Original Article
Increased Incidence of Lymphoproliferative Disorder after Immunosuppression with the Monoclonal Antibody OKT3 in Cardiac-Transplant Recipients
N Engl J Med 1990; 323:1723-1728December 20, 1990
- Abstract
- Abstract
Background.
A sudden increase in the incidence of post-transplantation lymphoproliferative disorder among the patients in our cardiac-transplantation program was temporally related to introduction of the immunosuppressive drug OKT3. This monoclonal antibody has come to be widely used in recent years both to prevent and to treat rejection after cardiac transplantation.
Methods.
In order to identify variables that predict the development of post-transplantation lymphoproliferative disorder, we analyzed retrospectively a series of 154 consecutive cardiac-transplant recipients at a single institution. Univariate analyses and multivariate analysis by logistic regression were performed.
Results.
Among 75 patients who did not receive OKT3, post-transplantation lymphoproliferative disorder developed in 1 (1.3 percent), as compared with 9 of 79 patients who received the drug (11.4 percent); the incidence among the OKT3-treated patients was ninefold higher (odds ratio, 9.5; 95 percent confidence interval, 1.6 to 54.7). According to multivariate analysis, the only factor significantly associated with the development of post-transplantation lymphoproliferative disorder was the use of OKT3 (P = 0.001). A significant increase in risk with increasing doses was also apparent: 4 of 65 patients who received a cumulative dose of 75 mg of OKT3 or less (6.2 percent) had post-transplantation lymphoproliferative disorder, whereas 5 of 14 patients who received more than 75 mg had the disorder (35.7 percent; P<0.001).
Conclusions.
The addition of OKT3 to the immunosuppressive regimen increases the incidence of post-transplantation lymphoproliferative disorder after cardiac transplantation, and the risk increases sharply after cumulative doses greater than 75 mg. We suggest that the risks and benefits of prophylactic OKT3 administration be reassessed in the light of these findings, particularly since the value of prophylactic immunotherapy in cardiac-transplant recipients remains to be clearly established. (N Engl J Med 1990; 323:1723–8.)
Media in This Article
Table 1
Comparison of Patients Who Had Post-transplantation Lymphoproliferative Disorder (PTLD) and Those Who Did Not.*Table 2
Characteristics of the Patients with Post-transplantation Lymphoproliferative Disorder (PTLD).*Article Activity
- Article
POST-TRANSPLANTATION lymphoproliferative disorder is a well-recognized, frequently fatal complication of immunosuppression.1 , 2 The term encompasses a spectrum of abnormal proliferations of B lymphocytes that occur after organ transplantation. Such lymphoproliferative disorders have been identified in the wider context of immunodeficiency in general — whether it is congenital, due to human immunodeficiency virus type 1 (HIV), or associated with intensive chemotherapy for leukemia.3 4 5 The disease has provided insights into the nature of lymphoid cancer and has assumed increasing clinical importance in view of the HIV epidemic and the rising number of organ-transplant recipients. The incidence of post-transplantation lymphoproliferative disorder varies with the organ transplanted; in a large series, Nalesnik et al. reported an incidence of 1 percent for renal transplantation, 1.8 percent for cardiac transplantation, 2.2 percent for liver transplantation, and 4.6 percent for heart—lung transplantation.2
The Epstein–Barr virus (EBV) is believed to have an important role in the pathogenesis of post-transplantation lymphoproliferative disorder. Clinical or serologic evidence of a primary or reactivated EBV infection often precedes the appearance of the disorder.6 Tumor tissue has been found to contain EBV DNA, though not in all cases,7 and to express viral proteins actively.8 The development of post-transplantation lymphoproliferative disorder in immunosuppressed patients is believed to result from inadequate T-cell control over EBV-driven B-cell proliferation.2 A histologic spectrum extending from lesions that appear reactive to large-cell non-Hodgkin's lymphoma has been recognized.9 Both poly-clonal and monoclonal proliferations have been identified on the basis of the cell-surface immunoglobulin phenotype.10 , 11 Immunogenotyping by DNA analysis has emerged as a more sensitive technique for determining the clonality of lymphoproliferations than immunophenotyping; monoclonal subpopulations have been identified by analysis for gene rearrangement in some tumors that appeared to be polyclonal on immunoglobulin staining.12 13 14 15 Cleary et al.16 have identified clonal immunoglobulin-gene rearrangements even in lesions that lack cellular immunoglobulin and have suggested that post-transplantation lymphoproliferative disorder is a neoplastic disorder from the outset.
We noted a sharp increase in the incidence of post-transplantation lymphoproliferative disorder over the past three years among cardiac-transplant recipients at our center and found that increase to be strongly associated with the use of the immunosuppressive agent OKT3. OKT3 is a murine monoclonal antibody, targeted against the human CD3-receptor—T-cell complex, that profoundly depletes circulating CD3+ T lymphocytes. The drug was initially reserved for the treatment of refractory episodes of rejection. It has recently come into widespread use in the perioperative period for prophylaxis against the rejection of cardiac transplants,17 particularly since the commercial availability of antithymocyte globulin became uncertain. Although it is widely used, the value of such prophylactic immunotherapy, whether with OKT3 or antithymocyte globulin, is controversial and remains to be clearly established. Nonrandomized studies have shown no definite advantage to such therapy in terms of either the incidence of rejection or survival; a prospective randomized trial has not yet been performed.18 , 19 The effect of OKT3 on the risk of post-transplantation lymphoproliferative disorder after cardiac transplantation has remained unknown.
Methods
Patient Population
We studied patients who received cardiac transplants at our center during a six-year period. Between March 11, 1984, the beginning of the cardiac-transplantation program, and March 31, 1990, 162 orthotopic cardiac transplantations were performed at Loyola University. Three patients received second transplants, with the data for each patient combined, and five patients who died of postoperative complications within three days of transplantation were excluded from the analysis. We therefore were able to include data on 154 patients in our analysis of variables associated with the risk of having post-transplantation lymphoproliferative disorder after cardiac transplantation. Seventy-five percent of patients were male, and 84 percent were white; their mean age (±SD) was 46±13 years, and there were roughly equal proportions of patients with dilated cardiomyopathy (47 percent) and ischemic cardiomyopathy (44 percent) among them.
Immunosuppressive Regimens
Eighty-six patients received prophylaxis with antithymocyte globulin (Atgam, Upjohn, Kalamazoo, Mich.; 5 mg per kilogram of body weight per day for 9 days), and 65 patients received OKT3 prophylactically (Orthoclone OKT3, Ortho Pharmaceutical, Raritan, N.J.; 5 mg per day for 14 days). Three patients received no prophylactic immunotherapy. OKT3, introduced in our center in November 1985, was initially used only for the treatment of refractory rejection (14 patients); subsequently, it was also used for prophylaxis. A total of 79 patients therefore received OKT3 for prophylaxis, treatment, or both. Whether or not they received OKT3, all patients received the following immunosuppressive regimen: methylprednisolone (500 mg intravenously before and during transplantation and 125 mg intravenously every eight hours for three doses postoperatively), azathioprine (2 mg per kilogram intravenously before transplantation, followed by 2 mg per kilogram per day orally, adjusted to maintain the white-cell count above 3.5×109 per liter), prednisone (1 mg per kilogram per day orally, tapered by 0.1 mg per kilogram every other day to 0.2 to 0.3 mg per kilogram per day, and reduced to 0.1 mg per kilogram per day after one year), and cyclosporine (5 to 8 mg per kilogram per day, adjusted to maintain the serum cyclosporine level within a specified target range). Until July 22, 1988, the Sandoz polyclonal-antibody assay for cyclosporine (Sandoz Pharmaceuticals, East Hanover, N.J.) was used, with a target range of 120 to 160 ng per milliliter for the first year after transplantation, 80 to 120 ng per milliliter for the second year, and 50 to 80 ng per milliliter for the third and subsequent years. After July 22, 1988, the Abbott TDx assay (Abbott Laboratories, North Chicago) was used, with a target range of 180 to 220 ng per milliliter for the first year, 140 to 180 ng per milliliter for the second year, and 100 to 140 ng per milliliter for the third and subsequent years. The results of these two assays are not readily convertible. For purposes of analysis, all cyclosporine levels were therefore expressed as a multiple of the number corresponding to the middle of the target range for the assay used and the year after transplantation.
Rejection episodes were treated in a uniform manner throughout the study period. Endomyocardial biopsies were graded on the basis of histologic examination as indicating mild, moderate, or severe rejection.20 Intensified immunosuppression was used only in cases of moderate or severe rejection. In the absence of hemodynamic compromise, the oral steroid dose was increased; if hemodynamic compromise was evident, 1 g of methylprednisolone per day was given intravenously for three days. Refractory rejection episodes were treated with either OKT3 (5 mg intravenously per day for 10 days) or antithymocyte globulin (5 mg per kilogram per day intravenously for 5 days). If rejection was not reversed, increased doses of OKT3 (up to 10 mg per day) or antithymocyte globulin (up to 15 mg per kilogram per day) were used.
Pathological Studies
The diagnosis of post-transplantation lymphoproliferative disorder was based on histologic examination of biopsy material in all cases. Lesions were classified according to the "working formulation" scheme.21 Immunophenotyping by staining, immunogenotyping by DNA analysis for clonal immunoglobulin-gene rearrangements, and Southern blot analysis for the presence of EBV DNA were performed on tumor specimens whenever it was technically feasible to do so.12 , 22
Statistical Analysis
Univariate analyses included Fisher's exact test or the chi-square test for categorical variables, and Student's t-test was used for continuous variables. The cumulative dose of OKT3 was converted to an ordinal variable (none, ≤75 mg, or >75 mg) for multivariate analysis. Multiple logistic regression was used to identify factors associated with post-transplantation lymphoproliferative disorder while adjusting for possible confounding variables. A two-sided alpha level of less than 0.05 was considered to indicate statistical significance. No adjustment was made for multiple testing.
Results
The Use of OKT3 and the Risk of Post-transplantation Lymphoproliferative Disorder
A number of variables were examined in order to identify any that might be associated with the development of post-transplantation lymphoproliferative disorder (Table 1Table 1
Comparison of Patients Who Had Post-transplantation Lymphoproliferative Disorder (PTLD) and Those Who Did Not.*). The factors analyzed were sex, race, indication for transplantation, age, body weight, use of OKT3, number of rejection episodes requiring intensified immunosuppression, use of antithymocyte globulin, cumulative dose of antithymocyte globulin, cumulative dose of methylprednisolone, and mean serum cyclosporine level. In the univariate analyses, the only factor demonstrated to differ significantly between the patients in whom post-transplantation lymphoproliferative disorder developed and those in whom it did not was the use of OKT3.Of 75 transplant recipients who did not receive OKT3, 1 had a lymphoproliferative disorder, for an incidence of 1.3 percent — similar to the 1.8 percent reported for a large series of cardiac-transplant recipients.2 Of 79 patients who received OKT3 for prophylaxis, treatment of rejection, or both, 9 had post-transplantation lymphoproliferative disorder, for an incidence of 11.4 percent. This represents an approximately ninefold greater risk (odds ratio, 9.5; 95 percent confidence interval, 1.6 to 54.7; P = 0.018 by Fisher's exact test). Because, over the course of time, 30 patients received both OKT3 and antithymocyte globulin, the use of this combination of agents was specifically assessed as a possible risk factor for post-transplantation lymphoproliferative disorder. Only two of those patients (6.7 percent) had post-transplantation lymphoproliferative disorder, however, whereas 7 of the remaining 49 patients who received OKT3 but not antithymocyte globulin had the disease (14.3 percent, P = 0.47).
The effect of the dose of OKT3 on the incidence of post-transplantation lymphoproliferative disorder was then assessed. All recipients of OKT3 who had post-transplantation lymphoproliferative disorder received prophylactic courses of the drug. A single course was generally 5 mg per day for 14 days, amounting to a total of 70 mg. Cumulative doses in excess of 75 mg were the result of an additional later course of OKT3 for treatment of refractory rejection in all but one patient, in whom the dose and duration of the prophylactic course were increased. Of 65 patients who received a cumulative dose of 75 mg or less of OKT3, 4 (6.2 percent) had post-transplantation lymphoproliferative disorder, as compared with 5 of 14 patients (35.7 percent) who received more than 75 mg (P<0.01). An analysis of the risk of post-transplantation lymphoproliferative disorder at cumulative doses of OKT3 ranging from none to more than 75 mg demonstrated a highly significant trend of increasing incidence with increasing dosage (MantelHaenszel chi-square, 16.0; P<0.0001). In order to adjust for possible confounding variables, a multivariate analysis was performed with use of logistic-regression techniques. The factors analyzed were the use of OKT3 (cumulative dose: none, ≤75 mg, or >75 mg), race, sex, cumulative dose of antithymocyte globulin, cumulative dose of methylprednisolone, mean serum cyclosporine level, number of rejection episodes requiring treatment, and cause of the preexisting cardiac disease. The only factor that significantly predicted the development of post-transplantation lymphoproliferative disorder when all other factors in the model were controlled was the use of OKT3 (P<0.001).
Timing and Clinical Features of Post-transplantation Lymphoproliferative Disorder In Relation to the Dose of OKT3
Table 2Table 2
Characteristics of the Patients with Post-transplantation Lymphoproliferative Disorder (PTLD).* summarizes the clinical characteristics of the 10 cases of post-transplantation lymphoproliferative disorder. The interval between transplantation and the appearance of post-transplantation lymphoproliferative disorder was very short, on the order of one to two months, in patients who received more than 75 mg of OKT3. The correlation between higher doses and shorter intervals was statistically significant (r = -0.91, P = 0.0006).Patients 2 through 5 received a single course of OKT3 (≤75 mg). Only one of these patients (Patient 5) presented with organ failure, systemic sepsis, and a tumor identifiable as polyclonal; two patients remained alive and disease-free after completing cytotoxic chemotherapy.
Patients 6 through 10 received more than 75 mg of OKT3. Their lesions were found to be polyclonal according to cellular-immunoglobulin phenotype; whenever we tested for it, a clonal immunoglobulin-gene rearrangement was detected. With one exception (Patient 10), these patients presented with extensive post-transplantation lymphoproliferative disorder, characterized by organ failure, systemic sepsis, or both. Death ensued rapidly, regardless of the type of treatment attempted. Patient 10 presented with limited disease classified as diffuse mixed lymphoma (polymorphic B-cell lymphoma by the system of Frizzera et al.9). The temporary withdrawal of immunosuppression and the administration of acyclovir were followed by rapid clinical resolution, and the patient remained in complete remission after four months.
Patient 1 was the only one in whom post-transplantation lymphoproliferative disorder developed who did not receive OKT3. The lesion was an extensive Burkitt's lymphoma with the t(8;22) translocation, according to cytogenetic analysis. The patient died of sepsis and refractory disease during cytotoxic chemotherapy. All the deaths listed in Table 2 were attributable to post-transplantation lymphoproliferative disorder.
Discussion
At our center, a substantial increase in the incidence of post-transplantation lymphoproliferative disorder followed the addition of OKT3 to the conventional immunosuppressive regimen for cardiac-transplant recipients. No other risk factor was found to be significantly associated with the increased incidence. We found a significant relation between the total dose of OKT3 and the risk of post-transplantation lymphoproliferative disorder. Although the reported incidence has varied, depending on the organ transplanted and the immunosuppressive regimen used, the risk of post-transplantation lymphoproliferative disorder has generally been considered to be related to the degree of immunosuppression. The disease has been found to occur with all forms of therapy against rejection.1 Earlier investigators noted a particularly high incidence after the introduction of cyclosporine,23 but the incidence diminished when blood levels were monitored and lower cyclosporine doses were used.24 In our series of patients, the increased risk of post-transplantation lymphoproliferative disorder seen with OKT3 was independent of the mean serum cyclosporine level.
In view of past experience, it should not be surprising that the addition of a potent immunosuppressive agent such as OKT3 increases the risk of post-transplantation lymphoproliferative disorder. Whether this increase results simply from greater total immunosuppression or whether mechanisms specific to OKT3 are involved cannot be determined from our data. An increased incidence of post-transplantation lymphoproliferative disorder has also been attributed to the use of another anti-CD3 monoclonal antibody, known as 64.1, after allogeneic bone marrow transplantation. T-cell depletion of donor marrow has been identified as a concomitant risk factor in that setting.25
Extensive circumstantial evidence links EBV with the development of post-transplantation lymphoproliferative disorder. Since primary EBV infection has been identified as carrying a higher risk than reactivated infection,6 it was important to determine whether the higher incidence of post-transplantation lymphoproliferative disorder in OKT3-treated patients was due to an incidental clustering of primary EBV infections in that group. This did not prove to be the case. Titers of IgG antibody to EBV-capsid antigen were measured before and at intervals after transplantation. Overall, 93 percent of patients had a positive titer ≥1:10) before transplantation. All but two initially seronegative patients became seropositive after transplantation, indicating that primary infection occurred in virtually all initially seronegative patients. Although only 5 percent of the patients in whom post-transplantation lymphoproliferative disorder did not develop were initially seronegative, 30 percent of the patients in whom the disorder did develop had negative results on serologic tests for EBV before transplantation (P = 0.025), indicating a higher frequency of primary infection in the group that had post-transplantation lymphoproliferative disorder. When patients were grouped according to whether they did or did not receive OKT3, however, no difference in the rate of initial seronegativity was found. The frequency of reactivated infection (an increase of fourfold or more in titer) in our series did not differ significantly between the patients who did and those who did not have post-transplantation lymphoproliferative disorder (P = 0.21). In 6 of the 10 patients with post-transplantation lymphoproliferative disorder (Patients 1, 3, 4, 5, 8, and 10), tumor tissue was examined for the presence of EBV DNA by Southern blot analysis; it was identified in all 6.
Although the strong correlation between the cumulative dose of OKT3 and the incidence of post-transplantation lymphoproliferative disorder could be interpreted as a dose–response phenomenon, the duration of exposure to the drug might be significant in this context. The number of days of OKT3 treatment was equivalent to the cumulative dose as an indicator of drug exposure, since the daily dose was uniform in all but seven patients, none of whom would be reclassified if the number of days of treatment were used as the measure of exposure. The interval between courses in the five patients who had post-transplantation lymphoproliferative disorder after receiving cumulative doses of more than 75 mg of OKT3 was generally much shorter (median, 13 days; range, 0 to 33), however, than in the nine patients who received more than 75 mg of OKT3 who did not have post-transplantation lymphoproliferative disorder (median, 115 days; range, 8 to 884; P = 0.02 by Mann-Whitney U test). This difference raises the possibility that the duration of T-cell suppression may be as relevant to the risk of post-transplantation lymphoproliferative disorder in the patients who received high-dose OKT3 therapy as cumulative drug exposure; firm conclusions cannot be drawn from the analysis of such small numbers.
There was a striking inverse correlation between the dose of OKT3 and the length of time to the appearance of post-transplantation lymphoproliferative disorder in our patients. A shortening of the interval between transplantation and the appearance of post-transplantation lymphoproliferative disorder, from an average of 30 months to an average of 6 months, was noted by Penn1 and others16 after the introduction of cyclosporine. Both the length of the time to appearance of the disorder and the clinical pattern of post-transplantation lymphoproliferative disorder in our series appear to have varied with the dose of OKT3; these correlations may correspond to the intensity of immunosuppression. A similar pattern has been observed after bone marrow transplantation.26 Presentation with widespread tumor, organ failure, systemic sepsis, or a combination of these, followed by a fulminant clinical course, has been considered rare.2 Five of the nine cases of post-transplantation lymphoproliferative disorder that occurred in our group of OKT3 recipients presented in this fashion (Patients 5, 6, 7, 8, and 9), however. Four of these five patients had received a cumulative dose of more than 75 mg of OKT3, all with short intervals between courses. Their tumors were found to be polyclonal by immunoglobulin phenotyping. Such a clinical picture is consistent with a model of multifocal polyclonal or multiclonal B-cell proliferations that arise independently and might be expected to occur more frequently in the patients in whom immunosuppression was most intense. Alternatively, the specific immune defects induced by OKT3 might predispose patients to this type of presentation. The clinical outcome of the patients in our series who presented with such multifocal, fulminant disease was uniformly dismal, regardless of treatment — in keeping with the experience of others.2 , 26 More circumscribed disease, later presentation, phenotypic monoclonality, and a more gradual clinical course were seen in all but one of the patients who received no more than 75 mg of OKT3. Interestingly, none of the three patients who required second transplantations have had post-transplantation lymphoproliferative disorder.
Starzl et al. have advocated the reduction of immunosuppression in the initial management of lymphoproliferative disorder after organ transplantation in general.23 Complete tumor regression has been documented in a small number of recipients of heart and heart—lung transplants in whom this was the sole therapy, whereas resolution of post-transplantation lymphoproliferative disorder has been achieved in a number of others by reduction in the degree of immunosuppression in combination with acyclovir, surgical resection, or other therapies.14 , 23 , 27 Primarily on the basis of their observations of renal-transplant recipients,11 , 28 Hanto et al. have emphasized the use of acyclovir, followed by reduction or cessation of immunosuppression. Both groups have noted that patients with late-presenting, widespread, phenotypically monoclonal disease rarely respond to such measures and have a high mortality rate.14 , 27 28 29
The addition of OKT3 to the immunosuppressive regimen increases the incidence of post-transplantation lymphoproliferative disorder after cardiac transplantation, and the risk increases sharply after cumulative doses above 75 mg of OKT3. Since early diagnosis and intervention are believed to improve the outcome, all patients who have received OKT3 should be followed up closely for early indications of post-transplantation lymphoproliferative disorder. We suggest that the risks and benefits of the prophylactic use of OKT3 be reassessed, particularly since the value of prophylactic immunotherapy in cardiac-transplant recipients has not been clearly established.
We are indebted to Laura Weber, Ronald Price, Jr., Melanie Danley, and Bonnie Grusk for help with data collection and processing and to Dr. Michael Mihalov and Suzanne Huber for assistance with the gene-rearrangement and EBV-DNA analyses.
Source Information
From the Section of Hematology/Oncology (L.J.S., R.I.F.) and the Section of Cardiology (M.R.C.-N., E.J.O., M.R.J., A.L.H.), Department of Medicine, the Department of Pathology (G.J.D.), and the Department of Thoracic and Cardiovascular Surgery (R.P.), Loyola University of Chicago, Maywood, Ill., and Hines Veterans Affairs Hospital, Hines, Ill.; and the Cooperative Studies Program, Hines Veterans Affairs Hospital, Hines, Ill. (S.G.F.). Address reprint requests to Dr. Swinnen at Loyola University Medical Center, Section of Hematology/Oncology, Bldg. 54, 2160 S. First Ave., Maywood, IL 60153.
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