Clinical Neurology and Neurosurgery 136 (2015) 110–115
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Extradural transcavernous approach to cavernous sinus cavernous hemangiomas Mei-Hua Li ∗ , Jian-Lan Zhao, Yi-Yun Li, Chun-Hui Zeng, Geng-Sheng Xu, Tao Hong Department of Neurosurgery, The First Afﬁliated Hospital of Nanchang University, Nanchang 330006, Jiangxi, PR China
a r t i c l e
i n f o
Article history: Received 21 April 2015 Received in revised form 3 June 2015 Accepted 6 June 2015 Available online 9 June 2015 Keywords: Cavernous sinus Extradural approach Cavernous hemangioma
a b s t r a c t Objective: Cavernous sinus cavernous hemangioma (CSCH) is a rare extra-axial vascular lesion and is difﬁcult to be removed due to their location, propensity for profuse bleeding during surgery, and relationship to complex neurovascular structures. The purpose of this study is to report our experience of the removal of CSCHs through a completely extradural transcavernous approach. Methods: Twelve patients with CSCH, who were operated through a purely extradural approach, were retrospectively studied. Clinical symptoms and signs, radiographic characteristics, operative techniques and outcomes of these patients were analyzed. Results: Headache and visual impairment were the most common clinical symptoms, followed by facial hypesthesia and ptosis. Radiographically, CSCHs have a characteristic pattern. On computed tomography (CT) scans, CSCHs are isodense or minimally hyperdense, with an intense homogenous contrast administration. Magnetic resonance image (MRI) scans revealed well-demarcated and hypo- to isointense lesions on T1-weighted images and characteristically, markedly hyperintense lesions on T2-weighted images. The T2-weighted images showed a marked homogeneous and an intense enhancement after contrast administration. All CSCHs were treated by a completely extradural transcavernous approach. Gross total excision was achieved in all 12 patients. Post-operative complication included transient cranial nerve dysfunction for 2–3 months in eight patients, and three patients developed a permanent VI nerve palsy. The follow-up period ranged from 4 to 117 months (mean 62 months), and no patient had experienced tumor recurrence. Conclusion: CSCHs are rare and challenging skull base tumors. The microsurgical resection, using an extradural transcavernous approach which allows complete tumor resection with an acceptable intraoperative and postoperative complications, should be considered as a favorable choice among all treatments. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Intracranial cavernous hemangiomas have been reported to have an incidence rate of 5–13% in all intracranial vascular malformations, and where intracranial cavernous hemangiomas occur most commonly is in the cerebral hemispheres . Cavernous sinus cavernous hemangioma (CSCH) is a rare extra-axial vascular neoplasm accounting for 1–3% of all cavernous sinus tumors [2–4]. These tumors are benign, well-encapsulated neoplasms arising within the conﬁnes of the cavernous sinus that produce symptoms that resulted from the progressive growth of tumors and the mass effect [4,5]. They are notoriously difﬁcult to be removed due to their location, propensity for profuse bleeding during surgery, and
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(M.-H. Li). http://dx.doi.org/10.1016/j.clineuro.2015.06.004 0303-8467/© 2015 Elsevier B.V. All rights reserved.
relationship to complex neurovascular structures [6–8]. Although some authors have described their extensive experience with the surgical treatment of cavernous sinus lesions with good clinical results [8–10], these uncommon tumors remain a neurosurgical challenge. The optimum treatment strategy remains a matter of controversy. Current treatment modalities include microsurgical resection, embolization, fractionated radiation therapy  and, more recently, stereotactic radiosurgery . The purpose of this study is to report our experience of the removal of CSCHs through a completely extradural transcavernous approach with a favorable morbidity. 2. Patients and methods Between January 2004 and March 2014, 12 patients with CSCH underwent operation in our department. All patients were operated through a purely extradural approach. Patients’ clinical ﬁndings,
M.-H. Li et al. / Clinical Neurology and Neurosurgery 136 (2015) 110–115
the size of tumors, surgical outcomes, complications, and long-term follow-up were reviewed. Computed tomography (CT) scans, magnetic resonance image (MRI) and magnetic resonance angiography (MRA) scans were obtained for all patients. Preoperative radiological diagnosis of the CSCH was made in all patients. Postoperative MRI scans were obtained for all patients to determine the extent of tumor removal. The follow-up period ranged from 4 months to 10 years.
4. Surgical technique All 12 patients were approached through a fronto-temporal osteoplastic craniotomy with zygomatic osteotomy. Intraoperative neurological functions about cranial nerves (III, IV, V, and VI) were monitored using commercially available hardware and software (Endeavor CR intraoperative monitor; VIASYS Healthcare, Nicolet Biomedical, Madison, WI). Key steps for the transcavernous approach of our surgery are shown in Fig. 3. The sphenoid ridge was removed using a high-speed electric drill (Midas Rex; Medtronic, Minneapolis, MN, USA) and the superior orbital ﬁssure was opened. The tentorial duplicature over the base of the anterior clinoid process was peeled and the anterior clinoid process was drilled extradurally. The optic canal was deroofed, the extra-cavernous extradural internal carotid artery was exposed. The temporal base was drilled, and the foramen spinosum was opened, and the middle meningeal artery was coagulated and cut. The meningeal layer of the lateral wall of the cavernous sinus was peeled away from the inner membranous layer using sharp and blunt dissection. The cranial nerves (cranial nerves III and IV, as well as V1, V2, and V3) in the lateral wall of the cavernous sinus were completely exposed. The tumor was bulging through either the lateral triangle (Parkinson’s triangle, between cranial nerves IV and V1 or the anterolateral triangle (Mullan’s triangle, between the V1 and V2 nerves). The vascular tumor was dissected and removed along the margin between tumor and the dura mater of cavernous sinus walls. The usual feeders from the meningo-hypophyseal trunk of the intra-cavernous ICA and middle meningeal artery were exposed and coagulated early in the course of the surgery. Cranial nerve VI was exposed in close proximity to the ICA. Lastly, the medial extension of the lesion into the sella was removed. Hemostasis was achieved using gentle packing with degraded cellulose (Surgicel; Johnson & Johnson Medical Ltd., New Yorkshire, United Kingdom), and blood loss was replaced using hemato-cell saver (Autotransfusion unit; Fresenius, Bad Homburg, Germany). Gross total resection was achieved in all patients (Figs. 1 and 2). Post-operative complications included transient cranial nerve dysfunction for 2–3
3. Results The clinical characteristics of patients were summarized in Table 1. There were three men and nine women with a mean age of 45.5 years (range 28–66 years). The duration of symptoms ranged from 3 months to 10 years. Of the 12 patients, 11 presented with headache, 10 with visual impairment, 4 with facial hypesthesia and 4 with ptosis. Of the 10 patients with visual impairment, there were four patients with barely perception of light, three with hand movement close to face, and one vision loss in one of the eyes due to the large tumor size and the long course of the disease. All patients were evaluated preoperatively by CT and contrastenhanced MRI scans. CT scans revealed isodense expansile lesions in the region of the cavernous sinus and middle cranial fossa. Signs of variable bony erosion of the anterior clinoid process, sphenoid ridge, or apex of the petrous bone were also revealed in some cases. No calciﬁcation or tumor necrosis was found in any patients. MRI revealed well-demarcated parasellar lesions, which were hypoor iso-intense on T1-weighted images and hyperintense on T2weighted images, with marked homogeneous enhancement after intravenous administration of contrast in all patients (Fig. 1). The tumors had well-deﬁned borders and extended variably into the sella (Fig. 2) and superior orbital ﬁssure. MRA was performed in all patients, and all tumors were occult despite the intensity vascularity encounted during surgery. No preoperative embolization was performed in any of our cases. Table 1 Demographic and clinical data of patients with cavernous sinus cavernous hemangioma. Extent of resection
GTR GTR GTR GTR GTR GTR GTR GTR GTR GTR GTR GTR
TCO Transient 6th nerve palsy Transient 3rd nerve palsy, Permanent 6th nerve palsy TCO TCO Transient 3rd nerve palsy None Permanent 6th nerve palsy TCO TCO Transient 3rd nerve palsy Transient 6th nerve palsy
EOM full EOM full Permanent 6th nerve palsy Permanent 6th nerve palsy EOM full EOM full EOM full Permanent 6th nerve palsy EOM full EOM full EOM full EOM full
67 85 117 109 74 4 93 65 49 37 23 25
Tumor size (cm)
Symptoms and signs
1 2 3 4 5 6 7 8 9 10 11 12
43/F 60/F 48/M 66/F 58/F 31/F 57/F 42/M 33/F 30/F 28/F 41/M
R L L L L R R R R L L R
6.5 × 6.3 5.5 × 5.0 6.2 × 5.5 6.8 × 6.1 5.9 × 4.8 6.6 × 5.3 4.5 × 4.0 6.4 × 5.6 6.3 × 3.6 5.7 × 4.4 6.1 × 6.2 3.5 × 3.3
H/A, bilateral poor vision H/A, L poor vision, L ptosis, L 3rd nerve palsy H/A, L vision loss H/A, L facial hypesthesia, bilateral poor vision H/A, L poor vision, L ptosis, L 3rd nerve palsy H/A, R facial hypesthesia, R poor vision H/A R facial hypesthesia, R poor vision H/A, R ptosis H/A, L ptosis, L poor vision H/A, L facial hypesthesia, L poor vision H/A
EOM, external ocular movements; F, female; GTR, gross tumor resection; H/A, headache; L, left; M, male; mo, months; R, right; TCO, transient complete ophthalmoplegia; yr, year.
M.-H. Li et al. / Clinical Neurology and Neurosurgery 136 (2015) 110–115
Fig. 1. MRI scans showing a right sellar and parasellar homogenously enhancing mass. (A) Iso-intense on T1-weighted images and (B) hyperintense on T2-weighted images. (C) Marked homogeneous enhancement after intravenous administration of contrast. (D) Postoperative axial contrast-enhanced MRI scans showing complete excision of the hemangioma. (E) Postoperative coronal contrast-enhanced MRI scans showing complete excision of the hemangioma. (F) Histopathology revealing large numbers of thin-walled vascular sinusoids, with single layer of endothelium-lined capillaries, and scanty connective tissue, which demonstrates the diagnosis of CSCH.
Fig. 2. MRI scans showing a right sellar and parasellar homogenously enhancing lesion encasing the right ICA and extending into the sella. (A) Hypo-intense on T1-weighted images. (B) Hyperintense on T2-weighted images. (C) Preoperative axial contrast-enhanced MRI scans showing marked homogeneous enhancement after intravenous administration of contrast. (D) Preoperative coronal contrast-enhanced MRI scans showing marked homogeneous enhancement after intravenous administration of contrast. (E) Postoperative axial contrast-enhanced MRI scans showing total removal of the tumor. (F) Postoperative coronal contrast-enhanced MRI scans showing total removal of the tumor.
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months in eight patients, and permanent VI nerve palsy in three patients. Vision improved in all patients with pre-operative visual diminution, but not in the case with pre-operative complete vision loss. Among those patients with pre-operation facial hypesthesia, partial improvement was achieved in two patients, while the other two patients remained essentially unchanged. In the eight patients without trigeminal nerve impairment before surgery, three patients developed additional trigeminal nerve disturbance, but resolved completely in 3 months after surgery. Postoperative MRI scans revealed gross total excision in all 12 patients. Histopathology revealed CSCH in all patients. All patients were evaluated clinically and by imaging 3 months after surgery and then on an annual basis. After a 4–117 months (mean, 62 months) follow-up, no patient had experienced tumor recurrence. 5. Discussion 5.1. Clinical and radiographic features CSCHs are rare vascular tumors that consist of endothelium linked vascular spaces. Typically, small tumors are located in the region of the cavernous sinus. As the tumors grow, they extend to and even occupy the entire middle cranial fossa. All features of these tumors presented their extradural locations, and the involvement of cranial nerves III, IV, and V, the pseudocapsule of the tumor and the encasement of intracavernous ICA by the tumor, which supported the hypothesis that these tumors arise within the cavernous sinus, as suggested by Linskey and Sekhar . The onset of clinical symptoms of these tumors is usually insidious, and symptoms are caused by the large size of the tumors . Patients usually present with headache and dysfunctions of the cranial nerves passing through the cavernous sinus, especially the ptosis and diplopia. Optic acuity is decreased when the optic nerve is compressed. Facial numbness or neuralgia may occur if the gasserian ganglion and cranial nerves V are involved. Unlike intraaxial cavernous hemangiomas, of which the hemorrhagic incidence is approximately 25% , CSCHs rarely exhibit bleeding. Another important characteristic of these tumors is that the majority of these patients are female. Radiographically, CSCHs have a characteristic pattern of extension toward the sella, superior orbit ﬁssure and Meckel’s cave as they grow. On CT scans, CSCHs are isodense or minimally hyperdense, with intense homogenous contrast administration. They may present pressure erosion of the petrous bone . MRI scans revealed well-demarcated and hypo- to isointense lesions on T1weighted images and characteristically, markedly hyperintense lesions on T2-weighted images, with marked homogeneous and intense enhancement after contrast administration . 5.2. Treatments to CSCH
Fig. 3. (A) Intraoperative photograph (a right fronto-temporal osteoplastic craniotomy with zygomatic osteotomy) showing the exploration of the superior orbital ﬁssure (SOF) after the drilling of the anterior clinoid process and the tumor (T). (B). Intraoperative photograph showing the extradural exposure of the cavernous hemangioma after peeling the outer meningeal layer (black arrow) away from the inner membranous layer (white arrow). (C) The tumor was totally removed through Parkinson’s triangle (between Cranial Nerve IV and V1) and Mullan’s triangle (between the V1 and V2 nerves). IV, trochlear nerve; V1, ophthalmic nerve; V2, maxillary nerve; V3, mandibular nerve.
A complete extradural approach was used to resect CSCHs in this decade considering that these tumors arise within the cavernous sinus [5,8–10]. Cranial nerves III, IV, and V (V1, V2, and V3) are always found stretched over the surface of the tumor in the overlying dura. The VI cranial nerve is the only cranial nerve truly within the cavernous sinus, and it mostly runs through the substance of the tumor. As the tumor growing laterally, it gradually dissected the two layers of dura lining the ﬂoor of the middle fossa so that it comes underneath cranial nerve V2 and, eventually, cranial nerve V3. Because of the presence of the pseudocapsule, there will always be a potential plane between the tumor and the overlying dura and cranial nerves. This plane makes it technically easy to preserve cranial nerves III, IV, and V (V1, V2, V3) when removing a cavernous hemangioma . A few series of CSCH surgery had been
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Table 2 Surgical outcomes in the recent series of cavernous sinus cavernous hemangioma surgeries. Authors
Mean follow-up (Mo)
Totally resection rate (%)
Complications rate (%)
Zhou et al.  Goel et al.  Suri et al.  Yin et al.  Bansal et al. 
2003 2003 2007 2013 2014
13 13 7 22 13
36 45 23.7 53 21
Intradural and extradural Extradural Extradural Extradural Extradural
92.3 92.3 85.7 81.8 92.3
0 0 0 0 0
N/A N/A 85.7 76 76.9
Mo, months; N/A, not available.
published in last decade (Table 2). In 2003, Goel et al.  described their experience with 13 cases of CSCHs, seven of which were operated by the complete extradural approach. Of these 13 cases, 12 patients had a complete tumor resection. The cranial nerve outcome in their series was poor, perhaps due to the large size of the tumors at diagnosis. Zhou et al.  retrospectively analyzed 20 surgically treated cases of CSCH, 13 of which were treated using the complete extradural approach. Complete tumor removal was achieved in 12 cases and all patients in this group were improved without tumor recurrence at a mean follow-up period of 3 years. Recently, Bansel and Suri et al. [9,10] reported their experience of 22 patients with CSCH over 14 years at a tertiary care center. Among these 22 patients, 13 were managed with microsurgical resection using a purely extradural transcavernous approach and nine with Gamma Knife radiosurgery. All but one patient had complete tumor excision in the surgical series. Transient ophthalmoparesis was the most common surgical complication. The optimum treatment strategy is still controversial. Current treatment modalities for symptomatic hemangiomas include microsurgical resection, embolization, fractionated radiation therapy, and stereotactic radiosurgery. Complete resection of cavernous sinus hemangioma is potentially curative but may be complicated by severe intraoperative hemorrhage and the complicated neurovascular structures. Because of the high possibility of profuse bleeding during surgical intervention combined with potential for long-term cranial nerve deﬁcits, some practitioners have focused on radiotherapy and stereotactic radiosurgery for treatment of these lesions. In most reports, radiosurgery is used as adjuvant therapy after partial tumor removal. Radiosurgery has also been used as the primary treatment modality with good results for several patients . Tumor shrinkage could be obtained using a relatively high dose; however, the critical structures around the cavernous sinus, such as the optic apparatus, usually limit the use of high radiation doses, especially for the treatment of large CSCHs. Therefore, microsurgical resection remains to be the ﬁrst choice for the treatment of radiation-resistant or large CSCHs, especially with optic apparatus compression. The ideal treatment for CSCH is total tumor removal with the preservation of neurological function. However, the surgery is difﬁcult because of the complex structures of the cavernous sinus, encased cranial nerves and ICA, and severe intraoperative bleeding [16,17]. Preoperative radiotherapy to decrease tumor size and vascularity , intraoperative hypothermia, vascular occlusion, and intraoperative hypotension had been suggested by some surgeons during surgery for successful and safe tumor excision . In our series, none of these techniques was used concerning the risk of their relative side effects. In our cases, we performed a basal temporal craniotomy with zygomatic osteotomy. We found that the extradural approach was the most appropriate route for these intracavernous sinus tumors. Temporal base drilling, widely exposure of the optic canal, superior orbital ﬁssure, and foramina spinosum, ovale, and rotundum was crucial. The dissection of the meningeal layer of the cavernous sinus lateral wall from the inner membranous layer enclosing the III, IV, V1, V2, and V3 cranial nerves was the key step. The triangles
for entry should be the anterolateral triangle (between cranial nerves V1 and V2) and the lateral triangle (between cranial nerves IV and V1) depending on the exact location of the tumor and the location of the maximum tumor bulge in the lateral wall of the cavernous sinus, but staying as far away from the III cranial nerve as possible to reduce the morbidity of oculomotor nerve palsy. Although en bloc resection is not possible in very large tumor, we do not advocate rapid decompression of the tumor via suction or via an ultrasonic surgical aspirator because it may result in increased blood loss and occasionally compulsive intraoperative bleeding, which has been reported to be as high as 12.5% in recent articles but older series reported up to 36% . Our surgical points included maximum dissection of the meningeal layer of the cavernous sinus lateral wall from the inner membranous layer, and early access to the arterial feeders from the meningo-hypophyseal trunk of the inter-cavernous ICA and middle meningeal artery, because early coagulation of the feeders results in a marked reduction of tumor vascularity, tumor volume and blood loss. Once the bulk of the tumor were reduced and devasculized, the hemostasis was usually spontaneous and tumor can be removed piecemeally. The VI cranial nerve could not be identiﬁed in its course within the cavernous sinus in two patients. It could be completely preserved in 9 of 10 cases which the VI cranial nerve could be identiﬁed. Of 12 patients, 11 suffered from complete or partial ophthalmoplegia in the immediate postoperative phase, and extraocular movements completely recovered in eight patients about 2–3 months following surgery. Three patients developed a permanent VIth cranial nerve palsy. 6. Conclusion CSCHs are rare and challenging skull base tumors. The microsurgical resection, using an extradural transcavernous approach which allows complete tumor resection with an acceptable intraoperative and postoperative morbidity, should be considered as the choice of a favorable choice among all treatments. Conﬂict of interest The authors declare that there are no conﬂicts of interest. Acknowledgments Since starting this research program at the ﬁrst afﬁliated hospital of Nanchang University in Nanchang, Professor Geng-Sheng Xu, MD, has supported the author’s interest. I am grateful to his support and help, and to everyone in the neurosurgery department in the ﬁrst afﬁliated hospital of Nanchang university. We thank all patients who agreed to join our research. References  Simard JM, Garcia-Bengochea F, Ballinger Jr WE, Mickle JP, Quisling RG. Cavernous angioma: a review of 126 collected and 12 new clinical cases. Neurosurgery 1986;18:162–72.
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