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A systematic review of extraneural meningioma metastasis: timing, evolution and outlook

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Abstract

Purpose

Extraneural meningioma metastasis is a rare occurrence and may pose a clinical challenge due to its unclear prognosis. In this systematic review, we analyze patient demographics, clinical characteristics, management strategies, and outcomes.

Methods

PubMed, EMBASE, Scopus, Cochrane, and Web of Science databases were searched from inception to February 23, 2024 for cases of metastatic meningioma according to PRISMA guidelines. Descriptive statistics, Mann–Whitney U test, Fisher's exact tests, Kaplan–Meier curves, and log-rank tests were used for selected analyses.

Results

A total of 288 patients (52% male) were included with an average age of 49 years at meningioma diagnosis. Tumors were distributed across WHO grade 1 (38%), 2 (36%), and 3 (26%). Most patients experienced intracranial recurrence (79%) and mean time to first metastasis was approximately 8 years. No change in WHO grade between primary and metastasis was observed for most cases (65%). Treatment of the initial metastasis was most often with surgery (43%), chemotherapy (20%), or no treatment (14%). Half of the patients were alive (50%) with an average follow-up of 3 years following metastasis. Overall median survival was 36 months for the entire cohort. This differed significantly between WHO grade 1 versus 2/3 meningioma primaries (168 vs. 15 months, p < 0.005).

Conclusion

Metastatic meningioma appears to be associated with more positive prognosis than other brain tumor types with extra-neural metastasis or metastasis in general. This is particularly true for cases arising from a WHO grade 1 meningioma.

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Data availability

No datasets were generated or analysed during the current study.

References

  1. AtherEnam S, Abdulrauf S, Mehta B et al (1996) Metastasis in meningioma. Acta Neurochir 138:1172–1178. https://doi.org/10.1007/BF01809747

    Article  Google Scholar 

  2. Adlakha A, Rao K, Adlakha H et al (1999) Meningioma metastatic to the lung. Mayo Clin Proc 74:1129–1133. https://doi.org/10.4065/74.11.1129

    Article  CAS  PubMed  Google Scholar 

  3. Ore CLD, Magill ST, Yen AJ et al (2019) Meningioma metastases: incidence and proposed screening paradigm. J Neurosurg 132:1447–1455. https://doi.org/10.3171/2019.1.JNS181771

    Article  Google Scholar 

  4. Forest F, Berremila S-A, Gyenes C et al (2014) Metastatic meningiomas: an unusual clinical and pathological diagnosis with highly variable outcome. J Neurooncol 120:411–421. https://doi.org/10.1007/s11060-014-1567-2

    Article  PubMed  Google Scholar 

  5. Rawat B, Franchetto AA, Elavathil J (1995) Extracranial metastases of meningioma. Neuroradiology 37:38–41. https://doi.org/10.1007/BF00588517

    Article  CAS  PubMed  Google Scholar 

  6. Glasauer FE, Yuan RHP (1963) Intracranial tumors with extracranial metastases: case report and review of the literature. J Neurosurg 20:474–493. https://doi.org/10.3171/jns.1963.20.6.0474

    Article  CAS  PubMed  Google Scholar 

  7. Page MJ, McKenzie JE, Bossuyt PM et al (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 372:n71. https://doi.org/10.1136/bmj.n71

    Article  PubMed  PubMed Central  Google Scholar 

  8. Howick J, Chalmers I, Glasziou P, Greenhalgh T, Heneghan C, Liberati A, Moschetti I, Phillips B, and Thornton H (2011) Explanation of the 2011 Oxford Centre for Evidence-Based Medicine (OCEBM) Levels of Evidence (Background Document). Oxford Centre for Evidence-Based Medicine. https://www.cebm.ox.ac.uk/resources/levels-of-evidence/explanation-of-the-2011-ocebm-levels-of-evidence/. Accessed 30 Nov 2022

  9. Critical Appraisal Tools | JBI. https://jbi.global/critical-appraisal-tools. Accessed 30 Nov 2022

  10. Mastorakos P, McGavern D (2019) The anatomy and immunology of vasculature in the central nervous system. Sci Immunol 4:eaav0492. https://doi.org/10.1126/sciimmunol.aav0492

  11. Hosainey SAM, Bouget D, Reinertsen I et al (2022) Are there predilection sites for intracranial meningioma? A population-based atlas. Neurosurg Rev 45:1543–1552. https://doi.org/10.1007/s10143-021-01652-9

    Article  PubMed  Google Scholar 

  12. Oya S, Kim S-H, Sade B, Lee JH (2011) The natural history of intracranial meningiomas: clinical article. J Neurosurg 114:1250–1256. https://doi.org/10.3171/2010.12.JNS101623

    Article  PubMed  Google Scholar 

  13. Aspelund A, Antila S, Proulx ST et al (2015) A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules. J Exp Med 212:991–999. https://doi.org/10.1084/jem.20142290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Ahn JH, Cho H, Kim J-H et al (2019) Meningeal lymphatic vessels at the skull base drain cerebrospinal fluid. Nature 572:62–66. https://doi.org/10.1038/s41586-019-1419-5

    Article  CAS  PubMed  Google Scholar 

  15. Louveau A, Smirnov I, Keyes TJ et al (2015) Structural and functional features of central nervous system lymphatic vessels. Nature 523:337–341. https://doi.org/10.1038/nature14432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Franzen A, Buchali A, Lieder A (2017) The rising incidence of parotid metastases: our experience from four decades of parotid gland surgery. Acta Otorhinolaryngol Ital 37:264–269. https://doi.org/10.14639/0392-100X-1095

  17. Riihimäki M, Thomsen H, Sundquist K et al (2018) Clinical landscape of cancer metastases. Cancer Med 7:5534–5542. https://doi.org/10.1002/cam4.1697

    Article  PubMed  PubMed Central  Google Scholar 

  18. (2012) Slower growth of skull base meningiomas compared with non–skull base meningiomas based on volumetric and biological studies. J Neurosurg 116(3). Journals. https://thejns.org/view/journals/j-neurosurg/116/3/article-p574.xml. Accessed 24 Jan 2024

  19. Budczies J, von Winterfeld M, Klauschen F et al (2014) The landscape of metastatic progression patterns across major human cancers. Oncotarget 6:570–583

    Article  PubMed Central  Google Scholar 

  20. Louis DN, Perry A, Wesseling P et al (2021) The 2021 WHO classification of tumors of the central nervous system: a summary. Neuro Oncol 23:1231–1251. https://doi.org/10.1093/neuonc/noab106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Ostrom QT, Price M, Neff C et al (2023) CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2016–2020. Neuro Oncol 25:iv1–iv99. https://doi.org/10.1093/neuonc/noad149

  22. Holleczek B, Zampella D, Urbschat S et al (2019) Incidence, mortality and outcome of meningiomas: a population-based study from Germany. Cancer Epidemiol 62:101562. https://doi.org/10.1016/j.canep.2019.07.001

    Article  PubMed  Google Scholar 

  23. Magill ST, Vasudevan HN, Seo K et al (2020) Multiplatform genomic profiling and magnetic resonance imaging identify mechanisms underlying intratumor heterogeneity in meningioma. Nat Commun 11:4803. https://doi.org/10.1038/s41467-020-18582-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Kodama K, Doi O, Higashiyama M et al (1991) Primary and metastatic pulmonary meningioma. Cancer 67:1412–1417. https://doi.org/10.1002/1097-0142(19910301)67:5%3c1412::AID-CNCR2820670523%3e3.0.CO;2-V

    Article  CAS  PubMed  Google Scholar 

  25. Fan H, Song L, Fan J et al (2023) Decoding meningioma heterogeneity and neoplastic cell—macrophage interaction through single-cell transcriptome profiling across pathological grades. J Transl Med 21:751. https://doi.org/10.1186/s12967-023-04445-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Yamasaki F, Yoshioka H, Hama S et al (2000) Recurrence of meningiomas. Cancer 89:1102–1110. https://doi.org/10.1002/1097-0142(20000901)89:5%3c1102::AID-CNCR20%3e3.0.CO;2-L

    Article  CAS  PubMed  Google Scholar 

  27. Mirimanoff RO, Dosoretz DE, Linggood RM et al (1985) Meningioma: analysis of recurrence and progression following neurosurgical resection. J Neurosurg 62:18–24. https://doi.org/10.3171/jns.1985.62.1.0018

    Article  CAS  PubMed  Google Scholar 

  28. Taylor BW, Marcus RB, Friedman WA et al (1988) The meningioma controversy: postoperative radiation therapy. Int J Radiat Oncol Biol Phys 15:299–304. https://doi.org/10.1016/s0360-3016(98)90008-6

    Article  PubMed  Google Scholar 

  29. Condra KS, Buatti JM, Mendenhall WM et al (1997) Benign meningiomas: primary treatment selection affects survival. Int J Radiat Oncol Biol Phys 39:427–436. https://doi.org/10.1016/s0360-3016(97)00317-9

    Article  CAS  PubMed  Google Scholar 

  30. Stafford SL, Perry A, Suman VJ et al (1998) Primarily resected meningiomas: outcome and prognostic factors in 581 Mayo Clinic patients, 1978 through 1988. Mayo Clin Proc 73:936–942. https://doi.org/10.4065/73.10.936

    Article  CAS  PubMed  Google Scholar 

  31. Soyuer S, Chang EL, Selek U et al (2004) Radiotherapy after surgery for benign cerebral meningioma. Radiother Oncol 71:85–90. https://doi.org/10.1016/j.radonc.2004.01.006

    Article  PubMed  Google Scholar 

  32. Lam Shin Cheung V, Kim A, Sahgal A, Das S (2018) Meningioma recurrence rates following treatment: a systematic analysis. J Neurooncol 136:351–361. https://doi.org/10.1007/s11060-017-2659-6

    Article  PubMed  Google Scholar 

  33. Ayerbe J, Lobato RD, de la Cruz J et al (1999) Risk Factors Predicting Recurrence in Patients Operated on for Intracranial Meningioma. A Multivariate Analysis. Acta Neurochir (Wien) 141:921–932. https://doi.org/10.1007/s007010050398

    Article  CAS  PubMed  Google Scholar 

  34. Smoll NR, Villanueva EV (2010) The epidemiology of extraneural metastases from primary brain, spinal cord, and meningeal tumors. Neurosurgery 67:E1470. https://doi.org/10.1227/NEU.0b013e3181f3d3dd

    Article  PubMed  Google Scholar 

  35. Palmisciano P, Ferini G, Barone F et al (2022) Extra-neural metastases from primary intracranial ependymomas: a systematic review. Front Oncol 12

  36. Noch EK, Sait SF, Farooq S et al (2021) A case series of extraneural metastatic glioblastoma at Memorial Sloan Kettering Cancer Center. Neurooncol Pract 8:325–336. https://doi.org/10.1093/nop/npaa083

    Article  PubMed  PubMed Central  Google Scholar 

  37. Nakayama Y, Horio H, Horiguchi S, Hato T (2014) Pulmonary and pleural metastases from benign meningeal meningioma: a case report. Ann Thorac Cardiovasc Surg 20:410–413. https://doi.org/10.5761/atcs.cr.11.01852

    Article  PubMed  Google Scholar 

  38. Mishkin B, Raizer JJ, Bell JB (2018) Widespread disseminated osseous metastases of intracranial meningioma with over 27-year-survivorship: a unique, idiosyncratic case. J Neurooncol 139:781–783. https://doi.org/10.1007/s11060-018-2926-1

    Article  PubMed  Google Scholar 

  39. Attuati L, Zaed I, Morselli C et al (2019) Multimodal management of metastatic malignant meningiomas: the role of radiosurgery in long-term local control. World Neurosurg 128:562–572. https://doi.org/10.1016/j.wneu.2019.05.058

    Article  PubMed  Google Scholar 

  40. Dincer A, Chow W, Shah R, Graham RS (2020) Infiltration of benign meningioma into sagittal sinus and subsequent metastasis to lung: case report and literature review. World Neurosurg 136:263–269. https://doi.org/10.1016/j.wneu.2019.12.131

    Article  PubMed  Google Scholar 

  41. Enomoto T, Aoki M, Kouzaki Y et al (2019) WHO grade I meningioma metastasis to the lung 26 years after initial surgery: a case report and literature review. NMC Case Rep J 6:125–129. https://doi.org/10.2176/nmccrj.cr.2019-0020

    Article  PubMed  PubMed Central  Google Scholar 

  42. Surov A, Gottschling S, Bolz J et al (2013) Distant metastases in meningioma: an underestimated problem. J Neurooncol 112:323–327. https://doi.org/10.1007/s11060-013-1074-x

    Article  PubMed  Google Scholar 

  43. Montgomery E, Sundarrajan C, Pernik M et al (2023) Metastatic meningioma: a systematic review of incidence and risk factors. Interdiscip Neurosurg 32:101720. https://doi.org/10.1016/j.inat.2023.101720

    Article  Google Scholar 

  44. Weiss L (1955) A metastasizing ependymoma of the cauda equina. Cancer 8:161–171. https://doi.org/10.1002/1097-0142(1955)8:1%3c161::AID-CNCR2820080123%3e3.0.CO;2-K

    Article  CAS  PubMed  Google Scholar 

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Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript. The authors also have no relevant financial or non-financial interests to disclose. All authors contributed meaningful to this manuscript as follows: Gina Watanabe: Methodology, Data curation, Validation, Writing (Original); Kurtis Young: Data curation, Validation; Erin Rauber: Data curation, Investigation; Mohammad Khan: Data curation, Investigation; Reannon Suzuki: Validation, Investigation; Robert Riestenberg: Validation, Writing (Review); Giuseppe Umana: Conceptualization, Writing (Review); Paolo Palmisciano: Conceptualization, Methodology, Writing (Review).

Author information

Authors and Affiliations

  1. John A. Burns School of Medicine, University of Hawaii at Manoa, 5080 Likini St #417, Honolulu, HI, 96818, USA

    Gina Watanabe & Reannon Suzuki

  2. Department of Otolaryngology, University of Nevada, Las Vegas, NV, USA

    Kurtis Young

  3. School of Medicine, University of Kansas, Kansas City, KS, USA

    Erin Rauber

  4. University of Indiana School of Medicine, Indianapolis, IN, USA

    Mohammad Faizan Khan

  5. Department of Neurological Surgery, University of California Davis, Sacramento, CA, USA

    Robert Riestenberg & Paolo Palmisciano

  6. Department of Neurosurgery, Trauma Center, Gamma Knife Center, Cannizzaro Hospital, Catania, Italy

    Giuseppe E. Umana

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  1. Gina Watanabe
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Contributions

All authors contributed meaningfully to this manuscript as follows: G.W.: Methodology, Data curation, Validation, Writing (Original); K.Y.: Data curation, Validation; E.R.: Data curation, Investigation; M.F.K.: Data curation, Investigation; R.S.: Validation, Investigation; R.R.: Validation, Writing (Review); G.E.U.: Conceptualization, Writing (Review); P.P.: Conceptualization, Methodology, Writing (Review).

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Correspondence to Gina Watanabe.

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Watanabe, G., Young, K., Rauber, E. et al. A systematic review of extraneural meningioma metastasis: timing, evolution and outlook. J Neurooncol (2024). https://doi.org/10.1007/s11060-024-04659-6

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