Predicting Hemodynamic Changes of Cerebral Blood Flow during Temporal Carotid Occlusion: A Review of Current Knowledge with Implication for Carotid Artery Stenting

Abstract

Carotid artery disease (CAD) plays an important role in the stroke development and its prevalence increases with aging of the population. Its wide variability of clinical manifestation ranges from incidental asymptomatic finding to devastating or fatal stroke, although cerebral collateral circulation is considered one of the major modifying factors. Over time, carotid artery stenting (CAS) has evolved into a reputable method for the treatment of patients with severe CAD. With expanding use of proximal protection systems resembling surgical clamp, there is an increasing demand to understand collateral cerebral circulation to protect patients from periprocedural hypoperfusion, which increases the risk of cerebral events. Transcranial Doppler ultrasound (TCD) is a useful tool allowing monitoring in real time during procedure patient́s cerebral hemodynamic status providing the operator with valuable information. Its role in predicting periprocedural hypoperfusion is, however, less well established. In this article, we discuss the role of cerebral collateral circulation, summarize the current knowledge regarding its evaluation with TCD and suggest future implications for CAS.

Keywords

cerebrovascular reserve - carotid occlusion - carotid stenting - carotid endarterectomy - transcranial Doppler - cerebral collateral circulation

• References

• 1 Donnan GA, Fisher M, Macleod M, Davis SM. Stroke. Lancet 2008; 371 (9624) 1612-1623
• 2 Sacco RL, Kargman DE, Gu Q, Zamanillo MC. Race-ethnicity and determinants of intracranial atherosclerotic cerebral infarction. The Northern Manhattan Stroke Study. Stroke 1995; 26 (1) 14-20
• 3 Spacek M, Veselka J. Carotid artery stenting - current status of the procedure. Arch Med Sci 2013; 9 (6) 1028-1034
• 4 Montorsi P, Caputi L, Galli S , et al. Microembolization during carotid artery stenting in patients with high-risk, lipid-rich plaque. A randomized trial of proximal versus distal cerebral protection. J Am Coll Cardiol 2011; 58 (16) 1656-1663
• 5 Bijuklic K, Wandler A, Hazizi F, Schofer J. The PROFI study (Prevention of Cerebral Embolization by Proximal Balloon Occlusion Compared to Filter Protection During Carotid Artery Stenting): a prospective randomized trial. J Am Coll Cardiol 2012; 59 (15) 1383-1389
• 6 Castro-Afonso LH, Abud LG, Rolo JG , et al. Flow reversal versus filter protection: a pilot carotid artery stenting randomized trial. Circ Cardiovasc Interv 2013; 6 (5) 552-559
• 7 Hetzel A, von Reutern G, Wernz MG, Droste DW, Schumacher M. The carotid compression test for therapeutic occlusion of the internal carotid artery. Comparison of angiography with transcranial Doppler sonography. Cerebrovasc Dis 2000; 10 (3) 194-199
• 8 Spacek M, Tesar D, Veselka J. The Paramount Role of the Anterior Communicating Artery in the Collateral Cerebral Circulation. Int J Angiol 2014; (e-pub ahead of print). doi: 10.1055/s-0034-1370889
• 9 Miralles M, Dolz JL, Cotillas J , et al. The role of the circle of Willis in carotid occlusion: assessment with phase contrast MR angiography and transcranial duplex. Eur J Vasc Endovasc Surg 1995; 10 (4) 424-430
• 10 Liebeskind DS. Collateral circulation. Stroke 2003; 34 (9) 2279-2284
• 11 Romero JR, Pikula A, Nguyen TN, Nien YL, Norbash A, Babikian VL. Cerebral collateral circulation in carotid artery disease. Curr Cardiol Rev 2009; 5 (4) 279-288
• 12 Hofmeijer J, Klijn CJ, Kappelle LJ, Van Huffelen AC, Van Gijn J. Collateral circulation via the ophthalmic artery or leptomeningeal vessels is associated with impaired cerebral vasoreactivity in patients with symptomatic carotid artery occlusion. Cerebrovasc Dis 2002; 14 (1) 22-26
• 13 Okudaira Y, Arai H, Sato K. Cerebral blood flow alteration by acetazolamide during carotid balloon occlusion: parameters reflecting cerebral perfusion pressure in the acetazolamide test. Stroke 1996; 27 (4) 617-621
• 14 Brozici M, van der Zwan A, Hillen B. Anatomy and functionality of leptomeningeal anastomoses: a review. Stroke 2003; 34 (11) 2750-2762
• 15 Hoksbergen AW, Fülesdi B, Legemate DA, Csiba L. Collateral configuration of the circle of Willis: transcranial color-coded duplex ultrasonography and comparison with postmortem anatomy. Stroke 2000; 31 (6) 1346-1351
• 16 Iqbal S. A comprehensive study of the anatomical variations of the circle of willis in adult human brains. J Clin Diagn Res 2013; 7 (11) 2423-2427
• 17 Alpers BJ, Berry RG, Paddison RM. Anatomical studies of the circle of Willis in normal brain. AMA Arch Neurol Psychiatry 1959; 81 (4) 409-418
• 18 Henderson RD, Eliasziw M, Fox AJ, Rothwell PM, Barnett HJM ; North American Symptomatic Carotid Endarterectomy Trial (NASCET) Group. Angiographically defined collateral circulation and risk of stroke in patients with severe carotid artery stenosis. Stroke 2000; 31 (1) 128-132
• 19 Telman G, Kouperberg E, Sprecher E, Gruberg L, Beyar R, Yarnitsky D. TCD evaluation before and after stenting in patients with severe primary carotid artery stenosis versus restenosis. J Endovasc Ther 2007; 14 (4) 483-488
• 20 Sánchez-Arjona MB, Sanz-Fernández G, Franco-Macías E, Gil-Peralta A. Cerebral hemodynamic changes after carotid angioplasty and stenting. AJNR Am J Neuroradiol 2007; 28 (4) 640-644
• 21 Silvestrini M, Troisi E, Matteis M, Cupini LM, Caltagirone C. Transcranial Doppler assessment of cerebrovascular reactivity in symptomatic and asymptomatic severe carotid stenosis. Stroke 1996; 27 (11) 1970-1973
• 22 Sorteberg A, Bakke SJ, Boysen M, Sorteberg W. Angiographic balloon test occlusion and therapeutic sacrifice of major arteries to the brain. Neurosurgery 2008; 63 (4) 651-660 , 660–661
• 23 Mathis JM, Barr JD, Jungreis CA , et al. Temporary balloon test occlusion of the internal carotid artery: experience in 500 cases. AJNR Am J Neuroradiol 1995; 16 (4) 749-754
• 24 Eckert B, Thie A, Carvajal M, Groden C, Zeumer H. Predicting hemodynamic ischemia by transcranial Doppler monitoring during therapeutic balloon occlusion of the internal carotid artery. AJNR Am J Neuroradiol 1998; 19 (3) 577-582
• 25 Brott TG, Halperin JL, Abbara S , et al. 2011 ASA/ACCF/AHA/AANN/AANS/ACR/ASNR/CNS/SAIP/SCAI/SIR/SNIS/SVM/SVS guideline on the management of patients with extracranial carotid and vertebral artery disease: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines, and the American Stroke Association, American Association of Neuroscience Nurses, American Association of Neurological Surgeons, American College of Radiology, American Society of Neuroradiology, Congress of Neurological Surgeons, Society of Atherosclerosis Imaging and Prevention, Society for Cardiovascular Angiography and Interventions, Society of Interventional Radiology, Society of NeuroInterventional Surgery, Society for Vascular Medicine, and Society for Vascular Surgery. J Am Coll Cardiol 2011; 57 (8) e16-e94
• 26 Garami Z, Lumsden AB. Intra-operative TCD monitoring. In: Alexandrov AV, , ed. Cerebrovascular Ultrasound in Stroke Prevention and Treatment. 2nd ed. Oxford, United Kingdom: Wiley-Blackwell Publishing; 2011: 214-227
• 27 Telman G, Kouperberg E, Nitecki S , et al. Preoperative cerebral hemodynamics and shunting during carotid endarterectomy in patients with severe unilateral carotid stenosis. J Clin Ultrasound 2007; 35 (9) 498-503
• 28 Visser GH, Wieneke GH, van Huffelen AC, Eikelboom BC. The use of preoperative transcranial Doppler variables to predict which patients do not need a shunt during carotid endarterectomy. Eur J Vasc Endovasc Surg 2000; 19 (3) 226-232
• 29 Anzola GP, Limoni P, Cavrini G. Predictors of carotid clamping intolerance during endarterectomy that would be wise to apply to stenting procedures. Cerebrovasc Dis 2008; 26 (5) 494-501
• 30 Thiel A, Zickmann B, Stertmann WA, Wyderka T, Hempelmann G. Cerebrovascular carbon dioxide reactivity in carotid artery disease. Relation to intraoperative cerebral monitoring results in 100 carotid endarterectomies. Anesthesiology 1995; 82 (3) 655-661
• 31 Lucertini G, Cariati P, Ermirio D , et al. Can cerebral vasoreactivity predict cerebral tolerance to carotid clamping during carotid endarterectomy?. Cardiovasc Surg 2002; 10 (2) 123-127
• 32 Belardi P, Lucertini G. Cerebral vasoreactivity does not predict cerebral ischaemia during carotid endarterectomy. J Cardiovasc Surg (Torino) 2003; 44 (6) 731-735
• 33 Lam JM, Smielewski P, al-Rawi P , et al. Prediction of cerebral ischaemia during carotid endarterectomy with preoperative CO2-reactivity studies and angiography. Br J Neurosurg 2000; 14 (5) 441-448
• 34 Fearn SJ, Picton AJ, Mortimer AJ, Parry AD, McCollum CN. The contribution of the external carotid artery to cerebral perfusion in carotid disease. J Vasc Surg 2000; 31 (5) 989-993
• 35 Stabile E, Salemme L, Sorropago G , et al. Proximal endovascular occlusion for carotid artery stenting: results from a prospective registry of 1,300 patients. J Am Coll Cardiol 2010; 55 (16) 1661-1667
• 36 Caplan LR, Hennerici M. Impaired clearance of emboli (washout) is an important link between hypoperfusion, embolism, and ischemic stroke. Arch Neurol 1998; 55 (11) 1475-1482
• 37 Orlandi G, Fanucchi S, Gallerini S , et al. Impaired clearance of microemboli and cerebrovascular symptoms during carotid stenting procedures. Arch Neurol 2005; 62 (8) 1208-1211
• 38 Spacek M, Veselka J. Microembolization following balloon deflation during proximally protected carotid artery stenting-a potential focus of procedure improvement?. Catheter Cardiovasc Interv 2014; 83 (7) 1185-1186
• 39 Wain RA, Veith FJ, Berkowitz BA , et al. Angiographic criteria reliably predict when carotid endarterectomy can be safely performed without a shunt. J Am Coll Surg 1999; 189 (1) 93-100 , discussion 100–101
• 40 Schomer DF, Marks MP, Steinberg GK , et al. The anatomy of the posterior communicating artery as a risk factor for ischemic cerebral infarction. N Engl J Med 1994; 330 (22) 1565-1570
• 41 Spacek M, Sorrell VL, Veselka J. Transcranial doppler ultrasound in the current era of carotid artery stenting. Ultraschall Med 2014; ; (e-pub ahead of print)