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Erschienen in: Annals of Hematology 2/2021

06.01.2021 | Original Article

ADAMTS-13–VWF axis in sickle cell disease patients

verfasst von: Valéria Sutana Ladeira, Amanda Rodrigues Barbosa, Marina Mendes Oliveira, Letícia Gonçalves Resende Ferreira, Wander Valadares de Oliveira Júnior, Cristiane de Oliveira Renó, Edna Afonso Reis, Daniel Gonçalves Chaves, Luci Maria Sant’Ana Dusse, Hérica Lima dos Santos, Melina de Barros Pinheiro, Danyelle Romana Alves Rios

Erschienen in: Annals of Hematology | Ausgabe 2/2021

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Abstract

Sickle cell disease (SCD) comprises a group of genetic disorders characterized by the presence of the hemoglobin (Hb) S in homozygosis or in heterozygosis with some other Hb variant or in interaction with thalassemia. SCD is characterized by a very complex pathophysiology, which determines a wide variability of clinical manifestations, including a chronic state of hypercoagulability responsible for the increased risk of thromboembolic events. ADAMTS13 and von Willebrand factor (VWF) play an important role in arterial and venous thrombosis. Thus, the aim of this study was to understand how the ADAMTS13-VWF axis behaves in sickle cell disease, as well as whether there is an association of these markers with the use of hydroxyurea (HU). This is a cross-sectional study conducted with 40 patients diagnosed with SCD and 40 healthy individuals. The analysis of the ADAMTS13-VWF axis was comparatively performed between groups of patients and controls and, afterwards, between patients with SCD who were users and non-users of HU. ADAMTS13 activity, ADAMTS13 activity/VWF:Ag, and ADAMTS13:Ag/VWF:Ag ratios were significantly lower and VWF:Ag levels significantly higher in SCD patients when compared to the controls. There was no statistically significant difference in ADAMTS13:Ag and VWF collagen binding (VWF:CB) levels between the groups evaluated. Among the categories of HU use, there was no statistically significant difference in any of the evaluated markers. As a conclusion, we could observe that the ADAMTS13-VWF axis is altered in SCD when compared to healthy individuals and that there is no association between these markers and the use of HU.
Literatur
1.
Zurück zum Zitat Ferraz MHDC, Murao M (2007) Diagnóstico laboratorial da doença falciforme em neonatos e após o sexto mês de vida. Rev Bras Hematol Hemoter 29:218–222CrossRef Ferraz MHDC, Murao M (2007) Diagnóstico laboratorial da doença falciforme em neonatos e após o sexto mês de vida. Rev Bras Hematol Hemoter 29:218–222CrossRef
2.
Zurück zum Zitat Chakravorty S, Williams TN (2015) Sickle cell disease: a neglected chronic disease of increasing global health importance. Arch Dis Child BMJ Publishing Group: 100: 48–53 Chakravorty S, Williams TN (2015) Sickle cell disease: a neglected chronic disease of increasing global health importance. Arch Dis Child BMJ Publishing Group: 100: 48–53
3.
Zurück zum Zitat Lim MY, Ataga KI, Key NS (2013) Hemostatic abnormalities in sickle cell disease. Current Opinion in Hematology. p. 472–7 Lim MY, Ataga KI, Key NS (2013) Hemostatic abnormalities in sickle cell disease. Current Opinion in Hematology. p. 472–7
4.
Zurück zum Zitat Noubouossie D, Key NS, Ataga KI (2016) Coagulation abnormalities of sickle cell disease: relationship with clinical outcomes and the effect of disease modifying therapies. Blood Rev 30:245–256CrossRef Noubouossie D, Key NS, Ataga KI (2016) Coagulation abnormalities of sickle cell disease: relationship with clinical outcomes and the effect of disease modifying therapies. Blood Rev 30:245–256CrossRef
5.
Zurück zum Zitat Pakbaz Z, Wun T (2014) Role of the hemostatic system on sickle cell disease pathophysiology and potential therapeutics. Hematology/Oncology Clinics of North America. p. 355–74 Pakbaz Z, Wun T (2014) Role of the hemostatic system on sickle cell disease pathophysiology and potential therapeutics. Hematology/Oncology Clinics of North America. p. 355–74
6.
Zurück zum Zitat Al-Awadhi A, Adekile A, Marouf R (2017) Evaluation of von Willebrand factor and ADAMTS-13 antigen and activity levels in sickle cell disease patients in Kuwait. J Thromb Thrombolysis Springer New York LLC 43:117–123CrossRef Al-Awadhi A, Adekile A, Marouf R (2017) Evaluation of von Willebrand factor and ADAMTS-13 antigen and activity levels in sickle cell disease patients in Kuwait. J Thromb Thrombolysis Springer New York LLC 43:117–123CrossRef
7.
Zurück zum Zitat Ataga KI, Moore CG, Hillery CA, Jones S, Whinna HC, Strayhorn D, Sohier C, Hinderliter A, Parise L V., Orringer EP. Coagulation activation and inflammation in sickle cell disease-associated pulmonary hypertension. Haematologica Haematologica; 2008; 93: 20–6 Ataga KI, Moore CG, Hillery CA, Jones S, Whinna HC, Strayhorn D, Sohier C, Hinderliter A, Parise L V., Orringer EP. Coagulation activation and inflammation in sickle cell disease-associated pulmonary hypertension. Haematologica Haematologica; 2008; 93: 20–6
8.
Zurück zum Zitat Ataga KI, Brittain JE, Desai P, May R, Jones S, Delaney J, Strayhorn D, Hinderliter A, Key NS. Association of coagulation activation with clinical complications in sickle cell disease. PLoS ONE. 2012 Ataga KI, Brittain JE, Desai P, May R, Jones S, Delaney J, Strayhorn D, Hinderliter A, Key NS. Association of coagulation activation with clinical complications in sickle cell disease. PLoS ONE. 2012
9.
Zurück zum Zitat Stypulkowski JB, Manfredini V. Alterações hemostáticas em pacientes com doença falciforme. Revista Brasileira de Hematologia e Hemoterapia. 2010. p. 56–62 Stypulkowski JB, Manfredini V. Alterações hemostáticas em pacientes com doença falciforme. Revista Brasileira de Hematologia e Hemoterapia. 2010. p. 56–62
10.
Zurück zum Zitat Damanhouri GA, Jarullah J, Marouf S, Hindawi SI, Mushtaq G, Kamal MA. Clinical biomarkers in sickle cell disease. Saudi Journal of Biological Sciences. Elsevier; 2015. p. 24–31 Damanhouri GA, Jarullah J, Marouf S, Hindawi SI, Mushtaq G, Kamal MA. Clinical biomarkers in sickle cell disease. Saudi Journal of Biological Sciences. Elsevier; 2015. p. 24–31
11.
Zurück zum Zitat Shah N, Thornburg C, Telen MJ, Ortel TL. Characterization of the hypercoagulable state in patients with sickle cell disease. Thromb Res; 2012; 130 Shah N, Thornburg C, Telen MJ, Ortel TL. Characterization of the hypercoagulable state in patients with sickle cell disease. Thromb Res; 2012; 130
12.
Zurück zum Zitat Cançado RD, Jesus JA. A doença falciforme no Brasil. Rev Bras Hematol Hemoter Elsevier BV; 2007; 29: 204–6 Cançado RD, Jesus JA. A doença falciforme no Brasil. Rev Bras Hematol Hemoter Elsevier BV; 2007; 29: 204–6
13.
Zurück zum Zitat Steinberg MH. Sickle cell anemia, the first molecular disease: overview of molecular etiology, pathophysiology, and therapeutic approaches. TheScientificWorldJournal. Scientific World Journal; 2008. p. 1295–324 Steinberg MH. Sickle cell anemia, the first molecular disease: overview of molecular etiology, pathophysiology, and therapeutic approaches. TheScientificWorldJournal. Scientific World Journal; 2008. p. 1295–324
14.
Zurück zum Zitat Noubouossie DCF, Lê PQ, Rozen L, Ziereisen F, Willems D, Demulder A, Ferster A. Thrombin generation in children with sickle cell disease: relationship with age, hemolysis, transcranial Doppler velocity, and hydroxyurea treatment. Eur J Haematol; 2013; 91: 46–54 Noubouossie DCF, Lê PQ, Rozen L, Ziereisen F, Willems D, Demulder A, Ferster A. Thrombin generation in children with sickle cell disease: relationship with age, hemolysis, transcranial Doppler velocity, and hydroxyurea treatment. Eur J Haematol; 2013; 91: 46–54
15.
Zurück zum Zitat Chen J, Chung DW (2018) Inflammation, von Willebrand factor, and ADAMTS13. Blood 132:141–147CrossRef Chen J, Chung DW (2018) Inflammation, von Willebrand factor, and ADAMTS13. Blood 132:141–147CrossRef
16.
Zurück zum Zitat Tonaco LC, Rios DRA, Vieira LM, Carvalho MG, Dusse LMS (2010) Púrpura trombocitopênica trombótica: O papel do fator von willebrand e da ADAMTS13. Rev Bras Hematol Hemoter 32:155–161CrossRef Tonaco LC, Rios DRA, Vieira LM, Carvalho MG, Dusse LMS (2010) Púrpura trombocitopênica trombótica: O papel do fator von willebrand e da ADAMTS13. Rev Bras Hematol Hemoter 32:155–161CrossRef
17.
Zurück zum Zitat South K, Lane DA (2018) ADAMTS-13 and von Willebrand factor: a dynamic duo. J Thromb Haemost 16:6–18CrossRef South K, Lane DA (2018) ADAMTS-13 and von Willebrand factor: a dynamic duo. J Thromb Haemost 16:6–18CrossRef
18.
Zurück zum Zitat Masias C, Cataland SR (2018) The role of ADAMTS13 testing in the diagnosis and management of thrombotic microangiopathies and thrombosis. Blood 132:903–910CrossRef Masias C, Cataland SR (2018) The role of ADAMTS13 testing in the diagnosis and management of thrombotic microangiopathies and thrombosis. Blood 132:903–910CrossRef
19.
Zurück zum Zitat Zheng XL (2013) Structure-function and regulation of ADAMTS-13 protease. J Thromb Haemost:11–23 Zheng XL (2013) Structure-function and regulation of ADAMTS-13 protease. J Thromb Haemost:11–23
20.
Zurück zum Zitat Shang D, Zheng XW, Niiya M, Zheng XL (2006) Apical sorting of ADAMTS13 in vascular endothelial cells and Madin-Darby canine kidney cells depends on the CUB domains and their association with lipid rafts. Blood 108:2207–2215CrossRef Shang D, Zheng XW, Niiya M, Zheng XL (2006) Apical sorting of ADAMTS13 in vascular endothelial cells and Madin-Darby canine kidney cells depends on the CUB domains and their association with lipid rafts. Blood 108:2207–2215CrossRef
21.
Zurück zum Zitat South K, Luken BM, Crawley JT, Phillips R, Thomas M, Collins RF, Deforche L, Vanhoorelbeke K, Lane DA (2014) Conformational activation of ADAMTS13. National Academy of Sciences 111:18578–18583CrossRef South K, Luken BM, Crawley JT, Phillips R, Thomas M, Collins RF, Deforche L, Vanhoorelbeke K, Lane DA (2014) Conformational activation of ADAMTS13. National Academy of Sciences 111:18578–18583CrossRef
22.
Zurück zum Zitat Turner NA, Nolasco L, Ruggeri ZM, Moake JL (2009) Endothelial cell ADAMTS-13 and VWF: production, release, and VWF string cleavage. Blood 114:5102–5111CrossRef Turner NA, Nolasco L, Ruggeri ZM, Moake JL (2009) Endothelial cell ADAMTS-13 and VWF: production, release, and VWF string cleavage. Blood 114:5102–5111CrossRef
23.
Zurück zum Zitat Roose E, Schelpe AS, Joly BS, Peetermans M, Verhamme P, Voorberg J, Greinacher A, Deckmyn H, De Meyer SF, Coppo P, Veyradier A, Vanhoorelbeke K (2018) An open conformation of ADAMTS-13 is a hallmark of acute acquired thrombotic thrombocytopenic purpura. J Thromb Haemost Blackwell Publishing Ltd 16:378–388CrossRef Roose E, Schelpe AS, Joly BS, Peetermans M, Verhamme P, Voorberg J, Greinacher A, Deckmyn H, De Meyer SF, Coppo P, Veyradier A, Vanhoorelbeke K (2018) An open conformation of ADAMTS-13 is a hallmark of acute acquired thrombotic thrombocytopenic purpura. J Thromb Haemost Blackwell Publishing Ltd 16:378–388CrossRef
24.
Zurück zum Zitat Tao Z, Peng Y, Nolasco L, Cal S, Lopez-Otin C, Li R, Moake JL, López JA, Dong JF (2005) Recombinant CUB-1 domain polypeptide inhibits the cleavage of ULVWF strings by ADAMTS13 under flow conditions. Blood 106:4139–4145CrossRef Tao Z, Peng Y, Nolasco L, Cal S, Lopez-Otin C, Li R, Moake JL, López JA, Dong JF (2005) Recombinant CUB-1 domain polypeptide inhibits the cleavage of ULVWF strings by ADAMTS13 under flow conditions. Blood 106:4139–4145CrossRef
25.
Zurück zum Zitat Uemura M, Tatsumi K, Matsumoto M, Fujimoto M, Matsuyama T, Ishikawa M, Iwamoto TA, Mori T, Wanaka A, Fukui H, Fujimura Y (2005) Localization of ADAMTS13 to the stellate cells of human liver. Blood 106:922–924CrossRef Uemura M, Tatsumi K, Matsumoto M, Fujimoto M, Matsuyama T, Ishikawa M, Iwamoto TA, Mori T, Wanaka A, Fukui H, Fujimura Y (2005) Localization of ADAMTS13 to the stellate cells of human liver. Blood 106:922–924CrossRef
26.
Zurück zum Zitat Levy GG, Nichols WC, Lian EC, Foroud T, McClintick JN, McGee BM, Yang AY, Siemieniak DR, Stark KR, Gruppo R, Sarode R, Shurin SB, Chandrasekaran V, Stabler SP, Sabio H, Bouhassira EE, Upshaw JD, Ginsburg D, Tsai HM (2001) Mutations in a member of the ADAMTS gene family cause thrombotic thrombocytopenic purpura. Nature. 413:488–494CrossRef Levy GG, Nichols WC, Lian EC, Foroud T, McClintick JN, McGee BM, Yang AY, Siemieniak DR, Stark KR, Gruppo R, Sarode R, Shurin SB, Chandrasekaran V, Stabler SP, Sabio H, Bouhassira EE, Upshaw JD, Ginsburg D, Tsai HM (2001) Mutations in a member of the ADAMTS gene family cause thrombotic thrombocytopenic purpura. Nature. 413:488–494CrossRef
27.
Zurück zum Zitat Turner N, Nolasco L, Tao Z, Dong JF, Moake J (2006) Human endothelial cells synthesize and release ADAMTS-13. J Thromb Haemost 4:1396–1404CrossRef Turner N, Nolasco L, Tao Z, Dong JF, Moake J (2006) Human endothelial cells synthesize and release ADAMTS-13. J Thromb Haemost 4:1396–1404CrossRef
28.
Zurück zum Zitat Liu L, Choi H, Bernardo A, Bergeron AL, Nolasco L, Ruan C, Moake JL, Dong JF (2005) Platelet-derived VWF-cleaving metalloprotease ADAMTS-13. J Thromb Haemost 3:2536–2544CrossRef Liu L, Choi H, Bernardo A, Bergeron AL, Nolasco L, Ruan C, Moake JL, Dong JF (2005) Platelet-derived VWF-cleaving metalloprotease ADAMTS-13. J Thromb Haemost 3:2536–2544CrossRef
29.
Zurück zum Zitat Suzuki M, Murata M, Matsubara Y, Uchida T, Ishihara H, Shibano T, Ashida SI, Soejima K, Okada Y, Ikeda Y. Detection of von Willebrand factor-cleaving protease (ADAMTS-13) in human platelets. Biochem Biophys Res Commun Academic Press Inc.; 2004; 313: 212–6 Suzuki M, Murata M, Matsubara Y, Uchida T, Ishihara H, Shibano T, Ashida SI, Soejima K, Okada Y, Ikeda Y. Detection of von Willebrand factor-cleaving protease (ADAMTS-13) in human platelets. Biochem Biophys Res Commun Academic Press Inc.; 2004; 313: 212–6
30.
Zurück zum Zitat Oliveira LMM, Amorim MVA, Corsini CA, Neto CCA, Chaves DG (2018) Standardization and comparison of nonautomated assays to measure the collagen binding activity of von Willebrand factor. Int J Lab Hematol 40:597–603CrossRef Oliveira LMM, Amorim MVA, Corsini CA, Neto CCA, Chaves DG (2018) Standardization and comparison of nonautomated assays to measure the collagen binding activity of von Willebrand factor. Int J Lab Hematol 40:597–603CrossRef
31.
Zurück zum Zitat Zhou Z, Han H, Cruz MA, López JA, Dong J, Guchhait P (2009) Haemoglobin blocks von Willebrand factor proteolysis by ADAMTS-13: a mechanism associated with sickle cell disease. Thromb Haemost 101:1070–1077CrossRef Zhou Z, Han H, Cruz MA, López JA, Dong J, Guchhait P (2009) Haemoglobin blocks von Willebrand factor proteolysis by ADAMTS-13: a mechanism associated with sickle cell disease. Thromb Haemost 101:1070–1077CrossRef
32.
Zurück zum Zitat Jousselme E, Jourdy Y, Rugeri L, Négrier C, Nougier C. Comparison of an automated chemiluminescent assay to a manual ELISA assay for determination of von Willebrand factor collagen binding activity on VWD plasma patients previously diagnosed through molecular analysis of VWF. Int J Lab Hematol Blackwell Publishing Ltd; 2018; 40: 77–83 Jousselme E, Jourdy Y, Rugeri L, Négrier C, Nougier C. Comparison of an automated chemiluminescent assay to a manual ELISA assay for determination of von Willebrand factor collagen binding activity on VWD plasma patients previously diagnosed through molecular analysis of VWF. Int J Lab Hematol Blackwell Publishing Ltd; 2018; 40: 77–83
33.
Zurück zum Zitat Sonneveld MAH, Franco OH, Ikram MA, Hofman A, Kavousi M, De Maat MPM, Leebeek FWG. Von Willebrand factor, ADAMTS13, and the risk of mortality: the Rotterdam study. Arterioscler Thromb Vasc Biol Lippincott Williams and Wilkins; 2016; 36: 2446–51 Sonneveld MAH, Franco OH, Ikram MA, Hofman A, Kavousi M, De Maat MPM, Leebeek FWG. Von Willebrand factor, ADAMTS13, and the risk of mortality: the Rotterdam study. Arterioscler Thromb Vasc Biol Lippincott Williams and Wilkins; 2016; 36: 2446–51
34.
Zurück zum Zitat Denorme F, Kraft P, Pareyn I, Drechsler C, Deckmyn H, Vanhoorelbeke K, Kleinschnitz C, De Meyer SF. Reduced ADAMTS13 levels in patients with acute and chronic cerebrovascular disease. PLoS One Public Library of Science; 2017; 12 Denorme F, Kraft P, Pareyn I, Drechsler C, Deckmyn H, Vanhoorelbeke K, Kleinschnitz C, De Meyer SF. Reduced ADAMTS13 levels in patients with acute and chronic cerebrovascular disease. PLoS One Public Library of Science; 2017; 12
35.
Zurück zum Zitat Zago MA, Pinto ACS. Fisiopatologia das doenças falciformes: Da mutação genética à insuficiência de múltiplos órgãos. Revista Brasileira de Hematologia e Hemoterapia. 2007. p. 207–14 Zago MA, Pinto ACS. Fisiopatologia das doenças falciformes: Da mutação genética à insuficiência de múltiplos órgãos. Revista Brasileira de Hematologia e Hemoterapia. 2007. p. 207–14
36.
Zurück zum Zitat Braga JAP (2007) Medidas gerais no tratamento das doenças falciformes. Rev Bras Hematol Hemoter 29:233–238CrossRef Braga JAP (2007) Medidas gerais no tratamento das doenças falciformes. Rev Bras Hematol Hemoter 29:233–238CrossRef
37.
Zurück zum Zitat Brasil. Ministério Da Saúde Secretaria De Atenção À Saúde Secretaria De Ciência, Tecnologia E Insumos Estratégicos Portaria Conjunta No. Ministério da Saúde. 2018. p. 38 Brasil. Ministério Da Saúde Secretaria De Atenção À Saúde Secretaria De Ciência, Tecnologia E Insumos Estratégicos Portaria Conjunta No. Ministério da Saúde. 2018. p. 38
38.
Zurück zum Zitat Gerotziafas GT, van Dreden P, Chaari M, Galea V, Khaterchi A, Lionnet F, Stankovic-Stojanovic K, Blanc-Brude O, Woodhams B, Maier-Redelsperger M, Girot R, Hatmi M, Elalamy I (2012) The acceleration of the propagation phase of thrombin generation in patients with steady-state sickle cell disease is associated with circulating erythrocyte-derived micro particles. Thromb Haemost 107:1044–1052CrossRef Gerotziafas GT, van Dreden P, Chaari M, Galea V, Khaterchi A, Lionnet F, Stankovic-Stojanovic K, Blanc-Brude O, Woodhams B, Maier-Redelsperger M, Girot R, Hatmi M, Elalamy I (2012) The acceleration of the propagation phase of thrombin generation in patients with steady-state sickle cell disease is associated with circulating erythrocyte-derived micro particles. Thromb Haemost 107:1044–1052CrossRef
39.
Zurück zum Zitat Kasar M, Boğa C, Yeral M, Asma S, Kozanoglu I, Ozdogu H (2014) Clinical significance of circulating blood and endothelial cell microparticles in sickle-cell disease. J Thromb Thrombolysis Kluwer Academic Publishers 38:167–175CrossRef Kasar M, Boğa C, Yeral M, Asma S, Kozanoglu I, Ozdogu H (2014) Clinical significance of circulating blood and endothelial cell microparticles in sickle-cell disease. J Thromb Thrombolysis Kluwer Academic Publishers 38:167–175CrossRef
40.
Zurück zum Zitat Nébor D, Romana M, Santiago R, Vachiery N, Picot J, Broquere C, Chaar V, Doumdo L, Odièvre MH, Benkerrou M, Elion J (2013) Fetal hemoglobin and hydroxycarbamide modulate both plasma concentration and cellular origin of circulating microparticles in sickle cell anemia children. Haematologica 98:862–867CrossRef Nébor D, Romana M, Santiago R, Vachiery N, Picot J, Broquere C, Chaar V, Doumdo L, Odièvre MH, Benkerrou M, Elion J (2013) Fetal hemoglobin and hydroxycarbamide modulate both plasma concentration and cellular origin of circulating microparticles in sickle cell anemia children. Haematologica 98:862–867CrossRef
41.
Zurück zum Zitat Westerman M, Pizzey A, Hirschman J, Cerino M, Weil-Weiner Y, Ramotar P, Eze A, Lawrie A, Purdy G, Mackie I, Porter J (2008) Microvesicles in haemoglobinopathies offer insights into mechanisms of hypercoagulability, haemolysis and the effects of therapy. Br J Haematol 142:126–135CrossRef Westerman M, Pizzey A, Hirschman J, Cerino M, Weil-Weiner Y, Ramotar P, Eze A, Lawrie A, Purdy G, Mackie I, Porter J (2008) Microvesicles in haemoglobinopathies offer insights into mechanisms of hypercoagulability, haemolysis and the effects of therapy. Br J Haematol 142:126–135CrossRef
42.
Zurück zum Zitat Brunetta DM, De Santis GC, Silva-Pinto AC, Oliveira De Oliveira LC, Covas DT (2015) Hydroxyurea increases plasma concentrations of microparticles and reduces coagulation activation and fibrinolysis in patients with sickle cell anemia. Acta Haematol S. Karger AG 133:287–294CrossRef Brunetta DM, De Santis GC, Silva-Pinto AC, Oliveira De Oliveira LC, Covas DT (2015) Hydroxyurea increases plasma concentrations of microparticles and reduces coagulation activation and fibrinolysis in patients with sickle cell anemia. Acta Haematol S. Karger AG 133:287–294CrossRef
43.
Zurück zum Zitat Koc A, Gumruk F, Gurgey A (2003) The effect of hydroxyurea on the coagulation system in sickle cell anemia and β-thalassemia intermedia patients: a preliminary study. Pediatr Hematol Oncol 20:429–434CrossRef Koc A, Gumruk F, Gurgey A (2003) The effect of hydroxyurea on the coagulation system in sickle cell anemia and β-thalassemia intermedia patients: a preliminary study. Pediatr Hematol Oncol 20:429–434CrossRef
44.
Zurück zum Zitat Cannas G, Poutrel S, Thomas X. Hydroxycarbamine: From an old drug used in malignant hemopathies to a current standard in sickle cell disease. Mediterranean Journal of Hematology and Infectious Diseases. Universita Cattolica del Sacro Cuore; 2017 Cannas G, Poutrel S, Thomas X. Hydroxycarbamine: From an old drug used in malignant hemopathies to a current standard in sickle cell disease. Mediterranean Journal of Hematology and Infectious Diseases. Universita Cattolica del Sacro Cuore; 2017
45.
Zurück zum Zitat McGann PT, Ware RE. Hydroxyurea for sickle cell anemia: what have we learned and what questions still remain? Curr Opin Hematol; 2011; 18: 158–165 McGann PT, Ware RE. Hydroxyurea for sickle cell anemia: what have we learned and what questions still remain? Curr Opin Hematol; 2011; 18: 158–165
46.
Zurück zum Zitat McGann PT, Ware RE. Hydroxyurea therapy for sickle cell anemia. Expert Opinion on Drug Safety. Taylor and Francis Ltd; 2015. p. 1749–58 McGann PT, Ware RE. Hydroxyurea therapy for sickle cell anemia. Expert Opinion on Drug Safety. Taylor and Francis Ltd; 2015. p. 1749–58
47.
Zurück zum Zitat Ware RE. How I use hydroxyurea to treat young patients with sickle cell anemia. Blood; 2010. p. 5300–11 Ware RE. How I use hydroxyurea to treat young patients with sickle cell anemia. Blood; 2010. p. 5300–11
48.
Zurück zum Zitat Piel FB, Steinberg MH, Rees DC. Sickle cell disease. New England Journal of Medicine. Massachussetts Medical Society; 2017. p. 1561–73 Piel FB, Steinberg MH, Rees DC. Sickle cell disease. New England Journal of Medicine. Massachussetts Medical Society; 2017. p. 1561–73
Metadaten
Titel
ADAMTS-13–VWF axis in sickle cell disease patients
verfasst von
Valéria Sutana Ladeira
Amanda Rodrigues Barbosa
Marina Mendes Oliveira
Letícia Gonçalves Resende Ferreira
Wander Valadares de Oliveira Júnior
Cristiane de Oliveira Renó
Edna Afonso Reis
Daniel Gonçalves Chaves
Luci Maria Sant’Ana Dusse
Hérica Lima dos Santos
Melina de Barros Pinheiro
Danyelle Romana Alves Rios
Publikationsdatum
06.01.2021
Verlag
Springer Berlin Heidelberg
Erschienen in
Annals of Hematology / Ausgabe 2/2021
Print ISSN: 0939-5555
Elektronische ISSN: 1432-0584
DOI
https://doi.org/10.1007/s00277-020-04385-9

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