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Journal of Neurology

, Volume 262, Issue 1, pp 165–172 | Cite as

Tissue microstructural changes in dementia with Lewy bodies revealed by quantitative MRI

  • Li SuEmail author
  • Andrew M. Blamire
  • Rosie Watson
  • Jiabao He
  • Benjamin Aribisala
  • John T. O’Brien
Original Communication

Abstract

We aimed to characterize dementia with Lewy bodies (DLB) by the quantitative MRI parameters of longitudinal relaxation time (qT1) and transverse relaxation time (qT2). These parameters reflect potential pathological changes in tissue microstructures, which may be detectable noninvasively in brain areas without evident atrophy, so may have potential value in revealing the early neuropathological changes in DLB. We conducted a cross-sectional study of subjects with DLB (N = 35) and similarly aged control participants (N = 35). All subjects underwent a detailed clinical and neuropsychological assessment and structural and quantitative 3T MRI. Quantitative MRI maps were obtained using relaxation time mapping methods. Statistical analysis was performed on gray matter qT1 and qT2 values. We found significant alterations of quantitative parameters in DLB compared to controls. In particular, qT1 decreases in bilateral temporal lobes, right parietal lobes, basal ganglia including left putamen, left caudate nucleus and left amygdala, and left hippocampus/parahippocampus; qT2 decreases in left putamen and increases in left precuneus. These regions showed only partial overlap with areas where grey matter loss was found, making atrophy an unlikely explanation for our results. Our findings support that DLB is predominantly associated with changes in posterior regions, such as visual association areas, and subcortical structures, and that qT1 and qT2 measurement can detect subtle changes not seen on structural volumetric imaging. Hence, quantitative MRI may compliment other imaging techniques in detecting early changes in DLB and in understanding neurobiological changes associated with the disorder.

Keywords

Dementia Lewy body disease Quantitative MRI Neuroimaging VBQ 

Notes

Acknowledgments

We thank Nikolaus Weiskopf for insightful discussion on voxel-based quantification methods. The study was funded by the Sir Jules Thorn Charitable Trust (grant ref: 05/JTA) and was supported by the National Institute for Health Research (NIHR) Newcastle Biomedical Research Centre and the Biomedical Research Unit in Lewy Body Dementia based at Newcastle upon Tyne Hospitals National Health Service (NHS) Foundation Trust and Newcastle University and the NIHR Biomedical Research Centre and Biomedical Research Unit in Dementia based at Cambridge University Hospitals NHS Foundation Trust and the University of Cambridge. The views expressed are those of the authors and not necessarily those of the NHS, the NIHR or the Department of Health.

Conflicts of interest

L. Su, A. Blamire, R. Watson, J. He and B. Aribisala report no disclosures. J. O’Brien has been a consultant for GE Healthcare, Servier, and Bayer Healthcare and has received honoraria for talks from Pfizer, GE Healthcare, Eisai, Shire, Lundbeck, Lilly, and Novartis.

Ethical standard

This research was approved by NHS National Research Ethics Service, Newcastle & North Tyneside 1 Research Ethics Committee on the 11th September 2008 (No. 05/Q0905/217).

Supplementary material

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Supplementary material 1 (DOCX 27 kb)
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Supplementary material 2 (DOCX 1369 kb)
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Supplementary material 3 (DOCX 17 kb)

References

  1. 1.
    McKeith IG, Dickson DW, Lowe J et al (2005) Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 65:1863–1872CrossRefPubMedGoogle Scholar
  2. 2.
    Watson R, O’Brien JT, Barber R, Blamire AM (2012) Patterns of gray matter atrophy in dementia with Lewy bodies: a voxel-based morphometry study. Int Psychogeriatr 24:532–543CrossRefPubMedGoogle Scholar
  3. 3.
    Watson R, Blamire AM, Colloby SJ et al (2012) Characterizing dementia with Lewy bodies by means of diffusion tensor imaging. Neurology 79:906–914PubMedCentralCrossRefPubMedGoogle Scholar
  4. 4.
    Burton EJ et al (2002) Patterns of cerebral atrophy in dementia with Lewy bodies using voxel-based morphometry. NeuroImage 17:618–630CrossRefPubMedGoogle Scholar
  5. 5.
    Beyer MK, Larsen JP, Aarsland D (2007) Gray matter atrophy in Parkinson disease with dementia and dementia with Lewy bodies. Neurology 69:747–754CrossRefPubMedGoogle Scholar
  6. 6.
    Whitwell JL et al (2007) Focal atrophy in dementia with Lewy bodies on MRI: a distinct pattern from Alzheimer’s disease. Brain 130:708–719PubMedCentralCrossRefPubMedGoogle Scholar
  7. 7.
    Lippa CF, Johnson R, Smith TW (1998) The medial temporal lobe in dementia with Lewy bodies: a comparative study with Alzheimer’s disease. Ann Neurol 43:102–106CrossRefPubMedGoogle Scholar
  8. 8.
    Burton EJ et al (2009) 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 132:195–203CrossRefPubMedGoogle Scholar
  9. 9.
    Lobotesis K, Fenwick JD, Phipps A et al (2001) Occipital hypoperfusion on SPECT in dementia with Lewy bodies but not AD. Neurology 56:643–649CrossRefPubMedGoogle Scholar
  10. 10.
    Minoshima S, Foster NL, Petrie EC et al (2002) Neuroimaging in dementia with Lewy bodies: metabolism, neurochemistry, and morphology. J Geriatr Psychiatry Neurol 15:200–209CrossRefPubMedGoogle Scholar
  11. 11.
    Hanyu H, Shimizu S, Hirao K et al (2006) Differentiation of dementia with Lewy bodies from Alzheimer’s disease using mini-mental state examination and brain perfusion SPECT. J Neurol Sci 250:97–102CrossRefPubMedGoogle Scholar
  12. 12.
    Sanchez-Castaneda C, Rene R, Ramirez-Ruiz B et al (2010) Frontal and associative visual areas related to visual hallucinations in dementia with Lewy bodies and Parkinson’s disease with dementia. Mov Disord 25:615–622CrossRefPubMedGoogle Scholar
  13. 13.
    Piggott MA, Marshall EF, Thomas N et al (1999) Striatal dopaminergic markers in dementia with Lewy bodies, Alzheimer’s and Parkinson’s diseases: rostrocaudal distribution. Brain 122(Pt 8):1449–1468CrossRefPubMedGoogle Scholar
  14. 14.
    McKeith I, O’Brien J, Walker Z et al (2007) Sensitivity and specificity of dopamine transporter imaging with 123I-FP-CIT SPECT in dementia with Lewy bodies: a phase III, multicentre study. Lancet Neurol 6:305–313CrossRefPubMedGoogle Scholar
  15. 15.
    Cousins DA, Burton EJ, Burn D et al (2003) Atrophy of the putamen in dementia with Lewy bodies but not Alzheimer’s disease: an MRI study. Neurology 61:1191–1195CrossRefPubMedGoogle Scholar
  16. 16.
    Tofts P (2003) Quantitative MRI of the brain: measuring changes caused by disease. Wiley, New YorkCrossRefGoogle Scholar
  17. 17.
    Draganski B, Ashburner J, Hutton C et al (2011) Regional specificity of MRI contrast parameter changes in normal ageing revealed by voxel-based quantification (VBQ). NeuroImage 55:1423–1434PubMedCentralCrossRefPubMedGoogle Scholar
  18. 18.
    Spencer NG, Bridgesb LR, Elderfield K et al (2013) Quantitative evaluation of MRI and histological characteristics of the 5xFAD Alzheimer mouse brain. NeuroImage 76:108–115CrossRefPubMedGoogle Scholar
  19. 19.
    Folstein M, Folstein S, McHugh P (1975) “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198CrossRefPubMedGoogle Scholar
  20. 20.
    Fahn S, R Elton, Members of the UPDRS Development Committee (1987) Unified Parkinson’s Disease Rating Scale. In: Fahn S, Marsden C, Calne D, Goldstein M (eds) Recent developments in Parkinson’s disease. Macmillan Health Care Information, Florham Park, pp 153–164Google Scholar
  21. 21.
    Cummings JL, Mega M, Gray K et al (1994) The Neuropsychiatric Inventory: comprehensive assessment of psychopathology in dementia. Neurology 44:2308–2314CrossRefPubMedGoogle Scholar
  22. 22.
    Bucks RS, Ashworth DL, Wilcock GK, Siegfried K (1996) Assessment of activities of daily living in dementia: development of the bristol activities of daily living scale. Age Ageing 25:113–120CrossRefPubMedGoogle Scholar
  23. 23.
    Clare S, Jezzard P (2001) Rapid T-1 mapping using multislice echo planar imaging. Magn Reson Med 45:630–634CrossRefPubMedGoogle Scholar
  24. 24.
    Ashburner J (2007) A fast diffeomorphic image registration algorithm. NeuroImage 38:95–113CrossRefPubMedGoogle Scholar
  25. 25.
    Jenkinson M, Beckmann CF, Behrens TEJ et al (2012) FSL. NeuroImage 62(2):782–790CrossRefPubMedGoogle Scholar
  26. 26.
    Tzourio-Mazoyer N, Landeau B, Papathanassiou D et al (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15:273–289CrossRefPubMedGoogle Scholar
  27. 27.
    O’Brien JT, Colloby S, Fenwick J et al (2004) Dopamine transporter loss visualized with FP-CIT SPECT in the differential diagnosis of dementia with Lewy bodies. Arch Neurol 61:919–925CrossRefPubMedGoogle Scholar
  28. 28.
    Klein JC, Eggers C, Kalbe E et al (2010) Neurotransmitter changes in dementia with Lewy bodies and Parkinson disease dementia in vivo. Neurology 74:885–892CrossRefPubMedGoogle Scholar
  29. 29.
    Edison P, Rowe CC, Rinne JO et al (2008) Amyloid load in Parkinson’s disease dementia and Lewy body dementia measured with [11C]PIB positron emission tomography. J Neurol Neurosurg Psychiatry 79:1331–1338CrossRefPubMedGoogle Scholar
  30. 30.
    Shimada H, Hirano S, Shinotoh H et al (2009) Mapping of brain acetylcholinesterase alterations in Lewy body disease by PET. Neurology 73:273–278CrossRefPubMedGoogle Scholar
  31. 31.
    Kantarci K, Avula R, Senjem ML et al (2010) Dementia with Lewy bodies and Alzheimer disease: neurodegenerative patterns characterized by DTI. Neurology 74:1814–1821PubMedCentralCrossRefPubMedGoogle Scholar
  32. 32.
    Callaghan MF, Freund P, Anderson E et al (2014) Widespread age-related differences in the human brain microstructure revealed by quantitative magnetic resonance imaging. Neurobiol Aging. doi: 10.1016/j.neurobiolaging.2014.02.008 PubMedCentralPubMedGoogle Scholar
  33. 33.
    Bunzeck N, Eckart C, Singh-Curry V et al (2013) Motor phenotype and magnetic resonance measures of basal ganglia iron levels in Parkinson’s disease. Parkinsonism Relat Disord 19(12):1136–1142PubMedCentralCrossRefPubMedGoogle Scholar
  34. 34.
    Gelman N, Ewing JR, Gorell JM et al (2001) Interregional variation of longitudinal relaxation rates in human brain at 3.0T: relation to estimated iron and water contents. Magn Reson Med 45:71–79CrossRefPubMedGoogle Scholar
  35. 35.
    MacKay A, Whittall K, Adler J et al (1994) In vivo visualization of myelin water in brain by magnetic resonance. Magn Reson Med 31:673–677CrossRefPubMedGoogle Scholar
  36. 36.
    Lutti A, Dick F, Sereno MI et al (2014) Using high-resolution quantitative mapping of R1 as an index of cortical myelination. Neuroimage 93:176–188CrossRefPubMedGoogle Scholar
  37. 37.
    Fukunaga M, Li TQ, van Gelderen P et al (2010) Layer-specific variation of iron content in cerebral cortex as a source of MRI contrast. Proc Natl Acad Sci USA 107:3834–3839PubMedCentralCrossRefPubMedGoogle Scholar
  38. 38.
    Gelman N, Ewing JR, Gorell JM et al (2001) Interregional variation of longitudinal relaxation rates in human brain at 3.0T: relation to estimated iron and water contents. Magn Reson Med 45:71–79CrossRefPubMedGoogle Scholar
  39. 39.
    Aribisala BS, He J, Blamire AM (2011) Comparative study of standard space and real space analysis of quantitative MR brain data. J Magn Reson Imaging 33(6):1503–1509CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Li Su
    • 1
    Email author
  • Andrew M. Blamire
    • 2
  • Rosie Watson
    • 3
  • Jiabao He
    • 4
  • Benjamin Aribisala
    • 5
  • John T. O’Brien
    • 1
  1. 1.Department of Psychiatry, School of Clinical MedicineUniversity of CambridgeCambridgeUK
  2. 2.Institute of Cellular Medicine and Newcastle Magnetic Resonance CentreNewcastle UniversityNewcastle upon TyneUK
  3. 3.Aged Care DepartmentRoyal Melbourne HospitalParkvilleAustralia
  4. 4.The Institute of Medical SciencesUniversity of AberdeenAberdeenUK
  5. 5.Division of Clinical Neurosciences, Western General HospitalUniversity of EdinburghEdinburghUK

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