Abstract
Introduction
Odontogenic infections affects the maxillary sinus mucosa. Cone Beam Computed Tomography (CBCT) is helpful in diagnosis of maxillary sinusitis of odontogenic origin. This cross-sectional study was planned with the aim to assess maxillary sinus changes associated with odontogenic infection by evaluating CBCT images.
Material and methods
In cross-sectional analytical study, total 213 patients (404 sinuses) were evaluated on CBCT after thorough clinical examination of the individuals and taking into consideration the history of rhino or allergic rhinitis. Based upon CBCT images and clinical examination, patients were divided into, study group (odontogenic infection) and control group (no associated odontogenic infection). Effect of the size of periapical lesion, spatial relationship of lesion to the sinus floor and periodontal bone loss on maxillary sinus changes were evaluated.
Results
Mucosal changes found in 200 sinuses (49.5%), mucosal thickening being the most prevalent and more commonly associated with odontogenic infections (p = 0.004). A significantly increased risk of mucosal thickening was observed with severe periodontal bone loss (p = 0.008). Size and spatial relationship of lesion to the maxillary sinus had no impact on the prevalence of mucosal thickening (p = 0.6, p = 0.4 respectively). Periodontal bone loss was 2.2 more likely to be associated with mucosal thickening than periapical or combined lesion.
Conclusions
Most prevalent sinus change was mucosal thickening. Periodontal bone loss was significantly associated with mucosal thickening. CBCT is an appropriate method for sinus evaluation.
Keywords: Cone Beam Computed Tomography, Maxillary sinusitis, Mucosal thickening, Odontogenic infection
1. Introduction
Maxillary sinuses are the pneumatic cavities within maxillary bone, lined by a thin membrane known as Schneiderian membrane, measuring approximately 1 mm in thickness.1 Maxillary posterior teeth lie in close proximity to the floor of the maxillary sinus. Though, sinus floor is supported by a heavy cortical bone, still the odontogenic infection from maxillary posterior teeth may irritate the sinus mucosa and subsequently leads to the changes in the sinus lining.2 Normally, sinus mucosa is not imaged radiographically but in case of the inflammation mucosa appears as non-corticated radiopaque band, along the floor and wall of sinus.3
Inflammatory mediators released by periapical and periodontal infection spread to the maxillary sinus directly or indirectly via bone marrow, blood vessels and lymphatics which subsequently leads to localized or generalized mucosal changes and mucosal sinusitis.4,5 According to the previous studies, periodontal bone loss has been found to be one of the principal cause of odontogenic maxillary sinusitis and thickening of the sinus mucosa.1,6 Hence, identification of the association between odontogenic infections and sinus pathologies is essential for the correct diagnosis and management of the patients.
Role of the radiographs in the diagnosis of odontogenic infections and maxillary sinus changes is very important. Conventional 2D radiographs have been used to assess the integrity of maxillary sinus floor and its anatomic relationship with roots of maxillary posterior teeth. Conventional radiographs being 2-D representations of 3-D structures with lot of superimpositions of the oral and maxillofacial structures makes it difficult to evaluate the relationship of roots, surrounding bone and periapical lesions with the maxillary sinus floor.7
Computed Tomography (CT) has been used as a gold standard diagnostic technique for sinus pathologies; but due to its low spatial resolution and high radiation dose to the patient it may not be an appropriate modality for diagnosis of odontogenic sinusitis.
Cone Beam Computed Tomography (CBCT), provides an accurate evaluation of maxillary sinus changes and its association with the adjacent teeth, bone and pathology without distortion and superimposition caused by teeth and surrounding structures with an additional advantage of better resolution and lower radiation exposure.1,8,9 Therefore, CBCT is the preferred modality for assessing patients who have both dental and sinus complains.
Some retrospective studies have found a significant association between mucosal thickening and odontogenic infections, but these studies lack an inclusion of control group with absence of odontogenic infections. Only one study considered the clinical symptoms while comparing the mucosal changes in maxillary sinus on CBCT.
Thus, the cross-sectional analytical study was planned with the aim to assess changes in maxillary sinus associated with the odontogenic infection by evaluating CBCT images, taking into consideration history of rhinitis or allergic sinusitis and clinically examining the patient on the day of the CBCT scan.
2. Material and methods
A cross-sectional analytical observational study was carried out on the patients who reported for CBCT for evaluation of posterior maxillary teeth or maxillary sinus for various diagnostic purposes in Department of Oral Medicine and Radiology. Ethical clearance was obtained from Institutional Ethical Committee (IEC/2019/5). Systemically healthy individuals were selected after satisfying the inclusion and exclusion criteria.
2.1. Inclusion criteria
-
1.
Patients with or without odontogenic pathologies of maxilla referred for CBCT imaging.
2.2. Exclusion criteria
-
1.
Patients who had undergone any medicinal or surgical treatment of sinusitis in past 1 year.
-
2.
Pregnant female patients
-
3
Presence of metal artefacts interfering with the view of the maxilla
-
4
Presence of trauma or pathologies like cysts, tumors, malignancy involving the maxilla
All the patients were screened for odontogenic infections by performing clinical examination and were evaluated for the history of sinusitis. CBCT scans were acquired using CS 9300 (Carestream Health Inc, Rochester NY, USA) operating at 60–90 kVp, 2–15 mA, 12–28 s acquisition time, voxel size between 90 and 300 μm and a limited field of view. Only those scans which completely displayed one or both maxillary sinuses were included in the study. 111 patients with 208 sinuses with odontogenic pathologies were allotted in the study group and 102 patients with 196 sinuses without odontogenic pathologies were allotted in the control group.
All the patients were evaluated clinically for the DMFT Index and Periodontal index while the CBCT scans were evaluated for CBCT Periapical Index, distance between the periapical pathology and the maxillary sinus floor, alveolar bone loss and sinus mucosal abnormalities.
2.3. Analysis of CBCT images
Dental imaging software 6.14.7.3 version was used for the evaluation. Multiplanar reformatted, panoramic and cross-sectional views of maxilla were used for evaluation and measurement. Both the image slice thickness and the slice interval were standardized at 1 mm 17-inch dell (intel R, Xenon R) LCD monitor with screen resolution of 1280 × 1024 was used to view under dim light condition. Density and contrast of images adjusted accordingly.
2.4. Assessment of sinus mucosal changes
The floor of maxillary sinus was traced and the total height of thickened mucosa was determined as vertical linear measurement from superior most point of mucosal thickening to the floor of the sinus. Mucosal thickening was considered to be present when the thickness of sinus mucosa was ≥ 3 mm. MS evaluation score ranged from 0 to 6 with the values interpreted as 0- no mucosal changes,1 - area without cortical bone and with soft tissue density, thickness >3 mm, parallel to sinus bone wall, 2- sinus poly, 3- antral pseudo cyst, 4- non-specific opacification, 5- periostitis, 6- antrolith.7 (Fig. 1A- 1F).
Fig. 1.
A multiplanar reformatted sagittal cone beam computed tomography images of maxillary sinus for mucosal changes showing (A) normal sinus without thickening (B) mucosal thickening >3mm (C) sinus polyp (D) antral pseudocyst (E) non specific opacifications (F) antrolith.
2.5. Assessment of periodontal bone loss and periapical lesion
All the maxillary posterior teeth were assessed for periodontal bone loss from the reconstructed panoramic and sagittal view at the mesial and distal surface of each tooth. Alveolar crest to cementoenamel junction distance of 2 mm was considered as the normal alveolar bone height. Periodontal bone loss was classified as severe, moderate or mild when at least one side of a tooth below the sinus had bone loss >50%, 25%–50% or <25% respectively.10
The presence or absence of periapical lesions was determined from the reconstructed panoramic, cross-sectional and sagittal views. A periapical lesion was recorded when the lamina dura was invisible and there was a periapical radiolucency around the root apex indicating bone destruction. A periapical lesion was considered to be present when at least one tooth below the sinus had a periapical lesion. Periapical lesions were classified according to the diameter of the hypodense area as follows- Score 0- intact periapical bone, score 1- >0.5–1 mm, score 2- >1–2 mm, score 3- >2–4 mm, score 4- >4–8 mm, score 5- >8 mm.11
The distance between the periapical lesion and the MS floor classified as 1- lesion juxtaposed to MS floor, 2- >0 mm to <2 mm and 3- ≥2 mm.7
2.6. Statistical analysis
Data was tabulated in Microsoft excel sheet and analysed using SPSS Software. The normality of distribution of data was determined using the Shapiro-Wilk test. Non parametric analyses were applied for the respective variables. The Chi square test was applied to analyse categoric data. Frequency (%) and mean ± SD of maxillary sinus abnormalities in both the groups and associations between periodontal disease, periapical lesion with mucosal thickening were assessed by using chi square test. A binary logistic regression analysis was used to determine the factors associated with the presence of maxillary sinus mucosal thickening. A p value < 0.05 was considered as significant for all outcomes.
3. Results
The CBCT images of 404 maxillary sinuses of 213 individuals (46.94% males and 53.05% females) were evaluated. In the present study, patients ranging from 15 to 88 years (mean age: 34) were included. History of rhinosinusitis or allergic sinusitis was present in 35 patients (19 in test group and 16 in control group).
3.1. Mucosal sinus changes prevalence and thickness
Among the 404 sinuses examined, 50.5% presented with no mucosal changes (mucosal thickness < 3 mm). Mucosal changes were observed in 200 sinuses (49.5%). The overall mean mucosal thickening was 6.19 ± 2.85 mm, with mean mucosal thickening of 6.35 ± 3.3 mm in study group and 6.03 ± 2.4 mm in control group (Table 1). Amongst these, mucosal thickening was the most prevalent finding (23%), followed by non-specific opacification (11.6%) and sinus polyp (7.2%) (Table 2). Intergroup comparison of sinus changes in both groups was statistically significant (p = 0.004).
Table 1.
Intergroup comparison of mean thickness of mucosal lining on CBCT.
| Group | N | Mean | Std. Deviation | P value |
|---|---|---|---|---|
| Study | 88 | 6.35 | 3.3 | 0.860 |
| Control | 60 | 6.03 | 2.4 |
Table 2.
Inter group comparison of MS evaluation score on CBCT.
| MS evaluation score |
P value | ||||||||
|---|---|---|---|---|---|---|---|---|---|
| score | 0 | 1 | 2 | 3 | 4 | 5 | 6 | ||
| Group | Test | 86 (41.3%) |
60 (28.8%) |
14 (6.7%) |
13 (6.3%) |
30 (14.4%) |
1 (0.5%) |
4 (1.9%) |
0.004* |
| Control | 118 (60.2%) |
33 (16.8%) |
15 (7.7%) |
12 (6.1%) |
17 (8.7%) |
0 (0.0%) |
1 (0.5%) |
||
| Total | 204 (50.5%) |
93 (23.0%) |
29 (7.2%) |
25 (6.2%) |
47 (11.6%) |
1 (0.2%) |
5 (1.2%) |
||
MS- maxillary sinus, *statistically significant.
3.2. Size of periapical lesion and mucosal changes
Most commonly seen periapical lesion were in size range of 0.5–1 mm (CBCTPI score = 1), followed by 1–2 mm (CBCTPI score = 2). Overall 59.8% cases with periapical lesions were associated with maxillary sinus changes (p = 0.646, Table 3).
Table 3.
Association between the size of periapical lesion and mucosal sinus abnormality on CBCT.
| Mucosal sinus thickening |
Total | P value | |||
|---|---|---|---|---|---|
| No | Yes | ||||
| CBCTPI score | 1 | 15 | 24 | 38 | 0.646 |
| 2 | 13 | 16 | 29 | ||
| 3 | 7 | 10 | 17 | ||
| 4 | 0 | 2 | 2 | ||
| Total | 35 (40.2%) |
52 (59.8%) |
87 (100.0%) |
||
CBCT PI- Cone Beam Computed Tomography periapical index.
3.3. Distance of periapical lesion from maxillary sinus and mucosal changes
The mean distance between the periapical lesion and sinus floor was 0.9 mm. Mucosal thickening was seen in 48.9% of cases when lesion was in contact with the sinus floor, in 39.1% cases when lesion was 0–2 mm away from the floor and in 33.3% when the lesion was >2 mm in distance. The results were statistically non-significant (p = 0.49, Table 4).
Table 4.
Association between the distance of periapical lesion from maxillary sinus floor and mucosal thickening on CBCT.
| Mucosal thickening |
Total | P value | |||
|---|---|---|---|---|---|
| No | Yes | ||||
| Distance of Periapical lesion from MS floor score | 1 | 25 | 24 | 49 | 0.495 |
| 2 | 14 | 9 | 23 | ||
| 3 | 10 | 5 | 15 | ||
| Total | 49 | 38 | 87 | ||
3.4. Periodontal bone loss and sinus mucosal abnormality
The association between sinus mucosal abnormality and periodontal bone loss was found to be highly statistically significant (p = 0.002, Table 5). The percentage of sinuses showing mucosal changes with mild, moderate and severe bone loss was 58.1%, 62.2% and 72% respectively. A significantly increased risk of mucosal thickening (72%) was observed when periodontal bone loss was severe (p = 0.008, Table 6).
Table 5.
Association of Mucosal Sinus abnormality with periodontal bone loss.
| Mucosal thickening absent | Mucosal thickening present | P value | |
|---|---|---|---|
| PBL No | 15 | 8 | 0.002* |
| PBL Yes | 71 | 114 | |
| Total | 86 | 152 |
PBL-periodontal bone loss, *statistically significant.
Table 6.
Association between the severity of periodontal bone loss and mucosal thickening.
| Mucosal thickening |
Total | P value | |||
|---|---|---|---|---|---|
| no | yes | ||||
| Periodontal bone loss score | 2 | 54 | 32 | 86 | 0.008* |
| 3 | 42 | 32 | 74 | ||
| 4 | 7 | 18 | 25 | ||
| Total | 103 | 82 | 185 | ||
*statistically significant.
On binary logistic regression analysis, it was found that the periodontal bone loss was 2.2 times more likely to be associated with sinus mucosal changes than periapical pathology alone or combined lesions (Table 7).
Table 7.
Association between periodontal bone loss, periapical lesion and combined lesion with mucosal changes.
| B | S.E. | Wald | df | Sig. | Exp(B) | |
|---|---|---|---|---|---|---|
| Periapical lesion | .999 | 2 | .607 | |||
| Periodontal lesion | .788 | .790 | .997 | 1 | .318 | 2.200 |
| combined | .725 | .798 | .826 | 1 | .364 | 2.065 |
| Constant | −.288 | .764 | .142 | 1 | .706 | .750 |
Binary logistic regression analysis.
4. Discussion
Pathologies involving maxillary sinus may be of odontogenic, infectious, rhinogenic, allergic, traumatic or neoplastic in origin12. In an asymptomatic individual, thickening of the sinus mucosa is evident on the routine radiographs in 8%–29% of the population.13,14 In 1943, Bauer first described the extension of periapical inflammation into maxillary sinus.4 Odontogenic diseases result in mucosal changes due to close anatomical relationship between maxillary posterior teeth and the sinus floor which have a higher prevalence of periapical lesions as well as greater susceptibility to periodontal disease.15,16 Maxillary sinus separated from teeth by the dense cortical bone which may or may not get perforated in case of odontogenic infections leading to mucosal changes. Reportedly, the most frequent alteration of the maxillary sinus is mucosal thickening followed by retention cysts and opacities.17
Many retrospective studies have been done so far to evaluate the association between the odontogenic infections and maxillary sinus abnormalities radiographically. But these studies did not consider the history of the allergic rhinosinusitis or clinical examination of the individuals. Also, there was a need to compare the radiographic changes in the sinus mucosa of patients with odontogenic etiology with those who had no odontogenic cause on clinical and radiographic examination.
Out of a total of 404 sinuses evaluated, mucosal sinus changes were present in 200 sinuses of 109 patients. In most of the previous studies, it has been seen that odontogenic sinusitis was more frequently seen in male patients.4,18, 19, 20 However, in the present study no significant difference in the distribution of gender was seen in both the groups (males 55, females-54).
All the participants in the present study recruited were above 12 years of age, as complete development of maxillary sinus occurs after the age of 12 years. The mean age of the patients was 34 years (ranging from 15 to 88), with mean age of 43 years in study group and 25 years in control group. The mean age in test group was consistent with the other studies reported in literature.7,9,10,17, 18, 19,21,22 There was significant difference in mean age in both the groups. This may be attributed to the fact that absence of periapical and periodontal disease was seen commonly in the younger age patient that constituted the control group.
Chronic rhinosinusitis can lead to decreased mucociliary clearance and hence, results in mucosal sinus epithelium changes. We found that 35 patients had a history of sinusitis (allergic or rhinitic). The distribution was however non-significant among the two groups. Hence history of sinusitis was not the confounding factor in the present study.
Mucosal thickening and mucosal cysts are the two most common findings of the maxillary sinus seen in asymptomatic individuals. The normal thickness of maxillary sinus mucosa is reported to be 0.8–1 mm.1 Various dimensions have been postulated by various authors to define mucosal thickening. This ranges from 1 mm,1,9,18 >2 mm3,6,19,23, 24, 25, 26, 27 and >3 mm7,19,21,28 by others. As most of these studies used panoramic imaging, accurate measurements of the mucosal thickness may not be possible. In the present study, changes in mucosal thickness were considered, if it was greater than 3 mm on CBCT. The mean mucosal thickness in our patients was 6.19 ± 2.85 mm with 6.35 ± 3.3 mm in study group and 6.03 ± 2.4 mm in control group. This was consistent with previous studies where mucosal thickening was found to be greater than 5 mm.1,3,18,19 Previous studies have reported the prevalence of mucosal thickening varying between 37 and 62%.3,17,18,23 In the present study, mucosal thickening was found in 23% of the patients. This lower prevalence may be because we also noted sinus poly (7.2%), antral pseudo cysts (6.2%), non-specific opacification (11.6%), periostitis (0.2%) and antrolith (1.2%) of the sinuses. So, the combined prevalence of the mucosal changes are consistent with the previous reports.7 Presence of mucosal thickening was significantly more in study group as compared to control group (p < 0.004) as patient recruited in study group had odontogenic infection.
Infected pulp releases toxins and virulence factors such as the collagenase and lysosomal enzymes which invade the periapical bone leading to the tissue breakdown and spread of infection to the maxillary sinuses and subsequently causing mucosal irritation. The majority of previous studies reported a positive association between periapical lesions and mucosal thickening.1, 2, 3,7,19,22,27 In present study, although maxillary sinus changes were more frequently seen in the patients with periapical lesions but results were not statistically significant. This observation was in concordance to the previous studies.18,23,28
On CBCT, periapical lesions are seen, as a hypodense area associated with apex of the teeth. In present study, CBCT periapical index (CBCT PI) score was used which was defined according to the diameter of the lesion.11 59.8% cases with periapical lesions had maxillary sinus changes which was consistent with the previous literature.1,4,7,17,25,28,29 However, this prevalence is less than that reported in some studies3,9,21,27,28 while it is more than that reported by few other authors.6,18,19,22, 23, 24 Few studies reported that the prevalence of maxillary sinus mucosal thickening increased with the size of the lesion.3 According to Nunes et al. when the size of periapical lesion was greater than 8 mm, all maxillary sinuses (100%) had abnormalities.7 Aksoy et al. stated that no correlation was found between the size of lesions and mucosal thickening (p = 0.64).30 Although, the present study failed to establish any correlation between the size of periapical pathology and the sinus mucosal changes, it is prudent to note that this may be due heterogeneity of the sample with regards to size of periapical pathology. We mainly had cases with a CBCTPI score of 1 and 2.
The proximity of the periapical lesions and mucosal sinus floor may be a potential factor for sinus mucosal irritation.31 Earlier studies reported that shorter the distance between periapical lesion and the maxillary sinus, greater the chances of chronic maxillary sinusitis and decrease in risk was observed as the distance increased.9,28 However, others reported no impact of proximity of the periapical lesions and mucosal thickening.3,17 In present study, the mean distance between periapical lesion and sinus floor was 0.9 mm. Among those patients with periapical lesions, 48.9% showed mucosal thickening when lesion was in contact with the sinus floor. On comparing the distance of periapical pathology from maxillary sinus and their effect on mucosal thickening, results came out to be statistically non-significant (p = 0.49). Hence, the spatial positioning of periapical lesions was not seen to have an impact upon the prevalence of mucosal thickening.
Periodontal disease may evoke irritation of the sinus mucosa, resulting in maxillary sinus thickening.32,33 Previous studies observed a resolution in the thickening of the maxillary sinus mucosa in response to a successful periodontal therapy.34,35 In our study, the frequency of occurrence of periodontal disease was 88.9%. Most common sinus change observed was mucosal thickening (28.8%) followed by the non-specific opacification (14.4%) in patients with periodontal disease. Association between mucosal sinus abnormality and periodontal bone loss was found to be highly statistically significant (p < 0.002).
Pathogenic bacteria, their products and inflammatory cytokines increased significantly at sites with severe periodontitis.18,36 We also found that the risk of mucosal sinus changes was related to degree of alveolar bone loss. An increased risk of mucosal thickening (72%) was observed when periodontal bone loss was severe. These results were similar to the previous studies.1,6,18
On applying binary logistic regression analysis, it was found that periodontal bone loss was significantly associated with mucosal thickening with an Odd's Ratio of 2.2, indicating that there is a 2.2-fold higher chance of occurrence of mucosal changes with periodontal bone loss as compared to periapical lesion or combined periapical and periodontal lesion. Previously, many studies identified the positive association between the periodontal disease and the mucosal thickening.1,6,9,18,19,21,26 In contrast Kasikcioglu et al. found an association between maxillary sinusitis and periapical lesions, with a significant OR of 2.03.22 Yoo et al. also found that the mucosal sinus thickening was higher at sites in which a tooth was extracted due to periodontal disease as compared to pulpal disease and root fracture.37 Similar to our study, their findings supported the role of periodontal disease on mucosal thickening.
The major strength of this study was that it was a Cross sectional study with a control group. Patient's history of sinusitis or medicinal treatment for sinusitis or any medical history related to sinusitis was taken into consideration. Clinical examination was done to evaluate the status of the teeth. However, the study included a small study population with heterogenous sample with respect to size of periapical lesion and severity of periodontal disease. Follow-up assessment of the changes in mucosal thickening after the treatment of periapical or periodontal lesion could not be done due to nature of the study.
5. Conclusion
Present study revealed that there is a positive correlation between odontogenic infections and sinus mucosal thickening. Sinus mucosal thickening was the most prevalent sinus abnormality seen in the odontogenic infections. Teeth with periodontal bone loss were 2.2 more likely to be associated with mucosal thickening than those with periapical or the combined lesions. Although, the size of the periapical lesion and its spatial relationship was not associated with the frequency of sinus abnormalities, severity of periodontal bone loss increased the risk of sinus mucosal changes. CBCT appears to be an appropriate imaging technique for sinus examination because of its higher resolution and lower radiation as compared to conventional CT.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Acknowledgments and disclosure statements
All authors contributed equally in the study. They have read and approved the content of the manuscript. All authors have made substantial contributions to conception and design of the study. SB, AG and AS have been involved in data collection and data analysis. SS, SB, HS have been involved in data interpretation, drafting the manuscript and AG revised it critically and have given final approval of the version to be published. Authors received no financial support for research, authorship and/or publication of this article. Authors do not have conflicts of interest.
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