Cerebral revascularisation: where are we now?
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《神经病学神经外科学杂志》
1 University Department of Neurosurgery, Addenbrooke’s Hospital, Cambridge, UK
2 Department of Neurosurgery (TTSH Campus), National Neuroscience Institute, Singapore
Correspondence to:
Mr P J Kirkpatrick
University Department of Neurosurgery, Block A Level 4, Addenbrooke’s Hospital, Cambridge CB2 2QQ, UK; pjk21@medschl.cam.ac.uk
Outcomes may be improved by standardising measurement of CBF and the surgical approach and centralising expertise
Keywords: cerebral blood flow; cerebrovascular reactivity; ec-ic bypass
Enthusiasm for delivering an alternative blood supply to the brain by surgical means has waxed and waned for over three decades. In situations where a major cerebral vessel is sacrificed for removal of macroscopic pathology (such as a skull base tumour or giant intracranial aneurysm), the need to replace lost cerebral blood flow (CBF) is obvious and often required as part of a staged surgical procedure.1,2 In such cases, the need and type of surgical bypass graft (high or low flow) is dictated by the presence or absence of adequate collateral vascular pathways, the design of the circle of Willis, and any extracranial to intracranial (EC-IC) vascular connections.3 Detailed cranial angiography and observation of the clinical and physiological responses to temporary test occlusion of parent vessels provide the relevant information. When reliably practised, daunting cervical and cranial pathologies can be approached confidently with acceptable morbidity.4 Although simple in principle, techniques for assessing the need for surgical bypass procedures are not always practised resulting in incomplete treatments, and/or high surgical morbidity from cerebral strokes. Centralisation of expertise and adoption of a more appropriate referral of difficult pathology will serve to address the variation in practice for such cases.
CEREBRAL REVASCULARISATION IN CHRONIC VASCULAR OCCLUSION
A far more intense debate surrounds the indications for cerebral revascularisation in the treatment of chronic vascular occlusive disease. Extracranial atheromatous degenerative vascular disease is by far the commonest pathological entity falling into this group,5,6 although intracranial atheroma and chronic inflammatory disease (Moya Moya) is significant in Eastern communities. Patients usually present with neurological events leading to investigation and identification of occlusive disease. However, unlike stenotic disease, occluded vessels do not attract a high risk of future embolic events.5–7 Most patients achieve normal or near normal CBF by means of the aforementioned collaterals. Only a minority of those who survive the occlusion without an immediate major stroke exist in a chronic state of low CBF. Accurate neurological evaluation of the presenting symptoms (retinal v cerebral) is clearly important in determining the risk of further clinical events.8 However, from a clinical and pathophysiological standpoint, these patients should be considered for CBF assessment and cerebral bypass surgery—not for CBF replacement but for CBF augmentation.9–11
WHY THE CONTINUED DEBATE?
Since the first description of an EC-IC bypass procedure by Yasargil,12 much harm has been done in the wide propagation of the procedure without resort to a sound physiological or clinical substrate, upon which to base the procedure. Most patients presenting with symptomatic carotid occlusive disease accommodate the pathology well; hence, most do not need a cerebral bypass. Undiscerning surgical practice raised medical concerns, the result was the controversial multicentre Cooperative Study (EC-IC Bypass Study) that failed to observe any benefit from the bypass procedure.13 The widespread surgical practice of EC-IC bypass collapsed, largely as a result of withdrawal of the funding mechanisms supporting the operation. Those who were more thoughtful in the application of EC-IC bypass procedures dissented.14–16 Why was there no selection of patients more suitable for the procedure, particularly those who were clinically symptomatic of cerebral hypoperfusion? Why were so many patients excluded from the study? Was the study cohort largely represented by patients in whom there was uncertainty? Indeed, was the uncertainty principle helpful in this regard? The Cooperative Study addressed only a part of contemporary surgical practice and failed to observe the basic physiological and clinical indications for the operation. A negative result was inevitable.
Some clinical doors remained open. Pioneers of selective EC-IC procedures have accumulated supporting and compelling information addressing a cohort of patients who attract high risks for future stroke, risks that reflect a chronic state of low CBF.9–11,17,18,19,20,21 Of the variety of techniques used to measure CBF, observations of baseline values are generally unhelpful. Activated studies measuring relative increases in CBF have greater predictive values for identifying those at risk.17–21 Hence a number of cerebrovascular reactivity indices have evolved which, although different, point in the same direction—impaired cerebrovascular reactivity is a risk factor for future strokes. Those with negative reactivity on acetazolamide activated xenon computed tomography (CT) have a 12-fold increase in incidence of stroke,22 and those with an increased oxygen extraction fraction indicating exhausted cerebrovascular reserve (measured using positron emission tomography (PET)) have an increased stroke risk of 30%.23,24 Likewise, severely impaired CBF reactivity to carbon dioxide (measured using transcranial Doppler flowmetry) also increases the risk by approximately 30%.18,25 Two ongoing randomised trials have adopted different physiological criteria upon which to base surgery. The North American Carotid Occlusion Surgery Study (COSS)26 is using PET derived oxygen extraction fraction, whereas the Japanese Extracranial to Intracranial Bypass Trial (JET)27 is using acetazolamide CBF activation measured with either single photon emission CT or xenon CT imaging. JET has already demonstrated significant short term gains for the surgical group, and the imaging modalities adopted have the obvious advantage of far wider clinical availability than PET derived indices.
The key questions remaining are:
What is the threshold for cerebral perfusion that defines the patient at risk?
Which technique for CBF measurement should be used?
Which cerebrovascular indices have the greatest sensitivity for prediction of stroke?
What are the absolute benefits of surgery?
What surgical procedure is best?
What rates for poor surgical outcome can be
Without a universally
CONCLUSION
With relatively small numbers of suitable cases, centralisation of expertise would be important for achieving a measure of surgical quality control. Once broad criteria for offering cerebral revascularisation have been
REFERENCES
Jafar JJ, Russell SM, Woo HH. Treatment of giant intracranial aneurysms with saphenous vein extracranial-intracranial bypass grafting: indications, operative technique and results in 29 patients. Neurosurgery 2002;51:138–46.
Sekhar LN, Bucur SD, Bank WO, et al. Venous and arterial bypass grafts for difficult tumours, aneurysms, and occlusive vascular lesions: evolution of surgical treatment and improved graft results. Neurosurgery 1999;44:1207–24.
Leibeskind DS. Collateral circulation. Stroke 2003;34:2279–84.
Tarr RW, Jungries CA, Horton JA, et al. Complications of pre-operative test occlusion of the internal carotid arteries: Experience in 300 cases. Skull Base Surg 1991;1:240–4.
Flaherrty ML, Flemming KD, McClelland R, et al. Population- based study of symptomatic internal carotid artery occlusion. Stroke 2004;35:349–52.
Pessin MS, Duncan GW, Mohr JP, et al. Clinical and angiographic features of carotid transient ischaemic attacks. N Engl J Med 1977;296:358–62.
Hankey GJ, Slattery JM, Warlow CP. The prognosis of hospital-referred transient ischaemic attacks. J Neurol Neurosurg Psychiatry 1991;54:793–802.
Klijn CJ, Kappelle LJ, van Huffelen AC, et al. Recurrent ischemia in symptomatic carotid occlusion: prognostic value of hemodynamic factors. Neurology 2000;26:1806–12.
Grubb RL, Derdeyn CP, Fritsch SM, et al. Importance of hemodynamic factors in the prognosis of symptomatic carotid occlusion. JAMA 1998;280:1055–60.
Yamauchi H, Fukuyama H, Nagahama Y, et al. Evidence of misery perfusion and risk for recurrent stroke in major cerebral arterial occlusive diseases from PET. J Neurol Neurosurg Psychiatry 1996;61:18–25.
Durham SR, Pentheny SL, Johnson DW. Increased stroke risk predicted by compromised cerebral blood flow reactivity. J Neurosurg 1993;79:483–9.
Yasargil MG. Anastomosis between the superficial temporal artery and a branch of the middle cerebral artery. In: Yasargil MG, ed. Microsurgery applied to neurosurgery. Stuttgart: Georg Thieme, 1969:105–15.
EC/IC Bypass Study Group. Failure of extracranial-intracranial arterial bypass to reduce the incidence of ischemic stroke. N Engl J Med 1985;313:1191–2000.
Ausman IA, Diaz FG. Critique of the extracranial-intracranial bypass study. Surg Neurol 1986;26:218–21.
Awad IA, Spetzler RF. Extracranial-intracranial bypass surgery: a critical analysis in light of the International Cooperative Study. Neurosurgery 1986;19:655–64.
Sundt TM. Was the international randomized trial of extracranial-intracranial arterial bypass representative of the population at risk? N Engl J Med 1987;316:814–16.
Gibbs JM, Leenders KL, Wise RJS, et al. Evaluation of cerebral perfusion pressure reserve in patients with carotid- artery occlusion. Lancet 1984;1:310–14.
Powers WJ, Tempel LW, Grubb RL Jr. Influence of cerebral hemodynamics on stroke: one year follow-up of 30 medically treated patients. Ann Neurol 1989;25:325–30.
Kleiser B, Widder B. Course of carotid occlusions with impaired cerebrovascular reactivity. Stroke 1992;23:171–4.
Ogasawara K, Ogawa A, Terasaki K, et al. Use of cerebrovascular reactivity in patients with symptomatic major cerebral artery occlusion to predict 5-year outcome: comparison of xenon-133 and iodine-123-IMP single-photon emission computed tomography. J Cereb Blood Flow Metab 2002;22:1142–8.
Kuroda S, Houkin K, Kamiyama H, et al. Long-term prognosis of medically treated patients with internal carotid or middle cerebral artery occlusion: can acetazolamide test predict it? Stroke 2001;32:2110–16.
Yonas H, Smith HA, Durham SR, et al. Increased stroke risk predicted by compromised cerebral blood flow reactivity. J Neurosurg 1993;79:483–9.
Derdeyn CP, Videen TO, Simmons NR, et al. Count-based PET method for predicting ischemic stroke in patients with symptomatic carotid arterial occlusion. Radiology 1999;212:499–506.
Yamauchi H, Fukuyama H, Nagahama Y, et al. Significance of increased oxygen extraction fraction in five-year prognosis of major cerebral arterial occlusive diseases. J Nucl Med 1999;40:1992–8.
Markus H, Cullinane M. Severely impaired cerebrovascular reactivity predicts stroke and TIA risk in patients with carotid artery stenosis and occlusion. Brain 2001;124:457–67.
Adams HP, Powers WJ, Grubb RL, et al. Preview of a new trial of extracranial to intracranial arterial anastomosis: the Carotid Occlusion Surgery Study. Neurosurg Clin North Am 2001;12:613–24.
Ogawa A . Cerebrovascular imaging and bypass surgery. Presented at the 1st Asian Pacific Stroke Conference against stroke. Hong Kong 2004.
Executive Committee for the Asymptomatic Carotid Atherosclerosis Study. Endarterectomy for asymptomatic carotid artery stenosis. JAMA 1995;273:1421–28.
Schmideck P, Piepgras A, Leinsinger G, et al. Improvement of cerebrovascular reserve capacity by EC-IC bypass surgery in patients with ICA occlusion and hemodynamic cerebral ischemia. 1994;81:236–44.
Gibbs JM, Wise RJS, Thomas DJ, et al. Cerebral hemodynamic changes after extracranial-intracranial bypass surgery. J Neurol Neurosurg Psychiatry 1987;50:140–50.
Powers WJ, Martin WRW, Herscovitch P, et al. Extracranial-intracranial bypass surgery: hemodynamic and metabolic effects. Neurology 1998;34:1168–74.
Samson Y, Baron JC, Bousser MG, et al. Effects of extracranial-intracranial arterial bypass on cerebral blood flow and oxygen metabolism in humans. Stroke 1985;16:609–16.
Yamashita T, Kashiwagi S, Nakano S, et al. The effects of EC-IC bypass surgery on resting cerebral blood flow and cerebrovascular reserve capacity studied with stable Xe-CT and acetazolamide test. Neuroradiology 1991;33:217–22.
Sasoh M, Ogasawara K, Kuroda K, et al. Effects of EC-IC bypass on cognitive impairment in patients with hemodynamic cerebral ischemia. Surg Neurol 2003;59:455–60.(P J Kirkpatrick1 and I Ng)
2 Department of Neurosurgery (TTSH Campus), National Neuroscience Institute, Singapore
Correspondence to:
Mr P J Kirkpatrick
University Department of Neurosurgery, Block A Level 4, Addenbrooke’s Hospital, Cambridge CB2 2QQ, UK; pjk21@medschl.cam.ac.uk
Outcomes may be improved by standardising measurement of CBF and the surgical approach and centralising expertise
Keywords: cerebral blood flow; cerebrovascular reactivity; ec-ic bypass
Enthusiasm for delivering an alternative blood supply to the brain by surgical means has waxed and waned for over three decades. In situations where a major cerebral vessel is sacrificed for removal of macroscopic pathology (such as a skull base tumour or giant intracranial aneurysm), the need to replace lost cerebral blood flow (CBF) is obvious and often required as part of a staged surgical procedure.1,2 In such cases, the need and type of surgical bypass graft (high or low flow) is dictated by the presence or absence of adequate collateral vascular pathways, the design of the circle of Willis, and any extracranial to intracranial (EC-IC) vascular connections.3 Detailed cranial angiography and observation of the clinical and physiological responses to temporary test occlusion of parent vessels provide the relevant information. When reliably practised, daunting cervical and cranial pathologies can be approached confidently with acceptable morbidity.4 Although simple in principle, techniques for assessing the need for surgical bypass procedures are not always practised resulting in incomplete treatments, and/or high surgical morbidity from cerebral strokes. Centralisation of expertise and adoption of a more appropriate referral of difficult pathology will serve to address the variation in practice for such cases.
CEREBRAL REVASCULARISATION IN CHRONIC VASCULAR OCCLUSION
A far more intense debate surrounds the indications for cerebral revascularisation in the treatment of chronic vascular occlusive disease. Extracranial atheromatous degenerative vascular disease is by far the commonest pathological entity falling into this group,5,6 although intracranial atheroma and chronic inflammatory disease (Moya Moya) is significant in Eastern communities. Patients usually present with neurological events leading to investigation and identification of occlusive disease. However, unlike stenotic disease, occluded vessels do not attract a high risk of future embolic events.5–7 Most patients achieve normal or near normal CBF by means of the aforementioned collaterals. Only a minority of those who survive the occlusion without an immediate major stroke exist in a chronic state of low CBF. Accurate neurological evaluation of the presenting symptoms (retinal v cerebral) is clearly important in determining the risk of further clinical events.8 However, from a clinical and pathophysiological standpoint, these patients should be considered for CBF assessment and cerebral bypass surgery—not for CBF replacement but for CBF augmentation.9–11
WHY THE CONTINUED DEBATE?
Since the first description of an EC-IC bypass procedure by Yasargil,12 much harm has been done in the wide propagation of the procedure without resort to a sound physiological or clinical substrate, upon which to base the procedure. Most patients presenting with symptomatic carotid occlusive disease accommodate the pathology well; hence, most do not need a cerebral bypass. Undiscerning surgical practice raised medical concerns, the result was the controversial multicentre Cooperative Study (EC-IC Bypass Study) that failed to observe any benefit from the bypass procedure.13 The widespread surgical practice of EC-IC bypass collapsed, largely as a result of withdrawal of the funding mechanisms supporting the operation. Those who were more thoughtful in the application of EC-IC bypass procedures dissented.14–16 Why was there no selection of patients more suitable for the procedure, particularly those who were clinically symptomatic of cerebral hypoperfusion? Why were so many patients excluded from the study? Was the study cohort largely represented by patients in whom there was uncertainty? Indeed, was the uncertainty principle helpful in this regard? The Cooperative Study addressed only a part of contemporary surgical practice and failed to observe the basic physiological and clinical indications for the operation. A negative result was inevitable.
Some clinical doors remained open. Pioneers of selective EC-IC procedures have accumulated supporting and compelling information addressing a cohort of patients who attract high risks for future stroke, risks that reflect a chronic state of low CBF.9–11,17,18,19,20,21 Of the variety of techniques used to measure CBF, observations of baseline values are generally unhelpful. Activated studies measuring relative increases in CBF have greater predictive values for identifying those at risk.17–21 Hence a number of cerebrovascular reactivity indices have evolved which, although different, point in the same direction—impaired cerebrovascular reactivity is a risk factor for future strokes. Those with negative reactivity on acetazolamide activated xenon computed tomography (CT) have a 12-fold increase in incidence of stroke,22 and those with an increased oxygen extraction fraction indicating exhausted cerebrovascular reserve (measured using positron emission tomography (PET)) have an increased stroke risk of 30%.23,24 Likewise, severely impaired CBF reactivity to carbon dioxide (measured using transcranial Doppler flowmetry) also increases the risk by approximately 30%.18,25 Two ongoing randomised trials have adopted different physiological criteria upon which to base surgery. The North American Carotid Occlusion Surgery Study (COSS)26 is using PET derived oxygen extraction fraction, whereas the Japanese Extracranial to Intracranial Bypass Trial (JET)27 is using acetazolamide CBF activation measured with either single photon emission CT or xenon CT imaging. JET has already demonstrated significant short term gains for the surgical group, and the imaging modalities adopted have the obvious advantage of far wider clinical availability than PET derived indices.
The key questions remaining are:
What is the threshold for cerebral perfusion that defines the patient at risk?
Which technique for CBF measurement should be used?
Which cerebrovascular indices have the greatest sensitivity for prediction of stroke?
What are the absolute benefits of surgery?
What surgical procedure is best?
What rates for poor surgical outcome can be
Without a universally
CONCLUSION
With relatively small numbers of suitable cases, centralisation of expertise would be important for achieving a measure of surgical quality control. Once broad criteria for offering cerebral revascularisation have been
REFERENCES
Jafar JJ, Russell SM, Woo HH. Treatment of giant intracranial aneurysms with saphenous vein extracranial-intracranial bypass grafting: indications, operative technique and results in 29 patients. Neurosurgery 2002;51:138–46.
Sekhar LN, Bucur SD, Bank WO, et al. Venous and arterial bypass grafts for difficult tumours, aneurysms, and occlusive vascular lesions: evolution of surgical treatment and improved graft results. Neurosurgery 1999;44:1207–24.
Leibeskind DS. Collateral circulation. Stroke 2003;34:2279–84.
Tarr RW, Jungries CA, Horton JA, et al. Complications of pre-operative test occlusion of the internal carotid arteries: Experience in 300 cases. Skull Base Surg 1991;1:240–4.
Flaherrty ML, Flemming KD, McClelland R, et al. Population- based study of symptomatic internal carotid artery occlusion. Stroke 2004;35:349–52.
Pessin MS, Duncan GW, Mohr JP, et al. Clinical and angiographic features of carotid transient ischaemic attacks. N Engl J Med 1977;296:358–62.
Hankey GJ, Slattery JM, Warlow CP. The prognosis of hospital-referred transient ischaemic attacks. J Neurol Neurosurg Psychiatry 1991;54:793–802.
Klijn CJ, Kappelle LJ, van Huffelen AC, et al. Recurrent ischemia in symptomatic carotid occlusion: prognostic value of hemodynamic factors. Neurology 2000;26:1806–12.
Grubb RL, Derdeyn CP, Fritsch SM, et al. Importance of hemodynamic factors in the prognosis of symptomatic carotid occlusion. JAMA 1998;280:1055–60.
Yamauchi H, Fukuyama H, Nagahama Y, et al. Evidence of misery perfusion and risk for recurrent stroke in major cerebral arterial occlusive diseases from PET. J Neurol Neurosurg Psychiatry 1996;61:18–25.
Durham SR, Pentheny SL, Johnson DW. Increased stroke risk predicted by compromised cerebral blood flow reactivity. J Neurosurg 1993;79:483–9.
Yasargil MG. Anastomosis between the superficial temporal artery and a branch of the middle cerebral artery. In: Yasargil MG, ed. Microsurgery applied to neurosurgery. Stuttgart: Georg Thieme, 1969:105–15.
EC/IC Bypass Study Group. Failure of extracranial-intracranial arterial bypass to reduce the incidence of ischemic stroke. N Engl J Med 1985;313:1191–2000.
Ausman IA, Diaz FG. Critique of the extracranial-intracranial bypass study. Surg Neurol 1986;26:218–21.
Awad IA, Spetzler RF. Extracranial-intracranial bypass surgery: a critical analysis in light of the International Cooperative Study. Neurosurgery 1986;19:655–64.
Sundt TM. Was the international randomized trial of extracranial-intracranial arterial bypass representative of the population at risk? N Engl J Med 1987;316:814–16.
Gibbs JM, Leenders KL, Wise RJS, et al. Evaluation of cerebral perfusion pressure reserve in patients with carotid- artery occlusion. Lancet 1984;1:310–14.
Powers WJ, Tempel LW, Grubb RL Jr. Influence of cerebral hemodynamics on stroke: one year follow-up of 30 medically treated patients. Ann Neurol 1989;25:325–30.
Kleiser B, Widder B. Course of carotid occlusions with impaired cerebrovascular reactivity. Stroke 1992;23:171–4.
Ogasawara K, Ogawa A, Terasaki K, et al. Use of cerebrovascular reactivity in patients with symptomatic major cerebral artery occlusion to predict 5-year outcome: comparison of xenon-133 and iodine-123-IMP single-photon emission computed tomography. J Cereb Blood Flow Metab 2002;22:1142–8.
Kuroda S, Houkin K, Kamiyama H, et al. Long-term prognosis of medically treated patients with internal carotid or middle cerebral artery occlusion: can acetazolamide test predict it? Stroke 2001;32:2110–16.
Yonas H, Smith HA, Durham SR, et al. Increased stroke risk predicted by compromised cerebral blood flow reactivity. J Neurosurg 1993;79:483–9.
Derdeyn CP, Videen TO, Simmons NR, et al. Count-based PET method for predicting ischemic stroke in patients with symptomatic carotid arterial occlusion. Radiology 1999;212:499–506.
Yamauchi H, Fukuyama H, Nagahama Y, et al. Significance of increased oxygen extraction fraction in five-year prognosis of major cerebral arterial occlusive diseases. J Nucl Med 1999;40:1992–8.
Markus H, Cullinane M. Severely impaired cerebrovascular reactivity predicts stroke and TIA risk in patients with carotid artery stenosis and occlusion. Brain 2001;124:457–67.
Adams HP, Powers WJ, Grubb RL, et al. Preview of a new trial of extracranial to intracranial arterial anastomosis: the Carotid Occlusion Surgery Study. Neurosurg Clin North Am 2001;12:613–24.
Ogawa A . Cerebrovascular imaging and bypass surgery. Presented at the 1st Asian Pacific Stroke Conference against stroke. Hong Kong 2004.
Executive Committee for the Asymptomatic Carotid Atherosclerosis Study. Endarterectomy for asymptomatic carotid artery stenosis. JAMA 1995;273:1421–28.
Schmideck P, Piepgras A, Leinsinger G, et al. Improvement of cerebrovascular reserve capacity by EC-IC bypass surgery in patients with ICA occlusion and hemodynamic cerebral ischemia. 1994;81:236–44.
Gibbs JM, Wise RJS, Thomas DJ, et al. Cerebral hemodynamic changes after extracranial-intracranial bypass surgery. J Neurol Neurosurg Psychiatry 1987;50:140–50.
Powers WJ, Martin WRW, Herscovitch P, et al. Extracranial-intracranial bypass surgery: hemodynamic and metabolic effects. Neurology 1998;34:1168–74.
Samson Y, Baron JC, Bousser MG, et al. Effects of extracranial-intracranial arterial bypass on cerebral blood flow and oxygen metabolism in humans. Stroke 1985;16:609–16.
Yamashita T, Kashiwagi S, Nakano S, et al. The effects of EC-IC bypass surgery on resting cerebral blood flow and cerebrovascular reserve capacity studied with stable Xe-CT and acetazolamide test. Neuroradiology 1991;33:217–22.
Sasoh M, Ogasawara K, Kuroda K, et al. Effects of EC-IC bypass on cognitive impairment in patients with hemodynamic cerebral ischemia. Surg Neurol 2003;59:455–60.(P J Kirkpatrick1 and I Ng)