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Closer to the Edge—The Value of Intraoperative Brain Mapping
Perspectives Commentary on: Intraoperative Subcortical Fiber Mapping with Subcortical-Cortical Evoked Potentials by Enatsu et al. World Neurosurg 86:478-483, 2016
Closer to the Edge—The Value of Intraoperative Brain Mapping Florian Roser1 and Marina Liebsch2
T
he article, “Intraoperative subcortical fiber mapping with subcortical-cortical evoked potentials,” is a highly valued contribution to the literature evaluating subcorticalcortical mapping in glioma surgery. It extends our knowledge in identifying motor cortical fiber tract integrity after resection of intrinsic brain tumors in eloquent areas. At present there is increasing amount of clinical and experimental data demonstrating various fiber tract identification either by imaging or by functional means. Recent studies have determined that complete resection of gliomas, even beyond contrast-enhancement, determines extent of survival more than any other treatment modality.1 Beyond the goal of radical resection, quality of life becomes the main determining factor for outcome analysis of our patients. In a sophisticated neurosurgical setup, numerous tools are available to achieve this goal, including navigation systems, intraoperative magnetic resonance imaging, awake surgery with intraoperative stimulation, fluorescence-guided surgery, or intraoperative neuromonitoring. Recently navigated transcranial magnetic stimulation (TMS)-based tractography of the corticospinal tract proved to be even more accurate and less operator dependent than standard techniques providing reliable anatomic and functional characterization of the motor pathway.2 However, among these modalities, continuous real-time monitoring of fiber tract integrity can be achieved only by electrophysiologic neuromonitoring. How can we combine our tools for the good of our patients? All of us have some experience in either method, or more than one, or even a combination. Recent studies demonstrate superiority when combining intraoperative treatment modalities.3 We might
Key words Arcuate fasciculus - Pyramidal tract - Subcortical stimulation - Subcortico-cortical evokedpotential -
Abbreviations and Acronyms MEP: Motor-evoked potential TMS: Transcranial magnetic stimulation
WORLD NEUROSURGERY 89: 689-691, MAY 2016
be tempted to use all tools to make resections safer. From the electrophysiologic point of view it is advisable to link and use as many application methods as possible in an operation scenario, to bundle as much functional information of corresponding brain areas in real-time. But, when combining intraoperative tools, we should be smart enough to understand the value of each of them and their added value in combination. In general monitoring gives us an almost continuous online feedback of the integrity of vulnerable neuronal structures or early registering of deteriorations to counteract. Strategically adapted to the surgical situation or procedure we can revert back to multimodal use of somatosensory-evoked potentials, motorevoked potentials (MEPs), brainstem auditory-evoked potentials, electroencephalography, or electromyelography. On the other hand, mapping means localization of functional neural structures, such as motor cortex, cranial nerve nuclei, or corticospinal tracts, to define secure borders of resection and preserve functional integrity. In this regard, negative mapping is as important for the detection of a missing function or a safe resection. For all intraoperative monitoring methods (especially cortical MEPs), it is important to create standardized and stable anesthetic conditions, to assign amplitudes and latency changes to surgical maneuvers, and not falsely interpret them due to changing anesthetic maneuvers (waiving boli, team communication deficits). Likewise, temperature, blood pressure, and several other vital signs should be kept constant or at least be included in the continuous assessment, as all can influence the development of electrophysiologic potentials independent from surgical manipulation. Intraoperative validations of monitoring
From the 1Department of Neurosurgery, Neurological Institute, Cleveland Clinic Abu Dhabi, UAE; and 2Department of Neurosurgery, University Hospital Tübingen, Tübingen, Germany To whom correspondence should be addressed: Florian Roser, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2016) 89:689-691. http://dx.doi.org/10.1016/j.wneu.2015.11.104
www.WORLDNEUROSURGERY.org
689
PERSPECTIVES
follow either the principle of amplitude reduction or latency delay, or can be associated with increasing stimulation thresholds.4,5
during awake surgeries, where plasticity of brain structures play an eminent role.
The integrity of the evoked potentials by transcranial motor stimulation derived from muscles of the periphery, face, or directly from the spinal cord (D-wave) gives us hints about the pyramidal tract and the precentral gyrus. Most important, we should not forget that even with the most dedicated conduction study, we measure and record only the function of a fraction of all fibers, the rapidly conducting ones. In addition, although MEP in spinal monitoring is assessed by the “all-or-nothing” principle, the assessment in cortical mapping is more difficult. Here not only tumor resection plays a role, so does the vascular situation of the respective tissue such as ischemia, coagulation of arterial feeders, or draining pathways.6
Of course, we all are striving to establish other techniques for patients who cannot undergo awake surgery. However, Enatsu et al still have to prove evidence of which fiber tracts they stimulated, in contrast to routine subcortical mapping where muscle responses are evidence of connectivity.
Ideally, direct cortical mapping should be done in 2 steps: phase reversal, followed by mapping of the precentral gyrus with identifying the hotspot for motor function. Therefore positive motor discharges with lower amplitude or discreetly prolonged latency can be detected from the supplemental motor cortex and the post central region, which is notably important for the decision-making process in the surgical strategy. At this point appropriate electrocorticography/electroencephalography during bipolar stimulation can be applied to identify and recognize early on the afterdischarges and seizures. More than a decade ago, direct cortical and subcortical monopolar mapping (train of five stimulation; 3e7 pulses; 500 Hz; maximum 25 mA) for identification of the motor cortex area (anodal stimulation) or subcortical fiber tracts (cathodal stimulation) was established and found widespread support.7
Because peripheral-stimulated somatosensory-evoked potentials are very prone to artifacts and the proposed technique by Enatsu et al reflects fiber stimulation close to the cortex, we doubt that this could be performed continuously. If not, it is very cumbersome. It can only be possible at the end of the resection and only to show a short static situation. More useful is the continuous dynamic monopolar subcortical stimulation, as advocated by Raabe et al,10 and implemented already into daily practice in many centers. One can get as close as 2 mm to the corticospinal tract with continuous dynamic stimulation, even with navigation of the stimulation probe.
One criticism of the presented data from Enatsu et al on subcortical-cortical stimulation is that the stimulation was performed with a grid at the end of resection and the distance validated with navigation performed before resection. We all know that in intra-axial tumor resection there can be significant brain shift after mass reduction, leading to inaccuracy of the navigation toward the end of the procedure. Therefore any estimation of distance to eloquent areas based on the navigation does not reflect reality. Language mapping and preservation of corresponding fiber tracts still represents a major challenge because of the complex network of language areas. Awake surgery and functional mapping, as the most established safest method, is not suitable for every patient due to clinical restraints or the patient’s psychologic profile. Repetetive TMS can help preoperatively to identify language-related areas, data that can be integrated into neuronavigation. Negative mapping points in the TMS can be used as safe negative targets intraoperatively. On the contrary, positive TMS language points, constituting preoperatively elicited deficits, are not necessarily associated with failure of function after resection. That would agree with the philosophy of Duffau8
REFERENCES 1. Hervey-Jumper SL, Berger MS. Role of surgical resection in low- and high-grade gliomas. Curr Treat Options Neurol. 2014;16:284. 2. Conti A, Raffa G, Granata F, Rizzo V, Germanò A, Tomasello F. Navigated transcranial magnetic
690
www.SCIENCEDIRECT.com
Likewise, Yamao et al9 use this technology after tumor removal, when applying single-pulse electrical stimulation to the white matter tract beneath the floor of the removal cavity to trace its connections to the language cortices. Assuming that they are stimulating the same pathways as in MEPs, but antidromically, the superiority of this method still has to be proven.
Neurosurgery, like no other surgical specialty, relies on the use of function observing techniques, with the vision not to leave any new neurological deficit after surgery in eloquent areas despite aiming for radicality of resection. This is why many methods are available at present. However, most still lack sufficient standardization to some extent. It is the general tendency in this fast-paced scientific world to be one of the first to present new theories and techniques, although they often might not be fully developed, described superficially, or reflect theories generated by a far too small number of cases. Many things certainly make sense from the scientific aspect; however, its routine use is often not feasible because of the excessive time required or lack of well-trained electrophysiologic staff to validate and interpret the highly scientific data in realtime. Equally important, is the willingness and patience of surgeons to respond to warnings, respecting inevitable intraoperative recovery periods. In addition, economic restrictions may apply. Time and safety issues, value redundancy, and lowering the operative effectiveness of the procedure should be taken into consideration when promoting a new technique. At present the method of choice to assess and localize, but also protect, the complex network of language from permanent damage continues to be mapping techniques in awake surgery.
stimulation for “somatotopic” tractography of the corticospinal tract. Neurosurgery. 2014;10(Suppl 4): 542-554. 3. Ille S, Sollmann N, Hauck T, Maurer S, Tanigawa N, Obermueller T, et al. Combined noninvasive language mapping by navigated transcranial magnetic stimulation and functional
MRI and its comparison with direct cortical stimulation. J Neurosurg. 2015;123:212-225. 4. Calancie B, Harris W, Brindle GF, Green BA, Landy HJ. Threshold-level repetitive transcranial electrical stimulation for intraoperative monitoring of central motor conduction. J Neurosurg. 2001;95(2 Suppl):161-168.
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2015.11.104
PERSPECTIVES
5. Szelényi A, Journée HL, Herrlich S, Galistu GM, van den Berg J, van Dijk JM. Experimental study of the course of threshold current, voltage and electrode impedance during stepwise stimulation from the skin surface to the human cortex. Brain Stimul. 2013;6:482-489. 6. Macdonald DB, Skinner S, Shils J, Yingling C. American Society of Neurophysiological Monitoring. Intraoperative motor evoked potential monitoring—a position statement by the American Society of Neurophysiological Monitoring. Clin Neurophysiol. 2013;124:2291-2316. 7. Kombos T, Suess O, Kern BC, Funk T, Hoell T, Kopetsch O, et al. Comparison between
monopolar and bipolar electrical stimulation of the motor cortex. Acta Neurochir (Wien). 1999;141: 1295-1301.
8. Duffau H. Awake mapping of the brain connectome in glioma surgery: concept is stronger than technology. Eur J Surg Oncol. 2015;41: 1261-1263.
9. Yamao Y, Matsumoto R, Kunieda T, Arakawa Y, Kobayashi K, Usami K, et al. Intraoperative dorsal language network mapping by using single-pulse electrical stimulation. Hum Brain Mapp. 2014;35: 4345-4361.
WORLD NEUROSURGERY 89: 689-691, MAY 2016
10. Raabe A, Beck J, Schucht P, Seidel K. Continuous dynamic mapping of the corticospinal tract during surgery of motor eloquent brain tumors: evaluation of a new method. J Neurosurg. 2014;120: 1015-1024.
Citation: World Neurosurg. (2016) 89:689-691. http://dx.doi.org/10.1016/j.wneu.2015.11.104 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
www.WORLDNEUROSURGERY.org
691
Closer to the Edge—The Value of Intraoperative Brain Mapping Florian Roser1 and Marina Liebsch2
T
he article, “Intraoperative subcortical fiber mapping with subcortical-cortical evoked potentials,” is a highly valued contribution to the literature evaluating subcorticalcortical mapping in glioma surgery. It extends our knowledge in identifying motor cortical fiber tract integrity after resection of intrinsic brain tumors in eloquent areas. At present there is increasing amount of clinical and experimental data demonstrating various fiber tract identification either by imaging or by functional means. Recent studies have determined that complete resection of gliomas, even beyond contrast-enhancement, determines extent of survival more than any other treatment modality.1 Beyond the goal of radical resection, quality of life becomes the main determining factor for outcome analysis of our patients. In a sophisticated neurosurgical setup, numerous tools are available to achieve this goal, including navigation systems, intraoperative magnetic resonance imaging, awake surgery with intraoperative stimulation, fluorescence-guided surgery, or intraoperative neuromonitoring. Recently navigated transcranial magnetic stimulation (TMS)-based tractography of the corticospinal tract proved to be even more accurate and less operator dependent than standard techniques providing reliable anatomic and functional characterization of the motor pathway.2 However, among these modalities, continuous real-time monitoring of fiber tract integrity can be achieved only by electrophysiologic neuromonitoring. How can we combine our tools for the good of our patients? All of us have some experience in either method, or more than one, or even a combination. Recent studies demonstrate superiority when combining intraoperative treatment modalities.3 We might
Key words Arcuate fasciculus - Pyramidal tract - Subcortical stimulation - Subcortico-cortical evokedpotential -
Abbreviations and Acronyms MEP: Motor-evoked potential TMS: Transcranial magnetic stimulation
WORLD NEUROSURGERY 89: 689-691, MAY 2016
be tempted to use all tools to make resections safer. From the electrophysiologic point of view it is advisable to link and use as many application methods as possible in an operation scenario, to bundle as much functional information of corresponding brain areas in real-time. But, when combining intraoperative tools, we should be smart enough to understand the value of each of them and their added value in combination. In general monitoring gives us an almost continuous online feedback of the integrity of vulnerable neuronal structures or early registering of deteriorations to counteract. Strategically adapted to the surgical situation or procedure we can revert back to multimodal use of somatosensory-evoked potentials, motorevoked potentials (MEPs), brainstem auditory-evoked potentials, electroencephalography, or electromyelography. On the other hand, mapping means localization of functional neural structures, such as motor cortex, cranial nerve nuclei, or corticospinal tracts, to define secure borders of resection and preserve functional integrity. In this regard, negative mapping is as important for the detection of a missing function or a safe resection. For all intraoperative monitoring methods (especially cortical MEPs), it is important to create standardized and stable anesthetic conditions, to assign amplitudes and latency changes to surgical maneuvers, and not falsely interpret them due to changing anesthetic maneuvers (waiving boli, team communication deficits). Likewise, temperature, blood pressure, and several other vital signs should be kept constant or at least be included in the continuous assessment, as all can influence the development of electrophysiologic potentials independent from surgical manipulation. Intraoperative validations of monitoring
From the 1Department of Neurosurgery, Neurological Institute, Cleveland Clinic Abu Dhabi, UAE; and 2Department of Neurosurgery, University Hospital Tübingen, Tübingen, Germany To whom correspondence should be addressed: Florian Roser, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2016) 89:689-691. http://dx.doi.org/10.1016/j.wneu.2015.11.104
www.WORLDNEUROSURGERY.org
689
PERSPECTIVES
follow either the principle of amplitude reduction or latency delay, or can be associated with increasing stimulation thresholds.4,5
during awake surgeries, where plasticity of brain structures play an eminent role.
The integrity of the evoked potentials by transcranial motor stimulation derived from muscles of the periphery, face, or directly from the spinal cord (D-wave) gives us hints about the pyramidal tract and the precentral gyrus. Most important, we should not forget that even with the most dedicated conduction study, we measure and record only the function of a fraction of all fibers, the rapidly conducting ones. In addition, although MEP in spinal monitoring is assessed by the “all-or-nothing” principle, the assessment in cortical mapping is more difficult. Here not only tumor resection plays a role, so does the vascular situation of the respective tissue such as ischemia, coagulation of arterial feeders, or draining pathways.6
Of course, we all are striving to establish other techniques for patients who cannot undergo awake surgery. However, Enatsu et al still have to prove evidence of which fiber tracts they stimulated, in contrast to routine subcortical mapping where muscle responses are evidence of connectivity.
Ideally, direct cortical mapping should be done in 2 steps: phase reversal, followed by mapping of the precentral gyrus with identifying the hotspot for motor function. Therefore positive motor discharges with lower amplitude or discreetly prolonged latency can be detected from the supplemental motor cortex and the post central region, which is notably important for the decision-making process in the surgical strategy. At this point appropriate electrocorticography/electroencephalography during bipolar stimulation can be applied to identify and recognize early on the afterdischarges and seizures. More than a decade ago, direct cortical and subcortical monopolar mapping (train of five stimulation; 3e7 pulses; 500 Hz; maximum 25 mA) for identification of the motor cortex area (anodal stimulation) or subcortical fiber tracts (cathodal stimulation) was established and found widespread support.7
Because peripheral-stimulated somatosensory-evoked potentials are very prone to artifacts and the proposed technique by Enatsu et al reflects fiber stimulation close to the cortex, we doubt that this could be performed continuously. If not, it is very cumbersome. It can only be possible at the end of the resection and only to show a short static situation. More useful is the continuous dynamic monopolar subcortical stimulation, as advocated by Raabe et al,10 and implemented already into daily practice in many centers. One can get as close as 2 mm to the corticospinal tract with continuous dynamic stimulation, even with navigation of the stimulation probe.
One criticism of the presented data from Enatsu et al on subcortical-cortical stimulation is that the stimulation was performed with a grid at the end of resection and the distance validated with navigation performed before resection. We all know that in intra-axial tumor resection there can be significant brain shift after mass reduction, leading to inaccuracy of the navigation toward the end of the procedure. Therefore any estimation of distance to eloquent areas based on the navigation does not reflect reality. Language mapping and preservation of corresponding fiber tracts still represents a major challenge because of the complex network of language areas. Awake surgery and functional mapping, as the most established safest method, is not suitable for every patient due to clinical restraints or the patient’s psychologic profile. Repetetive TMS can help preoperatively to identify language-related areas, data that can be integrated into neuronavigation. Negative mapping points in the TMS can be used as safe negative targets intraoperatively. On the contrary, positive TMS language points, constituting preoperatively elicited deficits, are not necessarily associated with failure of function after resection. That would agree with the philosophy of Duffau8
REFERENCES 1. Hervey-Jumper SL, Berger MS. Role of surgical resection in low- and high-grade gliomas. Curr Treat Options Neurol. 2014;16:284. 2. Conti A, Raffa G, Granata F, Rizzo V, Germanò A, Tomasello F. Navigated transcranial magnetic
690
www.SCIENCEDIRECT.com
Likewise, Yamao et al9 use this technology after tumor removal, when applying single-pulse electrical stimulation to the white matter tract beneath the floor of the removal cavity to trace its connections to the language cortices. Assuming that they are stimulating the same pathways as in MEPs, but antidromically, the superiority of this method still has to be proven.
Neurosurgery, like no other surgical specialty, relies on the use of function observing techniques, with the vision not to leave any new neurological deficit after surgery in eloquent areas despite aiming for radicality of resection. This is why many methods are available at present. However, most still lack sufficient standardization to some extent. It is the general tendency in this fast-paced scientific world to be one of the first to present new theories and techniques, although they often might not be fully developed, described superficially, or reflect theories generated by a far too small number of cases. Many things certainly make sense from the scientific aspect; however, its routine use is often not feasible because of the excessive time required or lack of well-trained electrophysiologic staff to validate and interpret the highly scientific data in realtime. Equally important, is the willingness and patience of surgeons to respond to warnings, respecting inevitable intraoperative recovery periods. In addition, economic restrictions may apply. Time and safety issues, value redundancy, and lowering the operative effectiveness of the procedure should be taken into consideration when promoting a new technique. At present the method of choice to assess and localize, but also protect, the complex network of language from permanent damage continues to be mapping techniques in awake surgery.
stimulation for “somatotopic” tractography of the corticospinal tract. Neurosurgery. 2014;10(Suppl 4): 542-554. 3. Ille S, Sollmann N, Hauck T, Maurer S, Tanigawa N, Obermueller T, et al. Combined noninvasive language mapping by navigated transcranial magnetic stimulation and functional
MRI and its comparison with direct cortical stimulation. J Neurosurg. 2015;123:212-225. 4. Calancie B, Harris W, Brindle GF, Green BA, Landy HJ. Threshold-level repetitive transcranial electrical stimulation for intraoperative monitoring of central motor conduction. J Neurosurg. 2001;95(2 Suppl):161-168.
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2015.11.104
PERSPECTIVES
5. Szelényi A, Journée HL, Herrlich S, Galistu GM, van den Berg J, van Dijk JM. Experimental study of the course of threshold current, voltage and electrode impedance during stepwise stimulation from the skin surface to the human cortex. Brain Stimul. 2013;6:482-489. 6. Macdonald DB, Skinner S, Shils J, Yingling C. American Society of Neurophysiological Monitoring. Intraoperative motor evoked potential monitoring—a position statement by the American Society of Neurophysiological Monitoring. Clin Neurophysiol. 2013;124:2291-2316. 7. Kombos T, Suess O, Kern BC, Funk T, Hoell T, Kopetsch O, et al. Comparison between
monopolar and bipolar electrical stimulation of the motor cortex. Acta Neurochir (Wien). 1999;141: 1295-1301.
8. Duffau H. Awake mapping of the brain connectome in glioma surgery: concept is stronger than technology. Eur J Surg Oncol. 2015;41: 1261-1263.
9. Yamao Y, Matsumoto R, Kunieda T, Arakawa Y, Kobayashi K, Usami K, et al. Intraoperative dorsal language network mapping by using single-pulse electrical stimulation. Hum Brain Mapp. 2014;35: 4345-4361.
WORLD NEUROSURGERY 89: 689-691, MAY 2016
10. Raabe A, Beck J, Schucht P, Seidel K. Continuous dynamic mapping of the corticospinal tract during surgery of motor eloquent brain tumors: evaluation of a new method. J Neurosurg. 2014;120: 1015-1024.
Citation: World Neurosurg. (2016) 89:689-691. http://dx.doi.org/10.1016/j.wneu.2015.11.104 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
www.WORLDNEUROSURGERY.org
691