Clinical Neurology and Neurosurgery 128 (2015) 112–116
Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Skull base atypical meningioma: Long term surgical outcome and prognostic factors Yu-Chi Wang a , Chi-Cheng Chuang a , Kuo-Chen Wei a , Yung-Hsin Hsu a , Peng-Wei Hsu a , Shih-Tseng Lee a , Chieh-Tsai Wu a , Chen-Kan Tseng b , Chun-Chieh Wang b , Yao-Liang Chen c , Shih-Min Jung d , Pin-Yuan Chen a,,∗ a
Department of Neurosurgery, Chang Gung Memorial Hospital at Linkou, Chang Gung University, Taoyuan, Taiwan, ROC Department of Radiation Oncology, Chang Gung Memorial Hospital at Linkou, Chang Gung University, Taoyuan, Taiwan, ROC c Department of Radiology, Chang Gung Memorial Hospital at Linkou, Chang Gung University, Taoyuan, Taiwan, ROC d Department of Pathology, Chang Gung Memorial Hospital at Linkou, Chang Gung University, Taoyuan, Taiwan, ROC b
a r t i c l e
i n f o
Article history: Received 18 September 2014 Received in revised form 2 November 2014 Accepted 10 November 2014 Available online 24 November 2014 Keywords: Atypical meningioma Skull base Surgery Radiotherapy MIB-1 index
a b s t r a c t Purpose: The aim of this study was to examine the clinical outcomes of treating atypical meningioma at the skull base region following surgical resection and adjuvant radiotherapy, and to analyze the association between clinical characteristics and progression free survival. Materials and methods: Twenty-eight patients with skull base atypical meningiomas underwent microsurgical resection between June 2001 and November 2009. The clinical characteristics of the patients and meningiomas, the extent of surgical resection, and complications after treatment were retrospectively analyzed. Results: Thirteen patients (46.4%) had disease recurrence or progression during follow up time. The median time to disease progression was 64 months. The extent of the surgical resection significantly impacted prognosis. Gross total resection (GTR) of the tumor improved progression free survival (PFS) compared to subtotal resection (STR, p = 0.011). An older patient age at diagnosis also resulted in a worse outcome (p = 0.024). An MIB-1 index 8% was also associated with a higher rate of progression (p = 0.031, Fig. 2). Sex did not contribute significantly to PFS, but age had a significant influence (p = 0.024). Neither the diameters nor the locations of the tumors were associated with disease progression. Upon multivariate analysis, only the completeness of the surgical resection and an MIB index 8% had recurrent tumors, while only 20% of the patients with an MIB-1 index 8%, had a 100% tumor recurrence rate, compared to only 50% in patients with an MIB index 8
MIB < 8
MIB > 8
MIB < 8
6 3 (50%) 2.50 (0.364–17.173)
5 1 (20%) –
4 4 (100%) 2.00 (0.648–3.472)
10 5 (50%) –
Table 4 Complication after surgical resection. Case no
Tumor location
Tumor diameter (cm)
Resection extent
Complication
1 2 3
Sphenoid ridge Petroclivus Petroclivus
8.3 5.5 4.2
GTR GTR STR
Hemiparesis Facial palsy Facial palsy
GTR is the accepted standard of care for benign meningioma [19–21]. However, GTR is complicated in the skull base because of the many critical surrounding structures, and aggressive resection can lead to severe morbidity [21]. STR, or partial resection, is an alternative treatment strategy that can be used to preserve neurological function [5,16]. In the current study, GTR was strongly predictive of prolonged PFS. These results are consistent with Zaher et al. and others who have reported that patients with atypical meningioma who underwent complete surgical resection had better survival rates than patients who underwent subtotal resection [22]. In our series, two patients who underwent GTR developed left hemiparesis or facial palsy following surgery, while one patient had facial palsy after STR. The relatively low complication rate after GTR in the skull base area suggests that aggressive surgical tumor resection using modern microsurgical techniques may be able to increase PFS without causing neurologic sequelae. However, Adachi et al. have shown there is a negative effect of extensive resection on neurological outcome in a subgroup of patients [5], and Scheitzach et al. reported that careful and complete decompression of adjacent structures is sufficient to relieve clinical symptoms rather than attempting to radically resect the entire tumor shell [23]. Thus, although surgery is indispensable for managing skull base atypical meningiomas, and there is a clear correlation between the extent of resection and the tumor recurrence rate, doubts about causing significant morbidity and neurological sequelae remain and likely contribute to continued STR [5]. The results of including adjuvant radiotherapy treatment following surgery in atypical meningioma are inconsistent [24]. There is conflicting evidence as to whether adjuvant radiotherapy delays tumor recurrence following complete resection or STR [10,25], or if its role remains unclear [26,27]. Thus, the existing data is insufficient to establish adjuvant radiotherapy as a standard of care in patients with atypical meningioma. In our series, there was no association between adjuvant radiotherapy and PFS in all patients using a Kaplan–Meier analysis. However, there was a strong trend toward increased PFS for patients who underwent adjuvant radiotherapy following STR. These findings are consistent with previous studies indicating that adjuvant radiotherapy significantly impacts the clinical outcome of patients with atypical meningioma [25]. We did not observe a significant difference in the PFS between patients that underwent GTR and did not receive adjuvant radiotherapy and patients who underwent STR and received adjuvant radiotherapy. This suggests that the combination of STR and adjuvant radiotherapy reduced tumor progression with similar efficacy as GTR only. Thus, STR followed by adjuvant radiotherapy could be an alternative to GTR. In the current study, there were no signs of tumor recurrence in the cohort that underwent the combination of GTR and adjuvant
radiotherapy. Although this subgroup was too small to yield a statistically significant improvement in PFS compared with GTR alone, the combination of GTR and adjuvant radiotherapy may increase PFS. The results of this case series support the use of adjuvant radiotherapy, regardless of whether GTR or STR is employed, for patients with atypical meningiomas at the skull base area. In our series, patient age at diagnosis was a prognostic factor for tumor recurrence in both univariate and multivariate analyses. A patient age >50 years of age was significantly correlated with reduced PFS (p = 0.026). Zaher et al. have reported improved survival in patients 8%, and this would require a larger sample size to form a definitive conclusion. Moreover, the 100% recurrence rate in subgroup of patients with an MIB-1 index >8% who did not receive radiotherapy, suggests that atypical meningiomas with pathological risk factors, such as a high MIB-1 index, should be candidates for adjuvant radiotherapy to improve local control. 5. Limitations This study is limited by the retrospective design owing to random bias. The retrospective design also does not provide the same quality of evidence as prospectively acquired population-based studies or randomized clinical trials. In addition, data from a single institute are susceptible to selection bias. Finally, the small number of patients was insufficiently powered to compare the relative impact of some variables in patients with atypical meningioma.
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Y.-C. Wang et al. / Clinical Neurology and Neurosurgery 128 (2015) 112–116
6. Conclusion The present retrospective case series confirmed that a total resection is the optimal treatment for atypical meningioma in the skull base region, if no severe complications are expected after extensive resection. Our findings also suggest that adjuvant radiotherapy following surgery is reasonable regardless of whether the surgical resection is complete or partial. In addition, both a young patient age and low MIB-1 index benefitted the PFS rate. This study did not demonstrate that the addition of adjuvant radiotherapy could lead to an increase in the overall survival rate. Tumor recurrence can lead to additional treatment burdens such as multiple operations or radiotherapy, and additional morbidity. Thus, it is important to prevent local tumor progression. Our findings and others suggest that a prospective, randomized clinical trial would provide key insights into the use of adjuvant radiotherapy in patients with atypical skull base meningioma. Acknowledgments This research was supported by the grants from National Science Council, Taiwan (No. 102-2334-B-182A-068-MY3), and ChangGung Memorial Hospital, Taiwan (No. CMRPG3C0041). References [1] Modha A, Gutin PH. Diagnosis and treatment of atypical and anaplastic meningiomas: a review. Neurosurgery 2005;57:538–50 [discussion 50]. [2] Fuller GN, Scheithauer BW. The 2007 revised World Health Organization (WHO) classification of tumours of the central nervous system: newly codified entities. Brain Pathol 2007;17:304–7. [3] Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol (Berl) 2007;114:97–109. [4] Marosi C, Hassler M, Roessler K, Reni M, Sant M, Mazza E, et al. Meningioma. Crit Rev Oncol Hematol 2008;67:153–71. [5] Adachi K, Kawase T, Yoshida K, Yazaki T, Onozuka S. ABC surgical risk scale for skull base meningioma: a new scoring system for predicting the extent of tumor removal and neurological outcome. Clinical article. J Neurosurg 2009;111:1053–61. [6] Kane AJ, Sughrue ME, Rutkowski MJ, Shangari G, Fang S, McDermott MW, et al. Anatomic location is a risk factor for atypical and malignant meningiomas. Cancer 2011;117:1272–8. [7] Pearson BE, Markert JM, Fisher WS, Guthrie BL, Fiveash JB. Hitting a moving target: evolution of a treatment paradigm for atypical meningiomas amid changing diagnostic criteria. Neurosurg Focus 2008;24:E3. [8] Goyal LK, Suh JH, Mohan DS, Prayson RA, Lee J, Barnett GH. Local control and overall survival in atypical meningioma: a retrospective study. Int J Radiat Oncol Biol Phys 2000;46:57–61. [9] Jo K, Park HJ, Nam DH, Lee JI, Kong DS, Park K, et al. Treatment of atypical meningioma. J Clin Neurosci 2010;17:1362–6. [10] 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 2009;64:56–60 [discussion]. [11] Combs SE, Schulz-Ertner D, Debus J, von Deimling A, Hartmann C. Improved correlation of the neuropathologic classification according to adapted world health organization classification and outcome after radiotherapy in patients with atypical and anaplastic meningiomas. Int J Radiat Oncol Biol Phys 2011;81:1415–21.
[12] Hug EB, Devries A, Thornton AF, Munzenride JE, Pardo FS, Hedley-Whyte ET, et al. Management of atypical and malignant meningiomas: role of high-dose, 3D-conformal radiation therapy. J Neurooncol 2000;48:151–60. [13] Choi CY, Soltys SG, Gibbs IC, Harsh GR, Jackson PS, Lieberson RE, et al. Cyberknife stereotactic radiosurgery for treatment of atypical (WHO grade II) cranial meningiomas. Neurosurgery 2010;67:1180–8. [14] El-Khatib M, El Majdoub F, Hoevels M, Kocher M, Muller RP, Steiger HJ, et al. Stereotactic LINAC radiosurgery for incompletely resected or recurrent atypical and anaplastic meningiomas. Acta Neurochir (Wien) 2011;153: 1761–7. [15] Attia A, Chan MD, Mott RT, Russell GB, Seif D, Daniel Bourland J, et al. Patterns of failure after treatment of atypical meningioma with gamma knife radiosurgery. J Neurooncol 2012;108:179–85. [16] Ohba S, Kobayashi M, Horiguchi T, Onozuka S, Yoshida K, Ohira T, et al. Longterm surgical outcome and biological prognostic factors in patients with skull base meningiomas. J Neurosurg 2011;114:1278–87. [17] Dziuk TW, Woo S, Butler EB, Thornby J, Grossman R, Dennis WS, et al. Malignant meningioma: an indication for initial aggressive surgery and adjuvant radiotherapy. J Neurooncol 1998;37:177–88. [18] Hardesty DA, Wolf AB, Brachman DG, McBride HL, Youssef E, Nakaji P, et al. The impact of adjuvant stereotactic radiosurgery on atypical meningioma recurrence following aggressive microsurgical resection. J Neurosurg 2013;119:475–81. [19] Ichinose T, Goto T, Ishibashi K, Takami T, Ohata K. The role of radical microsurgical resection in multimodal treatment for skull base meningioma. J Neurosurg 2010;113:1072–8. [20] Mathiesen T, Lindquist C, Kihlstrom L, Karlsson B. Recurrence of cranial base meningiomas. Neurosurgery 1996;39:2–7 [discussion 8–9]. [21] van Alkemade H, de Leau M, Dieleman EM, Kardaun JW, van Os R, Vandertop WP, et al. Impaired survival and long-term neurological problems in benign meningioma. Neurooncology 2012;14:658–66. [22] Zaher A, Abdelbari Mattar M, Zayed DH, Ellatif RA, Ashamallah SA. Atypical meningioma: a study of prognostic factors. World Neurosurg 2013;80: 549–53. [23] Scheitzach J, Schebesch KM, Brawanski A, Proescholdt MA. Skull base meningiomas: neurological outcome after microsurgical resection. J Neurooncol 2014;116:381–6. [24] Milosevic MF, Frost PJ, Laperriere NJ, Wong CS, Simpson WJ. Radiotherapy for atypical or malignant intracranial meningioma. Int J Radiat Oncol Biol Phys 1996;34:817–22. [25] Komotar RJ, Iorgulescu JB, Raper DM, Holland EC, Beal K, Bilsky MH, et al. The role of radiotherapy following gross-total resection of atypical meningiomas. J Neurosurg 2012;117:679–86. [26] Mair R, Morris K, Scott I, Carroll TA. Radiotherapy for atypical meningiomas. J Neurosurg 2011;115:811–9. [27] Stessin AM, Schwartz A, Judanin G, Pannullo SC, Boockvar JA, Schwartz TH, et al. Does adjuvant external-beam radiotherapy improve outcomes for nonbenign meningiomas? A surveillance, epidemiology, and end results (SEER)-based analysis. J Neurosurg 2012;117:669–75. [28] Sade B, Chahlavi A, Krishnaney A, Nagel S, Choi E, Lee JH. World Health Organization Grades II and III meningiomas are rare in the cranial base and spine. Neurosurgery 2007;61:1194–8 [discussion 8]. [29] Bruna J, Brell M, Ferrer I, Gimenez-Bonafe P, Tortosa A. Ki-67 proliferative index predicts clinical outcome in patients with atypical or anaplastic meningioma. Neuropathology 2007;27:114–20. [30] Nakasu S, Li DH, Okabe H, Nakajima M, Matsuda M. Significance of MIB-1 staining indices in meningiomas: comparison of two counting methods. Am J Surg Pathol 2001;25:472–8. [31] Torp SH, Lindboe CF, Granli US, Moen TM, Nordtomme T. Comparative investigation of proliferation markers and their prognostic relevance in human meningiomas. Clin Neuropathol 2001;20:190–5. [32] 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 2010;67:1124–32. [33] Park HJ, Kang HC, Kim IH, Park SH, Kim DG, Park CK, et al. The role of adjuvant radiotherapy in atypical meningioma. J Neurooncol 2013;115:241–7.
Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Skull base atypical meningioma: Long term surgical outcome and prognostic factors Yu-Chi Wang a , Chi-Cheng Chuang a , Kuo-Chen Wei a , Yung-Hsin Hsu a , Peng-Wei Hsu a , Shih-Tseng Lee a , Chieh-Tsai Wu a , Chen-Kan Tseng b , Chun-Chieh Wang b , Yao-Liang Chen c , Shih-Min Jung d , Pin-Yuan Chen a,,∗ a
Department of Neurosurgery, Chang Gung Memorial Hospital at Linkou, Chang Gung University, Taoyuan, Taiwan, ROC Department of Radiation Oncology, Chang Gung Memorial Hospital at Linkou, Chang Gung University, Taoyuan, Taiwan, ROC c Department of Radiology, Chang Gung Memorial Hospital at Linkou, Chang Gung University, Taoyuan, Taiwan, ROC d Department of Pathology, Chang Gung Memorial Hospital at Linkou, Chang Gung University, Taoyuan, Taiwan, ROC b
a r t i c l e
i n f o
Article history: Received 18 September 2014 Received in revised form 2 November 2014 Accepted 10 November 2014 Available online 24 November 2014 Keywords: Atypical meningioma Skull base Surgery Radiotherapy MIB-1 index
a b s t r a c t Purpose: The aim of this study was to examine the clinical outcomes of treating atypical meningioma at the skull base region following surgical resection and adjuvant radiotherapy, and to analyze the association between clinical characteristics and progression free survival. Materials and methods: Twenty-eight patients with skull base atypical meningiomas underwent microsurgical resection between June 2001 and November 2009. The clinical characteristics of the patients and meningiomas, the extent of surgical resection, and complications after treatment were retrospectively analyzed. Results: Thirteen patients (46.4%) had disease recurrence or progression during follow up time. The median time to disease progression was 64 months. The extent of the surgical resection significantly impacted prognosis. Gross total resection (GTR) of the tumor improved progression free survival (PFS) compared to subtotal resection (STR, p = 0.011). An older patient age at diagnosis also resulted in a worse outcome (p = 0.024). An MIB-1 index 8% was also associated with a higher rate of progression (p = 0.031, Fig. 2). Sex did not contribute significantly to PFS, but age had a significant influence (p = 0.024). Neither the diameters nor the locations of the tumors were associated with disease progression. Upon multivariate analysis, only the completeness of the surgical resection and an MIB index 8% had recurrent tumors, while only 20% of the patients with an MIB-1 index 8%, had a 100% tumor recurrence rate, compared to only 50% in patients with an MIB index 8
MIB < 8
MIB > 8
MIB < 8
6 3 (50%) 2.50 (0.364–17.173)
5 1 (20%) –
4 4 (100%) 2.00 (0.648–3.472)
10 5 (50%) –
Table 4 Complication after surgical resection. Case no
Tumor location
Tumor diameter (cm)
Resection extent
Complication
1 2 3
Sphenoid ridge Petroclivus Petroclivus
8.3 5.5 4.2
GTR GTR STR
Hemiparesis Facial palsy Facial palsy
GTR is the accepted standard of care for benign meningioma [19–21]. However, GTR is complicated in the skull base because of the many critical surrounding structures, and aggressive resection can lead to severe morbidity [21]. STR, or partial resection, is an alternative treatment strategy that can be used to preserve neurological function [5,16]. In the current study, GTR was strongly predictive of prolonged PFS. These results are consistent with Zaher et al. and others who have reported that patients with atypical meningioma who underwent complete surgical resection had better survival rates than patients who underwent subtotal resection [22]. In our series, two patients who underwent GTR developed left hemiparesis or facial palsy following surgery, while one patient had facial palsy after STR. The relatively low complication rate after GTR in the skull base area suggests that aggressive surgical tumor resection using modern microsurgical techniques may be able to increase PFS without causing neurologic sequelae. However, Adachi et al. have shown there is a negative effect of extensive resection on neurological outcome in a subgroup of patients [5], and Scheitzach et al. reported that careful and complete decompression of adjacent structures is sufficient to relieve clinical symptoms rather than attempting to radically resect the entire tumor shell [23]. Thus, although surgery is indispensable for managing skull base atypical meningiomas, and there is a clear correlation between the extent of resection and the tumor recurrence rate, doubts about causing significant morbidity and neurological sequelae remain and likely contribute to continued STR [5]. The results of including adjuvant radiotherapy treatment following surgery in atypical meningioma are inconsistent [24]. There is conflicting evidence as to whether adjuvant radiotherapy delays tumor recurrence following complete resection or STR [10,25], or if its role remains unclear [26,27]. Thus, the existing data is insufficient to establish adjuvant radiotherapy as a standard of care in patients with atypical meningioma. In our series, there was no association between adjuvant radiotherapy and PFS in all patients using a Kaplan–Meier analysis. However, there was a strong trend toward increased PFS for patients who underwent adjuvant radiotherapy following STR. These findings are consistent with previous studies indicating that adjuvant radiotherapy significantly impacts the clinical outcome of patients with atypical meningioma [25]. We did not observe a significant difference in the PFS between patients that underwent GTR and did not receive adjuvant radiotherapy and patients who underwent STR and received adjuvant radiotherapy. This suggests that the combination of STR and adjuvant radiotherapy reduced tumor progression with similar efficacy as GTR only. Thus, STR followed by adjuvant radiotherapy could be an alternative to GTR. In the current study, there were no signs of tumor recurrence in the cohort that underwent the combination of GTR and adjuvant
radiotherapy. Although this subgroup was too small to yield a statistically significant improvement in PFS compared with GTR alone, the combination of GTR and adjuvant radiotherapy may increase PFS. The results of this case series support the use of adjuvant radiotherapy, regardless of whether GTR or STR is employed, for patients with atypical meningiomas at the skull base area. In our series, patient age at diagnosis was a prognostic factor for tumor recurrence in both univariate and multivariate analyses. A patient age >50 years of age was significantly correlated with reduced PFS (p = 0.026). Zaher et al. have reported improved survival in patients 8%, and this would require a larger sample size to form a definitive conclusion. Moreover, the 100% recurrence rate in subgroup of patients with an MIB-1 index >8% who did not receive radiotherapy, suggests that atypical meningiomas with pathological risk factors, such as a high MIB-1 index, should be candidates for adjuvant radiotherapy to improve local control. 5. Limitations This study is limited by the retrospective design owing to random bias. The retrospective design also does not provide the same quality of evidence as prospectively acquired population-based studies or randomized clinical trials. In addition, data from a single institute are susceptible to selection bias. Finally, the small number of patients was insufficiently powered to compare the relative impact of some variables in patients with atypical meningioma.
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Y.-C. Wang et al. / Clinical Neurology and Neurosurgery 128 (2015) 112–116
6. Conclusion The present retrospective case series confirmed that a total resection is the optimal treatment for atypical meningioma in the skull base region, if no severe complications are expected after extensive resection. Our findings also suggest that adjuvant radiotherapy following surgery is reasonable regardless of whether the surgical resection is complete or partial. In addition, both a young patient age and low MIB-1 index benefitted the PFS rate. This study did not demonstrate that the addition of adjuvant radiotherapy could lead to an increase in the overall survival rate. Tumor recurrence can lead to additional treatment burdens such as multiple operations or radiotherapy, and additional morbidity. Thus, it is important to prevent local tumor progression. Our findings and others suggest that a prospective, randomized clinical trial would provide key insights into the use of adjuvant radiotherapy in patients with atypical skull base meningioma. Acknowledgments This research was supported by the grants from National Science Council, Taiwan (No. 102-2334-B-182A-068-MY3), and ChangGung Memorial Hospital, Taiwan (No. CMRPG3C0041). References [1] Modha A, Gutin PH. Diagnosis and treatment of atypical and anaplastic meningiomas: a review. Neurosurgery 2005;57:538–50 [discussion 50]. [2] Fuller GN, Scheithauer BW. The 2007 revised World Health Organization (WHO) classification of tumours of the central nervous system: newly codified entities. Brain Pathol 2007;17:304–7. [3] Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol (Berl) 2007;114:97–109. [4] Marosi C, Hassler M, Roessler K, Reni M, Sant M, Mazza E, et al. Meningioma. Crit Rev Oncol Hematol 2008;67:153–71. [5] Adachi K, Kawase T, Yoshida K, Yazaki T, Onozuka S. ABC surgical risk scale for skull base meningioma: a new scoring system for predicting the extent of tumor removal and neurological outcome. Clinical article. J Neurosurg 2009;111:1053–61. [6] Kane AJ, Sughrue ME, Rutkowski MJ, Shangari G, Fang S, McDermott MW, et al. Anatomic location is a risk factor for atypical and malignant meningiomas. Cancer 2011;117:1272–8. [7] Pearson BE, Markert JM, Fisher WS, Guthrie BL, Fiveash JB. Hitting a moving target: evolution of a treatment paradigm for atypical meningiomas amid changing diagnostic criteria. Neurosurg Focus 2008;24:E3. [8] Goyal LK, Suh JH, Mohan DS, Prayson RA, Lee J, Barnett GH. Local control and overall survival in atypical meningioma: a retrospective study. Int J Radiat Oncol Biol Phys 2000;46:57–61. [9] Jo K, Park HJ, Nam DH, Lee JI, Kong DS, Park K, et al. Treatment of atypical meningioma. J Clin Neurosci 2010;17:1362–6. [10] 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 2009;64:56–60 [discussion]. [11] Combs SE, Schulz-Ertner D, Debus J, von Deimling A, Hartmann C. Improved correlation of the neuropathologic classification according to adapted world health organization classification and outcome after radiotherapy in patients with atypical and anaplastic meningiomas. Int J Radiat Oncol Biol Phys 2011;81:1415–21.
[12] Hug EB, Devries A, Thornton AF, Munzenride JE, Pardo FS, Hedley-Whyte ET, et al. Management of atypical and malignant meningiomas: role of high-dose, 3D-conformal radiation therapy. J Neurooncol 2000;48:151–60. [13] Choi CY, Soltys SG, Gibbs IC, Harsh GR, Jackson PS, Lieberson RE, et al. Cyberknife stereotactic radiosurgery for treatment of atypical (WHO grade II) cranial meningiomas. Neurosurgery 2010;67:1180–8. [14] El-Khatib M, El Majdoub F, Hoevels M, Kocher M, Muller RP, Steiger HJ, et al. Stereotactic LINAC radiosurgery for incompletely resected or recurrent atypical and anaplastic meningiomas. Acta Neurochir (Wien) 2011;153: 1761–7. [15] Attia A, Chan MD, Mott RT, Russell GB, Seif D, Daniel Bourland J, et al. Patterns of failure after treatment of atypical meningioma with gamma knife radiosurgery. J Neurooncol 2012;108:179–85. [16] Ohba S, Kobayashi M, Horiguchi T, Onozuka S, Yoshida K, Ohira T, et al. Longterm surgical outcome and biological prognostic factors in patients with skull base meningiomas. J Neurosurg 2011;114:1278–87. [17] Dziuk TW, Woo S, Butler EB, Thornby J, Grossman R, Dennis WS, et al. Malignant meningioma: an indication for initial aggressive surgery and adjuvant radiotherapy. J Neurooncol 1998;37:177–88. [18] Hardesty DA, Wolf AB, Brachman DG, McBride HL, Youssef E, Nakaji P, et al. The impact of adjuvant stereotactic radiosurgery on atypical meningioma recurrence following aggressive microsurgical resection. J Neurosurg 2013;119:475–81. [19] Ichinose T, Goto T, Ishibashi K, Takami T, Ohata K. The role of radical microsurgical resection in multimodal treatment for skull base meningioma. J Neurosurg 2010;113:1072–8. [20] Mathiesen T, Lindquist C, Kihlstrom L, Karlsson B. Recurrence of cranial base meningiomas. Neurosurgery 1996;39:2–7 [discussion 8–9]. [21] van Alkemade H, de Leau M, Dieleman EM, Kardaun JW, van Os R, Vandertop WP, et al. Impaired survival and long-term neurological problems in benign meningioma. Neurooncology 2012;14:658–66. [22] Zaher A, Abdelbari Mattar M, Zayed DH, Ellatif RA, Ashamallah SA. Atypical meningioma: a study of prognostic factors. World Neurosurg 2013;80: 549–53. [23] Scheitzach J, Schebesch KM, Brawanski A, Proescholdt MA. Skull base meningiomas: neurological outcome after microsurgical resection. J Neurooncol 2014;116:381–6. [24] Milosevic MF, Frost PJ, Laperriere NJ, Wong CS, Simpson WJ. Radiotherapy for atypical or malignant intracranial meningioma. Int J Radiat Oncol Biol Phys 1996;34:817–22. [25] Komotar RJ, Iorgulescu JB, Raper DM, Holland EC, Beal K, Bilsky MH, et al. The role of radiotherapy following gross-total resection of atypical meningiomas. J Neurosurg 2012;117:679–86. [26] Mair R, Morris K, Scott I, Carroll TA. Radiotherapy for atypical meningiomas. J Neurosurg 2011;115:811–9. [27] Stessin AM, Schwartz A, Judanin G, Pannullo SC, Boockvar JA, Schwartz TH, et al. Does adjuvant external-beam radiotherapy improve outcomes for nonbenign meningiomas? A surveillance, epidemiology, and end results (SEER)-based analysis. J Neurosurg 2012;117:669–75. [28] Sade B, Chahlavi A, Krishnaney A, Nagel S, Choi E, Lee JH. World Health Organization Grades II and III meningiomas are rare in the cranial base and spine. Neurosurgery 2007;61:1194–8 [discussion 8]. [29] Bruna J, Brell M, Ferrer I, Gimenez-Bonafe P, Tortosa A. Ki-67 proliferative index predicts clinical outcome in patients with atypical or anaplastic meningioma. Neuropathology 2007;27:114–20. [30] Nakasu S, Li DH, Okabe H, Nakajima M, Matsuda M. Significance of MIB-1 staining indices in meningiomas: comparison of two counting methods. Am J Surg Pathol 2001;25:472–8. [31] Torp SH, Lindboe CF, Granli US, Moen TM, Nordtomme T. Comparative investigation of proliferation markers and their prognostic relevance in human meningiomas. Clin Neuropathol 2001;20:190–5. [32] 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 2010;67:1124–32. [33] Park HJ, Kang HC, Kim IH, Park SH, Kim DG, Park CK, et al. The role of adjuvant radiotherapy in atypical meningioma. J Neurooncol 2013;115:241–7.
