AUTHOR(S): Younis, George; Sawaya, Raymond, M.D. Department of Neurosurgery, The University of Texas, M. D. Anderson Cancer Center, Houston, Texas Neurosurgery 30; 932-934, 1992 ABSTRACT: Malignancy is rare in intracranial meningiomas. Although the topic is widely discussed, there is little agreement in the literature as to the histological and radiological features that warrant the diagnosis of malignant meningioma. Three patients are described who had soft-tissue masses and underlying osteolytic lesions on computed tomography. All three patients also had a large intracranial component that proved to be a malignant meningioma. Rarely do meningiomas have all three of these features. We propose that a meningioma causing osteolysis and soft-tissue extension should be considered malignant until proven otherwise. KEY WORDS: Malignant meningioma; Meningioma recurrence; Osteolysis; Scalp mass INTRODUCTION An osteolytic lesion of the skull may have several causes, including metastatic carcinoma, eosinophilic granuloma, myeloma, fibrous dysplasia, and osteogenic sarcoma (10). The most commonly suspected lesion in adults is metastatic disease; meningiomas are seldom suspected. Meningiomas are associated occasionally with extracranial masses; however, most of these masses, if palpable, are firm and are caused by hyperostosis (2) . Extracranial soft-tissue masses rarely arise in meningiomas. Thus, the presence of both lytic skull lesions and soft-tissue masses is unusual indeed. The following are three such cases, remarkable in that they share the diagnosis of a malignant meningioma. CASE REPORTS Patient 1 In 1977, a 69-year-old man was diagnosed with adenocarcinoma of the prostate and received radiation therapy to the pelvic nodes and the prostate. In January 1982, the patient developed a knot on the left side of his head that was mildly tender and growing. He experienced right arm weakness and dysphasia. A computed tomographic (CT) scan revealed an enhancing mass in the left frontoparietal region and a lytic lesion of the left paramedian and frontotemporal calvarium (Fig. 1). The tumor was excised in January 1983 and diagnosed as a meningothelial meningioma with no apparent
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malignant features. A residual tumor was noted and resected during cranioplasty 8 months later. Because of the moderate number of mitoses, focal necrosis, and some evidence of brain invasion found at the time of the second craniotomy, this mass was diagnosed as a malignant meningioma. In March 1985, the patient experienced difficulty in controlling his seizures, and a recurrent left frontal and parafalcine malignant meningioma was removed. At no time did the patient undergo a gross total resection of his tumor. The patient died in November 1986 from intracranial hypertension. Patient 2 This 80-year-old right-handed woman sought treatment in August 1986 for a right parietal lump and clumsiness of her left arm. She was noted to have a mass lesion eroding through her right parietal skull (Fig. 2). The tumor had infiltrated the inner and outer tables of the bone for 1 to 1.5 cm around its perimeter. This lesion was resected totally in December and was histologically remarkable for focal necrosis and densely cellular anaplastic nuclei but no mitotic figures. The tumor was diagnosed as a meningothelial meningioma, syncytial type. A CT scan showed no evidence of residual tumor. One month later, however, she experienced persisting clumsiness and sensory loss in her left arm. Furthermore, she found walking and moving her left arm difficult and experienced clumsiness in her left leg. In September 1987, we performed a second craniotomy and noted multiple large lobulated tumor masses on the surface of the brain and protruding into the white matter of the parietal lobe (Fig. 3). The tumor on the surface extended sheath-like and infiltrated the artificial dura, which had been placed previously. A gross total resection was accomplished. A histological review revealed moderate mitotic figures and focal necrosis. Since this tumor recurred to a large size approximately 8 months after a total resection and was histologically anaplastic, the diagnosis of a malignant meningioma was made. The patient did well postoperatively, but she still experienced left hand sensory loss and left foot numbness. She received 54 Gy of radiation therapy. As of April 1990, the patient was free of tumor recurrence. Patient 3 This 73-year-old man sought treatment for a large right parieto-occipital lesion in August 1990. When his physician attempted to remove the lesion in his office, it became apparent that the lesion was much deeper than the skin and, in fact, extended through the bone into the cranial cavity. A partial resection was later accomplished at a nearby hospital. A histological review of the tissue at our hospital revealed pleomorphic cells; diffusely infiltrating, dense fibrous connective tissue; a faint whorling pattern; and one mitosis. The final diagnosis on this partial resection was a malignant neoplasm consistent with a meningioma. CT scans and magnetic resonance imaging (MRI)
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Neurosurgery 1992-98 June 1992, Volume 30, Number 6 932 Intracranial Osteolytic Malignant Meningiomas Appearing as Extracranial Soft-Tissue Masses Case Report
DISCUSSION Meningiomas account for 15 to 20% of all intracranial neoplasms (2,16). Although typically benign, 1 to 11% of all meningiomas are malignant (6,11,13,14,16) . Furthermore, 4.2% of meningiomas that are initially histologically benign may later recur as histologically malignant neoplasms (6). Malignant meningiomas typically have a much higher rate of recurrence than their benign counterparts (12). Moreover, the risk of metastasis is increased in malignant cases (12). Although the histology of malignant meningiomas has been studied extensively, the literature shows little agreement on the histological features that positively indicate malignancy. The features most often associated with malignancy are those chosen by the World Health Organization: hypercellularity, loss of cellular architecture, focal necroses, nuclear pleomorphism, brain invasion, and increased numbers of mitotic figures (1,6,8,11-15). Some authors discuss the significance of atypical mitoses, which may include three-group metaphases, ball metaphases, telophase anomalies, and lymphocytetype nuclei consisting of condensed spheric nuclear material exhibiting all the characteristics of normal mitoses (4,11). In any case, the presence of only one of these features does not always indicate malignancy; thus, the degree of malignancy is often difficult to determine initially. In fact, two patients in this series had unrecognized malignant meningiomas after their first craniotomy. As for radiology, Dietemann et al. (3) contend that malignant meningiomas may be suspected by the following CT findings: moderate and heterogeneous contrast enhancement with or without cystic components, irregular tumor margin, and absence of surrounding edema. It is, however, important to note that their series comprised only five malignant meningiomas. According to New et al. (8), more than 50% of malignant meningiomas demonstrate "mushrooming," or extension of the tumor pannus along the surface of the brain at a distance from the main globular mass of the lesion. This was reported in five of seven malignant meningiomas and none of 250 benign meningiomas. On the other hand, in a study of 25 malignant and 205 benign meningiomas by Servo et al. (14), the following observations were
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made: heterogeneous contrast enhancement was seen in 8.1% of benign meningiomas and 4.2% of malignant ones; irregular tumor margin was seen in 3.4% of benign tumors and 12.5% of malignant ones; edema was absent in 43.9% of benign meningiomas and 32.0% of 25 malignant ones; and mushrooming was seen in 21% of 24 malignant meningiomas and 9% of 203 benign ones. None of the differences was significant. Thus, just as there is little histological agreement about indications of malignancy, there is little radiological agreement. In light of this, the characteristics shared by all three of our patients should be a warning of the potential for malignancy at the time these features are manifested. In 1970, Husaini (5) reported a meningioma that appeared as a lump on the forehead. Skull x-rays revealed a lytic lesion in the right frontal region. At surgery, however, there was no evidence of any intracranial component. Histologically, the tumor was composed of some whorl formations, a few psammoma bodies, some cellular pleomorphism, a few areas of necrosis, and very few mitotic figures. Although the diagnosis was a mesenchymal tumor of low malignancy at biopsy, the postoperative diagnosis was clearly a malignant meningioma. The tumor was irradiated and regressed for some time, only to recur about 9 months later. A craniectomy was performed approximately 3 months later, and the patient died the following day of complications resulting from the operative trauma. The operation revealed that the tumor left no impressions on the brain. Thus, although the meningioma reported by Husaini is similar to ours in the appearance of a softtissue mass, osteolytic lesion, and perhaps its malignancy, it was wholly extracranial, whereas our three tumors had extensive intracranial components. Another similar case was presented by McWhorter et al. (7) in 1976. This patient had a lytic skull lesion that involved only the outer table of the skull, leaving the inner table intact. The lesion was removed and, on histological examination, proved to be a meningioma. This patient had no soft-tissue mass, no intracranial extension, and no evidence of malignancy; however, the follow-up time in this patient was short. Some authors state that osteolysis alone may be helpful in predicting the malignancy of meningiomas because osteolytic meningiomas tend to be more aggressive (9). The literature does not address the incidence and significance of soft-tissue masses in malignant meningiomas. Since osteolytic meningiomas, extracranial soft-tissue masses in intracranial meningiomas, and malignant meningiomas are all rare conditions, our cases are especially significant in that each one contains all three of these elements. We therefore contend that osteolysis, when associated with a soft-tissue mass, is a strong reason to suspect a malignant meningioma. ACKNOWLEDGMENT This work was made possible by core grant CA16672. Received for publication, October 8, 1991; accepted, November 20, 1991.
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studies revealed an hourglass-shaped mass with a rather large midpart extending from near the scalp, through the meninges, and compressing the upper part of the brain convexity in the right parietooccipital area (Fig. 4). A craniotomy was performed, and a gross total excision of this intradural, extradural, and extracranial mass with the surrounding bone was accomplished (Fig. 5). A histological review revealed high cellularity, moderate pleomorphism, frequent mitoses, and widespread necrosis, as well as a bromodeoxyuridine index of 1.6%, consistent with a more aggressive meningioma. A diagnosis of a malignant meningioma was made, and 60 Gy of radiation therapy was given. Seven months later, the patient remains free of recurrence (Fig. 6).
Reprint requests: Raymond Sawaya, M.D., Box 64, The University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Blvd., Houston, TX 77030.
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2. 3.
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5. 6.
7. 8.
9. 10.
11.
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13. 14.
15. 16.
Alavarez F, Roda J, Romero MP, Morales C, Sarmiento M, Blazquez M: Malignant and atypical meningiomas: A reappraisal of clinical, histological, and computed tomographic features. Neurosurgery 20:688694, 1987. Cushing H, Eisenhardt L: Meningiomas. Springfield, IL, Charles C Thomas, 1938, pp 462-505. Dietemann H, Heldt N, Burguet JL, Medjek L, Maitrot D, Wackenheim A: CT findings in malignant meningiomas. Neuroradiology 23:207-209, 1982. Fabiani A, Trebini F, Favero M, Peres B, Palmucci L: The significance of atypical mitoses in malignant meningiomas. Acta Neuropathol 38:229-231, 1977. Husaini TA: An unusual osteolytic meningioma. J Pathol 101:57-58, 1970. Jaaskelainen J, Haltia M, Servo A: Atypical and anaplastic meningiomas: Radiology, surgery, radiotherapy, and outcome. Surg Neurol 25:233-242, 1986. McWhorter JM, Ghatak NR, Kelly DL: Extracranial meningioma presenting as lytic skull lesion. Surg Neurol 5:223-224, 1976. New PF, Hesselink JR, O'Carroll CP, Kleinman GM: Malignant meningiomas: CT and histologic criteria, including a new CT sign. AJNR 3:267-276, 1982. Olmsted WW, McGee TP: Prognosis in meningioma through evaluation of skull bone patterns. Radiology 123:375-377, 1977. Pearl GS, Takei Y, Parent AD, Boehm WM: Primary intraosseous meningioma presenting as a solitary osteolytic skull lesion: Case report. Neurosurgery 4:269-270, 1979. Rohringer M, Sutherland GR, Louw DF, Sima AA: Incidence and clinicopathological features of meningioma. J Neurosurg 71:665672, 1989. Rubinstein L: Tumors of the central nervous system, in Rubinstein L (ed): Atlas of Tumor Pathology, series 2, fasc 6. Washington, DC, Armed Forces Institute of Pathology, 1972, pp 186-189. Salcman M: Malignant meningiomas, in AlMefty O (ed): Meningiomas. New York, Raven Press, 1991, pp 75-85. Servo A, Porras M, Jaaskelainen J, Paetau A, Haltia M: Computed tomography and angiography do not reliably discriminate malignant meningiomas from benign ones. Neuroradiology 32:94-97, 1990. Thomas HG, Dolman CL, Berry K: Malignant meningioma: Clinical and pathological features. J Neurosurg 55:929-934, 1981. Zulch K: Brain Tumors . New York, Springer-
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REFERENCES: (1-16)
Figure 2. Patient 2. Extracranial soft-tissue mass (top). Surgically removed meningiomas and right parietal skull with attached tumor mass (bottom).
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Figure 1. Patient 1. Preoperative CT scan shows intracranial component of tumor mass (left) and skull destruction (right).
Figure 4. Patient 3. Preoperative MRI study reveals osteolysis and large intracranial and extracranial tumor mass pressing against the right parietooccipital area.
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Figure 3. Patient 2. Preoperative CT scan reveals a right parietal tumor mass and osteolysis (top left). Postoperative CT scan shows no indication of residual tumor (bottom). Less than 1 year later, two large malignant meningiomas have recurred (top right).
Figure 6. Patient 3. Preoperative CT scan reveals extensive osteolysis and extracranial extension by the malignant meningioma (left). Postoperative CT scan shows cranioplasty and no evidence of a residual tumor (right).
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Figure 5. Patient 3. Surgical photograph shows the bisected malignant meningioma, destruction of the skull, and tumoral invasion of the scalp.
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malignant features. A residual tumor was noted and resected during cranioplasty 8 months later. Because of the moderate number of mitoses, focal necrosis, and some evidence of brain invasion found at the time of the second craniotomy, this mass was diagnosed as a malignant meningioma. In March 1985, the patient experienced difficulty in controlling his seizures, and a recurrent left frontal and parafalcine malignant meningioma was removed. At no time did the patient undergo a gross total resection of his tumor. The patient died in November 1986 from intracranial hypertension. Patient 2 This 80-year-old right-handed woman sought treatment in August 1986 for a right parietal lump and clumsiness of her left arm. She was noted to have a mass lesion eroding through her right parietal skull (Fig. 2). The tumor had infiltrated the inner and outer tables of the bone for 1 to 1.5 cm around its perimeter. This lesion was resected totally in December and was histologically remarkable for focal necrosis and densely cellular anaplastic nuclei but no mitotic figures. The tumor was diagnosed as a meningothelial meningioma, syncytial type. A CT scan showed no evidence of residual tumor. One month later, however, she experienced persisting clumsiness and sensory loss in her left arm. Furthermore, she found walking and moving her left arm difficult and experienced clumsiness in her left leg. In September 1987, we performed a second craniotomy and noted multiple large lobulated tumor masses on the surface of the brain and protruding into the white matter of the parietal lobe (Fig. 3). The tumor on the surface extended sheath-like and infiltrated the artificial dura, which had been placed previously. A gross total resection was accomplished. A histological review revealed moderate mitotic figures and focal necrosis. Since this tumor recurred to a large size approximately 8 months after a total resection and was histologically anaplastic, the diagnosis of a malignant meningioma was made. The patient did well postoperatively, but she still experienced left hand sensory loss and left foot numbness. She received 54 Gy of radiation therapy. As of April 1990, the patient was free of tumor recurrence. Patient 3 This 73-year-old man sought treatment for a large right parieto-occipital lesion in August 1990. When his physician attempted to remove the lesion in his office, it became apparent that the lesion was much deeper than the skin and, in fact, extended through the bone into the cranial cavity. A partial resection was later accomplished at a nearby hospital. A histological review of the tissue at our hospital revealed pleomorphic cells; diffusely infiltrating, dense fibrous connective tissue; a faint whorling pattern; and one mitosis. The final diagnosis on this partial resection was a malignant neoplasm consistent with a meningioma. CT scans and magnetic resonance imaging (MRI)
Redistribution of this article permitted only in accordance with the publisher’s copyright provisions.
Neurosurgery 1992-98 June 1992, Volume 30, Number 6 932 Intracranial Osteolytic Malignant Meningiomas Appearing as Extracranial Soft-Tissue Masses Case Report
DISCUSSION Meningiomas account for 15 to 20% of all intracranial neoplasms (2,16). Although typically benign, 1 to 11% of all meningiomas are malignant (6,11,13,14,16) . Furthermore, 4.2% of meningiomas that are initially histologically benign may later recur as histologically malignant neoplasms (6). Malignant meningiomas typically have a much higher rate of recurrence than their benign counterparts (12). Moreover, the risk of metastasis is increased in malignant cases (12). Although the histology of malignant meningiomas has been studied extensively, the literature shows little agreement on the histological features that positively indicate malignancy. The features most often associated with malignancy are those chosen by the World Health Organization: hypercellularity, loss of cellular architecture, focal necroses, nuclear pleomorphism, brain invasion, and increased numbers of mitotic figures (1,6,8,11-15). Some authors discuss the significance of atypical mitoses, which may include three-group metaphases, ball metaphases, telophase anomalies, and lymphocytetype nuclei consisting of condensed spheric nuclear material exhibiting all the characteristics of normal mitoses (4,11). In any case, the presence of only one of these features does not always indicate malignancy; thus, the degree of malignancy is often difficult to determine initially. In fact, two patients in this series had unrecognized malignant meningiomas after their first craniotomy. As for radiology, Dietemann et al. (3) contend that malignant meningiomas may be suspected by the following CT findings: moderate and heterogeneous contrast enhancement with or without cystic components, irregular tumor margin, and absence of surrounding edema. It is, however, important to note that their series comprised only five malignant meningiomas. According to New et al. (8), more than 50% of malignant meningiomas demonstrate "mushrooming," or extension of the tumor pannus along the surface of the brain at a distance from the main globular mass of the lesion. This was reported in five of seven malignant meningiomas and none of 250 benign meningiomas. On the other hand, in a study of 25 malignant and 205 benign meningiomas by Servo et al. (14), the following observations were
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made: heterogeneous contrast enhancement was seen in 8.1% of benign meningiomas and 4.2% of malignant ones; irregular tumor margin was seen in 3.4% of benign tumors and 12.5% of malignant ones; edema was absent in 43.9% of benign meningiomas and 32.0% of 25 malignant ones; and mushrooming was seen in 21% of 24 malignant meningiomas and 9% of 203 benign ones. None of the differences was significant. Thus, just as there is little histological agreement about indications of malignancy, there is little radiological agreement. In light of this, the characteristics shared by all three of our patients should be a warning of the potential for malignancy at the time these features are manifested. In 1970, Husaini (5) reported a meningioma that appeared as a lump on the forehead. Skull x-rays revealed a lytic lesion in the right frontal region. At surgery, however, there was no evidence of any intracranial component. Histologically, the tumor was composed of some whorl formations, a few psammoma bodies, some cellular pleomorphism, a few areas of necrosis, and very few mitotic figures. Although the diagnosis was a mesenchymal tumor of low malignancy at biopsy, the postoperative diagnosis was clearly a malignant meningioma. The tumor was irradiated and regressed for some time, only to recur about 9 months later. A craniectomy was performed approximately 3 months later, and the patient died the following day of complications resulting from the operative trauma. The operation revealed that the tumor left no impressions on the brain. Thus, although the meningioma reported by Husaini is similar to ours in the appearance of a softtissue mass, osteolytic lesion, and perhaps its malignancy, it was wholly extracranial, whereas our three tumors had extensive intracranial components. Another similar case was presented by McWhorter et al. (7) in 1976. This patient had a lytic skull lesion that involved only the outer table of the skull, leaving the inner table intact. The lesion was removed and, on histological examination, proved to be a meningioma. This patient had no soft-tissue mass, no intracranial extension, and no evidence of malignancy; however, the follow-up time in this patient was short. Some authors state that osteolysis alone may be helpful in predicting the malignancy of meningiomas because osteolytic meningiomas tend to be more aggressive (9). The literature does not address the incidence and significance of soft-tissue masses in malignant meningiomas. Since osteolytic meningiomas, extracranial soft-tissue masses in intracranial meningiomas, and malignant meningiomas are all rare conditions, our cases are especially significant in that each one contains all three of these elements. We therefore contend that osteolysis, when associated with a soft-tissue mass, is a strong reason to suspect a malignant meningioma. ACKNOWLEDGMENT This work was made possible by core grant CA16672. Received for publication, October 8, 1991; accepted, November 20, 1991.
Redistribution of this article permitted only in accordance with the publisher’s copyright provisions.
studies revealed an hourglass-shaped mass with a rather large midpart extending from near the scalp, through the meninges, and compressing the upper part of the brain convexity in the right parietooccipital area (Fig. 4). A craniotomy was performed, and a gross total excision of this intradural, extradural, and extracranial mass with the surrounding bone was accomplished (Fig. 5). A histological review revealed high cellularity, moderate pleomorphism, frequent mitoses, and widespread necrosis, as well as a bromodeoxyuridine index of 1.6%, consistent with a more aggressive meningioma. A diagnosis of a malignant meningioma was made, and 60 Gy of radiation therapy was given. Seven months later, the patient remains free of recurrence (Fig. 6).
Reprint requests: Raymond Sawaya, M.D., Box 64, The University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Blvd., Houston, TX 77030.
1.
2. 3.
4.
5. 6.
7. 8.
9. 10.
11.
12.
13. 14.
15. 16.
Alavarez F, Roda J, Romero MP, Morales C, Sarmiento M, Blazquez M: Malignant and atypical meningiomas: A reappraisal of clinical, histological, and computed tomographic features. Neurosurgery 20:688694, 1987. Cushing H, Eisenhardt L: Meningiomas. Springfield, IL, Charles C Thomas, 1938, pp 462-505. Dietemann H, Heldt N, Burguet JL, Medjek L, Maitrot D, Wackenheim A: CT findings in malignant meningiomas. Neuroradiology 23:207-209, 1982. Fabiani A, Trebini F, Favero M, Peres B, Palmucci L: The significance of atypical mitoses in malignant meningiomas. Acta Neuropathol 38:229-231, 1977. Husaini TA: An unusual osteolytic meningioma. J Pathol 101:57-58, 1970. Jaaskelainen J, Haltia M, Servo A: Atypical and anaplastic meningiomas: Radiology, surgery, radiotherapy, and outcome. Surg Neurol 25:233-242, 1986. McWhorter JM, Ghatak NR, Kelly DL: Extracranial meningioma presenting as lytic skull lesion. Surg Neurol 5:223-224, 1976. New PF, Hesselink JR, O'Carroll CP, Kleinman GM: Malignant meningiomas: CT and histologic criteria, including a new CT sign. AJNR 3:267-276, 1982. Olmsted WW, McGee TP: Prognosis in meningioma through evaluation of skull bone patterns. Radiology 123:375-377, 1977. Pearl GS, Takei Y, Parent AD, Boehm WM: Primary intraosseous meningioma presenting as a solitary osteolytic skull lesion: Case report. Neurosurgery 4:269-270, 1979. Rohringer M, Sutherland GR, Louw DF, Sima AA: Incidence and clinicopathological features of meningioma. J Neurosurg 71:665672, 1989. Rubinstein L: Tumors of the central nervous system, in Rubinstein L (ed): Atlas of Tumor Pathology, series 2, fasc 6. Washington, DC, Armed Forces Institute of Pathology, 1972, pp 186-189. Salcman M: Malignant meningiomas, in AlMefty O (ed): Meningiomas. New York, Raven Press, 1991, pp 75-85. Servo A, Porras M, Jaaskelainen J, Paetau A, Haltia M: Computed tomography and angiography do not reliably discriminate malignant meningiomas from benign ones. Neuroradiology 32:94-97, 1990. Thomas HG, Dolman CL, Berry K: Malignant meningioma: Clinical and pathological features. J Neurosurg 55:929-934, 1981. Zulch K: Brain Tumors . New York, Springer-
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REFERENCES: (1-16)
Figure 2. Patient 2. Extracranial soft-tissue mass (top). Surgically removed meningiomas and right parietal skull with attached tumor mass (bottom).
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Figure 1. Patient 1. Preoperative CT scan shows intracranial component of tumor mass (left) and skull destruction (right).
Figure 4. Patient 3. Preoperative MRI study reveals osteolysis and large intracranial and extracranial tumor mass pressing against the right parietooccipital area.
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Figure 3. Patient 2. Preoperative CT scan reveals a right parietal tumor mass and osteolysis (top left). Postoperative CT scan shows no indication of residual tumor (bottom). Less than 1 year later, two large malignant meningiomas have recurred (top right).
Figure 6. Patient 3. Preoperative CT scan reveals extensive osteolysis and extracranial extension by the malignant meningioma (left). Postoperative CT scan shows cranioplasty and no evidence of a residual tumor (right).
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Figure 5. Patient 3. Surgical photograph shows the bisected malignant meningioma, destruction of the skull, and tumoral invasion of the scalp.
