Combined structural and diffusion tensor imaging detection of ischemic injury in moyamoya disease: relation to disease advancement and cerebral hypoperfusion

被引:26
作者
Kazumata, Ken [1 ]
Tokairin, Kikutaro [1 ]
Ito, Masaki [1 ]
Uchino, Haruto [1 ]
Sugiyama, Taku [1 ]
Kawabori, Masahito [1 ]
Osanai, Toshiya [1 ]
Tha, Khin Khin [2 ]
Houkin, Kiyohiro [1 ]
机构
[1] Hokkaido Univ, Grad Sch Med, Dept Neurosurg, Sapporo, Hokkaido, Japan
[2] Hokkaido Univ Hosp, Clin Res & Med Innovat Ctr, Sapporo, Hokkaido, Japan
关键词
cerebral blood flow; cognitive disorder; diffusion tensor imaging; moyamoya disease; volumetric magnetic resonance imaging; vascular disorders; WHITE-MATTER; PROCESSING SPEED; DAMAGE; DYSFUNCTION; PERFORMANCE; IMPAIRMENT; INTEGRITY; KURTOSIS; MRI;
D O I
10.3171/2020.1.JNS193260
中图分类号
R74 [神经病学与精神病学];
学科分类号
摘要
OBJECTIVE The microstructural integrity of gray and white matter is decreased in adult moyamoya disease, suggesting covert ischemic injury as a mechanism of cognitive dysfunction. Establishing a microstructural brain imaging marker is critical for monitoring cognitive outcomes following surgical interventions. The authors of the present study determined the pathophysiological basis of altered microstructural brain injury in relation to advanced arterial occlusion, cerebral hypoperfusion, and cognitive function. METHODS The authors examined 58 patients without apparent brain lesions and 30 healthy controls by using structural MRI, as well as diffusion tensor imaging (DTI). Arterial occlusion in each hemisphere was classified as early or advanced stage based on MRA and posterior cerebral artery (PCA) involvement. Regional cerebral blood flow (rCBF) was measured with N-isopropyl-p-[I-123]-iodoamphetamine SPECT. Furthermore, cognitive performance was examined using the Wechsler Adult Intelligence Scale, Third Edition and the Trail Making Test (TMT). Both voxel- and region of interest-based analyses were performed for groupwise comparisons, as well as correlation analysis, using parameters such as cognitive test scores; gray matter volume; fractional anisotropy (FA) of association fiber tracts, including the inferior frontooccipital fasciculus (IFOF) and superior longitudinal fasciculus (SLF); PCA involvement; and rCBF. RESULTS Compared to the early stages, advanced stages of arterial occlusion in the left hemisphere were associated with a lower Performance IQ (p = 0.031), decreased anterior cingulate volumes (p = 0.0001, uncorrected), and lower FA in the IFOF, cingulum, and forceps major (all p < 0.01, all uncorrected). There was no significant difference in rCBF between the early and the advanced stage. In patients with an advanced stage, PCA involvement was correlated with a significantly lower Full Scale IQ (p = 0.036), cingulate volume (p < 0.01, uncorrected), and FA of the left SLF (p = 0.0002, uncorrected) compared to those with an intact PCA. The rCBF was positively correlated with FA of the SLF, IFOF, and forceps major (r > 0.34, p < 0.05). Global gray matter volumes were moderately correlated with TMT part A (r = 0.40, p = 0.003). FA values in the left SLF were moderately associated with processing speed (r = 0.40, p = 0.002). CONCLUSIONS Although hemodynamic compensation may mask cerebral ischemia in advanced stages of adult moyamoya disease, the disease progression is detrimental to gray and white matter microstructure as well as cognition. In particular, additional PCA involvement in advanced disease stages may impair key neural substrates such as the cingulum and SLF. Thus, combined structural MRI and DTI are potentially useful for tracking the neural integrity of key neural substrates associated with cognitive function and detecting subtle anatomical changes associated with persistent ischemia, as well as disease progression.
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收藏
页码:1155 / 1164
页数:10
相关论文
共 34 条
[1]   Unified segmentation [J].
Ashburner, J ;
Friston, KJ .
NEUROIMAGE, 2005, 26 (03) :839-851
[2]   A fast diffeomorphic image registration algorithm [J].
Ashburner, John .
NEUROIMAGE, 2007, 38 (01) :95-113
[3]   The basis of anisotropic water diffusion in the nervous system - a technical review [J].
Beaulieu, C .
NMR IN BIOMEDICINE, 2002, 15 (7-8) :435-455
[4]   Executive dysfunction in adults with moyamoya disease is associated with increased diffusion in frontal white matter [J].
Calviere, Lionel ;
Kai, Guillaume Ssi Yan ;
Catalaa, Isabelle ;
Marlats, Fabienne ;
Bonneville, Fabrice ;
Larrue, V. .
JOURNAL OF NEUROLOGY NEUROSURGERY AND PSYCHIATRY, 2012, 83 (06) :591-593
[5]   Characterization of White Matter Injury in a Rat Model of Chronic Cerebral Hypoperfusion [J].
Choi, Bo-Ryoung ;
Kim, Dong-Hee ;
Bin Back, Dong ;
Kang, Chung Hwan ;
Moon, Won-Jin ;
Han, Jung-Soo ;
Choi, Dong-Hee ;
Kwon, Kyoung Ja ;
Shin, Chan Young ;
Kim, Bo-Ram ;
Lee, Jongmin ;
Han, Seol-Heui ;
Kim, Hahn Young .
STROKE, 2016, 47 (02) :542-+
[6]   Changes to White Matter Microstructure in Transient Ischemic Attack: A Longitudinal Diffusion Tensor Imaging Study [J].
Ferris, Jennifer K. ;
Edwards, Jodi D. ;
Ma, Jennifer A. ;
Boyd, Lara A. .
HUMAN BRAIN MAPPING, 2017, 38 (11) :5795-5803
[7]   Impact of posterior cerebral artery involvement on long-term clinical and social outcome of pediatric moyamoya disease [J].
Funaki, Takeshi ;
Takahashi, Jun C. ;
Takagi, Yasushi ;
Yoshida, Kazumichi ;
Araki, Yoshio ;
Kikuchi, Takayuki ;
Kataoka, Hiroharu ;
Iihara, Koji ;
Miyamoto, Susumu .
JOURNAL OF NEUROSURGERY-PEDIATRICS, 2013, 12 (06) :626-632
[8]   Vascular Contributions to Cognitive Impairment and Dementia A Statement for Healthcare Professionals From the American Heart Association/American Stroke Association [J].
Gorelick, Philip B. ;
Scuteri, Angelo ;
Black, Sandra E. ;
DeCarli, Charles ;
Greenberg, Steven M. ;
Iadecola, Costantino ;
Launer, Lenore J. ;
Laurent, Stephane ;
Lopez, Oscar L. ;
Nyenhuis, David ;
Petersen, Ronald C. ;
Schneider, Julie A. ;
Tzourio, Christophe ;
Arnett, Donna K. ;
Bennett, David A. ;
Chui, Helena C. ;
Higashida, Randall T. ;
Lindquist, Ruth ;
Nilsson, Peter M. ;
Roman, Gustavo C. ;
Sellke, Frank W. ;
Seshadri, Sudha .
STROKE, 2011, 42 (09) :2672-2713
[9]   Unraveling Specific Brain Microstructural Damage in Moyamoya Disease Using Diffusion Magnetic Resonance Imaging and Positron Emission Tomography [J].
Hara, Shoko ;
Hori, Masaaki ;
Ueda, Ryo ;
Hayashi, Shihori ;
Inaji, Motoki ;
Tanaka, Yoji ;
Maehara, Taketoshi ;
Ishii, Kenji ;
Aoki, Shigeki ;
Nariai, Tadashi .
JOURNAL OF STROKE & CEREBROVASCULAR DISEASES, 2019, 28 (04) :1113-1125
[10]   Microstructural Damage in Normal-Appearing Brain Parenchyma and Neurocognitive Dysfunction in Adult Moyamoya Disease [J].
Hara, Shoko ;
Hori, Masaaki ;
Murata, Syo ;
Ueda, Ryo ;
Tanaka, Yoji ;
Inaji, Motoki ;
Maehara, Taketoshi ;
Aoki, Shigeki ;
Nariai, Tadashi .
STROKE, 2018, 49 (10) :2504-2507