Surgical resection versus watchful waiting in low-grade gliomas

A S Jakola, A J Skjulsvik, K S Myrmel, K Sjåvik, G Unsgård, S H Torp, K Aaberg, T Berg, H Y Dai, K Johnsen, R Kloster, O Solheim, A S Jakola, A J Skjulsvik, K S Myrmel, K Sjåvik, G Unsgård, S H Torp, K Aaberg, T Berg, H Y Dai, K Johnsen, R Kloster, O Solheim

Abstract

Background: Infiltrating low-grade gliomas (LGG; WHO grade 2) typically present with seizures in young adults. LGGs grow continuously and usually transform to higher grade of malignancy, eventually causing progressive disability and premature death. The effect of up-front surgery has been controversial and the impact of molecular biology on the effect of surgery is unknown. We now present long-term results of upfront surgical resection compared with watchful waiting in light of recently established molecular markers.

Materials and methods: Population-based parallel cohorts were followed from two Norwegian university hospitals with different surgical treatment strategies and defined geographical catchment regions. In region A watchful waiting was favored while early resection was favored in region B. Thus, the treatment strategy in individual patients depended on their residential address. The inclusion criteria were histopathological diagnosis of supratentorial LGG from 1998 through 2009 in patients 18 years or older. Follow-up ended 1 January 2016. Making regional comparisons, the primary end-point was overall survival.

Results: A total of 153 patients (66 from region A, 87 from region B) were included. Early resection was carried out in 19 (29%) patients in region A compared with 75 (86%) patients in region B. Overall survival was 5.8 years (95% CI 4.5-7.2) in region A compared with 14.4 years (95% CI 10.4-18.5) in region B (P < 0.01). The effect of surgical strategy remained after adjustment for molecular markers (P = 0.001).

Conclusion: In parallel population-based cohorts of LGGs, early surgical resection resulted in a clinical relevant survival benefit. The effect on survival persisted after adjustment for molecular markers.

Keywords: astrocytoma; brain neoplasm; low-grade glioma; population based; survival; treatment outcome.

© The Author 2017. Published by Oxford University Press on behalf of the European Society for Medical Oncology.

Figures

Figure 1.
Figure 1.
Flow chart of patient inclusion.
Figure 2.
Figure 2.
Survival analysis comparing cohorts, where region A preferred biopsy while region B preferred early resection. In region A the median survival was 5.8 years (95% CI 4.5–7.2) compared with 14.4 years (95% CI 10.4–18.5) in region B.
Figure 3.
Figure 3.
Survival in cohorts (A–C) with adjustment for molecular risk-group (log-rank test, P = 0.001). Results are presented stratified according to risk groups (A) low-risk (B) medium-risk and (C) high-risk group. (A) IDH mutated, 1p19 codeleted LGGs (n =43). Median survival was not reached. (B) IDH mutated, non-codeleted LGGs (n =61). Median survival in region A was 5.6 years (95% CI 3.5–7.6) compared with 10.2 year (95% CI 6.9–13.4) in region B. (C) IDH wild-type LGGs (n=41). Median survival in region A was 1.4 year (95% CI 0.6–2.2) compared with 5.3 year (95% CI 0.0–20.0) in region B.

References

    1. Sanai N, Chang S, Berger MS.. Low-grade gliomas in adults. J Neurosurg 2011; 1: 18.
    1. Veeravagu A, Jiang B, Chang SD. et al. Biopsy versus resection for the management of low-grade gliomas. Cochrane Database Syst Rev 2013; 4: Cd009319.
    1. Capelle L, Fontaine D, Mandonnet E. et al. Spontaneous and therapeutic prognostic factors in adult hemispheric World Health Organization Grade II gliomas: a series of 1097 cases. J Neurosurg 2013; 118: 1–12.
    1. 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.
    1. Jakola AS, Myrmel KS, Kloster R. et al. Comparison of a strategy favoring early surgical resection vs a strategy favoring watchful waiting in low-grade gliomas. JAMA 2012; 308: 1881–1888.
    1. Jakola AS, Unsgard G, Myrmel KS. et al. Surgical strategy in grade II astrocytoma: a population-based analysis of survival and morbidity with a strategy of early resection as compared to watchful waiting. Acta Neurochir (Wien) 2013; 155: 2227–2235.
    1. Jakola AS, Unsgard G, Myrmel KS. et al. Surgical strategies in low-grade gliomas and implications for long-term quality of life. J Clin Neurosci 2014; 21: 1304–1309.
    1. Markert JM. The role of early resection vs biopsy in the management of low-grade gliomas. JAMA 2012; 308: 1918–1919.
    1. Buckner JC, Shaw EG, Pugh SL. et al. Radiation plus procarbazine, CCNU, and vincristine in low-grade glioma. N Engl J Med 2016; 374: 1344–1355.
    1. Myrseth E, Moller P, Pedersen PH, Lund-Johansen M.. Vestibular schwannoma: surgery or gamma knife radiosurgery? A prospective, nonrandomized study. Neurosurgery 2009; 64: 654–661; discussion 661–653.
    1. Jackson RJ, Fuller GN, Abi-Said D. et al. Limitations of stereotactic biopsy in the initial management of gliomas. Neuro-Oncology 2001; 3: 193–200.
    1. Pignatti F, van den Bent M, Curran D. et al. Prognostic factors for survival in adult patients with cerebral low-grade glioma. J Clin Oncol 2002; 20: 2076–2084.
    1. Louis DN, Perry A, Reifenberger G. et al. The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 2016; 131: 803–820.
    1. Suzuki H, Aoki K, Chiba K. et al. Mutational landscape and clonal architecture in grade II and III gliomas. Nat Genet 2015; 47: 458–468.
    1. Aldape K, Simmons ML, Davis RL. et al. Discrepancies in diagnoses of neuroepithelial neoplasms. Cancer 2000; 88: 2342–2349.
    1. Brat DJ, Verhaak RG, Aldape KD. et al. Comprehensive, Integrative Genomic Analysis of Diffuse Lower-Grade Gliomas. N Engl J Med 2015; 372: 2481–2498.
    1. Eckel-Passow JE, Lachance DH, Molinaro AM. et al. Glioma Groups Based on 1p/19q, IDH, and TERT Promoter Mutations in Tumors. N Engl J Med 2015; 372: 2499–2508.
    1. Louis D, Ohgaki H, Wiestler O. et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007; 114: 97–109.
    1. Reuss DE, Sahm F, Schrimpf D. et al. ATRX and IDH1-R132H immunohistochemistry with subsequent copy number analysis and IDH sequencing as a basis for an "integrated" diagnostic approach for adult astrocytoma, oligodendroglioma and glioblastoma. Acta Neuropathol 2015; 129: 133–146.
    1. von Elm E, Altman DG, Egger M. et al. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet 2007; 370: 1453–1457.
    1. 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.
    1. Roelz R, Strohmaier D, Jabbarli R. et al. Residual tumor volume as best outcome predictor in low grade glioma – a nine-years near-randomized survey of surgery vs. biopsy. Sci Rep 2016; 6: 32286..
    1. Pallud J, Mandonnet E, Duffau H. et al. Prognostic value of initial magnetic resonance imaging growth rates for World Health Organization grade II gliomas. Ann Neurol 2006; 60: 380–383.
    1. Rees J, Watt H, Jager HR. et al. Volumes and growth rates of untreated adult low-grade gliomas indicate risk of early malignant transformation. Eur J Radiol 2009; 72: 54–64.
    1. Cochereau J, Herbet G, Rigau V, Duffau H.. Acute progression of untreated incidental WHO Grade II glioma to glioblastoma in an asymptomatic patient. J Neurosurg 2016; 124: 141–145.
    1. Cordier D, Goze C, Schadelin S. et al. A better surgical resectability of WHO grade II gliomas is independent of favorable molecular markers. J Neurooncol 2015; 121: 185–193.
    1. Wang HY, Tang K, Liang TY. et al. The comparison of clinical and biological characteristics between IDH1 and IDH2 mutations in gliomas. J Exp Clin Cancer Res 2016; 35: 86..
    1. Johannesen TB, Langmark F, Lote K.. Cause of death and long-term survival in patients with neuro-epithelial brain tumours: a population-based study. Eur J Cancer 2003; 39: 2355–2363.
    1. Claus EB, Black PM.. Survival rates and patterns of care for patients diagnosed with supratentorial low-grade gliomas. Cancer 2006; 106: 1358–1363.
    1. Brasil Caseiras G, Ciccarelli O, Altmann DR. et al. Low-grade gliomas: six-month tumor growth predicts patient outcome better than admission tumor volume, relative cerebral blood volume, and apparent diffusion coefficient. Radiology 2009; 253: 505–512.

Source: PubMed

Sponsors en medewerkers

Medische omstandigheden

Geneesmiddelinterventies

3
Abonneren