Moyamoya Syndrome

Figure 1: Head CTA (left) and brain MRA rendering (right) showing bilateral middle cerebral artery (MCA) stenoses with reduced vascular filling within the MCA territories. Images taken 4-8 months post indirect revascularization via right-sided EDAS (encephalo-duro-arterio-synangiosis) demonstrating unchanged vascular pattern from baseline. Right-sided craniotomy can be seen on the CTA (left, asterisk).

Approximately 1 year following the R-EDAS procedure and without significant clinical improvement, brain perfusion showed delayed mean transit times (MMT) accentuated in the right MCA territory (Figure 2). In neuropsychological testing, memory function had significantly improved.

To stabilize and improve brain perfusion, a contralateral EDAS procedure was performed on the left side (Figure 3). With unremarkable hospital course, the patient recovered from the surgery and was discharged home.

Figure 2: CT perfusion imaging, mean transit time (MTT) mapping. Delayed MTT accentuated in the right middle cerebral artery territory (yellow bracket).

Figure 3: Head CT imaging post left-sided EDAS surgery. Unremarkable brain imaging. Bilateral craniotomy is seen from prior right-sided EDAS and current left-sided EDAS procedures.

Approximately 6 months later, with persistent left-hand weakness, the patient underwent multiple cranial burr holes placement to help improve paramedian vascular collateralization (Figure 4).

Figure 4: Head CT imaging following placement of multiple cranial burr holes.

Over the next months, the patient experienced a significant clinical improvement with reduced fatigue and increased processing speed and raised attention in neuropsychological testing (Figure 5).

Figure 5: Neuropsychological testing in five domains: memory, processing speed, attention, executive function, and visuospatial abilities. Performance at three time-points of clinical surgical history. Higher percentiles represent better function, where performance from 30th percentile and higher is considered normal.

Brain MRA 15 months following the second EDAS procedure and 10 months following burr holes placement showed increased vascular filling in both MCA territories (Figure 6).

Figure 6: Brain MRA rendering at two time-points of clinical surgical history. Marked improvement in vascular filling 26 months following the first EDAS surgery (right).

A total of 37 months following the first EDAS surgery, head CT perfusion imaging found no deficits in cerebral blood flow (CBF) or time to maximum value of residue function (Tmax) (Figure 7).

Figure 7: Head CT perfusion imaging, 37 months following first EDAS surgery. Time to maximum value of residue function (Tmax) of >4 sec observed in both hemispheres, but below threshold (left). Overall, no significant deficits in CBF or Tmax detected (right).

Treatment Considerations:

Moyamoya syndrome is a vaso-occlusive disease of intracranial arteries, typically with narrowing and occlusions of proximal vessels of the Circle of Willis, such as the distal internal carotid artery, middle cerebral artery and anterior cerebral artery^1,2. Most often, like in the patient of this case report, the cause is atherosclerosis in the presence of traditional vascular risk factors. Additional causes include sickle cell disease and neurofibromatosis type-1, among others. This is distinguished from the rarer moyamoya disease that has a non-atherosclerotic (unknown) mechanism and is more prevalent in East Asian populations.

Untreated, moyamoya syndrome tends to get worse. With progressing intracranial occlusive disease, the risk of stroke, long-term disability or death increases. Revascularization surgery is required when cerebral perfusion deficit and clinical symptoms have occurred, or the patient is at high risk of a cerebral ischemic event. Two principal methods of revascularization surgery can be offered, the direct and indirect. The indirect method, e.g. encephalo-duro-arterio-synangiosis or EDAS, offers a less invasive option compared to the direct surgical arterio-arterial anastomosis, e.g. between superficial temporal artery and middle cerebral artery, which can be difficult to accomplish^3,4. In EDAS surgery, extracranial arteries are placed on the brain surface through a craniotomy. The goal is natural revascularization of the affected brain region via de-novo collateralization between extracranial and intracranial arteries. Although less invasive, EDAS often requires several months to years for the growth-factor induced revascularization to occur. Next to clinical neurological follow-up, longitudinal neuropsychological testing is helpful to assess sometimes subtle, and other times dramatic improvements in cognitive function following surgery⁵. When the desired effect is delayed or only insufficient, bilateral revascularization surgery and burr hole placements can help accelerate the revascularization process.

Figure 8. Encephalo-duro-arterio-synangiosis, EDAS, for restoration of cerebral circulation. In this indirect revascularization procedure, an extracranial artery (superficial temporal artery) is exposed to the intracranial cerebral surface through the craniotomy without establishing a direct arterio-arterial anastomosis (left). The craniotomy is closed at the end of the procedure with the exposed external artery secured in the intracranial space (right). Under the influence of growth factors contained in the subarachnoid CSF de-novo vascular connections are created between external artery and cerebral arteries.

References:

1. Scott RM, Smith ER. Moyamoya Disease and Moyamoya Syndrome. N Engl J Med 2009; 360:1226-1237. https://www.nejm.org/doi/full/10.1056/nejmra0804622
2. Dlamini N, Muthusami P, Amlie-Lefond C. Childhood Moyamoya: Looking Back to the Future. Pediatr Neurol. 2019 Feb;91:11-19. doi: 10.1016/j.pediatrneurol.2018.10.006. https://www.sciencedirect.com/science/article/abs/pii/S0887899418308324
3. Gadgil N, Lam S, Payarali M et al. Indirect revascularization with the dural inversion technique for pediatric moyamoya disease: 20-year experience. J Neurosurg Pediatr 2018; 22: 541-9. https://thejns.org/pediatrics/view/journals/j-neurosurg-pediatr/22/5/article-p541.xml
4. Liu JJ, Steinberg GK. Direct Versus Indirect Bypass for Moyamoya Disease. Neurosurg Clin N Am. 2017 Jul;28(3):361-374. https://pubmed.ncbi.nlm.nih.gov/28600011/
5. Ando T, Shimada Y, Fujiwara S, et al. Revascularisation surgery improves cognition in adult patients with moyamoya disease. J Neurol Neurosurg Psychiatry. 2020 Mar;91(3):332-334. https://pubmed.ncbi.nlm.nih.gov/31836638/