Assessment of the relationship between the maxillary sinus and the canine root tip using cone beam computed tomography

Background The purpose of the present study is to investigate the relationship between the maxillary sinus and the canine root apices in cone beam computed tomographic images (CBCT) and to assess the amount of extension of the maxillary sinus to the anterior region of the jaw in different sexes and age groups. Methods CBCT of 300 individuals (154 males and 146 females) over 20 years (with a mean age of 35.12 ± 8.40 years) were evaluated. The subjects were categorized into three age groups (20–30, 30–40, and 40–50 years). When the maxillary sinus extended to the canine area, the vertical distance between them was measured, and their relationship was classified into three types: I (more than 2 mm distance), II (less than 2 mm distance or in-contact), and III (interlock). Results 413 out of 600 maxillary sinuses (68.8%) were extended into the canine area or beyond. Among them, 15 maxillary sinuses pneumatized into the incisor area (2.5%). The prevalence of the maxillary sinuses extended to the anterior region of the jaw was not significantly different between genders. However, it was significantly less frequent in the older age group and more frequent on the left side. In addition, the mean amount of anterior extension of the maxillary sinus (mm) was significantly lower in the older age group. Type I was the most frequent vertical relationship between the maxillary sinuses and canine apices with no significant difference in gender, side, and age groups. Conclusions In most cases, the maxillary sinus extended to the canine area and sometimes reached the incisor region. This necessitates paying more attention to the maxillary anterior sextant during surgical procedures.


Background
The maxillary sinuses are the largest paranasal sinuses which are very small at birth, but expand by physiologic pneumatization until completion of skeletal development [1], or around the age of 20 years [2]. The maxillary sinus often extends from the distal aspect of the canine tooth to the posterior wall of the maxilla above the tuberosity [3]. Occasionally, practitioners encounter pneumatization of the anterior part of the maxilla by sinus extension misinterpreted as a cystic lesion on the intraoral or panoramic radiographs [4]. The relationship between the maxillary sinus and dentition is important for dental procedures, particularly implant or apical surgeries and orthodontic treatment [5,6]. Moreover, the close proximity between these structures leads to infectious spread from periodontal or peri-apical lesions to the maxillary sinus which may cause maxillary sinusitis [7][8][9].
While the anterior part of the maxilla is often assumed as a relatively safe region for surgical intervention, based on a recent cone beam computed tomographic (CBCT) study [4], the maxillary sinus extended to the canine region in 68.9% of cases and to the incisor region in 15.5%. Two-or three-dimensional (2D or 3D) imaging has been used for evaluating the paranasal sinuses.
However, in cases with accompanying signs and symptoms regarding sinuses or need for a thorough examination of the sinuses prior to surgeries, 3D imagings are the modalities of choice [9]. In this regard, CBCT provides accurate and distortion-free images of the craniofacial bones with lower absorbed radiation dose compared with multi-slice computed tomography [17][18][19].
To the best of the authors' knowledge, there are only few CBCT studies regarding the relationship of the anterior teeth and maxillary sinus [20,21]. Therefore, the aim of the present study was to assess the location of the anterior border of the maxillary sinus in relation to the teeth and amount of anterior extension of the maxillary sinus (AEMS) beyond the canine tooth long axis. Moreover, the vertical distance between the maxillary sinus oor and canine apices was evaluated. To be included in the study, the eld of view of the CBCT images should cover the entire maxilla of the individuals over 20 years and both maxillary canines should be completely erupted with closed apices.

Methods
Exclusion criteria were distorted CBCT images due to metallic or motion artifacts, history of previous apical surgery, evidence of root resorption/fracture or bony pathologies, supernumerary/missing/extracted or impacted teeth in the maxillary anterior area, congenital anomalies, or severe jaw deformities. High-buccal canines, not being in line with the incisal/occlusal surface of the dentition, were also excluded from the study.
All CBCT images were obtained using New Tom Evo CBCT unit (QR S.R.L. Company, Verona, Italy) with the following technical parameters: 3 mA, 1.8 exposure time, 110 Kvp, 0.3 mm voxel size, axial pitch, and axial thickness of 0.3 mm. The Frankfort horizontal plane of all the subjects was parallel to the oor when acquiring the images. All the measurements were done using NNT software (NNT 9.2 Image Works, Verona, Italy) by two oral and maxillofacial radiologists with consensus. One third of CBCT scans (100) were re-evaluated by the same observers after a two-week-interval.
The study sample was categorized into three age groups: 20-30, 30-40, and 40-50 years. For each subject, the most anterior limit of the anterior border of the maxillary sinus was marked on the axial image. Then, panoramic views were reconstructed based on the curved line parallel to the dental arch at the cervical area on the axial image. The axial and reformatted panoramic views served as the reference image for localization of the anterior limit of the maxillary sinus. Bucco-lingual cross-sections were prepared perpendicular to the dental arch with 0.5 mm thickness and interval (Fig 1). Then, the location of the anterior border of the maxillary sinus was recorded in relation to different teeth. In cases with maxillary sinus extension to the canine region, AEMS beyond the canine tooth long axis, the vertical relationship between the maxillary sinus oor and canine apices, and the absolute vertical distance between the maxillary sinus oor and oor of the nasal fossa (MS-NF) were evaluated.
The number of slices (cross-sections) with sinus pneumatization beyond the canine tooth long axis was counted and multiplied by the slice thickness (0.5 mm) to calculate the AEMS beyond the canine tooth long axis (AEMS=Number of slices × Slice thickness). For example, if the maxillary sinus pneumatization existed on 6 slices beyond the canine tooth long axis, the AEMS would be 3 mm (6×0.5) (Fig 2).
Vertical relationship between the maxillary sinus oor and canine teeth apices was assessed based on the following classi cation (Fig 3): Type I: Apex located below the sinus oor with more than 2 mm distance Type II: Apex located below the sinus oor with less than 2 mm distance or being in contact with it.
Type III: Apex located above the sinus oor (protruded into the maxillary sinus)

Statistical analyses
Statistical analyses were conducted using the SPSS software (version 20; IMB; Chicago; IL). Quantitative and qualitative variables were described by mean ± standard deviation (SD) and frequency (percentage), respectively. Chi-square test was used to compare the AEMS as well as the type of vertical relationship between the maxillary sinus oor and canine apex in different genders, sides and age groups. ANOVA test was performed for comparison of the mean distances (mm) between the MS-NF, and the anterior extension of maxillary sinus in different age groups. P value <0.05 was considered statistically signi cant. The intra-class correlation coe cient (ICC) was also used to evaluate the intra-examiner error.

Results
CBCT images of 300 individuals (600 maxillary sinuses (met the study criteria and were evaluated. The mean age of the subjects was 35.12±8.40 years. The study sample consisted of 146 (48.7%) women with a mean age of 34.66±8.78 years and 154 (51.3%) men with a mean age of 35.56±8.03 years old. ICC was 96% which is considered a perfect agreement.
Out of 600 maxillary sinuses, 413 (68.83%) extended into the canine area or beyond. 15 sinuses (2.5 %), which belonged to 8 subjects, involved the incisor region. The location of the anterior border of the maxillary sinuses in relation to other teeth were as follows: 149 (24.83%) into the rst premolar, 36 (6%) into the second premolar, and 2 (0.33 %) into the rst molar area.
Sinus extension had bilateral symmetry in 244 individuals (81.33%) and was non-symmetrical in 56 (18.66%). Among the cases with symmetric sinus extension, 178 cases (59.33%) extended into canine region, and 66 cases (22%) extended posterior to the canine bilaterally. Table 1 shows the frequency of the maxillary sinuses which extended to the anterior region in different genders, sides, and age groups. Anterior extension was signi cantly more frequent in the left side (P value = 0.006) and less frequent in the older age group (40-50 years old) (P value =0.001). No gender difference was found in the prevalence of anterior extension of the maxillary sinus (P value =0.377).  The mean vertical distance between the maxillary sinus oor and canine apex, in cases with extended maxillary sinus into the canine region (type I and II), was 11.99 ±5.97 mm. 25 canine apices were located above the maxillary sinus oor (Type III). Their distances to the maxillary sinus oor were evaluated separately. The mean distance in this group was 4.71±3.83 mm. Although the distance between the maxillary sinus oor and canine apex increased with increase in age, the difference was not statistically signi cant (P value = 0.207). There was no signi cant difference between the right and left sides in this regard.
The oor of the nasal fossa was located below the sinus oor in most of the cases which extended to the canine area. The mean absolute distance of MS-NF was 10.13±4.76 mm in the study population, 9.84±4.77 mm for the right and 9.49±4.60 mm for the left sides. The difference between these values was not statistically signi cant.
The mean of AEMS beyond the maxillary canine long axis was 2.03±1.17 mm with a maximum extension of 16 mm. This value was 2.25±1.18 mm for the left side which was signi cantly more than the right side (2.04±1.08 mm). Extensive pneumatization of the maxillary sinus was detected in one case which involved the entire hard plate and extended to the central incisor region (Fig 5). Table 3 shows that the mean AEMS was signi cantly lower in the 40-50 year age group compared to the other age groups (P value =0.001). Moreover, the mean distance between MS-NF was signi cantly higher in the same age group compared with the two others (P value =0.001).

Discussion
In the present study, the amount of anterior extension of the maxillary sinus beyond the canine tooth long axis and the relationship between the root apex of the permanent maxillary canine and the maxillary sinus oor were evaluated in 300 CBCT images.
The proximity of the sinus oor and root apices of the maxillary teeth is of critical importance in several clinical procedures such as endodontic surgery, orthodontic treatment, and implant placement. CBCT scans, with dedicated 3D software allow the reconstruction of the image in three orthogonal planes precise morphometric measurements, and provision of accurate information for case selection, treatment planning, and avoidance of collateral damage during the surgery [17][18][19].
The relationship between the maxillary sinus oor and posterior teeth has already been evaluated in various studies [4,[10][11][12][13][14][15][16]. In contrast, few studies have addressed the relationship between the maxillary sinus oor and canine apex [4,[20][21][22]. AL-Qasab et al. [22] evaluated this relationship in a limited sample size (30 individuals) and in periapical radiographs. Ducommun et al. [21] evaluated 83 CBCT images for the distance between the apices of the anterior teeth to the nasal oor or maxillary sinus, whichever was closer, and they did not report the results separately for each structure. Their study also included the anterior teeth with apical lesions. To the best of our knowledge, only one comparable study has been published recently which evaluated the relationships between the maxillary teeth (molars, premolars, and canine) and maxillary sinus oor in CBCT [20].
The result of the present study shows that most of the maxillary sinuses (68.83%) extended to the canine area which is almost equal to Zhang et al.'s nding (68.9%) [4]. In contrast, Kim et al. [23] and Kopecka et al. [24] reported much less percentage of canine area pneumatization by the maxillary sinus, (33% and 2.4%, respectively). Regarding the pneumatization of the incisor region, Zhang et al. [4] reported a higher frequency (15.5%) in their study population compared to the present study (2.5%).
In this study, most of the maxillary sinuses (81.33 %) had bilateral symmetry with regard to the location of the anterior border in the jaw. This nding was in accordance with previous studies [2,25,26].
Comparably, Shahbazian et al. [27] reported the symmetric morphology of the maxillary sinus in 83% of their cases, and according to Hamdy et al.[28], the average linear cranio-caudal, antero-posterior, and medio-lateral measurements were almost bilaterally-matched in all cases. Based on our results, bilateral symmetry was even more common in those maxillary sinuses which extended into the canine area.
Further studies are required to con rm this result.
Despite the reported dissimilarity of the maxillary sinus volume between different genders [25,29], the frequency of the maxillary sinus which extended to the anterior region was similar in both genders in the present study. This result is almost comparable to those reported by Jun et al. [1] who found no signi cant difference in the maxillary sinus volume between the males and females after the developmental period.
The frequency of the maxillary sinus which extended to the anterior region and also the mean AEMS beyond the canine long axis were signi cantly lower in older cases (40-50 years) compared with the other age groups. Additionally, in the vertical dimension, the MS-NF was found to be signi cantly higher in the older age group. These ndings con rm those of Belgin et al. [25], Takahashi et al. [30] and Velasco-Torres et al.
[31] who found decreasing maxillary sinus volume with increase in age. Jun et al. [1] also showed that the maxillary sinus increased in size until the completion of skeletal development in both sexes and then an age-related decrease occurred in its volume. Similarly, Ariji et al. [2] reported an increasing maxillary sinus volume up to 20 years of age and a decline process subsequently. Contrary to all these ndings, Sahlstrand-Johnson et al. [32] reported that maxillary sinus volume was not related to age in their study sample.
Oishi et al. [20] found a negative correlation between the distance of maxillary sinus oor to the root apices of all teeth (posterior teeth and canine) and age in CBCT images. The same result was found by AL Qasab et al. [22] regarding the distance between the canine apex and maxillary sinus oor in periapical radiographs. Similarly, we found that the distance between the maxillary sinus oor and canine apex increased with increase in age; however, the difference was not statistically signi cant.
As part of this study, it was found that when the maxillary sinus extended to the canine area, the canine apices, most commonly (84.99 %), was located below the sinus oor at more than 2 mm distance (type I).
It was followed by types II and III relationship with much less percentage (8.96% and 6.05%, respectively). This order was in accordance with a recent study by Oishi et al. [20]. They de ned type 0 for those cases in which sinus oor did not appear above the root apices. Types I, II and III de ne the separate, in-contact and interlock relationship between the maxillary sinus oor and canine apices, respectively. They reported that whenever maxillary sinus appeared above the canine apices, type I was the most and type III was the least frequent relationship; this is similar to our ndings.
Oishi et al. [20] assessed the proximity of the maxillary canine and posterior teeth to the sinus oor in the standard sagittal and coronal planes. However, in the present study, the classi cation and measurements were done based on bucco-lingual cross-sections perpendicular to the dental arch of each side of the jaw. This corrected plane seems to be more sensible for evaluating the relationship and distance of the root apices and the sinus oor. In their study [20], the sample size weighted toward the female group (225) which was 3 times more than the male group (76). Moreover, the number of the younger subjects was twice that of the older age group. In the present study, we tried to select a similar number of male (154) and female (146) subjects and have a uniform subject distribution in different age groups to overcome the possible biases. We recommend further studies with lager sample size and wider age span in different population to evaluate the possible population-speci c variation.

Conclusion
Within the limitations of this study, the following conclusions may be drawn: 1. Most of the maxillary sinuses extended to the canine area. 2. In most cases with the maxillary sinus extended to the canine area, the canine apex was located more than 2 mm below the maxillary sinus oor. 3. The maxillary sinus could extend into the incisor region. This is particularly important for surgical procedures and implant treatment in the maxillary anterior region.
4. Extension of the maxillary sinus to the anterior region was less frequent in the older age group. 5. The mean absolute distance between the maxillary sinus and nasal oor was higher in the older age group.

Consent to participate:
Written consent had been taken at the time of radiographic examination from all the patients for probable use of their anonymous information in future research. The form will surely be available upon the journal requirement.
Availability of data and materials: The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.  A case in which the maxillary sinus extended to the canine area. In this case, the maxillary sinus could be seen in 8 cross-sections beyond the canine tooth long axis. Thus, the AEMS in this case is equal to 4 mm (8×0.5).

Figure 3
Three types of vertical relationship between the maxillary sinus oor and canine apex on bucco-lingual CBCT cross sections: Type I (> 2 mm distance), II (2 mm < distance or contact) and III (interlock) relationship.