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Subcortical volume changes in dementia with Lewy bodies and Alzheimer's disease. A comparison with healthy aging

Published online by Cambridge University Press:  17 November 2015

Rosie Watson
Affiliation:
Institute of Neuroscience, Campus for Ageing and Vitality, Newcastle University, Newcastle upon Tyne, UK The Florey Institute of Neuroscience and Mental Health and the Department of Medicine, Royal Melbourne Hospital, the University of Melbourne, and the Department of Aged Care, Royal Melbourne Hospital, Parkville, Melbourne, Victoria, Australia
Sean J. Colloby*
Affiliation:
Institute of Neuroscience, Campus for Ageing and Vitality, Newcastle University, Newcastle upon Tyne, UK
Andrew M. Blamire
Affiliation:
Newcastle Magnetic Resonance Centre and Institute of Cellular Medicine, Newcastle University, Newcastle upon Tyne, UK
John T. O’Brien
Affiliation:
Institute of Neuroscience, Campus for Ageing and Vitality, Newcastle University, Newcastle upon Tyne, UK Department of Psychiatry, University of Cambridge, Cambridge, UK
*
Correspondence should be addressed to: Dr Sean J. Colloby, PhD, Institute of Neuroscience, Campus for Ageing and Vitality, Newcastle University, Newcastle upon Tyne NE4 5PL, UK. Phone: +44-191-208-1321; Fax: +44-191-208-1301. E-mail: sean.colloby@ncl.ac.uk.

Abstract

Background: Differentiating Alzheimer's disease (AD) and dementia with Lewy bodies (DLB), two of the commonest forms of dementia in older age, remains a diagnostic challenge. To assist with better understanding of the differences between the conditions during life, we assessed limbic and subcortical brain volumes in AD, DLB, and healthy older individuals using magnetic resonance imaging (MRI), with the hypothesis that when compared with controls, subcortical volumes would be reduced to a greater extent in DLB than in AD.

Methods: One hundred participants (35 healthy controls, 32 AD, and 33 DLB) underwent 3 Tesla T1 weighted MR scanning. Volumes were automatically segmented for each participant using FreeSurfer, then expressed as a percentage of their total intracranial volumes. Group effects were assessed using multivariate analysis of covariance, controlling for age and gender.

Results: Significant group effects were apparent among subcortical brain volumes (F28,162 = 4.8, p < 0.001; Wilk's Λ = 0.30, partial η2 = 0.45), while univariate tests showed differences in all volumetric measures (p < 0.03) except in right caudate (p = 0.08). Post-hoc analyses indicated that while not significantly different from AD, changes compared to healthy subjects in left caudate, bilateral putamen, left thalamus, brainstem and total subcortical grey volume were more pronounced in DLB. Significant differences between AD and DLB were confined to the bilateral hippocampus (DLB > AD, p < 0.008).

Conclusions: For similar levels of dementia severity, DLB appears to have greater involvement of subcortical brain atrophy than AD. Further investigation of the subcortical brain structures in DLB is warranted to fully understand their neurobiological role in this disease.

Type
Research Article
Copyright
Copyright © International Psychogeriatric Association 2015 

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References

Almeida, O. P., Burton, E. J., McKeith, I., Gholkar, A., Burn, D. and O’Brien, J. T. (2003). MRI study of caudate nucleus volume in Parkinson's disease with and without dementia with Lewy bodies and Alzheimer's disease. Dementia & Geriatric Cognitive Disorders, 16, 5763.CrossRefGoogle ScholarPubMed
Barber, R., Ballard, C., McKeith, I. G., Gholkar, A. and O’Brien, J. T. (2000). MRI volumetric study of dementia with Lewy bodies: a comparison with AD and vascular dementia. Neurology, 54, 13041309.CrossRefGoogle ScholarPubMed
Barber, R., McKeith, I., Ballard, C. and O’Brien, J. (2002). Volumetric MRI study of the caudate nucleus in patients with dementia with Lewy bodies, Alzheimer's disease, and vascular dementia. Journal of Neurology, Neurosurgery and Psychiatry, 72, 406407.CrossRefGoogle ScholarPubMed
Basso, M. A., Uhlrich, D. and Bickford, M. E. (2005). Cortical function: a view from the thalamus. Neuron, 45, 485488.CrossRefGoogle ScholarPubMed
Braak, H., Del Tredici, K., Rub, U., de Vos, R. A., Jansen Steur, E. N. and Braak, E. (2003). Staging of brain pathology related to sporadic Parkinson's disease. Neurobiology of Aging, 24, 197211.CrossRefGoogle ScholarPubMed
Burton, E. J., McKeith, I. G., Burn, D. J., Williams, E. D. and O’ Brien, J. T. (2004). Cerebral atrophy in Parkinson's disease with and without dementia: a comparison with Alzheimer's disease, dementia with Lewy bodies and controls. Brain, 127, 791800.CrossRefGoogle ScholarPubMed
Burton, E. J. et al. (2002). Patterns of cerebral atrophy in dementia with Lewy bodies using voxel-based morphometry. Neuroimage, 17, 618630.CrossRefGoogle ScholarPubMed
Chang, C. C., Liu, J. S., Chang, Y. Y., Chang, W. N., Chen, S. S. and Lee, C. H. (2008). (99 m) Tc-ethyl cysteinate dimer brain SPECT findings in early stage of dementia with Lewy bodies and Parkinson's disease patients: a correlation with neuropsychological tests. European Journal of Neurology, 15, 6165.CrossRefGoogle Scholar
Cho, H. et al. (2013). Changes in subcortical structures in early-versus late-onset Alzheimer's disease. Neurobiology of Aging, 34, 17401747.CrossRefGoogle ScholarPubMed
Cousins, D. A., Burton, E. J., Burn, D., Gholkar, A., McKeith, I. G. and O’Brien, J. T. (2003). Atrophy of the putamen in dementia with Lewy bodies but not Alzheimer's disease: an MRI study. Neurology, 61, 11911195.CrossRefGoogle Scholar
Dale, A. M., Fischl, B. and Sereno, M. I. (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage, 9, 179194.CrossRefGoogle ScholarPubMed
de Jong, L. W. et al. (2008). Strongly reduced volumes of putamen and thalamus in Alzheimer's disease: an MRI study. Brain, 131, 32773285.CrossRefGoogle ScholarPubMed
Fahn, S., Elton, R., Marsden, C. D. and Goldstein, M. (1987). Unified Parkinson's Disease Rating Scale. In Fahn, S., Marsden, C., Calne, D. and Goldstein, M. (eds.), Recent Development in Parkinson's Disease (pp. 153164). Florham Park, UK: Macmillan Health Care Information.Google Scholar
Fischl, B. and Dale, A. M. (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of National Academy of Sciences of USA, 97, 1105011055.CrossRefGoogle ScholarPubMed
Fischl, B., Sereno, M. I. and Dale, A. M. (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage, 9, 195207.CrossRefGoogle Scholar
Fischl, B. et al. (2002). Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron, 33, 341355.CrossRefGoogle Scholar
Folstein, M., Folstein, S. and McHugh, P. (1975). “Mini-mental state.” A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189198.CrossRefGoogle ScholarPubMed
Galasko, D. (2001). Lewy bodies and dementia. Current Neurology Neuroscience Reports, 1, 435441.CrossRefGoogle ScholarPubMed
Hanyu, H., Shimizu, S., Tanaka, Y., Hirao, K., Iwamoto, T. and Abe, K. (2007). MR features of the substantia innominata and therapeutic implications in dementias. Neurobiology of Aging, 28, 548554.CrossRefGoogle ScholarPubMed
Karas, G. B. et al. (2003). A comprehensive study of gray matter loss in patients with Alzheimer's disease using optimized voxel-based morphometry. Neuroimage, 18, 895907.CrossRefGoogle ScholarPubMed
Mak, E. et al. (2015a). Longitudinal assessment of global and regional atrophy rates in Alzheimer's disease and dementia with Lewy bodies. Neuroimage: Clinical, 7, 456462.CrossRefGoogle ScholarPubMed
Mak, E. et al. (2015b). Progressive cortical thinning and subcortical atrophy in dementia with Lewy bodies and Alzheimer's disease. Neurobiology of Aging, 36, 17431750.CrossRefGoogle ScholarPubMed
McKeith, I. G., Fairbairn, A. F., Perry, R. H. and Thompson, P. (1994). The clinical diagnosis and misdiagnosis of senile dementia of Lewy body type (SDLT). British Journal of Psychiatry, 165, 324332.CrossRefGoogle ScholarPubMed
McKeith, I. G. et al. (2005). Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology, 65, 18631872.CrossRefGoogle ScholarPubMed
McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D. and Stadlan, E. (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, 939944.CrossRefGoogle ScholarPubMed
Pedro, T. et al. (2012). Volumetric brain changes in thalamus, corpus callosum and medial temporal structures: mild Alzheimer's disease compared with amnestic mild cognitive impairment. Dementia and Geriatric Cognitive Disorders, 34, 149155.CrossRefGoogle ScholarPubMed
Piggott, M. A. et al. (1999). Striatal dopaminergic markers in dementia with Lewy bodies, Alzheimer's and Parkinson's diseases: rostrocaudal distribution. Brain, 122, 14491468.CrossRefGoogle ScholarPubMed
Roh, J. H. et al. (2011). Volume reduction in subcortical regions according to severity of Alzheimer's disease. Journal of Neurology, 258, 10131020.CrossRefGoogle ScholarPubMed
Sanchez-Benavides, G., Gomez-Anson, B., Sainz, A., Vives, Y., Delfino, M. and Pena-Casanova, J. (2010). Manual validation of FreeSurfer's automated hippocampal segmentation in normal aging, mild cognitive impairment, and Alzheimer Disease subjects. Psychiatry Research, 181, 219225.CrossRefGoogle ScholarPubMed
Seidel, K. et al. (2015). The brainstem pathologies of Parkinson's disease and dementia with Lewy bodies. Brain Pathology, 25, 121135.CrossRefGoogle ScholarPubMed
Shimizu, S., Hanyu, H., Hirao, K., Sato, T., Iwamoto, T. and Koizumi, K. (2008). Value of analyzing deep gray matter and occipital lobe perfusion to differentiate dementia with Lewy bodies from Alzheimer's disease. Annals of Nuclear Medicine, 22, 911916.CrossRefGoogle ScholarPubMed
Stepan-Buksakowska, I. et al. (2014). Cortical and subcortical atrophy in Alzheimer's disease: parallel atrophy of thalamus and hippocampus. Alzheimer's Diseaase and Associated Disorders, 28, 6572.CrossRefGoogle ScholarPubMed
Takahashi, R. et al. (2010). Measurement of gray and white matter atrophy in dementia with Lewy bodies using diffeomorphic anatomic registration through exponentiated lie algebra: a comparison with conventional voxel-based morphometry. American Journal of Neuroradiology (AJNR), 31, 18731878.CrossRefGoogle ScholarPubMed
Watson, R., O’Brien, J. T., Barber, R. and Blamire, A. M. (2012b). Patterns of gray matter atrophy in dementia with Lewy bodies: a voxel-based morphometry study. International Psychogeriatrics, 24, 532540.CrossRefGoogle ScholarPubMed
Watson, R. et al. (2012a). Characterizing dementia with Lewy bodies by means of diffusion tensor imaging. Neurology, 79, 906914.CrossRefGoogle ScholarPubMed
Whitwell, J. L. et al. (2007). Focal atrophy in dementia with Lewy bodies on MRI: a distinct pattern from Alzheimer's disease. Brain, 130, 708719.CrossRefGoogle ScholarPubMed
Zarei, M. et al. (2010). Combining shape and connectivity analysis: an MRI study of thalamic degeneration in Alzheimer's disease. Neuroimage, 49, 18.CrossRefGoogle ScholarPubMed