Abstract
Introduction
Tumor recurrence patterns after resection of intracranial low-grade gliomas (LGG) generally remain obscured. The objective of the present retrospective study was their multifaceted analysis, evaluation of associated factors, and assessment of impact on prognosis.
Methods
Study group comprised 81 consecutive adult patients (46 men and 35 women; median age, 37 years) with recurrent diffuse astrocytomas (DA; 51 cases) and oligodendrogliomas (OD; 30 cases). The median length of follow-up after primary surgery was 6.7 years.
Results
Early (within 2 years after primary surgery) and non-early (> 2 years after primary surgery) recurrence was noted in 23 (28%) and 58 (72%) cases, respectively. Fast (≤ 6 months) and slow ( > 6 months) radiological progression of relapse was noted in 31 (38%) and 48 (59%) cases, respectively. Tumor recurrence was local and non-local in 71 (88%) and 10 (12%) cases, respectively. Recurrence patterns have differed in OD, IDH1-mutant DA, and IDH wild-type DA. Early onset, fast radiological progression, and non-local site of relapse had statistically significant negative impact on overall survival of patients and were often associated with malignant transformation of the tumor (38 cases). However, in subgroup with extent of resection ≥ 90% (56 cases) no differences in recurrence characteristics were found between 3 molecularly defined groups of LGG.
Conclusions
Recurrence patterns after resection of LGG show significant variability, differ in distinct molecularly defined types of tumors, and demonstrate definitive impact on prognosis. Aggressive resection at the time of primary surgery may result in more favorable characteristics of recurrence at the time of its development.
Similar content being viewed by others
References
Hochberg FH, Pruitt A (1980) Assumptions in the radiotherapy of glioblastoma. Neurology 30:907–911
Choucair AK, Levin VA, Gutin PH, Davis RL, Silver P, Edwards MS, Wilson CB (1986) Development of multiple lesions during radiation therapy and chemotherapy in patients with gliomas. J Neurosurg 65:654–658
Wallner KE, Galicich JH, Krol G, Arbit E, Malkin MG (1989) Patterns of failure following treatment for glioblastoma multiforme and anaplastic astrocytoma. Int J Radiat Oncol Biol Phys 16:1405–1409
Liang BC, Thornton AF Jr, Sandler HM, Greenberg HS (1991) Malignant astrocytomas: focal tumor recurrence after focal external beam radiation therapy. J Neurosurg 75:559–563
Konishi Y, Muragaki Y, Iseki H, Mitsuhashi N, Okada Y (2012) Patterns of intracranial glioblastoma recurrence after aggressive surgical resection and adjuvant management: retrospective analysis of 43 cases. Neurol Med Chir (Tokyo) 52:577–586
Ferguson SD, Momin EN, Weinberg JS (2018) Surgical management of recurrent intracranial gliomas. Prog Neurol Surg 30:218–231
van den Bent MJ, Afra D, de Witte O, Ben Hassel M, Schraub S, Hoang-Xuan K, Malmström PO, Collette L, Piérart M, Mirimanoff R, Karim AB (2005) Long-term efficacy of early versus delayed radiotherapy for low-grade astrocytoma and oligodendroglioma in adults: the EORTC 22845 randomised trial. Lancet 366:985–990
Lebrun C, Fontaine D, Bourg V, Ramaioli A, Chanalet S, Vandenbos F, Lonjon M, Fauchon F, Paquis P, Frenay M (2007) Treatment of newly diagnosed symptomatic pure low-grade oligodendrogliomas with PCV chemotherapy. Eur J Neurol 14:391–398
Smith JS, Chang EF, Lamborn KR, Chang SM, Prados MD, Cha S, Tihan T, Vandenberg S, McDermott MW, Berger MS (2008) Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 26:1338–1345
Ahmadi R, Dictus C, Hartmann C, Zürn O, Edler L, Hartmann M, Combs S, Herold-Mende C, Wirtz CR, Unterberg A (2009) Long-term outcome and survival of surgically treated supratentorial low-grade glioma in adult patients. Acta Neurochir (Wien) 151:1359–1365
Martino J, Taillandier L, Moritz-Gasser S, Gatignol P, Duffau H (2009) Re-operation is a safe and effective therapeutic strategy in recurrent WHO grade II gliomas within eloquent areas. Acta Neurochir (Wien) 151:427–436
Chaichana KL, McGirt MJ, Laterra J, Olivi A, Quiñones-Hinojosa A (2010) Recurrence and malignant degeneration after resection of adult hemispheric low-grade gliomas. J Neurosurg 112:10–17
Daniels TB, Brown PD, Felten SJ, Wu W, Buckner JC, Arusell RM, Curran WJ, Abrams RA, Schiff D, Shaw EG (2011) Validation of EORTC prognostic factors for adults with low-grade glioma: a report using intergroup 86-72-51. Int J Radiat Oncol Biol Phys 81:218–224
Okita Y, Narita Y, Miyakita Y, Ohno M, Matsushita Y, Fukushima S, Sumi M, Ichimura K, Kayama T, Shibui S (2012) IDH1/2 mutation is a prognostic marker for survival and predicts response to chemotherapy for grade II gliomas concomitantly treated with radiation therapy. Int J Oncol 41:1325–1336
Komori T, Muragaki Y, Chernov MF (2018) Pathology and genetics of gliomas. Prog Neurol Surg 31:1–37
Shaw EG, Berkey B, Coons SW, Bullard D, Brachman D, Buckner JC, Stelzer KJ, Barger GR, Brown PD, Gilbert MR, Mehta M (2008) Recurrence following neurosurgeon-determined gross-total resection of adult supratentorial low-grade glioma: results of a prospective clinical trial. J Neurosurg 109:835–841
Muragaki Y, Iseki H, Maruyama T, Kawamata T, Yamane F, Nakamura R, Kubo O, Takakura K, Hori T (2006) Usefulness of intraoperative magnetic resonance imaging for glioma surgery. Acta Neurochir Suppl 98:67–75
Muragaki Y, Iseki H, Maruyama T, Tanaka M, Shinohara C, Suzuki T, Yoshimitsu K, Ikuta S, Hayashi M, Chernov M, Hori T, Okada Y, Takakura K (2011) Information-guided surgical management of gliomas using low-field-strength intraoperative MRI. Acta Neurochir Suppl 109:67–72
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 114:97–109
Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW (2016) The 2016 world health organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 131:803–820
Nitta M, Muragaki Y, Maruyama T, Ikuta S, Komori T, Maebayashi K, Iseki H, Tamura M, Saito T, Okamoto S, Chernov M, Hayashi M, Okada Y (2015) Proposed therapeutic strategy for adult low-grade glioma based on aggressive tumor resection. Neurosurg Focus 38(1):E7
van den Bent MJ, Wefel JS, Schiff D, Taphoorn MJ, Jaeckle K, Junck L, Armstrong T, Choucair A, Waldman AD, Gorlia T, Chamberlain M, Baumert BG, Vogelbaum MA, Macdonald DR, Reardon DA, Wen PY, Chang SM, Jacobs AH (2011) Response assessment in neuro-oncology (a report of the RANO group): assessment of outcome in trials of diffuse low-grade gliomas. Lancet Oncol 12:583–593
Olson JD, Riedel E, DeAngelis LM (2000) Long-term outcome of low-grade oligodendroglioma and mixed glioma. Neurology 54:1442–1448
Schomas DA, Laack NN, Brown PD (2009) Low-grade gliomas in older patients: long-term follow-up from Mayo Clinic. Cancer 115:3969–3978
Iwadate Y, Matsutani T, Hasegawa Y, Shinozaki N, Higuchi Y, Saeki N (2011) Favorable long-term outcome of low-grade oligodendrogliomas irrespective of 1p/19q status when treated without radiotherapy. J Neurooncol 102:443–449
Jakola AS, Myrmel KS, Kloster R, Torp SH, Lindal S, Unsgård G, Solheim O (2012) Comparison of a strategy favoring early surgical resection vs a strategy favoring watchful waiting in low-grade gliomas. JAMA 308:1881–1888
Pignatti F, van den Bent M, Curran D, Debruyne C, Sylvester R, Therasse P, Afra D, Cornu P, Bolla M, Vecht C, Karim AB (2002) Prognostic factors for survival in adult patients with cerebral low-grade glioma. J Clin Oncol 20:2076–2084
Chang EF, Smith JS, Chang SM, Lamborn KR, Prados MD, Butowski N, Barbaro NM, Parsa AT, Berger MS, McDermott MM (2008) Preoperative prognostic classification system for hemispheric low-grade gliomas in adults. J Neurosurg 109:817–824
Eckel-Passow JE, Lachance DH, Molinaro AM, Walsh KM, Decker PA, Sicotte H, Pekmezci M, Rice T, Kosel ML, Smirnov IV, Sarkar G, Caron AA, Kollmeyer TM, Praska CE, Chada AR, Halder C, Hansen HM, McCoy LS, Bracci PM, Marshall R, Zheng S, Reis GF, Pico AR, O'Neill BP, Buckner JC, Giannini C, Huse JT, Perry A, Tihan T, Berger MS, Chang SM, Prados MD, Wiemels J, Wiencke JK, Wrensch MR, Jenkins RB (2015) Glioma groups based on 1p/19q, IDH, and TERT promoter mutations in tumors. N Engl J Med 372:2499–2508
Gozé C, Bezzina C, Gozé E, Rigau V, Maudelonde T, Bauchet L, Duffau H (2012) 1p/19q loss but not IDH1 mutations influences WHO grade II gliomas spontaneous growth. J Neurooncol 108:69–75
Brat DJ, Aldape K, Colman H, Holland EC, Louis DN, Jenkins RB, Kleinschmidt-DeMasters BK, Perry A, Reifenberger G, Stupp R, von Deimling A, Weller M (2018) cIMPACT-NOW update 3: recommended diagnostic criteria for “Diffuse astrocytic glioma, IDH-wildtype, with molecular features of glioblastoma, WHO grade IV”. Acta Neuropathol 136:805–810
Ius T, Isola M, Budai R, Pauletto G, Tomasino B, Fadiga L, Skrap M (2012) Low-grade glioma surgery in eloquent areas volumetric analysis of extent of resection and its impact on overall survival: a single-institution experience in 190 patients. J Neurosurg 117:1039–1052
Buckner JC, Shaw EG, Pugh SL, Chakravarti A, Gilbert MR, Barger GR, Coons S, Ricci P, Bullard D, Brown PD, Stelzer K, Brachman D, Suh JH, Schultz CJ, Bahary JP, Fisher BJ, Kim H, Murtha AD, Bell EH, Won M, Mehta MP, Curran WJ Jr (2016) Radiation plus procarbazine, CCNU, and vincristine in low-grade glioma. N Engl J Med 374:1344–1355
Narita Y (2018) Chemotherapy of diffuse astrocytoma (WHO grade II) in adults. Prog Neurol Surg 31:145–215
Funding
None. The authors do not have any personal or institutional financial interests in drugs, materials, or devices described in this paper.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
This study contains no conflict of interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Fukuya, Y., Ikuta, S., Maruyama, T. et al. Tumor recurrence patterns after surgical resection of intracranial low-grade gliomas. J Neurooncol 144, 519–528 (2019). https://doi.org/10.1007/s11060-019-03250-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11060-019-03250-8