Volume 8, Issue 1 (Continuous publishing 2022)                   Iran J Neurosurg 2022, 8(1): 0-0 | Back to browse issues page


XML Print


Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:

Sungkaro K, Sae-heng S. Metastasis of Malignant Intracranial Meningioma to the Lung: Report of a Case and Review of the Relevant Literature. Iran J Neurosurg 2022; 8 (1) : 9
URL: http://irjns.org/article-1-306-en.html
1- Department of Surgery, Faculty of Medicine, Prince of Songkla University, Songkhla, Thailand , kanisorn7640@gmail.com
2- Department of Surgery, Faculty of Medicine, Prince of Songkla University, Songkhla, Thailand
Full Text [PDF 1792 kb]   (344 Downloads)     |   Abstract (HTML)  (1225 Views)
Full Text:   (468 Views)
1. Background and Importance
Extracranial metastasis of meningioma has a low incidence rate [12]. A few cases have been reported in the literature. The pathophysiology of metastasis in meningioma is still being debated. The authors described a patient who suffered from multiple pulmonary metastases of meningioma. This case also highlights the malignant transformation of the World Health Organization (WHO) grade I meningioma.
2. Case Presentation
A 47-year-old female was admitted to a provincial hospital due to hemiparesis on the right side. Cranial Computed Tomography (CT) demonstrated a homogeneously enhanced tumor at the left temporal lobe measuring 5.7x5.0x4.0 centimeters (Figure 1A).

Consequently, the patient underwent an operation at the provincial hospital involving a left craniotomy with partial tumor removal, after which she was transferred to our hospital. At our hospital, she was still not fully conscious and had a motor weakness. The postoperative cranial CT revealed a residual tumor that was 5.0x4.1x3.5 centimeters in size. Therefore, the patient underwent a decompressive craniectomy with total tumor resection. After surgery, the patient gradually regained consciousness and improved motor weakness without any new neurological impairment. 
From the histological findings, tumor cells formed lobules where they appeared to form a syncytium with oval nuclei, occasionally showing central clearing (Figure 1B). A diagnosis of WHO grade I meningothelial meningioma was made. 
Two years after the second surgery, the patient suffered from progressive right hemiparesis again. Magnetic resonance imaging of the brain showed a recurrent homogeneously enhanced mass protruding through the craniectomy site, 6.2x7.0x5.5 centimeters in size (Figure 1C). The patient underwent a re-explored wound with subtotal tumor resection. Microscopic examination of this surgical specimen showed hypercellularity, small cells with a high nuclear to cytoplasmic ratio, and a sheeting pattern with mitosis 4/10 high-power field (Figure 1D), and tumor cells were immunoreactive for the Epithelial Membrane Antigen (EMA) (Figure 1E). In addition, brain invasion was observed from this specimen (Figure 1F). Therefore, the diagnosis was WHO grade II atypical meningioma, and postoperative radiotherapy was performed. 
One month after the third operation, she developed a cough during follow-up and her chest x-ray showed multiple lung masses (Figure 2A).

Therefore, she underwent a CT-guided biopsy of the right lung mass (Figure 2B). Histopathology of the biopsy specimens showed a sheeting pattern, hypercellularity with small cells, and a high nuclear to cytoplasmic ratio (Figure 2C). Moreover, a tumor showed immunoreaction for EMA that was in concordance with an intracranial tumor (Figure 2D). Finally, pulmonary metastatic meningioma was diagnosed, and the patient refused further treatment. However, she has since received a follow-up and was still able to manage daily activities from the time of the previous follow-up.
3. Discussion
Extracranial metastasis of meningioma is an uncommon presentation. The incidence of meningioma metastasis was reported to be 0.18-0.67% [12]. Common metastatic sites include the lungs and intra-abdominal organs. According to Stoller et al. [3], the proportion of extracranial metastasis to lung/pleura, musculoskeletal system, liver, lymph node, and kidney was reported at 35%, 17%, 13%, 11%, and 8%, respectively. Moreover, EMA is one of the biomarkers used for the diagnosis of meningioma and 80% of this biomarker is positive in meningioma [4]. In the present case, EMA was expressed in both intracranial and lung lesions that confirmed metastasis of meningioma. 
We reviewed cases of intracranial meningioma with pulmonary metastasis from the literature. The characteristics of the patients, intracranial meningioma, and pulmonary metastases are summarized in Table 1 [5, 6, 7, 8, 9, 10, 11, 12, 13, 141516171819].


This rare scenario is more frequently observed in the fifth-to-seventh decades of life, and tumors are usually located in the parasagittal region. Histological diagnosis of intracranial meningioma was equally observed for both benign and malignant tumors after the first surgery. The disease relapses in most cases; however, malignant transformation is an uncommon presentation. The present case had recurrent disease with malignant transformation and distant metastasis, which is in concordance with other prior reports [10, 11, 15]. Additionally, the majority of pulmonary metastasis cases involve multiple bilateral metastases. 
The pathogenesis for distant metastasis of meningioma has been inconclusive. Frydrychowicz et al. reported two patients with atypical meningioma and pulmonary metastasis with a deletion of chromosomes 1p and 22 by cytogenetic analysis [14]. In the era of translational medicine, various biomarkers have been studied in genetic alteration for an explanation [20, 21]. The C-X-C chemokine receptor type 4/C-X-C motif chemokine ligand 12 (CXCR4/CXCL12) axis has been discussed for the metastasis ability of malignant tumor cells [20, 22]. Zagzag et al. [22] studied the CXCR4/CXCL12 axis that involved migration and metastasis of glial cell tumors. In addition, no association is reported among NF2, CDKN2A, BAP1, ARID1A, and TP53 mutations between disseminated and non-disseminated meningiomas [23]. 
Higher grade, more frequent metastasis has been found in the literature review. The incidence of extracranial metastatic meningioma grade I ranged from 3.6-29.3%, grade II ranged from 6.8-57.1%, and grade III ranged from 39.3-63.9% according to prior studies [12]. The present case was initially diagnosed with meningothelial meningioma, WHO grade I with malignant transformation to atypical meningioma. Finally, extracranial metastasis developed into multiple pulmonary metastases. 
Nakasu et al. [24] conducted a systematic review and meta-analysis of malignant transformation in benign meningioma and found that the incidence rate of malignant transformation of meningioma was 2.98/1000 patient-years (95% confidence interval 1.9–4.3) and non-skull-based meningioma had a higher proportion of this event than skull-based meningioma. However, the molecular mechanism of malignant transformation has remained under investigation. 
Shao et al. [25] reviewed the pathogenesis for malignancy development of meningioma, which is closely related to the chromosomal variations and abnormal molecular signals involved, as follows: chromosomal loss of 1p, 6q, 10, 14q, and 18q and gains at 1q, 9q, 12q, 15q, 17q, and 20q. Meanwhile, Tunthanathip et al. investigated the whole-genome sequencing of five patients with low-grade glioma who developed malignant transformation and proposed the hypothesis that alterations of various genes, such as IDH 1, KMT2C, and GGT1 may be involved in the processes of malignant transformation of glioma [20, 26, 27]. 
Because distant metastasis of this tumor is rare, there is no standard treatment for metastatic meningioma; chemotherapy is the only alternative treatment. The prognosis for patients with metastasis is poor; a previous study reported that patients with metastatic meningioma were significantly associated with a poor prognosis compared to patients without metastasis [2]. Moreover, the median survival time for patients with metastasis was 35 months (Interquartile Range [IQR] 8–69), while patients without metastasis had a median survival time of 50 months (IQR, 25–84) [2].
4. Conclusion
In summary, we presented a case of pulmonary metastatic meningioma that developed malignant transformation before distant metastasis. Further study of the genetic alteration should be conducted in the future for the pathogenesis of both malignant transformation and extracranial metastasis. 

Ethical Considerations
Compliance with ethical guidelines

Informed consent was obtained from the patient for publication. 

Funding
This research did not receive any grant from funding agencies in the public, commercial, or non-profit sectors.

Authors' contributions
Conceptualization and design: Kanisorn Sungkaro, Sakchai Sae-heng; Data collection: Kanisorn Sungkaro; Data analysis and interpretation: Kanisorn Sungkaro, Sakchai Sae-heng; Drafting the article: Kanisorn Sungkaro; Critically revising the article: Kanisorn Sungkaro, Sakchai Sae-heng; Reviewing submitted version of manuscript: Kanisorn Sungkaro, Sakchai Sae-heng; Approving the final version of the manuscript: Kanisorn Sungkaro, Sakchai Sae-heng.

Conflict of interest
The authors declared no conflict of interest.


References
  1. Dalle Ore CL, Magill ST, Yen AJ, Sahhin MN, Lee DS, Lucas CG, et al. Meningioma metastases: Incidence and proposed screening paradigm. Journal of Neurosurgery. 2019; 132(5):1447-55. [DOI:10.3171/2019.1.JNS181771] [PMID]
  2. Vuong HG, Ngo TNM, Dunn IF. Incidence, risk factors, and prognosis of meningiomas with distant metastases at presentation. Neurooncology Advances. 2021; 3(1):vdab084. [DOI:10.1093/noajnl/vdab084] [PMID] [PMCID]
  3. Stoller JK, Kavuru M, Mehta AC, Weinstein CE, Estes ML, Gephardt GN. Intracranial meningioma metastatic to the lung. Cleveland Clinic Journal of Medicine. 1987; 54(6):521-7. [DOI:10.3949/ccjm.54.6.521] [PMID]
  4. Ayoubi S, Dunn IF, Al-Mefty O. Meningiomas. In: Kaye AH, Laws ER, editors. Brain tumors: An Encyclopedic Approach. Amsterdam: Saunder/Elsevier; 2011. [DOI:10.1016/B978-0-443-06967-3.00031-4]
  5. Hishima T, Fukayama M, Funata N, Mochizuki M, Hayashi Y, Koike M, et al. Intracranial meningioma masquerading as a primary pleuropulmonary tumor. Pathology International. 1995; 45(8):617-21. [DOI:10.1111/j.1440-1827.1995.tb03512.x] [PMID]
  6. Murrah CP, Ferguson ER, Jennelle RL, Guthrie BL, Holman WL. Resection of multiple pulmonary metastases from a recurrent intracranial meningioma. The Annals of Thoracic Surgery. 1996; 61(6):1823-4. [DOI:10.1016/0003-4975(96)00064-1] [PMID]
  7. Adlakha A, Rao K, Adlakha H, Perry A, Crotty TB, Scheithauer BW, et al. Meningioma metastatic to the lung. Mayo Clinic Proceedings. 1999; 74(11):1129-33). [DOI:10.4065/74.11.1129] [PMID]
  8. Figueroa BE, Quint DJ, McKeever PE, Chandler WF. Extracranial metastatic meningioma. The British Journal of Radiology. 1999; 72(857):513-6. [DOI:10.1259/bjr.72.857.10505022] [PMID]
  9. Teague SD, Conces DJ Jr. Metastatic meningioma to the lungs. Journal of Thoracic Imaging. 2005; 20(1):58-60. [DOI:10.1097/01.rti.0000139388.80395.6e] [PMID]
  10. D’Aiuto M, Veronesi G, Pelosi G, Presicci PF, Ferraroli GM, Gasparri R, et al. Two-year survival after multiple bilateral lung metastasectomies for cranial meningioma. The Annals of Thoracic Surgery. 2005; 80(3):1129-30. [DOI:10.1016/j.athoracsur.2004.02.146] [PMID]
  11. Erman T, Hanta I, Haciyakupoğlu S, Zorludemir S, Zeren H, Göçer AI. Huge bilateral pulmonary and pleural metastasis from intracranial meningioma: A case report and review of the literature. Journal of Neuro-Oncology. 2005; 74(2):179-81. [DOI:10.1007/s11060-004-3014-2] [PMID]
  12. Fabi A, Nuzzo C, Vidiri A, Ciccarese M, Felici A, Cattani F, Cognetti F. Bone and lung metastases from intracranial meningioma. Anticancer Research. 2006; 26(5B):3835-7. [PMID]
  13. Psaras T, Pantazis G, Steger V, Meyermann R, Honegger J, Beschorner R. Benign meningioma developing late lung metastases: Case report and review of the literature. Clinical Neuropathology. 2009; 28:453-9. [DOI:10.5414/NPP28453] [PMID]
  14. Frydrychowicz C, Holland H, Hantmann H, Gradistanac T, Hoffmann KT, Mueller W, et al. Two cases of atypical meningioma with pulmonary metastases: A comparative cytogenetic analysis of chromosomes 1p and 22 and a review of the literature. Neuropathology. 2015; 35(2):175-83. [DOI:10.1111/neup.12177] [PMID]
  15. Mutnuru PC, Ahmed SF, Uppin SG, Lachi PK. Pulmonary metastases from intracranial meningioma. Lung India. 2015; 32(6):661-3. [DOI:10.4103/0970-2113.168120] [PMID] [PMCID]
  16. Wang M, Zhan R, Zhang C, Zhou Y. Multiple pulmonary metastases in recurrent intracranial meningioma: Case report and literature review. Journal of International Medical Research. 2016; 44(3):742-52. [DOI:10.1177/0300060515618053] [PMID] [PMCID]
  17. Honda Y, Shirayama R, Morita H, Kusuhara K. Pulmonary and pleural metastasis of intracranial anaplastic meningioma in a 3-year-old boy: A case report. Molecular and Clinical Oncology. 2017; 7(4):633-6. [DOI:10.3892/mco.2017.1375] [PMID] [PMCID]
  18. Enomoto T, Aoki M, Kouzaki Y, Abe H, Imamura N, Iwasaki A, et al. WHO grade I meningioma metastasis to the lung 26 years after initial surgery: A case report and literature review. NMC Case Report Journal. 2019:cr-2019. [DOI:10.2176/nmccrj.cr.2019-0020] [PMID] [PMCID]
  19. Utsumi T, Saito T, Ishida M, Maru N, Matsui H, Taniguchi Y, et al. Solitary pulmonary metastasis after meningioma surgery of the head: A case report. Surgical Case Reports. 2022; 8(1):26. [DOI:10.1186/s40792-022-01379-9] [PMID] [PMCID]
  20. Tunthanathip T. Role of Biomarkers in brain tumor. In: Tunthanathip T, editor. Translational Medicine in Neurosurgery. Bangkok: Sahamit Pattana printing; 2022.
  21. Tunthanathip T, Duangsuwan J, Wattanakitrungroj N, Tongman S, Phuenpathom N. Comparison of intracranial injury predictability between machine learning algorithms and the nomogram in pediatric traumatic brain injury. Neurosurgery Focus. 2021; 51(5):E7. [DOI:10.3171/2021.8.FOCUS2155] [PMID]
  22. Zagzag D, Lukyanov Y, Lan L, Ali MA, Esencay M, Mendez O, et al. Hypoxia-inducible factor 1 and VEGF upregulate CXCR4 in glioblastoma: Implications for angiogenesis and glioma cell invasion. Laboratory Investigation. 2006; 86:1221-32. [DOI:10.1038/labinvest.3700482] [PMID]
  23. Williams EA, Santagata S, Wakimoto H, Shankar GM, Barker FG, Sharaf R, et al. Distinct genomic subclasses of high-grade/progressive meningiomas: NF2-associated, NF2-exclusive, and NF2-agnostic. Acta Neuropathologica Communications. 2020; 8(1):1-0. [DOI:10.1186/s40478-020-01040-2] [PMID] [PMCID]
  24. Nakasu S, Notsu A, Na K, Nakasu Y. Malignant transformation of WHO grade I meningioma after surgery or radiosurgery: Systematic review and meta-analysis of observational studies. Neurooncology Advances. 2020; 2(1):vdaa129 [DOI:10.1093/noajnl/vdaa129] [PMID] [PMCID]
  25. Shao Z, Liu L, Zheng Y, Tu S, Pan Y, Yan S, et al. Molecular mechanism and approach in progression of meningioma. Frontiers in Oncology. 2020; 10:538845. [DOI:10.3389/fonc.2020.538845] [PMID] [PMCID]
  26. Tunthanathip T, Ratanalert S, Sae-Heng S, Oearsakul T, Sakarunchai I, Kaewborisutsakul A, et al. Prognostic factors and clinical nomogram predicting survival in high-grade glioma. Journal of Cancer Research and Therapeutics. 2021; 17(4):1052. [DOI:10.4103/jcrt.JCRT_233_19] [PMID]
  27. Tunthanathip T, Sangkhathat S. Temozolomide for patients with wild-type isocitrate dehydrogenase (IDH) 1 glioblastoma using propensity score matching. Clinical Neurology and Neurosurgery. 2020; 191:105712. [DOI:10.1016/j.clineuro.2020.105712] [PMID]
Type of Study: Case report | Subject: Brain Tumors

Add your comments about this article : Your username or Email:
CAPTCHA

Send email to the article author


Rights and Permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

© 2024 CC BY-NC 4.0 | Iranian Journal of Neurosurgery

Designed & Developed by: Yektaweb