Treatment of essential thrombocythemia in Europe: a prospective long-term observational study of 3649 high-risk patients in the EXELS study
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1 Published Ahead of Print on October 27, 2017, as doi: /haematol Copyright 2017 Ferrata Storti Foundation. Treatment of essential thrombocythemia in Europe: a prospective long-term observational study of 3649 high-risk patients in the EXELS study by Gunnar Birgegard, Carlos Besses, Martin Griesshammer, Luigi Gugliotta, Claire N. Harrison, Mohamed Hamdani, Jackie Wu, Henri Achenbach, and Jean-Jacques Kiladjian Haematologica 2017 [Epub ahead of print] Citation: Birgegard G, Besses C, Griesshammer M, Gugliotta L, Harrison CN, Hamdani M, Wu J, Achenbach H, and Kiladjian J-J. Treatment of essential thrombocythemia in Europe: a prospective long-term observational study of 3649 high-risk patients in the EXELS study. Haematologica. 2017; 102:xxx doi: /haematol Publisher's Disclaimer. E-publishing ahead of print is increasingly important for the rapid dissemination of science. Haematologica is, therefore, E-publishing PDF files of an early version of manuscripts that have completed a regular peer review and have been accepted for publication. E-publishing of this PDF file has been approved by the authors. After having E-published Ahead of Print, manuscripts will then undergo technical and English editing, typesetting, proof correction and be presented for the authors' final approval; the final version of the manuscript will then appear in print on a regular issue of the journal. All legal disclaimers that apply to the journal also pertain to this production process.
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23 Z 1. Swerdlow SH, Campo E, Harris NL, et al. WHO classification of tumours of haemopoietic and lymphoid tissues, 2nd edition. 4th ed. Lyon: IARC Press; Barbui T, Barosi G, Birgegard G, et al. Philadelphia-negative classical myeloproliferative neoplasms: critical concepts and management recommendations from European LeukemiaNet. J Clin Oncol. 2011;29(6): Xagrid Summary of Product Characteristics, Shire Pharmaceuticals Ltd (Accessed 3 September 2015, at _Product_Information/human/000480/WC pdf.) 4. Cortelazzo S, Finazzi G, Ruggeri M, et al. Hydroxyurea for patients with essential thrombocythemia and a high risk of thrombosis. N Engl J Med. 1995;332(17): Spivak JL, Hasselbalch H. Hydroxycarbamide: a user's guide for chronic myeloproliferative disorders. Expert Rev Anticancer Ther. 2011;11(3): Cerquozzi S, Tefferi A. Blast transformation and fibrotic progression in polycythemia vera and essential thrombocythemia: a literature review of incidence and risk factors. Blood Cancer J. 2015;5:e Kiladjian JJ, Chevret S, Dosquet C, Chomienne C, Rain JD. Treatment of polycythemia vera with hydroxyurea and pipobroman: final results of a randomized trial initiated in J Clin Oncol. 2011;29(29): Gisslinger H, Gotic M, Holowiecki J, et al. Anagrelide compared with hydroxyurea in WHO-classified essential thrombocythemia: the ANAHYDRET Study, a randomized controlled trial. Blood. 2013;121(10): Harrison CN, Campbell PJ, Buck G, et al. Hydroxyurea compared with anagrelide in high-risk essential thrombocythemia. N Engl J Med. 2005;353(1): Michiels JJ. Diagnostic criteria of the myeloproliferative disorders (MPD): essential thrombocythaemia, polycythaemia vera and chronic megakaryocytic granulocytic metaplasia. Neth J Med. 1997;51(2): Tefferi A, Thiele J, Orazi A, et al. Proposals and rationale for revision of the World Health Organization diagnostic criteria for polycythemia vera, essential thrombocythemia, and primary myelofibrosis: recommendations from an ad hoc international expert panel. Blood. 2007;110(4): Collett D. Modeling survival data in medical research, 2nd edition. Boca Raton, FL: Chapman & Hall/CRC; dd
24 13. Chu DK, Hillis CM, Leong DP, Anand SS, Siegal DM. Benefits and risks of antithrombotic therapy in essential thrombocythemia: a systematic review. Ann Intern Med. 2017;167(3): Harrison C. Rethinking disease definitions and therapeutic strategies in essential thrombocythemia and polycythemia vera. Hematology Am Soc Hematol Educ Program. 2010;2010: Ejerblad E, Kvasnicka HM, Thiele J, et al. Diagnosis according to World Health Organization determines the long-term prognosis in patients with myeloproliferative neoplasms treated with anagrelide: Results of a prospective long-term follow-up. Hematology. 2013;18(1): Laguna MS, Kornblihtt LI, Marta RF, Michiels JJ, Molinas FC. Effectiveness of anagrelide in the treatment of symptomatic patients with essential thrombocythemia. Clin Appl Thromb Hemost. 2000;6(3): Storen EC, Tefferi A. Long-term use of anagrelide in young patients with essential thrombocythemia. Blood. 2001;97(4): Lahuerta-Palacios JJ, Bornstein R, Fernandez-Debora FJ, et al. Controlled and uncontrolled thrombocytosis. Its clinical role in essential thrombocythemia. Cancer. 1988;61(6): Schmitz S, Stauch M, Schlag R. Anagrelide for the treatment of thrombocythaemia in daily clinical practice: a post-marketing observational survey on efficacy and safety performed in Germany. Onkologie. 2010;33(1-2): Buxhofer-Ausch V, Steurer M, Sormann S, et al. Influence of platelet and white blood cell counts on major thrombosis - analysis from a patient registry in essential thrombocythemia. Eur J Haematol. 2016;97(6): Birgegard G, Bjorkholm M, Kutti J, et al. Adverse effects and benefits of two years of anagrelide treatment for thrombocythemia in chronic myeloproliferative disorders. Haematologica. 2004;89(5): Engel PJ, Johnson H, Baughman RP, Richards AI. High-output heart failure associated with anagrelide therapy for essential thrombocytosis. Ann Intern Med. 2005;143(4): Valera MC, Parant O, Vayssiere C, Arnal JF, Payrastre B. Essential thrombocythemia and pregnancy. Eur J Obstet Gynecol Reprod Biol. 2011;158(2): Barbui T, Finazzi G, Carobbio A, et al. Development and validation of an International Prognostic Score of thrombosis in World Health Organization-essential thrombocythemia (IPSET-thrombosis). Blood. 2012;120(26): dd
25 25. Passamonti F, Rumi E, Arcaini L, et al. Prognostic factors for thrombosis, myelofibrosis, and leukemia in essential thrombocythemia: a study of 605 patients. Haematologica. 2008;93(11): Campbell PJ, Maclean C, Beer PA, et al. Correlation of blood counts with vascular complications in essential thrombocythemia: analysis of the prospective PT1 cohort. Blood. 2012;120(7): Lekovic D, Gotic M, Sefer D, Mitrovic-Ajtic O, Cokic V, Milic N. Predictors of survival and cause of death in patients with essential thrombocythemia. Eur J Haematol 2015;95(5): Tefferi A, Gangat N, Wolanskyj A. The interaction between leukocytosis and other risk factors for thrombosis in essential thrombocythemia. Blood. 2007;109(9):4105. dd
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35 Supplementary Data - Treatment of essential thrombocythemia in Europe: a prospective long-term observational study of 3649 high-risk patients in the EXELS study Gunnar Birgegård, Carlos Besses, Martin Griesshammer, Luigi Gugliotta, Claire N. Harrison, Mohamed Hamdani, Jackie Wu, Henri Achenbach and Jean-Jacques Kiladjian Supplementary Table 1. Cumulative event rates of thrombohemorrhagic events by overalltreatment analysis population. Treatment at time of event Predefined event Patients (events) n Anagrelide N=1127 Event rate Patients (events) n Other CRT N=2909 Event rate Anagrelide + other CRT N=451 Patients (events) n Event rate Major thrombotic events 66 (78) (267) (22) 2.37 With A-A 44 (51) (184) (11) 1.66 Without A-A 25 (27) (83) (11) 4.48 Arterial thrombotic 55 (65) (200) (21) 2.25 events With A-A 38 (45) (145) (11) 1.66 Without A-A 18 (20) (55) (10) 4.08 Venous thrombotic 12 (13) (67) (1) 0.11 events With A-A 6 (6) (39) Without A-A 7 (7) (28) (1) 0.39 Major hemorrhagic 30 (35) (59) (7) 0.69 events With A-A 25 (28) (38) (3) 0.49 Without A-A 7 (7) (21) (4) 1.2 Total thrombohemorrhagic 92 (113) (326) (29) 2.86 events With A-A 65 (79) (222) (14) 1.99 Without A-A 32 (34) (104) (15) 5.4 A-A, anti-aggregatory; CRT, cytoreductive therapy. 1
36 Supplementary Table 2. Cumulative event rates of other predefined events by overalltreatment analysis population. Treatment at time of event Predefined event Patients (events) n Anagrelide N=1127 Event rate Patients (events) n Other CRT N=2909 Event rate Anagrelide + other CRT N=451 Patients (events) n Event rate Any predefined event 262 (469) 739 (1332) 75 (137) Congestive heart failure 21 (24) (48) (3) 0.34 Cardiomyopathy 5 (5) (9) Atrial fibrillation 10 (11) (43) (4) 0.47 Other cardiovascular symptoms 63 (79) (134) (26) 2.83 Severe mucocutaneous disorders 7 (8) (74) (7) 0.69 Pulmonary hypertension 5 (5) (7) Pulmonary fibrosis/interstitial 2 (2) (10) pneumonia Pancreatitis (4) Rhabdomyolysis/myalgia 3 (3) (4) Non-hematological malignancy 17 (18) (161) (5) 0.46 CRT, cytoreductive therapy; PDE, predefined event. *Nine pregnancies in seven subjects were reported in the no treatment group (data not shown). 2
37 Supplementary Table 3. Most common cardiovascular predefined events by overall treatment population. Treatment at time of event Anagrelide N=1127 Other CRT N=2909 Anagrelide + other CRT N=451 Predefined event Patients, n (%) Events, n Patients, n (%) Events, n Patients, n (%) Events, n Palpitations 19 (1.69) 21 6 (0.21) 6 8 (1.77) 8 Tachycardia 23 (2.04) 26 4 (0.14) 5 6 (1.33) 6 Arrhythmias (excluding tachycardia) 16 (1.42) (1.65) 56 5 (1.11) 5 CRT, cytoreductive therapy. 3
38 Supplementary Table 4. Cumulative event rates of suspected serious adverse reactions by overall-treatment analysis population and organ class, in the overall treatment safety population. SSAR system organ class Patients (events) n Anagrelide N=1127 Patientyears exposure * Event rate ** Patients (events) n Other CRT N=2909 Patientyears exposure * Event rate** Patients (events) n Total N=451 Patientyears exposure * 4 Event rate ** Any SSAR 37 (49) (77) (118) Blood and lymphatic system 2 (2) (16) (16) disorders Cardiac disorders 17 (22) (5) (26) Gastrointestinal disorders 6 (6) (6) (11) General disorders and administration 1 (1) (1) < (2) site conditions Immune system disorders (1) < (1) <0.01 Infections and infestations 1 (1) (3) (4) Injury, poisoning, and procedural 1 (1) (2) (3) complications Investigations (1) < (1) <0.01 Musculoskeletal and connective 1 (1) (1) <0.01 tissue disorders Neoplasm benign, malignant, and unspecified 2 (2) (19) (20) (including cysts and polyps) Nervous system disorders 2 (2) (10) (11) Psychiatric disorders 1 (1) (1) < (1) <0.01 Reproductive system and (1) < (1) <0.01 breast disorders Respiratory thoracic, and mediastinal 7 (9) (4) (12) disorders Skin and subcutaneous disorders (6) (6) Vascular disorders 1 (1) (1) < (2) CRT, cytoreductive therapy; SSAR, suspected serious adverse reactions. *Exposure is calculated at the time of each event, or up to the end of the study for patients who did not experience an event.
39 **The event rate is calculated as the number of patients with events/100 patient-years exposure. Patients who received anagrelide + other are included in both the anagrelide and other treatment groups for analysis of SSARs. Events are excluded if the start date was on or after the date of first treatment change (or date of first treatment change plus 28 days if followed by a no-treatment period). Since subjects were allowed to switch treatments during the study, they could be counted in more than one treatment group in the overall-treatment analysis. 5
40 Supplementary Table 5. Baseline characteristics considered in the multivariate analysis. Baseline characteristics ET diagnosis* (WHO, PVSG, other) Age* (<65 years, 65 years) Sex* Time since diagnosis* (0 <1 years, 1 <5 years, 5 <10 years, 10 years) Cardiovascular risk factors* Normal cardiac function* Aspirin at registration** Hemorrhagic or vascular events* Initial platelet count 1000x10 9 /L* Blood pressure Body mass index Hypercholesterolemia* Diabetes* Smoking* Hypertension* ET, essential thrombocythemia; PVSG, Polycythemia Vera Study Group; WHO, World Health Organization. *Indicates baseline characteristics included in the Cox regression model to account for imbalance between anagrelide vs anagrelide + anti-aggregatory therapy at registration. **The variable aspirin at registration was used for the multivariate analysis in the overall population to identify risk factors. The variable anti-aggregatory therapy at registration was used for the multivariate analysis in the first-treatment population. 6
41 Supplementary Figure 1. EXELS study design. *Includes all patients who received at least one dose of CRT. Seventy-two patients were excluded from the safety population as they did not receive CRT post-registration. **Other CRT group includes patients who received: hydroxycarbamide, busulphan, interferon-α, pegylated interferon, pipobroman, sodium phosphate P32, thromboreductin (anagrelide). ***Includes patients who did not receive CRT within 10 days of study registration, but subsequently initiated CRT, or patients for whom no CRT information was available. 7
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