Sensorimotor outcomes after resection for perirolandic drug-resistant epilepsy: a systematic review and individual patient data meta-analysis

Nathan A. ShlobinDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, Illinois;

Search for other papers by Nathan A. Shlobin in
jns
Google Scholar
PubMed
Close
 BA
,
Andrew WangDepartment of Neurosurgery, David Geffen School of Medicine, University of California, Los Angeles, California;

Search for other papers by Andrew Wang in
jns
Google Scholar
PubMed
Close
 MS
,
H. Westley PhillipsDepartment of Neurosurgery, David Geffen School of Medicine, University of California, Los Angeles, California;

Search for other papers by H. Westley Phillips in
jns
Google Scholar
PubMed
Close
 MD
,
Han YanDivision of Neurosurgery, Hospital for Sick Children, Toronto, Ontario;

Search for other papers by Han Yan in
jns
Google Scholar
PubMed
Close
 MD
,
George M. IbrahimDivision of Neurosurgery, Hospital for Sick Children, Toronto, Ontario;

Search for other papers by George M. Ibrahim in
jns
Google Scholar
PubMed
Close
 MD, PhD
,
Lior M. ElkaimDivision of Neurology and Neurosurgery, McGill University, Montreal, Quebec, Canada;

Search for other papers by Lior M. Elkaim in
jns
Google Scholar
PubMed
Close
 MD
,
Shuang WangPediatric Epilepsy Center, Peking University First Hospital, Beijing, China;

Search for other papers by Shuang Wang in
jns
Google Scholar
PubMed
Close
 MD
,
Xiaoyan LiuPediatric Epilepsy Center, Peking University First Hospital, Beijing, China;

Search for other papers by Xiaoyan Liu in
jns
Google Scholar
PubMed
Close
 MD
,
Lixin CaiPediatric Epilepsy Center, Peking University First Hospital, Beijing, China;

Search for other papers by Lixin Cai in
jns
Google Scholar
PubMed
Close
 MD
,
Dang K. NguyenDivision of Neurology, University of Montreal Hospital Centre (CHUM), Montreal;
CHUM Research Centre, Montreal;
Department of Neuroscience, University of Montreal; and

Search for other papers by Dang K. Nguyen in
jns
Google Scholar
PubMed
Close
 MD, PhD
,
Aria FallahDepartment of Neurosurgery, David Geffen School of Medicine, University of California, Los Angeles, California;

Search for other papers by Aria Fallah in
jns
Google Scholar
PubMed
Close
 MD, MSc, FRCSC
, and
Alexander G. WeilDivision of Neurosurgery, Sainte-Justine University Hospital and University of Montreal Hospital Centre (CHUM), Montreal;
Department of Neuroscience, University of Montreal; and
Sainte-Justine Research Centre, University of Montreal, Quebec, Canada

Search for other papers by Alexander G. Weil in
jns
Google Scholar
PubMed
Close
 MD, FRCSC
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $525.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $624.00
USD  $45.00
USD  $525.00
USD  $624.00
Print or Print + Online Sign in

OBJECTIVE

The prevalence of long-term postoperative sensorimotor deficits in children undergoing perirolandic resective epilepsy surgery is unclear. The risk of developing these deficits must be weighed against the potential reduction in seizure frequency after surgery. In this study, the authors investigated the prevalence of sensorimotor deficits after resective surgery at ≥ 1 year postoperatively.

METHODS

A systematic review and individual patient data meta-analysis was conducted using PubMed, Embase, and Scopus databases. Subgroups of patients were identified and categorized according to their outcomes as follows: group A patients were denoted as seizure free with no postoperative sensorimotor deficits; group B patients experienced seizure recurrence with no deficit; group C patients were seizure free with deficits; and group D patients were not seizure free and with deficits. Rates of sensory deficits were examined in patients undergoing postcentral gyrus resection, and rates of motor deficits were aggregated in patients undergoing precentral gyrus resection.

RESULTS

Of 797 articles resulting from the database searches, 6 articles including 164 pediatric patients at a mean age of 7.7 ± 5.2 years with resection for drug-resistant perirolandic epilepsy were included in the study. Seizure freedom was observed in 118 (72.9%) patients at a mean follow-up of 3.4 ± 1.8 years. In total, 109 (66.5%) patients did not develop sensorimotor deficits at last follow-up, while 55 (33.5%) had permanent deficits. Ten (14.3%) of 70 patients with postcentral gyrus resection had permanent sensory deficits. Of the postcentral gyrus resection patients, 41 (58.6%) patients were included in group A, 19 (27.1%) in group B, 7 (10.0%) in group C, and 3 (4.3%) in group D. Forty (37.7%) of 106 patients with precentral resections had permanent motor deficits. Of the precentral gyrus resection patients, 50 (47.2%) patients were in group A, 16 (15.1%) in group B, 24 (22.6%) in group C, and 16 (15.1%) in group D. Patients without focal cortical dysplasia were more likely to have permanent motor deficits relative to those with focal cortical dysplasia in the precentral surgery cohort (p = 0.02).

CONCLUSIONS

In total, 58.6% of patients were seizure free without deficit, 27.1% were not seizure free and without deficit, 10.0% were seizure free but with deficit, and 4.3% were not seizure free and with deficit. Future studies with functional and quality-of-life data, particularly for patients who experience seizure recurrence with no deficits (as in group B in the present study) and those who are seizure free with deficits (as in group C) after treatment, are necessary to guide surgical decision-making.

ABBREVIATIONS

DRE = drug-resistant epilepsy; FCD = focal cortical dysplasia; IPD = individual patient data; IPDMA = IPD meta-analysis; MST = multiple subpial transection; pDRE = drug-resistant perirolandic epilepsy; RD = risk difference; RNS = responsive neurostimulation.
  • Collapse
  • Expand

Image from Tran et al. (pp 394–399).

  • 1

    Kwan P, Schachter SC, Brodie MJ. Drug-resistant epilepsy. N Engl J Med. 2011;365(10):919926.

  • 2

    Mohanraj R, Norrie J, Stephen LJ, Kelly K, Hitiris N, Brodie MJ. Mortality in adults with newly diagnosed and chronic epilepsy: a retrospective comparative study. Lancet Neurol. 2006;5(6):481487.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Lawn ND, Bamlet WR, Radhakrishnan K, O’Brien PC, So EL. Injuries due to seizures in persons with epilepsy: a population-based study. Neurology. 2004;63(9):15651570.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    McCagh J, Fisk JE, Baker GA. Epilepsy, psychosocial and cognitive functioning. Epilepsy Res. 2009;86(1):114.

  • 5

    Delev D, Send K, Wagner J, et al. Epilepsy surgery of the rolandic and immediate perirolandic cortex: surgical outcome and prognostic factors. Epilepsia. 2014;55(10):15851593.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Pondal-Sordo M, Diosy D, Téllez-Zenteno JF, Girvin JP, Wiebe S. Epilepsy surgery involving the sensory-motor cortex. Brain. 2006;129(Pt 12):33073314.

  • 7

    Ostergard TA, Miller JP. Surgery for epilepsy in the primary motor cortex: a critical review. Epilepsy Behav. 2019;91:1319.

  • 8

    de Oliveira RS, Santos MV, Terra VC, Sakamoto AC, Machado HR. Tailored resections for intractable rolandic cortex epilepsy in children: a single-center experience with 48 consecutive cases. Childs Nerv Syst. 2011;27(5):779785.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Gopinath S, Roy AG, Vinayan KP, et al. Seizure outcome following primary motor cortex-sparing resective surgery for perirolandic focal cortical dysplasia. Int J Surg. 2016;36(Pt B):466476.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Yan H, Toyota E, Anderson M, et al. A systematic review of deep brain stimulation for the treatment of drug-resistant epilepsy in childhood. J Neurosurg Pediatr. 2018;23(3):274284.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Shimizu T, Maehara T, Hino T, et al. Effect of multiple subpial transection on motor cortical excitability in cortical dysgenesis. Brain. 2001;124(Pt 7):13361349.

  • 12

    Singhal NS, Numis AL, Lee MB, et al. Responsive neurostimulation for treatment of pediatric drug-resistant epilepsy. Epilepsy Behav Case Rep. 2018;10:2124.

  • 13

    Kokoszka MA, Panov F, La Vega-Talbott M, McGoldrick PE, Wolf SM, Ghatan S. Treatment of medically refractory seizures with responsive neurostimulation: 2 pediatric cases. J Neurosurg Pediatr. 2018;21(4):421427.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71.

  • 15

    Shlobin NA, Moher D. Commentary: Preferred Reporting Items for Systematic Reviews and Meta-Analyses 2020 Statement: what neurosurgeons should know. Neurosurgery. 2021;89(5):E267E268.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    World Bank country and lending groups. World Bank. Accessed June 30, 2022. https://datahelpdesk.worldbank.org/knowledgebase/articles/906519-world-bank-country-and-lending-groups

    • Search Google Scholar
    • Export Citation
  • 17

    Burns PB, Rohrich RJ, Chung KC. The levels of evidence and their role in evidence-based medicine. Plast Reconstr Surg. 2011;128(1):305310.

  • 18

    Sterne JAC, Hernán MA, Reeves BC, et al. ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions. BMJ. 2016;355:i4919.

  • 19

    Behdad A, Limbrick DD Jr, Bertrand ME, Smyth MD. Epilepsy surgery in children with seizures arising from the rolandic cortex. Epilepsia. 2009;50(6):14501461.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Benifla M, Sala F Jr, Jane J Jr, et al. Neurosurgical management of intractable rolandic epilepsy in children: role of resection in eloquent cortex Clinical article. J Neurosurg Pediatr. 2009;4(3):199216.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Chen HH, Chen C, Hung SC, et al. Cognitive and epilepsy outcomes after epilepsy surgery caused by focal cortical dysplasia in children: early intervention maybe better. Childs Nerv Syst. 2014;30(11):18851895.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    DuanYu N, GuoJun Z, Liang Q, LiXin C, Tao Y, YongJie L. Surgery for perirolandic epilepsy: epileptogenic cortex resection guided by chronic intracranial electroencephalography and electric cortical stimulation mapping. Clin Neurol Neurosurg. 2010;112(2):110117.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Sandok EK, Cascino GD. Surgical treatment for perirolandic lesional epilepsy. Epilepsia. 1998;39(suppl 4):S42S48.

  • 24

    Wang S, Zhang H, Liu C, et al. Surgical treatment of children with drug-resistant epilepsy involving the Rolandic area. Epileptic Disord. 2021;23(2):376384.

  • 25

    Otsubo H, Chitoku S, Ochi A, et al. Malignant rolandic-sylvian epilepsy in children: diagnosis, treatment, and outcomes. Neurology. 2001;57(4):590596.

  • 26

    Tandon N, Tong BA, Friedman ER, et al. Analysis of morbidity and outcomes associated with use of subdural grids vs stereoelectroencephalography in patients with intractable epilepsy. JAMA Neurol. 2019;76(6):672681.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Jehi L, Morita-Sherman M, Love TE, et al. Comparative effectiveness of stereotactic electroencephalography versus subdural grids in epilepsy surgery. Ann Neurol. 2021;90(6):927939.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Mullin JP, Shriver M, Alomar S, et al. Is SEEG safe? A systematic review and meta-analysis of stereo-electroencephalography-related complications. Epilepsia. 2016;57(3):386401.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29

    Kovac S, Vakharia VN, Scott C, Diehl B. Invasive epilepsy surgery evaluation. Seizure. 2017;44:125136.

  • 30

    Podkorytova I, Hoes K, Lega B. Stereo-encephalography versus subdural electrodes for seizure localization. Neurosurg Clin N Am. 2016;27(1):97109.

  • 31

    Sacino MF, Huang SS, Schreiber J, Gaillard WD, Oluigbo CO. Is the use of stereotactic electroencephalography safe and effective in children? A meta-analysis of the use of stereotactic electroencephalography in comparison to subdural grids for invasive epilepsy monitoring in pediatric subjects. Neurosurgery. 2019;84(6):11901200.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Katz JS, Abel TJ. Stereoelectroencephalography versus subdural electrodes for localization of the epileptogenic zone: what is the evidence? Neurotherapeutics. 2019;16(1):5966.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Bjellvi J, Cross JH, Gogou M, et al. Classification of complications of epilepsy surgery and invasive diagnostic procedures: a proposed protocol and feasibility study. Epilepsia. 2021;62(11):26852696.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Seiam AHR, Dhaliwal H, Wiebe S. Determinants of quality of life after epilepsy surgery: systematic review and evidence summary. Epilepsy Behav. 2011;21(4):441445.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Macrodimitris S, Sherman EM, Williams TS, Bigras C, Wiebe S. Measuring patient satisfaction following epilepsy surgery. Epilepsia. 2011;52(8):14091417.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Shlobin NA, Sheldon M, Lam S. Informed consent in neurosurgery: a systematic review. Neurosurg Focus. 2020;49(5):E6.

  • 37

    Shlobin NA, Clark JR, Hoffman SC, Hopkins BS, Kesavabhotla K, Dahdaleh NS. Patient education in neurosurgery: part 1 of a systematic review. World Neurosurg. 2021;147:202214.e1.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Shlobin NA, Clark JR, Hoffman SC, Hopkins BS, Kesavabhotla K, Dahdaleh NS. Patient education in neurosurgery: part 2 of a systematic review. World Neurosurg. 2021;147:190201.e1.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Krishnaiah B, Ramaratnam S, Ranganathan LN. Subpial transection surgery for epilepsy. Cochrane Database Syst Rev. 2018;11:CD008153.

  • 40

    Ma BB, Fields MC, Knowlton RC, et al. Responsive neurostimulation for regional neocortical epilepsy. Epilepsia. 2020;61(1):96106.

  • 41

    Yan H, Ibrahim GM. Resective epilepsy surgery involving eloquent cortex in the age of responsive neurostimulation: a value-based decision-making framework. Epilepsy Behav. 2019;99:106479.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    Panov F, Ganaha S, Haskell J, et al. Safety of responsive neurostimulation in pediatric patients with medically refractory epilepsy. J Neurosurg Pediatr. 2020;26(5):525532.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Bercu MM, Friedman D, Silverberg A, et al. Responsive neurostimulation for refractory epilepsy in the pediatric population: a single-center experience. Epilepsy Behav. 2020;112:107389.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Nagahama Y, Zervos TM, Murata KK, et al. Real-world preliminary experience with responsive neurostimulation in pediatric epilepsy: a multicenter retrospective observational study. Neurosurgery. 2021;89(6):9971004.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45

    Englot DJ, Chang EF. Rates and predictors of seizure freedom in resective epilepsy surgery: an update. Neurosurg Rev. 2014;37(3):389405.

  • 46

    Matias CM, Sharan A, Wu C. Responsive neurostimulation for the treatment of epilepsy. Neurosurg Clin N Am. 2019;30(2):231242.

  • 47

    Shlobin NA, Rosenow JM. Ethical considerations in the implantation of neuromodulatory devices. Neuromodulation. 2022;25(2):P222P231.

  • 48

    Shlobin NA, Campbell JM, Rosenow JM, Rolston JD. Ethical considerations in the surgical and neuromodulatory treatment of epilepsy. Epilepsy Behav. 2022;127:108524.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 49

    McDonald PJ, Hrincu V, Connolly MB, et al. Novel neurotechnological interventions for pediatric drug-resistant epilepsy: physician perspectives. J Child Neurol. 2021;36(3):222229.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 50

    Fallah A. Moving beyond evidence-based medicine: incorporating patient values and preferences. Epilepsy Behav. 2015;53:209210.

  • 51

    Wiebe S, Wahby S, Lawal OA, et al. Development and validation of the Epilepsy Surgery Satisfaction Questionnaire (ESSQ-19). Epilepsia. 2020;61(12):27292738.

Metrics

All Time Past Year Past 30 Days
Abstract Views 807 807 72
Full Text Views 93 93 6
PDF Downloads 126 126 10
EPUB Downloads 0 0 0