Indirect Revascularization in a patient with a Stenosis of the Middle Cerebral Artery

Figure 1. Isolated, proximal right middle cerebral artery stenosis of moyamoya type (cerebral angiogram left; arrow). Brain perfusion anomaly in the territories of anterior and middle cerebral arteries (CT perfusion right).

A 60-year-old woman experienced seizure episodes and left-sided neurological symptoms. Brain imaging showed right-hemispheric stroke and isolated, proximal right middle cerebral artery stenosis of moyamoya type (Figures 1,2). CT perfusion imaging confirmed perfusion anomaly with increased time to maximum blood flow (Tmax) bilaterally but accentuated in the right middle cerebral artery territory (Figures 1,3). Left-hemispheric perfusion anomaly was likely due to extensive right-hemispheric collateralization from the anterior cerebral artery (Figure 2) further increasing the risk for ischemic events.

Figure 2. Proximal right middle cerebral artery stenosis of moyamoya type (CT angiogram left and conventional angiogram middle/right; arrow). Incomplete filling of branches of the right middle cerebral artery (M) (internal carotid artery injection middle/right). Extensive collateral flow from the ipsilateral anterior cerebral artery (A) into the middle cerebral artery territorial branches (right).

Figure 3. CT perfusion imaging at baseline (top) and 8 months after EDAS (bottom). Diffuse perfusion anomaly bilaterally with accentuation of the right hemisphere with Tmax >6s in 13ml of brain tissue volume and CBF<30% in 7ml of tissue volume (top). 8 months a post-EDAS significant improvement of perfusion parameters with the absence of tissue with Tmax >6s and reduction of tissue volume with CBF<30% to 3ml (bottom). An indirect revascularization procedure (encephalo-duro-arterio- synangiosis, EDAS) was performed by neurosurgeon John A. Grant, M.D. to restore cerebral circulation and help prevent future strokes (Figure 4). Eight months following the procedure the patient was clinically stable and brain perfusion parameters had significantly improved (Figure 3). Further improvement of brain perfusion can be expected over time.

Figure 4. Encephalo-duro-arterio-synangiosis, EDAS for restoration of cerebral circulation. In this indirect revascularization procedure an external 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. Superficial temporal artery, STA (yellow solid arrow) and parietal branch of STA (yellow dotted arrow). Illustration by: E. Y. C.

SUMMARY:
Symptomatic intracranial stenosis of cerebral arteries may be treated with direct or indirect revascularization surgery where extracranial arteries are placed intracranially through a craniotomy either with an arterio-arterial anastomosis (direct revascularization) or without such an anastomosis (indirect EDAS). The indirect surgical procedure is less invasive and less burdensome compared to the direct method. However, the indirect EDAS often requires several months for the growth- factor induced revascularization to occur between extracranial and cerebral arteries.

REFERENCES
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.