PDF herunterladen
Semin Thromb Hemost 2022; 48(08): 880-888
DOI: 10.1055/s-0042-1756187
Review Article

One Hundred Years of Congenital Fibrinogen Disorders

Alessandro Casini
1   Division of Angiology and Hemostasis, University Hospitals of Geneva, Geneva, Switzerland
2   Department of Medicine, Faculty of Medicine, University of Geneva, Geneva, Switzerland
,
Philippe de Moerloose
2   Department of Medicine, Faculty of Medicine, University of Geneva, Geneva, Switzerland
,
Marguerite Neerman-Arbez
2   Department of Medicine, Faculty of Medicine, University of Geneva, Geneva, Switzerland
3   Department of Genetic Medicine and Development, Faculty of Medicine, University of Geneva, Geneva, Switzerland
› Institutsangaben
› Weitere Informationen
    Lizenzen und Reprints

Abstract

Congenital fibrinogen disorders encompass a broad range of fibrinogen defects characterized by a wide molecular and clinical spectrum. From the first clinical description of afibrinogenemia in 1920, many major achievements have contributed to a better understanding of these complex disorders. The finding of causative mutations in all three fibrinogen genes has contributed to reveal the molecular mechanisms involved in biosynthesis of the fibrinogen molecule and to clarify the basic processes of fibrin polymerization and fibrinolysis. The compilation of abundant cases with detailed genetic, biological, and clinical features has enabled the classification of congenital fibrinogen disorders into several types and subtypes. Thus, the recent classification of congenital fibrinogen disorder is based not only on the clottable and antigenic fibrinogen levels but also on the patient's clinical phenotype and genotype. Fibrinogen supplementation is the cornerstone of bleeding management in fibrinogen disorders. Since the discovery of blood fractionation, the method of production of fibrinogen concentrate has been progressively modified to significantly improve purity and safety. Nevertheless, the availability of such products is still limited to a few countries and the optimal threshold of fibrinogen to target is still not established. In this review, we describe the major advances that have characterized 100 years of congenital fibrinogen disorders, focusing on afibrinogenemia and dysfibrinogenemia.

Keywords

afibrinogenemia - dysfibrinogenemia - fibrinogen


Publikationsverlauf

Artikel online veröffentlicht:
02. September 2022

© 2022. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 

  • References

  • 1 Owen CA. A History of Blood Coagulation. In: Nichols WL, Bowie EJW, Rochester MN. eds. Mayo Foundation for Medical Education and Research ed. 2001
    Google Scholar
  • 2 Costa-Filho R, Hochleitner G, Wendt M, Teruya A, Spahn DR. Over 50 years of fibrinogen concentrate. Clin Appl Thromb Hemost 2016; 22 (02) 109-114
    CrossrefPubMedGoogle Scholar
  • 3 Casini A, de Moerloose P, Neerman-Arbez M. Clinical features and management of congenital fibrinogen deficiencies. Semin Thromb Hemost 2016; 42 (04) 366-374
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 4 Neerman-Arbez M, de Moerloose P, Casini A. Laboratory and genetic investigation of mutations accounting for congenital fibrinogen disorders. Semin Thromb Hemost 2016; 42 (04) 356-365
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 5 Palla R, Peyvandi F, Shapiro AD. Rare bleeding disorders: diagnosis and treatment. Blood 2015; 125 (13) 2052-2061
    CrossrefPubMedGoogle Scholar
  • 6 Casini A, Neerman-Arbez M, de Moerloose P. Heterogeneity of congenital afibrinogenemia, from epidemiology to clinical consequences and management. Blood Rev 2021; 48: 100793
    CrossrefPubMedGoogle Scholar
  • 7 Mosesson MW, DiOrio JP, Müller MF. et al. Studies on the ultrastructure of fibrin lacking fibrinopeptide B (beta-fibrin). Blood 1987; 69 (04) 1073-1081
    CrossrefPubMedGoogle Scholar
  • 8 Weisel JW, Litvinov RI. Mechanisms of fibrin polymerization and clinical implications. Blood 2013; 121 (10) 1712-1719
    CrossrefPubMedGoogle Scholar
  • 9 Weisel JW. Why dysfibrinogenaemias still matter. Thromb Haemost 2009; 102 (03) 426-427
    PubMedGoogle Scholar
  • 10 Rabe F, Saloman E. Ueber-faserstoffmangel im blute bei einem falle von hemophilie. Arch Intern Med (Chic) 1920; (95) 2-14
    PubMedGoogle Scholar
  • 11 De Silva CC, Thanabalasundaram RS. Congenital afibrinogenemia. BMJ 1951; 2 (4723): 86-88
    CrossrefPubMedGoogle Scholar
  • 12 Inamoto Y, Terao T. First report of case of congenital afibrinogenemia with successful delivery. Am J Obstet Gynecol 1985; 153 (07) 803-804
    CrossrefPubMedGoogle Scholar
  • 13 Dickenman RC, Brown HJ, Hiratzka T, Vetne G. Thrombotic thrombocytopenic purpura with associated afibrinogenemia; report of case. J Mich State Med Soc 1955; 54 (12) 1421-1425
    PubMedGoogle Scholar
  • 14 Gallet S, Tran Minh V, Louis D, Cotton JB, Berthier JC, Hartemann E. Massive hemoperitoneum caused by rupture of the spleen, a complication of congenital afibrinogenemia. Conservative treatment. Pediatrie 1985; 40 (05) 385-391
    PubMedGoogle Scholar
  • 15 Bridey F, Négrier C, Duval C, Ariëns R, de Moerloose P, Casini A. Impaired factor XIII activation in patients with congenital afibrinogenemia. Haematologica 2019; 104 (03) e111-e113
    CrossrefPubMedGoogle Scholar
  • 16 Colvin RB, Mosesson MW, Dvorak HF. Delayed-type hypersensitivity skin reactions in congenital afibrinogenemia lack fibrin deposition and induration. J Clin Invest 1979; 63 (06) 1302-1306
    CrossrefPubMedGoogle Scholar
  • 17 Henderson J, Donaldson G, Scarborough H. Congenital afibrinogenemia report of a case with a review of the literature. QJM 1945; 14: 101-111
    PubMedGoogle Scholar
  • 18 Lagier R, Bouvier CA, Van Strijthem N. Skeletal changes in congenital fibrinogen abnormalities. Skeletal Radiol 1980; 5 (04) 233-239
    CrossrefPubMedGoogle Scholar
  • 19 Imperato C, Dettori AG. Congenital hypofibrinogenemia with fibrinoasthenia. Helv Paediatr Acta 1958; 13 (04) 380-399
    PubMedGoogle Scholar
  • 20 Ménaché D. Dysfibrinogénémie constitutionnelle et familiale. Paper presented at: Proc 9th Congr Europ Soc Haemat Lisbon. New York: S. Karger Basel; 1963: 1255-1259
    Google Scholar
  • 21 Beck EA, Charache P, Jackson DP. A new inherited coagulation disorder caused by an abnormal fibrinogen (‘fibrinogen Baltimore’). Nature 1965; 208 (5006): 143-145
    CrossrefPubMedGoogle Scholar
  • 22 Forman WB, Ratnoff OD, Boyer MH. An inherited qualitative abnormality in plasma fibrinogen: fibrinogen Cleveland. J Lab Clin Med 1968; 72 (03) 455-472
    PubMedGoogle Scholar
  • 23 Mammen EF, Prasad AS. Familial dysfibrinogenemia—“Detroit fibrinogen”. Verh Dtsch Ges Inn Med 1968; 74: 140-144
    PubMedGoogle Scholar
  • 24 Blombäck M, Blombäck B, Mammen EF, Prasad AS. Fibrinogen Detroit—a molecular defect in the N-terminal disulphide knot of human fibrinogen?. Nature 1968; 218 (5137): 134-137
    CrossrefPubMedGoogle Scholar
  • 25 Soria J, Soria C, Samama M, Poirot E, Kling C. Fibrinogen Troyes—fibrinogen Metz. Two new cases of congenital dysfibrinogenemia. Thromb Diath Haemorrh 1972; 27 (03) 619-633
    PubMedGoogle Scholar
  • 26 Al-Mondhiry H, Bilezikian SB, Nossel HL. Fibrinogen "“New York”—an abnormal fibrinogen associated with thromboembolism: functional evaluation. Blood 1975; 45 (05) 607-619
    CrossrefPubMedGoogle Scholar
  • 27 Denninger MH, Finlayson JS, Reamer LA, Parquet-Gernez A, Goudemand M, Menache D. Congenital dysfibrinogenemia: fibrinogen Lille. Thromb Res 1978; 13 (03) 453-466
    CrossrefPubMedGoogle Scholar
  • 28 Mosesson MW, Amrani DL, Ménaché D. Studies on the structural abnormality of fibrinogen Paris I. J Clin Invest 1976; 57 (03) 782-790
    CrossrefPubMedGoogle Scholar
  • 29 Mosesson MW, Feldmann G, Ménaché D. Electron microscopy of fibrin Paris I. Blood 1980; 56 (01) 80-83
    CrossrefPubMedGoogle Scholar
  • 30 Jandrot-Perrus M, Mosesson MW, Denninger MH, Ménaché D. Studies of platelet fibrinogen from a subject with a congenital plasma fibrinogen abnormality (fibrinogen Paris I). Blood 1979; 54 (05) 1109-1116
    CrossrefPubMedGoogle Scholar
  • 31 Casini A, Neerman-Arbez M, Ariëns RA, de Moerloose P. Dysfibrinogenemia: from molecular anomalies to clinical manifestations and management. J Thromb Haemost 2015; 13 (06) 909-919
    CrossrefPubMedGoogle Scholar
  • 32 Ebert RF. Index of Variant Human Fibrinogens. Boca Raton, Ann Arbor, Boston: CRC Press ed.; 1994
    Google Scholar
  • 33 Mosesson MW. Hereditary Fibrinogen Abnormalities. In: Kaushansky K, Lichtman M, Beutler E. et al. eds. Williams Hematology. 7th ed.. New York, NY: McGraw-Hil; 2005
    Google Scholar
  • 34 Neerman-Arbez M, de Moerloose P. Hereditary fibrinogen abnormalities. In: Kaushansky K, Lichtman M, Beutler E. et al, eds., Williams Hematology. 8th ed.. New York, NY: McGraw-Hil; 2010: 1-33
    Google Scholar
  • 35 Hanss M, Biot F. A database for human fibrinogen variants. Ann N Y Acad Sci 2001; 936: 89-90
    CrossrefPubMedGoogle Scholar
  • 36 Pauling L, Itano HA. et al. Sickle cell anemia a molecular disease. Science 1949; 110 (2865): 543-548
    CrossrefPubMedGoogle Scholar
  • 37 Blombäck B. Travels with fibrinogen. J Thromb Haemost 2006; 4 (08) 1653-1660
    CrossrefPubMedGoogle Scholar
  • 38 Doolittle RF. The structure and evolution of vertebrate fibrinogen. Ann N Y Acad Sci 1983; 408: 13-27
    CrossrefPubMedGoogle Scholar
  • 39 Kant JA, Lord ST, Crabtree GR. Partial mRNA sequences for human A alpha, B beta, and gamma fibrinogen chains: evolutionary and functional implications. Proc Natl Acad Sci U S A 1983; 80 (13) 3953-3957
    CrossrefPubMedGoogle Scholar
  • 40 Neerman-Arbez M, Honsberger A, Antonarakis SE, Morris MA. Deletion of the fibrinogen [correction of FibroGen] alpha-chain gene (FGA) causes congenital afibrinogenemia. J Clin Invest 1999; 103 (02) 215-218
    CrossrefPubMedGoogle Scholar
  • 41 Ni H, Denis CV, Subbarao S. et al. Persistence of platelet thrombus formation in arterioles of mice lacking both von Willebrand factor and fibrinogen. J Clin Invest 2000; 106 (03) 385-392
    CrossrefPubMedGoogle Scholar
  • 42 Casini A, de Moerloose P. How I treat dysfibrinogenemia. Blood 2021; 138 (21) 2021-2030
    CrossrefPubMedGoogle Scholar
  • 43 Wada Y, Lord ST. A correlation between thrombotic disease and a specific fibrinogen abnormality (A alpha 554 Arg–>Cys) in two unrelated kindred, Dusart and Chapel Hill III. Blood 1994; 84 (11) 3709-3714
    CrossrefPubMedGoogle Scholar
  • 44 Soria J, Soria C, Caen P. A new type of congenital dysfibrinogenaemia with defective fibrin lysis–Dusard syndrome: possible relation to thrombosis. Br J Haematol 1983; 53 (04) 575-586
    CrossrefPubMedGoogle Scholar
  • 45 Koopman J, Haverkate F, Grimbergen J. et al. Molecular basis for fibrinogen Dusart (A alpha 554 Arg–>Cys) and its association with abnormal fibrin polymerization and thrombophilia. J Clin Invest 1993; 91 (04) 1637-1643
    CrossrefPubMedGoogle Scholar
  • 46 Collet JP, Soria J, Mirshahi M. et al. Dusart syndrome: a new concept of the relationship between fibrin clot architecture and fibrin clot degradability: hypofibrinolysis related to an abnormal clot structure. Blood 1993; 82 (08) 2462-2469
    CrossrefPubMedGoogle Scholar
  • 47 Collet JP, Woodhead JL, Soria J. et al. Fibrinogen Dusart: electron microscopy of molecules, fibers and clots, and viscoelastic properties of clots. Biophys J 1996; 70 (01) 500-510
    CrossrefPubMedGoogle Scholar
  • 48 Haverkate F, Samama M. Familial dysfibrinogenemia and thrombophilia. Report on a study of the SSC Subcommittee on Fibrinogen. Thromb Haemost 1995; 73 (01) 151-161
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 49 Lak M, Keihani M, Elahi F, Peyvandi F, Mannucci PM. Bleeding and thrombosis in 55 patients with inherited afibrinogenaemia. Br J Haematol 1999; 107 (01) 204-206
    CrossrefPubMedGoogle Scholar
  • 50 Peyvandi F, Haertel S, Knaub S, Mannucci PM. Incidence of bleeding symptoms in 100 patients with inherited afibrinogenemia or hypofibrinogenemia. J Thromb Haemost 2006; 4 (07) 1634-1637
    CrossrefPubMedGoogle Scholar
  • 51 Peyvandi F. Epidemiology and treatment of congenital fibrinogen deficiency. Thromb Res 2012; 130 (Suppl. 02) S7-S11
    CrossrefPubMedGoogle Scholar
  • 52 Casini A, Undas A, Palla R, Thachil J, de Moerloose P. Subcommittee on Factor XIII and Fibrinogen. Diagnosis and classification of congenital fibrinogen disorders: communication from the SSC of the ISTH. J Thromb Haemost 2018; 16 (09) 1887-1890
    CrossrefPubMedGoogle Scholar
  • 53 de Moerloose P, Boehlen F, Neerman-Arbez M. Fibrinogen and the risk of thrombosis. Semin Thromb Hemost 2010; 36 (01) 7-17
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 54 De Marco L, Girolami A, Zimmerman TS, Ruggeri ZM. von Willebrand factor interaction with the glycoprotein IIb/IIa complex. Its role in platelet function as demonstrated in patients with congenital afibrinogenemia. J Clin Invest 1986; 77 (04) 1272-1277
    CrossrefPubMedGoogle Scholar
  • 55 Korte W, Feldges A. Increased prothrombin activation in a patient with congenital afibrinogenemia is reversible by fibrinogen substitution. Clin Investig 1994; 72 (05) 396-398
    CrossrefPubMedGoogle Scholar
  • 56 Hemker HC, Giesen P, Al Dieri R. et al. Calibrated automated thrombin generation measurement in clotting plasma. Pathophysiol Haemost Thromb 2003; 33 (01) 4-15
    CrossrefPubMedGoogle Scholar
  • 57 de Bosch NB, Mosesson MW, Ruiz-Sáez A, Echenagucia M, Rodriguez-Lemoin A. Inhibition of thrombin generation in plasma by fibrin formation (Antithrombin I). Thromb Haemost 2002; 88 (02) 253-258
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 58 Mosesson MW, Antithrombin I. Antithrombin I. Inhibition of thrombin generation in plasma by fibrin formation. Thromb Haemost 2003; 89 (01) 9-12
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 59 Dupuy E, Soria C, Molho P. et al. Embolized ischemic lesions of toes in an afibrinogenemic patient: possible relevance to in vivo circulating thrombin. Thromb Res 2001; 102 (03) 211-219
    CrossrefPubMedGoogle Scholar
  • 60 Casini A, von Mackensen S, Santoro C. et al; QualyAfib Study Group. Clinical phenotype, fibrinogen supplementation, and health-related quality of life in patients with afibrinogenemia. Blood 2021; 137 (22) 3127-3136
    CrossrefPubMedGoogle Scholar
  • 61 Casini A, Blondon M, Lebreton A. et al. Natural history of patients with congenital dysfibrinogenemia. Blood 2015; 125 (03) 553-561
    CrossrefPubMedGoogle Scholar
  • 62 Zhou J, Ding Q, Chen Y. et al. Clinical features and molecular basis of 102 Chinese patients with congenital dysfibrinogenemia. Blood Cells Mol Dis 2015; 55 (04) 308-315
    CrossrefPubMedGoogle Scholar
  • 63 Cohn EJ, Oncley JL, Strong LE, Hughes WL, Armstrong SH. Chemical, clinical, and immunological studies on the products of human plasma fractionation. I. The characterization of the protein fractions of human plasma. J Clin Invest 1944; 23 (04) 417-432
    CrossrefPubMedGoogle Scholar
  • 64 Cohn EJ. Blood proteins and their therapeutic value. Science 1945; 101 (2612): 51-56
    CrossrefPubMedGoogle Scholar
  • 65 Nitschmann H, Kistler P, Joss A. Dried fraction I for clinical use from smallest plasma pools, sterile without filtration. Vox Sang 1957; 2 (02) 100-103
    CrossrefPubMedGoogle Scholar
  • 66 Stampfli K. The therapeutic use of fibrinogen (fraction I of Cohn) in fibrinogen deficiency diseases and thrombocytopenias. Ther Umsch 1957; 14 (09) 259-263
    PubMedGoogle Scholar
  • 67 Casini A, de Moerloose P. Fibrinogen concentrates in hereditary fibrinogen disorders: past, present and future. Haemophilia 2020; 26 (01) 25-32
    CrossrefPubMedGoogle Scholar
  • 68 Kreuz W, Meili E, Peter-Salonen K. et al. Pharmacokinetic properties of a pasteurised fibrinogen concentrate. Transfus Apheresis Sci 2005; 32 (03) 239-246
    CrossrefPubMedGoogle Scholar
  • 69 Kreuz W, Meili E, Peter-Salonen K. et al. Efficacy and tolerability of a pasteurised human fibrinogen concentrate in patients with congenital fibrinogen deficiency. Transfus Apheresis Sci 2005; 32 (03) 247-253
    CrossrefPubMedGoogle Scholar
  • 70 Manco-Johnson MJ, Dimichele D, Castaman G. et al; FIBRINOGEN CONCENTRATE STUDY GROUP. Pharmacokinetics and safety of fibrinogen concentrate. J Thromb Haemost 2009; 7 (12) 2064-2069
    CrossrefPubMedGoogle Scholar
  • 71 Négrier C, Rothschild C, Goudemand J. et al. Pharmacokinetics and pharmacodynamics of a new highly secured fibrinogen concentrate. J Thromb Haemost 2008; 6 (09) 1494-1499
    CrossrefPubMedGoogle Scholar
  • 72 Bornikova L, Peyvandi F, Allen G, Bernstein J, Manco-Johnson MJ. Fibrinogen replacement therapy for congenital fibrinogen deficiency. J Thromb Haemost 2011; 9 (09) 1687-1704
    CrossrefPubMedGoogle Scholar
  • 73 De Vries A, Rosenberg T, Kochwa S, Boss JH. Precipitating antifibrinogen antibody appearing after fibrinogen infusions in a patient with congenital afibrinogenemia. Am J Med 1961; 30: 486-494
    CrossrefPubMedGoogle Scholar
  • 74 Négrier C, Rothschild C, Borg JY. et al. Post-authorization safety study of Clottafact®, a triply secured fibrinogen concentrate in congenital afibrinogenemia. A prospective observational study. Vox Sang 2016; 111 (04) 383-390
    CrossrefPubMedGoogle Scholar
  • 75 Solomon C, Gröner A, Ye J, Pendrak I. Safety of fibrinogen concentrate: analysis of more than 27 years of pharmacovigilance data. Thromb Haemost 2015; 113 (04) 759-771
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 76 Lasky J, Teitel J, Wang M, Dalton D, Schmidt DS, Brainsky A. Fibrinogen concentrate for bleeding in patients with congenital fibrinogen deficiency: observational study of efficacy and safety for prophylaxis and treatment. Res Pract Thromb Haemost 2020; 4 (08) 1313-1323
    CrossrefPubMedGoogle Scholar
  • 77 Casini A, Duval C, Pan X, Tintillier V, Biron-Andreani C, Ariëns RAS. Fibrin clot structure in patients with congenital dysfibrinogenaemia. Thromb Res 2016; 137: 189-195
    CrossrefPubMedGoogle Scholar
  • 78 Feller T, Connell SDA, Ariëns RAS. Why fibrin biomechanical properties matter for hemostasis and thrombosis. J Thromb Haemost 2022; 20 (01) 6-16
    CrossrefPubMedGoogle Scholar
  • 79 Byrnes JR, Wolberg AS. Red blood cells in thrombosis. Blood 2017; 130 (16) 1795-1799
    CrossrefPubMedGoogle Scholar
  • 80 Ajjan R, Lim BC, Standeven KF. et al. Common variation in the C-terminal region of the fibrinogen beta-chain: effects on fibrin structure, fibrinolysis and clot rigidity. Blood 2008; 111 (02) 643-650
    CrossrefPubMedGoogle Scholar
  • 81 Ariëns RA, Philippou H, Nagaswami C, Weisel JW, Lane DA, Grant PJ. The factor XIII V34L polymorphism accelerates thrombin activation of factor XIII and affects cross-linked fibrin structure. Blood 2000; 96 (03) 988-995
    CrossrefPubMedGoogle Scholar
  • 82 Liu CY, Koehn JA, Morgan FJ. Characterization of fibrinogen New York 1. A dysfunctional fibrinogen with a deletion of B beta(9-72) corresponding exactly to exon 2 of the gene. J Biol Chem 1985; 260 (07) 4390-4396
    CrossrefPubMedGoogle Scholar
  • 83 Koopman J, Haverkate F, Grimbergen J. et al. Abnormal fibrinogens IJmuiden (B beta Arg14—-Cys) and Nijmegen (B beta Arg44—-Cys) form disulfide-linked fibrinogen-albumin complexes. Proc Natl Acad Sci U S A 1992; 89 (08) 3478-3482
    CrossrefPubMedGoogle Scholar
  • 84 Koopman J, Haverkate F, Lord ST, Grimbergen J, Mannucci PM. Molecular basis of fibrinogen Naples associated with defective thrombin binding and thrombophilia. Homozygous substitution of B beta 68 Ala—-Thr. J Clin Invest 1992; 90 (01) 238-244
    CrossrefPubMedGoogle Scholar
  • 85 Bentolila S, Samama MM, Conard J, Horellou MH, Ffrench P. Association of dysfibrinogenemia and thrombosis. Apropos of a family (Fibrinogen Melun) and review of the literature. Ann Med Interne (Paris) 1995; 146 (08) 575-580
    PubMedGoogle Scholar
  • 86 Marchi R, Lundberg U, Grimbergen J. et al. Fibrinogen Caracas V, an abnormal fibrinogen with an Aalpha 532 Ser–>Cys substitution associated with thrombosis. Thromb Haemost 2000; 84 (02) 263-270
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 87 Santacroce R, Cappucci F, Pisanelli D. et al. Inherited abnormalities of fibrinogen: 10-year clinical experience of an Italian group. Blood Coagul Fibrinolysis 2006; 17 (04) 235-240
    CrossrefPubMedGoogle Scholar
  • 88 Miesbach W, Scharrer I, Henschen A, Neerman-Arbez M, Spitzer S, Galanakis D. Inherited dysfibrinogenemia: clinical phenotypes associated with five different fibrinogen structure defects. Blood Coagul Fibrinolysis 2010; 21 (01) 35-40
    CrossrefPubMedGoogle Scholar
  • 89 Shapiro SE, Phillips E, Manning RA. et al. Clinical phenotype, laboratory features and genotype of 35 patients with heritable dysfibrinogenaemia. Br J Haematol 2013; 160 (02) 220-227
    CrossrefPubMedGoogle Scholar
  • 90 Smith N, Bornikova L, Noetzli L. et al. Identification and characterization of novel mutations implicated in congenital fibrinogen disorders. Res Pract Thromb Haemost 2018; 2 (04) 800-811
    CrossrefPubMedGoogle Scholar
  • 91 Castaman G, Giacomelli SH, Biasoli C, Contino L, Radossi P. Risk of bleeding and thrombosis in inherited qualitative fibrinogen disorders. Eur J Haematol 2019; 103 (04) 379-384
    CrossrefPubMedGoogle Scholar
  • 92 Wypasek E, Klukowska A, Zdziarska J. et al. Genetic and clinical characterization of congenital fibrinogen disorders in Polish patients: identification of three novel fibrinogen gamma chain mutations. Thromb Res 2019; 182: 133-140
    CrossrefPubMedGoogle Scholar
  • 93 Simurda T, Zolkova J, Kolkova Z. et al. Comparison of clinical phenotype with genetic and laboratory results in 31 patients with congenital dysfibrinogenemia in northern Slovakia. Int J Hematol 2020; 111 (06) 795-802
    CrossrefPubMedGoogle Scholar
  • 94 Zhou P, Yu M, Peng Y, Ma P, Wan L. Identification and characterization of novel mutations in Chinese patients with congenital fibrinogen disorders. Blood Cells Mol Dis 2021; 86: 102489
    CrossrefPubMedGoogle Scholar
  • 95 Lissitchkov T, Madan B, Djambas Khayat C. et al. Efficacy and safety of a new human fibrinogen concentrate in patients with congenital fibrinogen deficiency: an interim analysis of a Phase III trial. Transfusion 2018; 58 (02) 413-422
    CrossrefPubMedGoogle Scholar
  • 96 Ross C, Rangarajan S, Karimi M. et al. Pharmacokinetics, clot strength and safety of a new fibrinogen concentrate: randomized comparison with active control in congenital fibrinogen deficiency. J Thromb Haemost 2018; 16 (02) 253-261
    CrossrefPubMedGoogle Scholar
  • 97 Djambas Khayat C, El Khorassani M, Lambert T. et al. Clinical pharmacology, efficacy and safety study of a triple-secured fibrinogen concentrate in adults and adolescent patients with congenital fibrinogen deficiency. J Thromb Haemost 2019; 17 (04) 635-644
    CrossrefPubMedGoogle Scholar
  • 98 Djambas Khayat C, El Khorassani M, Aytaç S. et al. Pharmacology, efficacy and safety of a triple-secured fibrinogen concentrate in children less than or equal to 12 years with afibrinogenaemia. Thromb Haemost 2020; 120 (06) 957-967
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 99 Lissitchkov T, Madan B, Djambas Khayat C. et al. Fibrinogen concentrate for treatment of bleeding and surgical prophylaxis in congenital fibrinogen deficiency patients. J Thromb Haemost 2020; 18 (04) 815-824
    CrossrefPubMedGoogle Scholar
  • 100 Djambas Khayat C, Lohade S, D'Souza F. et al. Efficacy and safety of fibrinogen concentrate for on-demand treatment of bleeding and surgical prophylaxis in paediatric patients with congenital fibrinogen deficiency. Haemophilia 2021; 27 (02) 283-292
    CrossrefPubMedGoogle Scholar
  • 101 Ross CR, Subramanian S, Navarro-Puerto J. et al. Pharmacokinetics, surrogate efficacy and safety evaluations of a new human plasma-derived fibrinogen concentrate (FIB Grifols) in adult patients with congenital afibrinogenemia. Thromb Res 2021; 199: 110-118
    CrossrefPubMedGoogle Scholar