WHO grade I meningiomas: classification-tree for prognostic factors of survival

Abstract

World Health Organization (WHO) grade I meningiomas are intracranial extracerebral tumors, in which microsurgery as a stand-alone therapy provides high rates of disease control and low recurrence rates. Our aim was to identify prognostic factors of overall survival and time-to-retreat (OS; TTR) in a cohort of patients with surgically managed WHO grade I meningioma. Patients with WHO grade I meningiomas from a retrospectively (1990 to 2002) and prospectively managed (2003 to 2010) databank of Oslo University Hospital, Norway, were included. The mean follow-up was 9.2 ± 5.7 years, with a total of 11,414 patient-years. One thousand three hundred fifty-five patients were included. The mean age was 58 ± 13.2, mean Karnofsky Performance Status (KPS) 92.6 ± 26.1 and female-to-male ratio 2.5:1. The 1-year, 5-year, 10-year, 15-year, and 20-year probabilities were 0.98, 0.91, 0.87, 0.84, and 0.8 for TTR. Patient age (OR 0.92 [0.91, 0.94]), male sex (OR 0.59 [0.45, 0.76]), preoperative KPS ≥ 70 (OR 2.22 [1.59, 3.13]), skull base location (OR 0.77 [0.60, 1]), and the occurrence of a postoperative hematoma (OR 0.44 [0.26, 0.76]) were identified as independent prognostic factors of OS. Patient age (OR 1.02 [1.01, 1.03]) and skull base location (OR 0.30 [0.21, 0.45]) were independent predictors of decreased PFS. Using a recursive partitioning analysis, we suggest a classification tree for the prediction of 5-year PFS based on patient and tumor characteristics. The findings from this cohort of meningioma WHO I patients helps to identify patients at risk of recurrence and tailor the therapeutic management.

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References

  1. 1.

    Aboukais R, Zairi F, Reyns N, Le Rhun E, Touzet G, Blond S, Lejeune J-P (2014) Surgery followed by radiosurgery: a deliberate valuable strategy in the treatment of intracranial meningioma. Clin Neurol Neurosurg 124:123–126. https://doi.org/10.1016/j.clineuro.2014.06.035

    Article  PubMed  Google Scholar 

  2. 2.

    Achey RL, Gittleman H, Schroer J, Khanna V, Kruchko C, Barnholtz-Sloan JS (2018) Non-malignant and malignant meningioma incidence and survival in the elderly from 2005-2015 using the central brain tumor registry of the United States. Neuro-Oncol. 21:380–391. https://doi.org/10.1093/neuonc/noy162

    Article  PubMed Central  Google Scholar 

  3. 3.

    Adeberg S, Hartmann C, Welzel T, Rieken S, Habermehl D, von Deimling A, Debus J, Combs SE (2012) Long-term outcome after radiotherapy in patients with atypical and malignant meningiomas--clinical results in 85 patients treated in a single institution leading to optimized guidelines for early radiation therapy. Int J Radiat Oncol Biol Phys 83:859–864. https://doi.org/10.1016/j.ijrobp.2011.08.010

    Article  PubMed  Google Scholar 

  4. 4.

    Adegbite AB, Khan MI, Paine KW, Tan LK (1983) The recurrence of intracranial meningiomas after surgical treatment. J Neurosurg 58:51–56. https://doi.org/10.3171/jns.1983.58.1.0051

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Aizer AA, Bi WL, Kandola MS, Lee EQ, Nayak L, Rinne ML, Norden AD, Beroukhim R, Reardon DA, Wen PY, Al-Mefty O, Arvold ND, Dunn IF, Alexander BM (2015) Extent of resection and overall survival for patients with atypical and malignant meningioma. Cancer 121:4376–4381. https://doi.org/10.1002/cncr.29639

    Article  PubMed  Google Scholar 

  6. 6.

    Aras Y, Akcakaya MO, Aydoseli A, Izgi N (2013) Staged surgery for sylvian fissure meningiomas without dural attachment: report of two cases. Clin Neurol Neurosurg 115:1527–1529. https://doi.org/10.1016/j.clineuro.2012.12.010

    Article  PubMed  Google Scholar 

  7. 7.

    Barrett OC, Hackney JR, McDonald AM, Willey CD, Bredel M, Fiveash JB (2018) Pathologic predictors of local recurrence in atypical meningiomas following gross total resection. Int J Radiat Oncol Biol Phys 103:453–459. https://doi.org/10.1016/j.ijrobp.2018.09.019

    Article  PubMed  Google Scholar 

  8. 8.

    Baumgarten P, Gessler F, Schittenhelm J, Skardelly M, Tews DS, Senft C, Dunst M, Imoehl L, Plate KH, Wagner M, Steinbach JP, Seifert V, Mittelbronn M, Harter PN (2016) Brain invasion in otherwise benign meningiomas does not predict tumor recurrence. Acta Neuropathol (Berl) 132:479–481. https://doi.org/10.1007/s00401-016-1598-1

    Article  Google Scholar 

  9. 9.

    Beks JW, de Windt HL (1988) The recurrence of supratentorial meningiomas after surgery. Acta Neurochir 95:3–5

    CAS  Article  Google Scholar 

  10. 10.

    Bi WL, Abedalthagafi M, Horowitz P, Agarwalla PK, Mei Y, Aizer AA, Brewster R, Dunn GP, Al-Mefty O, Alexander BM, Santagata S, Beroukhim R, Dunn IF (2016) Genomic landscape of intracranial meningiomas. J Neurosurg 125:525–535. https://doi.org/10.3171/2015.6.JNS15591

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Bowles AP, Perkins E (1999) Long-term remission of malignant brain tumors after intracranial infection: a report of four cases. Neurosurgery 44:636–642 discussion 642-643

    Article  Google Scholar 

  12. 12.

    Budohoski KP, Clerkin J, Millward CP, O’Halloran PJ, Waqar M, Looby S, Young AMH, Guilfoyle MR, Fitzroll D, Devadass A, Allinson K, Farrell M, Javadpour M, Jenkinson MD, Santarius T, Kirollos RW (2018) Predictors of early progression of surgically treated atypical meningiomas. Acta Neurochir 160:1813–1822. https://doi.org/10.1007/s00701-018-3593-x

    Article  PubMed  Google Scholar 

  13. 13.

    Chen Y-R, Ugiliweneza B, Burton E, Woo SY, Boakye M, Skirboll S (2017) The effect of postoperative infection on survival in patients with glioblastoma. J Neurosurg 127:807–811. https://doi.org/10.3171/2016.8.JNS16836

    Article  PubMed  Google Scholar 

  14. 14.

    Combs SE, Farzin M, Boehmer J, Oehlke O, Molls M, Debus J, Grosu A-L (2018) Clinical outcome after high-precision radiotherapy for skull base meningiomas: pooled data from three large German centers for radiation oncology. Radiother Oncol J Eur Soc Ther Radiol Oncol 127:274–279. https://doi.org/10.1016/j.radonc.2018.03.006

    Article  Google Scholar 

  15. 15.

    Corniola MV, Lemée J-M, Da Broi M, Joswig H, Schaller K, Helseth E, Meling TR (2019) Posterior fossa meningiomas: perioperative predictors of extent of resection, overall survival and progression-free survival. Acta Neurochir 161:1003–1011. https://doi.org/10.1007/s00701-019-03862-z

    Article  PubMed  Google Scholar 

  16. 16.

    Davidson L, Fishback D, Russin JJ, Weiss MH, Yu C, Pagnini PG, Zelman V, Apuzzo MLJ, Giannotta SL (2007) Postoperative gamma knife surgery for benign meningiomas of the cranial base. Neurosurg Focus 23:E6. https://doi.org/10.3171/FOC-07/10/E6

    Article  PubMed  Google Scholar 

  17. 17.

    De Bonis P, Albanese A, Lofrese G, de Waure C, Mangiola A, Pettorini BL, Pompucci A, Balducci M, Fiorentino A, Lauriola L, Anile C, Maira G (2011) Postoperative infection may influence survival in patients with glioblastoma: simply a myth. Neurosurgery 69:864–868; discussion 868-869. https://doi.org/10.1227/NEU.0b013e318222adfa

    Article  PubMed  Google Scholar 

  18. 18.

    Duntze J, Metellus P, Litre C-F, Eap C, Theret E, Colin P, Peruzzi P, Rousseaux P (2012) Management of WHO grade II and II meningiomas: retrospective study of surgical series of 36 cases at a single institution. Neurochirurgie 58:275–281. https://doi.org/10.1016/j.neuchi.2012.01.006

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Escribano Mesa JA, Alonso Morillejo E, Parrón Carreño T, Huete Allut A, Narro Donate JM, Méndez Román P, Contreras Jiménez A, Pedrero García F, Masegosa González J (2018) Risk of recurrence in operated parasagittal meningiomas: a logistic binary regression model. World Neurosurg 110:e112–e118. https://doi.org/10.1016/j.wneu.2017.10.087

    Article  PubMed  Google Scholar 

  20. 20.

    Fonkem E, Dandashi JA, Stroberg E, Garrett D, Harris FS, El Nihum IM, Cooper J, Dayawansa S, Huang JH (2016) A retrospective analysis of meningioma in Central Texas. J Epidemiol Glob Health 6:87–93. https://doi.org/10.1016/j.jegh.2016.01.001

    Article  PubMed  Google Scholar 

  21. 21.

    Fors MM, Viada CE, Gonzalez P (2017) Use of recursive partitioning analysis in clinical trials and meta-analysis of randomized clinical trials, 1990-2016. Rev Recent Clin Trials 12:3–7. https://doi.org/10.2174/1574887111666160916144658

    Article  PubMed  Google Scholar 

  22. 22.

    Franco DeMonte, Michael W. McDermott, Ossama Al-Mefty Al-Mefty’s Meningiomas, Thieme Medical. New-York

  23. 23.

    Goldbrunner R, Minniti G, Preusser M, Jenkinson MD, Sallabanda K, Houdart E, von Deimling A, Stavrinou P, Lefranc F, Lund-Johansen M, Moyal EC-J, Brandsma D, Henriksson R, Soffietti R, Weller M (2016) EANO guidelines for the diagnosis and treatment of meningiomas. Lancet Oncol 17:e383–e391. https://doi.org/10.1016/S1470-2045(16)30321-7

    Article  PubMed  Google Scholar 

  24. 24.

    Gousias K, Schramm J, Simon M (2016) The Simpson grading revisited: aggressive surgery and its place in modern meningioma management. J Neurosurg 125:551–560. https://doi.org/10.3171/2015.9.JNS15754

    Article  PubMed  Google Scholar 

  25. 25.

    Gupta PK, Sastry Kolluri VR, Das S, Chandra Mouli BA, Narayana Swamy KS, Das BS (1989) Recurrences in meningioma after surgery. Acta Neurochir 100:104–107

    CAS  Article  Google Scholar 

  26. 26.

    Hasseleid BF, Meling TR, Rønning P, Scheie D, Helseth E (2012) Surgery for convexity meningioma: Simpson grade I resection as the goal: clinical article. J Neurosurg 117:999–1006. https://doi.org/10.3171/2012.9.JNS12294

    Article  PubMed  Google Scholar 

  27. 27.

    Ildan F, Erman T, Göçer AI, Tuna M, Bağdatoğlu H, Cetinalp E, Burgut R (2007) Predicting the probability of meningioma recurrence in the preoperative and early postoperative period: a multivariate analysis in the midterm follow-up. Skull Base Off J North Am Skull Base Soc Al 17:157–171. https://doi.org/10.1055/s-2007-970554

    Article  Google Scholar 

  28. 28.

    Kallio M, Sankila R, Hakulinen T, Jääskeläinen J (1992) Factors affecting operative and excess long-term mortality in 935 patients with intracranial meningioma. Neurosurgery 31:2–12

    CAS  PubMed  Google Scholar 

  29. 29.

    Karimi S, Vyas MV, Gonen L, Tabasinejad R, Ostrom QT, Barnholtz-Sloan J, Suppiah S, Zadeh G, Aldape K (2017) Prognostic significance of preoperative neutrophilia on recurrence-free survival in meningioma. Neuro-Oncol 19:1503–1510. https://doi.org/10.1093/neuonc/nox089

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Kaur G, Sayegh ET, Larson A, Bloch O, Madden M, Sun MZ, Barani IJ, James CD, Parsa AT (2014) Adjuvant radiotherapy for atypical and malignant meningiomas: a systematic review. Neuro-Oncol 16:628–636. https://doi.org/10.1093/neuonc/nou025

    Article  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Konglund A, Rogne SG, Helseth E, Meling TR (2013) Meningioma surgery in the very old-validating prognostic scoring systems. Acta Neurochir 155:2263–2271; discussion 2271. https://doi.org/10.1007/s00701-013-1872-0

    Article  PubMed  Google Scholar 

  32. 32.

    Konglund A, Rogne SG, Lund-Johansen M, Scheie D, Helseth E, Meling TR (2013) Outcome following surgery for intracranial meningiomas in the aging. Acta Neurol Scand 127:161–169. https://doi.org/10.1111/j.1600-0404.2012.01692.x

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Kreßner M, Arlt F, Riepl W, Meixensberger J (2018) Prognostic factors of microsurgical treatment of intracranial meningiomas - a multivariate analysis. PLoS One 13:e0202520. https://doi.org/10.1371/journal.pone.0202520

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Lemée J-M, Corniola MV, Da Broi M, Joswig H, Scheie D, Schaller K, Helseth E, Meling TR (2019) Extent of resection in meningioma: predictive factors and clinical implications. Sci Rep 9:5944. https://doi.org/10.1038/s41598-019-42451-z

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. 35.

    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 (Berl) 131:803–820. https://doi.org/10.1007/s00401-016-1545-1

    Article  Google Scholar 

  36. 36.

    Markovic M, Antunovic V, Milenkovic S, Zivkovic N (2013) Prognostic value of peritumoral edema and angiogenesis in intracranial meningioma surgery. J BUON Off J Balk Union Oncol 18:430–436

    CAS  Google Scholar 

  37. 37.

    McCarthy BJ, Davis FG, Freels S, Surawicz TS, Damek DM, Grutsch J, Menck HR, Laws ER (1998) Factors associated with survival in patients with meningioma. J Neurosurg 88:831–839. https://doi.org/10.3171/jns.1998.88.5.0831

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Meling TR, Da Broi M, Scheie D, Helseth E (2018) Skull base versus non-skull base meningioma surgery in the elderly. Neurosurg Rev. https://doi.org/10.1007/s10143-018-1005-6

  39. 39.

    Meling TR, Da Broi M, Scheie D, Helseth E (2018) Meningiomas - skull-base vs non-skull base. Neurosurg Rev (in press 42:163–173. https://doi.org/10.1007/s10143-018-0976-7

    Article  PubMed  Google Scholar 

  40. 40.

    Meling TR, Da Broi M, Scheie D, Helseth E, Smoll NR (2019) Meningioma surgery-are we making progress? World Neurosurg 125:e205–e213. https://doi.org/10.1016/j.wneu.2019.01.042

    Article  PubMed  Google Scholar 

  41. 41.

    Ostrom QT, Bauchet L, Davis FG, Deltour I, Fisher JL, Langer CE, Pekmezci M, Schwartzbaum JA, Turner MC, Walsh KM, Wrensch MR, Barnholtz-Sloan JS (2014) The epidemiology of glioma in adults: a “state of the science” review. Neuro-Oncol. 16:896–913. https://doi.org/10.1093/neuonc/nou087

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. 42.

    Patil CG, Veeravagu A, Lad SP, Boakye M (2010) Craniotomy for resection of meningioma in the elderly: a multicentre, prospective analysis from the National Surgical Quality Improvement Program. J Neurol Neurosurg Psychiatry 81:502–505. https://doi.org/10.1136/jnnp.2009.185074

    Article  PubMed  Google Scholar 

  43. 43.

    Phonwijit L, Khawprapa C, Sitthinamsuwan B (2017) Progression-free survival and factors associated with postoperative recurrence in 126 patients with atypical intracranial meningioma. World Neurosurg 107:698–705. https://doi.org/10.1016/j.wneu.2017.08.057

    Article  PubMed  Google Scholar 

  44. 44.

    Preusser M, Brastianos PK, Mawrin C (2018) Advances in meningioma genetics: novel therapeutic opportunities. Nat Rev Neurol 14:106–115. https://doi.org/10.1038/nrneurol.2017.168

    CAS  Article  PubMed  Google Scholar 

  45. 45.

    Sankila R, Kallio M, Jääskeläinen J, Hakulinen T (1992) Long-term survival of 1986 patients with intracranial meningioma diagnosed from 1953 to 1984 in Finland. Comparison of the observed and expected survival rates in a population-based series. Cancer 70:1568–1576

    CAS  Article  Google Scholar 

  46. 46.

    Sanna M, Bacciu A, Falcioni M, Taibah A, Piazza P (2007) Surgical management of jugular foramen meningiomas: a series of 13 cases and review of the literature. Laryngoscope 117:1710–1719. https://doi.org/10.1097/MLG.0b013e3180cc20a3

    Article  PubMed  Google Scholar 

  47. 47.

    Savardekar AR, Patra DP, Bir S, Thakur JD, Mohammed N, Bollam P, Georgescu M-M, Nanda A (2018) Differential tumor progression patterns in skull base versus non-skull base meningiomas: a critical analysis from a long-term follow-up study and review of literature. World Neurosurg 112:e74–e83. https://doi.org/10.1016/j.wneu.2017.12.035

    Article  PubMed  Google Scholar 

  48. 48.

    Schipmann S, Schwake M, Sporns PB, Voß KM, Sicking J, Spille DC, Hess K, Paulus W, Stummer W, Brokinkel B (2018) Is the Simpson grading system applicable to estimate the risk of tumor progression after microsurgery for recurrent intracranial meningioma? World Neurosurg 119:e589–e597. https://doi.org/10.1016/j.wneu.2018.07.215

    Article  PubMed  Google Scholar 

  49. 49.

    Shakir SI, Souhami L, Petrecca K, Mansure JJ, Singh K, Panet-Raymond V, Shenouda G, Al-Odaini AA, Abdulkarim B, Guiot M-C (2018) Prognostic factors for progression in atypical meningioma. J Neurosurg 1(9):1240–1248. https://doi.org/10.3171/2017.6.JNS17120

    Article  Google Scholar 

  50. 50.

    Sicking J, Voß KM, Spille DC, Schipmann S, Holling M, Paulus W, Hess K, Steinbicker AU, Stummer W, Grauer O, Wölfer J, Brokinkel B (2018) The evolution of cranial meningioma surgery-a single-center 25-year experience. Acta Neurochir 160:1801–1812. https://doi.org/10.1007/s00701-018-3617-6

    Article  PubMed  Google Scholar 

  51. 51.

    da Silva CE, Peixoto de Freitas PE (2016) Recurrence of skull base meningiomas: the role of aggressive removal in surgical treatment. J Neurol Surg Part B Skull Base 77:219–225. https://doi.org/10.1055/s-0035-1566251

    Article  Google Scholar 

  52. 52.

    Simpson D (1957) The recurrence of intracranial meningiomas after surgical treatment. J Neurol Neurosurg Psychiatry 20:22–39

    CAS  Article  Google Scholar 

  53. 53.

    Takase H, Kawasaki T, Tateishi K, Yokoyama T-A, Murata H, Kawahara N (2017) Characteristics and surgical strategies for posterior clinoid process meningioma: two case reports and review of the literature. Neurosurg Rev 40:163–169. https://doi.org/10.1007/s10143-016-0774-z

    Article  PubMed  Google Scholar 

  54. 54.

    Vasudevan HN, Braunstein SE, Phillips JJ, Pekmezci M, Tomlin BA, Wu A, Reis GF, Magill ST, Zhang J, Feng FY, Nicholaides T, Chang SM, Sneed PK, McDermott MW, Berger MS, Perry A, Raleigh DR (2018) Comprehensive molecular profiling identifies FOXM1 as a key transcription factor for meningioma proliferation. Cell Rep 22:3672–3683. https://doi.org/10.1016/j.celrep.2018.03.013

    CAS  Article  PubMed  Google Scholar 

  55. 55.

    Voß KM, Spille DC, Sauerland C, Suero Molina E, Brokinkel C, Paulus W, Stummer W, Holling M, Jeibmann A, Brokinkel B (2017) The Simpson grading in meningioma surgery: does the tumor location influence the prognostic value? J Neuro-Oncol 133:641–651. https://doi.org/10.1007/s11060-017-2481-1

    Article  Google Scholar 

  56. 56.

    Zouaoui S, Darlix A, Rigau V, Mathieu-Daudé H, Bauchet F, Bessaoud F, Fabbro-Peray P, Trétarre B, Figarella-Branger D, Taillandier L, Loiseau H, Bauchet L, French Brain Tumor DataBase (FBTDB) Participants and Investigators, with the participation of the Société française de neurochirurgie (SFNC), Club de neuro-oncologie de la SFNC, Société française de neuropathologie (SFNP), Association des neuro-oncologues d’expression française (ANOCEF) (2018) Descriptive epidemiology of 13,038 newly diagnosed and histologically confirmed meningiomas in France: 2006–2010. Neurochirurgie 64:15–21. doi: https://doi.org/10.1016/j.neuchi.2014.11.013

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Acknowledgments

The authors would like to thank Bernt Filip Hasseleid MD, Andreas Mathisen MD, Andreas Hessen Schei MD, and Kristina M. Ødegaard MD for their valuable contributions in collecting data for this manuscript and the neurosurgeons of Rikshospitalet and Ullevaal for their dedicated patient care.

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Data collection: TRM, EH, DS.

Statistical analysis: JML.

Manuscript drafting: JML, HJ, MDB, MVC, TRM.

Critical revision: all authors.

Manuscript approval: all authors.

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Correspondence to Jean-Michel Lemée.

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Lemée, J., Joswig, H., Da Broi, M. et al. WHO grade I meningiomas: classification-tree for prognostic factors of survival. Neurosurg Rev 43, 749–758 (2020). https://doi.org/10.1007/s10143-019-01117-0

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Keywords

  • Meningioma
  • Overall survival
  • Prognostic factors
  • Time-to-retreat
  • WHO grade I