Acta Neurochir (2015) 157:29–36 DOI 10.1007/s00701-014-2282-7
CLINICAL ARTICLE - VASCULAR
Surgical anatomy and preservation of the middle meningeal artery during bypass surgery for moyamoya disease Satoshi Hori & Daina Kashiwazaki & Naoki Akioka & Tomohide Hayashi & Emiko Hori & Kimiko Umemura & Yukio Horie & Satoshi Kuroda
Received: 4 September 2014 / Accepted: 13 November 2014 / Published online: 28 November 2014 # Springer-Verlag Wien 2014
Abstract Background The middle meningeal artery (MMA) is known to function as one of the important collateral routes in moyamoya disease. However, the anterior branch frequently courses within the lesser wing of the sphenoid bone and can easily be damaged during craniotomy for bypass surgery. This prospective study aimed to study the surgical anatomy of the MMA and to establish the technique to preserve it during bypass surgery for moyamoya disease. Methods Twenty-two patients with moyamoya disease underwent STA-MCA anastomosis combined with indirect bypass on 27 sides. The anatomical relationship between the anterior branch of the MMA and lesser wing was classified into three types: the bridge, monorail, and tunnel types. During surgery, the lesser wing was carefully resected with a rongeur or high-speed diamond drill to preserve the anterior branch of the MMA. Results The anterior branch of the MMA was classified into the bridge type in 5 sides (18.5 %), monorail type in 10 sides (37.0 %), and tunnel type in 12 sides (44.5 %). Patient age was closely related to the anatomical findings (χ2 test, p=0.0168). Careful resection of the lesser wing with a rongeur could preserve bridge- and monorail-type MMAs (100 and 71.4 %, respectively). However, drilling out of the lesser wing under a surgical microscope was essential to preserve the tunnel-type MMA. Intraoperative indocyanine green
S. Hori (*) : D. Kashiwazaki : N. Akioka : T. Hayashi : S. Kuroda Department of Neurosurgery, Graduate School of Medicine and Pharmacological Science, University of Toyama, 2630 Sugitani, Toyama 930-0194, Japan e-mail: [email protected] S. Hori : E. Hori : K. Umemura : Y. Horie Department of Neurosurgery, Stroke Center, Saiseikai Toyama Hospital, Toyama, Japan
videoangiography was useful to confirm patency during surgery. Conclusions It is essential to understand the surgical anatomy of the MMA around the pterion in order to preserve its anterior branch during bypass surgery for moyamoya disease. Keywords Moyamoya disease . Bypass surgery . Middle meningeal artery . Sphenoid bone
Introduction Moyamoya disease is an uncommon cerebrovascular disease characterized by progressive occlusion of the terminal portion of the internal carotid artery and its main branches within the circle of Willis. This occlusion results in the formation of a fine vascular network (moyamoya vessels) at the base of the brain [1, 2]. Clinical features of moyamoya disease differ substantially between children and adults. Most pediatric patients with moyamoya disease develop a transient ischemic attack (TIA) or cerebral infarction, whereas about half of adult patients develop intracranial bleeding, and the other half develop TIA or cerebral infarction [1]. Nowadays, it is well known that surgical revascularization improves the cerebral hemodynamics and prevents further ischemic and hemorrhagic stroke [3–7]. Surgical procedures for moyamoya disease can be classified into three categories: direct bypass, indirect bypass, and combined bypass. Direct bypass procedures are represented by superficial temporal artery to middle cerebral artery (STA-MCA) anastomosis. Direct bypass is useful to improve the cerebral hemodynamics and resolve ischemic attacks immediately after surgery. The frequency of postoperative ischemic stroke is lower after direct or combined bypass than it is after indirect bypass. Surgical procedures for indirect bypass are characteristic for moyamoya disease. Indirect bypass surgery that induces spontaneous angiogenesis between
30
the brain surface and vascularized donor tissues is technically simple to do and has been widely used. The superficial temporal artery (STA), dura mater, temporal muscle, and galeal tissue have been used as the pediculate donor tissues [1]. The middle meningeal artery (MMA) can provide important collateral flow through the dura mater. Especially, its anterior (frontal) branch provides collateral blood flow to the anterior cerebral artery (ACA) territory through the falx [8, 9]. On the other hand, the MMA 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 the sphenoid. Thereafter, it is divided into an anterior and posterior branch at a variable point [10, 11]. It is well known that the course of the anterior branch of the MMA around the pterion is not simple [11]. Ma et al. (2012) precisely analyzed the bone structure around the pterion and found that the vascular marking of the MMA consisted of a groove in 30 %, a complete canal in 49 %, and a disrupted or partial canal in the remainder [12]. Shimizu et al. (2008) also reported that the MMA pierced the tunnel located on the temporal side of the lesser wing of the sphenoid bone in about 75 % of adults [13]. However, no study has precisely analyzed the relationship between the MMA and pterion from the surgical point of view, although conventional frontotemporal craniotomy may easily damage the MMA during bypass surgery for moyamoya disease. To avoid this problem, the authors modified the craniotomy technique, but could not always preserve the MMA [4, 9]. This study, therefore, aimed to precisely analyze the anatomical relationship between the MMA and sphenoid bone and to develop a surgical technique to preserve the MMA during bypass surgery for moyamoya disease.
Methods Patients This prospective study included a total of 22 patients who underwent surgical revascularization for moyamoya disease between April 2012 and March 2014 at Toyama University Hospital and its affiliated hospital. All of them were diagnosed with moyamoya disease based on the guideline for the diagnosis of moyamoya disease set by the Research Committee on Moyamoya Disease (spontaneous occlusion of the circle of Willis) of the Ministry of Health, Welfare and Labor of Japan [14]. There were 9 children and 13 adults, 8 males and 14 females. Mean age was 12.8±5.0 and 40.4±11.9 years in pediatric and adult patients, respectively. In pediatric patients, clinical presentation included TIAs in five, ischemic stroke in two, and headache in two. In adult patients, clinical presentation included TIAs in four, ischemic stroke in three, and
Acta Neurochir (2015) 157:29–36
hemorrhagic stroke in six (Table 1). All patients provided informed consent, and their identity was protected. Radiological examinations Using a 1.5-T MR apparatus, time-of-flight (TOF) MR angiography was performed in all patients before surgery. The anatomical relationship between the anterior branch of the MMA and lesser wing of the sphenoid bone was precisely analyzed on the raw images of TOF-MR angiography. Plain CT scans were also performed to visualize the bony groove or tunnel around the pterion in all patients. Cerebral angiography and/or MR angiography was employed to evaluate the blood flow in the anterior branch of the MMA in all patients at 3 to 4 months after surgery. Surgical treatment Surgical revascularization was performed on a total of 27 sides, including 11 and 16 hemispheres in 9 pediatric and 13 adult patients, respectively. All patients underwent superficial temporal artery to middle cerebral artery (STA-MCA) anastomosis combined with indirect synangiosis, encephalo-duromyo-arterio-pericranial synangiosis (EDMAPS) [4]. As shown in Fig. 1, the frontal and parietal branches of the STA were dissected from the scalp under a surgical microscope (Fig. 1a). The temporal muscle and frontal pericranium were dissected as the vascularized flaps for the indirect bypass (Fig. 1b). To perform large frontotemporal craniotomy, five burr holes were made (Fig. 1c). The burr hole at the center of craniotomy site was made rostral to the pterion to preserve the anterior branch of the MMA, because it is known to pierce the bony tunnel of the middle meningeal groove just beneath the junction of the sphenoparietal, sphenosquamosal, and squamosal sutures [13]. A heart-shaped craniotomy was performed, preserving the lesser wing of the sphenoid bone (Fig. 1d). Then, the lesser wing was carefully resected, preserving the anterior branch of the MMA, using a rongeur or high-speed drill (see below). The dura was incised and rolled back, preserving the main branches of the MMA. One or two branches of the STA were anastomosed to the cortical branches of the MCA in an end-toside fashion with 10-0 or 11-0 nylon threads. The clamping time of the recipient was approximately 20 to 30 min. Furthermore, the anastomosed STA grafts were attached onto the brain surface as long as possible, which can induce indirect angiogenesis between them. The dural flaps were turned into the epiarachnoid space (Fig. 1f). Then, the brain surface was covered, using the temporal muscle and frontal pericranium (Fig. 1g). The patency of the anterior branch of the MMA was confirmed in all patients, using indocyanine green (ICG)
Acta Neurochir (2015) 157:29–36 Table 1
31
Characteristics of the patients with moyamoya disease MMA
Patient no.
Age/sex
Onset type
Operation
Type
Drill
Preservation
1 2 3 4
4/F 47/F 39/M 31/F 31/F 14/M 10/M 10/M 42/F 12/F 26/M 26/M 27/F 51/M
CI CI ICH, IVH IVH IVH TIA CI CI CI TIA TIA TIA TIA CI
Right STA-MCA (S)+EDMAPS Right STA-MCA (D)+EDMAPS Right STA-MCA (S)+EDMAPS Right STA-MCA (S)+EDMAPS Left STA-MCA (S)+EDMAPS Left STA-MCA (S)+EDMAPS Left STA-MCA (D)+EDMAPS Right STA-MCA (D)+EDMAPS Left STA-MCA (D)+EDMAPS Left STA-MCA (S)+EDMAPS Right STA-MCA (S)+EDMAPS Left STA-MCA (S)+EDMAPS Left STA-MCA (S)+EDMAPS Left STA-MCA (D)+EDMAPS
Bridge Tunnel Tunnel Tunnel Tunnel Bridge Monorail Tunnel Tunnel Monorail Monorail Bridge Monorail Monorail
− − − − − − − + + − − − − +
+ − − − − + − + + + + + − +
38/F 15/F 46/F 16/M 45/F 28/F 29/F 69/F 49/F 18/M 18/M 7/M 19/F
TIA TIA SAH headache ICH TIA TIA ICH, IVH ICH TIA TIA headache TIA
Left STA-MCA (S)+EDMAPS Left STA-MCA (D)+EDMAPS Left STA-MCA (D)+EDMAPS Right STA-MCA (D)+EDMAPS Right STA-MCA (D)+EDMAPS Left STA-MCA (S)+EDMAPS Right STA-MCA (S)+EDMAPS Right STA-MCA (D)+EDMAPS Right STA-MCA (S)+EDMAPS Left STA-MCA (S)+EDMAPS Right STA-MCA (S)+EDMAPS Left STA-MCA (D)+EDMAPS Left STA-MCA (D)+EDMAPS
Tunnel Monorail Tunnel Tunnel Monorail Monorail Tunnel Tunnel Bridge Tunnel Monorail Bridge Monorail
− − + + − − + + − + + − +
− + + + + + + + + + + + +
5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22
MMA=middle meningeal artery; CI=cerebral infarction; ICH=intracerebral hemorrhage; IVH=intraventricular hemorrhage; TIA=transient ischemic attack; SAH=subarachnoid hemorrhage; STA=superficial temporal artery; MCA=middle cerebral artery; S=single; D=double; EDMAPS=encephaloduro-myo-arterio-pericranial synangiosis
videoangiography during surgery and/or postoperative cerebral angiography.
looks like a tunnel. The bony tunnel is usually complete, but is deformed in some cases.
Surgical anatomy of the MMA In this study, the anatomical relationship between the anterior branch of the MMA and lesser wing of the sphenoid bone was classified into three types: the bridge, monorail, and tunnel types (Fig. 2). In the bridge type, the anterior branch of the MMA runs within the shallow groove in the medial surface of the bone, which looks like a bridge over a river. In the monorail type, the anterior branch of the MMA runs within the deep groove in the medial surface of the bone, which looks like a monorail vehicle over a rail. In the tunnel type, the anterior branch of the MMA is completely enclosed within the bony canal in the lesser wing of the sphenoid bone, which
Results Based on intraoperative observations, the anterior branch of the MMA was classified as the bridge type in 5 sides (18.5 %), monorail type in 10 sides (37.0 %), and tunnel type in 12 sides (44.5 %). The findings correlated very well with preoperative CT and MR angiography in all patients (Fig. 2). Patient age was closely related to the anatomical relationship between the anterior branch of the MMA and lesser wing of the sphenoid bone (Fig. 3). There was a significant difference between them when the patients were divided into two
32
Acta Neurochir (2015) 157:29–36
Acta Neurochir (2015) 157:29–36
33
Fig. 1
Intraoperative photographs show the step-by-step procedures of superficial temporal artery to middle cerebral artery (STA-MCA) anastomosis and encephalo-duro-myo-arterio-pericranial synangiosis (EDMAPS). a Following the curved skin incision, the frontal (*) and parietal branches of the STA (**) are dissected under a surgical microscope. b The temporal muscle (M) and frontal pericranium (P) are dissected from the skull and preserved as the vascularized flaps. c The burr hole just rostral to the pterion (arrow) is made to locate the anterior branch of the middle meningeal artery (MMA). d Heart-shaped frontotemporal craniotomy is performed, leaving the lesser wing of the sphenoid bone intact (arrow). Note the wide extension of the craniotomy to the frontal area. e The lesser wing of the sphenoid bone is carefully resected with a rongeur or high-speed diamond drill to preserve the anterior branch of the MMA (arrow). f The dura mater is opened, keeping the main branches of the MMA intact. The frontal branch of the STA is anastomosed to the cortical branch of the MCA. The dural pedicles are turned into the epiarachnoid space. g The dural windows are closed with the temporal muscle (M) and frontal pericranium (P)
Fig. 3 Column graph shows the relationship between patient age and anatomical findings of the anterior branch of the MMA around the pterion
groups: the patients younger than 30 years and those older (χ2 test, p=0.0168). Table 2 summarizes the relationship between the anatomy of the MMA branch and its preservation during craniotomy. It was quite easy to preserve the bridge-type anterior branch of the MMA by piecemeal resection of the lesser wing of the sphenoid bone with a rongeur. The bridge-type MMA branch could be preserved during surgery in all five sides (Fig. 4a–c). Careful piece-by-piece resection of the lesser wing with a rongeur was essential to preserve monorail-type MMAs, because the MMA
branch was tightly attached to the cranium inside the groove. As a result, the monorail-type MMA branch could be preserved in five (71.4 %) of seven sides when a rongeur was used to remove the lesser wing. However, it was quite easy to preserve the monorail-type MMA branch in all three sides (100 %) when the lesser wing was carefully drilled out using a high-speed diamond drill. On the other hand, the tunnel-type MMA branches could not be preserved in spite of careful bone resection with a rongeur because they were tightly attached to the entirely surrounding bone. Therefore, the lesser wing was
Fig. 2 The anatomical relationship between the anterior branch of the MMA and lesser wing of the sphenoid bone is classified into the bridge (a), monorail (b), or tunnel type (c). Upper panels demonstrate the representative findings of the plain CT scan in each type. Arrows show a shallow groove (a), deep groove (b), and bony tunnel (c). The middle panels show the representative findings of raw images on time-of-flight MR angiography in each type. Arrows indicate the flow signal of the anterior branch of the MMA. Lower panels show figurative photographs of each type
34 Table 2
Acta Neurochir (2015) 157:29–36 The rate of preservation of the MMA using a high-speed drill
Type
N (%)
Drill
Preservation (%)
Bridge Monorail
5 (18.5) 7 (25.9) 3 (11.1) 5 (18.5) 7 (25.9)
− − + − +
5 (100) 5 (71.4) 3 (100) 0 (0.0) 7 (100)
Tunnel
drilled out to preserve tunnel-type MMAs using a high-speed diamond drill, which made it possible to preserve it in all seven sides (Fig. 4d–f). The patency of the anterior branch of the MMA could easily be confirmed using intraoperative ICG videoangiography. Postoperative cerebral angiography and/or MR angiography could also evaluate it in all patients (Fig. 5). The results show that no ischemic stroke occurred within 7 days after surgery. In addition, no patients experienced any ischemic or hemorrhagic stroke during a mean follow-up period of 16 months.
Discussion This study clearly demonstrates a significant anatomical variation of the anterior branch of the MMA around the pterion among patients with moyamoya disease. The anterior branch of the MMA ran just within the middle meningeal groove in 15 (55.6 %) of 27 sides. The groove was quite shallow in 5/15 (bridge type), but deep in 10/15 (monorail type). On the other hand, the anterior branch of the MMA penetrated the bony tunnel in the lesser wing of the sphenoid bone in the other 12 Fig. 4 Intraoperative photographs demonstrate surgical techniques to resect the lesser wing of the sphenoid bone after heart-shaped frontotemporal craniotomy with a rongeur (a-c) or high-speed diamond drill (d-f)
(44.4 %) of 27 sides. The finding differs greatly from those in previous studies. For example, Shimizu et al. (2008) found 59 tunnels on 78 sides (75.6 %). Ma et al. (2012) also reported that the vascular marking for the anterior branch of the MMA consisted of a groove in 30 % of 152 sides and a tunnel in the other 70 %. Age differences of the samples in each study may explain this discrepancy. Thus, these previous studies analyzed only adult skulls. However, the present study included 9 children and 13 adults with moyamoya disease. In fact, statistical analysis reveals a significant difference in the anatomical relationship between patients younger than 30 years and those older. Therefore, the bony tunnel may develop with growth, although there are no previous studies on this issue. From the viewpoint of surgical revascularization for moyamoya disease, this study provides novel information on developing a surgical technique to preserve the anterior branch of the MMA, which can provide important collateral flow to the ACA territory. As reported previously, a heart-shaped craniotomy with a burr hole rostral to the pterion can make it easy to preserve the anterior branch of the MMA during craniotomy in all patients with moyamoya disease [4, 9]. As the next step, in order to preserve the anterior branch of the MMA when resecting the lesser wing of the sphenoid, it is essential to recognize the anatomical relationship between them. In this study, based on our experience, their relationships were classified into three types: the bridge, monorail, and tunnel. In all patients with bridge-type MMA, the resection of the lesser wing with a ronguer preserved it quite easily. In a majority of patients with monorail-type MMA, careful and piecemeal resection with a rongeur could preserve it, although it was sometimes impossible, especially when the middle meningeal groove was very deep. In this study, it was difficult to preserve tunnel-type
Acta Neurochir (2015) 157:29–36
35
Fig. 5 White-light (a) and near infrared photographs (b) during surgery reveal that intraoperative ICG videoangiography can visualize the blood flow in the preserved MMA (arrowheads) as well as the STA-MCA anastomosis (*). Anteroposterior (c) and lateral (d) projection of postoperative external carotid angiography demonstrates that the anterior branch of the MMA is preserved and supplies blood flow to the anterior cerebral artery territory (arrows). Postoperative MR angiography (e) reveals that the STA (*), MMA (arrowhead), and the deep temporal artery (arrow) are patent 4 months after surgery
MMA when resecting the lesser wing with a rongeur, mainly because of the long (~15 mm) bony tunnel, despite the small caliber of the MMA [10]. On the other hand, it was possible to preserve it when resecting with a high-speed diamond drill under a surgical microscope. The resection of the lesser wing of the sphenoid is essential to performing STA-MCA double anastomosis targeted to the frontal and temporal branches of the MCA and to yield a wide attachment between the temporal lobe and temporal muscle, an important donor tissue for an indirect bypass. The clinical significance of the surgical technique in this study is still obscure. However, it is valuable to maintain the cerebral hemodynamics in the frontal lobe, especially in pediatric patients, because they are at higher risk for poor intellectual outcome [15]. Longer follow-up study in a larger cohort is warranted to evaluate this hypothesis. In this study, the anatomical relationship between the anterior branch of the MMA and lesser wing of the sphenoid bone
could be evaluated using MR angiography or 3D-CTA. These less invasive modalities allowed us to anticipate it before surgery. In addition, ICG videoangiography was quite useful to evaluate whether the anterior branch of the MMA could be preserved or not during surgery. The findings on ICG videoangiography correlated very well with postoperative cerebral angiography and/or MR angiography. MR angiography can easily visualize the increased calibers of the branches of the external carotid artery that participate in surgical collaterals. The branches include the STA, MMA, and deep temporal artery (DTA), which normally supply the blood flow to the temporal muscle [16]. In this study, postoperative radiological examinations were performed 3 to 4 months after surgery. The results showed that MR angiography clearly revealed all of these branches increased their calibers by providing collateral blood flow through the indirect bypass after surgery as well as confirmed the patency of the anastomosis.
36
Acta Neurochir (2015) 157:29–36
Conclusion It is essential to understand the surgical anatomy of the MMA around the pterion in order to preserve its anterior branch during surgery because it can potentially function as important collaterals to the ACA territory in moyamoya disease. Bridge and monorail-type MMA can be preserved by carefully resecting the lesser wing of the sphenoid bone. However, the lesser wing should be drilled out with a high-speed diamond drill under a surgical microscope to preserve the tunnel-type MMA. Pre-, intra-, and postoperative imaging modalities such as MR angiography, 3D-CTA, ICG videoangiography, and cerebral angiography are quite useful to evaluate the surgical anatomy and preservation of MMA during bypass surgery for moyamoya disease.
9.
10.
11. 12.
13.
14. Acknowledgments This study was partly supported by a grant from the Research Committee on Moyamoya Disease sponsored by the Ministry of Health, Labor, and Welfare of Japan.
15.
Conflict of interest None 16.
References 1. Kuroda S, Houkin K (2008) Moyamoya disease: current concepts and future perspectives. Lancet Neurol 7:1056–1066 2. Suzuki J, Takaku A (1969) Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288–299 3. Karasawa J, Touho H, Ohnishi H, Miyamoto S, Kikuchi H (1992) Long-term follow-up study after extracranial-intracranial bypass surgery for anterior circulation ischemia in childhood moyamoya disease. J Neurosurg 77:84–89 4. Kuroda S, Houkin K, Ishikawa T, Nakayama N, Iwasaki Y (2010) Novel bypass surgery for moyamoya disease using pericranial flap: its impacts on cerebral hemodynamics and long-term outcome. Neurosurgery 66:1093–1101 5. Matsushima T, Inoue K, Kawashima M, Inoue T (2012) History of the development of surgical treatments for moyamoya disease. Neurol Med Chir (Tokyo) 52:278–286 6. Miyamoto S, Akiyama Y, Nagata I, Karasawa J, Nozaki K, Hashimoto N, Kikuchi H (1998) Long-term outcome after STAMCA anastomosis for moyamoya disease. Neurosurg Focus 5:e5 7. Mukawa M, Nariai T, Matsushima Y, Tanaka Y, Inaji M, Maehara T, Aoyagi M, Ohno K (2012) Long-term follow-up of surgically treated juvenile patients with moyamoya disease. J Neurosurg Pediatr 10: 451–456 8. Dusick JR, Gonzalez NR, Martin NA (2011) Clinical and angiographic outcomes from indirect revascularization surgery for
moyamoya disease in adults and children: a review of 63 procedures. Neurosurgery 68:34–43, discussion 43 Kuroda S, Houkin K (2012) Bypass surgery for moyamoya disease— concept and essence of surgical technique. Neurol Med Chir (Tokyo) 52:287–294 Harthmann da Silva T, Ellwanger JH, Silva HT, Moraes D, Dotto AC, Viera Vde A, de Campos D (2013) Morphometric analysis of the middle meningeal artery organization in humans— embryological considerations. J Neurol Surg Part B, Skull base 74: 108–112 Plummer SC III (1896) Research on the surgical anatomy of the middle meningeal artery. Ann Surg 23:540–572 Ma S, Baillie LJ, Stringer MD (2012) Reappraising the surface anatomy of the pterion and its relationship to the middle meningeal artery. Clin Anat 25:330–339 Shimizu S, Hagiwara H, Utsuki S, Oka H, Nakayama K, Fujii K (2008) Bony tunnel formation in the middle meningeal groove: an anatomic study for safer pterional craniotomy. Minim Invasive Neurosurg 51:329–332 Research Committee on the Pathology and Treatment of Spontaneous Occlusion of the Circle of Willis (2012) Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo) 52:245–266 Kuroda S, Houkin K, Ishikawa T, Nakayama N, Ikeda J, Ishii N, Kamiyama H, Iwasaki Y (2004) Determinants of intellectual outcome after surgical revascularization in pediatric moyamoya disease: a multivariate analysis. Childs Nerv Syst 20:302–308 Houkin K, Nakayama N, Kuroda S, Ishikawa T, Nonaka T (2004) How does angiogenesis develop in pediatric moyamoya disease after surgery? A prospective study with MR angiography. Childs Nerv Syst 20:734–741
Comments This is an important article about preservation of the MMA frontal branch at the time of craniotomy during the STA-MCA bypass surgery for Moyamoya disease. The meaning of this preservation is to protect the collateral circulation to the anterior cerebral artery ACA via the connecting vasculature of the Falx cerebri, as the paper indicates. The perfusion territory of the ACA is considered to be important for the intellectual development and its maintenance. On the other hand, direct STA-ACA bypass would come into question although this topic has not been discussed in the article : How to perform the STA-ACA bypass? , preservation of the MMA towards the midline at the time of craniotomy for the bypass, and so on. With the addition of the latter the article would have been more interesting and exciting. Y.Yonekawa Kyoto, Japan Reference: Yonekawa Y (2009) Brain revascularization by extracranial-intracranial arterial bypass In Sindou M (ed.): Practical Handbook of Neurosurgery, Springer, Vol 1 pp355-381
CLINICAL ARTICLE - VASCULAR
Surgical anatomy and preservation of the middle meningeal artery during bypass surgery for moyamoya disease Satoshi Hori & Daina Kashiwazaki & Naoki Akioka & Tomohide Hayashi & Emiko Hori & Kimiko Umemura & Yukio Horie & Satoshi Kuroda
Received: 4 September 2014 / Accepted: 13 November 2014 / Published online: 28 November 2014 # Springer-Verlag Wien 2014
Abstract Background The middle meningeal artery (MMA) is known to function as one of the important collateral routes in moyamoya disease. However, the anterior branch frequently courses within the lesser wing of the sphenoid bone and can easily be damaged during craniotomy for bypass surgery. This prospective study aimed to study the surgical anatomy of the MMA and to establish the technique to preserve it during bypass surgery for moyamoya disease. Methods Twenty-two patients with moyamoya disease underwent STA-MCA anastomosis combined with indirect bypass on 27 sides. The anatomical relationship between the anterior branch of the MMA and lesser wing was classified into three types: the bridge, monorail, and tunnel types. During surgery, the lesser wing was carefully resected with a rongeur or high-speed diamond drill to preserve the anterior branch of the MMA. Results The anterior branch of the MMA was classified into the bridge type in 5 sides (18.5 %), monorail type in 10 sides (37.0 %), and tunnel type in 12 sides (44.5 %). Patient age was closely related to the anatomical findings (χ2 test, p=0.0168). Careful resection of the lesser wing with a rongeur could preserve bridge- and monorail-type MMAs (100 and 71.4 %, respectively). However, drilling out of the lesser wing under a surgical microscope was essential to preserve the tunnel-type MMA. Intraoperative indocyanine green
S. Hori (*) : D. Kashiwazaki : N. Akioka : T. Hayashi : S. Kuroda Department of Neurosurgery, Graduate School of Medicine and Pharmacological Science, University of Toyama, 2630 Sugitani, Toyama 930-0194, Japan e-mail: [email protected] S. Hori : E. Hori : K. Umemura : Y. Horie Department of Neurosurgery, Stroke Center, Saiseikai Toyama Hospital, Toyama, Japan
videoangiography was useful to confirm patency during surgery. Conclusions It is essential to understand the surgical anatomy of the MMA around the pterion in order to preserve its anterior branch during bypass surgery for moyamoya disease. Keywords Moyamoya disease . Bypass surgery . Middle meningeal artery . Sphenoid bone
Introduction Moyamoya disease is an uncommon cerebrovascular disease characterized by progressive occlusion of the terminal portion of the internal carotid artery and its main branches within the circle of Willis. This occlusion results in the formation of a fine vascular network (moyamoya vessels) at the base of the brain [1, 2]. Clinical features of moyamoya disease differ substantially between children and adults. Most pediatric patients with moyamoya disease develop a transient ischemic attack (TIA) or cerebral infarction, whereas about half of adult patients develop intracranial bleeding, and the other half develop TIA or cerebral infarction [1]. Nowadays, it is well known that surgical revascularization improves the cerebral hemodynamics and prevents further ischemic and hemorrhagic stroke [3–7]. Surgical procedures for moyamoya disease can be classified into three categories: direct bypass, indirect bypass, and combined bypass. Direct bypass procedures are represented by superficial temporal artery to middle cerebral artery (STA-MCA) anastomosis. Direct bypass is useful to improve the cerebral hemodynamics and resolve ischemic attacks immediately after surgery. The frequency of postoperative ischemic stroke is lower after direct or combined bypass than it is after indirect bypass. Surgical procedures for indirect bypass are characteristic for moyamoya disease. Indirect bypass surgery that induces spontaneous angiogenesis between
30
the brain surface and vascularized donor tissues is technically simple to do and has been widely used. The superficial temporal artery (STA), dura mater, temporal muscle, and galeal tissue have been used as the pediculate donor tissues [1]. The middle meningeal artery (MMA) can provide important collateral flow through the dura mater. Especially, its anterior (frontal) branch provides collateral blood flow to the anterior cerebral artery (ACA) territory through the falx [8, 9]. On the other hand, the MMA 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 the sphenoid. Thereafter, it is divided into an anterior and posterior branch at a variable point [10, 11]. It is well known that the course of the anterior branch of the MMA around the pterion is not simple [11]. Ma et al. (2012) precisely analyzed the bone structure around the pterion and found that the vascular marking of the MMA consisted of a groove in 30 %, a complete canal in 49 %, and a disrupted or partial canal in the remainder [12]. Shimizu et al. (2008) also reported that the MMA pierced the tunnel located on the temporal side of the lesser wing of the sphenoid bone in about 75 % of adults [13]. However, no study has precisely analyzed the relationship between the MMA and pterion from the surgical point of view, although conventional frontotemporal craniotomy may easily damage the MMA during bypass surgery for moyamoya disease. To avoid this problem, the authors modified the craniotomy technique, but could not always preserve the MMA [4, 9]. This study, therefore, aimed to precisely analyze the anatomical relationship between the MMA and sphenoid bone and to develop a surgical technique to preserve the MMA during bypass surgery for moyamoya disease.
Methods Patients This prospective study included a total of 22 patients who underwent surgical revascularization for moyamoya disease between April 2012 and March 2014 at Toyama University Hospital and its affiliated hospital. All of them were diagnosed with moyamoya disease based on the guideline for the diagnosis of moyamoya disease set by the Research Committee on Moyamoya Disease (spontaneous occlusion of the circle of Willis) of the Ministry of Health, Welfare and Labor of Japan [14]. There were 9 children and 13 adults, 8 males and 14 females. Mean age was 12.8±5.0 and 40.4±11.9 years in pediatric and adult patients, respectively. In pediatric patients, clinical presentation included TIAs in five, ischemic stroke in two, and headache in two. In adult patients, clinical presentation included TIAs in four, ischemic stroke in three, and
Acta Neurochir (2015) 157:29–36
hemorrhagic stroke in six (Table 1). All patients provided informed consent, and their identity was protected. Radiological examinations Using a 1.5-T MR apparatus, time-of-flight (TOF) MR angiography was performed in all patients before surgery. The anatomical relationship between the anterior branch of the MMA and lesser wing of the sphenoid bone was precisely analyzed on the raw images of TOF-MR angiography. Plain CT scans were also performed to visualize the bony groove or tunnel around the pterion in all patients. Cerebral angiography and/or MR angiography was employed to evaluate the blood flow in the anterior branch of the MMA in all patients at 3 to 4 months after surgery. Surgical treatment Surgical revascularization was performed on a total of 27 sides, including 11 and 16 hemispheres in 9 pediatric and 13 adult patients, respectively. All patients underwent superficial temporal artery to middle cerebral artery (STA-MCA) anastomosis combined with indirect synangiosis, encephalo-duromyo-arterio-pericranial synangiosis (EDMAPS) [4]. As shown in Fig. 1, the frontal and parietal branches of the STA were dissected from the scalp under a surgical microscope (Fig. 1a). The temporal muscle and frontal pericranium were dissected as the vascularized flaps for the indirect bypass (Fig. 1b). To perform large frontotemporal craniotomy, five burr holes were made (Fig. 1c). The burr hole at the center of craniotomy site was made rostral to the pterion to preserve the anterior branch of the MMA, because it is known to pierce the bony tunnel of the middle meningeal groove just beneath the junction of the sphenoparietal, sphenosquamosal, and squamosal sutures [13]. A heart-shaped craniotomy was performed, preserving the lesser wing of the sphenoid bone (Fig. 1d). Then, the lesser wing was carefully resected, preserving the anterior branch of the MMA, using a rongeur or high-speed drill (see below). The dura was incised and rolled back, preserving the main branches of the MMA. One or two branches of the STA were anastomosed to the cortical branches of the MCA in an end-toside fashion with 10-0 or 11-0 nylon threads. The clamping time of the recipient was approximately 20 to 30 min. Furthermore, the anastomosed STA grafts were attached onto the brain surface as long as possible, which can induce indirect angiogenesis between them. The dural flaps were turned into the epiarachnoid space (Fig. 1f). Then, the brain surface was covered, using the temporal muscle and frontal pericranium (Fig. 1g). The patency of the anterior branch of the MMA was confirmed in all patients, using indocyanine green (ICG)
Acta Neurochir (2015) 157:29–36 Table 1
31
Characteristics of the patients with moyamoya disease MMA
Patient no.
Age/sex
Onset type
Operation
Type
Drill
Preservation
1 2 3 4
4/F 47/F 39/M 31/F 31/F 14/M 10/M 10/M 42/F 12/F 26/M 26/M 27/F 51/M
CI CI ICH, IVH IVH IVH TIA CI CI CI TIA TIA TIA TIA CI
Right STA-MCA (S)+EDMAPS Right STA-MCA (D)+EDMAPS Right STA-MCA (S)+EDMAPS Right STA-MCA (S)+EDMAPS Left STA-MCA (S)+EDMAPS Left STA-MCA (S)+EDMAPS Left STA-MCA (D)+EDMAPS Right STA-MCA (D)+EDMAPS Left STA-MCA (D)+EDMAPS Left STA-MCA (S)+EDMAPS Right STA-MCA (S)+EDMAPS Left STA-MCA (S)+EDMAPS Left STA-MCA (S)+EDMAPS Left STA-MCA (D)+EDMAPS
Bridge Tunnel Tunnel Tunnel Tunnel Bridge Monorail Tunnel Tunnel Monorail Monorail Bridge Monorail Monorail
− − − − − − − + + − − − − +
+ − − − − + − + + + + + − +
38/F 15/F 46/F 16/M 45/F 28/F 29/F 69/F 49/F 18/M 18/M 7/M 19/F
TIA TIA SAH headache ICH TIA TIA ICH, IVH ICH TIA TIA headache TIA
Left STA-MCA (S)+EDMAPS Left STA-MCA (D)+EDMAPS Left STA-MCA (D)+EDMAPS Right STA-MCA (D)+EDMAPS Right STA-MCA (D)+EDMAPS Left STA-MCA (S)+EDMAPS Right STA-MCA (S)+EDMAPS Right STA-MCA (D)+EDMAPS Right STA-MCA (S)+EDMAPS Left STA-MCA (S)+EDMAPS Right STA-MCA (S)+EDMAPS Left STA-MCA (D)+EDMAPS Left STA-MCA (D)+EDMAPS
Tunnel Monorail Tunnel Tunnel Monorail Monorail Tunnel Tunnel Bridge Tunnel Monorail Bridge Monorail
− − + + − − + + − + + − +
− + + + + + + + + + + + +
5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22
MMA=middle meningeal artery; CI=cerebral infarction; ICH=intracerebral hemorrhage; IVH=intraventricular hemorrhage; TIA=transient ischemic attack; SAH=subarachnoid hemorrhage; STA=superficial temporal artery; MCA=middle cerebral artery; S=single; D=double; EDMAPS=encephaloduro-myo-arterio-pericranial synangiosis
videoangiography during surgery and/or postoperative cerebral angiography.
looks like a tunnel. The bony tunnel is usually complete, but is deformed in some cases.
Surgical anatomy of the MMA In this study, the anatomical relationship between the anterior branch of the MMA and lesser wing of the sphenoid bone was classified into three types: the bridge, monorail, and tunnel types (Fig. 2). In the bridge type, the anterior branch of the MMA runs within the shallow groove in the medial surface of the bone, which looks like a bridge over a river. In the monorail type, the anterior branch of the MMA runs within the deep groove in the medial surface of the bone, which looks like a monorail vehicle over a rail. In the tunnel type, the anterior branch of the MMA is completely enclosed within the bony canal in the lesser wing of the sphenoid bone, which
Results Based on intraoperative observations, the anterior branch of the MMA was classified as the bridge type in 5 sides (18.5 %), monorail type in 10 sides (37.0 %), and tunnel type in 12 sides (44.5 %). The findings correlated very well with preoperative CT and MR angiography in all patients (Fig. 2). Patient age was closely related to the anatomical relationship between the anterior branch of the MMA and lesser wing of the sphenoid bone (Fig. 3). There was a significant difference between them when the patients were divided into two
32
Acta Neurochir (2015) 157:29–36
Acta Neurochir (2015) 157:29–36
33
Fig. 1
Intraoperative photographs show the step-by-step procedures of superficial temporal artery to middle cerebral artery (STA-MCA) anastomosis and encephalo-duro-myo-arterio-pericranial synangiosis (EDMAPS). a Following the curved skin incision, the frontal (*) and parietal branches of the STA (**) are dissected under a surgical microscope. b The temporal muscle (M) and frontal pericranium (P) are dissected from the skull and preserved as the vascularized flaps. c The burr hole just rostral to the pterion (arrow) is made to locate the anterior branch of the middle meningeal artery (MMA). d Heart-shaped frontotemporal craniotomy is performed, leaving the lesser wing of the sphenoid bone intact (arrow). Note the wide extension of the craniotomy to the frontal area. e The lesser wing of the sphenoid bone is carefully resected with a rongeur or high-speed diamond drill to preserve the anterior branch of the MMA (arrow). f The dura mater is opened, keeping the main branches of the MMA intact. The frontal branch of the STA is anastomosed to the cortical branch of the MCA. The dural pedicles are turned into the epiarachnoid space. g The dural windows are closed with the temporal muscle (M) and frontal pericranium (P)
Fig. 3 Column graph shows the relationship between patient age and anatomical findings of the anterior branch of the MMA around the pterion
groups: the patients younger than 30 years and those older (χ2 test, p=0.0168). Table 2 summarizes the relationship between the anatomy of the MMA branch and its preservation during craniotomy. It was quite easy to preserve the bridge-type anterior branch of the MMA by piecemeal resection of the lesser wing of the sphenoid bone with a rongeur. The bridge-type MMA branch could be preserved during surgery in all five sides (Fig. 4a–c). Careful piece-by-piece resection of the lesser wing with a rongeur was essential to preserve monorail-type MMAs, because the MMA
branch was tightly attached to the cranium inside the groove. As a result, the monorail-type MMA branch could be preserved in five (71.4 %) of seven sides when a rongeur was used to remove the lesser wing. However, it was quite easy to preserve the monorail-type MMA branch in all three sides (100 %) when the lesser wing was carefully drilled out using a high-speed diamond drill. On the other hand, the tunnel-type MMA branches could not be preserved in spite of careful bone resection with a rongeur because they were tightly attached to the entirely surrounding bone. Therefore, the lesser wing was
Fig. 2 The anatomical relationship between the anterior branch of the MMA and lesser wing of the sphenoid bone is classified into the bridge (a), monorail (b), or tunnel type (c). Upper panels demonstrate the representative findings of the plain CT scan in each type. Arrows show a shallow groove (a), deep groove (b), and bony tunnel (c). The middle panels show the representative findings of raw images on time-of-flight MR angiography in each type. Arrows indicate the flow signal of the anterior branch of the MMA. Lower panels show figurative photographs of each type
34 Table 2
Acta Neurochir (2015) 157:29–36 The rate of preservation of the MMA using a high-speed drill
Type
N (%)
Drill
Preservation (%)
Bridge Monorail
5 (18.5) 7 (25.9) 3 (11.1) 5 (18.5) 7 (25.9)
− − + − +
5 (100) 5 (71.4) 3 (100) 0 (0.0) 7 (100)
Tunnel
drilled out to preserve tunnel-type MMAs using a high-speed diamond drill, which made it possible to preserve it in all seven sides (Fig. 4d–f). The patency of the anterior branch of the MMA could easily be confirmed using intraoperative ICG videoangiography. Postoperative cerebral angiography and/or MR angiography could also evaluate it in all patients (Fig. 5). The results show that no ischemic stroke occurred within 7 days after surgery. In addition, no patients experienced any ischemic or hemorrhagic stroke during a mean follow-up period of 16 months.
Discussion This study clearly demonstrates a significant anatomical variation of the anterior branch of the MMA around the pterion among patients with moyamoya disease. The anterior branch of the MMA ran just within the middle meningeal groove in 15 (55.6 %) of 27 sides. The groove was quite shallow in 5/15 (bridge type), but deep in 10/15 (monorail type). On the other hand, the anterior branch of the MMA penetrated the bony tunnel in the lesser wing of the sphenoid bone in the other 12 Fig. 4 Intraoperative photographs demonstrate surgical techniques to resect the lesser wing of the sphenoid bone after heart-shaped frontotemporal craniotomy with a rongeur (a-c) or high-speed diamond drill (d-f)
(44.4 %) of 27 sides. The finding differs greatly from those in previous studies. For example, Shimizu et al. (2008) found 59 tunnels on 78 sides (75.6 %). Ma et al. (2012) also reported that the vascular marking for the anterior branch of the MMA consisted of a groove in 30 % of 152 sides and a tunnel in the other 70 %. Age differences of the samples in each study may explain this discrepancy. Thus, these previous studies analyzed only adult skulls. However, the present study included 9 children and 13 adults with moyamoya disease. In fact, statistical analysis reveals a significant difference in the anatomical relationship between patients younger than 30 years and those older. Therefore, the bony tunnel may develop with growth, although there are no previous studies on this issue. From the viewpoint of surgical revascularization for moyamoya disease, this study provides novel information on developing a surgical technique to preserve the anterior branch of the MMA, which can provide important collateral flow to the ACA territory. As reported previously, a heart-shaped craniotomy with a burr hole rostral to the pterion can make it easy to preserve the anterior branch of the MMA during craniotomy in all patients with moyamoya disease [4, 9]. As the next step, in order to preserve the anterior branch of the MMA when resecting the lesser wing of the sphenoid, it is essential to recognize the anatomical relationship between them. In this study, based on our experience, their relationships were classified into three types: the bridge, monorail, and tunnel. In all patients with bridge-type MMA, the resection of the lesser wing with a ronguer preserved it quite easily. In a majority of patients with monorail-type MMA, careful and piecemeal resection with a rongeur could preserve it, although it was sometimes impossible, especially when the middle meningeal groove was very deep. In this study, it was difficult to preserve tunnel-type
Acta Neurochir (2015) 157:29–36
35
Fig. 5 White-light (a) and near infrared photographs (b) during surgery reveal that intraoperative ICG videoangiography can visualize the blood flow in the preserved MMA (arrowheads) as well as the STA-MCA anastomosis (*). Anteroposterior (c) and lateral (d) projection of postoperative external carotid angiography demonstrates that the anterior branch of the MMA is preserved and supplies blood flow to the anterior cerebral artery territory (arrows). Postoperative MR angiography (e) reveals that the STA (*), MMA (arrowhead), and the deep temporal artery (arrow) are patent 4 months after surgery
MMA when resecting the lesser wing with a rongeur, mainly because of the long (~15 mm) bony tunnel, despite the small caliber of the MMA [10]. On the other hand, it was possible to preserve it when resecting with a high-speed diamond drill under a surgical microscope. The resection of the lesser wing of the sphenoid is essential to performing STA-MCA double anastomosis targeted to the frontal and temporal branches of the MCA and to yield a wide attachment between the temporal lobe and temporal muscle, an important donor tissue for an indirect bypass. The clinical significance of the surgical technique in this study is still obscure. However, it is valuable to maintain the cerebral hemodynamics in the frontal lobe, especially in pediatric patients, because they are at higher risk for poor intellectual outcome [15]. Longer follow-up study in a larger cohort is warranted to evaluate this hypothesis. In this study, the anatomical relationship between the anterior branch of the MMA and lesser wing of the sphenoid bone
could be evaluated using MR angiography or 3D-CTA. These less invasive modalities allowed us to anticipate it before surgery. In addition, ICG videoangiography was quite useful to evaluate whether the anterior branch of the MMA could be preserved or not during surgery. The findings on ICG videoangiography correlated very well with postoperative cerebral angiography and/or MR angiography. MR angiography can easily visualize the increased calibers of the branches of the external carotid artery that participate in surgical collaterals. The branches include the STA, MMA, and deep temporal artery (DTA), which normally supply the blood flow to the temporal muscle [16]. In this study, postoperative radiological examinations were performed 3 to 4 months after surgery. The results showed that MR angiography clearly revealed all of these branches increased their calibers by providing collateral blood flow through the indirect bypass after surgery as well as confirmed the patency of the anastomosis.
36
Acta Neurochir (2015) 157:29–36
Conclusion It is essential to understand the surgical anatomy of the MMA around the pterion in order to preserve its anterior branch during surgery because it can potentially function as important collaterals to the ACA territory in moyamoya disease. Bridge and monorail-type MMA can be preserved by carefully resecting the lesser wing of the sphenoid bone. However, the lesser wing should be drilled out with a high-speed diamond drill under a surgical microscope to preserve the tunnel-type MMA. Pre-, intra-, and postoperative imaging modalities such as MR angiography, 3D-CTA, ICG videoangiography, and cerebral angiography are quite useful to evaluate the surgical anatomy and preservation of MMA during bypass surgery for moyamoya disease.
9.
10.
11. 12.
13.
14. Acknowledgments This study was partly supported by a grant from the Research Committee on Moyamoya Disease sponsored by the Ministry of Health, Labor, and Welfare of Japan.
15.
Conflict of interest None 16.
References 1. Kuroda S, Houkin K (2008) Moyamoya disease: current concepts and future perspectives. Lancet Neurol 7:1056–1066 2. Suzuki J, Takaku A (1969) Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288–299 3. Karasawa J, Touho H, Ohnishi H, Miyamoto S, Kikuchi H (1992) Long-term follow-up study after extracranial-intracranial bypass surgery for anterior circulation ischemia in childhood moyamoya disease. J Neurosurg 77:84–89 4. Kuroda S, Houkin K, Ishikawa T, Nakayama N, Iwasaki Y (2010) Novel bypass surgery for moyamoya disease using pericranial flap: its impacts on cerebral hemodynamics and long-term outcome. Neurosurgery 66:1093–1101 5. Matsushima T, Inoue K, Kawashima M, Inoue T (2012) History of the development of surgical treatments for moyamoya disease. Neurol Med Chir (Tokyo) 52:278–286 6. Miyamoto S, Akiyama Y, Nagata I, Karasawa J, Nozaki K, Hashimoto N, Kikuchi H (1998) Long-term outcome after STAMCA anastomosis for moyamoya disease. Neurosurg Focus 5:e5 7. Mukawa M, Nariai T, Matsushima Y, Tanaka Y, Inaji M, Maehara T, Aoyagi M, Ohno K (2012) Long-term follow-up of surgically treated juvenile patients with moyamoya disease. J Neurosurg Pediatr 10: 451–456 8. Dusick JR, Gonzalez NR, Martin NA (2011) Clinical and angiographic outcomes from indirect revascularization surgery for
moyamoya disease in adults and children: a review of 63 procedures. Neurosurgery 68:34–43, discussion 43 Kuroda S, Houkin K (2012) Bypass surgery for moyamoya disease— concept and essence of surgical technique. Neurol Med Chir (Tokyo) 52:287–294 Harthmann da Silva T, Ellwanger JH, Silva HT, Moraes D, Dotto AC, Viera Vde A, de Campos D (2013) Morphometric analysis of the middle meningeal artery organization in humans— embryological considerations. J Neurol Surg Part B, Skull base 74: 108–112 Plummer SC III (1896) Research on the surgical anatomy of the middle meningeal artery. Ann Surg 23:540–572 Ma S, Baillie LJ, Stringer MD (2012) Reappraising the surface anatomy of the pterion and its relationship to the middle meningeal artery. Clin Anat 25:330–339 Shimizu S, Hagiwara H, Utsuki S, Oka H, Nakayama K, Fujii K (2008) Bony tunnel formation in the middle meningeal groove: an anatomic study for safer pterional craniotomy. Minim Invasive Neurosurg 51:329–332 Research Committee on the Pathology and Treatment of Spontaneous Occlusion of the Circle of Willis (2012) Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo) 52:245–266 Kuroda S, Houkin K, Ishikawa T, Nakayama N, Ikeda J, Ishii N, Kamiyama H, Iwasaki Y (2004) Determinants of intellectual outcome after surgical revascularization in pediatric moyamoya disease: a multivariate analysis. Childs Nerv Syst 20:302–308 Houkin K, Nakayama N, Kuroda S, Ishikawa T, Nonaka T (2004) How does angiogenesis develop in pediatric moyamoya disease after surgery? A prospective study with MR angiography. Childs Nerv Syst 20:734–741
Comments This is an important article about preservation of the MMA frontal branch at the time of craniotomy during the STA-MCA bypass surgery for Moyamoya disease. The meaning of this preservation is to protect the collateral circulation to the anterior cerebral artery ACA via the connecting vasculature of the Falx cerebri, as the paper indicates. The perfusion territory of the ACA is considered to be important for the intellectual development and its maintenance. On the other hand, direct STA-ACA bypass would come into question although this topic has not been discussed in the article : How to perform the STA-ACA bypass? , preservation of the MMA towards the midline at the time of craniotomy for the bypass, and so on. With the addition of the latter the article would have been more interesting and exciting. Y.Yonekawa Kyoto, Japan Reference: Yonekawa Y (2009) Brain revascularization by extracranial-intracranial arterial bypass In Sindou M (ed.): Practical Handbook of Neurosurgery, Springer, Vol 1 pp355-381
