The use of diffusion-tensor imaging to assess microstructural integrity of white matter of patients with Alzheimer’s disease
https://doi.org/10.20862/0042-4676-2018-99-6-295-304
Abstract
Objective. To compare diffusion-tensor imaging (DTI) measures in different anatomic regions of the brain in patients with an isolated Alzheimer's disease (AD) and patients with AD and small-vessel disease (SVD).
Material and methods. 20 AD patients, aged 66 (±10), of whom 11 AD patients had an isolated neurodegenerative process and 9 patients, who were diagnosed with AD+SVD, were examined. A research was made on a 3 T Siemens Magnetom Skyra MR-scanner. All participants underwent the same imaging protocol, which included standard clinical- and diffusion tensor pulse sequences. With an MR-image processing software package Olea Medical Sphere 3.0, fractional anisotropy (FA), mean diffusivity (MD), axial and radial diffusivity (AxD and RxD) were measured in different brain regions.
Results. Significant differences in DTI measures (FA, MD, AxD, RxD), indicating more severe white matter microstructural damage in AD+SVD patients, compared with patients with an isolated AD, were observed in middle thalamic radiation, upper and lower longitudinal bundles, posterior part of cingulate gyrus and genu of corpus callosum.
Conclusion. DTI is an informative method, highly sensitive in detecting difference in white matter microstructural integrity of brain tissue in individuals with an isolated AD and patients with AD+SVD.
Keywords
About the Authors
V. A. PerepelovRussian Federation
Vsevolod A. Perepelov - Radiologist of A.Ya. Kozhevnikov Clinic of Nervous System Diseases.
Ul. Trubetskaya, 8, stroenie 2, Moscow, 119991
V. I. Solodovnikov
Russian Federation
Cand. Tech. Sc., Senior Researcher.
Ul. Marshala Biryuzova, 7a, Odintsovo,143000
V. E. Sinitsyn
Russian Federation
Dr. Med. Sc., Professor, Chief of Chair of Radiology and Radiotherapy, Lomonosov Moscow State University.
Lomonosovskiy prospect, 27, korpus 1, Moscow, 119992; ul. Barrikadnaya, 2/1, Moscow, 125993
E. M. Perepelova
Russian Federation
Cand. Med. Sc., Head of Department of Radiology of the University Pediatric Clinic.
Ul. Trubetskaya, 8, stroenie 2, Moscow, 119991
N. N. Koberskaya
Russian Federation
Cand. Med. Sc., Assistant of Chair of Nervous Diseases and Neurosurgery.
Ul. Trubetskaya, 8, stroenie 2, Moscow, 119991
V. N. Gridin
Russian Federation
Dr. Tech. Sc., Professor, Scientific Adviser.
Ul. Marshala Biryuzova, 7a, Odintsovo,143000
N. N. Yakhno
Russian Federation
Dr. Med. Sc., Professor of Chair of Nervous Diseases and Neurosurgery, Academician of the Russian Academy of Sciences, Head of Neurology Department of Biomedicine Technopark.
Ul. Trubetskaya, 8, stroenie 2, Moscow, 119991
References
1. Yakhno N.N., Zakharov V.V., Lokshina A.B., Koberskaya N.N., Mkhitaryan E.A. Dementia. Guide for doctors. 3rd ed. Moscow: MEDPress-Inform; 2011 (in Russ.).
2. Jellinger K.A. Prevalence and impact of cerebrovascular lesions in Alzheimer and Lewy body diseases. Neuro-degener. Dis. 2010; 7: 112-5. DOI: 10.1159/000285518
3. Toledo J.B., Arnold S.E., Raible K., Brettschneider J., Xie S.X., Grossman M. et al. Contribution of cerebrovascular disease in autopsy confirmed neurodegenerative disease cases in the National Alzheimer’s Coordinating Centre. Brain. 2013; 136: 2697-706. DOI: 10.1093/brain/awt188
4. Risacher S.L., Shen L., West J.D., Kim S., McDonald B.C., Beckett L.A. et al. Longitudinal MRI atrophy biomarkers: relationship to conversion in the ADNI cohort. Neurobiol. Aging. 2010; 31 (8): 1401-18. DOI: 10.1016/j.neurobiolaging.2010.04.029
5. Desikan R.S., Cabral H.J., Fischl B., Guttmann C.R., Blacker D., Hyman B.T. et al. Temporoparietal MR imaging measures of atrophy in subjects with mild cognitive impairment that predict subsequent diagnosis of Alzheimer disease. Am. J. Neuroradiol. 2009; 30 (3): 532-8. DOI: 10.3174/ajnr.A1397
6. Sabuncu M.R., Desikan R.S., Sepulcre J., Yeo B.T., Liu H., Schmansky N.J. et al. The dynamics of cortical and hippocampal atrophy in Alzheimer disease. Alzheimer's Disease Neuroimaging Initiative. Arch. Neurol. 2011; 68 (8): 1040-8. DOI: 10.1001/archneurol.2011.167
7. Braak H., Braak E. Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiol Aging. 1995; 16 (3): 271-8; discussion 278-84. DOI: 10.1001/archneurol.2011.167
8. Brun A., Englund E. A white matter disorder in dementia of the Alzheimer type: a pathoanatomical study. Ann. Neurol. 1986; 19: 253-62. DOI: 10.1002/ana.410190306
9. Canu E., Agosta F, Spinelli E.G., Magnani G., Marcone A., Scola E. et al. White matter microstructural damage in Alzheimer’s disease at different ages of onset. Neurobiol. Aging. 2013; 34: 2331-40. DOI: 10.1016/j.neurobiolaging.2013.03.026
10. Weiner M.W., Veitch D.P., Aisen P.S., Beckett L.A., Cairns N.J., Green R.C. et al. The Alzheimer’s Disease Neuroimaging Initiative: a review of papers published since its inception. Review article. Alzheimer’s & Dementia. 2012; 8: 1-68. DOI: 10.1016/j.jalz.2014.11.001
11. Bozzali M., Falini A., Franceschi M., Cercignani M., Zuffi M., Scotti G. et al. White matter damage in Alzheimer's disease assessed in vivo using diffusion tensor magnetic resonance imaging. J. Neurol. Neuro-surg. Psychiatry. 2002; 72 (6): 742-6. DOI: 10.1136/jnnp.72.6.742
12. Mielke M.M., Kozauer N.A., Chan K.C., George M., Toroney J., Zerrate M. et al. Regionally-specif-ic diffusion tensor imaging in mild cognitive impairment and Alzheimer's disease. Neuroimage. 2009; 46 (1): 47-55. DOI: 10.1016/j.neuroimage.2009.01.054
13. Alves G.S., Sudo F.K., de Oliveira Alves C.E., Ericeira-Valente L., Madeira Moreira D., Engelhardt E. et al. Diffusion tensor imaging studies in vascular disease: a review of the literature. Dement. Neuropsychol. 2012; 6 (3): 158-63. DOI: 10.1590/S1980-57642012DN06030008
14. Grinberg L.T., Thal D.R. Vascular pathology in the aged human brain. Acta Neuropathol. 2010; 119: 277-90. DOI: 10.1007/s00401-010-0652-7
15. Radue E.W., Weigel M., Wiest R., Urbach H. Introduction to magnetic resonance imaging for neurologists. Neuroimaging. 2016; 22 (5): 1379-98. DOI: 10.1212/CON.0000000000000391
16. Jellison B.J., Field A.S., Medow J., Lazar М., Shariar M.S., Andrew L.A. Diffusion tensor imaging of cerebral white matter: a pictorial review of physics, fiber tract anatomy, and tumor imaging patterns. Am. J. Neuroradiol. 2004; 25 (3): 356-69.
17. Pronin I.N., Fadeeva L.M., Zakharova N.E., Dolgushin M.B., Podo-prigora A.E., Kornienko V.N. Diffusion-tensor magnetic-resonance imaging and tractography. Annaly Klinicheskoy i Eksperimental’noy Nevrologii (Annals of Clinical and Experimental Neurology). 2008; 2 (1): 36-40 (in Russ.).
18. Kitaev S.V., Popova T.A. Principles of diffusion tensor visualization and its application in neurology. Annaly Klinicheskoy i Eksperimental’noy Nevrologii (Annals of Clinical and Experimental Neurology). 2012; 6 (1): 48-54 (in Russ.).
19. Nir T.M., Jahanshad N., Villalon-Reina J.E., Toga A.W., Jack C.R., Weiner M.W. et al. Effectiveness of regional DTI measures in distinguishing Alzheimer's disease, MCI, and normal aging. Neuroimage Clin. 2013; 3: 180-95. DOI: 10.1016/j.nicl.2013.07.006
20. Soares J.M., Marques P, Alves V., Sousa N. A hitchhiker's guide to diffusion tensor imaging. Front Neurosci. 2013; 7: 31. DOI: 10.3389/fnins.2013.00031
21. Alexander A.L., Hasan K., Kin-dlmann G., Parker D.L., Tsuru-da J.S. A geometric comparison of diffusion anisotropy measures. Magn. Reson. Med. 2000; 44: 283-91.
22. Snook L., Plewes C., Beaulieu C. Voxel based versus region of interest analysis in diffusion tensor imaging of neurodevelopment. Neuroimage. 2007; 34 (1): 243-52. DOI: 10.1016/j.neuroimage.2006.07.021
23. Srivastava S., Bhatia M.S., Bhar-gava S.K., Kumari R., Chandra S. A diffusion tensor imaging study using a voxel-based analysis, region-of-interest method to analyze white matter abnormalities in first-episode, treatment-naive major depressive disorder. J. Neuropsychiatry Clin. Neurosci. 2016; 28 (2): 131-7. DOI: 10.1176/appi.neu-ropsych.15050120
24. Oishi K., Faria A.V., van Zijl P. C. M., Mori S. MRI atlas of human white matter. 2nd ed. Baltimore: Academic Press; 2010.
25. Frisoni G.B., Pievani M., Testa C., Sabattoli F, Bresciani L., Bonet-ti M. et al. The topography of grey matter involvement in early and late onset Alzheimer’s disease. Brain. 2007; 3 (130): 720-30. DOI: 10.1093/brain/awl377
26. Moller C., Vrenken H., Jiskoot L., Versteeg A., Barkhof F., Scheltens P et al. Different patterns of gray matter atrophy in early- and late-onset Alzheimer’s disease. Neuro-biol. Aging. 2013; 8: 2014-22. DOI: 10.1016/j.neurobiolaging.2013.02.013
27. Mungas D., Jagust W.J., Reed B.R., Kramer J.H., Weiner M.W., Schuff N. et al. MRI predictors of cognition in subcortical ischemic vascular disease and Alzheimer’s disease. Neurology. 2001; 57: 2229-35.
28. Deramecourt V., Slade J.Y., Oakley A.E., Perry R.H., Ince PG., Maurage C.A. et al. Staging and natural history of cerebrovascular pathology in dementia. Neurology. 2012; 78 (14): 1043-50. DOI: 10.1212/WNL.0b013e31824e8e7f
29. Kim Y.J., Kwon H.K., Lee J.M., Kim Y.J., Kim H.J., Jung N.Y. et al. White matter microstructural changes in pure Alzheimer’s disease and subcortical vascular dementia. Eur. J. Neurol. 2015; 22 (4): 709-16. DOI: 10.1111/ene.12645
30. Fu J.-L., Zhang T., Chang Ch., Zhang Y.-Z., Li W.-B. The value of diffusion tensor imaging in the differential diagnosis of subcortical ischemic vascular dementia and Alzheimer’s disease in patients with only mild white matter alterations on T2-weighted images. Acta Radiologica. 2012; 53: 312-7. DOI: 10.1258/ar.2011.110272
31. DeCarli C., Mungas D., Harvey D., Reed B., Weiner M., Chui H. et al. Memory impairment, but not cerebrovascular disease, predicts progression of MCI to dementia. Neurology. 2004; 63 (2): 220-7.
32. Smith E.E., Egorova S., Blacker D., Killiany R.J., Muzikansky A., Dickerson B.C. et al. Magnetic resonance imaging white matter hyperintensities and brain volume in the prediction of mild cognitive impairment and dementia cognitive impairment and dementia. Arch. Neurol. 2008; 65 (1): 94-100. DOI: 10.1001/archneurol.2007.23
33. Song S.K., Sun S.W., Ju W.K., Lin S.J., Cross A.H., Neufeld A.H. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage. 2003; 20: 1714-22.
34. Sun S.W., Liang H.F., Trinkaus K., Cross A.H., Armstrong R.C., Song S.K. Noninvasive detection of cuprizone induced axonal damage and demyelination in the mouse corpus callosum. Magn. Reson. Med. 2006; 55: 302-8. DOI: 10.1002/mrm.20774
35. Kraus M.F., Susmaras T., Caugh-lin B.P, Walker C.J., Sweeney J.A., Little D.M. White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain. 2007; 130: 2508-19. DOI: 10.1093/brain/awm216
36. Counsell S.J., Shen Y., Board-man J.P, Larkman D.J., Kapellou O., Ward P. et al. Axial and radial diffu-sivity in preterm infants who have diffuse white matter changes on magnetic resonance imaging at term-equivalent age. Pediatrics. 2006; 117: 376-86. DOI: 10.1542/peds.2005-0820
37. Vernooij M.W., de Groot M., van der Lugt A., Ikram M.A., Krestin G.P, Hofman A. et al. White matter atrophy and lesion formation explain the loss of structural integrity of white matter in aging. Neuroimage. 2008; 43 (3): 470-7. DOI: 10.1016/j.neuroimage.2008.07.052
Review
For citations:
Perepelov V.A., Solodovnikov V.I., Sinitsyn V.E., Perepelova E.M., Koberskaya N.N., Gridin V.N., Yakhno N.N. The use of diffusion-tensor imaging to assess microstructural integrity of white matter of patients with Alzheimer’s disease. Journal of radiology and nuclear medicine. 2018;99(6):295-304. (In Russ.) https://doi.org/10.20862/0042-4676-2018-99-6-295-304