Advertisement

Systematic Review and Meta-Analysis of Interventions to Improve Access and Coverage of Adolescent Immunizations

      Abstract

      Vaccination strategies are among the most successful and cost-effective public health strategies for preventing disease and death. Until recently, most of the existing immunization programs targeted infants and children younger than 5 years which have successfully resulted in reducing global infant and child mortality. Adolescent immunization has been relatively neglected, leaving a quarter of world's population underimmunized and hence vulnerable to a number of preventable diseases. In recent years, a large number of programs have been launched to increase the uptake of different vaccines in adolescents; however, the recommended vaccination coverage among the adolescent population overall remains very low, especially in low- and middle-income countries. Adolescent vaccination has received significantly more attention since the advent of the human papillomavirus (HPV) vaccine in 2006. However, only half of the adolescent girls in the United States received a single dose of HPV vaccine while merely 43% and 33% received two and three doses, respectively. We systematically reviewed literature published up to December 2014 and included 23 studies on the effectiveness of interventions to improve immunization coverage among adolescents. Moderate-quality evidence suggested an overall increase in vaccination coverage by 78% (relative risk: 1.78; 95% confidence interval: 1.41–2.23). Review findings suggest that interventions including implementing vaccination requirement in school, sending reminders, and national permissive recommendation for adolescent vaccination have the potential to improve immunization uptake. Strategies to improve coverage for HPV vaccines resulted in a significant decrease in the prevalence of HPV by 44% and genital warts by 33%; however, the quality of evidence was low. Analysis from single studies with low- or very low–quality evidence suggested significant decrease in varicella deaths, measles incidence, rubella susceptibility, and incidence of pertussis while the impact was nonsignificant for incidence of mumps with their respective vaccines. Further rigorous evidence is needed to evaluate the effectiveness of strategies to improve immunization uptake among adolescents from low- and middle-income countries.

      Keywords

      Vaccination programs are among the most successful and cost-effective public health strategies for preventing infections. Until recently, most of the existing immunization programs targeted infants and children younger than 5 years which have successfully resulted in reducing global infant and child mortality [

      National Foundation for Infectious Diseases: Adolescent vaccination bridging from a strong childhood foundation to a healthy adulthood: A report on strategies to increase adolescent immunization rates. Available at: http://www2.aap.org/immunization/pediatricians/pdf/ImmunizationofAdolescents_nfid.pdf. Accessed November 16, 2015.

      ]. As a result, adolescent immunization has been overshadowed, leaving a quarter of world's population vulnerable to a number of preventable diseases. Estimates suggest that around 35 million American adolescents fail to receive at least one recommended vaccine [
      National Foundation of Infectious Diseases
      Adolescent vaccination: Bridging from a strong childhood foundation to a healthy adulthood.
      ]. In 2012, only half of the adolescent girls in the United States received a single dose of human papillomavirus (HPV) vaccine while merely 43% and 33% received two and three doses, respectively [
      Human papillomavirus vaccination coverage among adolescent girls, 2007–2012, and postlicensure vaccine safety monitoring, 2006–2013—United States.
      ]. Missed vaccination opportunities for adolescent vaccination against tetanus, diphtheria, pertussis (TDaP), tetravalent meningococcal conjugate vaccine, and HPV are also common in the United States since adolescents are less likely to utilize preventive care [
      • Wong C.A.
      • Taylor J.A.
      • Wright J.A.
      • et al.
      Missed opportunities for adolescent vaccination, 2006-2011.
      ].
      Infectious and vaccine-preventable diseases disproportionately affect the low- and middle-income countries (LMICs) and disadvantaged populations in high-income countries (HICs). There were an estimated 266,000 deaths from cervical cancer worldwide in 2012, accounting for 7.5% of all female cancer deaths, of which nearly 85% occurred in developing countries [
      World Health Organization
      Globocan 2012: Estimated cancer incidence, mortality and prevalence worldwide.
      ]. The worldwide prevalence of infection with HPV in women without cervical abnormalities is 11%–12% with higher rates in Sub-Saharan Africa (24%), Eastern Europe (21%), and Latin America (16%) [
      • Forman D.
      • de Martel C.
      • Lacey C.J.
      • et al.
      Global burden of human papillomavirus and related diseases.
      ]. The proportion of invasive cervical cancer cases is higher in the LMICs with a relatively higher mortality/incidence ratio compared to the HICs [
      WHO/ICO Information center on HPV and Cervical Cancer
      Human papilomavirus and related cancers in Ethiopia.
      ,
      • Fitzmaurice C.
      • Dicker D.
      • Pain A.
      • et al.
      The global burden of cancer 2013.
      ]. In U.S. settings, African-American girls were less likely to have either initiated or completed the three-dose HPV vaccination series [
      • Kessels S.J.M.
      • Marshall H.S.
      • Watson M.
      • et al.
      Factors associated with HPV vaccine uptake in teenage girls: A systematic review.
      ]. This warrants an additional focus on adolescents from LMICs and underprivileged populations in HICs as they also deserve a healthy transition into adulthood.
      The recommended immunization during adolescence by the World Health Organization includes three doses of hepatitis B (for high-risk groups if not previously immunized), Td booster, one dose of rubella (adolescent girls and/or childbearing-aged women if not previously vaccinated), and two doses of HPV for females (9–14 years) and three doses for those aged 15 years and above [
      World Health Organization
      WHO recommendations for routine immunization—Summary tables.
      ]. Low immunization rates in adolescents have a wide array of implications: outbreaks of vaccine-preventable diseases, negative effects on quality of life, and increased disease associated costs. Importantly, low immunization rates establish reservoirs of disease in adolescents that can affect others, including high-risk infants, elderly persons, and persons with underlying medical conditions.
      Adolescent vaccination is a growing topic that has received significantly more attention since the advent of the HPV vaccine in 2006. In recent years, large number of programs have been launched to increase the uptake of different vaccines in adolescent populations; however, the recommended vaccination coverage among adolescents still remains low. These changes reflect an increased emphasis on the importance of adolescent immunization, but by themselves they will not sufficiently increase awareness or immunization rates [

      National Foundation for Infectious Diseases: Adolescent vaccination bridging from a strong childhood foundation to a healthy adulthood: A report on strategies to increase adolescent immunization rates. Available at: http://www2.aap.org/immunization/pediatricians/pdf/ImmunizationofAdolescents_nfid.pdf. Accessed November 16, 2015.

      ]. The American Academy of Pediatrics suggests implementing one or more of the strategies including reminder calls, prompts or standing orders, strong provider recommendation, including all recommended vaccination at every visit, provider feedback, educating patients and their parents, addressing costs, and setting up vaccination clinics to increase immunization coverage in adolescents [
      American Academy of Pediatrics Immunization Resources
      Adolescent immunizations: Strategies for increasing coverage rates.
      ].
      This article is part of a series of reviews conducted to evaluate the effectiveness of potential interventions for adolescent health and well-being. Detailed framework, methodology, and other potential interventions have been discussed in separate articles [
      • Salam R.A.
      • Faqqah A.
      • Sajjad N.
      • et al.
      Improving adolescent sexual and reproductive health: A systematic review of potential interventions.
      ,
      • Salam R.A.
      • Hooda M.
      • Das J.K.
      • et al.
      Interventions to improve adolescent nutrition: A systematic review and meta-analysis.
      ,
      • Das J.K.
      • Salam R.A.
      • Arshad A.
      • et al.
      Interventions for adolescent substance abuse: An overview of systematic reviews.
      ,
      • Das J.K.
      • Salam R.A.
      • Lassi Z.S.
      • et al.
      Interventions for adolescent mental health: an overview of systematic reviews.
      ,
      • Salam R.A.
      • Arshad A.
      • Das J.K.
      • et al.
      Interventions to prevent unintentional injuries among adolescents: A systematic review and meta-analysis.
      ,
      • Salam R.A.
      • Das J.K.
      • Lassi Z.S.
      • Bhutta Z.A.
      Adolescent health interventions: Conclusions, evidence gaps, and research priorities.
      ,
      • Salam R.A.
      • Das J.K.
      • Lassi Z.S.
      • Bhutta Z.A.
      Adolescent health and well-being: Background and methodology for review of potential interventions.
      ]. In this article, we systematically reviewed published literature to ascertain the effectiveness of interventions to improve immunization coverage among adolescents.

      Methods

      We reviewed all literature published up to December 2014 to identify studies on interventions to improve vaccination coverage. We did not restrict our search to any time limits or geographical settings. For the purpose of this review, the adolescent population was defined as aged 11–19 years; however, since many studies targeted youth along with adolescents, exceptions were made to include studies targeting adolescents and youth. Based on the current recommended vaccines for adolescents [
      Centers for Disease Control and Prevention
      Vaccine recommendations of the ACIP.
      ], search was conducted to identify studies focusing on improving coverage for HPV; measles, mumps, rubella (MMR); TDaP; meningococcal conjugate vaccine; and varicella vaccines among adolescents and youth. Studies were excluded if they targeted age groups other than adolescents and youth or did not report segregated data for the age group of interest. Studies were excluded if the intervention was aimed at comparing the efficacy/effectiveness of different vaccine preparations, assessing changes in antibody titers in individual subjects, or comparing various modes of delivering vaccines without control or baseline data.
      Our priority was to select existing randomized controlled trials (RCTs), quasitrials, and before–after studies in which the intervention was directed toward the adolescent and youth and reported immunization coverage outcomes. Search strategy was developed using appropriate keywords, medical subject heading, and free text terms. The following principal sources of electronic reference libraries were searched to access the available data: The Cochrane Library, Medline, PubMed, Popline, LILACS, CINAHL, EMBASE, World Bank's JOLIS search engine, CAB Abstracts, British Library for Development Studies at IDS, the World Health Organization regional databases, Google, and Google Scholar. The titles and abstracts of all studies identified were screened independently by two reviewers for relevance and matched. Any disagreements on selection of studies between these two primary abstractors were resolved by the third reviewer. After retrieval of the full texts of all the studies that met the inclusion/exclusion criteria, data from each study were abstracted independently and in duplicate into a standardized form. Studies that met the inclusion criteria were selected and double data abstracted on a standardized abstraction sheet. Quality assessment of the included RCTs was done according to the Cochrane risk of bias assessment tool. We conducted a meta-analysis for individual studies using the software Review Manager, version 5.3 (Cochrane Collaboration, London, United Kingdom). Pooled statistics were reported as the relative risk (RR) for categorical variables and standard mean difference for continuous variables between the experimental and control groups with 95% confidence intervals (CIs). A grade of “high,” “moderate,” “low,” and “very low” was used for grading the overall evidence indicating the strength of an effect on specific health outcome according to the Grading of Recommendations Assessment, Development and Evaluation criteria [
      • Walker N.
      • Fischer-Walker C.
      • Bryce J.
      • et al.
      Standards for CHERG reviews of intervention effects on child survival.
      ].

      Results

      Figure 1 describes the search flow while characteristics of the included studies are detailed in Table 1. The search yielded 10,274 titles across all databases that were screened for the purpose of this review. Screening the relevant abstracts resulted in 51 full texts that were further screened after which 23 studies were included in this review [
      • Zhuo J.
      • Geng W.
      • Hoekstra E.J.
      • et al.
      Impact of supplementary immunization activities in measles-endemic areas: A case study from Guangxi, China.
      ,
      • Ogbuanu I.U.
      • Kutty P.K.
      • Hudson J.M.
      • et al.
      Impact of a third dose of measles-mumps-rubella vaccine on a mumps outbreak.
      ,
      • Nguyen H.Q.
      • Jumaan A.O.
      • Seward J.F.
      Decline in mortality due to varicella after implementation of varicella vaccination in the United States.
      ,
      • Quinn H.E.
      • McIntyre P.B.
      The impact of adolescent pertussis immunization, 2004-2009: Lessons from Australia.
      ,
      • Nelson D.B.
      • Layde M.M.
      • Chatton T.B.
      Rubella susceptibility in inner-city adolescents: The effect of a school immunization law.
      ,
      • Baandrup L.
      • Blomberg M.
      • Dehlendorff C.
      • et al.
      Significant decrease in the incidence of genital warts in young Danish women after implementation of a national human papillomavirus vaccination program.
      ,
      • Bauer H.M.
      • Wright G.
      • Chow J.
      Evidence of human papillomavirus vaccine effectiveness in reducing genital warts: An analysis of California public family planning administrative claims data, 2007-2010.
      ,
      • Markowitz L.E.
      • Hariri S.
      • Lin C.
      • et al.
      Reduction in human papillomavirus (HPV) prevalence among young women following HPV vaccine introduction in the United States, National Health and Nutrition Examination Surveys, 2003-2010.
      ,
      • Mesher D.
      • Soldan K.
      • Howell-Jones R.
      • et al.
      Reduction in HPV 16/18 prevalence in sexually active young women following the introduction of HPV immunisation in England.
      ,
      • Musto R.
      • Siever J.E.
      • Johnston J.C.
      • et al.
      Social equity in human papillomavirus vaccination: A natural experiment in Calgary Canada.
      ,
      • Read T.R.
      • Hocking J.S.
      • Chen M.Y.
      • et al.
      The near disappearance of genital warts in young women 4 years after commencing a national human papillomavirus (HPV) vaccination programme.
      ,
      • Reiter P.L.
      • Gilkey M.B.
      • Brewer N.T.
      HPV vaccination among adolescent males: Results from the National Immunization Survey-Teen.
      ,
      • Averhoff F.
      • Linton L.
      • Peddecord K.M.
      • et al.
      A middle school immunization law rapidly and substantially increases immunization coverage among adolescents.
      ,
      • Bugenske E.
      • Stokley S.
      • Kennedy A.
      • Dorell C.
      Middle school vaccination requirements and adolescent vaccination coverage.
      ,
      • Carlson J.A.
      • Lewis C.A.
      Effect of the immunization program in Ontario schools.
      ,
      • Fogarty K.J.
      • Massoudi M.S.
      • Gallo W.
      • et al.
      Vaccine coverage levels after implementation of a middle school vaccination requirement, Florida, 1997-2000.
      ,
      • Harper P.G.
      • Murray D.M.
      An organizational strategy to improve adolescent measles-mumps-rubella vaccination in a low socioeconomic population. A method to reduce missed opportunities.
      ,
      • Kempe A.
      • Barrow J.
      • Stokley S.
      • et al.
      Effectiveness and cost of immunization recall at school-based health centers.
      ,
      • Kharbanda E.O.
      • Stockwell M.S.
      • Colgrove J.
      • et al.
      Changes in Tdap and MCV4 vaccine coverage following enactment of a statewide requirement of Tdap vaccination for entry into sixth grade.
      ,
      • Moss J.L.
      • Reiter P.L.
      • Dayton A.
      • Brewer N.T.
      Increasing adolescent immunization by webinar: A brief provider intervention at federally qualified health centers.
      ,
      • Stockwell M.S.
      • Kharbanda E.O.
      • Martinez R.A.
      • et al.
      Text4Health: Impact of text message reminder-recalls for pediatric and adolescent immunizations.
      ,
      • Suh C.A.
      • Saville A.
      • Daley M.F.
      • et al.
      Effectiveness and net cost of reminder/recall for adolescent immunizations.
      ,
      • Szilagyi P.G.
      • Albertin C.
      • Humiston S.G.
      • et al.
      A randomized trial of the effect of centralized reminder/recall on immunizations and preventive care visits for adolescents.
      ], of which four were RCTs, three quasirandomized trials, and 16 before–after studies. Of the 23 included studies, seven [
      • Baandrup L.
      • Blomberg M.
      • Dehlendorff C.
      • et al.
      Significant decrease in the incidence of genital warts in young Danish women after implementation of a national human papillomavirus vaccination program.
      ,
      • Bauer H.M.
      • Wright G.
      • Chow J.
      Evidence of human papillomavirus vaccine effectiveness in reducing genital warts: An analysis of California public family planning administrative claims data, 2007-2010.
      ,
      • Markowitz L.E.
      • Hariri S.
      • Lin C.
      • et al.
      Reduction in human papillomavirus (HPV) prevalence among young women following HPV vaccine introduction in the United States, National Health and Nutrition Examination Surveys, 2003-2010.
      ,
      • Mesher D.
      • Soldan K.
      • Howell-Jones R.
      • et al.
      Reduction in HPV 16/18 prevalence in sexually active young women following the introduction of HPV immunisation in England.
      ,
      • Read T.R.
      • Hocking J.S.
      • Chen M.Y.
      • et al.
      The near disappearance of genital warts in young women 4 years after commencing a national human papillomavirus (HPV) vaccination programme.
      ,
      • Reiter P.L.
      • Gilkey M.B.
      • Brewer N.T.
      HPV vaccination among adolescent males: Results from the National Immunization Survey-Teen.
      ] focused on the HPV, 11 studies [
      • Averhoff F.
      • Linton L.
      • Peddecord K.M.
      • et al.
      A middle school immunization law rapidly and substantially increases immunization coverage among adolescents.
      ,
      • Bugenske E.
      • Stokley S.
      • Kennedy A.
      • Dorell C.
      Middle school vaccination requirements and adolescent vaccination coverage.
      ,
      • Carlson J.A.
      • Lewis C.A.
      Effect of the immunization program in Ontario schools.
      ,
      • Fogarty K.J.
      • Massoudi M.S.
      • Gallo W.
      • et al.
      Vaccine coverage levels after implementation of a middle school vaccination requirement, Florida, 1997-2000.
      ,
      • Harper P.G.
      • Murray D.M.
      An organizational strategy to improve adolescent measles-mumps-rubella vaccination in a low socioeconomic population. A method to reduce missed opportunities.
      ,
      • Kempe A.
      • Barrow J.
      • Stokley S.
      • et al.
      Effectiveness and cost of immunization recall at school-based health centers.
      ,
      • Kharbanda E.O.
      • Stockwell M.S.
      • Colgrove J.
      • et al.
      Changes in Tdap and MCV4 vaccine coverage following enactment of a statewide requirement of Tdap vaccination for entry into sixth grade.
      ,
      • Moss J.L.
      • Reiter P.L.
      • Dayton A.
      • Brewer N.T.
      Increasing adolescent immunization by webinar: A brief provider intervention at federally qualified health centers.
      ,
      • Stockwell M.S.
      • Kharbanda E.O.
      • Martinez R.A.
      • et al.
      Text4Health: Impact of text message reminder-recalls for pediatric and adolescent immunizations.
      ,
      • Suh C.A.
      • Saville A.
      • Daley M.F.
      • et al.
      Effectiveness and net cost of reminder/recall for adolescent immunizations.
      ,
      • Szilagyi P.G.
      • Albertin C.
      • Humiston S.G.
      • et al.
      A randomized trial of the effect of centralized reminder/recall on immunizations and preventive care visits for adolescents.
      ] implemented interventions to improve coverage of multiple vaccines recommended for adolescents while measles [
      • Zhuo J.
      • Geng W.
      • Hoekstra E.J.
      • et al.
      Impact of supplementary immunization activities in measles-endemic areas: A case study from Guangxi, China.
      ], MMR [
      • Ogbuanu I.U.
      • Kutty P.K.
      • Hudson J.M.
      • et al.
      Impact of a third dose of measles-mumps-rubella vaccine on a mumps outbreak.
      ], varicella [
      • Nguyen H.Q.
      • Jumaan A.O.
      • Seward J.F.
      Decline in mortality due to varicella after implementation of varicella vaccination in the United States.
      ], rubella [
      • Nelson D.B.
      • Layde M.M.
      • Chatton T.B.
      Rubella susceptibility in inner-city adolescents: The effect of a school immunization law.
      ], and TDaP [
      • Quinn H.E.
      • McIntyre P.B.
      The impact of adolescent pertussis immunization, 2004-2009: Lessons from Australia.
      ] vaccines were assessed in one study each. All the studies were conducted in HICs of the United States, Canada, Australia, Denmark, and England. Included studies mainly focused on evaluating the impact of licensing and mass provision of vaccines as a part of national-level vaccination program to increase provision and coverage of adolescent vaccination, availability of free vaccines, implementing vaccination requirement before entry into school, reminder letters, telephone calls, and training of clinic staff on adolescent vaccines and strategies to improve immunization rates. Target populations in all studies were adolescents aged 11–19 years except three studies in the HPV vaccine category that targeted adolescents and youth till the age of 24 years.
      Figure thumbnail gr1
      Figure 1Search flow diagram. MCV = meningococcal conjugate vaccine; VZV = varicella zoster vaccine.
      Table 1Characteristics of included studies
      StudyStudy designCountrySettingInterventionTarget populationControlOutcomes assessed
      Measles
       Zhuo et al.
      • Zhuo J.
      • Geng W.
      • Hoekstra E.J.
      • et al.
      Impact of supplementary immunization activities in measles-endemic areas: A case study from Guangxi, China.
      Before–afterChinaCommunitySupplementary immunization activitiesAll agesNo supplementary immunization activityIncidence of measles
      MMR
       Ogbuanu et al.
      • Ogbuanu I.U.
      • Kutty P.K.
      • Hudson J.M.
      • et al.
      Impact of a third dose of measles-mumps-rubella vaccine on a mumps outbreak.
      Before–afterUnited StatesSchoolSelective school-based immunization9–14 yearsNo interventionIncidence of mumps
      Varicella
       Nguyen et al.
      • Nguyen H.Q.
      • Jumaan A.O.
      • Seward J.F.
      Decline in mortality due to varicella after implementation of varicella vaccination in the United States.
      Before–afterUnited StatesNationwide vaccinationUniversal childhood varicella vaccination programAll ages (outcome assessed for 10–19 years)Before implementation of childhood varicella immunizationNumber of deaths caused by varicella infection
      TDaP
       Quinn and McIntyre
      • Quinn H.E.
      • McIntyre P.B.
      The impact of adolescent pertussis immunization, 2004-2009: Lessons from Australia.
      Before–afterAustraliaSchoolSchool-based delivery of TDaP12–19 yearsNonavailability of school-based immunizationIncidence of pertussis
      Rubella
       Nelson et al.
      • Nelson D.B.
      • Layde M.M.
      • Chatton T.B.
      Rubella susceptibility in inner-city adolescents: The effect of a school immunization law.
      Before–afterUnited StatesSchoolVaccination requirement in schoolGirls older than 10 yearsBefore the vaccination requirementRubella susceptibility
      HPV
       Baandrup et al.
      • Baandrup L.
      • Blomberg M.
      • Dehlendorff C.
      • et al.
      Significant decrease in the incidence of genital warts in young Danish women after implementation of a national human papillomavirus vaccination program.
      Before–afterDenmarkCountrywide provisionLicensing and mass provision of HPV as part of National HPV Program12–19 yearsAbsence of nationwide HPV availabilityIncidence of genital warts
       Bauer et al.
      • Bauer H.M.
      • Wright G.
      • Chow J.
      Evidence of human papillomavirus vaccine effectiveness in reducing genital warts: An analysis of California public family planning administrative claims data, 2007-2010.
      Before–afterUnited StatesCountrywide provisionIntroduction population-level administration of HPV vaccine<21 yearsNonavailability of population-level vaccinationIncidence of genital warts
       Markowitz et al.
      • Markowitz L.E.
      • Hariri S.
      • Lin C.
      • et al.
      Reduction in human papillomavirus (HPV) prevalence among young women following HPV vaccine introduction in the United States, National Health and Nutrition Examination Surveys, 2003-2010.
      Before–afterUnited StatesCountrywide provisionIntroduction of HPV vaccine into routine immunization schedule14- to 24-year-old femalesHPV vaccine not included in routine immunization schedulePrevalence of HPV
       Mesher et al.
      • Mesher D.
      • Soldan K.
      • Howell-Jones R.
      • et al.
      Reduction in HPV 16/18 prevalence in sexually active young women following the introduction of HPV immunisation in England.
      Before–afterEnglandCountrywide provisionIntroduction of National HPV Immunization Program16- to 24-year-old femalesNonavailability of population-level vaccinationPrevalence of HPV
       Musto et al.
      • Musto R.
      • Siever J.E.
      • Johnston J.C.
      • et al.
      Social equity in human papillomavirus vaccination: A natural experiment in Calgary Canada.
      QuasitrialCanadaSchool and communityWithin schools vaccination during Grades 1, 5, and 99- to 11- and 13- to 15-year-old femalesCommunity-based vaccine availability at local community clinics by appointmentVaccine uptake
       Read et al.
      • Read T.R.
      • Hocking J.S.
      • Chen M.Y.
      • et al.
      The near disappearance of genital warts in young women 4 years after commencing a national human papillomavirus (HPV) vaccination programme.
      Before–afterAustraliaClinicIntroduction of National HPV Vaccination Program12- to 18-year-old femalesHPV vaccine not included in national immunization scheduleIncidence of genital warts
       Reiter et al.
      • Reiter P.L.
      • Gilkey M.B.
      • Brewer N.T.
      HPV vaccination among adolescent males: Results from the National Immunization Survey-Teen.
      Before–afterUnited StatesNationwide recommendationNational permissive recommendation for HPV vaccine11- to 17-year-old malesNo recommendationVaccine initiation
      Multivaccine
       Averhoff et al.
      • Averhoff F.
      • Linton L.
      • Peddecord K.M.
      • et al.
      A middle school immunization law rapidly and substantially increases immunization coverage among adolescents.
      Before–afterUnited StatesSchoolVaccination requirement in schoolFifth- through eighth-grade studentsStudents not subject to the requirementVaccine coverage
       Bugenske et al.
      • Bugenske E.
      • Stokley S.
      • Kennedy A.
      • Dorell C.
      Middle school vaccination requirements and adolescent vaccination coverage.
      QuasitrialUnited StatesSchoolVaccination requirement in school13–17 yearsStudents not subject to the requirementVaccine coverage
       Carlson and Lewis
      • Carlson J.A.
      • Lewis C.A.
      Effect of the immunization program in Ontario schools.
      Before–afterCanadaSchoolVaccination requirement in schoolGrades 7–13Students not subject to the requirementVaccine coverage
       Fogarty et al.
      • Fogarty K.J.
      • Massoudi M.S.
      • Gallo W.
      • et al.
      Vaccine coverage levels after implementation of a middle school vaccination requirement, Florida, 1997-2000.
      Before–afterUnited StatesSchoolVaccination requirement in schoolSeventh-grade studentsNo controlVaccine coverage
       Harper and Murray
      • Harper P.G.
      • Murray D.M.
      An organizational strategy to improve adolescent measles-mumps-rubella vaccination in a low socioeconomic population. A method to reduce missed opportunities.
      QuasitrialUnited StatesClinicClinic staff recommended vaccine on every visit11–18 yearsNo recommendationVaccine coverage
       Kempe et al.
      • Kempe A.
      • Barrow J.
      • Stokley S.
      • et al.
      Effectiveness and cost of immunization recall at school-based health centers.
      RCTUnited StatesSchoolRecall reminders for vaccinationSixth-grade male studentsNo recommendationVaccine coverage
       Kharbanda et al.
      • Kharbanda E.O.
      • Stockwell M.S.
      • Colgrove J.
      • et al.
      Changes in Tdap and MCV4 vaccine coverage following enactment of a statewide requirement of Tdap vaccination for entry into sixth grade.
      Before–afterUnited StatesHospitalVaccination requirement in school11–14 yearsStudents not subject to the requirementVaccine coverage
       Moss et al.
      • Moss J.L.
      • Reiter P.L.
      • Dayton A.
      • Brewer N.T.
      Increasing adolescent immunization by webinar: A brief provider intervention at federally qualified health centers.
      Before–afterUnited StatesClinicClinic staff were invited to attend 1-hour one-on-one webinar on adolescent vaccines and strategies to improve immunization rates such as reviewing and flagging charts, decreasing missed opportunities, recalls, and establishing center guidelines for immunizations.12–17 yearsNo staff trainingVaccine coverage
       Stockwell et al.
      • Stockwell M.S.
      • Kharbanda E.O.
      • Martinez R.A.
      • et al.
      Text4Health: Impact of text message reminder-recalls for pediatric and adolescent immunizations.
      RCTUnited StatesCommunityText message reminders for vaccination12–18 yearsNo reminderVaccine coverage
       Suh et al.
      • Suh C.A.
      • Saville A.
      • Daley M.F.
      • et al.
      Effectiveness and net cost of reminder/recall for adolescent immunizations.
      RCTUnited StatesClinicReminders letters and calls for vaccination11–18 yearsNo reminderVaccine coverage
       Szilagyi et al.
      • Szilagyi P.G.
      • Albertin C.
      • Humiston S.G.
      • et al.
      A randomized trial of the effect of centralized reminder/recall on immunizations and preventive care visits for adolescents.
      RCTUnited StatesClinicMail letters and telephone reminders for vaccination11–17 yearsNo reminderVaccine coverage
      HPV = human papillomavirus; MMR = measles, mumps, rubella; RCT = randomized controlled trial; TDaP = tetanus, diphtheria, pertussis.
      Moderate-quality evidence from 13 studies suggested an overall increase in vaccination coverage by 78% (RR: 1.78; 95% CI: 1.41–2.23; Figure 2) [
      • Musto R.
      • Siever J.E.
      • Johnston J.C.
      • et al.
      Social equity in human papillomavirus vaccination: A natural experiment in Calgary Canada.
      ,
      • Averhoff F.
      • Linton L.
      • Peddecord K.M.
      • et al.
      A middle school immunization law rapidly and substantially increases immunization coverage among adolescents.
      ,
      • Bugenske E.
      • Stokley S.
      • Kennedy A.
      • Dorell C.
      Middle school vaccination requirements and adolescent vaccination coverage.
      ,
      • Carlson J.A.
      • Lewis C.A.
      Effect of the immunization program in Ontario schools.
      ,
      • Fogarty K.J.
      • Massoudi M.S.
      • Gallo W.
      • et al.
      Vaccine coverage levels after implementation of a middle school vaccination requirement, Florida, 1997-2000.
      ,
      • Harper P.G.
      • Murray D.M.
      An organizational strategy to improve adolescent measles-mumps-rubella vaccination in a low socioeconomic population. A method to reduce missed opportunities.
      ,
      • Kempe A.
      • Barrow J.
      • Stokley S.
      • et al.
      Effectiveness and cost of immunization recall at school-based health centers.
      ,
      • Kharbanda E.O.
      • Stockwell M.S.
      • Colgrove J.
      • et al.
      Changes in Tdap and MCV4 vaccine coverage following enactment of a statewide requirement of Tdap vaccination for entry into sixth grade.
      ,
      • Moss J.L.
      • Reiter P.L.
      • Dayton A.
      • Brewer N.T.
      Increasing adolescent immunization by webinar: A brief provider intervention at federally qualified health centers.
      ,
      • Stockwell M.S.
      • Kharbanda E.O.
      • Martinez R.A.
      • et al.
      Text4Health: Impact of text message reminder-recalls for pediatric and adolescent immunizations.
      ,
      • Suh C.A.
      • Saville A.
      • Daley M.F.
      • et al.
      Effectiveness and net cost of reminder/recall for adolescent immunizations.
      ,
      • Szilagyi P.G.
      • Albertin C.
      • Humiston S.G.
      • et al.
      A randomized trial of the effect of centralized reminder/recall on immunizations and preventive care visits for adolescents.
      ]. Subgroup analysis suggests that vaccination requirement in school, reminders, and national permissive recommendation had a significant impact on improving coverage while clinic staff training showed a nonsignificant impact. Strategies to improve coverage for HPV vaccines including countrywide provision and clinic-based delivery resulted in a significant decrease in the prevalence of HPV by 44% (RR: .56; 95% CI: .38–.82; Figure 3) [
      • Markowitz L.E.
      • Hariri S.
      • Lin C.
      • et al.
      Reduction in human papillomavirus (HPV) prevalence among young women following HPV vaccine introduction in the United States, National Health and Nutrition Examination Surveys, 2003-2010.
      ,
      • Mesher D.
      • Soldan K.
      • Howell-Jones R.
      • et al.
      Reduction in HPV 16/18 prevalence in sexually active young women following the introduction of HPV immunisation in England.
      ] and genital warts by 33% (RR: .66; 95% CI: .52–.84; Figure 4) [
      • Baandrup L.
      • Blomberg M.
      • Dehlendorff C.
      • et al.
      Significant decrease in the incidence of genital warts in young Danish women after implementation of a national human papillomavirus vaccination program.
      ,
      • Bauer H.M.
      • Wright G.
      • Chow J.
      Evidence of human papillomavirus vaccine effectiveness in reducing genital warts: An analysis of California public family planning administrative claims data, 2007-2010.
      ,
      • Read T.R.
      • Hocking J.S.
      • Chen M.Y.
      • et al.
      The near disappearance of genital warts in young women 4 years after commencing a national human papillomavirus (HPV) vaccination programme.
      ]; however, the quality of evidence was low. Since only one study each was included for measles, mumps, pertussis, and varicella vaccines, it was not possible to pool results. Analysis from single studies with low or very low quality suggested significant decrease in varicella deaths (RR: .74; 95% CI: .56–.98), measles incidence (RR: .12; 95% CI: .03–.38), rubella susceptibility (RR: .27; 95% CI: .15–.46), and incidence of pertussis (RR: .24; 95% CI: .16–.36) while the impact was nonsignificant for incidence of mumps (RR: .96; 95% CI: .42–2.18).
      Figure thumbnail gr2
      Figure 2Forest plot for the impact of strategies on vaccination coverage. IV = inverse variance; MCV = meningococcal conjugate vaccine; SE = standard error.
      Figure thumbnail gr3
      Figure 3Forest plot for the prevalence of HPV. IV = inverse variance; SE = standard error.
      Figure thumbnail gr4
      Figure 4Forest plot for the prevalence of genital warts. IV = inverse variance; SE = standard error.
      The outcome quality was rated to be “moderate” for vaccine coverage; “low” for the prevalence of HPV, genital warts, and mump incidence; and “very low” for varicella deaths, measles incidence, rubella susceptibility, and incidence of pertussis. The outcome quality was downgraded due to nonrobust designs, heterogeneity, and limited generalizability to HICs only. A summary of quality of evidence is provided in Table 2.
      Table 2Summary of findings for the effect of interventions for improving immunization coverage among adolescents
      Quality assessmentSummary of findings
      Number of studiesDesignLimitationsConsistencyDirectnessNumber of eventsRR (95% CI)
      Generalizability to population of interestGeneralizability to intervention of interestInterventionControl
      Vaccine coverage: moderate outcome-specific quality of evidence
       13 studies (14 data sets)RCT, quasi, and observational studiesStudy designs not robustTwelve studies suggest benefitAll studies targeted adolescents aged 11–19 years in developed countriesInterventions included vaccination requirement in school, reminders, and national permissive recommendation5,0924,3031.78 (1.41–2.23)
      HPV prevalence: low outcome-specific quality of evidence
       Two studiesObservational studiesStudy designs not robustBoth studies suggest benefitStudies targeted adolescents aged 14–24 years in developed countriesIntervention included introducing HPV vaccine into routine immunization499554.56 (.38–.82)
      Incidence of genital warts: low outcome-specific quality of evidence
       Three studiesObservational studiesStudy designs not robustAll three studies suggest benefitAll studies from developed countries targeting adolescents from age 12 to 21 yearsAll studies focused on increased provision of HPV vaccine through national HPV programs3,8755,409.66 (.52–.84)
      Varicella deaths: very low outcome-specific quality of evidence
       OneObservational studyStudy design not robustOnly one studyIntervention targeted all age groups in the United States, outcomes reported for 10- to 19-year age groupUniversal childhood varicella vaccination program77104.74 (.56–.98)
      Mumps incidence: low outcome-specific quality of evidence
       OneQuasitrialNo randomization (quasitrial)Only one studyAdolescents 9–14 years in the United StatesSchool-based immunization287.96 (.42–2.21)
      Pertussis incidence: very low outcome-specific quality of evidence
       OneObservational studyStudy design not robustOnly one studyInterventions targeted adolescents 12–19 years in AustraliaSchool-based delivery of TDaP vaccine31128.24 (.16–.36)
      Rubella susceptibility: very low outcome specific quality of evidence
       OneObservational studyStudy design not robustOnly one studyInterventions targeted adolescent girls >10 years in the United StatesVaccination requirement in school1549.27 (.15–.46)
      Measles incidence: very low outcome-specific quality of evidence
       OneObservational studyStudy design not robustOnly one studyInterventions targeted all ages in ChinaSupplementary immunization activities326.12 (.03–.38)
      CI = confidence interval; HPV = human papillomavirus; RCT = randomized controlled trial; RR = relative risk; TDaP = Tetanus, diphtheria, pertussis.

      Discussion

      Our review findings suggest that strategies to increase HPV, TDaP, MMR, and varicella vaccination uptake among adolescents can significantly improve the coverage for these vaccines. Implementing vaccination requirement in school, sending reminders, and national permissive recommendation for adolescent vaccination has the potential to improve immunization uptake. These interventions have also led to significant decline in the prevalence of HPV and genital warts; incidence of measles and pertussis; rubella susceptibility; and varicella deaths. However, these findings should be interpreted with caution since these are from single studies with low or very low quality. Furthermore, these studies capture the incremental benefits of vaccination of those who may have missed earlier doses or failed to seroconvert to earlier doses since these vaccines are usually given at younger ages.
      All the included studies were conducted in HICs depicting dearth of evidence evaluating the effectiveness of strategies to improve immunization uptake among adolescent from LMICs. This could also be attributable to the scope of review since our review was restricted to strict inclusion and exclusion criteria, and we did not include gray literature reporting various country case studies. Furthermore, recent state mandatory vaccination and exception policies could also have affected the vaccination coverage rates; however, these programs and policy interventions do not lend themselves to intervention studies. One of the limitations of the review was that the search terms were in English, and hence foreign language articles may not have been identified. There is lack of rigorously designed studies since most of the existing studies have utilized the pre- and postimplementation data after the approval of vaccine legislation or national launch of vaccination program without having a control site. Only a single study each for MMR, TDaP, varicella, and meningococcal vaccines were found, showing a lack of focus evaluating the impact of uptake for vaccines other than HPV. This highlights the need for further studies to assess the uptake and delivery platforms to deliver these vaccines in adolescent population. Included studies targeted various overlapping adolescent and youth age groups that might have led to variations in the outcome effect.
      Despite the high burden of infectious diseases and low immunization coverage in LMICs, strategies to improve vaccine coverage for adolescent age group are minimal. Although there are existing data outlining what exists in LMICs for delivering adolescent immunization, primarily through school-based approaches; however, there are little data that have systematically been evaluated for the impact of strategies to increase coverage [
      World Health Organization
      Immunization, vaccines and biologicals: Data, statistics and graphics.
      ]. Various countries' case studies have documented experiences from LMICs with existing school-based immunization programs, for example, in Indonesia, Malaysia, Sri Lanka, and Tunisia; however, they lack rigorous evaluations [
      World Health Organization
      Immunization, vaccines and biologicals: School-based immunization.
      ]. For HPV, various national-level programs are in place especially in LMICs; Bhutan is the first LMIC to roll out a national HPV vaccination program, followed by Rwanda and Uganda. These programs suggest that vaccine uptake can be improved by providing evidence-based education and outreach; however, experiences in these countries underscore complex challenges and planning to ensure sustainability [
      • Adams P.
      Reaching teenagers with three-times jab is a first for most countries.
      ]. The number of LMICs that have introduced HPV vaccination is relatively low; however, the coverage levels in these countries are relatively higher than in some HIC. Enabling factors for improved coverage in LMICs include political will, nationwide sensitization campaign, school-based vaccination, and community involvement [
      World Health Organization
      Immunization, vaccines and biologicals: Data, statistics and graphics.
      ,
      World Health Organization
      Immunization, vaccines and biologicals: School-based immunization.
      ,
      • Adams P.
      Reaching teenagers with three-times jab is a first for most countries.
      ,
      • Binagwaho A.
      • Wagner C.M.
      • Gatera M.
      • et al.
      Achieving high coverage in Rwanda's national human papillomavirus vaccination programme.
      ].
      Despite the availability of the HPV vaccine in HICs like the United States, the uptake remains low. Vaccine utilization is a multifactorial phenomenon which depends on several factors including vaccine acceptability, perceived disease susceptibility, perceived benefit of vaccination, and intention to receive the particular vaccine. A recent systematic review on barriers to HPV vaccination among adolescents in the United States suggests financial concerns and parental attitudes as barriers to HPV vaccination [
      • Holman D.M.
      • Benar V.
      • Roland K.B.
      • et al.
      Barriers to human papillomavirus vaccination among US Adolescents. A systematic review of the literature.
      ,
      • Cassidy B.
      • Elizabeth A.S.
      Uptake of the human papillomavirus vaccine: A review of the literature and report of a quality assurance project.
      ]. Good understanding and knowledge of the factors and importance of vaccine in target population are important for tailoring vaccine improvement strategies and subsequent success of the program in achieving targeted vaccine coverage [
      • Middleman A.B.
      • Rosenthal S.L.
      • Rickert V.I.
      • et al.
      Adolescent immunizations: A position paper of the Society for Adolescent Medicine.
      ]. It is imperative to develop and test context-specific strategies to improve adolescent vaccine uptake and dose completion rates. Educational interventions could increase knowledge and clear misconceptions related to seriousness of vaccine-preventable infection and cervical cancer, susceptibility of adolescents to infection, and risk of infection. Such strategies would also address barriers to adolescent vaccine uptake and dose completion, such as parental concerns about vaccine safety, and effectiveness [
      • Tissot A.M.
      • Zimet G.D.
      • Rosenthal S.L.
      • et al.
      Effective strategies for HPV vaccine delivery: The views of pediatricians.
      ]. Very few of the included studies in our review utilized mHealth/eHealth technology for improving immunization coverage which could be one of the potentially effective strategies to target adolescent age group especially in LMIC settings owing to the higher use in this age group and recent explosion in Internet access in developing countries due to the emergence of mobile Internet [

      John D Piette a, KC Lun b, Lincoln A Moura c, Hamish SF Fraser d, Patricia N Mechael e, John Powell f & Shariq R Khoja g. Impacts of e-health on the outcomes of care in low- and middle-income countries: Where do we go from here? Bulletin of the World Health Organization. Available at: http://www.who.int/bulletin/volumes/90/5/11-099069/en/index.html. Accessed November 16, 2015.

      ]. One of the concerns with the introduction of HPV vaccine in low-resourced high-burden countries is lack of cost-effective data; however, some recent analysis suggests that HPV vaccination is likely to be cost-effective, especially in LMICs [
      • Jit M.
      • Brisson M.
      • Portnoy A.
      • Hutubessy R.
      Cost-effectiveness of female human papillomavirus vaccination in 179 countries: A PRIME modelling study.
      ,
      • Fesenfeld M.
      • Hutubessy R.
      • Jit M.
      Cost-effectiveness of human papillomavirus vaccination in low and middle income countries: A systematic review.
      ].
      Improving vaccination coverage to decrease the burden of these preventable diseases would require an integrated approach ranging from mass availability of vaccines at the national level to targeting adolescents in school and during health care visits to optimize the effectiveness of immunization programs. Besides these programs, there is a need for an increased emphasis on the importance of adolescent immunization by identifying and overcoming barriers to adolescent vaccination. Further research is needed to explore why missed vaccination opportunities occur and to develop evidence-based strategies to reduce missed opportunities and improve adolescent vaccination coverage.

      Acknowledgments

      All authors contributed to finalizing the manuscript.

      Funding Sources

      The preparation and publication of these papers was made possible through an unrestricted grant from the Bill & Melinda Gates Foundation (BMGF).

      References

      1. National Foundation for Infectious Diseases: Adolescent vaccination bridging from a strong childhood foundation to a healthy adulthood: A report on strategies to increase adolescent immunization rates. Available at: http://www2.aap.org/immunization/pediatricians/pdf/ImmunizationofAdolescents_nfid.pdf. Accessed November 16, 2015.

        • National Foundation of Infectious Diseases
        Adolescent vaccination: Bridging from a strong childhood foundation to a healthy adulthood.
        2012 (Available at:) (Accessed November 16, 2015)
      2. Human papillomavirus vaccination coverage among adolescent girls, 2007–2012, and postlicensure vaccine safety monitoring, 2006–2013—United States.
        Morbidity Mortality Weekly Rep. 2013; (Available at:) (Accessed November 16, 2015)
        • Wong C.A.
        • Taylor J.A.
        • Wright J.A.
        • et al.
        Missed opportunities for adolescent vaccination, 2006-2011.
        J Adolesc Health. 2013; 53: 492-497
        • World Health Organization
        Globocan 2012: Estimated cancer incidence, mortality and prevalence worldwide.
        2012 (Available at:) (Accessed November 16, 2015)
        • Forman D.
        • de Martel C.
        • Lacey C.J.
        • et al.
        Global burden of human papillomavirus and related diseases.
        Vaccine. 2012; 30: F12-F23
        • WHO/ICO Information center on HPV and Cervical Cancer
        Human papilomavirus and related cancers in Ethiopia.
        (Summary report)2010 (Available at:) (Accessed November 16, 2015)
        • Fitzmaurice C.
        • Dicker D.
        • Pain A.
        • et al.
        The global burden of cancer 2013.
        JAMA Oncol. 2015; 4: 505
        • Kessels S.J.M.
        • Marshall H.S.
        • Watson M.
        • et al.
        Factors associated with HPV vaccine uptake in teenage girls: A systematic review.
        Vaccine. 2012; 30: 3546-3556
        • World Health Organization
        WHO recommendations for routine immunization—Summary tables.
        2015 (Available at:) (Accessed November 16, 2015)
        • American Academy of Pediatrics Immunization Resources
        Adolescent immunizations: Strategies for increasing coverage rates.
        2013 (Available at:) (Accessed November 16, 2015)
        • Salam R.A.
        • Faqqah A.
        • Sajjad N.
        • et al.
        Improving adolescent sexual and reproductive health: A systematic review of potential interventions.
        J Adolesc Health. 2016; 59: S11-S28
        • Salam R.A.
        • Hooda M.
        • Das J.K.
        • et al.
        Interventions to improve adolescent nutrition: A systematic review and meta-analysis.
        J Adolesc Health. 2016; 59: S29-S39
        • Das J.K.
        • Salam R.A.
        • Arshad A.
        • et al.
        Interventions for adolescent substance abuse: An overview of systematic reviews.
        J Adolesc Health. 2016; 59: S61-S75
        • Das J.K.
        • Salam R.A.
        • Lassi Z.S.
        • et al.
        Interventions for adolescent mental health: an overview of systematic reviews.
        J Adolesc Health. 2016; 59: S49-S60
        • Salam R.A.
        • Arshad A.
        • Das J.K.
        • et al.
        Interventions to prevent unintentional injuries among adolescents: A systematic review and meta-analysis.
        J Adolesc Health. 2016; 59: S76-S87
        • Salam R.A.
        • Das J.K.
        • Lassi Z.S.
        • Bhutta Z.A.
        Adolescent health interventions: Conclusions, evidence gaps, and research priorities.
        J Adolesc Health. 2016; 59: S88-S92
        • Salam R.A.
        • Das J.K.
        • Lassi Z.S.
        • Bhutta Z.A.
        Adolescent health and well-being: Background and methodology for review of potential interventions.
        J Adolesc Health. 2016; 59: S4-S10
        • Centers for Disease Control and Prevention
        Vaccine recommendations of the ACIP.
        2014 (Available at:) (Accessed November 16, 2015)
        • Walker N.
        • Fischer-Walker C.
        • Bryce J.
        • et al.
        Standards for CHERG reviews of intervention effects on child survival.
        Int J Epidemiol. 2010; 39: i21-i31
        • Zhuo J.
        • Geng W.
        • Hoekstra E.J.
        • et al.
        Impact of supplementary immunization activities in measles-endemic areas: A case study from Guangxi, China.
        J Infect Dis. 2011; 204: S455-S462
        • Ogbuanu I.U.
        • Kutty P.K.
        • Hudson J.M.
        • et al.
        Impact of a third dose of measles-mumps-rubella vaccine on a mumps outbreak.
        Pediatrics. 2012; 130: e1567-e1574
        • Nguyen H.Q.
        • Jumaan A.O.
        • Seward J.F.
        Decline in mortality due to varicella after implementation of varicella vaccination in the United States.
        N Engl J Med. 2005; 352: 450-458
        • Quinn H.E.
        • McIntyre P.B.
        The impact of adolescent pertussis immunization, 2004-2009: Lessons from Australia.
        Bull World Health Organ. 2011; 89: 666-674
        • Nelson D.B.
        • Layde M.M.
        • Chatton T.B.
        Rubella susceptibility in inner-city adolescents: The effect of a school immunization law.
        Am J Public Health. 1982; 72: 710-713
        • Baandrup L.
        • Blomberg M.
        • Dehlendorff C.
        • et al.
        Significant decrease in the incidence of genital warts in young Danish women after implementation of a national human papillomavirus vaccination program.
        Sex Transm Dis. 2013; 40: 130-135
        • Bauer H.M.
        • Wright G.
        • Chow J.
        Evidence of human papillomavirus vaccine effectiveness in reducing genital warts: An analysis of California public family planning administrative claims data, 2007-2010.
        Am J Public Health. 2012; 102: 833-835
        • Markowitz L.E.
        • Hariri S.
        • Lin C.
        • et al.
        Reduction in human papillomavirus (HPV) prevalence among young women following HPV vaccine introduction in the United States, National Health and Nutrition Examination Surveys, 2003-2010.
        J Infect Dis. 2013; 208: 385-393
        • Mesher D.
        • Soldan K.
        • Howell-Jones R.
        • et al.
        Reduction in HPV 16/18 prevalence in sexually active young women following the introduction of HPV immunisation in England.
        Vaccine. 2013; 32: 26-32
        • Musto R.
        • Siever J.E.
        • Johnston J.C.
        • et al.
        Social equity in human papillomavirus vaccination: A natural experiment in Calgary Canada.
        BMC Public Health. 2013; 13: 640
        • Read T.R.
        • Hocking J.S.
        • Chen M.Y.
        • et al.
        The near disappearance of genital warts in young women 4 years after commencing a national human papillomavirus (HPV) vaccination programme.
        Sex Transm Infect. 2011; 87: 544-547
        • Reiter P.L.
        • Gilkey M.B.
        • Brewer N.T.
        HPV vaccination among adolescent males: Results from the National Immunization Survey-Teen.
        Vaccine. 2013; 31: 2816-2821
        • Averhoff F.
        • Linton L.
        • Peddecord K.M.
        • et al.
        A middle school immunization law rapidly and substantially increases immunization coverage among adolescents.
        Am J Public Health. 2004; 94: 978-984
        • Bugenske E.
        • Stokley S.
        • Kennedy A.
        • Dorell C.
        Middle school vaccination requirements and adolescent vaccination coverage.
        Pediatrics. 2012; 129: 1056-1063
        • Carlson J.A.
        • Lewis C.A.
        Effect of the immunization program in Ontario schools.
        Can Med Assoc J. 1985; 133: 215-216
        • Fogarty K.J.
        • Massoudi M.S.
        • Gallo W.
        • et al.
        Vaccine coverage levels after implementation of a middle school vaccination requirement, Florida, 1997-2000.
        Public Health Rep. 2004; 119: 163-169
        • Harper P.G.
        • Murray D.M.
        An organizational strategy to improve adolescent measles-mumps-rubella vaccination in a low socioeconomic population. A method to reduce missed opportunities.
        Arch Fam Med. 1994; 3: 257-262
        • Kempe A.
        • Barrow J.
        • Stokley S.
        • et al.
        Effectiveness and cost of immunization recall at school-based health centers.
        Pediatrics. 2012; 129: e1446-e1452
        • Kharbanda E.O.
        • Stockwell M.S.
        • Colgrove J.
        • et al.
        Changes in Tdap and MCV4 vaccine coverage following enactment of a statewide requirement of Tdap vaccination for entry into sixth grade.
        Am J Public Health. 2010; 100: 1635-1640
        • Moss J.L.
        • Reiter P.L.
        • Dayton A.
        • Brewer N.T.
        Increasing adolescent immunization by webinar: A brief provider intervention at federally qualified health centers.
        Vaccine. 2012; 30: 4960-4963
        • Stockwell M.S.
        • Kharbanda E.O.
        • Martinez R.A.
        • et al.
        Text4Health: Impact of text message reminder-recalls for pediatric and adolescent immunizations.
        Am J Public Health. 2012; 102: e15-e21
        • Suh C.A.
        • Saville A.
        • Daley M.F.
        • et al.
        Effectiveness and net cost of reminder/recall for adolescent immunizations.
        Pediatrics. 2012; 129: e1437-e1445
        • Szilagyi P.G.
        • Albertin C.
        • Humiston S.G.
        • et al.
        A randomized trial of the effect of centralized reminder/recall on immunizations and preventive care visits for adolescents.
        Acad Pediatr. 2013; 13: 204-213
        • World Health Organization
        Immunization, vaccines and biologicals: Data, statistics and graphics.
        2015 (Available at:) (Accessed November 16, 2015)
        • World Health Organization
        Immunization, vaccines and biologicals: School-based immunization.
        2015 (Available at:) (Accessed November 16, 2015)
        • Adams P.
        Reaching teenagers with three-times jab is a first for most countries.
        Bull World Health Organ. 2012; 90 (World Health Organization): 874
        • Binagwaho A.
        • Wagner C.M.
        • Gatera M.
        • et al.
        Achieving high coverage in Rwanda's national human papillomavirus vaccination programme.
        Bull World Health Organ. 2012; 90: 623-628
        • Holman D.M.
        • Benar V.
        • Roland K.B.
        • et al.
        Barriers to human papillomavirus vaccination among US Adolescents. A systematic review of the literature.
        JAMA Pediatr. 2014; 168: 76-82
        • Cassidy B.
        • Elizabeth A.S.
        Uptake of the human papillomavirus vaccine: A review of the literature and report of a quality assurance project.
        J Pediatr Health Care. 2012; 26: 92-101
        • Middleman A.B.
        • Rosenthal S.L.
        • Rickert V.I.
        • et al.
        Adolescent immunizations: A position paper of the Society for Adolescent Medicine.
        J Adolesc Health. 2006; 38: 321-327
        • Tissot A.M.
        • Zimet G.D.
        • Rosenthal S.L.
        • et al.
        Effective strategies for HPV vaccine delivery: The views of pediatricians.
        J Adolesc Health. 2007; 41: 119-125
      3. John D Piette a, KC Lun b, Lincoln A Moura c, Hamish SF Fraser d, Patricia N Mechael e, John Powell f & Shariq R Khoja g. Impacts of e-health on the outcomes of care in low- and middle-income countries: Where do we go from here? Bulletin of the World Health Organization. Available at: http://www.who.int/bulletin/volumes/90/5/11-099069/en/index.html. Accessed November 16, 2015.

        • Jit M.
        • Brisson M.
        • Portnoy A.
        • Hutubessy R.
        Cost-effectiveness of female human papillomavirus vaccination in 179 countries: A PRIME modelling study.
        The Lancet Glob Health. 2014; 2: e406-e414
        • Fesenfeld M.
        • Hutubessy R.
        • Jit M.
        Cost-effectiveness of human papillomavirus vaccination in low and middle income countries: A systematic review.
        Vaccine. 2013; 31: 3786-3804

      Linked Article

      • Evidence and Evidence Gaps in Adolescent Health
        Journal of Adolescent HealthVol. 59Issue 4
        • Preview
          The momentum to bring adolescents and young adults to center stage in global health and international development is palpable. Adolescents are increasingly seen as a crucial group for the success of the newly adopted Agenda for Sustainable Development [1]. Sitting within the Agenda for Sustainable Development framework, the 2030 Global Strategy for Women's, Children's and Adolescents' Health has extended the Every Woman, Every Child agenda to adolescence [2]. The strategy articulates the need for adolescent responsive health systems as well as social determinants, a focus that extends to legal and policy environments [3].
        • Full-Text
        • PDF
        Open Access