Associations between clinical outcome and tractography based on navigated transcranial magnetic stimulation in patients with language-eloquent brain lesions

OBJECTIVENavigated transcranial magnetic stimulation (nTMS) in combination with diffusion tensor imaging fiber tracking (DTI FT) is increasingly used to locate subcortical language-related pathways. The aim of this study was to establish nTMS-based DTI FT for preoperative risk stratification by evaluating associations between lesion-to-tract distances (LTDs) and aphasia and by determining a cut-off LTD value to prevent surgery-related permanent aphasia.METHODSFifty patients with left-hemispheric, language-eloquent brain tumors underwent preoperative nTMS language mapping and nTMS-based DTI FT, followed by tumor resection. nTMS-based DTI FT was performed with a predefined fractional anisotropy (FA) of 0.10, 0.15, 50% of the individual FA threshold (FAT), and 75% FAT (minimum fiber length [FL]: 100 mm). The arcuate fascicle (AF), superior longitudinal fascicle (SLF), inferior longitudinal fascicle (ILF), uncinate fascicle (UC), and frontooccipital fascicle (FoF) were identified in nTMS-based tractography, and minimum LTDs were measured between the lesion and the AF and between the lesion and the closest other subcortical language-related pathway (SLF, ILF, UC, or FoF). LTDs were then associated with the level of aphasia (no/transient or permanent surgery-related aphasia, according to follow-up examinations).RESULTSA significant difference in LTDs was observed between patients with no or only surgery-related transient impairment and those who developed surgery-related permanent aphasia with regard to the AF (FA = 0.10, p = 0.0321; FA = 0.15, p = 0.0143; FA = 50% FAT, p = 0.0106) as well as the closest other subcortical language-related pathway (FA = 0.10, p = 0.0182; FA = 0.15, p = 0.0200; FA = 50% FAT, p = 0.0077). Patients with surgery-related permanent aphasia showed the lowest LTDs in relation to these tracts. Thus, LTDs of ≥ 8 mm (AF) and ≥ 11 mm (SLF, ILF, UC, or FoF) were determined as cut-off values for surgery-related permanent aphasia.CONCLUSIONSnTMS-based DTI FT of subcortical language-related pathways seems suitable for risk stratification and prediction in patients suffering from language-eloquent brain tumors. Thus, the current role of nTMS-based DTI FT might be expanded, going beyond the level of being a mere tool for surgical planning and resection guidance.

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Interhemispheric connectivity revealed by diffusion tensor imaging fiber tracking derived from navigated transcranial magnetic stimulation maps as a sign of language function at risk in patients with brain tumors

Journal of Neurosurgery ◽

10.3171/2016.1.jns152053 ◽

2017 ◽

Vol 126 (1) ◽

pp. 222-233 ◽

Cited By ~ 10

Author(s):

Nico Sollmann ◽

Chiara Negwer ◽

Lorena Tussis ◽

Theresa Hauck ◽

Sebastian Ille ◽

...

Keyword(s):

Diffusion Tensor Imaging ◽

Brain Tumors ◽

Magnetic Stimulation ◽

Diffusion Tensor ◽

Fiber Tracking ◽

Language Function ◽

Navigated Transcranial Magnetic Stimulation ◽

Language Mapping ◽

Interhemispheric Connectivity

OBJECTIVE Resection of brain tumors in language-eloquent areas entails the risk of postoperative aphasia. It has been demonstrated via navigated transcranial magnetic stimulation (nTMS) that language function can partially shift to the unaffected hemisphere due to tumor-induced plasticity. Therefore, this study was designed to evaluate whether interhemispheric connectivity (IC) detected by nTMS-based diffusion tensor imaging–fiber tracking (DTI-FT) can be used to predict surgery-related aphasia in patients with brain tumors. METHODS Thirty-eight patients with left-sided perisylvian brain lesions underwent cortical language mapping of both hemispheres by nTMS prior to awake surgery. Then, nTMS-based DTI-FT was conducted with a fractional anisotropy (FA) of 0.01 and 0.2 to visualize nTMS-based IC. Receiver operating characteristics were calculated for the prediction of a postoperative (irrespective of the preoperative state) and a new surgery-related aphasia by the presence of detectable IC. RESULTS Language mapping by nTMS was possible in all patients. Seventeen patients (44.7%) suffered from surgery-related worsening of language performance (transient aphasia according to 3-month follow-up in 16 subjects [42.1%]; new permanent aphasia according to 3-month follow-up in 1 patient [2.6%]). Regarding the correlation of aphasia to nTMS-based IC, statistically significant differences were revealed for both evaluated FA values. However, better results were observed for tractography with an FA of 0.2, which led to a specificity of 93% (postoperative aphasia) and 90% (surgery-related aphasia). For postoperative aphasia, the corresponding OR was 0.1282 (95% CI 0.0143–1.1520), and for surgery-related aphasia the OR was 0.1184 (95% CI 0.0208–0.6754). CONCLUSIONS According to these results, IC detected by preoperative nTMS-based DTI-FT might be regarded as a risk factor for surgery-related aphasia, with a specificity of up to 93%. However, because the majority of enrolled patients suffered from transient aphasia postoperatively, it has to be evaluated whether this approach distinctly leads to similar results among patients with permanent language deficits. Despite this restriction, this approach might contribute to individualized patient consultation prior to tumor resection in clinical practice.

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Preoperative language mapping by repetitive navigated transcranial magnetic stimulation and diffusion tensor imaging fiber tracking and their comparison to intraoperative stimulation

Neuroradiology ◽

10.1007/s00234-016-1685-y ◽

2016 ◽

Vol 58 (8) ◽

pp. 807-818 ◽

Cited By ~ 13

Author(s):

Nico Sollmann ◽

Antonia Kubitscheck ◽

Stefanie Maurer ◽

Sebastian Ille ◽

Theresa Hauck ◽

...

Keyword(s):

Diffusion Tensor Imaging ◽

Transcranial Magnetic Stimulation ◽

Magnetic Stimulation ◽

Diffusion Tensor ◽

Fiber Tracking ◽

Navigated Transcranial Magnetic Stimulation ◽

Language Mapping ◽

And Diffusion

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Pediatric navigated transcranial magnetic stimulation motor and language mapping combined with diffusion tensor imaging tractography: clinical experience

Journal of Neurosurgery Pediatrics ◽

10.3171/2020.4.peds20174 ◽

2020 ◽

Vol 26 (5) ◽

pp. 583-593

Author(s):

Tizian Rosenstock ◽

Thomas Picht ◽

Heike Schneider ◽

Peter Vajkoczy ◽

Ulrich-Wilhelm Thomale

Keyword(s):

Diffusion Tensor Imaging ◽

Transcranial Magnetic Stimulation ◽

Magnetic Stimulation ◽

Surgical Planning ◽

Diffusion Tensor ◽

Fiber Tracking ◽

Navigated Transcranial Magnetic Stimulation ◽

Language Mapping ◽

Eloquent Areas ◽

Dti Fiber Tracking

OBJECTIVEIn adults, navigated transcranial magnetic stimulation (nTMS) has been established as a preoperative examination method for brain tumors in motor- and language-eloquent locations. However, the clinical relevance of nTMS in children with brain tumors is still unclear. Here, the authors present their initial experience with nTMS-based surgical planning and family counseling in pediatric cases.METHODSThe authors analyzed the feasibility of nTMS and its influence on counseling and surgical strategy in a prospective study conducted between July 2017 and September 2019. The main inclusion criterion was a potential benefit from functional mapping data derived from nTMS and/or nTMS-enhanced tractography in pediatric patients who presented to the authors’ department prior to surgery for lesions close to motor- and/or speech-eloquent areas. The study was undertaken in 14 patients (median age 7 years, 8 males) who presented with different brain lesions.RESULTSMotor mapping combined with cortical seed area definition could be performed in 10 children (71%) to identify the corticospinal tract by additional diffusion tensor imaging (DTI). All motor mappings could be performed successfully without inducing relevant side effects. In 7 children, nTMS language mapping was performed to detect language-relevant cortical areas and DTI fiber tractography was performed to visualize the individual language network. nTMS examination was not possible in 4 children because of lack of compliance (n = 2), syncope (n = 1), and preexisting implant (n = 1). After successful mapping, the spatial relation between lesion and functional tissue was used for surgical planning in all 10 patients, and 9 children underwent nTMS-DTI integrated neuronavigation. No surgical complications or unexpected neurological deterioration was observed. In all successful nTMS cases, better function-based counseling was offered to the families. In 6 of 10 patients the surgical strategy was adapted according to nTMS data, and in 6 of 10 cases the extent of resection (EOR) was redefined.CONCLUSIONSnTMS and DTI fiber tracking were feasible for the majority of children. Presurgical counseling as well as surgical planning for the approach and EOR were improved by the nTMS examination results. nTMS in combination with DTI fiber tracking can be regarded as beneficial for neurosurgical procedures in eloquent areas in the pediatric population.

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Associations between clinical outcome and navigated transcranial magnetic stimulation characteristics in patients with motor-eloquent brain lesions: a combined navigated transcranial magnetic stimulation–diffusion tensor imaging fiber tracking approach

Journal of Neurosurgery ◽

10.3171/2016.11.jns162322 ◽

2018 ◽

Vol 128 (3) ◽

pp. 800-810 ◽

Cited By ~ 18

Author(s):

Nico Sollmann ◽

Noémie Wildschuetz ◽

Anna Kelm ◽

Neal Conway ◽

Tobias Moser ◽

...

Keyword(s):

Risk Assessment ◽

Diffusion Tensor Imaging ◽

Transcranial Magnetic Stimulation ◽

Brain Tumors ◽

Magnetic Stimulation ◽

Diffusion Tensor ◽

Fiber Tracking ◽

Low Grade ◽

Navigated Transcranial Magnetic Stimulation ◽

Resting Motor Threshold

OBJECTIVENavigated transcranial magnetic stimulation (nTMS) and diffusion tensor imaging fiber tracking (DTI FT) based on nTMS data are increasingly used for preoperative planning and resection guidance in patients suffering from motor-eloquent brain tumors. The present study explores whether nTMS-based DTI FT can also be used for individual preoperative risk assessment regarding surgery-related motor impairment.METHODSData derived from preoperative nTMS motor mapping and subsequent nTMS-based tractography in 86 patients were analyzed. All patients suffered from high-grade glioma (HGG), low-grade glioma (LGG), or intracranial metastasis (MET). In this context, nTMS-based DTI FT of the corticospinal tract (CST) was performed at a range of fractional anisotropy (FA) levels based on an individualized FA threshold ([FAT]; tracking with 50%, 75%, and 100% FAT), which was defined as the highest FA value allowing for visualization of fibers (100% FAT). Minimum lesion-to-CST distances were measured, and fiber numbers of the reconstructed CST were assessed. These data were then correlated with the preoperative, postoperative, and follow-up status of motor function and the resting motor threshold (rMT).RESULTSAt certain FA levels, a statistically significant difference in lesion-to-CST distances was observed between patients with HGG who had no impairment and those who developed surgery-related transient or permanent motor deficits (75% FAT: p = 0.0149; 100% FAT: p = 0.0233). In this context, no patient with a lesion-to-CST distance ≥ 12 mm suffered from any new surgery-related permanent paresis (50% FAT and 75% FAT). Furthermore, comparatively strong negative correlations were observed between the rMT and lesion-to-CST distances of patients with surgery-related transient paresis (Spearman correlation coefficient [rs]; 50% FAT: rs = –0.8660; 75% FAT: rs = –0.8660) or surgery-related permanent paresis (50% FAT: rs = –0.7656; 75% FAT: rs = –0.6763).CONCLUSIONSThis is one of the first studies to show a direct correlation between imaging, clinical status, and neurophysiological markers for the integrity of the motor system in patients with brain tumors. The findings suggest that nTMS-based DTI FT might be suitable for individual risk assessment in patients with HGG, in addition to being a surgery-planning tool. Importantly, necessary data for risk assessment were obtained without significant additional efforts, making this approach potentially valuable for direct clinical use.

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Distinct approaches to language pathway tractography: comparison of anatomy-based, repetitive navigated transcranial magnetic stimulation (rTMS)–based, and rTMS-enhanced diffusion tensor imaging–fiber tracking

Journal of Neurosurgery ◽

10.3171/2020.12.jns204028 ◽

2021 ◽

pp. 1-12

Author(s):

Luca L. Silva ◽

Mehmet S. Tuncer ◽

Peter Vajkoczy ◽

Thomas Picht ◽

Tizian Rosenstock

Keyword(s):

Diffusion Tensor Imaging ◽

Transcranial Magnetic Stimulation ◽

Magnetic Stimulation ◽

Clinical Utility ◽

Surgical Planning ◽

Diffusion Tensor ◽

Fiber Tracking ◽

Navigated Transcranial Magnetic Stimulation ◽

Language Mapping ◽

Language Pathways

OBJECTIVE Visualization of subcortical language pathways by means of diffusion tensor imaging–fiber tracking (DTI-FT) is evolving as an important tool for surgical planning and decision making in patients with language-suspect brain tumors. Repetitive navigated transcranial magnetic stimulation (rTMS) cortical language mapping noninvasively provides additional functional information. Efforts to incorporate rTMS data into DTI-FT are promising, but the lack of established protocols makes it hard to assess clinical utility. The authors performed DTI-FT of important language pathways by using five distinct approaches in an effort to evaluate the respective clinical usefulness of each approach. METHODS Thirty patients with left-hemispheric perisylvian lesions underwent preoperative rTMS language mapping and DTI. FT of the principal language tracts was conducted according to different strategies: Ia, anatomical landmark based; Ib, lesion-focused landmark based; IIa, rTMS based; IIb, rTMS based with postprocessing; and III, rTMS enhanced (based on a combination of structural and functional data). The authors analyzed the respective success of each method in revealing streamlines and conducted a multinational survey with expert clinicians to evaluate aspects of clinical utility. RESULTS The authors observed high usefulness and accuracy ratings for anatomy-based approaches (Ia and Ib). Postprocessing of rTMS-based tractograms (IIb) led to more balanced perceived information content but did not improve the usefulness for surgical planning and risk assessment. Landmark-based tractography (Ia and Ib) was most successful in delineating major language tracts (98% success), whereas rTMS-based tractography (IIa and IIb) frequently failed to reveal streamlines and provided less complete tractograms than the landmark-based approach (p < 0.001). The lesion-focused landmark-based (Ib) and the rTMS-enhanced (III) approaches were the most preferred methods. CONCLUSIONS The lesion-focused landmark-based approach (Ib) achieved the best ratings and enabled visualization of the principal language tracts in almost all cases. The rTMS-enhanced approach (III) was positively evaluated by the experts because it can reveal cortico-subcortical connections, but the functional relevance of these connections is still unclear. The use of regions of interest derived solely from cortical rTMS mapping (IIa and IIb) leads to cluttered images that are of limited use in clinical practice.

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Impairment of preoperative language mapping by lesion location: a functional magnetic resonance imaging, navigated transcranial magnetic stimulation, and direct cortical stimulation study

Journal of Neurosurgery ◽

10.3171/2014.10.jns141582 ◽

2015 ◽

Vol 123 (2) ◽

pp. 314-324 ◽

Cited By ~ 42

Author(s):

Sebastian Ille ◽

Nico Sollmann ◽

Theresa Hauck ◽

Stefanie Maurer ◽

Noriko Tanigawa ◽

...

Keyword(s):

Transcranial Magnetic Stimulation ◽

Positive Predictive Value ◽

Predictive Value ◽

Magnetic Stimulation ◽

Cortical Stimulation ◽

Awake Surgery ◽

Navigated Transcranial Magnetic Stimulation ◽

Language Mapping ◽

Direct Cortical Stimulation ◽

Neurosurgical Patients

OBJECT Language mapping by repetitive navigated transcranial magnetic stimulation (rTMS) is increasingly used and has already replaced functional MRI (fMRI) in some institutions for preoperative mapping of neurosurgical patients. Yet some factors affect the concordance of both methods with direct cortical stimulation (DCS), most likely by lesions affecting cortical oxygenation levels. Therefore, the impairment of the accuracy of rTMS and fMRI was analyzed and compared with DCS during awake surgery in patients with intraparenchymal lesions. METHODS Language mapping was performed by DCS, rTMS, and fMRI using an object-naming task in 27 patients with left-sided perisylvian lesions, and the induced language errors of each method were assigned to the cortical parcellation system. Subsequently, the receiver operating characteristics were calculated for rTMS and fMRI and compared with DCS as ground truth for regions with (w/) and without (w/o) the lesion in the mapped regions. RESULTS The w/ subgroup revealed a sensitivity of 100% (w/o 100%), a specificity of 8% (w/o 5%), a positive predictive value of 34% (w/o: 53%), and a negative predictive value (NPV) of 100% (w/o: 100%) for the comparison of rTMS versus DCS. Findings for the comparison of fMRI versus DCS within the w/ subgroup revealed a sensitivity of 32% (w/o: 62%), a specificity of 88% (w/o: 60%), a positive predictive value of 56% (w/o: 62%), and a NPV of 73% (w/o: 60%). CONCLUSIONS Although strengths and weaknesses exist for both rTMS and fMRI, the results show that rTMS is less affected by a brain lesion than fMRI, especially when performing mapping of language-negative cortical regions based on sensitivity and NPV.

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