Original Article
The Clinical Course of Pulmonary Embolism
N Engl J Med 1992; 326:1240-1245May 7, 1992
- Abstract
- Abstract
Background.
Pulmonary embolism is a potentially fatal disorder. Information about the outcome of clinically recognized pulmonary embolism is sparse, particularly given that new treatments for more seriously ill patients are now available.
Methods.
We prospectively followed 399 patients with pulmonary embolism diagnosed by lung scanning and pulmonary angiography, who were enrolled in a multicenter diagnostic trial. We reviewed all hospitalizations, all new investigations of pulmonary embolism, and all deaths among the patients within one year of diagnosis.
Results.
Of the 399 patients, 375 (94 percent) received treatment for pulmonary embolism, usually conventional anticoagulation. Only 10 patients (2.5 percent) died of pulmonary embolism; 9 of them had clinically suspected recurrent pulmonary embolism. Clinically apparent pulmonary embolism recurred in 33 patients (8.3 percent), of whom 45 percent died during follow-up.
Ninety-five patients with pulmonary embolism (23.8 percent) died within one year. The conditions associated with these deaths were cancer (relative risk, 3.8; 95 percent confidence interval, 2.3 to 6.4), left-sided congestive heart failure (relative risk, 2.7; 95 percent confidence interval, 1.5 to 4.6), and chronic lung disease (relative risk, 2.2; 95 percent confidence interval, 1.2 to 4.0). The most frequent causes of death in patients with pulmonary embolism were cancer (in 34.7 percent), infection (22.1 percent), and cardiac disease (16.8 percent).
Conclusions.
When properly diagnosed and treated, clinically apparent pulmonary embolism was an uncommon cause of death, and it recurred in only a small minority of patients. Most deaths were due to underlying diseases. Patients with pulmonary embolism who had cancer, congestive heart failure, or chronic lung disease had a higher risk of dying within one year than did other patients with pulmonary embolism. (N Engl J Med 1992; 326:1240–5.)
Media in This Article
Figure 1
One-Year Mortality Curve in 399 Patients with Pulmonary Embolism.Table 1
Selected Base-Line Characteristics of 399 Patients with Pulmonary Embolism.Article Activity
- Article
PULMONARY embolism is a potentially fatal disorder for which anticoagulation therapy improves the outcome. Untreated, clinically apparent pulmonary embolism has been associated with a 30 percent hospital mortality rate, whereas the mortality rate for treated patients has been reported to be in the range of 8 percent.1 2 3 4 5 Reported rates of recurrence for correctly treated pulmonary embolism have ranged from 2 percent to 50 percent.6 7 8 These data are derived from small trials, small series, or autopsy reports, most of which were collected over a decade ago.
Interest in the natural history of pulmonary embolism has been rekindled by several recent developments. Advances in the treatment of malignant, cardiac, and pulmonary diseases may have influenced the types of patients presenting with pulmonary embolism. Treatment may be changing, with wider use of thrombolytic therapy and inferior vena cava filters.9 , 10 Patients have now been identified who present with chronic pulmonary embolism amenable only to surgical therapy.11
We report on the follow-up of a large number of patients in a national multicenter study who had clinically recognized pulmonary embolism.12 This study compared radionuclide lung scanning with pulmonary angiography in the diagnosis of pulmonary embolism. The protocol left therapeutic decisions up to the individual clinicians but required follow-up for all patients. This provided the opportunity to characterize the one-year clinical outcome in a large group of patients in whom pulmonary embolism was well documented and whose treatment represented prevailing medical practice.
Methods
Overall Study Design
The data analyzed and reported here are from the multicenter Prospective Investigation of Pulmonary Embolism Diagnosis (PIOPED) project. The protocol of this study has been reported elsewhere12 and was approved by the institutional review board at each hospital. Patients who had radionuclide lung scans ordered to evaluate suspected acute pulmonary embolism were recruited in six teaching hospitals from 1984 to 1985. A total of 1493 patients consented to participate in the study and were randomly assigned to one of two study groups: mandatory angiography (933 patients), which was the subject of an earlier report on the sensitivity and specificity of a lung scan,12 and angiography performed at the discretion of the attending physician (560 patients). The scans and angiograms were read at each hospital and again by the investigators at the coordinating center, who were unaware of each patient's clinical status.
This report describes only the patients who were found to have pulmonary embolism. This subgroup represented 26.8 percent of the 1487 patients assessed for this condition. An additional six patients were not included in this review because their lung scans were not interpretable.
Treatment
After diagnostic studies were performed, decisions about treatment and follow-up were made by the patients' attending physicians. Information about treatments given for pulmonary embolism was collected by reviewing the charts during hospitalization and at discharge from the hospital. Data on the duration and intensity of outpatient anticoagulation therapy were not collected. We classified treatment in four categories, as follows: (1) conventional therapy (intravenous heparin followed by conventional anticoagulation with warfarin or parenteral heparin13 , 14), (2) alternative therapy (including either thrombolytic therapy or embolectomy during hospitalization, followed by conventional anticoagulation with warfarin or parenteral heparin, or the insertion of any form of device into the inferior vena cava), (3) unconventional therapy (the use of antiplatelet agents, any other antithrombotic regimen, or both, given without the intention of achieving full anticoagulation), and (4) no treatment.
Follow-up Procedures
The purpose of prospective follow-up was to detect and analyze clinical events that could represent recurrences of pulmonary embolism or deaths due to this disorder. By design, this protocol detected only symptomatic events. After discharge from the hospital, each patient was contacted by telephone at 1, 3, 6, and 12 months. The reporting of any of the following events led to a detailed review of the patient's medical records by the outcome-classification committee: rehospitalization, any new investigation for pulmonary embolism, complications of anticoagulation, or death. In this review, all available clinical information was surveyed, including hospital and autopsy records, death certificates, and original radiographic studies.
Definition of Pulmonary Embolism
At entry into the study, the patients were classified as having pulmonary embolism if they met specific diagnostic criteria. Acute pulmonary embolism was diagnosed by pulmonary angiography when an embolus was identified that was obstructing a vessel or the outline of an embolus within a vessel (a filling defect) was present. Patients for whom there was evidence at autopsy of acute pulmonary embolism shortly after angiography were also classified as having had pulmonary embolism at entry. The final diagnosis of pulmonary embolism was based on the angiogram, unless the review by the outcome-classification committee contradicted the initial classification on the basis of the findings of repeat pulmonary angiography or autopsy. When there were disagreements between the angiogram readings of the outcome-classification committee and those of the investigators in the coordinating center, the committee's determination took precedence. Patients were not included in this analysis if both the angiogram and the review by the outcome-classification committee were inconclusive.
Outcomes
Causes of death and the presence of recurrent pulmonary embolism were assessed for one year after entry into the study. The cause of each death was established after a review of all available clinical information, findings at autopsy (if performed), and the patient's death certificate. Patients were classified as having died from pulmonary embolism if, in the opinion of the outcome-classification committee, this condition was the immediate or underlying cause of death. Diagnostic studies for recurrent pulmonary embolism were ordered by the attending physician on the basis of clinical suspicion and were not part of the study protocol.
Base-Line Variables
Data were collected at entry into the study on underlying illnesses, symptoms and signs, medications, arterial blood gas analyses, and the results of chest radiography and electrocardiography. Patients were considered to have coronary heart disease, chronic obstructive lung disease, or interstitial lung disease if these conditions occurred at any time before the study diagnosis. Otherwise, coexisting diseases were considered to be present if they occurred within three months before entry into the study. Pulmonary hypertension was defined as a mean pulmonary arterial pressure of ≥30 mm Hg measured just before pulmonary angiography. Ischemic heart disease was defined as a history of myocardial infarction or coronary heart disease. Left-sided congestive heart failure was defined as the presence of an S3 gallop, a history of congestive heart failure, or pulmonary edema on chest radiography. Chronic lung disease was defined by a history of chronic obstructive pulmonary disease or interstitial lung disease or by the presence of chronic obstructive lung disease or pulmonary fibrosis on chest radiography.
Statistical Analysis
The univariate relation between base-line characteristics and death was examined by chi-square statistics for categorical variables15 and t-tests for continuous variables.16 Fisher's exact test was used when the expected values were less than five.17 Differences in survival with respect to base-line characteristics were assessed by the Wilcoxon statistic.18 Because chi-square tests for proportions of patients surviving and Wilcoxon tests for survival consistently yielded similar results, only the chi-square P values are presented here. All P values are two-tailed.
We developed a Cox proportional-hazards model to identify predictors of death in patients with pulmonary embolism. To assess the reliability of the model, we used a split-sample technique. The 399 patients with pulmonary embolism were randomly assigned to one of two groups: a derivation set containing two thirds of the patients and a validation set containing the remaining third. We then developed the Cox proportional-hazards model18 by using backward stepwise variable selection19 in the derivation data set. The candidate variables entered in this data set were either (1) associated with death in the univariate analyses (P<0.2) and present in at least 10 percent of the patients with pulmonary embolism or (2) clinically relevant in their own right. We limited the number of such variables to nine, because the derivation data set included only 65 patients who died. To validate the model, variables remaining after the backward stepwise variable-selection process were forced into a fixed Cox proportional-hazards model with the confirmatory data set. The variables were then examined for statistical significance, and the beta coefficients were compared with the results from the derivation set. Relative risks and 95 percent confidence intervals were calculated by standard methods.19
The analyses were performed at the Robert Wood Johnson Medical School with a data tape provided by the study's data and coordinating center. SAS version 6.0320 was used in all the analyses except those involving the Cox proportional-hazard models, which were run with SAS version 5.18.21
Results
Characteristics of the Study Population
Three hundred ninety-nine of the 1487 patients (26.8 percent) were found to have pulmonary embolism at entry into the study and are included in this report. Three hundred eighty-two had pulmonary embolism identified on angiogram readings by investigators at the coordinating center; 4 had negative readings by these investigators, but pulmonary embolism was determined to be present by the outcome-classification committee; 1 had an uncertain angiogram reading with pulmonary embolism determined to be present by the outcome-classification committee; and 12 had no angiogram, but pulmonary embolism was determined to be present by the committee. One year of follow-up was complete for 396 of the 399 patients (99 percent). The distribution of selected base-line characteristics in the patients with pulmonary embolism is presented in Table 1Table 1
Selected Base-Line Characteristics of 399 Patients with Pulmonary Embolism.. Eighteen patients (4.5 percent) had a diagnosis of deep venous thrombosis at discharge.Deaths
Ninety-five patients with pulmonary embolism (23.8 percent) died within one year of entry into the study. As shown by the mortality curve in Figure 1Figure 1
One-Year Mortality Curve in 399 Patients with Pulmonary Embolism., most of the deaths occurred early in the follow-up period. Twenty-two percent occurred within one week of entry, and 23 percent within two weeks. The inhospital mortality rate for patients with pulmonary embolism was 9.5 percent.Only 10 of the 399 patients with pulmonary embolism (2.5 percent) died from that condition. Table 2Table 2
Causes of Death in 95 Patients with Pulmonary Embolism. shows the underlying causes of death in the patients who died during the year of follow-up. Of the 95 deaths in the patients with pulmonary embolism, 34.7 percent were due to cancer, 22.1 percent to sepsis, 16.8 percent to cardiac disease, and only 10.5 percent to pulmonary embolism.Of the 10 deaths due to pulmonary embolism, 8 occurred within one week of entry into the study, and 9 occurred within two weeks. Five of these patients died within one day of entry into the study.
Treatment of Pulmonary Embolism
The vast majority of the patients with pulmonary embolism (94 percent) received some form of treatment for that condition. Two hundred ninety-one patients (73 percent) received conventional therapy. Thirty-eight patients (10 percent) had interruption of the vena cava, 23 (6 percent) had thrombolytic therapy, and 1 (0.25 percent) underwent embolectomy. For 24 patients (6 percent), neither inpatient nor outpatient treatment for thromboembolism was provided. Of these 24 patients, 19 had negative angiogram readings at the local hospital that were in disagreement with later readings at the coordinating center. The remaining 22 patients (6 percent) received unconventional antithrombotic therapy for thromboembolism.
Of the 291 patients receiving conventional treatment, 56 (19.2 percent) died within one year of entry into the study. The one-year mortality rate in patients who had interruption of the vena cava was 36.8 percent; in those receiving thrombolytic therapy, it was 8.7 percent; in those receiving unconventional treatment, 45.5 percent; and in untreated patients, 50.0 percent. Among the 12 untreated patients who died, pulmonary embolism was the cause of only one death. The remaining 11 untreated patients were critically ill at entry into the study and died of their underlying diseases. Of the 10 patients who died of pulmonary embolism, only 1 was untreated.
Predictors of Death
The factors found on univariate analysis to be associated with mortality were age greater than 60 years, congestive heart failure, pulmonary hypertension, ischemic heart disease, chronic lung disease, cancer, and stroke (Table 3Table 3
Selected Characteristics of 399 Patients and Their Relation to Mortality.). In the stepwise Cox proportional-hazards analysis, mortality was associated in the derivation set with cancer (relative risk, 3.8; 95 percent confidence interval, 2.3 to 6.4), left-sided congestive heart failure (relative risk, 2.7; 95 percent confidence interval, 1.5 to 4.6), history of chronic lung disease (relative risk, 2.2; 95 percent confidence interval, 1.2 to 4.0), and age greater than 60 (relative risk, 2.2; 95 percent confidence interval, 1.2 to 4.1). The results were similar in the validation set, except that the variable of age greater than 60 was not significantly associated with the one-year mortality rate (Table 4Table 4
Characteristics Associated with One-Year Mortality in the 399 Study Patients.*).Recurrent Pulmonary Embolism
Thirty-three of the 399 patients with pulmonary embolism (8.3 percent) had a clinically apparent recurrence of pulmonary embolism in the year of follow-up, as determined by the finding of a new pulmonary embolism at autopsy (in 7 patients) or on angiography (13 patients), by the development of new perfusion-scan defects consistent with a high probability of pulmonary embolism (8 patients), or by a convincing clinical presentation (5 patients). These recurrences developed soon after diagnosis, with 16 of the 33 patients (48 percent) having recurrences within one week of entry into the study. The rates of recurrence were similar among the treatment groups. Of the 33 patients with a recurrence, 15 (45 percent) died during the follow-up period, with pulmonary embolism accounting for nine of these deaths. Of the 10 patients who died from pulmonary embolism in this study, 9 had recurrent pulmonary embolism.
Discussion
Although the one-year mortality rate among the 399 patients with clinically apparent pulmonary embolism was nearly 24 percent, death from pulmonary embolism itself occurred in only 2.5 percent. Cardiac disease, pulmonary disease, cancer, and sepsis accounted for nearly two thirds of the 95 deaths. Most patients dying of pulmonary embolism were already quite ill, and pulmonary embolism was often the final event in a setting of serious cardiopulmonary disease or cancer. Deaths from pulmonary embolism usually occurred within two weeks after the diagnosis was made. This finding is consistent with the notion that the lethal effects of pulmonary embolism are most pronounced early in a patient's course.22
Among the patients with pulmonary embolism, cancer was associated with a nearly fourfold increase in mortality at one year, and left-sided congestive heart failure with a nearly threefold increase. Ischemic heart disease was not an independent predictor of death, perhaps because in patients with heart disease left ventricular function is the most important factor associated with survival.23 , 24
The results of our study are consistent with outcomes previously observed in patients with clinically recognized pulmonary embolism. In two large therapeutic trials, the two-week mortality rate for pulmonary embolism was approximately 8 percent, whereas the six-month mortality rate was 13 percent.25 , 26 In another report, patients with pulmonary embolism had a 17 percent mortality rate, but pulmonary embolism was itself the cause of death in only 3 percent of the patients.22 In patients without preexisting cardiac or pulmonary disease, the reported one-year mortality rate was low, ranging from 3 percent to 9 percent.27 , 28 In patients with massive pulmonary embolism, Hall et al. described an 18 percent in-hospital mortality rate, with a five-year mortality rate of 17 percent among those surviving to discharge.29 We conclude, with the authors of these reports, that when correctly diagnosed and treated, pulmonary embolism is an unusual cause of death.
Cardiac disease is a major contributor to mortality in patients with pulmonary embolism.6 , 22 , 28 Although we confirmed this association, we also found that cancer was a frequent cause of death. This observation probably reflects the introduction of more aggressive treatments in patients with advanced cancer. Such improved care may also have evolved with regard to chronic lung disease, the other contributor to mortality. Our findings support the concept that pulmonary embolism often accompanies advanced illnesses that predispose patients to thromboembolism: venous stasis, hypercoagulable states, or vascular injury.
Clinically apparent recurrent pulmonary embolism was diagnosed in 8.3 percent of our patients. This suggests that symptomatic recurrent pulmonary embolism occurs in a small minority of patients with properly diagnosed and treated disease, as previously hypothesized.8 , 26 , 28 29 30 31 In previous prospective therapeutic studies, rates of recurrence have ranged from 4 percent to 17 percent.25 , 26 The higher rates have often been based on the results of follow-up lung scanning rather than on the development of new symptoms.8 , 32 , 33 In our series, we chose to investigate patients for a recurrence of pulmonary embolism if they had new symptoms. Asymptomatic recurrent pulmonary emboli may have gone undiagnosed.
In our patients, pulmonary embolism recurred most frequently during the first week of follow-up. Previous reports have described a similarly vulnerable period in the first four to six weeks of therapy, when thromboembolic recurrence is most common.13 , 34 Such recurrence was associated with a case fatality rate of 45 percent during follow-up, and 9 of 10 deaths from this condition in this series were in patients with recurrences. Therefore, recurrent pulmonary embolism often had lethal consequences.
Since the study protocol did not prescribe treatment for pulmonary embolism, the therapy given the patients reflected practice preferences in our six tertiary care hospitals. Most patients received conventional anticoagulation therapy with heparin followed by warfarin. A relatively small percentage (16 percent) received thrombolytic drugs or interruption of the vena cava. Bias in patient selection may make comparison of the outcomes associated with each therapy misleading. Nonetheless, our data support the belief that in most patients standard anticoagulation therapy alone was associated with infrequent recurrences and deaths from pulmonary embolism.
There are two limitations to our study. All our patients were thought to have pulmonary embolism, and they all underwent diagnostic evaluation. The overall population of patients with pulmonary embolism is broader than our study group and includes those whose emboli are never diagnosed. The prognosis of patients with unsuspected emboli is unknown, and unrecognized pulmonary embolism remains a major cause of mortality in the hospital.35 A second limitation is that our follow-up period was limited to one year. Most pulmonary emboli recur within a few months of follow-up, as our results confirm. However, the incidence of recurrent pulmonary embolism beyond one year remains unknown.
In our study, pulmonary embolism occurred most often in the presence of chronic disease, and the underlying diseases, rather than pulmonary embolism itself, were responsible for most of the deaths. The deaths from pulmonary embolism, as well as the recurrences of the disorder, tended to occur within two weeks of the diagnosis. Conventional anticoagulation therapy was associated with low mortality from pulmonary embolism and with infrequent recurrences. When clinically apparent pulmonary embolism did recur, however, it was associated with a high death rate.
Supported in part by the National Heart, Lung, and Blood Institute.
We are indebted to Robert McMahon, Ph.D., for assistance in planning the regression analyses, to Sharon Pruitt for assistance with the outcome-classification committee, to Patricia Cerro for assistance in the preparation of the manuscript, and to the other investigators for their efforts in carrying out the study.
Source Information
From the Division of General Internal Medicine, Department of Medicine, University of Medicine and Dentistry of New Jersey, Robert Wood Johnson Medical School, New Brunswick (J.L.C., A.D.); the Departments of Medicine (M.A.K., H.I.P., J.S.S.) and Radiology (M.A.S., A.A.), University of Pennsylvania School of Medicine, and the Leonard Davis Institute of Health Economics (J.S.S.), Philadelphia; the Department of Medicine, University of Michigan Medical School, Ann Arbor (J.G.W.); the Department of Medicine, Duke University Medical School, Durham, N.C. (W.J.F.); the Department of Medicine, Massachusetts General Hospital, Boston (B.T.T.); the Department of Medicine, Henry Ford Hospital, Detroit (J.P.); and the Maryland Medical Research Institute, Baltimore (T.E.H., M.L.T.). Address reprint requests to Dr. Carson at the Division of General Internal Medicine, University of Medicine and Dentistry of New Jersey, Robert Wood Johnson Medical School, 97 Paterson St., New Brunswick, NJ 08903.
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