Value of K_i-67 Labeling Index in Predicting Recurrence of WHO Grade I Cranial Base Meningiomas

Abstract

Objectives Assess impact of K_i-67 labeling index (LI; K_i-67 LI) on risk of recurrence or progression of WHO grade I meningiomas.

Study Design Retrospective study of adult patients who underwent resection of cranial base meningioma between 2004 and 2016.

Results 272 patients fulfilled criteria for inclusion in the study. Average age was 61.8 years; 196 (72%) were females. Simpson's grade 1 resection was noted in 77 patients (32%), grade 2 in 39 (16%), grade 3 in 36 (15%), and grade 4 in 88 (37%). The K_i-67 LI was low (1–4%) in 214 (78.7%), intermediate (5–9%) in 44 (16.2%), and high (>10%) in 14 (5.2%). Median follow-up was 39 months (IQR: 16–71 months); 221 (87.1%) tumors remained stable or did not recur, 19 (7.4%) recurred, and 14 (5.5%) progressed. Compared with tumors with low K_i-67 LI, those with intermediate K_i-67 LI had 2.47 times (2.47 [1.09–5.59], p = 0.03), and those with high K_i-67 LI had 3.38 times (3.38 [1.16–9.89], p = 0.03) higher risk of recurrence or progression. Tumors with K_i-67 LI > 4% had a shorter time to recurrence or progression (p = 0.01). Recurrence or progression-free survival rates at 3, 5, and 10 years for tumors with low K_i-67 LI were 95%, 89%, and 75%, respectively; tumors with intermediate K_i-67 LI, 87%, 69%, and 52%, respectively; tumors with high K_i-67 LI, 78%, 49%, and 49%, respectively.

Conclusions Following surgical resection of a WHO grade I cranial base meningioma, K_i-67 LI > 4% may predict an increased risk of recurrence or progression of residual tumor.

Keywords

meningioma - cranial base meningioma - meningioma recurrence - K_i-67 labeling index

• References

• 1 Claus EB, Bondy ML, Schildkraut JM, Wiemels JL, Wrensch M, Black PM. Epidemiology of intracranial meningioma. Neurosurgery 2005; 57 (06) 1088-1095 , discussion 1088–1095
• 2 Wiemels J, Wrensch M, Claus EB. Epidemiology and etiology of meningioma. J Neurooncol 2010; 99 (03) 307-314
• 3 Tufan K, Dogulu F, Kurt G, Emmez H, Ceviker N, Baykaner MK. Intracranial meningiomas of childhood and adolescence. Pediatr Neurosurg 2005; 41 (01) 1-7
• 4 Perry A, Stafford SL, Scheithauer BW, Suman VJ, Lohse CM. Meningioma grading: an analysis of histologic parameters. Am J Surg Pathol 1997; 21 (12) 1455-1465
• 5 Riemenschneider MJ, Perry A, Reifenberger G. Histological classification and molecular genetics of meningiomas. Lancet Neurol 2006; 5 (12) 1045-1054
• 6 Louis DN, Ohgaki H, Wiestler OD. , et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007; 114 (02) 97-109
• 7 Louis DN, Perry A, Reifenberger G. , et al. The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 2016; 131 (06) 803-820
• 8 Perry A, Gutmann DH, Reifenberger G. Molecular pathogenesis of meningiomas. J Neurooncol 2004; 70 (02) 183-202
• 9 Bi WL, Abedalthagafi M, Horowitz P. , et al. Genomic landscape of intracranial meningiomas. J Neurosurg 2016; 125 (03) 525-535
• 10 Simpson D. The recurrence of intracranial meningiomas after surgical treatment. J Neurol Neurosurg Psychiatry 1957; 20 (01) 22-39
• 11 Sughrue ME, Kane AJ, Shangari G. , et al. The relevance of Simpson grade I and II resection in modern neurosurgical treatment of World Health Organization grade I meningiomas. J Neurosurg 2010; 113 (05) 1029-1035
• 12 Hasseleid BF, Meling TR, Ronning P, Scheie D, Helseth E. Surgery for convexity meningioma: Simpson grade I resection as the goal: clinical article. J Neurosurg 2012; 111 (06) 999-1006
• 13 Ehresman JS, Garzon-Muvdi T, Rogers D. , et al. The relevance of Simpson grade resections in modern neurosurgical treatment of World Health Organization grade I, II, and III meningiomas. World Neurosurg 2018; 109: e588-e593
• 14 Gallagher MJ, Jenkinson MD, Brodbelt AR, Mills SJ, Chavredakis E. WHO grade 1 meningioma recurrence: are location and Simpson grade still relevant?. Clin Neurol Neurosurg 2016; 141: 117-121
• 15 Abdel-Aziz KM, Froelich SC, Dagnew E. , et al. Large sphenoid wing meningiomas involving the cavernous sinus: conservative surgical strategies for better functional outcomes. Neurosurgery 2004; 54 (06) 1375-1383 , discussion 1383–1384
• 16 Nanda A, Javalkar V, Banerjee AD. Petroclival meningiomas: study on outcomes, complications and recurrence rates. J Neurosurg 2011; 114 (05) 1268-1277
• 17 Mirimanoff RO, Dosoretz DE, Linggood RM, Ojemann RG, Martuza RL. Meningioma: analysis of recurrence and progression following neurosurgical resection. J Neurosurg 1985; 62 (01) 18-24
• 18 Adegbite AB, Khan MI, Paine KWE, Tan LK. The recurrence of intracranial meningiomas after surgical treatment. J Neurosurg 1983; 58 (01) 51-56
• 19 Sarkar A, Chiocca EA. Prognostic indicators. J Neurosurg 2006; 105 (02) 161-162 , discussion 162
• 20 Pravdenkova S, Al-Mefty O, Sawyer J, Husain M. Progesterone and estrogen receptors: opposing prognostic indicators in meningiomas. J Neurosurg 2006; 105 (02) 163-173
• 21 Bruno S, Darzynkiewicz Z. Cell cycle dependent expression and stability of the nuclear protein detected by Ki-67 antibody in HL-60 cells. Cell Prolif 1992; 25 (01) 31-40
• 22 Li LT, Jiang G, Chen Q, Zheng JN. Ki67 is a promising molecular target in the diagnosis of cancer (review). Mol Med Rep 2015; 11 (03) 1566-1572
• 23 Gerdes J, Lemke H, Baisch H, Wacker HH, Schwab U, Stein H. Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J Immunol 1984; 133 (04) 1710-1715
• 24 Ho DM, Hsu CY, Ting LT, Chiang H. Histopathology and MIB-1 labeling index predicted recurrence of meningiomas: a proposal of diagnostic criteria for patients with atypical meningioma. Cancer 2002; 94 (05) 1538-1547
• 25 İldan F, Erman T, Göçer AI. , 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 2007; 17 (03) 157-171
• 26 Lin DY, Wei LJ, Ying Z. Checking the Cox model with cumulative sums of martingale-based residuals. Biometrika 1993; 80: 557-572
• 27 Pirzkall A, Debus J, Haering P. , et al. Intensity modulated radiotherapy (IMRT) for recurrent, residual, or untreated skull-base meningiomas: preliminary clinical experience. Int J Radiat Oncol Biol Phys 2003; 55 (02) 362-372
• 28 Kreil W, Luggin J, Fuchs I, Weigl V, Eustacchio S, Papaefthymiou G. Long term experience of gamma knife radiosurgery for benign skull base meningiomas. J Neurol Neurosurg Psychiatry 2005; 76 (10) 1425-1430
• 29 Zachenhofer I, Wolfsberger S, Aichholzer M. , et al. 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 2006; 58 (01) 28-36 , discussion 28–36
• 30 Davidson L, Fishback D, Russin JJ. , et al. Postoperative Gamma knife surgery for benign meningiomas of the cranial base. Neurosurg Focus 2007; 23 (04) E6
• 31 Minniti G, Clarke E, Cavallo L. , et al. Fractionated stereotactic conformal radiotherapy for large benign skull base meningiomas. Radiat Oncol 2011; 6 (01) 36
• 32 Starke RM, Williams BJ, Hiles C, Nguyen JH, Elsharkawy MY, Sheehan JP. Gamma knife surgery for skull base meningiomas. J Neurosurg 2012; 116 (03) 588-597
• 33 Maier H, Ofner D, Hittmair A, Kitz K, Budka H. Classic, atypical, and anaplastic meningioma: three histopathological subtypes of clinical relevance. J Neurosurg 1992; 77 (04) 616-623
• 34 Mukhopadhyay M, Das C, Kumari M, Sen A, Mukhopadhyay B, Mukhopadhyay B. Spectrum of meningioma with special reference to prognostic utility of ER,PR and Ki67 expression. J Lab Physicians 2017; 9 (04) 308-313
• 35 Maeda I, Abe K, Koizumi H. , et al. Comparison between Ki67 labeling index determined using image analysis software with virtual slide system and that determined visually in breast cancer. Breast Cancer 2016; 23 (05) 745-751
• 36 Savardekar AR, Patra DP, Bir S. , et al. Differential tumor progression patterns in skull base versus non-skull base meningiomas: a critical analysis from a long-term follow-up study and review of literature. World Neurosurg 2018; 112: e74-e83
• 37 Oya S, Kawai K, Nakatomi H, Saito N. 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. J Neurosurg 2012; 117 (01) 121-128
• 38 Marciscano AE, Stemmer-Rachamimov AO, Niemierko A. , et al. Benign meningiomas (WHO grade I) with atypical histological features: correlation of histopathological features with clinical outcomes. J Neurosurg 2016; 124 (01) 106-114
• 39 Nanda A, Bir SC, Maiti TK, Konar SK, Missios S, Guthikonda B. Relevance of Simpson grading system and recurrence-free survival after surgery for World Health Organization grade I meningioma. J Neurosurg 2017; 126 (01) 201-211
• 40 Voß KM, Spille DC, Sauerland C. , et al. The Simpson grading in meningioma surgery: does the tumor location influence the prognostic value?. J Neurooncol 2017; 133 (03) 641-651
• 41 Ayerbe J, Lobato RD, de la Cruz J. , et al. Risk factors predicting recurrence in patients operated on for intracranial meningioma. A multivariate analysis. Acta Neurochir (Wien) 1999; 141 (09) 921-932