Maxilo-facial surgery
THREE-DIMENSIONAL ASSESSMENT OF THE PHARYNGEAL AIRWAY
AND MAXILLARY SINUS VOLUMES IN INDIVIDUALS WITH
NON-SYNDROMIC CLEFT LIP AND PALATE
Ana NEMŢOI1, Yllka DECOLLI1, Ana Elena PETCU2, Sidonia SUSANU3,
Simona GAVRILESCU4, Alexandru NEMŢOI5, Danisia HABA6
PhD student, Dept. Oral and Maxillofacial Surgery, “Gr. T. Popa” University of Medicine and Pharmacy, Iasi, Romania
Lecturer, Dept. Oral and Maxillofacial Surgery, “Gr. T. Popa” University of Medicine and Pharmacy, Iasi, Romania
3
Plastic surgeon, Dept. Pediatric Surgery, “Gr. T. Popa” University of Medicine and Pharmacy, Iasi, Romania
4
Lecturer, Dept. Pediatric Surgery, “Gr. T. Popa” University of Medicine and Pharmacy, Iasi, Romania
5
Assistant lecturer, Dept. Anatomy, “Gr. T. Popa” University of Medicine and Pharmacy, Iasi, Romania
6
Professor, Dept. Oral and Maxillofacial Surgery, “Gr. T. Popa” University of Medicine and Pharmacy, Iasi, Romania
Corresponding author: [email protected]
1
2
Abstract
Introduction: Children with cleft lip and palate (CLP)
are known to have airway problems. Introduction of ConeBeam CT (CBCT) and imaging software has facilitated
generation of 3D images for assessing the volume of
maxillary sinuses and pharyngeal airway. Consequently,
the present study aimed at evaluating and comparing the
maxillary sinus and pharyngeal airway volume of patients
with cleft lip and palate in healthy patients, using cone
beam computed tomography (CBCT) images.
Materials and method: The sample group included 27
individuals (15 with cleft lip and palate subjects and 12
healthy subjects). The pharyngeal airway and each
maxillary sinus were three-dimensionally assessed,
segmented and their volume was calculated. A comparison
between the right and left sinus was performed by Student
t-test, and the differences between the control and cleft
groups were calculated using ANOVA.
Results: No statistically significant differences were
found when the maxillary sinuses volumes from each side
were compared (p >0.05). The unilateral CLP patients
presented the lowest sinus volume. Individuals with CLP
did not exhibit a total airway volume smaller than the nonCLP controls.
Conclusions: 3D imaging using CBCT and Romexis
software is reliable for assessing maxillary sinus and
pharyngeal airway volume. The present study showed that
the pharyngeal airway is not compromised in CLP
individuals. The unilateral CLP individuals present
maxillary sinuses with smaller volumes, no differences
being recorded between the cleft and non-cleft side.
Keywords: cone beam CT, pharyngeal airway and maxillary
sinus volumes, cleft lip and palate
1. INTRODUCTION
Patients with cleft lip and palate (CLP) present
several anatomical variations, apart from the gap
between the nasal and maxillary processes. For
example, alteration in midface structures is a
common finding in affected individuals.
International Journal of Medical Dentistry
Anatomical abnormalities associated with CLP
increase the risk of airway complications [1]. CLP
are frequently associated with nasal abnormalities,
such as septal deviation, nostril atresia, turbinate
hypertrophy, maxillary constriction, vomerine
spurs and alar constriction [2-6].
In part, these abnormalities are attributed to
the congenital defect itself and also to the surgeries
done to repair the orofacial defect [7,8].
Collectively, nasal abnormalities tend to reduce
the dimensions of the nasal cavity and airway
functions [4,9]. These differences may lead to
numerous impairments, potentially affecting the
health condition of the ear, nose and throat. Sinus
disease, mainly sinusitis, is frequently noted in
CLP patients [10-12]; this highlights the importance
of the maxillary sinus, as a major component of
the midface, and the need of a better understanding
of its role both in the developmental process and
in the manifestation of the disease.
Previous studies evaluated the area of maxillary
sinuses of CLP patients using different imaging
modalities, such as conventional radiographs and
multi-slice computed tomography (MSCT) [11,
13–17]. However, area estimation is a twodimensional (2D) assessment of a threedimensional (3D) structure, therefore potentially
limited and prone to error. In this respect, a 3D
volumetric evaluation of the sinuses appears as a
more accurate option to better understand the
complexity of these structures. Moreover, CBCT
is also replacing several MSCT studies, due to its
lower cost and lower radiation dose [18].
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Ana NEMŢOI, Yllka DECOLLI, Ana Elena PETCU, Sidonia SUSANU, Simona GAVRILESCU, Alexandru NEMŢOI,
Danisia HABA
With the increased application of cone beam
computed tomography (CBCT) in dental practice,
more patients with CLP are undergoing CBCT
scanning prior to alveolar bone grafting
procedures. The CBCT image allows visualization
of structures in all three planes, providing a 3D
view of both defects and structures.
Airway patency has been evaluated by twodimensional (2D) radiographic imaging, such as
lateral and anterior-posterior cephalometric
films and functional studies, e.g., rhinomanometry
and plethysmography [19-22].
Previous studies have shown that 3D
imaging using CBCT is a simple and effective
method to accurately analyze the airway
[23,24]. Recently, numerous studies have been
performed using CBCT, for assessing the
airway in relation with facial morphology in
individuals with sleep apnea [25,26]. At
present, few CBCT studies devoted to the
airway of individuals with CLP have been
published, despite the frequently occurring
airway problems in such subjects [2-5].
The present study compares the volume of the
maxillary sinuses and pharyngeal airway in
patients with cleft lip and palate to patients without
cleft, by means of CBCT images, and assesses the
differences between the right and left sides, and
also between the cleft and non-cleft sides.
The experimental group included 27
individuals (15 with cleft lip and palate and 12
healthy subjects).
The exclusion criteria were: 1) history of
treatment for sleep-disordered breathing,
including tonsillectomy, adenoidectomy, or
recurrent tonsillitis; 2) frequent colds (6 or more
per year); 3) history of dysphagia and continuous
positive airway pressure therapy. A further
exclusion criterion for the control groups
included any type of syndrome. All individuals
with CLP had no maxillary expansion and
alveolar bone grafting.
Patients’ skeletal maturity was determined by
the cervical vertebral maturation method
developed by Baccetti et al. [23]. The juvenile
subjects were in cervical stages 2 and 3, and the
adolescent subjects - in stages 4 and 5. The
juvenile group was formed of 9 individuals with
CLP and 7 individuals without CLP; the
adolescent one included 6 individuals with CLP
and 5 without CLP (Table 1).
Seven patients in the juvenile group with CLP
had unilateral CLP, and 2 had bilateral CLP. In
the adolescent group with CLP, 6 patients had
unilateral CLP. Lip closure by Millard-type lip
repair had been performed in most patients, at a
mean age of 3.8 months (SD, 1.2 months), and
closure of the palate had been performed by
pushback palatoplasty and the Furlow method,
at a mean age of 8.6 months (SD, 3.9 months).
Bone grafting had been done at a mean age of
10.2 years (SD, 1.4 years). No patient had
undergone pharyngeal flap surgery.
2. MATERIALS AND METHOD
A retrospective study was developed on
subjects recruited from the Plastic Surgery Clinic,
“St. Mary” Emergency Hospital for Children, Iasi.
Table 1. Subjects and their ages in the 4 groups
Group
N
Age (year)
Juvenile (CS 2 and 3)
Adolescent (CS 4 and 5)
CLP
Control
CLP
Control
9
7
6
5
9.6±1.2
10.8±1.8
13.7±0.7
14.4±1.3
CS, Cervical stage of cervical vertebral maturation
All control subjects had normal craniofacial
morphology with no jaw deformities. The control
group included 19 individuals who were gender,
age, and Sella-Nasion (SN) matched with the
experimental group. The inclusion criteria
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referred to Angle Class I malocclusion with
beginning CBCT records for starting orthodontic
treatment and no prior orthodontic treatment, no
habitual mouth breathing recorded and no prior
adenoidectomy and/or tonsillectomy.
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THREE-DIMENSIONAL ASSESSMENT OF THE PHARYNGEAL AIRWAY AND MAXILLARY SINUS VOLUMES IN
INDIVIDUALS WITH NON-SYNDROMIC CLEFT LIP AND PALATE
The protocol of the investigation was reviewed
and approved by the Ethics Committee of the
Faculty of Dentistry, “Gr. T. Popa” University of
Medicine and Pharmacy, Iasi, Romania. Before
the CBCT scan, patients’ parents were fully
informed on the purpose of this study and on the
risks associated with CBCT.
The equipment used was PlanmecaPromax
3D CBCT Mid (Planmeca OY, Helsinki, Finland).
Scanning was performed by selecting a 200 x 170
mm view field and the following exposure
parameters: 90 kV, 12 mA, 13.8 sec and 0.4 x 0,
4x 0, 4 mm voxel size. DICOM files were imported
into Romexis 3.0.1 (Planmeca OY, Helsinki,
Finland), a software capable of volume rendering.
To achieve the axial, coronal and sagittal sections,
the CBCT reconstructions were established with
a 1 mm thickness, at a distance of 1 mm.
First, a CBCT technician de-identified the files,
removing the name, sex and date of birth from
the DICOM, after which the files were reoriented
to a standardized view. Next, in a secluded room
with dim light, a well-calibrated oral radiologist
with experience in tomographic appraisal
performed the assessment of images.
The maxillary sinuses were evaluated
separately (right/left and cleft/non-cleft). The
threshold was defined with the Measure Ellipsoid
Tool, to include the sinus space and to remove
any artifact and background. After threshold
selection, a three-dimensional editing was used
to obtain refined surfaces of the segmentation,
resulting in a VOI subsequently rendered into a
shaded surface mesh, and each segmented
volume (cm3) was calculated (Figs. 1, 2).
Fig. 1.Multiplanar reconstruction of CBCT images demonstrating the contours
of the segmented sinuses: sagittal (A), coronal (B) and axial (C) views
Fig. 2. Antero-posterior (A) and sagittal (B) views of 3D CBCT images superimposed with the 3D
segmentation of the maxillary sinuses and the isolated 3D volume (C)
The pharyngeal airway was segmented and the
volume was rendered in a multiplanar
reconstruction (MPR) mode. The threshold tool
International Journal of Medical Dentistry
was used to select the pharyngeal airway space.
The threshold was defined by the Measure Cube
Tool, to include the pharyngeal airway. The 3D
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Ana NEMŢOI, Yllka DECOLLI, Ana Elena PETCU, Sidonia SUSANU, Simona GAVRILESCU, Alexandru NEMŢOI,
Danisia HABA
Region Growing function was used to create a 3D
displaying the pharyngeal airway space from each
region of interest. The volume (cm3) was determined
from the total airway segmentation. The airway
was further segmented into three sections:
nasopharynx, oropharynx and hypopharynx. The
superior border of the nasopharynx was defined
as the posterior choana and inferiorly as to the
horizontal line along the hard and soft palates. The
oropharynx was defined superiorly by the soft
palate and inferiorly by the vallecula. The
hypopharynx was defined superiorly by the hyoid
bone and vallecula and inferiorly by the junction
of the larynx and oesophagus (Fig. 3).
The linear measurement tool in the Romexis
3.0.1 software was used to determine SN, to
properly match the experimental and control
groups.
Fig. 3. 2D sagital (A) and 3D sagittal (B) views of CBCT images superimposed with
the 3D segmentation of the pharyngeal airway and the isolated 3D volume (C)
Fig. 4. Two-dimensional axial slice images of the pharyngeal airway in the 3 defined planes:
A - nasal floor plane; B - soft palate plane; C - epiglottal plane
All volumetric values obtained were tabulated,
and Student t-test was performed to compare the
maxillary sinus volumes between the sides, the
right and left part of the control and BCLP
groups, the cleft and non-cleft sides of UCLP
group, the pharyngeal airway volume between
the cleft and the non-cleft group.
The average volume of the sinuses and
pharyngeal airway was calculated, resulting in
an average value for each patient, and ANOVA
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was used to determine the differences among the
volumes of UCLP, BCLP and control (non-cleft)
groups. Statistical analyses were performed with
a SAS software version 9.4 (Cary, NC, USA). The
level of significance was set at p < 0.05.
3. RESULTS
The final sample consisted of 27 CBCT images,
including 12 control subjects and 15 individuals
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THREE-DIMENSIONAL ASSESSMENT OF THE PHARYNGEAL AIRWAY AND MAXILLARY SINUS VOLUMES IN
INDIVIDUALS WITH NON-SYNDROMIC CLEFT LIP AND PALATE
with cleft lip and palate (13 UCLP and 2 BCLP).
As a result, a total number of 54 maxillary sinuses
and 27 pharyngeal airways were evaluated.
The first statistical analysis was performed to
compare the volumes of the maxillary sinuses
between the sides in the juvenile or adolescent
control and the CLP group. To this end, the
applied Student t-test showed no statistical
significant differences in any group, among the
right and left sides in the juvenile or adolescent
control group, or among the cleft and non-cleft
sides in the CLP group (p > 0.05).
The average volume of the sinuses was then
calculated, individual values being obtained for
each patient in part. As the distribution of data
was not normal, the log of these values was
calculated for statistical evaluation. Next,
ANOVA was performed to evaluate the volumes
among the groups: juvenile or adolescent control,
UCLP and BCLP. All comparisons gave
significant differences, with p < 0.0001, when the
juvenile or adolescent control group was
compared to the UCLP, and p = 0.0009,
comparatively with BCLP. The lowest volume of
the sinus was recorded in the UCLP group.
Fig. 5. Average values of the volumes of maxillary
sinuses
The airway volumes were not significantly
different in the juvenile or adolescent control and
CLP groups. The nasopharynx showed an
average volume of 6.40 cm3, with a standard
deviation of 1.2 cm3 in the juvenile CLP group
and an average volume of 4.24 cm3, with a
standard deviation of 1.8 cm3, respectively, in the
juvenile control group (Fig. 1). The nasopharynx
showed an average volume of 9.75 cm3, with a
standard deviation of 1.3 cm3 in the adolescent
International Journal of Medical Dentistry
CLP group, and an average volume of 3.83 cm3
with a standard deviation of 1.7 cm3, respectively,
in the adolescent control group (Fig. 2).
The oropharynx showed an average volume
of 5.00 cm3, with a standard deviation of 1.5 cm3
in the juvenile CLP group, and an average
volume of 8.57 cm3 with a standard deviation of
2.1 cm3, respectively, in the juvenile control
group (Fig. 3). The oropharynx showed an
average volume of 6.19 cm3 with a standard
deviation of 1.9 cm3 in the adolescent CLP group
and an average volume of 10.72 cm3 with a
standard deviation of 2.3 cm3, respectively, in the
adolescent control group (Fig. 4).
Fig. 6. Average values of the volumes of pharyngeal
airway
More specifically, the CLP and control groups
were assessed based on age. The juvenile males
with clefts had an average airway volume of 5.4
cm3 with a standard deviation of 2.1 cm3, whereas
the juvenile control males had an average volume
of 6.1 cm3, with a standard deviation of 4.1 cm3.
The juvenile females with clefts had an average
airway volume of 5.6 cm3 with a standard
deviation of 2.1 mm, while the juvenile control
females had an average airway volume of 6.3
cm3, with a standard deviation of 2.3 mm.
The adolescent males with clefts had an
average airway volume of 8.4 cm3 with a standard
deviation of 1.1 cm3, and the adolescent control
males showed an average volume of 9.1 cm3 with
a standard deviation of 2.3 cm3. The adolescent
females with clefts had an average airway volume
of 8.6 cm3 with a standard deviation of 1.1 mm,
and the adolescent control females had an
average airway volume of 9.3 cm3, with a
standard deviation of 1.3 mm.
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Ana NEMŢOI, Yllka DECOLLI, Ana Elena PETCU, Sidonia SUSANU, Simona GAVRILESCU, Alexandru NEMŢOI,
Danisia HABA
4. DISCUSSION
The goal of the study was to develop a reliable
3-D analysis to measure certain characteristics of
the pharyngeal airway in children with CLP, and
to compare the findings with a non-CLP control
group, matched as to age and sex.
The present study attempted at elucidating
the volumetric characteristics of the subjects, as
well as at comparing these findings with previous
reports that had used different methodologies to
assess this anatomic structure.
In the current study, significant differences
were found between the control and the CLP
groups, disagreeing with previous studies, that
demonstrated no differences in the structure and
development of maxillary sinuses between the
cleft palate patients and the age-matched controls
[13,15,27]. A possible explanation for the altered
volume is the fact that the maxillary sinus
develops embryonically in a different way in
cleft palate patients, comparatively with patients
with normal palate [18].
Equally, no significant differences were
recorded between the sides, or between the right
and left sides, in the control and CLP groups.
This result differs from that obtained by Hiosaka
et al., who reported larger maxillary sinuses on
the non-cleft side in patients with UCLP [17].
On the other hand, our results agree with those
of Suzuki et al. and Lee and You, who also observed
similar volumes between sides [14,27].
The hypothesis on which the present study is
based is that children with CLP had smaller
pharyngeal airways, compared to tose from the
non-CLP control group. Our data evidenced no
significant difference in pharyngeal airway
volume in CLP children, comparatively with
non-CLP children.
However, this was only a retrospective study
with sample size limited to a small number of
previously obtained scans of children with CLP.
The respiratory cycle was not controlled during the
scans. Respiration is a dynamic action that may not
be accurately depicted in a static 3-D image.
The images were taken before maxillary
expansion, so that the smaller airway volume
found in CLP children could be the result of the
absence of expansion. Future studies should
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compare the volume in different regions of the
pharynx (naso-, oro- and hypopharynx) to
elucidate precisely where the airway is larger,
and should also explore the airway length
differences between CLP and control.
5. CONCLUSIONS
Among the patients without CLP, the
oropharyngeal airway was larger in the
adolescent control than in the juvenile control
group, but no significant differences were
observed between the CLP groups. Thus, the
narrow pharyngeal airway in patients with CLP
might result in a functional impairment of
breathing in adolescent, rather than in juvenile
patients. Subjects with CLP present maxillary
sinuses with smaller volumes than the agematched control subjects.
Cone beam computed tomography can be
regarded as equivalent to CT with regard to the
diagnostic information provided for CLP
patients, yet with a considerably shorter
investigation time and lower purchase costs, as
well as lower radiation exposure. Further
investigations are necessary to clarify the
relationship between the pharyngeal structure
and airway function, and maxillary sinus
expansion in patients with CLP.
References
1. Jena AK, Singh SP, Utreja AK. Sagittal mandibular
development effects on the dimensions of the awake
pharyngeal airway passage. Angle Orthod.
2010;80:1061-7.
2. Taylor M, Hans MG, Strohl KP, Nelson S, Broadbent
BH. Soft tissue growth of the oropharynx. Angle
Orthod. 1996;66:393-400.
3. Tourn_e LPM. Growth of the pharynx and its physiologic implications. Am J Orthod Dentofacial Orthop. 1991;99:129-39.
4. MacLean JE, Hayward P, Fitzgerald DA, Waters K.
Cleft lip and/or palate and breathing during sleep.
Sleep Med Rev. 2009;13: 345-54.
5. Imamura N, Ono T, Hiyama S, Ishiwata Y, Kuroda
T. Comparison of the sizes of adenoidal tissues and
upper airways of subjects with and without cleft lip
and palate. Am J Orthod Dentofacial Orthop.
2002;122:189-94.
6. Oosterkamp BCM, Remmelink HJ, Pruim GJ,
Hoekema A, Dijkstra PU. Craniofacial,
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THREE-DIMENSIONAL ASSESSMENT OF THE PHARYNGEAL AIRWAY AND MAXILLARY SINUS VOLUMES IN
INDIVIDUALS WITH NON-SYNDROMIC CLEFT LIP AND PALATE
craniocervical, and pharyngeal morphology in bilateral cleft lip and palate and obstructive sleep apnea
patients. Cleft Palate Craniofac J. 2007;44:1-7.
7. Warren DW, Hairfield WM, Dalston ET, Sidman JD,
Pillsbury HC. Effects of cleft lip and palate on the
nasal airway in children. Arch Otolaryngol Head
Neck Surg. 1988;114:987-92.
8. Hairfield WM, Warren DW, Seaton DL. Prevalence
of mouthbreathing in cleft lip and palate. Cleft
Palate J. 1988;25:135-8.
9. Drake AF, Davis JU, Warren DW. Nasal airway size
in cleft and noncleft children. Laryngoscope.
1993;103:915-7.
10. Jaffe BF, DeBlanc CB. Sinusitis in children with cleft
lip and palate. Arch. Otolaryngol. 1971;93:479–482.
11. Ishikawa Y, Kawano M, Honjo I, Amitani R. The
cause of nasal sinusitis in patients with cleft palate.
Arch Otolaryngol Head Neck Surg. 1989;115: 442–
446.
12. Ishikawa Y, Amitani R. Nasal and paranasal sinus
disease in patients with congenital velopharyngeal
insufficiency. Arch Otolaryngol Head Neck Surg.
1994;120:861–865.
13. Suzuki H, Yamaguchi T, Furukawa M. Rhinologic
computed tomographic evaluation in patients with
cleft lip and palate. Arch Otolaryngol Head Neck
Surg. 1999;125:1000–1004.
14. Suzuki H, Yamaguchi T, Furukawa M. Maxillary
sinus development and sinusitis in patients with
cleft lip and palate. Auris Nasus Larynx. 2000;27:253–
256.
15. Robinson HE, Zerlin GK, Passy V. Maxillary sinus
development in patients with cleft palates as compared to those with normal palates. Laryngoscope.
1982;92:183–187.
16. Francis P, Raman R, Korula P, Korah I. Pneumatization of the paranasal sinuses (maxillary and frontal) in cleft lip and palate. Arch Otolaryngol Head
Neck Surg. 1990;116:920–922.
17. Hikosaka M, Nagasao T, Ogata H, Kaneko T, Kishi
K. Evaluation of maxillary sinus volume in cleft
International Journal of Medical Dentistry
alveolus patients using 3-dimensional computed
tomography. J Craniofac Surg. 2013; 24:e23–e26.
18. Kuijpers MA, Pazera A, Admiraal RJ, Berge´ SJ, Vissink A, Pazera P. Incidental findings on cone beam
computed tomography scans in cleft lip and palate
patients. Clin Oral Invest.2014; 18:1237–1244.
19. Rose E, Staats R, Thissen U, Otten JE, Schmelzeisen
R, Jonas I. Sleep-related obstructive disordered breathing in cleft palate patients after palatoplasty.
Plast Reconstr Surg.2002;110: 392-6.
20. Marcus CL. Clinical and pathophysiological aspects
of obstructive sleep apnea in children. Pediatr Pulmonol Suppl.1997;16: 123-4.
21. Martin O, Muelas L, Vinas MJ. Nasopharyngeal
cephalometric study of ideal occlusions. Am J Orthod Dentofacial Orthop.2006;130:436.e1-9.
22. Baumrind S, Frantz RC. The reliability of head film
measurements. 2. Conventional angular and linear
measures. Am J Orthod.1971;60:505-17.
23. Baccetti T, Franchi L, McNamara JJA. The cervical
vertebral maturation (CVM) method for the assessment of optimal treatment timing in dentofacial orthopedics. Semin Orthod. 2005;11:119-29.
24. Zhao Y, Nguyen M, Gohl E, Mah JK, Sameshima G,
Enciso R. Oropharyngeal airway changes after rapid
palatal expansion evaluated with cone-beam computed tomography. Am J Orthod Dentofacial
Orthop.2010;137(Suppl):S71-8.
25. Liao YF, Mars M. Long-term effects of lip repair on
dentofacial morphology in patients with unilateral
cleft lip and palate. Cleft Palate Craniofac
J.2005;42:526-32.
26. Holst AI, Holst S, Nkenke E, Fenner M, Hirschfelder
U. Vertical and sagittal growth in patients with unilateral and bilateral cleft lip and palate—a retrospective cephalometric evaluation. Cleft Palate
Craniofac J.2009;46:512-20.
27. Lee SS, You DS. Radiographic study on maxillary
sinus development and nasal septum deviation in
cleft palate patient. Korean J Oral Maxillofac Radiol.
1992;22:305–313.
231