Targeted therapy for patients with chronic myeloid leukemia: clinical trial experience and challenges in inter-trial comparisons

References

• Rowley JD. Letter: A new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature 1973;243:290–293.
   PubMed Web of Science ®Google Scholar
• Quintás-Cardama A, Cortes J. Molecular biology of bcr-abl1-positive chronic myeloid leukemia. Blood 2009;113:1619–1630.
   PubMed Web of Science ®Google Scholar
• Howlader N, Noone A, Krapcho M, . SEER Cancer Statistics Review, 1975-2008. Based on November 2010 SEER data submission, posted to the SEER web site 2011. Bethesda, MD: National Cancer Institute. Available from: http://seer.cancer.gov/csr/1975_2008/
   Google Scholar
• Perrotti D, Jamieson C, Goldman J, . Chronic myeloid leukemia: mechanisms of blastic transformation. J Clin Invest 2010;120:2254–2264.
   PubMed Web of Science ®Google Scholar
• Druker BJ, Tamura S, Buchdunger E, . Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med 1996;2:561–566.
   PubMed Web of Science ®Google Scholar
• Okimoto RA, Van Etten RA. Navigating the road toward optimal initial therapy for chronic myeloid leukemia. Curr Opin Hematol 2011;18:89–97.
   PubMed Web of Science ®Google Scholar
• O’Brien SG, Guilhot F, Larson RA, .; IRIS Investigators. Imatinib compared with interferon and low-dose cytarabine for newly diagnosed chronic-phase chronic myeloid leukemia. N Engl J Med 2003;348:994–1004.
   PubMed Web of Science ®Google Scholar
• Deininger M, O’Brien SG, Guilhot F, . International randomized study of interferon vs STI571 (IRIS) 8-year follow up: sustained survival and low risk for progression or events in patients with newly diagnosed chronic myeloid leukemia in chronic phase (CML-CP) treated with imatinib. Blood 2009;114(Suppl. 1): Abstract 1126.
   Google Scholar
• Druker BJ, Guilhot F, O’Brien SG, .; IRIS Investigators. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N Engl J Med 2006;355:2408–2417.
   PubMed Web of Science ®Google Scholar
• Weisberg E, Manley PW, Breitenstein W, . Characterization of AMN107, a selective inhibitor of native and mutant Bcr-Abl. Cancer Cell 2005;7:129–141.
   PubMed Web of Science ®Google Scholar
• Lombardo LJ, Lee FY, Chen P, . Discovery of N-(2-chloro-6-methyl-phenyl)-2-(6-(4-(2-hydroxyethyl)-piperazin-1-yl)-2-methylpyrimidin-4-ylamino)thiazole-5-carboxamide (BMS-354825), a dual Src/Abl kinase inhibitor with potent antitumor activity in preclinical assays. J Med Chem 2004;47:6658–6661.
   PubMed Web of Science ®Google Scholar
• Kantarjian HM, Giles F, Gattermann N, . Nilotinib (formerly AMN107), a highly selective BCR-ABL tyrosine kinase inhibitor, is effective in patients with Philadelphia chromosome-positive chronic myelogenous leukemia in chronic phase following imatinib resistance and intolerance. Blood 2007;110:3540–3546.
   PubMed Web of Science ®Google Scholar
• Kantarjian HM, Giles FJ, Bhalla KN, . Nilotinib is effective in patients with chronic myeloid leukemia in chronic phase after imatinib resistance or intolerance: 24-month follow-up results. Blood 2011;117:1141–1145.
   PubMed Web of Science ®Google Scholar
• Cortes JE, Hochhaus A, le Coutre PD, . Minimal cross-intolerance with nilotinib in patients with chronic myeloid leukemia in chronic or accelerated phase who are intolerant to imatinib. Blood 2011;117:5600–5606.
   PubMed Web of Science ®Google Scholar
• Kantarjian H, Pasquini R, Hamerschlak N, . Dasatinib or high-dose imatinib for chronic-phase chronic myeloid leukemia after failure of first-line imatinib: a randomized phase 2 trial. Blood 2007;109: 5143–5150.
   PubMed Web of Science ®Google Scholar
• Hochhaus A, Kantarjian HM, Baccarani M, . Dasatinib induces notable hematologic and cytogenetic responses in chronic-phase chronic myeloid leukemia after failure of imatinib therapy. Blood 2007;109:2303–2309.
   PubMed Web of Science ®Google Scholar
• Cortes J, Rousselot P, Kim DW, . Dasatinib induces complete hematologic and cytogenetic responses in patients with imatinib-resistant or -intolerant chronic myeloid leukemia in blast crisis. Blood 2007;109:3207–3213.
   PubMed Web of Science ®Google Scholar
• Guilhot F, Apperley J, Kim DW, . Dasatinib induces significant hematologic and cytogenetic responses in patients with imatinib-resistant or -intolerant chronic myeloid leukemia in accelerated phase. Blood 2007;109:4143–4150.
   PubMed Web of Science ®Google Scholar
• Apperley JF, Cortes JE, Kim DW, . Dasatinib in the treatment of chronic myeloid leukemia in accelerated phase after imatinib failure: the START A trial. J Clin Oncol 2009;27:3472–3479.
   PubMed Web of Science ®Google Scholar
• Hochhaus A, Baccarani M, Deininger M, . Dasatinib induces durable cytogenetic responses in patients with chronic myelogenous leukemia in chronic phase with resistance or intolerance to imatinib. Leukemia 2008;22:1200–1206.
   PubMed Web of Science ®Google Scholar
• Kantarjian H, Pasquini R, Levy V, . Dasatinib or high-dose imatinib for chronic-phase chronic myeloid leukemia resistant to imatinib at a dose of 400 to 600 milligrams daily: two-year follow-up of a randomized phase 2 study (START-R). Cancer 2009;115:4136–4147.
   PubMed Web of Science ®Google Scholar
• Shah NP, Kantarjian HM, Kim DW, . Intermittent target inhibition with dasatinib 100 mg once daily preserves efficacy and improves tolerability in imatinib-resistant and -intolerant chronic-phase chronic myeloid leukemia. J Clin Oncol 2008;26:3204–3212.
   PubMed Web of Science ®Google Scholar
• Khoury HJ, Goldberg SL, Mauro MJ, . Dasatinib lack of cross intolerance to imatinib in patients (pts) with chronic myelogenous leukemia chronic phase (CML-CP) intolerant to imatinib: a retrospective analysis of safety. J Clin Oncol 2008;26(15 Suppl.): Abstract 7015.
   Google Scholar
• Fava C, Kantarjian HM, Jabbour E, . Failure to achieve a complete hematologic response at the time of a major cytogenetic response with second-generation tyrosine kinase inhibitors is associated with a poor prognosis among patients with chronic myeloid leukemia in accelerated or blast phase. Blood 2009;113:5058–5063.
   PubMed Web of Science ®Google Scholar
• Saglio G, Kim DW, Issaragrisil S, .; ENESTnd Investigators. Nilotinib versus imatinib for newly diagnosed chronic myeloid leukemia. N Engl J Med 2010;362:2251–2259.
   PubMed Web of Science ®Google Scholar
• Kantarjian H, Shah NP, Hochhaus A, . Dasatinib versus imatinib in newly diagnosed chronic-phase chronic myeloid leukemia. N Engl J Med 2010;362:2260–2270.
   PubMed Web of Science ®Google Scholar
• DeAngelo DJ, Attar EC. Use of dasatinib and nilotinib in imatinib-resistant chronic myeloid leukemia: translating preclinical findings to clinical practice. Leuk Lymphoma 2010;51:363–375.
   PubMed Web of Science ®Google Scholar
• Puttini M, Coluccia AM, Boschelli F, . In vitro and in vivo activity of SKI-606, a novel Src-Abl inhibitor, against imatinib-resistant Bcr-Abl + neoplastic cells. Cancer Res 2006;66:11314–11322.
   PubMed Web of Science ®Google Scholar
• Golas JM, Arndt K, Etienne C, . SKI-606, a 4-anilino-3-quinolinecarbonitrile dual inhibitor of Src and Abl kinases, is a potent antiproliferative agent against chronic myelogenous leukemia cells in culture and causes regression of K562 xenografts in nude mice. Cancer Res 2003;63:375–381.
   PubMed Web of Science ®Google Scholar
• Redaelli S, Piazza R, Rostagno R, . Activity of bosutinib, dasatinib, and nilotinib against 18 imatinib-resistant BCR/ABL mutants. J Clin Oncol 2009;27:469–471.
   PubMed Web of Science ®Google Scholar
• Cortes JE, Kantarjian HM, Brummendorf TH, . Safety and efficacy of bosutinib (SKI-606) in chronic phase Philadelphia chromosome-positive CML patients with resistance or intolerance to imatinib. Blood 2011;118:4567–4576.
   PubMed Web of Science ®Google Scholar
• Gambacorti-Passerini C, Kim D-W, Kantarjian HM, . An ongoing phase 3 study of bosutinib (SKI-606) versus imatinib in patients with newly diagnosed chronic phase chronic myeloid leukemia. Blood 2010;116(Suppl. 1): Abstract 208.
   Google Scholar
• Cortes J, Talpaz M, Bixby D, . A phase 1 trial of oral ponatinib (AP24534) in patients with refractory chronic myelogenous leukemia (CML) and other hematologic malignancies: emerging safety and clinical response findings. Blood 2010;116(Suppl. 1): Abstract 210.
   Google Scholar
• Cortes-Franco J, Dombret H, Schafhausen P, . Danusertib hydrochloride (PHA-739358), a multi-kinase aurora inhibitor, elicits clinical benefit in advanced chronic myeloid leukemia and Philadelphia chromosome positive acute lymphoblastic leukemia. Blood 2009;114(Suppl. 1): Abstract 864.
   Google Scholar
• Carpiuc KT, Rosti G, Castagnetti F, . Indirect comparisons of second-generation tyrosine kinase inhibitors in CML: case study using baseline population characteristics. Onco Targets Ther 2010;3:205–210.
   PubMed Web of Science ®Google Scholar
• Song F, Loke YK, Walsh T, . Methodological problems in the use of indirect comparisons for evaluating healthcare interventions: survey of published systematic reviews. BMJ 2009;338:b1147.
   PubMed Web of Science ®Google Scholar
• Signorovitch JE, Wu EQ, Yu AP, . Comparative effectiveness without head-to-head trials: a method for matching-adjusted indirect comparisons applied to psoriasis treatment with adalimumab or etanercept. Pharmacoeconomics 2010;28:935–945.
   PubMed Web of Science ®Google Scholar
• Talpaz M, Shah NP, Kantarjian H, . Dasatinib in imatinib-resistant Philadelphia chromosome-positive leukemias. N Engl J Med 2006;354:2531–2541.
   PubMed Web of Science ®Google Scholar
• Shah NP, Kim DW, Kantarjian H, . Potent, transient inhibition of BCR-ABL with dasatinib 100 mg daily achieves rapid and durable cytogenetic responses and high transformation-free survival rates in chronic phase chronic myeloid leukemia patients with resistance, suboptimal response or intolerance to imatinib. Haematologica 2010;95:232–240.
   PubMed Web of Science ®Google Scholar
• Giles FJ, Abruzzese E, Rosti G, . Nilotinib is active in chronic and accelerated phase chronic myeloid leukemia following failure of imatinib and dasatinib therapy. Leukemia 2010;24:1299–1301.
   PubMed Web of Science ®Google Scholar
• Al-Kali A, Kantarjian H, Shan J, . Current event-free survival after sequential tyrosine kinase inhibitor therapy for chronic myeloid leukemia. Cancer 2011;117:327–335.
   PubMed Web of Science ®Google Scholar
• Baccarani M, Saglio G, Goldman J, .; European LeukemiaNet. Evolving concepts in the management of chronic myeloid leukemia: recommendations from an expert panel on behalf of the European LeukemiaNet. Blood 2006;108:1809–1820.
   PubMed Web of Science ®Google Scholar
• Yu AP, Johnson S, Wang ST, . Cost utility of adalimumab versus infliximab maintenance therapies in the United States for moderately to severely active Crohn's disease. Pharmacoeconomics 2009;27:609–621.
   PubMed Web of Science ®Google Scholar
• Signorovitch JE, Wu EQ, Betts KA, . Comparative efficacy of nilotinib and dasatinib in newly diagnosed chronic myeloid leukemia: a matching-adjusted indirect comparison of randomized trials. Curr Med Res Opin 2011;27:1263–1271.
   PubMed Web of Science ®Google Scholar
• O’Brien S, Berman E, Moore JO, . NCCN Task Force report: tyrosine kinase inhibitor therapy selection in the management of patients with chronic myelogenous leukemia. J Natl Compr Canc Netw 2011;9(Suppl. 2):S1–S25.
   PubMed Web of Science ®Google Scholar
• Baccarani M, Cortes J, Pane F, .; European LeukemiaNet. Chronic myeloid leukemia: an update of concepts and management recommendations of European LeukemiaNet. J Clin Oncol 2009;27:6041–6051.
   PubMed Web of Science ®Google Scholar
• Agrawal M, Garg RJ, Cortes J, . Tyrosine kinase inhibitors: the first decade. Curr Hematol Malig Rep 2010;5:70–80.
   PubMed Web of Science ®Google Scholar
• Hughes T, Saglio G, Branford S, . Impact of baseline BCR-ABL mutations on response to nilotinib in patients with chronic myeloid leukemia in chronic phase. J Clin Oncol 2009;27: 4204–4210.
   PubMed Web of Science ®Google Scholar
• Müller MC, Cortes JE, Kim DW, . Dasatinib treatment of chronic-phase chronic myeloid leukemia: analysis of responses according to preexisting BCR-ABL mutations. Blood 2009;114: 4944–4953.
   PubMed Web of Science ®Google Scholar
• Branford S, Melo JV, Hughes TP. Selecting optimal second-line tyrosine kinase inhibitor therapy for chronic myeloid leukemia patients after imatinib failure: does the BCR-ABL mutation status really matter? Blood 2009;114:5426–5435.
   PubMed Web of Science ®Google Scholar
• O’Hare T, Eide CA, Deininger MW. Bcr-Abl kinase domain mutations, drug resistance, and the road to a cure for chronic myeloid leukemia. Blood 2007;110:2242–2249.
   PubMed Web of Science ®Google Scholar
• de Groot RP, Raaijmakers JA, Lammers JW, . STAT5 activation by BCR-Abl contributes to transformation of K562 leukemia cells. Blood 1999;94:1108–1112.
   PubMed Web of Science ®Google Scholar
• Sattler M, Mohi MG, Pride YB, . Critical role for Gab2 in transformation by BCR/ABL. Cancer Cell 2002;1:479–492.
   PubMed Web of Science ®Google Scholar
• Wang L, Giannoudis A, Lane S, . Expression of the uptake drug transporter hOCT1 is an important clinical determinant of the response to imatinib in chronic myeloid leukemia. Clin Pharmacol Ther 2008;83:258–264.
   PubMed Web of Science ®Google Scholar
• White DL, Saunders VA, Dang P, . Most CML patients who have a suboptimal response to imatinib have low OCT-1 activity: higher doses of imatinib may overcome the negative impact of low OCT-1 activity. Blood 2007;110:4064–4072.
   PubMed Web of Science ®Google Scholar
• Giannoudis A, Davies A, Lucas CM, . Effective dasatinib uptake may occur without human organic cation transporter 1 (hOCT1): implications for the treatment of imatinib-resistant chronic myeloid leukemia. Blood 2008;112:3348–3354.
   PubMed Web of Science ®Google Scholar
• Davies A, Jordanides NE, Giannoudis A, . Nilotinib concentration in cell lines and primary CD34 + chronic myeloid leukemia cells is not mediated by active uptake or efflux by major drug transporters. Leukemia 2009;23:1999–2006.
   PubMed Web of Science ®Google Scholar
• Dohse M, Scharenberg C, Shukla S, . Comparison of ATP-binding cassette transporter interactions with the tyrosine kinase inhibitors imatinib, nilotinib, and dasatinib. Drug Metab Dispos 2010;38: 1371–1380.
   PubMed Web of Science ®Google Scholar
• Hegedus C, Ozvegy-Laczka C, Apati A, . Interaction of nilotinib, dasatinib and bosutinib with ABCB1 and ABCG2: implications for altered anti-cancer effects and pharmacological properties. Br J Pharmacol 2009;158: 1153–1164.
   PubMed Web of Science ®Google Scholar
• Testa L, Zoccai GB, Porto I, . Adjusted indirect meta-analysis of aspirin plus warfarin at international normalized ratios 2 to 3 versus aspirin plus clopidogrel after acute coronary syndromes. Am J Cardiol 2007;99:1637–1642.
   PubMed Web of Science ®Google Scholar
• Vis PM, van Baardewijk M, Einarson TR. Duloxetine and venlafaxine-XR in the treatment of major depressive disorder: a meta-analysis of randomized clinical trials. Ann Pharmacother 2005;39:1798–1807.
   PubMed Web of Science ®Google Scholar
• Nixon R, Bansback N, Brennan A. The efficacy of inhibiting tumour necrosis factor alpha and interleukin 1 in patients with rheumatoid arthritis: a meta-analysis and adjusted indirect comparisons. Rheumatology (Oxford) 2007;46:1140–1147.
   PubMed Web of Science ®Google Scholar
• Griffin S, Bojke L, Main C, . Incorporating direct and indirect evidence using Bayesian methods: an applied case study in ovarian cancer. Value Health 2006;9:123–131.
   PubMed Web of Science ®Google Scholar