Hematological manifestations of antiphospholipid syndrome: Going beyond thrombosis

Lim, 2013, Antiphospholipid syndrome, Hematology Am Soc Hematol Educ Program, 2013, 675, 10.1182/asheducation-2013.1.675 Miyakis, 2006, International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS), J Thromb Haemost, 4, 295, 10.1111/j.1538-7836.2006.01753.x Dabit, 2022, Epidemiology of antiphospholipid syndrome in the general population, Curr Rheumatol Rep, 23, 85, 10.1007/s11926-021-01038-2 Pregnolato, 2013, Anti-phosphatidylserine/prothrombin antibodies: an additional diagnostic marker for APS?, Immunol Res, 56, 432, 10.1007/s12026-013-8421-z Bertolaccini, 2014, 14th international congress on antiphospholipid antibodies task force. Report on antiphospholipid syndrome laboratory diagnostics and trends, Autoimmun Rev, 13, 917, 10.1016/j.autrev.2014.05.001 Rodeghiero, 2009, Standardization of terminology, definitions and outcome criteria in immune thrombocytopenic purpura of adults and children: report from an international working group, Blood, 113, 2386, 10.1182/blood-2008-07-162503 Bidot, 2005, Antiphospholipid antibodies in immune thrombocytopenic purpura tend to emerge in exacerbation and decline in remission, Br J Haematol, 128, 366, 10.1111/j.1365-2141.2004.05314.x Harris, 1985, Anticardiolipin antibodies in autoimmune thrombocytopenic purpura, Br J Haematol, 59, 231, 10.1111/j.1365-2141.1985.tb02989.x Stasi, 1994, Prevalence and clinical significance of elevated antiphospholipid antibodies in patients with idiopathic thrombocytopenic purpura, Blood, 84, 4203, 10.1182/blood.V84.12.4203.bloodjournal84124203 Pierrot-Deseilligny Despujol, 2008, Antiphospholipid antibodies in adults with immune thrombocytopenic purpura, Br J Haematol, 142, 638, 10.1111/j.1365-2141.2008.07228.x Dayama, 2017, Incidence of antiphospholipid antibodies in patients with immune thrombocytopenia and correlation with treatment with steroids in north Indian population, Clin Appl Thromb Hemost, 23, 657, 10.1177/1076029616643820 Dash, 2004, Lupus anticoagulant in immune thrombocytopenic purpura, Indian J Pediatr, 71, 505, 10.1007/BF02724290 Hisada, 2017, Thrombotic risk stratification by platelet count in patients with antiphospholipid antibodies: a longitudinal study, J Thromb Haemost, 15, 1782, 10.1111/jth.13763 George, 1996, Idiopathic thrombocytopenic purpura: a practice guideline developed by explicit methods for the American Society of Hematology, Blood, 88, 3, 10.1182/blood.V88.1.3.3 Sciascia, 2014, Thrombotic risk assessment in systemic lupus erythematosus: validation of the global antiphospholipid syndrome score in a prospective cohort, Arthritis Care Res (Hoboken), 66, 1915, 10.1002/acr.22388 Radin, 2018, Extra-criteria manifestations of antiphospholipid syndrome: risk assessment and management, Semin Arthritis Rheum, 48, 117, 10.1016/j.semarthrit.2017.12.006 Veneri, 2009, Thrombocytopenias: a clinical point of view, Blood Transfus, 7, 75 Cuadrado, 1997, Thrombocytopenia in the antiphospholipid syndrome, Ann Rheum Dis, 56, 194, 10.1136/ard.56.3.194 Demetrio Pablo, 2017, Thrombocytopenia as a thrombotic risk factor in patients with antiphospholipid antibodies without disease criteria, Med Clin (Barc), 148, 394, 10.1016/j.medcli.2016.11.026 Chaturvedi, 2017, Diagnosis and management of the antiphospholipid syndrome, Blood Rev, 31, 406, 10.1016/j.blre.2017.07.006 Breen, 2015, Endothelial and platelet microparticles in patients with antiphospholipid antibodies, Thromb Res, 135, 368, 10.1016/j.thromres.2014.11.027 Proulle, 2014, Platelets are required for enhanced activation of the endothelium and fibrinogen in a mouse thrombosis model of APS, Blood, 124, 611, 10.1182/blood-2014-02-554980 Cikrikcioglu, 2010, Splenomegaly in primary antiphospholipid syndrome without accompanying portal hypertension or comorbidity, Pathophysiol Haemost Thromb, 37, 104, 10.1159/000327506 Avcin, 2003, Evans syndrome associated with antiphospholipid antibodies, J Pediatr Hematol Oncol, 25, 755, 10.1097/00043426-200309000-00017 Zarza, 2020, Evans syndrome associated with antiphospholipid antibodies in a patient with SARS-COV-2 infection, Hematol Transfus Cell Ther, 42, 309, 10.1016/j.htct.2020.08.003 Audia, 2020, Evans’ syndrome: from diagnosis to treatment, J Clin Med, 9, 10.3390/jcm9123851 Artim-Esen, 2015, The significance and management of thrombocytopenia in antiphospholipid syndrome, Curr Rheumatol Rep, 17, 14, 10.1007/s11926-014-0494-8 Vreede, 2019, Cryptic conspirators: a conversation about thrombocytopenia and antiphospholipid syndrome, Curr Opin Rheumatol, 31, 231, 10.1097/BOR.0000000000000595 Neunert, 2011, The American Society of Hematology 2011 evidence-based practice guideline for immune thrombocytopenia, Blood, 117, 4190, 10.1182/blood-2010-08-302984 Shibata, 1994, Autoantibodies to heparin from patients with antiphospholipid antibody syndrome inhibit formation of antithrombin III-thrombin complexes, Blood, 83, 2532, 10.1182/blood.V83.9.2532.2532 Pengo, 1995, Binding of autoimmune cardiolipin-reactive antibodies to heparin: a mechanism of thrombosis?, Thromb Res, 78, 371, 10.1016/0049-3848(95)00070-8 Hoppensteadt, 2008, The relationship between the antiphospholipid syndrome and heparin-induced thrombocytopenia, Hematol Oncol Clin North Am, 22, v Ibrahim, 2019, A patient with remote heparin-induced thrombocytopenia and antiphospholipid syndrome requiring cardiopulmonary bypass: do current guidelines apply?, Semin Cardiothorac Vasc Anesth, 23, 256, 10.1177/1089253218779081 Cervera, 2015, Morbidity and mortality in the antiphospholipid syndrome during a 10-year period: a multicentre prospective study of 1000 patients, Ann Rheum Dis, 74, 1011, 10.1136/annrheumdis-2013-204838 Pazzola, 2015, The challenge of bleeding in antiphospholipid antibody-positive patients, Curr Rheumatol Rep, 17, 7, 10.1007/s11926-014-0481-0 Lara, 2010, Diffuse alveolar hemorrhage, Chest, 137, 1164, 10.1378/chest.08-2084 Krause, 2012, Update on diffuse alveolar hemorrhage and pulmonary vasculitis, Immunol Allergy Clin North Am, 32, 587, 10.1016/j.iac.2012.08.001 Stoots, 2019, Clinical insights into diffuse alveolar hemorrhage in antiphospholipid syndrome, Curr Rheumatol Rep, 21, 56, 10.1007/s11926-019-0852-7 Bucciarelli, 2006, Mortality in the catastrophic antiphospholipid syndrome: causes of death and prognostic factors in a series of 250 patients, Arthritis Rheum, 54, 2568, 10.1002/art.22018 Cartin-Ceba, 2014, Primary antiphospholipid syndrome-associated diffuse alveolar hemorrhage, Arthritis Care Res (Hoboken), 66, 301, 10.1002/acr.22109 Espinosa, 2002, The lung in the antiphospholipid syndrome, Ann Rheum Dis, 61, 195, 10.1136/ard.61.3.195 Ramon, 2013, Primary adrenal insufficiency due to bilateral adrenal hemorrhage-adrenal infarction in the antiphospholipid syndrome: long-term outcome of 16 patients, J Clin Endocrinol Metab, 98, 3179, 10.1210/jc.2012-4300 Anson, 1947, The blood supply of the kidney, suprarenal gland, and associated structures, Surg Gynecol Obstet, 84, 313 Espinosa, 2003, Adrenal involvement in the antiphospholipid syndrome: clinical and immunologic characteristics of 86 patients, Medicine (Baltimore), 82, 106, 10.1097/00005792-200303000-00005 Mazodier, 2012, Lupus anticoagulant-hypoprothrombinemia syndrome: report of 8 cases and review of the literature, Medicine (Baltimore), 91, 251, 10.1097/MD.0b013e31826b971f Reddy, 2015, Early detection of lupus anticoagulant-hypoprothrombinemia syndrome by rotational thromboelastometry, Blood, 126, 4699, 10.1182/blood.V126.23.4699.4699 Erkan, 1999, Lupus anticoagulant-hypoprothrombinemia syndrome associated with systemic lupus erythematosus: report of 2 cases and review of literature, Lupus, 8, 560, 10.1191/096120399678840846 Austin, 2008, The VWF/ADAMTS13 axis in the antiphospholipid syndrome: ADAMTS13 antibodies and ADAMTS13 dysfunction, Br J Haematol, 141, 536, 10.1111/j.1365-2141.2008.07074.x Hanna, 2017, 1, e1 Scully, 2012, Guidelines on the diagnosis and management of thrombotic thrombocytopenic purpura and other thrombotic microangiopathies, Br J Haematol, 158, 323, 10.1111/j.1365-2141.2012.09167.x Viner, 2017, A rare combination of thrombotic thrombocytopenic purpura and antiphospholipid syndrome, Blood Coagul Fibrinolysis, 28, 411, 10.1097/MBC.0000000000000608 Espinosa, 2004, Thrombotic microangiopathic haemolytic anaemia and antiphospholipid antibodies, Ann Rheum Dis, 63, 730, 10.1136/ard.2003.007245 Ardiles, 1998, Anticardiolipin antibodies in classic pediatric hemolytic-uremic syndrome: a possible pathogenic role, Nephron, 78, 278, 10.1159/000044936 Shiari, 2014, Atypical hemolytic-uremic syndrome associated with antiphospholipid antibodies and antiphospholipid syndrome; a novel presentation, Pediatr Rheumatol, 12, P363, 10.1186/1546-0096-12-S1-P363 Mitra, 1997, 89, 1224 Yamazaki, 2002, Von Willebrand factor-cleaving protease activity in patients of collagen disease with antiphospholipid antibodies, Rinsho Byori, 50, 301 Chaturvedi, 2020, Complement activity and complement regulatory gene mutations are associated with thrombosis in APS and CAPS, Blood, 135, 239, 10.1182/blood.2019003863 Coolman, 2010, Medical record validation of maternally reported history of preeclampsia, J Clin Epidemiol, 63, 932, 10.1016/j.jclinepi.2009.10.010 Asherson, 2007, Microangiopathic antiphospholipid-associated syndromes revisited new concepts relating to antiphospholipid antibodies and syndromes, J Rheumatol, 34, 1793 Steegers, 2010, Pre-eclampsia, Lancet, 376, 631, 10.1016/S0140-6736(10)60279-6 Pécourt, 2021, Is the presence of antiphospholipid antibodies a poor prognostic factor for patients with hemolysis, elevated liver enzymes, and low platelet count syndrome?, Am J Obstet Gynecol, 225, 10.1016/j.ajog.2021.03.039 Ulander, 2006, Pregnancy-associated recurrent liver necrosis in patient with antiphospholipid syndrome, Lupus, 15, 889, 10.1177/0961203306072385 Appenzeller, 2011, HELLP syndrome and its relationship with antiphospholipid syndrome and antiphospholipid antibodies, Semin Arthritis Rheum, 41, 517, 10.1016/j.semarthrit.2011.05.007 Freire de Carvalho, 2021, Thrombotic microangiopathy in primary antiphospholipid syndrome is linked to stroke and less deep venous thrombosis, Eur Rev Med Pharmacol Sci, 25, 7369 Wani, 2010, Catastrophic cerebral antiphospholipid syndrome presenting as cerebral infarction with haemorrhagic transformation after sudden withdrawal of warfarin in a patient with primary antiphospholipid syndrome, BMJ Case Rep, 2010, 10.1136/bcr.09.2009.2243 Chaturvedi, 2019, Complement in the pathophysiology of the antiphospholipid syndrome, Front Immunol, 10, 449, 10.3389/fimmu.2019.00449 Lonze, 2014, Eculizumab prevents recurrent antiphospholipid antibody syndrome and enables successful renal transplantation, Am J Transplant, 14, 459, 10.1111/ajt.12540 Bernardoff, 2022, Antiphospholipid antibodies and the risk of autoimmune hemolytic anemia in patients with systemic lupus erythematosus: a systematic review and meta-analysis, Autoimmun Rev, 21, 10.1016/j.autrev.2021.102913 Gelman, 2021, Cold agglutinin-mediated autoimmune hemolytic Anemia in association with antiphospholipid syndrome, Acta Haematol, 144, 693, 10.1159/000516295 Ames, 2020, Antiphospholipid antibodies and autoimmune Haemolytic Anaemia: a systematic review and Meta-analysis, Int J Mol Sci, 21, 10.3390/ijms21114120 Rottem, 2006, Autoimmune hemolytic anaemia in the antiphospholipid syndrome, Lupus, 15, 473, 10.1191/0961203306lu2336oa Klack, 2013, The prevalence of iron deficiency anemia in primary antiphospholipid syndrome: primer antifosfolipid sendromda demir eksikligi anemisinin prevalansi, Turkish J Rheumatol, 28, 10.5606/tjr.2013.2717 Simoncini, 2005, Role of reactive oxygen species and p38 MAPK in the induction of the pro-adhesive endothelial state mediated by IgG from patients with anti-phospholipid syndrome, Int Immunol, 17, 489, 10.1093/intimm/dxh229 Agmon-Levin, 2013, Ferritin in the antiphospholipid syndrome and its catastrophic variant (cAPS), Lupus, 22, 1327, 10.1177/0961203313504633 Martinez-Berriotxoa, 2004, Homocysteine, antiphospholipid antibodies and risk of thrombosis in patients with systemic lupus erythematosus, Lupus, 13, 927, 10.1191/0961203304lu2035oa Jiang, 2021, Clinical characteristics and prognosis of patients with isolated thrombotic vs. obstetric antiphospholipid syndrome: a prospective cohort study, Arthritis Res Ther, 23:138 Avivi, 2002, Hyperhomocysteinemia is common in patients with antiphospholipid syndrome and may contribute to expression of major thrombotic events, Blood Coagul Fibrinolysis, 13, 169, 10.1097/00001721-200203000-00013 Carvalho, 2021, Vitamin B12 and primary antiphospholipid syndrome, Lupus, 30, 1025, 10.1177/09612033211004712 Tefferi, 2015, Myeloproliferative neoplasms: a contemporary review, JAMA Oncol, 1, 97, 10.1001/jamaoncol.2015.89 Yalavarthi, 2015, Release of neutrophil extracellular traps by neutrophils stimulated with antiphospholipid antibodies: a newly identified mechanism of thrombosis in the antiphospholipid syndrome, Arthritis & rheumatology (Hoboken, NJ), 67, 2990, 10.1002/art.39247 Sayar, 2021, Thrombotic antiphospholipid syndrome: a practical guide to diagnosis and management, Thromb Res, 198, 213, 10.1016/j.thromres.2020.10.010 Sayar, 2021, Coexistent antiphospholipid syndrome and myeloproliferative neoplasm, Lupus, 30, 1502, 10.1177/09612033211021154 de Groot, 2012, Pathophysiology of thrombotic APS: where do we stand?, Lupus, 21, 704, 10.1177/0961203312438631 Del Porto, 2018, Systemic lupus erythematosus and myelofibrosis: a case report and revision of literature, Leuk Res Rep, 9, 58 Belfeki, 2019, Autoimmune myelofibrosis: a rare haematological involvement in systemic lupus erythematosus, BMJ Case Rep, 12, 10.1136/bcr-2018-227520 Mertz, 2021, Clinical spectrum and therapeutic management of auto-immune myelofibrosis: a nation-wide study of 30 cases, Haematologica, 106, 871, 10.3324/haematol.2020.249896 Erkan, 2003, Long term outcome of catastrophic antiphospholipid syndrome survivors, Ann Rheum Dis, 62, 530, 10.1136/ard.62.6.530 Gómez-Puerta, 2006, Antiphospholipid antibodies associated with malignancies: clinical and pathological characteristics of 120 patients, Semin Arthritis Rheum, 35, 322, 10.1016/j.semarthrit.2005.07.003 Meng, 2020, Probable catastrophic antiphospholipid syndrome secondary to chronic myelomonocytic leukaemia in an adult patient and a mini review, Lupus, 29, 1287, 10.1177/0961203320937349 El Hasbani, 2022, Thalassemia and autoimmune diseases: absence of evidence or evidence of absence?, Blood Rev, 52, 10.1016/j.blre.2021.100874 Kashef, 2008, Antiphospholipid antibodies and hepatitis C virus infection in Iranian thalassemia major patients, Int J Lab Hematol, 30, 11, 10.1111/j.1751-553X.2007.00916.x Giordano, 1998, Lupus anticoagulant, anticardiolipin antibodies and hepatitis C virus infection in thalassaemia, Br J Haematol, 102, 903, 10.1046/j.1365-2141.1998.00853.x Chinsuwan, 2020, High prevalence of antiphospholipid antibodies in children with non-transfusion dependent thalassemia and possible correlations with microparticles, Mediterr J Hematol Infect Dis, 12, 10.4084/mjhid.2020.071 Atichartakarn, 2004, Correction of hypercoagulability and amelioration of pulmonary arterial hypertension by chronic blood transfusion in an asplenic hemoglobin E/beta-thalassemia patient, Blood, 103, 2844, 10.1182/blood-2003-09-3094 Neunert, 2019, American Society of Hematology 2019 guidelines for immune thrombocytopenia, Blood Adv, 3, 3829, 10.1182/bloodadvances.2019000966 Tektonidou, 2019, EULAR recommendations for the management of antiphospholipid syndrome in adults, Ann Rheum Dis, 78, 1296, 10.1136/annrheumdis-2019-215213 Tenti, 2016, Intravenous immunoglobulins and antiphospholipid syndrome: how, when and why? A review of the literature, Autoimmun Rev, 15, 226, 10.1016/j.autrev.2015.11.009 Arnold, 2007, Systematic review: efficacy and safety of rituximab for adults with idiopathic thrombocytopenic purpura, Ann Intern Med, 146, 25, 10.7326/0003-4819-146-1-200701020-00006 Berman, 2013, Rituximab use in the catastrophic antiphospholipid syndrome: descriptive analysis of the CAPS registry patients receiving rituximab, Autoimmun Rev, 12, 1085, 10.1016/j.autrev.2013.05.004 Wang, 2016, Efficacy and safety of thrombopoietin receptor agonists in patients with primary immune thrombocytopenia: a systematic review and meta-analysis, Sci Rep, 6, 39003, 10.1038/srep39003 Vreede, 2019, Cryptic conspirators: a conversation about thrombocytopenia and antiphospholipid syndrome, Curr Opin Rheumatol, 31, 231, 10.1097/BOR.0000000000000595 Galindo, 1999, Splenectomy for refractory thrombocytopenia in the antiphospholipid syndrome, Rheumatology (Oxford), 38, 848, 10.1093/rheumatology/38.9.848 Sevim, 2019, Is there a role for immunosuppression in antiphospholipid syndrome?, Hematology Am Soc Hematol Educ Program, 2019, 426, 10.1182/hematology.2019000073 Bajaj, 1983, A mechanism for the hypoprothrombinemia of the acquired hypoprothrombinemia-lupus anticoagulant syndrome, Blood, 61, 684, 10.1182/blood.V61.4.684.684 Pengo, 2020, Prothrombin is responsible for the lupus cofactor phenomenon in a patient with lupus anticoagulant/hypoprothrombinemia syndrome, TH Open, 4 Satta, 2011, Toll-like receptor 2 mediates the activation of human monocytes and endothelial cells by antiphospholipid antibodies, Blood, 117, 5523, 10.1182/blood-2010-11-316158 Biswas, 2017, TLR2 plays a key role in platelet Hyperreactivity and accelerated thrombosis associated with hyperlipidemia, Circ Res, 121, 951, 10.1161/CIRCRESAHA.117.311069 Xie, 2014, The role of TLR4 in pathophysiology of antiphospholipid syndrome-associated thrombosis and pregnancy morbidity, Br J Haematol, 164, 165, 10.1111/bjh.12587 Cognasse, 2008, Toll-like receptor 4 ligand can differentially modulate the release of cytokines by human platelets, Br J Haematol, 141, 84, 10.1111/j.1365-2141.2008.06999.x Aslam, 2006, Platelet toll-like receptor expression modulates lipopolysaccharide-induced thrombocytopenia and tumor necrosis factor-alpha production in vivo, Blood, 107, 637, 10.1182/blood-2005-06-2202 Cognasse, 2007, Lipopolysaccharide induces sCD40L release through human platelets TLR4, but not TLR2 and TLR9, Intensive Care Med, 33, 382, 10.1007/s00134-006-0488-8 Cockrell, 2008, Annexin A2: biology and relevance to the antiphospholipid syndrome, Lupus, 17, 943, 10.1177/0961203308095329 Zhang, 2010, A novel annexin A2 protein with platelet aggregation-inhibiting activity from amphibian Bombina maxima skin, Toxicon, 56, 458, 10.1016/j.toxicon.2010.04.015 Zhang, 2016, Anti-β2 glycoprotein I antibodies in complex with β2 glycoprotein I induce platelet activation via two receptors: apolipoprotein E receptor 2′ and glycoprotein I bα, Front Med, 10, 76, 10.1007/s11684-015-0426-7 Weeterings, 2006, Glycoprotein Ibalpha-mediated platelet adhesion and aggregation to immobilized thrombin under conditions of flow, Arterioscler Thromb Vasc Biol, 26, 670, 10.1161/01.ATV.0000200391.70818.a9 Urbanus, 2008, Platelet activation by dimeric beta2-glycoprotein I requires signaling via both glycoprotein Ibalpha and apolipoprotein E receptor 2′, J Thromb Haemost, 6, 1405, 10.1111/j.1538-7836.2008.03021.x Robertson, 2009, Deficiency of LRP8 in mice is associated with altered platelet function and prolonged time for in vivo thrombosis, Thromb Res, 123, 644, 10.1016/j.thromres.2008.07.003 Huang, 2021, VWF, platelets and the antiphospholipid syndrome, Int J Mol Sci, 22 Bury, 2019, Mechanisms of thrombocytopenia in platelet-type von Willebrand disease, Haematologica, 104, 1473, 10.3324/haematol.2018.200378 Sacharidou, 2018, Antiphospholipid antibodies induce thrombosis by PP2A activation via apoER2-Dab2-SHC1 complex formation in endothelium, Blood, 131, 2097, 10.1182/blood-2017-11-814681 Hollerbach, 2019, Platelet activation by antiphospholipid antibodies depends on epitope specificity and is prevented by mTOR inhibitors, Thromb Haemost, 119, 1147, 10.1055/s-0039-1685453 Qiao, 2015, The platelet fc receptor, FcγRIIa, Immunol Rev, 268, 241, 10.1111/imr.12370 Bregani, 1992, Antiphospholipid antibodies and splenic thrombosis in a patient with idiopathic myelofibrosis (antiphospholipid antibodies and thrombosis), Haematologica, 77, 516 Niki, 1995, Hematological remission of primary myelofibrosis with antiphospholipid antibody following treatment of azathioprine, Rinsho Ketsueki, 36, 141 Katayama, 1999, Primary myelofibrosis with fatal mesenteric arterial thromboembolism caused by antiphospholipid syndrome, Rinsho Ketsueki, 40, 646 Breccia, 2004, Paroxysmal cold haemoglobinuria as a tardive complication of idiopathic myelofibrosis, Eur J Haematol, 73, 304, 10.1111/j.1600-0609.2004.00301.x