Anatomical and subcortical invasiveness in diffuse low-grade astrocytomas differ between IDH status and provide prognostic information
Keywords:
Astrocytomas, low-grade gliomas, IDH status, DTI, white matter, Brain-Grid
Abstract
Background: Diffuse astrocytomas preferentially infiltrate eloquent areas affecting the outcome. A preoperative understanding of isocitrate dehydrogenase (IDH) status may offer opportunities for specific targeted therapies impacting treatment management. The aim of this study was to analyze clinical, topographical, radiological in WHO 2 astrocytomas with different IDH status and the long-term patient’s outcome.
Methods: A series of confirmed WHO 2 astrocytoma patients (between 2005 and 2015) were retrospectively analyzed. MRI sequences (FLAIR) were used for tumor volume segmentation and to create a frequency map of their locations into the Montreal Neurological Institute (MNI) space. The Brain-Grid (BG) system (standardized radiological tool of intersected lines according to anatomical landmarks) was used as an overlay for infiltration analysis of each tumor. Long-term follow-up was used to perform a survival analysis.
Results: Forty patients with confirmed IDH status (26 IDH-mutant, IDHm/14 IDH-wild type, IDHwt) according to WHO 2021 classification were included with a mean follow-up of 7.8 years. IDHm astrocytomas displayed a lower number of BG-voxels (P < 0.05) and were preferentially located in the anterior insular region. IDHwt group displayed a posterior insular and peritrigonal location. IDHwt group displayed a shorter OS compared with IDHm (P < 0.05), with the infiltration of 7 or more BG-voxels as an independent factor predicting a shorter OS.
Conclusions: IDHm and IDHwt astrocytomas differed in preferential location, number of BG-voxels and OS at long follow-up time. The number of BG-voxels affected the OS in IDHwt was possibly reflecting higher tumor invasiveness. We encourage the systematic use of alternative observational tools, such as gradient maps and the Brain-Grid analysis, to better detect differences of tumor invasiveness in diffuse low-grade gliomas subtypes.
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References
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26. Latini F, Larsson EM, Ryttlefors M. Rapid and accurate MRI segmentation of peritumoral brain edema in meningiomas. Clin Neuroradiol. 2017 Jun;27:145–52. doi: 10.1007/s00062-015-0481-0
27. Zetterling M, Roodakker KR, Berntsson SG, Edqvist PH, Latini F, Landtblom AM, et al. Extension of diffuse low-grade gliomas beyond radiological borders as shown by the coregistration of histopathological and magnetic resonance imaging data. JNS. 2016 Nov;125:1155–66. doi: 10.3171/2015.10.JNS15583
28. Latini F, Axelson H, Fahlström M, Jemstedt M, Alberius Munkhammar Å, Zetterling M, et al. Role of preoperative assessment in predicting tumor-induced plasticity in patients with diffuse gliomas. JCM. 2021 Mar 7;10:1108. doi: 10.3390/jcm10051108
29. Smith JS, Chang EF, Lamborn KR, Chang SM, Prados MD, Cha S, et al. Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol. 2008 Mar 10;26:1338–45. doi: 10.1200/JCO.2007.13.9337
30. Motomura K, Chalise L, Ohka F, Aoki K, Tanahashi K, Hirano M, et al. Neurocognitive and functional outcomes in patients with diffuse frontal lower-grade gliomas undergoing intraoperative awake brain mapping. J Neurosurg. 2019 May 17;132(6):1683–1691. doi: 10.1093/neuros/nyaa447_847
31. Duffau H. Diffuse low-grade glioma, oncological outcome and quality of life: a surgical perspective. Curr Opin Oncol. 2018;30:383–9. doi: 10.1097/CCO.0000000000000483
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34. Still MEH, Roux A, Huberfeld G, Bauchet L, Baron MH, Fontaine D, et al. Extent of resection and residual tumor thresholds for postoperative total seizure freedom in epileptic adult patients harboring a supratentorial diffuse low-grade glioma. Neurosurgery. 2019 Aug 1;85(2):E332–E340. doi: 10.1093/neuros/nyy481
35. Pallud J, Blonski M, Mandonnet E, Audureau E, Fontaine D, Sanai N, et al. Velocity of tumor spontaneous expansion predicts long-term outcomes for diffuse low-grade gliomas. Neuro-Oncology. 2013 May;15:595–606. doi: 10.1093/neuonc/nos331
36. Hartmann C, Hentschel B, Wick W, Capper D, Felsberg J, Simon M, et al. Vol. 120, Acta neuropathologica. Acta Neuropathol; 2010 [cited 2020 Sep 21]. Patients with IDH1 wild type anaplastic astrocytomas exhibit worse prognosis than IDH1-mutated glioblastomas, and IDH1 mutation status accounts for the unfavorable prognostic effect of higher age: implications for classification of gliomas. Available from: https://pubmed.ncbi.nlm.nih.gov/21088844/
37. Metellus P, Coulibaly B, Colin C, de Paula AM, Vasiljevic A, Taieb D, et al. Absence of IDH mutation identifies a novel radiologic and molecular subtype of WHO grade II gliomas with dismal prognosis. Acta Neuropathol. 2010 Dec;120:719–29. doi: 10.1007/s00401-010-0777-8
38. Ng S, Duffau H. Brain plasticity profiling as a key support to therapeutic decision-making in low-grade glioma oncological strategies. Cancers (Basel). 2023 Jul 20;15:3698. doi: 10.3390/cancers15143698
39. Poulen G, Gozé C, Rigau V, Duffau H. Huge heterogeneity in survival in a subset of adult patients with resected, wild-type isocitrate dehydrogenase status, WHO grade II astrocytomas. J Neurosurg. 2018 Apr 20;130(4):1289–1298.
40. Vivas-Buitrago T, Domingo RA, Tripathi S, De Biase G, Brown D, Akinduro OO, et al. Influence of supramarginal resection on survival outcomes after gross-total resection of IDH–wild-type glioblastoma. J Neurosurg. 2022 Jan 1;136:1–8. doi: 10.3171/2020.10.JNS203366
41. Jacobo JA, Mejia-Perez S, Moreno-Jimenez S. The role of neoadjuvant therapy to improve the extent of resection in ‘Unresectable’ gliomas. World Neurosurg. 2021 Feb;146:53–8. doi: 10.1016/j.wneu.2020.10.109
42. Blonski M, Taillandier L, Herbet G, Maldonado IL, Beauchesne P, Fabbro M, et al. Combination of neoadjuvant chemotherapy followed by surgical resection as a new strategy for WHO grade II gliomas: a study of cognitive status and quality of life. J Neurooncol. 2012 Jan;106:353–66. doi: 10.1007/s11060-011-0670-x
43. Mellinghoff IK, van den Bent MJ, Blumenthal DT, Touat M, Peters KB, Clarke J, et al. Vorasidenib in IDH1- or IDH2-mutant low-grade glioma. N Engl J Med. 2023 Aug 17;389:589–601. doi: 10.1056/NEJMoa2304194
44. Mellinghoff IK, Lu M, Wen PY, Taylor JW, Maher EA, Arrillaga-Romany I, et al. Vorasidenib and ivosidenib in IDH1-mutant low-grade glioma: a randomized, perioperative phase 1 trial. Nat Med. 2023 Mar;29:615–22. doi: 10.1038/s41591-022-02141-2
2. Ostrom QT, Gittleman H, Fulop J, Liu M, Blanda R, Kromer C, et al. CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2008–2012. Neuro-Oncology. 2015 Oct;17 Suppl 4:iv1–62. doi: 10.1093/neuonc/nov189
3. Louis DN, Perry A, Wesseling P, Brat DJ, Cree IA, Figarella-Branger D, et al. The 2021 WHO classification of tumors of the central nervous system: a summary. Neuro Oncol. 2021 Aug 2;23:1231–51. doi: 10.1093/neuonc/noab106
4. Corell A, Carstam L, Smits A, Henriksson R, Jakola AS. Age and surgical outcome of low-grade glioma in Sweden. Acta Neurol Scand. 2018 Oct;138:359–68. doi: 10.1093/neuonc/noab106
5. Smits A, Jakola AS. Clinical presentation, natural history, and prognosis of diffuse low-grade gliomas. Neurosurg Clin N Am. 2019 Jan;30:35–42. doi: 10.1016/j.nec.2018.08.002
6. Youssef G, Miller JJ. Lower grade gliomas. Curr Neurol Neurosci Rep. 2020;20. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7244462/ [cited 25 August 2020].
7. Olar A, Wani KM, Alfaro-Munoz KD, Heathcock LE, van Thuijl HF, Gilbert MR, et al. IDH mutation status and role of WHO grade and mitotic index in overall survival in grade II-III diffuse gliomas. Acta Neuropathol. 2015 Apr;129:585–96. doi: 10.1007/s00401-015-1398-z
8. Reuss DE, Kratz A, Sahm F, Capper D, Schrimpf D, Koelsche C, et al. Adult IDH wild type astrocytomas biologically and clinically resolve into other tumor entities. Acta Neuropathol. 2015 Sep;130:407–17. doi: 10.1007/s00401-015-1454-8
9. Duffau H. A personalized longitudinal strategy in low-grade glioma patients: predicting oncological and neural interindividual variability and its changes over years to think one step ahead. J Pers Med. 2022 Oct 1;12:1621. doi: 10.3390/jpm12101621
10. Mandonnet E, Duffau H. An attempt to conceptualize the individual onco-functional balance: why a standardized treatment is an illusion for diffuse low-grade glioma patients. Crit Rev Oncol Hematol. 2018 Feb;122:83–91. doi: 10.1016/j.critrevonc.2017.12.008
11. Jakola AS, Myrmel KS, Kloster R, Torp SH, Lindal S, Unsgård G, et al. Comparison of a strategy favoring early surgical resection vs a strategy favoring watchful waiting in low-grade gliomas. JAMA. 2012 Nov 14;308:1881–8. doi: 10.1001/jama.2012.12807
12. Jakola AS, Unsgård G, Myrmel KS, Kloster R, Torp SH, Losvik OK, 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 Dec;155:2227–35. doi: 10.1007/s00701-013-1869-8
13. Jakola AS, Unsgård G, Myrmel KS, Kloster R, Torp SH, Sagberg LM, et al. Surgical strategies in low-grade gliomas and implications for long-term quality of life. J Clin Neurosci. 2014 Aug;21:1304–9. doi: 10.1016/j.jocn.2013.11.027
14. Ius T, Angelini E, Thiebaut de Schotten M, Mandonnet E, Duffau H. Evidence for potentials and limitations of brain plasticity using an atlas of functional resectability of WHO grade II gliomas: towards a ‘minimal common brain’. Neuroimage. 2011 Jun 1;56:992–1000. doi: 10.1016/j.neuroimage.2011.03.022
15. Sarubbo S, De Benedictis A, Merler S, Mandonnet E, Balbi S, Granieri E, et al. Towards a functional atlas of human white matter. Hum Brain Mapp. 2015 Aug;36:3117–36. doi: 10.1002/hbm.22832
16. Parisot S, Darlix A, Baumann C, Zouaoui S, Yordanova Y, Blonski M, et al. A probabilistic atlas of diffuse WHO Grade II glioma locations in the brain. PLoS One. 2016 Jan 11;11:e0144200. doi: 10.1371/journal.pone.0144200
17. Latini F, Fahlström M, Hesselager G, Zetterling M, Ryttlefors M. Differences in the preferential location and invasiveness of diffuse low‐grade gliomas and their impact on outcome. Cancer Med. 2020 Jun 14;9:5446–58. doi: 10.1002/cam4.3216
18. Giese A, Loo MA, Rief MD, Tran N, Berens ME. Substrates for astrocytoma invasion. Neurosurgery. 1995 Aug;37:294–301; discussion 301–2. doi: 10.1097/00006123-199508000-00015
19. Aghi MK, Nahed BV, Sloan AE, Ryken TC, Kalkanis SN, Olson JJ. The role of surgery in the management of patients with diffuse low grade glioma: a systematic review and evidence-based clinical practice guideline. J Neurooncol. 2015 Dec;125:503–30. doi: 10.1007/s11060-015-1867-1
20. Van den Bent MJ, Smits M, Kros JM, Chang SM. Diffuse infiltrating oligodendroglioma and astrocytoma. J Clin Oncol. 2017 Jul 20;35:2394–401. doi: 10.1200/JCO.2017.72.6737
21. Jakola AS, Unsgård G, Myrmel KS, Kloster R, Torp SH, Lindal S, et al. Low grade gliomas in eloquent locations – implications for surgical strategy, survival and long term quality of life. PLoS One. 2012;7:e51450. doi: 10.1371/journal.pone.0051450
22. Duffau H. Dynamic interplay between lower-grade glioma instability and brain metaplasticity: proposal of an original model to guide the therapeutic strategy. Cancers. 2021 Sep 23;13:4759. doi: 10.3390/cancers13194759
23. Duffau H, Capelle L. Preferential brain locations of low-grade gliomas. Cancer. 2004 Jun 15;100:2622–6. doi: 10.1002/cncr.20297
24. Capelle L, Fontaine D, Mandonnet E, Taillandier L, Golmard JL, Bauchet L, et al. Spontaneous and therapeutic prognostic factors in adult hemispheric World Health Organization Grade II gliomas: a series of 1097 cases: clinical article. J Neurosurg. 2013 Jun;118:1157–68. doi: 10.3171/2013.1.JNS121
25. Latini F, Fahlström M, Berntsson SG, Larsson EM, Smits A, Ryttlefors M. A novel radiological classification system for cerebral gliomas: the Brain-Grid. PLoS One. 2019;14:e0211243. doi: 10.1371/journal.pone.0211243
26. Latini F, Larsson EM, Ryttlefors M. Rapid and accurate MRI segmentation of peritumoral brain edema in meningiomas. Clin Neuroradiol. 2017 Jun;27:145–52. doi: 10.1007/s00062-015-0481-0
27. Zetterling M, Roodakker KR, Berntsson SG, Edqvist PH, Latini F, Landtblom AM, et al. Extension of diffuse low-grade gliomas beyond radiological borders as shown by the coregistration of histopathological and magnetic resonance imaging data. JNS. 2016 Nov;125:1155–66. doi: 10.3171/2015.10.JNS15583
28. Latini F, Axelson H, Fahlström M, Jemstedt M, Alberius Munkhammar Å, Zetterling M, et al. Role of preoperative assessment in predicting tumor-induced plasticity in patients with diffuse gliomas. JCM. 2021 Mar 7;10:1108. doi: 10.3390/jcm10051108
29. Smith JS, Chang EF, Lamborn KR, Chang SM, Prados MD, Cha S, et al. Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol. 2008 Mar 10;26:1338–45. doi: 10.1200/JCO.2007.13.9337
30. Motomura K, Chalise L, Ohka F, Aoki K, Tanahashi K, Hirano M, et al. Neurocognitive and functional outcomes in patients with diffuse frontal lower-grade gliomas undergoing intraoperative awake brain mapping. J Neurosurg. 2019 May 17;132(6):1683–1691. doi: 10.1093/neuros/nyaa447_847
31. Duffau H. Diffuse low-grade glioma, oncological outcome and quality of life: a surgical perspective. Curr Opin Oncol. 2018;30:383–9. doi: 10.1097/CCO.0000000000000483
32. McKhann GM, Duffau H. Low-grade glioma: epidemiology, pathophysiology, clinical features, and treatment. Neurosurg Clin N Am. 2019;30:xiii–xiv. doi: 10.1016/j.nec.2018.10.001
33. Pallud J, Fontaine D, Duffau H, Mandonnet E, Sanai N, Taillandier L, et al. Natural history of incidental World Health Organization grade II gliomas. Ann Neurol. 2010 Nov;68:727–33. doi: 10.1002/ana.22106
34. Still MEH, Roux A, Huberfeld G, Bauchet L, Baron MH, Fontaine D, et al. Extent of resection and residual tumor thresholds for postoperative total seizure freedom in epileptic adult patients harboring a supratentorial diffuse low-grade glioma. Neurosurgery. 2019 Aug 1;85(2):E332–E340. doi: 10.1093/neuros/nyy481
35. Pallud J, Blonski M, Mandonnet E, Audureau E, Fontaine D, Sanai N, et al. Velocity of tumor spontaneous expansion predicts long-term outcomes for diffuse low-grade gliomas. Neuro-Oncology. 2013 May;15:595–606. doi: 10.1093/neuonc/nos331
36. Hartmann C, Hentschel B, Wick W, Capper D, Felsberg J, Simon M, et al. Vol. 120, Acta neuropathologica. Acta Neuropathol; 2010 [cited 2020 Sep 21]. Patients with IDH1 wild type anaplastic astrocytomas exhibit worse prognosis than IDH1-mutated glioblastomas, and IDH1 mutation status accounts for the unfavorable prognostic effect of higher age: implications for classification of gliomas. Available from: https://pubmed.ncbi.nlm.nih.gov/21088844/
37. Metellus P, Coulibaly B, Colin C, de Paula AM, Vasiljevic A, Taieb D, et al. Absence of IDH mutation identifies a novel radiologic and molecular subtype of WHO grade II gliomas with dismal prognosis. Acta Neuropathol. 2010 Dec;120:719–29. doi: 10.1007/s00401-010-0777-8
38. Ng S, Duffau H. Brain plasticity profiling as a key support to therapeutic decision-making in low-grade glioma oncological strategies. Cancers (Basel). 2023 Jul 20;15:3698. doi: 10.3390/cancers15143698
39. Poulen G, Gozé C, Rigau V, Duffau H. Huge heterogeneity in survival in a subset of adult patients with resected, wild-type isocitrate dehydrogenase status, WHO grade II astrocytomas. J Neurosurg. 2018 Apr 20;130(4):1289–1298.
40. Vivas-Buitrago T, Domingo RA, Tripathi S, De Biase G, Brown D, Akinduro OO, et al. Influence of supramarginal resection on survival outcomes after gross-total resection of IDH–wild-type glioblastoma. J Neurosurg. 2022 Jan 1;136:1–8. doi: 10.3171/2020.10.JNS203366
41. Jacobo JA, Mejia-Perez S, Moreno-Jimenez S. The role of neoadjuvant therapy to improve the extent of resection in ‘Unresectable’ gliomas. World Neurosurg. 2021 Feb;146:53–8. doi: 10.1016/j.wneu.2020.10.109
42. Blonski M, Taillandier L, Herbet G, Maldonado IL, Beauchesne P, Fabbro M, et al. Combination of neoadjuvant chemotherapy followed by surgical resection as a new strategy for WHO grade II gliomas: a study of cognitive status and quality of life. J Neurooncol. 2012 Jan;106:353–66. doi: 10.1007/s11060-011-0670-x
43. Mellinghoff IK, van den Bent MJ, Blumenthal DT, Touat M, Peters KB, Clarke J, et al. Vorasidenib in IDH1- or IDH2-mutant low-grade glioma. N Engl J Med. 2023 Aug 17;389:589–601. doi: 10.1056/NEJMoa2304194
44. Mellinghoff IK, Lu M, Wen PY, Taylor JW, Maher EA, Arrillaga-Romany I, et al. Vorasidenib and ivosidenib in IDH1-mutant low-grade glioma: a randomized, perioperative phase 1 trial. Nat Med. 2023 Mar;29:615–22. doi: 10.1038/s41591-022-02141-2
Published
2024-09-03
How to Cite
Zetterling M., Fahlström M., & Latini F. (2024). Anatomical and subcortical invasiveness in diffuse low-grade astrocytomas differ between IDH status and provide prognostic information. Upsala Journal of Medical Sciences, 129, e10799. https://doi.org/10.48101/ujms.v129.10799
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