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��ࡱ�>��	x{����w�������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������]�����bjbj{�{�:��1\�1\�=,�������������������8���<��3f���.��3333333$X5�8H+3���`@���+3��L�3�#�#�#�f���1$�#�3�#�#:_(,�(�����.&M�����T"��(
�1�30�3�(RV8*#�V8�(�(>V8�=+����#�����+3+3�#����3������������������������������������������������������������������������V8���������HJ:Incidentally detected pulmonary metastasis from recurrent atypical meningioma with superior sagittal sinus invasion � case report and literature review 
Davide Nasi M.D. 1, Corrado Iaccarino M.D. 2-3, Elisabetta Froio M.D. 4, Silvia Serra M.D. 4, Elena Tagliavini M.D. 4, Nourallah Eshraghi M.D. 5, Franco Servadei M.D. 2-3, Reza Ghadirpour M.D. 2-3

1 Clinic of Neurosurgery, Polytechnic University of Marche, Umberto I General Hospital, Ancona, Italy 
2  Neurosurgery-Neurotraumatology Unit, University Hospital of Parma, Parma, Italy 
3  Neurosurgery Unit, IRCCS �Arcispedale Santa Maria Nuova� of Reggio Emilia, Reggio Emilia, Italy 
4 Pathology Department, IRCCS �Arcispedale Santa Maria Nuova� of Reggio Emilia, Reggio Emilia, Italy 
5 Departmen of Surgery, Qom University of� Medical Sciences and Heath Service, Iran
Corresponding Author 
Davide Nasi M.D. 
Phone: 00390521704666 
Fax: 00390521704634 
Email:  HYPERLINK "mailto:davidenasi83@gmail.com" davidenasi83@gmail.com


Abstract 
Meningioma is a common brain tumor but despite its high prevalence, extracranial metastasis is really rare, as it may be seen in lung, bone, intraspinal, liver and cervical lymph nodes decreasingly. We report a case of metastases to lung incidentally founded from an intracranial recurrent atypical meningioma with superior sagittal sinus invasion previously treated with good control. This report highlights that in the rare case of unique incidentally founded pulmonary lesion and apparent control of the intracranial disease, the differential diagnosis of metastastic meningioma, primary lung meningioma or others lung tumor can be very challenging . The revision of pertinent literature suggests that the invasion of venous sinuses should be considered as a major risk factor for distant metastases.

Key words: meningioma, extracranial metastasis, pulmonary metastasis


Introduction
Meningiomas are common tumors in neuroaxis and account for a 13% to 26% of primary intracranial neoplasms [1,2]. 
Usually meningiomas are associated with a benign clinical course [3-5] and gross total resection is curative in most cases. However local recurrence has been repprted in 9% to 32% of cases [4,5]; in addition local invasion to adjacent tissues like dura, cranial bone and underlying brain is a common problem in many cases [4,5]. Just like other tumors the other type of recurrence includes near and distant metastases. Involvement of orbit, paranasal sinuses, nasopharynx, cranial bones, skin and subcutis are some examples of near metastases while distant targets are lung, pleura, abdomen and liver, lymph node, bones, decreasingly [5].
Based on its histopathologic features and the association with the tendency to relapse and to pursue an aggressive clinical course, meningioma is subdivided by World Health Organization (WHO) into three grades (1): Grade I (benign) that is the most common (88�95% of meningiomas), and its invasion rate is the lowest, grade II (atypical) with higher rate of invasion to brain but less to extracranial and higher rate of local recurrence after surgical resection. (5 7% of meningiomas), and grade III (anaplastic) with tendency to malignant change and highest recurrence rate (1 2% of meningiomas) [4]. However this classi�cation does not include the occurrence of metastasis in meningioma course history in its grading.
In this article we report case of metastases to lung incidentally founded from an intracranial recurrent atypical meningioma with superior sagittal sinus invasion previously treated with good control. This case highlights the difficulty for diagnosis for pathologists and physicians who are not always aware of this unusual presentation of this disease. Moreover risk factors for extracranial metastasis, metastatic routes and treatments were described by literature review.

Case Report
The patient is a 47 years-old (y/o) man and was admitted for the first time in 2006 for one month history of visual acuity reduction and headache. In ophthalmologic examination papilledema was detected and a computed tomography (CT) scan showed a solid hyperdense mass (diameter 4x6 cm) in left frontal lobe. Brain magnetic resonance imaging (MRI) demonstrated a wide dural based, round, well defined and non homogeneously enhanced mass in the left frontal lobe and accompanying edema that cause mild midline shift (Figure 1ab). Its location was near the superior sagital sinus (SSS) but doesn�t invade it. He underwent a craniotomy during few days and tumor resection achieved Simpson grade II (complete removal of tumor and its visible extensions by coagulation of its dural attachment veri�ed by surgical microscopy). In that time preoperation pulmonary evaluation with chest-X-ray (CXR) was normal. Histopathological studies showed a bundles of meningothelial and spindle cells with high nuclear / cytoplasmic ratio, prominent nucleoli, sheet-like growth and atypical mitotic figures (Figure 2a). The immunohistochemical profile showed positivity for vimentin and epithelial membrane antigen (EMA) and demonstrated the high Ki-67 (MIB 1) labelling indices (Figure 2bcd).  This histopathological investigation led to a diagnosis of an atypical meningioma (WHO Grade II) according to WHO criteria. After 18 months, the patient presented a symptomatic recurrence of the tumor and a second microsurgical resection was performed. However at this stage the SSS was involved and a residual of meningioma infiltrating the SSS was left (Simpson grade IV: partial removal, leaving intradural tumor in situ). Pathologic evaluation again showed atypical meningioma with previous pathologic features. Preoperative CXR in this time also was normal. Postsurgical therapy after the second resection included focal targeted radiation therapy with an overall dose of 60 Gy. For 30 months the patient was followed without specific problem until January 2010 when he developed status epilepticus and admitted at our department. MRI imaging showed a stability of residual of meningioma and his seizure was treated medically. Nevertheless, during hospitalization a routine CXR demonstrated a round solid mass in left lung with 5 x 4 cm diameter and prominent lymph node on the other side without pleural effusion, confirmed by high resolution computed tomography (HRCT) (Figure 3ab). Retrograde evaluations of previous CXRs didn't show any mass in that location. Lung biopsy with brushing was performed and histological examination showed neoplastic meningothelial cells infiltrating the bronchial wall (Figure 4a). In magnified view the tumor consists of spindle cells with whorling or fascicular patterns (Figure 4b). Immunohistochemical stains reveal the positivity of the neoplastic cells for Vimentin and their negativity for AE1/AE3 cytokeratins (Figure 4cd). The pulmonary metastasis was treated by surgery followed by radiotherapy. After one year of follow up there was no change in patient condition and both brain and chest imaging were negative respectively for progression or recurrence of lesions. 

Discussion   
Although meningioma is the most common intracranial tumor, distant extracranial dissemination is really rare. In fact prevalence of meningioma metastases reported in literature is 0.15 % [4]. In literatures the most target organs of extracranial metastases were recognized mostly as lung, axial bones and intraspinal. Frequency of organs involvement in details consists of:  lungs (37,2%), bone (16,5%), intraspinal (15,2%), liver (9,2%), pleura (5,5%) and cervical lymph nodes (4,9%). Single case reports of metastatic meningioma to others organs include kidney, muscle, parotid gland, adrenal gland, thyroid gland and spleen [4]. Distant metastasis of meningioma is a well defined entity and was described from when meningioma was announced; Cushing first reported a recurring meningioma which had metastasized to the lung in an autopsy on 1938.
After review of pertinent literature, several factors that predict occurrence of metastases in meningiomas were identified. The first risk factor well established was histological malignancy including high cellularity, cellular heterogeneity, high mitosis rate, nuclear pleomorphism, tumor necrosis, and brain invasion. In fact in a recent review by Surov et al. [5] about 61 % of metastatic meningiomas are grade II or III. In addition the papillary variant present the highest risk of late distant metastases.
However these factors, and consequently the WHO classification are not able to predict the risk of metastasis in meningiomas grade 1 or in cases, such as ours, in which the metastatic dissemination occurs after the recurrence of a meningioma that maintains the same histological characteristics [3]. In this regard, 75% of patients with extracranial metastases of meningiomas presented an invasion of a venous sinus, such our patient. Thus the invasion of venous sinus appears as an important risk factor and must taken into account in the pre- and post- surgical treatment planning. Other factors predictive for metastatic meningioma are previous craniotomy, local recurrences and dissemination in cerebrospinal �uid (CSF) [1-5].
The most common pathways of metastasis in meningiomas are considered to be through the venous circulation and CSF [3-5]. Dissemination through the jugular vein represents a hematogenous way to cervical organs or the lungs while via the paravertebral venous plexus, that have several connections with the veins of the skull, spinal canal, vertebral column, and the intercostal veins of the thoracoabdominal, meningioma can spread to vertebrae, kidney and perirenal tissue, and adrenal glands [4].  The liver may be affected if metastases pass through the right atrium into the inferior vena cava and further into the hepatic veins. The dissemination through the CSF were reported in several cases, inclunding patients with ventriculo-peritoneal shunts. An others pathway of dissemination include the lymphatic vessels (for example for the tumor that invade lymphatics surrounding the cranial nerves).
According to the data published, usually the metastases were detected after recurrence of the primary intracranial meningioma because surgical manipulation seems to affect the normal tumors cohesion encouraging the spread through the CSF or blood [1-5]. Therefore, as previously suggested, the surgical resection might initiate metastatic dissemination. Nevertheless, occasionally in some papers the metastases were diagnosed at first and then original intracranial meningioma were detected and then removed. Beyond this in most of patients the tumor tends to metastasize late and it is estimated that the interval between the detection of the primary tumor and the first metastasis is 4,8 years and can reach 24 years in some reports [2,4,5].
Generally metastatic lesion to lung are symptomatic with local symptoms or major signs. Also some papers reported asymptomatic lung metastases found incidentally by CXR or by CT as in our case [4]. Moreover the majority of patients presented multiple non calcified metastatic nodules in different sizes in both peripheral and hilar region, while are rare the cases with a single lesion [4,5]. This observation is very important because in the rare case, such our patient, of a unique pulmonary tumor, the differential diagnosis of metastastic meningioma, primary lung meningioma or others lung tumor can be very challenging [5]. Then pathologists and physicians need to be aware of this unusual histopathological entities. 
Because of its rarity there is still great controversy regarding the best means of management for distant metastasis of meningioma. Generally the data published in literature (even if obtained by case reports or small series) suggest that surgical treatment of recurrence and  metastases with adjuvant radiotherapy increases survival [5]. Another remarkable point is the fact that in grade I meningiomas disease progression or death appear to be lower than in atypical or anaplastic meningiomas [5]. Radiotherapy or radiosurgery alone are reserved for palliative treatment of non resectable lesions. Some authors reported the use chemotherapies or immunotherapies for the treatment of extracranial metastases of meningioma; however  their ef�ciency appears limited [1-5]. 



Conclusions
Extracranial metastasis as well as local recurrence must be considered in atypical meningioma. Although extracranial metastases are well documented in the literature, in the rare case of unique incidentally founded pulmonary lesion (such in our case) and apparent control of the intracranial disease, the differential diagnosis of metastastic meningioma, primary lung meningioma or others lung tumor can be very challenging  and then pathologists and physicians need to be aware of this unusual histopathological entities. Finally, the invasion of venous sinuses should be considered as a major risk factor for distant metastases.

Patient Consent
The patient has consented to the submission of the case report for submission to the journal.
Conflict of interest
All authors certify that they have NO affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers� bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in the subject matter or materials discussed in thismanuscript.
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Erman T, Hanta I, Haciyakupoglu S, Zorludemir S, Zeren H, Gocer AI. (2005) Huge bilateral pulmonary and pleural metastasis from intracranial meningioma: a case report and review of the literature. J Neurooncol 74(2):179-81.
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Perry A, Scheithauer BW, Stafford SL, Lohse CM, Wollan PC. (1999) "Malignancy" in meningiomas: a clinicopathologic study of 116 patients, with grading implications. Cancer 85(9):2046-56
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FIGURE LEGENDS
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Figure 2
A.B. Chest high resolution computed tomography (HRCT) showing a round mass in the left lung hilum (black arrow) and prominent lymph nodes on the other side without pleural effusion. 
C. .Neoplastic meningothelial cells infiltrating the bronchial wall (Hematoxylin-Eosin, x 20)
D. In magnified view the tumor consists of spindle cells with whorling or fascicular patterns (Hematoxylin-Eosin,x 40).E.F.  Immunohistochemical stains reveal the positivity of the neoplastic cells for Vimentin
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