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Association of Maternal Cervical Cancer Screening Adherence with Adolescent HPV Vaccination Among Adolescent-Mother Pairs

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Abstract

Less than two-thirds of US adolescents are up-to-date with HPV vaccination. While mothers engaged in preventive care are more likely to seek preventive care for their children, current studies on associations between maternal cervical cancer screening (CCS) and adolescent HPV vaccination are needed. We assessed associations between maternal preventive service utilization and adolescent HPV vaccination using electronic health record data from a healthcare system in Washington State. We included adolescents (11–17 years) and their mothers with ≥ 1 primary care visit between 2018 and 2020. Outcomes were HPV vaccine initiation and completion. The primary exposure was maternal adherence to guideline-recommended CCS. Secondary exposures were maternal breast cancer screening adherence (for mothers ≥ 52 years) and ≥ 1 wellness visit ≤ 2 years. We used Generalized Estimating Equations to estimate prevalence ratios, and explore effect modification by adolescent sex, adolescent provider characteristics, and maternal language interpreter use. Of 4121 adolescents, 66% had a CCS-adherent mother, 82% initiated HPV vaccination, and 49% completed the series. CCS adherence was associated with higher initiation (adjusted prevalence ratio (APR):1.10, 95%CI:1.06–1.13) and completion (APR:1.16, 95%CI:1.08–1.23). Associations were stronger for male vs. female adolescents, adolescents who had a primary care provider in family practice vs. pediatrics, and adolescents who had the same primary care provider as their mother vs. not. Recent maternal wellness visit was also associated with higher initiation (APR:1.04, 95%CI:1.01–1.07) and completion (APR:1.12, 95%CI:1.05–1.20). Results suggest that delivering healthcare through a family-centered approach and engaging mothers in broad preventive care could increase adolescent HPV vaccination coverage.

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Deidentified data will be made available to researchers whose proposed use of the data has been approved for a specified purpose, with a signed data access agreement. Deidentified data will be made available without investigator support to researchers with adequate resources to cover the regulatory and data sharing costs.

References

  1. Bogani, G., Serati, M., Maggiore, U. L. R., Ditto, A., Gardella, B., Ferrero, S., & Raspagliesi, F. (2019). Cervical intraepithelial neoplasia in women who had vaccination against HPV. International Journal of Gynecology and Obstetrics, 147(2), 233–237. https://doi.org/10.1002/ijgo.12934.

    Article  CAS  PubMed  Google Scholar 

  2. Chen, S. T., Huybrechts, K. F., Bateman, B. T., & Hernández-Díaz, S. (2020). Trends in human papillomavirus vaccination in commercially insured children in the United States. Pediatrics, 146(4), e20193557. https://doi.org/10.1542/peds.2019-3557

    Article  PubMed  Google Scholar 

  3. Smith, R. A., Andrews, K. S., Brooks, D., Fedewa, S. A., Manassaram-Baptiste, D., Saslow, D., & Wender, R. C. (2019). Cancer screening in the United States, 2019: A review of current American Cancer Society guidelines and current issues in cancer screening. CA: A Cancer Journal for Clinicians, 69(3), 184–210. https://doi.org/10.3322/caac.21557.

    Article  PubMed  Google Scholar 

  4. Senkomago, V., Henley, S., Jane, Thomas, C. C., Mix, J. M., Markowitz, L. E., & Saraiya, M. (n.d.). Morbidity and Mortality weekly report human papillomavirus-attributable Cancers-United States, 2012–2016. Retrieved from https://www.cdc.gov/cancer/uscs.

  5. Centers for Disease Control and Prevention (2020). Vaccines and Preventable Diseases: Administering HPV Vaccine, 1–2.

  6. World Health Organisation. (2020). Global strategy to accelerate the elimination of cervical cancer as a public health problem and its associated goals and targets for the period 2020–2030 (Vol. 2). United Nations General Assembly.

    Google Scholar 

  7. Office of Disease Prevention and Health Promotion. (n.d.). (n.d.). Healthy people 2030. U.S. Department of Health and Human Services.

  8. Pingali, C., Yankey, D., Elam-Evans, L. D., Markowitz, L. E., Valier, M. R., Fredua, B., & Singleton, J. A. (2023). Morbidity and mortality weekly report vaccination coverage among adolescents aged 13–17 Years-National Immunization Survey-Teen, United States, 2022. Centers for Disease Control and Prevention | MMWR (Vol. 72). Retrieved from https://www.cdc.gov/vaccines/imz-managers/nis/downloads/NIS-TEEN.

  9. Walker, T. Y., Elam-Evans, L. D., Williams, C. L., Fredua, B., Yankey, D., Markowitz, L. E., & Stokley, S. (2020). Trends in human papillomavirus (HPV) vaccination initiation among adolescents aged 13–17 by metropolitan statistical area (MSA) status, National Immunization Survey–Teen, 2013–2017. Human Vaccines and Immunotherapeutics, 16(3), 554–561. https://doi.org/10.1080/21645515.2019.1671765.

    Article  PubMed  Google Scholar 

  10. Agrawal, S., & Morain, S. R. (2018). Who calls the shots? The ethics of adolescent self-consent for HPV vaccination. Journal of Medical Ethics, 44(8), 531–535. https://doi.org/10.1136/medethics-2017-104694.

    Article  PubMed  Google Scholar 

  11. Nguyen, K. H., Santibanez, T. A., Stokley, S., Lindley, M. C., Fisher, A., Kim, D., & Singleton, J. (2021). Parental vaccine hesitancy and its association with adolescent HPV vaccination. Vaccine, 39(17), 2416–2423. https://doi.org/10.1016/j.vaccine.2021.03.048.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Markovitz, A. R., Song, J. Y., Paustian, M. L., & Reda, E., D. K (2014). Association between maternal preventive care utilization and adolescent vaccination: It’s not just about pap testing. Journal of Pediatric and Adolescent Gynecology, 27(1), 29–36. https://doi.org/10.1016/j.jpag.2013.08.012.

    Article  PubMed  Google Scholar 

  13. Lefevere, E., Hens, N., Theeten, H., Van Den Bosch, K., Beutels, P., De Smet, F., & Van Damme, P. (2011). Like mother, like daughter? Mother’s history of cervical cancer screening and daughter’s Human Papillomavirus vaccine uptake in Flanders (Belgium). Vaccine. https://doi.org/10.1016/j.vaccine.2011.08.039

    Article  PubMed  Google Scholar 

  14. Chao, C., Slezak, J. M., Coleman, K. J., & Jacobsen, S. J. (2009). Papanicolaou screening behavior in mothers and human papillomavirus vaccine uptake in adolescent girls. American Journal of Public Health, 99(6), 1137–1142. https://doi.org/10.2105/AJPH.2008.147876.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Lutringer-Magnin, D., Cropet, C., Barone, G., Canat, G., Kalecinski, J., Leocmach, Y., & Lasset, C. (2013). HPV vaccination among French girls and women aged 14–23 years and the relationship with their mothers’ uptake of pap smear screening: A study in general practice. Vaccine, 31(45), 5243–5249. https://doi.org/10.1016/j.vaccine.2013.08.068.

    Article  CAS  PubMed  Google Scholar 

  16. Sander, B. B., Vázquez Prada, M., Rebolj, M., Lynge, E., & Branth, V., P (2015). Mothers’ and their daughters’ use of preventive measures against cervical cancer. Scandinavian Journal of Public Health, 43(4), 415–422. https://doi.org/10.1177/1403494815574155.

    Article  PubMed  Google Scholar 

  17. Spencer, A. M., Brabin, L., Verma, A., & Roberts, S. A. (2013). Mothers’ screening histories influence daughters’ vaccination uptake: An analysis of linked cervical screening and human papillomavirus vaccination records in the North West of England. European Journal of Cancer, 49(6), 1264–1272. https://doi.org/10.1016/j.ejca.2012.12.001.

    Article  Google Scholar 

  18. UW Medicine (2021). Fact Book 2021. Retrieved from https://www.uwmedicine.org/sites/stevie/files/2021-04/Fact-Book-03-20201.pdf.

  19. Hechter, R. C., Chao, C., Sy, L. S., Ackerson, B. K., Slezak, J. M., Sidell, M. A., & Jacobsen, S. J. (2013). Quadrivalent human papillomavirus vaccine uptake in adolescent boys and maternal utilization of preventive care and history of sexually transmitted infections. American Journal of Public Health, 103(9), 63–68. https://doi.org/10.2105/AJPH.2013.301495.

    Article  Google Scholar 

  20. Saslow, D., Solomon, D., Lawson, H. W., Killackey, M., Kulasingam, S. L., Cain, J., & Myers, E. R. (2012). 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: A Cancer Journal for Clinicians, 62(3), 147–172. https://doi.org/10.3322/caac.21139

    Article  PubMed  Google Scholar 

  21. Preventive, U. S., Task, S., & Cancer, A. (n.d.). Breast cancer screening guidelines for women some organizations release different breast cancer screening guidelines for women who are considered to be at high risk of developing breast cancer. Different, 2–4.

  22. CDC SVI (2018 Documentation). (n.d.). Retrieved from https://www.census.gov/programs-surveys/acs/technical.

  23. Venturelli, F., Baldacchini, F., Campari, C., Perilli, C., Pascucci, M. G., Finarelli, A. C., Moscara, L., & Rossi, P. G. (2017). Association between mothers ’ screening uptake and daughters ’ HPV vaccination : a quasi-experimental study on the effect of an active invitation campaign. BMJ Open. https://doi.org/10.1136/bmjopen-2017-016189

    Article  PubMed  PubMed Central  Google Scholar 

  24. Monnat, S. M., & Wallington, S. F. (2013). Is there an association between maternal pap test use and adolescent human papillomavirus vaccination? Journal of Adolescent Health, 52(2), 212–218. https://doi.org/10.1016/j.jadohealth.2012.05.015.

    Article  Google Scholar 

  25. Labeit, A. M., & Peinemann, F. (2017). Determinants of a GP visit and cervical cancer screening examination in Great Britain. PLos One. https://doi.org/10.1371/journal.pone.0174363

    Article  PubMed  PubMed Central  Google Scholar 

  26. Tinsley, B. J. (1992). Multiple Influences on the acquisition and socialization of children’s health attitudes and behavior: An Integrative Review. Child Development. https://doi.org/10.1111/j.1467-8624.1992.tb01680.x

    Article  PubMed  Google Scholar 

  27. Bowung, A. (1389). Implications of preventive health behaviour for cervical and breast cancer screening programmes: A review (Vol. 6). Retrieved from https://academic.oup.com/fampra/article/6/3/224/426954.

  28. Razuka-Ebela, D., Zile, I., Tzivian, L., Ebela, I., Polaka, I., Parshutin, S., & Leja, M. (2020). Does family history of cancer influence undergoing screening and gastrointestinal investigations? Journal of gastrointestinal and liver diseases: JGLD, 29(4), 523–528.

    PubMed  Google Scholar 

  29. Deguara, M., Calleja, N., & England, K. (2021). Cervical cancer and screening: Knowledge, awareness and attitudes of women in Malta. Journal of Preventive Medicine and Hygiene, 61(4), E584–E592. https://doi.org/10.15167/2421-4248/jpmh2020.61.4.1521.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Tong, S. T., Webel, B. K., Donahue, E. E., Richards, A., Sabo, R. T., Brooks, E. M., & Krist, A. H. (2021). Understanding the value of the wellness visit: A descriptive study. American Journal of Preventive Medicine, 61(4), 591–595. https://doi.org/10.1016/j.amepre.2021.02.023

    Article  PubMed  PubMed Central  Google Scholar 

  31. McMurry, T. L., Lobo, J. M., Kang, H., Kim, S., Balkrishnan, R., Anderson, R., & Sohn, M.-W. (2022). Annual wellness visits are associated with increased use of preventive services in patients with diabetes living in the diabetes belt. Diabetes Epidemiology and Management. https://doi.org/10.1016/j.deman.2022.100094

    Article  PubMed  PubMed Central  Google Scholar 

  32. Fontham, E. T. H., Wolf, A. M. D., Church, T. R., Etzioni, R., Flowers, C. R., Herzig, A., & Smith, R. A. (2020). Cervical cancer screening for individuals at average risk: 2020 guideline update from the American Cancer Society. CA: A Cancer Journal for Clinicians, 70(5), 321–346. https://doi.org/10.3322/caac.21628

    Article  PubMed  Google Scholar 

  33. Smith, P. J., Stokley, S., Bednarczyk, R. A., Orenstein, W. A., & Omer, S. B. (2016). HPV vaccination coverage of teen girls: The influence of health care providers. Vaccine, 34(13), 1604–1610. https://doi.org/10.1016/j.vaccine.2016.01.061.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Markowitz, L. E., Dunne, E. F., Saraiya, M., Lawson, H. W., Chesson, H., & Unger, E. R. (2007). Quadrivalent Human Papillomavirus Vaccine Recommendations of the Advisory Committee on Immunization Practices (ACIP).

  35. Lindley, M. C., Jeyarajah, J., Yankey, D., Curtis, C. R., Markowitz, L. E., & Stokley, S. (2016). Comparing human papillomavirus vaccine knowledge and intentions among parents of boys and girls. Human Vaccines and Immunotherapeutics, 12(6), 1519–1527. https://doi.org/10.1080/21645515.2016.1157673.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Kempe, A., O’Leary, S. T., Markowitz, L. E., Crane, L. A., Hurley, L. P., Brtnikova, M., & Lindley, M. C. (2019). HPV vaccine delivery practices by primary care physicians. Pediatrics. https://doi.org/10.1542/peds.2019-1475

    Article  PubMed  Google Scholar 

  37. Lindsay, A. C., Delgado, D., Valdez, M. J., Restrepo, E., & Guzman, Y. M. (2022). I don’t think he needs the HPV Vaccine cause boys can’t have cervical Cancer: A qualitative study of Latina Mothers’ (mis) understandings about human papillomavirus transmission, Associated Cancers, and the vaccine. Journal of Cancer Education, 37(2), 370–378. https://doi.org/10.1007/s13187-020-01824-z.

    Article  PubMed  Google Scholar 

  38. Millar, M. M., Edwards, S. L., Herget, K. A., Orleans, B., Ofori-Atta, B. S., Kirchhoff, A. C., Nagala, M., & Sweeney, C. (2022). Adherence to guideline-recommended cancer screening among Utah cancer survivors. Cancer Medicine. https://doi.org/10.1002/cam4.5168

    Article  PubMed  PubMed Central  Google Scholar 

  39. Van Til, L., MacQuarrie, C., & Herbert, R. (2003). Understanding the barriers to cervical cancer screening among older women. Qualitative Health Research, 13(8), 1116–1131. https://doi.org/10.1177/1049732303255975.

    Article  PubMed  Google Scholar 

  40. McCauley, L., Phillips, R. L., Meisnere, M., & Robinson, S. K. (2021). Implementing high-quality primary care: Rebuilding the foundation of health care. National Academies Press.

    Book  Google Scholar 

  41. Cataldi, J. R., O’Leary, S. T., Markowitz, L. E., Allison, M. A., Crane, L. A., Hurley, L. P., Brtnikova, M., Beaty, B. L., Gorman, C., Meites, E., Lindley, M. C., & Kempe, A. (2021). Changes in strength of recommendation and perceived barriers to human papillomavirus vaccination: Longitudinal analysis of primary care physicians, 2008–2018. Journal of Pediatrics, 234, 149-157.e3. https://doi.org/10.1016/j.jpeds.2021.03.002

    Article  PubMed  Google Scholar 

  42. Pingali, C., Yankey, D., Elam-Evans, L. D., Markowitz, L. E., Valier, M. R., Fredua, B. Singleton, J. A. (2021). Morbidity and Mortality Weekly Report National Vaccination Coverage Among Adolescents Aged 13-17 Years-National Immunization Survey-Teen, United States, 2021. Retrieved from https://www.cdc.gov/mmwr/volumes/72/wr/pdfs/mm7234a3-H.pdf

  43. Smulian, E. A., Mitchell, K. R., & Stokley, S. (2016). Interventions to increase HPV vaccination coverage: A systematic review Human Vaccines and Immunotherapeutics. Taylor and Francis Inc.

    Google Scholar 

  44. Bumatay, S., Dickinson, C., Larsen, R., Stock, I., Day, M. R., Hatch, B., & Carney, P. A. (2023). A comparison of electronic health records and the Oregon state immunization registry for human papilloma virus vaccine delivery (2005–2022). Vaccine. https://doi.org/10.1016/j.vaccine.2023.08.017

    Article  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Dr. M. Rebecca O’Connor in the School of Nursing at the University of Washington, for her dedication and commitment to monitoring the integrity and quality of the research process.

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The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

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Authors and Affiliations

  1. Department of Epidemiology, University of Washington School of Public Health, 3980 15th Ave NE, UW Box # 351619, Seattle, WA, 98195, USA

    Adino Tesfahun Tsegaye, John Lin & Rachel L. Winer

  2. Department of Family Medicine, University of Washington School of Medicine, Seattle, USA

    Allison Cole

  3. Department of Biostatistics, University of Washington School of Public Health, Seattle, USA

    Adam A Szpiro

  4. Gender Equality Division, Bill & Melinda Gates Foundation, Seattle, USA

    Darcy W. Rao

  5. Departments of Global Health, Medicine (Infectious Diseases), Pediatrics and Epidemiology, University of Washington, Seattle, USA

    Judd Walson

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  1. Adino Tesfahun Tsegaye
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Correspondence to Adino Tesfahun Tsegaye.

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Tsegaye, A.T., Lin, J., Cole, A. et al. Association of Maternal Cervical Cancer Screening Adherence with Adolescent HPV Vaccination Among Adolescent-Mother Pairs. J Community Health (2024). https://doi.org/10.1007/s10900-024-01333-w

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