Correspondence

Donor-Type Microchimerism Associated with Graft Rejection Eight Years after Liver Transplantation

N Engl J Med 1994; 330:646-647March 3, 1994

Article

To the Editor:

Transplantation of solid-organ allografts can induce long-term donor-type microchimerism1 by migration of passenger mononuclear cells2,3. So far, microchimerism has been described only in immunologically stable patients after liver or kidney transplantation4. An association between persistent chimerism and graft acceptance has been suggested. We describe persistent donor-type microchimerism in a patient with therapy-resistant graft rejection late after liver transplantation.

In December 1984 a 17-year-old boy (HLA-A1,11; B7,8; Cw7; DRw15,w17) received a liver transplant (Donor 1: HLA-A1,25; B18,w52; DR1,4) for end-stage primary sclerosing cholangitis. After an early episode of rejection that responded to steroids, he had an uneventful course over the next eight years. Maintenance immunosuppression included cyclosporine, azathioprine, and prednisolone. In January 1992 the dose of cyclosporine was reduced because of suspected nephrotoxicity. Over the following months, the patient had recurrent episodes of diarrhea. In June 1992 liver enzyme levels became abnormal; a liver biopsy showed liver-cell necrosis with slight portal infiltrates and some subendothelial lymphocyte accumulation. In July jaundice developed; a liver biopsy showed moderate-to-severe acute graft rejection. Treatment with intravenous cyclosporine and then tacrolimus (FK 506) was not successful. In September 1992 the patient received a second liver transplant (Donor 2: HLA-A3; B7,18; Cw7; DRw4,w13). Histologic evaluation of the excised liver revealed endotheliitis, bile-duct damage, and confluent pericentral hepatocyte necroses but no vasculopathy. This suggested mainly persistent acute rejection, but also early chronic rejection. After the second transplantation, graft function became normal. The patient is currently in good health, with normal liver function while taking cyclosporine, azathioprine, and low doses of steroids.

Samples were obtained separately from the patient several days before the second transplantation (liver, skin, bone marrow, and blood) and at the time of transplantation (lymph node and small intestine). They were analyzed by a nested-polymerase-chain-reaction technique based on the method described by Bein et al.5. To detect donor-specific and recipient-specific DNA sequences, oligonucleotide probes specific for DRB1 alleles of the donor and the recipient were used in the second step, in the presence of 2 micro Ci of [α³²P]deoxycytidine triphosphate. Donor-specific DR1 sequences were detected in the liver, skin, intestine, and peripheral blood, but were undetectable in mesenteric lymph nodes and bone marrow (Table 1Table 1Allele-Specific DRB1 DNA in the Recipient of a Second Liver Graft.). Signals were very strong in the liver tissue and weaker in the skin, blood, and intestine. Recipient-specific DRw15 sequences were detectable at similar strength in all samples. The specificity of amplification products was confirmed by hybridization with oligonucleotide probes. A skin-biopsy specimen obtained nine weeks after the second transplantation showed positive signals for both DR1 and DRw13, but not for DRw15. This demonstrated the presence of chimerism due to the new graft and the disappearance of chimerism due to the first graft (Table 1).

Our findings point to three important aspects of graft-induced microchimerism. First, the disappearance of chimerism after the second transplantation suggests that chimerism represents an actively balanced state. This state may require the presence of the graft, either for a protective function or as a continuing reservoir of migrating cells. Second, the persistence of donor-type microchimerism during severe acute rejection suggests that T-cell alloresponsiveness may not be the only mechanism responsible for controlling chimerism. Third, the presence of donor-type microchimerism in blood and various tissues may not indicate an immunologically stable situation. Inadequate immune suppression of patients in these circumstances may be fatal. Thus, despite suggestions of the immunomodulatory effects of donor-type chimerism, the clinical and immunologic relevance of persistent graft-induced microchimerism is still unclear.

Hans J. Schlitt, M.D.
Joachim Hundrieser, Ph.D.
Burckhardt Ringe, M.D.
Rudolf Pichlmayr, Hon.F.R.C.S.
Medizinische Hochschule, D-30623 Hannover, Germany

5 References

1. 1

   Starzl TE, Demetris AJ, Trucco M, et al. Systemic chimerism in human female recipients of male livers. Lancet 1992;340:876-877
   CrossRef | Web of Science | Medline

2. 2

   Schlitt HJ, Raddatz G, Steinhoff G, Wonigeit K, Pichlmayr R. Passenger lymphocytes in human liver allografts and their potential role after transplantation. Transplantation 1993;56:951-955
   CrossRef | Web of Science | Medline

3. 3

   Schlitt HJ, Kanehiro H, Raddatz G, et al. Persistence of donor lymphocytes in liver allograft recipients. Transplantation 1993;56:1001-1007
   CrossRef | Web of Science | Medline

4. 4

   Starzl TE, Demetris AJ, Trucco M, et al. Chimerism and donor-specific nonreactivity 27 to 29 years after kidney allotransplantation. Transplantation 1993;55:1272-1277
   CrossRef | Web of Science | Medline

5. 5

   Bein G, Glaser R, Kirchner H. Rapid HLA-DRB1 genotyping by nested PCR amplification. Tissue Antigens 1992;39:68-73
   CrossRef | Web of Science | Medline

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1. 1

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2. 2

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3. 3

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4. 4

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   CrossRef

5. 5

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   CrossRef

6. 6

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   CrossRef

7. 7

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   CrossRef

8. 8

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   CrossRef

9. 9

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   CrossRef

10. 10

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    Full Text

11. 11

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    CrossRef

12. 12

    Aurèle Taieb, Julio A. Clavijo-Alvarez, Giselle G. Hamad, W.P. Andrew Lee. (2007) Immunologic Approaches to Composite Tissue Allograft. The Journal of Hand Surgery 32:7, 1072-1085
    CrossRef

13. 13

    M. Sykes. (2007) Immune tolerance: mechanisms and application in clinical transplantation. Journal of Internal Medicine 262:3, 288-310
    CrossRef

14. 14

    Grégoire Wieërs, Jérémie Gras, Christophe Bourdeaux, Dinh Quang Truong, Dominique Latinne, Raymond Reding. (2007) Monitoring tolerance after human liver transplantation. Transplant Immunology 17:2, 83-93
    CrossRef

15. 15

    Maria Siemionow, Serdar Nasir. (2007) Chimerism and bone marrow based therapies in transplantation. Microsurgery 27:5, 510-521
    CrossRef

16. 16

    Raymond Reding, Jérémie Gras, Dinh Quang Truong, Grégoire Wieërs, Dominique Latinne. (2006) The immunological monitoring of alloreactive responses in liver transplant recipients: A review. Liver Transplantation 12:3, 373-383
    CrossRef

17. 17

    Thomas E. Starzl, Fadi G. Lakkis. (2006) The unfinished legacy of liver transplantation: Emphasis on immunology. Hepatology 43:S1, S151-S163
    CrossRef

18. 18

    Christoph J. Mache, Wolfgang Schwinger, Stephan Spendel, Otto Zach, Sigrid Regauer, Ekkehard Ring. (2006) Skin transplantation to monitor clinical donor-related tolerance in mixed hematopoietic chimerism. Pediatric Transplantation 10:1, 128-131
    CrossRef

19. 19

    Christopher C. Silliman. (2005) Immunomodulatory Effects of Stored Packed Red Blood Cells in the Injured Patient. Transfusion Alternatives in Transfusion Medicine 6:4, 23-30
    CrossRef

20. 20

    Florence Bettens, Jean-Marie Tiercy, Nathalie Campanile, Emiliano Giostra, Pietro Majno, Laura Rubbia, Eddy Roosnek, Gilles Mentha, Jean Villard. (2005) Microchimerism after liver transplantation: Absence of rejection without abrogation of anti-donor cytotoxic T-lymphocyte-mediated alloreactivity. Liver Transplantation 11:3, 290-297
    CrossRef

21. 21

    Frans Claas. (2004) Chimerism as a tool to induce clinical transplantation tolerance. Current Opinion in Immunology 16:5, 578-583
    CrossRef

22. 22

    Spiros Delis, Gaetano Ciancio, George W. Burke, Rolando Garcia-Morales, Joshua Miller. (2004) Donor bone marrow transplantation. Transplant Immunology 13:2, 105-115
    CrossRef

23. 23

    Eric G. Jacquet, Carrie L. Schanie, Isabelle Fugier-Vivier, Sharon S. Willer, Suzanne T. Ildstad. (2003) Facilitating cells as a venue to establish mixed chimerism and tolerance. Pediatric Transplantation 7:5, 348-357
    CrossRef

24. 24

    James M. Mathew, Rolando O. Garcia-Morales, Manuel Carreno, Yide Jin, Laphalle Fuller, Bonnie Blomberg, Robert Cirocco, George W. Burke, Gaetano Ciancio, Camillo Ricordi, Violet Esquenazi, Andreas G. Tzakis, Joshua Miller. (2003) Immune responses and their regulation by donor bone marrow cells in clinical organ transplantation. Transplant Immunology 11:3-4, 307-321
    CrossRef

25. 25

    Christophe Ferrand, Sylvain Perruche, Eric Robinet, Anton Martens, Pierre Tiberghien, Philippe Saas. (2003) How should chimerism be decoded?1. Transplantation 75:Supplement, 50S-54S
    CrossRef

26. 26

    Kathryn J. Wood. (2003) Passenger leukocytes and microchimerism: what role in tolerance induction?. Transplantation 75:Supplement, 17S-20S
    CrossRef

27. 27

    Anthony P. Monaco, Peter Medawar. (2003) Chimerism in organ transplantation: conflicting experiments and clinical observations. Transplantation 75:Supplement, 13S-16S
    CrossRef

28. 28

    Takashi Ajiki, Masafumi Takahashi, Seiichiro Inoue, Yasunaru Sakuma, Shigetaka Oyama, Takashi Kaneko, Yoji Hakamata, Takashi Murakami, Akihiro Kume, Yusei Kariya, Yuichi Hoshino, Eiji Kobayashi. (2003) Generation of donor hematolymphoid cells after rat-limb composite grafting. Transplantation 75:5, 631-636
    CrossRef

29. 29

    Toyokazu Okuda, Takashi Ishikawa, Olga Azhipa, Naoya Ichikawa, Anthony J. Demetris, Thomas E. Starzl, Noriko Murase. (2002) Early passenger leukocyte migration and acute immune reactions in the rat recipient spleen during liver engraftment: with particular emphasis on donor major histocompatibility complex class II+ cells1. Transplantation 74:1, 103-111
    CrossRef

30. 30

    Yukihiro Itabashi, Shunji Narumi, Kenichi Hakamada, Nobukazu Watanabe, Kazunori Aoki, Mutsuo Sasaki. (2002) Allogeneic chimerism established with a mixture of low dose bone marrow cells and splenocytes in sublethally irradiated mice. Transplant Immunology 10:1, 25-30
    CrossRef

31. 31

    SARAH GODDARD, DAVID H ADAMS. (2002) New approaches to immunosuppression in liver transplantation. Journal of Gastroenterology and Hepatology 17:2, 116-126
    CrossRef

32. 32

    R.W.G. Gruessner, K.Y. Zhang, M. Dunning, R.E. Nakhleh, A.C. Gruessner. (2001) Bone marrow augmentation in kidney transplantation: a large animal study. Transplant International 14:3, 159-169
    CrossRef

33. 33

    Marty T. Sellers, Mark H. Deierhoi, John J. Curtis, Robert S. Gaston, Bruce A. Julian, Douglas C. Lanier, Arnold G. Diethelm. (2001) TOLERANCE IN RENAL TRANSPLANTATION AFTER ALLOGENEIC BONE MARROW TRANSPLANTATION???6-YEAR FOLLOW-UP. Transplantation 71:11, 1681-1683
    CrossRef

34. 34

    C. Rothmeier, E. Roux, A. Spiliopoulos, M. Gerbase, L. P. Nicod. (2001) EARLY CHIMERISM OF MACROPHAGES AND LYMPHOCYTES IN LUNG TRANSPLANT RECIPIENTS IS PREDICTIVE OF GRAFT TOLERANCE1. Transplantation 71:9, 1329-1333
    CrossRef

35. 35

    Megan Sykes. (2001) Mixed Chimerism and Transplant Tolerance. Immunity 14:4, 417-424
    CrossRef

36. 36

    Thomas Wekerle, Megan Sykes. (2001) M IXED C HIMERISM AND T RANSPLANTATION T OLERANCE. Annual Review of Medicine 52:1, 353-370
    CrossRef

37. 37

    Mitsuhisa Takatsuki, Shinji Uemoto, Yukihiro Inomata, Seisuke Sakamoto, Michihiro Hayashi, Mikiko Ueda, Takashi Kanematsu, Koichi Tanaka. (2001) Analysis of alloreactivity and intragraft cytokine profiles in living donor liver transplant recipients with graft acceptance. Transplant Immunology 8:4, 279-286
    CrossRef

38. 38

    V. Donckier, M. Toungouz, M. Goldman. (2001) Transplantation tolerance and mixed chimerism: at the frontier of clinical application. Transplant International 14:1, 1-5
    CrossRef

39. 39

    Amrik Sahota, Sujuan Gao, John Hayes, Rahul M Jindal. (2000) Microchimerism and rejection: a meta-analysis. Clinical Transplantation 14:4, 345-350
    CrossRef

40. 40

    S. Löffeler, D. Meyer, C. Otto, H.-J. Gassel, W. Timmermann, K. Ulrichs, A. Thiede. (2000) Different kinetics of donor cell populations after isolated liver and combined liver/small bowel transplantation. Transplant International 13:S1, S537-S540
    CrossRef

41. 41

    Krovvidi S. R. SivaSai, Martin Jendrisak, Brian F. Duffy, Donna Phelan, Mark Ravenscraft, Todd Howard, T. Mohanakumar. (2000) CHIMERISM IN PERIPHERAL BLOOD OF SENSITIZED PATIENTS WAITING FOR RENAL TRANSPLANTATION1,2. Transplantation 69:4, 538-544
    CrossRef

42. 42

    K.J. Kao. (2000) Mechanisms and new approaches for the allogeneic blood transfusion-induced immunomodulatory effects. Transfusion Medicine Reviews 14:1, 12-22
    CrossRef

43. 43

    Saiho Ko, Andrea Deiwick, Mark D. Jäger, Astrid Dinkel, Frank Rohde, Rainer Fischer, Tung-Yu Tsui, Karl L. Rittmann, Kurt Wonigeit, Hans J. Schlitt. (1999) The functional relevance of passenger leukocytes and microchimerism for heart allograft acceptance in the rat. Nature Medicine 5:11, 1292-1297
    CrossRef

44. 44

    Thomas Wekerle, Megan Sykes. (1999) MIXED CHIMERISM AS AN APPROACH FOR THE INDUCTION OF TRANSPLANTATION TOLERANCE1. Transplantation 68:4, 459-467
    CrossRef

45. 45

    PJ Horton, A Handa, SEF Marshall, KI Welsh. (1999) Donor-specific bone marrow and long-term survival of allogeneic arm transplant. The Lancet 354:9176, 424-425
    CrossRef

46. 46

    Y. Fuchimoto, C. Huang, A. Shimizu, J. Seebach, S. Arn, D.h. Sachs. (1999) An allelic non-histocompatibility antigen with wide tissue distribution as a marker for chimerism in pigs. Tissue Antigens 54:1, 43-52
    CrossRef

47. 47

    T. SATO, A. DEIWICK, G. RADDATZ, K. KOYAMA, H. J. SCHLITT. (1999) Interactions of allogeneic human mononuclear cells in the two-way mixed leucocyte culture (MLC): influence of cell numbers, subpopulations and cyclosporin. Clinical and Experimental Immunology 115:2, 301-308
    CrossRef

48. 48

    Hirofumi Ota, Mitsukazu Gotoh, Hiroki Ohzato, Li He, Takahiko Tanigawa, Hiroaki Nagano, Keizo Dono, Yutaka Takeda, Masaki Okuyama, Junzo Shimizu, Koji Umeshita, Shoji Nakamori, Masato Sakon, Isamu Nishisho, Morito Monden. (1999) MICROCHIMERISM IN THYMUS IS ASSOCIATED WITH UP-REGULATED T HELPER TYPE 1 CYTOKINE TRANSCRIPTION DURING CARDIAC ALLOGRAFT REJECTION IN RATS1,2. Transplantation 67:1, 165-173
    CrossRef

49. 49

    Peta J. O'Connell, Adamma Mba-Jonas, Glen E. Leverson, Dennis M. Heisey, Keith C. Meyer, Robert B. Love, William J. Burlingham. (1998) STABLE LUNG ALLOGRAFT OUTCOME CORRELATES WITH THE PRESENCE OF INTRAGRAFT DONOR-DERIVED LEUKOCYTES1. Transplantation 66:9, 1167-1174
    CrossRef

50. 50

    Kamal M. Okasha, Taher A. Al-Tweigeri, Alfonso V. Jurado, Ahmed S. Shoker. (1998) ANALYSIS OF THE RELATIONSHIP BETWEEN CHIMERISM AND THE ALLOGENEIC HUMORAL RESPONSE1. Transplantation 66:8, 1028-1034
    CrossRef

51. 51

    Masanobu Terakura, Noriko Murase, Anthony J. Demetris, Qing Ye, Angus W. Thomson, Thomas E. Starzl. (1998) LYMPHOID/NONLYMPHOID COMPARTMENTALIZATION OF DONOR LEUKOCYTE CHIMERISM IN RAT RECIPIENTS OF HEART ALLOGRAFTS, WITH OR WITHOUT ADJUNCT BONE MARROW1. Transplantation 66:3, 350-357
    CrossRef

52. 52

    F. Navarro, P. Portalès, J. P. Pageaux, P. F. Perrigault, J. M. F. Fabre, J. Domergue, J. Clot. (1998) Activated sub-populations of lymphocytes and natural killer cells in normal liver and liver grafts before transplantation. Liver 18:4, 259-263
    CrossRef

53. 53

    John Devlin, Derek Doherty, Linda Thomson, Terence Wong, Peter Donaldson, Bernard Portmann, Roger Williams. (1998) Defining the outcome of immunosuppression withdrawal after liver transplantation. Hepatology 27:4, 926-933
    CrossRef

54. 54

    Barbara j van der Mast, Nicole M van Besouw, Bouke G Hepkema, Willem Weimar, Aad P van de Berg, Maarten JH Slooff, Frans HJ Claas. (1998) Mutual tolerance after liver and not after heart transplantation? Evaluation of patient-anti-donor and donor-anti-patient responses by mixed lymphocyte culture. Transplant Immunology 6:1, 33-38
    CrossRef

55. 55

    Arthur J Matas. (1998) Risk factors for chronic rejection - a clinical perspective. Transplant Immunology 6:1, 1-11
    CrossRef

56. 56

    IRVIN PARADIS. (1998) Bronchiolitis Obliterans: Pathogenesis, Prevention, and Management. The American Journal of the Medical Sciences 315:3, 161-178
    CrossRef

57. 57

    John F. Valente, J. Wesley Alexander. (1998) IMMUNOBIOLOGY OF RENAL TRANSPLANTATION. Surgical Clinics of North America 78:1, 1-26
    CrossRef

58. 58

    Anneke De Vries-Van Der Zwan, Arit C. Besseling, Marjolein A. Van Der Pol, Leo P. De Waal, Claire J. P. Boog. (1998) Specific Tolerance Induction and Organ Transplantation. Leukemia & Lymphoma 31:1-2, 131-142
    CrossRef

59. 59

    Haval Shirwan, Guo D. Wu, Luqman Barwari, Allen Liu, Donald V. Cramer. (1997) INDUCTION OF ALLOGRAFT NONRESPONSIVENESS AFTER INTRATHYMIC INOCULATION WITH DONOR CLASS I ALLOPEPTIDES. Transplantation 64:12, 1671-1676
    CrossRef

60. 60

    Boris Nikolic, Megan Sykes. (1997) Bone marrow chimerism and transplantation tolerance. Current Opinion in Immunology 9:5, 634-640
    CrossRef

61. 61

    Krovvidi S.R. Sivasai, Yael G. Alevy, Brian F. Duffy, Daniel C. Brennan, Gary G. Singer, Surendra Shenoy, Jeffrey A. Lowell, Todd Howard, T. Mohanakumar. (1997) PERIPHERAL BLOOD MICROCHIMERISM IN HUMAN LIVER AND RENAL TRANSPLANT RECIPIENTS. Transplantation 64:3, 427-432
    CrossRef

62. 62

    J SMITH. (1997) Use of allogeneic bone marrow labeled with neomycin resistance gene to examine bone marrow-derived chimerism in experimental organ transplantation. Cell Transplantation 6:4, 369-376
    CrossRef

63. 63

    C. Knoop, M. Andrien, V. Defleur, M. Antoine, P. de Francquen, M. Goldman, M. Estenne. (1997) LUNG REJECTION OCCURS IN LUNG TRANSPLANT RECIPIENTS WITH BLOOD CHIMERISM1. Transplantation 64:1, 167-169
    CrossRef

64. 64

    Rainer W.G. Gruessner, Fatih M. Uckun, Jacques Pirenne, Raouf E. Nakhleh, Enrico Benedetti, Ihor Bekersky, Christoph Troppmann, Angelika C. Gruessner. (1997) RECIPIENT PRECONDITIONING AND DONOR-SPECIFIC BONE MARROW INFUSION IN A PIG MODEL OF TOTAL BOWEL TRANSPLANTATION. Transplantation 63:1, 12-20
    CrossRef

65. 65

    George V. Mazariegos, Jorge Reyes, Ignazio R. Marino, Anthony J. Demetris, Bridget Flynn, William Irish, John McMichael, John J. Fung, Thomas E. Starzl. (1997) WEANING OF IMMUNOSUPPRESSION IN LIVER TRANSPLANT RECIPIENTS12. Transplantation 63:2, 243-249
    CrossRef

66. 66

    Jacques Pirenne, Angelika C Gruessner, Enrico Benedetti, Christoph Troppmann, Raouf E Nakhleh, Fatih M Uckun, Rainer W.G Gruessner. (1997) Donor-specific unmodified bone marrow transfusion does not facilitate intestinal engraftment after bowel transplantation in a porcine model. Surgery 121:1, 79-88
    CrossRef

67. 67

    Cynthia McSherry, Annette Jackson, Marshall I. Hertz, R. Morton Bolman, Kay Savik, Nancy L. Reinsmoen. (1996) SEQUENTIAL MEASUREMENT OF PERIPHERAL BLOOD ALLOGENEIC MICROCHIMERISM LEVELS AND ASSOCIATION WITH PULMONARY FUNCTION1. Transplantation 62:12, 1811-1818
    CrossRef

68. 68

    Kimikazu Hamano, Mary-Anne Rawsthorne, Andrew R. Bushell, Peter J. Morris, Kathryn J. Wood. (1996) EVIDENCE THAT THE CONTINUED PRESENCE OF THE ORGAN GRAFT AND NOT PERIPHERAL DONOR MICROCHIMERISM IS ESSENTIAL FOR MAINTENANCE OF TOLERANCE TO ALLOANTIGEN IN VIVO IN ANTI-CD4 TREATED RECIPIENTS1,2. Transplantation 62:6, 856-860
    CrossRef

69. 69

    Thomas E. Starzl, Noriko Murase, Anthony J. Demetris, Shiguang Qian. (1996) MICROCHIMERISM: INACCURATE LITERATURE CITATIONS. Transplantation 62:5, 703
    CrossRef

70. 70

    F. Fandrich, T. Jahnke, J. Peters, B. Exner, A. Papachrysanthou, N. Zavazava. (1996) Circumvention of natural killer cell and T-cell mediated allogeneic target killing with tacrolimus (FK506) in small bowel transplantation related graft-vs-host disease. Transplant International 9:s1, S263-S268
    CrossRef

71. 71

    Hideki Ishida, Tatsuo Kawai, Kazunari Tanabe, Yutaro Hayasaka, Mineko Yasuo, Hiroshi Toma, Kazuo Ota. (1996) STATUS OF MICROCHIMERISM IN RECIPIENTS 15 YEARS AFTER LIVING RELATED KIDNEY TRANSPLANTATION. Transplantation 62:1, 126-128
    CrossRef

72. 72

    Haval Shirwan, Hong K. Wang, Luqman Barwari, Leonard Makowka, Donald V. Cramer. (1996) PRETRANSPLANT INJECTION OF ALLOGRAFT RECIPIENTS WITH DONOR BLOOD OR LYMPHOCYTES PERMITS ALLOGRAFT TOLERANCE WITHOUT THE PRESENCE OF PERSISTENT DONOR MICROCHIMERISM1. Transplantation 61:9, 1382-1386
    CrossRef

73. 73

    Jean P. Molleston, Yael G. Alevy, Krovvidi S. R. SivaSai, T. Mohankumar, Todd K. Howard. (1996) EVIDENCE THAT PEDIATRIC LIVER TRANSPLANT RECIPIENTS MAY UNDERGO LATE REJECTION EPISODES IN SPITE OF DONOR-SPECIFIC MICROCHIMERISM1. Transplantation 61:4, 656,657
    CrossRef

74. 74

    Andrew Bushell, Thomas C. Pearson, Peter J. Morris, Kathryn J. Wood. (1996) DONOR-RECIPIENT MICROCHIMERISM AND TOLERANCE INDUCTION (REPLY). Transplantation 61:1, 170171
    CrossRef

75. 75

    Michiyoshi Hisanaga, Joachim Hundrieser, Klaus B??ker, Kay Uthoff, Gereon Raddatz, Thorsten Wahlers, Kurt Wonigeit, Rudolf Pichlmayr, Hans J??rgen Schlitt. (1996) DEVELOPMENT, STABILITY, AND CLINICAL CORRELATIONS OF ALLOGENEIC MICROCHIMERISM AFTER SOLID ORGAN TRANSPLANTATION1. Transplantation 61:1, 40-45
    CrossRef

76. 76

    Hans Jürgen Schlitt, Sabine Schäfers, Andrea Deiwick, Kai-Uwe Eckardt, Torsten Pietsch, Wolfram Ebell, Björn Nashan, Burckhardt Ringe, Kurt Wonigeit, Rudolf Pichlmayr. (1995) Extramedullary erythropoiesis in human liver grafts. Hepatology 21:3, 689-696
    CrossRef

77. 77

    Nancy L. Ascher. (1995) Microchimerism in organ transplantation. Liver Transplantation and Surgery 1:1, 43-46
    CrossRef

78. 78

    Nancy L. Reinsmoen, Cynthia McSherry, Blanche Chavers, Marshall I. Hertz, Arthur J. Matas. (1995) Correlation of donor antigen-specific hyporeactivity with allogeneic microchimerism in kidney and lung recipients. Pediatric Nephrology 9:S1, S35-S39
    CrossRef

79. 79

    Sophie Caillat-Zucman, Christophe Legendre, Caroline Suberbielle, Christine Bodemer, Laure-Hélène Noël, Henri Kreis, Jean-François Bach. (1994) Microchimerism frequency two to thirty years after cadaveric kidney transplantation. Human Immunology 41:1, 91-95
    CrossRef

80. 80

    H.J Schlitt, J Hundrieser, M Hisanaga, K Wonigeit, R Pichlmayr, K Uthoff, M Karck, T Wahlers. (1994) Patterns of donor-type microchimerism after heart transplantation. The Lancet 343:8911, 1469-1471
    CrossRef