REVIEW ARTICLE Duplex Ultrasonography of Vertebral and Subclavian Arteries Vijay G. Kalaria, MD, FACC, FSCAI, Sony Jacob, MD, William Irwin, RVT, and Robert M. Schainfeld, DO, Indianapolis, Indiana, and Boston, Massachusetts Duplex ultrasonography of the vertebral artery is an integral part of extracranial cerebrovascular screening and provides noninvasive diagnostic clues for subclavian or vertebral artery stenosis. This review describes technique for the ultrasound examination of the vertebral and subclavian arteries. Duplex images from various patients are used to illustrate a spectrum of hemodynamic changes that occur in the vertebral artery Doppler signal caused by subclavian artery stenosis and subclavian vertebral steal. (J Am Soc Echocardiogr 2005;18:1107-1111.) Hemodynamically significant subclavian artery stenosis (subclavian steal syndrome) may manifest clinically as ipsilateral arm claudication, arm numbness, vertebrobasilar symptoms, 1 or cardiac ischemia (in patients with a left internal mammary artery bypass graft). Duplex ultrasonography of the vertebral artery is an integral part of extracranial cerebrovascular noninvasive screening and provides diagnostic clues for subclavian or vertebral artery stenosis. Competing flow from the ipsilateral subclavian artery and contralateral vertebral artery by the circle of Willis lead to an alteration in the Doppler velocity profile of the ipsilateral vertebral artery. TECHNIQUES From the Krannert Institute of Cardiology, Indiana University, and St Elizabeth s Medical Center, Tufts University School of Medicine, Boston, Massachusetts (W.I., R.M.S.). Reprint requests: Vijay G. Kalaria, MD, FACC, FSCAI, Vascular Interventions, Krannert Institute of Cardiology, Indiana University School of Medicine, Clarian Cardiovascular Center, E404, 1800 N Capitol Ave, Indianapolis, IN 46202 (E-mail: vkalaria@ iupui.edu). 0894-7317/$30.00 Copyright 2005 by the American Society of Echocardiography. doi:10.1016/j.echo.2005.06.005 Vertebral Artery Duplex Examination Vertebral artery duplex examination is carried out in a supine position with the patient s head turned to the side and angling the ultrasound probe laterally from the carotid artery. A linear transducer with 4- to 8-MHz frequency capabilities is commonly used to examine the extracranial vasculature. Vertebral artery, the first major branch of the subclavian artery, is identified using color Doppler and grayscale imaging coursing between the transverse processes of the cervical spine (Figure 1). In a healthy patient, vertebral artery pulse Doppler velocity profile is conventionally displayed above the baseline (Figure 2). This vessel after following a relatively straight course in the neck for a short distance then enters the C6 vertebra and can be examined in 3 segments (Figure 1): the proximal, pretransverse portion; the intertransverse portion; and the atlas loop. 2 During extracranial cerebrovascular examination the intertransverse portion of vertebral artery is routinely interrogated. Examination of the atlas loop is performed by placing the probe below the mastoid process, lateral to the sternocleidomastoid muscle, and maintaining the probe directed toward the contralateral orbit. While interrogating the origin of the vertebral artery (Figure 2), neck artery branches can be mistaken for the vertebral artery. The soft sounds of an artery supplying a low-resistance cerebral bed and transmitted pulsation obtained by tapping at the mastoid process are useful clues to differentiate the vertebral artery from other subclavian branches. 3 The caliber of vertebral arteries is often variable in many patients with the left vertebral being dominant and larger in up to 25% of patients. 4 Normal vertebral artery flow is antegrade with a steep increase to a peak systolic velocity of 50 cm/s (range: 19-96 cm/s) (Figure 2). 4 Vertebral Artery Duplex Examination with Subclavian Steal The Duplex recordings from several patients illustrating a spectrum of hemodynamic changes in the vertebral artery under varying degrees of subclavian stenosis are portrayed in Figures 3 to 7. Latent subclavian steal manifests as early to midsystolic dip in the vertebral Doppler waveform profile (Figure 3). This is postulated to occur as a high-velocity blood flow jet, created by a proximal ipsilateral subclavian artery lesion that leads to a pressure decrease in the 1107
1108 Kalaria et al October 2005 Figure 3 Latent subclavian steal syndrome (partial stenosis) with early systolic deceleration (dip marked by arrows) is reflected in systolic flow portion of Doppler waveform. Figure 1 Schematic representation of vertebral artery segments and extracranial course. V 0, Ostium; V 1, pretransverse portion; V 2, intertransverse portion; V 3, atlas loop; V 4, intracranial. Figure 4 Latent subclavian steal syndrome with bidirectional systolic flow in ipsilateral vertebral artery. Figure 2 Normal antegrade flow in vertebral artery (above baseline) with Doppler incident angle of 60 degrees to vessel wall. Arrow, Pulse wave Doppler cursor positioned in vertebral artery; body, cervical vertebrae acoustic shadowing. vertebral artery transiently siphoning flow from the feeding contralateral vertebral artery (Figure 3). Such transient, mid- to late-systolic velocity deceleration in the vertebral artery waveform is also termed as a presteal waveform or bunny waveform because of its resemblance to the profile of a rabbit. The depth of this midsystolic dip has been correlated with the severity of subclavian artery stenosis. 5 With an increasing degree of stenosis, the vertebral artery systolic flow becomes bidirectional with a reversal from mid to late systole (Figure 4). Complete subclavian steal results in a retrograde flow pattern in the ipsilateral vertebral artery (Figure 5 and 6). Inflating a blood pressure cuff placed on the ipsilateral arm to suprasystolic pressure allows manipulation of flow direction in the vertebral artery in a suggested case of subclavian steal syndrome (from retrograde to antegrade). Sudden deflation of the blood pressure cuff and subsequent hyperemia accentuates subclavian steal. A latent steal waveform in the vertebral artery can be converted to complete steal waveform using such provocative maneuvers by exaggerating the pressure decrease across the subclavian artery stenosis. 5 Reversal of flow in the
Volume 18 Number 10 Kalaria et al 1109 Figure 5 Progressive subclavian stenosis with systolic flow reversal, antegrade diastolic flow, and overall low-amplitude velocity. Figure 7 Vertebral artery stenosis (ostial or proximal). Slow increasing (tardus) and low amplitude (parvus) pulse Doppler velocity waveform. Figure 6 Hemodynamically significant subclavian artery stenosis showing prominent retrograde systolic flow with no significant diastolic antegrade component. right vertebral artery in patients with ipsilateral innominate artery stenosis or occlusion supplies not only the ipsilateral arm, but also serves as an important collateral supply to the right carotid artery distribution. 6 Above-described changes in the vertebral artery flow secondary to a proximal subclavian or innominate artery stenosis (Figures 3-6) contrast with parvus et tardus vertebral artery Doppler profile (Figure 7) because of ipsilateral ostial or proximal vertebral artery stenosis. Parvus refers to diminished amplitude and rounding of the systolic peak and tardus to delayed or prolonged early systolic acceleration. The relationship between the peak systolic velocity in the vertebral artery and the severity of the vertebral stenosis is not well established. A systolic velocity greater than 100 cm/s or double the peak systolic velocity, as compared with the normal proximal artery, accompanied by disturbed flow pattern (aliasing) is generally suggestive of a hemodynamically significant stenosis. 4 However, in severe ostial vertebral artery stenosis, systolic flow velocities may be significantly impeded (Figure 7). Doppler waveforms are also affected by factors besides arterial stenosis including cardiac conditions such as low cardiac output, valvular heart disease, distal vessel stenosis or occlusion, and stenosis in contralateral or intracerebral vessels. 7 Vertebral artery Duplex changes are frequently diagnosed incidentally during an extracranial carotid ultrasound examination; hence, close correlation with symptoms is warranted before any interventions are performed. 8,9 Subclavian Artery Duplex Examination Technique The subclavian artery is insonated in the supraclavicular fossa. It is vital to keep the Doppler angle of the ultrasound beam as close to 60 degrees as possible to the long axis of the vessel being imaged. A normal Doppler velocity waveform recorded from the proximal subclavian artery is triphasic: a highamplitude systolic component with steep acceleration/deceleration and a clear window beneath the systolic peak; an early diastolic negative signal; and, finally, late diastolic brief forward flow (Figure 8). The third phase of late diastolic forward flow may be absent in certain patients who are older because of vessel stiffness and loss of compliance. With diameter reduction between 0% and 49%, there is focal systolic velocity acceleration and spectral broadening. Ostial or proximal subclavian artery stenosis is classified between 50% to 99% when there is elevated systolic velocity, along with a loss of biphasic waveform (Figure 9), and presence of poststenotic turbulence (aliasing). 10 On Doppler signal, the poststenotic turbulence appears as a bidirectional signal
1110 Kalaria et al October 2005 Figure 8 Normal subclavian artery Duplex waveform. with marked spectral broadening and decreasing velocities, especially as the sample volume is moved distal to the stenosis. 11 Low-amplitude, monophasic waveforms are suggestive of preocclusive subclavian stenosis. Distal waveforms in the upper extremity for patients with a significant proximal stenosis are usually damped and monophasic; although this finding may be present even in certain healthy patients with a low-resistance arm circulation. 12 Dynamic duplex testing with elevated and hyperabducted arm positioning allows differentiation of a fixed atherosclerotic proximal subclavian stenosis from thoracic outlet syndrome. In a recent populationbased study by Shadman et al, 13 subclavian artery stenosis was present in 2% of free-living population with an increased prevalence of 7% in patients with clinical cardiovascular disease. Routine bilateral arm blood pressure measurements allow diagnosis of occult peripheral vascular disease; avoid a false diagnosis of normotension; and complement vertebral artery duplex examination. An interarm systolic pressure difference of greater than 15 mm Hg is usually considered a significant pressure difference. 13 Duplex ultrasonography of the subclavian artery and the vertebral artery can detect stenosis greater than 50% with a moderately high sensitivity (80% range) and an excellent negative predictive value ( 95%). 14 Duplex ultrasonography is also highly useful in clinical follow-up of patients after revascularization procedures. Percutaneous revascularization modalities are currently favored compared with operation in properly selected patients who are symptomatic, as restenosis incidence is low (3%-6% of treated patients 15,16 ). Clinical correlation of hemodynamic findings with symptoms is warranted before any revascularization procedure. Meticulous attention to these patterns demonstrated on the duplex ultrasound of both vertebral and subclavian arteries clarifies the diagnosis of varying degrees of subclavian vertebral steal and allows for the differentiation from vertebral artery stenosis. A prompt and accurate diagnosis and understanding on the physician s part to identify these subtle clues during the noninvasive vascular assessment of these patients is paramount in optimizing their subsequent treatment. REFERENCES Figure 9 Abnormal subclavian artery duplex waveform showing elevated peak systolic velocity, spectral broadening, and loss of triphasic waveform. Arrow, Acoustic bruit signal. 1. Reivich M, Holling HE, Roberts B, et al. Reversal of blood flow through the vertebral artery and its effect on cerebral circulation. N Engl J Med 1961;265:878-85. 2. Sidhu PS. Ultrasound of the carotid and vertebral arteries. Br Med Bull 2000;56:346-66. 3. Hennerici M, Neuerburg-Heusler D. Vascular diagnosis with ultrasound. New York: Thieme; 1998. 4. Trattnig S, Hubsch P, Schuster H, et al. Color-coded Doppler imaging of normal vertebral arteries. Stroke 1990;21:1222-5. 5. Kliewer MA, Hertzberg BS, Kim DH, et al. Vertebral artery Doppler waveform changes indicating subclavian steal physiology. AJR Am J Roentgenol 2000;174:815-9. 6. Roederer GO, Langlois YE, Strandness DEJ. Cerebral arterial flow and cerebral vascular insufficiency. In: Condon RE, Decosse J, editors. Surgical care II. Philadelphia: Lea and Febiger; 1985. p. 199-234. 7. Rohren EM, Kliewer MA, Carroll BA, et al. A spectrum of Doppler waveforms in the carotid and vertebral arteries. AJR Am J Roentgenol 2003;181:1695-704. 8. Hennerici M, Klemm C, Rautenberg W. The subclavian steal phenomenon: a common vascular disorder with rare neurologic deficits. Neurology 1988;38:669-73. 9. Bornstein NM, Norris JW. Subclavian steal: a harmless hemodynamic phenomenon? Lancet 1986;2:303-5. 10. Strandness DE. Upper extremity arterial evaluation. In: Strandness DE, editor. Duplex scanning in vascular disorders. Philadelphia: Lippincott Williams and Wilkins; 2002. p. 267-72. 11. Primozich JF. Extracranial arterial system. In: Strandness DE, editor. Duplex scanning in vascular disorders. Philadelphia: Lippincott Williams and Wilkins; 2002. p. 202-5.
Volume 18 Number 10 Kalaria et al 1111 12. Strandness DE. Hemodynamics of arterial stenosis and occlusion. In: Strandness DE, editor. Duplex scanning in vascular disorders. Philadelphia: Lippincott Williams and Wilkins; 2002. p. 70-1. 13. Shadman R, Criqui MH, Bundens WP, et al. Subclavian artery stenosis: prevalence, risk factors, and association with cardiovascular diseases. J Am Coll Cardiol 2004;44:618-23. 14. Ackerstaff RG, Hoeneveld H, Slowikowski JM, et al. Ultrasonic duplex scanning in atherosclerotic disease of the innominate, subclavian and vertebral arteries: a comparative study with angiography. Ultrasound Med Biol 1984;10:409-18. 15. Al-Mubarak N, Liu MW, Dean LS, et al. Immediate and late outcomes of subclavian artery stenting. Catheter Cardiovasc Interv 1999;46:169-72. 16. Hadjipetrou P, Cox S, Piemonte T, et al. Percutaneous revascularization of atherosclerotic obstruction of aortic arch vessels. J Am Coll Cardiol 1999;33:1238-45.