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1 All authors: Department of Radiology, Medical College of Wisconsin and Froedtert Memorial Lutheran Hospital, 9200 W Wisconsin Ave., Milwaukee, WI 53226-3596.
Received April 9, 2004;
accepted after revision June 30, 2004.
Address correspondence to L. R. Goodman
(lgoodman{at}mcw.edu).
Abstract
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MATERIALS AND METHODS. All patients were examined using 8- or 16-MDCT. Reported findings on combined CT pulmonary angiography and CT venography of 1,435 consecutive patients were analyzed retrospectively. The charts of patients of interest with ISSPE or with indeterminate or inconclusive pulmonary embolism results were analyzed for clinician response and recurrent symptoms of venous thromboembolism in both treated and untreated patients during the following 3 months.
RESULTS. We studied 207 patients of interest, and follow-up was available on 192 (92.8%) (67 ISSPEs, 125 inconclusive). Of the 192 patients, 25 (37%) of 67 patients with ISSPE and 108 (86%) of 125 patients with inconclusive results did not receive anticoagulation. Two patients with ISSPE and two patients with inconclusive results returned with new symptoms suggesting recurrent venous thromboembolism, but no venous thromboembolism was found. Thirteen (10%) of 133 untreated patients died without clinical evidence of recurrent venous thromboembolism. In 61 patients who received anticoagulation (42/67 [63%] ISSPE and 17/125 [14%] inconclusive), five patients returned with venous thromboembolism symptoms. None had recurrent emboli. Two (3%) of 61 patients who received anticoagulation died of other diseases.
CONCLUSION. Patients with ISSPE more commonly received anticoagulation than not. In the patients who did not receive anticoagulation, no recurrent pulmonary embolism was identified on follow-up. In most patients with inconclusive findings on CT pulmonary angiography, clinicians chose to withhold anticoagulation without additional imaging workup. No adverse effects of this clinical decision were uncovered.
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Historically, approximately 6% of patients with a suspected pulmonary embolism have had isolated subsegmental thromboembolism (ISSPE) when studied by conventional angiography [15, 16]. Because patients with proven pulmonary embolism are believed to have an increased risk of recurrence in the near future, even patients with small emboli are usually treated with anticoagulation. However, few good historical data show a need to anticoagulate patients with an ISSPE. If small pulmonary embolisms are not clinically important under certain circumstances, then perhaps anticoagulation, with its associated expense, morbidity, and mortality, can be avoided. It is not clear how clinicians are responding to the detection of small pulmonary embolisms reported on MDCT when there is no CT evidence of deep venous thrombosis (DVT).
In addition, a number of CT studies are suboptimal because of patient- or equipment-related problems. We also looked at clinician response to these inconclusive MDCT reports. Probably a number of pulmonary embolisms are missed in these patients. Most of these undetected pulmonary embolisms are probably small, because larger pulmonary embolisms often can be detected on suboptimal scans.
It would be difficult, and perhaps unethical, to conduct a prospective controlled study in which one withheld anticoagulation in a large group of symptomatic patients with proven pulmonary embolism. This article reports the results of a retrospective outcome study of patients with reported MDCT findings of ISSPE and no DVT, or inconclusive CT findings for pulmonary embolism and no DVT, to determine clinician response and to compare the 3-month clinical recurrence rate of patients with venous thromboembolism who did not receive anticoagulation with those who did.
Specifically, this project addresses three questions: How do physicians respond to a CT report of "ISSPE, no DVT?" How do physicians respond to a CT report of "inconclusive for pulmonary embolism, no DVT?" And what is the subsequent venous thromboembolism rate for these patients, whether receiving anticoagulation or observed?
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CT Protocol
Standard technique for MDCT pulmonary arteriography at our institution is
to use 120 mL of nonionic contrast material injected at a rate of 4 mL/sec,
and with a scanning delay of 20–28 sec. Scanning is performed from the
diaphragm to the lung apices on an 8- or 16-MDCT scanner (LightSpeed, GE
Healthcare) using 140 kVp, 300–500 mA, 0.5- to 0.7-sec rotation time,
and pitch of 1.375. Slice thickness is 1.25 mm. In obese patients, 2.5-mm
images are reconstructed in an effort to reduce image noise. After 3.5 min
from the start of the contrast injection, 5-mm axial images are obtained every
2 cm from the iliac crest to the knees to evaluate the iliac, femoral, and
popliteal veins. These axial scans are obtained at 120 kVp, 210 mA, and
0.8-sec rotation. In this study, all scans were interpreted by faculty
radiologists at one of several workstations. No standard format was used for
reporting. Multiplanar reconstructions were not used routinely but could be
used at the discretion of the interpreting physician.
Data Collection
The impressions of the final CT reports were retrospectively analyzed, and
the patients were classified into groups on the basis of the presence or
absence of pulmonary embolism, the location of the most central pulmonary
embolism (central, segmental, or subsegmental), and the presence or absence of
DVT. In approximately 9% of cases, some uncertainty existed regarding
depiction of the peripheral pulmonary vessel and the reviewer stated that
small pulmonary embolism could not be excluded because of patient-related
factors, technical factors, or unspecified reasons. These patients with a
suboptimal or indeterminate scan are termed "inconclusive." No
scans were excluded from the study because of quality concerns.
The charts of patients of interest (ISSPE or inconclusive) were reviewed by one of the authors for the clinician response to the scan results and for a 3-month follow-up to look for evidence for recurrent pulmonary embolism or DVT symptoms. Other imaging studies for venous thromboembolism within 72 hr of the index CT were recorded, as were the results of those studies. Charts were also reviewed to establish whether patients received anticoagulation (before or after CT) and whether clinicians gave the diagnosis of venous thromboembolism on the discharge summary. All hospitalizations and clinic visits during the next 3 months were reviewed for possible symptoms related to pulmonary embolism or DVT. Records of follow-up visits were closely reviewed for new imaging studies related to venous thromboembolism, for subsequent anticoagulation, and for patient outcomes. Charts of patients who died were analyzed for evidence of venous thromboembolism contributing to that death. Autopsy results were reviewed.
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Patients of interest included 77 patients with reported ISSPE (mean age, 51.0 years; 38 women and 39 men) and 130 patients with an inconclusive pulmonary embolism study (mean age, 51.2 years; 59 women and 71 men). These 207 patients included 138 inpatients (67%), 13 outpatients (6%), and 56 emergency department patients (27%). Fifteen patients of interest (7%), 10 with reported ISSPE and five with inconclusive findings, were lost to follow-up.
Patients with ISSPE
Of the 77 patients who had a diagnosis of ISSPE and no DVT, 32 patients
(42%) did not receive anticoagulation. Of these 32 patients, 25 (78%) had an
adequate 3-month follow-up (Fig.
1). Of these 25 patients, two patients had symptoms suggesting
recurrent pulmonary embolism, and both subsequently had repeated MDCT that was
negative for venous thromboembolism (Table
2). Five of the 25 patients died of other causes while in the
hospital. The causes of death were listed as gun-shot wound, traumatic brain
injury with acute respiratory distress syndrome (with autopsy showing no
pulmonary embolism), intracranial hemorrhage, sepsis and eventual cardiac
arrest, and sepsis and acute renal failure in the setting of end-stage
astrocytoma. Pulmonary embolism was not listed as a cause of mortality or
morbidity in any of these patients.
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Of patients with ISSPE who received anticoagulation, 42 (93%) of 45 had follow-up and 14 had already been receiving anticoagulation therapy before CT because of underlying medical conditions or a history of thromboembolic disease. Anticoagulation was continued in these patients, and one of these patients died of an unrelated cause (metastatic lung carcinoma) within the next 3 months. Thirty-one patients received anticoagulation because of the results of CT pulmonary angiography showing ISSPE. Two patients had symptoms consistent with pulmonary embolism in the next 3 months, and both subsequently had negative findings on MDCT. One patient died within a month of the initial study; autopsy showed no evidence of pulmonary embolism but indicated peritonitis and hemorrhage as the cause of death. During the 3 months, five (15%) of 33 untreated patients died and two (4.4%) of 45 patients undergoing anticoagulation died.
Of the patients with ISSPE, 22 (28.6%) had another imaging study (including either ventilation–perfusion scanning, lower extremity sonography, upper extremity sonography, pulmonary angiography, or repeated MDCT) within 72 hr of the index CT (Table 3). Overall, nine studies were done before and 13 studies after the index MDCT. Seven of these patients underwent ventilation–perfusion scanning, five before CT (results ranging from negative to high probability for pulmonary embolism) and two after CT (one reported as negative and one as low probability for pulmonary embolism). Eleven patients underwent lower extremity sonography: sonographic findings for one patient were positive for DVT before CT; for two patients were negative for DVT before CT; and for eight patients were negative for DVT after CT. One patient had upper extremity sonography that was positive for DVT before CT. Two patients had repeated CT, both of which showed no changes (i.e., ISSPE only). One patient underwent pulmonary angiography after CT that showed negative findings. Of the nine studies performed after the initial CT pulmonary angiography, two (one ventilation–perfusion scanning and one angiography) did not support the CT pulmonary angiography diagnosis of ISSPE.
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Patients with Inconclusive CT Findings
One hundred thirty patients (9%) had inconclusive results for pulmonary
embolism and no DVT. Five of these patients (4%) were lost to follow-up. Eight
died of unrelated causes during the follow-up period. Three patients were
treated with warfarin because of presumed pulmonary embolism (two of these
patients had no further studies; one had ventilation–perfusion scanning
that was nondiagnostic because of obesity). Twelve of the 130 patients had
been receiving anticoagulation before CT, and this was continued. Two other
patients were given warfarin after the time of the inconclusive CT (one
because of known DVT, one because of valve replacement). Thus, 17 (13%) of 130
patients with inconclusive results on pulmonary embolism studies received
anticoagulation, and 113 patients did not. Seventeen and 108 patients,
respectively, had an adequate 3-month follow-up. Symptoms suggestive of
pulmonary embolism recurred in three (18%) of 17 patients receiving
anticoagulation and in two (2%) of 108 untreated patients
(Fig. 2 and
Table 4). Pulmonary embolism in
all five patients was subsequently ruled out by repeated CT pulmonary
angiography. Two patients had symptoms suggesting lower extremity DVT in the
following 3 months with no pulmonary symptoms. Lower extremity sonography was
equivocal for one; and one was already receiving warfarin because of aortic
valve replacement. Eight patients died of unrelated medical problems (one each
from esophageal cancer, pancreatic cancer, breast cancer, pneumonia, acute
monocytic leukemia, and acute respiratory distress syndrome; and two from
brain metastases), and none of these patients received anticoagulation.
Pulmonary embolism was not implicated in any of these deaths. Thus, no
recurrent venous thromboembolism was found in either the treated or untreated
patients with inconclusive CT reports during the follow-up period.
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In the inconclusive subgroup, 36 patients (27%) had at least one other imaging study within 72 hr of the index CT. Overall, 19 studies were done before and 17 studies after the index MDCT (Table 5). Nineteen of these patients had ventilation–perfusion scanning: 11 of these examinations were performed before CT (results ranging from invalid because of obesity to intermediate probability) and eight after CT (five negative for pulmonary embolism, and three, low probability for pulmonary embolism). Thirteen patients underwent lower extremity sonography (including two patients who also had ventilation–perfusion scanning): three with results positive for DVT before CT; five with negative results for DVT before CT; and five patients with negative results for DVT after CT. Four patients had repeated CT (including two patients who also had ventilation–perfusion scanning). Findings in all four were negative. In the 17 studies done after the index CT, results of five ventilation–perfusion scans, five lower extremity sonograms, and four CTs were interpreted as negative, and three ventilation–perfusion scans, as low probability. Thus, no imaging evidence of venous thromboembolism was discovered on the 17 studies performed in the 3 days (72 hours) after inconclusive CT results.
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Several major limitations of this study should be emphasized. First, there was no gold standard for the presence or absence of venous thromboembolism. Therefore, our results reflect actual clinical practice rather than the consequences of true subsegmental pulmonary embolism, because false-positive and false-negative cases may have been included in the study population. Establishing a gold standard for ISSPE is difficult. Stein et al. [15] and Diffin et al. [16] have emphasized that even with pulmonary angiography, experienced reviewers often disagree on the presence or absence of pulmonary embolism at the subsegmental level.
Second, our follow-up was based solely on retrospective review of clinical records, imaging procedures, anticoagulation records, and autopsies. Although it is unlikely that major recurrent pulmonary embolism would go un-noted in this review, it is possible that minor symptoms of venous thromboembolism were not recognized, were not studied, and resolved spontaneously. Because the nine patients who returned with signs and symptoms suggesting pulmonary embolism all had negative subsequent workups, it is unlikely that any initially had large central emboli. However, it is possible that impediments to the CT diagnosis of pulmonary embolism on the index examination (respiratory motion, obesity, metallic clips, distorted anatomy) also may have degraded the follow-up CT studies, making the diagnosis of recurrent pulmonary embolism equally difficult.
It is also possible that some patients with signs and symptoms of pulmonary embolism were seen at other facilities and therefore were beyond the reach of our review. Fifteen patients (7%) of interest were lost to follow-up, including 12 who did not receive anticoagulation. Fifteen patients (7%) of interest died during the follow-up period. It is possible that undetected pulmonary embolism contributed to some of their deaths, although no such occurrence was reported. Many autopsy studies attest to the large number of patients who die of, or with, undetected pulmonary embolism. Two autopsies were negative for pulmonary embolism. Thus, 15 lost patients are not accounted for and 13 patients who died were not fully evaluated.
Finally, physician selection clearly had a role in determining who received anticoagulation and who was untreated. It would have been helpful to know the preimaging clinical likelihood of venous thromboembolism relative to the decision to treat or not to treat. Structured clinical likelihood scores, as suggested by Wells et al. [17], are not routinely used at our hospital, and nonstructured thoughts are hazardous to assess in retrospect. Probably patients with high clinical probability or limited cardiopulmonary reserve [18] were more likely to be treated than other patients.
Although our study had limitations, the data resulting from our study are in keeping with data from other published studies of venous thromboembolism. In this study, we observed ISSPE in 77 (24.4%) of 316 patients in whom CT pulmonary angiography was interpreted as positive for pulmonary embolism. Similarly, de Monye et al. [19] reported that 22.3% of patients with CT-depicted pulmonary embolism had ISSPE. Diffin et al. [16] observed ISSPE in 17% of patients with pulmonary embolism using conventional angiography. Overall, 5.4% of the total study population of patients with suspected pulmonary embolism were diagnosed with ISSPE, similar to the results of prior angiographic studies that reported ISSPE in 4–6% of all patients [15, 16, 19].
Our study found the rate of indeterminate or suboptimal scans to be 9.1%. In our categorization, any hesitation or uncertainty on the part of the reviewer was included in this group. Reports of inconclusive studies in the literature are in the same range [11, 20].
In our study, 32 (42%) of 77 patients thought to have ISSPE and no DVT and 113 (87%) of 130 patients with inconclusive findings and no DVT did not receive anticoagulation. Most did not have additional imaging studies at the time of the index case. One must presume that, of the 113 patients with suboptimal scans, some had a small undetected pulmonary embolism. Yet, in our study, no clinically apparent pulmonary embolisms were discovered within 3 months of the initial MDCT in either group. Among the 25 patients with ISSPE and the 100 patients with inconclusive studies who were followed up without anticoagulation for 3 months, only nine patients had clinical events suggestive of acute pulmonary embolism, and all nine subsequently had negative studies for pulmonary embolism. These results are in the same range as negative findings on conventional angiography or negative findings on scintigraphy [21]. The CT pulmonary angiography results are undoubtedly improved by the documented absence of DVT at CT venography in our patients.
The clinical relevance of small pulmonary embolism is difficult to ascertain. There is little in the literature concerning outcomes of patients with proven small emboli who did not receive anticoagulation. Stein et al. [22], in reviewing the Prospective Investigation of Pulmonary Embolism Diagnosis (PIOPED) results, found 20 patients who were initially diagnosed as being free of pulmonary embolism and not treated but who subsequently were judged by the expert review panel as having small pulmonary emboli. One patient (5%) died of recurrent pulmonary embolism and one patient (5%) had a nonfatal recurrent pulmonary embolism. All 20 untreated patients had fewer than three mismatched segmental perfusion defects, and pulmonary angiograms showed segmental or smaller clots in 16 (84%) of 19 patients. At our hospital, Schultz et al. [23] reported 17 trauma patients with no symptoms of venous thromboembolism who had minor clot burden and no DVT on MDCT. Patients did not receive anticoagulation, and none developed signs or symptoms of recurrent pulmonary emboli during their hospitalization. The 10 patients with available 3-month follow-up had no evidence of thromboembolic disease. These patients were studied during the same time period as our study and are included in our results.
To date, at least seven clinical outcome studies of patients with negative findings on CT pulmonary angiography who were un-treated have been published. At 3–12 months, the subsequent pulmonary embolus rate was approximately 1%, with a fatality rate of 0.2–0.6% [24]. If MDCT is in fact 90–95% sensitive, 5–10% of these patients can be presumed to have an untreated small pulmonary embolism.
Hull et al. [25] monitored 371 patients with good cardiopulmonary reserve who had low- or intermediate-probability results on ventilation–perfusion scanning, serial negative findings on deep venous impedance plethysmography, and no anticoagulation for 3 months. Stein et al. [26] estimate that 21% of these patients had an un-treated small pulmonary embolism. Subsequent clinically apparent venous thromboembolism was found in 2.7% of cases. In an earlier study, Hull et al. [18] compared two groups with low-probability ventilation–perfusion scans who did not receive anticoagulation: 117 with poor cardiopulmonary reserve and 627 with good cardiopulmonary reserve. Twelve (10%) of the 117 and 12 (2%) of the 627 had venous thromboembolism during the 3-month follow-up.
Gurney [3] has suggested that small emboli are common and that a healthy lung acts as a filter to protect the systemic circulation. Small emboli are usually asymptomatic and resolve unnoticed. Pulmonary emboli may be incidental findings on CT performed for other reasons. Approximately 2% of inpatients and approximately 0.5% of outpatients have incidental emboli diagnosed on contrast-enhanced CT performed for other reasons [27].
The importance of small pulmonary embolism must be balanced against the risk of anticoagulation, which includes a 1% fatality rate and a 7% major complication rate per treatment year [28].
Our study suggests that patients who receive a CT diagnosis of ISSPE, under certain circumstances (i.e., good cardiopulmonary reserve, self-limited risk factors), may not need anticoagulation. Because ISSPE may be the warning of subsequent pulmonary embolism from the deep veins, negative findings on a lower extremity study are mandatory. This is clearly a departure from traditional teaching, and additional retrospective and prospective outcome studies will be required to prove or disprove this.
MDCT pulmonary angiography and venography for suspected venous thromboembolism are safe, readily available, and increasingly being used. Recent advances in technology allow faster scanning, thinner images, and more reproducible interpretations [9]. At least in a small, physician-selected group of patients with negative results on CT venography, patients with MDCT findings of ISSPE or suboptimal results did not have detectable pulmonary embolism within a 3-month period. Perhaps further studies will show that anticoagulation can safely be withheld from patients who meet these criteria.
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