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Increased Extracellular Fluid Is Associated with White Matter Fiber Yu et al. Fluids Barriers CNS (2021) 18:29 https://doi.org/10.1186/s12987-021-00264-1 Fluids and Barriers of the CNS RESEARCH Open Access Increased extracellular fuid is associated with white matter fber degeneration in CADASIL: in vivo evidence from difusion magnetic resonance imaging Xinfeng Yu1†, Xinzhen Yin2†, Hui Hong1, Shuyue Wang1, Yeerfan Jiaerken1, Fan Zhang3, Ofer Pasternak3,4, Ruiting Zhang1, Linglin Yang5, Min Lou2, Minming Zhang1* and Peiyu Huang1* Abstract Background: White matter hyperintensities (WMHs) are one of the hallmarks of cerebral small vessel disease (CSVD), but the pathological mechanisms underlying WMHs remain unclear. Recent studies suggest that extracellular fuid (ECF) is increased in brain regions with WMHs. It has been hypothesized that ECF accumulation may have detrimental efects on white matter microstructure. To test this hypothesis, we used cerebral autosomal-dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL) as a unique CSVD model to investigate the relationships between ECF and fber microstructural changes in WMHs. Methods: Thirty-eight CADASIL patients underwent 3.0 T MRI with multi-model sequences. Parameters of free water (FW) and apparent fber density (AFD) obtained from difusion-weighted imaging (b 0 and 1000 s/mm2) were respectively used to quantify the ECF and fber density. WMHs were split into four subregions= with four levels of FW using quartiles (FWq1 to FWq4) for each participant. We analyzed the relationships between FW and AFD in each subregion of WMHs. Additionally, we tested whether FW of WMHs were associated with other accompanied CSVD imaging markers including lacunes and microbleeds. Results: We found an inverse correlation between FW and AFD in WMHs. Subregions of WMHs with high-level of FW (FWq3 and FWq4) were accompanied with decreased AFD and with changes in FW-corrected difusion tensor imag- ing parameters. Furthermore, FW was also independently associated with lacunes and microbleeds. Conclusions: Our study demonstrated that increased ECF was associated with WM degeneration and the occur- rence of lacunes and microbleeds, providing important new insights into the role of ECF in CADASIL pathology. Improving ECF drainage might become a therapeutic strategy in future. Keywords: White matter, Extracellular fuid, Cerebral small vessel diseases, CADASIL, MRI, Difusion-weighted imaging Introduction White matter hyperintensities (WMHs) on MRI scans *Correspondence: [email protected]; [email protected]; are one of the hallmarks of cerebral small vessel disease [email protected]; [email protected] †Xinfeng Yu and Xinzhen Yin contributed equally (CSVD), which are associated with cognitive impair- 1 Department of Radiology, The 2nd Afliated Hospital, Zhejiang ment, dementia, stroke and even death [1–3]. However, University School of Medicine, No.88 Jiefang Road, Shangcheng District, the pathological mechanisms leading to WMHs remain Hangzhou 310009, China Full list of author information is available at the end of the article unclear. WMHs are the earliest and most frequent © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Yu et al. Fluids Barriers CNS (2021) 18:29 Page 2 of 13 observed imaging feature in cerebral autosomal-domi- difusion metrics (including AFD and FW-corrected nant arteriopathy with subcortical infarcts and leukoen- DTI metrics). Given that WMHs commonly accompany cephalopathy (CADASIL) [4] which is a monogenic lacunes and microbleeds, we further explored the cor- CSVD caused by Notch 3 gene mutations [5]. Unlike spo- relations between ECF in WMHs with both lacunes and radic CSVD, the occurrence and progression of WMHs microbleeds. are less dependent on cardiovascular risk factors and age in CADASIL [6]. Terefore, CADASIL could serve as a Methods unique model for investigating the pathological mecha- Participants nisms of WMHs. Te study was approved by the Medical Ethics Commit- Accumulating studies of CADASIL provide the evi- tee of the Second Afliated Hospital, Zhejiang University dence that WMHs are strongly related to increased School of Medicine and written informed consent was extracellular fuid (ECF). For example, a neuropathologi- obtained from all subjects. We enrolled 38 patients with cal study has demonstrated that WMHs in the anterior CADASIL. Te diagnosis of CADASIL was confrmed by temporal lobe of CADASIL refect fuid accumulation in genetic testing with a pathogenic mutation in the Notch enlarged perivascular spaces (PVS), together with the loss 3 gene which has been described in our previous study of WM [7]. A recent study of CADASIL patients reveals [15]. Te following clinical variables were documented that changes in difusion MRI signals within WMHs are for each subject: age, gender, the history of hypertension, mainly driven by increased extracellular free water [8]. diabetes mellitus, hyperlipidemia, and smoking. In addi- Furthermore, ECF are diferentially distributed in the tion, the presence/absence of symptoms including tran- WMHs, with higher ECF in specifc regions of WMHs sient ischemic attack/stroke, headache, psychiatric and such as anterior temporal lobe [9]. However, the asso- cognitive impairments were also recorded. Te disease ciation between increased ECF and white matter (WM) duration was defned as the length of time between initial microstructural changes in WMHs has not yet been symptom onset and brain MRI examination. determined. It has been argued that increased ECF would result in a build-up of substances toxic (e.g., plasma pro- Data acquisition teins) to the WM microstructure [10, 11]. Although dif- All patients were examined using a 3.0 T whole body- fusion tensor imaging (DTI) is a well-established method scanner (Discovery MR750, GE Healthcare, Milwaukee, for quantifying microstructural WM alterations in vivo, WI) equipped with an 8-channel phased array head coil. the model ftting would be largely infuenced by the Te details of MR sequence are shown in Additional extracellular water and intravoxel crossing fbers which fle 1: Methods. happen to be seen in WMHs [12]. Recent difusion MRI methods applying novel post- Image processing processing approaches can be used to achieve more direct Overview of the image processing pipeline for each sub- in vivo characterization of both intra- and extracellular ject is shown in Fig. 1. properties of WM tissue. For example, free water (FW) imaging using bi-tensor model could potentially separate Difusion preprocessing the difusion signals from extracellular FW and tissue Te preprocessing steps of difusion data included compartment [13]. Apparent fber density (AFD) imaging denoising, eddy-current and echo-planar imaging (EPI) using constrained spherical deconvolution (CSD) allows distortion correction and motion correction, gibbs ring- the resolution of crossing fbers in voxels containing mul- ing removal, bias-feld correction. In addition to EPI dis- tiple fber orientations, and it could estimates the fraction tortion, the preprocessing steps were processed using of space occupied by a fber bundle [14]. a combination of commands in the MRtrix3 package, In this study, in a cohort of patients with CADASIL, we FMRIB Software Library (FSL) and Advanced Normali- characterized the ECF (indexed by FW) and fber density zation Tools (ANTs). Te EPI distortion was corrected (indexed by AFD) in WMHs using the two advanced dif- using the bdp correction algorithm implemented in the fusion approaches. We hypothesized that increased ECF BrainSuite software package (https:// brain suite. org). would be associated with fber microstructural changes in WMHs. Considering the heterogeneity of ECF distri- Free water estimation bution in WMHs, we classifed FW in individual WMHs FW analysis has been described in detail elsewhere [8, into four levels using quartiles and used lesion probabil- 13, 16]. Briefy, the preprocessed difusion data was ft- ity map (LPM) to understand the distribution of diferent ted with a bi-tensor model within each voxel: the frst one levels of ECF in WMHs. We analyzed the relationships models FW difusion, defning as an isotropic difusion, between diferent levels of ECF and microstructural and the second one models the tissue compartment. Te Yu et al. Fluids Barriers CNS (2021) 18:29 Page 3 of 13 Fig. 1 Overview of the image processing pipeline for each subject. A The single-shell difusion data (b 0, 1000 s/mm2) were preprocessed and = then were separately ftted into bi-tensor, single tensor and CSD models. The difusion parameters including FW, FW-corrected DTI metrics (FAt, MDt, ADt, RDt) and conventional DTI metrics (FA, MD, AD, RD) were estimated. B WMHs mask was created by FLAIR image using the toolbox of LST in SPM12 and WM mask was generated from T1 image using FSL FAST. Both masks of WMHs and WM were co-registered into the individual b 0 s/mm2 (b0) image using ANTs. Then, NAWM was made by subtracting the WMHs mask from the WM mask, and it was subsequently eroded = by two voxels to avoid partial volume efects. C The mask of WMHs was split into four sub-masks with using FW quartiles.
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