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(Radiology. 2000;216:744-751.)
© RSNA, 2000


Vascular and Interventional Radiology

Deep Venous Thrombosis: Detection by Using Indirect CT Venography1

Matthew D. Cham, MD, David F. Yankelevitz, MD, Dorith Shaham, MD, Ami A. Shah, MD, Leonard Sherman, MD, Andrew Lewis, MD, Jurgen Rademaker, MD, Gregory Pearson, MD, Junsung Choi, MD, William Wolff, MD, Pilar M. Prabhu, MD, Michael Galanski, MD, Robert A. Clark, MD, H. Dirk Sostman, MD and Claudia I. Henschke, MD, For the Pulmonary CT Angiography-Indirect CT Venography Cooperative Group

1 From the New York Presbyterian Hospital/Weill Medical College of Cornell University, 525 E 68th St, Bldg Starr-8A23, New York, NY 10021 (D.F.Y.). The Department of Radiology, the New York Presbyterian Hospital, Cornell Campus, New York, NY (M.D.C., D.F.Y., A.A.S., H.D.S., C.I.H.); the Department of Radiology, Hadassah University Hospital, Israel (D.S.); the Department of Radiology, the New York Hospital of Queens, New York, NY (L.S., W.W.); the Department of Radiology, St Barnabas Hospital, Bronx, NY (A.L., P.M.P.); the Department of Radiology, Charite, Campus Virchow Hospital, Berlin, Germany (J.R.); the Department of Radiology, the Hannover Medical School, Hannover, Germany (M.G.); the Department of Radiology, the New York Presbyterian Hospital, Columbia Campus, New York, NY (G.P.); and the Department of Radiology, the H. Lee Moffitt Cancer Center and Research Institute, Tampa, Fla (J.C., R.A.C.). Received June 11, 1999; revision requested August 3; revision received December 8; accepted December 16. Financial support is listed at the end of this article. Address correspondence to D.F.Y.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To assess the clinical benefits of performing indirect computed tomographic (CT) venography after pulmonary CT angiography to detect deep venous thrombosis (DVT) in patients suspected of having a pulmonary embolism.

MATERIALS AND METHODS: The authors prospectively enrolled 541 consecutive patients who underwent pulmonary CT angiography for suspected pulmonary embolism at seven institutions. Using a protocol that optimizes venous enhancement without additional contrast material injection, the authors obtained contiguous images from the pelvis to the popliteal fossa. Ultrasonography (US) also was performed in 116 patients.

RESULTS: DVT was found at indirect CT venography in 45 (8%), and pulmonary embolism was found at pulmonary CT angiography in 91 (17%) of 541 patients. Among the 45 patients with DVT, DVT occurred in 16 patients who had no pulmonary embolism at pulmonary CT angiography, which increased the diagnosis of thromboembolic disease by 18%. Among 116 patients who underwent US and indirect CT venography, 15 had DVT at US, and in all 15, DVT also was seen at indirect CT venography. In four additional cases, DVT was seen at only indirect CT venography.

CONCLUSION: Among patients suspected to have pulmonary embolism, a substantial number had DVT in the absence of pulmonary embolism. Combined pulmonary CT angiography–indirect CT venography can depict these cases with accuracy comparable to that of US and thus could have a significant effect on patient care.

Index terms: Computed tomography (CT), angiography, 944.12916 • Embolism, pulmonary, 60.721 • Pulmonary arteries, CT, 944.12915, 944.12916 • Pulmonary arteries, thrombosis, 944.751


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Deep venous thrombosis (DVT) is a serious clinical condition that affects millions of people worldwide. Pulmonary embolism and DVT have been described as different manifestations of the same disease process (1,2). DVT often is asymptomatic and is associated with recurrent DVT and pulmonary embolism when treated inadequately (36). In one prospective series, five (83%) of six patients who developed pulmonary embolism after normal pulmonary angiography had either a history or prior evidence of DVT (7). In the United States alone, the progression of DVT into pulmonary embolism has been estimated to cause 40,000–200,000 deaths annually (810). The accurate detection of DVT thus is necessary for prompt treatment.

Ventilation-perfusion (V-P) scanning has been the most commonly used noninvasive examination for diagnosing pulmonary embolism. About 90% of patients with high-probability V-P results have DVT (11,12). However, about 70% of patients evaluated for pulmonary embolism do not have high-probability V-P scans and may require further evaluation, as up to 40% have DVT (11,1316). As a result, many algorithms designed for the diagnosis of pulmonary embolism now include DVT imaging to detect thromboembolic disease (14,17). Ultimately, the detection of thromboembolic disease is used to determine patient care.

Many institutions now include computed tomography (CT) as their initial diagnostic examination for pulmonary embolism. Technical advances in CT of the pulmonary arteries (pulmonary CT angiography) have enabled the accurate detection of pulmonary embolism down to the level of the segmental pulmonary arteries (18). Because of the need to further evaluate those patients who do not receive a diagnosis of pulmonary embolism, some investigators have examined the deep venous system by using CT. Initially, direct CT venography of the lower extremities was used to detect DVT. This had a sensitivity of 100% (44 of 44 patients) and a specificity of 96% (57 of 59 patients) compared with conventional venography and was superior in detecting thrombus extension into the pelvic veins and the inferior vena cava (19). However, direct CT venography required an additional contrast material injection. We thought this was unnecessary, since newer CT protocols, referred to as indirect CT venography, have been developed to assess the deep venous system immediately after pulmonary CT angiography (20,21).

The benefits of indirect CT venography are numerous: First, it uses only the contrast material already in circulation from pulmonary CT angiography. Second, it maximally enhances the pelvic and lower extremity veins while maintaining optimum pulmonary arterial enhancement during pulmonary CT angiography (20). Third, it adds only 3 minutes to the overall examination time. Fourth, it can be used to evaluate for both pulmonary embolism and DVT by using a single examination, which allows for the immediate treatment of patients who have only DVT.

Our goal was to assess the incremental information provided by the addition of indirect CT venography to pulmonary CT angiography to help detect DVT in patients suspected of having a pulmonary embolism. Part of this assessment included a comparison with duplex ultrasonography (US) and V-P scanning. We also evaluated the overall technical quality of the images.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
To determine the additional information provided by indirect CT venography as an adjunct to pulmonary CT angiography, we used the standard New York Presbyterian Hospital (Cornell Campus) pulmonary CT angiographic and indirect CT venographic protocol, which was designed to optimize the venous enhancement of the lower extremity while maintaining near-maximal enhancement in the pulmonary arteries (20). Although this examination was performed for accepted clinical indications and was considered acceptable for patient care, institutional review board approval was obtained. Informed consent was obtained from each patient after the nature of the procedure had been explained fully.

The protocol was as follows: First, digital scout CT images of the chest, pelvis, and lower extremities to the level of the knees were obtained. Next, 140 mL of nonionic contrast material (iohexol [Omnipaque 300; Nycomed Amersham, Princeton, NJ]) was infused through an arm vein at 3 mL per second. Helical CT was started after a delay of 28 seconds. Images were obtained from the inferior pulmonary veins up to the aortic arch and spanned about 12–15 cm, with a section width of 3 mm and a pitch of 1.6–1.0. The patient was instructed to hyperventilate for five breaths and to hold his or her breath during the pulmonary CT angiographic portion of the examination. Helical scanning of the pelvis and the lower extremities began 120 seconds after pulmonary CT angiography was completed. This 120-second delay was used because it produced near-optimum enhancement in the lower extremity veins in a majority of patients (20). Lower extremity scanning was performed from the iliac crest down to the popliteal fossa, with a section width of 10 mm and with a pitch of 1:1. Calf imaging was not performed because it was found to be unnecessary in patients at risk for clinically important thromboembolic disease (22). The remainder of the chest, not scanned during the pulmonary CT angiographic portion of the protocol, was scanned after the completion of indirect CT venography. Standard photography was performed (that is, no unique parameters or settings were used to acquire the images), and reconstruction for the pulmonary CT angiographic portion was performed at 1-mm intervals. Indirect CT venography was evaluated by using standard 10-mm nonoverlapping images.

Between May 27, 1998, and March 15, 1999, we prospectively enrolled 541 consecutive patients who underwent pulmonary CT angiography for the suspicion of pulmonary embolism. Among the 541 patients, 233 (43%) were men and 308 (57%) were women. The patients were aged 18–98 years, with a median age of 65 years. The patient population was composed of all inpatients and outpatients whose physicians had ordered combined pulmonary CT angiography and indirect CT venography for the suspicion of pulmonary embolism. The protocol did not set any guidelines with regard to the ordering of pulmonary CT angiography-indirect CT venography, so clinicians ordered them as necessary. It is estimated that 90% of the patient population were inpatients.

The participating hospitals were the New York Presbyterian Hospital’s Cornell Campus (Cornell); the New York Hospital of Queens (Queens); the Hadassah University Hospital of Israel (Hadassah); St Barnabas Hospital (St Barnabas); the Medical School of Hannover, Germany (Hannover); the New York Presbyterian Hospital’s Columbia Campus (Columbia); and the H. Lee Moffitt Cancer Center (Moffitt). All seven institutions were given the same protocol and contributed 251, 125, 86, 29, 25, 14, and 11 cases, respectively.

The CT scanners used by each institution were as follows: Cornell, Queens, and St Barnabas used HiSpeed Advantage CT/I scanners (GE Medical Systems, Milwaukee, Wis); Hannover and Columbia used Somatom Plus 4 scanners (Siemens Medical Systems, Iselin, NJ); Moffitt used a Somatom Plus 5 scanner (Siemens Medical Systems); and Hadassah used a TwinFlash scanner (Elscint, Haifa, Israel). The tube current and amperage used were those of the standard pelvic CT protocol at all institutions, around 150 kV and 200 mA.

For each patient, we performed pulmonary CT angiography that was followed by indirect CT venography, which resulted in approximately 140 images in the pulmonary arteries and 60 images in the pelvis and the lower extremities. At each participating institution, one to three radiologists were involved in reading the pulmonary CT angiographic–indirect CT venographic images. At Hannover, pulmonary CT angiography has been performed since 1995. At Cornell and Hadassah, pulmonary CT angiography has been performed since 1996. At Queens and Columbia, pulmonary CT angiography has been performed since 1997. The remaining two institutions began performing pulmonary CT angiography in 1998. In all institutions, indirect CT venography was a new examination.

One radiologist reviewed each image and used a structured data form to record whether pulmonary embolism and/or DVT were present and where their specific locations were. Information about the technical quality of pulmonary CT angiography and indirect CT venography and the results of other examinations (US, V-P scanning, conventional pulmonary angiography, and conventional venography) also were recorded. Radiologists read the pulmonary CT angiographic–indirect CT venographic images as a part of clinical care and were not required to be blinded to the prior results of US and V-P scanning. As only one radiologist read each study, interobserver variability could not be assessed. All data sheets were sent to the data coordinating center at the New York Presbyterian Hospital’s Cornell Campus for entry into the pulmonary CT angiography–indirect CT venography database.

Thrombi and emboli were defined as low-attenuating partial or complete intraluminal filling defects surrounded by a high-attenuating ring of enhanced blood that were seen on at least two consecutive transverse images. Streaking artifacts were distinguished from clots in several ways. Clots usually were seen on consecutive images, as opposed to streaking artifacts. In addition, streaking artifacts extended through the vessels and into the surrounding soft tissues. These usually could be identified by narrowing the window levels to enhance the contrast. In addition, the streaking artifacts had very straight borders, as opposed to clots, which were rounded. In the chest region, all pulmonary arteries were assessed down to the subsegmental branches. For the pelvis and lower extremities, the deep veins were assessed from the inferior vena cava to the popliteal veins.

The technical quality of the pulmonary CT angiographic–indirect CT venographic images was defined by the level of enhancement achieved in the pulmonary arteries and in the lower extremity veins. This enhancement was obtained by recording the attenuation level (in Hounsfield units) within circular or elliptic regions of interest placed over the main pulmonary artery and the common femoral vein. If an embolus in the pulmonary arteries or a thrombus in the pelvis or in the leg veins was present, it was assessed in a similar fashion. In cases in which two or more DVTs or pulmonary embolism clots were present in a given patient, the mean clot attenuation levels were recorded for that patient.

The same radiologist at each institution placed the regions of interest. Region-of-interest attenuation measurements for pulmonary CT angiography were obtained at the level of the main pulmonary arterial bifurcation and for indirect CT venography at the level of the greater trochanter. These levels were selected to minimize the partial volume effect on the measurements. The common femoral vein at the level of the greater trochanter not only is relatively large and is easier to assess but also represents the most distal and potentially least-enhanced venous blood in the lower extremities. When the attenuation levels of the vessels were being measured, careful attention was paid to not include any low-attenuating clots within the regions of interest. This prevented low-attenuating clots in the main pulmonary artery or in the common femoral vein from downgrading the measured technical quality of the examination.

The technical quality of each pulmonary CT angiographic–indirect CT venographic examination was also rated as excellent, good, fair, or poor, depending on the subjective appearance of specific regions of interest. For pulmonary CT angiography, this criterion correlated so closely with the actual attenuation levels of the main pulmonary artery that we chose to describe these categories on the basis of attenuation values. Although patient size and motion artifacts can affect image quality, these did not affect our ability to detect clots when the attenuation levels were adequate. However, artifacts did create difficulties when enhancement was poor. When the main pulmonary artery had an attenuation level greater than 200 HU, the technical quality of the examination was rated as "excellent"; a rating of 150–199 HU, "good"; 100–149 HU, "fair"; and less than 99 HU, "poor."

Indirect CT venography was rated as "excellent" when the attenuation of the common femoral vein was greater than that of the adjacent muscle and was equal to that of the common femoral artery. The study was rated as "good" when the common femoral venous enhancement was greater than the muscular enhancement but was lower than the common femoral arterial enhancement. The study was rated as "fair" when the common femoral venous enhancement was equal to the adjacent muscular enhancement and was less than the common femoral arterial enhancement. The study was rated as "poor" when the enhancement of the common femoral vein was less than that of the adjacent muscle and of the common femoral artery.

For all cases, the results of lower extremity venous US, V-P scanning, conventional pulmonary angiography, and conventional venography were recorded when imaging was performed within 7 days of pulmonary CT angiography–indirect CT venography. These additional studies were ordered as part of the routine clinical evaluation and were not performed or interpreted as part of a specific protocol. No guidelines were set in the protocol with regard to these additional examinations, so clinicians ordered them as necessary. Whenever the results of one examination disagreed with those of either pulmonary CT angiography or indirect CT venography, all examination results in that patient were reviewed, and the treatment was documented. This review did not change the initial interpretation that already had been recorded. All retrospective reviews of US images involved only the repeat assessment of the saved images.

The paired t test was performed to compare the attenuation levels of vessels and their respective thromboembolic clots. The pooled t test was performed to compare the attenuation levels of pulmonary embolic clots and deep venous thrombosis clots. A P value of .01 was considered to indicate a significant difference.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Quality of Pulmonary CT Angiography–Indirect CT Venography
The ratings of the technical quality of the 541 pulmonary CT angiographic–indirect CT venographic examinations are shown in Table 1. The quality of pulmonary CT angiography consistently was higher than that of indirect CT venography (Fig 1). Pulmonary CT angiography was rated as good to excellent in 514 (95%) cases, while indirect CT venography was rated as good to excellent in 414 (77%). Among the 514 patients with good to excellent pulmonary CT angiographic ratings, 401 (78%) also had good to excellent indirect CT venographic ratings.


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TABLE 1. Technical Quality of the Pulmonary CT Angiographic and Indirect CT Venographic Components of the Combined Examination
 


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Figure 1. Graph shows the technical quality rating of the pulmonary CT angiographic-indirect CT venographic components of the examination. Pulmonary CT angiographic images (white bars) were rated as excellent to good in 95% of cases, whereas CT venographic images (black bars) were rated as excellent to good in 77% of cases (n = 541).

 
Twelve patients had inconclusive indirect CT venographic findings, and none had inconclusive pulmonary CT angiographic findings. Inconclusive findings were defined as findings from which diagnoses could not be rendered confidently. Among all 12 patients with inconclusive indirect CT venographic findings, DVT clots were suggested in the superficial femoral vein in nine, in the common femoral vein in two, and in the popliteal vein in one. The inconclusive results were attributed to very poor venous enhancement in six (50%), to irregularly shaped partial filling defects or to streaking artifacts in five, and to a soft-tissue mass impinging on the vessel in one. Among these 12 patients with inconclusive findings, US was performed in only four. No DVT was seen in these four at US, although one of them had positive findings at both pulmonary CT angiography and V-P scanning. The findings in only 12 of the 34 patients with poor-quality indirect CT venographic images were considered inconclusive because venous enhancement in most cases was adequate enough for a diagnosis to be rendered confidently. Contrary to published literature (23,24) in which it is suggested that 5%–10% of pulmonary CT angiography will have inconclusive results, none of the pulmonary CT angiographic findings were reported as inconclusive. Only four pulmonary CT angiographic studies had main pulmonary arterial attenuation less than 100 HU. Although this places them in the category of poor-quality enhancement in accordance with our own criteria, the readers still considered them to be interpretable.

Attenuation Measurements from Regions of Interest
The mean attenuation of the main pulmonary artery was 280 HU (95% CI: 272, 287 HU; median, 270 HU), and the mean attenuation of the common femoral vein was 101 HU (95% CI: 99, 103 HU; median, 100 HU) (Fig 2).



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Figure 2. Graph shows the mean attenuation measurements in four regions of interest, which are accompanied by a 95% CI. MPA = main pulmonary artery, PE = pulmonary embolism, and CFV = common femoral vein.

 
Among the 541 patients, pulmonary embolism was detected in 91 (17%) patients, and DVT was detected in 45 (8%) patients. The pulmonary embolism clot had a mean attenuation of 49 HU (95% CI: 44, 54 HU; median, 48 HU), and the DVT clot had a mean attenuation of 51 HU (95% CI: 45, 57 HU; median, 55 HU). Among the patients with pulmonary embolism, the mean pulmonary embolism clot attenuation was significantly less than the mean main pulmonary arterial attenuation (49 vs 284 HU, respectively; paired t test, P < .001). Among patients with DVT, the mean clot attenuation of the deep venous system was also significantly lower than the mean attenuation of the central femoral vein (51 vs 109 HU, respectively; paired t test, P < .001). Among those who had pulmonary embolism and DVT, there was no significant difference between the mean attenuations of the pulmonary embolism and of the DVT clots (48 vs 51 HU, respectively; paired t test, P = .25). Among those who had either pulmonary embolism or DVT, there was no significant difference between the mean attenuations of the pulmonary embolism clots and of the DVT clots (49 vs 50 HU, respectively; pooled t test, P = .91).

Incremental Benefit of Pulmonary CT Angiography–Indirect CT Venography versus Pulmonary CT Angiography Alone
Twenty-nine (32%) of 91 patients with pulmonary embolism also had DVT. Likewise, 29 (64%) of 45 with DVT also had pulmonary embolism. Both pulmonary embolism and DVT were absent in 426 (79%) of 541 cases (Table 2).


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TABLE 2. Results of Pulmonary CT Angiography and Indirect CT Venography
 
The incremental benefit of adding indirect CT venography to a basic pulmonary CT angiographic protocol is shown in Table 2. While 91 patients had pulmonary embolism, an additional 16 had DVT without pulmonary embolism and were treated appropriately. This is an 18% increase in the percentage of positive cases, which requires changes in medical management as a result of indirect CT venography.

Comparative Studies
Among the 541 subjects, 182 underwent one or more studies within 7 days of pulmonary CT angiography–indirect CT venography: 116 underwent duplex US, 107 underwent V-P scanning, four underwent conventional pulmonary angiography, and none underwent conventional venography.

Of the 116 patients who underwent US in addition to pulmonary CT angiography–indirect CT venography (Table 3), 108 (93%) had concordant results, four (3%) had discordant results, and four (3%) had inconclusive CT venographic results. In all four patients with discordant results, DVT was seen at indirect CT venography when US findings were negative. Retrospective review of results in these four patients showed that, on one US image, a popliteal venous clot was present. The other three DVTs not identified at US were in the right common femoral vein in two cases and were in the right superficial femoral vein in one. US and indirect CT venography were performed on the same day in two of these four patients with discordant findings, and US preceded CT venography by 1 day in the other two patients. Indirect CT venographic images were rated as good to excellent in two of these three DVTs.


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TABLE 3. Number of Patients Who Received a Diagnosis of DVT
 
US did not depict any clots in the four patients with inconclusive indirect CT venographic findings. One of these four patients had high-probability V-P scanning and positive pulmonary CT angiographic results, while three had negative pulmonary CT angiographic results. One of these three with negative pulmonary CT angiographic results did not undergo V-P scanning, while two of these three had low-probability V-P scanning results. In 26 additional patients in whom DVT was diagnosed by using indirect CT venography, no concomitant US was performed. One patient who was not examined with US had a clot in only the inferior vena cava that would not have been expected to be positive at US. In addition, seven patients had pelvic clots that involved the iliac veins, all of which were accompanied by clots in the lower extremities. Only three of these seven patients were examined with US. In one of these three patients, US depicted a common iliac vein DVT, and in two of the three patients, the pelvic clot was not detected.

In 107 patients, both V-P scanning and pulmonary CT angiography-indirect CT venography were performed (Table 4). For the purposes of this study, the high-probability V-P scans in patients who thus required treatment were considered positive, and normal V-P scans in patients who did not require treatment were considered negative. All intermediate, indeterminate, and low-probability V-P scans also were considered negative, since they were not indications for anticoagulation and potentially required further evaluation. In 94 (88%) patients, the results of pulmonary CT angiography–indirect CT venography and of V-P scanning were concordant (12 positive, 82 negative); in 13 (12%), they were not. Among the 13 patients with discordant results, seven had negative pulmonary CT angiographic results, with high-probability V-P scans, while six had pulmonary embolism on pulmonary CT angiographic scans but had low- to indeterminate-probability V-P scans.


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TABLE 4. Comparison of Pulmonary CT Angiographic and V-P Scanning Findings
 
Retrospective review of the seven negative pulmonary CT angiographic results confirmed that no clot could be seen and that six of these seven were rated as excellent and one as poor. On the other hand, review of the seven high-probability V-P scans revealed that four actually were indeterminate, an additional one was misinterpreted because of a vascular malformation seen at conventional pulmonary angiography, and two were confirmed as high probability at review. Retrospective review of the six positive pulmonary CT angiographic findings revealed that one was actually negative, one was a motion-limited study, three had well-defined filling defects and remained discordant, and one was associated with a DVT (at US and indirect CT venography) that made the pulmonary CT angiographic finding more likely. Among the six non–high-probability V-P scans, three were indeterminate, three were low-probability, and none were normal at review. One of these three low-probability V-P scans was found to have a mismatched perfusion defect at review.

Only four of 541 patients underwent conventional pulmonary angiography. Three patients had both positive conventional pulmonary angiographic and positive pulmonary CT angiographic results, while the fourth had negative conventional pulmonary angiographic results and had negative pulmonary CT angiographic results.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In patients undergoing pulmonary CT angiography for the suspicion of pulmonary embolism, the addition of indirect CT venography provides considerable benefits. By adding only 3 minutes to the required scanning time for pulmonary CT angiography and by adding no additional contrast material, we could detect DVT with high concordance with the standard examination, US (Fig 3). In the 116 patients who underwent lower extremity venous Doppler US, there were no cases in which US findings were positive and indirect CT venographic findings were negative. The percentage of cases in which US findings were negative and indirect CT venographic findings were positive indicates an area for further research, but we speculate that these US images were false-negative on the basis of prior research with magnetic resonance imaging in patients with DVT (25). The retrospective reviews of discordant US results also were limited, as real-time data were not saved, which potentially concealed clots that may have been missed at the initial US reading. There also is the possibility of overinterpretation of the indirect CT venographic findings, which requires further blinded studies of indirect CT venography and US. The radiation dosage of the indirect CT venographic component of the examination is slightly less than that of a standard pelvic CT scan. In the future, we can potentially decrease this further by using higher-pitched sequences.



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Figure 3. Transverse CT section shows DVT in the left common femoral vein (arrow), which was detected at indirect CT venography.

 
We found that the addition of CT venography increased the diagnosis of thromboembolism by 18%, as DVT occurred in 16 patients who had no evidence of pulmonary embolism. This is an important benefit of combined pulmonary CT angiography-indirect CT venography, since other algorithms require additional examinations to evaluate the venous system, which may increase expense and may further delay diagnosis and treatment.

By using our standard protocol without additional contrast material injection, the attenuation of the common femoral vein was significantly higher than that of the DVT. This difference in enhancement between vessel and clot not only reflects the quality of the examination but also provides greater confidence in making the diagnosis. Although it is conceivable that some of the common femoral venous and DVT clot attenuation levels were indistinguishable and thus were excluded from measurement, no additional DVT was found in those 116 patients who also underwent US; therefore, such a scenario is unlikely.

The objective mean attenuation measurements and their corresponding 95% CIs, as shown in Figure 2, illustrate the degree of pulmonary arterial, deep pelvic, and lower extremity venous enhancement achieved by using the pulmonary CT angiographic-indirect CT venographic protocol. The common femoral vein and DVT clot attenuation levels were significantly different, which reflects the contrast material optimization inherent in the combined pulmonary CT angiographic–indirect CT venographic protocol.

Our mean DVT clot attenuation was 51 HU, with a median value of 55 HU. These results were similar to those reported in the literature (19), in which acute DVTs had clot attenuation levels averaging approximately 60 HU or greater. In addition, our attenuation measurements for pulmonary embolism and DVT clots were not significantly different. As the appearance of acute pulmonary embolism differs from that of chronic pulmonary embolism, and both pulmonary embolism and DVT were present in the same patients in 29 cases, with no appreciable difference in attenuation, we are confident that our attenuation measurements for DVT represent the correct values for acute DVT. This provides additional evidence that the combined protocol allows for the detection of acute DVT.

The attenuation difference between the opacified pulmonary arterial blood and the embolus was much greater than the difference between the opacified common femoral venous blood and the DVT clot. This was expected, since there is more dilution of contrast material during the latter portion of the protocol.

The frequency of DVT detected at indirect CT venography, in the absence of pulmonary embolism (by using either pulmonary CT angiography or V-P scanning), differs considerably from that reported in previously published studies (11,13,16,26). Among the 450 patients in our study with negative pulmonary CT angiographic findings, only 16 (4%) had positive indirect CT venographic findings. Similarly, among the 88 patients in our study who did not have a high-probability V-P scanning result, DVT was detected in six (7%). Although this proportion was much lower than the 25%–30% positive-for-DVT rate in similar groups of patients (11,13,16,26), it still is substantially higher than the rate of incidental DVT in the hospital-based population, which is estimated to be 1% (15 of 1,400 patients) (27). Among our patients with high-probability V-P scans (19 patients) or with positive pulmonary CT angiographic findings (91 patients), only seven (37%) and 29 (32%), respectively, had positive indirect CT venographic findings. These results are consistent with the reported frequency of DVT in patients with proved pulmonary embolism, which is 29%–43% (13,28).

Although this decreased prevalence of pulmonary embolism may be accounted for by differences in the inclusion criteria of other studies, we have additional evidence that our population of patients who underwent pulmonary CT angiography-indirect CT venography had a lower prevalence of pulmonary embolism than the total population of patients suspected to have pulmonary embolism. In previous studies (29,30) at the New York Presbyterian Hospital’s Cornell Campus, the overall prevalence of pulmonary embolism was found to be 33% compared with our current finding of 17%. The patient population in the current study was not composed of all patients admitted for the suspicion of pulmonary embolism; rather, it included only patients referred for pulmonary CT angiography-indirect CT venography because of a suspicion of pulmonary embolism. This makes it particularly difficult to characterize the study population in comparison with the overall population suspected to have pulmonary embolism.

At the New York Presbyterian Hospital’s Cornell Campus, the number of V-P examinations ordered is approximately double that of the pulmonary CT angiographic–indirect CT venographic examinations ordered each month. Therefore, as a result of selection bias, a majority of patients suspected of having pulmonary embolism were not included in our study population. Depending on each clinician’s rationale for ordering pulmonary CT angiography–indirect CT venography versus V-P scanning, the apparent incidence of DVT could vary. In those patients in whom V-P scanning is performed as the initial study, conclusive results such as high probability or normal generally would have a greater influence on the decision to forego additional studies, as opposed to low-probability or indeterminate results, which usually warrant further evaluation. This may partially account for the lower incidence of DVT in our patients suspected to have pulmonary embolism.

Among our 541 patients suspected to have pulmonary embolism, only seven (1%) had pelvic venous DVTs, and all seven of these patients had additional DVTs in the lower extremities. Only one case involved the inferior vena cava alone and would not have been identified at US. There was a relatively low prevalence of pelvic involvement in our population; it has been reported that the pelvic veins are involved in 15 (7%) of 226 patients suspected to have pulmonary embolism and in 15 (11%) of 137 patients with pulmonary embolism (31). However, these seven patients with pelvic DVT involvement composed 16% of the 45 total patients with positive CT venographic findings. This is consistent with the reported incidence of pelvic DVT, which is estimated at 11%–30%, among patients with objective evidence of DVT (32,33). This suggests that our low prevalence less likely was due to an inability to detect pelvic clots. Our low prevalence can be explained by only a difference in our patient population. We have already addressed the potential for selection bias. With regard to the possibility that pelvic clots were missed, we found that pelvic veins were more difficult to evaluate compared with leg veins. This was due primarily to the pelvic veins’ oblique course relative to the plane of scanning. This, in conjunction with the 10-mm CT section thickness, made the evaluation of these vessels more difficult relative to the leg veins, which generally run perpendicular to the plane of section. In the future, we may consider a lesser section thickness for the pelvic evaluation.

Conventional venography is the traditional standard of reference for detecting DVT, but its invasive nature and high rate of adverse reactions have made it unacceptable for routine use. Because of its safety and speed, US has become the most commonly used diagnostic tool for the detection of DVT and has been shown to have a sensitivity and specificity of up to 97% and 97% (34), respectively. Because of the complete absence of conventional venographic studies, it was only practical for us to compare our indirect CT venographic results with those of US. Likewise, conventional pulmonary angiography was performed in only four of 541 cases. While all four conventional pulmonary angiographic results were concordant with the pulmonary CT angiographic results, these findings are limited by the small number of conventional pulmonary angiograms. However, the substantial agreement rate between patients who underwent CT venography and those who also underwent US suggests that combined pulmonary CT angiography–indirect CT venography at least has a sensitivity and specificity similar to those of the more generally used algorithms, which include US. This requires confirmation and further research.

The technical quality of pulmonary CT angiography was rated as good to excellent in 95% of patients. Among this group of patients with good to excellent pulmonary CT angiographic ratings, 78% also had good to excellent indirect CT venographic ratings. Thus, it is possible to obtain a technically high-quality venous finding in the majority of patients with only a single examination. Those patients who had fair to poor pulmonary CT angiographic findings (27 patients [5%]) also had a high rate of fair to poor indirect CT venographic evaluations (14 patients [52%]).

During the past several years, the use of CT for the evaluation of pulmonary embolism has increased, with pulmonary CT angiography becoming the initial diagnostic examination performed at an increasing number of institutions (35). This pattern can be expected to continue with further improvements in CT technology. It will be easier to obtain thinner CT sections and in less time with newer multiple–detector row CT scanners. This should lead to further quality improvement in the findings. Thus, there is an even greater incentive to maximize all available diagnostic information that can be obtained during this examination, which includes the evaluation of the venous system.


    FOOTNOTES
 
Abbreviations: DVT = deep venous thrombosis, V-P = ventilation-perfusion

Author contributions: Guarantors of integrity of entire study, D.F.Y., M.D.C., C.I.H. Guarantors of integrity of entire study, D.F.Y., M.D.C., C.I.H.; study concepts, D.F.Y.; study design, D.F.Y., H.D.S., A.A.S.; definition of intellectual content, D.F.Y., M.D.C., C.I.H.; literature research, M.D.C., D.F.Y., C.I.H., A.A.S.; clinical studies, D.F.Y., M.D.C., L.S., D.S., A.L., J.R., G.P., J.C., A.A.S., H.D.S., W.W., P.M.P., M.G., R.A.C.; data acquisition, M.D.C., D.F.Y., A.A.S., D.S., L.S., A.L., P.M.P., J.R., M.G., G.P., J.C., R.A.C.; data analysis, M.D.C., D.F.Y., C.I.H.; statistical analysis, C.I.H., M.D.C., D.F.Y.; manuscript preparation, M.D.C., D.F.Y., C.I.H.; manuscript editing, M.D.C., D.F.Y., C.I.H., H.D.S., D.S., J.R.; manuscript review, all authors.

Members of the Pulmonary CT Angiography-CT Venography Cooperative Group: Matthew D. Cham, MD, David F. Yankelevitz, MD, Dorith Shaham, MD, Ami A. Shah, MD, Leonard Sherman, MD, Andrew Lewis, MD, Jurgen Rademaker, MD, Gregory Pearson, MD, Junsung Choi, MD, William Wolff, MD, Pilar M. Prabhu, MD, Michael Galanski, MD, Robert A. Clark, MD, H. Dirk Sostman, MD, and Claudia I. Henschke, MD.

Funding/Support: This cooperative study was sponsored by the Society of Thoracic Radiology. C.I.H. was supported by the Health Policy and Technology Assessment Division.


    REFERENCES
 TOP
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 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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