Transfusion and Apheresis Science
Volume 35, Issue 1 , Pages 59-69 , August 2006

ABO-histo blood group incompatibility in hematopoietic stem cell and solid organ transplantation

  • Georg Stussi

      Affiliations

    • Department of Internal Medicine, University Hospital Basel, Switzerland
    • Department of Internal Medicine, Laboratory for Transplantation Immunology, University Hospital Zürich, Rämistrasse 100, C HOER 31, CH-8091 Zürich, Switzerland
  • ,
  • Jörg Halter

      Affiliations

    • Department of Internal Medicine, University Hospital Basel, Switzerland
  • ,
  • Urs Schanz

      Affiliations

    • Department of Internal Medicine, Clinic for Hematology, University Hospital Zürich, Switzerland
  • ,
  • Jörg D. Seebach

      Affiliations

    • Department of Internal Medicine, Laboratory for Transplantation Immunology, University Hospital Zürich, Rämistrasse 100, C HOER 31, CH-8091 Zürich, Switzerland
    • Corresponding Author InformationCorresponding author. Tel.: +41 1 255 4134; fax: +41 1 255 4445.

Received 13 March 2006 ,Accepted 19 May 2006.

References 

  1. Reddy P, Ferrara JL. Immunobiology of acute graft-versus-host disease. Blood Rev. 2003;17:187–194
  2. Shlomchik WD. Antigen presentation in graft-vs-host disease. Exp Hematol. 2003;31:1187–1197
  3. Stussi G, Huggel K, Lutz HU, et al. Isotype-specific detection of ABO blood group antibodies using a novel flow cytometric method. Br J Haematol. 2005;130:954–963
  4. Klumpp TR. Immunohematologic complications of bone marrow transplantation. Bone Marrow Transplant. 1991;8:159–170
  5. Seebach JD, Stussi G, Passweg JR, et al. ABO blood group barrier in allogeneic bone marrow transplantation revisited. Biol Blood Marrow Transplant. 2005;11:1006–1013
  6. LaRoche V, Eastlund DT, McCullough J. Immunohematologic aspects of allogeneic hematopoietic progenitor cell transplantation. Immunohematol. 2004;20:217–225
  7. Rowley SD, Liang PS, Ulz L. Transplantation of ABO-incompatible bone marrow and peripheral blood stem cell components. Bone Marrow Transplant. 2000;26:749–757
  8. Worel N, Greinix HT, Keil F, et al. Severe immune hemolysis after minor ABO-mismatched allogeneic peripheral blood progenitor cell transplantation occurs more frequently after nonmyeloablative than myeloablative conditioning. Transfusion. 2002;42:1293–1301
  9. Hows J, Beddow K, Gordon SE, et al. Donor-derived red blood cell antibodies and immune hemolysis after allogeneic bone marrow transplantation. Blood. 1986;67:177–181
  10. Gajewski JL, Petz LD, Calhoun L, et al. Hemolysis of transfused group O red blood cells in minor ABO-incompatible unrelated-donor bone marrow transplants in patients receiving cyclosporine without posttransplant methotrexate. Blood. 1992;79:3076–3085
  11. Kim JG, Sohn SK, Kim DH, et al. Impact of ABO incompatibility on outcome after allogeneic peripheral blood stem cell transplantation. Bone Marrow Transplant. 2005;35:489–495
  12. Petz LD. Immune hemolysis associated with transplantation. Semin Hematol. 2005;42:145–155
  13. Robertson VM, Dickson LG, Romond EH, Ash RC. Positive antiglobulin tests due to intravenous immunoglobulin in patients who received bone marrow transplant. Transfusion. 1987;27:28–31
  14. Lasky LC, Warkentin PI, Kersey JH, et al. Hemotherapy in patients undergoing blood group incompatible bone marrow transplantation. Transfusion. 1983;23:277–285
  15. Bensinger WI, Buckner CD, Thomas ED, Clift RA. ABO-incompatible marrow transplants. Transplantation. 1982;33:427–429
  16. Buckner CD, Clift RA, Sanders JE, et al. ABO-incompatible marrow transplants. Transplantation. 1978;26:233–238
  17. Bensinger WI, Baker DA, Buckner CD, Clift RA, Thomas ED. Immunoadsorption for removal of A and B blood-group antibodies. N Engl J Med. 1981;304:160–162
  18. Bensinger WI, Buckner CD, Clift RA, et al. Comparison of techniques for dealing with major ABO-incompatible marrow transplants. Transplant Proc. 1987;19:4605–4608
  19. Ho WG, Champlin RE, Feig SA, Gale RP. Transplantation of ABH incompatible bone marrow: gravity sedimentation of donor marrow. Br J Haematol. 1984;57:155–162
  20. Nussbaumer W, Schwaighofer H, Gratwohl A, et al. Transfusion of donor-type red cells as a single preparative treatment for bone marrow transplants with major ABO incompatibility. Transfusion. 1995;35:592–595
  21. Scholl S, Klink A, Mugge LO, et al. Safety and impact of donor-type red blood cell transfusion before allogeneic peripheral blood progenitor cell transplantation with major ABO mismatch. Transfusion. 2005;45:1676–1683
  22. Damodar S, George B, Mammen J, et al. Pre-transplant reduction of isohaemagglutinin titres by donor group plasma infusion does not reduce the incidence of pure red cell aplasia in major ABO-mismatched transplants. Bone Marrow Transplant. 2005;36:233–235
  23. Webb IJ, Soiffer RJ, Andersen JW, et al. In vivo adsorption of isohemagglutinins with fresh frozen plasma in major ABO-incompatible bone marrow transplantation. Biol Blood Marrow Transplant. 1997;3:267–272
  24. Blacklock HA, Gilmore MJ, Prentice HG, et al. ABO-incompatible bone-marrow transplantation: removal of red blood cells from donor marrow avoiding recipient antibody depletion. Lancet. 1982;2:1061–1064
  25. Braine HG, Sensenbrenner LL, Wright SK, et al. Bone marrow transplantation with major ABO blood group incompatibility using erythrocyte depletion of marrow prior to infusion. Blood. 1982;60:420–425
  26. Dinsmore RE, Reich LM, Kapoor N, et al. ABH incompatible bone marrow transplantation: removal of erythrocytes by starch sedimentation. Br J Haematol. 1983;54:441–449
  27. Tsang KS, Li CK, Wong AP, et al. Processing of major ABO-incompatible bone marrow for transplantation by using dextran sedimentation. Transfusion. 1999;39:1212–1219
  28. Raimondi R, Soli M, Lamparelli T, et al. ABO-incompatible bone marrow transplantation: a GITMO survey of current practice in Italy and comparison with the literature. Bone Marrow Transplant. 2004;34:321–329
  29. Toren A, Dacosta Y, Manny N, et al. Passenger B-lymphocyte-induced severe hemolytic disease after allogeneic peripheral blood stem cell transplantation. Blood. 1996;87:843–844
  30. Laurencet FM, Samii K, Bressoud A, et al. Massive delayed hemolysis following peripheral blood stem cell transplantation with minor ABO incompatibility. Hematol Cell Ther. 1997;39:159–162
  31. Oziel TS, Faucher BC, Chabannon C, et al. Early and fatal immune haemolysis after so-called ‘minor’ ABO-incompatible peripheral blood stem cell allotransplantation. Bone Marrow Transplant. 1997;19:1155–1156
  32. Salmon JP, Michaux S, Hermanne JP, et al. Delayed massive immune hemolysis mediated by minor ABO incompatibility after allogeneic peripheral blood progenitor cell transplantation. Transfusion. 1999;39:824–827
  33. Bornhauser M, Ordemann R, Paaz U, et al. Rapid engraftment after allogeneic ABO-incompatible peripheral blood progenitor cell transplantation complicated by severe hemolysis. Bone Marrow Transplant. 1997;19:295–297
  34. Bolan CD, Childs RW, Procter JL, Barrett AJ, Leitman SF. Massive immune haemolysis after allogeneic peripheral blood stem cell transplantation with minor ABO incompatibility. Br J Haematol. 2001;112:787–795
  35. Lapierre V, Oubouzar N, Auperin A, et al. Influence of the hematopoietic stem cell source on early immunohematologic reconstitution after allogeneic transplantation. Blood. 2001;97:2580–2586
  36. Sniecinski IJ, Oien L, Petz LD, Blume KG. Immunohematologic consequences of major ABO-mismatched bone marrow transplantation. Transplantation. 1988;45:530–534
  37. Stussi G, Muntwyler J, Passweg JR, et al. Consequences of ABO incompatibility in allogeneic hematopoietic stem cell transplantation. Bone Marrow Transplant. 2002;30:87–93
  38. Worel N, Greinix HT, Schneider B, et al. Regeneration of erythropoiesis after related- and unrelated-donor BMT or peripheral blood HPC transplantation: a major ABO mismatch means problems. Transfusion. 2000;40:543–550
  39. Lee JH, Lee KH, Kim S, et al. Anti-A isoagglutinin as a risk factor for the development of pure red cell aplasia after major ABO-incompatible allogeneic bone marrow transplantation. Bone Marrow Transplant. 2000;25:179–184
  40. Benjamin RJ, Connors JM, McGurk S, Churchill WH, Antin JH. Prolonged erythroid aplasia after major ABO-mismatched transplantation for chronic myelogenous leukemia. Biol Blood Marrow Transplant. 1998;4:151–156
  41. Gmür JP, Burger J, Schaffner A, et al. Pure red cell aplasia of long duration complicating major ABO-incompatible bone marrow transplantation. Blood. 1990;75:290–295
  42. Griffith LM, McCoy JP, Bolan CD, et al. Persistence of recipient plasma cells and anti-donor isohaemagglutinins in patients with delayed donor erythropoiesis after major ABO incompatible non-myeloablative haematopoietic cell transplantation. Br J Haematol. 2005;128:668–675
  43. Rozman P, Kosir A, Bohinjec M. Is the ABO incompatibility a risk factor in bone marrow transplantation?. Transpl Immunol. 2005;14:159–169
  44. Mueller RJ, Stussi G, Odermatt B, et al. Major ABO incompatible hematopoietic stem cell transplantation: study of posttransplant pure red cell aplasia and endothelial chimerism. Xenotransplantation. 2006;13:126–132
  45. Reviron J, Schenmetzler C, Bussel A, Devergie A, Gluckman E. Evidence for different kinds of major ABO incompatibility in transplantation due to the interplay of qualitative and quantitative factors: application to the management of 62 bone marrow recipients. Transplant Proc. 1987;19:4623–4628
  46. Wada H, Suda T, Miura Y, et al. Expression of major blood group antigens on human erythroid cells in a two phase liquid culture system. Blood. 1990;75:505–511
  47. Tulliez M, Villeval JL, Lejeune F, et al. Expression of blood group A antigen during erythroid differentiation in A1 and A2 subjects. Leukemia. 1987;1:44–51
  48. Stussi G, Huggel K, Schanz U, Passweg JR, Seebach JD. Levels of anti-A/B antibodies after ABO-incompatible hematopoietic stem cell transplantation. Transplant Proc. 2005;37:1385–1387
  49. Veelken H, Wasch R, Behringer D, Bertz H, Finke J. Pure red cell aplasia after allogeneic stem cell transplantation with reduced conditioning. Bone Marrow Transplant. 2000;26:911–915
  50. Barge AJ, Johnson G, Witherspoon R, Torok-Storb B. Antibody-mediated marrow failure after allogeneic bone marrow transplantation. Blood. 1989;74:1477–1480
  51. Selleri C, Raiola A, De RG, et al. CD34+-enriched donor lymphocyte infusions in a case of pure red cell aplasia and late graft failure after major ABO-incompatible bone marrow transplantation. Bone Marrow Transplant. 1998;22:605–607
  52. Bierman PJ, Warkentin P, Hutchins MR, Klassen LW. Pure red cell aplasia following ABO mismatched marrow transplantation for chronic lymphocytic leukemia: response to antithymocyte globulin. Leuk Lymphoma. 1993;9:169–171
  53. Martelli M, Ponchio L, Beguin Y, et al. Pure red cell aplasia following peripheral stem cell transplantation: complete response to a short course of high-dose recombinant human erythropoietin. Haematologica. 1994;79:456–459
  54. Maschan AA, Skorobogatova EV, Balashov DN, et al. Successful treatment of pure red cell aplasia with a single dose of rituximab in a child after major ABO incompatible peripheral blood allogeneic stem cell transplantation for acquired aplastic anemia. Bone Marrow Transplant. 2002;30:405–407
  55. Ohta S, Yokoyama H, Ise T, et al. Apheresis therapy for prolonged red cell aplasia after major ABO-mismatched bone marrow transplantation. Intern Med. 1997;36:487–491
  56. Roychowdhury DF, Linker CA. Pure red cell aplasia complicating an ABO-compatible allogeneic bone marrow transplantation, treated successfully with antithymocyte globulin. Bone Marrow Transplant. 1995;16:471–472
  57. Ustun C, Celebi H, Arat M, et al. Treatment of aregeneratoric anemia following an ABO-incompatible allogeneic peripheral blood stem cell transplantation: a case report. Ther Apher. 1999;3:275–277
  58. Verholen F, Stalder M, Helg C, Chalandon Y. Resistant pure red cell aplasia after allogeneic stem cell transplantation with major ABO mismatch treated by escalating dose donor leukocyte infusion. Eur J Haematol. 2004;73:441–446
  59. Warkentin PI, Hilden JM, Kersey JH, Ramsay NK, McCullough J. Transplantation of major ABO-incompatible bone marrow depleted of red cells by hydroxyethyl starch. Vox Sang. 1985;48:89–104
  60. Mielcarek M, Leisenring W, Torok-Storb B, Storb R. Graft-versus-host disease and donor-directed hemagglutinin titers after ABO-mismatched related and unrelated marrow allografts: evidence for a graft-versus-plasma cell effect. Blood. 2000;96:1150–1156
  61. Gale RP, Feig S, Ho W, et al. ABO blood group system and bone marrow transplantation. Blood. 1977;50:185–194
  62. Canals C, Muniz-Diaz E, Martinez C, et al. Impact of ABO incompatibility on allogeneic peripheral blood progenitor cell transplantation after reduced intensity conditioning. Transfusion. 2004;44:1603–1611
  63. Mehta J, Powles R, Sirohi B, et al. Does donor-recipient ABO incompatibility protect against relapse after allogeneic bone marrow transplantation in first remission acute myeloid leukemia?. Bone Marrow Transplant. 2002;29:853–859
  64. Goldman J, Liesveld J, Nichols D, Heal J, Blumberg N. ABO incompatibility between donor and recipient and clinical outcomes in allogeneic stem cell transplantation. Leuk Res. 2003;27:489–491
  65. Worel N, Kalhs P, Keil F, et al. ABO mismatch increases transplant-related morbidity and mortality in patients given nonmyeloablative allogeneic HPC transplantation. Transfusion. 2003;43:1153–1161
  66. Benjamin RJ, McGurk S, Ralston MS, Churchill WH, Antin JH. ABO incompatibility as an adverse risk factor for survival after allogeneic bone marrow transplantation. Transfusion. 1999;39:179–187
  67. Erker CG, Steins MB, Fischer RJ, et al. The influence of blood group differences in allogeneic hematopoietic peripheral blood progenitor cell transplantation. Transfusion. 2005;45:1382–1390
  68. Benjamin RJ, Antin JH. ABO-incompatible bone marrow transplantation: the transfusion of incompatible plasma may exacerbate regimen-related toxicity. Transfusion. 1999;39:1273–1274
  69. Heal JM, Blumberg N. The second century of ABO: and now for something completely different. Transfusion. 1999;39:1155–1159
  70. Martinez MT, Bucher C, Stussi G, et al. Transplant-associated microangiopathy (TAM) in recipients of allogeneic hematopoietic stem cell transplants. Bone Marrow Transplant. 2005;36:993–1000
  71. Bacigalupo A, Van Lint MT, Occhini D, et al. ABO compatibility and acute graft-versus-host disease following allogeneic bone marrow transplantation. Transplantation. 1988;45:1091–1094
  72. Keever-Taylor CA, Bredeson C, Loberiza FR, et al. Analysis of risk factors for the development of GVHD after T cell-depleted allogeneic BMT: effect of HLA disparity, ABO incompatibility, and method of T-cell depletion. Biol Blood Marrow Transplant. 2001;7:620–630
  73. Hershko C, Gale RP, Ho W, Fitchen J. ABH antigens and bone marrow transplantation. Br J Haematol. 1980;44:65–73
  74. Kalaycioglu M, Copelan E, Avalos B, et al. Survival after ABO-incompatible allogeneic bone marrow transplant after a preparative regimen of busulfan and cyclophosphamide. Bone Marrow Transplant. 1995;15:105–110
  75. Tanabe K, Takahashi K, Sonda K, et al. Long-term results of ABO-incompatible living kidney transplantation: a single-center experience. Transplantation. 1998;65:224–228
  76. Karakayali H, Moray G, Demirag A, et al. Long-term follow-up of ABO-incompatible renal transplant recipients. Transplant Proc. 1999;31:256–257
  77. Takahashi K, Saito K, Takahara S, et al. Excellent long-term outcome of ABO-incompatible living donor kidney transplantation in Japan. Am J Transplant. 2004;4:1089–1096
  78. Takahashi K. ABO incompatible kidney transplantation. Elsevier Science Ltd; 2002;
  79. Ishida H, Koyama I, Sawada T, et al. Anti-AB titer changes in patients with ABO incompatibility after living related kidney transplantations: survey of 101 cases to determine whether splenectomies are necessary for successful transplantation. Transplantation. 2000;70:681–685
  80. Shishido S, Asanuma H, Tajima E, et al. Abo-incompatible living-donor kidney transplantation in children. Transplantation. 2001;72:1037–1042
  81. Tyden G, Kumlien G, Genberg H, et al. ABO incompatible kidney transplantations without splenectomy, using antigen-specific immunoadsorption and rituximab. Am J Transplant. 2005;5:145–148
  82. Winters JL, Gloor JM, Pineda AA, Stegall MD, Moore SB. Plasma exchange conditioning for ABO-incompatible renal transplantation. J Clin Apheresis. 2004;19:79–85
  83. Gloor JM, Lager DJ, Moore SB, et al. ABO-incompatible kidney transplantation using both A2 and non-A2 living donors. Transplantation. 2003;75:971–977
  84. Bailey LL, Nehlsen-Cannarella SL, Concepcion W, Jolley WB. Baboon-to-human cardiac xenotransplantation in a neonate. JAMA. 1985;254:3321–3329
  85. West LJ, Pollock-Barziv SM, Dipchand AI, et al. ABO-incompatible heart transplantation in infants. N Engl J Med. 2001;344:793–800
  86. Fan X, Ang A, Pollock-Barziv SM, et al. Donor-specific B-cell tolerance after ABO-incompatible infant heart transplantation. Nat Med. 2004;10:1227–1233
  87. Rao JN, Hasan A, Hamilton JR, et al. ABO-incompatible heart transplantation in infants: the Freeman Hospital experience. Transplantation. 2004;77:1389–1394
  88. Schmoeckel M, Dabritz SH, Kozlik-Feldmann R, et al. Successful ABO-incompatible heart transplantation in two infants. Transpl Int. 2005;18:1210–1214
  89. Rodriguez RJ, Addonizio LJ, Lamour JM, et al. Pediatric heart transplantation across ABO blood type barriers: a case study. Prog Transplant. 2005;15:161–165
  90. Pierson RN, Loyd JE, Goodwin A, et al. Successful management of an ABO-mismatched lung allograft using antigen-specific immunoadsorption, complement inhibition, and immunomodulatory therapy1. Transplantation. 2002;74:79–84
  91. Koestner SC, Kappeler A, Schaffner T, et al. Histo-blood group type change of the graft from B to O after ABO mismatched heart transplantation. Lancet. 2004;363:1523–1525
  92. Banner NR, Rose ML, Cummins D, et al. Management of an ABO-incompatible lung transplant. Am J Transplant. 2004;4:1192–1196
  93. Cooper DK. Clinical survey of heart transplantation between ABO blood group-incompatible recipients and donors. J Heart Transplant. 1990;9:376–381
  94. Campion EW. A death at Duke. N Engl J Med. 2003;348:1083–1084
  95. Pancevski B. Swiss hospital investigates heart transplant “experiment”. Lancet. 2005;366:624
  96. Soares MP, Lin Y, Sato K, Stuhlmeier KM, Bach FH. Accommodation. Immunol Today. 1999;20:434–437
  97. Fehr T, Sykes M. Tolerance induction in clinical transplantation. Transpl Immunol. 2004;13:117–130
  98. West LJ. B-cell tolerance following ABO-incompatible infant heart transplantation. Transplantation. 2006;81:301–307
  99. Mohiuddin MM, Ogawa H, Yin DP, Shen J, Galili U. Antibody-mediated accommodation of heart grafts expressing an incompatible carbohydrate antigen. Transplantation. 2003;75:258–262
  100. Ogawa H, Mohiuddin MM, Yin DP, et al. Mouse-heart grafts expressing an incompatible carbohydrate antigen. II. Transition from accommodation to tolerance. Transplantation. 2004;77:366–373
  101. Quaini F, Urbanek K, Beltrami AP, et al. Chimerism of the transplanted heart. N Engl J Med. 2002;346:5–15
  102. Lagaaij EL, Cramer-Knijnenburg GF, van Kemenade FJ, et al. Endothelial cell chimerism after renal transplantation and vascular rejection. Lancet. 2001;357:33–37
  103. Mezey E, Key S, Vogelsang G, et al. Transplanted bone marrow generates new neurons in human brains. Proc Natl Acad Sci USA. 2003;100:1364–1369
  104. Korbling M, Katz RL, Khanna A, et al. Hepatocytes and epithelial cells of donor origin in recipients of peripheral-blood stem cells. N Engl J Med. 2002;346:738–746
  105. Thiele J, Varus E, Wickenhauser C, et al. Chimerism of cardiomyocytes and endothelial cells after allogeneic bone marrow transplantation in chronic myeloid leukemia. An autopsy study. Pathologe. 2002;23:405–410
  106. Meignin V, Soulier J, Brau F, et al. Little evidence of donor-derived epithelial cells in early digestive acute graft-versus-host disease. Blood. 2004;103:360–362

PII: S1473-0502(06)00091-7

doi: 10.1016/j.transci.2006.05.009

Transfusion and Apheresis Science
Volume 35, Issue 1 , Pages 59-69 , August 2006