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Evaluation of Odontogenic Maxillary Sinusitis with Cone Beam Computed Tomography: A Retrospective Study with Review of Literature

Aim and Objectives: The purpose of this study was to describe the radiographic characteristics of odontogenic maxillary sinusitis as seen on cone beam computed tomography (CBCT) scans and determine whether any tooth or any tooth root, was more frequently associated with this disease. Materials and Methods: The present study included 500 CBCT images that included the entire maxillary sinus of both the sides in all the three planes. The modified classification of Abrahams and Glassberg was used to assess maxillary sinusitis of odontogenic origin. Furthermore, the proximity of the tooth root to the sinus floor, periapical pathology, and the septae within the maxillary sinus were also assessed. Results: In the present study, 1000 hemimaxillas were analyzed. Majority of the cases (74.9%) the apex of either tooth was touching the floor of the sinus. While 16.9% were in close relationship to the sinus while 8.2% of the cases, the apices were present within the sinus. Furthermore, in the present study, 38 of the total cases had an odontogenic cause of maxillary sinusitis, whereas 273 of them had a nonodontogenic cause, 96 have an undetermined cause, and the rest 593 cases had healthy sinus. Conclusion: The incidence of odontogenic sinusitis is likely under-reported in the available literature. The introduction of low-dose CBCT is particularly useful to establish a definitive diagnosis to augment in the treatment of chronic maxillary sinusitis of odontogenic origin.


Introduction
O dontogenic pain originating from the maxillary sinus can pose a diagnostic challenge for the clinician. As the roots of the maxillary posterior teeth are close to the floor of the sinus, along with common innervation, there is a probable reason for pathosis of the sinus to cause dental symptoms. [1] It is believed that the breach of the Schneiderian membrane owing to microbial incursion in periapical infections, [2] periodontal disease or iatrogenic factors [3] increases the risk of maxillary sinusitis. The progress of a periapical lesion in maxillary posterior teeth can give rise to inflammatory changes in the mucosal lining of the maxillary sinus and subsequently, sinus floor. [5] Radiographic imaging has always played an imperative role in establishing the odontogenic etiology of (mostly chronic) maxillary sinusitis and complement results of the clinical examination. [6] The purpose of this retrospective study was to describe the radiographic characteristics of odontogenic maxillary sinusitis as seen on cone beam computed tomography (CBCT) scans and to determine whether any tooth or any tooth root, was more frequently associated with this disease.

Materials and Methods
The present study included 500 CBCT images that included the entire maxillary sinus of both the sides in all the three planes. The source of data for the study was patients that reported to the department of oral medicine and radiology from January 2017 to 2018. The CBCT had been advised for the evaluation of teeth in the posterior region of maxilla for various diagnostic purposes. A prior ethical approval was obtained from the Institutional Ethical Committee (Letter No: KIIT/KIDS/IEC0345) before the start of the study. The CBCT scans were done using Hyperion X9 digital imaging system (Myray, Italy). The images were obtained at 70-75 kV, 8-10 mA, and 11-12.3 s exposure time. The field of view size was 11 mm × 8 mm with a 300-μm image resolution. For evaluation of the CBCT scans, a 21-inch LCD monitor's (HP L1910, Hewlett-Packard Development Co., Palo Alto, CA, USA) with 1280 × 1024 pixel was used. The NNT Imaging Software (v4.6) Windows edition (Myray, Italy) was used. Images were selected considering a high-level technical standard (i.e., appropriate sharpness, density, and contrast), clearly showing the maxillary posterior teeth apices and the sinuses floor. An assessment of the topographic relationship of each root to the maxillary sinus floor was conducted in CBCT images.
For the purpose of this study, diagnostic criteria for sinusitis diagnosis were developed based on published literature. [7] Based on these criteria, the maxillary sinusitis/pathology was divided into four categories [ Figures 1-6].
The relationship of the tooth apex to the floor of the maxillary sinus and periapical lesion to the floor of the maxillary sinus is depicted in Figure 1.

Results
In the present study, 1000 hemimaxillas were analyzed. A total of 500 participants including 314 males and 186 females participated in the study. All the participants in the present study were adults and were between the ages of 25-65 years. In the present study, descriptive statistics was used to summarize the features of odontogenic and nonodontogenic sinusitis. Statistical Package for the Social Sciences (SPSS; IBM, California, USA) version 20.0 was used to perform the statistical analysis. Student's t-test was used to assess the relation (P < 0.05 was considered to be statistically In general, the apices of premolars and molars are in close proximity to the floor of the maxillary sinus. Majority of the cases (74.9%), the apex of either tooth was touching the floor of the sinus. A total of 16.9% of the cases had a close relationship to the sinus while 8.2% of the cases the apices were present within the sinus [ Table 1]. In the present study, out of the 1000 maxillary sinus, 606 were healthy, 387 had sinusitis, six had mucous retention cyst, and only one participant had calcification within the maxillary sinus [ Table 2]. On the other hand, out of the 1000 hemimaxillas, 671 cases had healthy teeth while 139 (out of 1000) had a history of extraction done of which 69 cases had healthy sinus whereas 70 of them had sinus pathology. Fifty-eight (out of 1000) had a history of root canal treatment done in which the ratio of healthy and diseased sinus was equal. Sixty (out of 1000) had periodontitis out of which only nine cases had healthy sinus, while the others had diseased sinus. Seventeen (out of 1000) had periapical pathology out of which only three had a healthy sinus while the rest 14 had diseased sinus. Forty-seven (out of 1000) had carious teeth with no periapical pathology out of which 21 had a healthy sinus whereas 26 had diseased sinus. Similarly, eight (out of 1000) had restorations done in the teeth out of which seven had healthy sinus whereas only one had a diseased sinus [ Table 3].
Interestingly, majority of the cases having either periodontitis or periapical pathology had sinus pathology.
Majority of the cases 749 (out of 1000) the apices of the teeth were touching the sinus floor of which 294 had a sinus pathology whereas 455 were normal. Similarly, 82 (out of 1000) of the cases had the apices of the teeth within the sinus cavity of which 44 had sinus pathologies while 38 were healthy [ Table 4].
Out of the 1000 hemimaxillas, 361 had periapical pathology. In 270 (out of 361) cases, the periapical    lesion was in close proximity to the sinus of which 125 had no sinus pathology while 145 had diseased sinus. In 54 (out of 361) cases, the periapical lesion was touching the floor of the maxillary sinus of which 18 had no sinus pathology while 36 had diseased sinus. Similarly, in 37 (out of 361) cases, the periapical lesion was present within the maxillary sinus of which only 10 had a healthy sinus while 27 had diseased sinus [ Table 5].

Discussion
An extensive search for various articles was done through Google Scholar, PubMed, Cochrane Library, and EMBASE. It included all articles published between the year 2000 and 2018. The keywords used were "odontogenic sinusitis," "chronic maxillary sinusitis," "sinusitis of dental origin," "sinusitis of undetermined origin," "chronic apical periodontitis," "periapical pathology and sinusitis," and "iatrogenic sinusitis." All the articles including case reports, case series, review, retrospective, and prospective studies were sorted out to gather all descriptions regarding odontogenic cause of maxillary sinusitis, and the type of imaging modality used  [ Table 6 ].
In the present study, the incidence of odontogenic-related sinusitis was more commonly seen in males than in females. This was in accordance with the study done by Vallo et al. [32] All the participants in the present study were above 12 years of age, as the       maxillary sinus is not completely developed before the age of 12 years. [33] Two-dimensional (2D) imaging has a very limited diagnostic value in identifying maxillary sinusitis because the radiologic signs are nonspecific. Carious lesions and periapical radiolucencies can be appreciated in Intraoral Periapical Radiograph (IOPAR) because periapical radiograph has a higher spatial resolution. [34] However, such lesions must attain considerable size to be seen periapical radiograph. [35,36] Whereas panoramic radiographs have a lower sensitivity than IOPAR in identifying periapical lesions. [37] 3D-computed tomography is considered to be the most acceptable method for visualization of nasal and paranasal sinuses. As it has a higher contrast resolution and eliminates, the superposition of anatomical structures. [38] Thus, 2D imaging is of little or no use for accurate morphometric assessment. [39] 3D-imaging overcomes the 2D limitations by providing multiplanar views with no magnifications, superimpositions, and distortions. [40] Panoramic studies have demonstrated the root-maxillary sinus relationship in 39%-57% of the cases. [41,42] With due advancement in 3D imaging the prevalence of root apices protruding into the maxillary sinus ranges from 5% to 10%. [24,39,40] In the present study, when the tip of tooth root was in contact with the floor of maxillary sinus, the incidence of mucosal thickening was lower than when the tip of root exceeded and protruded within the floor of the maxillary sinus. This finding was in accordance with the study done by Lu et al. [11] There is histological evidence of a thin cortical bone surrounding the maxillary sinus with perforation present in 14%-28% of the cases. [41] Due to this perforation or absence of thin layers of cortical bone, the periodontal tissues are in direct contact with the maxillary sinus mucosa. The knowledge of which is essential for planning dental treatment. Many researchers have found out that an odontogenic irritation may be potentially influenced by the proximity between roots of the teeth with periapical lesions and floor of sinus. [32,43,44] CBCT increases the accuracy of detecting periapical lesions when compared to conventional imaging modalities. [36,45] However, the interpretation of CBCT must be carried out cautiously as incipient and chronic periapical lesions detected by a CBCT examination might present low potential for identifying sinus inflammatory signs and symptoms. CBCT is far superior to multislice CT in terms of image resolutions, as thinner sections can be achieved. Apart from that CBCT equipment have reduced radiation exposures and a low equipment cost when compared to multi-slice CT. [10] Some studies have shown that the root of the 2 nd maxillary molar is closest to sinus. [36,46] It was found out that Mesio-Buccal root of maxillary 2 nd molar is on average 0.67 mm closer to the sinus than the palatal root of maxillary 1 st molar. [39] This finding was consistent with the present study as well. On the contrary, it is the palatal root of the maxillary 1 st molar that is most commonly associated with maxillary sinusitis as it is the first permanent maxillary molar to erupt into the oral cavity. [8,47] Distinguishing a healthy and a diseased sinus radiographically is not so problematic keeping into consideration its shape, loci, and lobulations. Because the sinus it is air-filled, the sinus appears radiolucent and has clearly defined margins. [4] In case of diseased sinus; a clinician may easily identify clouding (opacifications), mucosal thickening and or accumulation of fluid. [48] Previous studies have suggested the thickness of the mucosal lining of the sinus to be in the range from 2 to 6 mm. [32,47,[49][50][51][52] However, the study done by Maillet et al., the average amount of mucosal thickening was 7.4 mm. [9] The current investigation was a retrospective study of existing scans only and did not include patient symptoms, or the reasons for the referral for CBCT scans. Maillet et al. in their study found 75% prevalence of maxillary sinusitis associated with dental conditions. [9] According to previous studies, there is a definitive odontogenic cause for diseased maxillary sinus of which apical periodontitis accounts for 83% of all cases. Furthermore, the prevalence of other sinus disorders such as mucosal thickening, mucous retention cyst, and odontogenic maxillary sinusitis ranges from 8% to 29%, 2%-36%, and 10%-86%, respectively. [53][54][55][56]   The detection rate of mucosal thickening was significantly higher in the Implant group than in the nonimplant group. The detection rates for the features analyzed were significantly lower on panoramic radiographs Contd... There is a moderate risk for false diagnosis of findings of the maxillary sinus if only panoramic radiography is used. Based on the ten predefined conditions, solely maxillary bone cysts penetrating into the sinus were frequently detected differently comparing 2D-3D diagnostics. Additionally, on panoramic radiographs, the inter-observer comparison demonstrated that basal septa were significantly often rated differently and the intra-observer comparison showed a significant lack in reliability in detecting maxillary bone cysts penetrating into the sinus Contd...  [57] In addition, in previous studies, the prevalence of flat mucosal thickening of the maxillary sinus ranged from 23.7% to 38.1%, polypoid mucosal thickening ranged from 6.5% to 19.4%, acute maxillary sinusitis 3.6%, partial opacification of maxillary sinus 12%, and total opacification of maxillary sinus 7%, respectively. [58,59] Several authors have reported that around 10%-12% of the total maxillary sinus pathology has an odontogenic cause. [4,50,60] In the present study, 51.8% of the participants had odontogenic sinusitis, whereas 65.4% of the total participants had a diseased maxillary sinus along with periapical lesions. This was in accordance with the previously computed tomography studies that demonstrated around 71%-86% of sinus infections have an odontogenic cause. [47] Several studies have reported a great variability in the prevalence of incidental findings in the maxillary sinus of asymptomatic subjects when multiplanar images are used. Multislice CT scan studies have found abnormalities in the maxillary sinus in 30% of the cases. [61,62] Whereas, CBCT studies have found abnormalities in maxillary sinus in 24.6% to 56.3% of the cases. [57][58][59] In the present study, the prevalence of abnormalities in the maxillary sinus was 39.4% which was in accordance with the previous studies. However, a study done by Rege et al. the prevalence was as high as 68.3%. [12] The discrepancy could be due to the sampling criteria selected for the study, the study design, variations in image interpretation, diagnostic criteria for maxillary sinusitis, and the influence of the climate in different geographical areas. [63,64]

Conclusion
The incidence of odontogenic sinusitis is likely under-reported in the available literature. Radiographic analysis plays a pivotal role in the diagnosis of odontogenic sinusitis. It has been established in the published literature that 2D-imaging modalities may obscure the origin of odontogenic maxillary sinusitis. The introduction of low-dose CBCT is particularly useful to establish a definitive diagnosis to augment in the treatment of chronic maxillary sinusitis of odontogenic origin. Retrospective Literature Odontogenic sinusitis is an inflammatory condition of the paranasal sinuses that is the result of dental pathology, most often resulting from prior dentoalveolar procedures, infections of maxillary dentition, or maxillary dental trauma CBCT=Cone beam computed tomography, OP/OPG/PAN=Panoramic radiography, CT/CT Scan=Conventional computed tomography, EPT=Electric pulp testing, IOPA=Intraoral periapical radiograph, MSDO=Maxillary sinus disorders