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Brain morphological and microstructural features in cryptogenic late-onset temporal lobe epilepsy: a structural and diffusion MRI study

  • Functional Neuroradiology
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Abstract

Purpose

Although epilepsy in the elderly has attracted attention recently, there are few systematic studies of neuroimaging in such patients. In this study, we used structural MRI and diffusion tensor imaging (DTI) to investigate the morphological and microstructural features of the brain in late-onset temporal lobe epilepsy (TLE).

Methods

We recruited patients with TLE and an age of onset > 50 years (late-TLE group) and age- and sex-matched healthy volunteers (control group). 3-Tesla MRI scans, including 3D T1-weighted images and 15-direction DTI, showed normal findings on visual assessment in both groups. We used Statistical Parametric Mapping 12 (SPM12) for gray and white matter structural normalization and comparison and used Tract-Based Spatial Statistics (TBSS) for fractional anisotropy and mean diffusivity comparisons of DTI. In both methods, p < 0.05 (family-wise error) was considered statistically significant.

Results

In total, 30 patients with late-onset TLE (mean ± SD age, 66.8 ± 8.4; mean ± SD age of onset, 63.0 ± 7.6 years) and 40 healthy controls (mean ± SD age, 66.6 ± 8.5 years) were enrolled. The late-onset TLE group showed significant gray matter volume increases in the bilateral amygdala and anterior hippocampus and significantly reduced mean diffusivity in the left temporofrontal lobe, internal capsule, and brainstem. No significant changes were evident in white matter volume or fractional anisotropy.

Conclusions

Our findings may reflect some characteristics or mechanisms of cryptogenic TLE in the elderly, such as inflammatory processes.

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References

  1. Brodie MJ, Kwan P (2005) Epilepsy in elderly people. BMJ 331(7528):1317–1322. https://doi.org/10.1136/bmj.331.7528.1317

    Article  PubMed  PubMed Central  Google Scholar 

  2. Stefan H (2011) Epilepsy in the elderly: facts and challenges. Acta Neurol Scand 124(4):223–237. https://doi.org/10.1111/j.1600-0404.2010.01464.x

    Article  PubMed  CAS  Google Scholar 

  3. Sillanpaa M, Kalviainen R, Klaukka T, Helenius H, Shinnar S (2006) Temporal changes in the incidence of epilepsy in Finland: nationwide study. Epilepsy Res 71(2–3):206–215. https://doi.org/10.1016/j.eplepsyres.2006.06.017

    Article  PubMed  Google Scholar 

  4. Stefan H, May TW, Pfafflin M, Brandt C, Furatsch N, Schmitz B, Wandschneider B, Kretz R, Runge U, Geithner J, Karakizlis C, Rosenow F, Kerling F (2014) Epilepsy in the elderly: comparing clinical characteristics with younger patients. Acta Neurol Scand 129(5):283–293. https://doi.org/10.1111/ane.12218

    Article  PubMed  CAS  Google Scholar 

  5. Tanaka A, Akamatsu N, Shouzaki T, Toyota T, Yamano M, Nakagawa M, Tsuji S (2013) Clinical characteristics and treatment responses in new-onset epilepsy in the elderly. Seizure 22(9):772–775. https://doi.org/10.1016/j.seizure.2013.06.005

    Article  PubMed  Google Scholar 

  6. Malter MP, Widman G, Galldiks N, Stoecker W, Helmstaedter C, Elger CE, Wagner J (2016) Suspected new-onset autoimmune temporal lobe epilepsy with amygdala enlargement. Epilepsia 57(9):1485–1494. https://doi.org/10.1111/epi.13471

    Article  PubMed  CAS  Google Scholar 

  7. von Podewils F, Suesse M, Geithner J, Gaida B, Wang ZI, Lange J, Dressel A, Grothe M, Kessler C, Langner S, Runge U, Bien CG (2017) Prevalence and outcome of late-onset seizures due to autoimmune etiology: a prospective observational population-based cohort study. Epilepsia 58(9):1542–1550. https://doi.org/10.1111/epi.13834

    Article  CAS  Google Scholar 

  8. Ashburner J, Friston KJ (2000) Voxel-based morphometry--the methods. NeuroImage 11(6 Pt 1):805–821. https://doi.org/10.1006/nimg.2000.0582

    Article  PubMed  CAS  Google Scholar 

  9. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TE (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage 31(4):1487–1505. https://doi.org/10.1016/j.neuroimage.2006.02.024

    Article  PubMed  Google Scholar 

  10. Engel J Jr (1996) Introduction to temporal lobe epilepsy. Epilepsy Res 26(1):141–150

    Article  PubMed  Google Scholar 

  11. Campos BM, Coan AC, Beltramini GC, Liu M, Yassuda CL, Ghizoni E, Beaulieu C, Gross DW, Cendes F (2015) White matter abnormalities associate with type and localization of focal epileptogenic lesions. Epilepsia 56(1):125–132. https://doi.org/10.1111/epi.12871

    Article  PubMed  Google Scholar 

  12. Ashburner J (2007) A fast diffeomorphic image registration algorithm. NeuroImage 38(1):95–113. https://doi.org/10.1016/j.neuroimage.2007.07.007

    Article  PubMed  Google Scholar 

  13. Smith SM (2002) Fast robust automated brain extraction. Hum Brain Mapp 17(3):143–155. https://doi.org/10.1002/hbm.10062

    Article  PubMed  Google Scholar 

  14. Keller SS, Wieshmann UC, Mackay CE, Denby CE, Webb J, Roberts N (2002) Voxel based morphometry of grey matter abnormalities in patients with medically intractable temporal lobe epilepsy: effects of side of seizure onset and epilepsy duration. J Neurol Neurosurg Psychiatry 73(6):648–655

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Bonilha L, Rorden C, Castellano G, Pereira F, Rio PA, Cendes F, Li LM (2004) Voxel-based morphometry reveals gray matter network atrophy in refractory medial temporal lobe epilepsy. Arch Neurol 61(9):1379–1384. https://doi.org/10.1001/archneur.61.9.1379

    Article  PubMed  Google Scholar 

  16. McMillan AB, Hermann BP, Johnson SC, Hansen RR, Seidenberg M, Meyerand ME (2004) Voxel-based morphometry of unilateral temporal lobe epilepsy reveals abnormalities in cerebral white matter. NeuroImage 23(1):167–174. https://doi.org/10.1016/j.neuroimage.2004.05.002

    Article  PubMed  Google Scholar 

  17. Keller SS, Roberts N (2008) Voxel-based morphometry of temporal lobe epilepsy: an introduction and review of the literature. Epilepsia 49(5):741–757. https://doi.org/10.1111/j.1528-1167.2007.01485.x

    Article  PubMed  Google Scholar 

  18. Riederer F, Lanzenberger R, Kaya M, Prayer D, Serles W, Baumgartner C (2008) Network atrophy in temporal lobe epilepsy: a voxel-based morphometry study. Neurology 71(6):419–425. https://doi.org/10.1212/01.wnl.0000324264.96100.e0

    Article  PubMed  CAS  Google Scholar 

  19. Yasuda CL, Betting LE, Cendes F (2010) Voxel-based morphometry and epilepsy. Expert Rev Neurother 10(6):975–984. https://doi.org/10.1586/ern.10.63

    Article  PubMed  Google Scholar 

  20. Otte WM, van Eijsden P, Sander JW, Duncan JS, Dijkhuizen RM, Braun KP (2012) A meta-analysis of white matter changes in temporal lobe epilepsy as studied with diffusion tensor imaging. Epilepsia 53(4):659–667. https://doi.org/10.1111/j.1528-1167.2012.03426.x

    Article  PubMed  Google Scholar 

  21. Mueller SG, Laxer KD, Cashdollar N, Buckley S, Paul C, Weiner MW (2006) Voxel-based optimized morphometry (VBM) of gray and white matter in temporal lobe epilepsy (TLE) with and without mesial temporal sclerosis. Epilepsia 47(5):900–907. https://doi.org/10.1111/j.1528-1167.2006.00512.x

    Article  PubMed  PubMed Central  Google Scholar 

  22. Hanby MF, Al-Bachari S, Makin F, Vidyasagar R, Parkes LM, Emsley HC (2015) Structural and physiological MRI correlates of occult cerebrovascular disease in late-onset epilepsy. Neuroimage Clin 9:128–133. https://doi.org/10.1016/j.nicl.2015.07.016

    Article  PubMed  PubMed Central  Google Scholar 

  23. Bower SP, Vogrin SJ, Morris K, Cox I, Murphy M, Kilpatrick CJ, Cook MJ (2003) Amygdala volumetry in "imaging-negative" temporal lobe epilepsy. J Neurol Neurosurg Psychiatry 74(9):1245–1249. https://doi.org/10.1136/jnnp.74.9.1245

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Mitsueda-Ono T, Ikeda A, Inouchi M, Takaya S, Matsumoto R, Hanakawa T, Sawamoto N, Mikuni N, Fukuyama H, Takahashi R (2011) Amygdalar enlargement in patients with temporal lobe epilepsy. J Neurol Neurosurg Psychiatry 82(6):652–657. https://doi.org/10.1136/jnnp.2010.206342

    Article  PubMed  Google Scholar 

  25. Sone D, Ito K, Taniguchi G, Murata Y, Nakata Y, Watanabe Y, Okazaki M, Sato N, Matsuda H, Watanabe M (2015) Evaluation of amygdala pathology using (11)C-methionine positron emission tomography/computed tomography in patients with temporal lobe epilepsy and amygdala enlargement. Epilepsy Res 112:114–121. https://doi.org/10.1016/j.eplepsyres.2015.02.018

    Article  PubMed  Google Scholar 

  26. Beh SM, Cook MJ, D'Souza WJ (2016) Isolated amygdala enlargement in temporal lobe epilepsy: a systematic review. Epilepsy Behav 60:33–41. https://doi.org/10.1016/j.yebeh.2016.04.015

    Article  PubMed  Google Scholar 

  27. Coan AC, Morita ME, Campos BM, Bergo FP, Kubota BY, Cendes F (2013) Amygdala enlargement occurs in patients with mesial temporal lobe epilepsy and hippocampal sclerosis with early epilepsy onset. Epilepsy Behav 29(2):390–394. https://doi.org/10.1016/j.yebeh.2013.08.022

    Article  PubMed  Google Scholar 

  28. Sone D, Ikemura M, Saito Y, Taniguchi G, Kunii N (2017) Marked accumulation of oligodendroglia-like cells in temporal lobe epilepsy with amygdala enlargement and hippocampal sclerosis. Neuropathology. https://doi.org/10.1111/neup.12410

  29. Reyes A, Thesen T, Kuzniecky R, Devinsky O, McDonald CR, Jackson GD, Vaughan DN, Blackmon K (2017) Amygdala enlargement: temporal lobe epilepsy subtype or nonspecific finding? Epilepsy Res 132:34–40. https://doi.org/10.1016/j.eplepsyres.2017.02.019

    Article  PubMed  PubMed Central  Google Scholar 

  30. Sone D, Ota M, Maikusa N, Kimura Y, Sumida K, Yokoyama K, Imabayashi E, Watanabe M, Watanabe Y, Okazaki M, Sato N, Matsuda H (2016) White matter abnormalities in patients with temporal lobe epilepsy and amygdala enlargement: comparison with hippocampal sclerosis and healthy subjects. Epilepsy Res 127:221–228. https://doi.org/10.1016/j.eplepsyres.2016.09.011

    Article  PubMed  Google Scholar 

  31. Lv RJ, Sun ZR, Cui T, Guan HZ, Ren HT, Shao XQ (2014) Temporal lobe epilepsy with amygdala enlargement: a subtype of temporal lobe epilepsy. BMC Neurol 14:194. https://doi.org/10.1186/s12883-014-0194-z

    Article  PubMed  PubMed Central  Google Scholar 

  32. Sone D, Matsuda H, Ota M, Maikusa N, Kimura Y, Sumida K, Yokoyama K, Imabayashi E, Watanabe M, Watanabe Y, Okazaki M, Sato N (2016) Graph theoretical analysis of structural neuroimaging in temporal lobe epilepsy with and without psychosis. PLoS One 11(7):e0158728. https://doi.org/10.1371/journal.pone.0158728

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Rathore C, Radhakrishnan K (2015) Concept of epilepsy surgery and presurgical evaluation. Epileptic Disord 17(1):19–31; quiz 31. https://doi.org/10.1684/epd.2014.0720

    Article  PubMed  Google Scholar 

  34. Wagner J, Weber B, Elger CE (2015) Early and chronic gray matter volume changes in limbic encephalitis revealed by voxel-based morphometry. Epilepsia 56(5):754–761. https://doi.org/10.1111/epi.12968

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Psychiatry, National Center of Neurology and Psychiatry, Tokyo, Japan

    Daichi Sone, Yutaka Watanabe & Mitsutoshi Okazaki

  2. Integrative Brain Imaging Center, National Center of Neurology and Psychiatry, 4-1-1 Ogawa-Higashi, Kodaira, Tokyo, 187-8551, Japan

    Daichi Sone & Hiroshi Matsuda

  3. Department of Radiology, National Center of Neurology and Psychiatry, Tokyo, Japan

    Noriko Sato & Yukio Kimura

Authors
  1. Daichi Sone
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  2. Noriko Sato
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  3. Yukio Kimura
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  4. Yutaka Watanabe
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  5. Mitsutoshi Okazaki
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  6. Hiroshi Matsuda
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Corresponding author

Correspondence to Daichi Sone.

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Funding

This study was funded in part by grants from the Japan Epilepsy Research Foundation (JERF TENKAN 17009) and the Japan Society for the Promotion of Science (KAKENHI Grant Number JP17H07385) (both to DS).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

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Sone, D., Sato, N., Kimura, Y. et al. Brain morphological and microstructural features in cryptogenic late-onset temporal lobe epilepsy: a structural and diffusion MRI study. Neuroradiology 60, 635–641 (2018). https://doi.org/10.1007/s00234-018-2019-z

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  • DOI: https://doi.org/10.1007/s00234-018-2019-z

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