Significance of Simpson grading system in modern meningioma surgery: integration of the grade with MIB-1 labeling index as a key to predict the recurrence of WHO Grade I meningiomas

Clinical article

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Object

Techniques for the surgical treatment of meningioma have undergone many improvements since Simpson established the neurosurgical dogma for meningioma surgery in his seminal paper published in 1957. This study aims to assess the clinical significance and limitations of the Simpson grading system in relation to modern surgery for WHO Grade I benign meningiomas and to explore the potential of the cell proliferation index to complement the limitations in predicting their recurrence.

Methods

The surgical records of patients who underwent resection of intracranial meningiomas at the University of Tokyo Hospital between January 1995 and August 2010 were retrospectively analyzed. The authors investigated the relationships between recurrence-free survival (RFS) and Simpson grade or MIB-1 labeling index value.

Results

A total of 240 patients harboring 248 benign meningiomas were included in this study. Simpson Grade IV resection was associated with a significantly shorter RFS than Simpson Grade I, II, or III resection (p < 0.001), while no statistically significant difference was noted in RFS between Simpson Grades I, II, and III. Among meningiomas treated by Simpson Grade II and III resections, however, multivariate analysis revealed that an MIB-1 index of 3% or higher was associated with a significantly shorter time to recurrence.

Conclusions

The clinical significance of the different management strategies related to Simpson Grade I–III resection may have been diluted in the modern surgical era. The MIB-1 index can differentiate tumors with a high risk of recurrence, which could be beneficial for planning tailored optimal follow-up strategies. The results of this study appear to provide a significant backing for the recent shift in meningioma surgery from attempting aggressive resection to valuing the quality of the patient's life.

Abbreviations used in this paper:LI = labeling index; RFS = recurrence-free survival.
Article Information

Contributor Notes

Address correspondence to: Soichi Oya, M.D., Ph.D., Department of Neurosurgery, University of Tokyo, 7-3-1 Hongo Bunkyo, Tokyo 113-8655, Japan. email: sooya-tky@umin.ac.jp.Please include this information when citing this paper: published online May 4, 2012; DOI: 10.3171/2012.3.JNS111945.
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References
  • 1

    Abramovich CMPrayson RA: Histopathologic features and MIB-1 labeling indices in recurrent and nonrecurrent meningiomas. Arch Pathol Lab Med 123:7938001999

    • Search Google Scholar
    • Export Citation
  • 2

    Adegbite ABKhan MIPaine KWTan LK: The recurrence of intracranial meningiomas after surgical treatment. J Neurosurg 58:51561983

    • Search Google Scholar
    • Export Citation
  • 3

    Aguiar PHTsanaclis AMTella OI JrPlese JP: Proliferation rate of intracranial meningiomas as defined by the monoclonal antibody MIB-1: correlation with peritumoural oedema and other clinicoradiological and histological characteristics. Neurosurg Rev 26:2212282003

    • Search Google Scholar
    • Export Citation
  • 4

    Amatya VJTakeshima YSugiyama KKurisu KNishisaka TFukuhara T: Immunohistochemical study of Ki-67 (MIB-1), p53 protein, p21WAF1, and p27KIP1 expression in benign, atypical, and anaplastic meningiomas. Hum Pathol 32:9709752001

    • Search Google Scholar
    • Export Citation
  • 5

    Black PMMorokoff APZauberman J: Surgery for extra-axial tumors of the cerebral convexity and midline. Neurosurgery 62:6 Suppl 3111511232008

    • Search Google Scholar
    • Export Citation
  • 6

    Crompton MRGautier-Smith PC: The prediction of recurrence in meningiomas. J Neurol Neurosurg Psychiatry 33:80871970

  • 7

    Heros RC: Simpson grade and treatment. Editorial J Neurosurg 113:102610282010

  • 8

    Hirsch WLSekhar LNLanzino GPomonis SSen CN: Meningiomas involving the cavernous sinus: value of imaging for predicting surgical complications. AJR Am J Roentgenol 160:108310881993

    • Search Google Scholar
    • Export Citation
  • 9

    Iwai YYamanaka KIkeda H: Gamma Knife radiosurgery for skull base meningioma: long-term results of low-dose treatment. J Neurosurg 109:8048102008

    • Search Google Scholar
    • Export Citation
  • 10

    Jääskeläinen J: Seemingly complete removal of histologically benign intracranial meningioma: late recurrence rate and factors predicting recurrence in 657 patients. A multivariate analysis. Surg Neurol 26:4614691986

    • Search Google Scholar
    • Export Citation
  • 11

    Jellinger KSlowik F: Histological subtypes and prognostic problems in meningiomas. J Neurol 208:2792981975

  • 12

    Kärjä VSandell PJKauppinen TAlafuzoff I: Does protein expression predict recurrence of benign World Health Organization grade I meningioma?. Hum Pathol 41:1992072010

    • Search Google Scholar
    • Export Citation
  • 13

    Kasuya HKubo OTanaka MAmano KKato KHori T: Clinical and radiological features related to the growth potential of meningioma. Neurosurg Rev 29:2932972006

    • Search Google Scholar
    • Export Citation
  • 14

    Kim YJKetter RSteudel WIFeiden W: Prognostic significance of the mitotic index using the mitosis marker anti-phosphohistone H3 in meningiomas. Am J Clin Pathol 128:1181252007

    • Search Google Scholar
    • Export Citation
  • 15

    Kleihues PBurger PCScheithauer BW: The new WHO Classification of brain tumours. Brain Pathol 3:2552681993

  • 16

    Kleihues PCavanee WK: World Health Organization Classification of Tumours: Pathology and Genetics: Tumours of the Nervous System LyonIARC Press2000

    • Search Google Scholar
    • Export Citation
  • 17

    Kunishio KOhmoto TFuruta TMatsumoto KNishimoto A: Factors influencing the recurrence rate of intracranial meningiomas after surgery. Neurol Med Chir (Tokyo) 34:81851994

    • Search Google Scholar
    • Export Citation
  • 18

    Mathiesen TLindquist CKihlström LKarlsson B: Recurrence of cranial base meningiomas. Neurosurgery 39:291996

  • 19

    McGovern SLAldape KDMunsell MFMahajan ADeMonte FWoo SY: A comparison of World Health Organization tumor grades at recurrence in patients with non-skull base and skull base meningiomas. Clinical article. J Neurosurg 112:9259332010

    • Search Google Scholar
    • Export Citation
  • 20

    Melamed SSahar ABeller AJ: The recurrence of intracranial meningiomas. Neurochirurgia (Stuttg) 22:47511979

  • 21

    Mendenhall WMMorris CGAmdur RJFoote KDFriedman WA: Radiotherapy alone or after subtotal resection for benign skull base meningiomas. Cancer 98:147314822003

    • Search Google Scholar
    • Export Citation
  • 22

    Mirimanoff RODosoretz DELinggood RMOjemann RGMartuza RL: Meningioma: analysis of recurrence and progression following neurosurgical resection. J Neurosurg 62:18241985

    • Search Google Scholar
    • Export Citation
  • 23

    Nakaguchi HFujimaki TMatsuno AMatsuura RAsai ASuzuki I: Postoperative residual tumor growth of meningioma can be predicted by MIB-1 immunohistochemistry. Cancer 85:224922541999

    • Search Google Scholar
    • Export Citation
  • 24

    Nakasu SFukami TJito JNozaki K: Recurrence and regrowth of benign meningiomas. Brain Tumor Pathol 26:69722009

  • 25

    Nakasu SLi DHOkabe HNakajima MMatsuda M: Significance of MIB-1 staining indices in meningiomas: comparison of two counting methods. Am J Surg Pathol 25:4724782001

    • Search Google Scholar
    • Export Citation
  • 26

    Nakaya KChernov MKasuya HIzawa MHayashi MKato K: Risk factors for regrowth of intracranial meningiomas after gamma knife radiosurgery: importance of the histopathological grade and MIB-1 index. Minim Invasive Neurosurg 52:2162212009

    • Search Google Scholar
    • Export Citation
  • 27

    Naumann MMeixensberger J: Factors influencing meningioma recurrence rate. Acta Neurochir (Wien) 107:1081111990

  • 28

    Pollock BEStafford SLUtter AGiannini CSchreiner SA: Stereotactic radiosurgery provides equivalent tumor control to Simpson Grade 1 resection for patients with small- to medium-size meningiomas. Int J Radiat Oncol Biol Phys 55:100010052003

    • Search Google Scholar
    • Export Citation
  • 29

    Rezanko TAkkalp AKTunakan MSari AA: MIB-1 counting methods in meningiomas and agreement among pathologists. Anal Quant Cytol Histol 30:47522008

    • Search Google Scholar
    • Export Citation
  • 30

    Roser FSamii MOstertag HBellinzona M: The Ki-67 proliferation antigen in meningiomas. Experience in 600 cases. Acta Neurochir (Wien) 146:37442004

    • Search Google Scholar
    • Export Citation
  • 31

    Schiffer DGhimenti CFiano V: Absence of histological signs of tumor progression in recurrences of completely resected meningiomas. J Neurooncol 73:1251302005

    • Search Google Scholar
    • Export Citation
  • 32

    Sekhar LNLevine ZTSarma S: Grading of meningiomas. J Clin Neurosci 8:Suppl 1172001

  • 33

    Simpson D: The recurrence of intracranial meningiomas after surgical treatment. J Neurol Neurosurg Psychiatry 20:22391957

  • 34

    Skullerud KLöken AC: The prognosis in meningiomas. Acta Neuropathol 29:3373441974

  • 35

    Smith SJBoddu SMacarthur DC: Atypical meningiomas: WHO moved the goalposts?. Br J Neurosurg 21:5885922007

  • 36

    Stafford SLPerry ASuman VJMeyer FBScheithauer BWLohse CM: Primarily resected meningiomas: outcome and prognostic factors in 581 Mayo Clinic patients, 1978 through 1988. Mayo Clin Proc 73:9369421998

    • Search Google Scholar
    • Export Citation
  • 37

    Strassner CBuhl RMehdorn HM: Recurrence of intracranial meningiomas: did better methods of diagnosis and surgical treatment change the outcome in the last 30 years?. Neurol Res 31:4784822009

    • Search Google Scholar
    • Export Citation
  • 38

    Sughrue MEKane AJShangari GRutkowski MJMcDermott MWBerger MS: The relevance of Simpson Grade I and II resection in modern neurosurgical treatment of World Health Organization Grade I meningiomas. Clinical article. J Neurosurg 113:102910352010

    • Search Google Scholar
    • Export Citation
  • 39

    Tyagi AChakrabarty AFranks A: MIB1 proliferation index in meningiomas: does it predict recurrence? A clinicopathological study. Br J Neurosurg 18:3573612004

    • Search Google Scholar
    • Export Citation
  • 40

    Vankalakunti MVasishta RKDas Radotra BKhosla VK: MIB-1 immunolabeling: a valuable marker in prediction of benign recurring meningiomas. Neuropathology 27:4074122007

    • Search Google Scholar
    • Export Citation
  • 41

    Vranic APopovic MCör APrestor BPizem 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 67:112411322010

    • Search Google Scholar
    • Export Citation
  • 42

    Zachenhofer IWolfsberger SAichholzer MBertalanffy ARoessler KKitz K: Gamma-knife radiosurgery for cranial base meningiomas: experience of tumor control, clinical course, and morbidity in a follow-up of more than 8 years. Neurosurgery 58:28362006

    • Search Google Scholar
    • Export Citation
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