Download superior and supreme turbinate, crista galli process, uncinate process

Rom J Morphol Embryol 2014, 55(3 Suppl):1099–1104
ORIGINAL PAPER
RJME
Romanian Journal of
Morphology & Embryology
http://www.rjme.ro/
The anatomo-radiological study of unusual extrasinusal
pneumatizations: superior and supreme turbinate, crista
galli process, uncinate process
MIHAIL DAN COBZEANU1), VASILICA BÂLDEA2), MIRCEA CĂTĂLIN BÂLDEA3), PATRICIA SONIA VONICA1),
BOGDAN MIHAIL COBZEANU1)
1)
2)
3)
Department of Otorhinolaryngology, “Grigore T. Popa” University of Medicine and Pharmacy, Iassy, Romania
Department of Otorhinolaryngology, Emergency County Hospital, Buzau, Romania
Department of Oro-Maxillo-Facial Surgery, “Carol Davila” University of Medicine and Pharmacy, Bucharest, Romania
Abstract
Introduction: One of the aspects that have an influence on rhinosinusal endoscopic surgery is extrasinusal pneumatization, which can also
affect less common structures at this level. The pneumatization of the superior and supreme turbinates, uncinate process and crista galli are
perfect examples of this situation. The diagnosis is made only through imaging methods. Materials and Methods: This is a retrospective
anatomo-radiological study analyzing 205 CT scans of the facial sinuses performed over a three years period. All patients were symptomatic
and the CT scans were performed to assess the cases prior to surgery. Ninety-seven patients were females and 108 males, aged between
18 and 91 years. Results: The prevalence of pneumatization and the prevalence of the different pneumatization types (superior and supreme
turbinate, uncinate process and crista galli) were determined. Conclusions: The pneumatization of the supreme turbinate (10.24%) was less
common than that of the superior turbinate (29.76%) and affected all its anatomical variations (A, B, C). Pneumatization of the crista galli
process was recorded in 22.92% of the cases, especially in association with type 2, while the prevalence of pneumatized uncinate process
was of only 3.41% (uni- or bilateral).
Keywords: anatomo-radiological study, unusual extrasinusal pneumatization, turbinates, crista galli, uncinate process.
 Introduction
The nasal turbinates can contain one or more aerated
cells. While the pneumatization of the middle turbinate
has often been described, pneumatized superior turbinates
[1, 2], supreme turbinates, uncinate process and crista galli
are rare [3, 4].
The superior turbinate belongs to the ethmoid bone,
medially limiting the superior meatus in which the cells
of the posterior ethmoid and of the sphenoid drain [5].
Usually, it is about half the length of the middle turbinate,
being situated above its posterior half [6]. The ostium of
the sphenoid sinus is located medially and superior to the
postero-inferior portion of the superior meatus [7]. Thus,
the superior turbinate serves as an essential landmark
during endoscopic posterior ethmoidectomy and sphenoidectomy surgery. The superior turbinate is also known as
the “forgotten turbinate” [8] as it is difficult to identify
through nasal endoscopy, a preoperative CT scan being
recommended.
The supreme turbinate is a rare anatomic variation.
It can be uni- or bilateral, sometimes pneumatized by a
posterior ethmoid cell which drains into the posterior
ethmoid/sphenoidal sinus, as described by Stammberger
[9]. There are three types of association between the
superior and supreme turbinates. Type A is the most
common one, with the supreme turbinate being smaller
than the superior one. Type B (superior and supreme
turbinate have the same size) and type C (supreme
turbinate larger than the superior one) are rare. The
ISSN (print) 1220–0522
supreme meatus is located on the infero-lateral side of the
supreme turbinate and contains the ostium of a posterior
ethmoidal cell [3, 4, 10, 11].
The uncinate process is a thin ethmoid bone plate,
which fuses inferiorly with the ethmoid process of the
inferior nasal turbinate [12]. It is a key structure of the
ethmoid bone and forms the semilunar hiatus at the level
of the lateral nasal wall. Its pneumatization is a rare
abnormality. The uncinate process occupies the free
infundibular zones and may generate areas of mucosal
contrast [13]. The prevalence of this anatomic variation is
estimated between 0.4–13% by different authors [14–17].
The crista galli is an endoscopic surgical landmark
in frontal sinus approach and pituitary surgery. It can be
pneumatized resulting in a small-aired sinus with no
clinical echo. The excessive pneumatization can lead to
ENT-related headache or may be the origin of neurological symptoms with frontal lobe implications [3, 4].
When pneumatization is associated with congenital
malformations involving midline defects (meningocele or
defective embryological development of the ectoderm
near crista galli), the clinical manifestations become
obvious [18].
The study purpose was to determine the general prevalence and that of the less common types of extrasinusal
pneumatization: superior nasal turbinate, supreme nasal
turbinate, uncinate process, crista galli, and if their different
associations vary with age, gender, chronic recurrent
rhinosinusitis.
ISSN (on-line) 2066–8279
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Mihail Dan Cobzeanu et al.
 Materials and Methods
We retrospectively investigated the preoperative CT
scans performed in the Iassy and Buzău (Romania)
outpatient or emergency departments, in the interval
January 2008–June 2010, in 205 patients with ENTrelated symptoms. The subjects were aged 18–91 years,
97 females (47.32%) and 108 males (52.68%); informed
consent was obtained.
The results refer to ENT symptomatic patients and
not general population. Spiral tomography technique was
used to expose the facial sinuses for better image accuracy,
allowing complex bone reconstruction. Pneumatization
of every air cell found at this level was considered, no
matter its size or location.
Table 1 – Estimated parameters in patients vs. presence
of superior turbinate pneumatization
(df=1)
χ
2
2
0.4273801
Pearson’s 
Correlation factor (Spearman’s rank r) 0.0995907
p (95% CI)
0.51328
0.51564
Figures 3–6 present the different types of superior
turbinate pneumatization according to extension, localization and drainage type.
 Results
Superior turbinate pneumatization
Superior turbinate pneumatization was identified in
61 subjects, the prevalence being 29.76% (61/205). Thirty
(27.78%) were men and 31 (31.96%) women (Figure 1).
Thirty-six (17.56%) were bilateral, 25 (12.2%) unilateral,
14 (6.83%) left and 11 (5.37%) right (Figure 2).
Figure 3 – CT scan of the paranasal sinuses, coronal
reconstructions. Bilateral superior turbinate pneumatization: 1. Small size pneumatization without rhinosinusitis; 2. Hyperpneumatization with left mucocele.
Figure 4 – CT scan of the paranasal sinuses, coronal
and axial slices. Bilateral superior turbinate pneumatization: 1. Coronal section; 2. Axial section; 3. Bilateral
pneumatized superior turbinate drainage on the sphenoid sinus.
Figure 1 – Gender distribution of cases by the presence/
absence of superior turbinate pneumatization.
Figure 5 – CT scan of the paranasal sinuses, coronal
sections. Anatomic variations of superior turbinate
pneumatization: 1. Left superior turbinate pneumatization with uncinate process insertion and right
pneumatization of the superior turbinate; 2. Right
superior turbinate pneumatization, type C; 3. Left
superior turbinate pneumatization with drainage on
the suprabullar recess.
Figure 2 – Distribution of cases by superior turbinate
pneumatization type.
Statistical results (Table 1) show that in our patients
there was no significant association between gender and
superior turbinate pneumatization (χ2=0.427, p=0.51328,
95% CI).
Figure 6 – CT scan of the paranasal sinuses. Pneumatization of the left superior turbinate revealed by all
types of sections: 1. Coronal slice: hyperpneumatization with septum and uncinate process mucosal
contact; 2. Sagittal section: the pneumatization of the
posterior part of the superior turbinate and association
with left unpneumatized supreme turbinate; 3. Axial
section: the left superior turbinate pneumatization.
The anatomo-radiological study of unusual extrasinusal pneumatizations: superior and supreme turbinate…
Superior turbinate is best studied on coronal sections,
but it also can be identified on axial and sagittal sections
as in Figure 6.
Supreme turbinate pneumatization
Supreme turbinate was identified in 61/205 cases,
prevalence of 29.76%, of which 43 (20.97%) were bilateral
and 18 (8.78%) unilateral. Its pneumatization was found
in 21/205 (10.24%) subjects. Of these, 10/205 (4.88%)
were bilateral and 11/205 (5.37%) unilateral, six (2.93%)
left and five (2.44%) right (Figure 7).
1101
four (1.95%) men and three (1.46%) women. Bilateral uncinate process pneumatization was present in 3/205 (1.46%)
subjects, and unilateral in 4/205 (1.95%) (Figure 10). All
cases of unilateral uncinate process pneumatization where
found only on the left side. The mean age of patients with
this anatomical variation was 45.67±26.39 years [3, 4].
Figure 10 – Uncinate process pneumatization.
Figures 11–13 show various types of pneumatized
uncinate processes.
Figure 7 – Supreme turbinate pneumatization.
Figures 8 and 9 present different imaging appearances
of supreme turbinate pneumatization variations depending
on location, extension or drainage.
Figure 8 – CT scan of the paranasal sinuses. Anatomic
variations of supreme turbinate pneumatizations:
1. Right pneumatization type C; 2. Left pneumatization
type C; 3. Bilateral pnematization type C, with left
drainage on the sphenoid sinus; 4. Left pneumatization type A associated with lamelar pneumatzation of
ipsilateral superior turbinate.
Figure 11 – CT scan of the paranasal sinuses, coronal
sections: 1. Bilateral uncinate proces pneumatization
with pathological process on the left; 2. Left uncinate
process pneumatization associated with right uncinate
medialization.
Figure 12 – CT scan of the
paranasal sinuses, coronal
section: 1. Bilateral uncinate
process pneumatization.
Figure 9 – CT scan of the paranasal sinuses, sagittal
reconstructions, successive sections: 1. Superior turbinate pneumatization; 2. Supreme turbinate pneumatization.
Uncinate process pneumatization
Uncinate process pneumatization (uncinate bulla) is
one of the anatomical variations of this surgical landmark,
possibly associated with diminished sinus ventilation,
especially of the frontal recess, anterior ethmoid, ethmoidal
infundibulum region. We identified 7/205 (3.41%) cases,
Figure 13 – CT scan of the paranasal sinuses, axial
sections: 1. Left uncinate process pneumatization associated with type 5 ipsilateral septal deviation (Mladina
classification); 2. Left uncinate process pneumatization
associated with ipsilateral concha bullosa.
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Mihail Dan Cobzeanu et al.
Crista galli pneumatization
We first identified the three types of crista galli
according to their location to the ethmoidal lamina
cribriformis, finding the following prevalences: type I –
crista galli situated entirely above the lamina cribriformis,
48/205 (23.41%) cases; type II – crista galli situated less
than 1/2 of its height under the lamina cribriformis,
127/205 (61.65%) cases; type III – crista galli situated
more than 1/2 of its height under the lamina cribriformis,
30/205 (14.64%) cases [4].
Pneumatization was found in all types of crista galli,
but in different proportions: pneumatized type I – 9/205
(4.39%) cases; pneumatized type II – 27/205 (13.17%)
cases; pneumatized type III – 11/205 (5.36%) cases [4].
The prevalence of crista galli, both in pneumatized and
unpneumatized forms are presented in Figure 14.
Figure 14 – Distribution of cases by crista galli pneumatization type.
Figures 15–17 present different imaging appearances
of variations of crista galli.
Figure 17 – CT of the paranasal sinuses, coronal
reconstructions. Crista galli pneumatization: 1. Type II
with symmetric ethmoid roof; 2. Type I associated with
superior turbinate pneumatization; 3. Type III. Dotted
line: cribriform plate of the ethmoid bone.
 Discussion
Superior turbinate pneumatization
In the few published studies on superior turbinate
pneumatization the prevalence is different probably
because of the different evaluation methods. The highest
prevalence is reported by direct visualization in cadaver
studies. Van Alyea studied the ethmoid labirinth of 100
cadavers finding pneumatization in 57% (the highest
value), unrelated to rhinosinusitis [19]. This relationship
was reported by other authors following endoscopic
studies. In 1991, Stammberger found rhinosinusitis and
significant superior turbinate pneumatization in a small
group of patients, all with indication for functional
endoscopic sinus surgery (FESS) [9]. He also described
a bilateral pneumatization extending between the middle
turbinate and the nasal septum causing mucosal contact
and thus causing headache and hyposmia or anosmia by
olfactive fossa block. In 1996, Clerico reported three
cases of extensive superior turbinate pneumatization with
severe migraines not responding to usual medication
[8]. Turbinate pneumatization is still a rare cause of
headache [1, 10], this being also supported by our research
(Figure 5). CT imaging studies [20] for rhinosinusitis
found a prevalence of 48% for the superior turbinate
pneumatization (27% unilateral and 21% bilateral),
comparable to that found by Van Alyea in cadaver studies
(57%). In our radio-anatomical research, the prevalence
was 29.75% (61/205 cases), lower than in the two previous
studies by Van Alyea [19] or Ariyürek et al. [20], with
similar prevalence for bilateral and unilateral cases. The
superior turbinate is a constant landmark for identifying
both the sphenoethmoid recess and the superior resection
border of the natural sphenoid ostium [21].
Supreme turbinate pneumatization
Figure 15 – CT scan of sinuses, axial slice (1) and
coronal reconstructions (2 and 3). Unpneumatized crista
galli types: 1. Type I; 2. Type II; 3. Type III.
Figure 16 – CT scan of sinuses, axial (1 and 2) and
coronal (3) sections. Crista galli pneumatization:
1. Type I; 2. Drainage of the partial pneumatized
crista galli type I on the frontal sinus; type II associated
with ethmoidal roof asymmetry.
When it exists, the supreme turbinate serves as a
surgical landmark for the posterior ethmoid and sphenoid
approach [22–24]. It is less used as a landmark than the
superior turbinate, because it is inconstant.
The inferior supreme turbinate attachment is lateral
to the sphenoid ostium. Usually the ostium is identified
between the inferior attachment of supreme turbinate
situated laterally and nasal septum medially. The sphenoid
ostium has a round or oval shape. The opening of the
sphenoid ostium can be hidden by the medial part of
supreme turbinate, which is bent downwards [25]. The
sphenoid ostium is located on the anterior wall of sphenoid
sinus, 1.5 cm above the floor; the optic nerve and internal
carotid artery can often lie on the lateral sides of the sinus
[26].
The anatomo-radiological study of unusual extrasinusal pneumatizations: superior and supreme turbinate…
Orhan et al. [27] developed a study based on
microscopy of 20 adult cadavers for the anatomical
variants of superior and supreme turbinates. They found
a prevalence of 60% for the supreme turbinate (the
highest value reported) and described the types. The
radio-anatomical studies report a lower prevalence for
supreme turbinate than direct microscopic visualization
studies. Orhan et al. [27] found 58% prevalence for type
A and 41.7% for type B and type C. In types B and C,
the supreme turbinate can easily be damaged being
similar to other structures and difficult to recognize, in
those cases causing hyposmia or anosmia.
In our study using imaging material, we obtained a
prevalence of the supreme turbinate of only 29.75%
because the small turbinates (less than 2 mm) were
ignored. Bilateral forms were predominant, 60.65% of
the supreme turbinates presenting pneumatization.
Uncinate process pneumatization
Pneumatized uncinate process (uncinate bulla), as
one of the variants of uncinate process that favor an
inflammatory pathology or increase the surgical risk
(difficult orientation during uncinectomy) can decrease
sinus ventilation [28]. Imaging studies reveal that the
pneumatization of the uncinate process is due to overpneumatization of the agger nasi cell [29].
Pneumatization of the uncinate process occurs by the
extension of the agger nasi cell into the anterior-superior
part of the uncinate process [14, 30]. Many studies give
a small percentage to this anatomical variation, between
0.4% and 13%. Kennedy and Zinreich [15] found the
presence of uncinate bulla in 1/230 patients (0.4%, the
lowest value). Bolger et al. [14] also found a low value
of 2.5% on 202 CT scans. Arslan et al. [29] found a
prevalence of 4%, Earwaker [16] of 9.1%, and Riello
and Boasquevisque [17] of 13%. Due to its rarity, there
are also authors who found no cases in some study
groups [14]. Kantarci et al. [13] reported a prevalence of
5% assessed on 512 CT scans. These authors consider that
changes of the uncinate process can cause an important
functional blockage of the osteomeatal complex.
In our study, the prevalence of uncinate process
pneumatization of 3.41% (7/205 cases) is comparable to
that of Bolger et al. [14]. The prevalence of 4% found by
Arslan et al. [31] is also close to our finding. Most cases
(85.71%) showed various radiological signs of former
rhinosinusitis indicating a possible role in the pathogenesis
of rhinosinusitis. When associated with other anatomical
variations that cause the narrowing of ethmoid infundibulum (Haller cell, middle turbinate abnormalities, concha
bullosa), the risk of recurrent chronic rhinosinusitis
increases. These anatomical variations were also often
identified in our study.
Crista galli pneumatization
Crista galli is a median ridge of bone that projects
from the cribriform plate of the ethmoid bone, and
serves as a landmark in endoscopic surgery. It can be
pneumatized, containing a cell usually coming from
anterior ethmoid. Usually, this anatomical variation has
no clinical response and can only be revealed on preoperative radiographs. The identification of crista galli,
1103
pneumatized or not, can be done in both axial and coronal
planes, but relevant considerations are better made with
the last mentioned. Anatomical variations of this surgical
landmark regard various aspects of morphology in relation
to the cribriform plate of the ethmoid or its pneumatization. All forms described morphologically can be pneumatized. Hajiioannou et al. [18] describe in their studies
a crista galli classification in three categories and give a
prevalence of pneumatization of 14.1%.
The research could determine the prevalence for each
type of crista galli pneumatization, the rates found by us
being comparable to those in the mentioned studies, type II
having the highest prevalence of 61.95% (127/205). Crista
galli pneumatization was observed in 47 (47/205) cases,
with a prevalence of 22.92%, slightly higher than in other
studies [3].
 Conclusions
Pneumatization of the superior and supreme turbinate
can only be diagnosed by imaging, best by coronal sections.
Its prevalence is 29.76% and 10.24%, respectively, all types
being identified and bilateral variations more common.
Pneumatization of uncinate process, rare anatomical variation, unilateral or bilateral (3.41%) with predominantly
unilateral forms, is often associated with anterior rhinosinusitis (85.71%). Crista galli pneumatization, identified
in all three types (I, II, III) is a rare anatomical variation,
with a prevalence of 22.92%, type II being the most
commonly seen. Coronal sections are preferred to detect
the pneumatization of all investigated structures, but axial
and sagittal ones may also be useful, because they allow a
better assessment of the degree of extension and location,
and the association of other anatomical variations at this
level.
Acknowledgments
This study is part of the “Anatomical variations of
surgical landmarks used in the diagnosis and endoscopic
rhinosinusal approach” project, and has been approved by
the Research Ethics Committee of the “Grigore T. Popa”
University of Medicine and Pharmacy, Iassy, Romania,
No. 15368/09.08.2011.
Author contribution
All authors have equally contributed to the manuscript.
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Corresponding author
Mihail Dan Cobzeanu, Professor, MD, PhD, Department of Otorhinolaryngology, “Grigore T. Popa” University of
Medicine and Pharmacy, 16 Universităţii Street, 700115 Iassy, Romania; Phone +40722–628 390, e-mail:
[email protected]
Received: December 3, 2013
Accepted: November 7, 2014