Abstract
Background
Despite considerable rates of recurrence and mortality in atypical meningiomas, reliable predictors for estimating postoperative long-term prognosis remain elusive.
Methods
Clinical, histopathological, and radiological variables from 138 patients, including 64 females and 74 males (46% and 54%, median age 62 years), who underwent surgery for intracranial atypical meningioma were retrospectively analyzed. Associations between variables and recurrence and mortality were investigated using uni- and multivariate analyses.
Results
Gross total (GTR) and subtotal resection (STR) was achieved in 81% and 19% of cases, respectively. Within a median follow-up of 62 months, recurrence occurred in 52 (38%) and mortality in 22 (16%) cases. In patients who did not receive adjuvant irradiation, recurrence rates were higher after STR than after GTR (32% vs 63%, p = 0.025). In univariate analyses, only intratumoral calcifications on preoperative MRI (p = 0.012) and the presence of brain invasion in the absence of other histological grading criteria (p = 0.010) were correlated with longer progression-free intervals (PFI). In multivariate analyses, patient age was positively (HR 1.03, 95%CI 1.04–1.05; p = 0.018) and the presence of brain invasion as the only grading criterion (HR 0.37, 95%CI 0.19–0.74; p = 0.005) was negatively related with progression, while rising age at the time of surgery (HR 1.07, 95%CI 1.03–1.12; p = 0.001) was prognostic for mortality.
Conclusions
PFI was longer in brain invasive but otherwise histological benign meningiomas and in tumors displaying calcifications on preoperative MRI. Advancing patient age and lower Karnofsky Performance Score were associated with higher overall mortality.
Similar content being viewed by others
References
Adeli A, Hess K, Mawrin C, Streckert EMS, Stummer W, Paulus W, Kemmling A, Holling M, Heindel W, Schmidt R, Spille DC, Sporns PB, Brokinkel B (2018) Prediction of brain invasion in patients with meningiomas using preoperative magnetic resonance imaging. Oncotarget 9:35974–35982
Aghi MK, Carter BS, Cosgrove GR, Ojemann RG, Amin-Hanjani S, Martuza RL, Curry WT Jr, Barker FG II (2009) Long-term recurrence rates of atypical meningiomas after gross total resection with or without postoperative adjuvant radiation. Neurosurgery 64:56–60 discussion 60
Aizer AA, Arvold ND, Catalano P, Claus EB, Golby AJ, Johnson MD, Al-Mefty O, Wen PY, Reardon DA, Lee EQ, Nayak L, Rinne ML, Beroukhim R, Weiss SE, Ramkissoon SH, Abedalthagafi M, Santagata S, Dunn IF, Alexander BM (2014) Adjuvant radiation therapy, local recurrence, and the need for salvage therapy in atypical meningioma. Neuro-Oncology 16:1547–1553
Biczok A, Kraus T, Suchorska B, Terpolilli NA, Thorsteinsdottir J, Giese A, Tonn JC, Schichor C (2018) TERT promoter mutation is associated with worse prognosis in WHO grade II and III meningiomas. J Neuro-Oncol. https://doi.org/10.1007/s11060-018-2912-7
Brokinkel B, Hess K, Mawrin C (2017) Brain invasion in meningiomas-clinical considerations and impact of neuropathological evaluation: a systematic review. Neuro-Oncology 19:1298–1307
Brokinkel B, Holling M, Spille DC, Hess K, Sauerland C, Bleimuller C, Paulus W, Wolfer J, Stummer W (2017) Surgery for meningioma in the elderly and long-term survival: comparison with an age- and sex-matched general population and with younger patients. J Neurosurg 126:1201–1211
Brokinkel B, Stummer W, Sporns P (2018) Simpson grade IV resections of skull base meningiomas: does the postoperative tumor volume impact progression? J Neuro-Oncol 137(1):219–221
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
Champeaux C, Dunn L (2016) World Health Organization grade II meningioma: a 10-year retrospective study for recurrence and prognostic factor assessment. World Neurosurg 89:180–186
Champeaux C, Wilson E, Shieff C, Khan AA, Thorne L (2016) WHO grade II meningioma: a retrospective study for outcome and prognostic factor assessment. J Neuro-Oncol 129:337–345
Chen WC, Magill ST, Wu A, Vasudevan HN, Morin O, Aghi MK, Theodosopoulos PV, Perry A, McDermott MW, Sneed PK, Braunstein SE, Raleigh DR (2018) Histopathological features predictive of local control of atypical meningioma after surgery and adjuvant radiotherapy. J Neurosurg. https://doi.org/10.3171/2017.9.JNS171609
Endo T, Narisawa A, Ali HS, Murakami K, Watanabe T, Watanabe M, Jokura H, Endo H, Fujimura M, Sonoda Y, Tominaga T (2016) A study of prognostic factors in 45 cases of atypical meningioma. Acta Neurochir 158:1661–1667
Goldbrunner R, Minniti G, Preusser M, Jenkinson MD, Sallabanda K, Houdart E, von Deimling A, Stavrinou P, Lefranc F, Lund-Johansen M, Moyal EC, Brandsma D, Henriksson R, Soffietti R, Weller M (2016) EANO guidelines for the diagnosis and treatment of meningiomas. Lancet Oncol 17:e383–e391
Goutagny S, Nault JC, Mallet M, Henin D, Rossi JZ, Kalamarides M (2014) High incidence of activating TERT promoter mutations in meningiomas undergoing malignant progression. Brain Pathol 24:184–189
Hammouche S, Clark S, Wong AH, Eldridge P, Farah JO (2014) Long-term survival analysis of atypical meningiomas: survival rates, prognostic factors, operative and radiotherapy treatment. Acta Neurochir 156:1475–1481
Hasan S, Young M, Albert T, Shah AH, Okoye C, Bregy A, Lo SS, Ishkanian F, Komotar RJ (2015) The role of adjuvant radiotherapy after gross total resection of atypical meningiomas. World Neurosurg 83:808–815
Hess K, Spille DC, Adeli A, Sporns PB, Brokinkel C, Grauer O, Mawrin C, Stummer W, Paulus W, Brokinkel B (2018) Brain invasion and the risk of seizures in patients with meningioma. J Neurosurg. https://doi.org/10.3171/2017.11.JNS172265
Huang RY, Bi WL, Griffith B, Kaufmann TJ, la Fougere C, Schmidt NO, Tonn JC, Vogelbaum MA, Wen PY, Aldape K, Nassiri F, Zadeh G, Dunn IF, International Consortium on M (2019) Imaging and diagnostic advances for intracranial meningiomas. Neuro-Oncology 21:i44–i61
Jenkinson MD, Javadpour M, Haylock BJ, Young B, Gillard H, Vinten J, Bulbeck H, Das K, Farrell M, Looby S, Hickey H, Preusser M, Mallucci CL, Hughes D, Gamble C, Weber DC (2015) The ROAM/EORTC-1308 trial: radiation versus observation following surgical resection of atypical meningioma: study protocol for a randomised controlled trial. Trials 16:519
Katz LM, Hielscher T, Liechty B, Silverman J, Zagzag D, Sen R, Wu P, Golfinos JG, Reuss D, Neidert MC, Wirsching HG, Baumgarten P, Herold-Mende C, Wick W, Harter PN, Weller M, von Deimling A, Snuderl M, Sen C, Sahm F (2018) Loss of histone H3K27me3 identifies a subset of meningiomas with increased risk of recurrence. Acta Neuropathol 135:955–963
Kawahara Y, Nakada M, Hayashi Y, Kai Y, Hayashi Y, Uchiyama N, Nakamura H, Kuratsu J, Hamada J (2012) Prediction of high-grade meningioma by preoperative MRI assessment. J Neuro-Oncol 108:147–152
Klinger DR, Flores BC, Lewis JJ, Hatanpaa K, Choe K, Mickey B, Barnett S (2015) Atypical meningiomas: recurrence, reoperation, and radiotherapy. World Neurosurg 84:839–845
Li H, Zhang YS, Zhang GB, Zhang GJ, Wang B, Li D, Wu Z, Zhang JT (2019) Treatment protocol, long-term follow-up, and predictors of mortality in 302 cases of atypical meningioma. World Neurosurg 122:e1275–e1284
Li H, Zhao M, Jiao Y, Ge P, Li Z, Ma J, Wang S, Cao Y, Zhao J (2016) Prediction of high-grade pediatric meningiomas: magnetic resonance imaging features based on T1-weighted, T2-weighted, and contrast-enhanced T1-weighted images. World Neurosurg 91:89–95
Lin BJ, Chou KN, Kao HW, Lin C, Tsai WC, Feng SW, Lee MS, Hueng DY (2014) Correlation between magnetic resonance imaging grading and pathological grading in meningioma. J Neurosurg 121:1201–1208
Liu Y, Chotai S, Chen M, Jin S, Qi ST, Pan J (2015) Preoperative radiologic classification of convexity meningioma to predict the survival and aggressive meningioma behavior. PLoS One 10:e0118908
Masalha W, Heiland DH, Franco P, Delev D, Haaker JG, Schnell O, Scheiwe C, Grauvogel J (2018) Atypical meningioma: progression-free survival in 161 cases treated at our institution with surgery versus surgery and radiotherapy. J Neuro-Oncol 136:147–154
Nanda A, Bir SC, Konar S, Maiti T, Kalakoti P, Jacobsohn JA, Guthikonda B (2016) Outcome of resection of WHO grade II meningioma and correlation of pathological and radiological predictive factors for recurrence. J Clin Neurosci 31:112–121
Pereira BJA, de Almeida AN, Paiva WS, Teixeira MJ, Marie SKN (2018) Impact of radiotherapy in atypical meningioma recurrence: literature review. Neurosurg Rev. https://doi.org/10.1007/s10143-018-0959-8
Perry A, Louis DN, von Deimling A, Sahm F, Rushing EJ, Mawrin C, Claus EB, Loeffler J, Sadetzki S (2016) Meningiomas. In: Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Ellison DW, Figarella-Branger D, Perry A, Reifenberger G, von Deimlig A (eds) WHO classification of tumors of the central nervous system. International Agency on Cancer Research, Lyon, pp 232–245
Peyre M, Gauchotte G, Giry M, Froehlich S, Pallud J, Graillon T, Bielle F, Cazals-Hatem D, Varlet P, Figarella-Branger D, Loiseau H, Kalamarides M (2018) De novo and secondary anaplastic meningiomas: a study of clinical and histomolecular prognostic factors. Neuro-Oncology 20:1113–1121
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
Rogers L (2017) Observation or radiation therapy in treating patients with newly diagnosed grade II meningioma that has been completely removed by surgery (NCT03180268). https://clinicaltrials.gov/ct2/show/NCT03180268. Accessed 6 March 2019
Rogers L, Zhang P, Vogelbaum MA, Perry A, Ashby LS, Modi JM, Alleman AM, Galvin J, Brachman D, Jenrette JM, De Groot J, Bovi JA, Werner-Wasik M, Knisely JPS, Mehta MP (2018) Intermediate-risk meningioma: initial outcomes from NRG oncology RTOG 0539. J Neurosurg 129:35–47
Rydzewski NR, Lesniak MS, Chandler JP, Kalapurakal JA, Pollom E, Tate MC, Bloch O, Kruser T, Dalal P, Sachdev S (2018) Gross total resection and adjuvant radiotherapy most significant predictors of improved survival in patients with atypical meningioma. Cancer 124:734–742
Shakir SI, Souhami L, Petrecca K, Mansure JJ, Singh K, Panet-Raymond V, Shenouda G, Al-Odaini AA, Abdulkarim B, Guiot MC (2018) Prognostic factors for progression in atypical meningioma. J Neurosurg 129:1240–1248
Sicking J, Voss KM, Spille DC, Schipmann S, Holling M, Paulus W, Hess K, Steinbicker AU, Stummer W, Grauer O, Wolfer J, Brokinkel B (2018) The evolution of cranial meningioma surgery-a single-center 25-year experience. Acta Neurochir 160:1801–1812
Simpson D (1957) The recurrence of intracranial meningiomas after surgical treatment. J Neurol Neurosurg Psychiatry 20:22–39
Spille DC, Hess K, Sauerland C, Sanai N, Stummer W, Paulus W, Brokinkel B (2016) Brain invasion in meningiomas: incidence and correlations with clinical variables and prognosis. World Neurosurg 93:346–354
Sun SQ, Kim AH, Cai C, Murphy RK, DeWees T, Sylvester P, Dacey RG, Grubb RL, Rich KM, Zipfel GJ, Dowling JL, Leuthardt EC, Leonard JR, Evans J, Simpson JR, Robinson CG, Perrin RJ, Huang J, Chicoine MR (2014) Management of atypical cranial meningiomas, part 1: predictors of recurrence and the role of adjuvant radiation after gross total resection. Neurosurgery 75:347–354 discussion 354-345; quiz 355
Wang C, Kaprealian TB, Suh JH, Kubicky CD, Ciporen JN, Chen Y, Jaboin JJ (2017) Overall survival benefit associated with adjuvant radiotherapy in WHO grade II meningioma. Neuro-Oncology 19:1263–1270
Yoon H, Mehta MP, Perumal K, Helenowski IB, Chappell RJ, Akture E, Lin Y, Marymont MA, Sejpal S, Parsa A, Chandler JR, Bendok BR, Rosenow J, Salamat S, Kumthekar P, Raizer JK, Baskaya MK (2015) Atypical meningioma: randomized trials are required to resolve contradictory retrospective results regarding the role of adjuvant radiotherapy. J Cancer Res Ther 11:59–66
Zhi M, Girvigian MR, Miller MJ, Chen JC, Schumacher AJ, Rahimian J, Lodin K (2019) Long-term outcomes of newly diagnosed resected atypical meningiomas and the role of adjuvant radiotherapy. World Neurosurg 122:e1153–e1161
Funding
This research was funded by the “Codman Stipendium zur Förderung der kranialen Neurochirurgie” of the Deutsche Gesellschaft für Neurochirurgie.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Author BB received funding from the “Codman Stipendium zur Förderung der kranialen Neurochirurgie” of the Deutsche Gesellschaft für Neurochirurgie.” BB and all other authors declare that they have no conflicts of interest.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Data collection and scientific use were approved by the local ethics committee (Münster 2018-061-f-S).
Informed consent
Informed consent was obtained from all participants included in the study.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article is part of the Topical Collection on Tumor - Meningioma
Rights and permissions
About this article
Cite this article
Streckert, E.M.S., Hess, K., Sporns, P.B. et al. Clinical, radiological, and histopathological predictors for long-term prognosis after surgery for atypical meningiomas. Acta Neurochir 161, 1647–1656 (2019). https://doi.org/10.1007/s00701-019-03956-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00701-019-03956-8