White matter hyperintensities are positively associated with cortical thickness in Alzheimer's disease

Journal of Alzheimer's Disease

Volumn 39, Issue 2, 2014, Pages 409-422

  Jacobs, Heidi I L ^a,b,c   Clerx, Lies ^a,b   Gronenschild, Ed H B M ^b,c   Aalten, Pauline ^b,c   Verhey, Frans R J ^b,c  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

Compensation; cortical thickness; dementia; hypertrophy; inflammation; white matter hyperintensities

Indexed keywords

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN ATROPHY; CLINICAL ARTICLE; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); DISEASE ASSOCIATION; DISEASE COURSE; HUMAN; MALE; MEMORY DISORDER; MIDDLE AGED; MILD COGNITIVE IMPAIRMENT; PARIETAL LOBE; PRIORITY JOURNAL; TEMPORAL GYRUS; WHITE MATTER;

COMPENSATION; CORTICAL THICKNESS; DEMENTIA; HYPERTROPHY; INFLAMMATION; WHITE MATTER HYPERINTENSITIES;

AGED; ALZHEIMER DISEASE; BRAIN; FRONTAL LOBE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MILD COGNITIVE IMPAIRMENT; NERVE FIBERS, MYELINATED; ORGAN SIZE; PARIETAL LOBE; TEMPORAL LOBE;

EID: 84893949167     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-131232     Document Type: Article

References (73)

1. Schneider JA,Wilson RS, Cochran EJ, Bienias JL, Arnold SE, Evans DA, Bennett DA (2003) Relation of cerebral infarctions to dementia and cognitive function in older persons. Neurology 60, 1082-1088.
2. Debette S, Bombois S, Bruandet A, Delbeuck X, Lepoittevin S, Delmaire C, Leys D, Pasquier F (2007) Subcortical hyperintensities are associated with cognitive decline in patients with mild cognitive impairment. Stroke 38, 2924-2930.
3. Jacobs HIL, Visser PJ, Van Boxtel MP, Frisoni GB, Tsolaki M, Papapostolou P, Nobili F, Wahlund LO, Minthon L, Frolich L, Hampel H, Soininen H, van de Pol L, Scheltens P, Tan FE, Jolles J, Verhey FR (2012) The association between white matter hyperintensities and executive decline in mild cognitive impairment is network dependent. Neurobiol Aging 33, 201.e201-208.
4. Portet F, Ousset PJ, Visser PJ, Frisoni GB, Nobili F, Scheltens P, Vellas B, Touchon J (2006) Mild cognitive impairment (MCI) in medical practice: A critical review of the concept and new diagnostic procedure. Report of the MCI Working Group of the European Consortium on Alzheimer's Disease. J Neurol Neurosurg Psychiatry 77, 714-718.
5. Burns JM, Church JA, Johnson DK, Xiong C, Marcus D, FotenosAF, Snyder AZ, Morris JC, BucknerRL(2005) White matter lesions are prevalent but differentially related with cognition in aging and early Alzheimer disease. Arch Neurol 62, 1870-1876.
6. de Mendonca A, Ribeiro F, Guerreiro M, Palma T, Garcia C (2005) Clinical significance of subcortical vascular disease in patients with mild cognitive impairment. Eur J Neurol 12, 125-130.
7. de Groot JC, de Leeuw FE, Oudkerk M, van Gijn J, Hofman A, Jolles J, Breteler MM (2000) Cerebral white matter lesions and cognitive function: The Rotterdam Scan Study. Ann Neurol 47, 145-151.
8. de Groot JC, De Leeuw FE, Oudkerk M, Van Gijn J, Hofman A, Jolles J, BretelerMM(2002) Periventricular cerebral white matter lesions predict rate of cognitive decline. Ann Neurol 52, 335-341.
9. Sachdev P, Wen W (2005) Should we distinguish between periventricular and deep white matter hyperintensities? Stroke 36, 2342-2343; author reply 2343-2344.
10. Ylikoski R, Ylikoski A, Erkinjuntti T, Sulkava R, Raininko R, Tilvis R (1993) White matter changes in healthy elderly persons correlate with attention and speed of mental processing. Arch Neurol 50, 818-824.
11. Gouw AA, Seewann A, van der Flier WM, Barkhof F, Rozemuller AM, Scheltens P, Geurts JJ (2011) Heterogeneity of small vessel disease: A systematic review of MRI and histopathology correlations. J Neurol Neurosurg Psychiatry 82, 126-135.
12. Scheltens P, Barkhof F, Leys D, Wolters EC, Ravid R, Kamphorst W (1995) Histopathologic correlates of white matter changes on MRI in Alzheimer's disease and normal aging. Neurology 45, 883-888.
13. DeCarli C, Murphy DG, Tranh M, Grady CL, Haxby JV, Gillette JA, Salerno JA, Gonzales-Aviles A, Horwitz B, Rapoport SI, Schapiro MB (1995) The effect of white matter hyperintensity volume on brain structure, cognitive performance, and cerebral metabolism of glucose in 51 healthy adults. Neurology 45, 2077-2084.
14. Inzitari D (2000) Age-related white matter changes and cognitive impairment. Ann Neurol 47, 141-143.
15. Taylor WD, Payne ME, Krishnan KR, Wagner HR, Provenzale JM, Steffens DC, MacFall JR (2001) Evidence of white matter tract disruption in MRI hyperintensities. Biol Psychiatry 50, 179-183.
16. Delbeuck X,Van der Linden M, Collette F (2003) Alzheimer's disease as a disconnection syndrome? Neuropsychol Rev 13, 79-92.
17. Raz N, Lindenberger U, Rodrigue KM, Kennedy KM, Head D, Williamson A, Dahle C, Gerstorf D, Acker JD (2005) Regional brain changes in aging healthy adults: General trends, individual differences and modifiers. Cereb Cortex 15, 1676-1689.
18. Raz N, Rodrigue KM (2006) Differential aging of the brain: Patterns, cognitive correlates and modifiers. Neurosci Biobehav Rev 30, 730-748.
19. Raz N, Rodrigue KM, Kennedy KM, Acker JD (2007) Vascular health and longitudinal changes in brain and cognition in middle-aged and older adults. Neuropsychology 21, 149-157.
20. Capizzano AA, Acion L, Bekinschtein T, Furman M, Gomila H, Martinez A, Mizrahi R, Starkstein SE (2004) White matter hyperintensities are significantly associated with cortical atrophy in Alzheimer's disease. J Neurol Neurosurg Psychiatry 75, 822-827.
21. Wen W, Sachdev PS, Chen X, Anstey K (2006) Gray matter reduction is correlated with white matter hyperintensity volume: A voxel-based morphometric study in a large epidemiological sample. Neuroimage 29, 1031-1039.
22. Rossi R, Boccardi M, Sabattoli F, Galluzzi S, Alaimo G, Testa C, Frisoni GB (2006) Topographic correspondence between white matter hyperintensities and brain atrophy. J Neurol 253, 919-927.
23. Ha SY,Youn YC, Kim S, HsiungGY, AhnSW, ShinHW, Park KY, Park TH, Kim SS, Kee BS, Kwon OS (2012) A voxelbased morphometric study of cortical gray matter volume changes in Alzheimer's disease with white matter hyperintensities. J Clin Neurosci 19, 1506-1510.
24. Seo SW, Lee JM, Im K, Park JS, Kim SH, Kim ST, Ahn HJ, Chin J, Cheong HK, Weiner MW, Na DL (2012) Cortical thinning related to periventricular and deep white matter hyperintensities. Neurobiol Aging 33, 1156-1167.
25. Wen W, Sachdev P (2004) The topography of white matter hyperintensities on brain MRI in healthy 60-to 64-year-old individuals. Neuroimage 22, 144-154.
26. Jacobs HIL, Van Boxtel MP, Uylings HB, Gronenschild EH, Verhey FR, Jolles J (2011) Atrophy of the parietal lobe in preclinical dementia. Brain Cogn 75, 154-163.
27. Jacobs HIL,Van Boxtel MPJ, Gronenschild EHBM,Williams VJ, Uylings HBM, Burgmans S, Jolles J, Verhey FRJ (2012) Patterns of grey and white matter changes in individuals at risk for Alzheimer's disease. Curr Alzheimer Res 9, 1097-1105.
28. Jacobs HIL, Van Boxtel MPJ, Jolles J, Verhey FRJ, Uylings HBM (2012) Parietal cortex matters in Alzheimer's disease: An overview of structural, functional and metabolic findings. Neurosci Biobehav Rev 36, 297-309.
29. Desikan RS, Cabral HJ, Fischl B, Guttmann CR, Blacker D, Hyman BT, Albert MS, Killiany RJ (2009) Temporoparietal MR imaging measures of atrophy in subjects with mild cognitive impairment that predict subsequent diagnosis of Alzheimer disease. AJNR Am J Neuroradiol 30, 532-538.
30. Desikan RS, Fischl B, Cabral HJ, Kemper TL, Guttmann CR, Blacker D, Hyman BT, Albert MS, Killiany RJ (2008) MRI measures of temporoparietal regions show differential rates of atrophy during prodromal AD. Neurology 71, 819-825.
31. Du AT, Schuff N, Chao LL, Kornak J, Ezekiel F, Jagust WJ, Kramer JH, Reed BR, Miller BL, Norman D, Chui HC,Weiner MW (2005) White matter lesions are associated with cortical atrophy more than entorhinal and hippocampal atrophy. Neurobiol Aging 26, 553-559.
32. Ashburner J, Friston KJ (2000) Voxel-based morphometry-the methods. Neuroimage 11, 805-821.
33. Ridgway GR, Henley SM, Rohrer JD, Scahill RI,Warren JD, Fox NC (2008) Ten simple rules for reporting voxel-based morphometry studies. Neuroimage 40, 1429-1435.
34. Fischl B (2012) FreeSurfer. Neuroimage 62, 774-781.
35. Petersen RC, Negash S (2008) Mild cognitive impairment: An overview. CNS Spectr 13, 45-53.
36. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (1984) Clinical diagnosis of Alzheimer's disease: Report of the NINCDS-ADRDAWork Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34, 939-944.
37. Hamilton M (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry 23, 56-62.
38. Scheltens P, Leys D, Barkhof F, Huglo D, Weinstein HC, Vermersch P, Kuiper M, Steinling M, Wolters EC, Valk J (1992) Atrophy of medial temporal lobes on MRI in "probable" Alzheimer's disease and normal ageing: Diagnostic value and neuropsychological correlates. J Neurol Neurosurg Psychiatry 55, 967-972.
39. Clerx L, van Rossum IA, Burns L, Knol DL, Scheltens P, Verhey F, Aalten P, Lapuerta P, van de Pol L, van Schijndel R, de Jong R, Barkhof F, Wolz R, Rueckert D, Bocchetta M, Tsolaki M, Nobili F, Wahlund LO, Minthon L, Frolich L, Hampel H, Soininen H, Visser PJ (2013) Measurements of medial temporal lobe atrophy for prediction of Alzheimer's disease in subjects with mild cognitive impairment. Neurobiol Aging 34, 2003-2013.
40. Dubois B, Feldman HH, Jacova C, Cummings JL, Dekosky ST, Barberger-Gateau P, Delacourte A, Frisoni G, Fox NC, Galasko D, Gauthier S, Hampel H, Jicha GA, Meguro K, O'Brien J, Pasquier F, Robert P, Rossor M, Salloway S, Sarazin M, de Souza LC, Stern Y, Visser PJ, Scheltens P (2010) Revising the definition of Alzheimer's disease: A new lexicon. Lancet Neurol 9, 1118-1127.
41. Albert MS, Dekosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, Gamst A, Holtzman DM, Jagust WJ, Petersen RC, Snyder PJ, Carrillo MC, Thies B, Phelps CH (2011) The diagnosis of mild cognitive impairment due to Alzheimer's disease: Recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 7, 270-279.
42. Gronenschild EH, Habets P, Jacobs HI, Mengelers R, Rozendaal N, van Os J, MarcelisM(2012) The effects of FreeSurfer version, workstation type, and Macintosh operating system version on anatomical volume and cortical thickness measurements. PLoS One 7, e38234.
43. Han X, Jovicich J, Salat D, van der Kouwe A, Quinn B, Czanner S, Busa E, Pacheco J, Albert M, Killiany R, Maguire P, Rosas D, Makris N, Dale A, Dickerson B, Fischl B (2006) Reliability of MRI-derived measurements of human cerebral cortical thickness: The effects of field strength, scanner upgrade and manufacturer. Neuroimage 32, 180-194.
44. Sled JG, Zijdenbos AP, Evans AC (1998) A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17, 87-97.
45. Hagler DJ Jr, Saygin AP, Sereno MI (2006) Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data. Neuroimage 33, 1093-1103.
46. Pengas G, Pereira JM, Williams GB, Nestor PJ (2009) Comparative reliability of total intracranial volume estimation methods and the influence of atrophy in a longitudinal semantic dementia cohort. J Neuroimag 19, 37-46.
47. Keihaninejad S, Heckemann RA, Fagiolo G, Symms MR, Hajnal JV, Hammers A (2010) A robust method to estimate the intracranial volume across MRI field strengths (1.5T and 3T). Neuroimage 50, 1427-1437.
48. SmithSM(2002) Fast robust automated brain extraction.Hum Brain Mapp 17, 143-155.
49. Henskens LH, Kroon AA, van Oostenbrugge RJ, Gronenschild EH, Hofman PA, Lodder J, de Leeuw PW (2009) Associations of ambulatory blood pressure levels with white matter hyperintensity volumes in hypertensive patients. J Hypertens 27, 1446-1452.
50. Nyul LG, Udupa JK (1999) On standardizing the MR image intensity scale. Magn Reson Med 42, 1072-1081.
51. Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31, 968-980.
52. Maheswaran S, Barjat H, Rueckert D, Bate ST, Howlett DR, Tilling L, Smart SC, Pohlmann A, Richardson JC, Hartkens T, Hill DL, Upton N, Hajnal JV, James MF (2009) Longitudinal regional brain volume changes quantified in normal aging and Alzheimer's APP x PS1 mice using MRI. Brain Res 1270, 19-32.
53. OhES, SavonenkoAV, King JF, FangmarkTuckerSM,Rudow GL, Xu G, Borchelt DR, Troncoso JC (2009) Amyloid precursor protein increases cortical neuron size in transgenic mice. Neurobiol Aging 30, 1238-1244.
54. West MJ, Bach G, Soderman A, Jensen JL (2009) Synaptic contact number and size in stratum radiatum CA1 of APP/PS1DeltaE9 transgenic mice. Neurobiol Aging 30, 1756-1776.
55. Iacono D, Markesbery WR, Gross M, Pletnikova O, Rudow G, Zandi P, Troncoso JC (2009) The Nun study: Clinically silent AD, neuronal hypertrophy, and linguistic skills in early life. Neurology 73, 665-673.
56. Riudavets MA, Iacono D, Resnick SM, O'Brien R, Zonderman AB, Martin LJ, Rudow G, Pletnikova O, Troncoso JC (2007) Resistance to Alzheimer's pathology is associated with nuclear hypertrophy in neurons. Neurobiol Aging 28, 1484-1492.
57. Iacono D, O'Brien R, Resnick SM, Zonderman AB, Pletnikova O, Rudow G, An Y, West MJ, Crain B, Troncoso JC (2008) Neuronal hypertrophy in asymptomatic Alzheimer disease. J Neuropathol Exp Neurol 67, 578-589.
58. Braak H, Braak E (1996) Development of Alzheimer-related neurofibrillary changes in the neocortex inversely recapitulates cortical myelogenesis. Acta Neuropathol (Berl) 92, 197-201.
59. Thal DR, Rub U, Orantes M, Braak H (2002) Phases of A beta-deposition in the human brain and its relevance for the development of AD. Neurology 58, 1791-1800.
60. Reid AT, van Norden AG, de Laat KF, van Oudheusden LJ, ZwiersMP, EvansAC, de Leeuw FE,Kotter R (2010) Patterns of cortical degeneration in an elderly cohort with cerebral small vessel disease. Hum Brain Mapp 31, 1983-1992.
61. Fortea J, Sala-Llonch R, Bartres-Faz D, Bosch B, Llado A, Bargallo N, Molinuevo JL, Sanchez-Valle R (2010) Increased cortical thickness and caudate volume precede atrophy in PSEN1 mutation carriers. J Alzheimers Dis 22, 909-922.
62. Solito E, Sastre M (2012) Microglia function in Alzheimer's disease. Front Pharmacol 3, 1-10.
63. Wyss-Coray T (2006) Inflammation in Alzheimer disease: Driving force, bystander or beneficial response? Nat Med 12, 1005-1015.
64. Brickman AM, Muraskin J, Zimmerman ME (2009) Structural neuroimaging in Altheimer's disease: Do white matter hyperintensities matter? Dialogues Clin Neurosci 11, 181-190.
65. van Dijk EJ, Prins ND, Vermeer SE, Vrooman HA, Hofman A, Koudstaal PJ, BretelerMM(2005) C-reactive protein and cerebral small-vessel disease: The Rotterdam Scan Study. Circulation 112, 900-905.
66. Serrano-Pozo A, Mielke ML, Gomez-Isla T, Betensky RA, Growdon JH, Frosch MP, Hyman BT (2011) Reactive glia not only associates with plaques but also parallels tangles in Alzheimer's disease. Am J Pathol 179, 1373-1384.
67. Laske C, Stransky E, Leyhe T, Eschweiler GW, Wittorf A, Richartz E, Bartels M, Buchkremer G, Schott K (2006) Stage-dependent BDNF serum concentrations in Alzheimer's disease. J Neural Transm 113, 1217-1224.
68. Jacobs HIL, Van Boxtel MPJ, Heinecke A, Gronenschild EHBM, Backes WH, Jolles J, Verhey FRJ (2012) Functional integration of parietal lobe activity in early Alzheimer's disease. Neurology 78, 352-360.
69. Sperling RA, Dickerson BC, Pihlajamaki M, Vannini P, LaViolette PS,VitoloOV, Hedden T, Becker JA, Rentz DM, Selkoe DJ, JohnsonKA(2010) Functional alterations in memory networks in early Alzheimer's disease. Neuromolecular Med 12, 27-43.
70. SeoSW, ImK, Lee JM, Kim YH, Kim ST, Kim SY,YangDW, Kim SI, Cho YS, Na DL (2007) Cortical thickness in singleversus multiple-domain amnestic mild cognitive impairment. Neuroimage 36, 289-297.
71. McKeeAC,AuR, Cabral HJ,KowallNW, Seshadri S,Kubilus CA, Drake J,Wolf PA (2006) Visual association pathology in preclinical Alzheimer disease. J Neuropathol Exp Neurol 65, 621-630.
72. Jacobs HIL, Van Boxtel MPJ, Gronenschild EHBM, Uylings HBM, Jolles J, Verhey FRJ (2013) Decreased grey matter diffusivity: A potential early Alzheimer's disease biomarker? Alzheimers Dementia 9, 93-97.
73. Admiraal-Behloul F, van den Heuvel DM, Olofsen H, van Osch MJ, van der Grond J, van BuchemMA,Reiber JH (2005) Fully automatic segmentation of white matter hyperintensities in MR images of the elderly. Neuroimage 28, 607-617.