Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration

Joanna M Wardlaw, Eric E Smith, Geert J Biessels, Charlotte Cordonnier, Franz Fazekas, Richard Frayne, Richard I Lindley, John T O'Brien, Frederik Barkhof, Oscar R Benavente, Sandra E Black, Carol Brayne, Monique Breteler, Hugues Chabriat, Charles Decarli, Frank-Erik de Leeuw, Fergus Doubal, Marco Duering, Nick C Fox, Steven Greenberg, Vladimir Hachinski, Ingo Kilimann, Vincent Mok, Robert van Oostenbrugge, Leonardo Pantoni, Oliver Speck, Blossom C M Stephan, Stefan Teipel, Anand Viswanathan, David Werring, Christopher Chen, Colin Smith, Mark van Buchem, Bo Norrving, Philip B Gorelick, Martin Dichgans, STandards for ReportIng Vascular changes on nEuroimaging (STRIVE v1), Joanna M Wardlaw, Eric E Smith, Geert J Biessels, Charlotte Cordonnier, Franz Fazekas, Richard Frayne, Richard I Lindley, John T O'Brien, Frederik Barkhof, Oscar R Benavente, Sandra E Black, Carol Brayne, Monique Breteler, Hugues Chabriat, Charles Decarli, Frank-Erik de Leeuw, Fergus Doubal, Marco Duering, Nick C Fox, Steven Greenberg, Vladimir Hachinski, Ingo Kilimann, Vincent Mok, Robert van Oostenbrugge, Leonardo Pantoni, Oliver Speck, Blossom C M Stephan, Stefan Teipel, Anand Viswanathan, David Werring, Christopher Chen, Colin Smith, Mark van Buchem, Bo Norrving, Philip B Gorelick, Martin Dichgans, STandards for ReportIng Vascular changes on nEuroimaging (STRIVE v1)

Abstract

Cerebral small vessel disease (SVD) is a common accompaniment of ageing. Features seen on neuroimaging include recent small subcortical infarcts, lacunes, white matter hyperintensities, perivascular spaces, microbleeds, and brain atrophy. SVD can present as a stroke or cognitive decline, or can have few or no symptoms. SVD frequently coexists with neurodegenerative disease, and can exacerbate cognitive deficits, physical disabilities, and other symptoms of neurodegeneration. Terminology and definitions for imaging the features of SVD vary widely, which is also true for protocols for image acquisition and image analysis. This lack of consistency hampers progress in identifying the contribution of SVD to the pathophysiology and clinical features of common neurodegenerative diseases. We are an international working group from the Centres of Excellence in Neurodegeneration. We completed a structured process to develop definitions and imaging standards for markers and consequences of SVD. We aimed to achieve the following: first, to provide a common advisory about terms and definitions for features visible on MRI; second, to suggest minimum standards for image acquisition and analysis; third, to agree on standards for scientific reporting of changes related to SVD on neuroimaging; and fourth, to review emerging imaging methods for detection and quantification of preclinical manifestations of SVD. Our findings and recommendations apply to research studies, and can be used in the clinical setting to standardise image interpretation, acquisition, and reporting. This Position Paper summarises the main outcomes of this international effort to provide the STandards for ReportIng Vascular changes on nEuroimaging (STRIVE).

Copyright © 2013 Elsevier Ltd. All rights reserved.

Figures

Figure 1
Figure 1
Variable fates of lesions related to small vessel disease and the convergence of acute lesions with different causes but similar late appearances on MRI Arrows indicate possible late fates of acute MRI findings. Blue arrows indicate common fates of recent small subcortical infarcts, green arrows indicate less common fates, and red lines indicate least common late fates. ICH=intracranial haemorrhage.
Figure 2
Figure 2
MRI findings for lesions related to small vessel disease Shows examples (upper) and schematic representation (middle) of MRI features for changes related to small vessel disease, with a summary of imaging characteristics (lower) for individual lesions. DWI=diffusion-weighted imaging. FLAIR=fluid-attenuated inversion recovery. SWI=susceptibility-weighted imaging. GRE=gradient-recalled echo.
Figure 3
Figure 3
Secondary brain atrophy in a 55-year-old patient with documented small vessel disease Baseline (middle). The follow-up scan (T1-weighted MRI; right) shows clear sulcal widening (arrow B, C, and D), particularly in occipital regions, and ventricular enlargement (arrow A) without new infarctions during the observational period. Fluid-attenuated inversion recovery image (left) shows substantial white matter hyperintensity.

References

    1. Norrving B. Lacunar infarcts: no black holes in the brain are benign. Pract Neurol. 2008;8:222–228.
    1. Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol. 2010;9:689–701.
    1. Kivipelto M, Helkala EL, Laakso M. Midlife vascular risk factors and Alzheimer's disease in later life: longitudinal, population based study. BMJ. 2001;322:1447–1451.
    1. Dichgans M, Zietemann V. Prevention of vascular cognitive impairment. Stroke. 2012;43:3137–3146.
    1. Brayne C, Richardson K, Matthews FE. Neuropathological correlates of dementia in over-80-year-old brain donors from the population-based Cambridge City over-75s cohort (CC75C) study. J Alzheimers Dis. 2009;18:645–658.
    1. Matthews FE, Brayne C, Lowe J, McKeith I, Wharton SB, Ince P. Epidemiological pathology of dementia: attributable-risks at death in the Medical Research Council Cognitive Function and Ageing Study. PLoS Med. 2009;6:e1000180.
    1. Neuropathology Group of the Medical Research Council Cognitive function and ageing study (MRC CFAS) Lancet. 2001;357:169–175.
    1. Schneider JA, Arvanitakis Z, Bang W, Bennett DA. Mixed brain pathologies account for most dementia cases in community-dwelling older persons. Neurology. 2007;69:2197–2204.
    1. Potter GM, Marlborough FJ, Wardlaw JM. Wide variation in definition, detection, and description of lacunar lesions on imaging. Stroke. 2010;42:359–366.
    1. Zhu YC, Dufouil C, Tzourio C, Chabriat H. Silent brain infarcts: a review of MRI diagnostic criteria. Stroke. 2011;42:1140–1145.
    1. Hachinski V, Iadecola C, Petersen RC. National Institute of Neurological Disorders and Stroke–Canadian Stroke Network vascular cognitive impairment harmonization standards. Stroke. 2006;37:2220–2241.
    1. Gorelick PB, Scuteri A, Black SE. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2011;42:2672–2713.
    1. Editorial A united approach to vascular disease and neurodegeneration. Lancet Neurol. 2012;11:293.
    1. Kang DW, Han MK, Kim HJ. New ischemic lesions coexisting with acute intracerebral hemorrhage. Neurology. 2012;79:848–855.
    1. Chowdhury D, Wardlaw JM, Dennis MS. Are multiple acute small subcortical infarctions caused by embolic mechanisms? J Neurol Neurosurg Psychiatry. 2004;75:1416–1420.
    1. Doubal FN, Dennis MS, Wardlaw JM. Characteristics of patients with minor ischaemic strokes and negative MRI: a cross sectional study. J Neurol Neurosurg Psychiatry. 2011;82:540–542.
    1. Potter GM, Doubal FN, Jackson CA. Counting cavitating lacunes underestimates the burden of lacunar infarction. Stroke. 2010;41:267–272.
    1. Moreau F, Patel S, Lauzon ML. Cavitation after acute symptomatic lacunar stroke depends on time, location, and MRI sequence. Stroke. 2012;43:1837–1842.
    1. Koch S, McClendon MS, Bhatia R. Imaging evolution of lacunar stroke–leukoariosis or lacune? Neurology. 2011;77:1091–1095.
    1. Donnan GA, Bladin PF, Berkovic SF, Longley WA, Saling MM. The stroke syndrome of striatocapsular infarction. Brain. 1991;114:51–70.
    1. Fisher CM. Lacunar infarcts—a review. Cerebrovasc Dis. 1991;1:311–320.
    1. Vermeer SE, Longstreth WT, Jr, Koudstaal PJ. Silent brain infarcts: a systematic review. Lancet Neurol. 2007;6:611–619.
    1. Santos M, Gold G, Kovari E. Differential impact of lacunes and microvascular lesions on poststroke depression. Stroke. 2009;40:3557–3562.
    1. Choi P, Ren M, Phan TG. Silent infarcts and cerebral microbleeds modify the associations of white matter lesions with gait and postural stability: population-based study. Stroke. 2012;43:1505–1510.
    1. Snowdon DA, Greiner LH, Mortimer JA, Riley KP, Greiner PA, Markesbery WR. Brain infarction and the clinical expression of Alzheimer disease. The Nun Study. JAMA. 1997;277:813–817.
    1. Franke CL, van Swieten JC, van Gijn J. Residual lesions on computed tomography after intracerebral hemorrhage. Stroke. 1991;22:1530–1533.
    1. Vermeer SE, den Heijer T, Koudstaal PJ, Oudkerk M, Hofman A, Breteler MM. Incidence and risk factors of silent brain infarcts in the population-based Rotterdam Scan Study. Stroke. 2003;34:392–396.
    1. Longstreth WT, Jr, Bernick C, Manolio TA, Bryan N, Jungreis CA, Price TR. Lacunar infarcts defined by magnetic resonance imaging of 3660 elderly people. The Cardiovascular Health Study. Arch Neurol. 1998;55:1217–1225.
    1. Debette S, Markus HS. The clinical importance of white matter hyperintensities on brain magnetic resonance imaging: systematic review and meta-analysis. BMJ. 2010;341:c3666.
    1. Gouw AA, Seewann A, van der Flier WM. Heterogeneity of small vessel disease: a systematic review of MRI and histopathology correlations. J Neurol Neurosurg Psychiatry. 2011;82:126–135.
    1. de Laat KF, Tuladhar AM, van Norden AGW, Norris DG, Zwiers MP, de Leeuw F-E. Loss of white matter integrity is associated with gait disorders in cerebral small vessel disease. Brain. 2011;134:73–83.
    1. Windham BG, Griswold ME, Shibata D, Penman A, Catellier DJ, Mosley TH., Jr Covert neurological symptoms associated with silent infarcts from midlife to older age: the Atherosclerosis Risk in Communities study. Stroke. 2012;43:1218–1223.
    1. Saini M, Ikram K, Hilal S, Qiu A, Venketasubramanian N, Chen C. Silent stroke: not listened to rather than silent. Stroke. 2012;3:3102–3104.
    1. Haley AP, Hoth KF, Gunstad J. Subjective cognitive complaints relate to white matter hyperintensities and future cognitive decline in patients with cardiovascular disease. Am J Geriatr Psychiatry. 2009;17:976–985.
    1. Inzitari D, Pracucci G, Poggesi A. Changes in white matter as determinant of global functional decline in older independent outpatients: three year follow-up of LADIS (leukoaraiosis and disability) study cohort. BMJ. 2009;339:279–282.
    1. Hachinski VC, Potter P, Merskey H. Leukoaraiosis. Arch Neurol. 1987;44:21–23.
    1. Pollock H, Hutchings M, Weller RO, Zhang E-T. Perivascular spaces in the basal gangli of the human brain: their relationship to lacunes. J Anat. 1997;191:337–346.
    1. Groeschel S, Chong WK, Surtees R, Hanefeld F. Virchow-Robin spaces on magnetic resonance images: normative data, their dilatation, and a review of the literature. Neuroradiology. 2006;48:745–754.
    1. Doubal FN, MacLullich AM, Ferguson KJ, Dennis MS, Wardlaw JM. Enlarged perivascular spaces on MRI are a feature of cerebral small vessel disease. Stroke. 2010;41:450–454.
    1. Kwee RM, Kwee TC. Virchow-Robin spaces at MR imaging. Radiographics. 2007;27:1071–1086.
    1. Zhu YC, Tzourio C, Soumare A, Mazoyer B, Dufouil C, Chabriat H. 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.
    1. MacLullich AM, Wardlaw JM, Ferguson KJ, Starr JM, Seckl JR, Deary IJ. Enlarged perivascular spaces are associated with cognitive function in healthy elderly men. J Neurol Neurosurg Psychiatry. 2004;75:1519–1523.
    1. Poirier J, Derouesne C. Cerebral lacunae. A proposed new classification. Clin Neuropathol. 1984;3:266.
    1. Heier LA, Bauer CJ, Schwartz L, Zimmerman RD, Morgello S, Deck MDF. Large Virchow-Robin spaces: MR-clinical correlation. AJNR Am J Neuroradiol. 1989;10:929–936.
    1. Patankar TF, Mitra D, Varma A, Snowden J, Neary D, Jackson A. Dilatation of the Virchow-Robin space is a sensitive indicator of cerebral microvascular disease: study in elderly patients with dementia. AJNR Am J Neuroradiol. 2005;26:1512–1520.
    1. Rouhl RPW, van Oostenbrugge RJ, Knottnerus ILH, Staals JEA, Lodder J. Virchow-Robin spaces relate to cerebral small vessel disease severity. J Neurol. 2008;255:692–696.
    1. Zhu YC, Dufouil C, Mazoyer B. 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.
    1. Chen W, Song X, Zhang Y. Assessment of the Virchow-Robin Spaces in Alzheimer disease, mild cognitive impairment, and normal aging, using high-field MR imaging. AJNR Am J Neuroradiol. 2011;32:1490–1495.
    1. Braffman BH, Zimmerman RA, Trojanowski JQ, Gonatas NK, Hickey WF, Schlaepfer WW. Brain MR: pathologic correlation with gross and histopathology. 2. Hyperintense white-matter foci in the elderly. AJR Am J Roentgenol. 1988;151:559–566.
    1. Bokura H, Kobayashi S, Yamaguchi S. Distinguishing silent lacunar infarction from enlarged Virchow-Robin spaces: a magnetic resonance imaging and pathological study. J Neurol. 1998;245:116–122.
    1. Awad IA, Johnson PC, Spetzler RF, Hodak JA. Incidental subcortical lesions identified on magnetic resonance imaging in the elderly. II Postmortem pathological correlations. Stroke. 1986;17:1090–1097.
    1. Shoamanesh A, Kwok CS, Benavente O. Cerebral microbleeds: histopathological correlation of neuroimaging. Cerebrovasc Dis. 2011;32:528–534.
    1. De Reuck J, Auger F, Cordonnier C. Comparison of 7·0-T T*-magnetic resonance imaging of cerebral bleeds in post-mortem brain sections of Alzheimer patients with their neuropathological correlates. Cerebrovasc Dis. 2011;31:511–517.
    1. Fazekas F, Kleinert R, Roob G. Histopathologic analysis of foci of signal loss on gradient-echo T2*-weighted MR images in patients with spontaneous intracerebral hemorrhage: evidence of microangiopathy-related microbleeds. AJNR Am J Neuroradiol. 1999;20:637–642.
    1. Dichgans M, Holtmannspotter M, Herzog J, Peters N, Bergmann M, Yousry TA. Cerebral microbleeds in CADASIL: a gradient-echo magnetic resonance imaging and autopsy study. Stroke. 2002;33:67–71.
    1. Tatsumi S, Shinohara M, Yamamoto T. Direct comparison of histology of microbleeds with postmortem MR images: a case report. Cerebrovasc Dis. 2008;26:142–146.
    1. Cordonnier C, Al-Shahi Salman R, Wardlaw J. Spontaneous brain microbleeds: systematic review, subgroup analyses and standards for study design and reporting. Brain. 2007;130:1988–2003.
    1. Vernooij MW, van der Lugt A, Ikram MA. Prevalence and risk factors of cerebral microbleeds: the Rotterdam Scan Study. Neurology. 2008;70:1208–1214.
    1. Knudsen KA, Rosand J, Karluk D, Greenberg SM. Clinical diagnosis of cerebral amyloid angiopathy: validation of the Boston criteria. Neurology. 2001;56:537–539.
    1. Greenberg SM, Vernooij MW, Cordonnier C. Cerebral microbleeds: a guide to detection and interpretation. Lancet Neurol. 2009;8:165–174.
    1. Sperling RA, Jack CR, Jr, Black SE. Amyloid-related imaging abnormalities in amyloid-modifying therapeutic trials: recommendations from the Alzheimer's Association Research Roundtable Workgroup. Alzheimers Dement. 2011;7:367–385.
    1. Lammie GA, Lindley R, Keir S, Wiggam MI. Stress-related primary intracerebral hemorrhage: autopsy clues to underlying mechanism. Stroke. 2000;31:1426–1448.
    1. Broderick J, Connolly S, Feldmann E. Guidelines for the management of spontaneous intracerebral hemorrhage in adults: 2007 update: a guideline from the American Heart Association/American Stroke Association Stroke Council, High Blood Pressure Research Council, and the Quality of Care and Outcomes in Research Interdisciplinary Working Group. Stroke. 2007;38:2001–2202.
    1. Qureshi AI, Tuhrim S, Broderick JP, Batjer HH, Hondo H, Hanley DF. Spontaneous intracerebral hemorrhage. N Engl J Med. 2001;344:1450–1460.
    1. Jackson CA, Sudlow CL. Is hypertension a more frequent risk factor for deep than for lobar supratentorial intracerebral haemorrhage? J Neurol Neurosurg Psychiatry. 2006;77:1244–1252.
    1. Bhattathiri PS, Gregson B, Prasad KSM. Reliability assessment of computerized tomography scanning measurements in intracerebral hematoma. Neurosurg Focus. 2003;15:1–5.
    1. Linn J, Halpin A, Demaerel P. Prevalence of superficial siderosis in patients with cerebral amyloid angiopathy. Neurology. 2010;74:1346–1350.
    1. Kumar N, Cohen-Gadol AA, Wright RA, Miller GM, Piepgras DG, Ahlskog JE. Superficial siderosis. Neurology. 2006;66:1144–1152.
    1. Jack CR., Jr Alliance for aging research AD biomarkers work group: structural MRI. Neurobiol Aging. 2011;32:S48–S57.
    1. Walters RJ, Fox NC, Crum WR, Taube D, Thomas DJ. Haemodialysis and cerebral oedema. Nephron. 2001;87:143–147.
    1. Duning T, Kloska S, Steinstrater O, Kugel H, Heindel W, Knecht S. Dehydration confounds the assessment of brain atrophy. Neurology. 2005;64:548–550.
    1. Bobinski M, de Leon MJ, Wegiel J. The histological validation of post mortem magnetic resonance imaging-determined hippocampal volume in Alzheimer's disease. Neuroscience. 2000;95:721–725.
    1. Jagust WJ, Zheng L, Harvey DJ. Neuropathological basis of magnetic resonance images in aging and dementia. Ann Neurol. 2008;63:72–80.
    1. Black S, Gao F, Bilbao J. Understanding white matter disease. Imaging–pathological correlations in vascular cognitive impairment. Stroke. 2009;40:S48–S52.
    1. Appelman AP, Exalto LG, van der Graaf Y, Biessels GJ, Mali WP, Geerlings MI. White matter lesions and brain atrophy: more than shared risk factors? A systematic review. Cerebrovasc Dis. 2009;28:227–242.
    1. Aribisala BS, Valdes Hernandez MC, Royle NA. Brain atrophy associations with white matter lesions in the ageing brain: the Lothian Birth Cohort 1936. Eur Radiol. 2013;23:1084–1092.
    1. Mungas D, Jagust WJ, Reed BR. MRI predictors of cognition in subcortical ischemic vascular disease and Alzheimer's disease. Neurology. 2001;57:2229–2235.
    1. Levy-Cooperman N, Ramirez J, Lobaugh NJ, Black SE. Misclassified tissue volumes in Alzheimer disease patients with white matter hyperintensities: importance of lesion segmentation procedures for volumetric analysis. Stroke. 2008;39:1134–1141.
    1. Carmichael O, Schwarz C, Drucker D. Longitudinal changes in white matter disease and cognition in the first year of the Alzheimer disease neuroimaging initiative. Arch Neurol. 2010;67:1370–1378.
    1. Wardlaw JM, Brindle W, Casado AM. A systematic review of the utility of 1·5 versus 3 Tesla magnetic resonance brain imaging in clinical practice and research. Eur Radiol. 2012;22:2295–2303.
    1. Potter G, Doubal F, Jackson C, Sudlow C, Dennis M, Wardlaw J. Associations of clinical stroke misclassification (‘clinical–imaging dissociation’) in acute ischemic stroke. Cerebrovasc Dis. 2010;29:395–402.
    1. Valdes Hernandez MC, Morris Z, Dickie DA. Close correlation between quantitative and qualitative assessments of white matter lesions. Neuroepidemiology. 2012;40:13–22.
    1. Gao FQ, Swartz RH, Scheltens P. Complexity of MRI white matter hyperintensity assessments in relation to cognition in aging and dementia from the Sunnybrook Dementia Study. J Alzheimers Dis. 2011;26(suppl 3):379–388.
    1. Wang X, Valdes Hernandez MC, Doubal F, Chappell FM, Wardlaw JM. How much do focal infarcts distort white matter lesions and global cerebral atrophy measures? Cerebrovasc Dis. 2012;34:336–342.
    1. Wong KS, Gao S, Chan YL. Mechanisms of acute cerebral infarctions in patients with middle cerebral artery stenosis: a diffusion-weighted imaging and microemboli monitoring study. Ann Neurol. 2002;52:74–81.
    1. Seifert T, Enzinger C, Storch MK, Pichler G, Niederkorn K, Fazekas F. Acute small subcortical infarctions on diffusion weighted MRI: clinical presentation and aetiology. J Neurol Neurosurg Psychiatry. 2005;76:1520–1524.
    1. Longstreth WT, Jr, Manolio TA, Arnold A. Clinical correlates of white matter findings on cranial magnetic resonance imaging of 3301 elderly people. The Cardiovascular Health Study. Stroke. 1996;27:1274–1282.
    1. Wahlund LO, Barkhof F, Fazekas F. A new rating scale for age-related white matter changes applicable to MRI and CT. Stroke. 2001;32:1318–1322.
    1. Bocti C, Swartz RH, Gao FQ, Sahlas DJ, Behl P, Black SE. A new visual rating scale to assess strategic white matter hyperintensities within cholinergic pathways in dementia. Stroke. 2005;36:2126–2131.
    1. Prins ND, van Straaten ECW, van Dijk EJ. Measuring progression of cerebral white matter lesions on MRI. Visual rating and volumetrics. Neurology. 2004;62:1533–1539.
    1. Kapeller P, Barber R, Vermeulen RJ. Visual rating of age-related white matter changes on magnetic resonance imaging: scale comparison, interrater agreement, and correlations with quantitative measurements. Stroke. 2003;34:441–445.
    1. Fazekas F, Barkhof F, Wahlund LO. CT and MRI rating of white matter lesions. Cerebrovasc Dis. 2003;13:31–36.
    1. Ramirez J, Gibson E, Quddus A. Lesion Explorer: a comprehensive segmentation and parcellation package to obtain regional volumetrics for subcortical hyperintensities and intracranial tissue. Neuroimage. 2011;54:963–973.
    1. Jeerakathil T, Wolf PA, Beiser A. Stroke risk profile predicts white matter hyperintensity volume: the Framingham Study. Stroke. 2004;35:1857–1861.
    1. van den Heuvel DMJ, ten Dam VH, de Craen AJ. Measuring longitudinal white matter changes: comparison of a visual rating scale with a volumetric measurement. AJNR Am J Neuroradiol. 2006;27:875–878.
    1. Valdes Hernandez MC, Ferguson KJ, Chappell FM, Wardlaw JM. New multispectral MRI data fusion technique for white matter lesion segmentation: method and comparison with thresholding in FLAIR images. Eur Radiol. 2010;20:1684–1691.
    1. Firbank MJ, Minett T, O'Brien JT. Changes in DWI and MRS associated with white matter hyperintensities in elderly subjects. Neurology. 2003;61:950–954.
    1. Barnes SR, Haacke EM, Ayaz M, Boikov AS, Kirsch W, Kido D. Semiautomated detection of cerebral microbleeds in magnetic resonance images. Magn Reson Imaging. 2011;29:844–852.
    1. Seghier ML, Kolanko MA, Leff AP, Jager HR, Gregoire SM, Werring DJ. Microbleed detection using automated segmentation (MIDAS): a new method applicable to standard clinical MR images. PLoS One. 2011;6:e17547.
    1. Cordonnier C, Potter GM, Jackson CA. Improving interrater agreement about brain microbleeds. Development of the brain observer microbleed scales (BOMBS) Stroke. 2009;49:94–99.
    1. Gregoire SM, Chaudhary UJ, Brown MM. The microbleed anatomical rating scale (MARS): reliability of a tool to map brain microbleeds. Neurology. 2009;73:1759–1766.
    1. Scheltens P, Pasquier F, Weerts JG, Barkhof F, Leys D. Qualitative assessment of cerebral atrophy on MRI: inter- and intra-observer reproducibility in dementia and normal aging. Eur Neurol. 1997;37:95–99.
    1. Farrell C, Chappell F, Armitage PA. Development and initial testing of normal reference MR images for the brain at ages 65–70 and 75–80 years. Eur Radiol. 2008;19:177–183.
    1. Ashburner J, Csernansky JG, Davatzikos C, Fox NC, Frisoni GB, Thompson PM. Computer-assisted imaging to assess brain structure in healthy and diseased brains. Lancet Neurol. 2003;2:79–88.
    1. O'Sullivan M, Jouvent E, Saemann PG. Measurement of brain atrophy in subcortical vascular disease: a comparison of different approaches and the impact of ischaemic lesions. Neuroimage. 2008;43:312–320.
    1. de Bresser J, Portegies MP, Leemans A, Biessels GJ, Kappelle LJ, Viergever MA. A comparison of MR based segmentation methods for measuring brain atrophy progression. Neuroimage. 2011;54:760–768.
    1. Frisoni GB, Jack CR. Harmonization of magnetic resonance-based manual hippocampal segmentation: a mandatory step for wide clinical use. Alzheimers Dement. 2011;7:171–174.
    1. Duering M, Righart R, Csandi E. Incident subcortical infarcts induce focal thinning in connected cortical regions. Neurology. 2012;79:2025–2028.
    1. Smith EE, Schneider JA, Wardlaw JM, Greenberg SM. Cerebral microinfarcts: the invisible lesions. Lancet Neurol. 2012;11:272–282.
    1. Brundel M, de Bresser J, van Dillen JJ, Kappelle LJ, Biessels GJ. Cerebral microinfarcts: a systematic review of neuropathological studies. J Cereb Blood Flow Metab. 2012;32:425–436.
    1. van Veluw SJ, Zwanenburg JJ, Engelen-Lee J. In vivo detection of cerebral cortical microinfarcts with high-resolution 7T MRI. J Cereb Blood Flow Metab. 2012;33:322–329.

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