Longitudinal patterns of leukoaraiosis and brain atrophy in symptomatic small vessel disease

Brain

Volumn 139, Issue 4, 2016, Pages 1136-1151

  Lambert, Christian ^a   Benjamin, Philip ^a,b   Zeestraten, Eva ^a   Lawrence, Andrew J ^c   Barrick, Thomas R ^a   Markus, Hugh S ^c  

^a ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^b IMPERIAL COLLEGE HEALTHCARE NHS TRUST   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

atrophy; longitudinal; small vessel disease; voxel based quantification; white matter hyperintensities

Indexed keywords

AGED; ARTICLE; BRAIN ATROPHY; BRAIN REGION; BRAIN SIZE; CEREBROVASCULAR DISEASE; CORPUS CALLOSUM; DISEASE COURSE; FEMALE; FOLLOW UP; GRAY MATTER; HUMAN; LACUNAR STROKE; LEUKOARAIOSIS; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; MEDIAL FRONTAL CORTEX; NUCLEAR MAGNETIC RESONANCE IMAGING; OCCIPITAL CORTEX; PATHOGENESIS; PRIORITY JOURNAL; TISSUE REPAIR; WHITE MATTER LESION; ATROPHY; BRAIN; CEREBRAL SMALL VESSEL DISEASES; COHORT ANALYSIS; MIDDLE AGED; PATHOLOGY; PROSPECTIVE STUDY; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ATROPHY; BRAIN; CEREBRAL SMALL VESSEL DISEASES; COHORT STUDIES; DISEASE PROGRESSION; FEMALE; FOLLOW-UP STUDIES; HUMANS; LEUKOARAIOSIS; LONGITUDINAL STUDIES; MALE; MIDDLE AGED; PROSPECTIVE STUDIES;

EID: 84964465050     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aww009     Document Type: Article

References (60)

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. Cerebrovas Dis 2009; 28: 227-42.
2. Artero S, Tiemeier H, Prins ND, Sabatier R, Breteler MM, Ritchie K. Neuroanatomical localisation and clinical correlates of white matter lesions in the elderly. J Neurol Neurosurg Psychiatry 2004; 75: 1304-8.
3. Ashburner J, Friston KJ. Unified segmentation. NeuroImage 2005; 26: 839-51.
4. Ashburner J, Friston KJ. Diffeomorphic registration using geodesic shooting and Gauss-Newton optimization. NeuroImage 2011; 55: 954-67.
5. Ashburner J, Ridgway GR. Symmetric diffeomorphic modeling of longitudinal structural MRI. Front Neurosci 2012; 6: 197
6. Bamford J, Sandercock P, Jones L, Warlow C. The natural history of lacunar infarction: the Oxfordshire Community Stroke Project. Stroke 1987; 18: 545-51.
7. Benjamin P, Lawrence AJ, Lambert C, Patel B, Chung AW, MacKinnon AD, et al. Thalamic lacunar infarcts connecting to the prefrontal cortex associate with impaired processing speed. Neuroimage 2014; 4: 828-37.
8. 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. Am J Roentgenol 1988; 151: 559-66.
9. Cambron M, D'Haeseleer M, Laureys G, Clinckers R, Debruyne J, De Keyser J. White-matter astrocytes, axonal energy metabolism, and axonal degeneration in multiple sclerosis. J Cereb Blood Flow Metab 2012; 32: 413-24.
10. Curnes JT, Burger PC, Djang WT, Boyko OB. MR imaging of compact white matter pathways. Am J Neuroradiol 1988; 9: 1061-8.
11. Craggs LJ, Yamamoto Y, Ihara M, Fenwick R, Burke M, Oakley AE, et al. White matter pathology and disconnection in the frontal lobe in cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL). Neuropathol Appl Neurobiol 2014; 40: 591-602.
12. 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.
13. DeCarli C, Fletcher E, Ramey V, Harvey D, Jagust WJ. Anatomical mapping of white matter hyperintensities (WMH): exploring the relationships between periventricular WMH, deep WMH, and total WMH burden. Stroke 2005; 36: 50-5.
14. de Laat KF, Reid AT, Grim DC, Evans AC, Kö tter R, van Norden AG, et al. Cortical thickness is associated with gait disturbances in cerebral small vessel disease. NeuroImage 2012; 59: 1478-84.
15. De Leeuw FE, De Groot JC, Achten E, Oudkerk M, Ramos LMP, Heijboer R, et al. Prevalence of cerebral white matter lesions in elderly people: a population based magnetic resonance imaging study. The Rotterdam Scan Study. J Neurol Neurosurg Psychiatry 2001; 70: 9-14.
16. Du AT, Schuff N, Chao LL, Kornak J, Ezekiel F, Jagust WJ, et al. White matter lesions are associated with cortical atrophy more than entorhinal and hippocampal atrophy. Neurobiol Aging 2005; 26: 553-9.
17. Dufouil C, Chalmers J, Coskun O, Besancon V, Bousser MG, et al. Effects of blood pressure lowering on cerebral white matter hyperintensities in patients with stroke the PROGRESS (Perindopril Protection Against Recurrent Stroke Study) magnetic resonance imaging substudy. Circulation 2005; 112: 1644-50.
18. Draganski B, Ashburner J, Hutton C, Kherif F, Frackowiak RSJ, Helms G, et al. Regional specificity of MRI contrast parameter changes in normal ageing revealed by voxel-based quantification (VBQ). Neuroimage 2011; 55: 1423-34.
19. Duering M, Zieren N, Hervé D, Jouvent E, Reyes S, Peters N, et al. Strategic role of frontal white matter tracts in vascular cognitive impairment: a voxel-based lesion-symptom mapping study in CADASIL. Brain 2011; 134: 2366-75.
20. Duering M, Righart R, Wollenweber FA, Zietemann V, Gesierich B, et al. Acute infarcts cause focal thinning in remote cortex via degeneration of connecting fiber tracts. Neurology 2015; 84: 1685-92.
21. Dunn JT, Clark-Papasavas C, Marsden P, Baker S, Cleij M, Kapur S, et al. Establishing test-retest reliability of an adapted [18F]fallypride imaging protocol in older people. J Cereb Blood Flow Metab 2013; 33: 1098-103.
22. Erten-Lyons D, Woltjer R, Kaye J, Mattek N, Dodge HH, Green S, et al. Neuropathologic basis of white matter hyperintensity accumulation with advanced age. Neurology 2013; 81: 977-83.
23. Fazekas F, Kleinert R, Offenbacher H, Schmidt R, Kleinert G, Payer F, et al. Pathologic correlates of incidental MRI white matter signal hyperintensities. Neurology 1993; 43: 1683-9
24. Fernando MS, Simpson JE, Matthews F, Brayne C, Lewis CE, Barber R, et al. White matter lesions in an unselected cohort of the elderly: molecular pathology suggests origin from chronic hypoperfusion injury. Stroke 2006; 37: 1391-8.
25. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 2002; 33: 341-55.
26. Garde E, Lykke Mortensen E, Rostrup E, Paulson OB. Decline in intelligence is associated with progression in white matter hyperintensity volume. J Neurol Neurosurg Psychiatry 2005; 76: 1289-91.
27. Godin O, Maillard P, Crivello F, Alpérovitch A, Mazoyer B, et al. Association of white-matter lesions with brain atrophy markers: the three-city Dijon MRI study. Cerebrovasc Dis 2009; 28: 177-84.
28. Gouw AA, Seewann A, van der Flier WM, Barkhof F, Rozemuller AM, Scheltens P, et al. Heterogeneity of small vessel disease: a systematic review of MRI and histopathology correlations. J Neurol Neurosurg Psychiatry 2011; 82: 126-35.
29. Gunning-Dixon FM, Raz N. Neuroanatomical correlates of selected executive functions in middle-aged and older adults: a prospective MRI study. Neuropsychologia 2003; 41: 1929-41.
30. Hassan A, Hunt BJ, O'Sullivan M, Parmar K, Bamford JM, Briley D, et al. Markers of endothelial dysfunction in lacunar infarction and ischaemic leukoaraiosis. Brain 2003; 126: 424-32.
31. Hutton C, Draganski B, Ashburner J, Weiskopf N. A comparison between voxel-based cortical thickness and voxel-based morphometry in normal aging. NeuroImage 2009; 48: 371-80.
32. Jeerakathil T, Wolf PA, Beiser A, Massaro J, Seshadri S, D'Agostino RB, et al. Stroke risk profile predicts white matter hyperintensity volume: the Framingham study. Stroke 2004; 35: 1857-61.
33. Jokinen H, Lipsanen J, Schmidt R, Fazekas F, Gouw AA, van der Flier WM, et al. Brain atrophy accelerates cognitive decline in cerebral small vessel disease the LADIS study. Neurology 2012; 78: 1785-92.
34. Kraha A, Turner H, Nimon K, Zientek LR, Henson RK. Tools to support interpreting multiple regression in the face of multicollinearity. Front Psychol 2011; 3: 44-44.
35. Lambert C, Janakan SN, Barrick TR, Markus HS. Characterising the grey matter correlates of Leukoaraiosis in cerebral small vessel disease. NeuroImage: Clinical 2015; 9: 194-205.
36. Lambert C, Lutti A, Helms G, Frackowiak R, Ashburner J. Multiparametric brainstem segmentation using a modified multivariate mixture of Gaussians. NeuroImage 2013; 2: 684-94.
37. Lawrence AJ, Patel B, Morris RG, MacKinnon AD, Rich PM, Barrick TR, et al. Mechanisms of cognitive impairment in cerebral small vessel disease: multimodal MRI results from the St George's Cognition and Neuroimaging in Stroke (SCANS) study. PloS One 2013; 8: e61014
38. Lawrence AJ, Chung AW, Morris RG, Markus HS, Barrick TR. Structural network efficiency is associated with cognitive impairment in small-vessel disease. Neurology 2014; 83: 304-11.
39. Munoz DG, Hastak SM, Harper B, Lee D, Hachinski VC. Pathologic correlates of increased signals of the centrum ovale on magnetic resonance imaging. Arch Neurol 1993; 50: 492-7.
40. Nitkunan A, Lanfranconi S, Charlton RA, Barrick TR, Markus HS. Brain atrophy and cerebral small vessel disease a prospective followup study. Stroke 2011; 42: 133-8.
41. Ossenkoppele R, Cohn-Sheehy BI, La Joie R, Vogel JW, Mö ller C, Lehmann M, et al. Atrophy patterns in early clinical stages across distinct phenotypes of Alzheimer's disease. Hum Brain Mapp 2015; 36: 4421-37.
42. O'Sullivan MRCP, Jones DK, Summers PE, Morris RG, Williams SCR, Markus HS. Evidence for cortical "disconnection" as a mechanism of age-related cognitive decline. Neurology 2001; 57: 632-38.
43. Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 2010; 9: 689-701.
44. Pantoni L, Garcia JH, Gutierrez JA. Cerebral white matter is highly vulnerable to Ischemia. Stroke 1996; 27: 1641-7.
45. Pantoni L, Garcia JH. Pathogenesis of leukoaraiosis a review. Stroke 1997; 28: 652-9.
46. Patel B, Markus HS. Magnetic resonance imaging in cerebral small vessel disease and its use as a surrogate disease marker. Int J Stroke 2011; 6: 47-59.
47. Price S, Paviour D, Scahill R, Stevens J, Rossor M, Lees A, et al. Voxel-based morphometry detects patterns of atrophy that help differentiate progressive supranuclear palsy and Parkinson's disease. Neuroimage 2004; 23: 663-9.
48. Raji CA, Lopez OL, Kuller LH, Carmichael OT, Longstreth WT Jr, Gach HM, et al. White matter lesions and brain gray matter volume in cognitively normal elders. Neurobiol Aging 2012; 33: 834-e7
49. Revesz T, Hawkins CP, Du Boulay EP, Barnard RO, McDonald WI. Pathological findings correlated with magnetic resonance imaging in subcortical arteriosclerotic encephalopathy (Binswanger's disease). J Neurol Neurosurg Psychiatry 1989; 52: 1337-44.
50. Schmahmann JD, Pandya D. Fiber pathways of the brain. OUP USA; 2009.
51. Smith EE, Schneider JA, Wardlaw JM, Greenberg SM. Cerebral microinfarcts: the invisible lesions. Lancet Neurol 2012; 11: 272-82.
52. Steffens DC, Potter GG, McQuoid DR, MacFall JR, Payne ME, Burke JR, et al. Longitudinal magnetic resonance imaging vascular changes, apolipoprotein E genotype, and development of dementia in the neurocognitive outcomes of depression in the elderly study. Am J Geriatr Psychiatry 2007; 15: 839-49.
53. Tamnes CK, Walhovd KB, Dale AM, Østby Y, Grydeland H, Richardson G, et al. Brain development and aging: overlapping and unique patterns of change. Neuroimage 2013; 68: 63-74.
54. Tessa C, Lucetti C, Giannelli M, Diciotti S, Poletti M, Danti S, et al. Progression of brain atrophy in the early stages of Parkinson's disease: a longitudinal tensor-based morphometry study in de novo patients without cognitive impairment. Hum Brain Mapp 2014; 35: 3932-44.
55. Tuladhar AM, Reid AT, Shumskaya E, de Laat KF, van Norden AG, van Dijk EJ, et al. Relationship between white matter hyperintensities, cortical thickness, and cognition. Stroke 2015; 46: 425-32.
56. Wardlaw JM, Smith EE, Biessels GJ, Cordonnier C, Fazekas F, Frayne R, et al. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 2013; 12: 822-38.
57. Wender R, Brown AM, Fern R, Swanson RA, Farrell K, Ransom BR. Astrocytic glycogen influences axon function and survival during glucose deprivation in central white matter. J Neurosci 2000; 20: 6804-10.
58. Whitwell JL, Przybelski SA, Weigand SD, Knopman DS, Boeve BF, Petersen RC, et al. 3D maps from multiple MRI illustrate changing atrophy patterns as subjects progress from mild cognitive impairment to Alzheimer's disease. Brain 2007; 130: 1777-86.
59. Yamauchi H, Fukuda H, Oyanagi C. Significance of white matter high intensity lesions as a predictor of stroke from arteriolosclerosis. J Neurol Neurosurg Psychiatry 2002; 72: 576-82.
60. Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, et al. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. NeuroImage 2006; 31: 1116-28.