RSS-Feed abonnieren
DOI: 10.1055/a-2254-5651
Perivascular spaces and where to find them – MR imaging and evaluation methods
Artikel in mehreren Sprachen: English | deutsch
Abstract
Background Perivascular spaces (synonym: Virchow-Robin spaces) were first described over 150 years ago. They are defined as the fluid-filled spaces surrounding the small penetrating cerebral vessels. They gained growing scientific interest especially with the postulation of the so-called glymphatic system and their possible role in neurodegenerative and neuroinflammatory diseases.
Methods PubMed was used for a systematic search with a focus on literature regarding MRI imaging and evaluation methods of perivascular spaces. Studies on human in-vivo imaging were included with a focus on studies involving healthy populations. No time frame was set. The nomenclature in the literature is very heterogeneous with terms like “large”, “dilated”, “enlarged” perivascular spaces whereas borders and definitions often remain unclear. This work generally talks about perivascular spaces.
Results This review article discusses the morphologic MRI characteristics in different sequences. With the continual improvement of image quality, more and tinier structures can be depicted in detail. Visual analysis and semi or fully automated segmentation methods are briefly discussed.
Conclusion If they are looked for, perivascular spaces are apparent in basically every cranial MRI examination. Their physiologic or pathologic value is still under debate.
Key Points
-
Perivascular spaces can be seen in basically every cranial MRI examination.
-
Primarily T2-weighend sequences are used for visual analysis. Additional sequences are helpful for distinction from their differential diagnoses.
-
There are promising approaches for the semi or fully automated segmentation of perivascular spaces with the possibility to collect more quantitative parameters.
Citation Format
-
Seehafer S, Larsen N, Aludin S et al. Perivascular spaces and where to find them – MRI imaging and evaluation methods. Fortschr Röntgenstr 2024; 196: 1029 – 1036
Publikationsverlauf
Eingereicht: 06. November 2023
Angenommen: 20. Dezember 2023
Artikel online veröffentlicht:
26. Februar 2024
© 2024. Thieme. All rights reserved.
Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany
-
References
- 1 Durand-Fardel M. Traite du ramollissement du cerveau. Paris: Balliere; 1843
- 2 Virchow R. Ueber die Erweiterung kleinerer Gefäße. 1851
- 3 Robin Ch. Recherches sur quelques particularités de la structure des capillaires de l’encéphale, Journal de physiologie. 1859
- 4 Iliff JJ, Wang M, Liao Y. 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
- 5 Zhu Y-C, Dufouil C, Mazoyer B. et al. Frequency and location of dilated Virchow-Robin spaces in elderly people: a population-based 3D MR imaging study. AJNR Am J Neuroradiol 2011; 32: 709-713
- 6 Zong X, Park SH, Shen D. et al. Visualization of perivascular spaces in the human brain at 7T: sequence optimization and morphology characterization. Neuroimage 2016; 125: 895-902
- 7 Bouvy WH, Biessels GJ, Kuijf HJ. et al. Visualization of Perivascular Spaces and Perforating Arteries With 7 T Magnetic Resonance Imaging. Invest Radiol 2014; 49: 307-313
- 8 Cai K, Tain R, Das S. et al. The feasibility of quantitative MRI of perivascular spaces at 7T. J Neurosci Methods 2015; 256: 151-156
- 9 Tsutsumi S, Ono H, Ishii H. et al. Visualization of the periventricular Virchow-Robin spaces with ependymal openings. Childs Nerv Syst 2018; 34: 1529-1533
- 10 Saeki N, Sato M, Kubota M. et al. MR imaging of normal perivascular space expansion at midbrain. AJNR Am J Neuroradiol 2005; 26 (03) 566-571
- 11 Perosa V, Oltmer J, Munting LP. et al. Perivascular space dilation is associated with vascular amyloid-β accumulation in the overlying cortex. Acta Neuropathol 2022; 143: 331-348
- 12 Wardlaw JM, Smith EE, Biessels GJ. et al. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. The Lancet Neurology 2013; 12: 822-838
- 13 Cerase A, Vallone IM, Muccio CF. et al. Regression of dilated perivascular spaces of the brain. Surg Radiol Anat 2010; 32: 555-561
- 14 Taydas O, Erarslan Y, Ates OF. et al. Tumefactive perivascular space demonstrated with post-contrast time-of-flight MR angiography. Neurochirurgie 2020; 66: 50-52
- 15 Jochems ACC, Blair GW, Stringer MS. et al. Relationship Between Venules and Perivascular Spaces in Sporadic Small Vessel Diseases. Stroke 2020; 51: 1503-1506
- 16 George IC, Arrighi-Allisan A, Delman BN. et al. A Novel Method to Measure Venular Perivascular Spaces in Patients with MS on 7T MRI. AJNR Am J Neuroradiol 2021; 42: 1069-1072
- 17 Awad IA, Johnson PC, Spetzler RF. et al. Incidental subcortical lesions identified on magnetic resonance imaging in the elderly. II. Postmortem pathological correlations. Stroke 1986; 17: 1090-1097
- 18 Oztürk MH, Aydingöz U. Comparison of MR signal intensities of cerebral perivascular (Virchow-Robin) and subarachnoid spaces. J Comput Assist Tomogr 2002; 26: 902-904
- 19 Naganawa S, Nakane T, Kawai H. et al. Differences in Signal Intensity and Enhancement on MR Images of the Perivascular Spaces in the Basal Ganglia versus Those in White Matter. Magn Reson Med Sci 2018; 17: 301-307
- 20 Deike-Hofmann K, Reuter J, Haase R. et al. Glymphatic Pathway of Gadolinium-Based Contrast Agents Through the Brain: Overlooked and Misinterpreted. Invest Radiol 2019; 54: 229-237
- 21 Naganawa S, Nakane T, Kawai H. et al. Gd-based Contrast Enhancement of the Perivascular Spaces in the Basal Ganglia. Magn Reson Med Sci 2017; 16: 61-65
- 22 Sepehrband F, Barisano G, Sheikh-Bahaei N. et al. Image processing approaches to enhance perivascular space visibility and quantification using MRI. Sci Rep 2019; 9
- 23 Taoka T, Masutani Y, Kawai H. 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: 172-178
- 24 Taoka T, Ito R, Nakamichi R. et al. Diffusion-weighted image analysis along the perivascular space (DWI-ALPS) for evaluating interstitial fluid status: age dependence in normal subjects. Jpn J Radiol 2022; 40: 894-902
- 25 Choi Y, Nam Y, Choi Y. et al. MRI-visible dilated perivascular spaces in healthy young adults: A twin heritability study. Hum Brain Mapp 2020; 41: 5313-5324
- 26 Zhu Y-C, Tzourio C, Soumaré A. et al. Severity of dilated Virchow-Robin spaces is associated with age, blood pressure, and MRI markers of small vessel disease: a population-based study. Stroke 2010; 41: 2483-2490
- 27 Potter GM, Doubal FN, Jackson CA. et al. Enlarged Perivascular Spaces and Cerebral Small Vessel Disease. International Journal of Stroke 2015; 10: 376-381
- 28 Rajani RM, Ratelade J, Domenga-Denier V. et al. Blood brain barrier leakage is not a consistent feature of white matter lesions in CADASIL. Acta Neuropathol Commun 2019; 7: 187
- 29 Charidimou A, Boulouis G, Pasi M. et al. MRI-visible perivascular spaces in cerebral amyloid angiopathy and hypertensive arteriopathy. Neurology 2017; 88: 1157-1164
- 30 Gabrielli O, Polonara G, Regnicolo L. et al. Correlation between cerebral MRI abnormalities and mental retardation in patients with mucopolysaccharidoses. Am J Med Genet A 2004; 125A: 224-231
- 31 Kwee RM, Kwee TC. Virchow-Robin spaces at MR imaging. Radiographics 2007; 27: 1071-1086
- 32 Rawal S, Croul SE, Willinsky RA. et al. Subcortical cystic lesions within the anterior superior temporal gyrus: a newly recognized characteristic location for dilated perivascular spaces. AJNR Am J Neuroradiol 2014; 35: 317-322
- 33 Heier LA, Bauer CJ, Schwartz L. et al. Large Virchow-Robin spaces: MR-clinical correlation. AJNR Am J Neuroradiol 1989; 10: 929-936
- 34 Adams HHH, Cavalieri M, Verhaaren BFJ. et al. Rating method for dilated Virchow-Robin spaces on magnetic resonance imaging. Stroke 2013; 44: 1732-1735
- 35 Jungreis CA, Kanal E, Hirsch WL. et al. Normal perivascular spaces mimicking lacunar infarction: MR imaging. Radiology 1988; 169: 101-104
- 36 Groeschel S, Chong WK, Surtees R. et al. Virchow-Robin spaces on magnetic resonance images: normative data, their dilatation, and a review of the literature. Neuroradiology 2006; 48: 745-754
- 37 Salzman KL, Osborn AG, House P. et al. Giant tumefactive perivascular spaces. AJNR Am J Neuroradiol 2005; 26 (02) 298-305
- 38 Idiculla PS, Gurala D, Siddiqui JH. Giant tumefactive perivascular spaces: an incidental finding. Acta Neurol Belg 2020; 120: 1443-1444
- 39 Potter GM, Chappell FM, Morris Z. et al. Cerebral perivascular spaces visible on magnetic resonance imaging: development of a qualitative rating scale and its observer reliability. Cerebrovasc Dis 2015; 39: 224-231
- 40 Adams HH, Hilal S, Schwingenschuh P. et al. A priori collaboration in population imaging: The Uniform Neuro‐Imaging of Virchow‐Robin Spaces Enlargement consortium. Alzheimer’s & Dementia: Diagnosis, Assessment & Disease Monitoring 2015; 1: 513-520
- 41 Fazekas F, Chawluk JB, Alavi A. et al. MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. American Journal of Roentgenology 1987; 149: 351-356
- 42 Zdanovskis N, Platkājis A, Kostiks A. et al. Combined Score of Perivascular Space Dilatation and White Matter Hyperintensities in Patients with Normal Cognition, Mild Cognitive Impairment, and Dementia. Medicina (Kaunas) 2022; 58
- 43 Descombes X, Kruggel F, Wollny G. et al. An object-based approach for detecting small brain lesions: application to Virchow-Robin spaces. IEEE Trans Med Imaging 2004; 23: 246-255
- 44 Wang X, Del Valdés Hernández MC, Doubal F. et al. Development and initial evaluation of a semi-automatic approach to assess perivascular spaces on conventional magnetic resonance images. J Neurosci Methods 2016; 257: 34-44
- 45 Niazi M, Karaman M, Das S. et al. Quantitative MRI of Perivascular Spaces at 3T for Early Diagnosis of Mild Cognitive Impairment. AJNR Am J Neuroradiol 2018; 39: 1622-1628
- 46 Boespflug EL, Schwartz DL, Lahna D. et al. MR Imaging-based Multimodal Autoidentification of Perivascular Spaces (mMAPS): Automated Morphologic Segmentation of Enlarged Perivascular Spaces at Clinical Field Strength. Radiology 2018; 286: 632-642
- 47 Schwartz DL, Boespflug EL, Lahna DL. et al. Autoidentification of perivascular spaces in white matter using clinical field strength T1 and FLAIR MR imaging. Neuroimage 2019; 202: 116126
- 48 Frangi A, Niessen W, Vincken K. et al. M. Multiscale vessel enhancement filtering. Medical Image Computing and Computer-Assisted Intervention (MICCAI98). 1998: 130-137
- 49 Ballerini L, Lovreglio R, Del Valdés Hernández MC. et al. Perivascular Spaces Segmentation in Brain MRI Using Optimal 3D Filtering. Sci Rep 2018; 8: 2132
- 50 Bernal J, Valdés-Hernández MDC, Escudero J. et al. Assessment of perivascular space filtering methods using a three-dimensional computational model. Magn Reson Imaging 2022; 93: 33-51
- 51 Spijkerman JM, Zwanenburg J, Bouvy WH. et al. Automatic quantification of perivascular spaces in T2-weighted images at 7 T MRI. Cerebral Circulation – Cognition and Behavior 2022; 3: 100142
- 52 Hou Y, Park SH, Wang Q. et al. Enhancement of Perivascular Spaces in 7T MR Image using Haar Transform of Non-local Cubes and Block-matching Filtering. Sci Rep 2017; 7: 8569
- 53 Park SH, Zong X, Gao Y. et al. Segmentation of perivascular spaces in 7T MR image using auto-context model with orientation-normalized features. Neuroimage 2016; 134: 223-235
- 54 Zhang J, Gao Y, Park SH. et al. Structured Learning for 3-D Perivascular Space Segmentation Using Vascular Features. IEEE Trans Biomed Eng 2017; 64: 2803-2812
- 55 Boutinaud P, Tsuchida A, Laurent A. et al. 3D Segmentation of Perivascular Spaces on T1-Weighted 3 Tesla MR Images With a Convolutional Autoencoder and a U-Shaped Neural Network. Front. Neuroinform 2021; 15
- 56 Lian C, Zhang J, Liu M. et al. Multi-channel multi-scale fully convolutional network for 3D perivascular spaces segmentation in 7T MR images. Med Image Anal 2018; 46: 106-117
- 57 Dubost F, Yilmaz P, Adams H. et al. Enlarged perivascular spaces in brain MRI: Automated quantification in four regions. Neuroimage 2019; 185: 534-544