Moyamoya disease is a progressive occlusive vasculopathy that involves the supraclinoid internal carotid arteries and Circle of Willis, and results in the formation of collateral vessels at the skull base. The progressive nature of this disease leads to cerebral ischemia and sometimes intracerebral hemorrhage. The treatment of moyamoya disease is mainly surgical revascularization, using revascularization techniques that include direct, indirect, and combined strategies. Here we discuss the available options for revascularization as well as our opinions regarding the surgical management of patients with moyamoya disease.
Key points
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Surgical revascularization is the main therapy for moyamoya disease, as it prevents risk of future stroke.
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Surgical options can be divided into indirect, direct, or combined approaches.
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In general, a direct bypass is performed in patients with occlusive disease (occlusion of internal carotid artery [ICA] or middle cerebral artery [MCA]).
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In general, an indirect bypass is reserved for patients with stenosis and not occlusion of the ICA or MCA, and in cases when the donor or recipient arteries are too small.
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Competing flows after a direct bypass may cause stagnation in the existing collateral supply or occasionally accelerate occlusion of an already stenosed native circulation.
Introduction
In 1957, Takeuchi and Shimizu first described a progressive occlusive vasculopathy that involves the supraclinoid internal carotid arteries and Circle of Willis and results in the formation of arterial collaterals at the skull base. In 1969, Suzuki and Takaku termed this network of collateral formation seen on angiography as “moyamoya,” meaning “puff of smoke” in Japanese.
Moyamoya disease is now widely accepted as a disease process that not only affects patients of Asian descent, but is also prevalent in North America and Europe. Familial cases account for approximately 15% of the disease. In 2012, Starke and colleagues analyzed the moyamoya patients admitted to US hospitals from 2002 to 2008 using the National Inpatient Sample. A total of 2280 patients were admitted with a diagnosis of moyamoya disorder, which translated to an incidence of 0.57 per 100,000 persons per year. This was considerably higher than the incidence of 0.086 per 100,000 persons per year in Washington State and California from 1987 to 1998.
In Japan, a recent analysis of patients with moyamoya disease admitted in 2003 yielded an annual rate of 0.54 per 100,000, which was close to the findings of Starke and colleagues in North America. The prevalence of moyamoya disease in Japan nearly doubled with almost a 100% increase from 3900 patients in 1994 to 7700 cases in 2003. It is, however, difficult to determine if this increase in prevalence represents increased awareness and improved diagnostic measures or an actual increase in disease incidence.
The pathophysiology of moyamoya disease remains unclear. Pathologic specimens have shown that the outer diameters of the carotid artery are diminutive with increased intimal thickening. Caspase-3–dependent apoptosis has been implicated as a possible contributor to the pathophysiology of moyamoya disease. Fibrin deposition along with the elastic laminae abnormalities and microaneurysm formation within the dilated moyamoya vessels may contribute to intracranial hemorrhage in these patients. Conversely, stenosed moyamoya vessels can lead to thrombosis and subsequent brain ischemia. Children in Asian populations tend to present with brain ischemia due to inadequate moyamoya collateral formation and nearly 50% of adults present with intracerebral hemorrhage due to the fragility of the collateral vessels that have formed over time. Outside of Asia, moyamoya disease may have different phenotypical considerations. In the North American cohort, only 14.6% of adults and 2.1% of children presented with hemorrhage, and of 902 patients at Stanford with moyamoya disease, 16% of adults and 6% of pediatric patients presented with hemorrhage.
Introduction
In 1957, Takeuchi and Shimizu first described a progressive occlusive vasculopathy that involves the supraclinoid internal carotid arteries and Circle of Willis and results in the formation of arterial collaterals at the skull base. In 1969, Suzuki and Takaku termed this network of collateral formation seen on angiography as “moyamoya,” meaning “puff of smoke” in Japanese.
Moyamoya disease is now widely accepted as a disease process that not only affects patients of Asian descent, but is also prevalent in North America and Europe. Familial cases account for approximately 15% of the disease. In 2012, Starke and colleagues analyzed the moyamoya patients admitted to US hospitals from 2002 to 2008 using the National Inpatient Sample. A total of 2280 patients were admitted with a diagnosis of moyamoya disorder, which translated to an incidence of 0.57 per 100,000 persons per year. This was considerably higher than the incidence of 0.086 per 100,000 persons per year in Washington State and California from 1987 to 1998.
In Japan, a recent analysis of patients with moyamoya disease admitted in 2003 yielded an annual rate of 0.54 per 100,000, which was close to the findings of Starke and colleagues in North America. The prevalence of moyamoya disease in Japan nearly doubled with almost a 100% increase from 3900 patients in 1994 to 7700 cases in 2003. It is, however, difficult to determine if this increase in prevalence represents increased awareness and improved diagnostic measures or an actual increase in disease incidence.
The pathophysiology of moyamoya disease remains unclear. Pathologic specimens have shown that the outer diameters of the carotid artery are diminutive with increased intimal thickening. Caspase-3–dependent apoptosis has been implicated as a possible contributor to the pathophysiology of moyamoya disease. Fibrin deposition along with the elastic laminae abnormalities and microaneurysm formation within the dilated moyamoya vessels may contribute to intracranial hemorrhage in these patients. Conversely, stenosed moyamoya vessels can lead to thrombosis and subsequent brain ischemia. Children in Asian populations tend to present with brain ischemia due to inadequate moyamoya collateral formation and nearly 50% of adults present with intracerebral hemorrhage due to the fragility of the collateral vessels that have formed over time. Outside of Asia, moyamoya disease may have different phenotypical considerations. In the North American cohort, only 14.6% of adults and 2.1% of children presented with hemorrhage, and of 902 patients at Stanford with moyamoya disease, 16% of adults and 6% of pediatric patients presented with hemorrhage.
Patient evaluation overview
At Stanford, all patients obtain an MRI brain, MR perfusion with and without Diamox, 6-vessel angiogram, neuropsychiatric testing, and surgical clearance from the anesthesia team before surgery. In patients with bilateral moyamoya disease, the more symptomatic hemisphere is treated first. The contralateral hemisphere is usually treated 1 week later, assuming the first surgery was uneventful. Initial surgical laterality is dependent on the patient’s clinical symptomatology with associated MRI findings of infarcts and/or poor cerebral blood flow augmentation after administration of acetazolamide (Diamox). A more ominous finding after Diamox administration is a steal phenomenon in which a paradoxic decrease in regional blood flow occurs likely related to maximal arterial dilation in some regions at baseline. We believe these patients are at highest risk for future strokes and require strict blood pressure management in the perioperative period. A contraindication to planned surgery is the presence of an acute (DWI +/ADC+ [Diffusion weighted imaging (DWI); apparent diffusion coefficient (ADC)]) or subacute (DWI+/ADC−) infarct, even a very small one.
Nonsurgical treatment options
Nonsurgical medical therapy using aspirin, mannitol, steroids, and vasodilators have been largely unsuccessful. Left untreated, 23.8% to nearly 49.0% of patients have symptomatic progression over 6 years. In a 2007 Japanese multicenter survey, outcomes in asymptomatic patients with untreated moyamoya disease showed a 3.2% annual risk for any stroke. A similar study conducted in North America demonstrated an annual ischemic stroke rate of 13.3% and a hemorrhage rate of 1.7%. Other approaches include intravenous infusion of calcium channel blockers, such as nimodipine or verapamil, which have provided symptomatic improvement in patients with moyamoya disease. Their efficacy, however, has not yet been proven.
Endovascular therapy has also been attempted to help reestablish immediate blood flow to the oxygen-deprived brain. Khan and colleagues reviewed the results of angioplasty and stenting on 5 adult patients, all of whom went on to develop repeated ischemic attacks despite treatment ( Fig. 1 ). Although cerebral blood flow may have improved in the short term, 70% to 90% in stent stenosis in 4 patients and occlusion in 1 patient on follow-up angiograms proved this method of treatment was not sustainable. All patients went on to receive a revascularization procedure.
Surgical treatment options
Medical therapy as the sole treatment modality has been largely supplanted by surgical revascularization procedures due to the ongoing risk of cerebral ischemia or hemorrhage.
In general, cerebral revascularization surgery can be divided into 3 categories:
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Direct revascularization
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Indirect revascularization using adjacent or distant vascularized tissue
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Combined techniques (direct plus indirect)
Direct Bypass Technique
Superficial temporal artery to middle cerebral artery (STA-MCA) bypass has been used since 1973 by Kikuchi and Karasawa and remains the procedure of choice when direct revascularization is desired. Direct revascularization has the added benefit of immediately augmenting blood flow to the oxygen-deprived brain by suturing an extracranial artery directly to cortical branches on the brain surface.
At Stanford, we make an attempt to perform direct bypasses on all patients who are symptomatic with occlusion of the internal carotid artery (ICA) or MCA. Because we harvest a generous cuff of vascularized soft tissue surrounding a long segment of scalp artery and then place this in intimate contact with the brain surface in addition to the direct anastomosis, indirect revascularization also occurs over the next 3 to 6 months. All procedures are done under mild hypothermia to target a core temperature of 33°C for neuroprotection. Monitoring of intraoperative electroencephalogram is an important adjunct to surgery, particularly during clamping of the recipient vessel and when confirmation of burst suppression is used before performing the anastomosis.
Both the frontal or parietal branch of the STA can be used for anastomosis and preoperative angiogram aids in choosing the appropriate donor vessel. In general, the parietal branch is used when the vessel diameter is adequate. Too large of a parietal branch is also not desirable, as flow from the donor vessel that is too robust can lead to competing blood flow with the native collateral circulation and promote ischemia, or in rare cases cerebral hyperperfusion. The natural course of the parietal branch also facilitates a craniotomy over the frontotemporal region to better expose M4 vessels emerging from the Sylvian fissure.
The patient is positioned supine with the head turned away from the surgical side and fixated in a Mayfield head holder. Typically, a shoulder roll is placed to prevent excessive neck turning that can result in decreased venous outflow and is particularly important in patients with Down syndrome who may be predisposed to craniocervical instability. The STA branch of interest is then insonated using a handheld Doppler to map the course of the donor vessel ( Fig. 2 ). We typically begin mapping the STA above the zygomatic arch. If the parietal branch is chosen, the frontal branch is preserved should another revascularization procedure be needed in the future.
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Usually a curvilinear incision is planned over the STA. Under high magnification, the initial dissection begins at the proximal STA. The dissection is carried out superficially through the dermis and subcutaneous tissue using Littler scissors. Hemostasis in the dermis can be controlled using low current bipolar electrocautery.
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Small hook retractors are used to facilitate exposure as the dissection is carried toward the convexity. Throughout the dissection, patency of the STA is periodically monitored using the handheld Doppler. Papaverine can be used to prevent STA spasm during dissection. We aim to dissect out approximately 9 cm of STA before creating a vascular cuff that will serve as a means for additional indirect collaterals on the brain surface.
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After the STA has been isolated from the underlying temporalis fascia, self-retaining retractors are placed to prepare for the craniotomy. The temporalis fascia and muscle are then incised in an H-shaped fashion using monopolar electrocautery and carefully lifted off the skull. The assistant surgeon helps protect the STA during muscle dissection and craniotomy to avoid iatrogenic injury to the donor vessel.
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A 6 × 6 cm craniotomy is then created over the frontotemporal region with a burr hole strategically placed at the most inferior aspect to serve as a conduit for STA passage into the intracranial space.
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A short segment (∼0.5 cm) of the proximal STA just distal to the origin of the frontal branch is prepared by removing all adherent soft tissue to accommodate placement of a temporary clip. Next, 1 cm of the most distal part of the STA is then prepared in a similar fashion using fine micro scissors.
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The dura is then opened in a stellate fashion and tacked up. Under high magnification, the arachnoid is opened to identify an appropriate recipient artery. We aim to find an M4 artery emerging from the Sylvian fissure that is preferentially ≥0.8 mm and also perpendicular to the Sylvian fissure, if possible ( Fig. 3 ).
Fig. 3
Intraoperative STA-MCA bypass. ( A ) The STA should be at least 0.8 mm in diameter to achieve an adequate anastomosis. ( B ) After wide opening of the arachnoid, a recipient M4 branch is chosen and used as the recipient vessel. ( C ) Using low profile Lazic (Peter Lazic GmbH, Tuttlingen, Germany) 3-mm temporary clips, the M4 vessel is temporarily occluded. ( D ) An elliptical arteriotomy is made in the recipient vessel. Methylene blue or indigo carmine dye is then applied to the M4 vessel to improve visualization. The toe of the fishmouthed STA is sutured first using 10 to 0 Monosof (Convidien, Mansfield, MA) suture. ( E ) The heel of the STA is then sutured. ( F ) The side walls are sutured using 10 to 0 Monosof sutures, ensuring not to catch the back wall of the recipient vessel. ( G ) Once the anastomosis is completed, the STA and its vascular cuff are placed onto the cortical surface. ( H ) ICG video angiography is used to confirm patency of the anastomosis.
( From Gooderham P, Steinberg GK. Intracranial-Extracranial Bypass surgery for Moyamoya Disease. In: Spetzler M, Kalani Y, Nakaji P , editors. Neurovascular Surgery 2nd Edition. New York: Thieme; 2015(95). p. 1156–71. with permission.)
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Once isolated from the underlying cortex, blood flow is measured in the cortical MCA branch and cut STA using an ultrasonic quantitative and directional flow probe (Charbel microflow probe; Transonics Systems, Inc, Ithaca, NY). A high-visibility background is then placed beneath the recipient artery.
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A 45° cut is made at the distal STA and flushed with heparinized saline while the proximal STA is temporarily clipped. Before temporary clipping of the recipient artery, burst suppression is achieved along with a mean arterial pressure of 90 to 100 mm Hg.
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Lazic temporary clips (Peter Lazic GmbH, Tuttlingen, Germany) are then applied on the recipient artery proximal and distal to the planned anastomosis.
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An elliptical arteriotomy is made on the cortical vessel and stained with methylene blue or indigo carmine. An end-to-side microanastomosis is then completed with the use of Monosof suture (10–0) (Covidien, Dublin, Ireland). We prefer an interrupted suture technique, starting with the initial toe stitch followed by a heel stitch. Stitches are placed evenly apart (usually 3 on each side in addition to the 2 end stitches), ensuring not to catch the back wall of the recipient artery with each suture. Once the anastomosis is complete, the temporary clips are first removed from the recipient artery followed by the proximal STA.
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Using the Charbel microflow probe, the quantitative blood flow and its directionality in relation to the Sylvian fissure is measured in the recipient artery both proximal and distal to the anastomosis. A final measurement of the distal STA blood flow after the bypass is also recorded. Finally, the patency of the bypass is confirmed using intraoperative indocyanine green (ICG) video angiography.
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For closure, the dural leaflets are reapproximated loosely, ensuring not to compromise the parent STA. The bone flap is replaced with the inferior burr hole serving as an unobstructed passageway for the STA to enter the intracranial space. Doppler ultrasound is recommended throughout the closure to make certain no flow-limiting stenosis/occlusion of the STA has occurred during final closure.
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