Journal of Clinical Neuroscience 21 (2014) 927–933
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Clinical Study
Pure endoscopic expanded endonasal approach for olfactory groove and tuberculum sellae meningiomas Osaama H. Khan a,⇑, Boris Krischek a, Damian Holliman a, George Klironomos a, Walter Kucharczyk b, Allan Vescan c, Fred Gentili a, Gelareh Zadeh a a b c
Division of Neurosurgery, University Health Network, Toronto Western Hospital, University of Toronto, 399 Bathurst Street, Ontario M5T 2S8, Canada Department of Diagnostic Imaging, University Health Network, Toronto Western Hospital, University of Toronto, Ontario, Canada Department of Otolaryngology-Head and Neck Surgery, Mount Sinai Hospital, University of Toronto, Ontario, Canada
a r t i c l e
i n f o
Article history: Received 14 October 2013 Accepted 18 October 2013
Keywords: Anterior skull base CSF leak Minimally invasive Naso-septal flap Transcribiform Transplanum Transsphenoidal
a b s t r a c t The expanded endoscopic endonasal (EEE) approach for the removal of olfactory groove (OGM) and tuberculum sellae (TSM) meningiomas is currently becoming an acceptable surgical approach in neurosurgical practice, although it is still controversial with respect to its outcomes, indications and limitations. Here we provide a review of the available literature reporting results with use of the EEE approach for these lesions together with our experience with the use of the endoscope as the sole means of visualization in a series of patients with no prior surgical biopsy or resection. Surgical cases between May 2006 and January 2013 were retrospectively reviewed. Twenty-three patients (OGM n = 6; TSM n = 17) were identified. In our series gross total resection (GTR) was achieved in 4/6 OGM (66.7%) and 11/17 (64.7%) TSM patients. Vision improved in the OGM group (2/2) and 8/11 improved in the TSM group with no change in visual status in the remaining three patients. Post-operative cerebrospinal fluid (CSF) leak occurred in 2/6 (33%) OGM and 2/17 (11.8%) TSM patients. The literature review revealed a total of 19 OGM and 174 TSM cases which were reviewed. GTR rate was 73% for OGM and 56.3% for TSM. Post-operative CSF leak was 30% for OGM and 14% for TSM. With careful patient selection and a clear understanding of its limitations, the EEE technique is both feasible and safe. However, longer follow-ups are necessary to better define the appropriate indications and ideal patient population that will benefit from the use of these newer techniques. Crown Copyright Ó 2013 Published by Elsevier Ltd. All rights reserved.
1. Introduction The management of anterior skull base meningiomas (ASM), including olfactory groove meningiomas (OGM) and tuberculum sellae meningiomas (TSM), has evolved over the past decade. Following the introduction and successful application of endoscopic techniques for paranasal and sellar pathologies, expanded endoscopic endonasal techniques (EEE) have made resection of intra-dural lesions, including ASM, feasible. OGM represent approximately 10% of all intracranial meningiomas and arise from the cribriform plate and/or the frontosphenoid suture. They often present with loss of olfactory nerve function, varying degrees of edema and mass effect involving the frontal lobes [1]. TSM represent 5–10% of intracranial meningiomas, and are believed to arise from the tuberculum sella, chiasmatic sulcus and diaphragma sellae [2,3]. Their location and proximity to critical neurovascular structures make them surgically challenging. ⇑ Corresponding author. Tel.: +1 416 603 5800x3712; fax: +1 416 603 5298. E-mail address: [email protected] (O.H. Khan). http://dx.doi.org/10.1016/j.jocn.2013.10.015 0967-5868/Crown Copyright Ó 2013 Published by Elsevier Ltd. All rights reserved.
They commonly present with insidious visual disturbance [4,5] with endocrine dysfunction tending to be a late consequence [6]. Visual field loss and reduced visual acuity typically occurs through displacement of the chiasm posteriorly and the optic nerves superolaterally, respectively [4,7]. However there is a spectrum based on size and growth patterns, wherein some OGM can extend to involve anatomical regions where TSM typically arise. There are a number of well-established microsurgical transcranial approaches that have been used and are considered the standard of care for the resection of ASM [5–11]. However there remains some concern regarding the transcranial approaches. The multiple methods suggest that no one approach is optimal and all of the open approaches involve some degree of frontal lobe brain retraction and long-term encephalomalacia [6,12,13]. Likewise the limited tunnel view optics of the microscope results in decreased illumination and access of deep seated structures. Recognized complications include injury of the optic apparatus or its blood supply with post-operative worsening of vision [13]. In an effort to address these limitations and minimize manipulation of the brain and neurovascular structures, as well
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as bring about early devascularization of the tumor and allow better visualization of the perichiasmatic anatomy, the techniques used for the endoscopic transnasal approach to pituitary and sella/parasellar lesions have been considered. They hold the promise of significant advantage over open approaches and as a result the EEE approach has been advocated as a surgical approach that can allow for access and removal of select anterior skull base tumors. While the feasibility of these innovative approaches has been documented, the indications and limitations of the EEE approach remain to be fully delineated. [14–16]. Indeed there remains significant controversy among skull base surgeons as to whether there are any indications for the use of these techniques for these specific lesions [17–19]. Although many studies have been published to demonstrate the safety and effectiveness of this approach, a study that compares open to endoscopic approaches with data from multiple institutions and long-term follow-up is needed. In this article, we report our own experience with the EEE approach for OGM and TSM using the endoscope as the sole means of visualization (‘‘pure’’ EEE). In addition, we review the available literature regarding the use of the pure EEE approach for these lesions in order to provide a summary of the current understanding in this field and determine if there are important factors that can be used as common indicators for selecting a patient subpopulation with OSM and TSM that might benefit from this approach.
2. Materials and methods 2.1. Patient characteristics Following institutional Research Ethics Board approval a prospectively maintained database of all surgical cases between May 2006 and January 2013 was retrospectively reviewed. Twenty-three patients with ASM were identified who had pure EEE approach surgery. A retrospective chart review was carried out to obtain details of patient demographics, and signs and symptoms on presentation and follow-up. This included pre- and post-operative ophthalmology assessments and endocrine abnormalities, MRI for tumor volume, surrounding edema, vascular encasement and the relationship of the tumor to the optic apparatus, and the operative record for the duration of operation, blood loss and any operative complications. Other parameters documented included hospital length of stay, pathology reports, and pre-operative and follow-up visit reports. Neurocognitive assessments were available for a small cohort of this population (Table 1). 2.2. Radiological assessment Our routine institutional practice is to undertake pre-operative MRI with and without administration of gadolinium contrast. In
Table 1a Demographics and clinical characteristics of olfactory groove meningioma patients Age/Sex
Symptoms
Tumor size (cm)
GTR
Post-op CSF leak
Re-operation for CSF leak
Length of stay (days)
Visual improvement
Follow-up (months)
53/F 65/F 53/F 33/F 43/F 75/F
H/a Incidental Incidental Visual changes H/a, seizures, personality changes Incidental
3.5 3.5 3.1 4.1 4.2 2.2 2.2 2.5 2.9 4.2 4 3.6 3.4 4.6 4.9 3.5 3.5 3.1
Yes No Yes Yes No Yes
No No No Yes Yes No
No No No Yes Yes No
5 10 5 18 7 7
Yes N/A N/A Yes N/A N/A
3 3 3 3 9 3
CSF = cerebrospinal fluid, GTR = gross total resection, F = female, H/a = headache, N/A = not applicable Post-op = post-operative.
Table 1b Demographics and clinical characteristics of tuberculum sellae meningioma patients Age/Sex
Symptoms
Pre-op endocrine abnormality
Tumor size (cm)
GTR
Postop CSF leak
Reoperation for CSF leak
Post-op endocrine abnormality
39/F
H/a
1.7 1.4 1.4
Yes
No
No
Elevated prolactin
76/M
H/a, memory changes, visual changes Hypopituitarism Visual changes Visual changes Visual changes Visual changes Visual changes Visual changes Visual changes Visual changes Visual changes H/a H/a H/a Visual changes, anosmia Incidental
Hypothyroid, elevated prolactin No
1.4 1.4 1.5
No
No
No
No
Hypopituitarism No No No No No No No No No No No No No
1.7 1.6 1.3 2.5 2.3 1.5 0.8 0.9 1 2.9 2.8 1.5 2.4 2.3 1.9 1.7 1.5 1.4 2.8 2.3 2 2.9 2.3 1.7 3.2 2.5 2.4 3.2 3.1 2.2 3.3 3.1 2.8 2.4 2.8 2 1.7 1.3 1 1 1.5 1.5
No Yes Yes Yes Yes Yes Yes No No No No Yes Yes Yes
No No No Yes No No No No No No No Yes No No
No No No Yes No No No No No No No Yes No No
Hypopituitarism Transient DI No No No No No No No No No Transient DI No No
No
2.7 2.7 2.1
Yes
No
No
No
60/F 40/F 73/F 45/F 69/M 44/F 76/F 88/F 85/F 68/M 52/F 77/M 63/F 68/F 62/F
Visual improvement
Followup (months)
5
N/A
16
5
No
10 10 5 19 4 4 9 14 4 5 6 19 7 5
No Yes Yes Yes Yes Yes No Yes No Yes No Yes N/A Yes
19 22 26 3 9 7 4 6 12 14 3 5 2 2
5
N/A
3
Length of stay (days)
1
CSF = cerebrospinal fluid, DI = diabetes insipidus, GTR = gross total resection, F = female, H/a = headache, M = male, N/A = not applicable Pre-op = pre-operative, Postop = post-operative.
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addition to an immediate CT scan within the first 24 hours after the operation, a post-operative MRI was performed routinely at 3 and 12 months, and yearly thereafter.
outcome data included tumor resection rates and post-operative cerebrospinal fluid (CSF) leak incidences.
2.3. Ophthalmological and endocrinological assessment
3. Results
All patients had formal ophthalmological examinations (visual acuity and perimetry) pre-operatively and at 3 months post-operatively, in addition to bedside visual acuity and field-testing before discharge. A complete endocrinological assessment was undertaken pre- and post-operatively (including adrenal, gonadal and thyroid axis) for patients with TSM and those with OGM who demonstrated concern for involvement of the pituitary gland and stalk. Specific monitoring for diabetes insipidus was carried out by measuring urine specific gravity, serum sodium, and fluid balance during the in-patient post-operative period.
3.1. Patient series
2.4. Surgical technique The EEE approach has been previously described; our approach is broadly similar with certain nuances emphasized [4,15,20–22]. All operations were carried out by an interdisciplinary team including a neurosurgeon and an ear, nose and throat (ENT) endoscopic skull base rhinologist. After induction of anesthesia, all patients were given broad spectrum antibiotics. The head was slightly extended and rotated to the right by 10° with the position fixed in a three-pin Mayfield holder. Frameless stereotactic navigation (Stealth; Medtronic, Jacksonville, FL, USA) was used in all surgeries. A pure endoscopic approach was undertaken using mainly a 0° 4 mm endoscope (Karl Storz & Co., Tuttlingen, Germany). In all cases a binasal approach using a right middle turbinectomy with a unilateral, vascularized nasoseptal flap was raised on the sphenopalatine artery, to be used as part of the skull base reconstruction after tumor removal [23]. A wide anterior sphenoidotomy under image guidance and with the aid of Doppler ultrasound was performed. For OGM, our surgical approach is similar to above with the addition of a transethmoidal transcribriform approach as previously described [15]. We did not violate the frontal sinus in our series of OGM patients and therefore we did not require a DRAF III or modified Lofthrop procedure. A multilayered reconstruction was used to close the dural defect with DuraGen (Integra NeuroCare, San Diego, CA, USA) and autogenous fascia lata placed as an inlay (intradurally) and then another layer of fascia lata as an outlay (extradurally). Next the harvested vascularized nasoseptal flap was laid over, fully covering the dural and fascia lata graft with the edges in contact with adjacent surrounding bone edges. Next, tissue glue (Tisseel; Baxter, Deerfield, IL, USA) was applied after the flap edges were covered with Surgicel (Ethicon, Cornelia, GA, USA) collagen sponge squares as the final layer. Usually an inflated balloon catheter was used for approximately 4 days as a scaffold and nasal packing was used to prevent graft migration. Post-operative antibiotics were continued until the nasal packing was removed. 2.5. Literature search A PubMed literature search was performed using the following search headings: ‘‘tuberculum sellae’’, ‘‘olfactory grove’’, ‘‘meningioma’’, ‘‘endoscopic’’, ‘‘endonasal’’, ‘‘extended transsphenoidal’’ and ‘‘expanded endonasal approach’’. Articles were retrieved and reviewed for patients undergoing pure EEE approaches in addition to all references therein being assessed for further relevant cases. Single case reports were excluded. Inclusion criteria were: (1) data presented in a disaggregated fashion; (2) patients clearly identifiable as having undergone a pure EEE approach for either OGM or TSM with no previous biopsy and/or surgery; and (3) minimum
Twenty-three patients with either OGM (n = 6) or TSM (n = 17) were treated by the senior authors (F.G. and G.Z.) using the pure EEE approach during the study period (Table 1). The median age at the time of surgery was 53 (range 43–71) and 62 (range 37–86) years for OGM and TSM patients, respectively. The presenting symptom varied with incidental (3/6), headache (2/6) and visual changes (1/6) in the OGM group while visual changes (visual disturbance, either acute deterioration, visual field deficit or both) was the major symptom (11/17) in the TSM group. The maximum diameter of the tumor ranged from 1.3–5.2 cm for OGM and 1–3.3 cm for TSM. Peritumoral edema was present in four OGM patients and one TSM patient. The optic apparatus was involved in 3/6 OGM and 15/17 TSM patients. The duration of surgery was a mean of 8.75 hours and 7.4 hours in the OGM and TSM groups, respectively. In regards to skull base reconstruction, only the first patient in 2006 had a nasoseptal flap that was not utilized. In the remaining patients both neurosurgeons used a nasoseptal flap, however, there was a notable difference in reconstruction, with F.G. preferring fascia lata and autologous fat whereas G.Z. preferred a synthetic collagen for the inlay closure. Average blood loss was 1000 cc in OGM patients and 200 cc in TSM patients. A gross total resection (Simpson grade I and II) was achieved in 4/6 OGM (66.7%) and 11/17 (64.7%) TSM patients. The residual tumor for the OGM patients was on the carotid in one patient and the falx in the other. Of the six partial resections in the TSM group, five had residual tumor adherent to or encasing the carotid and the other residual was adherent to the anterior clinoid. Fig. 1 demonstrates typical pre- and postoperative appearances. No patient experienced a deterioration of their visual status. Two OGM patients who had visual disturbances pre-operatively had improved vision post-operatively. In the TSM series, 11 patients had visual disturbance prior to surgery. Five of these patients showed no improvement of vision post-operatively and at follow-up. Of the six TSM patients with improvement, all had improved visual acuity and three had improved visual fields on formal assessment. For one TSM patient with advanced age and medical co-morbidities the pre-operative intention was to decompress the optic apparatus in an attempt to preserve vision. Their vision improved postoperatively with no endocrine abnormality or CSF leak. There was no peri-operative mortality, although one patient died 3 months post-operatively after the worsening of a pre-existing respiratory disease. There were no endocrine abnormalities in the OGM group. Endocrine disturbance was noted in three TSM patients post-operatively, with transient syndrome of inappropriate anti-diuretic hormone in two and transient diabetes insipidus in the other. One patient experienced toxic shock syndrome post-operatively, despite being on appropriate standard post-operative antibiotics, for which the cause was not identified. Post-operative CSF leaks occurred in four patients (OGM 2/6; TSM 2/17) one of whom also had a CSF infection. CSF leaks were explored with use of the endoscope, and repaired with fascia lata and/or DuraGen. Lumbar drainage was used for 3–5 days. One TSM patient underwent craniotomy after 2 years of follow-up for residual tumor on the anterior clinoid because of recurrence of the presenting symptom of visual deterioration. Their vision improved after this second operation with no residual tumor and no change in pathology. Pathology in all
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Fig. 1. Coronal (A, E, C, G) and sagittal (B, F, D, H) T1-weighted pre- and post-operative MRI with gadolinium contrast for patients who underwent a pure endoscopic endonasal approach with a nasoseptal flap for closure. Representative images from a 53-year-old woman with olfactory groove meningioma who presented with headaches (A, B), and achieved gross total resection with no cerebrospinal fluid leak as shown at 6 month follow-up (C, D). Representative images of a tuberculum sellae meningioma in a 40-year-old woman with visual changes (E, F). Follow-up imaging at 26 months showing no residual tumor with no cerebrospinal fluid leak (G, H).
patients was meningioma World Health Organization Grade I except one TSM patient with Grade II meningioma. No patients underwent either pre-operative or post-operative radiation or chemotherapy. The average follow-up period was 4 months (range 3– 9 months) in the OGM series and 9.4 months in the TSM series (range 3–26 months). 3.2. Literature review We identified a total of 14 articles with adequate disaggregated data describing a further 24 OGM [15,24,25] and 174 TSM [14–16,18,20,21,26–33] [34,35] patients who had undergone a pure EEE approach for surgical management. The contents of these articles, in combination with our patient series, are detailed in Table 2 and Table 3. With the addition of our series gross total resection was achieved in 73% and 56.3% of patients with a cumulative post-operative CSF leak rate of 30% and 14% in OGM and TSM patients, respectively. 4. Discussion ASM vary in their presentation due to their location. OGM are usually midline but as their size increases they may become asymmetric. The frontal lobes are always displaced superiorly and posteriorly. Their growth can also occur inferiorly through the cribriform plate into the ethmoid sinus, through the planum sphenoidale into the sphenoid sinus, or laterally through the orbit [26,36]. Their diagnosis is often made late due to their insidious growth. TSM often cause displacement of the optic chiasm posteriorly and optic nerves superolaterally, resulting in visual impairment, the most common symptom on presentation, and often optic atrophy [5,17,37]. Preservation of visual function is the most important indication for surgery [8,38]. The pure EEE approach is believed to have a number of advantages including: (1) elimination of brain retraction and a lack of optic apparatus manipulation with the wide removal of cranial base bone; (2) early control of vascular supply by devascularization of the tumor and preservation of the
supply to the optic nerves and chiasm from the hypophyseal vessels; (3) no facial/scalp incision for improved cosmesis; and (4) it is well tolerated by patients. [39] The published literature on the pure EEE approach for OGM and TSM is limited. Several reports are of endoscope-assisted microscopic approaches; that is, the endoscope is only introduced at the end of the microscopic procedure to assess resection [26,27,40]. Others detail a mixed case series of endoscope-assisted and pure endoscopic approaches [29]. Thus assessment of the limitations and potential adverse effects and benefits can be difficult. We report our experience of the pure EEE approach for OGM and TSM while combining our data with reports containing disaggregated data that can be clearly identified as a pure EEE approach. Unfortunately, the literature is restricted by a lack of consistency in reported parameters. Overall, including our series, there were 30 OGM and 174 TSM treated via a pure EEE approach, of which the majority were women as identified previously [8]. In general, the follow-up periods preclude complete comparison to other approaches [6,17,41]. However, the published series do not report any tumor recurrences in the patients who had a gross total resection. The GTR rates in our series of 66.7% (4/6) for OGM and 64.7% (11/ 17) for TSM compare well with the pure EEE resection rates of 77% for OGM and 56.3% for TSM of the combined published series with ours included. Similarly, these results compare well with the GTR rates seen in published series of transcranial excisions [8,37,41,42]. Optic canal (OC) invasion by TSM has been reported to occur in 24–75% of transcranial cases [2,17]. The exact site of invasion (medial or lateral in the canal) has led to intense debate as to which is the most rational approach for dealing with OC invasion [17,19,42]. Proponents of the EEE approach have suggested that as most OC invasion is medial, it is most effectively managed by an endonasal medio-lateral route [19]. Two OGM and four TSM patients in our series had OC invasion and this was readily dealt with via a pure EEE approach. Two of the four TSM patients had a residual tumor on the optic nerve. Only one of the two TSM patients with residual tumor on the optic nerve had improvement of vision, while the other patient’s vision was similar to their pre-operative state.
3–60, mean 29.4 9/ 30 = 30% 22/ 30 = 73% 5M 25F = 30 Total
CSF = cerebrospinal fluid, DI = diabetes insipidus, GTR = gross total resection, F = female, H/a = headache, ICA = internal carotid artery, M = male, N/A = not applicable. a Integra NeuroCare, San Diego, CA, USA. b Covidien, Dublin, Ireland. c Pfizer, New York, NY, USA.
3–27, mean 10 1/5 Intradural fat, tensor fascia, vascularized nasoseptal flap, surgical, DuraSealb, Gelfoamc, bone 2/ 5(40%) ICA Visual (3/5), H/a (2/ 5), anosmia (1/5) 1M 4F Padhye et al. 2012[25]
28–74, mean 54
1M 3F de Divitiis et al. 2008 [14]
35–65, mean 49
1.4–5.8
4/5(80%)
1/ 4(25%) None 4/ 4(100%)
None
8–12, mean 9.8 None
3/4 normal, 1/4 unchanged 2/3 unchanged No
5–32, mean 13.5
12–48 None Improved 8/8 (100%) N/A No
Changed over time: initially fibrin glue/ dural substitute/fat; then DuraGena ‘‘inlay’’ with nasoseptal flap, fat/ Gelfoamc Mixed (collagen sponge, dural subsitute, fibrinogen sealant), latterly pedicled flap 4/ 15(27%) Cavernous sinus
Incidental (1), visual (8), seizure (2), H/a (5), anosmia (1) H/a (1), psychiatric (2), hyposmia (1), visual (1) 35–79, mean 58 3M 12F
Volume 3.1– 109.3 cm3, mean 47.6 cm3 2–4.8
10/ 15(66.7%)
3–9 None Improved 2/2(100%) H/a (2), visual (1), incidental (3) 33–71, median 53 6F
Khan et al. 2013 (current series) Gardner et al. 2008 [15]
3.1–4.9
4/ 6(66.7%)
Carotid, falx
2/ 6(33%)
Nasoseptal flap
No (only if leak)
5–18, mean (8.7)
Post-op endocrine abnormality Presenting symptoms Tumor size(cm) Age range (years) Patients Authors and year
Table 2 Reports of olfactory groove meningiomas in the literature
GTR
Site of residual disease
CSF leak rate
Reconstruction technique
Lumbar drainage
Length of stay (days)
Visual outcome
Follow-up range (months)
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All the published reports (Table 2, Table 3) contained patients who were objectively assessed for visual status pre- and postoperatively. The cause of visual disturbance is believed to be compression leading to ischemia and demyelination of the optic apparatus [17]. Visual improvement appears to be the norm with the remainder of patients remaining stable. Vision rarely appears to deteriorate after the EEE approach but has been reported in transcranial TSM series at rates of 11–29% [15]. It has been suggested that visual improvement is more common if symptoms have been present for less than 6 months [8]. Only one of our patients had symptoms for less than 6 months. Other series of the pure EEE approach tend not to report the duration of presenting symptoms. After the pure EEE approach transient or permanent endocrine dysfunction was absent in all OGM patients, but was transient in two TSM patients. Observed rates of post-operative endocrine dysfunction ranged from 0–33% for TSM when reported (Table 2). Most of these are disorders of sodium homeostasis, and this reflects the close proximity of the pituitary stalk during fine dissection of the tumor. Reconstruction of the anterior cranial base and closure of the dural defect has been accomplished via a number of methods. Most series included the use of a fascial graft or a dural synthetic substitute augmented with combinations of fat, mucoperichondrium, collagen sponge and fibrinogen sealant [43]. The reconstruction is then be held in place by nasal packing or a Foley catheter balloon. Lately several groups, including our own, have adopted the use of the nasoseptal vascularized flap [23] as a means of reducing post-operative CSF leaks, with significant success. A further advantage of this type of reconstruction for the skull base is its apparent tolerance of radiotherapy, which is sometimes required for lesions in the anterior skull base [44]. Other means of closure of skull base defects include the ‘‘gasket-seal’’ technique which has also shown success in reducing CSF leaks [45]. In our report, the combined CSF leak rate was 30% for OGM and 14% for TSM (Table 2, Table 3). A meta-analysis of endoscopic surgery for OGM and TSM in 2010 reported a CSF leak rate of 31.6% and 24.8%, respectively. Open cranial surgery had a CSF leak rate of 6.3% for OGM and 4.3% for TSM [46]. A thorough discussion of open versus endoscopic resection has been adequately addressed in the paper by Komotar et al [46]. One explanation for our four patients with CSF leak is that one patient was the only one in the series who did not have a nasoseptal flap, only fascia lata and fat, while the other three did not have autologous fascia lata as an inlay. Interestingly, in a mixed series of ASM the highest CSF leak incidence was seen with the smallest tumors, the tuberculum lesions [15]. We did not find any relationship between size and occurrence of CSF leaks in both OGM and TSM patients. All the published series included in this review are retrospective studies from high volume centers with a subspecialty multidisciplinary approach to the EEE method, creating an associated inherent recognized bias due to referral basis and the nature of the practice being prone to reporting bias. It is likely that patient selection combined with the surgeon’s familiarity of the approach and availability of an ENT surgeon will mean that the pure EEE approach for ASM will increase at these high volume centers, which further highlights the need for reporting of outcomes. Additional important issues to consider before using this approach for ASM are tumor size, OC invasion and relationship to adjacent neurovascular structures. Based on our experience, key features of relative contra-indication include extension lateral to the optic canal, presence of extreme mass effect on the frontal lobes due to brain edema or tumor mass, presence of hydrocephalus, previous surgery (open or EEE approach), and concerning features on MRI for malignant disease. Relative factors that would require careful consideration pre-operatively include superior extension of the tumor, and calcification within or surrounding the tumor.
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Table 3 Reports of tuberculum sellae meningiomas in the literature Reconstruction technique
Lumbar drainage
11/17(54%) ICA, sella, optic nerve
2/17 (11.8%)
Mixed (fascia lata and nasoseptal flap)
N/A
15/19(79%) N/A
1/19(5%)
Fascia lata, mucosal flap
No (only if 4–19, mean post-op 7.7 leak) N/A N/A
1.3–3.1
Visual (7), H/a (1)
3/8(38%)
N/A
0/8(0%)
Fascia lata
N/A
N/A
1.7–3.5
Visual (3), facial numbness (1)
1/8(13%)
1/8(13%)
Fat and fascia lata
Yes
N/A
N/A
Visual (2)
2/2(100%)
ICA, cavernous sinus None
0/2(0%)
Mixed (fascia lata and nasoseptal flap)
Yes
1.6–4.5
Visual:VA (5), VF (7)
6/16(38%)
Mixed (fascia lata, methacrylate, mucoperichondrium, fibrin glue)
2.5–4.0
Visual (11), H/a (1)
11/21(52%) Optic canal
1/22 (4.5%)
1.3–3.2
Visual 6 (VA 6, VF 6), H/a (2)
6/7(86%)
1.5–3
Visual (10)
6/1346%
Volume 2.1– 16.2 cm3, mean 7.5 cm3 2–3.5
Patients
Age range (years)
Tumor size range (cm)
Presenting symptoms
GTR
Khan et al. 2013 (current series)
4M 13F
0.8–3.3
Visual (11), H/a (5), incidental (1)
Ogawa et al. 2012[32]
5M 14F
0.9–2.9
Van gompel et al. 2011[18]
8M
Bowers et al. 2011[29]
4M 4F
Liu et al. 2011[31]
1M 1F
Ceylan et al. 2011[30]
9M 7F
Wang et al. 2010[4]
12M 9F
de Divitiis et al. 2008[14]
3M 4F
37–86, median 60 43–79, mean 58.9 31–77, median 69 39–77, median 66 Aged 62 and 38 32–78, median 51 27–67, median 52 47–80, mean 58.7
Fatemiet al.2009[27] 3M 10F
Gardner et al. 2008[15]
13M 12F
Laufer et al. 2007[16] 3M
Kitanoet al.2007[26] 2M 14F
Padhyeet al.2012[25] 2F
Chowdhury et al. 2012[33]
2M 4F
Attia et al. 2012[35]
6F
Bohman et al. 2012[34]
2M 3F
Total
71M 103F = 174
31–77, mean 51.3 39–72, median 53
51–73, median 66 42–76, mean 53.8 65–66, mean 65.5 29–52, mean 39.5 31–74, mean 56.5 25–77, mean 53.2
Site of residual disease
Length of stay, range (days)
Visual outcome
Postoperative Endocrine abnormality
6 improved, 5 unchanged
2/13 transient SIADH 3–26, (15%), 1/13 transient DI median 10 (7.7%) None 3–59
14/19 improved, 3 unchanged, 2 deteriorated 5 improved, 3 unchanged
Follow-up range (months)
None
3–65, median 9.5
N/A
N/A
N/A
N/A
Improved (100%)
None
1.5 & 3
Yes
6–8
6 improved, 3 unchanged
1/9 permanent DI
3–33, median 20
Fat and dural substitute
No
2–5
11 improved, 1 unchanged
1/12 transient DI (8%)
6–60, median 28
2/7(29%)
Mixed (collagen sponge, dural subsitute, fibrinogen sealant), latterly pedicled flap
No (only if 5–21, post-op median 9 leak)
1/7 transient DI (14%)
0.75–51, median 24
4/ 13(30%)
Abdominal fat, collagen sponge, titanium mesh, bioglue sealant
Yes (48 hours)
1–13, median 4
1/13 hypopituitarism(7.7%)
6–65, median 27
Visual (10), H/a (1), incidental (1), prior residual tumor (1)
Cavernous sinus, carotid 11/25(44%) Cavernous sinus
5 improved,2 unchanged (3 transient worsening) 9/10 improved,1/10 unchanged
8/ 25(32%)
Mixed
No
N/A
Improved (100%)
1 hypopituitarism
23–58, median 40
Visual 3/3
2/3(66%)
1/3(33%)
Fascia lata and Tisseela or DuraSealb then Floseala
Yes (1)
N/A
3/3improved (100%) 1/3 permanent DI (33%) 6–12, median 9
Cisternal 0/16(0%) and vascular
Optic canal
A-com
Visual (16) Volume 1–20.3 mm3
12/16(75%) Not 2/ Sutured abdominal fascia, Gore-Texc, documented 16(12.5%) hydroxyapatite cement
Yes (9/16) N/A
1.4–2
Visual (2)
2/2(100%)
N/A
0/2(0%)
No
Mean 9
2–4
Visual (6), H/a (2)
5/6(83%)
A-com/A2 segment
1/6(17%)
Intradural fat, tensor fascia, vascularized septal flap, surgical, DuraSealb, Gelfoamd, bone Fascia lata inlay graft, thigh fat
Yes
N/A
1–4
Visual (5), H/a (1)
5/6(83%)
ICA, optic canal
0/6(0%)
Fat, fascia lata inlay – buttress with Medporee, nasoseptal flap, DuraSealb
Yes
N/A
1.4–3
Visual (5), H/a (2)
4/5(80%)
Not 1/5(20%) documented
Nasoseptal flap, fascia lata, fat, DuraGenf
Yes 3/5
N/A
98/ 174 = 56.3%
10/16 improved None (81%), 6/16worse (38%) 2/2 improved (100%) Hyopnatremia (50%)
3–6
3/6 improved, 2/6 unchanged, 1/6 deteriorated 3/6 improved, 2/6 unchanged, 1/6 deteriorated 4/5 improved, 1/5 stable
2/6 hyponatremia (33%)
2–12, mean 7
-
3–39.5, mean 20.75
2/5 hyponatremia (40%)
2–17, mean 7.8
Mean 3
24/ 174 = 14%
A-com = anterior communicating artery, CSF = cerebrospinal fluid, DI = diabetes insipidus, GTR = gross total resection, F = female, H/a = headache, ICA = internal carotid artery, M = male, N/A = not available, SIADH = syndrome of inappropriate anti-diuretic hormone, VA = visual acuity, VF = visual field. a Baxter, Deerfield, IL, USA. b Covidien, Dublin, Ireland. c W. L. Gore & Associates, Newark, DE, USA. d Pfizer, New York, NY, USA. e Stryker, Kalamazoo, MI, USA. f Integra NeuroCare, San Diego, CA, USA.
O.H. Khan et al. / Journal of Clinical Neuroscience 21 (2014) 927–933
CSF leak rate
Authors and year
O.H. Khan et al. / Journal of Clinical Neuroscience 21 (2014) 927–933
5. Conclusion Based on our experience together with results of reported case series the pure EEE approach for OGM and TSM can be safely utilized by surgeons appropriately experienced in endoscopic endonasal procedures. We can identify important relative contraindications such as extension lateral to the optic canal, presence of significant mass effect on the frontal lobes and potential intratumoral calcification, which should caution against use of the EEE approach. Overall, as we continue and increase our experience with this surgical approach it is important to maintain and report longer-term follow-up to be able to accurately assess the recurrence rates of ASM excised via an EEE approach. Conflicts of interest/disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. Acknowledgements D.H. was the recipient of a European Association of NeuroOncology Educational Fellowship grant. References [1] Coppens J, Couldwell W. Olfactory groove meningiomas. In: Pamir MN, Black PM, Fahlbusch R, editors. Meningiomas: a comprehensive text. Philadelphia: Saunders; 2009. [2] Yasargil M. Microneurosurgery, vol. 4b. Stuttgart, Germany: Thieme; 1996. [3] de Divitiis E, Esposito F, Cappabianca P, et al. Tuberculum sellae meningiomas: high route or low route? A series of 51 consecutive cases. Neurosurgery 2008;62:556–63 [discussion 556–63]. [4] Wang Q, Lu XJ, Ji WY, et al. Visual outcome after extended endoscopic endonasal transsphenoidal surgery for tuberculum sellae meningiomas. World Neurosurg 2010;73:694–700. [5] Goel A, Muzumdar D, Desai KI. Tuberculum sellae meningioma: a report on management on the basis of a surgical experience with 70 patients. Neurosurgery 2002;51:1358–63 [discussion 1363–4]. [6] Fahlbusch R, Schott W. Pterional surgery of meningiomas of the tuberculum sellae and planum sphenoidale: surgical results with special consideration of ophthalmological and endocrinological outcomes. J Neurosurg 2002;96: 235–43. [7] Chi JH, McDermott MW. Tuberculum sellae meningiomas. Neurosurg Focus 2003;14:e6. [8] Ganna A, Dehdashti AR, Karabatsou K, et al. Fronto-basal interhemispheric approach for tuberculum sellae meningiomas; long-term visual outcome. Br J Neurosurg 2009;23:422–30. [9] Avci E, Akture E, Seckin H, et al. Level I to III craniofacial approaches based on Barrow classification for treatment of skull base meningiomas: surgical technique, microsurgical anatomy, and case illustrations. Neurosurg Focus 2011;30:E5. [10] DeMonte F. Surgical treatment of anterior basal meningiomas. J Neurooncol 1996;29:239–48. [11] Hentschel SJ, DeMonte F. Olfactory groove meningiomas. Neurosurg Focus 2003;14:e4. [12] Andrews BT, Wilson CB. Suprasellar meningiomas: the effect of tumor location on postoperative visual outcome. J Neurosurg 1988;69:523–8. [13] Kim TW, Jung S, Jung TY, et al. Prognostic factors of postoperative visual outcomes in tuberculum sellae meningioma. Br J Neurosurg 2008;22:231–4. [14] de Divitiis E, Esposito F, Cappabianca P, et al. Endoscopic transnasal resection of anterior cranial fossa meningiomas. Neurosurg Focus 2008;25:E8. [15] Gardner PA, Kassam AB, Thomas A, et al. Endoscopic endonasal resection of anterior cranial base meningiomas. Neurosurgery 2008;63:36–52 [discussion 52–4]. [16] Laufer I, Anand VK, Schwartz TH. Endoscopic, endonasal extended transsphenoidal, transplanum transtuberculum approach for resection of suprasellar lesions. J Neurosurg 2007;106:400–6. [17] Mahmoud M, Nader R, Al-Mefty O. Optic canal involvement in tuberculum sellae meningiomas: influence on approach, recurrence, and visual recovery. Neurosurgery 2010;67:ons108–18 [discussion ons118–9]. [18] Van Gompel JJ, Frank G, Pasqini E, et al. Expanded endonasal endoscopic resection of anterior fossa meningiomas: report of 13 cases and meta-analysis of the literature. Neurosurg Focus 2011;30:E15.
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[19] Fernandez-Miranda JC, Gardner PA, Snyderman CH. Endoscopic endonasal approach for tuberculum sellae meningiomas. Neurosurgery 2011;69:E260–1. [20] Castelnuovo P, Pistochini A, Locatelli D. Different surgical approaches to the sellar region: focusing on the ‘‘two nostrils four hands technique’’. Rhinology 2006;44:2–7. [21] de Divitiis E et al. Extended endoscopic transsphenoidal approach for tuberculum sellae meningiomas. Neurosurgery 2008;62:1192–201. [22] Dehdashti AR et al. Expanded endoscopic endonasal approach for anterior cranial base and suprasellar lesions: indications and limitations. Neurosurgery 2009;64:677–87 [discussion 687–9]. [23] Hadad G et al. A novel reconstructive technique after endoscopic expanded endonasal approaches: vascular pedicle nasoseptal flap. Laryngoscope 2006; 116:1882–6. [24] de Divitiis E, Cavallo LM, Cappabianca P, et al. Extended endoscopic endonasal transsphenoidal approach for the removal of suprasellar tumors: part 2. Neurosurgery 2007;60:46–58 [discussion 58–9]. [25] Padhye V et al. Endoscopic endonasal resection of anterior skull base meningiomas. Otolaryngol Head Neck Surgery 2012;147:575–82. [26] Kitano M, Taneda M, Nakao Y. Postoperative improvement in visual function in patients with tuberculum sellae meningiomas: results of the extended transsphenoidal and transcranial approaches. J Neurosurg 2007; 107:337–46. [27] Fatemi N, Dusick JR, de Paiva Neto MA, et al. Endonasal versus supraorbital keyhole removal of craniopharyngiomas and tuberculum sellae meningiomas. Neurosurgery 2009;64(5 Suppl. 2):269–84 [discussion 284–6]. [28] Wang Q, Lan Q, Lu XJ. Extended endoscopic endonasal transsphenoidal approach to the suprasellar region: anatomic study and clinical considerations. J Clin Neurosci 2010;17:342–6. [29] Bowers CA, Altay T, Couldwell WT. Surgical decision-making strategies in tuberculum sellae meningioma resection. Neurosurg Focus 2011;30:E1. [30] Ceylan S, Koc K, Anik I. Extended endoscopic transphenoidal approach for tuberculum sellae meningiomas. Acta Neurochir 2011;153:1–9. [31] Liu JK, Chrisyiano LD, Patel SK, et al. Surgical nuances for removal of tuberculum sellae meningiomas with optic canal involvement using the endoscopic endonasal extended transsphenoidal transplanum transtuberculum approach. Neurosurg Focus 2011;30:E2. [32] Ogawa Y, Tominaga T. Extended transsphenoidal approach for tuberculum sellae meningioma–what are the optimum and critical indications? Acta Neurochir 2012;154:621–6. [33] Chowdhury FH, Haque MR, Goel AH, et al. Endoscopic endonasal extended transsphenoidal removal of tuberculum sellae meningioma (TSM): an experience of six cases. Br J Neurosurg 2012;26:692–9. [34] Bohman LE, Stein SC, Newman JG, et al. Endoscopic versus open resection of tuberculum sellae meningiomas: a decision analysis. ORL J Otorhinolaryngol Relat Spec 2012;74:255–63. [35] Attia M, Kandasamy J, Jakimovski D, et al. The importance and timing of optic canal exploration and decompression during endoscopic endonasal resection of tuberculum sella and planum sphenoidale meningiomas. Neurosurgery 2012;71(1 Suppl. Operative):58–67. [36] Bonfils P, Brasnu D, Roux FX, et al. Olfactory meningioma with ethmoidoorbital extension. Diagnostic and therapeutic problems. Apropos of a case. Ann Otolaryngol Chir Cervicofac 1988;105:179–81. [37] Arai H, Sato K, Okuda M, et al. Transcranial transsphenoidal approach for tuberculum sellae meningiomas. Acta Neurochir 2000;142:751–6 [discussion 756–7]. [38] Park CK, Jung HW, Yang SY, et al. Surgically treated tuberculum sellae and diaphragm sellae meningiomas: the importance of short-term visual outcome. Neurosurgery 2006;59:238–43 [discussion 238–43]. [39] Frank G, Pasquini E. Tuberculum sellae meningioma: the extended transsphenoidal approach – for the virtuoso only? World Neurosurg 2010; 73: 625–6. [40] Cook SW, Smith Z, Kelly DF. Endonasal transsphenoidal removal of tuberculum sellae meningiomas: technical note. Neurosurgery 2004;55: 239–44 [discussion 244–6]. [41] Nakamura M, Roser F, Struck F, et al. Tuberculum sellae meningiomas: clinical outcome considering different surgical approaches. Neurosurgery 2006;59: 1019–28 [discussion 1028–9]. [42] Taha AN, Erkmen K, Dunn IF, et al. Meningiomas involving the optic canal: pattern of involvement and implications for surgical technique. Neurosurg Focus 2011;30:E12. [43] Kassam A, Carrau RL, Snyderman CH, et al. Evolution of reconstructive techniques following endoscopic expanded endonasal approaches. Neurosurg Focus 2005;19:E8. [44] Aghi MK, Carter BS, Cosgrove GR, et al. Long-term recurrence rates of atypical meningiomas after gross total resection with or without postoperative adjuvant radiation. Neurosurgery 2009;64:56–60 [discussion 60]. [45] Garcia-Navarro V, Anand VK, Schwartz TH. 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Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical Study
Pure endoscopic expanded endonasal approach for olfactory groove and tuberculum sellae meningiomas Osaama H. Khan a,⇑, Boris Krischek a, Damian Holliman a, George Klironomos a, Walter Kucharczyk b, Allan Vescan c, Fred Gentili a, Gelareh Zadeh a a b c
Division of Neurosurgery, University Health Network, Toronto Western Hospital, University of Toronto, 399 Bathurst Street, Ontario M5T 2S8, Canada Department of Diagnostic Imaging, University Health Network, Toronto Western Hospital, University of Toronto, Ontario, Canada Department of Otolaryngology-Head and Neck Surgery, Mount Sinai Hospital, University of Toronto, Ontario, Canada
a r t i c l e
i n f o
Article history: Received 14 October 2013 Accepted 18 October 2013
Keywords: Anterior skull base CSF leak Minimally invasive Naso-septal flap Transcribiform Transplanum Transsphenoidal
a b s t r a c t The expanded endoscopic endonasal (EEE) approach for the removal of olfactory groove (OGM) and tuberculum sellae (TSM) meningiomas is currently becoming an acceptable surgical approach in neurosurgical practice, although it is still controversial with respect to its outcomes, indications and limitations. Here we provide a review of the available literature reporting results with use of the EEE approach for these lesions together with our experience with the use of the endoscope as the sole means of visualization in a series of patients with no prior surgical biopsy or resection. Surgical cases between May 2006 and January 2013 were retrospectively reviewed. Twenty-three patients (OGM n = 6; TSM n = 17) were identified. In our series gross total resection (GTR) was achieved in 4/6 OGM (66.7%) and 11/17 (64.7%) TSM patients. Vision improved in the OGM group (2/2) and 8/11 improved in the TSM group with no change in visual status in the remaining three patients. Post-operative cerebrospinal fluid (CSF) leak occurred in 2/6 (33%) OGM and 2/17 (11.8%) TSM patients. The literature review revealed a total of 19 OGM and 174 TSM cases which were reviewed. GTR rate was 73% for OGM and 56.3% for TSM. Post-operative CSF leak was 30% for OGM and 14% for TSM. With careful patient selection and a clear understanding of its limitations, the EEE technique is both feasible and safe. However, longer follow-ups are necessary to better define the appropriate indications and ideal patient population that will benefit from the use of these newer techniques. Crown Copyright Ó 2013 Published by Elsevier Ltd. All rights reserved.
1. Introduction The management of anterior skull base meningiomas (ASM), including olfactory groove meningiomas (OGM) and tuberculum sellae meningiomas (TSM), has evolved over the past decade. Following the introduction and successful application of endoscopic techniques for paranasal and sellar pathologies, expanded endoscopic endonasal techniques (EEE) have made resection of intra-dural lesions, including ASM, feasible. OGM represent approximately 10% of all intracranial meningiomas and arise from the cribriform plate and/or the frontosphenoid suture. They often present with loss of olfactory nerve function, varying degrees of edema and mass effect involving the frontal lobes [1]. TSM represent 5–10% of intracranial meningiomas, and are believed to arise from the tuberculum sella, chiasmatic sulcus and diaphragma sellae [2,3]. Their location and proximity to critical neurovascular structures make them surgically challenging. ⇑ Corresponding author. Tel.: +1 416 603 5800x3712; fax: +1 416 603 5298. E-mail address: [email protected] (O.H. Khan). http://dx.doi.org/10.1016/j.jocn.2013.10.015 0967-5868/Crown Copyright Ó 2013 Published by Elsevier Ltd. All rights reserved.
They commonly present with insidious visual disturbance [4,5] with endocrine dysfunction tending to be a late consequence [6]. Visual field loss and reduced visual acuity typically occurs through displacement of the chiasm posteriorly and the optic nerves superolaterally, respectively [4,7]. However there is a spectrum based on size and growth patterns, wherein some OGM can extend to involve anatomical regions where TSM typically arise. There are a number of well-established microsurgical transcranial approaches that have been used and are considered the standard of care for the resection of ASM [5–11]. However there remains some concern regarding the transcranial approaches. The multiple methods suggest that no one approach is optimal and all of the open approaches involve some degree of frontal lobe brain retraction and long-term encephalomalacia [6,12,13]. Likewise the limited tunnel view optics of the microscope results in decreased illumination and access of deep seated structures. Recognized complications include injury of the optic apparatus or its blood supply with post-operative worsening of vision [13]. In an effort to address these limitations and minimize manipulation of the brain and neurovascular structures, as well
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as bring about early devascularization of the tumor and allow better visualization of the perichiasmatic anatomy, the techniques used for the endoscopic transnasal approach to pituitary and sella/parasellar lesions have been considered. They hold the promise of significant advantage over open approaches and as a result the EEE approach has been advocated as a surgical approach that can allow for access and removal of select anterior skull base tumors. While the feasibility of these innovative approaches has been documented, the indications and limitations of the EEE approach remain to be fully delineated. [14–16]. Indeed there remains significant controversy among skull base surgeons as to whether there are any indications for the use of these techniques for these specific lesions [17–19]. Although many studies have been published to demonstrate the safety and effectiveness of this approach, a study that compares open to endoscopic approaches with data from multiple institutions and long-term follow-up is needed. In this article, we report our own experience with the EEE approach for OGM and TSM using the endoscope as the sole means of visualization (‘‘pure’’ EEE). In addition, we review the available literature regarding the use of the pure EEE approach for these lesions in order to provide a summary of the current understanding in this field and determine if there are important factors that can be used as common indicators for selecting a patient subpopulation with OSM and TSM that might benefit from this approach.
2. Materials and methods 2.1. Patient characteristics Following institutional Research Ethics Board approval a prospectively maintained database of all surgical cases between May 2006 and January 2013 was retrospectively reviewed. Twenty-three patients with ASM were identified who had pure EEE approach surgery. A retrospective chart review was carried out to obtain details of patient demographics, and signs and symptoms on presentation and follow-up. This included pre- and post-operative ophthalmology assessments and endocrine abnormalities, MRI for tumor volume, surrounding edema, vascular encasement and the relationship of the tumor to the optic apparatus, and the operative record for the duration of operation, blood loss and any operative complications. Other parameters documented included hospital length of stay, pathology reports, and pre-operative and follow-up visit reports. Neurocognitive assessments were available for a small cohort of this population (Table 1). 2.2. Radiological assessment Our routine institutional practice is to undertake pre-operative MRI with and without administration of gadolinium contrast. In
Table 1a Demographics and clinical characteristics of olfactory groove meningioma patients Age/Sex
Symptoms
Tumor size (cm)
GTR
Post-op CSF leak
Re-operation for CSF leak
Length of stay (days)
Visual improvement
Follow-up (months)
53/F 65/F 53/F 33/F 43/F 75/F
H/a Incidental Incidental Visual changes H/a, seizures, personality changes Incidental
3.5 3.5 3.1 4.1 4.2 2.2 2.2 2.5 2.9 4.2 4 3.6 3.4 4.6 4.9 3.5 3.5 3.1
Yes No Yes Yes No Yes
No No No Yes Yes No
No No No Yes Yes No
5 10 5 18 7 7
Yes N/A N/A Yes N/A N/A
3 3 3 3 9 3
CSF = cerebrospinal fluid, GTR = gross total resection, F = female, H/a = headache, N/A = not applicable Post-op = post-operative.
Table 1b Demographics and clinical characteristics of tuberculum sellae meningioma patients Age/Sex
Symptoms
Pre-op endocrine abnormality
Tumor size (cm)
GTR
Postop CSF leak
Reoperation for CSF leak
Post-op endocrine abnormality
39/F
H/a
1.7 1.4 1.4
Yes
No
No
Elevated prolactin
76/M
H/a, memory changes, visual changes Hypopituitarism Visual changes Visual changes Visual changes Visual changes Visual changes Visual changes Visual changes Visual changes Visual changes H/a H/a H/a Visual changes, anosmia Incidental
Hypothyroid, elevated prolactin No
1.4 1.4 1.5
No
No
No
No
Hypopituitarism No No No No No No No No No No No No No
1.7 1.6 1.3 2.5 2.3 1.5 0.8 0.9 1 2.9 2.8 1.5 2.4 2.3 1.9 1.7 1.5 1.4 2.8 2.3 2 2.9 2.3 1.7 3.2 2.5 2.4 3.2 3.1 2.2 3.3 3.1 2.8 2.4 2.8 2 1.7 1.3 1 1 1.5 1.5
No Yes Yes Yes Yes Yes Yes No No No No Yes Yes Yes
No No No Yes No No No No No No No Yes No No
No No No Yes No No No No No No No Yes No No
Hypopituitarism Transient DI No No No No No No No No No Transient DI No No
No
2.7 2.7 2.1
Yes
No
No
No
60/F 40/F 73/F 45/F 69/M 44/F 76/F 88/F 85/F 68/M 52/F 77/M 63/F 68/F 62/F
Visual improvement
Followup (months)
5
N/A
16
5
No
10 10 5 19 4 4 9 14 4 5 6 19 7 5
No Yes Yes Yes Yes Yes No Yes No Yes No Yes N/A Yes
19 22 26 3 9 7 4 6 12 14 3 5 2 2
5
N/A
3
Length of stay (days)
1
CSF = cerebrospinal fluid, DI = diabetes insipidus, GTR = gross total resection, F = female, H/a = headache, M = male, N/A = not applicable Pre-op = pre-operative, Postop = post-operative.
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addition to an immediate CT scan within the first 24 hours after the operation, a post-operative MRI was performed routinely at 3 and 12 months, and yearly thereafter.
outcome data included tumor resection rates and post-operative cerebrospinal fluid (CSF) leak incidences.
2.3. Ophthalmological and endocrinological assessment
3. Results
All patients had formal ophthalmological examinations (visual acuity and perimetry) pre-operatively and at 3 months post-operatively, in addition to bedside visual acuity and field-testing before discharge. A complete endocrinological assessment was undertaken pre- and post-operatively (including adrenal, gonadal and thyroid axis) for patients with TSM and those with OGM who demonstrated concern for involvement of the pituitary gland and stalk. Specific monitoring for diabetes insipidus was carried out by measuring urine specific gravity, serum sodium, and fluid balance during the in-patient post-operative period.
3.1. Patient series
2.4. Surgical technique The EEE approach has been previously described; our approach is broadly similar with certain nuances emphasized [4,15,20–22]. All operations were carried out by an interdisciplinary team including a neurosurgeon and an ear, nose and throat (ENT) endoscopic skull base rhinologist. After induction of anesthesia, all patients were given broad spectrum antibiotics. The head was slightly extended and rotated to the right by 10° with the position fixed in a three-pin Mayfield holder. Frameless stereotactic navigation (Stealth; Medtronic, Jacksonville, FL, USA) was used in all surgeries. A pure endoscopic approach was undertaken using mainly a 0° 4 mm endoscope (Karl Storz & Co., Tuttlingen, Germany). In all cases a binasal approach using a right middle turbinectomy with a unilateral, vascularized nasoseptal flap was raised on the sphenopalatine artery, to be used as part of the skull base reconstruction after tumor removal [23]. A wide anterior sphenoidotomy under image guidance and with the aid of Doppler ultrasound was performed. For OGM, our surgical approach is similar to above with the addition of a transethmoidal transcribriform approach as previously described [15]. We did not violate the frontal sinus in our series of OGM patients and therefore we did not require a DRAF III or modified Lofthrop procedure. A multilayered reconstruction was used to close the dural defect with DuraGen (Integra NeuroCare, San Diego, CA, USA) and autogenous fascia lata placed as an inlay (intradurally) and then another layer of fascia lata as an outlay (extradurally). Next the harvested vascularized nasoseptal flap was laid over, fully covering the dural and fascia lata graft with the edges in contact with adjacent surrounding bone edges. Next, tissue glue (Tisseel; Baxter, Deerfield, IL, USA) was applied after the flap edges were covered with Surgicel (Ethicon, Cornelia, GA, USA) collagen sponge squares as the final layer. Usually an inflated balloon catheter was used for approximately 4 days as a scaffold and nasal packing was used to prevent graft migration. Post-operative antibiotics were continued until the nasal packing was removed. 2.5. Literature search A PubMed literature search was performed using the following search headings: ‘‘tuberculum sellae’’, ‘‘olfactory grove’’, ‘‘meningioma’’, ‘‘endoscopic’’, ‘‘endonasal’’, ‘‘extended transsphenoidal’’ and ‘‘expanded endonasal approach’’. Articles were retrieved and reviewed for patients undergoing pure EEE approaches in addition to all references therein being assessed for further relevant cases. Single case reports were excluded. Inclusion criteria were: (1) data presented in a disaggregated fashion; (2) patients clearly identifiable as having undergone a pure EEE approach for either OGM or TSM with no previous biopsy and/or surgery; and (3) minimum
Twenty-three patients with either OGM (n = 6) or TSM (n = 17) were treated by the senior authors (F.G. and G.Z.) using the pure EEE approach during the study period (Table 1). The median age at the time of surgery was 53 (range 43–71) and 62 (range 37–86) years for OGM and TSM patients, respectively. The presenting symptom varied with incidental (3/6), headache (2/6) and visual changes (1/6) in the OGM group while visual changes (visual disturbance, either acute deterioration, visual field deficit or both) was the major symptom (11/17) in the TSM group. The maximum diameter of the tumor ranged from 1.3–5.2 cm for OGM and 1–3.3 cm for TSM. Peritumoral edema was present in four OGM patients and one TSM patient. The optic apparatus was involved in 3/6 OGM and 15/17 TSM patients. The duration of surgery was a mean of 8.75 hours and 7.4 hours in the OGM and TSM groups, respectively. In regards to skull base reconstruction, only the first patient in 2006 had a nasoseptal flap that was not utilized. In the remaining patients both neurosurgeons used a nasoseptal flap, however, there was a notable difference in reconstruction, with F.G. preferring fascia lata and autologous fat whereas G.Z. preferred a synthetic collagen for the inlay closure. Average blood loss was 1000 cc in OGM patients and 200 cc in TSM patients. A gross total resection (Simpson grade I and II) was achieved in 4/6 OGM (66.7%) and 11/17 (64.7%) TSM patients. The residual tumor for the OGM patients was on the carotid in one patient and the falx in the other. Of the six partial resections in the TSM group, five had residual tumor adherent to or encasing the carotid and the other residual was adherent to the anterior clinoid. Fig. 1 demonstrates typical pre- and postoperative appearances. No patient experienced a deterioration of their visual status. Two OGM patients who had visual disturbances pre-operatively had improved vision post-operatively. In the TSM series, 11 patients had visual disturbance prior to surgery. Five of these patients showed no improvement of vision post-operatively and at follow-up. Of the six TSM patients with improvement, all had improved visual acuity and three had improved visual fields on formal assessment. For one TSM patient with advanced age and medical co-morbidities the pre-operative intention was to decompress the optic apparatus in an attempt to preserve vision. Their vision improved postoperatively with no endocrine abnormality or CSF leak. There was no peri-operative mortality, although one patient died 3 months post-operatively after the worsening of a pre-existing respiratory disease. There were no endocrine abnormalities in the OGM group. Endocrine disturbance was noted in three TSM patients post-operatively, with transient syndrome of inappropriate anti-diuretic hormone in two and transient diabetes insipidus in the other. One patient experienced toxic shock syndrome post-operatively, despite being on appropriate standard post-operative antibiotics, for which the cause was not identified. Post-operative CSF leaks occurred in four patients (OGM 2/6; TSM 2/17) one of whom also had a CSF infection. CSF leaks were explored with use of the endoscope, and repaired with fascia lata and/or DuraGen. Lumbar drainage was used for 3–5 days. One TSM patient underwent craniotomy after 2 years of follow-up for residual tumor on the anterior clinoid because of recurrence of the presenting symptom of visual deterioration. Their vision improved after this second operation with no residual tumor and no change in pathology. Pathology in all
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Fig. 1. Coronal (A, E, C, G) and sagittal (B, F, D, H) T1-weighted pre- and post-operative MRI with gadolinium contrast for patients who underwent a pure endoscopic endonasal approach with a nasoseptal flap for closure. Representative images from a 53-year-old woman with olfactory groove meningioma who presented with headaches (A, B), and achieved gross total resection with no cerebrospinal fluid leak as shown at 6 month follow-up (C, D). Representative images of a tuberculum sellae meningioma in a 40-year-old woman with visual changes (E, F). Follow-up imaging at 26 months showing no residual tumor with no cerebrospinal fluid leak (G, H).
patients was meningioma World Health Organization Grade I except one TSM patient with Grade II meningioma. No patients underwent either pre-operative or post-operative radiation or chemotherapy. The average follow-up period was 4 months (range 3– 9 months) in the OGM series and 9.4 months in the TSM series (range 3–26 months). 3.2. Literature review We identified a total of 14 articles with adequate disaggregated data describing a further 24 OGM [15,24,25] and 174 TSM [14–16,18,20,21,26–33] [34,35] patients who had undergone a pure EEE approach for surgical management. The contents of these articles, in combination with our patient series, are detailed in Table 2 and Table 3. With the addition of our series gross total resection was achieved in 73% and 56.3% of patients with a cumulative post-operative CSF leak rate of 30% and 14% in OGM and TSM patients, respectively. 4. Discussion ASM vary in their presentation due to their location. OGM are usually midline but as their size increases they may become asymmetric. The frontal lobes are always displaced superiorly and posteriorly. Their growth can also occur inferiorly through the cribriform plate into the ethmoid sinus, through the planum sphenoidale into the sphenoid sinus, or laterally through the orbit [26,36]. Their diagnosis is often made late due to their insidious growth. TSM often cause displacement of the optic chiasm posteriorly and optic nerves superolaterally, resulting in visual impairment, the most common symptom on presentation, and often optic atrophy [5,17,37]. Preservation of visual function is the most important indication for surgery [8,38]. The pure EEE approach is believed to have a number of advantages including: (1) elimination of brain retraction and a lack of optic apparatus manipulation with the wide removal of cranial base bone; (2) early control of vascular supply by devascularization of the tumor and preservation of the
supply to the optic nerves and chiasm from the hypophyseal vessels; (3) no facial/scalp incision for improved cosmesis; and (4) it is well tolerated by patients. [39] The published literature on the pure EEE approach for OGM and TSM is limited. Several reports are of endoscope-assisted microscopic approaches; that is, the endoscope is only introduced at the end of the microscopic procedure to assess resection [26,27,40]. Others detail a mixed case series of endoscope-assisted and pure endoscopic approaches [29]. Thus assessment of the limitations and potential adverse effects and benefits can be difficult. We report our experience of the pure EEE approach for OGM and TSM while combining our data with reports containing disaggregated data that can be clearly identified as a pure EEE approach. Unfortunately, the literature is restricted by a lack of consistency in reported parameters. Overall, including our series, there were 30 OGM and 174 TSM treated via a pure EEE approach, of which the majority were women as identified previously [8]. In general, the follow-up periods preclude complete comparison to other approaches [6,17,41]. However, the published series do not report any tumor recurrences in the patients who had a gross total resection. The GTR rates in our series of 66.7% (4/6) for OGM and 64.7% (11/ 17) for TSM compare well with the pure EEE resection rates of 77% for OGM and 56.3% for TSM of the combined published series with ours included. Similarly, these results compare well with the GTR rates seen in published series of transcranial excisions [8,37,41,42]. Optic canal (OC) invasion by TSM has been reported to occur in 24–75% of transcranial cases [2,17]. The exact site of invasion (medial or lateral in the canal) has led to intense debate as to which is the most rational approach for dealing with OC invasion [17,19,42]. Proponents of the EEE approach have suggested that as most OC invasion is medial, it is most effectively managed by an endonasal medio-lateral route [19]. Two OGM and four TSM patients in our series had OC invasion and this was readily dealt with via a pure EEE approach. Two of the four TSM patients had a residual tumor on the optic nerve. Only one of the two TSM patients with residual tumor on the optic nerve had improvement of vision, while the other patient’s vision was similar to their pre-operative state.
3–60, mean 29.4 9/ 30 = 30% 22/ 30 = 73% 5M 25F = 30 Total
CSF = cerebrospinal fluid, DI = diabetes insipidus, GTR = gross total resection, F = female, H/a = headache, ICA = internal carotid artery, M = male, N/A = not applicable. a Integra NeuroCare, San Diego, CA, USA. b Covidien, Dublin, Ireland. c Pfizer, New York, NY, USA.
3–27, mean 10 1/5 Intradural fat, tensor fascia, vascularized nasoseptal flap, surgical, DuraSealb, Gelfoamc, bone 2/ 5(40%) ICA Visual (3/5), H/a (2/ 5), anosmia (1/5) 1M 4F Padhye et al. 2012[25]
28–74, mean 54
1M 3F de Divitiis et al. 2008 [14]
35–65, mean 49
1.4–5.8
4/5(80%)
1/ 4(25%) None 4/ 4(100%)
None
8–12, mean 9.8 None
3/4 normal, 1/4 unchanged 2/3 unchanged No
5–32, mean 13.5
12–48 None Improved 8/8 (100%) N/A No
Changed over time: initially fibrin glue/ dural substitute/fat; then DuraGena ‘‘inlay’’ with nasoseptal flap, fat/ Gelfoamc Mixed (collagen sponge, dural subsitute, fibrinogen sealant), latterly pedicled flap 4/ 15(27%) Cavernous sinus
Incidental (1), visual (8), seizure (2), H/a (5), anosmia (1) H/a (1), psychiatric (2), hyposmia (1), visual (1) 35–79, mean 58 3M 12F
Volume 3.1– 109.3 cm3, mean 47.6 cm3 2–4.8
10/ 15(66.7%)
3–9 None Improved 2/2(100%) H/a (2), visual (1), incidental (3) 33–71, median 53 6F
Khan et al. 2013 (current series) Gardner et al. 2008 [15]
3.1–4.9
4/ 6(66.7%)
Carotid, falx
2/ 6(33%)
Nasoseptal flap
No (only if leak)
5–18, mean (8.7)
Post-op endocrine abnormality Presenting symptoms Tumor size(cm) Age range (years) Patients Authors and year
Table 2 Reports of olfactory groove meningiomas in the literature
GTR
Site of residual disease
CSF leak rate
Reconstruction technique
Lumbar drainage
Length of stay (days)
Visual outcome
Follow-up range (months)
O.H. Khan et al. / Journal of Clinical Neuroscience 21 (2014) 927–933
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All the published reports (Table 2, Table 3) contained patients who were objectively assessed for visual status pre- and postoperatively. The cause of visual disturbance is believed to be compression leading to ischemia and demyelination of the optic apparatus [17]. Visual improvement appears to be the norm with the remainder of patients remaining stable. Vision rarely appears to deteriorate after the EEE approach but has been reported in transcranial TSM series at rates of 11–29% [15]. It has been suggested that visual improvement is more common if symptoms have been present for less than 6 months [8]. Only one of our patients had symptoms for less than 6 months. Other series of the pure EEE approach tend not to report the duration of presenting symptoms. After the pure EEE approach transient or permanent endocrine dysfunction was absent in all OGM patients, but was transient in two TSM patients. Observed rates of post-operative endocrine dysfunction ranged from 0–33% for TSM when reported (Table 2). Most of these are disorders of sodium homeostasis, and this reflects the close proximity of the pituitary stalk during fine dissection of the tumor. Reconstruction of the anterior cranial base and closure of the dural defect has been accomplished via a number of methods. Most series included the use of a fascial graft or a dural synthetic substitute augmented with combinations of fat, mucoperichondrium, collagen sponge and fibrinogen sealant [43]. The reconstruction is then be held in place by nasal packing or a Foley catheter balloon. Lately several groups, including our own, have adopted the use of the nasoseptal vascularized flap [23] as a means of reducing post-operative CSF leaks, with significant success. A further advantage of this type of reconstruction for the skull base is its apparent tolerance of radiotherapy, which is sometimes required for lesions in the anterior skull base [44]. Other means of closure of skull base defects include the ‘‘gasket-seal’’ technique which has also shown success in reducing CSF leaks [45]. In our report, the combined CSF leak rate was 30% for OGM and 14% for TSM (Table 2, Table 3). A meta-analysis of endoscopic surgery for OGM and TSM in 2010 reported a CSF leak rate of 31.6% and 24.8%, respectively. Open cranial surgery had a CSF leak rate of 6.3% for OGM and 4.3% for TSM [46]. A thorough discussion of open versus endoscopic resection has been adequately addressed in the paper by Komotar et al [46]. One explanation for our four patients with CSF leak is that one patient was the only one in the series who did not have a nasoseptal flap, only fascia lata and fat, while the other three did not have autologous fascia lata as an inlay. Interestingly, in a mixed series of ASM the highest CSF leak incidence was seen with the smallest tumors, the tuberculum lesions [15]. We did not find any relationship between size and occurrence of CSF leaks in both OGM and TSM patients. All the published series included in this review are retrospective studies from high volume centers with a subspecialty multidisciplinary approach to the EEE method, creating an associated inherent recognized bias due to referral basis and the nature of the practice being prone to reporting bias. It is likely that patient selection combined with the surgeon’s familiarity of the approach and availability of an ENT surgeon will mean that the pure EEE approach for ASM will increase at these high volume centers, which further highlights the need for reporting of outcomes. Additional important issues to consider before using this approach for ASM are tumor size, OC invasion and relationship to adjacent neurovascular structures. Based on our experience, key features of relative contra-indication include extension lateral to the optic canal, presence of extreme mass effect on the frontal lobes due to brain edema or tumor mass, presence of hydrocephalus, previous surgery (open or EEE approach), and concerning features on MRI for malignant disease. Relative factors that would require careful consideration pre-operatively include superior extension of the tumor, and calcification within or surrounding the tumor.
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Table 3 Reports of tuberculum sellae meningiomas in the literature Reconstruction technique
Lumbar drainage
11/17(54%) ICA, sella, optic nerve
2/17 (11.8%)
Mixed (fascia lata and nasoseptal flap)
N/A
15/19(79%) N/A
1/19(5%)
Fascia lata, mucosal flap
No (only if 4–19, mean post-op 7.7 leak) N/A N/A
1.3–3.1
Visual (7), H/a (1)
3/8(38%)
N/A
0/8(0%)
Fascia lata
N/A
N/A
1.7–3.5
Visual (3), facial numbness (1)
1/8(13%)
1/8(13%)
Fat and fascia lata
Yes
N/A
N/A
Visual (2)
2/2(100%)
ICA, cavernous sinus None
0/2(0%)
Mixed (fascia lata and nasoseptal flap)
Yes
1.6–4.5
Visual:VA (5), VF (7)
6/16(38%)
Mixed (fascia lata, methacrylate, mucoperichondrium, fibrin glue)
2.5–4.0
Visual (11), H/a (1)
11/21(52%) Optic canal
1/22 (4.5%)
1.3–3.2
Visual 6 (VA 6, VF 6), H/a (2)
6/7(86%)
1.5–3
Visual (10)
6/1346%
Volume 2.1– 16.2 cm3, mean 7.5 cm3 2–3.5
Patients
Age range (years)
Tumor size range (cm)
Presenting symptoms
GTR
Khan et al. 2013 (current series)
4M 13F
0.8–3.3
Visual (11), H/a (5), incidental (1)
Ogawa et al. 2012[32]
5M 14F
0.9–2.9
Van gompel et al. 2011[18]
8M
Bowers et al. 2011[29]
4M 4F
Liu et al. 2011[31]
1M 1F
Ceylan et al. 2011[30]
9M 7F
Wang et al. 2010[4]
12M 9F
de Divitiis et al. 2008[14]
3M 4F
37–86, median 60 43–79, mean 58.9 31–77, median 69 39–77, median 66 Aged 62 and 38 32–78, median 51 27–67, median 52 47–80, mean 58.7
Fatemiet al.2009[27] 3M 10F
Gardner et al. 2008[15]
13M 12F
Laufer et al. 2007[16] 3M
Kitanoet al.2007[26] 2M 14F
Padhyeet al.2012[25] 2F
Chowdhury et al. 2012[33]
2M 4F
Attia et al. 2012[35]
6F
Bohman et al. 2012[34]
2M 3F
Total
71M 103F = 174
31–77, mean 51.3 39–72, median 53
51–73, median 66 42–76, mean 53.8 65–66, mean 65.5 29–52, mean 39.5 31–74, mean 56.5 25–77, mean 53.2
Site of residual disease
Length of stay, range (days)
Visual outcome
Postoperative Endocrine abnormality
6 improved, 5 unchanged
2/13 transient SIADH 3–26, (15%), 1/13 transient DI median 10 (7.7%) None 3–59
14/19 improved, 3 unchanged, 2 deteriorated 5 improved, 3 unchanged
Follow-up range (months)
None
3–65, median 9.5
N/A
N/A
N/A
N/A
Improved (100%)
None
1.5 & 3
Yes
6–8
6 improved, 3 unchanged
1/9 permanent DI
3–33, median 20
Fat and dural substitute
No
2–5
11 improved, 1 unchanged
1/12 transient DI (8%)
6–60, median 28
2/7(29%)
Mixed (collagen sponge, dural subsitute, fibrinogen sealant), latterly pedicled flap
No (only if 5–21, post-op median 9 leak)
1/7 transient DI (14%)
0.75–51, median 24
4/ 13(30%)
Abdominal fat, collagen sponge, titanium mesh, bioglue sealant
Yes (48 hours)
1–13, median 4
1/13 hypopituitarism(7.7%)
6–65, median 27
Visual (10), H/a (1), incidental (1), prior residual tumor (1)
Cavernous sinus, carotid 11/25(44%) Cavernous sinus
5 improved,2 unchanged (3 transient worsening) 9/10 improved,1/10 unchanged
8/ 25(32%)
Mixed
No
N/A
Improved (100%)
1 hypopituitarism
23–58, median 40
Visual 3/3
2/3(66%)
1/3(33%)
Fascia lata and Tisseela or DuraSealb then Floseala
Yes (1)
N/A
3/3improved (100%) 1/3 permanent DI (33%) 6–12, median 9
Cisternal 0/16(0%) and vascular
Optic canal
A-com
Visual (16) Volume 1–20.3 mm3
12/16(75%) Not 2/ Sutured abdominal fascia, Gore-Texc, documented 16(12.5%) hydroxyapatite cement
Yes (9/16) N/A
1.4–2
Visual (2)
2/2(100%)
N/A
0/2(0%)
No
Mean 9
2–4
Visual (6), H/a (2)
5/6(83%)
A-com/A2 segment
1/6(17%)
Intradural fat, tensor fascia, vascularized septal flap, surgical, DuraSealb, Gelfoamd, bone Fascia lata inlay graft, thigh fat
Yes
N/A
1–4
Visual (5), H/a (1)
5/6(83%)
ICA, optic canal
0/6(0%)
Fat, fascia lata inlay – buttress with Medporee, nasoseptal flap, DuraSealb
Yes
N/A
1.4–3
Visual (5), H/a (2)
4/5(80%)
Not 1/5(20%) documented
Nasoseptal flap, fascia lata, fat, DuraGenf
Yes 3/5
N/A
98/ 174 = 56.3%
10/16 improved None (81%), 6/16worse (38%) 2/2 improved (100%) Hyopnatremia (50%)
3–6
3/6 improved, 2/6 unchanged, 1/6 deteriorated 3/6 improved, 2/6 unchanged, 1/6 deteriorated 4/5 improved, 1/5 stable
2/6 hyponatremia (33%)
2–12, mean 7
-
3–39.5, mean 20.75
2/5 hyponatremia (40%)
2–17, mean 7.8
Mean 3
24/ 174 = 14%
A-com = anterior communicating artery, CSF = cerebrospinal fluid, DI = diabetes insipidus, GTR = gross total resection, F = female, H/a = headache, ICA = internal carotid artery, M = male, N/A = not available, SIADH = syndrome of inappropriate anti-diuretic hormone, VA = visual acuity, VF = visual field. a Baxter, Deerfield, IL, USA. b Covidien, Dublin, Ireland. c W. L. Gore & Associates, Newark, DE, USA. d Pfizer, New York, NY, USA. e Stryker, Kalamazoo, MI, USA. f Integra NeuroCare, San Diego, CA, USA.
O.H. Khan et al. / Journal of Clinical Neuroscience 21 (2014) 927–933
CSF leak rate
Authors and year
O.H. Khan et al. / Journal of Clinical Neuroscience 21 (2014) 927–933
5. Conclusion Based on our experience together with results of reported case series the pure EEE approach for OGM and TSM can be safely utilized by surgeons appropriately experienced in endoscopic endonasal procedures. We can identify important relative contraindications such as extension lateral to the optic canal, presence of significant mass effect on the frontal lobes and potential intratumoral calcification, which should caution against use of the EEE approach. Overall, as we continue and increase our experience with this surgical approach it is important to maintain and report longer-term follow-up to be able to accurately assess the recurrence rates of ASM excised via an EEE approach. Conflicts of interest/disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. Acknowledgements D.H. was the recipient of a European Association of NeuroOncology Educational Fellowship grant. References [1] Coppens J, Couldwell W. Olfactory groove meningiomas. In: Pamir MN, Black PM, Fahlbusch R, editors. Meningiomas: a comprehensive text. Philadelphia: Saunders; 2009. [2] Yasargil M. Microneurosurgery, vol. 4b. Stuttgart, Germany: Thieme; 1996. [3] de Divitiis E, Esposito F, Cappabianca P, et al. Tuberculum sellae meningiomas: high route or low route? A series of 51 consecutive cases. Neurosurgery 2008;62:556–63 [discussion 556–63]. [4] Wang Q, Lu XJ, Ji WY, et al. Visual outcome after extended endoscopic endonasal transsphenoidal surgery for tuberculum sellae meningiomas. World Neurosurg 2010;73:694–700. [5] Goel A, Muzumdar D, Desai KI. Tuberculum sellae meningioma: a report on management on the basis of a surgical experience with 70 patients. Neurosurgery 2002;51:1358–63 [discussion 1363–4]. [6] Fahlbusch R, Schott W. Pterional surgery of meningiomas of the tuberculum sellae and planum sphenoidale: surgical results with special consideration of ophthalmological and endocrinological outcomes. J Neurosurg 2002;96: 235–43. [7] Chi JH, McDermott MW. Tuberculum sellae meningiomas. Neurosurg Focus 2003;14:e6. [8] Ganna A, Dehdashti AR, Karabatsou K, et al. Fronto-basal interhemispheric approach for tuberculum sellae meningiomas; long-term visual outcome. Br J Neurosurg 2009;23:422–30. [9] Avci E, Akture E, Seckin H, et al. Level I to III craniofacial approaches based on Barrow classification for treatment of skull base meningiomas: surgical technique, microsurgical anatomy, and case illustrations. Neurosurg Focus 2011;30:E5. [10] DeMonte F. Surgical treatment of anterior basal meningiomas. J Neurooncol 1996;29:239–48. [11] Hentschel SJ, DeMonte F. Olfactory groove meningiomas. Neurosurg Focus 2003;14:e4. [12] Andrews BT, Wilson CB. Suprasellar meningiomas: the effect of tumor location on postoperative visual outcome. J Neurosurg 1988;69:523–8. [13] Kim TW, Jung S, Jung TY, et al. Prognostic factors of postoperative visual outcomes in tuberculum sellae meningioma. Br J Neurosurg 2008;22:231–4. [14] de Divitiis E, Esposito F, Cappabianca P, et al. Endoscopic transnasal resection of anterior cranial fossa meningiomas. Neurosurg Focus 2008;25:E8. [15] Gardner PA, Kassam AB, Thomas A, et al. Endoscopic endonasal resection of anterior cranial base meningiomas. Neurosurgery 2008;63:36–52 [discussion 52–4]. [16] Laufer I, Anand VK, Schwartz TH. Endoscopic, endonasal extended transsphenoidal, transplanum transtuberculum approach for resection of suprasellar lesions. J Neurosurg 2007;106:400–6. [17] Mahmoud M, Nader R, Al-Mefty O. Optic canal involvement in tuberculum sellae meningiomas: influence on approach, recurrence, and visual recovery. Neurosurgery 2010;67:ons108–18 [discussion ons118–9]. [18] Van Gompel JJ, Frank G, Pasqini E, et al. Expanded endonasal endoscopic resection of anterior fossa meningiomas: report of 13 cases and meta-analysis of the literature. Neurosurg Focus 2011;30:E15.
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