Biology of Blood and Marrow Transplantation
Volume 12, Issue 7 , Pages 758-769 , July 2006

Impact of Donor and Recipient Sex and Parity on Outcomes of HLA-Identical Sibling Allogeneic Hematopoietic Stem Cell Transplantation

  • Alison W. Loren

      Affiliations

    • Stem Cell Transplant Program, Abramson Cancer Center, University of Pennsylvania, Philadelphia, Pennsylvania
    • Center for Clinical Epidemiology & Biostatistics, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania
    • Corresponding Author InformationCorrespondence and reprint requests: Alison W. Loren, MD, MS, Stem Cell Transplant Program, Abramson Cancer Center, University of Pennsylvania, 16 Penn Tower, 3400 Spruce Street, Philadelphia, PA 19104.
  • ,
  • Greta R. Bunin

      Affiliations

    • Center for Clinical Epidemiology & Biostatistics, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania
    • Division of Oncology, Children’s Hospital of Philadelphia, Philadelphia, Pennsylvania
  • ,
  • Christian Boudreau

      Affiliations

    • Center for International Blood and Marrow Transplant Research (CIBMTR), Medical College of Wisconsin, Milwaukee, Wisconsin
    • Department of Statistics & Actuarial Science, University of Waterloo, Waterloo, Ontario, Canada
  • ,
  • Richard E. Champlin

      Affiliations

    • Department of Blood and Marrow Transplantation, MD Anderson Cancer Center, Houston, Texas
  • ,
  • Avital Cnaan

      Affiliations

    • Center for Clinical Epidemiology & Biostatistics, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania
    • Division of Biostatistics & Epidemiology, Children’s Hospital of Philadelphia, Philadelphia, Pennsylvania
  • ,
  • Mary M. Horowitz

      Affiliations

    • Center for International Blood and Marrow Transplant Research (CIBMTR), Medical College of Wisconsin, Milwaukee, Wisconsin
  • ,
  • Fausto R. Loberiza

      Affiliations

    • Center for International Blood and Marrow Transplant Research (CIBMTR), Medical College of Wisconsin, Milwaukee, Wisconsin
    • Section of Hematology/Oncology, Department of Internal Medicine, University of Nebraska Medical Center, Omaha, Nebraska
  • ,
  • David L. Porter

      Affiliations

    • Stem Cell Transplant Program, Abramson Cancer Center, University of Pennsylvania, Philadelphia, Pennsylvania

Received 19 January 2006 ,Accepted 27 March 2006.

References 

  1. Gale RP , Bortin MM , van Bekkum DW , et al.   Risk factors for acute graft-versus-host disease . Br J Haematol . 1987;67:397–406
  2. Flowers ME , Pepe MS , Longton G , et al.   Previous donor pregnancy as a risk factor for acute graft-versus-host disease in patients with aplastic anaemia treated by allogeneic marrow transplantation . Br J Haematol . 1990;74:492–496
  3. Atkinson K , Farrell C , Chapman G , Downs K , Penny R , Biggs J . Female marrow donors increase the risk of acute graft-versus-host disease (effect of donor age and parity and analysis of cell subpopulations in the donor marrow inoculum) . Br J Haematol . 1986;63:231–239
  4. Weisdorf D , Hakke R , Blazar B , et al.   Risk factors for acute graft-versus-host disease in histocompatible donor bone marrow transplantation . Transplantation . 1991;51:1197–1203
  5. Nash RA , Pepe MS , Storb R , et al.   Acute graft-versus-host disease (analysis of risk factors after allogeneic marrow transplantation and prophylaxis with cyclosporine and methotrexate) . Blood . 1992;80:1838–1845
  6. Carlens S , Ringden O , Remberger M , et al.   Risk factors for chronic graft-versus-host disease after bone marrow transplantation (a retrospective single centre analysis) . Bone Marrow Transplant . 1998;22:755–761
  7. Remberger M , Kumlien G , Aschan J , et al.   Risk factors for moderate-to-severe chronic graft-versus-host disease after allogeneic hematopoietic stem cell transplantation . Biol Blood Marrow Transplant . 2002;8:674–682
  8. Przepiorka D , Smith TL , Folloder J , et al.   Risk factors for acute graft-versus-host disease after allogeneic blood stem cell transplantation . Blood . 1999;94:1465–1470
  9. Bross DS , Tutschka PJ , Farmer ER , et al.   Predictive factors for acute graft-versus-host disease in patients transplanted with HLA-identical bone marrow . Blood . 1984;63:1265–1270
  10. Randolph SSB , Gooley TA , Warren EH , Appelbaum FR , Riddell SR . Female donors contribute to a selective graft-versus-leukemia effect in male recipients of HLA-matched, related hematopoietic stem cell transplants . Blood . 2004;103:347–352
  11. Kollman C , Howe CW , Anasetti C , et al.   Donor characteristics as risk factors in recipients after transplantation of bone marrow from unrelated donors (the effect of donor age) . Blood . 2001;98:2043–2051
  12. Schroder J , Tiilikainen A , De la Chapelle A . Fetal leukocytes in the maternal circulation after delivery. I. Cytological aspects . Transplantation . 1974;17:346–354
  13. Bianchi DW . Prenatal diagnosis by analysis of fetal cells in maternal blood . J Pediatr . 1995;127:847–856
  14. Lo YM , Lo ES , Watson N , et al.   Two-way cell traffic between mother and fetus (biologic and clinical implications) . Blood . 1996;88:4390–4395
  15. Lo YM , Lau TK , Chan LY , Leung TN , Chang AM . Quantitative analysis of the bidirectional fetomaternal transfer of nucleated cells and plasma DNA . Clin Chem . 2000;46:1301–1309
  16. Thomas MR , Williamson R , Craft I , Yazdani N , Rodeck CH . Y chromosome sequence DNA amplified from peripheral blood of women in early pregnancy . Lancet . 1994;343:413–414
  17. Stott LM , Barker RN , Urbaniak SJ . Identification of alloreactive T-cell epitopes on the Rhesus D protein . Blood . 2000;96:4011–4019
  18. Newman PJ , McFarland JG , Aster RH . Alloimmune thrombocytopenias . In:  Loscalzo J ,  Schafer AI editor. Thrombosis and Hemorrhage . 2nd ed.. Baltimore: Williams & Wilkins; 1998;p. 599–615
  19. Skacel PO , Stacey TE , Tidmarsh CE , Contreras M . Maternal alloimmunization to HLA, platelet and granulocyte-specific antigens during pregnancy (its influence on cord blood granulocyte and platelet counts) . Br J Haematol . 1989;71:119–123
  20. Regan L , Braude PR , Hill DP . A prospective study of the incidence, time of appearance and significance of anti-paternal lymphocytotoxic antibodies in human pregnancy . Hum Reprod . 1991;6:294–298
  21. Rebibou JM , Chabod J , Dupont I , Chalopin JM , Tiberghien P . The interest of flow cytometry for the detection of pregnancy-induced alloimmunization . Transplant Proc . 2000;32:2747
  22. Verdijk RM , Kloosterman A , Pool J , et al.   Pregnancy induces minor histocompatibility antigen-specific cytotoxic T cells (implications for stem cell transplantation and immunotherapy) . Blood . 2004;103:1961–1964
  23. Farber CM , Wachtel SS , Cunningham-Rundles C . Immune complexes containing H-Y antigen and maternal IgG in cord serum . Clin Exp Immunol . 1982;50:450–453
  24. James E , Chai JG , Dewchand H , Macchiarulo E , Dazzi F , Simpson E . Multiparity induces priming to male-specific minor histocompatibility antigen, HY, in mice and humans . Blood . 2003;102:388–393
  25. Miklos DB , Kim HT , Zorn E , et al.   Antibody responses to multiple H-Y minor histocompatibility antigens are induced after allogeneic stem cell transplantation and in normal female donors . Blood . 2003;102:950a
  26. Miklos DB , Kim HT , Zorn E , et al.   Antibody response to DBY minor histocompatibility antigen is induced after allogeneic stem cell transplantation and in healthy female donors . Blood . 2004;103:353–359
  27. Butturini A , Seeger RC , Gale RP . Recipient immune-competent T lymphocytes can survive intensive conditioning for bone marrow transplantation . Blood . 1986;68:954–956
  28. Voogt PJ , Fibbe WE , Marijt WA , et al.   Rejection of bone-marrow graft by recipient-derived cytotoxic T lymphocytes against minor histocompatibility antigens . Lancet . 1990;335:131–134
  29. Gale RP , Horowitz MM , Butturini A , Barrett AJ , Kolb HJ . What determines who develops graft-versus-host disease (the graft or the host (or both)?) . Bone Marrow Transplant . 1992;10:99–102
  30. 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
  31. Stussi G , Seebach L , Muntwyler J , Schanz U , Gmur J , Seebach JD . Graft-versus-host disease and survival after ABO-incompatible allogeneic bone marrow transplantation (a single-centre experience) . Br J Haematol . 2001;113:251–253
  32. 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
  33. Glucksberg H , Storb R , Fefer A , et al.   Clinical manifestations of graft-versus-host disease in human recipients of marrow from HL-A-matched sibling donors . Transplantation . 1974;18:295–304
  34. Gooley TA , Leisenring W , Crowley J , Storer BE . Estimation of failure probabilities in the presence of competing risks (new representations of old estimators) . Stat Med . 1999;18:695–706
  35. Klein JP , Rizzo JD , Zhang MJ , Keiding N . Statistical methods for the analysis and presentation of the results of bone marrow transplants. Part 2: regression modeling . Bone Marrow Transplant . 2001;28:1001–1011
  36. Benjamini Y , Hochberg Y . Controlling the false discovery rate (a practical and powerful approach to multiple testing) . J R Stat Soc B . 1995;57:289–300
  37. Goulmy E , Termijtelen A , Bradley BA , van Rood JJ . Y-antigen killing by T cells of women is restricted by HLA . Nature . 1977;266:544–545
  38. Wang W , Meadows LR , den Haan JM , et al.   Human H-Y (a male-specific histocompatibility antigen derived from the SMCY protein) . Science . 1995;269:1588–1590
  39. Rufer N , Wolpert E , Helg C , et al.   HA-1 and the SMCY-derived peptide FIDSYICQV (H-Y) are immunodominant minor histocompatibility antigens after bone marrow transplantation . Transplantation . 1998;66:910–916
  40. Bianchi DW , Zickwolf GK , Weil GJ , Sylvester S , DeMaria MA . Male fetal progenitor cells persist in maternal blood for as long as 27 years postpartum . Proc Natl Acad Sci U S A . 1996;93:705–708
  41. Starzl TE , Demetris AJ , Murase N , Trucco M , Thomson AW , Rao AS . The lost chord (microchimerism and allograft survival) . Immunol Today . 1996;17:577–584
  42. Evans PC , Lambert N , Maloney S , Furst DE , Moore JM , Nelson JL . Long-term fetal microchimerism in peripheral blood mononuclear cell subsets in healthy women and women with scleroderma . Blood . 1999;93:2033–2037
  43. Ichinohe T , Teshima T , Matsuoka K-i , Maruya E , Saji H . Fetal-maternal microchimerism (impact on hematopoietic stem cell transplantation) . Curr Opin Immunol . 2005;17–546
  44. Ochiai N , Shimazaki C , Fuchida S , et al.   Successful non-T cell-depleted HLA haplo-identical three-loci mismatched hematopoietic stem cell transplantation from mother to son based on the feto-maternal microchimerism in chronic myelogenous leukemia . Bone Marrow Transplant . 2002;30:793–796
  45. Shimazaki C , Ochiai N , Uchida R , et al.   Non-T-cell-depleted HLA haploidentical stem cell transplantation in advanced hematologic malignancies based on the feto-maternal microchimerism . Blood . 2003;101:3334–3336
  46. Yoshihara T , Morimoto A , Inukai T , et al.   Non-T-cell-depleted HLA haploidentical stem cell transplantation based on feto-maternal microchimerism in pediatric patients with advanced malignancies . Bone Marrow Transplant . 2004;34:373–375
  47. Hall JM , Lingenfelter P , Adams SL , Lasser D , Hansen JA , Bean MA . Detection of maternal cells in human umbilical cord blood using fluorescence in situ hybridization . Blood . 1995;86:2829–2832
  48. Maloney S , Smith A , Furst DE , et al.   Microchimerism of maternal origin persists into adult life . J Clin Invest . 1999;104:41–47
  49. Scaradavou A , Carrier C , Mollen N , Stevens C , Rubinstein P . Detection of maternal DNA in placental/umbilical cord blood by locus-specific amplification of the noninherited maternal HLA gene . Blood . 1996;88:1494–1500
  50. Socie G , Gluckman E , Carosella E , Brossard Y , Lafon C , Brison O . Search for maternal cells in human umbilical cord blood by polymerase chain reaction amplification of two minisatellite sequences . Blood . 1994;83:340–344
  51. Molitor ML , Haynes LD , Jankowska-Gan E , Mulder A , Burlingham WJ . HLA class I noninherited maternal antigens in cord blood and breast milk . Hum Immunol . 2004;65:231
  52. van Rood JJ , Loberiza FR , Zhang M-J , et al.   Effect of tolerance to noninherited maternal antigens on the occurrence of graft-versus-host disease after bone marrow transplantation from a parent or an HLA-haploidentical sibling . Blood . 2002;99:1572–1577
  53. Ichinohe T , Uchiyama T , Shimazaki C , et al.   Feasibility of HLA-haploidentical hematopoietic stem cell transplantation between noninherited maternal antigen (NIMA)-mismatched family members linked with long-term fetomaternal microchimerism . Blood . 2004;104:3821–3828
  54. Lambert NC , Evans PC , Hashizumi TL , et al.   Cutting edge: persistent fetal microchimerism in T lymphocytes is associated with HLA-DQA1*0501: implications in autoimmunity . J Immunol . 2000;164:5545–5548
  55. Johnson KL , Samura O , Nelson JL , McDonnell MdWM , Bianchi DW . Significant fetal cell microchimerism in a nontransfused woman with hepatitis C (Evidence of long-term survival and expansion) . Hepatology . 2002;36:1295–1297
  56. Srivatsa B , Srivatsa S , Johnson KL , Samura O , Lee SL , Bianchi DW . Microchimerism of presumed fetal origin in thyroid specimens from women (a case-control study) . Lancet . 2001;358:2034–2038
  57. Khosrotehrani K , Bianchi DW . Multi-lineage potential of fetal cells in maternal tissue (a legacy in reverse) . J Cell Sci . 2005;118:1559–1563
  58. Nelson JL , Furst DE , Maloney S , et al.   Microchimerism and HLA-compatible relationships of pregnancy in scleroderma . Lancet . 1998;351:559–562
  59. Artlett CM , Smith JB , Jimenez SA . Identification of fetal DNA and cells in skin lesions from women with systemic sclerosis . N Engl J Med . 1998;338:1186–1191
  60. Khosrotehrani K , Johnson KL , Cha DH , Salomon RN , Bianchi DW . Transfer of fetal cells with multilineage potential to maternal tissue . JAMA . 2004;292:75–80
  61. Adams KM , Lambert NC , Heimfeld S , et al.   Male DNA in female donor apheresis and CD34-enriched products . Blood . 2003;102:3845–3847

PII: S1083-8791(06)00290-4

doi: 10.1016/j.bbmt.2006.03.015

Biology of Blood and Marrow Transplantation
Volume 12, Issue 7 , Pages 758-769 , July 2006