Correlation Study Between Extracranial Internal Carotid Artery Disease And Hemorrhagic Moyamoya Disease

Part ?: Association between Champagne Bottle Neck Sign of Internal Carotid Artery and Ipsilateral Hemorrhagic Stroke in Patients with Moyamoya DiseaseBackground and purposeMoyamoya disease(MMD)is an uncommon cerebrovascular disorder characterized by progressive occlusion in the terminal portion of internal carotid artery(ICA)and its main branches within the circle of Willis(1).In adult MMD patients,intracranial hemorrhage accounts for half of primary manifestations and the outcome is poor(2,3).Clinically,evaluation of patients with MMD at risk for intracranial hemorrhage is mostly focused on intracranial characteristics such as peripheral aneurysms in the collateral vessels or moyamoya vessels and saccular aneurysms in the circle of Willis(4,5),extended choroidal anastomosis or thalamic perforating arteries(6,7,9)and involvement of posterior cerebral artery(PCA)(8,9).However,the relationship between characteristics of extracranial carotid arteries and ipsilateral intracranial hemorrhage in MMD patients remains unknown.The rapid luminal diameter reduction in proximal ICA(ICA/common carotid artery(CCA)?0.5),characterized by champagne bottle neck sign(CBNS),is a novel approach to assess MMD according to recent publications(10,11).The CBNS has been demonstrated to be associated with ischemic cerebral events(12).In contrast,the relationship between CBNS in ICAs and hemorrhagic cerebral events is still unclear.PurposeTo assess the association between champagne bottle neck sign(CBNS)in carotid artery and intracranial hemorrhage in patients with moyamoya disease(MMD).MethodsFrom January 2016 to December 2017,a total of 76 consecutive patients with MMD without definite risk factors associated intracranial hemorrhage who underwent preoperative angiography were included in this retrospective study.CBNS was defined as luminal diameter of internal carotid artery(ICA)/common carotid artery(CCA)? 0.5 on angiographic imaging.The right and left cerebral hemisphere in each patient was separately identified as hemorrhagic and none-hemorrhagic.The association between CBNS and intracranial hemorrhage was analyzed.ResultsOf 76 MMD patients,intracranial hemorrhage was found in 44(28.9%)hemispheres of 152 and 6.8%(3/44)had multiple events.Compared carotid arteries without intracranial hemorrhage in the ipsilateral hemispheres,those with intracranial hemorrhage in the ipsilateral hemispheres had significantly smaller luminal diameter ratio of ICA/CCA(0.49 ± 0.11 vs.0.55 ± 0.12,p < 0.01)and higher prevalence of CBNS(63.7% vs.41.7%,p = 0.01).For hemispheres with intracranial hemorrhage,those with ipsilateral carotid artery CBNS had significantly higher prevalence of hemorrhage at posterior territories than those without(57.1% vs.23.1%,p=0.05).Logistic regression revealed that CBNS was significantly associated with ipsilateral intracranial hemorrhage before(OR,2.45;95% CI,1.19-5.05;p=0.02)and after(OR,3.23;95% CI,1.48-7.06;p<0.01)adjusted for confounding factors.ConclusionCBNS is significantly associated with intracranial hemorrhage at ipsilateral hemisphere in MMD patients,particularly for intracranial hemorrhage at posterior territories.Part ?: Disruption of Carotid Arterial Wall Structure(DCAWS)in Moyamoya DiseaseBackgroundIt has been shown that MMD not only involves the intracranial cerebral arteries,but also affects extracranial carotid arteries by the previous autopsy studies and case reports(13,14).However,the characteristics of involvement of extracranial carotid arteries in MMD patients has been rarely described.We found that CBNS was prevalent in MMD patients and significantly associated with intracranial hemorrhage in ipsilateral hemisphere,particularly hemorrhage at posterior territories.However,it remains unknown that if MMD patients with CBNS have arteriopathy in extracranial carotid arteries.Ultrasound imaging is the most convenient non-invasive approach in assessing extracranial carotid artery disease.The intima and media of carotid artery can be well delineated by ultrasound(15,16).The diseases which damage the integrity of carotid arterial wall structure can be potentially identified by ultrasound imaging with high resolution probe.The pathological changes of MMD have been consistently reported in the scientific literature.Although the pathological findings have not been uniform,the most prominent features have been excessive tortuous and duplication or deficiencies in the internal elastic lamina(IEL)and thinned media(13,14,17,18).We hypothesized that a substantial number of patients presence of disruption carotid arterial wall structure(DCAWS)which could be evaluated by ultrasound imaging.PurposeTo investigate the association between arteriopathy severity and disruption carotid arterial wall structure(DCAWS)in patients with moyamoya disease(MMD).MethodsSixty consecutive patients with MMD were recruited and underwent carotid ultrasound imaging and cerebral catheter angiography.Presence of DCAWS was determined by ultrasound imaging.The diameter of proximal ICA,bulb and distal common carotid artery(CCA)were measured,respectively.The stenotic-occlusive location of ICA,presence of occlusion in distal ICA and involvement of posterior cerebral artery(PCA)were evaluated by angiography.The imaging characteristics between patients with and without DCAWS were compared.The correlation between imaging characteristics and DCAWS was analyzed.ResultsThe DCAWS was found in 35%(21/60)MMD patients and 23.3%(14/60)had bilateral artery involvement.Compared arteries with none DCAWS,those with DCAWS had significantly more prevalence of Suzuki stage V-VI(77.8% vs.56.0%,p=0.077),smaller diameter in ICA(0.22±0.05 cm vs.0.29±0.07 cm,p<0.001)and CCA(0.48±0.07 cm vs.0.53±0.06 cm,p=0.001),higher prevalence of CBNS(72.2% vs.44.0%,p=0.005),stenotic-occlusive lesions below PCom A(75.0% vs.17.9%,p<0.001)and involvement of PCA(66.7% vs.23.1%,p<0.001).After adjusted for confounding factors,stenotic-occlusive lesions below PCom A(OR,5.776;95% CI,1.557-21.423;p=0.009),involvement of PCA(OR,4.631;95% CI,1.400-15.321;p=0.012)and ICA diameter <0.24 cm(OR,5.782;95% CI,1.536-21.760;p=0.009)were significantly associated with DCAWS in MMD,respectively.ConclusionThe DCAWS in MMD detected by ultrasound is significantly associated with smaller arterial diameter,more severe stenotic-occlusive lesions involving PCA and inferior segments of ICA,indicating that patients with DCAWS may have systemic multifocal arteriopathy.Part ?:Proximal Internal Carotid Artery Stenosis Associates with Diffuse Wall Thickening in Petrous Arterial Segment of Moyamoya Disease Patients: A Three-Dimensional Magnetic Resonance Wall Imaging StudyBackgroundMoyamoya disease(MMD)is a cerebrovascular disorder which not only involves the intracranial arteries but also affects extracranial carotid arteries.It has been shown that rapid reduction of the diameter at the proximal portion of extracranial ICA can occur in a substantial number of MMD patients.Previous study reported that patients with severe carotid atherosclerotic stenosis had diffuse wall thickening(DWT)in ipsilateral petrous internal carotid artery which may aggravate cerebral ischemia and affect the efficiency of revascularization treatment(19).However,it is unknown whether the DWT can be detected at petrous ICA in MMD patients.According to several recent studies,the phenomenon of diffuse wall thickening could be explained by a series of pathophysiological processes of ischemia injury and inflammation reaction(19-21).Therefore,it is important to find an effective surrogate for DWT and characterize the vessel wall of MMD patients prior to surgery.Recently,3D MR vessel wall imaging has been proposed to characterize the vascular diseases,such as atherosclerotic disease(22-24),dissection(25),and MMD(26)benefiting from excellent blood suppression and large longitudinal coverage.Of 3D MR vessel wall imaging techniques,T1 imaging with an improved motion-sensitized driven-equilibrium(i MSDE)-prepared volumetric isotropic turbo spin-echo acquisition(VISTA)sequence is expected to minimize the intravascular artifacts and intravascular enhancement after the Gadolinium administration in a relatively shorter examination duration(27).This technique can well delineate arterial morphology and compositional features when given gadolinium contrast.PurposeTo investigate the association between proximal ICA luminal narrowing and diffuse wall thickening(DWT)in ipsilateral petrous ICA in moyamoya disease(MMD)patients.MethodsForty-one MMD patients(mean age 42.8±11.0 years,19 males)were recruited and underwent MR vessel wall imaging for carotid arteries.The diameter of ICA and common carotid artery(CCA)were measured on DSA.The luminal narrowing of proximal ICA was evaluated by the diameter ratio of ICA to CCA(DR ICA/CCA).The wall thickness of the petrous ICA was measured on T1-VISTA images.The enhancement degree of petrous ICA was recorded and graded into 4 grades(none to marked)on the CE-T1-VISTA images.The correlation between wall thickness in petrous ICA and DR ICA/CCA was analyzed.ResultsIn total,81 arteries from 41 patients were included for final analysis and 19 showed DWT in petrous ICA.Proximal ICA luminal narrowing was significantly correlated with the wall thickness in petrous ICA(r=-0.434,P<.001).Logistic regression analysis revealed that OR of DR ICA/CCA with decrease of 0.1 was 3.731(95% CI 1.725-6.585,P<.001)and 4.433(95% CI 1.980-9.925,P<.001)in discriminating presence of DWT of petrous ICA before and after adjusting for confounding factors.An increasing trend was found in prevalence of DWT(P=.02)and wall thickness(P=.01)with enhancement grades in petrous ICA.ConclusionThe proximal ICA luminal narrowing is significantly associated with wall thickness and diffuse wall thickening in ipsilateral petrous ICA in MMD patients.