Characteristics of Maxillary Sinus Ostia and Its Correlation With Anatomic Variations of the Osteomeatal Complex and Demographic Parameters Hacer Eberliköse (  hcrulutuerk@gmail.com ) Ankara Medipol University Derviş Yılmaz Gazi University Orhan Gülen Turkish Ministry of Health Research Article Keywords: Accessory maxillary ostium, Concha bullosa, Haller Cells, Septum Deviatiom primary maxillary ostium, maxillary sinus oor elevation Posted Date: August 22nd, 2022 DOI: https://doi.org/10.21203/rs.3.rs-1942452/v1 License:   This work is licensed under a Creative Commons Attribution 4.0 International License. Read Full License Page 1/15 Abstract Objectives Knowledge of the anatomy and variations of the maxillary sinus is essential for high surgery success. This retrospective study aimed to evaluate the characteristics of the primary maxillary ostium (PMO) and accessory maxillary ostium (AMO) in association with demographic and sinonasal ndings using cone beam computed tomography (CBCT) in a statistically highly reliable population. Materials and Methods The CBCT images of 385 patients were examined. The prevalence, localization, and height of PMO and AMO were evaluated with respect to sex, Schneiderian membrane (SM) thickness, concha bullosa, Haller Cells, and septal deviation. Results Analysis showed that the mean PMO diameter was 1.42 ± 0.62 mm. Although 11.6% of the PMO was in the inferior region, 60.4% was in the middle and 28% in the superior region. The mean AMO diameter was 2.55 ± 1.25 mm. Although 45.4% of the AMO was in the inferior region, 48% was in the middle and 6.6% in the superior region. Moreover, SM thickness seemed to in uence the height. Conclusion The effect of age and SM on the height and diameter of PMO was found to be statistically signi cant.A signi cant positive relationship was found between PMO and AMO height. Also, a signi cant relationship was observed between the presence of AMO and septum deviation. Clinical Relevance : The presence of AMO, PMO diameter, and height should be added to the preoperative evaluation criteria for the success of sinus oor evaluation. Especially, sinonasal and demographic conditions should be carefully examined preoperatively for the long-term success of the surgery. Introduction Dental implant treatments are a widely used and safe treatment option to achieve functional and cosmetic results [1]. However, the residual bone height in the posterior maxillae decrease after a tooth extraction is caused by alveolar remodeling and sinus pneumatization. Sinus oor elevations are one of Page 2/15 the preferred methods to increase insu cient residual bone height for restoring dentition. Prior to sinus oor elevation, the health condition of the maxillary sinus is a very critical component for long-term success. Cone beam computed tomography (CBCT) has been used in the literature for evaluating the health of the maxillary sinus region [2]. Either in ammatory diseases in dentition related to the maxillary sinus or preoperative changes in the maxillary region, such as concha bullosa (CB), Haller cells (HC), and septum deviation (SD) can lead to the disturbance in the mucociliary activity, causing the failure of dental implants after sinus oor elevation [3]. The primary maxillary ostium (PMO) is the most important anatomical structure that ensures the continuity of mucociliary activity. The PMO is usually located in the superomedial part of the medial wall of the maxillary sinus. Often, the oval-shaped PMO connects the maxillary sinus to the middle meatus of the nasal cavity. The pathological conditions around the ostium negatively affect mucociliary activity. These conditions can lead to in ammation in the maxillary sinus, causing the failure of sinus oor elevation. A second opening in the medial wall of the maxillary sinus, between the uncinate process and the inferior concha in a membranous area, is the accessory maxillary ostium (AMO)[2]. Whether AMO negatively affects maxillary sinus health is a matter of debate. On the one hand, some authors considered AMO as a predisposing factor for sinusitis because 30% of patients with chronic sinusitis have AMO. [4]On the other hand, Yeung et al. showed that AMO was an anatomic formation, with no relation with sinus pathology [2, 4]. The health status of the maxillary sinus has a close relationship with both anatomic formations[2]. For a better assessment of this critical region, a detailed examination of CBCT images with a large eld of view (FOV) before surgery makes it possible to avoid intraoperative and postoperative complications and ensure long-term success. This study aimed to examine the presence, location, and diameter of PMO and AMO using CBCT images. Besides these factors, demographic data, SM thickness, dentition, endodontic treatment, periodontal diseases, CB, SD, and HC were analyzed for possible correlations. These examinations facilitated a longterm successful treatment outcome for clinicians. Materials And Methods This retrospective study was performed on 385 CBCT images taken between December 2018 and December 2019. The radiographic images of 770 maxillary sinuses were taken from the database of a dental imaging center to evaluate anatomical structures and pathological changes in the maxillary sinus region. CBCT scans were included when both the maxillary sinus and the bilateral orbital oor were included in the radiographic image. This study was approved by the ethical review board of Gazi University and followed the Declaration of Helsinki. CBCT imaging and Analysis Page 3/15 The CBCT images were inspected with Kodak Carestream Version 3.8.6.0 on a 15.6-inch screen with 1920 × 1080 resolution in a quiet room. The images were examined at 50-min intervals for a total of 4 h each day. All images were analyzed by one examiner with 20 years of experience as a maxillofacial radiologist. After 2 weeks, 20% of the evaluation was re-evaluated. Maxillary sinuses were examined in axial, sagittal, and coronal planes, and the primary ostium was detected from the coronal images of CBCT. The medial wall of the maxillary sinuses had a trapezoidal shape with a larger posterior side and was divided into the cranial and caudal parts by the inferior turbinate [5]. In every patient, the height of the sinus was traced from the superior part of the inferior concha’s bone aspect to the highest point of the maxillary sinus on the posterior-most coronal image on which the primary maxillary sinus ostium was visible. The sinus region superior to the inferior concha was divided into three regions so that every region was one third of the sinus height from the inferior concha (inferior/middle/superior) (Fig. 1). The measurements were standardized in parallel by drawing a vertical line perpendicular to the guiding horizontal line on the CBCT image (Fig. 2). In the sagittal planes, the anterior−posterior position of the ostium was assessed in relation to the teeth, if available. Also, the distance of the open ostium was measured in millimeters (orbital inferomedial edge-uncinate prominence) on the posterior-most coronal image on which the primary maxillary sinus ostium was visible. The same measurements for the height were made for AMO (Fig. 3). The coronal slices, where the SM was observed as the thickest, were examined. SM thickness was evaluated from the maxillary sinus oor to the thickest point of the membrane. According to Soikonnen and Ainoma, SMs thicker than 5 mm were accepted as pathological[6]. The dentition type of the posterior maxillae, with the exclusion of the third molar, was recorded. Further, the status of the dentition was evaluated to account for endodontic treatment or periodontal disease that can affect the health of the maxillary sinus. HC, CB, and SD, as well as the patient-related parameters such as sex and age (at the time of CBCT), were recorded. Statistical analysis The chi-square tests and ANOVA were used to investigate the relationship and characteristics of the parameters. Cohen kappa values were evaluated for intraobserver repeatability. Results A total of 770 maxillary sinus CBCT images taken from 385 patients, aged 18–79 years, were included in the study. Also, 63% (n = 242) of the images were taken from female patients, and 37% (n = 143) of the images from male patients. Page 4/15 The intraobserver repeatability was very high in terms of the presence, height, and diameter of PMO (kappa values = 0.94, 0.89, and 0.86, respectively), and the presence, height, and diameter of AMO (kappa values = 0.94, 0.89, and 0.86, respectively). Characteristics of PMO and AMO regarding demographic data The mean score for PMO presence was 87.3% (Tables 1 and 2). Further analysis showed that the mean PMO diameter was 1.42 ± 0.62 mm. Although 11.6% of the PMO was in the inferior region, 60.4% was in the middle and 28% in the superior region (Table 1). Page 5/15 Table 1 PMO and AMO characteristics Coronal PMO POM height (n = 672) Sagittal PMO (n = 672) n % Visible 672 87.3 Obstructed 98 12.7 Inferior 78 11.6 Middle 406 60.4 Superior 188 28.0 1. Premolar (R) 14 2.1 2. Premolar(R) 120 17.9 1. Molar (R) 183 27.2 2. Molar (R) 8 1.2 1. Premolar (L) 22 3.2 2. Premolar(L) 144 21.4 1. Molar (L) 176 26.1 2. Molar (L) 5 0.7 0–7.2 1.42 ± 0.62 Visible 152 19.7 Obstructed 618 80.3 İnferior 69 45.4 Middle 73 48.0 Superior 10 6.6 0.6–9.3 2.55 ± 1.25 PMO diameter (n = 672) Min−Max, Mean ± SD Coronal AMO AMO height (n = 152) AMO diameter (n = 152) Min−Max, Mean ± SD (R), Right maxilla; (L), left maxilla. Page 6/15 Table 2 PMO and AMO in relation with potential in uencing factors Potential in uencing factors (P value) PMO patency PMO height PMO diameter AMO patency AMO height AMO diameter Age (mean) 46.66 ± 5.487 0.00a* 0.00a* 0.00a* 0.542b* 0.616b* 0.771b* Sex Female 0.003b* P = 0.00c* 0.919d* 0.702b* 0.004c* (90%) (superior) (1.457 ± 0.6061) (19%) (Middle) 0.25d* (2.703 ± 1.3277) Male (83%) (Superior) (1.447 ± 0.6082) (21%) (Middle) (2.457 ± 1.2033) Dentate 0.305a 0.788a* (29%) (4%) One tooth missing (10%) (2%) More than one (20%) (5%) Total 28% 6% Yes 0.643b* (11%) 0.450b* 0.790b* 0.419b* (64%) 0.013a* 0.846a* Dentition Endodontic treatment (23%) No Periodontal disease Periodontal healthy (26%) Periodontal disease SM thickening CB 36% Healthy (< 5 mm) 0.00a* (59%) (11%) Pathology (> 5 mm) (41%) (9%) 0.00a* 0.00a 0.00a (45%) 0.00a 0.575a* 0.407a* (14%) a, Chi-square; b, continuity correction chi-square; c, Z test; d, Mann–Whitney U, *P < 0.05. Page 7/15 Potential in uencing factors (P value) PMO patency SD 0.908b* PMO height PMO diameter AMO height AMO diameter 0.0416b* (5%) (20%) HC AMO patency 0.507b* 0.963b** (17%) (22%) a, Chi-square; b, continuity correction chi-square; c, Z test; d, Mann–Whitney U, *P < 0.05. The effect of age on the patency, height, and diameter of PMO was found to be statistically signi cant (Table 2). The P value demonstrated an opposite and weak relationship between the height of PMO and age. The sagittal position of PMO in relation to the dentition is listed in Table 1. The presence of AMO was observed in approximately 21% of male patients and 19% in female patients. The mean AMO diameter was 2.55 ± 1.25 mm. Although 45.4% of the AMO was in the inferior region, 48% was in the middle and 6.6% in the superior region (Table 1). A signi cant positive relationship was found between PMO and AMO height (P = 0.00). Dental conditions Approximately 32% of female patients and 25% of male patients had no tooth de ciency. Table 2 shows the summary statistics for dentation. Endodontic treatment was detected in 95 teeth in the examined images. A statistically signi cant relationship was not found between endodontic treatment and PMO/AMO patency, height, and diameter (Table 2). Periodontal disease was observed in approximately 16% of the maxillary sinuses examined (Table 2). The chi-square analysis revealed a statistically signi cant relationship between SM thickness and periodontal disease (P = 0.009). Sinonasal conditions The thickest membrane height of 9.431 mm was seen in the patient aged 65 years. A statistically positive relationship was observed between age and membrane thickness (P = 0.00). Also, SM thickness was observed to be severe in the absence of PMO. The statistical analysis showed a signi cant relationship between SM thickness and PMO presence, diameter, and height (P = 0.0) (Table 2). The SM was thicker in the presence of AMO. Also, a statistically signi cant relationship was observed between the height of AMO and Schneiderian membrane thickness (P = 0.013) (Table 2). Page 8/15 Interestingly, a signi cant relationship was noted between the presence of AMO and SD (Table 2). Among the 385 patients, CB was detected in 112 female patients and 68 male patients. A signi cant relationship was found between CB and PMO diameter, and SM thickness (Table 2). Discussion This study aimed to gure out both dental and sinus-related variations according to maxillary ostia in 385 patients and 770 maxillary sinuses. It also assessed the importance of PMO and AMO in oral surgeries, especially sinus lift operations. A study by Hwang et al. found that the PMO was localized 29.9 mm ± 5.1 mm above the palatal bone in the South Korean population, regardless of sex differentiation [7]. The difference between the outcomes might result from the difference in anatomical formations. The standardization of the area was di cult because of the complexity of the region. In the present study, the medial sinus wall was examined by dividing it into three parts to make more standard and comparable measurements. Hwang et al. reported that the PMO moved inferiorly and laterally as age increased [7]. The reason for the displacement of PMO was that the mid-face moved clockwise with respect to the cranial base as the age increased. However, the number of participants in different age groups should be increased to better interpret the relationship between age and PMO height. The sinus lift should be carefully evaluated, especially in elderly individuals. The results of this study showed a statistically meaningful relationship between age and PMO diameter. However, Yeung et al. did not nd any involvement between PMO diameter and age [8]. The difference between both studies might be due to the age distribution of the patient population included in the study. A statistically meaningful relationship was detected between PMO diameter and CB. The PMO diameter was found to be 1.95 mm in the presence of CB. One of the signi cant ndings of this study was that the increased PMO diameter in the presence of CB might negatively affect the air ow in the sinus. Yeung et al. reported that an obstructive PMO was more common in the case of a pathological increase in the thickness of the SM [8]. Guo et al. reported that the PMO was narrowed immediately after sinus oor augmentation surgery but returned to its baseline after 6 months [9]. Shanbag et al. stated that narrowing in the PMO was frequently found on the SM with thickness more than 10 mm [10]. A comparison of the ndings with those of other studies con rmed that sinus drainage was impaired in the absence of PMO, and therefore SM thickening occurred. In the present case, the PMO reached its maximum diameter in the presence of an SM with a thickness of more than 20 mm. The narrowing or widening of the PMO diameter, unlike its physiological width, caused similar effects on SM. Kirhene et al. stated that a widening of the maxillary ostium had negative effects because of the decrease in the nitric oxide (NO) level[11]. The decrease in the NO level caused reinfection of the sinus, and hence the SM thickness increased. One of the most important outcomes of the study Page 9/15 was that the presence of PMO decreased and the presence of AMO increased when the thickness of the SM increased. A possible explanation for this might be that sinus drainage disorder occurred with SM thickening. Another important result to mention was the relationship between PMO height and SM thickness. No studies that established a relationship between these two factors were encountered in literature reviews conducted so far. It is predicted that air circulation in the maxillary sinus is impaired with increasing the PMO height, and thus SM thickening occurs. The presence of AMO has gained importance due to the increase in surgical procedures involving the sinus area [8]. However, the ndings revealed that the SM was thicker in the presence of AMO. This situation supported the assumption that the AMO was a pathological variation rather than a physiological one. A statistically signi cant relationship was detected between SD and the presence of AMO. The study by Ozel et al. found the AMO more frequently on the side with SD [12]. The reason for this was shown as SD disrupting the air ow of the maxillary sinus and the pathological presence of AMO. PMO diameter, height, and presence of AMO should be included besides the factors to be considered before sinus lift, which Tavelli et al. listed in their systematic review in 2017. Considering the outcome observed in the present study, it was presumed that the patency and location of the PMO should be carefully evaluated before the surgical operation to prevent the obstruction of the ostium, especially when a signi cant amount of grafting was needed. Therefore, in the consensus decision published by the European Osseointegration Association in 2011, it was emphasized that expanding the FOV of the CBCT to include the osteomeatal complex is important to avoid postoperative complications [13]. Consequently, it was anticipated that a detailed and conscious examination of the surgical area with CBCT might contribute to predicting possible complications and factors to be evaluated before surgery. Considering these factors during the treatment planning phase may ensure the avoidance of complications and longterm success. Declarations All authors conceived and designed the analysis. H.E and O. G collected the data All authors performed the analysis H.E and D.y wrote the main manuscript H.E prepared the tables D.Y prepared the gures Page 10/15 All authors reviewes the manuscript Ethics Approval and Consent to Participate: Not Applicable Funding:Not funding was obtained for this study Con ict of Interest: The authors declare that they have no con ict of interest References 1. Chan HL,Wang H-L (2011) Sinus pathology and anatomy in relation to complications in lateral window sinus augmentation. Implant Dentistry 20:406–412. 2. Yeung AWK, Colsoul N, Montalvao C, Hung K, Jacobs R and Bornstein MM (2019) Visibility, location, and morphology of the primary maxillary sinus ostium and presence of accessory ostia: a retrospective analysis using cone beam computed tomography (CBCT). Clinical oral investigations:1–10. 3. Manor Y, Mardinger O, Bietlitum I, Nashef A, Nissan J and Chaushu G (2010) Late signs and symptoms of maxillary sinusitis after sinus augmentation. 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Hwang K, Wu X, Kim H and Kang YH (2018) Localization of the Maxillary Ostium in Relation to the Reduction of Depressed Nasomaxillary Fractures. Journal of Craniofacial Surgery 29:1358–1362. . AWK, Tanaka R, Khong P-L, von Arx T and Bornstein MM (2018) Frequency, location, and association with dental pathology of mucous retention cysts in the maxillary sinus. A radiographic study using cone beam computed tomography (CBCT). Clinical oral investigations 22:1175–1183. 9. Guo ZZ, Liu Y, Qin L, Song YL, Xie C and Li DH (2016) Longitudinal response of membrane thickness and ostium patency following sinus oor elevation: a prospective cohort study. Clinical oral implants research 27:724–729. 10. Shanbhag S, Karnik P, Shirke P and Shanbhag V (2014) Cone-beam computed tomographic analysis of sinus membrane thickness, ostium patency, and residual ridge heights in the posterior maxilla: implications for sinus oor elevation. Clinical oral implants research 25:755–760. Page 11/15 11. Kirihene RK, Rees G and Wormald P-J (2002) The in uence of the size of the maxillary sinus ostium on the nasal and sinus nitric oxide levels. American journal of rhinology 16:261–264. 12. Ozel HE, Ozdogan F, Esen E, Genc MG, Genc S and Selcuk A (2015) The association between septal deviation and the presence of a maxillary accessory ostium. International Forum of Allergy & Rhinology. 2015. p. 1177–1180 13. Harris D, Horner K, Gröndahl K, Jacobs R, Helmrot E, Benic GI, Bornstein MM, Dawood A and Quirynen M (2012) EAO guidelines for the use of diagnostic imaging in implant dentistry 2011. A consensus workshop organized by the European Association for Osseointegration at the Medical University of Warsaw. Clinical oral implants research 23:1243–1253. Figures Page 12/15 Figure 1 Medial wall of the maxillary sinus. Page 13/15 Figure 2 Height measurements in the coronal slices of a CBCT image [with the guiding horizontal line (a) and perpendicular vertical line (b). Page 14/15 Figure 3 Visible AMO in coronal slices of the CBCT image (*AMO). Page 15/15