Correspondence
Donor T Cells to Treat EBV-Associated Lymphoma
N Engl J Med 1994; 331:679-680September 8, 1994
- Article
To the Editor:
Papadopoulos et al. (April 28 issue)1 report complete remission in five patients who received unmanipulated donor T cells as therapy for Epstein-Barr virus (EBV)-associated lymphoproliferation after allogeneic bone marrow transplantation. We have administered donor T cells to a patient in whom this complication developed, and we agree that this therapy produces clinical responses. However, its wider application may be limited by substantial toxicity.
A three-year-old boy with juvenile chronic myeloid leukemia presented with fevers, pulmonary nodules, and retroperitoneal lymphadenopathy eight months after the transplantation of T-cell-depleted bone marrow, with two mismatched antigens, from his brother. A biopsy confirmed immunoblastic lymphoma, and EBV was detected in the tumor by amplification of viral DNA with the polymerase chain reaction and by immunofluorescence staining for the viral antigens LMP-1 and EBNA-2. His disease progressed rapidly, and he received 106 CD3+ T cells per kilogram of body weight from his donor and had resolution of fevers and nodules over the next 6 to 10 weeks. However, grade IV graft-versus-host disease (GVHD) of his skin, gastrointestinal tract, and liver also developed, which responded to high-dose methylprednisolone and antithymocyte globulin.
Although our patient remains in complete remission 16 months after T-cell therapy and his GVHD is now quiescent, his therapy was associated with substantial morbidity. In addition, two patients in the report of Papadopoulos et al. died of pneumonitis, suggesting that the treatment of established disease may result in lethal inflammatory responses in affected organs. An infusion of unmanipulated donor lymphocytes inevitably includes alloreactive T cells that can induce both these complications. Therefore, we have begun to use EBV-specific cytotoxic T lymphocytes to mediate an antilymphoproliferative effect in the absence of GVHD2.
2 ReferencesHelen E. Heslop, M.D.
Malcolm K. Brenner, M.B.
Cliona M. Rooney, Ph.D.
St. Jude Children's Research Hospital, Memphis, TN 381031
Papadopoulos EB ,Ladanyi M ,Emanuel D , et al. Infusions of donor leukocytes to treat Epstein-Barr virus-associated lymphoproliferative disorders after allogeneic bone marrow transplantation. N Engl J Med 1994;330:1185-1191
Full Text | Web of Science | Medline2
Heslop HE ,Brenner MK ,Rooney CM , et al. Clinical Protocol: administration of neomycin resistance gene marked EBV specific cytotoxic T lymphocytes to recipients of mismatched-related or phenotypically similar unrelated donor marrow grafts. Hum Gene Ther 1994;5:381-397
CrossRef | Web of Science | Medline
Author/Editor Response
The authors reply:
To the Editor: The case reported by Heslop and colleagues again confirms the efficacy of infusions of unirradiated donor leukocytes in the treatment of EBV-associated lymphomas that complicate allogeneic marrow grafts, but they correctly point out that these infusions may also contain alloreactive T cells capable of initiating GVHD. Unlike our patients, all of whom received HLA-identical grafts, the patient described by Heslop et al. received a graft with a two-antigen mismatch. Since the frequency of alloreactive T-cell precursors capable of recognizing the major HLA alloantigens exponentially exceeds the frequencies of T-cell precursors reactive to minor alloantigens,1 severe GVHD is not unexpected.
For these reasons, we fully concur with Heslop et al. that infusions of cloned EBV-specific effectors, depleted of alloreactive T cells, should circumvent the risk of GVHD, as has already been demonstrated in phase 1 studies of cloned cytomegalovirus-specific T cells2. However, such an approach presents substantial logistic difficulties, since in this disease the progression from diagnosis to death is generally rapid. The approach requires the establishment of EBV-transformed donor B-cell lines for use as stimulators and the subsequent development and expansion of EBV-specific T-cell clones without alloreactivity. Moreover, it is unclear whether EBV-specific cytotoxic cells alone can eradicate these lymphomas or whether additional factors are required from helper cells, natural killer cells, or lymphokine-activated killer cells.
An alternate, more rapid approach developed by Servida et al.3 involves the use of T cells sensitized to donor EBV-lymphoblastoid cell lines in vitro and genetically modified to express both a novel surface marker for the selection of effectors and a thymine kinase gene that induces their sensitivity to ganciclovir3,4.
Heslop et al. also express concern about the inflammatory potential of the donor leukocyte infusions and their contribution to lethal pneumonia in two of our patients. In both patients, extensive pulmonary infiltrates and respiratory compromise preceded the leukocyte infusions. Furthermore, their respiratory status did not change during the first two to three days after the infusion. Nevertheless, we cannot absolutely rule out the possibility that a cytotoxic reaction produced by the effector cells contributed to the pulmonary insufficiency. However, there is no reason to expect that preactivated, EBV-specific cytotoxic T cells selected in vitro will be any less likely to induce an inflammatory reaction.
4 ReferencesEsperanza B. Papadopoulos, M.D.
Richard J. O'Reilly, M.D.
Memorial Sloan-Kettering Cancer Center, New York, NY 100211
Kaminski E ,Hows J ,Man S , et al. Prediction of graft versus host disease by frequency analysis of cytotoxic T cells after unrelated donor bone marrow transplantation. Transplantation 1989;48:608-613
Web of Science | Medline2
Riddell SR ,Watanabe KS ,Goodrich JM ,Li CR ,Agha ME ,Greenberg PD . Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones. Science 1992;257:238-241
CrossRef | Web of Science | Medline3
Servida P ,Rossini S ,Traversari C , et al. Gene transfer into peripheral blood lymphocytes for in vivo immunomodulation of donor anti-tumor immunity in a patient affected by EBV-induced lymphoma. Blood 1993;82:Suppl 1:214a-214a abstract.
Web of Science4
Mavilio F ,Ferrari G ,Rossini S , et al. Peripheral blood lymphocytes as target cells of retroviral vector-mediated gene transfer. Blood 1994;83:1988-1997
Web of Science | Medline
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