Peer-Review Reports
The Endoscopic Endonasal Approach for Extradural and Intradural Clivus Lesions Eduardo de Arnaldo Silva Vellutini1,2, Leonardo Balsalobre2,3, Diego Rodrigo Hermann2, Aldo Cassol Stamm2,3
- OBJECTIVE:
To report the use of the endoscopic transnasal transclival approach to treat tumors involving the clivus region.
Key words Chordoma - Clivus - Endonasal - Endoscopic -
- METHODS:
Abbreviations and Acronyms CSF: Cerebrospinal fluid GTR: Gross total resection MRI: Magnetic resonance imaging STR: Subtotal resection From the 1DFV Neurosurgery, São Paulo; 2São Paulo Skull Base Center, São Paulo; and 3 Department of Otolaryngology, Head and Neck Surgery, Federal University of São Paulo, São Paulo, Brazil To whom correspondence should be addressed: Eduardo de Arnaldo Silva Vellutini, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014) 82, 6S:S106-S115. http://dx.doi.org/10.1016/j.wneu.2014.07.031 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
INTRODUCTION Despite progress in new surgical techniques in recent decades, an effective and safe treatment for lesions involving the clivus and adjacent areas is still challenging. A deep surgical field surrounded by a complex anatomy with important neurovascular structures and the infiltrative nature of most tumors located in this area are limiting factors. Many transcranial and transfacial approaches has been described for radical removal of these lesions with low morbidity (2, 4, 5, 18, 29). Performance of endoscopic endonasal surgery has steadily increased in recent years as well as its indications for clivus lesions, replacing classic transfacial approaches in some cases. Major advantages of the transnasal approach include the best lighting in a deep field; no need for brain retraction; and the possibility of dural reconstruction using pedicled flaps of the nasal mucosa, which significantly decrease the risk of postoperative complications (6, 8, 9, 16, 19, 25, 27, 28).
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The clinical records of 38 patients with clivus lesions were retrospectively reviewed to determine the surgical technique used. All patients were surgically treated using any of the options of the endoscopic transnasal transclival approach at the São Paulo Skull Base Center from 2000e2011. A transsphenoidal, transpterygoidal, retropharyngeal, or a combination of approaches was chosen based on the tumor topography.
- RESULTS:
Chordomas were the most frequent tumor (26 of 38), followed by chondrosarcoma (2 of 38). Biopsy only was performed in 6 patients with metastasis to the clivus, and 1 patient with fibrous dysplasia underwent a planned partial resection. Gross total resection (GTR) was achieved in 15 of 31 (48%) patients with indications for GTR. For centrally located tumors, GTR was achieved in 75% (15 of 20 patients). Fistula was the most frequent complication (6 of 31; 19%) but was much lower in the most recent series using the nasoseptal flap (1 of 16; 6%). Tumors with lateral extensions or with previous treatment had the worst results. The presence of intradural extension was not a limiting factor for GTR.
- CONCLUSION:
Endoscopic transnasal surgery is an alternative approach to treatment of clivus lesions, and, in expert hands, this technique can obtain good results. Lateral extension and previous treatment were factors that could make the surgery more difficult. Intradural extension did not limit the radicality of the removal.
In this article, we describe the experience of the São Paulo Skull Base Center in the last 11 years with 38 patients with different clivus tumors. The technical variations of the transnasal endoscopic transclival approaches related to the tumor topography and its influence in the surgical results are discussed. MATERIALS AND METHODS At the São Paulo Skull Base Center during the period 2000e2011, 38 patients including 21 (54.8%) male and 17 (45.2%) female patients with clivus tumors of different etiologies were treated. The mean age of patients was 46 years (range, 6e79 years). The lesions were diagnosed as chordomas in 26 patients, and chondrosarcomas were diagnosed in 2 patients. Others tumors diagnosed were myoepithelioma (1 case), meningioma (1 case), angiosarcoma (1 case), plasmacytoma
(1 case), breast cancer metastasis (2 cases), fibrous dysplasia (1 case), lymphoma (1 case), prostate cancer metastasis (1 case), and adenoid cystic carcinoma (1 case). The most frequent initial symptoms were sixth cranial nerve palsy (61%) and headache (30%). All patients underwent neuroradiologic examinations including magnetic resonance imaging (MRI) and computed tomography scanning during the preoperative and postoperative periods. A bone window computed tomography scan and computed tomography angiography were performed to demonstrate the extent of bone destruction and involvement of skull base arteries. Based on preoperative image screening, the tumor was classified as located in the upper or lower clivus, with or without lateral or intradural extension. The craniocaudal reference was the relationship of the tumor to the floor of the sphenoid sinus. Lateral extension in the upper clivus
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meant that the tumor extended beyond the lateral part of the internal carotid artery. Location in the lower clivus meant the tumor was lateral to the occipital condyle and hypoglossal canal. The tumor extension in the craniocaudal and lateral direction was the determining factor in choosing the type of endoscopic endonasal transclival approach used in these cases. The extent of the surgical resection was assessed by performing MRI at 3 months and 6 months after surgery and every 6e12 months thereafter. The following definitions were applied for degree of resection: gross total resection (GTR) means no residual tumor on microsurgical inspection and no evidence of tumor on MRI 6 months after surgery; subtotal resection (STR) means 20% of tumor remaining (24). All patients underwent variations of the endoscopic transnasal transclival approach based on tumor topography. The purpose of the surgery was radical resection in most cases (31 patients—26 chordomas, 2 chondrosarcomas, 1 meningioma, 1 angiosarcoma, and 1 adenoid cystic carcinoma). In 6 patients with metastatic tumors, the intent of the approach was a biopsy only. In 1 patient (patient number 34 with fibrous dysplasia and nasal obstruction), only a partial removal was planned. The follow-up period ranged from 6 months to 11 years. The patients were classified according to the grade of tumor removal. Two-tailed Fisher exact test was used to detect significant differences in proportions of the analyzed factors; a P value 0.05 was considered a significant result. Odds ratios were calculated by the Woolf method (30) or by the modified method described by Haldane (12) when critical entities were zero. Statistical analysis was performed using SPSS for Mac Version 16.0 (SPSS, Inc., Chicago, Illinois, USA). Surgical Technique Surgery is usually carried out under hypotensive general anesthesia. The patient is positioned supine with the head up from about 30 degrees to reduce venous hemorrhage. New technology is incorporated in the surgical armamentarium if possible, including image guidance, monitoring of cranial nerves (especially abducens nerve [cranial nerve VI], oculomotor nerve
ENDOSCOPIC ENDONASAL APPROACH FOR CLIVUS LESIONS
[cranial nerve III], and caudal cranial nerves), micro-Doppler to identify the course of major vessels, and intraoperative MRI to verify removal. The routine use of lumbar drains or shunts is unnecessary. The first step is preparation of the nasal cavity to allow adequate exposure of the deep surgical field and to enable the creation of a vascularized flap for final reconstruction of the skull base. Access is by the combined binostril approach using the transnasal and transseptal route (26); this allows for a 3- or 4-handed surgical technique with increased angles of approach. A 5-mm 0-degree Hopkins endoscope allows better visualization than the standard 4-mm scope (KARL STORZ GmbH & Co., Tuttlingen, Germany). Topical decongestants via local infiltration are used to maximize nasal patency, to aid the flap elevation and decongest the nose further. A third generation cephalosporin is administered prophylactically. A hemitransfixion septal incision is made, and the mucoperichondrium and mucoperiosteum are elevated from the septum. A pedicled flap is harvested to use in the reconstruction. The flap should be a generous size, larger than the defect that will be produced. To reduce bleeding from the free edges of the mucosal flap and remaining in situ mucosa, the incision is made with a monopolar diathermy needle. In primary cases, when the septum is intact, the flap should be made as anterior as possible and can be started in the mucocutaneous transition; the nasal floor mucosa can be used to enlarge the flap, pedicled all around the vascular bundle of the sphenopalatine foramen. Most of the septal cartilage and bone are removed, leaving a sheet of contralateral mucosa as the remaining septum (an L-shaped cartilage strut to support the nasal dorsum and tip). The inferior turbinate is usually left in situ but may be trimmed if it precludes access. In revision cases or when there is a preexisting septal defect, the flap is harvested from the lateral wall and floor of the nose. In this case, an incision is made under the middle turbinate, and the mucosa is dissected off the lateral wall of the nose, around the inferior turbinate and the nasal cavity floor. A mucosal island is left around the opening of the nasolacrimal duct. The bone of the inferior turbinate can be removed if a lateral flap is harvested. This flap is pedicled around the
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sphenopalatine vessels and can be stored in the maxillary sinus during the surgery. The next step is tumor exposure, which is done based on the tumor extension. There are 3 different variations of the endoscopic transnasal transclival approach: 1) Tumors in the midline of the upper clivus are removed through an endoscopic transnasal transsphenoidal approach. 2) For tumors that extend lateral to the carotid artery, access should be by a transnasal transpterygoidal approach. 3) Tumors in the lower clivus are removed through a transnasal retropharyngeal approach. In most cases, owing to the infiltrative nature of clivus tumors, the surgical approach may be a combination of 2 or all 3 variations (Figure 1). Tumors in the Midline of the Upper Clivus. The anterior wall of the sphenoid sinus is initially removed with a Kerrison
Figure 1. Endoscopic view with total exposure of the clivus. After a wide sphenoidotomy, the bony impression of the bilateral internal carotid artery (ICA), sella (S), and clivus (C) can be seen. The sphenoid floor (SF) is the limit of the lower clivus behind the nasopharynx (NP). The view of different approaches is delineated by the colored areas: transnasal transsphenoidal medial (blue), transpterygoidal (yellow), and retropharyngeal (purple).
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Table 1. Clinical, Radiologic, Histologic, and Surgical Characteristics of Patients Case Age (years)/Sex
Clinical Features
Topography Lateral Extension Intradural UC
Histology
Approach Resection Complications
1
12/female
CN VI
No
Chordoma
TS
GTR
2
53/female
NO, HA
UC
3
46/female
VL, CN V
UC
Lat
No
Chordoma
TS-TP
STR
Bilat
No
Chordoma
TS-TP
STR
4
18/male
CN VI, cervical pain
UC/LC
Lat
Yes
Chordoma
TS-TP-RP
STR
5
36/male
CN III, VI
UC
6
74/male
CN VI, HA
UC
Lat
No
Chordoma
TS-TP
STR
F
Yes
Chordoma
TS
GTR
F, M
7
45/female
CN III, VI, hemiparesis
UC
8
43/male
VL, CN III, VI
UC
No
Chordoma
TS-TP
PR
F, ED, S, D
Yes
Chordoma
TS
PR
F
9
24/male
CN VI, VII
UC
No
Chordoma
TS
GTR
10
26/female
HL, CN VII
UC
11
22/female
HA
UC
No
Chondrosarcoma
TS-TP
PR
Yes
Chordoma
TS
GTR
12
45/female
Hemiparesis
13
63/female
CN VI
UC
Yes
Chordoma
TS
GTR
UC
No
Chordoma
TS
PR
14
56/male
CN VI, dysphasia
UC/LC
Lat
Yes
Chordoma
TS-TP-RP
PR
15
53/female
VL, CN III, V, VI
UC/LC
16
29/male
CN VI
UC
Lat
No
Chordoma
TS-TP-RP
PR
Yes
Chordoma
TS
GTR
17
64/female
CN VI
UC
No
Chordoma
TS
GTR
18
33/male
CN VI, X, XI
UC
Yes
Chordoma
TS
GTR
19
6/female
Brainstem dysfunction
UC
Yes
Chordoma
TS
PR
20
59/male
HA
UC
No
Chordoma
TS-TP
STR
21
78/female
HA, CN VI, III
UC
No
Chordoma
TS
GTR
22
15/male
HA
UC
Yes
Chordoma
TS
GTR
23
28/male
HA
UC
No
Chordoma
TS
GTR
24
53/male
HA
UC
No
Chordoma
TS
GTR
25
56/male
HA
UC
Yes
Chordoma
TS
GTR
26
54/female
CN VI
UC
No
Chondrosarcoma
TS
GTR
27
58/male
CN III, IV, VI
UC
Yes
Chordoma
TS
STR
28
40/male
HA, CN VI
UC
Lat
No
Chordoma
TS-TP
STR
29
32/male
HL
LC
Lat
No
Myoepithelioma
RP
Bx
30
65/female
Dysphagia
LC
Yes
Meningioma
RP
STR
31
39/male
VL, CN VI
UC
No
Angiosarcoma
TS
GTR
32
42/male
CN VI
UC
No
Plasmacytoma
TS
Bx
33
54/female
CN XII
LC
No
Breast cancer metastasis RP
Bx
34
50/male
NO
UC
No
Fibrous dysplasia
TS
PR
35
79/female
CN VI
LC
Lat
No
Lymphoma
RP
Bx
36
64/female
CN VI
UC
Lat
No
Breast cancer metastasis TS
Bx
37
79/male
CN VI
UC
No
Prostate metastasis
Bx
38
56/male
CN VI
LC
No
Adenoid cystic carcinoma RP
Bilat
Lat
Lat
Lat
Lat
TS
CN VI
F, M, P, E, D
S
F, P, M
PE, D
STR
CN, cranial nerve; UC, upper clivus; TS, transsphenoidal approach; GTR, gross total resection; NO, nasal obstruction; HA, headache; Lat, lateral extension; TP, transpterygoid approach; STR, subtotal resection; VL, visual loss; Bilat, bilateral extension; LC, lower clivus; RP, retropharyngeal approach; F, cerebrospinal fluid fistula; M, meningitis; PR, partial resection; ED, endocrinologic dysfunction; S, stroke; D, death; HL, hearing loss; P, pneumocephalus; E, epistaxis; Bx, biopsy; PE, pulmonary embolism.
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Figure 2. Case 35. (A) Intraoperative navigation with computed tomography scans of an inferior clivus lymphoma (yellow). (B) Retropharyngeal approach for biopsy of the tumor (T). Note the vidian nerve (arrow) and the
punch and then drilled out using a cutting burr, as low as possible, to expose the entire clivus and to allow better flap position for skull base reconstruction. The identification of key anatomic structures
transition of the petrous and paraclival internal carotid artery (asterisk). C, clivus; S, sella.
of the sphenoid sinus, such as the floor of the sella, the internal carotid artery prominence, the optic nerve canals, and the upper clivus, is facilitated. Then the mucosa is reflected off the clivus bone.
Table 2. Cases (n ¼ 31) in Which Total Resection Was Attempted Lateral Extension Histology/Surgical Approach Chordoma (n ¼ 26)
Yes (n [ 11) 9 (34.6%)
No (n [ 20) 17 (65.4%)
e
17
TS-TP
7
e
TS-TP-RP
2
e
1 (50%)
1 (50%)
TS
Chondrosarcoma (n ¼ 2) TS
e
1
TS-TP
1
e
Meningioma (n ¼ 1)
e
RP
e
Angiosarcoma (n ¼ 1)
e
TS Adenoid cystic carcinoma (n ¼ 1) RP
e 1 (100%) 1
TS, transsphenoidal; TP, transpterygoid; RP, retropharyngeal.
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1 (100%) 1 1 (100%) 1 e e
Removal of the clivus bone is necessary not only to access the tumor but also to remove the infiltrated bone; this is a requisite for complete tumor removal, and it is done carefully using a 5-mm or 6-mm diamond drill. The limits of bone removal in this access are the floor of the sella superiorly, the internal carotid arteries laterally, and the sphenoid sinus floor inferiorly. Extradural lesions usually can be removed with normal or ultrasonic suction. In the case of chordomas, is very important to verify that the limits of the removed bone are tumor-free. For intradural exposure, if not already breached by the tumor, the dura mater needs to be incised. In extradural tumors with intradural extension, bleeding from the basilar plexus is not as intense because it is partially occluded by the tumor and may signify the infiltration limits. In purely intradural tumors, the basilar venous plexus bleeding can be problematic, and control is achieved using SURGICEL and SURGIFLO (Ethicon, Inc., Somerville, New Jersey, USA). Time, patience, head-up position, and hypotension all help hemostasis. Care is needed to avoid damaging of the sixth cranial nerve, located at two thirds of the way down the clivus between the 2 dural layers.
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Figure 3. Case 22. Chordoma in the upper clivus without lateral extension. (A) Preoperative magnetic resonance imaging scan showing the tumor with an intradural extension. (B) Postoperative magnetic resonance imaging scan after total removal. In the sphenoid sinus, the septal flap covering the clivus defect can be seen. (C) Intraoperative view after total removal. Bulging of arachnoid membrane (A) through the clivus (C), between both internal carotid arteries (ICA) under the sellar floor (S). (D) Postoperative computed tomography scan demonstrates the extent of bone removal.
The internal (meningeal) layer of dura mater is opened in the midline, superiorly in the clivus, avoiding the basilar artery. When the dura mater is opened, bipolar diathermy can be used to control dural bleeding. After careful tumor removal and perfect hemostasis, the reconstruction can begin. Tumors Lateral to the Carotid Artery. For lesions extending lateral to the sphenoid sinus and to the carotid artery, the transnasal transpterygoidal approach complements the transnasal transsphenoidal approach. The key of this approach is centralizing it on the vertical portion of the carotid artery. It is usually combined with the removal of the medial and posterior walls of the maxillary sinus. In most cases, the removal of the ethmoid sinus cells and the middle turbinate is required. In these cases, the nasal septal flap needs to be prepared on the contralateral side because the sphenopalatine artery on the same side of the lesion will be coagulated. The medial wall of the maxillary sinus is removed to create an opening that extends inferiorly to the nasal floor, to the nasolacrimal duct anteriorly, and to the pterygoid plate
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posteriorly. The posterior wall of the maxillary sinus is opened to enlarge the sphenopalatine foramen and to expose the periosteum of the pterygopalatine infratemporal fossae. The pterygoid plates are removed with a drill or Kerrison punch to expose the lateral portion of the sphenoid sinus and the cavernous sinus. Anatomic references that should always be kept in mind are the lamina papyracea, the vidian nerve that runs toward the vertical ascendant portion of the carotid artery, the maxillary artery in the sphenopalatine fossae, and the maxillary portion of the trigeminal nerve, which runs on the maxillary sinus roof. The cranial nerves related to this approach are the abducens nerve, the oculomotor nerve and the trigeminal nerve. In tumors that originate medial to the carotid artery, the nerves will be laterally displaced. Tumors in the Lower Clivus. To deal with tumors originating in the lower clivus, lower than the floor of the sphenoid sinus or that extends to it secondarily, the best approach is the transnasalretropharyngeal. After making the nasal septal flap, the sphenoid sinus is opened
and its entire floor is drilled out. The lateral dissection limits will be the vertical portion of the carotid artery, which can be identified by the vidian nerve canal. Below the sphenoid sinus, the nasopharynx is opened and the longus capitis muscle is exposed. The lateral retraction of this structure allows the exposition of the inferior clivus, the atlantoaxial membrane, the anterior arch of cervical vertebrae C1 and C2. The limits of this dissection are the pharyngeal portion of the carotid artery and the occipital condyle laterally and the soft palate inferiorly. The removal of more than 1/3 of the occipital condyles can create an occipitocervical instability, which needs to be fixed. The cranial nerves related to this approach are the lower cranial nerves, especially the hypoglossal nerve, which runs more anteriorly to the level of the occipital condyle. Care must be taken with the vertebral artery in the lower portion of C2, where it has a more medial course. Reconstruction Successful skull base reconstruction is key to avoid cerebrospinal fluid (CSF) leaks and infectious complications. Dural defects in the clivus region are under more pressure of the cerebrospinal fluid and can be more problematic. The “triple F” technique (fat, fascia, and flap) is used. Free fat grafts are used to fill dead space and form a buttress for a fascia lata inlay graft. More than 1 layer of fascia may be used. The inlay graft and layers of fascia are covered with the pedicled nasoseptal or lateral nasal flap supplied by the sphenopalatine artery. The use of a vascularized flap reduces CSF leaks significantly (9). Fibrin glue is not typically necessary but may be used to hold the graft and flap in position. SPONGOSTAN (Ethicon, Inc.) and GELFOAM (Pfizer, Inc., New York, New York, USA) are used in layers over the flap and followed by packing with gauze soaked in antibiotic cream. The packing is supported by Rapid Rhino 900 (ArthroCare ENT, Sunnyvale, California, USA) or similar packing. RESULTS The endoscopic transnasal transclival approach was used in all patients. GTR was achieved in 15 (48%) of 31 patients, STR was achieved in 9 (29%) patients, and partial resection was achieved in 7 (23%) patients. In 6 patients, surgical planning
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Figure 4. Case 28. Chordoma in the upper clivus with lateral extension. (A) Axial magnetic resonance imaging scan with gadolinium shows the tumor. (B) Intraoperative magnetic resonance imaging scan shows the tumor resection. (C) Intraoperative navigation system. Note the relationship between the internal carotid artery and the tumor. (D) Endoscopic view through the transpterygoid approach of the petrous apex (arrow) after tumor removal, lateral to the right internal carotid artery (ICA).
included a biopsy only (1 myoepithelioma, 1 plasmacytoma, 1 lymphoma, and 3 metastases). In 1 patient with fibrous dysplasia, a partial resection was recommended (Table 1 and Figure 2). Table 2 shows 31 cases in which total resection was attempted, divided in 2 groups (with and without lateral extension). The patients with tumors restricted to the midline (n ¼ 20) (Figure 3) had better results: 15 of 20 tumors (13 chordomas, 1 chondrosarcoma, and 1 angiosarcoma) were totally removed (75%), 2 of 20 (10%) were subtotally removed, and 3 of 20 (15%) were partially removed. In the group of 11 patients (35.5%) with tumors with lateral extensions (Figure 4), only STR (7 of 11; 64%) and partial resection (4 of 11; 36%) could be achieved. The presence of lateral extension of the tumor was a negative predictive factor for GTR (P < 0.001). To evaluate other factors that could influence GTR, the results of patients with tumors without lateral extension were analyzed. Among the patients with midline
tumors, there were no statistical differences related to GTR based on gender, age, surgical approach, histology, presence of intradural extension, or previous surgery (Table 3). There were 13 patients with intradural extension to the posterior fossa (12 chordomas and 1 meningioma) (Figures 5 and 6). GTR was achieved in 7 of 13 (54%) of these cases. In cases of tumors with extension to the posterior fossa but without lateral extension, GTR was observed in 7 of 11 patients (64%). Previous surgeries had been performed in 10 cases. In this group, only 3 patients (30%) had GTR, and the tumor was located medially in the upper clivus (Table 4). In patients operated on for the first time, GTR was achieved in 12 of 21 (57%). Among patients in whom an attempt at radical removal was made, only 5 had tumors infiltrating the lower clivus. In 2 patients (numbers 14 and 15) with chordomas invading the whole clivus, a partial resection was performed. In patient number 4
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with lateral extension of the inferior part, STR was performed. STR was also performed in the patient with meningioma and the patient with adenoid cystic carcinoma. The most frequent complication was CSF fistula occurring in 6 of 31 patients (19%) in whom total removal was attempted. This rate decreased to 1 of 16 patients (6%) after the use of a nasoseptal flap for skull base reconstruction. Preoperative sixth cranial nerve dysfunction could be improved in only 5 of 23 patients (22%). Only 1 patient (number 10) had a new permanent sixth cranial nerve impairment. Other complications were meningitis (3 of 31 patients), endocrinologic dysfunction (1 of 31 patients), pneumocephalus (2 of 31 patients), epistaxis (1 of 31 patients), and stroke (2 of 31 patients). The surgical mortality in our series was 9.5% (3 of 31 patients). Patient number 7 died of contralateral occlusion of the middle cerebral artery. Patient number 12 died of infectious complications secondary to a patent CSF fistula after a fourth surgery and radiotherapy. Patient number 30, with clivus meningioma, died of a pulmonary embolism on the fifth postoperative day. DISCUSSION The most frequent tumors of the clivus are chordomas and chondrosarcomas (1, 4, 14), which arise from embryonic remnants and may display infiltrative and aggressive behavior despite the benign histology (17, 22). There were 28 patients in our series with this diagnosis, and proposed treatment was complete surgical resection followed by radiotherapy and radiosurgery (4, 6, 19, 29). Surgery in 3 other patients with a different histologic diagnosis (meningioma, angiosarcoma, and adenoid cystic carcinoma) had the same goal. Metastases to the clivus are usually secondary to hematogenous dissemination and may have various etiologies (7, 20, 21). The surgical indication is always related to the tumor histology and is followed by radiotherapy. The transnasal transclival endoscopic approach for biopsy in patients with metastases has been demonstrated to be very useful, confirming diagnosis with no associated morbidity. For 1 patient with fibrous dysplasia with nasal obstruction, planned partial resection was the therapeutic management.
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Table 3. Prevalence of Gross Total Resection Based on Gender, Intradural Extension, and Histology of Tumor for 20 Patients with Tumors Restricted to the Midline Gross Total Resection Yes (n [ 15)
No (n [ 5)
Sex
P Value
Total (n [ 20)
0.62
Male
9 (60%)
2 (40%)
11 (55%)
Female
6 (40%)
3 (60%)
9 (45%)
41.7 20.8
Age (years)
47.0 24.5
Intradural extension
0.64
43.1 21.3
0.32
Yes
7 (46.7%)
4 (80%)
No
8 (53.3%)
1 (20%)
Histology
11 (55%) 9 (45%) 0.29
Chordoma
13 (86.7%)
Chondrosarcoma Meningioma Angiosarcoma
4 (80%)
2 (13.3%) —
17 (85%)
—
1 (5%)
1 (20%)
1 (6.7%)
1 (5%)
—
Surgical approach
1 (5%) 0.25
TS
15 (100%)
4 (80%)
RP
—
1 (20%)
Previous surgery
19 (95%) 1 (5%) 0.56
Yes
3 (20.0%)
2 (40.0%)
5 (25.0%)
No
12 (80.0%)
3 (60.0%)
15 (75.0%)
TS, transsphenoidal; RP, retropharyngeal.
Classically, clivus tumors were removed through lateral or posterolateral approaches with the advantages of minimizing CSF fistula and avoiding contamination through paranasal sinuses,
a nonsterile surgical corridor (23). The disadvantage, besides cerebral retraction, was the need to dislocate neural and vascular structures to reach the clivus (10). Considering the midline location and
Figure 5. Case 6. Preoperative magnetic resonance imaging scan of a clivus chordoma with a large intradural extension. The operative view after total tumor removal shows the neurovascular structures of the posterior fossa. B, basilar artery; P, pons; III, oculomotor nerve.
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epidural origin of most clivus lesions, a great development of the anterior surgical approaches could be seen in the past decades. The classic transfacial with external incision and sublabial with lateral osteotomy approaches (2, 5, 18), although cosmetically appropriate, do not enable adequate lateral vision. At the same time, the development of nasosinusal endoscopic surgery allowed expansion of indications beyond paranasal sinuses. Among the factors that permitted evolution of the technique, the multidisciplinary teamwork of ENT surgeons and neurosurgeons stands out. The sum of experiences also permitted the incorporation of intraoperative technologies, such as neuronavigation, MRI, micro-Doppler, and electrophysiologic monitoring, and surgical instruments adapted to the technique (6). Following pioneering work by Jho et al. (15), several series of clivus tumors operated on with an exclusive endoscopic technique reported results similar to the traditional series but with lower complication rates (6, 8-10, 13, 16, 24, 25, 28). From a surgical point of view, the clivus is divided into 3 segments (upper, middle, and lower) delimited by the Dorello canal and the jugular foramen as anatomic landmarks (5, 18). However, these landmarks are not well defined from a ventral view of the clivus, and other classifications are often used. Al-Mefty and Arnautovic (2) designated the upper clivus as the posterior wall of the sphenoid sinus, and Cavallo et al. (3) divided the posterior skull base into cranial (from the posterior interclinoid line to the floor of the sella turcica), middle (from the floor of the sella turcica to the line connecting the hypoglossal canals), and caudal (at the level of the craniovertebral junction) sections. We divide the clivus into 2 segments from the anterior surgical approach aspect: the upper clivus, which is the region above the sphenoid sinus floor, and the lower clivus situated below the sphenoid sinus floor. The separation of tumors based on topography has proven to be useful in the choice of approach and surgical prognosis. Upper clivus tumors (above the sphenoid sinus floor) were operated through the classic transnasal transsphenoidal approach. In lesions with expansion lateral to the carotid artery, the approach was extended to the pterygoid fossa. Lower clivus tumors (below sphenoid sinus floor) were operated
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Figure 6. Case 30. Posterior fossa lower clivus meningeoma. (A) Sagittal view demonstrates the craniocaudal extension of the tumor, lower than the sphenoid sinus. (B) Axial view demonstrates a midline tumor, anterior to the trajectory of the lower cranial nerves. (C) Intraoperative view after a retropharyngeal approach and subtotal resection of the tumor. B, basilar artery; VA, vertebral arteries; MO, medulla oblongata; P, pons; AICA, anterior-inferior cerebellar artery.
through the transnasal retropharyngeal approach. The results of these techniques are compared and discussed here in relation to GTR because there is no consensus on what constitutes STR. Some authors classify STR as a maximum of 20% residual tumor (80% resection) (6, 8, 24), and others define SRT as 95% (10, 28) or 90% (4) resection. Among the 31 patients in our series who were treated with the intention of radical resection of the tumor and with diverse extension of the lesion, we achieved GTR in 15 (48%) patients. Dehdashti et al. (6) described 58% of their patients with GTR and reported several series of chordoma resection through different approaches
(lateral, anterior transfacial, and endoscopic) and with variable tumor extension, obtaining GTR in 33%e66%. Sen et al. (23) reported 53% GTR in 17 patients with chordomas and chondrosarcomas operated with transcranial approaches, and Colli and Al-Mefty (4) reported 49.2% with transcranial and transfacial approaches. Among endoscopic series, Stippler et al. (28) obtained GTR in 45% (n ¼ 9) of patients with chordoma, and Fraser et al. (9) reported 60% complete removal in different types of tumors with indications for radical resection. Komotar et al. (16) compared microscopic and endoscopic series and observed a significantly higher percentage of GTR (61.0% vs. 48.1%, P ¼ 0.010), fewer cranial
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nerve deficits (1.3% vs. 24.2%, P < 0.001), fewer incidences of meningitis (0.9% vs. 5.9%, P ¼ 0.029), less mortality (4.7% vs. 21.6%, P < 0.001), and fewer local recurrences (16.9% vs. 40.0%, P ¼ 0.0001) in the endoscopic cohort. There was no significant difference in the incidence of postoperative CSF leak. If we restrict the group of clivus tumors to intradural or extradural lesions without lateral extension, we obtained GTR in 75% (15 of 20 patients) in our series. This result is similar to GTR in 79% reported by Al-Mefty and Arnautovic (2); these authors used microscopic anterior clivectomy supplemented with endoscopy for midline clivus tumors. The endoscopic technique assisted in visualization and removal of intradural tumors that were not visible under the microscope; this was helpful in 42% of their patients. Series of exclusively endoscopic approaches and series of microscopic and endoscopic approaches have similar outcomes. However, when the surgical team becomes adapted to the endoscopic vision, closer to the surgical field and with better illumination, the endoscopic technique is used throughout the surgery. Another advantage of the endoscopic technique is the use of both nostrils enabling bimanual work, with no restriction in the use of surgical instruments in a less invasive approach. Among the factors that might have had an influence on the radical resection of clivus tumors, the lateral expansion was more decisive. No patient with a lateral expansion tumor had a GTR, whereas GTR was achieved in 75% (P < 0.001) of patients with tumors with no lateral expansion. With the use of an endoscope, the lateral portions of the tumor are visualized; however, the tumor’s adhesions to important neurovascular structures are the limiting factor preventing a radical resection. Nevertheless, in contrast to some authors (6, 23), we believe that the transnasal endoscopic approach, purely transsphenoidal or complemented by a transpterygoid approach, is the first choice for clivus tumors. Eventually, combination with a lateral approach for residual tumor at the occipital condyle (8) or at the posterior petrous apex is needed. The radical removal of tumors that infiltrate the dura mater or expand to posterior fossa increases the chances of postoperative
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Table 4. Cases That Had Previous Surgeries (Chordoma and Chondrosarcoma Cases) Case Number 4
Previous Surgery
Surgical Approach
Resection
2 craniotomies
TS þ TP
ST
epistaxis (1 of 31 patients) are due to the relationship between tumor and neurovascular structures and not the approach itself.
7
4 craniotomies, 1 transnasal approach
TS þ TP
P
CONCLUSIONS
8
2 craniotomies, 1 transnasal approach
TS
P
12
2 craniotomies
TS
GT
As a less invasive and more direct surgical approach than other transfacial approaches, the endoscopic transnasal approach is an effective alternative for treatment of patients with clivus tumors of any origin. Although endoscopic transnasal surgery is mainly indicated for centrally located tumors, tailoring the approach to the anatomy makes it possible to expose and remove clivus tumors with any extension. Early results show this approach to equivalent to other techniques, and it should be considered an important option in cranial base surgery.
14
5 craniotomies, 1 midfacial degloving
TS þ TP
P
15
3 craniotomies
TS þ TP
P
19
1 craniotomy
TS
P
21
1 transnasal approach
TS
GT
25
1 craniotomy/1 transnasal approach
TS
GT
28
2 transnasal approaches
TS þ TP
ST
TS, transsphenoidal; TP, transpterygoid; ST, subtotal; P, partial; GT, gross total.
CSF fistula, a complication that is difficult to manage and related to serious infection and high morbidity. This increased risk of CSF fistula has always been the argument against the use of the anterior surgical corridor for tumor with intradural expansion. However, endoscopic surgery has evolved not only in regard to access to skull base tumors but also in regard to the possibilities of reconstruction of various dural defects. The use of vascularized flaps of the nasal mucosa was first described by Hadad et al. (11) using the septal mucosa. Flaps were subsequently expanded for other possibilities of reconstruction (13), decreasing the chances of CSF fistula. In our series of patients undergoing surgery with the goal of radical resection, the rate of postoperative fistula was high, around 19% (6 of 31 patients). However, if we select patients operated on after the development of mucosal flaps, the incidence decreases to 6% (1 of 16 patients). Fraser et al. (9) described CSF fistula in 4.8% of all transclival approaches, with a rate of 0% in cases in which either the gasket-seal or the septum flap was used. A review of the literature by these authors showed series of cases with CSF fistula rates ranging from 0%e33%. The possibility of reconstruction through the mucous membranes of the nasal cavity also transformed the transnasal endoscopic approach into an approach with less morbidity and improved patients’ functional recovery. Because all possibilities of reconstruction must be preserved, there is
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greater care in handling the nasal structures while performing access. The binostril approach described (26) and used in all transnasal endoscopic skull base surgeries, besides allowing the use of at least 3 instruments through both nostrils, preserves the contralateral septal mucosa avoiding complications such as nasal septal perforation and minimizing crusts in the postoperative period. The possibility of better results with the reconstruction of the skull base, greater experience with endoscopic surgery, and better surgical instruments has resulted in greater ease in removing tumors with intradural and posterior fossa expansion. The presence of dural invasion (intradural) was apparently not a limiting factor in medial tumors. GTR was achieved in 7 of 13 patients with dural invasion and 8 of 18 tumors without dural opening (P ¼ 0.32). As described by other authors (8, 28), previous surgery was also a determining factor in the surgical outcome of our patients. Only 3 of 10 (30%) patients with a prior surgery had a GTR, whereas the rate was 12 of 21 (57%) patients for the rest of the series. In our series, when comparing only midline tumors, this difference was not statistically significant probably because of the lower number of cases. Nasal cavity and intradural adhesions and especially the difficulty of obtaining an adequate mucosal flap for the reconstruction were the greatest obstacles in previously operated patients. Other complications mentioned in Results except for 1 patient with postoperative
REFERENCES 1. Al-Mefty O, Arnautovic KI: Surgical seeding of chordomas. J Neurosurg 95:798-803, 2001. 2. Al-Mefty O, Kadri PAS, Hasan DM, Isolan GR, Pravdenkova S: Anterior clivectomy: surgical technique and clinical applications clinical article. J Neurosurg 109:783-793, 2008. 3. Cavallo LM, Esposito I, Notaris M, Esposito F, Tschabitscher M, Cappabianca P: Endoscopic anatomy of the clivus and posterior fossa. In: Stamm AC, ed. Transnasal Endoscopic Skull Base and Brain Surgery. Stuttgart: Thieme; 2011: 265-274. 4. Colli BO, Al-Mefty O: Chordomas of the craniocervical junction: follow-up review and prognostic factors. J Neurosurg 95:933-943, 2001. 5. Couldwell WT, Weiss MH, Rabb C, Liu JK, Apfelbaum RI, Fukushima T: Variations on the standard transsphenoidal approach to the sellar region, with emphasis on the extended approaches and parasellar approaches: surgical experience in 105 cases. Neurosurgery 55:539-550, 2004. 6. Dehdashti AR, Karabatsou K, Ganna A, Witterick I, Gentili F: Expanded endoscopic endonasal approach for treatment of clival chordomas: early results in 12 patients. Neurosurgery 63:299-309, 2008. 7. Escarda A, Vaquer P, Bonet L, Miralbes S, Gomez C, Obrador A: Clivus metastasis from hepatocarcinoma associated with transarterial hepatic chemoembolization. Gastroenterol Hepatol 29:401-404, 2006. 8. Frank G, Sciarretta V, Calbucci F, Farneti G, Mazzatenta D, Pasquini E: The endoscopic transnasal transsphenoidal approach for the treatment of cranial base chordomas and chondrosarcomas. Neurosurgery 59 (1 Suppl 1): ONS50-ONS57, 2006.
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9. Fraser JF, Nyquist GG, Moore N, Anand VK, Schwartz TH: Endoscopic endonasal minimal access approach to the clivus: case series and technical nuances. Neurosurgery 67 (3 Suppl Operative):ONS150-ONS158, 2010. 10. Fraser JF, Nyquist GG, Moore N, Anand VK, Schwartz TH: Endoscopic endonasal transclival resection of chordomas: operative technique, clinical outcome and review of the literature. J Neurosurg 112:1061-1069, 2010. 11. Hadad G, Bassagasteguy L, Carrau RL, Mataza JC, Kassam A, Snyderman CH, Mintz A: A novel reconstructive technique after endoscopic expanded endonasal approaches: vascular pedicle nasoseptal flap. Laryngoscope 116:1882-1886, 2006. 12. Haldane JBS: The estimation and significance of the logarithm of a ratio of frequencies. Ann Hum Genet 20:309-311, 1956. 13. Harvey RJ, Nogueira JF Jr, Schlosser RJ, Patel SJ, Vellutini E, Stamm AC: Closure of large skull base defects after endoscopic transnasal craniotomy. J Neurosurg 111:371-379, 2009. 14. Heffelfinger MJ, Dahlim DC, MacCarty CS, Beabout JW: Chordomas and cartilaginous tumors at the skull base. Cancer 32:410-420, 1973. 15. Jho HD, Carrau RL, McLaughlin MR, Somaza SC: Endoscopic transsphenoidal resection of a large chordoma in the posterior fossa. Acta Neurochir (Wien) 139:343-347, 1997. 16. Komotar RJ, Starke RM, Raper DM, Anand VK, Schwartz TH: The endoscope-assisted ventral approach compared with open microscopeassisted surgery for clival chordomas. World Neurosurg 76:318-327, 2011. 17. Kuge A, Sato S, Sakurada K, Takemura S, Kikuchi Z, Saito Y, Kayama T: Technical notes on
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endoscopic transnasal transsphenoidal approach for clival chondrosarcoma. Sarcoma 2011:953047, 2011. 18. Liu JK, Decker D, Schaefer SD, Moscatello AL, Orlandi RR, Weiss MH, Couldwell WT: Zones of approach for craniofacial resection: minimizing facial incisions for resection of anterior cranial base and paranasal sinus tumors. Neurosurgery 53:1126-1137, 2003. 19. Lund VJ, Stammberger H, Nicolai P, Castelnuovo P: European position paper on endoscopic management of tumours of the nose, paranasal sinuses and skull base. Rhinol Suppl 22:1-143, 2010. 20. Malloy KA: Prostate cancer metastasis to clivus causing cranial nerve VI palsy. Optometry 78: 55-62, 2007. 21. Marchese-Ragona R, Maria Ferraro S, Marioni G, Staffieri C, Manara R, Restivo DA, Staffieri A: Abducent nerve paralysis: first clinical sign of clivus metastasis from tonsillar carcinoma. Acta Otolaryngol 128:713-716, 2008. 22. O’Connell JX, Renard LG, Liebsch NJ, Efird JT, Munzenrider JE, Rosenberg AE: Base of skull chordoma. A correlative study of histologic and clinical features of 62 cases. Cancer 74:2261-2267, 1994. 23. Sen CN, Sekhar LN, Schramm VL, Janecka IP: Chordoma and chondrosarcoma of the cranial base: an 8-year experience. Neurosurgery 25: 931-940, 1989. 24. Stamm A, Pignatari S: Transnasal endoscopyassisted surgery of the skull base. In: Flint PW, Haughey BH, Lund VJ, Niparko JK, Richardson MA, Robbins KT, Thomas JR, eds. Cummings Otolaryngology Head and Neck Surgery. 5th ed. Philadelphia: Mosby; 2010.
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25. Stamm AC, Balsalobre L, Hermann DR, Chisholm E: Endonasal endoscopic approach to clival and posterior fossa chordomas. Oper Tech Otolaryngol Head Neck Surg 22:274-280, 2011. 26. Stamm AC, Pignatari S, Vellutini E, Harvey RJ, Nogueira JF Jr: A novel approach allowing binostril work to the sphenoid sinus. Otolaryngol Head Neck Surg 138:531-532, 2008. 27. Stamm AC, Pignatari SS, Vellutini E: Transnasal endoscopic surgical approaches to the clivus. Otolaryngol Clin North Am 39:639-656, 2006. 28. Stippler M, Gardner PA, Snyderman CH, Carrau RL, Prevedello DM, Kassam AB: Endoscopic endonasal approach for clival chordomas. Neurosurgery 64:268-278, 2009. 29. Tamaki N, Nagashima T, Ehara K, Motooka Y, Barua KK: Surgical approaches and strategies for skull base chordomas. Neurosurg Focus 10:E9, 2001. 30. Woolf B: On estimating the relation between blood group and disease. Ann Hum Genet 19: 251-253, 1955.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 18 September 2013; accepted 25 July 2014 Citation: World Neurosurg. (2014) 82, 6S:S106-S115. http://dx.doi.org/10.1016/j.wneu.2014.07.031 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
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The Endoscopic Endonasal Approach for Extradural and Intradural Clivus Lesions Eduardo de Arnaldo Silva Vellutini1,2, Leonardo Balsalobre2,3, Diego Rodrigo Hermann2, Aldo Cassol Stamm2,3
- OBJECTIVE:
To report the use of the endoscopic transnasal transclival approach to treat tumors involving the clivus region.
Key words Chordoma - Clivus - Endonasal - Endoscopic -
- METHODS:
Abbreviations and Acronyms CSF: Cerebrospinal fluid GTR: Gross total resection MRI: Magnetic resonance imaging STR: Subtotal resection From the 1DFV Neurosurgery, São Paulo; 2São Paulo Skull Base Center, São Paulo; and 3 Department of Otolaryngology, Head and Neck Surgery, Federal University of São Paulo, São Paulo, Brazil To whom correspondence should be addressed: Eduardo de Arnaldo Silva Vellutini, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014) 82, 6S:S106-S115. http://dx.doi.org/10.1016/j.wneu.2014.07.031 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
INTRODUCTION Despite progress in new surgical techniques in recent decades, an effective and safe treatment for lesions involving the clivus and adjacent areas is still challenging. A deep surgical field surrounded by a complex anatomy with important neurovascular structures and the infiltrative nature of most tumors located in this area are limiting factors. Many transcranial and transfacial approaches has been described for radical removal of these lesions with low morbidity (2, 4, 5, 18, 29). Performance of endoscopic endonasal surgery has steadily increased in recent years as well as its indications for clivus lesions, replacing classic transfacial approaches in some cases. Major advantages of the transnasal approach include the best lighting in a deep field; no need for brain retraction; and the possibility of dural reconstruction using pedicled flaps of the nasal mucosa, which significantly decrease the risk of postoperative complications (6, 8, 9, 16, 19, 25, 27, 28).
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The clinical records of 38 patients with clivus lesions were retrospectively reviewed to determine the surgical technique used. All patients were surgically treated using any of the options of the endoscopic transnasal transclival approach at the São Paulo Skull Base Center from 2000e2011. A transsphenoidal, transpterygoidal, retropharyngeal, or a combination of approaches was chosen based on the tumor topography.
- RESULTS:
Chordomas were the most frequent tumor (26 of 38), followed by chondrosarcoma (2 of 38). Biopsy only was performed in 6 patients with metastasis to the clivus, and 1 patient with fibrous dysplasia underwent a planned partial resection. Gross total resection (GTR) was achieved in 15 of 31 (48%) patients with indications for GTR. For centrally located tumors, GTR was achieved in 75% (15 of 20 patients). Fistula was the most frequent complication (6 of 31; 19%) but was much lower in the most recent series using the nasoseptal flap (1 of 16; 6%). Tumors with lateral extensions or with previous treatment had the worst results. The presence of intradural extension was not a limiting factor for GTR.
- CONCLUSION:
Endoscopic transnasal surgery is an alternative approach to treatment of clivus lesions, and, in expert hands, this technique can obtain good results. Lateral extension and previous treatment were factors that could make the surgery more difficult. Intradural extension did not limit the radicality of the removal.
In this article, we describe the experience of the São Paulo Skull Base Center in the last 11 years with 38 patients with different clivus tumors. The technical variations of the transnasal endoscopic transclival approaches related to the tumor topography and its influence in the surgical results are discussed. MATERIALS AND METHODS At the São Paulo Skull Base Center during the period 2000e2011, 38 patients including 21 (54.8%) male and 17 (45.2%) female patients with clivus tumors of different etiologies were treated. The mean age of patients was 46 years (range, 6e79 years). The lesions were diagnosed as chordomas in 26 patients, and chondrosarcomas were diagnosed in 2 patients. Others tumors diagnosed were myoepithelioma (1 case), meningioma (1 case), angiosarcoma (1 case), plasmacytoma
(1 case), breast cancer metastasis (2 cases), fibrous dysplasia (1 case), lymphoma (1 case), prostate cancer metastasis (1 case), and adenoid cystic carcinoma (1 case). The most frequent initial symptoms were sixth cranial nerve palsy (61%) and headache (30%). All patients underwent neuroradiologic examinations including magnetic resonance imaging (MRI) and computed tomography scanning during the preoperative and postoperative periods. A bone window computed tomography scan and computed tomography angiography were performed to demonstrate the extent of bone destruction and involvement of skull base arteries. Based on preoperative image screening, the tumor was classified as located in the upper or lower clivus, with or without lateral or intradural extension. The craniocaudal reference was the relationship of the tumor to the floor of the sphenoid sinus. Lateral extension in the upper clivus
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meant that the tumor extended beyond the lateral part of the internal carotid artery. Location in the lower clivus meant the tumor was lateral to the occipital condyle and hypoglossal canal. The tumor extension in the craniocaudal and lateral direction was the determining factor in choosing the type of endoscopic endonasal transclival approach used in these cases. The extent of the surgical resection was assessed by performing MRI at 3 months and 6 months after surgery and every 6e12 months thereafter. The following definitions were applied for degree of resection: gross total resection (GTR) means no residual tumor on microsurgical inspection and no evidence of tumor on MRI 6 months after surgery; subtotal resection (STR) means 20% of tumor remaining (24). All patients underwent variations of the endoscopic transnasal transclival approach based on tumor topography. The purpose of the surgery was radical resection in most cases (31 patients—26 chordomas, 2 chondrosarcomas, 1 meningioma, 1 angiosarcoma, and 1 adenoid cystic carcinoma). In 6 patients with metastatic tumors, the intent of the approach was a biopsy only. In 1 patient (patient number 34 with fibrous dysplasia and nasal obstruction), only a partial removal was planned. The follow-up period ranged from 6 months to 11 years. The patients were classified according to the grade of tumor removal. Two-tailed Fisher exact test was used to detect significant differences in proportions of the analyzed factors; a P value 0.05 was considered a significant result. Odds ratios were calculated by the Woolf method (30) or by the modified method described by Haldane (12) when critical entities were zero. Statistical analysis was performed using SPSS for Mac Version 16.0 (SPSS, Inc., Chicago, Illinois, USA). Surgical Technique Surgery is usually carried out under hypotensive general anesthesia. The patient is positioned supine with the head up from about 30 degrees to reduce venous hemorrhage. New technology is incorporated in the surgical armamentarium if possible, including image guidance, monitoring of cranial nerves (especially abducens nerve [cranial nerve VI], oculomotor nerve
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[cranial nerve III], and caudal cranial nerves), micro-Doppler to identify the course of major vessels, and intraoperative MRI to verify removal. The routine use of lumbar drains or shunts is unnecessary. The first step is preparation of the nasal cavity to allow adequate exposure of the deep surgical field and to enable the creation of a vascularized flap for final reconstruction of the skull base. Access is by the combined binostril approach using the transnasal and transseptal route (26); this allows for a 3- or 4-handed surgical technique with increased angles of approach. A 5-mm 0-degree Hopkins endoscope allows better visualization than the standard 4-mm scope (KARL STORZ GmbH & Co., Tuttlingen, Germany). Topical decongestants via local infiltration are used to maximize nasal patency, to aid the flap elevation and decongest the nose further. A third generation cephalosporin is administered prophylactically. A hemitransfixion septal incision is made, and the mucoperichondrium and mucoperiosteum are elevated from the septum. A pedicled flap is harvested to use in the reconstruction. The flap should be a generous size, larger than the defect that will be produced. To reduce bleeding from the free edges of the mucosal flap and remaining in situ mucosa, the incision is made with a monopolar diathermy needle. In primary cases, when the septum is intact, the flap should be made as anterior as possible and can be started in the mucocutaneous transition; the nasal floor mucosa can be used to enlarge the flap, pedicled all around the vascular bundle of the sphenopalatine foramen. Most of the septal cartilage and bone are removed, leaving a sheet of contralateral mucosa as the remaining septum (an L-shaped cartilage strut to support the nasal dorsum and tip). The inferior turbinate is usually left in situ but may be trimmed if it precludes access. In revision cases or when there is a preexisting septal defect, the flap is harvested from the lateral wall and floor of the nose. In this case, an incision is made under the middle turbinate, and the mucosa is dissected off the lateral wall of the nose, around the inferior turbinate and the nasal cavity floor. A mucosal island is left around the opening of the nasolacrimal duct. The bone of the inferior turbinate can be removed if a lateral flap is harvested. This flap is pedicled around the
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sphenopalatine vessels and can be stored in the maxillary sinus during the surgery. The next step is tumor exposure, which is done based on the tumor extension. There are 3 different variations of the endoscopic transnasal transclival approach: 1) Tumors in the midline of the upper clivus are removed through an endoscopic transnasal transsphenoidal approach. 2) For tumors that extend lateral to the carotid artery, access should be by a transnasal transpterygoidal approach. 3) Tumors in the lower clivus are removed through a transnasal retropharyngeal approach. In most cases, owing to the infiltrative nature of clivus tumors, the surgical approach may be a combination of 2 or all 3 variations (Figure 1). Tumors in the Midline of the Upper Clivus. The anterior wall of the sphenoid sinus is initially removed with a Kerrison
Figure 1. Endoscopic view with total exposure of the clivus. After a wide sphenoidotomy, the bony impression of the bilateral internal carotid artery (ICA), sella (S), and clivus (C) can be seen. The sphenoid floor (SF) is the limit of the lower clivus behind the nasopharynx (NP). The view of different approaches is delineated by the colored areas: transnasal transsphenoidal medial (blue), transpterygoidal (yellow), and retropharyngeal (purple).
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Table 1. Clinical, Radiologic, Histologic, and Surgical Characteristics of Patients Case Age (years)/Sex
Clinical Features
Topography Lateral Extension Intradural UC
Histology
Approach Resection Complications
1
12/female
CN VI
No
Chordoma
TS
GTR
2
53/female
NO, HA
UC
3
46/female
VL, CN V
UC
Lat
No
Chordoma
TS-TP
STR
Bilat
No
Chordoma
TS-TP
STR
4
18/male
CN VI, cervical pain
UC/LC
Lat
Yes
Chordoma
TS-TP-RP
STR
5
36/male
CN III, VI
UC
6
74/male
CN VI, HA
UC
Lat
No
Chordoma
TS-TP
STR
F
Yes
Chordoma
TS
GTR
F, M
7
45/female
CN III, VI, hemiparesis
UC
8
43/male
VL, CN III, VI
UC
No
Chordoma
TS-TP
PR
F, ED, S, D
Yes
Chordoma
TS
PR
F
9
24/male
CN VI, VII
UC
No
Chordoma
TS
GTR
10
26/female
HL, CN VII
UC
11
22/female
HA
UC
No
Chondrosarcoma
TS-TP
PR
Yes
Chordoma
TS
GTR
12
45/female
Hemiparesis
13
63/female
CN VI
UC
Yes
Chordoma
TS
GTR
UC
No
Chordoma
TS
PR
14
56/male
CN VI, dysphasia
UC/LC
Lat
Yes
Chordoma
TS-TP-RP
PR
15
53/female
VL, CN III, V, VI
UC/LC
16
29/male
CN VI
UC
Lat
No
Chordoma
TS-TP-RP
PR
Yes
Chordoma
TS
GTR
17
64/female
CN VI
UC
No
Chordoma
TS
GTR
18
33/male
CN VI, X, XI
UC
Yes
Chordoma
TS
GTR
19
6/female
Brainstem dysfunction
UC
Yes
Chordoma
TS
PR
20
59/male
HA
UC
No
Chordoma
TS-TP
STR
21
78/female
HA, CN VI, III
UC
No
Chordoma
TS
GTR
22
15/male
HA
UC
Yes
Chordoma
TS
GTR
23
28/male
HA
UC
No
Chordoma
TS
GTR
24
53/male
HA
UC
No
Chordoma
TS
GTR
25
56/male
HA
UC
Yes
Chordoma
TS
GTR
26
54/female
CN VI
UC
No
Chondrosarcoma
TS
GTR
27
58/male
CN III, IV, VI
UC
Yes
Chordoma
TS
STR
28
40/male
HA, CN VI
UC
Lat
No
Chordoma
TS-TP
STR
29
32/male
HL
LC
Lat
No
Myoepithelioma
RP
Bx
30
65/female
Dysphagia
LC
Yes
Meningioma
RP
STR
31
39/male
VL, CN VI
UC
No
Angiosarcoma
TS
GTR
32
42/male
CN VI
UC
No
Plasmacytoma
TS
Bx
33
54/female
CN XII
LC
No
Breast cancer metastasis RP
Bx
34
50/male
NO
UC
No
Fibrous dysplasia
TS
PR
35
79/female
CN VI
LC
Lat
No
Lymphoma
RP
Bx
36
64/female
CN VI
UC
Lat
No
Breast cancer metastasis TS
Bx
37
79/male
CN VI
UC
No
Prostate metastasis
Bx
38
56/male
CN VI
LC
No
Adenoid cystic carcinoma RP
Bilat
Lat
Lat
Lat
Lat
TS
CN VI
F, M, P, E, D
S
F, P, M
PE, D
STR
CN, cranial nerve; UC, upper clivus; TS, transsphenoidal approach; GTR, gross total resection; NO, nasal obstruction; HA, headache; Lat, lateral extension; TP, transpterygoid approach; STR, subtotal resection; VL, visual loss; Bilat, bilateral extension; LC, lower clivus; RP, retropharyngeal approach; F, cerebrospinal fluid fistula; M, meningitis; PR, partial resection; ED, endocrinologic dysfunction; S, stroke; D, death; HL, hearing loss; P, pneumocephalus; E, epistaxis; Bx, biopsy; PE, pulmonary embolism.
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Figure 2. Case 35. (A) Intraoperative navigation with computed tomography scans of an inferior clivus lymphoma (yellow). (B) Retropharyngeal approach for biopsy of the tumor (T). Note the vidian nerve (arrow) and the
punch and then drilled out using a cutting burr, as low as possible, to expose the entire clivus and to allow better flap position for skull base reconstruction. The identification of key anatomic structures
transition of the petrous and paraclival internal carotid artery (asterisk). C, clivus; S, sella.
of the sphenoid sinus, such as the floor of the sella, the internal carotid artery prominence, the optic nerve canals, and the upper clivus, is facilitated. Then the mucosa is reflected off the clivus bone.
Table 2. Cases (n ¼ 31) in Which Total Resection Was Attempted Lateral Extension Histology/Surgical Approach Chordoma (n ¼ 26)
Yes (n [ 11) 9 (34.6%)
No (n [ 20) 17 (65.4%)
e
17
TS-TP
7
e
TS-TP-RP
2
e
1 (50%)
1 (50%)
TS
Chondrosarcoma (n ¼ 2) TS
e
1
TS-TP
1
e
Meningioma (n ¼ 1)
e
RP
e
Angiosarcoma (n ¼ 1)
e
TS Adenoid cystic carcinoma (n ¼ 1) RP
e 1 (100%) 1
TS, transsphenoidal; TP, transpterygoid; RP, retropharyngeal.
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1 (100%) 1 1 (100%) 1 e e
Removal of the clivus bone is necessary not only to access the tumor but also to remove the infiltrated bone; this is a requisite for complete tumor removal, and it is done carefully using a 5-mm or 6-mm diamond drill. The limits of bone removal in this access are the floor of the sella superiorly, the internal carotid arteries laterally, and the sphenoid sinus floor inferiorly. Extradural lesions usually can be removed with normal or ultrasonic suction. In the case of chordomas, is very important to verify that the limits of the removed bone are tumor-free. For intradural exposure, if not already breached by the tumor, the dura mater needs to be incised. In extradural tumors with intradural extension, bleeding from the basilar plexus is not as intense because it is partially occluded by the tumor and may signify the infiltration limits. In purely intradural tumors, the basilar venous plexus bleeding can be problematic, and control is achieved using SURGICEL and SURGIFLO (Ethicon, Inc., Somerville, New Jersey, USA). Time, patience, head-up position, and hypotension all help hemostasis. Care is needed to avoid damaging of the sixth cranial nerve, located at two thirds of the way down the clivus between the 2 dural layers.
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Figure 3. Case 22. Chordoma in the upper clivus without lateral extension. (A) Preoperative magnetic resonance imaging scan showing the tumor with an intradural extension. (B) Postoperative magnetic resonance imaging scan after total removal. In the sphenoid sinus, the septal flap covering the clivus defect can be seen. (C) Intraoperative view after total removal. Bulging of arachnoid membrane (A) through the clivus (C), between both internal carotid arteries (ICA) under the sellar floor (S). (D) Postoperative computed tomography scan demonstrates the extent of bone removal.
The internal (meningeal) layer of dura mater is opened in the midline, superiorly in the clivus, avoiding the basilar artery. When the dura mater is opened, bipolar diathermy can be used to control dural bleeding. After careful tumor removal and perfect hemostasis, the reconstruction can begin. Tumors Lateral to the Carotid Artery. For lesions extending lateral to the sphenoid sinus and to the carotid artery, the transnasal transpterygoidal approach complements the transnasal transsphenoidal approach. The key of this approach is centralizing it on the vertical portion of the carotid artery. It is usually combined with the removal of the medial and posterior walls of the maxillary sinus. In most cases, the removal of the ethmoid sinus cells and the middle turbinate is required. In these cases, the nasal septal flap needs to be prepared on the contralateral side because the sphenopalatine artery on the same side of the lesion will be coagulated. The medial wall of the maxillary sinus is removed to create an opening that extends inferiorly to the nasal floor, to the nasolacrimal duct anteriorly, and to the pterygoid plate
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posteriorly. The posterior wall of the maxillary sinus is opened to enlarge the sphenopalatine foramen and to expose the periosteum of the pterygopalatine infratemporal fossae. The pterygoid plates are removed with a drill or Kerrison punch to expose the lateral portion of the sphenoid sinus and the cavernous sinus. Anatomic references that should always be kept in mind are the lamina papyracea, the vidian nerve that runs toward the vertical ascendant portion of the carotid artery, the maxillary artery in the sphenopalatine fossae, and the maxillary portion of the trigeminal nerve, which runs on the maxillary sinus roof. The cranial nerves related to this approach are the abducens nerve, the oculomotor nerve and the trigeminal nerve. In tumors that originate medial to the carotid artery, the nerves will be laterally displaced. Tumors in the Lower Clivus. To deal with tumors originating in the lower clivus, lower than the floor of the sphenoid sinus or that extends to it secondarily, the best approach is the transnasalretropharyngeal. After making the nasal septal flap, the sphenoid sinus is opened
and its entire floor is drilled out. The lateral dissection limits will be the vertical portion of the carotid artery, which can be identified by the vidian nerve canal. Below the sphenoid sinus, the nasopharynx is opened and the longus capitis muscle is exposed. The lateral retraction of this structure allows the exposition of the inferior clivus, the atlantoaxial membrane, the anterior arch of cervical vertebrae C1 and C2. The limits of this dissection are the pharyngeal portion of the carotid artery and the occipital condyle laterally and the soft palate inferiorly. The removal of more than 1/3 of the occipital condyles can create an occipitocervical instability, which needs to be fixed. The cranial nerves related to this approach are the lower cranial nerves, especially the hypoglossal nerve, which runs more anteriorly to the level of the occipital condyle. Care must be taken with the vertebral artery in the lower portion of C2, where it has a more medial course. Reconstruction Successful skull base reconstruction is key to avoid cerebrospinal fluid (CSF) leaks and infectious complications. Dural defects in the clivus region are under more pressure of the cerebrospinal fluid and can be more problematic. The “triple F” technique (fat, fascia, and flap) is used. Free fat grafts are used to fill dead space and form a buttress for a fascia lata inlay graft. More than 1 layer of fascia may be used. The inlay graft and layers of fascia are covered with the pedicled nasoseptal or lateral nasal flap supplied by the sphenopalatine artery. The use of a vascularized flap reduces CSF leaks significantly (9). Fibrin glue is not typically necessary but may be used to hold the graft and flap in position. SPONGOSTAN (Ethicon, Inc.) and GELFOAM (Pfizer, Inc., New York, New York, USA) are used in layers over the flap and followed by packing with gauze soaked in antibiotic cream. The packing is supported by Rapid Rhino 900 (ArthroCare ENT, Sunnyvale, California, USA) or similar packing. RESULTS The endoscopic transnasal transclival approach was used in all patients. GTR was achieved in 15 (48%) of 31 patients, STR was achieved in 9 (29%) patients, and partial resection was achieved in 7 (23%) patients. In 6 patients, surgical planning
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Figure 4. Case 28. Chordoma in the upper clivus with lateral extension. (A) Axial magnetic resonance imaging scan with gadolinium shows the tumor. (B) Intraoperative magnetic resonance imaging scan shows the tumor resection. (C) Intraoperative navigation system. Note the relationship between the internal carotid artery and the tumor. (D) Endoscopic view through the transpterygoid approach of the petrous apex (arrow) after tumor removal, lateral to the right internal carotid artery (ICA).
included a biopsy only (1 myoepithelioma, 1 plasmacytoma, 1 lymphoma, and 3 metastases). In 1 patient with fibrous dysplasia, a partial resection was recommended (Table 1 and Figure 2). Table 2 shows 31 cases in which total resection was attempted, divided in 2 groups (with and without lateral extension). The patients with tumors restricted to the midline (n ¼ 20) (Figure 3) had better results: 15 of 20 tumors (13 chordomas, 1 chondrosarcoma, and 1 angiosarcoma) were totally removed (75%), 2 of 20 (10%) were subtotally removed, and 3 of 20 (15%) were partially removed. In the group of 11 patients (35.5%) with tumors with lateral extensions (Figure 4), only STR (7 of 11; 64%) and partial resection (4 of 11; 36%) could be achieved. The presence of lateral extension of the tumor was a negative predictive factor for GTR (P < 0.001). To evaluate other factors that could influence GTR, the results of patients with tumors without lateral extension were analyzed. Among the patients with midline
tumors, there were no statistical differences related to GTR based on gender, age, surgical approach, histology, presence of intradural extension, or previous surgery (Table 3). There were 13 patients with intradural extension to the posterior fossa (12 chordomas and 1 meningioma) (Figures 5 and 6). GTR was achieved in 7 of 13 (54%) of these cases. In cases of tumors with extension to the posterior fossa but without lateral extension, GTR was observed in 7 of 11 patients (64%). Previous surgeries had been performed in 10 cases. In this group, only 3 patients (30%) had GTR, and the tumor was located medially in the upper clivus (Table 4). In patients operated on for the first time, GTR was achieved in 12 of 21 (57%). Among patients in whom an attempt at radical removal was made, only 5 had tumors infiltrating the lower clivus. In 2 patients (numbers 14 and 15) with chordomas invading the whole clivus, a partial resection was performed. In patient number 4
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with lateral extension of the inferior part, STR was performed. STR was also performed in the patient with meningioma and the patient with adenoid cystic carcinoma. The most frequent complication was CSF fistula occurring in 6 of 31 patients (19%) in whom total removal was attempted. This rate decreased to 1 of 16 patients (6%) after the use of a nasoseptal flap for skull base reconstruction. Preoperative sixth cranial nerve dysfunction could be improved in only 5 of 23 patients (22%). Only 1 patient (number 10) had a new permanent sixth cranial nerve impairment. Other complications were meningitis (3 of 31 patients), endocrinologic dysfunction (1 of 31 patients), pneumocephalus (2 of 31 patients), epistaxis (1 of 31 patients), and stroke (2 of 31 patients). The surgical mortality in our series was 9.5% (3 of 31 patients). Patient number 7 died of contralateral occlusion of the middle cerebral artery. Patient number 12 died of infectious complications secondary to a patent CSF fistula after a fourth surgery and radiotherapy. Patient number 30, with clivus meningioma, died of a pulmonary embolism on the fifth postoperative day. DISCUSSION The most frequent tumors of the clivus are chordomas and chondrosarcomas (1, 4, 14), which arise from embryonic remnants and may display infiltrative and aggressive behavior despite the benign histology (17, 22). There were 28 patients in our series with this diagnosis, and proposed treatment was complete surgical resection followed by radiotherapy and radiosurgery (4, 6, 19, 29). Surgery in 3 other patients with a different histologic diagnosis (meningioma, angiosarcoma, and adenoid cystic carcinoma) had the same goal. Metastases to the clivus are usually secondary to hematogenous dissemination and may have various etiologies (7, 20, 21). The surgical indication is always related to the tumor histology and is followed by radiotherapy. The transnasal transclival endoscopic approach for biopsy in patients with metastases has been demonstrated to be very useful, confirming diagnosis with no associated morbidity. For 1 patient with fibrous dysplasia with nasal obstruction, planned partial resection was the therapeutic management.
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Table 3. Prevalence of Gross Total Resection Based on Gender, Intradural Extension, and Histology of Tumor for 20 Patients with Tumors Restricted to the Midline Gross Total Resection Yes (n [ 15)
No (n [ 5)
Sex
P Value
Total (n [ 20)
0.62
Male
9 (60%)
2 (40%)
11 (55%)
Female
6 (40%)
3 (60%)
9 (45%)
41.7 20.8
Age (years)
47.0 24.5
Intradural extension
0.64
43.1 21.3
0.32
Yes
7 (46.7%)
4 (80%)
No
8 (53.3%)
1 (20%)
Histology
11 (55%) 9 (45%) 0.29
Chordoma
13 (86.7%)
Chondrosarcoma Meningioma Angiosarcoma
4 (80%)
2 (13.3%) —
17 (85%)
—
1 (5%)
1 (20%)
1 (6.7%)
1 (5%)
—
Surgical approach
1 (5%) 0.25
TS
15 (100%)
4 (80%)
RP
—
1 (20%)
Previous surgery
19 (95%) 1 (5%) 0.56
Yes
3 (20.0%)
2 (40.0%)
5 (25.0%)
No
12 (80.0%)
3 (60.0%)
15 (75.0%)
TS, transsphenoidal; RP, retropharyngeal.
Classically, clivus tumors were removed through lateral or posterolateral approaches with the advantages of minimizing CSF fistula and avoiding contamination through paranasal sinuses,
a nonsterile surgical corridor (23). The disadvantage, besides cerebral retraction, was the need to dislocate neural and vascular structures to reach the clivus (10). Considering the midline location and
Figure 5. Case 6. Preoperative magnetic resonance imaging scan of a clivus chordoma with a large intradural extension. The operative view after total tumor removal shows the neurovascular structures of the posterior fossa. B, basilar artery; P, pons; III, oculomotor nerve.
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epidural origin of most clivus lesions, a great development of the anterior surgical approaches could be seen in the past decades. The classic transfacial with external incision and sublabial with lateral osteotomy approaches (2, 5, 18), although cosmetically appropriate, do not enable adequate lateral vision. At the same time, the development of nasosinusal endoscopic surgery allowed expansion of indications beyond paranasal sinuses. Among the factors that permitted evolution of the technique, the multidisciplinary teamwork of ENT surgeons and neurosurgeons stands out. The sum of experiences also permitted the incorporation of intraoperative technologies, such as neuronavigation, MRI, micro-Doppler, and electrophysiologic monitoring, and surgical instruments adapted to the technique (6). Following pioneering work by Jho et al. (15), several series of clivus tumors operated on with an exclusive endoscopic technique reported results similar to the traditional series but with lower complication rates (6, 8-10, 13, 16, 24, 25, 28). From a surgical point of view, the clivus is divided into 3 segments (upper, middle, and lower) delimited by the Dorello canal and the jugular foramen as anatomic landmarks (5, 18). However, these landmarks are not well defined from a ventral view of the clivus, and other classifications are often used. Al-Mefty and Arnautovic (2) designated the upper clivus as the posterior wall of the sphenoid sinus, and Cavallo et al. (3) divided the posterior skull base into cranial (from the posterior interclinoid line to the floor of the sella turcica), middle (from the floor of the sella turcica to the line connecting the hypoglossal canals), and caudal (at the level of the craniovertebral junction) sections. We divide the clivus into 2 segments from the anterior surgical approach aspect: the upper clivus, which is the region above the sphenoid sinus floor, and the lower clivus situated below the sphenoid sinus floor. The separation of tumors based on topography has proven to be useful in the choice of approach and surgical prognosis. Upper clivus tumors (above the sphenoid sinus floor) were operated through the classic transnasal transsphenoidal approach. In lesions with expansion lateral to the carotid artery, the approach was extended to the pterygoid fossa. Lower clivus tumors (below sphenoid sinus floor) were operated
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Figure 6. Case 30. Posterior fossa lower clivus meningeoma. (A) Sagittal view demonstrates the craniocaudal extension of the tumor, lower than the sphenoid sinus. (B) Axial view demonstrates a midline tumor, anterior to the trajectory of the lower cranial nerves. (C) Intraoperative view after a retropharyngeal approach and subtotal resection of the tumor. B, basilar artery; VA, vertebral arteries; MO, medulla oblongata; P, pons; AICA, anterior-inferior cerebellar artery.
through the transnasal retropharyngeal approach. The results of these techniques are compared and discussed here in relation to GTR because there is no consensus on what constitutes STR. Some authors classify STR as a maximum of 20% residual tumor (80% resection) (6, 8, 24), and others define SRT as 95% (10, 28) or 90% (4) resection. Among the 31 patients in our series who were treated with the intention of radical resection of the tumor and with diverse extension of the lesion, we achieved GTR in 15 (48%) patients. Dehdashti et al. (6) described 58% of their patients with GTR and reported several series of chordoma resection through different approaches
(lateral, anterior transfacial, and endoscopic) and with variable tumor extension, obtaining GTR in 33%e66%. Sen et al. (23) reported 53% GTR in 17 patients with chordomas and chondrosarcomas operated with transcranial approaches, and Colli and Al-Mefty (4) reported 49.2% with transcranial and transfacial approaches. Among endoscopic series, Stippler et al. (28) obtained GTR in 45% (n ¼ 9) of patients with chordoma, and Fraser et al. (9) reported 60% complete removal in different types of tumors with indications for radical resection. Komotar et al. (16) compared microscopic and endoscopic series and observed a significantly higher percentage of GTR (61.0% vs. 48.1%, P ¼ 0.010), fewer cranial
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nerve deficits (1.3% vs. 24.2%, P < 0.001), fewer incidences of meningitis (0.9% vs. 5.9%, P ¼ 0.029), less mortality (4.7% vs. 21.6%, P < 0.001), and fewer local recurrences (16.9% vs. 40.0%, P ¼ 0.0001) in the endoscopic cohort. There was no significant difference in the incidence of postoperative CSF leak. If we restrict the group of clivus tumors to intradural or extradural lesions without lateral extension, we obtained GTR in 75% (15 of 20 patients) in our series. This result is similar to GTR in 79% reported by Al-Mefty and Arnautovic (2); these authors used microscopic anterior clivectomy supplemented with endoscopy for midline clivus tumors. The endoscopic technique assisted in visualization and removal of intradural tumors that were not visible under the microscope; this was helpful in 42% of their patients. Series of exclusively endoscopic approaches and series of microscopic and endoscopic approaches have similar outcomes. However, when the surgical team becomes adapted to the endoscopic vision, closer to the surgical field and with better illumination, the endoscopic technique is used throughout the surgery. Another advantage of the endoscopic technique is the use of both nostrils enabling bimanual work, with no restriction in the use of surgical instruments in a less invasive approach. Among the factors that might have had an influence on the radical resection of clivus tumors, the lateral expansion was more decisive. No patient with a lateral expansion tumor had a GTR, whereas GTR was achieved in 75% (P < 0.001) of patients with tumors with no lateral expansion. With the use of an endoscope, the lateral portions of the tumor are visualized; however, the tumor’s adhesions to important neurovascular structures are the limiting factor preventing a radical resection. Nevertheless, in contrast to some authors (6, 23), we believe that the transnasal endoscopic approach, purely transsphenoidal or complemented by a transpterygoid approach, is the first choice for clivus tumors. Eventually, combination with a lateral approach for residual tumor at the occipital condyle (8) or at the posterior petrous apex is needed. The radical removal of tumors that infiltrate the dura mater or expand to posterior fossa increases the chances of postoperative
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Table 4. Cases That Had Previous Surgeries (Chordoma and Chondrosarcoma Cases) Case Number 4
Previous Surgery
Surgical Approach
Resection
2 craniotomies
TS þ TP
ST
epistaxis (1 of 31 patients) are due to the relationship between tumor and neurovascular structures and not the approach itself.
7
4 craniotomies, 1 transnasal approach
TS þ TP
P
CONCLUSIONS
8
2 craniotomies, 1 transnasal approach
TS
P
12
2 craniotomies
TS
GT
As a less invasive and more direct surgical approach than other transfacial approaches, the endoscopic transnasal approach is an effective alternative for treatment of patients with clivus tumors of any origin. Although endoscopic transnasal surgery is mainly indicated for centrally located tumors, tailoring the approach to the anatomy makes it possible to expose and remove clivus tumors with any extension. Early results show this approach to equivalent to other techniques, and it should be considered an important option in cranial base surgery.
14
5 craniotomies, 1 midfacial degloving
TS þ TP
P
15
3 craniotomies
TS þ TP
P
19
1 craniotomy
TS
P
21
1 transnasal approach
TS
GT
25
1 craniotomy/1 transnasal approach
TS
GT
28
2 transnasal approaches
TS þ TP
ST
TS, transsphenoidal; TP, transpterygoid; ST, subtotal; P, partial; GT, gross total.
CSF fistula, a complication that is difficult to manage and related to serious infection and high morbidity. This increased risk of CSF fistula has always been the argument against the use of the anterior surgical corridor for tumor with intradural expansion. However, endoscopic surgery has evolved not only in regard to access to skull base tumors but also in regard to the possibilities of reconstruction of various dural defects. The use of vascularized flaps of the nasal mucosa was first described by Hadad et al. (11) using the septal mucosa. Flaps were subsequently expanded for other possibilities of reconstruction (13), decreasing the chances of CSF fistula. In our series of patients undergoing surgery with the goal of radical resection, the rate of postoperative fistula was high, around 19% (6 of 31 patients). However, if we select patients operated on after the development of mucosal flaps, the incidence decreases to 6% (1 of 16 patients). Fraser et al. (9) described CSF fistula in 4.8% of all transclival approaches, with a rate of 0% in cases in which either the gasket-seal or the septum flap was used. A review of the literature by these authors showed series of cases with CSF fistula rates ranging from 0%e33%. The possibility of reconstruction through the mucous membranes of the nasal cavity also transformed the transnasal endoscopic approach into an approach with less morbidity and improved patients’ functional recovery. Because all possibilities of reconstruction must be preserved, there is
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greater care in handling the nasal structures while performing access. The binostril approach described (26) and used in all transnasal endoscopic skull base surgeries, besides allowing the use of at least 3 instruments through both nostrils, preserves the contralateral septal mucosa avoiding complications such as nasal septal perforation and minimizing crusts in the postoperative period. The possibility of better results with the reconstruction of the skull base, greater experience with endoscopic surgery, and better surgical instruments has resulted in greater ease in removing tumors with intradural and posterior fossa expansion. The presence of dural invasion (intradural) was apparently not a limiting factor in medial tumors. GTR was achieved in 7 of 13 patients with dural invasion and 8 of 18 tumors without dural opening (P ¼ 0.32). As described by other authors (8, 28), previous surgery was also a determining factor in the surgical outcome of our patients. Only 3 of 10 (30%) patients with a prior surgery had a GTR, whereas the rate was 12 of 21 (57%) patients for the rest of the series. In our series, when comparing only midline tumors, this difference was not statistically significant probably because of the lower number of cases. Nasal cavity and intradural adhesions and especially the difficulty of obtaining an adequate mucosal flap for the reconstruction were the greatest obstacles in previously operated patients. Other complications mentioned in Results except for 1 patient with postoperative
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Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 18 September 2013; accepted 25 July 2014 Citation: World Neurosurg. (2014) 82, 6S:S106-S115. http://dx.doi.org/10.1016/j.wneu.2014.07.031 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
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