White matter asymmetries in patients with cerebral small vessel disease

Abstract

White matter (WM) asymmetries of the human brain have been well documented using diffusion tensor imaging (DTI). The purpose of this study was to investigate white matter asymmetry across the whole brain in cerebral small vessel disease (SVD) patients and evaluate the relation between the factors which often represent disease's existence and white matter asymmetry. A total of 105 nondemented elderly with cerebral SVD patients aged between 60 and 85 years were included in this study. All participants underwent T1 MPRAGE, fluid-attenuated inversion recovery and DTI scanning. With tract-based spatial statistics (TBSS) in DTI, this study examined the WM asymmetries and the correlations between WM asymmetries and four distinct factors such as deep white matter hyperintensities (DWMH) score, periventricularhyperintensities (PVH) score, cerebral microbleed (CMB) number and lacune number. Our study suggests the asymmetric microstructural change in SVD patients involving the right more injured than the left. The four factors jointly affect right brain anisotropy decrease in the middle cerebellar peduncle, the cerebral peduncle, the pontine crossing tract, the corticospinal tract, the medial lemniscus, the posterior limb of internal capsule and the frontal pattern of white matter. The results of our study demonstrated the lost right white matter may be the mainly origin of dysfunction in SVD patients. This asymmetry should help to evaluate prognostic indicators of disease progression in lesion-based neuropathology.

Keywords

White matter (WM) asymmetries cerebral small vessel disease FA asymmetry

Get full access to this article

View all access options for this article.

References

Abdul-Kareem

I.A.

, Stancak

and Parkes

L.M.

, Plasticity of the superior and middle cerebellar peduncles in musicians revealed by quantitative analysis of volume and number of streamlines based on diffusion tensor tractography, The Cerebellum 10(3) (2011), 611–623. doi:10.1007/s12311-011-0274-1.

Acosta-Cabronero

, Williams

G.B.

and Pengas

, Absolute diffusivities define the landscape of white matter degeneration in Alzheimer's disease, Brain 133(2) (2010), 529–539. doi:10.1093/brain/awp257.

Ardekani

, Kumar

and Bartzokis

, Exploratory voxel-based analysis of diffusion indices and hemispheric asymmetry in normal aging, Magnetic Resonance Imaging 25(2) (2007), 154. doi:10.1016/j.mri.2006.09.045.

Baker

J.G.

, Williams

A.J.

and Ionita

C.C.

, Cerebral small vessel disease: Cognition, mood, daily functioning, and imaging findings from a small pilot sample, Dementia & Geriatric Cognitive Disorders Extra 2(1) (2012), 169–179. doi:10.1159/000333482.

Beaton

A.A.

, The relation of planum temporale asymmetry and morphology of the corpus callosum to handedness, gender, and dyslexia: A review of the evidence, Brain and Language 60(2) (1997), 255–322.

Bogousslavsky

and Regli

, Capsular genu syndrome, Neurology 40(10) (1990), 1499–1502. doi:10.1212/WNL.40.10.1499.

Bosch

, Arenazaurquijo

E.M.

and Rami

, Multiple DTI index analysis in normal aging, amnestic MCI and AD. Relationship with neuropsychological performance, Neurobiology of Aging 33(1) (2012), 61–74. doi:10.1016/j.neurobiolaging.2010.02.004.

Braffman

B.H.

, Zimmerman

R.A.

, Trojanowski

J.Q.

and Brain

M.R.

, Pathologic correlation with Gross and histopathology. 1. Lacunar infarction and Virchow-Robin spaces, AJR Am J Roentgenol 151(3) (1988), 551–558. doi:10.2214/ajr.151.3.551.

Büchel

, Raedler

, Sommer

and Sach

, White matter asymmetry in the human brain: A diffusion tensor MRI study, Cerebral Cortex 14(9) (2004), 945–951. doi:10.1093/cercor/bhh055.

10.

Cabeza

, Hemispheric asymmetry reduction in older adults: The HAROLD model, Psychology & Aging 17(1) (2002), 85–100. doi:10.1037/0882-7974.17.1.85.

11.

Canu

, Mclaren

D.G.

and Fitzgerald

M.E.

, Microstructural diffusion changes are independent of macrostructural volume loss in moderate to severe Alzheimer's disease, Journal of Alzheimers Disease 19(3) (2010), 963–976. doi:10.3233/JAD-2010-1295.

12.

Charlton

R.A.

, Morris

R.G.

and Nitkunan

, et al., The cognitive profiles of CADASIL and sporadic small vessel disease, Neurology 66(10) (2006), 1523–1526.

13.

De Schotten

M.T.

, Ffytche

D.H.

and Bizzi

, Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography, Neuroimage 54(1) (2011), 49–59. doi:10.1016/j.neuroimage.2010.07.055.

14.

Della

N.R.

, Ginestroni

and Tessa

, Brain white matter tracts degeneration in friedreich ataxia. An in vivo MRI study using tract-based spatial statistics and voxel-based morphometry, Neuroimage 40(1) (2008), 19–25. doi:10.1016/j.neuroimage.2007.11.050.

15.

Eckert

M.A.

, Keren

N.I.

and Roberts

D.R.

, Age-related changes in processing speed: Unique contributions of cerebellar and prefrontal cortex, Frontiers in Human Neuroscience 4(1) (2010), 10–17.

16.

Eluvathingal

T.J.

, Hasan

K.M.

and Kramer

, Quantitative diffusion tensor tractography of association and projection fibers in normally developing children and adolescents, Cerebral Cortex 17(12) (2007), 2760–2768. doi:10.1093/cercor/bhm003.

17.

Fazekas

, Chawluk

J.B.

, Alavi

, Hurtig

H.I.

and Zimmerman

R.A.

, Mr signal abnormalities at 1.5 t in Alzheimer's dementia and normal aging, Ajr American Journal of Roentgenology 149(2) (1987), 351–356. doi:10.2214/ajr.149.2.351.

18.

Folstein

M.F.

, Folstein

S.E.

and McHugh

P.R.

, Mini-Mental State: A Practical Method for Grading the Cognitive State of Patients for the Clinician, Vol. 47, Pergamon Press, 1975, pp. 496–499.

19.

Geschwind

and Galaburda

A.M.

, Cerebral Dominance: The Biological Foundations, Harvard University Press, 1984.

20.

Gong

, Jiang

and Zhu

, Asymmetry analysis of cingulum based on scale-invariant parameterization by diffusion tensor imaging, Human Brain Mapping 24(2) (2005), 92–98. doi:10.1002/hbm.20072.

21.

Happé

, Booth

and Charlton

, Executive function deficits in autism spectrum disorders and attention-deficit/hyperactivity disorder: Examining profiles across domains and ages, Brain Cogn 61(1) (2006), 25–39. doi:10.1016/j.bandc.2006.03.004.

22.

Huster

R.J.

, Westerhausen

and Kreuder

, Morphologic asymmetry of the human anterior cingulate cortex, Neuroimage 34(3) (2007), 888–895. doi:10.1016/j.neuroimage.2006.10.023.

23.

Jahanshad

, Lee

A.D.

and Barysheva

, Genetic influences on brain asymmetry: A DTI study of 374 twins and siblings, Neuroimage 52(2) (2010), 455–469. doi:10.1016/j.neuroimage.2010.04.236.

24.

Jones

D.K.

, Lythgoe

and Horsfield

M.A.

, Characterization of white matter damage in ischemic leukoaraiosis with diffusion tensor MRI, Stroke 30(2) (1999), 393–397. doi:10.1161/01.STR.30.2.393.

25.

Kim

, Lee

S.K.

and Lee

J.D.

, Decreased fractional anisotropy of middle cerebellar peduncle in crossed cerebellar diaschisis: Diffusion-tensor imaging-positron-emission tomography correlation study, Ajnr Am J Neuroradiol 26(26) (2005), 2224–2228.

26.

Kleffner

, Deppe

, Mohammadi

et al., Diffusion tensor imaging demonstrates fiber impairment in susac syndrome, Neurology 70(2) (2008), 1867–1869. doi:10.1212/01.wnl.0000280580.95671.01.

27.

Kljajevic

, White matter architecture of the language network, Translational Neuroscience 5(4) (2014), 239–252. doi:10.2478/s13380-014-0232-8.

28.

Koziol

J.A.

, Wagner

and Sobel

D.F.

, Asymmetries in the spatial distributions of enhancing lesions and black holes in relapsing-remitting MS, Journal of Clinical Neuroscience 12(8) (2005), 895–901. doi:10.1016/j.jocn.2004.11.010.

29.

Liu

, Liu

and Liu

, Investigation of cerebral iron deposition in aged patients with ischemic cerebrovascular disease using susceptibility-weighted imaging, Therapeutics & Clinical Risk Management 12 (2016), 1239–1247. doi:10.2147/TCRM.S107783.

30.

Makris

, Kennedy

D.N.

and Mcinerney

, Segmentation of subcomponents within the superior longitudinal fascicle in humans: A quantitative, in vivo, DT-MRI study, Cerebral Cortex 15(6) (2005), 854–869. doi:10.1093/cercor/bhh186.

31.

Masri

O.A.

, An essay on the human corticospinal tract: History, development, anatomy, and connections, Neuroanatomy 10 (2011), 1–4.

32.

Møller

, Frandsen

and Andersen

, Dynamic changes in corticospinal tracts after stroke detected by fibretracking, Journal of Neurology Neurosurgery & Psychiatry 78(6) (2007), 587–592. doi:10.1136/jnnp.2006.100248.

33.

Mühlau

, Gaser

and Wohlschläger

A.M.

, Striatal gray matter loss in Huntington's disease is leftward biased, Movement Disorders 22(8) (2007), 1169–1173. doi:10.1002/mds.21137.

34.

Murphy

M.L.

and Frodl

, Meta-analysis of diffusion tensor imaging studies shows altered fractional anisotropy occurring in distinct brain areas in association with depression, Biology of Mood & Anxiety Disorders 1(1) (2011), 3–12. doi:10.1186/2045-5380-1-3.

35.

Nathan

P.W.

, Smith

M.C.

and Deacon

, The corticospinal tracts in man, Course and location of fibres at different segmental levels 113(2) (1990), 303–324.

36.

Nitkunan

, Barrick

T.R.

and Charlton

R.A.

, Multimodal MRI in cerebral small vessel disease: Its relationship with cognition and sensitivity to change over time, Stroke 39(7) (2008), 1999–2005. doi:10.1161/STROKEAHA.107.507475.

37.

Park

H.J.

, Westin

C.F.

and Kubicki

, White matter hemisphere asymmetries in healthy subjects and in schizophrenia: A diffusion tensor MRI study, Neuroimage 23(1) (2004), 213–223. doi:10.1016/j.neuroimage.2004.04.036.

38.

Patel

and Markus

H.S.

, Magnetic resonance imaging in cerebral small vessel disease and its use as a surrogate disease marker, International Journal of Stroke 6(1) (2011), 47–59. doi:10.1111/j.1747-4949.2010.00552.x.

39.

Powell

H.W.

, Parker

G.J.

and Alexander

D.C.

, Hemispheric asymmetries in language-related pathways: A combined functional MRI and tractographystudy, Neuroimage 32(1) (2006), 388–399. doi:10.1016/j.neuroimage.2006.03.011.

40.

Prins

N.D.

, Van Dijk

E.J.

and Den Heijer

Cerebral small-vessel disease and decline in information processing speed, executive function and memory, Brain 128(9) (2005), 2034. doi:10.1093/brain/awh553.

41.

Reich

, Smith

S.C.

and Zackowski

, Quantitative characterization of the corticospinal tract at 3T, American Journal of Neuroradiology 27(10) (2006), 2168–2178.

42.

Risberg

, Halsey

J.H.

and Wills

E.L.

, Hemispheric specialization in normal man studied by bilateral measurements of the regional cerebral blood flow. A study with the 133-Xe inhalation technique, Brain 98(3) (1975), 511–524. doi:10.1093/brain/98.3.511.

43.

Rueckert

, Sonoda

L.I.

and Hayes

, Nonrigid registration using free-form deformations: Application to breast MR images, IEEE Transactions on Medical Imaging 18(8) (1999), 712–721. doi:10.1109/42.796284.

44.

Schiavone

, Charlton

R.A.

and Barrick

T.R.

, Imaging age-related cognitive decline: A comparison of diffusion tensor and magnetization transfer MRI, Journal of Magnetic Resonance Imaging Jmri 29(1) (2009), 23–30. doi:10.1002/jmri.21572.

45.

Schmidt

, Ropele

and Ferro

, Diffusion-weighted imaging and cognition in the leukoariosis and disability in the elderly study, Stroke; a journal of cerebral circulation 41(5) (2010), e402–e408. doi:10.1161/STROKEAHA.109.576629.

46.

Schretlen

D.J.

, Varvaris

and Vannorsdall

T.D.

, Brain white matter volume abnormalities in Lesch–Nyhan disease and its variants, Neurology 84(2) (2015), 190–196. doi:10.1212/WNL.0000000000001128.

47.

Simonyan

, Tovarmoll

and Ostuni

, Focal white matter changes in spasmodic dysphonia: A combined diffusion tensor imaging and neuropathological study, Brain 131(2) (2008), 447–459. doi:10.1093/brain/awm303.

48.

Smith

S.M.

, Jenkinson

and Johansen-Berg

, Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data, Neuroimage 31(4) (2006), 1487–1505. doi:10.1016/j.neuroimage.2006.02.024.

49.

Smith

S.M.

, Johansenberg

and Jenkinson

, Acquisition and voxelwise analysis of multi-subject diffusion data with tract-based spatial statistics, Nature Protocols 2(3) (2007), 499–503. doi:10.1038/nprot.2007.45.

50.

Takao

, Hayashi

and Ohtomo

, White matter asymmetry in healthy individuals: A diffusion tensor imaging study using tract-based spatial statistics, Neuroscience 193(15) (2011), 291–299. doi:10.1016/j.neuroscience.2011.07.041.

51.

Toga

A.W.

and Thompson

P.M.

, Mapping brain asymmetry, Nature Reviews Neuroscience 4(1) (2003), 37–48. doi:10.1038/nrn1009.

52.

Toosy

A.T.

, Werring

D.J.

and Orrell

R.W.

, Diffusion tensor imaging detects corticospinal tract involvement at multiple levels in amyotrophic lateral sclerosis, Journal of Neurology Neurosurgery & Psychiatry 74(9) (2003), 1250–1257. doi:10.1136/jnnp.74.9.1250.

53.

van Dijk

E.J.

, Prins

N.D.

and Vrooman

H.A.

, Progression of cerebral small vessel disease in relation to risk factors and cognitive consequences: Rotterdam scan study, Stroke 39(10) (2008), 2712–2719. doi:10.1161/STROKEAHA.107.513176.

54.

Van Ewijk

, Heslenfeld

D.W.

and Zwiers

M.P.

, Diffusion tensor imaging in attention deficit/hyperactivity disorder: A systematic review and meta-analysis, Neuroscience & Biobehavioral Reviews 36(4) (2012), 1093–1106. doi:10.1016/j.neubiorev.2012.01.003.

55.

van Norden

A.G.

, de Laat

K.F.

and Gons

R.A.

, Causes and consequences of cerebral small vessel disease. The RUN DMC study: A prospective cohort study. Study rationale and protocol, BMC Neurology 11(1) (2011), 29. doi:10.1186/1471-2377-11-29.

56.

Vandermosten

, Price

C.J.

and Golestani

, Plasticity of white matter connectivity in phonetics experts, Brain Structure & Function 221(7) (2015), 1–9.

57.

Werring

D.J.

, Toosy

A.T.

, Clark

C.A.

, Parker

G.J.

, Barker

G.J.

, Miller

D.H.

and Thompson

A.J.

, Diffusion tensor imaging can detect and quantify corticospinal tract degeneration after stroke, Journal of Neurology Neurosurgery & Psychiatry 69(2) (2000), 269–272. doi:10.1136/jnnp.69.2.269.

58.

Yakupoglu

, Civelek

and Onal

, Surgery decision in brainstem mass resection by diffusion tensor based fiber tracking assistance: A report of four cases, Journal of Neurological Sciences 29(1) (2012), 117–121.

59.

Yasmin

, Aoki

and Abe

, Tract-specific analysis of white matter pathways in healthy subjects: A pilot study using diffusion tensor MRI, Neuroradiology 51(12) (2009), 831–840. doi:10.1007/s00234-009-0580-1.

60.

Yin

, Han

and Ge

, Inferior frontal white matter asymmetry correlates with executive control of attention, Human Brain Mapping 34(4) (2013), 796–813. doi:10.1002/hbm.21477.