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Non-pharmacological treatment options of drug-resistant epilepsy in subcortical band heterotopia: systematic review and illustrative case

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Abstract

Objective

Subcortical band heterotopia is a rare X-linked neuronal migration disorder primarily in females often associated with drug-resistant epilepsy. The aim of this study is to review the literature for non-pharmacological treatment options of drug-resistant epilepsy in subcortical band heterotopia.

Material and methods

In accordance with the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines, we performed a systematic review. Entering the keywords “double cortex,” “subcortical band heterotopia,” and “subcortical laminar heterotopia,” we searched Scopus and PubMed databases. We paid particular attention to type of invasive and non-invasive treatment, radiological presentation, and outcome. We also describe a related case report, managed at Alder Hey Children’s Hospital, Liverpool.

Results

The systematic literature review yielded 25 patients with subcortical band heterotopia and drug-resistant epilepsy who underwent non-pharmacological treatment. Including our patient, 26 patients were reported. The patients’ mean age at seizure onset was 6.5 years (range 0.2–23) with a female sex predilection (5.25:1). The patients’ mean age at invasive or non-invasive treatment was 21.5 years (range 6.5–51). The 26 patients underwent 29 non-pharmacological treatments. Ten patients underwent corpus callosotomy; 8 patients had a formal temporal lobectomy. Three patients had focal cortical resection. Two patients respectively had multiple subpial transections, insertion of a vagal nerve stimulator, or deep brain stimulation of the bilateral anterior nuclei of the thalamus. One patient underwent responsive focal neurostimulation. Another patient had transcutaneous stimulation of the vagal nerve. Sixteen patients reported a reduction or the disappearance of the seizures; 1 patient had no improvement. The outcome of 2 patients was classified class I, of 1 patient class II, of 1 patient class III, and of 5 patients class IV according to the Engel Epilepsy Surgery Outcome Scale.

Conclusion

Mainly corpus callosotomy and formal temporal lobectomy have been performed as non-pharmacological treatment with few cases published overall. Several other invasive procedures and one non-invasive technique are based on case reports. The small number of reported cases prevents drawing a firm conclusion as to which non-pharmacological treatment is the best treatment option for refractive epilepsy in patients with subcortical band heterotopia.

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References

  1. Hehr U, Uyanik G, Aigner L, Couillard-Despres S, Winkler J (2007) DCX-related disorders. In: Adam MP, Ardinger HH, Pagon RA, Wallace SE, Bean LJH, Gripp KW, Mirzaa GM, Amemiya A, editors. GeneReviews® [Internet]. Seattle (WA): University of Washington, Seattle; 1993–2022

  2. Barkovich AJ, Guerrini R, Battaglia G, Kalifa G, N’Guyen T, Parmeggiani A, Santucci M, Giovanardi-Rossi P, Granata T, D’Incerti L (1994) Band heterotopia: correlation of outcome with magnetic resonance imaging parameters. Ann Neurol 36(4):609–617. https://doi.org/10.1002/ana.410360409

    Article  CAS  PubMed  Google Scholar 

  3. Dobyns WB, Andermann E, Andermann F, Czapansky-Beilman D, Dubeau F, Dulac O, Guerrini R, Hirsch B, Ledbetter DH, Lee NS, Motte J, Pinard JM, Radtke RA, Ross ME, Tampieri D, Walsh CA, Truwit CL (1996) X-linked malformations of neuronal migration. Neurology 47(2):331–339. https://doi.org/10.1212/wnl.47.2.331

    Article  CAS  PubMed  Google Scholar 

  4. Jacob H (1938) Genetisch verschiedene Gruppen entwicklungsgestörter Gehirne. Genetisch verschiedene Gruppen entwicklungsgestörter Gehirne. Springer, Berlin, Heidelberg, pp 615–648

    Chapter  Google Scholar 

  5. Palmini A, Andermann F, de Grissac H, Tampieri D, Robitaille Y, Langevin P, Desbiens R, Andermann E (1993) Stages and patterns of centrifugal arrest of diffuse neuronal migration disorders. Dev Med Child Neurol 35(4):331–339. https://doi.org/10.1111/j.1469-8749.1993.tb11645.x

    Article  CAS  PubMed  Google Scholar 

  6. Bahi-Buisson N, Souville I, Fourniol FJ, Toussaint A, Moores CA, Houdusse A, Lemaitre JY, Poirier K, Khalaf-Nazzal R, Hully M, Leger PL, Elie C, Boddaert N, Beldjord C, Chelly J, Francis F, SBH-LIS European Consortium (2013) New insights into genotype-phenotype correlations for the doublecortin-related lissencephaly spectrum. Brain 136(Pt 1):223–244. https://doi.org/10.1093/brain/aws323

  7. Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PloS Med 6(7). https://doi.org/10.1371/journal.pmed.1000097

  8. Palmini A, Andermann F, Aicardi J, Dulac O, Chaves F, Ponsot G, Pinard JM, Goutières F, Livingston J, Tampieri D et al (1991) Diffuse cortical dysplasia, or the ‘double cortex’ syndrome: the clinical and epileptic spectrum in 10 patients. Neurology 41(10):1656–1662. https://doi.org/10.1212/wnl.41.10.1656

    Article  CAS  PubMed  Google Scholar 

  9. Landy HJ, Curless RG, Ramsay RE, Slater J, Ajmone-Marsan C, Quencer RM (1993) Corpus callosotomy for seizures associated with band heterotopia. Epilepsia 34(1):79–83. https://doi.org/10.1111/j.1528-1157.1993.tb02379.x

    Article  CAS  PubMed  Google Scholar 

  10. Raymond AA, Fish DR, Sisodiya SM, Alsanjari N, Stevens JM, Shorvon SD (1995) Abnormalities of gyration, heterotopias, tuberous sclerosis, focal cortical dysplasia, microdysgenesis, dysembryoplastic neuroepithelial tumour and dysgenesis of the archicortex in epilepsy. Clinical, EEG and neuroimaging features in 100 adult patients. Brain 118 ( Pt 3):629–60. https://doi.org/10.1093/brain/118.3.629

  11. Vossler DG, Lee JK, Ko TS (1999) Treatment of seizures in subcortical laminar heterotopia with corpus callosotomy and lamotrigine. J Child Neurol 14(5):282–288. https://doi.org/10.1177/088307389901400503

    Article  CAS  PubMed  Google Scholar 

  12. Bernasconi A, Martinez V, Rosa-Neto P, D’Agostino D, Bernasconi N, Berkovic S, MacKay M, Harvey AS, Palmini A, da Costa JC, Paglioli E, Kim HI, Connolly M, Olivier A, Dubeau F, Andermann E, Guerrini R, Whisler W, de Toledo-Morrell L, Morrell F, Andermann F (2001) Surgical resection for intractable epilepsy in “double cortex” syndrome yields inadequate results. Epilepsia 42(9):1124–1129. https://doi.org/10.1046/j.1528-1157.2001.39900.x

    Article  CAS  PubMed  Google Scholar 

  13. Russo GL, Tassi L, Cossu M, Cardinale F, Mai R, Castana L, Colombo N, Bramerio M (2003) Focal cortical resection in malformations of cortical development. Epileptic Disord 5(Suppl 2):S115–S123

    PubMed  Google Scholar 

  14. Kawai K, Shimizu H, Yagishita A, Maehara T, Tamagawa K (2004) Clinical outcomes after corpus callosotomy in patients with bihemispheric malformations of cortical development. J Neurosurg 101(1 Suppl):7–15. https://doi.org/10.3171/ped.2004.101.2.0007

    Article  PubMed  Google Scholar 

  15. Tai PC, McKean JD, Wheatley BM, Gross DW (2004) Surgical resection for intractable epilepsy in “double cortex” syndrome can yield adequate results. Epilepsia 45(5):562–3, author reply 563–4. https://doi.org/10.1111/j.0013-9580.2004.t01-2-62803.x

  16. Saito Y, Sugai K, Nakagawa E, Sakuma H, Komaki H, Sasaki M, Maegaki Y, Ohno K, Sato N, Kaneko Y, Otsuki, (2009) Treatment of epilepsy in severely disabled children with bilateral brain malformations. J Neurol Sci 277(1–2):37–49. https://doi.org/10.1016/j.jns.2008.10.009

    Article  PubMed  Google Scholar 

  17. Cukiert A, Mariani PP, Burattini JA, Cukiert CM, Forster C, Baise C, Argentoni-Baldochi M, Mello V (2009) Parkinsonism induced by VNS in a child with double-cortex syndrome. Epilepsia 50(12):2667–2669. https://doi.org/10.1111/j.1528-1167.2009.02255.x

    Article  PubMed  Google Scholar 

  18. Franco A, Pimentel J, Campos AR, Morgado C, Pinelo S, Ferreira AG, Bentes C (2016) Stimulation of the bilateral anterior nuclei of the thalamus in the treatment of refractory epilepsy: two cases of subcortical band heterotopia. Epileptic Disord 18(4):426–430. https://doi.org/10.1684/epd.2016.0878

    Article  PubMed  Google Scholar 

  19. Damiano JA, Do H, Ozturk E, Burgess R, Kalnins R, Jones NC, Dobrovic A, Berkovic SF, Hildebrand M (2017) Sensitive quantitative detection of somatic mosaic mutation in “double cortex” syndrome. Epileptic Disord 19(4):450–455. https://doi.org/10.1684/epd.2017.0944

    Article  PubMed  Google Scholar 

  20. von Wrede R, Moskau-Hartmann S, Rüber T, Helmstaedter C, Surges R (2019) Sustained seizure freedom with transcutaneous vagal nerve stimulation in drug-resistant epilepsy caused by subcortical band heterotopias. Seizure 70:25–26. https://doi.org/10.1016/j.seizure.2019.06.026

    Article  Google Scholar 

  21. Gilliam FG, Ssentongo P, Sather M, Kawasawa YI (2021) Case report: PAFAH1B1 mutation and posterior band heterotopia with focal temporal lobe epilepsy treated by responsive neurostimulation. Front Neurol 12:779113. https://doi.org/10.3389/fneur.2021.779113

    Article  PubMed  PubMed Central  Google Scholar 

  22. Matsuhashi A, Matsuo T, Kumada S (2022) Incremental changes in interhemispheric functional connectivity after two-stage corpus callosotomy in a patient with subcortical band heterotopia. Epilepsy Behav Rep 18:100525. https://doi.org/10.1016/j.ebr.2022.100525

    Article  PubMed  PubMed Central  Google Scholar 

  23. Engel J Jr, Ness V, Rassmussen TB, Ojemann LM (1993) Outcome with respect to epileptic seizures. In: Engel J (ed) Surgical treatment of the epilepsies, 2nd edn. Raven Press, New York, pp 609–621

    Google Scholar 

  24. Morrell F, Whisler WW, Bleck TP (1989) Multiple subpial transection: a new approach to the surgical treatment of focal epilepsy. J Neurosurg 70(2):231–239. https://doi.org/10.3171/jns.1989.70.2.0231

    Article  CAS  PubMed  Google Scholar 

  25. Smith MC (1998) Multiple subpial transection in patients with extratemporal epilepsy. Epilepsia 39(Suppl 4):S81–S89. https://doi.org/10.1111/j.1528-1157.1998.tb05128.x

    Article  PubMed  Google Scholar 

  26. Durnford AJ, Rodgers W, Kirkham FJ, Mullee MA, Whitney A, Prevett M, Kinton L, Harris M, Gray WP (2011) Very good inter-rater reliability of Engel and ILAE epilepsy surgery outcome classifications in a series of 76 patients. Seizure 20(10):809–812. https://doi.org/10.1016/j.seizure.2011.08.004

    Article  PubMed  Google Scholar 

  27. Hect JL, Alattar AA, Harford EE, Reecher H, Fernandes DT, Esplin N, McDowell M, Abel TJ (2022) Stereotactic laser interstitial thermal therapy for the treatment of pediatric drug-resistant epilepsy: indications, techniques, and safety. Childs Nerv Syst 38(5):961–970. https://doi.org/10.1007/s00381-022-05491-x

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Neurosurgery, Alder Hey Children’s NHS Foundation Trust, Liverpool, UK

    Arthur R. Kurzbuch, Ben Cooper & Jonathan R. Ellenbogen

  2. Department of Neurology, Alder Hey Children’s NHS Foundation Trust, Liverpool, UK

    Anil Israni

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  1. Arthur R. Kurzbuch
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Contributions

ARK: conception and design, acquisition of data, analysis and interpretation of data, drafting the article, approved the final version of the manuscript on behalf of all authors. BC: analysis and interpretation of data, critically revising the article. AI: analysis and interpretation of data, critically revising the article. JRE: conception and design, analysis and interpretation of data, critically revising the article.

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Correspondence to Arthur R. Kurzbuch.

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Kurzbuch, A.R., Cooper, B., Israni, A. et al. Non-pharmacological treatment options of drug-resistant epilepsy in subcortical band heterotopia: systematic review and illustrative case. Childs Nerv Syst 39, 451–462 (2023). https://doi.org/10.1007/s00381-022-05638-w

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