The pathophysiology and consequences of red blood cell storage

Anaesthesia

Volumn 70, Issue S1, 2015, Pages

  Orlov, D ^a   Karkouti, K ^a  

^a TORONTO GENERAL HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD STORAGE; CELL SURVIVAL; ERYTHROCYTE; ERYTHROCYTE MEMBRANE; ERYTHROCYTE TRANSFUSION; HUMAN; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY;

BLOOD PRESERVATION; CELL SURVIVAL; ERYTHROCYTE MEMBRANE; ERYTHROCYTE TRANSFUSION; ERYTHROCYTES; HUMANS; OXIDATIVE STRESS;

EID: 84925224639     PISSN: 00032409     EISSN: 13652044     Source Type: Journal    
DOI: 10.1111/ANAE.12891     Document Type: Review

References (135)

1. Flegel WA, Natanson C, Klein HG. Does prolonged storage of red blood cells cause harm? British Journal of Haematology 2014; 165: 3–16.
2. Hardwick J. Blood storage and transportation. ISBT Science Series 2014; 3: 177–96.
3. Hess JR. Scientific problems in the regulation of red blood cell products. Transfusion 2012; 52: 1827–35.
4. Hess JR, Sparrow RL, van der Meer PF, Acker JP, Cardigan RA, Devine DV. Red blood cell hemolysis during blood bank storage: using national quality management data to answer basic scientific questions. Transfusion 2009; 49: 2599–603.
5. Ross JF, Finch CA, Peacock WC, Sammons ME. The in vitro preservation and post-transfusion survival of stored blood. Journal of Clinical Investigation 1947; 26: 687–703.
6. Ness PM. Does transfusion of stored red blood cells cause clinically important adverse effects? A critical question in search of an answer and a plan. Transfusion 2011; 51: 666– 7.
7. Hogman CF, Meryman HT. Storage parameters affecting red blood cell survival and function after transfusion. Transfusion Medicine Reviews 1999; 13: 275–96.
8. Greer P. Wintrobe’s Clinical Hematology, 13th edn. Philadel-phia, PA: Lippincott Williams & Wilkins Publishers, 2014.
9. Yoshida T, Shevkoplyas SS. Anaerobic storage of red blood cells. Blood Transfusion 2010; 8: 220–36.
10. Hess JR. Measures of stored red blood cell quality. Vox San-guinis 2014; 107: 1–9.
11. Ruddell JP, Lippert LE, Babcock JG, Hess JR. Effect of 24-hour storage at 25 degrees C on the in vitro storage characteris-tics of CPDA-1 packed red cells. Transfusion 1998; 38: 424– 8.
12. Graubarth H, Mackler B, Guest GM. Effects of acidosis on uti-lization of glucose in erythrocytes and leucocytes. American Journal of Physiology 1953; 172: 301–8.
13. Flatt JF, Bawazir WM, Bruce LJ. The involvement of cation leaks in the storage lesion of red blood cells. Frontiers in Physiology 2014; 5: 214.
14. Tinmouth A, Fergusson D, Yee IC, Hebert PC. Clinical consequences of red cell storage in the critically ill. Transfusion 2006; 46: 2014–27.
15. Bennett-Guerrero E, Veldman TH, Doctor A, et al. Evolution of adverse changes in stored RBCs. Proceedings of the National Academy of Sciences USA 2007; 104: 17063–8.
16. Minetti G, Ciana A, Profumo A, et al. Cell age-related mono-valent cations content and density changes in stored human erythrocytes. Biochimica et Biophysica Acta 2001; 1527: 149–55.
17. Luten M, Roerdinkholder-Stoelwinder B, Schaap NP, de Grip WJ, Bos HJ, Bosman GJ. Survival of red blood cells after transfusion: a comparison between red cells concentrates of different storage periods. Transfusion 2008; 48: 1478– 85.
18. D’Alessandro A, D’Amici GM, Vaglio S, Zolla L. Time-course investigation of SAGM-stored leukocyte-filtered red bood cell concentrates: from metabolism to proteomics. Haema-tologica 2012; 97: 107–15.
19. Almizraq R, Tchir JD, Holovati JL, Acker JP. Storage of red blood cells affects membrane composition, microvesicula-tion, and in vitro quality. Transfusion 2013; 53: 2258–67.
20. Karon BS, van Buskirk CM, Jaben EA, Hoyer JD, Thomas DD. Temporal sequence of major biochemical events during blood bank storage of packed red blood cells. Blood Transfusion 2012; 10: 453–61.
21. Salzer U, Zhu R, Luten M, et al. Vesicles generated during storage of red cells are rich in the lipid raft marker stoma-tin. Transfusion 2008; 48: 451–62.
22. Almac E, Ince C. The impact of storage on red cell function in blood transfusion. Best Practice & Research Clinical Ana-esthesiology 2007; 21: 195–208.
23. Karger R, Lukow C, Kretschmer V. Deformability of red blood cells and correlation with ATP content during storage as leukocyte-depleted whole blood. Transfusion Medicine and Hemotherapy 2012; 39: 277–82.
24. Umbreit J. Methemoglobin – it’s not just blue: a concise review. American Journal of Hematology 2007; 82: 134–44.
25. Hentschel WM, Wu LL, Tobin GO, et al. Erythrocyte cation transport activities as a function of cell age. Clinica Chimica Acta 1986; 157: 33–43.
26. Lutz HU, Bogdanova A. Mechanisms tagging senescent red blood cells for clearance in healthy humans. Fronteries in Physiology 2013; 4: 387.
27. Kanias T, Acker JP. Biopreservation of red blood cells – the struggle with hemoglobin oxidation. FEBS Journal 2010; 277: 343–56.
28. Buehler PW, Karnaukhova E, Gelderman MP, Alayash AI. Blood aging, safety, and transfusion: capturing the ‘‘radical’’ menace. Antioxidants & Redox Signaling 2011; 14: 1713–28.
29. Garcia-Santos D, Schranzhofer M, Horvathova M, et al. Heme oxygenase 1 is expressed in murine erythroid cells where it controls the level of regulatory heme. Blood 2014; 123: 2269–77.
30. Hess JR. Red cell storage. Journal of Proteomics 2010; 73: 368–73.
31. Reeder BJ. The redox activity of hemoglobins: from physio-logic functions to pathologic mechanisms. Antioxidants & Redox Signaling 2010; 13: 1087–123.
32. Raval JS, Fontes J, Banerjee U, Yazer MH, Mank E, Palmer AF. Ascorbic acid improves membrane fragility and decreases haemolysis during red blood cell storage. Transfusion Medicine 2013; 23: 87–93.
33. Balagopalakrishna C, Manoharan PT, Abugo OO, Rifkind JM. Production of superoxide from hemoglobin-bound oxygen under hypoxic conditions. Biochemistry 1996; 35: 6393–8.
34. Jozwik M, Jozwik M, Jozwik M, Szczypka M, Gajewska J, Laskowska-Klita T. Antioxidant defence of red blood cells and plasma in stored human blood. Clinica Chimica Acta 1997; 267: 129–42.
35. Collard K, White D, Copplestone A. The influence of storage age on iron status, oxidative stress and antioxidant protection in paediatric packed cell units. Blood Transfusion 2014; 12: 210–9.
36. Mohanty JG, Nagababu E, Rifkind JM. Red blood cell oxida-tive stress impairs oxygen delivery and induces red blood cell aging. Frontiers in Physiology 2014; 5: 84.
37. Kriebardis AG, Antonelou MH, Stamoulis KE, Economou-Pet-ersen E, Margaritis LH, Papassideri IS. Progressive oxidation of cytoskeletal proteins and accumulation of denatured hemoglobin in stored red cells. Journal of Cellular and Molecular Medicine 2007; 11: 148–55.
38. Antonelou MH, Kriebardis AG, Papassideri IS. Aging and death signalling in mature red cells: from basic science to transfusion practice. Blood Transfusion 2010; 8(Suppl 3): s39–47.
39. Cardo LJ, Hmel P, Wilder D. Stored packed red blood cells contain a procoagulant phospholipid reducible by leukode-pletion filters and washing. Transfusion and Apheresis Science 2008; 38: 141–7.
40. Berezina TL, Zaets SB, Morgan C, et al. Influence of storage on red blood cell rheological properties. Journal of Surgical Research 2002; 102: 6–12.
41. Bosman GJ, Werre JM, Willekens FL, Novotny VM. Erythrocyte ageing in vivo and in vitro: structural aspects and implications for transfusion. Transfusion Medicine 2008; 18: 335–47.
42. Frank SM, Abazyan B, Ono M, et al. Decreased erythrocyte deformability after transfusion and the effects of erythrocyte storage duration. Anesthesia and Analgesia 2013; 116: 975–81.
43. Greenwalt TJ, McGuinness CG, Dumaswala UJ. Studies in red blood cell preservation: 4. Plasma vesicle hemoglobin exceeds free hemoglobin. Vox Sanguinis 1991; 61: 14–7.
44. Kriebardis AG, Antonelou MH, Stamoulis KE, Economou-Petersen E, Margaritis LH, Papassideri IS. RBC-derived vesicles during storage: ultrastructure, protein composition, oxi-dation, and signaling components. Transfusion 2008; 48: 1943–53.
45. Rubin O, Crettaz D, Canellini G, Tissot JD, Lion N. Microparti-cles in stored red blood cells: an approach using flow cytom-etry and proteomic tools. Vox Sanguinis 2008; 95: 288–97.
46. Gao Y, Lv L, Liu S, Ma G, Su Y. Elevated levels of thrombin-generating microparticles in stored red blood cells. Vox San-guinis 2013; 105: 11–7.
47. Rubin O, Delobel J, Prudent M, et al. Red blood cell-derived microparticles isolated from blood units initiate and propa-gate thrombin generation. Transfusion 2013; 53: 1744–54.
48. Gladwin MT, Kim-Shapiro DB. Storage lesion in banked blood due to hemolysis-dependent disruption of nitric oxide homeostasis. Current Opinion in Hematology 2009; 16: 515–23.
49. Donadee C, Raat NJ, 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: 465–76.
50. Liu C, Liu X, Janes J, et al. Mechanism of faster NO scavenging by older stored red blood cells. Redox Biology 2014; 2: 211–9.
51. Liu C, Zhao W, Christ GJ, Gladwin MT, Kim-Shapiro DB. Nitric oxide scavenging by red cell microparticles. Free Radical Biology and Medicine 2013; 65: 1164–73.
52. Minneci PC, Deans KJ, Zhi H, et al. Hemolysis-associated endothelial dysfunction mediated by accelerated NO inacti-vation by decompartmentalized oxyhemoglobin. Journal of Clinical Investigation 2005; 115: 3409–17.
53. Bosman GJ. Survival of red blood cells after transfusion: processes and consequences. Frontiers in Physiology 2013; 4: 376.
54. Ozment CP, Mamo LB, Campbell ML, Lokhnygina Y, Ghio AJ, Turi JL. Transfusion-related biologic effects and free hemo-globin, heme, and iron. Transfusion 2013; 53: 732–40.
55. Vermeulen Windsant IC, de Wit NC, Sertorio JT, et al. Blood transfusions increase circulating plasma free hemoglobin levels and plasma nitric oxide consumption: a prospective observational pilot study. Critical Care 2012; 16: R95.
56. Uchida I, Tashiro C, Koo YH, Mashimo T, Yoshiya I. Carbo-xyhemoglobin and methemoglobin levels in banked blood. Journal of Clinical Anesthesia 1990; 2: 86–90.
57. Marwah SS, Blann A, Harrison P, et al. Increased non-trans-ferrin bound iron in plasma-depleted SAG-M red blood cell units. Vox Sanguinis 2002; 82: 122–6.
58. Ebaugh G Jr, Emerson CP, Ross JF. The use of radioactive chromium 51 as an erythrocyte tagging agent for the deter-mination or red cell survival in vivo. Journal of Clinical Investigation 1953; 32: 1260–76.
59. Buehler PW, Abraham B, Vallelian F, et al. Haptoglobin pre-serves the CD163 hemoglobin scavenger pathway by shielding hemoglobin from peroxidative modification. Blood 2009; 113: 2578–86.
60. Thomsen JH, Etzerodt A, Svendsen P, Moestrup SK. The hap-toglobin-CD163-heme oxygenase-1 pathway for hemoglobin scavenging. Oxidative Medicine and Cellular Longevity 2013; 2013: 523652.
61. Rother RP, Bell L, Hillmen P, Gladwin MT. The clinical sequelae of intravascular hemolysis and extracellular plasma hemoglobin: a novel mechanism of human dis-ease. Journal of the American Medical Association 2005; 293: 1653–62.
62. Schaer DJ, Buehler PW, Alayash AI, Belcher JD, Vercellotti GM. Hemolysis and free hemoglobin revisited: exploring hemoglobin and hemin scavengers as a novel class of ther-apeutic proteins. Blood 2013; 121: 1276–84.
63. Wagener FA, Eggert A, Boerman OC, et al. Heme is a potent inducer of inflammation in mice and is counteracted by heme oxygenase. Blood 2001; 98: 1802–11.
64. Graca-Souza AV, Arruda MA, de Freitas MS, Barja-Fidalgo C, Oliveira PL. Neutrophil activation by heme: implications for inflammatory processes. Blood 2002; 99: 4160–5.
65. Sassa S. Why heme needs to be degraded to iron, biliverdin IXalpha, and carbon monoxide? Antioxidants & Redox Signaling 2004; 6: 819–24.
66. Nemeth E, Ganz T. Regulation of iron metabolism by hepci-din. Annual Review of Nutrition 2006; 26: 323–42.
67. Hod EA, Brittenham GM, Billote GB, et al. Transfusion of human volunteers with older, stored red blood cells produces extravascular hemolysis and circulating non-transfer-rin-bound iron. Blood 2011; 118: 6675–82.
68. Stapley R, Owusu BY, Brandon A, et al. Erythrocyte storage increases rates of NO and nitrite scavenging: implications for transfusion-related toxicity. The Biochemical Journal 2012; 446: 499–508.
69. Baek JH, D’Agnillo F, Vallelian F, et al. Hemoglobin-driven pathophysiology is an in vivo consequence of the red blood cell storage lesion that can be attenuated in guinea pigs by haptoglobin therapy. Journal of Clinical Investigation 2012; 122: 1444–58.
70. Wojczyk BS, Kim N, Bandyopadhyay S, et al. Macrophages clear refrigerator storage-damaged red blood cells and sub-sequently secrete cytokines in vivo, but not in vitro, in a murine model. Transfusion 2014 Jul 20. doi 10.1111/trf. 12755.
71. Ozment CP, Turi JL. Iron overload following red blood cell transfusion and its impact on disease severity. Biochimica et Biophysica Acta 2009; 1790: 694–701.
72. Hod EA, Zhang N, Sokol SA, et al. Transfusion of red blood cells after prolonged storage produces harmful effects that are mediated by iron and inflammation. Blood 2010; 115: 4284–92.
73. Roback JD. Vascular effects of the red blood cell storage lesion. Hematology American Society of Hematology Education Program 2011; 2011: 475–9.
74. Karkouti K. Transfusion and risk of acute kidney injury in cardiac surgery. British Journal of Anaesthesia 2012; 109 (Suppl 1): i29–38.
75. Karkouti K, Wijeysundera DN, Yau TM, et al. Advance tar-geted transfusion in anemic cardiac surgical patients for kidney protection: an unblinded randomized pilot clinical trial. Anesthesiology 2012; 116: 613–21.
76. Baron DM, Yu B, Lei C, et al. Pulmonary hypertension in lambs transfused with stored blood is prevented by breath-ing nitric oxide. Anesthesiology 2012; 116: 637–47.
77. Brown CH, Grega M, Selnes OA, et al. Length of red cell unit storage and risk for delirium after cardiac surgery. Anesthesia and Analgesia 2014; 119: 242–50.
78. Yazdanbakhsh K, Bao W, Zhong H. Immunoregulatory effects of stored red blood cells. Hematology American Society of Hematology Education Program 2011; 2011: 466–9.
79. Hod EA, Spitalnik SL. Stored red blood cell transfusions: iron, inflammation, immunity, and infection. Transfusion Clinique et Biologique 2012; 19: 84–9.
80. Berra L, Coppadoro A, Yu B, et al. Transfusion of stored autologous blood does not alter reactive hyperemia index in healthy volunteers. Anesthesiology 2012; 117: 56–63.
81. Weiskopf RB, Feiner J, Hopf H, et al. Fresh blood and aged stored blood are equally efficacious in immediately reversing anemia-induced brain oxygenation deficits in humans. Anesthesiology 2006; 104: 911–20.
82. Weiskopf RB, Feiner J, Toy P, et al. Fresh and stored red blood cell transfusion equivalently induce subclinical pulmonary gas exchange deficit in normal humans. Anesthesia and Analgesia 2012; 114: 511–9.
83. Edgren G, Kamper-Jorgensen M, Eloranta S, et al. Duration of red blood cell storage and survival of transfused patients. Transfusion 2010; 50: 1185–95.
84. Eikelboom JW, Cook RJ, Liu Y, Heddle NM. Duration of red cell storage before transfusion and in-hospital mortality. American Heart Journal 2010; 159: 737–43.
85. Gajic O, Rana R, Mendez JL, et al. Acute lung injury after blood transfusion in mechanically ventilated patients. Transfusion 2004; 44: 1468–74.
86. Gajic O, Rana R, Winters JL, et al. Transfusion-related acute lung injury in the critically ill: prospective nested case-con-trol study. American Journal of Respiratory and Critical Care Medicine 2007; 176: 886–91.
87. Gauvin F, Spinella PC, Lacroix J, et al. Association between length of storage of transfused red blood cells and multiple organ dysfunction syndrome in pediatric intensive care patients. Transfusion 2010; 50: 1902–13.
88. Juffermans NP, Vlaar AP, Prins DJ, Goslings JC, Binnekade JM. The age of red blood cells is associated with bacterial infections in critically ill trauma patients. Blood Transfusion 2012; 10: 290–5.
89. Keller ME, Jean R, LaMorte WW, Millham F, Hirsch E. Effects of age of transfused blood on length of stay in trauma patients: a preliminary report. The Journal of Trauma 2002; 53: 1023–5.
90. Koch CG, Li L, Sessler DI, et al. Duration of red-cell storage and complications after cardiac surgery. New England Journal of Medicine 2008; 358: 1229–39.
91. Leal-Noval SR, Jara-Lopez I, Garcia-Garmendia JL, et al. Influence of erythrocyte concentrate storage time on postsurgi-cal morbidity in cardiac surgery patients. Anesthesiology 2003; 98: 815–22.
92. Leal-Noval SR, Munoz-Gomez M, Arellano-Orden V, et al. Impact of age of transfused blood on cerebral oxygenation in male patients with severe traumatic brain injury. Critical Care Medicine 2008; 36: 1290–6.
93. McKenny M, Ryan T, Tate H, Graham B, Young VK, Dowd N. Age of transfused blood is not associated with increased postoperative adverse outcome after cardiac surgery. British Journal of Anaesthesia 2011; 106: 643–9.
94. Murrell Z, Haukoos JS, Putnam B, Klein SR. The effect of older blood on mortality, need for ICU care, and the length of ICU stay after major trauma. The American Surgeon 2005; 71: 781–5.
95. Mynster T, Nielsen HJ. Storage time of transfused blood and disease recurrence after colorectal cancer surgery. Diseases of the Colon and Rectum 2001; 44: 955–64.
96. Offner PJ, Moore EE, Biffl WL, Johnson JL, Silliman CC. Increased rate of infection associated with transfusion of old blood after severe injury. Archives of Surgery 2002; 137: 711–6.
97. Pettila V, Westbrook AJ, Nichol AD, et al. Age of red blood cells and mortality in the critically ill. Critical Care 2011; 15: R116.
98. Phelan HA, Eastman AL, Aldy K, et al. Prestorage leukoreduc-tion abrogates the detrimental effect of aging on packed red cells transfused after trauma: a prospective cohort study. American Journal of Surgery 2012; 203: 198–204.
99. Purdy FR, Tweeddale MG, Merrick PM. Association of mortality with age of blood transfused in septic ICU patients. Canadian Journal of Anaesthesia 1997; 44: 1256–61.
100. Robinson SD, Janssen C, Fretz EB, et al. Red blood cell storage duration and mortality in patients undergoing percuta-neous coronary intervention. American Heart Journal 2010; 159: 876–81.
101. Saager L, Turan A, Dalton JE, Figueroa PI, Sessler DI, Kurz A. Erythrocyte storage duration is not associated with increased mortality in noncardiac surgical patients: a retrospective analysis of 6,994 patients. Anesthesiology 2013; 118: 51–8.
102. Sanders J, Patel S, Cooper J, et al. Red blood cell storage is associated with length of stay and renal complications after cardiac surgery. Transfusion 2011; 51: 2286–94.
103. Spinella PC, Carroll CL, Staff I, et al. Duration of red blood cell storage is associated with increased incidence of deep vein thrombosis and in hospital mortality in patients with traumatic injuries. Critical Care 2009; 13: R151.
104. Taylor RW, O’Brien J, Trottier SJ, et al. Red blood cell transfusions and nosocomial infections in critically ill patients. Critical Care Medicine 2006; 34: 2302–8.
105. Vamvakas EC, Carven JH. Transfusion and postoperative pneumonia in coronary artery bypass graft surgery: effect of the length of storage of transfused red cells. Transfusion 1999; 39: 701–10.
106. Vamvakas EC, Carven JH. Length of storage of transfused red cells and postoperative morbidity in patients undergoing coronary artery bypass graft surgery. Transfusion 2000; 40: 101–9.
107. van de Watering L, Lorinser J, Versteegh M, Westendord R, Brand A. Effects of storage time of red blood cell transfusions on the prognosis of coronary artery bypass graft patients. Transfusion 2006; 46: 1712–8.
108. van Straten AH, Soliman Hamad MA, Martens EJ, et al. Effect of storage time of transfused plasma on early and late mortality after coronary artery bypass grafting. Journal of Thoracic and Cardiovascular Surgery 2011; 141: 238– 43.
109. Vandromme MJ, McGwin G Jr, Marques MB, Kerby JD, Rue LW III, Weinberg JA. Transfusion and pneumonia in the trauma intensive care unit: an examination of the temporal relationship. The Journal of Trauma 2009; 67: 97–101.
110. Weinberg JA, McGwin G Jr, Griffin RL, et al. Age of transfused blood: an independent predictor of mortality despite universal leukoreduction. The Journal of Trauma 2008; 65: 279–82.
111. Weinberg JA, McGwin G Jr, Marques MB, et al. Transfusions in the less severely injured: does age of transfused blood affect outcomes? The Journal of Trauma 2008; 65: 794–8.
112. Weinberg JA, McGwin G Jr, Vandromme MJ, et al. Duration of red cell storage influences mortality after trauma. The Journal of Trauma 2010; 69: 1427–31.
113. Yap CH, Lau L, Krishnaswamy M, Gaskell M, Yii M. Age of transfused red cells and early outcomes after cardiac sur-gery. Annals of Thoracic Surgery 2008; 86: 554–9.
114. Zallen G, Offner PJ, Moore EE, et al. Age of transfused blood is an independent risk factor for postinjury multiple organ failure. American Journal of Surgery 1999; 178: 570–2.
115. Aubron C, Syres G, Nichol A, et al. A pilot feasibility trial of allocation of freshest available red blood cells versus stan-dard care in critically ill patients. Transfusion 2012; 52: 1196–202.
116. Fernandes CJ Jr, Akamine N, De Marco FV, De Souza JA, Lagudis S, Knobel E. Red blood cell transfusion does not increase oxygen consumption in critically ill septic patients. Critical Care 2001; 5: 362–7.
117. Fernandes da Cunha DH, Nunes Dos Santos AM, Kopelman BI, et al. Transfusions of CPDA-1 red blood cells stored for up to 28 days decrease donor exposures in very low-birth-weight premature infants. Transfusion Medicine 2005; 15: 467–73.
118. Hebert PC, Chin-Yee I, Fergusson D, et al. A pilot trial evalu-ating the clinical effects of prolonged storage of red cells. Anestheisa and Analgesia 2005; 100: 1433–8.
119. Heddle NM, Cook RJ, Arnold DM, et al. The effect of blood storage duration on in-hospital mortality: a randomized controlled pilot feasibility trial. Transfusion 2012; 52: 1203–12.
120. Kor DJ, Kashyap R, Weiskopf RB, et al. Fresh red blood cell transfusion and short-term pulmonary, immunologic, and coagulation status: a randomized clinical trial. American Journal of Respiratory and Critical Care Medicine 2012; 185: 842–50.
121. Walsh TS, McArdle F, McLellan SA, et al. Does the storage time of transfused red blood cells influence regional or global indexes of tissue oxygenation in anemic critically ill patients? Critical Care Medicine 2004; 32: 364–71.
122. Wasser MN, Houbiers JG, D’Amaro J, et al. The effect of fresh versus stored blood on post-operative bleeding after coronary bypass surgery: a prospective randomized study. British Journal of Haematology 1989; 72: 81–4.
123. Yuruk K, Milstein DM, Bezemer R, Bartels SA, Biemond BJ, Ince C. Transfusion of banked red blood cells and the effects on hemorrheology and microvascular hemodynamics in anemic hematology outpatients. Transfusion 2013; 53: 1346–52.
124. Fergusson DA, Hebert P, Hogan DL, et al. Effect of fresh red blood cell transfusions on clinical outcomes in premature, very low-birth-weight infants: the ARIPI randomized trial. Journal of The American Medical Association 2012; 308: 1443–51.
125. Karkouti K. From the Journal archives: the red blood cell storage lesion: past, present, and future. Canadian Journal of Anesthesia 2014; 61: 583–6.
126. Zimrin AB, Hess JR. Current issues relating to the transfusion of stored red blood cells. Vox Sanguinis 2009; 96: 93–103.
127. Lelubre C, Piagnerelli M, Vincent JL. Association between duration of storage of transfused red blood cells and morbidity and mortality in adult patients: myth or reality? Transfusion 2009; 49: 1384–94.
128. Triulzi DJ, Yazer MH. Clinical studies of the effect of blood storage on patient outcomes. Transfusion and Apheresis Science 2010; 43: 95–106.
129. Vamvakas EC. Meta-analysis of clinical studies of the pur-ported deleterious effects of ‘‘old’’ (versus ‘‘fresh’’) red blood cells: are we at equipoise? Transfusion 2010; 50: 600–10.
130. Wang D, Sun J, Solomon SB, Klein HG, Natanson C. Transfusion of older stored blood and risk of death: a meta-analy-sis. Transfusion 2012; 52: 1184–95.
131. Zubair AC. Clinical impact of blood storage lesions. American Journal of Hematology 2010; 85: 117–22.
132. O’Donnell J, Boulton FE, Manning RA, Laffan MA. Amount of H antigen expressed on circulating von Willebrand factor is modified by ABO blood group genotype and is a major determinant of plasma von Willebrand factor antigen levels. Arteriosclerosis, Thrombosis, and Vascular Biology 2002; 22: 335–41.
133. Wiggins KL, Smith NL, Glazer NL, et al. ABO genotype and risk of thrombotic events and hemorrhagic stroke. Journal of Thrombosis and Haemostasis 2009; 7: 263–9.
134. Carpeggiani C, Coceani M, Landi P, Michelassi C, L’abbate A. ABO blood group alleles: a risk factor for coronary artery disease. An angiographic study. Atherosclerosis 2010; 211: 461–6.
135. Pereira A. Will clinical studies elucidate the connection between the length of storage of transfused red blood cells and clinical outcomes? An analysis based on the simulation of randomized controlled trials. Transfusion 2013; 53: 34– 40.