Polycythemia Vera: An Appraisal of the Biology and Management 10 Years After the Discovery of JAK2 V617F.

Polycythemia vera (PV) is a chronic myeloproliferative neoplasm that is associated with a substantial symptom burden, thrombohemorrhagic complications, and impaired survival. A decade after the seminal discovery of an activating mutation in the tyrosine kinase JAK2 in nearly all patients with PV, new treatment options are finally beginning to emerge, necessitating a critical reappraisal of the underlying pathogenesis and therapeutic modalities available for PV. Herein, we comprehensively review clinical aspects of PV including diagnostic considerations, natural history, and risk factors for thrombosis. We summarize recent studies delineating the genetic basis of PV, including their implications for evolution to myelofibrosis and secondary acute myeloid leukemia. We assess the quality of evidence to support the use of currently available therapies, including aspirin, phlebotomy, hydroxyurea, and interferon. We analyze recent studies evaluating the safety and efficacy of JAK inhibitors, such as ruxolitinib, and evaluate their role in the context of other available therapies for PV. This review provides a framework for practicing hematologists and oncologists to make rational treatment decisions for patients with PV.

[1]  Paola Guglielmelli,et al.  Effect of mutation order on myeloproliferative neoplasms. , 2015, The New England journal of medicine.

[2]  M. Griesshammer,et al.  Ruxolitinib versus standard therapy for the treatment of polycythemia vera. , 2015, The New England journal of medicine.

[3]  J. Hernández-Boluda,et al.  Target hematologic values in the management of essential thrombocythemia and polycythemia vera , 2015, European journal of haematology.

[4]  S. Carillo,et al.  Presence of calreticulin mutations in JAK2-negative polycythemia vera. , 2014, Blood.

[5]  T. Barbui,et al.  Long-term survival and blast transformation in molecularly annotated essential thrombocythemia, polycythemia vera, and myelofibrosis. , 2014, Blood.

[6]  M. Ochs,et al.  Two clinical phenotypes in polycythemia vera. , 2014, The New England journal of medicine.

[7]  R. Hoffman,et al.  The orally bioavailable MDM2 antagonist RG7112 and pegylated interferon α 2a target JAK2V617F-positive progenitor and stem cells. , 2014, Blood.

[8]  K. Döhner,et al.  Distinct clustering of symptomatic burden among myeloproliferative neoplasm patients: retrospective assessment in 1470 patients. , 2014, Blood.

[9]  R. Hoffman,et al.  Optimal therapy for polycythemia vera and essential thrombocythemia can only be determined by the completion of randomized clinical trials , 2014, Haematologica.

[10]  M. Björkholm,et al.  Leukemic transformation in myeloproliferative neoplasms: therapy-related or unrelated? , 2014, Best practice & research. Clinical haematology.

[11]  Hongwei Wang,et al.  Epidemiology of myeloproliferative neoplasms in the United States , 2014, Leukemia & lymphoma.

[12]  T. Barbui,et al.  An overview on CALR and CSF3R mutations and a proposal for revision of WHO diagnostic criteria for myeloproliferative neoplasms , 2014, Leukemia.

[13]  J. D. Fitzpatrick,et al.  Somatic CALR mutations in myeloproliferative neoplasms with nonmutated JAK2. , 2013, The New England journal of medicine.

[14]  P. Campbell,et al.  Order Matters: Sequence Of Mutation Acquisition In Myeloproliferative Neoplasms Impacts Disease Pathogenesis and Stem Cell Potency , 2013 .

[15]  M. Cazzola,et al.  A phase 2 study of ruxolitinib, an oral JAK1 and JAK2 inhibitor, in patients with advanced polycythemia vera who are refractory or intolerant to hydroxyurea , 2013, Cancer.

[16]  F. Camargo,et al.  Essential role of PR-domain protein MDS1-EVI1 in MLL-AF9 leukemia. , 2013, Blood.

[17]  R. Silver,et al.  Evaluation of WHO criteria for diagnosis of polycythemia vera: a prospective analysis. , 2013, Blood.

[18]  M. Cazzola,et al.  Mutations and prognosis in primary myelofibrosis , 2013, Leukemia.

[19]  O. Abdel-Wahab,et al.  Molecular analysis of patients with polycythemia vera or essential thrombocythemia receiving pegylated interferon α-2a. , 2013, Blood.

[20]  M. Cazzola,et al.  Survival and prognosis among 1545 patients with contemporary polycythemia vera: an international study , 2013, Leukemia.

[21]  T. Barbui,et al.  Revised response criteria for polycythemia vera and essential thrombocythemia: an ELN and IWG-MRT consensus project. , 2013, Blood.

[22]  T. Barbui,et al.  A phase II study of Givinostat in combination with hydroxycarbamide in patients with polycythaemia vera unresponsive to hydroxycarbamide monotherapy , 2013, British journal of haematology.

[23]  P. Campbell,et al.  Clonal analyses reveal associations of JAK2V617F homozygosity with hematologic features, age and gender in polycythemia vera and essential thrombocythemia , 2013, Haematologica.

[24]  E. Ejerblad,et al.  Patients with polycythemia vera have worst impairment of quality of life among patients with newly diagnosed myeloproliferative neoplasms , 2013, Leukemia & lymphoma.

[25]  T. Barbui,et al.  Cardiovascular events and intensity of treatment in polycythemia vera. , 2013, The New England journal of medicine.

[26]  S. Bojesen,et al.  Diagnostic value of JAK2 V617F somatic mutation for myeloproliferative cancer in 49 488 individuals from the general population , 2013, British journal of haematology.

[27]  M. Griesshammer,et al.  Myeloproliferative neoplasm (MPN) symptom assessment form total symptom score: prospective international assessment of an abbreviated symptom burden scoring system among patients with MPNs. , 2012, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[28]  B. Bellosillo,et al.  Red cell mass measurement in patients with clinically suspected diagnosis of polycythemia vera or essential thrombocythemia , 2012, Haematologica.

[29]  P. Campbell,et al.  JAK2V617F homozygosity arises commonly and recurrently in PV and ET, but PV is characterized by expansion of a dominant homozygous subclone. , 2012, Blood.

[30]  T. Barbui,et al.  Front-line therapy in polycythemia vera and essential thrombocythemia. , 2012, Blood reviews.

[31]  A. Nagler,et al.  JAK2V617F allele burden is associated with transformation to myelofibrosis , 2012, Leukemia & lymphoma.

[32]  R. Mesa,et al.  Association between quality of life and clinical parameters in patients with myeloproliferative neoplasms , 2012, Leukemia & lymphoma.

[33]  B. Bellosillo,et al.  Assessment and prognostic value of the European LeukemiaNet criteria for clinicohematologic response, resistance, and intolerance to hydroxyurea in polycythemia vera. , 2012, Blood.

[34]  A. Rademaker,et al.  Age-related differences in disease characteristics and clinical outcomes in polycythemia vera , 2011, Leukemia & lymphoma.

[35]  W. Vainchenker,et al.  Complete Hematological, Molecular and Histological Remissions without Cytoreductive Treatment Lasting After Pegylated-Interferon α-2a (peg-IFNα-2a) Therapy in Polycythemia Vera (PV): Long Term Results of a Phase 2 Trial , 2011 .

[36]  S. Chevret,et al.  Treatment of polycythemia vera with hydroxyurea and pipobroman: final results of a randomized trial initiated in 1980. , 2011, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[37]  T. Barbui,et al.  The Myeloproliferative Neoplasm Symptom Assessment Form (MPN-SAF): international prospective validation and reliability trial in 402 patients. , 2011, Blood.

[38]  F. Granath,et al.  Treatment-related risk factors for transformation to acute myeloid leukemia and myelodysplastic syndromes in myeloproliferative neoplasms. , 2011, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[39]  M. Griesshammer,et al.  Philadelphia-negative classical myeloproliferative neoplasms: critical concepts and management recommendations from European LeukemiaNet. , 2011, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[40]  A. Tefferi,et al.  LNK mutations in JAK2 mutation-negative erythrocytosis. , 2010, The New England journal of medicine.

[41]  M. Cazzola,et al.  A prospective study of 338 patients with polycythemia vera: the impact of JAK2 (V617F) allele burden and leukocytosis on fibrotic or leukemic disease transformation and vascular complications , 2010, Leukemia.

[42]  J. Gotlib,et al.  JAK2 V617F and beyond: role of genetics and aberrant signaling in the pathogenesis of myeloproliferative neoplasms , 2010, Expert review of hematology.

[43]  J. Soulier,et al.  Mutation in TET2 in myeloid cancers. , 2009, The New England journal of medicine.

[44]  T. Barbui,et al.  Leukocytosis is a risk factor for recurrent arterial thrombosis in young patients with polycythemia vera and essential thrombocythemia , 2009, American journal of hematology.

[45]  T. Barbui,et al.  JAK2V617F allele burden and thrombosis: a direct comparison in essential thrombocythemia and polycythemia vera. , 2009, Experimental hematology.

[46]  T. Barbui,et al.  Perspectives on thrombosis in essential thrombocythemia and polycythemia vera: is leukocytosis a causative factor? , 2009, Blood.

[47]  M. Griesshammer,et al.  Response criteria for essential thrombocythemia and polycythemia vera: result of a European LeukemiaNet consensus conference. , 2009, Blood.

[48]  D. Gilliland,et al.  TET2 mutations and their clinical correlates in polycythemia vera, essential thrombocythemia and myelofibrosis , 2009, Leukemia.

[49]  S. Chevret,et al.  Pegylated interferon-alfa-2a induces complete hematologic and molecular responses with low toxicity in polycythemia vera. , 2008, Blood.

[50]  H. Kantarjian,et al.  The natural history and treatment outcome of blast phase BCR-ABL- myeloproliferative neoplasms. , 2008, Blood.

[51]  R. Silver,et al.  The revised World Health Organization diagnostic criteria for polycythemia vera, essential thrombocytosis, and primary myelofibrosis: an alternative proposal. , 2008, Blood.

[52]  P. Fenaux,et al.  Classification of myeloproliferative disorders in the JAK2 era: is there a role for red cell mass? , 2008, Leukemia.

[53]  P. Guglielmelli,et al.  Influence of JAK2V617F allele burden on phenotype in essential thrombocythemia , 2008, Haematologica.

[54]  M. Cazzola,et al.  A dynamic prognostic model to predict survival in post-polycythemia vera myelofibrosis. , 2007, Blood.

[55]  C. Bloomfield,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. , 2007, Blood.

[56]  A. Tefferi,et al.  Leucocytosis in polycythaemia vera predicts both inferior survival and leukaemic transformation , 2007, British journal of haematology.

[57]  Paola Guglielmelli,et al.  Clinical profile of homozygous JAK2 617V>F mutation in patients with polycythemia vera or essential thrombocythemia. , 2007, Blood.

[58]  T. Barbui,et al.  Prospective identification of high-risk polycythemia vera patients based on JAK2V617F allele burden , 2007, Leukemia.

[59]  A. Tefferi,et al.  Prevalence and clinicopathologic correlates of JAK2 exon 12 mutations in JAK2V617F-negative polycythemia vera , 2007, Leukemia.

[60]  A. Tefferi,et al.  Clinical correlates of JAK2V617F allele burden in essential thrombocythemia , 2007, Cancer.

[61]  T. Barbui,et al.  Leukocytosis as a major thrombotic risk factor in patients with polycythemia vera. , 2007, Blood.

[62]  M. Stratton,et al.  JAK2 exon 12 mutations in polycythemia vera and idiopathic erythrocytosis. , 2007, The New England journal of medicine.

[63]  T. Barbui,et al.  The haematocrit and platelet target in polycythemia vera , 2007, British journal of haematology.

[64]  P. Campbell,et al.  Progenitors homozygous for the V617F mutation occur in most patients with polycythemia vera, but not essential thrombocythemia. , 2006, Blood.

[65]  J. D. van der Walt,et al.  Hydroxyurea compared with anagrelide in high-risk essential thrombocythemia. , 2005, The New England journal of medicine.

[66]  Mario Cazzola,et al.  A gain-of-function mutation of JAK2 in myeloproliferative disorders. , 2005, The New England journal of medicine.

[67]  Stefan N. Constantinescu,et al.  A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera , 2005, Nature.

[68]  T. Barbui,et al.  Vascular and neoplastic risk in a large cohort of patients with polycythemia vera. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[69]  T. Barbui,et al.  Acute leukemia in polycythemia vera: an analysis of 1638 patients enrolled in a prospective observational study. , 2005, Blood.

[70]  Sandra A. Moore,et al.  Activating mutation in the tyrosine kinase JAK2 in polycythemia vera, essential thrombocythemia, and myeloid metaplasia with myelofibrosis. , 2005, Cancer cell.

[71]  P. Campbell,et al.  Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders , 2005, The Lancet.

[72]  M. Cazzola,et al.  Life expectancy and prognostic factors for survival in patients with polycythemia vera and essential thrombocythemia. , 2004, The American journal of medicine.

[73]  T. Barbui,et al.  Efficacy and safety of low-dose aspirin in polycythemia vera. , 2004, The New England journal of medicine.

[74]  Francesca Bray,et al.  The Evidence-Based Primary Care Handbook , 2000, BMJ : British Medical Journal.

[75]  Gruppo Italiano Studio Policitemia Polycythemia Vera: The Natural History of 1213 Patients Followed for 20 Years , 1995, Annals of Internal Medicine.

[76]  T. Barbui,et al.  Hydroxyurea for patients with essential thrombocythemia and a high risk of thrombosis. , 1995, The New England journal of medicine.

[77]  J. Goldberg,et al.  Therapeutic recommendations in polycythemia vera based on Polycythemia Vera Study Group protocols. , 1986, Seminars in hematology.

[78]  Fortuin Nj,et al.  Non-hematologic effects of chronic iron deficiency. A study of patients with polycythemia vera treated solely with venesections. , 1982 .

[79]  N. Fortuin,et al.  Non‐Hematologic Effects of Chronic Iron Deficiency: A STUDY OF PATIENTS WITH POLYCYTHEMIA VERA TREATED SOLELY WITH VENESECTIONS , 1982, Medicine.

[80]  J. Goldberg,et al.  Increased incidence of acute leukemia in polycythemia vera associated with chlorambucil therapy. , 1981, The New England journal of medicine.

[81]  Ledlie Em Polycythæmia , 1966 .

[82]  R. Gibbs,et al.  Whole-exome sequencing of polycythemia vera revealed novel driver genes and somatic mutation shared by T cells and granulocytes , 2014, Leukemia.

[83]  A. Green,et al.  A Polycythemia Vera Updated: Diagnosis, Pathobiology, and Treatment. , 2000, Hematology. American Society of Hematology. Education Program.

[84]  栗山 茂久 The expressiveness of the body and the divergence of Greek and Chinese medicine , 1999 .

[85]  Berlin Ni Prologue: polycythemia vera. The closing of the Wasserman-Polycythemia Vera Study Group era. , 1997 .

[86]  L. Wasserman,et al.  From efficacy to safety: a Polycythemia Vera Study group report on hydroxyurea in patients with polycythemia vera. , 1997, Seminars in hematology.

[87]  N. Berlin Prologue: polycythemia vera. The closing of the Wasserman-Polycythemia Vera Study Group era. , 1997, Seminars in hematology.

[88]  Polycythemia vera: the natural history of 1213 patients followed for 20 years. Gruppo Italiano Studio Policitemia. , 1995, Annals of internal medicine.

[89]  E. M. Ledlie Treatment of polycythaemia by 32-P. , 1966, Proceedings of the Royal Society of Medicine.