Moyamoya Disease, Basic Concepts of Diagnostics, and Treatment
Moyamoya disease (MMD) is a rare condition where the supraclinoid part of internal carotid artery is slowly and progressively becoming stenotic, and also it often involves both middle cerebral arteries and anterior cerebral arteries (Fig. 26.1) . The term moyamoya means a puff of smoke in Japanese, and it was first reported by Takeuchi and Shimizu in 1957 with Japanese language .
Its etiology still remains unknown. The moyamoya syndrome (MMS) has similar clinical and angiographic characteristics to MMD but might be associated with Down’s syndrome, neurofibromatosis type 1 (NF-1), prior irradiation, and sickle-cell disease.
Although MMD was initially found in Asian patients, it has been increasingly reported in patients of all demographic groups; the exact incidence is not completely known .
Japanese studies report an annual incidence between 0.35 and 0.94/100,000 persons per year and annual prevalence between 3.16 and 10.5 per 100,000 persons [4, 5, 6]. Female has twice the number compare with male [4, 5].
26.2 Signs and Symptoms
There is a classification that is supported by the Ministry of Health and Welfare of Japan, which classified the moyamoya diseases (MMD) based on its presentation in to four: ischemic, hemorrhagic, epileptic, and “other.” In children, it is more common to see the ischemic type, while in the adult it is more common to see they present with hemorrhage. It is reported that the hemorrhage presentation of MMD is approximately seven times higher in adult patients (14.6%) if we compare with the pediatric group (2.1%) . Occasionally patients may also present with seizure, headaches, or behavioral changes. Some studies suggest a relation between headaches and hypoperfusion leading to cortical depression and associated migraine symptoms . Others have suggested that dilation of dural and meningeal vessels irritate the pain fibers on the dura, resulting in a migraine-like headache that is refractive to medical therapies . This headache initially persisted in 63% of patients even after cerebral revascularization, although it would often improve over time. Based on angiographic studies, the typical course of disease can be classified into six stages. The first description was written by Suzuki and Takaku (1969). They describe it in six stages. Stage I: on the early stage, it is started with the narrowing of carotid bifurcation at the neck and also the ICA bifurcation. Stage II: it is also called moyamoya initiation, which is characterized by dilated ACA, MCA, and further narrowing of ICA bifurcation. Stage III: this stage is called moyamoya intensification; the ICA bifurcation is much narrower, and ACA and MCA now become narrow as well. Stage IV: this stage is called moyamoya minimization; the occlusive changes in ICA and tenuous ACA and MCA happened slowly. Stage V: This stage is called moyamoya reduction; the occlusion of ICA, ACA, and MCA becomes very severe. Stage VI: this stage is called moyamoya disappearance; the ICA is totally occluded, and the brain tries to get supplied from ECA.
26.3 Natural History and Prognosis
The disease inevitably progresses if left untreated. In a patient whose both side vessels are narrowing, the risk of stroke after 5 years is up to 82% . The National Register of all asymptomatic moyamoya in Japan finds that 3.2% of them will get stroke even if they were treated medically . On the other hand, the stroke or death rate prior, during, and after the surgical revascularization is something between 5.5%  and 17%  over 5 years, and this results in demonstrating that the surgery may offer a benefit to the patients.
The diagnoses of MMD or MMS should be considered in any patient, especially in a child or young adult who presents with neurologic deficits or symptoms secondary to cerebral ischemia or hemorrhage. Radiologic evaluation may include CT; MRI; cerebral angiography and cerebral perfusion studies, including CT perfusion, xenon-enhanced CT, or PET; MR perfusion; and SPECT or CT imaging without and with acetazolamide challenge. Cerebral angiography, CT angiography, and MR angiography imaging can reveal intracerebral vascular occlusion along with the resulting moyamoya vessels. CT and MRI can reveal hemorrhage or ischemic changes.
26.5 Approach and Steps of Surgery
Currently we still do not have a good randomized study that compares medical treatment versus surgical revascularization for patients with MMD, but in good hand surgeon, they claim that the stroke rate is significantly reduced in surgically treated group. As discussed in the previous section, the natural history of these patients is to progress, and the risk of recurrent stroke is extremely high with medical management only. The main medical treatment option for these patients is antiplatelet therapy. All patients are on aspirin pre- and postoperatively. Full anticoagulation drugs such as warfarin are rarely used.
One of the obvious indications to recommend surgery for moyamoya patients is multiple episodes of TIA (transient ischemic attack), RIND (reversible ischemic neurological deficit), or even stroke. The purpose of the surgery is to prevent the next episode by reestablishing adequate blood supply to the affected cortex. There are two ways to reestablish the blood supply to the brain. Adult and older children may have direct bypass surgery to revascularize the brain vessels, and the children under 10 years old may have indirect bypass surgery because their vessels are very tiny and tend to fail if we do direct bypass.
26.5.1 Bypass Surgery of the Brain
Bypass surgery of the brain is a revascularization either between extracranial vessel and intracranial vessel or between intracranial vessel and another intracranial vessel by using graft (saphenous vein, radial artery, etc.) The purpose of the bypass is to reestablish another route or reroute blood flow from the narrowed, blocked, or damaged vessel and supply the distal part of the artery. It is very common to just use the natural provided artery such as from the STA (superficial temporal artery) and directly bypass it to the MCA (middle cerebral artery). Just after the bypass, it may show an instant upgrading blood flow to the distal part of the narrowed artery. Certain people may have a very tiny superficial temporal artery, and we might think the size is not big enough to provide long-term support, and then saphenous vein or radial artery may be harvested to make an anastomosis from the extracranial carotid artery to the distal part of the narrowed vessel. The surgeon will look at the angiogram or nowadays the CT angiogram to decide and plan the surgery.
26.5.2 EDAS (Encephaloduroarteriosynangiosis)
EDAS (encephaloduroarteriosynangiosis) surgery is considered as an indirect way of establishing new vascularization in the brain. It is using the superficial temporal artery that was dissected from the surrounding soft tissue and is placed in direct contact with the cortical surface. The artery should not be kinking at its entry point to the cortical surface and at its distal part where it is going back to supply the scalp. Some fine suture should be placed to hold the artery on the cortical surface. The bone flap is repositioned and secured with miniplate and screw, but the entry and exit of the STA have to make sure there is no pressure at all. Over a period, we expect some new vessel forming to supply the brain. It is important to remember that the STA is always kept intact, so it will give branches to the brain.
26.5.3 EMS (Encephalo-Myo-Synangiosis)
EMS (encephalo-myo-synangiosis) surgery is also considered as indirect way of establishing new vascularization by using temporalis muscle as the source of the angiogenesis to the brain. The muscle is gently dissected, and through the opening of the bone at the temporal base, the muscle is laid on top of the cortical surface. It is very important to have a meticulous bleeding control to avoid postoperative blood accumulation, but be careful not to coagulate too much of the temporal muscle because we don’t want to make the muscle de-vascularized. Closing the dura with the muscle underneath it is sometimes challenging, but surgeons need to do the closing meticulously. The muscle is a very good source of blood supply to the brain, and they may spread angiogenesis all over the brain.
26.5.4 EDAMS (Encephalo-Duro-Arterio-Myo-Synangiosis)
EDAMS (encephalo-duro-arterio-myo-synangiosis) surgery is a combination EDAS and EMS at the same time.
26.5.5 Omental Transposition Surgery
Omental transposition surgery is also another option for indirect way to establish revascularization in the brain by using omentum from the abdomen. The omentum is a special fat tissue that surrounds abdominal organs, and it spreads very fast to any part of the abdomen that needs support. It has rich blood supply. When it is placed on the surface of the cerebral cortex, it is expected that it will grow and spread very fast to supply the brain and improve the blood supply.
26.5.6 Multiple Burr Holes
Another option of indirect revascularization of the cortex is by doing multiple burr holes all over the skull and expecting that the scalp vessel will go through the burr hole and provide vascular supply to the cortex.
Patients with MMD although have occlusion of the internal carotid arteries, but usually the external carotid artery is patent. Surgical effort uses the external carotid artery to supply blood to ischemic cortex by either creating a direct or indirect revascularization bypass. A direct bypass usually require adequate superficial temporal artery (STA) at the ipsilateral side and then anastomosed directly to a distal M4 segment of middle cerebral artery (MCA). The indirect revascularization is performed by using a vascularized tissue that is also supplied by external carotid artery, including the dura, temporalis muscle, the STA itself, and even pericranium. The vascularized tissue is laid on the cortical surface and expect the new blood vessel will be formed and ingrowth toward the cortex. There is no good randomized study that compares the direct and indirect revascularization in terms of their safety and efficacy. The literature review also failed to reveal a difference in surgical morbidity or stroke rate (perioperative or long term) between the direct and indirect methods. Many institutions will perform direct revascularization for adults and indirect revascularization for children because of the smaller and more friable caliber of the vessels in children. However, there are many groups that perform indirect bypass for adult patients as well [15, 16]. According to Gordon Li et al., they recommend to perform direct bypass on all patients whenever possible, unless the STA or MCA is too small or friable. Direct revascularization surgery may provide an immediate increase in cortical blood flow and treat the ischemic cortex immediately. In the case with bilateral MMD, it is obvious to treat the symptomatic side first. If they are both asymptomatic, it is better to treat and revascularize the non-dominant hemisphere first because of higher incidence of transient neurologic symptoms following the surgery on dominant cortex. The second surgery for the contralateral side is generally 1–4 weeks after the first surgery, unless there were significant complications after the first procedure.
26.5.7 Direct Revascularization
Prior to the surgery, it is important to assess the size of frontal and parietal branch of STA by using CT angiography or conventional angiography. The larger diameter branch is chosen as the donor vessel. The patient is positioned supine and the head is hold with head holder. The head is elevated above the heart and turned to the side, bringing the frontotemporal region uppermost in the field. Stimulating and recording electrodes are placed for monitoring of bilateral somatosensory evoked potentials (SSEP) and bilateral EEG. Cooling to approximately 33 °C is accomplished by either using cooling blanket and bladder irrigation or by putting IV catheter (InnerCool Therapies Philips, Andover, MA) into the inferior vena cava. In general, the InnerCool catheter is placed in the larger patients who are more difficult to cool and rewarm via surface techniques.
26.5.8 Indirect Revascularization
If the patient has a very small STA (<0.6 mm) or the vessel is too fragile for suture, then we perform an indirect revascularization (encephaloduroarteriosynangiosis (EDAS) or encephaloduromyosynangiosis (EDMS)). We have abandoned options such as free omental flap transplantation or pedicle omental flap transposition. In a similar fashion to the direct bypass procedure, patients are positioned and prepped, the STA and generous soft tissue cuff are harvested, and the craniotomy is performed. The arachnoid overlying the deep sulci and fissures is microscopically opened, and the STA with the cuff of soft tissue is laid directly on the pial surface of the cortex. The closure should be meticulously done to avoid postoperative bleeding.
26.6 Expert Opinion
Although there are risks to direct and indirect revascularization procedures for MMD, according to data by several authors, they suggest that surgery is superior to medical management of these patients.
26.7 Things to Be Observed and Postoperative Care/Follow-Up
Patients are generally discharged after three to four hospital nights (the first night is spent in the intensive care unit). They are then evaluated clinically 1 week after each surgery and subsequently at 6 months, then 3 years, and finally at 10 years. It is important to perform MRI, SPECT, or Xenon CT and cerebral angiography at 6 months, 3 years, and 10 years.
- 1.Fukui M. Guidelines for the diagnosis and treatment of spontaneous occlusion of the Circle of Willis (“Moyamoya” disease). Research Committee on Spontaneous Occlusion of the Circle of Willis (Moyamoya disease) of the Ministry of Health and Welfare, Japan. Clin Neurol Neurosurg. 1997;99(Suppl 2):S238–40.CrossRefGoogle Scholar
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