STA-MCA Surgery for Moyamoya Disease

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Superficial temporal artery to middle cerebral artery (STA-MCA) = bypass=20 surgery was developed as a treatment for patients with ischemic=20 cerebrovascular disease secondary to vascular lesions that are=20 inaccessible by carotid endarterectomy. Direct measurements of = blood=20 pressure within middle cerebral artery branches showed = significantly=20 decreased pressures in patients with intracranial occlusive = disease who=20 experienced transient ischemic attacks (TIAs) or minor stroke. A = direct=20 bypass to the middle cerebral artery would provide a collateral = channel=20 for additional blood flow to these ischemic areas and, in theory, = improve=20 perfusion.

COMMON INDICATIONS FOR SUPERFICIAL = TEMPORAL=20 ARTERY TO MIDDLE CEREBRAL ARTERY BYPASS

Atherosclerotic Disease

The most common indication for STA-MCA bypass has been = symptomatic=20 atherosclerotic disease of the intracranial internal carotid = artery (Figs.=20 1, 2, = 3) = or the=20 MCA (Figs. 3, = 4). = These=20 patients experience decreases in cerebral blood flow (CBF) that = produce=20 what has been called "misery perfusion." Ischemic regions of = cortex could=20 benefit from collateral flow and should decrease patient symptoms = related=20 to low CBF. The most frequently performed STA-MCA bypass is a = direct=20 arterial anastomosis from a branch of the STA to an MCA branch = emerging=20 from the sylvian fissure. Such grafts have been shown to result in = additional blood flow of 25 to 50 mL/min, which may increase as = the graft=20 matures (9). Increased flow rates may be obtained with = interposition vein=20 grafts, which deliver flows of as much as l00 mL/min immediately = after=20 anastomosis, or by grafting the STA to more proximal M2 segments = within=20 the sylvian fissure (9,57). Yasargil et al.(67) performed the = first=20 successful microvascular STA in 1967. Subsequent studies show that = the=20 procedure had high long-term patency rates and low perioperative = morbidity=20 and mortality rates (6,7,9,11,15,44,45,58). Two of these studies=20 documented improved regional CBF and anecdotal improvement in = clinical=20 symptoms and decreased risk for risk for future stroke (59,68). = These=20 series also revealed patency rates ranging from 87% to 100%; = mortality=20 rates of 0% to 4.4%; and low morbidity rates for strokes (2.7%), = TIAs=20 (7.3%), seizures (5.4%), hemorrhages (4%), and wound infection = (1%)=20 (6,7,9,11,15,44,45,59,68). However, these series lacked a matched = control=20 population treated with medical therapy and followed various = methods of=20 patient selection and evaluation criteria. In an attempt to = clarify this=20 issue, the International Cooperative Extracranial-lntracranial = bypass=20 study was begun in 1977 and completed in 1985 (1). This study = failed to=20 show a benefit of surgical bypass over medical management with = aspirin in=20 reducing the risk for fatal or nonfatal strokes, and it resulted = in=20 further questions regarding patient selection. The study was = criticized=20 for the large number of patients who underwent surgery outside of = the=20 study (56), the failure to separate hemodynamic causes of vascular = insufficiency from embolic causes (38), the variability in = obtaining=20 routine preoperative angiograms and CBF studies (38), and the lack = of a=20 trial of medical therapy in many patients before surgical bypass = (38).

Recent analysis since the completion of the EC-IC cooperative = study=20 seems to show that a select group of patients may benefit from = STA-MCA=20 bypass procedures. These patients have CBF and metabolism studies, = such as=20 xenon computed tomography or positron emission tomography scans, = that=20 indicate poor or absent vascular reserve (18,19,26,33,40,47,65), = and they=20 have not responded to medical management with recurrent symptoms = while=20 taking antiplatelet agents or anticoagulation. Generally their = angiograms=20 show poor collateral flow and often an occluded ipsilateral = carotid=20 artery. Two studies have shown that patients with carotid stenosis = or=20 occlusion and impaired hemodynamic reserve have a 12-fold greater = risk for=20 stroke during a 2-year period compared with similar patients with = carotid=20 stenosis or occlusion but without impaired reserve (36% stroke = rate versus=20 4% stroke rate) (63). Other studies confirm a significantly higher = ipsilateral stroke rate for patients with carotid occlusion with=20 compromised hemodynamic reserve (16,25,26,66). Patients with = carotid=20 occlusion and impaired hemodynamic reserve have a 6.4% to 14% = annual=20 ipsilateral stroke rate, whereas patients with severely impaired=20 hemodynamic measurements have a 16.2% to 59.7% annual ipsilateral = stroke=20 rate (25,26,41,63,66,70). By comparison, all symptomatic patients = with=20 carotid occlusion (without CBF measurements) have an annual = ipsilateral=20 stroke rate of 1.6% to 2.8% (25,26,41,63,66,70). Usually no other=20 alternative treatments are available to such patients with = impaired=20 reserve. With careful preoperative evaluation, they are the most = likely to=20 benefit from STA-MCA bypass. Gewirtz et al. (13) reviewed the = Stanford=20 series of 14 patients who did not respond to medical therapy after = a=20 carotid artery occlusion and who had poor hemodynamic reserve = (with=20 paradoxical steal) based on acetazolamide xenon computed = tomographic=20 scans. Thirteen of the patients had no further strokes at a mean = follow-up=20 of 49 months (range, 8-77 months). One patient (7%) experienced a = stroke 2=20 weeks after his STA-MCA procedure when he underwent emergent = coronary=20 artery bypass surgery for unstable angina and became hypotensive = during=20 surgery. Of the nine patients who underwent a second xenon = computed=20 tomographic scan after surgery, eight patients showed improved = hemodynamic=20 reserve after acetazolamide therapy. Other investigators also = found=20 favorable clinical results after STA-MCA bypass in patients with = internal=20 carotid artery occlusion and impaired hemodynamic reserve = (47.62).

Moyamoya Disease

Moyamoya disease is a progressive disease of the internal = carotid=20 artery, MCA, and anterior cerebral artery characterized by = occlusion of=20 these vessels, which show intimal proliferation (2,17,36,64). = Children=20 with this disease usually have strokes, whereas adults have = ischemic=20 symptoms or intracranial hemorrhage. The natural history of = untreated=20 moyamoya disease is poor, with a 73% rate of major deficit or = death more=20 than 2 years after diagnosis in children (36) and a similarly poor = prognosis in adults (24,43). The first STA-MCA bypass for moyamoya = disease=20 was performed by Yasargil and Yonekawa in 1972 (68), and since = then=20 several small series have been reported. Karasawa et al. described = 12=20 patients with moyamoya disease who underwent bypass, with 10 = patients=20 (83%) having good to excellent results (24). Quest and Correll = reported a=20 similar outcome in 11 of 13 patients (85%) (43). Ishikawa et al. = (22)=20 compared STA-MCA bypass (48 procedures) with indirect = revascularization=20 methods (16 procedures), such as = encephalo-duro-arterio-myosynangiosis, in=20 pediatric patients with moyamoya disease and found that the = incidence of=20 postoperative ischemic events was significantly decreased in the = direct=20 bypass group (10%) compared with the indirect group (56%; p = <0.01).=20 They concluded that direct revascularization is the procedure of = choice=20 over indirect revascularization whenever possible. Matsushima et = al. (31)=20 found a similar advantage of direct revascularization compared = with=20 indirect methods, although with a smaller group of patients. At = Stanford,=20 since 1991 we have performed 59 (as of June 2000) STA-MCA = grafts=20 in patients with moyamoya disease (ages 5 to 63; Fig. = 4) with=20 excellent overall clinical results (5,14,55). Six patients had = temporary=20 minor worsening after operation that resolved with volume = expansion, and=20 one patient had a postoperative hemorrhage into a previously = ischemic=20 region. The mean follow-up was 43 months, ranging from 1 month to = 7 years,=20 and 95% of patients were neurologically stable or improved. = Persistent=20 TIAs developed in one patient after occlusion of a STA-MCA bypass = with=20 short vein interposition. Follow-up angiography showed that 97% of = grafts=20 were patent, and hemodynamic reserve was shown to be improved on = CBF=20 studies in most patients. There were no perioperative deaths, but = one=20 adult died of a myocardial infarction 72 months after bypass, and = another=20 adult died 18 months after an external carotid to MCA bypass using = a vein=20 interposition (from hemorrhage into ischemic brain). Of 12 = children with=20 moyamoya disease (in 19 hemispheres) treated with STA-MCA bypasses = (8=20 after strokes and in 5 with refractory TIAs), none have = experienced new=20 strokes (mean follow-up, 35 months; range, 12-65 months) (14).=20 Postoperative angiograms show successful revascularization of the = MCA=20 distribution in 89% of the cases, and postoperative xenon computed = tomographic scans showed increased augmentation with acetazolamide = compared with the results of the preoperative study (14).

PREOPERATIVE RADIOGRAPHIC EVALUATION

Bilateral carotid angiograms are performed to evaluate donor = and=20 recipient vessels and collateral circulation. The size and = location of=20 optimal vessels to be used for the anastomosis are identified. A = balloon=20 test occlusion can be performed to determine the tolerance of = particular=20 vessels if planned occlusion is required. Patient who have poor = results of=20 this test need prophylactic revascularization. Xenon computed = tomographic=20 CBF studies (Figs. 1, = 2, = 3) = or=20 provocative induced hypotension during test occlusion may provide=20 additional information regarding tolerance to occlusion = (50,54,69).=20 Intraoperative electroencephalography, microvascular Doppler = studies, and=20 somatosensory evoked potentials are useful adjuncts. Postoperative = bypass=20 patency is usually evaluated with conventional cerebral = angiography. but=20 recent studies show that the results of magnetic resonance = angiography=20 correlate reasonably well with those of conventional angiography=20 (27,28,42)

OPERATIVE TECHNIQUE

General Principles

Several operative generalities are applicable to STA-MCA=20 revascularization procedures. The patient is positioned with his = or her=20 head above the heart to reduce venous cerebral congestion. Doppler = ultrasound is used to identify the location of donor vessels.=20 Hyperventilation and a-adrenergic agents=20 are not recommended because of their vasoconstrictive effects, but = mild=20 hypothermia (33=B0C) and barbiturates are used routinely to = provide a=20 cerebral protective effect during arterial occlusion. = Vasoconstrictive=20 agents such as epinephrine should not be used during scalp = infiltration.=20 Intraoperative monitoring with electroencephalography and evoked=20 potentials provide early detection of ischemic changes.

Microinstruments and the operating neurosurgical microscope are = used=20 routinely for revascularization procedures. Donor vessels should = be=20 selected with a diameter =B31 = mm because=20 smaller vessels have higher occlusion rates, provide less blood = flow, and=20 are more difficult to anastomose. Short vein interposition grafts = between=20 the proximal STA and MCA branches may be used when the distal MCA = is too=20 small or not available. Papaverine is useful in preventing = vascular=20 spasm.

If a short venous interposition graft is needed, the saphenous = vein is=20 the vessel of choice. It is harvested adjacent to the ankle, side = branches=20 are carefully ligated, and care is taken to avoid any laceration = to the=20 vein itself. The vein is irrigated with heparinized saline and = inspected=20 for any lacerations that would require surgical repair before use. = The=20 vein is stored in heparinized saline until it is needed. Sometimes = the=20 superficial temporal vein can be used for a short interposition = graft if=20 its diameter is sufficiently large.

Hemodynamic control is the primary goal of postoperative = management.=20 Hypertension may result in excessive bleeding at the anastomotic = site.=20 Intraparenchymal hemorrhages, from increased perfusion of the = brain, and a=20 possible leak in the anastomotic site are other complications. = Conversely,=20 hypotension may cause graft occlusion, resulting in clinical = ischemia. In=20 such cases, an emergent angiogram and graft revision may be = necessary.=20 Prophylactic anticoagulants may be started on the first = postoperative day,=20 although aspirin is usually adequate. A cerebrospinal fluid leak = is a=20 potential complication, particularly when vein grafts are used, = because of=20 the deliberately loose dural closure, which prevents excessive = pressure on=20 the donor vessel.

Operative Technique for = Superficial=20 Temporal Artery to Middle Cerebral Artery Bypass With or Without = Short=20 Vein Graft

The patient is positioned with the head turned to the = contralateral=20 side and the temporal bone parallel to the floor, and the = patient's head=20 is fixed in a three-point Mayfield headrest. After the hair is = shaved from=20 the scalp, a Doppler ultrasound is used to mark out the course of = the STA=20 and its branches (Fig. = 8).=20 After local infiltration of the scalp, an incision is made with a = #15=20 blade and the superficial temporal artery is identified and = harvested with=20 a generous cuff of soft tissue surrounding the artery (Fig. = 9).=20 Either the frontal or parietal STA branch may be used, depending = on=20 diameter size and suitable length. Smaller branches of the artery = are=20 isolated and carefully coagulated to prevent injury to the STA or = they are=20 tied off. The length of the artery required depends on the = distance from=20 the artery to the graft site and on whether a short vein segment = will be=20 used. A craniotomy is performed in the midfrontal-temporal bone = overlying=20 the sylvian fissure (Fig. = 10).=20 The dura is opened and recipient vessels are identified. Optimal = recipient=20 vessels have outer luminal diameters =B31=20 mm. A microvac subdural drain is placed to remove cerebrospinal = fluid=20 during operation.

The recipient MCA/branch (usually the M3 or M4 branch emerging = from the=20 sylvian fissure) is chosen (Fig. = 11)=20 based on diameter, location (the angular MCA branch is the optimal = recipient), and orientation (perpendicular to the surgeon if = possible).=20 Dissection of the arachnoid layer over a 6- to 10-mm segment = exposes this=20 vessel, and tiny branches are coagulated and divided if necessary. = A=20 high-visibility background is placed to facilitate anastomosis (Fig. = 12). A=20 temporary aneurysm clip is placed on the proximal STA donor, and = the=20 distal STA is ligated and divided at the proper length. The = temporary clip=20 is opened briefly to verify good flow through the STA. Then the = STA is=20 flushed with heparinized saline and the distal tip of this vessel = is=20 stripped of all fascial tissue and cut in an oblique manner (Fig. = 13).=20 Microvascular clips (Fig. = 14) or=20 temporary aneurysm clips (Fig. = 15)=20 are placed on each side of the recipient vessel to prevent = bleeding. An=20 arteriotomy is performed by cutting an elliptical or = diamond-shaped=20 portion of the superior wall of the recipient vessel. The = recipient branch=20 is irrigated with heparinized saline. Indigo carmine blue dye can = be used=20 to stain the edges of the MCA vessel, thereby facilitating = suturing.=20 Anastomosis is performed under the neuromicroscope using 10-0 = interrupted=20 monofilament suture (or alternatively, running 10-0 monofilament = suture)=20 (Fig.=20 16). Corner stitches are placed first, followed by stitches at = the far=20 wall, and finally those at the near wall. The intimal layer must = be=20 included with each interrupted stitch, but significant narrowing = of the=20 anastomotic site should be avoided. Temporary clips are removed.=20 Significant bleeding may indicate the need for an additional = stitch,=20 whereas small amounts of bleeding may be treated with Gelfoam or = Surgicel.=20 If the donor vessel is a short vein segment, a proximal = anastomosis to the=20 STA is performed first using 10-0 or 9-0 monofilament suture. The = vein=20 must be of an appropriate length to avoid any kinks in the vein. = An=20 arteriotomy is made in the superficial temporal artery, and 10-0=20 monofilament sutures are used to anchor the corner stitches, = followed by=20 stitches at the back and the front walls. Once the anastomosis is = complete=20 (Figs. 17, 18, 19), a=20 Doppler ultrasound may be used to test patency. We have found a=20 quantitative and directional Doppler useful in the measurement of = flow=20 through the MCA segment and the STA before anastomosis, and in the = STA and=20 proximal and distal MCA segments after bypass. The dura is then = closed=20 loosely around the STA graft and the bone is trimmed to avoid any=20 compromise of the STA. The galeal layer and skin are closed, with = care=20 taken to avoid graft compromise.

POSTOPERATIVE ISSUES

Patency, Morbidity, and Mortality Rates

Many large series of STA to MCA bypass grafts are reviewed in = the=20 literature. They reveal patency rates ranging from 87% to 100%, = mortality=20 rates of 0 to 4.4%, and morbidity rates for strokes (2.7% ), TIAs = (7.3% ),=20 seizures (5.4%), hemorrhages (4%), and wound infection (1%)=20 (6,7,9,11,15,44,45,59,68). The EC-IC study noted a patency rate of = 96% and=20 a mortality rate of 0.6%.

Long- Term Effects of Revascularization

Several authors have examined the long-term effects of STA-MCA = bypass=20 on cerebral circulation. Tsuda et al. (60) showed (using SPECT = studies)=20 improved cortical regional CBF and cognition 3 years after the = bypass.=20 Similarly, positron emission tomography scans have shown increases = in=20 regional CBF and decreases in oxygen extraction fraction after=20 revascularization (32,35).

Complications

There are several potential complications of STA-MCA bypass = procedures.=20 Ischemic changes usually result from either compression of the = donor=20 vessel by the scalp closure, graft occlusion or stenosis at the=20 anastomosis site, or emboli. Doppler and angiography studies = generally=20 identify the cause. As discussed above, hypertension may result in = anastomosis leak or parenchymal hemorrhage, and increased = perfusion may=20 cause cerebral edema and disautoregulation. In addition, because a = loose=20 dural closure is necessary to avoid any compression of the donor = vessel,=20 cerebrospinal fluid leak, pseudomeningocele, and subdural hygromas = are=20 possible, although rare. Scalp ischemia, although a theoretical = risk, is=20 extremely unusual. Finally, as with other craniotomies, systemic = surgical=20 complications include myocardial infarction, pneumonia, deep = venous=20 thrombosis, and pulmonary emboli.

CONCLUSIONS

Extracranial-to-intracranial (STA-MCA) revascularization = procedures=20 have proved useful in selected patients with cerebral ischemia. = Judicious=20 preoperative evaluation coupled with attentive intraoperative = techniques=20 and postoperative management have minimized morbidity and = mortality rates=20 while improving patient outcome. Improvements in our understanding = of the=20 indications for such procedures should further refine the patient=20 population that will benefit from these revascularization = procedures.

FIG.=20 1

3D"Figure

A 43-year-old man had expressive = aphasia and=20 mild right hemiparesis as a result of persistent left = hemisphere=20 TIAs despite therapeutic warfarin sodium and low molecular = weight=20 heparin. (A) A preoperative magnetic = resonance=20 image showed watershed infarct in the left centrum semiovale = deep=20 white matter (arrows). Pretreatment xenon computed = tomographic=20 imaging (B) before and (C) = after=20 acetazolamide administration revealed impaired hemodynamic = reserve=20 with paradoxical steal in the left frontoparietal region = (arrows).=20 The right hemisphere showed normal augmentation of cerebral = blood=20 flow after acetazolamide. A left common carotid cerebral = angiogram=20 showed occlusion of the AI anterior cerebral and MI middle = cerebral=20 arteries (straight arrow), seen in the (D)=20 anteroposterior and (E) lateral views. The = parietal=20 branch of the left superficial temporal artery = (E,=20 curved arrow) was later used as the donor vessel for = superficial=20 temporal artery to middle cerebral artery (STA-MCA) bypass.=20 (F) A right anteroposterior internal = carotid artery=20 cerebral angiogram revealed absence of aright A1 anterior = cerebral=20 artery and no filling of the contralateral left middle = cerebral=20 artery territory. No posterior communicating arteries were=20 visualized on carotid or vertebrobasilar injections. The = patient=20 underwent a left STA-MCA bypass with subsequent resolution = of his=20 TIAs. (G) A postoperative anteroposterior = and=20 (H) lateral left external carotid cerebral=20 angiogram (7 weeks after surgery) showed marked enlargement = of the=20 STA (arrow) with excellent filling of the middle cerebral = and=20 anterior cerebral artery territories from the STA graft. A=20 postoperative xenon CT scan (also 7 weeks after surgery)=20 (I) before and (J) after=20 acetazolamide challenge showed improved hemodynamic reserve = in the=20 left frontoparietal regions (arrows). After operation, the = patient=20 has had no further TIAs or strokes while taking aspirin = during the=20 last 5 years.

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FIG.=20 2

3D"Figure

A 61-year-old man had acute left = hemiparesis=20 and a single TIA consisting of right arm weakness.=20 (A) A T2 axial magnetic resonance image of = his head=20 shows multiple right hemisphere white matter infarcts = (arrows) and a=20 left parietal infarct (arrowhead). (B) A = magnetic=20 resonance angiogram of the patient's neck revealed bilateral = internal carotid artery occlusions (arrows). A xenon = computed=20 tomographic scan was performed and showed = (C) poor=20 baseline cerebral blood flow bilaterally and = (D)=20 minimal augmentation after the administration of = acetazolamide. A=20 cerebral angiogram performed with a right common carotid = artery=20 injection showed primarily external carotid vessels in the=20 (E) anteroposterior and = (F)=20 lateral views. The right supraclinoid carotid artery (arrow, = F) fills slightly via the right ophthalmic = artery=20 (arrowhead, F). A left common carotid = artery=20 angiogram shows filling of the external carotid branches = only, seen=20 on (G) anteroposterior and = (H)=20 lateral views (the arrow shows the superficial temporal = artery [STA]=20 on the lateral view). The patient underwent aright = superficial=20 temporal artery to middle cerebral artery (STA-MCA) bypass=20 procedure, followed 6 weeks later by a left STA-MCA bypass. =

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FIG.=20 3

3D"Figure

Same patient as in Figure=20 2. Three weeks after the second bypass, a right external = carotid=20 angiogram showed excellent filling of the MCA distribution = in the=20 (A) anteroposterior and = (B)=20 lateral views. The anastomosis site (arrow, = A and=20 B) can be seen in both views, as can = retrograde=20 flow down the proximal MCA (arrowhead, A). = A left=20 external carotid angiogram showed excellent filling of the = left MCA=20 in the (C) anteroposterior and = (D)=20 lateral views with the anastomosis site visible (arrow.=20 D). The patient's left hemiparesis resolved = over 2=20 months with rehabilitation and he was neurologically normal. = He has=20 had no further TIAs.

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FIG.=20 4

3D"Figure

A 35-year-old woman had right = hemiparesis=20 and expressive aphasia after a left cerebral stroke. = Evaluation=20 revealed bilateral moyamoya disease. (A) A=20 pretreatment T2 MRI axial image shows watershed distribution = infarcts in the left hemisphere. A left common carotid = cerebral=20 angiogram revealed poor filling above the supraclinoid = internal=20 carotid artery (arrow) in the (B) = anteroposterior=20 and (C) lateral views. She underwent a = right=20 superficial temporal artery to middle cerebral artery = (STA-MCA)=20 bypass, followed 1 week later by a left STA-MCA bypass.=20 Post-treatment angiography showed excellent filling of the = MCA=20 vessels bilaterally from the STA-MCA grafts. A left common = carotid=20 cerebral angiogram shows the STA-MCA anastomosis site (solid = arrow)=20 in both the (D) anteroposterior and=20 (E) lateral views. Retrograde filling down = the MCA=20 to the Al-Ml junction (D, arrowhead) was = evident,=20 as was filling of the bilateral A2 anterior cerebral = arteries from=20 the graft. The patient has had no further ischemic symptoms = and mild=20 improvement in her aphasia 1 year after surgery.=20

Ba= ck=20 to Moyamoya=20 Disease

FIG.=20 8

3D"Figure

A typical skin incision. The main incision is = planned over=20 the superficial temporal artery (STA), with a T extension to = allow=20 exposure of the bone.