Tooth Extraction as a Risk Factor for Maxillary Sinus Pneumatization: A Case-control Study

Purpose Maxillary sinus pneumatization following teeth extraction may require various treatment plans such as sinus lifting and alveolar grafting procedures to obtain sufficient alveolar bone height for implant surgery. The aim of this study was to identify sinus pneumatization and to help in determining the proper time for preprosthetic surgery following extraction of maxillary sinus related teeth. Methods We evaluated 75 teeth extraction related to maxillary sinus floor. The panoramic radiographs were evaluated before and after extraction of the posterior maxillary teeth. The radiographs were divided into 5 groups according to duration after extraction. Two reference points (the first point corresponds to the nasal spine while the second point corresponds to the most inferior point of the floor of the maxillary sinus wall) were determined on digital panoramic radiographs before and after teeth extraction and the distance between both aforementioned points was measured. Results The amount of pneumatization was found to be increased with time. The pneumatization within the first 6 months was limited. However, a sudden increase of pneumatization after 6th month, especially the highest between 18th and 24th months, was observed. The mean pneumatization amount was found to be highest in the 1st molar group. Conclusion According to the results of the present study, surgeons should not be waited any more than 6 months after tooth extraction for preprosthetic surgery in the posterior maxillary region as long as physiological healing of extraction socket is allowed.


Background
Currently, dental implant-supported prosthetic treatment is the most common procedure for edentulism. However, due to pneumatization and severe alveolar bone ridge height problems related to the sinus floor, implant placement might not be feasible. Although there are various treatments, such as sinus elevation or bone grafting procedures, to increase the alveolar bone height for implant surgery, it is important to understand the correlation between the process of sinus pneumatization and related factors [1].
The maxillary sinus has the largest volume of all paranasal sinuses. It continues to pneumatize until the permanent teeth erupt from alveolar bone after birth.
Pneumatization is a physiological process that leads to an increase in the volume of the paranasal sinuses during growth [2,3]. It is known that the maxillary sinus floor reaches the same level as the nasal floor at age 12-13. Maxillary sinus pneumatization ends after eruption of the third molars. The pneumatization period appears in the osteoid layer on histology, with osteoclastic resorption of the cortical walls of the sinus [4].
The biological process of sinus formation is not clearly understood. Previous studies have reported that heredity [5], nasal mucous membrane pressure [3], craniofacial settlement, bone density, growth hormones [2], sinus air pressure [1] and sinus surgery [6] may play roles in this process.
Although clinicians and researchers presume that sinus pneumatization in relation to maxillary tooth extraction is common knowledge, there have only been a few radiographic studies published in the literature investigating changes in the maxillary sinus floor level in relation to the other anatomical structures before and after the removal of a tooth [2,4,[7][8][9]. This phenomenon has been described in various ways, such as disuse atrophy and a decrease in functional forces transferred to the bone after tooth loss causing a shift in the remodeling process toward bone resorption [2,4] and expansion of the sinus volume toward the edentulous alveolar ridge. The rate and degree of pneumatization after tooth removal may be affected by roots extending into the sinus having a thin cortical bone layer [2,4]. This thin bone may break and dislocate during extraction, potentially causing the sinus to expand toward the socket. Additionally, larger amounts of pneumatization can occur after molar extraction [7]. These larger defects can be observed in the alveolar bone after molar extraction, and the longer healing period required allows the sinus to pneumatize.
Cone-beam computed tomography (CBCT) is a current diagnostic tool that provides three-dimensional (3D) images and detailed sections for evaluating the relationship between the margin of the alveolar bone and the maxillary sinus floor status [1].
However, there is a lack of studies using CBCT to analyze sinus floor pneumatization in the edentulous posterior maxilla. Additionally, to obtain correct knowledge by conventional panoramic evaluation is still crucial for private clinics at the first stage of many health systems in countries that do not use CBCT.
The purpose of this study was to evaluate the maxillary sinus pneumatization in relation to tooth extraction according to time, tooth type and other factors using reference lines and landmarks on a panoramic view. Additionally, this study aimed to identify an ideal time for bone grafting or implant treatment procedures and to determine the possible need for sinus elevation procedures.

Methods
The participants were patients who underwent at least one premolar or molar tooth extraction associated with the sinus membrane in Erciyes University Faculty of Dentistry Department of Oral and Maxillofacial Surgery. All patients provided written informed consent. Panoramic radiographs taken before and after extraction were assessed (CLINIVIEW dental imaging software, CLINIVIEW, Finland). A total of 128 panoramic films from 42 patients (19 females, 23 males) were examined. The ages of the participants were between 46 and 70 years old. A total of 75 extractions (5 premolars, 27 first molars, 33 second molars, 10 third molar) were performed.
Patients were divided into 5 groups according to the follow-up time between the first and second radiological examinations. The follow-up periods and the number of patients in each group are shown in Table 1.
The follow-up period ranged from 1 day to 2 years. Two reference points were selected on the panoramic films, and the amount of pneumatization was calculated by measuring the distance between these two reference points using the CLINIVIEW software program (CLINIVIEW, Finland). The first reference point was a line parallel to the Frankfort horizontal plane passing through the most superior point of the anterior nasal spine. The second reference point was a line parallel to the Frankfort horizontal plane passing through the most inferior point of the sinus (Figure 1).
The distance between these two points was regarded as the amount of sinus pneumatization ( Figure 2). For determination of the amount of magnification from the panoramic films taken before and after extraction, the distance between the lines parallel to the Frankfort horizontal plane passing through the top of the crown and the apex of the root of the canine or premolar was calculated. In edentulous patients, the distance between the top and the bottom of the metal ball in the panoramic radiographs was measured, and the amount of magnification was calculated using a simple ratio. This ratio was applied to the postextraction radiographs to calculate the amount of actual pneumatization (Figure 3). The average amount of pneumatization was calculated by dividing the obtained total amount of pneumatization from each group by the number of subjects.

Statistical analysis
Data analysis was performed with SigmaPlot 12.0. The Shapiro-Wilk test was used to determine the normality of the data distribution. The Mann-Whitney U test was performed for the comparison of sinus pneumatization between preextraction and postextraction according to sex. The one-way Kruskal-Wallis test was used for the comparison of tooth types, time periods and cases of multiple tooth extractions ( Figures 4, 5, 6). In all analyses, a significance level of p<0.05 was used.

Results
The amount of pneumatization obtained from the subjects in the 5 different time interval groups was recorded. The average amount of pneumatization, the maximum and minimum amounts of pneumatization and the number of teeth causing pneumatization after extraction are given ( Table 2). The amount of pneumatization increased over time during the follow-up period. In the first 6 months, sinus pneumatization was limited. After 6 months, pneumatization suddenly increased, and between 18-24 months, the amount of pneumatization was at its maximum.
The maximum amount of pneumatization was 6 mm, which was observed after the extraction of a first molar. The average amount of pneumatization according to tooth type is given (Table 3). The amount of pneumatization was greater after the extraction of teeth with an infected root and the extraction of molars, which lifted the sinus membrane by their roots in a curved manner.

Discussion
Dental implant installation in the upper posterior region, an accurate diagnosis and a better understanding of bone remodeling in the area may be valuable for optimum treatment planning. Currently, cone-beam computed tomography (CBCT) is a common diagnostic tool that supports three-dimensional (3D) imaging and provides thin, detailed sections to assess the relationship between the maxillary sinus floor and the alveolar bone ridge. Although this method reduces the overlapping of anatomical structures and enables a better assessment, there is still a lack of studies using CBCT to analyze sinus floor pneumatization in the posterior maxilla.
Additionally, obtaining correct knowledge by conventional panoramic evaluation is still crucial for private clinics at the first stage of many health systems in countries that do not use CBCT [1]. The purpose of this study was to determine the amount of sinus pneumatization after the extraction of maxillary teeth in the premolar and molar regions associated with the maxillary sinus via the evaluation of panoramic views.
In spite of common belief, only a few studies have described the phenomenon of pneumatization of the maxillary sinus [2,4,[7][8][9][10]. Previous studies that were conducted by assessing panoramic radiographs or repeated radiographs have demonstrated the potential for differences in scale and/or mismatching, which might arise from comparing two different panoramic radiographs with differences in terms In contrast, our study shows rapid sinus expansion in the first 6 months. Therefore, preprosthetic treatments, such as dental implant surgery, should be performed in the first 6 months after extractions in the molar region. Otherwise, additional procedures, likesuch as sinus elevation and grafting, might be needed.
Extensive sinus expansion occurred in cases of the extraction of more than one tooth in the same area. At sites of multiple extractions, bone resistance is reduced, and severe sinus pneumatization can occur [2]. After extraction, adjacent teeth transport the occlusal forces to the extraction socket. This force transmission to the alveolar bone has been considered to reduce the amount of sinus expansion [2].
This may be the reason why in our study, we found greater sinus expansion after the extraction of first upper molars than 2nd upper molars. There are a few limitations to the present study. One of these is the use of panoramic radiographs to measure changes in alveolar ridge and maxillary sinus dimensions. Although reference points were used to superimpose different radiographs, the use of cone-beam computerized tomography (CBCT) could verify sinus pneumatization changes. Second, pneumatization was associated with various factors except for tooth extraction in the maxillary posterior region. We evaluated only the correlation between tooth extraction and pneumatization with a small sample size. Further studies including CBCT examinations and larger sample sizes should be conducted to evaluate different factors and confirm these findings.

Conclusion
In conclusion, greater sinus pneumatization occurs mostly after the extraction of two or more adjacent teeth, first or third second molars with thinner bone, teeth that elevate the sinus floor and teeth in the sinus mucosa. According to our findings, implant placement is suggested to be performed in the first 6 months after extraction. Therefore, surgeons can avoid additional procedures, such as sinus elevation surgery, which can be complicated and require longer treatment times.
Additionally, the clinician should consider preserving bone height by immediate implantation with simultaneous bone grafting at the time of tooth extraction.
Further studies should investigate the effect of socket grafting with not only different grafting materials but also PRF or tissue engineering procedures involving stem cells and/or immediate implantation for the prevention of pneumatization of the maxillary sinus.

Ethics Approval and Consent to Participate
Permission for the study was granted by the Erciyes University Ethics Committee sectional study. Brazilian oral research. 2018; 32.     Figure 1 The distance between these two points is regarded as the amount of sinus pneumatization.

Figure 2
The distance between these two points is regarded as the amount of sinus pneumatization.

Figure 3
Postextraction radiographs were used to calculate the amount of the pneumatization.

Figure 4
Differences in pneumatization by tooth type.

Figure 5
Changes in pneumatization over time.

Figure 6
Differences in pneumatization by number of extracted teeth.