Cost-effectiveness analysis of multigene expression profiling assays to guide adjuvant therapy decisions in women with invasive early-stage breast cancer.


Journal

The pharmacogenomics journal
ISSN: 1473-1150
Titre abrégé: Pharmacogenomics J
Pays: United States
ID NLM: 101083949

Informations de publication

Date de publication:
02 2020
Historique:
received: 30 05 2018
accepted: 27 03 2019
revised: 07 10 2018
pubmed: 28 5 2019
medline: 5 1 2021
entrez: 28 5 2019
Statut: ppublish

Résumé

Gene expression profiling (GEP) testing using 12-gene recurrence score (RS) assay (EndoPredict®), 58-gene RS assay (Prosigna®), and 21-gene RS assay (Oncotype DX®) is available to aid in chemotherapy decision-making when traditional clinicopathological predictors are insufficient to accurately determine recurrence risk in women with axillary lymph node-negative, hormone receptor-positive, and human epidermal growth factor-receptor 2-negative early-stage breast cancer. We examined the cost-effectiveness of incorporating these assays into standard practice. A decision model was built to project lifetime clinical and economic consequences of different adjuvant treatment-guiding strategies. The model was parameterized using follow-up data from a secondary analysis of the Anastrozole or Tamoxifen Alone or Combined randomized trial, cost data (2017 Canadian dollars) from the London Regional Cancer Program (Canada) and secondary Canadian sources. The 12-gene, 58-gene, and 21-gene RS assays were associated with cost-effectiveness ratios of $36,274, $48,525, and $74,911/quality-adjusted life year (QALY) gained and resulted in total gains of 379, 284.3, and 189.5 QALYs/year and total budgets of $12.9, $14.2, and $16.6 million/year, respectively. The total expected-value of perfect information about GEP assays' utility was $10.4 million/year. GEP testing using any of these assays is likely clinically and economically attractive. The 12-gene and 58-gene RS assays may improve the cost-effectiveness of GEP testing and offer higher value for money, although prospective evidence is still needed. Comparative field evaluations of GEP assays in real-world practice are associated with a large societal benefit and warranted to determine the optimal and most cost-effective assay for routine use.

Identifiants

pubmed: 31130722
doi: 10.1038/s41397-019-0089-x
pii: 10.1038/s41397-019-0089-x
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

27-46

Références

Canadian Cancer Society’s Advisory Committee on Cancer Statistics. Canadian cancer statistics 2017. Toronto, ON: Canadian Cancer Society; 2017.
Ghafoor A, Jemal A, Ward E, Cokkinides V, Smith R, Thun M. Trends in breast cancer by race and ethnicity. CA Cancer J Clin. 2003;53:342–55.
pubmed: 15224974
Members of the Breast Cancer Disease Site Group. Surgical management of early-stage invasive breast cancer. In: Brackstone M, Tey R, reviewers. Program in evidence-based care evidence-based series no.: 1-1 Version 3. Education and Information 2015. Toronto, ON: Cancer Care Ontario; 2011. Endorsed 19 Nov 2010.
Eisen A, Fletcher GG, Gandhi S, Mates M, Freedman OC, Dent SF, et al. Optimal systematic therapy for early female breast cancer. In: Program in evidence-based care evidence-based series no.: 1–21. Toronto, ON: Cancer Care Ontario; 2014.
Early Breast Cancer Trialists' Collaborative Group, Peto R, Davies C, Godwin J, Gray R, Pan HC, et al. Comparisons between different polychemotherapy regimens for early breast cancer: meta-analyses of long-term outcome among 100,000 women in 123 randomised trials. Lancet. 2012;379:432–44.
Gyorffy B, Hatzis C, Sanft T, Hofstatter E, Aktas B, Pusztai L. Multigene prognostic tests in breast cancer: past, present, future. Breast Cancer Res. 2015;17:11.
pubmed: 25848861 pmcid: 4307898
Paik S, Shak S, Tang G, Kim C, Baker J, Cronin M, et al. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med. 2004;351:2817–26.
pubmed: 15591335 pmcid: 15591335
Paik S, Tang G, Shak S, Kim C, Baker J, Kim W, et al. Gene expression and benefit of chemotherapy in women with node-negative, estrogen receptor-positive breast cancer. J Clin Oncol. 2006;24:3726–34.
pubmed: 16720680
Mamounas EP, Tang G, Fisher B, Paik S, Shak S, Costantino JP, et al. Association between the 21-gene recurrence score assay and risk of locoregional recurrence in node-negative, estrogen receptor-positive breast cancer: results from NSABP B-14 and NSABP B-20. J Clin Oncol. 2010;28:1677–83.
pubmed: 20065188 pmcid: 2849763
Albain KS, Barlow WE, Shak S, Hortobagyi GN, Livingston RB, Yeh IT, et al. Prognostic and predictive value of the 21-gene recurrence score assay in postmenopausal women with node-positive, oestrogen-receptor-positive breast cancer on chemotherapy: a retrospective analysis of a randomised trial. Lancet Oncol. 2010;11:55–65.
pubmed: 20005174
Dowsett M, Cuzick J, Wale C, Forbes J, Mallon EA, Salter J, et al. Prediction of risk of distant recurrence using the 21-gene recurrence score in node-negative and node-positive postmenopausal patients with breast cancer treated with anastrozole or tamoxifen: a TransATAC study. J Clin Oncol. 2010;28:1829–34.
pubmed: 20212256
Ioannidis JP. Is molecular profiling ready for use in clinical decision making? Oncologist. 2007;12:301–11.
pubmed: 17405894
Sestak I, Dowsett M, Zabaglo L, Lopez-Knowles E, Ferree S, Cowens JW, et al. Factors predicting late recurrence for estrogen receptor-positive breast cancer. J Natl Cancer Inst. 2013;105:1504–11.
pubmed: 24029245 pmcid: 3787911
Kos Z, Nielsen TO. Developing a new generation of breast cancer clinical gene expression tests. Breast Cancer Res. 2014;16:103.
pubmed: 25928431 pmcid: 4100317
Michiels S, Ternes N, Rotolo F. Statistical controversies in clinical research: prognostic gene signatures are not (yet) useful in clinical practice. Ann Oncol. 2016;27:2160–7.
pubmed: 27634691 pmcid: 5178139
Hannouf MB, Xie B, Brackstone M, Zaric GS. Cost-effectiveness of a 21-gene recurrence score assay versus Canadian clinical practice in women with early-stage estrogen- or progesterone-receptor-positive, axillary lymph-node negative breast cancer. BMC Cancer. 2012;12:447.
pubmed: 23031196 pmcid: 3488327
Tsoi DT, Inoue M, Kelly CM, Verma S, Pritchard KI. Cost-effectiveness analysis of recurrence score-guided treatment using a 21-gene assay in early breast cancer. Oncologist. 2010;15:457–65.
pubmed: 20421264 pmcid: 3227972
Chang MC, Souter LH, Kamel-Reid S, Rutherford M, Bedard P, Trudeau M, et al. Clinical utility of multigene profiling assays in early-stage breast cancer. In: Program in evidence-based care recommendation report no.: MOAC-4. Toronto, ON: Cancer Care Ontario. Available on the CCO website: www.cancercare.on.ca/toolbox/qualityguidelines/clin-program/pathlabebs/pebc_moleconc/ . Accessed 10 July 2017.
Buus R, Sestak I, Kronenwett R, Denkert C, Dubsky P, Krappmann K, et al. Comparison of EndoPredict and EPclin with oncotype DX recurrence score for prediction of risk of distant recurrence after endocrine therapy. J Natl Cancer Inst. 2016;108. https://doi.org/10.1093/jnci/djw149 .
pmcid: 5241904
Dowsett M, Sestak I, Lopez-Knowles E, Sidhu K, Dunbier AK, Cowens JW, et al. Comparison of PAM50 risk of recurrence score with oncotype DX and IHC4 for predicting risk of distant recurrence after endocrine therapy. J Clin Oncol. 2013;31:2783–90.
pubmed: 23816962
Sestak I, Buus R, Cuzick J, Dubsky P, Kronenwett R, Denkert C, et al. Comparison of the performance of 6 prognostic signatures for estrogen receptor-positive breast cancer: a secondary analysis of a randomized clinical trial. JAMA Oncol. 2018;4:545–53.
pubmed: 29450494 pmcid: 5885222
Inadomi JM. Decision analysis and economic modelling: a primer. Eur J Gastroenterol Hepatol. 2004;16:535–42.
pubmed: 15167154
Younis T, Rayson D, Thompson K. Primary G-CSF prophylaxis for adjuvant TC or FEC-D chemotherapy outside of clinical trial settings: a systematic review and meta-analysis. Support Care Cancer. 2012;20:2523–30.
pubmed: 22252548
Petrelli F, Borgonovo K, Cabiddu M, Lonati V, Barni S. Mortality, leukemic risk, and cardiovascular toxicity of adjuvant anthracycline and taxane chemotherapy in breast cancer: a meta-analysis. Breast Cancer Res Treat. 2012;135:335–46.
pubmed: 22689092
Guidelines for the economic evaluation of health technologies. 4th ed. Ottawa, Canada: CADTH; 2017.
Sonnenberg FA, Beck JR. Markov models in medical decision making: a practical guide. Med Decis Making. 1993;13:322–38.
pubmed: 8246705
Levine MN, Julian JA, Bedard PL, Eisen A, Trudeau ME, Higgins B, et al. Prospective evaluation of the 21-gene recurrence score assay for breast cancer decision-making in Ontario. J Clin Oncol. 2016;34:1065–71.
pubmed: 26598746
Cancer Care Ontario. Cancer Care Ontario GCSF recommendations 2016. https://www.cancercare.on.ca/common/pages/UserFile.aspx?fileId=352101 . Accessed 24 July 2017.
Chatterjee K, Zhang J, Honbo N, Karliner JS. Doxorubicin cardiomyopathy. Cardiology. 2010;115:155–62.
pubmed: 20016174
Kirwan CC, McDowell G, McCollum CN, Byrne GJ. Incidence of venous thromboembolism during chemotherapy for breast cancer: impact on cancer outcome. Anticancer Res. 2011;31:2383–8.
pubmed: 21737669
Wolff AC, Blackford AL, Visvanathan K, Rugo HS, Moy B, Goldstein LJ, et al. Risk of marrow neoplasms after adjuvant breast cancer therapy: the national comprehensive cancer network experience. J Clin Oncol. 2015;33:340–8.
pubmed: 25534386
Statistics Canada/Health Statistics Division. Life Tables, Canada and the Provinces, 2000–2002. Ottawa, Ontario, Canada: Minister of Industry; 2006. Publication 84-537-XIE.
Cuzick J, Sestak I, Baum M, Buzdar A, Howell A, Dowsett M, et al. Effect of anastrozole and tamoxifen as adjuvant treatment for early-stage breast cancer: 10-year analysis of the ATAC trial. Lancet Oncol. 2010;11:1135–41.
pubmed: 21087898
Ministry of Health and Long‐Term Care. Out‐of‐Country Program. Kingston, ON, Canada: Ministry of Health and Long‐Term Care; 2016.
Prosigna [Package Insert]. Seattle, WA: NanoString Technologies, Inc. Available at http://www.lifelabsgenetics.com/breast-cancer-prosigna-assay/paymentinformation . Accessed 18 June 2017.
British Colombia Cancer Agency. Laboratory services, oncotype Dx testing and Prosigna testing. BC, Canada. Available at http://www.bccancer.bc.ca/health-professionals/clinical-resources/laboratory-services . Accessed 13 Nov 2017.
Alberta Health Services. Laboratory services, breast cancer molecular testing. AB, Canada: Oncologist. Available at https://www.albertahealthservices.ca/assets/wf/lab/wf-lab-breast-cancer-molecular-testing-oncologist.pdf . Accessed 13 Nov 2017.
Bank of Canada. Home>Rates and Statistics>Related Information>Inflation Calculator [Web resource]. Ottawa, ON: Bank of Canada. Available at www.bankofcanada.ca/en/rates/inflationcalc.html. Accessed 20 June 2013.
Statistics Canada, National Center for Health Statistics, Centers for Disease Control and Prevention: Joint Canada/United States Survey of Health, 2002–03; 2004.
McKenna C, Claxton K. Addressing adoption and research design decisions simultaneously: the role of value of sample information analysis. Med Decis Making. 2011;31:853–65.
pubmed: 21393558
Laupacis A, Feeny D, Detsky AS, Tugwell PX. Tentative guidelines for using clinical and economic evaluations revisited. CMAJ. 1993;148:927–9.
pubmed: 8448707 pmcid: 1490721
Laupacis A. Economic evaluations in the Canadian common drug review. Pharmacoeconomics. 2006;24:1157–62.
pubmed: 17067199
Sparano JA. TAILORx: trial assigning individualized options for treatment (Rx). Clin Breast Cancer. 2006;7:347–50.
pubmed: 17092406
Hayes DF. Targeting adjuvant chemotherapy: a good idea that needs to be proven! J Clin Oncol. 2012;30:1264–7.
pubmed: 22355050
Bartlett J, Canney P, Campbell A, Cameron D, Donovan J, Dunn J, et al. Selecting breast cancer patients for chemotherapy: the opening of the UK OPTIMA trial. Clin Oncol. 2013;25:109–16.
Sparano JA, Gray RJ, Makower DF, Pritchard KI, Albain KS, Hayes DF, et al. Prospective validation of a 21-gene expression assay in breast cancer. N Engl J Med. 2015;373:2005–14.
pubmed: 26412349 pmcid: 4701034
Butts C, Kamel-Reid S, Batist G, Chia S, Blanke C, Moore M, et al. Benefits, issues, and recommendations for personalized medicine in oncology in Canada. Curr Oncol. 2013;20:e475–83.
pubmed: 24155644 pmcid: 3805416
Filipits M, Rudas M, Jakesz R, Dubsky P, Fitzal F, Singer CF, et al. A new molecular predictor of distant recurrence in ER-positive, HER2-negative breast cancer adds independent information to conventional clinical risk factors. Clin Cancer Res. 2011;17:6012–20.
pubmed: 21807638
Parker JS, Mullins M, Cheang MC, Leung S, Voduc D, Vickery T, et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol. 2009;27:1160–7.
pubmed: 19204204 pmcid: 19204204
Tang G, Cuzick J, Costantino JP, Dowsett M, Forbes JF, Crager M, et al. Risk of recurrence and chemotherapy benefit for patients with node-negative, estrogen receptor-positive breast cancer: recurrence score alone and integrated with pathologic and clinical factors. J Clin Oncol. 2011;29:4365–72.
pubmed: 22010013 pmcid: 3221521
Duffy MJ, Harbeck N, Nap M, Molina R, Nicolini A, Senkus E, et al. Clinical use of biomarkers in breast cancer: updated guidelines from the European Group on Tumor Markers (EGTM). Eur J Cancer. 2017;75:284–98.
pubmed: 28259011
National Institute for Health and Care Excellence. Overview—tumour profiling tests to guide adjuvant chemotherapy decisions in people with breast cancer (update of DG10). Issue date: November 2017.
van't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature. 2002;415:530–6.
Cardoso F, van't Veer LJ, Bogaerts J, Slaets L, Viale G, Delaloge S, et al. 70-Gene signature as an aid to treatment decisions in early-stage breast cancer. N Engl J Med. 2016;375:717–29.
pubmed: 27557300
Briggs AH, Ades AE, Price MJ. Probabilistic sensitivity analysis for decision trees with multiple branches: use of the Dirichlet distribution in a Bayesian framework. Med Decis Making. 2003;23:341–50.
pubmed: 12926584
Blum JL, Flynn PJ, Yothers G, Asmar L, Geyer CE, Jacobs SA, et al. Interim joint analysis of the ABC (anthracyclines in early breast cancer) phase III trials (USOR 06-090, NSABP B-46I/USOR 07132, NSABP B-49 [NRG Oncology]) comparing docetaxel+cyclophosphamide (TC) v anthracycline/taxane-based chemotherapy regimens (TaxAC) in women with high-risk, HER2-negative breast cancer. J Clin Oncol. 2016;34.
Jones S, Holmes FA, O'Shaughnessy J, Blum JL, Vukelja SJ, McIntyre KJ, et al. Docetaxel with cyclophosphamide is associated with an overall survival benefit compared with doxorubicin and cyclophosphamide: 7-year follow-up of US Oncology Research Trial 9735. J Clin Oncol. 2009;27:1177–83.
pubmed: 19204201
Ontario Ministry of Health and Long-Term Care. Ontario Health Insurance (OHIP) schedule of benefits and fees; 2007. http://www.health.gov.on.ca/english/providers/program/ohip/sob/sobmn.html . Accessed 13 Aug 2017.
Mittmann N, Verma S, Koo M, Alloul K, Trudeau M. Cost effectiveness of tac versus fac in adjuvant treatment of node-positive breast cancer. Curr Oncol. 2010;17:7–16.
pubmed: 20179798 pmcid: 2826781
Lathia N, Isogai PK, De Angelis C, Smith TJ, Cheung M, Mittmann N, et al. Cost-effectiveness of filgrastim and pegfilgrastim as primary prophylaxis against febrile neutropenia in lymphoma patients. J Natl Cancer Inst. 2013;105:1078–85.
pubmed: 23873405
Skedgel C, Rayson D, Younis T. The cost-utility of sequential adjuvant trastuzumab in women with Her2/Neu-positive breast cancer: an analysis based on updated results from the HERA Trial. Value Health. 2009;12:641–8.
pubmed: 19490562
Guanella R, Ducruet T, Johri M, Miron MJ, Roussin A, Desmarais S, et al. Economic burden and cost determinants of deep vein thrombosis during 2 years following diagnosis: a prospective evaluation. J Thromb Haemost. 2011;9:2397–405.
pubmed: 21951970
Wehler E, Zhao Z, Pinar Bilir S, Munakata J, Barber B. Economic burden of toxicities associated with treating metastatic melanoma in eight countries. Eur J Health Econ. 2017;18:49–58.
pubmed: 26721505
Levy AR, Zou D, Risebrough N, Buckstein R, Kim T, Brereton N. Cost-effectiveness in Canada of azacitidine for the treatment of higher-risk myelodysplastic syndromes. Curr Oncol. 2014;21:e29–40.
pubmed: 24523619 pmcid: 3921046
Peasgood T, Ward SE, Brazier J. Health-state utility values in breast cancer. Expert Rev Pharm Outcomes Res. 2010;10:553–66.
Lucioni C, Finelli C, Mazzi S, Oliva EN. Costs and quality of life in patients with myelodysplastic syndromes. Am J Blood Res. 2013;3:246–59.
pubmed: 23997987 pmcid: 3755523
Enden T, Wik HS, Kvam AK, Haig Y, Klow NE, Sandset PM. Health-related quality of life after catheter-directed thrombolysis for deep vein thrombosis: secondary outcomes of the randomised, non-blinded, parallel-group CaVenT study. BMJ Open. 2013;3:e002984.
pubmed: 23988361 pmcid: 3758969

Auteurs

Malek B Hannouf (MB)

Department of Surgery, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada.

Gregory S Zaric (GS)

Ivey School of Business, Western University, London, ON, Canada.
Department of Epidemiology and Biostatistics, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada.

Phillip Blanchette (P)

London Regional Cancer Program, Department of Oncology, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada.

Christine Brezden-Masley (C)

Faculty of Medicine, University of Toronto, Toronto, ON, Canada.
Division of Hematology and Oncology, St. Michael's Hospital, Toronto, ON, Canada.

Mike Paulden (M)

School of Public Health, University of Alberta, Edmonton, AB, Canada.

Christopher McCabe (C)

The Institute of Health Economics, Edmonton, AB, Canada.
Faculty of Medicine, Department of Emergency Medicine, University of Alberta, Edmonton, AB, Canada.

Jacques Raphael (J)

London Regional Cancer Program, Department of Oncology, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada.

Muriel Brackstone (M)

Department of Surgery, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada. muriel.brackstone@lhsc.on.ca.
London Regional Cancer Program, Department of Oncology, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada. muriel.brackstone@lhsc.on.ca.

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