Quantitative Hemodynamic Study In Moyamoya Disease Based On 4D Flow MRI

Objective:Moyamoya disease is a special chronic cerebrovascular disease characterized by progressive stenosis and/or occlusion of the internal carotid artery.The present techniques for evaluating cerebral perfusion in moyamoya disease are limited hemodynamic examinations,whose biggest deficiency is that they cannot evaluate the hemodynamic state of a local area or a single blood vessel.The emerging technique,4D Flow MRI,has great potential in the quantitative evaluation of hemodynamics in vivo and has been used in intracranial aneurysms,cerebral arteriovenous malformations,and other diseases.However,there is no study on the use of 4D Flow MRI to evaluate the hemodynamics of moyamoya disease.The purpose of this study was to evaluate hemodynamic and morphological characteristics of moyamoya disease,the long-term changes of the internal carotid artery after combined revascularization,and its relationship with outcomes based on 4D Flow MRI.Materials and Methods:1.Patients diagnosed with moyamoya disease in West China Hospital,Sichuan University,from July 2018 to January 2020,were prospectively recruited as the case group.For the control group,volunteers in the same period were recruited.The Vessel Explorer2 software was employed to analyze 4D Flow MRI sequences and calculate the hemodynamic parameters of the internal carotid siphon.The Materialise Mimics software was utilized to analyze 3D TOF MRA sequences and calculate the morphological parameters of the internal carotid siphon.Compared with the normal internal carotid artery in the control group,we explored the hemodynamic and morphological characteristics of the siphon segment of the internal carotid artery in patients with moyamoya disease,such as mean/maximum flow,mean/maximum velocity,mean/maximum wall shear stress,cross-sectional area,normalized area,curvature,and tortuosity of anterior/posterior bends of the internal carotid siphon.The relationships between hemodynamics/morphology and clinical features such as sex,age,Suzuki stage,and symptom severity were analyzed.2.Patients with moyamoya disease who were diagnosed and received combined revascularization in West China Hospital,Sichuan University,from July 2018 to January 2020 were prospectively recruited.The Vessel Explorer2 software was employed to analyze the 4D Flow MRI sequences of pre-and post-operation and calculate hemodynamic parameters of the internal carotid siphon.The Materialise Mimics software was utilized to analyze the 3D TOF MRA sequences of pre-and postoperation and calculate the morphological parameters of the internal carotid siphon.The changes of all hemodynamic and morphological parameters were compared before and after revascularization in patients with moyamoya disease.The relationships between hemodynamic/morphological changes and clinical features such as sex,age,Suzuki stage,and symptom severity were also analyzed.3.To further analyze and explore the relationship between the hemodynamic and morphological parameters of the internal carotid artery in moyamoya disease and the long-term outcomes,including clinical symptom improvement,cerebral perfusion improvement,and intracranial vascular remodeling after combined revascularization.Results:1.In this part,66 and 56 participants were included as the moyamoya disease group and control group,respectively.We obtained 132 and 64 internal carotid arteries in the moyamoya disease group and the control group,respectively.The mean/maximum flow(P <0.001,P <0.001)and the mean/maximum velocity(P=0.008,P <0.001)of the internal carotid siphon,the cross-sectional area(P <0.001,P<0.001),the normalized area(P <0.001,P <0.001),and the tortuosity(P <0.001,P<0.001)of the anterior/posterior bends of the internal carotid siphon in patients with moyamoya disease were significantly lower than those in the control group.However,the curvature of the anterior bend of the internal carotid siphon in moyamoya disease patients was significantly larger than the control participants(P =0.030).There was no significant difference in other hemodynamic and morphological parameters between the two groups(P >0.05).Subgroup analysis showed that hemodynamics and morphology of the internal carotid siphon in patients with moyamoya disease showed significantly different characteristics in different sex,age,Suzuki stage,and severity of the disease.2.A total of 35 patients(15 males and 20 females)with moyamoya disease were included in this section.The imaging follow-up period was 7(5-10)months.During the long-term follow-up,the mean flow(P <0.001,P =0.002)and the maximum flow(P <0.001,P =0.001)of the bilateral internal carotid siphon,the tortuosity of anterior bond bends(P =0.023,P <0.001),and the tortuosity of posterior bends(P =0.002,P=0.042)of the bilateral internal carotid siphon were significantly decreased.Subgroup analysis revealed that the hemodynamic and morphological changes of the internal carotid artery in moyamoya disease were significantly different in sex,age,Suzuki stage,and severity of disease during long-term follow-up after revascularization.3.A total of 35 patients with moyamoya disease were included in this section.In the patients with good improvement of clinical symptoms during long-term follow-up,the mean flow(P =0.004,P =0.003)and the maximum flow(P =0.008,P =0.003)of the bilateral internal carotid siphon,the tortuosity of the anterior bends of the bilateral internal carotid siphon(P =0.017,P =0.025),and the tortuosity of the posterior siphon bend on the surgical side(P =0.024)were significantly lower than before revascularization.However,in the patients with excellent improvement of clinical symptoms during long-term follow-up,the mean flow(P =0.015),the maximum flow(P =0.009),the tortuosity of the posterior bend(P =0.041)of the posterior siphon bend on the surgical side,and the tortuosity of the anterior bend of the contralateral internal carotid siphon(P =0.008)were significantly lower than before revascularization.In the patients with improved cerebral perfusion at long-term follow-up after revascularization,the mean flow(P =0.001,P =0.006)and the maximum flow(P<0.001,P =0.005)of the bilateral internal carotid siphon,the tortuosity of the anterior bend(P =0.014)and the posterior bend(P =0.005)of internal carotid siphon on the surgical side,and the tortuosity of the anterior bend of the contralateral internal carotid siphon(P =0.004)were significantly lower than before revascularization.In the patients with no improvement of cerebral perfusion during long-term follow-up,only the cross-sectional area(P =0.005)and the normalized area(P =0.006)of the anterior bend of the contralateral internal carotid siphon were significantly larger than those before revascularization.In patients with vascular remodeling effect of grade 0 during long-term follow-up,only the maximum wall shear stress of the internal carotid siphon on the surgical side(P =0.016)and the tortuosity of the anterior bend of the contralateral internal carotid siphon(P =0.038)were significantly lower than before revascularization.In the patients with vascular remodeling effect of grade I during long-term follow-up,the mean flow(P =0.026,P =0.013)and the maximum flow(P=0.023,P =0.010)of the bilateral internal carotid artery,the mean flow velocity(P=0.041)and the tortuosity of the posterior bend(P =0.005)of the internal carotid siphon on the surgical side,and the tortuosity of the anterior bend(P =0.001)and the posterior bend(P =0.037)of the contralateral internal carotid siphon were significantly lower than before revascularization.However,the cross-sectional area(P =0.025,P=0.016)and the normalized area(P =0.021,P =0.019)of the anterior/posterior bends of the contralateral internal carotid siphon were significantly increased compared with before revascularization.In patients with vascular remodeling effect of II or III grade during long-term follow-up,the mean flow(P =0.014,P =0.028)and the maximum flow(P =0.018,P =0.023)of the bilateral internal carotid siphon were significantly lower than those before operation(P =0.014,P =0.028),but there was no significant difference in other parameters compared with before revascularization(P =0.014,P=0.028).Conclusion:1.We firstly utilized the 4D Flow MRI technique to detect the hemodynamic characteristics of moyamoya disease and demonstrated significant differences in several hemodynamic and morphological parameters of the internal carotid siphon between moyamoya disease and healthy controls.The clinical characteristics such as sex,age,Suzuki stage,and severity of the disease were associated with the characteristics and changes of the hemodynamics and morphology of patients with moyamoya disease.2.The changes of morphological parameters of the internal carotid artery in patients with moyamoya disease are related to the changes of main hemodynamic parameters,and the results of their linkage may help maintain the stability of wall shear stress in the internal carotid artery.3.This study firstly proposed that the mean/maximum flow and the tortuosity of anterior/posterior bends of the bilateral internal carotid siphon might be predictors of the long-term prognosis after combined revascularization in moyamoya disease.4.4D Flow MRI is a new technical method to evaluate the hemodynamics of moyamoya disease,which can directly detect intravascular hemodynamics.It has an excellent prospect for observation,understanding,and study of the pathophysiological mechanism of moyamoya disease.