Advertisement

Journal of Cancer Survivorship

, Volume 13, Issue 5, pp 730–738 | Cite as

Suboptimal uptake of human papillomavirus (HPV) vaccine in survivors of childhood and adolescent and young adult (AYA) cancer

  • Sharon M. CastellinoEmail author
  • Kristen E. Allen
  • Katherine Pleasant
  • Graham Keyes
  • Katherine A. Poehling
  • Janet A. Tooze
Article
  • 115 Downloads

Abstract

Purpose

To estimate the population-based incidence of HPV vaccination after childhood cancer.

Methods

Pediatric and young adult cancer survivors identified in the institutional Comprehensive Cancer Center registry were linked to the North Carolina Immunization Registry (NCIR). Initiation and completion of any HPV vaccine was evaluated in survivors born between 1984 and 2002 with an NCIR record by December 2014. Descriptive statistics and Kaplan-Meier estimates of cumulative incidence were stratified by sex and age at eligibility for vaccine. Cox proportional hazards were conducted and stratified by sex.

Results

Among 879 (n = 428 female; n = 451 male) study-eligible cancer survivors without prior HPV vaccination (n = 501 < 18 years, n = 378 ≥ 18 years at the time of eligibility), the cumulative incidence of HPV vaccine initiation following cancer therapy was 48.1% among females at 8.2 years and 29.2% among males at 5.0 years after vaccine eligibility among those < 18 years, and 6.2% among females at 8.1 years and 2.0% among males at 4.2 years after vaccine eligibility among those ≥ 18 years. Among those who initiated vaccination, 53% of females and 43% of males completed a 3-dose series. Younger age at cancer diagnosis (≤ 10 and 11–14 years vs. ≥ 15 years) and shorter interval from diagnosis to vaccine eligibility were more likely to initiate vaccination in models adjusted for age at eligibility, race/ethnicity, cancer type, relapse, and transplant.

Conclusions

Despite the benefit of a cancer prevention strategy, cancer survivors are sub-optimally vaccinated against HPV.

Implications for Cancer Survivors

Immunization registries can help oncologists and primary care providers identify gaps in vaccination and target HPV vaccine delivery in survivors.

Keywords

Human papilloma virus (HPV) vaccine Childhood cancer Adolescent and young adult (AYA) cancer survivor Vaccine-preventable disease Immunization registry 

Notes

Acknowledgments

The authors would like to thank the Department of Emory Department of Pediatrics Grant and Manuscript Support Core.

Funding

Wake Forest Vaccine Center grant (Castellino); Biostatistics and Bioinformatics Shared Resource, Wake Forest Comprehensive Cancer Center , and NCI Cancer Center Support Grant (P30 CA012197).

Compliance with ethical standards

Conflict of interest

Dr. Castellino receives research funding from Bristol Meyers Squibb for an observational study not relevant to this work. Dr. Poehling received research funding for observational studies from the National Institutes of Health and MedImmune for an observational study not relevant to this work. The remaining authors declare they have no conflict of interest.

Compliance of ethical approval

All procedures performed in the study were in accordance with the ethical standards and approval of the Wake Forest School of Medicine institutional review board and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The IRB determined that the retrospective nature of this study using publicly available databases did not require individual informed consent.

Supplementary material

11764_2019_791_MOESM1_ESM.docx (1.5 mb)
ESM 1 (DOCX 1579 kb)

References

  1. 1.
    Meites E, Kempe A, Markowitz LE. 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;65:1405–8.CrossRefGoogle Scholar
  2. 2.
    Petrosky E, Bocchini JA, Hariri S, Chesson H, Curtis CR, Saraiya M, 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;64:300–4.PubMedPubMedCentralGoogle Scholar
  3. 3.
    Garland SM, Brotherton JML, Moscicki AB, Kaufmann AM, Stanley M, Bhatla N, et al. HPV vaccination of immunocompromised hosts. Papillomavirus Res. 2017 [cited 2018 May 10];4:35–8. Available from: http://linkinghub.elsevier.com/retrieve/pii/S2405852117300253.
  4. 4.
    Stobbe M. Vaccine panel gives nod to HPV shots for men up to age 26. Associated Press; 2019. Available from: https://www.apnews.com/e341072cbfa040369fd157bd255ed40a.
  5. 5.
    Walker TY, Elam-Evans LD, Singleton JA, Yankey D, Markowitz LE, Fredua B, et al. National, regional, state, and selected local area vaccination coverage among adolescents aged 13-17 years - United States, 2016. MMWR Morb Mortal Wkly Rep. 2017;66:874–82.CrossRefGoogle Scholar
  6. 6.
    Henderson TO, Nathan PC, Whitton J, Leisenring WM, Neglia JP, Fowler B, et al. Human papillomavirus (HPV)-associated malignancies as subsequent malignant neoplasms (SMN) in survivors of childhood cancer: a report from the Childhood Cancer Survivor Study (CCSS). 15th International Conference on Long-Term Complications of Treatment of Children and Adolescents for Cancer; 2017.Google Scholar
  7. 7.
    Oeffinger KC, Mertens AC, Sklar CA, Kawashima T, Hudson MM, Meadows AT, et al. Chronic health conditions in adult survivors of childhood cancer. N Engl J Med. 2006;355:1572–82.CrossRefGoogle Scholar
  8. 8.
    Ojha RP, Tota JE, Offutt-Powell TN, Klosky JL, Minniear TD, Jackson BE, et al. Human papillomavirus-associated subsequent malignancies among long-term survivors of pediatric and young adult cancers. PLoS One. 2013;8:e70349.CrossRefGoogle Scholar
  9. 9.
    Meadows AT, Friedman DL, Neglia JP, Mertens AC, Donaldson SS, Stovall M, et al. Second neoplasms in survivors of childhood cancer: findings from the Childhood Cancer Survivor Study cohort. J Clin Oncol Off J Am Soc Clin Oncol. 2009;27:2356–62.CrossRefGoogle Scholar
  10. 10.
    Temkin SM, Seibel NL. Are we missing an opportunity for cancer prevention? Human papillomavirus vaccination for survivors of pediatric and young adult cancers: HPV Vaccines and Childhood Cancer Survivors. Cancer. 2015 [cited 2018 Mar 29];121:3395–402. Available from: http://doi.wiley.com/10.1002/cncr.29515.
  11. 11.
    Children’s Oncology Group. Long-term follow-up guidelines for survivors of childhood, adolescent, and young adult cancers, Version 4.0. Monrovia, CA; 2013. Available from: http://www.survivorshipguidelines.org/pdf/LTFUGuidelines_40.pdf.
  12. 12.
    Smith RA, Brooks D, Cokkinides V, Saslow D, Brawley OW. Cancer screening in the United States, 2013: a review of current American Cancer Society guidelines, current issues in cancer screening, and new guidance on cervical cancer screening and lung can. CA Cancer J Clin. 2013;63:87–105.CrossRefGoogle Scholar
  13. 13.
    National Comprehensive Cancer Network. Cervical Cancer. National Comprehensive Cancer Network Clinical Practice Guideline V3. 2013 [cited 2018 Jun 18]. Available from: www.nccn.org.
  14. 14.
    Hoffman L, Okcu MF, Dreyer ZE, Suzawa H, Bryant R, Middleman AB. Human papillomavirus vaccination in female pediatric cancer survivors. J Pediatr Adolesc Gynecol. 2012 [cited 2018 Mar 29];25:305–7. Available from: http://linkinghub.elsevier.com/retrieve/pii/S1083318812000873.
  15. 15.
    Klosky JL, Russell KM, Canavera KE, Gammel HL, Hodges JR, Foster RH, et al. Risk factors for non-initiation of the human papillomavirus vaccine among adolescent survivors of childhood cancer. Cancer Prev Res (Phila Pa). 2013 [cited 2018 Mar 29];6:1101–10. Available from: http://cancerpreventionresearch.aacrjournals.org/cgi/doi/10.1158/1940-6207.CAPR-13-0127.
  16. 16.
    Klosky JL, Hudson MM, Chen Y, Connelly JA, Wasilewski-Masker K, Sun C-L, et al. Human papillomavirus vaccination rates in young cancer survivors. J Clin Oncol. 2017 [cited 2018 Mar 29];35:3582–90. Available from: http://ascopubs.org/doi/10.1200/JCO.2017.74.1843.
  17. 17.
    Recommended Immunization Schedule for Children and Adolescents Aged 18 Years or Younger, United States, 2018. Centers for Disease Control and Prevention; 2018. Available from: https://www.cdc.gov/vaccines/schedules/hcp/imz/child-adolescent.html.
  18. 18.
    Recommended Immunization Schedule for Adults Aged 19 Years or Older, United States, 2018. Centers for Disease Control and Prevention; 2018 [cited 2018 Mar 29]. Available from: https://www.cdc.gov/vaccines/schedules/downloads/adult/adult-combined-schedule.pdf.
  19. 19.
    Rubin LG, Levin MJ, Ljungman P, Davies EG, Avery R, Tomblyn M, et al. Executive summary: 2013 IDSA clinical practice guideline for vaccination of the immunocompromised host. Clin Infect Dis. 2014 [cited 2019 Jul 10];58:309–18. Available from: https://academic.oup.com/cid/article-lookup/doi/10.1093/cid/cit816.
  20. 20.
    Nathan PC, Greenberg ML, Ness KK, Hudson MM, Mertens AC, Mahoney MC, et al. Medical care in long-term survivors of childhood cancer: a report from the childhood cancer survivor study. J Clin Oncol Off J Am Soc Clin Oncol. 2008;26:4401–9.CrossRefGoogle Scholar
  21. 21.
    Kirchhoff AC, Mann K, Warner EL, Kaddas HK, Fair D, Fluchel M, et al. HPV vaccination knowledge, intentions, and practices among caregivers of childhood cancer survivors. Hum Vaccines Immunother. 2019 [cited 2019 Jul 10];1–9. Available from: https://www.tandfonline.com/doi/full/10.1080/21645515.2019.1619407.
  22. 22.
    Dayton A. Improving quality of health care using the North Carolina Immunization Registry. N C Med J. 2014 [cited 2019 Apr 1];75:198–203. Available from: http://www.ncmedicaljournal.com/lookup/doi/10.18043/ncm.75.3.198.
  23. 23.
    VFC Eligibility Criteria. Centers for Disease Control and Prevention; 2014 [cited 2019 Apr 1]. Available from: https://www.cdc.gov/vaccines/programs/vfc/providers/eligibility.html.
  24. 24.
    Trogdon JG, Shafer P, Lindsay B, Coyne-Beasley T. Impact of introduction of the 9-valent human papillomavirus vaccine on vaccination coverage of youth in North Carolina. Vaccine. 2018;36:1304–9.CrossRefGoogle Scholar
  25. 25.
    Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009 [cited 2018 Apr 26];42:377–81. Available from: http://linkinghub.elsevier.com/retrieve/pii/S1532046408001226.
  26. 26.
    Klosky JL, Gamble HL, Spunt SL, Randolph ME, Green DM, Hudson MM. Human papillomavirus vaccination in survivors of childhood cancer. Cancer. 2009 [cited 2018 Mar 29];115:5627–36. Available from: http://doi.wiley.com/10.1002/cncr.24669.
  27. 27.
    Centers for Disease Control and Prevention (CDC). National and state vaccination coverage among adolescents aged 13–17 years--United States, 2012. MMWR Morb Mortal Wkly Rep. 2013;62:685–93.Google Scholar
  28. 28.
    Elam-Evans LD, Yankey D, Jeyarajah J, Singleton JA, Curtis RC, MacNeil J, et al. National, regional, state, and selected local area vaccination coverage among adolescents aged 13-17 years--United States, 2013. MMWR Morb Mortal Wkly Rep. 2014;63:625–33.PubMedPubMedCentralGoogle Scholar
  29. 29.
    Reagan-Steiner S, Yankey D, Jeyarajah J, Elam-Evans LD, Curtis CR, MacNeil 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;65:850–8.CrossRefGoogle Scholar
  30. 30.
    Reagan-Steiner S, Yankey D, Jeyarajah J, Elam-Evans LD, Singleton JA, Curtis CR, 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;64:784–92.CrossRefGoogle Scholar
  31. 31.
    National Health Interview Survey. Centers for Disease Control and Prevention; 2018 [cited 2018 Mar 29]. Available from: https://www.cdc.gov/nchs/nhis/data-questionnaires-documentation.htm.
  32. 32.
    Williams WW, Lu P-J, O’Halloran A, Kim DK, Grohskopf LA, Pilishvili T, et al. Surveillance of vaccination coverage among adult populations — United States, 2014. MMWR Surveill Summ. 2016 [cited 2018 Mar 29];65:1–36. Available from: http://www.cdc.gov/mmwr/volumes/65/ss/ss6501a1.htm.
  33. 33.
    Williams WW, Lu P-J, O’Halloran A, Kim DK, Grohskopf LA, Pilishvili T, et al. Surveillance of vaccination coverage among adult populations - United States, 2015. Morb Mortal Wkly Rep Surveill Summ Wash DC 2002. 2017;66:1–28.Google Scholar
  34. 34.
    Williams WW, Lu P-J, O’Halloran A, Bridges CB, Pilishvili T, Hales CM, et al. Noninfluenza vaccination coverage among adults - United States, 2012. MMWR Morb Mortal Wkly Rep. 2014;63:95–102.PubMedPubMedCentralGoogle Scholar
  35. 35.
    Williams WW, Lu P-J, O’Halloran A, Bridges CB, Kim DK, Pilishvili T, et al. Vaccination coverage among adults, excluding influenza vaccination - United States, 2013. MMWR Morb Mortal Wkly Rep. 2015;64:95–102.PubMedPubMedCentralGoogle Scholar
  36. 36.
    Martin DW, Lowery NE, Brand B, Gold R, Horlick G. Immunization information systems: a decade of progress in law and policy. J Public Health Manag Pract JPHMP. 2015;21:296–303.CrossRefGoogle Scholar
  37. 37.
    North Carolina Immunization Program (NCIP) Requirements. North Carolina Department of Health and Human Services; 2018 [cited 2018 Apr 19]. Available from: http://www.immunize.nc.gov/providers/vpdreporting.htm.
  38. 38.
    Centers for Disease Control and Prevention (CDC). Immunization information systems progress--United States, 2006. MMWR Morb Mortal Wkly Rep. 2008;57:289–91.Google Scholar
  39. 39.
    The North Carolina Immunization Registry. North Carolina Department of Health and Human Services; 2017 [cited 2018 Mar 29]. Available from: http://www.immunize.nc.gov/providers/ncir.htm.
  40. 40.
    Groom H, Hopkins DP, Pabst LJ, Murphy Morgan J, Patel M, Calonge N, et al. Immunization information systems to increase vaccination rates: a community guide systematic review. J Public Health Manag Pract JPHMP. 2015;21:227–48.CrossRefGoogle Scholar
  41. 41.
    Choi N, Curtis CR, Loharikar A, Fricchione M, Jones E, Balzer E, et al. Successful use of interventions in combination to improve human papillomavirus vaccination coverage rates among adolescents—Chicago, 2013 to 2015. Acad Pediatr. 2018 [cited 2018 Jul 11];18:S93–100. Available from: http://linkinghub.elsevier.com/retrieve/pii/S1876285917304965.
  42. 42.
    Farmar A-LM, Love-Osborne K, Chichester K, Breslin K, Bronkan K, Hambidge SJ. Achieving high adolescent HPV vaccination coverage. Pediatrics. 2016;138:e20152653.CrossRefGoogle Scholar
  43. 43.
    Rosenthal SL, Weiss TW, Zimet GD, Ma L, Good MB, Vichnin MD. Predictors of HPV vaccine uptake among women aged 19-26: importance of a physician’s recommendation. Vaccine. 2011;29:890–5.CrossRefGoogle Scholar
  44. 44.
    Wagner AL, Shrivastwa N, Potter RC, Lyon-Callo SK, Boulton ML. Pneumococcal and meningococcal vaccination among Michigan children with sickle cell disease. J Pediatr. 2018.Google Scholar
  45. 45.
    Berenson AB, Rupp R, Dinehart EE, Cofie LE, Kuo Y-F, Hirth JM. Achieving high HPV vaccine completion rates in a pediatric clinic population. Hum Vaccines Immunother. 2018;1–8.Google Scholar
  46. 46.
    Holman DM, Benard V, Roland KB, Watson M, Liddon N, Stokley S. Barriers to human papillomavirus vaccination among US adolescents: a systematic review of the literature. JAMA Pediatr. 2014;168:76–82.CrossRefGoogle Scholar
  47. 47.
    Dorell C, Yankey D, Kennedy A, Stokley S. Factors that influence parental vaccination decisions for adolescents, 13 to 17 years old: National Immunization Survey-Teen, 2010. Clin Pediatr (Phila). 2013;52:162–70.CrossRefGoogle Scholar
  48. 48.
    Kester LM, Zimet GD, Fortenberry JD, Kahn JA, Shew ML. A national study of HPV vaccination of adolescent girls: rates, predictors, and reasons for non-vaccination. Matern Child Health J. 2013;17:879–85.CrossRefGoogle Scholar
  49. 49.
    Clark SJ, Cowan AE, Filipp SL, Fisher AM, Stokley S. Parent perception of provider interactions influences HPV vaccination status of adolescent females. Clin Pediatr (Phila). 2016;55:701–6.CrossRefGoogle Scholar
  50. 50.
    Perkins RB, Clark JA, Apte G, Vercruysse JL, Sumner JJ, Wall-Haas CL, et al. Missed opportunities for HPV vaccination in adolescent girls: a qualitative study. Pediatrics. 2014;134:e666–74.CrossRefGoogle Scholar
  51. 51.
    Markowitz L. HPV Vaccines. Atlanta, GA; 2018. Available from: https://www.cdc.gov/vaccines/acip/meetings/live-mtg-2018-06.html.
  52. 52.
    Choi N, Curtis CR, Loharikar A, Fricchione M, Jones E, Balzer E, et al. Successful use of interventions in combination to improve human papillomavirus vaccination coverage rates among adolescents—Chicago, 2013 to 2015. Acad Pediatr. 2018;18:S93–100.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Sharon M. Castellino
    • 1
    • 2
    Email author
  • Kristen E. Allen
    • 2
  • Katherine Pleasant
    • 3
  • Graham Keyes
    • 1
  • Katherine A. Poehling
    • 1
    • 3
  • Janet A. Tooze
    • 3
    • 4
  1. 1.Department of PediatricsWake Forest School of MedicineWinston-SalemUSA
  2. 2.Department of Pediatrics – Hematology/Oncology, Emory University School of Medicine; The Aflac Cancer and Blood Disorders CenterChildren’s Healthcare of AtlantaAtlantaUSA
  3. 3.Division of Public Health SciencesWake Forest School of MedicineWinston-SalemUSA
  4. 4.Wake Forest Comprehensive Cancer CenterWake Forest School of MedicineWinston-SalemUSA

Personalised recommendations