Treatment free remission in CML: from the concept to practice. François-Xavier Mahon. Cancer Center Bordeaux Université Bordeaux, France
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1 Treatment free remission in CML: from the concept to practice François-Xavier Mahon Cancer Center Bordeaux Université Bordeaux, France
2 CML is a model Philadelphia chromosome t(9;22) (q34;q11) BCR-ABL gene BCR-ABL drives CML cells Imatinib Tyrosine kinase inhibitors First results of treatment cessation 2020 Curing CML?
3 Introduction Stopping treatment is an emerging goal of CML management Several studies have demonstrated the feasibility of stopping treatment A sustained DMR on long-term TKI therapy seems to be necessary prior to attempting TFR Consistent results over time from ongoing studies validated the concept of TFR Sauβele S, et al. Leukemia Hughes TP and Ross DM. Blood
4 Rea D et al. Cancer 2018 (14): KR
5 Treatment free remission Lessons from the past: how can we propose stopping treatment? Why stop TKI treatment in CML patients? Results of clinical trials Safety Predictive Factors Possible criteria for TKI discontinuation Future steps
6 Treatment free remission Lessons from the past: how can we propose stopping treatment? Why stop TKI treatment in CML patients? Results of clinical trials Safety Predictive Factors Possible criteria for TKI discontinuation Future steps
7 Lessons from the past : how can we propose stopping treatment? Mahon et al. J Clin Oncol 2001; 20:
8 Treatment-free persistent minimum residual disease without relapse with interferon KR patients stopped IFN with a median follow up after discontinuation of 8 years (5-18). In 9 of them the persistence of leukemic cells after discontinuation of IFN without CML relapse was demonstrated by RQ-PCR. 100% (IRIS baseline) 100 % BCR-ABL/ABL 10% % 0.1% (IRIS MMR) % % 0.001% MR 4 MR 4.5 MR 5 Mahon FX, et al. Blood (ASH Meeting) 2010;116:2299. Cross N et al Leukemia (2012) 26,
9
10 Treatment free remission Lessons from the past : how can we propose stopping treatment? Why stop TKI treatment in CML patients? Results of clinical trials Safety Predictive Factors Possible criteria for TKI discontinuation Future steps
11 Why stop TKI treatment in CML patients? Off-target effects of TKI Severe adverse drug reactions i.e., pulmonary arterial hypertension or pleural effusion TKI-Associated Cardiovascular Toxicity Side effects that impair quality of life
12 Why stop TKI treatment in CML patients? Family planning and pregnancy The TKI treatment in children may alter patient growth Patients requests are also important Is TKI a lifelong treatment? Ethical issue
13 Two important issues must be considered : Quality of life and pharmacoeconomics J Clin Oncol 2016;34:2851-7
14 Treatment free remission Lessons from the past : how can we propose stopping treatment? Why stop TKI treatment in CML patients? Results of clinical trials Safety Predictive Factors Possible criteria for TKI discontinuation Future steps
15 Treatment free remission trials STIM1 ASTIM STIK2 DADI ENEStop and ENESTfreedom EUROSKI KID study META- ANALYSIS JALSG-STIM213
16 STIM1: First Study to Investigate TKI cessation Study Design Start Imatinib DMR Sustained DMR for 2 y STOP IMATINIB N = 100 TFR 5 RQ-PCR assessments during these 2 y RQ-PCR every month in the first year and every 2 mo thereafter Molecular relapse or recurrence : Confirmed BCR-ABL1 transcript positivity in 2 consecutive RQ-PCR assessments with a 1-log increase in the second assessment relative to the first, or loss of MMR in 1 assessment Mahon FX, et al. Lancet Oncol. 2010;11: Etienne G, et al. JCO. 2017;35: Sixth data point checked in centralized laboratory Sustained DMR (no detectable BCR-ABL1 for 2 consecutive years with a sensitivity of > 4.5 logs
17 STIM 1: Molecular Recurrence Free Survival (N = 100) The median molecular follow-up after treatment discontinuation is 77 months (range, 9 to 95 months) Etienne G, et al. JCO. 2017;35:
18 ASTIM: Treatment-free remission using loss of MMR to define molecular relapse Rousselot P, et al. J Clin Oncol. 2014;32(5):
19 META- ANALYSIS 509 patients included only patients on imatinib. 15 cohort studies Nine studies were at low-risk of bias Overall weighted mean molecular relapse rate of CML was 51% Weighted mean molecular relapse rate at 6-month follow-up was 41% Eighty percent of molecular relapses occurred within the first 6 months All 509 patients were alive at 2-year follow-up one patient had progressed to a blastic crisis
20 Patients With MR4.5, % Second-Generation TKIs Are Associated With Higher Rates of MR Nilotinib 300 mg BID (n = 282) Imatinib 400 mg QD (n = 283) By 4 Years 54% P <.0001 By 5 Years 56% P <.0001 By 6 Years 70 40% P < % P <.0001 By 1 Year 25% P <.0001 By 2 Years 32% P <.0001 By 3 Years 30 31% 33% % % % % 48 Data cutoff: May 22, Time Since Randomization, months Rates of MR4.5 by 6 years were consistently higher with nilotinib vs imatinib Leukemia May;30(5):
21 STOP 2G-TKI : Treatment-free remission STOP-2G (N=60) The median molecular follow-up after treatment discontinuation: 47 months, range; Rea et al; Blood 2017; 129:
22 Enroll ENESTfreedom: TFR Following Frontline Nilotinib (144 weeks, about 3-year follow-up) ENESTfreedom is a single-arm, phase 2 study Adults with CML-CP b2a2 and/or b3a2 transcripts 2 years of frontline nilotinib MR 4.5 at screening (central laboratory) RQ-PCR every 12 weeks Nilotinib consolidation phase (52 weeks) No sustained DMR a Sustained DMR a First 48 weeks: RQ-PCR every 4 weeks Second 48 weeksr: RQ-PCR every 6 weeks Thereafter: RQ-PCR every 12 weeks TFR phase b,c Nilotinib continuation phase No sustained DMR a Sustained DMR a TFR-2 phase b Nilotinib treatment reinitiation upon loss of MMR Prolonged continuation phase IS, International Scale; MMR, major molecular response (BCR-ABL1 IS 0.1%); MR 4.5, BCR-ABL1 IS %; RQ-PCR, real-time quantitative polymerase chain reaction (standardized to the IS). a Sustained DMR defined as the following (in the last 4 quarterly PCR assessments): MR 4.5 in the last assessment, no assessment worse than MR 4 (BCR-ABL1 IS 0.01%), and 2 assessments between MR 4 and MR 4.5. b Patients will be followed up for up to 264 weeks after the last patient entered the TFR phase. c This analysis was based on a cutoff date of October 11, 2017, at which time all patients who entered the TFR phase had completed 144 weeks of TFR, entered the nilotinib reinitiation phase, or discontinued from the study. Saglio et al. EHA 2018; (Abstract PF368)
23 TFS, % ENESTfreedom: TFR Following Frontline Nilotinib (144 weeks, about 3-year follow-up) TFR rate at 144 weeks was 46.8% (89/190) Of 93 patients in TFR at 96 weeks, 4 were no longer in the TFR phase at 144 weeks - Only 3 had confirmed loss of MR I Patients Events Censored Censored observations week TFR rate (primary endpoint): 51.6% 96-week TFR rate: 48.9% 144-week TFR rate: 46.8%(89/190) 144-week TFS rate: 51.6% (98/190) Time Since TFR Start, weeks No. at Risk:Events 190: 0 120:70 99:89 95:91 93:93 92:94 77:97 10:97 0:97 a TFS was estimated using the Kaplan-Meier method and was defined as the time from the date of start of TFR to the date of earliest occurrence of an event (loss of MMR, progression to accelerated phase [AP] or blast crisis [BC], death due to any cause up to the end of the TFR phase, or reinitiation of nilotinib due to any cause). b Defined as no loss of MMR and no reinitiation of nilotinib in the first 48 weeks of TFR.
24 Enroll ENESTop: TFR Following Second line Nilotinib (144 weeks, about 3-year follow-up) Adults with CML-CP RQ-PCR every 12 weeks First year: RQ-PCR every 4 weeks Second year: RQ-PCR every 6 weeks Thereafter: RQ-PCR every 12 weeks 3 years of TKI therapy (first imatinib for > 4 weeks, then nilotinib for 2 years) No documented MR 4.5 at time of switch to nilotinib Achieved MR 4.5 on nilotinib Nilotinib consolidation phase (52 weeks) Confirmed a loss of MR 4.5 No confirmed a loss of MR 4.5 Criteria for reinitiating nilotinib: Loss of MMR or Confirmed c loss of MR 4 TFR phase b Nilotinib continuation phase d (52 weeks) No confirmed a loss of MR 4.5 TFR-2 phase b Nilotinib treatment reinitiation phase IS, International Scale; MMR, major molecular response (BCR-ABL1 IS 0.1%); MR 4, BCR-ABL1 IS 0.01%; MR 4.5, BCR-ABL1 IS %; RQ-PCR, real-time quantitative polymerase chain reaction; TKI, tyrosine kinase inhibitor. a Confirmed loss of MR 4.5 was defined as BCR-ABL1 IS > %, confirmed in a second assessment within 4 weeks. b Patients will be followed up for up to 264 weeks after the last patient entered the TFR phase. c Confirmed loss of MR 4 was defined as BCR-ABL1 IS > 0.01%, confirmed in a second assessment within 4 weeks. d Patients with confirmed loss of MR 4.5 during the continuation phase continued nilotinib treatment in the prolonged continuation phase until 264 weeks after the last patient entered the TFR phase or until discontinuation due to unacceptable toxicity, disease progression, investigator discretion, or withdrawal of consent. Mahon et al. J Clin Oncol 36, 2018 (suppl; abstr 7003)
25 27 ENESTop: TFR Following Second line Nilotinib (144 weeks, about 3-year follow-up) 100 Treatment-Free Survival, % a week TFR rate b (primary endpoint): 57.9% (73/126) 96-week TFR rate: 53.2% (67/126) 144-week TFR rate: 48.4% (61/126) 144-week TFS rate: 52.0% (95% CI, 42.9%-60.4%) Patients Events Censored 65 I I I Censored observations TFR rate at 144 weeks was 48.4% (61/126) Of 67 patients in TFR at 96 weeks, 6 were no longer in the TFR phase at 144 weeks - Only 3 had confirmed loss of MR 4 at 108, 120, and 144 weeks, respectively At risk:events Time Since TFR Start, weeks 126:0 107:1976:49 74:51 73:52 72:53 71:53 69:54 67:55 66:56 65:57 63:59 50:60 31:61 14:61 1:61 0:61 AP/BC, accelerated phase/blast crisis; TFS, treatment-free survival. a Defined as the Kaplan-Meier estimate of the time from the start of TFR until the earliest of any of the following: loss of MMR, confirmed loss of MR 4, treatment reinitiation due to any cause, progression to AP/BC, or death due to any cause. b Defined as the proportion of patients without loss of MMR, confirmed loss of MR 4, or treatment reinitiation. c At the 48-week data cutoff, all patients had completed 48 weeks of TFR, restarted nilotinib, or discontinued the study. Mahon et al. J Clin Oncol 36, 2018 (suppl; abstr 7003)
26 EURO-SKI design Patients included between May 2012 and December 2014 TKI treatment 3 years Molecular recurence defined as BCR-ABL >0.1% (loss of MMR) at one time point. MR 4 1 year Screening phase (confirmation of MR 4 in central lab) q4w RQ-PCR q6w RQ-PCR every 3 rd month 6 weeks Year 1 Year 2 Year 3 Informed consent Stop TKI Follow-up EURO-SKI presented by FX Mahon at ASH 2016 Clinicaltrials.gov. identifier NCT
27 Participating countries of the EUROSKI Trial France 17 Norway 4 Denmark 4 Netherlands 3 Germany 21 Sweden 9 Czech Rep 6 Finland 1 Country Czech Republic Number of sites Number of patients 6 64 Denmark 4 33 Finland 1 31 France Germany Greece 1 44 Netherlands 3 96 Norway 4 27 Portugal 1 27 Spain 1 9 Sweden Total Portugal 1 Spain 1 Greece 1 29 EURO-SKI presented by FX Mahon at ASH 2016
28 Molecular recurrence-free survival (n=755) Months MRFS (95% CI) 6 months 61% (58% - 65%) 12 months 55% (51% - 58%) 18 months 52% (49% - 56%) 24 months 50% (47% - 54%) 36 months 47 % (43% - 51%) EURO-SKI presented by FX Mahon at ASH 2016
29 Treatment free remission Lessons from the past : how can we propose stopping treatment? Why stop TKI treatment in CML patients? Results of clinical trials Safety Predictive Factors Possible criteria for TKI discontinuation Future steps
30 Response to TKI Re-initiation: ENESTfreedom Cumulative incidence of MMR and MR 4.5 regained after nilotinib re-challenge 50% of all retreated patients achieved MMR and MR 4.5 by week 7.9 and week 15.0 of treatment re-initiation, respectively 99%(90/91) regained MMR after re-initiation at 144 weeks Hochhaus A, et al. Leukemia 2017, 31, Saglio et al. EHA 2018; (Abstract PF368)
31 Adverse events: TKI withdrawal syndrome? Musculoskeletal pain Joint pain Arthralgia Other Musculoskeletal pain in CML patients after discontinuation of imatinib: a tyrosine kinase inhibitor withdrawal syndrome? Richter J, et al. J Clin Oncol Mori et al. Am J Hematol 2015 Lee et al. Haematologica 2016
32 Musculoskeletal pain after stopping nilotinib AE grouping, n (%) b Consolidatio n (n = 100) ENESTfreedom First 48 weeks of TFR (n = 100) Second 48 weeks of TFR (n = 100) Consolidation (n = 73) ENESTop* First 48 weeks of TFR (n = 73) Second 48 weeks of TFR (n = 73) Musculoskeletal pain 17 (17) 34 (34) 9 (9) 10 (14) 35 (48) 11 (15) Rash 5 (5) 1 (1) 1 (1) 3 (4) 0 2 (3) CVEs 3 (3) 2 (2) 1 (1) 2 (3) 0 2 (3) Ischemic heart disease Ischemic cerebrovascular events 1 (1) 0 1 (1) 1 (1) (1) 1 (1) Peripheral arterial occlusive disease 1 (1) 1 (1) 0 1 (1) 0 1 (1) Other (1) c Fluid retention 3 (3) 4 (4) 4 (4) 2 (3) 9 (12) 7 (10) Local label is not approved Hochhaus A, et al. Leukemia 2017, 31, Hughes T et al., Poster presentation at EHA Annual Meeting; June 23,
33 Dasatinib Discontinuation in Patients with Chronic-Phase CML and Stable DMR (DASFREE, N=84) Forty-three of 84 pts (51%) lost MMR. Shah N et al. ASH 2017
34 Treatment free remission Lessons from the past : how can we propose stopping treatment? Why stop TKI treatment in CML patients? Results of clinical trials Safety Predictive Factors Possible criteria for TKI discontinuation Future steps
35 Sokal score and treatment duration in the STIM1 study Etienne G, et al. JCO. 2017;35:
36 Takahashi N et al. Int J Hematol., 2017, DOI /s x KR
37 DADI (dasatinib discontinuation) Study (N=88) N=88 Imagawa et al. Lancet Haematol 2015; 2: e528-e535.
38 Rea Rea et al. et Blood. al; Blood 2014;124(21) 2017; 129: [abstract 811]. Treatment-Free Survival in MMR, % KR STOP 2G-TKI: TFR Following Second- Generation TKIs 100 Frontline/imatinib intolerant (n = 40) Suboptimal response/imatinib resistance (n = 12) At 12 mo: 65.6% (95% CI, 50.2%-79.7%) 41.6% (95% CI, 13.7%-65.5%) 20 0 P = Months After 2G-TKI Discontinuation
39 Duration of DMR Has Most Impact on the Success of Cessation of TKI Treatment in CML - Results from the EURO-SKI Trial Using the minimal p-value approach a 3.1 years cut-off was significant and chosen with respect to patient safety Saussele S et al.lancet Oncol. in press 2018
40 Duration of DMR Has Most Impact on the Success of Cessation of TKI Treatment in CML - Results from the EURO-SKI Trial KR Saussele S et al; Lancet Oncol. 2018;19:
41
42 Treatment free remission Lessons from the past : how can we propose stopping treatment? Why stop TKI treatment in CML patients? Results of clinical trials Safety Predictive Factors Possible criteria for TKI discontinuation Future steps
43 Clinical practice In US : NCCN Guideline but no molecular biology standardisation In Europe : ESMO Guideline, ELN (European leukaemia net) recommendation is in progress
44 Recommendation or personal guidance of stopping TKIS in good responder patients outside a clinical trial KR Key prerequisites Declaration to an international or national registry Very strict molecular monitoring with a certified laboratory expressing the results on the IS with sensitivity strictly >4-log No patient history of resistance to treatment Patients Patients with CP-CML treated with TKI for at least 5 y Three points of BCR-ABL level per year mandatory with MR4 during 3 following years or MR4.5 during 2 following years (1 point in MR4 could be acceptable) Molecular monitoring during TFR Monthly for the first 12 mo, every 2 mo in year 2, and every 3 mo thereafter Molecular relapse Defined by loss of MMR or BCR-ABL level IS >0.1%, which trigger for re-initiation of TKI therapy Re-challenge the treatment with the same TKI in the following month after loss of MMR Mahon FX Hematology Am Soc Hematol Educ Program 2017.
45 Rea D et al. Cancer 2018 (14): KR
46 Treatment free remission Lessons from the past : how can we propose stopping treatment? Why stop TKI treatment in CML patients? Results of clinical trials Safety Predictive Factors Possible criteria for TKI discontinuation Future steps
47 Treatment-Free Remission after a second Stop 69 Patients, Median follow-up 39 months (5-116) KR Legros L et al. Cancer 2017
48 Dose reduction option: The British Destiny study First chronic phase CML patients in at least stable MMR On TKI for at least 3 years Decreased their TKI to half the standard dose* for 12 months followed by complete cessation 174 patients (male 98; female 76) Molecular recurrence (lost MMR) lower in patients with stable MR 4 at entry (3 of 125 patients; 2.4%) than in those in MR 3 but not MR 4 (9 of 49 patients; 18.4%) (P <.001) *imatinib 200mg daily, nilotinib 200mg twice daily, or dasatinib 50mg daily. Clark RE, et al. Lancet Haematol. 2017, 7:e310-e316.
49 Going for Cure in CML is possible Cure (from the Latin cura which means care) disappearance of the disease and return to a normal healthy state. We could also take the example from microbiology and infectious diseases that persistence of bacteria does not necessarily imply relapse. John Goldman proposed some years ago the definition of operational cure. * Using an ultrasensitive PCR technique, a low level of BCR-ABL transcripts can be found in the blood of normal individuals. # Goldman J, Gordon M. Leuk Lymphoma. 2006;47:1-7. Biernaux C, et al. Blood. 1995;86: #Bose S, et al. Blood. 1998;92:
50 Subgroup of CML-SCs with a distinct molecular signature that selectively persisted during prolonged therapy
51 Conclusions TKI discontinuation is increasingly attempted in select CML patients with sustained DMR Multiple studies conducted with >2500 CML patients have shown ~50% patients with sustained DMR remain in remission for years upon TKI discontinuation Nilotinib received EU and US approval for inclusion of TFR data in product label in 2017 based on its largest clinical TFR programs showing higher rates of DMR. Patients who need re-treatment regain response promptly A peculiar TKI withdrawal syndrome in patients is possible TKI discontinuation is already occurring outside of clinical trials Saussele et al; Leukemia (2016) 30,
52
53 CURING CML is like to land on the Moon Improving outcomes for patients with CML globally
54 The CML patients Giora Sharf and Jan Geissler from The CML advocate network
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