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Human Papillomavirus Vaccine Interventions in the U.S.: A Systematic Review and Meta-analysis

Published:February 15, 2019DOI:https://doi.org/10.1016/j.amepre.2018.10.033

      Context

      Despite current recommendations, human papillomavirus vaccine uptake remains low. A systematic review and meta-analysis assessed the effectiveness of interventions targeting human papillomavirus vaccine initiation and completion among children, adolescents, and young adults aged 9–26 years.

      Evidence acquisition

      Three electronic databases (CINAHL, OVID, and Web of Science) were searched for articles published in English peer-reviewed journals between January 2006 and January 2017 of U.S. studies that evaluated intervention strategies and reported post-intervention human papillomavirus vaccine initiation or completion rates among individuals aged 9–26 years. Study characteristics and outcomes were extracted. Data were collected in 2016 and analyzed in 2017.

      Evidence synthesis

      Reviewers screened 983 unique titles and abstracts, read 241 full-text articles, and extracted data from 30 articles meeting the inclusion criteria (12 behavioral, ten environmental, four informational, and four combination strategies). Published EQUATOR (Enhancing the Quality and Transparency of Health Research) guidelines were used to assess study quality. Random effects meta-analyses were conducted. The meta-analyses included 17 RCTs and quasi-experiments involving 68,623 children, adolescents, and young adults. The pooled relative incidence estimates were 1.84 (95% CI=1.36, 2.48) for human papillomavirus vaccine initiation and 1.50 (95% CI=1.23, 1.83) for completion. Behavioral and informational interventions doubled human papillomavirus vaccine initiation (relative incidence estimate=2.04, 95% CI=1.36, 3.06 and relative incidence estimate=1.92, 95% CI=1.27, 2.91, respectively). Behavioral interventions increased completion by 68% (relative incidence estimate=1.68, 95% CI=1.25, 2.27).

      Conclusions

      Evidence supports behavioral interventions for increasing human papillomavirus vaccine initiation and completion. Future studies are needed to assess the effectiveness of interventions in reaching diverse populations and reducing missed opportunities for human papillomavirus vaccination.
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      REFERENCES

        • Braaten KP
        • Laufer MR
        Human papillomavirus (HPV), HPV-related disease, and the HPV vaccine.
        Rev Obstet Gynecol. 2008; 1: 2-10
        • Hilton S
        • Hunt K
        • Bedford H
        • Petticrew M
        School nurses’ experiences of delivering the UK HPV vaccination programme in its first year.
        BMC Infect Dis. 2011; 11: 226
        • Bosch X
        • Harper D
        Prevention strategies of cervical cancer in the HPV vaccine era.
        Gynecol Oncol. 2006; 103: 21-24
      1. CDC. HPV Vaccine Information for Young Women. www.cdc.gov/std/hpv/stdfact-hpv-vaccine-young-women.htm. Published January 3, 2017. Accessed 2017.

        • Dochez C
        • Bogers JJ
        • Verhelst R
        • Rees H
        HPV vaccines to prevent cervical cancer and genital warts: an update.
        Vaccine. 2014; 32: 1595-1601
        • Schiffman M
        • Wentzensen N
        • Wacholder S
        • Kinney W
        • Gage JC
        • Castle PE
        Human papillomavirus testing in the prevention of cervical cancer.
        J Natl Cancer Inst. 2011; 103: 368-383
        • Thomas TL
        • Strickland O
        • Diclemente R
        • Higgins M
        An opportunity for cancer prevention during preadolescence and adolescence: stopping human papillomavirus (HPV)-related cancer through HPV vaccination.
        J Adolesc Health. 2013; 52: S60-S68
        • Walboomers JM
        • Jacobs MV
        • Manos MM
        • et al.
        Human papillomavirus is a necessary cause of invasive cervical cancer worldwide.
        J Pathol. 1999; 189: 12-19
      2. CDC. Basic Information about HPV-associated cancers. www.cdc.gov/cancer/hpv/basic_info. Published September 5, 2013. Accessed August 24, 2014.

      3. CDC. HPV-Associated Cancers Statistics. www.cdc.gov/cancer/hpv/statistics/index.htm. Published 2014. Accessed April 2, 2018.

        • Petrosky E
        • Bocchini Jr., JA
        • Hariri S
        • et al.
        Use of 9-valent human papillomavirus (HPV) vaccine: updated HPV vaccination recommendations of the Advisory Committee on Immunization Practices.
        MMWR Morb Mortal Wkly Rep. 2015; 64: 300-304
        • Markowitz LE
        • Dunne EF
        • Saraiya M
        • et al.
        Human papillomavirus vaccination: recommendations of the Advisory Committee on Immunization Practices (ACIP).
        MMWR Recomm Rep. 2014; 63: 1-30
        • Shah PD
        • Gilkey MB
        • Pepper JK
        • Gottlieb SL
        • Brewer NT
        Promising alternative settings for HPV vaccination of U.S. adolescents.
        Expert Rev Vaccines. 2014; 13: 235-246
      4. Office of Disease Prevention and Health Promotion, Immunization and Infectious Diseases.
        Healthy People. 2020; (Published 2015)
        • Walling EB
        • Benzoni N
        • Dornfeld J
        • et al.
        Interventions to improve HPV vaccine uptake: a systematic review.
        Pediatrics. 2016; 138 (:e20153863.)
        • The FUTURE I/II Study Group
        Four year efficacy of prophylactic human papillomavirus quadrivalent vaccine against low grade cervical, vulvar, and vaginal intraepithelial neoplasia and anogenital warts: randomised controlled trial.
        BMJ. 2010; 341: c3493
        • Reagan-Steiner S
        • Yankey D
        • Jeyarajah J
        • et al.
        National, regional, state, and selected local area vaccination coverage among adolescents aged 13–17 years—United States, 2014.
        MMWR Morb Mortal Wkly Rep. 2015; 64: 784-792
        • HHS
        Accelerating HPV Vaccine Uptake: Urgency for Action to Prevent Cancer.
        HHS, Washington, DC2014
      5. CDC. Clinician FAQ: CDC Recommendations for HPV Vaccine 2-Dose Schedules. www.cdc.gov/hpv/downloads/hcvg15-ptt-hpv-2dose.pdf. Published November 30, 2016. Accessed 2018.

        • Committee on Infectious Diseases
        HPV vaccine recommendations.
        Pediatrics. 2012; 129: 602-605
      6. National Cancer Institute. Preventing cervical cancer: the development of HPV vaccines. www.cancer.gov/research/progress/discovery/hpv-vaccines. Published December 2, 2016. Accessed 2018.

        • American College of Obstetrics and Gynecologists’ Committee on Adolescent Health Care
        Committee Opinion No. 641: Human Papillomavirus Vaccination.
        Obstet Gynecol. 2015; 126: e38-e43
        • National Association of School Nurses
        NASN position statement: immunizations.
        NASN Sch Nurse. 2011; 26: 121-122
        • Block SL
        • Nolan T
        • Sattler C
        • et al.
        Comparison of the immunogenicity and reactogenicity of a prophylactic quadrivalent human papillomavirus (types 6, 11, 16, and 18) L1 virus-like particle vaccine in male and female adolescents and young adult women.
        Pediatrics. 2006; 118: 2135-2145
        • Fu LY
        • Bonhomme LA
        • Cooper SC
        • Joseph JG
        • Zimet GD
        Educational interventions to increase HPV vaccination acceptance: a systematic review.
        Vaccine. 2014; 32: 1901-1920
        • Niccolai LM
        • Hansen CE
        Practice- and community-based interventions to increase human papillomavirus vaccine coverage: a systematic review.
        JAMA Pediatr. 2015; 169: 686-692
        • Kessels SJ
        • Marshall HS
        • Watson M
        • Braunack-Mayer AJ
        • Reuzel R
        • Tooher RL
        Factors associated with HPV vaccine uptake in teenage girls: a systematic review.
        Vaccine. 2012; 30: 3546-3556
        • Priest HM
        • Knowlden AP
        Systematic review of primary prevention human papillomavirus interventions targeting college students.
        Int J Sex Health. 2015; 27: 125-144
        • Bartlett JA
        • Peterson JA
        The uptake of human papillomavirus (HPV) vaccine among adolescent females in the United States: a review of the literature.
        J Sch Nurs. 2011; 27: 434-446
        • Holman DM
        • Benard V
        • Roland KB
        • Watson M
        • Liddon N
        • Stokley S
        Barriers to human papillomavirus vaccination among U.S. adolescents: a systematic review of the literature.
        JAMA Pediatr. 2014; 168: 76-82
        • Allen JD
        • Coronado GD
        • Williams RS
        • et al.
        A systematic review of measures used in studies of human papillomavirus (HPV) vaccine acceptability.
        Vaccine. 2010; 28: 4027-4037
        • Brewer NT
        • Fazekas KI
        Predictors of HPV vaccine acceptability: a theory-informed, systematic review.
        Prev Med. 2007; 45: 107-114
        • Cassidy B
        • Schlenk EA
        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
        • Chan ZC
        • Chan TS
        • Ng KK
        • Wong ML
        A systematic review of literature about women's knowledge and attitudes toward human papillomavirus (HPV) vaccination.
        Public Health Nurs. 2012; 29: 481-489
        • Fisher H
        • Trotter CL
        • Audrey S
        • MacDonald-Wallis K
        • Hickman M
        Inequalities in the uptake of human papillomavirus vaccination: a systematic review and meta-analysis.
        Int J Epidemiol. 2013; 42: 896-908
        • Lin CJ
        • Zimmerman RK
        • Nowalk MP
        • Huang HH
        • Raviotta JM
        Randomized controlled trial of two dosing schedules for human papillomavirus vaccination among college age males.
        Vaccine. 2014; 32: 693-699
        • Rickert VI
        • Auslander BA
        • Cox DS
        • et al.
        School-based vaccination of young U.S. males: impact of health beliefs on intent and first dose acceptance.
        Vaccine. 2014; 32: 1982-1987
        • Brewer NT
        • Gottlieb SL
        • Reiter PL
        • et al.
        Longitudinal predictors of human papillomavirus vaccine initiation among adolescent girls in a high-risk geographic area.
        Sex Transm Dis. 2011; 38: 197-204
        • Kharbanda EO
        • Stockwell MS
        • Fox HW
        • Andres R
        • Lara M
        • Rickert VI
        Text message reminders to promote human papillomavirus vaccination.
        Vaccine. 2011; 29: 2537-2541
        • Chao C
        • Preciado M
        • Slezak J
        • Xu L
        A randomized intervention of reminder letter for human papillomavirus vaccine series completion.
        J Adolesc Health. 2015; 56: 85-90
        • Moher D
        • Liberati A
        • Tetzlaff J
        • Altman DG
        • PRISMA Group
        Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.
        PLoS Med. 2009; 6e1000097
        • Bennett AT
        • Patel DA
        • Carlos RC
        • et al.
        Human papillomavirus vaccine uptake after a tailored, online educational intervention for female university students: a randomized controlled trial.
        J Womens Health (Larchmt). 2015; 24: 950-957
        • Berenson AB
        • Rahman M
        • Hirth JM
        • Rupp RE
        • Sarpong KO
        A human papillomavirus vaccination program for low-income postpartum women.
        Am J Obstet Gynecol. 2016; 215 (318.e1–318.e9)
        • Casey BR
        • Crosby RA
        • Vanderpool RC
        • Dignan M
        • Bates W
        Predictors of initial uptake of human papillomavirus vaccine uptake among rural Appalachian young women.
        J Prim Prev. 2013; 34: 71-80
        • Cassidy B
        • Braxter B
        • Charron-Prochownik D
        • Schlenk EA
        A quality improvement initiative to increase HPV vaccine rates using an educational and reminder strategy with parents of preteen girls.
        J Pediatr Health Care. 2014; 28: 155-164
        • Chung RJ
        • Walter EB
        • Kemper AR
        • Dayton A
        Keen on teen vaccines: improvement of adolescent vaccine coverage in rural North Carolina.
        J Adolesc Health. 2015; 56: S14-S16
        • Crosby RA
        • Casey BR
        • Vanderpool R
        • Collins T
        • Moore GR
        Uptake of free HPV vaccination among young women: a comparison of rural versus urban rates.
        J Rural Health. 2011; 27: 380-384
        • Daley MF
        • Kempe A
        • Pyrzanowski J
        • et al.
        School-located vaccination of adolescents with insurance billing: cost, reimbursement, and vaccination outcomes.
        J Adolesc Health. 2014; 54: 282-288
        • Eldred SV
        • Hamid HS
        • Snider JC
        • et al.
        A medical student-driven “vaccine blitz” at a school-based health center as an effective way to improve adolescent vaccination rates.
        Fam Med. 2015; 47: 546-548
        • Fiks AG
        • Grundmeier RW
        • Mayne S
        • et al.
        Effectiveness of decision support for families, clinicians, or both on HPV vaccine receipt.
        Pediatrics. 2013; 131: 1114-1124
        • Lee HY
        • Koopmeiners JS
        • McHugh J
        • Raveis VH
        • Ahluwalia JS
        mHealth pilot study: text messaging intervention to promote HPV vaccination.
        Am J Health Behav. 2016; 40: 67-76
        • Hopfer S
        Effects of a narrative HPV vaccination intervention aimed at reaching college women: a randomized controlled trial.
        Prev Sci. 2012; 13: 173-182
        • Joseph NP
        • Bernstein J
        • Pelton S
        • et al.
        Brief client-centered motivational and behavioral intervention to promote HPV vaccination in a hard-to-reach population: a pilot randomized controlled trial.
        Clin Pediatr (Phila). 2016; 55: 851-859
        • Moore GR
        • Crosby RA
        • Young A
        • Charnigo R
        Low rates of free human papillomavirus vaccine uptake among young women.
        Sex Health. 2010; 7: 287-290
        • Patel DA
        • Zochowski M
        • Peterman S
        • Dempsey AF
        • Ernst S
        • Dalton VK
        Human papillomavirus vaccine intent and uptake among female college students.
        J Am Coll Health. 2012; 60: 151-161
        • Patel A
        • Stern L
        • Unger Z
        • et al.
        Staying on track: a cluster randomized controlled trial of automated reminders aimed at increasing human papillomavirus vaccine completion.
        Vaccine. 2014; 32: 2428-2433
        • Perkins RB
        • Zisblatt L
        • Legler A
        • Trucks E
        • Hanchate A
        • Gorin SS
        Effectiveness of a provider-focused intervention to improve HPV vaccination rates in boys and girls.
        Vaccine. 2015; 33: 1223-1229
        • Pierre Joseph N
        • Clark JA
        • Mercilus G
        • Wilbur M
        • Figaro J
        • Perkins R
        Racial and ethnic differences in HPV knowledge, attitudes, and vaccination rates among low-income African-American, Haitian, Latina, and Caucasian young adult women.
        J Pediatr Adolesc Gynecol. 2014; 27: 83-92
        • Richman AR
        • Maddy L
        • Torres E
        • Goldberg EJ
        A randomized intervention study to evaluate whether electronic messaging can increase human papillomavirus vaccine completion and knowledge among college students.
        J Am Coll Health. 2016; 64: 269-278
        • Staras SAS
        • Vadaparampil ST
        • Livingston MD
        • Thompson LA
        • Sanders AH
        • Shenkman EA
        Increasing human papillomavirus vaccine initiation among publicly insured Florida adolescents.
        J Adolesc Health. 2015; 56: S40-S46
        • Stubbs BW
        • Panozzo CA
        • Moss JL
        • Reiter PL
        • Whitesell DH
        • Brewer NT
        Evaluation of an intervention providing HPV vaccine in schools.
        Am J Health Behav. 2014; 38: 92-102
        • Underwood NL
        • Weiss P
        • Gargano LM
        • et al.
        Human papillomavirus vaccination among adolescents in Georgia.
        Hum Vaccin Immunother. 2015; 11: 1703-1708
        • Vanderpool RC
        • Casey BR
        • Crosby RA
        HPV-related risk perceptions and HPV vaccine uptake among a sample of young rural women.
        J Community Health. 2011; 36: 903-909
        • Vanderpool RC
        • Breheny PJ
        • Tiller PA
        • et al.
        Implementation and evaluation of a school-based human papillomavirus vaccination program in rural Kentucky.
        Am J Prev Med. 2015; 49: 317-323
        • Wright JD
        • Govindappagari S
        • Pawar N
        • et al.
        Acceptance and compliance with postpartum human papillomavirus vaccination.
        Obstet Gynecol. 2012; 120: 771-782
        • Szilagyi PG
        • Humiston SG
        • Gallivan S
        • Albertin C
        • Sandler M
        • Blumkin A
        Effectiveness of a citywide patient immunization navigator program on improving adolescent immunizations and preventive care visit rates.
        Arch Pediatr Adolesc Med. 2011; 165: 547-553
      7. Centre for Statistics in Medicine, University of Oxford. Enhancing the QUAlity and Transparency Of health Research (EQUATOR) reporting guidelines. www.equator-network.org/reporting-guidelines/. Accessed April 26, 2017.

        • Vandenbroucke JP
        • von Elm E
        • Altman DG
        • et al.
        Strengthening the Reporting of Observational Studies in Epidemiology (STROBE): explanation and elaboration.
        Epidemiology. 2007; 18: 805-835
      8. CONSORT Transparent Reporting of Trials. Consolidated Standards of Reporting Trials (CONSORT) Statement. www.consort-statement.org/. Published 2010. Accessed April 6, 2017.

        • Sullivan KM
        • Dean A
        • Soe MM
        OpenEpi: a web-based epidemiologic and statistical calculator for public health.
        Public Health Rep. 2009; 124: 471-474
        • Riley RD
        • Higgins JP
        • Deeks JJ
        Interpretation of random effects meta-analyses.
        BMJ. 2011; 342: d549
        • Jones CL
        • Jensen JD
        • Scherr CL
        • Brown NR
        • Christy K
        • Weaver J
        The health belief model as an explanatory framework in communication research: exploring parallel, serial, and moderated mediation.
        Health Commun. 2015; 30: 566-576
        • Davey Smith G
        • Egger M
        • Phillips AN
        Meta-analysis. Beyond the grand mean.
        BMJ. 1997; 315: 1610-1614
        • Egger M
        • Smith GD
        Meta-analysis: potentials and promise.
        BMJ. 1997; 315: 1371-1374
        • Greenland S
        Can meta-analysis be salvaged?.
        Am J Epidemiol. 1994; 140: 783-787