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Acquired factor XIII deficiency: A review

Published:October 30, 2018DOI:https://doi.org/10.1016/j.transci.2018.10.013

      Abstract

      Acquired factor XIII (FXIII) deficiency is a rare bleeding disorder that can manifest with spontaneous or delayed life-threatening hemorrhage. Causes of acquired deficiency include immune-mediated inhibition, as well as non-immune FXIII hyperconsumption or hyposynthesis. The occurrence of acquired FXIII deficiency can be idiopathic or may be associated with comorbidities, such as malignancies or autoimmune disorders. Recognition of acquired FXIII deficiency and its underlying cause is imperative, as treatment options vary depending on the etiology. Diagnosis requires quantitative FXIII testing in addition to supplemental inhibitor studies if the clinical situation suggests an immune-mediated pathophysiology. Treatment may involve FXIII replacement, antifibrinolytic administration, and/or inhibitor eradication. However, treatment targets and thresholds are undefined in acquired FXIII deficiency. This review will focus on the clinical characteristics, diagnostic issues and therapeutic options for both immune and non-immune acquired FXIII deficiency. Cases are described to illustrate the clinical features of acquired FXIII deficiency.

      Keywords

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      References

        • Muszbek L.
        • Bereczky Z.
        • Bagoly Z.
        • Komaromi I.
        • Katona E.
        Factor XIII: a coagulation factor with multiple plasmatic and cellular functions.
        Physiol Rev. 2011; 91: 931-972https://doi.org/10.1152/physrev.00016.2010
        • Komáromi I.
        • Bagoly Z.
        • Muszbek L.
        Factor XIII: novel structural and functional aspects.
        J Thromb Haemost. 2011; 9: 9-20https://doi.org/10.1111/j.1538-7836.2010.04070.x
        • Lorand L.
        Factor XIII: structure, activation, and interactions with fibrinogen and fibrin.
        Ann N Y Acad Sci. 2001; 936: 291-311
        • Souri M.
        • Kaetsu H.
        • Ichinose A.
        Sushi domains in the B subunit of factor XIII responsible for oligomer assembly.
        Biochemistry. 2008; 47: 8656-8664https://doi.org/10.1021/bi8006143
        • Inbal A.
        • Dardik R.
        Role of coagulation factor XIII (FXIII) in angiogenesis and tissue repair.
        Pathophysiol Haemost Thromb. 2006; 35: 162-165https://doi.org/10.1159/000093562
        • Dorgalaleh A.
        • Naderi M.
        • Hosseini M.S.
        • Alizadeh S.
        • Hosseini S.
        • Tabibian S.
        • et al.
        Factor XIII deficiency in Iran: a comprehensive review of the literature.
        Semin Thromb Hemost. 2015; 41: 323-329https://doi.org/10.1055/s-0034-1395350
        • Schroeder V.
        • Kohler H.P.
        Factor XIII deficiency: an update.
        Semin Thromb Hemost. 2013; 39: 632-641https://doi.org/10.1055/s-0033-1353392
        • Lorand L.
        • Velasco P.T.
        • Rinne J.R.
        • Amare M.
        • Miller L.K.
        • Zucker M.L.
        Autoimmune antibody (IgG Kansas) against the fibrin stabilizing factor (factor XIII) system.
        Proc Natl Acad Sci U S A. 1988; 85: 232-236
        • Levy J.H.
        • Greenberg C.
        Biology of Factor XIII and clinical manifestations of Factor XIII deficiency.
        Transfusion. 2013; 53: 1120-1131https://doi.org/10.1111/j.1537-2995.2012.03865.x
        • Muszbek L.
        • Katona E.
        Diagnosis and management of congenital and acquired FXIII deficiencies.
        Semin Thromb Hemost. 2016; 1https://doi.org/10.1055/s-0036-1572326
        • Ichinose A.
        Autoimmune acquired factor XIII deficiency due to anti-factor XIII/13 antibodies: a summary of 93 patients.
        Blood Rev. 2017; 31: 37-45https://doi.org/10.1016/j.blre.2016.08.002
        • Luo Y.Y.
        • Zhang G.S.
        Acquired factor XIII inhibitor: clinical features, treatment, fibrin structure and epitope determination.
        Haemophilia. 2011; 17: 393-398https://doi.org/10.1111/j.1365-2516.2010.02459.x
        • Dorgalaleh A.
        • Rashidpanah J.
        Blood coagulation factor XIII and factor XIII deficiency.
        Blood Rev. 2016; 30: 461-475https://doi.org/10.1016/j.blre.2016.06.002
        • Kohler H.P.
        • Ichinose A.
        • Seitz R.
        • Ariens R.A.S.
        • Muszbek L.
        Diagnosis and classification of factor XIII deficiencies.
        J Thromb Haemost. 2011; 9: 1404-1406https://doi.org/10.1111/j.1538-7836.2011.04315.x
        • 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: 814-826https://doi.org/10.1111/hae.12145
        • Katona É
        • Pénzes K.
        • Molnár É
        • Muszbek L.
        Measurement of factor XIII activity in plasma.
        Clin Chem Lab Med. 2012; 50: 1191-1202https://doi.org/10.1515/cclm-2011-0730
        • Duncan E.M.
        • Dale B.J.
        • Lloyd J.V.
        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: 340-348https://doi.org/10.1097/MBC.0000000000000037
        • Hsu P.
        • Zantek N.D.
        • Meijer P.
        • Hayward C.P.M.
        • Brody J.
        • Zhang X.
        • 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: 232-238https://doi.org/10.1055/s-0034-1365841
        • Ichinose A.
        • Kohler H.P.
        • Philippou H.
        • et al.
        Recommendation for ISTH/SSC Criterion 2015 for autoimmune acquired factor XIII/13 deficiency.
        Thromb Haemost. 2016; 116: 772-774https://doi.org/10.1160/TH16-05-0362
        • Ajzner E.
        • Muszbek L.
        Kinetic spectrophotometric factor XIII activity assays: the subtraction of plasma blank is not omissible [corrected].
        J Thromb Haemost. 2004; 2: 2075-2077https://doi.org/10.1111/j.1538-7836.2004.00986.x
        • 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: 268-273
        • 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: 127-135
        • Franchini M.
        • Frattini F.
        • Crestani S.
        • Bonfanti C.
        Acquired FXIII inhibitors: a systematic review.
        J Thromb Thrombolysis. 2013; 36: 109-114https://doi.org/10.1007/s11239-012-0818-3
        • Tone K.J.
        • James T.E.
        • Fergusson D.A.
        • Tinmouth A.
        • Tay J.
        • Avey M.T.
        • et al.
        Acquired factor XIII inhibitor in hospitalized and perioperative patients: a systematic review of case reports and case series.
        Transfus Med Rev. 2016; 30: 123-131https://doi.org/10.1016/j.tmrv.2016.04.001
        • Ahmad F.
        • Solymoss S.
        • Poon M.C.
        • Berube C.
        • Sullivan A.K.
        Characterization of an acquired IgG inhibitor of coagulation factor XIII in a patient with systemic lupus erythematosus.
        Br J Haematol. 1996; 93: 700-703
        • Lim W.
        • Moffat K.
        • Hayward C.P.M.
        Prophylactic and perioperative replacement therapy for acquired factor XIII deficiency.
        J Thromb Haemost. 2004; 2: 1017-1019https://doi.org/10.1111/j.1538-7836.2004.00728.x
        • Milner G.R.
        • Holt P.J.
        • Bottomley J.
        • Maciver J.E.
        Practolol therapy associated with a systemic lupus erythematosus-like syndrome and an inhibitor to factor XIII.
        J Clin Pathol. 1977; 30: 770-773
        • Lopaciuk S.
        • Bykowska K.
        • McDonagh J.M.
        • McDonagh R.P.
        • Yount W.J.
        • Fuller C.R.
        • et al.
        Difference between type I autoimmune inhibitors of fibrin stabilization in two patients with severe hemorrhagic disorder.
        J Clin Invest. 1978; 61: 1196-1203https://doi.org/10.1172/JCI109035
        • Gailani D.
        An IgG inhibitor against coagulation factor XIII: resolution of bleeding after plasma immunoadsorption with staphylococcal protein A.
        Am J Med. 1992; 92: 110-112
        • Miesbach W.
        Rituximab in the treatment of factor XIII inhibitor possibly caused by Ciprofloxacin.
        Thromb Haemost. 2005; 93: 1001-1003
        • Ajzner É
        • Schlammadinger Á
        • Kerényi A.
        • Bereczky Z.
        • Katona É
        • Haramura G.
        • 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: 723-725https://doi.org/10.1182/blood-2008-09-179333
        • Souri M.
        • Osaki T.
        • Ichinose A.
        Anti-factor XIII A subunit (FXIII-A) autoantibodies block FXIII-A 2 B 2 assembly and steal FXIII-A from native FXIII-A 2 B 2.
        J Thromb Haemost. 2015; 13: 802-814https://doi.org/10.1111/jth.12877
        • Lorand L.
        Hemorrhagic disorders of fibrin stabilization.
        in: Ogston D. Bennet B. Hemost. biochem. physiol. pathol. Wiley, London, UK1977: 290-294
        • Lorand L.
        • Maldonado N.
        • Fradera J.
        • Atencio A.C.
        • Robertson B.
        • Urayama T.
        Haemorrhagic syndrome of autoimmune origin with a specific inhibitor against fibrin stabilizing factor (factor XIII).
        Br J Haematol. 1972; 23: 17-27https://doi.org/10.1111/j.1365-2141.1972.tb03455.x
        • 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: 65-74
        • 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: 618-620https://doi.org/10.1111/j.1365-2516.2012.02763.x
        • 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: 661-668https://doi.org/10.1160/TH12-12-0936
        • Pénzes K.
        • Vezina C.
        • Bereczky Z.
        • Katona É
        • Kun M.
        • Muszbek L.
        • et al.
        Alloantibody developed in a factor XIII A subunit deficient patient during substitution therapy; characterization of the antibody.
        Haemophilia. 2015; 22: 268-275https://doi.org/10.1111/hae.12786
        • Nijenhuis a V.M.
        • van Bergeijk L.
        • Huijgens P.C.
        • Zweegman S.
        Acquired factor XIII deficiency due to an inhibitor: a case report and review of the literature.
        Haematologica. 2004; 89: ECR14
        • Boehlen F.
        • Casini A.
        • Chizzolini C.
        • Mansouri B.
        • Kohler H.P.
        • Schroeder V.
        • et al.
        Acquired factor XIII deficiency: a therapeutic challenge.
        Thromb Haemost. 2013; 109: 479-487https://doi.org/10.1160/TH12-08-0604
        • Ngo Sack F.
        • Galinat H.
        • Egreteau P.-Y.
        • Mollard L.M.
        • Fortin H.
        • Berthou C.
        • et al.
        Efficacy of rituximab in acquired factor XIII inhibitor after arterial rFVIIa-induced thrombosis.
        Haemophilia. 2013; 19: e93-4https://doi.org/10.1111/hae.12069
        • Rivard G.E.
        • 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: 711-716
        • Otis P.T.
        • Feinstein D.I.
        • Rapaport S.I.
        • Patch M.J.
        An acquired inhibitor of fibrin stabilization associated with isoniazid therapy: clinical and biochemical observations.
        Blood. 1974; 44: 771-781
        • Rosenberg R.D.
        • Colman R.W.
        • Lorand L.
        A new haemorrhagic disorder with defective fibrin stabilization and cryofibrinogenaemia.
        Br J Haematol. 1974; 26: 269-284
        • Ichinose A.
        Hemorrhagic acquired factor XIII (13) deficiency and acquired hemorrhaphilia 13 revisited.
        Semin Thromb Hemost. 2011; 37: 382-388https://doi.org/10.1055/s-0031-1276587
        • Seitz R.
        • Leugner F.
        • Katschinski M.
        • Immel A.
        • Kraus M.
        • Egbring R.
        • et al.
        Ulcerative colitis and Crohn’s disease: factor XIII, inflammation and haemostasis.
        Digestion. 1994; 55: 361-367https://doi.org/10.1159/000201166
        • Kohler H.P.
        • Ariëns R.A.S.
        • Catto A.J.
        • Carter A.M.
        • Miller G.J.
        • Cooper J.A.
        • et al.
        Factor XIII A-subunit concentration predicts outcome in stroke subjects and vascular outcome in healthy, middle-aged men.
        Br J Haematol. 2002; 118: 825-832
        • Kucher N.
        • Schroeder V.
        • Kohler H.P.
        Role of blood coagulation factor XIII in patients with acute pulmonary embolism. Correlation of factor XIII antigen levels with pulmonary occlusion rate, fibrinogen, D-dimer, and clot firmness.
        Thromb Haemost. 2003; 90: 434-438https://doi.org/10.1160/TH03-07-0031
        • Prenzel F.
        • Pfaffle R.
        • Thiele F.
        • Schuster V.
        Decreased factor XIII activity during severe Henoch-Schoenlein purpura – does it play a role?.
        Klin Padiatr. 2006; 218: 174-176https://doi.org/10.1055/s-2006-933401
        • Zeerleder S.
        • Schroeder V.
        • Lämmle B.
        • Wuillemin W.A.
        • Hack C.E.
        • Kohler H.P.
        Factor XIII in severe sepsis and septic shock.
        Thromb Res. 2007; 119: 311-318https://doi.org/10.1016/j.thromres.2006.02.003
        • Lodemann P.
        • Kolbeck H.
        • Held T.K.
        • Ivaskevicius V.
        • Oldenburg J.
        • Schweigerer L.
        • 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: 427-429https://doi.org/10.1007/s00277-012-1582-3
        • Wettstein P.
        • Haeberli A.
        • Stutz M.
        • Rohner M.
        • Corbetta C.
        • Gabi K.
        • et al.
        Decreased factor XIII availability for thrombin and early loss of clot firmness in patients with unexplained intraoperative bleeding.
        Anesth Analg. 2004; 99: 1564-1569https://doi.org/10.1213/01.ANE.0000134800.46276.21
        • Gando S.
        • Kamiya K.
        • Makise H.
        • Tedo I.
        • Nakanishi Y.
        Wound healing, blood coagulation and fibrinolysis during operations involving gastric cancer surgery.
        Nihon Geka Gakkai Zasshi. 1989; 90: 59-63
        • Gerlach R.
        • Tölle F.
        • Raabe A.
        • Zimmermann M.
        • Siegemund A.
        • Seifert V.
        Increased risk for postoperative hemorrhage after intracranial surgery in patients with decreased factor XIII activity: implications of a prospective study.
        Stroke. 2002; 33: 1618-1623https://doi.org/10.1161/01.STR.0000017219.83330.FF
        • Gödje O.
        • Gallmeier U.
        • Schelian M.
        • Grünewald M.
        • Mair H.
        Coagulation factor XIII reduces postoperative bleeding after coronary surgery with extracorporeal circulation.
        Thorac Cardiovasc Surg. 2006; 54: 26-33https://doi.org/10.1055/s-2005-872853
        • Korte W.C.
        • Szadkowski C.
        • Ga A.
        • Gabi K.
        Factor XIII substitution in surgical cancer patients at high risk for intraoperative bleeding.
        2009: 239-245
        • Kanda A.
        • Kaneko K.
        • Obayashi O.
        • Mogami A.
        • Presentation C.
        The massive bleeding after the operation of hip joint surgery with the acquired haemorrhagic coagulation factor XIII(13) deficiency: two case reports.
        Case Rep Orthop. 2013; 2013: 3-7
        • Lison S.
        • Weiss G.
        • Spannagl M.
        • Heindl B.
        Postoperative changes in procoagulant factors after major surgery.
        Blood Coagul Fibrinolysis. 2011; 22: 190-196https://doi.org/10.1097/MBC.0b013e328343f7be
        • Von Rappard S.
        • Hinnen C.
        • Lussmann R.
        • Rechsteiner M.
        • Korte W.
        Factor XIII deficiency and thrombocytopenia are frequent modulators of postoperative clot firmness in a surgical intensive care unit.
        Transfus Med Hemother. 2017; 44: 85-92https://doi.org/10.1159/000468946
        • Blome M.
        • Isgro F.
        • Kiessling A.H.
        • Skuras J.
        • Haubelt H.
        • Hellstern P.
        • et al.
        Relationship between factor XIII activity, fibrinogen, haemostasis screening tests and postoperative bleeding in cardiopulmonary bypass surgery.
        Thromb Haemost. 2005; 94: 853-858https://doi.org/10.1160/TH04-12-0799
        • Adelmann D.
        • Klaus D.A.
        • Illievich U.M.
        • Krenn C.G.
        • Krall C.
        • Kozek-Langenecker S.
        • et al.
        Fibrinogen but not factor XIII deficiency is associated with bleeding after craniotomy.
        Br J Anaesth. 2014; 113: 628-633https://doi.org/10.1093/bja/aeu133
        • Chamouard P.
        • Grunebaum L.
        • Wiesel M.L.
        • Sibilia J.
        • Coumaros G.
        • Wittersheim C.
        • et al.
        Significance of diminished factor XIII in Crohn’s disease.
        Am J Gastroenterol. 1998; 93: 610-614https://doi.org/10.1111/j.1572-0241.1998.174_b.x
        • Hayat M.
        • Ariëns R.A.S.
        • Moayyedi P.
        • Grant P.J.
        • O’Mahony S.
        Coagulation factor XIII and markers of thrombin generation and fibrinolysis in patients with inflammatory bowel disease.
        Eur J Gastroenterol Hepatol. 2002; 14: 249-256https://doi.org/10.1097/00042737-200203000-00008
        • Van Bodegraven A.A.
        • Tuynman H.A.R.E.
        • Schoorl M.
        • Kruishoop A.M.
        • Bartels P.C.M.
        Fibrinolytic split products, fibrinolysis, and factor XIII activity in inflammatory bowel disease.
        Scand J Gastroenterol. 1995; 30: 580-585https://doi.org/10.3109/00365529509089793
        • Shin J.I.
        • Lee J.S.
        Severe gastrointestinal vasculitis in Henoch-Schoenlein purpura: pathophysiologic mechanisms, the diagnostic value of factor XIII, and therapeutic options [1].
        Eur J Pediatr. 2007; 166: 1199-1200https://doi.org/10.1007/s00431-007-0415-1
        • Sano H.
        • Izumida M.
        • Shimizu H.
        • Ogawa Y.
        Risk factors of renal involvement and significant proteinuria in Henoch-Schönlein purpura.
        Eur J Pediatr. 2002; 161: 196-201https://doi.org/10.1007/s00431-002-0922-z
        • Kamitsuji H.
        • Tani K.
        • Yasui M.
        • Taniguchi A.
        • Taira K.
        • Tsukada S.
        • et al.
        Activity of blood coagulation Factor XIII as a prognostic indicator in patients with Henoch-Schönlein purpura - Efficacy of Factor XIII substitution.
        Eur J Pediatr. 1987; 146: 519-523https://doi.org/10.1007/BF00441608
        • Suzuki R.
        • Toda H.
        • Takamura Y.
        Dynamics of blood coagulation factor XIII in ulcerative colitis and preliminary study of the factor XIII concentrate.
        Blut. 1989; 59: 162-164https://doi.org/10.1007/BF00320061
        • Lorenz R.
        • Heinmüller M.
        • Classen M.
        • Tornieporth N.
        • Gain T.
        Substitution of factor XIII: a therapeutic approach to ulcerative colitis.
        Haemostasis. 1991; 21: 5-9
        • Utani A.
        • Ohta M.
        • Shinya A.
        • Ohno S.
        • Takakuwa H.
        • Yamamoto T.
        • et al.
        Successful treatment of adult Henoch-Schonlein purpura with factor XIII concentrate.
        J Am Acad Dermatol. 1991; 24: 438-442https://doi.org/10.1016/0190-9622(91)70068-D
        • Shimomura N.
        • Kawai K.
        • Watanabe S.
        • Katsuumi K.
        • Ito M.
        Adult Henoch-Schönlein purpura with severe abdominal pain treated with dapsone and factor XIII concentrate.
        J Dermatol. 2005; 32: 124-127
        • Tacke F.
        • Fiedler K.
        • Depka M.
        • Luedde T.
        • Hecker H.
        • Manns M.P.
        • et al.
        Clinical and prognostic role of plasma coagulation factor XIII activity for bleeding disorders and 6-year survival in patients with chronic liver disease.
        Liver Int. 2006; 26: 173-181https://doi.org/10.1111/j.1478-3231.2005.01205.x
        • Wiegering V.
        • Andres O.
        • Schlegel P.G.
        • Deinlein F.
        • Eyrich M.
        • Sturm A.
        Hyperfibrinolysis and acquired factor XIII deficiency in newly diagnosed pediatric malignancies.
        Haematologica. 2013; 98: 5-6https://doi.org/10.3324/haematol.2013.089045
        • Peck-Radosavljevic M.
        Review article: coagulation disorders in chronic liver disease.
        Aliment Pharmacol Ther. 2007; 26: 21-28https://doi.org/10.1111/j.1365-2036.2007.03509.x
        • Petri M.
        • Ellman L.
        • Carey R.
        Acquired factor XIII deficiency with chronic myelomonocytic leukemia.
        Ann Intern Med. 1983; 99https://doi.org/10.7326/0003-4819-99-5-638
        • Teich M.
        • Longin E.
        • Dempfle C.E.
        • König S.
        Factor XIII deficiency associated with valproate treatment.
        Epilepsia. 2004; 45: 187-189https://doi.org/10.1111/j.0013-9580.2004.28302.x
        • Mokuda S.
        • Murata Y.
        • Sawada N.
        • Matoba K.
        • Yamada A.
        • Onishi M.
        • et al.
        Tocilizumab induced acquired factor XIII deficiency in patients with rheumatoid arthritis.
        PLoS One. 2013; 8https://doi.org/10.1371/journal.pone.0069944
        • 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: 5111-5117https://doi.org/10.1182/blood-2011-10-386045
        • Solomon C.
        • Korte W.
        • Fries D.
        • Pendrak I.
        • Joch C.
        • Gröner A.
        • et al.
        Safety of factor XIII concentrate: analysis of more than 20 years of pharmacovigilance data.
        Transfus Med Hemother. 2016; 43: 365-373https://doi.org/10.1159/000446813
        • Dreyfus M.
        • Barrois D.
        • Borg J.-Y.
        • Claeyssens S.
        • Torchet M.-F.
        • Arnuti B.
        • et al.
        Successful long-term replacement therapy with FXIII concentrate (Fibrogammin® P) for severe congenital factor XIII deficiency: a prospective multicentre study.
        J Thromb Haemost. 2011; 9: 1264-1266https://doi.org/10.1111/j.1538-7836.2011.04281.x
        • Karkouti K.
        • von Heymann C.
        • Jespersen C.M.
        • Korte W.
        • Levy J.H.
        • Ranucci M.
        • et al.
        Efficacy and safety of recombinant factor XIII on reducing blood transfusions in cardiac surgery: a randomized, placebo-controlled, multicenter clinical trial.
        J Thorac Cardiovasc Surg. 2013; 146: 927-939https://doi.org/10.1016/j.jtcvs.2013.04.044
        • Caudill J.S.C.
        • Nichols W.L.
        • Plumhoff E.A.
        • Schulte S.L.
        • Winters J.L.
        • Gastineau D.A.
        • et al.
        Comparison of coagulation factor XIII content and concentration in cryoprecipitate and fresh-frozen plasma.
        Transfusion. 2009; 49: 765-770https://doi.org/10.1111/j.1537-2995.2008.02021.x
        • Mitchell J.L.
        • Lionikiene A.S.
        • Fraser S.R.
        • Whyte C.S.
        • Booth N.A.
        • Mutch N.J.
        Functional factor XIII-A is exposed on the stimulated platelet surface.
        Blood. 2014; 124: 3982-3990https://doi.org/10.1182/blood-2014-06-583070
        • Lorand L.
        • Velasco P.T.
        • Murthy S.N.
        • Lefebvre P.
        • Green D.
        Autoimmune antibody in a hemorrhagic patient interacts with thrombin-activated factor XIII in a unique manner.
        Blood. 1999; 93: 909-917
        • 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: 396-401https://doi.org/10.1097/MBC.0b013e328345f566
        • Janbain M.
        • Nugent D.J.
        • Powell J.S.
        • St-Louis J.
        • Frame V.B.
        • Leissinger C.A.
        Use of Factor XIII (FXIII) concentrate in patients with congenital FXIII deficiency undergoing surgical procedures.
        Transfusion. 2015; 55: 45-50https://doi.org/10.1111/trf.12784