Resection of the intracavernous sinus tumors using a purely endoscopic endonasal approach.

ORIGINAL ARTICLE

Resection of the Intracavernous Sinus Tumors Using a Purely Endoscopic Endonasal Approach Zhang Qiuhang, MD, PhD,* Guo Hongchuan, MD, PhD,* Kong Feng, MD, PhD,* Chen Ge, MD, PhD,* Liang Jiantao, MD, PhD,* Li Mingchu, MD, PhD,* Bao Yuhai, MD, PhD,* and Ling Feng, MD, PhDÞ Abstract: Resection of the cavernous sinus (CS) lesions has been a surgical challenge because the anatomy of the CS presents a high grade of complexity. This report describes the feasibility of the purely endoscopic endonasal approach to the CS. Twenty-five patients with intracavernous sinus tumors were treated with a purely endoscopic endonasal approach. The indications, efficacy, surgical techniques, and complications of this approach were discussed. Gross total resection occurred in 19 cases (76%), subtotal resection occurred in 2 cases (8%), and partial resection occurred in 4 cases (16%) including pituitary adenoma in 10 cases (total 70%; subtotal 10%; partial 20%), meningioma in 6 cases (total 66.6%; subtotal 16.7%, partial 16.7%), schwannoma in 5 cases (100%, total 5), malignant tumor in 4 cases (total 75%; subtotal 25%). All patients experienced resolution or improvement of symptoms. No patient experienced intraoperative complication and new neurological deficit. Only 1 case of postoperative cerebrospinal fluid leakage repaired via endoscopic endonasal approach on the 14th day after the surgery. The purely endoscopic endonasal approach to the CS in appropriately evaluated patients can be used to address a wide variety of benign and malignant tumor pathology with favorable outcomes and a low incidence of complications. Key Words: Cavernous sinus, endoscopic endonasal approach, tumor, surgery (J Craniofac Surg 2014;25: 295Y302)

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ince the early description of the direct surgical treatment of carotid-cavernous fistula through the lateral wall of the cavernous What Is This Box? A QR Code is a matrix barcode readable by QR scanners, mobile phones with cameras, and smartphones. The QR Code links to the online version of the article.

From the *Skull Base Surgery Center and †Department of Neurosurgery, Capital Medical University, Xuanwu Hospital, Beijing, People’s Republic of China. Received June 18, 2013. Accepted for publication September 17, 2013. Address correspondence and reprint requests to Zhang Qiuhang, MD, PhD, Skull Base Surgery Center of Capital Medical University, Xuanwu Hospital, No. 45 Changchunjie St, Xicheng District, Beijing, People’s Republic of China, 100053; E-mail: [email protected] The author reports no conflicts of interest. Copyright * 2014 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000000428

The Journal of Craniofacial Surgery

sinus (CS) was documented by Parkinson’s1 in 1965,1 resection of the CS lesions has been a surgical challenge for the skull base surgeon, because of the anatomical complexity of the CS and the important value of the structures such as the cavernous carotid artery, the third, fourth, sixth, and the first division of fifth cranial nerves (CNs), and the sympathetic plexus contained in this ‘‘jewelry box.’’2 With the introduction of the operating microscope in skull base surgery, the microanatomic studies of the CS and microscopic transcranial and transsphenoidal CS surgery have been described.3Y17 Most of the illustrative cases in the reports of microscopic transsphenoidal approach were only with the grade 0-1 CS involvement based on the Knosp-Steiner criteria14 because the surgical exposure provided by a microscopic transsphenoidal approach is too limited to allow direct visualization of the CS. Recently, anatomic studies and clinical reviews have demonstrated the feasibility of the endoscopic endonasal approach to the CS. Several authors reported their experiences in resection of pituitary adenomas invading the medial wall of the CS with limited numbers.2,18Y28 They suggest that this approach might play a role in the treatment of pituitary adenomas with CS extension or in the biopsy of CS lesions. However, the indications, efficacy, and safety of the endoscopic endonasal approach are not known clearly. The risk of internal carotid artery (ICA) injury, the troublesome CS bleeding, and the technical difficulties are also in the area of the controversy. In this article, we report our experience of treating CS tumors with a purely endoscopic endonasal approach to discuss the indications, efficacy, surgical techniques, and complications of this approach.

PATIENTS AND METHODS Twenty-five patients (12 men and 13 women; mean age, 46.8 years; range, 23Y67 years) with CS tumors were surgically treated using a purely endoscopic endonasal approach at the Skull Base Surgery Center, Capital Medical University, Xuanwu Hospital, by the authors from January 2004 to January 2012. The distribution of tumor pathology was as follows: pituitary adenoma in 10 cases, meningioma in 6 cases, schwannoma in 5 cases, squamous carcinoma in 2 cases, neuroendocrine carcinoma in 1 case, and chondrosarcoma in 1 case. The major symptoms and signs were as follows: headache in 12 patients, oculomotor nerve paralysis in 8 patients, visual dysfunction or blindness in 9 patients, facial numbness in 6 patients, abducens nerve paralysis in 3 patients, hearing loss in 1 patient, and cerebrospinal fluid (CSF) leak in 1 patient (Table 1). Patients with lesions that extended into the CS were included. Records of included patients were reviewed for age, sex, location of tumor, symptoms, pathology, surgical outcomes, complications, and follow-up. Tumor extension into the CS and grade of tumor resection were confirmed by perioperative magnetic resonance imaging (MRI) and intraoperatively based on direct inspection with the endoscope. The classification of El-Kalliny et al11 for CS lesions was used: type I, intracavernous, involving both medial and lateral walls; type II, interdural, in which the tumor extends only into the lateral wall and

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TABLE 1. Surgical Findings and Results in 25 Intracavernous Sinus Tumors via a Purely Endoscopic Endonasal Approach Patient No. Age, y/Sex 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

53/F 30/M 50/M 45/M 44/F 59/F 47/M 24/F 50/M 58/M 67/M 29/F 67/F 49/F 44/F 51/F 50/M

18 19 20 21 22

31/F 36/F 52/M 42/M 67/M

23 24 25

35/F 67/M 23/F

Location of Tumor

Symptoms

Pathology

Bilateral CS, sella, clivus H/a; R III CN palsy Pituitary adenoma Bilateral CS, sella H/a; CSF Pituitary adenoma Bilateral CS, sella H/a; L poor vision Pituitary adenoma Bilateral CS, sella H/a Pituitary adenoma Bilateral CS, sella H/a; R III CN palsy Pituitary adenoma LCS, sella, 3rd ventricle Bilateral poor vision Pituitary adenoma L CS No Pituitary adenoma R CS R III CN palsy Pituitary adenoma Bilateral CS H/a; bilateral poor vision 2 y Pituitary adenoma L CS L poor vision ;L temporal hemianopia Pituitary adenoma L CS L III CN palsy; L blindness Meningioma L CS L poor vision, visual field defect Meningioma L CS, IF L diplopia; L blindness Meningioma L CS No Meningioma L CS; IF Left hearing loss Meningioma L CS; IF L diplopia, L poor vision Meningioma L CS; IF L nasal obstruction; L hyposmia; Trigeminal schwannoma L facial numbness R CS, IF R facial numbness Trigeminal schwannoma R CS, IF R facial numbness Trigeminal schwannoma R CS, IF R facial numbness Trigeminal schwannoma L CS, IF L facial numbness Trigeminal schwannoma L CS, IF L diplopia ; L III CN palsy; Carcinoma L blindness R CS, IF R facial numbness Neuroendocrine carcinoma R CS; sella R VI CN palsy ; R III CN palsy Carcinoma Bilateral CS; left IF L Poor vision ; L III CN palsy Chondrosarcoma

Surgical Outcomes

Complication

Follow-up, mo

Total L total, R partial Total Subtotal Total Partial Total Total Total Total Subtotal Total Total Partial Total Total Total

No CSF rhinorrhea No No No No No No No No No No No No No No No

58 48 18 8 18 80 40 96 8 46 33 47 33 16 53 40 52

Total Total Total Total Total

No No No No No

59 95 53 41 14

Total Total Ltotal; Rpartial

No No No

58 40 10

CS indicates cavernous sinus; F, female; H/a, headache; IF, infratemporal fossa; L, left; M, male; R, right.

between the inner and outer layers; type III, invasive, involving the medial, lateral, superior, inferior, and posterior invasion.11 The goal of surgery preoperatively was to completely remove the tumors and decompress the CS. Postoperative MRI with gadolinium was obtained within 10 days after the surgery. The grade of resection was defined as follows: total removal means no residual tumor; subtotal removal means less than 5% of the tumor remained; and partial removal means less than 30% of the tumor remained.

Surgical Technique The patient, who is under general anesthesia and orotracheal intubation, is positioned supine with their heads slightly extended and turned to the right, facing the surgeon; head clamps were not used. The patient is given third- or fourth-generation cephalosporin antibiotics for perioperative prophylaxis. Zero- and 30-degree wideangle endoscopes with lens diameter of 4 mm and length of 18 cm (Karl Storz, Tuttlingen, Germany) are used. The bilateral nasal membrane was decongested twice by insertion of cotton pieces soaked with 1% dicaine and 1:100,000 adrenaline. The ‘‘three- or four-handed technique’’ was used through the bilateral nasal cavity. The primary surgeon operated with endoscopes and dissecting instruments or drill through the right nasal cavity, and the second surgeon held the appropriately angled instruments and the continuous suction to help keep the surgical field clear through the left nasal cavity while the surgery was performed. Part of the inferior turbinate and the middle turbinate were removed to allow good maneuverability. The posterior septal artery, originating from the lateral sphenopalatine artery and lying between the anteroinferior wall of the sphenoid sinus and the posterior

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septum, was coagulated first. Excessive bleeding was controlled with bipolar or monopolar coagulations.

Medial Approach An incision was made through the posterior septal mucosa to expose the rostrum of the sphenoid sinus. When the anterior wall of the sphenoid sinus was removed, the landmarks on the posterior wall of the sphenoid sinus, including the sellar floor, optic nerve protuberance, ICA protuberance, clival indentation, and opticcarotid recess, were exposed and identified. For the tumors with extension to the pterygopalatine fossa from the midline, the medial pterygoid process was excised surgically by the drill. After the bone of the sella and ICA protuberance were removed with a high-speed drill, the intrasellar tumor was totally removed. Then the tumor involving CS was removed through the medial wall of the CS.

Lateral Approach The uncinate process was removed to open the maxillary sinus and expose the posterior wall of the maxillary sinus and the inferior wall of the orbit. The bone of the medial and inferior wall of the orbit, pterygoid process, foramen rotundum, and ICA protuberance was removed using a diamond drill, elevator, and rongeur to expose the anterior, lateral, and inferior wall of the CS. The medial wall of the CS is opened using a vertical incision (in some cases, the anterior wall of the CS can be opened at the same time) to expose the tumor in the CS. Removal of the tumor between the ICA and the lateral wall with a rongeur, elevator, and appropriately angled suctions was performed. After complete tumor resection, the lateral, superior, posterior, and inferior wall of the CS can be exposed. The field of intracavernous sinus was examined for residual tumor with 0- and 30-degree * 2014 Mutaz B. Habal, MD




wide-field endoscopes. The CS was packed with gelatin sponge, and the dura defects were repaired using an absorbable artificial dura (Ethisorb dura patch; Johnson & Johnson, Woluwe, Belgium) or lata fascia. Finally, the sphenoid sinus packing was used with iodoform gauze for 10 days.

RESULTS In this series, gross total resection occurred in 19 cases (76%), subtotal resection occurred in 2 cases (8%), and partial resection occurred in 4 cases (16%). Histologically, among the 10 patients with pituitary adenoma, 7 (70%) had gross total removal, 1 (10%) had subtotal removal, and 2 (20%) had partial removal. Among the 6 patients with meningioma, 4 (66.7%) had gross total removal, 1 (16.7%) had subtotal removal, and 1 (16.7%) had partial removal. Among the 4 patients with malignant tumor, 3 (75%) had gross total removal, and 1 (25%) had partial removal. All the 5 patients with schwannoma had total removal. All patients experienced resolution or improvement of symptoms. No patient experienced intraoperative complication such as the ICA rupture and injury of the ophthalmic artery and so on. New neurological deficit was not present after surgery. Only 1 case of postoperative CSF leakage (1 of 25, rate 4%) was encountered that developed to delayed meningitis, which was treated with antibiotics. The CSF leak was repaired via endoscopic endonasal approach on the 14th day after the surgery. There were no operative or

Resection of Intracavernous Sinus Tumors

perioperative deaths. At the time of this review, no patient with total removal of the tumor has experienced a recurrence for the follow-up period (8Y96 months).

ILLUSTRATIVE CASES Patient 1 A 53-year-old woman presented with headache for 2 years and right upper eyelid descensus for 2 months. The preoperative enhanced MRI demonstrated a pituitary adenoma with invasion of bilateral CS, greater on the left CS (Figs. 1AYC). She had undergone a transnasal biopsy 3 months before in a local hospital. During the biopsy, there was a sudden onset of headache and loss of consciousness. Computed tomography showed a subarachnoid hemorrhage, whereas the digital subtraction angiography was negative. The patient recovered about 1 month later, but still had right CNs III and IV palsies. Gross total removal of the tumor was achieved using the purely endoscopic endonasal approach in January 2008 at the Skull Base Center, Capital Medical University, Xuanwu Hospital. The surgical procedure took 3 hours; intraoperative bleeding was 2500 mL. Histopathologic examination revealed the lesion was a pituitary adenoma. The postoperative enhanced MRI 1 week after the surgery showed the tumor was removed completely (Figs. 1DYF). Her preoperative headache had disappeared completely by 10 days, and the CN III palsy recovered completely in 3 months postoperatively. No

FIGURE 1. Preoperative sagittal, axial, and coronal (AYC) enhanced MRI image of patient 1 demonstrated an invasive pituitary adenoma with paraclival extension and invasion of bilateral CS, greater on the left CS. Postoperative sagittal, axial, and coronal (DYF) enhanced MRI image 1 week after the surgery showed the tumor was removed completely.

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complications occurred. The patient was discharged on the second week after the surgery. At the time of 58 months’ follow-up evaluation, there was no evidence of recurrence.

Patient 2 A 52-year-old man complained of headache and right-sided facial numbness for 1 year and visual dysfunction for 6 months. Preoperative MRI demonstrated an oval, smooth-edged tumor, approximately 70 53 61 mm, located in the right infratemporal fossa, protruding to the middle cranial fossa, extending to the right CS and compressing the right orbital apex and optic nerve (Figs. 2A, B). The tumor was completely removed via the purely endoscopic endonasal approach in January 2008 (Figs. 2C, D). The surgical time was 2 hours; intraoperative bleeding was 1500 mL. The postoperative histopathologic findings indicated schwannoma. There was no intraoperative or postoperative complications. No recurrence occurred during the follow-up period of 53 months.

Patient 3 A 51-year-old woman presented with a 3 months’ history of progressive left-sided visual loss and diplopia. Preoperative MRI demonstrated a solitary lesion in the left CS (Figs. 3A, B). Gross total


removal of the tumor was achieved in July 30, 2009 (Figs. 3C, D). The whole surgical procedure took 4 hours; intraoperative bleeding was 900 mL. Pathologic diagnosis was meningioma. Her left visual acuity was improved at 1 week after surgery, and she was discharged 10 days after the surgery. There was no a new neurological deficit and no any postoperative complications. At the time of the 40-month follow-up evaluation, there was no evidence of recurrence.

Patient 4 A 23-year-old woman presented with a 3 months’ history of headache, diplopia, bilateral visual acuity decrease, left ptosis, and eyeball fixation. Her right visual acuity was finger-counting, and left was 0.12. Light reflex was weak on the right side, whereas it disappeared on the left side. Her right abducens nerve was palsy. Preoperative MRI demonstrated the lesion in the bilateral CS, sella, clivus, and the left infratemporal fossa (Figs. 4AYC). She underwent purely endoscopic endonasal surgery in December 29, 2011. It took 4 hours for the whole surgical procedure. The intraoperative bleeding was 1900 mL. The pathologic evaluation confirmed chondrosarcoma. Postoperative enhanced MRI showed the lesion in the left CS, sella, clivus, and infratemporal fossa was completely removed, whereas the partial tumor in the right CS remained (Figs. 4DYF). Her left visual acuity and the CNs III and VI palsies were improved at 1 week after

FIGURE 2. Preoperative MRI of patient 2 demonstrated a solitary inhomogeneous enhancing lesion that extended to the right CS (A, B). Postoperative MRI demonstrated the enhancing lesion was completely removed (C, D).

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FIGURE 3. Preoperative MRI demonstrated a solitary inhomogeneous enhancing lesion in the left CS (A, B). Postoperative MRI demonstrated the enhancing lesion was completely removed (C, D).

surgery. She was discharged after 12 days without new neurological deficit and no any other complications. The residual chondrosarcoma was treated by the adjunct radiotherapy, which remained under control after a 10-month follow-up period (Fig. 5).

DISCUSSION The goal of CS surgery is complete tumor resection without creating additional neurological deficits. In the past 2 decades, the microscopic transsphenoidal approaches, which are anatomically directed to the CS, have been suggested for CS lesions.6,7,9 Recently, in an anatomic study, after comparing the microscopic transsphenoidal approach with the endoscopic endonasal approach for CS surgery, Doglietto et al22 have documented that because of the deep, narrow midline corridor provided by the Hardy speculum (retractor), the microscopic transsphenoidal approach does not allow adequate exposure of neurovascular structures in the CS, as well as good maneuverability of instruments. Conversely, the endoscopic endonasal approach can provide the wider vision and clearer view of anatomic structures in CS and can allow a good surgical maneuverability after a wide sphenoidotomy is performed.22 Although different endoscopic endonasal approaches to the CS have been studied in the cadaver dissection,18,22,24 few authors have described their experiences with endoscopic endonasal approaches to the CS, with limited numbers.2,28,29 In the current study, we described

25 CS tumors with various pathologic types surgically treated with purely endoscopic endonasal approach with favorable outcomes. By the purely endoscopic endonasal approach, it is possible to visualize and access both the medial and lateral aspects of the CS from medial and/or lateral corridor. Selection of the medial approach, the lateral approach, or combined medial-lateral approach to the CS depends on the location and the extension of the tumor. During the endoscopic endonasal surgery, 0-degree endoscope is easily and frequently used to achieve good visualization of CS, whereas the 30degree endoscope is helpful in the final exploration. The use of both nostrils can increase the working space and provides better maneuverability for the ‘‘3- or 4-hand technique.’’ A comprehensive understanding of the CS anatomy is critical to avoid complications. The landmarks in CS are the ICA, the third CN, and the maxillary branch of the trigeminal nerve, but those landmarks are not always visible in the presence of a pathologic process. Opening the CS does not cause the peeling away of the periosteal layer of the lateral wall. Only the abducens is left exposed below and lateral to the ICA; the remaining nerves are protected by and embedded between the 2 layers, periosteal and dural, which make up the lateral wall of the CS. Although intraoperative stereotactic navigation could be useful to delineate the extent of tumor and its relationship with the carotid artery, it is difficult to determine the virtual neurovascular structures after the opening of CS and debulking of the tumor



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FIGURE 4. Preoperative MRI demonstrated a solitary inhomogeneous enhancing (A, coronal) and inhomogeneous high T2-weighted signal ( B, axial; C, coronal) lesion in the bilateral CS, sella, clivus, and the left infratemporal fossa. Postoperative enhanced coronal (D) and T2-weighted axial (E) and coronal (F) MRI scans 10 days after the surgery showed the lesion in the left CS, sella, clivus, and infratemporal fossa was completely removed but partial tumor residual in the right CS.

because of soft tissue drift. In our series, the intraoperative navigation was used in only 3 cases. Besides the surgeon’s experience, the pathology type and the density of the tumor impact the extent of tumor removal in the endoscopic endonasal CS surgery. The ideal lesions for the endoscopic approaches are soft tumors such as pituitary adenomas, schwannomas, and some soft meningiomas as well as some malignant tumors without infiltrating the ICA. On the contrary, hard, solid tumors such as meningiomas that are known to infiltrate the ICA and the CNs may limit the indications for endoscopic endonasal approach, but biopsy. Generally, the lateral approach was used in meningiomas, schwannomas, and malignant tumors of CS in our series. Combined approaches were used in cases with lesions involving the multiple adjacent skull base subsites. As shown in Table 1, schwannomas had the highest percentage of 100% gross total resection that may be attributed to the schwannomas being usually located inferiorly and laterally to the ICA. Pituitary adenoma had a higher percentage of gross total resection than meningioma because of the use of combined medial-lateral-anterior approach. Meningiomas represent 41% of all CS neoplasms.30 These tumors are usually close to critical

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structures, such as CNs and ICA, and sometimes infiltrate them.31Y33 To completely remove the tumor, CS should be opened for dissecting the tumor from the intracavernous CNs and from the carotid artery. Total resection of CS meningiomas is not always feasible and when possible is associated with high morbidity and mortality rates, even in centers with the most experienced surgeons. Over the last decade, the most important series of microsurgically treated displayed recurrence and progression rates range from 6% to 25% and 4.5% to 65%, respectively, with a mean 5-year progression-free survival rate of 50%. Furthermore, the mortality and morbidity rates are still high, ranging from 2% to 7% and from 10% to 65%.34 To decrease the complications, stereotactic radiosurgery, or a less radical surgical treatment followed by stereotactic radiosurgery, has been used as alternative procedures.35,36 In our series, 6 meningiomas were totally removed in 3 cases and subtotally and partially removed in 2 cases with no severe morbidity. The data of the current study support the low rate of serious complications encountered in our series of endoscopic endonasal approach to the CS. Only 1 case of pituitary adenoma, which had the preoperative CSF leaks in the sellar floor, had postoperative CSF * 2014 Mutaz B. Habal, MD





FIGURE 5. A 23-year-old woman with chondrosarcoma; intraoperative endoscopic view showed the landmarks on the posterior wall of the sphenoid sinus were exposed and identified after open the anterior wall of the sphenoid sinus (A). The lateral wall of the CS is opened using a vertical incision after puncture (B). The tumor in the left CS was removed using forceps and suction (C). The CNs in the lateral wall of the left CS were exposed (D). The CS segment of left ICA was completely exposed (E). The lateral, superior, posterior, and inferior wall of the CS was exposed after complete removal of the tumors (F). The superior, lateral wall of the right CS and CS segment of right ICA were exposed after partial removal tumor in the right CS (G). Repair the anterior and lateral wall of the left CS with a nasal septal mucosal flap (H). L-CS indicates left cavernous sinus; R-CS, right cavernous sinus; S, suction.

leaks that need surgical treatment. There were no surgery-related perioperative complications. The absence of postoperative CSF leak and other severe morbidities may be attributed to the superior and posterior wall of the CS having no defects. To avoid the fatal morbidity caused by the ICA rupture, only when the safety of ICA is ensured can the pathologies at the superior and posterior wall of CS be managed. Although the surgeons pay attention to prevent ICA through their experience and surgical technique, injury of ICA may still be possible. The endovascular intervention may be necessary in case of carotid artery injury.

CONCLUSIONS The purely endoscopic endonasal approach to the CS in appropriately evaluated patients can be used to address a wide variety of benign and malignant tumor pathologic findings with favorable outcomes and a low incidence of complications. The ideal lesions for the endoscopic approach are soft tumors. In the endoscopic approach, CNs III, IV, V, and VI and the ICA in cavernous sinus can be exposed and prevented.

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