Original Article
Comparison of Plasma Exchange with Plasma Infusion in the Treatment of Thrombotic Thrombocytopenic Purpura
N Engl J Med 1991; 325:393-397August 8, 1991
- Abstract
- Abstract
Background.
Thrombotic thrombocytopenic purpura is an uncommon disease with a high mortality rate even with current treatment. The cause of the syndrome and its optimal treatment are unknown. Although both plasma exchange and plasma infusion have been useful treatments, it is not clear which is superior. In this report we describe a prospective randomized trial comparing plasma exchange with plasma infusion for the treatment of thrombotic thrombocytopenic purpura.
Methods.
One hundred two patients with thrombotic thrombocytopenic purpura were randomly assigned to receive either plasma exchange or plasma infusion with fresh-frozen plasma on seven of the first nine days after entry into the trial. The total volume of plasma received by patients undergoing plasma exchange was three times that received by patients undergoing plasma infusion. All the patients also received aspirin and dipyridamole. The outcomes in the two groups were compared at the end of the first treatment cycle (day 9) and after six months.
Results.
At the end of the first treatment cycle patients receiving plasma exchange had a higher rate of response as defined by an increase in the platelet count (24 of 51 patients) than those who received plasma infusion (13 of 51, P = 0.025). Of the 51 patients treated with plasma exchange, 2 died, whereas 8 of the 51 patients who received plasma infusion died (P = 0.035).
After six months the outcome in the plasma-exchange group was still superior, with a response observed in 40 of 51 patients, whereas 25 of 51 patients in the plasma-infusion group responded (P = 0.002). Eleven patients in the plasma-exchange group died, as did 19 patients in the plasma-infusion group (P = 0.036). The overall mortality was 29 percent.
Conclusions.
Plasma exchange is more effective than plasma infusion in the treatment of thrombotic thrombocytopenic purpura. (N Engl J Med 1991; 325:393–7.)
Article Activity
- Article
THROMBOTIC thrombocytopenic purpura, although an uncommon disease, is important for two reasons. Untreated, it has a high mortality that may be as great as 90 percent1; current treatment lowers this mortality dramatically. Second, the thrombotic complications of the disorder involve platelets, and it is possible that thrombotic thrombocytopenic purpura has many features in common with more widespread platelet-mediated disorders, such as myocardial infarction and stroke. Thrombotic thrombocytopenic purpura is characterized by thrombocytopenia, microangiopathic hemolytic anemia, and the presence of platelet-rich thrombi. These thrombi are probably responsible for the ischemic events that often characterize the disorder, including both neurologic and renal impairment. Because of the rarity of the condition and its frequently poor outcome, many different treatments were used in the past, but the anecdotal nature of reports of their use made it difficult to assess their efficacy accurately.
Major benefit was first observed when patients with acute thrombotic thrombocytopenic purpura were treated with plasma delivered by either exchange2 or infusion.3 , 4 Proponents of plasma infusion suggest that benefit is related to the administration of a substance that is deficient in patients with thrombotic thrombocytopenic purpura. Proponents of plasma exchange suggest that not only is a deficient factor replaced, but toxic substances are also removed during the exchange procedure. Although a review of case reports5 suggests that the two treatments have a similar rate of success (60 to 80 percent of patients respond to treatment), they are difficult to interpret because of their retrospective outcome and because of the small numbers of patients involved. Because case reports are selective and may not be representative of the disease, we also lack accurate information about the typical presentation of patients with thrombotic thrombocytopenic purpura and the overall prognosis.
In this report, we describe a national trial in which the great majority of patients presenting with thrombotic thrombocytopenic purpura in Canada during a seven-year period were randomly assigned to treatment with aspirin and dipyridamole and either plasma exchange or plasma infusion with fresh-frozen plasma. The intent was not only to determine which therapy was more effective, but also to obtain a more precise picture of the prognosis for patients with thrombotic thrombocytopenic purpura treated with these modern protocols.
Methods
Subjects
All the patients given a diagnosis of thrombotic thrombocytopenic purpura at any of 16 participating medical centers in Canada were considered for entry into the trial, which commenced in March 1982. Specific eligibility criteria were as follows: the presence of thrombocytopenia (defined as a platelet count of less than 100×109 per liter), microangiopathic hemolytic anemia (as indicated by the presence of red-cell fragmentation on a peripheral-blood film), no identifiable cause for the thrombocytopenia and microangiopathic hemolytic anemia (e.g., disseminated intravascular coagulation, carcinoma, or eclampsia), and no history of congestive heart failure or anuria that in the opinion of the attending physician rendered the patient unable to tolerate plasma infusion. Patients with a history of thrombotic thrombocytopenic purpura were not excluded from the study. Informed consent was obtained from all the patients before entry.
Study Design
Patients were randomly assigned to receive either plasma exchange or plasma infusion with fresh-frozen plasma, according to a scheme that ensured a balanced allocation within each center. One group received plasma exchange with fresh-frozen plasma as the replacement for a minimum of seven procedures over the first nine hospital days, with treatment on the first three days being essential. The volume exchanged was 1.5 times the predicted plasma volume for the first three procedures, and 1.0 times the predicted volume thereafter. The other group received plasma infusion daily until the end of a cycle of treatment. The volume of plasma infused was 30 ml per kilogram of body weight over the first 24 hours, followed by 15 ml per kilogram each day thereafter. If the patients were unable to tolerate this fluid load because of their cardiac or renal condition, diuretics were used. A cycle of treatment was defined as the period from randomization to one of the following events: death, clinical deterioration to the extent that the patient was taken off the protocol (which for patients receiving plasma infusion usually meant crossing over to plasma exchange), early response, or the completion of seven days of treatment.
All the patients received dipyridamole (400 mg per day) and aspirin (325 mg per day) by mouth for a minimum of two weeks after entry. Outcome was assessed at the end of the first cycle of treatment (day 9) and again six months after randomization.
Study End Points
Outcome measures included vital status, absolute platelet count, increase in platelet count, and neurologic status (as measured by the eye opening—motor—verbal response score). A complete response was defined as an improvement in the platelet count to more than 150×109 per liter for two consecutive days, with no deterioration in neurologic status. In all the patients who responded, treatment was tapered over the course of five procedures during the next two weeks. Any patients who had a partial response continued to receive the same treatment five times over a period of seven days; their condition was then reassessed. Patients who responded to treatment initially but relapsed once therapy was discontinued were considered to have an incomplete response and were given the same therapy that had produced the initial response.
In patients whose condition did not improve, as defined by a failure of the platelet count to increase to more than 150×109 per liter or by deterioration in the neurologic status at the end of the first cycle, treatment was considered to have failed. Patients in whom plasma infusion failed were allowed to cross over to plasma exchange, and the outcome was reassessed after a cycle of seven treatments in nine days. Patients in whom plasma exchange failed continued treatment at their physicians' discretion.
Randomization
To assign a patient to treatment the attending physician or apheresis nurse contacted the study coordinator. The eligibility criteria were reviewed, and the patient was randomly assigned to one of the treatment arms according to a predetermined allocation scheme. A stratified randomization scheme was used at first, but it soon resulted in an overall allocation of five plasma-exchange patients and nine plasma-infusion patients, which caused concern among the participating physicians. Patients were then assigned to treatment in the ratio of 2 to plasma exchange for every 1 to plasma infusion until the imbalance was corrected when there were 13 patients in each group. Stratification was discontinued for the remainder of the trial.
Monitoring
The study was monitored continuously by the consulting statistician to detect any marked excess in the number of deaths in either group. Patients' survival at the end of the first treatment cycle was assessed, and cases were paired on a chronologic basis. All the pairs were evaluated so that if one arm clearly showed a better rate of survival the study could be terminated. The response to treatment was not monitored in a similar fashion.
Statistical Analysis and Analytic Strategy
On the basis of information in the literature concerning the response to plasma exchange and plasma infusion, it was calculated that 50 patients would be required in each group to demonstrate a 20 percent difference in outcome between the two arms at a level of significance of P = 0.05.
The exact binomial test6 was used to test the statistical significance of the difference in outcome between the two groups. The 95 percent confidence intervals for the differences between the two treatment groups in the proportion of patients who responded and survivors were also computed.
Analysis was carried out both to assess response, as determined by our earlier criteria, and to compare the number of deaths in each treatment arm at the end of the first cycle and six months after entry into the trial. Since death was used as an outcome measure to determine a stopping rule, the hypothesis was not statistically tested for this outcome; instead, the survival curves over the six-month period were compared with the Breslow—Gehan test.7
Laboratory Testing
Hematologic evaluation was carried out at each participating institution (27 hospitals in 13 cities) by the routine methods of each center. To avoid error caused by incorrectly including red-cell fragments, platelets were counted manually in all cases. No attempt was made to characterize the material causing a positive direct antiglobulin test.
Results
Comparability of the Groups
One hundred three patients were enrolled in the trial over a seven-year period. The condition of one patient assigned to the plasma-infusion group improved rapidly before he had received any treatment, and he never received either plasma infusion or plasma exchange. Attending clinicians decided that this patient did not have thrombotic thrombocytopenic purpura, and the patient was therefore eliminated from the analysis. Of the remaining patients, 51 were randomly assigned to receive plasma exchange, and 51 to receive plasma infusion. There were 67 women and 35 men in the study, and their average (±SD) age was 40.5±14.3 years. Eleven patients with a history of thrombotic thrombocytopenic purpura were enrolled in the study. A summary of the demographic and clinical indexes is shown in Table 1Table 1
Demographic Characteristics of the Study Patients at Entry.*. Base-line data are shown in Table 2Table 2
Laboratory Findings at Entry.*. All the patients had thrombocytopenia; at entry, the average platelet count was 23.3±16.9×109 per liter, with a range of 1×109 to 94×109 per liter. Red-cell fragmentation was seen on all 102 blood films. The average reticulocyte count was 324±221.6×109 per liter. Three patients in the plasma-infusion group had very high bilirubin levels (more than 200 μmol per liter), leading to a higher mean bilirubin level in the patients in that group. It is unlikely, however, that red-cell hemolysis was greater in the plasma-infusion group than in the plasma-exchange group, since the lactate dehydrogenase level, another indicator of red-cell hemolysis, was higher in the plasma-exchange group than in the plasma-infusion group (1407 vs. 1248 units per liter). The direct antiglobulin test was positive in only three patients, one of whom also had rheumatoid factor.Fluctuating neurologic abnormalities were present in 64 of the patients at entry. Neurologic signs subsequently developed in another eight patients during the course of the disease, including one patient with classic thrombotic thrombocytopenic purpura, as determined by gingival biopsy at entry, who did not present with neurologic signs but who subsequently had transient confusion. Of the 38 patients who did not present with neurologic signs, 7 subsequently died, and 5 of them had neurologic signs before death.
Twenty-four of the 102 patients had fever at entry. Sixty patients had renal abnormalities at entry; 53 of them had an elevated level of blood urea nitrogen, and 47 had an elevated creatinine level.
Treatments Received
The patients in the plasma-exchange group received an average of 15.8 treatments (range, 3 to 36) over two or three cycles. Twelve patients received nine plasma exchanges or fewer. Plasma infusion was carried out for an average of 7.7 days (range, 1 to 31). Treatment failed in 31 patients in the plasma-infusion group, and they subsequently received an average of 12.8 plasma exchanges (range, 1 to 37).
A total of 1284 plasma exchanges and 432 plasma infusions were carried out in the 102 patients in the study. The patients who underwent plasma exchange received an average of 21.5±7.8 liters of plasma by the end of the first cycle, whereas those undergoing plasma infusion received an average of 6.7±3.3 liters. Most patients tolerated the procedures well. Six plasma-exchange patients and five plasma-infusion patients had no complications during any procedure. Most complications were minor and occurred in less than one quarter of the procedures. Forty-one patients had nausea, 34 hypotension, 27 an increase in pulse or respiration (or both), 10 dizziness, 17 chills, and 9 edema. The most common reaction was hives, which occurred in 35 patients during more than half of their procedures. Eight patients had bleeding as a complication; seven had bleeding from the gastrointestinal tract, and one had hematuria. Bleeding was controlled in all but one patient receiving plasma exchange, who died of massive gastrointestinal bleeding. Four patients in each group had seizures during a procedure.
Early Outcome
The analysis at the end of the first cycle showed a higher rate of response (defined as a platelet count of more than 150×109 per liter and no new neurologic events) in patients receiving plasma exchange than in patients receiving plasma infusion (P = 0.025) (Table 3Table 3
Results at the End of the First Cycle.). The condition of 12 patients assigned to plasma infusion deteriorated rapidly, and on clinical grounds they were transferred to plasma exchange before the intended end of the first cycle of treatment. These patients were considered to represent failures of plasma infusion. No patients were transferred from plasma exchange to plasma infusion.Given the high case fatality rate in this disease, survival is the most clinically relevant outcome. Five of the 12 patients who were transferred early to plasma exchange died, but because the moment of crossover defined the end of the first cycle, they must be counted as having survived the first cycle of plasma infusion. This approach is conservative, since four of the five died before the intended end of the first cycle (on day nine) and would thus have been considered to have died in the plasma-infusion group if they had not been transferred to plasma exchange.
Late Outcome
We also analyzed the patients' outcome six months after entry into the study. At various times after the end of the first cycle of treatment, 19 more patients in the plasma-infusion group were transferred to plasma exchange on clinical grounds. Fifteen of these patients had not responded at the end of the first cycle, and four had responded but later relapsed. These crossover patients underwent plasma exchange according to the study protocol. There was no crossover from plasma exchange to plasma infusion.
In 10 of the patients who originally responded to plasma exchange, the platelet count again fell after an average of 5.3 days, and they had an average of 15.4±8.2 additional exchanges over a period of 19.6 days before achieving a complete response with no further relapse. Similarly, two of the patients receiving plasma infusion relapsed after an initial response and received additional plasma infusions with no further relapse. In 16 patients undergoing plasma exchange and 2 receiving plasma infusion, treatment failed at the end of the first cycle but eventually succeeded.
Thus, in the final analysis 51 patients (40 of whom survived) received plasma exchange alone, 20 received plasma infusion alone (10 survived), and 31 received first plasma infusion and then plasma exchange (22 survived).
Using predetermined response criteria and regarding the early crossover patients as representing failures of plasma infusion, we found that the results of the late analysis again favored plasma exchange (P = 0.002) (Table 4Table 4
Results after Six Months.). The results of this analysis are conservative, since they attribute to plasma infusion 15 eventual responses among the crossover patients, although plasma infusion had already failed in 11 of those patients and 4 others had had incomplete responses. Using survival as the outcome with an intention-to-treat approach, we found that results in the plasma-exchange group were still superior. This finding is confirmed by the survival curve shown in Figure 1Figure 1
Survival of Patients with Thrombotic Thrombocytopenic Purpura. (P = 0.036).Outcomes in the 11 patients with a history of thrombotic thrombocytopenic purpura (6 in the plasma-exchange group and 5 in the plasma-infusion group) were indistinguishable from those in the other study patients both at the end of the first cycle and after six months.
Discussion
An analysis of response (as defined in the study) and survival showed that plasma exchange is superior to plasma infusion in the treatment of thrombotic thrombocytopenic purpura, both at the end of the first cycle of treatment and after six months. The significantly lower death rate when plasma was exchanged (P = 0.036) suggests a possible role for the removal of some plasma constituent in addition to the supply of fresh plasma. However, our study was not designed to determine whether the improved outcome with plasma exchange was attributable to the removal of a toxic material or to the administration of plasma in larger volumes than is possible with simple plasma infusion. Furthermore, no attempt was made to define the optimal schedule for either plasma exchange or plasma infusion. Instead, the clinicians at the 1981 annual meeting of the Canadian Apheresis Study Group made an empirical decision to adopt and adhere to the then-standard plasma-exchange and plasma-infusion treatment regimens for thrombotic thrombocytopenic purpura.
The use of aspirin and dipyridamole was considered to be an essential component of treatment for thrombotic thrombocytopenic purpura at the time the study was designed, and this represented the consensus of the Canadian hematologists involved in the study. Eight patients who were in the trial and thus receiving these drugs had bleeding complications.
An increased frequency or duration of plasma exchange might well produce even better results. Clearly, many patients required and received plasma exchange beyond a single treatment cycle; 42 of the 51 plasma-exchange patients received more than seven treatments. Thirty-one of the 51 plasma-infusion patients switched to plasma exchange at some point during treatment, and 17 of these patients underwent more than seven plasma exchanges. Since incomplete responses were relatively common in both groups, it is important to follow patients even after an apparent early response. Several weeks of therapy may be needed for a satisfactory outcome. Although interpretation of our results is complicated by the crossovers, all were necessary to preserve the clinical credibility of the study. Many patients whose condition did not respond to plasma infusion subsequently responded to plasma exchange, and this adds strength to the conclusion that plasma exchange is the better treatment.
The eventual response to plasma exchange was not predictable from the platelet count at presentation or the changes in the platelet count by day 9. Furthermore, the presence of neurologic signs did not predict a poor outcome with either plasma exchange or plasma infusion. The fact that only 64 of the 102 patients presented with neurologic findings and that only 24 had fever may reflect a relatively early presentation of these patients to the study, possibly contributing to the successful responses to treatment. Approximately half the patients tested had normal creatinine clearance; patients with poor or nonexistent renal function were not eligible for randomization. This trial therefore involved a subgroup of patients with thrombotic thrombocytopenic purpura who may be considered to have less severe disease.
Since neurologic signs, fever, and impaired renal function were not consistently present in our patients at entry, some might argue that they did not all meet the criteria for a diagnosis of thrombotic thrombocytopenic purpura. The validity of our diagnostic criteria is supported, however, by the fact that in eight patients neurologic signs developed only after treatment was initiated. Our patients were comparable to others described in the literature who had variable presentations, often without all the classic signs of thrombotic thrombocytopenic purpura. A review by Ridolfi and Bell8 reported that 98 percent of patients with thrombotic thrombocytopenic purpura had microangiopathic hemolytic anemia, 83 percent thrombocytopenic purpura, 84 percent neurologic symptoms, and 76 percent renal disease. Clearly, the diagnostic pentad is not uniformly present in this syndrome.
We observed a substantial mortality rate in our patients with thrombotic thrombocytopenic purpura, indicating that although plasma exchange and combined drug therapy have considerable benefit and probably represent the best available treatment, thrombotic thrombocytopenic purpura remains a disease in which treatment is not yet optimal. A better understanding of the pathophysiology of thrombotic thrombocytopenic purpura should lead to more effective treatment. Until that time, plasma exchange with fresh-frozen plasma should be used to treat patients with the disorder.
Supported by a grant (6613–1158) from the National Health Research and Development Program, Canada.
We are indebted to Dr. David Nathan, Harvard Medical School, and Dr. Michael Gent, McMaster University, who acted as outside consultants; and to Mr. Greg Tricklebank, Ms. Ann Kasaboski, Ms. Carole Herbert, and the study coordinators across Canada who collected and collated the data and without whose help this study would not have been possible.
Source Information
From the Departments of Medicine and Pathology, University of Ottawa, Ottawa, Ont. (G.A.R.); the Department of Medicine, University of Toronto, Toronto (K.H.S.); the Department of Medicine, University of British Columbia, Vancouver (N.A.B.); the Department of Pediatrics, University of Toronto (V.S.B.); the Department of Pathology, McMaster University, Hamilton, Ont. (J.G.K.); and the Department of Epidemiology, University of Ottawa (R.C.N., R.A.S.). Address reprint requests to Dr. Rock at the Canadian Apheresis Study Group, 206–435 St. Laurent Blvd., Ottawa, ON K1K 2Z8, Canada.
* The members of the Canadian Apheresis Study Group are as follows: Grenfell Adams, M.D., Barrett Benny, M.D., Noel A. Buskard, M.D., Robert Card, M.D., William F. Clark, M.D., Peter Ford, M.D., Philip Gordon, M.D., Max Katz, M.D., John Klassen, M.D., Pierre Leblond, M.D., Mariette Lepine-Martin, M.D., Jack McBride, M.D., Philip Mickelson, M.D., Rama C. Nair, Ph.D., Harry Rayner, M.D., Gail A. Rock, Ph.D., M.D., Kenneth H. Shumak, M.D., Robert A. Spasoff, M.D., Marion Sternbach, M.D., and David M.C. Sutton, M.D.
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