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Acute hyperperfusion syndrome complicating EC-IC bypass
  1. S I Stiver,
  2. C S Ogilvy
  1. Cerebrovascular Surgery, Neurosurgical Service, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts, USA
  1. Correspondence to:
 Dr Shirley I Stiver, Beth Israel Deaconess Medical Center, Boston, Massachusetts, USA;
 sstiver{at}caregroup.harvard.edu

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The extracranial-intracranial (EC-IC) arterial bypass study has been criticised for failing to select for patients with chronic haemodynamic insufficiency and for revascularisation with low flow grafts, which may augment perfusion inadequately.1 We report a case of EC-IC bypass in a patient with severe intracranial carotid stenosis and compromised cerebrovascular reserve, which was complicated by intraoperative hyperperfusion syndrome. Hyperperfusion syndrome as a result of EC-IC bypass is not well documented and its occurrence directly after bypass has not been reported before. We discuss the pathophysiology and prophylactic measures of this complication, with special attention to the nature of the bypass performed.

A 48 year old right handed woman presented with a four month history of recurrent transient ischaemic attacks characterised by left sided symptoms of perioral paraesthesia, hand numbness, and upper extremity weakness (grade 4/5). The attacks were refractory to treatment with ticlid, a platelet aggregation inhibitor, and at the time of admission to hospital she was having several episodes daily, each lasting up to 15 minutes. She was therapeutically heparinised, her blood pressure was augmented to 150–180 mm Hg with intravenous vasopressors, and florinef treatment was begun to expand her vascular volume. The transient ischaemic attacks persisted unabated despite three weeks of this regimen in the intensive care unit.

Preoperative T2 weighted magnetic resonance images revealed a few small scattered subcortical signal changes, but no evidence of a previous cerebrovascular event. Cerebral angiography showed severe right supraclinoid internal carotid artery and proximal right M1 stenoses with contribution to filling of the middle cerebral tree from pial collaterals. The cervical carotid arteries were normal. Transcranial Doppler studies with carbon dioxide vasodilatation challenge showed flow limiting stenosis with compromised cerebrovascular reserve.

On the basis of these data and the refractory nature of the symptoms, we decided to proceed with a high flow revascularisation procedure. An autologous saphenous vein graft was inserted into a proximal M2 branch and the external cervical carotid artery in end to side fashion. During this time the patient's systolic blood pressure was maintained between 160 and 180 mm Hg, and she had been cooled to 34°C and treated with 20% mannitol (100 g). An intraoperative angiogram, performed immediately after completion of the anastomoses, confirmed patency of the bypass graft and normal filling of the middle cerebral tree.

As we were preparing to close the craniotomy, approximately 45 minutes after flow was established through the bypass graft, the brain became massively swollen. A temporary clip was placed across the graft, and the brain relaxed, becoming soft with return of pulsatility. A second intraoperative angiogram showed evidence of hyperperfusion syndrome with the presence of a dense vascular blush throughout the middle cerebral tree (fig 1). Attempts to limit flow through the graft failed and a permanent clip was placed across the graft. Postoperative serial computed tomography showed intracranial haemorrhage and cerebral oedema with progressive mass effect, commensurate with a worsening neurological state. After discussions with the family, aggressive supportive measures were withdrawn and the patient died.

Symptoms of intracranial stenotic lesions are usually haemodynamic in aetiology and develop after the collateral blood supply fails to support metabolic demands despite maximum oxygen extraction. Management of patients refractory to treatment with antiplatelet or anticoagulant agents, blood pressure augmentation, and blood volume expansion is difficult. There is a high risk of stroke, and several studies have argued strongly in favour of EC-IC bypass in these patients. Consequently, a decision was made in this case to carry out a high flow bypass from the external carotid artery to an M2 branch of the middle cerebral artery. The long nature of the lesion in the supraclinoid carotid, extending into the proximal M1 segment, was judged not amenable to angioplasty. We failed to consider seriously the use of a low flow bypass graft.

Hyperperfusion following cerebral revascularisation is well recognised, particularly in the context of carotid endarterectomy. Its occurrence secondary to EC-IC bypass is not surprising. Intracerebral haemorrhages can complicate both superficial temporal artery to middle cerebral artery (STA-MCA) and saphenous vein EC-IC bypasses for carotid occlusive disease, but evidence for hyperperfusion as the underlying cause of these haemorrhages is not established. A dense perfusion blush on the intraoperative angiogram documented hyperperfusion following connection of the EC-IC bypass in this case (fig 1). In chronically ischaemic brain, hyperperfusion syndrome is thought to arise as a result of disturbed cerebral autoregulation.2 The vasculature is maximally dilated and following restoration of flow vascular reactivity is impaired and unable to vasoconstrict appropriately, to protect the capillary bed against the increased perfusion pressure. Low signal oedematous changes and cerebral haemorrhage result, as was evidenced on postoperative computed tomography in this case.

Several factors led to the development of hyperperfusion syndrome in our case. Preoperatively we failed to recognise that altered microvascular permeability of the chronically hypoperfused brain may lower the safe threshold for ischaemia and hypertension.3 Despite neuroprotective measures, temporary occlusion of the M2 branch for the bypass may have resulted in a serious degree of ischaemia, and our routine practice of modestly raising the patient's blood pressure during temporary clipping may have been detrimental in this setting. Given the increased susceptibility of the chronically ischaemic blood brain–barrier to injury, the choice of a high flow bypass was in retrospect an error. Depending on the diameter of the graft, saphenous vein bypass grafts provide flows to 110 ml/min.4 By comparison, STA-MCA bypasses generate flows through the graft in the range of 10 to 60 ml/min (mean, 28 ml/min).5 Revascularisation is instituted to rescue tissue with blood flows of 20–25 ml/100 g/min from dropping to 10–15 ml/100 g/min leading to cell death.6 This incremental augmentation of blood flow can be achieved by a low flow STA-MCA bypass with a lower risk of complications. Over time, adaptation will occur, allowing increased flow through the bypass graft to be tolerated more safely than if an ischaemic brain is subjected acutely to these high flows.

Patients with intracranial stenosis and compromised cerebrovascular reserve—highlighted as a group most likely to benefit from EC-IC bypass—are at high risk for hyperperfusion syndrome. Strict attention to judicious choice of bypass conduit, minimising ischaemic time for the anastomosis, optimal neuroprotection, and meticulous control of blood pressure and intravenous fluids is mandatory to minimise complications of hyperperfusion syndrome and optimise the potential benefit of EC-IC bypass in these patients.

Figure 1

Intraoperative right carotid artery angiogram showing hyperperfusion, as evidenced by a dense vascular blush in the middle cerebral artery distribution.

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