Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter March 19, 2015

Molecular mechanisms of erythrocyte aging

  • Richard S. Hoehn

    From left to right: Richard Hoehn, Peter Jernigan, and Alex Chang are surgical residents at the University of Cincinnati College of Medicine, currently participating in a research fellowship. Their areas of research interest include blood banking, trauma, and sphingolipids. Timothy Pritts is a trauma surgeon at the University of Cincinnati, with research interests including blood banking, shock and resuscitation, lung injury, and traumatic brain injury. Michael Edwards is the chairman of surgery at the University of Cincinnati, with specific research interests including sphingolipids and translational medicine, and is also an avid car racing enthusiast.

    , Peter L. Jernigan , Alex L. Chang , Michael J. Edwards and Timothy A. Pritts EMAIL logo
From the journal Biological Chemistry

Abstract

Anemia and hemorrhagic shock are leading causes of morbidity and mortality worldwide, and transfusion of human blood products is the ideal treatment for these conditions. As human erythrocytes age during storage in blood banks they undergo many biochemical and structural changes, termed the red blood cell ‘storage lesion’. Specifically, ATP and pH levels decrease as metabolic end products, oxidative stress, cytokines, and cell-free hemoglobin increase. Also, membrane proteins and lipids undergo conformational and organizational changes that result in membrane loss, viscoelastic changes and microparticle formation. As a result, transfusion of aged blood is associated with a host of adverse consequences such as decreased tissue perfusion, increased risk of infection, and increased mortality. This review summarizes current research detailing the known parts of the erythrocyte storage lesion and their physiologic consequences.


Corresponding author: Timothy A. Pritts, Department of Surgery and Institute for Military Medicine, University of Cincinnati, 231 Albert Sabin Way, Cincinnati, OH 45267–0558, USA, e-mail:

About the author

Richard S. Hoehn

From left to right: Richard Hoehn, Peter Jernigan, and Alex Chang are surgical residents at the University of Cincinnati College of Medicine, currently participating in a research fellowship. Their areas of research interest include blood banking, trauma, and sphingolipids. Timothy Pritts is a trauma surgeon at the University of Cincinnati, with research interests including blood banking, shock and resuscitation, lung injury, and traumatic brain injury. Michael Edwards is the chairman of surgery at the University of Cincinnati, with specific research interests including sphingolipids and translational medicine, and is also an avid car racing enthusiast.

Acknowledgments

TAP was supported in part by grant R01 GM107625 from the National Institute of General Medical Sciences of the US National Institutes of Health. The authors would also like to acknowledge Dr. Erich Gulbins of the University of Duisburg-Essen for his contributions to this project and others.

References

Aatonen, M.T., Ohman, T., Nyman, T.A., Laitinen, S., Grönholm, M., and Siljander, P.R. (2014). Isolation and characterization of platelet-derived extracellular vesicles. J. Extracell. Vesicles 3, 10.3402/jev.v3.24692. Published online 2014 Aug 6.10.3402/jev.v3.24692Search in Google Scholar PubMed PubMed Central

Adar, T., Ben-Ami, R., Elstein, D., Zimran, P., Berliner, S., Yedgar, S., and Barshtein, G. (2008). Increased red blood cell aggregation in patients with Gaucher disease is non-inflammatory. Clin. Hemorheol. Microcirc. 40, 113–118.10.3233/CH-2008-1121Search in Google Scholar

Aguilera-Romero, A., Gehin, C., and Riezman, H. (2014). Sphingolipid homeostasis in the web of metabolic routes. Biochim. Biophys. Acta 1841, 647–656.10.1016/j.bbalip.2013.10.014Search in Google Scholar PubMed

Anniss, A.M. and Sparrow, R.L. (2006). Storage duration and white blood cell content of red blood cell (RBC) products increases adhesion of stored RBCs to endothelium under flow conditions. Transfusion 46, 1561–1567.10.1111/j.1537-2995.2006.00944.xSearch in Google Scholar PubMed

Awojoodu, A.O., Keegan, P.M., Lane, A.R., Zhang, Y., Lynch, K.R., Platt, M.O., and Botchwey, E.A. (2014). Acid sphingomyelinase is activated in sickle cell erythrocytes and contributes to inflammatory microparticle generation in SCD. Blood 124, 1941–1950.10.1182/blood-2014-01-543652Search in Google Scholar PubMed PubMed Central

Azarov, I., Huang, K.T., Basu, S., Gladwin, M.T., Hogg, N., and Kim-Shapiro, D.B. (2005). Nitric oxide scavenging by red blood cells as a function of hematocrit and oxygenation. J. Biol. Chem. 280, 39024–39032.10.1074/jbc.M509045200Search in Google Scholar PubMed

Baek, J.H., D’Agnillo, F., Vallelian, F., Pereira, C.P., Williams, M.C., Jia, Y., Schaer, D.J., and 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. J. Clin. Invest. 122, 1444–1458.10.1172/JCI59770Search in Google Scholar PubMed PubMed Central

Baron, D.M., Yu, B., Lei, C., Bagchi, A., Beloiartsev, A., Stowell, C.P., Steinbicker, A.U., Malhotra, R., Bloch, K.D., and Zapol, W.M. (2012). Pulmonary hypertension in lambs transfused with stored blood is prevented by breathing nitric oxide. Anesthesiology 116, 637–647.10.1097/ALN.0b013e318246ef77Search in Google Scholar PubMed PubMed Central

Belizaire, R.M., Makley, A.T., Campion, E.M., Sonnier, D.I., Goodman, M.D., Dorlac, W.C., Friend, L.A., Lentsch, A.B., and Pritts, T.A. (2012a). Resuscitation with washed aged packed red blood cell units decreases the proinflammatory response in mice after hemorrhage. J. Trauma Acute Care Surg. 73, S128–S133.10.1097/TA.0b013e3182606301Search in Google Scholar PubMed PubMed Central

Belizaire, R.M., Prakash, P.S., Richter, J.R., Robinson, B.R., Edwards, M.J., Caldwell, C.C., Lentsch, A.B., and Pritts, T.A. (2012b). Microparticles from stored red blood cells activate neutrophils and cause lung injury after hemorrhage and resuscitation. J. Am. Coll. Surg. 214, 648–655; discussion 656–657.10.1016/j.jamcollsurg.2011.12.032Search in Google Scholar PubMed PubMed Central

Bennett-Guerrero, E., Veldman, T.H., Doctor, A., Telen, M.J., Ortel, T.L., Reid, T.S., Mulherin, M.A., Zhu, H., Buck, R.D., Califf, R.M., et al. (2007). Evolution of adverse changes in stored RBCs. Proc. Natl. Acad. Sci. USA 104, 17063–17068.10.1073/pnas.0708160104Search in Google Scholar

Berezina, T.L., Zaets, S.B., Morgan, C., Spillert, C.R., Kamiyama, M., Spolarics, Z., Deitch, E.A., and Machiedo, G.W. (2002). Influence of storage on red blood cell rheological properties. J. Surg. Res. 102, 6–12.10.1006/jsre.2001.6306Search in Google Scholar

Bicalho, B., Holovati, J.L., and Acker, J.P. (2013). Phospholipidomics reveals differences in glycerophosphoserine profiles of hypothermically stored red blood cells and microvesicles. Biochim. Biophys. Acta 1828, 317–326.10.1016/j.bbamem.2012.10.026Search in Google Scholar

Blumberg, N., Zhao, H., Wang, H., Messing, S., Heal, J.M., and Lyman, G.H. (2007). The intention-to-treat principle in clinical trials and meta-analyses of leukoreduced blood transfusions in surgical patients. Transfusion 47, 573–581.10.1111/j.1537-2995.2007.01158.xSearch in Google Scholar

Bosman, G.J., Lasonder, E., Groenen-Döpp, Y.A., Willekens, F.L., and Werre, J.M. (2012). The proteome of erythrocyte-derived microparticles from plasma: new clues for erythrocyte aging and vesiculation. J. Proteomics 76, 203–210.10.1016/j.jprot.2012.05.031Search in Google Scholar

Brakenridge, S.C., Phelan, H.A., Henley, S.S., Golden, R.M., Kashner, T.M., Eastman, A.E., Sperry, J.L., Harbrecht, B.G., Moore, E.E, Cuschieri, J., et al. (2011). Early blood product and crystalloid volume resuscitation: risk association with multiple organ dysfunction after severe blunt traumatic injury. J. Trauma 71, 299–305.10.1097/TA.0b013e318224d328Search in Google Scholar

Brown, C.H., Grega, M., Selnes, O.A., McKhann, G.M., Shah, A.S., LaFlam, A., Savage, W.J., Frank, S.M., Hogue, C.W., and Gottesman, R.F. (2014). Length of red cell unit storage and risk for delirium after cardiac surgery. Anesth. Analg. 119, 242–250.10.1213/ANE.0000000000000134Search in Google Scholar

Cancelas, J.A., Dumont, L.J., Maes, L.A., Rugg, N., Herschel, L., Whitley, P.H., Szczepiokowski, Z.M., Siegel, A.H., Hess, J.R., and Zia, M. (2014). Additive solution-7 reduces the red blood cell cold storage lesion. Transfusion 55, 491–498.10.1111/trf.12867Search in Google Scholar

Capraro, L., Kuitunen, A., Vento, A.E., Suojaranta-Ylinen, R., Kolho, E., and Pettilä, V. (2007). Universal leukocyte reduction of transfused red cells does not provide benefit to patients undergoing cardiac surgery. J. Cardiothorac. Vasc. Anesth. 21, 232–236.10.1053/j.jvca.2006.07.013Search in Google Scholar

Card, R.T. (1988). Red cell membrane changes during storage. Transfus Med Rev. 2, 40–47.10.1016/S0887-7963(88)70030-9Search in Google Scholar

Cleemput, I., Leys, M., Ramaekers, D., and Bonneux, L. (2006). Balancing evidence and public opinion in health technology assessments: the case of leukoreduction. Int. J. Technol. Assess. Health Care 22, 403–407.10.1017/S0266462306051312Search in Google Scholar

Cohen, M.H. (1981). Influence of tumor burden on red blood cell deformability in small cell lung cancer patients. Ann. Clin. Res. 13, 387–391.Search in Google Scholar

Corwin, H.L., Gettinger, A., Pearl, R.G., Fink, M.P., Levy, M.M., Abraham, E., MacIntyre, N.R., Shabot, M.M., Duh, M.S., Shapiro, M.J. (2004). The CRIT Study: anemia and blood transfusion in the critically ill–current clinical practice in the United States. Crit. Care Med. 32, 39–52.10.1097/01.CCM.0000104112.34142.79Search in Google Scholar

Dinkla, S., Wessels, K., Verdurmen, W.P., Tomelleri, C., Cluitmans, J.C., Fransen, J., Fuchs, B., Schiller, J., Joosten, I., Brock, R., et al. (2012). Functional consequences of sphingomyelinase-induced changes in erythrocyte membrane structure. Cell Death Dis. 3, e410.10.1038/cddis.2012.143Search in Google Scholar

Donadee, C., Raat, N.J., Kanias, T., Tejero, J., Lee, J.S., Kelley, E.E., Zhao, X., Liu, C., Reynolds, H., Azarov, I., et al. (2011). Nitric oxide scavenging by red blood cell microparticles and cell-free hemoglobin as a mechanism for the red cell storage lesion. Circulation 124, 465–476.10.1161/CIRCULATIONAHA.110.008698Search in Google Scholar

Dumaswala, U.J., Zhuo, L., Jacobsen, D.W., Jain, S.K., and Sukalski, K.A. (1999). Protein and lipid oxidation of banked human erythrocytes: role of glutathione. Free Radic. Biol. Med. 27, 1041–1049.10.1016/S0891-5849(99)00149-5Search in Google Scholar

Dumont, L.J. and AuBuchon, J.P. (2008). Evaluation of proposed FDA criteria for the evaluation of radiolabeled red cell recovery trials. Transfusion 48, 1053–1060.10.1111/j.1537-2995.2008.01642.xSearch in Google Scholar PubMed

Fergusson, D., Khanna, M.P., Tinmouth, A., and Hébert, P.C. (2004). Transfusion of leukoreduced red blood cells may decrease postoperative infections: two meta-analyses of randomized controlled trials. Can. J. Anaesth. 51, 417–424.10.1007/BF03018302Search in Google Scholar PubMed

Ferraris, V.A., Brown, J.R., Despotis, G.J., Hammon, J.W., Reece, T.B., Saha, S.P., Song, H.K., Clough, E.R., Shore-Lesserson, L.J., Goodnough, L.T., et al. (2011). 2011 update to the Society of Thoracic Surgeons and the Society of Cardiovascular Anesthesiologists blood conservation clinical practice guidelines. Ann. Thorac. Surg. 91, 944–982.10.1016/j.athoracsur.2010.11.078Search in Google Scholar PubMed

Flatt, J.F., Bawazir, W.M., and Bruce, L.J. (2014). The involvement of cation leaks in the storage lesion of red blood cells. Front Physiol. 5, 214.10.3389/fphys.2014.00214Search in Google Scholar PubMed PubMed Central

Friese, R.S., Sperry, J.L., Phelan, H.A., and Gentilello, L.M. (2008). The use of leukoreduced red blood cell products is associated with fewer infectious complications in trauma patients. Am. J. Surg. 196, 56–61.10.1016/j.amjsurg.2007.08.063Search in Google Scholar PubMed

Frietsch, T., Karger, R., Schöler, M., Huber, D., Bruckner, T., Kretschmer, V., Schmidt, S., Leidinger, W., and Weiler-Lorentz, A. (2008). Leukodepletion of autologous whole blood has no impact on perioperative infection rate and length of hospital stay. Transfusion 48, 2133–2142.10.1111/j.1537-2995.2008.01804.xSearch in Google Scholar PubMed

Fung, M.K., Moore, K., Ridenour, M., Mook, W., and Triulzi, D.J. (2006). Clinical effects of reverting from leukoreduced to nonleukoreduced blood in cardiac surgery. Transfusion 46, 386–91.10.1111/j.1537-2995.2006.00733.xSearch in Google Scholar PubMed

Gao, Y., Lv, L., Liu, S., Ma, G., and Su, Y. (2013). Elevated levels of thrombin-generating microparticles in stored red blood cells. Vox Sang. 105, 11–17.10.1111/vox.12014Search in Google Scholar PubMed

Gong, M.N., Thompson, B.T., Williams, P., Pothier, L., Boyce, P.D. and Christiani, D.C. (2005). Clinical predictors of and mortality in acute respiratory distress syndrome: potential role of red cell transfusion. Crit. Care Med. 33, 1191–1198.10.1097/01.CCM.0000165566.82925.14Search in Google Scholar

Greenwalt, T.J., Bryan, D.J., and Dumaswala, U.J. (1984). Erythrocyte membrane vesiculation and changes in membrane composition during storage in citrate-phosphate-dextrose-adenine-1. Vox. Sang. 47, 261–270.10.1111/j.1423-0410.1984.tb01596.xSearch in Google Scholar PubMed

Greenwalt, T.J., McGuinness, C.G., and Dumaswala, U.J. (1991). Studies in red blood cell preservation: 4. Plasma vesicle hemoglobin exceeds free hemoglobin. Vox. Sang. 61, 14–17.10.1111/j.1423-0410.1991.tb00920.xSearch in Google Scholar PubMed

Haradin, A.R., Weed, R.I., and Reed, C.F. (1969). Changes in physical properties of stored erythrocytes relationship to survival in vivo. Transfusion 9, 229–237.10.1111/j.1537-2995.1969.tb04929.xSearch in Google Scholar PubMed

Hatakeyama, T., Sato, T., Taira, E., Kuwahara, H., Niidome, T., and Aoyagi, H. (1999). Characterization of the interaction of hemolytic lectin CEL-III from the marine invertebrate, Cucumaria echinata, with artificial lipid membranes: involvement of neutral sphingoglycolipids in the pore-forming process. J. Biochem. 125, 277–284.10.1093/oxfordjournals.jbchem.a022284Search in Google Scholar PubMed

Hébert, P.C., Wells, G., Blajchman, M.A., Marshall, J., Martin, C., Pagliarello, G., Tweeddale, M., Schweitzer, I., Yetisir, E. (1999). 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, 409–417.10.1056/NEJM199902113400601Search in Google Scholar PubMed

Hébert, P.C., Fergusson, D., Blajchman, M.A., Wells, G.A., Kmetic, A., Coyle, D., Heddle, N., Germain, M., Goldman, M., Toye, B., et al. (2003). Clinical outcomes following institution of the Canadian universal leukoreduction program for red blood cell transfusions. J. Am. Med. Assoc. 289, 1941–1949.10.1001/jama.289.15.1941Search in Google Scholar PubMed

Hess, J.R. (2010a). Conventional blood banking and blood component storage regulation: opportunities for improvement. Blood Transfus. 8 (Suppl. 3), s9–15.Search in Google Scholar

Hess, J.R. (2010b). Red cell changes during storage. Transfus. Apher. Sci. 43, 51–59.10.1016/j.transci.2010.05.009Search in Google Scholar PubMed

Hod, E.A., Zhang, N., Sokol, S.A., Wojczyk, B.S., Francis, R.O., Ansaldi, D., Francis, K.P., Della-Latta, P., Whittier, S., Sheth, S., et al. (2010). Transfusion of red blood cells after prolonged storage produces harmful effects that are mediated by iron and inflammation. Blood 115, 4284–4292.10.1182/blood-2009-10-245001Search in Google Scholar PubMed PubMed Central

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., et al. (2011). Transfusion of human volunteers with older, stored red blood cells produces extravascular hemolysis and circulating non-transferrin-bound iron. Blood 118, 6675–6682.10.1182/blood-2011-08-371849Search in Google Scholar PubMed PubMed Central

Holcomb, J.B. and Pati, S. (2013). Optimal trauma resuscitation with plasma as the primary resuscitative fluid: the surgeon’s perspective. Hematology Am. Soc. Hematol. Educ. Program 2013, 656–659.10.1182/asheducation-2013.1.656Search in Google Scholar PubMed

Holcomb, J.B., Jenkins, D., Rhee, P., Johannigman, J., Mahoney, P., Mehta, S., Cox, E.D., Gehrke, M.J., Beilman, G.J., Schreiber, M., et al. (2007). Damage control resuscitation: directly addressing the early coagulopathy of trauma. J. Trauma 62, 307–310.10.1097/TA.0b013e3180324124Search in Google Scholar PubMed

Holcomb, J.B., del Junco, D.J., Fox, E.E., Wade, C.E., Cohen, M.J., Schreiber, M.A., Alarcon, L.H., Bai, Y., Brasel, K.J., Bulger, E.M., et al. (2013). The prospective, observational, multicenter, major trauma transfusion (PROMMTT) study: comparative effectiveness of a time-varying treatment with competing risks. J. Am. Med. Assoc. Surg. 148, 127–136.10.1001/2013.jamasurg.387Search in Google Scholar PubMed PubMed Central

Holst, L.B., Haase, N., Wetterslev, J., Wernerman, J., Guttormsen, A.B., Karlsson, S., Johansson, P.I., Aneman, A., Marianne, L., Vang, M.D., et al. (2014). Lower versus higher hemoglobin threshold for transfusion in septic shock. N. Engl. J. Med. 371, 1381–1391.10.1056/NEJMoa1406617Search in Google Scholar PubMed

Horvath, K.A., Acker, M.A., Chang, H., Bagiella, E., Smith, P.K., Iribarne, A., Kron, I.L., Lackner, P., Argenziano, M., Ascheim, D.D., et al. (2013). Blood transfusion and infection after cardiac surgery. Ann. Thorac. Surg. 95, 2194–2201.10.1016/j.athoracsur.2012.11.078Search in Google Scholar PubMed PubMed Central

Hu, X., Patel, R.P., Weinberg, J.A., Marques, M.B., Ramos, T.N., and Barnum, S.R. (2014). Membrane attack complex generation increases as a function of time in stored blood. Transfus. Med. 24, 114–116.10.1111/tme.12109Search in Google Scholar PubMed PubMed Central

Izzo, P., Manicone, A., Spagnuolo, A., Lauta, V.M., Di Pasquale, A., and Di Monte, D. (1999). Erythrocytes stored in CPD SAG-mannitol: evaluation of their deformability. Clin. Hemorheol. Microcirc. 21, 335–339.Search in Google Scholar

Jy, W., Johansen, M.E., Bidot, C., Horstman, L.L., and Ahn, Y.S. (2013). Red cell-derived microparticles (RMP) as haemostatic agent. Thromb Haemost. 110, 751–760.10.1160/TH12-12-0941Search in Google Scholar PubMed

Karon, B.S., Hoyer, J.D., Stubbs, J.R., and Thomas, D.D. (2009). Changes in Band 3 oligomeric state precede cell membrane phospholipid loss during blood bank storage of red blood cells. Transfusion 49, 1435–1442.10.1111/j.1537-2995.2009.02133.xSearch in Google Scholar PubMed PubMed Central

Kauvar, D.S., Lefering, R. and Wade, C.E. (2006). Impact of hemorrhage on trauma outcome: an overview of epidemiology, clinical presentations, and therapeutic considerations. J. Trauma 60, S3–11.10.1097/01.ta.0000199961.02677.19Search in Google Scholar PubMed

Khan, F.A., Fisher, M.A., and Khakoo, R.A. (2007). Association of hemochromatosis with infectious diseases: expanding spectrum. Int. J. Infect. Dis. 11, 482–487.10.1016/j.ijid.2007.04.007Search in Google Scholar PubMed

King, K.E., Shirey, R.S., Thoman, S.K., Bensen-Kennedy, D., Tanz, W.S., and Ness, P.M. (2004). Universal leukoreduction decreases the incidence of febrile nonhemolytic transfusion reactions to RBCs. Transfusion 44, 25–29.10.1046/j.0041-1132.2004.00609.xSearch in Google Scholar PubMed

Klug, P.P., Lessin, L.S., and Radice, P. (1974). Rheological aspects of sickle cell disease. Arch. Intern. Med. 133, 577–590.10.1001/archinte.1974.00320160071007Search in Google Scholar

Koch, C.G., Figueroa, P.I., Li, L., Sabik, J.F., Mihaljevic, T., and Blackstone, E.H. (2013). Red blood cell storage: how long is too long? Ann. Thorac. Surg. 96, 1894–1899.10.1016/j.athoracsur.2013.05.116Search in Google Scholar PubMed

Koch, C.G., Li, L., Sessler, D.I., Figueroa, P., Hoeltge, G.A., Mihaljevic, T., and Blackstone, E.H. (2008). Duration of red-cell storage and complications after cardiac surgery. N. Engl. J. Med. 358, 1229–1239.10.1056/NEJMoa070403Search in Google Scholar PubMed

Koshiar, R.L., Somajo, S., Norström, E., and Dahlbäck, B. (2014). Erythrocyte-derived microparticles supporting activated protein C-mediated regulation of blood coagulation. PLoS One 9, e104200.Search in Google Scholar

Kriebardis, A.G., Antonelou, M.H., Stamoulis, K.E., Economou-Petersen, E., Margaritis, L.H., and Papassideri, I.S. (2007). Storage-dependent remodeling of the red blood cell membrane is associated with increased immunoglobulin G binding, lipid raft rearrangement, and caspase activation. Transfusion 47, 1212–1220.10.1111/j.1537-2995.2007.01254.xSearch in Google Scholar PubMed

Kriebardis, A.G., Antonelou, M.H., Stamoulis, K.E., Economou-Petersen, E., Margaritis, L.H., and Papassideri, I.S. (2008). RBC-derived vesicles during storage: ultrastructure, protein composition, oxidation, and signaling components. Transfusion 48, 1943–1953.10.1111/j.1537-2995.2008.01794.xSearch in Google Scholar PubMed

Lacroix, R., Robert, S., Poncelet, P., and Dignat-George, F. (2010). Overcoming limitations of microparticle measurement by flow cytometry. Semin. Thromb. Hemost. 36, 807–818.10.1055/s-0030-1267034Search in Google Scholar PubMed

Lawrie, A.S., Albanyan, A., Cardigan, R.A., Mackie, I.J., and Harrison, P. (2009). Microparticle sizing by dynamic light scattering in fresh-frozen plasma. Vox Sang. 96, 206–12.10.1111/j.1423-0410.2008.01151.xSearch in Google Scholar PubMed

Liu, C., Zhao, W., Christ, G.J., Gladwin, M.T., and Kim-Shapiro, D.B. (2013). Nitric oxide scavenging by red cell microparticles. Free Radic. Biol. Med. 65, 1164–1173.10.1016/j.freeradbiomed.2013.09.002Search in Google Scholar PubMed PubMed Central

Llewelyn, C.A., Taylor, R.S., Todd, A.A., Stevens, W., Murphy, M.F., Williamson, L.M., and Group, L.S. (2004). The effect of universal leukoreduction on postoperative infections and length of hospital stay in elective orthopedic and cardiac surgery. Transfusion 44, 489–500.10.1111/j.1537-2995.2004.03325.xSearch in Google Scholar PubMed

Lutz, H.U., Liu, S.C., and Palek, J. (1977). Release of spectrin-free vesicles from human erythrocytes during ATP depletion. I. Characterization of spectrin-free vesicles. J. Cell Biol. 73, 548–560.10.1083/jcb.73.3.548Search in Google Scholar PubMed PubMed Central

Mahfoudhi, E., Lecluse, Y., Driss, F., Abbes, S., Flaujac, C., and Garçon, L. (2012). Red cells exchanges in sickle cells disease lead to a selective reduction of erythrocytes-derived blood microparticles. Br. J. Haematol. 156, 545–547.10.1111/j.1365-2141.2011.08897.xSearch in Google Scholar PubMed

Makley, A.T., Goodman, M.D., Friend, L.A., Deters, J.S., Johannigman, J.A., Dorlac, W.C., Lentsch, A.B., and Pritts, T.A. (2010a). Resuscitation with fresh whole blood ameliorates the inflammatory response after hemorrhagic shock. J. Trauma 68, 305–311.10.1097/TA.0b013e3181cb4472Search in Google Scholar PubMed PubMed Central

Makley, A.T., Goodman, M.D., Friend, L.A., Johannigman, J.A., Dorlac, W.C., Lentsch, A.B., and Pritts, T.A. (2010b). Murine blood banking: characterization and comparisons to human blood. Shock 34, 40–45.10.1097/SHK.0b013e3181d494fdSearch in Google Scholar PubMed PubMed Central

Mangalmurti, N.S., Xiong, Z., Hulver, M., Ranganathan, M., Liu, X.H., Oriss, T., Fitzpatrick, M., Rubin, M., Triulzi, D., Choi, A., et al. (2009). Loss of red cell chemokine scavenging promotes transfusion-related lung inflammation. Blood 113, 1158–1166.10.1182/blood-2008-07-166264Search in Google Scholar PubMed PubMed Central

Matot, I., Katz, M., Pappo, O., Zelig, O., Corchia, N., Yedgar, S., Barshtein, G., Bennett-Guerrero, E., and Abramovitch, R. (2013). Resuscitation with aged blood exacerbates liver injury in a hemorrhagic rat model. Crit. Care Med. 41, 842–849.10.1097/CCM.0b013e3182711b38Search in Google Scholar PubMed

Mynster, T. and Nielsen, H.J. (2000). The impact of storage time of transfused blood on postoperative infectious complications in rectal cancer surgery. Danish RANX05 Colorectal Cancer Study Group. Scand. J. Gastroenterol. 35, 212–217.10.1080/003655200750024416Search in Google Scholar PubMed

Nagura, Y., Tsuno, N.H., Tanaka, M., Matsuhashi, M., and Takahashi, K. (2013). The effect of pre-storage whole-blood leukocyte reduction on cytokines/chemokines levels in autologous CPDA-1 whole blood. Transfus. Apher. Sci. 49, 223–230.10.1016/j.transci.2013.01.006Search in Google Scholar PubMed

Nathens, A.B., Nester, T.A., Rubenfeld, G.D., Nirula, R., and Gernsheimer, T.B. (2006). The effects of leukoreduced blood transfusion on infection risk following injury: a randomized controlled trial. Shock 26, 342–347.10.1097/01.shk.0000228171.32587.a1Search in Google Scholar PubMed

Neuman, R., Hayek, S., Rahman, A., Poole, J.C., Menon, V., Sher, S., Newman, J.L., Karatela, S., Polhemus, D., Lefer, D.J., et al. (2014). Effects of storage-aged red blood cell transfusions on endothelial function in hospitalized patients. Transfusion Nov 13, doi: 10.1111/trf.12919. [Epub ahead of print].10.1111/trf.12919Search in Google Scholar PubMed PubMed Central

Offner, P.J., Moore, E.E., Biffl, W.L., Johnson, J.L., and Silliman, C.C. (2002). Increased rate of infection associated with transfusion of old blood after severe injury. Arch. Surg. 137, 711–6; discussion 716–717.10.1001/archsurg.137.6.711Search in Google Scholar PubMed

Ozment, C.P. and Turi, J.L. (2009). Iron overload following red blood cell transfusion and its impact on disease severity. Biochim. Biophys. Acta 1790, 694–701.10.1016/j.bbagen.2008.09.010Search in Google Scholar PubMed

Palmer, R.M., Ferrige, A.G., and Moncada, S. (1987). Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327, 524–526.10.1038/327524a0Search in Google Scholar PubMed

Phelan, H.A., Sperry, J.L., and Friese, R.S. (2007). Leukoreduction before red blood cell transfusion has no impact on mortality in trauma patients. J. Surg. Res. 138, 32–36.10.1016/j.jss.2006.07.048Search in Google Scholar PubMed

Plurad, D., Belzberg, H., Schulman, I., Green, D., Salim, A., Inaba, K., Rhee, P., and Demetriades, D. (2008). Leukoreduction is associated with a decreased incidence of late onset acute respiratory distress syndrome after injury. Am. Surg. 74, 117–123.10.1177/000313480807400205Search in Google Scholar

Purdy, F.R., Tweeddale, M.G., and Merrick, P.M. (1997). Association of mortality with age of blood transfused in septic ICU patients. Can. J. Anaesth. 44, 1256–1261.10.1007/BF03012772Search in Google Scholar PubMed

Relevy, H., Koshkaryev, A., Manny, N., Yedgar, S., and Barshtein, G. (2008). Blood banking-induced alteration of red blood cell flow properties. Transfusion 48, 136–146.Search in Google Scholar

Reynolds, J.D., Ahearn, G.S., Angelo, M., Zhang, J., Cobb, F., and Stamler, J.S. (2007). S-nitrosohemoglobin deficiency: a mechanism for loss of physiological activity in banked blood. Proc. Natl. Acad. Sci. USA 104, 17058–17062.10.1073/pnas.0707958104Search in Google Scholar PubMed PubMed Central

Rigamonti, A., McLaren, A.T., Mazer, C.D., Nix, K., Ragoonanan, T., Freedman, J., Harrington, A., and Hare, G.M. (2008). Storage of strain-specific rat blood limits cerebral tissue oxygen delivery during acute fluid resuscitation. Br. J. Anaesth. 100, 357–364.10.1093/bja/aem401Search in Google Scholar PubMed

Robertson, C.S., Hannay, H.J., Yamal, J.M., Gopinath, S., Goodman, J.C., Tilley, B.C., Baldwin, A., Rivera Lara, L., Saucedo-Crespo, H., Ahmed, O., et al. (2014). Effect of erythropoietin and transfusion threshold on neurological recovery after traumatic brain injury: a randomized clinical trial. J. Am. Med. Assoc. 312, 36–47.10.1001/jama.2014.6490Search in Google Scholar PubMed PubMed Central

Salzer, U., Zhu, R., Luten, M., Isobe, H., Pastushenko, V., Perkmann, T., Hinterdorfer, P., and Bosman, G.J. (2008). Vesicles generated during storage of red cells are rich in the lipid raft marker stomatin. Transfusion 48, 451–462.10.1111/j.1537-2995.2007.01549.xSearch in Google Scholar PubMed

Sauaia, A., Moore, F.A., Moore, E.E., Haenel, J.B., Read, R.A., and Lezotte, D.C. (1994). Early predictors of postinjury multiple organ failure. Arch. Surg. 129, 39–45.10.1001/archsurg.1994.01420250051006Search in Google Scholar PubMed

Schorn, M.N. and Phillippi, J.C. (2014). Volume replacement following severe postpartum hemorrhage. J. Midwifery Womens Health 59, 336–343.10.1111/jmwh.12186Search in Google Scholar PubMed

Seghatchian, J. (2006). Platelet storage lesion: an update on the impact of various leukoreduction processes on the biological response modifiers. Transfus. Apher. Sci. 34, 125–130.10.1016/j.transci.2005.09.002Search in Google Scholar PubMed

Şekeroğlu, M.R., Huyut, Z., and Him, A. (2012). The susceptibility of erythrocytes to oxidation during storage of blood: effects of melatonin and propofol. Clin. Biochem. 45, 315–9.10.1016/j.clinbiochem.2011.12.021Search in Google Scholar PubMed

Shapiro, M.J., Gettinger, A., Corwin, H.L., Napolitano, L., Levy, M., Abraham, E., Fink, M.P., MacIntyre, N., Pearl, R.G., and Shabot, M.M. (2003). Anemia and blood transfusion in trauma patients admitted to the intensive care unit. J. Trauma 55, 269–273; discussion 273–274.10.1097/01.TA.0000080530.77566.04Search in Google Scholar PubMed

Sharma, A.D., Slaughter, T.F., Clements, F.M., Sreeram, G., Newman, M.F., Phillips-Bute, B., Bredehoeft, S.J., Smith, P.K., and Stafford-Smith, M. (2002). Association of leukocyte-depleted blood transfusions with infectious complications after cardiac surgery. Surg. Infect. (Larchmt) 3, 127–133.10.1089/109629602760105790Search in Google Scholar PubMed

Silliman, C.C., Voelkel, N.F., Allard, J.D., Elzi, D.J., Tuder, R.M., Johnson, J.L. and Ambruso, D.R. (1998). Plasma and lipids from stored packed red blood cells cause acute lung injury in an animal model. J. Clin. Invest. 101, 1458–1467.10.1172/JCI1841Search in Google Scholar PubMed PubMed Central

Solheim, B.G., Flesland, O., Brosstad, F., Mollnes, T.E., and Seghatchian, J. (2003). Improved preservation of coagulation factors after pre-storage leukocyte depletion of whole blood. Transfus. Apher. Sci. 29, 133–139.10.1016/S1473-0502(03)00117-4Search in Google Scholar

Solheim, B.G., Flesland, O., Seghatchian, J., and Brosstad, F. (2004). Clinical implications of red blood cell and platelet storage lesions: an overview. Transfus. Apher. Sci. 31, 185–189.10.1016/j.transci.2004.09.004Search in Google Scholar

Sowemimo-Coker, S.O. (2014). Evaluation of an experimental filter designed for improving the quality of red blood cells (RBCs) during storage by simultaneously removing white blood cells and immunomodulators and improving RBC viscoelasticity and Band 3 proteins. Transfusion 54, 592–601.10.1111/trf.12330Search in Google Scholar

Sparrow, R.L. (2012). Time to revisit red blood cell additive solutions and storage conditions: a role for “omics” analyses. Blood Transfus. 10 (Suppl. 2), s7–11.Search in Google Scholar

Spinella, P.C., Carroll, C.L., Staff, I., Gross, R., Mc Quay, J., Keibel, L., Wade, C.E., and 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. Crit. Care 13, R151.10.1186/cc8050Search in Google Scholar

Stadler, A. and Linderkamp, O. (1989). Flow behavior of neonatal and adult erythrocytes in narrow capillaries. Microvasc. Res. 37, 267–279.10.1016/0026-2862(89)90045-9Search in Google Scholar

Stowell, S.R., Winkler, A.M., Maier, C.L., Arthur, C.M., Smith, N.H., Girard-Pierce, K.R., Cummings, R.D., Zimring, J.C., and Hendrickson, J.E. (2012). Initiation and regulation of complement during hemolytic transfusion reactions. Clin. Dev. Immunol. 2012, 307093.10.1155/2012/307093Search in Google Scholar PubMed PubMed Central

Sweeney, J., Kouttab, N., and Kurtis, J. (2009). Stored red blood cell supernatant facilitates thrombin generation. Transfusion 49, 1569–1579.10.1111/j.1537-2995.2009.02196.xSearch in Google Scholar PubMed

Tsai, A.G., Cabrales, P., and Intaglietta, M. (2004). Microvascular perfusion upon exchange transfusion with stored red blood cells in normovolemic anemic conditions. Transfusion 44, 1626–1634.10.1111/j.0041-1132.2004.04128.xSearch in Google Scholar PubMed

Tsukada, K., Sekizuka, E., Oshio, C., and Minamitani, H. (2001). Direct measurement of erythrocyte deformability in diabetes mellitus with a transparent microchannel capillary model and high-speed video camera system. Microvasc. Res. 61, 231–239.10.1006/mvre.2001.2307Search in Google Scholar PubMed

van de Watering, L.M., Hermans, J., Houbiers, J.G., van den Broek, P.J., Bouter, H., Boer, F., Harvey, M.S., Huysmans, H.A., and Brand, A. (1998). Beneficial effects of leukocyte depletion of transfused blood on postoperative complications in patients undergoing cardiac surgery: a randomized clinical trial. Circulation 97, 562–568.10.1161/01.CIR.97.6.562Search in Google Scholar PubMed

Van Der Meijden, P.E., Van Schilfgaarde, M., Van Oerle, R., Renné, T., ten Cate, H., and Spronk, H.M. (2012). Platelet- and erythrocyte-derived microparticles trigger thrombin generation via factor XIIa. J. Thromb. Haemost. 10, 1355–1362.10.1111/j.1538-7836.2012.04758.xSearch in Google Scholar PubMed

van Hulst, M., Bilgin, Y.M., van de Watering, L.M., de Vries, R., van Oers, M.H., Brand, A., and Postma, M.J. (2005). Cost-effectiveness of leucocyte-depleted erythrocyte transfusion in cardiac valve surgery. Transfus. Med. 15, 209–217.10.1111/j.1365-3148.2005.00573.xSearch in Google Scholar PubMed

Vaughn, M.W., Huang, K.T., Kuo, L., and Liao, J.C. (2000). Erythrocytes possess an intrinsic barrier to nitric oxide consumption. J. Biol. Chem. 275, 2342–2348.10.1074/jbc.275.4.2342Search in Google Scholar PubMed

Vincent, J.L., Baron, J.F., Reinhart, K., Gattinoni, L., Thijs, L., Webb, A., Meier-Hellmann, A., Nollet, G., Peres-Bota, D. (2002). Anemia and blood transfusion in critically ill patients. J. Am. Med. Assoc. 288, 1499–1507.10.1001/jama.288.12.1499Search in Google Scholar PubMed

Vlaar, A.P., Hofstra, J.J., Levi, M., Kulik, W., Nieuwland, R., Tool, A.T., Schultz, M.J., de Korte, D., and Juffermans, N.P. (2010). Supernatant of aged erythrocytes causes lung inflammation and coagulopathy in a “two-hit” in vivo syngeneic transfusion model. Anesthesiology 113, 92–103.10.1097/ALN.0b013e3181de6f25Search in Google Scholar PubMed

Wagner, G.M., Chiu, D.T., Qju, J.H., Heath, R.H., and Lubin, B.H. (1987). Spectrin oxidation correlates with membrane vesiculation in stored RBCs. Blood 69, 1777–1781.10.1182/blood.V69.6.1777.1777Search in Google Scholar

Walford, G. and Loscalzo, J. (2003). Nitric oxide in vascular biology. J. Thromb. Haemost. 1, 2112–2118.10.1046/j.1538-7836.2003.00345.xSearch in Google Scholar PubMed

Wallis, J.P., Chapman, C.E., Orr, K.E., Clark, S.C., and Forty, J.R. (2002). Effect of WBC reduction of transfused RBCs on postoperative infection rates in cardiac surgery. Transfusion 42, 1127–1134.10.1046/j.1537-2995.2002.00181.xSearch in Google Scholar PubMed

Watkins, T.R., Rubenfeld, G.D., Martin, T.R., Nester, T.A., Caldwell, E., Billgren, J., Ruzinski, J., and Nathens, A.B. (2008). Effects of leukoreduced blood on acute lung injury after trauma: a randomized controlled trial. Crit. Care Med. 36, 1493–1499.10.1097/CCM.0b013e318170a9ceSearch in Google Scholar PubMed

Wehrli, G. (2012). Blood banking and transfusion medicine for the nephrologist. Semin. Dial. 25, 114–118.10.1111/j.1525-139X.2011.01021.xSearch in Google Scholar PubMed

Weinberg, J.A., McGwin, G., Marques, M.B., Cherry, S.A., Reiff, D.A., Kerby, J.D., and Rue, L.W. (2008). Transfusions in the less severely injured: does age of transfused blood affect outcomes? J. Trauma 65, 794–798.Search in Google Scholar

Weinberg, J.A., McGwin, G., Vandromme, M.J., Marques, M.B., Melton, S.M., Reiff, D.A., Kerby, J.D., and Rue, L.W. (2010). Duration of red cell storage influences mortality after trauma. J Trauma 69, 1427–31; discussion 1431–1432.10.1097/TA.0b013e3181fa0019Search in Google Scholar

Weinberg, J.A., Barnum, S.R., and Patel, R.P. (2011). Red blood cell age and potentiation of transfusion-related pathology in trauma patients. Transfusion 51, 867–873.10.1111/j.1537-2995.2011.03098.xSearch in Google Scholar

Westerman, M., Pizzey, A., Hirschman, J., Cerino, M., Weil-Weiner, Y., Ramotar, P., Eze, A., Lawrie, A., Purdy, G., Mackie, I., et al. (2008). Microvesicles in haemoglobinopathies offer insights into mechanisms of hypercoagulability, haemolysis and the effects of therapy. Br. J. Haematol. 142, 126–135.10.1111/j.1365-2141.2008.07155.xSearch in Google Scholar

Willekens, F.L., Werre, J.M., Groenen-Döpp, Y.A., Roerdinkholder-Stoelwinder, B., de Pauw, B., and Bosman, G.J. (2008). Erythrocyte vesiculation: a self-protective mechanism? Br. J. Haematol. 141, 549–556.10.1111/j.1365-2141.2008.07055.xSearch in Google Scholar

Wolfe, L.C., Byrne, A.M., and Lux, S.E. (1986). Molecular defect in the membrane skeleton of blood bank-stored red cells. Abnormal spectrin-protein 4.1-actin complex formation. J. Clin. Invest. 78, 1681–1686.10.1172/JCI112762Search in Google Scholar

Xiong, Z., Cavaretta, J., Qu, L., Stolz, D.B., Triulzi, D., and Lee, J.S. (2011). Red blood cell microparticles show altered inflammatory chemokine binding and release ligand upon interaction with platelets. Transfusion 51, 610–621.10.1111/j.1537-2995.2010.02861.xSearch in Google Scholar

Yuana, Y., Bertina, R.M., and Osanto, S. (2011). Pre-analytical and analytical issues in the analysis of blood microparticles. Thromb. Haemost. 105, 396–408.10.1160/TH10-09-0595Search in Google Scholar

Zallen, G., Offner, P.J., Moore, E.E., Blackwell, J., Ciesla, D.J., Gabriel, J., Denny, C., and Silliman, C.C. (1999). Age of transfused blood is an independent risk factor for postinjury multiple organ failure. Am. J. Surg. 178, 570–572.10.1016/S0002-9610(99)00239-1Search in Google Scholar

Zecher, D., Cumpelik, A., and Schifferli, J.A. (2014). Erythrocyte-derived microvesicles amplify systemic inflammation by thrombin-dependent activation of complement. Arterioscler. Thromb. Vasc. Biol. 34, 313–320.10.1161/ATVBAHA.113.302378Search in Google Scholar PubMed

Received: 2014-12-2
Accepted: 2015-3-10
Published Online: 2015-3-19
Published in Print: 2015-6-1

©2015 by De Gruyter

Downloaded on 28.3.2024 from https://www.degruyter.com/document/doi/10.1515/hsz-2014-0292/html
Scroll to top button