Cranial Intraosseous Meningioma: Spectrum of neuroimaging findings with respect to histopathological grades in 65 patients A.T. uran Ilica, Mahmud Mossa-Basha, Elcin Zan, Ami Vikani, Jay J. Pillai, Sachin Gujar, Nafi Aygun, Izlem Izbudak PII: DOI: Reference:
S0899-7071(14)00148-X doi: 10.1016/j.clinimag.2014.05.013 JCT 7635
To appear in:
Journal of Clinical Imaging
Received date: Revised date: Accepted date:
5 December 2013 23 April 2014 28 May 2014
Please cite this article as: uran Ilica AT, Mossa-Basha Mahmud, Zan Elcin, Vikani Ami, Pillai Jay J., Gujar Sachin, Aygun Nafi, Izbudak Izlem, Cranial Intraosseous Meningioma: Spectrum of neuroimaging findings with respect to histopathological grades in 65 patients, Journal of Clinical Imaging (2014), doi: 10.1016/j.clinimag.2014.05.013
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
Cranial Intraosseous Meningioma: Spectrum of neuroimaging findings with
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respect to histopathological grades in 65 patients
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A.Turan Ilica1, Mahmud Mossa-Basha1, Elcin Zan1, Ami Vikani1, Jay J. Pillai1, Sachin Gujar1, Nafi Aygun1, Izlem Izbudak1
Russell H. Morgan Department of Radiology and Radiological Sciences, The Johns Hopkins Medical Institutions, Baltimore, Maryland, USA
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1 The
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Corresponding Author: Izlem Izbudak, M.D. Assistant Professor of Radiology Division of Neuroradiology The Russell H. Morgan Department of Radiology and Radiological Sciences Johns Hopkins Hospital 600 N. Wolfe Street Phipps B-126-B Baltimore, MD 21287 e-mail: [email protected]
ACCEPTED MANUSCRIPT Abstract The aim of this study was to determine various imaging features of intraosseous
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meningiomas (IOMs) and differentiate low grade from high-grade tumors. The
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histopathologic evaluation revealed WHO grade I tumor in 56 (86 %) patients, grade II in 8 (12%) and grade III in 1 (2 %) patient. WHO grade I was considered low grade and II and III were designated as high grade. Hyperostosis was observed most commonly in
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low-grade IOMs. Mixed hyperostotic/lytic pattern with radial bony spiculations, and presence of a scalp mass seem to be more frequently associated with higher grade
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IOMs.
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Abbreviations: IOM= Intraosseous meningioma
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Keywords: Cranium, Hyperostosis, Meningioma, Intraosseous
ACCEPTED MANUSCRIPT Introduction Primary extradural meningiomas are rare, accounting less than 2% of all
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meningiomas. Intraosseous meningiomas ( IOMs) are a subset of primary extradural
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meningiomas and represent about two thirds of all extradural meningiomas(1-3). Osseous involvement by meningiomas may be primary or secondary, but it may be difficult to classify these as either primary or secondary with respect to its origin site,
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based on the neuroimaging appearance, surgical findings or histologic features (3). Based on published data and our experience, we believe such a differentiation cannot
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be definitively made with imaging or histopathology (3-8).
Although several distinct features of IOMs have been described (9,10), to the
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best of our knowledge, cross sectional imaging analyses of IOMs including MRI have not yet been reported. The aim of the present study was to review a series of IOMs to determine various imaging features of IOMs and differentiate low grade from high-grade
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tumors.
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Materials and Methods
After institutional review board approval, the pathology database was queried for
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reports with the key words “intraosseous meningioma” and “meningioma within the bone” from December 2000 to February 2012. From this list, a total of 81 patients were
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identified. Sixteen patients, whose tumor mass within bone was proven to represent secondary osseous invasion according to pathology were excluded. Sixty-five patients whose mean tumor mass within bone was equal to or greater than 50 % of the total mass were included in the study. For all patients, the available clinical records, operative reports and pathology reports were reviewed. Neuroimaging data, including CT and/or MR were retrieved from our picture archiving and communication system (PACS) and were retrospectively analyzed. Although odds ratio associated with meningioma are considerably high for female population, this study aimed to evaluate intraosseous meningioma in general. CT scans were obtained on multidetector CT scanners, including 4, 16 and 64row detectors from Siemens (Siemens AG, Erlangen, Germany), and Toshiba (Toshiba Medical Systems, Otawara, Japan). Images were obtained with helical technique and
ACCEPTED MANUSCRIPT 0.75 mm -1 mm thickness and reconstructed at 3-5-mm-slice thickness and intervals in a soft-tissue and bone algorithm. Further CT parameters were as follows: x-ray tube current = 400 mAs, 120 kVP, and FOV = 24.0 cm x 24.0 cm. Nine patients underwent
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CT with intravenous administration of non-ionic iodinated contrast.
The MRI examinations were performed at either 1.5T or 3T magnet strength on scanners from different manufacturers: Philips (Philips Medical Systems, Best, the
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Netherlands), GE (GE Medical Systems, Milwaukee, Wisconsin), and Siemens (Siemens AG, Erlangen, Germany). The MRI protocol included diffusion-weighted
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images, T1 weighted images, fast spin-echo T2 weighted images, fluid attenuated inversion recovery (FLAIR) images, and contrast enhanced T1 weighted images. All
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patients underwent post contrast imaging after intravenous administration of gadolinium based contrast media. The sagittal T1W sequence was obtained with parameters as follows: range of TRs, 520–696 ms and TEs, 4.6–14 ms; matrix size range from 192 ×
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192 to 512 × 196; FOV range from 190 × 190 mm to 240 × 240 mm; and range of section thickness/spacing from 1/1 to 5/7 mm. The axial T2W sequence was obtained
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with the range of TR, 2500–7000 ms and TE, 83.136–112 ms; matrix size range from 256 × 184 to 448 × 335; FOV range from 159 × 200 mm to 240 × 240 mm; and the
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range of section thickness/spacing from 2/2 to 5/5-mm. FLAIR sequence parameters were the following: TR, 6000 ms; TE, 120 ms; TI, 2000 ms; section thickness, 5 mm;
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FOV, 23 cm; and matrix size, 256 × 256. A neuroradiologist with 8 years of experience in this field (I.I.) and a general radiologist with 7 years of experience (A.T.I.) reviewed all the CT and MR exams retrospectively and noted findings in consensus. They were blinded to the pathologic grade of the IOMs. In the event of disagreement between the two reviewers, a third neuroradiologist with 15 years of experience (N. A.) adjudicated. Image analysis The locations of the meningiomas were divided into three groups: sphenoid ridge (greater
sphenoid
wing),
other
skull
base
regions
and
calvarial
convexity.
Characteristics evaluated on CT included the location of the tumor, bone density
ACCEPTED MANUSCRIPT (hyperostotic, lytic or mixed), and presence of bone expansion, contour irregularity or radial bony spiculations, and dural calcification. Expansion was defined when the bone lesion thickness was greater than the thickness of the adjacent normal calvarial bone.
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Contour irregularity was defined if there were irregular inner or outer calvarial bony
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surfaces instead of normal smooth borders. Radial oriented bony spiculations along the calvarial surface were also noted if present. Dural calcification is defined as a linear high
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density structure above 100 HU along the dural surface subjacent to the IOM on CT. Presence of dural enhancement or an adjacent intracranial dural or extracranial scalp
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soft tissue mass was noted. The osseous characteristics were evaluated using bone window algorithm (400-600 HU window level, 2400-2600 HU window width).
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On MR, the presence of dural enhancement or an adjacent intracranial dural or extracranial soft tissue mass, and adjacent parenchymal edema were evaluated. Dural enhancement was defined as a linear enhancement not thicker than 3 mm. Nodular or
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linear dural based soft tissue enhancement greater than 3 mm was defined as mass. Cerebral edema was defined as present if there is increased T2/FLAIR signal on MR in
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the adjacent parenchyma. To quantify the extent of edema, the distance from the maximum inner edge of region of maximum edema to the nearest point of meningioma
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border was measured in mm. If there was no white matter FLAIR hyperintensity, it was accepted as ‘‘no edema’’. If the white matter FLAIR hyperintensity is less than tumor, it
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was accepted as ‘‘minimal edema’’. If the extension of edema was equal or greater than tumor it was accepted as ‘‘extensive edema’’. Results Of the 65 patients included in the study, 42 had both MR and CT scans, 23 had either MR (n= 12) or CT scan (n=11). The distribution, demographics and WHO grades of the cases are summarized in Table 1. The two reviewers disagreed on only 3 cases and those were evaluated by a third neuoradiologist independently and a final consensus was achieved. Sphenoid ridge and calvarial convexity predominated over the other locations (Fig. 1-3). Most of the calvarial convexity IOMs originated in the frontal or parietal
ACCEPTED MANUSCRIPT region, except 2 occipital lesions. The 8 other skull base lesions included 7 anterior and middle cranial fossa lesions (planum sphenoidale and parasellar region) and 1 posterior skull base (temporal bone) tumor. In patients with cranial convexity lesions, a lump in
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the scalp was the most common clinical presentation, whereas patients with sphenoid
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ridge meningiomas had visual disturbances. Cranial nerve deficits were the chief complaint for the other skull base IOM. The patient with a temporal bone meningioma
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presented with hearing loss.
All meningiomas were classified as Grade I (benign), Grade II (atypical) or Grade
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III (anaplastic/malignant) according to the features set in the World Health Organization classification system (11). WHO grade I was considered low grade and II and III were
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designated as high grade.
Among the higher-grade tumors (grades II and III), 6 were at the convexity, 2
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involved the skull base and 1 lesion was in the sphenoid ridge (Fig. 4). Non sphenoid skull base and convexity IOMs were more commonly higher grade relative to sphenoid
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ridge IOMs.
Lytic lesions were found in 4 (8%) patients (1 sphenoid, 1 convexity and 2 skull
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base), all of which were grade I on the histopathological examination (Fig. 5). Radial spiculations were observed in three cases with higher grades (2 grade II and 1 grade III
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patients) but in none of the low grade lesions. Bone expansion was common in all grades (44/65) but always present in higher grades (9/9).
An association with edema was more prominent in the higher grades (8/8 in grade II and 1/1 in grade III) as compared to lower grades (23/42) among patients who have available MRI exams. Edema extension was minimal in all WHO grade I patients with available MR exams (23/42). There was extensive edema in all WHO grade II and III patients.
Five patients presented with scalp mass: 4 with grade II and 1 with grade III lesions. None of the grade I patients had associated extra cranial scalp mass. The presence of scalp mass was a strong predictor of higher grade.
ACCEPTED MANUSCRIPT The sphenoid ridge was the only location wherein an intraosseous meningioma without an adjacent dural-based mass was observed. Among the 35 sphenoid ridge
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meningiomas, 12 cases had no dural mass, and all were grade I.
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Enhancement of bone was not observed in the hyperostotic IOMs. Whereas all mixed and lytic IOMs enhanced prominently (Fig. 5). The loss of definition in the outer cortex was an additional finding that we observed in 1 grade I calvarial convexity IOM
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(Fig. 6). CT and MR features and related WHO grades of patients were summarized in
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Table 2.
Discussion
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Primary extradural meningiomas are classified as purely extracalvarial (type I), purely calvarial (type II), or calvarial with extracalvarial extension (type III). Based on the site of the tumor, Lang et al. subdivided type II and type III lesions into convexity
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(C) or skull-base (B) forms (1-3). In this study, 53 % of the IOMs were in the sphenoid ridge, 33% in the calvarial convexity and 14% in the skull base. In the literature, the
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corresponding ratios were 70-90% in the sphenoid ridge and 10-28 % in the calvarial convexity (1-3, 9, 12). Meningiomatous cells are known to invade the Haversian canals
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to stimulate osteoblastic activity, which has led to suggestion of the term “hyperostosing” as synonymous with “invading” whenever bone involvement occurs (4,
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8-10). We observed hyperostosis in the majority of the histologically grade I IOMs. Mixed pattern and osteolysis, and radial spiculation were prominent at higher grades in our cohort.
Hyperostosis in the sphenoidal region or other skull bones is a well-known feature of IOMs as well as dural meningiomas without actual bone infiltration (2). Our study showed 68% of IOMs were hyperostotic, 24 % of IOMs were mixed, and 8% of IOMs were lytic. The rates observed by us were similar to those reported by Crawford et al. (13). Our data suggest that IOMs that grow slowly are usually hyperostotic. We did not observe a higher grade in the pure lytic lesions. In their study Crawford et al. used plain skull radiographs and did not differentiate pure lytic lesions from mixed types. In our study, a mixed pattern of osseous involvement was associated with higher grade of meningioma.
ACCEPTED MANUSCRIPT Bassiouni H et al. (1) reviewed dural involvement in a series of 16 consecutive patients with a cranial vault extradural meningioma. Infiltration of the dura was evident on pathological examination in 14 cases in which the dura was resected. In two
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patients, the dura had a normal appearance intraoperatively and was left in situ. In both
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instances, the tumor recurred, and the meningioma showed diffuse involvement of the dura at repeat surgical resection. We have similar observations in terms of dural
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involvement as all of our dural specimens revealed infiltration even without dural mass on MR and we suggest that a dural involvement should always be suspected and the
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dura excised at the site of craniotomy followed by the placement of a dural graft. Brain edema is an important prognostic imaging finding in the preoperative
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period; it is responsible for clinical deficits related to the involved parenchyma and is associated with the violation of the arachnoid membrane, increasing the risk of postoperative complications (4). The presence and degree of edema correlated well
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with increased grade in our study. Mixed subtype (hyperostotic and lytic) with extra cranial soft-tissue mass was found to be more aggressive than hyperostotic and lytic
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subtypes in our study population.
In our study, no contrast enhancement was noted in grade I hyperostotic IOMs
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on MR by using fat saturated T1 weighted sequence. Changhong L. et al. reported striking contrast enhancement in their cohort of intraosseous meningiomas by using CT
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(10). They measured the mean CT number of the IOM in the hyperdense regions before and after intravenous contrast administration and found over 25 HU increase in density; from 76.5 HU to 101.5 HU (10). They found this degree of enhancement similar to dural meningioma enhancement.
T1 weighted MR image with fat saturation is the most
sensitive technique to evaluate contrast enhancement of a bone lesion and we believe this evaluation is limited on CT scan when both the bone tissue and the contrast have high CT numbers. In our study, the degree of enhancement is correlated with grade of IOMs. The enhancement rate was 78% in grade I but 100% for both Grade II and III. The pure hyperostotic IOM in sphenoid ridge showed fewer enhancements than other sites and types.
ACCEPTED MANUSCRIPT The differential diagnosis of IOM consists of fibrous dysplasia (FD), osteoma, skull metastasis, and calvarial hemangioma (12, 14-16, 21, 22). The cystic type of FD typically involves the calvarium (there is widening of the intradiploic space, with thinning
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of the outer table and little involvement of the inner table). Although both FD and IOM
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can cause osseous expansion, these disease entities can be differentiated by the osseous contours. IOM results in cortical table irregularities, while with FD, there are
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smooth contours of the inner and outer table. Cortical surface irregularity was observed in nearly all cases in our series (64/65). The age distribution also differs between the
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two lesions. Fibrous dysplasia typically stops developing after puberty; an IOM generally develops after puberty and continues to grow slowly (17). Metastatic skull lesions are
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mostly osteolytic on CT and often have an invasive appearance with poorly defined tumor margins and extensive peritumoral edema when compared with IOMs (18). Calvarial hemangiomas are often confused with IOMs and are usually round, lytic
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lesions that arise predominantly from the diploic space with a characteristic sunburst, radiating spoke wheel or web-like pattern of trabecular thickening (19). For osteolytic the
differential
diagnosis
is
broad
and
should
include
chondroma,
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types,
chondrosarcoma, dermoid, epidermoid tumor, brown tumor, multiple myeloma,
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plasmacytoma, giant cell tumor, aneurysmal bone cyst, eosinophilic granuloma, or metastatic cancer (2, 20).
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There were several limitations in our study. First, the operative reports did not always specify whether the osseous pathology specimens included a dural component. Therefore, dural involvement was assumed in those cases based on thickening and enhancement seen on postcontrast MR images. Second, of all patients with pathologically proven IOM, exclusion of 16 patients with secondary osseous involvement by an adjacent dural-based en plaque meningioma was made on the basis of pathology reports. Although none of our remaining 65 patients have pathology reports showing secondary osseous involvement, there was not enough histopathological proof available to exclude secondary involvement. Therefore we made the inclusion criteria using imaging studies. According to this imaging criteria the patients whose mean tumor mass within the bone was equal or greater than 50 % of total mass were accepted to have IOMs. Some of the inclusions had to be presumptive since these criteria are still
ACCEPTED MANUSCRIPT controversial in the literature. Although Changhong L. et al. proposed that dural invasion precludes a diagnosis of IOM, most authors claim that the localization of the mean tumor mass within the bone allows determination of the site of origin of the tumor, even
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Conclusion:
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allow cross modality correlation of imaging features.
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in the presence of dural invasion (3, 10). Third, not all patients had both CT and MR to
In summary, categorical differences exist in location, imaging pattern, dural
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involvement, and prognosis of IOMs. Mixed hyperostotic/lytic pattern of osseous involvement with presence of radial bony spiculations, and extracranial scalp mass
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seem to be more frequently associated with higher grade IOMs.
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Acknowledgements:
We would like to thank a brilliant medical student, the late Evrim Kimyonok, who had
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contributed to this project at the beginning of our study. Evrim had many successful
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years ahead of her; but her great potential was unfortunately left untapped. We also would like to thank Ami Vikani, Jefferson Scott Graves and David Yousem for their contributions to the preparation of this manuscript.
References 1. Matschke J, Addo J, Bernreuther C, Zustin J. Osseous changes in meningioma en plaque. Anticancer Research 2011:31:591-6. 2. James B. Ames B.Elder, Roscoe Atkinson,Chi-Shingzee, Thomas C.Chen. Primary intraosseous meningioma. Neurosurg Focus 2007:23:13.
ACCEPTED MANUSCRIPT 3. Lang FF, Macdonald OK, Fuller GN, et al: Primary extradural meningiomas: a report on nine cases and review of the literature from the era of computerized tomography
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scanning. J Neurosurg 2000:93:940–50.
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4. Talacchi A, Corsini F, Gerosa M. Hyperostosing meningiomas of the cranial vault with and without tumor mass. Acta Neurochir 2011:153:53-61.
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5. Arana E, Menor F, Lloret RM. Intraosseous meningioma. J Neurosurg 1996:85:362–
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6. Politi M, Romeike BF, Papanagiotou P, et al. Intraosseous hemangioma of the skull
Neuroradiology 2005:26:2049–52.
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with duraltail sign: radiologic features with pathologic correlation. AJNR Am J
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7. Derome PJ, Visot A. Bony reaction and invasion in meningiomas,in Al-Mefty O (ed): Meningiomas. New York: Raven Press; 1991:169–80.
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8. Arana E, Diaz C, Latorre FF, et al. Primary intraosseous meningiomas. Acta
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Radiologica 1996:37:937–42.
9. Kim KS, Rogers LF and Goldblatt D: CT features of hyperostosing meningioma en
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plaque. AJR Am J Roentgenol 1987:149:1017-23. 10. Changhong L, Naiyin C, Yuehuan G, et al. Primary intraosseous meningiomas of the skull. Clin Radiol 1997:52:546–50. 11. Perry A, Louis DN, Scheithauer BW, et al. Meningiomas. In: Louis DN, Ohgaki H, Wiestler OD et al. WHO Classification of Tumours of the Central Nervous System 2007. 12. Shrivastava RK, Sen C, Costantino PD, et al. Sphenoorbitalmeningiomas: surgical limitations and lessons learned in their long-term management. J Neurosurg 2005:103:491-7.
ACCEPTED MANUSCRIPT 13. Crawford TS, Kleinschmidt-DeMasters BK, Lillehei KO. Primary intraosseous meningioma. J Neurosurg 83:912-915.
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14. Osborn G. Meningiomas and other nonglial neoplasms. In: Diagnostic
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neuroradiology. St Louis: Mosby; 1994:579.
15. Jochen W., Alfred C.. Primary intraosseous meningioma in a skull of the medieval
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period of Southwestern Germany. Int. J. Osteoarchaeol. 2002:12:385–92.
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16. Cushing W, Eisenharld T. Meningiomas. Their classification, regional behaviour, life history and surgical end results. Hafner Publ. Co., New York 1962.
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17. Hansen-Knarhoi M, Poole MD. Preoperative difficulties in differentiating intraosseous meningiomas and fibrous dysplasia around the orbital apex.J
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Craniomaxillofac Surg 1994:22:226-30.
18. Chen TY, Lee HJ, Wu TC, et al. Intracranial dural metastatic prostate cancer can
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mimic meningioma: a report of two cases. Clin Imaging 2011:35:391-4.
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19. Malde R, Moss T, Malcolm G, et al. Multiple intraosseous calvarial hemangiomas mimicking metastasis from renal cell carcinoma. Adv Urol 2008:176392. doi:
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10.1155/2008/176392
20. Agrawal V, Ludwig N, Agrawal A, Bulsara KR. Intraosseous intracranial meningioma. AJNR Am J Neuroradiol. 2007: 28:314-5.
ACCEPTED MANUSCRIPT Figure Legends
Fig 1 Low grade sphenoidal IOM with homogenous hyperostotic appearance. Axial
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precontrast T1 weighted (W) (a) and coronal T 1 W (d) images show an expanded,
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hypointense, right sphenoid ridge intraosseous mass with superficial irregularity bulging into the right orbit. Post contrast T1 W image (b) shows no prominent enhancement of
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intraosseous mass but mild thickening of the adjacent dura. Nonenhancing central subdural layer was compatible with calcification which is better confirmed on previous
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CT with dural lucent interface (c). Superficial irregularity, expansion and subdural calcification in this location is pathognomonic with the diagnosis of IOM. An expansile
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intraosseous very similar looking fibrous dysplasia has typically no superficial irregularity.
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Fig. 2 Low grade calvarial IOM. CT scan with bone window (b) shows hyperostosis in midline occipital calvarial region. Hyperostosis is of homogeneous density with inner,
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outer tables and diploe not distinguishable as separate structures. There is no prominent surface irregularity on both sides of the lesion. CT scan with soft tissue
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window (a) shows no apparent dural mass.
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Fig. 3 Low grade temporal bone IOM. Coronal post contrast T1 W image shows expansion of left squamous temporal bone with minimal subjacent dural enhancement.
Fig. 4 High grade (III) calvarial IOM. CT scan with soft tissue window shows a right frontal calvarial mass with extracalvarial and intracalvarial components and adjacent cerebral hypoattenuation suggesting edema. CT with bone window shows bony spiculations arising from the outer cortex (arrowhead).
Fig. 5 Low grade calvarial IOM. CT scan with soft tissue window (a) looks mostly normal except subtle outward bulging of right frontal bone. CT scan with bone window (b) shows lytic intraosseous bone lesion with erosion of the inner table. Fat suppressed axial T2 weighted image (c) shows increased intradiploic signal with loss of inner table.
ACCEPTED MANUSCRIPT Post contrast axial T1 weighted image (d) shows prominent enhancement of intradiploic mass without any dural mass.
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Fig. 6 Low grade calvarial IOM. (a) Sagittal T1 W image shows expansion of the frontal
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calvarial bone. (b) Coronal fat-suppressed T2 W image shows expansion and increased diploic signal without obvious inner and outer table erosion. Post contrast axial T1 W
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image (c) shows loss of definition of outer cortex. Enhancement of diploic space in the lesion is similar to that of remaining diploic space. There is also no dural enhencement
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suggesting thickening or mass.
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ACCEPTED MANUSCRIPT Table 1. Demographics, distribution and histopathologic grades of IOMs.
Other skull base regions 8(14) 56/35/69 8/0 5 3
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Calvarial convexity 22(33) 58/26/91 16/6 16 5
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Number of patients (n,%) Age(mean/min/max) Sex(F/M) Grade I II
Sphenoid ridge 35(53) 56/32/81 27/8 35 0
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Tumor Location
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N (Number of CT scans) Hyperostotic Lytic Mixed Cortical irregularity Radial bony spiculation Dural calcification N (Number of MR scans) Dural enhancement Dural mass Cerebral edema Enhancement in the bone lesion Scalp mass Expansion of the bone
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Number of Patients Radiologic Feature CT
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Table 2. CT and MR imaging features of IOMs
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MR
Either CT or MR
Grade I 56
Grade II 8
Grade III 1
49 36 4 9 27 0 5 42
3 0 0 3 3 2 2 8
1 0 0 1 1 1 0 1
42 34 23 31
8 8 8 8
1 1 1 1
0 35
4 8
1 1
S0899-7071(14)00148-X doi: 10.1016/j.clinimag.2014.05.013 JCT 7635
To appear in:
Journal of Clinical Imaging
Received date: Revised date: Accepted date:
5 December 2013 23 April 2014 28 May 2014
Please cite this article as: uran Ilica AT, Mossa-Basha Mahmud, Zan Elcin, Vikani Ami, Pillai Jay J., Gujar Sachin, Aygun Nafi, Izbudak Izlem, Cranial Intraosseous Meningioma: Spectrum of neuroimaging findings with respect to histopathological grades in 65 patients, Journal of Clinical Imaging (2014), doi: 10.1016/j.clinimag.2014.05.013
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
Cranial Intraosseous Meningioma: Spectrum of neuroimaging findings with
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respect to histopathological grades in 65 patients
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A.Turan Ilica1, Mahmud Mossa-Basha1, Elcin Zan1, Ami Vikani1, Jay J. Pillai1, Sachin Gujar1, Nafi Aygun1, Izlem Izbudak1
Russell H. Morgan Department of Radiology and Radiological Sciences, The Johns Hopkins Medical Institutions, Baltimore, Maryland, USA
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1 The
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Corresponding Author: Izlem Izbudak, M.D. Assistant Professor of Radiology Division of Neuroradiology The Russell H. Morgan Department of Radiology and Radiological Sciences Johns Hopkins Hospital 600 N. Wolfe Street Phipps B-126-B Baltimore, MD 21287 e-mail: [email protected]
ACCEPTED MANUSCRIPT Abstract The aim of this study was to determine various imaging features of intraosseous
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meningiomas (IOMs) and differentiate low grade from high-grade tumors. The
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histopathologic evaluation revealed WHO grade I tumor in 56 (86 %) patients, grade II in 8 (12%) and grade III in 1 (2 %) patient. WHO grade I was considered low grade and II and III were designated as high grade. Hyperostosis was observed most commonly in
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low-grade IOMs. Mixed hyperostotic/lytic pattern with radial bony spiculations, and presence of a scalp mass seem to be more frequently associated with higher grade
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IOMs.
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Abbreviations: IOM= Intraosseous meningioma
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Keywords: Cranium, Hyperostosis, Meningioma, Intraosseous
ACCEPTED MANUSCRIPT Introduction Primary extradural meningiomas are rare, accounting less than 2% of all
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meningiomas. Intraosseous meningiomas ( IOMs) are a subset of primary extradural
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meningiomas and represent about two thirds of all extradural meningiomas(1-3). Osseous involvement by meningiomas may be primary or secondary, but it may be difficult to classify these as either primary or secondary with respect to its origin site,
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based on the neuroimaging appearance, surgical findings or histologic features (3). Based on published data and our experience, we believe such a differentiation cannot
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be definitively made with imaging or histopathology (3-8).
Although several distinct features of IOMs have been described (9,10), to the
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best of our knowledge, cross sectional imaging analyses of IOMs including MRI have not yet been reported. The aim of the present study was to review a series of IOMs to determine various imaging features of IOMs and differentiate low grade from high-grade
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tumors.
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Materials and Methods
After institutional review board approval, the pathology database was queried for
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reports with the key words “intraosseous meningioma” and “meningioma within the bone” from December 2000 to February 2012. From this list, a total of 81 patients were
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identified. Sixteen patients, whose tumor mass within bone was proven to represent secondary osseous invasion according to pathology were excluded. Sixty-five patients whose mean tumor mass within bone was equal to or greater than 50 % of the total mass were included in the study. For all patients, the available clinical records, operative reports and pathology reports were reviewed. Neuroimaging data, including CT and/or MR were retrieved from our picture archiving and communication system (PACS) and were retrospectively analyzed. Although odds ratio associated with meningioma are considerably high for female population, this study aimed to evaluate intraosseous meningioma in general. CT scans were obtained on multidetector CT scanners, including 4, 16 and 64row detectors from Siemens (Siemens AG, Erlangen, Germany), and Toshiba (Toshiba Medical Systems, Otawara, Japan). Images were obtained with helical technique and
ACCEPTED MANUSCRIPT 0.75 mm -1 mm thickness and reconstructed at 3-5-mm-slice thickness and intervals in a soft-tissue and bone algorithm. Further CT parameters were as follows: x-ray tube current = 400 mAs, 120 kVP, and FOV = 24.0 cm x 24.0 cm. Nine patients underwent
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CT with intravenous administration of non-ionic iodinated contrast.
The MRI examinations were performed at either 1.5T or 3T magnet strength on scanners from different manufacturers: Philips (Philips Medical Systems, Best, the
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Netherlands), GE (GE Medical Systems, Milwaukee, Wisconsin), and Siemens (Siemens AG, Erlangen, Germany). The MRI protocol included diffusion-weighted
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images, T1 weighted images, fast spin-echo T2 weighted images, fluid attenuated inversion recovery (FLAIR) images, and contrast enhanced T1 weighted images. All
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patients underwent post contrast imaging after intravenous administration of gadolinium based contrast media. The sagittal T1W sequence was obtained with parameters as follows: range of TRs, 520–696 ms and TEs, 4.6–14 ms; matrix size range from 192 ×
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192 to 512 × 196; FOV range from 190 × 190 mm to 240 × 240 mm; and range of section thickness/spacing from 1/1 to 5/7 mm. The axial T2W sequence was obtained
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with the range of TR, 2500–7000 ms and TE, 83.136–112 ms; matrix size range from 256 × 184 to 448 × 335; FOV range from 159 × 200 mm to 240 × 240 mm; and the
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range of section thickness/spacing from 2/2 to 5/5-mm. FLAIR sequence parameters were the following: TR, 6000 ms; TE, 120 ms; TI, 2000 ms; section thickness, 5 mm;
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FOV, 23 cm; and matrix size, 256 × 256. A neuroradiologist with 8 years of experience in this field (I.I.) and a general radiologist with 7 years of experience (A.T.I.) reviewed all the CT and MR exams retrospectively and noted findings in consensus. They were blinded to the pathologic grade of the IOMs. In the event of disagreement between the two reviewers, a third neuroradiologist with 15 years of experience (N. A.) adjudicated. Image analysis The locations of the meningiomas were divided into three groups: sphenoid ridge (greater
sphenoid
wing),
other
skull
base
regions
and
calvarial
convexity.
Characteristics evaluated on CT included the location of the tumor, bone density
ACCEPTED MANUSCRIPT (hyperostotic, lytic or mixed), and presence of bone expansion, contour irregularity or radial bony spiculations, and dural calcification. Expansion was defined when the bone lesion thickness was greater than the thickness of the adjacent normal calvarial bone.
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Contour irregularity was defined if there were irregular inner or outer calvarial bony
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surfaces instead of normal smooth borders. Radial oriented bony spiculations along the calvarial surface were also noted if present. Dural calcification is defined as a linear high
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density structure above 100 HU along the dural surface subjacent to the IOM on CT. Presence of dural enhancement or an adjacent intracranial dural or extracranial scalp
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soft tissue mass was noted. The osseous characteristics were evaluated using bone window algorithm (400-600 HU window level, 2400-2600 HU window width).
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On MR, the presence of dural enhancement or an adjacent intracranial dural or extracranial soft tissue mass, and adjacent parenchymal edema were evaluated. Dural enhancement was defined as a linear enhancement not thicker than 3 mm. Nodular or
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linear dural based soft tissue enhancement greater than 3 mm was defined as mass. Cerebral edema was defined as present if there is increased T2/FLAIR signal on MR in
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the adjacent parenchyma. To quantify the extent of edema, the distance from the maximum inner edge of region of maximum edema to the nearest point of meningioma
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border was measured in mm. If there was no white matter FLAIR hyperintensity, it was accepted as ‘‘no edema’’. If the white matter FLAIR hyperintensity is less than tumor, it
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was accepted as ‘‘minimal edema’’. If the extension of edema was equal or greater than tumor it was accepted as ‘‘extensive edema’’. Results Of the 65 patients included in the study, 42 had both MR and CT scans, 23 had either MR (n= 12) or CT scan (n=11). The distribution, demographics and WHO grades of the cases are summarized in Table 1. The two reviewers disagreed on only 3 cases and those were evaluated by a third neuoradiologist independently and a final consensus was achieved. Sphenoid ridge and calvarial convexity predominated over the other locations (Fig. 1-3). Most of the calvarial convexity IOMs originated in the frontal or parietal
ACCEPTED MANUSCRIPT region, except 2 occipital lesions. The 8 other skull base lesions included 7 anterior and middle cranial fossa lesions (planum sphenoidale and parasellar region) and 1 posterior skull base (temporal bone) tumor. In patients with cranial convexity lesions, a lump in
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the scalp was the most common clinical presentation, whereas patients with sphenoid
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ridge meningiomas had visual disturbances. Cranial nerve deficits were the chief complaint for the other skull base IOM. The patient with a temporal bone meningioma
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presented with hearing loss.
All meningiomas were classified as Grade I (benign), Grade II (atypical) or Grade
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III (anaplastic/malignant) according to the features set in the World Health Organization classification system (11). WHO grade I was considered low grade and II and III were
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designated as high grade.
Among the higher-grade tumors (grades II and III), 6 were at the convexity, 2
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involved the skull base and 1 lesion was in the sphenoid ridge (Fig. 4). Non sphenoid skull base and convexity IOMs were more commonly higher grade relative to sphenoid
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ridge IOMs.
Lytic lesions were found in 4 (8%) patients (1 sphenoid, 1 convexity and 2 skull
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base), all of which were grade I on the histopathological examination (Fig. 5). Radial spiculations were observed in three cases with higher grades (2 grade II and 1 grade III
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patients) but in none of the low grade lesions. Bone expansion was common in all grades (44/65) but always present in higher grades (9/9).
An association with edema was more prominent in the higher grades (8/8 in grade II and 1/1 in grade III) as compared to lower grades (23/42) among patients who have available MRI exams. Edema extension was minimal in all WHO grade I patients with available MR exams (23/42). There was extensive edema in all WHO grade II and III patients.
Five patients presented with scalp mass: 4 with grade II and 1 with grade III lesions. None of the grade I patients had associated extra cranial scalp mass. The presence of scalp mass was a strong predictor of higher grade.
ACCEPTED MANUSCRIPT The sphenoid ridge was the only location wherein an intraosseous meningioma without an adjacent dural-based mass was observed. Among the 35 sphenoid ridge
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meningiomas, 12 cases had no dural mass, and all were grade I.
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Enhancement of bone was not observed in the hyperostotic IOMs. Whereas all mixed and lytic IOMs enhanced prominently (Fig. 5). The loss of definition in the outer cortex was an additional finding that we observed in 1 grade I calvarial convexity IOM
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(Fig. 6). CT and MR features and related WHO grades of patients were summarized in
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Table 2.
Discussion
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Primary extradural meningiomas are classified as purely extracalvarial (type I), purely calvarial (type II), or calvarial with extracalvarial extension (type III). Based on the site of the tumor, Lang et al. subdivided type II and type III lesions into convexity
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(C) or skull-base (B) forms (1-3). In this study, 53 % of the IOMs were in the sphenoid ridge, 33% in the calvarial convexity and 14% in the skull base. In the literature, the
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corresponding ratios were 70-90% in the sphenoid ridge and 10-28 % in the calvarial convexity (1-3, 9, 12). Meningiomatous cells are known to invade the Haversian canals
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to stimulate osteoblastic activity, which has led to suggestion of the term “hyperostosing” as synonymous with “invading” whenever bone involvement occurs (4,
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8-10). We observed hyperostosis in the majority of the histologically grade I IOMs. Mixed pattern and osteolysis, and radial spiculation were prominent at higher grades in our cohort.
Hyperostosis in the sphenoidal region or other skull bones is a well-known feature of IOMs as well as dural meningiomas without actual bone infiltration (2). Our study showed 68% of IOMs were hyperostotic, 24 % of IOMs were mixed, and 8% of IOMs were lytic. The rates observed by us were similar to those reported by Crawford et al. (13). Our data suggest that IOMs that grow slowly are usually hyperostotic. We did not observe a higher grade in the pure lytic lesions. In their study Crawford et al. used plain skull radiographs and did not differentiate pure lytic lesions from mixed types. In our study, a mixed pattern of osseous involvement was associated with higher grade of meningioma.
ACCEPTED MANUSCRIPT Bassiouni H et al. (1) reviewed dural involvement in a series of 16 consecutive patients with a cranial vault extradural meningioma. Infiltration of the dura was evident on pathological examination in 14 cases in which the dura was resected. In two
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patients, the dura had a normal appearance intraoperatively and was left in situ. In both
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instances, the tumor recurred, and the meningioma showed diffuse involvement of the dura at repeat surgical resection. We have similar observations in terms of dural
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involvement as all of our dural specimens revealed infiltration even without dural mass on MR and we suggest that a dural involvement should always be suspected and the
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dura excised at the site of craniotomy followed by the placement of a dural graft. Brain edema is an important prognostic imaging finding in the preoperative
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period; it is responsible for clinical deficits related to the involved parenchyma and is associated with the violation of the arachnoid membrane, increasing the risk of postoperative complications (4). The presence and degree of edema correlated well
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with increased grade in our study. Mixed subtype (hyperostotic and lytic) with extra cranial soft-tissue mass was found to be more aggressive than hyperostotic and lytic
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subtypes in our study population.
In our study, no contrast enhancement was noted in grade I hyperostotic IOMs
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on MR by using fat saturated T1 weighted sequence. Changhong L. et al. reported striking contrast enhancement in their cohort of intraosseous meningiomas by using CT
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(10). They measured the mean CT number of the IOM in the hyperdense regions before and after intravenous contrast administration and found over 25 HU increase in density; from 76.5 HU to 101.5 HU (10). They found this degree of enhancement similar to dural meningioma enhancement.
T1 weighted MR image with fat saturation is the most
sensitive technique to evaluate contrast enhancement of a bone lesion and we believe this evaluation is limited on CT scan when both the bone tissue and the contrast have high CT numbers. In our study, the degree of enhancement is correlated with grade of IOMs. The enhancement rate was 78% in grade I but 100% for both Grade II and III. The pure hyperostotic IOM in sphenoid ridge showed fewer enhancements than other sites and types.
ACCEPTED MANUSCRIPT The differential diagnosis of IOM consists of fibrous dysplasia (FD), osteoma, skull metastasis, and calvarial hemangioma (12, 14-16, 21, 22). The cystic type of FD typically involves the calvarium (there is widening of the intradiploic space, with thinning
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of the outer table and little involvement of the inner table). Although both FD and IOM
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can cause osseous expansion, these disease entities can be differentiated by the osseous contours. IOM results in cortical table irregularities, while with FD, there are
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smooth contours of the inner and outer table. Cortical surface irregularity was observed in nearly all cases in our series (64/65). The age distribution also differs between the
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two lesions. Fibrous dysplasia typically stops developing after puberty; an IOM generally develops after puberty and continues to grow slowly (17). Metastatic skull lesions are
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mostly osteolytic on CT and often have an invasive appearance with poorly defined tumor margins and extensive peritumoral edema when compared with IOMs (18). Calvarial hemangiomas are often confused with IOMs and are usually round, lytic
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lesions that arise predominantly from the diploic space with a characteristic sunburst, radiating spoke wheel or web-like pattern of trabecular thickening (19). For osteolytic the
differential
diagnosis
is
broad
and
should
include
chondroma,
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types,
chondrosarcoma, dermoid, epidermoid tumor, brown tumor, multiple myeloma,
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plasmacytoma, giant cell tumor, aneurysmal bone cyst, eosinophilic granuloma, or metastatic cancer (2, 20).
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There were several limitations in our study. First, the operative reports did not always specify whether the osseous pathology specimens included a dural component. Therefore, dural involvement was assumed in those cases based on thickening and enhancement seen on postcontrast MR images. Second, of all patients with pathologically proven IOM, exclusion of 16 patients with secondary osseous involvement by an adjacent dural-based en plaque meningioma was made on the basis of pathology reports. Although none of our remaining 65 patients have pathology reports showing secondary osseous involvement, there was not enough histopathological proof available to exclude secondary involvement. Therefore we made the inclusion criteria using imaging studies. According to this imaging criteria the patients whose mean tumor mass within the bone was equal or greater than 50 % of total mass were accepted to have IOMs. Some of the inclusions had to be presumptive since these criteria are still
ACCEPTED MANUSCRIPT controversial in the literature. Although Changhong L. et al. proposed that dural invasion precludes a diagnosis of IOM, most authors claim that the localization of the mean tumor mass within the bone allows determination of the site of origin of the tumor, even
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Conclusion:
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allow cross modality correlation of imaging features.
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in the presence of dural invasion (3, 10). Third, not all patients had both CT and MR to
In summary, categorical differences exist in location, imaging pattern, dural
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involvement, and prognosis of IOMs. Mixed hyperostotic/lytic pattern of osseous involvement with presence of radial bony spiculations, and extracranial scalp mass
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seem to be more frequently associated with higher grade IOMs.
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Acknowledgements:
We would like to thank a brilliant medical student, the late Evrim Kimyonok, who had
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contributed to this project at the beginning of our study. Evrim had many successful
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years ahead of her; but her great potential was unfortunately left untapped. We also would like to thank Ami Vikani, Jefferson Scott Graves and David Yousem for their contributions to the preparation of this manuscript.
References 1. Matschke J, Addo J, Bernreuther C, Zustin J. Osseous changes in meningioma en plaque. Anticancer Research 2011:31:591-6. 2. James B. Ames B.Elder, Roscoe Atkinson,Chi-Shingzee, Thomas C.Chen. Primary intraosseous meningioma. Neurosurg Focus 2007:23:13.
ACCEPTED MANUSCRIPT 3. Lang FF, Macdonald OK, Fuller GN, et al: Primary extradural meningiomas: a report on nine cases and review of the literature from the era of computerized tomography
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scanning. J Neurosurg 2000:93:940–50.
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4. Talacchi A, Corsini F, Gerosa M. Hyperostosing meningiomas of the cranial vault with and without tumor mass. Acta Neurochir 2011:153:53-61.
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5. Arana E, Menor F, Lloret RM. Intraosseous meningioma. J Neurosurg 1996:85:362–
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63.
6. Politi M, Romeike BF, Papanagiotou P, et al. Intraosseous hemangioma of the skull
Neuroradiology 2005:26:2049–52.
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with duraltail sign: radiologic features with pathologic correlation. AJNR Am J
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7. Derome PJ, Visot A. Bony reaction and invasion in meningiomas,in Al-Mefty O (ed): Meningiomas. New York: Raven Press; 1991:169–80.
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8. Arana E, Diaz C, Latorre FF, et al. Primary intraosseous meningiomas. Acta
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Radiologica 1996:37:937–42.
9. Kim KS, Rogers LF and Goldblatt D: CT features of hyperostosing meningioma en
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plaque. AJR Am J Roentgenol 1987:149:1017-23. 10. Changhong L, Naiyin C, Yuehuan G, et al. Primary intraosseous meningiomas of the skull. Clin Radiol 1997:52:546–50. 11. Perry A, Louis DN, Scheithauer BW, et al. Meningiomas. In: Louis DN, Ohgaki H, Wiestler OD et al. WHO Classification of Tumours of the Central Nervous System 2007. 12. Shrivastava RK, Sen C, Costantino PD, et al. Sphenoorbitalmeningiomas: surgical limitations and lessons learned in their long-term management. J Neurosurg 2005:103:491-7.
ACCEPTED MANUSCRIPT 13. Crawford TS, Kleinschmidt-DeMasters BK, Lillehei KO. Primary intraosseous meningioma. J Neurosurg 83:912-915.
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14. Osborn G. Meningiomas and other nonglial neoplasms. In: Diagnostic
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neuroradiology. St Louis: Mosby; 1994:579.
15. Jochen W., Alfred C.. Primary intraosseous meningioma in a skull of the medieval
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period of Southwestern Germany. Int. J. Osteoarchaeol. 2002:12:385–92.
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16. Cushing W, Eisenharld T. Meningiomas. Their classification, regional behaviour, life history and surgical end results. Hafner Publ. Co., New York 1962.
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17. Hansen-Knarhoi M, Poole MD. Preoperative difficulties in differentiating intraosseous meningiomas and fibrous dysplasia around the orbital apex.J
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Craniomaxillofac Surg 1994:22:226-30.
18. Chen TY, Lee HJ, Wu TC, et al. Intracranial dural metastatic prostate cancer can
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mimic meningioma: a report of two cases. Clin Imaging 2011:35:391-4.
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19. Malde R, Moss T, Malcolm G, et al. Multiple intraosseous calvarial hemangiomas mimicking metastasis from renal cell carcinoma. Adv Urol 2008:176392. doi:
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10.1155/2008/176392
20. Agrawal V, Ludwig N, Agrawal A, Bulsara KR. Intraosseous intracranial meningioma. AJNR Am J Neuroradiol. 2007: 28:314-5.
ACCEPTED MANUSCRIPT Figure Legends
Fig 1 Low grade sphenoidal IOM with homogenous hyperostotic appearance. Axial
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precontrast T1 weighted (W) (a) and coronal T 1 W (d) images show an expanded,
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hypointense, right sphenoid ridge intraosseous mass with superficial irregularity bulging into the right orbit. Post contrast T1 W image (b) shows no prominent enhancement of
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intraosseous mass but mild thickening of the adjacent dura. Nonenhancing central subdural layer was compatible with calcification which is better confirmed on previous
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CT with dural lucent interface (c). Superficial irregularity, expansion and subdural calcification in this location is pathognomonic with the diagnosis of IOM. An expansile
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intraosseous very similar looking fibrous dysplasia has typically no superficial irregularity.
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Fig. 2 Low grade calvarial IOM. CT scan with bone window (b) shows hyperostosis in midline occipital calvarial region. Hyperostosis is of homogeneous density with inner,
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outer tables and diploe not distinguishable as separate structures. There is no prominent surface irregularity on both sides of the lesion. CT scan with soft tissue
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window (a) shows no apparent dural mass.
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Fig. 3 Low grade temporal bone IOM. Coronal post contrast T1 W image shows expansion of left squamous temporal bone with minimal subjacent dural enhancement.
Fig. 4 High grade (III) calvarial IOM. CT scan with soft tissue window shows a right frontal calvarial mass with extracalvarial and intracalvarial components and adjacent cerebral hypoattenuation suggesting edema. CT with bone window shows bony spiculations arising from the outer cortex (arrowhead).
Fig. 5 Low grade calvarial IOM. CT scan with soft tissue window (a) looks mostly normal except subtle outward bulging of right frontal bone. CT scan with bone window (b) shows lytic intraosseous bone lesion with erosion of the inner table. Fat suppressed axial T2 weighted image (c) shows increased intradiploic signal with loss of inner table.
ACCEPTED MANUSCRIPT Post contrast axial T1 weighted image (d) shows prominent enhancement of intradiploic mass without any dural mass.
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Fig. 6 Low grade calvarial IOM. (a) Sagittal T1 W image shows expansion of the frontal
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calvarial bone. (b) Coronal fat-suppressed T2 W image shows expansion and increased diploic signal without obvious inner and outer table erosion. Post contrast axial T1 W
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image (c) shows loss of definition of outer cortex. Enhancement of diploic space in the lesion is similar to that of remaining diploic space. There is also no dural enhencement
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Figure 6c
ACCEPTED MANUSCRIPT Table 1. Demographics, distribution and histopathologic grades of IOMs.
Other skull base regions 8(14) 56/35/69 8/0 5 3
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Calvarial convexity 22(33) 58/26/91 16/6 16 5
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Number of patients (n,%) Age(mean/min/max) Sex(F/M) Grade I II
Sphenoid ridge 35(53) 56/32/81 27/8 35 0
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Tumor Location
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N (Number of CT scans) Hyperostotic Lytic Mixed Cortical irregularity Radial bony spiculation Dural calcification N (Number of MR scans) Dural enhancement Dural mass Cerebral edema Enhancement in the bone lesion Scalp mass Expansion of the bone
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Number of Patients Radiologic Feature CT
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Table 2. CT and MR imaging features of IOMs
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Either CT or MR
Grade I 56
Grade II 8
Grade III 1
49 36 4 9 27 0 5 42
3 0 0 3 3 2 2 8
1 0 0 1 1 1 0 1
42 34 23 31
8 8 8 8
1 1 1 1
0 35
4 8
1 1
