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IDH wild-type WHO grade II diffuse low-grade gliomas. A heterogeneous family with different outcomes. Systematic review and meta-analysis

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Abstract

WHO grade II diffuse low-grade gliomas (DLGGs) were recently divided into sub-groups on the basis of their molecular profiles. IDH wild-type (IDH-wt) tumors seem to be associated with unfavorable prognoses due to biological similarities to glioblastomas. The authors performed a systematic review and meta-analysis of literature examining epidemiology, clinical characteristics, management, and the outcome of IDH-wt grade II DLGGs. According to PRISMA guidelines, a comprehensive review of studies published from January 2009 to October 2017 was carried out. The authors identified series that examined the prevalence rate, clinical and radiological characteristics, treatment, and outcome of IDH-wt DLGGs. Variables influencing outcomes were analyzed using a random-effects meta-analysis model. Finally, a meta-regression analysis was performed to examine the impact of therapeutic strategies on the effect-size. Twenty-two studies were included in this systematic review. The IDH-wt prevalence rate was 22.9% (95% CI 18.4–27.4%). The hazard ratio for this molecular subgroup in the DLGGs population was 3.46 (95% CI 2.24–5.36; p < 0.001), and the heterogeneity was significant (I2 = 85%, τ2 = 0.88) (HR range 1.28–376). Nonetheless, publication bias did not affect the analysis (p = 0.176). The meta-regression revealed that the extent of resection and post-operative chemotherapy affected the outcome in the IDH-wt subgroup (p < 0.001 and 0.015, respectively), with no significant association of the HR with the rate of RT or RT + CHT. The prevalence of IDH-wt tumors is approximately 23% of DLGGs. The absence of IDH mutation is associated with a heterogeneous outcome, and its therapeutic relevance for postoperative management remains unclear. Maximal surgical resection improves the overall survival in the DLGGs population, beyond molecular status. Further molecular stratification is needed to better understand IDH-wt behavior and therapeutic response.

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References

  1. Ahmadi R, Stockhammer F, Becker N, Hohlen K, Misch M, Christians A, Dictus C, Herold-Mende C, Capper D, Unterberg A, von Deimling A, Wick W, Hartmann C (2012) No prognostic value of IDH1 mutations in a series of 100 WHO grade II astrocytomas. J Neuro-Oncol 109:15–22. https://doi.org/10.1007/s11060-012-0863-y

    Article  CAS  Google Scholar 

  2. Aibaidula A, Chan AK-Y, Shi Z, Li Y, Zhang R, Yang R, Li KK-W, Chung NY-F, Yao Y, Zhou L, Wu J, Chen H, Ng H-K (2017) Adult IDH wild-type lower-grade gliomas should be further stratified. Neuro-Oncology 19:1327–1337. https://doi.org/10.1093/neuonc/nox078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Baumert BG, Hegi ME, van den Bent MJ, von Deimling A, Gorlia T, Hoang-Xuan K, Brandes AA, Kantor G, Taphoorn MJB, Ben HM, Hartmann C, Ryan G, Capper D, Kros JM, Kurscheid S, Wick W, Enting R, Reni M, Thiessen B, Dhermain F, Bromberg JE, Feuvret L, Reijneveld JC, Chinot O, Gijtenbeek JMM, Rossiter JP, Dif N, Balana C, Bravo-Marques J, Clement PM, Marosi C, Tzuk-Shina T, Nordal RA, Rees J, Lacombe D, Mason WP, Stupp R (2016) Temozolomide chemotherapy versus radiotherapy in high-risk low-grade glioma (EORTC 22033-26033): a randomised, open-label, phase 3 intergroup study. Lancet Oncol 17:1521–1532. https://doi.org/10.1016/S1470-2045(16)30313-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bette S, Kaesmacher J, Huber T, Delbridge C, Ringel F, Boeckh-Behrens T, Meyer B, Zimmer C, Kirschke JS, Gempt J (2016) Value of early postoperative FLAIR volume dynamic in glioma with no or minimal enhancement. World Neurosurg 91:548–559.e1. https://doi.org/10.1016/j.wneu.2016.03.034

    Article  PubMed  Google Scholar 

  5. 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 J-P, Fisher BJ, Kim H, Murtha AD, Bell EH, Won M, Mehta MP, Curran WJ (2016) Radiation plus procarbazine, CCNU, and vincristine in low-grade glioma. N Engl J Med 374:1344–1355. https://doi.org/10.1056/NEJMoa1500925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Cairncross G, Wang M, Shaw E, Jenkins R, Brachman D, Buckner J, Fink K, Souhami L, Laperriere N, Curran W, Mehta M (2013) Phase III trial of chemoradiotherapy for anaplastic oligodendroglioma: long-term results of RTOG 9402. J Clin Oncol 31:337–343. https://doi.org/10.1200/JCO.2012.43.2674

    Article  CAS  PubMed  Google Scholar 

  7. Cordier D, Gozé C, Schädelin S, Rigau V, Mariani L, Duffau H (2015) A better surgical resectability of WHO grade II gliomas is independent of favorable molecular markers. J Neuro-Oncol 121:185–193. https://doi.org/10.1007/s11060-014-1623-y

    Article  CAS  Google Scholar 

  8. Cordier D, Schadelin S, Duffau H (2015) Influence of 1p19q status and Ki67 index to predict extent of resection in WHO grade II gliomas: a virtual patient model. J Neuro-Oncol 123:317–318. https://doi.org/10.1007/s11060-015-1790-5

    Article  Google Scholar 

  9. Darlix A, Deverdun J, Menjot de Champfleur N, Castan F, Zouaoui S, Rigau V, Fabbro M, Yordanova Y, Le Bars E, Bauchet L, Gozé C, Duffau H (2017) IDH mutation and 1p19q codeletion distinguish two radiological patterns of diffuse low-grade gliomas. J Neuro-Oncol 133:37–45. https://doi.org/10.1007/s11060-017-2421-0

    Article  CAS  Google Scholar 

  10. de Groot J, Sontheimer H (2011) Glutamate and the biology of gliomas. Glia 59:1181–1189. https://doi.org/10.1002/glia.21113

    Article  PubMed  Google Scholar 

  11. De Witt Hamer PC, Robles SG, Zwinderman AH, Duffau H, Berger MS (2012) Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis. J Clin Oncol 30:2559–2565. https://doi.org/10.1200/JCO.2011.38.4818

    Article  PubMed  Google Scholar 

  12. Deeks J, Higgins J, Altman D (2011) Identifying and assessing heterogeneity. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0. The Cochrane Collaboration. John Wiley & Sons Ltd, Chichester 

  13. Douw L, Klein M, Fagel SS, van den Heuvel J, Taphoorn MJ, Aaronson NK, Postma TJ, Vandertop WP, Mooij JJ, Boerman RH, Beute GN, Sluimer JD, Slotman BJ, Reijneveld JC, Heimans JJ (2009) Cognitive and radiological effects of radiotherapy in patients with low-grade glioma: long-term follow-up. Lancet Neurol 8:810–818. https://doi.org/10.1016/S1474-4422(09)70204-2

    Article  PubMed  Google Scholar 

  14. Duffau H (2009) A personal consecutive series of surgically treated 51 cases of insular WHO grade II glioma: advances and limitations—clinical article. J Neurosurg 110:696–708. https://doi.org/10.3171/2008.8.JNS08741

    Article  PubMed  Google Scholar 

  15. Duffau H, Mandonnet E (2013) The “onco-functional balance” in surgery for diffuse low-grade glioma: integrating the extent of resection with quality of life. Acta Neurochir 155:951–957. https://doi.org/10.1007/s00701-013-1653-9

    Article  PubMed  Google Scholar 

  16. Duffau H, Lopes M, Arthuis F, Bitar A, Sichez J-P, Van Effenterre R, Capelle L (2005) Contribution of intraoperative electrical stimulations in surgery of low grade gliomas: a comparative study between two series without (1985–96) and with (1996–2003) functional mapping in the same institution. J Neurol Neurosurg Psychiatry 76:845–851. https://doi.org/10.1136/jnnp.2004.048520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Etxaniz O, Carrato C, de Aguirre I, Queralt C, Munoz A, Ramirez JL, Rosell R, Villa S, Diaz R, Estival A, Teixidor P, Indacochea A, Ahjal S, Vila L, Balana C (2017) IDH mutation status trumps the Pignatti risk score as a prognostic marker in low-grade gliomas. J Neuro-Oncol 135:1–12. https://doi.org/10.1007/s11060-017-2570-1

    Article  Google Scholar 

  18. Figarella-Branger D, Maues De Paula A, Colin C, Bouvier C (2011) Histomolecular classification of adult diffuse gliomas: the diagnostic value of immunohistochemical markers. Rev Neurol (Paris) 167:683–690. https://doi.org/10.1016/j.neurol.2011.07.006

    Article  CAS  Google Scholar 

  19. Fisher BJ, Hu C, Macdonald DR, Lesser GJ, Coons SW, Brachman DG, Ryu S, Werner-Wasik M, Bahary J-P, Liu J, Chakravarti A, Mehta M (2015) Phase 2 study of temozolomide-based chemoradiation therapy for high-risk low-grade gliomas: preliminary results of radiation therapy oncology group 0424. Int J Radiat Oncol Biol Phys 91:497–504. https://doi.org/10.1016/j.ijrobp.2014.11.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Goze C, Blonski M, Le Maistre G, Bauchet L, Dezamis E, Page P, Varlet P, Capelle L, Devaux B, Taillandier L, Duffau H, Pallud J (2014) Imaging growth and isocitrate dehydrogenase 1 mutation are independent predictors for diffuse low-grade gliomas. Neuro-Oncology 16:1100–1109. https://doi.org/10.1093/neuonc/nou085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Hathout L, Pope WB, Lai A, Nghiemphu PL, Cloughesy TF, Ellingson BM (2015) Radial expansion rates and tumor growth kinetics predict malignant transformation in contrast-enhancing low-grade diffuse astrocytoma. CNS Oncol 4:247–256. https://doi.org/10.2217/cns.15.16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Higgins JPT, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560. https://doi.org/10.1136/bmj.327.7414.557

    Article  PubMed  PubMed Central  Google Scholar 

  23. Houillier C, Wang X, Kaloshi G, Mokhtari K, Guillevin R, Laffaire J, Paris S, Boisselier B, Idbaih A, Laigle-Donadey F, Hoang-Xuan K, Sanson M, Delattre J-Y (2010) IDH1 or IDH2 mutations predict longer survival and response to temozolomide in low-grade gliomas. Neurology 75:1560–1566. https://doi.org/10.1212/WNL.0b013e3181f96282

    Article  CAS  PubMed  Google Scholar 

  24. 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: clinical article. J Neurosurg 117:1039–1052. https://doi.org/10.3171/2012.8.JNS12393

    Article  PubMed  Google Scholar 

  25. Iwadate Y, Matsutani T, Hirono S, Ikegami S, Shinozaki N, Saeki N (2015) IDH1 mutation is prognostic for diffuse astrocytoma but not low-grade oligodendrogliomas in patients not treated with early radiotherapy. J Neuro-Oncol 124:493–500. https://doi.org/10.1007/s11060-015-1863-5

    Article  CAS  Google Scholar 

  26. Kessler J, Guttler A, Wichmann H, Rot S, Kappler M, Bache M, Vordermark D (2015) IDH1(R132H) mutation causes a less aggressive phenotype and radiosensitizes human malignant glioma cells independent of the oxygenation status. Radiother Oncol 116:381–387. https://doi.org/10.1016/j.radonc.2015.08.007

    Article  CAS  PubMed  Google Scholar 

  27. Khasraw M, Lassman AB (2009) Neuro-oncology: late neurocognitive decline after radiotherapy for low-grade glioma. Nat Rev Neurol 5:646–647. https://doi.org/10.1038/nrneurol.2009.194

    Article  PubMed  Google Scholar 

  28. Leeper HE, Caron AA, Decker PA, Jenkins RB, Lachance DH, Giannini C (2015) IDH mutation, 1p19q codeletion and ATRX loss in WHO grade II gliomas. Oncotarget 6:30295–30305. https://doi.org/10.18632/oncotarget.4497

    Article  PubMed  PubMed Central  Google Scholar 

  29. Lewandowska MA, Furtak J, Szylberg T, Roszkowski K, Windorbska W, Rytlewska J, Jozwicki W (2014) An analysis of the prognostic value of IDH1 (isocitrate dehydrogenase 1) mutation in Polish glioma patients. Mol Diagn Ther 18:45–53. https://doi.org/10.1007/s40291-013-0050-7

    Article  CAS  PubMed  Google Scholar 

  30. Li M-Y, Wang Y-Y, Cai J-Q, Zhang C-B, Wang K-Y, Cheng W, Liu Y-W, Zhang W, Jiang T (2015) Isocitrate dehydrogenase 1 gene mutation is associated with prognosis in clinical low-grade gliomas. PLoS One 10:e0130872. https://doi.org/10.1371/journal.pone.0130872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Liubinas SV, D’Abaco GM, Moffat BM, Gonzales M, Feleppa F, Nowell CJ, Gorelik A, Drummond KJ, O’Brien TJ, Kaye AH, Morokoff AP (2014) Commentary on IDH1 mutation is associated with seizures and protoplasmic subtype in patients with low-grade gliomas. Epilepsia 55:1678–1679. https://doi.org/10.1111/epi.12744

    Article  CAS  Google Scholar 

  32. Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison (2016) The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 131:803–820. https://doi.org/10.1007/s00401-016-1545-1

    Article  PubMed  Google Scholar 

  33. Mandonnet E, Delattre J-Y, Tanguy M-L, Swanson KR, Carpentier AF, Duffau H, Cornu P, Van Effenterre R, Alvord ECJ, Capelle L (2003) Continuous growth of mean tumor diameter in a subset of grade II gliomas. Ann Neurol 53:524–528. https://doi.org/10.1002/ana.10528

    Article  PubMed  Google Scholar 

  34. Mandonnet E, Pallud J, Clatz O, Taillandier L, Konukoglu E, Duffau H, Capelle L (2008) Computational modeling of the WHO grade II glioma dynamics: principles and applications to management paradigm. Neurosurg Rev 31:263–268. https://doi.org/10.1007/s10143-008-0128-6

    Article  PubMed  Google Scholar 

  35. Metellus P, Coulibaly B, Colin C, De Paula AM, Vasiljevic A, Taieb D, Barlier A, Boisselier B, Mokhtari K, Wang XW, Loundou A, Chapon F, Pineau S, Ouafik L, Chinot O, Figarella-Branger D (2010) Absence of IDH mutation identifies a novel radiologic and molecular subtype of WHO grade II gliomas with dismal prognosis. Acta Neuropathol 120:719–729. https://doi.org/10.1007/s00401-010-0777-8

    Article  PubMed  Google Scholar 

  36. Moher D, Liberati A, Tetzlaff J, Altman DG, Grp P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement (reprinted from annals of internal medicine). Phys Ther 89:873–880. https://doi.org/10.1371/journal.pmed.1000097

    Article  PubMed  Google Scholar 

  37. Mukasa A, Takayanagi S, Saito K, Shibahara J, Tabei Y, Furuya K, Ide T, Narita Y, Nishikawa R, Ueki K, Saito N (2012) Significance of IDH mutations varies with tumor histology, grade, and genetics in Japanese glioma patients. Cancer Sci 103:587–592. https://doi.org/10.1111/j.1349-7006.2011.02175.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Myung JK, Cho HJ, Park C-K, Kim S-K, Phi JIH, Park S-H (2012) IDH1 mutation of gliomas with long-term survival analysis. Oncol Rep 28:1639–1644. https://doi.org/10.3892/or.2012.1994

    Article  CAS  PubMed  Google Scholar 

  39. Nobusawa S, Watanabe T, Kleihues P, Ohgaki H (2009) IDH1 mutations as molecular signature and predictive factor of secondary glioblastomas. Clin Cancer Res 15:6002–6007. https://doi.org/10.1158/1078-0432.CCR-09-0715

    Article  CAS  PubMed  Google Scholar 

  40. 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. https://doi.org/10.3892/ijo.2012.1564

    Article  CAS  PubMed  Google Scholar 

  41. Olar A, Wani KM, Alfaro-Munoz KD, Heathcock LE, van Thuijl HF, Gilbert MR, Armstrong TS, Sulman EP, Cahill DP, Vera-Bolanos E, Yuan Y, Reijneveld JC, Ylstra B, Wesseling P, Aldape KD (2015) IDH mutation status and role of WHO grade and mitotic index in overall survival in grade II–III diffuse gliomas. Acta Neuropathol 129:585–596. https://doi.org/10.1007/s00401-015-1398-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Parsons DW, Jones S, Zhang X, Lin JC-H, Leary RJ, Angenendt P, Mankoo P, Carter H, Siu I-M, Gallia GL, Olivi A, McLendon R, Rasheed BA, Keir S, Nikolskaya T, Nikolsky Y, Busam DA, Tekleab H, Diaz LAJ, Hartigan J, Smith DR, Strausberg RL, Marie SKN, Shinjo SMO, 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 321:1807–1812. https://doi.org/10.1126/science.1164382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Patel T, Bander ED, Venn RA, Powell T, Cederquist GY-M, Schaefer PM, Puchi LA, Akhmerov A, Ogilvie S, Reiner AS, Moussazadeh N, Tabar V (2017) The role of extent of resection in IDH1 wild-type or mutant low-grade gliomas. Neurosurgery 82:808–814. https://doi.org/10.1093/neuros/nyx265

    Article  PubMed Central  Google Scholar 

  44. Pignatti F, van den Bent M, Curran D, Debruyne C, Sylvester R, Therasse P, Afra D, Cornu P, Bolla M, Vecht C, Karim ABMF (2002) Prognostic factors for survival in adult patients with cerebral low-grade glioma. J Clin Oncol 20:2076–2084. https://doi.org/10.1200/JCO.2002.08.121

    Article  PubMed  Google Scholar 

  45. Potts MB, Smith JS, Molinaro AM, Berger MS (2012) Natural history and surgical management of incidentally discovered low-grade gliomas: clinical article. J Neurosurg 116:365–372. https://doi.org/10.3171/2011.9.JNS111068

    Article  PubMed  Google Scholar 

  46. Poulen G, Goze C, Rigau V, Duffau H (2018) Huge heterogeneity in survival data in a subset of adult IDH wild type lower-grade astrocytomas surgically removed. J Neurosurg:1–10. https://doi.org/10.3171/2017.10.JNS171825

  47. Ren X, Cui X, Lin S, Wang J, Jiang Z, Sui D, Li J, Wang Z (2012) Co-deletion of chromosome 1p/19q and IDH1/2 mutation in glioma subsets of brain tumors in Chinese patients. PLoS One 7:e32764. https://doi.org/10.1371/journal.pone.0032764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Reuss DE, Kratz A, Sahm F, Capper D, Schrimpf D, Koelsche C, Hovestadt V, Bewerunge-Hudler M, Jones DTW, Schittenhelm J, Mittelbronn M, Rushing E, Simon M, Westphal M, Unterberg A, Platten M, Paulus W, Reifenberger G, Tonn J-C, Aldape K, Pfister SM, Korshunov A, Weller M, Herold-Mende C, Wick W, Brandner S, von Deimling A (2015) Adult IDH wild type astrocytomas biologically and clinically resolve into other tumor entities. Acta Neuropathol 130:407–417. https://doi.org/10.1007/s00401-015-1454-8

    Article  CAS  PubMed  Google Scholar 

  49. Reuss DE, Sahm F, Schrimpf D, Wiestler B, Capper D, Koelsche C, Schweizer L, Korshunov A, Jones DTW, Hovestadt V, Mittelbronn M, Schittenhelm J, Herold-Mende C, Unterberg A, Platten M, Weller M, Wick W, Pfister SM, von Deimling A (2015) 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 129:133–146. https://doi.org/10.1007/s00401-014-1370-3

    Article  CAS  PubMed  Google Scholar 

  50. Roelz R, Strohmaier D, Jabbarli R, Kraeutle R, Egger K, Coenen VA, Weyerbrock A, Reinacher PC (2016) Residual tumor volume as best outcome predictor in low grade glioma—a nine-years near-randomized survey of surgery vs. biopsy. Sci Rep 6:32286. https://doi.org/10.1038/srep32286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Sanai N, Chang S, Berger MS (2011) Low-grade gliomas in adults: a review. J Neurosurg 115:948–965. https://doi.org/10.3171/2011.7.JNS101238

    Article  PubMed  Google Scholar 

  52. Scott JN, Brasher PMA, Sevick RJ, Rewcastle NB, Forsyth PA (2002) How often are nonenhancing supratentorial gliomas malignant? A population study. Neurology 59:947–949

    Article  CAS  PubMed  Google Scholar 

  53. Signorelli F, Guyotat J, Elisevich K, Barbagallo GMV (2010) Review of current microsurgical management of insular gliomas. Acta Neurochir 152:19–26. https://doi.org/10.1007/s00701-009-0450-y

    Article  PubMed  Google Scholar 

  54. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, Hau P, Brandes AA, Gijtenbeek J, Marosi C, Vecht CJ, Mokhtari K, Wesseling P, Villa S, Eisenhauer E, Gorlia T, Weller M, Lacombe D, Cairncross JG, Mirimanoff RORO (2009) Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 10:459–466. https://doi.org/10.1016/S1470-2045(09)70025-7

    Article  CAS  PubMed  Google Scholar 

  55. Tanaka K, Sasayama T, Mizukawa K, Takata K, Sulaiman NS, Nishihara M, Kohta M, Sasaki R, Hirose T, Itoh T, Kohmura E (2015) Combined IDH1 mutation and MGMT methylation status on long-term survival of patients with cerebral low-grade glioma. Clin Neurol Neurosurg 138:37–44. https://doi.org/10.1016/j.clineuro.2015.07.019

    Article  PubMed  Google Scholar 

  56. Tang C, yu ZZ, chao CL, Sun Z, Zhang Y, Qin Z, Yao Y, fu ZL (2016) Subgroup characteristics of insular low-grade glioma based on clinical and molecular analysis of 42 cases. J Neuro-Oncol 126:499–507. https://doi.org/10.1007/s11060-015-1989-5

    Article  CAS  Google Scholar 

  57. Tanriover N, Rhoton ALJ, Kawashima M, Ulm AJ, Yasuda A (2004) Microsurgical anatomy of the insula and the Sylvian fissure. J Neurosurg 100:891–922. https://doi.org/10.3171/jns.2004.100.5.0891

    Article  PubMed  Google Scholar 

  58. The Cancer Genome Atlas Research Network (2015) Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. N Engl J Med 372:2481–2498. https://doi.org/10.1056/NEJMoa1402121.Comprehensive

    Article  PubMed Central  Google Scholar 

  59. Thon N, Eigenbrod S, Kreth S, Lutz J, Tonn J-C, Kretzschmar H, Peraud A, Kreth F-W (2012) IDH1 mutations in grade II astrocytomas are associated with unfavorable progression-free survival and prolonged postrecurrence survival. Cancer 118:452–460. https://doi.org/10.1002/cncr.26298

    Article  CAS  PubMed  Google Scholar 

  60. Tierney JF, Stewart LA, Ghersi D, Burdett S, Sydes MR (2007) Practical methods for incorporating summary time-to-event data into meta-analysis. Trials 8:16. https://doi.org/10.1186/1745-6215-8-16

    Article  PubMed  PubMed Central  Google Scholar 

  61. van den Bent MJ, Dubbink HJ, Marie Y, Brandes AA, Taphoorn MJB, Wesseling P, Frenay M, Tijssen CC, Lacombe D, Idbaih A, van Marion R, Kros JM, Dinjens WNM, Gorlia T, Sanson M (2010) IDH1 and IDH2 mutations are prognostic but not predictive for outcome in anaplastic oligodendroglial tumors: a report of the European Organization for Research and Treatment of Cancer Brain Tumor Group. Clin Cancer Res 16:1597–1604. https://doi.org/10.1158/1078-0432.CCR-09-2902

    Article  CAS  PubMed  Google Scholar 

  62. Verger E, Salamero M, Conill C (1992) Can Karnofsky performance status be transformed to the Eastern Cooperative Oncology Group scoring scale and vice versa? Eur J Cancer 28:1328–1330. https://doi.org/10.1016/0959-8049(92)90510-9

    Article  Google Scholar 

  63. Wahl M, Phillips JJ, Molinaro AM, Lin Y, Perry A, Haas-Kogan DA, Costello JF, Dayal M, Butowski N, Clarke JL, Prados M, Nelson S, Berger MS, Chang SM (2017) Chemotherapy for adult low-grade gliomas: clinical outcomes by molecular subtype in a phase II study of adjuvant temozolomide. Neuro-Oncology 19:242–251. https://doi.org/10.1093/neuonc/now176

    Article  CAS  PubMed  Google Scholar 

  64. Waqar M, Hanif S, Brodbelt AR, Rathi N, Das K, Zakaria R, Walker C, Jenkinson MD (2015) Prognostic factors in lobar World Health Organization grade II astrocytomas. World Neurosurg 84:154–162. https://doi.org/10.1016/j.wneu.2015.02.045

    Article  PubMed  Google Scholar 

  65. Watanabe T, Nobusawa S, Kleihues P, Ohgaki H (2009) IDH1 mutations are early events in the development of astrocytomas and oligodendrogliomas. Am J Pathol 174:1149–1153. https://doi.org/10.2353/ajpath.2009.080958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M, Tugwell P (2013) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomized studies in meta-analyses. Ottawa Hosp Res Inst 1–4. https://doi.org/10.2307/632432

  67. Wijnenga MMJ, French PJ, Dubbink HJ, Dinjens WNM, Atmodimedjo PN, Kros JM, Smits M, Gahrmann R, Rutten G-J, Verheul JB, Fleischeuer R, Dirven CMF, Vincent AJPE, van den Bent MJ (2017) The impact of surgery in molecularly defined low-grade glioma: an integrated clinical, radiological and molecular analysis. Neuro-Oncology 20:103–112. https://doi.org/10.1093/neuonc/nox176

    Article  CAS  PubMed Central  Google Scholar 

  68. Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, Kos I, Batinic-Haberle I, Jones S, Riggins GJ, Friedman H, Friedman A, Reardon D, Herndon J, Kinzler KW, Velculescu VE, Vogelstein B, Bigner DD (2009) IDH1 and IDH2 mutations in gliomas. N Engl J Med 360:765–773. https://doi.org/10.1056/NEJMoa0808710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Yasargil MG, Von AK, Cavazos E, Doczi T, Reeves JD, Roth P (1992) Tumours of the limbic and paralimbic systems. Acta Neurochir 118:40–52

    Article  CAS  PubMed  Google Scholar 

  70. Youland RS, Kreofsky CR, Schomas DA, Brown PD, Buckner JC, Laack NN (2017) The impact of adjuvant therapy for patients with high-risk diffuse WHO grade II glioma. J Neuro-Oncol 135:535–543. https://doi.org/10.1007/s11060-017-2599-1

    Article  CAS  Google Scholar 

  71. Yuen TI, Morokoff AP, Bjorksten A, D’Abaco G, Paradiso L, Finch S, Wong D, Reid CA, Powell KL, Drummond KJ, Rosenthal MA, Kaye AH, O’Brien TJ (2012) Glutamate is associated with a higher risk of seizures in patients with gliomas. Neurology 79:883–889. https://doi.org/10.1212/WNL.0b013e318266fa89

    Article  CAS  PubMed  Google Scholar 

  72. Zeng A, Hu Q, Liu Y, Wang Z, Cui X, Li R, Yan W, You Y (2015) IDH1/2 mutation status combined with Ki-67 labeling index defines distinct prognostic groups in glioma. Oncotarget 6:30232–30238. https://doi.org/10.18632/oncotarget.4920

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Ms. Beth De Felici for the English revision.

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Authors and Affiliations

  1. Department of Neurosurgery, Azienda Ospedaliero Universitaria Pisana (AOUP), Via Paradisa 2, 56100, Pisa, Italy

    Davide Tiziano Di Carlo, Federico Cagnazzo, Nicola Benedetto & Paolo Perrini

  2. Department of Neurosurgery, Gui de Chauliac Hospital, CHU Montpellier, Montpellier University Medical Center, 80, Avenue Augustin Fliche, 34295, Montpellier, France

    Hugues Duffau

  3. Institute for Neuroscience of Montpellier, INSERM U1051, Team “Plasticity of Central Nervous System, Human Stem Cells and Glial Tumors,” Saint Eloi Hospital, Montpellier University Medical Center, Montpellier, France

    Hugues Duffau

  4. Department of Clinical and Experimental Medicine, Section of Statistics, University of Pisa, Pisa, Italy

    Riccardo Morganti

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  1. Davide Tiziano Di Carlo
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  2. Hugues Duffau
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  3. Federico Cagnazzo
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Correspondence to Davide Tiziano Di Carlo.

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Supplementary Fig. 1. Forest plot of IDH-wt prevalence among DLGG population. Supplementary Fig. 2. Forest plot of HR of recurrence for IDH-wt tumors among DLGG population. Supplementary Fig. 3. Forest plot of HR of malignant progression for IDH-wt tumors among DLGG population (PDF 468 kb)

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Di Carlo, D.T., Duffau, H., Cagnazzo, F. et al. IDH wild-type WHO grade II diffuse low-grade gliomas. A heterogeneous family with different outcomes. Systematic review and meta-analysis. Neurosurg Rev 43, 383–395 (2020). https://doi.org/10.1007/s10143-018-0996-3

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  • DOI: https://doi.org/10.1007/s10143-018-0996-3

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