Advertisement

Cervical Cancer Incidence in Young U.S. Females After Human Papillomavirus Vaccine Introduction

  • Fangjian Guo
    Correspondence
    Address correspondence to: Fangjian Guo, MD, PhD, Department of Obstetrics & Gynecology, Center for Interdisciplinary Research in Women’s Health, The University of Texas Medical Branch, 301 University Boulevard, Galveston TX 77555
    Affiliations
    Department of Obstetrics & Gynecology and Center for Interdisciplinary Research in Women’s Health, The University of Texas Medical Branch at Galveston, Galveston, Texas
    Search for articles by this author
  • Leslie E. Cofie
    Affiliations
    Department of Obstetrics & Gynecology and Center for Interdisciplinary Research in Women’s Health, The University of Texas Medical Branch at Galveston, Galveston, Texas
    Search for articles by this author
  • Abbey B. Berenson
    Affiliations
    Department of Obstetrics & Gynecology and Center for Interdisciplinary Research in Women’s Health, The University of Texas Medical Branch at Galveston, Galveston, Texas
    Search for articles by this author

      Introduction

      Since 2006, human papillomavirus vaccine has been recommended for young females in the U.S. This study aimed to compare cervical cancer incidence among young women before and after the human papillomavirus vaccine was introduced.

      Methods

      This cross-sectional study used data from the National Program for Cancer Registries and Surveillance, Epidemiology, and End Results Incidence–U.S. Cancer Statistics 2001–2014 database for U.S. females aged 15–34 years. This study compared the 4-year average annual incidence of invasive cervical cancer in the 4 years before human papillomavirus vaccine was introduced (2003–2006) and the 4 most recent years in the vaccine era (2011–2014). Joinpoint regression models of cervical incidence from 2001 to 2014 were fitted to identify the discrete joints (year) that represent statistically significant changes in the direction of the trend after the introduction of human papillomavirus vaccination in 2006. Data were collected in 2001–2014, released, and analyzed in 2017.

      Results

      The 4-year average annual incidence rates for cervical cancer in 2011–2014 were 29% lower than that in 2003–2006 (6.0 vs 8.4 per 1,000,000 people, rate ratio=0.71, 95% CI=0.64, 0.80) among females aged 15–24 years, and 13.0% lower among females aged 25–34 years. Joinpoint analyses of cervical cancer incidence among females aged 15–24 years revealed a significant joint at 2009 for both squamous cell carcinoma and non–squamous cell carcinoma. Among females aged 25–34 years, there was no significant decrease in cervical cancer incidence after 2006.

      Conclusions

      A significant decrease in the incidence of cervical cancer among young females after the introduction of human papillomavirus vaccine may indicate early effects of human papillomavirus vaccination.
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to American Journal of Preventive Medicine
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • de Sanjose S.
        • Quint W.G.
        • Alemany L.
        • et al.
        Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study.
        Lancet Oncol. 2010; 11: 1048-1056https://doi.org/10.1016/S1470-2045(10)70230-8
        • Harper D.M.
        • Franco E.L.
        • Wheeler C.
        • et al.
        Efficacy of a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and 18 in young women: a randomised controlled trial.
        Lancet. 2004; 364: 1757-1765https://doi.org/10.1016/S0140-6736(04)17398-4
        • FUTURE II Study Group
        Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions.
        N Engl J Med. 2007; 356: 1915-1927https://doi.org/10.1056/NEJMoa061741
        • Joura E.A.
        • Giuliano A.R.
        • Iversen O.E.
        • et al.
        A 9-valent HPV vaccine against infection and intraepithelial neoplasia in women.
        N Engl J Med. 2015; 372: 711-723https://doi.org/10.1056/NEJMoa1405044
        • Petrosky E.
        • Bocchini Jr., J.A.
        • 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
        • 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, 2015.
        MMWR Morb Mortal Wkly Rep. 2016; 65: 850-858https://doi.org/10.15585/mmwr.mm6533a4
        • Hariri S.
        • Johnson M.L.
        • Bennett N.M.
        • et al.
        Population-based trends in high-grade cervical lesions in the early human papillomavirus vaccine era in the United States.
        Cancer. 2015; 121: 2775-2781https://doi.org/10.1002/cncr.29266
        • 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: 385-393https://doi.org/10.1093/infdis/jit192
        • Brotherton J.M.
        • Fridman M.
        • May C.L.
        • Chappell G.
        • Saville A.M.
        • Gertig D.M.
        Early effect of the HPV vaccination programme on cervical abnormalities in Victoria, Australia: an ecological study.
        Lancet. 2011; 377: 2085-2092https://doi.org/10.1016/S0140-6736(11)60551-5
        • Flagg E.W.
        • Torrone E.A.
        • Weinstock H.
        Ecological association of human papillomavirus vaccination with cervical dysplasia prevalence in the United States, 2007–2014.
        Am J Public Health. 2016; 106: 2211-2218https://doi.org/10.2105/AJPH.2016.303472
        • Berenson A.B.
        • Laz T.H.
        • Rahman M.
        Reduction in vaccine-type human papillomavirus prevalence among women in the United States, 2009–2012.
        J Infect Dis. 2016; 214: 1961-1964https://doi.org/10.1093/infdis/jiw515
        • U.S. Preventive Services Task Force
        The Guide to Clinical Preventive Services. 2014; (Accessed March 8, 2018)
        • Saslow D.
        • Solomon D.
        • Lawson H.W.
        • et al.
        American Cancer Society, American Society for Colposcopy and Cervical Pathology, and American Society for Clinical Pathology screening guidelines for the prevention and early detection of cervical cancer.
        CA Cancer J Clin. 2012; 62: 147-172https://doi.org/10.3322/caac.21139
        • Committee on Practice Bulletins—Gynecology
        ACOG Practice Bulletin Number 131: Screening for cervical cancer.
        Obstet Gynecol. 2012; 120: 1222-1238
      1. NPCR and SEER Incidence–USCS Public Use Databases. www.cdc.gov/cancer/npcr/public-use/index.htm. Accessed October 15, 2017.

        • Nitschmann C.
        • May T.
        • Mirkovic J.
        • Feldman S.
        Screening history among women with invasive cervical cancer in an academic medical center: will we miss cancers following updated guidelines?.
        J Womens Health (Larchmt). 2016; 25: 826-831https://doi.org/10.1089/jwh.2015.5394
        • NAACCR Race and Ethnicity Work Group
        NAACCR Guideline for Enhancing Hispanic/Latino Identification: Revised NAACCR Hispanic/Latino Identification Algorithm [NHIA v2.2.1].
        (September) North American Association of Central Cancer Registries, Springfield, IL2011
        • Tiwari R.C.
        • Clegg L.X.
        • Zou Z.
        Efficient interval estimation for age-adjusted cancer rates.
        Stat Methods Med Res. 2006; 15: 547-569https://doi.org/10.1177/0962280206070621
        • Kim H.J.
        • Fay M.P.
        • Feuer E.J.
        • Midthune D.N.
        Permutation tests for joinpoint regression with applications to cancer rates.
        Stat Med. 2000; 19 (http://doi.org/10.1002/(SICI)1097-0258(20000215)19:3<335::AID-SIM336<3.0.CO;2-Z): 335-351
      2. Joinpoint Regression Program, Version 4.5.0.1 - June 2017; Statistical Methodology and Applications Branch, Surveillance Research Program, National Cancer Institute.
      3. Public-Use Data Files and Documentation. www.cdc.gov/nchs/data_access/ftp_data.htm. Accessed January 12, 2018.

        • Meites E.
        • Kempe A.
        • Markowitz L.E.
        Use of a 2-dose schedule for human papillomavirus vaccination–updated recommendations of the Advisory Committee on Immunization Practices.
        MMWR Morb Mortal Wkly Rep. 2016; 65: 1405-1408https://doi.org/10.15585/mmwr.mm6549a5
        • Drolet M.
        • Bénard É.
        • Boily M.C.
        • et al.
        Population-level impact and herd effects following human papillomavirus vaccination programmes: a systematic review and meta-analysis.
        Lancet Infect Dis. 2015; 15: 565-580https://doi.org/10.1016/S1473-3099(14)71073-4
        • Markowitz L.E.
        • Liu G.
        • Hariri S.
        • Steinau M.
        • Dunne E.F.
        • Unger E.R.
        Prevalence of HPV after introduction of the vaccination program in the United States.
        Pediatrics. 2016; 137: 1-9https://doi.org/10.1542/peds.2015-1968
        • Guo F.
        • Hirth J.M.
        • Berenson A.B.
        Comparison of HPV prevalence between HPV-vaccinated and non-vaccinated young adult women (20–26 years).
        Hum Vaccin Immunother. 2015; 11: 2337-2344https://doi.org/10.1080/21645515.2015.1066948
        • Oliver S.E.
        • Unger E.R.
        • Lewis R.
        • et al.
        Prevalence of human papillomavirus among females after vaccine introduction-National Health and Nutrition Examination Survey, United States, 2003–2014.
        J Infect Dis. 2017; 216: 594-603https://doi.org/10.1093/infdis/jix244
        • Hirth J.M.
        • Chang M.
        • Resto V.A.
        • Group H.S.
        Prevalence of oral human papillomavirus by vaccination status among young adults (18–30 years old).
        Vaccine. 2017; 35: 3446-3451https://doi.org/10.1016/j.vaccine.2017.05.025
        • Berenson A.B.
        • Hirth J.M.
        • Chang M.
        Change in human papillomavirus prevalence among U.S. women aged 18-59 years, 2009–2014.
        Obstet Gynecol. 2017; 130: 693-701https://doi.org/10.1097/AOG.0000000000002193
        • Hariri S.
        • Bennett N.M.
        • Niccolai L.M.
        • et al.
        Reduction in HPV 16/18-associated high grade cervical lesions following HPV vaccine introduction in the United States–2008–2012.
        Vaccine. 2015; 33: 1608-1613https://doi.org/10.1016/j.vaccine.2015.01.084
        • Mahmud S.M.
        • Kliewer E.V.
        • Lambert P.
        • Bozat-Emre S.
        • Demers A.A.
        Effectiveness of the quadrivalent human papillomavirus vaccine against cervical dysplasia in Manitoba, Canada.
        J Clin Oncol. 2014; 32: 438-443https://doi.org/10.1200/JCO.2013.52.4645
        • Pollock K.G.
        • Kavanagh K.
        • Potts A.
        • et al.
        Reduction of low- and high-grade cervical abnormalities associated with high uptake of the HPV bivalent vaccine in Scotland.
        Br J Cancer. 2014; 111: 1824-1830https://doi.org/10.1038/bjc.2014.479
        • Baldur-Felskov B.
        • Dehlendorff C.
        • Junge J.
        • Munk C.
        • Kjaer S.K.
        Incidence of cervical lesions in Danish women before and after implementation of a national HPV vaccination program.
        Cancer Causes Control. 2014; 25: 915-922https://doi.org/10.1007/s10552-014-0392-4
        • Benard V.B.
        • Thomas C.C.
        • King J.
        • Massetti G.M.
        • Doria-Rose V.P.
        • Saraiya M.
        Vital signs: cervical cancer incidence, mortality, and screening–United States, 2007–2012.
        MMWR Morb Mortal Wkly Rep. 2014; 63: 1004-1009
        • Beachler D.C.
        • Tota J.E.
        • Silver M.I.
        • et al.
        Trends in cervical cancer incidence in younger U.S. women from 2000 to 2013.
        Gynecol Oncol. 2017; 144: 391-395https://doi.org/10.1016/j.ygyno.2016.11.031
        • CDC
        Sexually Transmitted Disease Surveillance 2016.
        HHS, Atlanta, GA2017
        • ACOG Committee on Practice Bulletins—Gynecology
        ACOG Practice Bulletin no. 109: cervical cytology screening.
        Obstet Gynecol. 2009; 114: 1409-1420https://doi.org/10.1097/AOG.0b013e3181c6f8a4
        • Whitlock E.P.
        • Vesco K.K.
        • Eder M.
        • Lin J.S.
        • Senger C.A.
        • Burda B.U.
        Liquid-based cytology and human papillomavirus testing to screen for cervical cancer: a systematic review for the U.S. Preventive Services Task Force.
        Ann Intern Med. 2011; 155: 687-697https://doi.org/10.7326/0003-4819-155-10-201111150-00376
        • Saslow D.
        • Runowicz C.D.
        • Solomon D.
        • et al.
        American Cancer Society guideline for the early detection of cervical neoplasia and cancer.
        CA Cancer J Clin. 2002; 52: 342-362https://doi.org/10.3322/canjclin.52.6.342
        • Castanon A.
        • Landy R.
        • Sasieni P.D.
        Is cervical screening preventing adenocarcinoma and adenosquamous carcinoma of the cervix?.
        Int J Cancer. 2016; 139: 1040-1045https://doi.org/10.1002/ijc.30152
        • Wang S.S.
        • Sherman M.E.
        • Hildesheim A.
        • Lacey J.V.
        • Devesa S.
        Cervical adenocarcinoma and squamous cell carcinoma incidence trends among white women and black women in the United States for 1976–2000.
        Cancer. 2004; 100: 1035-1044https://doi.org/10.1002/cncr.20064
        • Castellsagué X.
        • Díaz M.
        • de Sanjosé S.
        • et al.
        Worldwide human papillomavirus etiology of cervical adenocarcinoma and its cofactors: implications for screening and prevention.
        J Natl Cancer Inst. 2006; 98: 303-315https://doi.org/10.1093/jnci/djj067