RETROGRADE CEREBRAL EMBOLISM L. A. WILSON A. L. PRIOR A. K. YATES R. G. GOSLING R. W. ROSS RUSSELL
Guy’s Hospital and St. Thomas’ Hospital, London Cerebral embolism may complicate lesions of the subclavian arteries or aortic isthmus distal to the origins of the vertebral or carotid arteries. This may be due to retrograde propagation of occlusive thrombus. In other cases the vessels are patent but there are periods of reverse blood flow, creating a potential for reflux of embolic material to the ostia of the neck vessels.
Introduction CEREBRAL embolism is usually caused by disease in or neck arteries. However, it may complicate subclavian-artery disease distal to the origin of the vertebral arteries1-3 and has been suggested to arise from aortic plaques immediately distal to the origin of the left subclavian artery.4 We report here five such cases of cerebral embolism and discuss the mechanism and implications for clinical management.
artery lumen in case 1 in relation occlusion of the axillary artery.
Case-reports Case1 A left-handed managed 35, presented with a two-month history of aching discomfort in the right upper arm, exacerbated by use of that limb. He had also noted tingling in the fingers of the right hand, particularly the ring and little fingers. When exposed to cold the hand turned pale and blue and the fingertips became painful. At examination the abnormal findings were a right supraclavicular bruit, absence of right arm pulses, and coldness and discoloration of the right hand. A right cervical rib was evident at X-ray. Doppler ultra-
sound measurement of blood velocities demonstrated compression of the right subclavian artery, varying with head position, with complete block from the distal end of the axillary artery. Angiography (fig. 1) showed dilatation and irregularity of the lumen of the right subclavian artery in relation to the cervical rib and total occlusion of the axillary artery about 10 cm distally with faint filling of forearm vessels. Surgery was planned but, eleven days after initial investigation, he suddenly lost the use of his left arm and leg and his face became twisted. There was no headache, vomiting, or loss of consciousness. Examination confirmed a dense left hemiplegia. Speech, sensation, and the visual fields remained normal. Computerised tomography showed a large area of low attenuation deep in the right cerebral hemisphere in middle-
JA, Hoevels J, Simert G, Tylen U, Vang J. Clinical aspects of nonsurgical percutaneous transhepatic bile drainage in obstructive lesions of the extrahepatic bile ducts. Ann Surg 1976; 189: 58-61. 9. Ring EJ, Oleaga JA, Freiman DB, Husted JW, Lunderquist A. Therapeutic applications of catheter cholangiography. Radiology 1978; 128: 333-38. 10. Dawson JL. Jaundice and anoxic renal damage: protective effect of mannitol. Br Med J 1964; i: 810-11. 11. Bomzon L, Kew MC, Rosendorff C. The effect of phenoxybenzamine and saralasin on the altred renal blood flow associated with obstructive jaundice in baboons. Clin Exp Pharmacol Physiol 1977; 4: 365-73. 12. Bomzon L, Witton PB, McCalden A. Impaired skeletal muscle vasomotor response to infused noradrenaline in baboons with obstructive jaundice. Clin 8. Hansson
Sci Mol Med 1978; 55: 109-12. Rheingold OJ, Butson D, et al. Relief of malignant obstructive jaundice by percutaneous insertion of a permanent prosthesis in the biliary tree. Ann Intern Med 1978; 89: 589-93.
13. Pereiras V,
the right subclavian the cervical rib, with
cerebral-artery distribution. Doppler ultrasound now showed a striking change in the blood-velocity pattern in the proximal part of the right subclavian artery, suggesting extension of occlusion to its proximal part. At operation the right subclavian artery was found to be thrombosed to its origin, with considerable periarterial inflammation in relation to the large cervical rib. The cervical rib was excised and a right cervical sympathectomy performed. Treatment continues with anticoagulants and rehabilitation.
Case 2 A 21-year-old left-handed woman presented eight weeks after csesarean section following a sudden attack of weakness and loss of feeling in the left arm. This was associated with drooping of her left lower face, some word-finding difficulty, and impaired vision to the left with an impression of glare in the left eye. This episode lasted about four minutes and was followed by complete recovery. A year before she had had a similar attack. Examination revealed a pulsatile swelling at the base of the neck on the right, over which a loud systolic bruit was audible. Head turning to the left caused reduction or disappearance of the right arm pulse. She was normotensive, with no abnormality on cardiac or neurological examination. Plain chest X-ray revealed bilateral cervical ribs. Selective angiography showed no abnormality of either carotid artery or the left subclavian artery; there was stenosis of the right subclavian artery with dilatation in relation to the anterior end of the right cervical rib. Doppler ultrasound measurement of blood-flow velocities in the left subclavian artery showed a normal pattern and a minimal disturbance on head rotation. However, in the right subclavian artery with the head in a central position, there was a pronounced oscillation in the flow pattern proximal to the stenosis. There were three periods of reverse flow in each cardiac cycle. Further, with head rotation to the left or right there was progressive reduction in the brachial flow velocities and almost complete cessation of brachial flow when the head was rotated to the extreme left (fig. 2). Three further similar transient ischæmic attacks occurred. At operation the scalenus anterior and the fibrous band com-
Fig. 2-Effect velocities in
of head turning to the left on right brachial blood case 2 before (visit 1) and after operation (visit 2).
the subclavian artery were divided. The cervical rib, which the lower brachial plexus and subclavian artery arched, was removed. The right subclavian artery was pulsatile with no palpable occlusion of the lumen, so the artery was not opened. The patient recovered uneventfully and has had no further cerebral ischsemic attacks in the three years since operation. Postoperative ultrasound examination showed a normal right brachial sonogram with no change on head turning.
4-Dilatation and lumen in case 3.
A 38-year-old man complained of numbness and tingling in the left hand for three years, especially with exposure to cold. For the three weeks preceding admission to hospital these symptoms had been much more intense. With lifting at work the left arm became numb, weak, and painful, these symptoms being relieved only be rest. He had also noted that his left arm was colder than his right. Three weeks previously he had suddenly developed vertigo and loss of control of his limbs so that he could not walk properly. These symptoms resolved over three days. The day before admission he had a sudden recurrence of vertigo with diplopia and incoordination of his arms and legs. Again these symptoms resolved, but thereafter he noted impairment of vision to the left. At examination the left forearm and hand were cold, and no pulses could be felt below the middle of the upper arm. The left subclavian artery was prominent and pulsatile. Blood pressure and heart sounds were normal, and no bruits were heard over any vessels. There was a left homonymous hemianopia with central sparing, but no other neurological abnormalities were found. Plain X-rays showed bilateral cervical ribs. Doppler ultrasound (fig. 3) showed pronounced oscillatory flow velocities in the left subclavian artery, the retrograde flow increasing on head turning to either side, with complete arter-
of the left subclavian artery
ial block 10 cm proximal to the antecubital fossa. A smaller flow disturbance was demonstrated in theright subclavian artery, also with a retrograde component. At angiography the vertebral and carotid arteries were normal. There was some dilatation of the right subclavian artery distal to the right cervical rib. The lumen of the left subclavian artery (fig. 4) was irregular in relation to the large left cervical rib, with an adjacent dilatation. The left brachial artery in the upper arm and two major branches of the posterior circumflex humeral artery were occluded. The left cervical rib and a fibromuscular band were excised. The subclavian artery was not opened. Postoperatively treatment continued with anticoagulants. The pulses remained absent, but the hand was warmer and virtually free of symptoms. Repeat angiography showed no evidence of thrombus or other obstruction of the subclavian artery.
Case 4 A
in all four limbs, causing her to fall to the floor without loss of consciousness. Weakness of the left arm resolved over the next two days. She was not taking any medication. Ten years previously, in a motor-cycle accident, she had sustained injuries to her head, chest (with a pneumothorax), and left hip (with fracture-dislocation). Subsequently, a persistent right Horner’s syndrome and a left foot-
speech difficulty and weakness
drop were documented. Six days after the recent event, examination showed nonfluent dysphasia, constructional dyspraxia, a right Horner’s syndrome, and a right homonymous hemianopia. On the right there was weakness of the lower face, weakness of pyramidal distribution, cortical sensory loss in the arm and leg, hyperreflexia, and an extensor plantar response. On the left there was impairment of joint-position sense in the hand and foot
Fig. 3-Doppler-shift (proportional
grams from left subclavian artery in case 3. Retrograde flow velocities with the head central (F) considerably on head turning to the right (R) or left (L).
and weakness of dorsiflexion of the foot and toes and of eversion and slightly of inversion of the foot. The optic fundi were normal. Blood pressureaveraged 1501100 mm Hg. A systolic bruit was heard over the upper precordium. Computerised axial tomography showed a large infarct in left-middle-cerebral-artery distribution, and a moderate-sized infarct in the posterior frontal and anterior parietal lobes on the right. The electrocardiogram, echocardiogram, and haematological findings were normal. Chest radiograph showed an aneurysm of the aortic isthmus, with a thin rim of calcification. Arch aortogram (fig. 3) confirmed the presence of an
sponses became extensor. White bodies were observed to traverse the retinal arteries in the right eye. Carotid-artery pulses remained normal. Cerebrospinal fluid was normal.
In’an effort to prevent further embolism, the right common carotid artery was ligated and, through a separate incision, the right subclavian artery was ligated proximal to the aneurysm. The patient remained unconscious and died two days later. At necropsy massive infarction of the right cerebral hemisphere was found. Aneurysmal dilatations of both subclavian arteries were filled with laminated ante-mortem thrombus which on the right extended continuously back into the innominate artery. The aortic arch and the innominate and both subclavian arteries showed severe atheroma. Several pieces of ante-mortem thrombus were impacted against the proximal side of the common-carotid-artery ligature. Distal to this ligature, a saddle embolus at the common-carotid bifurcation obstructed both the external and internal carotid arteries. Otherwise the vessels in the neck and at the base of the brain were all patent and free from atheroma.
Fig. 5-Aortic aneurysm seen at angiography in case 4. aortic aneurysm arising just distal to the origin of the left subclavian artery; there was no evidence of dissection and no abnormality of the proximal aorta, left carotid artery, or vertebral arteries; the right internal carotid artery was occluded at its origin. At operation, after three months’ rehabilitation and anticoagulation, a Gott heparin-bonded bypass tube was inserted proximally into the arch of the aorta and distally into the mid descending thoracic aorta. The anerysm was excised, and aortic continuity was re-established with a knitted ’Dacron’ graft. Microscopical examination confirmed the pathological features of a long-standing traumatic aneurysm. There was no intraluminal clot. The patient made a good postoperative recovery.
Case 5 A 50-year-old man complained of numbness in his right forearm for two months. For several weeks he had had a dull ache in the right axilla and forearm and some weakness of the right hand. On examination, there was a smooth pulsating swelling above the medial half of the right clavicle. The right brachial and radial pulses were stronger than those on the left. Blood pressure in the right arm was 160/110 mm Hg, in the left arm
120/80 mm Hg. At angiography the right subclavian artery was dilated and 2 cm above the tortuous, with no filling of the vessel lateral margin of the scapula. The left subclavian artery was also widened and was occluded opposite the left first rib. The carotid arteries were normal. Two weeks later the patient suddenly developed headache and loss of vision in the right eye. The right arm pulses were absent and the right subclavian aneurysm was no longer pulsatile. Later that day, he suddenly became unconscious and developed twitching in the left arm and leg. Both plantar re-
Stroke due to cerebral embolism from arterial abnormalities such as these described has been attributed either to the reflux of embolic material during diastole and its subsequent carriage into the intracranial circulation during the ensuing systole4 or to the retrograde propagation of thrombus from the site of arterial disease back to the ostia of the neck vessels.5.6 The youth of our patients makes vascular lesions other than those discovered unlikely, and in none did investigation reveal any other potential source of embolism. In the presence of a cervical rib, as in the first three patients, the subclavian artery is liable to repeated trauma. The resulting localised arterial damage may be associated with mural thrombosis and distal embolism into the arm.7 Retrograde propagation of thrombus from damage to the subclavian and axillary arteries has been seen6,8 and has been held to be the means whereby emboli have gained access to the vertebral or right internal carotid arteries.9 Symonds was the first to suggest this as the mechanism for acute left hemiplegia in patients with cervical ribs, and this contention is supported by clinical, angiographic, and surgical evidence.3,10 This we considered the mechanism in our first case, the Doppler ultrasound and operative findings following the stroke indicating extension of occlusion of the right subclavian artery to its origin. Post-mortem examination of our fifth case also confirmed this mechanism. However, the subclavian artery has not always been occluded in such cases.3 Doppler ultrasound and angiography in our second and third patients demonstrated patency of the subclavian arteries. Furthermore, ultrasound studies provide evidence of another potential mechanism in such cases. The top two traces of fig. 6 show the distribution of Doppler-shift ultrasound frequencies (proportional to blood velocities) in the right subclavian artery in the mid-clavicular fossa of a normal subject, simultaneously with the Doppler-shift from the right common carotid artery at the base of the neck and the electrocardiogram and heart sounds. Both anterograde and retrograde flow occur across the whole subclavian lumen in cardiac systole, whereas the commoncarotid velocities are all forward. The accepted explanation for this phenomenon" is the differing amounts of reflection of the pressure pulse from the vascular beds served by these two arteries. The effect of diminishing
patient, with recent acute cerebral infarccardiac or vascular lesions as a potential sorce of embolism other than the typical post-traumatic aneurysm of the aortic isthmus. Reflux of blood occurs normally in the aortic arch during diastole. McCall3 described eight cases of cerebral infarction thought to be due to embolism in which necropsy revealed no source of emboli in the heart or neck vessels but an ulcerated plaque was found in the region of the aortic isthmus. Diastolic reflux of embolic material was the suggested mechanism in these cases. No evidence of retrograde propagation of thrombus was found in our patient, although she had had a period of anticoagulation before The fourth
sonograms in a normal subject from the left carotid and left subclavian arteries before and after
Fig. 6-Doppler common
the reflections to the subclavian artery by opening up the vascular beds of the forearm and hand by exercise is shown in the two lower traces of fig. 6. The velocity distributions in the two arteries are now almost identical. In cases 2 and 3 the blood-velocity distributions in the subclavian arteries concerned showed excessive reverse flow during cardiac systole and further small amounts of reverse flow in diastole at rest. In addition the initial amount of reverse flow was considerably increased by head turning to the right or the left (fig. 3). This is consistent with the progressive closure of the subclavian artery distal to the point of measurement as the head is turned to either side. The resultant area under the curve in fig. 3, with the head far right or left, is close to zero, indicating complete occlusion in these positions. The average flow velocities for those first periods of approximately 10 ms of retrograde flow were of the order-of 50 cm/s. Thus emboli from mural thrombus in the damaged subclavian artery might be swept back an average of 5 cm. It would therefore be possible for such emboli to enter the vertebral or right common carotid arteries during diastole of the same heart beat. Reflux of embolic material is therefore the probable explanation of stroke in these cases, the following cardiac contraction carrying the embolic material into the right internal carotid artery from the innominate artery or into the vertebral arteries. Barnett12 has postulated a somewhat similar mechanism of embolism from the study of occluded internal carotid arteries, emboli reaching the brain through the external carotid artery having been "scoured out" of the carotid stump during systole.
We conclude that reflux of emboli from thrombus in the subclavian arteries and aortic isthmus may result in stroke. Furthermore, reflux of embolic material to the brain may complicate forcible unblocking of arteriovenous shunts’3 and retrograde aortic perfusion. 14 We use the Gott shunt routinely when operating on aneurysms in the region of the aortic isthmus, since this technique reduces the risk of reflux embolism. Atriofemoral and femoro-femoral bypass both increase the potential for retrograde embolism in patients with aortic lesions. The presentation of the first four patients to one hospital in the past three years indicates a need to consider such distal arterial lesions in the investigation of patients with strokes, especially in young patients in whom strokes are often embolic in origin. The usefulness of Doppler ultrasound in the investigation of possible thoracic-inlet syndromes is apparent. The evidence is that stroke may complicate such lesions by two mechanisms-by retrograde propagation of thrombus from sites of arterial damage or by reflux of embolic material from such sites. We thank Mr F. G. Ellis and Dr R. K. Knight for permission to report cases under their care and Dr R. D. Hoare and Dr H. M. Saxton for angiography.
Requests for reprints should be addressed to L. A. W., of Neurology, Guy’s Hospital, London SE 1 9RT.
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