Thrombosis in myeloproliferative disorders: Pathogenetic facts and speculation

Leukemia

Volumn 22, Issue 11, 2008, Pages 2020-2028

  Landolfi, R ^a,b   Di Gennaro, L ^a   Falanga, A ^c  

^a CATHOLIC UNIVERSITY   (Italy)

^b OASI RESEARCH INSTITUTE IRCCS   (Italy)

^c OSPEDALI RIUNITI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; ANAGRELIDE; ANTICOAGULANT AGENT; ANTITHROMBOCYTIC AGENT; ANTIVITAMIN K; BLOOD CLOTTING FACTOR 5 LEIDEN; CLOPIDOGREL; HEPARIN; HYDROXYUREA; JANUS KINASE 2; LOW MOLECULAR WEIGHT HEPARIN; PLACEBO; TICLOPIDINE;

ARTERY THROMBOSIS; CLINICAL TRIAL; DEEP VEIN THROMBOSIS; DRUG EFFICACY; ERYTHROCYTOSIS; GENE MUTATION; HUMAN; LEUKOCYTE COUNT; LOW DRUG DOSE; MICROANGIOPATHY; MYELOPROLIFERATIVE DISORDER; NEUTROPHIL; PATHOGENESIS; POLYCYTHEMIA VERA; PRIORITY JOURNAL; REVIEW; THROMBOCYTE ANOMALY; THROMBOCYTHEMIA; THROMBOCYTOSIS; THROMBOPHILIA; THROMBOSIS; VEIN THROMBOSIS; VENOUS THROMBOEMBOLISM;

EID: 56249099333     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2008.253     Document Type: Review

References (96)

1. Carobbio A, Antonioli E, Guglielmelli P, Vannucchi AM, Delaini F, Guerini V et al. Leukocytosis and risk stratification assessment in essential thrombocythemia. J Clin Oncol 2008; 26: 2732-2736.
2. Landolfi R, Di Gennaro L, Barbui T, De Stefano V, Finazzi G, Marfisi R et al. Leukocytosis as a major thrombotic risk factor in patients with Polycythemia Vera. Blood 2007; 109: 2446-2452.
3. Falanga A, Marchetti M, Evangelista V, Vignoli A, Licini M, Balicco M et al. Polymorphonuclear leukocyte activation and hemostasis in patients with essential thrombocythemia and polycythemia vera. Blood 2000; 96: 4261-4266.
4. Falanga A, Marchetti M, Vignoli A, Balducci D, Barbui T. Leukocyte-platelet interaction in patients with essential thrombocythemia and polycythemia vera. Exp Hematol 2005; 33: 523-530.
5. Landolfi R, Marchioli R, Kutti J, Gisslinger H, Tognoni G, Patrono C et al. Efficacy and safety of low dose aspirin in polycythemia vera. N Engl J Med 2004; 350: 114-124.
6. Harrison CN, Campbell PJ, Buck G, Wheatley K, East CL, Bareford D et al. United Kingdom Medical Research Council Primary Thrombocythemia 1 Study. Hydroxyurea compared with anagrelide in high-risk essential thrombocythemia. N Engl J Med 2005; 353: 33-45.
7. Baxter EJ, Scott LM, Campbell PJ, East C, Fourouclas N, Swanton S et al. Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders. Lancet 2005; 365: 1054-1061.
8. James C, Ugo V, Le Couedic JP, Staerk J, Delhommeau F, Lacout C et al A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature 2005; 434: 1144-1148.
9. Michiels JJ, Berneman Z, Bockstaele DV, van der Planken M, De Raeve H, Schroyens W. Clinical and laboratory features, pathology of platelet-mediated thrombosis and bleeding complications and the molecular etiology of essential thrombocythemia and polycythemia vera: therapeutic implications. Semin Thromb Hemost 2006; 32: 174-207.
10. Michiels JJ, Abels J, Steketee J, Van Vliet HH, Vuzevski VD. Erythromelalgia caused by platelet-mediated arteriolar inflammation and thrombosis in thrombocythemia. Ann Intern Med 1985; 102: 466-471.
11. Kurzrock R, Cohen PR. Erythromelalgia: Review of clinical characteristics and pathophysiology. Am J Med 1991; 91: 416-422.
12. Zucker S, Mielke CH. Classification of thrombocytosis based on platelet function test: Correlation with hemorrhagic and thrombotic complications. J Lab Clin Med 1972; 80: 385-394.
13. Michiels JJ, Koudstaal P, Mulder A, Van Vliet HH. Transient neurological and ocular manifestations in primary thrombocythemia. Neurology 1993; 43: 1107-1110.
14. Gruppo Italiano Studio Policitemia. Polycythemia vera: The natural history of 1213 patients followed for 20 years. Ann Intern Med 1995; 123: 656-664.
15. Passamonti F, Brusamolino E, Lazzarino M, Baraté C, Klersy C, Orlandi E et al. Efficacy of pipobroman in the treatment of polycythemia vera: Long-term results in 163 patients. Haematologica 2000; 85 1011-1018.
16. Marchioli R, Finazzi G, Landolfi R, Kutti J, Gisslinger H, Patrono C et al. Vascular and neoplastic risk in a large cohort of patients with polycythemia vera. J Clin Oncol 2005; 23: 2224-2232.
17. Gangat N, Strand J, Li CY, Wu W, Pardanani A, Tefferi A. Leucocytosis in polycythaemia vera predicts both inferior survival and leukaemic transformation. Br J Haematol 2007; 138: 354-358.
18. Chim CS, Kwong YL, Lie AK, Ma SK, Chan CC, Wong LG et al. Long-term outcome of 231 patients with essential thrombocythemia: prognostic factors for thrombosis, bleeding, myelofibrosis, and leukemia. Arch Intern Med 2005; 165: 2651-2658.
19. Besses C, Cervantes F, Pereira A, Florensa L, Sole F, Hernandez- Boluda JC et al. Major vascular complications in essential thrombocythemia: A study of the predictive factors in a series of 148 patients. Leukemia 1999; 13: 150-154.
20. Wolanskyj AP, Schwager SM, McClure RF, Larson DR, Tefferi A. Essential thrombocythemia beyond the first decade: Life expectancy, long-term complication rates, and prognostic factors. Mayo Clin Proc 2006; 81: 159-166.
21. Jensen MK, de Nelly Brown P, Nielsen OJ, Hasselbalch HC. Incidence, clinical features and outcome of essential thrombocythaemia in well defined geographical area. Eur J Hematol 2000; 65: 132-139.
22. Campbell PJ, Scott LM, Buck G, Wheatley K, East CL, Marsden JT et al Definition of subtypes of essential thrombocythaemia and relation to polycythaemia vera based on JAK2 V617F mutation status: A prospective study. Lancet 2005; 366: 1945-1953.
23. Carobbio A, Finazzi G, Guerini V, Spinelli O, Delaini F, Marchioli R et al. Leukocytosis is a risk factor for thrombosis in essential thrombocythemia: Interaction with treatment, standard risk factors and Jak2 mutation status. Blood 2007; 109: 2310-2313.
24. Rossi C, Randi ML, Zerbinati P, Rinaldi V, Girolami A. Acute coronary disease in essential thrombocythemia and polycythemia vera. J Intern Med 1998; 244: 49-53.
25. De Stefano V, Za T, Rossi E, Vannucchi AM, Ruggeri M, Elli E et al Recurrent thrombosis in patients with polycythemia vera and essential thrombocythemia: Incidence, risk factors, and effect of treatments. Haematologica 2008; 93: 372-380.
26. Reisner SA, Rinkevich D, Markiewicz W, Tatarsky I, Brenner B. Cardiac involvement in patients with myeloproliferative disorders. Am J Med 1992; 93: 498-504.
27. Najean Y, Mugnier P, Dresch C, Rain JD. Polycythaemia vera in young people: An analysis of 58 cases diagnosed before 40 years. Br J Haematol 1987; 67: 285-291.
28. Perea G, Remacha A, Besses C, Jimenez M, Florensa L, Cervantes F. Is polycythemia vera a serious disease in young adults? Haematologica 2001; 86: 543-544.
29. Chait Y, Condat B, Casalz-Hatem D, Rufat P, Atmani S, Chaoui D et al Relevance of the criteria commonly used to diagnose myeloproliferative disorder in patients with splanchnic thrombosis. Br J Haematol 2005; 129: 553-560.
30. Briere JB. Budd-Chiari Sindrome and Portal Vein Thrombosis associated with Myeloproliferative disorders: Diagnosis and management. Semin Thromb Haemost 2006; 32: 208-218.
31. Primignani M, Barosi G, Bergamaschi G, Gianelli U, Fabris F, Reati R et al. Role of the JAK2 mutation in the diagnosis of chronic myeloproliferative disorders in splanchnic vein thrombosis. Hepatology 2006; 44: 1528-1534.
32. Patel RK, Lea NC, Heneghan MA, Westwood NB, Milojkovic D, Thanigaikumar M et al. Prevalence of the activating JAK2 tyrosine kinase mutation V617F in the Budd-Chiari syndrome. Gastroenterology 2006; 130: 2031-2038.
33. Pearson TC, Wetherley-Mein G. Vascular occlusive episodes and venous haematocrit in primary proliferative polycythemia. Lancet 1978; 2: 1219-1222.
34. Kwaan HC, Wang J. Hyperviscosity in polycythemia vera and other red cell abnormalities. Semin Thromb Hemost 2003; 29: 451-458.
35. Turitto VT, Weiss HJ. Platelet and red cell involvement in mural thrombogenesis. Ann NY Acad Sci 1983; 416: 363-376.
36. Huang PY, Hellums JD. Aggregation and disaggregation kinetics of human blood platelets: The disaggregation under shear stress of platelet aggregates. Biophys J 1993; 65: 354-361.
37. Landolfi R, Ciabattoni G, Patrignani P, Castellana MA, Pogliani E, Bizzi B et al. Increased thromboxane biosynthesis in patients with polycythemia vera: Evidence for aspirin-suppressible platelet activation in vivo. Blood 1992; 80: 1965-1971.
38. Schafer AI. Molecular basis of the diagnosis and treatment of polycythemia vera and essential thrombocythemia. Blood 2006; 107: 4214-4222.
39. Turitto VT, Weiss HJ. Red blood cells: Their dual role in thrombus formation. Science 1980; 207: 541-543.
40. Yedgar S, Koshkaryev A, Barshtein G. The red blood cell in vascular occlusion. Pathophysiol Haemost Thromb 2002; 32: 263-268.
41. Pearson MJ, Lipowsky HH. Influence of erythrocyte aggregation on leukocyte margination in postcapillary venules of rat mesentery. Am J Physiol Heart Circ Physiol 2000; 279: 1460-1471.
42. Wautier MP, EI Nemer W, Gane P, Rain JD, Cartron JP, Colin Y et al Increased adhesion to endothelial cells of erythrocytes from patients with polycythemia vera is mediated by laminin alpha5 chain and Lu/BCAM. Blood 2007; 110: 894-901.
43. Cortelazzo S, Finazzi G, Ruggeri M, Vestri O, Galli M, Rodeghiero F et al. Hydroxyurea for patients with essential thrombocythemia and a high risk of thrombosis. N Engl J Med 1995; 332: 1132-1136.
44. Buss DH, Stuart JJ, Lipscomb GE. The incidence of thrombotic and hemorrhagic disorders in association with extreme thrombocytosis: An analysis of 129 cases. Am J Hematol 1985; 20: 365-372.
45. Landolfi R, Cipriani MC, Novarese L. Thrombosis and bleeding in polycythemia vera and essential thrombocythemia: Pathogenetic mechanisms and prevention. Best Pract Res Clin Haematol 2006; 19: 617-633.
46. Landolfi R, Rocca B, Patrono C. Bleeding and thrombosis in myeloproliferative disorders: Mechanism and treatment. Crit Rev Oncol hematol 1995; 20: 203-222.
47. Elliott MA, Tefferi A. Thrombosis and haemorrage in polycythemia vera and essential thrombocythemia. Br J Haematol 2004; 128: 275-290.
48. Baker RI, Manoharan A. Platelet function in myeloproliferative disorders: Characterization and sequential studies show multiple platelet abnormalities, and change with time. Eur J Haematol 1988; 95: 82-86.
49. Wu KK. Platelet hyperaggregability and thrombosis in patients with thrombocythemia. Ann Intern Med 1978; 88: 7-11.
50. Valles J, Santos MT, Aznar J, Martinez M, Moscardo A, Pinon M et al Platelet-erythrocyte interactions enhance alpha (IIb)beta(3) integrin receptor activation and P-selectin expression during platelet recruitment: Down-regulation by aspirin ex vivo. Blood 2002; 99 3978-3984.
51. Jensen MK, de Nully Brown P, Lund BV, Nielsen O, Hasselbalch HC. Increased platelet activation and abnormal membrane glycoprotein content and redistribution in myeloproliferative disorders. Br J Haematol 2000; 110: 116-124.
52. Murphy S, Davis JL, Walsh PN, Gardner FH. Template bleeding time and clinical hemorrhage in myeloproliferative disease. Arch Intern Med 1978; 138: 1251-1253.
53. Alvarez-Larrán A, Cervantes F, Bellosillo B, Giralt M, Juliá A, Hernández-Boluda JC et al. Essential thrombocythemia in young individuals: Frequency and risk factors for vascular events and evolution to myelofibrosis in 126 patients. Leukemia 2007; 21 1218-1223.
54. Falanga A, Marchetti M, Barbui T, Smith CW. Pathogenesis of thrombosis in essential thrombocythemia and polycythemia vera: The role of neutrophils. Semin Hematol 2005; 42: 239-247.
55. Afshar-Kharghan V, Thiagarajan P. Leukocyte adhesion and thrombosis. Curr Opin Hematol 2006; 13: 34-39.
56. de Gaetano G, Cerletti C, Evangelista V. Recent advances in plateletpolymorphonuclear leukocyte interaction. Haemostasis 1999; 29: 41-49.
57. Celi A, Pellegrini G, Lorenzet R, De Blasi A, Ready N, Furie BC et al P-selectin induces the expression of tissue factor on monocytes. Proc Natl Acad Sci USA 1994; 91: 8767-8771.
58. Li N, Goodall AH, Hjemdahl P. A sensitive flow cytometric assay for circulating platelet-leukocyte aggregates. Br J Haematol 1997; 99: 808-816.
59. Ott I, Neumann FJ, Gawaz M, Schmitt M, Schömig A. Increased neutrophil-platelet adhesion in patients with unstable angina. Circulation 1996; 94: 1239-1246.
60. Rosendaal FR. Risk factors for venous thrombosis: Prevalence, risk, and interaction. Semin Hematol 1997; 34: 171-187.
61. Cortelazzo S, Viero P, Finazzi G, D'Emilio A, Rodeghiero F, Barbui T. Incidence and risk factors for thrombotic complications in a historical cohort of 100 patients with essential thrombocythemia. J Clin Oncol 1990; 8: 556-562.
62. De Stefano V, Za T, Rossi E, Vannucchi AM, Ruggeri M, Elli E et al Recurrent thrombosis in patients with polycythemia vera or essential thrombocythemia: Efficacy of treatment in preventing re-thrombosis in different clinical settings. Blood 2006; 108: 119a.
63. Jantunen R, Juvonen E, Ikkala E, Oksanen K, Anttila P, Ruutu T. The predictive value of vascular risk factors and gender for the development of thrombotic complications in essential thrombocythemia. Ann Hematol 2001; 80: 74-78.
64. Gangat N, Wolanskyj AP, McClure RF, Li CY, Schwager S, Wu W et al. Risk stratification for survival and leukemic transformation in essential thrombocythemia: A single institutional study of 605 patients. Leukemia 2007; 21: 271-276.
65. Tefferi A, Gangat N, Wolanskyj A. The interaction between leukocytosis and other risk factors for thrombosis in essential thrombocythemia. Blood 2007; 109: 4105.
66. Afshar-Kharghan VLA, Gray L, Padilla A, Borthakur G, Roberts S, Pruthi R et al. Hemostatic gene polymorphisms and the prevalence of thrombohemorrhagic complications in polycythemia vera and essential thrombocythemia. Blood 2001; 98: 471a.
67. Dicato MA, Schroell B, Berchem GJ. V Leiden mutations, prothrombin and methylene-tetrahydrofolate reductase are not risk factors for thromboembolic disease in essential thrombocythemia. Blood 1999; 94: 111a.
68. Ruggeri M, Gisslinger H, Tosetto A, Rintelen C, Mannhalter C, Pabinger I et al. Factor V Leiden mutation carriership and venous thromboembolism in polycythemia vera and essential thrombocythemia. Am J Hematol 2002; 71: 1-6.
69. Gisslinger H, Rodeghiero F, Ruggeri M, Heis-Vahidi Fard N, Mannhalter C, Papagiannopoulos M et al. Homocysteine levels in polycythaemia vera and essential thrombocythaemia. Br J Haematol 1999; 105 551-555.
70. Faurschou M, Nielsen OJ, Jensen MK, Hasselbalch HC. High prevalence of hyperhomocysteinemia due to marginal deficiency of cobalamin or folate in chronic myeloproliferative disorders. Am J Hematol 2000; 65 136-140.
71. Amitrano L, Guardascione MA, Ames PR, Margaglione M, Antinolfi I, Iannaccone L et al. Thrombophilic genotypes, natural anticoagulants, and plasma homocysteine in myeloproliferative disorders: relationship with splanchnic vein thrombosis and arterial disease. Am J Hematol 2003; 72: 75-81.
72. Gisslinger H, Rodeghiero F, Ruggeri M, Heis-Vahidi Fard N, Mannhalter C, Papagiannopoulos M et al. Homocysteine levels in polycythaemia vera and essential thrombocythaemia. Br J Haematol 1999; 105 551-555.
73. Kornblihtt LI, Heller PG, Correa G, Castañón M, Genoud V, Vassallu P et al. Associated thrombophilic defects in essential thrombocythaemia: Their relationship with clinical manifestations. Thromb Res 2003; 112: 131-135.
74. Robertson B, Urquhart C, Ford I, Townend J, Watson HG, Vickers MA et al. Platelet and coagulation activation markers in myeloproliferative diseases: Relationships with JAK2 V617 F status, clonality, and antiphospholipid antibodies. J Thromb Haemost 2007; 5: 1679-1685.
75. Landolfi R, Di Gennaro L. Prevention of thrombosis in polycythemia vera and essential thrombocythemia. Haematologica 2008; 93: 331-335.
76. Maugeri N, Giordano G, Petrilli MP, Fraticelli V, de Gaetano G, Cerletti C et al. Inhibition of tissue factor expression by hydroxyurea in polymorphonuclear leukocytes from patients with myeloproliferative disorders: A new effect for an old drug? J Thromb Haemost 2006; 4: 2593-2598.
77. Patrono C, Baigent C, Hirsh J, Roth G. Antiplatelet drugs: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines. Chest 2008; 133: 199S-233S.
78. Patrono C, García Rodríguez LA, Landolfi R, Baigent C. Low-dose aspirin for the prevention of atherothrombosis. N Engl J Med 2005; 353: 2373-2383.
79. van Genderen PJ, Mulder PG, Waleboer M, van de Moesdijk D, Michiels JJ. Prevention and treatment of thrombotic complications in essential thrombocythaemia: Efficacy and safety of aspirin. Br J Haematol 1997; 97: 179-184.
80. Ruggeri M, Rodeghiero F, Tosetto A, Castaman G, Scognamiglio F, Finazzi G et al. Postsurgery outcomes in patients with polycythemia vera and essential thrombocythemia: A retrospective survey. Blood 2008; 111: 666-671.
81. Hirsh J, Guyatt G, Albers GW, Harrington G, Schünemann HJ. Antithrombotic and thrombolytic therapy: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines (8th Edition). Chest 2008; 133 Suppl: 110-112.
82. Gayoso JM. 5-year incidence of thrombocytosis and the effect on heparin dose response and heparin requirements. J Extra Corpor Technol 1999; 31: 184-190.
83. Cazzola M, Skoda R. Gain of function, loss of control - a molecular basis for chronic myeloproliferative disorders. Haematologica 2005; 90: 871-874.
84. Levine RL, Pardanani A, Tefferi A, Gilliland DG. Role of JAK2 in the pathogenesis and therapy of myeloproliferative disorders. Nat Rev Cancer 2007; 7: 673-683.
85. Colaizzo D, Amitrano L, Tiscia GL, Scenna G, Grandone E, Guardascione MA et al. The JAK2 V617F mutation frequently occurs in patients with portal and mesenteric venous thrombosis. J Thromb Haemost 2007; 5: 55-61.
86. Boissinot M, Lippert E, Girodon F, Dobo I, Fouassier M, Masliah C et al. Latent myeloproliferative disorder revealed by the JAK2-V617F mutation and endogenous megakaryocytic colonies in patients with splanchnic vein thrombosis. Blood 2006; 108: 3223-3224.
87. Primignani M, Barosi G, Bergamaschi G, Gianelli U, Fabris F, Reati R et al. Role of the JAK2 mutation in the diagnosis of chronic myeloproliferative disorders in splanchnic vein thrombosis. Hepatology 2006; 44: 1528-1534.
88. Patel RK, Lea NC, Heneghan MA, Westwood NB, Milojkovic D, Thanigaikumar M et al. Prevalence of the activating JAK2 tyrosine kinase mutation V617F in the Budd-Chiari syndrome. Gastroenterology 2006; 130: 2031-2038.
89. De Stefano V, Fiorini A, Rossi E, Za T, Farina G, Chiusolo P. Prevalence of the JAK2 V617F mutation among patients with splanchnic or cerebral venous thrombosis and without overt myeloproliferative disorders. J Thromb Haemost 2007; 5: 708-714.
90. Kiladjian JJ, Cervantes F, Leebeek FW, Marzac C, Cassinat B, Chevret S et al. The impact of JAK2 and MPL mutations on diagnosis and prognosis of splanchnic vein thrombosis. A report on 241 cases. Blood 2008; 111: 4922-4929.
91. Pardanani A, Lasho TL, Hussein K, Schwager SM, Finke CM, Pruthi RK et al. JAK2V617F mutation screening as part of the hypercoagulable work-up in the absence of splanchnic venous thrombosis or overt myeloproliferative neoplasm: Assessment of value in a series of 664 consecutive patients. Mayo Clin Proc 2008; 83: 457-459.
92. Arellano-Rodrigo E, Alvarez-Larran A, Reverter JC, Villamor N, Colomer D, Cervantes F. Increased platelet and leukocyte activation as contributing mechanisms for thrombosis in essential thrombocythemia and correlation with the JAK2 mutational status. Haematologica 2006; 91: 169-175.
93. Falanga A, Marchetti M, Vignoli A, Balducci D, Russo L, Guerini V et al. V617F JAK-2 mutation in patients with essential thrombocythemia: relation to platelet, granulocyte, and plasma hemostatic and inflammatory molecules. Exp Hematol 2007; 35: 702-711.
94. Muller I, Klocke A, Alex M, Kotzsch M, Luther T, Morgenstern E et al Intravascular tissue factor initiates coagulation via circulating microvesicles and platelets. FASEB J 2003; 17: 476-478.
95. Falati S, Liu Q, Gross P, Merrill-Skoloff G, Chou J, Vandendries E et al. Accumulation of tissue factor into developing thrombi in vivo is dependent upon microparticle P-selectin glycoprotein ligand 1 and platelet P-selectin. J Exp Med 2003; 197: 1585-1598.
96. Myers DD, Hawley AE, Farris DM, Wrobleski SK, Thanaporn P, Schaub RG et al. P-selectin and leukocyte microparticles are associated with venous thrombogenesis. J Vasc Surg 2003; 38: 1075-1089.