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Deep Venous Thrombosis with Suspected Pulmonary Embolism: Detection with Combined CT Venography and Pulmonary Angiography¹

¹ From the Department of Radiology, Roswell Park Cancer Institute, Elm and Carlton Sts, Buffalo, NY 14263 (P.A.L., D.L.K., Z.D.G.), and the Department of Radiology, Winthrop University Hospital, Mineola, NY (D.S.K., D.A.B.). From the 1999 RSNA scientific assembly. Received July 7, 2000; revision requested August 19; revision received October 4; accepted October 11. Address correspondence to P.A.L. (e-mail: peter.loud@roswellpark.org).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: To determine the frequency and location of deep venous thrombosis at computed tomographic (CT) venography after CT pulmonary angiography in a large series of patients clinically suspected of having pulmonary embolism and to compare the accuracy of CT venography with lower-extremity venous sonography.

MATERIALS AND METHODS: Venous phase images were acquired from the diaphragm to the upper calves after completion of CT pulmonary angiography in 650 patients (373 women, 277 men; age range, 18–99 years; mean age, 63 years) to determine the presence and location of deep venous thrombosis. Results of CT venography were compared with those of bilateral lower-extremity venous sonography in 308 patients.

RESULTS: A total of 116 patients had pulmonary embolism and/or deep venous thrombosis, including 27 patients with pulmonary embolism alone, 31 patients with deep venous thrombosis alone, and 58 patients with both. Among 89 patients with deep venous thrombosis, thrombosis was bilateral in 26, involved the abdominal or pelvic veins in 11, and was isolated to the abdominal or pelvic veins in four. In patients in whom sonographic correlation was available, CT venography had a sensitivity of 97% and a specificity of 100% for femoropopliteal deep venous thrombosis.

CONCLUSION: Combined CT venography and pulmonary angiography can accurately depict the femoropopliteal deep veins, permitting concurrent testing for venous thrombosis and pulmonary embolism. CT venography also defines pelvic or abdominal thrombus, which was seen in 17% of patients with deep venous thrombosis.

Index terms: Computed tomography (CT), angiography, 9*.12914², 9*.12915, 9*.12916 • Embolism, pulmonary, 60.72 • Pulmonary angiography, 944.12914, 944.12915, 944.12916 • Veins, thrombosis, 9*.751, 9*.12914

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Pulmonary thromboembolism is a feared complication of deep venous thrombosis (DVT). The mortality rate in untreated cases is 25%–30%, whereas the mortality rate in treated cases decreases to 5%–8% (1). More than 90% of pulmonary emboli arise from deep veins of the legs and pelvis, and the primary risk factor for recurrent pulmonary embolism is the presence of residual proximal venous thrombosis (2,3).

Unfortunately, both pulmonary embolism and DVT are conditions that are notoriously difficult to diagnose clinically. Diagnostic algorithms for the evaluation of suspected thromboembolism have traditionally included ventilation-perfusion lung scanning and conventional pulmonary angiography to evaluate the lungs and lower-extremity sonography to evaluate the leg veins, but they have recently evolved to include computed tomography (CT) (4). CT pulmonary angiography is increasingly being used to evaluate suspected pulmonary embolism because it accurately defines emboli to the level of segmental pulmonary arteries and reveals other nonembolic causes of thoracic symptoms (5–7).

Because pulmonary embolism and venous thrombosis are different aspects of the same disease, a single study that accurately defines both processes would be a valuable addition to the diagnostic regimen. Combined CT venography and pulmonary angiography was reported in 1998 (8). This test, which consists of helical CT pulmonary angiography followed by venous phase CT performed from the diaphragm to the calves, allows concurrent evaluation of pulmonary embolism and DVT. This technique uses the venous enhancement that follows rapid peripheral venous infusion of iodinated contrast medium for helical CT pulmonary angiography and therefore requires no additional contrast medium to image the deep veins. Findings of several subsequent studies (9–11) in which CT venography was compared with lower-extremity sonography have indicated that it is accurate for the evaluation of femoropopliteal DVT.

The purpose of this study was to determine the frequency and location of DVT with combined CT venography and pulmonary angiography in 650 consecutive patients referred for evaluation of suspected pulmonary embolism. In a subset of 308 patients, we compared the results with those of lower-extremity venous sonography.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Between September 1997 and April 2000, 650 consecutive patients suspected of having pulmonary embolism (373 women, 277 men; age range, 18–99 years; mean age, 63 years) underwent CT venography and pulmonary angiography. The two participating institutions were Winthrop University Hospital, Mineola, NY, and Roswell Park Cancer Institute, Buffalo, NY, which contributed 509 and 141 cases, respectively. The patient population included 71 patients from an earlier preliminary study (10). Other patients were excluded during that period due to contraindications to contrast medium administration, such as allergy or renal insufficiency, and unavailable venous access.

Slightly different protocols were used at the two participating hospitals. Either 120 mL of iohexol 350 (Omnipaque; Nycomed Amersham, Princeton, NJ) was administered at a rate of 3 mL/sec or 150 mL of iohexol 240 (Omnipaque; Nycomed Amersham) was administered at a rate of 3–5 mL/sec through an intravenous catheter in the arm. To evaluate the pulmonary arteries, a scanner (HiSpeed Advantage; GE Medical Systems, Milwaukee, Wis) was used to generate images with a section thickness of 3–5 mm and a pitch of 1.8 or 2.0 from the diaphragm to the aortic arch during a single breath hold, beginning 20–25 seconds after the start of contrast medium infusion. At both hospitals, transverse venous images, 5–10 mm thick, were acquired at 5-cm intervals during approximately 40 seconds from the diaphragm to the upper calves. At one hospital, the venous study began 3 minutes after the start of contrast material infusion and included images acquired from the upper calves up to the diaphragm. At the other, the venous study began 3 minutes after contrast material administration and included images acquired from the diaphragm to the upper calves. Both protocols, therefore, were used to image the femoropopliteal veins between 3 and 4 minutes after the administration of contrast material. A total of 18–20 venous images were typically obtained.

All CT scans were evaluated for DVT by one of three radiologists (P.A.L., D.S.K., D.L.K.) blinded to the results of any previous venous imaging. All radiologists were fellowship trained in body imaging and had an additional 4–8 years in practice. Criteria for a diagnosis of DVT were an intraluminal filling defect or localized nonopacification of a venous segment. The location of DVT was recorded in all patients. In 85 patients, pulmonary embolism was diagnosed at helical CT pulmonary angiography.

The results of all patients undergoing bilateral lower-extremity venous sonography within 24 hours before or after CT examination were reviewed. Sonography was performed as part of the patient’s clinical evaluation and involved the use of a standard compression and Doppler technique from the popliteal trifurcation to the inguinal level, which included the popliteal vein and the superficial, deep, and common femoral veins (12). Sonographic findings were considered positive if thrombus prevented complete collapse of the vein during manual compression and caused a lack of flow at Doppler examination. The reported results of sonography were reviewed independently by one of two authors (P.A.L., D.S.K.), and findings were compared with CT venographic results. In four cases in which CT venography revealed femoropopliteal DVT and initial sonographic findings were negative, a repeat sonographic examination was performed at the clinician’s request, with particular attention to the area of concern at CT. In all other cases, sonographers were blinded to CT venographic results.

Sensitivity, specificity, and positive and negative predictive values from CT venography, compared with lower-extremity venous sonography, were calculated. Cases with CT-depicted DVT isolated to the calf veins, iliac veins, and vena cava were excluded from these calculations, as sonography of these areas was not routinely performed.

	RESULTS

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Among 650 patients examined, 534 (82%) showed no evidence of pulmonary embolism or DVT. Among 116 (18%) with positive CT scans—that is, those with evidence of pulmonary embolism and/or DVT—58 had both pulmonary embolism and DVT (Fig 1), 27 had pulmonary embolism without DVT, and 31 had DVT without pulmonary embolism (Fig 2).

View larger version (75K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. Transverse contrast-enhanced CT venogram and pulmonary angiogram in a 71-year-old man with pulmonary embolism and DVT. (a) CT scan obtained at the level of the lower chest shows an embolus in a right lower-lobe pulmonary artery (arrow). (b) Venous phase CT scan obtained at the level of the knee shows DVT as a nonenhancing filling defect that expands the left popliteal vein (arrow). (c) CT scan obtained at the inguinal level shows thrombus in the left common femoral vein (arrow).

View larger version (65K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. Transverse contrast-enhanced CT venogram and pulmonary angiogram in a 71-year-old man with pulmonary embolism and DVT. (a) CT scan obtained at the level of the lower chest shows an embolus in a right lower-lobe pulmonary artery (arrow). (b) Venous phase CT scan obtained at the level of the knee shows DVT as a nonenhancing filling defect that expands the left popliteal vein (arrow). (c) CT scan obtained at the inguinal level shows thrombus in the left common femoral vein (arrow).

View larger version (111K): [in this window] [in a new window] [Download PPT slide]   Figure 1c. Transverse contrast-enhanced CT venogram and pulmonary angiogram in a 71-year-old man with pulmonary embolism and DVT. (a) CT scan obtained at the level of the lower chest shows an embolus in a right lower-lobe pulmonary artery (arrow). (b) Venous phase CT scan obtained at the level of the knee shows DVT as a nonenhancing filling defect that expands the left popliteal vein (arrow). (c) CT scan obtained at the inguinal level shows thrombus in the left common femoral vein (arrow).

View larger version (82K): [in this window] [in a new window] [Download PPT slide]   Figure 2. Transverse CT scan obtained at the midthigh level in a 68-year-old woman with DVT shows a nonenhancing thrombus in the duplicated left superficial femoral veins (arrows). CT pulmonary angiography failed to show pulmonary embolism.

View larger version (87K): [in this window] [in a new window] [Download PPT slide]   Figure 3a. Transverse CT scans in a 62-year-old woman with DVT extending to the inferior vena cava. CT pulmonary angiography failed to show pulmonary embolism. (a) Upper pelvic image shows thrombus in the right common iliac vein (arrow). (b) Lower abdominal image shows thrombus in the inferior vena cava (arrow).

View larger version (86K): [in this window] [in a new window] [Download PPT slide]   Figure 3b. Transverse CT scans in a 62-year-old woman with DVT extending to the inferior vena cava. CT pulmonary angiography failed to show pulmonary embolism. (a) Upper pelvic image shows thrombus in the right common iliac vein (arrow). (b) Lower abdominal image shows thrombus in the inferior vena cava (arrow).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
One of the criticisms of helical CT pulmonary angiography as a screening test for pulmonary thromboembolism is that emboli in small subsegmental pulmonary arterial branches may be missed, leading to inadequate treatment in patients at risk for larger, potentially fatal recurrent emboli, namely, patients with DVT. Therefore, lower-extremity venous sonography has been advocated for use in patients with leg symptoms suggestive of DVT or in those with a negative or equivocal finding at helical CT pulmonary angiography (13). If the accuracy of combined CT venography and pulmonary angiography for the detection of DVT is similar to that of sonography, its use could potentially eliminate the need for separate venous imaging in many patients, and it could expedite the diagnostic work-up of thromboembolism.

The frequency and location of DVT revealed with combined CT venography and pulmonary angiography in this study are similar to those previously reported (14) with the use of conventional venography in patients with pulmonary embolism. Analysis of data in 89 patients with DVT showed the upper location of thrombosis to reach the calf or popliteal vein in 25 (28%), the superficial femoral vein in 18 (20%), the common femoral vein in 31 (35%), and the iliac veins or vena cava in 15 (17%). While most DVT propagate craniad from the calf, we found a number of isolated thrombi in the femoral veins, the pelvis, and the abdomen. These may represent fragments of previously larger clots, as most of these patients had pulmonary embolism.

In 31 (5%) of 650 patients examined, DVT was detected with no evidence of pulmonary embolism. This increased the number of positive scans by 36% (from 85 to 116). It is possible that subsegmental pulmonary emboli were undetected in some of these patients at CT. However, because the treatment of both DVT and pulmonary embolism includes anticoagulation, one could reasonably argue that missed subsegmental emboli, in the presence of anticoagulation therapy for DVT, are of little consequence.

In this study, the sensitivity and specificity of CT venography, compared with bilateral venous sonography, were 97% and 100% for femoropopliteal DVT detection, respectively. Two false-negative CT venograms were related to short areas of superficial and common femoral vein clot that were likely missed due to the 5-cm section interval used for DVT screening. Both of the patients with these findings had pulmonary embolism. Such small clot fragments could presumably be detected by decreasing the section interval to 2–3 cm.

Our use of a 5-cm interval between venous images is based on the fact that small isolated thrombi are unusual (15) and that even limited sonographic surveys that include only the popliteal and common femoral veins depict the great majority of venous thrombi (16). Some researchers (11) obtain contiguous CT venous phase images without a section interval. Given the high sensitivity and specificity that we have shown by using a 5-cm interval between venous images, the elimination of the section interval entirely would lead to only a minimal increase in sensitivity for DVT despite a substantial increase in radiation dose, number of images, and cost.

We acquire CT venous phase images 3–4 minutes after the initiation of contrast medium infusion into an arm vein. This delay allows venous blood to mix uniformly with contrast medium and return from the lower leg. Mean femoral venous attenuations of 94–112 HU have been reported (9,17,18) after the administration of standard contrast medium doses at CT pulmonary angiography. Studies of femoral vein attenuation after helical CT pulmonary angiography show a gradual decline after peak enhancement (17). Although peak venous enhancement may occur 2–3 minutes after the administration of contrast material in most patients, waiting 3–4 minutes allows for uniform enhancement in all patients, including those with slower circulation times. The principle underlying our slightly longer delay, therefore, is to achieve a diagnostic image in virtually all patients, rather than an aesthetically superior image in most patients and a nondiagnostic image in the remainder.

Unlike sonography, CT venography consistently depicts the large pelvic and abdominal veins, which harbored clots in 15 (17%) of 89 patients in whom DVT was seen at CT. Moreover, in three (4%) of 85 patients with pulmonary embolism, DVT was confined to the iliac veins or inferior vena cava, with no evidence of distal DVT. The detection of thrombi in the large pelvic or abdominal veins is important for prognostication in terms of future pulmonary embolism and severity of postphlebitic symptoms (19). CT venography also provides the radiologist with a useful road map for planning interventional procedures, such as vena caval filter placement or thrombolysis.

One limitation of this study is the lack of sonographic correlation in the majority of patients. The patients that did undergo sonography had a higher prevalence of DVT. Although we did not evaluate the symptoms for which the patients were referred or predisposition to DVT, it is likely that a higher percentage of patients in this group had lower-extremity symptoms or increased risk factors for DVT. Another limitation of our study is the lack of confirmation of most cases of DVT depicted at CT venography in the veins of the upper calf, pelvis, and abdomen with findings from another imaging test. Comparison of CT venography with conventional venography with the use of bilateral pedal venous injection, the accepted standard for the evaluation of lower-extremity and iliac DVT, would provide more complete confirmation of CT venographic results but would require additional venipunctures and contrast medium administration. As with sonography, differentiation of acute and chronic DVT can be difficult with CT venography. Further research is needed to determine if certain CT features of DVT can be used to reliably predict the age of thrombus.

In 85 patients with pulmonary embolism, DVT was depicted at CT venography in 56 (66%). In previously published findings of patients with pulmonary embolism, DVT was found in 71%–83% of patients with conventional bilateral leg venography (14,20) and in 38%–49% of patients with bilateral leg sonography (21,22). This suggests that the overall DVT detection rate with CT venography in our patient population more closely approximates that of conventional venography than that of sonography, possibly due to detection of additional DVT in the veins of the calf, pelvis, or abdomen.

In summary, while helical CT pulmonary angiography addresses pulmonary embolism and other nonembolic disease in the chest, the addition of venous phase imaging of the legs, pelvis, and abdomen allows concurrent, accurate evaluation for underlying femoropopliteal venous thrombus—the major risk factor for subsequent embolism. Furthermore, CT venography depicts pelvic and abdominal thrombi and thus provides an important advantage over lower-extremity sonographic screening for DVT.

	FOOTNOTES

 
² 9*. Vascular system, location unspecified.

Abbreviation: DVT = deep venous thrombosis

Author contributions: Guarantors of integrity of entire study, P.A.L., D.S.K.; study concepts, P.A.L.; study design, P.A.L., D.S.K.; literature research, P.A.L.; clinical studies, P.A.L., D.S.K.; data acquisition and analysis/interpretation, P.A.L., D.S.K.; statistical analysis, P.A.L.; manuscript preparation and definition of intellectual content, P.A.L.; manuscript editing and revision/review, all authors; manuscript final version approval, P.A.L., D.S.K.

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				J. P. Kanne and T. A. Lalani Role of Computed Tomography and Magnetic Resonance Imaging for Deep Venous Thrombosis and Pulmonary Embolism Circulation, March 30, 2004; 109(12_suppl_1): I-15 - I-21. [Abstract] [Full Text]

				R. J. Lipchik, L. R. Goodman, A. Perrier, M. Nendaz, F. Sarasin, H. Bounameaux, and N. Howarth Cost-effectiveness of Computed Tomography in Diagnosis of Pulmonary Embolism Am. J. Respir. Crit. Care Med., January 1, 2004; 169(1): 129 - 130. [Full Text] [PDF]

				S. C. Cramer, G. Rordorf, J. H. Maki, L. A. Kramer, J. C. Grotta, W. S. Burgin, J. A. Hinchey, C. Benesch, K. L. Furie, H. L. Lutsep, et al. Increased Pelvic Vein Thrombi in Cryptogenic Stroke: Results of the Paradoxical Emboli From Large Veins in Ischemic Stroke (PELVIS) Study Stroke, January 1, 2004; 35(1): 46 - 50. [Abstract] [Full Text] [PDF]

				D. Han, K. S. Lee, T. Franquet, N. L. Muller, T. S. Kim, H. Kim, O J. Kwon, and H. S. Byun Thrombotic and Nonthrombotic Pulmonary Arterial Embolism: Spectrum of Imaging Findings RadioGraphics, November 1, 2003; 23(6): 1521 - 1539. [Abstract] [Full Text] [PDF]

				British Thoracic Society guidelines for the management of suspected acute pulmonary embolism Thorax, June 1, 2003; 58(6): 470 - 483. [Full Text] [PDF]

				M. J.L. van Strijen, W. de Monye, J. Schiereck, G. J. Kieft, M. H. Prins, M. V. Huisman, P. M.T. Pattynama, and for the Advances in New Technologies Evaluating th Single-Detector Helical Computed Tomography as the Primary Diagnostic Test in Suspected Pulmonary Embolism: A Multicenter Clinical Management Study of 510 Patients Ann Intern Med, February 18, 2003; 138(4): 307 - 314. [Abstract] [Full Text] [PDF]

				M. S. Ginsberg, J. Oh, A. Welber, and D. M. Panicek Clinical Usefulness of Imaging Performed After CT Angiography That Was Negative for Pulmonary Embolus in a High-Risk Oncologic Population Am. J. Roentgenol., November 1, 2002; 179(5): 1205 - 1208. [Abstract] [Full Text] [PDF]

				D. S. Katz, P. A. Loud, D. Bruce, A. M. Gittleman, R. Mueller, D. L. Klippenstein, and Z. D. Grossman Combined CT Venography and Pulmonary Angiography: A Comprehensive Review RadioGraphics, October 1, 2002; 22(90001): S3 - 19. [Abstract] [Full Text] [PDF]

				J. R. Mayo, L. H. Ketai, P. A. Loud, Z. D. Grossman, D. S. Katz, and A. M. Gittleman Invited Commentary * Authors' Response RadioGraphics, October 1, 2002; 22(90001): S20 - 24. [Full Text] [PDF]

				C.J. Herold Spiral computed tomography of pulmonary embolism Eur. Respir. J., February 1, 2002; 19(35_suppl): 13S - 21s. [Abstract] [Full Text] [PDF]