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Functional Recovery After Surgical Resection of Low Grade Gliomas In J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.74.7.901 on 1 July 2003. Downloaded from 901 PAPER Functional recovery after surgical resection of low grade gliomas in eloquent brain: hypothesis of brain compensation H Duffau, L Capelle, D Denvil, N Sichez, P Gatignol, M Lopes, M-C Mitchell, J-P Sichez, R Van Effenterre ............................................................................................................................. J Neurol Neurosurg Psychiatry 2003;74:901–907 Objectives: To describe functional recovery after surgical resection of low grade gliomas (LGG) in elo- quent brain areas, and discuss the mechanisms of compensation. Methods: Seventy-seven right-handed patients without deficit were operated on for a LGG invading primary and/or secondary sensorimotor and/or language areas, as shown anatomically by pre-operative MRI and intraoperatively by electrical brain stimulation and cortico-subcortical mapping. Results: Tumours involved 31 supplementary motor areas, 28 insulas, 8 primary somatosensory areas, 4 primary motor areas, 4 Broca’s areas, and 2 left temporal language areas. All patients had immedi- See end of article for ate post-operative deficits. Recovery occurred within 3 months in all except four cases (definitive mor- authors’ affiliations bidity: 5%). Ninety-two percent of the lesions were either totally or extensively resected on ....................... post-operative MRI. Conclusions: These findings suggest that spatio-temporal functional re-organisation is possible in peri- Correspondence to: Dr Duffau, Service de tumoural brain, and that the process is dynamic. The recruitment of compensatory areas with long term Neurochirurgie, Hôpital de perilesional functional reshaping would explain why: before surgery, there is no clinical deficit despite la Salpêtrière, 47–83 Bd the tumour growth in eloquent regions; immediately after surgery, the occurrence of a deficit, which de l’hôpital, 75651 Paris, could be due to the resection of invaded areas participating (but not essential) to the function; and why Cedex 13, France; email: hugues.duffau@ three months after surgery, almost complete recovery had occurred. This brain plasticity, which psl.ap-hop-paris.fr decreases the long term risk of surgical morbidity, may be used to extend the limits of surgery in elo- ....................... quent areas. esection of infiltrative tumours such as low grade gliomas and/or primary functional brain areas. This series comprises (LGG) that are located in eloquent brain areas remains a 37 males and 40 females (mean age 37 years) who all neurosurgical challenge. Although many studies show presented with seizures and a normal neurological examina- R http://jnnp.bmj.com/ that the quality of life and the median survival in LGG seems tion (except a mild dysphasia in three cases). A neuropsycho- correlated to the extent of resection,1–6 the role of resection logical evaluation using a standardised questionnaire30 remains unproven.3 Additionally, resection of these tumours, showed that all the patients were right handed. with no clearly defined boundaries and often occurring in Pre-operative MRI showed a tumour involving the supple- functional regions, carries a high risk (13–19.7%) of perma- mentary motor area (SMA) in 31 cases (9 right, 22 left), the nent deficit.7–9 The development of methods of pre-operative insular lobe in 28 cases (20 right, 8 left), the primary somato- neurofunctional imaging (NFI)10–14 and intra-operative electri- sensory area (S1) in eight cases (5 right, 3 left), the primary cal stimulations (IES)2 15–21 functional mapping has allowed motor area (M1) in four cases (three non-dominant facial the identification and the organisation of specific brain regions—in one case with also infiltration of S1 of the face— on September 24, 2021 by guest. Protected copyright. regions. These techniques can be used to decrease the risk of and one hand/forearm left site), Broca’s area in four cases complications following surgical resection of tumours in (pars opercularis Brodman Area (BA) 44, pars triangularis eloquent brain. However, if brain functions are considered to (BA 45), and the left dominant temporal lobe in two cases. remain in their classical anatomical locations, and these loca- All surgical procedures used IES (5 mm spaced tips bipolar tions are infiltrated by tumour, then excision of the tumour electrode, biphasic current with pulse duration of 1 ms, will either be considered impossible or result in an unaccept- frequency of 60 Hz, intensity of 4 to 18 mA, Ojemann Cortical 19 able postoperative morbidity. Given the brain plasticity and stimulator, Radionics*).17 18 The patients harboring tumours 22 23 functional compensation seen after stroke, with congenital involving the right supplementary and primary motor areas, 24 25 malformations or following brain injury, we hypothesise and the right insular lobe underwent surgery under general that brain infiltration by gliomas leads to reshaping or local anaesthesia, with cortical and sub-cortical IES allowing the reorganisation of functional networks. This would explain the detection of the whole cortico-spinal pathways.31 Although the frequent lack of clinical deficit despite LGG growing in motor mapping definition might be considered as not very 27–29 eloquent brain areas, and also the transient nature of post- accurate under general anaesthesia, particularly in subcortical operative deficits. To illustrate the background to this hypoth- regions, we have recently shown the effectiveness of such a esis we describe our experience and observations of functional technique,32 without “awake surgery”. Conversely, the patients recovery in patients having resection of LGG from eloquent with left and somatosensory tumours were operated under brain regions. PATIENTS AND METHODS ............................................................. Between November 1996 and June 2001, a consecutive series Abbreviations: IES, electrical stimulations; LGG, low grade gliomas; of 77 patients had resection of LGG, with IES, from secondary NFI, neurofunctional imaging; SMA, supplementary motor area www.jnnp.com www.jnnp.com 902 Table 1 Clinical, radiological, and surgical characteristics of the 77 patients (37 males, 40 females; mean age 37 years) with resection in a glioma in secondary and/or primary functional brain areas Number Presenting Cortico-subcortical functional boundaries identified by intraoperative Quality of Glioma location of cases symptoms Clinical examination stimulations Clinical results resection Supplementary motor area 31 Seizures Normal except mild Posteriorly: primary motor cortex and pyramidal pathways Laterally: language 31 immediate post-operative SMA syndromes, with 31 (sub) total Right 9 dysphasia in 2 left structures (left gliomas) recovery within 1–3 months 1 residual right lower gliomas limb monoparesia Improvements of the 2 Left 22 preoperative dysphasias Insular lobe 28 Seizures Normal except mild Insular cortex: language areas (left gliomas) Deeply: internal capsule (in all 20 immediate motor deficits and 7 mild speech 22 (sub) total Right 20 dysphasia in 1 left cases) and language pathways (left gliomas) disturbances (left gliomas) Recovery within 3 months 6 partial (left glioma except 3 residual hemiparesia Improvement of the gliomas) Left 8 preoperative dysphasia Primary somatosensory area 8 Seizures Normal Anteriorly: primary motor cortex and pyramidal pathways 8 severe immediate sensory loss, with recovery within 8 (sub) total Right 5 3 months 2 mild residual dysesthesias Left 3 Primary motor area 4 Seizures Normal Face area resection: primary motor cortex and pyramidal pathways of the 3 immediate central facial palsies and 1 4 total Facial 3 upper limb (lateral limb) hypophonia, with recovery within 1 month Upper limb 1 “Upper limb area” resection, after functional reorganisation (second surgery): Immediate right upper limb after resection of the all motor sites around the “silent” region (while “eloquent” 2 years before) “upper limb area” with recovery within 2 weeks Broca’s area 4 Seizures Normal All language structures around the glioma: posteriorly, within precentral gyrus; 4 immediate slight speech disturbances, with 4 total medially, within middle frontal gyrus recovery within 1 week Left temporal language area 2 Seizures Normal “Language area” resection, after functional reorganisation (second surgery): 2 immediate dysphasias, with recovery within 3 2 total all language sites were behind the invaded “silent” region (while “eloquent” months several months before) sponding whitetures, fibres notably deeply. theleft head LGG, the of resection was theIES, pursued thus up incorporating caudate total to SMA the nucleus removalprimary language (fig and struc- motor 1). Laterally, pathways in corre- were detectedLGG, by cortico-subcortical theare resection summarised in wasThe table clinical, continued 1. radiological, and In surgical posteriorlyRESULTS surgery data of of until the medial 77 the precentral patients motor and language mappings. local anaesthesia with performance of intraoperative sensori- hemiplegia, then completely recoveredparacentral within area). one The month. patientposterior had edge an of immediate the post-surgical glioma surgical removal, cavity with comes resection intoPostoperative of the axial the contact and supplementary with sagittal motorboundaries the T1-weighted area of MRI, (the the showing resection. ausing A, total electrical anterior; stimulations, P, represented posterior;corresponding
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