Clinical Neurology and Neurosurgery 115 (2013) 12881292

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Clinical Neurology and Neurosurgery

journal homepage: www.elsevier.com/locate/clineuro

Preservation of olfaction in surgery of olfactory groove meningiomas

Woo-Youl Jang, Shin Jung , Tae-Young Jung, Kyung-Sub Moon, In-Young Kim
Department of Neurosurgery, Chonnam National University Research Institute of Medical Sciences, Chonnam National University Hwasun Hospital and Medical School, Gwangju,
South Korea

a r t i c l e

i n f o

Article history:
Received 13 August 2012
Received in revised form
10 November 2012
Accepted 2 December 2012
Available online 10 January 2013
Keywords:
Olfaction
Olfactory groove meningiomas
Surgical approach

a b s t r a c t
Introduction: Olfaction is commonly considered as secondary among the sensory functions, perhaps
reecting a lack of interest in sparing olfaction after surgery for the olfactory groove meningiomas
(OGM). However, considering the repercussions of olfaction for the quality of life, the assessment of postoperative olfaction should be necessary. We retrospectively reviewed the olfactory outcome in patients
with OGM and investigated the factors associated with sparing the post-operative olfaction.
Methods: Between 1993 and 2012, 40 patients with OGM underwent surgical resection and estimated
the olfactory function using the Korean version of SnifnSticks test (KVSS). Variable factors, such as
tumor size, degree of preoperative edema, tumor consistency, preoperative olfactory function, surgical approaches, patients age, and gender were analyzed with attention to the post-operative olfactory
function.
Results: Anatomical and functional preservation of olfactory structures were achieved in 26 patients (65%)
and 22 patients (55%), respectively. Among the variable factors, size of tumor was signicant related to
the preservation of post-operative olfaction. (78.6% in size <4 cm and 42.3% in size >4 cm, p = 0.035).
Sparing the olfaction was signicantly better in patients without preoperative olfactory dysfunction
(84.6%) compared with ones with preoperative olfactory dysfunction (40.7%, p = 0.016). The frontolateral
approach achieved much more excellent post-operative olfactory function (71.4%) than the bifrontal
approach (36.8%, p = 0.032).
Conclusions: If the tumor was smaller than 4 cm and the patients did not present olfactory dysfunction preoperatively, the possibility of sparing the post-operative olfaction was high. Among the variable surgical
approaches, frontolateral route may be preferable sparing the post-operative olfaction.
2012 Elsevier B.V. All rights reserved.

1. Introduction
Olfactory groove meningiomas (OGMs) originate from the dura
over the cribriform plate and usually grow slowly [15]. Therefore,
when the patient is diagnosed with a OGM, the size of tumor is
frequently large [2,68]. Because of the anatomical location and
large size of OGM, loss of olfaction after surgical resection has been
considered inevitable and the sparing of olfactory ability in surgery
of OGM has been overlooked [9]. However, the loss of olfaction can
cause the disability to smell food, consequently resulting in a lack
of interest in eating [10]. Preservation of olfactory function after
surgical resection of OGM is certainly important for the quality of
life and should be required more attention.

Corresponding author at: Department of Neurosurgery, Brain Tumor Clinic and

Gamma Knife Center, Chonnam National University Hwasun Hospital and Medical
School, 322 Seoyong-ro, Hwasun-eup, Hwasun-gun, Jeollanam-do 519-763, South
Korea. Tel.: +82 61 379 7666; fax: +82 61 379 7673.
E-mail address: sjung@chonnam.ac.kr (S. Jung).
0303-8467/$ see front matter 2012 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.clineuro.2012.12.004

In this study, we retrospectively analyzed the surgical outcome

of OGMs, especially focusing on the olfactory function and associated factors.
2. Patients and methods
Between January 1994 and March 2012, 40 patients with OGM
were treated initially by surgery in our institute. They accounted
for approximately 4.4% of 905 patients with primary intracranial
meningiomas who underwent surgical resection during the same
period.
All the patients were examined by computed tomography (CT)
and magnetic resonance imaging (MRI) before surgery. Based on
the maximum diameter measured from any single MRI plane, the
size of the tumor was calculated. Peritumoral edema was estimated
by using the criteria proposed by Gilbert et al. [11]. Tumor consistency was classied based on intra-operative ndings. According
to the operative assessment, the nature of the tumor was dened
as soft when the tumor could be aspirated with a suction tube or
ultrasonic aspiration apparatus and hard when the tumor could
not be aspirated, even with an ultrasonic aspiration apparatus.

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Table 1
Baseline characteristics according to surgical approach.
Variable

Frontolateral approach (n = 21)

Bifrontal approach (n = 19)

P-value

Sex (female)
Age (years)
Pre-operative olfaction (hyposmia/anosmia)
Tumor size (cm)
Peritumoral edema (moderate to severe)
Intraoperative consistency (soft)

10 (47.6%)
52.71 11.68
12 (57.1%)
4.29 1.57
12 (57.1%)
8 (38.1%)

7 (36.8%)
54.68 11.46
15 (78.96%)
4.86 1.67
16 (84.2%)
8 (42.1%)

0.538*
0.594
0.186*
0.275
0.089*
0.525*

Chi-square test.
Independent-sample t-test.

Tumor resection involved two major approaches: the bifrontal

approach and frontolateral approach. Frontolateral approach was
performed via ipsilateral access of the tumor-dominant or nostril with olfactory dysfunction. The extent of tumor removal was
based on intra-operative assessment and contrast-enhanced MRI
performed after surgery.
Olfactory function was estimated by using the Korean version
of SnifnSticks (KVSS) test, which is composed of perception
threshold test, odor discrimination test, and odor identication test
[2,12]. Scores of each scale ranged from 0 to 16, and total KVSS
scores ranged from 0 to 48. Anosmia was dened as total scores less
than 15 and sparing of olfactory function as the olfaction was preserved on at least one side. Preserved olfaction included normosmia
and also hyposmia, KVSS score is more than 16. Post-operative
examination of olfactory function was performed within 2 weeks
after surgery.
Statistical analyses were performed using the SPSS program
package. Fishers exact test was used to evaluate the correlation
between preservation of olfactory function and variable factors
such as tumor size, degree of preoperative edema, tumor consistency, histopathological grade, preoperative olfactory function,
surgical approaches, patient age, and sex. Independent-sample ttests and Chi-square tests were used for comparison of clinical
characteristics. A p value <0.05 was considered statistically signicant in each analysis.
3. Results
3.1. Clinical features and surgical outcome
Among the 40 patients with OGM, 17 (81.5%) were female and
23 (18.5%) male. Mean age was 51.9 years (range, 3374 years).
Visual impairment was the most common presenting symptom (12
patients, 30%) followed by headache (10 patients, 25%), deterioration of consciousness (seven patients, 17.5%), and disturbance of
olfaction (six patients, 15%). However, the neurological examination revealed that disturbance of olfaction was most common sign
(27 patients, 67.5%) followed by visual impairment (21 patients,
52.5%) The mean maximum tumor diameter was 4.59 cm (range,
1.88.0 cm). Twenty-eight patients showed moderate to severe
degree of peritumoral edema on pre-operative MRI. Gross total
resection, dened as Simpson grades I and II, was achieved in 37 of
the 40 patients (92.5%). Post-operative hemorrhage occurred in two
patients and cerebrospinal uid leak in two patients. Recurrences
were noted in three patients (7.5%), all of whom underwent repeat
surgery. Adjuvant radiotherapy was performed in two patients
because of remnant tumor and recurrent atypical meningioma,
respectively. The mean follow-up period for all patients was 58.3
months (range, 3184 months). Histopathological ndings showed
that seven meningiomas were WHO grade II, one was WHO grade
III, and the remaining 32 meningiomas were WHO grade I. Three
patients underwent subtotal tumor resection (Simpson grade III)
were diagnosed with WHO grade I meningiomas, histopathologically. Two patients (5%) suffered from visual deterioration after

surgery. Anatomical preservation of olfactory tract was achieved in

26 patients (65%). Among them, bilateral olfactory tracts were in
anatomical continuity in 19 patients and only one olfactory tract
in seven patients. Sparing of olfactory function was achieved in
22 patients (55%). Preoperative MRI demonstrated that symmetric
growth pattern was in 29 patients and asymmetric growth pattern
in 11 patients, respectively. Among the 11 patients with asymmetric growth pattern, ve had a preoperative olfactory dysfunction.
The side of tumor extension corresponded with nostril with olfactory dysfunction. Olfactory function of ipsilateral to the tumor was
sacriced but that of contralateral to the tumor was preserved in
all 5 cases, even improved in one cases. Preservation of both olfactory functions after surgery was achieved in all six patients without
preoperative olfactory dysfunction.
3.2. Prognostic factors associated with preserved olfaction after
surgery
Several variable factors were analyzed in relation to the postoperative olfactory function. Among the 13 patients without
preoperative disturbance of olfaction, 11 patients (84.6%) showed
preservation of olfactory function. By comparison, 11 of 27 patients
(40.7%) with preoperative disturbance of olfaction showed preservation of olfactory function. Therefore, a pre-operative olfaction
was signicantly associated with preservation of olfactory function
after surgery (p = 0.016). The chance of preserving olfaction after
surgery was signicantly increased in meningiomas smaller than
4 cm compared to ones larger than 4 cm (78.6% vs. 42.3%, respectively; p = 0.035). Among the 40 patients, a frontolateral approach
was undertaken in 21 patients and a bifrontal approach was undertaken in 19 patients. We retrospectively compared the baseline
characteristics between the two patient groups with respect to
the surgical approach (Table 1). There was no signicant difference between the two groups, including gender, age, pre-operative
olfactory status, tumor size, consistency, and peritumoral edema,
histopatholgical grade. The mean tumor size was 4.29 1.57 cm in
the frontolateral approach group compared with 4.86 1.67 cm in
the bifrontal approach group. Post-operatively, olfaction was preserved in 15 patients (71.4%) in the frontolateral approach group.
But, post-operatively, olfaction was preserved in seven patients
(36.8%) in bifrontal approach group (p = 0.032). The variable factors related to preserving post-operative olfaction are summarized
in Table 2.
3.3. Illustrative case
A 73-year-old woman presented with anosmia. Pre-operative
KVSS score was 9 in the right nose and 14 in the left nose. The
MR images demonstrated that bilateral extended huge tumor with
homogeneous enhancement in the olfactory groove (Fig. 1a and
b). The tumor was resected via a right frontolateral approach.
Based on the intra-operative ndings, the meningioma originated
from the dural of the cribriform plate and planum sphenoidale.
Left olfactory nerve was preserved anatomically although right

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Table 2
Prognostic factors related to post-operative preservation of olfactory function in olfactory groove meningioma.
Prognostic factor

Sex
Female
Male
Age (year)
<50
50
Peritumoral edema
None to mild
Moderate to severe
Tumor size (cm)
<4
4
Pre-operative olfaction
Normosmia
Hyposmia/anosmia
Tumor consistency
Soft
Hard
Surgical approach
Frontolateral
Bifrontal

Post-operative olfaction
Sacrice

Preserve

5 (29.4%)
13 (56.5%)

12 (70.6%)
22 (43.5%)

5 (29.4%)
13 (56.5%)

12 (70.6%)
22 (43.5%)

4 (33.3%)
14 (50.0%)

8 (66.7%)
14 (50.0%)

3 (21.4%)
15 (57.72%)

11 (78.6%)
11 (42.3%)

2 (15.4%)
16 (59.3%)

11 (84.6%)
11 (40.7%)

7 (43.8%)
11 (45.8%)

9 (56.3%)
13 (54.2%)

6 (28.6%)
12 (63.2%)

15 (71.4%)
7 (36.8%)

olfactory nerve was sacriced (Fig. 1c and d). Gross total resection
was achieved (Fig. 1e and f) and post-operative KVSS score of left
nose was improved to 22.
4. Discussion
OGM comprise approximately 413% of all intracranial meningiomas [1,5,8,13,14]. Most patients with OGM suffer from
headache, visual impairment, personality change, and memory
disturbance [1,15]. Considering the anatomical location of OGM,
olfactory impairment could be the earliest symptom, but only a
few patients present anosmia [2,9]. Disturbance of olfaction in
patients with OGM usually occurs gradually and affects the unilateral nose [2]. Therefore, most patients do not recognize the
olfactory dysfunction because of maintained olfactory function
of the non-affected side of the nose. In the present study, only
six patients (15%) presented disturbance of olfaction, although 27
patients (67.5%) actually had abnormality on olfactory function test.
The loss of olfaction can cause profound psychological problems
affecting to occupation and quality of life [10,16]. Unfortunately,
investigations of olfactory function after resection of OGM have
rarely been done and the results of early studies were disappointing
[2,4,17]. Efforts to preserve post-operative olfaction have increased
as the concern for the quality of life after surgery has increased. Yet,
most patients tolerate a loss of unilateral olfactory function and the
sparing of olfaction in one portion of the nose is considered acceptable. Presently, 21 patients maintained their olfaction and did not
suffer from diminished smell and taste after surgery, although nine
patients retained only unilateral olfaction.
Tumor size and pre-operative olfactory dysfunction are thought
to affect post-operative olfactory function. Tumor size correlates
with olfactory dysfunction and is a major problem for surgical treatment [1,14]. A prior study demonstrated that the chance to spare
the post-operative olfactory function contralateral to the tumor is
signicantly increased in small-sized OGM (<3 cm) and preoperative normosmia [2]. OGM is a slow, indolent growing tumor that
gradually and chronically compresses and distorts the olfactory
nerve, resulting in degeneration and distortion of this nerve and
related apparatus [4]. Therefore, if the tumor is large in a patient
with pre-operative olfactory dysfunction, the olfactory nerve is
more vulnerable to surgical manipulation and, consequently, disruption of blood supply to the olfactory nerves or direct damage of

P-value

Odd ratio

0.094

3.120

0.094

3.120

0.335

2.000

0.035

5.000

0.016

8.000

0.897

1.088

0.032

4.286

olfactory nerve may result in post-operative olfactory dysfunction

[2,4]. Presently, the preservation rate of post-operative olfaction
was higher in patients without pre-operative olfactory dysfunction
than in patients with pre-operative olfactory dysfunction (84.6%
vs. 40.7%, respectively; p = 0.016). The likelihood of sparing postoperative olfaction was greater when the tumor was under 4 cm in
diameter (78.6% in size 4 cm vs. 42.3% in size <4 cm, p = 0.035).
Variable surgical approaches have been used for OGM resection,
such as unilateral frontal, bifrontal, pterional, frontoorbitonasal,
supraorbital (key-hole), endoscopic endonasal and combined
craniofacial approaches. Among them, the bifrontal and frontolateral approaches are performed in our institute. The bifrontal
approach can provide direct access the both sides of the tumor, vascular pedicle, and the ethmoidal area of origin [1,5]. Wide exposure
offers a good chance for radical resection of a tumor and sufcient
reconstruction of the skull base [1,7,13]. Therefore, the bifrontal
approach is considered as a suitable accessible route for large-togiant OGM. However, there are some well-known disadvantages.
First is the opening of the frontal sinus, which demands the surgical technique of exenteration, packing, and sealing [5,14]. Second is
the ligation of the superior sagittal sinus, which infrequently contributes to brain edema and which requires a frontal lobectomy [7].
Third is the late visualization of the optic apparatus and the anterior cerebral complex [13]. The olfactory nerve is also viewed later
after a major part of the tumor has been removed. Therefore, the
chance to damage the olfactory nerve is higher than other surgical
approaches. Compared to the bifrontal approach, which accesses
the tumor through the superior aspect of the tumor, the frontolateral approach accesses the tumor through the lateral region of the
tumor. Olfactory tracts are displaced laterally in large OGM [13].
Therefore, this approach can allow the early visualization of neurovascular structures including the olfactory system [1,13]. Unless
the meningiomas involve the olfactory nerve, it is possible to dissect the nerve from the tumor under direct visualization and to
preserve the olfactory nerve anatomically. Another advantage of
the frontolateral approach is the absence of requirement for the
retraction of the contralateral frontal lobe to transect or damage the
contralateral olfactory nerve [7,18]. Therefore, anatomical preservation of contralateral olfactory nerve is possible and the chance
of preservation of olfaction at least one nostril is higher than using
the bifrontal approach. Bassiouni et al. suggested that a unilateral
surgical approach is suitable to spare the contralateral olfactory

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Fig. 1. Preoperative contrast-enhanced T1-weighted axial (a) and sagittal (b) MR images show a giant olfactory groove meningioma with symmetrical growth on both side.
Perioperative photographs before (c) and after (d) mass removal demonstrate that left olfactory nerve was in anatomical continuity after tumor removal. Post-operative
contrast-enhanced T1-weighted axial (e) and sagittal (f) MR images reveal that there was no evidence of recurrence after complete removal of tumor. Rt., right; Lt., left; ON,
optic nerve; OFN, olfactory nerve.

apparatus undisturbed, although there was no statistical signicance to these observations [4]. Our study also showed that the
preservation of post-operative olfaction correlated with surgical
approaches. Among the 21 patients underwent surgical resection
of OGM through the frontolateral approach, 15 patients maintained
their olfaction, although there were six patients with sacrice of
one olfactory nerve and preservation of only contralateral nostril
(p = 0.032). The frontolateral approach is thought to be limited in

the resection of the contralateral extended tumor because of inadequate visualization [13]. However, removal of the anterior falx
can provide a sufcient view of the contralateral extended portions and, recently, frontolateral or lateral supraorbital approach
was suggested, even in huge lesions with bilateral extension [18].
In our experience, six patients with bilateral extended OGM >5 cm
underwent surgical resection through the frontolateral approach.
All had gross total resection without surgical complications.

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Currently, intra-operative neurophysiological monitorings in

the operation room are being commonly performed for minimizing the iatrogenic neurological decits. Olfactory evoked potentials
(OEPs), recorded in response to electrical stimulation of the olfactory mucosa, can provide reliable reection of olfactory functions
under constant conditions [19]. One study used the OEPs during the
surgery of brain tumors and did not report post-operative anosima
or worsening the olfaction [20]. Therefore, prospective studies that
investigate the usefulness and limitations of OEPs in surgery of
OGM are needed in the future.
5. Conclusions
Considering that the olfaction is an important perception in
emotional and social life, preservation of olfaction in OGM surgery
should be tried. Especially, the chances of preservation of postoperative olfaction are greater for small-sized tumors and in
patients without preoperative olfactory dysfunction. Although
there are variable factors should be considered when choosing a
surgical approach, the frontolateral route is suitable to preserve the
olfactory function, even in large tumors with bilateral extension.
Acknowledgement
This research was supported by Leading Foreign Research
Institute Recruitment Program through the National Research
Foundation of Korea (NRF) funded by the Ministry of Education,
Science and Technology (MEST).
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