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Lifetime Costs for Treated Follicular Lymphoma Patients in the US

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Abstract

Background and Objective

The objective of this study was to estimate the lifetime costs of patients receiving treatment for follicular lymphoma (FL) in the United States.

Methods

A Markov model was programmed in hēRo3 with a 6-month cycle length, 35-year time horizon (lifetime projection), and health states for line of treatment, response, receipt of maintenance therapy among responders, transformation to diffuse large B-cell lymphoma (DLBCL), development of second primary malignancy (SPM), and death. The model was used to estimate the expected lifetime costs of FL (in 2019 USD), including costs of drug acquisition and administration, transplant procedures, radiotherapy, adverse events, follow-up, DLBCL, SPM, end-of-life care, and indirect costs. Model inputs were based on published sources.

Results

In the US, patients with FL receiving treatment have a life expectancy of approximately 14.5 years from initiation of treatment and expected lifetime direct and indirect costs of US$515,884. Costs of drugs for induction therapy represent the largest expenditure (US$233,174), followed by maintenance therapy costs (US$88,971) and terminal care costs (US$57,065). Despite the relatively advanced age of these patients, indirect costs (due to patient morbidity and mortality and caregiver lost work time) represent a substantial share of total costs (US$40,280). Treated FL patients spend approximately 6.9 years in the health states associated with first-line therapy. Approximately 66 and 46% continue to second- and third-line therapies, respectively. The mean (95% credible interval) of expected lifetime costs based on the probabilistic sensitivity analyses was US$559,202 (421,997–762,553).

Conclusions

In the US, the expected lifetime costs of care for FL patients who receive treatment is high. The results highlight the potential economic benefits that might be achieved by treatments for FL that prevent or delay disease progression.

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References

  1. Surveillance Epidemiology and End Results Program. Cancer stat facts: NHL—follicular lymphoma: National Cancer Institute; 2020. [cited 2020 June 26]. Available from: https://seer.cancer.gov/statfacts/html/follicular.html.

  2. Mariotto AB, Yabroff KR, Shao Y, Feuer EJ, Brown ML. Projections of the cost of cancer care in the United States: 2010–2020. J Natl Cancer Inst. 2011;103(2):117–28. https://doi.org/10.1093/jnci/djq495 (Epub 2011/01/14).

    Article  PubMed  PubMed Central  Google Scholar 

  3. Bachy E, Seymour JF, Feugier P, Offner F, Lopez-Guillermo A, Belada D, et al. sustained progression-free survival benefit of rituximab maintenance in patients with follicular lymphoma: long-term results of the PRIMA study. J Clin Oncol. 2019;37(31):2815–24. https://doi.org/10.1200/JCO.19.01073 (Epub 2019/07/25).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. van Oers MH, Van Glabbeke M, Giurgea L, Klasa R, Marcus RE, Wolf M, et al. Rituximab maintenance treatment of relapsed/resistant follicular non-Hodgkin’s lymphoma: long-term outcome of the EORTC 20981 phase III randomized intergroup study. J Clin Oncol. 2010;28(17):2853–8. https://doi.org/10.1200/JCO.2009.26.5827 (Epub 2010/05/05).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Flinn IW, Miller CB, Ardeshna KM, Tetreault S, Assouline SE, Mayer J, et al. DYNAMO: a phase II study of duvelisib (IPI-145) in patients with refractory indolent non-hodgkin lymphoma. J Clin Oncol. 2019;37(11):912–22. https://doi.org/10.1200/JCO.18.00915 (Epub 2019/02/12).

    Article  CAS  PubMed  Google Scholar 

  6. Dreyling M, Morschhauser F, Bouabdallah K, Bron D, Cunningham D, Assouline SE, et al. Phase II study of copanlisib, a PI3K inhibitor, in relapsed or refractory, indolent or aggressive lymphoma. Ann Oncol. 2017;28(9):2169–78. https://doi.org/10.1093/annonc/mdx289 (Epub 2017/06/22).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Gopal AK, Kahl BS, de Vos S, Wagner-Johnston ND, Schuster SJ, Jurczak WJ, et al. PI3Kdelta inhibition by idelalisib in patients with relapsed indolent lymphoma. N Engl J Med. 2014;370(11):1008–18. https://doi.org/10.1056/NEJMoa1314583 (Epub 2014/01/24).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. COPIKTRA (duvelisib), capsules for oral use [prescribing information]. Needham, MA: Verastem Inc.; September 2019.

  9. ALIQOPA (copanlisib) for injection [prescribing information]. Whippany: Bayer HealthCare Pharmaceuticals Inc.; 2020.

  10. ZYDELIG® (idelalisib) [prescribing information]. Foster City: Gilead Sciences, Inc.; 2018.

  11. Chen Q, Ayer T, Nastoupil LJ, Rose AC, Flowers CR. Comparing the cost-effectiveness of rituximab maintenance and radioimmunotherapy consolidation versus observation following first-line therapy in patients with follicular lymphoma. Value Health. 2015;18(2):189–97. https://doi.org/10.1016/j.jval.2014.12.017 (Epub 2015/03/17).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Hornberger J, Chien R, Friedmann M, Han L, Shewade A, Satram-Hoang S, et al. Cost-effectiveness of rituximab as maintenance therapy in patients with follicular non-Hodgkin lymphoma after responding to first-line rituximab plus chemotherapy. Leuk Lymphoma. 2012;53(12):2371–7. https://doi.org/10.3109/10428194.2012.694429 (Epub 2012/05/18).

    Article  CAS  PubMed  Google Scholar 

  13. Prica A, Chan K, Cheung M. Frontline rituximab monotherapy induction versus a watch and wait approach for asymptomatic advanced-stage follicular lymphoma: a cost-effectiveness analysis. Cancer. 2015;121(15):2637–45. https://doi.org/10.1002/cncr.29372 (Epub 2015/04/17).

    Article  CAS  PubMed  Google Scholar 

  14. Soini EJO, Martikainen JA, Nousiainen T. Treatment of follicular non-Hodgkin’s lymphoma with or without rituximab: cost-effectiveness and value of information based on a 5-year follow-up. Ann Oncol. 2011;22(5):1189–97. https://doi.org/10.1093/annonc/mdq582 (Epub 2010/12/08).

    Article  CAS  PubMed  Google Scholar 

  15. Griffiths RI, Gleeson ML, Mikhael J, Danese MD. Impact on Medical cost, cumulative survival, and cost-effectiveness of adding rituximab to first-line chemotherapy for follicular lymphoma in elderly patients: an observational cohort study based on SEER-Medicare. J Cancer Epidemiol. 2012;2012:978391. https://doi.org/10.1155/2012/978391 (Epub 2012/09/13).

    Article  PubMed  PubMed Central  Google Scholar 

  16. Wang HI, Roman E, Crouch S, Aas E, Burton C, Patmore R, et al. A Generic model for follicular lymphoma: predicting cost, life expectancy, and quality-adjusted-life-year using UK population-based observational data. Value Health. 2018;21(10):1176–85. https://doi.org/10.1016/j.jval.2018.03.007 (Epub 2018/10/14).

    Article  PubMed  PubMed Central  Google Scholar 

  17. US Bureau of Labor Statistics. CPI—all urban consumers. Medical care in US city average, all urban 2019. [cited 2020 May]. Available from: https://data.bls.gov/cgi-bin/surveymost?cu.

  18. Magnano L, Alonso-Alvarez S, Alcoceba M, Rivas-Delgado A, Muntanola A, Nadeu F, et al. Life expectancy of follicular lymphoma patients in complete response at 30 months is similar to that of the Spanish general population. Br J Haematol. 2019;185(3):480–91. https://doi.org/10.1111/bjh.15805 (Epub 2019/02/23).

    Article  CAS  PubMed  Google Scholar 

  19. Siddhartha G, Vijay P. R-CHOP versus R-CVP in the treatment of follicular lymphoma: a meta-analysis and critical appraisal of current literature. J Hematol Oncol. 2009;2:14. https://doi.org/10.1186/1756-8722-2-14 (Epub 2009/03/25).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Wagner-Johnston ND, Link BK, Byrtek M, Dawson KL, Hainsworth J, Flowers CR, et al. Outcomes of transformed follicular lymphoma in the modern era: a report from the National LymphoCare Study (NLCS). Blood. 2015;126(7):851–7. https://doi.org/10.1182/blood-2015-01-621375 (Epub 2015/06/25).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Giri S, Bhatt VR, Verma V, Pathak R, Bociek RG, Vose JM, et al. Risk of second primary malignancies in patients with follicular lymphoma: a United States population-based study. Clin Lymphoma Myeloma Leuk. 2017;17(9):569–74. https://doi.org/10.1016/j.clml.2017.06.028 (Epub 2017/07/16).

    Article  PubMed  Google Scholar 

  22. National Cancer Institute S, Epidemiology, and End Results Program. Cancer query system: SEER survival statistics. [cited 2020 May]. Available from: https://seer.cancer.gov/canques/survival.html.

  23. Arias E, Xu J. United States life tables, 2017. CDC Natl Vital Stat Rep. 2019;68(7):1–66.

    Google Scholar 

  24. Novartis data on file. Primary market research conducted by Kantar Health using survey of 58 practicing physicians. 2019.

  25. 2019 ASP drug pricing files [Internet]. 2019. Available from: https://www.cms.gov/Medicare/Medicare-Fee-for-Service-Part-B-Drugs/McrPartBDrugAvgSalesPrice/2019ASPFiles.

  26. Centers for Medicare and Medicaid Services. Medicare part B drug average sales price [updated December 17, 2020]. Available from: https://www.cms.gov/Medicare/Medicare-Fee-for-Service-Part-B-Drugs/McrPartBDrugAvgSalesPrice.

  27. IBM Corporation. IBM Micromedex RED BOOK. Available (for purchase) at: http://www.micromedexsolutions.com/home/dispatch. Accessed: Feb 2020.

  28. Mullins CD, Seal B, Seoane-Vazquez E, Sankaranarayanan J, Asche CV, Jayadevappa R, et al. Good research practices for measuring drug costs in cost-effectiveness analyses: Medicare, Medicaid and other US government payers perspectives: the ISPOR Drug Cost Task Force report—Part IV. Value Health. 2010;13(1):18–24. https://doi.org/10.1111/j.1524-4733.2009.00604.x (Epub 2009/10/08).

    Article  PubMed  Google Scholar 

  29. Center for Medicare and Medicaid Services. Physician fee schedule search. Available at: https://www.cms.gov/apps/physician-fee-schedule/search/search-results.aspx?Y=0&T=0&HT=0&CT=3&H1=96521&M=5. Accessed on: Jan 2020.

  30. Maziarz RT, Hao Y, Guerin A, Gauthier G, Gauthier-Loiselle M, Thomas SK, et al. Economic burden following allogeneic hematopoietic stem cell transplant in patients with diffuse large B-cell lymphoma. Leuk Lymphoma. 2018;59(5):1133–42. https://doi.org/10.1080/10428194.2017.1375100 (Epub 2017/09/22).

    Article  PubMed  Google Scholar 

  31. Bentley T, Philllips S. 2017 US organ and tissue transplant cost estimates and discussion. Milliman Research Report. 2017.

  32. Healthcare Cost and Utilization Project (HCUP). https://hcupnet.ahrq.gov/ [Internet]. 2017.

  33. GlaxoSmithKline. Ofatumumab (Humax-CD20) with CHOP (cyclophosphamide, doxorubicin, vincristine, predisolone) in follicular lymphoma (FL) patients (MUNIN). 2011. Available from: https://clinicaltrials.gov/ct2/show/results/NCT00494780?view=results.

  34. Barr PM, Li H, Burack WR, LeBlanc M, Smith SM, Gopal AK, et al. R-CHOP, radioimmunotherapy, and maintenance rituximab in untreated follicular lymphoma (SWOG S0801): a single-arm, phase 2, multicentre study. Lancet Haematol. 2018;5(3):e102–8. https://doi.org/10.1016/S2352-3026(18)30001-2 (Epub 2018/02/06).

    Article  PubMed  PubMed Central  Google Scholar 

  35. University of Washington. Vorinostat, rituximab, ifosfamide, carboplatin, and etoposide in treating patients with relapsed or refractory lymphoma or previously untreated T-cell non-Hodgkin lymphoma or mantle cell lymphoma. 2017. Available from: https://clinicaltrials.gov/ct2/show/results/NCT00601718?view=results.

  36. University of Arizona. Rituximab, yttrium Y 90 ibritumomab tiuxetan in patients W/relapsed stage II, III, or IV follicular NHL (ESHAP). 2019. Available from: https://clinicaltrials.gov/ct2/show/results/NCT00732498.

  37. National Comprehensive Cancer Network. NCCN clinical practice guidelines in oncology version 4.2020 B-cell lymphomas. 2020.

  38. Center for Medicare and Medicaid Services. Clinical laboratory fee schedule files (2019 Q4). Available at: https://www.cms.gov/Medicare/Medicare-Fee-for-Service-Payment/ClinicalLabFeeSched/Clinical-Laboratory-Fee-Schedule-Files.

  39. Morrison VA, Bell JA, Hamilton L, Ogbonnaya A, Shih HC, Hennenfent K, et al. Economic burden of patients with diffuse large B-cell and follicular lymphoma treated in the USA. Future Oncol. 2018;14(25):2627–42. https://doi.org/10.2217/fon-2018-0267 (Epub 2018/06/19).

    Article  CAS  PubMed  Google Scholar 

  40. Friedberg JW. Relapsed/refractory diffuse large B-cell lymphoma. Hematol Am Soc Hematol Educ Progr. 2011;2011:498–505. https://doi.org/10.1182/asheducation-2011.1.498 (Epub 2011/12/14).

    Article  Google Scholar 

  41. Roth JA, Sullivan SD, Lin VW, Bansal A, Purdum AG, Navale L, et al. Cost-effectiveness of axicabtagene ciloleucel for adult patients with relapsed or refractory large B-cell lymphoma in the United States. J Med Econ. 2018;21(12):1238–45. https://doi.org/10.1080/13696998.2018.1529674 (Epub 2018/09/28).

    Article  PubMed  Google Scholar 

  42. National Cancer Institute. Estimates of national expenditures for cancer care by cancer site and year 2018 [updated March 8, 2019]. Available from: https://progressreport.cancer.gov/after/economic_burden.

  43. Kutikova L, Bowman L, Chang S, Long SR, Arning M, Crown WH. Medical costs associated with non-Hodgkin’s lymphoma in the United States during the first two years of treatment. Leuk Lymphoma. 2006;47(8):1535–44. https://doi.org/10.1080/10428190600573325 (Epub 2006/09/13).

    Article  PubMed  Google Scholar 

  44. Cheung MC, Imrie KR, Friedlich J, Buckstein R, Lathia N, Mittmann N. The impact of follicular (FL) and other indolent non-Hodgkin’s lymphomas (NHL) on work productivity-a preliminary analysis. Psychooncology. 2009;18(5):554–9. https://doi.org/10.1002/pon.1404 (Epub 2008/10/24).

    Article  PubMed  Google Scholar 

  45. Biogen, Genentech. RITUXAN® (rituximab) for injection, for intravenous use [full prescribing information]. Initial US Approval: 1997. Revised: 3/2020. Available at: https://www.gene.com/download/pdf/rituxan_prescribing.pdf. Accessed: May 2020.

  46. US Bureau of Labor Statistics. Civilian labor force participation rate by age, sex, race, and ethnicity [updated September 4, 2019; cited 2020 May]. Available from: https://www.bls.gov/emp/tables/civilian-labor-force-participation-rate.htm.

  47. US Bureau of Labor Statistics. Median usual weekly earnings of women and men who are full-time wage and salary workers, by age, 2016 annual averages [updated August 25, 2017; cited 2020 May]. Available from: https://www.bls.gov/opub/ted/2017/womens-and-mens-earnings-by-age-in-2016.htm.

  48. Sanders GD, Neumann PJ, Basu A, Brock DW, Feeny D, Krahn M, et al. Recommendations for conduct, methodological practices, and reporting of cost-effectiveness analyses: second panel on cost-effectiveness in health and medicine. JAMA. 2016;316(10):1093–103. https://doi.org/10.1001/jama.2016.12195 (Epub 2016/09/14).

    Article  PubMed  Google Scholar 

  49. Martin P, Byrtek M, Dawson K, Ziemiecki R, Friedberg JW, Cerhan JR, et al. Patterns of delivery of chemoimmunotherapy to patients with follicular lymphoma in the United States: results of the National LymphoCare Study. Cancer. 2013;119(23):4129–36. https://doi.org/10.1002/cncr.28350 (Epub 2013/09/06).

    Article  CAS  PubMed  Google Scholar 

  50. Link BK, Day BM, Zhou X, Zelenetz AD, Dawson KL, Cerhan JR, et al. Second-line and subsequent therapy and outcomes for follicular lymphoma in the United States: data from the observational National LymphoCare Study. Br J Haematol. 2019;184(4):660–3. https://doi.org/10.1111/bjh.15149 (Epub 2018/04/04).

    Article  PubMed  Google Scholar 

  51. Caglayan C, Terawaki H, Ayer T, Goldstein JS, Rai A, Chen Q, et al. Assessing the effectiveness of treatment sequences for older patients with high-risk follicular lymphoma with a multistate model. Clin Lymphoma Myeloma Leuk. 2019;19(5):300 e5-309 e5. https://doi.org/10.1016/j.clml.2018.12.019 (Epub 2019/01/29).

    Article  Google Scholar 

  52. Albarmawi H, Nagarajan M, Onukwugha E, Gandhi AB, Keating KN, Appukkuttan S, et al. Follicular lymphoma treatment patterns between 2000 and 2014: a SEER-Medicare analysis of elderly patients. Future Oncol. 2020;16(8):353–65. https://doi.org/10.2217/fon-2019-0660 (Epub 2020/02/12).

    Article  CAS  PubMed  Google Scholar 

  53. Batlevi CL, Sha F, Alperovich A, Ni A, Smith K, Ying Z, et al. Follicular lymphoma in the modern era: survival, treatment outcomes, and identification of high-risk subgroups. Blood Cancer J. 2020;10(7):74. https://doi.org/10.1038/s41408-020-00340-z (Epub 2020/07/18).

    Article  PubMed  PubMed Central  Google Scholar 

  54. Jackson CH. flexsurv: a platform for parametric survival modeling in R. J Stat Softw. 2016. https://doi.org/10.18637/jss.v070.i08 (Epub 2016/05/12).

    Article  PubMed  PubMed Central  Google Scholar 

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Correspondence to Thomas E. Delea.

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Funding

Support for this study was provided by Novartis, Inc., East Hanover, NJ, USA. The authors were responsible for all content and editorial decisions, and they received no honoraria related to the development of this publication.

Conflict of interests

TED is an employee and owner of PAI. PAI received research funding from Novartis for this study. CE and MH are employees of PAI. PAI received research funding from Novartis for this study. QM, RR, SRI, and JZ are employees of Novartis. Novartis provided research funding to PAI for this study. RTM: Honoraria, membership on an entity’s Board of Directors or advisory committees and research funding: Novartis; Consultancy and honoraria: Incyte, Juno; Honoraria: Kite, Jazz Pharmaceuticals; Patents & Royalties: Athersys, Inc.; Employment: Oregon Health & Science University (OHSU); with regard to the consultant services and payment from Novartis, this potential conflict of interest has been reviewed and managed by OHSU.

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Data availability statement

The authors declare that all input data to parameterize the model are available within the article. The model can be re-built entirely based on the information provided.

Code availability

The information reported in this article is sufficient to replicate the results of the study. The model used in the article includes a proprietary code and is not provided.

Author contributions

TED, CE, MH, QM: Study design, data collection, data analysis, interpretation of results, writing of draft and final manuscript. RR, JZ, SRI, RTM: Data collection, data analysis, interpretation of results, writing of draft and review of final manuscript.

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Eichten, C., Ma, Q., Delea, T.E. et al. Lifetime Costs for Treated Follicular Lymphoma Patients in the US. PharmacoEconomics 39, 1163–1183 (2021). https://doi.org/10.1007/s40273-021-01052-3

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