|Year : 2018 | Volume
| Issue : 4 | Page : 83-87
Progress of diagnosis and surgical treatment in children with moyamoya disease
Hongbo Zhang1, Mengmeng Bai2, Zhiqi Chen1, Zhengliang Li1, Shizhong Zhang1, Wen Li3
1 Department of Neurosurgery, Zhujiang Hospital; The National Key Clinic Specialty, The Engineering Technology Research Center of Education Ministry of China, The Neurosurgery Institute of Guangdong Province, Guangdong Provincial Key Laboratory on Brain Function Repair and Regeneration, Southern Medical University, Guangzhou, Guangdong, China
2 Department of Graduate School, Chengde Medical University, Chengde, Hebei, China
3 Department of Pediatrics, Chengde Central Hospital, The Second Clinical College of Chengde Medical College, Chengde, Hebei, China
|Date of Submission||28-Nov-2018|
|Date of Acceptance||18-Dec-2018|
|Date of Web Publication||26-Dec-2018|
Prof. Shizhong Zhang
No. 253, Middle Industrial Road, Guangzhou 510280, Guangdong
Source of Support: None, Conflict of Interest: None
Moyamoya disease (MMD), also known as abnormal intracranial vascular network, is a group of chronic progressive stenosis or occlusion of bilateral main branches of Willis ring (siphon segment of internal carotid artery and anterior and middle cerebral arteries, sometimes including the origin of posterior cerebral artery), followed by abnormal collateral small vascular network. The disease is known as MMD because it presents many dense piles of small blood vessels that appear as “puff of smoke” on cerebral angiogram. At present, great progress has been made in the field of epidemiology, pathogenesis, clinical manifestations, diagnosis, and treatment of adult MMD. However, the disease characteristics considerably differ in children. Therefore, this article will review the diagnosis, treatment, and prognosis of MMD in children.
Keywords: Children, diagnosis, imaging, Moyamoya disease, surgery
|How to cite this article:|
Zhang H, Bai M, Chen Z, Li Z, Zhang S, Li W. Progress of diagnosis and surgical treatment in children with moyamoya disease. Transl Surg 2018;3:83-7
|How to cite this URL:|
Zhang H, Bai M, Chen Z, Li Z, Zhang S, Li W. Progress of diagnosis and surgical treatment in children with moyamoya disease. Transl Surg [serial online] 2018 [cited 2019 Dec 9];3:83-7. Available from: http://www.translsurg.com/text.asp?2018/3/4/83/248614
| Introduction|| |
Moyamoya disease (MMD) is a cerebrovascular disease characterized by progressive stenosis and occlusion of the distal end of the internal carotid artery, the middle cerebral artery (MCA), and the proximal end of the anterior cerebral artery (sometimes involving the posterior cerebral artery), usually accompanied by a large amount of tiny blood vessels, giving “puff of smoke” appearance at the base of the brain. The disease was first described by Shimizu and Bamboo in Japan in 1955 and was named by Suzuki in 1966.,, An epidemiological survey in 2003 showed that the morbidity of MMD in Japan was about 60.03/100,000. A regional epidemiological survey conducted in Hokkaido, Japan, in 2006, showed that the prevalence rate was about 105/100,000 and the incidence rate was about 0.94/100,000., Although the diagnosis and treatment of MMD is advancing, the efficiency still needs to be improved. Imaging for diagnosis and surgery for treatment are the most commonly chosen options so far. MMD in children is characterized by threatening symptoms such as ischemia, headache, seizures, and paralysis.
| Epidemiological Characteristics and Clinical Manifestations|| |
MMD is more common in Asia, particularly in China and Japan, and observed mostly among girls. It has two peaks; one in childhood and the other in adulthood, and a large number of studies have found that the proportion of children is higher than that of adults. It is most commonly observed in children aged under 10 years, with cerebral ischemia being the most common condition (61.2%), and in adults aged between 30 and 40 years,,, with cerebral hemorrhage (62.4%) being the most common condition.
The symptoms associated with cerebral ischemia were commonly observed in children with MMD compared to adults, and the symptoms associated with hemorrhagic stroke were relatively rare. Limb weakness and hemiplegia were the most common clinical manifestations in children. The incidence of transient ischemic attacks and epilepsy is significantly higher in children than in adults, and the course of MMD in children is repeated. Although headache is also one of the important clinical manifestations of children's MMD, most patients have irregular headache episodes, uncertain location, and no obvious symptoms.
| Imaging as a Diagnostic Tool|| |
At present, the diagnosis of MMD depends on imaging, besides considering the age and clinical manifestations in children. Computed tomography (CT), CT angiography (CTA), magnetic resonance imaging (MRI), magnetic resonance angiography (MRA), digital subtraction angiography (DSA), transcranial Doppler (TCD), electroencephalogram (EEG), and other imaging methods are widely used in clinic, and DSA is considered the “gold standard” for the diagnosis of this disease. In 1997, the MMD Research Committee of the Ministry of Health and Welfare of Japan put forward diagnostic guidelines. The radiological diagnostic criteria for MMD are as follows: stenosis or occlusion at the end of internal carotid artery, the beginning of MCA and anterior cerebral artery; abnormal vascular network near the occlusion, visible in the filling phase of basilar cranial artery; and bilateral involvement. All the above three conditions need to be satisfied, and the cardiovascular disease (CVD) caused by atherosclerosis, autoimmune diseases, various intracranial infections, brain tumors, Down's syndrome, neurofibromatosis, craniocerebral trauma, and head irradiation needs to be excluded.
Computed tomography and computed tomography angiography
CT scan can show cerebral infarction, cerebral hemorrhage, brain atrophy, and other changes and can also observe the pathological changes of brain parenchyma. However, due to its low specificity, it is easy to misdiagnose MMD under CT. CTA is a noninvasive angiographic technique, where the postprocessing technology, multi-planar reformation, volume rendering, and maximum intensity projection can make a definite diagnosis of children's MMD in time. Multislice spiral CT angiography (MSCTA) can be used to carry out a variety of image postprocessing techniques, such as multidimensional and stereoscopic observation of blood vessels, and to understand the relationship between pathological vessels and the surrounding brain tissue structure. MSCTA has the advantage of being noninvasive while reducing radiation exposure. The evaluation of the compensatory ability of collateral circulation and cerebral perfusion of smoky vessels is slightly insufficient, and thus CT cannot directly reflect the hemodynamic changes of MMD.,
Magnetic resonance imaging and magnetic resonance angiography
The application of MRI, MRA, MRV, and MRP provides a noninvasive method for the detection of pathological vessels in MMD, which can reflect the morphological manifestations of vessels, blood supply of brain tissue, and perfusion status of MMD. MRI is noninvasive, more sensitive, and more accurate in detecting the scope and location of infarction lesions. MRA can show the stenosis and occlusion of bilateral internal carotid artery and its branches in varying degrees and the formation of abnormal intracranial vascular network. When DSA cannot be performed, MRA can clearly show the following manifestations: stenosis or occlusion of the end segment of internal carotid artery and/or the beginning segment of anterior cerebral artery and MCA; abnormal vascular network in basal ganglia (MRI can show more than two obvious vascular flow empty shadows in ipsilateral basal ganglia); and bilateral presence of the lesions. Although MRI combined with MRA can show the lesions of MMD, MRA still has some limitations, such as display of blood vessels and being not suitable for claustrophobic patients. MRA can easily exaggerate the degree of stenosis, misjudge stenosis as occlusion, and show poor collateral circulation. Therefore, DSA is still necessary for those who are highly suspected of MMD and who have not been diagnosed or planned to undergo surgical treatment by MRA.
Digital subtraction angiography
DSA plays a very important role in the diagnosis of MMD. It can clarify the location, nature, and the compensation of collateral vascular blood supply in Wills circulation attacked and can also provide complete accurate vascular lesions information for later treatment. It is the gold standard for the diagnosis of MMD. However, it is not a preferred method because of its traumatic approach and limitation of examination conditions. The imaging features of DSA in the diagnosis of MMD in children are as follows: bilateral or unilateral end of internal carotid artery, stenosis or occlusion of MCA, and proximal segment of anterior cerebral artery at varying degrees, involving posterior cerebral artery; formation of abnormal vascular network of skull base; and formation of extensive collateral circulation. DSA can clearly show the compensatory blood supply of vertebrobasilar artery system, branches of external carotid artery, ophthalmic artery, dense and irregular smoky vascular network at the base of the brain, and secondary aneurysms. Some studies suggest that there is no significant difference in the risk of cerebral angiography in children with MMD, compared with other groups of CVD.
TCD, a noninvasive, easy-to-obtain method of blood flow detection, can directly detect the hemodynamic changes of blood vessels on the surface and skull base and is very suitable for real-time evaluation of blood flow velocity and spectrum shape of intracranial and extracranial vessels, reflecting the changes of cerebral hemodynamics. Therefore, TCD can also be used as an effective method to predict the efficacy of encephalo-duro-arterio-synangiosis (EDAS) surgery, which is of great significance to surgical interventions and prognostic evaluation.
It is suggested that more than 50% of children with MMD show a single-phase, slow-wave, high-pressure phase on EEG after overventilation, which may be due to the decrease of cerebral perfusion reserve. This EEG manifestation can be considered as a change in the clinical characteristics of children with MMD. However, the disadvantage of EEG is that it is impossible to quantify the detailed indicators of cerebral perfusion reserve.
Magnetic resonance perfusion imaging technology can be used to assess cerebral hemodynamic status in MMD patients. Single-photon emission CT (SPECT), positron emission tomography, CT perfusion, arterial spin-labeling (ASL), functional MRI (fMRI) based on oxygen level-dependent measurement, and other methods may also serve the purpose. Compared with DSA, SPECT is also considered the gold standard for diagnosing cerebrovascular reserve capacity. However, because of its radioactivity and low spatial resolution, SPECT is not preferred as the best choice for the diagnosis of CVD in children. ASL is a magnetic resonance technique developed in recent years to quantitatively analyze cerebral hemodynamics, without injecting contrast agent. Perfusion-weighted imaging and ASL can achieve the purpose of assessing cerebral vascular reserve without injecting exogenous vasodilators. Blood oxygenation level-dependent fMRI can adjust patients' carbon dioxide inhalation through a special mask device so as to evaluate patients' cerebrovascular responsiveness noninvasively. However, the examination takes a long time and the compliance of children with MMD will be challenged.
In conclusion, CT and MRI examination of MMD in children can clearly show the changes of brain parenchyma, such as cerebral hemorrhage, cerebral infarction, and the formation of encephalomalacia, caused by MMD. Moreover, MRI is more sensitive to the ischemic manifestations of MMD than CT. MRA still has some limitations, such as easy exaggeration of the degree of stenosis and misjudging stenosis as occlusion. DSA can clearly show the location of Willis ring lesions in children and evaluate collateral circulation and external carotid artery blood flow status. It is the golden standard for the diagnosis of MMD in children.
| Etiology and Pathological Diagnostic Basis|| |
Recently, research results on the etiology and pathology of MMD in children are also being reported, which is hoped to help in the diagnosis of the condition. We can probably find help from the following three aspects: genetic factors, cytokines, and environmental factors.
Some studies have found that the 3p, 6q, 17q, 8q23, and 12p12 loci of chromosome of patients with MMD have genetic linkage. In 2011, Kamada et al. discovered a major susceptibility gene related to MMD, RNF213 gene. It was found that P.R4859K mutation in RNF213 gene existed in 95% of familial and 79% of sporadic MMD patients. RNF213 gene knockout in zebrafish resulted in irregular formation of main artery wall and abnormal angiogenesis. It can be speculated that RNF213 gene may be involved in a new signal pathway related to intracranial angiogenesis, and its mechanism still needs further study. These genetic susceptibility factors may explain the high incidence, familial predisposition, and the combination of other genetic diseases in Asian countries, such as Japan and Korea.
Basic fibroblast growth factor
A large number of studies have confirmed that basic fibroblast growth factor (bFGF) has mitogen activity and can participate in the formation of new blood vessels, which may play an important role in the occurrence and development of MMD in children. Some scholars reported that the level of bFGF in CSF of patients with MMD increased significantly, especially in patients undergoing indirect revascularization. Other angiogenic factors (interleukin-8, platelet-derived growth factor, GF-beta, epidermal growth factor, and vascular endothelial growth factor) did not show significant changes.,
Astrocytes secrete vascular endothelial growth factor
Immunohistologic analysis of brain tissue of MMD patients by Sakamoto et al. revealed a significant increase in vascular endothelial progenitor cells (EPCs) (VECs). These EPCs were found to be involved in the recruitment of VECs and in the formation of collateral vessels in MMD.
Matrix metalloproteinases and other related cytokines
In 2009, Fujimura et al. found that the serum MMP-9 level in MMD patients was significantly higher than that in healthy control group, with no significant difference in MMP-2 levels between the groups. In addition, related studies have found that platelet-derived growth factor, hepatocyte growth factor, nitric oxide, EPCs, and serum microRNAs may also play an important role in the pathogenesis of MMD.,,
| Surgery|| |
The purpose of cerebrovascular reconstruction is to establish new anastomotic branches to improve the blood supply of ischemic brain tissue. Surgical treatment can effectively reduce ischemic effect and prevent mental retardation. According to previous reports, the incidence of stroke in asymptomatic children with MMD is 3.2% per year. Without active surgical treatment, 37% of the patients will show symptoms related to nervous system damage and 3% of the patients will die. This again emphasizes the necessity of active surgical treatment for children with MMD. However, a meta-analysis studying the effectiveness of various surgical treatments in 1448 patients from 57 studies published between 1966 and 2004 showed that the rates of patients receiving direct, indirect, and combined vascular reconstruction were 4%, 73%, and 23%, respectively, and there was no difference in the efficacy among these three surgical methods. On the contrary, the key factors for a good prognosis seem to be surgeon's experience and strict monitoring with meticulous care of children by medical institutions.,
As for the treatment of MMD, vascular reconstruction through surgery is generally considered to be an effective method. Early surgical treatment can reverse the course of the disease. However, there are no definite surgical indications and specific timing.
Direct revascularization can immediately improve cerebral blood flow and reduce neurological deficits. Specific surgical methods can be divided into: (1) superficial temporal artery-MCA (STA-MCA) branch anastomosis; (2) occipital artery-MCA branch anastomosis; and (3) occipital artery-posterior cerebral artery anastomosis. Among them, the STA-MCA is the most commonly used method in adults. However, in children, a high requirement for recipient and donor blood vessels and doctors' surgical skills limits the wide clinical application of STA-MCA.
Indirect revascularization can produce spontaneous vascular anastomosis and improve the blood supply to ischemic brain tissue. The cerebral cortex in the surgical area is in a hypoperfusion state, which is the basis for the growth of extracranial vessels on to the surface of the brain. The severer the cerebral cortex ischemia is, the faster the intracranial and extracranial vascular growth is. With MMD, ischemia worsens slowly and progressively and the indirect anastomosis gradually increases the blood supply to the intracranial vessels. Specific surgical methods can be divided into: (1) EDAS; (2) encephalo-muscular vascular fusion; (3) encephalo-duro-artero-myosynangiosis; (4) skull drilling, dural and arachnoid membranectomy, and omentum transplantation. Because the cerebral cortical artery and STA in children are slender and thin, direct vascular reconstruction is not only difficult to anastomose, but also easy to destroy the formed dural–cerebral collateral circulation, and the anastomosed vessels may undergo restenosis or occlusion due to the progress of the disease. The long-term effect is difficult to confirm. Therefore, EDAS is an effective method. Because of its simple operation, minimal trauma, and no damage to the original collateral circulation, it has become the preferred treatment for children scheduled for MMD surgery.,, Imai et al. studied 48 children with MMD, undergoing surgical treatment. It was found that only four patients had complications during the perioperative period and only one patient had recurrent transient ischemia. The other children showed good clinical effects. Guzman et al. tracked 96 children with MMD after operation (76.2% STA-MCA and 23.8% involving other indirect operations). It was found that only three children had poor prognosis 30 days after operation, while the other 93 children had a good prognosis. These reports suggest that indirect revascularization is not only effective, but also has a good prognosis. However, indirect revascularization also has its drawbacks, such as long duration of the surgery. Therefore, indirect revascularization is not recommended for emergencies requiring immediate improvement of blood circulation.
At present, combined revascularization is the trend in MMD treatment. It combines the advantages of both direct revascularization and indirect revascularization. It can not only improve blood supply to the ischemic brain as soon as possible, but also maximize the use of external carotid artery blood supply. Some authors divided the surgery scheduled for MMD children into EDAS group and EDAS combined with multipoint drilling group. After 6–17 months of follow-up, 69.05% of all the children's symptoms were improved. The improvement rate of EDAS group was 52.63% and that of EDAS combined with multipoint drilling group was 82.61%, suggesting the advantage of combination approach. The clinical prognosis of children with MMD was good and the improvement rate of EDAS combined with multipoint drilling of skull was more obvious, which shows the effectiveness of combined operation, and its long-term effect needs further study.
Other surgical methods and medical treatment
In addition to the above three surgical methods, the application of intravascular technology in the treatment of MMD and its related complications is also being explored. Recent reports have described attempts to use intravascular tools such as catheters to open stenotic vessels, but, unfortunately, the effect is not obvious. Of course, more data are needed to assess the acute effects of endovascular therapy (including angioplasty and the use of vasodilators and thrombolytics). Vasodilators and anticoagulants such as fasudil and aspirin can be used in the treatment of MMD, but the therapeutic effect is not ideal.
| Conclusion|| |
The diagnosis and treatment of MMD in children are still complex, and the selection and judgment of surgical strategies are also very important. Both of them play a decisive role in the prognosis of children with MMD. The etiology, pathology, and the diagnosis of children with MMD are constantly being improved to help improve the cure rate.
Financial support and sponsorship
This project was supported by China Postdoctoral Science Foundation Grant (2018M640802) and the Development Plan of Science and Technical Research of Chengde in China (201706A026).
Conflicts of interest
There are no conflicts of interest.
| References|| |
Han DH, Kwon OK, Byun BJ, Choi BY, Choi CW, Choi JU, Choi SG, Doh JO, Han JW, Jung S, Kang SD, Kim DJ, Kim HI, Kim HD, Kim MC, Kim SC, Kim SC, Kim Y, Kwun BD, Lee BG, Lim YJ, Moon JG, Park HS, Shin MS, Song JH, Suk JS, Yim MB; Korean Society for Cerebrovascular Disease. A co-operative study: Clinical characteristics of 334 Korean patients with Moyamoya disease treated at neurosurgical institutes (1976-1994). The Korean Society for Cerebrovascular Disease. Acta Neurochir (Wien)
Ge P, Zhang Q, Ye X, Wang S, Zhang D, Zhao J. Clinical features, surgical treatment, and long-term outcome in children with hemorrhagic Moyamoya disease. J Stroke Cerebrovasc Dis
Baltsavias G, Khan N, Valavanis A. The collateral circulation in pediatric Moyamoya disease. Childs Nerv Syst
Lee S, Rivkin MJ, Kirton A, deVeber G, Elbers J; International Pediatric Stroke Study. Moyamoya disease in children: Results from the international pediatric stroke study. J Child Neurol
Yonekawa Y. Operative neurosurgery: Personal view and historical backgrounds (9) Moyamoya angiopathy (MMA): Past history and status presents. No Shinkei Geka
Research Committee on the Pathology and Treatment of Spontaneous Occlusion of the Circle of Willis; Health Labour Sciences Research Grant for Research on Measures for Intractable Diseases. Guidelines for diagnosis and treatment of Moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo)
Kim JS. Moyamoya disease: Epidemiology, clinical features, and diagnosis. J Stroke
Ofer A, Nitecki SS, Linn S, Epelman M, Fischer D, Karram T, Litmanovich D, Schwartz H, Hoffman A, Engel A. Multidetector CT angiography of peripheral vascular disease: A prospective comparison with intraarterial digital subtraction angiography. AJR Am J Roentgenol
Piao J, Wu W, Yang Z, Yu J. Research progress of Moyamoya disease in children. Int J Med Sci
Takanashi J. Moyamoya disease in children. Brain Dev
Seo WK, Choi CW, Kim CK, Oh K. Contrast-enhanced color-coded Doppler sonography in Moyamoya disease: A retrospective study. Ultrasound Med Biol
Cho A, Chae JH, Kim HM, Lim BC, Hwang H, Hwang YS, Phi JH, Kim SK, Wang KC, Cho BK, Kim KJ. Electroencephalography in pediatric Moyamoya disease: Reappraisal of clinical value. Childs Nerv Syst
Goetti R, Warnock G, Kuhn FP, Guggenberger R, O'Gorman R, Buck A, Khan N, Scheer I. Quantitative cerebral perfusion imaging in children and young adults with Moyamoya disease: Comparison of arterial spin-labeling-MRI and H (2)[(15)O]-PET. AJNR Am J Neuroradiol
Ishii Y, Nariai T, Tanaka Y, Mukawa M, Inaji M, Maehara T, Ohno K. Practical clinical use of dynamic susceptibility contrast magnetic resonance imaging for the surgical treatment of Moyamoya disease. Neurosurgery
Huang S, Guo ZN, Shi M, Yang Y, Rao M. Etiology and pathogenesis of Moyamoya disease: An update on disease prevalence. Int J Stroke
Kamada F, Aoki Y, Narisawa A, Abe Y, Komatsuzaki S, Kikuchi A, Kanno J, Niihori T, Ono M, Ishii N, Owada Y, Fujimura M, Mashimo Y, Suzuki Y, Hata A, Tsuchiya S, Tominaga T, Matsubara Y, Kure S. A genome-wide association study identifies RNF213 as the first Moyamoya disease gene. J Hum Genet
Bao XY, Fan YN, Liu Y, Wang QN, Zhang Y, Zhu B, Liu B, Duan L. Circulating endothelial progenitor cells and endothelial cells in Moyamoya disease. Brain Behav
Yoshimoto T, Houkin K, Takahashi A, Abe H. Angiogenic factors in Moyamoya disease. Stroke
Zhou L, Wang QS. Genetic study on Moyamoya disease. Zhongguo Xian Dai Shen Jing Ji Bing Za Zhi
Sakamoto S, Kiura Y, Yamasaki F, Shibukawa M, Ohba S, Shrestha P, Sugiyama K, Kurisu K. Expression of vascular endothelial growth factor in Dura mater of patients with Moyamoya disease. Neurosurg Rev
Fujimura M, Watanabe M, Narisawa A, Shimizu H, Tominaga T. Increased expression of serum matrix metalloproteinase-9 in patients with Moyamoya disease. Surg Neurol
Li S, Zhao W, Han C, Rajah GB, Ren C, Xu J, Shang S, Meng R, Ding Y, Ji X. Safety and efficacy of remote ischemic conditioning in pediatric Moyamoya disease patients treated with revascularization therapy. Brain Circ
Fung LW, Thompson D, Ganesan V. Revascularisation surgery for paediatric Moyamoya: A review of the literature. Childs Nerv Syst
Hohenhaus M, Shah MJ, Eckenweiler M, van Velthoven V. Decompressive hemicraniectomy in the management of acute stroke in children with Moyamoya disease: The difficult balance between the spontaneous postoperative revascularization process and the need for cranial reconstruction. Childs Nerv Syst
Acker G, Fekonja L, Vajkoczy P. Surgical management of Moyamoya disease. Stroke
Macyszyn L, Attiah M, Ma TS, Ali Z, Faught R, Hossain A, Man K, Patel H, Sobota R, Zager EL, Stein SC. Direct versus indirect revascularization procedures for Moyamoya disease: A comparative effectiveness study. J Neurosurg
Oliveira RS, Amato MC, Simao GN, Abud DG, Avidago EB, Specian CM, Machado HR. Effect of multiple cranial burr hole surgery on prevention of recurrent ischemic attacks in children with Moyamoya disease. Neuropediatrics
Zhang Y, Bao XY, Duan L, Yang WZ, Li DS, Zhang ZS, Han C, Zhao F, Zhang Q, Wang QN. Encephalo-duro-arterio-synangiosis for pediatric Moyamoya disease: Long-term follow-up of 100 cases at a single center. J Neurosurg Pediatr
Rodriguez-Hernandez A, Josephson SA, Lawton MT. Bypass surgery for the prevention of ischemic stroke: Current indications and techniques. Neurocirugia (Astur)
Hsu YH, Kuo MF, Hua MS, Yang CC. Selective neuropsychological impairments and related clinical factors in children with Moyamoya disease of the transient ischemic attack type. Childs Nerv Syst
Imai H, Miyawaki S, Ono H, Nakatomi H, Yoshimoto Y, Saito N. The importance of encephalo-myo-synangiosis in surgical revascularization strategies for Moyamoya disease in children and adults. World Neurosurg
Guzman R, Lee M, Achrol A, Bell-Stephens T, Kelly M, Do HM, Marks MP, Steinberg GK. Clinical outcome after 450 revascularization procedures for Moyamoya disease. Clinical article. J Neurosurg
Arikan F, Rubiera M, Serena J, Rodríguez-Hernández A, Gándara D, Lorenzo-Bosquet C, Tomasello A, Chocrón I, Quintana-Corvalan M, Sahuquillo J. Revascularization experience and results in ischaemic cerebrovascular disease: Moyamoya disease and carotid occlusion. Neurocirugía (English Edition)
Blauwblomme T, Mathon B, Naggara O, Kossorotoff M, Bourgeois M, Puget S, Meyer P, Brousse V, de Montalembert M, Brunelle F, Zerah M, Sainte-Rose C. Long-term outcome after multiple burr hole surgery in children with Moyamoya angiopathy: A single-center experience in 108 hemispheres. Neurosurgery
Narisawa A, Fujimura M, Tominaga T. Efficacy of the revascularization surgery for adult-onset Moyamoya disease with the progression of cerebrovascular lesions. Clin Neurol Neurosurg
Khan N, Dodd R, Marks MP, Bell-Stephens T, Vavao J, Steinberg GK. Failure of primary percutaneous angioplasty and stenting in the prevention of ischemia in Moyamoya angiopathy. Cerebrovasc Dis