Predictive and prognostic biomarkers in the era of new targeted therapies for chronic lymphocytic leukemia

References

• Howlader N, Morton LM, Feuer EJ, et al. Contributions of subtypes of non-Hodgkin lymphoma to mortality trends. Cancer Epidemiol Biomarkers Prev. 2016;25:174–179.
   PubMed Web of Science ®Google Scholar
• Ballman KV. Biomarker: predictive or prognostic? J Clin Oncol. 2015;33:3968–3971.
   PubMed Web of Science ®Google Scholar
• Minden M. Is it time to redefine prognostic and predictive in oncology? J Clin Oncol. 2016;34:1702–1703.
   PubMed Web of Science ®Google Scholar
• Landau DA, Tausch E, Taylor-Weiner AN, et al. Mutations driving CLL and their evolution in progression and relapse. Nature. 2015;526:525–530.
   PubMed Web of Science ®Google Scholar
• Puente XS, Beà S, Valdés-Mas R, et al. Non-coding recurrent mutations in chronic lymphocytic leukaemia. Nature. 2015;526:519–524.
   PubMed Web of Science ®Google Scholar
• Stilgenbauer S, Schnaiter A, Paschka P, et al. Gene mutations and treatment outcome in chronic lymphocytic leukemia: results from the CLL8 trial. Blood. 2014;123:3247–3254.
   PubMed Web of Science ®Google Scholar
• Guièze R, Robbe P, Clifford R, et al. Presence of multiple recurrent mutations confers poor trial outcome of relapsed/refractory CLL. Blood. 2015;126:2110–2117.
   PubMed Web of Science ®Google Scholar
• Zenz T, Vollmer D, Trbusek M, et al. TP53 mutation profile in chronic lymphocytic leukemia: evidence for a disease specific profile from a comprehensive analysis of 268 mutations. Leukemia. 2010;24:2072–2079.
   PubMed Web of Science ®Google Scholar
• Pospisilova S, Gonzalez D, Malcikova J, et al. ERIC recommendations on TP53 mutation analysis in chronic lymphocytic leukemia. Leukemia. 2012;26:1458–1461.
   PubMed Web of Science ®Google Scholar
• Mohr J, Helfrich H, Fuge M, et al. DNA damage-induced transcriptional program in CLL: biological and diagnostic implications for functional p53 testing. Blood. 2011;117:1622–1632.
   PubMed Web of Science ®Google Scholar
• Hallek M, Fischer K, Fingerle-Rowson G, et al. Addition of rituximab to fludarabine and cyclophosphamide in patients with chronic lymphocytic leukaemia: a randomised, open-label, phase 3 trial. Lancet. 2010;376:1164–1174.
   PubMed Web of Science ®Google Scholar
• Robak T, Dmoszynska A, Solal-Céligny P, et al. Rituximab plus fludarabine and cyclophosphamide prolongs progression-free survival compared with fludarabine and cyclophosphamide alone in previously treated chronic lymphocytic leukemia. J Clin Oncol. 2010;28:1756–1765.
   PubMed Web of Science ®Google Scholar
• Badoux XC, Keating MJ, Wang X, et al. Fludarabine, cyclophosphamide, and rituximab chemoimmunotherapy is highly effective treatment for relapsed patients with CLL. Blood. 2011;117:3016–3024.
   PubMed Web of Science ®Google Scholar
• Eichhorst B, Fink AM, Bahlo J, et al. First-line chemoimmunotherapy with bendamustine and rituximab versus fludarabine, cyclophosphamide, and rituximab in patients with advanced chronic lymphocytic leukaemia(CLL10): an international, open-label, randomised, phase 3, non-inferiority trial. Lancet Oncol. 2016;17:928–942.
   PubMed Web of Science ®Google Scholar
• Goede V, Fischer K, Busch R, et al. Obinutuzumab plus chlorambucil in patients with CLL and coexisting conditions. N Engl J Med. 2014;370:1101–1110.
   PubMed Web of Science ®Google Scholar
• Hillmen P, Robak T, Janssens A, et al. Chlorambucil plus ofatumumab versus chlorambucil alone in previously untreated patients with chronic lymphocytic leukaemia (COMPLEMENT 1): a randomised, multicentre, open-label phase 3 trial. Lancet. 2015;385:1873–1883.
   PubMed Web of Science ®Google Scholar
• Lee HJ, Gallardo M, Ma H, et al. p53-independent ibrutinib responses in an Eμ-TCL1 mouse model demonstrates efficacy in high-risk CLL. Blood Cancer J. 2016;6:e434.
   PubMed Web of Science ®Google Scholar
• Anderson MA, Deng J, Seymour JF, et al. The BCL2 selective inhibitor venetoclax induces rapid onset apoptosis of CLL cells in patients via aTP53-independent mechanism. Blood. 2016;127:3215–3224.
   PubMed Web of Science ®Google Scholar
• O'Brien S, Jones JA, Coutre S, et al. Safety and efficacy and safety of ibrutinib in patients with relapsed or refractory chronic lymphocytic leukemia or small lymphocytic leukemia with 17p deletion: results from the phase II RESONATE™-17 trial. Blood. 2014;124:327.
   Web of Science ®Google Scholar
• Byrd JC, Furman RR, Coutre SE, et al. Three-year follow-up of treatment-naïve and previously treated patients with CLL and SLL receiving single-agent ibrutinib. Blood. 2015;125:2497–2506.
   PubMed Web of Science ®Google Scholar
• Farooqui MZ, Valdez J, Martyr S, et al. Ibrutinib for previously untreated and relapsed or refractory chronic lymphocytic leukaemia with TP53 aberrations: a phase 2, single-arm trial. Lancet Oncol. 2015;16:169–176.
   PubMed Web of Science ®Google Scholar
• Burger JA, Keating MJ, Wierda WG, et al. Safety and activity of ibrutinib plus rituximab for patients with high-risk chronic lymphocytic leukaemia: a single-arm, phase 2 study. Lancet Oncol. 2014;15:1090–1099.
   PubMed Web of Science ®Google Scholar
• Furman RR, Sharman JP, Coutre SE, et al. Idelalisib and rituximab in relapsed chronic lymphocytic leukemia. N Engl J Med. 2014;370:997–1007.
   PubMed Web of Science ®Google Scholar
• Stilgenbauer S, Eichhorst B, Schetelig J, et al. Venetoclax in relapsed or refractory chronic lymphocytic leukaemia with 17p deletion: a multicentre, open-label, phase 2 study. Lancet Oncol. 2016;17:768–778.
   PubMed Web of Science ®Google Scholar
• Hallek M, Cheson BD, Catovsky D, et al. Guidelines for the diagnosis and treatment of chronic lymphocytic leukemia: a report from the International Workshop on Chronic Lymphocytic Leukemia updating the National Cancer Institute-Working Group 1996 guidelines. Blood. 2008;111:5446–5456.
   PubMed Web of Science ®Google Scholar
• Oscier D, Dearden C, Eren E, et al. Guidelines on the diagnosis, investigation and management of chronic lymphocytic leukaemia. Br J Haematol. 2012;159:541–564.
   PubMed Web of Science ®Google Scholar
• Eichhorst B, Robak T, Montserrat E, et al. Chronic lymphocytic leukaemia: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2015;26:v78–v84.
   PubMed Web of Science ®Google Scholar
• Zelenetz AD, Gordon LI, Wierda WG, et al. Chronic lymphocytic leukemia/small lymphocytic lymphoma, version 1.2015. J Natl Compr Canc Netw. 2015;13:326–362.
   PubMed Web of Science ®Google Scholar
• Rossi D, Khiabanian H, Spina V, et al. Clinical impact of small TP53 mutated subclones in chronic lymphocytic leukemia. Blood. 2014;123:2139–2147.
   PubMed Web of Science ®Google Scholar
• Malcikova J, Stano-Kozubik K, Tichy B, et al. Detailed analysis of therapy-driven clonal evolution of TP53 mutations in chronic lymphocytic leukemia. Leukemia. 2015;29:877–885.
   PubMed Web of Science ®Google Scholar
• Nadeu F, Delgado J, Royo C, et al. Clinical impact of clonal and subclonal TP53, SF3B1, BIRC3, NOTCH1, and ATM mutations inchronic lymphocytic leukemia. Blood. 2016;127:2122–2130.
   PubMed Web of Science ®Google Scholar
• Pospisilova S, Sutton LA, Malcikova J, et al. Innovation in the prognostication of chronic lymphocytic leukemia: how far beyond TP53 gene analysis can we go? Haematologica. 2016;101:263–265.
   PubMed Web of Science ®Google Scholar
• Fabbri G, Rasi S, Rossi D, et al. Analysis of the chronic lymphocytic leukemia coding genome: role of NOTCH1 mutational activation. J Exp Med. 2011;208:1389–1401.
   PubMed Web of Science ®Google Scholar
• Pozzo F, Bittolo T, Arruga F, et al. NOTCH1 mutations associate with low CD20 level in chronic lymphocytic leukemia: evidence for a NOTCH1 mutation-driven epigenetic dysregulation. Leukemia. 2016;30:182–189.
   PubMed Web of Science ®Google Scholar
• Vardi A, Agathangelidis A, Sutton LA, et al. Immunogenetic studies of chronic lymphocytic leukemia: revelations and speculations about ontogeny and clinical evolution. Cancer Res. 2014;74:4211–4216.
   PubMed Web of Science ®Google Scholar
• Lin KI, Tam CS, Keating MJ, et al. Relevance of the immunoglobulin VH somatic mutation status in patients with chronic lymphocytic leukemia treated with fludarabine, cyclophosphamide, and rituximab (FCR) or related chemoimmunotherapy regimens. Blood. 2009;113:3168–3171.
   PubMed Web of Science ®Google Scholar
• Rossi D, Terzi-di-Bergamo L, De Paoli L, et al. Molecular prediction of durable remission after first-line fludarabine-cyclophosphamide-rituximab inchronic lymphocytic leukemia. Blood. 2015;126:1921–1924.
   PubMed Web of Science ®Google Scholar
• Fischer K, Bahlo J, Fink AM, et al. Long-term remissions after FCR chemoimmunotherapy in previously untreated patients with CLL: updated results of the CLL8 trial. Blood. 2016;127:208–215.
   PubMed Web of Science ®Google Scholar
• Thompson PA, Tam CS, O'Brien SM, et al. Fludarabine, cyclophosphamide, and rituximab treatment achieves long-term disease-free survival in IGHV-mutated chronic lymphocytic leukemia. Blood. 2016;127:303–309.
   PubMed Web of Science ®Google Scholar
• Burger JA, Tedeschi A, Barr PM, et al. Ibrutinib as initial therapy for patients with chronic lymphocytic leukemia. N Engl J Med. 2015;373:2425–2437.
   PubMed Web of Science ®Google Scholar
• Ghia P, Stamatopoulos K, Belessi C, et al. ERIC recommendations on IGHV gene mutational status analysis in chronic lymphocytic leukemia. Leukemia. 2007;21:1–3.
   PubMed Web of Science ®Google Scholar
• Tam CS, O'Brien S, Plunkett W, et al. Long-term results of first salvage treatment in CLL patients treated initially with FCR (fludarabine, cyclophosphamide, rituximab). Blood. 2014;124:3059–3064.
   PubMed Web of Science ®Google Scholar
• Cramer P, Isfort S, Bahlo J, et al. Outcome of advanced chronic lymphocytic leukemia following different first-line and relapse therapies: a meta-analysis of five prospective trials by the German CLL Study Group (GCLLSG). Haematologica. 2015;100:1451–1459.
   PubMed Web of Science ®Google Scholar
• Fornecker LM, Aurran-Schleinitz T, Michallet AS, et al. Salvage outcomes in patients with first relapse after fludarabine, cyclophosphamide, and rituximab for chronic lymphocytic leukemia: the French intergroup experience. Am J Hematol. 2015;90:511–514.
   PubMed Web of Science ®Google Scholar
• Goede V, Cramer P, Busch R, et al. Interactions between comorbidity and treatment of chronic lymphocytic leukemia: results of German Chronic Lymphocytic Leukemia Study Group trials. Haematologica. 2014;99:1095–1100.
   PubMed Web of Science ®Google Scholar
• Goede V, Bahlo J, Chataline V, et al. Evaluation of geriatric assessment in patients with chronic lymphocytic leukemia: Results of the CLL9 trial of the German CLL study group. Leuk Lymphoma. 2016;57:789–796.
   PubMed Web of Science ®Google Scholar
• Byrd JC, Brown JR, O'Brien S, et al. Ibrutinib versus ofatumumab in previously treated chronic lymphoid leukemia. N Engl J Med. 2014;371:213–223.
   PubMed Web of Science ®Google Scholar
• Parikh SA, Shanafelt TD. Prognostic factors and risk stratification in chronic lymphocytic leukemia. Semin Oncol. 2016;43:233–240.
   PubMed Web of Science ®Google Scholar
• Parikh SA, Strati P, Tsang M, et al. Should IGHV status and FISH testing be performed in all CLL patients at diagnosis? A systematic review and meta-analysis. Blood. 2016;127:1752–1760.
   PubMed Web of Science ®Google Scholar
• Bulian P, Shanafelt TD, Fegan C, et al. CD49d is the strongest flow cytometry-based predictor of overall survival in chronic lymphocytic leukemia. J Clin Oncol. 2014;32:897–904.
   PubMed Web of Science ®Google Scholar
• Wierda WG, O'Brien S, Wang X, et al. Prognostic nomogram and index for overall survival in previously untreated patients with chronic lymphocytic leukemia. Blood. 2007;109:4679–4685.
   PubMed Web of Science ®Google Scholar
• Gentile M, Mauro FR, Rossi D, et al. Italian external and multicentric validation of the MD Anderson Cancer Center nomogram and prognostic index for chronic lymphocytic leukaemia patients: analysis of 1502 cases. Br J Haematol. 2014;167:224–232.
   PubMed Web of Science ®Google Scholar
• Pflug N, Bahlo J, Shanafelt TD, et al. Development of a comprehensive prognostic index for patients with chronic lymphocytic leukemia. Blood. 2014;124:49–62.
   PubMed Web of Science ®Google Scholar
• Molica S, Giannarelli D, Mirabelli R, et al. Unavailability of thymidine kinase does not preclude the use of German comprehensive prognostic index: results of an external validation analysis in early chronic lymphocytic leukemia and comparison with MD Anderson Cancer Center model. Eur J Haematol. 2016;96:72–77.
   PubMed Web of Science ®Google Scholar
• International CLL-IPI. working group An international prognostic index for patients with chronic lymphocytic leukaemia (CLL-IPI): a meta-analysis of individual patient data. Lancet Oncol. 2016;17:779–790.
   PubMed Web of Science ®Google Scholar
• Gentile M, Shanafelt TD, Rossi D, et al. Validation of the CLL-IPI and comparison with the MDACC prognostic index: analysis of 1364 newly diagnosed patients. Blood. 2016;128:2093–2095.
   PubMed Web of Science ®Google Scholar
• da Cunha-Bang C, Christiansen I, Niemann CU. The International prognostic index for patients with chronic lymphocytic leukemia (CLL-IPI) applied in a population-based cohort. Blood. 2016;128:2181–2183.
   PubMed Web of Science ®Google Scholar
• Döhner H, Stilgenbauer S, Benner A, et al. Genomic aberrations and survival in chronic lymphocytic leukemia. N Engl J Med. 2000;343:1910–1916.
   PubMed Web of Science ®Google Scholar
• Rossi D, Rasi S, Spina V, et al. Integrated mutational and cytogenetic analysis identifies new prognostic subgroups in chronic lymphocytic leukemia. Blood. 2013;121:1403–1412.
   PubMed Web of Science ®Google Scholar
• Jeromin S, Weissmann S, Haferlach C, et al. SF3B1 mutations correlated to cytogenetics and mutations in NOTCH1, FBXW7, MYD88, XPO1 and TP53 in 1160 untreated CLL patients. Leukemia. 2014;28:108–117.
   PubMed Web of Science ®Google Scholar
• Baliakas P, Hadzidimitriou A, Sutton LA, et al. Recurrent mutations refine prognosis in chronic lymphocytic leukemia. Leukemia. 2015;29:329–336.
   PubMed Web of Science ®Google Scholar
• Jain P, Keating M, Wierda W, et al. Outcomes of patients with chronic lymphocytic leukemia after discontinuing ibrutinib. Blood. 2015;125:2062–2067.
   PubMed Web of Science ®Google Scholar
• Thompson PA, O'Brien SM, Wierda WG, et al. Complex karyotype is a stronger predictor than del(17p) for an inferior outcome in relapsed or refractory chronic lymphocytic leukemia patients treated with ibrutinib-based regimens. Cancer. 2015;121:3612–3621.
   PubMed Web of Science ®Google Scholar
• Thompson PA, O'Brien SM, Xiao L, et al. β2 -microglobulin normalization within 6 months of ibrutinib-based treatment is associated with superior progression-free survival in patients with chronic lymphocytic leukemia. Cancer. 2016;122:565–573.
   PubMed Web of Science ®Google Scholar
• Maddocks KJ, Ruppert AS, Lozanski G, et al. Etiology of ibrutinib therapy discontinuation and outcomes in patients with chronic lymphocytic leukemia. JAMA Oncol. 2015;1:80–87.
   PubMed Web of Science ®Google Scholar
• Böttcher S, Ritgen M, Fischer K, et al. Minimal residual disease quantification is an independent predictor of progression-free and overall survival in chronic lymphocytic leukemia: a multivariate analysis from the randomized GCLLSG CLL8 trial. J Clin Oncol. 2012;30:980–988.
   PubMed Web of Science ®Google Scholar
• Strati P, Keating MJ, O'Brien SM, et al. Eradication of bone marrow minimal residual disease may prompt early treatment discontinuation in CLL. Blood. 2014;123:3727–3732.
   PubMed Web of Science ®Google Scholar