Surgical Management of Midline Anterior Skull Base Meningiomas

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Chapter 34 Surgical Management of Midline Anterior Skull Base Meningiomas

Surgical Anatomy

Meningiomas arising in the midline of the anterior fossa are generally separated in the more ventral olfactory groove meningiomas and the more dorsal planum sphenoidale and tuberculum sellae meningiomas. Olfactory groove meningiomas arise over the cribriform plate of the ethmoid bone and the area of the frontosphenoid suture. Those tumors may grow symmetrically around the crista galli and thus may involve any part of the planum of the sphenoid bone or extend predominantly to one side. They occurred with a frequency of less than 6% in our series of 1200 meningiomas. Of all anterior skull base meningiomas, 22% were pure olfactory groove meningiomas. Of these, 7% had at least one additional meningioma at a different location. Planum sphenoidale/tuberculum sellae meningiomas arise from the roof of the sphenoid sinus and the tuberculum sellae, which is an area between the optic nerves and the anterior clinoid processes belonging to the frontal part of the middle cranial fossa. The tuberculum sellae is located between the chiasmatic grooves and on either side at the optic foramen, which transmits the optic nerve and ophthalmic artery to the orbit. Behind the optic foramen, the anterior clinoid process is directed posteriorly and medially and attaches to the tentorium cerebelli. These structures are frequently overgrown by these types of meningiomas, as are the posteriorly located dural folds of the sella turcica and the lateral adjacent cavernous sinus (Fig. 34-1). Planum sphenoidale/tuberculum sellae meningiomas occurred at rates similar to those of olfactory groove meningiomas in our series: less than 6% of all intracranial meningiomas but 21% of anterior skull base meningiomas.

The planum sphenoidale and tuberculum sellae are part of the sphenoid bone. The former is a dorsal extension beyond the ethmoid bone and part of the anterior cranial base; the latter belongs to the middle cranial base. Whereas planum sphenoidale meningiomas usually push the optic nerves dorsally and caudally, tuberculum sellae meningiomas lead to an upward bulging of these structures. However, it is often difficult to clearly separate these tumors simply based on their bony covering. Rather, their relationship to the optic nerves and chiasm can distinguish these tumors as to their most likely origin. Both entities might grow between, around, and beyond the optic nerves. Depending on the exact extension, tuberculum sellae tumors are usually approached either frontolaterally or strictly laterally from the pterion using an angle that allows viewing posterior to the optic nerves.

Branches of the ethmoidal, meningeal, and ophthalmic arteries enter through the midline of the base of the skull and constitute the primary blood supply of those tumors. In smaller tumors, the A2 segments of the anterior cerebral arteries usually are not involved in the tumor capsule but rather are separated from the tumor by a rim of cerebral tissue and arachnoid. However, in large tumors, these and additional segments, e.g., the frontopolar or other small branches originating from the anterior cerebral arteries, may adhere to the posterior and superior tumor capsule. They should be meticulously coagulated and separated from the capsule to avoid postoperative bleeding.

The olfactory nerves either are displaced laterally on the lower surface of the tumor or are adherent, compressed, or even not visible while diffusely spread within the tumor capsule. Preservation of these nerves should be attempted in small tumors, resulting in displacement of one or both nerves. Once the olfactory nerves are compressed by large tumors or even tightly involved in the tumor capsule, it is difficult to preserve them, and this becomes almost impossible when the tumor has a broad attachment to the dura and infiltrates adjacent, often hypertrophic bone. In addition, in large tumors, the optic nerves and chiasm may be displaced downward and posteriorly, which is in contrast to tumors originating from the sella region.

Clinical Presentation

Olfactory groove meningiomas are on average larger than meningiomas at different locations in our series. This is most likely due to the relative lack of focal symptoms at the frontal base with smaller meningiomas. For large tumors, the slow growth rate allows surrounding tissues to adapt. Many symptoms are difficult to localize neurotopically, and the initial consultations of family and physicians often tend toward interpretation of these as functional personality changes rather than focal cerebral symptoms. Personality changes, such as apathy and akinesia, can be common when the tumors grow to larger size; in our series, this was found in up to 13% of patients. Onset of these symptoms is gradual, and they may not be observed early in their course. Other common symptoms include headache and visual deficits, both of which were more frequent in frontal meningiomas than in any other type of meningioma in our series. Because the optic nerves and chiasm are compressed superiorly by the tumor, an inferior visual defect was most common in up to one third of our patients. The Foster-Kennedy syndrome of unilateral optic atrophy and contralateral papilledema, although originally described in olfactory groove meningiomas,1 occurred in only a small number of patients.

Double vision is a rare symptom, occurring in less than 6% of patients. In our series, smelling disorders up to anosmia were apparent in 64.5% of the patients that were diagnosed based purely on the routine preoperative workup. Only 7.1% were completely anosmic preoperatively. Interestingly, anosmia is not an important symptom for most patients, most likely because it develops slowly. In Cushing and Eisenhardt’s series, the sense of smell was the primary symptom in only 3 of the 29 patients.2 Bakay reported that even if anosmia was apparent, it was not the leading symptom.3

Epilepsy was less frequent, occurring in 12% of cases, compared to all other supratentorial sites and was only lower, occurring in 8% of cases, in medial sphenoid wing tumors. Planum sphenoidale and tuberculum sellae meningiomas encompassed a further 21% of frontobasal meningiomas in our series. They presented more frequently with visual pathway symptoms than did olfactory groove meningiomas and less frequently with disorders of smell. Symptomatic epilepsy was also rare in these more dorsal tumors and occurred only in very large lesions.

Evaluation of Radiologic Studies in Planning the Operation

The standard diagnostic means for evaluation of anterior midline meningiomas such is magnetic resonance imaging (MRI), because it can delineate the mass effect relationship to other important structures such as the optic nerves, the relationship to the anterior cerebral arteries, and the elevation of the frontal lobes. However, cranial computed tomography (CT) and angiography are important adjuncts if the destruction of the anterior skull base, the infiltration of the ethmoid bone, the relationship of the major vessels, and the vascular supply are of interest.

Noncontrast CT scanning classically demonstrates a dural-based, homogeneous tumor of increased density compared to the surrounding brain, with variable mass effect and surrounding edema. Hyperostosis of the adjacent skull base is a common feature. Contrast agent administration produces dramatic homogeneous enhancement of the tumor and often reveals a dural tumor tail.

For preoperative and diagnostic evaluation, MRI is essential and provides additional information and good soft-tissue differentiation. With T1-weighted MRI, the tumor is of equivalent signal intensity compared to the surrounding brain, and T2-weighted MRI reveals that the tumor signal is slightly increased compared to the normal brain but less than that of cerebrospinal fluid. Fluid-attenuated inversion recovery and T2-weighted MRI highlight surrounding edema. With administration of gadolinium contrast medium, MRI demonstrates homogeneous tumor enhancement. It is crucial to analyze the relationship of the optic nerves and anterior cerebral arteries to the tumor capsule. Magnetic resonance angiography may provide essential information about blood supply and displaced arteries or even arteries embedded within the tumor. In correlation with CT, the extension into the osseous structures, the underlying ethmoid and sphenoid sinuses, and the foramina yields additional information. Modern imaging tools easily facilitate the coregistration of many imaging modalities to visualize the tumor from any angle and to plan the operation virtually.

In recent years, angiography generally has not been indicated unless embolization is planned. The classic angiographic appearance of a meningioma is that of increasing hypervascular tumor blush throughout the arterial phase, persisting well into the late venous phase with slow washout. Hypervascularity may complicate and lengthen the operation. Therefore, embolization may be considered, which involves the devascularization of the tumor’s blood supply through the placement of an embolic agent via a microcatheter into the feeding arteries. However, the surgeon should be aware of a considerable rate of hemorrhagic and ischemic complications when using small particles for embolization.47

General Aspects of Surgical Management

As the majority of meningiomas are benign, well-circumscribed extra-axial tumors, complete surgical removal should be the primary goal in most instances. The neurologic integrity has to be preserved as it would be in any other neurosurgical procedure. Due to the relation of anterior midline meningiomas to adjacent neurologic eloquent areas, complete tumor removal even with resection of infiltrated dura or removal of infiltrated bone might be achieved with low morbidity in most cases. However, when tumors are firmly attached to the anterior vessels or the optic chiasm, complete removal might constitute a high risk for damage of those structures. In these cases a small piece of adherent capsule might remain and is controlled by periodic MRI scans. Upon recurrence, reoperation and adjuvant radiation therapy may be considered.

The decision for surgery should not be based on age alone as long as the patient’s general health condition is stable and the patient is increasingly hampered by neurologic symptoms. Because symptoms usually occur late and at larger tumor volumes that are often increased by surrounding edema, there are rarely alternatives to surgical treatment.

On examination, the sense of smell is often compromised; however, remaining function is difficult to test and a formal olfactogram should be requested. If unaltered, the patient should be warned about the loss of this function.

Preoperatively, steroids are only applied if significant edema is present. Intraoperatively, a steroid bolus, e.g., dexamethasone of up to 24 mg, is given and subsequently weaned over a period of 3 to 7 days postoperatively. When the patient arrives in the operating room, intravenous antibiotics are given once as a prophylaxis and for one week afterward if the frontal sinus was opened.

After induction of anesthesia, the application of intravenous glycerol or 15% mannitol might be considered in a case of extensive edema.

Bifrontal Approach

General Considerations

The bifrontal approach was first described by Horsley8 and Cushing9 and was later proposed by Tönnes,10 who preserved the frontal brain tissue by a subfrontal approach.11 Many others have used the bifrontal approach for large tumors of the frontal base, such as Al-Mefty,12 Nakamura et al.,13 and Ransohoff and Nockels.14 A bifrontal craniotomy might be considered for patients with large tumors because this approach gives direct access to all sides of the tumor. Due to the wide exposure, retraction on the frontal lobes is minimal. It simultaneously allows interruption of the blood supply, preparation of the frontobasal matrix of the tumor, and concomitant decompression. There is usually no problem from the ligation of the anterior sagittal sinus. However, venous drainage should be evaluated by preoperative imaging to avoid venous congestion, and coagulation of draining veins from the anterior frontal lobe should be avoided of possible. A navigation system might be used to avoid opening the frontal sinus; however, if the frontal sinus is entered, meticulous closure of the defect should prevent any complications.

Operative Technique

The patient is placed in the supine position with the knees slightly flexed and the head slightly elevated and extended. A three-point skeletal-fixation headrest system is used. Usually, only a small area of hair needs to be shaved to prepare a coronal incision through the skin while preserving the pericranial tissue. The skin of the posterior aspect of the incision is elevated, and the pericranial tissue is incised below the skin. This step gives extra pericranial tissue, which might be used later to cover the floor of the anterior fossa and to patch the convex dura as needed. The skin flap and underlying tissue, including the pericranial tissue, are then turned down together using fishhooks. According to the size and extension of the tumor, bur holes are placed just below the end of the anterior temporal line or keyholes are placed above the pterion and on each side of the sagittal sinus anterior to the skin incision (Figs. 34-2 and 34-3).

After blunt dissection of the dura from the tabula interna of the skull bone, particularly in the midline area, the bone flap is usually cut in one piece. The bone is cut just above the supraorbital ridge from each side as far medially as possible. Usually, this process leaves about 1 cm of bone in the midline. Here, because of the irregular bone projecting from the inner table of the skull, sawing might be difficult. If complete cutting across the frontal sinus is not possible, the outer table is cut separately. The inner table is then broken as the bone is elevated, and the free bone flap is removed. A rarely necessary method is to cut a right frontal bone flap first, free the sagittal sinus, and then cut a second bone flap across the midline to the left side.

The frontal sinuses are entered frequently. Whether the mucosa needs to be completely removed remains controversial. A multilayered closure of the frontal sinus is prepared. First, a layer of bone wax is used to close the sinus during the intracerebral part of the operation. For final closure, a pericranial flap is formed (Fig. 34-3) that can be inserted once the tumor is removed. The pericranial flap should be sutured to the frontal edge of the dura and intradurally as far posterior as possible to cover any defects (Fig. 34-4). In addition, frontobasal dura gaps can be covered that occurred during tumor and dural matrix removal. In case of an opened ethmoid sinus, the pericranial tissue should cover this too. Sutures are placed along the edge of the craniotomy to control epidural bleeding.

A slightly curved dural incision is performed over each medial inferior frontal lobe adjacent to the edge of the craniotomy opening but leaving a sufficient rim for safe and convenient closure of the dura. Depending on the bony removal, the dural opening can be curved basally or upward. This incision can be tailored to the specific line of approach to the meningioma. If a lateral approach is needed, in addition to the midline approach, the dural opening is extended as needed. It is carried medially near the edge of the sagittal sinus, thereby allowing good exposure yet protecting most of both frontal lobes during the operation. Bridging veins from the anterior frontal lobe to the midline area might be coagulated and divided if necessary. To obtain better exposure of the sagittal sinus, the frontal lobes might be carefully retracted. Then the sagittal sinus is divided between two silk sutures, and the falx is cut (Fig. 34-3). The frontal lobes are gently retracted slightly laterally and posteriorly to open the view to the anterior and superior surface of the tumor, lying in the midline with attachments to the falx and crista galli.

Generally, two alternative procedures are suggested. Particularly in large olfactory groove meningiomas, we prefer devascularization of the tumor as early as possible and only minor debulking for preparation along the base of the skull. This procedure seems to be associated with less blood loss and does not produce difficult angles for dissecting of the tumor capsule from the surrounding brain parenchyma. The dissection along the base is alternated with internal decompression of the tumor to gradually bring into view the base and to remove the bulk of the tumor. This brings down the rim of the tumor and the brain tissue toward the skull base. The cerebral cortex is carefully separated from the tumor capsule by division of arachnoid and small vascular attachments. The self-retaining retractors are repositioned accordingly.

The alternative procedure is to remove the core of the tumor first. This leads to higher blood loss and poorer control of the blood supply during debulking. However, preparation of the skull base after debulking of the tumor is easier compared to the initial devascularization procedure. The initial step in that procedure is to open the anterior capsule of the tumor. If histology is in doubt, a biopsy might be taken now for frozen-section histology. Depending on the amount of bleeding, large parts of the anterior and midline portion of the tumor can be removed before the part of the tumor capsule that is attached at the anterior midline is divided. Numerous small blood vessels that penetrate the bone in the frontal fossa usually constitute the main blood supply for those tumors. Therefore, in cases of heavy bleeding after starting debulking the tumor, it might be necessary to switch strategies and do the basal devascularization first. Those vessels are occluded by bipolar coagulation and, occasionally, bone wax or soft drilling with a diamond drill.

Devascularization of the tumor as early as possible is especially important in large olfactory groove meningiomas. As the debulking progresses, the remaining tumor is brought down away from the brain tissue toward the cribriform plate, where most of the work takes place. Thus, it is an alternating procedure of dissection along the base and internal decompression of the tumor, resulting in the exposure of the base and removal of the bulk of the tumor. For decompression, an ultrasound surgical aspirator can be used that is effective even for tumors of firm consistency. By preventing the frontal lobes from falling into the decompression area by self-retaining retractors, there is enough space to dissect the tumor capsule from the adjacent frontal brain parenchyma. Care should be taken to avoid pressure on the frontal lobes and consecutive postoperative edema or even intraparenchymal hemorrhage. The preparation of the posterior tumor capsule is the most challenging step, because branches of the anterior artery complex might be adjacent to or even involved in the tumor capsule. In most cases, at least the larger vessels can be separated by a small rim of cerebral cortex and arachnoid between the adventitia and the outer tumor capsule. However, when those vessels are firmly embedded within the tumor capsule, a tumor remnant should be left in place. Smaller branches or the frontopolar artery being spread in the capsule might be considered to be occluded and divided if there is no alternative that may not cause a problem.15

The optic nerves and the anterior clinoid process can be visualized by preparing farther back to the sphenoid wing and then medially. If a large tumor has displaced the optic nerves posteriorly and inferiorly, localization might be more difficult because the displacement is frequently associated with arachnoid thickening.

After identification of the involved adjacent neurologic structures and removal of the bulk of the tumor, the area of dural attachment should be meticulously coagulated or preferentially excised. Infiltrated hyperostotic bone should be removed by a high-speed diamond drill. In our view, hyperostosis may contain remaining tumor cells, and the osseous and tumorous vascular supply usually originates from this area. Similarly, any tumor entering the ethmoid sinus should be resected. The region of the excised dura should be covered with a sheet of Tacho-seal,TachoSil, TM or something similar; with a vascularized galeal–periosteal patch or fascia lata over the defect, the patch should be sutured to the remaining dura margin with single stitches and sealed along the border with fibrin glue (Fig. 34-4). Another layer of gelatin sponge is placed over the fascia. The layers might be augmented with fibrin glue.

The convexity dura is closed with another graft of pericranial tissue, and the bone flap is fixed by nonresorbable sutures or miniplates. The bur holes are filled with bone dust or cranioplasty material. A subcutaneous wound drain should be left in place before wound closure.

Unilateral Subfrontal Approach

Operative Technique

The patient’s position depends on the involvement of the midline structures, the displacement and orientation of the A2 segments, and the optic nerve structures. In general, the head is slightly extended posteriorly to allow the frontal lobes to follow gravity. A regular frontal skin incision behind the hair line is used that might be extended over the midline, if anterior and medial visualization are considered. A pericranial flap is always prepared to cover potential dural tears or removed tumor matrix in case of anterior middle fossa involvement (Fig. 34-6). This is not necessary for isolated tuberculum sellae tumors. The craniotomy should aim to visualize the sylvian fissure if posterior retraction along the sphenoid wing is required, remain very low above the plane of the frontal skull base, and extend close to the midline as far as necessary. The craniotomy should be shaped according to the expected irregularities of the frontal skull base, which might otherwise hinder clear visualization along a one-sided trajectory.

For isolated tuberculum sellae tumors a regular pterional craniotomy suffices, whereas for very large tuberculum sellae tumors extending to the frontal base a modified frontal approach might be necessary.

Tumor Removal

Two principle approaches are feasible to begin tumor removal: (1) detach the tumor from its vascularization and dural matrix by dissecting the dural plane and then debulk the tumor safely without further blood loss or (2) enter the tumor directly and debulk before entering into the tumor–brain plane. Both approaches have their merits: we prefer initial dural detachment because the tumor can be rendered bloodless without increasing the compression of the surrounding structures. A narrow window is formed along the dural plane that devascularizes the tumor and makes it movable to a certain degree. Then, the interface of the tumor with the brain can be seen by gentle pulling of the tumor and continuous stepwise resection. With smaller lesions, the tumor can be extracted in toto at this time. The surgeon has to be aware that the arteries are pushed upward and are seen at a late stage of preparation. The contralateral olfactory nerve is the last structure to be identified along the frontal skull base clearly and often has a dense subarachnoid layer that should be preserved.

The alternative technique to initial devascularization is debulking, which was introduced as early as 1938 in the classic monograph by Cushing and Eisenhardt.1 However, even central decompression rarely leads to shrinking of the tumor because these are usually rather stiff and attached to the surrounding brain. The preparation should aim to preserve the olfactory nerves and A2 segments. Therefore, these structures should be visualized as early as possible. Before approaching the dural matrix of the tumor, the olfactory nerve should be freed of the surrounding arachnoid scarring, which is easier from a lateral approach. Piecemeal preparation might be necessary to maintain olfactory nerve integrity because this nerve is particularly vulnerable to bipolar cauterization and inadvertent suctioning. We prefer to protect the nerve with a nonadherent covering such as Bicol collagen sponges rather than using a Cottonoid. If the optic nerves are reached by the tumor, dissection should proceed in an arachnoid plane, which can be of varying thickness and clarity. If a thin layer of tumor is approaching the optic nerves and seems to enter the middle cranial fossa, careful inspection of this side using a bayonet mirror or an endoscope should facilitate visualization of all tumor compartments and their removal using curettes and coagulation of the remaining matrix using an angled bipolar cautery.

Arteries are frequently embedded within thickened arachnoid layers of the tumor capsule. It is necessary to continuously reevaluate the correct plane of dissection because tumor feeding arteries are difficult to differentiate from frontal lobe branches. When the surgeon is in doubt, every vessel is prepared with its arachnoid covering.

Tuberculum sellae meningiomas that push the optic structures upward and do not extend anteriorly can be approached from a pterional craniotomy. Tuberculum sellae meningiomas extending anteriorly and pushing the optic nerves laterally should be considered for a modified frontal approach (Fig. 34-7). If the carotid artery is engulfed and the medial sphenoid wing or the cavernous sinus is involved, any combined approach that includes a pterional opening is recommended.

Olfactory groove meningiomas most frequently underwent radical removal (Simpson grade I and II in more than 94%), which was reflected in only two recurrences (3%) compared to 14% of recurrences/residual tumors for all intracranial meningiomas, in our series (Table 34-1).

Key References

Al-Mefty O. Surgical technique for the juxtasellar area. In: Al-Mefty O., editor. Surgery of the Cranial Base (Foundations of Neurological Surgery, 2 ed.). Boston: Kluwer Academic Publishers; 2010:73-89.

Bakay L. Olfactory meningiomas. The missed diagnosis. JAMA. 1984;251:53-55.

Bendszus M., Monoranu C.M., Schutz A., et al. Neurologic complications after particle embolization of intracranial meningiomas. AJNR Am J Neuroradiol. 2005;26:1413-1419.

Carli D.F., Sluzewski M., Beute G.N., et al. Complications of particle embolization of meningiomas: frequency, risk factors, and outcome. AJNR Am J Neuroradiol. 2010;31:152-154.

Cushing H., Eisenhardt L. Meningiomas, Their Classification, Regional Behaviour, Life History and Surgical End Results. Springfield, Illinois: Charles C. Thomas; 1938.

Hassler W., Zentner J. Pterional approach for surgical treatment of olfactory groove meningiomas. Neurosurgery. 1989;25:942-945.

Kallmes D.F., Evans A.J., Kaptain G.J., et al. Hemorrhagic complications in embolization of a meningioma: case report and review of the literature. Neuroradiology. 1997;39:877-880.

Nakamura M., Struck M., Roser F., et al. Olfactory groove meningiomas: clinical outcome and recurrence rates after tumor removal through the frontolateral and bifrontal approach. Neurosurgery. 2007;60:844-852.

Ransohoff J., Nockels R.P. Olfactory groove and planum meningiomas. In: Apuzzo M.L.J., editor. Brain Surgery Complication Avoidance and Management. New York: Churchill Livingstone; 1993:203-219.

Wakhloo A.K., Juengling F.D., Van Velthoven V., et al. Extended preoperative polyvinyl alcohol microembolization of intracranial meningiomas: assessment of two embolization techniques. AJNR Am J Neuroradiol. 1993;14:571-582.

Numbered references appear on Expert Consult.

References

1. Al-Mefty O. Surgical technique for the juxtasellar area. In: Al-Mefty O., editor. Surgery of the Cranial Base (Foundations of Neurological Surgery, 2 ed.). Boston: Kluwer Academic Publishers; 2010:73-89.

2. Cushing H., Eisenhardt L. Meningiomas: Their Classification, Regional Behaviour, Life History, and Surgical End Results. Springfield, Illinois: Charles C. Thomas; 1938.

3. Bakay L. Olfactory meningiomas. The missed diagnosis. JAMA. 1984;251:53-55.

4. Bendszus M., Monoranu C.M., Schutz A., et al. Neurologic complications after particle embolization of intracranial meningiomas. AJNR Am J Neuroradiol. 2005;26:1413-1419.

5. Carli D.F., Sluzewski M., Beute G.N., et al. Complications of particle embolization of meningiomas: frequency, risk factors, and outcome. AJNR Am J Neuroradiol. 2010;31:152-154.

6. Kallmes D.F., Evans A.J., Kaptain G.J., et al. Hemorrhagic complications in embolization of a meningioma: case report and review of the literature. Neuroradiology. 1997;39:877-880.

7. Wakhloo A.K., Juengling F.D., Van Velthoven V., et al. Extended preoperative polyvinyl alcohol microembolization of intracranial meningiomas: assessment of two embolization techniques. AJNR Am J Neuroradiol. 1993;14:571-582.

8. Horsley V. On the technique of operations on the central nervous system. Br. Med. J. 1906;2:411-423.

9. Cushing H. The meningiomas arising from the olfactory groove and their removal by the aid of electrosurgery. Lancet. 1927;1:1329-1339.

10. Tönnies W. Zur Operation der Meningeome der Siebbeinplatte. Zentralblatt für Neurochirurgie. 1938;1:1-7.

11. Hassler W., Zentner J. Pterional approach for surgical treatment of olfactory groove meningiomas. Neurosurgery. 1989;25:942-945.

12. Al-Mefty O. Surgical technique for the juxtasellar area. In: Al-Mefty O., editor. Surgery of the Cranial Base (Foundations of Neurological Surgery, 2 ed.). Boston: Kluwer Academic Publishers; 2010:73-89.

13. Nakamura M., Struck M., Roser F., et al. Olfactory groove meningiomas: clinical outcome and recurrence rates after tumor removal through the frontolateral and bifrontal approach. Neurosurgery. 2007;60:844-852.

14. Ransohoff J., Nockels R.P. Olfactory groove and planum meningiomas. In: Apuzzo M.L.J., editor. Brain Surgery Complication Avoidance and Management. New York: Churchill Livingstone; 1993:203-219.

15. Ojemann R.G., Martuza R.L. Surgical management of olfactory groove meningiomas. In: Schmidek H.H., Roberts D.W. Operative neurosurgical techniques: indications, methods, and results. Philadelphia: WB Saunders Company; 2006:207.

16. Mayfrank L., Gilsbach J.M. Interhemispheric approach for microsurgical removal of olfactory groove meningiomas. Br J Neurosurg. 1996;10:541-545.

17. Paterniti S., Fiore P., Levita A., et al. Basal meningiomas. A retrospective study of 139 surgical cases. J Neurosurg Sci. 1999;43:107-113.

18. Tsikoudas A., Martin-Hirsch D.P. Olfactory groove meningiomas. Clin Otolaryngol Allied Sci. 1999;24:507-509.

19. Turazzi S., Cristofori L., Gambin R., et al. The pterional approach for the microsurgical removal of olfactory groove meningiomas. Neurosurgery. 1999;45:821-825.

20. Zevgaridis D., Medele R.J., Muller A., et al. Meningiomas of the sellar region presenting with visual impairment: impact of various prognostic factors on surgical outcome in 62 patients. Acta Neurochir (Wien). 2001;143:471-476.

21. Hentschel S.J., DeMonte F. Olfactory groove meningiomas. Neurosurg Focus. 2003;14:e4.

22. Romani R., Lehecka M., Gaal E., et al. Lateral supraorbital approach applied to olfactory groove meningiomas: experience with 66 consecutive patients. Neurosurgery. 2009;65:39-52.