Alzheimer's & Dementia: The Journal of the Alzheimer's Association
Volume 6, Issue 5 , Pages 394-403 , September 2010

White matter is altered with parental family history of Alzheimer's disease

  • Barbara B. Bendlin

      Affiliations

    • Geriatric Research Educational and Clinical Center, William S. Middleton Memorial Veterans Hospital, Madison, WI, USA
    • Department of Medicine, University of Wisconsin School of Medicine and Public Health, Madison, WI, USA
  • ,
  • Michele L. Ries

      Affiliations

    • Department of Medicine, University of Wisconsin School of Medicine and Public Health, Madison, WI, USA
  • ,
  • Elisa Canu

      Affiliations

    • Geriatric Research Educational and Clinical Center, William S. Middleton Memorial Veterans Hospital, Madison, WI, USA
    • Department of Medicine, University of Wisconsin School of Medicine and Public Health, Madison, WI, USA
  • ,
  • Aparna Sodhi

      Affiliations

    • Geriatric Research Educational and Clinical Center, William S. Middleton Memorial Veterans Hospital, Madison, WI, USA
    • Department of Medicine, University of Wisconsin School of Medicine and Public Health, Madison, WI, USA
  • ,
  • Mariana Lazar

      Affiliations

    • Department of Radiology, New York University School of Medicine, New York, NY, USA
  • ,
  • Andrew L. Alexander

      Affiliations

    • Department of Medical Physics, University of Wisconsin School of Medicine and Public Health, Madison, WI, USA
    • Department of Psychiatry, University of Wisconsin School of Medicine and Public Health, Madison, WI, USA
    • Waisman Laboratory for Brain Imaging and Behavior, Madison, WI, USA
  • ,
  • Cynthia M. Carlsson

      Affiliations

    • Geriatric Research Educational and Clinical Center, William S. Middleton Memorial Veterans Hospital, Madison, WI, USA
    • Department of Medicine, University of Wisconsin School of Medicine and Public Health, Madison, WI, USA
  • ,
  • Mark A. Sager

      Affiliations

    • Geriatric Research Educational and Clinical Center, William S. Middleton Memorial Veterans Hospital, Madison, WI, USA
    • Department of Medicine, University of Wisconsin School of Medicine and Public Health, Madison, WI, USA
  • ,
  • Sanjay Asthana

      Affiliations

    • Geriatric Research Educational and Clinical Center, William S. Middleton Memorial Veterans Hospital, Madison, WI, USA
    • Department of Medicine, University of Wisconsin School of Medicine and Public Health, Madison, WI, USA
  • ,
  • Sterling C. Johnson

      Affiliations

    • Geriatric Research Educational and Clinical Center, William S. Middleton Memorial Veterans Hospital, Madison, WI, USA
    • Department of Medicine, University of Wisconsin School of Medicine and Public Health, Madison, WI, USA
    • Corresponding Author InformationCorresponding author. Tel.: 608-256-1901; Fax: 608-280-7165.

References 

  1. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, et al. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science. 1993;261:921–923
  2. Lind J, Larsson A, Persson J, Ingvar M, Nilsson LG, Bäckman L, et al. Reduced hippocampal volume in non-demented carriers of the apolipoprotein E epsilon4: relation to chronological age and recognition memory. Neurosci Lett. 2006;396:23–27
  3. Wishart HA, Saykin AJ, McAllister TW, Rabin LA, McDonald BC, Flashman LA, et al. Regional brain atrophy in cognitively intact adults with a single APOE epsilon4 allele. Neurology. 2006;67:1221–1224
  4. Bookheimer SY, Strojwas MH, Cohen MS, Saunders AM, Pericak-Vance MA, Mazziotta JC, et al. Patterns of brain activation in people at risk for Alzheimer's disease. N Engl J Med. 2000;343:450–456
  5. Reiman EM, Caselli RJ, Yun LS, Chen K, Bandy D, Minoshima S, et al. Preclinical evidence of Alzheimer's disease in persons homozygous for the epsilon 4 allele for apolipoprotein E. N Engl J Med. 1996;334:752–758
  6. Fleisher AS, Bondi MW, Taylor C, Perry M, Liu TT, Thal LJ, et al. IC-P-043 Functional perfusion MRI shows decreased hippocampal signal with normal aging in ApoE4 carriers. Alzheimers Dement. 2006;2:S671–S672
  7. Nierenberg J, Pomara N, Hoptman MJ, Sidtis JJ, Ardekani BA, Lim KO. Abnormal white matter integrity in healthy apolipoprotein E epsilon4 carriers. Neuroreport. 2005;16:1369–1372
  8. Persson J, Lind J, Larsson A, Ingvar M, Cruts M, Van Broeckhoven C, et al. Altered brain white matter integrity in healthy carriers of the APOE epsilon4 allele: a risk for AD?. Neurology. 2006;66:1029–1033
  9. Cherbuin N, Leach LS, Christensen H, Anstey KJ. Neuroimaging and APOE genotype: a systematic qualitative review. Dement Geriatr Cogn Disord. 2007;24:348–362
  10. Mayeux R, Sano M, Chen J, Tatemichi T, Stern Y. Risk of dementia in first-degree relatives of patients with Alzheimer's disease and related disorders. Arch Neurol. 1991;48:269–273
  11. Green RC, Cupples LA, Go R, Benke KS, Edeki T, Griffith PA, et al. Risk of dementia among white and African American relatives of patients with Alzheimer disease. JAMA. 2002;287:329–336
  12. Jayadev S, Steinbart EJ, Chi YY, Kukull WA, Schellenberg GD, Bird TD. Conjugal Alzheimer disease: risk in children when both parents have Alzheimer disease. Arch Neurol. 2008;65:373–378
  13. Martinez M, Campion D, Brice A, Hannequin D, Dubois B, Didierjean O, et al. Apolipoprotein E epsilon4 allele and familial aggregation of Alzheimer disease. Arch Neurol. 1998;55:810–816
  14. Johnson SC, Ries ML, Hess TM, Carlsson CM, Gleason CE, Alexander AL, et al. Effect of Alzheimer disease risk on brain function during self-appraisal in healthy middle-aged adults. Arch Gen Psychiatry. 2007;64:1163–1171
  15. Johnson SC, Schmitz TW, Trivedi MA, Ries ML, Torgerson BM, Carlsson CM, et al. The influence of Alzheimer disease family history and apolipoprotein E epsilon4 on mesial temporal lobe activation. J Neurosci. 2006;26:6069–6076
  16. Xu G, McLaren DG, Ries ML, Fitzgerald ME, Bendlin BB, Rowley HA, et al. The influence of parental history of Alzheimer's disease and apolipoprotein E {varepsilon}4 on the BOLD signal during recognition memory. Brain. 2009;132(Pt 2):383–391
  17. Fleisher AS, Podraza KM, Bangen KJ, Taylor C, Sherzai A, Sidhar K, et al. Cerebral perfusion and oxygenation differences in Alzheimer's disease risk. Neurobiol Aging. 2009;30:1737–1748
  18. Bassett SS, Yousem DM, Cristinzio C, Kusevic I, Yassa MA, Caffo BS, et al. Familial risk for Alzheimer's disease alters fMRI activation patterns. Brain. 2006;129:1229–1239
  19. Mosconi L, Mistur R, Switalski R, Brys M, Glodzik L, Rich K, et al. Declining brain glucose metabolism in normal individuals with a maternal history of Alzheimer disease. Neurology. 2009;72:513–520
  20. Mosconi L, Brys M, Switalski R, Mistur R, Glodzik L, Pirraglia E, et al. Maternal family history of Alzheimer's disease predisposes to reduced brain glucose metabolism. Proc Natl Acad Sci U S A. 2007;104:19067–19072
  21. Basser PJ. Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR Biomed. 1995;8:333–344
  22. Basser PJ, Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B. 1996;111:209–219
  23. Bartzokis G. Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimer's disease. Neurobiol Aging. 2004;25:5–18author reply 49–62
  24. Desai MK, Sudol KL, Janelsins MC, Mastrangelo MA, Frazer ME, Bowers WJ. Triple-transgenic Alzheimer's disease mice exhibit region-specific abnormalities in brain myelination patterns prior to appearance of amyloid and tau pathology. Glia. 2009;57:54–65
  25. Salat DH, Tuch DS, van der Kouwe AJ, Greve DN, Pappu V, Lee SY, et al. White matter pathology isolates the hippocampal formation in Alzheimer's disease. Neurobiol Aging. 2010;31:244–256
  26. Duan JH, Wang HQ, Xu J, Lin X, Chen SQ, Kang Z, et al. White matter damage of patients with Alzheimer's disease correlated with the decreased cognitive function. Surg Radiol Anat. 2006;28:150–156
  27. Zhang Y, Schuff N, Du AT, Rosen HJ, Kramer JH, Gorno-Tempini ML, et al. White matter damage in frontotemporal dementia and Alzheimer's disease measured by diffusion MRI. Brain. 2009;132(Pt 9):2579–2592
  28. Medina D, DeToledo-Morrell L, Urresta F, Gabrieli JD, Moseley M, Fleischman D, et al. White matter changes in mild cognitive impairment and AD: a diffusion tensor imaging study. Neurobiol Aging. 2006;27:663–672
  29. Fellgiebel A, Wille P, Muller MJ, Winterer G, Scheurich A, Vucurevic G, et al. Ultrastructural hippocampal and white matter alterations in mild cognitive impairment: a diffusion tensor imaging study. Dement Geriatr Cogn Disord. 2004;18:101–108
  30. Rose SE, Janke AL, Chalk JB. Gray and white matter changes in Alzheimer's disease: a diffusion tensor imaging study. J Magn Reson Imaging. 2008;27:20–26
  31. Rose SE, McMahon KL, Janke AL, O'Dowd B, de Zubicaray G, Strudwick MW, et al. Diffusion indices on magnetic resonance imaging and neuropsychological performance in amnestic mild cognitive impairment. J Neurol Neurosurg Psychiatry. 2006;77:1122–1128
  32. Fellgiebel A, Muller MJ, Wille P, Dellani PR, Scheurich A, Schmidt LG, et al. Color-coded diffusion-tensor-imaging of posterior cingulate fiber tracts in mild cognitive impairment. Neurobiol Aging. 2005;26:1193–1198
  33. Sager MA, Hermann B, La Rue A. Middle-aged children of persons with Alzheimer's disease: APOE genotypes and cognitive function in the Wisconsin Registry for Alzheimer's Prevention. J Geriatr Psychiatry Neurol. 2005;18:245–249
  34. Morris JC, Heyman A, Mohs RC, Hughes JP, van Belle G, Fillenbaum G, et al. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD): part I—clinical and neuropsychological assessment of Alzheimer's disease. Neurology. 1989;39:1159–1165
  35. Folstein MF, Folstein SE, McHugh PR. “Mini Mental State”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12:189–198
  36. Wechsler D. Wechsler Adult Intelligence Scale. 3rd ed.. New York, NY: Psychological Corporation; 1997;
  37. Spreen O, Strauss E. A compendium of neuropsychological tests. New York, NY: Oxford University Press; 1998;
  38. Reitan RM, Wolfson D. The Halstead-Reitan neuropsychological test battery: theory and clinical interpretation. 2nd ed.. Tucson, AZ: Neuropsychology Press; 1993;
  39. Benton AL. Neuropsychological assessment. Annu Rev Psychol. 1994;45:1–23
  40. Bendlin BB, Ries ML, Lazar M, Alexander AL, Dempsey RJ, Rowley HA, et al. Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging. Neuroimage. 2008;42:503–514
  41. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage. 2004;23(Suppl 1):S208–S219
  42. Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, Neufeld AH. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage. 2003;20:1714–1722
  43. Pierpaoli C, Barnett A, Pajevic S, Chen R, Penix LR, Virta A, et al. Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. Neuroimage. 2001;13:1174–1185
  44. Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage. 2002;17:1429–1436
  45. Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, et al. Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage. 2005;26:132–140
  46. Naggara O, Oppenheim C, Rieu D, Raoux N, Rodrigo S, Dalla Barba G, et al. Diffusion tensor imaging in early Alzheimer's disease. Psychiatr Res. 2006;146:243–249
  47. Zhang Y, Schuff N, Jahng GH, Bayne W, Mori S, Schad L, et al. Diffusion tensor imaging of cingulum fibers in mild cognitive impairment and Alzheimer disease. Neurology. 2007;68:13–19
  48. Kavcic V, Ni H, Zhu T, Zhong J, Duffy CJ. White matter integrity linked to functional impairments in aging and early Alzheimer's disease. Alzheimers Dement. 2008;4:381–389
  49. Sugihara S, Kinoshita T, Matsusue E, Fujii S, Ogawa T. Usefulness of diffusion tensor imaging of white matter in Alzheimer disease and vascular dementia. Acta Radiol. 2004;45:658–663
  50. Choo IH, Lee DY, Oh JS, Lee JS, Lee DS, Song IC, et al. Posterior cingulate cortex atrophy and regional cingulum disruption in mild cognitive impairment and Alzheimer's disease. Neurobiol Aging. 2010;31:772–779
  51. Rose SE, Chen F, Chalk JB, Zelaya FO, Strugnell WE, Benson M, et al. 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. 2000;69:528–530
  52. Kantarci K, Jack CR, Xu YC, Campeau NG, O'Brien PC, Smith GE, et al. Mild cognitive impairment and Alzheimer disease: regional diffusivity of water. Radiology. 2001;219:101–107
  53. Ronen I, Kim KH, Garwood M, Ugurbil K, Kim DS. Conventional DTI vs. slow and fast diffusion tensors in cat visual cortex. Magn Reson Med. 2003;49:785–790
  54. Shepherd TM, Ozarslan E, Yachnis AT, King MA, Blackband SJ. Diffusion tensor microscopy indicates the cytoarchitectural basis for diffusion anisotropy in the human hippocampus. AJNR Am J Neuroradiol. 2007;28:958–964
  55. Cho H, Yang DW, Shon YM, Kim BS, Kim YI, Choi YB, et al. Abnormal integrity of cortico-cortical tracts in mild cognitive impairment: a diffusion tensor imaging study. J Korean Med Sci. 2008;23:477–483
  56. Kim H, Piao Z, Liu P, Bingaman W, Diehl B. Secondary white matter degeneration of the corpus callosum in patients with intractable temporal lobe epilepsy: a diffusion tensor imaging study. Epilepsy Res. 2008;81:136–142
  57. Taoka T, Iwasaki S, Sakamoto M, Nakagawa H, Fukusumi A, Myochin K, et al. Diffusion anisotropy and diffusivity of white matter tracts within the temporal stem in Alzheimer disease: evaluation of the “tract of interest” by diffusion tensor tractography. AJNR Am J Neuroradiol. 2006;27:1040–1045
  58. Fujie S, Namiki C, Nishi H, Yamada M, Miyata J, Sakata D, et al. The role of the uncinate fasciculus in memory and emotional recognition in amnestic mild cognitive impairment. Dement Geriatr Cogn Disord. 2008;26:432–439
  59. Chua TC, Wen W, Chen X, Kochan N, Slavin MJ, Trollor JN, et al. Diffusion tensor imaging of the posterior cingulate is a useful biomarker of mild cognitive impairment. Am J Geriatr Psychiatry. 2009;17:602–613
  60. Wang L, Goldstein FC, Veledar E, Levey AI, Lah JJ, Meltzer CC, et al. Alterations in cortical thickness and white matter integrity in mild cognitive impairment measured by whole-brain cortical thickness mapping and diffusion tensor imaging. AJNR Am J Neuroradiol. 2009;30:893–899
  61. Bartzokis G, Lu PH, Geschwind DH, Edwards N, Mintz J, Cummings JL. Apolipoprotein E genotype and age-related myelin breakdown in healthy individuals: implications for cognitive decline and dementia. Arch Gen Psychiatry. 2006;63:63–72
  62. Bartzokis G, Lu PH, Geschwind DH, Tingus K, Huang D, Mendez MF, et al. Apolipoprotein E affects both myelin breakdown and cognition: implications for age-related trajectories of decline into dementia. Biol Psychiatry. 2007;62:1380–1387
  63. Honea RA, Vidoni E, Harsha A, Burns JM. Impact of APOE on the healthy aging brain: a voxel-based MRI and DTI study. J Alzheimers Dis (in press).
  64. Ertekin-Taner N, Younkin LH, Yager DM, Parfitt F, Baker MC, Asthana S, et al. Plasma amyloid beta protein is elevated in late-onset Alzheimer disease families. Neurology. 2008;70:596–606
  65. La Rue A, Hermann B, Jones JE, Johnson S, Asthana S, Sager MA. Effect of parental family history of Alzheimer's disease on serial position profiles. Alzheimers Dement. 2008;4:285–290
  66. Snowden JS, Stopford CL, Julien CL, Thompson JC, Davidson Y, Gibbons L, et al. Cognitive phenotypes in Alzheimer's disease and genetic risk. Cortex. 2007;43:835–845
  67. Handley OJ, Morrison CM, Miles C, Bayer AJ. ApoE gene and familial risk of Alzheimer's disease as predictors of odour identification in older adults. Neurobiol. Aging. 2006;27:1425–1430
  68. Edland SD, Silverman JM, Peskind ER, Tsuang D, Wijsman E, Morris JC. Increased risk of dementia in mothers of Alzheimer's disease cases: evidence for maternal inheritance. Neurology. 1996;47:254–256
  69. La Rue A, O'Hara R, Matsuyama SS, Jarvik LF. Cognitive changes in young-old adults: effect of family history of dementia. J Clin Exp Neuropsychol. 1995;17:65–70
  70. Hom J, Turner MB, Risser R, Bonte FJ, Tintner R. Cognitive deficits in asymptomatic first-degree relatives of Alzheimer's disease patients. J Clin Exp Neuropsychol. 1994;16:568–576
  71. Scheltens P, Barkhof F, Leys D, Wolters EC, Ravid R, Kamphorst W. Histopathologic correlates of white matter changes on MRI in Alzheimer's disease and normal aging. Neurology. 1995;45:883–888
  72. Roher AE, Weiss N, Kokjohn TA, Kuo YM, Kalback W, Anthony J, et al. Increased A beta peptides and reduced cholesterol and myelin proteins characterize white matter degeneration in Alzheimer's disease. Biochemistry. 2002;41:11080–11090
  73. Braak H, Braak E. Development of Alzheimer-related neurofibrillary changes in the neocortex inversely recapitulates cortical myelogenesis. Acta Neuropathol. 1996;92:197–201
  74. Rogers J, Webster S, Lue LF, Brachova L, Civin WH, Emmerling M, et al. Inflammation and Alzheimer's disease pathogenesis. Neurobiol Aging. 1996;17:681–686
  75. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, et al. Inflammation and Alzheimer's disease. Neurobiol Aging. 2000;21:383–421
  76. McGeer EG, McGeer PL. Inflammatory processes in Alzheimer's disease. Prog Neuropsychopharmacol Biol Psychiatry. 2003;27:741–749
  77. McGeer PL, McGeer EG. Local neuroinflammation and the progression of Alzheimer's disease. J Neurovirol. 2002;8:529–538
  78. Braak H, Braak E. Frequency of stages of Alzheimer-related lesions in different age categories. Neurobiol Aging. 1997;18:351–357
  79. Roher AE, Kuo YM, Esh C, Knebel C, Weiss N, Kalback W, et al. Cortical and leptomeningeal cerebrovascular amyloid and white matter pathology in Alzheimer's disease. Mol Med. 2003;9:112–122
  80. Stenset V, Bjornerud A, Fjell AM, Walhovd KB, Hofoss D, Due-Tønnessen P, et al. Cingulum fiber diffusivity and CSF T-tau in patients with subjective and mild cognitive impairment. Neurobiol Aging. 2009 May 9;[Epublication ahead of print]
  81. Bartzokis G, Sultzer D, Lu PH, Nuechterlein KH, Mintz J, Cummings JL. Heterogeneous age-related breakdown of white matter structural integrity: implications for cortical “disconnection” in aging and Alzheimer's disease. Neurobiol Aging. 2004;25:843–851
  82. Schmierer K, Wheeler-Kingshott CA, Boulby PA, Scaravilli F, Altmann DR, Barker GJ, et al. Diffusion tensor imaging of post mortem multiple sclerosis brain. Neuroimage. 2007;35:467–477
  83. Gouw AA, Seewann A, Vrenken H, van der Flier WM, Rozemuller JM, Barkhof F, et al. Heterogeneity of white matter hyperintensities in Alzheimer's disease: post-mortem quantitative MRI and neuropathology. Brain. 2008;131:3286–3298
  84. Larsson EM, Englund E, Sjobeck M, Latt J, Brockstedt S. MRI with diffusion tensor imaging post-mortem at 3.0 T in a patient with frontotemporal dementia. Dement Geriatr Cogn Disord. 2004;17:316–319
  85. Englund E, Sjobeck M, Brockstedt S, Latt J, Larsson EM. Diffusion tensor MRI post mortem demonstrated cerebral white matter pathology. J Neurol. 2004;251:350–352
  86. Snook L, Plewes C, Beaulieu C. Voxel based versus region of interest analysis in diffusion tensor imaging of neurodevelopment. Neuroimage. 2007;34:243–252
  87. Chao TC, Chou MC, Yang P, Chung HW, Wu MT. Effects of interpolation methods in spatial normalization of diffusion tensor imaging data on group comparison of fractional anisotropy. Magn Reson Imaging. 2009;27:681–690
  88. Yarkoni T. Big correlations in little studies: inflated fMRI correlations reflect low statistical power. Perspect Psychol Sci. 2009;4:294–298

PII: S1552-5260(09)02333-4

doi: 10.1016/j.jalz.2009.11.003

Alzheimer's & Dementia: The Journal of the Alzheimer's Association
Volume 6, Issue 5 , Pages 394-403 , September 2010