Association of white matter hyperintensities and gray matter volume with cognition in older individuals without cognitive impairment

Brain Structure and Function

Volumn 221, Issue 4, 2016, Pages 2135-2146

  Arvanitakis, Zoe ^a,b   Fleischman, Debra A ^a,b   Arfanakis, Konstantinos ^a,b,c   Leurgans, Sue E ^a,b   Barnes, Lisa L ^a,b   Bennett, David A ^a,b  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

^c ILLINOIS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Aging; Brain; Cognition; Gray matter; MRI; Volume; Voxel wise analyses; White matter hyperintensities

Indexed keywords

AGED; AGING; ARTICLE; BRAIN SIZE; CLINICAL EVALUATION; COGNITION; COHORT ANALYSIS; COMMUNITY LIVING; DEPTH PERCEPTION; EDUCATIONAL STATUS; EPISODIC MEMORY; FEMALE; GRAY MATTER VOLUME; HUMAN; IMAGING SOFTWARE; MALE; NERVOUS SYSTEM PARAMETERS; NEUROIMAGING; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; SEMANTIC MEMORY; WHITE MATTER; WHITE MATTER HYPERINTENSITY; WORKING MEMORY; BRAIN; GRAY MATTER; NEUROPSYCHOLOGICAL TEST; PATHOLOGY; PHYSIOLOGY; PSYCHOLOGY; VERY ELDERLY;

AGED, 80 AND OVER; AGING; BRAIN; COGNITION; FEMALE; GRAY MATTER; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEUROPSYCHOLOGICAL TESTS; WHITE MATTER;

EID: 84926175401     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-015-1034-7     Document Type: Article

References (70)

1. Aggarwal NT, Wilson RS, Bienias JL, De Jager PL, Bennett DA, Evans DA, DeCarli C (2010) The association of magnetic resonance imaging measures with cognitive function in a biracial population sample. Arch Neurol 67(4):475–482. doi:10.1001/archneurol.2010.42
2. Ardekani BA, Guckemus S, Bachman A, Hoptman MJ, Wojtaszek M, Nierenberg J (2005) Quantitative comparison of algorithms for inter-subject registration of 3D volumetric brain MRI scans. J Neurosci Methods 42:67–76
3. Arfanakis K, Fleischman DA, Grisot G, Barth CM, Varentsova A, Morris MC, Barnes LL (2013) Bennett DA (2013) Systemic inflammation in non-demented elderly human subjects: brain microstructure and cognition. PLoS One 8(8):e73107. doi:10.1371/journal.pone.0073107 (eCollection)
4. Au R, Massaro JM, Wolf PA, Young ME, Beiser A, Seshadri S, D’Agostino RB, DeCarli C (2006) Association of white matter hyperintensity volume with decreased cognitive functioning: the Framingham Heart Study. Arch Neurol 63(2):246–250
5. Bennett DA, Wilson RS, Schneider JA, Evans DA, Aggarwal NT, Arnold SE, Cochran EJ, Berry-Kravis E, Bienias JL (2003) Apolipoprotein E epsilon4 allele, AD pathology, and the clinical expression of Alzheimer’s disease. Neurology 60(2):246–252
6. Bennett DA, Schneider JA, Wilson RS, Bienias JL, Arnold SE (2004) Neurofibrillary tangles mediate the association of amyloid load with clinical Alzheimer disease and level of cognitive function. Arch Neurol 61(3):378–384
7. Bennett DA, Schneider JA, Buchman AS, Barnes LL, Boyle PA, Wilson RS (2012a) Overview and findings from the Rush Memory and Aging Project. Curr Alzheimer Res 9(6):646–663
8. Bennett DA, Wilson RS, Boyle PA, Buchman AS, Schneider JA (2012b) Relation of neuropathology to cognition in persons without cognitive impairment. Ann Neurol 72(4):599–609. doi:10.1002/ana.23654
9. Birdsill AC, Koscik RL, Jonaitis EM, Johnson SC, Okonkwo OC, Hermann BP, Larue A, Sager MA, Bendlin BB (2014) Regional white matter hyperintensities: aging, Alzheimer’s disease risk, and cognitive function. Neurobiol Aging 35(4):769–776 (Epub 2013 Oct 10)
10. Bis JC, DeCarli C, Smith AV, van der Lijn F, Crivello F, Fornage M, Debette S, Shulman JM, Schmidt H, Srikanth V, et al. Cohorts for Heart and Aging Research in Genomic Epidemiology Consortium (2012) Common variants at 12q14 and 12q24 are associated with hippocampal volume. Nat Genet 44(5):545–551
11. Breteler MM, van Swieten JC, Bots ML, Grobbee DE, Claus JJ, van den Hout JH, van Harskamp F, Tanghe HL, de Jong PT, van Gijn J et al (1994) Cerebral white matter lesions, vascular risk factors, and cognitive function in a population-based study: the Rotterdam Study. Neurology 44(7):1246–1252
12. Burton EJ, Kenny RA, O’Brien J, Stephens S, Bradbury M, Rowan E, Kalaria R, Firbank M, Wesnes K, Ballard C (2004) White matter hyperintensities are associated with impairment of memory, attention, and global cognitive performance in older stroke patients. Stroke 35(6):1270–1275 (Epub 2004 Apr 29)
13. Carmichael O, Schwarz C, Drucker D, Fletcher E, Harvey D, Beckett L, Jack CR Jr, Weiner M, DeCarli C, Initiative Alzheimer’s Disease Neuroimaging (2010) Longitudinal changes in white matter disease and cognition in the first year of the Alzheimer disease neuroimaging initiative. Arch Neurol 67(11):1370–1378. doi:10.1001/archneurol.2010.284
14. Carmichael O, Mungas D, Beckett L, Harvey D, Tomaszewski Farias S, Reed B, Olichney J, Miller J, Decarli C (2012) MRI predictors of cognitive change in a diverse and carefully characterized elderly population. Neurobiol Aging 33(1):83–95. doi:10.1016/j.neurobiolaging.2010.01.021 (Epub 2010 Apr 1)
15. Chauhan G, Adams HH, Bis JC, Weinstein G, Yu L, Töglhofer AM, Smith AV, van der Lee S J, Gottesman RF, Thomson R et al (2015) Association of Alzheimer’s disease GWAS loci with MRI markers of brain aging. Neurobiol Aging. doi:10.1016/j.neurobiolaging.2014.12.028 (Epub ahead of print)
16. Debette S, Markus HS (2010) The clinical importance of white matter hyperintensities on brain magnetic resonance imaging: systematic review and meta-analysis. BMJ 341:c3666. doi:10.1136/bmj.c3666
17. 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(11):2924–2930 (Epub 2007 Sep 20)
18. DeCarli C, Murphy DG, Tranh M, Grady CL, Haxby JV, Gillette JA, Salerno JA, Gonzales-Aviles A, Horwitz B, Rapoport SI et al (1995) The effect of white matter hyperintensity volume on brain structure, cognitive performance, and cerebral metabolism of glucose in 51 healthy adults. Neurology 45(11):2077–2084
19. Fleischman DA, Arfanakis K, Kelly JF, Rajendran N, Buchman AS, Morris MC, Barnes LL, Bennett DA (2010) Regional brain cortical thinning and systemic inflammation in older persons without dementia. J Am Geriatr Soc 58(9):1823–1825. doi:10.1111/j.1532-5415.2010.03049.x (no abstract available)
20. Fleischman DA, Yu L, Arfanakis K, Han SD, Barnes LL, Arvanitakis Z, Boyle PA, Bennett DA (2013) Faster cognitive decline in the years prior to MR imaging is associated with smaller hippocampal volumes in cognitively healthy older persons. Front Aging Neurosci 5:21. doi:10.3389/fnagi.2013.00021 (eCollection 2013)
21. Fleischman DA, Leurgans S, Arfanakis K, Arvanitakis Z, Barnes LL, Boyle PA, Han SD, Bennett DA (2014) Gray-matter macrostructure in cognitively healthy older persons: associations with age and cognition. Brain Struct Funct 219(6):2029–2049
22. Fletcher E, Raman M, Huebner P, Liu A, Mungas D, Carmichael O, DeCarli C (2013) Loss of fornix white matter volume as a predictor of cognitive impairment in cognitively normal elderly individuals. JAMA Neurol 70(11):1389–1395. doi:10.1001/jamaneurol.2013.3263
23. Gouw AA, van der Flier WM, Fazekas F, van Straaten EC, Pantoni L, Poggesi A, Inzitari D, Erkinjuntti T, Wahlund LO, Waldemar G, Schmidt R, Scheltens P, Barkhof F, LADIS Study Group (2008) Progression of white matter hyperintensities and incidence of new lacunes over a 3-year period: the Leukoaraiosis and Disability study. Stroke 39(5):1414–1420. doi:10.1161/STROKEAHA.107.498535 (Epub 2008 Mar 6)
24. 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(2):126–135. doi:10.1136/jnnp.2009.204685 (Epub 2010 Oct 9)
25. Gunning-Dixon FM, Raz N (2000) The cognitive correlates of white matter abnormalities in normal aging: a quantitative review. Neuropsychology 14(2):224–232
26. Gunning-Dixon FM, Raz N (2003) Neuroanatomical correlates of selected executive functions in middle-aged and older adults: a prospective MRI study. Neuropsychologia 41(14):1929–1941
27. He J, Wong VS, Fletcher E, Maillard P, Lee DY, Iosif AM, Singh B, Martinez O, Roach AE, Lockhart SN, Beckett L, Mungas D, Farias ST, Carmichael O, DeCarli C (2012) The contributions of MRI-based measures of gray matter, white matter hyperintensity, and white matter integrity to late-life cognition. AJNR Am J Neuroradiol 33(9):1797–1803. doi:10.3174/ajnr.A3048 (Epub 2012 Apr 26)
28. Hedden T, Mormino EC, Amariglio RE, Younger AP, Schultz AP, Becker JA, Buckner RL, Johnson KA, Sperling RA, Rentz DM (2012) Cognitive profile of amyloid burden and white matter hyperintensities in cognitively normal older adults. J Neurosci 32(46):16233–16242. doi:10.1523/JNEUROSCI.2462-12.2012
29. Ishikawa H, Meguro K, Ishii H, Tanaka N, Yamaguchi S (2012) Silent infarction or white matter hyperintensity and impaired attention task scores in a nondemented population: the Osaki-Tajiri Project. J Stroke Cerebrovasc Dis 21(4):275–282. doi:10.1016/j.jstrokecerebrovasdis.2010.08.008 (Epub 2010 Oct 25)
30. Jack CR Jr, Petersen RC, Xu Y, O’Brien PC, Smith GE, Ivnik RJ, Boeve BF, Tangalos EG, Kokmen E (2000) Rates of hippocampal atrophy correlate with change in clinical status in aging and AD. Neurology 55(4):484–489
31. Jeerakathil T, Wolf PA, Beiser A, Massaro J, Seshadri S, D’Agostino RB, DeCarli C (2004) Stroke risk profile predicts white matter hyperintensity volume: the Framingham Study. Stroke 35(8):1857–1861 (Epub 2004 Jun 24)
32. Kerber KA, Whitman GT, Brown DL, Baloh RW (2006) Increased risk of death in community-dwelling older people with white matter hyperintensities on MRI. J Neurol Sci 250(1–2):33–38 (Epub 2006 Aug 4)
33. Kloppenborg RP, Nederkoorn PJ, Geerlings MI, van den Berg E (2014) Presence and progression of white matter hyperintensities and cognition: a meta-analysis. Neurology 82(23):2127–2138 (Epub 2014 May 9)
34. Kramer JH, Mungas D, Reed BR, Wetzel ME, Burnett MM, Miller BL, Weiner MW, Chui HC (2007) Longitudinal MRI and cognitive change in healthy elderly. Neuropsychology 21(4):412–418
35. Lo RY, Jagust WJ, Alzheimer’s Disease Neuroimaging Initiative (2012) Vascular burden and Alzheimer disease pathologic progression. Neurology 79(13):1349–1355 (Epub 2012 Sep 12)
36. Maillard P, Carmichael O, Fletcher E, Reed B, Mungas D, DeCarli C (2012) Coevolution of white matter hyperintensities and cognition in the elderly. Neurology 79(5):442–448. doi:10.1212/WNL.0b013e3182617136 (Epub 2012 Jul 18)
37. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (1984) Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology 34(7):939–944
38. Mueller SG, Mack WJ, Mungas D, Kramer JH, Cardenas-Nicolson V, Lavretsky H, Greene M, Schuff N, Chui HC, Weiner MW (2010) Influences of lobar gray matter and white matter lesion load on cognition and mood. Psychiatry Res 181(2):90–96. doi:10.1016/j.pscychresns.2009.08.002 (Epub 2010 Jan 13)
39. Murray ME, Senjem ML, Petersen RC, Hollman JH, Preboske GM, Weigand SD, Knopman DS, Ferman TJ, Dickson DW, Jack CR Jr (2010) Functional impact of white matter hyperintensities in cognitively normal elderly subjects. Arch Neurol 67(11):1379–1385. doi:10.1001/archneurol.2010.280
40. Nordahl CW, Ranganath C, Yonelinas AP, Decarli C, Fletcher E, Jagust WJ (2006) White matter changes compromise prefrontal cortex function in healthy elderly individuals. J Cogn Neurosci 18(3):418–429
41. Novak V, Last D, Alsop DC, Abduljalil AM, Hu K, Lepicovsky L, Cavallerano J, Lipsitz LA (2006) Cerebral blood flow velocity and periventricular white matter hyperintensities in type 2 diabetes. Diabetes Care 29(7):1529–1534
42. Papp KV, Kaplan RF, Springate B, Moscufo N, Wakefield DB, Guttmann CR, Wolfson L (2014) Processing speed in normal aging: effects of white matter hyperintensities and hippocampal volume loss. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn 21(2):197–213. doi:10.1080/13825585.2013.795513 (Epub 2013 Jul 29)
43. Raji CA, Lopez OL, Kuller LH, Carmichael OT, Longstreth WT Jr, Gach HM, Boardman J, Bernick CB, Thompson PM, Becker JT (2012) White matter lesions and brain gray matter volume in cognitively normal elders. Neurobiol Aging 33(4):834.e7–834.e16. doi:10.1016/j.neurobiolaging.2011.08.010 (Epub 2011 Sep 23)
44. Raz N, Yang Y, Dahle CL (1822) Land S (2012) Volume of white matter hyperintensities in healthy adults: contribution of age, vascular risk factors, and inflammation-related genetic variants. Biochim Biophys Acta 3:361–369. doi:10.1016/j.bbadis.2011.08.007 (Epub 2011 Aug 25)
45. Rost NS, Rahman RM, Biffi A, Smith EE, Kanakis A, Fitzpatrick K, Lima F, Worrall BB, Meschia JF, Brown RD Jr, Brott TG, Sorensen AG, Greenberg SM, Furie KL, Rosand J (2010) White matter hyperintensity volume is increased in small vessel stroke subtypes. Neurology 75(19):1670–1677. doi:10.1212/WNL.0b013e3181fc279a
46. Royle NA, Booth T, Valdés Hernández MC, Penke L, Murray C, Gow AJ, Maniega SM, Starr J, Bastin ME, Deary IJ, Wardlaw JM (2013) Estimated maximal and current brain volume predict cognitive ability in old age. Neurobiol Aging 34(12):2726–2733. doi:10.1016/j.neurobiolaging.2013.05.015 (Epub 2013 Jul 11)
47. Satizabal CL, Zhu YC, Mazoyer B, Dufouil C, Tzourio C (2012) Circulating IL-6 and CRP are associated with MRI findings in the elderly: the 3C-Dijon Study. Neurology 78(10):720–727
48. Silbert LC, Nelson C, Howieson DB, Moore MM, Kaye JA (2008) Impact of white matter hyperintensity volume progression on rate of cognitive and motor decline. Neurology 71(2):108–113. doi:10.1212/01.wnl.0000316799.86917.37
49. Silbert LC, Howieson DB, Dodge H, Kaye JA (2009) Cognitive impairment risk: white matter hyperintensity progression matters. Neurology 73(2):120–125. doi:10.1212/WNL.0b013e3181ad53fd
50. Silbert LC, Dodge HH, Perkins LG, Sherbakov L, Lahna D, Erten-Lyons D, Woltjer R, Shinto L, Kaye JA (2012) Trajectory of white matter hyperintensity burden preceding mild cognitive impairment. Neurology 79(8):741–747. doi:10.1212/WNL.0b013e3182661f2b (Epub 2012 Jul 25)
51. Smith SM (2002) Fast robust automated brain extraction. Hum Brain Mapp 17(3):143–155
52. Smith SM, Nichols TE (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localization in cluster inference. Neuroimage 44:83–98
53. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl 1):S208–S219
54. Smith EE, Salat DH, Jeng J, McCreary CR, Fischl B, Schmahmann JD, Dickerson BC, Viswanathan A, Albert MS, Blacker D, Greenberg SM (2011) Correlations between MRI white matter lesion location and executive function and episodic memory. Neurology 76(17):1492–1499. doi:10.1212/WNL.0b013e318217e7c8
55. Söderlund H, Nilsson LG, Berger K, Breteler MM, Dufouil C, Fuhrer R, Giampaoli S, Hofman A, Pajak A, de Ridder M, Sans S, Schmidt R, Launer LJ (2006) Cerebral changes on MRI and cognitive function: the CASCADE study. Neurobiol Aging 27(1):16–23
56. Stein JL, Medland SE, Vasquez AA, Hibar DP, Senstad RE, Winkler AM, Toro R, Appel K, Bartecek R, Bergmann Ø, Enhancing Neuro Imaging Genetics through Meta-Analysis Consortium et al (2012) Identification of common variants associated with human hippocampal and intracranial volumes. Nat Genet 44(5):552–561. doi:10.1038/ng.2250
57. Taki Y, Kinomura S, Sato K, Goto R, Wu K, Kawashima R, Fukuda H (2011) Correlation between gray/white matter volume and cognition in healthy elderly people. Brain Cogn 75(2):170–176. doi:10.1016/j.bandc.2010.11.008 (Epub 2010 Dec 4)
58. van der Flier WM, van Straaten EC, Barkhof F, Verdelho A, Madureira S, Pantoni L, Inzitari D, Erkinjuntti T, Crisby M, Waldemar G, Schmidt R, Fazekas F, Scheltens P (2005) Small vessel disease and general cognitive function in nondisabled elderly: the LADIS study. Stroke 36(10):2116–2120
59. van den Heuvel DM, ten Dam VH, de Craen AJ, Admiraal-Behloul F, Olofsen H, Bollen EL, Jolles J, Murray HM, Blauw GJ, Westendorp RG, van Buchem MA (2006) Increase in periventricular white matter hyperintensities parallels decline in mental processing speed in a non-demented elderly population. J Neurol Neurosurg Psychiatry 77(2):149–153
60. Vannorsdall TD, Waldstein SR, Kraut M, Pearlson GD, Schretlen DJ (2009) White matter abnormalities and cognition in a community sample. Arch Clin Neuropsychol 24(3):209–217. doi:10.1093/arclin/acp037 (Epub 2009 Jul 18)
61. Wakefield DB, Moscufo N, Guttmann CR, Kuchel GA, Kaplan RF, Pearlson G, Wolfson L (2010) White matter hyperintensities predict functional decline in voiding, mobility, and cognition in older adults. J Am Geriatr Soc 58(2):275–281. doi:10.1111/j.1532-5415.2009.02699.x (Epub 2010 Jan 26)
62. Wen W, Sachdev PS, Li JJ, Chen X, Anstey KJ (2009) White matter hyperintensities in the forties: their prevalence and topography in an epidemiological sample aged 44–48. Hum Brain Mapp 30(4):1155–1167. doi:10.1002/hbm.20586
63. Westlye LT, Reinvang I, Rootwelt H, Espeseth T (2012) Effects of APOE on brain white matter microstructure in healthy adults. Neurology 79(19):1961–1969. doi:10.1212/WNL.0b013e3182735c9c (Epub 2012 Oct 24)
64. Wirth M, Villeneuve S, Haase CM, Madison CM, Oh H, Landau SM, Rabinovici GD, Jagust WJ (2013) Associations between Alzheimer disease biomarkers, neurodegeneration, and cognition in cognitively normal older people. JAMA Neurol 70(12):1512–1519. doi:10.1001/jamaneurol.2013.4013
65. Wright CB, Festa JR, Paik MC, Schmiedigen A, Brown TR, Yoshita M, DeCarli C, Sacco R, Stern Y (2008) White matter hyperintensities and subclinical infarction: associations with psychomotor speed and cognitive flexibility. Stroke 39(3):800–805. doi:10.1161/STROKEAHA.107.484147 (Epub 2008 Feb 7)
66. Wright CB, Moon Y, Paik MC, Brown TR, Rabbani L, Yoshita M, DeCarli C, Sacco R, Elkind MS (2009) Inflammatory biomarkers of vascular risk as correlates of leukoariosis. Stroke 40(11):3466–3471. doi:10.1161/STROKEAHA.109.559567 (Epub 2009 Aug 20)
67. Xu H, Stamova B, Jickling G, Tian Y, Zhan X, Ander BP, Liu D, Turner R, Rosand J, Goldstein LB, Furie KL, Verro P, Johnston SC, Sharp FR, Decarli CS (2010) Distinctive RNA expression profiles in blood associated with white matter hyperintensities in brain. Stroke 41(12):2744–2749. doi:10.1161/STROKEAHA.110.591875 (Epub 2010 Oct 21)
68. Ylikoski A, Erkinjuntti T, Raininko R, Sarna S, Sulkava R, Tilvis R (1995) White matter hyperintensities on MRI in the neurologically nondiseased elderly. Analysis of cohorts of consecutive subjects aged 55–85 years living at home. Stroke 26(7):1171–1177
69. Yoshita M, Fletcher E, Harvey D, Ortega M, Martinez O, Mungas DM, Reed BR, DeCarli CS (2006) Extent and distribution of white matter hyperintensities in normal aging, MCI, and AD. Neurology 67(12):2192–2198
70. Zacharaki EI, Kanterakis S, Bryan RN, Davatzikos C (2008) Measuring brain lesion progression with a supervised tissue classification system. Med Image Comput Comput Assist Interv 11(Pt 1):620–627