Journal of Korean Neurosurgical Society

  • 제65권2호
  • /
  • Pages.297-306
  • /
  • 2022
  • /
  • 2005-3711(pISSN)
  • /
  • 1598-7876(eISSN)
대한신경외과학회 (The Korean Neurosurgical Society)
권호 표지
DOI QR코드

DOI QR Code

Clinical Implications of the Mitotic Index as a Predictive Factor for Malignant Transformation of Atypical Meningiomas

  • Kwon, Sae Min (Department of Neurosurgery, Dongsan Medical Center, Keimyung University School of Medicine) ;
  • Kim, Jeong Hoon (Department of Neurological Surgery, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Kim, Young-Hoon (Department of Neurological Surgery, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Hong, Seok Ho (Department of Neurological Surgery, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Cho, Young Hyun (Department of Neurological Surgery, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Kim, Chang Jin (Department of Neurological Surgery, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Nam, Soo Jeong (Department of Pathology, Asan Medical Center, University of Ulsan College of Medicine)
  • 투고 : 2021.05.10
  • 심사 : 2021.08.23
  • 발행 : 2022.03.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Objective : Intracranial atypical meningiomas have a poor prognosis and high rates of recurrence. Moreover, up to one-third of the recurrences undergo high-grade transformation into malignant meningiomas. We aimed to investigate the clinical factors that can predict the propensity of malignant transformation from atypical to anaplastic meningiomas. Methods : Between 2001 and 2018, all patients with atypical meningioma, in whom the tumors had undergone malignant transformation to anaplastic meningioma, were included. The patients' medical records documenting the diagnosis of atypical meningioma prior to malignant transformation were reviewed to identify the predictors of transformation. The control group comprised 56 patients with atypical meningiomas who were first diagnosed between January 2017 and December 2018 and had no malignant transformation. Results : Nine patients in whom the atypical meningiomas underwent malignant transformation were included. The median time interval from diagnosis of atypical meningioma to malignant transformation was 19 months (range, 7-78). The study group showed a significant difference in heterogeneous enhancement (77.8% vs. 33.9%), bone invasion (55.6% vs. 12.5%), mitotic index (MI; 14.8±4.9 vs. 3.5±3.9), and Ki-67 index (20.7±13.9 vs. 9.5±7.1) compared with the control group. In multivariate analysis, increased MI (odds ratio, 1.436; 95% confidence interval, 1.127-1.900; p=0.004) was the only significant factor for predicting malignant transformation. Conclusion : An increased MI within atypical meningiomas might be used as a predictor of malignant transformation. Tumors at high risk for malignant transformation might require more attentive surveillance and management than other atypical meningiomas.

키워드

과제정보

This research was supported by the Bisa Research Grant of Keimyung University in 2019.

참고문헌

  1. Adegbite AB, Khan MI, Paine KW, Tan LK : The recurrence of intracranial meningiomas after surgical treatment. J Neurosurg 58 : 51-56, 1983 https://doi.org/10.3171/jns.1983.58.1.0051
  2. Aghi MK, Carter BS, Cosgrove GR, Ojemann RG, Amin-Hanjani S, Martuza RL, et al. : Long-term recurrence rates of atypical meningiomas after gross total resection with or without postoperative adjuvant radiation. Neurosurgery 64 : 56-60; discussion 60, 2009 https://doi.org/10.1227/01.NEU.0000330399.55586.63
  3. Aizer AA, Bi WL, Kandola MS, Lee EQ, Nayak L, Rinne ML, et al. : Extent of resection and overall survival for patients with atypical and malignant meningioma. Cancer 121 : 4376-4381, 2015 https://doi.org/10.1002/cncr.29639
  4. Al-Mefty O, Kadri PA, Pravdenkova S, Sawyer JR, Stangeby C, Husain M : Malignant progression in meningioma: documentation of a series and analysis of cytogenetic findings. J Neurosurg 101 : 210-218, 2004 https://doi.org/10.3171/jns.2004.101.2.021
  5. Alvarez F, Roda JM, Perez Romero M, Morales C, Sarmiento MA, Blazquez MG : Malignant and atypical meningiomas: a reappraisal of clinical, histological, and computed tomographic features. Neurosurgery 20 : 688-694, 1987 https://doi.org/10.1227/00006123-198705000-00003
  6. Ammendola S, Bariani E, Eccher A, Capitanio A, Ghimenton C, Pantanowitz L, et al. : The histopathological diagnosis of atypical meningioma: glass slide versus whole slide imaging for grading assessment. Virchows Arch 478 : 474-756, 2021
  7. Arai H, Beppu T, Wada T, Yoshida Y, Kubo Y, Suzuki M, et al. : Pathological analyses of early recurrence and malignant transformation in meningiomas. Brain Tumor Pathol 15 : 37-40, 1998 https://doi.org/10.1007/BF02482099
  8. Ayerbe J, Lobato RD, de la Cruz J, Alday R, Rivas JJ, Gomez PA, et al. : Risk factors predicting recurrence in patients operated on for intracranial meningioma. A multivariate analysis. Acta Neurochir (Wien) 141 : 921-932, 1999 https://doi.org/10.1007/s007010050398
  9. Barresi V, Lionti S, Caliri S, Caffo M : Histopathological features to define atypical meningioma: what does really matter for prognosis? Brain Tumor Pathol 35 : 168-180, 2018 https://doi.org/10.1007/s10014-018-0318-z
  10. Bollag RJ, Vender JR, Sharma S : Anaplastic meningioma: progression from atypical and chordoid morphotype with morphologic spectral variation at recurrence. Neuropathology 30 : 279-287, 2010 https://doi.org/10.1111/j.1440-1789.2009.01060.x
  11. Brokinkel B, Spille DC, Brokinkel C, Hess K, Paulus W, Bormann E, et al. : The Simpson grading: defining the optimal threshold for gross total resection in meningioma surgery. Neurosurg Rev 44 : 1713-1720, 2021 https://doi.org/10.1007/s10143-020-01369-1
  12. Budohoski KP, Clerkin J, Millward CP, O'Halloran PJ, Waqar M, Looby S, et al. : Predictors of early progression of surgically treated atypical meningiomas. Acta Neurochir (Wien) 160 : 1813-1822, 2018 https://doi.org/10.1007/s00701-018-3593-x
  13. Claus EB, Bondy ML, Schildkraut JM, Wiemels JL, Wrensch M, Black PM : Epidemiology of intracranial meningioma. Neurosurgery 57 : 1088-1095; discussion 1088-1095, 2005 https://doi.org/10.1227/01.NEU.0000188281.91351.B9
  14. Dietemann JL, Heldt N, Burguet JL, Medjek L, Maitrot D, Wackenheim A : CT findings in malignant meningiomas. Neuroradiology 23 : 207-209, 1982 https://doi.org/10.1007/BF00342542
  15. Domingues PH, Sousa P, Otero A, Goncalves JM, Ruiz L, de Oliveira C, et al. : Proposal for a new risk stratification classification for meningioma based on patient age, WHO tumor grade, size, localization, and karyotype. Neuro Oncol 16 : 735-747, 2014 https://doi.org/10.1093/neuonc/not325
  16. Duregon E, Cassenti A, Pittaro A, Ventura L, Senetta R, Ruda R, et al. : Better see to better agree: phosphohistone H3 increases interobserver agreement in mitotic count for meningioma grading and imposes new specific thresholds. Neuro Oncol 17 : 663-669, 2015 https://doi.org/10.1093/neuonc/nov002
  17. Goldbrunner R, Minniti G, Preusser M, Jenkinson MD, Sallabanda K, Houdart E, et al. : EANO guidelines for the diagnosis and treatment of meningiomas. Lancet Oncol 17 : e383-e391, 2016 https://doi.org/10.1016/S1470-2045(16)30321-7
  18. Ide M, Jimbo M, Kubo O, Yamamoto M, Imanaga H : Peritumoral brain edema associated with meningioma--histological study of the tumor margin and surrounding brain. Neurol Med Chir (Tokyo) 32 : 65-71, 1992 https://doi.org/10.2176/nmc.32.65
  19. Ildan F, Erman T, Gocer AI, Tuna M, Bagdatoglu H, Cetinalp E, 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 17 : 157-171, 2007 https://doi.org/10.1055/s-2007-970554
  20. Ishino S, Hashimoto N, Fushiki S, Date K, Mori T, Fujimoto M, et al. : Loss of material from chromosome arm 1p during malignant progression of meningioma revealed by fluorescent in situ hybridization. Cancer 83 : 360-366, 1998 https://doi.org/10.1002/(SICI)1097-0142(19980715)83:2<360::AID-CNCR21>3.0.CO;2-Q
  21. Jaaskelainen J, Haltia M, Laasonen E, Wahlstrom T, Valtonen S : The growth rate of intracranial meningiomas and its relation to histology. An analysis of 43 patients. Surg Neurol 24 : 165-172, 1985 https://doi.org/10.1016/0090-3019(85)90180-6
  22. Jaaskelainen J, Haltia M, Servo A : Atypical and anaplastic meningiomas: radiology, surgery, radiotherapy, and outcome. Surg Neurol 25 : 233-242, 1986 https://doi.org/10.1016/0090-3019(86)90233-8
  23. Jellinger K, Slowik F : Histological subtypes and prognostic problems in meningiomas. J Neurol 208 : 279-298, 1975 https://doi.org/10.1007/BF00312803
  24. Kawahara Y, Nakada M, Hayashi Y, Kai Y, Hayashi Y, Uchiyama N, et al. : Prediction of high-grade meningioma by preoperative MRI assessment. J Neurooncol 108 : 147-152, 2012 https://doi.org/10.1007/s11060-012-0809-4
  25. Kim D, Niemierko A, Hwang WL, Stemmer-Rachamimov AO, Curry WT, Barker FG, et al. : Histopathological prognostic factors of recurrence following definitive therapy for atypical and malignant meningiomas. J Neurosurg 128 : 1123-1132, 2018 https://doi.org/10.3171/2016.11.jns16913
  26. Krayenbuhl N, Pravdenkova S, Al-Mefty O : De novo versus transformed atypical and anaplastic meningiomas: comparisons of clinical course, cytogenetics, cytokinetics, and outcome. Neurosurgery 61 : 495-503; discussion 503-504, 2007 https://doi.org/10.1227/01.NEU.0000290895.92695.22
  27. Kwon SM, Kim JH, Yoo HJ, Kim YH, Hong SH, Cho YH, et al. : Predictive factors for high-grade transformation in benign meningiomas. Clin Neurol Neurosurg 195 : 105897, 2020 https://doi.org/10.1016/j.clineuro.2020.105897
  28. Lamszus K, Kluwe L, Matschke J, Meissner H, Laas R, Westphal M : Allelic losses at 1p, 9q, 10q, 14q, and 22q in the progression of aggressive meningiomas and undifferentiated meningeal sarcomas. Cancer Genet Cytogenet 110 : 103-110, 1999 https://doi.org/10.1016/S0165-4608(98)00209-X
  29. Lee KD, DePowell JJ, Air EL, Dwivedi AK, Kendler A, McPherson CM : Atypical meningiomas: is postoperative radiotherapy indicated? Neurosurg Focus 35 : E15, 2013 https://doi.org/10.3171/2013.9.FOCUS13325
  30. Lindblom A, Ruttledge M, Collins VP, Nordenskjold M, Dumanski JP : Chromosomal deletions in anaplastic meningiomas suggest multiple regions outside chromosome 22 as important in tumor progression. Int J Cancer 56 : 354-357, 1994 https://doi.org/10.1002/ijc.2910560310
  31. Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, et al. : The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol (Berl) 131 : 803-820, 2016 https://doi.org/10.1007/s00401-016-1545-1
  32. Maiuri F, Mariniello G, Barbato M, Corvino S, Guadagno E, Chiariotti L, et al. : Malignant intraventricular meningioma: literature review and case report. Neurosurg Rev, 2021 [Epub ahead of print]
  33. Mantle RE, Lach B, Delgado MR, Baeesa S, Belanger G : Predicting the probability of meningioma recurrence based on the quantity of peritumoral brain edema on computerized tomography scanning. J Neurosurg 91 : 375-383, 1999 https://doi.org/10.3171/jns.1999.91.3.0375
  34. Nakasu S, Nakasu Y, Nakajima M, Matsuda M, Handa J : Preoperative identification of meningiomas that are highly likely to recur. J Neurosurg 90 : 455-462, 1999 https://doi.org/10.3171/jns.1999.90.3.0455
  35. Nanda A, Bir SC, Konar S, Maiti T, Kalakoti P, Jacobsohn JA, et al. : Outcome of resection of WHO grade II meningioma and correlation of pathological and radiological predictive factors for recurrence. J Clin Neurosci 31 : 112-121, 2016 https://doi.org/10.1016/j.jocn.2016.02.021
  36. Olar A, Wani KM, Sulman EP, Mansouri A, Zadeh G, Wilson CD, et al. : Mitotic index is an independent predictor of recurrence-free survival in meningioma. Brain Pathol 25 : 266-275, 2015 https://doi.org/10.1111/bpa.12174
  37. Olmsted WW, McGee TP : Prognosis in meningioma through evaluation of skull bone patterns. Radiology 123 : 375-377, 1977 https://doi.org/10.1148/123.2.375
  38. Palma L, Celli P, Franco C, Cervoni L, Cantore G : Long-term prognosis for atypical and malignant meningiomas: a study of 71 surgical cases. J Neurosurg 86 : 793-800, 1997 https://doi.org/10.3171/jns.1997.86.5.0793
  39. Perry A, Scheithauer BW, Stafford SL, Lohse CM, Wollan PC : "Malignancy" in meningiomas: a clinicopathologic study of 116 patients, with grading implications. Cancer 85 : 2046-2056, 1999
  40. Perry A, Stafford SL, Scheithauer BW, Suman VJ, Lohse CM : Meningioma grading: an analysis of histologic parameters. Am J Surg Pathol 21 : 1455-1465, 1997 https://doi.org/10.1097/00000478-199712000-00008
  41. Peyre M, Gauchotte G, Giry M, Froehlich S, Pallud J, Graillon T, et al. : De novo and secondary anaplastic meningiomas: a study of clinical and histomolecular prognostic factors. Neuro Oncol 20 : 1113-1121, 2018 https://doi.org/10.1093/neuonc/nox231
  42. Ribalta T, McCutcheon IE, Aldape KD, Bruner JM, Fuller GN : The mitosis-specific antibody anti-phosphohistone-H3 (PHH3) facilitates rapid reliable grading of meningiomas according to WHO 2000 criteria. Am J Surg Pathol 28 : 1532-1536, 2004 https://doi.org/10.1097/01.pas.0000141389.06925.d5
  43. Salah F, Tabbarah A, ALArab Y N, Asmar K, Tamim H, Makki M, et al. : Can CT and MRI features differentiate benign from malignant meningiomas? Clin Radiol 74 : 898.e15-898.e23, 2019 https://doi.org/10.1016/j.crad.2019.07.020
  44. Salpietro FM, Alafaci C, Lucerna S, Iacopino DG, Todaro C, Tomasello F : Peritumoral edema in meningiomas: microsurgical observations of different brain tumor interfaces related to computed tomography. Neurosurgery 35 : 638-641; discussion 641-642, 1994 https://doi.org/10.1227/00006123-199410000-00009
  45. San-Miguel T, Cerda-Nicolas M, Gil-Benso R, Callaghan RC, MunozHidalgo L, Lopez-Gines C : Evolution to malignancy: a genetic stepwise study of tumor suppressor genes loss in a recurrent meningioma. Clin Neuropathol 34 : 237-239, 2015 https://doi.org/10.5414/NP300839
  46. Simpson D : The recurrence of intracranial meningiomas after surgical treatment. J Neurol Neurosurg Psychiatry 20 : 22-39, 1957 https://doi.org/10.1136/jnnp.20.1.22
  47. Sun SQ, Kim AH, Cai C, Murphy RK, DeWees T, Sylvester P, et al. : 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 354-355; quiz 355, 2014 https://doi.org/10.1227/NEU.0000000000000461
  48. Vranic A, Popovic M, Cor A, Prestor B, Pizem J : Mitotic count, brain invasion, and location are independent predictors of recurrence-free survival in primary atypical and malignant meningiomas: a study of 86 patients. Neurosurgery 67 : 1124-1132, 2010 https://doi.org/10.1227/NEU.0b013e3181eb95b7
  49. Wang F, Xu D, Liu Y, Lin Y, Wei Q, Gao Q, et al. : Risk factors associated with postoperative recurrence in atypical intracranial meningioma: analysis of 263 cases at a single neurosurgical centre. Acta Neurochir (Wien) 161 : 2563-2570, 2019 https://doi.org/10.1007/s00701-019-04073-2
  50. Younis G, Sawaya R : Intracranial osteolytic malignant meningiomas appearing as extracranial soft-tissue masses. Neurosurgery 30 : 932-935, 1992 https://doi.org/10.1097/00006123-199206000-00022