Cancer Causes & Control

, Volume 29, Issue 6, pp 551–561 | Cite as

Sociodemographic disparities in the occurrence of medical conditions among adolescent and young adult Hodgkin lymphoma survivors

  • Theresa H. M. Keegan
  • Qian Li
  • Amy Steele
  • Elysia M. Alvarez
  • Ann Brunson
  • Christopher R. Flowers
  • Sally L. Glaser
  • Ted Wun
Original paper



Hodgkin lymphoma (HL) survivors experience high risks of second cancers and cardiovascular disease, but no studies have considered whether the occurrence of these and other medical conditions differ by sociodemographic factors in adolescent and young adult (AYA) survivors.


Data for 5,085 patients aged 15–39 when diagnosed with HL during 1996–2012 and surviving ≥ 2 years were obtained from the California Cancer Registry and linked to hospitalization data. We examined the impact of race/ethnicity, neighborhood socioeconomic status (SES), and health insurance on the occurrence of medical conditions (≥ 2 years after diagnosis) and the impact of medical conditions on survival using multivariable Cox proportional hazards regression.


Twenty-six percent of AYAs experienced at least one medical condition and 15% had ≥ 2 medical conditions after treatment for HL. In multivariable analyses, Black HL survivors had a higher likelihood (vs. non-Hispanic Whites) of endocrine [hazard ratio (HR) = 1.37, 95% confidence interval (CI) 1.05–1.78] and circulatory system diseases (HR = 1.58, CI 1.17–2.14); Hispanics had a higher likelihood of endocrine diseases [HR = 1.24 (1.04–1.48)]. AYAs with public or no insurance (vs. private/military) had higher likelihood of circulatory system diseases, respiratory system diseases, chronic kidney disease/renal failure, liver disease, and endocrine diseases. AYAs residing in low SES neighborhoods (vs. high) had higher likelihood of respiratory system and endocrine diseases. AYAs with these medical conditions or second cancers had an over twofold increased risk of death.


Strategies to improve health care utilization for surveillance and secondary prevention among AYA HL survivors at increased risk of medical conditions may improve outcomes.


Hodgkin lymphoma Insurance Adolescent Young adult Race/ethnicity Second cancer Circulatory system Respiratory system Endocrine system 



This work was supported by the Rich and Weissman Family Lymphoma and Survivorship Fund St. Baldrick’s Research Grant. In addition, Dr. Flowers’ effort was supported by the National Cancer Institute U01CA195568 and K24CA208132, and Dr. Wun’s effort also supported by the National Center for Advancing Translational Sciences TR000002. The collection of cancer incidence data used in this study was supported by the California Department of Public Health as part of the statewide cancer reporting program mandated by California Health and Safety Code Section103885; the National Cancer Institute’s Surveillance, Epidemiology and End Results Program under contract HHSN261201000140C awarded to the Cancer Prevention Institute of California, contract HHSN261201000035C awarded to the University of Southern California, and contract HHSN261201000034C awarded to the Public Health Institute; and the Centers for Disease Control and Prevention’s National Program of Cancer Registries, under agreement U58DP003862-01 awarded to the California Department of Public Health. The ideas and opinions expressed herein are those of the author(s) and endorsement by the State of California, Department of Public Health the National Cancer Institute, and the Centers for Disease Control and Prevention or their Contractors and Subcontractors is not intended nor should be inferred.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. For this type of study formal consent is not required.

Supplementary material

10552_2018_1025_MOESM1_ESM.docx (22 kb)
Supplementary material 1 (DOCX 22 KB)


  1. 1.
    Nass SJ, Beaupin LK, Demark-Wahnefried W, Fasciano K, Ganz PA, Hayes-Lattin B, Hudson MM, Nevidjon B, Oeffinger KC, Rechis R, Richardson LC, Seibel NL, Smith AW (2015) Identifying and addressing the needs of adolescents and young adults with cancer: summary of an Institute of Medicine workshop. Oncologist 20(2):186–195. CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Tai E, Buchanan N, Townsend J, Fairley T, Moore A, Richardson LC (2012) Health status of adolescent and young adult cancer survivors. Cancer 118(19):4884–4891. CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Kaul S, Veeranki SP, Rodriguez AM, Kuo YF (2016) Cigarette smoking, comorbidity, and general health among survivors of adolescent and young adult cancer. Cancer. Google Scholar
  4. 4.
    Chao C, Xu L, Bhatia S, Cooper R, Brar S, Wong FL, Armenian SH (2016) Cardiovascular disease risk profiles in survivors of adolescent and young adult (AYA) cancer: the Kaiser permanente AYA cancer survivors study. J Clin Oncol. Google Scholar
  5. 5.
    Howlader N, Noone AM, Krapcho M, Garshell J, Miller D, Altekruse SF, Kosery CL, Yu M, Ruhl J, Tatalovich Z, Cho H, Mariotto A, Lewis DR, Chen HS, Feuer EJ, Cronin KA (eds) (2015) SEER Cancer Statistics Review, 1975–2012., based on November 2014 SEER data submission, posted to the SEER web site, April 2015 edn. National Cancer Institute, Bethesda, MD
  6. 6.
    Keegan TH, DeRouen MC, Parsons HM, Clarke CA, Goldberg D, Flowers CR, Glaser SL (2016) Impact of treatment and insurance on socioeconomic disparities in survival after adolescent and young adult Hodgkin lymphoma: a population-based study. Cancer Epidemiol Biomarkers Prev 25(2):264–273. CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    van Nimwegen FA, Schaapveld M, Janus CP, Krol AD, Petersen EJ, Raemaekers JM, Kok WE, Aleman BM, van Leeuwen FE (2015) Cardiovascular disease after Hodgkin lymphoma treatment: 40-year disease risk. JAMA Intern Med 175(6):1007–1017. CrossRefPubMedGoogle Scholar
  8. 8.
    Hodgson DC (2011) Late effects in the era of modern therapy for Hodgkin lymphoma. Hematol Am Soc Hematol Educ Progr 2011:323–329. Google Scholar
  9. 9.
    Ng AK (2014) Current survivorship recommendations for patients with Hodgkin lymphoma: focus on late effects. Blood 124(23):3373–3379. CrossRefPubMedGoogle Scholar
  10. 10.
    Ng AK (2011) Review of the cardiac long-term effects of therapy for Hodgkin lymphoma. Br J Haematol 154(1):23–31. CrossRefPubMedGoogle Scholar
  11. 11.
    Castellino SM, Geiger AM, Mertens AC, Leisenring WM, Tooze JA, Goodman P, Stovall M, Robison LL, Hudson MM (2011) Morbidity and mortality in long-term survivors of Hodgkin lymphoma: a report from the Childhood Cancer Survivor Study. Blood 117(6):1806–1816. CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Matasar MJ, Ford JS, Riedel ER, Salz T, Oeffinger KC, Straus DJ (2015) Late morbidity and mortality in patients with Hodgkin’s lymphoma treated during adulthood. J Natl Cancer Inst. PubMedGoogle Scholar
  13. 13.
    Schaapveld M, Aleman BM, van Eggermond AM, Janus CP, Krol AD, van der Maazen RW, Roesink J, Raemaekers JM, de Boer JP, Zijlstra JM, van Imhoff GW, Petersen EJ, Poortmans PM, Beijert M, Lybeert ML, Mulder I, Visser O, Louwman MW, Krul IM, Lugtenburg PJ, van Leeuwen FE (2015) Second cancer risk up to 40 years after treatment for Hodgkin’s lymphoma. N Engl J Med 373(26):2499–2511. CrossRefPubMedGoogle Scholar
  14. 14.
    Bhuller KS, Zhang Y, Li D, Sehn LH, Goddard K, McBride ML, Rogers PC (2016) Late mortality, secondary malignancy and hospitalisation in teenage and young adult survivors of Hodgkin lymphoma: report of the Childhood/Adolescent/Young Adult Cancer Survivors Research Program and the BC Cancer Agency Centre for Lymphoid Cancer. Br J Haematol 172(5):757–768. CrossRefPubMedGoogle Scholar
  15. 15.
    Rugbjerg K, Olsen JH (2016) Long-term risk of hospitalization for somatic diseases in survivors of adolescent or young adult cancer. JAMA Oncol 2(2):193–200. CrossRefPubMedGoogle Scholar
  16. 16.
    Fritz F, Percy C, Jack A, Shanmugaratnan K, Sobin L, Parkin DM, Whelan S (eds) (2000) International classification of diseases for oncology, 3 edn. World Health Organization, GenevaGoogle Scholar
  17. 17.
    Chao C, Xu L, Bell E, Cooper R, Mueller L (2016) Long-term health outcomes in survivors of childhood cancer diagnosed between 1990 and 2000 in a Large US Integrated Health Care System. J Pediatr Hematol Oncol 38(2):123–130. CrossRefPubMedGoogle Scholar
  18. 18.
    Cella L, Conson M, Caterino M, De Rosa N, Liuzzi R, Picardi M, Grimaldi F, Solla R, Farella A, Salvatore M, Pacelli R (2012) Thyroid V30 predicts radiation-induced hypothyroidism in patients treated with sequential chemo-radiotherapy for Hodgkin’s lymphoma. Int J Radiat Oncol Biol Phys 82(5):1802–1808. CrossRefPubMedGoogle Scholar
  19. 19.
    Smith EC, Ziogas A, Anton-Culver H (2012) Association between insurance and socioeconomic status and risk of advanced stage Hodgkin lymphoma in adolescents and young adults. Cancer 118(24):6179–6187. CrossRefPubMedGoogle Scholar
  20. 20.
    Rosenberg AR, Kroon L, Chen L, Li CI, Jones B (2015) Insurance status and risk of cancer mortality among adolescents and young adults. Cancer 121(8):1279–1286. CrossRefPubMedGoogle Scholar
  21. 21.
    Yost K, Perkins C, Cohen R, Morris C, Wright W (2001) Socioeconomic status and breast cancer incidence in California for different race/ethnic groups. Cancer Causes Control 12(8):703–711CrossRefPubMedGoogle Scholar
  22. 22.
    Clarke CA, Glaser SL (2004) Population-based surveillance of HIV-associated cancers: utility of cancer registry data. J Acquir Immune Defic Syndr 36(5):1083–1091CrossRefPubMedGoogle Scholar
  23. 23.
    Olszewski AJ, Castillo JJ (2016) Outcomes of HIV-associated Hodgkin lymphoma in the era of antiretroviral therapy. AIDS 30(5):787–796. CrossRefPubMedGoogle Scholar
  24. 24.
    Lin G, So Y, Johnston G (2012) Analyzing survival data with competing risks using SAS® Software. Proceedings of the SAS® Global Forum 2012 Conference. SAS Institute Inc, Cary, NCGoogle Scholar
  25. 25.
    Gray R (1988) A class of K-sample tests for comparing the cumulative incidence of a competing risk. Ann Stat 16:1141–1154CrossRefGoogle Scholar
  26. 26.
    Rugbjerg K, Maraldo M, Aznar MC, Cutter DJ, Darby SC, Specht L, Olsen JH (2017) Long-term hospitalisation rates among 5-year survivors of Hodgkin lymphoma in adolescence or young adulthood: a nationwide cohort study. Int J Cancer 140(10):2232–2245. CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Xavier AC, Costa LJ (2015) Changes in the use of radiation therapy for early classical Hodgkin lymphoma in adolescents and young adults: implications for survival and second malignancies. Leuk Lymphoma. Google Scholar
  28. 28.
    Kirchhoff AC, Lyles CR, Fluchel M, Wright J, Leisenring W (2012) Limitations in health care access and utilization among long-term survivors of adolescent and young adult cancer. Cancer 118(23):5964–5972. CrossRefPubMedGoogle Scholar
  29. 29.
    Keegan TH, Tao L, DeRouen MC, Wu XC, Prasad P, Lynch CF, Shnorhavorian M, Zebrack BJ, Chu R, Harlan LC, Smith AW, Parsons HM, Group AHSC. (2014) Medical care in adolescents and young adult cancer survivors: what are the biggest access-related barriers? J Cancer Surviv 8(2):282–292. CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Kaul S, Fluchel M, Spraker-Perlman H, Parmeter CF, Kirchhoff AC (2016) Health care experiences of long-term survivors of adolescent and young adult cancer. Support Care Cancer. PubMedGoogle Scholar
  31. 31.
    Bleyer A, Ulrich C, Martin S (2012) Young adults, cancer, health insurance, socioeconomic status, and the Patient Protection and Affordable Care Act. Cancer 118(24):6018–6021. CrossRefPubMedGoogle Scholar
  32. 32.
    Adams SH, Newacheck PW, Park MJ, Brindis CD, Irwin CE Jr (2007) Health insurance across vulnerable ages: patterns and disparities from adolescence to the early 30 s. Pediatrics 119(5):e1033–e1039. CrossRefGoogle Scholar
  33. 33.
    Parsons HM, Schmidt S, Harlan LC, Kent EE, Lynch CF, Smith AW, Keegan TH, Collaborative AH (2014) Young and uninsured: insurance patterns of recently diagnosed adolescent and young adult cancer survivors in the AYA HOPE study. Cancer 120(15):2352–2360. CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Guy GP Jr, Yabroff KR, Ekwueme DU, Virgo KS, Han X, Banegas MP, Soni A, Zheng Z, Chawla N, Geiger AM (2015) Healthcare expenditure burden among non-elderly cancer survivors, 2008–2012. Am J Prev Med 49(6 Suppl 5):S489–S497. Google Scholar
  35. 35.
    American Society of Clinical O (2016) The State of Cancer Care in America, 2016: a report by the American Society of Clinical Oncology. J Oncol Pract 12 (4):339–383. CrossRefGoogle Scholar
  36. 36.
    Keegan TH, Clarke CA, Chang ET, Shema SJ, Glaser SL (2009) Disparities in survival after Hodgkin lymphoma: a population-based study. Cancer Causes Control 20(10):1881–1892. CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Centers for Disease Control and Prevention (2013) Coronary heart disease and stroke deaths—United States, 2009. MMWR 62(Suppl 3):157–160Google Scholar
  38. 38.
    Golden SH, Brown A, Cauley JA, Chin MH, Gary-Webb TL, Kim C, Sosa JA, Sumner AE, Anton B (2012) Health disparities in endocrine disorders: biological, clinical, and nonclinical factors—an endocrine society scientific statement. J Clin Endocrinol Metab 97(9):E1579–E1639. CrossRefGoogle Scholar
  39. 39.
    Jagsi R, Abrahamse P, Hawley ST, Graff JJ, Hamilton AS, Katz SJ (2012) Underascertainment of radiotherapy receipt in Surveillance, Epidemiology, and End Results registry data. Cancer 118(2):333–341. CrossRefPubMedGoogle Scholar
  40. 40.
    Noone AM, Lund JL, Mariotto A, Cronin K, McNeel T, Deapen D, Warren JL (2014) Comparison of SEER treatment data with medicare claims. Med Care. Google Scholar
  41. 41.
    Khimani N, Chen YH, Mauch PM, Recklitis C, Diller L, Silver B, Ng AK (2013) Influence of new late effects on quality of life over time in Hodgkin lymphoma survivors: a longitudinal survey study. Ann Oncol 24(1):226–230. CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Center for Oncology Hematology Outcomes Research and Training (COHORT) and Division of Hematology and OncologyUniversity of California Davis School of MedicineSacramentoUSA
  2. 2.Department of PediatricsUniversity of California Davis School of MedicineSacramentoUSA
  3. 3.Department of Hematology and Oncology, Winship Cancer InstituteEmory UniversityAtlantaUSA
  4. 4.Cancer Prevention Institute of CaliforniaFremontUSA
  5. 5.Department of Health Research and Policy (Epidemiology)Stanford University School of MedicineStanfordUSA

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