Meningiomas account for approximately 4% of all
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1 Intraorbital Meningiomas A Pathologic Review Using Current World Health Organization Criteria Deepali Jain, MD; Katayoon B. Ebrahimi, MD; Neil R. Miller, MD; Charles G. Eberhart, MD, PhD N Context. Meningiomas represent approximately 4% of all intraorbital tumors and can arise from the optic nerve or extend into the orbit from adjacent structures. Objective. To examine a cohort of intraorbital meningiomas and use the current World Health Organization (WHO) scheme to assess the effect of changes to the classification of tumors at this site. Design. The histopathology and clinical findings of intraorbital meningiomas resected between 1968 and 2008 at our institution were reviewed according to the WHO 2007 classification scheme. Results. A total of 51 intraorbital meningiomas were reviewed. The mean age at presentation was 45 years, but 5 tumors arose in children. Two patients were known to have neurofibromatosis type 2, and 1 had inherited retinoblastoma. Orbital meningiomas were more frequently encountered in women (30 cases) than in men (21 cases). In 21 patients, the tumor was associated with the optic nerve. The most common (25 of 51 tumors; 49%) histopathologic subtype was meningothelial. Most (47 of 51; 92%) of the tumors were WHO grade I. Four tumors (8%) were WHO grade II, with 4 or more mitotic figures per 10 high-power fields, brain invasion, chordoid histology, or a combination of these features. Conclusions. Intraorbital meningiomas were most frequently of the meningothelial or transitional subtypes and were WHO grade I. One relatively common intracranial subtype, fibrous meningioma, was not encountered. The percentage of WHO grade II tumors in the orbit (8%) is similar to that reported for intracranial tumors using the current grading scheme. (Arch Pathol Lab Med. 2010;134: ) Meningiomas account for approximately 4% of all intraorbital masses and fall into 2 broad categories. 1 Primary lesions derive from cells lining the intraorbital or, less commonly, intracanalicular segments of the optic nerve. They represent the most common tumors of the optic nerve sheath. 2 In one series of 1264 orbital lesions, 29 (2%) were primary optic nerve sheath meningiomas. 1 Secondary intraorbital meningiomas arise intracranially and subsequently extend into the orbit. 3,4 These tumors most often arise from the sphenoid wing, but additional sites include clinoid, planum sphenoidale, frontoparietal area, and olfactory groove. 5 Some secondary tumors are quite large, and both orbits can be involved. In the same single-institution series of 1264 tumors referred to above, 24 (2%) were secondary meningiomas. 1 Intraorbital meningiomas are identified most frequently in middle-aged women. 2 Clinical features vary depending on the site of the tumor, with painless, progressive visual loss representing the most common presenting complaint in patients whose tumors arise from the nerve sheath. 6 Accepted for publication August 11, From the Departments of Pathology (Drs Jain and Eberhart), Ophthalmology (Drs Ebrahimi, Miller, and Eberhart), Neurosurgery (Dr Miller), and Oncology (Dr Eberhart), Johns Hopkins Medical Institutions, Baltimore, Maryland. The authors have no relevant financial interest in the products or companies described in this article. Reprints: Charles G. Eberhart, MD, PhD, Departments of Ophthalmology and Oncology, Johns Hopkins University School of Medicine, 720 Rutland Ave, Ross Bldg 558, Baltimore, MD ( ceberha@jhmi.edu). Proptosis or other mass effects are commonly observed in secondary intraorbital meningioma cases. 1 Treatment options have traditionally been limited for primary tumors, but recently, fractionated radiotherapy, and particularly stereotactic or 3-dimensional conformal radiation, has been reported to result in an excellent shortterm and long-term visual prognosis 6,7 (N.R.M., unpublished data, 2009). A number of meningioma subtypes have been proposed through the years, and the current (2007) World Health Organization (WHO) classification includes 15 named entities. 8 The criteria for grading of meningiomas have also varied and were significantly changed in the 2000 update of the WHO classification scheme. These changes were largely based on several reports by Perry and colleagues, 9,10 in which the relationship between pathologic subtype, mitotic index, invasive capacity, and other microscopic factors was correlated with tumor recurrence. Some of the more significant changes affecting tumor grade include classifying (1) meningiomas showing central nervous system invasion as grade II rather than grade III, (2) meningiomas with 4 or more mitotic figures per 10 high-power fields (HPFs) as grade II, (3) clear cell and chordoid meningiomas as grade II, (4) papillary and rhabdoid meningiomas as grade III, and (5) tumors with 20 or more mitotic figures per 10 HPFs as grade III. 8 Intraorbital meningiomas have previously been reported to have histologic features similar to those of intracranial ones, with meningothelial and transitional types encountered most commonly 11 ; however, most of the studies in which pathologic subtype and grade was 766 Arch Pathol Lab Med Vol 134, May 2010 WHO Grading of Intraorbital Meningiomas Jain et al
2 reported in detail were performed before the updates to the WHO classification in Herein, we describe the histopathologic subtypes and WHO grades of 51 intraorbital meningiomas using the current classification scheme. When applying these newer criteria, we found that more tumors were classified as grade II, predominantly because of their increased mitotic activity. MATERIALS AND METHODS A retrospective review of the pathology records of the Neuropathology and Eye Pathology Laboratories at the Johns Hopkins Hospital (Baltimore, Maryland) was performed with institutional review board approval, and 51 intraorbital meningiomas diagnosed between 1968 and 2008 were identified. This included 3 autopsies, 5 enucleations, 2 exenterations, 38 resections, and 3 biopsies. Available clinical data, including patient age, sex, and imaging and surgical findings were also reviewed. Hematoxylin-eosin stained slides from all cases were examined by 2 neuropathologists (D.J. and C.G.E.) using the WHO 2007 classification scheme. RESULTS A total of 51 intraorbital meningiomas were reviewed (Table 1), with clinical follow-up information available in 16 cases (31%). The mean age at presentation was 45 years (range, 8 96 years); 5 tumors arose in children/adolescents, aged 8 to 15 years. Two patients had neurofibromatosis type 2 (NF-2), and 1 had inherited retinoblastoma with prior radiation therapy including the orbit and brain. No other patients were known to have received radiation therapy. Intraorbital meningiomas were more frequently encountered in women (30 cases; 59%) than in men (21 cases; 41%). In 21 patients (13 women, 8 men), the tumor was associated with the optic nerve. All of these tumors were unilateral, except for a case of NF-2 (case 24), in which there were bilateral tumors. In the remaining 30 patients, the optic nerve was not known to be involved, and the lesions were considered secondary. The most common (25 of 51 tumors; 49%) histopathologic subtype overall was meningothelial, with an additional 22 tumors (43%) being classified as transitional. Two tumors (4%) were atypical meningiomas with increased mitotic activity. One tumor (2%) was angiomatous (Figure, A), and 1 (2%) had a predominantly chordoid growth pattern (Figure, B). In addition to this classification by subtype, focal microcystic or angiomatous changes were present in 2 tumors each, and focal secretory change in 1. Most (47 of 51; 92%) of the meningiomas were WHO grade I. Four tumors (8%) were classified as WHO grade II (atypical), 2 in men and 2 in women. Three of these cases (21, 50, and 51) contained 4 or more mitotic figures per 10 HPFs (Figure, C). Case 51, in addition to showing elevated mitotic activity, was of the chordoid variant in which tumor cells formed elongated strands similar to those seen in chordomas. This tumor also showed brain invasion. The fourth tumor (case 35) was classified as WHO grade II because of brain invasion in the intracranial region in which it arose. Only one grade II orbital meningioma behaved in an aggressive fashion. That patient (case 50) died with progressive tumor 1 month after the diagnosis. In contrast, the patient presented as case 21 was tumor-free 30 years after diagnosis and ultimately died of heart disease. In case 35, the patient does not show radiographic evidence of tumor recurrence at last follow-up 2 years following the initial surgery. Finally, in case 51, the most recent radiographic images, taken one year after surgery and radiotherapy, showed only some cerebral edema, which is more likely due to treatment effect than recurrent tumor. The other microscopic features we assessed also lacked clear associations with poor outcome. Two cases (8 and 20) showed optic nerve invasion (Figure, D), but it is not clear whether that is equivalent to brain invasion in justifying an increased grade. Follow-up was available in case 20, and that patient remains disease-free 28 years after diagnosis. The second case with optic nerve invasion was an autopsy. Infiltration of dura, bone, muscle (Figure, E), orbital fat, lacrimal gland (Figure, F), choroid, or sclera was observed microscopically in 21 cases, but none of these features are thought to be prognostically significant. In some of these specimens, multiple tissues were found to be invaded by tumor (Table 1). Invasion of choroid and sclera was only detected in 2 cases, which were enucleated. One of these infiltrating tumors (case 23) recurred 12 years after initial resection. Two patients (cases 24 and 50) died of their disease 1 month and 9 years after diagnosis, respectively. However, the other 3 patients in this group with available follow-up had no evidence of tumor regrowth 2 to 8 years after initial resection. DISCUSSION Meningiomas are generally benign, WHO grade I tumors, associated with prolonged, recurrence-free survival, but a subset are clinically more aggressive. The WHO classification scheme attempts to predict which tumors are most likely to recur, placing lesions with worrisome histopathologic features into grade II (atypical) or grade III (malignant) categories. 8 This grading system was developed primarily through clinicopathologic correlations using intracranial meningiomas, and the current WHO classification has not been applied to a large series of intraorbital tumors. We, therefore, reviewed the pathology of all intraorbital meningiomas resected at our institution in 40 years, using WHO criteria to grade them. The overall distribution of intraorbital meningioma subtypes in our series was similar to that previously reported at this site, with the meningothelial (19%), mixed meningothelial/transitional (31%), and transitional (50%) variants accounting for almost all of the tumors Consistent with previous reports, psammomatous and fibroblastic variants, both relatively frequent intracranially, were not encountered in the orbit in our series; however, the overall frequencies of grade I (92%), and grade II (8%) intraorbital meningiomas were roughly similar to those reported for primarily intracranial series (Table 2). 9,14 We did not identify any grade III intraorbital meningiomas. In contrast to previous reports concerning intracranial meningiomas, 9 we did not observe higher histologic grade associated with men. Indeed, 2 of the 4 patients (50%) with atypical orbital meningiomas in our series were women. Another interesting finding was the association of angiomatous changes with higher grade in one case and with optic nerve invasion in 2 others. Angiomatous change has not been associated with increased biologic aggressiveness in intracranial meningioma. 8 We identified optic nerve invasion in 2 of the cases in our series, but it is not clear whether that is equivalent to intracranial brain invasion in prognostic effect. The meningothelial pial septae form an extensive network within the optic nerve, and meningioma cells should be able to infiltrate the nerve parenchyma along these preexisting pathways without having to extend invasive Arch Pathol Lab Med Vol 134, May 2010 WHO Grading of Intraorbital Meningiomas Jain et al 767
3 Case No. Table 1. Age, y/sex Site Diagnosis fingers unsupported by nonneoplastic meningothelial tissue. This contrasts to some degree with the situation in the brain, in which tumor extension into neural tissue has fewer paths to follow, as the Virchow-Robin spaces created by meningothelial cells surrounding larger penetrating vessels are not as densely spaced as pial septae in the optic nerve. Nevertheless, previous reports of intraorbital meningiomas have, in general, not increased tumor grade because of invasion of the optic nerve, although the WHO classification and Armed Forces Institute of Pathology Tumor Pathology Series do not explicitly deal with this issue. 6,8,11,15 In our series, 2 cases showed unequivocal optic nerve invasion. One of these also Clinicopathologic Features of 51 Cases of Orbital Meningioma WHO Grade Other Features 1 20/M ON Transitional I Dura invasion 2 53/F ON Transitional I Dura invasion 3 32/M ON Transitional I 4 51/F ON Transitional I 5 58/F ON Transitional I Bone, dura, nerve sheath invasion 6 73/F ON Transitional I Focal microcystic 7 28/M ON Transitional I Choroidal invasion 8 71/F ON Transitional I ON invasion, 1 mitosis/10 HPFs, focal angiomatous 9 57/F ON Meningothelial I 10 42/F ON Meningothelial I 11 48/F ON Meningothelial I 12 8/F ON Meningothelial I 13 14/F ON Meningothelial I 14 29/M ON Meningothelial I 15 17/M ON Meningothelial I Muscle invasion 16 57/F ON Meningothelial I 17 62/M ON Meningothelial I 18 54/F ON Meningothelial I Multiple small foci of tumor 19 96/M ON Meningothelial I 20 28/M ON Angiomatous I ON invasion, 3 mitoses/10 HPFs 21 37/F ON Atypical with angiomatous II 5 mitoses/10 HPFs features 22 40/F Orbit Transitional I Muscle invasion 23 21/F Orbit Transitional I Bone invasion 24 28/M Orbit Transitional I NF-2, bilateral, muscle, lacrimal gland and bone invasion 25 61/F Orbit Transitional I Bone invasion 26 60/F Orbit Transitional I 27 71/M Orbit Transitional I 28 31/F Orbit Transitional I Focal secretory features; bone and dura invasion 29 13/F Orbit Transitional I Muscle invasion 30 78/F Orbit Transitional I Orbital fat invasion 31 16/M Orbit Transitional I 32 27/M Orbit Transitional I 33 52/F Orbit Transitional I 34 15/M Orbit Transitional I NF /F Orbit Transitional II Brain, bone and dura invasion, 1 mitosis/10 HPFs 36 44/F Orbit Meningothelial I Bone invasion 37 48/F Orbit Meningothelial I Muscle, bone, and lacrimal gland invasion, focal microcystic 38 52/F Orbit Meningothelial I Muscle and bone invasion 39 45/M Orbit Meningothelial I 40 43/F Orbit Meningothelial I 41 43/F Orbit Meningothelial I Bone invasion 42 55/F Orbit Meningothelial I 43 73/F Orbit Meningothelial I Bone invasion 44 15/M Orbit Meningothelial I Invasion of perivascular sheaths in sclera 45 19/F Orbit Meningothelial I 46 71/M Orbit Meningothelial I 47 62/M Orbit Meningothelial I Muscle invasion 48 34/M Orbit Meningothelial I 49 47/M Orbit Meningothelial I 50 75/M Orbit Atypical II 6 mitoses/10 HPFs, dura invasion 51 43/M Orbit Chordoid II Prior radiation for retinoblastoma, 4 mitoses/10 HPFs, brain invasion Abbreviations: HPFs, high-power fields; NF, neurofibromatosis; ON, optic nerve; WHO, World Health Organization. displayed a somewhat increased proliferative index (3 mitotic figures per 10 HPFs), but neither had additional clinical or pathologic features that seemed to justify classification as grade II. We have access to clinical follow-up in one of these cases, and the patient is doing well 28 years after diagnosis. Overall, it seems to us most appropriate not to equate optic nerve invasion with brain invasion for the purposes of grading. Intraorbital meningiomas can also invade other ocular structures, including, rarely, the optic disk, retina, or choroid. 6 We found choroidal invasion with overlying retinal gliosis in one case. Additional examples of tumor spread in our series include invasion of the lacrimal gland 768 Arch Pathol Lab Med Vol 134, May 2010 WHO Grading of Intraorbital Meningiomas Jain et al
4 A, Angiomatous variant of meningioma with interspersed thick-walled vascular channels (arrow). B, Chordoid meningioma with tumor cells arranged in cords, alternating with bluish myxoid stroma. C, A World Health Organization grade II, atypical meningioma with mitotic activity (arrow), highlighted in the inset (arrow). D, Meningothelial tumor cells invade optic nerve (ON) parenchyma and also proliferate in the subarachnoid space. Invasion among bundles of skeletal muscle (E) or into lacrimal gland (F, asterisk) was also seen in some cases (hematoxylin-eosin, original magnifications 3400 [A through C and inset], 340 [D], 3200 [E], and 3100 [F]). in 2 cases (one NF-2-associated) and infiltration of the dura, orbital bone, muscle, scleral canals or fat in 19 sporadic cases. Two grade II lesions also showed dural invasion. The age at presentation of patients with optic nerve meningiomas is typically younger than for intracranial meningiomas. 4 Childhood optic nerve sheath meningiomas are generally associated with NF-2 and have been reported to be more aggressive than those in adults. 16 Neurofibromatosis type 2 associated meningiomas are often multicentric, and patients may have separate intracranial and intraorbital tumors. 17 The incidence of optic nerve sheath meningiomas in patients with NF-2 is reported to be 2 to 8%. 16 Neurofibromatosis type 2 gene mutations predominantly occur in transitional and fibroblastic meningiomas, whereas the meningothelial variant is less affected. 18 Our 2 NF-2 associated cases also displayed a transitional subtype, with one recurring twice during the period of 7 years. Both of the patients in these cases died of their disease, at 4 and 9 years after diagnosis, respectively. One grade II meningioma in our series was of the chordoid subtype and arose in a patient with bilateral, inherited retinoblastoma. It was a secondary lesion arising in a field of prior radiation and was associated with significant intracranial disease and brain invasion. Chordoid meningiomas have an increased potential for Variables Table 2. Comparison of Intracranial and Intraorbital Meningiomas Intracranial Meningiomas in Perry et al, Intracranial Meningiomas in Yao, Intraorbital Meningiomas in Present Study, 2009 Patients, No Mean age, y 57 (median) F:M ratio 2:1 1.6:1 1.4:1 Most common histologic type, % Meningothelial, 63.5 Meningothelial, 41 Meningothelial, 49 Grade I, % Grade II, % Grade III, % Association of histologic grade to sex M, higher grade No association to grade; however, M associated with recurrence No association Arch Pathol Lab Med Vol 134, May 2010 WHO Grading of Intraorbital Meningiomas Jain et al 769
5 recurrence and are, therefore, considered grade II. 8 This tumor also had an elevated proliferative index, with 4 mitotic figures per 10 HPFs. To our knowledge, chordoid meningiomas have not been reported previously in the orbit. In summary, intraorbital meningiomas are most frequently either meningothelial or transitional subtypes and WHO grade I. The percentage of grade I and II tumors in the orbit is similar to that reported for intracranial tumors using the current WHO grading scheme. Most cases now have an increased grade because of elevated mitotic activity, a relatively new addition to the WHO classification scheme. Invasion of the optic nerve is identified in some cases, but this alone seems insufficient to justify diagnosis of a grade II lesion. In addition, of the 4 higher grade cases in our series, only one tumor recurred rapidly, suggesting that grade II features in the current WHO scheme are only occasionally associated with poor clinical outcomes in orbital meningioma patients References 1. Shields JA, Shields CL, Scartozzi R. Survey of 1264 patients with orbital tumors and simulating lesions: the 2002 Montgomery Lecture, part 1. Ophthalmology. 2004;111(5): Miller NR. Primary tumours of the optic nerve and its sheath. Eye. 2004; 18(11): Wilson WB. Meningiomas of the anterior visual system. Surv Ophthalmol. 1981;26(3): Dutton JJ. Optic nerve sheath meningiomas. Surv Ophthalmol. 1992;37(3): Turbin RE, Pokorny K. Diagnosis and treatment of orbital optic nerve sheath meningioma. Cancer Control. 2004;11(5): Eddleman CS, Liu JK. Optic nerve sheath meningioma: current diagnosis and treatment. Neurosurg Focus. 2007;23(5):E4. 7. Andrews DW, Faroozan R, Yang BP, et al. Fractionated stereotactic radiotherapy for the treatment of optic nerve sheath meningiomas: preliminary observations of 33 optic nerves in 30 patients with historical comparison to observation with or without prior surgery. Neurosurgery. 2002;51(4): Perry A, Louis DN, Scheithauer BW, Budka H, von Deimling A. Meningiomas. In: Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, eds. WHO Classification of Tumours of the Central Nervous System. 4th ed. Lyon, France: IARC Press; 2007: World Health Organization Classification of Tumours; vol Perry A, Stafford SL, Scheithauer BW, Suman VJ, Lohse CM. Meningioma grading: an analysis of histologic parameters. Am J Surg Pathol. 1997;21(12): 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(9): Saeed P, Rootman J, Nugent RA, White VA, Mackenzie IR, Koornneef L. Optic nerve sheath meningiomas. Ophthalmology. 2003;110(10): Marquardt MD, Zimmerman LE. Histopathology of meningiomas and gliomas of the optic nerve. Hum Pathol. 1982;13(3): Rootman J, Saeed P. Optic nerve meningiomas. In: Rootman J, ed. Diseases of the Orbit: A Multidisciplinary Approach. Philadelphia, PA: JB Lippincott; 1988: Yao YT. Clinicopathologic analysis of 615 cases of meningioma with special reference to recurrence. J Formos Med Assoc. 1994;93(2): Font RL, Croxatto JO, Rao NA. Tumors of the optic nerve and optic nerve head. In: Silverberg SG, Sobin LH, eds. Tumors of the Eye and Ocular Adnexa. Washington, DC, Armed Forces Institute of Pathology; 2006: Atlas of Tumor Pathology; 4th series, fascicle Bosch MM, Wichman WW, Boltshauser E, Landau K. Optic nerve sheath meningiomas in patients with neurofibromatosis type 2. Arch Ophthalmol. 2006; 124(3): Dutton JJ. Optic nerve gliomas and meningiomas. Neurol Clin. 1991;9(1): Lamszus K. Meningioma pathology, genetics, and biology. J Neuropathol Exp Neurol. 2004;63(4): Arch Pathol Lab Med Vol 134, May 2010 WHO Grading of Intraorbital Meningiomas Jain et al
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