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 Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 8  |  Issue : 2  |  Page : 78-86

Effectiveness of cerebral bypass revascularisation procedures in adult cerebrovascular ischaemic stroke: Looking beyond COSS – A single surgeon's experience of 7 years


1 Department of Neurosurgery, Apollo Proton Cancer Centre, Chennai, Tamil Nadu, India
2 Department of Neurosurgery and Neurology, Institute of Neurosciences, SIMS Hospitals, Chennai, Tamil Nadu, India
3 Department of Neurology, Apollo Speciality Hospital, Perungudi, Chennai, Tamil Nadu, India
4 Department of Nuclear Medicine, Anderson Diagnostics Pvt Limited, Chennai, Tamil Nadu, India

Date of Submission09-Dec-2020
Date of Decision15-Dec-2020
Date of Acceptance17-Dec-2020
Date of Web Publication3-Feb-2021

Correspondence Address:
Dr. V R Roopesh Kumar
Department of Neurosurgery, Apollo Proton Cancer Centre, Chennai, Tamil Nadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcvs.jcvs_30_20

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  Abstract 


Context: Adults with haemodynamic stroke secondary to cerebrovascular ischaemic events, continue to develop stroke despite optimum medical management.
Aims: This study aims to identify patients with adult ischaemic stroke presenting with significant haemodynamic failure based on radiological and molecular imaging and perform Revascularisation procedure to prevent further stroke.
Settings and Design: This is a retrospective database analysis of patients with CVOD requiring cerebral revasularisation procedure from 2013 to 2019.
Materials and Methods: Twenty-two adult patients with age ranging from 26 to 72 years presenting with recurrent transient ischaemic attacks (TIAs) were evaluated for haemodynamic insufficiency by neuroimaging and acetazolamide challenged single-photon emission computed tomography perfusion. Those with decompensated haemodynamic insufficiency underwent cerebral revascularisation with superficial temporal artery (STA) to middle cerebral artery (MCA) bypass.
Results: Of the 22 patients, in 12 patients, the procedure was done electively and in remaining 10 patients as emergency (<48 h of the onset of symptoms). Ninety-one per cent of the patients recovered well without any further TIAs. Neurological worsening was observed in 4.5%. Two patients who presented with refractory migraine like symptoms improved dramatically without further headaches. Uneventful wound complications were associated in 9% of cases. Follow-up radiological evaluation showed good graft patency in 95% (21/22) patients. The single case of graft thrombosis developed new MCA territory infarct requiring prolonged rehabilitation for the neurological deterioration.
Conclusion: Cerebral revascularisation with STA-MCA bypass in selected patients with impending haemodynamic insufficiency results in good outcome and prevents further strokes despite continuing optimum medical therapy.

Keywords: Adult ischaemic stroke, recurrent stroke, revascularisation procedures, single-photon emission computed tomogram ACZ challenge, superficial temporal artery-middle cerebral artery bypass


How to cite this article:
Kumar V R, Ratha V, Nair R, Karthikeyan S, Rajendran A, Soundararajan R. Effectiveness of cerebral bypass revascularisation procedures in adult cerebrovascular ischaemic stroke: Looking beyond COSS – A single surgeon's experience of 7 years. J Cerebrovasc Sci 2020;8:78-86

How to cite this URL:
Kumar V R, Ratha V, Nair R, Karthikeyan S, Rajendran A, Soundararajan R. Effectiveness of cerebral bypass revascularisation procedures in adult cerebrovascular ischaemic stroke: Looking beyond COSS – A single surgeon's experience of 7 years. J Cerebrovasc Sci [serial online] 2020 [cited 2021 Jun 16];8:78-86. Available from: http://www.jcvs.com/text.asp?2020/8/2/78/308635




  Introduction Top


The Global Burden of Diseases study has established stroke as the second leading cause of death worldwide.[1] Recent literature points towards a 26% increase in global stroke deaths during the past two decades alone.[2],[3] Despite the numerous measures taken world-wide, stroke remains a major global public health problem especially in lower income countries.[4] A substantial number of stroke cases are attributable to extra cranial (EC) and intracranial (IC) steno-occlusive disease which unfortunately cannot be managed by medical therapy alone. However, two major international trials failed (EC-IC bypass study and COSS study) failed to demonstrate the benefit of surgical revascularisation. However, some significant flaws in the studies, makes it imperative for us to look beyond them and explore the role of revascularisation procedures in adult ischaemic events.

Through this article, we wish to share our 7 years' experience with the revascularisation bypass procedure, its indications, technical considerations, complications and clinical outcomes for both prophylactic and therapeutic EC-IC bypass in adult ischaemic strokes secondary to steno-occlusive disease.


  Materials and Methods Top


This is a retrospective database analysis of 22 symptomatic patients with atherosclerotic occlusive disease requiring cerebral revasularisation procedure from January 2013 to January 2019 with a minimum of 1 year follow-up.

Selection criteria

The decision to do revascularisation was made by the stroke team consisting of neuro-physician, neurosurgeon, neuro-radiologist and neuro anaesthetist. The following criteria were used for selecting the revascularisation procedure:

  1. Patients with complete internal carotid artery (ICA) or middle cerebral artery (MCA) occlusion with Type III response on single-photon emission computed tomogram (SPECT) computed tomography (CT) or magnetic resonance (MR) perfusion with acetazolamide (ACZ) challenge
  2. Patients with fluctuating neurological signs on the best medical management in an acute stage who were not fit to undergo ACZ challenge
  3. CT perfusion images showing large areas of ischaemic penumbra and relatively small area of established infarct.


The need for revascularisation in view of the ongoing stroke and the risk of further stroke with best medical management were discussed with the patient and the family. After obtaining informed consent, patients were taken up for cerebral revascularisation with superficial temporal artery (STA) to MCA anastomosis.

Patient demographics

The age ranged from 26 to 72 years with 2:1 male:female ratio. Ninety per cent of the patients had extra cranial (EC) carotid disease and remaining had intra cranial (IC) disease (MCA occlusion). Ten patients had the procedure done as emergency (<48 h of onset of symptoms) and remaining 12 patients had an elective procedure. The demographic, operative, radiological and outcome details are summarised in [Table 1].
Table 1: Demographic, radiological and surgical details

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Investigations

Patients presenting with transient ischaemic attacks (TIAs) or minor strokes were initially evaluated with MR imaging (MRI) brain along with MR angiogram of neck and brain. Subsequently, those with steno-occlusive disease, underwent a 4-vessel cerebral digital subtraction angiography (DSA). Patients with complete occlusion of either Internal carotid or MCA and clinically stable were further investigated to assess the cerebrovascular reserve (CVR) with SPECT with ACZ challenge.[5] Accordingly, after doing a basal SPECT cerebral perfusion study, 500 mg of ACZ was administered orally every 15 min for 3 doses (total of 1500 mg). Fifteen minutes after the last dose,99mTc ethyl cysteinate dimer was injected intravenously and imaging was repeated after 45 min. The pre- and post-ACZ perfusion was compared and was grouped into three groups [Table 2]. Those who demonstrated paradoxical decrease of cerebral perfusion in the ischaemic territory (Type III response) after ACZ challenge were selected and counselled for cerebral revascularisation procedure. In the last 4 patients, the ACZ challenge was done with MR perfusion studies instead of SPECT due to difficulty in shifting the patients to another diagnostic centre.
Table 2: Grouping of patients after single-photon emission tomogram acetazolamide challenge image to assess the cerebrovascular reserve

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Those patients with fluctuating neurological symptoms and unable to undergo the ACZ challenge were investigated with CT perfusion studies.

Surgery

Patients were placed in supine position with 45° head tilt. The STA branches were marked pre-operatively using colour Doppler and skin marking was made. The STA was dissected beneath the skin flap for about 10–12 cm from the tragus under operating microscope and all the branches were divided using ligatures. The STA branch with larger diameter was chosen for the anastomosis and the other branch was divided. A craniotomy measuring 5–6 cm diameter was done using high speed drill centring over the sylvian point [Figure 1]. After durotomy, the M4 branch which is relatively larger and located in the centre of the flap is selected as recipient. The arachnoid over the vessel was then opened and 1 cm of the recipient vessel was prepared by micro coagulating the perforators. A rubber dam would be placed beneath the recipient branch and the segment to be anastomosed was trapped by mini temporary aneurysm clips. The donor vessel was then prepared by creating a fish mouth to increase the luminal diameter across the stoma. Anastomosis was done using 10-0 interrupted ethilon sutures in usual sequence, initially heel and toe stitch, back wall and finally the front wall. The average duration of anastomosis ranged between 30 and 40 min and adequate cerebral perfusion was maintained during the cross clamping by induced hypertension. Intra operative neuro monitoring was done for the last 4 patients using somatosensory evoked potential and electroencephalogram to ensure stable cerebral physiology perioperatively. On completion of the anastomosis, the flow and patency of the anastomosis was confirmed with indocyanine green (ICG) angiography. All patients received 75 mg of acetyl salicylic acid in the peri-operative period and was continued indefinitely in the post-operative period as well.
Figure 1: Post-operative computed tomography angiography showing the craniotomy and anastomosis

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  Results Top


Twenty patients had complete occlusion of ICA at the origin soon after the bifurcation. The remaining two patients had MCA occlusion in M1 segment. Symptomatically, these patients had recurrent TIAs and were on best medical management consisting of dual antiplatelets and statins. Three patients had hyper homocysteinaemia. One patient presented with unilateral visual symptoms and two patients presented with refractory migraine like symptoms. All patients had varying degrees of water shed infarcts on MRI especially in flair sequences. Eight patients showed Type III response on ACZ challenge SPECT studies and the last four patients who underwent MR perfusion with ACZ challenge also had the same response. During the same period, nine patients with preserved perfusion (Type II response) and another three patients with Type III response (who denied surgery and lost for further follow up) were not included in this study. In ten patients, who had acute symptoms and had fresh infarcts in the water shed zones in diffusion weighted images (DWIs), did not undergo ACZ challenge and they were evaluated with CT perfusion. These patients demonstrated large areas of ischaemic penumbra with small areas of established infarcts. They were monitored in the intensive care unit and best medical therapy along with induced hypertension were administered by stroke physician. They had varying degrees of motor signs and language dysfunction. One patient had dense right hemiplegia, aphasia and had both ICA and left vertebral artery occluded with right vertebral artery alone supporting the entire IC circulation.

Following the surgery, patients were monitored in the intensive care unit and were shifted to room once they were neurologically stable. CT angiography (CTA) was performed on the 1st post-operative day to assess the graft patency. In 4 patients, there was significant spasm of the donor vessel and they were administered oral nimodipine 60 mg 6th hourly. Aspirin and statins were continued. Thirteen out of 22 patients were hypertensive and antihypertensive medications were withheld for a month to improve cerebral perfusion. Patients were discharged on the 5th post-operative day unless they were in acute stage who required longer hospitalisation.

Out of 22, ten patients who underwent emergency STA-MCA bypass were symptomatically better and did not have fresh neurological signs following surgery. The patient who had dense right hemiplegia and aphasia showed gradual recovery and by 3 months she was ambulant with minimal support and was able to verbalise to her needs. In the remaining 12 patients, who had the procedure done as elective, 11/12 patients did not experience any fresh neurological signs. One patient had new infarct in the distal MCA territory and the CTA showed thrombosis of the graft. He was managed conservatively and had prolonged hospital stay. After 6 weeks, he was ambulant with support but could not recover to pre-operative stage. Two patients who had migraine like symptoms became asymptomatic after the surgery. None of the patients experienced TIAs on further follow-up. A repeat CT perfusion after 1 month demonstrated improved cerebral perfusion in all the patients. The STA diameter progressively enlarged on the follow-up imaging. At 3 months' post-surgery, a repeat SPECT CT perfusion with ACZ challenge was performed in 16 patients which demonstrated Type I response. Four patients who underwent MR perfusion instead of SPECT preoperatively were evaluated with same modality and had improved perfusion. Two patients had wound related morbidity with cerebrospinal fluid leak and were managed appropriately. This however did not affect the graft patency. The following are some illustrative cases where cerebral revascularisation has proven benefit over and above the best medical therapies alone.

Case 1

A 45-year-old male patient developed acute onset left hemiparesis, which improved partially over the next few days. CTA showed near-total occlusion of supraclinoid ICA on the right side. CT perfusion showed significantly reduced cerebral blood flow (CBF) with large areas of penumbra suggesting stage III haemodynamic failure. He underwent right STA–MCA anastomosis following which he had no further symptoms. At 2-year follow-up, he remains asymptomatic and imaging showed improved cerebral perfusion in right hemisphere [Figure 2]a, [Figure 2]b, [Figure 2]c, [Figure 2]d, [Figure 2]e, [Figure 2]f.
Figure 2: (a) Computed tomography angiography of the brain showing significant stenosis of right clinoidal internal carotid artery. (b) Computed tomography angiography of supratentorial circulation showing normal vessel candelabra. (c) Computed tomography perfusion of the brain showing significant ischaemic penumbra in the right hemisphere. (d and e) Post-operative computed tomography angiography of the brain showing good patency of superficial temporal artery-middle cerebral artery bypass. (f) Post-operative computed tomography perfusion showing improved cerebral perfusion in the right hemisphere

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Case 2

A 26-year-old man had recurrent episodes of slurring of speech and right hemiparesis of 5-day duration. MRI showed multiple watershed infarcts in the left hemisphere and CTA showed left supraclinoid ICA total occlusion. DSA revealed left supraclinoid ICA occlusion just beyond the ophthalmic artery with partial reformation of left M1 through anterior cerebral artery collaterals. Despite medical management and intensive care monitoring, he continued to have recurrent episodes of TIAs in the intensive care unit. He underwent emergency left STA–MCA anastomosis. Follow-up CTA showed improved collateral circulation on left MCA territory. Three-month follow-up CT perfusion showed good improvement in CBF. His symptoms were also resolved [Figure 3]a, [Figure 3]b, [Figure 3]c, [Figure 3]d, [Figure 3]e, [Figure 3]f, [Figure 3]g.
Figure 3: (a) Diffusion-weighted magnetic resonance imaging of the brain showing multiple infarcts in left hemisphere in deep basal ganglia and centrum semi ovale. (b) Computed tomography angiography showing occlusion of left internal carotid artery and proximal middle cerebral artery. (c) digital subtraction angiography showing no filling beyond left supraclinoidal ICA. (d and e) Inadequate cross-circulation and collaterals from contralateral and posterior circulation. (f and g) Post-operative computed tomography angiography showing good patency of left superficial temporal artery-middle cerebral artery bypass and improved collateral circulation

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Case 3

A 65-year-old woman had right hand weakness and speech slurring for 10 days with acute progression to hemiplegia and aphasia in the same day. MRI brain showed left hemispheric watershed infarct and MRA showed bilateral ICA occlusion. DSA revealed bilateral ICA occlusion at origin, 80% stenosis of left vertebral artery, and right vertebral artery supplying the whole of supratentorial compartment. Emergency left STA–MCA anastomosis was performed. She gradually improved, and at 3-month follow-up, CT perfusion showed improved CBF in the supratentorial compartment. Her hemiparesis and aphasia also improved making her independent and communicate verbally [Figure 4]a, [Figure 4]b, [Figure 4]c, [Figure 4]d, [Figure 4]e, [Figure 4]f, [Figure 4]g.
Figure 4: (a) Diffusion-weighted magnetic resonance imaging of the brain showing large infarct in left deep centrum semi ovale, (b) digital subtraction angiography showing occlusion of the right internal carotid artery immediately distal to bifurcation, (c) digital subtraction angiography showing occlusion of left ICA immediately distal to bifurcation. (d) digital subtraction angiography showing filling of entire supratentorial circulation through right vertebral artery. (e-g) Post-operative computed tomography angiography showing good patency of left superficial temporal artery-middle cerebral artery bypass and improved collateralisation in left the hemisphere

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  Discussion Top


In India, the pooled data incorporating all the studies reveal that ischaemic stroke occurs in 68%–80%, of which, EC carotid disease accounts for 25%–26% and IC carotid disease for 30% of ischaemic stroke cases.[5] To further compound the issue, the 2-year risk of subsequent ipsilateral ischaemic stroke in the context of best medical therapy has been estimated at 10%–15% for EC carotid disease and 15%–20% for IC atherosclerotic disease.[6],[7] Our initial experience in 2013 gave us the impetus to look beyond the results of COSS study.[8] These data of high recurrence rate despite medical treatment and are reshaping our understanding of the management of ischaemic stroke.

Pathophysiology

In steno-occlusive disease, the brain vasculature compensates by post-stenotic vasodilatation which may be global or regional. [Table 3] describes the stages of haemodynamic insufficiency. This helps the parenchyma in maintaining its cerebral metabolic rate of oxygen (CMRO2) [Stage 1 of haemodynamic insufficiency]. Additional compensation happens by increasing the oxygen extraction fraction (OEF) [Stage 2 of haemodynamic insufficiency]. When the compensatory mechanisms of vasodilatation and OEF are exceeded by reduced cerebral perfusion, CMRO2 declines and subsequent infarction occur [Stage 3 of hemodynamic insufficiency]. With large vessel occlusion, this is the most common in the deep white matter and grey matter of the border zones (watershed areas) of vascular territories.[9],[10] The occurrence of this ischaemia depends on the cerebral collateral circulation which vary from individual to individual and so the risk of stroke.
Table 3: Stages of hemodynamic insufficiency

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Radiological evaluation

Routine radiological evaluation such as CT, MRI and DSA can directly measure the length of the occluded artery, the degree of reverse filling by the distal blood flow of the occluded artery but fails to identify the patients at risk of stroke. Soft radiological signs like internal border zone infarctions, rosary like pattern on DWIs can suggest chronic large vessel occlusion. CT or MR perfusion studies can help in guiding therapy especially in emergency situations where SPECT cannot be done. Increased cerebral blood volume denotes stressed autoregulation and denotes haemodynamic insufficiency still compensated by autoregulation. A reduction in CBF implicates further reduction in perfusion suggesting decompensation. Reduced CBF and prolongation of mean transit time suggests haemodynamic insufficiency warranting cerebral revascularisation.

Molecular imaging

In patients, who are stable, molecular imaging with vasodilator challenge can guide further in deciding the need for revascularisation. SPECT imaging is one of the most common methods for assessing CVR. ACZ, a reversible carbonic anhydrase inhibitor causes increase in carbonic acid and acidosis, leading to reduced vascular resistance and vasodilation in compliant microvasculature. A 30%–60% increase in CBF is achieved in healthy controls 1 h after oral administration of ACZ. In steno-occlusive disease, the microvasculature distal to stenosis are in maximally dilated state and administration of ACZ causes shunting of blood to normally perfused areas causing paradoxical reduction in perfusion across ischaemic territory (steal phenomena denoting Type 3 response and significant haemodynamic insufficiency). This subset of patients with Type 3 response is most likely to fail medical therapy and will benefit from flow augmentation to prevent a major stroke. Non-invasive arterial spin labelling MRI perfusion imaging can identify the impaired CVR similar to the SPECT and also monitor the post-operative changes of CVR, without any radiation or contrast agents.[11]

Major clinical trials and lessons learnt

After the results of International EC-IC Bypass trial in 1985 and the recent COSS study (2011),[12] an entire generation of Neurosurgeons have evolved under the shadows of their results and are unaware of effective utilisation of cerebrovascular flow augmentation procedures like By-pass in the treatment of adult ischaemic disease. There are flaws in the studies and nonetheless, although the best medical therapy is more effective than in the past, it is still not curative and many patients with severe haemodynamic insufficiency fare poorly.[13] The COSS eligible patient might still benefit from flow-augmentation bypass if peri-operative morbidity can be sufficiently lowered, much lower than reported in COSS and EC-IC bypass trial.[14] Technical innovations, well performed microvascular anastomosis along with the use of ICG-angiography can lower the peri-operative complications rates.[15]

Indications for surgical treatment

In the present study, we aim to identify a subgroup of patients who have exhausted brain vascular reserve capacity to the maximum and with any further oligemia exacerbated by haemodynamic challenge, they become symptomatic. These patients were not included in any trials and represent possible bypass candidates.

  1. Patients presenting with ongoing haemodynamic symptoms despite optimal medical therapy
  2. Patients who develop ischaemic symptoms with postural changes or blood pressure variation (for instance patients with debilitating orthostatic hypoperfusion syndrome or limb shaking TIAs)
  3. Patients with symptomatic carotid occlusion and particularly marked haemodynamic impairment as documented by ACZ challenged SPECT CT who may have a significant risk for subsequent stroke.
  4. Patients harbouring multiple EC arterial occlusions, not amenable to carotid endarterectomy or stenting, who are symptomatic despite best medical therapy.
  5. Patients with chronic retinal ischaemia resulting in progressive visual loss
  6. Patients with neurovascular headache refractory to medications


Amongst individuals suffering acute or evolving stroke, patients who could benefit from bypass surgery might be the ones presenting with the following criteria:

  1. Acute stroke or stroke in progress (fluctuating or worsening symptoms) despite maximal applicable medical and interventional treatment
  2. Major cerebral artery occlusion, with documented region of penumbra and with a small area of infarction (to avoid haemorrhagic conversion of an acute infarction) as noticed by CT/MR perfusion.[16],[17],[18]


The eventual benefit of bypass surgery over medical therapy in these individuals will most likely not be testable in RCTs. [Figure 5] demonstrates the algorithmic approach for management of cerebrovascular ischaemic events in adults.
Figure 5: Algorithmic approach for the management of cerebrovascular ischaemic events in adults

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Thus, cerebrovascular flow augmentation bypass procedure is highly effective in Stage III haemodynamic failure and symptomatic patients with Stage I or II haemodynamic failure. However, in asymptomatic patients with complete occlusion of ICA and Stage I hemodynamic failure, the role of revascularisation is questionable.[13],[14],[19]


  Conclusion Top


Despite many trials showing the superiority of medical therapy, it is still not curative and many patients with hemodynamic failure fare poorly. Recent critical appraisal of COSS results demonstrated that the overall result would change if perioperative complications could be lowered.[20] Patients with severe steno-occlusive disease continue to have significant event rates, despite medical therapy. It is imperative to understand the stages of haemodynamic impairment in adult ischaemic events as cerebrovascular flow augmentation through EC-IC By-pass procedure results in significant improvement in hemodynamic parameters and lowers the stroke recurrence in selected symptomatic Stage II and III haemodynamic failure.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Murray CJ. Lopez AD, World Health Organization, World Bank & Harvard School of Public Health. Global health statistics: A compendium of incidence, prevalence and mortality estimates for over 200 conditions / Christopher J. L. Murray, Alan D. Lopez. Harvard School of Public Health. 1996. Available from: https://apps.who.int/iris/handle/10665/4. [Last accessed on 2020 Oct 05]  Back to cited text no. 1
    
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Strong K, Mathers C. The global burden of stroke. In: Mohr JP, Grotta JC, Wolf PA, Moskowitz MA, Mayberg MR, Von Kummer R, editors. Stroke: Pathophysiology, Diagnosis and Management. 5th ed. Philadelphia, PA: Elsevier; 2011. pp. 279–89.  Back to cited text no. 2
    
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Strong K, Mathers C, Bonita R. Preventing stroke: Saving lives around the world. Lancet Neurol 2007;6:182-7.  Back to cited text no. 3
    
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Feigin VL, Lawes CM, Bennett DA, Barker-Collo SL, Parag V. Worldwide stroke incidence and early case fatality reported in 56 population-based studies: A systematic review. Lancet Neurol 2009;8:355-69.  Back to cited text no. 4
    
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Vagal AS, Leach JL, Fernandez-Ulloa M, Zuccarello M. The acetazolamide challenge: Techniques and applications in the evaluation of chronic cerebral ischemia. AJNR Am J Neuroradiol 2009;30:876-84.  Back to cited text no. 5
    
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Wasay M, Khatri IA, Kaul S. Stroke in South Asian countries. Nat Rev Neurol 2014;10:135-43.  Back to cited text no. 6
    
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Giles MF, Rothwell PM. Risk of stroke early after transient ischaemic attack: A systematic review and meta-analysis. Lancet Neurol 2007;6:1063-72.  Back to cited text no. 7
    
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Flaherty ML, Flemming KD, McClelland R, Jorgensen NW, Brown RD Jr. Population-based study of symptomatic internal carotid artery occlusion: Incidence and long-term follow-up. Stroke 2004;35:e349-52.  Back to cited text no. 8
    
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Roopesh Kumar VR, Narayan SK, Madhugiri VS, Sasidharan GM, Gundamaneni SK. Cerebral revascularization with superficial temporal - middle cerebral artery anastomosis for complete carotid occlusion: An emerging modality for preventing recurrent stroke. Ann Indian Acad Neurol 2013;16:521-4.  Back to cited text no. 9
    
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Smith RD. Extracranial-intracranial bypass in cerebral ischemia. Ochsner J 2003;5:31-5.  Back to cited text no. 10
    
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Derdeyn CP, Videen TO, Yundt KD, Fritsch SM, Carpenter DA, Grubb RL, et al. Variability of cerebral blood volume and oxygen extraction: Stages of cerebral haemodynamic impairment revisited. Brain 2002;125:595-607.  Back to cited text no. 11
    
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Yun TJ, Paeng JC, Sohn CH, Kim JE, Kang HS, Yoon BW, et al. Monitoring cerebrovascular reactivity through the use of arterial spin labeling in patients with moyamoya disease. Radiology 2016;278:205-13.  Back to cited text no. 12
    
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Powers WJ, Clarke WR, Grubb RL Jr., Videen TO, Adams HP Jr., Derdeyn CP, et al. Extracranial-intracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: The Carotid Occlusion Surgery Study randomized trial. JAMA 2011;306:1983-92.  Back to cited text no. 13
    
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Amin-Hanjani S, Barker FG 2nd, Charbel FT, Connolly ES Jr., Morcos JJ, Thompson BG, et al. Extracranial-intracranial bypass for stroke-is this the end of the line or a bump in the road? Neurosurgery 2012;71:557-61.  Back to cited text no. 14
    
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Reynolds MR, Derdeyn CP, Grubb RL Jr., Powers WJ, Zipfel GJ. Extracranial-intracranial bypass for ischemic cerebrovascular disease: What have we learned from the Carotid Occlusion Surgery Study? Neurosurgical Focus FOC 2014;36:E9.  Back to cited text no. 15
    
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Kaku Y, Yamashita K, Kokuzawa J, Kanou K, Tsujimoto M. Superficial temporal artery-middle cerebral artery bypass using local anesthesia and a sedative without endotracheal general anesthesia. J Neurosurg 2012;117:288-94.  Back to cited text no. 16
    
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Campbell BC, Mitchell PJ, Kleinig TJ, Dewey HM, Churilov L, Yassi N, et al. Endovascular therapy for ischemic stroke with perfusion-imaging selection. N Engl J Med 2015;372:1009-18.  Back to cited text no. 17
    
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Hwang G, Oh CW, Bang JS, Jung CK, Kwon OK, Kim JE, et al. Superficial temporal artery to middle cerebral artery bypass in acute ischemic stroke and stroke in progress. Neurosurgery 2011;68:723-9.  Back to cited text no. 18
    
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Horiuchi T, Nitta J, Ishizaka S, Kanaya K, Yanagawa T, Hongo K. Emergency EC-IC bypass for symptomatic atherosclerotic ischemic stroke. Neurosurg Rev 2013;36:559-64.  Back to cited text no. 19
    
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Kuroda S, Kawabori M, Hirata K, Shiga T, Kashiwazaki D, Houkin K, et al. Clinical significance of STA-MCA double anastomosis for hemodynamic compromise in post-JET/COSS era. Acta Neurochir (Wien) 2014;156:77-83.  Back to cited text no. 20
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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