Influence of the topography of brain damage on depression and fatigue in patients with multiple sclerosis

Abstract

Objectives:

Involvement of selected central nervous system (CNS) regions has been associated with depression and fatigue in MS. We assessed whether specific regional patterns of lesion distribution and atrophy of the gray (GM) and white matter (WM) are associated with these symptoms in MS.

Methods:

Brain dual-echo and 3D T1-weighted images were acquired from 123 MS patients (69 depressed (D), 54 non-depressed (nD), 64 fatigued, 59 non-fatigued) and 90 controls. Lesion distribution, GM and WM atrophy were estimated using VBM and SPM8.

Results:

Gender, age, disease duration and conventional MRI characteristics did not differ between D-MS and nD-MS patients. Fatigued patients experienced higher EDSS and depression than non-fatigued ones. Lesion distribution and WM atrophy were not related to depression and fatigue. Atrophy of regions in the frontal, parietal and occipital lobes had a combined effect on depression and fatigue. Atrophy of the left middle frontal gyrus and right inferior frontal gyrus were selectively related to depression. No specific pattern of GM atrophy was found to be related to fatigue.

Conclusions:

Depression in MS is linked to atrophy of cortical regions located in the bilateral frontal lobes. A distributed pattern of GM atrophy contributes to the concomitant presence of depression and fatigue in these patients.

Keywords

Multiple sclerosis magnetic resonance imaging depression fatigue regional damage atrophy

Get full access to this article

View all access options for this article.

References

Sadovnick

Remick

Allen

. Depression and multiple sclerosis. Neurology 1996; 46: 628–632.

Kessler

Borges

Walters

Prevalence of and risk factors for lifetime suicide attempts in the national comorbidity survey. Arch Gen Psychiatry 1999; 56: 617–626.

Minden

Schiffer

Affective disorders in multiple sclerosis. Review and recommendations for clinical research. Arch Neurol 1990; 47: 98–104.

Benedict

Weinstock-Guttman

Fishman

. Prediction of neuropsychological impairment in multiple sclerosis: Comparison of conventional magnetic resonance imaging measures of atrophy and lesion burden. Arch Neurol 2004; 61: 226–230.

Zabad

Patten

Metz

The association of depression with disease course in multiple sclerosis. Neurology 2005; 64: 359–360.

Pujol

Bello

Deus

. Lesions in the left arcuate fasciculus region and depressive symptoms in multiple sclerosis. Neurology 1997; 49: 1105–1110.

Bakshi

Czarnecki

Shaikh

. Brain MRI lesions and atrophy are related to depression in multiple sclerosis. Neuroreport 2000; 11: 1153–1158.

Zorzon

Zivadinov

Nasuelli

. Depressive symptoms and MRI changes in multiple sclerosis. Eur J Neurol 2002; 9: 491–496.

Honer

Hurwitz

. Temporal lobe involvement in multiple sclerosis patients with psychiatric disorders. Arch Neurol 1987; 44: 187–190.

10.

Feinstein

Kartsounis

Miller

. Clinically isolated lesions of the type seen in multiple sclerosis: A cognitive, psychiatric, and MRI follow up study. J Neurol Neurosurg Psychiatry 1992; 55: 869–876.

11.

Zorzon

de Masi

Nasuelli

. Depression and anxiety in multiple sclerosis. A clinical and MRI study in 95 subjects. J Neurol 2001; 248: 416–421.

12.

Feinstein

Roy

Lobaugh

. Structural brain abnormalities in multiple sclerosis patients with major depression. Neurology 2004; 62: 586–590.

13.

Feinstein

O’Connor

Akbar

. Diffusion tensor imaging abnormalities in depressed multiple sclerosis patients. Mult Scler 2010; 16: 189–196.

14.

Gold

O’Connor

Gill

. Detection of altered hippocampal morphology in multiple sclerosis-associated depression using automated surface mesh modeling. Hum Brain Mapp. Epub ahead of print 30 July 2012. DOI: 10.1002/hbm.22154.

15.

Montgomery

Asberg

A new depression scale designed to be sensitive to change. Br J Psychiatry 1979; 134: 382-389.

16.

Krupp

LaRocca

Muir-Nash

. The fatigue severity scale. Application to patients with multiple sclerosis and systemic lupus erythematosus. Arch Neurol 1989; 46: 1121–1123.

17.

Fischer

Rudick

Cutter

. The Multiple Sclerosis Functional Composite Measure (MSFC): An integrated approach to MS clinical outcome assessment. National MS Society Clinical Outcomes Assessment Task Force. Mult Scler 1999; 5: 244–250.

18.

Riccitelli

Rocca

Forn

. Voxelwise assessment of the regional distribution of damage in the brains of patients with multiple sclerosis and fatigue. AJNR Am J Neuroradiol 2011; 32: 874–879.

19.

Tzourio-Mazoyer

Landeau

Papathanassiou

. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002; 15: 273–289.

20.

Mori

Wanaka

Van Zijl

PCM

. MRI atlas of human white matter. Amsterdam: The Netherlands: Elsevier, 2005.

21.

Krupp

Coyle

Doscher

. Fatigue therapy in multiple sclerosis: Results of a double-blind, randomized, parallel trial of amantadine, pemoline, and placebo. Neurology 1995; 45: 1956–1961.

22.

Bakshi

Miletich

Henschel

. Fatigue in multiple sclerosis: Cross-sectional correlation with brain MRI findings in 71 patients. Neurology 1999; 53: 1151–1153.

23.

Colombo

Martinelli Boneschi

Rossi

. MRI and motor evoked potential findings in nondisabled multiple sclerosis patients with and without symptoms of fatigue. J Neurol 2000; 247: 506–509.

24.

Pardini

Bonzano

Mancardi

. Frontal networks play a role in fatigue perception in multiple sclerosis. Behav Neurosci 2010; 124: 329–336.

25.

Riccitelli

Rocca

Pagani

. Cognitive impairment in multiple sclerosis is associated to different patterns of gray matter atrophy according to clinical phenotype. Hum Brain Mapp 2011; 32: 1535–1543.

26.

Riccitelli

Rocca

Pagani

. Mapping regional grey and white matter atrophy in relapsing–remitting multiple sclerosis. Mult Scler 2012; 18: 1027–1037.

27.

Sepulcre

Masdeu

Goni

. Fatigue in multiple sclerosis is associated with the disruption of frontal and parietal pathways. Mult Scler 2009; 15: 337–344.

28.

Liu

Guo

. Classification of different therapeutic responses of major depressive disorder with multivariate pattern analysis method based on structural MR scans. PLoS One 2012; 7: e40968.

29.

Bora

Fornito

Pantelis

. Gray matter abnormalities in Major Depressive Disorder: A meta-analysis of voxel based morphometry studies. J Affect Disord 2012; 138: 9–18.

30.

Wagner

Maril

Bjork

. Prefrontal contributions to executive control: fMRI evidence for functional distinctions within lateral prefrontal cortex. Neuroimage 2001; 14: 1337–1347.

31.

Walker

Berard

Berrigan

. Detecting cognitive fatigue in multiple sclerosis: Method matters. J Neurol Sci 2012; 316: 86–92.

32.

van Tol

van der Wee

van den Heuvel

. Regional brain volume in depression and anxiety disorders. Arch Gen Psychiatry 2010; 67: 1002–1011.

33.

Wang

LaBar

Smoski

. Prefrontal mechanisms for executive control over emotional distraction are altered in major depression. Psychiatry Res 2008; 163: 143–155.

34.

Bremner

Vythilingam

. Regional brain metabolic correlates of alpha-methylparatyrosine-induced depressive symptoms: Implications for the neural circuitry of depression. JAMA 2003; 289: 3125–3134.

35.

Yue

. Voxelwise meta-analysis of gray matter reduction in major depressive disorder. Prog Neuropsychopharmacol Biol Psychiatry 2012; 36: 11–16.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

0.03 MB