The relation of maxillary root apices and the maxillary sinus floor among patients with different skeletal patterns in Iraqi samples

Background: Understanding the morphological characteristics between the floor of the maxillary sinus and the tips of the maxillary posterior roots is crucial in orthodontics involving diagnosis and treatment planning. The aim of this study was to evaluate the distances from the maxillary posterior root apices to the inferior wall of the maxillary sinus, thickness and density of maxillary sinus floor using cone-beam computed tomography images and the relationships between roots and maxillary sinus according to gonial angle and skeletal pattern. Materials and methods: Three-dimensional images of each root were checked, and the distances were measured along the true vertical axis from the apex of the root to the sinus floor, and the thickness and density of maxillary sinus floor in 60 patients (30 males, 30 female) aged 18 to 25 years. Evaluation of the differences between groups which classified to gonial angle and skeletal pattern which were done according to the comparsion between the mean statistic tests. Results: results showed that the density of floor of maxillary sinus at the first molar roots region in class III were significantly lower than class I and II, also the distance between the floor of maxillary sinus and both distobuccal and palatal roots of first molar were significantly lower in class I than other classes, while the thickness of maxillary sinus floor at the distobuccal root of first molar were significantly higher in class III than other classes. In gonial angle difference, the maxillary sinus floor density and distance to the maxillary posterior roots had no significant difference in all groups, while the thickness of maxillary sinus floor at distobuccal and palatal of second molar roots region were significantly higher in large gonial angle than small and normal angles. Conclusion: subjects with class I skeletal pattern have small distance between the maxillary sinus floor and the maxillary posterior roots due to the pneumatisation of maxillary sinus causing more difficult and time consuming orthodontic treatment.


INTRODUCTION
In adults, the maxillary sinus differs in its projection due to the presence of 'Hillocks' which are elevations in the surface of sinus floor that occur in 50 % of population when the floor projects among adjacent teeth or roots (1) . In these cases, the sinus floor thickness is clearly diminished. When the roots project into the sinus floor many complications occur involving oroantral fistulae or displacement of root into the sinus or cavity that usually happen after extractions of maxillary molars (2) .
The sinus floor is made by the alveolar process of maxilla and locate about 12.5 mm beneath the floor of the nasal cavity. Casually a delicate layer of mucous lining is the only detachment of the roots of teeth from the maxillary sinus (3) .
The occlusion is influenced by vertical relationship of the upper and lower jaws. The effect is more obvious at the gonial angle when there is difference in the shape of the lower jaw.
Whenever the gonial angle is high, the mandible prone to increase vertical dimension of the face, and in severe cases causes an anterior open bite. In contrast, the mandible with a low gonial angle prone to decrease vertical dimension of the face.
During movement of tooth in orthodontic field and placement of implant, some problems may occur caused by maxillary sinus. Intrusion of maxillary posterior teeth into the maxillary sinus may cause tipping and periapical root resorption histologically and even radiographically (4,5). furthermore, the angled placement of microimplants has high risk of destroying the maxillary sinus (6). Therefore, problems like sinus perforation, and the resorption of root during the intrusion of molar can be stopped by the recognition about the distance between the roots of maxillary posterior teeth to the floor of maxillary sinus.
The thickness of the bone layer of the sinus floor is reduced significantly due to the presence of the roots of the posterior maxillary teeth within the maxillary sinus floor(MSF). However, most roots that project into the sinus are normally covered by a delicate cortical layer on histologic sections, and the rates of real perforation are not more than 14% to 28% (7) .
Bone density is defined as the amount of bone tissue in a specific volume of bone (8) . Many studies illustrate the importance of cone beam computerized tomography CBCT scans in the recognition of the topography of the maxillary sinus and its correlation with the tips of the maxillary posterior roots (9)(10)(11) . The advantages of CBCT are low radiation dose and easier technology than the other technologies (12) .
The aim of this study was to assess the relationships between maxillary posterior roots and maxillary sinus floor according to skeletal pattern, and gonial angle by using cone beam computed tomography images which include measuring the distances between maxillary posterior root apices and inferior wall of maxillary sinus, the cortical bone thickness and density of maxillary sinus floor in the region closest to the root apices and in the furcation areas.

MATERIALS AND METHODS
This study composed of CBCT images has been taken in the Specialized Health Centre in Al-Sadr city / 3D radiographic department using Kodak 9500 Cone Beam 3D system machine that made in France (serial number: 420354AFXL057) with Carestream (CS) 3D Imaging software for patients who were attending from December 2017 till May 2018. From the 671 patients that included 436 females and 235 male aged from 15 years to 28 years that was sent for CBCT for the diagnosis of impacted third molars, impacted canine, and for orthodontic purposes, 60 Iraqi samples (30 males: 10 class I, 10 class II, 10 class III; and 30 females: 10 class I, 10 class II, 10 class III) ranged between 18-25 years chosen according to the stratified random sampling probability. An informed consent must be made for the subject to be part of the study of different skeletal pattern (class I, class II, and class III) that have been determined clinically by palpation with two-fingers method (13) . All patients were included except with these exclusion criteria which include: history of previous orthodontic treatment, missing posterior teeth (excluding the third molars), pathologic lesions or abnormalities of the maxillary sinus, radiographic signs of periapical disease, medical history. According to Foster (13) extra-orally, the assessment of the skeletal pattern clinically. On the CBCT images, the distances from the upper posterior teeth root tips to the inferior wall of the floor of maxillary sinus were measured. The 3-dimensional (3D) measurements were done with Carestream (CS) 3D Imaging system software (KODAK dental imaging 9500 3D, France). Positive values were given to the distances that measured when there was no contact between the root and floor of the sinus ( Figure 1), while negative values were given to the distances measured when the side of the root had contact with the sinus floor or the root penetrated into the maxillary sinus (14,15) .

Figure 1: When the root had no contact with
sinus floor, the distance was recorded as a positive value If the root apex is in contact or penetrate the maxillary sinus, the thickness is given value of 0.00 mm (14) . Measuring MSF cortical bone thickness in the region closest to the upper posterior root apices and in the furcation areas ( Figure 2).

Figure 2: The cortical thickness of the inferior wall of the maxillary sinus
The density of the inferior wall of MSF was measured above the maxillary posterior root apices in both sides Above the root tip of second premolar, and above the furcation area for both first and second molars, the density of inferior wall of the sinus was measured by placing the mouse on three locations in MSF, and obtaining the mean of three readings that had been appeared on the lower right corner of screen ( Figure 3).

Figure 3: Measurement of density
The gonial angle can be measured from panoramic view and the location was determined from drawing two lines, a perpendicular line that touches the posterior border of ramus, and a horizontal line touches the mandibular inferior border. In order to impede rotation of the line, two points were determined contact each line. The angle was achieved from the meeting of the horizontal and vertical lines (16,17) (Figure 4). Okşayan et al. (17) confirmed that the values of gonial angle obtained from lateral cephalometry and orthopantomogram had no significant differences between Class I, II, and III malocclusion group. After measurements were done 3 groups obtained: large (≥ 132), normal (119-131), and small (≤ 118) gonial angle groups.

RESULTS
The sample include 60 subjects (30 males, and 30 females) was divided into 3 groups according to gonial angle:14 samples with large (≥ 132), 33 samples with normal (119-131), and 13 samples with small (≤ 118) gonial angle groups. Also the sample divided according to skeletal pattern into 20 samples with Class I, 20 samples with Class II and 20 samples with Class III groups.
Descriptive statistics and Class difference of the distance between floor of maxillary sinus and root apex of maxillary posterior teeth: The longest distance between the sinus floor and root apices seen in class I with no protrusion at the second premolars (mean value, 0.580), and the more protruded roots into the sinus were the palatal roots of the first molars that found in class I (mean value, -4.075). Regarding the sagittal jaw relationship, the study showed a statistical significance at the distobuccal, and palatal roots of the first molars by using ANOVA test, then the difference in distances between class I and III in both roots found by using Tukey's test (Table 1)

Descriptive statistics and Class difference of the cortical bone thickness:
The mean thickness of the sinus floor above root apices according to classes. The greatest thickness of inferior wall seen in class III above the furcation area of the first molar roots (mean value, 1.058), while the lowest thickness found in class I at the mesiobuccal root of the second molar teeth (mean value, 0). The Kruskal Wallis H Test showed statistical significance found at the distobuccal root of the first molar, and by using Mann Whitney test, the difference in thickness found between class I and III as in (Table 2).

Descriptive statistics and Class difference of the cortical bone density:
The mean density of the sinus floor above root apices according to classes. The highest density of the sinus floor found in class I above the second premolar root (mean value, 671.700), while the lowest density found in class III above the second molar root (mean value, 660.050). The ANOVA test showed statistical significant difference in density found at the first molar root, and by using Tukey's HSD test, the difference in density found between class I and III, as well as between class II and III as in (Table 3).

Descriptive statistics and Gonial angle difference of the distance between floor of maxillary sinus and root apex of maxillary posterior teeth:
The longest distance between sinus floor and root apices found in normal gonial angle patients with no protrusion at second premolar roots (mean value, 1.172), while the more protruded roots into the sinus were the mesiobuccal roots of second molar that found in small gonial angle patients (mean value, -3.328). In general, no statistical significace difference in distance among different groups of gonial angle as in (Table 4).

Descriptive statistics and Gonial angle difference of the cortical bone thickness:
The mean thickness (mm) of the sinus floor above root apices according to gonial angle. The greatest thickness of inferior wall seen in large gonial angle at the furcation area of the second molar roots (mean value, 1.085), while the lowest thickness found in normal gonial angle at the mesiobuccal root of the second molar teeth (mean value, 0.065). The Kruskal Wallis H Test showed a significance found at the distobuccal, and palatal root of the second molars. Through using Mann Whitney test, the difference in thickness in the distobuccal root of second molar found between small and large gonial angle, while in the palatal root of second molar, the difference found between normal and large gonial angle as in (Table 5).

Descriptive statistics and Gonial angle difference of the cortical bone density:
The mean density of the sinus floor above root apices according to gonial angle. The highest density of the sinus floor found in normal gonial angle above the second premolar root (mean value, 673.793), while the lowest density found in small gonial angle above the second molar root (mean value, 476.222) show in (Table  6).

DISCUSSION
The CBCT supplies accurate images with no distortion and overlapping of the nearby structures of the bone that surround root apices, so that CBCT has been used in diagnosis and treatment planning widely (15) .

Distance:
This study showed a significant difference regarding the sagittal jaw relationship at the distobuccal, and palatal roots of the first molars.
All roots of patients with a small gonial angle showed a more protrusion into the sinus than normal and large gonial angle. This was not agreed with Ahn and Park (15) , who revealed that all roots of patients with a large gonial angle showed a significantly closer relationship to the sinus floor or more protrusion of the roots into the sinus than the roots of patients in the normal and small gonial angle groups. During the treatment of open-bite cases, intrusion of the maxillary molar teeth is required which is difficult, because of the close distance between the maxillary posterior root tips and the sinus floor (18) . Patients that have small gonial angle need light intrusion force in order to decrease resorption of root. Clinicians must pay attention when determining the amount and direction of the orthodontic forces during treatment (15) .

Thickness:
According to class differences the smallest and greatest thickness of the MSF that had been found over the mesiobuccal root of second molar, and over the furcation of first molar apex, respectively. This study agreed with Estrela et al (14) , in which the smallest thickness had been found over the mesiobuccal root of second molar, but disagreed with Yoshmine (19) in both greatest and smallest thickness. Harrison (20) reported that the minimum thickness of inferior wall of the maxillary sinus found over the second molar root which was consistent with the present study, while in the study of Kwak et al. (21) the cortical thickness over the distobuccal root of the second molar was the thinnest which disagreed with the results of this study obtained from class difference. The differences between these studies were because of the high thickness of MSF in this study found over the furcation area of both first and second molars in addition to other reasons as difference in methodology, number of subjects, and ethnicity.
A statistical significance had been found in second molar roots in gonial angle differences only. It is interesting to observe that the area of greatest distance between the root tips of maxillary posterior teeth and the MSF coincided with the area of the greatest thickness near to the apex (second premolars), and the area of lowest distance steeth and the MSF coincided with the lowest thickness near to the apex (second molars).

Density:
The density of sinus floor was measured by placing the mouse on the MSF over the roots of second premolar, and above the furcation areas of both first and second molar roots, the value of the density appeared on the lower right corner of screen A statistical significance found in density over the furcation of first molar in which subject with class III had the lowest density of all classes. When observing the gonial angle difference, the greatest density of the floor of maxillary sinus was observed above the root apex of second premolar in subject with normal gonial angle with (mean value, 673.793). No statistical significance had been found in density over all the roots. There are no previous studies conducted the measurement of density of the MSF, so that, the results of this study cannot be compared with other studies.

CONCLUSION
The more protruded root into the sinus floor were the mesiobuccal root apices of the second molars and the palatal root apices of first molars, and the farthest from the floor of sinus were second premolar root apices. The greatest thickness of maxillary sinus floor found over the bifurcation area of both first and second molar roots, while the smallest thickness appeared over the mesiobuccal and distobuccal root apices of second molars. The greatest density of maxillary sinus floor found over the second premolar root apices and the smallest appeared over the furcation of second molar root apices. In class difference, the density of maxillary first molar in class III were significantly lower than class I and II, while the distance of both distobuccal and palatal roots of maxillary first molar and the thickness of distobuccal roots of maxillary first molar were significantly higher in class I, and class III, respectively than other classes. In gonial angle difference, the density and distance had no significant difference in all groups, while the thickness of distobuccal and palatal roots of maxillary second molar were significantly higher in large gonial angle than small and normal angles.