Diffusion tensor imaging studies in vascular disease: a review of the literature

Alves, Gilberto Sousa; Sudo, Felipe Kenji; Alves, Carlos Eduardo de Oliveira; Ericeira-Valente, Letice; Moreira, Denise Madeira; Engelhardt, Eliasz; Laks, Jerson

doi:10.1590/S1980-57642012DN06030008

ABSTRACT

Cerebrovascular disease (CVD) is often present in old age and may be associated with microstructural pathology of white matter (WM) and cognitive dysfunction. The current review investigated the relationship between CVD, cognitive status and WM integrity as assessed by diffusion tensor imaging (DTI).

Methods:

DTI studies were searched on ISI and Pubmed databases from 2002 to 2012.

Results:

Studies evidenced DTI changes in WM as associated with vascular disease and provide increasing support for DTI as a valuable method for early detection of CVD.

Conclusion:

DTI parameters can serve as important biomarkers in monitoring vascular disease progression and treatment response and may represent a surrogate marker of WM tract integrit.

Key words:
diffusion tensor; DTI; neuroimaging; vascular disease; white matter; cognition; vascular cognitive impairment

RESUMO

A doença cérebro-vascular (DCV) está frequentemente presente na idade avançada, podendo se associar à patologia microscópica da substância branca (SB) e à disfunção cognitiva. A presente revisão investiga a relação entre DCV, status cognitivo e a integridade da SB, através da avaliação pelo tensor de difusão (DTI).

Métodos:

Os estudos em DTI foram selecionados a partir das bases ISI e Pubmed entre 2002 e 2012.

Resultados:

Os estudos evidenciaram alterações do DTI na SB associadas à doença vascular e fornecem evidencia importante para o DTI como um método valioso para a detecção precoce da DCV.

Conclusão:

Os parâmetros do DTI podem servir como importantes biomarcadores na monitoração da doença vascular quanto a sua progressão e resposta terapêutica e parecem representar um marcador substituto da integridade da SB.

Palavras-chave:
tensor de difusão; DTI; neuroimagem; doença vascular; substância branca; cognição; prejuízo cognitivo vascular

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REFERENCES

DeCarli C, Fletcher E, Ramey V, Harvey D, Jagust WJ. Anatomical Mapping of White Matter Hyperintensities (WMH) Exploring the Relationships Between Periventricular WMH, Deep WMH, and Total WMH Burden. Stroke 2005;36:50-55.
Hardiman O, Doherty CP (editors) Neurodegenerative Disorders: A Clinical Guide, Springer; 2011.
Inzitari D, Pracucci G, Poggesi A, et al. Changes in white matter as determinant of global functional decline in older independent outpatients: three year follow-up of LADIS (leukoaraiosis and disability) study cohort. BMJ 2009;339: b2477.
Le Bihan D, Mangin JF, Poupon C, et al.Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 2001;13: 534-546.
Damoiseaux JS, Smith SM, Witter MP, et al. White matter tract integrity in aging and Alzheimer's disease. Hum Brain Mapp 2009;30:1051-1059.
Bosch B, Arenaza-Urquijo EM, Rami L, et al. (Multiple DTI index analysis in normal aging, amnestic MCI and AD. Relationship with neuropsychological performance. Neurobiol Aging 2012;33:61-74.
Basser PJ, Mattiello J, LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 1994;103: 247-254.
Pierpaoli C, Basser PJ. .Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 1996;36:893-906.
Alexopoulos GS, Kiosses DN, Choi SJ, Murphy CF, Lim KO. Frontal White Matter Microstructure and Treatment Response of Late-Life Depression: A Preliminary Study. Am J Psychiatry 2002;159:1929-1932.
Nobuhara K, Okugawa G, Sugimoto T, et al. Frontal white matter anisotropy and symptom severity of late-life depression: a magnetic resonance diffusion tensor imaging study. J Neurol Neurosurg Psychiatry 2006;77:120-122.
Taylor WD, MacFall JR, Payne ME, et al. (Late-life depression and microstructural abnormalities in dorsolateral prefrontal cortex white matter. Am J Psychiatry 2004;161:1293-1296.
Sexton CE, Kalu UG, Filippini N, Mackay CE, Ebmeier KP. A meta-analysis of diffusion tensor imaging in mild cognitive impairment and Alzheimer's disease. Neurobiol. Aging 2011;32:2322.e5-18.
Smith SM, Jenkinson M, Johansen-Berg H, et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 2006;31:1487-1505.
Snook L, Plewes C, Beaulieu C. Voxel based versus region of interest analysis in diffusion tensor imaging of neurodevelopment. NeuroImage 2007;34:243-252.
O'Dwyer L, Lamberton F, Bokde ALW, et al. Multiple Indices of Diffusion Identifies White Matter Damage in Mild Cognitive Impairment and Alzheimer's Disease. PLoS One 2011;6: e21745.
Kantarci K, Petersen RC, Boeve BF, et al. DWI predicts future progression to Alzheimer's disease in amnestic mild cognitive impairment. Neurology 2005;64:902-904.
Zhang Y, Schuff N, Jahng G-H, et al. Diffusion tensor imaging of cingulum fibers in mild cognitive impairment and Alzheimer disease. Neurology 2007;68:13-19.
Beaulieu C, Does MD, Snyder RE, Allen PS..Changes in water diffusion due to Wallerian degeneration in peripheral nerve. Magn Reson Med 1996;36:627-631.
Smith SM, Johansen-Berg H, Jenkinson M, et al. Acquisition and voxelwise analysis of multi-subject diffusion data with Tract-Based Spatial Statistics. Nat Protocols 2007;2:499-503.
Otsuka Y, Yamauchi H, Sawamoto N, Iseki K, Tomimoto H, Fukuyama H.Diffuse tract damage in the hemispheric deep white matter may correlate with global cognitive impairment and callosal atrophy in patients with extensive leukoaraiosis. Am J Neuroradiol 2012;33:726-732.
Román GC, Sachdev P, Royall DR, et al. Vascular cognitive disorder: a new diagnostic category updating vascular cognitive impairment and vascular dementia. J Neurol Sci 2004; 226:81-87.
Fu J-L, Zhang T, Chang C, 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 Radiol 2012;53:312-317.
Black S, Gao F, Bilbao J. Understanding White Matter Disease Imaging-Pathological Correlations in Vascular Cognitive Impairment. Stroke 2009; 40:S48-S52.
O'Sullivan M, Morris RG, Huckstep B, Jones DK, Williams SCR, Markus HS. Diffusion tensor MRI correlates with executive dysfunction in patients with ischaemic leukoaraiosis. J Neurol Neurosurg Psychiatry 2004;75: 441-447.
Mills S, Cain J, Purandare N, Jackson A. Biomarkers of cerebrovascular disease in dementia. Br J Radiol 2007;(Spec No 2):S128-145.
Shim YS, Yoon B, Shon Y-M, Ahn K-J, Yang D-W. Difference of the hippocampal and white matter microalterations in MCI patients according to the severity of subcortical vascular changes: Neuropsychological correlates of diffusion tensor imaging. Clin Neurol Neurosurg 2008;110:552-561.
Vernooij MW, de Groot M, van der Lugt A, et al. White matter atrophy and lesion formation explain the loss of structural integrity of white matter in aging. Neuroimage 2008;43:470-477.
Vernooij MW, Ikram MA, Vrooman HA, et al. White matter microstructural integrity and cognitive function in a general elderly population. Arch Gen Psychiatry 2009;66:545-553.
[Kennedy KM, Raz N. Pattern of normal age-related regional differences in white matter microstructure is modified by vascular risk. Brain Res 2009;1297: 41-56.
Chalela JA, Wolf RL, Maldjian JA, Kasner SE. MRI identification of early white matter injury in anoxic-ischemic encephalopathy. Neurology 2001;56: 481-485.
Schmidt R, Ropele S, Ferro J, et al. Diffusion-weighted imaging and cognition in the leukoariosis and disability in the elderly study. Stroke 2004;41: e402-408.
Burgmans S, van Boxtel MPJ, Gronenschild EHBM, et al. Multiple indicators of age-related differences in cerebral white matter and the modifying effects of hypertension. Neuroimage 2010;49: 2083-2093.
Raz N, Rodrigue KM, Acker JD. Hypertension and the brain: vulnerability of the prefrontal regions and executive functions. Behav Neurosci 2003;117:1169-1180.
Raz N, Lindenberger U, Rodrigue KM, et al.Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex 2005;15:1676-1689.
Strassburger TL, Lee HC, Daly EM, et al. Interactive effects of age and hypertension on volumes of brain structures. Stroke 1997;28:1410-1417.
Breteler MM, van Swieten JC, Bots ML, et al. Cerebral white matter lesions, vascular risk factors, and cognitive function in a population-based study: the Rotterdam Study. Neurology 1994;44:1246-1252.
Goldstein IB, Bartzokis G, Hance DB, Shapiro D. Relationship between blood pressure and subcortical lesions in healthy elderly people. Stroke 1998;29: 765-772.
[Murray AD, Staff RT, Shenkin SD, Deary IJ, Starr JM, Whalley LJ. Brain white matter hyperintensities: relative importance of vascular risk factors in nondemented elderly people. Radiology 2005;237:251-257.
Salat DH, Williams VJ, Leritz EC, et al. Inter-individual variation in blood pressure is associated with regional white matter integrity in generally healthy older adults. Neuroimage 2012;59:181-192.
Acosta-Cabronero J, Williams GB, Pengas G, Nestor PJ. Absolute diffusivities define the landscape of white matter degeneration in Alzheimer's disease. Brain 2010;133:529-539.
Sun SW, Liang HF, Trinkaus K, Cross AH, Armstrong RC, Song SK. Noninvasive detection of cuprizone induced axonal damage and demyelination in the mouse corpus callosum. Magn Reson Med 2006;55: 302-308.
Song SK, Yoshino J, Le TQ, et al. Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 2005;26:132-140.
Sullivan EV, Rohlfing T, Pfefferbaum A. Quantitative fiber tracking of lateral and interhemispheric white matter systems in normal aging: relations to timed performance. Neurobiol Aging 2010;31:464-481.
Counsell SJ, Shen Y, Boardman JP, et al. Axial and radial diffusivity in preterm infants who have diffuse white matter changes on magnetic resonance imaging at term-equivalent age. Pediatrics 2006;117:376-386.
Chen S, Kang Z, Hu X, Hu B, Zou Y. Diffusion tensor imaging of the brain in patients with Alzheimer's disease and cerebrovascular lesions. J Zhejiang Univ Sci B 2007;8: 242-247.
Zhou Y, Lin F, Zhu J, et al. Whole brain diffusion tensor imaging histogram analysis in vascular cognitive impairment. J Neurol Sci 2008;268:60-64.

Publication Dates

Publication in this collection
Jul-Sep 2012

History

Received
12 June 2012
Accepted
15 Aug 2012

This is an open-access article distributed under the terms of the Creative Commons Attribution License

[1] DeCarli C, Fletcher E, Ramey V, Harvey D, Jagust WJ. Anatomical Mapping of White Matter Hyperintensities (WMH) Exploring the Relationships Between Periventricular WMH, Deep WMH, and Total WMH Burden. Stroke 2005;36:50-55.

[2] Hardiman O, Doherty CP (editors) Neurodegenerative Disorders: A Clinical Guide, Springer; 2011.

[3] Inzitari D, Pracucci G, Poggesi A, et al. Changes in white matter as determinant of global functional decline in older independent outpatients: three year follow-up of LADIS (leukoaraiosis and disability) study cohort. BMJ 2009;339: b2477.

[4] Le Bihan D, Mangin JF, Poupon C, et al.Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 2001;13: 534-546.

[5] Damoiseaux JS, Smith SM, Witter MP, et al. White matter tract integrity in aging and Alzheimer's disease. Hum Brain Mapp 2009;30:1051-1059.

[6] Bosch B, Arenaza-Urquijo EM, Rami L, et al. (Multiple DTI index analysis in normal aging, amnestic MCI and AD. Relationship with neuropsychological performance. Neurobiol Aging 2012;33:61-74.

[7] Basser PJ, Mattiello J, LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 1994;103: 247-254.

[8] Pierpaoli C, Basser PJ. .Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 1996;36:893-906.

[9] Alexopoulos GS, Kiosses DN, Choi SJ, Murphy CF, Lim KO. Frontal White Matter Microstructure and Treatment Response of Late-Life Depression: A Preliminary Study. Am J Psychiatry 2002;159:1929-1932.

[10] Nobuhara K, Okugawa G, Sugimoto T, et al. Frontal white matter anisotropy and symptom severity of late-life depression: a magnetic resonance diffusion tensor imaging study. J Neurol Neurosurg Psychiatry 2006;77:120-122.

[11] Taylor WD, MacFall JR, Payne ME, et al. (Late-life depression and microstructural abnormalities in dorsolateral prefrontal cortex white matter. Am J Psychiatry 2004;161:1293-1296.

[12] Sexton CE, Kalu UG, Filippini N, Mackay CE, Ebmeier KP. A meta-analysis of diffusion tensor imaging in mild cognitive impairment and Alzheimer's disease. Neurobiol. Aging 2011;32:2322.e5-18.

[13] Smith SM, Jenkinson M, Johansen-Berg H, et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 2006;31:1487-1505.

[14] Snook L, Plewes C, Beaulieu C. Voxel based versus region of interest analysis in diffusion tensor imaging of neurodevelopment. NeuroImage 2007;34:243-252.

[15] O'Dwyer L, Lamberton F, Bokde ALW, et al. Multiple Indices of Diffusion Identifies White Matter Damage in Mild Cognitive Impairment and Alzheimer's Disease. PLoS One 2011;6: e21745.

[16] Kantarci K, Petersen RC, Boeve BF, et al. DWI predicts future progression to Alzheimer's disease in amnestic mild cognitive impairment. Neurology 2005;64:902-904.

[17] Zhang Y, Schuff N, Jahng G-H, et al. Diffusion tensor imaging of cingulum fibers in mild cognitive impairment and Alzheimer disease. Neurology 2007;68:13-19.

[18] Beaulieu C, Does MD, Snyder RE, Allen PS..Changes in water diffusion due to Wallerian degeneration in peripheral nerve. Magn Reson Med 1996;36:627-631.

[19] Smith SM, Johansen-Berg H, Jenkinson M, et al. Acquisition and voxelwise analysis of multi-subject diffusion data with Tract-Based Spatial Statistics. Nat Protocols 2007;2:499-503.

[20] Otsuka Y, Yamauchi H, Sawamoto N, Iseki K, Tomimoto H, Fukuyama H.Diffuse tract damage in the hemispheric deep white matter may correlate with global cognitive impairment and callosal atrophy in patients with extensive leukoaraiosis. Am J Neuroradiol 2012;33:726-732.

[21] Román GC, Sachdev P, Royall DR, et al. Vascular cognitive disorder: a new diagnostic category updating vascular cognitive impairment and vascular dementia. J Neurol Sci 2004; 226:81-87.

[22] Fu J-L, Zhang T, Chang C, 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 Radiol 2012;53:312-317.

[23] Black S, Gao F, Bilbao J. Understanding White Matter Disease Imaging-Pathological Correlations in Vascular Cognitive Impairment. Stroke 2009; 40:S48-S52.

[24] O'Sullivan M, Morris RG, Huckstep B, Jones DK, Williams SCR, Markus HS. Diffusion tensor MRI correlates with executive dysfunction in patients with ischaemic leukoaraiosis. J Neurol Neurosurg Psychiatry 2004;75: 441-447.

[25] Mills S, Cain J, Purandare N, Jackson A. Biomarkers of cerebrovascular disease in dementia. Br J Radiol 2007;(Spec No 2):S128-145.

[26] Shim YS, Yoon B, Shon Y-M, Ahn K-J, Yang D-W. Difference of the hippocampal and white matter microalterations in MCI patients according to the severity of subcortical vascular changes: Neuropsychological correlates of diffusion tensor imaging. Clin Neurol Neurosurg 2008;110:552-561.

[27] Vernooij MW, de Groot M, van der Lugt A, et al. White matter atrophy and lesion formation explain the loss of structural integrity of white matter in aging. Neuroimage 2008;43:470-477.

[28] Vernooij MW, Ikram MA, Vrooman HA, et al. White matter microstructural integrity and cognitive function in a general elderly population. Arch Gen Psychiatry 2009;66:545-553.

[29] [Kennedy KM, Raz N. Pattern of normal age-related regional differences in white matter microstructure is modified by vascular risk. Brain Res 2009;1297: 41-56.

[30] Chalela JA, Wolf RL, Maldjian JA, Kasner SE. MRI identification of early white matter injury in anoxic-ischemic encephalopathy. Neurology 2001;56: 481-485.

[31] Schmidt R, Ropele S, Ferro J, et al. Diffusion-weighted imaging and cognition in the leukoariosis and disability in the elderly study. Stroke 2004;41: e402-408.

[32] Burgmans S, van Boxtel MPJ, Gronenschild EHBM, et al. Multiple indicators of age-related differences in cerebral white matter and the modifying effects of hypertension. Neuroimage 2010;49: 2083-2093.

[33] Raz N, Rodrigue KM, Acker JD. Hypertension and the brain: vulnerability of the prefrontal regions and executive functions. Behav Neurosci 2003;117:1169-1180.

[34] Raz N, Lindenberger U, Rodrigue KM, et al.Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex 2005;15:1676-1689.

[35] Strassburger TL, Lee HC, Daly EM, et al. Interactive effects of age and hypertension on volumes of brain structures. Stroke 1997;28:1410-1417.

[36] Breteler MM, van Swieten JC, Bots ML, et al. Cerebral white matter lesions, vascular risk factors, and cognitive function in a population-based study: the Rotterdam Study. Neurology 1994;44:1246-1252.

[37] Goldstein IB, Bartzokis G, Hance DB, Shapiro D. Relationship between blood pressure and subcortical lesions in healthy elderly people. Stroke 1998;29: 765-772.

[38] [Murray AD, Staff RT, Shenkin SD, Deary IJ, Starr JM, Whalley LJ. Brain white matter hyperintensities: relative importance of vascular risk factors in nondemented elderly people. Radiology 2005;237:251-257.

[39] Salat DH, Williams VJ, Leritz EC, et al. Inter-individual variation in blood pressure is associated with regional white matter integrity in generally healthy older adults. Neuroimage 2012;59:181-192.

[40] Acosta-Cabronero J, Williams GB, Pengas G, Nestor PJ. Absolute diffusivities define the landscape of white matter degeneration in Alzheimer's disease. Brain 2010;133:529-539.

[41] Sun SW, Liang HF, Trinkaus K, Cross AH, Armstrong RC, Song SK. Noninvasive detection of cuprizone induced axonal damage and demyelination in the mouse corpus callosum. Magn Reson Med 2006;55: 302-308.

[42] Song SK, Yoshino J, Le TQ, et al. Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 2005;26:132-140.

[43] Sullivan EV, Rohlfing T, Pfefferbaum A. Quantitative fiber tracking of lateral and interhemispheric white matter systems in normal aging: relations to timed performance. Neurobiol Aging 2010;31:464-481.

[44] Counsell SJ, Shen Y, Boardman JP, et al. Axial and radial diffusivity in preterm infants who have diffuse white matter changes on magnetic resonance imaging at term-equivalent age. Pediatrics 2006;117:376-386.

[45] Chen S, Kang Z, Hu X, Hu B, Zou Y. Diffusion tensor imaging of the brain in patients with Alzheimer's disease and cerebrovascular lesions. J Zhejiang Univ Sci B 2007;8: 242-247.

[46] Zhou Y, Lin F, Zhu J, et al. Whole brain diffusion tensor imaging histogram analysis in vascular cognitive impairment. J Neurol Sci 2008;268:60-64.

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