Long Term Low Molecular Weight Heparin Anticoagulant Therapy Modulates Thrombin Generation and D-dimer in Patients with Cancer and Venous Thromboembolism

References

• Falanga A, Marchetti M, Vignoli A. Coagulation and cancer: biological and clinical aspects. J Thromb Haemost 2013;11(2):223–233.
   PubMed Web of Science ®Google Scholar
• Falanga A, Russo L. Epidemiology, risk and outcomes of venous thromboembolism in cancer. Hamostaseologie 2012;32(2):115–125.
   PubMed Web of Science ®Google Scholar
• Heit JA, Mohr DN, Silverstein MD, Petterson TM, O'Fallon WM, Melton LJ, 3rd. Predictors of recurrence after deep vein thrombosis and pulmonary embolism: a population-based cohort study. Arch Intern Med. 2000;160(6):761–768.
   PubMed Web of Science ®Google Scholar
• Falanga A, Marchetti M, Russo L. The mechanisms of cancer-associated thrombosis. Thromb Res. 2015;135(Suppl 1):S8–S11.
   PubMed Web of Science ®Google Scholar
• Prandoni P, Lensing AW, Piccioli A, Bernardi E, Simioni P, Girolami B, et al. Recurrent venous thromboembolism and bleeding complications during anticoagulant treatment in patients with cancer and venous thrombosis. Blood. 2002;100(10):3484–3488.
   PubMed Web of Science ®Google Scholar
• Lee AY, Levine MN, Baker RI, Bowden C, Kakkar AK, Prins M, et al. Low-molecular-weight heparin versus a coumarin for the prevention of recurrent venous thromboembolism in patients with cancer. N Engl J Med. 2003;349(2):146–153.
   PubMed Web of Science ®Google Scholar
• Schulman S, Zondag M, Linkins L, Pasca S, Cheung YW, de Sancho M, et al. Recurrent venous thromboembolism in anticoagulated patients with cancer: management and short-term prognosis. J Thromb Haemost. 2015;13(6):1010–1018.
   PubMed Web of Science ®Google Scholar
• Cohen AT, Katholing A, Rietbrock S, Bamber L, Martinez C. Epidemiology of first and recurrent venous thromboembolism in patients with active cancer. A population-based cohort study. Thromb Haemost. 2017;117(1):57–65.
   PubMed Web of Science ®Google Scholar
• Lee AY, Bauersachs R, Janas MS, Jarner MF, Kamphuisen PW, Meyer G, et al. CATCH: a randomised clinical trial comparing long-term tinzaparin versus warfarin for treatment of acute venous thromboembolism in cancer patients. BMC Cancer 2013;13:284.
   PubMed Web of Science ®Google Scholar
• Louzada ML, Majeed H, Wells PS. Efficacy of Low- molecular- weight- heparin versus Vitamin K antagonists for long term treatment of cancer-associated venous thromboembolism in adults: a systematic review of randomized controlled trials. Thromb Res. 2009;123(6):837–844.
   PubMed Web of Science ®Google Scholar
• Lee AY, Kamphuisen PW, Meyer G, Bauersachs R, Janas MS, Jarner MF, et al. Tinzaparin vs warfarin for treatment of acute venous thromboembolism in patients with active cancer: a randomized clinical trial. JAMA. 2015;314(7):677–686.
   PubMed Web of Science ®Google Scholar
• Kyrle PA. Predicting recurrent venous thromboembolism in cancer: is it possible? Thromb Res. 2014;133(Suppl 2):S17–S22.
   PubMed Web of Science ®Google Scholar
• Louzada ML, Majeed H, Dao V, Wells PS. Risk of recurrent venous thromboembolism according to malignancy characteristics in patients with cancer-associated thrombosis: a systematic review of observational and intervention studies. Blood Coagul Fibrinolysis. 2011;22(2):86–91.
   PubMed Web of Science ®Google Scholar
• Louzada ML, Carrier M, Lazo-Langner A, Dao V, Kovacs MJ, Ramsay TO, et al. Development of a clinical prediction rule for risk stratification of recurrent venous thromboembolism in patients with cancer-associated venous thromboembolism. Circulation 2012;126(4):448–454.
   PubMed Web of Science ®Google Scholar
• den Exter PL, Kooiman J, Huisman MV. Validation of the Ottawa prognostic score for the prediction of recurrent venous thromboembolism in patients with cancer-associated thrombosis. J Thromb Haemost. 2013;11(5):998–1000.
   PubMed Web of Science ®Google Scholar
• Trujillo-Santos J, Nieto JA, Tiberio G, Piccioli A, Di Micco P, Prandoni P, et al. Predicting recurrences or major bleeding in cancer patients with venous thromboembolism. Findings from the RIETE Registry. Thromb Haemost. 2008;100(3):435–439.
   PubMed Web of Science ®Google Scholar
• Sallah S, Husain A, Sigounas V, Wan J, Turturro F, Sigounas G, et al. Plasma coagulation markers in patients with solid tumors and venous thromboembolic disease receiving oral anticoagulation therapy. Clin Cancer Res. 2004;10(21):7238–7243.
   PubMed Web of Science ®Google Scholar
• Menapace LA, McCrae KR, Khorana AA. Predictors of recurrent venous thromboembolism and bleeding on anticoagulation. Thromb Res. 2016;140(Suppl 1):S93–S98.
   PubMed Web of Science ®Google Scholar
• Ten Cate H. Thrombin generation in clinical conditions. Thromb Res. 2012;129(3):367–370.
   PubMed Web of Science ®Google Scholar
• Marchetti M, Castoldi E, Spronk HM, van Oerle R, Balducci D, Barbui T, et al. Thrombin generation and activated protein C resistance in patients with essential thrombocythemia and polycythemia vera. Blood 2008;112(10):4061–4068.
   PubMed Web of Science ®Google Scholar
• ten Cate-Hoek AJ, Dielis AW, Spronk HM, van Oerle R, Hamulyak K, Prins MH, et al. Thrombin generation in patients after acute deep-vein thrombosis. Thromb Haemost. 2008;100(2):240–245.
   PubMed Web of Science ®Google Scholar
• Ay C, Dunkler D, Simanek R, Thaler J, Koder S, Marosi C, et al. Prediction of venous thromboembolism in patients with cancer by measuring thrombin generation: results from the Vienna Cancer and Thrombosis Study. J Clin Oncol. 2011;29(15):2099–2103.
   PubMed Web of Science ®Google Scholar
• Ay C, Vormittag R, Dunkler D, Simanek R, Chiriac AL, Drach J, et al. D-dimer and prothrombin fragment 1 + 2 predict venous thromboembolism in patients with cancer: results from the Vienna Cancer and Thrombosis Study. J Clin Oncol. 2009;27(25):4124–4129.
   PubMed Web of Science ®Google Scholar
• Cosmi B, Legnani C, Cini M, Guazzaloca G, Palareti G. The role of D-dimer and residual venous obstruction in recurrence of venous thromboembolism after anticoagulation withdrawal in cancer patients. Haematologica 2005;90(5):713–715.
   PubMed Web of Science ®Google Scholar
• Marchetti M, Tartari CJ, Russo L, Panova-Noeva M, Leuzzi A, Rambaldi A, et al. Phospholipid-dependent procoagulant activity is highly expressed by circulating microparticles in patients with essential thrombocythemia. Am J Hematol. 2014;89(1):68–73.
   PubMed Web of Science ®Google Scholar
• Duchemin J, Pan-Petesch B, Arnaud B, Blouch MT, Abgrall JF. Influence of coagulation factors and tissue factor concentration on the thrombin generation test in plasma. Thromb Haemost. 2008;99(4):767–773.
   PubMed Web of Science ®Google Scholar
• Al Dieri R, Peyvandi F, Santagostino E, Giansily M, Mannucci PM, Schved JF, et al. The thrombogram in rare inherited coagulation disorders: its relation to clinical bleeding. Thromb Haemost. 2002;88(4):576–582.
   PubMed Web of Science ®Google Scholar
• Segers O, van Oerle R, ten Cate H, Rosing J, Castoldi E. Thrombin generation as an intermediate phenotype for venous thrombosis. Thromb Haemost. 2010;103(1):114–122.
   PubMed Web of Science ®Google Scholar
• Falanga A, Tartari CJ, Marchetti M. Microparticles in tumor progression. Thromb Res. 2012;129(Suppl 1):S132–S136.
   PubMed Web of Science ®Google Scholar
• Swystun LL, Mukherjee S, Liaw PC. Breast cancer chemotherapy induces the release of cell-free DNA, a novel procoagulant stimulus. J Thromb Haemost. 2011;9(11):2313–2321.
   PubMed Web of Science ®Google Scholar
• Gould TJ, Vu TT, Swystun LL, Dwivedi DJ, Mai SH, Weitz JI, et al. Neutrophil extracellular traps promote thrombin generation through platelet-dependent and platelet-independent mechanisms. Arterioscler Thromb Vasc Biol. 2014;34(9):1977–1984.
   PubMed Web of Science ®Google Scholar
• Spronk HM, Dielis AW, Panova-Noeva M, van Oerle R, Govers-Riemslag JW, Hamulyak K, et al. Monitoring thrombin generation: is addition of corn trypsin inhibitor needed? Thromb Haemost. 2009;101(6):1156–1162.
   PubMed Web of Science ®Google Scholar
• Buyue Y, Misenheimer TM, Sheehan JP. Low molecular weight heparin inhibits plasma thrombin generation via direct targeting of factor IXa: contribution of the serpin-independent mechanism. J Thromb Haemost. 2012;10(10):2086–2098.
   PubMed Web of Science ®Google Scholar
• Hemker HC, Beguin S. Low molecular weight heparin inhibits plasma thrombin generation via direct targeting of factor IXa: a rebuttal. J Thromb Haemost. 2013;11(3):564.
   PubMed Web of Science ®Google Scholar
• Gionis MN, Ioannou CV, Katsamouris AN, Katonis P, Balalis K, Sfyridaki K, et al. The study of the thrombin generation mechanism and the effect of low molecular weight heparin as thromboprophylaxis in patients undergoing total knee and hip replacement. Thromb Res. 2013;132(6):685–691.
   PubMed Web of Science ®Google Scholar
• Gerotziafas GT, Petropoulou AD, Verdy E, Samama MM, Elalamy I. Effect of the anti-factor Xa and anti-factor IIa activities of low-molecular-weight heparins upon the phases of thrombin generation. J Thromb Haemost. 2007;5(5):955–962.
   PubMed Web of Science ®Google Scholar
• Tripodi A, Legnani C, Chantarangkul V, Cosmi B, Palareti G. Mannucci PM. High thrombin generation measured in the presence of thrombomodulin is associated with an increased risk of recurrent venous thromboembolism. J Thromb Haemost. 2008;6(8):1327–1333.
   PubMed Web of Science ®Google Scholar
• Hron G, Kollars M, Binder BR, Eichinger S, Kyrle PA. Identification of patients at low risk for recurrent venous thromboembolism by measuring thrombin generation. JAMA. 2006;296(4):397–402.
   PubMed Web of Science ®Google Scholar
• Blackwell K, Haroon Z, Broadwater G, Berry D, Harris L, Iglehart JD, et al. Plasma D-dimer levels in operable breast cancer patients correlate with clinical stage and axillary lymph node status. J Clin Oncol. 2000;18(3):600–608.
   PubMed Web of Science ®Google Scholar
• Kasthuri RS, Taubman MB, Mackman N. Role of tissue factor in cancer. J Clin Oncol. 2009;27(29):4834–4838.
   PubMed Web of Science ®Google Scholar
• Antoniou D, Pavlakou G, Stathopoulos GP, Karydis I, Chondrou E, Papageorgiou C, et al. Predictive value of D-dimer plasma levels in response and progressive disease in patients with lung cancer. Lung Cancer. 2006;53(2):205–210.
   PubMed Web of Science ®Google Scholar
• Dirix LY, Salgado R, Weytjens R, Colpaert C, Benoy I, Huget P, et al. Plasma fibrin D-dimer levels correlate with tumour volume, progression rate and survival in patients with metastatic breast cancer. Br J Cancer. 2002;86(3):389–395.
   PubMed Web of Science ®Google Scholar
• Ma X, Li Y, Zhang J, Huang J, Liu L. Prognostic role of D-dimer in patients with lung cancer: a meta-analysis. Tumour Biol. 2014;35(3):2103–2109.
   PubMed Web of Science ®Google Scholar
• Ay C, Dunkler D, Pirker R, Thaler J, Quehenberger P, Wagner O, et al. High D-dimer levels are associated with poor prognosis in cancer patients. Haematologica 2012;97(8):1158–1164.
   PubMed Web of Science ®Google Scholar
• Stender MT, Larsen AC, Sall M, Thorlacius-Ussing O. D-Dimer predicts prognosis and non-resectability in patients with pancreatic cancer: a prospective cohort study. Blood Coagul Fibrinolysis. 2016;27(5):597– 601.
   PubMed Web of Science ®Google Scholar
• Nakamura K, Nakayama K, Ishikawa M, Katagiri H, Minamoto T, Ishibashi T, et al. High Pre-treatment plasma D-dimer level as a potential prognostic biomarker for cervical carcinoma. Anticancer Res. 2016;36(6):2933– 2938.
   PubMed Web of Science ®Google Scholar