Intramedullary and extramedullary solitary fibrous tumor of the cervical spine
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1 J Neurosurg (Spine 4) 100: , 2004 Intramedullary and extramedullary solitary fibrous tumor of the cervical spine Case report and review of the literature ROBERT J. BOHINSKI, M.D., PH.D., EHUD MENDEL, M.D., KENNETH D. ALDAPE, M.D., AND LAURENCE D. RHINES, M.D. Departments of Neurosurgery and Pathology, The University of Texas M. D. Anderson Cancer Center, Houston, Texas Solitary fibrous tumor is a spindle cell tumor deriving from mesenchymal cells that arises most commonly in the pleura. Only very recently has this tumor been reported in the spine. A solitary fibrous tumor strongly resembles other spindle cell neoplasms of the spine and may be an unrecognized entity if not routinely considered in the differential diagnosis of spinal neoplasms. The authors report an unusual intra- and extramedullary location for a solitary fibrous tumor of the cervical spine. Findings in this case and a comprehensive review of the literature indicate that solitary fibrous tumors can originate from various spinal anatomical substrates and mimic both intra- and extramedullary tumor types. KEY WORDS solitary fibrous tumor cervical spine CD34 S OLITARY fibrous tumor is an uncommon spindle cell lesion that was initially described as a pleura-based neoplasm of mesothelial cell origin. 14 Recently, increased awareness of this tumor type has led to recognition of its occurrence in various extrathoracic and nonserosal sites, including the abdominopelvic viscera, the extraaxial cranial and paracranial compartments, and the spine. 5 Although initially thought to arise from mesothelial cells, it is now believed to arise from mesenchymal cells, which explains its occurrence throughout the body. Intracranial solitary fibrous tumors arise from the dura mater and have been termed meningeal solitary fibrous tumors. 17 Because of their dural basis and spindle cell architecture, intracranial solitary fibrous tumors have been confused with both hemangiopericytoma and meningioma. 4,21 In the spine, few cases of solitary fibrous tumor have been reported, and it is not clear which spinal anatomical structure (that is, dura, leptomeninges, nerve root, or spinal cord) is responsible for giving rise to these tumors. Carneiro, et al., 4 reported the first cases of solitary fibrous tumor affecting the spine in Since this initial report of two patients with intraspinal solitary fibrous tumor, only 11 other cases have been clearly documented in the literature. 1,3,9,12,13,15,16,19,20,23 These cases have not been comprehensively reviewed, and thus spinal solitary fibrous tumors have not been distinguished as a distinct Abbreviations used in this paper: EMA = epithelial membrane antigen; MR = magnetic resonance. 358 clinical entity. The definitive diagnosis of solitary fibrous tumor can only be made based on the results of detailed immunohistochemical staining. 11 Because the differential diagnosis for intraspinal spindle cell neoplasms contains entities that are by far more common than solitary fibrous tumor, a degree of awareness of this latter diagnosis is necessary to direct appropriate immunohistochemical studies. In this report, we describe a solitary fibrous tumor located in both the intra- and extramedullary compartments of the spine. A review of previously reported cases demonstrates that solitary fibrous tumors can arise from distinctly different spinal anatomical substrates, suggesting that the ubiquitous mesenchymal cell also gives rise to these tumors in the spine. In addition, the clinical, neuroimaging, and histological characteristics of these tumors as they affect the spine are discussed. Emphasis is placed on the differentiation of solitary fibrous tumor from other more common spindle cell neoplasms that affect the spine. Case Report History. This 49-year-old woman presented with a 1-year history of neck pain and stiffness. During the course of these symptoms, she sought various forms of medical therapy without relief. Eventually, she experienced a burning sensation in her left hand that gradually progressed more proximally to include the elbow. Her medical history was significant only for allergic sinusitis. Additionally she had a 1-year history of a recalcitrant chronic cough of unknown origin that at first preceded and later seemed to initiate progression of her cervical symptoms.
2 Cervical solitary fibrous tumor FIG. 1. Preoperative sagittal MR images revealing an intraspinal C-4 mass associated with extensive spinal cord edema. Left: A T 2 -weighted image. Center: A T 1 -weighted image. Right: A T 1 -weighted, Gd-enhanced image. Examination. On examination, the patient s cranial nerve function was normal. Motor power in all extremities was within normal limits. Deep tendon reflexes were slightly more active on the left side compared with normal function on the right. Toes were downgoing to plantar stimulation. Her gait was well coordinated. Light touch was decreased in her left hand only. No errors occurred on proprioceptive testing. Results of the remainder of the physical examination were normal. Magnetic resonance imaging of the cervical spine revealed a 1.5-cm well-circumscribed intradural mass at C-4 that appeared to be located posterior to the spinal cord. Compared with spinal cord parenchyma, the mass was hypointense on T 2 -weighted MR images (Fig. 1 left) and isointense on T 1 -weighted sequences (Fig. 1 center). Gadolinium enhancement was strong and nearly homogeneous (Fig. 1 right). Contrast-enhanced axial MR images demonstrated a possible intra- and extramedullary tumor location, as suggested by the presence of a waistlike constrictive band that appeared to divide the mass into nearly equal halves (Fig. 2). A significant amount of peritumoral edema extended within the spinal cord parenchyma from C-2 to C-7 and was best visualized on T 2 -weighted sequences (Fig. 1 left). Laboratory testing, including screening tests for neurodegenerative diseases, showed normal results. Cerebrospinal fluid chemistry and cytology levels were normal. Prior to surgery, a short therapeutic course of dexamethasone lessened the patient s sensory symptoms. Operation. A C3 5 laminectomy was performed. The tumor was immediately apparent after opening the dura and was located deep to the arachnoid (Fig. 3 upper). No attachment of the tumor to the dura, arachnoid, or nerve root was found. Tumor consistency was very firm, and a tough pseudocapsule anchored the mass to the posterior columns of the spinal cord. Sharp dissection at the tumor spinal cord interface was performed. This interface corresponded to the waistlike constriction that was apparent on preoperative MR imaging (Fig. 2). Further dissection demonstrated that the dumbbell-shaped morphology of the tumor represented nearly equal intra- and extramedullary components (Fig. 3 center). The well-circumscribed character of the mass allowed establishment of a clear plane of dissection. The tumor was resected en bloc by sharply freeing its fibrous attachments to the posterior columns. Intraoperative photographs of the tumor bed demonstrate the extent of intramedullary involvement (Fig. 3 center and lower). Histopathological Examination. The en bloc specimen measured cm. Evaluation of H & E stained tissue samples demonstrated a spindle cell neoplasm. Immunohistochemical staining on formalin-fixed, parafinembedded tissue was negative for S100 and EMA (ruling out nerve sheath tumor and meningioma, respectively) but strongly and diffusely positive for CD34. Thick collagen bands were present throughout the tumor, which is a feature typical of solitary fibrous tumor but not heman- FIG. 2. Preoperative axial T 1 -weighted Gd-enhanced MR image of the cervical spine. Arrows indicate a waistlike constrictive band, seeming to divide the mass into nearly equal halves. 359
3 R. J. Bohinski, et al. FIG. 4. Photomicrograph showing a solitary fibrous tumor specimen. Results indicated a spindle cell tumor in poorly formed fascicles adjacent to dense collagenous bands. H & E, original magnification 200. giopericytoma (Fig. 4). Focal areas of high cellularity and nuclear pleomorphism were also present. Postoperative Course. In the immediate postoperative period, physical examination demonstrated markedly decreased proprioceptive sensation in all four extremities with preserved motor power. Although this deficit was initially quite disabling, the patient experienced rapid recovery of her sensory abilities. At 10-month follow-up examination, she only complained of mildly decreased sensation in both hands. She was able to return to her previous full-time employment. Ten months after surgery, MR imaging demonstrated complete resolution of peritumoral edema and no evidence of recurrent tumor. FIG. 3. Intraoperative photographs obtained just after opening the dura and arachnoid (upper), following circumscription of the extramedullary portion of the tumor (center), and after gross-total removal of the tumor (lower). No attachment to dura, arachnoid, or nerve root was found. Discussion A comprehensive summary of reported cases of solitary fibrous tumor affecting the spine is provided in Table 1. To date, almost every reported case of intraspinal solitary fibrous tumor involves a unique anatomical site. In other words, no single anatomical structure, such as nerve root, dura, or spinal cord parenchyma, was responsible for providing the cellular origin of the tumor in all cases. More than any other feature, an unusual tumor location and site of attachment should raise suspicion of a solitary fibrous tumor because, unlike meningioma or schwannoma, they do not typically involve the dura or nerve roots. On the other hand, in half of all intraspinal solitary fibrous tumors some type of attachment to the spinal cord itself was demonstrated; this characteristic is not commonly seen with other spindle cell tumors. In our case, an alternative diagnosis to meningioma or schwannoma was considered at the time of surgery because no attachment of the tumor to dura, arachnoid, or nerve root was found. Locations that closely mimic those associated with schwannoma and meningioma, however, have also been described. 13,15 Considered in the context of previously reported cases, findings in our case emphasize the ability of these tumors to take cellular origin from distinctly different anatomical structures in and around the spine (Table 2). On MR imaging, nearly all intraspinal solitary fibrous tumors appeared to be well-defined, homogeneous to slightly heterogeneous, enhancing lesions that were isointense on T 1 -weighted sequences and hypointense on T 2 - weighted images (Table 1). Despite this uniform MR imag- 360
4 Cervical solitary fibrous tumor TABLE 1 Summary of clinicopathological features of intraspinal solitary fibrous tumor reported in the literature* MRI Appearance Neuro- Age Symptoms Location Well Extent logical Re- (yrs), Size Contrast Circum- of Re- Follow Out- cur- Authors & Year Sex Type Duration Level Compartment Attachment (cm) T 1 T 2 Enhancement scribed? section Up come rence Carneiro, et al., , F leg pain, numbness, 3 yrs unclear ID: IM EM LM, SC firm 1.2 NS NS NS NS STR 5 yrs imp yes & weakness; BBI 54, F leg pain, numbness, & 6 mos L-2 ED dura 2.0 NS NS NS yes GTR 7 yrs imp no weakness; BBI Alston, et al., , M Brown Séquard syndrome T4 5 ID: IM SC loose 3.0 NS iso homog str yes GTR 2 mos imp no Malek, et al., , M leg pain & paresthesias; BBI 1.5 yrs T7 8 ID: EM SC loose 1.5 NS hypo homog weak yes GTR NS imp NS Brunori, et al., , M arm paresthesias & weakness; Oc C3 TD: EM dura 9.0 NS NS homog str yes GTR 12 mos imp NS urinary retention 46, F lt leg sciatica 8 mos T12 L1 ID: EM NS 1.6 NS NS homog str yes GTR 4 mos imp no Kanahara, et al., , M leg numbness 1 yr C6 7 ID: IM EM NS 1.0 hypo hypo homog weak yes NS NS NS NS Kataoka, et al., , F arm & leg numbness 2 yrs C-5 TD: EM C-5 root, dura 4.0 NS NS irregular yes NS NS NS NS Donnellan, et al., , F low-back pain, leg numbness 7 mos L-1 ED NS 2.0 iso iso homog str yes GTR unclear imp no & weakness Mordani, et al., , M arm & leg paresthesias C-5 ID: IM NS ~1.5 iso hypo irregular yes GTR 18 mos NS no Vorster, et al., , M leg numbness 18 mos T2 3 ID: EM SC firm ~1.5 NS hypo homog str yes GTR 7 mos sbl no Kurtkaya, et al., , F right leg weakness 1 mo T-3 ID: EM dura ~2.0 iso hypo homog str yes GTR 12 mos imp no Obara, et al., , F quadriparesis 1 yr C2 5 ED unclear 8.0 NS iso homog str yes GTR 12 mos imp no present case 48, F neck pain, arm paresthesias 3 yrs C-4 ID: IM EM SC firm 1.5 iso hypo homog str yes GTR 10 mos sbl no * BBI = bowel and bladder incontinence; ED = extradural; EM = extramedullary; GTR = gross-total resection; homog str = homogeneously strong enhancement; homog weak = homogeneously weak enhancement; hypo = hypointense; ID = intradural; IM = intramedullary; imp = improved; iso = isointense; LM = leptomeninges; NS = not stated; SC = spinal cord; sbl = stable; TD = transdural. 361
5 R. J. Bohinski, et al. TABLE 2 Locations of intraspinal solitary fibrous tumors reported in the literature Location No. of Cases extradural only w/ extraspinal extension 1 w/o extraspinal extension 2 intradural only intramedullary 2 extramedullary 4 intra- & extramedullary 3 transdural extramedullary 2 ing appearance, these signal characteristics are nonspecific and indistinguishable from those of a typical meningioma. Although a dural tail sign may be seen in association with intracranial solitary fibrous tumors, it has not been reported for these tumors in the spine. Therefore, an MR imaging documented meningioma-like mass without evidence of a dural tail sign should raise suspicion for a solitary fibrous tumor. Compared with schwannomas, which typically display hyperintense signal on T 2 -weighted sequences, all previously described intraspinal solitary fibrous tumors were either hypointense or isointense on T 2 -weighted sequences. Hence, T 2 signal characteristics may also be of some diagnostic value. Solitary fibrous tumors are similar in gross and histological features to other spindle cell neoplasms. The histopathological findings in our case are typical for such a lesion. Grossly, they are firm, well circumscribed, and pink to tan in color. On H & E staining, tumor cells are found surrounded by dense collagen networks in fascicular, storiform, herringbone, or patternless arrangements. 4,5 Despite the architectural similarity to other spindle cell tumors, the immunohistochemical profile is distinct. 21 The CD34 antigen is a 110-kD transmembrane glycoprotein that was originally described as a marker of human hematopoietic stem cells 8 but it has since been described in a wide variety of mesenchymally based neoplasms, including solitary fibrous tumor. 11 The staining of solitary fibrous tumors with CD34 is characteristically strong and diffuse. 21 Whereas schwannomas and meningiomas typically stain positive for S100 and EMA, respectively, solitary fibrous tumors do not. It should be noted, however, that CD34 staining is not restricted to solitary fibrous tumors and may be seen in hemangiopericytomas, meningiomas, and schwannomas. 6 In hemangiopericytoma, CD34 expression has been reported in 30% of cases, but the staining pattern tended to be focal, patchy and was weaker than that of nearby endothelial cells. 21 In meningiomas, if CD34 staining is present, it is either weak or restricted to areas of increased vascularity. 4,21 Strong and diffuse positive staining for CD34, but negative staining for S100 and EMA, thus primarily distinguishes solitary fibrous tumor from most other spindle cell tumors. Recently, consistent bcl-2 immunoreactivity was reported in both intra- and extrathoracic solitary fibrous tumors, suggesting that it may serve as an additional marker for these tumors. 7,13 Clinical experience with solitary fibrous tumor in the spine is based on relatively short follow-up periods and few cases. Significantly, more of these tumors have been described in the chest and other extrathoracic locations. 2,10 Not surprisingly, their behavior throughout the body is similar. 11,22 Therefore, preliminary inferences about the behavior of these tumors in the spine can be based on their behavior elsewhere. Histologically, the majority of extraspinal solitary fibrous tumors appear to be benign but up to 30% have atypical features. 2,10 Additionally, between 15 and 20% may show local invasion, intrathoracic spread, or distant metastases. 5 Malignant variants of pleural-based solitary fibrous tumor have been reported and usually contain areas of increased mitotic rate and cellular pleomorphism. 18 Whether intra- or extrathoracic, tumor recurrence seems to relate most strongly to the initial extent of resection. Only one of these spine-based tumors has recurred, but this was 5 years after a subtotal resection. 4 Similar clinical behavior following gross-total resection has been observed for intracranial solitary fibrous tumors that arise from the meninges. In 23 reported cases of the latter, only two recurrences have been documented. 17 Recurrence, however, can occur years after apparent gross-total removal, and thus long-term follow up is still recommended. 4,11,17 Conclusions Solitary fibrous tumor should be considered in the differential diagnosis of any intraspinal tumor regardless of location, but an unusual location or absence of anticipated dural or nerve root attachment should raise suspicion for this increasingly recognized diagnosis. The tumor may be misdiagnosed as one of the more common spindle cell tumors of the spine if appropriate immunohistochemical studies are not performed. Gross-total resection remains the mainstay of treatment, providing excellent clinical and oncological outcomes. Recurrence after gross-total resection and malignant variants of solitary fibrous tumor are uncommon. References 1. Alston SR, Francel PC, Jane JA Jr: Solitary fibrous tumor of the spinal cord. Am J Surg Pathol 21: , Briselli M, Mark EJ, Dickersin GR: Solitary fibrous tumors of the pleura: eight new cases and review of 360 cases in the literature. Cancer 47: , Brunori A, Cerasoli S, Donati R, et al: Solitary fibrous tumor of the meninges: two new cases and review of the literature. Surg Neurol 51: , Carneiro SS, Scheithauer BW, Nascimento AG, et al: Solitary fibrous tumor of the meninges: a lesion distinct from fibrous meningioma. A clinicopathologic and immunohistochemical study. Am J Clin Pathol 106: , Chan JK: Solitary fibrous tumour everywhere, and a diagnosis in vogue. Histopathology 31: , Chaubal A, Paetau A, Zoltick P, et al: CD34 immunoreactivity in nervous system tumors. Acta Neuropathol 88: , Chilosi M, Facchetti F, Dei Tos AP, et al: bcl-2 expression in pleural and extrapleural solitary fibrous tumours. J Pathol 181: , Civin CI, Strauss LC, Brovall C, et al: Antigenic analysis of hematopoiesis. III. A hematopoietic progenitor cell surface antigen defined by a monoclonal antibody raised against KG-1a cells. J Immunol 133: ,
6 Cervical solitary fibrous tumor 9. Donnellan RB, Govender D, Chite SH, et al: An unusual presentation of solitary fibrous tumor. Spine 25: , England DM, Hochholzer L, McCarthy MJ: Localized benign and malignant fibrous tumors of the pleura. A clinicopathologic review of 223 cases. Am J Surg Pathol 13: , Hasegawa T, Matsuno Y, Shimoda T, et al: Extrathoracic solitary fibrous tumors: their histological variability and potentially aggressive behavior. Hum Pathol 30: , Kanahara T, Hirokawa M, Shimizu M, et al: Solitary fibrous tumor of the spinal cord. Report of a case with scrape cytology. Acta Cytol 43: , Kataoka H, Akiyama Y, Kubo S, et al: Solitary fibrous tumor of the spinal nerve rootlet: case report and literature survey. Pathol Int 49: , Klemperer P, Rabin C: Primary neoplasms of the pleura. A report of five cases. Arch Pathol 11: , Kurtkaya O, Elmaci I, Sav A, et al: Spinal solitary fibrous tumor: seventh reported case and review of the literature. Spinal Cord 39:57 60, Malek AM, Weller SJ, Price DL Jr, et al: Solitary fibrous tumor presenting as a symptomatic intraspinal mass: case report. Neurosurgery 40: , Martin AJ, Fisher C, Igbaseimokumo U, et al: Solitary fibrous tumours of the meninges: case series and literature review. J Neurooncol 54:57 69, Moran CA, Suster S, Koss MN: The spectrum of histologic growth patterns in benign and malignant fibrous tumors of the pleura. Semin Diagn Pathol 9: , Mordani JP, Haq IU, Singh J: Solitary fibrous tumour of the spinal cord. Neuroradiology 42: , Obara Y, Matsumoto M, Chiba K, et al: Solitary cervical fibrous tumor. Case illustration. J Neurosurg (Spine 1) 98:111, Perry A, Scheithauer BW, Nascimento AG: The immunophenotypic spectrum of meningeal hemangiopericytoma: a comparison with fibrous meningioma and solitary fibrous tumor of meninges. Am J Surg Pathol 21: , Vallat-Decouvelaere AV, Dry SM, Fletcher CD: Atypical and malignant solitary fibrous tumors in extrathoracic locations: evidence of their comparability to intra-thoracic tumors. Am J Surg Pathol 22: , Vorster SJ, Prayson RA, Lee JH: Solitary fibrous tumor of the thoracic spine. Case report and review of the literature. J Neurosurg (Spine 2) 92: , 2000 Manuscript received July 10, Accepted in final form January 13, Address reprint requests to: Laurence D. Rhines, M.D., Department of Neurosurgery, Box 442, The University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Boulevard, Houston, Texas lrhines@mdanderson.org. 363
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