Surgical Techniques in Moyamoya Vasculopathy. Peter Vajkoczy

Chapter 19. Individualized Extracranial-Intracranial Revascularization in the Treatment of Late-Stage Moyamoya Disease


Late stage moyamoya disease is defined as the one at stage 5 to 6 of Suzuki’s grading system, despite of spontaneous collaterals from branches of external carotid artery, cerebral revascularization is still necessary in most patients. But the diversity and complexity of collateral paths make it difficult to preserve the already-formed collaterals, which is the principle of this kind of surgical procedure. Individualized revascularization seems to be an effective solution. Here we will introduce a set of strategies, including individualized designation of skin f lap, temporal muscle flap, bone flap, dura matter flap, and target revascularization. The set of strategies is proved to be safe and effective in our single institution case series.

Keywords: moyamoya disease, Suzuki stage, extracranial- intracranial revascularization, spontaneous collaterals, individualized revascularization

19.1 History and Initial Description

Late-stage moyamoya disease (MMD) is defined as the one at stage 5 to 6 of Suzuki’s grading system and is characterized by spontaneous collaterals from branches of external carotid artery. In a series of 336 patients affected by late-stage MMD treated in the Department of Neurosurgery of Huashan hospital from 2005 to 2015, spontaneous collaterals are fully developed in only 3 cases (1% of the entire series) without any symptoms or cerebral hemodynamic impairment who need no surgical treatment (Fig. 19.1). About 333 patients of late-stage MMD were operated for cerebral ischemia or intracranial hemorrhage, or both, with impaired hemodynamics which could be detected by CT perfusion (CTP) or single-photon emission computed tomography (SPECT) routinely.

19.2 Indications

The indication of individualized extracranial-intracranial (EC-IC) revascularization in late-stage MMD is carefully analyzed. Microsurgical treatment of the patients is planned with attention to any preexisted spontaneous collaterals, ischemic symptoms, and hemorrhagic history.

19.3 Key Principles

The key principle of the surgery is to use all the three layered external carotid artery (ECA) branches including superficial temporal artery (STA), posterior auricular artery (PAA) or occipital artery (OA) that are feeding the scalp, deep temporal artery (DTA) feeding the temporal muscle, and middle meningeal artery (MMA) feeding the dura, meanwhile preserving the already-formed collaterals.

19.4 SWOT Analysis

19.4.1 Strength

 Combined direct and indirect approach allows the full use of all the branches coming from the ECA, while preserving preexisted spontaneous collaterals.

19.4.2 Weaknesses

 Due to poorer MCA vessel networks of late-stage MMD, the recipient artery may not distribute blood flow as efficiently as in early stage MMD with heathier MCA vessel network.

 The mean blood flow in bypass is reduced compared with those bypass flow performed in patients with early stage of MMD.

 There can be a competition between the bypass flow and the original flow in MCA network that may cause blood flow congestion and edema of the cortex, which have consequently higher occurrence of postoperative transient neurological deficit.

19.4.3 Opportunities

 Carefully designed revascularization, based on a comprehensive understanding of clinical symptoms, spontaneous collaterals, hemodynamic characters, and recipient artery networks, could replace the blood flow to most suffering ischemic area of the brain cortex.

 Late stage of MMD already has some spontaneous stomas from ECA branches with a better potential to form new stomas by encephalo-duro-myo-synangiosis (EDMS), the indirect part of the surgery.

19.4.4 Threats

 Due to the barrier of ventricles, although the ischemic condition of deep structure such as thalamus and basal ganglion could be improved, the blood flow via the moyamoya vessels is still needed in most cases.

• The occurrence of rehemorrhage cannot be totally obliterated.

19.5 Contraindications

The contraindications to perform this technique are when the ECA already developed full collateral blood flow.

19.6 Special Considerations

Neurosurgeons should analyze the spontaneous collaterals in the preoperative digital subtraction angiography

(DSA) very carefully (Fig. 19.2). Main collateral paths in the abovementioned group of 336 cases are listed in Table 19.1.

MMA is the most common source of spontaneous collaterals. It enters the floor of the middle cranial fossa through the foramen spinosum, passes laterally on to the temporal bone, and curves anteriorly over the great wing of sphenoid. Thereafter, it divides into anterior and posterior branch. MMA can provide important collateral flow through dura mater. Normally, it is the anterior (frontal) branch that provides collateral blood flow to anterior cerebral artery (ACA) territory through falx. MMA could be originated from ophthalmic artery in anatomic variated cases. MMA is vulnerable to the routine pterional craniotomy because hyperplasia MMA may be located deep in the cranial sulcus, increasing the risk of damage, causing post-procedural ischemic stroke.

Scalp arteries, such as STA, OA, and sometimes PAA, are rare sources of spontaneous collaterals, but in patients with any kind of craniotomy history like cerebral hematoma evacuation or external ventricular drainage, the proportion is greatly increased. In this situation, individualized designation of scalp flap is of great importance.

Heparin saline irrigation is recommended only during anastomosis; we do not recommend a general heparinization.

19.7 Pitfalls, Risk Assessment, and Complications

 In some cases, direct bypass may not be feasible due to the small size of recipient artery.

 Sometimes the dimeter ratio of donor-recipient artery is larger than 2.5 times, the operator may quit direct bypass because of the high possibility of postoperative hemorrhage.

 The recipient MCA network is very poor on DSA and MR angiography (MRA). There is poor blood flow in some branches of MCA that looks pale and poorly filled under microscope. It is also a contradiction for direct bypass.

 The EC-IC revascularization holds the potential risk of postoperative transient neurological deficits, seizure, and postoperative hemorrhage.

19.8 Special Instructions, Position, and Anesthesia

Supine position was used as a routine for STA-MCA or PAA-MCA bypass. Park-bench position was used for OA- PCA bypass. The use of head clamp should be avoided to protect contralateral STA. Blood pressure was maintained within the patient’s baseline range throughout the surgical procedural. Hyperventilation was avoided in order to prevent vasoconstriction. During the perioperative period, blood volume was expanded using crystalloid, normally 1.25 to 1.4 times maintenance through postoperative day 2.

19.9 Patient Position with Skin Incision and Key Surgical Steps

19.9.1 Skin Incision

The main concern of individualized designation of skin incision is to recognize the preexisted spontaneous anastomosis; meanwhile, the bone flap should cover the ischemic area. Selected ECA angiogram is routinely performed before surgery; MRA or CT angiography (CTA) could not provide all the necessary details of spontaneous collaterals.

In our routine procedure, an extended pterional skin incision is adopted to make full use of DTA of temporal muscle and of STA branches located in the scalp flap. The incision is extended by 1.0 to 1.5 cm above the superior temporal line. Individualized adjustments would be made in the following situations (Fig. 19.3):

1. Spontaneous collaterals from STA branch are carefully identified in the angiography. The area of ischemic cortex is defined by CT perfusion or SPECT. Scalp incision should be adjusted forward or backward so as to avoid injury of scalp artery with preexisted spontaneous collaterals and to cover the ischemic cortex.

2. When routine pterional craniotomy cannot cover ischemic region, the procedure can be planned differently. For example, in patients with ischemic bilateral ACA territory, bilateral frontal lobe should be covered in the way that a coronal incision is adopted (Fig. 19.1; Fig. 19.8). When the ischemic area is located in the occipital lobe, horseshoe-shape scalp incision covering the temporal-parietal-occipital lobe is adopted.

19.9.2 Temporal Muscle

Spontaneous anastomosis from temporal muscle could be formed only in patients with a history of craniotomy, and rest part of temporal muscle outside bone window could still be used as donor tissue. The temporal muscle is dissected from the temporal bone without using monopolar so that the entire DTA network is kept intact (Fig. 19.4). DTA normally is small and the distal part could not be recognized clearly in preoperative DSA. Any incision of the temporal muscle could hurt the DTA network and result in poor collateral flow. We therefore avoid temporal muscle incision except in very thick ones.

19.9.3 Bone Flap

MMA is the most common source of spontaneous collaterals in late-stage MMD, and it is vulnerable in craniotomy. Kuroda analyzed the relationship between MMA and pterion and divided it into the following: (1) bridge, (2) monorail, and (3) tunnel types. The extent of difficulty to preserve MMA integrity increases from type a to c. In routine single-window pterional craniotomy, it is very difficult and time-consuming to preserve MMA; we thus developed another double-window craniotomy.

Preoperative localization of MMA is of paramount importance. The groove of MMA in cranium could be seen in DSA mask images clearly (Fig. 19.7a), and the relationship between MMA groove and coronal suture is of great help in localizing MMA in craniotomy. The relation between MMA and STA is also helpful. The course of MMA is approximately parallel to that of STA parietal branch, by 2 to 3 cm anteriorly (Fig. 19.5a).

1. Single-window bone flap.

When MMA groove is shallow and vague in DSA mask images, a single-window heart-shape craniotomy is performed. The bone window is expanded carefully towards sphenoidal crest to the site where MMA perforated from the bone, preserving the lesser wing of sphenoid bone (Fig. 19.5).

When transdural collaterals could be identified on the convexity of frontal lobe, there’s no ischemic area in frontal lobe, a single-window bone flap posterior to MMA would be adopted (Fig. 19.6).

2. Double-window bone flaps.

When MMA groove is deep and clear in DSA mask images, we prefer double-window bone flaps-anterior and posterior to MMA respectively, a bone bridge is left to cover the course of MMA. We created a complex of dura, MMA, middle meningeal vein (MMV), and covered-bone bridge (Fig. 19.7). We believe that this is the best way to protect MMA and the distal spontaneous stomas.

In patients with ischemia of bilateral ACA territory, bilateral frontal lobe should be covered, a coronal incision and bifrontal bone flaps should be adopted (Fig. 19.8).

19.9.4 Dura Mater

The integrity of MMA network is the most important aspect in order to preserve the vascular support. Since the potential of MMA as donor is great, every single branch of MMA should be preserved. Dura mater would be incised along each main branch of MMA separately. Radial incisions were made on the remaining part of the dura mater. After hemostasis, dura mater is flipped over with its outer surface being in close contact with the cortex(Fig. 19.9).

Sometimes, the bleeding of accompanying MMV is difficult to control. The coagulation using bipolar could damage MMA. In this condition, keeping the patency of MMA and hemostasis of accompanying MMV could be attained simultaneously by means of barrel-suturing (Fig. 19.9f, g), which is what we call “Chinese spring roll.” The margin of the dura mater was sutured into a shape of barrel with the inner surface facing outside. The barrel is exactly like a “Chinese spring roll,” containing MMA, accompanying veins, and some gelfoam strip.

19.9.5 Target Revascularization

Ischemic area could be defined by hemodynamic evaluation as CTP or SPECT. Spontaneous collaterals in latestage MMD created some normal-perfused island in the ischemic hemisphere. If the recipient artery located in this kind of normal perfused area, the pressure difference between donor and recipient (AP of Poiseuille’s Law, q= T x гл4 x Ap/8gl, AP is the only explanation for driving the blood flow) could be too small to form a sustainable bypass. AP is a dynamically changing parameter after surgery until achieving a balanced condition after all the spontaneous stoma formed. This progress may take 6 months or even longer. The competitive blood flow for bypass comes not only from the internal carotid artery system, but also progressively from the collateral blood flow via the spontaneous stoma originated from MMA and DTA. On the basis of these two facts, target revascularization is reasonable, which may facilitate blood flow to where it is mostly demanded with greatest AP. There are two different blood flow pressure gradients in MCA networks. One is still keeping the physiological direction from proximal to distal. The pressure gradient is Pproxi- mal>Pdistal. The other is reversed, Pproximal<Pdistal (Fig. 19.10). Operators could recognize the different pressure gradient after careful scrutinize of DSA and SPECT (Fig. 19.11a-d). Intraoperative indocyanine green (ICG) angiogram is also helpful in localizing the recipient area. In cases of good MCA network, which can bear more blood flow from donor arteries, double barrel bypass would be considered, sometimes only using single branch of STA (Fig. 19.11 f). The totally infarcted area should be avoided as revascularization is in vain.

19.9.6 The Simplest Anastomosis Techniques

The recipient artery of late-stage MMD is usually fragile and with a lot of small branches. The vessel wall is very thin. We use two or three curved mini temporal clips to occlude the recipient artery. In this way, we can preserve all the small branches without using bipolar. No rubber mat or silicon rubber tube is needed. Interrupted suturing is adopted to guarantee the possibility of the stoma’s expanding. Square knot is carefully made without any kinking of the suture. The vascular intima is never touched in anastomosing. The stoma location near a bifurcation is preferred because it can distribute the blood flow more efficiently (Fig. 19.12).

In some cases, the wall of recipient artery is almost transparent under microscope. A tiny perforator could be left open on purpose to let small amount of blood flow reflux into the cavity of the recipient artery. This maneuver can give the recipient artery a small pressure. The stoma is kept opening for facilitating the anastomosing. With the different color of blood, the vessel wall could be seen more clearly under microscope. The irrigating of heparin saline by assistant could prevent the thrombosis.

19.10 Difficulties Encountered

A challenge encountered is extremely thin vessel wall of the recipient artery, which not only raise the difficulty of anastomosis, but also increase the risk of hemorrhage from the needle hole. We use a small piece of arachnoid membrane as a scarf for supporting the stomas (Fig. 19.12b).

19.11 Bailout, Rescue, and Salvage Maneuvers

The hemorrhage from the needle holes or some small teared holes of the extremely thin recipient artery wall is really difficult to treat. It needs some extra autologous tissue for fixing as a patch outside of the vessel wall. We normally use arachnoid membrane or fat tissue as a patch.

Postoperative complications, such as hemorrhage in distant location, status epilepticus, and severe edema, are often considered to be results of hyperperfusion, in a few cases, sacrifice of the direct bypass is maybe the only choice. In case of postoperative cerebral infarction in contralateral hemisphere, emergent combined revascularization surgery could be considered.

19.12 Tips, Pearls, and Lessons Learned

To dissect STA from the inner side of scalp is a safe and fast way. Closing the incision of superficial temporal fascia from inner side of the scalp could prevent delayed scalp healing or infection effectively.

We could create double barrel bypass with one single parietal STA in cases with good MCA network, which may introduce STA blood flow to a wider area but keeping the frontal branch for feeding scalp flap.

Double-window craniotomy, with a complex consisted of dura, MMA, MMV, and bone bridge, is the best way to keep the integrity of MMA and distal spontaneous stomas.

“Chinese spring roll” containing MMA, accompanying veins, and some gelfoam strip are the solution for keeping the patency of MMA and hemostasis of accompanying MMV simultaneously.

The simplest anastomosis technique is effective in shortening average temporary occulting time, while preserving all branches of the recipient artery.

The autologous tissue such as arachnoid membrane and fat tissue could be used as a “patch” outside of the

extremely thin recipient vessel wall for hemostasis and strengthening the stoma.

A tiny perforator could be left open on purpose to let small amount of blood flow reflux into the cavity to keep the recipient artery open for facilitating the anastomosing.

Determinants of blood flow after bypass are including: carrying capacity of STA, AP = P(donor)-P(recipient), carrying capacity of recipient artery and integrity of MCA network.

Suggested Readings

Suzuki J, Takaku A. Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base ofbrain. Arch Neurol. 1969; 20(3):288- 299

Kuroda S, Houkin K. Moyamoya disease: current concepts and future perspectives. Lancet Neurol. 2008; 7(11):1056-1066

Matsushima T, Inoue K, Kawashima M, Inoue T. History of the development of surgical treatments for moyamoya disease. Neurol Med Chir (Tokyo). 2012; 52(5):278-286

Kuroda S, Houkin K. Bypass surgery for moyamoya disease: concept and essence of surgical techniques. Neurol Med Chir (Tokyo). 2012; 52(5): 287-294

Xu B, Song DL, Mao Y, et al. Superficial temporal artery-middle cerebral artery bypass combined with encephalo-duro-myo-synangiosis in treating moyamoya disease: surgical techniques, indications and midterm follow-up results. Chin Med J (Engl). 2012; 125(24):4398-4405

Xu B, Song DL, Mao Y, Xu H, Gu YX, Chen G. Use superficial temporal arterymiddle cerebral artery bypass combined with encephalo-duro-myo-synangiosis to treat moyamoya disease. Chin J Cerebrovasc Dis (Chin). 2007; 4:445-448

Shimizu S, Hagiwara H, Utsuki S, Oka H, Nakayama K, Fujii K. Bony tunnel formation in the middle meningeal groove: an anatomic study for safer pterional craniotomy. Minim Invasive Neurosurg. 2008; 51(6):329-332

Ma S, Baillie LJ, Stringer MD. Reappraising the surface anatomy of the pterion and its relationship to the middle meningeal artery. Clin Anat. 2012; 25(3):330-339

Hori S, Kashiwazaki D, Akioka N, et al. Surgical anatomy and preservation of the middle meningeal artery during bypass surgery for moyamoya disease. Acta Neurochir (Wien). 2015; 157(1):29-36

Chen L, Xu B, Wang Y, Liao Y, Pan H, Wang Y. Preoperative evaluation of moyamoya spontaneous anastomosis of combined revascularization donor vessels in adults by duplexultrasonography. Br J Neurosurg. 2017 (Nov):1360-1366

Wang Y, Chen L, Wang Y, et al. Hemodynamic study with duplex ultrasonography on combined (direct/indirect) revascularization in adult moyamoya disease. J Stroke Cerebrovasc Dis. 2014; 23(10):2573-2579

If you find an error or have any questions, please email us at Thank you!