Letter to the Editor. Navigated TMS in pediatric neurosurgery

Tizian RosenstockCharité–Universitätsmedizin Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
Berlin Institute of Health at Charité–Universitätsmedizin Berlin, BIH Biomedical Innovation Academy, Berlin, Germany

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Thomas PichtCharité–Universitätsmedizin Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
Cluster of Excellence: “Matters of Activity. Image Space Material,” Humboldt University, Berlin, Germany

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Ulrich-Wilhelm ThomaleCharité–Universitätsmedizin Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany

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TO THE EDITOR: With great interest, we read the retrospective study by Schramm et al.1 (Schramm S, Mehta A, Auguste KI, et al. Navigated transcranial magnetic stimulation mapping of the motor cortex for preoperative diagnostics in pediatric epilepsy. J Neurosurg Pediatr. 2021;28[3]:287-294), who reviewed their database from a single institution. Preoperative motor mapping with navigated transcranial magnetic stimulation (nTMS) has been well-studied in adults and its advantages have led to the establishment of nTMS mapping as a technique for preoperative workup.2 Studies on the application of nTMS in children are mostly consistent, although its application can be more challenging due to a potential lack of compliance and increased resting motor threshold in children, which was nicely elaborated by the authors. We strongly agree with the authors that patients with known epilepsy (and receiving antiepileptic medication) should also be studied for preoperative functional evaluation, although this was considered a contraindication in some previous reports.

In addition to the well-described experience of applying nTMS in pediatric neurosurgery, we would like to add previously published reports to further complete the well-elaborated discussion by Schramm et al. In a prospective study, our group investigated the use of nTMS motor and language mapping in children undergoing surgery in motor- and/or speech-eloquent areas.3 In addition to demonstrating the feasibility of nTMS in children, we combined this technique with nTMS-based tractography for preoperative planning (i.e., defining the optimal approach to avoid eloquent areas). The motor cortex and the corticospinal tract were analyzed for motor-eloquent lesions as well as language-eloquent cortical areas, together with the complex network of language tracts for language-associated lesions in neurooncology as well as for epilepsy surgery cases. The assessment not only impacted the surgical procedure in terms of intraoperative visualization and determining the extent of resection/surgical approach, but also improved the counseling and understanding of the surgical intervention for both the parents and the child.

In addition to the experience noted above, other published studies that evaluated the use of preoperative nTMS in children could be added.47 Two independent case reports of a 3-year old boy with a Rolandic ganglioglioma6 and a 6-year old boy with a left perisylvian tumor7 demonstrated the feasibility of nTMS motor and language mapping in children. In an observational study of 14 children, cortical language mapping was correlated with direct cortical stimulation (DCS), and heterogeneous agreement on sensitivity and specificity but high negative predictive value was found.4 Another study aimed to examine bilateral language processing in 3 children prior to an epilepsy surgical intervention.5 In addition to studies analyzing language representation, a publication in 2013 investigated a mixed cohort of children and adults with epilepsy and demonstrated the feasibility and reliability of nTMS motor mapping with suitable accuracy compared to invasive electrical stimulation.8 All studies investigating the use of nTMS exclusively in pediatric neurosurgical cases are summarized in Table 1.

TABLE 1.

Overview of pediatric nTMS studies

Authors & YearNo. of ChildrenObjectiveResults
Coburger et al., 201261nTMS motor mapping in a 3-year-old boy w/ a Rolandic ganglioglioma compared to DCSSuccessful nTMS motor mapping w/ high DCS agreement
Lehtinen et al., 2018414nTMS language mapping in children w/ epilepsy compared to DCSFeasible nTMS language mapping w/ heterogenous agreement but high negative predictive value of 95% compared to DCS
Rosenstock et al., 201971nTMS motor + language mapping + nTMS-based tractography of corticospinal tract & language network in a 6-year-old boy w/ lt perisylvian tumornTMS mapping + tractography supported surgical planning + intraop resection
Rejnö-Habte Selassie et al., 202053nTMS language mapping in 1 child w/ tumor & in 2 children w/ epilepsy-causing lesionsFeasible bihemispheric mapping of receptive language function in 2 of 3 children
Rosenstock et al., 2020314Children w/ brain tumors & epilepsy-causing lesions in motor-/language-eloquent area, w/ the same protocol as applied as Rosenstock et al., 2019,7 studyFeasible in 10 children (71%), not feasible in 4 children: lack of compliance (n = 2), syncope (n = 1), preexisting implant (n = 1); improved counseling in all cases; modified surgical strategy in 6 cases; adapted aimed extent of resection in 6 cases

We hope that we are adding further valuable published experiences to the presented discussion and would like to further emphasize that the algorithm presented by Schramm et al. is noteworthy for future development of nTMS in pediatric neurosurgery. The authors are to be congratulated for providing deep insight into the characteristics of nTMS motor mapping in children.

Acknowledgments

The authors acknowledge the support of the Cluster of Excellence: “Matters of Activity. Image Space Material” funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany’s Excellence Strategy (EXC 2025–390648296). Dr. Rosenstock is a participant in the BIH Charité Digital Clinician Scientist Program funded by the Charité–Universitätsmedizin Berlin and the Berlin Institute of Health at Charité (BIH).

References

  • 1

    Schramm S, Mehta A, Auguste KI, Tarapore PE. Navigated transcranial magnetic stimulation mapping of the motor cortex for preoperative diagnostics in pediatric epilepsy. J Neurosurg Pediatr. 2021;28(3):287294.

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  • 2

    Jeltema HR, Ohlerth AK, de Wit A, et al. Comparing navigated transcranial magnetic stimulation mapping and “gold standard” direct cortical stimulation mapping in neurosurgery: a systematic review. Neurosurg Rev. 2021;44(4):19031920.

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    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Rosenstock T, Picht T, Schneider H, Vajkoczy P, Thomale UW. Pediatric navigated transcranial magnetic stimulation motor and language mapping combined with diffusion tensor imaging tractography: clinical experience. J Neurosurg Pediatr. 2020;26(5):583593.

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

    Lehtinen H, Makela JP, Makela T, et al. Language mapping with navigated transcranial magnetic stimulation in pediatric and adult patients undergoing epilepsy surgery: comparison with extraoperative direct cortical stimulation. Epilepsia Open. 2018;3(2):224235.

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    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Rejnö-Habte Selassie G, Pegenius G, Karlsson T, Viggedal G, Hallböök T, Elam M. Cortical mapping of receptive language processing in children using navigated transcranial magnetic stimulation. Epilepsy Behav. 2020;103(Pt A):106836.

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

    Coburger J, Karhu J, Bittl M, Hopf NJ. First preoperative functional mapping via navigated transcranial magnetic stimulation in a 3-year-old boy. J Neurosurg Pediatr. 2012;9(6):660664.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7

    Rosenstock T, Picht T, Schneider H, Koch A, Thomale UW. Left perisylvian tumor surgery aided by TMS language mapping in a 6-year-old boy: case report. Childs Nerv Syst. 2019;35(1):175181.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8

    Vitikainen AM, Salli E, Lioumis P, Makela JP, Metsahonkala L. Applicability of nTMS in locating the motor cortical representation areas in patients with epilepsy. Acta Neurochir (Wien). 2013;155(3):507518.

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Severin SchrammKlinikum rechts der Isar, Technische Universität München, Munich, Germany

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Aashna MehtaBerkeley School of Public Health, University of California, Berkeley, CA

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Kurtis I. AugusteUniversity of California, San Francisco, CA

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Phiroz E. TaraporeUniversity of California, San Francisco, CA

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Response

We appreciate the letter by Rosenstock et al. regarding our previously published article, in which we retrospectively analyzed 16 pediatric cases that underwent nTMS motor mapping before epilepsy surgery.

In their letter, the authors provide a comprehensive overview of other instances of nTMS application for preoperative localization of cortical functions in pediatric patients. The authors reference previous studies on motor mapping in pediatric patients, citing two single case reports that include pediatric motor mapping in the context of tumor resection,1,2 as well as a recent study of 14 pediatric cases in which 10 partial to full motor mappings were achieved.3

In the context of our study, the case report by Coburger et al. provides an interesting perspective, due to the very young age of the mapped patient (3 years).2 The authors report that in pediatric patients, relatively high stimulation intensities may be required to elicit reliable motor evoked potentials (MEPs). In our own study, an analogous observation was made, with higher patient age correlating significantly with MEP elicitability. Both papers interpret their respective findings in the context of incomplete myelination within the developing brain. In response to the heightened requirements regarding stimulation intensity in the pediatric population, Coburger et al. made use of undirected motor preactivation by letting the patient play a video game to elicit MEPs more easily, which may provide an elegant way to enable motor mapping when it is otherwise not possible. Other potential avenues to facilitate MEP generation might be found in alternative nTMS protocols, such as paired-pulse approaches, which have shown promising results in adults.4

Another very important perspective on the topic of pediatric nTMS motor mapping is provided in the noted study of 14 clinical cases by Rosenstock et al.3 This report is very interesting due to its great detail on the further use of the data generated in nTMS mapping, such as for subsequent diffusion tensor imaging fiber tracking, surgical planning, and communication with patients and parents, aspects that were not the focus of our retrospective analysis. The authors report that in more than half of the cases in which mapping was obtained, the surgical procedure was adjusted due to the mapping results. This finding stresses the importance that accurate information of both cortical and subcortical function distribution can have for optimal clinical course management. We want to commend the authors for their detailed work in providing this insight to the wider community and thank them for the valuable commentary.

References

  • 1

    Rosenstock T, Picht T, Schneider H, Koch A, Thomale UW. Left perisylvian tumor surgery aided by TMS language mapping in a 6-year-old boy: case report. Childs Nerv Syst. 2019;35(1):175181.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2

    Coburger J, Karhu J, Bittl M, Hopf NJ. First preoperative functional mapping via navigated transcranial magnetic stimulation in a 3-year-old boy. J Neurosurg Pediatr. 2012;9(6):660664.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3

    Rosenstock T, Picht T, Schneider H, Vajkoczy P, Thomale UW. Pediatric navigated transcranial magnetic stimulation motor and language mapping combined with diffusion tensor imaging tractography: clinical experience. J Neurosurg Pediatr. 2020;26(5):583593.

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

    Sollmann N, Zhang H, Kelm A, et al. Paired-pulse navigated TMS is more effective than single-pulse navigated TMS for mapping upper extremity muscles in brain tumor patients. Clin Neurophysiol. 2020;131(12):28872898.

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    • PubMed
    • Search Google Scholar
    • Export Citation
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  • Expand

Figure from Candela-Cantó et al. (pp 61–70).

  • 1

    Schramm S, Mehta A, Auguste KI, Tarapore PE. Navigated transcranial magnetic stimulation mapping of the motor cortex for preoperative diagnostics in pediatric epilepsy. J Neurosurg Pediatr. 2021;28(3):287294.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2

    Jeltema HR, Ohlerth AK, de Wit A, et al. Comparing navigated transcranial magnetic stimulation mapping and “gold standard” direct cortical stimulation mapping in neurosurgery: a systematic review. Neurosurg Rev. 2021;44(4):19031920.

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

    Rosenstock T, Picht T, Schneider H, Vajkoczy P, Thomale UW. Pediatric navigated transcranial magnetic stimulation motor and language mapping combined with diffusion tensor imaging tractography: clinical experience. J Neurosurg Pediatr. 2020;26(5):583593.

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

    Lehtinen H, Makela JP, Makela T, et al. Language mapping with navigated transcranial magnetic stimulation in pediatric and adult patients undergoing epilepsy surgery: comparison with extraoperative direct cortical stimulation. Epilepsia Open. 2018;3(2):224235.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Rejnö-Habte Selassie G, Pegenius G, Karlsson T, Viggedal G, Hallböök T, Elam M. Cortical mapping of receptive language processing in children using navigated transcranial magnetic stimulation. Epilepsy Behav. 2020;103(Pt A):106836.

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

    Coburger J, Karhu J, Bittl M, Hopf NJ. First preoperative functional mapping via navigated transcranial magnetic stimulation in a 3-year-old boy. J Neurosurg Pediatr. 2012;9(6):660664.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7

    Rosenstock T, Picht T, Schneider H, Koch A, Thomale UW. Left perisylvian tumor surgery aided by TMS language mapping in a 6-year-old boy: case report. Childs Nerv Syst. 2019;35(1):175181.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8

    Vitikainen AM, Salli E, Lioumis P, Makela JP, Metsahonkala L. Applicability of nTMS in locating the motor cortical representation areas in patients with epilepsy. Acta Neurochir (Wien). 2013;155(3):507518.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 1

    Rosenstock T, Picht T, Schneider H, Koch A, Thomale UW. Left perisylvian tumor surgery aided by TMS language mapping in a 6-year-old boy: case report. Childs Nerv Syst. 2019;35(1):175181.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2

    Coburger J, Karhu J, Bittl M, Hopf NJ. First preoperative functional mapping via navigated transcranial magnetic stimulation in a 3-year-old boy. J Neurosurg Pediatr. 2012;9(6):660664.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3

    Rosenstock T, Picht T, Schneider H, Vajkoczy P, Thomale UW. Pediatric navigated transcranial magnetic stimulation motor and language mapping combined with diffusion tensor imaging tractography: clinical experience. J Neurosurg Pediatr. 2020;26(5):583593.

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

    Sollmann N, Zhang H, Kelm A, et al. Paired-pulse navigated TMS is more effective than single-pulse navigated TMS for mapping upper extremity muscles in brain tumor patients. Clin Neurophysiol. 2020;131(12):28872898.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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