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REVIEW

Thrombotic Pathogenesis and Laboratory Diagnosis in Cancer Patients, An Update

ORCID Icon &
Pages 259-272 | Received 10 Aug 2022, Accepted 04 Jan 2023, Published online: 22 Jan 2023

References

  • Khorana AA, Mackman N, Falanga A, et al. Cancer-associated venous thromboembolism. Nat Rev Dis Primers. 2022;8(1):1–18. doi:10.1038/s41572-022-00336-y
  • Nasser NJ, Fox J, Agbarya A. Potential mechanisms of cancer-related hypercoagulability. Cancers. 2020;12(3):566. doi:10.3390/cancers12030566
  • Stark K, Schubert I, Joshi U, et al. Distinct pathogenesis of pancreatic cancer microvesicle–associated venous thrombosis identifies new antithrombotic targets in vivo. Arterioscler Thromb Vasc Biol. 2018;38:772–786. doi:10.1161/ATVBAHA.117.310262
  • Falanga A, Russo L, Milesi V, Vignoli A. Mechanisms and risk factors of thrombosis in cancer. Crit Rev Oncol Hematol. 2017;118:79–83. doi:10.1016/j.critrevonc.2017.08.003
  • Levi M. Cancer-related coagulopathies. Thromb Res. 2014;133:S70–S75. doi:10.1016/S0049-3848(14)50012-6
  • Eichinger S. Cancer associated thrombosis: risk factors. Thromb Res. 2016;140:S12–S17. doi:10.1016/S0049-3848(16)30092-5
  • Sheth RA, Niekamp A, Quencer KB, et al. Thrombosis in cancer patients: etiology, incidence, and management. Cardiovasc Diagn Ther. 2017;7(3):S178–S185. doi:10.21037/cdt.2017.11.02
  • Streiff MB, Holmstrom B, Angelini D, et al. Cancer-associated venous thromboembolic disease, version 2.2021, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw. 2021;19(10):1181–1201. doi:10.6004/jnccn.2021.0047
  • Wells P, Anderson D. The diagnosis and treatment of venous thromboembolism. Hematology Am Soc Hematol Educ Program. 2013;2013:457–463. doi:10.1182/asheducation-2013.1.457
  • Mulder FI, Horváth-Puhó E, van Es N, et al. Venous thromboembolism in cancer patients: a population-based cohort study. Blood. 2021;137(14):1959–1969. doi:10.1182/blood.2020007338
  • Hayashida K, Kawabata Y, Saito K, et al. Prevalence and risk factors of preoperative venous thromboembolism in patients with malignant musculoskeletal tumors: an analysis based on D-dimer screening and imaging. Thromb J. 2022;20(1):22. doi:10.1186/s12959-022-00382-2
  • Mandoj C, Tomao L, Conti L. Coagulation in brain tumors: biological basis and clinical implications. Front Neurol. 2019;10:181. doi:10.3389/fneur.2019.00181
  • Falanga A, Marchetti M, Russo L. The mechanisms of cancer-associated thrombosis. Thromb Res. 2015;135(1):S8–S11. doi:10.1016/S0049-3848(15)50432-5
  • Abdol Razak NB, Jones G, Bhandari M, Berndt MC, Metharom P. Cancer-associated thrombosis: an overview of mechanisms, risk factors, and treatment. Cancers. 2018;10(10):380. doi:10.3390/cancers10100380
  • Sun HJ, Wu ZY, Nie XW, Bian JS. Role of endothelial dysfunction in cardiovascular diseases: the link between inflammation and hydrogen sulfide. Front Pharmacol. 2020;10:1568. doi:10.3389/fphar.2019.01568
  • Fuentes HE, Tafur AJ, Caprini JA. Cancer-associated thrombosis. Dis Mon. 2016;62(5):121–158. doi:10.1016/j.disamonth.2016.03.003
  • Connolly GC, Francis CW. Cancer-associated thrombosis. Hematology Am Soc Hematol Educ Program. 2013;2013:684–691. doi:10.1182/asheducation-2013.1.684
  • Navi BB, Reiner AS, Kamel H, et al. Risk of arterial thromboembolism in patients with cancer. J Am Coll Cardiol. 2017;70(8):926–938. doi:10.1016/j.jacc.2017.06.047
  • Luo X, Lv Y, Bai X, et al. Plaque erosion: a distinctive pathological mechanism of acute coronary syndrome. Front Cardiovasc Med. 2021;8:711453. doi:10.3389/fcvm.2021.711453
  • Tuzovic M, Herrmann J, Iliescu C, Marmagkiolis K, Ziaeian B, Yang EH. Arterial thrombosis in patients with cancer. Curr Treat Options Cardiovasc Med. 2018;20(5):40. doi:10.1007/s11936-018-0635-x
  • Levi M. Management of cancer-associated disseminated intravascular coagulation. Thromb Res. 2016;140(1):S66–70. doi:10.1016/S0049-3848(16)30101-3
  • Wada H, Matsumoto T, Suzuki K, et al. Differences and similarities between disseminated intravascular coagulation and thrombotic microangiopathy. Thromb J. 2018;16:14. doi:10.1186/s12959-018-0168-2
  • Thachil J, Falanga A, Levi M, Liebman H, Di Nisio M. Scientific and standardization committee of the international society on thrombosis and hemostasis. Management of cancer-associated disseminated intravascular coagulation: guidance from the SSC of the ISTH. J Thromb Haemost. 2015;13(4):671–675. doi:10.1111/jth.12838
  • Dirweesh A, Siddiqui W, Khan M, Iyer P, Seelagy M. Adenocarcinoma of the lung presenting as thrombotic thrombocytopenic purpura. Respir Med Case Rep. 2017;21:82–83. doi:10.1016/j.rmcr.2017.04.004
  • Zheng XL. ADAMTS13 and von Willebrand factor in thrombotic thrombocytopenic purpura. Annu Rev Med. 2015;66:211–225. doi:10.1146/annurev-med-061813-013241
  • Nolasco L, Nolasco J, Feng S, Afshar-Kharghan V, Moake J. Human complement factor H is a reductase for large soluble von Willebrand factor multimers--brief report. Arterioscler Thromb Vasc Biol. 2013;33(11):2524–2528. doi:10.1161/ATVBAHA.113.302280
  • Piazza G. Venous thromboembolism and cancer. Circulation. 2013;128:2614–2618. doi:10.1161/CIRCULATIONAHA.113.002702
  • Hisada Y, Mackman N. Cancer cell-derived tissue factor-positive extracellular vesicles: biomarkers of thrombosis and survival. Curr Opin Hematol. 2019;26(5):349–356. doi:10.1097/MOH.0000000000000521
  • Gardiner C, Harrison P, Belting M, et al. Extracellular vesicles, tissue factor, cancer and thrombosis - discussion themes of the ISEV 2014 Educational Day. J Extracell Vesicles. 2015;4:26901. doi:10.3402/jev.v4.26901
  • Geddings JE, Mackman N. Tumor-derived tissue factor–positive microparticles and venous thrombosis in cancer patients. Blood. 2013;122:1873–1880. doi:10.1182/blood-2013-04-460139
  • Shindo K, Aishima S, Ohuchida K, et al. Podoplanin expression in cancer-associated fibroblasts enhances tumor progression of invasive ductal carcinoma of the pancreas. Mol Cancer. 2013;12(1):168. doi:10.1186/1476-4598-12-168
  • Gagliano N, Celesti G, Tacchini L, et al. Epithelial-to-mesenchymal transition in pancreatic ductal adenocarcinoma: characterization in a 3D-cell culture model. World J Gastroenterol. 2016;22(18):4466–4483. doi:10.3748/wjg.v22.i18.4466
  • Payne H, Ponomaryov T, Watson SP, Brill A. Mice with a deficiency in CLEC-2 are protected against deep vein thrombosis. Blood. 2017;129(14):2013–2020. doi:10.1182/blood-2016-09-742999
  • Riedl J, Preusser M, Nazari PM, et al. Podoplanin expression in primary brain tumors induces platelet aggregation and increases risk of venous thromboembolism. Blood. 2017;129(13):1831–1839. doi:10.1182/blood-2016-06-720714
  • Mege D, Panicot-Dubois L, Ouaissi M, et al. The origin and concentration of circulating microparticles differ according to cancer type and evolution: a prospective single-center study. Int J Cancer. 2016;138(4):939–948. doi:10.1002/ijc.29837
  • Zwicker JI. Risking thromboembolism: podoplanin and glioma. Blood. 2017;129(13):1742–1743. doi:10.1182/blood-2017-02-763524
  • Urano T, Suzuki Y, Iwaki T, Sano H, Honkura N, Castellino FJ. Recognition of Plasminogen Activator Inhibitor Type 1 as the Primary Regulator of Fibrinolysis. Curr Drug Targets. 2019;20(16):1695–1701. doi:10.2174/1389450120666190715102510
  • Tipoe TL, Wu WKK, Chung L, et al. Plasminogen activator inhibitor 1 for predicting sepsis severity and mortality outcomes: a systematic review and meta-analysis. Front Immunol. 2018;9:1218. doi:10.3389/fimmu.2018.01218
  • Chen N, Ren M, Li R, et al. Bevacizumab promotes venous thromboembolism through the induction of PAI-1 in a mouse xenograft model of human lung carcinoma. Mol Cancer. 2015;14:140. doi:10.1186/s12943-015-0418-x
  • Lal I, Dittus K, Holmes CE. Platelets, coagulation and fibrinolysis in breast cancer progression. Breast Cancer Res. 2013;15(4):207. doi:10.1186/bcr3425
  • Woei-A-Jin FJ, Tesselaar ME, Garcia Rodriguez P, Romijn FP, Bertina RM, Osanto S. Tissue factor-bearing microparticles and CA19.9: two players in pancreatic cancer-associated thrombosis? Br J Cancer. 2016;115(3):332–338. doi:10.1038/bjc.2016.170
  • Wojtukiewicz MZ, Sierko E, Hempel D, Tucker SC, Honn KV. Platelets and cancer angiogenesis nexus. Cancer Metastasis Rev. 2017;36(2):249–262. doi:10.1007/s10555-017-9673-1
  • Leal AC, Mizurini DM, Gomes T, et al. Tumor-derived exosomes induce the formation of neutrophil extracellular traps: implications for the establishment of cancer-associated thrombosis. Sci Rep. 2017;7(1):6438. doi:10.1038/s41598-017-06893-7
  • McDonald B, Davis RP, Kim SJ, et al. Platelets and neutrophil extracellular traps collaborate to promote intravascular coagulation during sepsis in mice. Blood. 2017;129(10):1357–1367. doi:10.1182/blood-2016-09-741298
  • Martinod K, Wagner DD. Thrombosis: tangled up in NETs. Blood. 2014;123(18):2768–2776. doi:10.1182/blood-2013-10-463646
  • Lam FW, Cruz MA, Parikh K, Rumbaut RE. Histones stimulate von Willebrand factor release in vitro and in vivo. Haematologica. 2016;101(7):e277–279. doi:10.3324/haematol.2015.140632
  • Mauracher LM, Posch F, Martinod K, et al. Citrullinated histone H3, a biomarker of neutrophil extracellular trap formation, predicts the risk of venous thromboembolism in cancer patients. J Thromb Haemost. 2018;16(3):508–518. doi:10.1111/jth.13951
  • Kaur S, Kumar S, Momi N, Sasson AR, Batra SK. Mucins in pancreatic cancer and its microenvironment. Nat Rev Gastroenterol Hepatol. 2013;10(10):607–620. doi:10.1038/nrgastro.2013.120
  • Galgano L, Guidetti GF, Torti M, Canobbio I. The controversial role of LPS in platelet activation in vitro. Int J Mol Sci. 2022;23(18):10900. doi:10.3390/ijms231810900
  • Muz B, de la Puente P, Azab F, Azab AK. The role of hypoxia in cancer progression, angiogenesis, metastasis, and resistance to therapy. Hypoxia. 2015;3:83–92. doi:10.2147/HP.S93413
  • Di Virgilio F, Adinolfi E. Extracellular purines, purinergic receptors and tumor growth. Oncogene. 2017;36(3):293–303. doi:10.1038/onc.2016.206
  • Rojas A, Delgado-López F, Perez-Castro R, et al. HMGB1 enhances the protumoral activities of M2 macrophages by a RAGE-dependent mechanism. Tumour Biol. 2016;37(3):3321–3329. doi:10.1007/s13277-015-3940-y
  • Tadie JM, Bae HB, Jiang S, et al. HMGB1 promotes neutrophil extracellular trap formation through interactions with Toll-like receptor 4. Am J Physiol Lung Cell Mol Physiol. 2013;304(5):L342–L349. doi:10.1152/ajplung.00151.2012
  • Abdel-Razeq H, Mansour A, Abdulelah H, et al. Thromboembolic events in cancer patients on active treatment with cisplatin-based chemotherapy: another look! Thromb J. 2018;16:2. doi:10.1186/s12959-018-0161-9
  • Rangaswamy C, Mailer RK, Englert H, Konrath S, Renné T. The contact system in liver injury. Semin Immunopathol. 2021;43(4):507–517. doi:10.1007/s00281-021-00876-7
  • Tawil N, Bassawon R, Rak J. Oncogenes and clotting factors: the emerging role of tumor cell genome and epigenome in cancer-associated thrombosis. Semin Thromb Hemost. 2019;45(4):373–384. doi:10.1055/s-0039-1687891
  • Rak J. Cancer genes and blood clots. Blood. 2021;137(15):1996–1997. doi:10.1182/blood.2020009967
  • Heraudeau A, Delluc A, Le Henaff M, et al. Risk of venous thromboembolism in association with factor V Leiden in cancer patients - The EDITH case-control study. PLoS One. 2018;13(5):e0194973. doi:10.1371/journal.pone.0194973
  • Tinholt M, Viken MK, Dahm AE, et al. Increased coagulation activity and genetic polymorphisms in the F5, F10 and EPCR genes are associated with breast cancer: a case-control study. BMC Cancer. 2014;14:845. doi:10.1186/1471-2407-14-845
  • Paulsen B, Skille H, Smith EN, et al. Fibrinogen gamma gene rs2066865 and risk of cancer-related venous thromboembolism. Haematologica. 2020;105(7):1963–1968. doi:10.3324/haematol.2019.224279
  • Ekim M, Ekim H, Yılmaz YK. The prevalence of Factor V Leiden, prothrombin G20210A, MTHFR C677T and MTHFR A1298C mutations in healthy Turkish population. Hippokratia. 2015;19(4):309–313.
  • Ünlü B, Versteeg HH. Cancer-associated thrombosis: the search for the holy grail continues. Res Pract Thromb Haemost. 2018;2(4):622–629. doi:10.1002/rth2.12143
  • Grover SP, Tissue Factor: MN. An essential mediator of hemostasis and trigger of thrombosis. Arterioscler Thromb Vasc Biol. 2018;38(4):709–725. doi:10.1161/ATVBAHA.117.309846
  • Patel H, Sun H, Hussain AN, Vakde T. Advances in the diagnosis of venous thromboembolism: a literature review. Diagnostics. 2020;10(6):365. doi:10.3390/diagnostics10060365
  • Jenne CN, Urrutia R, Kubes P. Platelets: bridging hemostasis, inflammation, and immunity. Int J Lab Hematol. 2013;35(3):254–261. doi:10.1111/ijlh.12084
  • Hisada Y, Mackman N. Cancer-associated pathways and biomarkers of venous thrombosis. Blood. 2017;130(13):1499–1506. doi:10.1182/blood-2017-03-743211
  • Riondino S, Ferroni P, Zanzotto FM, Roselli M, Guadagni F. Predicting VTE in cancer patients: candidate biomarkers and risk assessment models. Cancers. 2019;11(1):95. doi:10.3390/cancers11010095
  • Borgen PO, Reikeras O. Prothrombin fragment F1+2 in plasma and urine during total Hip arthroplasty. J Orthop. 2017;14(4):475–479. doi:10.1016/j.jor.2017.08.001
  • Duarte RCF, Ferreira CN, Rios DRA, Reis HJD, Carvalho MDG. Thrombin generation assays for global evaluation of the hemostatic system: perspectives and limitations. Rev Bras Hematol Hemoter. 2017;39(3):259–265. doi:10.1016/j.bjhh.2017.03.009
  • Rimpo K, Tanaka A, Ukai M, Ishikawa Y, Hirabayashi M, Shoyama T. Thrombin-antithrombin complex measurement using a point-of-care testing device for diagnosis of disseminated intravascular coagulation in dogs. PLoS One. 2018;13(10):e0205511. doi:10.1371/journal.pone.0205511
  • Chung HW, Lim JB. Clinical significance of elevated serum soluble CD40 ligand levels as a diagnostic and prognostic tumor marker for pancreatic ductal adenocarcinoma. J Transl Med. 2014;12:102. doi:10.1186/1479-5876-12-102
  • Lord MS, Cheng B, Farrugia BL, McCarthy S, Whitelock JM. Platelet factor 4 binds to vascular proteoglycans and controls both growth factor activities and platelet activation. J Biol Chem. 2017;292(10):4054–4063. doi:10.1074/jbc.M116.760660
  • Gutierrez LS, Gutierrez J. Thrombospondin 1 in metabolic diseases. Front Endocrinol. 2021;12:638536. doi:10.3389/fendo.2021.638536
  • Castaman G, Linari S. Diagnosis and treatment of von Willebrand disease and rare bleeding disorders. J Clin Med. 2017;6(4):45. doi:10.3390/jcm6040045
  • Mussbacher M, Salzmann M, Brostjan C, et al. Cell type-specific roles of NF-κB linking inflammation and thrombosis. Front Immunol. 2019;10:85. doi:10.3389/fimmu.2019.00085