Risk Factors for Thromboembolic Events and Bleeding in Patients With Stomach Cancer: A Cohort Study



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Abstract

BACKGROUND: Stomach cancer is associated with systemic disturbances, including impaired hemostasis, which may result in thrombosis and bleeding, significantly affecting the prognosis, quality of life, and risk of fatal outcome.

AIM: The study aimed to identify risk factors for thrombosis and bleeding in patients with stomach cancer, assess the prognostic value of existing risk scores using a retrospective analysis of our own findings, and propose ways to improve them.

METHODS: The study analyzed medical records of 178 patients with stomach cancer who were treated at Sechenov University in 2021–2023. The medical records were grouped based on two independent variables: the presence of thromboembolic events (25 patients with and 150 patients without thromboembolic events) and the presence of bleeding (23 patients with and 155 patients without bleeding). The outcomes were assessed by examining imaging findings (ultrasound and computed tomography) specified in medical records, which allowed confirming or ruling out thromboembolic events, as well as initial examination findings and discharge summaries following hospitalization for chemotherapy. Qualitative variables are presented as mean ± standard deviation, whereas categorical variables are presented as absolute values and percentages. Intergroup differences were assessed using the Mann–Whitney and Pearson’s chi-squared tests. Significant associations for thromboembolic events and bleeding were identified using multivariate regression analysis. The prognostic value of scores was assessed using ROC analysis (AUC, sensitivity, specificity). SPSS 23.0 was used for statistical analysis.

RESULTS: Patients with chronic heart failure had an 11-fold greater risk of thromboembolic events than patients without chronic heart failure (odds ratio [OR] 11.12; 95% confidence interval [CI] 3.14–38.74; p = 0.001). Chronic kidney disease was associated with more than a 5-fold greater risk (OR 5.07; 95% CI 2.02–12.71; p = 0.002), and varicose veins with more than an 8-fold greater risk (OR 8.12; 95% CI 2.87–22.94; p = 0.001). Adding these factors to the Khorana score improved its prognostic value: in ROC analysis, AUC was 0.823 compared to 0.615 at baseline. This indicates a high discriminatory capability of the modified model (AUC > 0.8). The REACH score showed a high prognostic value for assessing the risk of bleeding (AUC = 0.738).

CONCLUSION: Adding chronic heart failure, chronic kidney disease, and varicose veins to the Khorana score improves its prognostic value for assessing the risk of thromboembolic events. The REACH score was effective in predicting the risk of bleeding.

About the authors

Margarita P. Zaikina

First Moscow State Medical University

Author for correspondence.
Email: zaikina.rita@gmail.com
ORCID iD: 0000-0001-8118-0522
SPIN-code: 6900-9278

PhD student, Depart. of Faculty Therapy No. 1

Russian Federation, Moscow

Maksim I. Tkachev

First Moscow State Medical University

Email: tkachev_m_i@staff.sechenov.ru
ORCID iD: 0000-0002-2252-7773
SPIN-code: 4898-3310

MD, Cand. Sci. (Medicine), Assistant Professor, Depart. of Cardiovascular Surgery

Russian Federation, Moscow

Dmitry A. Napalkov

First Moscow State Medical University

Email: napalkov_d_a@staff.sechenov.ru
ORCID iD: 0000-0001-6241-2711
SPIN-code: 2894-5010

MD, Dr. Sci. (Medicine), Professor, Depart. of Faculty Therapy No. 1

Russian Federation, Moscow

Anastasia A. Sokolova

First Moscow State Medical University

Email: sokolova_a_a@staff.sechenov.ru
ORCID iD: 0000-0001-5938-8917
SPIN-code: 2153-3542

MD, Dr. Sci. (Medicine), Professor, Depart. of Faculty Therapy No. 1

Russian Federation, Moscow

Victor V. Fomin

First Moscow State Medical University

Email: fomin_v_v_1@staff.sechenov.ru
ORCID iD: 0000-0002-2682-4417
SPIN-code: 8465-2747

MD, Dr. Sci. (Medicine), Professor, Corresponding Member of the Russian Academy of Sciences, Head, Depart. of Faculty Therapy No. 1

Russian Federation, Moscow

References

  1. Sung H, Ferlay J, Siegel RL, et al. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin. 2021;71(3):209–249. doi: 10.3322/caac.21660 EDN: MRLXRI
  2. Peng Q, Zhu J, Zhang Y, Jing Y. Blood hypercoagulability and thrombosis mechanisms in cancer patients — A brief review. Heliyon. 2024;10(19):e38831. doi: 10.1016/j.heliyon.2024.e38831 EDN: HARUTO
  3. Falanga A, Marchetti M, Russo L. Venous thromboembolism in the hematologic malignancies. Curr Opin Oncol. 2012;24(6):702–710. doi: 10.1097/CCO.0b013e3283592331 EDN: YEKMMR
  4. Khorana AA, Dalal M, Lin J, Connolly GC. Incidence and predictors of venous thromboembolism (VTE) among ambulatory high-risk cancer patients undergoing chemotherapy in the United States. Cancer. 2013;119(3):648–655. doi: 10.1002/cncr.27772
  5. Key NS, Khorana AA, Kuderer NM, et al. Venous Thromboembolism Prophylaxis and Treatment in Patients With Cancer: ASCO Clinical Practice Guideline Update. J Clin Oncol. 2020;38(5):496–520. doi: 10.1200/jco.19.01461 EDN: PGIUVH
  6. Timp JF, Braekkan SK, Versteeg HH, Cannegieter SC. Epidemiology of cancer-associated venous thrombosis. Blood. 2013;122(10):1712–1723. doi: 10.1182/blood-2013-04-460121 EDN: OJDFFW
  7. Khorana AA, Francis CW, Culakova E, et al. Thromboembolism is a leading cause of death in cancer patients receiving outpatient chemotherapy. J Thromb Haemost. 2007;5(3):632–634. doi: 10.1111/j.1538-7836.2007.02374.x
  8. Lyman GH, Bohlke K, Khorana AA, et al; American Society of Clinical Oncology. Venous thromboembolism prophylaxis and treatment in patients with cancer: american society of clinical oncology clinical practice guideline update 2014. J Clin Oncol. 2015;33(6):654–656. doi: 10.1200/JCO.2014.59.7351
  9. Li A, Garcia DA, Lyman GH, Carrier M. Direct oral anticoagulant (DOAC) versus low-molecular-weight heparin (LMWH) for treatment of cancer associated thrombosis (CAT): A systematic review and meta-analysis. Thromb Res. 2019;173:158–163. doi: 10.1016/j.thromres.2018.02.144 EDN: CAWXOK
  10. Khorana AA, Kuderer NM, Culakova E, et al. Development and validation of a predictive model for chemotherapy-associated thrombosis. Blood. 2008;111(10):4902–4907. doi: 10.1182/blood-2007-10-116327
  11. Somonova OV, Antukh EA, Vardanyan AV, et al. Thromboembolic complications. Zlokachestvennye organy. 2023;13(3s2-2):167–178. doi: 10.18027/2224-5057-2023-13-3s2-2-167-178 EDN: WOYENK
  12. Mulder FI, Candeloro M, Kamphuisen PW, et al; CAT-prediction collaborators. The Khorana score for prediction of venous thromboembolism in cancer patients: a systematic review and meta-analysis. Haematologica. 2019;104(6):1277–1287. doi: 10.3324/haematol.2018.209114
  13. 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(9):1494–1501. doi: 10.3324/haematol.2017.169060
  14. Englisch C, Nopp S, Moik F, et al. The Vienna CATScore for predicting cancer-associated venous thromboembolism: an external validation across multiple time points. ESMO Open. 2025;10(2):104130. doi: 10.1016/j.esmoop.2024.104130 EDN: LGYTJH
  15. Tang L, Wu YY, Lip GY, et al. Heart failure and risk of venous thromboembolism: a systematic review and meta-analysis. Lancet Haematol. 2016;3(1):e30–44. doi: 10.1016/S2352-3026(15)00228-8
  16. Königsbrügge O, Lötsch F, Reitter EM, et al. Presence of varicose veins in cancer patients increases the risk for occurrence of venous thromboembolism. J Thromb Haemost. 2013;11(11):1993–2000. doi: 10.1111/jth.12408
  17. Zhan Y, Fu X, Bi W, Li G. Risk factors for venous thromboembolism in patients with chronic kidney disease: a systematic review and meta-analysis. Ren Fail. 2024;46(2):2431149. doi: 10.1080/0886022X.2024.2431149
  18. Poénou G, Tolédano E, Helfer H, et al. Assessment of bleeding risk in cancer patients treated with anticoagulants for venous thromboembolic events. Front Cardiovasc Med. 2023;10:1132156. doi: 10.3389/fcvm.2023.1132156
  19. Escobar A, Salem AM, Dickson K, et al. Anticoagulation and bleeding in the cancer patient. Support Care Cancer. 2022;30(10):8547–8557. doi: 10.1007/s00520-022-07136-w EDN: NZKIER
  20. Wilkins T, Wheeler B, Carpenter M. Upper Gastrointestinal Bleeding in Adults: Evaluation and Management. Am Fam Physician. 2020;101(5):294–300. EDN: MIQSGI
  21. Costable NJ, Greenwald DA. Upper Gastrointestinal Bleeding. Clin Geriatr Med. 2021;37(1):155–172. doi: 10.1016/j.cger.2020.09.001 EDN: FVGGVM
  22. Bosch FTM, Mulder FI, Huisman MV, et al. Risk factors for gastrointestinal bleeding in patients with gastrointestinal cancer using edoxaban. J Thromb Haemost. 2021;19(12):3008–3017. doi: 10.1111/jth.15516 EDN: TWPDKJ

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