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Thromb Haemost 2011; 105(01): 5-13
DOI: 10.1160/TH10-08-0504
Review Article
Schattauer GmbH

ABO blood group as a potential risk factor for venous thromboembolism in acutely injured patients

Sarah K. Muellner
1   Center for Translational Injury Research, Houston, Texas, USA
,
Elliott R. Haut
2   Department of Surgery, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA
,
Michael B. Streiff
3   Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA
4   Johns Hopkins Anticoagulation Service and Outpatient Clinics, Baltimore, Maryland, USA
,
John B. Holcomb
1   Center for Translational Injury Research, Houston, Texas, USA
5   Department of Surgery, University of Texas Health Science Center, Houston, Texas, USA
,
Bryan A. Cotton
1   Center for Translational Injury Research, Houston, Texas, USA
5   Department of Surgery, University of Texas Health Science Center, Houston, Texas, USA
› Author Affiliations
Further Information

Publication History

Received: 01 August 2010

Accepted after minor revision: 23 September 2010

Publication Date:
22 November 2017 (online)

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Summary

Venous thromboembolism (VTE) is a major health problem that results in a significant burden on hospitals and patients. VTE screening and prophylaxis protocols in trauma patients vary significantly among hospitals and providers. In addition, many patients develop VTE even in the absence of “high-risk” categories. Therefore, more research is needed to better understand and prevent VTE in these patients. ABO blood group has long been recognised as a risk factor for VTE, but its contribution to VTE risk in the trauma setting is poorly studied. This paper reviews the literature describing the link between ABO blood group and VTE risk and the implications for VTE screening and prophylaxis in trauma patients. The effect of ABO blood groups are genotype-dependent – in most populations the A1 allele and the B allele increase risk while A2, O1, and O2 decrease risk of VTE. ABO group is a major determinant of plasma von Willebrand factor (vWF) and factor VIII levels, thereby (partially) mediating the effects of ABO blood group on VTE susceptibility. In addition, ABH antigens alter plasma levels of vWF via clearance mechanisms, which are in turn mediated by ADAMTS13. ABO blood group is a risk factor for VTE that warrants further investigation in trauma patients.

Keywords

Deep-vein thrombosis - hypercoagulability - pulmonary embolism - surgery - venous thrombosis
 

  • References

  • 1 Heit JA. et al. Incidence of venous thromboembolism in hospitalized patients vs community residents. Mayo Clin Proc 2001; 76: 1102-1110.
    CrossrefPubMedGoogle Scholar
  • 2 Cundiff DK. Anticoagulation therapy for venous thromboembolism. MedGenMed 2004; 06: 5.
    PubMedGoogle Scholar
  • 3 Hull RD. et al. Cost-effectiveness of pulmonary embolism diagnosis. Arch Intern Med 1996; 156: 68-72.
    CrossrefPubMedGoogle Scholar
  • 4 White RH. The epidemiology of venous thromboembolism. Circulation 2003; 107 23 Suppl 1 I4-8.
    PubMedGoogle Scholar
  • 5 Geerts WH. et al. Prevention of venous thromboembolism: the Seventh ACCP Conference on Antithrombotic and Thrombolytic Therapy. Chest 2004; 126 (Suppl. 03) 338S-400S.
    CrossrefPubMedGoogle Scholar
  • 6 Prevention of venous thrombosis and pulmonary embolism.. NIH Consensus Development. J Am Med Assoc 1986; 256: 744-749.
    CrossrefPubMedGoogle Scholar
  • 7 Anderson Jr. FA, Wheeler HB. Physician practices in the management of venous thromboembolism: a community-wide survey. J Vasc Surg 1992; 16: 707-714.
    CrossrefPubMedGoogle Scholar
  • 8 Paciaroni M. et al. Prevention of venous thromboembolism after acute spinal cord injury with low-dose heparin or low-molecular-weight heparin. Thromb Haemost 2008; 99: 978-980.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 9 Hitos K, Fletcher JP. Venous thromboembolism and fractured neck of femur. Thromb Haemost 2005; 94: 991-996.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 10 Gando S. et al. Combined activation of coagulation and inflammation has an important role in multiple organ dysfunction and poor outcome after severe trauma. Thromb Haemost 2002; 88: 943-949.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 11 Gando S. et al. Significant correlations between tissue factor and thrombin markers in trauma and septic patients with disseminated intravascular coagulation. Thromb Haemost 1998; 79: 1111-1115.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 12 Sevitt S, Gallagher N. Venous thrombosis and pulmonary embolism. A clinico-pathological study in injured and burned patients. Br J Surg 1961; 48: 475-489.
    CrossrefPubMedGoogle Scholar
  • 13 Geerts WH. et al. A prospective study of venous thromboembolism after major trauma. N Engl J Med 1994; 331: 1601-1606.
    CrossrefPubMedGoogle Scholar
  • 14 Azu MC. et al. Venous thromboembolic events in hospitalized trauma patients. Am Surg 2007; 73: 1228-1231.
    PubMedGoogle Scholar
  • 15 Carter YM. et al. Deep venous thrombosis and ABO blood group are unrelated in trauma patients. J Trauma 2002; 52: 112-116.
    PubMedGoogle Scholar
  • 16 Knudson MM. et al. Thromboembolism after trauma: an analysis of 1602 episodes from the American College of Surgeons National Trauma Data Bank. Ann Surg 2004; 240: 490-498.
    CrossrefPubMedGoogle Scholar
  • 17 Piotrowski JJ. et al. Is deep vein thrombosis surveillance warranted in high-risk trauma patients?. Am J Surg 1996; 172: 210-213.
    CrossrefPubMedGoogle Scholar
  • 18 Schreiber MA. et al. Hypercoagulability is most prevalent early after injury and in female patients. J Trauma 2005; 58: 475-481.
    CrossrefPubMedGoogle Scholar
  • 19 Shackford SR. et al. Venous thromboembolism in patients with major trauma. Am J Surg 1990; 159: 365-369.
    CrossrefPubMedGoogle Scholar
  • 20 Rogers FB. et al. Practice management guidelines for the prevention of venous thromboembolism in trauma patients: the EAST practice management guidelines work group. J Trauma 2002; 53: 142-164.
    CrossrefPubMedGoogle Scholar
  • 21 van Vliet HA. et al. The effect of the levonorgestrel-releasing intrauterine system on the resistance to activated protein C (APC). Thromb Haemost 2009; 101: 691-695.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 22 Pomp ER. et al. Polymorphisms in the protein C gene as risk factor for venous thrombosis. Thromb Haemost 2009; 101: 62-67.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 23 Pai N. et al. Hereditary basis of protein C deficiency (PCD) in thrombosis patients: first report from India. Thromb Haemost 2009; 101: 785-787.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 24 Anderson Jr. FA, Spencer FA. Risk factors for venous thromboembolism. Circulation 2003; 107 23 Suppl 1 I9-16.
    CrossrefPubMedGoogle Scholar
  • 25 White RH, Keenan CR. Effects of race and ethnicity on the incidence of venous thromboembolism. Thromb Res 2009; 123 (Suppl. 04) S11-17.
    CrossrefPubMedGoogle Scholar
  • 26 Landefeld CS. Noninvasive diagnosis of deep vein thrombosis. J Am Med Assoc 2008; 300: 1696-1697.
    CrossrefPubMedGoogle Scholar
  • 27 Segal JB. et al. Review of the evidence on diagnosis of deep venous thrombosis and pulmonary embolism. Ann Fam Med 2007; 05: 63-73.
    CrossrefPubMedGoogle Scholar
  • 28 Jeger V. et al. Can RapidTEG accelerate the search for coagulopathies in the patient with multiple injuries?. J Trauma 2009; 66: 1253-1257.
    CrossrefPubMedGoogle Scholar
  • 29 Kaufmann CR. et al. Usefulness of thrombelastography in assessment of trauma patient coagulation. J Trauma 1997; 42: 716-722.
    CrossrefPubMedGoogle Scholar
  • 30 Jeeji R, Dutta S. Pitfall in interpretation of TEG results. Eur J Anaesthesiol 2008; 25: 693-694.
    CrossrefPubMedGoogle Scholar
  • 31 Geerts WH, Bergqvist D, Pineo GF. et al. Prevention of venous thromboembolism: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines (8th Edition). Chest 2008; 133 (Suppl. 06) 381S-453S.
    CrossrefPubMedGoogle Scholar
  • 32 Kelly AM, Patel S, Carlos RC. et al. Multidetector row CT pulmonary angiography and indirect venography for the diagnosis of venous thromboembolic disease in intensive care unit patients. Acad Radiol 2006; 13: 486-495.
    CrossrefPubMedGoogle Scholar
  • 33 Kluge A, Mueller C, Strunk J. et al. Experience in 207 combined MRI examinations for acute pulmonary embolism and deep vein thrombosis. AJR Am J Roentgenol 2006; 186: 1686-1696.
    CrossrefPubMedGoogle Scholar
  • 34 Beyer-Westendorf J. Safety of venous ultrasound in suspected DVT--still a matter of concern?. Thromb Haemost 2009; 102: 5-6.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 35 Brasel KJ. et al. Cost-effective prevention of pulmonary embolus in high-risk trauma patients. J Trauma 1997; 42: 456-462.
    CrossrefPubMedGoogle Scholar
  • 36 Burns GA. et al. Prospective ultrasound evaluation of venous thrombosis in high-risk trauma patients. J Trauma 1993; 35: 405-408.
    CrossrefPubMedGoogle Scholar
  • 37 Napolitano LM. et al. Asymptomatic deep venous thrombosis in the trauma patient: is an aggressive screening protocol justified?. J Trauma 1995; 39: 651-659.
    CrossrefPubMedGoogle Scholar
  • 38 Velmahos GC. et al. Inability of an aggressive policy of thromboprophylaxis to prevent deep venous thrombosis (DVT) in critically injured patients: are current methods of DVT prophylaxis insufficient?. J Am Coll Surg 1998; 187: 529-533.
    CrossrefPubMedGoogle Scholar
  • 39 Haut ER. et al. Can increased incidence of deep vein thrombosis (DVT) be used as a marker of quality of care in the absence of standardized screening? The potential effect of surveillance bias on reported DVT rates after trauma. J Trauma 2007; 63: 1132-1137.
    CrossrefPubMedGoogle Scholar
  • 40 Haut ER. et al. Predictors of posttraumatic deep vein thrombosis (DVT): hospital practice versus patient factors-an analysis of the National Trauma Data Bank (NTDB). J Trauma 2009; 66: 994-1001.
    CrossrefPubMedGoogle Scholar
  • 41 Pierce CA. et al. Surveillance bias and deep vein thrombosis in the national trauma data bank: the more we look, the more we find. J Trauma 2008; 64: 932-937.
    CrossrefPubMedGoogle Scholar
  • 42 Flinn WR. et al. Prospective surveillance for perioperative venous thrombosis. Experience in 2643 patients. Arch Surg 1996; 131: 472-480.
    CrossrefPubMedGoogle Scholar
  • 43 Masroujeh R. et al. Underutilization of venous thromboemoblism prophylaxis in medical patients in a tertiary care center. J Thromb Thrombolysis 2008; 26: 138-141.
    CrossrefPubMedGoogle Scholar
  • 44 Richardson W. et al. Guidelines for deep venous thrombosis prophylaxis during laparoscopic surgery. Surg Endosc 2007; 21: 2331-2334.
    CrossrefPubMedGoogle Scholar
  • 45 Raslan AM. et al. Prophylaxis for venous thrombo-embolism in neurocritical care: a critical appraisal. Neurocrit Care 2010; 12: 297-309.
    CrossrefPubMedGoogle Scholar
  • 46 Anonymous.. Making Health Care Safer: A Critical Analysis of Patient Safety Practices. AHRQ Publication No 01-E057 2001 [cited 2009 December 01]; http://archive.ahrq.gov/clinic/ptsafety/summary.htm.
    PubMedGoogle Scholar
  • 47 Cohen AT. et al. Venous thromboembolism risk and prophylaxis in the acute hospital care setting (ENDORSE study): a multinational cross-sectional study. Lancet 2008; 371: 387-394.
    CrossrefPubMedGoogle Scholar
  • 48 Knudson MM. et al. Thromboembolism following multiple trauma. J Trauma 1992; 32: 2-11.
    CrossrefPubMedGoogle Scholar
  • 49 Winchell RJ. et al. Risk factors associated with pulmonary embolism despite routine prophylaxis: implications for improved protection. J Trauma 1994; 37: 600-606.
    CrossrefPubMedGoogle Scholar
  • 50 Adams RC. et al. Four years of an aggressive prophylaxis and screening protocol for venous thromboembolism in a large trauma population. J Trauma 2008; 65: 300-308.
    CrossrefPubMedGoogle Scholar
  • 51 Carlin AM. et al. Prophylactic and therapeutic inferior vena cava filters to prevent pulmonary emboli in trauma patients. Arch Surg 2002; 137: 521-527.
    CrossrefPubMedGoogle Scholar
  • 52 Rogers FB. et al. Five-year follow-up of prophylactic vena cava filters in high-risk trauma patients. Arch Surg 1998; 133: 406-412.
    CrossrefPubMedGoogle Scholar
  • 53 McMurtry AL. et al. Increased use of prophylactic vena cava filters in trauma patients failed to decrease overall incidence of pulmonary embolism. J Am Coll Surg 1999; 189: 314-320.
    CrossrefPubMedGoogle Scholar
  • 54 Rodriguez JL. et al. Early placement of prophylactic vena caval filters in injured patients at high risk for pulmonary embolism. J Trauma 1996; 40: 797-804.
    CrossrefPubMedGoogle Scholar
  • 55 Morelli VM. et al. ABO blood group genotypes and the risk of venous thrombosis: effect of factor V Leiden. J Thromb Haemost 2005; 03: 183-185.
    CrossrefPubMedGoogle Scholar
  • 56 Morelli VM. et al. ABO blood group genotypes, plasma von Willebrand factor levels and loading of von Willebrand factor with A and B antigens. Thromb Haemost 2007; 97: 534-541.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 57 Procare-GEHT Group.. ABO blood group but not haemostasis genetic polymorphisms significantly influence thrombotic risk: a study of 180 homozygotes for the Factor V Leiden mutation. Br J Haematol 2006; 135: 697-702.
    CrossrefPubMedGoogle Scholar
  • 58 Jick H. et al. Venous thromboembolic disease and ABO blood type. A cooperative study. Lancet 1969; 01: 539-542.
    PubMedGoogle Scholar
  • 59 Ketch TR. et al. ABO blood types: influence on infarct size, procedural characteristics and prognosis. Thromb Res 2008; 123: 200-205.
    CrossrefPubMedGoogle Scholar
  • 60 Koster T. et al. Role of clotting factor VIII in effect of von Willebrand factor on occurrence of deep-vein thrombosis. Lancet 1995; 345: 152-155.
    CrossrefPubMedGoogle Scholar
  • 61 Mercier B. et al. Phenotypic but not allelic ABO blood group association with risk of venous thrombosis. Thromb Haemost 2005; 93: 388-389.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 62 Minano A. et al. AB0 blood group and risk of venous or arterial thrombosis in carriers of factor V Leiden or prothrombin G20210A polymorphisms. Haematologica 2008; 93: 729-734.
    CrossrefPubMedGoogle Scholar
  • 63 Ohira T. et al. ABO blood group, other risk factors and incidence of venous thromboembolism: the Longitudinal Investigation of Thromboembolism Etiology (LITE). J Thromb Haemost 2007; 05: 1455-1461.
    CrossrefPubMedGoogle Scholar
  • 64 Talbot S. et al. ABO blood-groups and venous thromboembolic disease. Lancet 1970; 01: 1257-1259.
    PubMedGoogle Scholar
  • 65 Tirado I. et al. The ABO blood group genotype and factor VIII levels as independent risk factors for venous thromboembolism. Thromb Haemost 2005; 93: 468-474.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 66 Wu O. et al. ABO(H) blood groups and vascular disease: a systematic review and meta-analysis. J Thromb Haemost 2008; 06: 62-69.
    PubMedGoogle Scholar
  • 67 Robert A, Eschwege V. Systeme de groupe sanguine ABO et thrombose veineuse profonde. Sang Thrombose Vaisseaux 2004; 16: 96-100.
    PubMedGoogle Scholar
  • 68 Schleef M. et al. Relationship between ABO and Secretor genotype with plasma levels of factor VIII and von Willebrand factor in thrombosis patients and control individuals. Br J Haematol 2004; 128: 100-107.
    PubMedGoogle Scholar
  • 69 Wiggins KL. et al. ABO genotype and risk of thrombotic events and hemorrhagic stroke. J Thromb Haemost 2009; 07: 263-269.
    CrossrefPubMedGoogle Scholar
  • 70 Paiva SG. et al. Polymorphisms in exons 6 and 7 of the ABO locus and their association with venous thrombosis in young Brazilian patients. Blood Coagul Fibrinol 2009; 20: 122-128.
    CrossrefPubMedGoogle Scholar
  • 71 Wautrecht JC. et al. The role of ABO blood groups in the incidence of deep vein thrombosis. Thromb Haemost 1998; 79: 688-689.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 72 Orstavik KH. et al. Possible effect of secretor locus on plasma concentration of factor VIII and von Willebrand factor. Blood 1989; 73: 990-993.
    PubMedGoogle Scholar
  • 73 O’Donnell J. et al. Genotype at the secretor blood group locus is a determinant of plasma von Willebrand factor level. Br J Haematol 2002; 116: 350-356.
    CrossrefPubMedGoogle Scholar
  • 74 Gallinaro L. et al. A shorter von Willebrand factor survival in O blood group subjects explains how ABO determinants influence plasma von Willebrand factor. Blood 2008; 111: 3540-3545.
    CrossrefPubMedGoogle Scholar
  • 75 Nossent AY. et al. von Willebrand factor and its propeptide: the influence of secretion and clearance on protein levels and the risk of venous thrombosis. J Thromb Haemost 2006; 04: 2556-2562.
    CrossrefPubMedGoogle Scholar
  • 76 O’Donnell J. et al. Amount of H antigen expressed on circulating von Willebrand factor is modified by ABO blood group genotype and is a major determinant of plasma von Willebrand factor antigen levels. Arterioscler Thromb Vasc Biol 2002; 22: 335-341.
    CrossrefPubMedGoogle Scholar
  • 77 O’Donnell J, Laffan MA. The relationship between ABO histo-blood group, factor VIII and von Willebrand factor. Transfus Med 2001; 11: 343-351.
    CrossrefPubMedGoogle Scholar
  • 78 Nichols TC. et al. Function of von Willebrand factor after crossed bone marrow transplantation between normal and von Willebrand disease pigs: effect on arterial thrombosis in chimeras. Proc Natl Acad Sci USA 1995; 92: 2455-2459.
    CrossrefPubMedGoogle Scholar
  • 79 Kuijpers MJ. et al. Facilitating roles of murine platelet glycoprotein Ib and alphaIIbbeta3 in phosphatidylserine exposure during vWF-collagen-induced thrombus formation. J Physiol 2004; 558: 403-415.
    CrossrefPubMedGoogle Scholar
  • 80 Ruggeri ZM. Von Willebrand factor, platelets and endothelial cell interactions. J Thromb Haemost 2003; 01: 1335-1342.
    CrossrefPubMedGoogle Scholar
  • 81 Vlot AJ. et al. Factor VIII and von Willebrand factor. Thromb Haemost 1998; 79: 456-465.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 82 Koedam JA. et al. Inactivation of human factor VIII by activated protein C. Cofactor activity of protein S and protective effect of von Willebrand factor. J Clin Invest 1988; 82: 1236-1243.
    CrossrefPubMedGoogle Scholar
  • 83 Sadler JE. et al. Impact, diagnosis and treatment of von Willebrand disease. Thromb Haemost 2000; 84: 160-174.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 84 Orstavik KH. et al. Factor VIII and factor IX in a twin population. Evidence for a major effect of ABO locus on factor VIII level. Am J Hum Genet 1985; 37: 89-101.
    PubMedGoogle Scholar
  • 85 Bowen DJ. Genome-wide linkage analysis of von Willebrand factor plasma levels implicates the ABO locus as a principal determinant: should we overlook ADAMTS13?. Thromb Haemost 2003; 90: 961 author reply 962.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 86 Souto JC. et al. Genome-wide linkage analysis of von Willebrand factor plasma levels: results from the GAIT project. Thromb Haemost 2003; 89: 468-474.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 87 Yamamoto F. et al. Molecular genetic basis of the histo-blood group ABO system. Nature 1990; 345: 229-233.
    CrossrefPubMedGoogle Scholar
  • 88 Clausen H, Hakomori S. ABH and related histo-blood group antigens; immuno-chemical differences in carrier isotypes and their distribution. Vox Sang 1989; 56: 1-20.
    CrossrefPubMedGoogle Scholar
  • 89 Oriol R. et al. Genetic regulation of the expression of ABH and Lewis antigens in tissues. APMIS Suppl 1992; 27: 28-38.
    PubMedGoogle Scholar
  • 90 Girma JP. et al. Structure-function relationship of human von Willebrand factor. Blood 1987; 70: 605-611.
    PubMedGoogle Scholar
  • 91 Matsui T. et al. ABO blood group antigens on human plasma von Willebrand factor after ABO-mismatched bone marrow transplantation. Blood 1999; 94: 2895-2900.
    PubMedGoogle Scholar
  • 92 O’Donnell J. et al. Human umbilical vein endothelial cells differ from other endothelial cells in failing to express ABO blood group antigens. J Vasc Res 2000; 37: 540-547.
    CrossrefPubMedGoogle Scholar
  • 93 Sodetz JM. et al. Carbohydrate composition and identification of blood group A, B, and H oligosaccharide structures on human Factor VIII/von Willebrand factor. J Biol Chem 1979; 254: 10754-10760.
    PubMedGoogle Scholar
  • 94 Jenkins PV, O’Donnell JS. ABO blood group determines plasma von Willebrand factor levels: a biologic function after all?. Transfusion 2006; 46: 1836-1844.
    CrossrefPubMedGoogle Scholar
  • 95 Gill JC. et al. The effect of ABO blood group on the diagnosis of von Willebrand disease. Blood 1987; 69: 1691-1695.
    PubMedGoogle Scholar
  • 96 Bowen DJ. An influence of ABO blood group on the rate of proteolysis of von Willebrand factor by ADAMTS13. J Thromb Haemost 2003; 01: 33-40.
    CrossrefPubMedGoogle Scholar
  • 97 Federici AB. et al. Carbohydrate moiety of von Willebrand factor is not necessary for maintaining multimeric structure and ristocetin cofactor activity but protects from proteolytic degradation. J Clin Invest 1984; 74: 2049-2055.
    CrossrefPubMedGoogle Scholar
  • 98 McKinnon TA. et al. N-linked glycosylation of VWF modulates its interaction with ADAMTS13. Blood 2008; 111: 3042-3049.
    CrossrefPubMedGoogle Scholar
  • 99 Jitsuhara Y. et al. Chaperone-like functions of high-mannose type and complex-type N-glycans and their molecular basis. J Biochem 2002; 132: 803-811.
    CrossrefPubMedGoogle Scholar
  • 100 Dong JF. Cleavage of ultra-large von Willebrand factor by ADAMTS-13 under flow conditions. J Thromb Haemost 2005; 03: 1710-1716.
    CrossrefPubMedGoogle Scholar
  • 101 Mannucci PM. et al. Plasma levels of von Willebrand factor regulate ADAMTS-13, its major cleaving protease. Br J Haematol 2004; 126: 213-218.
    CrossrefPubMedGoogle Scholar
  • 102 Wagner DD. et al. Initial glycosylation and acidic pH in the Golgi apparatus are required for multimerization of von Willebrand factor. J Cell Biol 1986; 102: 1320-1324.
    CrossrefPubMedGoogle Scholar
  • 103 Marchetti G. et al. Influence of low-density lipoprotein (LDL) receptor-related protein and ABO blood group genotypes on factor XI levels. Thromb Haemost 2008; 99: 789-790.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 104 Lenting PJ. et al. The light chain of factor VIII comprises a binding site for low density lipoprotein receptor-related protein. J Biol Chem 1999; 274: 23734-23739.
    CrossrefPubMedGoogle Scholar
  • 105 Saenko EL. et al. Role of the low density lipoprotein-related protein receptor in mediation of factor VIII catabolism. J Biol Chem 1999; 274: 37685-37692.
    CrossrefPubMedGoogle Scholar
  • 106 Zhang Q. et al. Structural specializations of A2, a force-sensing domain in the ultralarge vascular protein von Willebrand factor. Proc Natl Acad Sci USA 2009; 106: 9226-9231.
    CrossrefPubMedGoogle Scholar
  • 107 Pettersen EF. et al. UCSF Chimera--a visualization system for exploratory research and analysis. J Comput Chem 2004; 25: 1605-1612.
    CrossrefPubMedGoogle Scholar
  • 108 Sharma OP. et al. Venous thromboembolism in trauma patients. Am Surg 2007; 73: 1173-1180.
    PubMedGoogle Scholar
  • 109 Shima M. et al. ABO blood group genotype and plasma von Willebrand factor in normal individuals. Vox Sang 1995; 68: 236-240.
    CrossrefPubMedGoogle Scholar
  • 110 Millar CM, Brown SA. Oligosaccharide structures of von Willebrand factor and their potential role in von Willebrand disease. Blood Rev 2006; 20: 83-92.
    CrossrefPubMedGoogle Scholar