Red blood cell transfusion in surgical cancer patients: Targets, risks, mechanistic understanding and further therapeutic opportunities

Transfusion and Apheresis Science

Volumn 56, Issue 3, 2017, Pages 291-304

  Tzounakas, Vassilis L ^a   Seghatchian, Jerard ^b   Grouzi, Elissavet ^c   Kokoris, Styliani ^d   Antonelou, Marianna H ^a  

^a UNIVERSITY OF ATHENS   (Greece)

^b International Consultancy in Blood Components Quality Safety Improvement   (United Kingdom)

^c Saint Savvas General Anticancer Hospital   (Greece)

^d IASO GENERAL HOSPITAL   (Greece)

Author keywords

Cancer recurrence; Donor and recipient variation; Perioperative transfusion; Red blood cell storage lesion; TRIM

Indexed keywords

BIOLOGICAL RESPONSE MODIFIER; PLASTICIZER;

ADVERSE OUTCOME; ANEMIA; BLOOD CLOTTING; CANCER MORTALITY; CANCER PATIENT; CANCER PROGNOSIS; CANCER RECURRENCE; ERYTHROCYTE PRESERVATION; ERYTHROCYTE TRANSFUSION; HUMAN; IMMUNOCOMPETENCE; IMMUNOSTIMULATION; INFECTION; INFLAMMATION; LEUKOCYTE; PERIOPERATIVE PERIOD; PERSONALIZED MEDICINE; REVIEW; RISK ASSESSMENT; SOLID MALIGNANT NEOPLASM; SURGICAL PATIENT; THROMBOCYTE; THROMBOSIS; NEOPLASM; PATHOLOGY; PROCEDURES; RISK;

ANEMIA; ERYTHROCYTE TRANSFUSION; HUMANS; NEOPLASMS; RISK;

EID: 85020723074     PISSN: 14730502     EISSN: 18781683     Source Type: Journal    
DOI: 10.1016/j.transci.2017.05.015     Document Type: Review

References (218)

1. Antonelou, M.H., Seghatchian, J., Insights into red blood cell storage lesion: toward a new appreciation. Transfus Apher Sci 55 (2016), 292–301.
2. McAteer, M.J., Dumont, L.J., Cancelas, J., Rugg, N., Vassallo, R., Whitley, P., et al. Multi-institutional randomized control study of haemolysis in stored red cell units prepared manually or by an automated system. Vox Sang 99 (2010), 34–43.
3. Dumont, L.J., AuBuchon, J.P., Evaluation of proposed FDA criteria for the evaluation of radiolabeled red cell recovery trials. Transfusion 48 (2008), 1053–1060.
4. Tzounakas, V.L., Kriebardis, A.G., Papassideri, I.S., Antonelou, M.H., Donor-variation effect on red blood cell storage lesion: a close relationship emerges. Proteomics Clin Appl, 2016.
5. Sparrow, R.L., Red blood cell components: time to revisit the sources of variability. Blood Transfus 15 (2017), 116–125.
6. Ho, J., Sibbald, W.J., Chin-Yee, I.H., Effects of storage on efficacy of red cell transfusion: when is it not safe?. Crit Care Med 31 (2003), S687–S697.
7. Escobar, G.A., Cheng, A.M., Moore, E.E., Johnson, J.L., Tannahill, C., Baker, H.V., et al. Stored packed red blood cell transfusion up-regulates inflammatory gene expression in circulating leukocytes. Ann Surg 246 (2007), 129–134.
8. Garraud, O., Tariket, S., Sut, C., Haddad, A., Aloui, C., Chakroun, T., et al. Transfusion as an inflammation hit: knowns and unknowns. Front Immunol, 7, 2016, 534.
9. Fransen, E., Maessen, J., Dentener, M., Senden, N., Buurman, W., Impact of blood transfusions on inflammatory mediator release in patients undergoing cardiac surgery. Chest 116 (1999), 1233–1239.
10. Ishijima, N., Suzuki, H., Blood transfusion and postoperative serum interleukin-6 levels in colorectal cancer patients. Hepatogastroenterology 45 (1998), 1011–1013.
11. van Hilten, J.A., van de Watering, L.M., van Bockel, J.H., van de Velde, C.J., Kievit, J., Brand, R., et al. Effects of transfusion with red cells filtered to remove leucocytes: randomised controlled trial in patients undergoing major surgery. BMJ, 328, 2004, 1281.
12. Antonelou, M.H., Seghatchian, J., Update on extracellular vesicles inside red blood cell storage units: adjust the sails closer to the new wind. Transfus Apher Sci 55 (2016), 92–104.
13. Danesh, A., Inglis, H.C., Jackman, R.P., Wu, S., Deng, X., Muench, M.O., et al. Exosomes from red blood cell units bind to monocytes and induce proinflammatory cytokines, boosting T-cell responses in vitro. Blood 123 (2014), 687–696.
14. Cognasse, F., Hamzeh-Cognasse, H., Laradi, S., Chou, M.L., Seghatchian, J., Burnouf, T., et al. The role of microparticles in inflammation and transfusion: a concise review. Transfus Apher Sci 53 (2015), 159–167.
15. Davenport, R.D., Pathophysiology of hemolytic transfusion reactions. Semin Hematol 42 (2005), 165–168.
16. Gladwin, M.T., Kim-Shapiro, D.B., Storage lesion in banked blood due to hemolysis-dependent disruption of nitric oxide homeostasis. Curr Opin Hematol 16 (2009), 515–523.
17. Shalev, O., Manny, N., Sharon, R., Posttransfusional hemolysis in recipients of glucose-6-phosphate dehydrogenase-deficient erythrocytes. Vox Sang 64 (1993), 94–98.
18. Huang, C.S., Sung, Y.C., Huang, M.J., Yang, C.S., Shei, W.S., Tang, T.K., Content of reduced glutathione and consequences in recipients of glucose-6-phosphate dehydrogenase deficient red blood cells. Am J Hematol 57 (1998), 187–192.
19. Hod, E.A., Red blood cell transfusion-induced inflammation: myth or reality. ISBT Sci Ser 10 (2015), 188–191.
20. Hudson, T.J., Genome variation and personalized cancer medicine. J Intern Med 274 (2013), 440–450.
21. Dunn, A., Carter, J., Carter, H., Anemia at the end of life: prevalence, significance, and causes in patients receiving palliative care. J Pain Symptom Manage 26 (2003), 1132–1139.
22. Uceda Torres, M.E., Rodriguez Rodriguez, J.N., Sanchez Ramos, J.L., Alvarado Gomez, F., Transfusion in palliative cancer patients: a review of the literature. J Palliat Med 17 (2014), 88–104.
23. Ludwig, H., Van Belle, S., Barrett-Lee, P., Birgegard, G., Bokemeyer, C., Gascon, P., et al. The European Cancer Anaemia Survey (ECAS): a large, multinational, prospective survey defining the prevalence, incidence, and treatment of anaemia in cancer patients. Eur J Cancer 40 (2004), 2293–2306.
24. Neoh, K., Stanworth, S., Pasricha, S.R., Bennett, M.I., Estimating prevalence of functional iron deficiency anaemia in advanced cancer. Support Care Cancer 25 (2017), 1209–1214.
25. Gilreath, J.A., Stenehjem, D.D., Rodgers, G.M., Diagnosis and treatment of cancer-related anemia. Am J Hematol 89 (2014), 203–212.
26. Velasquez, J.F., Cata, J.P., Transfusions of blood products and cancer outcomes. Rev Esp Anestesiol Reanim 62 (2015), 461–467.
27. Weber, R.S., Jabbour, N., Martin, R.C. II, Anemia and transfusions in patients undergoing surgery for cancer. Ann Surg Oncol 15 (2008), 34–45.
28. Whitaker, B.I., The United States Department of Health and Human Services. 2015, 2011 National Blood Collection and Utilization Survey, Rockville, MD.
29. Valsami, S., Grouzi, E., Pouliakis, A., Fountoulaki-Paparisos, L., Kyriakou, E., Gavalaki, M., et al. Red blood cell transfusions in Greece: results of a survey of red blood cell use in 2013. Turk J Haematol 34 (2017), 52–58.
30. Nakamura, T., Grimer, R., Gaston, C., Carter, S., Tillman, R., Abudu, A., et al. The relationship between pretreatment anaemia and survival in patients with adult soft tissue sarcoma. J Orthop Sci 18 (2013), 987–993.
31. de Almeida, J.P., Vincent, J.L., Galas, F.R., de Almeida, E.P., Fukushima, J.T., Osawa, E.A., et al. Transfusion requirements in surgical oncology patients: a prospective, randomized controlled trial. Anesthesiology 122 (2015), 29–38.
32. Bergamin, F.S., Almeida, J.P., Landoni, G., Galas, F.R., Fukushima, J.T., Fominskiy, E., et al. Liberal versus restrictive transfusion strategy in critically ill oncologic patients: the transfusion requirements in critically ill oncologic patients randomized controlled trial. Crit Care Med, 2017.
33. Loor, G., Rajeswaran, J., Li, L., Sabik, J.F. III, Blackstone, E.H., McCrae, K.R., et al. The least of 3 evils: exposure to red blood cell transfusion, anemia, or both?. J Thorac Cardiovasc Surg 146 (2013), 1480–1487 e6.
34. Kim, Y., Spolverato, G., Lucas, D.J., Ejaz, A., Xu, L., Wagner, D., et al. Red cell transfusion triggers and postoperative outcomes after major surgery. J Gastrointest Surg 19 (2015), 2062–2073.
35. Al-Refaie, W.B., Parsons, H.M., Markin, A., Abrams, J., Habermann, E.B., Blood transfusion and cancer surgery outcomes: a continued reason for concern. Surgery 152 (2012), 344–354.
36. Rygard, S.L., Holst, L.B., Wetterslev, J., Johansson, P.I., Perner, A., Higher vs. lower haemoglobin threshold for transfusion in septic shock: subgroup analyses of the TRISS trial. Acta Anaesthesiol Scand 61 (2017), 166–175.
37. Holst, L.B., Haase, N., Wetterslev, J., Wernerman, J., Guttormsen, A.B., Karlsson, S., et al. Lower versus higher hemoglobin threshold for transfusion in septic shock. N Engl J Med 371 (2014), 1381–1391.
38. Hebert, P.C., Wells, G., Blajchman, M.A., Marshall, J., Martin, C., Pagliarello, G., et al. A multicenter, randomized, controlled clinical trial of transfusion requirements in critical care. Transfusion Requirements in Critical Care Investigators, Canadian Critical Care Trials Group. N Engl J Med 340 (1999), 409–417.
39. Hebert, P.C., Carson, J.L., Transfusion threshold of 7 g per deciliter – the new normal. N Engl J Med 371 (2014), 1459–1461.
40. Cata, J.P., Wang, H., Gottumukkala, V., Reuben, J., Sessler, D.I., Inflammatory response, immunosuppression, and cancer recurrence after perioperative blood transfusions. Br J Anaesth 110 (2013), 690–701.
41. Opelz, G., Graver, B., Terasaki, P.I., Induction of high kidney graft survival rate by multiple transfusion. Lancet 1 (1981), 1223–1225.
42. Hu, W., Zhang, Y., Jiang, Z., Wang, L., Li, J., Chen, S., et al. The tumor promoting roles of erythropoietin/erythropoietin receptor signaling pathway in gastric cancer. Tumour Biol 37 (2016), 11523–11533.
43. Cao, Y., Erythropoietin in cancer: a dilemma in risk therapy. Trends Endocrinol Metab 24 (2013), 190–199.
44. Carson, J.L., Guyatt, G., Heddle, N.M., Grossman, B.J., Cohn, C.S., Fung, M.K., et al. Clinical practice guidelines from the AABB: red blood cell transfusion thresholds and storage. JAMA 316 (2016), 2025–2035.
45. Carson, J.L., Stanworth, S.J., Roubinian, N., Fergusson, D.A., Triulzi, D., Doree, C., et al. Transfusion thresholds and other strategies for guiding allogeneic red blood cell transfusion. Cochrane Database Syst Rev, 10, 2016, CD002042.
46. Goubran, H.A., Elemary, M., Radosevich, M., Seghatchian, J., El-Ekiaby, M., Burnouf, T., Impact of transfusion on cancer growth and outcome. Cancer Growth Metastasis 9 (2016), 1–8.
47. Amato, A., Pescatori, M., Perioperative blood transfusions for the recurrence of colorectal cancer. Cochrane Database Syst Rev, 2006, CD005033.
48. Acheson, A.G., Brookes, M.J., Spahn, D.R., Effects of allogeneic red blood cell transfusions on clinical outcomes in patients undergoing colorectal cancer surgery: a systematic review and meta-analysis. Ann Surg 256 (2012), 235–244.
49. Luan, H., Ye, F., Wu, L., Zhou, Y., Jiang, J., Perioperative blood transfusion adversely affects prognosis after resection of lung cancer: a systematic review and a meta-analysis. BMC Surg, 14, 2014, 34.
50. Wang, T., Luo, L., Huang, H., Yu, J., Pan, C., Cai, X., et al. Perioperative blood transfusion is associated with worse clinical outcomes in resected lung cancer. Ann Thorac Surg 97 (2014), 1827–1837.
51. Yao, H.S., Wang, Q., Wang, W.J., Hu, Z.Q., Intraoperative allogeneic red blood cell transfusion in ampullary cancer outcome after curative pancreatoduodenectomy: a clinical study and meta-analysis. World J Surg 32 (2008), 2038–2046.
52. Hwang, H.K., Jung, M.J., Lee, S.H., Kang, C.M., Lee, W.J., Adverse oncologic effects of intraoperative transfusion during pancreatectomy for left-sided pancreatic cancer: the need for strict transfusion policy. J Hepatobiliary Pancreat Sci 23 (2016), 497–507.
53. Sun, C., Wang, Y., Yao, H.S., Hu, Z.Q., Allogeneic blood transfusion and the prognosis of gastric cancer patients: systematic review and meta-analysis. Int J Surg 13 (2015), 102–110.
54. Elmi, M., Mahar, A., Kagedan, D., Law, C.H., Karanicolas, P.J., Lin, Y., et al. The impact of blood transfusion on perioperative outcomes following gastric cancer resection: an analysis of the American College of Surgeons National Surgical Quality Improvement Program database. Can J Surg 59 (2016), 322–329.
55. Kneuertz, P.J., Patel, S.H., Chu, C.K., Maithel, S.K., Sarmiento, J.M., Delman, K.A., et al. Effects of perioperative red blood cell transfusion on disease recurrence and survival after pancreaticoduodenectomy for ductal adenocarcinoma. Ann Surg Oncol 18 (2011), 1327–1334.
56. Soria, F., de Martino, M., Leitner, C.V., Moschini, M., Shariat, S.F., Klatte, T., Perioperative allogenic blood transfusion in renal cell carcinoma: risk factors and effect on long-term outcomes. Clin Genitourin Cancer, 2016.
57. Park, Y.H., Kim, Y.J., Kang, S.H., Kim, H.H., Byun, S.S., Lee, J.Y., et al. Association between perioperative blood transfusion and oncologic outcomes after curative surgery for renal cell carcinoma. J Cancer 7 (2016), 965–972.
58. Siemens, D.R., Jaeger, M.T., Wei, X., Vera-Badillo, F., Booth, C.M., Peri-operative allogeneic blood transfusion and outcomes after radical cystectomy: a population-based study. World J Urol, 2017.
59. Sui, W., Onyeji, I.C., Matulay, J.T., James, M.B., Theofanides, M.C., Wenske, S., et al. Perioperative blood transfusion in radical cystectomy: analysis of the National Surgical Quality Improvement Program database. Int J Urol 23 (2016), 745–750.
60. Chalfin, H.J., Liu, J.J., Gandhi, N., Feng, Z., Johnson, D., Netto, G.J., et al. Blood transfusion is associated with increased perioperative morbidity and adverse oncologic outcomes in bladder cancer patients receiving neoadjuvant chemotherapy and radical cystectomy. Ann Surg Oncol 23 (2016), 2715–2722.
61. Kim, J.K., Kim, H.S., Park, J., Jeong, C.W., Ku, J.H., Kim, H.H., et al. Perioperative blood transfusion as a significant predictor of biochemical recurrence and survival after radical prostatectomy in patients with prostate cancer. PLOS ONE, 11, 2016, e0154918.
62. Li, S.L., Ye, Y., Yuan, X.H., Association between allogeneic or autologous blood transfusion and survival in patients after radical prostatectomy: a systematic review and meta-analysis. PLOS ONE, 12, 2017, e0171081.
63. Tartter, P.I., Blood transfusion and infectious complications following colorectal cancer surgery. Br J Surg 75 (1988), 789–792.
64. Tartter, P.I., Perioperative blood transfusion and colorectal cancer recurrence: a review. J Surg Oncol 39 (1988), 197–200.
65. Aquina, C.T., Blumberg, N., Becerra, A.Z., Boscoe, F.P., Schymura, M.J., Noyes, K., et al. Association among blood transfusion, sepsis, and decreased long-term survival after colon cancer resection. Ann Surg, 2016.
66. Morner, M.E., Edgren, G., Martling, A., Gunnarsson, U., Egenvall, M., Preoperative anaemia and perioperative red blood cell transfusion as prognostic factors for recurrence and mortality in colorectal cancer – a Swedish cohort study. Int J Colorectal Dis 32 (2017), 223–232.
67. Ling, F.C., Hoelscher, A.H., Vallbohmer, D., Schmidt, D., Picker, S., Gathof, B.S., et al. Leukocyte depletion in allogeneic blood transfusion does not change the negative influence on survival following transthoracic resection for esophageal cancer. J Gastrointest Surg 13 (2009), 581–586.
68. Reeh, M., Ghadban, T., Dedow, J., Vettorazzi, E., Uzunoglu, F.G., Nentwich, M., et al. Allogenic blood transfusion is associated with poor perioperative and long-term outcome in esophageal cancer. World J Surg 41 (2017), 208–215.
69. Reim, D., Strobl, A.N., Buchner, C., Schirren, R., Mueller, W., Luppa, P., et al. Perioperative transfusion of leukocyte depleted blood products in gastric cancer patients negatively influences oncologic outcome: a retrospective propensity score weighted analysis on 610 curatively resected gastric cancer patients. Medicine (Baltimore), 95, 2016, e4322.
70. Woolley, A.L., Hogikyan, N.D., Gates, G.A., Haughey, B.H., Schechtman, K.B., Goldenberg, J.L., Effect of blood transfusion on recurrence of head and neck carcinoma. Retrospective review and meta-analysis. Ann Otol Rhinol Laryngol 101 (1992), 724–730.
71. Taniguchi, Y., Okura, M., Prognostic significance of perioperative blood transfusion in oral cavity squamous cell carcinoma. Head Neck 25 (2003), 931–936.
72. Yeoh, T.Y., Scavonetto, F., Weingarten, T.N., Karnes, R.J., van Buskirk, C.M., Hanson, A.C., et al. Perioperative allogeneic nonleukoreduced blood transfusion and prostate cancer outcomes after radical prostatectomy. Transfusion 54 (2014), 2175–2181.
73. Boehm, K., Beyer, B., Tennstedt, P., Schiffmann, J., Budaeus, L., Haese, A., et al. No impact of blood transfusion on oncological outcome after radical prostatectomy in patients with prostate cancer. World J Urol 33 (2015), 801–806.
74. Linder, B.J., Thompson, R.H., Leibovich, B.C., Cheville, J.C., Lohse, C.M., Gastineau, D.A., et al. The impact of perioperative blood transfusion on survival after nephrectomy for non-metastatic renal cell carcinoma (RCC). BJU Int 114 (2014), 368–374.
75. Moschini, M., Soria, F., Abufaraj, M., Foerster, B., D'Andrea, D., Damiano, R., et al. Impact of intra- and postoperative blood transfusion on the incidence, timing, and pattern of disease recurrence after radical cystectomy. Clin Genitourin Cancer, 2017.
76. De Oliveira, G.S. Jr., Schink, J.C., Buoy, C., Ahmad, S., Fitzgerald, P.C., McCarthy, R.J., The association between allogeneic perioperative blood transfusion on tumour recurrence and survival in patients with advanced ovarian cancer. Transfus Med 22 (2012), 97–103.
77. Warner, L.L., Dowdy, S.C., Martin, J.R., Lemens, M.A., McGree, M.E., Weaver, A.L., et al. The impact of perioperative packed red blood cell transfusion on survival in epithelial ovarian cancer. Int J Gynecol Cancer 23 (2013), 1612–1619.
78. Bogani, G., Ditto, A., Martinelli, F., Signorelli, M., Chiappa, V., Lopez, C., et al. Impact of blood transfusions on survival of locally advanced cervical cancer patients undergoing neoadjuvant chemotherapy plus radical surgery. Int J Gynecol Cancer 27 (2017), 514–522.
79. Eickhoff, J.H., Andersen, J., Laybourn, C., Perioperative blood transfusion does not promote recurrence and death after mastectomy for breast cancer. The Danish Breast Cancer Cooperative Group. Br J Surg 78 (1991), 1358–1361.
80. Rinker, B.D., Bowling, J.T., Vasconez, H.C., Blood transfusion and risk of metastatic disease or recurrence in patients undergoing immediate TRAM flap breast reconstruction: a clinical study and meta-analysis. Plast Reconstr Surg 119 (2007), 2001–2007.
81. Zaw, A.S., Kantharajanna, S.B., Maharajan, K., Tan, B., Vellayappan, B., Kumar, N., Perioperative blood transfusion: does it influence survival and cancer progression in metastatic spine tumor surgery?. Transfusion 57 (2017), 440–450.
82. Paulino Pereira, N.R., Beks, R.B., Janssen, S.J., Harris, M.B., Hornicek, F.J., Ferrone, M.L., et al. Are allogeneic blood transfusions associated with decreased survival after surgical treatment for spinal metastases?. Spine J 16 (2016), 951–961.
83. Yeh, J.J., Gonen, M., Tomlinson, J.S., Idrees, K., Brennan, M.F., Fong, Y., Effect of blood transfusion on outcome after pancreaticoduodenectomy for exocrine tumour of the pancreas. Br J Surg 94 (2007), 466–472.
84. van de Watering, L.M., Brand, A., Houbiers, J.G., Klein Kranenbarg, W.M., Hermans, J., van de Velde, C., Perioperative blood transfusions, with or without allogeneic leucocytes, relate to survival, not to cancer recurrence. Br J Surg 88 (2001), 267–272.
85. Lange, M.M., van Hilten, J.A., van de Watering, L.M., Bijnen, B.A., Roumen, R.M., Putter, H., et al. Leucocyte depletion of perioperative blood transfusion does not affect long-term survival and recurrence in patients with gastrointestinal cancer. Br J Surg 96 (2009), 734–740.
86. Koch, M., Antolovic, D., Reissfelder, C., Rahbari, N.N., Holoch, J., Michalski, I., et al. Leucocyte-depleted blood transfusion is an independent predictor of surgical morbidity in patients undergoing elective colon cancer surgery – a single-center analysis of 531 patients. Ann Surg Oncol 18 (2011), 1404–1411.
87. Perisanidis, C., Dettke, M., Papadogeorgakis, N., Schoppmann, A., Mittlbock, M., Kyzas, P.A., et al. Transfusion of allogenic leukocyte-depleted packed red blood cells is associated with postoperative morbidity in patients undergoing oral and oropharyngeal cancer surgery. Oral Oncol 48 (2012), 372–378.
88. Ng, T., Ryder, B.A., Chern, H., Sellke, F.W., Machan, J.T., Harrington, D.T., et al. Leukocyte-depleted blood transfusion is associated with decreased survival in resected early-stage lung cancer. J Thorac Cardiovasc Surg 143 (2012), 815–819.
89. Mynster, T., Nielsen, H.J., Storage time of transfused blood and disease recurrence after colorectal cancer surgery. Dis Colon Rectum 44 (2001), 955–964.
90. Edna, T.H., Bjerkeset, T., Perioperative blood transfusions reduce long-term survival following surgery for colorectal cancer. Dis Colon Rectum 41 (1998), 451–459.
91. Cata, J.P., Klein, E.A., Hoeltge, G.A., Dalton, J.E., Mascha, E., O'Hara, J., et al. Blood storage duration and biochemical recurrence of cancer after radical prostatectomy. Mayo Clin Proc 86 (2011), 120–127.
92. Heddle, N.M., Cook, R.J., Arnold, D.M., Liu, Y., Barty, R., Crowther, M.A., et al. Effect of short-term vs. long-term blood storage on mortality after transfusion. N Engl J Med, 375, 2016.
93. Vamvakas, E.C., Possible mechanisms of allogeneic blood transfusion-associated postoperative infection. Transfus Med Rev 16 (2002), 144–160.
94. Jensen, L.S., Andersen, A.J., Christiansen, P.M., Hokland, P., Juhl, C.O., Madsen, G., et al. Postoperative infection and natural killer cell function following blood transfusion in patients undergoing elective colorectal surgery. Br J Surg 79 (1992), 513–516.
95. Hendrickson, J.E., Hillyer, C.D., Noninfectious serious hazards of transfusion. Anesth Analg 108 (2009), 759–769.
96. Grivennikov, S.I., Greten, F.R., Karin, M., Immunity, inflammation, and cancer. Cell 140 (2010), 883–899.
97. Mantovani, A., Allavena, P., Sica, A., Balkwill, F., Cancer-related inflammation. Nature 454 (2008), 436–444.
98. Blajchman, M.A., Transfusion-associated immunomodulation and universal white cell reduction: are we putting the cart before the horse?. Transfusion 39 (1999), 665–670.
99. Heiss, M.M., Fraunberger, P., Delanoff, C., Stets, R., Allgayer, H., Strohlein, M.A., et al. Modulation of immune response by blood transfusion: evidence for a differential effect of allogeneic and autologous blood in colorectal cancer surgery. Shock 8 (1997), 402–408.
100. Blajchman, M.A., Bardossy, L., Carmen, R., Sastry, A., Singal, D.P., Allogeneic blood transfusion-induced enhancement of tumor growth: two animal models showing amelioration by leukodepletion and passive transfer using spleen cells. Blood 81 (1993), 1880–1882.
101. Kirkley, S.A., Cowles, J., Pellegrini, V.D. Jr., Harris, C.M., Boyd, A.D., Blumberg, N., Cytokine secretion after allogeneic or autologous blood transfusion. Lancet, 345, 1995, 527.
102. Giannattasio, A., Weil, S., Kloess, S., Ansari, N., Stelzer, E.H., Cerwenka, A., et al. Cytotoxicity and infiltration of human NK cells in in vivo-like tumor spheroids. BMC Cancer, 15, 2015, 351.
103. Matsumoto, Y., Tsujimoto, H., Ono, S., Shinomiya, N., Miyazaki, H., Hiraki, S., et al. Abdominal infection suppresses the number and activity of intrahepatic natural killer cells and promotes tumor growth in a murine liver metastasis model. Ann Surg Oncol 23:Suppl. 2 (2016), S257–S265.
104. Antonelou, M.H., Tzounakas, V.L., Velentzas, A.D., Stamoulis, K.E., Kriebardis, A.G., Papassideri, I.S., Effects of pre-storage leukoreduction on stored red blood cells signaling: a time-course evaluation from shape to proteome. J Proteomics 76 Spec No (2012), 220–238.
105. Hess, J.R., Greenwalt, T.G., Storage of red blood cells: new approaches. Transfus Med Rev 16 (2002), 283–295.
106. Lawrance, R.J., Cooper, A.J., Loizidou, M., Alexander, P., Taylor, I., Blood transfusion and recurrence of colorectal cancer: the role of platelet derived growth factors. Br J Surg 77 (1990), 1106–1109.
107. Frabetti, F., Musiani, D., Marini, M., Fanelli, C., Coppola, S., Ghibelli, L., et al. White cell apoptosis in packed red cells. Transfusion 38 (1998), 1082–1089.
108. Humbert, J.R., Fermin, C.D., Winsor, E.L., Early damage to granulocytes during storage. Semin Hematol 28 (1991), 10–13.
109. Nielsen, H.J., Reimert, C.M., Pedersen, A.N., Brunner, N., Edvardsen, L., Dybkjaer, E., et al. Time-dependent, spontaneous release of white cell- and platelet-derived bioactive substances from stored human blood. Transfusion 36 (1996), 960–965.
110. Bury, T.B., Corhay, J.L., Radermecker, M.F., Histamine-induced inhibition of neutrophil chemotaxis and T-lymphocyte proliferation in man. Allergy 47 (1992), 624–629.
111. Karam, O., Tucci, M., Toledano, B.J., Robitaille, N., Cousineau, J., Thibault, L., et al. Length of storage and in vitro immunomodulation induced by prestorage leukoreduced red blood cells. Transfusion 49 (2009), 2326–2334.
112. Cardo, L.J., Wilder, D., Salata, J., Neutrophil priming, caused by cell membranes and microvesicles in packed red blood cell units, is abrogated by leukocyte depletion at collection. Transfus Apher Sci 38 (2008), 117–125.
113. Belizaire, R.M., Prakash, P.S., Richter, J.R., Robinson, B.R., Edwards, M.J., Caldwell, C.C., et al. Microparticles from stored red blood cells activate neutrophils and cause lung injury after hemorrhage and resuscitation. J Am Coll Surg, 2012.
114. Hod, E.A., Zhang, N., Sokol, S.A., Wojczyk, B.S., Francis, R.O., Ansaldi, D., et al. Transfusion of red blood cells after prolonged storage produces harmful effects that are mediated by iron and inflammation. Blood 115 (2010), 4284–4292.
115. McFaul, S.J., Corley, J.B., Mester, C.W., Nath, J., Packed blood cells stored in AS-5 become proinflammatory during storage. Transfusion 49 (2009), 1451–1460.
116. Sparrow, R.L., Patton, K.A., Supernatant from stored red blood cell primes inflammatory cells: influence of prestorage white cell reduction. Transfusion 44 (2004), 722–730.
117. Silliman, C.C., Clay, K.L., Thurman, G.W., Johnson, C.A., Ambruso, D.R., Partial characterization of lipids that develop during the routine storage of blood and prime the neutrophil NADPH oxidase. J Lab Clin Med 124 (1994), 684–694.
118. Fox, L.M., Cox, D.G., Lockridge, J.L., Wang, X., Chen, X., Scharf, L., et al. Recognition of lyso-phospholipids by human natural killer T lymphocytes. PLoS Biol, 7, 2009, e1000228.
119. Olofsson, K.E., Andersson, L., Nilsson, J., Bjorkbacka, H., Nanomolar concentrations of lysophosphatidylcholine recruit monocytes and induce pro-inflammatory cytokine production in macrophages. Biochem Biophys Res Commun 370 (2008), 348–352.
120. Baumgartner, J.M., Silliman, C.C., Moore, E.E., Banerjee, A., McCarter, M.D., Stored red blood cell transfusion induces regulatory T cells. J Am Coll Surg 208 (2009), 110–119.
121. Ghio, M., Contini, P., Negrini, S., Mazzei, C., Zocchi, M.R., Poggi, A., Down regulation of human natural killer cell-mediated cytolysis induced by blood transfusion: role of transforming growth factor-beta(1), soluble Fas ligand, and soluble Class I human leukocyte antigen. Transfusion 51 (2011), 1567–1573.
122. Muszynski, J., Nateri, J., Nicol, K., Greathouse, K., Hanson, L., Hall, M., Immunosuppressive effects of red blood cells on monocytes are related to both storage time and storage solution. Transfusion 52 (2012), 794–802.
123. Ottonello, L., Ghio, M., Contini, P., Bertolotto, M., Bianchi, G., Montecucco, F., et al. Nonleukoreduced red blood cell transfusion induces a sustained inhibition of neutrophil chemotaxis by stimulating in vivo production of transforming growth factor-beta1 by neutrophils: role of the immunoglobulinlike transcript 1, sFasL, and sHLA-I. Transfusion 47 (2007), 1395–1404.
124. Long, K., Meier, C., Bernard, A., Williams, D., Davenport, D., Woodward, J., T-cell suppression by red blood cells is dependent on intact cells and is a consequence of blood bank processing. Transfusion 54 (2014), 1340–1347.
125. Bordin, J.O., Bardossy, L., Blajchman, M.A., Growth enhancement of established tumors by allogeneic blood transfusion in experimental animals and its amelioration by leukodepletion: the importance of the timing of the leukodepletion. Blood 84 (1994), 344–348.
126. Atzil, S., Arad, M., Glasner, A., Abiri, N., Avraham, R., Greenfeld, K., et al. Blood transfusion promotes cancer progression: a critical role for aged erythrocytes. Anesthesiology 109 (2008), 989–997.
127. Mandal, D., Mazumder, A., Das, P., Kundu, M., Basu, J., Fas-, caspase 8-, and caspase 3-dependent signaling regulates the activity of the aminophospholipid translocase and phosphatidylserine externalization in human erythrocytes. J Biol Chem 280 (2005), 39460–39467.
128. Antonelou, M.H., Kriebardis, A.G., Stamoulis, K.E., Economou-Petersen, E., Margaritis, L.H., Papassideri, I.S., Red blood cell aging markers during storage in citrate-phosphate-dextrose-saline-adenine-glucose-mannitol. Transfusion 50 (2010), 376–389.
129. Kriebardis, A.G., Antonelou, M.H., Stamoulis, K.E., Economou-Petersen, E., Margaritis, L.H., Papassideri, I.S., Storage-dependent remodeling of the red blood cell membrane is associated with increased immunoglobulin G binding, lipid raft rearrangement, and caspase activation. Transfusion 47 (2007), 1212–1220.
130. Kriebardis, A.G., Antonelou, M.H., Stamoulis, K.E., Economou-Petersen, E., Margaritis, L.H., Papassideri, I.S., RBC-derived vesicles during storage: ultrastructure, protein composition, oxidation, and signaling components. Transfusion 48 (2008), 1943–1953.
131. Dzieciatkowska, M., Silliman, C.C., Moore, E.E., Kelher, M.R., Banerjee, A., Land, K.J., et al. Proteomic analysis of the supernatant of red blood cell units: the effects of storage and leucoreduction. Vox Sang 105 (2013), 210–218.
132. Yu, H., Kortylewski, M., Pardoll, D., Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat Rev Immunol 7 (2007), 41–51.
133. Benson, D.D., Beck, A.W., Burdine, M.S., Brekken, R., Silliman, C.C., Barnett, C.C. Jr., Accumulation of pro-cancer cytokines in the plasma fraction of stored packed red cells. J Gastrointest Surg 16 (2012), 460–468.
134. Barnett, C.C. Jr., Beck, A.W., Holloway, S.E., Kehler, M., Schluterman, M.K., Brekken, R.A., et al. Intravenous delivery of the plasma fraction of stored packed erythrocytes promotes pancreatic cancer growth in immunocompetent mice. Cancer 116 (2010), 3862–3874.
135. Patel, M.B., Proctor, K.G., Majetschak, M., Extracellular ubiquitin increases in packed red blood cell units during storage. J Surg Res 135 (2006), 226–232.
136. Baumgartner, J.M., Nydam, T.L., Clarke, J.H., Banerjee, A., Silliman, C.C., McCarter, M.D., Red blood cell supernatant potentiates LPS-induced proinflammatory cytokine response from peripheral blood mononuclear cells. J Interferon Cytokine Res 29 (2009), 333–338.
137. Arosa, F.A., Pereira, C.F., Fonseca, A.M., Red blood cells as modulators of T cell growth and survival. Curr Pharm Des 10 (2004), 191–201.
138. Bernard, A., Meier, C., Ward, M., Browning, T., Montgomery, A., Kasten, M., et al. Packed red blood cells suppress T-cell proliferation through a process involving cell–cell contact. J Trauma 69 (2010), 320–329.
139. Reid, M.E., Mohandas, N., Red blood cell blood group antigens: structure and function. Semin Hematol 41 (2004), 93–117.
140. Wither, M., Dzieciatkowska, M., Nemkov, T., Strop, P., D'Alessandro, A., Hansen, K.C., Hemoglobin oxidation at functional amino acid residues during routine storage of red blood cells. Transfusion 56 (2016), 421–426.
141. de Wolski, K., Fu, X., Dumont, L.J., Roback, J.D., Waterman, H., Odem-Davis, K., et al. Metabolic pathways that correlate with post-transfusion circulation of stored murine red blood cells. Haematologica, 2016.
142. Luten, M., Roerdinkholder-Stoelwinder, B., Schaap, N.P., de Grip, W.J., Bos, H.J., Bosman, G.J., Survival of red blood cells after transfusion: a comparison between red cells concentrates of different storage periods. Transfusion 48 (2008), 1478–1485.
143. Hogman, C.F., Meryman, H.T., Storage parameters affecting red blood cell survival and function after transfusion. Transfus Med Rev 13 (1999), 275–296.
144. Wojczyk, B.S., Kim, N., Bandyopadhyay, S., Francis, R.O., Zimring, J.C., Hod, E.A., et al. Macrophages clear refrigerator storage-damaged red blood cells and subsequently secrete cytokines in vivo, but not in vitro, in a murine model. Transfusion 54 (2014), 3186–3197.
145. Cholette, J.M., Henrichs, K.F., Alfieris, G.M., Powers, K.S., Phipps, R., Spinelli, S.L., et al. Washing red blood cells and platelets transfused in cardiac surgery reduces postoperative inflammation and number of transfusions: results of a prospective, randomized, controlled clinical trial. Pediatr Crit Care Med 13 (2012), 290–299.
146. Hod, E.A., Brittenham, G.M., Billote, G.B., Francis, R.O., Ginzburg, Y.Z., Hendrickson, J.E., et al. Transfusion of human volunteers with older, stored red blood cells produces extravascular hemolysis and circulating non-transferrin-bound iron. Blood 118 (2011), 6675–6682.
147. Brittenden, J., Heys, S.D., Ross, J., Eremin, O., Natural killer cells and cancer. Cancer 77 (1996), 1226–1243.
148. Yakar, I., Melamed, R., Shakhar, G., Shakhar, K., Rosenne, E., Abudarham, N., et al. Prostaglandin e(2) suppresses NK activity in vivo and promotes postoperative tumor metastasis in rats. Ann Surg Oncol 10 (2003), 469–479.
149. Blumberg, N., Heal, J.M., Effects of transfusion on immune function. Cancer recurrence and infection. Arch Pathol Lab Med 118 (1994), 371–379.
150. Kim, P.S., Iyer, R.K., Lu, K.V., Yu, H., Karimi, A., Kern, R.M., et al. Expression of the liver form of arginase in erythrocytes. Mol Genet Metab 76 (2002), 100–110.
151. D'Alessandro, A., Dzieciatkowska, M., Nemkov, T., Hansen, K.C., Red blood cell proteomics update: is there more to discover?. Blood Transfus 15 (2017), 182–187.
152. Popovic, P.J., Zeh, H.J. 3rd, Ochoa, J.B., Arginine and immunity. J Nutr 137 (2007), 1681S–1686S.
153. Bernard, A., Kasten, M., Meier, C., Manning, E., Freeman, S., Adams, W., et al. Red blood cell arginase suppresses Jurkat (T cell) proliferation by depleting arginine. Surgery 143 (2008), 286–291.
154. Bronte, V., Zanovello, P., Regulation of immune responses by L-arginine metabolism. Nat Rev Immunol 5 (2005), 641–654.
155. Rodriguez, P.C., Quiceno, D.G., Zabaleta, J., Ortiz, B., Zea, A.H., Piazuelo, M.B., et al. Arginase I production in the tumor microenvironment by mature myeloid cells inhibits T-cell receptor expression and antigen-specific T-cell responses. Cancer Res 64 (2004), 5839–5849.
156. Procter, L.D., Meier, C.F., Hamilton, C., Gerughty, A.R., Overall, P., Santapuram, P., et al. y+ cationic amino acid transport of arginine in packed red blood cells. J Surg Res 179 (2013), e183–e187.
157. Mollinedo, F., Palomero-Rodriguez, M.A., Sanchez-Conde, P., Garcia-Navas, R., Laporta-Baez, Y., de Vicente-Sanchez, J., et al. Arginase as a new concern in blood transfusion. Blood Transfus 12:Suppl. 1 (2014), s165–s166.
158. Bernard, A., Meier, C., Lopez, N., May, J., Chang, P., Boulanger, B., et al. Packed red blood cell-associated arginine depletion is mediated by arginase. J Trauma 63 (2007), 1108–1112 [discussion 12].
159. Palomero-Rodriguez, M.A., Laporta-Baez, Y., Sanchez-Conde, M.P., Mollinedo, F., Inflammatory response, immunosuppression, and cancer recurrence after perioperative blood transfusion. Br J Anaesth 112 (2014), 576–577.
160. Munder, M., Mollinedo, F., Calafat, J., Canchado, J., Gil-Lamaignere, C., Fuentes, J.M., et al. Arginase I is constitutively expressed in human granulocytes and participates in fungicidal activity. Blood 105 (2005), 2549–2556.
161. Tissot, J.D., Rubin, O., Canellini, G., Analysis and clinical relevance of microparticles from red blood cells. Curr Opin Hematol 17 (2010), 571–577.
162. Kriebardis, A., Antonelou, M., Stamoulis, K., Papassideri, I., Cell-derived microparticles in stored blood products: innocent-bystanders or effective mediators of post-transfusion reactions?. Blood Transfus 10:Suppl. 2 (2012), s25–s38.
163. Straat, M., van Hezel, M.E., Boing, A., Tuip-De Boer, A., Weber, N., Nieuwland, R., et al. Monocyte-mediated activation of endothelial cells occurs only after binding to extracellular vesicles from red blood cell products, a process mediated by beta-integrin. Transfusion 56 (2016), 3012–3020.
164. Straat, M., Boing, A.N., Tuip-De Boer, A., Nieuwland, R., Juffermans, N.P., Extracellular vesicles from red blood cell products induce a strong pro-inflammatory host response, dependent on both numbers and storage duration. Transfus Med Hemother 43 (2016), 302–305.
165. Zecher, D., Cumpelik, A., Schifferli, J.A., Erythrocyte-derived microvesicles amplify systemic inflammation by thrombin-dependent activation of complement. Arterioscler Thromb Vasc Biol 34 (2014), 313–320.
166. van Doormaal, F.F., Kleinjan, A., Di Nisio, M., Buller, H.R., Nieuwland, R., Cell-derived microvesicles and cancer. Neth J Med 67 (2009), 266–273.
167. Falanga, A., Russo, L., Milesi, V., The coagulopathy of cancer. Curr Opin Hematol 21 (2014), 423–429.
168. Lichtenberger, L.M., Fang, D., Bick, R.J., Poindexter, B.J., Phan, T., Bergeron, A.L., et al. Unlocking aspirin's chemopreventive activity: role of irreversibly inhibiting platelet cyclooxygenase-1. Cancer Prev Res (Phila) 10 (2017), 142–152.
169. Janowska-Wieczorek, A., Marquez-Curtis, L.A., Wysoczynski, M., Ratajczak, M.Z., Enhancing effect of platelet-derived microvesicles on the invasive potential of breast cancer cells. Transfusion 46 (2006), 1199–1209.
170. Janowska-Wieczorek, A., Wysoczynski, M., Kijowski, J., Marquez-Curtis, L., Machalinski, B., Ratajczak, J., et al. Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int J Cancer 113 (2005), 752–760.
171. Berezina, T.L., Zaets, S.B., Morgan, C., Spillert, C.R., Kamiyama, M., Spolarics, Z., et al. Influence of storage on red blood cell rheological properties. J Surg Res 102 (2002), 6–12.
172. Garnier, D., Milsom, C., Magnus, N., Meehan, B., Weitz, J., Yu, J., et al. Role of the tissue factor pathway in the biology of tumor initiating cells. Thromb Res 125:Suppl. 2 (2010), S44–S50.
173. Geddings, J.E., Hisada, Y., Boulaftali, Y., Getz, T.M., Whelihan, M., Fuentes, R., et al. Tissue factor-positive tumor microvesicles activate platelets and enhance thrombosis in mice. J Thromb Haemost 14 (2016), 153–166.
174. Magnus, N., Garnier, D., Meehan, B., McGraw, S., Lee, T.H., Caron, M., et al. Tissue factor expression provokes escape from tumor dormancy and leads to genomic alterations. Proc Natl Acad Sci U S A 111 (2014), 3544–3549.
175. Amirkhosravi, A., Meyer, T., Sackel, D., Desai, H., Biddinger, R., Amaya, M., et al. Platelet microparticles upregulate TF and VEGF in endothelial and melanoma cells in a CD40 ligand-dependent manner: possible role in angiogenesis and metastasis. Blood, 100(11 Prt II), 2002 63b. Ab 3721.
176. Aleshnick, M., Foley, J.H., Keating, F.K., Butenas, S., Procoagulant activity in stored units of red blood cells. Biochem Biophys Res Commun 474 (2016), 680–685.
177. 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 51 (2011), 1086–1095.
178. Gao, Y., Lv, L., Liu, S., Ma, G., Su, Y., Elevated levels of thrombin-generating microparticles in stored red blood cells. Vox Sang 105 (2013), 11–17.
179. Lima, L.G., Chammas, R., Monteiro, R.Q., Moreira, M.E., Barcinski, M.A., Tumor-derived microvesicles modulate the establishment of metastatic melanoma in a phosphatidylserine-dependent manner. Cancer Lett 283 (2009), 168–175.
180. Al-Nedawi, K., Meehan, B., Kerbel, R.S., Allison, A.C., Rak, J., Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci U S A 106 (2009), 3794–3799.
181. Huang, X., Bennett, M., Thorpe, P.E., A monoclonal antibody that binds anionic phospholipids on tumor blood vessels enhances the antitumor effect of docetaxel on human breast tumors in mice. Cancer Res 65 (2005), 4408–4416.
182. Al-Nedawi, K., Meehan, B., Micallef, J., Lhotak, V., May, L., Guha, A., et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol 10 (2008), 619–624.
183. Estep, T.N., Pedersen, R.A., Miller, T.J., Stupar, K.R., Characterization of erythrocyte quality during the refrigerated storage of whole blood containing di-(2-ethylhexyl) phthalate. Blood 64 (1984), 1270–1276.
184. AuBuchon, J.P., Estep, T.N., Davey, R.J., The effect of the plasticizer di-2-ethylhexyl phthalate on the survival of stored RBCs. Blood 71 (1988), 448–452.
185. Takeshita, A., Inagaki, K., Igarashi-Migitaka, J., Ozawa, Y., Koibuchi, N., The endocrine disrupting chemical, diethylhexyl phthalate, activates MDR1 gene expression in human colon cancer LS174T cells. J Endocrinol 190 (2006), 897–902.
186. Hurst, C.H., Waxman, D.J., Activation of PPARalpha and PPARgamma by environmental phthalate monoesters. Toxicol Sci 74 (2003), 297–308.
187. Inoue, K., Kawaguchi, M., Yamanaka, R., Higuchi, T., Ito, R., Saito, K., et al. Evaluation and analysis of exposure levels of di(2-ethylhexyl) phthalate from blood bags. Clin Chim Acta 358 (2005), 159–166.
188. Rael, L.T., Bar-Or, R., Ambruso, D.R., Mains, C.W., Slone, D.S., Craun, M.L., et al. Phthalate esters used as plasticizers in packed red blood cell storage bags may lead to progressive toxin exposure and the release of pro-inflammatory cytokines. Oxid Med Cell Longev 2 (2009), 166–171.
189. Cancelas, J.A., Rugg, N., Nestheide, S., Hill, S.E., Emanuele, R.M., McKenzie, D.S., The purified vepoloxamer prevents haemolysis in 42-day stored, DEHP/PVC-free red blood cell units. Blood Transfus 15 (2017), 165–171.
190. Blumberg, N., Deleterious clinical effects of transfusion immunomodulation: proven beyond a reasonable doubt. Transfusion 45 (2005), 33S–39S [discussion 9S-40S].
191. Vamvakas, E.C., Blajchman, M.A., Transfusion-related immunomodulation (TRIM): an update. Blood Rev 21 (2007), 327–348.
192. Kristiansson, M., Soop, M., Saraste, L., Sundqvist, K.G., Post-operative circulating cytokine patterns – the influence of infection. Intensive Care Med 19 (1993), 395–400.
193. Stark, M.J., Keir, A.K., Andersen, C.C., Does non-transferrin bound iron contribute to transfusion related immune-modulation in preterms?. Arch Dis Child Fetal Neonatal Ed 98 (2013), F424–F429.
194. Keir, A.K., McPhee, A.J., Andersen, C.C., Stark, M.J., Plasma cytokines and markers of endothelial activation increase after packed red blood cell transfusion in the preterm infant. Pediatr Res 73 (2013), 75–79.
195. Miki, C., Hiro, J., Ojima, E., Inoue, Y., Mohri, Y., Kusunoki, M., Perioperative allogeneic blood transfusion, the related cytokine response and long-term survival after potentially curative resection of colorectal cancer. Clin Oncol (R Coll Radiol) 18 (2006), 60–66.
196. Grimshaw, K., Sahler, J., Spinelli, S.L., Phipps, R.P., Blumberg, N., New frontiers in transfusion biology: identification and significance of mediators of morbidity and mortality in stored red blood cells. Transfusion 51 (2011), 874–880.
197. Jensen, L.S., Kissmeyer-Nielsen, P., Wolff, B., Qvist, N., Randomised comparison of leucocyte-depleted versus buffy-coat-poor blood transfusion and complications after colorectal surgery. Lancet 348 (1996), 841–845.
198. Houbiers, J.G., Brand, A., van de Watering, L.M., Hermans, J., Verwey, P.J., Bijnen, A.B., et al. Randomised controlled trial comparing transfusion of leucocyte-depleted or buffy-coat-depleted blood in surgery for colorectal cancer. Lancet 344 (1994), 573–578.
199. Radwanski, K., Garraud, O., Cognasse, F., Hamzeh-Cognasse, H., Payrat, J.M., Min, K., The effects of red blood cell preparation method on in vitro markers of red blood cell aging and inflammatory response. Transfusion 53 (2013), 3128–3138.
200. Chasse, M., McIntyre, L., Tinmouth, A., Acker, J., English, S.W., Knoll, G., et al. Clinical effects of blood donor characteristics in transfusion recipients: protocol of a framework to study the blood donor–recipient continuum. BMJ Open, 5, 2015, e007412.
201. Whitney, A.R., Diehn, M., Popper, S.J., Alizadeh, A.A., Boldrick, J.C., Relman, D.A., et al. Individuality and variation in gene expression patterns in human blood. Proc Natl Acad Sci U S A 100 (2003), 1896–1901.
202. Silliman, C.C., Voelkel, N.F., Allard, J.D., Elzi, D.J., Tuder, R.M., Johnson, J.L., et al. Plasma and lipids from stored packed red blood cells cause acute lung injury in an animal model. J Clin Invest 101 (1998), 1458–1467.
203. Casagrande, G., Arienti, F., Mazzocchi, A., Taverna, F., Ravagnani, F., Costantino, M., Application of controlled shear stresses on the erythrocyte membrane as a new approach to promote molecule encapsulation. Artif Organs 40 (2016), 959–970.
204. Villa, C.H., Anselmo, A.C., Mitragotri, S., Muzykantov, V., Red blood cells: supercarriers for drugs, biologicals, and nanoparticles and inspiration for advanced delivery systems. Adv Drug Deliv Rev 106 (2016), 88–103.
205. Pishesha, N., Bilate, A.M., Wibowo, M.C., Huang, N.J., Li, Z., Dhesycka, R., et al. Engineered erythrocytes covalently linked to antigenic peptides can protect against autoimmune disease. Proc Natl Acad Sci U S A, 2017.
206. Domenech, C., Thomas, X., Chabaud, S., Baruchel, A., Gueyffier, F., Mazingue, F., et al. L-Asparaginase loaded red blood cells in refractory or relapsing acute lymphoblastic leukaemia in children and adults: results of the GRASPALL 2005-01 randomized trial. Br J Haematol 153 (2011), 58–65.
207. Bachet, J.B., Gay, F., Marechal, R., Galais, M.P., Adenis, A., Ms, C.D., et al. Asparagine synthetase expression and phase I study with L-asparaginase encapsulated in red blood cells in patients with pancreatic adenocarcinoma. Pancreas 44 (2015), 1141–1147.
208. Rodriguez, P.L., Harada, T., Christian, D.A., Pantano, D.A., Tsai, R.K., Discher, D.E., Minimal “Self” peptides that inhibit phagocytic clearance and enhance delivery of nanoparticles. Science 339 (2013), 971–975.
209. Luk, B.T., Fang, R.H., Hu, C.M., Copp, J.A., Thamphiwatana, S., Dehaini, D., et al. Safe and immunocompatible nanocarriers cloaked in RBC membranes for drug delivery to treat solid tumors. Theranostics 6 (2016), 1004–1011.
210. van Dommelen, S.M., Vader, P., Lakhal, S., Kooijmans, S.A., van Solinge, W.W., Wood, M.J., et al. Microvesicles and exosomes: opportunities for cell-derived membrane vesicles in drug delivery. J Control Release 161 (2012), 635–644.
211. Villa, C.H., Seghatchian, J., Muzykantov, V., Drug delivery by erythrocytes: “Primum non nocere”. Transfus Apher Sci 55 (2016), 275–280.
212. Kim-Shapiro, D.B., Lee, J., Gladwin, M.T., Storage lesion: role of red blood cell breakdown. Transfusion 51 (2011), 844–851.
213. Burger, P., Kostova, E., Bloem, E., Hilarius-Stokman, P., Meijer, A.B., van den Berg, T.K., et al. Potassium leakage primes stored erythrocytes for phosphatidylserine exposure and shedding of pro-coagulant vesicles. Br J Haematol 160 (2013), 377–386.
214. Bosman, G.J., Survival of red blood cells after transfusion: processes and consequences. Front Physiol, 4, 2013, 376.
215. Glynn, S.A., Klein, H.G., Ness, P.M., The red blood cell storage lesion: the end of the beginning. Transfusion 56 (2016), 1462–1468.
216. Vamvakas, E.C., Allogeneic blood transfusion and cancer recurrence: 20 years later. Transfusion 54 (2014), 2149–2153.
217. Muszynski, J.A., Spinella, P.C., Cholette, J.M., Acker, J.P., Hall, M.W., Juffermans, N.P., et al. Transfusion-related immunomodulation: review of the literature and implications for pediatric critical illness. Transfusion 57 (2017), 195–206.
218. Tzounakas, V.L., Kriebardis, A.G., Seghatchian, J., Papassideri, I.S., Antonelou, M.H., Unraveling the Gordian knot: red blood cell storage lesion and transfusion outcomes. Blood Transfus 15 (2017), 126–130.