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Subclavian Steal Syndrome: Diagnosis with Perfusion Metrics from Contrast-enhanced MR Angiographic Bolus-timing Examination—Initial Experience¹

¹ From the Department of Radiology, New York University School of Medicine, 550 First Ave, New York, NY 10016. Received April 20, 2004; revision requested June 29; revision received July 23; accepted August 20. Address correspondence to C.W. (e-mail: cw262@med.nyu.edu).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: To retrospectively determine whether differential temporal changes in signal intensity of the vertebral arteries, measured at a bolus-timing examination with a test dose of a gadolinium-based contrast agent, are present in patients with subclavian steal syndrome.

MATERIALS AND METHODS: Institutional review board exemption was obtained, and informed consent was not required for this retrospective study. The study complied with the Health Insurance Portability and Accountability Act. Twenty-five patients with known or clinically suspected atherosclerotic disease of the aortic arch and branch vessels underwent breath-hold contrast material–enhanced magnetic resonance (MR) angiography with circulation time derived from a timing examination by using a test bolus of a gadolinium-based contrast agent. Eight patients (three men and five women aged 54–80 years; mean, 70 years) had subclavian stenosis or occlusion with retrograde vertebral artery flow confirmed with time-of-flight MR angiography, nine patients (eight men and one woman aged 31–91 years; mean, 70 years) had mild to severe ostial stenosis of a single vertebral artery, and eight patients (including four men and four women aged 53–86 years; mean, 73 years) had normal vertebral arteries. The difference in time to peak signal intensity between the right and left vertebral arteries was compared among the three groups by using Fisher exact and Cochran–Mantel-Haenszel tests.

RESULTS: The delay in peak enhancement in the ipsilateral vertebral artery ranged from 2 to 4 seconds (mean, 2.5 seconds) in all eight patients with subclavian steal syndrome. In eight of nine patients with ostial vertebral artery stenosis and eight controls, both vertebral arteries filled simultaneously. The presence of unilateral delayed vertebral artery enhancement was significantly associated with retrograde flow in patients with subclavian steal syndrome, compared with patients with normal flow (P < .01) and those with ostial vertebral artery stenosis (P < .01).

CONCLUSION: A bolus-timing examination performed with a test bolus of the gadolinium-based contrast agent via the neck vessels that demonstrates at least a 2-second delay in peak contrast enhancement in the right or left vertebral arteries may, in the appropriate clinical setting, indicate subclavian steal syndrome.

© RSNA, 2005

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
The term subclavian steal describes a vascular disorder in which occlusion or stenosis of the subclavian artery or the brachiocephalic trunk proximal to the vertebral artery origin causes altered vascular hemodynamics that result in low-velocity and/or retrograde flow in the ipsilateral vertebral artery distal to the subclavian artery narrowing (1–5). The vertebralartery effectively steals blood from the posterior cerebral circulation. Subclavian steal syndrome may be manifested clinically by arm claudication or hand numbness and a decrease of at least 20 mm Hg in blood pressure in the upper limb on the affected side, symptoms that may be exacerbated by exercise of the ipsilateral upper limb. Cerebral symptoms may involve nonhemispheric regions of the brain and may lead to dizziness, vertigo, and visual disturbances.

Historically, the reference standard for the definitive diagnosis of subclavian steal syndrome was demonstration of vertebral artery blood flow reversal at invasive angiography, which can also depict narrowing in the subclavian artery or the brachiocephalic trunk. Noninvasive continuous-wave Doppler ultrasonography (US) of the neck can help to determine the direction of flow in the vertebral artery but cannot reliably image the proximal intrathoracic subclavian artery (4–6). In addition, evaluation of the vertebral arteries with duplex US may be difficult in obese patients and requires skilled technicians (7,8).

Several studies have shown the utility of magnetic resonance (MR) angiography for the effective and noninvasive diagnosis of subclavian steal syndrome (7,9–12). Several MR angiography techniques that have been described in the literature can demonstrate the reversal of flow in a vertebral artery. These include two-dimensional time-of-flight MR imaging with a selective presaturation pulse applied first above and then below the volume of interest. Phase-contrast MR imaging can also be used to detect reversal of flow, but the images may be degraded by susceptibility effects or aliasing artifact. More recently, three-dimensional contrast material–enhanced MR angiography has been used to evaluate the proximal aortic arch vessels as well as the vertebral arteries (2). However, while this technique can be used to evaluate the vertebral arteries for stenosis and occlusion, it cannot be used to directly determine flow direction.

A bolus-timing examination with a test-bolus injection is widely used to optimize contrast-enhanced MR angiography, is easy to interpret, and is not vendor specific (13,14). When performing MR angiography in the transverse plane at the level of the neck vessels, we noticed a delay in peak vertebral artery enhancement, compared with that in the contralateral vertebral artery, in patients with occlusive disease of the subclavian artery or the brachiocephalic trunk. We hypothesized that this delay might be due to retrograde vertebral artery flow. Thus, the purpose of our study was to retrospectively determine whether differential temporal changes in signal intensity of the vertebral arteries, measured at a bolus-timing examination with a test dose of a gadolinium-based contrast agent, are present in subclavian steal syndrome.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Patients
We retrospectively searched an MR database at our institution by using the terms subclavian steal, vertebral artery stenosis, and normal aortic arch, which yielded records of 30, 68, and 138 patients, respectively. Twenty-two of 30 patients with subclavian steal syndrome were excluded because the bolus-timing examination was performed at a level inferior to the origins of the vertebral arteries (at the level of the aortic arch). This left a total of eight patients, three men and five women aged 54–80 years (mean, 70 years), in whom subclavian artery stenosis or occlusion was depicted at three-dimensional contrast-enhanced MR angiography with ipsilateral retrograde vertebral artery flow and confirmed at two-dimensional time-of-flight MR angiography. Of these eight patients, one had mild (<50%) stenosis, four had severe (>75%) stenosis, and three had occlusion of the subclavian artery determined with electronic caliper measurements at prospective image interpretation. Another nine consecutive patients, including eight men and one woman aged 31–91 years (mean, 70 years), who had unilateral vertebral artery stenosis and bilateral antegrade vertebral artery blood flow demonstrated at two-dimensional time-of-flight MR angiography, were selected as a control group. Of these nine patients, two had mild (<50%) stenosis, four had moderate (50%–75%) stenosis, and three had severe (>75%) stenosis of a single vertebral artery. Another group of eight consecutive patients, including four men and four women aged 53–86 years (mean, 73 years) who had no lesion in any of the aortic arch or proximal cervical vessels, were selected as the normal-aortic-arch control group; four of these patients, however, had unilateral internal carotid artery disease. Age distributions according to sex are reported in Table 1. Institutional review board exemption was obtained, and informed consent was not required for the retrospective study. Our study complied with the Health Insurance Portability and Accountability Act.

After a localizer sequence was applied, a timing examination to measure circulation time from the antecubital vein to the common carotid artery was performed with breath holding at end expiration. In each patient, a 1-mL test bolus of gadopentetate dimeglumine (Magnevist; Berlex Laboratories, Wayne, NJ), followed by 20 mL saline, was infused at 2 mL/sec by using an MR-compatible injector (Spectris MR Injector SBT 200; MEDRAD, Pittsburgh, Pa). During the infusion of contrast material and the saline flush, a transverse magnetization-prepared turbo fast low-angle shot sequence (repetition time msec/echo time msec/inversion time msec, 500/1.3–4.2/260–300; flip angle, 20°–25°; section thickness, 10 mm) was applied in a single location at the middle level in the neck, below the carotid bifurcation, every second for 30–60 seconds. The field of view and matrix were 30 cm and 128 x 256, respectively. The turbo fast low-angle shot sequence was used because unenhanced blood yields low signal intensity, thereby minimizing flow-related enhancement. Data acquisition for the bolus-timing examination commenced at the same time. Breath-hold contrast-enhanced three-dimensional MR angiography of the aortic arch and neck vessels was subsequently performed during end expiration, by using the circulation time derived from the bolus-timing examination.

Analysis of Images Obtained during Bolus Timing
To determine the time to peak arterial contrast enhancement, circular regions of interest were manually drawn over both the common carotid and vertebral arteries by a single reader (C.W., 1 year of experience with MR angiography) who was not involved in any of the clinical studies. The regions of interest were of a fixed size (10 pixels) and shape (circle). An additional region of interest was placed over skeletal muscle in the neck to serve as background.

Data and Statistical Analysis
Signal intensity values that were measured and reported automatically by the workstation software supplied by the MR imager manufacturer (Syngo; Siemens) were recorded for the entire duration of the timing examination. Signal intensity values for the arteries were divided by the value for the adjacent musculature, to obtain values that were corrected for background. The MR angiographic data recorded for every subject consisted of the time to peak signal intensity (TP) in the left and right vertebral arteries (denoted as TP_VL and TP_VR, respectively) and in the left and right common carotid arteries (TP_CL and TP_CR, respectively). Delay in time to peak signal intensity between vertebral arteries (DV) was calculated for each subject as DV = TP_VL – TP_VR, and delay in time to peak signal intensity between carotid arteries (DC), as DC = TP_CL – TP_CR. For the eight patients with subclavian steal syndrome, the recorded data also included the peak signal intensities achieved in the vertebral arteries ipsilateral and contralateral to the subclavian artery narrowing (PI_i, PI_c). Relative peak signal intensity (RPI) in the vertebral artery ipsilateral to the stenosed subclavian artery was calculated as a percentage of the peak signal intensity in the contralateral vertebral artery, as RPI = (PI_i/PI_c) · 100.

The Mann-Whitney test was used to assess age differences between the sexes or between patients with a delay in time to peak signal intensity and patients without such a delay. Sex differences with respect to vertebral and carotid artery delays to peak enhancement were assessed by using both the Mann-Whitney and the Fisher exact tests: The Mann-Whitney test was used to test actual values of delays in the vertebral and carotid arteries; the Fisher exact test was used to assess results in the vertebral and carotid arteries that were encoded as 0 (negative delay) or as greater than 0 (positive delay). Subject groups defined in terms of clinical status (presence of subclavian steal syndrome, presence of vertebral artery stenosis, or control) were compared with respect to distribution of the sexes by using the Fisher exact test and with respect to age distribution by using the Kruskal-Wallis test. There was no significant association of subject age or sex with either clinical status or delay in time to peak enhancement. However, because the association of sex with clinical status approached statistical significance, even though the study had low statistical power to detect differences according to sex, the analyses to assess the association of clinical status with delay in time to peak signal intensity were conducted both with and without control for the potential confounding effect of sex. Specifically, the Fisher exact test and the Cochran–Mantel-Haenszel test were used to evaluate the data for an association between clinical status and positive delay in time to peak signal intensity without adjustment for sex and with adjustment for sex, respectively. Spearman rank correlation coefficients were used to assess the associations between delay in time to peak enhancement in the vertebral arteries and time to peak enhancement values measured in the ipsilateral and contralateral vertebral arteries, relative peak signal intensity, and subject age in the group of patients with subclavian steal syndrome. All statistical analyses were conducted by using software (SAS for Windows, version 9.0; SAS Institute, Cary, NC). Each reported P value is two sided and is preceded by the name of the statistical test used to obtain it. Results were declared statistically significant with a two-sided significance level () of .05 (ie, P < .05).

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Time to Peak Enhancement
In all eight patients with subclavian steal syndrome, a discrepancy in time to peak signal intensity was found between the left and right vertebral arteries (Table 2). The average delay in vertebral artery peak enhancement in patients with subclavian steal syndrome was 2.5 seconds (range, 2–4 seconds), and the delay was always seen in the vessel ipsilateral to the diseased subclavian artery (Fig 1, Table 2). In one of the nine patients in the group with vertebral artery stenosis, a difference in time to peak enhancement was found between the vertebral arteries (Table 3). In this patient, there was a 1-second delay in peak signal intensity in the right vertebral artery compared with the time to peak signal intensity in the left vertebral artery, which was moderately stenosed. None of the eight patients in the normal-aortic-arch (control) group had a delay in peak enhancement in a vertebral artery (Fig 2).

View larger version (114K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. Left-sided subclavian steal in 67-year-old woman. (a) Thin maximum intensity projection coronal image from three-dimensional contrast-enhanced MR angiography of aortic arch and great vessels demonstrates occlusion (arrow) of the proximal left subclavian artery and a normal-appearing left vertebral artery (arrowhead) that originates from the left subclavian artery. (b) Transverse image from two-dimensional time-of-flight MR angiography (27/6.5; flip angle, 35°) of the neck vessels, with a presaturation band placed above the volume of interest, shows normal signal intensity in the common carotid arteries (arrowheads) and right vertebral artery (long arrow). There is no signal in the left vertebral artery (short arrow), a finding that indicates either occlusion or retrograde flow. (c) Transverse image from two-dimensional time-of-flight MR angiography (27/6.5; flip angle, 35°) of the neck vessels, with a presaturation band placed below the volume of interest, shows normal signal intensity of blood flowing in the internal jugular veins (arrowheads). As expected, there is no signal in the right vertebral artery (long arrow), whereas signal in the left vertebral artery (short arrow) indicates retrograde flow. Note that the signal in the left vertebral artery is weaker than that in the right vertebral artery in b. (d) Transverse image from bolus-timing examination (500/1.8/260; flip angle, 20°) in the neck vessels, acquired at the time of peak signal intensity in the right vertebral artery (t = 16 seconds), shows no contrast enhancement of the left vertebral artery (short arrow), while both common carotid arteries (arrowheads) and the right vertebral artery (long arrow) are enhanced. (e) Transverse image from bolus-timing examination in the neck vessels, obtained 2 seconds later than d (t = 18 seconds), shows delayed contrast enhancement in the left vertebral artery (short arrow) and residual enhancement in the common carotid arteries (arrowheads) and right vertebral artery (long arrow). Note that the left vertebral artery is enhanced to a lesser degree than is the right vertebral artery in d. (f) Signal intensity-time curve for vertebral artery enhancement, derived from bolus-timing examination, shows 2-second delay in peak arterial enhancement in the left vertebral artery (LVA) (t = 18 seconds) compared with that in the right vertebral artery (RVA) (t = 16 seconds). Peak signal intensity in the left vertebral artery is also decreased (parvus tardus) when compared with that in the right vertebral artery in c and e.

View larger version (122K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. Left-sided subclavian steal in 67-year-old woman. (a) Thin maximum intensity projection coronal image from three-dimensional contrast-enhanced MR angiography of aortic arch and great vessels demonstrates occlusion (arrow) of the proximal left subclavian artery and a normal-appearing left vertebral artery (arrowhead) that originates from the left subclavian artery. (b) Transverse image from two-dimensional time-of-flight MR angiography (27/6.5; flip angle, 35°) of the neck vessels, with a presaturation band placed above the volume of interest, shows normal signal intensity in the common carotid arteries (arrowheads) and right vertebral artery (long arrow). There is no signal in the left vertebral artery (short arrow), a finding that indicates either occlusion or retrograde flow. (c) Transverse image from two-dimensional time-of-flight MR angiography (27/6.5; flip angle, 35°) of the neck vessels, with a presaturation band placed below the volume of interest, shows normal signal intensity of blood flowing in the internal jugular veins (arrowheads). As expected, there is no signal in the right vertebral artery (long arrow), whereas signal in the left vertebral artery (short arrow) indicates retrograde flow. Note that the signal in the left vertebral artery is weaker than that in the right vertebral artery in b. (d) Transverse image from bolus-timing examination (500/1.8/260; flip angle, 20°) in the neck vessels, acquired at the time of peak signal intensity in the right vertebral artery (t = 16 seconds), shows no contrast enhancement of the left vertebral artery (short arrow), while both common carotid arteries (arrowheads) and the right vertebral artery (long arrow) are enhanced. (e) Transverse image from bolus-timing examination in the neck vessels, obtained 2 seconds later than d (t = 18 seconds), shows delayed contrast enhancement in the left vertebral artery (short arrow) and residual enhancement in the common carotid arteries (arrowheads) and right vertebral artery (long arrow). Note that the left vertebral artery is enhanced to a lesser degree than is the right vertebral artery in d. (f) Signal intensity-time curve for vertebral artery enhancement, derived from bolus-timing examination, shows 2-second delay in peak arterial enhancement in the left vertebral artery (LVA) (t = 18 seconds) compared with that in the right vertebral artery (RVA) (t = 16 seconds). Peak signal intensity in the left vertebral artery is also decreased (parvus tardus) when compared with that in the right vertebral artery in c and e.

View larger version (140K): [in this window] [in a new window] [Download PPT slide]   Figure 1c. Left-sided subclavian steal in 67-year-old woman. (a) Thin maximum intensity projection coronal image from three-dimensional contrast-enhanced MR angiography of aortic arch and great vessels demonstrates occlusion (arrow) of the proximal left subclavian artery and a normal-appearing left vertebral artery (arrowhead) that originates from the left subclavian artery. (b) Transverse image from two-dimensional time-of-flight MR angiography (27/6.5; flip angle, 35°) of the neck vessels, with a presaturation band placed above the volume of interest, shows normal signal intensity in the common carotid arteries (arrowheads) and right vertebral artery (long arrow). There is no signal in the left vertebral artery (short arrow), a finding that indicates either occlusion or retrograde flow. (c) Transverse image from two-dimensional time-of-flight MR angiography (27/6.5; flip angle, 35°) of the neck vessels, with a presaturation band placed below the volume of interest, shows normal signal intensity of blood flowing in the internal jugular veins (arrowheads). As expected, there is no signal in the right vertebral artery (long arrow), whereas signal in the left vertebral artery (short arrow) indicates retrograde flow. Note that the signal in the left vertebral artery is weaker than that in the right vertebral artery in b. (d) Transverse image from bolus-timing examination (500/1.8/260; flip angle, 20°) in the neck vessels, acquired at the time of peak signal intensity in the right vertebral artery (t = 16 seconds), shows no contrast enhancement of the left vertebral artery (short arrow), while both common carotid arteries (arrowheads) and the right vertebral artery (long arrow) are enhanced. (e) Transverse image from bolus-timing examination in the neck vessels, obtained 2 seconds later than d (t = 18 seconds), shows delayed contrast enhancement in the left vertebral artery (short arrow) and residual enhancement in the common carotid arteries (arrowheads) and right vertebral artery (long arrow). Note that the left vertebral artery is enhanced to a lesser degree than is the right vertebral artery in d. (f) Signal intensity-time curve for vertebral artery enhancement, derived from bolus-timing examination, shows 2-second delay in peak arterial enhancement in the left vertebral artery (LVA) (t = 18 seconds) compared with that in the right vertebral artery (RVA) (t = 16 seconds). Peak signal intensity in the left vertebral artery is also decreased (parvus tardus) when compared with that in the right vertebral artery in c and e.

View larger version (133K): [in this window] [in a new window] [Download PPT slide]   Figure 1d. Left-sided subclavian steal in 67-year-old woman. (a) Thin maximum intensity projection coronal image from three-dimensional contrast-enhanced MR angiography of aortic arch and great vessels demonstrates occlusion (arrow) of the proximal left subclavian artery and a normal-appearing left vertebral artery (arrowhead) that originates from the left subclavian artery. (b) Transverse image from two-dimensional time-of-flight MR angiography (27/6.5; flip angle, 35°) of the neck vessels, with a presaturation band placed above the volume of interest, shows normal signal intensity in the common carotid arteries (arrowheads) and right vertebral artery (long arrow). There is no signal in the left vertebral artery (short arrow), a finding that indicates either occlusion or retrograde flow. (c) Transverse image from two-dimensional time-of-flight MR angiography (27/6.5; flip angle, 35°) of the neck vessels, with a presaturation band placed below the volume of interest, shows normal signal intensity of blood flowing in the internal jugular veins (arrowheads). As expected, there is no signal in the right vertebral artery (long arrow), whereas signal in the left vertebral artery (short arrow) indicates retrograde flow. Note that the signal in the left vertebral artery is weaker than that in the right vertebral artery in b. (d) Transverse image from bolus-timing examination (500/1.8/260; flip angle, 20°) in the neck vessels, acquired at the time of peak signal intensity in the right vertebral artery (t = 16 seconds), shows no contrast enhancement of the left vertebral artery (short arrow), while both common carotid arteries (arrowheads) and the right vertebral artery (long arrow) are enhanced. (e) Transverse image from bolus-timing examination in the neck vessels, obtained 2 seconds later than d (t = 18 seconds), shows delayed contrast enhancement in the left vertebral artery (short arrow) and residual enhancement in the common carotid arteries (arrowheads) and right vertebral artery (long arrow). Note that the left vertebral artery is enhanced to a lesser degree than is the right vertebral artery in d. (f) Signal intensity-time curve for vertebral artery enhancement, derived from bolus-timing examination, shows 2-second delay in peak arterial enhancement in the left vertebral artery (LVA) (t = 18 seconds) compared with that in the right vertebral artery (RVA) (t = 16 seconds). Peak signal intensity in the left vertebral artery is also decreased (parvus tardus) when compared with that in the right vertebral artery in c and e.

View larger version (131K): [in this window] [in a new window] [Download PPT slide]   Figure 1e. Left-sided subclavian steal in 67-year-old woman. (a) Thin maximum intensity projection coronal image from three-dimensional contrast-enhanced MR angiography of aortic arch and great vessels demonstrates occlusion (arrow) of the proximal left subclavian artery and a normal-appearing left vertebral artery (arrowhead) that originates from the left subclavian artery. (b) Transverse image from two-dimensional time-of-flight MR angiography (27/6.5; flip angle, 35°) of the neck vessels, with a presaturation band placed above the volume of interest, shows normal signal intensity in the common carotid arteries (arrowheads) and right vertebral artery (long arrow). There is no signal in the left vertebral artery (short arrow), a finding that indicates either occlusion or retrograde flow. (c) Transverse image from two-dimensional time-of-flight MR angiography (27/6.5; flip angle, 35°) of the neck vessels, with a presaturation band placed below the volume of interest, shows normal signal intensity of blood flowing in the internal jugular veins (arrowheads). As expected, there is no signal in the right vertebral artery (long arrow), whereas signal in the left vertebral artery (short arrow) indicates retrograde flow. Note that the signal in the left vertebral artery is weaker than that in the right vertebral artery in b. (d) Transverse image from bolus-timing examination (500/1.8/260; flip angle, 20°) in the neck vessels, acquired at the time of peak signal intensity in the right vertebral artery (t = 16 seconds), shows no contrast enhancement of the left vertebral artery (short arrow), while both common carotid arteries (arrowheads) and the right vertebral artery (long arrow) are enhanced. (e) Transverse image from bolus-timing examination in the neck vessels, obtained 2 seconds later than d (t = 18 seconds), shows delayed contrast enhancement in the left vertebral artery (short arrow) and residual enhancement in the common carotid arteries (arrowheads) and right vertebral artery (long arrow). Note that the left vertebral artery is enhanced to a lesser degree than is the right vertebral artery in d. (f) Signal intensity-time curve for vertebral artery enhancement, derived from bolus-timing examination, shows 2-second delay in peak arterial enhancement in the left vertebral artery (LVA) (t = 18 seconds) compared with that in the right vertebral artery (RVA) (t = 16 seconds). Peak signal intensity in the left vertebral artery is also decreased (parvus tardus) when compared with that in the right vertebral artery in c and e.

View larger version (18K): [in this window] [in a new window] [Download PPT slide]   Figure 1f. Left-sided subclavian steal in 67-year-old woman. (a) Thin maximum intensity projection coronal image from three-dimensional contrast-enhanced MR angiography of aortic arch and great vessels demonstrates occlusion (arrow) of the proximal left subclavian artery and a normal-appearing left vertebral artery (arrowhead) that originates from the left subclavian artery. (b) Transverse image from two-dimensional time-of-flight MR angiography (27/6.5; flip angle, 35°) of the neck vessels, with a presaturation band placed above the volume of interest, shows normal signal intensity in the common carotid arteries (arrowheads) and right vertebral artery (long arrow). There is no signal in the left vertebral artery (short arrow), a finding that indicates either occlusion or retrograde flow. (c) Transverse image from two-dimensional time-of-flight MR angiography (27/6.5; flip angle, 35°) of the neck vessels, with a presaturation band placed below the volume of interest, shows normal signal intensity of blood flowing in the internal jugular veins (arrowheads). As expected, there is no signal in the right vertebral artery (long arrow), whereas signal in the left vertebral artery (short arrow) indicates retrograde flow. Note that the signal in the left vertebral artery is weaker than that in the right vertebral artery in b. (d) Transverse image from bolus-timing examination (500/1.8/260; flip angle, 20°) in the neck vessels, acquired at the time of peak signal intensity in the right vertebral artery (t = 16 seconds), shows no contrast enhancement of the left vertebral artery (short arrow), while both common carotid arteries (arrowheads) and the right vertebral artery (long arrow) are enhanced. (e) Transverse image from bolus-timing examination in the neck vessels, obtained 2 seconds later than d (t = 18 seconds), shows delayed contrast enhancement in the left vertebral artery (short arrow) and residual enhancement in the common carotid arteries (arrowheads) and right vertebral artery (long arrow). Note that the left vertebral artery is enhanced to a lesser degree than is the right vertebral artery in d. (f) Signal intensity-time curve for vertebral artery enhancement, derived from bolus-timing examination, shows 2-second delay in peak arterial enhancement in the left vertebral artery (LVA) (t = 18 seconds) compared with that in the right vertebral artery (RVA) (t = 16 seconds). Peak signal intensity in the left vertebral artery is also decreased (parvus tardus) when compared with that in the right vertebral artery in c and e.

View larger version (105K): [in this window] [in a new window] [Download PPT slide]   Figure 2. Transverse image from bolus-timing examination (500/1.8/260; flip angle, 20°) in a 53-year-old man with normal blood flow through the aortic arch and great vessels demonstrates simultaneous peak enhancement bilaterally of common carotid arteries (arrowheads) and vertebral arteries (arrows).

Correlations
In the group of patients with subclavian steal, there were no significant correlations (Spearman correlation, P > .28) between patient age and delay in peak enhancement in vertebral arteries (r = 0.192), relative peak signal intensity (r = 0.152), or time to peak enhancement in the contralateral (r = 0.339) and ipsilateral (r = 0.436) vertebral arteries. In six of eight patients with subclavian steal, there was a concomitant decrease of more than 20% (range, 20.4%–45.6%) in peak signal intensity in vertebral arteries in the affected side, compared with that in the contralateral vertebral arteries (parvus tardus phenomenon) (Table 2, Fig 1e).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Gadolinium-based contrast-enhanced three-dimensional MR angiography is widely performed for simultaneous evaluation of the aortic arch vessels and carotid arteries (13–18). Methods used to optimize selective arterial enhancement include a timing examination (13,14), MR fluoroscopy (17), automated bolus detection schemes (19), and time-resolved imaging (20). The benefit of a bolus-timing examination is that it can be performed with any MR imager, without proprietary software or additional software expense. We exploited the utility of this examination for gathering physiologic information regarding flow characteristics in the vertebral arteries in patients with and without subclavian steal syndrome.

Our study demonstrated a delay of at least 2 seconds in time to peak arterial enhancement in the vertebral artery ipsilateral to the side of subclavian steal in all patients with subclavian steal syndrome. This finding was not seen in patients with vertebral artery stenosis or those with normal vertebral arteries, and, therefore, the finding had 100% specificity for the diagnosis of subclavian steal syndrome.

The delay to peak enhancement was presumably due to increased bolus transit time, which in turn was caused by retrograde flow. We also noticed a concomitant decrease in peak vertebral arterial signal intensity in the affected side compared with that in the contralateral side in six (75%) of eight patients, which indicates a relative reduction of blood flow through the vertebral artery ipsilateral to the diseased subclavian artery. These findings are consistent with those in early experiments by Reivich et al (3), who used angiography and intraoperative flowmeters to demonstrate that retrograde vertebral arterial flow in patients with subclavian steal syndrome is decreased both in rate and in volume.

In our study patients with vertebral artery stenosis, a difference in time to peak enhancement was found in only one (11%) of nine patients. In this patient, the time to peak signal intensity in the stenotic vertebral artery was 1 second earlier than that in the contralateral vessel. This occurrence can be explained by the observation in prior US studies (6,21) that hemodynamic changes lead to increased flow velocity and earlier peak enhancement even in vessels with moderate stenosis. Conversely, the degree of stenosis may be so severe as to impede blood flow (as with stenoses that cause a reduction of 75% or more in the vessel cross-sectional area) or, in cases of occlusion, completely eliminate it (6). This phenomenon was not seen in our study, but we cannot exclude the possibility that severe stenoses may cause a delay in the time to peak signal intensity. Images from the patients in the control group demonstrated no significant differences in the time to peak signal intensity in the two vertebral arteries, and this finding indicates that equivalent circulation times may be expected through both vessels.

This study had several recognized limitations, including a retrospective design and a small number of patients. We attempted to minimize bias by consecutively selecting patients for each of the three study groups from our hospital database. Finally, we did not have conventional angiographic images for correlation with MR angiograms. However, breath-hold contrast-enhanced three-dimensional MR angiography has been accepted as a reliable test for evaluation of the great vessels and is currently the modality of choice at many institutions.

In conclusion, a bolus-timing examination in the neck vessels during which a difference of 2 seconds or more is observed between the times to peak enhancement in the vertebral arteries may indicate subclavian steal syndrome in the appropriate clinical setting. The absence of such a difference in time to peak enhancement probably excludes this diagnosis. In addition, this technique has potential for postoperative follow-up. Restoration of antegrade blood flow in the affected vertebral artery, seen as a disappearance of the delay in the time to peak signal intensity, would suggest successful correction of the syndrome. With the increasing use of MR angiography in imaging of vascular disorders, the bolus-timing examination can function as a supplemental tool for diagnosis or confirmation of subclavian steal syndrome.

	FOOTNOTES

 
² Current address: J.Z., Department of Radiology, Memorial Sloan-Kettering Cancer Center, New York, NY; G.A.K., Department of Radiology, Valley Hospital, Ridgewood, NJ.

Authors stated no financial relationship to disclose.

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

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 

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