Thrombosis Risk in Cancer Patients Receiving Red Blood Cell Transfusions

Seminars in Thrombosis and Hemostasis

Volumn 45, Issue 6, 2019, Pages 648-656

  Ramsey, Glenn ^a,b   Lindholm, Paul F ^a,b  

^a NORTHWESTERN MEMORIAL HOSPITAL   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

cancer; postoperative complications; red blood cell transfusion; venous thromboembolism

Indexed keywords

ARTICLE; CANCER PATIENT; CANCER REGISTRY; CANCER SURGERY; CARDIOVASCULAR RISK; ERYTHROCYTE TRANSFUSION; HOSPITAL PATIENT; HUMAN; MALIGNANT NEOPLASM; PERIOPERATIVE PERIOD; PRIORITY JOURNAL; SURGICAL PATIENT; UROLOGIC SURGERY; VENOUS THROMBOEMBOLISM; BLOOD TRANSFUSION; BLOOD TRANSFUSION REACTION; COMPLICATION; FEMALE; MALE; PROCEDURES; RISK FACTOR; THROMBOSIS;

BLOOD TRANSFUSION; FEMALE; HUMANS; MALE; RISK FACTORS; THROMBOSIS; TRANSFUSION REACTION;

EID: 85071788727     PISSN: 00946176     EISSN: 10989064     Source Type: Journal    
DOI: 10.1055/s-0039-1694763     Document Type: Article

References (71)

1. Weisel J. W. Litvinov R. I. Red blood cells: the forgotten player in hemostasis and thrombosis. J Thromb Haemost: 2019; 17 02 271 282
2. Kroll M. H. Michaelis L. C. Verstovsek S. Mechanisms of thrombogenesis in polycythemia vera. Blood Rev: 2015; 29 04 215 221
3. Barshtein G. Ben-Ami R. Yedgar S. Role of red blood cell flow behavior in hemodynamics and hemostasis. Expert Rev Cardiovasc Ther: 2007; 5 04 743 752
4. Begg T. B. Hearns J. B. Components in blood viscosity. The relative contribution of haematocrit, plasma fibrinogen and other proteins. Clin Sci: 1966; 31 01 87 93
5. Kwaan H. C. Wang J. Hyperviscosity in polycythemia vera and other red cell abnormalities. Semin Thromb Hemost: 2003; 29 05 451 458
6. Turitto V. T. Baumgartner H. R. Platelet interaction with subendothelium in a perfusion system: physical role of red blood cells. Microvasc Res: 1975; 9 03 335 344
7. Chen H. Angerer J. I. Napoleone M., et al. Hematocrit and flow rate regulate the adhesion of platelets to von Willebrand factor. Biomicrofluidics: 2013; 7 06 64113
8. Du V. X. Huskens D. Maas C. Al Dieri R. de Groot P. G. de Laat B. New insights into the role of erythrocytes in thrombus formation. Semin Thromb Hemost: 2014; 40 01 72 80
9. Becatti M. Marcucci R. Gori A. M., et al. Erythrocyte oxidative stress is associated with cell deformability in patients with retinal vein occlusion. J Thromb Haemost: 2016; 14 11 2287 2297
10. Dubovoy T. Engoren M. Thrombotic risks in red blood cell transfusions. Semin Thromb Hemost: 2016; 42 02 102 111
11. Lominadze D. Dean W. L. Involvement of fibrinogen specific binding in erythrocyte aggregation. FEBS Lett: 2002; 517 (1-3): 41 44
12. Byrnes J. R. Duval C. Wang Y., et al. Factor XIIIa-dependent retention of red blood cells in clots is mediated by fibrin α-chain crosslinking. Blood: 2015; 126 16 1940 1948
13. Wohner N. Sótonyi P. Machovich R., et al. Lytic resistance of fibrin containing red blood cells. Arterioscler Thromb Vasc Biol: 2011; 31 10 2306 2313
14. Bosman G. J. Werre J. M. Willekens F. LA. Novotný V. M. Erythrocyte ageing in vivo and in vitro: structural aspects and implications for transfusion. Transfus Med: 2008; 18 06 335 347
15. Chin-Yee I. Arya N. d'Almeida M. S. The red cell storage lesion and its implication for transfusion. Transfus Sci: 1997; 18 03 447 458
16. Rubin O. Crettaz D. Tissot J. D. Lion N. Microparticles in stored red blood cells: submicron clotting bombs? Blood Transfus: 2010; 8 03 s31 s38
17. Gao Y. Lv L. Liu S. Ma G. Su Y. Elevated levels of thrombin-generating microparticles in stored red blood cells. Vox Sang: 2013; 105 01 11 17
18. Donadee C. Raat N. J. Kanias T., et al. Nitric oxide scavenging by red blood cell microparticles and cell-free hemoglobin as a mechanism for the red cell storage lesion. Circulation: 2011; 124 04 465 476
19. Keating F. K. Butenas S. Fung M. K. Schneider D. J. Platelet-white blood cell (WBC) interaction, WBC apoptosis, and procoagulant activity in stored red blood cells. Transfusion: 2011; 51 05 1086 1095
20. Wautier M. P. Héron E. Picot J. Colin Y. Hermine O. Wautier J. L. Red blood cell phosphatidylserine exposure is responsible for increased erythrocyte adhesion to endothelium in central retinal vein occlusion. J Thromb Haemost: 2011; 9 05 1049 1055
21. Wautier J. L. Wautier M. P. Molecular basis of erythrocyte adhesion to endothelial cells in diseases. Clin Hemorheol Microcirc: 2013; 53 (1,2): 11 21
22. Mertens K. Bertina R. M. The contribution of Ca2+ and phospholipids to the activation of human blood-coagulation Factor X by activated Factor IX. Biochem J: 1984; 223 03 607 615
23. Biró E. Sturk-Maquelin K. N. Vogel G. MT., et al. Human cell-derived microparticles promote thrombus formation in vivo in a tissue factor-dependent manner. J Thromb Haemost: 2003; 1 12 2561 2568
24. Goel R. Patel E. U. Cushing M. M., et al. Association of perioperative red blood cell transfusions with venous thromboembolism in a North American registry. JAMA Surg: 2018; 153 09 826 833
25. Thai L. McCarn K. Stott W., et al. Venous thromboembolism in patients with head and neck cancer after surgery. Head Neck: 2013; 35 01 4 9
26. Lee H. K. Kim D. H. Jin U. S. Jeon Y. T. Hwang J. W. Park H. P. Effect of perioperative transfusion of old red blood cells on postoperative complications after free muscle sparing transverse rectus abdominis myocutaneous flap surgery for breast reconstruction. Microsurgery: 2014; 34 06 434 438
27. Sultan S. M. Jackson D. S. Erhard H. A., et al. Risk factors for postoperative venous thromboembolic complications after microsurgical breast reconstruction. J Reconstr Microsurg: 2018; 34 04 227 234
28. Martin J. T. Mahan A. L. Ferraris V. A., et al. Identifying esophagectomy patients at risk for predischarge versus postdischarge venous thromboembolism. Ann Thorac Surg: 2015; 100 03 932 938, discussion 938
29. Ejaz A. Spolverato G. Kim Y., et al. Defining incidence and risk factors of venous thromboemolism after hepatectomy. J Gastrointest Surg: 2014; 18 06 1116 1124
30. Newhook T. E. LaPar D. J. Walters D. M., et al. Impact of postoperative venous thromboembolism on postoperative morbidity, mortality, and resource utilization after hepatectomy. Am Surg: 2015; 81 12 1216 1223
31. Lee F. Y. Chu W. Chan R., et al. Incidence of deep vein thrombosis after colorectal surgery in a Chinese population. ANZ J Surg: 2001; 71 11 637 640
32. Nilsson K. R. Berenholtz S. M. Garrett-Mayer E. Dorman T. Klag M. J. Pronovost P. J. Association between venous thromboembolism and perioperative allogeneic transfusion. Arch Surg: 2007; 142 02 126 132, discussion 133
33. Xenos E. S. Vargas H. D. Davenport D. L. Association of blood transfusion and venous thromboembolism after colorectal cancer resection. Thromb Res: 2012; 129 05 568 572
34. Davenport D. L. Vargas H. D. Kasten M. W. Xenos E. S. Timing and perioperative risk factors for in-hospital and post-discharge venous thromboembolism after colorectal cancer resection. Clin Appl Thromb Hemost: 2012; 18 06 569 575
35. Rottenstreich A. Kalish Y. Kleinstern G. Yaacov A. B. Dux J. Nissan A. Factors associated with thromboembolic events following cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. J Surg Oncol: 2017; 116 07 914 920
36. Sugimachi K. Tajiri H. Kinjo N., et al. Incidence and predictors of deep venous thrombosis after abdominal oncologic surgery: prospective Doppler ultrasound screening. J Surg Res: 2012; 178 02 657 661
37. Bellini G. Teng A. Kotecha N., et al. The identification of risk factors for venous thromboembolism in gastrointestinal oncologic surgery. J Surg Res: 2016; 205 02 279 285
38. Secin F. P. Jiborn T. Bjartell A. S., et al. Multi-institutional study of symptomatic deep venous thrombosis and pulmonary embolism in prostate cancer patients undergoing laparoscopic or robot-assisted laparoscopic radical prostatectomy. Eur Urol: 2008; 53 01 134 145
39. Beyer J. Wessela S. Hakenberg O. W., et al. Incidence, risk profile and morphological pattern of venous thromboembolism after prostate cancer surgery. J Thromb Haemost: 2009; 7 04 597 604
40. Tollefson M. K. Karnes R. J. Rangel L. Carlson R. Boorjian S. A. Blood type, lymphadenectomy and blood transfusion predict venous thromboembolic events following radical prostatectomy with pelvic lymphadenectomy. J Urol: 2014; 191 03 646 651
41. Abel E. J. Wong K. Sado M., et al. Surgical operative time increases the risk of deep venous thrombosis and pulmonary embolism in robotic prostatectomy. JSLS: 2014; 18 02 282 287
42. Alberts B. D. Woldu S. L. Weinberg A. C. Danzig M. R. Korets R. Badani K. K. Venous thromboembolism after major urologic oncology surgery: a focus on the incidence and timing of thromboembolic events after 27,455 operations. Urology: 2014; 84 04 799 806
43. Chen E. C. Papa N. Lawrentschuk N. Bolton D. Sengupta S. Incidence and risk factors of venous thromboembolism after pelvic uro-oncologic surgery - a single center experience. BJU Int: 2016; 117 04 50 53
44. Lee S. J. Seo H. Kim H-C., et al. Effect of intraoperative red blood cell transfusion on postoperative complications after open radical cystectomy: old versus fresh stored blood. Clin Genitourin Cancer: 2015; 13 06 581 587
45. Chappidi M. R. Chalfin H. J. Johnson D. J., et al. Longer average blood storage duration is associated with increased risk of infection and overall morbidity following radical cystectomy. Urol Oncol: 2017; 35 02 38.e17 38.e24
46. Lyon T. D. Tollefson M. K. Shah P. H., et al. Temporal trends in venous thromboembolism after radical cystectomy. Urol Oncol: 2018; 36 08 361.e15 361.e21
47. Bhanvadia S. Kazerouni K. Bazargani S. T., et al. Validating the role of ABO blood type in risk of perioperative venous thromboembolism after radical cystectomy. World J Urol: 2019; 37 01 173 179
48. Yoo S. Song S. H. Go H., et al. Fate of newly developed pulmonary embolism after surgery for renal cell carcinoma with vena cava thrombus. Int Urol Nephrol: 2017; 49 07 1157 1163
49. Clément C. Rossi P. Aissi K., et al. Incidence, risk profile and morphological pattern of lower extremity venous thromboembolism after urological cancer surgery. J Urol: 2011; 186 06 2293 2297
50. Abu-Rustum N. R. Richard S. Wilton A., et al. Transfusion utilization during adnexal or peritoneal cancer surgery: effects on symptomatic venous thromboembolism and survival. Gynecol Oncol: 2005; 99 02 320 326
51. Sandadi S. Lee S. Walter A., et al. Incidence of venous thromboembolism after minimally invasive surgery in patients with newly diagnosed endometrial cancer. Obstet Gynecol: 2012; 120 05 1077 1083
52. Freeman A. H. Barrie A. Lyon L., et al. Venous thromboembolism following minimally invasive surgery among women with endometrial cancer. Gynecol Oncol: 2016; 142 02 267 272
53. Mahdi H. Aljebori Q. Lockart D. Moulton L. Risk of venous thromboembolism after laparoscopic surgery for gynecologic malignancy. J Minim Invasive Gynecol: 2016; 23 07 1057 1062
54. Merkow R. P. Bilimoria K. Y. McCarter M. D., et al. Post-discharge venous thromboembolism after cancer surgery: extending the case for extended prophylaxis. Ann Surg: 2011; 254 01 131 137
55. De Martino R. R. Goodney P. P. Spangler E. L., et al. Variation in thromboembolic complications among patients undergoing commonly performed cancer operations. J Vasc Surg: 2012; 55 04 1035 1040.e4
56. de Almeida J. P. Vincent J. L. Galas F. R., et al. Transfusion requirements in surgical oncology patients: a prospective, randomized controlled trial. Anesthesiology: 2015; 122 01 29 38
57. Khorana A. A. Francis C. W. Blumberg N. Culakova E. Refaai M. A. Lyman G. H. Blood transfusions, thrombosis, and mortality in hospitalized patients with cancer. Arch Intern Med: 2008; 168 21 2377 2381
58. Li M. Guo Q. Hu W. Incidence, risk factors, and outcomes of venous thromboembolism after oncologic surgery: A systematic review and meta-analysis. Thromb Res: 2019; 173 48 56
59. Marušič A. P. Locatelli I. Mrhar A., et al. Influence of prescribed blood products on the incidence of deep vein thrombosis and pulmonary embolism in surgical patients. Clin Appl Thromb Hemost: 2017; 23 08 938 942
60. Patel M. S. Ewing T. Kong A., et al. Risk factors for venous thromboembolism in critically ill nontrauma surgical patients who cannot receive chemical prophylaxis. Am J Surg: 2013; 206 03 300 306
61. Cloney M. Dhillon E. S. Roberts H. Smith Z. A. Koski T. R. Dahdaleh N. S. Predictors of readmissions and reoperations related to venous thromboembolic events after spine surgery: a single-institution experience with 6869 patients. World Neurosurg: 2018; 111 e91 e97
62. Kumar M. A. Boland T. A. Baiou M., et al. Red blood cell transfusion increases the risk of thrombotic events in patients with subarachnoid hemorrhage. Neurocrit Care: 2014; 20 01 84 90
63. Thurn L. Wikman A. Lindqvist P. G. Postpartum blood transfusion and hemorrhage as independent risk factors for venous thromboembolism. Thromb Res: 2018; 165 54 60
64. Dhillon N. K. Smith E. JT. Ko A., et al. The risk factors of venous thromboembolism in massively transfused patients. J Surg Res: 2018; 222 115 121
65. Hershman D. L. Buono D. L. Malin J. McBride R. Tsai W. Y. Neugut A. I. Patterns of use and risks associated with erythropoiesis-stimulating agents among Medicare patients with cancer. J Natl Cancer Inst: 2009; 101 23 1633 1641
66. Desborough M. JR. Colman K. S. Prick B. W., et al. Effect of restrictive versus liberal red cell transfusion strategies on haemostasis: systematic review and meta-analysis. Thromb Haemost: 2017; 117 05 889 898
67. Robitaille N. Lacroix J. Alexandrov L., et al. Excess of veno-occlusive disease in a randomized clinical trial on a higher trigger for red blood cell transfusion after bone marrow transplantation: a canadian blood and marrow transplant group trial. Biol Blood Marrow Transplant: 2013; 19 03 468 473
68. Rogers M. AM. Blumberg N. Bernstein S. J. Flanders S. A. Chopra V. Association between delivery methods for red blood cell transfusion and the risk of venous thromboembolism: a longitudinal study. Lancet Haematol: 2016; 3 12 e563 e571
69. Zander A. L. Olson E. J. Van Gent J. M., et al. Does resuscitation with plasma increase the risk of venous thromboembolism? J Trauma Acute Care Surg: 2015; 78 01 39 43, discussion 43-44
70. Schmidt A. E. Refaai M. A. Blumberg N. Platelet transfusion and thrombosis: more questions than answers. Semin Thromb Hemost: 2016; 42 02 118 124
71. Schmidt A. E. Henrichs K. F. Kirkley S. A. Refaai M. A. Blumberg N. Prophylactic preprocedure platelet transfusion is associated with increased risk of thrombosis and mortality. Am J Clin Pathol: 2017; 149 01 87 94