Long-term motor deficit in brain tumour surgery with preserved intra-operative motor-evoked potentials
Tóm tắt
Muscle motor-evoked potentials are commonly monitored during brain tumour surgery in motor areas, as these are assumed to reflect the integrity of descending motor pathways, including the corticospinal tract. However, while the loss of muscle motor-evoked potentials at the end of surgery is associated with long-term motor deficits (muscle motor-evoked potential-related deficits), there is increasing evidence that motor deficit can occur despite no change in muscle motor-evoked potentials (muscle motor-evoked potential-unrelated deficits), particularly after surgery of non-primary regions involved in motor control. In this study, we aimed to investigate the incidence of muscle motor-evoked potential-unrelated deficits and to identify the associated brain regions. We retrospectively reviewed 125 consecutive patients who underwent surgery for peri-Rolandic lesions using intra-operative neurophysiological monitoring. Intraoperative changes in muscle motor-evoked potentials were correlated with motor outcome, assessed by the Medical Research Council scale. We performed voxel–lesion–symptom mapping to identify which resected regions were associated with short- and long-term muscle motor-evoked potential-associated motor deficits. Muscle motor-evoked potentials reductions significantly predicted long-term motor deficits. However, in more than half of the patients who experienced long-term deficits (12/22 patients), no muscle motor-evoked potential reduction was reported during surgery. Lesion analysis showed that muscle motor-evoked potential-related long-term motor deficits were associated with direct or ischaemic damage to the corticospinal tract, whereas muscle motor-evoked potential-unrelated deficits occurred when supplementary motor areas were resected in conjunction with dorsal premotor regions and the anterior cingulate. Our results indicate that long-term motor deficits unrelated to the corticospinal tract can occur more often than currently reported. As these deficits cannot be predicted by muscle motor-evoked potentials, a combination of awake and/or novel asleep techniques other than muscle motor-evoked potentials monitoring should be implemented.
Từ khóa
Tài liệu tham khảo
Amunts, 2015, Architectonic mapping of the human brain beyond Brodmann, Neuron, 88, 1086, 10.1016/j.neuron.2015.12.001
Andrews, 1996, Normative values for isometric muscle force measurements obtained with hand-held dynamometers, Phys Ther, 76, 248, 10.1093/ptj/76.3.248
Appollonio, 2005, The frontal assessment battery (FAB): normative values in an Italian population sample, Neurol Sci, 26, 108, 10.1007/s10072-005-0443-4
Baker, 2018, The crossed frontal aslant tract: a possible pathway involved in the recovery of supplementary motor area syndrome, Brain Behav, 8, e00926, 10.1002/brb3.926
Bannur, 2000, Post-operative supplementary motor area syndrome: clinical features and outcome, Br J Neurosurg, 14, 204, 10.1080/026886900408379
Bello, 2014, Tailoring neurophysiological strategies with clinical context enhances resection and safety and expands indications in gliomas involving motor pathways, Neuro Oncol, 16, 1110, 10.1093/neuonc/not327
Bulubas, 2016, Motor areas of the frontal cortex in patients with motor eloquent brain lesions, JNS, 125, 1431, 10.3171/2015.11.JNS152103
Cattaneo, 2020, Cortico-cortical connectivity between the superior and inferior parietal lobules and the motor cortex assessed by intraoperative dual cortical stimulation, Brain Stimul, 13, 819, 10.1016/j.brs.2020.02.023
Cisek, 2005, Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action, Neuron, 45, 801, 10.1016/j.neuron.2005.01.027
De Renzi, 1980, Imitating gestures: a quantitative approach to ideomotor apraxia, Arch Neurol, 37, 6, 10.1001/archneur.1980.00500500036003
Duffau, 2013, The ‘onco-functional balance’ in surgery for diffuse low-grade glioma: integrating the extent of resection with quality of life, Acta Neurochir, 155, 951, 10.1007/s00701-013-1653-9
Earhart, 2011, The 9-hole peg test of upper extremity function: average values, test-retest reliability, and factors contributing to performance in people with Parkinson disease, J Neurol Phys Ther, 35, 157, 10.1097/NPT.0b013e318235da08
Fontaine, 2002, Somatotopy of the supplementary motor area: evidence from correlation of the extent of surgical resection with the clinical patterns of deficit, Neurosurgery, 50, 297
Han, 2018, Subcortical stimulation mapping of descending motor pathways for perirolandic gliomas: assessment of morbidity and functional outcome in 702 cases, J Neurosurg, 131, 201, 10.3171/2018.3.JNS172494
Howells, 2020, The role of left fronto-parietal tracts in hand selection: evidence from neurosurgery, Cortex, 128, 297, 10.1016/j.cortex.2020.03.018
Howells, 2018, Frontoparietal tracts linked to lateralized hand preference and manual specialization, Cereb Cortex, 28, 2482, 10.1093/cercor/bhy040
Hubel, 2013, Computerized measures of finger tapping: effects of hand dominance, age, and sex, Percept Mot Skills, 116, 929, 10.2466/25.29.PMS.116.3.929-952
Joynt, 1962, Behavioral and pathological correlates of motor impersistence, Neurology, 12, 876, 10.1212/WNL.12.12.876
Kim, 2013, Risk factor analysis of the development of new neurological deficits following supplementary motor area resection: clinical article, JNS, 119, 7, 10.3171/2013.3.JNS121492
Kofler, 1999, Preserved motor evoked potentials fail to predict functional outcome in quadriplegia because of bilateral lesions of the supplementary motor areas: a brief report, Am. J. Phys. Med. Rehabil, 78, 66, 10.1097/00002060-199901000-00018
Krieg, 2012, Predictive value and safety of intraoperative neurophysiological monitoring with motor evoked potentials in glioma surgery, Neurosurgery, 70, 1060, 10.1227/NEU.0b013e31823f5ade
Laplane, 1977, Clinical consequences of corticectomies involving the supplementary motor area in man, J Neurol Sci, 34, 301, 10.1016/0022-510X(77)90148-4
Moser, 2017, Resection of navigated transcranial magnetic stimulation-positive prerolandic motor areas causes permanent impairment of motor function, Neurosurgery, 81, 99, 10.1093/neuros/nyw169
Nachev, 2008, Functional role of the supplementary and pre-supplementary motor areas, Nat Rev Neurosci, 9, 856, 10.1038/nrn2478
Nachev, 2005, Volition and conflict in human medial frontal cortex, Curr. Biol, 15, 122, 10.1016/j.cub.2005.01.006
Neuloh, 2004, Motor evoked potential monitoring with supratentorial surgery, Neurosurgery, 54, 1061, 10.1227/01.NEU.0000119326.15032.00
Neuloh, 2007, Motor tract monitoring during insular glioma surgery, JNS, 106, 582, 10.3171/jns.2007.106.4.582
Neuloh, 2009, Are there false-negative results of motor evoked potential monitoring in brain surgery?, Cen Eur Neurosurg, 70, 171, 10.1055/s-0029-1225651
Neuloh, 2004, Monitoring of motor evoked potentials compared with somatosensory evoked potentials and microvascular Doppler ultrasonography in cerebral aneurysm surgery, J Neurosurg, 100, 389, 10.3171/jns.2004.100.3.0389
Oldfield, 1971, The assessment and analysis of handedness: the Edinburgh inventory, Neuropsychologia, 9, 97, 10.1016/0028-3932(71)90067-4
Osoba, 1996, The development and psychometric validation of a brain cancer quality-of-life questionnaire for use in combination with general cancer-specific questionnaires, Qual Life Res, 5, 139, 10.1007/BF00435979
Penfield, 1937, Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation, Brain, 60, 389, 10.1093/brain/60.4.389
Raabe, 2014, Continuous dynamic mapping of the corticospinal tract during surgery of motor eloquent brain tumors: evaluation of a new method, J Neurosurg, 120, 1015, 10.3171/2014.1.JNS13909
Rahman, 2017, The effects of new or worsened postoperative neurological deficits on survival of patients with glioblastoma, J Neurosurg, 127, 123, 10.3171/2016.7.JNS16396
Rech, 2020, New insights into the neural foundations mediating movement/language interactions gained from intrasurgical direct electrostimulations, Brain Cogn, 142, 105583, 10.1016/j.bandc.2020.105583
Rojkova, 2016, Atlasing the frontal lobe connections and their variability due to age and education: a spherical deconvolution tractography study, Brain Struct Funct, 221, 1751, 10.1007/s00429-015-1001-3
Rossi, 2018, Assessment of the praxis circuit in glioma surgery to reduce the incidence of postoperative and long-term apraxia: a new intraoperative test, J Neurosurg, 130, 17, 10.3171/2017.7.JNS17357
Sala, 2000, Prognostic value of motor evoked potentials elicited by multipulse magnetic stimulation in a surgically induced transitory lesion of the supplementary motor area: a case report, J Neurol Neurosurg Psychiatry, 69, 828, 10.1136/jnnp.69.6.828
Seidel, 2018, Postoperative navigated transcranial magnetic stimulation to predict motor recovery after surgery of tumors located in motor eloquent areas, Neurosurgery, 65, 124, 10.1093/neuros/nyy303.306
Szelényi, 2010, Intraoperative motor evoked potential alteration in intracranial tumor surgery and its relation to signal alteration in postoperative magnetic resonance imaging, Neurosurgery, 67, 302, 10.1227/01.NEU.0000371973.46234.46
Taniguchi, 1993, Modification of cortical stimulation for motor evoked potentials under general anesthesia: technical description, Neurosurgery, 32, 219, 10.1227/00006123-199302000-00011
Tate, 2011, Assessment of morbidity following resection of cingulate gyrus gliomas: clinical article, JNS, 114, 640, 10.3171/2010.9.JNS10709
Townsend, 2006, Linear encoding of muscle activity in primary motor cortex and cerebellum, J Neurophysiol, 96, 2578, 10.1152/jn.01086.2005
Vergani, 2014, White matter connections of the supplementary motor area in humans, J Neurol Neurosurg Psychiatry, 85, 1377, 10.1136/jnnp-2013-307492
Weller, 2014, EANO guideline for the diagnosis and treatment of anaplastic gliomas and glioblastoma, Lancet Oncol, 15, e395, 10.1016/S1470-2045(14)70011-7
Wijnenga, 2018, The impact of surgery in molecularly defined low-grade glioma: an integrated clinical, radiological, and molecular analysis, Neuro Oncol, 20, 103, 10.1093/neuonc/nox176
Yushkevich, 2006, User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability, Neuroimage, 31, 1116, 10.1016/j.neuroimage.2006.01.015