Biopsy versus resection in the management of malignant gliomas: a systematic review and meta-analysis

A review

Restricted access

Object

The aim of this study was to answer the question whether quality of life and progression-free and overall survival are increased in adults with supratentorial malignant glioma who are treated with cytoreductive resection as compared with those who only undergo biopsy.

Methods

A literature search of the electronic databases MEDLINE, EMBASE, and CENTRAL was performed to identify relevant studies published before May 2008. Hand-searching of reference lists of the identified studies and relevant review articles was also performed. A study was considered eligible, regardless of study design (prospective or retrospective), if: 1) quality of life and/or progression-free and/or overall survival was compared among adult patients undergoing biopsy or resection, and 2) patient age and Karnofsky Performance Scale scores were not significantly different among the 2 groups compared.

Results

One randomized controlled trial and 4 retrospective studies (involving a total of 1111 patients) were found eligible for this systematic review. A meta-analysis of the eligible studies demonstrated a significant increase in overall survival in the patients treated with resection instead of biopsy (hazard ratio 0.61, 95% CI 0.52–0.71, p < 0.0001, fixed-effect model). Although statistical pooling was not feasible, the available data suggest that quality of life was increased in patients treated with resection rather than biopsy, while there did not seem to be any significant difference in progression-free survival between the 2 groups.

Conclusions

Based on the best available evidence, it appears that cytoreductive resection in adults with supratentorial malignant glioma is associated with improved overall survival as compared with biopsy. However, well-designed prospective studies are needed for more solid conclusions to be drawn.

Abbreviations used in this paper: CENTRAL = Cochrane Central Register of Controlled Trials; HR = hazard ratio; ICP = intracranial pressure; KPS = Karnofsky Performance Scale; QOL = quality of life.

Article Information

Address correspondence to: Abraham Tsitlakidis, M.D., M.Sc., First Department of Neurosurgery, AHEPA University Hospital, Aristotle University of Thessaloniki, Stilponos Kyriakidi 1, 54636, Thessaloniki, Greece. email: abrahamtsitlakidis@yahoo.gr.

Please include this information when citing this paper: published online September 11, 2009; DOI: 10.3171/2009.7.JNS09758.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Flowchart illustrating the steps of the systematic review and meta-analysis. n = number of studies.

  • View in gallery

    Forest plot of quantitative synthesis of HRs with all the studies that were included in the meta-analysis. The position of the rectangles corresponds to the value of the effect measure for each study, their size to its respective weight, and the horizontal lines correspond to the 95% CI. The position of the diamond (dashed line) corresponds to the value of the resultant effect measure and its left and right angles to its 95% CI. An HR < 1 favors resection. An HR > 1 favors biopsy (inverse variance fixed-effect model).

  • View in gallery

    Funnel plot for the evaluation of publication bias. The vertical line corresponds to the resultant effect measure and the sloping lines to its confidence limits. Asymmetry in the allocation of the studies is an indication of publication bias (inverse variance fixed-effect model).

  • View in gallery

    Trim-and-fill funnel plot for the evaluation of the influence of publication bias in the results of the quantitative synthesis. The vertical continuous line corresponds to the meta-analysis outcome with (only) the original studies included, the empty circle to the hypothetical study that counterbalances the publication bias, and the vertical dashed line the meta-analysis outcome after the imputation of this study.

  • View in gallery

    Forest plots of quantitative synthesis of HR with the exclusion of the studies in which the influence of performance bias was dubious and/or the only outcome data were the Kaplan-Meier curves (A), and of HRs of studies with Grade 4/IV gliomas (B), Grade III and IV gliomas (inverse variance fixed effect model) (C), elderly patients (D), and wide range of ages (E). Inverse variance fixed-effect model (A, C, and E), and inverse variance random effects model (B and D).

References

1

Abramoff MDMagelhaes PJRam SJ: Image processing with ImageJ. Biophotonics International 11:36422004

2

Ammirati MVick NLiao YLCiric IMikhael M: Effect of the extent of surgical resection on survival and quality of life in patients with supratentorial glioblastomas and anaplastic astrocytomas. Neurosurgery 21:2012061987

3

Andreou JGeorge AEWise Ade Leon MKrieueff IIRansohoff J: CT prognostic criteria of survival after malignant glioma surgery. AJNR Am J Neuroradiol 4:4884901983

4

Aydin HSillenberg Ivon Lieven H: Patterns of failure following CT-based 3-D irradiation for malignant glioma. Strahlenther Onkol 177:4244312001

5

Barnholtz-Sloan JSWilliams VLMaldonado JLShahani DStockwell HGChamberlain M: Patterns of care and outcomes among elderly individuals with primary malignant astrocytoma. J Neurosurg 108:6426482008

6

Bauman GSIno YUeki KZlatescu MCFisher BJMacdonald DR: Allelic loss of chromosome 1p and radiotherapy plus chemotherapy in patients with oligodendrogliomas. Int J Radiat Oncol Biol Phys 48:8258302000

7

Bax LYu LMIkeda NTsuruta HMoons KGM: Development and validation of MIX: comprehensive free software for meta-analysis of causal research data. BMC Med Res Methodol 6:502006

8

Black P: Management of malignant glioma: role of surgery in relation to multimodality therapy. J Neurovirol 4:2272361998

9

Brandes AACompostella ABlatt VTosoni A: Glioblastoma in the elderly: current and future trends. Crit Rev Oncol Hematol 60:2562662006

10

Brandes AAMonfardini S: The treatment of elderly patients with high-grade gliomas. Semin Oncol 30:58622003

11

Buckner JC: Factors influencing survival in high-grade gliomas. Semin Oncol 30:10142003

12

Burger PCGreen SB: Patient age, histologic features, and length of survival in patients with glioblastoma multiforme. Cancer 59:161716251987

13

Burger PCVogel FSGreen SBStrike TA: Glioblastoma multiforme and anaplastic astrocytoma: pathologic criteria and prognostic implications. Cancer 56:110611111985

14

Burger PCVollmer RT: Histologic factors of prognostic significance in the glioblastoma multiforme. Cancer 46:117911861980

15

Burton ECPrados MD: Malignant gliomas. Curr Treat Options Oncol 1:4594682000

16

Byar DPGreen SBStrike TAPrognostic factors for malignant glioma. Walker MD: Oncology of the Nervous System BostonMartinus Nijhoff1983. 379395

17

CBTRUS: ChicagoCentral Brain Tumor Registry of the United States2008

18

Chang CHHorton JSchoenfeld DSalazer OPerez-Tamayo RKramer S: Comparison of postoperative radiotherapy and combined postoperative radiotherapy and chemotherapy in the multidisciplinary management of malignant gliomas. A joint Radiation Therapy Oncology Group and Eastern Cooperative Oncology Group study. Cancer 52:99710071983

19

Coffey RJLunsford LDTaylor FH: Survival after stereotactic biopsy of malignant gliomas. Neurosurgery 22:4654731988

20

Cox DR: Regression models and life tables. J R Stat Soc (B) 34:1872201972

21

Croteau DMikkelsen T: Adults with newly diagnosed high-grade gliomas. Curr Treat Options Oncol 2:5075152001

22

Curran WJ JrScott CBHorton JNelson JSWeinstein ASFischbach AJ: Recursive partitioning analysis of prognostic factors in three Radiation Therapy Oncology Group malignant glioma trials. J Natl Cancer Inst 85:7047101993

23

Daumas-Duport CScheithauer BO'Fallon JKelly P: Grading of astrocytomas. A simple and reproducible method. Cancer 62:215221651988

24

Davis LMartin JGoldstein SLAshkenazy M: A study of 211 patients with verified glioblastoma multiforme. J Neurosurg 6:33441949

25

Deeks JJAltman DGBradburn MJStatistical methods for examining heterogeneity and combining results from several studies in meta-analysis. Egger MDavey Smith GAltman DG: Systematic Reviews in Health Care: Meta-Analysis in Context ed 2LondonBMJ Publication Group2001. 228247

26

Deeks JJHiggins JPTAltman DGAnalysing and presenting results. Higgins JPTGreen S: Cochrane Handbook for Systematic Reviews of Interventions 4.2.6 Hoboken, NJWiley InterScience2006. Section 8 (http://209.211.250.105/resources/handbook/Handbook4.2.6Sep2006.pdf) [Accessed 14 July 2009]

27

DerSimonian RLaird N: Meta-analysis in clinical trials. Control Clin Trials 7:1771881986

28

Devaux BCO'Fallon JRKelly PJ: Resection, biopsy, and survival in malignant glial neoplasms. A retrospective study of clinical parameters, therapy, and outcome. J Neurosurg 78:7677751993

29

Duval STweedie R: Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in metaanalysis. Biometrics 56:4554632000

30

Duval SJTweedie RL: A nonparametric “trim and fill” method of accounting for publication bias in meta-analysis. J Am Stat Assoc 95:89982000

31

Egger MSmith GDSchneider MMinder C: Bias in metaanalysis detected by a simple, graphical test. BMJ 315:6296341997

32

Esteller MGarcia-Foncillas JAndion EGoodman SNHidalgo OFVanaclocha V: Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N Engl J Med 343:135013542000

33

Forsting MAlbert FKKunze SAdams HPZenner DSartor K: Extirpation of glioblastomas: MR and CT follow-up of residual tumor and regrowth patterns. AJNR Am J Neuroradiol 14:77871993

34

Frankel SAGerman WJ: Glioblastoma multiforme. Review of 219 cases with regard to natural history, pathology, diagnostic methods and treatment. J Neurosurg 15:4895031958

35

Garfield JSurgery of cerebral gliomas. Thomas DGTGraham DI: LondonButterworths1980. 301321

36

Gehan EAWalker MD: Prognostic factors for patients with brain tumors. Natl Cancer Inst Monogr 46:1891951977

37

Gilbert MRLoghin M: The treatment of malignant gliomas. Curr Treat Options Neurol 7:2933032005

38

Glioma Meta-Analysis Trialists (GMT) Group: Chemotherapy for high-grade glioma. Cochrane Database Syst Rev 4:CD0039132002

39

Graus FTortosa A: Neuro-oncology: setting new standards of management. Lancet Neurol 5:892006

40

Green SBByar DPWalker MDPistenmaa DAAlexander E JrBatzdorf U: Comparisons of carmustine, procarbazine, and high-dose methylprednisolone as additions to surgery and radiotherapy for the treatment of malignant glioma. Cancer Treat Rep 67:1211321983

41

Greenberg MS: Tumor. Handbook of Neurosurgery ed 5New YorkThieme Medical Publishers2001. 386505

42

Harbaugh KSBlack PM: Strategies in the surgical management of malignant gliomas. Semin Surg Oncol 14:26331998

43

Hauch HSajedi MWolff JE: Treatment arms summarizing analysis of 220 high-grade glioma studies. Anticancer Res 25:358535902005

44

Hegi MEDiserens ACGodard SDietrich PYRegli LOstermann S: Clinical trial substantiates the predictive value of O-6-methylguanine-DNA methyltransferase promoter methylation in glioblastoma patients treated with temozolomide. Clin Cancer Res 10:187118742004

45

Higgins JPTThompson SG: Quantifying heterogeneity in a meta-analysis. Stat Med 21:153915582002

46

Hitchcock ESato F: Treatment of malignant gliomata. J Neurosurg 21:4975051964

47

Hoshino T: A commentary on the biology and growth kinetics of low-grade and high-grade gliomas. J Neurosurg 61:8959001984

48

Ino YBetensky RAZlatescu MCSasaki HMacdonald DRStemmer-Rachamimov AO: Molecular subtypes of anaplastic oligodendroglioma: implications for patient management at diagnosis. Clin Cancer Res 7:8398452001

49

Ino YZlatescu MCSasaki HMacdonald DRStemmer-Rachamimov AOJhung S: Long survival and therapeutic responses in patients with histologically disparate high-grade gliomas demonstrating chromosome 1p loss. J Neurosurg 92:9839902000

50

Jaeckle KAEyre HJTownsend JJSchulman SKnudson HMBelanich M: Correlation of tumor O6 methylguanine-DNA methyltransferase levels with survival of malignant astrocytoma patients treated with bis-chloroethylnitrosourea: a Southwest Oncology Group study. J Clin Oncol 16:331033151998

51

Jelsma RBucy PC: The treatment of glioblastoma multiforme of the brain. J Neurosurg 27:3884001967

52

Jeremic BGrujicic DAntunovic VDjuric LStojanovic MShibamoto Y: Influence of extent of surgery and tumor location on treatment outcome of patients with glioblastoma multiforme treated with combined modality approach. J Neurooncol 21:1771851994

53

Kala MSramek VHoudek MVaverka MZmrzlik P: Treatment of glioblastoma multiforme. Cas Lek Cesk 132:6536561993

54

Karnofsky DABurchenal JHArmistead GC JrSoutham CMBernstein JLCraver LF: Triethylene melamine in the treatment of neoplastic disease. AMA Arch Intern Med 87:4775161951

55

Kelly PJHunt C: The limited value of cytoreductive surgery in elderly patients with malignant gliomas. Neurosurgery 34:62671994

56

Kim TSHalliday ALHedley-Whyte ETConvery K: Correlates of survival and the Daumas-Duport grading system for astrocytomas. J Neurosurg 74:27371991

57

Kiwit JCFloeth FWBock WJ: Survival in malignant glioma: analysis of prognostic factors with special regard to cytoreductive surgery. Zentralbl Neurochir 57:76881996

58

Kleihues PBurger PCScheithauer BW: Histological Typing of Tumors of the Central Nervous System ed 2BerlinSpringer1993

59

Kleihues PBurger PCScheithauer BW: The new WHO classification of brain tumours. Brain Pathol 3:2552681993

60

Kleihues PCavanee WK: Pathology and Genetics of Tumours of the Nervous System LyonIARC Press2000

61

Knüsel L: On the accuracy of statistical distributions in Microsoft Excel 2003. Computational Statistics and Data Analysis 48:4454492005

62

Kostron HRossler K: Surgical intervention in patients with malignant glioma. Wien Med Wochenschr 156:3383412006

63

Kreth FWBerlis ASpiropoulou VFaist MScheremet RRossner R: The role of tumor resection in the treatment of glioblastoma multiforme in adults. Cancer 86:211721231999

64

Kreth FWWarnke PCOstertag CB: The limited value of cytoreductive surgery in elderly patients with malignant gliomas. Neurosurgery 35:3443451994. (Letter)

65

Kreth FWWarnke PCOstertag CB: Progress in malignant glioma. J Neurosurg 100:113211332004. (Letter)

66

Kreth FWWarnke PCScheremet ROstertag CB: Surgical resection and radiation therapy versus biopsy and radiation therapy in the treatment of glioblastoma multiforme. J Neurosurg 78:7627661993

67

Laigle-Donadey FSanson M: [Pattern of care of high-grade gliomas.]. Rev Prat 56:177917862006. (Fr)

68

Lamborn KRChang SMPrados MD: Prognostic factors for survival of patients with glioblastoma: recursive partitioning analysis. Neuro Oncol 6:2272352004

69

Laws ERParney IFHuang WAnderson FMorris AMAsher A: Survival following surgery and prognostic factors for recently diagnosed malignant glioma: data from the Glioma Outcomes Project. J Neurosurg 99:4674732003

70

Marshall LFJennett BLangfitt TW: Needle biopsy for the diagnosis of malignant glioma. JAMA 228:141714181974

71

Martinez RJanka MSoldner FBehr R: Gross-total resection of malignant gliomas in elderly patients: implications in survival. Zentralbl Neurochir 68:1761812007

72

Mason WPMaestro RDEisenstat DForsyth PFulton DLaperriere N: Canadian recommendations for the treatment of glioblastoma multiforme. Curr Oncol 14:1101172007

73

Metcalfe SEGrant R: Biopsy versus resection for malignant glioma. Cochrane Database Syst Rev 3:CD0020342001

74

Mitchell PEllison DWMendelow AD: Surgery for malignant gliomas: mechanistic reasoning and slippery statistics. Lancet Neurol 4:4134222005

75

Nazzaro JMNeuwelt EA: The role of surgery in the management of supratentorial intermediate and high-grade astrocytomas in adults. J Neurosurg 73:3313441990

76

Nitta TSato K: Prognostic implications of the extent of surgical resection in patients with intracranial malignant gliomas. Cancer 75:272727311995

77

Parmar MKBTorri VStewart L: Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med 17:281528341998

78

Patwardhan RVShorter CWillis BKReddy PSmith DCaldito GC: Survival trends in elderly patients with glioblastoma multiforme: resective surgery, radiation, and chemotherapy. Surg Neurol 62:2072132004

79

Rostomily RCKeles GEBerger MS: Radical surgery in the management of low-grade and high-grade gliomas. Baillieres Clin Neurol 5:3453691996

80

Salcman M: The morbidity and mortality of brain tumors. A perspective on recent advances in therapy. Neurol Clin 3:2292571985

81

Salcman M: Resection and reoperation in neuro-oncology. Rationale and approach. Neurol Clin 3:8318421985

82

Salcman MSupratentorial gliomas: clinical features and surgical therapy. Wilkins RHRengachary SS: Neurosurgery New YorkMcGraw-Hill1985. Vol 1:579590

83

Salcman M: Surgical decision-making for malignant brain tumors. Clin Neurosurg 35:2853131989

84

Salcman MKaplan RSDucker TBAbdo HMontgomery E: Effect of age and reoperation on survival in the combined modality treatment of malignant astrocytoma. Neurosurgery 10:4544631982

85

Sandeman DRSandeman APBuxton PHughes HHChadwick DWWilliams IR: The management of patients with an intrinsic supratentorial brain tumour. Br J Neurosurg 4:2993121990

86

Sanders CEgger MDonovan JTallon DFrankel S: Reporting on quality of life in randomised controlled trials: bibliographic study. BMJ 317:119111941998

87

Sawaya RHammoud MSchoppa DHess KRWu SZShi WM: Neurosurgical outcomes in a modern series of 400 craniotomies for treatment of parenchymal tumors. Neurosurgery 42:104410561998

88

Shapiro WR: Treatment of neuroectodermal brain tumors. Ann Neurol 12:2312371982

89

Shapiro WRGreen SBBurger PCMahaley MS JrSelker RGVanGilder JC: Randomized trial of three chemotherapy regimens and two radiotherapy regimens and two radiotherapy regimens in postoperative treatment of malignant glioma. Brain Tumor Cooperative Group Trial 8001. J Neurosurg 71:191989

90

Shaw EG: Nothing ventured, nothing gained: treatment of glioblastoma multiforme in the elderly. J Clin Oncol 22:154015412004. (Comment)

91

Simpson JRHorton JScott CCurran WJRubin PFischbach J: 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 26:2392441993

92

Stupp RReni MGatta GMazza EVecht C: Anaplastic astrocytoma in adults. Crit Rev Oncol Hematol 63:72802007

93

Swanson KRRostomily RCAlvord EC Jr: A mathematical modelling tool for predicting survival of individual patients following resection of glioblastoma: a proof of principle. Br J Cancer 98:1131192008

94

Takeuchi KHoshino K: Statistical analysis of factors affecting survival after glioblastoma multiforme. Acta Neurochir (Wien) 37:57731977

95

Taylor MChambers APerry JBernstein M: Evidence-based review of the role of surgery for malignant glioma. Curr Oncol 11:53622004

96

Taylor SJTweedie RL: Practical estimates of the effect of publication bias in metaanalysis. Australian Epidemiologist 5:14171998

97

Turazzi SLicata C: Role of surgery in gliomas of cerebral hemispheres in adults. Forum (Genova) 10:84922000

98

Vecht CJAvezaat CJvan Putten WLEijkenboom WMStefanko 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 53:4664711990

99

Vives KPPiepmeier JM: Complications and expected outcome of glioma surgery. J Neurooncol 42:2893021999

100

Vuorinen VHinkka SFarkkila MJaaskelainen J: Debulking or biopsy of malignant glioma in elderly people—a randomised study. Acta Neurochir (Wien) 145:5102003

101

Walker MDAlexander E JrHunt WELeventhal CMMahaley MS JrMealey J: Evaluation of mithramycin in the treatment of anaplastic gliomas. J Neurosurg 44:6556671976

102

Walker MDAlexander E JrHunt WEMacCarty CSMahaley MS JrMealey J Jr: Evaluation of BCNU and/or radiotherapy in the treatment of anaplastic gliomas. A cooperative clinical trial. J Neurosurg 49:3333431978

103

Walker MDGreen SBByar DPAlexander E JrBatzdorf UBrooks WH: Randomized comparisons of radiotherapy and nitrosoureas for the treatment of malignant glioma after surgery. N Engl J Med 303:132313291980

104

Walker MDStrike TASheline GE: An analysis of dose effect relationship in the radiotherapy of malignant gliomas. Int J Radiat Oncol Biol Phys 5:172517311979

105

Warnke PC: Stereotactic volumetric resection of gliomas. Acta Neurochir Suppl 88:582003

106

Warnke PCKreth FWScheremet ROstertag CB: Response to Drs. Simpson, 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 clinical trials. Int J Radiat Oncol Biol Phys 29:2201994. (Letter)

107

Weir B: The relative significance of factors affecting postoperative survival in astrocytomas, grades 3 and 4. J Neurosurg 38:4484521973

108

Whitehead A: Estimating treatment difference in an individual trial. Meta-analysis of Controlled Clinical Trials Chichester, UKJohn Wiley & Sons, Ltd2002. 2356

109

Yuile PDent OCook RBiggs MLittle N: Survival of glioblastoma patients related to presenting symptoms, brain site and treatment variables. J Clin Neurosci 13:7477512006

110

Zulch KJ: Histological Typing of Tumors of the Central Nervous System. GenevaWorld Health Organization1979

TrendMD

Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 6 6 6
Full Text Views 108 108 27
PDF Downloads 91 91 33
EPUB Downloads 0 0 0

PubMed

Google Scholar