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Comparative Study of Multi-Delay Pseudo-Continuous Arterial Spin Labeling Perfusion MRI and CT Perfusion in Ischemic Stroke Disease

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Comparative Study of Multi-Delay Pseudo-Continuous Arterial Spin Labeling Perfusion MRI and CT Perfusion in Ischemic Stroke Disease fninf-15-719719 August 11, 2021 Time: 12:53 # 1 ORIGINAL RESEARCH published: 11 August 2021 doi: 10.3389/fninf.2021.719719 Comparative Study of Multi-Delay Pseudo-Continuous Arterial Spin Labeling Perfusion MRI and CT Perfusion in Ischemic Stroke Disease Xi Xu1†, Zefeng Tan2,3†, Meng Fan1†, Mengjie Ma1, Weimin Fang1, Jianye Liang1,4, Zeyu Xiao1, Changzheng Shi1,5* and Liangping Luo1,5* 1 Medical Imaging Center, The First Affiliated Hospital of Jinan University, Guangzhou, China, 2 Department of Neurology, The First Affiliated Hospital of Jinan University, Guangzhou, China, 3 Department of Neurology, Shun De Hospital of Jinan University, Foshan, China, 4 Department of Medical Imaging, Sun Yat-sen University Cancer Center, Guangzhou, China, 5 Engineering Research Center of Medical Imaging Artificial Intelligence for Precision Diagnosis and Treatment, Guangzhou, China With the aging population, stroke has gradually become the leading cause of death and disability among adults. It is necessary to verify whether multi-delay pseudo-continuous arterial spin labeling (pCASL) MRI can be used as a standard neuroimaging protocol in the patients with ischemic stroke. We aimed to investigate the clinical utility of multi- delay pCASL for evaluating cerebral perfusion in ischemic stroke disease. Twenty-one ischemic stroke patients [18 men and 3 women; median age, 62 years (age range, 37– Edited by: 84 years)] were enrolled in this study. All patients underwent examinations, including Heye Zhang, Sun Yat-sen University, China the multi-delay pCASL protocol (using 6 PLDs between 1,000 and 3,500 ms) and Reviewed by: computed tomography perfusion (CTP). The cerebral blood flow (CBF) and arterial KowsalyaDevi Pavuluri, transit time (ATT) maps were obtained by the multi-delay pCASL protocol, while CBF Mayo Clinic, United States and mean transit time (MTT) maps were derived by CTP measurements. Based on Xin Liu, Foshan University, China the voxel level analysis, Pearson correlation coefficients were used to estimate the *Correspondence: associations between the two modalities in the gray matter, white matter, and whole Changzheng Shi brain of each subject. Moderate to high positive associations between ASL-CBF and [email protected] Liangping Luo CTP-CBF were acquired by voxel-level-wise analysis in the gray matter, white matter, [email protected] and whole brain of the enrolled patients (all P < 0.005), and the average Pearson †These authors have contributed correlation coefficients were 0.647, 0.585, and 0.646, respectively. Highly significant equally to this work positive correlations between ASL-ATT and CTP-MTT were obtained by voxel-level-wise Received: 02 June 2021 associations in the gray matter, white matter, and whole brain (all P < 0.005), and the Accepted: 28 June 2021 average Pearson correlation coefficients were 0.787, 0.707, and 0.799, respectively. In Published: 11 August 2021 addition, significant associations between ASL and CT perfusion were obtained in the Citation: Xu X, Tan Z, Fan M, Ma M, gray, white matter and whole brain, according to the subgroup analyses of patient’s age Fang W, Liang J, Xiao Z, Shi C and and disease stage. There is a correlation between perfusion parameters from multi-delay Luo L (2021) Comparative Study pCASL and CT perfusion imaging in patients with ischemic stroke. Multi-delay pCASL of Multi-Delay Pseudo-Continuous Arterial Spin Labeling Perfusion MRI is radiation-free and non-invasive, and could be an alternative method to CT scans for and CT Perfusion in Ischemic Stroke assessing perfusion in ischemic stroke disease. Disease. Front. Neuroinform. 15:719719. Keywords: ischemic stroke, pseudo-continuous arterial spin labeling, CT perfusion, cerebral blood flow, arterial doi: 10.3389/fninf.2021.719719 transit time, mean transit time Frontiers in Neuroinformatics| www.frontiersin.org 1 August 2021| Volume 15| Article 719719 fninf-15-719719 August 11, 2021 Time: 12:53 # 2 Xu et al. pCASL in Ischemic Patients INTRODUCTION The Global Burden of Disease Study in 2015 provided a comprehensive assessment of 249 all-cause and cause-specific deaths across 195 countries and regions from 1980 to 2015; stroke was determined to be the second-leading cause of death worldwide (Wang et al., 2016). The 2019 statistical report from the American Heart Association on heart disease and stroke revealed that approximately 795,000 people experience a new or recurrent stroke each year (Benjamin et al., 2019). With the aging of the population, stroke has gradually become a leading cause of death and disability among adults in China. The social burden of stroke has gradually increased because of the increased morbidity and mortality (Vilela and Rowley, 2017). Stroke is a type of cerebrovascular disease characterized by the symptoms of cerebral ischemia or cerebral hemorrhage, and cerebral ischemia is the main cause of stroke (Benjamin et al., 2019). Early diagnosis and appropriate treatment of the disease can effectively improve the prognosis of patients. MRI and CT are routine imaging modalities that play important roles in evaluating the brain condition of patients. Because of the pathophysiological changes in stroke patients, the assessment FIGURE 1 | Flowchart of the comparison between ASL and CT perfusion. of microcirculation and cerebral perfusion is of great value for diagnosis and treatment. The development of CT image analysis to assess the function used to investigate the accuracy of multi-delay pCASL perfusion of different organs (e.g., brain, heart, carotid artery, etc.) MRI for estimating cerebral perfusion in ischemic stroke patients, constitutes a promising strategy for evaluating normal and using CTP as the reference standard. In this study, we aimed to abnormal physiology (Xu et al., 2018; Zhang et al., 2018). explore the feasibility and clinical utility of multi-delay pCASL by As known errors are associated with bolus-based perfusion comparison with CTP imaging in ischemic stroke. measurements (Wintermark et al., 2005), CT perfusion (CTP) is not regarded as the gold standard for calculating hemodynamic parameters. However, it is routinely used in clinical practice MATERIALS AND METHODS for perfusion evaluation, because it provides relatively accurate hemodynamic parameters, such as cerebral blood flow (CBF) and Patients mean transit time (MTT). It’s noting that the radiation damage The study was conducted in accordance with the principles of and contrast medium may not be suitable for some individuals. the Declaration of Helsinki, and the study protocol was approved Arterial spin labeling (ASL) perfusion MRI has gradually applied by the institutional review board of our hospital. A total of 21 in the clinic without radiation damage. Previously studies patients with ischemic stroke [18 men and 3 women; median age, have generally adopted a single post-labeling delay (PLD) time 62 years (age range, 37–84 years)] were enrolled between June (Wang et al., 2014), typically between 1.5 and 2 s, which may 2017 and March 2018. All patients underwent multi-delay pCASL underestimate perfusion due to prolonged arterial transit time and CTP examinations (Figure 1). (ATT) in ischemic stroke (MacIntosh et al., 2010). In recent The inclusion criteria were as follows: (1) All patients were years, multi-delay ASL sequences have been used to overcome confirmed as ischemic stroke according to clinical symptoms and this limitation. Wang et al.(2014) concluded the correlations imaging diagnosis (MRI or CT images); (2) To reduce additional between multi-delay pCASL and CTP in moyamoya disease, CT-associated radiation damage, patients who required CTP and indicated ASL could be a part of neuroimaging protocols examination based on their condition were enrolled in the study; in the moyamoya disease. They advised warranted studies of (3) Both CTP and ASL examinations were performed within 24 h. ischemic stroke, as the radiation-free and non-invasive ASL can The exclusion criteria were as follows: (1) Patients complicated provide perfusion information without the use of contrast agent. with severe parenchymal organ disease (heart, lung, liver and MacIntosh et al.(2010) adopted multi-delay pCASL (PLD times kidney); (2) Patients complicated with brain trauma, brain were set between 500 ms and 2,500 ms, a total of 9 intervals) tumor, intracranial hemorrhages, craniocerebral infection and in patients with acute ischemic stroke in a recent research. other mixed factors; (3) Patients with a cardiac pacemaker, non- Wang et al.(2013) made a comparison between multi-delay titanium alloy stent or internal plate fixation in vivo; (4) Unable ASL perfusion MRI and dynamic susceptibility contrast (DSC) to complete the examination due to claustrophobia. enhanced perfusion imaging in acute ischemic stroke disease. The results showed highly correlations between pCASL and DSC CBF Image Acquisition measurements. In our study, a wider range of PLD times was All included patients underwent CTP on a Toshiba Aquilion One adopted, totally 6 PLD times between 1,000 and 3,500 ms were scanner, which was set at 112∼187 mA and 80 kV. And the Frontiers in Neuroinformatics| www.frontiersin.org 2 August 2021| Volume 15| Article 719719 fninf-15-719719 August 11, 2021 Time: 12:53 # 3 Xu et al. pCASL in Ischemic Patients minimum section thickness was 0.5 mm. CTP scan was initiated TABLE 1 | clinical characteristics of patients at admission (n = 21). after injection of non-ionic iodinated contrast agent (Ultravist, Variable Patients (n = 21) 370 mg I/L; 50 ml at a rate of 6 ml/s) and physiological saline (30 ml at rate of 6 ml/s), using a power injector. The dynamic Patient demographics volume scan mode was turned on immediately after a delay of Median age, years (range) 62 (37–84) 7 s following the intravenous injection of contrast agent. The first Male (n,%) 18 (86) period was used as a mask; 11–36 s was used for the arterial phase, Female (n,%) 3 (14) and continuous scanning was performed at intervals of 2 s; 40– Disease stage 60 s was used for the venous phase for continuous scanning at Acute stage (n,%) 5 (24) intervals of 5 s.
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