Highlights in acute myeloid leukemia (AML): what is going to change?
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1 29 Highlights in acute myeloid leukemia (AML): what is going to change? C. Graux, MD, PhD SUMMARY The decision making process in AML integrates clinical features, an increasing amount of genetic information and minimal residual disease (MRD) data. Combining these data aims at answering the following questions: do I treat my patient with an intensive (= curative) or a non intensive (= non-curative) approach? do I have therapeutic targets to improve the current treatment? is there an indication for a stem cell transplantation (SCT), maintenance therapy, etc. Each new edition of ASH brings some new answers. This was again the case at the 206 annual ASH meeting. (BELG J HEMATOL 207;8():29-33) THE HEADHACHE OF PROGNOSTICATION The cytogenetic classification into «favorable», «intermediate» and «adverse» prognostic groups has been progressively refined by molecular information. As a result, some AML patients (pts) with a normal karyotype (NK), that would previously have been classified in the intermediate group, are now reallocated in more clinically relevant prognostic groups (favorable or adverse), according to the mutation status of NPM, FLT3 and CEPBA and their potential co-expression. The number of interfering molecular events that are currently detectable with newer techniques facilitate a more accurate prognostication for AML patients. However, it also makes things more complicated. For instance, AML with mutated RUNX, has recently been added to the 206 revised WHO classification of myeloid neoplasms and acute leukemia as a provisional, clinically relevant entity. However, this could be challenged by the observation of Haferlach et al. who analyzed 467 RUNX mutated AML cases. They concluded that not only the presence, but also the number of RUNX mutations, and mainly the conservation of one intact RUNX allele, is biologically and clinically relevant. Indeed, each subgroup is associated with a distinctive molecular signature and demonstrates a particular outcome, ranging from a 5 month median overall survival (OS) in case of RUNX WT loss on the other allele to 22 months in case of an isolated RUNX mutation. TYPE OF NPM INSERTION MATTERS The characteristics of the mutation itself is also important as was demonstrated for NPM. Frameshift mutations are the result of 4 base pair (bp) insertion in exon 2. Several genomic subsets of NPM insertions have been identified, with the type A variant (insertion of TCTG) being the most common. Researchers from Seattle looked into the prognostic value of the specific genotype of NPM insertion in a large cohort of 396 pediatric AML (COG) and,95 adult AML (SWOG) patients. They found that the type A variant, which is more prevalent in older pts (p=0.08), was associated with a significantly inferior outcome compared to non-type A variants (5 year event free survival [EFS] of 39% vs. 64%, p=0.0 and 5 year recurrence free survival [RFS] of 4% vs. 70%, p=0.002) regardless of age or FLT3/ITD status. 2 TP53 MUTATION AND PREDICTION OF TREATMENT OUTCOME The prognostic value of a mutation depends also on the treatment that is used. The impact of TP53 mutations on response to therapy has been analysed in the AZA- AML-00 study comparing azacitidine (AZA) with a Department of Hematology, CHU UCL Namur (Godinne). Please send all correspondence to: Carlos Graux, MD, PhD, Service Hématologie, CHU UCL Namur, Site de Godinne, Avenue docteru G. Thérasse, 5530 Yvoir, Tel : +32 (0) , carlos.graux@uclouvain.be. Conflict of interest: The author has nothing declare and indicates no potential conflict of interest.
2 CONGRESS HIGHLIGHTS 30 SPECIAL EDITION conventional care regimen (CCR) in older patients with AML. It appears that pts with TP53 mutations have a significantly better OS when they are treated with AZA than with CCR (7.2 vs. 2.4 months, p=0.026). However, this does not mean that hypomethylating agents (HMA) alone are satisfactory in this indication. It does confirm that, currently, HMA are probably the better treatment option in older, TP53 mutated AML patients. 3 Similar findings have recently been reported by Welch et al. in the NEJM for decitabine compared to chemotherapy. 4 THE LONG PARADE OF HMA COMBINATION THERAPIES DECITABINE + ATRA OR VALPROIC ACID, OR THE COMBINATION OF BOTH Lubbert at al. reported the results of a randomized trial in newly diagnosed AML patients >60 years who are unfit for induction (N=204). In this study, ATRA, valproic acid or both were added to decitabine. The authors concluded that the addition of ATRA to decitabine resulted in a higher ORR (CR/CRi/PR) of 2.9% vs. 3.5% (OR[95%CO]:.80[0.86,3.79], p=0.2.). In addition to this, a clinically relevant extension of median OS from 5. to 8.2 months was reported (HR[95%I]: 0.65[0.48,0.88], p=0.006), without additional toxicity. In contrast, the addition of VPA did not affect the ORR or the median OS. 5 HMA + VADASTUXIMAB TALIRINE Vadastuximab talirine (33A) is the new CD33-directed antibody-drug conjugate. The difference with gemtuzumab ozogamicin is that, instead of chalicheamicine, it links to 2 molecules of a pyrrolobenzodiazepine (PBD) dimer. This is a new agent that, once internalized, crosslinks DNA, leading to the death of CD33 positive leukemic cells. Preclinical studies demonstrated that HMA priming upregulates CD33 expression. Fathi et al. updated the phase study, already presented at the EHA, that was conducted in older patients who were ineligible (N=40) or refused to have intensive therapy (N=3). In this study, 33A was given as an IV infusion at the last day of HMA. In this update, the high ORR (CR/CRi) of 73% was confirmed. This was also the case in poor risk subgroups with obtention of MRD negativity in 47% of patients. Thrombocytopenia was the main toxicity. 6 AZA + PRACINOSTAT The combination of pracinostat, a potent oral class I, II, IV HDAC inhibitor, to AZA is expected to induce a re-expression of silenced genes in a synergistic fashion. Manero et al. reported the long-term survival and response analyses of the phase 2 study evaluating the combination in AML patients older than 65 years who are not eligible for induction therapy (N=50). A CR, CRi and morphologic leukemia free state was achieved in 42%, 4% and 6% of patients, respectively. The median duration of CR was 3.2 months (95%CI: ). With a median follow-up of 2 months, the median OS was 9. months (95%CI: 0.0-not reached). 7 AZA + PEVONEDISTAT Pevonedistat is a first-in-class NEDD8-activating enzyme inhibitor, disrupting proteasome-mediated protein degradation. Results of a phase I combination study with AZA conducted in older AML patients unlikely to benefit from standard induction therapy (N=6) was reported by Swords et al. A CR/CRi was obtained in 44% of response-evaluable patients (N=52). The median OS was 7.0 months for the MTD cohort. There was limited additional toxicity beyond what can be expected for AZA alone. 8 AZA + NIVOLUMAB The rational for the combination of AZA and nivolumab comes from the observation that AZA upregulates PD- and PD-L in AML, a process that is associated with resistance to AZA. 9 Daver et al. presented a phase IB/II study of Nivolumab in combination with AZA in 5 R/R AML patients. Nivolumab was given at a dose of 3mg/kg on day and 4 of AZA 75mg/m 2 days -7 cycles. Responses were evaluated at the end of 3 courses of therapy so that only 35/5 patients were evaluable. Durable CR/CRi or HI were achieved in 8% and 5% respectively. The median OS for the 35 evaluable patients was 9.3 months (range,.8-4.3). Although the study selected patients that were able to receive at least 3 cycles, this compares favorably to historical survival with AZA-based salvage protocols in similar patients. 0 HMA + QUIZARTINIB FLT3 mutations are found in nearly one third of newly diagnosed AML patients and are associated to a dismal prognosis. Quizartinib is a potent and selective FLT3- ITD inhibitor that demonstrated in vitro synergy with AZA or low dose ARA-C (LDAC). It is the rational for the combination study conducted by the MDACC in R/R (phase I) and untreated (phase II) FLT3 mutated AML/MDS/CMML patients. In total, 52 patients have been enrolled: 38 to AZA arm and 4 to LDAC arm.
3 3 Quizartinib 60 mg daily was identified as the recommended phase II dose. An ORR of 67% (CR=8, CRp=7, CRi=8, PR=2) was observed (23% in the LDAC arm and 77% in the AZA arm) all in patients with a FLT3-ITD mutation and without a D835 mutation. The median OS was 4.8 months for the total study group, 7.5 months for the LDAC arm and was not reached for the AZA arm. Clinically significant QTcF prolongations were infrequent. IMMUNOTHERAPY FOR AML? CD23, THE MYELOID TARGET? As a rule, immunotherapy works best when the disease load is reduced and is therefore particularly indicated to eliminate MRD. Leukemic stem cell (LSC) participates to MRD persistence and reappearance. The ideal target for immunotherapy has to be expressed on the surface of LSC. The majority of LSC lack CD33 expression and are not eliminated with CD33-targeting agents. By exploring the surfaceasome of AML blasts and LSCs, CD23 (IL-3 receptor α chain) has emerged as a very promising target for immunotherapeutic strategies in AML. Indeed, an aberrant expression is frequently observed in a subset of leukemic disorders, including AML, particularly in leukemic stem cells. Moreover, studies using flow cytometric analyses have shown that increased CD23 expression is associated with a poor prognosis. 2 SL-40 is a recombinant fusion protein consisting of human IL-3 (that dictates the specificity for CD23 expressing cells) and the catalytic unit of diphtheria toxin that, upon internalization, inhibits the translational machinery to initiate cell death. The ability of SL- 40 to deliver its toxin selectively to cancer cells and LSC could limit side effects by preventing exposure to other cells. Pemmaraju et al. reported the results of an ongoing phase 2 trial of SL-40 in patients with blastic plasmacytoïd dendritic cell neoplasm (BPDCN). This is a rare myeloid entity caracterized by a particular CD4, CD56, CD23, TCL- expression profile and frequent skin involvement (sometimes as primary site). Currently, there is no standard of care for these patients and an ALL type treatment is usually proposed. The OS is poor, arround 8-4 months. CD23 is overexpressed in nearly 00% of patients with BPDCN. Using SL-40 at the dose of 2 µg/kg, they obtained a 8% (3/6) CR/CRc when used in ste line and 3% (4/3) in R/R setting. 7/32 patients underwent an allo or auto stem cell transplantation. 3 Lane et al. reported the preliminary results of a study evaluating SL-40 in patients with AML in CR or CR2, with high risk of relapse including persistent MRD. They concluded that targeting MRD with SL-40 has the potential to reduce this chemoresistant cell population and could offer improved long-term outcomes for AML patients in remission with high risk of relapse. 4 CD23 is also the target in numerous other immunotherapeutic strategies: IMGN632, another CD23-directed antibody-drug conjugate, is currently under preclinical evaluation. It contains two engineered cysteines for the conjugation with indolinobenzodiazepine dimers for DNA alkylation. 5 A bispecific humanized IgG4 antibody (JNJ ) with silenced Fc function that can bind both CD23 on tumor cells and CD3 on T cells is able to recruit T cells to CD23-expressing tumor cells and induce their killing in vitro. 6 Allogeneic TCRα/β deficient CAR T-cells targeting CD23 prolong overall survival of AML and BPDCN patient-derived xenografts in pre-clinical studies. 7,8 NEW AGENTS IDH/2 INHIBITORS Recurrent somatic mutations in the metabolic enzymes isocitrate dehydrogenase and 2 (IDH/2) confer gainof-function activity in cancer cells, resulting in accumulation of the oncometabolite, D-2-hydroxyglutarate (2-HG). High levels of 2-HG result in epigenetic changes and impaired cellular differentiation. Much has been discussed about IDH/2 inhibitors during ASH 206. Since IDH/2 mutations are typically present in the founding clone of approximately 5% of AML cases, their inhibition represents an attractive therapeutic strategy. AG-20, a first-in-class, oral, potent, reversible, selective inhibitor of the IDH mutant enzyme is currently under evaluation in multiple single agent and combination clinical trials. DiNardo et al. presented the first data with this agent, demonstrating that treatment with single agent AG-20 can result in midh clearance as determined by NGS. 9 Studies with the IDH2 Inhibitor, enasidenib (AG22) and the pan IDH/IDH2 inhibitor AG88 are also ongoing. VENETOCLAX, THE BCL2 INHIBITOR The selective BCL-2 inhibitor venetoclax demonstrates single-agent activity in patients with relapsed and refractory AML. 20 It has been further evaluated in combination
4 CONGRESS HIGHLIGHTS 32 SPECIAL EDITION with HMA and ARA-C. Researchers from Australia reported a substantial added benefit of venetoclax combined to ARA-C in treatment-naïve AML patients aged 65 yr (CR+CRi+PR was 75% and 2 months OS estimate was 74,7% (95%CI: ). 2 Venetoclax is often associated with resistance due to its poor inhibition of MCL-. In fact, the RAF/MEK/ERK (MAPK) pathway is commonly activated in AML, which stabilizes anti-apoptotic MCL-. Han et al, suggested that results with venetoclax might be improved by targeting the MAPK signaling pathway with the MEK/2 inhibitor Cobimetinib. Combined efficacy of these agents is under clinical investigation in a phase I trial in elderly R/R AML. 22 OPTIMALISATION OF INDUCTION THERAPY: LESS IS MORE? HIGH DOSE ARA-C +/- VORINOSTAT Garcia-Manero et al. previously reported a historically high response rate of idarubicin (ida) and high-dose ara-c (IA) in combination with the HDAC inhibitor vorinostat (IA+V) compared to IA or SWOG 203 tested whether an IA induction (idarubicin 2 mg/m 2 x 3 days with ara-c.5 gr/m 2 x 4 days) with or without vorinostat could result in improved outcomes for younger AML patients compared to 7+3 (dauno 90 mg/m 2 x 3 days with ara-c 00 mg/m2 x 7 days). Of importance, patients receiving high-dose ara-c during the induction (IA and IA+V) were consolidated with a relative light consolidation program (idarubicin 8 mg/m 2 x 2 days with ara-c 0.75 gr/m 2 x 3 days) for up to 4 cycles (depending on transplant avaibility). The authors concluded that treatment with IA is not more effective than 7+3. Outcomes with IA or IA plus vorinostat are similar. In patients with favorable cytogenetics, outcomes were inferior with IA or IA+V when compared to 7+3, perhaps related to use of lower doses of ara-c during consolidation in the IA and IA+V arms. 24 These findings demonstrate once again that each time there is an attempt to improve remission rates by increasing the dose, the benefit in terms of OS is offset by increased toxicity. 7+3 COMBINED WITH SELINEXOR By inhibiting the primary export protein, XPO, selinexor maintains tumor suppressor proteins to the nucleus leading to their activation and an anti-leukemic effect as a single agent. Moreover, it inhibits DNA damage repair, rationalizing its use in combination with DNA damaging agents. Two phase studies of selinexor combined to 7+3 induction therapy have been presented in first line poor risk AML and R/R AML. Both indicate that the combination can be safely administered. The encouraging activity could represent this treatment as an interesting bridge to transplantation. 25, COMBINED WITH VADASTUXIMAB TALIRINE Erba et al. reported data on the combination of vadastuximab talirine (discussed earlier) with 7+3 induction therapy in pts with newly diagnosed AML. They obtained a 78% remission rate (CR+CRi) within the st induction cycle, 74% of which being MRD negative. No cases of veno-occlusive disease (VOD) or significant hepatotoxicity were observed COMBINED WITH CRENOLANIB Crenolanib, a type I oral FLT3 TKI, which inhibits both FLT3-ITD and FLT3-TKD mutations (D835, N84, etc) has also been safely combined with 3+7 induction chemotherapy in pts with newly-diagnosed, FLT3 mutated AML. A high CR rate of 88% with full count recovery was observed after one cycle of induction with an overall CR/CRi rate of 96%. High-dose ara-c consolidation and allo SCT could be administered on schedule. These results confirm the high added gain of targetting FLT3 in front-line therapy. 28 THE WINNER? Gilteritinib (ASP225) is a novel, highly potent and selective oral FLT3/AXL inhibitor with preclinical activity against FLT3-ITD activating and FLT3-D835 resistance mutations. The first-in-human phase /2 study (CHRYSALIS) of once-daily oral gilteritinib given to patients with R/R AML irrespective of FLT3 mutation status was reported by Perl at al. The results in this very poor risk cohort were impressive, with a 4% CRc (CR, CRp, CRi) and a 52% ORR in FLT3 mutation-positive patients (ITD ±D835) when given at a dose 80mg/d. Some responses were also observed in FLT3 wild-type patients (ORR=2%, CRc=9%). Of interest, the median time to best response is 7.2 months, the median duration of response is 20 weeks and the median OS was 3 weeks. 29 CONCLUSIONS The effective translation of research-based innovations into the treatment of AML patients will require collaborative efforts of academics and companies to organise big trials that can facilitate personalized treatment
5 33 CONGRESS HIGHLIGHTS decisions, based on genomic information. This will imply the characterisation of all known mutations in AML at the time of diagnosis and their monitoring during therapy. In this respect, next generation sequencing opens new perspectives for clono specific evaluation of MRD. 30 REFERENCES. Stengel, et al. The Number of RUNX Mutations and the Presence of One Intact RUNX Allele Influence Cytogenetic Abnormalities, Additional Molecular Mutations and Prognosis in RUNX Mutated AML. Abstract 284, ASH D. Selim, et al. Genomic Subtypes of Nucleophosmin (NPM) Mutations Are Associated with Clinical Outcome in AML a COG and SWOG Intergroup Collaboration. Abstract 285, ASH L. Tang, et al. Impact of Gene Mutations on Overall Survival in Older Patients with Acute Myeloid Leukemia (AML) Treated with Azacitidine (AZA) or Conventional Care Regimens (CCR). Abstract 2859, ASH Welch J, et al. TP53 and decitabine in acute myeloid leukemia and myelodysplastic syndromes. N Engl J Med 206 ;375(2): M. Lübbert, et al. Results of the Randomized Phase II Study Decider (AMLSG 4-09) Comparing Decitabine (DAC) with or without Valproic Acid (VPA) and with or without All-Trans Retinoic Acid (ATRA) Add-on in Newly Diagnosed Elderly Non-Fit AML Patients. Abstract 589, ASH AT. Fathi, et al. Vadastuximab Talirine Plus Hypomethylating Agents: A Well-Tolerated Regimen with High Remission Rate in Frontline Older Patients with Acute Myeloid Leukemia (AML). Abstract 59, ASH G. Garcia Manero, et al. A Phase 2 Study of Pracinostat and Azacitidine in Elderly Patients with Acute Myeloid Leukemia (AML) Not Eligible for Induction Chemotherapy: Response and Long-Term Survival Benefit. Abstract 00, ASH RT. Swords, et al. Results of a Clinical Study of Pevonedistat (Pev), a First-in-Class NEDD8-Activating Enzyme (NAE) Inhibitor, Combined with Azacitidine (Aza) in Older Patients (Pts) with Acute Myeloid Leukemia (AML). Abstract 98, ASH Yang H, et al. Expression of PD-L, PD-L2, PD- and CTLA4 in myelodysplastic syndromes is enhanced by treatment with hypomethylating agents. Leukemia 204;28(6): N. Daver, et al. Phase IB/II Study of Nivolumab in Combination with Azacytidine (AZA) in Patients (pts) with Relapsed Acute Myeloid Leukemia (AML) Abstract 763, ASH W. Abdelall, et al. The Combination of Quizartinib with Azacitidine or Low Dose Cytarabine Is Highly Active in Patients (Pts) with FLT3-ITD Mutated Myeloid Leukemias: Interim Report of a Phase I/II Trial. Abstract 642, ASH N. Arai, et al. Immunohistochemical Expression of CD23 Is Associated with an Inferior Clinical Outcome in Acute Myeloid Leukemia. Abstract 2887, ASH N. Pemmaraju, et al. MD3 Results from Phase 2 Trial Ongoing Expansion Stage of SL-40 in Patients with Blastic Plasmacytoid Dendritic Cell Neoplasm (BPDCN). Abstract 342, ASH AA. Lane, et al. Results from Ongoing Phase 2 Trial of SL-40 As Consolidation Therapy in Patients with Acute Myeloid Leukemia (AML) in Remission with High Relapse Risk Including Minimal Residual Disease (MRD). Abstract 25, ASH Y. Kovtun, et al. A CD23-Targeting Antibody-Drug Conjugate (ADC), IMGN632, Designed to Eradicate Acute Myeloid Leukemia (AML) Cells While Sparing Normal Bone Marrow Cells. Abstract 768, ASH F. Gaudet, et al. Development of a CD23xCD3 Bispecific Antibody (JNJ ) for the Treatment of Acute Myeloid Leukemia (AML). Abstract 2824, ASH R. Mani, et al. SL-40 Mediates Potent Cytotoxicity Against CD23+ AML and MDS with Excess Blasts and Demonstrates Therapeutic Benefit in PDX Model. Abstract 580, ASH T. Cai, et al. Pre-Clinical Studies of Anti-CD23 CAR-T Cells for the Treatment of Blastic Plasmacytoid Dendritic Cell Neoplasm (BPDCN). Abstract 4039, ASH CD. DiNardo, et al. Determination of IDH Mutational Burden and Clearance Via Next-Generation Sequencing in Patients with IDH Mutation-Positive Hematologic Malignancies Receiving AG-20, a First-in-Class Inhibitor of Mutant IDH. Abstract 070, ASH Konopleva M, et al. Efficacy and Biological Correlates of Response in a Phase II Study of Venetoclax Monotherapy in Patients with Acute Myelogenous Leukemia. Cancer discovery 206;6(0): A. Wei, et al. Safety and Efficacy of Venetoclax Plus Low-Dose Cytarabine in Treatment-Naive Patients Aged 65 Years with Acute Myeloid Leukemia. Abstract 02, ASH L. Han, et al. Targeting MAPK Signaling Pathway with Cobimetinib (GDC-0973) Enhances Anti-Leukemia Efficacy of Venetoclax (ABT-99/GDC-099) in Acute Myeloid Leukemia Models. Abstract 97, ASH Garcia-Manero G, et al. Phase II trial of vorinostat with idarubicin and cytarabine for patients with newly diagnosed acute myelogenous leukemia or myelodysplastic syndrome. J Clin Oncol 202;30(8): G. Garcia-Manero, et al. SWOG S203: A Randomized Phase III Study of Standard Cytarabine Plus Daunorubicin (7+3) Therapy Versus Idarubicin with High Dose Cytarabine (IA) with or without Vorinostat (IA+V) in Younger Patients with Previously Untreated Acute Myeloid Leukemia. Abstract 90, ASH KL. Sweet, et al. A Phase I Study of Selinexor in Combination with Daunorubicin and Cytarabine in Patients with Newly Diagnosed Poor-Risk Acute Myeloid Leukemia. Abstract 4040, ASH W. Fiedler, et al. Phase II Results of Ara-C and Idarubicin in Combination with the Selective Inhibitor of Nuclear Export (SINE) Compound Selinexor (KPT-330) in Patients with Relapsed or Refractory AML. Abstract 34, ASH HP. Erba, et al. A Phase b Study of Vadastuximab Talirine in Combination with 7+3 Induction Therapy for Patients with Newly Diagnosed Acute Myeloid Leukemia (AML). Abstract 2, ASH ES. Wang, et al. Crenolanib, a Type I FLT3 TKI, Can be Safely Combined with Cytarabine and Anthracycline Induction Chemotherapy and Results in High Response Rates in Patients with Newly Diagnosed FLT3 Mutant Acute Myeloid Leukemia (AML). Abstract 07, ASH AE. Perl, et al. Final Results of the Chrysalis Trial: A First-in-Human Phase /2 Dose-Escalation, Dose-Expansion Study ofgilteritinib (ASP225) in Patients with Relapsed/Refractory Acute Myeloid Leukemia (R/R AML). Abstract 069, ASH P. Hirsch, et al. Clono-Specific Evaluation of Minimal Residual Disease in Acute Myeloid Leukemia. Abstract 208, ASH 206.
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