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Original research
Impact of white matter networks on risk for memory decline following resection versus ablation in temporal lobe epilepsy
  1. Erik Kaestner1,
  2. Alena Stasenko1,
  3. Adam Schadler1,
  4. Rebecca Roth2,
  5. Kelsey Hewitt2,
  6. Anny Reyes1,
  7. Deqiang Qiu3,
  8. Leonardo Bonilha4,
  9. Natalie Voets5,
  10. Ranliang Hu3,
  11. Jon Willie6,
  12. Nigel Pedersen7,
  13. Jerry Shih8,
  14. Sharona Ben-Haim9,
  15. Robert Gross10,
  16. Daniel Drane2,
  17. Carrie R McDonald1,11
  1. 1 Radiation Medicine and Applied Sciences, University of California, San Diego, La Jolla, California, USA
  2. 2 Neurology, Emory University School of Medicine, Atlanta, Georgia, USA
  3. 3 Radiology and Imaging Sciences, Emory University, Atlanta, Georgia, USA
  4. 4 Department of Neurology, University of South Carolina System, Columbia, South Carolina, USA
  5. 5 NDCN, University of Oxford, Oxford, UK
  6. 6 Neurosurgery, Washington University in St Louis, St Louis, Missouri, USA
  7. 7 Neurology, UC Davis, Davis, California, USA
  8. 8 Neurosciences, University of California, San Diego, La Jolla, California, USA
  9. 9 Neurosurgery, University of California, San Diego, La Jolla, California, USA
  10. 10 Department of Neurological Surgery, Emory University School of Medicine, Atlanta, Georgia, USA
  11. 11 Psychiatry, University of California, San Diego, La Jolla, California, USA
  1. Correspondence to Dr Carrie R McDonald, Radiation Medicine and Applied Sciences, University of California, San Diego, La Jolla, California, USA; camcdonald{at}health.ucsd.edu

Abstract

Background With expanding neurosurgical options in epilepsy, it is important to characterise each options’ risk for postoperative cognitive decline. Here, we characterise how patients’ preoperative white matter (WM) networks relates to postoperative memory changes following different epilepsy surgeries.

Methods Eighty-nine patients with temporal lobe epilepsy with T1-weighted and diffusion-weighted imaging as well as preoperative and postoperative verbal memory scores (prose recall) underwent either anterior temporal lobectomy (ATL: n=38) or stereotactic laser amygdalohippocampotomy (SLAH; n=51). We computed laterality indices (ie, asymmetry) for volume of the hippocampus and fractional anisotropy (FA) of two deep WM tracts (uncinate fasciculus (UF) and inferior longitudinal fasciculus (ILF)).

Results Preoperatively, left-lateralised FA of the ILF was associated with higher prose recall (p<0.01). This pattern was not observed for the UF or hippocampus (ps>0.05). Postoperatively, right-lateralised FA of the UF was associated with less decline following left ATL (p<0.05) but not left SLAH (p>0.05), while right-lateralised hippocampal asymmetry was associated with less decline following both left ATL and SLAH (ps<0.05). After accounting for preoperative memory score, age of onset and hippocampal asymmetry, the association between UF and memory decline in left ATL remained significant (p<0.01).

Conclusions Asymmetry of the hippocampus is an important predictor of risk for memory decline following both surgeries. However, asymmetry of UF integrity, which is only severed during ATL, is an important predictor of memory decline after ATL only. As surgical procedures and pre-surgical mapping evolve, understanding the role of frontal-temporal WM in memory networks could help to guide more targeted surgical approaches to mitigate cognitive decline.

  • EPILEPSY
  • EPILEPSY, SURGERY
  • MEMORY
  • MRI

Data availability statement

Data are available upon reasonable request. The data that support the findings of this study are available from the corresponding author and co-authors, upon reasonable request.

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Data availability statement

Data are available upon reasonable request. The data that support the findings of this study are available from the corresponding author and co-authors, upon reasonable request.

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Footnotes

  • DD and CRM are joint senior authors.

  • Contributors EK: conceptualisation, data curation, formal analysis, project administration, supervision, visualisation, writing – original draft preparation. AStasenko: conceptualisation, data curation, writing – original draft preparation. ASchadler: data curation, visualisation, writing – review and editing. RR, KH, AR, DQ: data curation, writing – review and editing. LB, NV, NP: writing – review and editing. RH: investigation, data curation, writing – review and editing. JW, JSS, SB-H, RG: investigation, writing – review and editing. DLD: conceptualisation, data curation, funding acquisition, visualisation, writing – review and editing. CRM: conceptualisation, funding acquisition, project administration, resources, writing – original draft preparation, guarantor.

  • Funding We would like to acknowledge funding support from the National Institute of Health: K01NS124831 (EK), R01NS124585 (CRM) and R01NS088748 (DLD); F32NS119285-01A1 (AStasenko).

  • Competing interests None declared.

  • Provenance and peer review Not commissioned; externally peer reviewed.

  • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.