal, Canada. Available at: http://hpv2010.org/main/index.php?option=com_conference&view=presentation&id=1746&conference=1&Itemid=103.

      ,
      • Ogilvie G.
      • Anderson M.
      • Marra F.
      • et al.
      A population-based evaluation of a publicly funded, school-based HPV vaccine program in British Columbia, Canada: Parental factors associated with HPV vaccine receipt.
      ]. Voluntary school-based mass vaccination approaches have also been used in specific initiatives in the United States with some success [
      • Carpenter L.
      • Lott J.
      • Lawson B.
      • et al.
      Mass distribution of free, intranasally administered influenza vaccine in a public school system.
      ,
      • Goldstein S.
      • Cassidy W.
      • Hodgson W.
      • Mahoney F.
      Factors associated with student participation in a school-based hepatitis B immunization program.
      ,
      • Unti L.
      • Coyle K.
      • Woodruff B.
      • Boyer-Chuanroong L.
      Incentives and motivators in school-based hepatitis B vaccination programs.
      ,
      • Woodruff B.
      • Unti L.
      • Coyle K.
      • Boyer-Chuanroong L.
      Parents’ attitudes toward school-based hepatitis B vaccination of their children.
      ].
      In this issue of the Journal of Adolescent Health, Dempsey and Mendez model the effect of HPV vaccination on disease outcomes in the United States within the setting of a strict mandate for adolescent HPV vaccination compared with a situation where there is no mandate [
      • Dempsey A.F.
      • Mendez D.
      Examining future adolescent HPV vaccine uptake with and without a school mandate.
      ]. They conclude that strict mandates, which are associated with a much higher uptake of vaccine, will result in a more rapid and increased reduction in disease. However, strict mandates for HPV vaccination have been vehemently debated in the United States [
      • Udesky L.
      Push to mandate HPV vaccine triggers backlash in USA.
      ,
      • Haber G.
      • Marlow R.M.
      • Zimet G.D.
      The HPV vaccine mandate controversy.
      ]. Among several controversies, perhaps most challenging is the fact that genital HPV is exclusively sexually transmitted; therefore, infected individuals do not pose an immediate risk to others in the school setting. For hepatitis B, the rare possibility of transmission through blood as a result of accidents on school grounds counters this same concern.
      In the United States, most states have enacted legislation mandating vaccination of adolescents for vaccines recommended by the Advisory Committee on Immunization Practices (ACIP), with the exception of HPV [

      Immunize.org website. Available at: http://www.immunize.org/laws/. Viewed June 21, 2010.

      ]. For hepatitis B vaccination, 40 states have enacted legislation, or are in the progress of doing so, related to school entry mandates. The national level of coverage is now about 90% [

      Immunize.org website. Available at: http://www.immunize.org/laws/. Viewed June 21, 2010.

      ,
      • Stokley S.
      • Dorell C.
      • Yankey D.
      Centers for Disease Control. National, state, and local area vaccination coverage among adolescents aged 13–17 years—United States, 2008.
      ].
      To date, enactment of strict school-linked mandates for HPV vaccination has experienced significant opposition in most states where it has been proposed. According to the National Conference of State Legislatures’ website, at least 41 states, as well as the District of Columbia, have introduced legislation related to HPV vaccination. However, till recently only under half of those states have enacted legislation. Currently, “as of February 2010, 17 states have proposed HPV related legislation or resolutions in 2009–2010” []. Few proposals include strong mandates for HPV vaccination; the majority of them are concerned with either funding the vaccine or a requirement that information be provided to parents [].
      In this issue, Cates et al and Middleman and Tung also provide insight into parental perspectives of HPV vaccine issues [
      • Cates J.R.
      • Shafer A.
      • Carpentier F.D.
      • et al.
      How parents hear about human papillomavirus vaccine: Implications for uptake.
      ,
      • Middleman A.B.
      • Tung J.S.
      Urban middle school parent perspectives: The vaccines they are willing to have their children receive using school-based immunization programs.
      ]. Cates et al found that only 9% of parents recalled receiving information about HPV vaccine through school, even though the study was undertaken in North Carolina, where a mandate requires that schools provide information on HPV vaccine to parents of adolescents. Although this finding is disappointing, it is perhaps not surprising, as there are many steps involved in providing effective information to parents.
      “Less strict” vaccination mandates include those from which parents can opt out without specified explanation, and those which only require that information about the vaccine be provided to the parents. Such less strict mandates may not have the effect on coverage that stricter mandates have demonstrated [
      • Averhoff F.
      • Linton L.
      • Peddecord K.M.
      • et al.
      A middle school immunization law rapidly and substantially increases immunization coverage among adolescents.
      ,
      • Jacobs R.J.
      • Meyerhoff A.S.
      Effect of middle school entry requirements on hepatitis B vaccination coverage.
      ] and they may not be able to affect racial and ethnic disparities in vaccination completion [
      • Morita J.Y.
      • Ramirez E.
      • Trick W.E.
      Effect of a school-entry vaccination requirement on racial and ethnic disparities in hepatitis B immunization coverage levels among public school students.
      ]. These mandates remove the motivation required by parents to overcome the following barriers that exist in accessing a particular vaccine for their adolescent through a clinic delivery model. First, information to help parents (and adolescents) decide on vaccination must reach them and must be of a quality that it will motivate; and second, parents and adolescents need to attend a medical clinic on three separate occasions. This last point is a particular challenge because adolescents have low physician attendance compared with other age groups [
      • Rand C.M.
      • Szilagyi P.G.
      • Albertin C.
      • et al.
      Additional health care visits needed among adolescents for human papillomavirus vaccine delivery within medical homes: A national study.
      ]. The importance of a physician’s recommendation to vaccinate [
      • Brewer N.T.
      • Fazekas K.I.
      Predictors of HPV vaccine acceptability: A theory-informed, systematic review.
      ] will only apply for those adolescents who actually visit the physician. Finally, there may be out-of-pocket expenses for some of the adolescents, and the need to complete health insurance claim forms. Barriers to adolescent HPV vaccination are significant in the United States [
      • Dempsey A.F.
      • Davis M.M.
      Overcoming barriers to adherence to HPV vaccination recommendations.
      ].
      Voluntary school-based mass vaccination programs have been demonstrated to achieve high population coverage, most likely because it removes several obstacles to vaccination. The argument for school-based vaccination is a compelling one, but it is not without challenges.
      Middleman and Tung measured parental attitudes toward adolescent vaccinations being provided in schools in Texas [
      • Middleman A.B.
      • Tung J.S.
      Urban middle school parent perspectives: The vaccines they are willing to have their children receive using school-based immunization programs.
      ]. Although levels of enthusiasm were not high overall, the parents who had experienced school-based vaccination were more likely to be supportive of the approach. The Australian experience of school-based HPV vaccination has documented several strengths and some limitations [

      Cooper Robbins SC, Bernard D, McCaffery K, Skinner SR. “It’s a logistical nightmare!”: Recommendations for optimizing HPV school-based vaccination experiences. Sex Health (in press).

      ,
      • Watson M.
      • Shaw D.
      • Molchanoff L.
      • et al.
      Challenges, lessons learned, and results following the implementation of a human papillomavirus school vaccination program in South Australia.
      ]. However, most stakeholders, including school personnel, immunization nurses, public health professionals, adolescents, and parents, have reported satisfaction with the program [

      Cooper Robbins SC, Bernard D, McCaffery K, Skinner SR. “It’s a logistical nightmare!”: Recommendations for optimizing HPV school-based vaccination experiences. Sex Health (in press).

      ]. Identified points of satisfaction included the convenience of school-based vaccination and peer support at the time of vaccination [

      Cooper Robbins SC, Bernard D, McCaffery K, Skinner SR. “It’s a logistical nightmare!”: Recommendations for optimizing HPV school-based vaccination experiences. Sex Health (in press).

      ].
      The process of obtaining properly filled consent forms signed by the parents is one of the major challenges to school-based programs [
      • Guajardo A.
      • Middleman A.
      • Sansaricq K.
      School nurses identify barriers and solutions to implementing a school-based hepatitis B immunization program.
      ,
      • Stewart P.
      • MacDonald N.
      • Manion I.
      School-based hepatitis B immunization program: Follow-up of non-participants at first school clinic.
      ]. This process can be undertaken in different ways. For example, in the United Kingdom HPV vaccination program, consent forms are mailed home to parents, whereas in Australia, students are given consent forms to take home [
      • Brabin L.
      • Roberts S.A.
      • Stretch R.
      • et al.
      Uptake of first two doses of human papillomavirus vaccine by adolescent schoolgirls in Manchester: Prospective cohort study.
      ,

      Cooper Robbins SC, Bernard D, McCaffery K, Skinner SR. “It’s a logistical nightmare!”: Recommendations for optimizing HPV school-based vaccination experiences. Sex Health (in press).

      ]. The degree to which an adolescent’s role is recognized in the consent process also varies as follows: in the United Kingdom, an adolescent’s decision is accepted when a parent’s consent is absent only if the nurse vaccinating feels that the adolescent is competent to make that decision [

      NHS Immunisation Website. Available at: www.immunisation.nhs.uk/files/DH_HPV_consent_Mar08.pdf. 2008. Viewed June 30, 2010.

      ]. In Australia, written parental consent must be obtained before a student can be vaccinated at school, regardless of the student’s age or mental capacity [

      NSW DET Website. Available at: http://www.schools.nsw.edu.au/gotoschool/a-z/immunisation.php. Viewed June 16, 2010.

      ]. However, when a parent does not provide consent, a mature minor can theoretically access vaccination in a clinic setting, although they will face the barriers mentioned previously.
      Data also support appropriate education of teachers, parents, and adolescents about the process of vaccination in a school-based vaccination program [
      • Skinner S.R.
      • Imberger A.
      • Nolan T.
      • Lester R.
      • Glover S.
      • Bowes G.
      Randomised controlled trial of an educational strategy to increase school-based adolescent hepatitis B vaccination.
      ]. Other factors used in school-based vaccination programs, but less systematically studied, include incentives [
      • Unti L.
      • Coyle K.
      • Woodruff B.
      • Boyer-Chuanroong L.
      Incentives and motivators in school-based hepatitis B vaccination programs.
      ] and the effect on uptake of delivering more than one vaccination at a time [
      • Rivest P.
      • Grenier L.
      • Lonergan G.
      • Bedard L.
      Varicella vaccination for grades 4 and 5 students—From theory to practice.
      ].
      We believe that the most acceptable way to achieve high uptake of HPV vaccine is to offer voluntary school-based vaccination, provided that it is supported by effective consent processes, training, and best practice guidelines for the individuals providing the vaccination in the schools, and education for parents, adolescents, and teachers [

      Cooper Robbins SC, Bernard D, McCaffery K, Skinner SR. “It’s a logistical nightmare!”: Recommendations for optimizing HPV school-based vaccination experiences. Sex Health (in press).

      ]. The articles in this issue focus on immunization of female adolescents, but the same issues may apply to male adolescents, now that there is a permissive recommendation [
      • Centers for Disease Control
      FDA licensure of quadrivalent human papillomavirus vaccine (HPV4, Gardasil) for use in males and guidance from the Advisory Committee on Immunization Practices (ACIP).
      ] to immunize them. School delivery of vaccination may be more feasible in the context of offering the vaccine to all students, especially with new data suggesting that older male adolescents’ health care use is exceptionally low [
      • Dempsey A.F.
      • Freed G.L.
      Health care utilization by adolescents on Medicaid: Implications for delivering vaccines.
      ].
      There may be a perception that school-based vaccination is the more expensive option, but savings are likely through the large volume of individuals who are vaccinated en mass in a nonclinical setting. Moreover, this approach allows for more than one vaccine to be given at a time. Logistically, school-based vaccination also requires a federal funding arrangement, which allows for a vaccine to be provided free of charge to all.
      In cases where mandated HPV vaccination for adolescents is not achievable, then the United States and indeed other countries must consider school-based HPV vaccination programs. This initiative may fit within the scope of the nation’s reformed healthcare. Advocates of adolescent health, and the health of future generations of women in the United States, should seize this opportunity to put in place an effective strategy to significantly affect the scourge of HPV-related disease.

      Acknowledgments

      The authors thank Susan Rosenthal for her several critical readings of the editorial, and for offering valuable suggestions.
      Conflicts of interest: S.R.S. has received research and travel support to attend conferences to present data from G.S.K. Australia and C.S.L. Ltd has honoraria from G.S.K. Australia and C.S.L. Ltd for time on advisory boards and educational seminars, and is principal investigator on clinical trials of the HPV vaccine Cervarix, sponsored by G.S.K . S.C.C.R. is the recipient of travel grants from CSL Limited Australia .

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