Anatomical study of the maxillary sinus: which characteristics can influence its volume?

To investigate whether there is a relationship between the volume of the maxillary sinus and individual parameters such as gender, side, posterior tooth absence, sinus membrane thickening, bony septa, vertical and sagittal skeletal patterns. The tomographic volume of the maxillary sinus from 211 individuals (422 sides) was evaluated using Horos DICOM Viewer Software. Bony septa and sinus membrane thickening were classified as absent or present. At the same time, loss of one or more teeth in the posterior region of the maxilla (except for the third molars) was considered. The t test was applied to analyze maxillary sinus volume according to gender, age, side, posterior tooth absence, sinus membrane thickening and bony septa. A one-way analysis of variance (ANOVA) with Tukey’s post-hoc test was applied to compare sagittal and vertical patterns. Pearson’s correlation coefficient was also used to verify the association between maxillary sinus volume, age and skeletal patterns. Concerning the sagittal skeletal pattern, a statistically significant difference was observed between Classes II and III (p = 0.05) and it was confirmed by the Pearson’s correlation coefficient (r = − 0.107/p = 0.029). No statistically significant differences were observed between the maxillary sinus volume according to gender (p = 0.06), side (p = 0.37), posterior tooth absence (p = 0.92), sinus membrane thickening (p = 0.47), bony septa (0.89) and vertical skeletal pattern (p = 0.67). No significant differences were observed with age (r = − 0.076/p = 0.109) and the vertical skeletal pattern (r = − 0.078/p = 0.108). Maxillary sinus volume was influenced by the sagittal skeletal pattern and was higher in Class III individuals.


Introduction
The formation of the maxillary sinus begins in the 10th week of intrauterine development, during the primary process of extension, which is filling the air to increase volume. In the 20th week of pregnancy, when secondary pneumatization occurs, the maxillary sinus extends to the maxilla, measuring approximately 6-8 cm 3 at birth [6,11,28]. Subsequently, it continues to develop both laterally and inferiorly during rapid growth, from birth to 3 years of age and the second from 7 to 12 years of age [6]. The consecutive inferior growth is related to its invasion into the alveolar process, following the eruption of the permanent teeth, until finally extending 4 to 5 mm inferiorly to the nasal floor, presenting an average volume of 15 cm 3 between eighteen and twenty years of age [6,24].
The paranasal sinuses' development co-occurs with the viscerocranium bones, which are more extensive in the vertical and more minor in the horizontal direction. A relationship between the size of the facial bones and the maxillary sinus, which is the first paranasal sinus to be formed, is suggested [13]. The maxillary sinus may reflect the development of bony structures, which must be associated with determining the shape of the face's middle third. It is suggested that the maxillary sinus must play a crucial role in forming facial contours [11]. 1 3 In addition, a thin cortical structure in the maxillary sinuses, known as bony septa, is often on the sidewalls and floor. It may divide the sinus into two or more spaces. When they develop before birth, they are known as primary septa. The secondary septa appear after dental extractions, resulting from pneumatization of the maxillary sinus floor [8,23].
Sinus septa are thin, fragile, sickle-shaped bony projections inside the maxillary sinus. When located on the sinus floor, they present a greater chance of surgical complications because they firmly adhere to the maxillary sinus membrane, and alternative surgical access is recommended [8,23]. Another classification used to assess septa is orientation, which can be sagittal, mediolateral, or transversal [28]. In studies that used three-dimensional exams, the prevalence of bony septa in the maxillary sinus ranged from 25 to 70% [14,23].
Different studies have already measured the size, growth, and development of the maxillary sinus through dry skulls [31], panoramic radiographs [18], cone beam computed tomography (CBCT) [11,24], multidetector computed tomography (MDCT) [11,13,17,21] and magnetic resonance [2]. It is still controversial in the literature which factors are directly associated with the maxillary sinus volume due to the difficulty of following its development in individuals who do not present abnormalities in the bones of the face. In addition, measuring the maxillary sinus volume in clinical practice is difficult due to its location within the middle third of the face [17]. So, we aimed to investigate the relationship between the maxillary sinus volume with gender, side, posterior tooth absence, sinus membrane thickening, bony septa, and vertical and sagittal skeletal patterns. ). Based on a population size of 300 subjects, an expected frequency of 50%, an acceptable margin of error of 5%, and a 99% confidence level, this power calculation showed that at least 207 subjects were necessary for the investigation.

Materials and methods
The multidetector CT images from individuals over 18 years old were acquired as part of preoperative planning for orthognathic surgery. The images were acquired on a 64-channel device (Light Speed VCT; GE Healthcare Bio-Sciences, Piscataway, NJ, USA), operating at 120 kV and 200 mA, with a thickness/increment of 0.6 mm and Field of View (FOV) of 32 cm (full face). A total of 300 individuals were selected and submitted to a qualitative visual assessment of the maxillary sinus's anatomical variations in coronal, sagittal, and axial slices. It excluded images with poor quality, trauma or fracture in the face, pathological lesions in the maxilla, cleft lip and palate syndromes, previous facial surgery, and severe asymmetries. After the exclusion criteria, the final sample consisted of 211 individuals (422 maxillary sinus). Horos DICOM Viewer software (Horos Project, Geneva, Switzerland) was used to measure the volume of the maxillary sinuses. Bony septa and sinus membrane thickening were classified as absent or present. The normal mucosa's thickening would be above 2-3 mm according to Janner et al. [10]. At the same time, loss of one or more teeth in the posterior region of the maxilla (except for the third molars) was considered.
All the analyses were performed by a previously trained investigator with experience evaluating MDCT images. The zoom tool and brightness and contrast adjustments were allowed. Each maxillary sinus was delimited in the coronal slice every 3 mm. For this purpose, the "closed polygon" tool was selected, and images corresponding to the maxillary sinus contour were traced with a pointer in the innermost part of the sinus cortex. Then, the "calculate volume" tool was applied to generate the maxillary sinus volume measurement automatically (Fig. 1). After 30 days, 25% of the sample was re-assessed to calculate intraexaminer reproducibility.
Data were analyzed using IBM SPSS Statistics for Windows, version 22 (IBM Corp., Armonk, NY, USA). The intraclass correlation coefficient (ICC) was determined to assess intraexaminer reproducibility based on the Koo and Li [12] classification, i.e., poor (< 0.5), moderate (0.51 to 0.75), good (0.76 to 0.9), and excellent (> 0.91). The t test was used to analyze maxillary sinus volume according to sex, age, side, posterior tooth absence, sinus membrane thickening, and bony septa. A one-way analysis of variance (ANOVA) with Tukey's post-hoc test was applied to compare sagittal and vertical patterns. Pearson's correlation coefficient was also used to verify the association between maxillary sinus volume, age, and skeletal patterns. The significance level was set at 5% for all analyses.

Results
A total of 89 MDCT examinations were excluded. The final sample consisted of 211 individuals, including 125 women and 86 men, with a mean age of 32.58 (± 12.86 years). The ICC values demonstrated excellent intraexaminer reproducibility (0.998) in measuring the maxillary sinus volume. Comparisons of maxillary sinus volume with gender, side, posterior tooth absence, sinus membrane thickening, bony septa, and vertical and sagittal skeletal patterns are summarized in Table 1.

Discussion
The shape and size of the maxillary sinus can be easily observed in MDCT, and there have been many attempts to obtain its volumetric information, as it is the best index for measuring the paranasal sinuses [2]. In the present study, the volumetric analysis of the maxillary sinus allowed us to identify significant differences between Class II and III individuals. It is essential for implant planning, sinus lifts, dental extractions [15], and skeletal anchorage devices in orthodontics [29]. Additionally, the dimension and volume of the maxillary sinus are significant findings to be evaluated in orthodontic treatment planning, especially in cases with extractions, as the teeth are moved mesially and distally; in the intrusion of upper molars and premolars due to the alveolar extension of the sinus; and during the angulation of impacted maxillary teeth, as the impaction depth is affected by the dimensions of the maxillary sinus [17].
In this study, despite the cone-beam computed tomography (CBCT) emits a lower radiation dose than MDCT [20], a large FOV was necessary and justified for orthodontic/surgical planning since orthognathic patients with jaw deformities are traditionally referred to radiology departments for an MDCT scan of the skull for treatment planning. This preoperative scan enables surgeons to perform facial measurements to evaluate the deformity and guides the design and fabrication of the surgical splints used during surgery [27]. In addition, according to Gaia et al., linear measurements obtained from MDCT (0.6 mm resolution) and CBCT (0.25 mm resolution) images are precise and accurate [4]. Furthermore, a common critique of CBCT is that it cannot accurately measure soft tissue. In orthognathic surgery, soft tissue measurements and predictions are essential for preoperative analysis and treatment planning [33].
Methodologically, this investigation chose MDCT images because they are considered gold standard exams in the morphometric evaluation of the maxillary sinus. It overcomes the overlap, distortion, and magnification observed in twodimensional radiographs; in addition, it allows good visualization and distinction between bone tissue, adjacent mucosa, and air [11,13]. Studies using CT images commonly have used three-dimensional reconstructions to quantitatively measure the volume of the maxillary sinus and software combined with an imaging tool [11,21].
Volumetric measurements depend on the manual skill and experience of the observer; therefore, any inaccurate mapping of the sinus outline may influence the automatically calculated volume index [21]. Some authors estimate that a mathematical calculation finds the maxillary sinus volume based on three linear measurements (higher width, height, and length) [15]. However, these linear measurements may differ from the anatomical values since the maxillary sinus is a complex anatomical structure that does not have uniform boundaries. A previous study [21] identified an excellent correlation between manual and automatic methods for volumetric evaluation of the maxillary sinus. This suggests that manual delimitation, followed by automatic volume calculation, is the most accurate since it prevents the volume from being underestimated in mucosal thickening. For this reason, the semiautomatic method was performed in this investigation.
According to the present study, no significant differences were observed in the maxillary sinus volume according to gender and side. This finding corroborates with other studies [2,15,18]. On the other hand, other studies [6,25,29] found a significantly higher maxillary sinus volume in males, probably because of the greater proportions of the male face.
Previous CT-based studies have shown that several anatomic structures may influence the vertical and sagittal skeletal patterns [3,16,19,22,29,30]. In this context, when evaluating the relationship between the maxillary sinus volume and the different vertical skeletal patterns, the increase in the gonial angle found in hyperdivergent patients in the present study indicates a decrease in the sinus volume. This result was also seen in the work by Okşayan et al., where the hypodivergent group showed significantly better results than the hyperdivergent group in the right maxillary sinus length parameter (p < 0.05) [17]. Based on the sagittal skeletal pattern, Shrestha et al. [25] found that the maxillary sinus volume in Class II individuals was significantly larger than in Class III individuals. In our study, we found the opposite result, with Class III individuals having a considerably larger maxillary sinus volume than Class II individuals. This could be justified because of the small sample or other factors, e.g., airway space proportions and ethnic and racial differences in the population. In our study, no significant association between volume and status of the posterior maxillary dentition (complete or incomplete), in agreement with a previous study [24]. However, Velasco-Torres et al. [32] found the total maxillary sinus volume to be significantly smaller in fully and partially edentulous patients than in dentate subjects. This finding was influenced by age, as older patients had a smaller volume, regardless of gender and edentulism status [32]. Our study sample was from preoperative planning for an orthognathic surgery image bank. Therefore, we did not have individuals with full edentulism to compare with full dentate to assess the maxillary sinus volume. More studies are needed to verify the tooth absence in the shape and size of the maxillary sinus.
The prevalence of bony septa in the maxillary sinus ranged from 25 to 70% [14,23]. In our study, 47% of the maxillary sinus presented with bony septa, without a significant difference in the maxillary sinus volume. The correct identification of the bony septa is essential for safer surgical interventions and implant placement, as previous studies have shown that the presence of septa increases the risk of perforation during a sinus lift procedure and is associated with thinner sinus mucosa, especially in cases where the longitudinal or incomplete (secondary) arrangement may indicate a more complicated procedure during membrane elevation compared to the transverse structure of the bony septa [7,9,24,29]. Moreover, some authors concluded that to assess the risk of injury of surgically significant anatomical structures in the maxillary sinus and hard palate, the operator should have preoperative three-dimensional images in their mind based on anatomical knowledge and palpation [9].
The thickening of maxillary sinus membrane is considered a variation of normality or anatomical and could be affected by odontogenic inflammatory and other sinus conditions, such as mucous retention pseudocysts or sinus opacification [5,7,9], though, were not registered in this study. Hung et al. [7] reported that the exact cause-effect relationship between sinus pathology and accessory maxillary ostia dimensions should be further assessed. In the present study, the maxillary sinus volume was not influenced by the presence or absence of membrane thickening. However, only sinus membrane thickening was evaluated with values above 3 mm [10]. We decided not to measure it because the thickness of the sinus' mucosa varies throughout the maxillary sinus, depending on the region is more or less thick, therefore it is not uniform. Other sinus conditions, such as mucous retention pseudocysts or sinus opacification, were not registered in our study. Therefore, future studies are necessary to verify the influence of pathological conditions on the maxillary sinus volume measured.
Among the study's limitations was a cross-sectional radiological study using a convenience CT sample. The fact that we used an image database of patients who would undergo orthognathic surgery planning limited the sample size, especially with no clinical information about the respiratory, immunological or metabolic conditions of the individuals. Also, could be provided great ethnic diversity studied group. We believe that there is a possibility of the selected patients not being truly representative of the general population, since there was a mixed sample. Another study with specific sample or groups would not justify using tomography for the higher radiation dose. About the thickening of the mucosa, we decided not to measure because the thickness variation of the sinus' mucosa along the maxillary sinus. Before that, the membrane was not measured in the present study and the cause-effect was not available because we did not have sufficient clinical data to predict that they would influence the diagnosis. In addition, only volumetric measurements of the maxillary sinus were performed. Further multicentric studies using larger samples for each skeletal pattern, different races, and other respiratory or metabolic conditions are necessary.

Conclusion
The maxillary sinus volume was influenced by the sagittal skeletal pattern and was higher in Class III individuals. The parameters of gender, age, side, posterior tooth absence, sinus membrane thickening, bony septa and vertical skeletal pattern seem to have no relation between the maxillary sinus volume.

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