Abstract
Purpose
The method of diffusion tensor image analysis along the perivascular space (DTI-ALPS) was gathering attention to evaluate the brain’s glymphatic function or interstitial fluid dynamics. However, to the best knowledge, no study was conducted on the reproducibility of these automated methods for ALPS index values. Therefore, the current study evaluated the ALPS index reproducibility based on DTI-ALPS using two major automated calculation techniques in scan and rescan of the same subject on the same day.
Materials and methods
This study included 23 participants, including 2 with Alzheimer’s disease, 15 with mild cognitive impairment, and 6 with cognitive normals. Scan and rescan data of diffusion magnetic resonance images were obtained, as well as automatically index for ALPS (ALPS index) and ALPS index maintaining tensor vector orientation information (vALPS index) with region of interest on the template fractional anisotropy map calculated by FSL software.These ALPS indices were compared in terms of scan and rescan reproducibility.
Results
The absolute difference in ALPS-index values between scan and rescan was larger in the ALPS index than in the vALPS index by approximately 0.6% as the relative difference. Cohen’s d for the left and right ALPS indices between methods were 0.121 and 0.159, respectively.
Conclusion
The vALPS index based on DTI-ALPS maintaining tensor vector orientation information has higher reproducibility than the ALPS index. This result encourages a multisite study on the ALPS index with a large sample size and helps detect a subtle pathological change in the ALPS index.
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References
Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci Transl Med. 2012;4:147ra111.
Kress BT, Iliff JJ, Xia M, Wang M, Wei HS, Zeppenfeld D, et al. Impairment of paravascular clearance pathways in the aging brain. Ann Neurol. 2014;76:845–61.
Gaberel T, Gakuba C, Goulay R, Martinez De Lizarrondo S, Hanouz J-L, Emery E, et al. Impaired glymphatic perfusion after strokes revealed by contrast-enhanced MRI: a new target for fibrinolysis? Stroke. 2014;45:3092–6.
Iliff JJ, Lee H, Yu M, Feng T, Logan J, Nedergaard M, et al. Brain-wide pathway for waste clearance captured by contrast-enhanced MRI. J Clin Invest. 2013;123:1299–309.
Siebner HR, von Einsiedel HG, Conrad B. Magnetic resonance ventriculography with gadolinium DTPA: report of two cases [Internet]. Neuroradiology. 1997. https://doi.org/10.1007/s002340050436.
Taoka T, Masutani Y, Kawai H, Nakane T, Matsuoka K, Yasuno F, et al. Evaluation of glymphatic system activity with the diffusion MR technique: diffusion tensor image analysis along the perivascular space (DTI-ALPS) in Alzheimer’s disease cases. Jpn J Radiol. 2017;35:172–8.
Taoka T, Fukusumi A, Miyasaka T, Kawai H, Nakane T, Kichikawa K, et al. Structure of the medullary veins of the cerebral hemisphere and related disorders. Radiographics. 2017;37:281–97.
Bae YJ, Choi BS, Kim J-M, Choi J-H, Cho SJ, Kim JH. Altered glymphatic system in idiopathic normal pressure hydrocephalus. Parkinsonism Relat Disord. 2021;82:56–60.
Chen H-L, Chen P-C, Lu C-H, Tsai N-W, Yu C-C, Chou K-H, et al. Associations among cognitive functions, plasma DNA, and diffusion tensor image along the perivascular space (DTI-ALPS) in patients with Parkinson’s disease. Oxid Med Cell Longev. 2021;2021:4034509.
Steward CE, Venkatraman VK, Lui E, Malpas CB, Ellis KA, Cyarto EV, et al. Assessment of the DTI-ALPS parameter along the perivascular space in older adults at risk of dementia. J Neuroimaging. 2021;31:569–78.
Toh CH, Castillo M. Peritumoral brain edema volume in meningioma correlates with tumor fractional anisotropy but not apparent diffusion coefficient or cerebral blood volume. Neuroradiology. 2021;63:1263–70.
Yang G, Deng N, Liu Y, Gu Y, Yao X. Evaluation of glymphatic system using diffusion MR technique in T2DM cases. Front Hum Neurosci. 2020;14:300.
Yokota H, Vijayasarathi A, Cekic M, Hirata Y, Linetsky M, Ho M, et al. Diagnostic performance of glymphatic system evaluation using diffusion tensor imaging in idiopathic normal pressure hydrocephalus and mimickers. Curr Gerontol Geriatr Res. 2019;2019:5675014.
Zhang W, Zhou Y, Wang J, Gong X, Chen Z, Zhang X, et al. Glymphatic clearance function in patients with cerebral small vessel disease. Neuroimage. 2021;238: 118257.
Zhou W, Shen B, Shen W-Q, Chen H, Zheng Y-F, Fei J-J. Dysfunction of the glymphatic system might be related to iron deposition in the normal aging brain. Front Aging Neurosci. 2020;12: 559603.
Zhang Y, Zhang R, Ye Y, Wang S, Jiaerken Y, Hong H, et al. The influence of demographics and vascular risk factors on glymphatic function measured by diffusion along perivascular space. Front Aging Neurosci. 2021;13: 693787.
Carotenuto A, Cacciaguerra L, Pagani E, Preziosa P, Filippi M, Rocca MA. Glymphatic system impairment in multiple sclerosis: relation with brain damage and disability. Brain Oxf Acad. 2021;145:2785–95.
Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12:189–98.
Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. 2005;53:695–9.
Pfeffer RI, Kurosaki TT, Harrah CH Jr, Chance JM, Filos S. Measurement of functional activities in older adults in the community. J Gerontol. 1982;37:323–9.
Tournier J-D, Smith R, Raffelt D, Tabbara R, Dhollander T, Pietsch M, et al. MRtrix3: a fast, flexible and open software framework for medical image processing and visualisation. Neuroimage. 2019;202: 116137.
Cordero-Grande L, Christiaens D, Hutter J, Price AN, Hajnal JV. Complex diffusion-weighted image estimation via matrix recovery under general noise models. Neuroimage. 2019;200:391–404.
Kellner E, Dhital B, Kiselev VG, Reisert M. Gibbs-ringing artifact removal based on local subvoxel-shifts. Magn Reson Med. 2016;76:1574–81.
Graham MS, Drobnjak I, Jenkinson M, Zhang H. Quantitative assessment of the susceptibility artefact and its interaction with motion in diffusion MRI. PLoS ONE. 2017;12: e0185647.
Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM. FSL. Neuroimage. 2012;62:782–90.
Cohen J. A power primer. Psychol Bull. 1992;112:155–9.
Taoka T, Ito R, Nakamichi R, Kamagata K, Sakai M, Kawai H, et al. Reproducibility of diffusion tensor image analysis along the perivascular space (DTI-ALPS) for evaluating interstitial fluid diffusivity and glymphatic function: CHanges in Alps index on Multiple conditiON acquIsition eXperiment (CHAMONIX) study. Jpn J Radiol. 2022;40:147–58.
Alexander DC, Pierpaoli C, Basser PJ, Gee JC. Spatial transformations of diffusion tensor magnetic resonance images. IEEE Trans Med Imaging. 2001;20:1131–9.
Tatekawa H, Matsushita S, Ueda D, et al. Improved reproducibility of diffusion tensor image analysis along the perivascular space (DTI-ALPS) index: an analysis of reorientation technique of the OASIS-3 dataset. Jpn J Radiol. 2023;41(4):393–400. https://doi.org/10.1007/s11604-022-01370-2
McKnight CD, Trujillo P, Lopez AM, Petersen K, Considine C, Lin Y-C, et al. Diffusion along perivascular spaces reveals evidence supportive of glymphatic function impairment in Parkinson disease. Parkinsonism Relat Disord. 2021;89:98–104.
Nguchu BA, Zhao J, Wang Y, de Dieu UJ, Wang X, Qiu B, et al. Altered glymphatic system in middle-aged cART-treated patients with HIV: a diffusion tensor imaging study. Front Neurol. 2022;13: 819594.
Lee DA, Lee H-J, Park KM. Normal glymphatic system function in patients with migraine: A pilot study. Headache. 2022;62:718–25.
Lee DA, Park BS, Park S, Lee YJ, Ko J, Park KM. Glymphatic system function in patients with transient global amnesia. J Integr Neurosci. 2022;21:117.
Acknowledgements
This work was supported by JSPS KAKENHI Grant Number JP22H04926, 18K18164, and 21K12153. Data collection and sharing for this project was funded by the Alzheimer's Disease Neuroimaging Initiative (ADNI) (National Institutes of Health Grant U01 AG024904) and DOD ADNI (Department of Defense award number W81XWH-12-2-0012). ADNI is funded by the National Institute on Aging, the National Institute of Biomedical Imaging and Bioengineering, and through generous contributions from the following: AbbVie, Alzheimer's Association; Alzheimer's Drug Discovery Foundation; Araclon Biotech; BioClinica, Inc.; Biogen; Bristol-Myers Squibb Company; CereSpir, Inc.; Cogstate; Eisai Inc.; Elan Pharmaceuticals, Inc.; Eli Lilly and Company; EuroImmun; F. Hoffmann-La Roche Ltd and its affiliated company Genentech, Inc.; Fujirebio; GE Healthcare; IXICO Ltd.;Janssen Alzheimer Immunotherapy Research & Development, LLC.; Johnson & Johnson Pharmaceutical Research & Development LLC.; Lumosity; Lundbeck; Merck & Co., Inc.;Meso Scale Diagnostics, LLC.; NeuroRx Research; Neurotrack Technologies; Novartis Pharmaceuticals Corporation; Pfizer Inc.; Piramal Imaging; Servier; Takeda Pharmaceutical Company; and Transition Therapeutics. The Canadian Institutes of Health Research is providing funds to support ADNI clinical sites in Canada. Private sector contributions are facilitated by the Foundation for the National Institutes of Health (www.fnih.org). The grantee organization is the Northern California Institute for Research and Education, and the study is coordinated by the Alzheimer's Therapeutic Research Institute at the University of Southern California. ADNI data are disseminated by the Laboratory for Neuro Imaging at the University of Southern California.
Funding
Data collection and sharing for this project were funded by the ADNI (National Institutes of Health grant no. U01 AG024904) and Department of Defense ADNI (Department of Defense award number W81XWH-12-2-0012). This study was partially supported by the Juntendo Research Branding Project, JSPS KAKENHI I (grant nos. 16H06280, 18K18164, 18H02772, 19K17244, 21K07690, 21K12153, 22H04926, 23H02865), a Grant-in-Aid for Special Research in Subsidies for ordinary expenses of private schools from The Promotion and Mutual Aid Corporation for Private Schools of Japan, the Brain/MINDS Beyond program (grant no. JP19dm0307101) of the Japan Agency for Medical Research and Development (AMED), and AMED under grant number JP21wm0425006.
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This article used open-source data from the ADNI 3 brain project (https://adni.loni.usc.edu/adni-3/) and did not involve studies with human participants or animals performed by the authors at our institution.
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Saito, Y., Kamagata, K., Andica, C. et al. Reproducibility of automated calculation technique for diffusion tensor image analysis along the perivascular space. Jpn J Radiol 41, 947–954 (2023). https://doi.org/10.1007/s11604-023-01415-0
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DOI: https://doi.org/10.1007/s11604-023-01415-0