Value of Burr‐Hole Surgery as an Adjunct to Encephaloduroarteriosynangiosis in Treatment of Adult Moyamoya Disease: A Case Series

Abstract

Background

Using a single indirect revascularization technique in adult patients with moyamoya disease has been associated with inconsistent outcomes. Herein, we aimed to describe treatment outcomes following combined encephaloduroarteriosynangiosis plus burr‐hole surgery (BHS) in adult moyamoya disease.

Methods

Encephaloduroarteriosynangiosis combined with 1 anterior and 1 posterior burr hole per hemisphere was performed in 16 adults with moyamoya disease who presented to our center between 2013 and 2019. Patients were followed with clinical reassessments and cerebral angiograms to evaluate for neovascularization.

Results

Combined encephaloduroarteriosynangiosis and BHS procedures were performed on 24 hemispheres in 16 patients. Follow‐up ranged from 9 to 57 months, during which no new ischemic or hemorrhagic events, perioperative or long‐term complications, or deterioration of symptoms was observed. Follow‐up angiography showed evidence of additional neovascularization provided by the burr holes in 18 of the 24 hemispheres. Of 9 hemispheres with poor revascularization response to encephaloduroarteriosynangiosis, 5 achieved neovascularization at the burr‐hole sites. Older age, smoking, and cerebral infarction or hemorrhage on preoperative magnetic resonance imaging tended to correlate with absence of neovascularization following BHS.

Conclusions

BHS is a simple and safe procedure that can be done simultaneously with other indirect or direct revascularization procedures. It can provide additional neovascularization even in patients unresponsive to encephaloduroarteriosynangiosis (EDAS) and can be tailored to improve the blood flow in any vascular territory that may not be properly covered by standard revascularization procedures. We find value in adding BHS as an adjunct to other indirect or direct revascularization techniques such as encephaloduroarteriosynangiosis for treatment of adult moyamoya disease.

Nonstandard Acronyms and Abbreviations

BHS

burr‐hole surgery

DSA

digital subtraction angiography

MMD

moyamoya disease

STA

superficial temporal artery

Clinical Perspective

• Addition of 2 burr holes to the standard encephaloduroarteriosynangiosis procedure resulted in additional neovascularization in 75% of the treated hemispheres in adult patients with moyamoya disease. No complications were observed.

• The neovascularization provided by burr holes was independent from neovascularization status of the encephaloduroarteriosynangiosis site.

• Burr‐hole surgery is a simple and safe procedure that can be performed in adjunction to encephaloduroarteriosynangiosis in a single operation to enhance the extent of revascularization.

Moyamoya disease (MMD) refers to a progressive steno‐occlusive disorder at the distal internal carotid artery and proximal middle cerebral artery or anterior cerebral artery with abnormal collateral vessel formation at the base of the brain. ¹ The steno‐occlusive changes and compensatory abnormal vessel formation predispose patients to ischemic and hemorrhagic manifestations, respectively.

The current treatment paradigm is to prevent cerebral ischemia by augmenting cerebral blood flow using direct or indirect revascularization approaches. ² Indirect revascularization is widely accepted as the treatment of choice in pediatric MMD. ³ However, there are few reports of indirect revascularization surgery in adult MMD compared with pediatric MMD, and it is unclear whether indirect revascularization surgery is sufficiently effective in this subgroup of patients. Although encephaloduroarteriosynangiosis is the most widely used indirect technique, a significant portion of patients fail to develop neovascularization. ⁴ Given that burr‐hole surgery (BHS) can be done in addition to other techniques as a single procedure, we hypothesized that additional neovascularization in cortical areas not affected by encephaloduroarteriosynangiosis may be achieved by addition of BHS. Herein, we report our experience with a burr‐hole procedure in combination with encephaloduroarteriosynangiosis in a series of adult patients with MMD.

Methods

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Patients

This retrospective case series included consecutive adults with MMD treated at a single‐center teaching hospital by combined encephaloduroarteriosynangiosis and BHS between December 2013 and May 2019. The indication for revascularization was previous stroke or progressive disease on brain magnetic resonance imaging and digital subtraction angiography (DSA). We opted for indirect revascularization with encephaloduroarteriosynangiosis and burr holes rather than direct bypass in cases with relatively stable disease with low risk of rapid decompensation, and also in patients who were not eligible for direct bypass, considering the status of the donor and recipient vessels and patients’ comorbidities. Patients with moyamoya syndrome attributable to other disease entities, pediatric patients (<18 years old), and patients for whom DSA data before and at 1 year after surgery were not available were excluded. Institutional review board approval was obtained before commencement of the study. Informed consent was waived given the retrospective nature of the study.

Perioperative Evaluations

Preoperatively, all patients underwent a neurological examination, computed tomographic scanning or magnetic resonance imaging, and DSA. We reviewed the deidentified medical records of all eligible patients to assess possible risk factors associated with the treatment outcomes and development of postoperative complications, including age, sex, onset manifestation, smoking, hypertension, hyperlipidemia, diabetes, antiplatelet therapy, neurological status, and imaging findings. The angiographic stage of disease for each affected hemisphere was graded according to the Suzuki classification. ¹ Collateral supply formation was graded using the Matsushima scale. ⁵ Evaluation of moyamoya vessels was performed using a scale of 0 to 2 ⁴ : absent (0), no apparent generation of moyamoya vessels; fair (1), scarce and localized moyamoya vessels; and abundant (2), moyamoya vessels stretching into all directions. Neurological status was evaluated with the modified Rankin scale on admission.

Assessment of Outcomes

Patients were followed up postoperatively through scheduled visits, during which the changes in clinical status and surgical complications were recorded. Since neovascularization is expected to reach the maximum at ≈1 year ⁶, a follow‐up DSA was performed at 1 year following the surgery to assess neovascularization at the site of encephaloduroarteriosynangiosis and BHS and to evaluate for progression of disease. Collateral supply formation for encephaloduroarteriosynangiosis was graded using the Matsushima scale. ⁵ Neovascularization status at the location of burr holes was classified into 3 categories: grade 0, no vascularization; grade 1, limited to only burr hole; and grade 2, beyond burr hole (Figure 1).

Figure 1.

Cerebral digital subtracted angiography showing burr‐hole neovascularization grades. Neovascularization of burr‐hole surgery was classified into 3 categories. Grade 0, no neovascularization (A); grade 1, limited to only burr‐hole site (B); and grade 2, beyond burr‐hole site (C).

Surgical Technique

After induction of general anesthesia, patients were positioned for a frontotemporal craniotomy in a standard fashion. The superficial temporal artery (STA) was mapped on the scalp surface using a Doppler probe and was meticulously dissected out from the surrounding tissue. After temporal craniotomy, the STA was placed on the brain surface. The arachnoid was opened fairly widely in the areas where the vessel came in contact with the brain surface. The vessel was tacked to the arachnoid surface using 9‐0 nylon suture. Afterwards, 2 separate incisions were created, 1 frontally and 1 posteriorly in the frontal and anterior parietal area ≈2.5 cm in length. The perforator bit was used to create burr holes in these regions at least 3 cm from the midline. Bone chips were removed and bleeding was controlled using bipolar forceps. The dura was opened sharply in a wide circumferential fashion underneath the burr holes until there was good communication with the subarachnoid space. Bipolar coagulation was used to achieve hemostasis if there was bleeding. The wounds were closed by reapproximating the galea using interrupted 2‐0 buried Vicryl suture, after which the skin was closed using running 3‐0 nylon suture in an unlocked fashion. All procedures were performed by experienced neurosurgery faculty, assisted by fellows and residents with an adequate level of training.

Statistical Analysis

The categorical variables are presented as counts (with percentages), and continuous variables are presented as means±SD. Hemispheres were categorized into 2 groups based on the follow‐up neovascularization status of BHS, and analyzed for possible associations with multiple baseline and follow‐up clinical and radiologic variables, to decipher predictors and determinants of treatment response and failure. Two‐tailed t‐tests and the Mann‐Whitney U‐test were used to compare continuous variables as appropriate. The Pearson chi‐square test and Fisher exact test were used to compare categorical variables as appropriate. All statistical analysis was performed using SPSS software (version 22.0; IBM, Armonk, NY). A P value <0.05 was considered as statistically significant.

This case series has been reported in line with the Consensus Preferred Reporting of Case Series in Surgery Guideline. ⁷

Results

Baseline Characteristics

Sixteen patients (4 men and 12 women) were included in our series, 8 of whom underwent bilateral procedure. Therefore, 24 hemispheres were included in this study in total, with each hemisphere receiving encephaloduroarteriosynangiosis plus 2 burr holes, located anteriorly and posteriorly. The baseline demographic, clinical, imaging, and angiographic characteristics of the patients are summarized in Table 1. Mean age of the patients was 45.6 years (range, 24–72 years). Evaluation of brain magnetic resonance imaging/computed tomography on presentation revealed evidence of infarction and hemorrhage in 11 and 4 hemispheres, respectively.

Table 1.

Baseline Characteristics of Patients With Moyamoya Disease Treated by Encephaloduroarteriosynangiosis and Burr Hole

							Preoperative angiogram
							Collateral circulation		Moyamoya vessels
Case	Age	Sex	Type	Side	Clinical presentation	MRI presentation	Source	Extent	Source	Extent	Suzuki stage	Smoking	Hypertension	Hyperlipidemia	Diabetes	Antiplatelet therapy	mRS
1	72	F	Unilateral	Right	TIA	None	ACA, PCA	Abundant	ICA	Abundant	3	+	−	−	−	Aspirin	1
2	45	F	Bilateral	Right	Infarction	Infarction	−	Absent	−	Absent	5	+	−	−	−	Aspirin Clopidogrel	1
3	36	F	Bilateral	Right Left	TIA Asymptomatic	None None	PCA ACA, PCA	Abundant Abundant	ICA ICA	Fair Abundant	4 3	+	−	−	−	Aspirin	1
4	38	M	Bilateral	Right Left	Infarction Asymptomatic	Infarction None	ACA, PCA ACA, PCA	Fair Fair	ICA ICA	Fair Abundant	3 3		−	−	−	Aspirin	1
5	56	F	Bilateral	Left	Infarction	Infarction	PCA	Fair	ICA	Fair	4	−	−	+	+	Aspirin	3
6	48	F	Bilateral	Right Left	Asymptomatic Hemorrhage	Infarction Hemorrhage	PCA PCA	Fair Fair	−	Absent Absent	4 4	+	+	−	−	No	2
7	42	F	Bilateral	Right Left	TIA TIA	Infarction Infarction	PCA PCA	Fair Abundant	Ophthalmic A Ophthalmic A	Fair Abundant	4 4	+	+	−	−	Aspirin	1
8	25	F	Unilateral	Left	TIA	None	PCA	Fair	ICA	Fair	3	−	−	−	−	Aspirin	1
9	56	M	Unilateral	Left	Hemorrhage	Hemorrhage	PCA	Abundant	ICA	Abundant	3	+	+	+	−	Aspirin	1
10	50	F	Bilateral	Right Left	Asymptomatic TIA	None Infarction	PCA PCA	Abundant Fair	− ICA	Absent Abundant	5 3	−	+	−	−	Aspirin	1
11	53	F	Unilateral	Left	TIA	Infarction	ACA, PCA	Poor	ICA	Abundant	3	−	−	−	−	Aspirin	1
12	33	F	Bilateral	Right Left	Asymptomatic TIA	None Infarction	PCA PCA	Abundant Abundant	ICA ICA	Abundant Abundant	3 3	−	−	−	−	Aspirin	1
13	34	F	Bilateral	Left	Infarction	Infarction	PCA	Abundant	ICA	Abundant	4	−	−	−	+	Aspirin	1
14	55	M	Bilateral	Right Left	Asymptomatic Infarction	None Infarction	ACA, PCA ACA, PCA	Fair Fair	ICA ICA	Fair Fair	3 4	−	−	−	−	Aspirin	2
15	24	F	Bilateral	Right Left	Hemorrhage Asymptomatic	Hemorrhage None	ACA, PCA PCA	Abundant Abundant	ICA ICA	Abundant Abundant	3 4	−	−	−	−	Aspirin	1
16	64	M	Bilateral	Right	Hemorrhage	Hemorrhage	PCA	Fair	ICA	Fair	4	+	+	−	−	Aspirin	3

ACA indicates anterior cerebral artery; ICA, internal carotid artery; mRS, modified Rankin scale; PCA, posterior cerebral artery; and TIA, transient ischemic attack.

Clinical and Angiographic Outcomes

Clinical and angiographic follow‐up was performed after a mean follow‐up of 16.4 months (range 9–57 months) (Table 2). There was no mortality or morbidity after the surgical procedures. No new or worsening neurological deficits, rebleeding, immediate, or delayed complications were detected during the follow‐up period. Functional status as measured by modified Rankin scale improved in 5 patients, corresponding to 8 hemispheres (33.3%), and remained unchanged in the rest.

Table 2.

Postoperative Follow‐Up Characteristics of Patients With Moyamoya Disease Treated by Encephaloduroarteriosynangiosis and Burr‐Hole Surgery

Case	Site	Follow‐up duration (months)	Clinical outcome		Angiographic outcome
			mRS	Symptom change	Progression of stenosis	Neovascularization of encephaloduroarteriosynangiosis	Neovascularization of BHS
1	Right	14	0	Improved	−	Fair	0
2	Right	12	1	NC	−	No	0
3	Right Left	13.5 11.5	1	NC	+ +	Fair Fair	2 1
4	Right Left	9 10.5	1	NC	− −	Poor Poor	2 1
5	Left	57	3	NC	−	Good	2
6	Right Left	16 12	1	Improved	− −	Poor Good	2 1
7	Right Left	22 12	1	NC	− −	Good Fair	0 2
8	Left	18	1	NC	−	Poor	1
9	Left	12	1	NC	−	No	0
10	Right Left	50 15	0	Improved	− −	Good Good	2 1
11	Left	12	1	NC	−	Fair	1
12	Right Left	15 13	1	NC	− −	Good Good	2 2
13	Left	12	1	NC	+	Good	2
14	Right Left	10 12	1	Improved	− −	Poor No	1 0
15	Right Left	12 13	1	NC	+ −	Fair Fair	2 1
16	Right	12	2	Improved	−	No	0

Neovascularization of BHS: grade 0, no vascularization; grade 1, limited to only burr hole; grade 2, beyond burr hole. BHS indicates burr‐hole surgery; mRS, modified Rankin scale; and NC, no change.

Neovascularization of encephaloduroarteriosynangiosis in the follow‐up DSA based on the Matsushima classification was absent in 4 hemispheres (16.7%), poor in 5 hemispheres (20.8%), fair in 7 hemispheres (29.2%), and good in 8 hemispheres (33.3%). Evaluation of burr‐hole sites in follow‐up DSA showed evidence of neovascularization in 18 of 24 (75%) hemispheres that received BHS (Table 2). The extent of neovascularization was grade 0 (absent) in 6 (25%) hemispheres, grade 1 (within the burr hole area) in 8 (33.3%) hemispheres, and grade 2 (beyond the burr hole area) in 10 (41.7%) hemispheres. Neovascularization from either encephaloduroarteriosynangiosis or BHS or both was achieved in 20 (83.3%) hemispheres. The neovascularization derived mainly from the middle meningeal arteries, and superficial temporal arteries (to a lesser extent) for BHS, and from STA for encephaloduroarteriosynangiosis. A total of 13 of 15 (86.7%) hemispheres with good neovascularization for encephaloduroarteriosynangiosis also had fair or abundant neovascularization for BHS (Figure 2). Five of 9 (55.5%) hemispheres with poor neovascularization of encephaloduroarteriosynangiosis had fair or abundant neovascularization for BHS (Figure 3).

Figure 2.

Lateral angiograms of external carotid artery before the surgical treatment (A) and after 1 year (B). External carotid artery angiograms show progressive evidence of neoangiogenesis at the distal branches of the superficial temporal artery around encephaloduroarteriosynangiosis (arrowhead), and neoangiogenesis at the distal branches of the superficial temporal artery and middle meningeal artery around the surgical holes (circle).

Figure 3.

Lateral angiograms of external carotid artery before the surgical treatment (A) and after 1 year (B). External carotid artery angiograms show superficial temporal artery around encephaloduroarteriosynangiosis has underdeveloped collateral circulation (arrowhead), but the middle cerebral artery is retrogradely perfused from neoangiogenesis at the distal branches of the superficial temporal artery and middle meningeal artery around the burr holes (circle).

Factors Associated With Angiographic Outcomes of BHS

Several factors were analyzed for their potential predictive value for angiographic outcomes of BHS, as summarized in Table 3. The duration of follow‐up was not significantly different between the groups with and without neovascularization on follow‐up DSA (15.3±10.6 versus 14.0±4.0, respectively; P=0.45). Age was significantly associated with outcomes, as patients who experienced neovascularization after BHS were significantly younger than those with no neovascularization (40.2±10.5 versus 55.7±11.3 years‐old; P<0.01). Smoking had a clinically remarkable association with poor outcome, as 83.3% of patients with no neovascularization were active smokers compared with 27.7% of those with neovascularization (P=0.051). Ischemic or hemorrhagic presentation, Suzuki stage of disease, extent of collateral circulation or moyamoya vessels on baseline, and progression of stenosis of the major vessels on follow‐up did not have statistically significant associations with outcomes. Interestingly, neovascularization status of encephaloduroarteriosynangiosis was not predictive of neovascularization status of BHS on follow‐up DSA (P=0.15).

Table 3.

Analysis of Potential Factors Associated With Neovascularization at Burr‐Hole Sites

Variable			Neovascularization of BHS
			Presence	Absence	P value
N			18	6
Mean age (±SD)			40.2±10.5	55.7±11.3	0.0098
Male/Female			3/15	3/3	0.14
Smoking			5	5	0.051
Hypertension			5	3	0.36
Hyperlipidemia			1	1	0.45
Diabetes			2	0	1
Type	Bilateral		16	4	0.25
	Unilateral		2	2
Clinical onset	Asymptomatic		7	0	0.14
	Ischemic		9	4
	Hemorrhagic		2	2
MRI	None		8	1	0.32
	Infarction		8	3
	Hemorrhage		2	2
Preoperative angiogram	Suzuki stage	1	0	0	0.49
		2	0	0
		3	10	2
		4	7	3
		5	1	1
		6	0	0
	Collateral circulation	Good	17	5	0.45
		Poor	1	1
	Moyamoya vessels	Absent	3	1	1
		Fair	5	2
		Abundant	10	3
Postoperative angiogram	Follow‐up duration (mo)		15.3±10.6	14.0±4.0	0.45
	Revascularization of encephaloduroarteriosynangiosis	Good	13	2	0.15
		Poor	5	4
	Progression of stenosis	Yes	3	0	0.55
		No	15	6
Clinical outcome improved			5	3	0.36

BHS indicates burr‐hole surgery; and MRI, magnetic resonance imaging.

Discussion

Surgical revascularization for MMD can be accomplished by direct or indirect revascularization surgery. The widely used STA‐middle cerebral artery direct bypass and standard indirect revascularization techniques like encephaloduroarteriosynangiosis use the superficial or deep temporal artery and thus can be performed only in the vicinity of these arteries. Therefore, they mainly improve the flow in the middle cerebral artery territory. Consequently, the impairment of blood flow in the anterior or posterior cerebral artery regions can deteriorate despite good revascularization in the middle cerebral artery territory because of the progressive nature of MMD. ⁸ Another shortcoming is the fact that not all revascularization procedures are followed by prominent local neovascularization. A recent study reported poor neoangiogenesis in 67 of 198 (33.8%) hemispheres that had undergone encephaloduroarteriosynangiosis surgery in adult patients with MMD. ⁴ Although several factors ⁴ , ⁶ have been suggested to predict poor treatment response, a clear single etiology cannot be identified in the majority of poor responders. ⁹

To overcome both of the aforementioned shortcomings, it is reasonable that procedures that combine various surgical methods be pursued, aiming to provide revascularization from multiple sources to multiple regions of the ischemic cortex. This strategy would maximize the odds and extent of revascularization. In line with this strategy, and given the favorable results of BHS combined with other indirect or direct revascularization methods in children with MMD, ¹⁰ , ¹¹ we added an anterior and a posterior burr hole to standard encephaloduroarteriosynangiosis treatment in 16 adult patients with MMD. We found that BHS provided supplemental neovascularization in 75% of the treated hemispheres, while it was associated with no peri‐ or postoperative complications.

Based on our results, we recommend that BHS be used as a routine adjunct to other direct or indirect revascularization interventions for several reasons. In addition to providing supplementary neovascularization, the procedure was extremely safe, with no complications being detected during >1 year of follow‐up. Furthermore, the procedure is simple and can be performed easily in a single surgical session with other techniques. Performing 2 burr‐hole procedures only adds 20 to 30 minutes to the total time under anesthesia, which, given the remarkable neovascularization benefits that it can provide, allows for a favorable benefit‐to‐risk ratio. Addition of BHS enables the surgeon to provide revascularization for new ischemic cortical regions that are not covered by direct bypass or encephaloduroarteriosynangiosis and thus improve cerebral blood flow in any hemispheric territory (anterior, middle, and posterior cerebral arteries), as the site of burr holes can be preselected in any territory. Addition of BHS does not preclude future use of further revascularization techniques. In case MMD progresses or sufficient neovascularization is not obtained in the first procedure, other revascularization procedures can be added later, as no vessels in the external carotid artery system are injured during BHS. ⁶ Finally, our data suggest that neovascularization provided by BHS is independent of the failure or success of encephaloduroarteriosynangiosis revascularization, which enhances the value of BHS as an adjunctive treatment to encephaloduroarteriosynangiosis. We found that 5 of 9 (55.5%) hemispheres with poor neovascularization of encephaloduroarteriosynangiosis had fair or abundant neovascularization for BHS (Figure 3). This is partly explained by the fact that the source of neovascularization is different for encephaloduroarteriosynangiosis and BHS. The follow‐up DSAs showed that the feeding artery for the neovascularization of encephaloduroarteriosynangiosis was mainly the STA, whereas the feeding artery for BHS was mainly the middle meningeal artery, and to a lesser extent, the STA.

There is no guideline for how asymptomatic patients with MMD should be followed up and managed. In our study, we observed that neovascularization at BHS sites was detected in 100% of asymptomatic hemispheres. Presumably, vessel ingrowth helped stabilize the ischemic process in its early stages of progression in these hemispheres. Studies have reported development of symptomatic cerebrovascular events in 18% to 33% of initially asymptomatic adult MMD patients within 5 years of follow‐up. ¹² , ¹³ Given the excellent results of BHS in asymptomatic hemispheres, future investigation of monotherapy with BHS as an early preventive intervention in adults with progressive MMD might be considered.

We found that hemispheres with a baseline history of cerebral infarction or hemorrhage were less likely to develop neovascularization following BHS. Similar findings have been reported by previous studies of indirect revascularization in MMD. ⁴ , ¹⁴ It is thought that the need for blood flow may be reduced at the areas of damaged cerebral parenchyma, even at the sites showing hypovascularity on the DSA, because the available blood flow is sufficient for the remaining viable neural tissue. A reduced need for blood flow will translate into a decreased rate of neovascularization because of downregulation of angiogenic factors.

Our analysis revealed that patients who did not develop neovascularization at burr‐hole locations were significantly older than those who did (55.7±11.3 versus 40.2±10.5 years‐old; P<0.01). It is thought that indirect revascularization procedures are less likely to be effective in adult patients with MMD compared with pediatric patients. ³ A recent analysis of 231 hemispheres in patients aged 3 to 61 years who underwent indirect revascularization revealed that increasing age was a significant predictor of poor angiographic outcomes in patients with hemorrhagic onset. ⁴ The current study demonstrates that combined encephaloduroarteriosynangiosis and BHS surgery is associated with excellent outcomes at least in younger adults with a mean age of around 40. The poorer intrinsic neovascularization capability in adult patients is another rationale for addition of burr holes to standard indirect procedures, aiming to maximize revascularization odds via increasing the number of sources for neoangiogenesis.

This was a case series study with several limitations. First, we did not perform cerebral perfusion imaging studies as part of the follow‐up of our patients. Another limitation of the study is lack of long‐term angiographic follow‐up of the treated patients. Although neovascularization at 1 year is robust, further collateral vessel formation at burr hole or encephaloduroarteriosynangiosis sites may be observed if patients are followed up for a longer period (Figure 4). The number of cases was limited, which may have caused the study to be statistically underpowered to detect possible significant associations of outcomes with baseline and follow‐up demographic and angiographic variables. Finally, the limited number of patients treated with encephaloduroarteriosynangiosis alone or direct bypass in our center did not allow for comparison of the outcomes of encephaloduroarteriosynangiosis+BHS with these other therapeutic options. In light of the evidence of additional BHS‐induced neovascularization as provided by this study, future prospective comparative studies are warranted to further establish superior outcomes of this treatment approach.

Figure 4.

External carotid artery angiograms before (A), 14 months after (B), and 50 months after (C and D) the treatment. The image obtained 50 months after treatment (C) shows robust neovascularization at the site of the anterior burr hole (arrowhead) and encephaloduroarteriosynangiosis (circle), which have significantly increased compared with the images obtained at 14 months (B). Coronal view (D) shows pial collaterals from the left middle meningeal artery distal branches in the falx cerebri and crossing over to the right frontal burr hole and supplying contralateral cerebral cortex (arrowheads).

Conclusions

We describe a series of 16 adult patients with MMD treated with a combined indirect revascularization approach, using encephaloduroarteriosynangiosis in conjunction with anterior and posterior burr holes. We found that BHS provides additional neovascularization in the majority of cases, even in hemispheres that failed to develop satisfactory neoangiogenesis following encephaloduroarteriosynangiosis. This treatment strategy was not associated with any complications. We suggest that BHS be added as a standard method of treatment, in adjunction to other indirect or direct revascularization techniques such as encephaloduroarteriosynangiosis, for treatment of adult MMD.

Sources of Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not‐for‐profit sectors.

Disclosures

None.