Radiological Study of Maxillary Sinus using CBCT: Relationship between Mucosal Thickening and Common Anatomic Variants in Chronic Rhinosinusitis

Abstract

Introduction: Inflammatory diseases of the maxillary sinus
favour the thickening of the sinus mucosa. Therefore, it might
be possible to establish a radiological, pathological threshold
of mucosal thickening. Furthermore, there is an association
between common anatomic variants of the nose and maxillary
mucosal thickening.
Aim: To define the pathological thickening of maxillary sinus
mucosa and its association with the presence of common
anatomic variants (concha bullosa, Haller’s cell and accessory
maxillary ostium).
Materials and Methods: From March 2014 to February 2016,
Two hundred patients underwent Cone Beam Computed
Tomography (CBCT) of the paranasal sinus. We conducted
this retrospective study of total 70 patients, 34 patients i.e., a
total of 68 meatus-maxillary units (study group - those affected
by Chronic Rhinosinusitis (CRS) and another 36 patients i.e.,
a total of 72 meatus maxillary units (control group - without
symptoms of CRS). We assessed the degree of thickening of
the sinus mucosa distinguishing between ≥ 2mm or ≤ 2mm,
than we analysed the behaviour of the thickness in the study
group and in the control group. Chi-Square test was used to
compare mucosal thickening between study and control group
and the presence of some common anatomic variants or closure
of maxillary ostium.
Results: In the study group we observed a clear association
between maxillary mucosal thickening ≥ 2mm and CRS (p

Full text

Journal of Clinical and Diagnostic Research. 2016 Nov, Vol-10(11): MC07-MC10 77
DOI: 10.7860/JCDR/2016/22365.8931 Original Article
INTRODUCTION
Several authors have studied the relationship between anatomic
variants of the middle meatus and the incidence of Chronic
Rhinosinusitis (CRS) [1]. Conclusions reported by a great part of
literature are discordant. Indeed in contrast with many authors [2-6]
who assert that CRS is favored by the presence of anatomic variants,
other authors believe that CRS is not related to any anatomic variant
[1]. In order to establish the presence of a relationship between CRS
and anatomic variants, it is mandatory to establish when sinonasal
mucosal is pathological. According to Som [7] sinonasal mucosa
should not be visible and any thickening should be considered
anomalous. However, the progressive evolution of radiological
instrumentations has led to an ever greater image definition. Some
authors [8-10] have therefore, defined more precisely a threshold of
mucosal thickening above which it is correct to diagnose sinonasal
pathology. Maillet et al., defined that a mucosal thickening ≥ 2mm
is indicative of sinus inflammation [11]. In the indexed study we first
established the level of mucosal thickening associated with maxillary
sinus inflammation and then verified its effective relationship with
common anatomical variants (concha bullosa, maxillary accessory
ostium and Haller cell). Finally, we tested the relationship between
thickening of the sinus mucosa and obstruction of the maxillary
ostium.
MATERIALS AND METHODS
A retrospective study was conducted on 70 patients. All patients
came to our Rhinological Center from March 2014 to February 2016
and underwent a Cone Beam Computed Tomography (CBCT) of
the maxillary sinus by Galileos GAX9 (Sirona Dental System GmbH
Bensheim, Germany). The images were analysed by Sidexis XG
software (Sirona X-ray Imaging System Next Generation, Sirona
Dental System GmbH, Bensheim, Germany) [Table/Fig-1,2].
All patients performed a 15 days long preparatory treatment before
CBCT, using nasal washes with saline and no one was been
previously treated with vasoconstrictors. Moreover, before the
CBCT, a nasal endoscopy and a cytological analysis of the mucosa
were performed for all the patients. These assessments allowed us
to exclude patients with acute rhinosinusitis. We also excluded the
patients who were previously treated with endoscopic nasal surgery,
had allergic rhinitis, maxillary cysts, sinonasal polyposis, odontogenic
sinusitis, fungal sinusitis, sinonasal mucocele, neoplastic diseases,
Keywords: Concha bullosa, Haller cell, Inflammatory diseases, Maxillary accessory ostium, Sinus mucosa
Ear, Nose and Throat
Section
Radiological Study of Maxillary Sinus using
CBCT: Relationship between Mucosal
Thickening and Common Anatomic
Variants in Chronic Rhinosinusitis
MARCO CAPELLI1, PATRIZIA GATTI2
ABSTRACT
Introduction: Inflammatory diseases of the maxillary sinus
favour the thickening of the sinus mucosa. Therefore, it might
be possible to establish a radiological, pathological threshold
of mucosal thickening. Furthermore, there is an association
between common anatomic variants of the nose and maxillary
mucosal thickening.
Aim: To define the pathological thickening of maxillary sinus
mucosa and its association with the presence of common
anatomic variants (concha bullosa, Haller’s cell and accessory
maxillary ostium).
Materials and Methods: From March 2014 to February 2016,
Two hundred patients underwent Cone Beam Computed
Tomography (CBCT) of the paranasal sinus. We conducted
this retrospective study of total 70 patients, 34 patients i.e., a
total of 68 meatus-maxillary units (study group - those affected
by Chronic Rhinosinusitis (CRS) and another 36 patients i.e.,
a total of 72 meatus maxillary units (control group - without
symptoms of CRS). We assessed the degree of thickening of
the sinus mucosa distinguishing between ≥ 2mm or ≤ 2mm,
than we analysed the behaviour of the thickness in the study
group and in the control group. Chi-Square test was used to
compare mucosal thickening between study and control group
and the presence of some common anatomic variants or closure
of maxillary ostium.
Results: In the study group we observed a clear association
between maxillary mucosal thickening ≥ 2mm and CRS (p<0.01).
We however, observed no association between the presence
of common anatomic variations and thickening of the maxillary
mucosa and between the presence of common anatomic variations
and the study group. Instead, using a binary logistic regression,
we observed a significant association (p<0.01) between closure
of natural ostium of the maxillary sinus and mucosal thickening or
between closure of natural ostium and study group.
Conclusion: We believe that a thickening of the maxillary
mucosa ≥ 2mm and closure of natural maxillary ostium are
statistically associated with CRS. The common anatomical
variants do not seem to be associated with this condition.
[Table/Fig-1]: Measurement of mucosal thickening of maxillary sinus [facial CBCT,
coronal section]. [Table/Fig-2]: Mucosal thickening, Concha bullosa (red arrow) and
Haller’s cell (green arrow) [facial CBCT coronal section].

Marco Capelli and Patrizia Gatti, Radiological Study of Maxillary Sinus using CBCT www.jcdr.net
Journal of Clinical and Diagnostic Research. 2016 Nov, Vol-10(11): MC07-MC10
88
Age (years) n %
14 -35 18 25.71
35 -45 15 21.43
45 -60 19 27.15
60 -80 18 25.71
Mean-age (years) 45.69
Standard deviation-age (years) 15.45
Group Mucosal Thickening p-value
< 2mm ≥ 2mm
Study 4 64 < 0.01
Control 51 21
Group Concha bullosa p-value
Present Absent
Study 28 40 >0.01
Control 32 40
Accessory Ostium
Study 14 54 > 0.01
Haller’s cell
Study 31 37 > 0.01
Control 24 48
Natural sinus ostium
Study 31 37 <0.01
Control 69 3
Mucosal
Thickening (mm)
Concha bullosa p-value
Present Absent
< 2 26 29 > 0.01
≥ 2 34 51
Accessory Ostium
< 2 18 37 > 0.01
≥ 2 20 65
Haller’s cell
< 2 24 31 > 0.01
≥ 2 31 54
Natural Sinus Ostium
< 2 54 1 < 0.01
≥ 2 46 39
Mucosal Thickening Coefficient p-value
Concha bullosa
Present 0.044 > 0.01
Absent 0.0
Haller’s Cell
Present -0.641 > 0.01
Absent 0.0
Accessory Ostium
Present 0.210 > 0.01
Absent 0.0
Natural sinus ostium
Open 0.0 < 0.01
Close 3.99
Group Coefficient p-value
Concha bullosa
Present -0.336 > 0.01
Absent 0.0
Haller’s Cell
Present -0.522 > 0.01
Absent 0.0
Accessory Ostium
Present > 0.01
Absent 0.0
Natural sinus ostium
Open 0.0 <0.01
Close -3.355
[Table/Fig-3]: Sample structure by age.
[Table/Fig-4]: Chi-square test to compare mucosal thickening between study and
control group.
[Table/Fig-5]: Chi-square tests to compare anatomic variants and the natural sinus
ostium between study group and control group.
[Table/Fig-6]: Chi-square tests to compare anatomical variations between mucosal
thickening <2 and ≥2mm.
[Table/Fig-7]: Binary logistic regression between mucosal thickening and the
presence of common anatomic variants and natural sinus ostium.
Final model
0: Mucosal Thickening< 2
1: Mucosal Thickening ≥ 2
Mucosal Thickening = - 0.16 + 3.82 . Natural Sinus Ostium (Close)
[Table/Fig-8]: Binary logistic regression between the membership to a specific group
and the presence of common anatomic variants and natural sinus ostium.
Final model
0: Studygroup
1: Control group
Group = 0.8 - 3.312 . Natural Sinus Ostium (Close)
severe systemic metabolic disorders and cystic fibrosis. Thus, using
axial and coronal scans, both osteo-meatal complex together with
maxillary sinuses were analysed for a total of 140 meatus-maxillary
units.
We divided the population into two groups: the study group,
which included 34 patients (68 meatus–maxillary units) formed
by patients presenting symptoms of CRS in accordance with the
European Position Paper on Rhinosinusitis and Nasal Polyps 2012
criteria (EPOS), and the control group which included 36 patients
(72 meatus-maxillary units) formed by patients who did not present
symptoms of CRS. All patients gave their informed consent for the
examination. We evaluated in each patient the degree of thickening
of the mucosa of the maxillary sinus distinguishing between < or
≥ 2mm. We evaluated the relationship between thickening of the
maxillary mucosa and the presence of some common anatomical
variants (concha bullosa, accessory maxillary ostium and Haller cell)
and the relationship between symptoms of CRS and the presence
of those anatomic variants. Finally, we evaluated the association
between the closure of maxillary ostium and maxillary mucosal
thickening as well as the relationship between a close ostium and
CRS.
Statistical analyses were done using dedicated software programs:
MINITAB Inc. 17 and R Development Core Team (2015). A p-value
less than 0.01 were considered statistically significant in Chi-square
tests and in binary logistic regressions.
RESULTS
Of the 70, 36 were females and 34 males, aged between 14 and 80
years with a mean age of 46 years [Table/Fig-3].
Chi-square test was used to compare: the mucosal thickening
between study and control group [Table/Fig-4]; the presence of
anatomic variations (e.g., concha bullosa, Haller’s cell, accessory
ostium and natural sinus ostium) between study and control group
[Table/Fig-5] and between mucosal thickening < 2mm and ≥ 2mm
[Table/Fig-6];
A binary logistic regression was used to prove the relationship
between closed natural sinus ostium and the presence of a mucosal
thickening ≥ 2mm [Table/Fig-7] and the membership of patients to
the study group [Table/Fig-8].
In our study, we considered 140 sides (e.g., 68 from the study group
and 72 from the control group). There was a statistically significant

www.jcdr.net Marco Capelli and Patrizia Gatti, Radiological Study of Maxillary Sinus using CBCT
Journal of Clinical and Diagnostic Research. 2016 Nov, Vol-10(11): MC07-MC10 99
Anatomic
variation
Total Male Female
n % n % n %
Concha bullosa 37 52.86 19 27.15 18 25.71
Right 8 11.43 1 1.43 7 10.00
Left 6 8.57 3 4.29 3 4.29
Bilateral 23 32.86 15 21.43 8 11.43
Haller’scell 32 45.72 18 25.71 14 20.01
Right 1 1.43 1 1.43 0 0.00
Left 8 11.43 5 7.14 3 4.29
Bilateral 23 32.86 12 17.14 11 15.72
Accessory Ostium 29 41.43 13 18.57 16 22.86
Right 9 12.86 3 4.29 6 8.57
Left 11 15.71 5 7.14 6 8.57
Bilateral 9 12.86 5 7.14 4 5.72
[Table/Fig-9]: Sample structure by anatomic variants.
relationship between mucosal thickening ≥ 2mm and membership
of patients to the study group [Table/Fig-4].
Then, we analysed anatomic variations in order to determine their
effects on the severity of mucosal thickening and if the patients truly
belonged to the specific group.
The most common anatomic variant was concha bullosa, present
in 52.9% of our population, then the Haller cell (in 45.7%) and
finally the accessory maxillary ostium (41.4%). They were also
calculated for the incidence rates of anatomic variants in male and
female population and compared with each other. We did not find
statistically significant differences between genders [Table/Fig-9].
DISCUSSION
There are still many doubts about the radiological definition of
chronic maxillary rhinosinusitis. According to Som, sinus mucosa
in normal conditions should not be evident and its thickening would
be considered pathological [7]. Conversely other authors defined a
significant thickening of the sinus mucosa to be normal [12-15]. Rak
et al., stated that a mucosal thickening > 3mm can be detected in
an asymptomatic patient [12] while Phothikhun et al., concluded
that a 5mm thickness in many cases is not accompanied by clinical
manifestations [13]. We believe that a correct knowledge of the
maxillary inflammatory disease and its radiological presentation
has a clinical importance and is of fundamental importance in the
planning of certain surgical procedures such as sinus augmentation.
As for the mucosal thickening, we used the criteria of Maillet et al.,
and Lu et al., in which the thickening of the mucosa beyond 2 mm
was considered pathological [11,16]. Our data show that a maxillary
mucosal thickening ≥ 2mm is statistically associated to CRS
according to EPOS2012. We also observed a statistically significant
association between healthy patients and maxillary mucosa
thickening <2mm [Table/Fig-4]. Therefore, we had considered a
thickening of maxillary mucosa ≥ 2mm as pathological.
After establishing a pathological mucosal thickness, we evaluated the
relationship between the presence of common anatomical variants
and maxillary disease. Among the known anatomical variants we
have studied the concha bullosa, the maxillary accessory ostium
and Haller cell, because of their easily visible radiological features.
The concha bullosa was described for the first time in 1862 by
Zuckerlandl who called it a pneumatization of the middle turbinate.
Since then many authors have debated its correct definition. Some
authors define the concha bullosa as any pneumatization of middle
turbinate while others consider it a pneumatization corresponding
to 50% of the vertical diameter of the turbinate [1]. In our study,
we considered concha bullosa as any pneumatization of middle
turbinate. The incidence of concha bullosa varies widely in literature
(14-53%) [1]. In our study population, we observed an incidence of
52.9% of concha bullosa with a similar distribution between males
and females. Also the incidence of accessory maxillary ostium is
widely varied (0-43%) [17] as the incidence of the Haller cell (2-45%)
[1,2,5]. We observed an accessory maxillary ostium in 41.4% of
the population and an Haller cell in 45.7%. We did not observe a
significant prevalence according to gender [Table/Fig-9]. Results of
our study and few other authors [1,18], show that anatomic variants
analysed are not significantly associated with symptoms of CRS
[Table/Fig-8] and furthermore, they are not significantly associated
with an abnormal thickening of the maxillary mucosa [Table/Fig-7]
Finally, we observed a significant relationship between the closure of
the natural maxillary ostium, pathological thickening of the mucosa
and symptoms of CRS. These data, according to Carmeli et al.,
suggest an evident influence from natural ostium towards the status
of maxillary sinus [19]. We believe that, the ostium-infundibulum unit
should therefore, be subject to new and more extensive research
in order to understand more clearly the pathogenetic mechanisms
of chronic maxillary rhinosinusitis. According to other authors we
also emphasize the usefulness of CBCT for the radiological study of
diseases of the paranasal sinuses [20].
CONCLUSION
We conclude that in patients with CRS a mucosa maxillary
thickening ≥ 2mm, is not associated with the presence of concha
bullosa, accessory maxillary ostium and Haller cell. Finally, in patients
with CRS and pathological thickening of the maxillary mucosa we
observed an association with the closure of the natural maxillary
ostium.
ACKNOWLEDGEMENTS
Dr. Matilde Grecchi, for her contribution to the statistical analysis
and data presentation.
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Marco Capelli and Patrizia Gatti, Radiological Study of Maxillary Sinus using CBCT www.jcdr.net
Journal of Clinical and Diagnostic Research. 2016 Nov, Vol-10(11): MC07-MC10
1010
PARTICULARS OF CONTRIBUTORS:
1. Doctor, ENT Casa di Cura “Lecco”, Lecco, Italy.
2. Doctor, ENT Casa di Cura “Lecco”, Lecco, Italy.
NAME, ADDRESS, E-MAIL ID OF THE CORRESPONDING AUTHOR:
Dr. Marco Capelli,
Doctor, ENT Casa Di Cura Città Di Lecco Lecco, Lecco, Italy.
E-mail: info@otorinocremona.it
FINANCIAL OR OTHER COMPETING INTERESTS: None.
Date of Submission: Jun 28, 2016
Date of Peer Review: Aug 05, 2016
Date of Acceptance: Sep 17, 2016
Date of Publishing: Nov 01, 2016
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