ORIGINAL ARTICLE

Emergency EC-IC bypass for symptomatic atheroscleroticischemic stroke

Tetsuyoshi Horiuchi & Junpei Nitta & Shigetoshi Ishizaka &Kohei Kanaya & Takao Yanagawa & Kazuhiro Hongo

Received: 25 May 2012 /Revised: 10 March 2013 /Accepted: 5 May 2013# Springer-Verlag Berlin Heidelberg 2013

Abstract Previous studies have shown that extracranialin-tracranial (EC-IC) bypass surgery has no preventive effect onsubsequent ipsilateral ischemic stroke in patients with symp-tomatic atherosclerotic internal carotid occlusion and hemo-dynamic cerebral ischemia. A few studies have assessedwhether an urgent EC-IC bypass surgery is an effective treat-ment for main trunk stenosis or occlusion in acute stage. Theauthors retrospectively reviewed 58 consecutive patients whounderwent urgent EC-IC bypass for symptomatic internalcarotid artery or the middle cerebral artery stenosis or occlu-sion between January 2003 and December 2011. Clinicalcharacteristics and neuroimagings were evaluated and ana-lyzed. Based on preoperative angiogram, responsible lesionswere the internal carotid artery in 19 (32.8 %) patients and themiddle cerebral artery in 39 (67.2 %). No hemorrhagic com-plication occurred. Sixty-nine percent of patients showedimprovement of neurological function after surgery, and74.1 % of patients had favorable outcome. Unfavorable out-come was associated with insufficient collateral flow and newinfarction after bypass surgery.

Keywords Anastomosis . Athero-occlusive disease .

Extracranialintracranial bypass . Revascularization

Introduction

Recent randomized clinical trial in patients with atheroscle-rotic internal carotid artery (ICA) occlusion to medical orextracranialintracranial (EC-IC) bypass surgery in chronicstage found that superficial temporal artery (STA)middle

cerebral artery (MCA) bypass provided no benefit over med-ical therapy [8]. By contrast, surgical revascularization maybe effective to some patients who suffered from medication-resistance hemodynamic stroke in acute stage [37, 10].However, safety and efficacy of surgical revascularizationfor ischemic stroke in acute stage is still controversial. Wehave reported the efficacy of urgent embolectomy for theICA or MCA occlusion caused by embolism [4, 6]. In thepresent study, we analyzed our experience with early EC-ICbypass in acute ischemic stroke and stroke in progress due toarteriosclerosis.

Patients and methods

Patient population

From January 2003 toDecember 2011, 101 patients with steno-occlusive disease at the anterior circulation underwent EC-ICbypass. Of the 101 patients who underwent 104 procedures,there were 59 patients treated with urgent EC-IC bypass to treatacute ischemic stroke. Crescendo transient ischemic attackresistance to medical treatment and progressive ischemic strokedue to the steno-occlusive disease of ICA or MCA were alsotreated with direct bypass. The EC-IC bypass for moyamoya oratherosclerotic patients in the chronic phase was excluded. Weretrospectively analyzed hospital records, neuroimaging stud-ies, and operative reports. The study protocol was approved bythe institutional ethics committee.

Management of patients

On admission, the patient presenting with speech distur-bance, motor weakness, and/or cognitive dysfunction initial-ly underwent computed tomography (CT). Based on neuro-logical findings and CT, main trunk stenosis or occlusionwas suspected. Main artery stenosis or occlusion at the ICA

T. Horiuchi (*) : J. Nitta : S. Ishizaka :K. Kanaya :T. Yanagawa :K. HongoDepartment of Neurosurgery, Shinshu University School ofMedicine, 3-1-1 Asahi, Matsumoto 390-8621, Japane-mail: tetuyosi@shinshu-u.ac.jp

Neurosurg RevDOI 10.1007/s10143-013-0487-5

or MCA was generally detected using magnetic resonanceimaging (MRI) and confirmed with cerebral angiography.Embolus or atherosclerosis was diagnosed based on the pasthistory such as atrial fibrillation and neuroimages. The em-bolic stroke in patients with insufficient endovascular recana-lization was treated by the open embolectomy [3, 4, 6, 8]. TheEC-IC bypass was performed for steno-occlusive atheroscle-rosis. When it was difficult to distinguish the atherosclerosisfrom the embolus preoperatively, the affected artery was di-rectly visualized and the appropriate surgery was carried out.Surgical indications of urgent revascularization were previ-ously reported in detail [4, 6]. Briefly, inclusion criteria werethe following: (1) the patient who needed no support for dailylife before ictus; (2) severe neurological deficits with/withoutcognitive dysfunction were present; (3) diffusion-weightedimages revealed no abnormal findings orminimum early signsof ischemia on admission; (4) main artery stenosis or occlu-sion causing symptoms was confirmed; (5) medical treatment(bolus intravenous injection of heparin (5,000 IU) followed byweight-based dose of heparin infusion and oral antiplateletdrugs such as aspirin and clopidogrel) failed sufficient recan-alization and progression of ischemic symptoms; and (6)follow-up neuroimagings showed no new infarction at theaffected vascular territory.

Clinical characteristics and outcomes

The location of stenosis or occlusion was divided into fivegroups: cervical ICA, intradural ICA, proximal M1 segmentof MCA, distal M1 segment, and M2 segment. Preoperativeneurological conditions of patients were assessed byGlasgow Coma Scale. Patients outcome at discharge wasevaluated with Glasgow Outcome Scale and divided in twocategories: favorable outcome (good recovery and moderatedisability) or unfavorable outcome (severe disability, vege-tative state, and dead). Collateral flow through anterior com-municating artery, posterior communicating artery, and/orleptomeningeal anastomosis were checked by angiographyand categorized into three groups: (1) good flow, there wasno flow delay comparing with non-affected side in the arte-rial phase; (2) moderate flow, some arterial flow delay in thearterial phase without avascular area in the capillary phase;and (3) poor flow, presence of avascular area in the capillaryphase. Postoperatively, infarction area was evaluated andfollowed using CT and/or MRI.

Surgical techniques

EC-IC bypass was undertaken to restore cerebral blood flow atthe affected territory. The great majority of patients underwenturgent single or double STA-MCA anastomosis. Generally,M4segment was selected for the recipient. Based on intraoperativequalitative indocyanine green (ICG) videoangiography and/or

Doppler flowmeter findings, single or double anastomosis wascarried out. Control ICG videoangiography before anastomosisconfirmed recipient cortical arteries, which had slow antegradeor retrograde filling due to the atherosclerosis. The singlebypass was performed between the STA and one of the recip-ients. After the first bypass was complete, follow-up ICGdetermined if the blood flow had improved. If the blood flowincrease was observed at both frontal and temporal corticalarteries, we judged that the single bypass was sufficient. Bycontrast, when the blood flow increased at only frontal (ortemporal) lobe, the second bypass was carried out betweenthe STA and the one of cortical arteries at the temporal (orfrontal) lobe.

Statistical analysis

Univariate analyses employed the Pearsons 2 test (orFishers exact test when the expected frequency of eventswas

improved in 40 (69.0 %) patients after surgery. The bypasssurgery did not prevent the new infarction at the affectedvascular territory in 23 patients (39.7 %). Complications dur-ing perioperative periods are presented in Table 2. Majorcomplications happened in four patients. They included theperforator infarction (case 2) probably due to hemodynamicchange [1] and remote infarction (posterior cerebral arteryterritory). Two patients developed myocardial infarction andone died due to the myocardial infarction. No hemorrhagicinfarction happened after bypass. Postoperative MR angiog-raphy and/or angiogram were performed on 38 of the 58patients, 37 of whom had patent bypasses.

Forty-three (74.1 %) and 15 (25.9 %) patients had favor-able (good recovery, 29; moderate disability, 14) and unfa-vorable (severe disability, 14; vegetative state, 0; dead, 1)

outcomes, respectively. Favorable and unfavorable out-comes after urgent STA-MCA bypass were detailed inTable 3. Univariate analysis identified two significant asso-ciations for unfavorable outcome: insufficient collateral flow(P=.003) and new infarction after surgery (P

Illustrative case 1

This 70-year-old man presented with right hemiparesis,aphasia, agnosia, and acalculia. MRI demonstrated smallischemic lesions on diffusion-weighted images (Fig. 1),and subsequent angiograms disclosed the left M1proximalocclusion with moderate leptomeningeal collateral flow(Fig. 1). Medical treatment was not effective, and surgicaltreatment was performed on day 0. He underwent STA-MCAbypass. After fronto-temporal craniotomy, retrograde bloodflow of cortical arteries was confirmed. Firstly, the parietalbranch was anastomosed to the precentral artery with 18 minocclusion time. After anastomosis, blood flow increased inascending frontal and temporal cortical arteries, but notparietal arteries. Therefore, second bypass was carried outbetween the frontal branch and the anterior parietal artery.The second occlusion time of M4 arteries was 22 min.Postoperatively, he recovered well, and neurological symp-toms were resolved on day 1. No new infarction was seen onCT and MRI. He was discharged without neurological defi-cits on day 9. Postoperative angiogram 3 months later re-vealed the STA fed the left MCA territory (Fig. 2).

Illustrative case 2

A 70-year-old woman was transferred with global aphasia andwithout motor weakness. Neuroimages disclosed an M2 se-vere stenosis (Fig. 3). The lateral lenticulostriate arteries orig-inated from the stenotic portion (Fig. 3). She underwent singleSTA-MCA anastomosis uneventfully. After surgery, aphasiaimproved; however, right hemiparesis developed. Follow-upCT scans revealed new infarction in the basal ganglia and

Fig. 1 Case 1. ac Diffusion-weighted images reveal small infarctionarea in the left hemisphere. d, e Preoperative lateral view of left carotidangiograms showing middle cerebral artery occlusion and moderatecollateral flow through anterior cerebral artery

Fig. 2 Case 1. Anteroposterior (a) and lateral (b) projections of leftcarotid artery injection showing a good blood supply through bypass

Fig. 3 Case 2. Preoperative magnetic resonance imaging (a) demon-strates no infarction at the basal ganglia. Anteroposterior (b), oblique(c), and lateral (c) projections of left carotid artery injection showing asevere stenosis (arrow) at the superior trunk and perforating arteries(arrowhead) originating from the stenotic lesion

Fig. 4 Case 2. Postoperative computed tomography (a, b) revealingnewly developed infarction at the basal ganglia and coronal radiation,but not cortex

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coronal radiation fed by the lateral lenticulostriate arteries(Fig. 4). Postoperative angiogram was not performed. Shewas transferred to a rehabilitation hospital.

Discussion

Since there are only a few reports concerning urgent EC-ICbypass in atherosclerotic steno-occlusive disease, we retro-spectively evaluated 58 consecutive patients who underwenturgent EC-IC bypass surgery in an attempt to augment bloodflow of ischemic brain.

In general, early antegrade recanalization is the optimaltreatment for ischemic stroke. Although intravenous, intra-arterial, and mechanical thrombolysis are accepted as a stan-dard treatment in acute phase, they are often unsatisfactory.Additionally, late antegrade recanalization has a risk ofreperfusion-related hemorrhagic complication. We previouslyreported the efficacy of open embolectomy in patients withcardioembolic MCA or ICA occlusion [4, 6]. In patients withsymptomatic ICA or MCA arteriosclerosis except for segmen-tal cervical ICA stenosis, antegrade surgical revascularization isusually difficult. Therefore, EC-IC bypass is applied and aug-ments cerebral blood flow (CBF) with low-flow reperfusion.Emergency EC-IC bypass would improve neurological deficitsresulting from a small amount of blood flow into ischemicbrain related to steno-occlusion of arteriosclerosis. Nussbaumet al. [7] demonstrated excellent results of emergency bypass in13 carefully selected patients. Majority of patients (84.6 %)suffered ICA or MCA dissection, not atherosclerosis. All pa-tients improved from their preoperative neurological status, andeight (61.5 %) patients recovered completely within 6 monthsafter surgery. New infarction at the affected side was observedin only one patient. Hwang and colleagues [5] presented theirurgent EC-IC bypass results in nine patients with relativelysmall infarction (120 %), and fluctuating or progressive symptomsresistance to medical or endovascular therapy. They concludedthat urgent bypass was useful in highly selected patients eval-uated with multimodal and advanced CT and MRI. The CBFstudy is one of useful tools to assess necessity of revasculari-zation surgery. Recent advances of MRI perfusion imageswithout contrast medium demonstrated the potential of becom-ing the standard tool to estimate regional CBF in acute ischemicstroke [9]. However, it is very difficult to judge a treatablepenumbra area.

In the present study, we found that 69.0 % of patientsshowed an improvement of neurological function after sur-gery although new infarction area on CT or MRI developedin 40 % patients after bypass surgery. The risk factor ofunfavorable outcome was new infarction and collateral flow.However, age, side, sex, and affected location were notassociated with unfavorable outcome. The importance of

collateral flow has been reported in patients undergoingurgent cerebral revascularization surgery [3, 4, 11]. In thisstudy, collateral flow was evaluated with cerebral angiogra-phy and therapeutic penumbra was assumed according tofollow-up CT scan.

There were no hemorrhagic infarctions as a complicationin this study. This result was consistent with recent investi-gations [5, 7]. However, previous study [11] demonstratedthat 4 (11 %) of 35 patients had hemorrhagic infarction afterurgent bypass surgery. This study probably included patientssuffering from cardio-embolic stroke. In general, atheroscle-rosis gradually affects main trunk arteries compared withembolic stroke. We reported the hemorrhagic infarction afteropen embolectomy happened in 3 (10 %) of 30 patients [3].Therefore, low flow bypass surgery comparing with embo-lectomy and carotid endarterectomy may be a relative lowrisk of hemorrhagic transformation. According to recentpublications [5, 7] of urgent EC-IC bypass, no reperfusion-related complications were observed. In the present study,perforator infarction occurred after bypass surgery in thepresented case 2. Severe stenosis may result in occlusiondue to the counter blood supply through the anastomosis.Our findings indicated that apart from improvement of cor-tical blood flow, perforating artery occlusion can also occurafter bypass surgery. Therefore, special attention should bepaid in patients with perforating arteries originating from theseverely stenotic artery.

Conclusions

We reviewed 58 patients who underwent urgent EC-IC by-pass and presented the surgical results. This study is thelargest series to date. However, the present study has anumber of shortcomings that should be addressed. It doesnot include sufficient CBF evaluation, long-term follow-up,and a randomized medical control group. Until further stud-ies without these shortcomings are performed, the efficacyand safety of urgent EC-IC bypass for symptomatic ICA orMCA arteriosclerosis cannot be determined.

References

1. Hayashi T, Shirane R, FujimuraM, Tominaga T (2010) Postoperativeneurological deterioration in pediatric moyamoya disease: watershedshift and hyperperfusion. J Neurosurg Pediatr 6:7381

2. Horiuchi T, Kusano Y, Asanuma M, Hongo K (2012) Posteriorauricular arterymiddle cerebral artery bypass for additional surgeryof moyamoya disease. Acta Neurochir (Wien) 154:455456

3. Horiuchi T, Nitta J, Ogiwara T, Sakai K, Hongo K (2009) Outcomepredictors of open embolectomy in middle cerebral artery occlu-sion. Neurol Res 31:892894

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4. Horiuchi T, Nitta J, Sakai K, Tanaka Y, Hongo K (2007) Emergencyembolectomy for treatment of acute middle cerebral artery occlu-sion. J Neurosurg 106:257262

5. Hwang G, Oh CW, Bang JS, Jung CK, Kwon OK, Kim JE, Bae HJ,Han MK (2011) Superficial temporal artery to middle cerebralartery bypass in acute ischemic stroke and stroke in progress.Neurosurgery 68:723729

6. Murata T, Horiuchi T, Nitta J, Sakai K, Ogiwara T, Kobayashi S,Hongo K (2010) Urgent open embolectomy for cardioemboliccervical internal carotid artery occlusion. Neurosurg Rev 33:341348

7. Nussbaum ES, Janjua TM, Defillo A, Lowary JL, Nussbaum LA(2010) Emergency extracranial-intracranial bypass surgery foracute ischemic stroke. J Neurosurg 112:666673

8. Powers WJ, Clarke WR, Grubb RL Jr, Videen TO, Adams HPJr, Derdeyn CP (2011) Extracranialintracranial bypass surger-y for stroke prevention in hemodynamic cerebral ischemia: theCarotid Occlusion Surgery Study randomized trial. JAMA306:19831992

9. Rahmah NN, Horiuchi T, Kusano Y, Seguchi T, Hanaoka Y,Aoyama T, Hongo K Early changes of tissue perfusion after tissueplasminogen activator in hyperacute ischemic stroke: initial expe-riences with arterial spin labeling perfusion MRI. Neurol Med Chir(Tokyo) 53:213216

10. Sakai K, Nitta J, Horiuchi T, Ogiwara T, Kobayashi S, Tanaka Y,Hongo K (2008) Emergency revascularization for acute main-trunkocclusion in the anterior circulation. Neurosurg Rev 31:6976

11. Yoshimoto Y, Kwak S (1995) Superficial temporal arterymiddle cerebral artery anastomosis for acute cerebral ischemia:the effect of small augmentation of blood flow. Acta Neurochir(Wien) 137:128137

Comments

Akitsugu Kawashima, Tokyo, JapanThis article describes excellent results with emergency EC-IC by-

pass in a big cohort of acute ischemic stroke cases, induced by athero-sclerotic stenosis or occlusion of the ICA or MCA. The authors con-cluded that 69 % of the patients improved and only 8.6 % worsened bythis procedure. Emergency EC-IC bypass for acute ischemia has beentraditionally considered a contraindication, due to the potential reper-fusion ischemic injury1. However, the authors reported few surgicalcomplications, especially no hemorrhagic complications, despite thelarge number of cases. Recently, some papers stated similar findings2,3.These data may become also valuable for management by surgical acuteflow replacement in general.

Particular attention deserves the described 74.1 % favorable out-come (good recovery, 50 % and moderate disability, 24.1 % as GlasgowOutcome Scale) in patients treated with this procedure, which wassuperior to endovascular therapies (intravenous tissue plasminogenactivator application or intraarterial thrombolysis).4

As authors also indicate, this study has some limitations due to thelack of CBF evaluation and for not being a randomized control study.However these data may encourage the interest of neurosurgeons totreat atherosclerotic stroke and reconfirm these findings.

References1. Gratzl O, Schmiedek P, Spetzler R, Steinhoff H, Marguth F.

Clinical experience with extra-intracranial arterial anastomosis in 65cases. Journal of neurosurgery. 1976;44:313324

2. Diaz FG, Ausman JI, Mehta B, Dujovny M, de los Reyes RA,Pearce J, et al. Acute cerebral revascularization. Journal of neurosur-gery. 1985;63:200209

3. Nussbaum ES, Janjua TM, Defillo A, Lowary JL, Nussbaum LA.Emergency extracranial-intracranial bypass surgery for acute ischemicstroke. Journal of neurosurgery. 2010;112:666673

4. Ciccone A, Valvassori L, Nichelatti M, Sgoifo A, Ponzio M, SterziR, et al. Endovascular treatment for acute ischemic stroke. The NewEngland journal of medicine. 2013;368:904913

William J. Powers, Chapel Hill, USADr. Horiuchi and colleagues have documented their experience with

58 patients treated by urgent EC-IC bypass for acute ischemic strokebased on retrospective medical records review. These patients diffusion-weighted images revealed no abnormal findings or minimum early signsand medical therapy with heparin infusion and oral antiplatelet drugsfailed to provide sufficient recanalization and halt progression of ischemicsymptoms. Presumed atherosclerotic stenosis or occlusion of the internalcarotid artery (ICA) or middle cerebral artery (MCA) was confirmed byangiography. Thirty-four (58.6 %) were operated the day of onset andmost were operated within 2 days. Postoperative MR angiography and/orangiogram showed a patent bypass in 37 of 38 in whom it was performed.No patient received intravenous tPA, though it is not stated how manywould have met eligibility criteria. New infarction developed in 23(40 %), and major complications occurred in 4 including one death dueto myocardial infarction. Forty-three (74 %) patients had favorable (Glas-gow outcome score 45) and 15 (26 %) patients had unfavorable (Glas-gow outcome score, 13) outcome.

How do these data help us in treating patients with acute stroke withstenosis or occlusion of the MCA or ICA? They do not. In the absenceof a randomized control group, it is impossible to determine if the EC-IC bypass surgery helped or hurt these patients. The 74 % rate offavorable outcome is likely due to the careful selection of patients toexclude those with a large diffusion lesion, a major determinant of pooroutcome after stroke [1]. A patent bypass is not evidence of clinicalefficacy; reperfusion will only ameliorate the effects of acute ischemicstroke if performed very rapidly, probably within 6 h in those with persistent ICA orMCA occlusion provides no benefit [5] and even delays of one hourrender the better recanalization achieved by intra-arterial approaches nobetter than intravenous tPA [6]. Thus, revascularization by EC-ICbypass as reported here is highly unlikely to prove to be of benefit evenif tested in a randomized, controlled trial. The treatment of choice forthose with acute ischemic stroke with MCA or ICA occlusion who metNINDS or ECASS III criteria is intravenous tPA and for those who donot, it is anti-platelet therapy [2,3,7,8].

References1. Parsons MW, Christensen S, McElduff P, Levi CR, Butcher KS,

De Silva DA, Ebinger M, Barber PA, Bladin C, Donnan GA, Davis SMEchoplanar Imaging Thrombolytic Evaluation Trial (EPITHET) Inves-tigators (2010) Pretreatment diffusion- and perfusion-MR lesion vol-umes have a crucial influence on clinical response to stroke thrombol-ysis. J Cereb Blood Flow Metab 30:121425.

2. The National Institute of Neurological Disorders and Stroke rt-PAStroke Study Group (1995) Tissue plasminogen activator for acuteischemic stroke. N Engl J Med 333:15811588

3. Hacke W, Kaste M, Bluhmki E, Brozman M, Dvalos A, GuidettiD, Larrue V, Lees KR, Medeghri Z, Machnig T, Schneider D, VonKummer R, Wahlgren N, Toni D, For the ECASS Investigators(2008) Thrombolysis with alteplase 3 to 4.5 hours after acute ischemicstroke. N Engl J Med 359:13171329

4. Powers WJ (2012) Thromobolysis for acute ischemic stroke: isintra-arterial better than intravenous? A treatment effects model. JStroke Cerebrovasc Dis 21:4013.

5. Kidwell CS, Jahan R, Gornbein J, Alger JR, Nenov V, Ajani Z,Feng L, Meyer BC, Olson S, Schwamm LH, Yoo AJ, Marshall RS,Meyers PM, Yavagal DR, Wintermark M, Guzy J, Starkman S, Saver

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JL, M.D. for the MR RESCUE Investigators (2013) A trial of imagingselection and endovascular treatment for ischemic stroke. N Engl J Med368:91492

6. Ciccone A, M.D., Valvassori L, Nichelatti M, Sgoifo A, PonzioM, Sterzi R, Boccardi E, for the SYNTHESIS Expansion Investigators(2013) . Endovascular treatment for acute ischemic stroke. N Engl JMed 368:90413.

7. Chen ZM, Sandercock P, Pan HC, Counsell C, Collins R, Liu LS,Xie JX, Warlow C, Peto R on behalf of the CAST and IST collaborativegroups.(2000) Indications for early aspirin use in acute ischemic stroke:a combined analysis of 40 000 randomized patients from the ChineseAcute Stroke Trial and the International Stroke Trial. Stroke.31:12409

8. Wang Y, Johnston SC, Wang Y, Zhao X, Liu L, Wang D, Wang C,Wang C, Meng X, Cui L, Jia J, Dong Q, Xu A, Zeng J, Li Y, Wang Z,Xia H, for the CHANCE investigators. Clopidogrel and aspirin versusaspirin alone for the treatment of high-risk patients with acute non-disabling cerebrovascular event (CHANCE): a randomized, double-blind, placebo-controlled multicenter trial. Presented at the Internation-al Stroke Conference, Honolulu, HI February 8, 2013

Rod Samuelson, Phoenix, USAThe authors present and important series of 58 patients with emer-

gent EC-IC bypass for symptomatic atherosclerotic ischemic stroke.The included patients presented with acutely symptomatic stenosis orocclusion of the cervical/intracranial internal carotid artery or M1 / M2middle cerebral artery. This group of patients was not evaluated in thelarger (negative) trials for EC-IC bypass. Patient selection was by acareful process including severe symptoms, favorable neuroimaging,and lack of response to basic medical interventions. Endovascularinterventions were used on an unspecified number of patients as well.

In general, the patients had favorable outcomes, and 69 % hadimproved neurologic function postoperatively. However, 40 % of thepatients went on to have strokes in the affected vascular territory.

This is an important series of patients for study and consideration,although the algorithm for stroke treatment in these patients is some-what different than that advocated by the American Heart Association/American Stroke Association. My main reservation with this paper isthat some of the included patients may have benefited from IV tPA oradditional endovascular treatments. Intracranial atherosclerosis is not acontraindication for IV tPA that I am familiar with. Nevertheless, whenpatients are treated with emergent EC-IC bypass, they appear to have asimilar potential for favorable outcome as those treated with IV tPA orintra-arterial interventions.

For future study, comparison with patients who receive standardtherapies is in order. Intracranial balloon angioplasty and stenting is alsoan attractive alternative.

Albert van der Zwan, Utrecht, The NetherlandsThe study of Dr Horiuchi and colleagues clearly demonstrates that

early bypass surgery in a broad cohort of symptomatic internal carotidartery or the middle cerebral artery stenosis of occlusion can be donesafely performed within 2 days after the first ictus. Although previouspublications describe hyperperfusion rates between 0.6 and 15 %, theresults of this study are splendid with no hyperperfusion complicationshaving occurred.1,2,3

Yet, it is still unclear what the reason is for this. The explanation ofthis by suggesting that more proximal diseases like in this study couldbe the reason for this is not very strong as MCA stenosis is not onlyproximally located per se.

Yet, the absence of hemorrhagic conditions cannot be the final goal ofa study to determine a role for EC-IC bypass surgery in ischemic cerebralconditions. As the authors already denoted, this is a retrospective study onbypass surgeries performed on a broad scale of patients groups (stenosisor occlusion of the precommunicating ICA and postcommunicating ICAand MCA), still without DWI image infarcts, using one or two EC-ICbypasses without determining added blood flows.

This diversity of patients and therapy in this study is the reason thatthis study will not help us in deciding whether bypass surgery will bebeneficial for a selected group of patients.

Stenosis or occlusion of any artery and the existence of sufficientcollaterals play an important role in the final outcome. In addition, it isunclear whether in this cohort of patients pure hemodynamic or addi-tional embolic factors play a role in the neurological outcome. Theexistence of a stenosis does not tell us whether any infarction isoriginated in embolus or hemodynamics. In addition, the assessmentof the Glasgow Coma (Outcome) Scale in inclusion and follow-upcould miss essential factors in patient assessment 4. The therapeuticalwindow in this study varied between 0 and 2 days. In addition, thisrelatively broad time frame could disturb the results. Moreover, the useof one or two bypasses based on ICG does not give any informationabout flows that are added to the specific patients. ICG is, until now, noflow measurement technique. In the best, it can give information aboutflow velocities and direction. Therefore, to our experience, added flowsin this study may vary between 10 and 90 ml/min which is again a broadspectrum.

Finally, the described 74.1 % of patients having favorable outcomedoes not tell us what the additional value of the bypass was in thesepatients. In the COSS study, the functional outcome of the nonsurgicalpatients was much better than in previous studies (follow up, 2 years),and it is difficult to compare the results of the present study (follow up atdischarge) with the COSS study.4

In conclusion, this study is helpful in the discussion on the risk ofhemorrhagic complications of acute bypass surgery, but does not helpus in the search for selected patients that could benefit from this type ofsurgery. For that, we need more specific pathology inclusion, moredefined functional investigations (MRI, MRF, and MRS), and morequantitative data on the added flows than has been used in this (orCOSS) study.

Therefore, it is important that more studies like this encourageneurosurgeons in close cooperation with neurologists to perform morespecific research on selected patient groups that could benefit from EC-IC bypass surgery.

References1. The EC-IC Bypass Study. N Engl J Med. 1987;317:103010322. Sundt TM jr, Whisnant JP, Fode NC, Piepgras DG, Houser OW.

Results. Complications, and follow-up of 415 bypass-operations forocclusive disease of the carotid system. Mayo Clin Proc.1985;60(4):230240

3. Van Doormaal PC, Klijn CJM, van Doormaal PTC, Kapelle LJ,Regli L, Tulleken CAF, van der Zwan A. High-flow extracranial-to-intracranial excimer laser-assisted nonocclusive anastomosis bypass forsymptomatic carotid artery occlusion. Neurosurgery. 2011;68(4):16871693

4. Powers JP, Clarke WR, Grubb Jr RL, Videen TO, Adams jr HP,Derdeyn CP. Extracranial-intracranial bypass surgery for stroke preven-tion in hemodynamic cerebral ischemia. JAMA. 2011; 206(8):19831992

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Emergency EC-IC bypass for symptomatic atherosclerotic ischemic strokeAbstractIntroductionPatients and methodsPatient populationManagement of patientsClinical characteristics and outcomesSurgical techniquesStatistical analysis

ResultsIllustrative case 1Illustrative case 2

DiscussionConclusionsReferences