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KOR J CEREBROVASCULAR SURGERY September 2OO7 Vol. 9 No 3, page 177-82 가톨릭대학교성모병원신경외과가톨릭뇌신경센터오종양 최환영 주원일 조정기 박해관 이경진 나형균 박춘근 Effectiveness of Bypass surgery in Treatment and Prevention of Ischemic Symptoms due to Intracranial Arterial Stenosis JY Oh, MD, WY Choi, MD, WI Joo, MD, CK Cho, MD, HW Park, MD, KJ Lee, MD, HK Rha, MD, CK Park, MD Catholic Neuroscience Center, Department of Neurosurgery, St. Mary's Hospital Catholic University ABSTRACT Objective : Although extracranial-intracranial(ec-ic) bypass surgery is considered an appropriate treatment in selected cases of cerebrovascular ischemic disease, this procedure can also be associated with significant morbidity, some of which (especially intracranial stenotic lesions) paradoxically may be the direct result of the patent bypass. This study examined the effectiveness of EC-IC bypass surgery in the treatment and prevention of a cerebral infarct from an intracranial arterial stenosis. Methods : During the recent 7 years, EC-IC bypass surgery was performed on 90 patients whose cerebrovascular reserve capacity were significantly impaired due to an occlusion or stenosis(over 70%) of the ICA and/or MCA. Of these 90 consecutive patients, 33 patients had a stenosis of the intracranial ICA or MCA. Of these 33 patients, the type of ischemic episode was transient ischemic attack (TIA) in 11, reversible ischemic neurological deficit (RIND) in 9 and a complete stroke in 13. Results : The postoperative courses were uneventful in 26 cases, temporary neurologic deficit was found in 5, a permanent deficit was encountered in one and focal seizure occurred in one. The bypass patency was confirmed by a postoperative angiogram or MRA in all cases except for one. A postoperative cerebral blood flow study including acetazolimide stimulation showed significant improvement in all cases except for 2 cases (one case with bypass failure and the other with a post-bypass occlusion of the preoperative stenotic segment). During the follow up period after revascularization surgery, there were no further strokes in any patient who had undergone EC-IC bypass surgery. The postoperative long-term follow up angiogram or MRA showed an occlusion of the preoperative stenotic segment in 6 cases, progression in 7, regression in 2 and no change in the remaining 18. Conclusion : In view of these findings, EC- IC bypass surgery on a stenotic lesion of the intracranial ICA or MCA is effective andnot dangerous despite possibility of a post-bypass occlusion of the stenotic lesion. Therefore, the authors conclude that EC-IC bypass surgery constitutes an appropriate treatment for a subgroup of patients with an intracranial arterial stenosis. (Kor J Cerebrovascular Surgery 9(3):177-82, 2007) KEY WORDS : Intracranial arterial stenosis Extra-intracranial bypass surgery Hemodynamic cerebral ischemia Postbypass occlusion 서 론 논문접수일 : 2007 년 06 월 18 일심사완료일 : 2007 년 07 월 20 일교신저자 : 나형균, 서울시영등포구여의도동 62 번지가톨릭대학교성모병원신경외과전화 : (02) 3779-2161 전송 : (02) 785-6365 E-mail : hkrha@catholic.ac.kr 허혈성뇌혈관질환은주로경동맥및뇌내동맥의경화로인한동맥폐쇄또는협착으로발생한다. 이중뇌내동맥의협착이전체뇌허혈질환의 8~10% 를차지한다. 18) 그러나한국을포함하는아시아, 아프리카및히스페닉계통에서는서구에비해뇌내동맥의협착으로인한뇌경색증의빈도가높다. 11)17) 뇌 177

내동맥협착중, 중대뇌동맥협착의자연경과는비교적안정적이며예후도나쁘지않다는보고도있으나 12) 최근에발표된논문들은중대뇌동맥의협착환자에서내과적인치료만으로는매년 8~22% 정도의높은빈도로뇌경색증이유발된다고보고되고있다. 3)5) 특히 Corston 등 5) 은 21명의중대뇌동맥협착환자들의평균 6년간의장기추적결과 7명의환자에서재발하였으며이중 4명에서치명적인결과를나타났다고발표하였다. 이와같이증상이있는뇌내동맥협착환자는적절한내과적치료를받아도재발률이높아적극적으로관혈적치료가필요하다. 5)11)23) 뇌내동맥의협착환자에서내막절제술은시행하기가어려워선택되지않는다. 따라서뇌내동맥협착환자의수술적치료로는두개내-외혈관문합술이나혈관내수술로협착혈관을확장시킨후, 스텐트를삽입하는방법이이용되고있다. 그러나뇌내혈관협착환자에서의우회로수술은협착부위를통한정상방향의혈류와문합수술후우회혈관을통한역행성의혈류가협착부위에서충돌하게되어오히려기존의협착이악화되거나심지어는완전폐쇄를초래할수있다는보고가있으며, 1)7) 혈관내수술방법은중대뇌동맥의경우혈관의굵기가가늘어시술이어렵고성공하였다고하여도재협착의빈도가높다고알려져있으며또한시술중합병증이 4.8~8.3% 로보고되고있다. 23) 저자들은최근 7년간뇌내혈관협착환자들에서두개내-외혈관문합술로수술을시행한 33례를분석하여그결과를보고하고자한다. 대상및방법 일과성뇌허혈증상이있었거나경미한신경학적증상이남 아있는폐쇄성뇌혈관질환환자중뇌내혈관이 70% 이상좁아 진뇌내혈관협착환자를일차적인대상으로하였으며, 이들 환자에서, 안정시및 Acetazolimide를투여한후, SPECT (Single-Photon Emission Computed Tomography) 를 Table 1. Pathology of 90 patients with atherosclerotic hemodynamic cerebral ischemia performed EC-IC bypass Lesion site Number Ⅰ. Intracranial lesion 58(64%) 1. Stenosis 33(57%) 1 ICA 5 2 MCA 23 3 ICA, MCA 5 2. Occlusion, MCA 25(43%) Ⅱ. Extracranial lesion 32(36%) 1. ICA Occlusion 26 2. ICA Stenosis 6 Total 90 이용하여혈류예비능력을검사하였다. SPEG 검사결과혈류예비능력이현저히떨어진환자들에서뇌허혈증상의재발빈도가높다고알려져있으며 4)8)14)22) 저자들도뇌혈류량검사결과혈류예비능력이현저히떨어져재발의위험이높은혈역학적뇌허혈환자 33례를최종수술대상으로선택하였다. 16) 동맥경화성폐쇄성뇌혈관질환에서저자들이최근까지시행한두개내-외혈관문합술은 90례였으며이들예중, 이번연구의대상이되는두개내동맥협착이 33례였다. 33례의환자중중대뇌동맥협착이 23례, 두개내내경동맥협착이 5례, 두개내내경동맥및중대뇌동맥의동시협착이 5례였다 (Table 1). 수술전임상증상은일과성뇌허혈또는가역성허혈성신경학적결손으로수술전신경학적증상이없었던예가 20례, 뇌허혈발작후, 신경학적결손증상이남아있는환자가 13례였다. 수술방법은 33례중 3례에서대복제정맥 (2례) 이나요골동맥 (1례) 을이용한이식문합수술을, 2례에서측두동맥전두지및두정지모두를중대뇌동맥에문합하는이중문합수술을시행하였으며 28례에서기존의측두동맥-중대뇌동맥문합수술을시행하였다. 결과 수술합병증수술을시행한 33례중 26례는수술후, 수술후유증이전혀없었으나, 6례에서는수술후, 신경학적증상이악화되었으며이중 5례는일시적인증상으로수술 3주이내에완전회복되었으나한예에서는재관류손상으로생각되는언어장애증상이남아있다. 또한한예에서는수술후일시적인국소경련이있었다. 임상경과수술후, 임상증상의변화는신경학적증상이남아있던 13 례에서수술 3~6개월후, 미국국립보건원의뇌졸중척도 (NIHSS) 를기준으로판정하였으며이결과 8례에서호전을보였고, 4례에서는증상의변화가없었으며나머지한예에서는수술후, 재관류손상으로생각되는언어장애증상이일부악화되었다. 수술후, 추적관찰기간 (3개월 ~7년 ) 동안뇌허혈증상이재발된예는없었다. 수술후뇌혈관촬영및 MRA 촬영수술후, 문합부를통한재관류정도및수술전협착부위의변화를관찰하기위해서 19례에서는뇌혈관촬영을, 14례에서는 MRA를촬영하였다. 문합부를통한재관류는전체 33례중한예에서문합부폐쇄소견을보였으며 32례에서문합부를통한재관류가이루어졌다. 또한수술전, 후협착부위의협착 178 Kor J Cerebrovascular Surgery 9(3):177-82, 2007

오종양 최환영 주원일 조정기 박해관 이경진 나형균 박춘근 정도를비교하여협착부위가폐쇄된군을폐쇄군, 협착이 10% 이상진행된군을진행군, 10% 이상완화된군을완화군, 10% 미만의차이를나타낸군을변화없음으로분류하였다. 그결과 6례에서는수술전협착부위가완전폐쇄되었으며, 7례에서는협착이진행되었고, 2례에서는오히려협착이완화되었으며 18례에서는협착정도의변화가없었다. 협착부위가완전폐쇄된 6례중 1례에서만이일시적인신경학적증상이악화되었으나 5례에서는증상의악화가없었다 (Table 2). 수술후뇌혈류량의변화수술후, 안정기및 Acetazolimide를투여한후, 뇌혈류량검사를시행하였다. 뇌혈류량검사는병변부위와반대편의정상부위에서관심영역을정한후, 방사선동위원소양을측정하여양측을비교하여 Asymmetry index를측정하였으며수술전과비교하였다. 그결과문합부가폐쇄된 1례에서는변화가없었으며수술후협착부위가완전히폐쇄되어일시적인뇌허혈증상이나타났던한예에서는오히려감소하였으나나머지 31례에서는방사선동위원소양이 10% 이상증가된혈류예비능력의향상을보였다. 고찰 경동맥및뇌내동맥의협착이나폐쇄에의한뇌허혈증의치료및예방에있어서두개내-외혈관문합수술은이수술법이뇌허혈증상의예방에효과적이지못하다는 1985년도의국제적인합동연구결과 20) 의발표로그이용이매우제한되었으나이후, 혈역학적뇌허혈의개념이도입되고적절한적응증을갖는환자들에서이수술의효과가입증된이후, 현재까지꾸준히이용되고있다. 2)6)13)15)16)18)19)21)24)25) 그러나뇌내동맥의협착으로인하여뇌허혈증상이나타난환자에서의우회로수술은수술후, 오히려기존의협착이악화되거나심지어는완전 폐쇄를초래할수있다는보고가있어 7)9) 이수술을시행하는데있어제약이되어왔다. 그러나뇌내동맥의협착은충분한내과적치료를하더라도높은빈도로뇌허혈증상이재발하며재발할경우치명적인증상을유발한다고보고되고있다. 3)5) 현재이에대한예방및치료방법으로혈관내수술방법이시도되고있으며그동안의경험축적결과두개내내경동맥및추골, 기저동맥의경우긍정적인효과가보고되고있으나중대뇌동맥의경우혈관의굵기가가늘어시술이어렵고시술중, 합병증이나타날수있으며, 성공하여도재협착의빈도가높다고알려져있다. 11)23) 뇌내혈관협착환자에서우회로수술을시행할경우, 협착부위를통한정상방향의혈류와문합수술후, 우회혈관을통한역행성의혈류가협착부위에서충돌하게되어소용돌이 (vortex) 를일으키거나역행성의혈류에의해서정상방향의혈류에의한협착부위의혈류속도가감소되어오히려기존의협착이악화되거나심지어는완전폐쇄를초래할수있다고보고되고있으며저자들에따라서 20~25% 를보고하기도한다. 7)9) Gumerlock 등 9) 은 18명의협착환자에서우회로수술후 5례 (28%) 에서협착부위가완전폐쇄되고신경학적증상이악화되었다고발표하였으며따라서협착환자에서의두개내- 외혈관문합술은협착부위의위치, 환자의증상등을잘검토하여신중하게결정해야할것으로보고하였다. 저자들의경우, 두개내-외혈관문합술을시행한뇌내혈관협착환자 33례중수술후, 6례 (18%) 에서협착부위가완전히폐쇄되었다. 그러나 Gumerlock 등 9) 및 Furlan등 7) 의보고와는다르게이들 6례중영구적인신경학적결손증상이나타난예는없었으며한예에서만이일시적으로신경학적증상이나타났으나 2주이내에완전소실되었다. 수술전협착부위가수술후완전히막힌 6례중 4례에서는수술후 2주에촬영한뇌혈관촬영에서나타났으나 (Fig. 1) 2례는수술 1년후검사한뇌 MRA 상지연성으로폐쇄되었다 (Fig. 2). 또한수술후, 협착부위가심 Table 2. Postbypass change of degree of stenosis and correlation between degree of postbypass change of the preoperative stenosis and degree of circulation through the bypass Change of Degree Filling via bypass of stenosis No. Patients Excellent ** Fair Not Patent Occlusion 6(18%) 5 * Progression 7(21%) 3 * 1 * Regression 2(6%) 1 * No change 18(55%) 5 * 3 * 1 * * Degree of circulaton through bypass in 19 cases which was performed postoperative angiogram. ** Excellent means extensive circulation of main branch of the middle cerebral artery through the bypass. Kor J Cerebrovascular Surgery 9(3):177-82, 2007 179

해진예들은 7례있었으나모든예에서신경학적증상이재발되거나악화된예는없었으며오히려문합혈관을통한혈류증가로혈류예비능력의향상을보였다. 문합수술후협착부위가완전폐쇄되거나협착이심해진예들은혈관촬영결과대부분의예에서문합부를통한광범위한순환이이루어지고있는예들이었다 (Table 2). 즉, 문합부를통한광범위한순환으로기존의협착부위를통한혈류가감소되어협착부위가막히거나더욱좁아졌으리라생각되며따라서협착부위가막히거나좁아져도문합부를통한광범위한순환으로혈류예비능력은오히려향상을보였으리라판단된다. 중대뇌동맥의협착환자에서는문합수술후, 협착부위가완전폐쇄되는것을예방하기위하여, 수술후, 저혈압이초래되는것을막아야하고, 수술후, 조기에항혈소판제나항응고제등의복용이필요하며, 문합수술시고혈류문합보다는저혈류문합이도움이된다고알려져있다. 7)9) 뇌내혈관협착에의한뇌경색증은불충분한혈류로인한혈역학적저관류, 동맥벽의죽상편의파열로인한협착부위의혈전형성, 협착원위부혈전성폐쇄, 및관통동맥의폐쇄등에의해발병한다고알려져있으며이중불충분한 혈류로인한혈역학적저관류환자들에서두개내-외혈관문합술이이용될수있다. 11) 최근혈관내시술법의발달로뇌내혈관의협착에대해서도혈관확장및스텐트삽입수술이많이시도되고있으나이시술법은혈관굵기가 2.5~4.5mm정도의굵은혈관에서가능하기때문에뇌내혈관중중대뇌동맥의경우기술적으로시술이어려우며특히시술에성공하여도재협착의빈도가높다. Wojak 등 23) 은뇌내혈관협착환자에서혈관확장수술및스텐트삽입시술결과시술중뇌졸중이발병하거나사망할확률이 4.8% 라고하였으며시술후뇌졸중이재발하거나사망할빈도는 1년에 3% 라고보고하였다. 저자들의수술결과에서수술후 1례에서만이영구적인언어장애가있었으나이예는수술전혈관촬영직후, 혈관촬영에의한뇌손상이인지되었으나뇌손상부위가크지않아충분히치유될때까지기다리지않고서둘러 ( 혈관촬영후 1주일 ) 수술을시행한예로이미뇌손상을받은부위에재관류손상이새로가해져서합병증이나타났다고생각된다. Heros 등 10) 은이미뇌손상이있었던환자들에서는발병후 2개월후에우회로수술을시행하는것이안전하다고하였다. 저자들의수술예중영구 Fig. 1. Postoperative immediate occluded case A. Preoperative right carotid angiogram shows right middle cerebral artery stenosis. B. Postoperative right carotid angiogram shows an occlusion at the previous stenotic site. C. Postoperative external carotid angiogram shows extensive revascularization through patent bypass. Fig. 2. Postoperative delayed occluded case A. Preoperative Carotid angiogram shows right middle cerebral artery stenosis. B. Postoperative immediate MRA shows patent grafted STA and no change of preoperative stenosis of middle cerebral artery. C. Postoperative 1 year MRA shows more prominent grafted STA than the STA on immediate postoperative MRA and shows an occlusion at the previous stenotic site. 180 Kor J Cerebrovascular Surgery 9(3):177-82, 2007

오종양 최환영 주원일 조정기 박해관 이경진 나형균 박춘근 적신경학적결손이남아있는예는수술시기를잘조절하였을경우충분히예방할수있는합병증이라고판단되며이외의예들에서는최장 7년의추적관찰기간동안협착부위가수술후완전히막힌예들을포함하여전예에서증상이재발하거나악화된예들은없었다. 저자들의수술예중협착부위가완전히막힌예들은모두재관류수술에의해서막혔다고볼수없으며재관류수술후막혔다고하여도막힌 6례중뇌혈관촬영을시행한 5례모두에서이식혈관을통한광범위한순환이이루어지고있기때문에협착부위의폐쇄에의한증상이나타나지않았으리라판단되며또한일부예에서는협착부위가자연경과적으로막혔다고볼수도있기때문에이들예에서재관류수술을시행하지않았을경우, 뇌내혈관의중증협착환자의위험스런자연경과로미루어상당한후유증이나타났으리라생각할수있다. 따라서저자들의연구결과적정한수술적응증, 수술시기및수술후집중적인치료를시행할경우, 뇌내협착환자들에서도우회로수술은상당히안전하고효과적인수술로생각된다. 결 저자들은혈류량검사결과혈역학적뇌허혈로진단된뇌내동맥협착환자 33례에서두개-내외혈관문합수술을시행하여 3 개월 ~7년간의장기추적관찰결과좋은결과를얻었다. 수술후 18% 에서협착부위가완전폐쇄되었으나문합혈관을통한충분한재관류로영구적인신경학적결손증상은나타나지않았다. 전례에서추적관찰기간동안재발된예도없었다. 뇌내동맥의협착환자에서는두개내-외혈관문합술후협착부위가완전폐쇄되는것을예방하기위하여, 수술후저혈압이초래되는것을막아야하고, 수술후조기에항혈소판제나항응고제등의복용이필요하며, 문합수술시고혈류문합보다는저혈류문합이도움이된다. 따라서저자들의연구결과적정한수술적응증, 수술시기및수술후집중적인치료를시행할경우, 뇌내협착환자들에서도우회로수술은상당히안전하고효과적인수술로생각된다. 중심단어 : 뇌내동맥협착 혈역학적뇌허혈 두개내-외혈관문합수술. REFERENCES 01) Awad I, Furlan AJ, Little JR. Changes in intracranial stenotic lesions after extracranial-intracranial bypass surgery. J Neurosurg 60:771-6,1984 02) Anderson DE, Mclane MP, Reichman OH, Origitano TC. Improved cerebral blood flow and CO2 reactivity after microvascular anastomosis in patients at high risk for recurrent 론 stroke. Neurosurgery 31:26-34,1992 03) Chimowitz MI, Kokkinos J, Strong J, Brown MB, Levine SR, Silliman S, Pessin MS, Weichel E, Sila CA, Furlan AJ, Kargman DE, Sacco RL, Wityk RJ, Ford G, Fayad PB. The Wafarin-aspirin symptomatic intracranial disease study. Neurology 45:1488-93,1995 04) Chollet F, Celsis P, Clanet M. SPECT study of cerebral blood flow reactivity after acetezolimide in patients with transient ischemic attacks. Stroke 20:458-64,1988 05) Corston RN, Kendall BE, Marshall J. Prognosis in Middle Cerebral Artery Stenosis. Stroke 15:237-41,1984 06) Eguchi T. How to select the candidate of Revascularization and How to evaluate the surgical benefit. J Korean Neurosurg 27:47-51,1998 07) Furlan AJ, Little JR, Dohn DF. Arterial Occlusion Following Anastomosis of the Superficial Temporal Artery to Middle Cerebral Artery. Stroke 11(1):91-5, 1980 08) Grubb RL, Powers WJ. Risks of stroke and current indications for cerebral revascularization in patients with carotid occlusion. Neurosurgery Clinics of North America 36(3):473-85,2001 09) Gumerlock MK, Ono H, Neuwelt EA. Can a Patent Extracrnial- Intracranial Bypass Provoke the Conversion of an Intracranial Arterial Stenosis to a Symptomatic Occlusion? Neurosurgery 12(4):391-400,1983 10) Heros RC, Nelson PB. Intracerebral Hemorrhage after Microsurgical Cerebral Revascularization. Neurosurgery 6(4):371-5,1980 11) Higashida RT, Meyers PM. Intracranial angioplasty and stenting for cerebral atherosclerosis: new treatments for stroke are needed. Neuroradiology 48:367-72,2006 12) Hilton RL, Mohr JP, Ackerman RH, Adair CB, Fisher CM. Symptomatic middle cerebral artery stenosis. Ann Neurol 5:152-7,1979 13) Iwama T, Hashimoto N, Takagi Y, Tsukahara T, Hayashida K. Predictability of extracranial/intracranial bypass function : a retrospective study of patients with occlussive cerebrovascular disease. Neurosurgery 40:53-9,1997 14) Okudaira Y, Bandoh K, Arai H, Sato K. Evaluation of the acetazolamide test. Stroke 26:1234-9,1995 15) Powers WJ, Grubb RL, Raichle ME. Clinical results of extracranial-intracranial bypass surgery in patients with hemodynamic cerebrovascular disease. J Neurosurgery 79:61-7,1998 16) Rha HK, Lee KJ, Cho KK, Park SC, Park HK, Cho JK, Ji C, Son HS, Kang JK, Choi CR. Improvement of Cerebrovascular Reserve Capacity by Bypass Surgery in Patients with Hemodynamic Cerebral Ishemia. J Korean Neurosurg 28:35-41,1999 17) Sacco RL, Kargman DE, Gu Q, Zamanillo MC. Race ethnicity and determinants of intracranial atherosclerotic cerebral infarction. The Northern Manhattan stroke study 26(1):14-20,1995 18) Schmideck P, Piepgras A, Leinsinger G, Kirsch CM, Einhaupl K. Improvement of cerebrovascular reserve capacity by EC-IC arterial bypass surgery in patients with ICA occlusion and hemodynamic cerebral ischemia. J Neurosurg 81:236-44,1994 19) Spetzler RF and Hadley MN. Extracranial to intracranial bypass grafting. in Wilkins RH, Rengachary SS(eds). Neurosurgery ed 2 New York. McGRAW-Hill Health Professions Division 2:2157-67,1996 20) The EC/IC Bypass study group. Failure of Extracranial-intracranial arterial bypass to reduce the risk of ischemic stroke. Results of an international randomized trial. N Engl J Med 313:1191-200,1985 Kor J Cerebrovascular Surgery 9(3):177-82, 2007 181

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