Skip to main content
Neurotherapeutics logoLink to Neurotherapeutics
. 2009 Jul;6(3):478–486. doi: 10.1016/j.nurt.2009.04.005

Operative techniques for gliomas and the value of extent of resection

Nader Sanai 1, Mitchel S Berger 1,
PMCID: PMC5084184  PMID: 19560738

Summary

Refinement of neurosurgical technique has enabled safer operations with more aggressive outcomes. One cornerstone of modern-day practice is the utilization of intraoperative stimulation mapping. In addition to identifying critical motor pathways, this technique can be adapted to reliably identify language pathways. Given the individual variability of cortical language localization, such awake language mapping is essential to minimize language deficits following tumor resection. Our experience suggests that cortical language mapping is a safe and efficient adjunct to optimize tumor resection while preserving essential language sites, even in the setting of negative mapping data. However, the value of maximizing glioma resections remains surprisingly unclear, as there is no general consensus in the literature regarding the efficacy of extent of glioma resection in improving patient outcome. While the importance of resection in obtaining tissue diagnosis and alleviating symptoms is clear, a lack of Class I evidence prevents similar certainty in assessing the influence of extent of resection. Beyond an analysis of modern intraoperative mapping techniques, we examine every major clinical publication since 1990 on the role of extent of resection in glioma outcome. The mounting evidence suggests that, despite persistent limitations in the quality of available studies, a more extensive surgical resection is associated with longer life expectancy for both low-grade and high-grade gliomas.

Key Words: Language mapping, motor tracts, cortical stimulation, extent of resection

References

  • 1.Foerster O. The cerebral cortex of man. Lancet. 1931;2:309–312. [Google Scholar]
  • 2.Penfield W, Bolchey E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain. 1937;60:389–443. [Google Scholar]
  • 3.Penfield W, Erickson TC. Epilepsy and cerebral localization. A study of the mechanism, treatment, and prevention of epileptic seizures. 1941.
  • 4.Penfield W, Rasmussen T. Secondary sensory and motor representation. 1950.
  • 5.Ranck JB. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res. 1975;98:417–440. doi: 10.1016/0006-8993(75)90364-9. [DOI] [PubMed] [Google Scholar]
  • 6.Haglund MM, Ojemann GA, Blasdel GG. Optical imaging of bipolar cortical stimulation. J Neurosurg. 1993;78:785–793. doi: 10.3171/jns.1993.78.5.0785. [DOI] [PubMed] [Google Scholar]
  • 7.Haglund MM, Ojemann GA, Hochman DW. Optical imaging of epileptiform and functional activity in human cerebral cortex. Nature. 1992;358:668–671. doi: 10.1038/358668a0. [DOI] [PubMed] [Google Scholar]
  • 8.Herholz K, Thiel A, Wienhard K, et al. Individual functional anatomy of verb generation. Neuroimage. 1996;3:185–194. doi: 10.1006/nimg.1996.0020. [DOI] [PubMed] [Google Scholar]
  • 9.Ojemann G, Ojemann J, Lettich E, Berger M. Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg. 1989;71:316–326. doi: 10.3171/jns.1989.71.3.0316. [DOI] [PubMed] [Google Scholar]
  • 10.Ojemann GA, Whitaker HA. Language localization and variability. Brain Lang. 1978;6:239–260. doi: 10.1016/0093-934x(78)90061-5. [DOI] [PubMed] [Google Scholar]
  • 11.Ojemann GA. Individual variability in cortical localization of language. J Neurosurg. 1979;50:164–169. doi: 10.3171/jns.1979.50.2.0164. [DOI] [PubMed] [Google Scholar]
  • 12.Ojemann JG, Miller JW, Silbergeld DL. Reserved function in brain invaded by tumor. Neurosurgery. 1996;39:253–258. doi: 10.1097/00006123-199608000-00003. [DOI] [PubMed] [Google Scholar]
  • 13.Scitz RJ, Huang Y, Knorr U, et al. Large-scale plasticity of the human motor cortex. Neuroreport. 1995;6:742–744. doi: 10.1097/00001756-199503270-00009. [DOI] [PubMed] [Google Scholar]
  • 14.Wunderlich G, Knorr U, Herzog H, et al. Precentral glioma location determines the displacement of cortical hand representation. Neurosurgery. 1998;42:18–26. doi: 10.1097/00006123-199801000-00005. [DOI] [PubMed] [Google Scholar]
  • 15.Quinones-Hinojosa A, Ojemann SG, Sanai N, Dillon WP, Berger MS. Reoperative correlation of intraoperative cortical mapping with magnetic resonance imaging landmarks to predict localization of the Broca area. J Neurosurg. 2003;99:311–318. doi: 10.3171/jns.2003.99.2.0311. [DOI] [PubMed] [Google Scholar]
  • 16.Seghier ML, Lazeyras F, Pegna AJ, et al. Variability of fMRI activation during a phonological and semantic language task in healthy subjects. Hum Brain Mapp. 2004;23:140–155. doi: 10.1002/hbm.20053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Tzourio-Mazoyer N, Josse G, Crivello F, Mazoyer B. Interindividual variability in the hemispheric organization for speech. Neuroimage. 2004;21:422–435. doi: 10.1016/j.neuroimage.2003.08.032. [DOI] [PubMed] [Google Scholar]
  • 18.Turkeltaub PE, Eden GF, Jones KM, Zeffiro TA. Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. Neuroimage. 2002;16:765–780. doi: 10.1006/nimg.2002.1131. [DOI] [PubMed] [Google Scholar]
  • 19.Tzourio N, Crivello F, Mellet E, Nkanga-Ngila B, Mazoyer B. Functional anatomy of dominance for speech comprehension in left handers vs right handers. Neuroimage. 1998;8:1–16. doi: 10.1006/nimg.1998.0343. [DOI] [PubMed] [Google Scholar]
  • 20.Dehaene S, Dupoux E, Mehler J, et al. Anatomical variability in the cortical representation of first and second language. Neuroreport. 1997;8:3809–3815. doi: 10.1097/00001756-199712010-00030. [DOI] [PubMed] [Google Scholar]
  • 21.Steinmetz H, Scitz RJ. Functional anatomy of language processing: neuroimaging and the problem of individual variability. Neuropsychologia. 1991;29:1149–1161. doi: 10.1016/0028-3932(91)90030-c. [DOI] [PubMed] [Google Scholar]
  • 22.Josse G, Herve PY, Crivello F, Mazoyer B, Tzourio-Mazoyer N. Hemispheric specialization for language: Brain volume matters. Brain Res. 2006;1068:184–193. doi: 10.1016/j.brainres.2005.11.037. [DOI] [PubMed] [Google Scholar]
  • 23.Davies KG, Maxwell RE, Jennum P, et al. Language function following subdural grid-directed temporal lobectomy. Acta Neurol Scand. 1994;90:201–206. doi: 10.1111/j.1600-0404.1994.tb02706.x. [DOI] [PubMed] [Google Scholar]
  • 24.FitzGerald DB, Cosgrove GR, Ronner S, et al. Location of language in the cortex: a comparison between functional MR imaging and electrocortical stimulation. AJNR Am J Neuroradiol. 1997;18:1529–1539. [PMC free article] [PubMed] [Google Scholar]
  • 25.Skirboll SS, Ojemann GA, Berger MS, Lettich E, Winn HR. Functional cortex and subcortical white matter located within gliomas. Neurosurgery. 1996;38:678–684. [PubMed] [Google Scholar]
  • 26.Ojemann GA. Models of the brain organization for higher integrative functions derived with electrical stimulation techniques. Hum Neurobiol. 1982;1:243–249. [PubMed] [Google Scholar]
  • 27.Ojemann GA. Cortical organization of language. J Neurosci. 1991;11:2281–2287. doi: 10.1523/JNEUROSCI.11-08-02281.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Ojemann GA, Creutzfeldt OD. Nervous System V, Part 2. 1987:675–700.
  • 29.Ojemann GA. Organization of language cortex derived from investigations during neurosurgery. Seminars in Neuroscience. 1990;2:297–305. [Google Scholar]
  • 30.Haglund MM, Berger MS, Shamseldin M, Lettich E, Ojemann GA. Cortical localization of temporal lobe language sites in patients with gliomas. Neurosurgery. 1994;34:567–576. doi: 10.1227/00006123-199404000-00001. [DOI] [PubMed] [Google Scholar]
  • 31.Taylor MD, 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;90:35–41. doi: 10.3171/jns.1999.90.1.0035. [DOI] [PubMed] [Google Scholar]
  • 32.Hochberg FH, Pruitt A. Assumptions in the radiotherapy of glioblastoma. Neurology. 1980;30:907–911. doi: 10.1212/wnl.30.9.907. [DOI] [PubMed] [Google Scholar]
  • 33.Wallner KE, Galicich JH, Krol G, Arbit E, Malkin MG. Patterns of failure following treatment for glioblastoma multiforme and anaplastic astrocytoma. Int J Radiat Oncol Biol Phys. 1989;16:1405–1409. doi: 10.1016/0360-3016(89)90941-3. [DOI] [PubMed] [Google Scholar]
  • 34.Ebeling U, Steinmetz H, Huang YX, Kahn T. Topography and identification of the inferior precentral sulcus in MR imaging. AJR Am J Roentgenol. 1989;153:1051–1056. doi: 10.2214/ajr.153.5.1051. [DOI] [PubMed] [Google Scholar]
  • 35.Herholz K, Reulen HJ, von Stockhausen HM, et al. Preoperative activation and intraoperative stimulation of language-related areas in patients with glioma. Neurosurgery. 1997;41:1253–1260. doi: 10.1097/00006123-199712000-00004. [DOI] [PubMed] [Google Scholar]
  • 36.Carpentier A, Pugh KR, Westerveld M, et al. Functional MRI of language processing: dependence on input modality and temporal lobe epilepsy. Epilepsia. 2001;42:1241–1254. doi: 10.1046/j.1528-1157.2001.35500.x. [DOI] [PubMed] [Google Scholar]
  • 37.Sartorius CJ, Berger MS. Rapid termination of intraoperative stimulation-evoked seizures with application of cold Ringer’s lactate to the cortex. Technical note. J Neurosurg. 1998;88:349–351. doi: 10.3171/jns.1998.88.2.0349. [DOI] [PubMed] [Google Scholar]
  • 38.Duffau H, Capelle L, Denvil D, et al. 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;98:764–778. doi: 10.3171/jns.2003.98.4.0764. [DOI] [PubMed] [Google Scholar]
  • 39.Duffau H, Capelle L, Sichez N, et al. Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain. 2002;125:199–214. doi: 10.1093/brain/awf016. [DOI] [PubMed] [Google Scholar]
  • 40.Lacroix M, Abi-Said D, Fourney DR, et al. A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg. 2001;95:190–198. doi: 10.3171/jns.2001.95.2.0190. [DOI] [PubMed] [Google Scholar]
  • 41.Sanai N, Berger MS. Mapping the horizon: techniques to optimize tumor resection before and during surgery. Clin Neurosurg. 2008;55:14–19. [PubMed] [Google Scholar]
  • 42.Sanai N, Mirzadeh Z, Berger MS. Functional outcome after language mapping for glioma resection. N Engl J Med. 2008;358:18–27. doi: 10.1056/NEJMoa067819. [DOI] [PubMed] [Google Scholar]
  • 43.Berger MS. Lesions in functional (“eloquent”) cortex and sub-cortical white matter. Clin Neurosurg. 1993;41:443–463. [PubMed] [Google Scholar]
  • 44.Chollet F, DiPiero V, Wise RJ, et al. The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann Neurol. 1991;29:63–71. doi: 10.1002/ana.410290112. [DOI] [PubMed] [Google Scholar]
  • 45.Weder B, Scitz RJ. Deficient cerebral activation pattern in stroke recovery. Neuroreport. 1994;5:457–460. doi: 10.1097/00001756-199401120-00022. [DOI] [PubMed] [Google Scholar]
  • 46.Lewine JD, Astur RS, Davis LE, et al. Cortical organization in adulthood is modified by neonatal infarct: a case study. Radiology. 1994;190:93–96. doi: 10.1148/radiology.190.1.8259435. [DOI] [PubMed] [Google Scholar]
  • 47.Maldjian J, Atlas SW, Howard RS, et al. Functional magnetic resonance imaging of regional brain activity in patients with intracerebral arteriovenous malformations before surgical or endovascular therapy. J Neurosurg. 1996;84:477–483. doi: 10.3171/jns.1996.84.3.0477. [DOI] [PubMed] [Google Scholar]
  • 48.Grady MS, Jane JA, Steward O. Synaptic reorganization within the human central nervous system following injury. J Neurosurg. 1989;71:534–537. doi: 10.3171/jns.1989.71.4.0534. [DOI] [PubMed] [Google Scholar]
  • 49.Fandino J, Kollias SS, Wieser HG, 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;91:238–250. doi: 10.3171/jns.1999.91.2.0238. [DOI] [PubMed] [Google Scholar]
  • 50.Duffau H, Capelle L, Denvil D, et al. Functional recovery after surgical resection of low grade gliomas in eloquent brain: hypothesis of brain compensation. J Neurol Neurosurg Psychiatry. 2003;74:901–907. doi: 10.1136/jnnp.74.7.901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Thiel A, Herholz K, Koyuncu A, et al. Plasticity of language networks in patients with brain tumors: a positron emission tomography activation study. Ann Neurol. 2001;50:620–629. doi: 10.1002/ana.1253. [DOI] [PubMed] [Google Scholar]
  • 52.Duffau H, Bauchet L, Lehericy S, Capelle L. Functional compensation of the left dominant insula for language. Neuroreport. 2001;12:2159–2163. doi: 10.1097/00001756-200107200-00023. [DOI] [PubMed] [Google Scholar]
  • 53.Black P. Management of malignant glioma: role of surgery in relation to multimodality therapy. J Neurovirol. 1998;4:227–236. doi: 10.3109/13550289809114522. [DOI] [PubMed] [Google Scholar]
  • 54.Yasargil MG, Kadri PA, Yasargil DC. Microsurgery for malignant gliomas. J Neurooncol. 2004;69:67–81. doi: 10.1023/b:neon.0000041872.78927.d5. [DOI] [PubMed] [Google Scholar]
  • 55.Guthrie BL, Laws ER. Supratentorial low-grade gliomas. Neurosurg Clin N Am. 1990;1:37–48. [PubMed] [Google Scholar]
  • 56.Keles GE, Anderson B, Berger MS. The effect of extent of resection on time to tumor progression and survival in patients with glioblastoma multiforme of the cerebral hemisphere. Surg Neurol. 1999;52:371–379. doi: 10.1016/s0090-3019(99)00103-2. [DOI] [PubMed] [Google Scholar]
  • 57.Proescholdt MA, Macher C, Woertgen C, Brawanski A. Level of evidence in the literature concerning brain tumor resection. Clin Neurol Neurosurg. 2005;107:95–98. doi: 10.1016/j.clineuro.2004.02.025. [DOI] [PubMed] [Google Scholar]
  • 58.Sawaya R. Extent of resection in malignant gliomas: a critical summary. J Neurooncol. 1999;42:303–305. doi: 10.1023/a:1006167412835. [DOI] [PubMed] [Google Scholar]
  • 59.Grant R. Biopsy versus resection for malignant glioma (review). Cochrane Database Syst Rev 2006. [DOI] [PubMed]
  • 60.Nazzaro JM, Neuwelt EA. The role of surgery in the management of supratentorial intermediate and high-grade astrocytomas in adults. J Neurosurg. 1990;73:331–344. doi: 10.3171/jns.1990.73.3.0331. [DOI] [PubMed] [Google Scholar]
  • 61.Pierga JY, Hoang-Xuan K, Feuvret L, et al. Treatment of malignant gliomas in the elderly. J Neurooncol. 1999;43:187–193. doi: 10.1023/a:1006262918694. [DOI] [PubMed] [Google Scholar]
  • 62.Hess KR. Extent of resection as a prognostic variable in the treatment of gliomas. J Neurooncol. 1999;42:227–231. doi: 10.1023/a:1006118018770. [DOI] [PubMed] [Google Scholar]
  • 63.Sanai N, Berger MS. Glioma extent of resection and its impact on patient outcome. Neurosurgery. 2008;62:753–764. doi: 10.1227/01.neu.0000318159.21731.cf. [DOI] [PubMed] [Google Scholar]
  • 64.Hegi ME, Diserens AC, Gorlia T, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352:997–1003. doi: 10.1056/NEJMoa043331. [DOI] [PubMed] [Google Scholar]
  • 65.Keles GE, Chang EF, Lamborn KR, et al. Volumetric extent of resection and residual contrast enhancement on initial surgery as predictors of outcome in adult patients with hemispheric anaplastic astrocytoma. J Neurosurg. 2006;105:34–40. doi: 10.3171/jns.2006.105.1.34. [DOI] [PubMed] [Google Scholar]
  • 66.Leighton C, Fisher B, Bauman G, et al. Supratentorial low-grade glioma in adults: an analysis of prognostic factors and timing of radiation. J Clin Oncol. 1997;15:1294–1301. doi: 10.1200/JCO.1997.15.4.1294. [DOI] [PubMed] [Google Scholar]
  • 67.Nakamura M, Konishi N, Tsunoda S, et al. Analysis of prognostic and survival factors related to treatment of low-grade astrocytomas in adults. Oncology. 2000;58:108–116. doi: 10.1159/000012087. [DOI] [PubMed] [Google Scholar]
  • 68.Philippon JH, Clemenceau SH, Fauchon FH, Foncin JF. Supratentorial low-grade astrocytomas in adults. Neurosurgery. 1993;32:554–559. doi: 10.1227/00006123-199304000-00010. [DOI] [PubMed] [Google Scholar]
  • 69.Rajan B, Pickuth D, Ashley S, et al. The management of histologically unverified presumed cerebral gliomas with radiotherapy. Int J Radiat Oncol Biol Phys. 1994;28:405–413. doi: 10.1016/0360-3016(94)90064-7. [DOI] [PubMed] [Google Scholar]
  • 70.Shaw E, Arusell R, Scheithauer B, et al. Prospective randomized trial of lowversus high-dose radiation therapy in adults with supratentorial low-grade glioma: initial report of a North Central Cancer Treatment Group/Radiation Therapy Oncology Group/ Eastern Cooperative Oncology Group study. J Clin Oncol. 2002;20:2267–2276. doi: 10.1200/JCO.2002.09.126. [DOI] [PubMed] [Google Scholar]
  • 71.Yeh SA, Ho JT, Lui CC, et al. Treatment outcomes and prognostic factors in patients with supratentorial low-grade gliomas. Br J Radiol. 2005;78:230–235. doi: 10.1259/bjr/28534346. [DOI] [PubMed] [Google Scholar]
  • 72.Shaw EG, Daumas-Duport C, Scheithauer BW, et al. Radiation therapy in the management of low-grade supratentorial astrocytomas. J Neurosurg. 1989;70:853–861. doi: 10.3171/jns.1989.70.6.0853. [DOI] [PubMed] [Google Scholar]
  • 73.Laws ER, Taylor WF, Clifton MB, Okazaki H. Neurosurgical management of low-grade astrocytoma of the cerebral hemispheres. J Neurosurg. 1984;61:665–673. doi: 10.3171/jns.1984.61.4.0665. [DOI] [PubMed] [Google Scholar]
  • 74.North CA, North RB, Epstein JA, Piantadosi S, Wharam MD. Low-grade cerebral astrocytomas. Survival and quality of life after radiation therapy. Cancer. 1990;66:6–14. doi: 10.1002/1097-0142(19900701)66:1<6::aid-cncr2820660103>3.0.co;2-f. [DOI] [PubMed] [Google Scholar]
  • 75.Ito S, Chandler KL, Prados MD, et al. Proliferative potential and prognostic evaluation of low-grade astrocytomas. J Neurooncol. 1994;19:1–9. doi: 10.1007/BF01051043. [DOI] [PubMed] [Google Scholar]
  • 76.Nicolato A, Gerosa MA, Fina P, et al. Prognostic factors in low-grade supratentorial astrocytomas: a uni-multivariate statistical analysis in 76 surgically treated adult patients. Surg Neurol. 1995;44:208–221. doi: 10.1016/0090-3019(95)00184-0. [DOI] [PubMed] [Google Scholar]
  • 77.Whitton AC, Bloom HJ. Low grade glioma of the cerebral hemispheres in adults: a retrospective analysis of 88 cases. Int J Radiat Oncol Biol Phys. 1990;18:783–786. doi: 10.1016/0360-3016(90)90397-3. [DOI] [PubMed] [Google Scholar]
  • 78.Shibamoto Y, Kitakabu Y, Takahashi M, et al. Supratentorial low-grade astrocytoma. Correlation of computed tomography findings with effect of radiation therapy and prognostic variables. Cancer. 1993;72:190–195. doi: 10.1002/1097-0142(19930701)72:1<190::aid-cncr2820720134>3.0.co;2-y. [DOI] [PubMed] [Google Scholar]
  • 79.Karim AB, Maat B, Hatlevoll R, et al. A randomized trial on dose-response in radiation therapy of low-grade cerebral glioma: European Organization for Research and Treatment of Cancer (EORTC) Study 22844. Int J Radiat Oncol Biol Phys. 1996;36:549–556. doi: 10.1016/s0360-3016(96)00352-5. [DOI] [PubMed] [Google Scholar]
  • 80.Scerrati M, Roselli R, Iacoangeli M, Pompucci A, Rossi GF. Prognostic factors in low grade (WHO grade II) gliomas of the cerebral hemispheres: the role of surgery. J Neurol Neurosurg Psychiatry. 1996;61:291–296. doi: 10.1136/jnnp.61.3.291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 81.Lote K, Egeland T, Hager B, et al. Survival, prognostic factors, and therapeutic efficacy in low-grade glioma: a retrospective study in 379 patients. J Clin Oncol. 1997;15:3129–3140. doi: 10.1200/JCO.1997.15.9.3129. [DOI] [PubMed] [Google Scholar]
  • 82.Peraud A, Ansari H, Bise K, Reulen HJ. Clinical outcome of supratentorial astrocytoma WHO grade II. Acta Neurochir (Wien) 1998;140:1213–1222. doi: 10.1007/s007010050241. [DOI] [PubMed] [Google Scholar]
  • 83.van Veelen ML, Avezaat CJ, Kros JM, van Putten W, Vecht C. Supratentorial low grade astrocytoma: prognostic factors, dedifferentiation, and the issue of early versus late surgery. J Neurol Neurosurg Psychiatry. 1998;64:581–587. doi: 10.1136/jnnp.64.5.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 84.Bauman G, Pahapill P, Macdonald D, et al. Low grade glioma: a measuring radiographic response to radiotherapy. Can J Neurol Sci. 1999;26:18–22. [PubMed] [Google Scholar]
  • 85.Johannesen TB, Langmark F, Lote K. Progress in long-term survival in adult patients with supratentorial low-grade gliomas: a population-based study of 993 patients in whom tumors were diagnosed between 1970 and 1993. J Neurosurg. 2003;99:854–862. doi: 10.3171/jns.2003.99.5.0854. [DOI] [PubMed] [Google Scholar]
  • 86.Claus EB, Horlacher A, Hsu L, et al. Survival rates in patients with low-grade glioma after intraoperative magnetic resonance image guidance. Cancer. 2005;103:1227–1233. doi: 10.1002/cncr.20867. [DOI] [PubMed] [Google Scholar]
  • 87.McGirt MJ, Chaichana KL, Attenello FJ, et al. Extent of surgical resection is independently associated with survival in patients with hemispheric infiltrating low-grade gliomas. Neurosurgery. 2008;63:700–707. doi: 10.1227/01.NEU.0000325729.41085.73. [DOI] [PubMed] [Google Scholar]
  • 88.Smith JS, Chang EF, Lamborn KR, et al. Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol. 2008;26:1338–1345. doi: 10.1200/JCO.2007.13.9337. [DOI] [PubMed] [Google Scholar]
  • 89.Vecht CJ, Avezaat CJ, van Putten WL, Eijkenboom WM, Stefanko SZ. The influence of the extent of surgery on the neurological function and survival in malignant glioma. A retrospective analysis in 243 patients. J Neurol Neurosurg Psychiatry. 1990;53:466–471. doi: 10.1136/jnnp.53.6.466. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 90.Shibamoto Y, Yamashita J, Takahashi M, et al. Supratentorial malignant glioma: an analysis of radiation therapy in 178 cases. Radiother Oncol. 1990;18:9–17. doi: 10.1016/0167-8140(90)90018-r. [DOI] [PubMed] [Google Scholar]
  • 91.Curran WJ, Scott CB, Horton J, et al. Does extent of surgery influence outcome for astrocytoma with atypical or anaplastic foci (AAF)? A report from three Radiation Therapy Oncology Group (RTOG) trials. J Neurooncol. 1992;12:219–227. doi: 10.1007/BF00172709. [DOI] [PubMed] [Google Scholar]
  • 92.Simpson JR, Horton J, Scott C, et al. Influence of location and extent of surgical resection on survival of patients with glioblastoma multiforme: results of three consecutive Radiation Therapy Oncology Group (RTOG) clinical trials. Int J Radiat Oncol Biol Phys. 1993;26:239–244. doi: 10.1016/0360-3016(93)90203-8. [DOI] [PubMed] [Google Scholar]
  • 93.Dinapoli RP, Brown LD, Arusell RM, et al. Phase III comparative evaluation of PCNU and carmustine combined with radiation therapy for high-grade glioma. J Clin Oncol. 1993;11:1316–1321. doi: 10.1200/JCO.1993.11.7.1316. [DOI] [PubMed] [Google Scholar]
  • 94.Jeremic B, Grujicic D, Antunovic V, et al. Influence of extent of surgery and tumor location on treatment outcome of patients with glioblastoma multiforme treated with combined modality approach. J Neurooncol. 1994;21:177–185. doi: 10.1007/BF01052902. [DOI] [PubMed] [Google Scholar]
  • 95.Nitta T, Sato K. Prognostic implications of the extent of surgical resection in patients with intracranial malignant gliomas. Cancer. 1995;75:2727–2731. doi: 10.1002/1097-0142(19950601)75:11<2727::aid-cncr2820751115>3.0.co;2-h. [DOI] [PubMed] [Google Scholar]
  • 96.Barker FG, Prados MD, Chang SM, et al. Radiation response and survival time in patients with glioblastoma multiforme. J Neurosurg. 1996;84:442–448. doi: 10.3171/jns.1996.84.3.0442. [DOI] [PubMed] [Google Scholar]
  • 97.Brown PD, Maurer MJ, Rummans TA, et al. A prospective study of quality of life in adults with newly diagnosed high-grade gliomas: the impact of the extent of resection on quality of life and survival. Neurosurgery. 2005;57:495–504. doi: 10.1227/01.neu.0000170562.25335.c7. [DOI] [PubMed] [Google Scholar]
  • 98.Buckner JC, Schomberg PJ, McGinnis WL, et al. A phase III study of radiation therapy plus carmustine with or without recombinant interferon-alpha in the treatment of patients with newly diagnosed high-grade glioma. 2001;92:420–433. [DOI] [PubMed]
  • 99.Lamborn KR, Chang SM, Prados MD. Prognostic factors for survival of patients with glioblastoma: recursive partitioning analysis. Neuro-oncol. 2004;6:227–235. doi: 10.1215/S1152851703000620. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 100.Stark AM, Nabavi A, Mehdorn HM, Blomer U. Glioblastoma multiforme-report of 267 cases treated at a single institution. Surg Neurol. 2005;63:162–169. doi: 10.1016/j.surneu.2004.01.028. [DOI] [PubMed] [Google Scholar]
  • 101.Ushio Y, Kochi M, Hamada J, Kai Y, Nakamura H. Effect of surgical removal on survival and quality of life in patients with supratentorial glioblastoma. Neurol Med Chir (Tokyo) 2005;45:454–460. doi: 10.2176/nmc.45.454. [DOI] [PubMed] [Google Scholar]
  • 102.Duncan GG, Goodman GB, Ludgate CM, Rheaume DE. The treatment of adult supratentorial high grade astrocytomas. J Neurooncol. 1992;13:63–72. doi: 10.1007/BF00172947. [DOI] [PubMed] [Google Scholar]
  • 103.Hollerhage HG, Zumkeller M, Becker M, Dietz H. Influence of type and extent of surgery on early results and survival time in glioblastoma multiforme. Acta Neurochir (Wien) 1991;113:31–37. doi: 10.1007/BF01402111. [DOI] [PubMed] [Google Scholar]
  • 104.Huber A, Beran H, Becherer A, Prosenc N, Witzmann A. Supratentorial glioma: analysis of clinical and temporal parameters in 163 cases. Neurochirurgia (Stuttg) 1993;36:189–193. doi: 10.1055/s-2008-1053826. [DOI] [PubMed] [Google Scholar]
  • 105.Kowalczuk A, Macdonald RL, Amidei C, et al. Quantitative imaging study of extent of surgical resection and prognosis of malignant astrocytomas. Neurosurgery. 1997;41:1028–1036. doi: 10.1097/00006123-199711000-00004. [DOI] [PubMed] [Google Scholar]
  • 106.Levin VA, Yung WK, Bruner J, et al. Phase II study of accelerated fractionation radiation therapy with carboplatin followed by PCV chemotherapy for the treatment of anaplastic gliomas. Int J Radiat Oncol Biol Phys. 2002;53:58–66. doi: 10.1016/s0360-3016(01)02819-x. [DOI] [PubMed] [Google Scholar]
  • 107.Phillips TL, Levin VA, Ahn DK, et al. Evaluation of bromodeoxyuridine in glioblastoma multiforme: a Northern California Cancer Center Phase II study. Int J Radiat Oncol Biol Phys. 1991;21:709–714. doi: 10.1016/0360-3016(91)90690-6. [DOI] [PubMed] [Google Scholar]
  • 108.Pope WB, Sayre J, Perlina A, et al. MR imaging correlates of survival in patients with high-grade gliomas. AJNR Am J Neuroradiol. 2005;26:2466–2474. [PMC free article] [PubMed] [Google Scholar]
  • 109.Prados MD, Gutin PH, Phillips TL, et al. Highly anaplastic astrocytoma: a review of 357 patients treated between 1977 and 1989. Int J Radiat Oncol Biol Phys. 1992;23:3–8. doi: 10.1016/0360-3016(92)90537-r. [DOI] [PubMed] [Google Scholar]
  • 110.Puduvalli VK, Hashmi M, McAllister LD, et al. Anaplastic oligodendrogliomas: prognostic factors for tumor recurrence and survival. Oncology. 2003;65:259–266. doi: 10.1159/000074479. [DOI] [PubMed] [Google Scholar]
  • 111.Sandberg-Wollheim M, Malmstrom P, Stromblad LG, et al. A randomized study of chemotherapy with procarbazine, vincristine, and lomustine with and without radiation therapy for astrocytoma grades 3 and/or 4. Cancer. 1991;68:22–29. doi: 10.1002/1097-0142(19910701)68:1<22::aid-cncr2820680105>3.0.co;2-2. [DOI] [PubMed] [Google Scholar]
  • 112.Tortosa A, Vinolas N, Villa S, et al. Prognostic implication of clinical, radiologic, and pathologic features in patients with anaplastic gliomas. Cancer. 2003;97:1063–1071. doi: 10.1002/cncr.11120. [DOI] [PubMed] [Google Scholar]
  • 113.McGirt MJ, Chaichana KL, Gathinji M, et al. Independent association of extent of resection with survival in patients with malignant brain astrocytoma. J Neurosurg. 2009;110:156–162. doi: 10.3171/2008.4.17536. [DOI] [PubMed] [Google Scholar]
  • 114.Stummer W, Reulen HJ, Meinel T, et al. Extent of resection and survival in glioblastoma multiforme: identification of and adjustment for bias. Neurosurgery. 2008;62:564–576. doi: 10.1227/01.neu.0000317304.31579.17. [DOI] [PubMed] [Google Scholar]

Articles from Neurotherapeutics are provided here courtesy of Elsevier

RESOURCES