Original Article
Anti–B-Cell Monoclonal Antibodies in the Treatment of Severe B-Cell Lymphoproliferative Syndrome Following Bone Marrow and Organ Transplantation
N Engl J Med 1991; 324:1451-1456May 23, 1991
- Abstract
- Abstract
Background.
The B-cell lymphoproliferative syndrome is an infrequent life-threatening complication of marrow or organ transplantation that is the consequence of profound immunosuppression. The results of treatment have been disappointing, although a small number of patients have been cured by chemoradiotherapy or antiviral agents after a reduction in the dosage of immunosuppressive therapy. We report here the results of treating this disorder with anti—B-cell antibodies.
Methods.
Twenty-six patients in whom aggressive B-cell lymphoproliferative syndrome developed after bone marrow (n = 14) or organ (n = 12) transplantation received 0.2 mg of CD21 -specific and of CD24-specific antibodies per kilogram of body weight for 10 consecutive days in an open, prospective, multicenter trial.
Results.
The treatment was well tolerated. All patients had transient neutropenia, apparently because the CD24 molecule is also expressed on granulocytes. The treatment was ineffective in seven patients with monoclonal B-cell proliferation. In contrast, 16 patients with oligoclonal B-cell proliferation had complete remission. Systemic remission also occurred in two other patients with oligoclonal proliferation who had central nervous system involvement, although they subsequently died because of progression of the central nervous system disease. In one patient who died early, clonality was not determined. Of the 16 patients who had complete remission, 2 with persistent immunodeficiency due to graft (marrow) rejection or acute graft-versus-host disease had a relapse, and the 1 with graft-versus-host disease subsequently died. Eleven patients were alive and disease-free after a median follow-up of 35 months (5 of 14 marrow recipients and 6 of 12 organ recipients). Four other patients in complete remission died of unrelated causes 4 to 12 months after treatment.
Conclusions.
Intravenous administration of anti—B-cell antibodies may be effective in controlling diffuse, severe, oligoclonal B-cell proliferation not involving the central nervous system. (N Engl J Med 1991; 324: 1451–6.)
Media in This Article
Figure 1
Outcome in Patients with Oligoclonal B-Cell Lymphoproliferative Syndrome Treated with Anti—B-Cell Antibodies.Figure 2Actuarial Survival of 26 Patients with B-Cell Lymphopro-liferative Syndrome (BLPS) Treated with Anti—B-Cell Antibodies.
Article Activity
- Article
THE B-cell lymphoproliferative syndrome is an infrequent complication of marrow or organ transplantation. Epstein–Barr virus (EBV) has been found to induce such uncontrolled proliferation of B cells in patients who are immunodeficient.1 2 3 4 The clinical presentation varies from self-limited infectious mononucleosis to diffuse polyclonal or oligoclonal lymphoid proliferation to lymphoma.1 , 5 Host immunosuppression is the chief predisposing factor.6 , 7 The B-cell lymphoproliferative syndrome has been reported in 0.23 to 0.45 percent of recipients of HLA-identical bone marrow.8 , 9 Patients at risk were those who had severe graft-versus-host disease treated with anti-CD3 antibodies.8 , 9 Recipients of either HLA-matched transplants from unrelated donors or HLA-mismatched transplants are prone to the development of B-cell lymphoproliferative syndrome because of the occurrence of profound and long-term immunodeficiency. The syndrome has developed in 1 of 10 and 2 of 55 recipients of matched transplants from unrelated donors and in 6 of 25 and 7 of 80 recipients of HLA-nonidentical transplants depleted of T cells, according to various reports.8 9 10 11 In addition, 6 of 420 recipients of HLA-nonidentical transplants not depleted of T cells have been described with this complication.9
After organ transplantation, most cases of B-cell lymphoproliferative syndrome occur in patients with repeated rejection requiring immunosuppressive treatment with high-dose steroids, antithymocyte globulins, or monoclonal antibodies.1 The frequency of the syndrome after organ transplantation is estimated to be between 0.6 and 5 percent.1 , 2 According to one report, for example, the syndrome developed in 20 of 1467 recipients of liver transplants.12
The prognosis of B-cell lymphoproliferative syndrome is extremely poor in recipients of bone marrow transplants: there have been 29 deaths among 32 reported cases.8 9 10 11 After organ transplantation, about 40 percent of patients with the syndrome survive,1 , 12 either because of spontaneous resolution after the cessation of immunosuppressive therapy or possibly because of the efficacy of acyclovir,13 , 14 ganciclovir,15 or chemoradiotherapy in a very small number of patients with lymphoma.16 Interferon alfa together with gamma globulin produced promising results in five patients.16 In a preliminary report,17 we described remission after treatment with a combination of anti—B-cell antibodies in two patients in whom oligoclonal B-cell lymphoproliferative syndrome developed after bone marrow transplantation. We now report the results of an open, multicenter, prospective study of the use of the same antibodies (specific for CD21 and CD24) in 26 patients in whom the syndrome developed after bone marrow or organ transplantation.
Methods
Immunologic Investigations
The B-cell—specific antibodies used to characterize B cells in blood and biopsy samples of marrow and organ tissue when available included anti-immunoglobulin heavy-chain and light-chain isotype antibodies,17 ALB9 (CD24), BL13 (CD21), and IOB8 (Immunotech, CD23). Analyses were performed by indirect immunofluorescence, cytofluorometry, or light microscopy. Membrane immunofluorescence was analyzed on fresh cells, and intracytoplasmic fluorescence on fixed cells. Serum immunoglobulin levels were measured by nephelometry, and monoclonal immunoglobulin components by immunofixation.18 Immunoperoxidase staining of biopsy sections was performed as described elsewhere.19 Antimouse immunoglobulin antibodies were detected with a direct enzyme-linked immunosorbent assay.20
Patients
We treated 26 patients from 11 centers in whom B-cell lymphoproliferative syndrome developed after bone marrow or organ transplantation. The study includes two previously reported cases.17 The characteristics of the patients are described in Table 1Table 1
Characteristics of the Patients.*. Bone marrow donors were either HLA-nonidentical parents or HLA-matched unrelated donors. Rejection episodes requiring aggressive immuno-suppression (OKT3 used for three episodes, high-dose methylprednisolone used for eight, and antithymocyte globulins used for one) occurred in 10 of the 12 organ recipients in whom the syndrome developed.The B-cell lymphoproliferative syndrome was diagnosed on the basis of a finding of diffuse B-cell hyperplasia characterized by invasion of blood vessels and other organ structures, with disorganization of the nodal structure in lymph nodes.2 Lymphoplasmacytoid or lymphoblastic cells, together with small cells, predominated. Atypical cells and necrosis were noted in 9 of 10 patients after organ transplantation.
The clinical and laboratory features of the B-cell lymphoproliferative syndrome in these patients are shown in Table 2Table 2
Clinical and Biologic Characteristics of B-Cell Lymphoproliferative Syndrome.. The syndrome was found in a number of locations in 24 of the 26 patients. EBV was detected in 19 patients by hybridization with specific probes.21 Specific antibodies against EBV (viral-capsid antigen, early antigen, and Epstein–Barr nuclear antigen) were detected by an enzyme-linked immunosorbent assay in 8 of 26 patients, all of whom were organ recipients.The B-cell lymphoproliferative syndrome was separated into oligoclonal and monoclonal forms on the basis of immunologic analysis of proliferating B cells by membrane and intracytoplasmic indirect immunofluorescence with anti-immunoglobulin heavy-chain and light-chain antibodies and immunoperoxidase or with immunoperoxidase alone. The monoclonal form was defined as one in which a single heavy chain and a single light chain were present on the surface or in the cytoplasm of B lymphoblasts (or in both places). Oligoclonality was defined as the presence of several heavy chains in conjunction with distinct serum monoclonal immunoglobulin components identified by immunofixation.18 According to these criteria, four recipients of bone marrow transplants and three organtransplant recipients (two received a heart, and one a kidney) had the monoclonal form of the syndrome. Karyotyping of proliferating monoclonal B cells showed abnormalities in all four patients studied: t(3;22), double t(l;14) and t(8;22), a monosomy 21, and a 5q— deletion. No cytogenetic abnormalities were found in the five patients with oligoclonal B-cell proliferation who were karyo-typed.
Treatment with Monoclonal Anti—B-Cell Antibodies
ALB9 is a mouse IgGl specific for CD24,22 an antigen expressed by the B-cell line and granulocytes. BL13 is a mouse IgGl specific for CD21,23 the EBV receptor on B cells.24 Both antibodies were purified from ascites on staphylococcus A Sepharose columns. The antibody preparations were checked for pyrogenicity, DNA content, and sterility and suspended in saline at a final concentration of 0.5 mg per milliliter.
Patients were treated between August 20, 1985, and May 30, 1990. Inclusion in the study required the diagnosis of progressive B-cell lymphoproliferative syndrome. In organ-transplant recipients, therapy was initiated if either a reduction in the dose of immunosuppressive agents produced no response or unfavorable prognostic factors were present (rapidly progressive multivisceral infiltration, atypical nuclei and necrosis on histologic analysis, or both). Recipients of bone marrow transplants were receiving limited immunosuppressive therapy at the time of diagnosis of the B-cell lymphoproliferative syndrome (steroids in three and low-dose cyclosporine in four), and their regimen was not modified. Of a total of 34 patients (15 marrow recipients and 19 organ recipients) in whom the syndrome developed in the 11 participating centers during the study period, 27 (15 marrow recipients and 12 organ recipients) met the inclusion criteria; 1 was not treated because antibodies were not available at the time. The other seven patients were excluded because the syndrome resolved after reductions in the dose of immunosuppressive agents.
Treatment consisted of intravenous infusion of anti—B-cell antibodies for four to six hours every day for 10 days at a daily dose of 0.2 mg per kilogram of body weight. The treatment protocol was approved by the ethics committee of the Hôpital des Enfants-Malades. Informed consent was obtained from the patients, or from their parents if they were under 18 years of age. Treatment was started a median of 13 days (range, 3 to 55) after the onset of the B-cell lymphoproliferative syndrome in the recipients of bone marrow transplants and a median of 42 days (range, 10 to 90) in organtransplant recipients.
Treatment tolerance was graded according to the World Health Organization recommendations for grading of acute and subacute toxicity (from grade 1 to grade 4, according to severity). The end point of analysis was December 1, 1990.
Results
Tolerance
A grade 2 fever occurred in three patients, pain (grade 1 ) in two, and diarrhea, vomiting, and thrombocytopenia in one (grade 3 for each sign). All patients had transient neutropenia (grade 3 in 12 and grade 4 in 14) during the 10 days of treatment and for up to 5 days afterward. No patients generated antibodies against mouse immunoglobulins during the 10-day treatment period. Two patients were treated for longer periods (for 15 days and four further periods lasting 15 to 35 days) because of partial unresponsiveness in one and relapse in the other. Antimouse immunoglobulin antibodies developed in one of these patients on the 14th day of treatment, followed by transient hypotension. No antimouse immunoglobulin antibodies developed in the second patient.
B cells were not detectable in the blood during treatment in the 18 patients whose blood samples were analyzed, but they progressively reappeared during the 15 days following the end of treatment.
Efficacy
Some patients received antiviral agents or corticosteroids at some point after transplantation. Three of 14 marrow recipients and 2 of 12 organ recipients were treated with acyclovir. Two organ recipients received ganciclovir, and three marrow recipients received corticosteroids. Nine of the 14 marrow recipients and 8 of the 12 organ recipients did not receive any associated specific therapy. None of the patients received intravenous infusions of immunoglobulins, although all the bone marrow recipients received weekly intravenous infusions of immunoglobulin as prophylaxis. Eight of the 14 bone marrow recipients began to receive acyclovir (1500 mg per square meter of body-surface area) on the first day after transplantation as prophylaxis against cytomegalovirus.25 In 7 of the 12 organ recipients, the doses of immunosuppressive agents were reduced 11 to 60 days before anti—B-cell-antibody therapy was begun, and this approach was considered unsuccessful because of disease progression in all cases. One patient received acyclovir and one received ganciclovir 30 and 10 days, respectively, before treatment with anti—B-cell antibodies was begun, without apparent efficacy.
As shown in Table 3Table 3
Outcome of Treatment of Oligoclonal and Monoclonal B-Cell Lymphoproliferative Syndrome with Anti—B-Cell Antibodies., the infusion of anti—B-cell antibodies was associated with complete remission in 16 of the 26 patients. Complete remission was defined as the disappearance of all clinical manifestations of the B-cell lymphoproliferative syndrome, including shrinking of enlarged organs, associated with the disappearance of detectable B-cell lymphoblasts in blood and marrow, as well as the absence of in vitro spontaneous growth of B cells and a significant reduction in monoclonal immunoglobulin serum components. Complete remission was achieved within 15 to 45 days (median, 21).Complete remission occurred only in patients with oligoclonal B-cell lymphoproliferative syndrome; two such patients with involvement of the central nervous System had systemic remission but died of central nervous system disease progression. All patients with monoclonal B-cell lymphoproliferative syndrome died within 38 days of starting treatment. Salvage chemoradiotherapy in two patients and the administration of interferon alfa-2 to one patient were unsuccessful. Of 15 patients in complete remission who could be evaluated, expression of both CD21 and CD24 was detected on proliferative B cells in 10 and CD21 or CD24 in 5. Of seven patients who could be evaluated in whom treatment failed, CD21 and CD24 were detected in three and CD21 or CD24 in four. In all the patients either CD21 or CD24 was expressed.
Of the 16 patients who had complete remission, 2 marrow-transplant recipients had a relapse one and two months later (Fig. 1). These patients had prolonged immunodeficiency due either to graft rejection with autologous marrow reconstitution in a patient with the Wiskott—Aldrich syndrome or to concomitant Grade IV acute graft-versus-host disease. The first patient was treated successfully on four occasions with anti—B-cell antibodies, although relapse occurred after each course of treatment. Four other patients died in remission 120 to 438 days after the onset of the B-cell lymphoproliferative syndrome (Fig. 1 and 2Figure 1
Outcome in Patients with Oligoclonal B-Cell Lymphoproliferative Syndrome Treated with Anti—B-Cell Antibodies.). Eleven patients were alive and free of manifestations of the syndrome (five marrow recipients and six organ recipients) (Fig. 2) 8 to 60 months after treatment, with a functioning graft. Table 4Table 4
Treatments Received in Association with the Administration of Anti—B-Cell Antibodies in Long-Term Survivors. shows the associated treatments received by these long-term survivors; these treatments did not differ from those received by the other patients. In eight of the nine patients who could be evaluated normal B-cell functions returned, whereas one marrow-transplant recipient still had hypogammaglobulinemia 60 months after treatment. Four of the five marrow-transplant recipients were found to have EBV-specific antibodies. Four of five organ-transplant recipients were found to have antibodies against Epstein–Barr nuclear antigen; in contrast, one patient no longer had detectable anti-EBV antibodies.Discussion
In this study, we tested the possible efficacy of anti—B-cell monoclonal antibodies in controlling the proliferation of B cells in 26 recipients of bone marrow or organ transplants who had the B-cell lymphoproliferative syndrome. This work followed our preliminary report indicating the success of infusion of anti-CD21 and anti-CD24 antibodies in reducing uncontrolled proliferation of oligoclonal B cells in two recipients of HLA-nonidentical bone marrow.17 Our results indicate the possible efficacy of anti—B-cell antibodies in controlling nonmonoclonal B-cell lymphoproliferative syndrome, on the basis of both clinical and immunologic criteria; the treatment was not effective in patients with oligoclonal B-cell proliferation and central nervous system involvement. Early and late secondary effects were limited. In contrast, monoclonal B-cell proliferation did not respond to such treatment. No other variables were found to be predictive of treatment outcome.
The efficacy of therapy to suppress B-cell proliferation should be analyzed with caution, since spontaneous resolution of B-cell lymphoproliferative syndrome has been described1 , 2 and since some of our patients also received acyclovir, ganciclovir, or steroids in association with a reduction in the dosage of immunosuppressive therapy.13 14 15 Several facts argue against spontaneous resolution in this study group. Spontaneous regression of B-cell lymphoproliferative syndrome has only been reported after organ transplantation,13 and it was characterized as a "mononucleosis syndrome" in these cases.5 , 12 In contrast, the disease in our patients was more aggressive, since it occurred early after transplantation, involved multiple organs in all but two cases, was rapidly progressive, and usually had histologic markers of poor prognosis such as atypical nuclei, necrosis, or both.2 In addition, the reduction in the doses of immunosuppressive agents in seven organ-transplant recipients was initiated before treatment with anti—B-cell antibodies was begun, and was not successful. Long-term survivors in this series did not differ from the other patients with respect to associated treatments received. A relation between the antibody treatment and the control of the B-cell lymphoproliferative syndrome is further suggested by the fact that the response occurred 15 to 45 days after therapy was started and that the syndrome recurred after the cessation of therapy in two patients with persistent immunodeficiency. Furthermore, the readministration of anti—B-cell antibodies to these patients was successful on five occasions.
At least two therapeutic alternatives have been suggested in the control of oligoclonal B-cell lymphoproliferative syndrome. In a limited number of cases, interferon alfa-2 has been effective, with long-term cure in at least four patients.8 , 16 Similarly, a report that ganciclovir controlled a severe case of EBV-induced B-cell lymphoproliferative syndrome15 also warrants further study. Finally, therapy with cytotoxic drugs has rarely been effective in controlling the syndrome.1 , 26
Several factors in the treatment of B-cell lymphoproliferative syndrome with anti—B-cell antibodies remain to be elucidated. First, the optimal duration of treatment and dosages are unknown. In most of our patients the dose of antibody used appeared to be sufficient to saturate circulating targets, as shown by the disappearance of B cells. Second, it is not known whether the use of a single anti—B-cell antibody specific for either CD21 or CD24 (or another B-cell—specific membrane antigen) would be equally effective. A combination of antibodies with different specificities may be logical in view of the defective expression of some B-cell membrane proteins by lymphocytes in the B-cell lymphoproliferative syndrome26 and as observed in this study.
Taken as a whole, our results suggest that anti—B-cell antibodies can control some cases of nonmonoclonal B-cell proliferation without central nervous system involvement that occur after transplantation, with few side effects. The apparent efficacy of this treatment was particularly marked in the recipients of bone marrow transplants (9 of 14 had complete remission), since in previous reports very few patients recovered from the syndrome (3 of 32).8 9 10 11 In patients who have undergone organ transplantation, the early use of anti—B-cell antibodies may obviate the need to reduce the dosage of immunosuppressive agents, an action that can lead to loss of the graft. A controlled, randomized study of the use of anti—B-cell antibodies in the treatment of B-cell lymphoproliferative syndrome after organ transplantation would seem to be justified, given the slightly better prognosis of the syndrome in this setting.1 , 12 , 13
The following centers participated in this study: Department of Pediatrics, Hôpital de la Reine Fabiola, Brussels, Belgium (Dr. M. Hallé); Department of Nephrology and Intensive Care Unit, Hôpital E. Herriot, Lyons, France (Drs. J.L. Gamier and J.S. Mercatello); Department of Pneumology, Hôpital Louis Pradel, Lyons, France (Dr. J.F. Momex); Department of Pediatrics, Centre Hospitalier Régional, Nancy, France (Dr. P. Bordigoni); Intensive Care Unit, Centre Hospitalier Régional, Nantes, France (Dr. Y. Blanloeil); Department of Pediatrics, Hôpital des Enfants-Malades, Paris (Drs. J. Le Bidois, S. Blanche, A. Fischer, and P. Niaudet); Intensive Care Unit, Hôpital Bichat, Paris (Dr. J.P. Bedos); Department of Hematology, Centre Hospitalier Régional, Poitiers, France (Dr. E. Benz-Lemoine); and the Oncology Unit, Centre Hospitalier Régional, Strasbourg, France (Dr. P. Lutz).
We are indebted to Ms. D. Bresson for assistance in the preparation of the manuscript and to Dr. N. Brousse for immunohistologic studies.
Source Information
From Unité 132, INSERM (A.F., S.B., F.L.D., CG.), Unité de Cardiologie (J.L.B.), Unité de Néphrologie (P.N.), and Départment d'Hématologie (A.-M.F.), Hôpital des Enfants-Malades, Paris; Départment de Pédiatrie, Centre Hospitalier Régional, Nancy, France (P.B.); Unité de Néphrologie, Hôpital E. Herriot, Lyons, France (J.L.G.); Laboratoire de Microbiologie, Hôpital Saint-Louis, Paris (F.M.); and Immunotech, Marseilles, France (M.H.). Address reprint requests to Dr. Fischer at INSERM U 132, Hôpital des Enfants-Malades, 149 rue de Sèvres, 75743 Paris Cédex 15, France.
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