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Associations between Periapical Health of Maxillary Molars and Mucosal Thickening of Maxillary Sinuses in Cone-beam Computed Tomographic Images: A Retrospective Study
BASIC RESEARCH – TECHNOLOGY
Associations between Periapical Health of Maxillary Molars and Mucosal Thickening of Maxillary Sinuses in Cone-beam Computed Tomographic Images: A Retrospective Study ABSTRACT Introduction: This retrospective study aimed to assess the radiologic characteristics of the possible associations between mucosal thickening of the maxillary sinuses (MSs) and periodontal and anatomic conditions of healthy and diseased maxillary teeth. Methods: The periapical health of the maxillary molars in cone-beam computed tomographic (CBCT) images from 50 patients (mean age 5 40.60614.59 years) was evaluated using the CBCT–periapical index. Anatomic associations between maxillary molars and the inferior wall of the MSs and periodontal bone loss and its relation to MS pathology were assessed. The possible effects of these conditions on mucosal thickening of MSs were analyzed. Kruskal-Wallis, Mann-Whitney U, chi-square, and logistic regression (for relative risk) tests were used for statistical analysis. Results: : CBCT-periapical index 4 was the most frequently encountered apical periodontitis (AP) lesion. The risk for pathologic changes in the MSs was significantly higher in the presence of AP (P , .001). This risk was 62.364 times greater than that in areas of MSs adjacent to healthy teeth of the same patient (95% confidence interval, 7.968–488.14). Thicker MS mucosae were detected when the molar roots with AP were closer to the MSs (P , .004). No statistically significant difference was found between periodontal status and MS pathology. Conclusions: The findings of this study showed that MSs were affected by the endodontic health of adjacent molar teeth. Dental and medical practitioners should take into consideration the possible odontogenic causes while examining pathologic changes in the MS. (J Endod 2020;-:1–7.)
KEY WORDS Apical periodontitis; mucosal thickening; odontogenic maxillary sinusitis; periodontal bone loss; periapical health Odontogenic maxillary sinusitis, which can be caused by a maxillary tooth infection, periodontal bone loss, and/or endodontic treatment affecting the maxillary sinuses (MSs), is frequently encountered in routine otolaryngeal and clinical dental practice1–3. Odontogenic maxillary sinusitis accounts for approximately 10%–41% cases of maxillary sinusitis4; a radiologic examination can reveal its dental origin. It is well-known that 2-dimensional intraoral periapical radiography can provide limited data on the etiology, location, and size of periapical lesions, especially in maxillary molars, because of the superimposition of adjacent structures such as the palatal root or the zygomatic bone5. Cone-beam computed tomographic (CBCT) imaging, which is beneficial for assessing the relationship between the tooth morphology and the adjacent anatomic structures, is a valuable technique for the evaluation of periapical lesions6. Anatomic information regarding the structures forming the MS and their relationships with the posterior teeth are of great importance for a definitive diagnosis of the inflammatory pathologic
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Merve Sakir, DDS,* and Sebnem Ercalik Yalcinkaya, DDS, PhD†
SIGNIFICANCE No previous study has attempted comparison of the MSs adjacent to a molar tooth with a periapical lesion with MSs adjacent to healthy teeth in the same patient. This study aimed to address this gap in the literature.
From the *Department of Dentomaxillofacial Radiology, Faculty of Dentistry, Istanbul Okan University; and † Department of Dentomaxillofacial Radiology, Faculty of Dentistry, Marmara University, Istanbul, Turkey Address requests for reprints to Dr Merve Sakir, Department of Dentomaxillofacial Radiology, Faculty of Dentistry, Istanbul Okan University, Tuzla, Istanbul 34947, Turkey. E-mail address: merve.sakir@hotmail. com or [email protected] 0099-2399/$ - see front matter Copyright © 2019 American Association of Endodontists. https://doi.org/10.1016/ j.joen.2019.12.004
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changes that may occur in both MSs and periapical regions7. Apical periodontitis (AP) in teeth in which the root apices are close to the MS may reveal inflammatory changes in the MS4. In cases in which the periapical bone is thin (where the molar teeth are close to the MS), perforation of the MSs may also occur6. To the best of our knowledge, no previous study has attempted to compare the areas of the MS adjacent to molars with AP and the areas of the MS adjacent to healthy teeth of the same patient. Therefore, the aims of this retrospective study were 1. to evaluate the lesion sizes in molar roots with AP using the CBCT–periapical index (PAI) classification8, 2. to define the association between healthy teeth or molar roots with AP and mucosal thickening (MT), 3. to observe the effect of the periodontal health of adjacent teeth on MT, and 4. to investigate the proximity of molar roots to MSs and to measure the distance between the maxillary molar roots and the floor of the MSs.
MATERIALS AND METHODS The protocol of this study was approved by the Non-invasive Clinical Research Ethics Committee, Marmara University Dentistry Faculty, Istanbul, Turkey (project no: 2016-26). This study was performed retrospectively on the CBCT data obtained from patients who were referred to the Department of Dentomaxillofacial Radiology with different indications. CBCT images of 2000 patients were examined, and the images obtained from 50 patients between the ages of 18 and 65 years old were deemed fit for inclusion in the study. Patients showing the following CBCT findings were not included: 1. 2. 3. 4.
impacted third molars; AP in any other teeth; trauma to the integrity of the MS; and cysts, tumors, or history of any surgery related to the MS.
Because any improvements in root canal–treated molar teeth with hypodense lesions or the differentiating features of pathologic conditions cannot be assessed on radiographs and any such issues might affect the study data negatively, teeth with AP undergoing root canal treatment were also not included in this study. Diagnoses of pulpal sensitivity were searched in the clinical database of the faculty, and only nonvital molar teeth were included. Maxillary molar teeth with AP were identified using the available image data obtained from the Planmeca Promax 3D
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Mid CBCT unit (Planmeca Oy, Helsinki, Finland). The resulting images had a voxel size of 0.4 mm3 and a section thickness of 0.40 mm. Images of the maxilla and mandible, recorded at 90 kVP and 10 mA with a field of view of 16 ! 9 cm, were combined using the Romexis 3.83 software program (Planmeca Oy). One oral radiologist was trained and designated to detect AP and MS pathologies in CBCT images. The presence of APs in the maxillary first and second molars was examined, and the relationship with the MS was assessed using the CBCT images. The relationship between maxillary tooth roots and proximity of the teeth to the floor of the MSs were evaluated in vertical and horizontal planes. The relationship between the maxillary premolar and molar teeth with periodontal bone loss and MSs was determined. In this retrospective analysis of the periapical health of the maxillary first and second molar teeth, CBCT-PAI was used to measure the radiolucent areas according to the method developed by Estrela et al8 in 3 dimensions on the buccolingual, mesiodistal, and diagonal levels. The largest size of the AP lesion based on CBCT-PAI and the growth of the cortical bone were examined together with the extent of destruction in the cortical bone. The relationship between the maxillary tooth roots and the MS inferior wall was evaluated according to the classification proposed by Kwak et al9. The vertical relationships between the inferior wall of the MS and the roots of the maxillary molars were classified into 5 categories: types I to V. The horizontal relationships between the inferior wall of the MS and the roots of the maxillary molars were classified into 3 categories: types 1H to 3H. For the evaluation of MT, the classification proposed by Lu et al10 was used; this classification divided the MT into 5 classes. Periodontal bone loss is classified into 4 categories: 1, normal; 2, slight bone loss of ,25%; 3, medium bone loss of 25%–50%; and 4, severe bone loss of .50%11. The periapical conditions of the maxillary first and second molars, periodontal bone loss, and tooth roots were examined in relation to the MS inferior wall. In addition, the relationship between sinus MT and pathology, such as AP in molar teeth, was evaluated. Descriptive data analysis and statistical analysis were performed using SPSS Statistics software (Version 22.0; IBM Corp, Armonk, NY). Data were analyzed descriptively (frequencies, means, and standard deviations), and the associations among periapical lesions, periodontal bone loss, and the proximity of the teeth to the floor of the MSs were assessed using the chi-square test and the Fisher exact chisquare test. Logistic regression was used to
calculate the odds ratio and to assess the relative risk. The fit of the parameters to normal distribution was evaluated by the Shapiro-Wilk test. The Kruskal-Wallis test was used for quantitative data to compare the parameters that did not show a normal distribution, and the MannWhitney U test was used for determination of the groups that caused the difference. Spearman rho correlation analysis was used to examine the relationships among parameters that did not conform to normal distribution. The confidence interval (CI) was 95% (P , .05).
RESULTS The sex distribution of the patients was equal, and 52% of patients were between the ages of 18 and 39 years old and 48% were over 40 years of age (mean age 5 40.60 6 14.59 years). Of the AP cases, 32% were right first molars, 30% were right second molars, 20% were left first molars, and 18% were left second molars. When the sagittal plane distribution was examined using the classification proposed by Estrela et al8, 8% of the 50 AP cases belonged to CBCT-PAI 1, 16% to CBCT-PAI 2, 22% to CBCT-PAI 3, 40% to CBCT-PAI 4, and 14% to CBCT-PAI 5 (Fig. 1A–D). CBCT-PAI 4 was the most frequently encountered AP category, and bone destruction and/or expansion were observed in 66% of the 50 cases with AP. The frequency of MT in the MSs adjacent to molars with AP was 36%, whereas that in MSs not adjacent to molars with AP was 7%, with the difference being statistically significant (P , .02). The risk of MT in MSs adjacent to the molars with AP was found to be 3.4554 times higher than that in other areas of MSs of the same patient (95% CI, 1.2895– 9.2593; Table 1). The risk for pathologic changes in MSs adjacent to molars with AP was 98% and that in MSs not adjacent to molars with AP was 44%, with the 2 groups showing a statistically significant difference (P , .001). The risk for pathologic changes in MSs adjacent to molars with AP was found to be 62.364 times greater than the risk in the other areas of MSs of the same patient (95% CI, 7.968–488.14; Table 2, Fig. 2A–C). In assessments based on the CBCTPAI scoring system, the risk for pathologic changes in MSs adjacent to molar teeth in CBCT-PAI 1 to 3 cases were 95%, whereas the corresponding risk for other areas of MSs of the same patient was 39% (P , .002, Table 3). When the relative risk was evaluated, the risk for AP in MSs adjacent to the molar teeth of CBCT-PAI class 1 to 3 cases was 34.2222 times higher than that in other areas of MSs of the same patient (95% CI, 3.8997– 300.3196). The risk for pathologic changes in
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FIGURE 1 – CBCT images showing classification of apical periodontitis with CBCT-PAI. (A ) CBCT-PAI class 3 and mucosal thickening, (B ) CBCT-PAI class 5 and mucosal thickening, (C ) CBCT-PAI class 4 and polypoid lesion, and (D ) CBCT-PAI class 1 and retention cyst.
TABLE 1 - A Comparison of Mucosal Thickening of Maxillary Sinuses Adjacent to Molars with Apical Periodontitis and Healthy Teeth of the Same Patient Apical pathology alterations Presence
Absence
Total
n (%)
n (%)
N (%)
P value
18 (36) 32 (64) 50 (100)
7 (14) 43 (86) 50 (100)
25 (25) 75 (75) 100 (100)
.0137
MS mucosal thickening Presence Absence Total MS, maxillary sinus.
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MSs adjacent to molar teeth in CBCT-PAI 4 to 5 cases was 100%, whereas the corresponding risk in other areas of MSs of the same patient was 49% (P , .006, Table 3). In CBCT-PAI 4 and 5 cases, the risk of pathologic changes in MSs adjacent to the molar teeth was found to be 59.0741 times greater than that in the other areas of MSs of the same patient (95% CI, 3.2716– 1066.6747). In this study, the most common pathologic finding of MSs was MT (36%)
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TABLE 2 - A Comparison of Pathological Changes in Maxillary Sinuses Adjacent to Molars with Apical Periodontitis and Healthy Teeth of the Same Patient Apical pathology alterations Presence MS pathologic changes Presence Absence Total MS, maxillary sinuses.
Absence
Total
n (%)
n (%)
N (%)
P value
49 (98) 1 (2) 50 (100)
22 (44) 28 (56) 50 (100)
71 (100) 29 (100) 100 (100)
.0001
followed by polypoid lesions and retention cysts (20% each), partial opacity and total opacity (10% each), and antroliths (2%). Pathologic changes were observed in only 1 MS adjacent to teeth with AP. In the endodontic evaluation, 2% cases were categorized per CBCT-PAI as class 1, 10% as class 2, 14% as class 3, 34% as class 4, and 40% as class 5. In the periodontal evaluation, 22% cases were categorized as class 1, 26% as class 2, 20% as class 3, and 32% as class 411. The pathologic changes
FIGURE 2 – Unilateral imaging of sinus alterations (arrows ). The comparison of MSs adjacent to molars with AP and the areas of MSs adjacent to healthy teeth of the same patient. (A ) Mucosal thickening and (B and C ) polypoid lesion (according to Cho et al12).
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TABLE 3 - Comparisons between the Risk of Pathologic Changes in the Maxillary Sinuses (MSs) Adjacent to Conebeam Computed Tomographic (CBCT)–Periapical Index (PAI) 1 to 3 and 4 to 5 and That in the MSs Adjacent to Healthy Teeth
MS pathologic changes Apical pathology alterations (CBCT-PAI 1–3) Presence Absence Total Apical pathology alterations (CBCT-PAI 4–5) Presence Absence Total
Presence
Absence
Total
n (%)
n (%)
N (%)
P value
22 (95) 1 (5) 23 (100)
9 (39) 14 (61) 23 (100)
31 (54) 15 (46) 46 (100)
.0014
27 (100) 0 (0) 27 (100)
13 (49) 14 (51) 27 (100)
40 (74) 14 (26) 54 (100)
.0057
(according to Cho et al12) in MSs adjacent to teeth with periapical lesions were noted in 56% of cases; 2% showed the presence of an antrolith, 2% showed the presence of exostosis, 24% showed MT, 14% showed polyps, 8% showed retention cysts, and 4% showed total opacification. Polyps and partial or total opacification were observed in 80% of cases followed by destruction and expansion. There was a statistically significant difference between the frequency of particular pathologies in different age groups (P , .04). Retention cysts (36%) and partial opacification (21.7%) were observed more frequently in patients older than 40 years of age. MS pathologies did not reveal any significant differences in sex, age, or periapical health. The proximity of MSs to the molar teeth (first and second) noted in the mesiobuccal roots was 3.1 6 4.91mm; in the distobuccal roots, it was 3.4 6 5 mm; and in the palatal roots, it was 4.54 6 4.86 mm. The shortest distance observed for a single-rooted second molar was 1.71 6 2.81 mm. The most frequent vertical and horizontal relationships were types II and 2H, respectively. When the periodontal condition was evaluated, no statistically significant difference between the pathologic changes in MS and MT classification was detected. There was also no significant relationship between periodontal bone loss and MS pathologies. On the basis of Sheikhi et al.’s classification11, class 1 to 2 and class 3 to 4 were examined in 2 groups, and it was found that there was no statistically significant difference in MS pathologic changes and MT classification distributions.
DISCUSSION The thickness of the alveolar cortical plate and the roots of maxillary molars affect the spread of odontogenic infection, which, in turn, is the
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basis of treatment planning13. Previous studies have shown that dental pathologies may be associated with MT of MSs10,14–16. This study attempted to determine the potential pathologic risk for unilateral maxillary sinusitis adjacent to molars with AP by correlating endodontic, periodontal, and MS anatomic/ pathologic status. Although there is no consensus in the literature regarding the definition of odontogenic maxillary sinusitis, diagnosis is strongly based on clinical and radiologic symptoms. The management of sinusitis and the dental origin of the condition is essential in these cases17. A recent review that analyzed the etiology of odontogenic maxillary sinusitis among 674 patients verified that an iatrogenic etiology accounted for 65.7% of the cases, AP accounted for 25.1% of the cases, and marginal periodontitis accounted for 8.3% cases18. Various radiologic methods have been used to determine periapical health. The CBCT-PAI method developed by Estrela et al8 is a recent scoring index for the diagnosis of periapical lesions, and this method has been used in many studies and is reported to be highly effective19,20. Several studies have reported a significant relationship between periapical pathologic changes and MT of MSs10,14,16. This study found a significant correlation between AP and the risk for pathologic changes in MSs. The risk for pathologic changes in MSs was significantly higher in the presence of AP. Thicker mucosae were detected when molar roots with AP were closer to the MS. This issue requires a closer look regarding the aspect of causative risk factors of MS pathologies from the otolaryngeal and dental point of view. Lu et al10 indicated that MT increased with the CBCT-PAI score, and AP was positively correlated with MT. This study also showed a significant relationship between AP and MT. The CBCT-PAI score was significantly
higher in partial and total opacity cases. As the CBCT-PAI score increased, MT increased. Interestingly, the risk for pathologic changes in MSs adjacent to CBCT-PAI 4 to 5 molars was 34.22 times greater than that in MSs adjacent to CBCT-PAI 1 to 3 molars. In this research, the risk of MT in MSs adjacent to molars with AP was 3.4554 times higher than that in the other areas of MS of the same patient. In their review article, Eggmann et al21 reported that 51% of studies showed an association between AP and maxillary sinusitis, and they suggested the increased risk of developing maxillary sinusitis in the presence of AP. In our study, the pathologic changes and the MT of MSs agreed with the findings reported by Eggmann et al, and our results verified the probability of maxillary sinusitis as being 62.364 times more in the case of AP. The frequency of pathologic changes observed in the MSs in this study was consistent with that in previous reports22,23. Many studies have compared the frequency of MT in MSs in males and females. MT was reported as more common in males11,14, whereas the pathologic changes in MSs seem to occur more often in females24. In this study, no significant difference was observed between males and females. Previous CBCT studies by Phothikhun et al25 and Sheikhi et al11 observed a significant relationship between MT and periodontal bone loss. Ren et al26 reported MT in 48.9% of patients; they showed a significant relationship between vertical bone loss and MT and highlighted the need for the cooperation between periodontists and otolaryngologists in the treatment of maxillary sinusitis. In the literature review conducted by Eggmann et al21, 46% of studies found an association between periodontal health and maxillary sinusitis, whereas 44% found no relation and 10% found unclear relation. In our study, the mean MT was found to be higher in cases of class 3 and 4 bone loss. However, no significant relationship was found between periodontal bone loss and MT. Similarly, Phothikhun et al25 reported that the risk of MT was directly proportional to the severity of periodontal bone loss; however, they did not show any relationship between moderate or minimal bone loss and MT. In contrast, some researchers showed no relationship between periodontal health status and maxillary sinus mucosal thickening27–29. The determination of the proximity of MSs to the molar teeth is of great importance in preoperative planning and the evaluation of MS infections. Many studies have examined the location of maxillary premolars30 and molars relative to MSs. Kwak et al9 investigated the anatomic relationship of maxillary molars with
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the MS. They determined the horizontal relationship of maxillary molars with MSs. Other studies have found the horizontal type 2H relationship to be the most frequent7,9. In our study, the most common vertical relationship was found to be type I (54%), and the most common horizontal relationship was type 2H (92%); these findings were consistent with the results of previous studies. The closest neighborhood was reported to be the buccal root of second molars9,31,32. Similarly, our study observed the closest relationship to MS in the mesiobuccal root of second molar teeth. n and Welander33 reported that Nenze focal MT adjacent to the molars with AP decreased after successful root canal treatment. Nurbakhsh et al34 reported 30% complete improvement and 30% partial improvement in a study comparing 30 patients with AP before and after endodontic treatment. One limitation of the study was the retrospective design. The clinical follow-up data of the patients were not available. In our
study, only 1 patient had completed endodontic treatment, and MT disappeared after successful root canal treatment. This study highlighted the significant correlation between AP and MT. The rather high correlation between MS pathology and AP in this study can be explained by the inclusion criteria. The majority of the previous reports showed some association determined by nonspecific criteria not excluding certain cases. Root canal–treated and impacted teeth were excluded from our study; therefore, the sample size was less compared with that in these studies. All of these aspects restricted the size of the study group, and the research population was reduced to 50 out of 2000 patients.
CONCLUSION Based on these findings, MSs were significantly affected by the endodontic health of adjacent molars. Moreover, an increase in the size of AP was found to be
significantly correlated with an increased risk for developing MS inflammation. To evaluate the MS infections, a detailed dental examination for the presence of dental infections is essential. Because the study solely focused on the radiologic examination findings, the pre- and posttreatment clinical outcomes regarding the health of anatomic structures could not be evaluated. These results clearly indicate the need for future clinical studies to evaluate the relationship between endodontic health and MS infections by assessing the otolaryngeal and dental findings.
ACKNOWLEDGMENTS The authors thank Dr Nural Bekiroglu (Department of Biostatistics, Faculty of Medicine, Marmara University) for providing statistical guidance in this study. The authors deny any conflicts of interest related to this study.
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Associations between Periapical Health of Maxillary Molars and Mucosal Thickening of Maxillary Sinuses in Cone-beam Computed Tomographic Images: A Retrospective Study ABSTRACT Introduction: This retrospective study aimed to assess the radiologic characteristics of the possible associations between mucosal thickening of the maxillary sinuses (MSs) and periodontal and anatomic conditions of healthy and diseased maxillary teeth. Methods: The periapical health of the maxillary molars in cone-beam computed tomographic (CBCT) images from 50 patients (mean age 5 40.60614.59 years) was evaluated using the CBCT–periapical index. Anatomic associations between maxillary molars and the inferior wall of the MSs and periodontal bone loss and its relation to MS pathology were assessed. The possible effects of these conditions on mucosal thickening of MSs were analyzed. Kruskal-Wallis, Mann-Whitney U, chi-square, and logistic regression (for relative risk) tests were used for statistical analysis. Results: : CBCT-periapical index 4 was the most frequently encountered apical periodontitis (AP) lesion. The risk for pathologic changes in the MSs was significantly higher in the presence of AP (P , .001). This risk was 62.364 times greater than that in areas of MSs adjacent to healthy teeth of the same patient (95% confidence interval, 7.968–488.14). Thicker MS mucosae were detected when the molar roots with AP were closer to the MSs (P , .004). No statistically significant difference was found between periodontal status and MS pathology. Conclusions: The findings of this study showed that MSs were affected by the endodontic health of adjacent molar teeth. Dental and medical practitioners should take into consideration the possible odontogenic causes while examining pathologic changes in the MS. (J Endod 2020;-:1–7.)
KEY WORDS Apical periodontitis; mucosal thickening; odontogenic maxillary sinusitis; periodontal bone loss; periapical health Odontogenic maxillary sinusitis, which can be caused by a maxillary tooth infection, periodontal bone loss, and/or endodontic treatment affecting the maxillary sinuses (MSs), is frequently encountered in routine otolaryngeal and clinical dental practice1–3. Odontogenic maxillary sinusitis accounts for approximately 10%–41% cases of maxillary sinusitis4; a radiologic examination can reveal its dental origin. It is well-known that 2-dimensional intraoral periapical radiography can provide limited data on the etiology, location, and size of periapical lesions, especially in maxillary molars, because of the superimposition of adjacent structures such as the palatal root or the zygomatic bone5. Cone-beam computed tomographic (CBCT) imaging, which is beneficial for assessing the relationship between the tooth morphology and the adjacent anatomic structures, is a valuable technique for the evaluation of periapical lesions6. Anatomic information regarding the structures forming the MS and their relationships with the posterior teeth are of great importance for a definitive diagnosis of the inflammatory pathologic
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Merve Sakir, DDS,* and Sebnem Ercalik Yalcinkaya, DDS, PhD†
SIGNIFICANCE No previous study has attempted comparison of the MSs adjacent to a molar tooth with a periapical lesion with MSs adjacent to healthy teeth in the same patient. This study aimed to address this gap in the literature.
From the *Department of Dentomaxillofacial Radiology, Faculty of Dentistry, Istanbul Okan University; and † Department of Dentomaxillofacial Radiology, Faculty of Dentistry, Marmara University, Istanbul, Turkey Address requests for reprints to Dr Merve Sakir, Department of Dentomaxillofacial Radiology, Faculty of Dentistry, Istanbul Okan University, Tuzla, Istanbul 34947, Turkey. E-mail address: merve.sakir@hotmail. com or [email protected] 0099-2399/$ - see front matter Copyright © 2019 American Association of Endodontists. https://doi.org/10.1016/ j.joen.2019.12.004
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changes that may occur in both MSs and periapical regions7. Apical periodontitis (AP) in teeth in which the root apices are close to the MS may reveal inflammatory changes in the MS4. In cases in which the periapical bone is thin (where the molar teeth are close to the MS), perforation of the MSs may also occur6. To the best of our knowledge, no previous study has attempted to compare the areas of the MS adjacent to molars with AP and the areas of the MS adjacent to healthy teeth of the same patient. Therefore, the aims of this retrospective study were 1. to evaluate the lesion sizes in molar roots with AP using the CBCT–periapical index (PAI) classification8, 2. to define the association between healthy teeth or molar roots with AP and mucosal thickening (MT), 3. to observe the effect of the periodontal health of adjacent teeth on MT, and 4. to investigate the proximity of molar roots to MSs and to measure the distance between the maxillary molar roots and the floor of the MSs.
MATERIALS AND METHODS The protocol of this study was approved by the Non-invasive Clinical Research Ethics Committee, Marmara University Dentistry Faculty, Istanbul, Turkey (project no: 2016-26). This study was performed retrospectively on the CBCT data obtained from patients who were referred to the Department of Dentomaxillofacial Radiology with different indications. CBCT images of 2000 patients were examined, and the images obtained from 50 patients between the ages of 18 and 65 years old were deemed fit for inclusion in the study. Patients showing the following CBCT findings were not included: 1. 2. 3. 4.
impacted third molars; AP in any other teeth; trauma to the integrity of the MS; and cysts, tumors, or history of any surgery related to the MS.
Because any improvements in root canal–treated molar teeth with hypodense lesions or the differentiating features of pathologic conditions cannot be assessed on radiographs and any such issues might affect the study data negatively, teeth with AP undergoing root canal treatment were also not included in this study. Diagnoses of pulpal sensitivity were searched in the clinical database of the faculty, and only nonvital molar teeth were included. Maxillary molar teeth with AP were identified using the available image data obtained from the Planmeca Promax 3D
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Mid CBCT unit (Planmeca Oy, Helsinki, Finland). The resulting images had a voxel size of 0.4 mm3 and a section thickness of 0.40 mm. Images of the maxilla and mandible, recorded at 90 kVP and 10 mA with a field of view of 16 ! 9 cm, were combined using the Romexis 3.83 software program (Planmeca Oy). One oral radiologist was trained and designated to detect AP and MS pathologies in CBCT images. The presence of APs in the maxillary first and second molars was examined, and the relationship with the MS was assessed using the CBCT images. The relationship between maxillary tooth roots and proximity of the teeth to the floor of the MSs were evaluated in vertical and horizontal planes. The relationship between the maxillary premolar and molar teeth with periodontal bone loss and MSs was determined. In this retrospective analysis of the periapical health of the maxillary first and second molar teeth, CBCT-PAI was used to measure the radiolucent areas according to the method developed by Estrela et al8 in 3 dimensions on the buccolingual, mesiodistal, and diagonal levels. The largest size of the AP lesion based on CBCT-PAI and the growth of the cortical bone were examined together with the extent of destruction in the cortical bone. The relationship between the maxillary tooth roots and the MS inferior wall was evaluated according to the classification proposed by Kwak et al9. The vertical relationships between the inferior wall of the MS and the roots of the maxillary molars were classified into 5 categories: types I to V. The horizontal relationships between the inferior wall of the MS and the roots of the maxillary molars were classified into 3 categories: types 1H to 3H. For the evaluation of MT, the classification proposed by Lu et al10 was used; this classification divided the MT into 5 classes. Periodontal bone loss is classified into 4 categories: 1, normal; 2, slight bone loss of ,25%; 3, medium bone loss of 25%–50%; and 4, severe bone loss of .50%11. The periapical conditions of the maxillary first and second molars, periodontal bone loss, and tooth roots were examined in relation to the MS inferior wall. In addition, the relationship between sinus MT and pathology, such as AP in molar teeth, was evaluated. Descriptive data analysis and statistical analysis were performed using SPSS Statistics software (Version 22.0; IBM Corp, Armonk, NY). Data were analyzed descriptively (frequencies, means, and standard deviations), and the associations among periapical lesions, periodontal bone loss, and the proximity of the teeth to the floor of the MSs were assessed using the chi-square test and the Fisher exact chisquare test. Logistic regression was used to
calculate the odds ratio and to assess the relative risk. The fit of the parameters to normal distribution was evaluated by the Shapiro-Wilk test. The Kruskal-Wallis test was used for quantitative data to compare the parameters that did not show a normal distribution, and the MannWhitney U test was used for determination of the groups that caused the difference. Spearman rho correlation analysis was used to examine the relationships among parameters that did not conform to normal distribution. The confidence interval (CI) was 95% (P , .05).
RESULTS The sex distribution of the patients was equal, and 52% of patients were between the ages of 18 and 39 years old and 48% were over 40 years of age (mean age 5 40.60 6 14.59 years). Of the AP cases, 32% were right first molars, 30% were right second molars, 20% were left first molars, and 18% were left second molars. When the sagittal plane distribution was examined using the classification proposed by Estrela et al8, 8% of the 50 AP cases belonged to CBCT-PAI 1, 16% to CBCT-PAI 2, 22% to CBCT-PAI 3, 40% to CBCT-PAI 4, and 14% to CBCT-PAI 5 (Fig. 1A–D). CBCT-PAI 4 was the most frequently encountered AP category, and bone destruction and/or expansion were observed in 66% of the 50 cases with AP. The frequency of MT in the MSs adjacent to molars with AP was 36%, whereas that in MSs not adjacent to molars with AP was 7%, with the difference being statistically significant (P , .02). The risk of MT in MSs adjacent to the molars with AP was found to be 3.4554 times higher than that in other areas of MSs of the same patient (95% CI, 1.2895– 9.2593; Table 1). The risk for pathologic changes in MSs adjacent to molars with AP was 98% and that in MSs not adjacent to molars with AP was 44%, with the 2 groups showing a statistically significant difference (P , .001). The risk for pathologic changes in MSs adjacent to molars with AP was found to be 62.364 times greater than the risk in the other areas of MSs of the same patient (95% CI, 7.968–488.14; Table 2, Fig. 2A–C). In assessments based on the CBCTPAI scoring system, the risk for pathologic changes in MSs adjacent to molar teeth in CBCT-PAI 1 to 3 cases were 95%, whereas the corresponding risk for other areas of MSs of the same patient was 39% (P , .002, Table 3). When the relative risk was evaluated, the risk for AP in MSs adjacent to the molar teeth of CBCT-PAI class 1 to 3 cases was 34.2222 times higher than that in other areas of MSs of the same patient (95% CI, 3.8997– 300.3196). The risk for pathologic changes in
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FIGURE 1 – CBCT images showing classification of apical periodontitis with CBCT-PAI. (A ) CBCT-PAI class 3 and mucosal thickening, (B ) CBCT-PAI class 5 and mucosal thickening, (C ) CBCT-PAI class 4 and polypoid lesion, and (D ) CBCT-PAI class 1 and retention cyst.
TABLE 1 - A Comparison of Mucosal Thickening of Maxillary Sinuses Adjacent to Molars with Apical Periodontitis and Healthy Teeth of the Same Patient Apical pathology alterations Presence
Absence
Total
n (%)
n (%)
N (%)
P value
18 (36) 32 (64) 50 (100)
7 (14) 43 (86) 50 (100)
25 (25) 75 (75) 100 (100)
.0137
MS mucosal thickening Presence Absence Total MS, maxillary sinus.
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MSs adjacent to molar teeth in CBCT-PAI 4 to 5 cases was 100%, whereas the corresponding risk in other areas of MSs of the same patient was 49% (P , .006, Table 3). In CBCT-PAI 4 and 5 cases, the risk of pathologic changes in MSs adjacent to the molar teeth was found to be 59.0741 times greater than that in the other areas of MSs of the same patient (95% CI, 3.2716– 1066.6747). In this study, the most common pathologic finding of MSs was MT (36%)
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TABLE 2 - A Comparison of Pathological Changes in Maxillary Sinuses Adjacent to Molars with Apical Periodontitis and Healthy Teeth of the Same Patient Apical pathology alterations Presence MS pathologic changes Presence Absence Total MS, maxillary sinuses.
Absence
Total
n (%)
n (%)
N (%)
P value
49 (98) 1 (2) 50 (100)
22 (44) 28 (56) 50 (100)
71 (100) 29 (100) 100 (100)
.0001
followed by polypoid lesions and retention cysts (20% each), partial opacity and total opacity (10% each), and antroliths (2%). Pathologic changes were observed in only 1 MS adjacent to teeth with AP. In the endodontic evaluation, 2% cases were categorized per CBCT-PAI as class 1, 10% as class 2, 14% as class 3, 34% as class 4, and 40% as class 5. In the periodontal evaluation, 22% cases were categorized as class 1, 26% as class 2, 20% as class 3, and 32% as class 411. The pathologic changes
FIGURE 2 – Unilateral imaging of sinus alterations (arrows ). The comparison of MSs adjacent to molars with AP and the areas of MSs adjacent to healthy teeth of the same patient. (A ) Mucosal thickening and (B and C ) polypoid lesion (according to Cho et al12).
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TABLE 3 - Comparisons between the Risk of Pathologic Changes in the Maxillary Sinuses (MSs) Adjacent to Conebeam Computed Tomographic (CBCT)–Periapical Index (PAI) 1 to 3 and 4 to 5 and That in the MSs Adjacent to Healthy Teeth
MS pathologic changes Apical pathology alterations (CBCT-PAI 1–3) Presence Absence Total Apical pathology alterations (CBCT-PAI 4–5) Presence Absence Total
Presence
Absence
Total
n (%)
n (%)
N (%)
P value
22 (95) 1 (5) 23 (100)
9 (39) 14 (61) 23 (100)
31 (54) 15 (46) 46 (100)
.0014
27 (100) 0 (0) 27 (100)
13 (49) 14 (51) 27 (100)
40 (74) 14 (26) 54 (100)
.0057
(according to Cho et al12) in MSs adjacent to teeth with periapical lesions were noted in 56% of cases; 2% showed the presence of an antrolith, 2% showed the presence of exostosis, 24% showed MT, 14% showed polyps, 8% showed retention cysts, and 4% showed total opacification. Polyps and partial or total opacification were observed in 80% of cases followed by destruction and expansion. There was a statistically significant difference between the frequency of particular pathologies in different age groups (P , .04). Retention cysts (36%) and partial opacification (21.7%) were observed more frequently in patients older than 40 years of age. MS pathologies did not reveal any significant differences in sex, age, or periapical health. The proximity of MSs to the molar teeth (first and second) noted in the mesiobuccal roots was 3.1 6 4.91mm; in the distobuccal roots, it was 3.4 6 5 mm; and in the palatal roots, it was 4.54 6 4.86 mm. The shortest distance observed for a single-rooted second molar was 1.71 6 2.81 mm. The most frequent vertical and horizontal relationships were types II and 2H, respectively. When the periodontal condition was evaluated, no statistically significant difference between the pathologic changes in MS and MT classification was detected. There was also no significant relationship between periodontal bone loss and MS pathologies. On the basis of Sheikhi et al.’s classification11, class 1 to 2 and class 3 to 4 were examined in 2 groups, and it was found that there was no statistically significant difference in MS pathologic changes and MT classification distributions.
DISCUSSION The thickness of the alveolar cortical plate and the roots of maxillary molars affect the spread of odontogenic infection, which, in turn, is the
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basis of treatment planning13. Previous studies have shown that dental pathologies may be associated with MT of MSs10,14–16. This study attempted to determine the potential pathologic risk for unilateral maxillary sinusitis adjacent to molars with AP by correlating endodontic, periodontal, and MS anatomic/ pathologic status. Although there is no consensus in the literature regarding the definition of odontogenic maxillary sinusitis, diagnosis is strongly based on clinical and radiologic symptoms. The management of sinusitis and the dental origin of the condition is essential in these cases17. A recent review that analyzed the etiology of odontogenic maxillary sinusitis among 674 patients verified that an iatrogenic etiology accounted for 65.7% of the cases, AP accounted for 25.1% of the cases, and marginal periodontitis accounted for 8.3% cases18. Various radiologic methods have been used to determine periapical health. The CBCT-PAI method developed by Estrela et al8 is a recent scoring index for the diagnosis of periapical lesions, and this method has been used in many studies and is reported to be highly effective19,20. Several studies have reported a significant relationship between periapical pathologic changes and MT of MSs10,14,16. This study found a significant correlation between AP and the risk for pathologic changes in MSs. The risk for pathologic changes in MSs was significantly higher in the presence of AP. Thicker mucosae were detected when molar roots with AP were closer to the MS. This issue requires a closer look regarding the aspect of causative risk factors of MS pathologies from the otolaryngeal and dental point of view. Lu et al10 indicated that MT increased with the CBCT-PAI score, and AP was positively correlated with MT. This study also showed a significant relationship between AP and MT. The CBCT-PAI score was significantly
higher in partial and total opacity cases. As the CBCT-PAI score increased, MT increased. Interestingly, the risk for pathologic changes in MSs adjacent to CBCT-PAI 4 to 5 molars was 34.22 times greater than that in MSs adjacent to CBCT-PAI 1 to 3 molars. In this research, the risk of MT in MSs adjacent to molars with AP was 3.4554 times higher than that in the other areas of MS of the same patient. In their review article, Eggmann et al21 reported that 51% of studies showed an association between AP and maxillary sinusitis, and they suggested the increased risk of developing maxillary sinusitis in the presence of AP. In our study, the pathologic changes and the MT of MSs agreed with the findings reported by Eggmann et al, and our results verified the probability of maxillary sinusitis as being 62.364 times more in the case of AP. The frequency of pathologic changes observed in the MSs in this study was consistent with that in previous reports22,23. Many studies have compared the frequency of MT in MSs in males and females. MT was reported as more common in males11,14, whereas the pathologic changes in MSs seem to occur more often in females24. In this study, no significant difference was observed between males and females. Previous CBCT studies by Phothikhun et al25 and Sheikhi et al11 observed a significant relationship between MT and periodontal bone loss. Ren et al26 reported MT in 48.9% of patients; they showed a significant relationship between vertical bone loss and MT and highlighted the need for the cooperation between periodontists and otolaryngologists in the treatment of maxillary sinusitis. In the literature review conducted by Eggmann et al21, 46% of studies found an association between periodontal health and maxillary sinusitis, whereas 44% found no relation and 10% found unclear relation. In our study, the mean MT was found to be higher in cases of class 3 and 4 bone loss. However, no significant relationship was found between periodontal bone loss and MT. Similarly, Phothikhun et al25 reported that the risk of MT was directly proportional to the severity of periodontal bone loss; however, they did not show any relationship between moderate or minimal bone loss and MT. In contrast, some researchers showed no relationship between periodontal health status and maxillary sinus mucosal thickening27–29. The determination of the proximity of MSs to the molar teeth is of great importance in preoperative planning and the evaluation of MS infections. Many studies have examined the location of maxillary premolars30 and molars relative to MSs. Kwak et al9 investigated the anatomic relationship of maxillary molars with
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the MS. They determined the horizontal relationship of maxillary molars with MSs. Other studies have found the horizontal type 2H relationship to be the most frequent7,9. In our study, the most common vertical relationship was found to be type I (54%), and the most common horizontal relationship was type 2H (92%); these findings were consistent with the results of previous studies. The closest neighborhood was reported to be the buccal root of second molars9,31,32. Similarly, our study observed the closest relationship to MS in the mesiobuccal root of second molar teeth. n and Welander33 reported that Nenze focal MT adjacent to the molars with AP decreased after successful root canal treatment. Nurbakhsh et al34 reported 30% complete improvement and 30% partial improvement in a study comparing 30 patients with AP before and after endodontic treatment. One limitation of the study was the retrospective design. The clinical follow-up data of the patients were not available. In our
study, only 1 patient had completed endodontic treatment, and MT disappeared after successful root canal treatment. This study highlighted the significant correlation between AP and MT. The rather high correlation between MS pathology and AP in this study can be explained by the inclusion criteria. The majority of the previous reports showed some association determined by nonspecific criteria not excluding certain cases. Root canal–treated and impacted teeth were excluded from our study; therefore, the sample size was less compared with that in these studies. All of these aspects restricted the size of the study group, and the research population was reduced to 50 out of 2000 patients.
CONCLUSION Based on these findings, MSs were significantly affected by the endodontic health of adjacent molars. Moreover, an increase in the size of AP was found to be
significantly correlated with an increased risk for developing MS inflammation. To evaluate the MS infections, a detailed dental examination for the presence of dental infections is essential. Because the study solely focused on the radiologic examination findings, the pre- and posttreatment clinical outcomes regarding the health of anatomic structures could not be evaluated. These results clearly indicate the need for future clinical studies to evaluate the relationship between endodontic health and MS infections by assessing the otolaryngeal and dental findings.
ACKNOWLEDGMENTS The authors thank Dr Nural Bekiroglu (Department of Biostatistics, Faculty of Medicine, Marmara University) for providing statistical guidance in this study. The authors deny any conflicts of interest related to this study.
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