review
Does prolonged storage of red blood cells cause harm?
Willy A. Flegel,
Charles Natanson,
Harvey G. Klein,
Corresponding Author
Willy A. Flegel
Department of Transfusion Medicine and Critical Care Medicine Department, Clinical Center, National Institutes of Health, Bethesda, MD, USA
Correspondence: Willy A. Flegel, Department of Transfusion Medicine, Clinical Center, National Institutes of Health, Building 10, Room 1C711 MSC-1184, 10 Center Drive, Bethesda, MD 20892-1184, USA. E-mail: [email protected]Search for more papers by this authorCharles Natanson
Department of Transfusion Medicine and Critical Care Medicine Department, Clinical Center, National Institutes of Health, Bethesda, MD, USA
Search for more papers by this authorHarvey G. Klein
Department of Transfusion Medicine and Critical Care Medicine Department, Clinical Center, National Institutes of Health, Bethesda, MD, USA
Search for more papers by this authorWilly A. Flegel,
Charles Natanson,
Harvey G. Klein,
Corresponding Author
Willy A. Flegel
Department of Transfusion Medicine and Critical Care Medicine Department, Clinical Center, National Institutes of Health, Bethesda, MD, USA
Correspondence: Willy A. Flegel, Department of Transfusion Medicine, Clinical Center, National Institutes of Health, Building 10, Room 1C711 MSC-1184, 10 Center Drive, Bethesda, MD 20892-1184, USA. E-mail: [email protected]Search for more papers by this authorCharles Natanson
Department of Transfusion Medicine and Critical Care Medicine Department, Clinical Center, National Institutes of Health, Bethesda, MD, USA
Search for more papers by this authorHarvey G. Klein
Department of Transfusion Medicine and Critical Care Medicine Department, Clinical Center, National Institutes of Health, Bethesda, MD, USA
Search for more papers by this authorSummary
Red blood cells (RBCs) degrade progressively during the weeks of refrigerated storage. No universally accepted definition of ‘fresh’ or ‘old’ RBCs exists. While practices vary from country to country, preservative solutions permitting shelf life as long as 7 weeks have been licenced. Transfusion of stored RBCs, particularly those at the end of the approved shelf life, has been implicated in adverse clinical outcomes. The results of observational analyses, animal models and studies in volunteers have proved provocative, controversial and contradictory. A recently completed randomized controlled trial (RCT) in premature infants exemplifies the difficulties with moderately sized clinical studies. Several other RCTs are in progress. The effect of RBC storage may well vary according to the clinical setting. Resolution of the importance of the storage lesion may require large pragmatic clinical trials. In the meantime, institutions involved in blood collection and transfusion should explore strategies that assure blood availability, while limiting the use of the oldest RBCs currently approved by regulation.
References
- Alexander, J.T., Eli-Ali, A.M., Newman, J.L., Karatela, S., Predmore, B.L., Lefer, D.J., Sutliff, R.L. & Roback, J.D. (2013) Red blood cells stored for increasing periods produce progressive impairments in nitric oxide-mediated vasodilation. Transfusion, 53, 2619–2628.
- d'Almeida, M.S., Jagger, J., Duggan, M., White, M., Ellis, C. & Chin-Yee, I.H. (2000) A comparison of biochemical and functional alterations of rat and human erythrocytes stored in CPDA-1 for 29 days: implications for animal models of transfusion. Transfusion Medicine, 10, 291–303.
- Aubron, C., Syres, G., Nichol, A., Bailey, M., Board, J., Magrin, G., Murray, L., Presneill, J., Sutton, J., Vallance, S., Morrison, S., Bellomo, R. & Cooper, D.J. (2012) A pilot feasibility trial of allocation of freshest available red blood cells versus standard care in critically ill patients. Transfusion, 52, 1196–1202.
- Aubron, C., Nichol, A., Cooper, D.J. & Bellomo, R. (2013) Age of red blood cells and transfusion in critically ill patients. Annals of Intensive Care, 3, 2–3.
- AuBuchon, J.P., Estep, T.N. & Davey, R.J. (1988) The effect of the plasticizer di-2-ethylhexyl phthalate on the survival of stored RBCs. Blood, 71, 448–452.
- Badesch, D.B., Champion, H.C., Sanchez, M.A., Hoeper, M.M., Loyd, J.E., Manes, A., McGoon, M., Naeije, R., Olschewski, H., Oudiz, R.J. & Torbicki, A. (2009) Diagnosis and assessment of pulmonary arterial hypertension. Journal of the American College of Cardiology, 54, S55–S66.
- Baek, J.H., D'Agnillo, F., Vallelian, F., Pereira, C.P., Williams, M.C., Jia, Y., Schaer, D.J. & Buehler, P.W. (2012) 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. The Journal of Clinical Investigation, 122, 1444–1458.
- Baron, D.M., Yu, B., Lei, C., Bagchi, A., Beloiartsev, A., Stowell, C.P., Steinbicker, A.U., Malhotra, R., Bloch, K.D. & Zapol, W.M. (2012) Pulmonary hypertension in lambs transfused with stored blood is prevented by breathing nitric oxide. Anesthesiology, 116, 637–647.
- Bennett-Guerrero, E., Stafford-Smith, M., Waweru, P.M., Bredehoeft, S.J., Campbell, M.L., Haley, N.R., Phillips-Bute, B., Newman, M.F. & Bandarenko, N. (2009) A prospective, double-blind, randomized clinical feasibility trial of controlling the storage age of red blood cells for transfusion in cardiac surgical patients. Transfusion, 49, 1375–1383.
- Berra, L., Coppadoro, A., Yu, B., Lei, C., Spagnolli, E., Steinbicker, A.U., Bloch, K.D., Lin, T., Sammy, F.Y., Warren, H.S., Fernandez, B.O., Feelisch, M., Dzik, W.H., Stowell, C.P. & Zapol, W.M. (2012) Transfusion of stored autologous blood does not alter reactive hyperemia index in healthy volunteers. Anesthesiology, 117, 56–63.
- Beutler, E. & West, C. (1979) The storage of hard-packed red blood cells in citrate-phosphate-dextrose (CPD) and CPD-adenine (CPDA-1). Blood, 54, 280–284.
- Blajchman, M.A., Glynn, S.A., Josephson, C.D. & Kleinman, S.H. (2010) Clinical trial opportunities in transfusion medicine: proceedings of a National Heart, Lung, and Blood Institute State-of-the-Science Symposium. Transfusion Medicine Reviews, 24, 259–285.
- Blajchman, M.A., Carson, J.L., Eikelboom, J.W., Heddle, N.M., Lacroix, J., Lauer, M.S., Platt, R., Tilley, B., Triulzi, D., Vickers, A.J., Yusuf, S., Glynn, S., Mondoro, T.H. & Wagner, E. (2012) The role of comparative effectiveness research in transfusion medicine clinical trials: proceedings of a National Heart, Lung, and Blood Institute workshop. Transfusion, 52, 1363–1378.
- Bordin, J.O., Heddle, N.M. & Blajchman, M.A. (1994) Biologic effects of leukocytes present in transfused cellular blood products. Blood, 84, 1703–1721.
- Bundesärztekammer & Paul-Ehrlich-Institut (2010) Richtlinien zur Gewinnung von Blut und Blutbestandteilen und zur Anwendung von Blutprodukten (Hämotherapie) gemäß §§ 12 und 18 des Transfusionsgesetzes (TFG). Bundesanzeiger, 62, 3–36.
- van Buskirk, C.M., Kashyap, R., Thakur, S.J., Murray, D.L., Bryant, S.C., Winters, J.L., Stubbs, J.R. & Gajic, O. (2009) Red blood cell storage has no impact on clinical outcome in critically ill patients. (Abstract). Transfusion, 49, 10A.
- Carson, T.H. (2012) Standards for Blood Banks and Transfusion Services, 28th edn. AABB, Bethesda, MD.
- Cheng, C.K., Trethewey, D. & Sadek, I. (2010) Comprehensive survey of red blood cell unit life cycle at a large teaching institution in eastern Canada. Transfusion, 50, 160–165.
- Chin-Yee, I., Arya, N. & d'Almeida, M.S. (1997) The red cell storage lesion and its implication for transfusion. Transfusion Science, 18, 447–458.
- Cortes-Puch, I., Wang, D., Sun, J., Solomon, S.B., Remy, K.E., Fernandez, M., Feng, J., Kania, T., Bellavia, L., Sinchar, D., Perlegas, A., Solomon, M.A., Kelley, W.E., Popovsky, M.A., Gladwin, M.T., Kim-Shapiro, D.B., Klein, H.G. & Natanon, C. (2014) Washing older blood units before transfusion reduces plasma iron and improves outcomes in experimental canine pneumonia. Blood, 123 (in press).
- D'Amici, G.M., Mirasole, C., D'Alessandro, A., Yoshida, T., Dumont, L.J. & Zolla, L. (2012) Red blood cell storage in SAGM and AS3: a comparison through the membrane two-dimensional electrophoresis proteome. Blood Transfusion, 10, s46–s54.
- Donadee, C., Raat, N.J., Kanias, T., Tejero, J., Lee, J.S., Kelley, E.E., Zhao, X., Liu, C., Reynolds, H., Azarov, I., Frizzell, S., Meyer, E.M., Donnenberg, A.D., Qu, L., Triulzi, D., Kim-Shapiro, D.B. & Gladwin, M.T. (2011) Nitric oxide scavenging by red blood cell microparticles and cell-free hemoglobin as a mechanism for the red cell storage lesion. Circulation, 124, 465–476.
- Dumont, L.J. & AuBuchon, J.P. (2008) Evaluation of proposed FDA criteria for the evaluation of radiolabeled red cell recovery trials. Transfusion, 48, 1053–1060.
- Dumont, L.J., Yoshida, T. & AuBuchon, J.P. (2009) Anaerobic storage of red blood cells in a novel additive solution improves in vivo recovery. Transfusion, 49, 458–464.
- Dzik, W. (2008) Fresh blood for everyone? Balancing availability and quality of stored RBCs. Transfusion Medicine (Oxford, England), 18, 260–265.
- Edgren, G., Kamper-Jorgensen, M., Eloranta, S., Rostgaard, K., Custer, B., Ullum, H., Murphy, E.L., Busch, M.P., Reilly, M., Melbye, M., Hjalgrim, H. & Nyren, O. (2010) Duration of red blood cell storage and survival of transfused patients (CME). Transfusion, 50, 1185–1195.
- Eikelboom, J.W., Cook, R.J., Liu, Y. & Heddle, N.M. (2010) Duration of red cell storage before transfusion and in-hospital mortality. American Heart Journal, 159, 737–743.
- Fergusson, D.A., Hebert, P., Hogan, D.L., LeBel, L., Rouvinez-Bouali, N., Smyth, J.A., Sankaran, K., Tinmouth, A., Blajchman, M.A., Kovacs, L., Lachance, C., Lee, S., Walker, C.R., Hutton, B., Ducharme, R., Balchin, K., Ramsay, T., Ford, J.C., Kakadekar, A., Ramesh, K. & Shapiro, S. (2012) 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, 308, 1443–1451.
- Fernandes da Cunha, D.H., Nunes Dos Santos, A.M., Kopelman, B.I., Areco, K.N., Guinsburg, R., de Araujo, P.C., Chiba, A.K., Kuwano, S.T., Terzian, C.C. & Bordin, J.O. (2005) 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, 15, 467–473.
- Fernandes, C.J. Jr, Akamine, N., De Marco, F.V., De Souza, J.A., Lagudis, S. & Knobel, E. (2001) Red blood cell transfusion does not increase oxygen consumption in critically ill septic patients. Critical Care, 5, 362–367.
- Flegel, W.A. (2012) Fresh blood for transfusion: how old is too old for red blood cell units? [Editorial]. Blood Transfusion, 10, 247–251.
- Francis, R.O., Jhang, J.S., Pham, H.P., Hod, E.A., Zimring, J.C. & Spitalnik, S.L. (2013) Glucose-6-phosphate dehydrogenase deficiency in transfusion medicine: the unknown risks. Vox Sanguinis, 105, 271–282.
- Frank, S.M., Abazyan, B., Ono, M., Hogue, C.W., Cohen, D.B., Berkowitz, D.E., Ness, P.M. & Barodka, V.M. (2013) Decreased erythrocyte deformability after transfusion and the effects of erythrocyte storage duration. Anesthesia and Analgesia, 116, 975–981.
- Frenzel, T., Sibrowski, W. & Westphal, M. (2008) Red-cell storage and complications of cardiac surgery. The New England Journal of Medicine, 358, 2841–2842.
- Fung, Y.L., Tung, J.P., Foley, S.R., Simonova, G., Thom, O., Staib, A., Collier, J., Dunster, K.R., Solano, C., Shekar, K., Chew, M.S. & Fraser, J.F. (2013) Stored blood transfusion induces transient pulmonary arterial hypertension without impairing coagulation in an ovine model of nontraumatic haemorrhage. Vox Sanguinis, 105, 150–158.
- Gauvin, F., Spinella, P.C., Lacroix, J., Choker, G., Ducruet, T., Karam, O., Hebert, P.C., Hutchison, J.S., Hume, H.A. & Tucci, M. (2010) Association between length of storage of transfused red blood cells and multiple organ dysfunction syndrome in pediatric intensive care patients. Transfusion, 50, 1902–1913.
- Gilson, C.R., Kraus, T.S., Hod, E.A., Hendrickson, J.E., Spitalnik, S.L., Hillyer, C.D., Shaz, B.H. & Zimring, J.C. (2009) A novel mouse model of red blood cell storage and posttransfusion in vivo survival. Transfusion, 49, 1546–1553.
- Greening, D.W., Glenister, K.M., Sparrow, R.L. & Simpson, R.J. (2010) International blood collection and storage: clinical use of blood products. Journal of Proteomics, 73, 386–395.
- Hebert, P.C., Chin-Yee, I., Fergusson, D., Blajchman, M., Martineau, R., Clinch, J. & Olberg, B. (2005) A pilot trial evaluating the clinical effects of prolonged storage of red cells. Anesthesia and Analgesia, 100, 1433–1438, table.
- Heddle, N.M., Cook, R.J., Arnold, D.M., Crowther, M.A., Warkentin, T.E., Webert, K.E., Hirsh, J., Barty, R.L., Liu, Y., Lester, C. & Eikelboom, J.W. (2012) The effect of blood storage duration on in-hospital mortality: a randomized controlled pilot feasibility trial. Transfusion, 52, 1203–1212.
- Hendrickson, J.E., Hod, E.A., Hudson, K.E., Spitalnik, S.L. & Zimring, J.C. (2011) Transfusion of fresh murine red blood cells reverses adverse effects of older stored red blood cells. Transfusion, 51, 2695–2702.
- Hess, J.R. (2006) An update on solutions for red cell storage. Vox Sanguinis, 91, 13–19.
- Hess, J.R. (2012) Scientific problems in the regulation of red blood cell products. Transfusion, 52, 1827–1835.
- Hess, J.R., Hill, H.R., Oliver, C.K., Lippert, L.E., Rugg, N., Joines, A.D., Gormas, J.F., Pratt, P.G., Silverstein, E.B. & Greenwalt, T.J. (2003) Twelve-week RBC storage. Transfusion, 43, 867–872.
- Hess, J.R., Rugg, N., Joines, A.D., Gormas, J.F., Pratt, P.G., Silberstein, E.B. & Greenwalt, T.J. (2006) Buffering and dilution in red blood cell storage. Transfusion, 46, 50–54.
- Hess, J.R., Sparrow, R.L., van der Meer, P.F., Acker, J.P., Cardigan, R.A. & Devine, D.V. (2009) Red blood cell hemolysis during blood bank storage: using national quality management data to answer basic scientific questions. Transfusion, 49, 2599–2603.
- Hill, H.R., Oliver, C.K., Lippert, L.E., Greenwalt, T.J. & Hess, J.R. (2001) The effects of polyvinyl chloride and polyolefin blood bags on red blood cells stored in a new additive solution. Vox Sanguinis, 81, 161–166.
- Hod, E.A., Zhang, N., Sokol, S.A., Wojczyk, B.S., Francis, R.O., Ansaldi, D., Francis, K.P., La-Latta, P., Whittier, S., Sheth, S., Hendrickson, J.E., Zimring, J.C., Brittenham, G.M. & Spitalnik, S.L. (2010) Transfusion of red blood cells after prolonged storage produces harmful effects that are mediated by iron and inflammation. Blood, 115, 4284–4292.
- Hod, E.A., Brittenham, G.M., Billote, G.B., Francis, R.O., Ginzburg, Y.Z., Hendrickson, J.E., Jhang, J., Schwartz, J., Sharma, S., Sheth, S., Sireci, A.N., Stephens, H.L., Stotler, B.A., Wojczyk, B.S., Zimring, J.C. & Spitalnik, S.L. (2011) Transfusion of human volunteers with older, stored red blood cells produces extravascular hemolysis and circulating non-transferrin-bound iron. Blood, 118, 6675–6682.
- Hogman, C.F. (1985) In vitro haemolysis of SAG-M and CPD-A blood units. Vox Sanguinis, 48, 126–127.
- Hogman, C.F., Hedlund, K. & Zetterstrom, H. (1978) Clinical usefulness of red cells preserved in protein-poor mediums. The New England Journal of Medicine, 299, 1377–1382.
- Hu, W., Jin, R., Zhang, J., You, T., Peng, Z., Ge, X., Bronson, R.T., Halperin, J.A., Loscalzo, J. & Qin, X. (2010) The critical roles of platelet activation and reduced NO bioavailability in fatal pulmonary arterial hypertension in a murine hemolysis model. Blood, 116, 1613–1622.
- Janz, D.R., Zhao, Z., Koyama, T., May, A.K., Bernard, G.R., Bastarache, J.A., Young, P.P. & Ware, L.B. (2013) Longer storage duration of red blood cells is associated with an increased risk of acute lung injury in patients with sepsis. Annals of Intensive Care, 3, 33.
- Jeffers, A., Gladwin, M.T. & Kim-Shapiro, D.B. (2006) Computation of plasma hemoglobin nitric oxide scavenging in hemolytic anemias. Free Radical Biology & Medicine, 41, 1557–1565.
- Karam, O., Tucci, M., Bateman, S.T., Ducruet, T., Spinella, P.C., Randolph, A.G. & Lacroix, J. (2010) Association between length of storage of red blood cell units and outcome of critically ill children: a prospective observational study. Critical Care, 14, R57.
- Kennedy, M.S. (2011) Perinatal issues in transfusion practice. In: Technical Manual (ed. by J.D. Roback, B.J. Grossman, T. Harris & C.D. Hillyer), pp. 631–644. AABB, Bethesda, MD.
- Klein, H.G. (1999) Immunomodulatory aspects of transfusion: a once and future risk? Anesthesiology, 91, 861–865.
- Klein, H.G. (2012) Comparative effectiveness research: welcome to the real world. Transfusion, 52, 1162–1164.
- Klein, H.G. (2013) Should blood be an essential medicine? The New England Journal of Medicine, 368, 199–201.
- Klein, H.G. & Natanson, C. (2012) Red blood cell transfusion. Annals of Internal Medicine, 157, 753–754.
- Klein, H.G., Spahn, D.R. & Carson, J.L. (2007) Red blood cell transfusion in clinical practice. Lancet, 370, 415–426.
- Koch, C.G., Li, L., Sessler, D.I., Figueroa, P., Hoeltge, G.A., Mihaljevic, T. & Blackstone, E.H. (2008) Duration of red-cell storage and complications after cardiac surgery. The New England Journal of Medicine, 358, 1229–1239.
- Koch, C.G., Figueroa, P.I., Li, L., Sabik, J.F. III, Mihaljevic, T. & Blackstone, E.H. (2013) Red blood cell storage: how long is too long? The Annals of Thoracic Surgery, 96, 1894–1899.
- Kor, D.J., Kashyap, R., Weiskopf, R.B., Wilson, G.A., van Buskirk, C.M., Winters, J.L., Malinchoc, M., Hubmayr, R.D. & Gajic, O. (2012) 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, 185, 842–850.
- Lacroix, J., Hebert, P., Fergusson, D., Tinmouth, A., Blajchman, M.A., Callum, J., Cook, D., Marshall, J.C., McIntyre, L. & Turgeon, A.F. (2011) The Age of Blood Evaluation (ABLE) randomized controlled trial: study design. Transfusion Medicine Reviews, 25, 197–205.
- Leal-Noval, S.R., Munoz-Gomez, M., Rellano-Orden, V., Marin-Caballos, A., Maya-Villar, R., Marin, A., Puppo-Moreno, A., Ferrandiz-Millon, C., Flores-Cordero, J.M. & Murillo-Cabezas, F. (2008) Impact of age of transfused blood on cerebral oxygenation in male patients with severe traumatic brain injury. Critical Care Medicine, 36, 1290–1296.
- Lelubre, C. & Vincent, J.L. (2013) Relationship between red cell storage duration and outcomes in adults receiving red cell transfusions: a systematic review. Critical Care, 17, R66.
- Luban, N., Rais-Bahrami, K. & Short, B. (2006) I want to say one word to you - just one word - “plastics”. Transfusion, 46, 503–506.
- Luten, M., Roerdinkholder-Stoelwinder, B., Schaap, N.P., de Grip, W.J., Bos, H.J. & Bosman, G.J. (2008) Survival of red blood cells after transfusion: a comparison between red cells concentrates of different storage periods. Transfusion, 48, 1478–1485.
- McCullough, J. (2013) Red cell storage: does duration matter? Blood, 121, 1491–1492.
- McLaughlin, V.V., Langer, A., Tan, M., Clements, P.J., Oudiz, R.J., Tapson, V.F., Channick, R.N. & Rubin, L.J. (2013) Contemporary trends in the diagnosis and management of pulmonary arterial hypertension: an initiative to close the care gap. Chest, 143, 324–332.
- Middelburg, R.A., van de Watering, L.M., Briet, E. & van der Bom, J.G. (2013) Storage time of red blood cells and mortality of transfusion recipients. Transfusion Medicine Reviews, 27, 36–43.
- Minneci, P.C., Deans, K.J., Zhi, H., Yuen, P.S., Star, R.A., Banks, S.M., Schechter, A.N., Natanson, C., Gladwin, M.T. & Solomon, S.B. (2005) Hemolysis-associated endothelial dysfunction mediated by accelerated NO inactivation by decompartmentalized oxyhemoglobin. The Journal of Clinical Investigation, 115, 3409–3417.
- Moroff, G., Holme, S., Keegan, T. & Heaton, A. (1990) Storage of ADSOL-preserved red cells at 2.5 and 5.5 degrees C: comparable retention of in vitro properties. Vox Sanguinis, 59, 136–139.
- Murrell, Z., Haukoos, J.S., Putnam, B. & Klein, S.R. (2005) The effect of older blood on mortality, need for ICU care, and the length of ICU stay after major trauma. American Surgeon, 71, 781–785.
- Mynster, T. & Nielsen, H.J. (2001) Storage time of transfused blood and disease recurrence after colorectal cancer surgery. Diseases of the Colon and Rectum, 44, 955–964.
- Nester, T. & AuBuchon, J.P. (2011) Hemotherapy decisions and their outcomes. In: Technical Manual (ed. by J.D. Roback, B.J. Grossman, T. Harris & C.D. Hillyer), pp. 571–615. AABB, Bethesda, MD.
- Nicholson, S.E., Johnson, R.A., Craig, T., Myers, J.G., Durante, W., Stewart, R.M. & Johnson, F.K. (2011) Transfusion-related acute lung injury in a rat model of trauma-hemorrhage. Journal of Trauma, 70, 466–471.
- Orlina, A.R. & Josephson, A.M. (1969) Comparative viability of blood stored in ACD and CPD. Transfusion, 9, 62–69.
- Otani, T., Oki, K., Akino, M., Tamura, S., Naito, Y., Homma, C., Ikeda, H. & Sumita, S. (2012) Effects of helicopter transport on red blood cell components. Blood Transfusion, 10, 78–86.
- Pavenski, K., Saidenberg, E., Lavoie, M., Tokessy, M. & Branch, D.R. (2012) Red blood cell storage lesions and related transfusion issues: a Canadian Blood Services research and development symposium. Transfusion Medicine Reviews, 26, 68–84.
- Pereira, A. (2013) 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, 53, 34–40.
- Pettila, V., Westbrook, A.J., Nichol, A.D., Bailey, M.J., Wood, E.M., Syres, G., Phillips, L.E., Street, A., French, C., Murray, L., Orford, N., Santamaria, J.D., Bellomo, R. & Cooper, D.J. (2011) Age of red blood cells and mortality in the critically ill. Critical Care, 15, R116.
- Reiter, C.D., Wang, X., Tanus-Santos, J.E., Hogg, N., Cannon, R.O. III, Schechter, A.N. & Gladwin, M.T. (2002) Cell-free hemoglobin limits nitric oxide bioavailability in sickle-cell disease. Nature Medicine, 8, 1383–1389.
- Robinson, S.D., Janssen, C., Fretz, E.B., Berry, B., Chase, A.J., Siega, A.D., Carere, R.G., Fung, A., Simkus, G., Klinke, W.P. & Hilton, J.D. (2010) Red blood cell storage duration and mortality in patients undergoing percutaneous coronary intervention. American Heart Journal, 159, 876–881.
- Rock, G., Tocchi, M., Ganz, P.R. & Tackaberry, E.S. (1984) Incorporation of plasticizer into red cells during storage. Transfusion, 24, 493–498.
- Rother, R.P., Bell, L., Hillmen, P. & Gladwin, M.T. (2005) The clinical sequelae of intravascular hemolysis and extracellular plasma hemoglobin: a novel mechanism of human disease. Journal of the American Medical Association, 293, 1653–1662.
- Saager, L., Turan, A., Dalton, J.E., Figueroa, P.I., Sessler, D.I. & Kurz, A. (2013) Erythrocyte storage duration is not associated with increased mortality in noncardiac surgical patients: a retrospective analysis of 6,994 patients. Anesthesiology, 118, 51–58.
- Sakakibara, T. & Juji, T. (1986) Post-transfusion graft-versus-host disease after open heart surgery [Letter]. Lancet, 2, 1099.
- Schaer, D.J., Buehler, P.W., Alayash, A.I., Belcher, J.D. & Vercellotti, G.M. (2013) Hemolysis and free hemoglobin revisited: exploring hemoglobin and hemin scavengers as a novel class of therapeutic proteins. Blood, 121, 1276–1284.
- Schulman, C.I., Nathe, K., Brown, M. & Cohn, S.M. (2002) Impact of age of transfused blood in the trauma patient. Journal of Trauma, 52, 1224–1225.
- Simonova, G., Tung, J.P., Fraser, J.F., Do, H.L., Staib, A., Chew, M.S., Dunster, K.R., Glenister, K.M., Jackson, D.E. & Fung, Y.L. (2014) A comprehensive ovine model of blood transfusion. Vox Sanguinis, 106 (in press).
- Solheim, B.G., Flesland, O., Seghatchian, J. & Brosstad, F. (2004) Clinical implications of red blood cell and platelet storage lesions: an overview. Transfusion and Apheresis Science, 31, 185–189.
- Solomon, S.B., Wang, D., Sun, J., Kanias, T., Feng, J., Helms, C.C., Solomon, M.A., Alimchandani, M., Quezado, M., Gladwin, M.T., Kim-Shapiro, D.B., Klein, H.G. & Natanson, C. (2013) Mortality increases after massive exchange transfusion with older stored blood in canines with experimental pneumonia. Blood, 121, 1663–1672.
- Sparrow, R.L. (2012) Time to revisit red blood cell additive solutions and storage conditions: a role for “omics” analyses. Blood Transfusion, 10, s7–s11.
- Spinella, P.C., Carroll, C.L., Staff, I., Gross, R., Mc, Q.J., Keibel, L., Wade, C.E. & Holcomb, J.B. (2009) 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, 13, R151.
- Steiner, M.E., Assmann, S.F., Levy, J.H., Marshall, J., Pulkrabek, S., Sloan, S.R., Triulzi, D. & Stowell, C.P. (2010) Addressing the question of the effect of RBC storage on clinical outcomes: the Red Cell Storage Duration Study (RECESS) (Section 7). Transfusion and Apheresis Science, 43, 107–116.
- van Straten, A.H., Soliman Hamad, M.A., van Zundert, A.A., Martens, E.J., ter Woorst, J.F., de Wolf, A.M. & Scharnhorst, V. (2011) Effect of duration of red blood cell storage on early and late mortality after coronary artery bypass grafting. Journal of Thoracic and Cardiovascular Surgery, 141, 231–237.
- Tinmouth, A. & Chin-Yee, I. (2001) The clinical consequences of the red cell storage lesion. Transfusion Medicine Reviews, 15, 91–107.
- Tung, J.P., Fung, Y.L., Nataatmadja, M., Colebourne, K.I., Esmaeel, H.M., Wilson, K., Barnett, A.G., Wood, P., Silliman, C.C. & Fraser, J.F. (2011) A novel in vivo ovine model of transfusion-related acute lung injury (TRALI). Vox Sanguinis, 100, 219–230.
- Tung, J.P., Fraser, J.F., Nataatmadja, M., Colebourne, K.I., Barnett, A.G., Glenister, K.M., Zhou, A.Y., Wood, P., Silliman, C.C. & Fung, Y.L. (2012) Age of blood and recipient factors determine the severity of transfusion-related acute lung injury (TRALI). Critical Care, 16, R19.
- UK Blood Transfusion & Tissue Transplantation Services (2013) Guidelines for the Blood Transfusion Services in the United Kingdom, 8th edn. The Stationary Office, London.
- UK Legislation (2005) The Blood Safety and Quality Regulations 2005. Statutory Instruments 2005 No. 50. Health and Safety. © Crown copyright 2005.
- Vamvakas, E.C. (2007) Why have meta-analyses of randomized controlled trials of the association between non-white-blood-cell-reduced allogeneic blood transfusion and postoperative infection produced discordant results? Vox Sanguinis, 93, 196–207.
- Wagner, S.J., Glynn, S.A. & Welniak, L. (2014) Research opportunities in optimizing storage of red blood cell products. Transfusion, 54, doi: 10.1111/trf.12244
10.1111/trf.12244 Google Scholar
- Wallis, J.P., Wells, A.W., Babb, R.G., Stainsby, D. & Hamilton, P.J. (2005) Effect of storage age of transfused blood on 48 hour Hb increment and recovery of 2,3 DPG in haematology patients. (Abstract). British Journal of Haematology, 129, 1.
- Walsh, T.S., McArdle, F., McLellan, S.A., Maciver, C., Maginnis, M., Prescott, R.J. & McClelland, D.B. (2004) 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, 32, 364–371.
- Wang, D., Sun, J., Solomon, S.B., Klein, H.G. & Natanson, C. (2012) Transfusion of older stored blood and risk of death: a meta-analysis. Transfusion, 52, 1184–1195.
- Wang, D., Cortes-Puch, I., Sun, J., Solomon, S.B., Kanias, T., Remy, K.E., Feng, J., Alimchandani, M., Quezado, M., Helms, C.C., Perlegas, A., Gladwin, M.T., Kim-Shapiro, D.B., Klein, H.G. & Natanson, C. (2014) Transfusion of older stored blood worsens outcomes in canines depending on the presence and severity of pneumonia. Transfusion, 54 (in press).
10.1111/trf.12607 Google Scholar
- Wardrop, K.J. (1995) Selection of anticoagulant-preservatives for canine and feline blood storage. The Veterinary Clinics of North America. Small Animal Practice, 25, 1263–1276.
- Wardrop, K.J., Tucker, R.L. & Mugnai, K. (1997) Evaluation of canine red blood cells stored in a saline, adenine, and glucose solution for 35 days. Journal of Veterinary Internal Medicine, 11, 5–8.
- Wasser, M.N., Houbiers, J.G., D'Amaro, J., Hermans, J., Huysmans, H.A., van Konijnenburg, G.C. & Brand, A. (1989) The effect of fresh versus stored blood on post-operative bleeding after coronary bypass surgery: a prospective randomized study. British Journal of Haematology, 72, 81–84.
- van de Watering, L.M. (2011) Pitfalls in the current published observational literature on the effects of red blood cell storage. Transfusion, 51, 1847–1854.
- van de Watering, L.M. (2013) Effects of red blood cell storage in heavily transfused patients. Current Opinion in Anaesthesiology, 26, 204–207.
- van de Watering, L.M., Lorinser, J., Versteegh, M., Westendord, R. & Brand, A. (2006) Effects of storage time of red blood cell transfusions on the prognosis of coronary artery bypass graft patients. Transfusion, 46, 1712–1718.
- Weinberg, J.A., McGwin, G. Jr, Griffin, R.L., Huynh, V.Q., Cherry, S.A. III, Marques, M.B., Reiff, D.A., Kerby, J.D. & Rue, L.W. III (2008a) Age of transfused blood: an independent predictor of mortality despite universal leukoreduction. Journal of Trauma, 65, 279–282.
- Weinberg, J.A., McGwin, G. Jr, Marques, M.B., Cherry, S.A. III, Reiff, D.A., Kerby, J.D. & Rue, L.W. III (2008b) Transfusions in the less severely injured: does age of transfused blood affect outcomes? Journal of Trauma, 65, 794–798.
- Weinberg, J.A., McGwin, G. Jr, Vandromme, M.J., Marques, M.B., Melton, S.M., Reiff, D.A., Kerby, J.D. & Rue, L.W. III (2010) Duration of red cell storage influences mortality after trauma. Journal of Trauma, 69, 1427–1431.
- Weiskopf, R.B., Feiner, J., Hopf, H., Lieberman, J., Finlay, H.E., Quah, C., Kramer, J.H., Bostrom, A. & Toy, P. (2006) Fresh blood and aged stored blood are equally efficacious in immediately reversing anemia-induced brain oxygenation deficits in humans. Anesthesiology, 104, 911–920.
- Weiskopf, R.B., Feiner, J., Toy, P., Twiford, J., Shimabukuro, D., Lieberman, J., Looney, M.R., Lowell, C.A. & Gropper, M.A. (2012) Fresh and stored red blood cell transfusion equivalently induce subclinical pulmonary gas exchange deficit in normal humans. Anesthesia and Analgesia, 114, 511–519.
- Wilkinson, K.L., Brunskill, S.J., Doree, C., Hopewell, S., Stanworth, S., Murphy, M.F. & Hyde, C. (2011) The clinical effects of red blood cell transfusions: an overview of the randomized controlled trials evidence base. Transfusion Medicine Reviews, 25, 145–155.
- Willy, C., Reithmeier, W., Kuhlmann, W.D., Gerngross, H. & Flegel, W.A. (2000) Leukocyte depletion of red cell components prevents exposure of transfusion recipients to neutrophil elastase. Vox Sanguinis, 78, 19–27.
- Yap, C.H., Lau, L., Krishnaswamy, M., Gaskell, M. & Yii, M. (2008) Age of transfused red cells and early outcomes after cardiac surgery. The Annals of Thoracic Surgery, 86, 554–559.
- Yoshida, T. & Shevkoplyas, S.S. (2010) Anaerobic storage of red blood cells. Blood Transfusion, 8, 220–236.
- Yu, B., Raher, M.J., Volpato, G.P., Bloch, K.D., Ichinose, F. & Zapol, W.M. (2008) Inhaled nitric oxide enables artificial blood transfusion without hypertension. Circulation, 117, 1982–1990.
- Yürük, K., Milstein, D.M., Bezemer, R., Bartels, S.A., Biemond, B.J. & Ince, C. (2013) Transfusion of banked red blood cells and the effects on hemorrheology and microvascular hemodynamics in anemic hematology outpatients. Transfusion, 53, 1346–1352.
- Zehnder, L., Schulzki, T., Goede, J.S., Hayes, J. & Reinhart, W.H. (2008) Erythrocyte storage in hypertonic (SAGM) or isotonic (PAGGSM) conservation medium: influence on cell properties. Vox Sanguinis, 95, 280–287.
- Zimring, J.C., Welniak, L., Semple, J.W., Ness, P.M., Slichter, S.J. & Spitalnik, S.L. (2011) Current problems and future directions of transfusion-induced alloimmunization: summary of an NHLBI working group. Transfusion, 51, 435–441.
- Zubair, A.C. (2010) Clinical impact of blood storage lesions. American Journal of Hematology, 85, 117–122.
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