Abstract
Objectives: Despite the growing use of intraoperative functional mapping in supratentorial low grade glioma (LGG) surgery, few studies have compared series of patients operated on without and with direct electrical stimulation (DES) by the same team. The present study compared the rate of LGG surgery performed in eloquent areas, the rate of postoperative sequelae, and the quality of resection during two consecutive periods in the same department—the first without and the second with the use of intraoperative electrophysiology.
Methods: Between 1985 and 1996, 100 patients harbouring a supratentorial LGG underwent surgery with no functional mapping (S1). Between 1996 and 2003, 122 patients were operated on in the same department for a supratentorial LGG using intraoperative cortico-subcortical DES (S2).
Results: Comparison between the two series showed that 35% of LGGs were operated on in eloquent areas in S1 versus 62% in S2 (p<0.0001), with 17% severe permanent deficits in S1 versus 6.5% in S2 (p<0.019). On postoperative MRI, 37% of resections were subtotal and 6% total in S1 versus 50.8% and 25.4%, respectively, in S2 (p<0.001). In both groups, survival was significantly related to the quality of resection.
Conclusions: The results of the present study allow, for the first time, quantification of the contribution of intraoperative DES in LGG resection. Indeed, the use of this method leads to the extension of indications of LGG surgery within eloquent areas; to a decrease in the risk of sequelae; and to improvement of the quality of tumour resection, with an impact on survival.
Full Text
The Full Text of this article is available as a PDF (166.9 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Berger M. S., Deliganis A. V., Dobbins J., Keles G. E. The effect of extent of resection on recurrence in patients with low grade cerebral hemisphere gliomas. Cancer. 1994 Sep 15;74(6):1784–1791. doi: 10.1002/1097-0142(19940915)74:6<1784::aid-cncr2820740622>3.0.co;2-d. [DOI] [PubMed] [Google Scholar]
- Berger M. S., Ojemann G. A. Intraoperative brain mapping techniques in neuro-oncology. Stereotact Funct Neurosurg. 1992;58(1-4):153–161. doi: 10.1159/000098989. [DOI] [PubMed] [Google Scholar]
- Berger M. S., Ojemann G. A., Lettich E. Neurophysiological monitoring during astrocytoma surgery. Neurosurg Clin N Am. 1990 Jan;1(1):65–80. [PubMed] [Google Scholar]
- Blanshard H. J., Chung F., Manninen P. H., Taylor M. D., Bernstein M. Awake craniotomy for removal of intracranial tumor: considerations for early discharge. Anesth Analg. 2001 Jan;92(1):89–94. doi: 10.1097/00000539-200101000-00018. [DOI] [PubMed] [Google Scholar]
- Brell M., Ibáez J., Caral L., Ferrer E. Factors influencing surgical complications of intra-axial brain tumours. Acta Neurochir (Wien) 2000;142(7):739–750. doi: 10.1007/s007010070088. [DOI] [PubMed] [Google Scholar]
- Cabantog A. M., Bernstein M. Complications of first craniotomy for intra-axial brain tumour. Can J Neurol Sci. 1994 Aug;21(3):213–218. doi: 10.1017/s0317167100041184. [DOI] [PubMed] [Google Scholar]
- Cedzich C., Taniguchi M., Schäfer S., Schramm J. Somatosensory evoked potential phase reversal and direct motor cortex stimulation during surgery in and around the central region. Neurosurgery. 1996 May;38(5):962–970. doi: 10.1097/00006123-199605000-00023. [DOI] [PubMed] [Google Scholar]
- Cukiert A., Gronich G., Marino Júnior R. Surgical approaches to tumors and epileptogenic zones close to Wernicke's area. Arq Neuropsiquiatr. 1995 Sep;53(3-B):587–591. doi: 10.1590/s0004-282x1995000400006. [DOI] [PubMed] [Google Scholar]
- Danks R. A., Rogers M., Aglio L. S., Gugino L. D., Black P. M. Patient tolerance of craniotomy performed with the patient under local anesthesia and monitored conscious sedation. Neurosurgery. 1998 Jan;42(1):28–36. doi: 10.1097/00006123-199801000-00006. [DOI] [PubMed] [Google Scholar]
- Duffau H. Acute functional reorganisation of the human motor cortex during resection of central lesions: a study using intraoperative brain mapping. J Neurol Neurosurg Psychiatry. 2001 Apr;70(4):506–513. doi: 10.1136/jnnp.70.4.506. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Duffau H., Bauchet L., Lehéricy S., Capelle L. Functional compensation of the left dominant insula for language. Neuroreport. 2001 Jul 20;12(10):2159–2163. doi: 10.1097/00001756-200107200-00023. [DOI] [PubMed] [Google Scholar]
- Duffau H., Capelle L., Denvil D., Sichez N., Gatignol P., Lopes M., Mitchell M-C, Sichez J-P, Van Effenterre R. Functional recovery after surgical resection of low grade gliomas in eloquent brain: hypothesis of brain compensation. J Neurol Neurosurg Psychiatry. 2003 Jul;74(7):901–907. doi: 10.1136/jnnp.74.7.901. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Duffau H., Capelle L., Lopes M., Faillot T., Sichez J. P., Fohanno D. The insular lobe: physiopathological and surgical considerations. Neurosurgery. 2000 Oct;47(4):801–811. doi: 10.1097/00006123-200010000-00001. [DOI] [PubMed] [Google Scholar]
- Duffau H., Capelle L., Sichez J., Faillot T., Abdennour L., Law Koune J. D., Dadoun S., Bitar A., Arthuis F., Van Effenterre R. Intra-operative direct electrical stimulations of the central nervous system: the Salpêtrière experience with 60 patients. Acta Neurochir (Wien) 1999;141(11):1157–1167. doi: 10.1007/s007010050413. [DOI] [PubMed] [Google Scholar]
- Duffau H., Denvil D., Capelle L. Long term reshaping of language, sensory, and motor maps after glioma resection: a new parameter to integrate in the surgical strategy. J Neurol Neurosurg Psychiatry. 2002 Apr;72(4):511–516. doi: 10.1136/jnnp.72.4.511. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Duffau H., Denvil D., Lopes M., Gasparini F., Cohen L., Capelle L., Van Effenterre R. Intraoperative mapping of the cortical areas involved in multiplication and subtraction: an electrostimulation study in a patient with a left parietal glioma. J Neurol Neurosurg Psychiatry. 2002 Dec;73(6):733–738. doi: 10.1136/jnnp.73.6.733. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Duffau H., Sichez J. P., Lehéricy S. Intraoperative unmasking of brain redundant motor sites during resection of a precentral angioma: evidence using direct cortical stimulation. Ann Neurol. 2000 Jan;47(1):132–135. [PubMed] [Google Scholar]
- Duffau Hugues, Capelle Laurent, Denvil Dominique, Gatignol Peggy, Sichez Nicole, Lopes Manuel, Sichez Jean-Pierre, Van Effenterre Rémy. The role of dominant premotor cortex in language: a study using intraoperative functional mapping in awake patients. Neuroimage. 2003 Dec;20(4):1903–1914. doi: 10.1016/s1053-8119(03)00203-9. [DOI] [PubMed] [Google Scholar]
- Duffau Hugues, Capelle Laurent, Denvil Dominique, Sichez Nicole, Gatignol Peggy, Taillandier Luc, Lopes Manuel, Mitchell Mary-Christine, Roche Sabine, Muller Jean-Charles. Usefulness of intraoperative electrical subcortical mapping during surgery for low-grade gliomas located within eloquent brain regions: functional results in a consecutive series of 103 patients. J Neurosurg. 2003 Apr;98(4):764–778. doi: 10.3171/jns.2003.98.4.0764. [DOI] [PubMed] [Google Scholar]
- Duffau Hugues, Capelle Laurent. Preferential brain locations of low-grade gliomas. Cancer. 2004 Jun 15;100(12):2622–2626. doi: 10.1002/cncr.20297. [DOI] [PubMed] [Google Scholar]
- Duffau Hugues, Capelle Laurent, Sichez Nicole, Denvil Dominique, Lopes Manuel, Sichez Jean-Pierre, Bitar Ahmad, Fohanno Denis. Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain. 2002 Jan;125(Pt 1):199–214. doi: 10.1093/brain/awf016. [DOI] [PubMed] [Google Scholar]
- Ebel H., Ebel M., Schillinger G., Klimek M., Sobesky J., Klug N. Surgery of intrinsic cerebral neoplasms in eloquent areas under local anesthesia. Minim Invasive Neurosurg. 2000 Dec;43(4):192–196. doi: 10.1055/s-2000-11372. [DOI] [PubMed] [Google Scholar]
- Ebeling U., Fischer M., Kothbauer K. Surgery of astrocytomas in the motor and premotor cortex under local anesthesia: report of 11 cases. Minim Invasive Neurosurg. 1995 Jun;38(2):51–59. doi: 10.1055/s-2008-1053460. [DOI] [PubMed] [Google Scholar]
- Eisner W., Burtscher J., Bale R., Sweeney R., Koppelstätter F., Golaszewski S., Kolbitsch C., Twerdy K. Use of neuronavigation and electrophysiology in surgery of subcortically located lesions in the sensorimotor strip. J Neurol Neurosurg Psychiatry. 2002 Mar;72(3):378–381. doi: 10.1136/jnnp.72.3.378. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fadul C., Wood J., Thaler H., Galicich J., Patterson R. H., Jr, Posner J. B. Morbidity and mortality of craniotomy for excision of supratentorial gliomas. Neurology. 1988 Sep;38(9):1374–1379. doi: 10.1212/wnl.38.9.1374. [DOI] [PubMed] [Google Scholar]
- Fandino J., Kollias S. S., Wieser H. G., Valavanis A., Yonekawa Y. Intraoperative validation of functional magnetic resonance imaging and cortical reorganization patterns in patients with brain tumors involving the primary motor cortex. J Neurosurg. 1999 Aug;91(2):238–250. doi: 10.3171/jns.1999.91.2.0238. [DOI] [PubMed] [Google Scholar]
- Fried I. Functional neuroimaging in presurgical localization of essential cortical processing zones. Adv Neurol. 2000;83:297–303. [PubMed] [Google Scholar]
- Fukaya C., Katayama Y., Yoshino A., Kobayashi K., Kasai M., Yamamoto T. Intraoperative wake-up procedure with propofol and laryngeal mask for optimal excision of brain tumour in eloquent areas. J Clin Neurosci. 2001 May;8(3):253–255. doi: 10.1054/jocn.2000.0866. [DOI] [PubMed] [Google Scholar]
- Haglund M. M., Berger M. S., Shamseldin M., Lettich E., Ojemann G. A. Cortical localization of temporal lobe language sites in patients with gliomas. Neurosurgery. 1994 Apr;34(4):567–576. doi: 10.1227/00006123-199404000-00001. [DOI] [PubMed] [Google Scholar]
- Hermann B. P., Wyler A. R., Somes G., Clement L. Dysnomia after left anterior temporal lobectomy without functional mapping: frequency and correlates. Neurosurgery. 1994 Jul;35(1):52–57. doi: 10.1227/00006123-199407000-00008. [DOI] [PubMed] [Google Scholar]
- Holodny A. I., Schwartz T. H., Ollenschleger M., Liu W. C., Schulder M. Tumor involvement of the corticospinal tract: diffusion magnetic resonance tractography with intraoperative correlation. J Neurosurg. 2001 Dec;95(6):1082–1082. doi: 10.3171/jns.2001.95.6.1082. [DOI] [PubMed] [Google Scholar]
- Keles G. E., Lamborn K. R., Berger M. S. Low-grade hemispheric gliomas in adults: a critical review of extent of resection as a factor influencing outcome. J Neurosurg. 2001 Nov;95(5):735–745. doi: 10.3171/jns.2001.95.5.0735. [DOI] [PubMed] [Google Scholar]
- Krombach G. A., Spetzger U., Rohde V., Gilsbach J. M. Intraoperative localization of functional regions in the sensorimotor cortex by neuronavigation and cortical mapping. Comput Aided Surg. 1998;3(2):64–73. doi: 10.1002/(SICI)1097-0150(1998)3:2<64::AID-IGS3>3.0.CO;2-I. [DOI] [PubMed] [Google Scholar]
- Mandonnet Emmanuel, Delattre Jean-Yves, Tanguy Marie-Laure, Swanson Kristin R., Carpentier Antoine F., Duffau Hugues, Cornu Philippe, Van Effenterre Rémy, Alvord Ellsworth C., Jr, Capelle Laurent. Continuous growth of mean tumor diameter in a subset of grade II gliomas. Ann Neurol. 2003 Apr;53(4):524–528. doi: 10.1002/ana.10528. [DOI] [PubMed] [Google Scholar]
- Manninen Pirjo H., Tan Tong Khee. Postoperative nausea and vomiting after craniotomy for tumor surgery: a comparison between awake craniotomy and general anesthesia. J Clin Anesth. 2002 Jun;14(4):279–283. doi: 10.1016/s0952-8180(02)00354-9. [DOI] [PubMed] [Google Scholar]
- Meyer F. B., Bates L. M., Goerss S. J., Friedman J. A., Windschitl W. L., Duffy J. R., Perkins W. J., O'Neill B. P. Awake craniotomy for aggressive resection of primary gliomas located in eloquent brain. Mayo Clin Proc. 2001 Jul;76(7):677–687. doi: 10.4065/76.7.677. [DOI] [PubMed] [Google Scholar]
- Nimsky C., Ganslandt O., Fahlbusch R. Functional neuronavigation and intraoperative MRI. Adv Tech Stand Neurosurg. 2004;29:229–263. doi: 10.1007/978-3-7091-0558-0_6. [DOI] [PubMed] [Google Scholar]
- Peraud Aurelia, Meschede Magnus, Eisner Wilhelm, Ilmberger Josef, Reulen Hans-Jürgen. Surgical resection of grade II astrocytomas in the superior frontal gyrus. Neurosurgery. 2002 May;50(5):966–977. doi: 10.1097/00006123-200205000-00009. [DOI] [PubMed] [Google Scholar]
- Reithmeier T., Krammer M., Gumprecht H., Gerstner W., Lumenta C. B. Neuronavigation combined with electrophysiological monitoring for surgery of lesions in eloquent brain areas in 42 cases: a retrospective comparison of the neurological outcome and the quality of resection with a control group with similar lesions. Minim Invasive Neurosurg. 2003 Apr;46(2):65–71. doi: 10.1055/s-2003-39334. [DOI] [PubMed] [Google Scholar]
- Reulen H. J., Schmid U. D., Ilmberger J., Eisner W., Bise K. Tumorchirurgie im Sprachkortex in Lokalanästhesie. Neuropsychologisches und neurophysiologisches Monitoring während Operationen in der dominanten Hirnhälfte. Nervenarzt. 1997 Oct;68(10):813–824. doi: 10.1007/s001150050199. [DOI] [PubMed] [Google Scholar]
- Rostomily R. C., Berger M. S., Ojemann G. A., Lettich E. Postoperative deficits and functional recovery following removal of tumors involving the dominant hemisphere supplementary motor area. J Neurosurg. 1991 Jul;75(1):62–68. doi: 10.3171/jns.1991.75.1.0062. [DOI] [PubMed] [Google Scholar]
- Roux F. E., Ibarrola D., Tremoulet M., Lazorthes Y., Henry P., Sol J. C., Berry I. Methodological and technical issues for integrating functional magnetic resonance imaging data in a neuronavigational system. Neurosurgery. 2001 Nov;49(5):1145–1157. doi: 10.1097/00006123-200111000-00025. [DOI] [PubMed] [Google Scholar]
- Roux Franck-Emmanuel, Boulanouar Kader, Lotterie Jean-Albert, Mejdoubi Mehdi, LeSage James P., Berry Isabelle. Language functional magnetic resonance imaging in preoperative assessment of language areas: correlation with direct cortical stimulation. Neurosurgery. 2003 Jun;52(6):1335–1347. doi: 10.1227/01.neu.0000064803.05077.40. [DOI] [PubMed] [Google Scholar]
- Rutten G. J. M., Ramsey N. F., van Rijen P. C., Noordmans H. J., van Veelen C. W. M. Development of a functional magnetic resonance imaging protocol for intraoperative localization of critical temporoparietal language areas. Ann Neurol. 2002 Mar;51(3):350–360. doi: 10.1002/ana.10117. [DOI] [PubMed] [Google Scholar]
- Sarang A., Dinsmore J. Anaesthesia for awake craniotomy--evolution of a technique that facilitates awake neurological testing. Br J Anaesth. 2003 Feb;90(2):161–165. doi: 10.1093/bja/aeg037. [DOI] [PubMed] [Google Scholar]
- Sawaya R., Hammoud M., Schoppa D., Hess K. R., Wu S. Z., Shi W. M., Wildrick D. M. Neurosurgical outcomes in a modern series of 400 craniotomies for treatment of parenchymal tumors. Neurosurgery. 1998 May;42(5):1044–1056. doi: 10.1097/00006123-199805000-00054. [DOI] [PubMed] [Google Scholar]
- Schiffbauer Hagen, Berger Mitchel S., Ferrari Paul, Freudenstein Dirk, Rowley Howard A., Roberts Timothy P. L. Preoperative magnetic source imaging for brain tumor surgery: a quantitative comparison with intraoperative sensory and motor mapping. J Neurosurg. 2002 Dec;97(6):1333–1342. doi: 10.3171/jns.2002.97.6.1333. [DOI] [PubMed] [Google Scholar]
- Schmidt Meic H., Berger Mitchel S., Lamborn Kathleen R., Aldape Ken, McDermott Michael W., Prados Michael D., Chang Susan M. Repeated operations for infiltrative low-grade gliomas without intervening therapy. J Neurosurg. 2003 Jun;98(6):1165–1169. doi: 10.3171/jns.2003.98.6.1165. [DOI] [PubMed] [Google Scholar]
- Sobottka S. B., Bredow J., Beuthien-Baumann B., Reiss G., Schackert G., Steinmeier R. Comparison of functional brain PET images and intraoperative brain-mapping data using image-guided surgery. Comput Aided Surg. 2002;7(6):317–325. doi: 10.1002/igs.10060. [DOI] [PubMed] [Google Scholar]
- Tandon P., Mahapatra A. K., Khosla A. Operations on gliomas involving speech centres. Acta Neurochir Suppl (Wien) 1993;56:67–71. doi: 10.1007/978-3-7091-9239-9_11. [DOI] [PubMed] [Google Scholar]
- Taylor M. D., Bernstein M. Awake craniotomy with brain mapping as the routine surgical approach to treating patients with supratentorial intraaxial tumors: a prospective trial of 200 cases. J Neurosurg. 1999 Jan;90(1):35–41. doi: 10.3171/jns.1999.90.1.0035. [DOI] [PubMed] [Google Scholar]
- Vives K. P., Piepmeier J. M. Complications and expected outcome of glioma surgery. J Neurooncol. 1999 May;42(3):289–302. doi: 10.1023/a:1006163328765. [DOI] [PubMed] [Google Scholar]
- Wagner W., Tschiltschke W., Niendorf W. R., Schroeder H. W., Gaab M. R. Infrared-based neuronavigation and cortical motor stimulation in the management of central-region tumors. Stereotact Funct Neurosurg. 1997;68(1-4):112–116. doi: 10.1159/000099911. [DOI] [PubMed] [Google Scholar]
- Walsh A. R., Schmidt R. H., Marsh H. T. Cortical mapping and resection under local anaesthetic as an aid to surgery of low and intermediate grade gliomas. Br J Neurosurg. 1990;4(6):485–491. doi: 10.3109/02688699008993797. [DOI] [PubMed] [Google Scholar]
- Whittle I. R., Borthwick S., Haq N. Brain dysfunction following 'awake' craniotomy, brain mapping and resection of glioma. Br J Neurosurg. 2003 Apr;17(2):130–137. doi: 10.1080/0268869031000108873. [DOI] [PubMed] [Google Scholar]
- Whittle Ian R. Surgery for gliomas. Curr Opin Neurol. 2002 Dec;15(6):663–669. doi: 10.1097/01.wco.0000044761.39452.38. [DOI] [PubMed] [Google Scholar]
- Wiedemayer H., Sandalcioglu I. E., Armbruster W., Regel J., Schaefer H., Stolke D. False negative findings in intraoperative SEP monitoring: analysis of 658 consecutive neurosurgical cases and review of published reports. J Neurol Neurosurg Psychiatry. 2004 Feb;75(2):280–286. [PMC free article] [PubMed] [Google Scholar]
- Wood C. C., Spencer D. D., Allison T., McCarthy G., Williamson P. D., Goff W. R. Localization of human sensorimotor cortex during surgery by cortical surface recording of somatosensory evoked potentials. J Neurosurg. 1988 Jan;68(1):99–111. doi: 10.3171/jns.1988.68.1.0099. [DOI] [PubMed] [Google Scholar]
