Semin Thromb Hemost 2024; 50(03): 360-383
DOI: 10.1055/s-0043-1764381
Review Article

Platelet Parameters as Biomarkers for Thrombosis Risk in Cancer: A Systematic Review and Meta-analysis

Anne Lind Malte
1   Thrombosis and Haemostasis Research Unit, Department of Clinical Biochemistry, Aarhus University Hospital, Aarhus, Denmark
,
Johanne Andersen Højbjerg
1   Thrombosis and Haemostasis Research Unit, Department of Clinical Biochemistry, Aarhus University Hospital, Aarhus, Denmark
2   Department of Clinical Medicine, Aarhus University, Aarhus, Denmark
,
Julie Brogaard Larsen
1   Thrombosis and Haemostasis Research Unit, Department of Clinical Biochemistry, Aarhus University Hospital, Aarhus, Denmark
2   Department of Clinical Medicine, Aarhus University, Aarhus, Denmark
› Author Affiliations
Funding This study was supported by Department of Clinical Biochemistry, Aarhus University Hospital, Aarhus, Denmark.

Abstract

Cancer-associated thrombosis (CAT) is a major cause of both morbidity and mortality in cancer patients. Platelet count has been investigated as a predictor of CAT in various settings while knowledge on platelet activation parameters is sparse. This report provides a systematic review and meta-analysis on available literature on associations between platelet count and/or function and arterial and venous thrombosis in adult cancer patients. The review was performed according to the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) statement. PubMed and Embase were searched up to March 2022. The National Heart, Lung, and Blood Institute's tools were used for quality assessment. In total, 100 studies were included which investigated the association between CAT and platelet count (n = 90), platelet indices (n = 19), and platelet function/activation markers (n = 13) in patients with solid cancers (n = 61), hematological cancers (n = 17), or mixed cancer types (n = 22). Eighty-one studies had venous thrombosis as their outcome measure, while 4 had arterial thrombosis and 15 studies had both. We found significantly elevated odds ratio of 1.50 (95% confidence interval: 1.19–1.88) for thrombosis with higher platelet counts. We saw a tendency toward an association between markers of platelet activation in forms of mean platelet volume and soluble P selectin and both arterial and venous thrombosis. Only one study investigated dynamic platelet function using flow cytometry. In conclusion, platelet count is associated with CAT across different cancer types and settings. Platelet function or activation marker analysis may be valuable in assisting thrombosis risk assessment in cancer patients but is sparsely investigated so far.

Supplementary Material



Publication History

Article published online:
15 March 2023

© 2023. Thieme. All rights reserved.

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  • References

  • 1 Connolly GC, Francis CW. Cancer-Associated Thrombosis. American Society of Hematology Education Program; 2013: 684-691
  • 2 Kim AS, Khorana AA, McCrae KR. Mechanisms and biomarkers of cancer-associated thrombosis. Transl Res 2020; 225: 33-53
  • 3 Navi BB, Reiner AS, Kamel H. et al. Risk of arterial thromboembolism in patients with cancer. J Am Coll Cardiol 2017; 70 (08) 926-938
  • 4 Riedl J, Pabinger I, Ay C. Platelets in cancer and thrombosis. Hamostaseologie 2014; 34 (01) 54-62
  • 5 Khorana AA, Cohen AT, Carrier M. et al. Prevention of venous thromboembolism in ambulatory patients with cancer. ESMO Open 2020; 5 (06) e000948
  • 6 Prandoni P, Lensing AW, Piccioli A. et al. Recurrent venous thromboembolism and bleeding complications during anticoagulant treatment in patients with cancer and venous thrombosis. Blood 2002; 100 (10) 3484-3488
  • 7 Khorana AA, Kuderer NM, Culakova E, Lyman GH, Francis CW. Development and validation of a predictive model for chemotherapy-associated thrombosis. Blood 2008; 111 (10) 4902-4907
  • 8 Ay C, Dunkler D, Marosi C. et al. Prediction of venous thromboembolism in cancer patients. Blood 2010; 116 (24) 5377-5382
  • 9 Verso M, Agnelli G, Barni S, Gasparini G, LaBianca R. A modified Khorana risk assessment score for venous thromboembolism in cancer patients receiving chemotherapy: the PROTECHT score. Intern Emerg Med 2012; 7 (03) 291-292
  • 10 Louzada ML, Carrier M, Lazo-Langner A. 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 (04) 448-454
  • 11 van Es N, Di Nisio M, Cesarman G. et al. Comparison of risk prediction scores for venous thromboembolism in cancer patients: a prospective cohort study. Haematologica 2017; 102 (09) 1494-1501
  • 12 Mansfield AS, Tafur AJ, Wang CE, Kourelis TV, Wysokinska EM, Yang P. Predictors of active cancer thromboembolic outcomes: validation of the Khorana score among patients with lung cancer. J Thromb Haemost 2016; 14 (09) 1773-1778
  • 13 Muñoz Martín AJ, García Alfonso P, Rupérez Blanco AB, Pérez Ramírez S, Blanco Codesido M, Martín Jiménez M. Incidence of venous thromboembolism (VTE) in ambulatory pancreatic cancer patients receiving chemotherapy and analysis of Khorana's predictive model. Clin Transl Oncol 2014; 16 (10) 927-930
  • 14 Simanek R, Vormittag R, Ay C. et al. High platelet count associated with venous thromboembolism in cancer patients: results from the Vienna Cancer and Thrombosis Study (CATS). J Thromb Haemost 2010; 8 (01) 114-120
  • 15 Khorana AA, Mackman N, Falanga A. et al. Cancer-associated venous thromboembolism. Nat Rev Dis Primers 2022; 8 (01) 11
  • 16 Grover SP, Hisada YM, Kasthuri RS, Reeves BN, Mackman N. Cancer Therapy-Associated Thrombosis. Arterioscler Thromb Vasc Biol 2021; 41 (04) 1291-1305
  • 17 Connolly GC, Phipps RP, Francis CW. Platelets and cancer-associated thrombosis. Semin Oncol 2014; 41 (03) 302-310
  • 18 Falanga A, Marchetti M, Russo L. The mechanisms of cancer-associated thrombosis. Thromb Res 2015; 135 (Suppl 1): S8-S11
  • 19 Cooke NM, Egan K, McFadden S. et al. Increased platelet reactivity in patients with late-stage metastatic cancer. Cancer Med 2013; 2 (04) 564-570
  • 20 Caine GJ, Lip GY, Stonelake PS, Ryan P, Blann AD. Platelet activation, coagulation and angiogenesis in breast and prostate carcinoma. Thromb Haemost 2004; 92 (01) 185-190
  • 21 Cella G, Marchetti M, Vianello F. et al. Nitric oxide derivatives and soluble plasma selectins in patients with myeloproliferative neoplasms. Thromb Haemost 2010; 104 (01) 151-156
  • 22 Peterson JE, Zurakowski D, Italiano Jr JE. et al. VEGF, PF4 and PDGF are elevated in platelets of colorectal cancer patients. Angiogenesis 2012; 15 (02) 265-273
  • 23 Panella TJ, Peters W, White JG, Hannun YA, Greenberg CS. Platelets acquire a secretion defect after high-dose chemotherapy. Cancer 1990; 65 (08) 1711-1716
  • 24 The National Heart, Lung, and Blood Institute (NHLBI). Study Quality Assessment Tools. 2013. Accessed February 20, 2023 at: https://www.nhlbi.nih.gov/health-topics/study-quality-assessment-tools
  • 25 Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003; 327 (7414): 557-560
  • 26 Afsar CU, Gunaldi M, Kum P. et al. Pancreatic carcinoma, thrombosis and mean platelet volume: single center experience from the southeast region of Turkey. Asian Pac J Cancer Prev 2014; 15 (21) 9143-9146
  • 27 Akkiz H, Carr BI, Yalçın K K. et al. Characteristics of hepatocellular carcinoma aggressiveness factors in Turkish patients. Oncology 2018; 94 (02) 116-124
  • 28 Al-Asadi O, Almusarhed M, Eldeeb H. Predictive risk factors of venous thromboembolism (VTE) associated with peripherally inserted central catheters (PICC) in ambulant solid cancer patients: retrospective single Centre cohort study. Thromb J 2019; 17 (01) 2
  • 29 Albertin CL, Uppal S, Al-Niaimi AN, Seo S, Hinshaw JL, Hartenbach EM. Thrombocytosis is predictive of postoperative pulmonary embolism in patients with gynecologic cancer. Int J Gynecol Cancer 2015; 25 (06) 1096-1101
  • 30 Boone BA, Zenati MS, Rieser C. et al. Risk of venous thromboembolism for patients with pancreatic ductal adenocarcinoma undergoing preoperative chemotherapy followed by surgical resection. Ann Surg Oncol 2019; 26 (05) 1503-1511
  • 31 Carr BI, Guerra V. HCC and its microenvironment. Hepatogastroenterology 2013; 60 (126) 1433-1437
  • 32 Carr BI, Guerra V. Thrombocytosis and hepatocellular carcinoma. Dig Dis Sci 2013; 58 (06) 1790-1796
  • 33 Chen L, Feng Q, Wang W, Liu L. Incidence and related factors for low-extremity deep vein thrombosis in breast cancer patients who underwent surgical resection: what do we know and what should we care. Front Surg 2022; 9: 755671
  • 34 Chen Y, Qin QX, Qin C. et al. Specific biomarkers of prostate cancer-associated ischemic stroke: a case-control study. Med Sci Monit 2019; 25: 5536-5542
  • 35 Chen Y, Wang Y, Xie S. et al. A risk of venous thromboembolism algorithm as a predictor of venous thromboembolism in patients with colorectal cancer. Clin Appl Thromb Hemost 2021; 27: 107 60296211064900
  • 36 Cui LN, Li N, Fu S, Zhang X, Wang X, Wang RT. Combination of preoperative D-dimer and mean platelet volume predicts postoperative deep venous thrombosis in breast cancer patients. Cancer Biomark 2018; 21 (04) 909-913
  • 37 Epstein AS, Soff GA, Capanu M. et al. Analysis of incidence and clinical outcomes in patients with thromboembolic events and invasive exocrine pancreatic cancer. Cancer 2012; 118 (12) 3053-3061
  • 38 Falvella FS, Cremolini C, Miceli R. et al. Variant alleles in factor V, prothrombin, plasminogen activator inhibitor-1, methylenetetrahydrofolate reductase and risk of thromboembolism in metastatic colorectal cancer patients treated with first-line chemotherapy plus bevacizumab. Pharmacogenomics J 2017; 17 (04) 331-336
  • 39 Ferroni P, Guadagni F, Riondino S. et al. Evaluation of mean platelet volume as a predictive marker for cancer-associated venous thromboembolism during chemotherapy. Haematologica 2014; 99 (10) 1638-1644
  • 40 Ferroni P, Riondino S, Formica V. et al. Venous thromboembolism risk prediction in ambulatory cancer patients: clinical significance of neutrophil/lymphocyte ratio and platelet/lymphocyte ratio. Int J Cancer 2015; 136 (05) 1234-1240
  • 41 Filippova OT, Kim SW, Cowan RA. et al. Hematologic changes after splenectomy for ovarian cancer debulking surgery, and association with infection and venous thromboembolism. Int J Gynecol Cancer 2020; 30 (08) 1183-1188
  • 42 Fu X, Lu P, Ye G. et al. Analysis of the risk factors of peripherally inserted central catheter-associated venous thrombosis after chemotherapy in patients with lung cancer. Int J Clin Exp Med 2019; 12 (05) 5852-5859
  • 43 Gerotziafas GT, Taher A, Abdel-Razeq H. et al; COMPASS–CAT Working Group. A predictive score for thrombosis associated with breast, colorectal, lung, or ovarian cancer: the prospective COMPASS-Cancer-Associated Thrombosis Study. Oncologist 2017; 22 (10) 1222-1231
  • 44 Grilz E, Posch F, Königsbrügge O. et al. Association of platelet-to-lymphocyte ratio and neutrophil-to-lymphocyte ratio with the risk of thromboembolism and mortality in patients with cancer. Thromb Haemost 2018; 118 (11) 1875-1884
  • 45 Guven DC, Aksun MS, Sahin TK. et al. Poorer baseline performance status is associated with increased thromboembolism risk in metastatic cancer patients treated with immunotherapy. Support Care Cancer 2021; 29 (09) 5417-5423
  • 46 Iwata S, Kawai A, Ueda T, Ishii T. Japanese Musculoskeletal Oncology Group (JMOG). Symptomatic venous thromboembolism in patients with malignant bone and soft tissue tumors: a prospective multicenter cohort study. Ann Surg Oncol 2021; 28 (07) 3919-3927
  • 47 Kenmotsu H, Notsu A, Mori K. et al. Cumulative incidence of venous thromboembolism in patients with advanced cancer in prospective observational study. Cancer Med 2021; 10 (03) 895-904
  • 48 Kim SY, Burns ZT, Henry DH. The assessment of thrombotic risk using a predictive model in metastatic cancer patients undergoing first-line therapy. Thromb Res 2012; 130 (06) 967-970
  • 49 Koksal D, Safak O, Ozcan A, Agackiran Y, Erturk H, Findik G. Thromboembolic events in malignant pleural mesothelioma. Clin Appl Thromb Hemost 2016; 22 (04) 390-394
  • 50 Kuk A, Magnowska M, Suchy W. et al. Retrospective evaluation of thromboembolism risk in ovarian cancer patients treated with bevacizumab. Target Oncol 2017; 12 (04) 495-503
  • 51 Lin BX, Xu CS. Risk factors of PICC-related venous thrombosis in breast cancer patients undergoing chemotherapy. Int J Gen Med 2021; 14: 1337-1341
  • 52 Li N, Zhang FB, Li BJ, Wang RT. Combination of preoperative D-dimer and platelet distribution width predicts postoperative deep venous thrombosis in patients with cervical carcinoma. Asian Pac J Cancer Prev 2019; 20 (04) 1025-1029
  • 53 Li Z, Zhang G, Zhang M, Mei J, Weng H, Peng Z. Development and validation of a risk score for prediction of venous thromboembolism in patients with lung cancer. Clin Appl Thromb Hemost 2020; 26: 107 6029620910793
  • 54 López-Salazar J, Ramírez-Tirado LA, Gómez-Contreras N. et al. Cancer-associated prothrombotic pathways: leucocytosis, but not thrombocytosis, correlates with venous thromboembolism in women with ovarian cancer. Intern Med J 2020; 50 (03) 366-370
  • 55 Ma SG, Hu J, Huang Y. The risk factors for perioperative venous thromboembolism in patients with gynecological malignancies: a meta-analysis. Thromb Res 2020; 196: 325-334
  • 56 Man YN, Wang YN, Hao J. et al. Pretreatment plasma D-dimer, fibrinogen, and platelet levels significantly impact prognosis in patients with epithelial ovarian cancer independently of venous thromboembolism. Int J Gynecol Cancer 2015; 25 (01) 24-32
  • 57 Mandalà M, Barni S, Prins M. et al. Acquired and inherited risk factors for developing venous thromboembolism in cancer patients receiving adjuvant chemotherapy: a prospective trial. Ann Oncol 2010; 21 (04) 871-876
  • 58 Matsuo K, Hasegawa K, Yoshino K. et al. Venous thromboembolism, interleukin-6 and survival outcomes in patients with advanced ovarian clear cell carcinoma. Eur J Cancer 2015; 51 (14) 1978-1988
  • 59 Matsuo K, Yessaian AA, Lin YG. et al. Predictive model of venous thromboembolism in endometrial cancer. Gynecol Oncol 2013; 128 (03) 544-551
  • 60 Merkow RP, Bilimoria KY, McCarter MD. et al. Post-discharge venous thromboembolism after cancer surgery: extending the case for extended prophylaxis. Ann Surg 2011; 254 (01) 131-137
  • 61 Monreal M, Alastrue A, Rull M. et al. Upper extremity deep venous thrombosis in cancer patients with venous access devices – prophylaxis with a low molecular weight heparin (Fragmin). Thromb Haemost 1996; 75 (02) 251-253
  • 62 Navi BB, Sherman CP, Genova R. et al. Mechanisms of ischemic stroke in patients with cancer: a prospective study. Ann Neurol 2021; 90 (01) 159-169
  • 63 Nie D, Yang E, Li Z. Pretreatment thrombocytosis predict poor prognosis in patients with endometrial carcinoma: a systematic review and meta-analysis. BMC Cancer 2019; 19 (01) 73
  • 64 Park H, Jeong CW, Yuk H. et al. Influence of tumor thrombus on occurrence of distant venous thromboembolism and survival in patients with renal cell carcinoma after surgery. Clin Appl Thromb Hemost 2019; 25: 107 6029618823288
  • 65 Pedersen LM, Milman N. Prognostic significance of thrombocytosis in patients with primary lung cancer. Eur Respir J 1996; 9 (09) 1826-1830
  • 66 Peng SY, Wei T, Li XY, Yuan Z, Lin Q. A model to assess the risk of peripherally inserted central venous catheter-related thrombosis in patients with breast cancer: a retrospective cohort study. Support Care Cancer 2022; 30 (02) 1127-1137
  • 67 Pin S, Mateshaytis J, Ghosh S, Batuyong E, Easaw JC. Risk factors for venous thromboembolism in endometrial cancer. Curr Oncol 2020; 27 (04) 198-203
  • 68 Poruk KE, Firpo MA, Huerter LM. et al. Serum platelet factor 4 is an independent predictor of survival and venous thromboembolism in patients with pancreatic adenocarcinoma. Cancer Epidemiol Biomarkers Prev 2010; 19 (10) 2605-2610
  • 69 Quan X, Qin Q, Chen Y. et al. Independent risk factors and the potential predictors of bladder cancer-related ischemic stroke. J Int Med Res 2020; 48 (04) 30 0060520919227
  • 70 Riedl J, Kaider A, Marosi C. et al. Decreased platelet reactivity in patients with cancer is associated with high risk of venous thromboembolism and poor prognosis. Thromb Haemost 2017; 117 (01) 90-98
  • 71 Rink M, Riethdorf S, Yu H. et al. The impact of circulating tumor cells on venous thromboembolism and cardiovascular events in bladder cancer patients treated with radical cystectomy. J Clin Med 2020; 9 (11) 3478
  • 72 Schlick CJR, Liu JY, Yang AD, Bentrem DJ, Bilimoria KY, Merkow RP. Pre-operative, intra-operative, and post-operative factors associated with post-discharge venous thromboembolism following colorectal cancer resection. J Gastrointest Surg 2020; 24 (01) 144-154
  • 73 Schorling RM, Pfrepper C, Golombek T. et al. Evaluation of biomarkers for the prediction of venous thromboembolism in ambulatory cancer patients. Oncol Res Treat 2020; 43 (09) 414-427
  • 74 Shah MA, Capanu M, Soff G, Asmis T, Kelsen DP. Risk factors for developing a new venous thromboembolism in ambulatory patients with non-hematologic malignancies and impact on survival for gastroesophageal malignancies. J Thromb Haemost 2010; 8 (08) 1702-1709
  • 75 Shi S, Cheng J, Zhao Y, Chen W. Incidence, and preoperative and intraoperative prognostic factors of deep venous thrombosis in patients with glioma following craniotomy. Clin Neurol Neurosurg 2021; 210: 106998
  • 76 Suzuki T, Fujino S, Inaba S. et al. Venous thromboembolism in patents with lung cancer. Clin Appl Thromb Hemost 2020; 26: 107 6029620977910
  • 77 Thaler J, Ay C, Kaider A. et al. Biomarkers predictive of venous thromboembolism in patients with newly diagnosed high-grade gliomas. Neuro-oncol 2014; 16 (12) 1645-1651
  • 78 Tsoukalas N, Papakotoulas P, Christopoulou A. et al. Real-world data on thromboprophylaxis in active cancer patients: Where are we? Are we getting there?. Cancers (Basel) 2020; 12 (07) 1907
  • 79 Uhrig M, Simons D, Schlemmer HP. Incidental pulmonary emboli in stage IV melanoma patients: prevalence in CAT staging examinations and improved detection with vessel reconstructions based on dual energy CAT. PLoS One 2018; 13 (07) e0199458
  • 80 von Tempelhoff GF, Niemann F, Schneider DM, Kirkpatrick CJ, Hommel G, Heilmann L. Blood rheology during chemotherapy in patients with ovarian cancer. Thromb Res 1998; 90 (02) 73-82
  • 81 Wu X, Xue X, Tang J. et al. Evaluation of risk factors for venous thromboembolism in Chinese women with epithelial ovarian cancer. Int J Gynecol Cancer 2013; 23 (01) 65-72
  • 82 Xian Z, Chen Y, Chen L. et al. A clinical research on the potential pathogenesis of somatic cancer related cerebral venous sinus thrombosis. Medicine (Baltimore) 2019; 98 (19) e15134
  • 83 Yamagata K, Fukuzawa S, Uchida F, Ishibashi-Kanno N, Yanagawa T, Bukawa H. Is preoperative plate-lymphocyte ratio a predictor of deep vein thrombosis in patients with oral cancer during surgery?. J Oral Maxillofac Surg 2021; 79 (04) 914-924
  • 84 Yu I, Chen L, Ruan JY, Chang JT, Cheung WY. Risk and management of venous thromboembolisms in bevacizumab-treated metastatic colorectal cancer patients. Support Care Cancer 2016; 24 (03) 1199-1208
  • 85 Zhang W, Liu X, Cheng H, Yang Z, Zhang G. Risk factors and treatment of venous thromboembolism in perioperative patients with ovarian cancer in China. Medicine (Baltimore) 2018; 97 (31) e11754
  • 86 Al-Ani F, Wang YP, Lazo-Langner A. Development of a clinical prediction rule for venous thromboembolism in patients with acute leukemia. Thromb Haemost 2020; 120 (02) 322-328
  • 87 Bagratuni T, Kastritis E, Politou M. et al. Clinical and genetic factors associated with venous thromboembolism in myeloma patients treated with lenalidomide-based regimens. Am J Hematol 2013; 88 (09) 765-770
  • 88 Boersma RS, Hamulyak K, van Oerle R, Tuinenburg A, Ten Cate-Hoek AJ, Schouten HC. Biomarkers for prediction of central venous catheter related-thrombosis in patients with hematological malignancies. Clin Appl Thromb Hemost 2016; 22 (08) 779-784
  • 89 Chang H, Kuo MC, Shih LY. et al. Acute promyelocytic leukemia-associated thrombosis. Acta Haematol 2013; 130 (01) 1-6
  • 90 Del Principe MI, Buccisano F, Maurillo L. et al. Infections increase the risk of central venous catheter-related thrombosis in adult acute myeloid leukemia. Thromb Res 2013; 132 (05) 511-514
  • 91 Kato A, Takano H, Ichikawa A. et al. A retrospective cohort study of venous thromboembolism(VTE) in 1035 Japanese myeloma patients treated with thalidomide; lower incidence without statistically significant association between specific risk factors and development of VTE and effects of thromboprophylaxis with aspirin and warfarin. Thromb Res 2013; 131 (02) 140-144
  • 92 Kirkizlar O, Alp Kirkizlar T, Umit EG. et al. The incidence of venous thromboembolism and impact on survival in Hodgkin lymphoma. Clin Lymphoma Myeloma Leuk 2020; 20 (08) 542-547
  • 93 Libourel EJ, Klerk CPW, van Norden Y. et al. Disseminated intravascular coagulation at diagnosis is a strong predictor for thrombosis in acute myeloid leukemia. Blood 2016; 128 (14) 1854-1861
  • 94 Li X, Hou SL, Li X. et al. Risk factors of thromboembolism in lymphoma patients undergoing chemotherapy and its clinical significance. Clin Appl Thromb Hemost 2021; 27: 107 60296211037923
  • 95 Martella F, Cerrano M, Di Cuonzo D. et al. Frequency and risk factors for thrombosis in acute myeloid leukemia and high-risk myelodysplastic syndromes treated with intensive chemotherapy: a two centers observational study. Ann Hematol 2022; 101 (04) 855-867
  • 96 Qian H, Liu J, Xu C, Zhu W, Chen L. Predisposing factors and effect of bundle nursing in PICC-related upper extremity deep venous thrombosis in patients with non-Hodgkin's lymphoma undergoing chemotherapy. Am J Transl Res 2021; 13 (08) 9679-9686
  • 97 Rupa-Matysek J, Gil L, Barańska M, Dytfeld D, Komarnicki M. Mean platelet volume as a predictive marker for venous thromboembolism in patients treated for Hodgkin lymphoma. Oncotarget 2018; 9 (30) 21190-21200
  • 98 Rupa-Matysek J, Gil L, Kroll-Balcerzak R, Barańska M, Komarnicki M. Mean platelet volume as a predictive marker for venous thromboembolism and mortality in patients treated for diffuse large B-cell lymphoma. Hematol Oncol 2017; 35 (04) 456-464
  • 99 Sanfilippo KM, Carson KR, Wang TF. et al. Evaluation of the Khorana score for prediction of venous thromboembolism in patients with multiple myeloma. Res Pract Thromb Haemost 2022; 6 (01) e12634
  • 100 Vu K, Luong NV, Hubbard J. et al. A retrospective study of venous thromboembolism in acute leukemia patients treated at the University of Texas MD Anderson Cancer Center. Cancer Med 2015; 4 (01) 27-35
  • 101 Yuen HLA, Slocombe A, Heron V. et al. Venous thromboembolism in primary central nervous system lymphoma during frontline chemoimmunotherapy. Res Pract Thromb Haemost 2020; 4 (06) 997-1003
  • 102 Zhang X, Guo X. Risk factors of thrombosis in Chinese subjects with acute promyelocytic leukemia. Thromb J 2021; 19 (01) 42
  • 103 Ahmed S, Shahid RK, Bhatt H, Lee-Ying R, Lim J. Chemotherapy-related thrombocytosis: does it increase the risk of thromboembolism?. Oncology 2012; 82 (06) 327-332
  • 104 Ashrani AA, Gullerud RE, Petterson TM, Marks RS, Bailey KR, Heit JA. Risk factors for incident venous thromboembolism in active cancer patients: a population based case-control study. Thromb Res 2016; 139: 29-37
  • 105 Ay C, Simanek R, Vormittag R. et al. High plasma levels of soluble P-selectin are predictive of venous thromboembolism in cancer patients: results from the Vienna Cancer and Thrombosis Study (CATS). Blood 2008; 112 (07) 2703-2708
  • 106 Babilonia KM, Golightly LK, Gutman JA. et al. Antithrombotic therapy in patients with thrombocytopenic cancer: outcomes associated with reduced-dose, low-molecular-weight heparin during hospitalization. Clin Appl Thromb Hemost 2014; 20 (08) 799-806
  • 107 Dickmann B, Ahlbrecht J, Ay C. et al. Regional lymph node metastases are a strong risk factor for venous thromboembolism: results from the Vienna Cancer and Thrombosis Study. Haematologica 2013; 98 (08) 1309-1314
  • 108 Gong J, Drobni ZD, Alvi RM. et al. Immune checkpoint inhibitors for cancer and venous thromboembolic events. Eur J Cancer 2021; 158: 99-110
  • 109 Grilz E, Marosi C, Königsbrügge O. et al. Association of complete blood count parameters, D-dimer, and soluble P-selectin with risk of arterial thromboembolism in patients with cancer. J Thromb Haemost 2019; 17 (08) 1335-1344
  • 110 Haire WD, Lieberman RP, Edney J. et al. Hickman catheter-induced thoracic vein thrombosis. Frequency and long-term sequelae in patients receiving high-dose chemotherapy and marrow transplantation. Cancer 1990; 66 (05) 900-908
  • 111 Kewan T, Ko T, Flores M, Sallam Y, Haddad A, Daw H. Prognostic impact and risk factors of cancer-associated thrombosis events in stage-IV cancer patients treated with immune checkpoint inhibitors. Eur J Haematol 2021; 106 (05) 682-688
  • 112 Khorana AA, Francis CW, Culakova E, Lyman GH. Risk factors for chemotherapy-associated venous thromboembolism in a prospective observational study. Cancer 2005; 104 (12) 2822-2829
  • 113 Khorana AA, Kamphuisen PW, Meyer G. et al. Tissue factor as a predictor of recurrent venous thromboembolism in malignancy: biomarker analyses of the CATCH Trial. J Clin Oncol 2017; 35 (10) 1078-1085
  • 114 Kitayama H, Kondo T, Sugiyama J. et al. Venous thromboembolism in hospitalized patients receiving chemotherapy for malignancies at Japanese community hospital: prospective observational study. BMC Cancer 2017; 17 (01) 351
  • 115 Moore RA, Adel N, Riedel E. et al. High incidence of thromboembolic events in patients treated with cisplatin-based chemotherapy: a large retrospective analysis. J Clin Oncol 2011; 29 (25) 3466-3473
  • 116 Peippo MH, Kurki S, Lassila R, Carpén OM. Real-world features associated with cancer-related venous thromboembolic events. ESMO Open 2018; 3 (05) e000363
  • 117 Riedl J, Hell L, Kaider A. et al. Association of platelet activation markers with cancer-associated venous thromboembolism. Platelets 2016; 27 (01) 80-85
  • 118 Riedl J, Kaider A, Reitter EM. et al. Association of mean platelet volume with risk of venous thromboembolism and mortality in patients with cancer. Results from the Vienna Cancer and Thrombosis Study (CATS). Thromb Haemost 2014; 111 (04) 670-678
  • 119 Sinnamon AJ, Tong JKC, Bailey EA. et al. Prospective implementation of a standardized screening protocol for deep venous thrombosis in abdominal surgical oncology patients. J Surg Oncol 2018; 118 (03) 568-573
  • 120 Sutandyo N, Tobing DL. Kardinah. Risk factors of deep vein thrombosis in cancer patients. Iran J Blood Cancer 2018; 10 (04) 117-123
  • 121 van Es N, Louzada M, Carrier M. et al. Predicting the risk of recurrent venous thromboembolism in patients with cancer: a prospective cohort study. Thromb Res 2018; 163: 41-46
  • 122 Vemulapalli S, Chintala L, Tsimberidou AM. et al. Clinical outcomes and factors predicting development of venous thromboembolic complications in patients with advanced refractory cancer in a Phase I Clinic: the M. D. Anderson Cancer Center experience. Am J Hematol 2009; 84 (07) 408-413
  • 123 Zhang X, Huang JJ, Xia Y. et al. High risk of deep vein thrombosis associated with peripherally inserted central catheters in lymphoma. Oncotarget 2016; 7 (23) 35404-35411
  • 124 Agnelli G, Bolis G, Capussotti L. et al. A clinical outcome-based prospective study on venous thromboembolism after cancer surgery: the @RISTOS project. Ann Surg 2006; 243 (01) 89-95
  • 125 Adelborg K, Veres K, Horváth-Puhó E. et al. Thrombocytopenia among patients with hematologic malignancies and solid tumors: risk and prognosis. Blood 2021; 138 (Suppl 1): 3156-3156
  • 126 Skipper MT, Rubak P, Stentoft J, Hvas AM, Larsen OH. Evaluation of platelet function in thrombocytopenia. Platelets 2018; 29 (03) 270-276
  • 127 Buss DH, Stuart JJ, Lipscomb GE. The incidence of thrombotic and hemorrhagic disorders in association with extreme thrombocytosis: an analysis of 129 cases. Am J Hematol 1985; 20 (04) 365-372
  • 128 Montoro-García S, Schindewolf M, Stanford S, Larsen OH, Thiele T. The role of platelets in venous thromboembolism. Semin Thromb Hemost 2016; 42 (03) 242-251
  • 129 Abdol Razak NB, Jones G, Bhandari M, Berndt MC, Metharom P. Cancer-Associated thrombosis: an overview of mechanisms, risk factors, and treatment. Cancers (Basel) 2018; 10 (10) 380
  • 130 Bath P, Algert C, Chapman N, Neal B. PROGRESS Collaborative Group. Association of mean platelet volume with risk of stroke among 3134 individuals with history of cerebrovascular disease. Stroke 2004; 35 (03) 622-626
  • 131 Braekkan SK, Mathiesen EB, Njølstad I, Wilsgaard T, Størmer J, Hansen JB. Mean platelet volume is a risk factor for venous thromboembolism: the Tromsø Study, Tromsø, Norway. J Thromb Haemost 2010; 8 (01) 157-162
  • 132 Chu SG, Becker RC, Berger PB. et al. Mean platelet volume as a predictor of cardiovascular risk: a systematic review and meta-analysis. J Thromb Haemost 2010; 8 (01) 148-156
  • 133 Cil H, Yavuz C, Islamoglu Y. et al. Platelet count and mean platelet volume in patients with in-hospital deep venous thrombosis. Clin Appl Thromb Hemost 2012; 18 (06) 650-653
  • 134 Slavka G, Perkmann T, Haslacher H. et al. Mean platelet volume may represent a predictive parameter for overall vascular mortality and ischemic heart disease. Arterioscler Thromb Vasc Biol 2011; 31 (05) 1215-1218
  • 135 Mutlu H, Artis TA, Erden A, Akca Z. Alteration in mean platelet volume and platicrit values in patients with cancer that developed thrombosis. Clin Appl Thromb Hemost 2013; 19 (03) 331-333
  • 136 Ridker PM, Buring JE, Rifai N. Soluble P-selectin and the risk of future cardiovascular events. Circulation 2001; 103 (04) 491-495
  • 137 Tscharre M, Vogel B, Tentzeris I. et al. Prognostic impact of soluble P-selectin on long-term adverse cardiovascular outcomes in patients undergoing percutaneous coronary intervention. Thromb Haemost 2019; 119 (02) 340-347
  • 138 Ay C, Jungbauer LV, Sailer T. et al. High concentrations of soluble P-selectin are associated with risk of venous thromboembolism and the P-selectin Thr715 variant. Clin Chem 2007; 53 (07) 1235-1243
  • 139 Falanga A, Marchetti M, Vignoli A. Coagulation and cancer: biological and clinical aspects. J Thromb Haemost 2013; 11 (02) 223-233
  • 140 Mi Y, Yan S, Lu Y, Liang Y, Li C. Venous thromboembolism has the same risk factors as atherosclerosis: a PRISMA-compliant systemic review and meta-analysis. Medicine (Baltimore) 2016; 95 (32) e4495
  • 141 Prisco D, D'Elios MM, Cenci C, Ciucciarelli L, Tamburini C. Cardiovascular oncology: a new discipline inside internal medicine?. Intern Emerg Med 2014; 9 (04) 359-364