Skip to main content

Advertisement

Log in

The efficiency of humoral immune transfer depends on both the graft and the immunosuppressive treatment

  • Original Article
  • Published:
Transplant International

Abstract

The present study was designed to compare the efficiency of adoptive transfer of humoral immunity after liver, kidney, and heart transplantation in relation to the number of passenger lymphocytes, and to estimate the risk of a detrimental effect and the chance of a beneficial effect. Hepatitis B virus surface-antigen-vaccinated brown Norway rats (BNs) and AxC 9935 Irish (ACI rats) served as donors, and naïve Lewis (LEW) rats as recipients. The liver grafts contained 100 times more passenger lymphocytes than heart grafts, and the kidney grafts approximately ten times more, indicated by monoclonal CD45 antibody staining. Transient anti-HBs immunity did occur after transplantation of all three organ grafts. In all rejecting groups, the serum recipient-to-donor anti-HBs titer ratio (R/D ratio) was below 0.10%, with heart recipients showing half the level (0.05%) of liver recipients (0.09%). Under immunosuppression, R/D ratio doubled in liver or kidney recipients, but remained unaffected in heart recipients. Immune transfer was most efficient in immune-suppressed liver recipients in the spontaneously tolerant strain combination as indicated by a significantly higher R/D ratio (0.32%) and a longer titer persistence (up to 9 weeks) than in all other groups. Therefore, mainly liver and kidney graft recipients carry a risk, but also a chance of benefiting from the transfer of donor-derived immunity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

References

  1. Ahmed KY, Nunn G, Brazier DM, Bird GW, Crockett RE (1987) Hemolytic anemia resulting from autoantibodies produced by the donor's lymphocytes after renal transplantation. Transplantation 43:163–164

    CAS  PubMed  Google Scholar 

  2. Aikawa A, Yamashita M, Arai K, Hirayama N, Ohara T, Hasegawa A (1996) Degree and sequential change of peripheral blood microchimerism in renal transplant recipients. Transplant Proc 28:1288–1290

    CAS  PubMed  Google Scholar 

  3. Bird GW, Wingham J (1980) Anti-A autoantibodies with unusual properties in a patient on renal dialysis. Immunol Commun 9:155–159

    CAS  PubMed  Google Scholar 

  4. Bracey AW (1987) Anti-A of donor lymphocyte origin in three recipients of organs from the same donor. Vox Sang 53:181–183

    CAS  PubMed  Google Scholar 

  5. Brecher ME, Moore SB, Reisner RK, Rakela J, Krom RA (1989) Delayed hemolysis resulting from anti-A1 after liver transplantation. Am J Clin Pathol 91:232–235

    CAS  PubMed  Google Scholar 

  6. Burroughs AK (2000). Posttransplantation prevention and treatment of recurrent hepatitis C. Liver Transpl 6 [Suppl 2]:35–40

    Google Scholar 

  7. Ciancio G, Miller J, Garcia-Morales RO, Carreno M, Burke GW, III, Roth D (2001) Six-year clinical effect of donor bone marrow infusions in renal transplant patients. Transplantation 71:827–835

    CAS  PubMed  Google Scholar 

  8. Dahmen U, Li J, Dirsch O, Gu YL, Polywka S, Doebel L, Shen K, Broelsch CE (2003) Viral Hepatitis 10: (in press)

  9. Elwood ET, Larsen CP, Maurer DH, Routenberg KL, Neylan JF, Whelchel JD (1997) Microchimerism and rejection in clinical transplantation. Lancet 349:1358–1360

    Article  CAS  PubMed  Google Scholar 

  10. Friend PJ, McCarthy LJ, Filo RS, Leapman SB, Pescovitz MD, Lumeng L (1990) Transmission of idiopathic (autoimmune) thrombocytopenic purpura by liver transplantation. N Engl J Med 323:807–811

    CAS  PubMed  Google Scholar 

  11. Gottlieb DJ, Cryz SJ Jr, Furer E, Que JU, Prentice HG, Duncombe AS (1990) Immunity againstPseudomonas aeruginosa adoptively transferred to bone marrow transplant recipients. Blood 76:2470–2475

    CAS  PubMed  Google Scholar 

  12. Ilan Y, Nagler A, Adler R, Tur-Kaspa R, Slavin S, Shouval D (1993) Ablation of persistent hepatitis B by bone marrow transplantation from a hepatitis B-immune donor. Gastroenterology 104:1818–1821

    CAS  PubMed  Google Scholar 

  13. Jacobs LB, Shirey RS, Ness PM (1996) Hemolysis due to the simultaneous occurrence of passenger lymphocyte syndrome and a delayed hemolytic transfusion reaction in a liver transplant patient. Arch Pathol Lab Med 120:684–686

    CAS  PubMed  Google Scholar 

  14. Jilg W, Schmidt M, Deinhardt F (1989) A four-year experience with a recombinant hepatitis B vaccine. Infection 17:70–76

    CAS  PubMed  Google Scholar 

  15. Kamada N, Calne RY (1983) A surgical experience with five hundred thirty liver transplants in the rat. Surgery 93:64–69

    CAS  PubMed  Google Scholar 

  16. Kato S, Yabe H, Yabe M, Kimura M, Ito M, Tsuchida F (1990) Studies on transfer of varicella-zoster-virus specific T-cell immunity from bone marrow donor to recipient. Blood 75:806–809

    CAS  PubMed  Google Scholar 

  17. Lau GK, Lok AS, Liang RH, Lai CL, Chiu EK, Lau YL (1997) Clearance of hepatitis B surface antigen after bone marrow transplantation: role of adoptive immunity transfer. Hepatology 25:1497–1501

    CAS  PubMed  Google Scholar 

  18. Lee S, Willoughby WF, Smallwood CJ, Dawson A, Orloff MJ (1970) Heterotopic heart and lung transplantation in the rat. Am J Pathol 5:279–298

    Google Scholar 

  19. Legendre C, Caillat-Zucman S, Samuel D, Morelon S, Bismuth H, Bach JF (1997) Transfer of symptomatic peanut allergy to the recipient of a combined liver-and-kidney transplant. N Engl J Med 337:822–824

    Article  CAS  PubMed  Google Scholar 

  20. Leroux-Roels G, Abraham B, Fourneau M, De Clercq N, Safary A (2000) A comparison of two commercial recombinant vaccines for hepatitis B in adolescents. Vaccine 19:937–942

    Article  CAS  PubMed  Google Scholar 

  21. Li FK, Chan TM, Lai KN (2000) Alloimmune hemolysis after renal transplantation. Am J Nephrol 20:473–475

    Article  CAS  PubMed  Google Scholar 

  22. Lundgren G, Asaba H, Bergstrom J, Groth CG, Magnusson G, Moller E (1981) Fulminating anti-A autoimmune hemolysis with anuria in a renal transplant recipient: a therapeutic role of plasma exchange. Clin Nephrol 16:211–214

    PubMed  Google Scholar 

  23. Mangal AK, Growe GH, Sinclair M, Stillwell GF, Reeve CE, Naiman SC (1984) Acquired hemolytic anemia due to "auto"-anti-A or "auto"-anti-B induced by group O homograft in renal transplant recipients. Transfusion 24:201–205

    PubMed  Google Scholar 

  24. Masaki Y, Hirasawa A, Okuyama S, Tsujimoto G, Iwaya M, Li XK (1995) Microchimerism and heart allograft acceptance. Transplant Proc 27:148–150

    CAS  PubMed  Google Scholar 

  25. Morbidity and Mortality Weekly Report (1987) Update on hepatitis B prevention. MMWR Morb Mortal Wkly Rep 36:353–360, 366

    PubMed  Google Scholar 

  26. Oesterwitz H, Althaus P (1982) Orthotopic kidney transplantation in the rat with non-splinted end-to-end ureteric anastomosis: details of a technique. Urol Res 10:149–152

    CAS  PubMed  Google Scholar 

  27. Okamura R, Tanaka K, Asonuma K, Uemoto S, Katayama T, Tanaka M (1989) Immunological treatment with low dosage ciclosporin in rat liver allotransplantation. Eur Surg Res 21:235–242

    CAS  PubMed  Google Scholar 

  28. Orchard J, Young NT, Smith C, Thomas S, Darke C. (1990) Severe intravascular haemolysis in a renal transplant recipient due to anti-B of donor origin. Vox Sang 59:172–175

    CAS  PubMed  Google Scholar 

  29. Ostrow DH, Edwards B, Kimes D, Macioszek J, Irace H, Nelson L (1991) Quantitation of hepatitis B surface antibody by an automated microparticle enzyme immunoassay. J Virol Methods 32:265–276

    Article  CAS  PubMed  Google Scholar 

  30. Pausch V, Speiser P (1987) Hemolytic graft versus host reaction cause by immune "auto"-anti A1 formation in an A1 recipient following transplantation of an O kidney. With a review of studies up to now from the literature. Wien Klin Wochenschr 99:517–525

    CAS  PubMed  Google Scholar 

  31. Ramsey G (1991) Red cell antibodies arising from solid organ transplants. Transfusion 31:76–86

    CAS  PubMed  Google Scholar 

  32. Ramsey G, Cornell FW, Hahn LF, Larson P, Issitt LB, Starzl TE (1989) Red cell antibody problems in 1000 liver transplants. Transfusion 29:396–400

    CAS  PubMed  Google Scholar 

  33. Rizzetto M, Marzano A (2000) Posttransplantation prevention and treatment of recurrent hepatitis B. Liver Transpl 6 [Suppl 2]:47–51

    Google Scholar 

  34. Salamon DJ, Ramsey G, Nusbacher J, Yang S, Starzl TE, Israel L (1985) Anti-A production by a group O spleen transplanted to a group A recipient. Vox Sang 48:309–312

    CAS  PubMed  Google Scholar 

  35. Saxon A, Mitsuyasu R, Stevens R, Champlin RE, Kimata H, Gale RP (1986). Designed transfer of specific immune responses with bone marrow transplantation. J Clin Invest 78:959–967

    CAS  PubMed  Google Scholar 

  36. Shapiro R, Rao AS, Corry RJ, Valenti M, Zeevi A, Jordan ML (2001) Kidney transplantation with bone marrow augmentation: five-year outcomes Transplant Proc 33:1134–1135

    Article  CAS  Google Scholar 

  37. Shouval D, Ilan Y (1995). Immunization against hepatitis B through adoptive transfer of immunity. Intervirology 38:41–46

    CAS  PubMed  Google Scholar 

  38. Shouval D, Adler R, Ilan Y (1993) Adoptive transfer of immunity to hepatitis B virus in mice by bone marrow transplantation from immune donors. Hepatology 17:955–959

    CAS  PubMed  Google Scholar 

  39. Swanson JL, Sastamoinen RM, Steeper TA, Sebring ES (1987) Gm allotyping to determine the origin of red cell antibodies in recipients of solid organ transplants. Vox Sang 52:75–78

    CAS  PubMed  Google Scholar 

  40. Taaning E Jacobsen N (1994) Platelet transfusion refractoriness due to graft-derived anti-HPA-2b production after allogeneic bone-marrow transplantation. Transplant Proc 26:1826

    CAS  PubMed  Google Scholar 

  41. Taaning E, Morling N, Mortensen SA, Pettersson G, Simonsen AC (1994) Hemolytic anemia due to graft-derived anti-B production after lung transplantation. Transplant Proc 26:1739

    CAS  PubMed  Google Scholar 

  42. Tanner JE, Alfieri C (2001) The Epstein-Barr virus and post-transplant lymphoproliferative disease: interplay of immunosuppression, EBV, and the immune system in disease pathogenesis. Transpl Infect Dis 3:60–69

    Article  CAS  PubMed  Google Scholar 

  43. Van der Bij, Speich R (2001) Management of cytomegalovirus infection and disease after solid-organ transplantation. Clin Infect Dis 33 [Suppl 1]:32–37

  44. Vathsala A (1999) Viral hepatitis in renal transplantation. Transplant Proc 31:337–339

    Article  CAS  PubMed  Google Scholar 

  45. Winston DJ, Ho WG, Schiffman G, Champlin RE, Feig SA, Gale RP (1983) Pneumococcal vaccination of recipients of bone marrow transplants. Arch Intern Med 143:1735–1737

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Uta Dahmen.

About this article

Cite this article

Dahmen, U., Li, J., Gu, Y. et al. The efficiency of humoral immune transfer depends on both the graft and the immunosuppressive treatment. Transpl Int 16, 161–167 (2003). https://doi.org/10.1007/s00147-002-0518-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00147-002-0518-6

Keywords

Navigation