Novel anticancer agents for multiple myeloma: a review of the evidence for their therapeutic and economic value

References

• McCabe C, Bergmann L, Bosanquet N et al. Market and patient access to new oncology products in Europe: a current, multidisciplinary perspective. Ann. Oncol.20(3), 403–412 (2009).
   PubMed Web of Science ®Google Scholar
• Garber AM, McClellan MB. Satisfaction guaranteed – ‘payment by results’ for biologic agents. N. Engl. J. Med.357(16), 1575–1577 (2007).
   PubMed Web of Science ®Google Scholar
• Anderson KC. Lenalidomide and thalidomide: mechanisms of action – similarities and differences. Semin. Hematol.42(Suppl. 4), S3–S8 (2005).
   PubMed Web of Science ®Google Scholar
• Kane RC, Bross PF, Farrell AT, Pazdur R. Velcade: U.S. FDA approval for the treatment of multiple myeloma progressing on prior therapy. Oncologist8(6), 508–513 (2003).
   PubMed Web of Science ®Google Scholar
• Fuchs SY. The role of ubiquitin–proteasome pathway in oncogenic signaling. Cancer Biol. Ther.1(4), 337–341 (2002).
   PubMed Web of Science ®Google Scholar
• Richardson PG, Hideshima T, Mitsiades C, Anderson KC. The emerging role of novel therapies for the treatment of relapsed myeloma. J. Natl Compr. Cancer Netw.5(2), 149–162 (2007).
   PubMedGoogle Scholar
• Armoiry X, Fagnani F, Benboubker L et al. Management of relapsed or refractory multiple myeloma in French hospitals and estimation of associated direct costs: a multi-centre retrospective cohort study. J. Clin. Pharm. Ther.36(1), 19–26 (2011).
   PubMed Web of Science ®Google Scholar
• Bonkowski J, Vermeulen LC, Kolesar JM. The clinical utility of lenalidomide in multiple myeloma and myelodysplastic syndromes. J. Oncol. Pharm. Pract.16(4), 223–232 (2009).
   PubMedGoogle Scholar
• Knox C, Law V, Jewison T et al. Drug Bank 3.0: a comprehensive resource for ‘omics’ research on drugs. Nucl. Acids Res.39(Database issue), D1035–D1041 (2011).
   PubMed Web of Science ®Google Scholar
• Mitsiades CS, Hideshima T, Chauhan D et al. Emerging treatments for multiple myeloma: beyond immunomodulatory drugs and bortezomib. Semin. Hematol.46(2), 166–175 (2009).
   PubMed Web of Science ®Google Scholar
• Drummond MF, Schulpher MJ, Torrance GW, O’Brien BJ, Stoddart GL. Methods for the Economic Evaluation of Health Care Programmes (Third Edition). Oxford University Press, Oxford, UK (2005).
   Google Scholar
• Palumbo A, Attal M, Roussel M. Shifts in the therapeutic paradigm for patients newly diagnosed with multiple myeloma: maintenance therapy and overall survival. Clin. Cancer Res.17(6), 1253–1263 (2011).
   PubMed Web of Science ®Google Scholar
• Hulin C, Facon T, Rodon P et al. Efficacy of melphalan and prednisone plus thalidomide in patients older than 75 years with newly diagnosed multiple myeloma: IFM 01/01 trial. J. Clin. Oncol.27(22), 3664–3670 (2009).
   PubMed Web of Science ®Google Scholar
• Ludwig H, Hajek R, Tothova E et al. Thalidomide–dexamethasone compared with melphalan–prednisolone in elderly patients with multiple myeloma. Blood113(15), 3435–3442 (2009).
   PubMed Web of Science ®Google Scholar
• Palumbo A, Bringhen S, Caravita T et al. Oral melphalan and prednisone chemotherapy plus thalidomide compared with melphalan and prednisone alone in elderly patients with multiple myeloma: randomised controlled trial. Lancet367(9513), 825–831 (2006).
   PubMed Web of Science ®Google Scholar
• Palumbo A, Bringhen S, Liberati AM et al. Oral melphalan, prednisone, and thalidomide in elderly patients with multiple myeloma: updated results of a randomized controlled trial. Blood112(8), 3107–3114 (2008).
   PubMed Web of Science ®Google Scholar
• Waage A, Gimsing P, Fayers P et al. Melphalan and prednisone plus thalidomide or placebo in elderly patients with multiple myeloma. Blood116(9), 1405–1412 (2010).
   PubMed Web of Science ®Google Scholar
• Wijermans P, Schaafsma M, Termorshuizen F et al. Phase III study of the value of thalidomide added to melphalan plus prednisone in elderly patients with newly diagnosed multiple myeloma: the HOVON 49 study. J. Clin. Oncol.28(19), 3160–3166 (2010).
   PubMed Web of Science ®Google Scholar
• Mateos MV, Richardson PG, Schlag R et al. Bortezomib plus melphalan and prednisone compared with melphalan and prednisone in previously untreated multiple myeloma: updated follow-up and impact of subsequent therapy in the Phase III VISTA trial. J. Clin. Oncol.28(13), 2259–2266 (2010).
   PubMed Web of Science ®Google Scholar
• San Miguel JF, Schlag R, Khuageva NK et al. Bortezomib plus melphalan and prednisone for initial treatment of multiple myeloma. N. Engl. J. Med.359(9), 906–917 (2008).
   PubMed Web of Science ®Google Scholar
• Mateos MV, Oriol A, Martinez-Lopez J et al. Bortezomib, melphalan, and prednisone versus bortezomib, thalidomide, and prednisone as induction therapy followed by maintenance treatment with bortezomib and thalidomide versus bortezomib and prednisone in elderly patients with untreated multiple myeloma: a randomised trial. Lancet Oncol.11(10), 934–941 (2010).
   PubMed Web of Science ®Google Scholar
• Palumbo A, Bringhen S, Rossi D. Bortezomib–melphalan–prednisone–thalidomide followed by maintenance with bortezomib–thalidomide versus bortezomib–melphalan-prednisone for initial treatment of multiple myeloma: a randomised controlled trial. J. Clin. Oncol.28(34), 5101–5109 (2010).
   PubMed Web of Science ®Google Scholar
• Zonder JA, Crowley J, Hussein MA et al. Lenalidomide and high-dose dexamethasone compared with dexamethasone as initial therapy for multiple myeloma: a randomized Southwest Oncology Group trial (S0232). Blood116(26), 5838–5841 (2010).
   PubMed Web of Science ®Google Scholar
• Rajkumar SV, Blood E, Vesole D, Fonseca R, Greipp PR. Phase III clinical trial of thalidomide plus dexamethasone compared with dexamethasone alone in newly diagnosed multiple myeloma: a clinical trial coordinated by the Eastern Cooperative Oncology Group. J. Clin. Oncol.24(3), 431–436 (2006).
   PubMed Web of Science ®Google Scholar
• Rajkumar SV, Rosinol L, Hussein M et al. Multicenter, randomized, double-blind, placebo-controlled study of thalidomide plus dexamethasone compared with dexamethasone as initial therapy for newly diagnosed multiple myeloma. J. Clin. Oncol.26(13), 2171–2177 (2008).
   PubMed Web of Science ®Google Scholar
• Facon T, Mary JY, Hulin C et al. Melphalan and prednisone plus thalidomide versus melphalan and prednisone alone or reduced-intensity autologous stem cell transplantation in elderly patients with multiple myeloma (IFM 99–06): a randomised trial. Lancet370(9594), 1209–1218 (2007).
   PubMed Web of Science ®Google Scholar
• Barlogie B, Pineda-Roman M, van Rhee F et al. Thalidomide arm of Total Therapy 2 improves complete remission duration and survival in myeloma patients with metaphase cytogenetic abnormalities. Blood112(8), 3115–3121 (2008).
   PubMed Web of Science ®Google Scholar
• Barlogie B, Tricot G, Anaissie E et al. Thalidomide and hematopoietic-cell transplantation for multiple myeloma. N. Engl. J. Med.354(10), 1021–1030 (2006).
   PubMed Web of Science ®Google Scholar
• Lokhorst HM, van der Holt B, Zweegman S et al. A randomized Phase 3 study on the effect of thalidomide combined with adriamycin, dexamethasone, and high-dose melphalan, followed by thalidomide maintenance in patients with multiple myeloma. Blood115(6), 1113–1120 (2010).
   PubMed Web of Science ®Google Scholar
• Spencer A, Prince HM, Roberts AW et al. Consolidation therapy with low-dose thalidomide and prednisolone prolongs the survival of multiple myeloma patients undergoing a single autologous stem-cell transplantation procedure. J. Clin. Oncol.27(11), 1788–1793 (2009).
   PubMed Web of Science ®Google Scholar
• Harousseau JL, Attal M, Avet-Loiseau H et al. Bortezomib plus dexamethasone is superior to vincristine plus doxorubicin plus dexamethasone as induction treatment prior to autologous stem-cell transplantation in newly diagnosed multiple myeloma: results of the IFM 2005–2001 Phase III trial. J. Clin. Oncol.28(30), 4621–4629 (2010).
   PubMed Web of Science ®Google Scholar
• Cavo M, Tacchetti P, Patriarca F et al. Bortezomib with thalidomide plus dexamethasone compared with thalidomide plus dexamethasone as induction therapy before, and consolidation therapy after, double autologous stem-cell transplantation in newly diagnosed multiple myeloma: a randomised Phase 3 study. Lancet376(9758), 2075–2085 (2010).
   PubMed Web of Science ®Google Scholar
• Richardson PG, Sonneveld P, Schuster MW et al. Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N. Engl. J. Med.352(24), 2487–2498 (2005).
   PubMed Web of Science ®Google Scholar
• Richardson PG, Sonneveld P, Schuster M et al. Extended follow-up of a Phase 3 trial in relapsed multiple myeloma: final time-to-event results of the APEX trial. Blood110(10), 3557–3560 (2007).
   PubMed Web of Science ®Google Scholar
• Orlowski RZ, Nagler A, Sonneveld P et al. Randomized Phase III study of pegylated liposomal doxorubicin plus bortezomib compared with bortezomib alone in relapsed or refractory multiple myeloma: combination therapy improves time to progression. J. Clin. Oncol.25(25), 3892–3901 (2007).
   PubMed Web of Science ®Google Scholar
• Mikhael JR, Belch AR, Prince HM et al. High response rate to bortezomib with or without dexamethasone in patients with relapsed or refractory multiple myeloma: results of a global Phase 3b expanded access program. Br. J. Haematol.144(2), 169–175 (2008).
   PubMedGoogle Scholar
• Weber DM, Chen C, Niesvizky R et al. Lenalidomide plus dexamethasone for relapsed multiple myeloma in North America. N. Engl. J. Med.357(21), 2133–2142 (2007).
   PubMed Web of Science ®Google Scholar
• Dimopoulos M, Spencer A, Attal M et al. Lenalidomide plus dexamethasone for relapsed or refractory multiple myeloma. N. Engl. J. Med.357(21), 2123–2132 (2007).
   PubMed Web of Science ®Google Scholar
• Dimopoulos MA, Chen C, Spencer A et al. Long-term follow-up on overall survival from the MM-009 and MM-010 Phase III trials of lenalidomide plus dexamethasone in patients with relapsed or refractory multiple myeloma. Leukemia23(11), 2147–2152 (2009).
   PubMed Web of Science ®Google Scholar
• Castaneda CP, Brandenburg NA, Bwire R, Burton GH, Zeldis JB. Erythema multiforme/Stevens–Johnson syndrome/toxic epidermal necrolysis in lenalidomide-treated patients. J. Clin. Oncol.27(1), 156–157 (2009).
   PubMed Web of Science ®Google Scholar
• Verelst SGR, Termorshuizen F, Uyl-de Groot CA et al. Effect of thalidomide with melphalan and prednisone on health-related quality of life (HRQoL) in elderly patients with newly diagnosed multiple myeloma: a prospective analysis in a randomized trial. Ann. Hematol.90(12), 1427–1439 (2011).
   PubMed Web of Science ®Google Scholar
• Dubois D, Dhawan R, van de Velde H et al. Descriptive and prognostic value of patient-reported outcomes: the bortezomib experience in relapsed and refractory multiple myeloma. J. Clin. Oncol.24(6), 976–982 (2006).
   PubMed Web of Science ®Google Scholar
• Lee SJ, Richardson PG, Sonneveld P et al. Bortezomib is associated with better health-related quality of life than high-dose dexamethasone in patients with relapsed multiple myeloma: results from the APEX study. Br. J. Haematol.143(4), 511–519 (2008).
   PubMed Web of Science ®Google Scholar
• Mehta J, Duff SB, Gupta S. Cost effectiveness of bortezomib in the treatment of advanced multiple myeloma. Managed Care Interf.17(9), 52–61 (2004).
   PubMedGoogle Scholar
• Hornberger J, Rickert J, Dhawan R, Liwing J, Aschan J, Lothgren M. The cost–effectiveness of bortezomib in relapsed/refractory multiple myeloma: Swedish perspective. Eur. J. Haematol.85(6), 484–491 (2010).
   PubMed Web of Science ®Google Scholar
• Moller J, Nicklasson L, Murthy A. Cost–effectiveness of novel relapsed-refractory multiple myeloma therapies in Norway: lenalidomide plus dexamethasone vs bortezomib. J. Med. Econ.14(6), 690–697 (2011).
   PubMedGoogle Scholar
• Zeigler BP, Praehofer H, Kim TG. Theory of Modeling and Simulation: Integrating Discrete Event and Continuous Complex Dynamic Systems (2nd Edition). Academic Press, CA, USA (2000).
   Google Scholar
• Van Agthoven M, Segeren CM, Buijt I et al. A cost–utility analysis comparing intensive chemotherapy alone to intensive chemotherapy followed by myeloablative chemotherapy with autologous stem-cell rescue in newly diagnosed patients with stage II/III multiple myeloma; a prospective randomised Phase III study. Eur. J. Cancer40(8), 1159–1169 (2004).
   PubMed Web of Science ®Google Scholar
• Rowen D, Brazier J, Young T et al. Deriving a preference-based measure for cancer using the EORTC QLQ-C30. Value Health14(5), 721–731 (2011).
   PubMed Web of Science ®Google Scholar
• Mitsiades CS, Davies FE, Laubach JP et al. Future directions of next-generation novel therapies, combination approaches, and the development of personalized medicine in myeloma. J. Clin. Oncol.29(14), 1916–1923 (2011).
   PubMed Web of Science ®Google Scholar
• Glasziou PP, Simes RJ, Gelber RD. Quality adjusted survival analysis. Stat. Med.9(11), 1259–1276 (1990).
   PubMed Web of Science ®Google Scholar
• Simpson KN, Strassburger A, Jones WJ, Dietz B, Rajagopalan R. Comparison of Markov model and discrete-event simulation techniques for HIV. Pharmacoeconomics27(2), 159–165 (2009).
   PubMed Web of Science ®Google Scholar
• Heeg BM, Damen J, Buskens E, Caleo S, de Charro F, van Hout BA. Modelling approaches: the case of schizophrenia. Pharmacoeconomics26(8), 633–648 (2008).
   PubMed Web of Science ®Google Scholar
• Moreau P, Attal M, Pegourie B et al. Achievement of VGPR to induction therapy is an important prognostic factor for longer PFS in the IFM 2005–2001 trial. Blood117(11), 3041–3044 (2010).
   PubMedGoogle Scholar
• Niesvizky R, Richardson PG, Rajkumar SV et al. The relationship between quality of response and clinical benefit for patients treated on the bortezomib arm of the international, randomized, Phase 3 APEX trial in relapsed multiple myeloma. Br. J. Haematol.143(1), 46–53 (2008).
   PubMed Web of Science ®Google Scholar
• Harousseau JL, Attal M, Avet-Loiseau H. The role of complete response in multiple myeloma. Blood114(15), 3139–3146 (2009).
   PubMed Web of Science ®Google Scholar
• Gartlehner G, Moore CG. Direct versus indirect comparisons: a summary of the evidence. Int. J. Technol. Assess. Health Care24(2), 170–177 (2008).
   PubMed Web of Science ®Google Scholar
• Siegel DSD, Martin T, Wang M et al. PX-171-003-A1, an open-label, single-arm, Phase (Ph) II study of carfilzomib (CFZ) in patients (pts) with relapsed and refractory multiple myeloma (R/R MM): long-term follow-up and subgroup analysis. Presented at: American Society of Clinical Oncology Annual Meeting. Chicago, IL, USA, 3–7 June 2011.
   Google Scholar
• Rajkumar SV. Multiple myeloma: 2012 update on diagnosis, risk-stratification, and management. Am. J. Hematol.87(1), 78–88 (2012).
   PubMed Web of Science ®Google Scholar
• Rajkumar SV, Jacobus S, Callander NS et al. Lenalidomide plus high-dose dexamethasone versus lenalidomide plus low-dose dexamethasone as initial therapy for newly diagnosed multiple myeloma: an open-label randomised controlled trial. Lancet Oncol.11(1), 29–37 (2010).
   PubMed Web of Science ®Google Scholar
• Dimopoulos MA, Richardson PG, Brandenburg N et al. A review of second primary malignancy in patients with relapsed or refractory multiple myeloma treated with lenalidomide. Blood119(12), 2764–2767 (2012).
   PubMed Web of Science ®Google Scholar
• Landgren O, Thomas A, Mailankody S. Myeloma and second primary cancers. N. Engl. J. Med.365(23), 2241–2242 (2011).
   PubMed Web of Science ®Google Scholar
• Mahindra A, Cirstea D, Raje N. Novel therapeutic targets for multiple myeloma. Fut. Oncol.6(3), 407–418 (2010).
   PubMedGoogle Scholar
• Schey S, Ramasamy K. Pomalidomide therapy for myeloma. Expert Opin. Invest. Drugs20(5), 691–700 (2011).
   PubMed Web of Science ®Google Scholar
• Khan ML, Stewart AK. Carfilzomib: a novel second-generation proteasome inhibitor. Fut. Oncol.7(5), 607–612 (2011).
   PubMed Web of Science ®Google Scholar
• Lacy MQ, Hayman SR, Gertz MA et al. Pomalidomide (CC4047) plus low-dose dexamethasone as therapy for relapsed multiple myeloma. J. Clin. Oncol.27(30), 5008–5014 (2009).
   PubMed Web of Science ®Google Scholar
• Mikhael JR, Rajkumar V, Roy V et al. Efficacy of pomalidomide plus low-dose dexamethasone in multiple myeloma patients despite previous use of lenalidomide. Presented at: American Society of Clinical Oncology Annual Meeting. Chicago, IL, USA, 3–7 June 2011.
   Google Scholar
• Stewart AK, Kaufman JL, Jakubowiak AJ et al. The effect of carfilzomib (CFZ) in patients (Pts) with bortezomib (BTZ)-naive relapsed or refractory multiple myeloma (MM): updated results from the PX-171–004 study. Presented at: American Society of Clinical Oncology Annual Meeting. Chicago, IL, USA, 3–7 June 2011.
   Google Scholar
• Dimopoulos MA, Jagannath S, Yoon SS et al. Vantage 088: vorinostat in combination with bortezomib in patients with relapsed/refractory multiple myeloma: results of a global, randomized Phase 3 trial. Presented at: American Society of Hematology Annual Meeting. San Diego, CA, USA, 10–13 December 2011.
   Google Scholar
• Richardson PG, Wolf J, Jakubowiak A et al. Perifosine plus bortezomib and dexamethasone in patients with relapsed/refractory multiple myeloma previously treated with bortezomib: results of a multicenter Phase I/II trial. J. Clin. Oncol.29(32), 4243–4249 (2011).
   PubMed Web of Science ®Google Scholar
• Wolf JL, Jakubowiak AJ, Zonder JA et al. Perifosine plus bortezomib and dexamethasone in relapsed / refractory multiple myeloma patients previously treated with bortezomib: final results of a Phase I/II trial. Presented at: American Society of Hematology Annual Meeting. San Diego, CA, USA, 10–13 December 2011.
   Google Scholar
• Wolf JL, Siegel D, Goldschmidt H et al. Phase II trial of the pan-deacetylase inhibitor panobinostat as a single agent in advanced relapsed/refractory multiple myeloma. Leuk. Lymphoma doi:10.3109/10428194.661175 (2012) (Epub ahead of print).
   Google Scholar
• Offidani M, Polloni C, Cavallo F et al. Phase II study of melphalan, thalidomide and prednisone (MPT) combined with oral panobinostat in patients with relapsed/refractory MM. Leuk. Lymphoma doi:10.3109/10428194.664844 (2012) (Epub ahead of print).
   PubMedGoogle Scholar
• Jakubowiak AJ, Benson DM, Bensinger W et al. Phase I trial of anti-CS1 monoclonal antibody elotuzumab in combination with bortezomib in the treatment of relapsed/refractory multiple myeloma. J. Clin. Oncol. doi:10.1200/JCO.37.7069 (2012) (Epub ahead of print).
   PubMedGoogle Scholar
• Jagannath S, Dimopoulos MA, Lonial S. Combined proteasome and histone deacetylase inhibition: a promising synergy for patients with relapsed/refractory multiple myeloma. Leuk. Res.34(9), 1111–1118 (2010).
   PubMed Web of Science ®Google Scholar
• Korde N, Kristinsson SY, Landgren O. Monoclonal gammopathy of undetermined significance (MGUS) and smoldering multiple myeloma (SMM): novel biological insights and development of early treatment strategies. Blood117(21), 5573–5581 (2011).
   PubMed Web of Science ®Google Scholar
• Barlogie B, van Rhee F, Shaughnessy JD Jr et al. Seven-year median time to progression with thalidomide for smoldering myeloma: partial response identifies subset requiring earlier salvage therapy for symptomatic disease. Blood112(8), 3122–3125 (2008).
   PubMed Web of Science ®Google Scholar
• Mateos MV, Lopez-Corral L, Hernandez MT et al. Multicenter, randomized, open-label, Phase III trial of lenalidomide–dexamethasone (len/dex) vs therapeutic abstention in smoldering multiple myeloma at high risk of progression to symptomatic MM: results of the first interim analysis. Presented at: American Society of Hematology Annual Meeting. San Diego, CA, USA, 10–13 December 2011.
   Google Scholar
• Johnson SK, Heuck CJ, Albino AP et al. The use of molecular-based risk stratification and pharmacogenomics for outcome prediction and personalized therapeutic management of multiple myeloma. Int. J. Hematol.94(4), 321–333 (2011).
   PubMed Web of Science ®Google Scholar