Association between odontogenic factors and maxillary sinus mucosal characteristics: a retrospective CBCT study

Association between odontogenic factors and maxillary sinus mucosal characteristics: a retrospective CBCT study | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Association between odontogenic factors and maxillary sinus mucosal characteristics: a retrospective CBCT study Ming Liu, Taiwei Lin, Wenqin Chen, Yixuan Wu, Yi Zhang, Zhisheng Zhang, and 1 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-6491416/v1 This work is licensed under a CC BY 4.0 License Status: Under Review Version 1 posted 11 You are reading this latest preprint version Abstract Objectives The aim of this study was to investigate the effects of various dental and maxillary sinus (MS) variables on mucosal characteristics (MC), including maxillary sinus mucosal thickness (MT) and mucosal appearance (MA), using cone-beam computed tomography (CBCT) imaging. Materials and methods CBCT images of the MS (n=249) were reviewed from a total of 16439 patients who had undergone CBCT examinations for various dentomaxillofacial issues, leading to the identification and confirmation of odontogenic maxillary sinusitis (OMS). The MT and the distances between the maxillary sinus floor (MSF) and both the root apex and periapical lesion (PALs) were measured. The MA and situations of adjacent teeth were recorded. The relationships between these odontogenic factors and MC (including MT and MA) were evaluated. The data were analyzed using analysis of variance, χ2-test, and logistic regression. Results A total of 249 CBCT images exhibited OMS with specific mucosal characteristics. MT was significantly correlated with gender, tooth type, the distance between the root apex and the MSF, and the distance between the PALs and the MSF, whereas MA was significantly associated with all these above factors except gender. (P＜0.05). A logistic regression model showed that the severity of MT hyperplasia was significantly associated with male sex (OR: 2.441, 95% CI: 1.225 ~ 4.863, P 10 mm. (PALs: OR = 0.161 and 0.089, P < 0.05; root apex: OR = 0.212, P < 0.005). Conclusions Multiple factors, including gender, periapical infection, and the distance between the MSF and PALs/root apex, may have a precursor effect on the occurrence of MT and MA in the maxillary sinus. The severity of MT was significantly associated with male sex and the distance between the MSF and PALs/root apex. Odontogenic diseases represent significant risk factors for the development of maxillary sinus infections and should therefore be carefully considered by both dental and medical professionals in the comprehensive assessment and management of maxillary sinus lesions. Therefore, communication between dental surgeons and an otolaryngology specialist is important for the timely diagnosis and treatment of MT of dental origin. Clinical relevance The maxillary sinuses are notably affected by a range of odontogenic factors—such as patient gender, the proximity of the maxillary sinus floor (MSF) to the root apex or periapical lesion (PAL), and the type of tooth involved—all of which may play a contributory role in alterations of mucosal thickening (MT) and maxillary sinus anatomy (MA). Odontogenic conditions Maxillary sinus mucosal thickening Maxillary sinus mucosal appearance Cone-Beam Computed Tomography Figures Figure 1 Figure 2 Figure 3 1. Introduction The maxillary sinus (MS), a pyramid-shaped, air-filled cavity located within the maxillary bone, is uniquely susceptible to oral pathogenic microorganisms due to its close anatomical relationship with the roots of the maxillary molars and premolars. This proximity renders the MS more vulnerable to odontogenic infections than other paranasal sinuses. [ 1 ]. Odontogenic factors are reported to account for approximately 12% of maxillary sinusitis cases [ 2 ]. According to recent studies, Endodontic and periodontal infections are recognized as the main causes for odontogenic maxillary sinusitis (OMS), including apical periodontitis, endo-perio lesions, radicular cysts and periodontitis [ 3 , 4 ]. Although dental implants and endodontic material can also impinge on maxillary sinuses, these are considered rare causes of sinusitis [ 5 ]. The lining of the MS is composed of a mucous membrane that includes a pseudo-stratified epithelium with goblet cells, lamina propria, and periosteum-like structures [ 6 ]. This membrane, also known as the Schneiderian membrane, is highly susceptible to odontogenic infections [ 7 ]. The Schneiderian membrane is difficult to clearly delineate on Cone Beam Computed Tomography (CBCT) scans. Under physiological conditions, its thickness averages approximately 0.30 ± 0.17 mm; however, in the presence of infection or inflammation, this thickness may increase more than 10 times, indicating significant mucosal hypertrophy [ 8 ]. The diagnosis of OMS is relatively complex and subject to some controversy, requiring a combination of clinical and imaging assessments for accuracy. CBCT is the most reliable tool for the evaluation of structures within and adjacent to the MS, primarily since this technique provides three-dimensional imaging and, in certain cases, facilitates the evaluation of soft tissues [ 9 , 10 ]. A normal maxillary sinus is typically defined by the absence of detectable mucosal thickening (MT) or by a uniform MT measuring less than 2 mm, as observed on radiographic imaging (Fig. 1 A) [ 11 ]. Odontogenic maxillary sinusitis (OMS) is characterized by the presence of a localized soft tissue density within the sinus, with MT ≥ 2 mm, anatomically correlated with a tooth affected by pathological conditions such as dental caries, defective restorations, periapical lesions (PALs), or post-extraction changes [ 12 ]. However, the radiographic evaluation of the Schneiderian membrane and its association with odontogenic conditions remains a topic of ongoing debate. The presence and extent of mucosal thickening do not consistently correspond to underlying pathology, making it challenging to differentiate between physiological variations and pathological changes based solely on imaging findings. Aksoy et al. [ 13 ] found that the incidence of maxillary sinus mucosal thickening and maxillary sinus cysts was higher in male patients than in females. However, Zhang et al. [ 14 ] reported that there was no statistically significant difference in Schneiderian membrane thickening between genders. Moreover, most studies primarily focus on the association of mucosal thickening (MT) while overlooking mucosal appearance (MA) [ 15 – 17 ]. Therefore, this retrospective and cross-sectional study aimed to determine the association between the various odontogenic factors (including odontogenic diseases, tooth type, and the distance between the MSF and the PALs/root apex, etc.) in posterior maxillary area and the presence of maxillary sinus MT and MA using CBCT. 2. Material and methods 2.1. Subjects The clinical operation involved in this case was told to the patients and got the informed consent from the patients in accordance with the Declaration of Helsinki, and totally approved by the Ethics Committee of Stomatological Hospital of Xiamen Medical College. A total of 16,439 patients who underwent comprehensive maxillary Cone Beam Computed Tomography (CBCT) scans between January 2024 and December 2024 were initially considered for inclusion. Ultimately, 249 patients (aged 18–75 years, mean age 41.1 ± 13.92) were selected, all of whom demonstrated evidence of sinus changes in one or both maxillary sinuses. The study protocol adhered to the principles outlined in the Declaration of Helsinki, including all subsequent amendments and revisions. The selection and collection of data from patients' clinical histories were governed by the following inclusion criteria: (1) patients aged 18 years or older; (2) availability of complete maxillary CBCT scans, including panoramic, axial, and ortho-radial sections; (3) the presence of sinus membrane thickening in one or both maxillary sinuses; (4) evidence of periapical radiolucency, periodontitis, endo-perio lesions, or radicular cysts. Exclusion criteria included: (1) nasal symptoms (congestion, rhinorrhea, fever) within the past three months; (2) radiographic evidence of maxillary sinus cysts or sinusitis; (3) history of maxillofacial trauma, missing teeth, or dental implants in the posterior maxilla; (4) maxillofacial surgery within the past three months 2.2. Research methods CBCT images of 249 patients (115 females and 134 males; aged 18–75 years) meeting the inclusion and exclusion criteria were included in the study. The CBCT scans were acquired using a 12*8cm /15*15cm field of view (NewTom VGI, Quantitative Radiology s.r.l., Verona, Italy) to capture the maxillary anatomy. The unit operated at a fixed 110 kVp setting, with automated milliampere adjustments and a scan time of 36 seconds, producing 0.3-mm-thick axial slices with isotropic voxels. All measurements and analyses were jointly conducted by trained radiologists and endodontists proficient in using NNT analysis software (NNT 7.2.0, QR NewTom, Quantitative Radiology s.r.l., Verona, Italy). The software was used to reconstruct axial, coronal, and cross-sectional images for the assessment of the maxillary sinuses and their anatomical relationship with adjacent maxillary teeth. For each patient, CBCT measurements were performed three times, and the mean value was recorded as the result. 2.3. Assessment of MT Mucosal thickening (MT) was measured on coronal and sagittal CBCT sections at the point of greatest thickness from the maxillary sinus floor (MSF) to the highest point of the thickened mucosa, then recorded and classified as (Fig. 1 ) Grade 1: 2 to 10 mm (Moderate Schneiderian membrane thickening, Fig. B1 and B2) Grade 2: > 10 mm (Severe Schneiderian membrane thickening, Fig. C1 and C2) 2.4. Assessment of MA MA in the maxillary sinuses on CBCT scans were evaluated on the coronal and sagittal sections of CBCT scans and classified as (Fig. 1 ) Grade 1: Flat thickening. (Fig. D1 and D2) Grade 2: Polypoid thickening. (Fig. E1 and E2) Grade 3: Occluded (acute maxillary sinusitis). (Fig. F1 and F2) 2.5. Assessment of the periapical status The presence of premolars/molars and periapical lesions (PALs) in the posterior maxilla was documented. PALs were identified by loss or irregularity of the lamina dura with periapical radiolucency suggestive of bone destruction. In cases with multiple lesions, only the one in closest proximity to the sinus was recorded. The following parameters were used to evaluate the CBCT images: ● Tooth type (premolar / molar) ● Odontogenic diseases (Apical Periodontitis, Endo-perio lesion, Radicular cysts and Peri-odontitis) ● Distance between the root apex and MSF ● Distance between PALs and the MSF 2.5. 1. Distance between root apex and MSF The distance between MSF and the root apex was determined and recorded in the sagittal and coronal views for each tooth individually and classified as (Fig. 2 ) Type 1: Root apex protrudes into the MSF. (Fig. A1 and A2) Type 2: Root apex is in contact with the MSF (Fig. B1 and B2) Type 3: Root apex is near the MSF. (Fig. C1 and C2) 2.5. 2. Distance between PALs and MSF A periapical lesion (PAL) was defined as a radiolucency at the root apex with a thickness of ≥ 0.5 mm (at least twice the normal width of the periodontal ligament) on sagittal and coronal CBCT sections [ 18 ]. The shortest distance from the apex of the lesion to the maxillary sinus floor (MSF) was measured and classified as (Fig. 3 ) Type 1: 0.5–1 mm;(Fig. A1 and A2) Type 2: 1–2 mm;(Fig. B1 and B2) Type 3: >2 mm;(Fig. C1 and C2) 2 .6 Statistical analysis Pearson’s correlation analysis revealed strong intra- and inter-observer agreement for repeated measurements of membrane thickness and the distance between PALs and the MSF (r = 0.95 and r = 0.93, respectively). Maxillary sinus anatomy (MA) assessments were conducted independently, with discrepancies resolved through consensus. Statistical analysis was performed using IBM SPSS Statistics for Windows (Version 24.0, IBM Corp., Armonk, NY, USA). Group comparisons were conducted using the chi-squared test. Potential factors associated with MT were evaluated using multivariate binary logistic regression. A p-value < 0.05 was considered statistically significant. 3. Result 3.1. Prevalence of MT and MA Among the 249 patients with maxillary sinus mucosal thickening more than 2mm, 199 patients (79.9%) were associated with sinus mucosal thickening classified as Grade 1 (2 to 10 mm) while 50 patients had mucosal thickening greater than 10mm (Grade 2), accounting for 20.1% (Table 1). According to the MA, 65.9% of patients (164/249) had flat thickening, 22.1% (55/249) had polypoid thickening, and 12.0% (30/249) had occluded thickening (Table 2). 3.2. Mucosal Characteristics and Its Associated Factors Analysis The distribution of mucosal characteristics (MC) in maxillary sinusitis, including MT and MA, based on dental findings, is presented in Table 1 and Table 2. 3.2.1 Association between Age, Gender and MC Among the 249 patients, 115 (46.2%) were female, and 134 (53.8%) were male. The patients were divided into three age groups: one group for patients aged 18-35 years, another for those aged 35-50 years, and a third group for patients over 50 years of age. There was no statistically significant association between age and MT (P>0.05), but a significant correlation was found between gender and MT (P＜0.05) (Table 1). There was no statistically significant difference between age and gender in terms of magnitude of change of the MA (P＞0.05) (Table 2). 3.2.2 Anatomic relationship between tooth and MC Out of 16439 patients, 249 cases (1.5%) of maxillary sinus mucosal thickness were identified. The most affected teeth were maxillary first molars (MFM) (59.4%), maxillary second molar (MSM) (30.5%) and premolars (10.1%) respectively. But there was no significant association between the tooth type and MT (p＞0.05). Among these teeth, 72.7% of root apices protrude into MSF. As the distance between the root apex and the MSF increased, a significant association was observed between the distance and MT (p＜0.05) (Table 1). Both the tooth type and the distance between the root apex and MSF were associated with the MA (P＜0.05). The flat mucosal thickening of the maxillary sinus occurred most frequently in the MFM (77.7%). Moreover, an anatomical relationship where the root apex protrudes into the MSF (68.5%) was most closely associated with flat mucosal thickening (Table 2). 3.2.3. Association between Odontogenic disease, PALs and MC In the cases of MT, the prevalence of apical periodontitis was significantly higher (53.8%). Among the 249 patients, Grade 1 mucosal thickening (2 to 10 mm, moderate mucosal thickening) accounted for 79.9% (119/249), while flat mucosal thickening accounted for 65.9% (164/249). However, no significant correlation was found between the type of odontogenic disease and MT or MA (Table 1 and 2). Among these cases (Type 1 distance of the PALs to MSF), Grade 1 MT accounted for 75.1% (142/189), while flat mucosal thickening accounted for 59.3% (112/189). The distance between the PALs and MSF was significantly correlated with MT (P = 0.04) and MA (P = 0.002) (Table 1 and 2). 3.3. Binary Logistic Regression Analysis of Factors Influencing MT The binary logistic regression analysis indicated that male sex, types 2 (considering distance between the root apex and MSF), and distance of the PALs to MSF were significant associated with the severity of MT. The ORs and 95% CIs for these associations are shown in Tables 3. The severity of MT was significantly associated with male sex (OR = 2.441, P = 0.011). Patients with root apex in contact with the MSF (type 2) demonstrated a significant negative impact on MT, with a 0.212 times lower risk of increasing the MT severity compared to those with root apex extending into the MSF (type 1). Furthermore, patients with Type 2 (PALs located 1–2 mm from the MSF) and Type 3 (PALs located >2 mm from the MSF) also exhibited a significant negative impact on the MT. They were at a reduced risk of increasing the severity of MT by 0.161 and 0.089 times, respectively, compared to patients with PALs located 0.5–1 mm from the MSF (Type 1). 4. Discussion This study aimed to evaluate the effects of various odontogenic factors on MT and MA, which may contribute to the etiology of OMS. Accurately identifying the etiological factors of OMS is crucial for selecting the most appropriate treatment and preventing future cases [ 19 ]. While CT is regarded as the gold standard for imaging maxillary sinusitis, in this study, CBCT was utilized to assess the maxillary sinuses due to its lower radiation dose, higher resolution, and shorter screening time [ 20 , 21 ]. In the literature, odontogenic diseases [ 22 , 11 ];presence [ 22 , 4 , 23 ] and proximity [ 21 , 24 – 26 ] of PALs; and distance between root apex and MSF [ 27 – 29 ] have been evaluated for their possible influence on MS. Ince Yusufoglu et al. [ 30 ] reported a prevalence rate of MT (Moderate Schneiderian membrane thickening, Grade 1) in OMS of 87.3%. In our study, a relatively lower prevalence of Grade 1 (79.9%) was observed. This discrepancy between studies may be attributable to using different diagnostic criteria (2-10mm, >10mm) for assessing the pathological radiographic mucosal thickening in the study. Other explanations are probably due to the difference in the indication of CBCT scans, which were included in the study and sample size among the populations studied. Gender had no effect on the MA; however, a statistically significant correlation was observed in the MT. The findings of this study are consistent with those reported by Van et al [ 31 ]. Moreover, previous studies have established a positive correlation between sinusitis and smoking [ 32 ]. The higher proportion of male patients who smoke may also contribute to the observed differences. This outcome may be explained by the inclusion of smokers in the study population, rather than their exclusion [ 17 ]. In the literature on odontogenic diseases, the prevalence of PALs observed in our study is generally consistent with findings reported in previous studies. According to Goller-Bulut et al. [ 25 ], MFMs exhibited the highest prevalence of apical periodontitis among all affected teeth, indicating their significant association with periapical pathology. Shanbhag et al. and Maillet et al. [ 33 , 34 ] both identified the MFM as the most affected tooth and the leading cause of OMS, followed by the MSM. The higher prevalence of pathology in MFMs and MSMs may be attributed to their increased susceptibility to dental caries and pulpal disease [ 26 ]. The distance between the root apex and MSF is of significant clinical importance, as it can lead to various complications, including sinusitis, oroantral fistula formation, and the displacement of roots or materials into the MS [ 35 ]. In a recent study, Chand et al. [ 36 ] suggested that the transmission of microorganisms or toxins to the Schneiderian membrane from the lesion depends on the thickness of the remaining alveolar bone beneath the MS. This finding suggests that a greater distance between the maxillary sinus floor (MSF) and the root apex is associated with a reduced likelihood of odontogenic maxillary sinusitis (OMS), assuming other variables remain constant. However, both the findings of the present study and those of previous investigations [ 21 , 37 ] demonstrate an inverse relationship between the occurrence of MT and the proximity of tooth roots to the MSF. Furthermore, we found a significant relationship between severity of MT and the distance between the root apex and MSF. The patients with the root apex in contact with the MSF (type II) were at lower risk (0.212 times) of developing MT > 10 mm than those with the root apex protrudes into the MSF (type I). Additionally, existing studies [ 17 , 38 , 39 ] have primarily focused on the correlation between periodontal diseases and PALs and the radiographic appearance of the Schneiderian membrane. In contrast, our study evaluated the effects of different odontogenic diseases on MC and found no significant correlation. The distance between the PALs and MSF appears to be a factor associated with MT. Our study revealed that when the PALs were located 1–2 mm or > 2 mm from the MSF (Type 2 and Type 3), the likelihood of developing MT > 10 mm was reduced by 0.161 and 0.089 times, respectively, compared to when the PALs were located 0.5–1 mm from the MSF (Type 1). These findings align with those reported by Kuligowski et al. [ 40 ], Sghaireen [ 41 ], and Dagassan-Berndt et al. [ 42 ]. However, contrasting results were observed in studies by Zadsirjan et al. [ 43 ], Gürhan et al. [ 44 ], and Rege et al. [ 24 ], which found no association between the proximity of the PALs to the MSF and MT. It is important to note that factors such as infection severity and host resistance may influence the transmission of periapical infection to the MS. Therefore, these findings should be interpreted with caution, and further studies are warranted to elucidate the relationship between the MT and the PALs to the MSF. Several authors [ 21 , 25 ] observed that the prevalence of MT increased with the size of the lesion. Similarly, a significant increase in the likelihood of MT was noted as the severity of apical periodontitis advanced. Based on this postulate, the present study did not take account the sizes of lesions, but the distance of the PALs to the MSF was recorded. However, in the present study, a significant correlation was found between the distance of the PALs and MC (including MT and MA). Further work is required to establish the influence of overall sizes of all existing PALs. Within the limitations of this study, its retrospective design restricted the correlation between MT and MA with patients’ clinical presentations. Future prospective clinical studies are necessary to validate these findings and to evaluate the effects of endodontic and/or periodontal interventions on mucosal changes in cases of the OMS, highlighting the critical role of CBCT in monitoring sinus membrane alterations. Furthermore, the inclusion of detailed dental clinical parameters and microbiological analyses in patients presenting with Schneiderian membrane thickening may provide deeper insights into the underlying mechanisms of maxillary mucosal pathology. 5. Conclusions OMS shows a higher prevalence among males in the population seeking dental care. The severity of maxillary sinus mucosal hyperplasia increases with the presence of the PALs in the maxillary posterior teeth, particularly as the PALs and root apex approach closer to the MSF. Therefore, patients presenting with PALs in the maxillary posterior region should be closely monitored for OMS and related sinus symptoms. In cases where OMS is suspected, prompt and thorough examination is essential to establish an accurate diagnosis. Early-stage intervention, including the development of a comprehensive treatment plan in collaboration with otorhinolaryngology specialists, is highly recommended to ensure accurate diagnosis and effective management of odontogenic maxillary sinus pathology. Declarations Ethics, Consent to Participate, and Consent to Publish declarations 1. Ethics approval and consent to participate: The clinical operation involved in this case was told to the patients and got the informed consent from the patients in accordance with the Declaration of Helsinki, and totally approved by the Ethics Committee of Stomatological Hospital of Xiamen Medical College. All authors and patients have read and agreed to the published version of the manuscript. 2. Competing interests: All authors report no conflicts of interest in this work. 3. Consent for publication: All authors and patients have read and agreed to the published version of the manuscript. 4. Availability of data and materials: Not applicable. 5. Clinical trial number: KS20231212002. 6. Funding Declaration: This work was jointly supported by Xiamen Municipal Guiding Project for Medical and Health Care (No. 3502Z20224ZD1326), National Natural Science Foundation of China (82301047), Fujian provincial health technology project (2023GGB07), and Research Cultivation Fund project of Stomatological Hospital of Xiamen Medical College (2023XKCX0005). 7. Acknowledgements: Not applicable. 8. Data availability statement: The raw data supporting the conclusion of this article will be made available on request from the corresponding author. References Hauman CH, Chandler NP, Tong DC. Endodontic implications of the maxillary sinus: a review. Int Endod J. 2002;35(2):127-141. Yildirim D, Eroglu M, Salihoglu M, Yildirim AO, et al. The relationship between dental indentation and maxillary sinusitis. Open J Med Imaging. 2013;3(2):65-8. Lu Y, Liu Z, Zhang L, et al. 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Relationship between inferior wall of maxillary sinus and maxillary posterior teeth using cone beam computed tomography in healthy and chronic periodontitis patients. J Indian Soc Periodontol. 2017;21(6):466-472. Phothikhun S, Suphanantachat S, Chuenchompoonut V, et al. Cone-beam computed tomographic evidence of the association between periodontal bone loss and mucosal thickening of the maxillary sinus. J Periodontol. 2012; 83:557–564. Brüllmann DD, Schmidtmann I, Hornstein S, et al. Correlation of cone beam computed tomog-raphy (CBCT) findings in the maxillary sinus with dental diagnoses: a retrospective cross-sectional study. Clin Oral Invest. 2012;16(4):1023–1029. Eggmann F, Connert T, Bühler J, et al. Do periapical and periodontal pathologies affect Schneiderian membrane appearance? Systematic review of studies using cone-beam computed tomography. Clin Oral Invest. 2017; 21, 1611–1630. Kuligowski P, Jaroń A, Preuss O, Gabrysz-Trybek E, et al. Association between Odontogenic and Maxillary Sinus Conditions: A Retrospective Cone-Beam Computed Tomographic Study. J Clin Med. 2021;10(13):2849. Sghaireen MG. Thickening of Schneiderian membrane secondary to periapical lesions: A retrospective radiographic analysis. J Int Soc Prev Community Dent. 2020;10(3):316-322. Dagassan-Berndt DC, Zitzmann NU, Lambrecht JT, et al. Is the Schneiderian membrane thickness affected by periodontal disease? A cone beam computed tomography-based extended case series. J Int Acad Periodontol. 2013;15(3):75-82. Zadsirjan S, Sheikhi M, Dakhilalian A, et al. Association of Inflammatory Periapical Lesions with Maxillary Sinus Abnormalities: a Retrospective Cone-Beam Computed Tomography Study. J Dent (Shiraz). 2021;22(4):273-280. Gürhan C, Şener E, Mert A, et al. Evaluation of factors affecting the association between thickening of sinus mucosa and the presence of periapical lesions using cone beam CT. Int Endod J. 2020;53(10): 1339-1347. Tables Tables 1 to 3 are available in the Supplementary Files section Additional Declarations No competing interests reported. Supplementary Files Tables.docx Cite Share Download PDF Status: Under Review Version 1 posted Editorial decision: Revision requested 15 May, 2025 Reviews received at journal 13 May, 2025 Reviews received at journal 10 May, 2025 Reviews received at journal 05 May, 2025 Reviewers agreed at journal 30 Apr, 2025 Reviewers agreed at journal 29 Apr, 2025 Reviewers agreed at journal 29 Apr, 2025 Reviewers invited by journal 29 Apr, 2025 Editor assigned by journal 23 Apr, 2025 Submission checks completed at journal 23 Apr, 2025 First submitted to journal 20 Apr, 2025 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-6491416","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":449999565,"identity":"c9197f4b-de64-41cd-9f46-474223752f58","order_by":0,"name":"Ming Liu","email":"","orcid":"","institution":"Stomatological Hospital of Xiamen Medical College","correspondingAuthor":false,"prefix":"","firstName":"Ming","middleName":"","lastName":"Liu","suffix":""},{"id":449999566,"identity":"426227b3-5009-440e-9824-29c5ee263dc0","order_by":1,"name":"Taiwei Lin","email":"","orcid":"","institution":"Stomatological Hospital of Xiamen Medical College","correspondingAuthor":false,"prefix":"","firstName":"Taiwei","middleName":"","lastName":"Lin","suffix":""},{"id":449999567,"identity":"827ec5ec-25ab-4c8c-878d-615c6c61a396","order_by":2,"name":"Wenqin Chen","email":"","orcid":"","institution":"Stomatological Hospital of Xiamen Medical College","correspondingAuthor":false,"prefix":"","firstName":"Wenqin","middleName":"","lastName":"Chen","suffix":""},{"id":449999568,"identity":"a047693b-c9db-4326-b039-7d6b7978d357","order_by":3,"name":"Yixuan Wu","email":"","orcid":"","institution":"Stomatological Hospital of Xiamen Medical College","correspondingAuthor":false,"prefix":"","firstName":"Yixuan","middleName":"","lastName":"Wu","suffix":""},{"id":449999569,"identity":"24c75aa0-095b-4b8b-9947-1f448f5f3f3a","order_by":4,"name":"Yi Zhang","email":"","orcid":"","institution":"Stomatological Hospital of Xiamen Medical College","correspondingAuthor":false,"prefix":"","firstName":"Yi","middleName":"","lastName":"Zhang","suffix":""},{"id":449999570,"identity":"a463196a-af99-46f7-ae8e-cc6ec874ae0e","order_by":5,"name":"Zhisheng Zhang","email":"","orcid":"","institution":"Stomatological Hospital of Xiamen Medical College","correspondingAuthor":false,"prefix":"","firstName":"Zhisheng","middleName":"","lastName":"Zhang","suffix":""},{"id":449999571,"identity":"dd671c36-a711-47ef-9f92-0b7419b27db7","order_by":6,"name":"Qianju Wu","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAA4ElEQVRIiWNgGAWjYJCCAwwMbAz8DAwJIA5jA9FaJBsYEhuI1gIGBgcgqglrMbiRvPHAzx18iZvPH3j+mIfBRnbDAeZnD/BrSSs42HuGLXHbjYTEZh6GNOMNB9jMDfBpMbuRY3CAtw2khQGk5XDihgM8bBKEtBz8C9Syuf8ASMt/4rQcBtmygQHssAOEtdifeVZwWLaNzXgG0C8z5xgkG888zGaGV4tke/Lmj2/bjsn2959J+PCmwk6273jzM7xagAAUPMeAmCcBwmYmoB6qpQaI2Q8QVjsKRsEoGAUjEgAA57dRdg4d5LsAAAAASUVORK5CYII=","orcid":"","institution":"Stomatological Hospital of Xiamen Medical College","correspondingAuthor":true,"prefix":"","firstName":"Qianju","middleName":"","lastName":"Wu","suffix":""}],"badges":[],"createdAt":"2025-04-21 00:53:11","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-6491416/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-6491416/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":82150015,"identity":"dfe7c259-5f1d-413b-b623-7928212296f0","added_by":"auto","created_at":"2025-05-07 07:12:46","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":783396,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eClassification of maxillary sinus mucosal thickness (MT) and mucosal appearance (MA)\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eMT: A: Normal Schneiderian membrane thickening, 0 to 2 mm.\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eB: Moderate Schneiderian membrane thickening, 2 to 10 mm.\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eC: Severe Schneiderian membrane thickening, \u0026gt; 10 mm.\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eMA: D: Flat thickening.\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eE: Polypoid thickening.\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eF: Occluded (acute maxillary sinusitis)\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-6491416/v1/0dd30a97ec834aaecddbbb02.png"},{"id":82150010,"identity":"2bac8df5-a0d6-44a0-9d21-a4f8d3c89d68","added_by":"auto","created_at":"2025-05-07 07:12:45","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":364180,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eDistance between the root apex and maxillary sinus floor (MSF).\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eA: Type 1: Root apex protrudes into the MSF.\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eB: Type 2: Root apex is in contact with the MSF.\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eC: Type 3: Root apex is near the MSF.\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-6491416/v1/84019c8c02af12d4edb6bcb7.png"},{"id":82150025,"identity":"bffcf50d-91f0-4abf-95f1-9e5b118af554","added_by":"auto","created_at":"2025-05-07 07:12:46","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":375755,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eDistance between the periapical lesions (PALs) and maxillary sinus floor (MSF).\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eA: Type 1: 0.5–1 mm.\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eB: Type 2: 1–2 mm.\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eC: Type 3: ＞2 mm.\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-6491416/v1/4b3577142f194d860643d846.png"},{"id":82153956,"identity":"6e49b189-59ff-43a7-b823-d7122a7b9656","added_by":"auto","created_at":"2025-05-07 07:28:47","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":2611747,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-6491416/v1/f78f6c4c-b7ed-408d-b9a4-e023d6372d07.pdf"},{"id":82150024,"identity":"8e6659d8-81d6-433c-a210-7bb0072d1f8b","added_by":"auto","created_at":"2025-05-07 07:12:46","extension":"docx","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":33490,"visible":true,"origin":"","legend":"","description":"","filename":"Tables.docx","url":"https://assets-eu.researchsquare.com/files/rs-6491416/v1/1e8b1f5bac73c2f88987a94c.docx"}],"financialInterests":"No competing interests reported.","formattedTitle":"Association between odontogenic factors and maxillary sinus mucosal characteristics: a retrospective CBCT study","fulltext":[{"header":"1. Introduction","content":"\u003cp\u003eThe maxillary sinus (MS), a pyramid-shaped, air-filled cavity located within the maxillary bone, is uniquely susceptible to oral pathogenic microorganisms due to its close anatomical relationship with the roots of the maxillary molars and premolars. This proximity renders the MS more vulnerable to odontogenic infections than other paranasal sinuses. [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e]. Odontogenic factors are reported to account for approximately 12% of maxillary sinusitis cases [\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e]. According to recent studies, Endodontic and periodontal infections are recognized as the main causes for odontogenic maxillary sinusitis (OMS), including apical periodontitis, endo-perio lesions, radicular cysts and periodontitis [\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e, \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e]. Although dental implants and endodontic material can also impinge on maxillary sinuses, these are considered rare causes of sinusitis [\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e]. The lining of the MS is composed of a mucous membrane that includes a pseudo-stratified epithelium with goblet cells, lamina propria, and periosteum-like structures [\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e]. This membrane, also known as the Schneiderian membrane, is highly susceptible to odontogenic infections [\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e]. The Schneiderian membrane is difficult to clearly delineate on Cone Beam Computed Tomography (CBCT) scans. Under physiological conditions, its thickness averages approximately 0.30\u0026thinsp;\u0026plusmn;\u0026thinsp;0.17 mm; however, in the presence of infection or inflammation, this thickness may increase more than 10 times, indicating significant mucosal hypertrophy [\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e]. The diagnosis of OMS is relatively complex and subject to some controversy, requiring a combination of clinical and imaging assessments for accuracy. CBCT is the most reliable tool for the evaluation of structures within and adjacent to the MS, primarily since this technique provides three-dimensional imaging and, in certain cases, facilitates the evaluation of soft tissues [\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e, \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e]. A normal maxillary sinus is typically defined by the absence of detectable mucosal thickening (MT) or by a uniform MT measuring less than 2 mm, as observed on radiographic imaging (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eA) [\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e]. Odontogenic maxillary sinusitis (OMS) is characterized by the presence of a localized soft tissue density within the sinus, with MT\u0026thinsp;\u0026ge;\u0026thinsp;2 mm, anatomically correlated with a tooth affected by pathological conditions such as dental caries, defective restorations, periapical lesions (PALs), or post-extraction changes [\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eHowever, the radiographic evaluation of the Schneiderian membrane and its association with odontogenic conditions remains a topic of ongoing debate. The presence and extent of mucosal thickening do not consistently correspond to underlying pathology, making it challenging to differentiate between physiological variations and pathological changes based solely on imaging findings. Aksoy et al. [\u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e] found that the incidence of maxillary sinus mucosal thickening and maxillary sinus cysts was higher in male patients than in females. However, Zhang et al. [\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e] reported that there was no statistically significant difference in Schneiderian membrane thickening between genders. Moreover, most studies primarily focus on the association of mucosal thickening (MT) while overlooking mucosal appearance (MA) [\u003cspan additionalcitationids=\"CR16\" citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e]. Therefore, this retrospective and cross-sectional study aimed to determine the association between the various odontogenic factors (including odontogenic diseases, tooth type, and the distance between the MSF and the PALs/root apex, etc.) in posterior maxillary area and the presence of maxillary sinus MT and MA using CBCT.\u003c/p\u003e"},{"header":"2. Material and methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e\n \u003ch2\u003e2.1. Subjects\u003c/h2\u003e\n \u003cp\u003eThe clinical operation involved in this case was told to the patients and got the informed consent from the patients in accordance with the Declaration of Helsinki, and totally approved by the Ethics Committee of Stomatological Hospital of Xiamen Medical College. A total of 16,439 patients who underwent comprehensive maxillary Cone Beam Computed Tomography (CBCT) scans between January 2024 and December 2024 were initially considered for inclusion. Ultimately, 249 patients (aged 18\u0026ndash;75 years, mean age 41.1\u0026thinsp;\u0026plusmn;\u0026thinsp;13.92) were selected, all of whom demonstrated evidence of sinus changes in one or both maxillary sinuses. The study protocol adhered to the principles outlined in the Declaration of Helsinki, including all subsequent amendments and revisions.\u003c/p\u003e\n \u003cp\u003eThe selection and collection of data from patients\u0026apos; clinical histories were governed by the following inclusion criteria: (1) patients aged 18 years or older; (2) availability of complete maxillary CBCT scans, including panoramic, axial, and ortho-radial sections; (3) the presence of sinus membrane thickening in one or both maxillary sinuses; (4) evidence of periapical radiolucency, periodontitis, endo-perio lesions, or radicular cysts. Exclusion criteria included: (1) nasal symptoms (congestion, rhinorrhea, fever) within the past three months; (2) radiographic evidence of maxillary sinus cysts or sinusitis; (3) history of maxillofacial trauma, missing teeth, or dental implants in the posterior maxilla; (4) maxillofacial surgery within the past three months\u003c/p\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec4\" class=\"Section2\"\u003e\n \u003ch2\u003e2.2. Research methods\u003c/h2\u003e\n \u003cp\u003eCBCT images of 249 patients (115 females and 134 males; aged 18\u0026ndash;75 years) meeting the inclusion and exclusion criteria were included in the study. The CBCT scans were acquired using a 12*8cm /15*15cm field of view (NewTom VGI, Quantitative Radiology s.r.l., Verona, Italy) to capture the maxillary anatomy. The unit operated at a fixed 110 kVp setting, with automated milliampere adjustments and a scan time of 36 seconds, producing 0.3-mm-thick axial slices with isotropic voxels. All measurements and analyses were jointly conducted by trained radiologists and endodontists proficient in using NNT analysis software (NNT 7.2.0, QR NewTom, Quantitative Radiology s.r.l., Verona, Italy). The software was used to reconstruct axial, coronal, and cross-sectional images for the assessment of the maxillary sinuses and their anatomical relationship with adjacent maxillary teeth. For each patient, CBCT measurements were performed three times, and the mean value was recorded as the result.\u003c/p\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec5\" class=\"Section2\"\u003e\n \u003ch2\u003e2.3. Assessment of MT\u003c/h2\u003e\n \u003cp\u003eMucosal thickening (MT) was measured on coronal and sagittal CBCT sections at the point of greatest thickness from the maxillary sinus floor (MSF) to the highest point of the thickened mucosa, then recorded and classified as (Fig. \u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e)\u003c/p\u003e\n \u003cp\u003eGrade 1: 2 to 10 mm (Moderate Schneiderian membrane thickening, Fig. B1 and B2)\u003c/p\u003e\n \u003cp\u003eGrade 2: \u0026gt; 10 mm (Severe Schneiderian membrane thickening, Fig. C1 and C2)\u003c/p\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec6\" class=\"Section2\"\u003e\n \u003ch2\u003e2.4. Assessment of MA\u003c/h2\u003e\n \u003cp\u003eMA in the maxillary sinuses on CBCT scans were evaluated on the coronal and sagittal sections of CBCT scans and classified as (Fig. \u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e)\u003c/p\u003e\n \u003cp\u003eGrade 1: Flat thickening. (Fig. D1 and D2)\u003c/p\u003e\n \u003cp\u003eGrade 2: Polypoid thickening. (Fig. E1 and E2)\u003c/p\u003e\n \u003cp\u003eGrade 3: Occluded (acute maxillary sinusitis). (Fig. F1 and F2)\u003c/p\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec7\" class=\"Section2\"\u003e\n \u003ch2\u003e2.5. Assessment of the periapical status\u003c/h2\u003e\n \u003cp\u003eThe presence of premolars/molars and periapical lesions (PALs) in the posterior maxilla was documented. PALs were identified by loss or irregularity of the lamina dura with periapical radiolucency suggestive of bone destruction. In cases with multiple lesions, only the one in closest proximity to the sinus was recorded. The following parameters were used to evaluate the CBCT images:\u003c/p\u003e\n \u003cp\u003e● Tooth type (premolar / molar)\u003c/p\u003e\n \u003cp\u003e● Odontogenic diseases (Apical Periodontitis, Endo-perio lesion, Radicular cysts and Peri-odontitis)\u003c/p\u003e\n \u003cp\u003e● Distance between the root apex and MSF\u003c/p\u003e\n \u003cp\u003e● Distance between PALs and the MSF\u003c/p\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec8\" class=\"Section2\"\u003e\n \u003ch2\u003e2.5. 1. Distance between root apex and MSF\u003c/h2\u003e\n \u003cp\u003eThe distance between MSF and the root apex was determined and recorded in the sagittal and coronal views for each tooth individually and classified as (Fig. \u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003e)\u003c/p\u003e\n \u003cp\u003eType 1: Root apex protrudes into the MSF. (Fig. A1 and A2)\u003c/p\u003e\n \u003cp\u003eType 2: Root apex is in contact with the MSF (Fig. B1 and B2)\u003c/p\u003e\n \u003cp\u003eType 3: Root apex is near the MSF. (Fig. C1 and C2)\u003c/p\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec9\" class=\"Section2\"\u003e\n \u003ch2\u003e2.5. 2. Distance between PALs and MSF\u003c/h2\u003e\n \u003cp\u003eA periapical lesion (PAL) was defined as a radiolucency at the root apex with a thickness of \u0026ge;\u0026thinsp;0.5 mm (at least twice the normal width of the periodontal ligament) on sagittal and coronal CBCT sections [\u003cspan class=\"CitationRef\"\u003e18\u003c/span\u003e]. The shortest distance from the apex of the lesion to the maxillary sinus floor (MSF) was measured and classified as (Fig. \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003e)\u003c/p\u003e\n \u003cp\u003eType 1: 0.5\u0026ndash;1 mm;(Fig. A1 and A2)\u003c/p\u003e\n \u003cp\u003eType 2: 1\u0026ndash;2 mm;(Fig. B1 and B2)\u003c/p\u003e\n \u003cp\u003eType 3: \u0026gt;2 mm;(Fig. C1 and C2)\u003c/p\u003e\n\u003c/div\u003e\n\u003ch3\u003e2 .6 Statistical analysis\u003c/h3\u003e\n\u003cp\u003ePearson\u0026rsquo;s correlation analysis revealed strong intra- and inter-observer agreement for repeated measurements of membrane thickness and the distance between PALs and the MSF (r\u0026thinsp;=\u0026thinsp;0.95 and r\u0026thinsp;=\u0026thinsp;0.93, respectively). Maxillary sinus anatomy (MA) assessments were conducted independently, with discrepancies resolved through consensus. Statistical analysis was performed using IBM SPSS Statistics for Windows (Version 24.0, IBM Corp., Armonk, NY, USA). Group comparisons were conducted using the chi-squared test. Potential factors associated with MT were evaluated using multivariate binary logistic regression. A p-value\u0026thinsp;\u0026lt;\u0026thinsp;0.05 was considered statistically significant.\u003c/p\u003e"},{"header":"3. Result","content":"\u003cp\u003e\u003cem\u003e3.1. Prevalence of MT and MA\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eAmong the 249 patients with maxillary sinus mucosal thickening more than 2mm, 199 patients (79.9%) were associated with sinus mucosal thickening classified as Grade 1 (2 to 10 mm) while 50 patients had mucosal thickening greater than 10mm (Grade 2), accounting for 20.1% (Table 1). According to the MA, 65.9% of patients (164/249) had flat thickening, 22.1% (55/249) had polypoid thickening, and 12.0% (30/249) had occluded thickening (Table 2).\u003c/p\u003e\n\u003cp\u003e\u003cem\u003e3.2. Mucosal Characteristics and Its Associated Factors Analysis\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eThe distribution of mucosal characteristics (MC) in maxillary sinusitis, including MT and MA, based on dental findings, is presented in Table 1 and Table 2.\u003c/p\u003e\n\u003cp\u003e3.2.1 Association between Age, Gender and MC\u003c/p\u003e\n\u003cp\u003eAmong the 249 patients, 115 (46.2%) were female, and 134 (53.8%) were male. The patients were divided into three age groups: one group for patients aged 18-35 years, another for those aged 35-50 years, and a third group for patients over 50 years of age. There was no statistically significant association between age and MT (P\u0026gt;0.05), but a significant correlation was found between gender and MT (P＜0.05) (Table 1). There was no statistically significant difference between age and gender in terms of magnitude of change of the MA (P＞0.05) (Table 2).\u003c/p\u003e\n\u003cp\u003e3.2.2 Anatomic relationship between tooth and MC\u003c/p\u003e\n\u003cp\u003eOut of 16439 patients, 249 cases (1.5%) of maxillary sinus mucosal thickness were identified. The most affected teeth were maxillary first molars (MFM) (59.4%), maxillary second molar (MSM) (30.5%) and premolars (10.1%) respectively. But there was no significant association between the tooth type and MT (p＞0.05). Among these teeth, 72.7% of root apices protrude into MSF. As the distance between the root apex and the MSF increased, a significant association was observed between the distance and MT (p＜0.05) (Table 1). Both the tooth type and the distance between the root apex and MSF were associated with the MA (P＜0.05). The flat mucosal thickening of the maxillary sinus occurred most frequently in the MFM (77.7%). Moreover, an anatomical relationship where the root apex protrudes into the MSF (68.5%) was most closely associated with flat mucosal thickening (Table 2).\u003c/p\u003e\n\u003cp\u003e3.2.3. Association between Odontogenic disease, PALs and MC\u003c/p\u003e\n\u003cp\u003eIn the cases of MT, the prevalence of apical periodontitis was significantly higher (53.8%). Among the 249 patients, Grade 1 mucosal thickening (2 to 10 mm, moderate mucosal thickening) accounted for 79.9% (119/249), while flat mucosal thickening accounted for 65.9% (164/249). However, no significant correlation was found between the type of odontogenic disease and MT or MA (Table 1 and 2). Among these cases (Type 1 distance of the PALs to MSF), Grade 1 MT accounted for 75.1% (142/189), while flat mucosal thickening accounted for 59.3% (112/189). The distance between the PALs and MSF was significantly correlated with MT (P = 0.04) and MA (P = 0.002) (Table 1 and 2).\u003c/p\u003e\n\u003cp\u003e\u003cem\u003e3.3. Binary Logistic Regression Analysis of Factors Influencing MT\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eThe binary logistic regression analysis indicated that male sex, types 2 (considering distance between the root apex and MSF), and distance of the PALs to MSF were significant associated with the severity of MT. The ORs and 95% CIs for these associations are shown in Tables 3. The severity of MT was significantly associated with male sex (OR = 2.441, P = 0.011). Patients with root apex in contact with the MSF (type 2) demonstrated a significant negative impact on MT, with a 0.212 times lower risk of increasing the MT severity compared to those with root apex extending into the MSF (type 1). Furthermore, patients with Type 2 (PALs located 1\u0026ndash;2 mm from the MSF) and Type 3 (PALs located \u0026gt;2 mm from the MSF) also exhibited a significant negative impact on the MT. They were at a reduced risk of increasing the severity of MT by 0.161 and 0.089 times, respectively, compared to patients with PALs located 0.5\u0026ndash;1 mm from the MSF (Type 1). \u0026nbsp;\u0026nbsp;\u003c/p\u003e"},{"header":"4. Discussion","content":"\u003cp\u003eThis study aimed to evaluate the effects of various odontogenic factors on MT and MA, which may contribute to the etiology of OMS. Accurately identifying the etiological factors of OMS is crucial for selecting the most appropriate treatment and preventing future cases [\u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e19\u003c/span\u003e]. While CT is regarded as the gold standard for imaging maxillary sinusitis, in this study, CBCT was utilized to assess the maxillary sinuses due to its lower radiation dose, higher resolution, and shorter screening time [\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e, \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eIn the literature, odontogenic diseases [\u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e, \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e];presence [\u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e, \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e, \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e23\u003c/span\u003e] and proximity [\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e, \u003cspan additionalcitationids=\"CR25\" citationid=\"CR24\" class=\"CitationRef\"\u003e24\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e26\u003c/span\u003e] of PALs; and distance between root apex and MSF [\u003cspan additionalcitationids=\"CR28\" citationid=\"CR27\" class=\"CitationRef\"\u003e27\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e29\u003c/span\u003e] have been evaluated for their possible influence on MS. Ince Yusufoglu et al. [\u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e30\u003c/span\u003e] reported a prevalence rate of MT (Moderate Schneiderian membrane thickening, Grade 1) in OMS of 87.3%. In our study, a relatively lower prevalence of Grade 1 (79.9%) was observed. This discrepancy between studies may be attributable to using different diagnostic criteria (2-10mm, \u0026gt;10mm) for assessing the pathological radiographic mucosal thickening in the study. Other explanations are probably due to the difference in the indication of CBCT scans, which were included in the study and sample size among the populations studied.\u003c/p\u003e \u003cp\u003eGender had no effect on the MA; however, a statistically significant correlation was observed in the MT. The findings of this study are consistent with those reported by Van et al [\u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e31\u003c/span\u003e]. Moreover, previous studies have established a positive correlation between sinusitis and smoking [\u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e32\u003c/span\u003e]. The higher proportion of male patients who smoke may also contribute to the observed differences. This outcome may be explained by the inclusion of smokers in the study population, rather than their exclusion [\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eIn the literature on odontogenic diseases, the prevalence of PALs observed in our study is generally consistent with findings reported in previous studies. According to Goller-Bulut et al. [\u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e25\u003c/span\u003e], MFMs exhibited the highest prevalence of apical periodontitis among all affected teeth, indicating their significant association with periapical pathology. Shanbhag et al. and Maillet et al. [\u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e33\u003c/span\u003e, \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e34\u003c/span\u003e] both identified the MFM as the most affected tooth and the leading cause of OMS, followed by the MSM. The higher prevalence of pathology in MFMs and MSMs may be attributed to their increased susceptibility to dental caries and pulpal disease [\u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e26\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eThe distance between the root apex and MSF is of significant clinical importance, as it can lead to various complications, including sinusitis, oroantral fistula formation, and the displacement of roots or materials into the MS [\u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e35\u003c/span\u003e]. In a recent study, Chand et al. [\u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e36\u003c/span\u003e] suggested that the transmission of microorganisms or toxins to the Schneiderian membrane from the lesion depends on the thickness of the remaining alveolar bone beneath the MS. This finding suggests that a greater distance between the maxillary sinus floor (MSF) and the root apex is associated with a reduced likelihood of odontogenic maxillary sinusitis (OMS), assuming other variables remain constant. However, both the findings of the present study and those of previous investigations [\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e, \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e37\u003c/span\u003e] demonstrate an inverse relationship between the occurrence of MT and the proximity of tooth roots to the MSF. Furthermore, we found a significant relationship between severity of MT and the distance between the root apex and MSF. The patients with the root apex in contact with the MSF (type II) were at lower risk (0.212 times) of developing MT\u0026thinsp;\u0026gt;\u0026thinsp;10 mm than those with the root apex protrudes into the MSF (type I). Additionally, existing studies [\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e, \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e38\u003c/span\u003e, \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e39\u003c/span\u003e] have primarily focused on the correlation between periodontal diseases and PALs and the radiographic appearance of the Schneiderian membrane. In contrast, our study evaluated the effects of different odontogenic diseases on MC and found no significant correlation.\u003c/p\u003e \u003cp\u003eThe distance between the PALs and MSF appears to be a factor associated with MT. Our study revealed that when the PALs were located 1\u0026ndash;2 mm or \u0026gt;\u0026thinsp;2 mm from the MSF (Type 2 and Type 3), the likelihood of developing MT\u0026thinsp;\u0026gt;\u0026thinsp;10 mm was reduced by 0.161 and 0.089 times, respectively, compared to when the PALs were located 0.5\u0026ndash;1 mm from the MSF (Type 1). These findings align with those reported by Kuligowski et al. [\u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e40\u003c/span\u003e], Sghaireen [\u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e41\u003c/span\u003e], and Dagassan-Berndt et al. [\u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e42\u003c/span\u003e]. However, contrasting results were observed in studies by Zadsirjan et al. [\u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e43\u003c/span\u003e], G\u0026uuml;rhan et al. [\u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e44\u003c/span\u003e], and Rege et al. [\u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e24\u003c/span\u003e], which found no association between the proximity of the PALs to the MSF and MT. It is important to note that factors such as infection severity and host resistance may influence the transmission of periapical infection to the MS. Therefore, these findings should be interpreted with caution, and further studies are warranted to elucidate the relationship between the MT and the PALs to the MSF.\u003c/p\u003e \u003cp\u003eSeveral authors [\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e, \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e25\u003c/span\u003e] observed that the prevalence of MT increased with the size of the lesion. Similarly, a significant increase in the likelihood of MT was noted as the severity of apical periodontitis advanced. Based on this postulate, the present study did not take account the sizes of lesions, but the distance of the PALs to the MSF was recorded. However, in the present study, a significant correlation was found between the distance of the PALs and MC (including MT and MA). Further work is required to establish the influence of overall sizes of all existing PALs.\u003c/p\u003e \u003cp\u003eWithin the limitations of this study, its retrospective design restricted the correlation between MT and MA with patients\u0026rsquo; clinical presentations. Future prospective clinical studies are necessary to validate these findings and to evaluate the effects of endodontic and/or periodontal interventions on mucosal changes in cases of the OMS, highlighting the critical role of CBCT in monitoring sinus membrane alterations. Furthermore, the inclusion of detailed dental clinical parameters and microbiological analyses in patients presenting with Schneiderian membrane thickening may provide deeper insights into the underlying mechanisms of maxillary mucosal pathology.\u003c/p\u003e"},{"header":"5. Conclusions","content":"\u003cp\u003eOMS shows a higher prevalence among males in the population seeking dental care. The severity of maxillary sinus mucosal hyperplasia increases with the presence of the PALs in the maxillary posterior teeth, particularly as the PALs and root apex approach closer to the MSF. Therefore, patients presenting with PALs in the maxillary posterior region should be closely monitored for OMS and related sinus symptoms. In cases where OMS is suspected, prompt and thorough examination is essential to establish an accurate diagnosis. Early-stage intervention, including the development of a comprehensive treatment plan in collaboration with otorhinolaryngology specialists, is highly recommended to ensure accurate diagnosis and effective management of odontogenic maxillary sinus pathology.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eEthics, Consent to Participate, and Consent to Publish declarations\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e1. Ethics approval and consent to participate:\u0026nbsp;The clinical operation involved in this case was told to the patients and got the informed consent from the patients\u0026nbsp;in accordance with the Declaration of Helsinki,\u0026nbsp;and totally approved by the Ethics Committee of Stomatological Hospital of Xiamen Medical College. All authors and patients have read and agreed to the published version of the manuscript.\u003c/p\u003e\n\u003cp\u003e2. Competing interests: All authors report no conflicts of interest in this work.\u003c/p\u003e\n\u003cp\u003e3.\u0026nbsp;Consent for publication: All authors and patients have read and agreed to the published version of the manuscript.\u003c/p\u003e\n\u003cp\u003e4. Availability of data and materials:\u0026nbsp;Not applicable.\u003c/p\u003e\n\u003cp\u003e5. Clinical trial number: KS20231212002.\u003c/p\u003e\n\u003cp\u003e6. Funding Declaration:\u0026nbsp;This work was jointly supported by Xiamen Municipal Guiding Project for Medical and Health Care (No. 3502Z20224ZD1326), National Natural Science Foundation of China (82301047), Fujian provincial health technology project (2023GGB07), and Research Cultivation Fund project of Stomatological Hospital of Xiamen Medical College (2023XKCX0005).\u003c/p\u003e\n\u003cp\u003e7. Acknowledgements:\u0026nbsp;Not applicable.\u003c/p\u003e\n\u003cp\u003e8. Data availability statement: The raw data supporting the conclusion of this article will be made available on request from the corresponding author.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n \u003cli\u003eHauman CH, Chandler NP, Tong DC. Endodontic implications of the maxillary sinus: a review. Int Endod J. 2002;35(2):127-141.\u003c/li\u003e\n \u003cli\u003eYildirim D, Eroglu M, Salihoglu M, Yildirim AO, et al. The relationship between dental indentation and maxillary sinusitis. Open J Med Imaging. 2013;3(2):65-8.\u003c/li\u003e\n \u003cli\u003eLu Y, Liu Z, Zhang L, et al. Associations between maxillary sinus mucosal thickening and apical periodontitis using cone-beam computed tomography scanning: a retrospective study. J Endod. 2012;38(8):1069-1074.\u003c/li\u003e\n \u003cli\u003eNascimento EH, Pontual ML, Pontual AA, et al. Association between Odontogenic Conditions and Maxillary Sinus Disease: A Study Using Cone-beam Computed Tomography. 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Relationship between inferior wall of maxillary sinus and maxillary posterior teeth using cone beam computed tomography in healthy and chronic periodontitis patients. J Indian Soc Periodontol. 2017;21(6):466-472.\u003c/li\u003e\n \u003cli\u003ePhothikhun S, Suphanantachat S, Chuenchompoonut V, et al. Cone-beam computed tomographic evidence of the association between periodontal bone loss and mucosal thickening of the maxillary sinus. J Periodontol. 2012; 83:557\u0026ndash;564.\u003c/li\u003e\n \u003cli\u003eBr\u0026uuml;llmann DD, Schmidtmann I, Hornstein S, et al. Correlation of cone beam computed tomog-raphy (CBCT) findings in the maxillary sinus with dental diagnoses: a retrospective cross-sectional study. Clin Oral Invest. 2012;16(4):1023\u0026ndash;1029.\u003c/li\u003e\n \u003cli\u003eEggmann F, Connert T, B\u0026uuml;hler J, et al. Do periapical and periodontal pathologies affect Schneiderian membrane appearance? Systematic review of studies using cone-beam computed tomography. Clin Oral Invest. 2017; 21, 1611\u0026ndash;1630.\u003c/li\u003e\n \u003cli\u003eKuligowski P, Jaroń A, Preuss O, Gabrysz-Trybek E, et al. Association between Odontogenic and Maxillary Sinus Conditions: A Retrospective Cone-Beam Computed Tomographic Study. J Clin Med. 2021;10(13):2849.\u003c/li\u003e\n \u003cli\u003eSghaireen MG. Thickening of Schneiderian membrane secondary to periapical lesions: A retrospective radiographic analysis. J Int Soc Prev Community Dent. 2020;10(3):316-322.\u003c/li\u003e\n \u003cli\u003eDagassan-Berndt DC, Zitzmann NU, Lambrecht JT, et al. Is the Schneiderian membrane thickness affected by periodontal disease? A cone beam computed tomography-based extended case series. J Int Acad Periodontol. 2013;15(3):75-82.\u003c/li\u003e\n \u003cli\u003eZadsirjan S, Sheikhi M, Dakhilalian A, et al. Association of Inflammatory Periapical Lesions with Maxillary Sinus Abnormalities: a Retrospective Cone-Beam Computed Tomography Study. J Dent (Shiraz). 2021;22(4):273-280.\u003c/li\u003e\n \u003cli\u003eG\u0026uuml;rhan C, Şener E, Mert A, et al. Evaluation of factors affecting the association between thickening of sinus mucosa and the presence of periapical lesions using cone beam CT. Int Endod J. 2020;53(10): 1339-1347.\u003c/li\u003e\n\u003c/ol\u003e"},{"header":"Tables","content":"\u003cp\u003eTables 1 to 3 are available in the Supplementary Files section\u003c/p\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"bmc-medical-imaging","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"bmim","sideBox":"Learn more about [BMC Medical Imaging](http://bmcmedimaging.biomedcentral.com/)","snPcode":"","submissionUrl":"https://www.editorialmanager.com/bmim/default.aspx","title":"BMC Medical Imaging","twitterHandle":"BMC_series","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"em","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"Odontogenic conditions, Maxillary sinus mucosal thickening, Maxillary sinus mucosal appearance, Cone-Beam Computed Tomography","lastPublishedDoi":"10.21203/rs.3.rs-6491416/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-6491416/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003e\u003cstrong\u003eObjectives\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe aim of this study was to investigate the effects of various dental and maxillary sinus (MS) variables on mucosal characteristics (MC), including maxillary sinus mucosal thickness (MT) and mucosal appearance (MA), using cone-beam computed tomography (CBCT) imaging.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eMaterials and methods\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eCBCT images of the MS (n=249) were reviewed from a total of 16439 patients who had undergone CBCT examinations for various dentomaxillofacial issues, leading to the identification and confirmation of odontogenic maxillary sinusitis (OMS). The MT and the distances between the maxillary sinus floor (MSF) and both the root apex and periapical lesion (PALs) were measured. The MA and situations of adjacent teeth were recorded. The relationships between these odontogenic factors and MC (including MT and MA) were evaluated. The data were analyzed using analysis of variance, χ2-test, and logistic regression.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eResults\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eA total of 249 CBCT images exhibited OMS with specific mucosal characteristics. MT was significantly correlated with gender, tooth type, the distance between the root apex and the MSF, and the distance between the PALs and the MSF, whereas MA was significantly associated with all these above factors except gender. (P＜0.05). A logistic regression model showed that the severity of MT hyperplasia was significantly associated with male sex (OR: 2.441, 95% CI: 1.225 ~ 4.863, P\u0026lt; 0.05). The distance between the MSF and PALs or root apex in contact with the MSF (type 2) showed a significant relation with MT \u0026gt; 10 mm. (PALs: OR = 0.161 and 0.089, P \u0026lt; 0.05; root apex: OR = 0.212, P \u0026lt; 0.005).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConclusions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eMultiple factors, including gender, periapical infection, and the distance between the MSF and PALs/root apex, may have a precursor effect on the occurrence of MT and MA in the maxillary sinus. The severity of MT was significantly associated with male sex and the distance between the MSF and PALs/root apex. Odontogenic diseases represent significant risk factors for the development of maxillary sinus infections and should therefore be carefully considered by both dental and medical professionals in the comprehensive assessment and management of maxillary sinus lesions. Therefore, communication between dental surgeons and an otolaryngology specialist is important for the timely diagnosis and treatment of MT of dental origin.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eClinical relevance\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe maxillary sinuses are notably affected by a range of odontogenic factors—such as patient gender, the proximity of the maxillary sinus floor (MSF) to the root apex or periapical lesion (PAL), and the type of tooth involved—all of which may play a contributory role in alterations of mucosal thickening (MT) and maxillary sinus anatomy (MA).\u003c/p\u003e","manuscriptTitle":"Association between odontogenic factors and maxillary sinus mucosal characteristics: a retrospective CBCT study","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2025-05-07 07:12:41","doi":"10.21203/rs.3.rs-6491416/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Revision requested","date":"2025-05-15T04:40:07+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2025-05-13T22:24:18+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2025-05-10T16:48:07+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2025-05-05T06:35:03+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"25005556479117712064076307893450852655","date":"2025-04-30T05:07:54+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"63914019116433350402696461548919880368","date":"2025-04-29T12:51:40+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"99775651001040089125653915813096554537","date":"2025-04-29T09:33:59+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2025-04-29T08:33:59+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2025-04-23T07:37:50+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2025-04-23T07:36:48+00:00","index":"","fulltext":""},{"type":"submitted","content":"BMC Medical Imaging","date":"2025-04-21T00:45:33+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"bmc-medical-imaging","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"bmim","sideBox":"Learn more about [BMC Medical Imaging](http://bmcmedimaging.biomedcentral.com/)","snPcode":"","submissionUrl":"https://www.editorialmanager.com/bmim/default.aspx","title":"BMC Medical Imaging","twitterHandle":"BMC_series","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"em","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"eec21071-8788-47a0-a5b7-e8e9d5332217","owner":[],"postedDate":"May 7th, 2025","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"under-review","subjectAreas":[],"tags":[],"updatedAt":"2026-03-17T07:08:36+00:00","versionOfRecord":[],"versionCreatedAt":"2025-05-07 07:12:41","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-6491416","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-6491416","identity":"rs-6491416","version":["v1"]},"buildId":"8U1c8b4HqxoKbykW_rLl7","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}