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3.2 Generic Studies in Epilepsy

3.2.4 Malformations of Cortical Development

Diffusion measures evolve with brain maturation so may assist the detection of malformations of cortical development (MCD). Widespread diffusion changes comprising reduced FA and increased MD extending beyond the visible abnormality have been identified in MCD (Eriksson et al. 2001) and in other focal lesions (Dumas de la Roque et al. 2005). In tuberous sclerosis, ADC is elevated in both epileptic and non- epileptic tubers, but more so in the former (Jansen et al. 2003). In focal cortical dysplasia (FCD), fibre connectivity assessed by FA is reduced in subcortical white matter adjacent to the abnormality (Lee et al. 2004b) and is accompanied by a rise in MD although this may not extend to FCD without white matter

Paper Patients/ Controls

Pathology Laterality Analysis Regions Positive findings

Arfanakis et al. 2002

15 / 15 TLE (HS or MRI-negative)

- ROI EC/CC/IC EC/CC (FA, RD)

Concha et al. 2005

8 / 9 MTLE (HS) 6L, 2R Tractography Fornix, cingulum Bilateral fornix (FA, RD), cingulum (FA, MD, RD)

Thivard et al. 2005

35 / 36 MTLE (any) 18L, 17R ROI Hippocampus Contralateral MD

SPM Whole brain Ipsilateral hippocampus, temporal, posterior extratemporal (FA and/or MD); contralateral hippocampus, amygdala, temporal pole (MD) Kimiwada

et al. 2006

14 / 14 (children)

TLE (any) 11L, 3R ROI Hippocampus, thalamus,

lentiform

Bilateral hippocampus (FA), ipsilateral hippocampus (MD)

Gross et al. 2006

11 / 14 MTLE (HS) 7L, 4R ROI Hippocampus, EC/CC/IC EC/CC (FA, MD)

Yu et al. 2006

14 / 14 MTLE (HS or MRI-negative)

5L, 9R ROI Hippocampus Bilateral MD (ipsilateral greater)

Rodrigo et al. 2007

Focke et al. 2008

33 / 37 MTLE (HS) 21L, 12R SPM Whole brain LHS: Ipsilateral TL/FL, bilateral thalamus/cingulate (FA); ipsilateral TL/cingulum, bilateral FL (MD)

RHS: Ipsilateral TL (FA); ipsilateral hippocampus/TL (MD)

TBSS Whole brain LHS: Ipsilateral TL/fornix, bilateral thalamus/cingulate, bilateral FL (FA); ipsilateral TL/thalamus, bilateral cingulum/CC/EC (MD)

RHS: Ipsilateral TL/PHG/fornix, bilateral cingulum/CC (FA); ipsilateral TL/FL, bilateral parietal (MD)

Govindan et al. 2008 13 / 12 (children) TLE (MRI- negative)

All left Tractography UF, ILF, AF, CST Bilaterally in all (FA) - reversed asymmetry of AF

Gong et al. 2008

17 / 26 TLE (HS) 11L, 6R ROI Thalamus Reduced FA, increased MD bilaterally

10 / same TLE (no HS) 4L, 2R, 4 bilateral

No significant differences

Kim et al. 2008

10 / 10 TLE (any) 4L, 6R ROI Corpus callosum Reduced FA/AD, increased RD in splenium

Nilsson et al. 2008

8 / 10 (children)

TLE (any) 7L, 1R Tractography Temporal, cingulate Bilateral changes (MD, AD, RD)

Concha et al. 2009

17 / 25 TLE (HS) - ROI EC/CC EC/CC (FA, MD, RD) (both except MD in CC HS only)

13 / same TLE (MRI- negative)

6L, 2R, 5 bilateral

Tractography Fornix, cingulum, CC Bilateral cingulum (FA, MD, RD; both groups), bilateral fornix (FA, RD; HS only)

Knake et al. 2009

12 / 12 MTLE (HS) All left ROI Hippocampus, PHG, TL,

FL, CC

Ipsilateral hippocampus, PHG, CC (FA)

VBA (unspecified)

Whole brain Bilateral TL, CC, ipsilateral frontal (FA)

Ahmadi et al. 2009

21 / 21 TLE (any) 10L, 11R Tractography Cingulum, PHG, SLF, ILF, UF, fornix, ATR, IFOF

LTLE: reduced ipsilateral (6 tracts) and contralateral (4 tracts) RTLE: reduced ipsilateral (4 tracts)

Shon et al. 2010

19 / 20 TLE (HS) 12L, 7R SPM Whole brain LHS: Ipsilateral hippocampus, TL, FL, cingulate

RHS: Medial temporal/frontoparietal

18 / same TLE (non-HS) 10L, 8R LTLE: Ipsilateral posterior limbic (PHG/cingulate)

RTLE: No changes Bonilha et

al. 2010

23 / 34 MTLE (HS) 8L, 15R NPM Whole brain Medial TL, frontotemporal, orbitofrontal ipsi>contra (FA); FL, TL (MD in RHS)

Kim et al. 2010

9 / 16 TLE (HS) 5L, 4R ROI Thalamus Asymmetrical reduced FA

Bilateral increased MD 9 / same TLE (dysplasia) 5L, 4R Asymmetrical reduced FA Bilateral increased MD Meng et al. 2010 8 / 8 (children)

TLE (any) 6L, 2R ROI CC/EC/IC Bilateral IC/splenium (FA)

Bilateral IC/EC (MD) Kemmotsu

et al. 2011

36 / 36 TLE (any) 18L, 18R ROI (atlas) Fornix, PHG, UF, ILF, IFOF, AF

Bilateral changes (FA), more marked ipsilateral and LTLE (especially UF, ILF)

Afzali et al. 2011

19 / 12 TLE (any) 11L, 8R SPM/TBSS Whole brain TL/PHG/FL/EC/fornix/CC (FA)

Keller et al. 2013

10 / 81 TLE (MRI- negative)

All left SPM Whole brain Bilateral TL/CC/EC/thalamus (FA), CC/thalamus (MD)

Keller et al. 2012

62 / 68 TLE (HS) 41L, 21R ROI TL, FL, CC, IC,

brainstem, hippocampus, PHG, putamen, thalamus

LHS: bilateral hippocampus, PHG, TL, CC, FL, IC, brainstem (FA) RHS: right PHG, bilateral thalamus/CC (FA)

Liacu et al. 2012

9 / 10 TLE (HS) 7L, 2R Tractography Cingulum, fornix Bilateral changes (FA, RD)

9 / same TLE (MRI- negative)

8L, 1R Ipsilateral all (FA), cingulum (RD), no contralateral changes

Oguz et al. 2013

44 / 44 MTLE (HS) 22L, 22R TBSS Whole brain Temporal/extra-temporal especially ipsilateral (FA, MD); FA changes greatest in male/left, MD in female/right

Table 3.1 - Summary of cross sectional DTI studies in epilepsy

Pathology: HS = hippocampal sclerosis; Analysis: ROI = region-of-interest based, SPM = statistical parameter mapping, TBSS = tract-based spatial statistics, VBA = voxel-based analysis; Regions and Tracts: AF = arcuate fasciculus, ATR = anterior thalamic radiation, CC = corpus callosum, CST = corticospinal tract, EC = external capsule, FL = frontal lobe, IC = internal capsule, IFOF = inferior

fronto-occipital fasciculus, ILF = inferior longitudinal fasciculus, PHG = parahippocampal gyrus, SLF = superior longitudinal fasciculus, TL = temporal lobe, UF = uncinate fasciculus; Positive

Paper Patients/ Controls

Pathology Laterality Surgery Timepoints Analysis Regions Positive findings

Concha et al. 2006

3 / 1 Various - Corpus

callosotomy

0w/1w/2-4m Tractography Corpus callosum 1w: decreased FA/AD (axonal degradation) 2-4m: decreased FA, increased MD/RD (myelin degradation) Concha et al. 2007 8 / 22 HS 6L, 2R ATLR (3) or SAH (5) 0y/1y Tractography ROI Fornix, cingulum EC/genu/splenium

0: reduced FA, increased MD/RD bilateral fornix, cingulum, EC

1y: ipsilateral fornix/cingulum reduced FA/increased MD/RD; contralateral fornix, cingulum, EC did not normalise

Thivard et al. 2007

24 / 36 HS 12L, 12R ATLR (20)

or SAH (4)

0m/8m ROI Hippocampus 0: Increased MD ipsilateral, decreased MD

contralateral 8m: contralateral MD normalised Schoene- Bake et al. 2009 40 / 28 HS 19L, 21R ATLR (3) or SAH (37) No pre-op 3-11y

TBSS Whole brain LHS: reduced FA ipsilateral SLF, cingulum, CC, forceps minor, UF, IFOF, ILF, CST, contralateral ILF

RHS: reduced FA ipsilateral SLF, cingulum, CC, UF, ATR, IFOF, ILF, CST, contralateral posterior cingulum

McDonald et al. 2010

7 / none TLE 3L, 4R ATLR 0m/2m/12m ROI (atlas) Fornix, UF, PHC,

ATR, SLF, IFOF, ILF, CST, cingulum

2m: decreased FA ipsilateral ILF, PHC, UF, IFOF, CC, bilateral fornix

12m: no further change Yogarajah

et al. 2010

46 / none TLE 26L, 20R ATLR 0m/4m TBSS Whole brain LHS: reduced FA ipsilateral OR, PHG, SLF,

UF; bilateral ILF, fornix, AC; increased FA corona radiata, IC, EC; increased MD ipsilateral ILF, UF, AC, EC

RHS: reduced FA ipsilateral OR, PHG, SLF, UF, IFOF; bilateral ILF, fornix, AC; increased FA corona radiata; increased MD ipsilateral UF, AC, EC, bilateral fornix

Nguyen et al. 2011 22 / none (only 10 in post-op) HS 11L, 11R ATLR 0m/2-7m TBSS (left flipped)

Whole brain 0: reduced FA ipsilateral HIP/fornix/UF/CC, widespread increased MD

2-7m: increased MD ipsilateral anterior temporal

Faber et al. 2013

20 / none HS All left SAH 0m/3-

6m/12m

TBSS Whole brain 3-6m: reduced FA left cingulum, fornix 12m: in addition, reduced FA UF Liu et al. 2013 6 / 3 TLE 3L, 3R ATLR (4) or SAH (2) Many e.g. 0, 1/2/3/6d, 2m

Tractography Fornix Ipsilateral MD/AD/RD reduced by 2 days FA reduced/MD/RD rises by 1-4m

Table 3.2 - Summary of longitudinal DTI studies in epilepsy

Pathology and Analysis: as Table 3.1; Surgery: ATLR = anterior temporal lobe resection, SAH = selective amygdalohippocampectomy; Region and Tracts: AC = anterior commissure, ATR = anterior

The reduced FA could be a result of increased or abnormally located grey matter or pathological white matter with abnormal myelination or ectopic neurons whilst the increase in MD could reflect defective neurogenesis or cellular loss increasing the extracellular space (Eriksson et al. 2001). Improved diffusion models to study the extracellular volume could help disentangle these possibilities (Chapter 13).