Skip to main content
Top
Published in: International Journal of Hematology 1/2021

01-01-2021 | Disseminated Intravascular Coagulation | Progress in Hematology

Advances in the diagnosis and treatment of disseminated intravascular coagulation in haematological malignancies

Author: Takayuki Ikezoe

Published in: International Journal of Hematology | Issue 1/2021

Login to get access

Abstract

Haematological malignancies, including acute leukaemia and non-Hodgkin lymphoma, are one of the underlying diseases that frequently cause disseminated intravascular coagulation (DIC), an acquired thrombotic disorder. Concomitant DIC is associated with the severity of the underlying disease and poor prognosis. The Japanese Society on Thrombosis and Hemostasis released the new DIC diagnostic criteria in 2017. This criteria include coagulation markers such as soluble fibrin and the thrombin-antithrombin complex to more accurately evaluate the hypercoagulable state in patients. Among several groups of anticoagulants available, recombinant human soluble thrombomodulin is most frequently used to treat DIC caused by haematological malignancies in Japan. DIC is remitted in parallel with the improvement of the underlying haematological diseases; thus, there is room for debate regarding whether the treatment of DIC would improve the prognosis of patients. Haematopoietic stem cell transplantation as well as the recently introduced chimeric antigen receptor (CAR)-T-cell therapy are innovative therapies to produce a cure in a subset of patients with haematological malignancies. However, coagulopathy frequently occurs after these therapies, which limits the success of the treatment. For example, DIC is noted in approximately 50% of patients after CAT-T-cell therapy in conjunction with cytokine release syndrome. Hematopoietic stem cell transplantation (HSCT) causes endotheliitis, which triggers coagulopathy and the development of potentially lethal complications, such as sinusoidal obstruction syndrome/veno-occlusive disease and transplant-associated thrombotic microangiopathy. This review article describes the pathogenesis, clinical manifestation, diagnosis, and treatment of DIC caused by haematological malignancies, CAR-T-cell therapy, and HSCT.
Literature
1.
go back to reference Okajima K, Sakamoto Y, Uchiba M. Heterogeneity in the incidence and clinical manifestations of disseminated intravascular coagulation: a study of 204 cases. Am J Hematol. 2000;65(3):215–22.PubMed Okajima K, Sakamoto Y, Uchiba M. Heterogeneity in the incidence and clinical manifestations of disseminated intravascular coagulation: a study of 204 cases. Am J Hematol. 2000;65(3):215–22.PubMed
2.
go back to reference Singh B, Hanson AC, Alhurani R, Wang S, Herasevich V, Cartin-Ceba R, et al. Trends in the incidence and outcomes of disseminated intravascular coagulation in critically ill patients (2004-2010): a population-based study. Chest. 2013;143(5):1235–42.PubMed Singh B, Hanson AC, Alhurani R, Wang S, Herasevich V, Cartin-Ceba R, et al. Trends in the incidence and outcomes of disseminated intravascular coagulation in critically ill patients (2004-2010): a population-based study. Chest. 2013;143(5):1235–42.PubMed
3.
go back to reference Ikezoe T. Pathogenesis of disseminated intravascular coagulation in patients with acute promyelocytic leukemia, and its treatment using recombinant human soluble thrombomodulin. Int J Hematol. 2014;100(1):27–37.PubMed Ikezoe T. Pathogenesis of disseminated intravascular coagulation in patients with acute promyelocytic leukemia, and its treatment using recombinant human soluble thrombomodulin. Int J Hematol. 2014;100(1):27–37.PubMed
4.
go back to reference Uchiumi H, Matsushima T, Yamane A, Doki N, Irisawa H, Saitoh T, et al. Prevalence and clinical characteristics of acute myeloid leukemia associated with disseminated intravascular coagulation. Int J Hematol. 2007;86(2):137–42.PubMed Uchiumi H, Matsushima T, Yamane A, Doki N, Irisawa H, Saitoh T, et al. Prevalence and clinical characteristics of acute myeloid leukemia associated with disseminated intravascular coagulation. Int J Hematol. 2007;86(2):137–42.PubMed
5.
go back to reference Chi S, Ikezoe T. Disseminated intravascular coagulation in non-Hodgkin lymphoma. Int J Hematol. 2015;102(4):413–9.PubMed Chi S, Ikezoe T. Disseminated intravascular coagulation in non-Hodgkin lymphoma. Int J Hematol. 2015;102(4):413–9.PubMed
6.
go back to reference Carreras E, Diaz-Ricart M. The role of the endothelium in the short-term complications of hematopoietic SCT. Bone Marrow Transplant. 2011;46(12):1495–502.PubMed Carreras E, Diaz-Ricart M. The role of the endothelium in the short-term complications of hematopoietic SCT. Bone Marrow Transplant. 2011;46(12):1495–502.PubMed
7.
go back to reference Carreras E, Diaz-Ricart M. Early complications of endothelial origin. The EBMT handbook: hematopoietic stem cell transplantation and cellular therapies [Internet]. 7 Chapter 42. ed. Cham: Springer; 2019. p. 315–22. Carreras E, Diaz-Ricart M. Early complications of endothelial origin. The EBMT handbook: hematopoietic stem cell transplantation and cellular therapies [Internet]. 7 Chapter 42. ed. Cham: Springer; 2019. p. 315–22.
8.
go back to reference Falanga A, Iacoviello L, Evangelista V, Consonni R, Belotti D, D’Orazio A, et al. Loss of blast cell procoagulant activity and improvement of hemostatic variables in patients with acute promyelocytic leukemia given all-trans-retinoic acid. Blood. 1995;86:1072.PubMed Falanga A, Iacoviello L, Evangelista V, Consonni R, Belotti D, D’Orazio A, et al. Loss of blast cell procoagulant activity and improvement of hemostatic variables in patients with acute promyelocytic leukemia given all-trans-retinoic acid. Blood. 1995;86:1072.PubMed
9.
go back to reference Bauer KA, Rosenberg RD. Thrombin generation in acute promyelocytic leukemia. Blood. 1984;64:791.PubMed Bauer KA, Rosenberg RD. Thrombin generation in acute promyelocytic leukemia. Blood. 1984;64:791.PubMed
10.
go back to reference Mjers TJ, Rickles FR, Barb C, Cronlund M. Fibrinopeptide A in acute leukemia: relationship of activation of blood coagulation to disease activity. Blood. 1981;57:518. Mjers TJ, Rickles FR, Barb C, Cronlund M. Fibrinopeptide A in acute leukemia: relationship of activation of blood coagulation to disease activity. Blood. 1981;57:518.
11.
go back to reference Dicke C, Amirkhosravi A, Spath B, Jiménez-Alcázar M, Fuchs T, Davila M, Francis JL, Bokemeyer C, Langer F. Tissue factor-dependent and -independent pathways of systemic coagulation activation in acute myeloid leukemia: a single-center cohort study. Exp Hematol Oncol. 2015;6(4):22. Dicke C, Amirkhosravi A, Spath B, Jiménez-Alcázar M, Fuchs T, Davila M, Francis JL, Bokemeyer C, Langer F. Tissue factor-dependent and -independent pathways of systemic coagulation activation in acute myeloid leukemia: a single-center cohort study. Exp Hematol Oncol. 2015;6(4):22.
12.
go back to reference Sase T, Wada H, Yamaguchi M, Ogawa S, Kamikura Y, Nishikawa M, et al. Haemostatic abnormalities and thrombotic disorders in malignant lymphoma. Thromb Haemost. 2005;93(1):153–9.PubMed Sase T, Wada H, Yamaguchi M, Ogawa S, Kamikura Y, Nishikawa M, et al. Haemostatic abnormalities and thrombotic disorders in malignant lymphoma. Thromb Haemost. 2005;93(1):153–9.PubMed
13.
go back to reference Falanga A, Gordon SG. Isolation and characterization of cancer procoagulant: a cysteine proteinase from malignant tissue. Biochemistry. 1985;24:5558–67.PubMed Falanga A, Gordon SG. Isolation and characterization of cancer procoagulant: a cysteine proteinase from malignant tissue. Biochemistry. 1985;24:5558–67.PubMed
14.
go back to reference Falanga A, Alessio MG, Donati MB, Barbui T. A new procoagulant in acute leukemia. Blood. 1988;71:870–5.PubMed Falanga A, Alessio MG, Donati MB, Barbui T. A new procoagulant in acute leukemia. Blood. 1988;71:870–5.PubMed
15.
go back to reference Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, Che J, et al. HMG-1 as a late mediator of endotoxin lethality in mice. Science. 1999;285(5425):248–51.PubMed Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, Che J, et al. HMG-1 as a late mediator of endotoxin lethality in mice. Science. 1999;285(5425):248–51.PubMed
16.
go back to reference Ito T, Kawahara K, Nakamura T, Yamada S, Nakamura T, Abeyama K, et al. High-mobility group box 1 protein promotes development of microvascular thrombosis in rats. J Thromb Haemost. 2007;5(1):109–16.PubMed Ito T, Kawahara K, Nakamura T, Yamada S, Nakamura T, Abeyama K, et al. High-mobility group box 1 protein promotes development of microvascular thrombosis in rats. J Thromb Haemost. 2007;5(1):109–16.PubMed
17.
go back to reference Fuchs TA, Brill A, Duerschmied D, Schatzberg D, Monestier M, Myers DD Jr, et al. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci USA. 2010;107(36):15880–5.PubMed Fuchs TA, Brill A, Duerschmied D, Schatzberg D, Monestier M, Myers DD Jr, et al. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci USA. 2010;107(36):15880–5.PubMed
18.
go back to reference Xu J, Zhang X, Pelayo R, Monestier M, Ammollo CT, Semeraro F, et al. Extracellular histones are major mediators of death in sepsis. Nat Med. 2009;15(11):1318–21.PubMedPubMedCentral Xu J, Zhang X, Pelayo R, Monestier M, Ammollo CT, Semeraro F, et al. Extracellular histones are major mediators of death in sepsis. Nat Med. 2009;15(11):1318–21.PubMedPubMedCentral
19.
go back to reference McDonald B, Davis RP, Kim SJ, Tse M, Esmon CT, Kolaczkowska E, et al. Platelets and neutrophil extracellular traps collaborate to promote intravascular coagulation during sepsis in mice. Blood. 2017;129(10):1357–67.PubMedPubMedCentral McDonald B, Davis RP, Kim SJ, Tse M, Esmon CT, Kolaczkowska E, et al. Platelets and neutrophil extracellular traps collaborate to promote intravascular coagulation during sepsis in mice. Blood. 2017;129(10):1357–67.PubMedPubMedCentral
20.
go back to reference Nakahara M, Ito T, Kawahara K, Yamamoto M, Nagasato T, Shrestha B, et al. Recombinant thrombomodulin protects mice against histone-induced lethal thromboembolism. PLoS One. 2013;8(9):e75961.PubMedPubMedCentral Nakahara M, Ito T, Kawahara K, Yamamoto M, Nagasato T, Shrestha B, et al. Recombinant thrombomodulin protects mice against histone-induced lethal thromboembolism. PLoS One. 2013;8(9):e75961.PubMedPubMedCentral
21.
go back to reference Semeraro F, Ammollo CT, Morrissey JH, Dale GL, Friese P, Esmon NL, et al. Extracellular histones promote thrombin generation through platelet-dependent mechanisms: involvement of platelet TLR2 and TLR4. Blood. 2011;118(7):1952–61.PubMedPubMedCentral Semeraro F, Ammollo CT, Morrissey JH, Dale GL, Friese P, Esmon NL, et al. Extracellular histones promote thrombin generation through platelet-dependent mechanisms: involvement of platelet TLR2 and TLR4. Blood. 2011;118(7):1952–61.PubMedPubMedCentral
22.
go back to reference Harada-Shirado K, Wang X, Mori H, Fukatsu M, Takahashi H, Shichishima-Nakamura A, et al. Circulating intranuclear proteins may play a role in development of disseminated intravascular coagulation in individuals with acute leukemia. Int J Hematol. 2020;111(3):378–87.PubMed Harada-Shirado K, Wang X, Mori H, Fukatsu M, Takahashi H, Shichishima-Nakamura A, et al. Circulating intranuclear proteins may play a role in development of disseminated intravascular coagulation in individuals with acute leukemia. Int J Hematol. 2020;111(3):378–87.PubMed
25.
go back to reference Huang D, Yang Y, Sun J, Dong X, Wang J, Liu H, et al. Annexin A2-S100A10 heterotetramer is upregulated by PML/RARα fusion protein and promotes plasminogen-dependent fibrinolysis and matrix invasion in acute promyelocytic leukemia. Front Med. 2017;11(3):410–22.PubMed Huang D, Yang Y, Sun J, Dong X, Wang J, Liu H, et al. Annexin A2-S100A10 heterotetramer is upregulated by PML/RARα fusion protein and promotes plasminogen-dependent fibrinolysis and matrix invasion in acute promyelocytic leukemia. Front Med. 2017;11(3):410–22.PubMed
26.
go back to reference Menell JS, Cesarman GM, Jacovina AT, McLaughlin MA, Lev EA, Hajjar KA. Annexin II and bleeding in acute promyelocytic leukemia. N Engl J Med. 1999;340(13):994–1004.PubMed Menell JS, Cesarman GM, Jacovina AT, McLaughlin MA, Lev EA, Hajjar KA. Annexin II and bleeding in acute promyelocytic leukemia. N Engl J Med. 1999;340(13):994–1004.PubMed
27.
go back to reference O’Connell PA, Madureira PA, Berman JN, Liwski RS, Waisman DM. Regulation of S100A10 by the PML-RAR-α oncoprotein. Blood. 2011;117(15):4095–105.PubMed O’Connell PA, Madureira PA, Berman JN, Liwski RS, Waisman DM. Regulation of S100A10 by the PML-RAR-α oncoprotein. Blood. 2011;117(15):4095–105.PubMed
28.
go back to reference Godier A, Hunt BJ. Plasminogen receptors and their role in the pathogenesis of inflammatory, autoimmune and malignant disease. J Thromb Haemost. 2013;11(1):26–34.PubMed Godier A, Hunt BJ. Plasminogen receptors and their role in the pathogenesis of inflammatory, autoimmune and malignant disease. J Thromb Haemost. 2013;11(1):26–34.PubMed
29.
go back to reference Tapiovaara H, Alitalo R, Stephens R, Myöhänen H, Ruutu T, Vaheri A. Abundant urokinase activity on the surface of mononuclear cells from blood and bone marrow of acute leukemia patients. Blood. 1993;82:914–9.PubMed Tapiovaara H, Alitalo R, Stephens R, Myöhänen H, Ruutu T, Vaheri A. Abundant urokinase activity on the surface of mononuclear cells from blood and bone marrow of acute leukemia patients. Blood. 1993;82:914–9.PubMed
30.
go back to reference Nadir Y, Katz T, Sarig G, Hoffman R, Oliven A, Rowe JM. Hemostatic balance on the surface of leukemic cells: the role of tissue factor and urokinase plasminogen activator receptor. Haematologica. 2005;90:1549–56.PubMed Nadir Y, Katz T, Sarig G, Hoffman R, Oliven A, Rowe JM. Hemostatic balance on the surface of leukemic cells: the role of tissue factor and urokinase plasminogen activator receptor. Haematologica. 2005;90:1549–56.PubMed
31.
go back to reference Niiya K, Ozawa T, Tsuzawa T, Ueshima S, Matsuo O, Sakuragawa N. Transcriptional regulation of urokinase-type plasminogen activator receptor by cyclic AMP in PL-21 human myeloid leukemia cells: comparison with the regulation by phorbol myristate acetate. Thromb Haemost. 1998;79(3):574–8.PubMed Niiya K, Ozawa T, Tsuzawa T, Ueshima S, Matsuo O, Sakuragawa N. Transcriptional regulation of urokinase-type plasminogen activator receptor by cyclic AMP in PL-21 human myeloid leukemia cells: comparison with the regulation by phorbol myristate acetate. Thromb Haemost. 1998;79(3):574–8.PubMed
32.
go back to reference Pluchart C, Poitevin G, Colinart-Thomas M, Guimard G, Audonnet S, et al. Vincristine induces procoagulant activity of the human lymphoblastic leukemia cell line Jurkat through the release of extracellular vesicles. J Thromb Thrombolysis. 2019;48(2):195–202.PubMed Pluchart C, Poitevin G, Colinart-Thomas M, Guimard G, Audonnet S, et al. Vincristine induces procoagulant activity of the human lymphoblastic leukemia cell line Jurkat through the release of extracellular vesicles. J Thromb Thrombolysis. 2019;48(2):195–202.PubMed
33.
go back to reference Kubota T, Andoh K, Sadakata H, Tanaka H, Kobayashi N. Tissue factor released from leukemic cells. Thromb Haemost. 1991;65(1):59–63.PubMed Kubota T, Andoh K, Sadakata H, Tanaka H, Kobayashi N. Tissue factor released from leukemic cells. Thromb Haemost. 1991;65(1):59–63.PubMed
34.
go back to reference Walsh J, Wheeler HR, Geczy CL. Modulation of tissue factor on human monocytes by cisplatin and adriamycin. Br J Haematol. 1992;81(4):480–8.PubMed Walsh J, Wheeler HR, Geczy CL. Modulation of tissue factor on human monocytes by cisplatin and adriamycin. Br J Haematol. 1992;81(4):480–8.PubMed
35.
go back to reference de la Serna J, Montesinos P, Vellenga E, Rayón C, Parody R, León A, et al. Causes and prognostic factors of remission induction failure in patients with acute promyelocytic leukemia treated with all-trans retinoic acid and idarubicin. Blood. 2008;111(7):3395–402.PubMed de la Serna J, Montesinos P, Vellenga E, Rayón C, Parody R, León A, et al. Causes and prognostic factors of remission induction failure in patients with acute promyelocytic leukemia treated with all-trans retinoic acid and idarubicin. Blood. 2008;111(7):3395–402.PubMed
36.
go back to reference Di Bona E, Avvisati G, Castaman G, Luce Vegna M, De Sanctis V, et al. Early haemorrhagic morbidity and mortality during remission induction with or without all-trans retinoic acid in acute promyelocytic leukaemia. Br J Haematol. 2000;108(4):689–95.PubMed Di Bona E, Avvisati G, Castaman G, Luce Vegna M, De Sanctis V, et al. Early haemorrhagic morbidity and mortality during remission induction with or without all-trans retinoic acid in acute promyelocytic leukaemia. Br J Haematol. 2000;108(4):689–95.PubMed
37.
go back to reference Kim H, Lee JH, Choi SJ, Lee JH, Seol M, Lee YS, Kim WK, Lee JS, Lee KH. Risk score model for fatal intracranial hemorrhage in acute leukemia. Leukemia. 2006;20(5):770–6.PubMed Kim H, Lee JH, Choi SJ, Lee JH, Seol M, Lee YS, Kim WK, Lee JS, Lee KH. Risk score model for fatal intracranial hemorrhage in acute leukemia. Leukemia. 2006;20(5):770–6.PubMed
38.
go back to reference Ichikawa K, Edahiro Y, Gotoh A, Iiduka K, Komatsu N, Koike M. Co-occurrence of hyperleukocytosis and elevated fibrin-fibrinogen degradation product levels is a risk factor for early intracranial hemorrhage in patients with de novo acute leukemia. Int J Hematol. 2016;104(5):612–20.PubMed Ichikawa K, Edahiro Y, Gotoh A, Iiduka K, Komatsu N, Koike M. Co-occurrence of hyperleukocytosis and elevated fibrin-fibrinogen degradation product levels is a risk factor for early intracranial hemorrhage in patients with de novo acute leukemia. Int J Hematol. 2016;104(5):612–20.PubMed
39.
go back to reference Breccia M, Avvisati G, Latagliata R, Carmosino I, Guarini A, De Propris MS, et al. Occurrence of thrombotic events in acute promyelocytic leukemia correlates with consistent immunophenotypic and molecular features. Leukemia. 2007;21:79–83.PubMed Breccia M, Avvisati G, Latagliata R, Carmosino I, Guarini A, De Propris MS, et al. Occurrence of thrombotic events in acute promyelocytic leukemia correlates with consistent immunophenotypic and molecular features. Leukemia. 2007;21:79–83.PubMed
40.
go back to reference Kojima S, Nishioka C, Chi S, Yokoyama A, Ikezoe T. In vitro studies on the role of recombinant human soluble thrombomodulin in the context of retinoic acid mediated APL differentiation syndrome. Leuk Res. 2017;63:1–9.PubMed Kojima S, Nishioka C, Chi S, Yokoyama A, Ikezoe T. In vitro studies on the role of recombinant human soluble thrombomodulin in the context of retinoic acid mediated APL differentiation syndrome. Leuk Res. 2017;63:1–9.PubMed
41.
go back to reference Hashimoto S, Koike T, Tatewaki W, Seki Y, Sato N, Azegami T, et al. Fatal thromboembolism in acute promyelocytic leukemia during all-trans retinoic acid therapy combined with antifibrinolytic therapy for prophylaxis of hemorrhage. Leukemia. 1994;8(7):1113–5.PubMed Hashimoto S, Koike T, Tatewaki W, Seki Y, Sato N, Azegami T, et al. Fatal thromboembolism in acute promyelocytic leukemia during all-trans retinoic acid therapy combined with antifibrinolytic therapy for prophylaxis of hemorrhage. Leukemia. 1994;8(7):1113–5.PubMed
42.
go back to reference Tsukada N, Wada K, Aoki S, Hashimoto S, Kishi K, Takahashi M, et al. Induction therapy with all-trans retinoic acid for acute promyelocytic leukemia: a clinical study of 10 cases, including a fatal [correction of fetal] case with thromboembolism. Intern Med. 1996;35(1):10–4.PubMed Tsukada N, Wada K, Aoki S, Hashimoto S, Kishi K, Takahashi M, et al. Induction therapy with all-trans retinoic acid for acute promyelocytic leukemia: a clinical study of 10 cases, including a fatal [correction of fetal] case with thromboembolism. Intern Med. 1996;35(1):10–4.PubMed
43.
go back to reference Asakura H, Takahashi H, Uchiyama T, Eguchi Y, Okamoto K, Kawasugi K, et al. Proposal for new diagnostic criteria for DIC from the Japanese Society on Thrombosis and Hemostasis. Thromb J. 2016;14:42.PubMedPubMedCentral Asakura H, Takahashi H, Uchiyama T, Eguchi Y, Okamoto K, Kawasugi K, et al. Proposal for new diagnostic criteria for DIC from the Japanese Society on Thrombosis and Hemostasis. Thromb J. 2016;14:42.PubMedPubMedCentral
44.
go back to reference Asakura H, Takahashi H, Tsuji H, Matsushita T, Ninomiya H, Honda G, et al. Post-marketing surveillance of thrombomodulin alfa, a novel treatment of disseminated intravascular coagulation—safety and efficacy in 1,032 patients with hematologic malignancy. Thromb Res. 2014;133(3):364–70.PubMed Asakura H, Takahashi H, Tsuji H, Matsushita T, Ninomiya H, Honda G, et al. Post-marketing surveillance of thrombomodulin alfa, a novel treatment of disseminated intravascular coagulation—safety and efficacy in 1,032 patients with hematologic malignancy. Thromb Res. 2014;133(3):364–70.PubMed
45.
go back to reference Osone S, Fukushima K, Yano M, Kakazu M, Sano H, Kato Y, et al. Supportive care for hemostatic complications associated with pediatric leukemia: a national survey in Japan. Int J Hematol. 2019;110(6):743–50.PubMed Osone S, Fukushima K, Yano M, Kakazu M, Sano H, Kato Y, et al. Supportive care for hemostatic complications associated with pediatric leukemia: a national survey in Japan. Int J Hematol. 2019;110(6):743–50.PubMed
46.
go back to reference Ikezoe T. Thrombomodulin/activated protein C system in septic disseminated intravascular coagulation. J Intensive Care. 2015;3(1):1.PubMedPubMedCentral Ikezoe T. Thrombomodulin/activated protein C system in septic disseminated intravascular coagulation. J Intensive Care. 2015;3(1):1.PubMedPubMedCentral
47.
go back to reference Mosnier LO, Meijers JC, Bouma BN. Regulation of fibrinolysis in plasma by TAFI and protein C is dependent on the concentration of thrombomodulin. Thromb Haemost. 2001;85:5–11.PubMed Mosnier LO, Meijers JC, Bouma BN. Regulation of fibrinolysis in plasma by TAFI and protein C is dependent on the concentration of thrombomodulin. Thromb Haemost. 2001;85:5–11.PubMed
48.
go back to reference Abeyama K, Stern DM, Ito Y, Kawahara K, Yoshimoto Y, Tanaka M, et al. The N-terminal domain of thrombomodulin sequesters high-mobility group-B1 protein, a novel antiinflammatory mechanism. J Clin Investig. 2005;115:1267–74.PubMed Abeyama K, Stern DM, Ito Y, Kawahara K, Yoshimoto Y, Tanaka M, et al. The N-terminal domain of thrombomodulin sequesters high-mobility group-B1 protein, a novel antiinflammatory mechanism. J Clin Investig. 2005;115:1267–74.PubMed
49.
go back to reference Pan B, Wang X, Nishioka C, Honda G, Yokoyama A, Zeng L, et al. G-protein coupled receptor 15 mediates angiogenesis and cytoprotective function of thrombomodulin. Sci Rep. 2017;7(1):692.PubMedPubMedCentral Pan B, Wang X, Nishioka C, Honda G, Yokoyama A, Zeng L, et al. G-protein coupled receptor 15 mediates angiogenesis and cytoprotective function of thrombomodulin. Sci Rep. 2017;7(1):692.PubMedPubMedCentral
50.
go back to reference Ikezoe T, Yang J, Nishioka C, Honda G, Furihata M, Yokoyama A. Thrombomodulin protects endothelial cells from a calcineurin inhibitor-induced cytotoxicity by upregulation of extracellular signal-regulated kinase/myeloid leukemia cell-1 signaling. Arterioscler Thromb Vasc Biol. 2012;32(9):2259–70.PubMed Ikezoe T, Yang J, Nishioka C, Honda G, Furihata M, Yokoyama A. Thrombomodulin protects endothelial cells from a calcineurin inhibitor-induced cytotoxicity by upregulation of extracellular signal-regulated kinase/myeloid leukemia cell-1 signaling. Arterioscler Thromb Vasc Biol. 2012;32(9):2259–70.PubMed
51.
go back to reference Pan B, Wang X, Kojima S, Nishioka C, Yokoyama A, Honda G, et al. The fifth epidermal growth factor like region of thrombomodulin alleviates LPS-induced sepsis through interacting with GPR15. Thromb Haemost. 2017;117(3):570–9.PubMed Pan B, Wang X, Kojima S, Nishioka C, Yokoyama A, Honda G, et al. The fifth epidermal growth factor like region of thrombomodulin alleviates LPS-induced sepsis through interacting with GPR15. Thromb Haemost. 2017;117(3):570–9.PubMed
52.
go back to reference Pan B, Wang X, Kojima S, Nishioka C, Yokoyama A, Honda G, et al. The fifth epidermal growth factor-like region of thrombomodulin alleviates murine graft-versus-host disease in a G-protein coupled receptor 15 dependent manner. Biol Blood Marrow Transplant. 2017;23(5):746–56.PubMed Pan B, Wang X, Kojima S, Nishioka C, Yokoyama A, Honda G, et al. The fifth epidermal growth factor-like region of thrombomodulin alleviates murine graft-versus-host disease in a G-protein coupled receptor 15 dependent manner. Biol Blood Marrow Transplant. 2017;23(5):746–56.PubMed
53.
go back to reference Saito H, Maruyama I, Shimazaki S, Yamamoto Y, Aikawa N, Ohno R, et al. Efficacy and safety of recombinant human soluble thrombomodulin (ART-123) in disseminated intravascular coagulation: results of a phase III, randomized, double-blind clinical trial. J Thromb Haemost. 2007;5(1):31–41.PubMed Saito H, Maruyama I, Shimazaki S, Yamamoto Y, Aikawa N, Ohno R, et al. Efficacy and safety of recombinant human soluble thrombomodulin (ART-123) in disseminated intravascular coagulation: results of a phase III, randomized, double-blind clinical trial. J Thromb Haemost. 2007;5(1):31–41.PubMed
54.
go back to reference Matsushita T, Watanabe J, Honda G, Mimuro J, Takahashi H, Tsuji H, et al. Thrombomodulin alfa treatment in patients with acute promyelocytic leukemia and disseminated intravascular coagulation: a retrospective analysis of an open-label, multicenter, post-marketing surveillance study cohort. Thromb Res. 2014;133(5):772–81.PubMed Matsushita T, Watanabe J, Honda G, Mimuro J, Takahashi H, Tsuji H, et al. Thrombomodulin alfa treatment in patients with acute promyelocytic leukemia and disseminated intravascular coagulation: a retrospective analysis of an open-label, multicenter, post-marketing surveillance study cohort. Thromb Res. 2014;133(5):772–81.PubMed
55.
go back to reference Ikezoe T, Takeuchi A, Isaka M, Arakawa Y, Iwabu N, Kin T, et al. Recombinant human soluble thrombomodulin safely and effectively rescues acute promyelocytic leukemia patients from disseminated intravascular coagulation. Leuk Res. 2012;36(11):1398–402.PubMed Ikezoe T, Takeuchi A, Isaka M, Arakawa Y, Iwabu N, Kin T, et al. Recombinant human soluble thrombomodulin safely and effectively rescues acute promyelocytic leukemia patients from disseminated intravascular coagulation. Leuk Res. 2012;36(11):1398–402.PubMed
56.
go back to reference Kawano N, Kuriyama T, Yoshida S, Yamashita K, Ochiai H, Nakazaki S, et al. Clinical features and treatment outcomes of six patients with disseminated intravascular coagulation resulting from acute promyelocytic leukemia and treated with recombinant human soluble thrombomodulin at a single institution. Intern Med. 2013;52(1):55–62.PubMed Kawano N, Kuriyama T, Yoshida S, Yamashita K, Ochiai H, Nakazaki S, et al. Clinical features and treatment outcomes of six patients with disseminated intravascular coagulation resulting from acute promyelocytic leukemia and treated with recombinant human soluble thrombomodulin at a single institution. Intern Med. 2013;52(1):55–62.PubMed
57.
go back to reference Ikezoe T, Yang J, Nishioka C, Isaka M, Iwabu N, Sakai M, et al. Thrombomodulin enhances the antifibrinolytic and antileukemic effects of all-trans retinoic acid in acute promyelocytic leukemia cells. Exp Hematol. 2012;40(6):457–65.PubMed Ikezoe T, Yang J, Nishioka C, Isaka M, Iwabu N, Sakai M, et al. Thrombomodulin enhances the antifibrinolytic and antileukemic effects of all-trans retinoic acid in acute promyelocytic leukemia cells. Exp Hematol. 2012;40(6):457–65.PubMed
58.
go back to reference Takezako N, Sekiguchi N, Nagata A, Homma C, Takezako Y, Noto S, et al. Recombinant human thrombomodulin in the treatment of acute myeloid leukemia patients complicated by disseminated intravascular coagulation: retrospective analysis of outcomes between patients treated with heparin and recombinant human thrombomodulin therapy. Thromb Res. 2015;136(1):20–3.PubMed Takezako N, Sekiguchi N, Nagata A, Homma C, Takezako Y, Noto S, et al. Recombinant human thrombomodulin in the treatment of acute myeloid leukemia patients complicated by disseminated intravascular coagulation: retrospective analysis of outcomes between patients treated with heparin and recombinant human thrombomodulin therapy. Thromb Res. 2015;136(1):20–3.PubMed
59.
go back to reference Minakata D, Fujiwara SI, Ikeda T, Kawaguchi SI, Toda Y, Ito S, et al. Comparison of gabexate mesilate and nafamostat mesilate for disseminated intravascular coagulation associated with hematological malignancies. Int J Hematol. 2019;109(2):141–6.PubMed Minakata D, Fujiwara SI, Ikeda T, Kawaguchi SI, Toda Y, Ito S, et al. Comparison of gabexate mesilate and nafamostat mesilate for disseminated intravascular coagulation associated with hematological malignancies. Int J Hematol. 2019;109(2):141–6.PubMed
61.
go back to reference Schuster SJ, Maziarz RT, Rusch ES, Li J, Signorovitch JE, Romanov VV, et al. Grading and management of cytokine release syndrome in patients treated with tisagenlecleucel in the JULIET trial. Blood Adv. 2020;4(7):1432–9.PubMedPubMedCentral Schuster SJ, Maziarz RT, Rusch ES, Li J, Signorovitch JE, Romanov VV, et al. Grading and management of cytokine release syndrome in patients treated with tisagenlecleucel in the JULIET trial. Blood Adv. 2020;4(7):1432–9.PubMedPubMedCentral
62.
go back to reference Jiang H, Liu L, Guo T, Wu Y, Ai L, Deng J, Dong J, Mei H, Hu Y. Improving the safety of CAR-T cell therapy by controlling CRS-related coagulopathy. Ann Hematol. 2019;98(7):1721–32.PubMed Jiang H, Liu L, Guo T, Wu Y, Ai L, Deng J, Dong J, Mei H, Hu Y. Improving the safety of CAR-T cell therapy by controlling CRS-related coagulopathy. Ann Hematol. 2019;98(7):1721–32.PubMed
63.
go back to reference Wang Y, Qi K, Cheng H, Cao J, Shi M, Qiao J, et al. Coagulation disorders after chimeric antigen receptor T cell therapy: analysis of 100 patients with relapsed and refractory hematologic malignancies. Biol Blood Marrow Transplant. 2020;26(5):865–75.PubMed Wang Y, Qi K, Cheng H, Cao J, Shi M, Qiao J, et al. Coagulation disorders after chimeric antigen receptor T cell therapy: analysis of 100 patients with relapsed and refractory hematologic malignancies. Biol Blood Marrow Transplant. 2020;26(5):865–75.PubMed
64.
go back to reference Taylor FB Jr, Toh C-H, Hoots KW, Wada H, Levi M. Towards definition, clinical and laboratory criteria, and a scoring system for disseminated intravascular coagulation. Thromb Haemost. 2001;86:1327–30.PubMed Taylor FB Jr, Toh C-H, Hoots KW, Wada H, Levi M. Towards definition, clinical and laboratory criteria, and a scoring system for disseminated intravascular coagulation. Thromb Haemost. 2001;86:1327–30.PubMed
65.
go back to reference Ikezoe T, Takeuchi A, Chi S, Takaoka M, Anabuki K, Kim T, et al. Effect of recombinant human soluble thrombomodulin on clinical outcomes of patients with coagulopathy after hematopoietic stem cell transplantation. Eur J Haematol. 2013;91(5):442–7.PubMed Ikezoe T, Takeuchi A, Chi S, Takaoka M, Anabuki K, Kim T, et al. Effect of recombinant human soluble thrombomodulin on clinical outcomes of patients with coagulopathy after hematopoietic stem cell transplantation. Eur J Haematol. 2013;91(5):442–7.PubMed
66.
go back to reference Matsumoto T, Wada H, Nishiyama H, Hirano T, Sakakura M, Nishii K, et al. Hemostatic abnormalities and changes following bone marrow transplantation. Clin Appl Thromb Hemost. 2004;10:341–50.PubMed Matsumoto T, Wada H, Nishiyama H, Hirano T, Sakakura M, Nishii K, et al. Hemostatic abnormalities and changes following bone marrow transplantation. Clin Appl Thromb Hemost. 2004;10:341–50.PubMed
67.
go back to reference Mohty M, Malard F, Abecasis M, Aerts E, Alaskar AS, Aljurf M, et al. Prophylactic, preemptive, and curative treatment for sinusoidal obstruction syndrome/veno-occlusive disease in adult patients: a position statement from an international expert group. Bone Marrow Transplant. 2020;55(3):485–95.PubMed Mohty M, Malard F, Abecasis M, Aerts E, Alaskar AS, Aljurf M, et al. Prophylactic, preemptive, and curative treatment for sinusoidal obstruction syndrome/veno-occlusive disease in adult patients: a position statement from an international expert group. Bone Marrow Transplant. 2020;55(3):485–95.PubMed
68.
go back to reference DeLeve LD, Ito Y, Bethea NW, et al. Embolization by sinusoidal lining cells obstructs the microcirculation in rat sinusoidal obstruction syndrome. Am J Physiol Gastrointest Liver Physiol. 2003;284:G1045–52.PubMed DeLeve LD, Ito Y, Bethea NW, et al. Embolization by sinusoidal lining cells obstructs the microcirculation in rat sinusoidal obstruction syndrome. Am J Physiol Gastrointest Liver Physiol. 2003;284:G1045–52.PubMed
69.
go back to reference Corbacioglu S, Jabbour EJ, Mohty M. Risk factors for development of and progression of hepatic veno-occlusive disease/sinusoidal obstruction syndrome. Biol Blood Marrow Transplant. 2019;25(7):1271–80.PubMed Corbacioglu S, Jabbour EJ, Mohty M. Risk factors for development of and progression of hepatic veno-occlusive disease/sinusoidal obstruction syndrome. Biol Blood Marrow Transplant. 2019;25(7):1271–80.PubMed
70.
go back to reference Ikezoe T, Togitani K, Komatsu N, Isaka M, Yokoyama A. Successful treatment of sinusoidal obstructive syndrome after hematopoietic stem cell transplantation with recombinant human soluble thrombomodulin. Bone Marrow Transplant. 2010;45(4):783–5.PubMed Ikezoe T, Togitani K, Komatsu N, Isaka M, Yokoyama A. Successful treatment of sinusoidal obstructive syndrome after hematopoietic stem cell transplantation with recombinant human soluble thrombomodulin. Bone Marrow Transplant. 2010;45(4):783–5.PubMed
71.
go back to reference Ohwada C, Takeuchi M, Kawaguchi T, Tsukamoto S, Sakai S, Takeda Y, et al. Successful treatment with recombinant soluble thrombomodulin of two cases of sinusoidal obstructive syndrome/hepatic veno-occlusive disease after bone marrow transplantation. Am J Hematol. 2011;86(10):886–8.PubMed Ohwada C, Takeuchi M, Kawaguchi T, Tsukamoto S, Sakai S, Takeda Y, et al. Successful treatment with recombinant soluble thrombomodulin of two cases of sinusoidal obstructive syndrome/hepatic veno-occlusive disease after bone marrow transplantation. Am J Hematol. 2011;86(10):886–8.PubMed
72.
go back to reference Nakamura D, Yoshimitsu M, Kawada H, Inoue H, Kuroki T, Kaieda T, et al. Recombinant human soluble thrombomodulin for the treatment of hepatic sinusoidal obstructive syndrome post allogeneic hematopoietic SCT. Bone Marrow Transplant. 2012;47(3):463–4.PubMed Nakamura D, Yoshimitsu M, Kawada H, Inoue H, Kuroki T, Kaieda T, et al. Recombinant human soluble thrombomodulin for the treatment of hepatic sinusoidal obstructive syndrome post allogeneic hematopoietic SCT. Bone Marrow Transplant. 2012;47(3):463–4.PubMed
73.
go back to reference Inagaki J, Kurauchi K, Fukano R, Noguchi M, Okamura J. Heterogeneous response to recombinant thrombomodulin by grade of sinusoidal obstructive syndrome after pediatric stem cell transplantation. Bone Marrow Transplant. 2016;51(11):1543–5.PubMed Inagaki J, Kurauchi K, Fukano R, Noguchi M, Okamura J. Heterogeneous response to recombinant thrombomodulin by grade of sinusoidal obstructive syndrome after pediatric stem cell transplantation. Bone Marrow Transplant. 2016;51(11):1543–5.PubMed
74.
go back to reference Yakushijin K, Ikezoe T, Ohwada C, Kudo K, Okamura H, Goto H, et al. Clinical effects of recombinant thrombomodulin and defibrotide on sinusoidal obstruction syndrome after allogeneic hematopoietic stem cell transplantation. Bone Marrow Transplant. 2019;54(5):674–80.PubMed Yakushijin K, Ikezoe T, Ohwada C, Kudo K, Okamura H, Goto H, et al. Clinical effects of recombinant thrombomodulin and defibrotide on sinusoidal obstruction syndrome after allogeneic hematopoietic stem cell transplantation. Bone Marrow Transplant. 2019;54(5):674–80.PubMed
75.
go back to reference Ikezoe T, Yang J, Nishioka C, Pan B, Xu K, Furihata M, et al. The fifth epidermal growth factor-like region of thrombomodulin exerts cytoprotective function and prevents SOS in a murine model. Bone Marrow Transplant. 2017;52(1):73–9.PubMed Ikezoe T, Yang J, Nishioka C, Pan B, Xu K, Furihata M, et al. The fifth epidermal growth factor-like region of thrombomodulin exerts cytoprotective function and prevents SOS in a murine model. Bone Marrow Transplant. 2017;52(1):73–9.PubMed
76.
go back to reference Wang X, Pan B, Honda G, Wang X, Hashimoto Y, Ohkawara H, et al. Cytoprotective and pro-angiogenic functions of thrombomodulin are preserved in the C loop of the fifth epidermal growth factor-like domain. Haematologica. 2018;103(10):1730–40.PubMedPubMedCentral Wang X, Pan B, Honda G, Wang X, Hashimoto Y, Ohkawara H, et al. Cytoprotective and pro-angiogenic functions of thrombomodulin are preserved in the C loop of the fifth epidermal growth factor-like domain. Haematologica. 2018;103(10):1730–40.PubMedPubMedCentral
77.
go back to reference Richardson P, Aggarwal S, Topaloglu O, Villa KF, Corbacioglu S. Systematic review of defibrotide studies in the treatment of veno-occlusive disease/sinusoidal obstruction syndrome (VOD/SOS). Bone Marrow Transplant. 2019;54(12):1951–62.PubMedPubMedCentral Richardson P, Aggarwal S, Topaloglu O, Villa KF, Corbacioglu S. Systematic review of defibrotide studies in the treatment of veno-occlusive disease/sinusoidal obstruction syndrome (VOD/SOS). Bone Marrow Transplant. 2019;54(12):1951–62.PubMedPubMedCentral
78.
go back to reference Evangelista V, Piccardoni P, de Gaetano G, Cerletti C. Defibrotide inhibits platelet activation by cathepsin G released from stimulated polymorphonuclear leukocytes. Thromb Haemost. 1992;67(6):660–4.PubMed Evangelista V, Piccardoni P, de Gaetano G, Cerletti C. Defibrotide inhibits platelet activation by cathepsin G released from stimulated polymorphonuclear leukocytes. Thromb Haemost. 1992;67(6):660–4.PubMed
79.
go back to reference Paul W, Gresele P, Momi S, Bianchi G, Page CP. The effect of defibrotide on thromboembolism in the pulmonary vasculature of mice and rabbits and in the cerebral vasculature of rabbits. Br J Pharmacol. 1993;110(4):1565–71.PubMedPubMedCentral Paul W, Gresele P, Momi S, Bianchi G, Page CP. The effect of defibrotide on thromboembolism in the pulmonary vasculature of mice and rabbits and in the cerebral vasculature of rabbits. Br J Pharmacol. 1993;110(4):1565–71.PubMedPubMedCentral
80.
go back to reference Falanga A, Vignoli A, Marchetti M, Barbui T. Defibrotide reduces procoagulant activity and increases fibrinolytic properties of endothelial cells. Leukemia. 2003;17(8):1636–42.PubMed Falanga A, Vignoli A, Marchetti M, Barbui T. Defibrotide reduces procoagulant activity and increases fibrinolytic properties of endothelial cells. Leukemia. 2003;17(8):1636–42.PubMed
81.
go back to reference Schoergenhofer C, Buchtele N, Gelbenegger G, Derhaschnig U, Firbas C, Kovacevic KD, et al. Defibrotide enhances fibrinolysis in human endotoxemia—a randomized, double blind, crossover trial in healthy volunteers. Sci Rep. 2019;9(1):11136.PubMedPubMedCentral Schoergenhofer C, Buchtele N, Gelbenegger G, Derhaschnig U, Firbas C, Kovacevic KD, et al. Defibrotide enhances fibrinolysis in human endotoxemia—a randomized, double blind, crossover trial in healthy volunteers. Sci Rep. 2019;9(1):11136.PubMedPubMedCentral
82.
go back to reference Wang X, Pan B, Hashimoto Y, Ohkawara H, Xu K, Zeng L, et al. Defibrotide stimulates angiogenesis and protects endothelial cells from calcineurin inhibitor-induced apoptosis via upregulation of AKT/Bcl-xL. Thromb Haemost. 2018;118(1):161–73.PubMed Wang X, Pan B, Hashimoto Y, Ohkawara H, Xu K, Zeng L, et al. Defibrotide stimulates angiogenesis and protects endothelial cells from calcineurin inhibitor-induced apoptosis via upregulation of AKT/Bcl-xL. Thromb Haemost. 2018;118(1):161–73.PubMed
83.
go back to reference Khosla J, Yeh AC, Spitzer TR, Dey BR. Hematopoietic stem cell transplant-associated thrombotic microangiopathy: current paradigm and novel therapies. Bone Marrow Transplant. 2018;53(2):129–37.PubMed Khosla J, Yeh AC, Spitzer TR, Dey BR. Hematopoietic stem cell transplant-associated thrombotic microangiopathy: current paradigm and novel therapies. Bone Marrow Transplant. 2018;53(2):129–37.PubMed
84.
go back to reference Zeigler ZR, Rosenfeld CS, Andrews DF 3rd, Nemunaitis J, Raymond JM, Shadduck RK, et al. Plasma von Willebrand factor antigen (vWF:AG) and thrombomodulin (TM) levels in adult thrombotic thrombocytopenic purpura/hemolytic uremic syndromes (TTP/HUS) and bone marrow transplant-associated thrombotic microangiopathy (BMT-TM). Am J Hematol. 1996;53(4):213–20.PubMed Zeigler ZR, Rosenfeld CS, Andrews DF 3rd, Nemunaitis J, Raymond JM, Shadduck RK, et al. Plasma von Willebrand factor antigen (vWF:AG) and thrombomodulin (TM) levels in adult thrombotic thrombocytopenic purpura/hemolytic uremic syndromes (TTP/HUS) and bone marrow transplant-associated thrombotic microangiopathy (BMT-TM). Am J Hematol. 1996;53(4):213–20.PubMed
85.
go back to reference Takatsuka H, Wakae T, Mori A, Okada M, Suehiro A, Okamoto T, et al. Thrombotic thrombocytopenic purpura and hemolytic uremic syndrome following allogeneic bone marrow transplantation. Bone Marrow Transplant. 2002;29(11):907–11.PubMed Takatsuka H, Wakae T, Mori A, Okada M, Suehiro A, Okamoto T, et al. Thrombotic thrombocytopenic purpura and hemolytic uremic syndrome following allogeneic bone marrow transplantation. Bone Marrow Transplant. 2002;29(11):907–11.PubMed
86.
go back to reference Chua JS, Baelde HJ, Zandbergen M, Wilhelmus S, van Es LA, et al. Complement factor C4d is a common denominator in thrombotic microangiopathy. J Am Soc Nephrol. 2015;26(9):2239–47.PubMedPubMedCentral Chua JS, Baelde HJ, Zandbergen M, Wilhelmus S, van Es LA, et al. Complement factor C4d is a common denominator in thrombotic microangiopathy. J Am Soc Nephrol. 2015;26(9):2239–47.PubMedPubMedCentral
87.
go back to reference Noris M, Remuzzi G. Atypical hemolytic-uremic syndrome. N Engl J Med. 2009;361(17):1676–87.PubMed Noris M, Remuzzi G. Atypical hemolytic-uremic syndrome. N Engl J Med. 2009;361(17):1676–87.PubMed
88.
go back to reference Jodele S, Medvedovic M, Luebbering N, Chen J, Dandoy CE, Laskin BL, et al. Interferon-complement loop in transplant-associated thrombotic microangiopathy. Blood Adv. 2020;4(6):1166–77.PubMedPubMedCentral Jodele S, Medvedovic M, Luebbering N, Chen J, Dandoy CE, Laskin BL, et al. Interferon-complement loop in transplant-associated thrombotic microangiopathy. Blood Adv. 2020;4(6):1166–77.PubMedPubMedCentral
89.
go back to reference Jodele S, Davies SM, Lane A, Khoury J, Dandoy C, Goebel J, et al. Diagnostic and risk criteria for HSCT-associated thrombotic microangiopathy: a study in children and young adults. Blood. 2014;124(4):645–53.PubMedPubMedCentral Jodele S, Davies SM, Lane A, Khoury J, Dandoy C, Goebel J, et al. Diagnostic and risk criteria for HSCT-associated thrombotic microangiopathy: a study in children and young adults. Blood. 2014;124(4):645–53.PubMedPubMedCentral
90.
go back to reference Atefi G, Aisiku O, Shapiro N, et al. Complement activation in trauma patients alters platelet function. Shock. 2016;46:83–8.PubMed Atefi G, Aisiku O, Shapiro N, et al. Complement activation in trauma patients alters platelet function. Shock. 2016;46:83–8.PubMed
91.
92.
go back to reference Subramaniam S, Jurk K, Hobohm L, Jäckel S, Saffarzadeh M, Schwierczek K, et al. Distinct contributions of complement factors to platelet activation and fibrin formation in venous thrombus development. Blood. 2017;129(16):2291–302.PubMedPubMedCentral Subramaniam S, Jurk K, Hobohm L, Jäckel S, Saffarzadeh M, Schwierczek K, et al. Distinct contributions of complement factors to platelet activation and fibrin formation in venous thrombus development. Blood. 2017;129(16):2291–302.PubMedPubMedCentral
93.
go back to reference Yeates L, Slatter MA, Bonanomi S, Lim FLWI, Ong SY, Dalissier A, et al. Use of defibrotide to treat transplant-associated thrombotic microangiopathy: a retrospective study of the Paediatric Diseases and Inborn Errors Working Parties of the European Society of Blood and Marrow Transplantation. Bone Marrow Transplant. 2017;52(5):762–4.PubMed Yeates L, Slatter MA, Bonanomi S, Lim FLWI, Ong SY, Dalissier A, et al. Use of defibrotide to treat transplant-associated thrombotic microangiopathy: a retrospective study of the Paediatric Diseases and Inborn Errors Working Parties of the European Society of Blood and Marrow Transplantation. Bone Marrow Transplant. 2017;52(5):762–4.PubMed
94.
go back to reference Fujiwara H, Maeda Y, Sando Y, Nakamura M, Tani K, Ishikawa T, et al. Treatment of thrombotic microangiopathy after hematopoietic stem cell transplantation with recombinant human soluble thrombomodulin. Transfusion. 2016;56(4):886–92.PubMed Fujiwara H, Maeda Y, Sando Y, Nakamura M, Tani K, Ishikawa T, et al. Treatment of thrombotic microangiopathy after hematopoietic stem cell transplantation with recombinant human soluble thrombomodulin. Transfusion. 2016;56(4):886–92.PubMed
Metadata
Title
Advances in the diagnosis and treatment of disseminated intravascular coagulation in haematological malignancies
Author
Takayuki Ikezoe
Publication date
01-01-2021
Publisher
Springer Singapore
Published in
International Journal of Hematology / Issue 1/2021
Print ISSN: 0925-5710
Electronic ISSN: 1865-3774
DOI
https://doi.org/10.1007/s12185-020-02992-w

Other articles of this Issue 1/2021

International Journal of Hematology 1/2021 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine