Midlife measurements of white matter microstructure predict subsequent regional white matter atrophy in healthy adults - PubMed (original) (raw)
. 2014 May;35(5):2044-54.
doi: 10.1002/hbm.22311. Epub 2013 Jul 17.
Affiliations
- PMID: 23861348
- PMCID: PMC3895105
- DOI: 10.1002/hbm.22311
Midlife measurements of white matter microstructure predict subsequent regional white matter atrophy in healthy adults
Martina Ly et al. Hum Brain Mapp. 2014 May.
Abstract
Objectives: Although age-related brain changes are becoming better understood, midlife patterns of change are still in need of characterization, and longitudinal studies are lacking. The aim of this study was to determine if baseline fractional anisotropy (FA), obtained from diffusion tensor imaging (DTI) predicts volume change over a 4-year interval.
Experimental design: Forty-four cognitively healthy middle-age adults underwent baseline DTI and longitudinal T1-weighted magnetic resonance imaging. Tensor-based morphometry methods were used to evaluate volume change over time. FA values were extracted from regions of interest that included the cingulum, entorhinal white matter, and the genu and splenium of the corpus callosum. Baseline FA was used as a predictor variable, whereas gray and white matter atrophy rates as indexed by Tensor-based morphometry were the dependent variables.
Principal observations: Over a 4-year period, participants showed significant contraction of white matter, especially in frontal, temporal, and cerebellar regions (P < 0.05, corrected for multiple comparisons). Baseline FA in entorhinal white matter, genu, and splenium was associated with longitudinal rates of atrophy in regions that included the superior longitudinal fasciculus, anterior corona radiata, temporal stem, and white matter of the inferior temporal gyrus (P < 0.001, uncorrected for multiple comparisons).
Conclusions: Brain change with aging is characterized by extensive shrinkage of white matter. Baseline white matter microstructure as indexed by DTI was associated with some of the observed regional volume loss. The findings suggest that both white matter volume loss and microstructural alterations should be considered more prominently in models of aging and neurodegenerative diseases.
Keywords: aging; atrophy; diffusion tensor imaging; fractional anisotropy; longitudinal; microstructure; tensor-based morphometry.
Copyright © 2013 Wiley Periodicals, Inc.
Figures
Figure 1
White matter ROIs (shown in red) overlayed on the FA template image (skeletonized FA underlayed in light gray). The bilateral ROIs included: (A) cingulum bundle subjacent to posterior cingulate (119 voxels, MNI coordinates: ±11,−45, 28), (B) cingulum adjacent to hippocampus (60 voxels, MNI coordinates: ±20, −42, −2), (C) entorhinal white matter (96 voxels, MNI coordinates: ±24, −26, −19), (D) corticospinal tract (31 voxels, MNI coordinates: ±10, −20, −24), (E) splenium (49 voxels, MNI coordinates: ±1, −35, 14), and (F) genu (48 voxels, MNI coordinates: ±4, 23, −1) of the corpus callosum. (A–C) Sagittal view, (D) coronal view, and (E, F) an axial view.
Figure 2
Regions of tissue contraction for more than 4 years (P < 0.05, FWE corrected). As shown in the 3D render (A) and sagittal cross‐section (B), there was significant contraction in temporal stem white matter for more than 4 years. Additionally, as shown in the coronal sections (C), there was significant contraction in large portions of bilateral subcortical white matter and the cerebellum. The color bar represents _T_‐values.
Figure 3
Regions (A) where baseline FA from the splenium (green), entorhinal white matter (orange), and genu (blue) predict volume loss from baseline to follow‐up (P < 0.001, uncorrected). The statistical map is overlaid on coronal sections of the “CH2” template available in MRIcron (Rorden, 2007). The correlation between (B) baseline splenium FA and cerebellar hemisphere volume loss was r 2 = 0.25, P < 0.001 and (C) baseline genu FA and inferior temporal gyrus WM volume loss was r 2 = 0.33, P < 0.001. Data points represent individual participants. [Color figure can be viewed in the online issue, which is available at
.]
Similar articles
- Vascular burden and APOE ε4 are associated with white matter microstructural decline in cognitively normal older adults.
Williams OA, An Y, Beason-Held L, Huo Y, Ferrucci L, Landman BA, Resnick SM. Williams OA, et al. Neuroimage. 2019 Mar;188:572-583. doi: 10.1016/j.neuroimage.2018.12.009. Epub 2018 Dec 15. Neuroimage. 2019. PMID: 30557663 Free PMC article. - Evaluation of early cerebral metabolic, perfusion and microstructural changes in HCV-positive patients: a pilot study.
Bladowska J, Zimny A, Knysz B, Małyszczak K, Kołtowska A, Szewczyk P, Gąsiorowski J, Furdal M, Sąsiadek MJ. Bladowska J, et al. J Hepatol. 2013 Oct;59(4):651-7. doi: 10.1016/j.jhep.2013.05.008. Epub 2013 May 13. J Hepatol. 2013. PMID: 23680314 - White matter microstructure in late middle-age: Effects of apolipoprotein E4 and parental family history of Alzheimer's disease.
Adluru N, Destiche DJ, Lu SY, Doran ST, Birdsill AC, Melah KE, Okonkwo OC, Alexander AL, Dowling NM, Johnson SC, Sager MA, Bendlin BB. Adluru N, et al. Neuroimage Clin. 2014 Apr 21;4:730-42. doi: 10.1016/j.nicl.2014.04.008. eCollection 2014. Neuroimage Clin. 2014. PMID: 24936424 Free PMC article. - Grey and white matter abnormalities in temporal lobe epilepsy with and without mesial temporal sclerosis.
Scanlon C, Mueller SG, Cheong I, Hartig M, Weiner MW, Laxer KD. Scanlon C, et al. J Neurol. 2013 Sep;260(9):2320-9. doi: 10.1007/s00415-013-6974-3. Epub 2013 Jun 11. J Neurol. 2013. PMID: 23754695 Free PMC article. - Longitudinal study of callosal microstructure in the normal adult aging brain using quantitative DTI fiber tracking.
Sullivan EV, Rohlfing T, Pfefferbaum A. Sullivan EV, et al. Dev Neuropsychol. 2010;35(3):233-56. doi: 10.1080/87565641003689556. Dev Neuropsychol. 2010. PMID: 20446131 Free PMC article. Review.
Cited by
- Association of white matter microstructural integrity with cognition and dementia.
Power MC, Su D, Wu A, Reid RI, Jack CR, Knopman DS, Coresh J, Huang J, Kantarci K, Sharrett AR, Gottesman RG, Griswold ME, Mosley TH. Power MC, et al. Neurobiol Aging. 2019 Nov;83:63-72. doi: 10.1016/j.neurobiolaging.2019.08.021. Epub 2019 Aug 29. Neurobiol Aging. 2019. PMID: 31585368 Free PMC article. - FKBP5 genotype and structural integrity of the posterior cingulum.
Fani N, King TZ, Reiser E, Binder EB, Jovanovic T, Bradley B, Ressler KJ. Fani N, et al. Neuropsychopharmacology. 2014 Apr;39(5):1206-13. doi: 10.1038/npp.2013.322. Epub 2013 Nov 20. Neuropsychopharmacology. 2014. PMID: 24253961 Free PMC article. - Brain volumes and white matter diffusion across the adult lifespan in temporal lobe epilepsy.
Yasuda CL, Pimentel-Silva LR, Beltramini GC, Liu M, Machado de Campos B, Coan AC, Beaulieu C, Cendes F, Gross DW. Yasuda CL, et al. Ann Clin Transl Neurol. 2023 Jul;10(7):1106-1118. doi: 10.1002/acn3.51793. Epub 2023 May 19. Ann Clin Transl Neurol. 2023. PMID: 37208853 Free PMC article. - Microstructural white matter alterations in preclinical Alzheimer's disease detected using free water elimination diffusion tensor imaging.
Hoy AR, Ly M, Carlsson CM, Okonkwo OC, Zetterberg H, Blennow K, Sager MA, Asthana S, Johnson SC, Alexander AL, Bendlin BB. Hoy AR, et al. PLoS One. 2017 Mar 14;12(3):e0173982. doi: 10.1371/journal.pone.0173982. eCollection 2017. PLoS One. 2017. PMID: 28291839 Free PMC article. - Microstructural Changes of the Human Brain from Early to Mid-Adulthood.
Tian L, Ma L. Tian L, et al. Front Hum Neurosci. 2017 Aug 7;11:393. doi: 10.3389/fnhum.2017.00393. eCollection 2017. Front Hum Neurosci. 2017. PMID: 28824398 Free PMC article.
References
- Ardekani S, Kumar A, Bartzokis G, Sinha U (2007): Exploratory voxel‐based analysis of diffusion indices and hemispheric asymmetry in normal aging. Magn Reson Imaging 25:154–167. - PubMed
- Ashburner J, Friston KJ (2000): Voxel‐based morphometry—The methods. Neuroimage 11:805–821. - PubMed
- 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. - PubMed
- Bartzokis G, Beckson M, Lu PH, Nuechterlein KH, Edwards N, Mintz J (2001): Age‐related changes in frontal and temporal lobe volumes in men: A magnetic resonance imaging study. Arch Gen Psychiatry 58:461–465. - PubMed
Publication types
MeSH terms
Substances
Grants and funding
- UL1 TR000427/TR/NCATS NIH HHS/United States
- AG027161/AG/NIA NIH HHS/United States
- R01 AG027161/AG/NIA NIH HHS/United States
- R01 AG021155/AG/NIA NIH HHS/United States
- AG021155/AG/NIA NIH HHS/United States
- T32 AG000213/AG/NIA NIH HHS/United States
- P50 AG033514/AG/NIA NIH HHS/United States
- R01 AG037639/AG/NIA NIH HHS/United States
- P30 HD003352/HD/NICHD NIH HHS/United States
- I01 CX000165/CX/CSRD VA/United States
- T32 GM007507/GM/NIGMS NIH HHS/United States
LinkOut - more resources
Full Text Sources
Other Literature Sources