J Neurol Surg B Skull Base
DOI: 10.1055/s-0044-1786370
Original Article

Recurrence of Resected Skull Base Meningiomas during Long-term Follow-up: Incidence and Predisposing Factors

1   Faculty of Biology, Medicine, and Health, University of Manchester, Manchester, United Kingdom
,
2   Department of Neurosurgery, Manchester Centre for Clinical Neurosciences, Manchester, United Kingdom
3   Geoffrey Jefferson Brain Research Centre, University of Manchester, Manchester, United Kingdom
,
Callum Howard
1   Faculty of Biology, Medicine, and Health, University of Manchester, Manchester, United Kingdom
,
Jane Halliday
2   Department of Neurosurgery, Manchester Centre for Clinical Neurosciences, Manchester, United Kingdom
,
Omar Nathan Pathmanaban
2   Department of Neurosurgery, Manchester Centre for Clinical Neurosciences, Manchester, United Kingdom
3   Geoffrey Jefferson Brain Research Centre, University of Manchester, Manchester, United Kingdom
,
Charlotte Hammerbeck-Ward
2   Department of Neurosurgery, Manchester Centre for Clinical Neurosciences, Manchester, United Kingdom
,
Scott A. Rutherford
2   Department of Neurosurgery, Manchester Centre for Clinical Neurosciences, Manchester, United Kingdom
,
Andrew T. King
2   Department of Neurosurgery, Manchester Centre for Clinical Neurosciences, Manchester, United Kingdom
3   Geoffrey Jefferson Brain Research Centre, University of Manchester, Manchester, United Kingdom
› Author Affiliations

Abstract

Introduction Skull base meningiomas (SBMs) are often subtotally resected and there is a paucity of evidence regarding the long-term rates of postoperative tumor progression. We aimed to investigate the factors that influence tumor recurrence in patients with an extended period of follow-up.

Methods Surgically resected tumors with long-term radiological follow-up were included for analysis. Data were collected on patient demographics, anatomical location, Simpson grade, World Health Organization (WHO) grade, modality of reintervention, and functional status. Recurrence was defined as tumor progression requiring intervention. Kaplan–Meier method and log-rank test were used to calculate recurrence-free probability. Cox regression analysis was used to determine factors associated with tumor progression.

Results Sixty-one patients were identified. Median radiological follow-up was 11.25 (IQR 4.3) years. Median age at first surgery was 50 (IQR 17) years. A total of 55/61(90%) tumors were WHO grade I and 6/61(10%) were grade II. Gross total resection (GTR) was achieved in 37/61 (60.7%) patients with subtotal resection (STR) in 24/61 (39.3%). In total, 28/61(45.9%) demonstrated recurrence/regrowth with a median time to recurrence of 2.8 (IQR 5) years. Also, 15/37 (40.5%) and 13/24 (54.2%) patients with GTR and STR, respectively, had tumor recurrence. Of the 28 recurrences, 4/28 (14.3%) underwent reresection, 9/28 (32.1%) were managed with radiotherapy, and 15/28 (53.6%) received both reresection and radiotherapy. Tumor grade was the only significant predictor of tumor recurrence (p = 0.033). Neurological function at last follow-up was significantly worse (modified Rankin scale >2) in patients with recurrence (p = 0.035).

Conclusion Surgically resected SBMs are associated with a significant recurrence rate during prolonged follow-up, irrespective of the extent of resection achieved. We recommend a prolonged period of radiological surveillance for SBM following surgical resection.



Publication History

Received: 20 November 2023

Accepted: 31 March 2024

Article published online:
30 April 2024

© 2024. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Ostrom QT, Cioffi G, Gittleman H. et al. CBTRUS Statistical Report: Primary brain and other central nervous system tumors diagnosed in the United States in 2012-2016. Neuro-oncol 2019; 21 (Suppl. 05) v1-v100
  • 2 Holleczek B, Zampella D, Urbschat S. et al. Incidence, mortality and outcome of meningiomas: a population-based study from Germany. Cancer Epidemiol 2019; 62: 101562
  • 3 Hashimoto N, Rabo CS, Okita Y. et al. Slower growth of skull base meningiomas compared with non-skull base meningiomas based on volumetric and biological studies. J Neurosurg 2012; 116 (03) 574-580
  • 4 Zeidman LA, Ankenbrandt WJ, Du H, Paleologos N, Vick NA. Growth rate of non-operated meningiomas. J Neurol 2008; 255 (06) 891-895
  • 5 Niiro M, Yatsushiro K, Nakamura K, Kawahara Y, Kuratsu J. Natural history of elderly patients with asymptomatic meningiomas. J Neurol Neurosurg Psychiatry 2000; 68 (01) 25-28
  • 6 Herscovici Z, Rappaport Z, Sulkes J, Danaila L, Rubin G. Natural history of conservatively treated meningiomas. Neurology 2004; 63 (06) 1133-1134
  • 7 Olivero WC, Lister JR, Elwood PW. The natural history and growth rate of asymptomatic meningiomas: a review of 60 patients. J Neurosurg 1995; 83 (02) 222-224
  • 8 Yao X, Wei T, Zhang H, Li J, Tang A, Ren K. The natural growth rate of skull base meningiomas compared with non-skull base meningiomas. J Craniofac Surg 2019; 30 (04) 1231-1233
  • 9 Harris FS, Rhoton AL. Anatomy of the cavernous sinus. A microsurgical study. J Neurosurg 1976; 45 (02) 169-180
  • 10 Najera E, Muhsen BA, Borghei-Razavi H, Adada B. Cavernous sinus meningioma resection through orbitozygomatic craniotomy. World Neurosurg 2021; 148: 205
  • 11 Zawy Alsofy S, Nakamura M, Suleiman A. et al. Cerebral anatomy detection and surgical planning in patients with anterior skull base meningiomas using a virtual reality technique. J Clin Med 2021; 10 (04) 681
  • 12 Bhat AR, Wani MA, Kirmani AR, Ramzan AU. Histological-subtypes and anatomical location correlated in meningeal brain tumors (meningiomas). J Neurosci Rural Pract 2014; 5 (03) 244-249
  • 13 Lemée JM, Corniola MV, Da Broi M. et al. Extent of resection in meningioma: predictive factors and clinical implications. Sci Rep 2019; 9 (01) 5944
  • 14 Zada G, Başkaya MK, Shah MV. Introduction: surgical management of skull base meningiomas. Neurosurg Focus 2017; 43 (VideoSuppl2): Intro
  • 15 Chen CM, Huang APH, Kuo LT, Tu YK. Contemporary surgical outcome for skull base meningiomas. Neurosurg Rev 2011; 34 (03) 281-296 , discussion 296
  • 16 Nanda A, Vannemreddy P. Recurrence and outcome in skull base meningiomas: do they differ from other intracranial meningiomas?. Skull Base 2008; 18 (04) 243-252
  • 17 Nanda A, Bir SC, Maiti TK, Konar SK, Missios S, Guthikonda B. Relevance of Simpson grading system and recurrence-free survival after surgery for World Health Organization Grade I meningioma. J Neurosurg 2017; 126 (01) 201-211
  • 18 Simpson D. The recurrence of intracranial meningiomas after surgical treatment. J Neurol Neurosurg Psychiatry 1957; 20 (01) 22-39
  • 19 Ius T, Tel A, Minniti G. et al. Advances in multidisciplinary management of skull base meningiomas. Cancers (Basel) 2021; 13 (11) 2664
  • 20 Klinger DR, Flores BC, Lewis JJ, Barnett SL. The treatment of cavernous sinus meningiomas: evolution of a modern approach. Neurosurg Focus 2013; 35 (06) E8
  • 21 Correa SFM, Marta GN, Teixeira MJ. Neurosymptomatic carvenous sinus meningioma: a 15-years experience with fractionated stereotactic radiotherapy and radiosurgery. Radiat Oncol 2014; 9 (01) 27
  • 22 Magill ST, Lee DS, Yen AJ. et al. Surgical outcomes after reoperation for recurrent skull base meningiomas. J Neurosurg 2018; 130 (03) 876-883
  • 23 Aghi MK, Carter BS, Cosgrove GR. et al. Long-term recurrence rates of atypical meningiomas after gross total resection with or without postoperative adjuvant radiation. Neurosurgery 2009; 64 (01) 56-60 , discussion 60
  • 24 İldan F, Erman T, Göçer AI. et al. Predicting the probability of meningioma recurrence in the preoperative and early postoperative period: a multivariate analysis in the midterm follow-up. Skull Base 2007; 17 (03) 157-171
  • 25 Banks JL, Marotta CA. Outcomes validity and reliability of the modified Rankin scale: implications for stroke clinical trials: a literature review and synthesis. Stroke 2007; 38 (03) 1091-1096
  • 26 Brokinkel B, Spille DC, Brokinkel C. et al. The Simpson grading: defining the optimal threshold for gross total resection in meningioma surgery. Neurosurg Rev 2021; 44 (03) 1713-1720
  • 27 Chotai S, Schwartz TH. The Simpson grading: is it still valid?. Cancers (Basel) 2022; 14 (08) 2007
  • 28 von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP. STROBE Initiative. Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. BMJ 2007; 335 (7624) 806-808
  • 29 Gousias K, Schramm J, Simon M. The Simpson grading revisited: aggressive surgery and its place in modern meningioma management. J Neurosurg 2016; 125 (03) 551-560
  • 30 Voß KM, Spille DC, Sauerland C. et al. The Simpson grading in meningioma surgery: does the tumor location influence the prognostic value?. J Neurooncol 2017; 133 (03) 641-651
  • 31 Spille DC, Hess K, Bormann E. et al. Risk of tumor recurrence in intracranial meningiomas: comparative analyses of the predictive value of the postoperative tumor volume and the Simpson classification. J Neurosurg 2020; 134 (06) 1764-1771
  • 32 Behling F, Fodi C, Hoffmann E. et al. The role of Simpson grading in meningiomas after integration of the updated WHO classification and adjuvant radiotherapy. Neurosurg Rev 2021; 44 (04) 2329-2336
  • 33 Goldbrunner R, Stavrinou P, Jenkinson MD. et al. EANO guideline on the diagnosis and management of meningiomas. Neuro-oncol 2021; 23 (11) 1821-1834
  • 34 Patel AJ, Wan YW, Al-Ouran R. et al. Molecular profiling predicts meningioma recurrence and reveals loss of DREAM complex repression in aggressive tumors. Proc Natl Acad Sci U S A 2019; 116 (43) 21715-21726
  • 35 Lee YS, Lee YS. Molecular characteristics of meningiomas. J Pathol Transl Med 2020; 54 (01) 45-63
  • 36 Proctor DT, Ramachandran S, Lama S, Sutherland GR. Towards molecular classification of meningioma: evolving treatment and diagnostic paradigms. World Neurosurg 2018; 119 (Nov): 366-373
  • 37 Maas SLN, Stichel D, Hielscher T. et al; German Consortium on Aggressive Meningiomas (KAM). Integrated molecular-morphologic meningioma classification: a multicenter retrospective analysis, retrospectively and prospectively validated. J Clin Oncol 2021; 39 (34) 3839-3852
  • 38 Nassiri F, Liu J, Patil V. et al. A clinically applicable integrative molecular classification of meningiomas. Nature 2021; 597 (7874): 119-125
  • 39 Sughrue ME, Kane AJ, Shangari G. et al. The relevance of Simpson Grade I and II resection in modern neurosurgical treatment of World Health Organization Grade I meningiomas. J Neurosurg 2010; 113 (05) 1029-1035
  • 40 Richardson GE, Gillespie CS, Mustafa MA. et al. Clinical outcomes following re-operations for intracranial meningioma. Cancers (Basel) 2021; 13 (19) 4792
  • 41 Bligh ER, Sinha P, Smith D, Al-Tamimi YZ. Thirty-day mortality and survival in elderly patients undergoing neurosurgery. World Neurosurg 2020; 133: e646-e652
  • 42 Faramand A, Kano H, Niranjan A, Park KJ, Flickinger JC, Lunsford LD. Tumor control and cranial nerve outcomes after adjuvant radiosurgery for low-grade skull base meningiomas. World Neurosurg 2019; 127 (Jul): e221-e229
  • 43 Debus J, Wuendrich M, Pirzkall A. et al. High efficacy of fractionated stereotactic radiotherapy of large base-of-skull meningiomas: long-term results. J Clin Oncol 2001; 19 (15) 3547-3553
  • 44 Nutting C, Brada M, Brazil L. et al. Radiotherapy in the treatment of benign meningioma of the skull base. J Neurosurg 1999; 90 (05) 823-827
  • 45 Goldsmith BJ, Wara WM, Wilson CB, Larson DA. Postoperative irradiation for subtotally resected meningiomas. A retrospective analysis of 140 patients treated from 1967 to 1990. J Neurosurg 1994; 80 (02) 195-201
  • 46 Barbaro NM, Gutin PH, Wilson CB, Sheline GE, Boldrey EB, Wara WM. Radiation therapy in the treatment of partially resected meningiomas. Neurosurgery 1987; 20 (04) 525-528
  • 47 Kaul D, Budach V, Misch M, Wiener E, Exner S, Badakhshi H. Meningioma of the skull base: long-term outcome after image-guided stereotactic radiotherapy. Cancer Radiother 2014; 18 (08) 730-735
  • 48 Mehdorn HM. Intracranial meningiomas: a 30-year experience and literature review. Adv Tech Stand Neurosurg 2016; 139-184
  • 49 Chen WC, Lucas CG, Magill ST, Rogers CL, Raleigh DR. Radiotherapy and radiosurgery for meningiomas. Neurooncol Adv 2023; 5 (Suppl. 01) i67-i83
  • 50 Maclean J, Fersht N, Short S. Controversies in radiotherapy for meningioma. Clin Oncol (R Coll Radiol) 2014; 26 (01) 51-64
  • 51 Rogers L, Zhang P, Vogelbaum MA. et al. Intermediate-risk meningioma: initial outcomes from NRG Oncology RTOG 0539. J Neurosurg 2018; 129 (01) 35-47
  • 52 Fischer GF, Brügge D, Andratschke N. et al. Postoperative radiotherapy for meningiomas – a decision-making analysis. BMC Cancer 2022; 22 (01) 492
  • 53 Mendenhall WM, Morris CG, Amdur RJ, Foote KD, Friedman WA. Radiotherapy alone or after subtotal resection for benign skull base meningiomas. Cancer 2003; 98 (07) 1473-1482
  • 54 Rogers CL, Won M, Vogelbaum MA. et al. High-risk meningioma: initial outcomes from NRG Oncology/RTOG 0539. Int J Radiat Oncol Biol Phys 2020; 106 (04) 790-799
  • 55 Jenkinson MD, Waqar M, Farah JO. et al. Early adjuvant radiotherapy in the treatment of atypical meningioma. J Clin Neurosci 2016; 28 (Jun): 87-92
  • 56 Louis DN, Perry A, Wesseling P. et al. The 2021 WHO Classification of Tumors of the Central Nervous System: a summary. Neuro-oncol 2021; 23 (08) 1231-1251
  • 57 Louis DN, Ohgaki H, Wiestler OD. et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007; 114 (02) 97-109
  • 58 Bulleid LS, James Z, Lammie A, Hayhurst C, Leach PA. The effect of the revised WHO classification on the incidence of grade II meningioma. Br J Neurosurg 2020; 34 (05) 584-586
  • 59 Rogers L, Gilbert M, Vogelbaum MA. Intracranial meningiomas of atypical (WHO grade II) histology. J Neurooncol 2010; 99 (03) 393-405
  • 60 Apra C, Peyre M, Kalamarides M. Current treatment options for meningioma. Expert Rev Neurother 2018; 18 (03) 241-249