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Higher incidence of epilepsy in meningiomas located on the premotor cortex: a voxel-wise statistical analysis

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Abstract

Background

A substantial number of patients with brain tumors develop recurrent seizures, known as tumor-associated epilepsy. It is important to identify specific subgroups of brain tumor patients with higher incidences of epilepsy because a meta-analysis failed to certify the effectiveness of prophylactic anti-epileptic drugs (AEDs) to abort tumor-associated epilepsy as a whole.

Methods

To investigate the relationship between tumor location and incidence of epilepsy, we performed voxel-wise comparison between 3D MRI scans obtained from patients with meningioma-associated epilepsy and those from control patients using spatial normalization techniques on neuroimaging data. Variables such as age, tumor size, the degree of edema, and pathological diagnosis were also compared between the two groups.

Results

Our results showed the highest incidence of epilepsy when the tumor was located on the premotor cortex in the frontal lobe (Z-scores >2.0, Liebermeister’s quasi-exact test). The stepwise multiple regression analysis on the clinical data revealed that the tumor diameter (p < 0.001) and the patient’s age (p = 0.024) were positive and negative predictors, respectively, for the onset of epilepsy.

Conclusions

The incidence of epilepsy was higher in meningiomas located on the premotor cortex than on the other cortex. Larger volume also contributed to the onset of epilepsy. We suggest that variations of epilepsy incidence dependent on tumor characteristics can be considered when treating tumor-associated epilepsy.

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References

  1. Herman ST (2002) Epilepsy after brain insult: targeting epileptogenesis. Neurology 59:S21–S26

    Article  PubMed  Google Scholar 

  2. Glantz MJ, Cole BF, Forsyth PA, Recht LD, Wen PY, Chamberlain MC, Grossman SA, Cairncross JG (2000) Practice parameter: anticonvulsant prophylaxis in patients with newly diagnosed brain tumors. Report of the quality standards subcommittee of the American Academy of Neurology. Neurology 54:1886–1893

    Article  PubMed  CAS  Google Scholar 

  3. Glantz MJ, Cole BF, Friedberg MH, Lathi E, Choy H, Furie K, Akerley W, Wahlberg L, Lekos A, Louis S (1996) A randomized, blinded, placebo-controlled trial of divalproex sodium prophylaxis in adults with newly diagnosed brain tumors. Neurology 46:985–991

    Article  PubMed  CAS  Google Scholar 

  4. Rothoerl RD, Bernreuther D, Woertgen C, Brawanski A (2003) The value of routine electroencephalographic recordings in predicting postoperative seizures associated with meningioma surgery. Neurosurg Rev 26:108–112

    Article  PubMed  Google Scholar 

  5. Kawaguchi T, Kameyama S, Tanaka R (1996) Peritumoral edema and seizure in patients with cerebral convexity and parasagittal meningiomas. Neurol Med Chir (Tokyo) 36:568–573, discussion 573–564

    Article  CAS  Google Scholar 

  6. van Breemen MS, Wilms EB, Vecht CJ (2007) Epilepsy in patients with brain tumours: epidemiology, mechanisms, and management. Lancet Neurol 6:421–430

    Article  PubMed  Google Scholar 

  7. Bates E, Wilson SM, Saygin AP, Dick F, Sereno MI, Knight RT, Dronkers NF (2003) Voxel-based lesion-symptom mapping. Nat Neurosci 6:448–450

    PubMed  CAS  Google Scholar 

  8. Fridriksson J, Kjartansson O, Morgan PS, Hjaltason H, Magnusdottir S, Bonilha L, Rorden C (2010) Impaired speech repetition and left parietal lobe damage. J Neurosci 30:11057–11061

    Article  PubMed  CAS  Google Scholar 

  9. Karnath HO, Rennig J, Johannsen L, Rorden C (2011) The anatomy underlying acute versus chronic spatial neglect: a longitudinal study. Brain 134:903–912

    Article  PubMed  Google Scholar 

  10. Karnath HO, Rorden C, Ticini LF (2009) Damage to white matter fiber tracts in acute spatial neglect. Cereb Cortex 19:2331–2337

    Article  PubMed  Google Scholar 

  11. Saygin AP (2007) Superior temporal and premotor brain areas necessary for biological motion perception. Brain 130:2452–2461

    Article  PubMed  Google Scholar 

  12. Henry ML, Beeson PM, Stark AJ, Rapcsak SZ (2007) The role of left perisylvian cortical regions in spelling. Brain Lang 100:44–52

    Article  PubMed  Google Scholar 

  13. De Santis A, Baratta P, Bello L, Spagnoli D, Ceccarelli G, Songa V, De Silva E, Signoroni G, Villani RM (1996) Early postoperative seizures and endovenous phenytoin. Preliminary clinical data. J Neurosurg Sci 40:207–212

    PubMed  Google Scholar 

  14. Franceschetti S, Binelli S, Casazza M, Lodrini S, Panzica F, Pluchino F, Solero CL, Avanzini G (1990) Influence of surgery and antiepileptic drugs on seizures symptomatic of cerebral tumours. Acta Neurochir (Wien) 103:47–51

    Article  CAS  Google Scholar 

  15. Chozick BS, Reinert SE, Greenblatt SH (1996) Incidence of seizures after surgery for supratentorial meningiomas: a modern analysis. J Neurosurg 84:382–386

    Article  PubMed  CAS  Google Scholar 

  16. Lieu AS, Howng SL (2000) Intracranial meningiomas and epilepsy: incidence, prognosis and influencing factors. Epilepsy Res 38:45–52

    Article  PubMed  CAS  Google Scholar 

  17. Go KG, Wilmink JT, Molenaar WM (1988) Peritumoral brain edema associated with meningiomas. Neurosurgery 23:175–179

    Article  PubMed  CAS  Google Scholar 

  18. Rorden C, Brett M (2000) Stereotaxic display of brain lesions. Behav Neurol 12:191–200

    PubMed  Google Scholar 

  19. Crinion J, Ashburner J, Leff A, Brett M, Price C, Friston K (2007) Spatial normalization of lesioned brains: performance evaluation and impact on fMRI analyses. NeuroImage 37:866–875

    Article  PubMed  Google Scholar 

  20. Golay L, Schnider A, Ptak R (2008) Cortical and subcortical anatomy of chronic spatial neglect following vascular damage. Behav Brain Funct 4:43

    Article  PubMed  Google Scholar 

  21. Rorden C, Karnath HO, Bonilha L (2007) Improving lesion-symptom mapping. J Cogn Neurosci 19:1081–1088

    Article  PubMed  Google Scholar 

  22. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15:273–289

    Article  PubMed  CAS  Google Scholar 

  23. Friston KJ, Ashburner J, Frith C, Poline JB, Heather JD, Frackowiak RSJ (1995) Spatial registration and normalization of images. Hum Brain Mapp 2:165–189

    Article  Google Scholar 

  24. Chang EF, Potts MB, Keles GE, Lamborn KR, Chang SM, Barbaro NM, Berger MS (2008) Seizure characteristics and control following resection in 332 patients with low-grade gliomas. J Neurosurg 108:227–235

    Article  PubMed  Google Scholar 

  25. Mahaley MS Jr, Dudka L (1981) The role of anticonvulsant medications in the management of patients with anaplastic gliomas. Surg Neurol 16:399–401

    Article  PubMed  Google Scholar 

  26. Otten ML, Mikell CB, Youngerman BE, Liston C, Sisti MB, Bruce JN, Small SA, McKhann GM 2nd (2012) Motor deficits correlate with resting state motor network connectivity in patients with brain tumours. Brain 135:1017–1026

    Article  PubMed  Google Scholar 

  27. Schaller B (2005) Influences of brain tumor-associated pH changes and hypoxia on epileptogenesis. Acta Neurol Scand 111:75–83

    Article  PubMed  CAS  Google Scholar 

  28. Kim E, Lowenson JD, MacLaren DC, Clarke S, Young SG (1997) Deficiency of a protein-repair enzyme results in the accumulation of altered proteins, retardation of growth, and fatal seizures in mice. Proc Natl Acad Sci U S A 94:6132–6137

    Article  PubMed  CAS  Google Scholar 

  29. Aronica E, Gorter JA, Jansen GH, Leenstra S, Yankaya B, Troost D (2001) Expression of connexin 43 and connexin 32 gap-junction proteins in epilepsy-associated brain tumors and in the perilesional epileptic cortex. Acta Neuropathol 101:449–459

    PubMed  CAS  Google Scholar 

  30. Buckingham SC, Campbell SL, Haas BR, Montana V, Robel S, Ogunrinu T, Sontheimer H (2011) Glutamate release by primary brain tumors induces epileptic activity. Nat Med 17:1269–1274

    Article  PubMed  CAS  Google Scholar 

  31. Maas S, Patt S, Schrey M, Rich A (2001) Underediting of glutamate receptor GluR-B mRNA in malignant gliomas. Proc Natl Acad Sci U S A 98:14687–14692

    Article  PubMed  CAS  Google Scholar 

  32. Jin X, Prince DA, Huguenard JR (2006) Enhanced excitatory synaptic connectivity in layer v pyramidal neurons of chronically injured epileptogenic neocortex in rats. J Neurosci 26:4891–4900

    Article  PubMed  CAS  Google Scholar 

  33. Tauck DL, Nadler JV (1985) Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci 5:1016–1022

    PubMed  CAS  Google Scholar 

  34. Prince DA, Parada I, Scalise K, Graber K, Jin X, Shen F (2009) Epilepsy following cortical injury: cellular and molecular mechanisms as targets for potential prophylaxis. Epilepsia 50(Suppl 2):30–40

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported in part by a research grant to T.H. from The Japan Spina Bifida & Hydrocephalus Research Foundation.

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Authors and Affiliations

  1. Department of Neurosurgery, Kumamoto University Hospital, 1-1-1 Honjo, Chuo-ku, Kumamoto, 862-8556, Japan

    Tadashi Hamasaki, Kazumichi Yamada, Shigetoshi Yano, Hideo Nakamura, Keishi Makino, Taku-ichiro Hide, Yu Hasegawa, Jun-ichiro Kuroda & Jun-ichi Kuratsu

  2. Department of Diagnostic Imaging, Kumamoto University Hospital, 1-1-1 Honjo, Chuo-ku, Kumamoto, 862-8556, Japan

    Toshinori Hirai

  3. Laboratory for Neurosciences Department of Neurosurgery, Kumamoto University Hospital, 1-1-1 Honjo, Chuo-ku, Kumamoto, 862-8556, Japan

    Tadashi Hamasaki

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  1. Tadashi Hamasaki
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  2. Kazumichi Yamada
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Correspondence to Tadashi Hamasaki.

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Hamasaki, T., Yamada, K., Yano, S. et al. Higher incidence of epilepsy in meningiomas located on the premotor cortex: a voxel-wise statistical analysis. Acta Neurochir 154, 2241–2249 (2012). https://doi.org/10.1007/s00701-012-1511-1

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  • DOI: https://doi.org/10.1007/s00701-012-1511-1

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