An Analysis of The Relationship between The Maxillary Molars and The maxillary sinus floor in Adult Patient Using Cone-beam Computed Tomography

Background The aim of the study was to evaluate the anatomical relationship between the maxillary molars and the maxillary sinus by using cone beam computed tomography (CBCT). Methods A database of maxillary molars were obtained from 91 adult patients by means of images of CBCT. The internal angle, the alveolar bone width, and the distance between root apex and the wall of maxillary sinus were measured by CBCT. The vertical relationship between the maxillary molars and the maxillary sinus were analysed. Vertical relationship of the maxillary sinus was further evaluated. Results The value of the internal angle of maxillary third molar is 17.2 ± 11.5°. The width of the alveolar bone of third molar is 8.2 ± 1.7mm. Type III, IV and V were the most common relationship in the first and second molars. Type V and I were most frequently observed in the first and second molars. The inner angle of the second molar is larger than that of the first molar. The maxillary first molar had the smallest mean alveolar bone width, and the third molar had the largest average. Conclusion This study will provide reference for clinical practice, especially for root canal treatment and tooth implants.


Background
The position of the maxillary posterior teeth region is closely related to that of the maxillary sinus regarding the oral craniofacial anatomy. The close relationship between the maxillary sinus and the roots of the maxillary posterior teeth can lead to accidental oroantral communication. Special care must be taken in treatment planning in the maxillary posterior region. 1 For fear of the potential risk of perforation of the maxillary sinus floor during periapical surgery, this area has been considered as a restricted area 3 for dental implantation.
What is more, it is not unusual that infection of the root canal system may spread through the periapical tissues and reach essential anatomical structures resulting in several complications. The anatomical proximity of the root apices of the maxillary posterior teeth to the maxillary sinus floor may develop inflammatory, infectious or traumatic changes in the maxillary sinus. Pagin O figure out the relation between these anatomic structures should be considered in order to prevent an iatrogenic procedure and minimize the risks from an infectious disease within the sinus 2 . Even worse, incorrect or unstandard operational process during root canal treatment, such as overinstrumentation, overirrigation and overfilling, can raise the risk of making inroads for foreign materials into the maxillary sinus. Thus, the linear, angular and positional relationship between the maxillary posterior region and the maxillary sinus should be fully and clearly studied so as to provide meaningful referential value for making preoperative plans, for a reduced risk of failing tooth extraction or root canal treatment. The study of Lavasani SA et al shows an understanding of the maxillary posterior tooth anatomy for apical resection is beneficial to the endodontist 3 . At the same time, accurate imaging is mandatory for proper planning and implant placement prior to surgery. Although the first modern dental implant was performed in 1952, dental implant placement in the maxilla has not been widely implemented due to close proximity of the maxillary sinus and complications arising from surgery. The assessment of the location of the maxillary molars and premolars, the maxillary sinus, as well as the angulation of the alveolar crest and, in particular, the bone volume, is often a prerequisite for an appropriate planning. Jang JK et al think understanding the relationship of maxillary posterior teeth with the sinus floor and buccal cortex could provide clinicians valuable information to help reduce iatrogenic damage 4 . 4 Over the past years, some traditional methods such as X-ray periapical film and curved fault plane have attempted to evaluate the positional relationship between the maxillary posterior teeth and the maxillary sinus, whereas they have unignorable limitations.
Imaging problemaxillary sinus such as image overlap and distortion lower the precision of evaluating realistic anatomical positions. To be more precise, periapical radiographs were unable to determine the risk of perforation of the maxillary sinus floor during periapical surgery. Furthermore, because of the complex relationship between the adjacent structures, the exact relationship and measurement between the displayed root and the maxillary sinus is often inaccurate. Thanks to the rise of clinical application of cone beam computed tomography (CBCT), it can serve as an aid in the diagnosis and planning for the obscure and kotty dental diseases. It uses a rotating pyramidal shaped X-ray beam with detector in order to reconstruct axial images based on the defined volume by a single rotation. The importance of CBCT scans in the analysis of the morphological characteristics of the maxillary sinus and its relationship with the roots of the maxillary molars has been shown in some studies previously. CBCT has the advantages of undistorted image, high spatial resolution, accurate 3D angle and line lifting measurement. Lan M's team 5 , Ilgüy D et al 6 and Yoshimine S 7 figure out for an appropriate approach on dental implant treatment, evaluation of maxillary sinus and maxillary posterior teeth using CBCT can be recommended. In a nutshell, Cone-beam computed tomographic imaging is an effective method to study the position of the posterior teeth roots to the maxillary sinus floor 8 and it enabled better evaluation of maxillary sinus, posterior teeth and surrounding structures compared to other imaging tools 9, 10, 11 . CBCT imaging may assist surgeons to plan grafting and osteotomy procedures, while avoiding neurovascular structures 12 .

5
To date, few studies have combined the alveolar bone width, the internal angle and the relationship between the maxillary molars and the maxillary sinus to offer valuable information to clinicians. The study of Shokri A's team confirmed that protrusion of teeth roots into the maxillary sinus is more common in male than female 13 . Our study also takes gender into consideration. This time, we related image with clinical applications to provide a strong basis for clinical operations so as to avoid unnecessary accidental errors during dental practices.

Study sample
A database of 819 maxillary molars from 91 adult patients were obtained by using CBCT.
The patients included 24 males (26.37%) and 67 females (73.63%)with a mean age of 25.1 years (range, 18-41 years). Maxillary molars measurements were made on available CBCT images taken for the purpose of dental treatment for the maxillary premolars and molars.
All teeth were present without any malformations or bony defects in the maxilla. This study was approved by Tongji University, School of Dentistry. All patients were provided written informed consent before participating in the study. Furthermore, our research was conducted in full accordance with the World Medical Association Declaration of Helsinki. The internal angle (a), formed by the long axis of the maxillary premolars and the long axis of the alveolar bone, was measured on the cross-sectional CBCT images in accordance with the method of yoshimine et al. 9 7 Classification of the positional relationships in the direction of the axis of the tooth between the maxillary molars and the inferior wall of the maxillary sinus on the cross-sectional images.

CBCT Image Acquisition and Analysis
The vertical relationships in the direction of the axis of the tooth between the maxillary molars and the inferior wall of the maxillary sinus were evaluated and divided into 5 categories according to a revised standard according to the standard stated by the Yoshimine et al. 9 , as follows, Type I, the inferior wall of maxillary sinus is higher than the buccal root apex and palatal root apex of maxillary molars.
Type II, the inferior wall of the maxillary sinus is below the line formed by buccal root apex and the palatal root apex of the maxillary molars.
Type III, the buccal roots of the maxillary molars have a direct contact with the maxillary sinus inferior wall, and the palatal root apex of the maxillary molars is lower than the maxillary sinus inferior wall.
Type IV, the palatal roots of the maxillary molars have a direct contact with the maxillary sinus inferior wall, and the buccal root apex of the maxillary molars is lower than the maxillary sinus inferior wall.  Table I. Having completed the process of statistics, the internal angle of maxillary third molar (17.2 ± 11.5°) is obviously bigger than the other two teeth type (P<0.01). The 9 width is larger in third molar (8.2 ± 1.7mm). It can be easily seen that significant deviations exist between third molar and the other two teeth types. However, no distinct differences can be observed within the first molar teeth type and the second molar teeth type, respectively.
The distributions of the vertical relationships were classified into 5 categories and can be observed in Table II. As is shown in the table. The relation between tooth area and type of mentioned classification was statistically meaningful (p < 0.001). Accordingly, as for the vertical relationships, type III, IV and V relationship in which the maxillary sinus inferior wall is lower than the buccal root or palatal root of maxillary molars was most frequently observed with the first and second molars (73.4%, 74.4%). Meantime,the most common type observed in the first and second molars was type V (50.9%,50.3%)and type I (23.1%, 23.1% , accounting for more than 70 percent of the teeth collectively. Concerning the third molar teeth, the two types (type V and type I) are also most frequently observed, with rather similar percents (38.6% and 39.4%). Overall, type II is the least popular type among all the individual teeth type.
The means and SDs of the measurement of internal angle and bone width by categories on the cross-sectional 3-D CT images of CBCT are illustrated in Table III and Table V. In first molars and second molars, the angle is larger in latter ones. Compared to other types, the internal angle in Type III on the maxillary first molars (6.2±4.0°) is smaller with a great extent. In a sharp contrast, for second molars and third molars, the angle in Type III, which is 14.6 ± 8.7° and 23.1 ± 8.8° respectively, is significantly larger than the other types. For purpose of exploring the correlation between the mean distance and the mean internal angle, we conducted 2-tailed Pearson correlation statistic. As a consequence, there is weak correlation in the first molar teeth type(r = 0.457, p<0.05) and third molar teeth type, in type III(r = -0.400, p<0.1), meaning that some significant relation can be drawn from these two parameters in type III. Turning to the bone width (mm) in the mesial-distal direction of maxillary molars, no evident differences can be found among the 5 categorie in first molars, with a mean width of 7.8mm. Morever, the bone width in the mesial-distal direction of Type IV was largest on second molars (8.1 ± 0.6mm) and third molars (9.1 ± 1.5mm) among all the types.
The distance from each root apex (mesiobuccal root, distal buccal root and palatal root) to the inferior wall of maxillary sinus in the direction of the axis of the tooth of maxillary molars are shown in Figure.I. In general, in two-rooted maxillary second molars and third molars, it is that BL (1.31mm and 0.22mm) was larger than PL(1.83mm and 2.16mm). The distances of each root apex to the maxillary sinus interior wall in three-rooted molars were arranged as follows, PL>DBL>MBL. In conclusion, the distance of third molars (0.22mm) is smallest and that of first molars (1.37mm) is largest.
Regarding the mean distance of each apex to the inferior wall of maxillary sinus in the direction of the axis of the tooth, there exists statistically meaningful differences between in gender. To be more precise, for molar teeth type, longer distance exist between maxillary sinus and root apice of female, especially on second and third molar teeth (1.57mm, 2.31mm). It can be stated that gender is an effective variable in determining the tooth relationship with the maxillary sinus floor. These can offer partial explanation to the fact that in daily dental practices, it is more likely that male patients experience maxillary sinus perforation misdeeds.

Discussion
In summary, this study provides detailed information about the anatomic relationships between maxillary molars and the maxillary sinus floor as well as the internal angle and bone width of each molar teeth using CBCT analysis in Chinese patients. In addition to presenting detailed data about each individual teeth parameters, we also take gender into consideration, wondering if gender index makes a difference. A total of 91 patients (67 females and 24 males) with a mean age of 25.1 years (18-41 years) were assessed. To sum up, 471 maxillary molars (127 for third molar teeth, 171 for second molar teeth and 173 for first molar teeth) were evaluated. Having been accessed by strict statistics methods, our study comes to some conclusions. The distributions of the vertical relationships were classified into 5 categories where type III, IV and V relationship in which the maxillary sinus inferior wall is lower than the buccal root or palatal root of maxillary molars was most frequently observed with the first and second molars. The most common type observed in the first and second molars was type V and type I. Concernning the third molar teeth, most teeth also belonged to type V and type I respectively. In termaxillary sinus of Type III, IV and V, the root apex (buccal root or platal root or both) has a contact with or protrude into the inferior wall of maxillary sinus. Given the statistics, it is vital for clinicians to make accurate evaluations before implanting and extration, especially when dealing with teeth of high potential risk, such as the first molars and the second molars.
In first molars and second molars, the internal angle is larger in latter ones. In order to make an ideal preparation design before dental implantation, it is of great value to make an accurate crown angle of the axial walls on the maxillary molars. Sometimes the cleavage may occur due to a wrong insertion angle of dental implants, resulting in devastating outcomes, for both patients and clinicians. Thus, the internal angle cannot be more important to be assessed accurately before making treatment plans. This study presented a full view of the internal angle of each teeth type, making it more convenient for clinicians to plan corresponding dental treatments precisely.
We wondered if there is relation to some degree between the mean distance and the mean internal angle so that Pearson correlation was conducted. It came out that weak correlation can be obtained between these two parameters. Confined to our study, some significant relation can be drawn from these two parameters in first molars and third molars in type III. Futher investigation can be complemented to explore possible association.
In molar area, the mesial-distal width in third molars is largest. However, no distinct differences can be observed within the first molar teeth type and second molar teeth type, respectively. Morever, the bone width in the mesial-distal direction of Type IV was largest on second molars and third molars among all the types. Judging from the data illustrated above, clinicians gain the ability of evaluating the possibility of implanting teeth successfully, avoiding mismatching problemaxillary sinus.
The proximity of molars to the maxillary sinus floor differed according to tooth type and root numbers. In molar area, the third molar is closest to the maxillary sinus floor and the second molar is closer than the first molar, which presents a potential hazard for clinicians who practice tooth extraction, root canal treatment and so on. Take a look at varied root conditions in details, in two-rooted maxillary second molars and third molars, PL was smaller than BL. The distances of each root apex to the maxillary sinus interior wall in three-rooted molars were arranged as follows, PL>DBL>MBL. Overall, prior knowledge of the position of the root apex relative to the adjacent anatomic structures is beneficial for preoperative treatment planning and the prevention of complications. We come to a same Based on previous researches, we compared related parameters by gender difference. The results showed that male harboured a closer distance from root apex of maxillary molars to the inferior wall of maxillary sinus compared to female. An accepted explanation for 13 this condition has not been figured out, possible reason may be the growth pattern discrepancy in male and female and the fact that roots in male teeth are longer than that in female. It offers some sort of practical sense for dental treatments that gender should be taken into consideration when making preoperative plans.
Former studies have also been conducted for tomography evaluation by adopting cone beam computed tomography. Kang SH et al 15 16 . The apices of the mesiobuccal roots of the second molars had the shortest mean vertical distance to the maxillary sinus floor (0.18 mm) and the thickest mean horizontal distance to the buccal cortical plate (4.99 mm) among buccal roots of 3rooted molars (P < .001). In general, the findings were in accordance with our study, hinting that special care must be taken in treatment planning in the maxillary posterior region. Shokri A et al 17 performed the similar experiment, showing that although most of the teeth did not have contact with the sinus floor, the more posterior the maxillary teeth, the more probability for root protruding into the maxillary sinus. Other than that, it also confirmed that protrusion of teeth roots into the maxillary sinus is more common in male than female, taking gender as an unignorable influence factor. Thus, for patients undergoing implantation in maxillary posterior region, CBCT should be performed to determine the height of alveolar crest and anatomy of the maxillary sinus, especially for male patients. Ok E et al 18  using CBCT images, demonstrating that one-fifth of the patients may have a diameter of the SAC >1 mm, which is large enough to cause bleeding and/or paraesthesia. This study emphasized again CBCT's advantage of assisting surgeons to plan grafting and osteotomy procedures so as to avoid harming neurovascular structures 24 . A study led by Schneider AC found sex was the only factor influencing the dimension of the sinus membrane, 16 whereas patient age, season, and the endodontic status of neighboring teeth laid no significant influence on the thickness of the antral mucosa 25 . Before the application of CBCT has been maturely used, scientists took advantages of other means to evaluate the positional relationship between the molars and maxillary sinus. For the majority of the roots projecting on the sinus cavity in panoramic radiographs, no vertical protrusion into the sinus was observed in CT images. Roots that did protrude into the sinus in the CT showed a protrusion length that was much shorter than the projection length appearance using panoramic radiography. In most cases, particular findings of the maxillary sinus in panoramic imaging may be based on a rather examiner-dependent assessment. Due to the superimposition of different structures, low spatial resolution and visual loss of cortical plates or undulating concavities, precise evaluation of a maxillary sinus finding is difficult in 2D panoramic radiography. Therefore, a comparative reliable conclusion can be attained from a good number of studies that CBCT can better visualize maxillary sinus involvement for posterior teeth than other methods such as panoramic radiography.
In details, one study stated that periapical radiography could only spot approximately 40% of apical periodontitis on posterior maxillary teeth and 3% of all apical infections extending to the sinus, seen on CBCT 26 . The benefits of 3D-CT imaging over conventional CT for dental implant treatment are well known. Hence, as the spread of CBCT applications, clinicians should learn to make use of it to make better preoperative   Distance from root apex to the inferior wall of maxillary sinus in the direction of the axis of the tooth(mm).