Autoimmune Diseases Affecting Hemostasis: A Narrative Review
Abstract
:1. Introduction
2. A Brief Overview of Hemostasis
3. Autoimmune Disorders Leading to Bleeding
3.1. Acquired Hemophilia A
3.2. Other Acquired Bleeding Disorders Involving Clotting Factors
3.3. Acquired Von Willebrand Syndrome (AVWS)
3.4. Acquired Autoimmune Thrombocytopenia (ITP)
4. Autoimmune Disorders Leading to Thrombosis
4.1. Antiphospholipid Antibody Syndrome (APS)
4.2. Heparin Induced Thrombotic Thrombocytopenia (HITT), and HITT-like Syndromes (Including Vaccine Associated (Immune) Thrombotic Thrombocytopenia (VITT))
4.3. Acquired Immune Thrombotic Thrombocytopenia
5. Autoantibodies Interfering with Hemostasis in COVID-19 and after Vaccination against COVID-19
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Tiede, A.; Werwitzke, S.; Scharf, R.E. Laboratory diagnosis of acquired hemophilia A: Limitations, consequences, and challenges. Semin. Thromb. Hemost. 2014, 40, 803–811. [Google Scholar] [CrossRef] [PubMed]
- Teitel, J.; Ackery, A.D. Just the facts: How do I recognize, diagnose and treat acquired (autoimmune) hemophilia? Can. J. Emerg. Med. 2022, 24, 477–479. [Google Scholar] [CrossRef] [PubMed]
- Tay, L.; Duncan, E.; Singhal, D.; Al-Qunfoidi, R.; Coghlan, D.; Jaksic, W.; Szabo, F.; McRae, S.; Lloyd, J. Twelve years of experience of acquired hemophilia A: Trials and tribulations in South Australia. Semin. Thromb. Hemost. 2009, 35, 769–777. [Google Scholar] [CrossRef] [PubMed]
- Tang, Q.; Liao, J.; Xie, X. Acquired Hemophilia Associated with Rheumatic Diseases: A Case-Based Systematic Review. J. Inflamm. Res. 2022, 15, 4385–4393. [Google Scholar] [CrossRef]
- Webert, K.E. Acquired hemophilia A. Semin. Thromb. Hemost. 2012, 38, 735–741. [Google Scholar] [CrossRef] [PubMed]
- Coppola, A.; Favaloro, E.J.; Tufano, A.; Di Minno, M.N.; Cerbone, A.M.; Franchini, M. Acquired inhibitors of coagulation factors: Part I-acquired hemophilia A. Semin. Thromb. Hemost. 2012, 38, 433–446. [Google Scholar] [CrossRef]
- Federici, A.B.; Budde, U.; Castaman, G.; Rand, J.H.; Tiede, A. Current diagnostic and therapeutic approaches to patients with acquired von Willebrand syndrome: A 2013 update. Semin. Thromb. Hemost. 2013, 39, 191–201. [Google Scholar] [CrossRef]
- Nicol, C.; Pan-Petesch, B.; Ianotto, J.C. Acquired von Willebrand syndrome and lymphoid neoplasms: A review of malignancy management, and propositions of practical recommendations. Haemophilia 2022, 28, 938–949. [Google Scholar] [CrossRef]
- Stempel, J.M.; Podoltsev, N.A.; Zeidan, A.M.; Lee, A.I.; Shallis, R.M. Concealed by the convenient: Acquired von Willebrand syndrome in myeloproliferative neoplasm requires a thorough evaluation. Ann. Hematol. 2022, 101, 2559–2561. [Google Scholar] [CrossRef]
- Janjetovic, S.; Rolling, C.C.; Budde, U.; Schneppenhem, S.; Schafhausen, P.; Peters, M.C.; Bokemeyer, C.; Holstein, K.; Langer, F. Evaluation of different diagnostic tools for detection of acquired von Willebrand syndrome in patients with polycythemia vera or essential thrombocythemia. Thromb. Res. 2022, 218, 35–43. [Google Scholar] [CrossRef] [PubMed]
- Ghariani, I.; Braham, N.; Veyradier, A.; Bekir, L. Acquired von Willebrand syndrome: Five cases report and literature review. Thromb. Res. 2022, 218, 145–150. [Google Scholar] [CrossRef] [PubMed]
- Favaloro, E.J.; Wong, R.C.W. The antiphospholipid syndrome: A large elephant with many parts or an elusive chameleon disguised by many colours? Autoimmun. Highlights 2010, 1, 5–14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vandevelde, A.; Devreese, K.M.J. Laboratory Diagnosis of Antiphospholipid Syndrome: Insights and Hindrances. J. Clin. Med. 2022, 11, 2164. [Google Scholar] [CrossRef]
- Arreola-Diaz, R.; Majluf-Cruz, A.; Sanchez-Torres, L.E.; Hernandez-Juarez, J. The Pathophysiology of The Antiphospholipid Syndrome: A Perspective from The Blood Coagulation System. Clin. Appl. Thromb. Hemost. 2022, 28, 10760296221088576. [Google Scholar] [CrossRef]
- Killian, M.; van Mens, T.E. Risk of Thrombosis, Pregnancy Morbidity or Death in Antiphospholipid Syndrome. Front. Cardiovasc. Med. 2022, 9, 852777. [Google Scholar] [CrossRef]
- Hvas, A.M.; Favaloro, E.J.; Hellfritzsch, M. Heparin-induced thrombocytopenia: Pathophysiology, diagnosis and treatment. Expert Rev. Hematol. 2021, 14, 335–346. [Google Scholar] [CrossRef] [PubMed]
- Favaloro, E.J.; Mohammed, S.; Donikian, D.; Kondo, M.; Duncan, E.; Yacoub, O.; Zebeljan, D.; Ng, S.; Malan, E.; Yuen, A.; et al. A multicentre assessment of contemporary laboratory assays for heparin induced thrombocytopenia. Pathology 2021, 53, 247–256. [Google Scholar] [CrossRef] [PubMed]
- Lippi, G.; Favaloro, E.J. Cerebral Venous Thrombosis Developing after COVID-19 Vaccination: VITT, VATT, TTS, and More. Semin. Thromb. Hemost. 2022, 48, 8–14. [Google Scholar] [CrossRef]
- Thachil, J. COVID-19 Vaccine-Induced Immune Thrombosis with Thrombocytopenia (VITT) and the Shades of Grey in Thrombus Formation. Semin. Thromb. Hemost. 2022, 48, 15–18. [Google Scholar] [CrossRef]
- Favaloro, E.J.; Pasalic, L.; Lippi, G. Review and evolution of guidelines for diagnosis of COVID-19 vaccine induced thrombotic thrombocytopenia (VITT). Clin. Chem. Lab. Med. 2022, 60, 7–17. [Google Scholar] [CrossRef] [PubMed]
- Lippi, G.; Adcock, D.; Favaloro, E.J. Understanding the “philosophy” of laboratory hemostasis. Diagnosis 2019, 6, 223–226. [Google Scholar] [CrossRef]
- Lippi, G.; Favaloro, E.J. Hemostasis practice: State-of-the-art. J. Lab. Precis. Med. 2018, 3, 67. [Google Scholar] [CrossRef]
- Lippi, G.; Favaloro, E.J. Laboratory hemostasis: From biology to the bench. Clin. Chem. Lab. Med. 2018, 56, 1035–1045. [Google Scholar] [CrossRef]
- Margaglione, M.; Intrieri, M. Genetic Risk Factors and Inhibitor Development in Hemophilia: What Is Known and Searching for the Unknown. Semin. Thromb. Hemost. 2018, 44, 509–516. [Google Scholar] [CrossRef] [PubMed]
- Delignat, S.; Rayes, J.; Russick, J.; Kaveri, S.V.; Lacroix-Desmazes, S.; ABIRISK consortium. Inhibitor Formation in Congenital Hemophilia A: An Immunological Perspective. Semin. Thromb. Hemost. 2018, 44, 517–530. [Google Scholar] [CrossRef]
- Abdi, A.; Linari, S.; Pieri, L.; Voorberg, J.; Fijnvandraat, K.; Castaman, G. Inhibitors in Nonsevere Hemophilia A: What Is Known and Searching for the Unknown. Semin. Thromb. Hemost. 2018, 44, 568–577. [Google Scholar] [CrossRef]
- Santoro, C.; Quintavalle, G.; Castaman, G.; Baldacci, E.; Ferretti, A.; Riccardi, F.; Tagliaferri, A. Inhibitors in Hemophilia B. Semin. Thromb. Hemost. 2018, 44, 578–589. [Google Scholar] [CrossRef] [PubMed]
- Kershaw, G. Detection and Measurement of Factor Inhibitors. Methods Mol. Biol. 2017, 1646, 295–304. [Google Scholar] [CrossRef] [PubMed]
- Franchini, M.; Cappello, E.; Valdiserra, G.; Bonaso, M.; Moretti, U.; Focosi, D.; Tuccori, M. Investigating a Signal of Acquired Hemophilia Associated with COVID-19 Vaccination: A Systematic Case Review. Semin. Thromb. Hemost. 2022; online ahead of print. [Google Scholar] [CrossRef] [PubMed]
- Happaerts, M.; Vanassche, T. Acquired hemophilia following COVID-19 vaccination: Case report and review of literature. Res. Pract. Thromb. Haemost. 2022, 6, e12785. [Google Scholar] [CrossRef] [PubMed]
- Hosoi, H.; Tane, M.; Kosako, H.; Ibe, M.; Takeyama, M.; Murata, S.; Mushino, T.; Sonoki, T. Acute-type acquired hemophilia A after COVID-19 mRNA vaccine administration: A new disease entity? J. Autoimmun. 2022, 133, 102915. [Google Scholar] [CrossRef] [PubMed]
- Melmed, A.; Kovoor, A.; Flippo, K. Acquired hemophilia A after vaccination against SARS-CoV-2 with the mRNA-1273 (Moderna) vaccine. Bayl. Univ. Med. Cent. Proc. 2022, 35, 683–685. [Google Scholar] [CrossRef] [PubMed]
- Al Hennawi, H.; Al Masri, M.K.; Bakir, M.; Albarazi, M.; Jazaeri, F.; Almasri, T.N.; Shoura, S.J.; Barakeh, A.R.R.; Taftafa, A.; Khan, M.K.; et al. Acquired Hemophilia A Post-COVID-19 Vaccination: A Case Report and Review. Cureus 2022, 14, e21909. [Google Scholar] [CrossRef] [PubMed]
- Franchini, M.; Lippi, G.; Favaloro, E.J. Acquired inhibitors of coagulation factors: Part II. Semin. Thromb. Hemost. 2012, 38, 447–453. [Google Scholar] [CrossRef]
- Ichinose, A.; Osaki, T.; Souri, M. A Review of Coagulation Abnormalities of Autoimmune Acquired Factor V Deficiency with a Focus on Japan. Semin. Thromb. Hemost. 2022, 48, 206–218. [Google Scholar] [CrossRef]
- Sridharan, M.; Fylling, K.A.; Ashrani, A.A.; Chen, D.; Marshall, A.L.; Hook, C.C.; Cardel, L.K.; Nichols, W.L.; Pruthi, R.K. Clinical and laboratory diagnosis of autoimmune factor V inhibitors: A single institutional experience. Thromb. Res. 2018, 171, 14–21. [Google Scholar] [CrossRef]
- Imashuku, S.; Hasegawa, T.; Kubo, K.; Nakato, M.; Shima, M. Anti-Factor V inhibitor in patients with autoimmune diseases: Case report and literature review. Int. Med. Case Rep. J. 2011, 4, 31–34. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Favaloro, E.J.; Posen, J.; Ramakrishna, R.; Soltani, S.; McRae, S.; Just, S.; Aboud, M.; Low, J.; Gemmell, R.; Kershaw, G.; et al. Factor V inhibitors: Rare or not so uncommon? A multi-laboratory investigation. Blood Coagul. Fibrinolysis 2004, 15, 637–647. [Google Scholar] [CrossRef]
- Brenner, B.; Kuperman, A.A.; Watzka, M.; Oldenburg, J. Vitamin K-dependent coagulation factors deficiency. Semin. Thromb. Hemost. 2009, 35, 439–446. [Google Scholar] [CrossRef]
- Wada, H.; Usui, M.; Sakuragawa, N. Hemostatic abnormalities and liver diseases. Semin. Thromb. Hemost. 2008, 34, 772–778. [Google Scholar] [CrossRef]
- Lee, G.; Duan-Porter, W.; Metjian, A.D. Acquired, non-amyloid related factor X deficiency: Review of the literature. Haemophilia 2012, 18, 655–663. [Google Scholar] [CrossRef] [PubMed]
- Greipp, P.R.; Kyle, R.A.; Bowie, E.J. Factor-X deficiency in amyloidosis: A critical review. Am. J. Hematol. 1981, 11, 443–450. [Google Scholar] [CrossRef]
- Duga, S.; Salomon, O. Factor XI Deficiency. Semin. Thromb. Hemost. 2009, 35, 416–425. [Google Scholar] [CrossRef] [PubMed]
- Ichinose, A.; Japanese Collaborative Research Group (JCRG) on AH13 Hemorrhagic Acquired Coagulopathies. Inhibitors of Factor XIII/13 in older patients. Semin. Thromb. Hemost. 2014, 40, 704–711. [Google Scholar] [CrossRef]
- Ichinose, A. Hemorrhagic acquired factor XIII (13) deficiency and acquired hemorrhaphilia 13 revisited. Semin. Thromb. Hemost. 2011, 37, 382–388. [Google Scholar] [CrossRef]
- Muszbek, L.; Katona, É. Diagnosis and Management of Congenital and Acquired FXIII Deficiencies. Semin. Thromb. Hemost. 2016, 42, 429–439. [Google Scholar] [CrossRef]
- Roth, N.; Heidel, C.; Xu, C.; Hubauer, U.; Wallner, S.; Meindl, C.; Holzamer, A.; Hilker, M.; Creutzenberg, M.; Sossalla, S.; et al. The impact of bicuspid aortic valve morphology on von Willebrand factor function in patients with severe aortic stenosis and its change after TAVI. Clin. Res. Cardiol. 2022, 111, 1348–1357. [Google Scholar] [CrossRef]
- Virk, Z.M.; Song, A.B.; Badran, Y.R.; Al-Samkari, H. Systemic bevacizumab as salvage therapy for persistent severe bleeding and anemia in heyde syndrome following aortic valve replacement. J. Thromb. Thrombolysis 2022, 54, 255–259. [Google Scholar] [CrossRef] [PubMed]
- Theis, S.R.; Turner, S.D. Heyde Syndrome. In StatPearls [Internet]; StatPearls Publishing: Treasure Island, FL, USA, 2022. [Google Scholar]
- Kalbhenn, J.; Zieger, B. Bleeding During Veno-Venous ECMO: Prevention and Treatment. Front. Med. 2022, 9, 879579. [Google Scholar] [CrossRef]
- Arias, K.; Sun, W.; Wang, S.; Sorensen, E.N.; Feller, E.; Kaczorowski, D.; Griffith, B.; Wu, Z.J. Acquired platelet defects are responsible for nonsurgical bleeding in left ventricular assist device recipients. Artif. Organs 2022, 46, 2244–2256. [Google Scholar] [CrossRef] [PubMed]
- Owari, M.; Harada-Shirado, K.; Togawa, R.; Fukatsu, M.; Sato, Y.; Fukuchi, K.; Endo, M.; Takahashi, H.; Kimura, S.; Osaki, T.; et al. Acquired von Willebrand Syndrome in a Patient with Multiple Comorbidities, Including MALT Lymphoma with IgA Monoclonal Gammopathy and Hyperviscosity Syndrome. Int. Med. 2022, 9815–9822. [Google Scholar] [CrossRef] [PubMed]
- Ichinose, A.; Osaki, T.; Souri, M.; Favaloro, E.J. A Review of Autoimmune Acquired von Willebrand Factor Deficiency in Japan. Semin. Thromb. Hemost. 2022, 48, 911–925. [Google Scholar] [CrossRef]
- Al-Samkari, H.; Kuter, D.J. Immune Thrombocytopenia in Adults: Modern Approaches to Diagnosis and Treatment. Semin. Thromb. Hemost. 2020, 46, 275–288. [Google Scholar] [CrossRef]
- Cuker, A.; Prak, E.T.; Cines, D.B. Can immune thrombocytopenia be cured with medical therapy? Semin. Thromb. Hemost. 2015, 41, 395–404. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Provan, D.; Arnold, D.M.; Bussel, J.B.; Chong, B.H.; Cooper, N.; Gernsheimer, T.; Ghanima, W.; Godeau, B.; González-López, T.J.; Grainger, J.; et al. Updated international consensus report on the investigation and management of primary immune thrombocytopenia. Blood Adv. 2019, 3, 3780–3817. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Miyakis, S.; Lockshin, M.D.; Atsumi, T.; Branch, D.W.; Brey, R.L.; Cervera, R.; Derksen, R.H.; De Groot, P.G.; Koike, T.; Meroni, P.L.; et al. International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J. Thromb. Haemost. 2006, 4, 295–306. [Google Scholar] [CrossRef] [PubMed]
- Devreese, K.M.J.; de Groot, P.G.; de Laat, B.; Erkan, D.; Favaloro, E.J.; Mackie, I.; Martinuzzo, M.; Ortel, T.L.; Pengo, V.; Rand, J.H.; et al. Guidance from the Scientific and Standardization Committee for lupus anticoagulant/antiphospholipid antibodies of the International Society on Thrombosis and Haemostasis: Update of the guidelines for lupus anticoagulant detection and interpretation. J. Thromb. Haemost. 2020, 18, 2828–2839. [Google Scholar] [CrossRef]
- Devreese, K.M.J. Solid Phase Assays for Antiphospholipid Antibodies. Semin. Thromb. Hemost. 2022, 48, 661–671. [Google Scholar] [CrossRef]
- Moore, G.W. Testing for Lupus Anticoagulants. Semin. Thromb. Hemost. 2022, 48, 643–660. [Google Scholar] [CrossRef]
- Favaloro, E.J.; Pasalic, L. Lupus anticoagulant testing during anticoagulation, including direct oral anticoagulants. Res. Pract. Thromb. Haemost. 2022, 6, e12676. [Google Scholar] [CrossRef]
- Ieko, M.; Yoshida, M.; Naito, S.; Ohmura, K.; Takahashi, N. Lupus anticoagulant-hypoprothrombinemia syndrome and similar diseases: Experiences at a single center in Japan. Int. J. Hematol. 2019, 110, 197–204. [Google Scholar] [CrossRef]
- Warkentin, T.E. Platelet-activating anti-PF4 disorders: An overview. Semin. Hematol. 2022, 59, 59–71. [Google Scholar] [CrossRef]
- Warkentin, T.E.; Greinacher, A. Laboratory Testing for HIT and VITT antibodies: A Narrative Review. Semin. Thromb. Hemost. 2023; in press. [Google Scholar]
- Favaloro, E.J.; Pasalic, L.; Lippi, G. Antibodies against Platelet Factor 4 and Their Associated Pathologies: From HIT/HITT to Spontaneous HIT-Like Syndrome, to COVID-19, to VITT/TTS. Antibodies 2022, 11, 7. [Google Scholar] [CrossRef] [PubMed]
- Favaloro, E.J.; Pasalic, L.; Henry, B.; Lippi, G. Laboratory testing for platelet factor 4 antibodies: Differential utility for diagnosis/exclusion of heparin induced thrombocytopenia versus suspected vaccine induced thrombotic thrombocytopenia. Pathology 2022, 54, 254–261. [Google Scholar] [CrossRef] [PubMed]
- Lee, C.S.M.; Liang, H.P.H.; Connor, D.E.; Dey, A.; Tohidi-Esfahani, I.; Campbell, H.; Whittaker, S.; Capraro, D.; Favaloro, E.J.; Donikian, D.; et al. A novel flow cytometry procoagulant assay for diagnosis of vaccine-induced immune thrombotic thrombocytopenia. Blood Adv. 2022, 6, 3494–3506. [Google Scholar] [CrossRef] [PubMed]
- Favaloro, E.J.; Clifford, J.; Leitinger, E.; Parker, M.; Sung, P.; Chunilal, S.; Tran, H.; Kershaw, G.; Fu, S.; Passam, F.; et al. Assessment of immunological anti-platelet factor 4 antibodies for vaccine-induced thrombotic thrombocytopenia (VITT) in a large Australian cohort: A multicentre study comprising 1284 patients. J. Thromb. Haemost. 2022, 20, 2896–2908. [Google Scholar] [CrossRef]
- Favaloro, E.J. Laboratory testing for suspected COVID-19 vaccine-induced (immune) thrombotic thrombocytopenia. Int. J. Lab. Hematol. 2021, 43, 559–570. [Google Scholar] [CrossRef]
- Knöbl, P. Inherited and acquired thrombotic thrombocytopenic purpura (TTP) in adults. Semin. Thromb. Hemost. 2014, 40, 493–502. [Google Scholar] [CrossRef] [PubMed]
- Fogerty, A.E. Thrombocytopenia in Pregnancy: Approach to Diagnosis and Management. Semin. Thromb. Hemost. 2020, 46, 256–263. [Google Scholar] [CrossRef] [PubMed]
- Blennerhassett, R.; Curnow, J.; Pasalic, L. Immune-Mediated Thrombotic Thrombocytopenic Purpura: A Narrative Review of Diagnosis and Treatment in Adults. Semin. Thromb. Hemost. 2020, 46, 289–301. [Google Scholar] [CrossRef] [PubMed]
- Favaloro, E.J.; Pasalic, L.; Henry, B.; Lippi, G. Laboratory testing for ADAMTS13: Utility for TTP diagnosis/exclusion and beyond. Am. J. Hematol. 2021, 96, 1049–1055. [Google Scholar] [CrossRef]
- Favaloro, E.J.; Mohammed, S.; Chapman, K.; Swanepoel, P.; Zebeljan, D.; Sefhore, O.; Malan, E.; Clifford, J.; Yuen, A.; Donikian, D.; et al. A multicentre laboratory assessment of a new automated chemiluminescent assay for ADAMTS13 activity. J. Thromb. Haemost. 2021, 19, 417–428. [Google Scholar] [CrossRef]
- Favaloro, E.J.; Henry, B.M.; Lippi, G. Is Lupus Anticoagulant a Significant Feature of COVID-19? A Critical Appraisal of the Literature. Semin. Thromb. Hemost. 2022, 48, 55–71. [Google Scholar] [CrossRef] [PubMed]
- Favaloro, E.J.; Henry, B.M.; Lippi, G. COVID-19 and Antiphospholipid Antibodies: Time for a Reality Check? Semin. Thromb. Hemost. 2022, 48, 72–92. [Google Scholar] [CrossRef] [PubMed]
- Serrano, M.; Espinosa, G.; Serrano, A.; Cervera, R. COVID-19 and the antiphospholipid syndrome. Autoimmun. Rev. 2022, 21, 103206. [Google Scholar] [CrossRef]
- Ortega-Paz, L.; Talasaz, A.H.; Sadeghipour, P.; Potpara, T.S.; Aronow, H.D.; Jara-Palomares, L.; Sholzberg, M.; Angiolillo, D.J.; Lip, G.Y.H.; Bikdeli, B. COVID-19-Associated Pulmonary Embolism: Review of the Pathophysiology, Epidemiology, Prevention, Diagnosis, and Treatment. Semin. Thromb. Hemost. 2022; Epub ahead of print. [Google Scholar] [CrossRef]
- Candeloro, M.; Schulman, S. Arterial Thrombotic Events in Hospitalized COVID-19 Patients: A Short Review and Meta-Analysis. Semin. Thromb. Hemost. 2022; Epub ahead of print. [Google Scholar] [CrossRef] [PubMed]
- Fan, B.E.; Cheung, C. Post COVID-19 Arterial Thromboembolism: A Clear and Present Danger. Semin. Thromb. Hemost. 2022, 48, 112–114. [Google Scholar] [CrossRef]
- Aamodt, A.H.; Skattør, T.H. Cerebral Venous Thrombosis. Semin. Thromb. Hemost. 2022, 48, 309–317. [Google Scholar] [CrossRef] [PubMed]
- Lippi, G.; Favaloro, E.J. What We Know (and Do not Know) Regarding the Pathogenesis of Pulmonary Thrombosis in COVID-19. Semin. Thromb. Hemost. 2022; Epub ahead of print. [Google Scholar] [CrossRef] [PubMed]
- Cuker, A. The Case for Therapeutic-Intensity Anticoagulation in Patients with COVID-19-Associated Moderate Illness. Semin. Thromb. Hemost. 2022; Epub ahead of print. [Google Scholar] [CrossRef] [PubMed]
- Lippi, G.; Favaloro, E.J. Strength of Anticoagulation in Moderate to Severe COVID-19 Illness: In Medio Stat Virtus? Semin. Thromb. Hemost. 2022; Epub ahead of print. [Google Scholar] [CrossRef]
- Parisi, R.; Costanzo, S.; Di Castelnuovo, A.; de Gaetano, G.; Donati, M.B.; Iacoviello, L. Different Anticoagulant Regimens, Mortality, and Bleeding in Hospitalized Patients with COVID-19: A Systematic Review and an Updated Meta-Analysis. Semin. Thromb. Hemost. 2021, 47, 372–391. [Google Scholar] [CrossRef]
- Hashemi, A.; Madhavan, M.V.; Bikdeli, B. Pharmacotherapy for Prevention and Management of Thrombosis in COVID-19. Semin. Thromb. Hemost. 2020, 46, 789–795. [Google Scholar] [CrossRef]
- Favaloro, E.J.; Gilmore, G.; Arunachalam, S.; Mohammed, S.; Baker, R. Neutralising rivaroxaban induced interference in laboratory testing for lupus anticoagulant (LA): A comparative study using DOAC Stop and andexanet alfa. Thromb. Res. 2019, 180, 10–19. [Google Scholar] [CrossRef]
- Gendron, N.; Dragon-Durey, M.A.; Chocron, R.; Darnige, L.; Jourdi, G.; Philippe, A.; Chenevier-Gobeaux, C.; Hadjadj, J.; Duchemin, J.; Khider, L.; et al. Lupus Anticoagulant Single Positivity During the Acute Phase of COVID-19 Is Not Associated with Venous Thromboembolism or In-Hospital Mortality. Arthritis Rheumatol. 2021, 73, 1976–1985. [Google Scholar] [CrossRef] [PubMed]
- Espinosa, G.; Zamora-Martínez, C.; Pérez-Isidro, A.; Neto, D.; Bravo-Gallego, L.Y.; Prieto-González, S.; Viñas, O.; Moreno-Castaño, A.B.; Ruiz-Ortiz, E.; Cervera, R. Persistent Antiphospholipid Antibodies Are Not Associated with Worse Clinical Outcomes in a Prospective Cohort of Hospitalised Patients with SARS-CoV-2 Infection. Front. Immunol. 2022, 13, 911979. [Google Scholar] [CrossRef]
- Favaloro, E.J.; Henry, B.M.; Lippi, G. The complicated relationships of heparin-induced thrombocytopenia and platelet factor 4 antibodies with COVID-19. Int. J. Lab. Hematol. 2021, 43, 547–558. [Google Scholar] [CrossRef] [PubMed]
- Carnevale, S.; Giovanetti, M.; Benvenuto, D.; Ciccozzi, M.; Broccolo, F. Is Molecular Mimicry between hPF4 and SARS-CoV-2 Spike Protein a Potential Basis for Autoimmune Responses in Vaccinated and Naturally Infected Patients? Semin. Thromb. Hemost. 2022; Epub ahead of print. [Google Scholar] [CrossRef]
- Franchini, M.; Glingani, C.; De Donno, G.; Casari, S.; Caruso, B.; Terenziani, I.; Perotti, C.; Del Fante, C.; Sartori, F.; Pagani, M. The first case of acquired hemophilia A associated with SARS-CoV-2 infection. Am. J. Hematol. 2020, 95, E197–E198. [Google Scholar] [CrossRef]
- Chiurazzi, F.; Tufano, A.; Esposito, M.; D’Agostino, F.; Casoria, A.; Capasso, F.; Minno, G.D. Acquired Factor V Inhibitor after Coronavirus Disease 2019 (COVID-19). Semin. Thromb. Hemost. 2022, 48, 124–126. [Google Scholar] [CrossRef] [PubMed]
- Christensen, B.; Favaloro, E.J.; Lippi, G.; Van Cott, E.M. Hematology Laboratory Abnormalities in Patients with Coronavirus Disease 2019 (COVID-19). Semin. Thromb. Hemost. 2020, 46, 845–849. [Google Scholar] [CrossRef]
- Vadasz, Z.; Brenner, B.; Toubi, E. Immune-Mediated Coagulopathy in COVID-19 Infection. Semin. Thromb. Hemost. 2020, 46, 838–840. [Google Scholar] [CrossRef]
- Lippi, G.; Sanchis-Gomar, F.; Favaloro, E.J.; Lavie, C.J.; Henry, B.M. Coronavirus Disease 2019-Associated Coagulopathy. Mayo Clin. Proc. 2021, 96, 203–217. [Google Scholar] [CrossRef]
- Rivera-Correa, J.; Rodriguez, A. Autoantibodies during infectious diseases: Lessons from malaria applied to COVID-19 and other infections. Front. Immunol. 2022, 13, 938011. [Google Scholar] [CrossRef] [PubMed]
- Vahabi, M.; Ghazanfari, T.; Sepehrnia, S. Molecular mimicry, hyperactive immune system, and SARS-COV-2 are three prerequisites of the autoimmune disease triangle following COVID-19 infection. Int. Immunopharmacol. 2022, 112, 109183. [Google Scholar] [CrossRef]
- Boehm, B.A.; Packer, C.D. Persistent Relapsing Immune Thrombocytopenia Following COVID-19 Infection. Cureus 2022, 14, e27133. [Google Scholar] [CrossRef]
- Santhosh, S.; Malik, B.; Kalantary, A.; Kunadi, A. Immune Thrombocytopenic Purpura (ITP) Following Natural COVID-19 Infection. Cureus 2022, 14, e26582. [Google Scholar] [CrossRef] [PubMed]
- Alharbi, M.G.; Alanazi, N.; Yousef, A.; Alanazi, N.; Alotaibi, B.; Aljurf, M.; El Fakih, R. COVID-19 associated with immune thrombocytopenia: A systematic review and meta-analysis. Expert Rev. Hematol. 2022, 15, 157–166. [Google Scholar] [CrossRef]
- Fang, F.; Tse, B.; Pavenski, K. Relapse of immune thrombotic thrombocytopenic purpura (iTTP) possibly triggered by COVID-19 vaccination and/or concurrent COVID-19 infection. BMJ Case Rep. 2022, 15, e247524. [Google Scholar] [CrossRef] [PubMed]
- Chaudhary, H.; Nasir, U.; Syed, K.; Labra, M.; Reggio, C.; Aziz, A.; Shah, P.; Reddy, R.; Sangha, N. COVID-19-Associated Thrombotic Thrombocytopenic Purpura: A Case Report and Systematic Review. Hematol. Rep. 2022, 14, 253–260. [Google Scholar] [CrossRef]
- Favaloro, E.J.; Henry, B.M.; Lippi, G. Increased VWF and Decreased ADAMTS-13 in COVID-19: Creating a Milieu for (Micro)Thrombosis. Semin. Thromb. Hemost. 2021, 47, 400–418. [Google Scholar] [CrossRef]
- Favaloro, E.J.; Henry, B.M.; Lippi, G. VWF and ADAMTS13 in COVID-19 and beyond: A question of balance. EMJ Hematol. 2021, 9, 55–68. [Google Scholar]
- Henry, B.M.; Benoit, S.W.; de Oliveira, M.H.S.; Lippi, G.; Favaloro, E.J.; Benoit, J.L. ADAMTS13 activity to von Willebrand factor antigen ratio predicts acute kidney injury in patients with COVID-19: Evidence of SARS-CoV-2 induced secondary thrombotic microangiopathy. Int. J. Lab. Hematol. 2021, 43, 129–136. [Google Scholar] [CrossRef] [PubMed]
- Al-Allaf, A.W.; Neethu, M.; Al-Allaf, Y. A Case Series and Literature Review of the Association of COVID-19 Vaccination with Autoimmune Diseases: Causality or Chance? Cureus 2022, 14, e28677. [Google Scholar] [CrossRef] [PubMed]
- Saluja, P.; Amisha, F.; Gautam, N.; Goraya, H. A Systematic Review of Reported Cases of Immune Thrombocytopenia after COVID-19 Vaccination. Vaccines 2022, 10, 1444. [Google Scholar] [CrossRef] [PubMed]
- Sharma, K.; Patel, S.; Patel, Z.; Patel, K.B.; Shah, D.B.; Doshi, J.; Chokshi, P.; Sharma, C.; Amdani, M.M.; Parabtani, A.; et al. Immune Thrombocytopenia in Previously Healthy Individuals Following SARS-CoV-2 Vaccination (COVID-19 Immunization): A Descriptive Research of 70 Instances with a Focus on Biomarkers, Predictive Outcomes, and Consequences. Cureus 2022, 14, e26480. [Google Scholar] [CrossRef]
- Ben Saida, I.; Maatouk, I.; Toumi, R.; Bouslama, E.; Ben Ismail, H.; Ben Salem, C.; Boussarsar, M. Acquired Thrombotic Thrombocytopenic Purpura Following Inactivated COVID-19 Vaccines: Two Case Reports and a Short Literature Review. Vaccines 2022, 10, 1012. [Google Scholar] [CrossRef]
- Al-Beltagi, M.; Saeed, N.K.; Bediwy, A.S. COVID-19 disease and autoimmune disorders: A mutual pathway. World J. Methodol. 2022, 12, 200–223. [Google Scholar] [CrossRef]
- Bitzogli, K.; Jahaj, E.; Bakasis, A.D.; Kapsogeorgou, E.K.; Goules, A.V.; Stergiou, I.; Pezoulas, V.; Antoniadou, C.; Skendros, P.; Ritis, K.; et al. Incidence of autoantibodies related to systemic autoimmunity in patients with severe COVID-19 admitted to the intensive care unit. Clin. Exp. Rheumatol. 2022. [Google Scholar] [CrossRef] [PubMed]
- Mahroum, N.; Lavine, N.; Ohayon, A.; Seida, R.; Alwani, A.; Alrais, M.; Zoubi, M.; Bragazzi, N.L. COVID-19 Vaccination and the Rate of Immune and Autoimmune Adverse Events Following Immunization: Insights from a Narrative Literature Review. Front. Immunol. 2022, 13, 872683. [Google Scholar] [CrossRef] [PubMed]
‘Procoagulant’ | ‘Anticoagulant’ |
---|---|
Platelets | Protein C |
Clotting factors (fibrinogen [I], II, V, VII, VIII, IX, X, XI) | Protein S Antithrombin |
Factor XIII | Tissue-Factor Pathway Inhibitor |
Thrombin (activated FII) | ADAMTS13 |
von Willebrand factor (VWF) | Endothelial cells |
Factor V mutations (e.g., Leiden) | Heparin-like molecules |
Phospholipids, CaCl2 | |
ADP, ATP |
Conditions Associated with Bleeding | Conditions Associated with Thrombosis |
---|---|
Acquired hemophilia A (i.e., autoantibodies against FVIII) | Antiphospholipid (antibody) syndrome (APS) |
Autoantibodies against other coagulation proteins | Heparin induced thrombotic thrombocytopenia (HITT) |
Acquired von Willebrand syndrome (AVWS; only a proportion of AVWS are autoimmune related) | Autoimmune thrombotic thrombocytopenia (HIT-like) |
Acquired autoimmune thrombocytopenia (ITP) | Vaccine induced (immune) thrombotic thrombocytopenia (VITT) |
Acquired autoimmune thrombotic thrombocytopenia (iTTP) |
Reported Autoantibodies | Association with Derangement of Hemostasis |
---|---|
Antiphospholipid antibodies (aPL) | Antiphospholipid (antibody) syndrome (APS) (thrombosis) |
Autoantibodies against platelet factor 4 (PF4) | Heparin induced thrombotic thrombocytopenia (HITT) (thrombosis) Autoimmune thrombotic thrombocytopenia (HIT-like) (thrombosis) Vaccine induced (immune) thrombotic thrombocytopenia (VITT) (thrombosis) |
Autoantibodies against ADAMTS13 | Acquired autoimmune thrombotic thrombocytopenia (iTTP) (thrombosis) |
Autoantibodies against factor VIII (FVIII) | Acquired hemophilia A (bleeding) |
Autoantibodies against other factors | Various acquired factor deficiencies (generally bleeding) |
Autoantibodies against platelets | Acquired autoimmune thrombocytopenia (iITP) (bleeding) |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Favaloro, E.J.; Pasalic, L.; Lippi, G. Autoimmune Diseases Affecting Hemostasis: A Narrative Review. Int. J. Mol. Sci. 2022, 23, 14715. https://doi.org/10.3390/ijms232314715
Favaloro EJ, Pasalic L, Lippi G. Autoimmune Diseases Affecting Hemostasis: A Narrative Review. International Journal of Molecular Sciences. 2022; 23(23):14715. https://doi.org/10.3390/ijms232314715
Chicago/Turabian StyleFavaloro, Emmanuel J., Leonardo Pasalic, and Giuseppe Lippi. 2022. "Autoimmune Diseases Affecting Hemostasis: A Narrative Review" International Journal of Molecular Sciences 23, no. 23: 14715. https://doi.org/10.3390/ijms232314715