The Effect of Age and Gender on the Distance Between the Maxillary Sinus Cortical Bone and Maxillary Molars: A Cone-Beam Tomography Analysis

Abstract

Apical periodontitis may be associated with odontogenic sinusitis in cases where the apex of the root is close to, or even within, the maxillary sinus. This study investigated the anatomical relationship between the cortical sinus floor and the root apices of maxillary molars in relation to age and gender. Two hundred cone-beam computed tomography exams (FOV 5 × 5 cm or 8 × 8 cm) were evaluated to determine the proximity of the roots of the molars to the maxillary sinus, according to age group and gender. The maxillary second molar is the tooth with the closest contact with the maxillary sinus, mainly the mesial–buccal root. In maxillary first molars, the palatal root is the nearest one and sometimes lies inside the sinus. Considering the age factor, in the elderly group, lower distances were found for all roots for the male group. In the elderly group, the only difference was found in the female distobuccal root of tooth 16, which was found to be shorter than the males (p < 0.05). In conclusion, the distance between the cortical bone of the maxillary sinus and the root apices varies considerably, and smaller distances were found in older females and for the upper second molar, especially the mesial–buccal root.

1. Introduction

The maxillary sinuses are the largest paranasal sinuses and present significant differences in shape and volume among the population [1]. It has a pyramidal appearance based on the nasosinusal wall and an apex that extends to the root of the zygomatic bone. The posterior wall is bounded medially by the pterygomaxillary fossa and laterally by the infratemporal fossa; it is bounded laterally by the nasal cavity, superiorly by the orbital cavity, and inferiorly by the oral cavity [2,3]. The alveolar process forms the floor of the maxillary sinus and is usually limited anteriorly by the canine and posteriorly by the third molar [2], justifying the close relationship between the roots of the maxillary posterior teeth and this anatomical structure [4]. The adult patient exhibits complete maxillary sinus growth extending from the canine to the maxillary third molar, and often, the floor of the maxillary sinus is pneumatized and follows the apical portion of the maxillary posterior teeth, beginning with the eruption of the permanent teeth. The expansion and pneumatization of the maxillary sinus may continue throughout life [4]. Given its anatomical position, proper sinus evaluation is crucial for dentists, otolaryngologists, maxillofacial surgeons, and maxillofacial radiologists.

Panoramic radiography is commonly used in routine clinical practice to evaluate the maxillary complex [4]. However, due to the anatomical complexity of this region, 2D panoramic radiographs do not provide enough information about the relationship between the root apices of the maxillary posterior teeth and the cortical bone of the maxillary sinus. Given its 2D nature, the overlapping of the image is unavoidable, and the geometric and volumetric distortions of the examined anatomical region are common artifacts [5].

An accurate three-dimensional (3D) analysis of the sinuses is paramount for multiple diagnostic and treatment applications, where the evaluation of sinus changes, remodeling, volumetric analysis, or the creation of 3D virtual models is required. Moreover, some of the most frequent surgical procedures, including implant placement, sinus augmentation, and orthognathic surgery, require an adequate sinus assessment. However, despite its advantages, cone-beam computed tomography (CBCT) is still not as commonly used by dentists as panoramic radiography because it has some disadvantages compared to panoramic radiography, such as a higher radiation dose, difficulty in reading the examination by some inexperienced professionals, and higher costs [5,6]. However, CBCT allows greater accuracy between the anatomical relationship between the root apices of the upper posterior teeth and the cortex of the sinus [7,8].

There is significant divergence in the literature regarding the prevalence and clinical significance of anatomic variants of the paranasal sinuses, including whether these variants are more common in older age groups. Therefore, the aim of this study was to evaluate the relationship between the root apices of the maxillary molars and the cortical bone of the maxillary sinus floor according to age group and gender using CBCT.

2. Materials and Methods

This study was performed after approval by the local Institutional Research Ethics Committee(CEP) of Estácio de Sá University and was registered via Plataforma Brasil, with CAAE 50594215.8.0000.5284. The manuscript of this laboratory study was written according to the Preferred Reporting Items for Laboratory studies in Endodontology (PRILE) 2021 guidelines [9] (Figure 1). The CBCT examinations of the sample were obtained from the image database of the dental radiology service of the ODT Digital Dental Clinic located in the city of Rio de Janeiro, Brazil. The Free and Informed Consent Form (FICF) used was given out by the dental radiology service.

All assessed exams were obtained using the PreXion Elite 3D tomograph (PreXion, Inc., San Mateo, CA, USA) according to the manufacturer’s specifications. A small field of view (FOV 5 × 5 cm or 8 × 8 cm) was used, and images were reconstructed with voxel sizes of 0.1 mm and 0.15 mm, respectively. The operating parameters were 4.0 mA and 90 KV, using a continuous workflow with an acquisition time of 37 s in high-resolution mode and 19 s in standard mode. The reconstruction time at high resolution was 30 s, with a slice thickness of 0.5 mm. Two hundred CBCTs were included in the study. The patient’s age range was divided into2 groups: 18–59 years old (adults) and 60 years old onward (elderly). The youngest patient was 18 years old, and the oldest was 86 years old. The final sample consisted of 98 adult patients and 102 patients in the elderly group. Regarding gender, the number of female patients was 105, while the number of male patients was 95.

Three-dimensional analyses of the images were performed using public image visualization software RadiAnt 2022.2 (DICOM viewer, Poznan, Poland). Two hundred CBCT exams were analyzed. The inclusion criteria were complete maxilla or hemimaxilla exams and the presence of at least one posterior tooth in the evaluated region. Exclusion criteria were files that were incompatible with the visualization and manipulation of images in the software used; exams that precluded the clear analysis of images in the regions of interest; exams that showed images suggestive of a foreign body in the maxillary sinus; exams that showed evidence of a surgery of maxillary sinus floor elevation, orthognathic surgery, or surgery to correct fractures of the craniomaxillofacial complex; and exams that showed included or semi-included third molars.

After analyzing the entire CBCT volume, the sagittal tomographic slices were selected for a better visualization of the relationship between the periapex of the roots and the inner cortex of the maxillary sinus adjacent to this region. The distance between the root apex of the maxillary molar and the inner cortex of the maxillary sinus was measured using the linear measurement tool (RadiAnt, DICOM viewer). This linear measurement (in millimeters) was recorded for the subsequent analysis of the anatomical relationship between the tooth and the maxillary sinus, considering the age and gender (Figure 2).

Statistical Analysis

A total of 1262 roots of maxillary first and second molars were examined. The data distribution was tested for normality using the Shapiro–Wilk test. Then, the Mann–Whitney test was used to compare the distances (mm) from each root apex to the maxillary sinus between the identical roots of the left and right sides of the maxilla and between male and female genders. Comparisons of the overall data between adult and elderly groups and between same-gender and same-age groups were also performed. In addition, a group comparison was made using the Kruskal–Wallis test to evaluate the distance differences between the same tooth roots in the maxillary first and second molars. All values were analyzed using Prism 7.0 (GraphPad Software, Inc., La Jolla, CA, USA) and expressed as median, minimum, and maximum values. The significance level was set at 5%.

3. Results

The median values of the distances from the root apex to the maxillary sinus in the adult and elderly groups and the correlation with gender are shown in

Table 1. Median, minimum, and maximum values of distances between the apical foramen of the roots to the maxillary sinus (mm) for the overall adult group and for female and male adult groups.

Adult Group	Overall Median (Min–Max)	Female Median (Min–Max)	Male Median (Min–Max)
MB 16	1.63 (0.00–16.29)	2.31 (0.00–16.29)	1.50 (0.00–4.80)
DB 16	1.79 (0.00–10.09)	2.04 (0.00–10.09)	1.28 (0.00–5.84)
P 16	1.00 (0.00–12.45)	1.07 (0.00–12.45)	0.77 (0.00–5.18)
MB 17	0.42 (0.00–11.87)	0.41 (0.00–9.40)	0.21 (0.00–11.87)
DB 17	0.70 (0.00–13.76)	0.86 (0.00–10.64)	0.00 (0.00–13.76)
P 17	1.29 (0.00–12.27)	1.28 (0.00–11.92)	1.50 (0.00–12.27)
MB 26	1.07 (0.00–11.14)	1.28 (0.00–11.14)	0.86 (0.00–9.72)
DB 26	1.09 (0.00–11.19)	1.72 (0.00–11.19)	0,89 (0.00–7.89)
P 26	0.64 (0.00–10.68)	0.70 (0.00–6.67)	0.50 (0.00–10.86)
MB 27	0.86 (0.00–6.36)	0.92 (0.00–5.63)	0.64 (0.00–6.36)
DB 27	1.10 (0.00–8.85)	1.23 (0.00–5.96)	0.89 (0.00–8.85)
P 27	1.14 (0.00–9.71)	1.50 (0.00–9.71)	1.03 (0.00–9.20)

MB—mesial–buccal; DB—distal–buccal; P—palatal.

. Comparisons of the overall data of the adult group revealed significant differences between the palatal (P) root of tooth #16 vs. tooth #26 (p < 0.05) and the mesiobuccal (MB) roots of tooth #17 vs. tooth #27 (p < 0.05). In the elderly group, significant differences were found only between the MB root of tooth #16 vs. tooth #26 and the P root of tooth #27 vs. tooth #17 (p < 0.05). The Mann–Whitney test revealed no differences in distances comparing the same root of left and right sides (16 vs. 26 and 17 vs. 27) in the adult and elderly groups (p > 0.05).

3.1. Overall Comparison Between Genders

When the groups were compared in terms of gender, the shorter distance to the maxillary sinus was found in the P root of tooth #27 for adult males compared to the female P root (1.03 mm vs. 1.50 mm) (p < 0.05).

3.2. Adult vs.Elderly Tooth Comparison

The results of overall age groups revealed a significant difference in the median distance of the MB root apex towards the maxillary sinus of tooth #17 (0.79 mm of adult vs. 0.42 mm of elderly groups) and in the DB root of 0.70 mm (adult) vs. 1.03 mm (elderly) (p < 0.05).

In tooth #26, the adult group showed significantly shorter spacing (1.07 mm) than the elderly group (3.17 mm) in the MB root, 1.09 mm (adult) vs. 3.19 mm (elderly) in the DB root, and 0.64 mm (adult) vs. 1.91 mm (elderly) in the palatal root (p < 0.05).

Finally, tooth #27 also showed significant differences in the roots of MB (0.86 vs. 1.26 mm) and P (1.14 vs. 1.57 mm) in the roots between the adult and elderly groups (p < 0.05).

Figure 3 shows the mean distance in mm of each root in relation to the maxillary sinus by age group. In both the elderly and adult age groups, the MB root of the second molar had the lowest mean value, as did the P root of the maxillary first molar. In addition, the average readings were higher in elderly patients than in adult patients, and it was noticeable that, in adult patients, the male gender had greater proximity to the maxillary sinus, whereas in elderly female patients, contact with the maxillary sinus was more frequent. The mean values of the measurements between female and male adults show that the lowest mean values were found in male patients (Figure 3).

Figure 4 compares the mean value of measurements between female and male individuals in the elderly and shows that the lowest mean value was found in female patients, i.e., in the gender with greater proximity to the maxillary sinus. Figure 5 shows the mean measurements of each root of maxillary molars in elderly patients according to gender, showing lower measurements for women.

In Figure 6, the mean values of the left and right sides were compared. In both adults and the elderly, the mean values are close to each other, i.e., there are no significant differences.

On the other hand, when the groups were compared between adults and the elderly of the same gender (Figure 7), the distance between the female MB root of tooth #16 was higher in the adult than in the elderly groups (p < 0.05). The distance between the female MB and the P roots of tooth #26 and the DB root of tooth #27 was higher in the elderly groups than in the adult group (p < 0.05). Finally, no significant differences were found between male gender and adult versus elderly groups (p > 0.05), as shown in Figure 8.

The median values of the distances from the root apex to the maxillary sinus in the elderly groups and the correlation with gender are shown in

Table 2. Median, minimum, and maximum values of distances between the apical foramen of the roots to the maxillary sinus (mm) for the overall elderly group and for female and male adult groups.

Elderly Group	Overall Median (Min–Max)	Female Median (Min–Max)	Male Median (Min–Max)
MB 16	2.31 (0.00–16.29)	1.3 (0.00–16.29)	3.33 (0.00–4.80)
DB 16	3.21 (0.00–10.09)	2.02 (0.00–10.09)	4.4 (0.00–5.84)
P16	2.19 (0.00–12.45)	1.32 (0.00–12.45)	3.07 (0.00–5.18)
MB 17	1.95 (0.00–11.87)	1.87 (0.00–9.40)	2.04 (0.00–11.87)
DB 17	2.49 (0.00–13.76)	2.3 (0.00–10.64)	2.69 (0.00–13.76)
P17	2.39 (0.00–12.27)	2.28 (0.00–11.92)	2.5 (0.00–12.27)
MB 26	3.86 (0.00–11.14)	3.69 (0.00–11.14)	4.03 (0.00–9.72)
DB 26	3.5 (0.00–11.19)	3.31 (0.00–11.19)	3.7 (0.00–7.89)
P26	2.29 (0.00–10.68)	2.42 (0.00–6.67)	2.16 (0.00–10.86)
MB 27	1.74 (0.00–6.36)	1.68 (0.00–5.63)	1.81 (0.00–6.36)
DB 27	2.33 (0.00–8.85)	2.11 (0.00–5.96)	2.56 (0.00–8.85)
P27	3.13 (0.00–9.71)	2.16 (0.00–9.71)	4.11 (0.00–9.20)

.

4. Discussion

Maxillary sinusitis of endodontic origin is a frequent condition found when one or more teeth in the maxillary posterior region present endodontic infection. It can also be associated with endodontic treatment, apical periodontitis, and the position of the root apex in contact with the floor of the maxillary sinus [1,2,3,4]. The anatomical proximity between the root apices (especially from molars) and the sinus cortices makes periradicular pathology a potential source for the spread of this infection into the maxillary sinuses [3,4]. In this case, it is important to use an accurate imaging examination such as CBCT, which provides high-resolution images of the teeth and adjacent tissues in all planes, including the relationships between these structures to determine the distance between these anatomical structures and provide data to help physicians establish correct protocols [2,3,4].

It is necessary to emphasize the accuracy and sensitivity of CBCT compared to two-dimensional radiographs for the diagnosis of sinus changes, the assessment of the quality of endodontic treatment, and the detection of periapical lesions [2,3,4]. In the last 10 years, studies have adopted CBCT examination as the first choice for the evaluation of the paranasal sinuses and adjacent teeth [9,10]. For these reasons, CBCT scan was used to assess the study’s data, which allows an accurate measurement of the root apex–sinus distance. The used CBCT scanner was the PreXion Elite 3D tomograph (PreXion, Inc., San Mateo, CA, USA) with a small field of view (FOV 5 × 5 cm or 8 × 8 cm), which is considered the best protocol for endodontic assessments [3,11,12].

Previous studies [10,11,12,13,14] had already evaluated the relationship between the root apices of maxillary teeth and the inner cortical bone of the maxillary sinus floor by age group, as their understanding is essential for planning endodontic treatments, extractions, and implant planning. The maxillary second molar is located closer to the maxillary sinus [15,16], mainly with the MB root, while in the maxillary first molar, the root that extends more regularly into the maxillary sinus is the palatal one [15,16,17,18], which is consistent with the results of the present study.

Previous studies [17,18,19,20] in which volumetric analysis of the maxillary sinus was performed have shown that the maxillary sinus is generally closer to the region of the root apex in adolescence and adulthood, but with advancing age, the distance between the anatomical structures decreases [19], which is consistent with the results of this study. Maxillary molars with periapical lesions where their roots are in contact with the maxillary sinus may lead to maxillary sinus infections [21]. Special attention should be paid to the treatment of the MB canal, especially MB2, since the presence of apical periodontitis in this root may lead to sinusitis due to its proximity to the maxillary sinus [22].

Studies have reported that the anatomical variation in the maxillary sinus may also be related to different ethnicities [20,23], but in this study, it was not possible to perform this analysis because the ethnicity of the patients was not reported in the patient files.

Regarding gender dimorphism, some authors [23,24,25] have shown that male patients tend to have a larger maxillary sinus, and therefore, there is a greater likelihood of proximity between the root apices of the posterior teeth and the maxillary sinus. No relationship between the gender of the patient and the anatomical relationship between the structures was reported [15,20,26], which is similar to the results of this study.

Regarding the contraposition of the sides of the hemimaxilla, non-significant differences were reported in previous studies [24,27,28] and in this study. The analysis showed that the maxillary second molar is the tooth that has the closest contact with the maxillary sinus, especially with the MB root. In the maxillary first molar, the P root has the strongest contact with the sinus cortex. In addition, the greater the age, the greater the proximity between the maxillary sinus cortical and the root apices.

The close anatomical relationship between the root apices of the posterior maxillary teeth and the cortex of the maxillary sinus floor is in consensus in the literature [2,4,29,30,31]. According to Coutinho et al., 2020 [32], the close anatomical relationship between the root apices and the maxillary sinus did not show direct repercussions on the maxillary sinus. However, when the relationship between the presence of periradicular lesions and the maxillary sinus was taken into consideration, it was observed that among the sinuses considered healthy, the prevalence of lesions below the maxillary sinus cortex was 70.34% (n = 121) versus 27.9% (n = 48) of lesions close to the maxillary sinus but with maintenance of the cortical integrity, with only 1.74% (n = 3) of cases with lesions presenting rupture of the cortex of the maxillary sinus floor. In this study, it was observed that only this relationship is critical in the face of changes in the periapex [31,33].

5. Conclusions

The proximity between the cortical bone of the maxillary sinus and the root apices varies between the sides. Smaller distances are found in older females and for the upper second molar, especially the mesial–buccal root.