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Subclavian and Internal Jugular Veins at Doppler US: Abnormal Cardiac Pulsatility and Respiratory Phasicity as a Predictor of Complete Central Occlusion¹

¹ From Addenbrooke Hospital, Cambridge, England. Received June 2, 1998; revision requested July 27; revision received September 8; accepted November 20. Address reprint requests to M.C.P., Department of Neuroradiology, Manchester Royal Infirmary, Oxford Rd, Manchester, England M13 9WL.

	Abstract

TOP Abstract Introduction Materials and Methods Results Discussion References

 
In 21 consecutive patients, the authors analyzed changes in venous Doppler waveforms of damped or diminished cardiac pulsatility and respiratory phasicity. Each patient was suspected of having upper limb venous thrombosis, but thrombus was not visible at gray-scale ultrasonography (US) in the subclavian and brachiocephalic veins. US findings were compared with phlebographic findings. The results show that US can be used to establish the presence or absence of thrombosis in the distal portion of the brachiocephalic or subclavian veins, which are inaccessible to direct insonation.

Index terms: Thrombosis, US, 94.12984, 907.12984 • Veins, innominate, 9461.751 • Veins, jugular, 907.751 • Veins, subclavian, 9462.751 • Veins, thrombosis, 94.751, 907.751

	Introduction

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Symptoms and signs of central or upper limb venous thrombosis are not specific and may be mimicked by those of local infection, mediastinal malignancy, arm lymphedema due to radiation therapy or axillary surgery. Gray-scale ultrasonography (US) is sensitive and specific for the demonstration of thrombus in the axillary vein and the lateral course of the subclavian vein accessible to direct US, but it has been considered unreliable for the definition of thrombus in the central portion of the subclavian and brachiocephalic veins due to inadequate access to these vessels (1). In our institution, bilateral injection of contrast material via the basilic veins has been the technique of choice for demonstrating central venous thrombus.

Normal spectral Doppler signals of arm and neck veins are characterized by two phasic variations in amplitude. Cardiac pulsatility due to the retrograde pressure waves of right atrial contraction is synchronized to the pulse rate and frequently results in a biphasic signal. Superimposed on this is the phasic change in amplitude caused by variations in venous return as a result of the respiratory cycle with an increase on inspiration and decrease on expiration (Fig 1). These phasic changes are easily distinguishable. Cardiac pulsatility is a much more rapid phasic change that repeats with the cardiac cycle, which can be confirmed by means of palpitation of the radial artery. Respiratory phasicity is noted to coincide with the patient's respiratory rate, which can be confirmed by means of simple observation.

View larger version (53K): [in this window] [in a new window]   Figure 1a. (a) Left: Doppler waveform with velocity peaks that coincide with the cardiac cycle. Right: US scan depicts the corresponding gate used to sample a thrombus-free section of a subclavian vein. (b) Doppler waveform of the left subclavian vein (lt scv) shows that in addition to the rapid phasic changes in cardiac pulsatility, there is a further variation in amplitude that corresponds to inspiration and expiration.

View larger version (28K): [in this window] [in a new window]   Figure 1b. (a) Left: Doppler waveform with velocity peaks that coincide with the cardiac cycle. Right: US scan depicts the corresponding gate used to sample a thrombus-free section of a subclavian vein. (b) Doppler waveform of the left subclavian vein (lt scv) shows that in addition to the rapid phasic changes in cardiac pulsatility, there is a further variation in amplitude that corresponds to inspiration and expiration.

As a result, we prospectively evaluated the reduction or loss in respiratory phasicity and cardiac pulsatility of the Doppler waveform as a predictor of central venous occlusion. We tested the hypothesis that a reduction or loss of either or both of these phasic phenomena indicates the presence of central venous thrombus.

	Materials and Methods

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Between April 1996 and April 1997, we saw patients referred to us for US examination to evaluate possible upper limb thrombus. Symptoms and signs included arm or neck pain, localized erythema, arm swelling, dilated superficial collateral veins, and failure to aspirate blood or introduce fluid into an indwelling central venous catheter.

All US studies were performed by one experienced staff sonologist (L.H.B.) with the patient supine. The axillary, subclavian, and internal jugular veins were assessed for directly visualized thrombus by using established gray-scale and color Doppler techniques for upper arm and central venous US (2). If thrombus was directly visualized at gray-scale US, the patients were excluded from the study group.

The study group comprised 21 consecutive patients (eight men and 13 women; age range, 19–71 years; mean age, 42 years) suspected of having central venous or arm thrombosis, but no directly accessible thrombus was seen in the subclavian or jugular veins at preliminary gray-scale or color Doppler US. Eight of the study patients had acute leukemia, seven had a solid malignancy (including lymphoma), two had vasculitis, two were being treated with dialysis, and two were receiving long-term parenteral feeding. Eighteen of the study patients had undergone at least one previous central venous catheterization, and the central venous catheter was still in place in 16.

All study patients then underwent a more detailed US assessment of the axillary, subclavian, and internal jugular veins. The examination was performed in both transverse and longitudinal scanning planes with a variable-frequency 6–10-MHz linear-array transducer that usually operated at 7.5 MHz (Powervision; Toshiba Medical Systems, Tokyo, Japan). Lower operating frequencies were used in larger subjects. Preprogrammed venous scanning parameters were employed with a Doppler frequency of 5 MHz and pulse repetition frequency of 8 kHz. The Doppler angle, color box size, and color box angle were optimized manually as appropriate. However, the Doppler angle was kept constant for the comparison of right and left sides. Absolute flow velocities were not measured. The patient's head was initially turned approximately 45° contralateral to the side being scanned. During the study, the patients turned their heads through approximately 90° to assess whether this maneuver affected the signal.

As there is no convention in the literature, to our knowledge, we defined the term "proximal" as applied to a vein to refer to regions near the origin of the vein. We defined "distal" as referring to the more central course of the vein (ie, the proximal subclavian vein is toward the patient's axilla, and the distal subclavian vein is toward the patient's neck).

The results were analyzed in terms of two separate arm-neck vein units per patient (ie, each patient has a right and a left arm-neck vein unit).

The Doppler waveforms were then documented at four sites during quiet respiration: the right and left subclavian veins via an infraclavicular window and the right and left internal jugular veins. Each vein was assessed independently for the presence of respiratory phasicity and cardiac pulsatility. If absent or damped respiratory phasicity was observed, the veins were rescanned with increased respiratory excursions (Figs 2, 3). Augmentation by means of arm massage or Valsalva maneuver was not performed. The direction of flow in each of the four veins was also noted. The sonologist completed a form indicating the direction of blood flow and whether cardiac pulsatility or respiratory phasicity were normal, absent, or damped relative to findings on the contralateral asymptomatic side.

View larger version (39K): [in this window] [in a new window]   Figure 2. Left: Doppler waveform is abnormal on the basis of an absence of changes in either cardiac pulsatility or respiratory phasicity. Right: Corresponding US scan depicts the gate used to sample an apparently thrombus-free venous lumen.

View larger version (30K): [in this window] [in a new window]   Figure 3. Left: Doppler waveform obtained in the right subclavian vein (rt scv) shows normal changes. Right: Doppler waveform obtained in the left subclavian vein (lt scv) shows total damping of cardiac and respiratory phasic changes.

View larger version (98K): [in this window] [in a new window]   Figure 4. Phlebogram obtained in an internal jugular vein shows absent cardiac pulsatility and respiratory phasicity. Apparent cardiac pulsatility is caused by pulsation transmitted from the adjacent common carotid artery.

View larger version (57K): [in this window] [in a new window]   Figure 5. Schematic depicts the way the site of thrombosis is inferred from the location of abnormal signals. In. V = innominate (brachiocephalic) vein , Lt = left, Rt = right, SCV = subclavian vein, SVC = superior vena cava.

View larger version (133K): [in this window] [in a new window]   Figure 6a. (a, b) Phlebograms obtained in two patients with thrombosis of the medial portion (arrow) of each subclavian vein.

View larger version (132K): [in this window] [in a new window]   Figure 6b. (a, b) Phlebograms obtained in two patients with thrombosis of the medial portion (arrow) of each subclavian vein.

	Results

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Abnormal Spectral Waveforms
In 12 arm-neck vein units, the Doppler waveforms were damped. In all 12, the phlebographic findings (MR phlebography in one patient) confirmed the presence of occlusive thrombus as predicted at US. No patients had bilaterally abnormal waveforms, which would have implied either a coexistent right- and left-sided thrombus or superior vena cava thrombus.

Considering these 12 abnormal results further, four of the five abnormal left-sided arm-neck vein units showed absence of both cardiac pulsatility and respiratory phasicity at Doppler US in the internal jugular and subclavian veins. The sonologist predicted thrombus in the left brachiocephalic vein in all four cases, which was confirmed at phlebography. In the remaining case, cardiac pulsatility was absent in the subclavian and internal jugular veins but respiratory phasicity was absent in only the subclavian vein. The sonologist predicted thrombus but was unable to deduce from these findings whether it was in the left brachiocephalic vein or in only the subclavian vein. At phlebography, subclavian venous thrombus was seen.

Among the seven patients with right-sided thrombus, one had abnormal cardiac pulsatility and respiratory phasicity in the right subclavian and internal jugular veins, and right brachiocephalic venous thrombus was seen at phlebography. Three patients had abnormal cardiac pulsatility and respiratory phasicity of only the subclavian vein and were found to have isolated subclavian venous thrombus at phlebography as anticipated. In the remaining three right-sided studies, normal respiratory phasicity and cardiac pulsatility were demonstrated in the jugular vein. In the subclavian veins in these three cases, cardiac pulsatility was absent, but respiratory phasicity was normal. At phlebography in these three patients, isolated right subclavian venous thrombus was found.

In no case did thrombus at any site, jugular or subclavian, have diminished respiratory phasicity but normal cardiac pulsatility. In all 12 veins with distal thrombus, cardiac pulsatility was absent or damped. In three cases, phlebographically proved thrombus in a single vessel had abnormal cardiac pulsatility but normal respiratory phasicity. All three of these thrombi were in the right subclavian vein. In one left-sided study, cardiac pulsatility was diminished in the internal jugular vein and both cardiac pulsatility and respiratory phasicity were diminished in the subclavian vein. This suggests a diagnosis of brachiocephalic thrombosis, but occlusive thrombus was seen at phlebography in the subclavian vein that prevented adequate contrast material demonstration of the brachiocephalic vein.

At the time of the US examination, central venous catheters were in place in 17 arm-neck vein units. In seven of these cases, the Doppler waveforms were considered normal and findings were also normal at phlebography (ie, the presence of a central venous catheter in part of the lumen of an otherwise normal vein did not result in a false-positive diagnosis). This confirms the findings in a previous report (3).

In no case with thrombus proved at phlebography was retrograde venous blood flow seen in the directly accessible subclavian or internal jugular veins. No potentially confusing spectral changes were noted when the patient's neck was turned through an arc of approximately 90°. Partial occlusion was not seen in any of the 41 arm-neck vein units studied.

In summary, the sonologist correctly excluded thrombus in all 29 thrombus-free arm-neck vein units and predicted the presence of thrombus in all 12 arm-neck vein units with a thrombus. In 11 of the latter, the site was confirmed at phlebography. In the remaining case, the thrombus indicated at US could not be assessed fully at phlebography because total occlusion of the subclavian vein resulted in poor filling of the brachiocephalic vein.

For the combination of diminished respiratory phasicity and diminished cardiac pulsatility to identify the presence of thrombosis, sensitivity was 75% (nine of 12 arm-neck vein units), specificity 100% (29 of 29), positive predictive value 100% (nine of nine), and negative predictive value 91% (29 of 32). For the separate analysis of signs to identify the presence of thrombosis, with diminished or absent cardiac pulsatility, sensitivity was 100% (12 of 12), specificity 100% (29 of 29), positive predictive value 100% (12 of 12), and negative predictive value 100% (29 of 29) and with diminished or absent respiratory phasicity, sensitivity was 75% (nine of 12), specificity 100% (29 of 29), positive predictive value 100% (nine of nine), and negative predictive value 91% (29 of 32).

	Discussion

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Upper limb and central venous thrombosis may be caused by central venous catheterization, extrinsic vascular compression, vasculitis, or thrombotic tendency. Catheter placement is currently the most common etiologic factor, with thrombus reported in as many as 28% of patients with subclavian catheters (4). The risk of a pulmonary embolus has been estimated between 8% and 12% of all patients with upper limb thrombus (5–7), which is the source of 2%–4% of all pulmonary emboli (7,8). Among pulmonary emboli that originate from an upper limb source, 25% will prove fatal (5).

In 1986, abnormal cardiac pulsatility and respiratory phasicity were reported to be indicators of central venous occlusion in the superior vena cava (9). Subsequent US studies (1,10–13) have described the detection of thrombus in the brachiocephalic, subclavian, and axillary veins by means of direct demonstration of the thrombus, indirect demonstration of loss of venous compressibility, and direct demonstration of collateral vessels rather than by means of inference of the presence of thrombus on the basis of an abnormal Doppler waveform. Gray-scale US is extremely sensitive in the direct demonstration of thrombus in the axillary vein since the vein is superficial and has clear acoustic windows. Sensitivities of up to 95% have been reported (10). Unfortunately, access to the entire subclavian vein is limited by its passage deep to the clavicle or may be impeded by dressings or subcutaneous emphysema after insertion of a central venous catheter. Both the right and left brachiocephalic veins are relatively inaccessible to direct insonation, but the left vein is particularly inaccessible because of its retromanubrial course. Sensitivities reported for the detection of subclavian venous thrombus range from 55% to 100% (11–13). False-negative results in these studies were usually associated with thrombus in the distal subclavian vein, which cannot be directly insolated. In one study, the false-negative rate was 45% with all of these findings due to thrombus in the distal left subclavian vein (13). Therefore, previous authors (1,12,14) have not considered US reliable for the diagnosis of thrombus in the distal subclavian or brachiocephalic veins, or they have recommended that a negative US study be followed up with phlebography (12).

Findings in the current study indicate that the demonstration of normal cardiac pulsatility and respiratory phasicity in the accessible venous segment excludes thrombus in the inaccessible medial venous segments. (Sensitivity and specificity were 100% in 29 studies.)

Loss of cardiac pulsatility is a more sensitive predictor of venous obstruction than is reduced respiratory phasicity. If absent or damped pulsatility is used as the only parameter, sensitivity, specificity, and positive predictive value are each 100%. If decreased or absent respiratory phasicity is used either alone or in conjunction with diminished pulsatility, sensitivity is reduced to 75%, specificity remains 100%, and positive predictive value decreases to 91%. Neither changes in head position nor the presence of a central venous catheter in the insonated vein produced any false-positive Doppler US studies. The phenomenon of retrograde venous flow is insensitive for the diagnosis of occlusion, and it was not seen in our 12 patients with phlebographically proved thrombosis. Flow in the accessible subclavian or jugular veins was always anterograde.

There are several limitations to the present study. Pulsatility and phasicity are not absolute quantitative characteristics, and they vary in patients depending on factors such as the state of hydration. Nevertheless, an experienced sonologist was able to accurately judge whether these Doppler signs were normal, absent, or damped. Another limitation is that the sonologist was far more confident about diagnosis or exclusion of an abnormality since there was a normal unoccluded side for comparison. Although no bilateral occlusions were seen in any of our patients, it is possible that subtle damping of pulsatility or phasicity may be difficult to appreciate in the setting of bilateral or superior vena cava occlusions. We did not see partial or recanalized occlusions and, therefore, are unable to comment on potential changes in the Doppler waveform, but we acknowledge that a false-negative result is a possibility.

Our current policy when we insert a central venous catheter with US guidance is to perform a Doppler examination before the procedure. A vein is considered to be distally occluded if there is loss or damping of cardiac pulsatility or respiratory phasicity, and performance of phlebography is not necessary. If possible, another site will be chosen that has normal Doppler waveforms. Furthermore, our decision to perform anticoagulation is based on the Doppler findings without phlebography, which is reserved for rare cases in which Doppler findings are equivocal, such as normal respiratory phasicity but absent cardiac pulsatility, or in which clinical signs are extremely suggestive of venous occlusion in the upper arm or superior vena cava but Doppler findings are normal. It may be helpful for sonologists to undertake initial studies in conjunction with phlebography until adequate confidence is gained in the observation of normal and abnormal Doppler waveforms.

	Footnotes

 
Author contributions: Guarantors of integrity of entire study, M.C.P., L.H.B.; study concepts and design, M.C.P., L.H.B.; definition of intellectual content, all authors; literature research, M.C.P.; clinical studies, all authors; data acquisition, all authors; statistical analysis, M.C.P.; manuscript preparation, M.C.P., L.H.B.; manuscript editing and review, all authors.

	References

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