The Subclavian Steal Syndrome

COLLECTIVE REVIEW

The Subclavian Steal Syndrome Vincent A. Piccone, Jr., M.D., and Harry H. LeVeen, M.D.

T

he subclavian steal syndrome is characterized by cerebral ischemic attacks caused by reversal of blood flow through the vertebral artery consequent to arterial obstruction proximal to the origin of the vertebral artery (Fig. 1). While not a separate disease entity, the subclavian steal syndrome relates cerebral ischemia to a remote vascular lesion which is surgically correctable and more frequent than was anticipated. HISTORY

T h e anastomotic channels supplying the subclavian artery beyond a proximal occlusion were well described by the anatomists [54]. Detailed collateral pathways are found in Tagariello’s work with dogs and cadavers [94]. Contorni [141 demonstrated the vertebral-basilar-vertebral collateral artery flow with angiograms in human subjects for the first time in 1960. Contrast medium injected into the contralateral brachial artery of an asymptomatic patient with an absent left radial pulse flowed up the right vertebral artery, down the left vertebral artery, and onward to the left subclavian artery just distal to the occlusion. Rob [79], Toole [981, and Fields [29] discussed the “siphon” of the vertebral collateral artery at the third Princeton Conference on Cerebrovascular Diseases in January, 1961. Thus, while the necessity for brachiad flow in the vertebral collateral artery was recognized, the causal relationship between cerebral ischemic attacks and occlusion of the proximal subclavian artery remained obscure until later in 1961. Then Reivich and associates [78], in several case reports and animal experiments, clearly associated cerebral ischemic attacks with the reversed vertebral flow described by Contorni. At the same time, an editorial in the New From the Departments of Surgery, College of Medicine, State University of New York Downstate Medical Center and Veterans Administration Hospital, Brooklyn, N.Y. Address reprint requests to Dr. Piccone, Department of Surgery, l‘eterans Administration Hospital, Brooklyn, N.Y. 11209.

PICCONE AND LEVEEN

F I G . 1. Occlusion of the subclavian artery proximal to the vertebral artery causes shunting of blood from the cerebral circulation through the vertebral artery and into the subclavian artery.

England Joul-nal of Medicine [30] endowed the literature with the descriptive term subclavian steal. This nomenclature provoked lively competition typified by such names as “brain drain” [59], “grand larceny of the vertebral” for large steals [24], “subclavian snitch” for small steal [44],and “brachial-basilar insufficiency” [68]. T h e original, subclavian steal, has endured and has become the accepted name. ANATOMY

T h e anatomical basis for the subclavian steal syndrome is founded in collateral circulation which sustains flow in the subclavian artery after 52

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occlusion of the proximal portion. T h e collateral pathways [6, 55, 59, 67, 68, 711 (Fig. 2) include the following: 1 . external carotid artery to occipital artery to muscular branches of vertebral artery 2. external carotid artery to superior thyroid artery to inferior thyroid artery to thyrocervical trunk 3. superior epigastric artery, intercostal artery, and contralateral internal mammary artery to ipsilateral internal mammary artery

iim F I G . 2. T h e collateral circulation maintains flow in the subclauian artery aftei occlusion of the proximal portion. T h e m a i n pathways include contralateral uertebial arteries (a) and basilar arteries (b) t o ipsilateral uertebral arteries (c); external carotid artery (d) to superior thyroid artery (e) t o inferior thyroid artery ( f ) to thyrocervical trunk (g); external carotid artery (d) to occipital artery (h) to mttsciilar branches of uertebral arteries (i); aorta to posterior intercostal arteries (j) to sztpwioi intercostal arteries (k) to costocervical trunk (1); and superior epigastrzc arteyy (m) and anterior intercostal arteries (n) t o contralateral internal mammary urteiy (0)to ipsilateral internal mammary artery (p). VOL.

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4. aorta and posterior intercostal arteries to superior intercostal artery to costocervical trunk 5 . contralateral vertebral and basilar artery to vertebral artery

The unique and most essential of these collateral routes in terms of flow is the vertebral artery, which is usually the only sizable collateral [71]. Rapid retrograde flow consequent to proximal occlusion of the inflow vessel presupposes large collateral arteries with high pressures and high inflow capabilities. The basilar artery from the circle of Willis and the contralateral vertebral artery do provide this unusually high inflow capability (Fig. 3). The size of the basilar artery is comparable to the vertebral arteries and connects directly with each. The posterior communicating branches of the internal carotid arteries are also vessels of substantial size. High flows are thus directed into a low pressure system with almost no resistance in the shunt. Interruption of the subclavian artery proximal to the vertebral artery thus poses little threat of ischemia to the upper limb but diverts significant amounts of blood from the brain. HEMODYNAMICS

The hemodynamic changes in the subclavian steal syndrome have been studied experimentally in dogs and monkeys and are now well documented in man. Occlusive disease proximal to the origin of the A n t e r i o r communicating

Posterior

a

rior c e r e b r a l

Superior cerebr

A n t e r i o r sp i n al

F I G . 3 . Circle of Willis and uertebral-basilar axis, showing the large inflow urssels that make the subclauian steal possible.

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vertebral artery reduces the pressure in the subclavian artery distal to the obstruction. When the pressure at the subclavian end of the vertebral artery drops below the basilar artery pressure, the vertebral artery flow is reversed. Diversion of basilar artery blood can be of such magnitude that symptoms of cerebral ischemia ensue. Reivich and associates [78] used an electromagnetic flowmeter to show that a subclavian pressure 10% less than systemic arterial pressure would reverse flow in the vertebral artery. Sammartino and Toole [82] demonstrated reversal of flow in the vertebral artery immediately after establishment of a systemic-subclavian pressure differential exceeding 2 1 to 40 mm. Hg. A 50% reduction in the lumen of the subclavian or innominate artery is necessary to produce the critical pressure gradient of 10% 1173. Berger and associates [4] found that a 65 mm. Hg pressure differential across the stenotic lesion produced a reversed flow of 29 ml. per minute in a patient with a subclavian steal syndrome. Significant stenotic lesions of the subclavian artery without the steal phenomenon were noted by Gonzalez and associates [36], who suggested that the degree of participation of the vertebral artery as a collateral may be variable and depends, among other things, upon the inflow from the other collateral pathways. Regional hemodynamic changes have been measured in monkeys by multiple electromagnetic flowmeters. T h e reversed flow through the vertebral artery was greater than the normal forward flow [39]. When vertebral flow was reversed, flow in the contralateral vertebral artery and both carotid arteries showed marked compensatory increases, but the total cerebral flow, measured by summation of flowmeter readings and internal jugular vein drainage, was slightly decreased. When the posterior communicating branches of the middle cerebral artery were occluded, the compensatory increase in internal carotid flow was almost abolished, thus demonstrating the major role of these vessels in the collateral circuit [39]. Quantitative measurements in man show similar changes in cerebral hemodynamics. Hardesty and associates [40, 411 measured flow in the carotid and vertebral arteries of patients undergoing radical neck dissection. T h e average internal carotid artery flow was 370 ml. per minute, and the average vertebral artery flow was 45 ml. per minute (1 1% of the total cerebral artery flow). T h e total cerebral artery flow in patients under anesthesia was 830 ml. per minute. Kety and Schmidt [49] obtained a figure of 750 ml. per minute. Hardesty et al. [41] occluded the subclavian artery proximal to the origin of the vertebral artery and found a retrograde flow through the vertebral artery of 25 to 98 ml. per minute and a compensatory increase of 25 to 60 ml. per minute through the internal carotid artery. Reversed vertebral flow only partially compensates for the normal VOL.

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subclavian flow to the limbs. In dogs, the brachial vertebral flow amounted to 60% of normal subclavian flow [82]. Limb exercise, which even normally diverts blood from the vertebral to the subclavian circulation, augments the preexisting reversed flow during repetitive limb muscle contraction in dogs [82]. Such variations in flow indicate the possibility that retrograde flow may be intermittent. In some patients increased flow to a limb may be a prerequisite for inversion of the resting pressure gradient and for flow from the brain stem to the arm

WI.

ETIOLOGY

Atherosclerosis is the most frequently reported cause of the subclavian steal. However, these hemodynamic alterations may result from any lesion that prevents entrance of blood into the proximal subclavian artery at a pressure above that in the vertebral-basilar axis. Massumi [601, Bradley [71, and Gerber [34] have described congenital atresia of the subclavian artery at its origin with filling of the distal vessel by brachial flow through the vertebral artery. Kinking of the subclavian artery associated with pseudocoarctation of the aorta was reported by Lochaya [56]. Vianna et al. [lo21 described an unusual origin of the left subclavian artery below an aortic coarctation, with the distal aorta filling from reversed vertebral flow. A similar situation involving the right subclavian artery was found by Grollman and Horns [38]. Daves [24] reported the subclavian steal syndrome associated with atresia of the aortic arch between the origins of the left common carotid artery and the left subclavian artery. Emboli lodged proximal to the vertebral artery also caused the subclavian steal phenomenon [23, 37, 851. Such emboli are most often found in association with mitral stenosis and myocardial infarction. Ligation of the subclavian artery proximal to the origin of the vertebral artery during a surgical procedure necessitates filling of the distal subclavian artery by collaterals, including the vertebral arteries. Thus, Folger and Shah [31], examining angiograms of 114 children with Blalock-Taussig shunts, found a subclavian steal in 12 patients. Symptoms suggesting basilar artery insufficiency were present in 7 of the 12 children. Ligation of the subclavian artery during resection of a traumatic thoracic aortic aneurysm [61], similarly, may result in a subclavian steal flow pattern. Stenosis of the left subclavian origin secondary to suture line distortion can result from repair of a coarctation of the aorta [47]. Use of the subclavian artery in surgical treatment of coarctation of the aorta, as recommended by Shumaker [88], may produce retrograde vertebral flow unless flow to the distal subclavian artery is restored or the vertebral artery tied. 56

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Subclavian artery occlusion may result from trauma. Rojas and associates [813 reported reversed vertebral flow following luxation of the clavicle with compression and thrombosis of the subclavian artery against the vertebral column. Craddock and Logan [16] reported traumatic division of the subclavian artery by a bayonet, with filling of the subclavian artery from the vertebral artery after ligation of the divided artery. T h e vertebral artery itself can be obstructed by arteriosclerosis [76], kinking, or compression, as in cervical spondylosis [86], and cause ischemic symptoms [96]. T h e flow through the artery may be impeded or directed downward through the vertebral artery and out into the muscular branches beyond the obstruction. In this situation, reversed flow through the vertebral artery does not enter the subclavian artery, and a steal of lesser magnitude results. In summary, the subclavian steal phenomenon results from any condition that interferes with the flow into the vertebral artery and leaves the subclavian outflow intact. P A THOLOGY

Seventy-five percent of atherosclerotic obstructions of the subclavian artery are on the left side. T h e occlusive lesions causing a steal on the right side may occur in the innominate artery as well as in the subclavian artery [6, 28, 44, 47, 50, 67, 831. In patients with these lesions, blood flow is usually reversed in both the common carotid and the vertebral arteries [4, 621. However, Bosniak [6] and Killen and Gobbel [51] have reported innominate artery occlusion with a reversal of flow in the vertebral artery and reentry of this blood into the cerebral circulation via the right common carotid artery. Such hemodynamic changes would suggest an incomplete circle of Willis. Bilateral subclavian steals [12] have been reported but are rare. Arteriosclerotic narrowing or occlusion in the other extracranial arteries was noted in many cases [70, 84, 1041. CLIiVICd4L FEATURES

The patient with a subclavian steal phenomenon may be asymptomatic; however, cerebral symptoms or complaints referable to the arm are more frequent. Intermittent basilar artery insufficiency, described by Millikan and Siekert [63], is usually present and characterized by attacks of light-headedness, vertigo, and ataxia, incoordination, loss of equilibrium, syncope, transient attacks of bilateral blurred vision, and sensory and motor deficits of the extremities and face. Ischemic arm complaints include claudication, easy fatigue, coolness, paresthesias, and even gangrene of the fingertips.

PICCONE AND LEVEEN

Neurological manifestations of the subclavian steal syndrome result from ischemia or infarction of any structure perfused by the vertebralbasilar system, i.e., upper spinal cord, entire brain stem, cerebellum, labyrinth, cochlea, and occipital lobes. Consequently, many and varied signs and symptoms related to any or all of these structures are encountered, These include, in addition to those previously mentioned, dizziness, visual defects, headache, dysarthria, confusion, focal seizures, olfactory hallucinations [9], and major strokes. T h e virtual constellation of neurological complaints is best explained by the high incidence of coexisting occlusive lesions in other cephalic arteries. Wheeler [ 1041 found occlusive lesions in the other cranial arteries in 6 of 11 patients. Killen and associates [50] reviewed 80 patients with the subclavian steal syndrome and found occlusive lesions in 35%. Although attacks of vertebral-basilar insufficiency are usually transient and recurrent, permanent neurological damage may occur. Another 10% of patients are completely asymptomatic. Angiography, performed because of decreased blood pressure in one arm or the presence of another vascular lesion, is most frequently responsible for discovery of the subclavian steal in an asymptomatic patient. T h e neurological examination is usually negative, although fullfledged cerebrovascular accidents have occurred. Transient attacks are often associated with a diminished blood pressure or absent pulse in one arm. Killen [50] found the radial pulse diminished in two-thirds of the patients and not detectable in another one-third. T h e brachial systolic pressure difference was usually over 20 mm. Hg, averaging 50 mm. Hg, and as great as 140 mm. Hg. A bruit sometimes was heard in the supraclavicular regions. DIAGNOSTIC TESTS

T h e hemodynamic peculiarities of the subclavian steal phenomenon are the basis for several clinical tests. Ischemic attacks precipitated by exercise of the upper extremity have been used as an exercise tolerance test [68]. Whereas North and associates [68] reported consistent association of a positive exercise test and a subclavian steal, others were able to provoke ischemic episodes in only a small percentage of patients (Gonzalez et al. [36], 20%; Killen et al. [501, 25%; and Siekert et al. [89], 0). Javid and associates 1461 compressed the ipsilateral carotid artery to reduce intracranial arterial pressure and flow, thereby decreasing the retrograde flow into the arm and producing an abrupt diminution of the pulse. Ipsilateral carotid artery compression during bilateral brachial oscillometry revealed a distinct drop in pressure in the affected arm. Toole and Tulloch [loll used bilateral simultaneous sphygtno58

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nianonietry with audio detection and light indication of systolic pressure and pulse timing. Systolic brachial blood pressure differences in excess of 20 mm. Hg accompanied by a pulse delay were considered reliable criteria for clinically confirming the subclavian steal flow pattern. Inflation of a sphygmomanometer on the ipsilateral brachial artery temporarily reduces the subclavian steal and arrests acute cerebral ischemic attacks. The result is prognostic of the surgical outcome [72]. 0 I’HTH ALMODY NAMOMETRY

Killen and associates [50] reviewed the results of ophthalmodynamotlietry in 14 patients. Normal retinal artery pressures in 4 patients whose only occlusive lesion was that producing the subclavian steal syndrome and low pressures in patients with ipsilateral carotid occlusive lesions demonstrate the poor specificity of ophthalmodynamometry. DYE-DILUTION CURVES

Marshall and Mantini [59] used dye-dilution curves to demonstrate the subclavian steal. Indocyanin green, in comparison to the iodinecontaining contrast media, is not vasoactive. Dye was injected into one subclavian artery and a dilution curve was recorded from the opposite brachial artery. T h e early appearance of dye, long before the normal dye-circulation curve, proved that a short circuit existed between the arterial injection and sampling sites. 1 O N A L SENSATION TESTS A N D DIGITAL PLETHYSMOGRAPHY

These tests have also been used in detecting the subclavian steal syndrome. Creel and his associates [18] felt an abnormal time requirement for the tone-noise distinction test was an observable and frequently diagnostically useful aspect of vertebral artery insufficiency. Conrad and associates [13] showed the pulse delay with digital plethysmography . These clinical and laboratory tests are complementary but not essential, and cannot displace the need for angiography. The certain diagnosis of a subclavian steal syndrome can be obtained only from an arch aortogram with sequential roentgenograms. ANGIOGRAPHY

Several angiographic techniques have been used to demonstrate the retrograde vertebral flow which is characteristic of the subclavian steal syndrome. Percutaneous injection into the vertebral artery, catheter injection into the brachial or subclavian artery, and selective catheterization of the vertebral artery by transbrachial [77] or transfemoral [19] approach are inadequate and misleading. The pressure of percutaneous injection into the vertebral artery has caused displacement of blood in both directions and provided a radiological appearance

PICCONE AND LEVEEN

suggesting reversal of flow [73, 871. Gonzalez et al. [35, 361 describe retrograde flow in either vertebral artery upon injection of the opposite brachial artery. Injection into the left subclavian artery followed by serial roentgenograms showed retrograde flow down the right vertebral artery, and injection of the right subclavian showed retrograde flow down the left vertebral artery. An arch aortogram showed no occlusive or stenotic lesion in the subclavian or vertebral arteries and no retrograde vertebral flow. Cronquist [ 191 reported retrograde opacification of the opposite vertebral artery in 20% of all patients, even those without subclavian stenosis, in his experience with transfemoral selective vertebral catheterization. Rapid injection of contrast temporarily reverses the pressure gradient in the contralateral vertebral artery during the sequence and produces reversed flow. Curry and Howland [20] have pointed out the pitfalls in the radiological diagnosis of the subclavian steal syndrome, and Toole [loo] has emphasized the accuracy that only arch aortography provides. The arch aortography should be performed by the percutaneous or open technique, using an automatic injector and a rapid film changer (4 films per second for 4 seconds and 1.5 films per second for 2 seconds). Fifty cubic centimeters of 50% meglumine diatrizoate or other suitable contrast material injected into the ascending aorta should permit visualization of prograde flow in the nonstenotic vessels immediately after injection, and the late films will demonstrate reverse flow down the vertebral artery and into the subclavian artery. M A N A G E M E N T OF T H E SUBCLAVIAN S T E A L SYNDROME INDICATIONS FOR OPERATION

Operation often has been performed to relieve recurrent cerebral ischemic attacks, to prevent incipient strokes, and on occasion to ameliorate ischemic arm complaints. Fixed neurological deficits are generally regarded as not amenable to surgical correction. In rare instances hypoxia may impair cerebral cellular function without loss of viability. Early revascularization could then restore an apparently fixed deficit [72]. The asymptomatic patient with a subclavian steal resulting from arteriosclerosis poses another problem. McLaughlin and associates [62] and Couves and associates [ 151 successfully operated on asymptomatic patients. On the other hand, Ponsdomenech and associates [75], Gonzalez and associates [36], Javid et al. [461 in discussing the Gonzalez paper, and Molloy and Jones [641 believe subclavian steals in asymptomatic patients should not be corrected. Only the most meager data

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are available on the natural course of the asymptomatic patient. Wheeler [104], discussing the chance of a later stroke, described 3 asymptomatic patients with subclavian occlusive disease and unequal brachial blood pressures followed for 8 to 13 years. T h e presence of subclavian steal hemodynamics, however, was not specified. Piccone, Karvounis, and LeVeen [72] described a patient with an asymptomatic subclavian steal which was most probably of 8 years’ duration. Furthermore, symptomatic patients have, on occasion, benefited with passage of time [91]. Patients with the subclavian steal syndrome may be more susceptible to a cerebrovascular accident because some patients present with a major stroke which is relieved following correction of the steal. However, no statistics on this subject exist, and the number of reported operations is only now sufficiently large to project morbidity and mortality figures. T h e question of whether to operate on the asymptomatic patient thus must await (1) survival statistics on the natural course of the disease obtained from asymptomatic patients with a radiologically documented steal, and (2) the morbidity, mortality, and long-term results of the various surgical procedures. Spontaneous resolution of a traumatic subclavian steal syndrome has been reported by Mandlebaum [57]. However, the danger of hidden intrathoracic hemorrhage is real. Traumatic avulsion of the innominate artery and severance of the left subclavian artery as a cause of the subclavian steal syndrome have been described. Immediate surgical intervention should be considered in patients with an obviously traumatic subclavian steal syndrome. Management of the subclavian steal syndrome as a complication of the Blalock-Taussig operation is not yet well defined. Total repair of the tetralogy was accompanied by relief of the ischemic cerebral symptoms in the 2 symptomatic patients described by Folger and Shah [31]. Awareness that the Blalock operation can create the subclavian steal phenomenon on the right side, and that a Blalock operation modified to leave an intact vertebral-subclavian junction on the left side also can create a subclavian steal, should shift attention to prevention of this iatrogenic problem. Reivich [78] has emphasized ligation of the vertebral artery in conjunction with a Blalock operation on the right and performance of the operation as originally described [5] on the left. T h e adequacy of the contralateral vertebral artery in maintaining basilar circulation should be proved by angiography before ligation, because 2 to 3% of patients have an anomalous contralateral vertebral artery [97], and ligation of the only vertebral artery perfusing the basilar system would create a fatal basilar perfusion defect.

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Surgical Management of the Subclavian Steal Caused by Arteriosclerosis. Treatment has varied as to hemodynamic objectives, operative techniques, and surgical exposures. The procedures can be grouped as follows. 1. Restoration of prograde flow in the vertebral artery using a major thoracic approach. Thromboendarterectomy performed through a major thoracic incision with or without patch angioplasty, bypass grafts [2 11, and graft interposition are the procedures most commonly used to correct the subclavian steal syndrome. The goal of any such procedure is to reestablish prograde flow in the vertebral artery. The operative approach depends on the site of occlusion. T h e midsternotomy with an upward extension medial to the right sternocleidomastoid muscle provides excellent exposure of the innominate, right subclavian, and right common carotid arteries (Fig. 4). and is

FIG. 4 . Limited midsternotomy with extensions laterally and along the sternocleidomastoid mitscle provides easiest access to the right subclavian and innominate arteries. 62

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closed simply [ZO]. The downward length of the incision is limited by a lateral extension into the right third intercostal space. Midsternotomy is a less desirable approach to the left subclavian artery. The left subclavian artery originates from the posterior portion of the aortic arch, and the midsternotomy approaches the anterior aspect of that structure. Dissection of the phrenic, vagus, or recurrent laryngeal nerves as they cross the aortic arch introduces the hazard of nerve damage. T h e depth of the left subclavian artery in the wound does not provide adequate control of the left subclavian artery at its origin. Left thoracotomy improves the exposure and permits easy accessibility of the left subclavian artery at its origin. T h e results of establishing prograde flow in the vertebral artery by a major thoracic approach are hemodynamically and clinically documented. Removal of an obstructing lesion in the proximal right subclavian artery converted a retrograde flow of 29 ml. per minute through the vertebral artery into a forward flow of 97 ml. per minute [4]. In another patient, retrograde filling of the subclavian artery from the vertebral and carotid arteries was converted to a 440 ml. per minute forward flow through an aortoinnominate bypass graft [4]. Although this type of hemodynamic data is seldom obtained during surgical correction, the increasing number of clinical reports provide abundant documentation of the clinical changes following operation. Correction of symptoms and signs of cerebral ischemia, restoration of brachial blood pressure in the affected limb, and alleviation of the ischemic arm complaints are the criteria generally applied in evaluating the surgical procedure. T h e results of treatment by endarterectomy and bypass graft have been summarized from the literature (Table); they indicate that these operations, in general, successfully accomplished their goals with an acceptably low morbidity and mortality. Ninety-nine patients had operative correction by thromboendarterectomy, making it the most frequently used procedure for correction of the subclavian steal syndrome. Reporting of results is not standardized or complete in many instances. However, a major thoracic approach for endarterectomy was used in at least 63 patients, with successful revascularization in 59 patients. Failure occurred in 2 patients, and 2 patients died (3.4%). Autogenous and plastic bypass grafts were performed in 47 patients. A major thoracotomy was used in 38 patients. Success by the clinical criteria listed earlier was achieved in 37 patients, and 1 patient died. The adequacy of purely clinical criteria in evaluating the revascularization procedures has been challenged and the need for postoperative angiography emphasized 14, 721. Berger et al. 141 reported a stenosing lesion in the proximal left subclavian artery which did not produce a sufficient pressure gradient for a steal until the correction VOL.

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Endarterectomy and/or Patch Graft Author

Good

Reivich et al. [781 3 Mannick et al. [581 North et al. [681 2 Bosniak [61 1 Couves et al. [151 2 Irvine et al. [451 3 Johnson [471 2 Steinberg and Halpern [931 1 Sproul [921 2 Williams et al. [lo51 3 Callow 181 2 Ethier [28] 1 Gorman et al. [37l Heyman et al. [441 6 Sanger et al. [831 1 Siekert et al. 1891 Nemir et al. 1661 2 Pizarro and Roth 1741 Craddock and Logan [161 Gerard and Sabety [331 1 Henzel et al. [431 3 Killen et al. [501 11 Molloy and Jones [64] 1 Pineda and Smith [731 1 Tala et al. [951 8 McLaughlin [621 4 Ponsdomenech et al. [751 1 Wheeler [ 1041 7 Gonzalez et al. [361 5 Toole and Tulloch [loll 3 Berger et al. [41 1 Javid et al. [461 6 Lee et al. [531 2 Dumanian et al. [251 2 Piccone et al. [721 5 Total 92

?

Poor

Interposition or Bypass Graft

Died

Good

Poor

Died

1

1 2 1 2

1

1

2 1 1 1 1

1 3 1 1

1

3 1

13

5

2

3

4-

41

1 1

1

of the right subclavian steal improved the inflow into the vertebralbasilar axis. Surgical creation of the contralateral steal would have escaped detection without postoperative angiography. Evaluation of endarterectomy by clinical means alone poses a second problem. T w o possible hemodynamic situations may result from endarterectomy: (1) the vertebral flow may be stopped, as by dissection 64

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of the distal intimal flap across the vertebral ostium (Fig. 5); or (2) prograde flow may be reestablished in the vertebral artery. Whereas an intimal flap at the distal end of a peripheral endarterectomy would cause severe peripheral ischemia, an intimal flap at the vertebral ostium stops the steal and improves cerebral circulation. Endarterectomy with arrest of the steal or reestablishment of prograde vertebral flow would produce a similar brachial blood pressure in each arm and amelioration of ischemic cerebral complaints. T h e association of symptomatic improvement with the reestablishment of cephalad flow in the vertebral artery following endarterectomy is therefore unwarranted. In fact, cephalad flow in the vertebral arteries can be substantiated only by postoperative angiography. T h e incidence of obstruction at the vertebral artery ostium is important because (1) it is easily overlooked; (2)

C FIG. 5 . Endarterectomy complicated by an inlinzal flap at the vertebral ostium (A, B, C). Even though prograde pow through the vertebral arteiy has not been achieved, the steal has been stopped and the patient's symptoms have been relieved. VOL.

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the same hemodynamic result could have been achieved by simple ligation of the vertebral artery, a much smaller operation not requiring an open thoracotomy; and (3) thromboendarterectomy is the most frequent procedure employed. Endarterectomy or bypass graft aims to reestablish cephalad flow in the vertebral artery. In addition, the advantages of reestablishing prograde flow in the vertebral artery over simply arresting the steal should be known in terms of protection against future cerebrovascular accidents resulting from further atherosclerotic narrowing of other major arch vessels. Postoperative angiography will objectively define the results of revascularization surgery, and future retrospective studies comparing patients with arrested stealing and those with successful revascularization are then possible. 2. Revascularization hy improving flow in other major extracl-anial arteries and leaving the subclavian steal undisturbed. This approach is mentioned only because it has been used on occasion [l, 78, 80, 901. The other extracranial arteries may be obstructed in the cervical or intrathoracic portion. Some of the increased cerebral blood flow resulting from removal of these obstructions will undoubtedly find its way into the vertebral-basilar axis and be wasted as increased retrograde flow through the vertebral artery. Theoretically, ischemic complaints would be alleviated when the increase in total cerebral flow exceeds the increase in the subclavian steal. While the authors might use a different approach today, their success must be noted. If ischemic complaints are cerebral rather than vertebral-basilar, and occlusive carotid lesions coexist with the vertebral-subclavian steal, treatment of both hemodynamic disturbances might be preferable. In summary, the results of revascularization using any of the major thoracic operations, while in general very good, have been associated with some morbidity and mortality. Thoracotomy is undoubtedly a major challenge to the elderly patients who have arteriosclerotic lesions in their extracranial cerebral arteries. Other authors have sought to develop lesser operations which could hopefully achieve the same clinical improvements with a reduction in morbidity and mortality and thereby also be applicable in the very-poor-risk category of patients. Two approaches, ligation of the vertebral artery and transcervical revascularization, have been used. Transcervical revascularization has been achieved by endarterectomy, resection of the clavicle to place bypass grafts, carotid-subclavian bypass grafts, and vertebral or subclavian transposition to the carotid arteries. 3. Vertebral artery ligation. Ligation of the vertebral artery was reported by Rob [79] in 1961. T h e operation considerably improved a patient who was unsuitable for a thoracotomy. Objections to ligation of the vertebral artery were based on (1) 66

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isolated reports of ischemic brain damage and death consequent to ligation or occlusion of the vertebral artery for other reasons; and (2) the risk of ischemic damage to the ipsilateral upper extremity. Carpenter [ 101 and Murray [65] have described fatal cerebellar infarction following thrombosis of the vertebral artery. Jones et al. [48] describe two open-heart surgical patients who died in the early postoperative period with a clinical picture suggestive of basilar artery insufficiency following ligature of the vertebral artery to allow use of the subclavian artery for arterial cannulation. French and Haines [32] described fatal cerebral infarction consequent to open angiography and vertebral ligation. Another fatality following subclavian and vertebral artery ligation was reported by Thomas et al. [97]. On the other hand, ligation of the vertebral artery has been used for neurosurgical purposes. Dandy [22] performed unilateral vertebral artery ligation in 20 patients without a mishap. Elkin and Harris [27] ligated the vertebral artery in 10 patients with arteriovenous fistulas. Certainly, many vertebral arteries have been ligated during Blalock-Taussig operations. Vertebral artery ligation for neurosurgical problems should not be compared to ligation for correction of retrograde flow. Theoretical differences preclude using complications of the procedure in the first situation as a valid criticism of its use in the second. Ligation of the vertebral artery for neurosurgical conditions poses the danger of peripheral ischemia consequent to occlusion of the nutrient artery. Ligation of the vertebral artery having retrograde flow introduces the possibility of stasis, thrombosis, and cephalad propagation of the thrombus in an artery that is already draining blood from the dependent organ. Limited clinical experience with vertebral artery ligation for the subclavian steal syndrome does not suggest cephalad thrombosis to be a serious threat-even without the use of anticoagulants after the ligation. Ischemia and even gangrenous loss of the upper extremity have followed ligation of the subclavian artery during a Blalock-Taussig procedure [52, 1031, that is, when the collateral branches of the subclavian artery are all still intact. Angiograms of patients with subclavian steal often demonstrate the vertebral artery to be the largest collateral channel [71]. Cameron and Wright [91 reported a cold, pulseless arm following vertebral artery ligation for the subclavian steal syndrome. T h e patient was treated with anticoagulants. The radial pulse was detected again on the fourth postoperative day. It gradually increased, and the arm once again became warm. Thus, ligation of the vessel providing the greatest collateral flow to the limb must be considered cautiously for both theoretical and clinical reasons. Yum and Myers [ 1061 suggested temporary occlusion of the vertebral artery before placeVOI,.

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ment of the ligature. Viability of the arm is ascertained by changes in color, pulse, and blood pressure. Postoperative angiograms indicate the internal mammary artery to be the major collateral after ligation of the vertebral artery. Actual experience with ligation of the vertebral artery for the subclavian steal syndrome has been limited [9, 62, 79, 93, 101, 1061. T h e procedure has been used in only 6 of some 200 reported cases. The clinical results, however, compare favorably with those of the other approaches. All the patients experienced an amelioration of cerebral complaints, there were no deaths, and only one upper extremity was temporarily threatened by ischemia. The long-term results are not known. 4 . Restoration of prograde flow in the vertebral artery using a cervical approach. Transcervical subclavian or innominate endarterectomy, transposition of the proximal subclavian artery to the common carotid artery with an end-to-side anastomosis [69], transposition of the proximal vertebral artery to the common carotid artery [ 111, and the carotid-subclavian bypass graft [68] (Fig. 6) restore prograde flow through the vertebral artery without thoracotomy. Wheeler [ 1041 and others [8] have used the transcervical approach

V e r t e b r a / Transposition

FIG. 6 . Transcervical operations, exclusive of endarterectomy, which may be useful in establishing prograde flow in the vertebral artery. (Carotid-subclavian bypass: North [681; subclavian transposition: Parrott 1691; vertebral transposition: Clark and Perry [ I l l . )

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Subclauian Steal Syndrome

for endarterectomy. It is more applicable on the right side, where the subclavian artery is more accessible from the cervical approach. Resection of a portion of the clavicle may be necessary. T h e results [8, 25, 43, 53, 64, 68, 75, 83, 1041 compare favorably with those of the various other techniques. Nine patients were successfully treated, and 1 patient died postoperatively. T h e lack of enthusiasm for this approach stems from the poor proximal control, especially on the left side, and the inferior exposure of the subclavian artery compared with the thoracic approach. T h e carotid-subclavian bypass and the transposition operations offer transcervical revascularization without the somewhat risky problems of transcervical endarterectomy. The common carotid artery can be occluded safely during the short time required for the anastomosis [Z] because of the decreased cerebral oxygen requirement during general anesthesia, the considerable compensatory flow through the contralateral common carotid and vertebral arteries when one carotid is occluded, and the retrospective information that acute cerebral ischemic damage has not followed clamping of the common carotid artery under these circumstances. Dumanian [25] criticized the bypass procedures because of the theoretical possibility of siphoning blood away from the distal portion of the common carotid artery. Experimental electromagnetic flow studies on both carotid arteries, both vertebral arteries, and left subclavian arteries before and after carotid-subclavian bypass on dogs with a subclavian steal flow pattern demonstrated decreased flow in the left common carotid artery distal to the bypass graft and a decrease in the total cephalic blood flow which is accentuated by injection of papaverine into the distal subclavian artery [42]. Barner and associates [3] failed to confirm the decreased flow in the carotid distal to the bypass graft at rest but showed that distal carotid flow fell 15% during simulated brachial exercise. These theoretical and experimental objections to the carotid-subclavian bypass and transposition operations have not been realized clinically. In contrast, review of 13 cases from the literature [26, 36, 46, 68, 69, 751 suggests consistent relief of cerebral ischemic symptoms by the carotid-subclavian revascularization. Relief of ischemic complaints was achieved in 11 of the 13 patients. Both failures were in patients with occlusive lesions in other extracranial arteries. There were no operative deaths. In addition, Ehrenfeld and associates [261, investigating the hemodynamic effect of a graft taking its origin from an undiseased artery supplying another vascular bed, found that the effect was to enhance flow through the new parent artery rather than to “steal” blood from the peripheral bed of the artery from which the graft originated. Increased demand on the side supplied by the graft caused a tenfold increase in the parent artery flow without VOL.

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stealing from the contralateral extremity. After placement of a carotidsubclavian vein bypass graft in a patient, flow in the common carotid artery proximal to the graft increased from 600 ml. per minute to 850 ml. per minute, while flow in the carotid distal to the anastomosis remained unchanged at 600 ml. per minute. In summary, although revascularization by major thoracic procedures has provided good results with little morbidity and mortality, increased application of the carotid-subclavian bypass operation (1) might further reduce the morbidity and mortality and (2) might save many elderly patients the discomfort and inconvenience of a much larger operation. Barner and associates [3] feel that the carotid-subclavian bypass might be applied more often on the left side, where the nondominant arm, used less vigorously in exercise, would not siphon off blood during exercise that would otherwise enter the distal common carotid artery, On the right side, in younger patients, the proximal carotid inflow might be inadequate for perfusion of the carotid and subclavian arteries when the need of the dominant arm is increased during work. T h e authors, aware of these theoretically and experimentally established limitations, would emphasize the excellent clinical results of the carotid-subclavian bypass. Surgical Management of the Subclavian Steal Syndrome Consequent to Congenital Anomalies, Trauma, and Emboli. T h e unusual types of subclavian steal syndrome are managed according to the causative lesion. Symptoms are most often not present unless obstructing lesions coexist in other extracranial cerebral arteries. Symptoms may be present, however, and an attempt to elicit the presence of such complaints should be made. Embolectomy [231, repair of the causative congenital anomaly, or exploratory thoracotomy with repair of trauma would be the operative procedures employed. Correction of a subclavian steal syndrome consequent to anomalous origin of a left or right subclavian artery below a coarctation, atresia of the aortic arch between the left common carotid artery and the subclavian artery, and other congenital lesions would most often result from repair of the congenital lesion itself. REFERENCES 1 . Ashby, R. N., Karras, B. G., and Cannon, A. H. Clinical and roentgenographic aspects of the subclavian steal syndrome. Amer. J . Roentgen. 90:

535, 1963. 2. Bahnson, H. T., Spencer, F. C., and Quattlebaum, J. K. Surgical treatment of occlusive disease of the carotid artery. Ann. Surg. 149:711, 1959. 3. Barner, H. B., Rittenhouse, E. A., and Willman, V. L. Carotid-subclavian bypass for subclavian steal syndrome. J . Thorac. Cardiovasc. Surg. 55~773, 1968.

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Subclavian Steal Syndrome

4. Berger, R. L., Sidd, J. J., and Ramaswamy, K. Retrograde vertebral-artery flow produced by correction of subclavian steal syndrome. N e w Eng. J . M e d . 277:64, 1967. 5. Blalock, A., and Taussig, H. B. T h e surgical treatment of malformations of the heart in which there is pulmonary stenosis or pulmonary atresia. J . A . M . A . 128: 189, 1945. 6. Bosniak, M. A. A collateral pathway through the vertebral arteries associated with obstruction of the innominate and proximal subclavian arteries. Radiology 81:89, 1963. 7. Bradley, W. G. Congenital aortic arch abnormalities with the “subclaviansteal” pattern of blood flow. Brit. Heart J. 28:718, 1966. 8. Callow, A. D. Surgical management of varying patterns of vertebral-artery and subclavian-artery insufficiency. N e w Eng. J. M e d . 270:546, 1964. 9. Cameron, D. J., and Wright, I. S. Subclavian steal syndrome with olfactory hallucinations. Ann. Intern. M e d . 61: 128, 1964. 10. Carpenter, S. Injury of the neck as cause of vertebral artery thrombosis. J . Nezirosurg. 18:849, 1961. 11. Clark, K., and Perry, M. D. Carotid vertebral anastomosis: An alternate technique for repair of the subclavian steal syndrome. Ann. Szwg. 163:414, 1966. 12. Coder, D. M., Frey, R. L., Bernaty, P. E., and Sheps, S. G. Symptomatic bilateral subclavian steal. Mayo Clin. Proc. 40:473, 1965. 13. Conrad, M., Toole, J. F., and Janeway, R. Hemodynamics of the upper extremities in subclavian steal syndrome. Circulation 32:346, 1965. 14. Contorni, L. I1 circolo collaterale vertebra-vertebrale nella obliterazione dell’arteria succlavia alla sue origine. Mineroa Chir. 15:268, 1960. 15. Couves, C. M., Hilliard, J. R., and Pribram, H. F. W. Abnormalities of the vertebrobasilar circulation due to subclavian artery disease. Canad. M e d . Ass. J . 88:343, 1963. 16. Craddock, D. R., and Logan, A. T h e subclavian steal and its surgical management. Brit. J . Surg. 53:926, 1966. 17. Crawford, F. S., De Bakey, M. E., Blaisdell, F. W., Morris, G. C., and Fields, W. S. Hemodynamic alterations in patients with cerebral artery insufficiency before and after operation. Surgery 48:76, 1960. 18. Creel, W., Powers, S., Jr., and Bloomsliter, P. C. Tonal sensation as a criterion of vertebral artery insufficiency. Arch. Surg. (Chicago) 98:309, 1967. 19. Cronquist, S. Vertebral catheterization via the femoral artery. Acta Rndiol. [Ther.](Stockholm) 55: 113, 1961. 20. Curry, J. L., and Howland, W. J. Subclavian steal syndrome: Pitfalls in its diagnosis. Amer. J . Roentgen. 91: 1254, 1964. 21. Daicoff, G. R., Lancaster, J. R., Ranniger, K., and Moulder, P. V. Rationale for aorta-subclavian artery bypass. J. Thorac. Cardiovnsc. Surg. 49: 945, 1965. 22. Dandy, W. E. Zntracranial Arterial Aneurysms. Ithaca, N.Y.: Conistock, 1944. P. 98. 23. Dardik, H., Gender, S., Stern, W., and Glotzer, P. Subclavian steal syndrome secondary to embolism. Ann. Surg. 164:171, 1966. 24. Daves, M. L., and Treger, A. Vertebral grand larceny. Circu/ntion 29:911, 1964. 25. Dumanian, A. V., Frahm, Cl. J., Pascale, L. R., Teplinsky, L. L., and Santschi, D. R. T h e surgical treatment of the subclavian steal syndrome. J. Thorac. Cardiovasc. Surg. 50:22, 1965. 26. Ehrenfeld, W. K., Harris, J. D., and Wylie, E. J. Vascular “steal” phenomenon: An experimental study. Amer. J. Surg. 116: 192, 1968. 27. Elkin, D. C., and Harris, M. H. Arteriovenous aneurysm of the vertebral vessels: Report of ten cases. A n n . Surg. 124:934, 1946.

PICCONE AND LEVEEN 28. Ethier, R. Observations on retrograde vertebral blood flow. Amer. 1. Roentgen. 91:1245, 1964. 29. Fields, W. S. Technique of Surgical Therapy. In C. H. Millikan, R. G. Siekert, and J. P. Whisnant (Eds.), Cerebral J7ascular Diseases. New York: Grune & Stratton, 1961. 30. Fisher, C. M. Editorial. New Eng. J . Med. 265:912, 1961. 31. Folger, G. U., and Shah, K. D. Subclavian steal in patients with BlalockTaussig anastomosis. Circulation 31:241, 1965. 32. French, L. A., and Haines, G. L. Unilateral vertebral artery ligation: Report of a case ending fatally with thrombosis of the basilar artery. 1. Neurosurg. 7: 156, 1950. 33. Gerard, F. P., and Sabety, A. M. Subclavian steal syndrome. Arch. Surg. (Chicago) 93:984, 1966. 34. Gerber, N. Congenital atresia of the subclavian artery producing the “subclavian steal syndrome.” Amer. 1. Dis. Child. 113:709, 1967. 35. Gonzalez, L. L. Personal communication, 1969. 36. Gonzalez, L. L., Wiot, J. F., and Boyd, A. D. Retrograde flow in the vertebral artery. Arch. Surg. (Chicago) 91: 185, 1965. 37. Gorman, J. F., Navarre, J. R., and McLean, H. Subclavian steal syndrome. Arch. Surg. (Chicago) 88:350, 1964. 38. Grollman, J. H., and Horns, J. W. The collateral circulation in coarctation of the aorta with a distal subclavian artery. Radiology 83:622, 1964. 39. Handa, J., Ishikawa, S., Huber, P., and Meyer, J. S. Experimental production of the “subclavian steal”: Electromagnetic flow measurements in the monkey. Surgery 58:703, 1965. 40. Hardesty, W., Roberts, B., Toole, J. F., and Royster, H. P. Studies on carotid arterial flow. Surgery 49:251, 1961. 41. Hardesty, W. H., Whitacre, W. B., Toole, J. F., Randall, P., and Royster, H. P. Studies on vertebral blood flow in man. Surg. Gynec. Obstet. 116: 662, 1963. 42. Harper, J. A., Golding, A. L., Mazzei, E. A., and Cannon, J. A. An experimental hemodynamic study of the subclavian steal syndrome. Surg. Gynec. Obstet. 124:1212, 1967. 43. Henzel, J. H., Pories, W. J., Burget, D. E., and Smith, J. L. Subclavian steal: Evaluation and report of three cases. Amer. Surg. 32:591, 1966. 44. Heyman, A., Young, W. G., Jr., Dillon, J., Goree, J. A., Klein, L. J., and Tindall, G. Cerebral ischemia caused by occlusive lesions of the subclavian or innominate arteries. Arch. Neurol. (Chicago) 10:581, 1964. 45. Irvine, W. T., Luck, R. J., Sutton, D., and Walpita, P. R. Intrathoracic occlusion of great vessels causing cerebrovascular insufficiency. Lancet 1: 1177, 1963. 46. Javid, H., Julian, 0. C., Dye, W. S., and Hunter, J. A. Management of cerebral arterial insufficiency caused by reversal of flow. Arch. Surg. (Chicago) 90:634, 1965. 47. Johnson, T. E. Angiography in the general practice of radiology. Radiology 81:38, 1963. 48. Jones, T. W., Vetto, R. R., Winterscheid, L. C., Dillard, D. H., and Merendino. K. A. Arterial complications incident to cannulation in open-heart ’surgery with special ref&ence to the femoral artery. Ann. Surg. 152:969, 1960. 49. Kety, S. S., and Schmidt, C. F. The nitrous oxide method for the quantitative determination of cerebral blood flow in man: Theory, procedure, and normal values. J . Clin. Invest. 27:476, 1948. 50. Killen, D. A., Foster, J. H., Gobbel, W. G., Jr., Stevenson, S. E., Collins, H. A,, Billings, F. T., and Scott, H. W., Jr. The subclavian steal syndrome. J . Thorac. Cardiovasc. Surg. 51:539, 1966.

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Subclavian Steal Syndrome

51. Killen, D. A., a n d Gobbel, W. G., Jr. Subclavian steal-carotid recovery phenomenon. J . Thorac. Cardiovasc. Surg. 50:421, 1965. 52. Lam, C. R. T h e choice of the side for approach in operations for pulmonary stenosis. J . Thorac. Cnrdiovasc. Surg. 18:661, 1949. 53. Lee, R., Kieraldo, J. H., and Jamplis, R. W. Surgical treatment of the subclavian steal syndrome. Amer. J. Surg. 114:308, 1967. 54. LeVeen, H. H., and Piccone, V. A. Nylon-band chest closure. Arch. Szirg. (Chicago) 96: 36, 1968. 55. Lewis, W. H. Anatomy of the Human Body by Henry Gray (21st ed.). Philadelphia: Lea & Febiger, 1924. P. 1417. 56. Lochaya, S. Pseudocoarctation of the aorta with bicuspid aortic valve and kinked left subc!avian artery: A possible cause of subclavian steal. Amer. Heart J . 73:369, 1967. 57. Mandelbaum, I. Spontaneous resolution of traumatic subclavian steal syndrome. Amer. Swg. 165:314, 1967. 58. Mannick, J. A., Suter, C. G., and Hume, D. M. T h e “subclavian steal” syndrome: A further documentation. J.A.M.A. 182:254, 1962. 59. Marshall, R. J., and Mantini, E. L. Dynamics of collateral circulation in patients with subclavian steal. Circulation 31:249, 1965. 60. Massumi, R. A. T h e congenital variety of the “subclavian steal” syndrome. Cirru!ation 28: 1149, 1963. 61. McClenathan, J. M. Correction of retrograde vertebral artery flow and acquired coarctation of the aorta. New Eng. J . Med. 268:517, 1963. 62. McLaughlin, J. S., Linberg, E., Attar, S., Wolfel, D., and Cowley, R A. Cerebral vascular insufficiency: Syndromes of reversed blood flow in vessels supplying the brain. Amer. Surg. 33:317, 1967. 63. Millikan, C., and Siekert, R. Studies in cerebral vascular disease: I. Syndrome of intermittent insufficiency of the basilar arterial system. Proc. StaffMeet. Mayo Clin. 30:61, 1955. 64. Molloy, P. J., and Jones, E. W. Management of the subclavian steal syndrome. Thorax 21:347, 1967. 65. Murray, D. S. Post-traumatic thrombosis of the internal carotid and vertebral arteries after non-penetrating injuries of the neck. Brit. J. Szirg. 44:556, 1957. 66. Nemir, P., Jr., Bahabozorgin, S., and Wagner, D. E. Brachial-basilar insufficiency in the subclavian steal syndrome. J . Thorac. Cardiovasc. Surg. 50: 534, 1965. 67. Newton, T. H., and Wylie, E. J. Collateral circulation associated with occlusion of proximal subclavian and innominate arteries. Amer. J . Roentgen. 91:394, 1964. 68. North, R. R., Fields, W. S., De Bakey, M. E., and Crawford, E. S. Brachialbasilar insufficiency syndrome. Neurology 12:810, 1962. 69. Parrott, J. C. T h e subclavian steal syndrome. Arch. Surg. (Chicago) 88:661, 1964. 70. Patel, A., and Toole, J. F. Subclavian steal syndrome: Reversal of cephalic b!ood flow. Medicine (Baltimore) 44:289, 1963. 71. Philip, T., Samuel, E., and Duncan, J. G. Reversed vertebral artery blood flow in subclavian artery obstruction (subclavian steal). Clin. Radiol. 14:310, 1963. 72. Piccone, V. A., Karvounis, P., and LeVeen, H. H. T h e subclavian steal syndrome. Angiology. In press. 73. Pineda, A., and Smith, J. L. T r u e and false subclavian syndromes. Arch. Surg. (Chicago) 92:258, 1966. 74. Pizarro, A. R., and Roth, 0. T h e subclavian steal syndrome: A case report. Vasc. Dis.2:322, 1965. VOL.

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Subclavian Steal Syndiome

100. Toole, J. F. Reversed vertebral-artery flow. Subclavian-steal syndrome. Lancet 1:872, 1964. 101. Toole, J. F., and Tulloch, E. F. Bilateral simultaneous sphygmomanometry: A new diagnostic test for subclavian steal syndrome. Circulation 33:952, 1966. 102. Vianna, F. C., Borges, S., Bocanegra, J., GuinarPes, R., Gallucci, C., Yunis, C., Algranti, N., Balbo, R., Casanova, R., and Forte, V. Left aortic coarctation with post-coarctation subclavian collateral circulation through the vertebral arteries. Arq. B r a d . Cardiol. 14:261, 1964. 103. Webb, W. R., and Burford, T. H. Gangrene of arm following use of subclavian artery in a pulmonosystemic anastomosis. J. Thorac. Surg. 23: 199, 1952. 104. Wheeler, H. B. Surgical treatment of subclavian artery occlusions. N e w Eng. J. M e d . 276:711, 1967. 105. Williams, C. L., Scott, S. M., and Takaro, T. Subclavian steal. Circulation 28:14, 1963. 106. Yum, K. Y., and Myers, R. N. Vertebral artery ligation in management of the subclavian steal syndrome. Arch. Surg. (Chicago) 98: 199, 1969.

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