Skip to main content
Top
Published in: Journal of Neuro-Oncology 3/2014

01-12-2014 | Clinical Study

The butterfly effect on glioblastoma: is volumetric extent of resection more effective than biopsy for these tumors?

Authors: Kaisorn L. Chaichana, Ignacio Jusue-Torres, Ana Maria Lemos, Aaron Gokaslan, Eibar Ernesto Cabrera-Aldana, Ahmed Ashary, Alessandro Olivi, Alfredo Quinones-Hinojosa

Published in: Journal of Neuro-Oncology | Issue 3/2014

Login to get access

Abstract

A subset of patients with glioblastoma (GBM) have butterfly GBM (bGBM) that involve both cerebral hemispheres by crossing the corpus callosum. The prognoses, as well as the effectiveness of surgery and adjuvant therapy, are unclear because studies are few and limited. The goals of this study were to: (1) determine if bGBM have worse outcomes than patients with non-bGBM, (2) determine if surgery is more effective than biopsy, and (3) identify factors independently associated with improved outcomes for these patients. Adult patients who underwent surgery for a newly diagnosed primary GBM at an academic tertiary-care institution between 2007 and 2012 were retrospectively reviewed and tumors were volumetrically measured. Of the 336 patients with newly diagnosed GBM who were operated on, 48 (14 %) presented with bGBM, where 29 (60 %) and 19 (40 %) underwent surgical resection and biopsy, respectively. In multivariate analysis, a bGBM was independently associated with poorer survival [HR (95 % CI) 1.848 (1.250–2.685), p < 0.003]. In matched-pair analysis, patients who underwent surgical resection had improved median survival than biopsy patients (7.0 vs. 3.5 months, p = 0.03). In multivariate analysis, increasing percent resection [HR (95 % CI) 0.987 (0.977–0.997), p = 0.01], radiation [HR (95 % CI) 0.431 (0.225–0.812), p = 0.009], and temozolomide [HR (95 % CI) 0.413 (0.212–0. 784), p = 0.007] were each independently associated with prolonged survival among patients with bGBM. This present study shows that while patients with bGBM have poorer prognoses compared to non-bGBM, these patients can also benefit from aggressive treatments including debulking surgery, maximal safe surgical resection, temozolomide chemotherapy, and radiation therapy.
Literature
1.
go back to reference Chaichana K, Parker S, Olivi A, Quinones-Hinojosa A (2010) A proposed classification system that projects outcomes based on preoperative variables for adult patients with glioblastoma multiforme. J Neurosurg 112:997–1004PubMedCrossRef Chaichana K, Parker S, Olivi A, Quinones-Hinojosa A (2010) A proposed classification system that projects outcomes based on preoperative variables for adult patients with glioblastoma multiforme. J Neurosurg 112:997–1004PubMedCrossRef
2.
go back to reference Chaichana KL, Chaichana KK, Olivi A, Weingart JD, Bennett R, Brem H, Quinones-Hinojosa A (2011) Surgical outcomes for older patients with glioblastoma multiforme: preoperative factors associated with decreased survival. Clinical article. J Neurosurg 114:587–594PubMedCentralPubMedCrossRef Chaichana KL, Chaichana KK, Olivi A, Weingart JD, Bennett R, Brem H, Quinones-Hinojosa A (2011) Surgical outcomes for older patients with glioblastoma multiforme: preoperative factors associated with decreased survival. Clinical article. J Neurosurg 114:587–594PubMedCentralPubMedCrossRef
3.
go back to reference Chaichana KL, Halthore AN, Parker SL, Olivi A, Weingart JD, Brem H, Quinones-Hinojosa A (2011) Factors involved in maintaining prolonged functional independence following supratentorial glioblastoma resection. Clinical article. J Neurosurg 114:604–612PubMedCentralPubMedCrossRef Chaichana KL, Halthore AN, Parker SL, Olivi A, Weingart JD, Brem H, Quinones-Hinojosa A (2011) Factors involved in maintaining prolonged functional independence following supratentorial glioblastoma resection. Clinical article. J Neurosurg 114:604–612PubMedCentralPubMedCrossRef
4.
go back to reference Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, Lang FF, McCutcheon IE, Hassenbusch SJ, Holland E, Hess K, Michael C, Miller D, Sawaya R (2001) A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 95:190–198PubMedCrossRef Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, Lang FF, McCutcheon IE, Hassenbusch SJ, Holland E, Hess K, Michael C, Miller D, Sawaya R (2001) A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 95:190–198PubMedCrossRef
5.
go back to reference Laws ER, Parney IF, Huang W, Anderson F, Morris AM, Asher A, Lillehei KO, Bernstein M, Brem H, Sloan A, Berger MS, Chang S (2003) Survival following surgery and prognostic factors for recently diagnosed malignant glioma: data from the Glioma Outcomes Project. J Neurosurg 99:467–473PubMedCrossRef Laws ER, Parney IF, Huang W, Anderson F, Morris AM, Asher A, Lillehei KO, Bernstein M, Brem H, Sloan A, Berger MS, Chang S (2003) Survival following surgery and prognostic factors for recently diagnosed malignant glioma: data from the Glioma Outcomes Project. J Neurosurg 99:467–473PubMedCrossRef
6.
go back to reference Sanai N, Polley MY, McDermott MW, Parsa AT, Berger MS (2011) An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg 115:3–8PubMedCrossRef Sanai N, Polley MY, McDermott MW, Parsa AT, Berger MS (2011) An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg 115:3–8PubMedCrossRef
7.
go back to reference Dziurzynski K, Blas-Boria D, Suki D, Cahill DP, Prabhu SS, Puduvalli V, Levine N (2012) Butterfly glioblastomas: a retrospective review and qualitative assessment of outcomes. J Neurooncol 109:555–563PubMedCentralPubMedCrossRef Dziurzynski K, Blas-Boria D, Suki D, Cahill DP, Prabhu SS, Puduvalli V, Levine N (2012) Butterfly glioblastomas: a retrospective review and qualitative assessment of outcomes. J Neurooncol 109:555–563PubMedCentralPubMedCrossRef
8.
go back to reference Parsa AT, Wachhorst S, Lamborn KR, Prados MD, McDermott MW, Berger MS, Chang SM (2005) Prognostic significance of intracranial dissemination of glioblastoma multiforme in adults. J Neurosurg 102:622–628PubMedCrossRef Parsa AT, Wachhorst S, Lamborn KR, Prados MD, McDermott MW, Berger MS, Chang SM (2005) Prognostic significance of intracranial dissemination of glioblastoma multiforme in adults. J Neurosurg 102:622–628PubMedCrossRef
9.
go back to reference Balana C, Capellades J, Teixidor P, Roussos I, Ballester R, Cuello M, Arellano A, Florensa R, Rosell R (2007) Clinical course of high-grade glioma patients with a “biopsy-only” surgical approach: a need for individualised treatment. Clin Transl Oncol 9:797–803PubMedCrossRef Balana C, Capellades J, Teixidor P, Roussos I, Ballester R, Cuello M, Arellano A, Florensa R, Rosell R (2007) Clinical course of high-grade glioma patients with a “biopsy-only” surgical approach: a need for individualised treatment. Clin Transl Oncol 9:797–803PubMedCrossRef
11.
go back to reference Arora M, Praharaj SK (2007) Butterfly glioma of corpus callosum presenting as catatonia. World J Biol Psychiatry 8:54–55PubMedCrossRef Arora M, Praharaj SK (2007) Butterfly glioma of corpus callosum presenting as catatonia. World J Biol Psychiatry 8:54–55PubMedCrossRef
12.
go back to reference Galldiks N, Schroeter M, Fink GR, Kracht LW (2010) Interesting image. PET imaging of a butterfly glioblastoma. Clin Nucl Med 35:49–50PubMedCrossRef Galldiks N, Schroeter M, Fink GR, Kracht LW (2010) Interesting image. PET imaging of a butterfly glioblastoma. Clin Nucl Med 35:49–50PubMedCrossRef
13.
go back to reference Hammersen S, Brock M, Cervos-Navarro J (1998) Adult neuronal ceroid lipofuscinosis with clinical findings consistent with a butterfly glioma. Case report. J Neurosurg 88:314–318PubMedCrossRef Hammersen S, Brock M, Cervos-Navarro J (1998) Adult neuronal ceroid lipofuscinosis with clinical findings consistent with a butterfly glioma. Case report. J Neurosurg 88:314–318PubMedCrossRef
14.
go back to reference Osawa A, Maeshima S, Kubo K, Itakura T (2006) Neuropsychological deficits associated with a tumour in the posterior corpus callosum: a report of two cases. Brain Inj 20:673–676PubMedCrossRef Osawa A, Maeshima S, Kubo K, Itakura T (2006) Neuropsychological deficits associated with a tumour in the posterior corpus callosum: a report of two cases. Brain Inj 20:673–676PubMedCrossRef
15.
go back to reference Roche S, Godward S, Middleton A, Lane RJ (1993) Bifrontal glioma presenting as a gross movement disorder. Mov Disord 8:120–122PubMedCrossRef Roche S, Godward S, Middleton A, Lane RJ (1993) Bifrontal glioma presenting as a gross movement disorder. Mov Disord 8:120–122PubMedCrossRef
16.
go back to reference Witoonpanich P, Bamrungrak K, Jinawath A, Wongwaisayawan S, Phudhichareonrat S, Witoonpanich R (2011) Glioblastoma multiforme at the corpus callosum with spinal leptomeningeal metastasis. Clin Neurol Neurosurg 113:407–410PubMedCrossRef Witoonpanich P, Bamrungrak K, Jinawath A, Wongwaisayawan S, Phudhichareonrat S, Witoonpanich R (2011) Glioblastoma multiforme at the corpus callosum with spinal leptomeningeal metastasis. Clin Neurol Neurosurg 113:407–410PubMedCrossRef
17.
go back to reference Zakrzewska M, Szybka M, Zakrzewski K, Biernat W, Kordek R, Rieske P, Golanska E, Zawlik I, Piaskowski S, Liberski PP (2007) Diverse molecular pattern in a bihemispheric glioblastoma (butterfly glioma) in a 16-year-old boy. Cancer Genet Cytogenet 177:125–130PubMedCrossRef Zakrzewska M, Szybka M, Zakrzewski K, Biernat W, Kordek R, Rieske P, Golanska E, Zawlik I, Piaskowski S, Liberski PP (2007) Diverse molecular pattern in a bihemispheric glioblastoma (butterfly glioma) in a 16-year-old boy. Cancer Genet Cytogenet 177:125–130PubMedCrossRef
18.
go back to reference Stelzer KJ, Sauvé KI, Spence AM, Griffin TW, Berger MS (1997) Corpus callosum involvement as a prognostic factor for patients with high-grade astrocytoma. Int J Radiat Oncol Biol Phys 38:27–30CrossRef Stelzer KJ, Sauvé KI, Spence AM, Griffin TW, Berger MS (1997) Corpus callosum involvement as a prognostic factor for patients with high-grade astrocytoma. Int J Radiat Oncol Biol Phys 38:27–30CrossRef
19.
go back to reference Matsukado Y, Maccarty CS, Kernohan JW (1961) The growth of glioblastoma multiforme (astrocytomas, grades 3 and 4) in neurosurgical practice. J Neurosurg 18:636–644PubMedCrossRef Matsukado Y, Maccarty CS, Kernohan JW (1961) The growth of glioblastoma multiforme (astrocytomas, grades 3 and 4) in neurosurgical practice. J Neurosurg 18:636–644PubMedCrossRef
20.
go back to reference Devaux BC, O’Fallon JR, Kelly PJ (1993) Resection, biopsy, and survival in malignant glial neoplasms. A retrospective study of clinical parameters, therapy, and outcome. J Neurosurg 78:767–775PubMedCrossRef Devaux BC, O’Fallon JR, Kelly PJ (1993) Resection, biopsy, and survival in malignant glial neoplasms. A retrospective study of clinical parameters, therapy, and outcome. J Neurosurg 78:767–775PubMedCrossRef
21.
go back to reference Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol (Berl) 114:97–109CrossRef Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol (Berl) 114:97–109CrossRef
22.
go back to reference Kleihues P, Louis DN, Scheithauer BW, Rorke LB, Reifenberger G, Burger PC, Cavenee WK (2002) The WHO classification of tumors of the nervous system. J Neuropathol Exp Neurol 61:215–225 discussion 226–229PubMed Kleihues P, Louis DN, Scheithauer BW, Rorke LB, Reifenberger G, Burger PC, Cavenee WK (2002) The WHO classification of tumors of the nervous system. J Neuropathol Exp Neurol 61:215–225 discussion 226–229PubMed
23.
go back to reference Chaichana KL, Jusue-Torres I, Navarro-Ramirez R, Raza SM, Pascual-Gallego M, Ibrahim A, Hernandez-Hermann M, Gomez L, Ye X, Weingart JD, Olivi A, Blakeley J, Gallia GL, Lim M, Brem H, Quinones-Hinojosa A (2014) Establishing percent resection and residual volume thresholds affecting survival and recurrence for patients with newly diagnosed intracranial glioblastoma. Neuro Oncol 16:113–122PubMedCrossRef Chaichana KL, Jusue-Torres I, Navarro-Ramirez R, Raza SM, Pascual-Gallego M, Ibrahim A, Hernandez-Hermann M, Gomez L, Ye X, Weingart JD, Olivi A, Blakeley J, Gallia GL, Lim M, Brem H, Quinones-Hinojosa A (2014) Establishing percent resection and residual volume thresholds affecting survival and recurrence for patients with newly diagnosed intracranial glioblastoma. Neuro Oncol 16:113–122PubMedCrossRef
24.
go back to reference Chaichana KL, Cabrera-Aldana E, Jusue-Torres I, Wijesekera O, Olivi A, Rahman M, Quinones-Hinojosa A (2014) When gross total resection of a glioblastoma is possible, how much resection should be achieved? World Neurosurg (in press) Chaichana KL, Cabrera-Aldana E, Jusue-Torres I, Wijesekera O, Olivi A, Rahman M, Quinones-Hinojosa A (2014) When gross total resection of a glioblastoma is possible, how much resection should be achieved? World Neurosurg (in press)
25.
26.
go back to reference Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996PubMedCrossRef Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996PubMedCrossRef
27.
go back to reference Chaichana KL, McGirt MJ, Frazier J, Attenello F, Guerrero-Cazares H, Quinones-Hinojosa A (2008) Relationship of glioblastoma multiforme to the lateral ventricles predicts survival following tumor resection. J Neurooncol 89:219–224PubMedCrossRef Chaichana KL, McGirt MJ, Frazier J, Attenello F, Guerrero-Cazares H, Quinones-Hinojosa A (2008) Relationship of glioblastoma multiforme to the lateral ventricles predicts survival following tumor resection. J Neurooncol 89:219–224PubMedCrossRef
28.
go back to reference Lamborn KR, Chang SM, Prados MD (2004) Prognostic factors for survival of patients with glioblastoma: recursive partitioning analysis. Neuro Oncol 6:227–235PubMedCentralPubMedCrossRef Lamborn KR, Chang SM, Prados MD (2004) Prognostic factors for survival of patients with glioblastoma: recursive partitioning analysis. Neuro Oncol 6:227–235PubMedCentralPubMedCrossRef
29.
go back to reference Hart MG, Grant R, Garside R, Rogers G, Somerville M, Stein K (2008) Temozolomide for high grade glioma. Cochrane Database Syst Rev CD007415 Hart MG, Grant R, Garside R, Rogers G, Somerville M, Stein K (2008) Temozolomide for high grade glioma. Cochrane Database Syst Rev CD007415
30.
go back to reference Genc M, Zorlu AF, Atahan IL (2000) Accelerated hyperfractionated radiotherapy in supratentorial malignant astrocytomas. Radiother Oncol 56:233–238PubMedCrossRef Genc M, Zorlu AF, Atahan IL (2000) Accelerated hyperfractionated radiotherapy in supratentorial malignant astrocytomas. Radiother Oncol 56:233–238PubMedCrossRef
31.
go back to reference Kallenberg K, Goldmann T, Menke J, Strik H, Bock HC, Stockhammer F, Buhk JH, Frahm J, Dechent P, Knauth M (2013) Glioma infiltration of the corpus callosum: early signs detected by DTI. J Neurooncol 112:217–222PubMedCentralPubMedCrossRef Kallenberg K, Goldmann T, Menke J, Strik H, Bock HC, Stockhammer F, Buhk JH, Frahm J, Dechent P, Knauth M (2013) Glioma infiltration of the corpus callosum: early signs detected by DTI. J Neurooncol 112:217–222PubMedCentralPubMedCrossRef
32.
go back to reference Chaichana KL, Garzon-Muvdi T, Parker S, Weingart JD, Olivi A, Bennett R, Brem H, Quinones-Hinojosa A (2011) Supratentorial glioblastoma multiforme: the role of surgical resection versus biopsy among older patients. Ann Surg Oncol 18:239–245PubMedCrossRef Chaichana KL, Garzon-Muvdi T, Parker S, Weingart JD, Olivi A, Bennett R, Brem H, Quinones-Hinojosa A (2011) Supratentorial glioblastoma multiforme: the role of surgical resection versus biopsy among older patients. Ann Surg Oncol 18:239–245PubMedCrossRef
33.
go back to reference Chaichana KL, Parker SL, Mukherjee D, Cheng JS, Gokaslan ZL, McGirt MJ (2011) Assessment of the extent of surgical resection as a predictor of survival in patients with primary osseous spinal neoplasms. Clin Neurosurg 58:117–121PubMedCrossRef Chaichana KL, Parker SL, Mukherjee D, Cheng JS, Gokaslan ZL, McGirt MJ (2011) Assessment of the extent of surgical resection as a predictor of survival in patients with primary osseous spinal neoplasms. Clin Neurosurg 58:117–121PubMedCrossRef
34.
go back to reference Chaichana KL, Parker SL, Olivi A, Quinones-Hinojosa A (2009) Long-term seizure outcomes in adult patients undergoing primary resection of malignant brain astrocytomas. Clinical article. J Neurosurg 111:282–292PubMedCrossRef Chaichana KL, Parker SL, Olivi A, Quinones-Hinojosa A (2009) Long-term seizure outcomes in adult patients undergoing primary resection of malignant brain astrocytomas. Clinical article. J Neurosurg 111:282–292PubMedCrossRef
35.
go back to reference Chaichana KL, Zadnik P, Weingart JD, Olivi A, Gallia GL, Blakeley J, Lim M, Brem H, Quinones-Hinojosa A (2012) Multiple resections for patients with glioblastoma: prolonging survival. J Neurosurg 118(4):812–820PubMedCentralPubMedCrossRef Chaichana KL, Zadnik P, Weingart JD, Olivi A, Gallia GL, Blakeley J, Lim M, Brem H, Quinones-Hinojosa A (2012) Multiple resections for patients with glioblastoma: prolonging survival. J Neurosurg 118(4):812–820PubMedCentralPubMedCrossRef
36.
go back to reference Chaichana KL, Zaidi H, Pendleton C, McGirt MJ, Grossman R, Weingart JD, Olivi A, Quinones-Hinojosa A, Brem H (2011) The efficacy of carmustine wafers for older patients with glioblastoma multiforme: prolonging survival. Neurol Res 33:759–764PubMedCrossRef Chaichana KL, Zaidi H, Pendleton C, McGirt MJ, Grossman R, Weingart JD, Olivi A, Quinones-Hinojosa A, Brem H (2011) The efficacy of carmustine wafers for older patients with glioblastoma multiforme: prolonging survival. Neurol Res 33:759–764PubMedCrossRef
37.
go back to reference Keles GE, Anderson B, Berger MS (1999) The effect of extent of resection on time to tumor progression and survival in patients with glioblastoma multiforme of the cerebral hemisphere. Surg Neurol 52:371–379PubMedCrossRef Keles GE, Anderson B, Berger MS (1999) The effect of extent of resection on time to tumor progression and survival in patients with glioblastoma multiforme of the cerebral hemisphere. Surg Neurol 52:371–379PubMedCrossRef
38.
go back to reference McGirt MJ, Chaichana KL, Gathinji M, Attenello FJ, Than K, Olivi A, Weingart JD, Brem H, Quinones-Hinojosa AR (2009) Independent association of extent of resection with survival in patients with malignant brain astrocytoma. J Neurosurg 110:156–162PubMedCrossRef McGirt MJ, Chaichana KL, Gathinji M, Attenello FJ, Than K, Olivi A, Weingart JD, Brem H, Quinones-Hinojosa AR (2009) Independent association of extent of resection with survival in patients with malignant brain astrocytoma. J Neurosurg 110:156–162PubMedCrossRef
39.
go back to reference McGirt MJ, Mukherjee D, Chaichana KL, Than KD, Weingart JD, Quinones-Hinojosa A (2009) Association of surgically acquired motor and language deficits on overall survival after resection of glioblastoma multiforme. Neurosurgery 65:463–469 discussion 469–470PubMedCrossRef McGirt MJ, Mukherjee D, Chaichana KL, Than KD, Weingart JD, Quinones-Hinojosa A (2009) Association of surgically acquired motor and language deficits on overall survival after resection of glioblastoma multiforme. Neurosurgery 65:463–469 discussion 469–470PubMedCrossRef
40.
go back to reference Chang SM, Parney IF, McDermott M, Barker FG 2nd, Schmidt MH, Huang W, Laws ER Jr, Lillehei KO, Bernstein M, Brem H, Sloan AE, Berger M (2003) Perioperative complications and neurological outcomes of first and second craniotomies among patients enrolled in the Glioma Outcome Project. J Neurosurg 98:1175–1181PubMedCrossRef Chang SM, Parney IF, McDermott M, Barker FG 2nd, Schmidt MH, Huang W, Laws ER Jr, Lillehei KO, Bernstein M, Brem H, Sloan AE, Berger M (2003) Perioperative complications and neurological outcomes of first and second craniotomies among patients enrolled in the Glioma Outcome Project. J Neurosurg 98:1175–1181PubMedCrossRef
41.
go back to reference Ramakrishna R, Barber J, Kennedy G, Rizvi A, Goodkin R, Winn RH, Ojemann GA, Berger MS, Spence AM, Rostomily RC (2010) Imaging features of invasion and preoperative and postoperative tumor burden in previously untreated glioblastoma: correlation with survival. Surg Neurol Int 1 Ramakrishna R, Barber J, Kennedy G, Rizvi A, Goodkin R, Winn RH, Ojemann GA, Berger MS, Spence AM, Rostomily RC (2010) Imaging features of invasion and preoperative and postoperative tumor burden in previously untreated glioblastoma: correlation with survival. Surg Neurol Int 1
42.
go back to reference Sawaya R, Hammoud M, Schoppa D, Hess KR, Wu SZ, Shi WM, Wildrick DM (1998) Neurosurgical outcomes in a modern series of 400 craniotomies for treatment of parenchymal tumors. Neurosurgery 42:1044–1055 discussion 1055–1056PubMedCrossRef Sawaya R, Hammoud M, Schoppa D, Hess KR, Wu SZ, Shi WM, Wildrick DM (1998) Neurosurgical outcomes in a modern series of 400 craniotomies for treatment of parenchymal tumors. Neurosurgery 42:1044–1055 discussion 1055–1056PubMedCrossRef
43.
go back to reference Ferroli P, Schiariti M, Finocchiaro G, Salmaggi A, Castiglione M, Acerbi F, Tringali G, Farinotti M, Broggi M, Roberto C, Maccagnano E, Broggi G (2013) Operability of glioblastomas: “sins of action” versus “sins of non-action”. Neurol Sci 34(12):2107–2116PubMedCrossRef Ferroli P, Schiariti M, Finocchiaro G, Salmaggi A, Castiglione M, Acerbi F, Tringali G, Farinotti M, Broggi M, Roberto C, Maccagnano E, Broggi G (2013) Operability of glioblastomas: “sins of action” versus “sins of non-action”. Neurol Sci 34(12):2107–2116PubMedCrossRef
44.
go back to reference Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JE, Hau P, Mirimanoff RO, Cairncross JG, Janzer RC, Stupp R (2005) MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352:997–1003PubMedCrossRef Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JE, Hau P, Mirimanoff RO, Cairncross JG, Janzer RC, Stupp R (2005) MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352:997–1003PubMedCrossRef
45.
go back to reference Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Siu IM, Gallia GL, Olivi A, McLendon R, Rasheed BA, Keir S, Nikolskaya T, Nikolsky Y, Busam DA, Tekleab H, Diaz LA Jr, Hartigan J, Smith DR, Strausberg RL, Marie SK, Shinjo SM, Yan H, Riggins GJ, Bigner DD, Karchin R, Papadopoulos N, Parmigiani G, Vogelstein B, Velculescu VE, Kinzler KW (2008) An integrated genomic analysis of human glioblastoma multiforme. Science 321:1807–1812PubMedCentralPubMedCrossRef Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Siu IM, Gallia GL, Olivi A, McLendon R, Rasheed BA, Keir S, Nikolskaya T, Nikolsky Y, Busam DA, Tekleab H, Diaz LA Jr, Hartigan J, Smith DR, Strausberg RL, Marie SK, Shinjo SM, Yan H, Riggins GJ, Bigner DD, Karchin R, Papadopoulos N, Parmigiani G, Vogelstein B, Velculescu VE, Kinzler KW (2008) An integrated genomic analysis of human glioblastoma multiforme. Science 321:1807–1812PubMedCentralPubMedCrossRef
46.
go back to reference Gerber NK, Goenka A, Turcan S, Reyngold M, Makarov V, Kannan K, Beal K, Omuro A, Yamada Y, Gutin P, Brennan CW, Huse JT, Chan TA (2014) Transcriptional diversity of long-term glioblastoma survivors. Neuro Oncol 16(9):1186–1195PubMedCrossRef Gerber NK, Goenka A, Turcan S, Reyngold M, Makarov V, Kannan K, Beal K, Omuro A, Yamada Y, Gutin P, Brennan CW, Huse JT, Chan TA (2014) Transcriptional diversity of long-term glioblastoma survivors. Neuro Oncol 16(9):1186–1195PubMedCrossRef
Metadata
Title
The butterfly effect on glioblastoma: is volumetric extent of resection more effective than biopsy for these tumors?
Authors
Kaisorn L. Chaichana
Ignacio Jusue-Torres
Ana Maria Lemos
Aaron Gokaslan
Eibar Ernesto Cabrera-Aldana
Ahmed Ashary
Alessandro Olivi
Alfredo Quinones-Hinojosa
Publication date
01-12-2014
Publisher
Springer US
Published in
Journal of Neuro-Oncology / Issue 3/2014
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI
https://doi.org/10.1007/s11060-014-1597-9

Other articles of this Issue 3/2014

Journal of Neuro-Oncology 3/2014 Go to the issue