Preoperatively estimated graft flow rate contributes to the improvement of hemodynamics in revascularization for Moyamoya disease

      Highlights

      • l
        The influence of the graft in bypass surgery was evaluated using CFD analysis.
      • l
        The flow rate of the graft contributed to the improvements of hemodynamic changes.
      • l
        The size of the graft was important in postoperative hemodynamic improvements.

      Abstract

      Objectives: Superficial temporal artery (STA)-middle cerebral artery (MCA) bypass operation is an effective treatment for patients with Moyamoya disease, and the hemodynamic parameters are reported to be improved after operation. However, there is no report concerning hemodynamic changes from the viewpoint of the preoperative anatomical structure of grafts. In this study, we evaluated the correlation between the preoperatively estimated blood flow of the graft obtained through image-based computational fluid dynamics (CFD) analysis and the hemodynamic changes in the acute phase after revascularization. Materials and methods: A total of 30 hemispheric sides of 23 patients were examined. The blood flow, that is, flow rate (FR) of the STA branches that were anastomosed to the MCA was evaluated using CFD analysis based on computed tomography (CT) angiography imaging data. The correlations between the FR and the hemodynamic changes in the acute phase after revascularization obtained through CT perfusion were assessed. Results: The preoperatively estimated FR of the graft was moderately correlated with the changes in the mean transit time significantly and weakly correlated with those in the cerebral blood flow and cerebral blood volume. In addition, the FR was strongly correlated with age and the diameter of the STA from the origin to the bifurcation.Conclusion: The preoperatively estimated FR of the graft obtained through image-based CFD analysis contributed to the improvement of the mean transit time after revascularization. Because the FR of the graft was associated with the diameter of the STA, the size of the STA might be an important factor in postoperative hemodynamic changes. This might lead to the risk assessment of acute drastic hemodynamic changes as cerebral hyperperfusion, and consequently, better surgical outcomes might be expected.

      Key Words

      To read this article in full you will need to make a payment

      Subscribe:

      Subscribe to Journal of Stroke and Cerebrovascular Diseases
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Nishimoto A
        • Takeuchi S.
        Abnormal cerebrovascular network related to the internal cartoid arteries.
        J Neurosurg. 1968; 29: 255-260
        • Suzuki J
        • Takaku A
        Cerebrovascular "Moyamoya"; disease. Disease showing abnormal net-like vessels in base of brain.
        Arch Neurol. 1969; 20: 288-299
        • Ogawa A
        • Yoshimoto T
        • Suzuki J
        • et al.
        Cerebral blood flow in moyamoya disease. Part 1: correlation with age and regional distribution.
        Acta Neurochir (Wien). 1990; 105: 30-34
        • Kuroda S
        • Houkin K.
        Moyamoya disease: current concepts and future perspectives.
        Lancet Neurol. 2008; 7: 1056-1066
        • Lee M
        • Zaharchuk G
        • Guzman R
        • et al.
        Quantitative hemodynamic studies in moyamoya disease: a review.
        Neurosurg Focus. 2009; 26: E5
        • Hashimoto A
        • Mikami T
        • Komatsu K
        • et al.
        Assessment of hemodynamic compromise using computed tomography perfusion in combination with (123)I-IMP single-photon emission computed tomography without acetazolamide challenge test.
        J Stroke Cerebrovasc Dis. 2017; 26: 627-635
        • Suzuki H
        • Mikami T
        • Komatsu K
        • et al.
        Assessment of the cortical artery using computed tomography angiography for bypass surgery in moyamoya disease.
        Neurosurg Rev. 2017; 40: 299-307
        • Sasagawa A
        • Mikami T
        • Hirano T
        • et al.
        Characteristics of cerebral hemodynamics assessed by CT perfusion in moyamoya disease.
        J Clin Neurosci. 2018; 47: 183-189
        • Tian B
        • Xu B
        • Liu Q
        • et al.
        Adult Moyamoya disease: 320-multidetector row CT for evaluation of revascularization in STA-MCA bypasses surgery.
        Eur J Radiol. 2013; 82: 2342-2347
        • Zhang J
        • Wang J
        • Geng D
        • et al.
        Whole-brain CT perfusion and CT angiography assessment of Moyamoya disease before and after surgical revascularization: preliminary study with 256-slice CT.
        PLoS One. 2013; 8: e57595
        • Chen Y
        • Xu W
        • Guo X
        • et al.
        CT perfusion assessment of Moyamoya syndrome before and after direct revascularization (superficial temporal artery to middle cerebral artery bypass).
        Eur Radiol. 2016; 26: 254-261
        • Dai DW
        • Zhao WY
        • Zhang YW
        • et al.
        Role of CT perfusion imaging in evaluating the effects of multiple burr hole surgery on adult ischemic Moyamoya disease.
        Neuroradiology. 2013; 55: 1431-1438
      1. Zhang J, Li S, Fujimura M, et al. Hemodynamic analysis of the recipient parasylvian cortical arteries for predicting postoperative hyperperfusion during STA-MCA bypass in adult patients with Moyamoya disease. J Neurosurg 2019:1-8.

        • Steinman DA
        • Milner JS
        • Norley CJ
        • et al.
        Image-based computational simulation of flow dynamics in a giant intracranial aneurysm.
        AJNR Am J Neuroradiol. 2003; 24: 559-566
        • Jou LD
        • Quick CM
        • Young WL
        • et al.
        Computational approach to quantifying hemodynamic forces in giant cerebral aneurysms.
        AJNR Am J Neuroradiol. 2003; 24: 1804-1810
        • Shojima M
        • Oshima M
        • Takagi K
        • et al.
        Magnitude and role of wall shear stress on cerebral aneurysm: computational fluid dynamic study of 20 middle cerebral artery aneurysms.
        Stroke. 2004; 35: 2500-2505
        • Takao H
        • Murayama Y
        • Otsuka S
        • et al.
        Hemodynamic differences between unruptured and ruptured intracranial aneurysms during observation.
        Stroke. 2012; 43: 1436-1439
      2. Suzuki T, Stapleton CJ, Koch MJ, et al. Decreased wall shear stress at high-pressure areas predicts the rupture point in ruptured intracranial aneurysms. J Neurosurg 2019:1-7.

      3. Khan MO, Toro Arana V, Rubbert C, et al. Association between aneurysm hemodynamics and wall enhancement on 3D vessel wall MRI. J Neurosurg 2020:1-11.

        • Huang Q
        • Xu J
        • Cheng J
        • et al.
        Hemodynamic changes by flow diverters in rabbit aneurysm models: a computational fluid dynamic study based on micro-computed tomography reconstruction.
        Stroke. 2013; 44: 1936-1941
        • Xiang J
        • Damiano RJ
        • Lin N
        • et al.
        High-fidelity virtual stenting: modeling of flow diverter deployment for hemodynamic characterization of complex intracranial aneurysms.
        J Neurosurg. 2015; 123: 832-840
        • Kataoka H
        • Makino Y
        • Takanishi K
        • et al.
        Vascular responses to abrupt blood flow change after bypass surgery for complex intracranial aneurysms.
        Acta Neurochir (Wien). 2018; 160: 1945-1953
        • Zhu F
        • Qian Y
        • Xu B
        • et al.
        Quantitative assessment of changes in hemodynamics of the internal carotid artery after bypass surgery for moyamoya disease.
        J Neurosurg. 2018; 129: 677-683
      4. Satoh T, Yagi T, Onoda K, et al. Hemodynamic features of offending vessels at neurovascular contact in patients with trigeminal neuralgia and hemifacial spasm. J Neurosurg 2018:1-7.

        • Charbel FT
        • Zhao M
        • Amin-Hanjani S
        • et al.
        A patient-specific computer model to predict outcomes of the balloon occlusion test.
        J Neurosurg. 2004; 101: 977-988
        • Houkin K
        • Nakayama N
        • Kuroda S
        • et al.
        Novel magnetic resonance angiography stage grading for moyamoya disease.
        Cerebrovasc Dis. 2005; 20: 347-354
        • Kaku Y
        • Iihara K
        • Nakajima N
        • et al.
        Cerebral blood flow and metabolism of hyperperfusion after cerebral revascularization in patients with moyamoya disease.
        J Cereb Blood Flow Metab. 2012; 32: 2066-2075
        • Uchino H
        • Kuroda S
        • Hirata K
        • et al.
        Predictors and clinical features of postoperative hyperperfusion after surgical revascularization for Moyamoya disease: a serial single photon emission CT/positron emission tomography study.
        Stroke. 2012; 43: 2610-2616
        • Ogasawara K
        • Yukawa H
        • Kobayashi M
        • et al.
        Prediction and monitoring of cerebral hyperperfusion after carotid endarterectomy by using single-photon emission computerized tomography scanning.
        J Neurosurg. 2003; 99: 504-510
        • Furuya K
        • Kawahara N
        • Morita A
        • et al.
        Focal hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in a patient with moyamoya disease. Case Report.
        J Neurosurg. 2004; 100: 128-132
        • Fujimura M
        • Kaneta T
        • Shimizu H
        • et al.
        Symptomatic hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in a child with moyamoya disease.
        Child's Nerv Syst ChNS. 2007; 23: 1195-1198
        • Uchino H
        • Kazumata K
        • Ito M
        • et al.
        Crossed cerebellar diaschisis as an indicator of severe cerebral hyperperfusion after direct bypass for Moyamoya disease.
        Neurosurg Rev. 2020;
        • Yu J
        • Zhang J
        • Li J
        • et al.
        Cerebral hyperperfusion syndrome after revascularization surgery in patients with Moyamoya disease: systematic review and meta-analysis.
        World Neurosurg. 2020; 135 (e354): 357-366
        • Fujimura M
        • Gasche Y
        • Morita-Fujimura Y
        • et al.
        Early appearance of activated matrix metalloproteinase-9 and blood-brain barrier disruption in mice after focal cerebral ischemia and reperfusion.
        Brain Res. 1999; 842: 92-100
        • Fujimura M
        • Shimizu H
        • Mugikura S
        • et al.
        Delayed intracerebral hemorrhage after superficial temporal artery-middle cerebral artery anastomosis in a patient with moyamoya disease: possible involvement of cerebral hyperperfusion and increased vascular permeability.
        Surg Neurol. 2009; 71 (discussion 227): 223-227
        • Kameyama M
        • Fujimura M
        • Tashiro R
        • et al.
        Significance of quantitative cerebral blood flow measurement in the acute stage after revascularization surgery for adult Moyamoya disease: implication for the pathological threshold of local cerebral hyperperfusion.
        Cerebrovasc Dis. 2019; 48: 217-225
        • Guzman R
        • Lee M
        • Achrol A
        • et al.
        Clinical outcome after 450 revascularization procedures for moyamoya disease. Clinical article.
        J Neurosurg. 2009; 111: 927-935
        • Bot GM
        • Burkhardt JK
        • Gupta N
        • et al.
        Superficial temporal artery-to-middle cerebral artery bypass in combination with indirect revascularization in Moyamoya patients ≤ 3 years of age.
        J Neurosurg Pediatr. 2018; 23: 198-203
        • Sekhar LN
        • Natarajan SK
        • Ellenbogen RG
        • et al.
        Cerebral revascularization for ischemia, aneurysms, and cranial base tumors.
        Neurosurgery. 2008; 62 (discussion 1408-1310): 1373-1408
        • Ha EJ
        • Kim KH
        • Wang KC
        • et al.
        Long-term outcomes of indirect bypass for 629 children with Moyamoya disease: longitudinal and cross-sectional analysis.
        Stroke. 2019; 50: 3177-3183