|Year : 2019 | Volume
| Issue : 1 | Page : 41-46
Clinicopathological characteristics of meningiomas: Experience from a tertiary care hospital in the Kashmir Valley
Basharat Mubeen1, Rumana Makhdoomi1, Khursheed Nayil2, Danish Rafiq1, Altaf Kirmani2, Othman Salim1, Farhat Mustafa1, Aifa Aimen1, Sumat Khursheed1, Shazia Bashir1, Saba Shafi1, Altaf Ramzan2
1 Department of Pathology, Sher-I-Kashmir Institute of Medical Sciences, Srinagar, Jammu and Kashmir, India
2 Department of Neurosurgery, Sher-I-Kashmir Institute of Medical Sciences, Srinagar, Jammu and Kashmir, India
|Date of Web Publication||21-Feb-2019|
Dr. Rumana Makhdoomi
Department of Pathology, Sher-I-Kashmir Institute of Medical Sciences, Srinagar - 190 011, Jammu and Kashmir
Source of Support: None, Conflict of Interest: None
Background: Meningiomas comprise 15%–20% of all primary intracranial tumors. They are generally benign tumors, and most patients are cured after surgery and remain free of recurrence. However, some tumors behave in an aggressive manner, and patients develop local recurrence or metastasis. Overall prognosis is good. Patients and Methods: This is an 11-year retrospective study conducted in the Departments of Pathology and Neurosurgery at Sheri-I-Kashmir Institute of Medical Sciences, Kashmir, India. Besides the demographic profile, the parameters analyzed were location of tumor on imaging, histopathological subtype, and grade of tumor according to the 2007 WHO classification and recurrence at follow-up. Results: A total of 254 patients were included in our study, of which 205 (80.7%) were brain meningiomas and 49 (19.3%) were spinal, with an overall female: male ratio of 2:1. Female: male ratio was more in spinal meningiomas, 15.3:1. Most of our patients were in the 4–6th decade of life with a mean age of 48 years (range: 5–73 years). Meningothelial meningioma was the most common histological type. Of ten patients who showed recurrence, seven cases showed only recurrence, but no progression to higher grade and three cases showed recurrence with progression by one WHO-grade. We also noticed that recurrence was higher in Simpson Grades II and III. Conclusion: Meningiomas are common in females and most of the meningiomas do well after surgery. The recurrence rate was 3.93% in our study and Simpson grade of tumor excision and histopathological grade contribute significantly to the recurrence of the tumor.
Keywords: Meningioma, recurrence, Simpson grade, WHO grading
|How to cite this article:|
Mubeen B, Makhdoomi R, Nayil K, Rafiq D, Kirmani A, Salim O, Mustafa F, Aimen A, Khursheed S, Bashir S, Shafi S, Ramzan A. Clinicopathological characteristics of meningiomas: Experience from a tertiary care hospital in the Kashmir Valley. Asian J Neurosurg 2019;14:41-6
|How to cite this URL:|
Mubeen B, Makhdoomi R, Nayil K, Rafiq D, Kirmani A, Salim O, Mustafa F, Aimen A, Khursheed S, Bashir S, Shafi S, Ramzan A. Clinicopathological characteristics of meningiomas: Experience from a tertiary care hospital in the Kashmir Valley. Asian J Neurosurg [serial online] 2019 [cited 2019 Mar 20];14:41-6. Available from: http://www.asianjns.org/text.asp?2019/14/1/41/252596
| Introduction|| |
Meningiomas comprise 15%–20% of all primary intracranial tumors., They are twice as common in the female as in the male population, but a reverse male-to-female preponderance of 3:1 has been reported in the malignant form. The incidence increases with age with peak incidence between the ages of 40 and 60 years. A slight drop after the 8th decade has been noted. They are generally benign tumors, and most patients are cured after surgery and remain free of recurrence. However, some tumors behave in a more aggressive fashion, and patients develop local recurrence or metastasis. Histopathologically, meningiomas currently are separated into three grades, i.e., benign (ordinary) meningioma, atypical meningioma, and anaplastic (malignant) meningioma, that intend to reflect the clinical behavior of the tumors. In completely excised tumors, the 5-year recurrence rate for patients with benign meningiomas is 21%, and the rates for patients with atypical and anaplastic meningiomas range between 38% and 78%, respectively.,
| Patients and Methods|| |
This is a retrospective study conducted in the Departments of Pathology and Neurosurgery at Sheri-I-Kashmir Institute of Medical Sciences, Kashmir, India. The study period was from May 2003 to April 2014, a period of 11 years. All the patients diagnosed as meningiomas in our department were included in the study. The parameters analyzed included age, gender, location of tumor on imaging, histopathological subtype, and grade of tumor according to the 2007 WHO classification. All the cases were reviewed histologically by a single neuropathologist. In doubtful and high-grade lesions, special stains such as reticulin, phosphotungistic acid hematoxylin, and immunohistochemistry were used. Patients were followed up on outpatient basis in the Department of Neurosurgery. As per the departmental protocol, serial contrast computed tomography (CT) scans were performed at 1, 2, 5, and 10 years of surgery. Other than this, patients who presented with raised intracranial pressure symptoms or new onset neurodeficits were also subjected to contrast CT. There were three in-hospital mortalities and 1-year follow-up was available in 237, 2-year in 211, 5-year in 186, and 10-year in 83 patients.
| Results|| |
A total of 254 patients were included in the study. Overall, we had 170 females and 84 males; the ratio was 2:1, of which 205 (80.7%) were brain meningiomas and 49 (19.3%) were spinal. Location was supratentorial in 192 (75.6%) patients, infratentorial in 13 (5.1%), and spinal in 49 (19.3%) patients. Meningothelial meningioma was most common histological type (41.33%, 105/254), followed by transitional (18.50%, 47/254) and psamommatous (11.81%) [Table 1]. The WHO Grade I was seen in 229 (90.2%) patients, 14 (5.5%) had Grade II, and 11 (4.3%) had Grade III tumors [Table 2].
Of 205 patients, 129 (60%) were female and 85 (40%) were male. Most of our patients were in the 4–6th decade of life with age range of 5–73 years. Only 5 (0.02%) patients were in the pediatric age group. On the correlation of gender ratio with age, we found that females predominated males in the 4th, 5th, and 6th decade and this predominance is less pronounced in elderly and pediatric patients. Convexity meningioma was the most common subtype of meningioma, followed by parasagittal [Table 3] and [Figure 1].
|Figure 1: Magnetic resonance imaging brain shows convexity (a), parasagittal (b), anterior cranial base (c), and intraventricular meningiomas (d)|
Click here to view
Meningothelial meningioma was the most common histological type (41.9%), followed by transitional (20.9%), fibroblastic (10.7%), psamommatous (6.8%), and angiomatous (5.3%) [Table 3].
The WHO Grade I was seen in 180 (87.8%) patients, 14 (6.8%) had Grade II, and 11 (5.4%) had Grade III tumors [Table 2]. Similarly, we found that higher grade WHO Grade II and III meningiomas are more common in males as opposed to Grade I lesions which are more common in females, and the difference was statistically significant (P = 0.0084) [Table 4].
There were ten patients who had recurrences with age ranging from 24 to 65 years, five patients were male and five were female. The mean time taken for recurrence to develop was 4.7 years ranging from 1 to 9 years; six recurrences took place within 5 years of surgery and 4 within >5–10 years. We did not encounter recurrence after 10 years [Figure 2]. On recurrence, four patients had WHO Grade I, 5 had Grade II, and 1 had Grade III lesions. On studying the previous grade, we found that seven cases had Grade I, 2 had Grade II, and 1 had Grade III lesions. Grade II and Grade III lesions did not change their grade on recurrence in our study, but out of seven Grade I tumors, three cases morphed to higher grade (Grade II) [Table 5]. On analyzing cases of recurrence, we noticed a statistically significant relation with Simpson grade of excision and the WHO histopathological grade [Table 6] and [Table 7].
|Figure 2: Kaplan–Meier survival analysis shows the pattern of recurrence with time|
Click here to view
Of 49 patients, 46 (94%) patients were female and only 3 (6%) were male. Most of our patients presented in the 4–6th decade. We did not notice any pediatric patient with spinal meningiomas in our study. All the lesions were intradural and extramedullary. Dorsal spine (69.57%) was the most common site, followed by cervical (15.22%), cervicodorsal (10.87%), dorsolumbar (2.17%), and lumbar (2.17%). Meningothelial meningiomas (38.8%) were the most common histological type, followed by psammomatous (32.6%) and transitional (8.2%) [Table 1]. All the cases were WHO Grade I lesions [Table 2] and we did not note any recurrence in spine.
| Discussion|| |
Meningiomas are common tumors of the central nervous system that originate from the meningeal coverings of the spinal cord and the brain. Although the cell of origin has yet to be proven, meningiomas are probably derived from arachnoid cap cells. These cells form the outer layer of the arachnoid mater, and arachnoid villi show a striking cytological similarity to meningioma tumor cells. Meningiomas comprise 15%–20% of all primary intracranial tumors.,
These tumors are the most commonly reported in elderly patients with a peak incidence in the 7th decade of life. Nonetheless, they also occur in children. Meningiomas of the first two decades of life are distinctly less common, with a corresponding incidence of 1%–4%. In our study, the peak was seen in the 4–6th decade of life. Only five of our patients presented in the pediatric age group of 18 years or less. There is a clear bias toward women with a female: male ratio of about 2:1. Spinal meningiomas have an even greater predilection for females. In our study, the female: male ratio for spinal meningiomas was 15.3:1. The vast majority of meningiomas arise intracranial, intraspinal, or orbital locations. Intraventricular and epidural examples are uncommon. Within the cranial cavity, most meningiomas occur over the cerebral convexities and in the parasagittal area in association with the falx and venous sinus. Although they can potentially occur at any site in the meninges, about 90% are supratentorial and 10% are infratentorial. Uncommonly sited tumors include intraosseous meningiomas and extraneuraxial meningiomas. Meningiomas have also been reported in the lungs, mediastinum, and adrenal gland. We did not notice any extraneuraxial meningioma in our series. Spinal meningiomas occur less frequently than intracranial ones and account for approximately 7.5%–12.7% of all meningiomas., We observed 80.7% and19.3% cranial and spinal meningiomas, respectively. Most of our meningiomas were located over cerebral convexities followed by parasagittal meningiomas. Supratentorial meningiomas were seen in 75.6% and infratentorial in 5.1%. We observed one case of primary intraosseous meningiomas.
The most frequent location of spinal meningiomas is the thoracic region (67%–84%) followed by the cervical spine (14%–27%) and only rarely in the lumbar spine (2%–14%).,,,,,,, In spine, all our cases were intradural extramedullary. Most spinal meningiomas occurred in the thoracic region in our study.
Meningiomas are usually solitary but can be multiple. Rarely, meningiomas may grow as a flat, carpet-like mass, a pattern termed “en plaque meningioma.” We noticed one such case. In our study, we noticed only three cases of multiple meningiomas. All the 49 spinal meningiomas were WHO Grade I. Among brain meningiomas, 87.8% of cases were Grade I lesions, 6.8% Grade II, and 5.4% Grade III lesions [Table 2] which are consistent with world literature.,,,,, [Figure 3] Meningothelial, psammomatous, transitional, and fibroblastic meningiomas were the most common histological subtypes.
|Figure 3: (a) Microphotograph showing a whorling pattern in a fibroblastic meningioma (H and E, ×200). (b) Microphotograph showing clear cells in a clear cell meningioma (H and E, ×200). (c) Pleomorphic tumor cells with mitotic figures in an anaplastic meningioma (H and E, ×400). (d) Microphotograph showing papillary arrangement of cells in a papillary meningioma (H and E, ×200)|
Click here to view
Histopathology of the tumors in the pediatric population varies from those in the adult population. Overall, most series have shown a high incidence of atypical and anaplastic meningiomas in children as compared to the adult population. We in our series had only five children, two had rhabdoid and one each had anaplastic, meningothelial, and psammomatous meningioma. Overall in our series, 7.3% had an atypical and 2.9% had anaplastic histopathology. Meningiomas are predominantly seen in females. Mahmood et al. and Alvarez have reported male predominance for atypical and malignant meningiomas. Jääskeläinen et al. have reported an equal distribution for males and females. In our study, male: female ratio of 13:2 was seen in atypical meningiomas whereas equal gender distribution was seen in anaplastic meningiomas.
Meningiomas recur and some histological variants of meningioma are more likely to recur. While benign meningiomas have recurrence rates of about 7%–25%, atypical meningiomas recur in 29%–52% of cases, and anaplastic meningiomas at rates of 50%–94%., Malignant histopathological features are associated with shorter survival times, one series reporting a median survival of <2 years. In our 11-year study, only 10 (3.94%) cases were recurrent tumors. Several studies have reported higher recurrence rates for males than for females.,,, Nakasu et al. and several other authors found no association between tumor development in young patients (<40 years) and a high likelihood of recurrence. However, there also is evidence in the literature wherein a significant difference between age and recurrence has not been found., In our study, we found a definite influence of gender and age on recurrence. Pediatric (<18 years) and elderly population (>60 years) constituted 50% of our recurrent tumors, thus signifying the increased incidence of recurrence at extremes of age. We, however, did not notice any role of gender on the recurrence pattern. We had an equal number of males and females in the recurrence group. When meningiomas recur, progression to a higher histological grade is relatively uncommon., When this does occur, the change is almost always by only one grade, even with multiple recurrences. In our study, of ten cases who showed recurrence, seven cases showed only recurrence but no progression to higher grade and three cases showed recurrence with progression by one grade. There is complete agreement in the literature that radical surgery is one of the positive factors influencing the prognosis of benign and malignant meningiomas., The Simpson grading system has been the best-accepted predictor of recurrence since publication of Simpson's landmark article in 1957.
In our study, of ten cases which recurred, the histopathological examination of these recurrent tumors showed that four were WHO Grade I, 5 were Grade II, and 1 was Grade III lesion [Table 5]. When we studied their Simpson grade of excision, we found that 1 case had Grade I, seven cases had Grade II, and two cases had Grade III excision [Table 6]. Hence, in our study, we concluded that histological grade is not only the predictor of recurrence but Simpson grade of excision also has a considerable influence on recurrence pattern.
| Conclusion|| |
Meningiomas are benign tumors which are more common in females. The supratentorial location is more common than infratentorial, pediatric meningiomas are aggressive, and recurrence of meningiomas depends on the histological grade and Simpson grade of excision.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Ayerbe J, Lobato RD, de la Cruz J, Alday R, Rivas JJ, Gómez PA, et al.
Risk factors predicting recurrence in patients operated on for intracranial meningioma. A multivariate analysis. Acta Neurochir (Wien) 1999;141:921-32.
Coke CC, Corn BW, Werner-Wasik M, Xie Y, Curran WJ Jr. Atypical and malignant meningiomas: An outcome report of seventeen cases. J Neurooncol 1998;39:65-70.
Sutherland GR, Florell R, Louw D, Choi NW, Sima AA. Epidemiology of primary intracranial neoplasms in Manitoba, Canada. Can J Neurol Sci 1987;14:586-92.
Louis DN, Ohgaki H, Otmar DW, Cavenee WK, Burger PC, Jouvet A, et al.
The 2007 WHO classification of tumors of the central nervous system. Acta Neuropathol 2007;114:97-109.
Jääskeläinen J, Haltia M, Servo A. Atypical and anaplastic meningiomas: Radiology, surgery, radiotherapy, and outcome. Surg Neurol 1986;25:233-42.
McCarthy BJ, Davis FG, Freels S, Surawicz TS, Damek DM, Grutsch J, et al.
Factors associated with survival in patients with meningioma. J Neurosurg 1998;88:831-9.
Riemenschneider MJ, Perry A, Reifenberger G. Histological classification and molecular genetics of meningiomas. Lancet Neurol 2006;5:1045-54.
Germano IM, Edwards MS, Davis RL, Schiffer D. Intracranial meningiomas of the first two decades of life. J Neurosurg 1994;80:447-53.
Solero CL, Fornari M, Giombini S, Lasio G, Oliveri G, Cimino C, et al.
Spinal meningiomas: Review of 174 operated cases. Neurosurgery 1989;25:153-60.
Gottfried ON, Gluf W, Quinones-Hinojosa A, Kan P, Schmidt MH. Spinal meningiomas: Surgical management and outcome. Neurosurg Focus 2003;14:e2.
Khursheed N, Rumana M, Ramzan A. Primary intraosseous meningioma-case of the week. AJNR Am J Neuroradiol 2012:e303-4.
King AT, Sharr MM, Gullan RW, Bartlett JR. Spinal meningiomas: A 20-year review. Br J Neurosurg 1998;12:521-6.
Klekamp J, Samii M. Surgical results for spinal meningiomas. Surg Neurol 1999;52:552-62.
Levy WJ Jr., Bay J, Dohn D. Spinal cord meningioma. J Neurosurg 1982;57:804-12.
Roux FX, Nataf F, Pinaudeau M, Borne G, Devaux B, Meder JF. Intraspinal meningiomas: Review of 54 cases with discussion of poor prognosis factors and modern therapeutic management. Surg Neurol 1996;46:458-63.
Saito T, Arizono T, Maeda T, Terada K, Iwamoto Y. A novel technique for surgical resection of spinal meningioma. Spine (Phila Pa 1976) 2001;26:1805-8.
Younis GA, Sawaya R, DeMonte F, Hess KR, Albrecht S, Bruner JM. Aggressive meningeal tumors: Review of a series. J Neurosurg 1995;82;17-27.
Khursheed N, Rumana M, Ramzan A, Abrar W. En-plaque spinal meningioma: A rare entity. Neurosurg Q 2013;23:61-3.
Burger PC, Scheithauer BW, Vogel FS. Surgical Pathology of the Nervous System and Its Coverings. 3rd
ed. London: Churchill Livingstone; 1991. p. 307-571.
Keppes JJ. Meningiomas-Biology, Pathology and Differential Diagnosis. New York: Masson Publishing; 1982. p. 150-522.
Lantos PL, Vanden Berg SR, Kleihues P. Tumours of the nervous system. In: Graham DI, Lantos PL, editors. Greenfield's Neuropathology. 6th
ed. London: Arnold; 1996. p. 583-879.
Mehta N, Bhagwati S, Parulekar G. Meningiomas in children: A study of 18 cases. J Pediatr Neurosci 2009;4:61-5.
] [Full text]
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 1997;86:793-800.
Mahmood A, Caccamo DV, Tomecek FJ, Malik GM. Atypical and malignant meningiomas: A clinicopathological review. Neurosurgery 1993;33:955-63.
Perry A, Gutmann DH, Reifenberger G. Molecular pathogenesis of meningiomas. J Neurooncol 2004;70:183-202.
Perry A, Scheithauer BW, Stafford SL, Lohse CM, Wollan PC. “Malignancy” in meningiomas: A clinicopathologic study of 116 patients, with grading implications. Cancer 1999;85:2046-56.
Perry A, Stafford SL, Scheithauer BW, Suman VJ, Lohse CM. Meningioma grading: An analysis of histologic parameters. Am J Surg Pathol 1997;21:1455-65.
Boldrey E. The meningiomas. In: Minckler J, editor. Pathology of the Nervous System. New York: McGraw-Hill; 1971. p. 2125-44.
Gupta PK, Sastry Kolluri VR, Das S, Chandra Mouli BA, Narayana Swamy KS, Das BS. Recurrences in meningioma after surgery. Acta Neurochir (Wien) 1989;100:104-7.
Mahmood A, Qureshi NH, Malik GM. Intracranial meningiomas: Analysis of recurrence after surgical treatment. Acta Neurochir (Wien) 1994;126:53-8.
Nakasu S, Nakasu Y, Nakajima M, Matsuda M, Handa J. Preoperative identification of meningiomas that are highly likely to recur. J Neurosurg 1999;90:455-62.
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 1986;26:461-9.
Adegbite AB, Khan MI, Paine KW, Tan LK. The recurrence of intracranial meningiomas after surgical treatment. J Neurosurg 1983;58:51-6.
Modha A, Gutin PH. Diagnosis and treatment of atypical and anaplastic meningiomas: A review. Neurosurgery 2005;57:538-50.
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.
Salmon I, Kiss R, Levivier M, Remmelink M, Pasteels JL, Brotchi J, et al.
Characterization of nuclear DNA content, proliferation index, and nuclear size in a series of 181 meningiomas, including benign primary, recurrent, and malignant tumors. Am J Surg Pathol 1993;17:239-47.
Demaerel P, Wilms G, Lammens M, Marchal G, Plets C, Goffin J, et al.
Intracranial meningiomas: Correlation between MR imaging and histology in fifty patients. J Comput Assist Tomogr 1991;15:45-51.
Simpson D. The recurrence of intracranial meningiomas after surgical treatment. J Neurol Neurosurg Psychiatry 1957;20:22-39.
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7]