Catastrophic Thrombosis: A Narrative Review

Abstract

Catastrophic thrombosis is a severe condition characterized by a hypercoagulable tendency, leading to multiple thromboembolic events in different blood vessels, usually within a short timeframe. Several conditions have been associated with the development of catastrophic thrombosis, including the catastrophic antiphospholipid syndrome, thrombotic anti-platelet factor 4 immune disorders, thrombotic microangiopathies, cancers, the hyper-eosinophilic syndrome, pregnancy, infections, trauma, and drugs. Thrombotic storm represents a medical emergency whose management represents a serious challenge for physicians. Besides the prompt start of anticoagulation, a patient's prognosis depends on early recognition and possible treatment of the underlying condition. In this narrative review, we summarize the main characteristics of catastrophic thrombosis, analyzing the various conditions triggering such life-threatening complication. Finally, an algorithm with the diagnostic workup and the initial management of patients with catastrophic thrombosis is presented.

Keywords

catastrophic thrombosis - thrombotic storm - antiphospholipid syndrome - PF4 antibodies

Publikationsverlauf

Artikel online veröffentlicht:
16. August 2024

• References

• 1 Ortel TL, Kitchens CS, Erkan D. et al. Clinical causes and treatment of the thrombotic storm. Expert Rev Hematol 2012; 5 (06) 653-659
• 2 Kitchens CS, Erkan D, Brandão LR. et al. Thrombotic storm revisited: preliminary diagnostic criteria suggested by the thrombotic storm study group. Am J Med 2011; 124 (04) 290-296
• 3 Kitchens CS. Thrombotic storm: when thrombosis begets thrombosis. Am J Med 1998; 104 (04) 381-385
• 4 Ortel TL, Erkan D, Kitchens CS. How I treat catastrophic thrombotic syndromes. Blood 2015; 126 (11) 1285-1293
• 5 Vassiliou V, Gavriilaki E, Vlachaki E. et al. Thrombotic microangiopathy: an under-recognized cause of catastrophic thrombosis. Semin Thromb Hemost 2020; 46 (07) 768-777
• 6 Georgakopoulos A, Papadakis E, Koutroulis I. et al. Catastrophic antiphospholipid syndrome: a review of the recent literature. Front Immunol 2021; 12: 792748
• 7 Boissier F, Daghbouj N, Cointault O. et al. Thrombotic microangiopathy in critically ill patients: a review on pathophysiology, diagnosis, and therapy. J Clin Med 2021; 10 (04) 822
• 8 Chaturvedi S, McCrae KR. Thrombotic microangiopathy and associated renal disorders. Nephrol Dial Transplant 2020; 35 (11) 1844-1857
• 9 Kaur S, Bansal R, Kollimuttathuillam S. et al. The looming storm: blood and cytokines in COVID-19. Blood Rev 2021; 46: 100743
• 10 Charles J, Ploplis VA. COVID-19 induces cytokine storm and dysfunctional hemostasis. Curr Drug Targets 2022; 23 (17) 1603-1610
• 11 Asakura H, Ogawa H. COVID-19-associated coagulopathy and disseminated intravascular coagulation. Int J Hematol 2021; 113 (01) 45-57
• 12 Levi M, Thachil J. Coronavirus disease 2019 coagulopathy: disseminated intravascular coagulation and thrombotic microangiopathy-either, neither, or both. Semin Thromb Hemost 2020; 46 (07) 781-784
• 13 Tiwari NR, Phatak S, Sharma VR, Agarwal SK. COVID-19 and thrombotic microangiopathies. Thromb Res 2021; 202: 191-198
• 14 Asherson RA. The catastrophic antiphospholipid syndrome. J Rheumatol 1992; 19 (04) 508-512
• 15 Erkan D, Espinosa G, Cervera R. Catastrophic antiphospholipid syndrome: updated diagnostic algorithms. Autoimmun Rev 2010; 10 (02) 74-79
• 16 Asherson RA, Cervera R, de Groot PG. et al; Catastrophic Antiphospholipid Syndrome Registry Project Group. Catastrophic antiphospholipid syndrome: international consensus statement on classification criteria and treatment guidelines. Lupus 2003; 12 (07) 530-534
• 17 Ambati A, Knight JS, Zuo Y. Antiphospholipid syndrome management: a 2023 update and practical algorithm-based approach. Curr Opin Rheumatol 2023; 35 (03) 149-160
• 18 Knight JS, Branch DW, Ortel TL. Antiphospholipid syndrome: advances in diagnosis, pathogenesis, and management. BMJ 2023; 380: e069717
• 19 Favaloro EJ, Pasalic L, Lippi G. Classification criteria for the antiphospholipid syndrome: not the same as diagnostic criteria for antiphospholipid syndrome. Semin Thromb Hemost 2024; 50 (04) 605-608
• 20 Radin M, Cecchi I, Arbrile M. et al. Pediatric presentation of antiphospholipid syndrome: a review of recent literature with estimation of local prevalence. Semin Thromb Hemost 2024; 50 (02) 182-187
• 21 Aguirre Del-Pino R, Monahan RC, Huizinga TWJ, Eikenboom J, Steup-Beekman GM. Risk factors for antiphospholipid antibodies and antiphospholipid syndrome. Semin Thromb Hemost 2024; 50 (06) 817-828
• 22 Pengo V, Denas G. Antiphospholipid syndrome in patients with venous thromboembolism. Semin Thromb Hemost 2023; 49 (08) 833-839
• 23 Arachchillage DRJ, Pericleous C. Evolution of antiphospholipid syndrome. Semin Thromb Hemost 2023; 49 (03) 295-304
• 24 Thachil J, Favaloro EJ, Lippi G. Are antiphospholipid antibodies a surrogate risk factor for thrombosis in sepsis?. Semin Thromb Hemost 2024; 50 (02) 284-287
• 25 Aibar J, Schulman S. Arterial thrombosis in patients with antiphospholipid syndrome: a review and meta-analysis. Semin Thromb Hemost 2021; 47 (06) 709-723 (Erratum in: Semin Thromb Hemost. 2021 Sep;47(6):e1–e2. PMID: 33971678)
• 26 Marco-Rico A, Marco-Vera P. Thrombotic antiphospholipid syndrome and direct oral anticoagulants: unmet needs and review of the literature. Semin Thromb Hemost 2023; 49 (07) 736-743
• 27 Favaloro EJ, Henry BM, Lippi G. COVID-19 and antiphospholipid antibodies: time for a reality check?. Semin Thromb Hemost 2022; 48 (01) 72-92
• 28 Arcani R, Cauchois R, Suchon P. et al. “True” antiphospholipid syndrome in COVID-19: contribution of the follow-up of antiphospholipid autoantibodies. Semin Thromb Hemost 2023; 49 (01) 97-102
• 29 Gris JC, Guillotin F, Chéa M, Bourguignon C, Nouvellon É, Bouvier S. Antiphospholipid antibodies in pregnancy: maternal and neonatal implications. Semin Thromb Hemost 2023; 49 (04) 337-347
• 30 Siniscalchi C, Basaglia M, Riva M. et al. Catastrophic antiphospholipid syndrome: a review. Immuno 2024; 4: 1-13
• 31 Bitsadze V, Yakubova F, Khizroeva J. et al. Catastrophic antiphospholipid syndrome. Int J Mol Sci 2024; 25 (01) 668
• 32 Chaturvedi S, Braunstein EM, Brodsky RA. Antiphospholipid syndrome: complement activation, complement gene mutations, and therapeutic implications. J Thromb Haemost 2021; 19 (03) 607-616
• 33 Ortega-Hernandez OD, Agmon-Levin N, Blank M, Asherson RA, Shoenfeld Y. The physiopathology of the catastrophic antiphospholipid (Asherson's) syndrome: compelling evidence. J Autoimmun 2009; 32 (01) 1-6
• 34 Carmi O, Berla M, Shoenfeld Y, Levy Y. Diagnosis and management of catastrophic antiphospholipid syndrome. Expert Rev Hematol 2017; 10 (04) 365-374
• 35 Rodríguez-Pintó I, Moitinho M, Santacreu I. et al; CAPS Registry Project Group (European Forum on Antiphospholipid Antibodies). Catastrophic antiphospholipid syndrome (CAPS): descriptive analysis of 500 patients from the International CAPS Registry. Autoimmun Rev 2016; 15 (12) 1120-1124
• 36 Cervera R, Rodríguez-Pintó I, Legault K, Erkan D. 16th International Congress on Antiphospholipid Antibodies Task Force report on catastrophic antiphospholipid syndrome. Lupus 2020; 29 (12) 1594-1600
• 37 Legault K, Schunemann H, Hillis C. et al. McMaster RARE-Bestpractices clinical practice guideline on diagnosis and management of the catastrophic antiphospholipid syndrome. J Thromb Haemost 2018; 16 (08) 1656-1664
• 38 Rodríguez-Pintó I, Espinosa G, Erkan D, Shoenfeld Y, Cervera R. CAPS Registry Project Group. The effect of triple therapy on the mortality of catastrophic anti-phospholipid syndrome patients. Rheumatology (Oxford) 2018; 57 (07) 1264-1270
• 39 Jacobs L, Wauters N, Lablad Y, Morelle J, Taghavi M. Diagnosis and management of catastrophic antiphospholipid syndrome and the potential impact of the 2023 ACR/EULAR antiphospholipid syndrome classification criteria. Antibodies (Basel) 2024; 13 (01) 21
• 40 Asherson RA, Cervera R, Piette JC. et al. Catastrophic antiphospholipid syndrome. Clinical and laboratory features of 50 patients. Medicine (Baltimore) 1998; 77 (03) 195-207
• 41 Bucciarelli S, Espinosa G, Cervera R. et al; European Forum on Antiphospholipid Antibodies. Mortality in the catastrophic antiphospholipid syndrome: causes of death and prognostic factors in a series of 250 patients. Arthritis Rheum 2006; 54 (08) 2568-2576
• 42 Erkan D, Asherson RA, Espinosa G. et al; Catastrophic Antiphospholipid Syndrome Registry Project Group. Long term outcome of catastrophic antiphospholipid syndrome survivors. Ann Rheum Dis 2003; 62 (06) 530-533
• 43 Greinacher A, Warkentin TE. Thrombotic anti-PF4 immune disorders: HIT, VITT, and beyond. Hematology (Am Soc Hematol Educ Program) 2023; 2023 (01) 1-10
• 44 Warkentin TE. Platelet-activating anti-PF4 disorders: an overview. Semin Hematol 2022; 59 (02) 59-71
• 45 Yang C, Wang I, Chitkara A, Swankutty J, Patel R, Kubba SV. Anti-PF4 antibodies and their relationship with COVID infection. Hematol Transfus Cell Ther 2024; 46 (04) 516-523
• 46 Warkentin TE, Greinacher A. Laboratory testing for heparin-induced thrombocytopenia and vaccine-induced immune thrombotic thrombocytopenia antibodies: a narrative review. Semin Thromb Hemost 2023; 49 (06) 621-633
• 47 Warkentin TE. Heparin-induced thrombocytopenia. Curr Opin Crit Care 2015; 21 (06) 576-585
• 48 Warkentin TE. Heparin-induced thrombocytopenia (and autoimmune heparin-induced thrombocytopenia): an illustrious review. Res Pract Thromb Haemost 2023; 7 (08) 102245
• 49 Liu Z, Li L, Zhang H. et al. Platelet factor 4(PF4) and its multiple roles in diseases. Blood Rev 2024; 64: 101155
• 50 Johnston I, Sarkar A, Hayes V. et al. Recognition of PF4-VWF complexes by heparin-induced thrombocytopenia antibodies contributes to thrombus propagation. Blood 2020; 135 (15) 1270-1280
• 51 Pishko AM, Cuker A. Diagnosing heparin-induced thrombocytopenia: the need for accuracy and speed. Int J Lab Hematol 2021; 43 (Suppl. 01) 96-102
• 52 Warkentin TE. Autoimmune heparin-induced thrombocytopenia. J Clin Med 2023; 12 (21) 6921
• 53 Greinacher A, Selleng K, Warkentin TE. Autoimmune heparin-induced thrombocytopenia. J Thromb Haemost 2017; 15 (11) 2099-2114
• 54 Warkentin TE, Greinacher A. Spontaneous HIT syndrome: knee replacement, infection, and parallels with vaccine-induced immune thrombotic thrombocytopenia. Thromb Res 2021; 204: 40-51
• 55 Cuker A, Arepally GM, Chong BH. et al. American Society of Hematology 2018 guidelines for management of venous thromboembolism: heparin-induced thrombocytopenia. Blood Adv 2018; 2 (22) 3360-3392
• 56 Warkentin TE, Anderson JA. How I treat patients with a history of heparin-induced thrombocytopenia. Blood 2016; 128 (03) 348-359
• 57 Franchini M, Liumbruno GM, Pezzo M. COVID-19 vaccine-associated immune thrombosis and thrombocytopenia (VITT): diagnostic and therapeutic recommendations for a new syndrome. Eur J Haematol 2021; 107 (02) 173-180
• 58 Johansen S, Laegreid IJ, Ernstsen SL. et al. Thrombosis and thrombocytopenia after HPV vaccination. J Thromb Haemost 2022; 20 (03) 700-704
• 59 Dabbiru VAS, Müller L, Schönborn L, Greinacher A. Vaccine-induced immune thrombocytopenia and thrombosis (VITT)-insights from clinical cases, in vitro studies and murine models. J Clin Med 2023; 12 (19) 6126
• 60 Salih F, Kohler S, Schönborn L, Thiele T, Greinacher A, Endres M. Early recognition and treatment of pre-VITT syndrome after adenoviral vector-based SARS-CoV-2 vaccination may prevent from thrombotic complications: review of published cases and clinical pathway. Eur Heart J Open 2022; 2 (03) oeac036
• 61 Roytenberg R, García-Sastre A, Li W. Vaccine-induced immune thrombotic thrombocytopenia: what do we know hitherto?. Front Med (Lausanne) 2023; 10: 1155727
• 62 Cines DB, Greinacher A. Vaccine-induced immune thrombotic thrombocytopenia. Blood 2023; 141 (14) 1659-1665
• 63 Greinacher A, Thiele T, Warkentin TE, Weisser K, Kyrle PA, Eichinger S. Thrombotic thrombocytopenia after ChAdOx1 nCov-19 vaccination. N Engl J Med 2021; 384 (22) 2092-2101
• 64 Favaloro EJ, Clifford J, Leitinger E. et al. Assessment of immunological anti-platelet factor 4 antibodies for vaccine-induced thrombotic thrombocytopenia (VITT) in a large Australian cohort: a multicenter study comprising 1284 patients. J Thromb Haemost 2022; 20 (12) 2896-2908
• 65 Schulman S, Arnold DM, Bradbury CA. et al; International Society on Thrombosis and Haemostasis. 2023 ISTH update of the 2022 ISTH guidelines for antithrombotic treatment in COVID-19. J Thromb Haemost 2024; 22 (06) 1779-1797
• 66 Pavord S, Hunt BJ, Horner D, Bewley S, Karpusheff J. Guideline Committee. Vaccine induced immune thrombocytopenia and thrombosis: summary of NICE guidance. BMJ 2021; 375 (2195) n2195
• 67 Gabarin N, Arnold DM, Nazy I, Warkentin TE. Treatment of vaccine-induced immune thrombotic thrombocytopenia (VITT). Semin Hematol 2022; 59 (02) 89-96
• 68 Gresele P, Marietta M, Ageno W. et al. Management of cerebral and splanchnic vein thrombosis associated with thrombocytopenia in subjects previously vaccinated with Vaxzevria (AstraZeneca): a position statement from the Italian Society for the Study of Haemostasis and Thrombosis (SISET). Blood Transfus 2021; 19 (04) 281-283
• 69 Rosove MH. Thrombotic microangiopathies. Semin Arthritis Rheum 2014; 43 (06) 797-805
• 70 George JN, Nester CM. Syndromes of thrombotic microangiopathy. N Engl J Med 2014; 371 (07) 654-666
• 71 Kappler S, Ronan-Bentle S, Graham A. Thrombotic microangiopathies (TTP, HUS, HELLP). Emerg Med Clin North Am 2014; 32 (03) 649-671
• 72 Moake JL. Thrombotic microangiopathies. N Engl J Med 2002; 347 (08) 589-600
• 73 Joly BS, Coppo P, Veyradier A. Thrombotic thrombocytopenic purpura. Blood 2017; 129 (21) 2836-2846
• 74 George JN. Thrombotic thrombocytopenic purpura: from 1972 to 2022 and beyond. Semin Thromb Hemost 2022; 48 (08) 926-936
• 75 Woods AI, Paiva J, Dos Santos C, Alberto MF, Sánchez-Luceros A. From the discovery of ADAMTS13 to current understanding of its role in health and disease. Semin Thromb Hemost 2023; 49 (03) 284-294
• 76 Tsai HM. Physiologic cleavage of von Willebrand factor by a plasma protease is dependent on its conformation and requires calcium ion. Blood 1996; 87 (10) 4235-4244
• 77 Shatzel JJ, Taylor JA. Syndromes of thrombotic microangiopathy. Med Clin North Am 2017; 101 (02) 395-415
• 78 Rock GA, Shumak KH, Buskard NA. et al; Canadian Apheresis Study Group. Comparison of plasma exchange with plasma infusion in the treatment of thrombotic thrombocytopenic purpura. N Engl J Med 1991; 325 (06) 393-397
• 79 Kremer Hovinga JA, Coppo P, Lämmle B, Moake JL, Miyata T, Vanhoorelbeke K. Thrombotic thrombocytopenic purpura. Nat Rev Dis Primers 2017; 3: 17020
• 80 Lämmle B, Vanhoorelbeke K, Kremer Hovinga JA, Knöbl P. 100 years of thrombotic thrombocytopenic purpura: a story of death and life. Hamostaseologie 2024; 44 (01) 59-73
• 81 Capecchi M, Gazzola G, Agosti P. et al. Treatment of immune-mediated thrombotic thrombocytopenic purpura without plasma exchange. Haematologica 2024; 109 (06) 2019-2023
• 82 Bendapudi PK, Foy BH, Mueller SB. et al. Recombinant ADAMTS13 for immune thrombotic thrombocytopenic purpura. N Engl J Med 2024; 390 (18) 1690-1698
• 83 Freedman SB, van de Kar NCAJ, Tarr PI. Shiga toxin-producing Escherichia coli and the hemolytic-uremic syndrome. N Engl J Med 2023; 389 (15) 1402-1414
• 84 Franchini M. Atypical hemolytic uremic syndrome: from diagnosis to treatment. Clin Chem Lab Med 2015; 53 (11) 1679-1688
• 85 Raina R, Krishnappa V, Blaha T. et al. Atypical hemolytic-uremic syndrome: an update on pathophysiology, diagnosis, and treatment. Ther Apher Dial 2019; 23 (01) 4-21
• 86 Legendre CM, Licht C, Muus P. et al. Terminal complement inhibitor eculizumab in atypical hemolytic-uremic syndrome. N Engl J Med 2013; 368 (23) 2169-2181
• 87 Yerigeri K, Kadatane S, Mongan K. et al. Atypical hemolytic-uremic syndrome: genetic basis, clinical manifestations, and a multidisciplinary approach to management. J Multidiscip Healthc 2023; 16: 2233-2249
• 88 Young JA, Pallas CR, Knovich MA. Transplant-associated thrombotic microangiopathy: theoretical considerations and a practical approach to an unrefined diagnosis. Bone Marrow Transplant 2021; 56 (08) 1805-1817
• 89 Klion AD. Approach to the patient with suspected hypereosinophilic syndrome. Hematology (Am Soc Hematol Educ Program) 2022; 2022 (01) 47-54
• 90 Shomali W, Gotlib J. World Health Organization and International Consensus Classification of eosinophilic disorders: 2024 update on diagnosis, risk stratification, and management. Am J Hematol 2024; 99 (05) 946-968
• 91 Zemleduch T, Czapla A, Kimla P, Kudliński B. Rare case of a young male presented with abdominal pain, solid colon tumors, and eosinophilia, followed by tremendous thromboembolic complications and eventually diagnosed with idiopathic hypereosinophilic syndrome. Case Rep Med 2022; 2022: 1424749
• 92 Li D, Xu L, Lin D, Jiang S, Feng S, Zhu L. Acute pulmonary embolism and deep vein thrombosis secondary to idiopathic hypereosinophilic syndrome. Respir Med Case Rep 2018; 25: 213-215
• 93 Su WQ, Fu YZ, Liu SY. et al. Eosinophilia complicated with venous thromboembolism: a case report. World J Clin Cases 2022; 10 (06) 1952-1960
• 94 Buyuktas D, Eskazan AE, Borekci S. et al. Hypereosinophilic syndrome associated with simultaneous intracardiac thrombi, cerebral thromboembolism and pulmonary embolism. Intern Med 2012; 51 (03) 309-313
• 95 Aukstuolis K, Cooper JJ, Altman K, Lang A, Ayars AG. Hypereosinophilic syndrome presenting as coagulopathy. Allergy Asthma Clin Immunol 2022; 18 (01) 25
• 96 Todd S, Hemmaway C, Nagy Z. Catastrophic thrombosis in idiopathic hypereosinophilic syndrome. Br J Haematol 2014; 165 (04) 425
• 97 Wallace KL, Elias MK, Butterfield CL, Weiler L. Hypereosinophilic syndrome and thrombosis: a retrospective review. J Allergy Clin Immunol 2013; 131 (Supplement): 441
• 98 Leiva O, Baker O, Jenkins A. et al. Association of thrombosis with hypereosinophilic syndrome in patients with genetic alterations. JAMA Netw Open 2021; 4 (08) e2119812
• 99 Cugno M, Marzano AV, Lorini M, Carbonelli V, Tedeschi A. Enhanced tissue factor expression by blood eosinophils from patients with hypereosinophilia: a possible link with thrombosis. PLoS One 2014; 9 (11) e111862
• 100 Wang JG, Mahmud SA, Thompson JA, Geng JG, Key NS, Slungaard A. The principal eosinophil peroxidase product, HOSCN, is a uniquely potent phagocyte oxidant inducer of endothelial cell tissue factor activity: a potential mechanism for thrombosis in eosinophilic inflammatory states. Blood 2006; 107 (02) 558-565
• 101 Marx C, Novotny J, Salbeck D. et al. Eosinophil-platelet interactions promote atherosclerosis and stabilize thrombosis with eosinophil extracellular traps. Blood 2019; 134 (21) 1859-1872
• 102 Nguyen L, Saha A, Kuykendall A, Zhang L. Clinical and therapeutic intervention of hypereosinophilia in the era of molecular diagnosis. Cancers (Basel) 2024; 16 (07) 1383
• 103 Rashidi A, Silverberg ML, Conkling PR, Fisher SI. Thrombosis in acute promyelocytic leukemia. Thromb Res 2013; 131 (04) 281-289
• 104 Gialeraki A, Valsami S, Pittaras T, Panayiotakopoulos G, Politou M. Oral contraceptives and HRT risk of thrombosis. Clin Appl Thromb Hemost 2018; 24 (02) 217-225
• 105 Hill A, Kelly RJ, Hillmen P. Thrombosis in paroxysmal nocturnal hemoglobinuria. Blood 2013; 121 (25) 4985-4996 , quiz 5105