European Journal of Cardiovascular Medicine

One of the paranasal sinuses that the Egyptians originally identified is the maxillary sinus, which has been extensively studied regarding its structure, vascular architecture, and relationship to the teeth.[1,2] This particular study will be based on an important part of the maxillary sinus when it comes to interventional procedures, known as ‘SCHNEIDERIAN MEMBRANE.’ The mucous membrane that encloses the interior of the maxillary sinus cavity is known as the ‘Schneiderian membrane’[3]. Histologically, it is composed of highly vascularized connective tissue and an overlaying periosteum covered in a thin layer of pseudo-stratified ciliated epithelium[3,4]. Generally, the Schneiderian membrane is 1-2 mm thick. Nevertheless, its thickness can grow up to ten-to-fifteen fold when the mucosa becomes inflamed as a result of infection by organisms that are either odontogenic or non-odontogenic in origin. Mucosal thickening of the maxillary sinus is a typical radiographic observation in asymptomatic individuals in routine clinical practice; for this reason, the mucosal lining over 2 mm is deemed abnormal.[5,6] One can utilize CBCT for maxillary sinus diagnosis because CT is more expensive and radiation-prone. There are three types of reconstructions available: oblique, slice, and multi-planar (axial, frontal, and sagittal).[7] Schneiderian membrane thickness (SMT) is one of the significant factors to be considered during surgical procedures involving sinus-lifting procedures while placing dental implants in that location. Further, SMT is considered a key anatomic factor influencing sinus membrane perforation and subsequent implant failure, with membranes ≥2mm being more resistant. Schneiderian membrane thickness plays an important role in treatment planning of implant placement in maxillary posterior teeth wherein sinus lift procedures are warranted due to insufficient vertical height. The purpose of this study was to determine the relationship of Schneiderian membrane to the inflammatory pathologies of the teeth associated within the anatomic shape of the maxillary sinus including the maxillary premolars and maxillary molars.

AIM

To assess the thickness of the Schneiderian membrane in cases of inflammatory peri- apical pathologies involving periapical abscess, cyst, or granuloma in maxillary posterior teeth and, assessing the variation in its thickness based on the distance between the pathology and the membrane.

This study was an observational & retrospective study carried out in the Department of Oral Medicine and Radiology. The institutional ethical clearance was obtained, IREB Reference number: IREB/2024/OMR/05.

Sample size was determined using the estimated values from the literature - Sghaireen MG. Thickening of Schneiderian membrane secondary to periapical lesions: A retrospective radiographic analysis. J Int Soc Prev Community Dent. 2020 May 7;10(3):316-322. doi: 10.4103/jispcd.JISPCD_101_20. PMID: 32802778; PMCID: PMC7402264.

Here using the formula,

Total sample size = N = [(Z α +Z β )/C] 2 + 3

where Z α is the z variate of alpha error i.e. a constant with value 1.96, Z β is the z variate of beta error i.e. a constant with value 0.84

C = 0.5 * ln[(1+r)/(1-r)]

Inclusion –

As the sinuses are fully developed by the age of 18, scans of individuals aged more than or equal to 18 years were selected. The patients who had been advised CBCT maxilla or CBCT skull for the purpose of radiographic investigation were selected. The teeth showing evident periapical inflammatory pathologies like periapical abscess, granuloma or cyst were only selected for the study. The scans included male and female individuals who had sinus pathology and/or membrane thickening, detectable on a CBCT scan.

Exclusion-

Schneiderian membrane thickening which was in association with an edentulous region. Schneiderian membrane thickening associated with dental implants, bone grafts in or adjacent to maxillary sinus. Teeth which are not having any periapical pathology were excluded. Insufficient scan quality and movement artifacts in the CBCT images. Based on the calculated results, a total of 114 CBCT scans were selected from the archived data from the Department of Oral and Maxillofacial Radiology, for the time period between April 2023 and February 2024. The CBCT scans were recorded using Carestream CS 9600 CBCT Unit and were viewed on DELL P2422H LED Monitor. Imaging software CS 3D imaging software 9600, version 8 was used for the assessment of the scans. The scans have been obtained in the form of DICOM (Digital Imaging and Communications in Medicine) files.

Scans of the patients were evaluated for the following parameters – The presence of Schneiderian membrane thickening or any sinus pathologies (Figure 1). Measurements of Schneiderian membrane thickening in sagittal and panoramic sections (Figures 2 & 3). Distance between the base of the maxillary sinus and the tooth apex (Figure 4A). Distance between the base of the maxillary sinus and the border of the periapical pathology (Figure 4B).

Figure 1: Panoramic section showing Schneiderian membrane thickening on the left side maxillary sinus region. The right maxillary sinus shows no membrane thickening.

Figure 2: Measurement of the thickened Schneiderian membrane in panoramic section. A breach in the floor of the maxillary sinus seen in association with the teeth 17 and 18.

Figure 3: Measurement of the thickened Schneiderian membrane in the sagittal section in association with the teeth 17 and 18.

Figure 4(A): Measurement of the distance between the base of the maxillary sinus and tooth apex

Figure 4(B): Measurement of the distance between the base of the maxillary sinus and the border of the periapical pathology

Measurements were done as follows:

All the evaluation and measurements were done in the coronal and sagittal sections of the scan in the orthogonal view. The entire extension of the right and left maxillary sinus was examined individually in the anteroposterior sense on the coronal window to determine the thickening of the maxillary sinus floor. The slice thickness was 975 μm to get the accurate border of the thickening for the measurement. The Schneiderian membrane thickening was identified as it appeared as a hyper-dense layer in the inferior border of the maxillary sinus. The thickening of the Schneiderian membrane varied in each scan. The floor of the maxillary sinus was examined on both left and the right side.

Approximately 350 scans of maxilla were examined in the department CBCT system, out of which 114 samples were appropriate for inclusion in the study which showed the Schneiderian membrane thickening. The scans which did not show a hyper-dense layer of Schneiderian membrane thickening were not included in the study.

The coronal slice showing the Schneiderian membrane was selected. In the slice in which this point was identified, the guiding horizontal line of the axial slice was tangentially positioned at the point of interest, remaining fixed on this level and being shown in this position even when the coronal slice was changed, thus emphasizing the lowest point of the maxillary sinus floor.

In this slice, a vertical line was drawn, with the ruler tool, perpendicular to the guiding horizontal line, at the point of the tooth which showed a periapical pathology. The point on the periapical lesion where the maximum dimension of the periapical lesion and the Schneiderian membrane coincide will be taken into consideration. The ruler tool was then used to determine the measurements (in millimeters) in the sagittal section and the panoramic section (Figure 3).

In the same sagittal section, the measurement of the distance between the tooth and sinus is measured (Figure 4A, 4B). With a ruler tool, the distance between the tooth apex and the coinciding Schneiderian membrane is measured. In the same axis, the distance between the border of the periapical pathology and the Schneiderian membrane is measured (in millimeters).

After collecting all the necessary data, the findings were recorded in an Excel sheet and were later transferred to a master chart. This data was then subjected to statistical analysis.

Statistical analysis was done using descriptive & inferential statistics with the help of Student’s unpaired T-test and the software for the analysis - SPSS 27.0 version and GraphPad Prism 7 was used

This study included CBCT scans of 114 patients that had Schneiderian membrane thickness, detectable on CBCT scan. All the measurements were put on the tabulated form which included the name, age, gender, registration number, measurement of thickening of the Schneiderian membrane in the sagittal and panoramic section, measurement of the distance between the tooth apex and the Schneiderian membrane and measurement of the distance between the border of the periapical pathology and the Schneiderian membrane.

The patients included were of age between 17 -73 years. Among the scans taken, 48.2 % (n=55) were females and 51.8 % (n=59) males.

Inter-group comparison of mean age with Schneiderian membrane thickening was done. There was a statistically NON-SIGNIFICANT difference, seen for the values between the groups (p>0.05). This implies that the Schneiderian membrane thickening is not correlated to age in patients with periapical lesions.

Inter-group comparison of frequency of gender in relation to Schneiderian membrane thickening was done. There was a statistically a HIGHLY SIGNIFICANT difference seen for the frequency between the groups (p<0.01) with higher frequency for males with Schneiderian membrane thickening.

An inter-group comparison of frequencies of tooth number with Schneiderian membrane thickness was done. There was a statistically NON-SIGNIFICANT difference seen for the frequencies between the groups (p>0.05).

The P value is p<0.05 which indicates normality is not followed

The normality of numerical data was checked using Shapiro-Wilk test & was found that the data did not follow a normal curve; or for graded data, hence non-parametric tests have been used for comparisons.

Inter-group comparison was done using T-test. Comparison of frequencies of categories of variables with groups was done using Chi-square test. Inter-group comparison was done using Mann-Whitney U test.

For all the statistical tests, p<0.05 was considered to be statistically significant, keeping α error at 5% and β error at 20%, thus giving a power to the study as 80%.

Figure 5: Inter-group comparison of the distance between the tooth apex and Schneiderian membrane thickening

Figure 6: Inter-group comparison of the distance between the border of the periapical lesion and Schneiderian membrane thickening

An important anatomical component in maxillofacial surgery is the maxillary sinus. Prior to dental implant planning and sinus floor elevation, the operator may find significant benefits from assessing the size and pathology of the maxillary sinuses. ^[8,9,10] Consequently, in order to avoid potential surgical difficulties, accurate imaging of anatomic variations and diseases of the maxillary sinus and surrounding tissues is essential.[11,12,13]

Because the floor of the maxillary sinus is the declivity zone, which is more prominent at the level of the first and second molars,^[14,15,16] the maxillary sinus is composed of a pseudostratified epithelium with hair cells next to its own richly vascularised lamina that has contact with the bone tissue that borders the apices of the posterior teeth. ^[18,19] The Schneiderian membrane thickening was assessed using a variety of traditional and cutting-edge radiographic imaging techniques, such as magnetic resonance imaging, multi-slice computed tomography, and conventional PA. These days, CBCT is a routinely used advanced imaging tool for periodontal treatment planning evaluation, orthodontic therapy, maxillofacial surgical operations, and dental implant placement^.[14]

Recent research revealed the high prevalence of certain changes connected to the maxillary sinus, such as pneumatization,^[11] which may also play a role in the potential difficulties associated with upper jaw procedures. In doing so, the possible impact of significant confounding variables, such as the participants' medical conditions and bone density, was eliminated. In order to plan surgical therapies close to the membrane, like sinus lifting, which increases the risk of Schneiderian membrane perforation or other related complications, preoperative evaluation and assessment of the Schneiderian membrane thickening is crucial.^[12]

Comparing the thickness of the membrane between the two genders in the study, it was seen that the Schneiderian membrane thickening is greater in males than in females. In the previous study by Sghairee et al, in 2020, it was found that there is no significant difference between the membrane thickening between males and females.^[25] A few other studies gave significance for males showing more Schneiderian membrane thickening than females. The present study showed similar results as many previous studies.[11,12,17]

In this study, no statistically significant difference was found between Schneiderian membrane thickening and age. This finding was similar to several previous studies,^[16,17,18] which confirms that Schneiderian membrane thickening is not correlated to age. The study by M Rapani et al discussed the general thickness of Schneiderian membrane in various situations. The thickness of the Schneiderian membrane on cone-beam CT images was classified as Type I (not recordable), Type II (0-2 mm), Type III (3-4 mm), or Type IV (>4 mm).^[12] Based on these results it was concluded that a membrane 0-2 mm thick may be an important determinant of perforation. In the present study, we are considering a membrane more than 2mm as a pathological finding and was categorized as a positive scan for Schneiderian membrane thickening.

The Schneiderian membrane thickening is correlated to inflammatory lesions in close proximity to the sinus. Compared to average Schneiderian membrane thickening of less than 2 mm adjacent to healthy teeth, the average Schneiderian membrane thickening associated with adjacent periapical lesions was approximately 2.5 mm, which is considered a thickened Schneiderian membrane. Similar to the results of this study, various authors noted that the presence of periapical infection resulted in an increase in Schneiderian membrane thickening. ^[19,20,21]

In the present study, the periapical pathologies showed significance in showing a relation between Schneiderian membrane thickening and the periapical pathologies. The thickening of more than 2mm was considered as positive thickening, which was 83.3% amongst the 114 samples which were examined. The inter-group association of Schneiderian membrane thickening with periapical pathologies proved to show a significant association in accordance to the P-value calculated. A few other studies done before this, were successful in showing an association between Schneiderian membrane thickening and periapical pathologies. ^[21,22]

In the study by Maha Alghofaily et al, they tried to establish a relationship between the clinical symptoms and radiographic results in patients with mucosal thickening. Changes in the Schneiderian membrane may be temporary during an active disease. As this study was a retrospective analysis, it allowed them to link the association between endodontic disorders and sinus anomalies.^[22,23,24] In our present study, we have observed a significant correlation between the periapical pathologies and Schneiderian membrane thickening. The differentiating point between the previous studies and our present study is that we have measured the distance between the border of the periapical lesion to the Schneiderian membrane, and the distance between the tooth apex and the Schneiderian membrane. We found a correlation between the distance and the thickening of the Schneiderian membrane.

A significant relationship was found between the thickness of the Schneiderian membrane to the apex of the root which shows a periapical pathology. A significant relationship was found between the thickness of the Schneiderian membrane to the border of the periapical lesion showing a periapical radiolucency. It was observed in our study that decreased distance between the infection and the membrane leads to more thickening of the Schneiderian membrane. Similarly, it was observed in our study that increased distance between the infection and the membrane leads to less thickening of the Schneiderian membrane.

Schneiderian membrane thickness plays an important role in treatment planning of implant placement in maxillary posterior teeth wherein sinus lift procedures are warranted due to insufficient vertical height

In conclusion, our study demonstrated that, male patients tend to have more Schneiderian membrane thickening in comparison to female patients. The age of the patient does not show any significance with the thickening of the Schneiderian membrane.

In this study, all the maxillary molars were evaluated. Amongst them, the maxillary first molars showed the most association of periapical pathology with Schneiderian membrane thickening.

The present study mainly focused on discussing the association between periapical pathology and Schneiderian membrane thickening. A high significance was noted, and it proved that the periapical pathology in the maxillary posterior teeth showed evident Schneiderian membrane thickening assessed in cone beam computed tomography radiography. The distance between the tooth apex of the pathological tooth and the floor of the maxillary sinus showing Schneiderian membrane was noted. Along with that, the distance between the border of the periapical pathology and the floor of the maxillary sinus showing Schneiderian membrane thickening was noted. An evident significance was seen. It was observed that decreased distance between the infection and the membrane leads to more thickening of the Schneiderian membrane. Similarly, it was observed that increased distance between the pathology and the membrane leads to reduced thickening of the Schneiderian membrane.

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