Real-Time Ultrasound in the Diagnosis of Acute Deep Venous Thrombosis of the Lower Extremity
Wolfgang Habscheid, M.D. Margarethe Höhmann, M.D. Thomas Wilhelm, M.D. and Johannes Epping, M.D.
WÜRZBURG,
WEST GERMANY
Abstract One hundred twenty-six patients with clinically suspected acute deep venous thrombosis of the lower extremity (DVT) were examined comparatively with ultrasound and venography. In total, 174 lower extremity venograms were obtained. Ultrasonic examinations were performed on patients in the supine position. The venous segments were evaluated almost exclusively with transversal scanning. In the thigh, the only criterion for DVT was the reduced or absent compressibility of the venous lumen when gently compressed with the transducer. In the calf, normal unobstructed veins can usually not be viewed in the supine patient, whereas thrombotic veins appear as sonolucent, incompressible channels. Eight-three of the 174 lower extremity venograms were positive for DVT. In the majority of cases (53 of 83) the thrombotic process had involved two or more segments in combination. The sites of involvement of the different venous segments were distributed as follows: 24 occlusions of the common femoral vein, 52 of the superficial femoral vein, 56 of the popliteal vein, and 71 of the calf veins. Ultrasound had a sensitivity of 100% for thrombosis of the common femoral vein, 96% for the superficial femoral veins, 98% for the popliteal vein, and 93% for the calf veins. For the entire lower extremity, in regard to the diagnosis of thrombosis, the overall sensitivity was 95%. In 90% the extension of the occlusion was foreseen correctly. In no cases were false-positive results reported. Thus the overall specificity was 100%. The authors conclude that real-time ultrasound is a highly accurate method method for the diagnosis of DVT of the lower extremity. It is the only
indirect
From the
Department of Medicine
and
Radiology
of the
University
of
Würzburg, Würzburg,
599
Downloaded from ang.sagepub.com at University of British Columbia Library on June 25, 2015
West
Germany
600
capable of evaluating the venous system of the thigh, as well as that of the calf, with high accuracy. It should be the first choice of diagnostic imaging method in the diagnosis of deep venous thrombosis of the lower extremity. Introduction
x
The clinical diagnosis of deep venous thrombosis (DVT) of the lower extremity is known to be difficult and is accurate in only about 50% of the cases.’’2 Contrast venography is generally accepted as the gold standard for the diagnosis of DVT.’ It is, however, invasive, and a number of untoward responses after the administration of intravenous contrast material must be considered: 4-7 systemic anaphylactic reactions, local irritation, initiation of thrombophlebitis or even thrombosis, and aggravation of chronic renal or cardiac failure. Furthermore, the need for specialized equipment should not be underestimated. Therefore, numerous attempts have been made to develop other &dquo;indirect&dquo; noninvasive diagnostic procedures; Doppler ultrasound8’9 and plethysmographylO-12 have been found to be accurate in the evaluation of the thigh vein system, whereas the 1251-labeled fibrinogen test is sensitive to thrombus formation in calf veins. 1,11,14 Nonetheless, a noninvasive method of evaluating the venous system of the entire lower extremity that is easily performed and can be used prior to venography has not yet been established. Such a method would be beneficial, since the disease is often clinically oligosymptomatic. It is well known that thrombotic veins have a characteristic ultrasonic appearance and that there are several diagnosis patterns: they are not compressible’9’22 and usually show a typical intraluminous echo pattern, which cannot, however, always be demonstrated Further characteristic signs are the absence of vasodilatation during the Valsalva maneuver 16 and the widening of venous segments that lie distal to the occlusion.&dquo; Systemic investigations of the value of ultrasound in the diagnosis of DVT are rare and are limited mostly to the evaluation of the femoral vein or the popliteal vein. 16-24,39.40 Studies concerning calf vein thrombosis are missing completely. For this reason, we have completed a study involving a major patient population that examined the potential of ultrasound as a diagnostic imaging technique in suspected acute DVT in the thigh region, as well as in the calf. Patients and Methods
study was performed in 126 patients with clinically suspected acute DVT of the lower extremity. They ranged from seventeen to eighty-four years of age with a mean of 60.2 years. All patients underwent ultrasonic examination of both lower extremities. On the same day, venography of the symptomatic lower extremity was performed. If pulmonary embolism was suspected, bilateral lower extremity venograms were performed. In total, 174 venograms of one lower extremity were obtained. The ultrasonic and the venographic findings were interpreted by independent observers. Finally, the results were compared with one another. Discrepancies between the findings were not reinterpreted retrospectively. Contrast venography was carried out according the method of Rabinov and Paulin,3 except that ankle tourniquets were used to obtain optimal contrast filling of the deep veins. The criterion for acute DVT was the presence of an intraluminal filling defect, confirmed in two The
Downloaded from ang.sagepub.com at University of British Columbia Library on June 25, 2015
601
projections, or repeated nonfilling of a venous segment after different injections of Ultrasonography was performed using a common-type real-time scanner. The patient was examined in the supine position. The thigh was examined by ventral approach, moving the transversally applied transducer continuously from the inguinal region to the knee. For the evaluation of the popliteal vein and the calf veins (tibialis posterior and peroneal veins), the knee was flexed and transverse scans were obtained by posterior approach. A patent venous lumen can be compressed completely by the transducer (Fig. 1). The criterion for venous thrombosis was the markedly reduced or absent obturation of the venous lumen by gentle probe compression (Fig. 2). If present, an intraluminous echo pattern was registered but was not interpreted as thrombosis if the reaction to compression had been normal. The evaluation was performed mainly by transversal scanning. The examination along the longitudinal vascular axis is difficult since the transducer frequently deviates laterally during the compression maneuver. By moving the transducer continuously from the inguinal region to the knee, the common femoral vein is viewed medial to the artery. In the higher part of its course, the different
contrast material.
FIG. 1. Transverse scan of the normal common femoral vein. (left) Without probe compression. B. With probe compression. Note the complete obturation of the patent venous lumen in B. (right) AFC common femoral artery. VFC common femoral vein. =
=
FIG. 2. (left) Transverse scan of the superficial femoral vein with probe compression in the middle of the thigh; the occluded vein has the same echopattem as the patent artery but is not compressible. AFS superficial femoral artery, VFS superficial femoral vein. (right) Occlusion of the popliteal vein; the vein is widened and filled with an incompressible echogenic clot. AP = popliteal artery, VP popliteal vein. =
=
Downloaded from ang.sagepub.com at University of British Columbia Library on June 25, 2015
=
602
superficial femoral vein lies behind the artery, and in its lower part it lies external to the artery. In the popliteal space, the posterior approach shows the popliteal vein, which lies superficial to the artery. A sweep of the transducer in the cranial direction provides the view and the compression of the vessels in the adductor canal. Distally the junction of the calf veins forming the popliteal vein can frequently be seen. Patent calf veins can usually not be viewed in the supine patient. In thombosis, however, they become visible and appear as incompressible channels, which in cross-section scans look like worm-shaped, crosscut structures that continuously run through the ultrasonic image when the probe is moved (Fig. 3). The posterior tibial veins and the peroneal veins, when thrombotic, can be localized between the muscles near the tibia and fibula. They are examined by a dorsal approach. Occluded anterior tibial veins lie further beyond the assumed interosseus membrane between the tibia and the fibula. They can be viewed and submitted to compression by the peroneal region.
FIG. 3. (left) Contrast venography of the calf; the lack of visualization of the posterior femoral veins is suspicious of thrombosis. (right) Sonography proves the clots by showing two noncompressible echopoor venous segments.
Results
Among the 174 venograms of one lower extremity, which were performed in 126 patients, 83 were positive for deep venous thrombosis. The distribution regarding the site of the different venous groups is shown in Table I. In the majority of the cases (53 of 83) two or more segments were involved in combination. Isolated occlusions were found in the remain30 cases, the majority of which were calf vein thrombosis in 23 patients. The common ing femoral vein was involved in 24, the superficial femoral vein in 52, the popliteal vein in 56, and the calf veins in 71 cases. The difference between the total number of thromboses and the sum of occluded venous segments was due to the fact that at least two segments were mostly venous
involved. With venography as the diagnostic reference method, the accuracy of the sonographic findings compared with that of the venographic findings is shown in Table II. For the calf veins the sensitivity of ultrasound was 93 % overall and 87 % for patients with isolated calf involvement. Regarding the different venous segments of the thigh, the involvement of the common
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603 Distribution
of the
Venographically Identified
TABLE I Occlusions Regarding the
Different
Venous
Segments (n = 83)
femoral vein was correctly seen in all (sensitivity 100%), and occlusion of the superficial femoral vein was missed in 2 patients (sensitivity 96 % ) and of the popliteal vein in 1 patient
(sensitivity 98 % ) . Regarding the false-negative results 1 of the 2 missed superficial femoral vein occlusions was a small thrombus of 2 cm length near the adductor channel and 1 was an easily seen ascending thrombosis whose upper end was not correctly realized. One thrombosis of the popliteal vein originating from calf vein thrombosis was overlooked, whereas the calf involvement could be demonstrated by ultrasound. Of the 5 false-negative results concerning calf vein thrombosis, 3 were isolated to the calf. In the remaining 2, additional occlusions of upper venous
segments were viewed correctly. In these cases the lack of visibility of the calf involve-
by ultrasound could be due to long-standing organization of the thrombus.
Two of the 3 isolated calf vein occlusions were confined to one venous and overlooked had a thromgroup bus diameter of only approximately 3 mm. One was missed because of an atypically sonolucent echopattem of the muscle. Thus only 4 of the 83 thromboses were missed completely by ultrasound, and 3 of them were confined to the calf region. The overall sensitivity concerning the diagnosis of thrombosis was 95 % . In 90 % (75 of 83 cases) the extension was foreseen correctly. In no cases were false-positive results reported. Thus overall specificity was 100%. ment
TABLE n
Accuracy of Sonographic Findings Regarding the Location of Thrombosis Identified by Venography (n = 83)
*No
false-positive results in any location: overall specificity = 100 % . sensitivity concerning the diagnosis of thrombosis not regarding
**Overall
the exact extension: 95 % .
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604 Discussion
.
. , ’1
-
~
_
~
.
-
~ ~.
._ ,
.
’)~
the radiographic evaluation of the deep venous system of the lower extremity functions close to the optimal level of performance with the use of modern examination techniques, noninvasive methods for the diagnosis of DVT have met with great interest. The largely used noninvasive tests include Doppler ultrasound, occlusive-cuff plethysmography, and the 125I-Iabeled fibrinogen test. Methods with only sporadic application are thermography,25 ~’&dquo;’Tc-labeled plasmin test,26 and phleborheography.2g The number of methods suggest that their diagnostic information or application is problematic. Doppler ultrasound is a technique of great value in the diagnosis of thigh vein thromboSiS,3,9,29,30 (sensitivity and specificity, approximately 90%). It is not useful in the evaluation of the venous segments below the knee, where its sensitivity is low.9 It has the substantial disadvantage of showing only functional changes due to the thrombotic process. It cannot provide morphologic evidence of thrombosis. False-negative results can be expected in only partial occlusions, in obstructions with sufficient collateral venous drainage, and in congenital abnormalities with double or multiple abnormal vessels. False-positive results are found if the venous lumen is narrowed due to external compression such as hematomas or major edema. Properly used, occlusive-cuff plethysmography (applied as strain gauge-or impedanceplethysmography 10-12,31 is sensitive and specific in approximately 90 % of the cases in the diagnosis of thigh vein thrombosis. This method also reveals only functional changes and, similarly to Doppler ultrasound, is insensitive to calf vein thrombosis. It is not reliable in patients with severe chronic heart failure, in arterial vascular diseases, or in disorders with vascular narrowing by external compression. The I25I-labeled fibrinogen test is a complementary procedure and is able to compensate for the weaknesses of the foregoing methods. In the diagnosis of calf vein thrombosis, it is sensitive and specific in approximately 90% of the cases. 11,14,27,32,33 The test is not reliable in the evaluation of venous segments of the thigh. Furthermore, the results are available only twentyfour to forty-eight hours after the injection of the radionuclide, since uptake and accumulation of the tracer into the thrombotic material is only gradual. Further disadvantages and the handling of the radionuclide, as well as the need for specialized equipment. This test is strictly contraindicated in pregnant patients. False-positive results can be expected in patients with major soft-tissue trauma, hematomas, cellulitis, and thrombophlebitis and in patients who have had surgery on the extremities. False-negative results are reported in cases with a more chronic stage of thrombosis and during anticoagulation therapy. With the above-mentioned, commonly used, noninvasive methods, only a combined approach of either Doppler ultrasound or occlusive-cuff plethysmography and the ’25I-labeled fibrinogen test will provide sufficient diagnostic information on the deep venous system of the entire lower extremity. Although this procedure has been suggested by several authors,32 it has not been generally accepted, owing to the major efforts it requires in addition to the aforementioned disadvantages. The clinical importance of isolated calf vein thrombosis, which is frequently oligosymptomatic, is a controversial topic. 34,35 A postthrombotic syndrome rarely occurs. The risk of clinically important pulmonary thromboembolism is considered to be low owing to the small vol-
Although
&dquo;
’
~_
Downloaded from ang.sagepub.com at University of British Columbia Library on June 25, 2015
605 of the thrombi . 16 Nevertheless, the majority of the thigh vein thrombi develop from an obstruction of the venous system of the calf through ascending growth.3’’38 Thus, subsequently a hemodynamically important flow obstruction may occur. In outpatients with suspected calf vein thrombosis some physicians neglect the application of accurate procedures (venography, 1-labeled fibrinogen test). They are satisfied to just follow up the prior negative plethysmographic findings ten days later in order to detect early on a growth of a thrombus that might yet be present.34 In inpatients, however, common predisposing factors such as prolonged bed rest must be considered. Under these conditions, with the risk of undetected growth of a thrombus and the threat of clinically important pulmonary embolism, an accurate diagnostic test must be performed so that anticoagulation therapy can be instituted immediately if the results are positive. The results of this study, which was performed on a major patient population, indicate that real-time ultrasound is a highly accurate method for the diagnosis of DVT in the thigh, as well as in the calf. Among the noninvasive procedures, similar accuracy can be obtained only by the combined approach of either Doppler ultrasound or occlusive-cuff plethysmography and the 121 I-labeled fibrinogen test.’4,32 Contrary to other authors, we have markedly simplified the examination procedure without a reduction in accuracy, since we have visualized the venous lumen mainly by transversal scanning, and the only criterion for DVT was the absence of obliteration of the venous lumen by probe compression. Such evaluations are readily performed, and even the documentation of pathologic findings rarely requires more then ten minutes. An increased intraluminous echo pattern of thrombotic veins can generally be demonstrated in the common femoral vein and in the popliteal vein, which lie in a more superficial position. However, the superficial femoral vein, when thrombotic, often hardly differs in its sonographic appearance from the open, unobstructed lumen of the superficial femoral artery (Fig. 2). This vein lies deeper in its course than the aforementioned veins and the phenomenon may be caused by sound dispersion. It is unclear to what extent one can draw conclusions regarding the age of the thrombotic process from the echo density. In its more chronic stage the thrombi often show a higher echo density. A sonolucent marginal zone combined with partial obliteration of the lumen by compression indicates the presence of a floating thrombus. Unlike other investigators, 16-24,39,40 who found similar accuracy of the method in venous thrombosis of the thigh, we were able to demonstrate for the first time that with the ultrasonic examination technique introduced above, highly diagnostic information can be obtained on the venous segments of the calf, as well as of the thigh. In the supine patient the normal deep veins of the calf can usually not be visualized by ultrasound since their lumen is generally collapsed. In the presence of thrombosis, however, the vein becomes obstructed by the clot and dilated to sometimes grotesque proportions. Thus, in transversal scans it can be visualized accurately and appears as a worm-shaped, cross-cut channel that continuously runs through the ultrasonic image when the probe is moved (Fig. 3). It is sparse in its echo pattern and is not compressible. Frequently, the patient reports the palpation of the venous cord as painful. The posterior tibial veins and the peroneal veins, in each case two in number, are identified between the muscles near the tibia and fibula, whereas the anterior tibial veins lie further beyond the ume
Downloaded from ang.sagepub.com at University of British Columbia Library on June 25, 2015
606
assumed interosseus membrane between the two bones. Except for the anterior tibial veins, the differentiation of the various venous groups is altogether difficult, because of the frequent deviation of the veins by compression, especially in less muscular calves, and may be of minor clinical importance. ...,
,
~..
.
,_
’
Conclusions
Our results indicate that real-time ultrasonography, using the examination technique introduced above, is an almost ideal diagnostic imaging method; it should be the first choice in the diagnosis of suspected deep venous thrombosis of the lower extremity. With experience, ultrasonography is easily performed and interpreted. It can be repeated at any time and is able to provide correct information about diminution or growth of the thrombus during treatment. Adequate mobile equipment (real-time scanner; 5 MHz) is available at many locations. The results of the examination, which are performed in a short time, are available immediately. It is the only noninvasive method capable of accurately detecting DVT in the thigh, as well as in the calf. Thus, it can be used also as a screening procedure in addressing scientific questions. In our experience, ultrasonography is a complementary procedure to venography, especially in the presence of extensive thrombosis. Owing to reduced contrast material supply, the proximal end can sometimes not be determined venographically. It can, however, be clearly defined by ultrasonography. Lacking visualization of a venous group by contrast venography (especially in the calf) may be a technical problem or the result of a complete thrombosis. Ultrasound can answer the question be viewing the clot (Fig. 3). Two disadvantages of this method should be mentioned. First, it is operator-dependent, and second, it can frequently not be used in the evaluation of pelvic veins, because of overlying intestinal air. Isolated pelvic vein thrombosis, rarely occurs, however, and can be detected easily by Doppler ultrasound. The accuracy of duplex scanning was not a topic of this paper. Concerning the diagnosis of acute deep venous thrombosis of the lower extremity, it seems not to offer substantial advantage over real-time ultrasound but does provide further information in the evaluation of noncompressible pelvic veins and residual flow in nonoccluding thrombosis.
We
are
indebted to Dorothea
Acknowledgment Epping for exper assistance
in the
script.
preparation
of the ,
manu..
W. Habscheid, M. D. Medizinische Universitätsklinik Josef-Schneider-Str. 2 8700 Würzburg, West Germany
Downloaded from ang.sagepub.com at University of British Columbia Library on June 25, 2015
607
References 1. Barnes
cal
RW, Wu KK, Hoak JC: Fallibility of the clini-
diagnosis
of
venous
thrombosis. JAMA 234:605-
607, 1975. 2. Strandness DE, Summer DS: Acute venous thrombosis, a case of progress and confusion. JAMA 233:465470, 1975. 3. Rabinov K, Paulin S: Roentgen diagnosis of venous thrombosis in the leg. Arch Surg 104:134-144, 1972. 4. Albrechtson LL, Olson QCG: Thrombotic side effects of lower limb phlebography. Lancet 2:723-724, 1976. 5. Bettmann AM, Paulin S: Leg phlebography. The incidence, nature and modifications of undesirable side effects. Radiol Diagn 122:101-104, 1977. 6. Kristiansen P, Bergentz S-E, Bergquist D, et al: Thrombosis after elective phlebography as demonstrated with the -fibrinogen 125 test. Acta Radiol Diagn J 22:577-578, 1981. 7. Thomas ML, McDonald M: Complications of ascending phlebography of the leg. Br Med J 2:317-318, 1978. 8. Meadway J, Nicolaides AN, Walker CJ, et al: Value of Doppler ultrasound in diagnosis of clinically suspected deep venous thrombosis. Br Med J 2:552-554, 1975. 9. Sigel B, Popky GL, Wagner DK, et al: Comparison of clinical and Doppler ultrasound evaluation of confirmed lower extremity venous disease. Surgery 64:332-338, 1968. 10. Hull R, van Aken WG, Hirsh J, et al: Impedance plethysmography using the occlusive cuff technique in the diagnosis of venous thrombosis. Circulation 53 :696700, 1976. 11. Sandler DA, Martin RJ, Duncan JS, et al: Diagnosis of deep vein thrombosis. Comparison of clinical evaluation ultrasound, plethysmography and venoscan with x-ray venogram. Lancet 2:716-719, 1984. 12. Wheeler HB, O’Donnel JA, Anderson FA, et al: Occlusive impedance phlebography: A diagnostic procedure for venous thrombosis and pulmonary embolism. Prog Cardiovasc Dis 27:199-205, 1974. I-labeled 13. Kakkar VV, Nicolaides AN, Renney JTG: 125 fibrinogen test adapted for routine screening for deep vein thrombosis. Lancet 1:540-543, 1970. 14. Hull R, Hirsh J, Sackett DL, et al: Replacement of venography in suspected venous thrombosis by impedance plethysmography and 125 I-fibrinogen-leg-scanning. Ann Int Med 94:12-15, 1981. 15. Talbot SR: Use of real-time imaging in identifying deep venous thrombosis. A primary report. Bruit 6 :4142, 1982. 16. Effeney DJ, Friedmann MB, Godding GAW: Ileofemoral venous thrombosis. Real-time ultrasound diagnosis. Normal criteria and clinical application. Radiol 150:787-792, 1984. 17. Vogel P, Laing FD, Jeffrey RB, et al: Deep venous thrombus of the lower extremity. US evaluation. Radiol 163:747-751, 1987. 18. Appelmann PT, DeJong TE, Lampman LE: Deep venous thrombosis of the leg. US evaluation. Radiol 163:743-757, 1987. 19. Cronan JJ, Dorfman GS, Scola FH, et al: Deep venous thrombosis. US assessment using vein compression. Radiol 162:191-194, 1987.
20. Dauzat MM, Laroche J-R, Charras Ch, et al: Real time B-mode ultrasonography for better specificity in the noninvasive diagnosis of deep vein thrombosis. J Ultrasound Med 5:625-631, 1986. 21. Raghavendra BN, Rosen J, Riles Th, et al: Deep venous thrombosis. Detection by high-resolution realtime sonography. Radiol 152:789-793, 1984. 22. Raghavendra BN, Horii StC, Hilton S, et al: Deep venous thrombosis. Detection by probe compression of veins. J Ultrasound Med 5:89-95, 1986. 23. Sullivan DE, Peter DJ, Cranley JJ: Real time B mode venous ultrasound. J Vasc Surgery 1:465-471, 1984. 24. Lensing AWA, Prandoni P, Brandes D, et al: Detection of deep-vein thrombosis by real time B mode ultrasonography. N Engl J Med 320:342-345, 1989. 25. Jacobson H: Standardized leg temperature profiles in the diagnosis of acute deep venous thrombosis. Vasc Diagn Ther 3:55-58, 1983. 26. Adolfson L, Nordenfeld J, Olson H, et al: Diagnosis of Tc labeled plasmin. Acta deep vein thrombosis with 99m Med Scand 211:365-368, 1982. 27. Gomes AS, Webber MM, Buffkin D: Contrast venography vs radionuclide venography. A study of discrepancies and their possible significance. Radiol 142 :719723, 1982. 28. Cranley JJ, Canos AJ, Sull WS, et al: Phleborheographic technique for diagnosis of deep venous thrombosis of the lower extremities. Surg Gynec Obstet 141:331-359, 1975. 29. Holmes MCG: Deep venous thrombosis of the lower limbs diagnosed by ultrasound. Med J Australia 1:427430, 1973. 30. Evans DS, Cockett FB: Diagnosis of deep vein thrombosis with an ultrasonic Doppler technique. Br Med J 2:802-807, 1969. 31. Barnes RW, Hokanson EE, Wu KK, et al: Detection of deep venous thrombosis with an automatic electrically calibrated strain gauge plethysmograph. Surgery 82:219-223, 1977. 32. Hull R, Sackett OL, Powers P, et al: Combined use of leg scanning and impedance plethysmography in suspected venous thrombosis. N Engl J Med 296 :14971500, 1977. 33. Kakkar VV, Corrigan TP: Detection of deep vein thrombosis. Survey and current status. Progr Cardiovasc Dis 27:207-217, 1974. 34. Huismann MV, Büller HR, Tencate JW, et al: Serial impedance plethysmography for suspected deep venous thrombosis. N Engl J Med 314:823-828, 1986. 35. Lagerstedth CJ, Olson C-G, Fagher BO, et al: Need for long-term anticoagulant treatment in symptomatic calf vein thrombosis. Lancet 2:517-518, 1985. 36. Moser KM, LeMoine JR: Is embolic risk conditioned by location of deep vein thrombosis? Ann Int Med 94:439-444, 1981. 37. Nicolaides AN, Kakkar VV, Fields ES, et al: The origin of deep venous thrombosis: A venographic study. Br J Radiol 44:653-663, 1971. 38. Kakkar VV, Howe CT, Flaric C, et al: Natural history of postoperative deep vein thrombosis. Lancet 2:230233, 1969.
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608 39. Polak JF, O’Leary DH: Deep venous thrombosis in pregnancy: Noninvasive diagnosis. Radiol 166 :377-
379, 1988.
40. Aitken AGF, Godden DJ: Real-time ultrasound diagnosis of deep vein thrombosis: A comparison with venography. Clin Radiol 38:309-313, 1987.
Downloaded from ang.sagepub.com at University of British Columbia Library on June 25, 2015
Wolfgang Habscheid, M.D. Margarethe Höhmann, M.D. Thomas Wilhelm, M.D. and Johannes Epping, M.D.
WÜRZBURG,
WEST GERMANY
Abstract One hundred twenty-six patients with clinically suspected acute deep venous thrombosis of the lower extremity (DVT) were examined comparatively with ultrasound and venography. In total, 174 lower extremity venograms were obtained. Ultrasonic examinations were performed on patients in the supine position. The venous segments were evaluated almost exclusively with transversal scanning. In the thigh, the only criterion for DVT was the reduced or absent compressibility of the venous lumen when gently compressed with the transducer. In the calf, normal unobstructed veins can usually not be viewed in the supine patient, whereas thrombotic veins appear as sonolucent, incompressible channels. Eight-three of the 174 lower extremity venograms were positive for DVT. In the majority of cases (53 of 83) the thrombotic process had involved two or more segments in combination. The sites of involvement of the different venous segments were distributed as follows: 24 occlusions of the common femoral vein, 52 of the superficial femoral vein, 56 of the popliteal vein, and 71 of the calf veins. Ultrasound had a sensitivity of 100% for thrombosis of the common femoral vein, 96% for the superficial femoral veins, 98% for the popliteal vein, and 93% for the calf veins. For the entire lower extremity, in regard to the diagnosis of thrombosis, the overall sensitivity was 95%. In 90% the extension of the occlusion was foreseen correctly. In no cases were false-positive results reported. Thus the overall specificity was 100%. The authors conclude that real-time ultrasound is a highly accurate method method for the diagnosis of DVT of the lower extremity. It is the only
indirect
From the
Department of Medicine
and
Radiology
of the
University
of
Würzburg, Würzburg,
599
Downloaded from ang.sagepub.com at University of British Columbia Library on June 25, 2015
West
Germany
600
capable of evaluating the venous system of the thigh, as well as that of the calf, with high accuracy. It should be the first choice of diagnostic imaging method in the diagnosis of deep venous thrombosis of the lower extremity. Introduction
x
The clinical diagnosis of deep venous thrombosis (DVT) of the lower extremity is known to be difficult and is accurate in only about 50% of the cases.’’2 Contrast venography is generally accepted as the gold standard for the diagnosis of DVT.’ It is, however, invasive, and a number of untoward responses after the administration of intravenous contrast material must be considered: 4-7 systemic anaphylactic reactions, local irritation, initiation of thrombophlebitis or even thrombosis, and aggravation of chronic renal or cardiac failure. Furthermore, the need for specialized equipment should not be underestimated. Therefore, numerous attempts have been made to develop other &dquo;indirect&dquo; noninvasive diagnostic procedures; Doppler ultrasound8’9 and plethysmographylO-12 have been found to be accurate in the evaluation of the thigh vein system, whereas the 1251-labeled fibrinogen test is sensitive to thrombus formation in calf veins. 1,11,14 Nonetheless, a noninvasive method of evaluating the venous system of the entire lower extremity that is easily performed and can be used prior to venography has not yet been established. Such a method would be beneficial, since the disease is often clinically oligosymptomatic. It is well known that thrombotic veins have a characteristic ultrasonic appearance and that there are several diagnosis patterns: they are not compressible’9’22 and usually show a typical intraluminous echo pattern, which cannot, however, always be demonstrated Further characteristic signs are the absence of vasodilatation during the Valsalva maneuver 16 and the widening of venous segments that lie distal to the occlusion.&dquo; Systemic investigations of the value of ultrasound in the diagnosis of DVT are rare and are limited mostly to the evaluation of the femoral vein or the popliteal vein. 16-24,39.40 Studies concerning calf vein thrombosis are missing completely. For this reason, we have completed a study involving a major patient population that examined the potential of ultrasound as a diagnostic imaging technique in suspected acute DVT in the thigh region, as well as in the calf. Patients and Methods
study was performed in 126 patients with clinically suspected acute DVT of the lower extremity. They ranged from seventeen to eighty-four years of age with a mean of 60.2 years. All patients underwent ultrasonic examination of both lower extremities. On the same day, venography of the symptomatic lower extremity was performed. If pulmonary embolism was suspected, bilateral lower extremity venograms were performed. In total, 174 venograms of one lower extremity were obtained. The ultrasonic and the venographic findings were interpreted by independent observers. Finally, the results were compared with one another. Discrepancies between the findings were not reinterpreted retrospectively. Contrast venography was carried out according the method of Rabinov and Paulin,3 except that ankle tourniquets were used to obtain optimal contrast filling of the deep veins. The criterion for acute DVT was the presence of an intraluminal filling defect, confirmed in two The
Downloaded from ang.sagepub.com at University of British Columbia Library on June 25, 2015
601
projections, or repeated nonfilling of a venous segment after different injections of Ultrasonography was performed using a common-type real-time scanner. The patient was examined in the supine position. The thigh was examined by ventral approach, moving the transversally applied transducer continuously from the inguinal region to the knee. For the evaluation of the popliteal vein and the calf veins (tibialis posterior and peroneal veins), the knee was flexed and transverse scans were obtained by posterior approach. A patent venous lumen can be compressed completely by the transducer (Fig. 1). The criterion for venous thrombosis was the markedly reduced or absent obturation of the venous lumen by gentle probe compression (Fig. 2). If present, an intraluminous echo pattern was registered but was not interpreted as thrombosis if the reaction to compression had been normal. The evaluation was performed mainly by transversal scanning. The examination along the longitudinal vascular axis is difficult since the transducer frequently deviates laterally during the compression maneuver. By moving the transducer continuously from the inguinal region to the knee, the common femoral vein is viewed medial to the artery. In the higher part of its course, the different
contrast material.
FIG. 1. Transverse scan of the normal common femoral vein. (left) Without probe compression. B. With probe compression. Note the complete obturation of the patent venous lumen in B. (right) AFC common femoral artery. VFC common femoral vein. =
=
FIG. 2. (left) Transverse scan of the superficial femoral vein with probe compression in the middle of the thigh; the occluded vein has the same echopattem as the patent artery but is not compressible. AFS superficial femoral artery, VFS superficial femoral vein. (right) Occlusion of the popliteal vein; the vein is widened and filled with an incompressible echogenic clot. AP = popliteal artery, VP popliteal vein. =
=
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=
602
superficial femoral vein lies behind the artery, and in its lower part it lies external to the artery. In the popliteal space, the posterior approach shows the popliteal vein, which lies superficial to the artery. A sweep of the transducer in the cranial direction provides the view and the compression of the vessels in the adductor canal. Distally the junction of the calf veins forming the popliteal vein can frequently be seen. Patent calf veins can usually not be viewed in the supine patient. In thombosis, however, they become visible and appear as incompressible channels, which in cross-section scans look like worm-shaped, crosscut structures that continuously run through the ultrasonic image when the probe is moved (Fig. 3). The posterior tibial veins and the peroneal veins, when thrombotic, can be localized between the muscles near the tibia and fibula. They are examined by a dorsal approach. Occluded anterior tibial veins lie further beyond the assumed interosseus membrane between the tibia and the fibula. They can be viewed and submitted to compression by the peroneal region.
FIG. 3. (left) Contrast venography of the calf; the lack of visualization of the posterior femoral veins is suspicious of thrombosis. (right) Sonography proves the clots by showing two noncompressible echopoor venous segments.
Results
Among the 174 venograms of one lower extremity, which were performed in 126 patients, 83 were positive for deep venous thrombosis. The distribution regarding the site of the different venous groups is shown in Table I. In the majority of the cases (53 of 83) two or more segments were involved in combination. Isolated occlusions were found in the remain30 cases, the majority of which were calf vein thrombosis in 23 patients. The common ing femoral vein was involved in 24, the superficial femoral vein in 52, the popliteal vein in 56, and the calf veins in 71 cases. The difference between the total number of thromboses and the sum of occluded venous segments was due to the fact that at least two segments were mostly venous
involved. With venography as the diagnostic reference method, the accuracy of the sonographic findings compared with that of the venographic findings is shown in Table II. For the calf veins the sensitivity of ultrasound was 93 % overall and 87 % for patients with isolated calf involvement. Regarding the different venous segments of the thigh, the involvement of the common
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603 Distribution
of the
Venographically Identified
TABLE I Occlusions Regarding the
Different
Venous
Segments (n = 83)
femoral vein was correctly seen in all (sensitivity 100%), and occlusion of the superficial femoral vein was missed in 2 patients (sensitivity 96 % ) and of the popliteal vein in 1 patient
(sensitivity 98 % ) . Regarding the false-negative results 1 of the 2 missed superficial femoral vein occlusions was a small thrombus of 2 cm length near the adductor channel and 1 was an easily seen ascending thrombosis whose upper end was not correctly realized. One thrombosis of the popliteal vein originating from calf vein thrombosis was overlooked, whereas the calf involvement could be demonstrated by ultrasound. Of the 5 false-negative results concerning calf vein thrombosis, 3 were isolated to the calf. In the remaining 2, additional occlusions of upper venous
segments were viewed correctly. In these cases the lack of visibility of the calf involve-
by ultrasound could be due to long-standing organization of the thrombus.
Two of the 3 isolated calf vein occlusions were confined to one venous and overlooked had a thromgroup bus diameter of only approximately 3 mm. One was missed because of an atypically sonolucent echopattem of the muscle. Thus only 4 of the 83 thromboses were missed completely by ultrasound, and 3 of them were confined to the calf region. The overall sensitivity concerning the diagnosis of thrombosis was 95 % . In 90 % (75 of 83 cases) the extension was foreseen correctly. In no cases were false-positive results reported. Thus overall specificity was 100%. ment
TABLE n
Accuracy of Sonographic Findings Regarding the Location of Thrombosis Identified by Venography (n = 83)
*No
false-positive results in any location: overall specificity = 100 % . sensitivity concerning the diagnosis of thrombosis not regarding
**Overall
the exact extension: 95 % .
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604 Discussion
.
. , ’1
-
~
_
~
.
-
~ ~.
._ ,
.
’)~
the radiographic evaluation of the deep venous system of the lower extremity functions close to the optimal level of performance with the use of modern examination techniques, noninvasive methods for the diagnosis of DVT have met with great interest. The largely used noninvasive tests include Doppler ultrasound, occlusive-cuff plethysmography, and the 125I-Iabeled fibrinogen test. Methods with only sporadic application are thermography,25 ~’&dquo;’Tc-labeled plasmin test,26 and phleborheography.2g The number of methods suggest that their diagnostic information or application is problematic. Doppler ultrasound is a technique of great value in the diagnosis of thigh vein thromboSiS,3,9,29,30 (sensitivity and specificity, approximately 90%). It is not useful in the evaluation of the venous segments below the knee, where its sensitivity is low.9 It has the substantial disadvantage of showing only functional changes due to the thrombotic process. It cannot provide morphologic evidence of thrombosis. False-negative results can be expected in only partial occlusions, in obstructions with sufficient collateral venous drainage, and in congenital abnormalities with double or multiple abnormal vessels. False-positive results are found if the venous lumen is narrowed due to external compression such as hematomas or major edema. Properly used, occlusive-cuff plethysmography (applied as strain gauge-or impedanceplethysmography 10-12,31 is sensitive and specific in approximately 90 % of the cases in the diagnosis of thigh vein thrombosis. This method also reveals only functional changes and, similarly to Doppler ultrasound, is insensitive to calf vein thrombosis. It is not reliable in patients with severe chronic heart failure, in arterial vascular diseases, or in disorders with vascular narrowing by external compression. The I25I-labeled fibrinogen test is a complementary procedure and is able to compensate for the weaknesses of the foregoing methods. In the diagnosis of calf vein thrombosis, it is sensitive and specific in approximately 90% of the cases. 11,14,27,32,33 The test is not reliable in the evaluation of venous segments of the thigh. Furthermore, the results are available only twentyfour to forty-eight hours after the injection of the radionuclide, since uptake and accumulation of the tracer into the thrombotic material is only gradual. Further disadvantages and the handling of the radionuclide, as well as the need for specialized equipment. This test is strictly contraindicated in pregnant patients. False-positive results can be expected in patients with major soft-tissue trauma, hematomas, cellulitis, and thrombophlebitis and in patients who have had surgery on the extremities. False-negative results are reported in cases with a more chronic stage of thrombosis and during anticoagulation therapy. With the above-mentioned, commonly used, noninvasive methods, only a combined approach of either Doppler ultrasound or occlusive-cuff plethysmography and the ’25I-labeled fibrinogen test will provide sufficient diagnostic information on the deep venous system of the entire lower extremity. Although this procedure has been suggested by several authors,32 it has not been generally accepted, owing to the major efforts it requires in addition to the aforementioned disadvantages. The clinical importance of isolated calf vein thrombosis, which is frequently oligosymptomatic, is a controversial topic. 34,35 A postthrombotic syndrome rarely occurs. The risk of clinically important pulmonary thromboembolism is considered to be low owing to the small vol-
Although
&dquo;
’
~_
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605 of the thrombi . 16 Nevertheless, the majority of the thigh vein thrombi develop from an obstruction of the venous system of the calf through ascending growth.3’’38 Thus, subsequently a hemodynamically important flow obstruction may occur. In outpatients with suspected calf vein thrombosis some physicians neglect the application of accurate procedures (venography, 1-labeled fibrinogen test). They are satisfied to just follow up the prior negative plethysmographic findings ten days later in order to detect early on a growth of a thrombus that might yet be present.34 In inpatients, however, common predisposing factors such as prolonged bed rest must be considered. Under these conditions, with the risk of undetected growth of a thrombus and the threat of clinically important pulmonary embolism, an accurate diagnostic test must be performed so that anticoagulation therapy can be instituted immediately if the results are positive. The results of this study, which was performed on a major patient population, indicate that real-time ultrasound is a highly accurate method for the diagnosis of DVT in the thigh, as well as in the calf. Among the noninvasive procedures, similar accuracy can be obtained only by the combined approach of either Doppler ultrasound or occlusive-cuff plethysmography and the 121 I-labeled fibrinogen test.’4,32 Contrary to other authors, we have markedly simplified the examination procedure without a reduction in accuracy, since we have visualized the venous lumen mainly by transversal scanning, and the only criterion for DVT was the absence of obliteration of the venous lumen by probe compression. Such evaluations are readily performed, and even the documentation of pathologic findings rarely requires more then ten minutes. An increased intraluminous echo pattern of thrombotic veins can generally be demonstrated in the common femoral vein and in the popliteal vein, which lie in a more superficial position. However, the superficial femoral vein, when thrombotic, often hardly differs in its sonographic appearance from the open, unobstructed lumen of the superficial femoral artery (Fig. 2). This vein lies deeper in its course than the aforementioned veins and the phenomenon may be caused by sound dispersion. It is unclear to what extent one can draw conclusions regarding the age of the thrombotic process from the echo density. In its more chronic stage the thrombi often show a higher echo density. A sonolucent marginal zone combined with partial obliteration of the lumen by compression indicates the presence of a floating thrombus. Unlike other investigators, 16-24,39,40 who found similar accuracy of the method in venous thrombosis of the thigh, we were able to demonstrate for the first time that with the ultrasonic examination technique introduced above, highly diagnostic information can be obtained on the venous segments of the calf, as well as of the thigh. In the supine patient the normal deep veins of the calf can usually not be visualized by ultrasound since their lumen is generally collapsed. In the presence of thrombosis, however, the vein becomes obstructed by the clot and dilated to sometimes grotesque proportions. Thus, in transversal scans it can be visualized accurately and appears as a worm-shaped, cross-cut channel that continuously runs through the ultrasonic image when the probe is moved (Fig. 3). It is sparse in its echo pattern and is not compressible. Frequently, the patient reports the palpation of the venous cord as painful. The posterior tibial veins and the peroneal veins, in each case two in number, are identified between the muscles near the tibia and fibula, whereas the anterior tibial veins lie further beyond the ume
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606
assumed interosseus membrane between the two bones. Except for the anterior tibial veins, the differentiation of the various venous groups is altogether difficult, because of the frequent deviation of the veins by compression, especially in less muscular calves, and may be of minor clinical importance. ...,
,
~..
.
,_
’
Conclusions
Our results indicate that real-time ultrasonography, using the examination technique introduced above, is an almost ideal diagnostic imaging method; it should be the first choice in the diagnosis of suspected deep venous thrombosis of the lower extremity. With experience, ultrasonography is easily performed and interpreted. It can be repeated at any time and is able to provide correct information about diminution or growth of the thrombus during treatment. Adequate mobile equipment (real-time scanner; 5 MHz) is available at many locations. The results of the examination, which are performed in a short time, are available immediately. It is the only noninvasive method capable of accurately detecting DVT in the thigh, as well as in the calf. Thus, it can be used also as a screening procedure in addressing scientific questions. In our experience, ultrasonography is a complementary procedure to venography, especially in the presence of extensive thrombosis. Owing to reduced contrast material supply, the proximal end can sometimes not be determined venographically. It can, however, be clearly defined by ultrasonography. Lacking visualization of a venous group by contrast venography (especially in the calf) may be a technical problem or the result of a complete thrombosis. Ultrasound can answer the question be viewing the clot (Fig. 3). Two disadvantages of this method should be mentioned. First, it is operator-dependent, and second, it can frequently not be used in the evaluation of pelvic veins, because of overlying intestinal air. Isolated pelvic vein thrombosis, rarely occurs, however, and can be detected easily by Doppler ultrasound. The accuracy of duplex scanning was not a topic of this paper. Concerning the diagnosis of acute deep venous thrombosis of the lower extremity, it seems not to offer substantial advantage over real-time ultrasound but does provide further information in the evaluation of noncompressible pelvic veins and residual flow in nonoccluding thrombosis.
We
are
indebted to Dorothea
Acknowledgment Epping for exper assistance
in the
script.
preparation
of the ,
manu..
W. Habscheid, M. D. Medizinische Universitätsklinik Josef-Schneider-Str. 2 8700 Würzburg, West Germany
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607
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