Get Permission Mishra, Chand, Singh, Gupta, and Singh: A comparative evaluation of microsurgical excision of olfactory groove meningioma through unilateral (pterional) vs Bilateral (Bifrontal-transbasal) approach


Introduction

Olfactory groove meningiomas (OGMs) constitute 4-13% of all intracranial meningiomas, originating from the dura of the anterior cranial fossa over the cribriform plate and frontosphenoidal suture.1, 2, 3, 4, 5 Typically, OGMs manifest with hypo/anosmia, visual deterioration, mental changes, and headaches due to compression of the olfactory or optic nerve and frontal lobe. Seizures are also prevalent in these patients. 6, 7 Despite their slow growth, OGMs often remain clinically silent in their early stages, resulting in substantial tumor sizes at the time of diagnosis. 6, 7, 8, 9

Distinguishing OGMs from other midline meningiomas in the anterior cranial fossa, such as those in the planum sphenoidale and tuberculum sellae, is not merely an anatomical exercise but holds clinical significance. Meningiomas in these locations are commonly diagnosed earlier due to visual impairment.

The classical bifrontal craniotomy proves inadequate for safe exposure of large OGMs, evident from the incidence of life-threatening complications related to brain retraction. 1, 4, 5 Alternative surgical routes, including the pterional and subfrontal approaches, 1, 10, 11, 12, 13, 14, 15 expose the posterolateral surface of the tumor from a lateral view. The fronto-basal-orbital approach 5, 16 accesses the tumor from underneath, exposing its dural attachment first.

In our retrospective analysis of 30 OGM cases, we assessed clinical presentation, tumor characteristics, surgical approaches, and follow-up results following microsurgical intervention through a unilateral (pterional/subfrontal) or bilateral (bifrontal) craniotomy.

Materials and Methods

We scrutinized the records of patients treated for olfactory groove meningioma at our department (RMLIMS, Lucknow) through unilateral and bilateral approaches. A total of 30 patients who underwent OGM removal were reviewed, and their clinical data, radiological findings, and surgical outcomes were retrospectively analyzed.

We identified 30 patients with olfactory groove meningioma (18 females and 12 males), aged between 33 and 54 years, with a mean age of 41.4 years in the unilateral group and 40.4 years in the bilateral group. The preoperative median Karnofsky Performance Score (KPS) was 100 (range, 60-100). Headache was the most frequent complaint (40%), followed by visual impairment (26.6%), anosmia/hyposmia (16.6%), and mental changes (6.6%). In 2 patients (6.6%), OGMs were associated with seizures (Table 1). Tumor diagnosis was based on magnetic resonance imaging (MRI) and/or computed tomography (CT) with a contrast agent, with two patients undergoing cerebral digital subtraction angiography (DSA) for embolization purposes. A total of 16 surgical procedures were conducted, utilizing both the pterional (n=16, 53.3%) and bifrontal (n=14, 46.6%) approaches. The pterional approach closely adhered to the technique originally described by Yaşargil. In this method, the frontal bone's lateral part, the anterior segment of the squamous part of the temporal bone, and the lateral aspect of the greater wing of the sphenoid bone were mobilized and excised. To facilitate improved access and manipulation of the anterior fossa from a broader perspective, the frontal part of the bone flap was extended medially and inferiorly. Figure 1 illustrates the intraoperative steps following dural opening for this approach.

Table 1

Demographic data

No. of Cases

Female/ Male

Anosmia

Headache

Decreased visual activity

Hemiparesis

Personality changes

Seizure

30

18/12

5

12

8

1

2

2

Figure 1

After unilateral craniotomy,A: the dura is opened; B: The tumor (asterisk) and right olfactory nerve (pointed arrow) are seen; C: After devascularization and incision from the frontobasal dura; D: Tumor excision begins; E: When we reach the falx (arrowhead), it is incised and F: The contralateral tumor is excised; G: The basal dura is cauterized; H: and the right optic nerve is seen (black arrow).

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The bifrontal approach, closely mirrors the technique delineated by El Gindi. After a bicoronal scalp incision and periosteum dissection, a bifrontal bone flap was lowered to the orbital rim. The frontal sinus was opened, and its posterior wall and mucosa were excised, with subsequent closure of the frontonasal duct using muscle. Bilateral dural openings were performed, and tumor resection predominantly occurred from one side, with careful retraction of the non-dominant frontal lobe. The dominant frontal lobe's retraction was minimized as much as possible. In summary, a bifrontal craniotomy was executed after the release of supraorbital nerves. Subsequently, a bilateral orbitotomy was conducted, encompassing 2–2.5 cm of orbital roof crossing the midline just anterior to the crista galli. Post-procedure, the anterior skull base underwent reconstruction using a pedunculated flap of galea and abdominal fat to fill any residual dead space. (Figure 2).

Figure 2

After bilateralFrontal craniotomy reaching the subfrontal area, the dura is opened (A)&(B), devascularization and excision of the tumor after release of olfactory nerve(C)i. (D) After excision and cauterization of tumor bed.

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Statistical analysis

Data analysis was conducted using the statistical software package SPSS 21.0 for Windows (SPSS Inc., Chicago, IL). Categorical variables were compared using Pearson’s chi-squared test and Fisher exact test. A significance level of P<0.05 was considered statistically significant.

Results

A total of 30 patients diagnosed with olfactory groove meningioma were included in the study, comprising 18 females and 12 males. The age distribution ranged from 33 to 54 years, with a mean age of 41.4 years in the unilateral group and 40.4 years in the bilateral group.

In our series, total removal was achieved in 27 patients, while partial removal occurred in three patients. Of the 30 OGMs, 16 (53.3%) were treated with the pterional -subfrontal approach, and 14 (46.6%) with the bifrontal transbasal approach. The pterional approach was significantly more frequent for small and medium-sized OGMs (p <0.05).

Overall, gross total resection (GTR) was achieved in 27 procedures (90%), with 10% classified as subtotal resection (STR). The pterional approach allowed a significantly greater percentage of GTR than the bifrontal approach (p<0.05). Simpson’s grade I-II resection was achieved in 27 procedures (90%), with the pterional approach showing a significantly higher percentage of Simpson I-II removal compared to the bifrontal approach.

Postoperative cerebral edema occurred in 12 patients, with a rate of 25% in patients with a unilateral approach and 57.14% in patients with a bilateral approach. The mean surgical length was 2 hours for the unilateral approach and 3 hours for the bilateral approach.

Surgical approach and complications

Postoperative complications were observed in 7 out of 30 operations (23.3%). Complications were seen in 2 (12.5%) and 5 (35.7%) patients operated via the pterional and unifrontal approach, respectively. Edema and hematoma with contusion were the most frequent complications. Overall, reoperation for complications was required in 1 case (3.3%).

Contusions observed in 3 patients were treated with medical intervention. Cerebrospinal fluid (CSF) leak was observed in one patient operated via the frontal route and was successfully treated with lumbar drainage. One patient experienced intracranial hematoma, requiring surgical evacuation.(Table 2, Table 3)

Table 2

Comparison of Surgical Outcomes

Unilateral

Bilateral

Degree of removal

Total removal

15

12

Partial removal

1

2

Post-operative edema

4

8

Length of stay

5

7

Surgical length

2

3

Table 3

Preoperative symptomatology compared to postoperative resolution in our series

Symptoms

Preoperative signs and symptoms (number of cases)

Postoperative resolution of signs and symptoms (number of cases still with symptoms)

Olfactory deficits

10

7

Headache

8

2

Seizure

5

0

Visual deficits

4

2

Behavioral problems

2

1

Hemiparesis   

1

0

Histological grading of tumors

According to the World Health Organization (WHO) classification, 28 tumors (93.3%) were Grade 1, and 2 (6.6%) were Grade 2. One of the Grade 2 meningiomas was associated with recurrence.(Table 4)

Table 4

Resection level in our series Olfactory groove meningioma

Resection level (Simpson grade)

Unilateral (%)

Bilateral(%)

Grade 1

15(93.7)

12( 85.7 )

Grade 2

Grade 3

1

2(0.14 )

Grade 4

(0.06 )

Grade 5

0

0

Treatment outcomes

In the median 60-month follow-up period, the overall tumor control rate was 96.8%. Recurrence and re-growth rates were 1.6% each, with a median follow-up to recurrence/re-growth of 31 months. Longer recurrence-free survival (RFS) was associated with GTR and WHO Grade 1 (p<0.05), while other factors showed no prognostic value on RFS, including age, sex, preoperative Karnofsky Performance Score, tumor size, type of approach, presence of ethmoidal invasion, optic canal involvement, vascular encasement, and hyperostosis.(Table 5)

Table 5

Postoperative complications and outcomes

Complications

Unilateral

Bilateral

CSF leak

0

1

Wound infection

0

0

Postoperative edema

1

2

Death

0

0

Hydrocephalus

0

0

Postoperative hemorrhage

1

2

Visual loss

0

0

Infarction

0

0

Seizures

0

0

Discussion

Francesco Durante successfully performed the first Olfactory Groove Meningioma (OGM) resection in 1885 through a left frontal craniotomy. 17 In 1938, Cushing and Eisenhardt outlined OGM resection principles in a series of 22 patients, using a unilateral subfrontal approach. 18, 19 Despite numerous publications on OGM treatment, the optimal surgical approach remains controversial. Pterional, frontal, bifrontal, and their variations are the most reported open transcranial procedures for OGMs. 1, 2, 3, 4, 5, 13, 15, 18, 20, 21, 22, 23, 24, 25, 26, 27, 28

Nevertheless, the extensive dataset and long follow-up of OGM cases facilitate comparison of results with various surgical strategies. Key findings include: 1) higher mortality and severe complications with the bifrontal approach; 2) the pterional approach achieving a significantly greater percentage of Simpson I-II removal compared to bifrontal; 3) no retraction-related brain swelling in pterional cases, although postoperative CSF leak probability was higher with the bifrontal approach. Simpson grade I-II and WHO grade I were significant prognosticators for longer overall survival, with age and WHO grade being independent factors.

The pterional approach, introduced by Yaşargil, is widely used for vascular and neoplastic lesions in the anterior and middle cranial fossa. 29 Its advantages include early control of neurovascular structures, minimal damage to frontal lobes and olfactory nerves, and avoidance of frontal sinus transection, reducing the risk of CSF leak. 11, 13, 22, 30 However, it has a narrow working angle. The unifrontal approach, described by Olivecrona and Urban, spares the contralateral frontal lobe and superior sagittal sinus, avoiding bifrontal retraction and potential cognitive dysfunction. 5, 26 However, it has drawbacks like late exposure of distant neurovascular structures and the risk of CSF leak from frontal sinuses. 5, 22, 31

The ongoing debate on surgical strategy focuses on tumor resection extent and safety. Our study showed a GTR rate of 90%, with no significant difference between pterional (93.75%) and bifrontal (85.7%) approaches. Optic canal involvement was associated with tumor diameter, while vascular encasement occurred in 8.2% of cases. Postoperative complications varied, with life-threatening complications more frequent in bifrontal cases. No mortality was observed in our series.32, 33, 34, 35, 36, 37, 38, 39

The most critical factor in preventing recurrence was the extent of initial resection, supported by a median follow-up of 60 months. Paranasal sinus infiltration increased recurrence risk, especially when involved bone was not removed.

Conclusion

In conclusion, our extensive series highlights the higher risk associated with the bifrontal approach and identifies age and WHO grade as independent factors affecting overall survival in OGM patients. While Simpson grade I-II's prognostic power may be influenced by other variables, it should continue to be the standard for OGM care.

Source of Funding

None.

Conflict of Interest

None.

References

1 

H Bassiouni S Asgari D Stolke Olfactory groove meningiomas: Functional outcome in a series treated microsurgicallyActa Neurochir (Wien)2006149210921

2 

AV Ciurea SM Iencean RE Rizea FM Brehar Olfactory groove meningiomas: a retrospective study on 59 surgical casesNeurosurg Rev2012352195202

3 

BO Colli CG Carlotti JA Assirati MBM Santos L Neder AC Santos Olfactory groove meningiomas: surgical technique and follow-up reviewArq Neuropsiquiatr2007653B7959

4 

M Nakamura M Struck F Roser P Vorkapic M Samii Olfactory groove meningiomas: Clinical outcome and recurrence rates after tumor removal through the frontolateral and bifrontal approachNeurosurgery200760584452

5 

S Spektor J Valarezo DM Fliss Z Gil J Cohen J Goldman Olfactory groove meningiomas from neurosurgical and ear, nose, and throat perspectives: Approaches, techniques, and outcomesNeurosurger2005574 Suppl26880

6 

AD Bitter LC Stavrinou G Ntoulias AK Petridis M Dukagjin M Scholz The Role of the Pterional Approach in the Surgical Treatment of Olfactory Groove Meningiomas: A 20-year ExperienceJ Neurol Surg B Skull Base201374297102

7 

R Romani M Lehecka E Gaal S Toninelli O Celik M Niemela Lateral supraorbital approach applied to olfactory groove meningiomas: Experience with 66 consecutive patientsNeurosurgery20096513952

8 

A Welge-Luessen A Temmel C Quint B Moll S Wolf T Hummel Olfactory function in patients with olfactory groove meningiomaJ Neurol Neurosurg Psychiatry200170221821

9 

S El Gindi Olfactory groove meningioma: surgical techniques and pitfallsSurg Neurol20005464157

10 

G Rubin UB David M Gornish ZH Rappaport Meningiomas of the anterior cranial fossa floor. Review of 67 casesActa Neurochir (Wien)19941291-22630

11 

S Paterniti P Fiore A Levita A La Camera S Cambria Basal meningiomas. A retrospective study of 139 surgical casesJ Neurosurg Sci199943210713

12 

R Romani M Lehecka E Gaal S Toninelli O Celik M Niemela Lateral supraorbital approach applied to olfactory groove meningiomas: experience with 66 consecutive patientsNeurosurgery20096513952

13 

C Schaller V Rohde W Hassler Microsurgical removal of olfactory groove meningiomas via the pterional approachSkull Base Surg19944418992

14 

F Tomasello FF Angileri G Grasso F Granata FS De Ponte C Alafaci Giant olfactory groove meningiomas: extent of frontal lobes damage and long-term outcome after the pterional approachWorld Neurosurg2011763-43117

15 

S Turazzi L Cristofori R Gambin A Bricolo The pterional approach for the microsurgical removal of olfactory groove meningiomasNeurosurgery19994548215

16 

SJ Hentschel F Demonte Olfactory groove meningiomasNeurosurg Focus2003146e4

17 

F Estirpazione Durante Estirpazione di un tumore endocranicoArch Atti Soc Ital Chir188622525

18 

H Cushing L Eisenhardt The olfactory meningiomas with primary anosmia, in Meningiomas: Their Classification, Regional Behavior, Life History and Surgical End ResultsSpringfield IL: Charles C. Thomas193825082

19 

PHP de Aguiar A Tahara AN Almeida R Simm AN Silva MVC Maldaun Olfactory groove meningiomas: approaches and complicationsJ Clin Neurosci2009169116873

20 

JR De Almeida F Carvalho F Vaz Guimaraes Filho T R Kiehl M Koutourousiou S Su Comparison of endoscopic endonasal and bifrontal craniotomy approaches for olfactory groove meningiomas: A matched pair analysis of outcomes and frontal lobe changes on MRIJ Clin Neurosci20152211173341

21 

K El-Bahy Validity of the frontolateral approach as a minimally invasive corridor for olfactory groove meningiomasActa Neurochir (Wien)2009151101197205

22 

W Hassler J Zentner Pterional approach for surgical treatment of olfactory groove meningiomasNeurosurgery19892569425

23 

D Mielke L Mayfrank M N Psychogios V Rohde The anterior interhemispheric approach: a safe and effective approach to anterior skull base lesionsActa Neurochir (Wien)2014156468996

24 

HY Park HJ Seol DH Nam JI Lee DS Kong JH Kim Treatment outcomes after surgical resection of midline anterior skull base meningiomas at a single centerJ Clin Neurosci2012191216548

25 

S Telera CM Carapella F Caroli F Crispo G Cristalli L Raus Supraorbital keyhole approach for removal of midline anterior cranial fossa meningiomas: A series of 20 consecutive casesNeurosurg Rev20123516783

26 

H Tuna M Bozkurt M Ayten A Erdogan H Deda Olfactory groove meningiomasJ Clin Neurosci20051266648

27 

LA Zimmer PV Theodosopoulos Anterior skull base surgery: open versus endoscopicCurr Opin Otolaryngol Head Neck Surg2009172758

28 

LG Kempe GD Vanderark Anterior communicating artery aneurysms. Gyrus rectus approachNeurochirurgia (Stuttg)19711426370

29 

MG Yaşargil General Operative Techniques, in Microneurosurgery4Thieme-StrattonNew York198420833

30 

H Olivecrona H Urban Über Meningeome der SiebbeinplatteBrun’s Beitr Klin Chir 193516122453

31 

O Al-Mefty LN Sekhar IP Janecka Tuberculum sella and olfactory groove meningiomasSurgery of Cranial Base TumorsRaven PressNew York199350719

32 

R Babu A Barton SS Kasoff Resection of olfactory groove meningiomas: Technical note revisitedSurg Neurol199544656772

33 

F Obeid O Al-Mefty Recurrence of olfactory groove meningiomasNeurosurgery200353353442

34 

R Gazzeri M Galarza G Gazzeri Giant olfactory groove meningioma: Ophthalmological and cognitive outcome after bifrontal microsurgical approachActa Neurochir (Wien)200815011111725

35 

D Avella F M Salpietro C Alafaci F Tomasello Giant olfactory meningiomas: the pterional approach and its relevance for minimizing surgical morbiditySkull Base Surg1999912331

36 

AB Adegbite MI Khan KW Paine LK Tan The recurrence of intracranial meningiomas after surgical treatmentJ Neurosurg1983581516

37 

O Al-Mefty A Holoubi A Rifai JL Fox Microsurgical removal of suprasellar meningiomasNeurosurgery198516336472

38 

PM Black MeningiomasNeurosurgery199332464357

39 

PJ Derome G Guiot Bone problems in meningiomas invading the base of the skullClin Neurosurg1978254355110.1093/neurosurgery/25.cn_suppl_1.435



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Article History

Received : 16-10-2023

Accepted : 25-11-2023


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https://doi.org/10.18231/j.ijn.2023.040


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