Cerebral small vessel disease affects white matter microstructure in mild cognitive impairment

Human Brain Mapping

Volumn 35, Issue 6, 2014, Pages 2836-2851

  Papma, Janne M ^a   de Groot, Marius ^a   de Koning, Inge ^a   Mattace Raso, Francesco U ^a   van der Lugt, Aad ^a   Vernooij, Meike W ^a   Niessen, Wiro J ^a,b   van Swieten, John C ^a   Koudstaal, Peter J ^a   Prins, Niels D ^c   Smits, Marion ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Cerebral small vessel disease; Default mode network; Diffusion tensor imaging; Mild cognitive impairment

Indexed keywords

AGED; BRAIN; CEREBROVASCULAR DISEASE; COHORT ANALYSIS; COMPLICATION; DIFFUSION TENSOR IMAGING; FEMALE; HUMAN; IMAGE PROCESSING; MALE; MILD COGNITIVE IMPAIRMENT; MYELINATED NERVE; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; ORGAN SIZE; PATHOLOGY; REGRESSION ANALYSIS; WHITE MATTER;

AGED; BRAIN; CEREBRAL SMALL VESSEL DISEASES; COHORT STUDIES; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MILD COGNITIVE IMPAIRMENT; NERVE FIBERS, MYELINATED; NEUROPSYCHOLOGICAL TESTS; ORGAN SIZE; REGRESSION ANALYSIS; WHITE MATTER;

EID: 84899102572     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22370     Document Type: Article

References (90)

1. 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.
2. Bai F, Zhang Z, Watson DR, Yu H, Shi Y, Yuan Y, Qian Y, Jia J (2009): Abnormal integrity of association fiber tracts in amnestic mild cognitive impairment. J Neurol Sci 278:102-106.
3. Bai F, Zhang Z, Yu H, Shi Y, Yuan Y, Zhu W, Zhang X, Qian Y (2008): Default-mode network activity distinguishes amnestic type mild cognitive impairment from healthy aging: A combined structural and resting-state functional MRI study. Neurosci Lett 438:111-115.
4. Bartzokis G (2004): Age-related myelin breakdown: A developmental model of cognitive decline and Alzheimer's disease. Neurobiol Aging 25:5-18; author reply 49-62.
5. Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW (2007): Probabilistic diffusion tractography with multiple fibre orientations: What can we gain?. Neuroimage 34:144-155.
6. Bosch B, Arenaz-Urquijo EM, Rami L, Sala-Llonch R, Junqué C, Solé-Padullés C, Peňa-Gómez C, Bargalló N, Molinuevo JL, Bartrés-Faz D (2012): Multiple DTI index analysis in normal aging, amnestic MCI and AD. Relationship with neuropsychological performance. Neurobiol Aging 33:61-74.
7. Bozoki AC, Korolev IO, Davis NC, Hoisington LA, Berger KL (2012): Disruption of limbic white matter pathways in mild cognitive impairment and Alzheimer's disease: A DTI/FDG-PET study. Hum Brain Mapp 22:1792-1802.
8. Bozzali M, Filippi M, Magnani G, Cercignani M, Franceschi M, Schiatti E, Castiglioni S, Mossini R, Falautano M, Scotti G, Comi G, Falini A (2006): The contribution of voxel-based morphometry in staging patients with mild cognitive impairment. Neurology 67:453-460.
9. Braak H, Braak E (1991): Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82:239-259.
10. Buckner RL, Andrews-Hanna JR, Schacter DL (2008): The brain's default network: Anatomy, function, and relevance to disease. Ann NY Acad Sci 1124:1-38.
11. Chen TF, Lin CC, Chen YF, Liu HM, Hua MS, Huang YC, Chiu MJ (2009): Diffusion tensor changes in patients with amnesic mild cognitive impairment and various dementias. Psychiatry Res 173:15-21.
12. Cherubini A, Péran P, Spoletini I, Di Paulo M, Di Iulio F, Hagberg GE, Scancesario G, Gianni W, Bossù P, Caltagirone C, Sabatini U, Spalletta G (2010): Structures of mild cognitive impiarment and Alzheimer's disease patients. J Alzheimers Dis 19:1273-1282.
13. Chetelat G, Landeau B, Eustache F, Mezenge F, Viader F, de la Sayette V, Desgranges B, Baron JC (2005): Using voxel-based morphometry to map the structural changes associated with rapid conversion in MCI: a longitudinal MRI study. Neuroimage 27:934-946.
14. Chua TC, Wen W, Chen X, Kochan N, Slavin MJ, Trollor JN, Brodaty H, Sachdev PS (2009): Diffusion tensor imaging of the posterior cingulate is a useful biomarker of mild cognitive impairment. Am J Geriatr Psychiatry 17:602-613.
15. Damoiseaux JS, Greicius MD (2009): Greater than the sum of its parts: a review of studies combining structural connectivity and resting-state functional connectivity. Brain Struct Funct 213:525-533.
16. Damoiseaux JS, Smith SM, Witter MP, Sanz-Arigita EJ, Barkhof F, Scheltens P, Stam CJ, Zarei M, Rombouts SA (2009): White matter tract integrity in aging and Alzheimer's disease. Hum Brain Mapp 30:1051-1059.
17. de Boer R, Vrooman HA, van der Lijn F, Vernooij MW, Ikram MA, van der Lugt A, Breteler MM, Niessen WJ (2009): White matter lesion extension to automatic brain tissue segmentation on MRI. Neuroimage 45:1151-1161.
18. de Groot M, Verhaaren BFJ, de Boer R, Klein S, Hofman A, van der Lugt A, Ikram MA, Niessen WJ, Vernooij MW (2013): Changes in normal-appearing white matter precede development of white matter lesions. Stroke 44:1037-1042.
19. de Reuck J (1971): The human periventricular arterial blood supply and the anatomy of cerebral infarctions. Eur Neurol 5:321-334.
20. DeCarli C (2003): Mild cognitive impairment: Prevalence, prognosis, aetiology, and treatment. Lancet Neurol 2:15-21.
21. den Heijer T, van der Lijn F, Koudstaal PJ, Hofman A, van der Lugt A, Krestin GP, Niessen WJ, Breteler MM (2010): A 10-year follow-up of hippocampal volume on magnetic resonance imaging in early dementia and cognitive decline. Brain 133:1163-1172.
22. Dickerson BC, Goncharova I, Sullivan MP, Forchetti C, Wilson RS, Bennett DA, Beckett LA, deToledo-Morrell L (2001): MRI-derived entorhinal and hippocampal atrophy in incipient and very mild Alzheimer's disease. Neurobiol Aging 22:747-754.
23. Englund E, Brun A, Alling C (1988): White matter changes in dementia of Alzheimer's type. Biochemical and neuropathological correlates. Brain 111:1425-1439.
24. Erkinjuntti T, Gauthier S (2009): The concept of vascular cognitive impairment. Front Neurol Neurosci 24:79-85.
25. Fazekas F, Barkhof F, Wahlund LO, Pantoni L, Erkinjuntti T, Scheltens P, Schmidt R (2002): CT and MRI rating of white matter lesions. Cerebrovasc Dis 13(Suppl 2):31-36.
26. Frisoni GB, Galluzzi S, Bresciani L, Zanetti O, Geroldi C (2002): Mild cognitive impairment with subcortical vascular features: clinical characteristics and outcome. J Neurol 249:1423-1432.
27. Greicius MD, Krasnow B, Reiss AL, Menon V (2003): Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proc Natl Acad Sci USA 100:253-258.
28. Greicius MD, Srivastava G, Reiss AL, Menon V (2004): Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc Natl Acad Sci USA 101:4637-4642.
29. Greicius MD, Supekar K, Menon V, Dougherty RF (2009): Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 19:72-78.
30. Horsfield MA, Jones DK (2002): Applications of diffusion-weighted and diffusion tensor MRI to white matter diseases-A review. NMR Biomed 15:570-577.
31. Iadecola C (2010): The overlap between neurodegenerative and vascular factors in the pathogenesis of dementia. Acta Neuropathol 120:287-296.
32. 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 55:484-489.
33. Jenkinson M, Smith S (2001): A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143-156.
34. Kalus P, Slotboom J, Gallinat J, Mahlberg R, Cattapan-Ludewig K, Wiest R, Nyffeler T, Buri C, Federspiel A, Kunz D, Schroth G, Kiefer C (2006): Examining the gateway to the limbic system with diffusion tensor imaging: the perforant pathway in dementia. Neuroimage 30:713-720.
35. Karas GB, Scheltens P, Rombouts SA, Visser PJ, van Schijndel RA, Fox NC, Barkhof F (2004): Global and local gray matter loss in mild cognitive impairment and Alzheimer's disease. Neuroimage 23:708-716.
36. Kiuchi K, Morikawa M, Taoka T, Nagashima T, Yamauchi T, Makinodan M, Norimoto K, Hashimoto K, Kosaka J, Inoue Y, Kichikawa K (2009) Brain Res 1287:184-191.
37. Klein S, Staring M, Murphy K, Viergever MA, Pluim JP (2010): elastix: A toolbox for intensity-based medical image registration. IEEE Trans Med Imaging 29:196-205.
38. Liu Y, Spulber G, Lehtimaki KK, Kononen M, Hallikainen I, Grohn H, Kivipelto M, Hallikainen M, Vanninen R, Soininen H (2011): Diffusion tensor imaging and tract-based spatial statistics in Alzheimer's disease and mild cognitive impairment. Neurobiol Aging 32:1558-1571.
39. Longstreth WT, Jr., Manolio TA, Arnold A, Burke GL, Bryan N, Jungreis CA, Enright PL, O'Leary D, Fried L (1996): Clinical correlates of white matter findings on cranial magnetic resonance imaging of 3301 elderly people. The Cardiovascular Health Study. Stroke 27:1274-1282.
40. Luchsinger JA, Brickman AM, Reitz C, Cho SJ, Schupf N, Manly JJ, Tang MX, Small SA, Mayeux R, DeCarli C, Brown TR (2009): Subclinical cerebrovascular disease in mild cognitive impairment. Neurology 73:450-456.
41. Maillard P, Fletcher E, Harvey D, Carmichael O, Reed B, Mungas D, DeCarli C (2011): White matter hyperintensity penumbra. Stroke 42:1917-1922.
42. Maillard P, Carmichael O, Harvey D, Fletcher E, Reed B, Mungas D, DeCarli C (2013): FLAIR AND Diffusion MRI signals are independent predictors of white matter hyperintensities. AJNR Am J Neuroradiol 34:54-61.
43. Mayda AB, Westphal A, Carter CS, DeCarli C (2011): Late life cognitive control deficits are accentuated by white matter disease burden. Brain 134:1673-1683.
44. Mielke MM, Kozauer NA, Chan KCG, George M, Toroney J, Zerrate M, Bandeen-Roche K, Wang MC, van Zijl P, Pekar JJ, Mori S, Lyketos CG, Albert M (2009): Regionally-specific diffusion tensor imaging in mild cognitive impairment and Alzheimer's disease. Neuroimage 46:47-55.
45. Mori S, Kaufmann WE, Davatzikos C, Stieltjes B, Amodei L, Fredericksen K, Pearlson GD, Melhem ER, Solaiyappan M, Raymond GV, Moser HW, van Zijl PC (2002): Imaging cortical association tracts in the human brain using diffusion-tensor-based axonal tracking. Magn Reson Med 47:215-223.
46. Nordahl CW, Ranganath C, Yonelinas AP, DeCarli C, Reed BR, Jagust WJ (2005): Different mechanisms of episodic memory failure in mild cognitive impairment. Neuropsychologia 43:1688-1697.
47. O'Sullivan M, Summers PE, Jones DK, Jarosz JM, Williams SC, Markus HS (2001): Normal-appearing white matter in ischemic leukoaraiosis: a diffusion tensor MRI study. Neurology 57:2307-2310.
48. Pantoni L (2010): Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 9:689-701.
49. Perneczky R, Wagenpfeil S, Komossa K, Grimmer T, Diehl J, Kurz A (2006): Mapping scores onto stages: mini-mental state examination and clinical dementia rating. Am J Geriatr Psychiatry 14:139-144.
50. Petersen RC (2004): Mild cognitive impairment as a diagnostic entity. J Intern Med 256:183-194.
51. Prins ND, van Dijk EJ, den Heijer T, Vermeer SE, Jolles J, Koudstaal PJ, Hofman A, Breteler MM (2005): Cerebral small-vessel disease and decline in information processing speed, executive function and memory. Brain 128:2034-2041.
52. Raff MC, Whitmore AV, Finn JT (2002): Axonal self-destruction and neurodegeneration. Science 296:868-871.
53. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001): A default mode of brain function. Proc Natl Acad Sci USA 98:676-682.
54. Reed BR, Mungas DM, Kramer JH, Ellis W, Vinters HV, Zarow C, Jagust WJ, Chui HC (2007): Profiles of neuropsychological impairment in autopsy-defined Alzheimer's disease and cerebrovascular disease. Brain 130:731-739.
55. Rocca MA, Valsasina P, Absinta M, Riccitelli G, Rodegher ME, Misci P, Rossi P, Falini A, Comi G, Filippi M (2010): Default-mode network dysfunction and cognitive impairment in progressive MS. Neurology 74:1252-1259.
56. Rogalski EJ, Murphy CM, deToledo-Morrell L, Shah RC, Moseley ME, Bammer R, Stebbins GT (2009): Changes in parahippocampal white matter integrity in amnestic mild cognitive impairment: A diffusion tensor imaging study. Behav Neurol 21:51-61.
57. Rose SE, Chen F, Chalk JB, Zelaya FO, Strugnell WE, Benson M, Semple J, Doddrell DM (2000): Loss of connectivity in Alzheimer's disease: An evaluation of white matter tract integrity with colour coded MR diffusion tensor imaging. J Neurol Neurosurg Psychiatry 69:528-530.
58. Schmidtke K, Hull M (2005): Cerebral small vessel disease: how does it progress? J Neurol Sci 229:13-20.
59. Schneider JA, Bienias JL, Wilson RS, Berry-Kavis E, Evans DA, Bennett DA (2005): The apolipoprotein E4 allele increases the odds of chronic cerebral infarction detected at autopsy in older persons. Stroke 36:954-959.
60. Seeley WW, Crawford RK, Zhou J, Miller BL, Greicius MD (2009): Neurodegenerative diseases target large-scale human brain networks. Neuron 62:42-52.
61. Sexton CE, Kalu UG, Filippini N, Mackay CE, Ebmeier KP (2011): A meta-analysis of diffusion tensor imaging in mild cognitive impairment and Alzheimer's disease. Neurobiol Aging 32:e2325-e2318.
62. Smith SM (2002): Fast robust automated brain extraction. Hum Brain Mapp 17:143-155.
63. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TE (2006): Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487-1505.
64. Smith SM, Nichols TE (2009): Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44:83-98.
65. Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, Armstrong RC (2005): Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 26:132-140.
66. Stieltjes B, Kaufmann WE, van Zijl PC, Fredericksen K, Pearlson GD, Solaiyappan M, Mori S (2001): Diffusion tensor imaging and axonal tracking in the human brainstem. Neuroimage 14:723-735.
67. Sun SW, Liang HF, Le TQ, Armstrong RC, Cross AH, Song SK (2006): Differential sensitivity of in vivo and ex vivo diffusion tensor imaging to evolving optic nerve injury in mice with retinal ischemia. Neuroimage 32:1195-1204.
68. Sydykova D, Stahl R, Dietrich O, Ewers M, Reiser MF, Schoenberg SO, Moller HJ, Hampel H, Teipel SJ (2007): Fiber connections between the cerebral cortex and the corpus callosum in Alzheimer's disease: A diffusion tensor imaging and voxel-based morphometry study. Cereb Cortex 17:2276-2282.
69. Targosz-Gajniak M, Siuda J, Ochudlo S, Opala G (2009): Cerebral white matter lesions in patients with dementia-From MCI to severe Alzheimer's disease. J Neurol Sci 283:79-82.
70. Thal DR, Holzer M, Rüb U, Waldmann G, Günzel S, Zedlick D, Schober R (2000): Alzheimer-related tau-pathology in the perforant path arget zone and in the hippocampal stratum oriens and radiatum correlates with onset and degree of dementia. Exp Neurol 163:98-110.
71. Teipel SJ, Bokde AL, Meindl T, Amaro E Jr, Soldner J, Reiser MF, Herpertz SC, Moller HJ, Hampel H (2010): White matter microstructure underlying default mode network connectivity in the human brain. Neuroimage 49:2021-2032.
72. van den Heuvel M, Mandl R, Luigjes J, Hulshoff Pol H (2008): Microstructural organization of the cingulum tract and the level of default mode functional connectivity. J Neurosci 28:10844-10851.
73. van den Heuvel MP, Mandl RC, Kahn RS, Hulshoff Pol HE (2009): Functionally linked resting-state networks reflect the underlying structural connectivity architecture of the human brain. Hum Brain Mapp 30:3127-3141.
74. van der Lijn F, den Heijer T, Breteler MM, Niessen WJ (2008): Hippocampus segmentation in MR images using atlas registration, voxel classification, and graph cuts. Neuroimage 43:708-720.
75. Van der Lijn F, de Bruijne M, Klein S, den Heijer T, Hoogendam YY, van der Lugt A, Breteler MM, Niessen WJ (2012): Automated brain structure segmentation based on atlas registration and appearance models. IEEE Trans Med Imaging 31:276-286.
76. Verhage F (1964): Intelligentie en leeftijd: onderzoek bij Nederlanders van twaalf tot zevenenzeventig jaar [Intelligence and age: Research on Dutch People Aged Twelve to Seventy-Seven Years Old]. Assen: Van Gorcum.
77. Vernooij MW, de Groot M, van der Lugt A, Ikram MA, Krestin GP, Hofman A, Niessen WJ, Breteler MM (2008): White matter atrophy and lesion formation explain the loss of structural integrity of white matter in aging. Neuroimage 43:470-477.
78. Villain N, Desgranges B, Viader F, de la Sayette V, Mezenge F, Landeau B, Baron JC, Eustache F, Chetelat G (2008): Relationships between hippocampal atrophy, white matter disruption, and gray matter hypometabolism in Alzheimer's disease. J Neurosci 28:6174-6181.
79. Villeneuve S, Massoud F, Bocti C, Gauthier S, Belleville S (2011): The nature of episodic memory deficits in MCI with and without vascular burden. Neuropsychologia 49:3027-3035.
80. Vrooman HA, Cocosco CA, van der Lijn F, Stokking R, Ikram MA, Vernooij MW, Breteler MM, Niessen WJ (2007): Multi-spectral brain tissue segmentation using automatically trained k-Nearest-Neighbor classification. Neuroimage 37:71-81.
81. Wakana S, Caprihan A, Panzenboeck MM, Fallon JH, Perry M, Gollub RL, Hua K, Zhang J, Jiang H, Dubey P, Blitz A, van Zijl P, Mori S (2007): Reproducibility of quantitative tractography methods applied to cerebral white matter. Neuroimage 36:630-644.
82. Wakana S, Jiang H, Nagae-Poetscher LM, van Zijl PC, Mori S (2004): Fiber tract-based atlas of human white matter anatomy. Radiology 230:77-87.
83. Wang DS, Bennett DA, Mufson EJ, Mattila P, Cochran E, Dickson DW (2004): Contribution of changes in ubiquitin and myelin basic protein to age-related cognitive decline. Neurosci Res 48:93-100.
84. Witter MP, Wouterlood FG, Naber PA, Van Haeften T (2000): Anatomical organization of the parahippocampal-hippocampal network. Ann NY Acad Sci 911:1-24.
85. Woolrich MW, Jbabdi S, Patenaude B, Chappell M, Makni S, Behrens T, Beckmann C, Jenkinson M, Smith SM (2009): Bayesian analysis of neuroimaging data in FSL. Neuroimage 45:S173-S186.
86. Xie S, Xiao JX, Gong GL, Zang YF, Wang YH, Wu HK, Jiang XX (2006): Voxel-based detection of white matter abnormalities in mild Alzheimer disease. Neurology 66:1845-1849.
87. Yip AG, McKee AC, Green RC, Wells J, Young H, Cupples LA, Farrer La (2005): APOE, vascular pathology and the AD brain. Neurology 65:259-265
88. 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 67:2192-2198.
89. Zhou Y, Dougherty JH Jr, Hubner KF, Bai B, Cannon RL, Hutson RK (2008): Abnormal connectivity in the posterior cingulate and hippocampus in early Alzheimer's disease and mild cognitive impairment. Alzheimers Dement 4:265-270.
90. Zhuang L, Wen W, Zhu W, Trollor J, Kochan N, Crawford J, Reppermund S, Brodaty H, Sachdev P (2010): White matter integrity in mild cognitive impairment: A tract-based spatial statistics study. Neuroimage 53:16-25.