PDF herunterladen
Semin Thromb Hemost 2016; 42(04): 429-439
DOI: 10.1055/s-0036-1572326
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Diagnosis and Management of Congenital and Acquired FXIII Deficiencies

László Muszbek
1   Division of Clinical Laboratory Science and Vascular Biology, Department of Laboratory Medicine, Faculty of Medicine, University of Debrecen, Debrecen, Hungary
2   Thrombosis and Hemostasis Research Group of the Hungarian Academy of Sciences, University of Debrecen, Debrecen, Hungary
,
Éva Katona
1   Division of Clinical Laboratory Science and Vascular Biology, Department of Laboratory Medicine, Faculty of Medicine, University of Debrecen, Debrecen, Hungary
› Institutsangaben
Weitere Informationen

Publikationsverlauf

Publikationsdatum:
12. April 2016 (online)

    Lizenzen und Reprints

Abstract

Inherited deficiency of FXIII A subunit (FXIII-A) is a rare (1:2,000,000) but very severe bleeding diathesis. The incidence is much higher in communities where the practice of consanguineous marriage is combined with founder effect mutation. Because of the high risk of intracranial bleeding, life-long prophylaxis, preferably using FXIII concentrate, is mandatory. In FXIII-B subunit deficiency the bleeding diathesis is mild to moderate. FXIII deficiency is frequently associated with impaired wound healing. Women suffering from FXIII deficiency cannot carry pregnancies to term; in severe cases spontaneous abortion occurs in the first trimester. Plasma-derived heat-inactivated FXIII concentrate and recombinant FXIII-A are available for prophylaxis; a 4 weekly dose of 35 to 40 U/kg is recommended and a trough level of greater than 5% FXIII activity should be aimed for. During pregnancy, 2 weekly prophylaxis with a target trough level of greater than 10% is recommended, and during labor FXIII activity should exceed 30%. During surgical procedures, the target should be higher than 50% FXIII activity. Alloantibodies make FXIII deficiency difficult to manage, but fortunately they are extremely rare. Acquired FXIII deficiency may involve both subunits. Autoantibodies against FXIII subunits also manifest in severe bleeding complication with a relatively high mortality rate. The first-line test in the diagnosis of FXIII deficiency should be a quantitative functional assay based on the measurement of ammonia release or amine incorporation. The sensitivity of the traditional clot solubility assay is not sufficiently robust to enable proper screening. Antigen assays are needed for the classification of FXIII deficiencies. In the case of anti-FXIII antibodies, the diagnostic armory should be supplemented by a mixing test/Bethesda-type inhibitor assay and by assays that detect/measure the binding of antibodies to FXIII and to its subunits.

Keywords

bleeding diathesis - factor XIII - factor XIII assays - factor XIII deficiency - prophylaxis
 

  • References

  • 1 Komáromi I, Bagoly Z, Muszbek L. Factor XIII: novel structural and functional aspects. J Thromb Haemost 2011; 9 (1) 9-20
    CrossrefPubMedGoogle Scholar
  • 2 Muszbek L, Bereczky Z, Bagoly Z, Komáromi I, Katona É. Factor XIII: a coagulation factor with multiple plasmatic and cellular functions. Physiol Rev 2011; 91 (3) 931-972
    CrossrefPubMedGoogle Scholar
  • 3 Schroeder V, Kohler HP. New developments in the area of factor XIII. J Thromb Haemost 2013; 11 (2) 234-244
    CrossrefPubMedGoogle Scholar
  • 4 Schroeder V, Kohler HP. Factor XIII: structure and function. Semin Thromb Hemost 2016; 42 (4) 422-428
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 5 Köhler HP, Ichinose A, Seitz R, Ariens RA, Muszbek L ; Factor XIII and Fibrinogen SSC Subcommittee of The ISTH. Diagnosis and classification of factor XIII deficiencies. J Thromb Haemost 2011; 9 (7) 1404-1406
    CrossrefPubMedGoogle Scholar
  • 6 Shetty S, Shelar T, Mirgal D , et al. Rare coagulation factor deficiencies: a countrywide screening data from India. Haemophilia 2014; 20 (4) 575-581
    CrossrefPubMedGoogle Scholar
  • 7 Dorgalaleh A, Naderi M, Hosseini MS , et al. Factor XIII deficiency in Iran: a comprehensive review of the literature. Semin Thromb Hemost 2015; 41 (3) 323-329
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 8 Naderi M, Dorgalaleh A, Alizadeh S , et al. Clinical manifestations and management of life-threatening bleeding in the largest group of patients with severe factor XIII deficiency. Int J Hematol 2014; 100 (5) 443-449
    CrossrefPubMedGoogle Scholar
  • 9 Eshghi P, Cohan N, Lak M , et al. Arg77His and Trp187Arg are the most common mutations causing FXIII deficiency in Iran. Clin Appl Thromb Hemost 2012; 18 (1) 100-103
    CrossrefPubMedGoogle Scholar
  • 10 Morange P, Trigui N, Frère C , et al. Molecular characterization of a novel mutation in the factor XIII a subunit gene associated with a severe defect: importance of prophylactic substitution. Blood Coagul Fibrinolysis 2009; 20 (7) 605-606
    CrossrefPubMedGoogle Scholar
  • 11 Borhany M, Handrkova H, Cairo A , et al. Congenital factor XIII deficiency in Pakistan: characterization of seven families and identification of four novel mutations. Haemophilia 2014; 20 (4) 568-574
    CrossrefPubMedGoogle Scholar
  • 12 Hosseini S, Dorgalaleh A, Bamedi T , et al. First cases of severe congenital factor XIII deficiency in Southwestern Afghanistan in the vicinity of southeast of Iran. Blood Coagul Fibrinolysis 2015; 26 (8) 908-911
    PubMedGoogle Scholar
  • 13 Ivaskevicius V, Seitz R, Kohler HP , et al; Study Group. International registry on factor XIII deficiency: a basis formed mostly on European data. Thromb Haemost 2007; 97 (6) 914-921
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 14 El Mahmoudi H, Amor MB, Gouider E , et al. Small insertion (c.869insC) within F13A gene is dominant in Tunisian patients with inherited FXIII deficiency due to ancient founder effect. Haemophilia 2009; 15 (5) 1176-1179
    CrossrefPubMedGoogle Scholar
  • 15 Louhichi N, Medhaffar M, Hadjsalem I , et al. Congenital factor XIII deficiency caused by two mutations in eight Tunisian families: molecular confirmation of a founder effect. Ann Hematol 2010; 89 (5) 499-504
    CrossrefPubMedGoogle Scholar
  • 16 Mikkola H, Muszbek L, Laiho E , et al. Molecular mechanism of a mild phenotype in coagulation factor XIII (FXIII) deficiency: a splicing mutation permitting partial correct splicing of FXIII A-subunit mRNA. Blood 1997; 89 (4) 1279-1287
    PubMedGoogle Scholar
  • 17 Schroeder V, Meili E, Cung T, Schmutz P, Kohler HP. Characterisation of six novel A-subunit mutations leading to congenital factor XIII deficiency and molecular analysis of the first diagnosed patient with this rare bleeding disorder. Thromb Haemost 2006; 95 (1) 77-84
    PubMedGoogle Scholar
  • 18 Souri M, Izumi T, Higashi Y, Girolami A, Ichinose A. A founder effect is proposed for factor XIII B subunit deficiency caused by the insertion of triplet AAC in exon III encoding the second Sushi domain. Thromb Haemost 1998; 80 (2) 211-213
    PubMedGoogle Scholar
  • 19 Biswas A, Ivaskevicius V, Seitz R, Thomas A, Oldenburg J. An update of the mutation profile of factor 13 A and B genes. Blood Rev 2011; 25 (5) 193-204
    CrossrefPubMedGoogle Scholar
  • 20 Schroeder V, Kohler HP. Factor XIII deficiency: an update. Semin Thromb Hemost 2013; 39 (6) 632-641
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 21 Peyvandi F, Palla R, Menegatti M , et al; European Network of Rare Bleeding Disorders Group. Coagulation factor activity and clinical bleeding severity in rare bleeding disorders: results from the European Network of Rare Bleeding Disorders. J Thromb Haemost 2012; 10 (4) 615-621
    CrossrefPubMedGoogle Scholar
  • 22 Karimi M, Bereczky Z, Cohan N, Muszbek L. Factor XIII deficiency. Semin Thromb Hemost 2009; 35 (4) 426-438
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 23 Naderi M, Zarei T, Haghpanah S, Eshghi P, Miri-Moghaddam E, Karimi M. Intracranial hemorrhage pattern in the patients with factor XIII deficiency. Ann Hematol 2014; 93 (4) 693-697
    CrossrefPubMedGoogle Scholar
  • 24 Naderi M, Alizadeh S, Kazemi A , et al. Central nervous system bleeding in pediatric patients with factor XIII deficiency: a study on 23 new cases. Hematology 2015; 20 (2) 112-118
    CrossrefPubMedGoogle Scholar
  • 25 Duckert F, Jung E, Shmerling DH. A hitherto undescribed congenital haemorrhagic diathesis probably due to fibrin stabilizing factor deficiency. Thromb Diath Haemorrh 1960; 5: 179-186
    PubMedGoogle Scholar
  • 26 Inbal A, Lubetsky A, Krapp T , et al. Impaired wound healing in factor XIII deficient mice. Thromb Haemost 2005; 94 (2) 432-437
    PubMedGoogle Scholar
  • 27 Mahmoodi M, Peyvandi F, Afrasiabi A, Ghaffarpasand F, Karimi M. Bleeding symptoms in heterozygous carriers of inherited coagulation disorders in southern Iran. Blood Coagul Fibrinolysis 2011; 22 (5) 396-401
    CrossrefPubMedGoogle Scholar
  • 28 Seitz R, Duckert F, Lopaciuk S, Muszbek L, Rodeghiero F, Seligsohn U ; Study Group. ETRO Working Party on factor XIII questionnaire on congenital factor XIII deficiency in Europe: status and perspectives. Semin Thromb Hemost 1996; 22 (5) 415-418
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 29 Biswas A, Ivaskevicius V, Thomas A , et al. Eight novel F13A1 gene missense mutations in patients with mild FXIII deficiency: in silico analysis suggests changes in FXIII-A subunit structure/function. Ann Hematol 2014; 93 (10) 1665-1676
    CrossrefPubMedGoogle Scholar
  • 30 Sharief LA, Kadir RA. Congenital factor XIII deficiency in women: a systematic review of literature. Haemophilia 2013; 19 (6) e349-e357
    CrossrefPubMedGoogle Scholar
  • 31 Saito M, Asakura H, Yoshida T , et al. A familial factor XIII subunit B deficiency. Br J Haematol 1990; 74 (3) 290-294
    CrossrefPubMedGoogle Scholar
  • 32 Hashiguchi T, Saito M, Morishita E, Matsuda T, Ichinose A. Two genetic defects in a patient with complete deficiency of the b-subunit for coagulation factor XIII. Blood 1993; 82 (1) 145-150
    PubMedGoogle Scholar
  • 33 Ivaskevicius V, Biswas A, Loreth R , et al. Mutations affecting disulphide bonds contribute to a fairly common prevalence of F13B gene defects: results of a genetic study in 14 families with factor XIII B deficiency. Haemophilia 2010; 16 (4) 675-682
    PubMedGoogle Scholar
  • 34 Katona É, Pénzes K, Molnár É, Muszbek L. Measurement of factor XIII activity in plasma. Clin Chem Lab Med 2012; 50 (7) 1191-1202
    PubMedGoogle Scholar
  • 35 Ikemori R, Gruhl M, Shrivastava S, Shanberge JN. Solubility of fibrin clots in monochloroacetic acid. A reflection of serum pepsinogen levels. Am J Clin Pathol 1975; 63 (1) 49-56
    CrossrefPubMedGoogle Scholar
  • 36 Duncan EM, Dale BJ, Lloyd JV. Investigation of a link between raised levels of pepsinogen in blood as a mediator of in-vitro clot lysis in acid and a cause of abnormal factor XIII screening tests. Blood Coagul Fibrinolysis 2014; 25 (4) 340-348
    CrossrefPubMedGoogle Scholar
  • 37 Alam MM, Iftikhar AR, Mushtaq N, Fadoo Z. Ovarian haemorrhage: a rare presentation and diagnostic dilemma in factor XIII deficiency. J Pak Med Assoc 2014; 64 (2) 212-213
    PubMedGoogle Scholar
  • 38 Sanfelippo MJ, Mazza JJ, Mercier RJ. Symptomatic factor XIII deficiency with normal urea solubility test. Clin Lab 2014; 60 (12) 2099-2102
    PubMedGoogle Scholar
  • 39 Hsu P, Zantek ND, Meijer P , et al. Factor XIII Assays and associated problems for laboratory diagnosis of factor XIII deficiency: an analysis of International Proficiency testing results. Semin Thromb Hemost 2014; 40 (2) 232-238
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 40 Muszbek L, Polgár J, Fésüs L. Kinetic determination of blood coagulation factor XIII in plasma. Clin Chem 1985; 31 (1) 35-40
    PubMedGoogle Scholar
  • 41 Kárpáti L, Penke B, Katona E, Balogh I, Vámosi G, Muszbek L. A modified, optimized kinetic photometric assay for the determination of blood coagulation factor XIII activity in plasma. Clin Chem 2000; 46 (12) 1946-1955
    PubMedGoogle Scholar
  • 42 Fickenscher K, Aab A, Stüber W. A photometric assay for blood coagulation factor XIII. Thromb Haemost 1991; 65 (5) 535-540
    PubMedGoogle Scholar
  • 43 Ajzner E, Muszbek L. Kinetic spectrophotometric factor XIII activity assays: the subtraction of plasma blank is not omissible [corrected]. J Thromb Haemost 2004; 2 (11) 2075-2077
    CrossrefPubMedGoogle Scholar
  • 44 Lawrie AS, Green L, Mackie IJ, Liesner R, Machin SJ, Peyvandi F. Factor XIII—an under diagnosed deficiency—are we using the right assays?. J Thromb Haemost 2010; 8 (11) 2478-2482
    CrossrefPubMedGoogle Scholar
  • 45 Cini M, Legnani C, Frascaro M , et al. Measurement of factor XIII (FXIII) activity by an automatic ammonia release assay using iodoacetamide blank-procedure: no more overestimation in the low activity range and better detection of severe FXIII deficiencies. Clin Chem Lab Med 2015;
    PubMedGoogle Scholar
  • 46 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 (3) 988-995
    CrossrefPubMedGoogle Scholar
  • 47 Balogh I, Szôke G, Kárpáti L , et al. Val34Leu polymorphism of plasma factor XIII: biochemistry and epidemiology in familial thrombophilia. Blood 2000; 96 (7) 2479-2486
    PubMedGoogle Scholar
  • 48 Wartiovaara U, Mikkola H, Szôke G , et al. Effect of Val34Leu polymorphism on the activation of the coagulation factor XIII-A. Thromb Haemost 2000; 84 (4) 595-600
    PubMedGoogle Scholar
  • 49 Raut S, Merton RE, Rigsby P , et al; ISTH/SSC Factor XIII Subcommittee and the Factor XIII Standardization Working Party. A collaborative study to establish the 1st International Standard for factor XIII plasma. J Thromb Haemost 2007; 5 (9) 1923-1929
    CrossrefPubMedGoogle Scholar
  • 50 Muszbek L, Bagoly Z, Cairo A, Peyvandi F. Novel aspects of factor XIII deficiency. Curr Opin Hematol 2011; 18 (5) 366-372
    CrossrefPubMedGoogle Scholar
  • 51 Katona É, Muszbek L, Devreese K , et al. Factor XIII deficiency: complete phenotypic characterization of two cases with novel causative mutations. Haemophilia 2014; 20 (1) 114-120
    PubMedGoogle Scholar
  • 52 Katona E, Haramura G, Kárpáti L, Fachet J, Muszbek L. A simple, quick one-step ELISA assay for the determination of complex plasma factor XIII (A2B2). Thromb Haemost 2000; 83 (2) 268-273
    PubMedGoogle Scholar
  • 53 Katona E E, Ajzner E, Tóth K, Kárpáti L, Muszbek L. Enzyme-linked immunosorbent assay for the determination of blood coagulation factor XIII A-subunit in plasma and in cell lysates. J Immunol Methods 2001; 258 (1–2) 127-135
    CrossrefPubMedGoogle Scholar
  • 54 Dorgalaleh A, Farshi Y, Alizadeh SH , et al. Challenges in implementation of ISTH diagnostic algorithm for diagnosis and classification of factor XIII deficiency in Iran. J Thromb Haemost 2015; 13 (9) 1735-1736
    CrossrefPubMedGoogle Scholar
  • 55 Naderi M, Eshghi P, Cohan N, Haghpanah S, Karimi M. Evaluation of the FXIII deficiency prophylaxis intervals in large number of FXIII deficiency patients from Iran. Haemophilia 2013; 19 (3) e175-e176
    CrossrefPubMedGoogle Scholar
  • 56 Ashley C, Chang E, Davis J, Mangione A, Frame V, Nugent DJ. Efficacy and safety of prophylactic treatment with plasma-derived factor XIII concentrate (human) in patients with congenital factor XIII deficiency. Haemophilia 2015; 21 (1) 102-108
    CrossrefPubMedGoogle Scholar
  • 57 Nugent DJ, Ashley C, García-Talavera J, Lo LC, Mehdi AS, Mangione A. Pharmacokinetics and safety of plasma-derived factor XIII concentrate (human) in patients with congenital factor XIII deficiency. Haemophilia 2015; 21 (1) 95-101
    PubMedGoogle Scholar
  • 58 Lusher J, Pipe SW, Alexander S, Nugent D. Prophylactic therapy with fibrogammin P is associated with a decreased incidence of bleeding episodes: a retrospective study. Haemophilia 2010; 16 (2) 316-321
    CrossrefPubMedGoogle Scholar
  • 59 Fujii N, Souri M, Ichinose A. A short half-life of the administered factor XIII (FXIII) concentrates after the first replacement therapy in a newborn with severe congenital FXIII deficiency. Thromb Haemost 2012; 107 (3) 592-594
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 60 Janbain M, Nugent DJ, Powell JS, St-Louis J, Frame VB, Leissinger CA. Use of Factor XIII (FXIII) concentrate in patients with congenital FXIII deficiency undergoing surgical procedures. Transfusion 2015; 55 (1) 45-50
    CrossrefPubMedGoogle Scholar
  • 61 Lovejoy AE, Reynolds TC, Visich JE , et al. Safety and pharmacokinetics of recombinant factor XIII-A2 administration in patients with congenital factor XIII deficiency. Blood 2006; 108 (1) 57-62
    CrossrefPubMedGoogle Scholar
  • 62 Inbal A, Oldenburg J, Carcao M, Rosholm A, Tehranchi R, Nugent D. Recombinant factor XIII: a safe and novel treatment for congenital factor XIII deficiency. Blood 2012; 119 (22) 5111-5117
    CrossrefPubMedGoogle Scholar
  • 63 Brand-Staufer B, Carcao M, Kerlin BA , et al. Pharmacokinetic characterization of recombinant factor XIII (FXIII)-A2 across age groups in patients with FXIII A-subunit congenital deficiency. Haemophilia 2015; 21 (3) 380-385
    CrossrefPubMedGoogle Scholar
  • 64 Williams M, Will A, Stenmo C, Rosholm A, Tehranchi R. Pharmacokinetics of recombinant factor XIII in young children with congenital FXIII deficiency and comparison with older patients. Haemophilia 2014; 20 (1) 99-105
    PubMedGoogle Scholar
  • 65 Kerlin B, Brand B, Inbal A , et al. Pharmacokinetics of recombinant factor XIII at steady state in patients with congenital factor XIII A-subunit deficiency. J Thromb Haemost 2014; 12 (12) 2038-2043
    CrossrefPubMedGoogle Scholar
  • 66 Árokszállási A, Kerényi A, Katona É , et al. The use of recombinant factor XIII in a major bleeding episode of a patient with congenital factor XIII deficiency—the first experience. Haemophilia 2015; 21 (1) e118-e121
    CrossrefPubMedGoogle Scholar
  • 67 Lorand L, Urayama T, De Kiewiet JW, Nossel HL. Diagnostic and genetic studies on fibrin-stabilizing factor with a new assay based on amine incorporation. J Clin Invest 1969; 48 (6) 1054-1064
    CrossrefPubMedGoogle Scholar
  • 68 Godal HC. An inhibitor to fibrin stabilizing factor (FSF, factor XIII). Scand J Haematol 1970; 7 (1) 43-48
    PubMedGoogle Scholar
  • 69 Seiving B, Henriksson P, Stenberg P, Nilsson IM. A reversed activity staining procedure for detection of an acquired antibody against factor XIII in a girl with factor XIII deficiency. Br J Haematol 1992; 82 (2) 414-416
    CrossrefPubMedGoogle Scholar
  • 70 Rivard GE, St Louis J, Lacroix S, Champagne M, Rock G. Immunoadsorption for coagulation factor inhibitors: a retrospective critical appraisal of 10 consecutive cases from a single institution. Haemophilia 2003; 9 (6) 711-716
    CrossrefPubMedGoogle Scholar
  • 71 Pénzes K, Vezina C, Bereczky Z , et al. Alloantibody developed in a factor XIII A subunit deficient patient during substitution therapy; characterization of the antibody. Haemophilia 2015;
    PubMedGoogle Scholar
  • 72 Wada H, Souri M, Matsumoto R, Sugihara T, Ichinose A. Alloantibodies against the B subunit of plasma factor XIII developed in its congenital deficiency. Thromb Haemost 2013; 109 (4) 661-668
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 73 Tosetto A, Castaman G, Rodeghiero F. Acquired plasma factor XIII deficiencies. Haematologica 1993; 78 (6) (Suppl. 02) 5-10
    PubMedGoogle Scholar
  • 74 Franchini M, Frattini F, Crestani S, Bonfanti C. Acquired FXIII inhibitors: a systematic review. J Thromb Thrombolysis 2013; 36 (1) 109-114
    CrossrefPubMedGoogle Scholar
  • 75 Ichinose A, Osaki T, Souri M ; The Japanese Collaborative Research Group (JCRG) on AH13 (supported by the Japanese Ministry of Health, Labor, and Welfare). Clinical features of 32 new Japanese cases with autoimmune haemorrha-philia due to anti-factor XIII antibodies. Haemophilia 2015; 21 (5) 653-658
    CrossrefPubMedGoogle Scholar
  • 76 Lorand L. Acquired inhibitors of fibrin stabilization: a class of hemorrhagic disorders of diverse origins. In: Green D, ed. Anticoagulants: Physiologic, Pathologic and Pharmacologic. Boca Raton, FL: CRC Press; 1994: 169-191
    Google Scholar
  • 77 Kessel R, Hu C, Shore-Lesserson L, Rand J, Manwani D. A child with acquired factor XIII deficiency: case report and literature review. Haemophilia 2013; 19 (6) 814-826
    CrossrefPubMedGoogle Scholar
  • 78 Boehlen F, Casini A, Chizzolini C , et al. Acquired factor XIII deficiency: a therapeutic challenge. Thromb Haemost 2013; 109 (3) 479-487
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 79 Lodemann P, Kolbeck H, Held TK , et al. Acquired deficiency of coagulation factor XIII—possible evidence for a new link between coagulation and infection from a case. Ann Hematol 2013; 92 (3) 427-429
    CrossrefPubMedGoogle Scholar
  • 80 Ajzner E, Schlammadinger A, Kerényi A , et al. Severe bleeding complications caused by an autoantibody against the B subunit of plasma factor XIII: a novel form of acquired factor XIII deficiency. Blood 2009; 113 (3) 723-725
    CrossrefPubMedGoogle Scholar
  • 81 Lorand L. Hemorrhagic disorders of fibrin stabilization. In: Ogston D, Bennet B, ed. Hemostasis: Biochemistry, Physiology and Pathology. London, UK: Wiley; 1977: 290-294
    Google Scholar
  • 82 Fukue H, Anderson K, McPhedran P, Clyne L, McDonagh J. A unique factor XIII inhibitor to a fibrin-binding site on factor XIIIA. Blood 1992; 79 (1) 65-74
    PubMedGoogle Scholar
  • 83 Hayashi T, Kadohira Y, Morishita E, Asakura H, Souri M, Ichinose A. A case of acquired FXIII deficiency with severe bleeding symptoms. Haemophilia 2012; 18 (4) 618-620
    CrossrefPubMedGoogle Scholar
  • 84 Peyvandi F, Tagliabue L, Menegatti M , et al. Phenotype-genotype characterization of 10 families with severe a subunit factor XIII deficiency. Hum Mutat 2004; 23 (1) 98
    PubMedGoogle Scholar