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Comparison of navigated transcranial magnetic stimulation and functional magnetic resonance imaging for preoperative mapping in rolandic tumor surgery

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Abstract

Navigated transcranial magnetic stimulation (nTMS) is a novel tool for preoperative functional mapping. It detects eloquent cortical areas directly, comparable to intraoperative direct cortical stimulation (DCS). The aim of this study was to evaluate the advantage of nTMS in comparison with functional magnetic resonance imaging (fMRI) in the clinical setting. Special focus was placed on accuracy of motor cortex localization in patients with rolandic lesions. Thirty consecutive patients were enrolled in the study. All patients received an fMRI and nTMS examination preoperatively. Feasibility of the technique and spatial resolution of upper and lower extremity cortical mapping were compared with fMRI. Consistency of preoperative mapping with intraoperative DCS was assessed via the neuronavigation system. nTMS was feasible in all 30 patients. fMRI was impossible in 7 out of 30 patients with special clinical conditions, pediatric patients, central vascular lesions, or compliance issues. The mean accuracy to localize motor cortex of nTMS was higher than in fMRI. In the subgroup of intrinsic tumors, nTMS produced statistically significant higher accuracy scores of the lower extremity localization than fMRI. fMRI failed to localize hand or leg areas in 6 out of 23 cases. Using nTMS, a preoperative localization of the central sulcus was possible in all patients. Verification of nTMS motor cortex localization with DCS was achieved in all cases. The fMRI localization of the hand area proved to be postcentral in one case. nTMS has fewer restrictions for preoperative functional mapping than fMRI and requires only a limited level of compliance. nTMS scores higher on the accuracy scale than fMRI. nTMS represents a highly valuable supplement for the preoperative functional planning in the clinical routine.

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Acknowledgments

We thank Claudia Weissbach and Klarissa Belicke for performing neurophysiological recordings with outstanding motivation and enthusiasm.

Disclosure

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

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Authors and Affiliations

  1. Department of Neurosurgery, University of Ulm, Ludwig‐Heilmeyerstr. 2, 89312, Günzburg, Germany

    Jan Coburger

  2. Department of Neurosurgery, Klinikum Stuttgart, Kriegsbergstr. 60, 70174, Stuttgart, Germany

    Christian Musahl, Markus Bittl, Claudia Weissbach & Nikolai Hopf

  3. Department of Neuroradiology, Klinikum Stuttgart, Stuttgart, Germany

    Hans Henkes & Diana Horvath-Rizea

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  1. Jan Coburger
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  2. Christian Musahl
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Correspondence to Jan Coburger.

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Comments

Hugues Duffau, Montpellier, France

The authors compared navigated transcranial magnetic stimulation (nTMS) with preoperative functional magnetic resonance imaging (fMRI) and intraoperative direct cortical stimulation (DCS) to identify the primary motor cortex in a consecutive series of patients who underwent surgery for a lesion near or within the central region. They found that the cortical spatial resolution of nTMS was higher than of fMRI. Moreover, verification of nTMS motor cortex localization with DCS was achieved in all cases.

A very important message in this article is that nTMS was feasible in all cases, contrary to fMRI which was impossible in seven patients. Thus, preoperative nTMS may represent an interesting alternative to fMRI in pediatric, demented, or hemiplegic patients.

However, it is worth noting that, in this series, there were no significant differences between fMRI and nTMS. Therefore, the authors have to be cautious before to claim that the cortical spatial resolution of nTMS is higher than of fMRI, because this conclusion is not yet validated by their data. In addition, when Coburger et al. compared nTMS with DCS, they wrote that DCS had a cortical resolution of 10 mm within the gyrus, and that nTMS most likely had a very similar distribution. It is not totally true. Indeed, in glioma surgery, it was demonstrated that the combination of direct subcortical stimulation of the white matter pathways with DCS increased the spatial resolution, allowing an optimization of the resection until functional tracts have been encountered, with no margin [1, 2]. As a consequence, one should be aware about the impossibility for nTMS to perform subcortical mapping—which represents a main limitation in surgery for intra-axial brain tumor. This is the reason why it is dangerous to claim that “technically language mapping (using nTMS) similar to awake craniotomy is possible”, due to the fact that neural foundations of language are constituted by a subcortical connectivity which should absolutely be mapped and preserved intraoperatively because not able to be compensated when damaged [3, 4]. For all these reasons, intrasurgical direct electrical mapping remains the gold standard in glioma surgery, as recently demonstrated in a meta-analysis with more than 8,000 tumors [5].

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Matthias Krammer, Christianto B. Lumenta, Munich, Germany

This article is a good amendment to the existing literature dealing with the new method of navigated transcranial magnetic stimulation (nTMS) in comparison to functional MRI in patients with tumors in the rolandic area.

There are only few articles that describe the method of nTMS itself already.

The authors compare the two methods in 30 patients with very different benign and malignant tumors and vascular lesions. We think this is tolerable in such a paper that introduce a new method and is even necessary for further investigations. There exists up to date no articles with a bigger patient group. One problem is that it was not possible to perform fMRI in seven patients (23 %) due to compliance or other problems. This is a well-known problem of this method but makes statistical statements comparing the two methods in a patient group with 30 cases questionable.

The authors report about a patient where the fMRI showed the motor hand area postcentral and concluded that this is an error. According to the intraoperative control performed in this study with negative direct cortical stimulation this is really a false-positive localization. Kombos et al. (Acta Neurochir 799 (Wien) (1999) 141: 1295–1301) identified true functional motor areas 800 in the postcentral parietal location using direct monopolar and bipolar 801 stimulation results in 7.85 % few cases.

The authors report further about identification of the motor cortex even in hemiplegic patients. Do we look forward to get an improvement after tumor resection? This could be possible in our opinion in a hemiparetic patient and in hemiplegic patients with motor function improvement after antiedematous therapy, but in really hemiplegic patients? Is the surgical procedure in this case the same for infiltrating tumors in comparison to, e.g., meningioma? Do the authors stop tumor resection in a true hemiplegic patient with a glioblastoma when they reach the identified motor cortex and there is still vital and visible tumor?

Although it is not part of this study, we think that the most important tools for surgery in the rolandic area are the neurophysiological methods looking for the central sulcus with the phase reversal, direct cortical, and subcortical stimulation. Independent from the cortical localization of a tumor, it is also important during the resection to save the subcortical pathways. In opposite to nTMS, subcortical pathways could be identified by fMRI and MRI-DTI. A good new method is the combination of nTMS and DTI using the nTMS motor cortex region as starting point for the DTI generation.

Christopher Nimsky, Marburg, Germany

Preoperative functional mapping is an important part of preoperative planning and decision making in lesions close to eloquent brain areas. Magnetoencephalography (MEG) and functional magnetic resonance imaging (fMRI) were among the first techniques to identify these eloquent brain areas. Despite having different physical principles being the bases of these methods, a quite reliable identification of the motor cortex or language-related areas is possible. fMRI has the advantage to be widely available; however, the method is not able to identify the proper structures in all cases, so some groups prefer to combine the results of fMRI and MEG. The authors demonstrate the application of navigated transcranial magnetic stimulation (nTMS) and could show that it had fewer restrictions than fMRI in their series to identify the motor cortex. So potentially nTMS might also be an alternative for MEG, which is measuring the electrical activity directly, in contrast to fMRI measuring oxygen consumption. It will be interesting to see, whether nTMS will also be able to localize speech relevant areas, which might be even more interesting in a clinical setting.

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Coburger, J., Musahl, C., Henkes, H. et al. Comparison of navigated transcranial magnetic stimulation and functional magnetic resonance imaging for preoperative mapping in rolandic tumor surgery. Neurosurg Rev 36, 65–76 (2013). https://doi.org/10.1007/s10143-012-0413-2

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  • DOI: https://doi.org/10.1007/s10143-012-0413-2

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