Hostname: page-component-848d4c4894-pjpqr Total loading time: 0 Render date: 2024-06-19T23:49:40.544Z Has data issue: false hasContentIssue false

Patterns of brain atrophy on magnetic resonance imaging and the boundary between ageing and Alzheimer's disease

Published online by Cambridge University Press:  17 February 2010

Mike O'Sullivan*
Affiliation:
Cardiff University Brain Research and Imaging Centre (CUBRIC), Schools of Psychology and Medicine, Cardiff University, UK
*
Address for correspondence: Dr Mike O'Sullivan, School of Psychology, Tower Building, Park Place, Cardiff CF10 3AT. Email: OsullivanM4@cardiff.ac.uk

Summary

Clinicians are increasingly faced with the problem of interpreting subtle, early cognitive symptoms. Enhanced awareness of Alzheimer's disease (AD) and available treatments has led to a growing demand for early assessment. Although it is known that a proportion of individuals with mild cognitive impairment will progress to dementia in following years, our ability to identify these individuals and predict individual cognitive trajectories is limited. The emergence of disease-modifying treatments would make these problems more acute. In this review, the potential role of magnetic resonance imaging (MRI) in aiding the clinician in early diagnosis of AD will be considered. The changes in grey matter structure that accompany ‘normal’ ageing will be described briefly, before moving on to studies that have attempted to distinguish the onset of disease from this background of structural change. Volumetric methods range from measurements of single key structures, such as the hippocampus, to methods based on computational neuroanatomy, which evaluate subtle structural alterations across the whole brain simultaneously. Computational methods are rapidly evolving and already perform as well as radiologists in distinguishing AD from normal ageing at an individual level. This article aims to provide a practical knowledge of how and why these methods work, point out the main advantages and disadvantages and sketch out outstanding issues and possible future directions.

Type
Neuropsychiatry of old age
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1Knopman, DS, DeKosky, ST, Cummings, JL et al. Practice parameter: diagnosis of dementia (an evidence-based review). Report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 2001; 56: 1143–53.CrossRefGoogle Scholar
2Waldemar, G, Dubois, B, Emre, M et al. Recommendations for the diagnosis and management of Alzheimer's disease and other disorders associated with dementia: EFNS guideline. Eur J Neurol 2007; 14: e126.CrossRefGoogle ScholarPubMed
3Scheltens, P, Korf, ES. Contribution of neuroimaging in the diagnosis of Alzheimer's disease and other dementias. Curr Opin Neurol 2000; 13: 391–96.CrossRefGoogle ScholarPubMed
4Dubois, B, Feldman, HH, Jacova, C et al. Research criteria for the diagnosis of Alzheimer's disease: revising the NINCDS-ADRDA criteria. Lancet Neurol 2007; 6: 734–46.CrossRefGoogle ScholarPubMed
5Fox, NC, Schott, JM. Imaging cerebral atrophy: normal ageing to Alzheimer's disease. Lancet 2004; 363: 392–94.CrossRefGoogle ScholarPubMed
6Mueller, SG, Weiner, MW, Thal, LJ et al. The Alzheimer's disease neuroimaging initiative. Neuroimaging Clin N Am 2005; 15: 869–77.CrossRefGoogle ScholarPubMed
7Braak, H, Braak, E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol (Berl) 1991; 82: 239–59.CrossRefGoogle ScholarPubMed
8Walhovd, KB, Westlye, LT, Amlien, I et al. Consistent neuroanatomical age-related volume differences across multiple samples. Neurobiol Aging 2009; Epub: 29 June.Google Scholar
9Good, CD, Johnsrude, IS, Ashburner, J, Henson, RN, Friston, KJ, Frackowiak, RS. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 2001; 14: 2136.CrossRefGoogle ScholarPubMed
10Walhovd, KB, Fjell, AM, Reinvang, I et al. Effects of age on volumes of cortex, white matter and subcortical structures. Neurobiol Aging 2005; 26: 1261–70.CrossRefGoogle ScholarPubMed
11Lupien, SJ, Evans, A, Lord, C et al. Hippocampal volume is as variable in young as in older adults: implications for the notion of hippocampal atrophy in humans. Neuroimage 2007; 34: 479–85.CrossRefGoogle Scholar
12De Leeuw, FE, de Groot, JC, Achten, E et al. Prevalence of cerebral white matter lesions in elderly people: a population based magnetic resonance imaging study. The Rotterdam Scan Study. J Neurol Neurosurg Psychiatry 2001; 70: 914.CrossRefGoogle Scholar
13Espeseth, T, Westlye, LT, Fjell, AM, Walhovd, KB, Rootwelt, H, Reinvang, I. Accelerated age-related cortical thinning in healthy carriers of apolipoprotein E epsilon 4. Neurobiol Aging 2008; 29: 329–40.CrossRefGoogle ScholarPubMed
14Raz, N, Gunning-Dixon, F, Head, D, Rodrigue, KM, Williamson, A, Acker, JD. Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional differences in volume. Neurobiol Aging 2004; 25: 377–96.CrossRefGoogle ScholarPubMed
15De Leeuw, FE, Barkhof, F, Scheltens, P. White matter lesions and hippocampal atrophy in Alzheimer's disease. Neurology 2004; 62: 310–12.CrossRefGoogle ScholarPubMed
16Raz, N, Lindenberger, U, Rodrigue, KM et al. Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex 2005; 15: 1676–89.CrossRefGoogle ScholarPubMed
17Likeman, M, Anderson, VM, Stevens, JM et al. Visual assessment of atrophy on magnetic resonance imaging in the diagnosis of pathologically confirmed young-onset dementias. Arch Neurol 2005; 62: 1410–15.CrossRefGoogle ScholarPubMed
18Kloppel, S, Stonnington, CM, Barnes, J et al. Accuracy of dementia diagnosis: a direct comparison between radiologists and a computerized method. Brain 2008; 131: 2969–74.CrossRefGoogle Scholar
19Jack, CR Jr, Petersen, RC, O'Brien, PC, Tangalos, EG. MR-based hippocampal volumetry in the diagnosis of Alzheimer's disease. Neurology 1992; 42: 183–88.CrossRefGoogle ScholarPubMed
20Pruessner, JC, Li, LM, Serles, W et al. Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: minimizing the discrepancies between laboratories. Cereb Cortex 2000; 10: 433–42.CrossRefGoogle ScholarPubMed
21Zarow, C, Vinters, HV, Ellis, WG et al. Correlates of hippocampal neuron number in Alzheimer's disease and ischemic vascular dementia. Ann Neurol 2005; 57: 896903.CrossRefGoogle ScholarPubMed
22Csernansky, JG, Hamstra, J, Wang, L et al. Correlations between antemortem hippocampal volume and postmortem neuropathology in AD subjects. Alzheimer Dis Assoc Disord 2004; 18: 190–95.Google ScholarPubMed
23Schott, JM, Fox, NC, Frost, C et al. Assessing the onset of structural change in familial Alzheimer's disease. Ann Neurol 2003; 53: 181–88.CrossRefGoogle ScholarPubMed
24Jack, CR Jr, Petersen, RC, Xu, YC et al. Medial temporal atrophy on MRI in normal aging and very mild Alzheimer's disease. Neurology 1997; 49: 786–94.CrossRefGoogle ScholarPubMed
25Jack, CR Jr, Petersen, RC, Xu, YC et al. Prediction of AD with MRI-based hippocampal volume in mild cognitive impairment. Neurology 1999; 52: 1397–403.CrossRefGoogle ScholarPubMed
26Gerardin, E, Chetelat, G, Chupin, M et al. Multidimensional classification of hippocampal shape features discriminates Alzheimer's disease and mild cognitive impairment from normal aging. Neuroimage 2009; 47: 1476–86.CrossRefGoogle ScholarPubMed
27Visser, PJ, Scheltens, P, Verhey, FR et al. Medial temporal lobe atrophy and memory dysfunction as predictors for dementia in subjects with mild cognitive impairment. J Neurol 1999; 246: 477–85.CrossRefGoogle ScholarPubMed
28Colliot, O, Chetelat, G, Chupin, M et al. Discrimination between Alzheimer disease, mild cognitive impairment, and normal aging by using automated segmentation of the hippocampus. Radiology 2008; 248: 194201.CrossRefGoogle ScholarPubMed
29Frisoni, GB, Laakso, MP, Beltramello, A et al. Hippocampal and entorhinal cortex atrophy in frontotemporal dementia and Alzheimer's disease. Neurology 1999; 52: 91100.CrossRefGoogle ScholarPubMed
30Tierney, MC, Fisher, RH, Lewis, AJ et al. The NINCDS-ADRDA Work Group criteria for the clinical diagnosis of probable Alzheimer's disease: a clinicopathologic study of 57 cases. Neurology 1988; 38: 359–64.CrossRefGoogle ScholarPubMed
31Wahlund, LO, Almkvist, O, Blennow, K et al. Evidence-based evaluation of magnetic resonance imaging as a diagnostic tool in dementia workup. Top Magn Reson Imaging 2005; 16: 427–37.CrossRefGoogle ScholarPubMed
32Chetelat, G, Landeau, B, Eustache, F et al. Using voxel-based morphometry to map the structural changes associated with rapid conversion in MCI: a longitudinal MRI study. Neuroimage 2005; 27: 934–46.CrossRefGoogle ScholarPubMed
33Frisoni, GB, Pievani, M, Testa, C et al. The topography of grey matter involvement in early and late onset Alzheimer's disease. Brain 2007; 130: 720–30.CrossRefGoogle ScholarPubMed
34Baron, JC, Chetelat, G, Desgranges, B et al. In vivo mapping of gray matter loss with voxel-based morphometry in mild Alzheimer's disease. Neuroimage 2001; 14: 298309.CrossRefGoogle ScholarPubMed
35Davatzikos, C, Xu, F, An, Y, Fan, Y, Resnick, SM. Longitudinal progression of Alzheimer's-like patterns of atrophy in normal older adults: the SPARE-AD index. Brain 2009; 132: 2026–35.CrossRefGoogle ScholarPubMed
36Driscoll, I, Davatzikos, C, An, Y et al. Longitudinal pattern of regional brain volume change differentiates normal aging from MCI. Neurology 2009; 72: 1906–13.CrossRefGoogle ScholarPubMed
37Whitwell, JL, Shiung, MM, Przybelski, SA et al. MRI patterns of atrophy associated with progression to AD in amnestic mild cognitive impairment. Neurology 2008; 70: 512–20.CrossRefGoogle ScholarPubMed
38Whitwell, JL, Przybelski, SA, Weigand, SD et al. 3D maps from multiple MRI illustrate changing atrophy patterns as subjects progress from mild cognitive impairment to Alzheimer's disease. Brain 2007; 130: 1777–86.CrossRefGoogle ScholarPubMed
39Ashburner, J, Csernansky, JG, Davatzikos, C, Fox, NC, Frisoni, GB, Thompson, PM. Computer-assisted imaging to assess brain structure in healthy and diseased brains. Lancet Neurol 2003; 2: 7988.CrossRefGoogle ScholarPubMed
40Kloppel, S, Stonnington, CM, Chu, C et al. Automatic classification of MR scans in Alzheimer's disease. Brain 2008; 131: 681–89.CrossRefGoogle ScholarPubMed
41Davatzikos, C, Fan, Y, Wu, X, Shen, D, Resnick, SM. Detection of prodromal Alzheimer's disease via pattern classification of magnetic resonance imaging. Neurobiol Aging 2008; 29: 514–23.CrossRefGoogle ScholarPubMed
42Fan, Y, Batmanghelich, N, Clark, CM, Davatzikos, C. Spatial patterns of brain atrophy in MCI patients, identified via high-dimensional pattern classification, predict subsequent cognitive decline. Neuroimage 2008; 39: 1731–43.CrossRefGoogle ScholarPubMed
43Misra, C, Fan, Y, Davatzikos, C. Baseline and longitudinal patterns of brain atrophy in MCI patients, and their use in prediction of short-term conversion to AD: results from ADNI. Neuroimage 2009; 44: 1415–22.CrossRefGoogle ScholarPubMed
44Burton, EJ, Barber, R, Mukaetova-Ladinska, EB et al. Medial temporal lobe atrophy on MRI differentiates Alzheimer's disease from dementia with Lewy bodies and vascular cognitive impairment: a prospective study with pathological verification of diagnosis. Brain 2009; 132: 195203.CrossRefGoogle ScholarPubMed
45Scher, AI, Xu, Y, Korf, ES et al. Hippocampal shape analysis in Alzheimer's disease: a population-based study. Neuroimage 2007; 36: 818.CrossRefGoogle ScholarPubMed
46Van Der, ZJ, Sleegers, K, Van, BC. Invited article: the Alzheimer disease-frontotemporal lobar degeneration spectrum. Neurology 2008; 71: 1191–97.CrossRefGoogle Scholar
47Alladi, S, Xuereb, J, Bak, T et al. Focal cortical presentations of Alzheimer's disease. Brain 2007; 130: 2636–45.CrossRefGoogle ScholarPubMed
48Josephs, KA, Duffy, JR, Strand, EA et al. Clinicopathological and imaging correlates of progressive aphasia and apraxia of speech. Brain 2006; 129: 1385–98.CrossRefGoogle ScholarPubMed
49Rohrer, JD, Crutch, SJ, Warrington, EK, Warren, JD. Progranulin-associated primary progressive aphasia: A distinct phenotype? Neuropsychologia 2009; Epub: Sept 18.CrossRefGoogle Scholar
50Jack, CR Jr, Lowe, VJ, Weigand, SD et al. Serial PIB and MRI in normal, mild cognitive impairment and Alzheimer's disease: implications for sequence of pathological events in Alzheimer's disease. Brain 2009; 132: 1355–65.CrossRefGoogle ScholarPubMed
51O'Sullivan, M, Jones, DK, Summers, PE, Morris, RG, Williams, SC, Markus, HS. Evidence for cortical ‘disconnection’ as a mechanism of age-related cognitive decline. Neurology 2001; 57: 632–38.CrossRefGoogle ScholarPubMed
52Johansen-Berg, H, Behrens, TE. Just pretty pictures? What diffusion tractography can add in clinical neuroscience. Curr Opin Neurol 2006; 19: 379–85.CrossRefGoogle ScholarPubMed
53O'Sullivan, M, Summers, PE, Jones, DK, Jarosz, JM, Williams, SC, Markus, HS. Normal-appearing white matter in ischemic leukoaraiosis: a diffusion tensor MRI study. Neurology 2001; 57: 2307–10.CrossRefGoogle ScholarPubMed