Independent association of extent of resection with survival in patients with malignant brain astrocytoma

Clinical article

View More View Less
  • Department of Neurosurgery and Oncology, and Neuro-Oncology Surgical Outcomes Research Laboratory, Johns Hopkins School of Medicine, Baltimore, Maryland
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00
Print or Print + Online

Object

With recent advances in the adjuvant treatment of malignant brain astrocytomas, it is increasingly debated whether extent of resection affects survival. In this study, the authors investigate this issue after primary and revision resection of these lesions.

Methods

The authors retrospectively reviewed the cases of 1215 patients who underwent surgery for malignant brain astrocytomas (World Health Organization [WHO] Grade III or IV) at a single institution from 1996 to 2006. Patients with deep-seated or unresectable lesions were excluded. Based on MR imaging results obtained < 48 hours after surgery, gross-total resection (GTR) was defined as no residual enhancement, near-total resection (NTR) as having thin rim enhancement of the resection cavity only, and subtotal resection (STR) as having residual nodular enhancement. The independent association of extent of resection and subsequent survival was assessed via a multivariate proportional hazards regression analysis.

Results

Magnetic resonance imaging studies were available for review in 949 cases. The mean age and mean Karnofsky Performance Scale (KPS) score at time of surgery were 51 ± 16 years and 80 ± 10, respectively. Surgery consisted of primary resection in 549 patients (58%) and revision resection for tumor recurrence in 400 patients (42%). The lesion was WHO Grade IV in 700 patients (74%) and Grade III in 249 (26%); there were 167 astrocytomas and 82 mixed oligoastrocytoma. Among patients who underwent resection, GTR, NTR, and STR were achieved in 330 (35%), 388 (41%), and 231 cases (24%), respectively. Adjusting for factors associated with survival (for example, age, KPS score, Gliadel and/or temozolomide use, and subsequent resection), GTR versus NTR (p < 0.05) and NTR versus STR (p < 0.05) were independently associated with improved survival after both primary and revision resection of glioblastoma multiforme (GBM). For primary GBM resection, the median survival after GTR, NTR, and STR was 13, 11, and 8 months, respectively. After revision resection, the median survival after GTR, NTR, and STR was 11, 9, and 5 months, respectively. Adjusting for factors associated with survival for WHO Grade III astrocytoma (age, KPS score, and revision resection), GTR versus STR (p < 0.05) was associated with improved survival. Gross-total resection versus NTR was not associated with an independent survival benefit in patients with WHO Grade III astrocytomas. The median survival after primary resection of WHO Grade III (mixed oligoastrocytomas excluded) for GTR, NTR, and STR was 58, 46, and 34 months, respectively.

Conclusions

In the authors' experience with both primary and secondary resection of malignant brain astrocytomas, increasing extent of resection was associated with improved survival independent of age, degree of disability, WHO grade, or subsequent treatment modalities used. The maximum extent of resection should be safely attempted while minimizing the risk of surgically induced neurological injury.

Abbreviations used in this paper:

AA = anaplastic astrocytoma; CI = confidence interval; GBM = glioblastoma multiforme; GTR = gross-total resection; KPS = Karnofsky Performance Scale; NTR = near-total resection; RR = relative risk; STR = subtotal resection; WHO = World Health Organization.

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00

Contributor Notes

Address correspondence to: Alfredo Quiñones-Hinojosa, M.D., Brain Tumor Stem Cell Laboratory, Department of Neurosurgery and Oncology, 1550 Orleans Street, Cancer Research Building II, Room 253, Baltimore, Maryland 21231. email: aquinon2@jhmi.edu.

Please include this information when citing this paper: publishedonline October 10, 2008; DOI: 10.3171/2008.4.17536.

  • 1

    Barker FG II, , Prados MD, , Chang SM, , Gutin PH, , Lamborn KR, & Larson DA, et al. : Radiation response and survival time in patients with glioblastoma multiforme. J Neurosurg 84:442 448, 1996

    • Search Google Scholar
    • Export Citation
  • 2

    Berman JI, , Berger MS, , Chung SW, , Nagarajan SS, & Henry RG: Accuracy of diffusion tensor magnetic resonance imaging tractography assessed using intraoperative subcortical stimulation mapping and magnetic source imaging. J Neurosurg 107:488494, 2007

    • Search Google Scholar
    • Export Citation
  • 3

    Brem H, , Piantadosi S, , Burger PC, , Walker M, , Selker R, & Vick NA, et al. : Placebo-controlled trial of safety and efficacy of intraoperative controlled delivery by biodegradable polymers of chemotherapy for recurrent gliomas. The Polymer-Brain Tumor Treatment Group Lancet 345:10081012, 1995

    • Search Google Scholar
    • Export Citation
  • 4

    Buckner JC: Factors influencing survival in high-grade gliomas. Semin Oncol 30:1014, 2003

  • 5

    Butowski N, , Lamborn KR, , Berger MS, , Prados MD, & Chang SM: Historical controls for phase II surgically based trials requiring gross total resection of glioblastoma multiforme. J Neurooncol 85:8794, 2007

    • Search Google Scholar
    • Export Citation
  • 6

    Chang SM, , Parney IF, , Huang W, , Anderson FA Jr, , Asher AL, & Bernstein M, et al. : Patterns of care for adults with newly diagnosed malignant glioma. JAMA 293:557564, 2005

    • Search Google Scholar
    • Export Citation
  • 7

    Claes A, , Idema AJ, & Wesseling P: Diffuse glioma growth: a guerilla war. Acta Neuropathol 114:443458, 2007

  • 8

    Curran WJ Jr, , Scott CB, , Horton J, , Nelson JS, , Weinstein AS, & Fischbach AJ, et al. : Recursive partitioning analysis of prognostic factors in three Radiation Therapy Oncology Group malignant glioma trials. J Natl Cancer Inst 85:704710, 1993

    • Search Google Scholar
    • Export Citation
  • 9

    Dandy WE: Removal of right cerebral hemisphere for certain tumors with hemiplegia. JAMA 90:823825, 1928

  • 10

    DeAngelis LM: Brain tumors. N Engl J Med 344:114123, 2001

  • 11

    Dinapoli RP, , Brown LD, , Arusell RM, , Earle JD, , O'Fallon JR, & Buckner JC, et al. : Phase III comparative evaluation of PCNU and carmustine combined with radiation therapy for highgrade glioma. J Clin Oncol 11:13161321, 1993

    • Search Google Scholar
    • Export Citation
  • 12

    Guggisberg AG, , Honma SM, , Findlay AM, , Dalal SS, , Kirsch HE, & Berger MS, et al. : Mapping functional connectivity in patients with brain lesions. Ann Neurol 63:193203, 2007

    • Search Google Scholar
    • Export Citation
  • 13

    Hentschel SJ, & Lang FF: Current surgical management of glioblastoma. Cancer J 9:113125, 2003

  • 14

    Hess KR: Extent of resection as a prognostic variable in the treatment of gliomas. J Neurooncol 42:227231, 1999

  • 15

    House MG, , Gonen M, , Jarnagin WR, , D'Angelica M, , Dematteo RP, & Fong Y, et al. : Prognostic significance of pathologic nodal status in patients with resected pancreatic cancer. J Gastrointest Surg 11:15491555, 2007

    • Search Google Scholar
    • Export Citation
  • 16

    Jackson RJ, , Fuller GN, , Abi-Said D, , Lang FF, , Gokaslan ZL, & Shi WM, et al. : Limitations of stereotactic biopsy in the initial management of gliomas. Neuro-oncol 3:193200, 2001

    • Search Google Scholar
    • Export Citation
  • 17

    Keles GE, , Chang EF, , Lamborn KR, , Tihan T, , Chang CJ, & Chang SM, 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 105:3440, 2006

    • Search Google Scholar
    • Export Citation
  • 18

    Lacroix M, , Abi-Said D, , Fourney DR, , Gokaslan ZL, , Shi W, & DeMonte F, et al. : A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 95:190198, 2001

    • Search Google Scholar
    • Export Citation
  • 19

    Lamborn KR, , Chang SM, & Prados MD: Prognostic factors for survival of patients with glioblastoma: recursive partitioning analysis. Neuro-oncol 6:227235, 2004

    • Search Google Scholar
    • Export Citation
  • 20

    Laws ER, , Parney IF, , Huang W, , Anderson F, , Morris AM, & Asher A, et al. : Survival following surgery and prognostic factors for recently diagnosed malignant glioma: data from the Glioma Outcomes Project. J Neurosurg 99:467473, 2003

    • Search Google Scholar
    • Export Citation
  • 21

    Lawson HC, , Sampath P, , Bohan E, , Park MC, , Hussain N, & Olivi A, et al. : Interstitial chemotherapy for malignant gliomas: the Johns Hopkins experience. J Neurooncol 83:6170, 2007

    • Search Google Scholar
    • Export Citation
  • 22

    Louis DN, , Ohgaki H, , Wiestler OD, , Cavenee WK, , Burger PC, & Jouvet A, et al. : The 2007 WHO Classification of Tumours of the Central Nervous System. Acta Neuropathol 114:97109, 2007

    • Search Google Scholar
    • Export Citation
  • 23

    Metcalfe SE, & Grant R: Biopsy versus resection for malignant glioma. Cochrane Database Syst Rev 3:CD002034, 2005

  • 24

    Muragaki Y, , Iseki H, , Maruyama T, , Kawamata T, , Yamane F, & Nakamura R, et al. : Usefulness of intraoperative magnetic resonance imaging for glioma surgery. Acta Neurochir Suppl 98:6775, 2006

    • Search Google Scholar
    • Export Citation
  • 25

    Nazzaro JM, & Neuwelt EA: The role of surgery in the management of supratentorial intermediate and high-grade astrocytomas in adults. J Neurosurg 73:331344, 1990

    • Search Google Scholar
    • Export Citation
  • 26

    Ng WH, , Wan GQ, & Too HP: Higher glioblastoma tumour burden reduces efficacy of chemotherapeutic agents: in vitro evidence. J Clin Neurosci 14:261266, 2007

    • Search Google Scholar
    • Export Citation
  • 27

    Pang BC, , Wan WH, , Lee CK, , Khu KJ, & Ng WH: The role of surgery in high-grade glioma–is surgical resection justified? A review of the current knowledge. Ann Acad Med Singapore 36:358363, 2007

    • Search Google Scholar
    • Export Citation
  • 28

    Pirzkall A, , Li X, , Oh J, , Chang S, , Berger MS, & Larson DA, et al. : 3D MRSI for resected high-grade gliomas before RT: tumor extent according to metabolic activity in relation to MRI. Int J Radiat Oncol Biol Phys 59:126137, 2004

    • Search Google Scholar
    • Export Citation
  • 29

    Pope WB, , Sayre J, , Perlina A, , Villablanca JP, , Mischel PS, & Cloughesy TF: MR imaging correlates of survival in patients with high-grade gliomas. AJNR Am J Neuroradiol 26:24662474, 2005

    • Search Google Scholar
    • Export Citation
  • 30

    Quigley MR, & Maroon JC: The relationship between survival and the extent of the resection in patients with supratentorial malignant gliomas. Neurosurgery 29:385389, 1991

    • Search Google Scholar
    • Export Citation
  • 31

    Schiffbauer H, , Berger MS, , Ferrari P, , Freudenstein D, , Rowley HA, & Roberts TP: Preoperative magnetic source imaging for brain tumor surgery: a quantitative comparison with intraoperative sensory and motor mapping. J Neurosurg 97:1333 1342, 2002

    • Search Google Scholar
    • Export Citation
  • 32

    Simpson JR, , Horton J, , Scott C, , Curran WJ, , Rubin P, & Fischbach J, 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 26:239244, 1993

    • Search Google Scholar
    • Export Citation
  • 33

    Sneed PK, , Gutin PH, , Larson DA, , Malec MK, , Phillips TL, & Prados MD, et al. : Patterns of recurrence of glioblastoma multiforme after external irradiation followed by implant boost. Int J Radiat Oncol Biol Phys 29:719727, 1994

    • Search Google Scholar
    • Export Citation
  • 34

    Stewart LA: Chemotherapy in adult high-grade glioma: a systematic review and meta-analysis of individual patient data from 12 randomised trials. Lancet 359:10111018, 2002

    • Search Google Scholar
    • Export Citation
  • 35

    Stupp R, , Mason WP, , van den Bent MJ, , Weller M, , Fisher B, & Taphoorn MJ, et al. : Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987 996, 2005

    • Search Google Scholar
    • Export Citation
  • 36

    Tait MJ, , Petrik V, , Loosemore A, , Bell BA, & Papadopoulos MC: Survival of patients with glioblastoma multiforme has not improved between 1993 and 2004: analysis of 625 cases. Br J Neurosurg 21:496500, 2007

    • Search Google Scholar
    • Export Citation
  • 37

    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 53:466471, 1990

    • Search Google Scholar
    • Export Citation
  • 38

    Walker JA, , Quinones-Hinojosa A, & Berger MS: Intraoperative speech mapping in 17 bilingual patients undergoing resection of a mass lesion. Neurosurgery 54:113118, 2004

    • Search Google Scholar
    • Export Citation
  • 39

    Westphal M, , Ram Z, , Riddle V, , Hilt D, & Bortey E: Gliadel wafer in initial surgery for malignant glioma: long-term followup of a multicenter controlled trial. Acta Neurochir (Wien) 148:269275, 2006

    • Search Google Scholar
    • Export Citation
  • 40

    Whittle IR, , Lyles S, & Walker M: Gliadel therapy given for first resection of malignant glioma: a single centre study of the potential use of Gliadel. Br J Neurosurg 17:352354, 2003

    • Search Google Scholar
    • Export Citation
  • 41

    Yoshimoto M, , Tada K, , Nishimura S, , Makita M, , Iwase T, & Kasumi F, et al. : Favourable long-term results after surgical removal of lung metastases of breast cancer. Breast Cancer Res Treat [epub ahead of print] 2007

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 2008 802 99
Full Text Views 521 85 3
PDF Downloads 305 30 2
EPUB Downloads 0 0 0