Keywords cone-beam computed tomography - maxillary sinus - mucosal thickening - periapical
pathologies
Introduction
Maxillary sinusitis is a globally prevalent disease that is mainly caused by allergies
or respiratory infections.[1 ] The maxillary sinus (MS) floor extends from the first premolar to the maxillary
tuberosity but may reach the zygomatic bone, the alveolar ridge after extractions,
and the anterior canine. Due to the juxtaposition of the roots of maxillary posterior
teeth to the sinus floor, a substantial proportion of maxillary sinusitis cases has
an odontogenic origin.[2 ]
[3 ] The periapical infection has been shown to affect the sinus mucosa even without
perforation of the cortical sinus floor, with the infection spreading via bone marrow,
blood vessels, and lymphatics to the sinus. Bacteria, their toxins, and products of
pulpal necrosis may spread to the MS, and lead to inflammation.[4 ]
[5 ]
[6 ]
Normal sinus mucosa cannot be visualized on radiographs, but, when infected or due
to allergy, it may become thicker and, therefore, visible on images. Radiographic
findings are important in the diagnosis of odontogenic sinusitis. Two-dimensional
intraoral periapical (IOPA) radiograph can provide limited data on the location and
extent of periapical lesions of maxillary posterior teeth due to the superimposition
of adjacent structures such as palatal root or zygomatic bone.
Computerized tomography (CT)/multidetector CT is the gold standard diagnostic technique
for sinus pathologies; however, it may not be adequate for diagnosing maxillary sinusitis
of odontogenic origin because of its low spatial resolution.[7 ]
[8 ]
[9 ] Cone-beam computed tomographic (CBCT) imaging is beneficial for assessing the relationship
between the tooth morphology and the adjacent anatomic structures and is a valuable
technique for the evaluation of periapical lesions.[10 ] Therefore, CBCT that has a much lower radiation dose and higher spatial resolution
may be helpful for diagnosing maxillary sinusitis of odontogenic origin. Hence, in
this study, we aim to evaluate the association between maxillary posterior teeth periapical
pathologies and MS mucosal changes using CBCT images.[8 ]
Materials and Methods
This study was conducted among patients who visited the outpatient Department of Oral
Medicine and Radiology, The Oxford Dental College, Bangalore. The patients who clinically
presented with deep dental caries involving the pulp of maxillary posterior teeth
with pain and with or without associated symptoms of maxillary sinusitis (headache,
heaviness of head-on postural variations, nasal congestions) were included in this
study. One-hundred six teeth of patients who clinically presented with deep dental
caries involving the pulp of maxillary posterior teeth were enrolled in the study.
Before conducting the study, ethical clearance was obtained from the institutional
ethical board of The Oxford Dental College, and written informed consent was obtained
from the patients. After a detailed history including any history of sinusitis, the
intraoral examination was performed. The teeth with deep dental caries involving the
pulp were subjected to IOPA radiography. IOPA was performed on a conventional intraoral
machine at 70 kVp, 10 mA for 0.8 seconds. The radiograph was obtained using the bisecting
angle technique with Kodak E-speed films and was manually processed. The IOPA radiograph
was evaluated for any periapical pathology and the position of the roots of the maxillary
posterior teeth to the sinus. The patients presented with periapical pathologies were
subjected to CBCT examination.
CBCT imaging of the teeth was performed using Kodak Carestream CS 9300 system machine
set at 90 kVp, 10 mA, and 11.26 seconds with a typical voxel size of 90 μm. CS three-dimensional
imaging software was used for reconstruction and assessment. All the images were assessed
by two radiologists with varying levels of experience in reading CBCT images. The
images were assessed for the size of the periapical lesion, the presence of cortical
bone expansion or destruction, MS mucosal changes, the position of the root of the
tooth to the sinus floor, and the position of the upper edge of the lesion to the
sinus.
Before the measurements, the slice thickness of all the sections (sagittal, coronal,
and axial) of the CBCT image was adjusted to 75 μm. The periapical lesion size was
measured in all three sections (mesiodistal, bucco-palatal, and diagonal) on the CBCT
image using the working tool on the CS software. The sagittal section was used for
measuring the mesiodistal width of the lesion, and the coronal and axial sections
were used for bucco-palatal and diagonal measurements, respectively ([Fig. 1 ]). For the multirooted tooth, the lesion on all the roots was measured and the highest
measurement was considered. The periapical lesion was scored based on the CBCT-PAI
(periapical index).[11 ] The presence or absence of cortical bone expansion and destruction is inspected
in all the three sections(coronal, sagital, and axial) as shown in [Fig. 2 ].
CBCT-PAI
Score
Quantitative bone alterations in mineral structures
0
Intact periapical bone structures
1
Diameter of periapical radiolucency >0.5–1 mm
2
Diameter of periapical radiolucency >1–2 mm
3
Diameter of periapical radiolucency >2–4 mm
4
Diameter of periapical radiolucency >4–8 mm
5
Diameter of periapical radiolucency >8 mm
Score (n )
+E
Expansion of periapical cortical bone
Score (n )
+D
Destruction of periapical cortical bone
Fig. 1 Measurement of the size of periapical lesion on cone-beam computed tomography (CBCT)
image. The arrows show (A ) Mesiodistal measurement on sagittal section. (B ) Buccolingual measurement on coronal section of CBCT. (C ) Measurement of depth of periapical lesion on axial section.
Fig. 2 (A ) Sagittal section showing cortical bone destruction. (B ) Arrow shows coronal section showing cortical bone expansion.
The anatomical relationship between maxillary teeth and the sinus was determined for all the teeth ([Fig. 3 ]) and classified as[10 ]:
Type I: There was a space between the roots and the sinus floor,
Type II: At least one root of the tooth was in contact with the sinus floor,
Type III: At least one root of the tooth entered the sinus floor.
Fig. 3 Cone-beam computed tomography images showing the different anatomic relationships
between maxillary sinuses and teeth. (A ) Type 1—Presence of space between the roots and the sinus floor. (B ) Type 2—at least one root of the tooth in contact with the sinus floor. (C ) Arrow shows type 3—At least one root of the tooth into the sinus.
The relationship between the size of the upper edge of the lesion and the sinus floor
was measured in all the teeth ([Fig. 4 ]) and recorded as:
Type I: The lesion extending into the sinus
Type II: The lesion was juxtaposed to the MS floor (0 mm)
Type III: Distance from the top edge of the lesion to the sinus floor more than 0
to less than 2mm
Type IV: Distance from the top edge of the lesion to the sinus floor more than or
equal to 2mm
Fig. 4 Cone-beam computed tomography images showing the distance from the top edge of the
lesion to the floor of sinus. (A ) Type 1—The lesion extending into the sinus. (B ) Type 2—The lesion was juxtaposed to the maxillary sinus floor (0 mm). (C ) Type 3—Distance from the top edge of lesion (the arrow shows) to sinus floor more
than 0 to less than 2 mm. (D ) Type 4—Distance from the top edge of lesion to sinus floor more than or equal to
2mm.
The mucosal changes of the sinus were assessed in all three sections of the CBCT images.
The presence or absence of mucosal thickening (area without cortical bone and with
soft tissue density, thickness >3 mm, parallel to sinus bone wall)
Fig. 5 Type of mucosal thickening. The arrows show: (A ) Sagittal section showing the flat type of mucosal thickening. (B ) Sagittal section showing the polypoidal type of mucosal thickening.
Fig. 6 Coronal section showing the measurement of mucosal thickening.
Statistical Package for Social Sciences [SPSS] for Windows Version 22.0 Released 2013.
IBM Corp., Armonk, New York, United States was used to perform statistical analyses.
Chi-squared test was used to compare the cortical expansion and destruction, CBCT-PAI
scores, anatomical position of the tooth root to the sinus floor, and distance from
the tooth edge of the lesion to the sinus floor based on mucosal thickening. Similarly,
chi-squared test was also used to estimate the association between study variables
and different characteristics of sinus mucosal thickening among study subjects. The
level of significance was set at p -value less than 0.05.
Results
The study involved 19 premolars (18%) (8 on the right side and 11 on the left side)
and 87 molars (82%) (38 on the right side and 49 on the left side). In this study,
19.8% of participants were having a history of sinusitis and 99 teeth (93.4%) revealed
the presence of MS mucosal thickening. All the teeth with cortical bone destruction
(100%) and 26 teeth (78.8%) without cortical bone destruction showed the presence
of sinus mucosal thickening. This difference was statistically significant ([Table 1 ]).
Table 1
Comparison of CBCT-PAI, cortical expansion and destruction, anatomical position of
root to sinus floor, and distance from top edge of lesion to sinus floor with sinus
MT using chi-squared test
Variable
Category
MT present
MT absent
p -Value
n
%
n
%
CBCT-PAI
PAI 2
16
88.9
2
11.1
0.40
PAI 3
66
93.0
5
7.0
PAI 4
17
100.0
0
0.0
Cortical expansion
Present
15
88.2
2
11.8
0.35
Absent
84
94.4
5
5.6
Cortical destruction
Present
73
100.0
0
0.0
<0.001*
Absent
26
78.8
7
21.2
Anatomical position
Type I
21
75
7
25
<0.001*
Type II
38
100.0
0
0.0
Type III
40
100.0
0
0.0
Distance
Score 1
29
100.0
0
0.005*
Score 2
53
96.4
2
3.6
Score 3
12
80
3
20
Score 4
5
71.4
2
28.6
Abbreviations: CBCT-PAI, cone-beam computed tomography-periapical index; MT, mucosal
thickening.
* Statistically significant.
All the teeth with type II and type III anatomical position of the root to the sinus
floor showed the presence of sinus mucosal thickening (100%), whereas 75% (30) teeth
with type I anatomical position showed sinus mucosal thickening. The difference was
statistically significant with p -value less than 0.001([Table 1 ]).
In this study, all the teeth (29 teeth) with a distance from the top edge of the lesion
to the sinus floor of score 1 showed mucosal thickening (100%), whereas of score 2,
score 3 and score 4 showed 96.4%, 80%, and 71.4% of mucosal thickening, respectively.
Our study revealed that the shorter the distance of the periapical lesion to the sinus,
the higher chances of mucosal thickening and the difference was statistically significant
p = 0.005 ([Table 1 ]).
Out of 99 teeth showing the presence of MS mucosal thickening, 33 (31.1%) teeth showed
generalized mucosal thickening and 66 (62.3%) showed localized. The pattern of thickening
was flat in 69 (65.1%) teeth and polypoidal in 30 (28.3%) teeth. The grade of thickening
was moderate in 62 (58.5%) teeth and severe in 37 (34.9%) teeth ([Table 2 ]).
Table 2
Characteristics of mucosal thickening of maxillary sinus among study subjects
Variable
Category
n
%
Nature of thickening
NA
7
6.6
Generalized
33
31.1
Localized
66
62.3
Pattern
Normal
7
6.6
Flat
69
65.1
Polypoid
30
28.3
Grade
Normal
7
6.6
Moderate
62
58.5
Severe
37
34.9
Abbreviation: NA, not available.
* Statistically significant.
In this study, 69.7% of patients with PAI score 3 showed moderate mucosal thickening
as compared with 82.4% of patients with PAI score 4 that showed severe grade of thickening.
This difference was statistically significant with p -value less than 0.001 ([Table 3 ]). The anatomical position of root type II shows a significantly higher proportion
of moderate mucosal thickening (70.8%) than the anatomical position of root type III
with a severe grade of thickening (56.7%), which was statistically significant with
p -value equal to 0.03 ([Fig. 7 ]).
Table 3
Association between CBCT-PAI and characteristics of mucosal thickening using chi-squared
test
Type
CBCT-PAI
Generalized
Localized
p -Value
n
%
n
%
PAI 2
6
37.5
10
62.5
0.001[a ]
PAI 3
15
22.7
51
77.3
PAI 4
12
70.6
5
29.4
Pattern
Flat
Polypoid
PAI 2
11
68.8
5
31.3
0.87
PAI 3
47
71.2
19
28.8
PAI 4
11
64.7
6
35.3
Severity/grade
Moderate
Severe
PAI 2
13
81.3%
3
18.8%
<0.001[a ]
PAI 3
46
69.7%
20
30.3%
PAI 4
3
17.6%
14
82.4%
Abbreviation: CBCT-PAI, cone-beam computed tomography-periapical index.
a Statistically significant.
Fig. 7 Association between anatomical position of tooth root and distance of top edge of
the lesion to the sinus floor and grade of sinus mucosal thickening.
The interobserver reliability of different study variables between two observers showed
almost perfect agreement with Kappa value ranging from 0.91 to 1.00 that was statistically
significant at p -value equal to 0.001 and p -value less than 0.001([Table 4 ]).
Table 4
Interobserver reliability analysis for different study variables between two observers
using Kappa statistics
Variables
Category
Observer-1
Observer-2
Kappa value
p -Value
n
%
n
%
Mucosal thickening
Present
99
93.4
99
93.4
1.00
<0.001*
Absent
7
6.6
7
6.6
Cortical expansion
Present
17
16.0
15
14.2
0.96
<0.001*
Absent
89
84.0
91
85.8
Cortical destruction
Present
73
68.9
73
68.9
1.00
<0.001*
Absent
23
31.1
23
31.1
PAI
PAI 2
18
17.0
17
16.0
0.98
<0.001*
PAI 3
71
67.0
72
68.0
PAI 4
17
16.0
17
16.0
Anatomical positioning
Type I
28
26.4
28
26.4
0.96
<0.001*
Type II
48
45.3
46
43.4
Type III
30
28.3
32
30.2
Distance
Score 1
29
27.4
29
27.4
0.93
<0.001*
Score 2
55
51.9
53
50.0
Score 3
15
14.2
18
17.0
Score 4
7
6.5
6
5.6
Nature of thickening
NA
7
6.6
7
6.6
0.96
<0.001*
Generalized
33
31.1
30
28.3
Localized
66
62.3
69
65.1
Pattern
Normal
7
6.6
7
6.6
1.00
<0.001*
Flat
69
65.1
69
65.1
Polypoid
30
28.3
30
28.3
Grade
Normal
7
6.6
7
6.6
0.91
0.001*
Moderate
62
58.5
55
51.9
Severe
37
34.9
44
41.5
Abbreviations: NA, not available; PAI, periapical index.
Cohen's Kappa Value
≤ 0 indicates No agreement;
0.01–0.20 indicates none to slight agreement
0.21–0.40 indicates fair agreement
0.41–0.60 indicates moderate agreement
0.61–0.80 indicates substantial agreement and
0.81–1.00 indicates almost perfect agreement.
Discussion
In this study, a greater proportion (93.4%) of study participants revealed the presence
of MS mucosal thickening, and only 6.6% did not show any sinus mucosal changes. These
findings were in accordance with a study done by Shanbhag et al,[1 ] wherein a total of 243 patients, 60% prevalence of mucosal thickening was noted
and the teeth with periapical lesions were 9.75 times more likely to be associated
with mucosal thickening than those without. In another study by Lu et al[12 ] on 88 teeth with maxillary posterior teeth apical periodontitis, more than 80% had
MS mucosal thickening.
The symptoms of maxillary sinusitis include headache, heaviness of head-on postural
variation, nasal congestion, rhinorrhea, and/or foul odor and taste.[13 ] In this study, 19.8% (21) of participants gave a positive history of sinusitis among
which 95% (20) showed the presence of mucosal thickening. In most of these cases,
localized mucosal thickening (52%) was observed, whereas generalized thickening was
observed in 43% of cases with a history of sinusitis The infections of upper premolars
and molars (both periapical or periodontal) may spread beyond the supporting dental
tissues into the MS and cause sinusitis. Multiple conditions, including periapical
infection, root canal treatment, and close relationship between maxillary teeth and
sinus, may have a precursor effect on the occurrence of mucosal thickening in the
MS. After pulp necrosis, collagenase, lysosomal enzymes, and toxins produced by the
bacteria promote bacterial invasion and tissue breakdown in the periapical bone. Thus,
infections and their by-products from the teeth may spread to the MS and become a
potential cause of sinus mucosal irritation.[10 ] In this study, 100% of participants with a PAI score of 4 showed thickening of the
sinus mucosa and 93% with a score of PAI 3 showed mucosal thickening which revealed
an increase in the prevalence of mucosal thickening with an increase in the size of
periapical lesion; however, the difference was not statistically significant. Several
authors have correlated the size of the periapical lesion and mucosal thickening.
Lu et al[12 ] and Vallo et al[14 ] reported that the prevalence of MS mucosal thickening increased with the size of
the lesion. Similarly, a study by Goller-Bulut et al[15 ] on 205 patients who had 410 exposed MS reported that the mucosal thickening increased
as the degree of apical periodontitis increased. Cortical bone expansion and destruction
are the two variables in the CBCT-PAI. In our study, 88.2% of teeth with cortical
bone expansion showed the presence of mucosal thickening, whereas 100% of teeth with
cortical bone destruction were showing mucosal thickening. From the literature, the
palatal root of the maxillary first molar often penetrated into the sinus, the mesiobuccal
root of the second molar juxtaposed to the sinus, and the premolar roots seldom protruded
into the sinus cavity. This relationship may result in various risks, especially for
certain surgical procedures, such as tooth extraction and implant placement, or during
endodontic or orthodontic treatments.[16 ] In our study, 100% of participants with type II and III anatomical positions of
root to sinus showed mucosal thickening. On the contrary, a retrospective study done
by Aksoy and Orhan[9 ] concluded that the solely anatomic relationship seems not to affect the MS mucosal
thickening.
The close proximity of the periapical lesions and the MS may be a potential factor
in the thickening of the sinus mucosa. In this study, the top edge of the periapical
lesion extending into the sinus floor (100%) showed the highest number of abnormalities,
suggesting an effect of proximity of the periapical lesion on the sinus mucosa. This
was in accordance with the study done by Nunes et al,[2 ] which revealed that the highest number of abnormalities were found in association
with the teeth whose most apical lesion edge was sub adjacent to the floor of MS (distance = 0)
In contradiction, a study done by Rege et al[17 ] on 1,113 patients did not find any significant relation with the proximity of the
periapical lesion to the sinus mucosa. Similarly, a study by Lu et al[12 ] on 508 exposed sinuses did not reveal any association between periapical lesion
proximity and sinus abnormality.
Mucosal thickening can be classified as generalized and localized, flat and polypoid,[18 ]
[19 ] and moderate and severe. In our study, a higher proportion (62.3%) of localized
sinus mucosal thickening was present among the study participants. This study also
showed a variation in the prevalence of the type of mucosal thickening by the size
of the lesion. A higher proportion of PAI scores II and III (62.5% & 77.3%) showed
localized mucosal thickening, whereas PAI score IV showed generalized thickening of
mucosa (70.6%).
Polypoid lesions represent mucous retention cysts or mucosal polyps and appear as
dome-shaped radiopaque thickenings of the sinus mucosa.[20 ] A majority of the sinuses with thickened mucosa presented with a flat type of thickening
(65.1%), whereas polypoid thickening was observed less frequently (28.3%) in this
study. This finding was consistent with the study done by Shanbhag et al[1 ] and Gürhan et al.[21 ]
Most sinuses with thickened mucosa showed a moderate grade of thickening (58.5%),
whereas a severe grade of thickening was observed less frequently (37%) in this study.
The severity prevalence showed variation by the lesion's size and the anatomical position
of root to sinus. In this study, age did not influence the grade of mucosal thickening.
A higher proportion of moderate mucosal thickening was seen in anatomical position
type I and II (71.4 and 70.8%, respectively), whereas severe thickening was observed
higher in the type III anatomical position of the root, which indicates that the severity
of the thickening of the sinus mucosa increases with an increase in the size of the
lesion and close proximity of the root to the sinus floor.
The effect of the size of the periapical lesion and the spatial relationship of the
root and the top edge of the periapical lesion to the sinus floor was evaluated in
our study. However, the periodontal status of the teeth was not considered that could
cause sinus mucosal changes and this study also lacks control groups.
Conclusion
The findings of our study revealed a high prevalence of sinus mucosal thickening (93.4%,
n = 93) associated with periapical lesions. The prevalence of mucosal thickening increased
with the size of the lesion and with the presence of cortical bone destruction. A
significant increase in mucosal thickening incidence was found with the close proximity
of the root to the sinus floor. The generalized type of mucosal thickening was more
prevalent with larger periapical lesions and a significant increase in the severity
of the thickening was observed with an increase in the size of the lesion and closer
spatial relationship of the root to the sinus floor. This study also revealed the
presence of sinus mucosal thickening in the absence of symptoms of sinusitis.
The diagnosis and management of odontogenic maxillary sinusitis often present challenges.
Oral and maxillofacial radiologists play an important role in assessing the periapical
lesions and their association with sinus mucosal changes that often help otolaryngologists
in providing effective treatment. The early diagnosis and management of the periapical
lesions of maxillary posterior teeth can be helpful in preventing the spread of infection
into the MS.
