Olfactory Groove Meningiomas

Keywords: olfactory groove meningioma, anterior skull base meningioma, surgical approaches, endoscopic endonasal approach, endoscopic skull base surgery, outcomes, complications, recurrence

Daniel M. Prevedello, Alaa S. Montaser, Matias Gómez G., Bradley A. Otto, Ricardo L. Carrau

11.1 Introduction

Meningiomas are benign slow-growing tumors that account for approximately 20% of primary intracranial tumors, however, OGMs account for 8 to 13% of intracranial meningiomas. The first OGM was described in Cruveilhier’s Traite d’Anatomie in 1835, while the first successful resection of an OGM was performed in 1885 by Francesco Durante. ^{1,​ 2,​ 3,​ 4}

OGMs are unique tumors with special characteristics differentiating them from other brain lesions, including clinical presentation, neurological findings, surgery planning, outcomes, and complications. ¹ OGMs are generally classified according to their size (maximum diameter) into small (<2 cm), medium (2–4 cm), large (4–6 cm), and giant (>6 cm). Giant OGMs are especially problematic and represent a surgical challenge owing to the possible postoperative morbidity and parenchymal damage. ⁵

11.2 Preoperative Definition of the Lesion Features

11.2.1 Anatomical Consideration

The understanding of growth pattern and relationship with the surrounding critical neurovascular structures is very crucial for a successful surgical resection of OGMs. OGMs arise in the midline from the meningothelial cap cells at the region of the cribriform plate and the frontosphenoid suture and may extend from the crista galli to the planum sphenoidale, involving the whole anterior skull base. Although OGMs originate in the midline, they often have a tendency to extend unilaterally. ^{1,​ 3,​ 6,​ 7}

The site of origin may be uncertain when they are large and extend back to the sella turcica, therefore, posteriorly extending OGMs and tuberculum sellae meningiomas pose some similarities. They can be differentiated mainly by the location of the optic apparatus in relationship to the tumor. As OGMs grow, they displace the chiasm and optic nerves downward and posteriorly. On the contrary, because tuberculum sellae meningiomas occupy a subchiasmal position, they tend to elevate the chiasm and pushes the optic nerve superolaterally. ^{1,​ 7,​ 8}

In large and giant OGMs, the olfactory tracts are likely invaded and/or destroyed on both sides, thus, preservation of olfaction may be impossible. However, in smaller lesions, the olfactory tracts are laterally displaced over the orbital roofs and there is often a good chance to preserve both or at least one of the olfactory tracts. ^{7,​ 8} However, anatomical preservation of olfactory nerves doesn’t imply functional preservation of olfaction. Loss of smell after anatomic preservation of the olfactory tracts could be related to direct manipulation or ischemia.

OGMs usually produce hyperostosis of the anterior skull base (28.3–62% of cases) that is thought to be due to microinvasion by the tumor rather than an inflammatory reaction to it, therefore, incomplete resection of unrecognized bony invasion is associated with high rates of tumor recurrence. However, these neoplasms may also erode the skull base bone and extend into the nasal cavity, paranasal sinuses, and orbits. ^{1,​ 2,​ 9,​ 10}

OGMs, like all other anterior skull base meningiomas, are usually highly vascular and their resection may be complicated with significant bleeding. The vascularity of OGMs is derived from pial, dural, transosseous supply. Although the anterior and posterior ethmoidal arteries constitute the main arterial supply for OGMs, these tumors can also receive collaterals from several arteries such as anterior branches of the middle meningeal artery, meningeal branches of the ophthalmic artery and internal carotid artery (ICA), small branches of the anterior communicating artery (ACoA), and the distal maxillary artery. Encasement of critical vascular structures is not uncommon. The most common artery to be encased is the A2 segment of anterior cerebral artery (ACA) and its smaller branches such as the frontopolar or medial orbitofrontal artery, and ACoA. ^{1,​ 8,​ 11,​ 12,​ 13}

11.2.2 Clinical Presentation and Workup

Due to the slow growth nature of OGMs and their location, the clinical diagnosis is usually delayed. Thus, most of OGMs are diagnosed when they have attained larger size. In some series, 50 to 60% of the OGMs were larger than 6 cm in diameter at the time of surgery. ^{1,​ 8}

It is important from clinical and surgical perspectives to differentiate OGMs from planum sphenoidale and tuberculum sellae meningiomas. Typically, the latter presents at an early stage (smaller size) with visual deficits, while OGMs are usually clinically silent in the early stage and visual deterioration is often a late presentation. Additionally, OGMs frequently extend into the paranasal sinuses and the nasal cavity, which is a rare feature of meningiomas arising at the planum sphenoidale or tuberculum sellae. ⁴

The most frequently encountered symptoms are frontal lobe manifestations (such as personality changes, psychiatric symptoms, concentration difficulties, and apathy), headache, alteration of olfaction (hypo- or anosmia, often noted in retrospect by many patients), and finally visual disturbance (visual acuity and/or field changes). Typically, onset of these symptoms is very gradual that they are underestimated or may not be noted early in their course. ^{1,​ 3,​ 13,​ 14} Vision loss is usually only noted when these tumors achieve a very large size (large and giants).

Other common presenting symptoms are seizures, mental status changes, and incontinence. Although originally described in OGMs, Foster-Kennedy syndrome (unilateral optic atrophy with contralateral papilledema) occurs only in small number of cases. ^{7,​ 8,​ 15}

In general, the diagnosis is mainly made based on radiographic imaging. MRI is the imaging modality of choice for all meningiomas, including OGMs. CT is particularly important for assessment of skull base bony anatomy, including areas of hyperostosis and erosions that helps in diagnosis and preoperative planning of surgical strategy as well.

The appearance of OGMs in MRI and CT is similar to meningiomas located elsewhere. On MRI, OGMs are typically iso- to hypointense on T1-weighted imaging (T1WI) and iso- to hyperintense on T2-weighted imaging (T2WI). They typically show avid homogeneous gadolinium enhancement. Most meningiomas show the characteristic “dural tail”, a marginal dural thickening that tapers peripherally. MRI and magnetic resonance angiography (MRA) are helpful in defining the relationship of the tumor to the surrounding vascular structures such as ACA and ACoA. These are critical for surgical planning as vascular encasement may require a specific strategy.

On CT, OGMs appear as well-defined extra-axial lesions abutting the dura and displacing the normal brain. They are iso- to hyperdense on noncontrasted CT, with intense homogenous enhancement after contrast administration. OGMs are smooth in contour, however, multilobulated lesions are not uncommon. Calcification is another common finding. Cyst formation, atypical pattern of necrosis, or hemorrhage can be found in approximately 15% of cases. ^{1,​ 8,​ 14}

A thorough preoperative evaluation of the radiographic imaging is crucial for planning the surgical strategy, as it provides important information about the tumor such as its size and extent, presence of pial invasion, vascular encasement, hyperostosis, extent of frontal lobes edema, and hemodynamic and metabolic characteristics of the tumor. ^{16,​ 17}

11.3 Surgical Indications

As a general rule, the definitive treatment of meningiomas, including OGMs, is surgical resection. However, observation may be an option in patients with small OGMs that are accidentally discovered, and in elderly patients with asymptomatic lesions or who cannot withstand the surgical intervention due to their comorbidities. ⁸ Radiation therapy is usually reserved for cases with recurrent and/or high grade (atypical or anaplastic) lesions. ^{2,​ 18}

11.3.1 Planning the Surgical Strategy

Planning the surgical strategy to attack these tumors while achieving the optimum outcome with minimal complications is challenging, especially when attempting to preserve the olfaction. ¹⁹ Since the old report of first successful surgery of an OGM performed by Durante via a left frontal craniotomy in 1885, skull base surgeons have been trying to determine a surgical approach that allows safe and complete resection of OGM. However, this is still a matter of controversy. ^{1,​ 4,​ 13,​ 15}

 Goals of Surgery

Indeed, a total gross resection of the tumor, its dural attachment, and the involved bone (Simpson grade I resection) is the utmost goal of surgical intervention for meningiomas. This goal applies also to OGMs and can be achieved in most cases, despite the large size of the tumor, since OGMs often have an arachnoid membrane separating the tumor from practically all critical neurovascular structures, thus facilitating a complete resection. ^{1,​ 8} Nevertheless, total gross resection may not be a possibility in many cases, especially if there is vascular encasement of the ACA, ACoA, and/or ICA. Nonetheless, the extent of resection varies widely depending on the patient and tumor characteristics.

Other fundamental goals of surgical intervention are the preservation of neurological function, avoidance of new neurological morbidities, avoidance of approach-related complications, and achieving good cosmetic outcome.

Having said that, the surgical team must determine the goal of surgery during preoperative planning, taking into consideration not only the tumor characteristics, such as the tumor size, extension in different planes, pial invasion, and vascular encasement, but also the patient characteristics such as the patient’s age, comorbidities, clinical manifestations, and functional outcomes as such as olfaction presence and preservation. ^{20,​ 21}

 Selecting the Surgical Approach

While considering the most suitable approach for each patient, it is important to consider the approach that:

1. 
   

   Provides a more direct and early access to the nourishing vessels of the tumor. The main advantage of early attacking the blood supply of the tumor is reduction of intraoperative bleeding by transforming a highly-vascularized tumor into an avascular mass, thus, shortening the operative time and reducing the surgical morbidity. ²²

   
   
2. 
   

   Achieves a wide exposure enough to allow gross total resection of the tumor, affected bone, and dura, leading to better outcomes and less possibilities of recurrence. It should provide convenient exposure of the anterior skull base permitting better reconstruction as well.

   
   
3. 
   

   Minimizes brain retraction and manipulation of critical neurovascular structures, thus, decreasing the surgical morbidities.

It is crucial to consider whether there is pial invasion and/or vascular encasement. It is also important to keep in mind that the frontal lobes (especially when there is pial invasion, massive edema, and/or venous engorgement) and the optic apparatus (especially when there is chronic compression and secondary ischemia), are more vulnerable in certain situations that even minimal manipulations can cause a functional compromise. ²³ Furthermore, the surgical team experienced and familiar with different approaches plays a key role in selecting the most suitable approach for each case.

11.3.2 Preoperative Embolization

Embolization techniques are performed in some centers prior to the surgery to promote devascularization, with or without bilateral ligation of anterior and posterior ethmoidal arteries. ¹¹ However, the rule of preoperative embolization for OGMs is controversial. ¹² In our opinion, preoperative embolization is not indicated in most cases as the blood supply is often directly encountered and disconnected earlier in the case.

While it is true that preoperative embolization of the ethmoidal arteries reduces intraoperative blood loss, surgery time, and the need for blood transfusion, it has some drawbacks. One of the major drawbacks is that it carries a very high risk of blindness due to the risk of retrograde migration of particles through the multiple anastomoses between the external and internal carotid arteries in this territory with high possibility of occlusion of the ophthalmic artery. Another disadvantage is the technical difficulty in gaining access to the ethmoidal arteries, which is sometimes not possible, because of the anatomical distortion caused by the tumor. ¹²

11.4 Surgical Techniques

Different approaches have been described to achieve the best outcome with the least complications possible for OGM resection. These include a subfrontal access, either through unilateral/bilateral frontal craniotomy or transbasal approach, an anterolateral access through frontolateral approach, a lateral access through pterional approach, and a ventral access through EEA. A brief description of the potential advantages and disadvantages of each approach follows.

11.4.1 Subfrontal Approach with Unilateral or Bilateral Frontal Craniotomy

The subfrontal approach through unilateral or bilateral frontal craniotomy has been advocated for OGM by many authors and is one of the most commonly used approaches for OGMs. This approach is more suitable for large and giant OGMs as it provides a short surgical corridor with a broad exposure of the tumor and its basal dural attachment. It provides a good view for closure and reconstruction of the skull base with a pericranial flap. It allows also for drilling the hyperostotic anterior skull base bone and decompressing the optic nerves by deroofing of the optic canals if necessary. ^{14,​ 19}

In many cases, especially in large and giant high-riding OGMs, orbital rim osteotomy can be added to unilateral or bilateral subfrontal approaches to gain extra basal access and minimize brain retraction. However, this is more time consuming and may increase the risk of complications, therefore, it should be only performed in selected cases. ^{7,​ 13,​ 24}

In small lesions, early devascularization of the tumor at the basal dural attachment can be achieved easily without significant brain retraction. However, in case of large and giant OGMs, which is more common, devascularization is very difficult unless a sizeable internal debulking of the tumor is achieved first, otherwise, the brain cannot be retracted or relaxed, especially when there is a considerable tumor-induced frontal lobe edema. ¹¹

Overexposure and significant retraction of the frontal lobes is one of the main drawbacks of this approach increasing the risk of frontal lobe contusions and edema with resultant cognitive and emotional impairment. Excessive brain retraction is mainly due to the increased intracranial pressure and the difficulty of releasing cerebrospinal fluid (CSF) early in the procedure. Additionally, there is increased risk of injury to the critical surrounding neurovascular structures such as the optic apparatus, ICA, ACA, and ACoA, because they are only visualized late during tumor dissection. Other disadvantages include ligation of the superior sagittal sinus and the inevitable opening of frontal sinus with the risk of CSF leak and meningitis. ^{1,​ 6,​ 19,​ 21,​ 25}

Compared to bifrontal craniotomy, a unilateral frontal craniotomy provides the advantage of avoiding contralateral frontal lobe retraction and superior sagittal sinus violation. It is more suitable for tumors with predominant unilateral extension. In addition to difficulty of decreasing the intracranial pressure by releasing CSF prior to tumor dissection, and late visualization of critical neurovascular structures, unilateral frontal craniotomy has the disadvantage of smaller working window and narrower surgical corridor. ^{1,​ 19}

11.4.2 Transbasal Approach

This approach is more suitable for tumors extending caudally into the paranasal sinuses and/or the orbits as it provides excellent access to the paranasal sinuses (frontal, ethmoidal, and sphenoidal) and the orbits as well.

Ligation of the anterior ethmoidal arteries can be achieved early during the procedure, which contributes to devascularization of the tumor to great extent. The transbasal approach offers a lower basal access with less brain retraction, thus permitting early devascularization of the tumor at its basal dural attachment as well, and providing an excellent exposure of the anterior skull base for drilling the infiltrated bone and for skull base repair with pericranial flap. ^{2,​ 6,​ 11}

The disadvantages of this approach include prolonged surgical time, risk of long-term cosmetic defects due to removal of fronto-orbital bars, and higher CSF leak rates due to the wide exposure of the cranial base. ^{2,​ 6,​ 26} Furthermore, it also allows the visualization of the optic nerves only later in the case, and it could potentially put them in risk for damage.

11.4.3 Pterional Approach

The pterional approach have been advocated only for resection of small and medium size OGMs with pure intracranial extension and without skull base involvement, however, some authors suggest its use even for giant OGMs. ⁵ In cases of large and giant high-riding OGMs, orbital rim osteotomy can be added to gain extra basal access and minimize brain retraction. ²⁴

Compared to the subfrontal approach, the pterional approach provides several advantages including lower rates of postoperative CSF leak due to preservation of the frontal sinus, less brain retraction due to brain relaxation following CSF release by opening the basal cisterns prior to tumor manipulation, preservation of venous drainage of the frontal lobes leading to less congestion and edema, early identification and protection of the neurovascular structures, and potential sparing of the olfaction on the contralateral side. ⁵

One of the major drawbacks of utilizing the pterional approach in large and giant OGMs is that there may be blind areas on the contralateral side especially when the tumor has a significant superior extension requiring more retraction of the brain and/or falx to achieve a good control and resection, or in cases in which the planes of the orbital roofs and the ethmoid are different along the vertical axis. ^{1,​ 5,​ 6}

11.4.4 Frontolateral Approach

This approach combines the advantage of subfrontal and pterional approaches. It provides a wide angle of exposure to the tumor with the possibility of attacking the basal dural blood supply of the tumor early in the procedure (as in subfrontal approach), and it allows for early identification of the optic nerve and the ICA, avoidance of ligation of the superior sagittal sinus, and early brain relaxation by opening the basal cisterns and releasing CSF (as in pterional approach). ^{24,​ 27} Olfaction could be preserved by anatomic preservation of the contralateral olfactory nerve.

The disadvantages of this approach include longer operative time, and the higher possibility of CSF leak due to opening of the frontal sinus. Total gross resection may be limited through frontolateral approach in cases of large and giant OGMs encasing the ACA. ²⁷ Another downside of this approach is related to brain herniation through the craniotomy in very large and giant OGM with substantial brain edema. Contralateral hyperostosis can be difficult to drill and contralateral reconstruction can be challenging.

11.4.5 Supraorbital Keyhole Approach

The supraorbital keyhole craniotomy is a minimally invasive approach that provides access to a wide range of disease processes along the anterior skull base, including OGMs. Typically, an eyebrow incision is often used and the bone flap required is 3 × 2 cm.

This approach allows direct visualization of the lesion and the surrounding critical neurovascular structures. Compared to the subfrontal and pterional approaches, the supraorbital key hole approach necessitates much less brain retraction and avoids the need of splitting the Sylvian fissure. It offers the advantages of a minimally invasive surgery such as less operative time and improved postoperative pain. It also provides an excellent cosmetic outcome.

Additionally, the application of endoscopy through this approach allows for enhanced illumination and improved visualization, especially of hidden areas around the anatomic corners of the surgical field that were not adequately visualized by the microscope.

The main drawbacks of the supraorbital keyhole approach are the limited maneuverability of instruments, the possibility of violating the frontal sinus during performing the craniotomy (especially if the frontal sinus is large and well-pneumatized), and the risk of damage to the frontotemporal branch of the facial nerve. It is very difficult to expose the basal dural attachment of the tumor at the midline if the ethmoid and the orbital roofs lies in different planes which should be kept in mind while preoperatively planning the surgical strategy. ^{26,​ 28} The visualization of the olfactory groove can be compensated by the utilization of endoscopes, but it definitely increases the complexity of these cases.

11.4.6 Endoscopic Endonasal Approach

During the last two decades the extended EEAs to the ventral skull base have been advanced to great extent. Nowadays, EEA is considered one of the safe alternatives on the armamentarium of surgery to anterior skull base lesions, including OGMs.

EEA is an excellent option when the tumor is extending into the paranasal sinuses and/or the orbits. EEA is also more suitable in recurrent OGMs with paranasal sinuses extension especially when the first surgery was done through transcranial approach where the cribriform plate was not adequately drilled out and the pericranial flap has been used for previous skull base reconstruction.

It is to be emphasized that when approaching OGMs via EEA, the same microneurosurgical techniques and principles are applied during the procedure, such as internal debulking followed by capsule mobilization, extracapsular dissection of neurovascular structures, focal coagulation, and capsule removal. ^{21,​ 23}

In case of OGM, the main advantage of EEA is that it provides a wide ventral corridor with the most direct access to the anterior skull base, specifically the cribriform plate and planum sphenoidale, allowing early vascular control of the anterior and posterior ethmoidal arteries. Once the ethmoidal arteries are coagulated and cut, the tumor is significantly devascularized. ²³ Additionally, EEA allows for better drilling of the hyperostotic bone and complete resection of the dural attachment of the lesion, which are integral parts of the approach, leading to more complete (Simpson grade I) resection and lower rates of tumor recurrence. Furthermore, complete decompression of chronically compressed optic nerves without manipulating them and without damaging the perforating vessels to the chiasm are feasible through EEA leading to improved visual outcomes ^{1,​ 11,​ 28,​ 29}.

Other advantages of EEA include better visualization with near field magnification, avoidance of brain retraction, and minimal manipulation of the critical neurovascular structures, Therefore, EEA is associated with less morbidities and improved outcomes. Being minimally invasive surgery, EEA also carries the advantages of shorter hospital stay, less postoperative pain, and better cosmosis. ²

The main drawback of EEA is the higher risk of postoperative CSF leak, ^{1,​ 29} however, with the recent innovations in techniques used for skull base repair, including the vascularized nasoseptal flaps, the postoperative CSF leak rates have markedly decreased in experienced centers at rates between 5 and 10%. ^{28,​ 30}

In our opinion, the major limitations of EEA for OGMs include the inevitable risk of anosmia, especially in patients with some preoperative preserved olfaction, the risk of cerebrovascular accidents and/or hemorrhage in case of vascular encasement, and limited resection in cases of lateral extension of the lesion and/or its basal dural attachment beyond the medial orbital walls bilaterally.

Nevertheless, surgical experience, a multidisciplinary approach, adequate instruments and equipment, appropriate patient selection, and thorough preoperative planning are mandatory for achieving best results with these approaches.

11.4.7 Algorithm for Surgical Management of Olfactory Groove Meningiomas (Endoscopic Endonasal Approaches vs. Craniotomy vs. Two-stages Strategy)

Since there is no consensus regarding the best approach to resect OGMs, the authors have developed an algorithm for surgical management of OGMs (▶ Fig. 11.1). This algorithm is based on thorough preoperative evaluation of the tumor and patient characteristics as mentioned before (see subsection Planning the surgical strategy).

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Introduction Petroclival Meningiomas Foramen Magnum Meningioma Cerebellopontine Angle Meningiomas Instrumentation (Micro, Endo, IGS, MRI Application) Cavernous Sinus Meningiomas

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