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March 15, 2022; 98 (11) Research Article

Association Between Microstructural Asymmetry of Temporal Lobe White Matter and Memory Decline After Anterior Temporal Lobectomy

Alena Stasenko, Erik Kaestner, Anny Reyes, Sanam J. Lalani, Brianna Paul, Manu Hegde, Jonathan L. Helm, Sharona Ben-Haim, Carrie R. McDonald
First published January 20, 2022, DOI: https://doi.org/10.1212/WNL.0000000000200047
Alena Stasenko
From the Center for Multimodal Imaging and Genetics (A.S., E.K., A.R., C.R.M.) and Departments of Psychiatry (A.S., E.K., A.R., S.J.L., C.R.M.) and Neurosurgery (S.B.-H.), University of California, San Diego; San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R., C.R.M.); Department of Neurology (B.P., M.H.), University of California, San Francisco; and Department of Psychology (J.L.H.), San Diego State University, CA.
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Erik Kaestner
From the Center for Multimodal Imaging and Genetics (A.S., E.K., A.R., C.R.M.) and Departments of Psychiatry (A.S., E.K., A.R., S.J.L., C.R.M.) and Neurosurgery (S.B.-H.), University of California, San Diego; San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R., C.R.M.); Department of Neurology (B.P., M.H.), University of California, San Francisco; and Department of Psychology (J.L.H.), San Diego State University, CA.
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Anny Reyes
From the Center for Multimodal Imaging and Genetics (A.S., E.K., A.R., C.R.M.) and Departments of Psychiatry (A.S., E.K., A.R., S.J.L., C.R.M.) and Neurosurgery (S.B.-H.), University of California, San Diego; San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R., C.R.M.); Department of Neurology (B.P., M.H.), University of California, San Francisco; and Department of Psychology (J.L.H.), San Diego State University, CA.
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Sanam J. Lalani
From the Center for Multimodal Imaging and Genetics (A.S., E.K., A.R., C.R.M.) and Departments of Psychiatry (A.S., E.K., A.R., S.J.L., C.R.M.) and Neurosurgery (S.B.-H.), University of California, San Diego; San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R., C.R.M.); Department of Neurology (B.P., M.H.), University of California, San Francisco; and Department of Psychology (J.L.H.), San Diego State University, CA.
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Brianna Paul
From the Center for Multimodal Imaging and Genetics (A.S., E.K., A.R., C.R.M.) and Departments of Psychiatry (A.S., E.K., A.R., S.J.L., C.R.M.) and Neurosurgery (S.B.-H.), University of California, San Diego; San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R., C.R.M.); Department of Neurology (B.P., M.H.), University of California, San Francisco; and Department of Psychology (J.L.H.), San Diego State University, CA.
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Manu Hegde
From the Center for Multimodal Imaging and Genetics (A.S., E.K., A.R., C.R.M.) and Departments of Psychiatry (A.S., E.K., A.R., S.J.L., C.R.M.) and Neurosurgery (S.B.-H.), University of California, San Diego; San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R., C.R.M.); Department of Neurology (B.P., M.H.), University of California, San Francisco; and Department of Psychology (J.L.H.), San Diego State University, CA.
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Jonathan L. Helm
From the Center for Multimodal Imaging and Genetics (A.S., E.K., A.R., C.R.M.) and Departments of Psychiatry (A.S., E.K., A.R., S.J.L., C.R.M.) and Neurosurgery (S.B.-H.), University of California, San Diego; San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R., C.R.M.); Department of Neurology (B.P., M.H.), University of California, San Francisco; and Department of Psychology (J.L.H.), San Diego State University, CA.
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Sharona Ben-Haim
From the Center for Multimodal Imaging and Genetics (A.S., E.K., A.R., C.R.M.) and Departments of Psychiatry (A.S., E.K., A.R., S.J.L., C.R.M.) and Neurosurgery (S.B.-H.), University of California, San Diego; San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R., C.R.M.); Department of Neurology (B.P., M.H.), University of California, San Francisco; and Department of Psychology (J.L.H.), San Diego State University, CA.
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Carrie R. McDonald
From the Center for Multimodal Imaging and Genetics (A.S., E.K., A.R., C.R.M.) and Departments of Psychiatry (A.S., E.K., A.R., S.J.L., C.R.M.) and Neurosurgery (S.B.-H.), University of California, San Diego; San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R., C.R.M.); Department of Neurology (B.P., M.H.), University of California, San Francisco; and Department of Psychology (J.L.H.), San Diego State University, CA.
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Citation
Association Between Microstructural Asymmetry of Temporal Lobe White Matter and Memory Decline After Anterior Temporal Lobectomy
Alena Stasenko, Erik Kaestner, Anny Reyes, Sanam J. Lalani, Brianna Paul, Manu Hegde, Jonathan L. Helm, Sharona Ben-Haim, Carrie R. McDonald
Neurology Mar 2022, 98 (11) e1151-e1162; DOI: 10.1212/WNL.0000000000200047

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Abstract

Background and Objectives Risk for memory decline is a substantial concern in patients with temporal lobe epilepsy (TLE) undergoing anterior temporal lobectomy (ATL). Although prior studies have identified associations between memory and integrity of white matter (WM) networks within the medial temporal lobe (MTL) preoperatively, we contribute a study examining whether microstructural asymmetry of deep and superficial WM networks within the MTL predicts postoperative memory decline.

Methods Patients with drug-resistant TLE were recruited from 2 epilepsy centers in a prospective longitudinal study. All patients completed preoperative T1 and diffusion-weighted MRI (DWI) as well as preoperative and postoperative neuropsychological testing. Preoperative fractional anisotropy (FA) of the WM directly beneath the neocortex (i.e., superficial WM [SWM]) and of deep WM tracts associated with memory were calculated. Asymmetry was calculated for hippocampal volume and FA of each WM tract or region and examined in linear and logistic regressions with preoperative to postoperative memory change as the primary outcome.

Results Data were analyzed from 42 patients with TLE (19 left TLE [LTLE], 23 right TLE [RTLE]) who underwent ATL. Leftward FA asymmetry of the entorhinal SWM was associated with decline on prose and associative recall in LTLE, whereas leftward FA asymmetry of the uncinate fasciculus (UNC) was associated with decline on prose recall only. After controlling for preoperative memory score and hippocampal volume, leftward FA asymmetry of the entorhinal SWM uniquely contributed to decline in both prose and associative recall (β = −0.46; SE 0.14 and β = −0.68; SE 0.22, respectively) and leftward FA asymmetry of the UNC uniquely contributed to decline in prose recall (β = −0.31; SE 0.14). A model combining asymmetry of hippocampal volume and entorhinal FA correctly classified memory outcomes in 79% of patients with LTLE for prose (area under the curve [AUC] 0.89; sensitivity 82%; specificity 75%) and 81% of patients for associative (AUC 0.79; sensitivity 83%; specificity 80%) recall. Entorhinal SWM asymmetry was the strongest predictor in both models.

Discussion Preoperative asymmetry of deep WM and SWM integrity within the MTL is a strong predictor of postoperative memory decline in TLE, suggesting that surgical decision-making may benefit from considering each patient's WM network adequacy and reserve in addition to hippocampal integrity.

Classification of Evidence This study provides Class II evidence that preoperative asymmetry of deep WM and SWM integrity within the MTL is a predictor of postoperative memory decline.

Glossary

ATL=
anterior temporal lobectomy;
AUC=
area under the curve;
BVMT-R=
Brief Visuospatial Memory Test–Revised;
DWI=
diffusion-weighted imaging;
FA=
fractional anisotropy;
FDR=
false discovery rate;
FOV=
field of view;
ILF=
inferior longitudinal fasciculus;
LI=
laterality index (left – right/left + right);
LM=
Logical Memory;
LTLE=
left temporal lobe epilepsy;
MTS=
mesial temporal sclerosis;
NPV=
negative predictive value;
OR=
odds ratio;
PPV=
positive predictive value;
RCI-PE=
reliable change indices that account for practice effects;
ROI=
region of interest;
RTLE=
right temporal lobe epilepsy;
SLAH=
stereotactic laser amygdalohippocampotomy;
SWM=
superficial white matter;
TE=
echo time;
TLE=
temporal lobe epilepsy;
TR=
repetition time;
UCSD=
University of California, San Diego;
UCSF=
University of California, San Francisco;
UNC=
uncinate fasciculus;
VPA=
Verbal Paired Associates;
WM=
white matter

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Class of Evidence: NPub.org/coe

  • Received March 24, 2021.
  • Accepted in final form January 3, 2022.
  • © 2022 American Academy of Neurology
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