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1 Supplementary Appendix This appendix has been provided by the authors to give readers additional information about their work. Supplement to: Dimopoulos MA, Tedeschi A, Trotman J, et al. Phase 3 trial of ibrutinib plus rituximab in Waldenström s macroglobulinemia. N Engl J Med 2018;378: DOI: /NEJMoa
2 SUPPLEMENTARY APPENDIX TABLE OF CONTENTS: List of Participating Investigators... 3 Supplementary Methods... 4 Supplementary Results... 6 Supplementary Figures S1-S Supplementary Tables S1-S References
3 Participating Investigators and Patient Enrollment by Country Dr. Ranjani H. Advani, Dr. Bertrand Arnulf, Dr. Thérèse Aurran-Schleinitz, Dr. Luca Baldini, Dr. Jorge J. Castillo, Dr. Christine Chen, Dr. Robert Franklin Cornell, Dr. Martin Dreyling, Dr. Meletios Athanasios Dimopoulos, Dr. Jehan Dupuis, Dr. Herbert Eradat, Dr. Carlos Fernandez de Larrea, Dr. Pierre Feugier, Dr. Richard R. Furman, Dr. Ramon Garcia Sanz, Dr. Miquel Granell Gorrochategui, Dr. Evdoxia Hatjiharissi, Dr. Holger Hebart, Dr. Leonard Heffner, Dr. Charles Herbaux, Dr. Jose Angel Hernandez Rivas, Dr. Georg Hess, Dr. Lionel Karlin, Dr. Mary-Margaret Keating, Dr. Mary-Christine Kyrtsonis, Dr. Vincent Launay, Dr. Véronique Leblond, Dr. Hui-Peng Lee, Dr. Shuo Ma, Dr. Beatrice Mahe, Dr. Jeffrey Matous, Dr. Helen McCarthy, Dr. Albert Oriol Rocafiguera, Dr. Lorella Orsucci, Dr. Maria Lia Palomba, Dr. Michael Pfreundschuh, Dr. Chaim Shustik, Dr. Argiris Symeonidis, Dr. Dipti Talaulikar, Dr. Constantine Tam, Dr. Alessandra Tedeschi, Dr. Olivier Tournilhac, Dr. Ralf Ulrich Trappe, Dr. Judith Trotman, Dr. Marzia Varettoni, Dr. Christopher Paul Venner, Dr. David Vesole, Dr. Francesco Zaja. Country Number of Patients Enrolled Australia 22 Canada 15 France 27 Germany 6 Greece 23 Italy 23 Spain 13 United Kingdom 2 United States 19 Total 150 3
4 Supplementary Methods Study end points Sustained hematologic improvement was defined as an increase in hemoglobin sustained continuously for at least 56 days without transfusion or growth factors, as measured by an increase from baseline of 2 g/dl, or for patients with baseline anemia, an increase to a hemoglobin level of >11 g/dl. Quality of life end points included FACT-An total score and an anemia subscale score; clinically meaningful improvement was defined as an increase of 7 points in FACT-An total score and 6 points in anemia subscale score. 1 Safety assessments included evaluation of adverse events (AEs) and measurement of laboratory variables. The severity of the AEs was graded according to the Common Toxicity Criteria for Adverse Events, version Genomic analysis Bone marrow aspiration or formalin-fixed paraffin-embedded specimens of blood clots were collected prior to treatment initiation. No further process was performed to enrich tumor cells and a minimal tumor content of 10% evaluated by an external central pathology laboratory was required to pass the quality control for genetic sequencing. MYD88 and CXCR4 mutations status was assessed using the ACE Extended Cancer Panel targeted exome sequencing (Personalis, Menlo Park, CA). This panel includes over 1400 genes involved in cancer biology and more than 200 cancer-related noncoding RNAs. The limit of detection of the data analysis pipeline was set at 2% allele frequency. CXCR4WHIM somatic mutations were defined as any loss-of-function mutations, including premature termination nonsense point mutations and frameshift insertion or deletion mutations, located in the carboxyl terminal regions, usually between codon 311 to Statistical analysis 4
5 The primary analysis for PFS was a 2-sided log-rank test stratified according to IPSSWM (low, intermediate, high) and number of prior regimens (0, 1). The alpha spending for PFS was determined based on the actual information fraction using the O Brien-Fleming boundary. Tests of secondary end points were performed at the 2-sided significance level of 0.05 in a sequential hierarchical manner based on a closed testing procedure. The subgroup analyses of PFS are based on an unstratified Cox model. 5
6 Supplementary Results Consistent with the improvement in progression-free survival, analysis of the time to next treatment for the overall population showed a statistically significant advantage for ibrutinibrituximab compared with placebo-rituximab with 92% of patients on ibrutinib-rituximab versus 41% of patients on placebo-rituximab not requiring any subsequent therapy at 30 months (median, not reached vs months; P<0.001) (Fig. S6). 6
7 Supplementary Figures S1-S6 Figure S1. Consort Diagram. 150 randomized 1:1 75 randomized to ibrutinib/rituximab 75 randomized to placebo/rituximab 75 analyzed for efficacy outcomes 75 analyzed for efficacy outcomes 75 received daily ibrutinib (420 mg) and rituximab for up to 8 infusions (weeks 1-4 and 17-20) 75 received daily placebo and rituximab for up to 8 infusions (weeks 1-4 and 17-20) 19 discontinued ibrutinib Progressive disease 7 Adverse events 4 Withdrawal by patient 6 Investigator decision 2 5 discontinued rituximab early* Progressive disease 2 Adverse events 3 49 discontinued placebo Progressive disease 33 Adverse event 3 Withdrawal by patient 7 Investigator decision 6 22 discontinued rituximab early* Progressive disease 6 Adverse events 9 Withdrawal by patient 4 Investigator decision 3 56 continuing ibrutinib 70 completed rituximab therapy 26 continuing placebo 53 completed rituximab therapy 6 withdrew from study Death 3 Withdrawal of consent 3 11 withdrew from study Death 6 Lost to follow-up 1 Withdrawal of consent 4 56 continuing treatment at time of clinical cutoff 13 on post-treatment follow-up 26 continuing treatment 38 on post-treatment follow-up 69 on study follow-up at time of clinical cutoff 64 on study follow-up at time of clinical cutoff** *Discontinued rituximab before the completion of 8 infusions. **30 patients crossed over to ibrutinib after IRC-confirmed progression. 7
8 Figure S2. Progression-Free Survival by Prior Treatment History, Mutation Status, and IPSSWM Risk Score with versus Placebo-Rituximab. Shown are progression-free survival curves as assessed by the independent review committee in different subgroups. The tick marks indicate patients with censored data. Panel A and Panel B show progression-free survival for treatment-naïve and relapsed patients, respectively. Panel C shows progression-free survival by MYD88 and CXCR4 mutation status. Panel D shows progression-free survival for patients with low, intermediate, and high IPSSWM risk scores at baseline. A. Patients With Progression-Free Survival (%) Placebo-Rituximab Months No. at Risk Placebo-Rituximab
9 B. Patients With Progression-Free Survival (%) Placebo-Rituximab Months No. at Risk Placebo-Rituximab
10 C. Patients With Progression-Free Survival (%) No. at Risk Months MYD88 L265P /CXCR4 WT MYD88 L265P /CXCR4 WHIM MYD88 WT /CXCR4 WT Placebo-Rituximab MYD88 L265P /CXCR4 WT MYD88 L265P /CXCR4 WHIM MYD88 WT /CXCR4 WT Placebo-Rituximab MYD88 L265P /CXCR4 WT MYD88 L265P /CXCR4 WHIM MYD88 WT /CXCR4 WT MYD88 L265P /CXCR4 WT MYD88 L265P /CXCR4 WHIM MYD88 WT /CXCR4 WT
11 D. Patients With Progression-Free Survival (%) No. at Risk High Intermed. Low Placebo-Rituximab High High Intermediate Low Placebo-Rituximab High Intermediate Low Months Intermed. Low
12 Figure S3. Best Response Rates with and Placebo-Rituximab by Genotype. Shown are the best response to treatment as assessed by the independent review committee in each treatment group by MYD88 and CXCR4 mutation status. Categories for response assessments included complete response (CR), very good partial response (VGPR), partial response (PR), and minor response (MR). Best Response (%) Ibrutinib- Rituximab Placebo- Rituximab Ibrutinib- Rituximab Placebo- Rituximab Ibrutinib- Rituximab Placebo- Rituximab MYD88 L265P /CXCR4 WT MYD88 L265P /CXCR4 WHIM MYD88 WT /CXCR4 WT CR VGPR PR MR 12
13 Figure S4. Change in IgM Over Time with versus Placebo-Rituximab. Shown are the mean IgM levels over time for patients who had baseline IgM levels 50 g/l in each treatment arm. The error bars represent the standard error of the mean (SEM). Mean IgM (g/l) Placebo-Rituximab Months No. of Patients Placebo-Rituximab
14 Figure S5. Overall Treatment Course of Patients Treated with Who Experienced Atrial Fibrillation. Shown are individual patients on the ibrutinib-rituximab arm who experienced atrial fibrillation. The time is indicated in months since treatment initiation. Dose modifications, including dose reductions, treatment interruptions, and treatment discontinuations for each patient are shown. 67 years/male* 72 years/female 70 years/female* 76 years/male 75 years/male** 85 years/female 76 years/male 78 years/male 63 years/female* 77 years/male 72 years/female Months 420 mg 280 mg 140 mg Afib start Discontinuation due to Afib Afib end Withdrawal by Patient Ongoing treatment Discontinuation due to PD 0 mg PD by IRC *Atrial fibrillation is not associated with dose reduction or treatment interruption. **Only the first atrial fibrillation event resulted in treatment interruption. 14
15 Figure S6. Time to Next Treatment with versus Placebo-Rituximab. Shown is time to next treatment with ibrutinib-rituximab versus placebo-rituximab. The tick marks indicate patients with censored data. Patients Without Subsequent Therapy (%) Placebo-Rituximab 20 Placebo-Rituximab 10 Median (mo) 18.1 NR Hazard ratio 0.1 (95% CI, ), P< Months No. at Risk Placebo-Rituximab
16 Supplementary Tables S1-S6 Table S1. International Prognostic Scoring System for Waldenstrom s macroglobulinemia 3 Factors associated with Prognosis Value Age >65 years Hemoglobin 11.5 g/dl Platelet count 100 x 10 9 /L b2-microglobulin >3 mg/l Serum monoclonal IgM >7.0 g/dl Risk Category Score Low risk 0 or 1 factors ( 65 years) Intermediate risk 2 factors OR age > 65 years High risk >2 factors 16
17 Table S2. Modified Response and Progression Criteria for Investigator Assessment. Category Response Criteria* Complete response (CR) Very good partial response (VGPR) Partial response (PR) Minor response (MR) Stable disease (SD) Progressive disease (PD) Definition of Response Rates ǁ Serum IgM values in the normal range Disappearance of monoclonal protein by immunofixation (Note: Reconfirmation of CR status is required with a second immunofixation at any time point) No histological evidence of bone marrow involvement Complete resolution of lymphadenopathy /splenomegaly if present at baseline At least 90% reduction of serum IgM from baseline or serum IgM values in normal range Reduction in lymphadenopathy /splenomegaly if present at baseline At least 50% reduction of serum IgM from baseline Reduction in lymphadenopathy /splenomegaly if present at baseline At least 25% but less than 50% reduction of serum IgM from baseline Not meeting criteria for CR, VGPR, PR, MR, or progressive disease At least one of the following: A 25% increase in serum IgM with a total increase of at least 500 mg/dl from nadir Confirmation of the initial IgM increase is required when IgM is sole criterion for PD Appearance of new lymph nodes >1.5 cm in any axis, 50% increase from nadir in sum of product of diameters of one or more node, or 50% increase in longest diameter of a previously identified node >1 cm in short axis Appearance of new splenomegaly or 50% increase from nadir in enlargement of the spleen Appearance of new extranodal disease New or recurrent involvement in bone marrow New symptomatic disease (based on presence of malignant pleural effusion, Bing Neel syndrome, amyloidosis or light chain deposition disease, or other paraprotein-mediated disorder Overall response rate Major response rate Proportion of patients who achieve an MR or better Proportion of patients who achieve PR or better *Primary activity evaluations are based on independent review committee evaluations. A target lesion is defined as a lymph node with a long axis >1.5 cm or a short axis >1.0 cm. Splenomegaly is defined as the longest cranial-caudal measurement of the spleen >13 cm. 17
18 Nadir for serum IgM is defined as the lowest serum IgM value obtained at any time from baseline with the exception that serum IgM levels post-g will not be considered for up to 35 days. ǁ The protocol defines overall response rate as patients who achieve PR or better based on the standard definition used in other tumor types. In the Waldenström s Macroglobulinemia community, overall response refers to patients who achieve an MR or better and major response refers to patients who achieve a PR or better. 4 To minimize confusion and misinterpretation among hematologists, we are using the familiar terminology, as indicated in the table above, and not the protocol-specified definition. 18
19 Table S3. Reasons for Initiating Treatment. Variable no. of patients (%)* (n = 75) Placebo-Rituximab (n = 75) Any symptomatic disease criteria 75 (100) 75 (100) Fatigue 42 (56) 49 (65) Constitutional symptoms 19 (25) 29 (39) Night sweats 13 (17) 22 (29) Weight loss 10 (13) 14 (19) Fever 3 (4) 5 (7) Hemoglobin 10g/dL 20 (27) 28 (37) Serum IgM >5 g/dl with or without symptoms 18 (24) 12 (16) Peripheral neuropathy due to WM 15 (20) 8 (11) Hyperviscosity 9 (12) 10 (13) Lymphadenopathy 7 (9) 6 (8) Symptomatic hepatomegaly/splenomegaly/organ tissue 2 (3) 7 (9) infiltration Platelet count < /L 2 (3) 6 (8) Neuropathy related to WM 3 (4) 3 (4) Symptomatic cryoglobulinemia 2 (3) 3 (4) Cold agglutinin anemia 1 (1) 2 (2) IgM related immune hemolytic anemia/thrombocytopenia 0 4 (5) Amyloidosis related to WM 2 (3) 0 19
20 Table S4. Adverse Events Leading to Discontinuation of Treatment and Death. Patient Age/Sex Discontinuation of Ibrutinib Adverse Event Treatment Duration Outcome 64 years/male Interstitial lung disease (grade 2) 896 days Not recovered/resolved 76 years/male Atrial fibrillation (grade 3) 432 days Not recovered/resolved 78 years/male Atrial fibrillation (grade 3) 378 days Recovered/resolved 77 years/male Atrial fibrillation (grade 1) 82 days Not recovered/resolved Discontinuation of Rituximab Macular rash (grade 2) 82 days Recovered/resolved 78 years/male Prinzmetal angina (grade 3) 113 days Recovered/resolved 77 years/male Atrial fibrillation (grade 1) 22 days Not recovered/resolved Placebo-Rituximab Discontinuation of Placebo 60 years/male* Immune thrombocytopenic purpura (grade 4) 56 days Not recovered/resolved 73 years/male Brugada syndrome (grade 2) 45 days Not recovered/resolved 78 years/male** Asthenia (grade 3) 13 days Not recovered/resolved Discontinuation of Rituximab 43 years/male Infusion-related reactions (grade 2) 154 days Recovered/resolved 61 years/female Infusion-related reactions (grade 3) 134 days Recovered/resolved 62 years/male Infusion-related reactions (grade 2) 128 days Recovered/resolved 68 years/male Infusion-related reactions (grade 2) 120 days Recovered/resolved 59 years/female Infusion-related reactions (grade 3) 114 days Recovered/resolved 75 years/male Infusion-related reactions (grade 3) 111 days Recovered/resolved 73 years/male Brugada syndrome (grade 2) 42 days Not recovered/resolved 54 years/male Infusion-related reactions (grade 3) 8 days Recovered/resolved 78 years/male Asthenia (grade 3) 8 days Not recovered/resolved Deaths 60 years/male* Intracranial hemorrhage 56 days Death 66 years/male Nervous system disorder 30 days Death 78 years/male** Not specified 13 days Death *Same patient who discontinued treatment and subsequently died. ** Same patient who discontinued treatment and subsequently died. 20
21 Table S5. Adverse Events Leading to Dose Reductions of Ibrutinib in the Ibrutinib + Rituximab Arm. Patient Age/Sex 68 years/female Adverse Event Upper airway cough syndrome (grade 1) Start Date of Dose Reduction End Date of Dose Reduction Dose Reduced To Outcome Day 293 Day mg Not recovered/resolved Muscle spasms (grade 2) Day 810 Ongoing 140 mg Recovered/resolved 62 years/male Decreased neutrophil count (grade 3) 66 years/male Increased gamma glutamyl-transferase (grades 2 and 3) Day 121 Day mg Recovered/resolved Day 953 Ongoing 280 mg Recovered/resolved 76 years/male Atrial fibrillation (grade 3) Day 281 Day mg Recovered/resolved 66 years/male Neutropenia (grade 3) Day 684 Ongoing 280 mg Recovered/resolved 81 years/male Staphylococcal skin infection (grade 2) 83 years/female 77 years/female Allergic dermatitis (grade 3) Fatigue (grade 3; 2 episodes) Day 155 Day mg and 140 mg Recovered/resolved Day 449 Ongoing Recovered/resolved Day 297 Ongoing 280 mg and 140 mg Recovered/resolved Muscle spasms (grade 2) Day 232 Ongoing 280 mg Not recovered/resolved 63 years/male Joint swelling (grade 3) Day 566 Ongoing 280 mg and 140 mg Recovered/resolved 85 years/male Hematochezia (grade 2) Day 566 Ongoing 280 mg Recovered/resolved 72 years/female Atrial fibrillation (grade 3) Day 731 Ongoing 280 mg Recovered/resolved 61 years/male Neutropenia (grade 4) Day 155 Ongoing 280 mg Recovered/resolved 64 years/male Neutropenia (grade 4) Day 561 Ongoing 280 mg Recovered/resolved 21
22 Table S6. Summary of Major Hemorrhage Events* in Patients Treated with versus Placebo-Rituximab. Patient Age/Sex Major Hemorrhage Event Start Date End Date Action Taken Outcome 70 years/female Hemoptysis (grade 3) Day 349 Day 362 Dose not changed Recovered/resolved 83 years/male Melaena (grade 3) Day 842 Day 859 Drug interrupted Recovered/resolved 75 years/male Purpura Day 102 Day 116 Dose not changed Recovered/resolved Placebo-Rituximab 66 years/female Epistaxis (grade 3) Day 154 Day 180 Drug interrupted Recovered/resolved 60 years/male Immune thrombocytopenic purpura (grade 4) Gastrointestinal hemorrhage (grade 4) Intracranial hemorrhage (grade 5) Day 57 Ongoing Drug withdrawn Not recovered/resolved Day 70 Day 72 Not applicable Recovered/resolved Day 73 Ongoing Not applicable Fatal 76 years/male Hematuria (grade 3) Day 496 Day 502 Dose not changed Recovered/resolved *Major hemorrhage was defined as any serious or grade 3 hemorrhage or any grade central nervous system hemorrhage. 22
23 References 1. Cella D. The Functional Assessment of Cancer Therapy-Anemia (FACT-An) Scale: a new tool for the assessment of outcomes in cancer anemia and fatigue. Semin Hematol 1997;34(3 Suppl 2): Hunter ZR, Xu L, Yang G, et al. The genomic landscape of Waldenström macroglobulinemia is characterized by highly recurring MYD88 and WHIM-like CXCR4 mutations, and small somatic deletions associated with B-cell lymphomagenesis. Blood 2014;123, Morel P, Duhamel A, Gobbi P, et al. International prognostic scoring system for Waldenstrom macroglobulinemia. Blood 2009;113: Leblond V, Kastritis E, Advani R, et al. Treatment recommendations from the Eighth International Workshop on Waldenstrom's Macroglobulinemia. Blood 2016;128:
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