Genetic risk factors for venous thromboembolism

References

• Heit JA. Epidemiology of venous thromboembolism. Nat Rev Cardiol. 2015;12:464–474.
   PubMed Web of Science ®Google Scholar
• Donadini MP, Ageno W. Unusual site thrombosis. Semin Hematol. 2011;48:264–270.
   PubMed Web of Science ®Google Scholar
• Hansson PO, Welin L, Tibblin G, et al. Deep vein thrombosis and pulmonary embolism in the general population. ‘The study of men born in 1913ʹ. Arch Int Med. 1997;157:1665–1670.
   PubMed Web of Science ®Google Scholar
• Bell EJ, Lutsey PL, Basu S, et al. Lifetime risk of venous thromboembolism in two cohort studies. Am J Med. 2016;129:339.e19-26.
   Web of Science ®Google Scholar
• Goldhaber SZ. Venous thromboembolism: epidemiology and magnitude of the problem. Best Pract Res Clin Haematol. 2012;25:235–242.
   PubMed Web of Science ®Google Scholar
• Rosendaal FR. Venous thrombosis: a multicausal disease. Lancet. 1999;353:1167–1173.
   PubMed Web of Science ®Google Scholar
• White RH. The epidemiology of venous thromboembolism. Circulation. 2003;107:I4–8.
   PubMed Web of Science ®Google Scholar
• Ribeiro DD, Lijfering WM, Barreto SM, et al. Epidemiology of recurrent venous thrombosis. Braz J Med Biol Res. 2012;45:1–7.
   PubMed Web of Science ®Google Scholar
• Heit JA, Phelps MA, Ward SA, et al. Familial segregation of venous thromboembolism. J Thromb Haemost. 2004;2:731–736.
   PubMed Web of Science ®Google Scholar
• Tosetto A, Castaman G, Cappellari A, et al. The VITA project: heritability of resistance to activated protein C. Vincenza thrombophilia and arteriosclerosis. Thromb Haemost. 2000;84:811–814.
   PubMed Web of Science ®Google Scholar
• Zöller B, Ohlsson H, Sundquist J, et al. A sibling based design to quantify genetic and shared environmental effects of venous thromboembolism in Sweden. Thromb Res. 2017;149:82–87.
   PubMed Web of Science ®Google Scholar
• Larsen TB, Sørensen HT, Skytthe A, et al. Major genetic susceptibility for venous thromboembolism in men: a study of Danish twins. Epidemiology. 2003;14:328–332.
   PubMed Web of Science ®Google Scholar
• Zöller B, Li X, Ohlsson H, et al. Family history of venous thromboembolism as a risk factor and genetic research tool. Thromb Haemost. 2015;114:890–900.
   PubMed Web of Science ®Google Scholar
• Dahlbäck B, Carlsson M, Svensson PJ. Familial thrombophilia due to a previously unrecognized mechanism characterized by poor anticoagulant response to activated protein C: prediction of a cofactor to activated protein C. Proc Natl Acad Sci U S A. 1993;90:1004–1008.
   PubMed Web of Science ®Google Scholar
• Svensson PJ, Dahlbäck B. Resistance to activated protein C as a basis for venous thrombosis. N Engl J Med. 1994;330:517–522.
   PubMed Web of Science ®Google Scholar
• Bertina RM, Koeleman BP, Koster T, et al. Mutation in blood coagulation factor V associated with resistance to activated protein C. Nature. 1994;369:64–67.
   PubMed Web of Science ®Google Scholar
• Zöller B, Dahlbäck B. Linkage between inherited resistance to activated protein C and factor V gene mutation in venous thrombosis. Lancet. 1994;343:1536–1538.
   PubMed Web of Science ®Google Scholar
• Voorberg J, Roelse J, Koopman R, et al. Association of idiopathic venous thromboembolism with single point-mutation at Arg506 of factor V. Lancet. 1994;343:1535–1536.
   PubMed Web of Science ®Google Scholar
• Greengard JS, Sun X, Xu X, et al. Activated protein C resistance caused by Arg506Gln mutation in factor Va. Lancet. 1994;343:1361–1362.
   PubMed Web of Science ®Google Scholar
• Poort SR, Rosendaal FR, Reitsma PH, et al. A common genetic variation in the 3ʹ-untranslated region of the prothrombin gene is associated with elevated plasma prothrombin levels and an increase in venous thrombosis. Blood. 1996;88:3698–3703.
   PubMed Web of Science ®Google Scholar
• Zöller B, Li X, Ohlsson H, et al. Epidemiology of familial aggregation of venous thromboembolism. Semin Thromb Hemost. 2016;42:821–832.
   PubMed Web of Science ®Google Scholar
• Martinelli I, Bucciarelli P, Mannucci PM. Thrombotic risk factors: basic pathophysiology. Crit Care Med. 2010;38:S3–9.
   PubMed Web of Science ®Google Scholar
• Mannucci PM, Franchini M. Classic thrombophilic gene variants. Thromb Haemost. 2015;114:885–889.
   PubMed Web of Science ®Google Scholar
• Rosendaal FR, Reitsma PH. Genetics of venous thrombosis. J Thromb Haemost. 2009;7(Suppl 1):301–304.
   PubMedGoogle Scholar
• Zöller B, García de Frutos P, Hillarp A, et al. Thrombophilia as a multigenic disease. Haematologica. 1999;84:59–70.
   PubMed Web of Science ®Google Scholar
• Heijboer H, Brandjes DPM, Büller HR, et al. Deficiencies of coagulation‐inhibiting and fibrinolytic proteins in outpatients with deep‐vein thrombosis. N Engl J Med. 1990;323:1512–1516.
   PubMed Web of Science ®Google Scholar
• Koster T, Rosendaal FR, Briët E, et al. Protein C deficiency in a controlled series of unselected outpatients: an infrequent but clear risk factor for venous thrombosis (Leiden Thrombophilia Study). Blood. 1995;85:2756–2761.
   PubMed Web of Science ®Google Scholar
• Segers K, Dahlbäck B, Nicolaes GA. Coagulation factor V and thrombophilia: background and mechanisms. Thromb Haemost. 2007;98:530–542.
   PubMed Web of Science ®Google Scholar
• Cai H, Hua B, Fan L, et al. A novel mutation (g2172–>c) in the factor V gene in a Chinese family with hereditary activated protein C resistance. Thromb Res. 2010;125:545–548.
   PubMed Web of Science ®Google Scholar
• Nogami K, Shinozawa K, Ogiwara K, et al. Novel FV mutation (W1920R, FVNara) associated with serious deep vein thrombosis and more potent APC resistance relative to FVLeiden. Blood. 2014;123:2420–2428.
   PubMed Web of Science ®Google Scholar
• Guzmán N, Larama G, Ávila A, et al. Three novel variants in the coagulation factor V gene associated with deep venous thrombosis in Chilean patients with Amerindian ethnic background. Clin Chim Acta. 2015;444:24–28.
   PubMed Web of Science ®Google Scholar
• Pezeshkpoor B, Castoldi E, Mahler A, et al. Identification and functional characterization of a novel F5 mutation (Ala512Val, FVBonn) associated with activated protein C resistance. Thromb Haemost. 2016;14:1353–1363.
   Web of Science ®Google Scholar
• Miyawaki Y, Suzuki A, Fujita J, et al. Thrombosis from a prothrombin mutation conveying antithrombin resistance. N Engl J Med. 2012;366:2390–2396.
   PubMed Web of Science ®Google Scholar
• Djordjevic V, Kovac M, Miljic P, et al. A novel prothrombin mutation in two families with prominent thrombophilia–the first cases of antithrombin resistance in a Caucasian population. J Thromb Haemost. 2013;11:1936–1939.
   PubMed Web of Science ®Google Scholar
• Sivasundar S, Oommen AT, Prakash O, et al. Molecular defect of ‘Prothrombin Amrita’: substitution of arginine by glutamine (Arg553 to Gln) near the Na(+) binding loop of prothrombin. Blood Cells Mol Dis. 2013;50:182–183.
   PubMed Web of Science ®Google Scholar
• Bulato C, Radu CM, Campello E, et al. New prothrombin mutation (Arg596Trp, Prothrombin Padua 2) associated with venous thromboembolism. Arterioscler Thromb Vasc Biol. 2016;36:1022–1029.
   PubMed Web of Science ®Google Scholar
• Simioni P, Tormene D, Tognin G, et al. X-linked thrombophilia with a mutant factor IX (factor IX Padua). N Engl J Med. 2009;361:1671–1675.
   PubMed Web of Science ®Google Scholar
• Tam V, Patel N, Turcotte M, et al. Benefits and limitations of genome-wide association studies. Nat Rev Genet. 2019;20:467–484.
   PubMed Web of Science ®Google Scholar
• Trégouët DA, Heath S, Saut N, et al. Common susceptibility alleles are unlikely to contribute as strongly as the FV and ABO loci to VTE risk: results from a GWAS approach. Blood. 2009;113:5298–5303.
   PubMed Web of Science ®Google Scholar
• Buil A, Trégouët DA, Souto JC, et al. C4BPB/C4BPA is a new susceptibility locus for venous thrombosis with unknown protein S‐independent mechanism: results from genome‐wide association and gene expression analyses followed by case‐control studies. Blood. 2010;115:4644–4650.
   PubMed Web of Science ®Google Scholar
• Heit JA, Armasu SM, McCauley BM, et al. Identification of unique venous thromboembolism‐susceptibility variants in African‐Americans. Thromb Haemost. 2017;117:758–768.
   PubMed Web of Science ®Google Scholar
• Trégouët DA, Morange PE. What is currently known about the genetics of venous thromboembolism at the dawn of next generation sequencing technologies. Br J Haematol. 2018;180:335–345.
   PubMed Web of Science ®Google Scholar
• Lindström S, Wang L, Smith EN, et al. Genomic and transcriptomic association studies identify 16 novel susceptibility loci for venous thromboembolism. Blood. 2019;134:1645–1657.
   PubMed Web of Science ®Google Scholar
• Klarin D, Busenkell E, Judy R, et al. Genome-wide association analysis of venous thromboembolism identifies new risk loci and genetic overlap with arterial vascular disease. Nat Genet. 2019;51:1574–1579.
   PubMed Web of Science ®Google Scholar
• Bryk AH, Wiśniewski JR. Quantitative analysis of human red blood cell proteome. J Proteome Res. 2017;16:2752–2761.
   PubMedGoogle Scholar
• Westman JS, Stenfelt L, Vidovic K, et al. Allele-selective RUNX1 binding regulates P1 blood group status by transcriptional control of A4GALT. Blood. 2018;131:1611–1616.
   PubMed Web of Science ®Google Scholar
• Yasukochi Y, Sakuma J, Takeuchi I, et al. Identification of nine novel loci related to hematological traits in a Japanese population. Physiol Genomics. 2018;50:758–769.
   PubMed Web of Science ®Google Scholar
• Comertpay B, Gov E. Identification of key biomolecules in rheumatoid arthritis through the reconstruction of comprehensive disease-specific biological networks. Autoimmunity. 2020;53:156–166.
   PubMed Web of Science ®Google Scholar
• Wang C, Li YY, Li X, et al. Serum complement C4b, fibronectin, and prolidase are associated with the pathological changes of pulmonary tuberculosis. BMC Infect Dis. 2014;14:52.
   PubMed Web of Science ®Google Scholar
• Klarin D, Lynch J, Aragam K, et al. Genome-wide association study of peripheral artery disease in the million veteran program. Nat Med. 2019;25:1274–1279.
   PubMed Web of Science ®Google Scholar
• Connolly SJ, Eikelboom JW, Bosch J, et al. Rivaroxaban with or without aspirin in patients with stable coronary artery disease: an international, randomised, double-blind, placebo-controlled trial. Lancet. 2018;391:205–218.
   PubMed Web of Science ®Google Scholar
• Bonaca MP, Bauersachs RM, Anand SS, et al. Rivaroxaban in peripheral artery disease after revascularization. N Engl J Med. 2020 Mar 28 Epub ahead of print. DOI:10.1056/NEJMoa2000052.
   PubMed Web of Science ®Google Scholar
• Wainberg M, Sinnott-Armstrong N, Mancuso N, et al. Opportunities and challenges for transcriptome-wide association studies. Nat Genet. 2019;51:592–599.
   PubMed Web of Science ®Google Scholar
• Cunha ML, Meijers JC, Middeldorp S. Introduction to the analysis of next generation sequencing data and its application to venous thromboembolism. Thromb Haemost. 2015;114:920–932.
   PubMed Web of Science ®Google Scholar
• Lotta LA, Wang M, Yu J, et al. Identification of genetic risk variants for deep vein thrombosis by multiplexed next-generation sequencing of 186 hemostatic/pro-inflammatory genes. BMC Med Genomics. 2012;5:7.
   PubMed Web of Science ®Google Scholar
• Lotta LA, Tuana G, Yu J, et al. Next-generation sequencing study finds an excess of rare, coding single-nucleotide variants of ADAMTS13 in patients with deep vein thrombosis. J Thromb Haemost. 2013;11:1228–1239.
   PubMed Web of Science ®Google Scholar
• Pagliari MT, Lotta LA, de Haan HG, et al. Next-generation sequencing and in vitro expression study of ADAMTS13 single nucleotidevariants in deep vein thrombosis. PLoS One. 2016;11:e0165665.
   PubMedGoogle Scholar
• Rühle F, Witten A, Barysenka A, et al. Rare genetic variants in SMAP1, B3GAT2, and RIMS1 contribute to pediatric venous thromboembolism. Blood. 2017;129:783–790.
   PubMed Web of Science ®Google Scholar
• de Haan HG, van Hylckama Vlieg A, Lotta LA, et al. Targeted sequencing to identify novel genetic risk factors for deep vein thrombosis: a study of 734 genes. J Thromb Haemost. 2018;16:2432–2441.
   PubMed Web of Science ®Google Scholar
• Manderstedt E, Lind-Halldén C, Svensson P, et al. Next-generation sequencing of 17 genes associated with venous thromboembolism reveals a deficit of non-synonymous variants in procoagulant genes. Thromb Haemost. 2019;119:1441–1450.
   PubMed Web of Science ®Google Scholar
• Cunha MLR, Meijers JCM, Rosendaal FR, et al. Whole exome sequencing in thrombophilic pedigrees to identify genetic risk factors for venous thromboembolism. PLoS One. 2017;12:e0187699.
   PubMed Web of Science ®Google Scholar
• Halvorsen M, Lin Y, Sampson BA, et al. Whole exome sequencing reveals severe thrombophilia in acute unprovoked idiopathic fatal pulmonary embolism. EBioMedicine. 2017;17:95–100.
   PubMed Web of Science ®Google Scholar
• Lee EJ, Dykas DJ, Leavitt AD, et al. Whole-exome sequencing in evaluation of patients with venous thromboembolism. Blood Adv. 2017;1:1224–1237.
   PubMed Web of Science ®Google Scholar
• Lindström S, Brody JA, Turman C, et al. A large-scale exome array analysis of venous thromboembolism. Genet Epidemiol. 2019;43:449–457.
   PubMed Web of Science ®Google Scholar
• Kunz G, Ohlin AK, Adami A, et al. Naturally occurring mutations in the thrombomodulin gene leading to impaired expression and function. Blood. 2002;99:3646–3653.
   PubMed Web of Science ®Google Scholar
• Dennis J, Johnson CY, Adediran AS, et al. The endothelial protein C receptor (PROCR) Ser219Gly variant and risk of common thrombotic disorders: a HuGE review and meta-analysis of evidence from observational studies. Blood. 2012;119:2392–2400.
   PubMed Web of Science ®Google Scholar
• Diaz JA, Saha P, Cooley B, et al. Choosing a mouse model of venous thrombosis. Arterioscler Thromb Vasc Biol. 2019;39:311–318.
   PubMed Web of Science ®Google Scholar
• Cleuren AC, van Vlijmen BJ, Reitsma PH. Transgenic mouse models of venous thrombosis: fulfilling the expectations? Semin Thromb Hemost. 2007;33:610–616.
   PubMed Web of Science ®Google Scholar
• Cui J, Eitzman DT, Westrick RJ, et al. Spontaneous thrombosis in mice carrying the factor V Leiden mutation. Blood. 2000;96:4222–4226.
   PubMed Web of Science ®Google Scholar
• Paciullo F, Momi S, Gresele P. PCSK9 in haemostasis and thrombosis: possible pleiotropic effects of PCSK9 inhibitors in cardiovascular prevention. Thromb Haemost. 2019;119:359–367.
   PubMed Web of Science ®Google Scholar
• Law LA, Graham DK, Di Paola J, et al. GAS6/TAM pathway signaling hemostasis and thrombosis. Front Med (Lausanne). 2018;5:137.
   PubMed Web of Science ®Google Scholar
• Erickson LA, Fici GJ, Lund JE, et al. Development of venous occlusions in mice transgenic for the plasminogen activator inhibitor-1 gene. Nature. 1990;346:74–76.
   PubMed Web of Science ®Google Scholar
• Dahlbäck B, Villoutreix BO. Regulation of blood coagulation by the protein C anticoagulant pathway: novel insights into structure-function relationships and molecular recognition. Arterioscler Thromb Vasc Biol. 2005;25:1311–1320.
   PubMed Web of Science ®Google Scholar
• Zöller B. Genetics of venous thromboembolism revised. Blood. 2019;134:1568–1570.
   PubMed Web of Science ®Google Scholar
• Franz M, Rodriguez H, Lopes C, et al. GeneMANIA update 2018. Nucleic Acids Res. 2018;46:W60–4.
   PubMed Web of Science ®Google Scholar
• Konstantinides SV, Meyer G, Becattini C, et al. 2019 ESC guidelines for the diagnosis and management of acute pulmonary embolism developed in collaboration with the European Respiratory Society (ERS). Eur Heart J. 2020;41:543–603.
   PubMed Web of Science ®Google Scholar
• Kakkos SK, Kirkilesis GI, Tsolakis IA. Editor’s Choice - efficacy and safety of the new oral anticoagulants dabigatran, rivaroxaban, apixaban, and edoxaban in the treatment and secondary prevention of venous thromboembolism: a systematic review and meta-analysis of phase III trials. Eur J Vasc Endovasc Surg. 2014;48:565–575.
   PubMed Web of Science ®Google Scholar
• Agnelli G, Buller HR, Cohen A, et al. Apixaban for extended treatment of venous thromboembolism. N Engl J Med. 2013;368:699–708.
   PubMed Web of Science ®Google Scholar
• Campello E, Spiezia L, Simioni P. Diagnosis and management of factor V Leiden. Expert Rev Hematol. 2016;9:1139–1149.
   PubMed Web of Science ®Google Scholar
• Campello E, Spiezia L, Adamo A, et al. Thrombophilia, risk factors and prevention. Expert Rev Hematol. 2019;12:147–158.
   PubMed Web of Science ®Google Scholar
• Vernon E, Hiedemann B, Bowie BH. Economic evaluations of thrombophilia screening prior to prescribing combined oral contraceptives: a systematic and critical review. Appl Health Econ Health Policy. 2017;15:583–595.
   PubMed Web of Science ®Google Scholar
• Centers for Disease Control and Prevention (CDC). U.S. selected practice recommendations for contraceptive use, 2016. MMWR Recomm Rep Morb Mortal Wkly Rep. 2016;65(4):1–66.
   PubMed Web of Science ®Google Scholar
• World Health Organization. Medical eligibility criteria for contraceptive use. 5th Geneva: WHO. 2015. [cited 2020 Jul 20]. Available from: http://apps.who.int/iris/bitstream/10665/181468/1/9789241549158_eng.pdf?ua=1
   Google Scholar
• Wu O, Robertson L, Twaddle S, et al. Screening for thrombophilia in high-risk situations: a meta analysis and cost-effectiveness analysis. Br J Haematol. 2005;131:80–90.
   PubMed Web of Science ®Google Scholar
• Grody WW, Griffin JH, Taylor AK, et al. American College of Medical Genetics consensus statement on factor V Leiden mutation testing. Genet Med. 2001;3:139–148.
   PubMedGoogle Scholar
• Centers for Disease Control. US medical eligibility criteria (US MEC) for contraceptive use, 2016. [cited 2020 Jul 20] Available from:https://www.cdc.gov/reproductivehealth/contraception/mmwr/mec/summary.html
   Google Scholar
• van Vlijmen EF, Wiewel-Verschueren S, Monster TB, et al. Combined oral contraceptives, thrombophilia and the risk of venous thromboembolism: a systematic review and meta-analysis. J Thromb Haemost. 2016;14:1393–1403.
   PubMed Web of Science ®Google Scholar
• Gersh KC, Nagaswami C, Weisel JW. Fibrin network structure and clot mechanical properties are altered by incorporation of erythrocytes. Thromb Haemost. 2009;102:1169–1175.
   PubMed Web of Science ®Google Scholar
• Zöller B, Melander O, Svensson P, et al. Red cell distribution width and risk for venous thromboembolism: a population-based cohort study. Thromb Res. 2014;133:334–339.
   PubMed Web of Science ®Google Scholar
• Zöller B, Li X, Sundquist J, et al. Autoimmune diseases and venous thromboembolism: a review of the literature. Am J Cardiovasc Dis. 2012;2:171–183.
   PubMedGoogle Scholar
• Lindblad B, Svensson PJ, Dahlbäck B. Arterial and venous thromboembolism with fatal outcome and resistance to activated protein C. Lancet. 1994;343:917.
   PubMed Web of Science ®Google Scholar
• Holm J, Zöller B, Svensson PJ, et al. Myocardial infarction associated with homozygous resistance to activated protein C. Lancet. 1994;344:952–953.
   PubMed Web of Science ®Google Scholar
• Zöller B, Svensson PJ, He X, et al. Identification of the same factor V gene mutation in 47 out of 50 thrombosis-prone families with inherited resistance to activated protein C. J Clin Invest. 1994;94:2521–2524.
   PubMed Web of Science ®Google Scholar
• Zöller B, Berntsdotter A, García de Frutos P, et al. Resistance to activated protein C as an additional genetic risk factor in hereditary deficiency of protein S. Blood. 1995;85:3518–3523.
   PubMed Web of Science ®Google Scholar