Subclavian Steal Syndrome

 

INTRODUCTION

Background: Subclavian steal phenomenon (SSP) refers to subclavian artery steno-occlusive disease proximal to the origin of the vertebral artery and is associated with flow reversal in the vertebral artery. While Contorni first described retrograde flow in the vertebral artery in 1960, Reivich in 1961 first recognized the association between this phenomenon and neurologic symptoms. Fisher dubbed this combination of retrograde vertebral flow and neurologic symptoms subclavian steal syndrome (SSS), suggesting that blood is stolen by the ipsilateral vertebral artery from the contralateral vertebral artery. It was later suggested that such "steal" may cause brainstem ischemia and stroke, either continuously or secondary to arm exercise.

The term SSS should be reserved for retrograde vertebral artery flow associated with transient neurologic symptoms related to cerebral ischemia. SSP refers to retrograde flow in the vertebral artery only. First diagnosed angiographically in the early 1960s, SSS is now most commonly diagnosed during Doppler ultrasound (US) examination of the neck arteries.

Pathophysiology: The primary lesion causing vertebral artery flow reversal is proximal subclavian artery stenosis or occlusion, resulting in decreased blood pressure in the arm distal to the steno-occlusive disease. This pressure reduction initially causes ipsilateral vertebral artery blood flow alteration provided the subclavian disease is proximal to the origin of the vertebral artery.

Ultimately, a flow reversal occurs in the ipsilateral vertebral artery as compensatory collateral to the compromised vascular territory beyond the subclavian steno-occlusive lesion. Other potential collateral pathways are those between the external carotid artery (ECA) and the subclavian artery, from the occipital branch of the ECA to the deep cervical branch of the costocervical trunk, and from the superior thyroid artery of the ECA to the inferior thyroid artery branch of the thyrocervical trunk.

Classification of subclavian steal can be defined by territory from which blood is stolen, as described by Vollmar et al. Vollmar recognized 4 types of subclavian steal: vertebro-vertebral, carotid-basilar, external carotid-vertebral, and carotid-subclavian (can only occur with occlusion of brachiocephalic artery). Another classification is based on vertebral artery hemodynamics as described by Branchereau and colleagues. Hemodynamic abnormalities ranged from reduced antegrade vertebral flow (stage I), reversal of flow during reactive hyperemia testing of the arm (stage II), and permanent retrograde vertebral flow (stage III). The 3 stages correlate with disease severity with stage III, usually indicating subclavian artery occlusion.

Arm symptoms may be provoked by an increased blood flow requirement to the compromised upper extremity (eg, during arm exercise or after producing peripheral reactive hyperemia by arm cuff inflation), or, alternatively, by limiting vertebral compensatory flow to the subclavian artery (eg, during neck movements).

Subclavian steno-occlusive disease produces neurologic symptoms when compensatory flow to the subclavian artery from the vertebral artery diverts too much flow toward the arm and away from intracranial structures. The quality of collateral blood supply and the capacity to increase collateral flow to the intracranial circulation (brainstem in particular) may be the principle determinant as to which patient develops neurologic symptomatology.

In times of reversed flow in the vertebral arteries, the most important collateral circulation to the posterior fossa is through the circle of Willis, principally through the posterior communicating artery. In situations where this communication is absent or inadequate, possibly from concurrent extracranial carotid stenoses, increased demand in the ipsilateral upper extremity may cause neurologic symptoms. This is the foundation for the belief that hemodynamically important disease in the cerebral arterial circulation (or vessels supplying that circulation) is a prerequisite of SSS.

Spontaneous resolution of vertebrobasilar symptoms may be related to the establishment of extracranial collaterals to the subclavian circulation.

Frequency:

  • In the US: The Joint Study of Extracranial Arterial Occlusion reported a 17% incidence of subclavian or innominate artery stenosis but angiographic steal occurred in only 2.5% (168/6534) of cases; of those with angiographic steal, 80% had associated extracranial obstructions and 5.3% (9/168) had neurologic symptoms.

    A 6.4% incidence of SSP was observed in 500 asymptomatic patients with neck bruits undergoing Doppler US and subclavian steal test (to provoke vertebral artery flow reversal).

    In 680 symptomatic patients examined with angiography, 23% had severe proximal subclavian disease or occlusion with 6% showing reversed vertebral artery flow.

  • Internationally: Incidence of SSP is 1.3% (324/25,000) in European patients referred for carotid and vertebral artery Doppler US; of these patients, 5% have nonhemispheric neurologic symptoms.

    In the Far East, up to 36% (9/25) of patients undergoing surgical management of SSS have an etiology of Takayasu, with atherosclerosis accounting for the remaining patients. Nonatherosclerotic etiologies are rare in Caucasians.

Mortality/Morbidity: In SSS patients, risk of stroke is poorly documented but seems low. Bornstein and Norris prospectively followed 500 patients for 2-4 years, having documented SSP in 9% (45/500). None of their SSP patients had a stroke during the follow-up period while symptoms developed in 5 patients: 3 had dizzy spells and 2 had numbness of the affected arm at rest. Field et al noted that of 168 patients with vertebral flow reversal, only 5.35% (9/168) had vertebrobasilar symptoms and all of these 9 patients had other lesions that might explain their symptoms.

Despite apparent low stroke risk, patients with SSS may be severely debilitated by episodes of arm and related intracranial ischemia symptoms. Given the differences in survival between medically and surgically treated patients, surgical "prophylaxis" of stroke should be reserved for patients with disabling vertebrobasilar symptoms.

  • The presence of other extracranial arterial disease is a prerequisite to the development of symptoms. The reported incidence of associated extracranial stenotic disease is 24-80%.
  • Neurologic symptoms, when they occur, more likely are related to other extracranial arterial disease than to vertebral artery flow reversal.
  • Ackerman et al described a spontaneous remittence of vertebrobasilar symptoms that occurs in 50% of patients who were initially symptomatic. Only 15% of the initially asymptomatic patients experienced vertebrobasilar transient ischemic attacks during the follow-up period of at least 2 years.

Race: SSS is most frequently described in Caucasians because of increased incidence of atherosclerosis in this population.

In the Far East, as many as 36% (9/25) of patients undergoing surgical management of subclavian steal syndrome have Takayasu arteritis as the etiology, with atherosclerosis accounting for the remaining patients. Nonatherosclerotic etiologies are rare in Caucasians.

Sex: Incidence is greater in males than in females (1.5-2:1). However, when Takayasu arteritis is causative rather than atherosclerosis, there is a female predilection.

Age: SSS usually affects people older than 50 years when the disease is secondary to atherosclerosis while SSS presents far earlier (<30 y in 90%) when Takayasu arteritis is implicated.

Anatomy: The ratio of left-sided to right-sided SSP is 3-4:1; most likely, this relates to turbulence-related atherosclerosis in the proximally more acutely angled left subclavian artery.

In 2% of the population, the left vertebral artery arises directly from the aortic arch; in these patients, severe stenosis or occlusion of the proximal left subclavian artery would not reverse flow in the left vertebral artery (ie, it lacks communication with the subclavian artery).

Classify SSS by the territory from which blood is stolen as follows:

  • Vertebrovertebral

  • Carotid-basilar

  • External carotid-vertebral

  • Carotid-subclavian (occurs only on the right side with right brachiocephalic occlusion)

Coronary-subclavian steal syndrome refers to decreased or reversed internal mammary artery flow, which causes angina related to severe subclavian steno-occlusive disease in patients with in situ internal mammary-to-coronary artery graft.

Clinical Details:

History

Commonly asymptomatic, subclavian artery steno-occlusive disease associated with flow reversal in the ipsilateral vertebral artery is diagnosed as an incidental finding during Doppler US examination of the carotid and vertebral arteries.

Symptoms that occur (eg, dizziness, unsteadiness, vertigo, visual changes) most typically are related to vertebrobasilar and posterior cerebral circulation ischemia.

Arm ischemia occurs, causing arm claudication and rest pain.

SSS can be associated with hemispheric or global cerebral symptoms such as focal sensory or motor loss, dysphasia, and unilateral visual disturbances.

Concomitant carotid or cerebral artery disease is a factor.

Vertebrobasilar symptoms provoked by ipsilateral arm exercise are considered a characteristic, though rare, feature.

Neck movement may provoke symptoms.

In most patients, there is a clear provoking or reproducible event.

Hand ischemia is uncommon in SSS; therefore, consider a different etiology (eg, atheroembolic disease).

The physician often elicits a history of smoking, hypertension, hyperlipidemia, diabetes, and coronary and/or peripheral vascular disease.

Physical

Weak or absent radial and ulnar pulse in the presence of ipsilateral reduced blood pressure (change is >20 mm Hg) when compared to the contralateral arm suggests SSS.

A bruit may be localized to the proximal subclavian artery.

Reactive hyperemia testing (temporary arm cuff inflation above systolic pressure on the side of subclavian disease) can provoke vertebrobasilar symptoms by causing peripheral vasodilation and decreasing peripheral resistance with a resulting sump effect favoring increased flow from the vertebral circulation to the involved upper extremity.

Preferred Examination: Color Doppler US is the preferred examination.

Limitations of Techniques: Color Doppler US is operator-dependent; direct examination of the proximal subclavian is compromised by overlying clavicle, ribs, and sternum.

DIFFERENTIALS

Aorta, Dissection
Arteritis, Giant Cell
Arteritis, Takayasu
Embolization, Vascular Lesions


Other Problems to be Considered:

Causes of subclavian artery stenosis include atherosclerosis, Takayasu arteritis, giant cell arteritis, tumor encasement, trauma, previous surgical procedure
Causes of vertebrobasilar symptoms include cerebellar neoplasm, cerebellar degeneration, multiple sclerosis
Causes of arm symptoms include subclavian artery stenosis, neurologic causes, atheroembolism

 

X-RAY

Findings: No role exists for plain radiographs.


CAT SCAN

Findings: Atheroma-related calcification projected over the proximal subclavian artery may be apparent.

Absence of calcification does not rule out subclavian steno-occlusive disease, nor does the presence of calcification confirm it.

Contrast-enhanced CT scan with helical and multidetector scanners (and 3-D reconstructions) may aid in the diagnosis of subclavian steal steno-occlusive disease.

False Positives/Negatives: Inability to distinguish calcified plaque (which may be iso-dense to contrast) from contrast within the vessel lumen has the potential to compromise estimation of degree of stenosis and occlusion.

 

MRI

Findings: Two-dimensional and 3-dimensional time-of-flight MRA techniques can determine the presence of SSP.

Phase-contrast MRA measures vertebral artery flow direction and velocity.

With head and neck coils, and high-gradient MRI technology, gadolinium-enhanced MRA enables accurate depiction of proximal subclavian artery steno-occlusive disease.

MRA techniques do not require iodinated contrast (and its accompanying nephrotoxic and allergic side effects), but they can be time consuming.

Direct examination of the proximal subclavian artery is compromised by limitations in field of view and respiratory motion.

Lack of widespread availability, claustrophobia, and contraindications to MR (eg, pacemakers) limit MRA use (see Image 4, Image 5).

Degree of Confidence: Further examination is indicated when artifacts are caused by the following:

  • Motion

  • Venous enhancement that obscures arterial structures

  • Signal loss secondary to injection in ipsilateral upper extremity

  • Signal loss secondary to adjacent metallic clips or prostheses

False Positives/Negatives: T2 effects related to ipsilateral injection of gadolinium can cause a pseudo-occlusion appearance of the subclavian artery.

 

ULTRASOUND

Findings: SSP most commonly is diagnosed incidentally during carotid and vertebral artery color Doppler US.

The earliest waveform change associated with subclavian artery stenosis is a transient decrease in ipsilateral vertebral artery midsystolic velocity.

  • With progressive stenosis of the subclavian artery, midsystolic velocity slows further, then reverses direction until both systolic and diastolic flow are reversed.

  • Reactive hyperemia provoked by blood pressure cuff maneuver and arm exercise exaggerates this waveform change (subclavian steal test).
  • Total vertebral artery reversal of flow correlates with severe subclavian artery stenosis or occlusion.

  • Total vertebral flow reversal does not indicate the presence of related neurologic symptoms.

A parvus tardus waveform (prolonged systolic acceleration time with decreased peak systolic velocity) in the distal subclavian artery and brachial artery is expected with severe subclavian stenosis or occlusion; a monophasic waveform also replaces the usual triphasic Doppler signal in these vessels.

Transcranial color Doppler US enables examination of the basilar artery and arteries of the circle of Willis, characterizing collateral pathways. Flow reversal in the basilar artery is more likely when subclavian steal is symptomatic, particularly when carotid disease is present and is a potential alternative source of symptoms (see Image 10, Image 11).

Degree of Confidence: Demonstration of ipsilateral vertebral artery flow reversal with a parvus tardus waveform in the ipsilateral subclavian artery confirms the diagnosis of SSP.

  • US examination can document other arterial disease.

  • Investigate further if symptoms are atypical, suggesting a different intracranial or cardiac etiology.

False Positives/Negatives: A rare finding is vertebral artery flow reversal related to proximal vertebral artery occlusion (spinal artery steal) but without subclavian disease. In this syndrome, posterior fossa symptoms can occur with a normal subclavian artery, normal upper extremity blood pressures, and normal triphasic subclavian and brachial Doppler waveforms.

Lack of vertebral artery flow reversal can occur with severe left steno-occlusive subclavian disease when the left vertebral artery originates directly from the aortic arch, a variant that occurs in 6% of individuals and accounts for 14% of all arch vessel anomalies.

 

ANGIOGRAPHY

Findings: Conventional film-screen or digital angiography is the traditional test used for SSP diagnosis.

Arch aortography shows subclavian stenosis with antegrade vertebral flow in more minor subclavian stenosis.

In progressive subclavian stenosis, the filling of the vertebral artery becomes less obvious, until eventually, it fills in a retrograde fashion on more delayed imaging (see Image 1, Image 2).

Evaluation should detail the presence of concomitant disease in carotid, cerebral, and vertebrobasilar systems (see Image 8, Image 9).

Degree of Confidence: Misregistration and motion artifacts can compromise digital subtraction arteriography; if postprocessing does not overcome these problems, repeat contrast injection.

False Positives/Negatives: Spinal artery steal can cause vertebral artery flow reversal without subclavian steno-occlusive disease.

Subclavian steno-occlusive disease distal to the vertebral artery origin or left subclavian steno-occlusive disease associated with left vertebral origin directly from the aorta cannot be associated with vertebral artery flow reversal.

 

INTERVENTION

Intervention: Goals of treatment

  • Restore antegrade vertebral artery flow.

  • Alleviate cerebral hypoperfusion and its associated symptoms.

  • Improve arterial perfusion to the upper extremity.

  • Provide unobstructed flow to the left internal mammary artery when it is being used as a coronary artery bypass graft

Percutaneous revascularization

  • Percutaneous transluminal angioplasty initially has a high rate of technical success. While there are reservations about long-term patency, researchers have reported 3-year patency rates as high as 86%.

  • Despite the risk of embolism through the vertebral artery, stroke appears to be rare. This may be related to delayed establishment of antegrade flow in the vertebral artery after angioplasty.

  • Mortalities are rare. Complications usually are minor and related to access site hematoma.

  • Stent placement provides a higher initial success rate compared to angioplasty, particularly when treating subclavian occlusion. Initial reports suggest improved patency rates (3 y up to 90%) when compared to angioplasty alone. Balloon expandable stents or short self-expanding stents can be used, though the former are presently easier to precisely place and better able to resist recoil from surrounding calcified arteries (see Image 3, Image 6, Image 7).

Surgical revascularization

  • Carotid-subclavian bypass (CSB) with either synthetic graft or saphenous vein graft can be performed.

  • Prosthetic grafts reportedly have better 5-year patency rates (94% vs 58%).

  • Carotid-subclavian transposition (CST) is favored if there is distal embolization from the subclavian lesion.

  • Better long-term patency also is reported for CST than for CSB.

  • Axilloaxillary bypass is favored if ipsilateral carotid disease is present that cannot be treated. Unlike CSB, the autologous vein is favored.

  • Surgical treatments have documented mortality rates of 0.4-2.4%. Because of their morbidity and mortality, transthoracic subclavian and innominate endarterectomy have fallen out of favor.

  • Combined treatment of subclavian disease and concomitant carotid disease is associated with a better cure rate compared with repair of only one system.

Medical/Legal Pitfalls:

  • Failure to treat lesion-related symptoms; treating lesions only without symptoms
  • Recurrent or persistent brainstem transient ischemic attacks following surgical treatment of the subclavian lesion can occur in 10-24% of patients.
  • Failure to consider other causes of neurologic symptoms, including concomitant carotid, vertebrobasilar, and cerebral arterial disease and neoplasia

Special Concerns:

  • Controversy exists concerning the natural history of SSS; therefore, a decision to treat a symptomatic patient is not straightforward.
  • In such patients, the determination of other extracranial and intracranial arterial lesions influences management.
  • In the absence of other arterial disease, the risk of stroke appears to be negligible; reserve treatment of subclavian steal lesion for patients with debilitating vertebrobasilar transient ischemic attacks.

 

PICTURES

 
Caption: Picture 1. Arch aortogram initially shows apparent absence of left vertebral artery opacification. With delayed imaging on the same patient (right image), the left vertebral artery fills retrogradely to supply the left subclavian artery, confirming left subclavian steal phenomenon secondary to a severe stenosis of the proximal left subclavian artery.
Picture Type: X-RAY
Caption: Picture 2. Selective arteriogram (in patient shown in Picture 1) shows a severe proximal subclavian stenosis proximal to left internal mammary artery. The patient presented with angina having had a left internal mammary artery-left anterior descending coronary graft 12 months previously. Note nonopacification of the left vertebral artery and the filling defect consistent with in situ thrombus.
Picture Type: X-RAY
Caption: Picture 3. Thrombolysis was considered before angioplasty. As no antegrade left vertebral flow as demonstrated on the original digital subtraction arteriogram, thrombolysis was not performed. This line of treatment was determined in the belief that if any clot embolized to the coronary or vertebral circulations after percutaneous transluminal angioplasty (also a risk of thrombolysis alone), thrombolysis could then be performed with selective catheterization. After administration of vasodilators and anticoagulants, angioplasty with a 7-mm balloon restored antegrade flow to the left vertebral artery. The patient has had sustained relief from angina without embolic complication to either vertebral or coronary circulations. Both radial and ulnar pulses improved postangioplasty.
Picture Type: X-RAY
Caption: Picture 4. Gadolinium-enhanced magnetic resonance angiography maximum intensity projection image shows left subclavian artery occlusion in a patient with left subclavian steal phenomenon and aberrant right subclavian artery. The patient had no neurologic or arm symptoms, but the subclavian lesion eliminated the left internal mammary artery as a coronary bypass graft option.
Picture Type: MRI
Caption: Picture 5. Gadolinium-enhanced magnetic resonance angiogram (MRA) of right carotid-subclavian subclavian steal phenomenon. This tangential aortic arch maximum intensity projection view shows innominate artery occlusion and severe left proximal subclavian artery steno-occlusive lesion. Two-dimensional time-of-flight MRA confirmed retrograde flow in the right vertebral but not in the left vertebral artery. MRA tends to exaggerate the severity of steno-occlusive disease. While this MRA suggests a short occlusion of the left proximal subclavian, a severe stenosis rather than occlusion was documented on conventional catheter arteriography.
Picture Type: MRI
Caption: Picture 6. Conventional arteriogram in a 70-year-old man who previously had a carotid-subclavian bypass for dizziness related to subclavian steal syndrome. The bypass is occluded and a severe stenosis of the proximal subclavian artery is apparent. Note poor filling of right vertebral artery caused by retrograde flow documented on Doppler ultrasound; note also the bovine arch with common origin of right brachiocephalic trunk and left common carotid artery.
Picture Type: X-RAY
Caption: Picture 7. After stent placement, antegrade flow is restored in the right vertebral artery. Primary stenting was chosen because of theoretical risk of embolism to the left vertebral artery territory; however, there appears to be a time lag before restoration of antegrade vertebral artery flow after proximal subclavian revascularization that protects against this embolism risk. Other techniques to decrease the risk of vertebral artery embolism include decreasing peripheral resistance in the ipsilateral upper extremity (eg, with intra-arterial vasodilators or temporary blood pressure cuff inflation above systolic pressure) to promote vertebral artery retrograde flow during angioplasty or stenting.
Picture Type: X-RAY
Caption: Picture 8. Patient presented with cardiac ischemia after a left internal mammary artery-left anterior descending coronary graft and multiple coronary artery vein grafts. Subclavian steal cannot occur in this patient, as the left subclavian stenosis is distal to the left vertebral artery origin. Note antegrade flow in the left vertebral artery.
Picture Type: CT
Caption: Picture 9. Postangioplasty with a 9-mm balloon. The pressure gradient across the mid subclavian stenosis was reduced from 60-0 mm Hg.
Picture Type: CT
Caption: Picture 10. Normal antegrade right vertebral artery flow on Doppler ultrasound. With cephalad direction of insonation, the negative Doppler scale reading is consistent with flow going away from the direction of insonation in a normal cephalad antegrade fashion.
Picture Type: Photo
Caption: Picture 11. Doppler ultrasound shows reversed flow in the left vertebral artery consistent with left subclavian steal phenomenon. Doppler scale reading shows a negative deflection again; however, this time the direction of insonation is caudad, thus a negative scale Doppler reading indicates flow in a caudad direction and flow reversal in the left vertebral artery.
Picture Type: Photo

 

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