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Long-term efficacy and cognitive effects of bilateral hippocampal deep brain stimulation in patients with drug-resistant temporal lobe epilepsy

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Abstract

Purpose

Temporal lobe epilepsy patients treated with hippocampal deep brain stimulation (Hip-DBS) have rarely been reported before. Preoperative and postoperative cognitive function is seldom analyzed.

Methods

Seven patients with drug-resistant temporal lobe epilepsy were included in this study. Bilateral Hip-DBS was performed in these patients. The stimulator was activated 1 month after the implantation. Then, the patients returned for further adjustments 4 months after the surgery and reprogramming every year. The seizure frequency, Wechsler Adult Intelligence Scale-IV, and Wechsler memory scale-IV were assessed blindly as the outcomes at each follow-up.

Results

After a mean 48-month follow-up, the mean seizure frequency significantly decreased (p = 0.011, paired t test; decrease of 78.1%). One patient (14.3%) was seizure-free by the last follow-up; six of seven (85.7%) patients had reductions in seizure frequency of at least 50%; one patient (14.3%) who did not comply with the antiepileptic drug instructions had a less than 50% reduction in seizure frequency. In addition, there were no significant decreases in intelligence or verbal and visual memory from baseline to the last follow-up (p = 0.736, paired t test; p = 0.380, paired t test, respectively).

Conclusion

Hip-DBS could provide acceptable long-term efficacy and safety. For patients with drug-resistant temporal lobe epilepsy who are not suitable for resective surgery, Hip-DBS could become a potential therapeutic option.

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Abbreviations

AED:

Antiepileptic drug

DBS:

Deep brain stimulation

ANT-DBS:

Anterior nucleus thalamus deep brain stimulation

Hip-DBS:

Hippocampal deep brain stimulation

SPS:

Simple partial seizures

CPS:

Complex partial seizures

GTCS:

Generalized tonic-clonic seizures

WAIS-IV:

Wechsler Adult Intelligence Scale-IV

WMS-IV:

Wechsler Memory Scale-IV

FSIQ:

Full-Scale Intelligence Quotient

FSMQ:

Full-Scale Memory Quotient

AMI:

Auditory Memory Index

VMI:

Visual Memory Index

MTS:

Mesial temporal sclerosis

References

  1. Forsgren L, Beghi E, Oun A, Sillanpaa M (2005) The epidemiology of epilepsy in Europe - a systematic review. Eur J Neurol 12(4):245–253. https://doi.org/10.1111/j.1468-1331.2004.00992.x

    Article  CAS  PubMed  Google Scholar 

  2. Sander JW, Shorvon SD (1996) Epidemiology of the epilepsies. J Neurol Neurosurg Psychiatry 61(5):433–443. https://doi.org/10.1136/jnnp.61.5.433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Kwan P, Brodie MJ (2000) Early identification of refractory epilepsy. N Engl J Med 342(5):314–319. https://doi.org/10.1056/nejm200002033420503

    Article  CAS  PubMed  Google Scholar 

  4. Zaccara G, Citerio G, Del Gaudio A, Ferlisi M, Pugliese FR, Toni D (2020) Clinical pathways of epileptic seizures and status epilepticus: results from a survey in Italy. Neurol Sci 41:1571–1575. https://doi.org/10.1007/s10072-020-04270-3

    Article  PubMed  PubMed Central  Google Scholar 

  5. Marson AG, Al-Kharusi AM, Alwaidh M, Appleton R, Baker GA, Chadwick DW, Cramp C, Cockerell OC, Cooper PN, Doughty J, Eaton B, Gamble C, Goulding PJ, Howell SJ, Hughes A, Jackson M, Jacoby A, Kellett M, Lawson GR, Leach JP, Nicolaides P, Roberts R, Shackley P, Shen J, Smith DF, Smith PE, Smith CT, Vanoli A, Williamson PR (2007) The SANAD study of effectiveness of valproate, lamotrigine, or topiramate for generalised and unclassifiable epilepsy: an unblinded randomised controlled trial. Lancet 369(9566):1016–1026. https://doi.org/10.1016/s0140-6736(07)60461-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Tellez-Zenteno JF, Dhar R, Wiebe S (2005) Long-term seizure outcomes following epilepsy surgery: a systematic review and meta-analysis. Brain 128(Pt 5):1188–1198. https://doi.org/10.1093/brain/awh449

    Article  PubMed  Google Scholar 

  7. Kapur N, Prevett M (2003) Unexpected amnesia: are there lessons to be learned from cases of amnesia following unilateral temporal lobe surgery? Brain 126(Pt 12):2573–2585. https://doi.org/10.1093/brain/awg275

    Article  PubMed  Google Scholar 

  8. Helmstaedter C, Kurthen M, Lux S, Reuber M, Elger CE (2003) Chronic epilepsy and cognition: a longitudinal study in temporal lobe epilepsy. Ann Neurol 54(4):425–432. https://doi.org/10.1002/ana.10692

    Article  PubMed  Google Scholar 

  9. Cukiert A, Cukiert CM, Burattini JA, Mariani PP, Bezerra DF (2017) Seizure outcome after hippocampal deep brain stimulation in patients with refractory temporal lobe epilepsy: a prospective, controlled, randomized, double-blind study. Epilepsia 58(10):1728–1733. https://doi.org/10.1111/epi.13860

    Article  PubMed  Google Scholar 

  10. Mesraoua B, Deleu D, Al Hail H, Melikyan G, Boon P, Haider HA, Asadi-Pooya AA (2019) Electroencephalography in epilepsy: look for what could be beyond the visual inspection. Neurol Sci 40(11):2287–2291. https://doi.org/10.1007/s10072-019-04026-8

    Article  PubMed  Google Scholar 

  11. Ashraf-Ganjouei A, Rahmani F, Aarabi MH, Sanjari Moghaddam H, Nazem-Zadeh MR, Davoodi-Bojd E, Soltanian-Zadeh H (2019) White matter correlates of disease duration in patients with temporal lobe epilepsy: updated review of literature. Neurol Sci 40(6):1209–1216. https://doi.org/10.1007/s10072-019-03818-2

    Article  PubMed  Google Scholar 

  12. Cukiert A, Cukiert CM, Burattini JA, Lima AM (2014) Seizure outcome after hippocampal deep brain stimulation in a prospective cohort of patients with refractory temporal lobe epilepsy. Seizure 23(1):6–9. https://doi.org/10.1016/j.seizure.2013.08.005

    Article  PubMed  Google Scholar 

  13. Li MCH, Cook MJ (2018) Deep brain stimulation for drug-resistant epilepsy. Epilepsia 59(2):273–290. https://doi.org/10.1111/epi.13964

    Article  PubMed  Google Scholar 

  14. Fisher R, Salanova V, Witt T, Worth R, Henry T, Gross R, Oommen K, Osorio I, Nazzaro J, Labar D, Kaplitt M, Sperling M, Sandok E, Neal J, Handforth A, Stern J, DeSalles A, Chung S, Shetter A, Bergen D, Bakay R, Henderson J, French J, Baltuch G, Rosenfeld W, Youkilis A, Marks W, Garcia P, Barbaro N, Fountain N, Bazil C, Goodman R, McKhann G, Babu Krishnamurthy K, Papavassiliou S, Epstein C, Pollard J, Tonder L, Grebin J, Coffey R, Graves N (2010) Electrical stimulation of the anterior nucleus of thalamus for treatment of refractory epilepsy. Epilepsia 51(5):899–908. https://doi.org/10.1111/j.1528-1167.2010.02536.x

    Article  Google Scholar 

  15. Morrell MJ (2011) Responsive cortical stimulation for the treatment of medically intractable partial epilepsy. Neurology 77(13):1295–1304. https://doi.org/10.1212/WNL.0b013e3182302056

    Article  PubMed  Google Scholar 

  16. McLachlan RS, Pigott S, Tellez-Zenteno JF, Wiebe S, Parrent A (2010) Bilateral hippocampal stimulation for intractable temporal lobe epilepsy: impact on seizures and memory. Epilepsia 51(2):304–307. https://doi.org/10.1111/j.1528-1167.2009.02332.x

    Article  PubMed  Google Scholar 

  17. Jin H, Li W, Dong C, Wu J, Zhao W, Zhao Z, Ma L, Ma F, Chen Y, Liu Q (2016) Hippocampal deep brain stimulation in nonlesional refractory mesial temporal lobe epilepsy. Seizure 37:1–7. https://doi.org/10.1016/j.seizure.2016.01.018

    Article  CAS  PubMed  Google Scholar 

  18. Min B, Guoming L, Jian Z (2013) Treatment of mesial temporal lobe epilepsy with amygdalohippocampal stimulation: a case series and review of the literature. Exp Ther Med 5(4):1264–1268. https://doi.org/10.3892/etm.2013.968

    Article  PubMed  PubMed Central  Google Scholar 

  19. Vonck K, Boon P, Achten E, De Reuck J, Caemaert J (2002) Long-term amygdalohippocampal stimulation for refractory temporal lobe epilepsy. Ann Neurol 52(5):556–565. https://doi.org/10.1002/ana.10323

    Article  PubMed  Google Scholar 

  20. Tellez-Zenteno JF, McLachlan RS, Parrent A, Kubu CS, Wiebe S (2006) Hippocampal electrical stimulation in mesial temporal lobe epilepsy. Neurology 66(10):1490–1494. https://doi.org/10.1212/01.wnl.0000209300.49308.8f

    Article  CAS  PubMed  Google Scholar 

  21. Boex C, Seeck M, Vulliemoz S, Rossetti AO, Staedler C, Spinelli L, Pegna AJ, Pralong E, Villemure JG, Foletti G, Pollo C (2011) Chronic deep brain stimulation in mesial temporal lobe epilepsy. Seizure 20(6):485–490. https://doi.org/10.1016/j.seizure.2011.03.001

    Article  PubMed  Google Scholar 

  22. Velasco AL, Velasco F, Velasco M, Jimenez F, Carrillo-Ruiz JD, Castro G (2007) The role of neuromodulation of the hippocampus in the treatment of intractable complex partial seizures of the temporal lobe. Acta Neurochir Suppl 97(Pt 2):329–332. https://doi.org/10.1007/978-3-211-33081-4_36

    Article  CAS  PubMed  Google Scholar 

  23. Boon P, Vonck K, De Herdt V, Van Dycke A, Goethals M, Goossens L, Van Zandijcke M, De Smedt T, Dewaele I, Achten R, Wadman W, Dewaele F, Caemaert J, Van Roost D (2007) Deep brain stimulation in patients with refractory temporal lobe epilepsy. Epilepsia 48(8):1551–1560. https://doi.org/10.1111/j.1528-1167.2007.01005.x

    Article  PubMed  Google Scholar 

  24. Proposal for revised clinical and electroencephalographic classification of epileptic seizures. From the Commission on Classification and Terminology of the International League Against Epilepsy (1981). Epilepsia 22 (4):489–501. https://doi.org/10.1111/j.1528-1157.1981.tb06159.x

  25. Luders H, Acharya J, Baumgartner C, Benbadis S, Bleasel A, Burgess R, Dinner DS, Ebner A, Foldvary N, Geller E, Hamer H, Holthausen H, Kotagal P, Morris H, Meencke HJ, Noachtar S, Rosenow F, Sakamoto A, Steinhoff BJ, Tuxhorn I, Wyllie E (1998) Semiological seizure classification. Epilepsia 39(9):1006–1013. https://doi.org/10.1111/j.1528-1157.1998.tb01452.x

    Article  CAS  PubMed  Google Scholar 

  26. Piacentino M, Beggio G, Zordan L, Bonanni P (2018) Hippocampal deep brain stimulation: persistent seizure control after bilateral extra-cranial electrode fracture. Neurol Sci 39(8):1431–1435. https://doi.org/10.1007/s10072-018-3444-9

    Article  PubMed  Google Scholar 

  27. Tramoni-Negre E, Lambert I, Bartolomei F, Felician O (2017) Long-term memory deficits in temporal lobe epilepsy. Rev Neurol (Paris) 173(7–8):490–497. https://doi.org/10.1016/j.neurol.2017.06.011

    Article  CAS  Google Scholar 

  28. Menlove L, Reilly C (2015) Memory in children with epilepsy: a systematic review. Seizure 25:126–135. https://doi.org/10.1016/j.seizure.2014.10.002

    Article  PubMed  Google Scholar 

  29. Stroup E, Langfitt J, Berg M, McDermott M, Pilcher W, Como P (2003) Predicting verbal memory decline following anterior temporal lobectomy (ATL). Neurology 60(8):1266–1273. https://doi.org/10.1212/01.wnl.0000058765.33878.0d

    Article  CAS  PubMed  Google Scholar 

  30. Dulay MF, York MK, Soety EM, Hamilton WJ, Mizrahi EM, Goldsmith IL, Verma A, Grossman RG, Yoshor D, Armstrong DD, Levin HS (2006) Memory, emotional and vocational impairments before and after anterior temporal lobectomy for complex partial seizures. Epilepsia 47(11):1922–1930. https://doi.org/10.1111/j.1528-1167.2006.00812.x

    Article  PubMed  Google Scholar 

  31. Martin RC, Sawrie SM, Roth DL, Gilliam FG, Faught E, Morawetz RB, Kuzniecky R (1998) Individual memory change after anterior temporal lobectomy: a base rate analysis using regression-based outcome methodology. Epilepsia 39(10):1075–1082. https://doi.org/10.1111/j.1528-1157.1998.tb01293.x

    Article  CAS  PubMed  Google Scholar 

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Author information

Authors and Affiliations

Authors

Contributions

Shu Wang: Finish the manuscript, data analysis.

Meng Zhao: Revision, data collation.

Tianfu Li: Select patients, assessment of the scale.

Chunsheng Zhang: Follow-up, data collation.

Jian Zhou: Revision, data collation.

Mengyang Wang: Select patients, assessment of the scale.

Xiongfei Wang: Revision, data collation.

Kaiqiang Ma: Follow-up, data collation.

Guoming Luan: Team leader, Revision, select patients.

Yuguang Guan: Team leader, Revision, select patients.

Corresponding author

Correspondence to Yuguang Guan.

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The authors declare that they have no conflict of interest.

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None.

Research ethics

The local ethics committee approved this study. Written informed consent was provided by the patients or their guardians. All patients agreed to the procedure and to the use of their anonymized data for research purposes. This study was conducted following the 1964 Helsinki Declaration and its later amendments.

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Wang, S., Zhao, M., Li, T. et al. Long-term efficacy and cognitive effects of bilateral hippocampal deep brain stimulation in patients with drug-resistant temporal lobe epilepsy. Neurol Sci 42, 225–233 (2021). https://doi.org/10.1007/s10072-020-04554-8

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  • DOI: https://doi.org/10.1007/s10072-020-04554-8

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