Blood Reviews
Volume 21, Issue 6 , Pages 327-348 , November 2007

Transfusion-related immunomodulation (TRIM): An update

  • Eleftherios C. Vamvakas

      Affiliations

    • Department of Pathology and Laboratory Medicine, University of Ottawa, Faculty of Medicine, Canada
  • ,
  • Morris A. Blajchman

      Affiliations

    • Department of Pathology and Molecular Medicine, McMaster University Medical School, and Canadian Blood Services, Hamilton, Ontario, Canada
    • Corresponding Author InformationCorresponding author. Address: McMaster University, Department of Pathology and Molecular Medicine, 1200 Main St. West, Room 4N67, Hamilton, Ontario, Canada L8N 3Z5. Tel.: +1 905 525 9140x26276; fax: +1 905 527 4866.

References 

  1. Lagaaij EL, Ruigrok MB, van Rood JJ, et al. Blood transfusion induced changes in cell-mediated lympholysis: to immunize or not to immunize. J Immunol. 1991;147:3348–3352
  2. Roelen DL, van Rood JJ, Brand A, et al. Immunomodulation by blood transfusions. Vox Sang. 2000;78:273–275
  3. Sho M, Sandner SE, Najafian N, et al. New insights into the interactions between T-cell costimulatory blockade and conventional immunosuppressive drugs. Ann Surg. 2002;236:667–675
  4. Rothstein DM, Sayegh MH. T-cell costimulatory pathways in allograft rejection and tolerance. Immunol Rev. 2003;196:85–108
  5. Mincheff MS, Meryman HT. Costimulatory signals necessary for induction of T cell proliferation. Transplantation. 1990;49:768–772
  6. Brand A. Immunological aspects of blood transfusions. Transpl Immunol. 2002;10:183–190
  7. Brunson ME, Alexander JW. Mechanisms of transfusion-induced immunosuppression. Transfusion. 1990;30:651–658
  8. Blajchman MA, Bordin JO. Mechanisms of transfusion-associated immunosuppression. Curr Opin Hematol. 1994;1:457–461
  9. Opelz G, Sengar DP, Mickey MR, et al. Effect of blood transfusions on subsequent kidney transplants. Transplant Proc. 1973;5:253–259
  10. Gantt CL. Red blood cells for cancer patients. Lancet. 1981;2:363
  11. Peters WR, Fry RD, Fleshman JW, et al. Multiple blood transfusions reduce the recurrence rate of Crohn’s disease. Dis Colon Rectum. 1989;32:749–753
  12. Mowbray JF, Gibbings C, Liddell H, Reginald PW, Underwood JI, Beard RW. Controlled trial of treatment of recurrent spontaneous abortion by immunization with paternal cells. Lancet. 1985;1:941–943
  13. In:  Vamvakas EC,  Blajchman MA editor. Immunomodulatory Effects of Blood Transfusion. Bethesda, MD: AABB Press; 1999;295 pp.
  14. Bordin JO, Heddle NM, Blajchman MA. Biologic effects of leukocytes present in transfused cellular blood products. Blood. 1994;84:1705–1721
  15. Vamvakas EC, Blajchman MA. Deleterious clinical effects of transfusion-associated immunomodulation: fact or fiction?. Blood. 2001;97:1180–1195
  16. Blumberg N, Heal JM. Effects of transfusion on immune function: cancer recurrence and infection. Arch Pathol Lab Med. 1994;118:371–379
  17. Vamvakas E, Moore SB. Blood transfusions and postoperative septic complications. Transfusion. 1994;34:714–727
  18. Blumberg N. Deleterious clinical effects of transfusion immunomodulation: proven beyond reasonable doubt. Transfusion. 2005;45(August Suppl.):33S–39S
  19. Vamvakas E. Deleterious clinical effects of transfusion immunomodulation: proved beyond reasonable doubt. Transfusion. 2006;46:492–494
  20. van de Watering LMG, Hermans J, Houbiers JGA, et al. Beneficial effect of leukocyte depletion of transfused blood on post-operative complications in patients undergoing cardiac surgery: A randomized clinical trial. Circulation. 1998;97:562–568
  21. Bilgin YM, van de Watering LMG, Eijsman L, et al. Double-blind, randomized controlled trial on the effect of leukocyte-depleted erythrocyte transfusions in cardiac valve surgery. Circulation. 2004;109:2755–2760
  22. Boshkov LK, Furnary A, Morris C, Chien G, van Winkle D, Reik R. Prestorage leukoreduction of red cells in elective cardiac surgery: Results of a double-blind randomized controlled trial. Blood. 2004;104:112a;(abstract)
  23. Moore FA, Moore EE. Evolving concepts in the pathogenesis of postinjury multiple-organ failure. Surg Clin North Am. 1995;75:257–277
  24. Vedder NB, Fouty BW, Winn RK, Harlan JM. Role of neutrophils in generalized reperfusion injury associated with resuscitation from shock. Surgery. 1989;106:509–516
  25. Anderson BO, Harken AH. Multiple-organ failure: Inflammatory priming and activation sequences promote autologous tissue injury. J Trauma. 1990;30:S44–S49
  26. Botha AJ, Moore FA, Moore EE, Fontes B, Banerjee A, Peterson VM. Postinjury neutrophil priming and activation states: Therapeutic challenges. Shock. 1995;3:157–166
  27. Silliman CC, Clay KL, Thurman GW, et al. Partial characterization of lipids that develop during the routine storage of blood and prime the neutrophil NADPH oxidase. J Lab Clin Med. 1994;124:684–694
  28. Vamvakas EC. Possible mechanisms of allogeneic blood transfusion-associated postoperative infection. Transf Med Rev. 2002;16:144–160
  29. Fergusson D, Hébert P, Shapiro S. The before/after study design in transfusion medicine: Methodologic considerations. Transf Med Rev. 2002;16:296–303
  30. Singal DP, Leber B, Harnish DG, Frame B, Joseph S, Blajchman MA. Molecular genetic basis for the antiidiotypic antibody response associated with successful renal allograft survival in humans. Transplant Proc. 1991;23:1059–1062
  31. Goodarzi MO, Lee TH, Pallavicini MG, Donegan EA, Busch MP. Unusual kinetics of white cell clearance in transfused mice. Transfusion. 1995;35:145–149
  32. Dzik WH. Apoptosis, TGF-beta, and transfusion-related immunosuppression: Biologic versus clinical effects. Transfusion Apheresis Sci. 2003;29:127–129
  33. Kao KJ. Induction of humoral immune tolerance to major histocompatibility complex antigens by transfusions of UV-B irradiated leukocytes. Blood. 1996;88:4375–4382
  34. Gianotti L, Pyles T, Alexander JW, Fukushima R, Babcock GF. Identification of the blood component responsible for increased susceptibility to gut-derived infection. Transfusion. 1993;33:458–465
  35. Blajchman MA, Bardossy I, Carmen R, Sastry A, Singal DP. Allogeneic blood transfusion-induced enhancement of tumor growth: two animal models showing amelioration by leukodepletion and passive transfer using spleen cells. Blood. 1993;81:1880–1882
  36. Mincheff MS, Meryman HT, Kapoor V, et al. Blood transfusion and immunomodulation: a possible mechanism. Vox Sang. 1993;65:18–24
  37. Clark DA, Gorczynski RM, Blajchman MA. Transfusion-related immunomodulation due to blood dendritic cells expressing the CD200 tolerance-signaling molecules and alloantigen: Tumor growth is stimulated by TGFβ from suppressor-cell induction. Submitted for publication.
  38. Barclay AN, Wright GJ, Brooke G, Brown MH. CD200 and membrane protein interactions in the control of myeloid cells. Trend Immunol. 2003;23:285–290
  39. Gorczynski RM, Hadidi S, Yu G, Clark DA. The same immunoregulatory molecules contribute to successful pregnancy and transplantation. Amer J Reprod Immunol. 2002;48:18–26
  40. Reed SG. TGF-β in infections and infectious disease. Microbes and Infection. 1999;1:1313–1325
  41. Beko KR, Tran HO, Hewitt CW, et al. Mechanisms of prior blood transfusion-cyclosporine-induced tolerance: a potential role for immune-cellular chimerism. Transplant Proc. 1991;23:147–148
  42. Dzik WH. Mononuclear cell microchimerism and the immunomodulatory effect of transfusion. Transfusion. 1994;34:1007–1012
  43. Gafter U, Kalechman Y, Sredni B. Blood transfusion enhances production of T-helper-2 cytokines and transforming growth factor beta in humans. Clin Sci (Lond). 1996;91:519–523
  44. Kirkley SA, Cowles J, Pellegrini VD, et al. Blood transfusion and total joint replacement surgery: T-helper 2 cytokine secretion and clinical outcome. Transf Med. 1998;8:195–204
  45. Reed W, Lee TH, Norris PJ, Utter GH, Busch MP. Transfusion-associated microchimerism: a new complication of blood transfusions in severely ill patients. Semin Hematol. 2007;44:24–31
  46. Lee TH, Paglieroni T, Ohto H, Holland PV, Busch MP. Survival of donor leukocyte subpopulations in immunocompetent transfusion recipients: frequent long-term microchimerism in severe trauma patients. Blood. 1999;93:3127–3139
  47. Kruskall MS, Lee TH, Assmann SF, et al. Survival of transfused donor white blood cells in HIV-infected recipients. Blood. 2001;98:272–279
  48. Lee TH, Paglieroni T, Utter TH, et al. High-level long-term white-blood-cell microchimerism after transfusion of leukoreduced blood components to patients resuscitated after severe traumatic injury. Transfusion. 2005;35:1280–1290
  49. Utter GH, Nathens AB, Lee TH, et al. Leukoreduction of blood transfusions does not diminish transfusion-associated microchimerism in trauma patients. Transfusion. 2006;46:1863–1869
  50. Nathens AB, Nester TA, Rubenfeld GD, Nirula R, Gernsheimer TB. The effects of leukoreduced blood transfusion on infection risk following injury: A randomized controlled trial. Shock. 2006;26:342–347
  51. Nielsen HJ, Reimert CM, Pedersen AN, et al. Time-dependent, spontaneous release of white cell- and platelet-derived bioactive substances from stored human blood. Transfusion. 1996;36:960–965
  52. Bury TB, Corhay JL, Radermecker MF. Histamine-induced inhibition of neutrophil chemotaxis and T-lymphocyte proliferation in man. Allergy. 1992;47:624–629
  53. Peterson CG, Skoog V, Venge P. Human eosinophil cationic proteins (ECP and EPX) and their suppressive effects on lymphocyte proliferation. Immunobiology. 1986;171:1–13
  54. Ghio M, Contini P, Mazzei C, et al. Soluble HLA Class I, HLA Class II, and Fas ligand in blood components: a possible key to explain the immunomodulatory effects of allogeneic blood transfusion. Blood. 1999;93:1770–1777
  55. Puppo F, Contini P, Ghio M, et al. ;Soluble human MHC class I molecules induce soluble Fas-ligand secretion and trigger apoptosis in activated CD8+ Fas (CD95)+ T lymphocytes. Intern Immunol. 2000;12:195–203
  56. Pitti RM, Marster SA, Lawrence DA, et al. Genomic amplification of a decoy receptor for Fas ligand in lung and colon cancer. Nature. 1998;396:699–703
  57. Ashkenazi A, Dixit VM. Death receptors: Signaling and modulation. Science. 1998;281:1305–1308
  58. Innerhofer P, Luz G, Spotl L, et al. Immunologic changes following transfusion of autologous or allogeneic buffy-coated-poor versus leukocyte-depleted blood in patients undergoing arthroplasty. I. Proliferative T-cell responses and T-helper/T-suppressor cell balance. Transfusion. 1999;39:1089–1096
  59. Innerhofer P, Tilz G, Fuchs D, et al. Immunologic changes following transfusion of autologous or allogeneic buffy-coat-poor versus leukocyte-depleted blood transfusions in patients undergoing arthroplasty. II. Activation of T-cells, macrophages and cell-mediated lympholysis. Transfusion. 2000;40:821–827
  60. Hyllner M, Arnestad JP, Bengston JP, et al. Transfusion. 1997;37:264–268
  61. Schleuning M, Utz H, Heim M, Mempel W. Effects of leukocyte depletion on the formation of anaphylatoxins in stored whole blood. Infusionsther Transfusionmed. 1992;19:242–244
  62. Bordin JO, Bardossy L, Blajchman MA. Growth enhancement of established tumors by allogeneic blood transfusion in experimental animals and its amelioration by leukodepletion: the importance of timing of the leukodepletion. Blood. 1994;84:344–348
  63. Ghio M, Ottonello L, Contini P, et al. Transforming growth factor-beta-1 in supernatants from stored red blood cells inhibits neutrophil locomotion. Blood. 2003;102:1100–1107
  64. Ottonello L, Ghio M, Contini P, et al. RBC transfusion induces a sustained inhibition of neutrophil chemotaxis by stimulating in vivo production of TGF-β-1 by neutrophils. Role of the immunoglobulin-like transcript 1 (ILT1), sFasL, and sHLA-I. Transfusion 2007;47 (In press).
  65. Magee CC, Sayegh MH. Peptide-mediated immunosuppression. Curr Opin Immunol. 1997;9:669–675
  66. Chueh SC, Tian L, Wang M, Wang ME, Stepkowski SM, Kahan BD. Induction of tolerance toward rat cardiac allografts by treatment with allochimeric class I MHC antigen and FTY720. Transplantation. 1997;64:1407–1414
  67. Naji A. Induction of tolerance by intrathymic inoculation of alloantigen. Curr Opin Immunol. 1996;8:704–709
  68. Jensen LS, Andersen AJ, Christiansen PM, et al. Postoperative infection and natural killer cell function following blood transfusion in patients undergoing elective colorectal surgery. Br J Surg. 1992;79:513–516
  69. Busch ORC, Hop WCJ, van Papendrecht MAWH, et al. Blood transfusion and prognosis in colorectal cancer. N Engl J Med. 1993;328:1372–1376
  70. Heiss MM, Mempel W, Jausch K-W, et al. Beneficial effect of autologous blood transfusion on infectious complications after colorectal cancer surgery. Lancet. 1993;342:1328–1333
  71. Houbiers JGA, Brand A, van de Watering LMG, et al. Randomized controlled trial comparing transfusion of leucocyte-depleted or buffy-coat-depleted blood in surgery for colorectal cancer. Lancet. 1994;344:573–578
  72. Pertila JT, Salo MS, Jalonen JR, Kuttila KT, Viinamaki O, Pulkki KJ. Blood transfusion with autologous and leukocyte-depleted or standard allogeneic red blood cells and the immune response to open-heart surgery. Anesth Analg. 1994;79:654–660
  73. Jensen LS, Kissmeyer-Nielsen P, Wolff B, et al. Randomized comparison of leucocyte-depleted versus buffy-coat-poor blood transfusion and complications after colorectal surgery. Lancet. 1996;348:841–845
  74. Newman JH, Bowers M, Murphy J. The clinical advantages of autologous transfusion: A randomized, controlled study after knee replacement. J Bone Joint Surg Br. 1997;79:630–632
  75. Farrer A, Spark JI, Scott DJ. Autologous blood transfusion: The benefits for the patient undergoing abdominal aortic aneurysm repair. J Vasc Nurs. 1997;15:111–115
  76. Nielsen HJ, Hammer JH, Kraup AL, et al. Prestorage leukocyte filtration may reduce leukocyte-derived bioactive substance accumulation in patients operated for burn trauma. Burns. 1999;25:162–170
  77. Tartter PI, Mohandas K, Azar P, et al. Randomized trial comparing packed red cell blood transfusion with and without leukocyte depletion for gastrointestinal surgery. Am J Surg. 1998;176:462–466
  78. Titlestad IL, Ebbesen LS, Ainsworth AP, et al. Leukocyte-depletion of blood components does not significantly reduce the risk of infectious complications: Results of a double-blind, randomized study. Int J Colorectal Dis. 2001;16:147–153
  79. Thomas D, Wareham K, Cohen D, Hutchings H. Autologous blood transfusion in total knee replacement surgery. Br J Anaesth. 2001;86:669–673
  80. Collier A, Kalish L, Busch M, et al. Leukocyte-reduced red blood cell transfusions in patients with anemia and human immunodeficiency virus infection. JAMA. 2001;285:1592–1601
  81. Wong JCL, Torella F, Haynes SL, et al. Autologous versus allogeneic transfusion in aortic surgery: A multicenter randomized clinical trial. Ann Surg. 2002;235:145–151
  82. Dzik WH, Anderson JK, O’Neill EM, et al. A prospective, randomized clinical trial of universal WBC reduction. Transfusion. 2002;42:1114–1122
  83. Wallis JP, Chapman CE, Orr KE, et al. Effect of WBC reduction of transfused RBCs on postoperative infection rates in cardiac surgery. Transfusion. 2002;42:1127–1134
  84. van Hilten JA, van de Watering LMG, van Bockel JH, et al. Effects of transfusion with red cells filtered to remove leukocytes: Randomized controlled trial in patients undergoing major surgery. BMJ. 2004;328:1281–1284
  85. Bracey AW, Radovancevick R, Nussimeier NA, et al. Leukocyte-reduced blood in open-heart surgery patients: Effects on outcome. Transfusion. 2002;42(Suppl):5S
  86. Heiss MN, Mempel W, Delanoff C, et al. Blood transfusion-modulated tumor recurrence: first results of a randomized study of autologous versus allogeneic blood transfusion in colorectal cancer surgery. J Clin Oncol. 1994;12:1859–1867
  87. Lowry WS, Clark DA, Hanneman JH. Skin cancer and immunosuppression. Lancet. 1973;i:1290–1291
  88. Vamvakas EC. Transfusion-associated cancer recurrence and infection: Meta-analysis of the randomized controlled clinical trials. Transfusion. 1996;36:175–186
  89. Vamvakas EC, Pineda AA. Autologous transfusion and other approaches to reduce allogeneic blood exposure. In:  Contreras M editors. New Aspects of Blood Transfusion. Baillére’s Best Practice and Research in Clinical Haematology. Vol. 13:London, UK: WB Saunders; 2000;p. 533–547
  90. Bruggerman CA. Reactivation of latent CMV in the rat. Transplant Proc. 1991;23(Suppl.3):22–24
  91. Vamvakas E, Kaplan HS. Early transfusion and length of survival in acquired immune deficiency syndrome: Experience with a population receiving medical care at a public hospital. Transfusion. 1993;33:111–118
  92. Sloand E, Kumar P, Klein HG, et al. Transfusion of blood components to persons infected with human immunodeficiency virus type 1: Relationship to opportunistic infection. Transfusion. 1994;34:48–53
  93. Vamvakas E, Kaplan HS. Blood transfusion to AIDS patients: Relationship to opportunistic infection. Transfusion. 1994;34:740
  94. Vamvakas E. Meta-analysis of randomized controlled trials comparing the risk of postoperative infection between recipients of allogeneic and autologous blood transfusion. Vox Sang. 2002;83:339–346
  95. Vamvakas EC. White-blood-cell-containing allogeneic blood transfusion and postoperative infection or mortality: An updated meta-analysis. Vox Sang. 2007;92:224–232
  96. Diversity and heterogeneity [monograph on the Internet]. Oxford: the Cochrane Collaboration; c2002 [accessed 2006 April 13]. Available from: http://www.cochrane-net.org/openlearning/HTML/mod13-5.htm.
  97. Fergusson D, Hébert PC, Lee SK, et al. Clinical outcomes following institution of universal leukoreduction of blood transfusions for premature infants. JAMA. 2003;289:1950–1956
  98. Zallen G, Moore EE, Ciesla DJ, et al. Stored red blood cells selectively activate human neutrophils to release IL-8 and secretory PLA2. Shock. 2000;13:29–33
  99. Silliman CC, Ambruso DR, Boshkov LK. Transfusion-related acute lung injury. Blood. 2005;105:2266–2273
  100. Chin-Yee I, Keeney M, Krueger L, et al. Supernatant from stored red cells activates neutrophils. Transfus Med. 1998;8:49–56
  101. Johnson JL, Moore EE, Offner PJ, et al. Resuscitation with a blood substitute abrogates pathologic postinjury neutrophil cytotoxic function. J Trauma. 2001;50:449–455
  102. Hachida M, Hanayama N, Okamura T, et al. The role of leukocyte depletion in reducing injury to myocardium and lung during cardiopulmonary bypass. ASAIO J. 1995;41:M291–M294
  103. Gu YJ, de Vries AJ, Boonstra PW, et al. Leukocyte depletion results in improved lung function and reduced inflammatory response after cardiac surgery. J Thorac Cardiovasc Surg. 1996;112:494–500
  104. Pearl JM, Drinkwater DC, Laks H, et al. Leukocyte-depleted reperfusion of transplanted human hearts prevents ultrastructural evidence of reperfusion injury. J Surg Res. 1992;52:298–308
  105. Fransen E, Maessen J, Denterner M, et al. Impact of blood transfusions on inflammatory mediator release in patients undergoing cardiac surgery. Chest. 1999;116:1233–1239
  106. Habib RH, Zacharias A, Engoren M. Determinants of prolonged mechanical ventilation after coronary artery bypass grafting. Ann Thorac Surg. 1996;62:1164–1171
  107. Vamvakas EC, Carven JH. Allogeneic blood transfusion and postoperative duration of mechanical ventilation: Effects of red cell supernatant, platelet supernatant, plasma components, and total transfused fluid. Vox Sang. 2002;82:141–149
  108. Maetani S, Nishikawa T, Hirakawa A, et al. Role of blood transfusion in organ system failure following major abdominal surgery. Ann Surg. 1986;203:275–281
  109. Sauaia A, Moore FA, Moore EE, et al. Early predictors of postinjury multiple-organ failure. Arch Surg. 1994;129:39–45
  110. Trann DD, van Onselen EB, Wensink AJ, et al. Factors related to multiple-organ system failure and mortality in a surgical intensive care unit. Nephrol Dial Transplant. 1994;9(Suppl.4):172S–178S
  111. Peerless JR, Alexander J, Pinchak AC, et al. Oxygen delivery is an important predictor of outcome in patients with ruptured aortic aneurysms. Ann Surg. 1998;227:726–732
  112. Santamaria F, Villa MP, Werner B, et al. The effect of transfusion on pulmonary function in patients with thalassemia major. Pediatr Pulmonol. 1994;18:139–143
  113. Hébert PC, Blajchman MA, Cook DJ, et al. Do blood transfusions improve outcomes related to mechanical ventilation?. Chest. 2001;119:1850–1857
  114. 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;39:701–710
  115. Mynster T, Nielsen HJ. The impact of storage time of transfused blood on postoperative infectious complications in rectal cancer surgery. Scand J Gastroenterol. 2000;35:212–217
  116. Offner PLJ, Moore EE, Biff WL, Johnson JL, Silliman CC. Increased rate of infection associated with transfusion of old blood after severe injury. Arch Surg. 2002;137:711–716
  117. Leal-Noval SR, Jara-Lopez I, Garcia-Garmendix JL, et al. Influence of erythrocyte concentrate storage time on postsurgical morbidity in cardiac surgery patients. Anesthesiology. 2003;98:815–822
  118. Zallen G, Offner PJ, Moore EE, et al. Age of transfused blood is an independent risk factor for postinjury multiple-organ failure. Am J Surg. 1999;178:540–572
  119. Purdy FR, Tweeddale MG, Merrick PM. Association of mortality with age of blood transfused in septic ICU patients. Can J Anaesth. 1997;44:1256–1261
  120. Basran S, Frumento RJ, Cohen A, et al. The association between duration of storage of transfused red blood cells and morbidity and mortality after reoperative cardiac surgery. Anesth Analg. 2006;103:15–20
  121. van de Watering LMG, Lorinser J, Verseegh M, Westendorf R, Brand A. Effects of storage time on the prognosis of coronary artery bypass graft patients. Transfusion. 2006;46:1712–1718
  122. Tinmouth A, Fergusson D, Chin Yee I, Hebert PC. Clinical consequences of red-cell storage in the critically ill. Transfusion. 2006;46:2014–2027
  123. Baron JF, Gourdin M, Bertrand M, et al. The effect of universal leukodepletion of packed red blood cells on postoperative infections in high-risk patients undergoing abdominal aortic surgery. Anesth Analg. 2002;94:529–537
  124. Llewelyn CA, Taylor RS, Todd AA, et al. The effect of universal leukoreduction on postoperative infections and length of stay in elective orthopedic and cardiac surgery. Transfusion. 2004;44:489–500
  125. Hébert PC, Fergusson D, Blajchman MA, et al. Clinical outcomes following institution of the Canadian universal leukoreduction program for red blood cell transfusions. JAMA. 2003;289:1941–1949
  126. Volkova N, Klapper E, Pepkowitz SH, Denton T, Gillapsie G, Goldfinger D. A case-control study of the impact of WBC reduction on the cost of hospital care for patients undergoing coronary artery bypass graft surgery. Transfusion. 2002;42:1123–1126
  127. Blumberg N, Heal JM, Cowles JW, et al. Leukocyte-reduced transfusions in cardiac surgery: Results of an implementation trial. Am J Clin Pathol. 2002;118:376–381
  128. Vamvakas EC. White-blood-cell containing allogeneic blood transfusion, postoperative infection, and mortality: A meta-analysis of observational, “before-and-after” studies. Vox Sang. 2004;86:111–119
  129. Brand A, Houbiers JGA. Clinical studies of blood transfusion and cancer. In:  Vamvakas EC,  Blajchman MA editor. Immunomodulatory effects of allogeneic blood transfusion. Bethesda, MD: AABB Press; 1999;p. 145–190
  130. Chung M, Steinmetz OK, Gordon PH. Perioperative blood transfusion and outcome after resection for colorectal carcinoma. Br J Surg. 1993;80:427–432
  131. Vamvakas E. Perioperative blood transfusion and cancer recurrence: Meta-analysis for explanation. Transfusion. 1995;35:760–768
  132. Vamvakas EC, Blajchman MA. Universal white-cell reduction: The case for and against. Transfusion. 2001;41:691–712

PII: S0268-960X(07)00035-5

doi: 10.1016/j.blre.2007.07.003

Blood Reviews
Volume 21, Issue 6 , Pages 327-348 , November 2007