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Associations between Maxillary Sinus Mucosal Thickening and Apical Periodontitis Using Cone-Beam Computed Tomography Scanning: A Retrospective Study
Clinical Research
Associations between Maxillary Sinus Mucosal Thickening and Apical Periodontitis Using Cone-Beam Computed Tomography Scanning: A Retrospective Study Yu Lu, DDS,* Zhongjun Liu, DDS,* Lan Zhang, DDS,* Xuedong Zhou, DDS, PhD,* Qinghua Zheng, DDS,* Xingyu Duan, DDS,* Guangning Zheng, DDS,† Hu Wang, MD,† and Dingming Huang, DDS, PhD* Abstract Introduction: This study evaluated the pathologic and spatial associations between apical periodontitis of the maxillary premolars/molars and the maxillary sinus mucosal thickening using cone-beam computed tomography (CBCT) scanning. Methods: CBCT images of 372 patients with 508 exposed maxillary sinuses were inspected retrospectively. Clinical features such as sex and age of the patients and pathologic findings of the maxillary sinus and adjacent teeth were recorded, graded, and analyzed. Results: Maxillary sinus mucosal thickening was found in 180 (48.4%) patients and 235 (46.2%) sinuses. The prevalence of maxillary sinus mucosal thickening increased dramatically as the severity of apical periodontitis increased (from 41.5% in those without periodontal disease to 100%). However, the nature of the spatial relationship between the maxillary sinus floor and the infected root tips or between the sinus floor and periapical lesions did not appear to have an effect on the prevalence of maxillary sinus mucosal thickening. Patients over 60 years of age had the highest prevalence of maxillary sinus mucosal thickening. Conclusions: A retrospective inspection of CBCT images revealed that the prevalence and severity of maxillary sinus mucosal thickening were positively associated with the degree of apical periodontitis. CBCT imaging is applicable for the evaluation of the maxillary sinuses and adjacent teeth. (J Endod 2012;38:1069–1074)
Key Words Apical periodontitis, cone-beam computed tomography, maxillary sinus mucosal thickening
From the *State Key Laboratory of Oral Diseases, Department of Conservative Dentistry and the †Department of Oral Radiology, West China College of Stomatology, Sichuan University, Chengdu, China. Address requests for reprints to Dr Dingming Huang, Department of Conservative Dentistry, or Dr Hu Wang, Department of Radiology, 14# 3rd Section, Renmin South Road, Chengdu, Sichuan Province 610041, China. E-mail address: [email protected] or [email protected] 0099-2399/$ - see front matter Copyright ª 2012 American Association of Endodontists. doi:10.1016/j.joen.2012.04.027
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axillary sinusitis, or inflammation of the maxillary sinuses, may be infectious and is caused by bacterial, fungal, or viral agents. Approximately 10% to 12% of all maxillary sinusitis cases are caused by odontogenic infection, aided by the close proximity of the roots of the maxillary posterior teeth to the maxillary sinus cavities (1). A study by Eberhardt et al (2) reported a mean distance of 1.97 mm between the floor of the maxillary sinus and the roots of the adjoining maxillary premolar and molar teeth. The displacement of bacteria from infected periapical tissue often results in acute or chronic sinusitis. Several studies have reported varying prevalence rates of odontogenic maxillary sinusitis, ranging from 10% to 86% (1, 3–5). One recent study reported that 98 of 135 maxillary sinusitis cases were tooth related, presenting with changes in the integrity of the maxillary sinus floor (6). Apical periodontitis (7), periodontal disease (7, 8), implant therapy (9), and tooth extraction (10) are thought to increase the risk of maxillary sinusitis. Apical and marginal periodontitis together constitute 83% of all dental causes (7). The role of apical periodontitis in maxillary sinusitis has not been well documented, although it has been recorded in a few cases (11). The close anatomic proximity of root apices to the maxillary sinuses makes dental disease, especially periapical lesion, a potential source for the spread of the disease into the maxillary sinuses. Mild maxillary sinus mucosal thickening is a normal finding in a symptomless person (12). Vallo et al (13) reported maxillary sinus mucosal thickening in 12% of the 5,021 individuals in their study, but the mucosal thickening was greater than 2 mm in most of the patients with maxillary sinusitis (14). Therefore, sinus mucosal thickening more than 2 mm in depth was an important indicator of maxillary sinusitis and was considered to be a pathologic condition. A conservative treatment approach can be used to resolve the symptoms of a maxillary sinus infected by apical periodontitis. Cone-beam computed tomography (CBCT) scanning is a new 3-dimensional (3D) imaging modality that could be of clinical value not only during screening but also in planning treatments. One of the benefits of applying CBCT scanning for imaging of the paranasal sinuses, including the maxillary sinus, is the lower radiation dose when compared with computed tomography imaging (15, 16). Moreover, CBCT scanning allows for higher resolution and a reduced scanning time. This study was designed to assess the relationship between the sinus mucosal thickening and the degree of apical periodontitis, and the anatomic position of root tips and apical lesions, and the age of patients.
Materials and Methods This retrospective radiologic study was conducted with the approval of the Institutional Review Board of Sichuan University, Chengdu, China. CBCT scans of consecutive patients undergoing various procedures at the West China Hospital of Stomatology were collected from June 2009 through May 2011. Patients with at least one maxillary sinus exposure were included in the study. Patients with edentulous maxillae, patients having one or more maxillary implants, or patients who were scanned for the evaluation of an acute traumatic injury were excluded. A total of 372 patients (194 females and 178 males) who had 508 exposed maxillary sinuses met our inclusion criteria. The age
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Figure 1. Degrees of maxillary sinus mucosal thickening and apical periodontitis. (A) Normal mucosa of the maxillary sinus, (B) sinus mucosal thickening <2 mm, (C) mucosal thickening 2 to 4 mm, (D) mucosal thickening 4 to 10 mm, and (E) mucosal thickening >10 mm. (F) Normal periapical structures, (G) minor changes in bone structure, (H) changes in bone structure with some mineral loss, (I) periodontitis with a well-defined radiolucent area, and (J) severe periodontitis with exacerbating features. Arrows indicate the periapical lesion.
of the patients ranged from 11 to 72 years with a mean age of 35.8 15.53 years. To evaluate the influence of age on the prevalence and severity of maxillary sinus mucosal thickening, the patients’ records were separated into the following subgroups based on age: 0 to 18, 19 to 25, 26 to 40, 41 to 60, and >60 years of age. A 3D Accuitomo CBCT scanner (MCT-1[EX-2F]; J Morita Manufacturing, Kyoto, Japan) was used in this study, providing a grayscale image of 14 bits with a voxel size of 0.125 mm per side. The CBCT images were viewed using volume-rendering software (One Volume Viewer, J Morita, Japan) on a Dell 24-inch LCD monitor (1,920 1,200 resolution) (Dell Computer Corp, Ron Droke, TX). To ensure data reliability, 2 observers (trained specialists in endodontics) who were assisted by a radiologist with endodontic experience calibrated
their interpretations by reviewing and discussing 20 previously selected CBCT images of maxillary sinuses with different morphologies. Images of the study were evaluated twice, with a 1-week interval between assessments. Interreviewer reliability was assessed using Cohen k statistical analysis. Using the periapical index scoring system (17), the periapical status was graded as follows: 1, normal periapical structures; 2, small changes in bone structure; 3, changes in bone structure with some mineral loss; 4, periodontitis with a well-defined radiolucent area; and 5, severe periodontitis with exacerbating features (Fig. 1). If the patient had more than one tooth or root that was associated with a periapical lesion, the one with the most severe pathology was recorded. Maxillary sinuses were divided into 5 classes according to the maximal
Figure 2. Classifications of relations between the maxillary sinus floor and root tips or periapical lesion. (A) The root tip entered the sinus floor, (B) the root tip is in contact with the sinus floor, (C) a gap is present between the root tip and the sinus floor, (D) the lesion has entered the sinus floor, (E) the lesion is in contact with the sinus floor, and (F) a gap between the lesion and the sinus floor.
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Clinical Research TABLE 1. Classes of Maxillary Sinus Mucosal Thickening Identified by CBCT Imaging and the Association between Maxillary Mucosal Thickening and Periapical Lesion Types Periapical lesions†
Maxillary sinus
Maxillary sinusitis mucosal thickening*
Left
Right
Total
Type 1‡,§
Type 2‡
Type 3‡
Type 4‡
Type 5§
Total
Class 1 Class 2 Class 3 Class 4 Class 5 Total
113 34 75 32 14 268
91 35 68 32 14 240
204 69 143 64 28 508
196 63 121 44 19 443
3 1 8 4 2 18
2 1 1 7 2 13
3 4 9 6 5 27
0 0 4 3 0 7
204 69 143 64 28 508
Significant differences were found for the following comparisons: type 1 versus types 2, 3, and 4 (‡P < .01) and type 1 versus type 5 (§P < .01). *Classes based on maximal mucosal thickening: 1, normal; 2, <2 mm; 3, 2 to 4 mm (mild maxillary sinus mucosal thickening); 4, 4 to10 mm (moderate); and 5, >10 mm (severe). † Types follow the PAI scoring system: 1, normal periapical structures; 2, small changes in bone structure; 3, changes in bone structure with some mineral loss; 4, periodontitis with a well-defined radiolucent area; 5, severe periodontitis with exacerbating features.
mucosal thickening present in the exposed maxillary sinus: 1, normal (no mucosal thickening); 2, 0 to 2 mm; 3, 2 to 4 mm (mild maxillary sinus mucosal thickening); 4, 4 to10 mm (moderate); and 5, >10 mm (severe) (14) (Fig. 1). To investigate a possible correlation between oroantral communication and the CBCT findings, the images were inspected, and the positions of the root tips and periapical lesions in relation to the sinus floor were categorized. This permitted separation of the apices into 3 types of anatomic relationships: 1, with a gap or space between the root tip and the sinus floor; 2, the root tip touched the sinus floor; and 3, the root tip entered the sinus floor. (If there were more than one root, we recorded the root with the closest proximity.) The following categories were applied for the periapical lesions: 1, with a space between the lesion and the sinus floor; 2, the lesion was in contact with the sinus floor; and 3, the lesion entered the sinus floor (Fig. 2). After interexaminer calibration, axial, coronal, and sagittal sections of each image were evaluated. If there was a disagreement in the interpretation of images, a consensus was reached after discussion between the 2 observers. The mucosal thickness, periapical lesions of adjacent teeth and roots, tooth position, and patient sex and age were noted and recorded. Mucosal thickness was measured at the point of maximum thickness from the sinus floor. The diameter of the periapical lesion was measured at the maximum range. The complete data of patients, images, and assigned scores were statistically analyzed using SPSS16.0 for Windows (SPSS Inc, Chicago, IL). The chi-square test was used to compare groups. An error probability of <0.5 was accepted as significant.
Results Prevalence and Pathologic Degree of Maxillary Sinus Mucosal Thickening Mucosal thickening in either one or both maxillary sinuses was found in 180 (48.4%) of the patients. Fifty-five patients (14.8%) presented with mucosal thickenings >2 mm (class 3 or higher) in both sinuses and 125 patients (33.6%) in one sinus. Of the 372 investigated patient images, 192 (51.6%) presented with no maxillary sinusitis (ie, no mucosal thickening detected on the images or uniform mucosal thickening <2 mm) in either the left or right maxillary sinus. Among all the 508 exposed maxillary sinuses, 235 (46.2%) were associated with sinus mucosal thickening of varying degrees (Table 1). The mean maxillary sinus mucosal thickening was 2.78 mm (2.73 mm on the left side and 2.83 mm on the right side). In sinuses in which the thickening was more than 2 mm, the mean mucosal thickening was 5.59 mm (5.67 mm on the left side and 5.52 mm on the right side). Prevalence and Pathologic Degree of Periapical Lesions in Maxillary Sinus Mucosal Thickening Periapical lesions were found in 56 (29.2%) patients with maxillary sinus mucosal thickening (47 unilateral and 9 bilateral). There were 88 teeth and 175 roots that were associated with sinus mucosal thickening. Among the teeth with apical periodontitis, 28 were second premolars, 46 were first molars, 14 were second molars, and 1 was a third molar. Those roots found to be predominantly associated with
Figure 3. (A) The association between the periapical lesion and maxillary sinus mucosal thickening. The likelihood of identifying maxillary sinus mucosal thickening increased with the severity of the periapical lesion. (B) The correlation between the age of the patient and maxillary sinus mucosal thickening. The prevalence of maxillary sinus mucosal thickening increased with patients’ age.
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Clinical Research TABLE 2. The Anatomic Relationship between the Sinus Floor and the Root Tips of Adjacent Teeth and the Anatomic Relationship between the Sinus Floor and the Associated Periapical Lesion
Maxillary sinusitis mucosal thickening Class 1 Class 2 Class 3 Class 4 Class 5 Total
Anatomic relationship between the sinus floor and root tips*
Anatomic relationship between the sinus floor and the associated periapical lesion†
Type 1
Type 2
Type 3
Total
Type I
Type II
Type III
Total
126 52 95 41 17 331
38 7 23 11 4 83
40 10 25 12 7 94
208 69 143 64 28 508
3 2 10 5 2 22
1 2 7 5 2 17
3 2 10 7 4 26
7 6 27 17 8 65
*1, with a gap or space between the root tip and the sinus floor; 2, the root tip touched the sinus floor; and 3, the root tip entered the sinus floor. † I with a space between the lesion and the sinus floor; II, the lesion was in contact with the sinus floor; and III, the lesion entered the sinus floor.
maxillary sinus mucosal thickening were the mesiobuccal (44 roots) and distobuccal (38 roots) roots of the first molar and that of the second premolar (28 roots). The mean diameter of the apical periodontal lesion was 2.59 mm. The probability of maxillary sinus mucosal thickening increased dramatically as the degree of apical periodontitis increased (Fig. 3A). The prevalence of maxillary sinus mucosal thickening for a patient with no apical periodontitis was 41.5% (184/443) but increased to 77.8% (14/18), 76.9% (10/13,) 74.1% (20/27), and 100% (7/7) for those presenting with classes 2, 3, 4, and 5, respectively (Table 1).
Prevalence of Maxillary Sinus Mucosal Thickening and the Anatomic Relationship between the Sinus Floor and Associated Teeth The majority of patients, encompassing all degrees of maxillary sinus mucosal thickening, had an anatomic relationship between the root tip and sinus floor typified by a gap or space between the root tip and the sinus floor (331/508, Table 2). The prevalence of maxillary sinus mucosal thickening (a mean thickening of mucosae $2 mm) in these patients was 46.2% (153/331). In 83 patients, the root tip touched the sinus floor, and the prevalence of maxillary sinus mucosal thickening was 45.8% (38/83). In 94 patients, the root tip entered the sinus floor, and the prevalence of maxillary sinus mucosal thickening was 46.8% (44/94). Among those patients with periapical lesions (Table 2), 22 had a space between the sinus floor and the lesion (prevalence of maxillary sinus mucosal thickening = 77.3%, 17/22). The lesion was found to be in contact with the sinus floor in 17 patients (maxillary sinus mucosal thickening = 82.4%, 14/17), whereas in the remaining 26 patients with periapical lesions, the lesion entered the sinus floor (maxillary sinus mucosal thickening = 80.8%, 21/26). Age and Prevalence of Maxillary Sinus Mucosal Thickening Table 3 and Figure 3B show the correlation between age and maxillary sinus mucosal thickening. The prevalence of maxillary sinus mucosal thickening was 31.8% (14/44) among the juvenile patients (#18 years), 37.4% (34/91) among the young patients (19-25 years), 55.7% (49/88) among the adults (26-40 years), 60.7% (74/122) among the patients aged between 41 to 60 years, and 81.5% (22/27) among geriatric patients (>60 years). Differences between age groups and the likelihood of presenting with sinus mucosal thickening were statistically significant (P < .01), and patients more than 60 years of age were found to be most likely to present with the condition. 1072
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Discussion Conventional radiographic techniques used to diagnose maxillary sinus mucosal thickening and apical periodontitis include Xray radiography, magnetic resonance, computed tomography scanning, and conventional periapical radiography. CBCT scanning is a technological innovation developed in recent years and could be used in oral surgery, orthodontic evaluation, implant treatment planning, apical periodontitis evaluation, and periodontal disease planning (18). Some studies have reported that the accuracy of CBCT scanning parallels that of computed tomography scanning and conventional radiography in hard tissue and endodontics (19–22). CBCT imaging was helpful in elucidating the etiology and extent of the relationship between the dental pathology and the involved sinus (23). It was also helpful in evaluating the preoperative and postoperative conditions of the maxillary sinuses (24). Currently, CBCT systems can be classified into 2 categories: limited (dental and regional) and full (ortho or facial). The voxel size of the limited CBCT system is small (0.1-0.2 mm), offers higher resolution, and is better suited for endodontic applications (10). In this study, we evaluated the degrees of maxillary sinus mucosal thickening and apical periodontitis as well as the distance between the sinus floor and the root tips or apical lesions using the limited CBCT system because anatomic structures are seen in clearer detail than with the full CBCT system. Using CBCT scanning, Maillet et al (6) found that odontogenic sinusitis can be identified as localized thickening of the mucous membrane of the maxillary sinus associated with dental lesions. Ritter et al (3) reported mucosal thickenings in either one or both sinuses in 38.1% of patients. In comparison, Bolger et al (25) and H€ahnel et al (26), both using computed tomography scanning, found such thickenings in 83.2% and 60%, respectively. Studies based on magnetic resonance imaging found a prevalence of 50% (27). In our study, 48.4% were found with maxillary sinus mucosal thickening. This variation could be TABLE 3. The Relationship between the Degree of Maxillary Sinus Mucosal Thickening and Age of Patients Maxillary sinus mucosal thickening Age (y) Class 1 Class 2 Class 3 Class 4 Class 5 Total #18 19–25 26–40 41–60 >60 Total
24 48 27 33 4 134
6 9 12 15 1 43
10 22 29 42 11 117
3 10 14 20 6 52
1 2 6 12 5 24
44 91 88 122 27 372
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Clinical Research attributed to the differences in race or age as well as the different diagnostic techniques used. Maxillary sinusitis has been attributed to apical periodontitis and other odontogenic infections. The likelihood of a dental source of infection increased with the degree of mucosal thickening (5). However, to our knowledge, there have been no other reports associating the severity of apical periodontitis with maxillary sinus mucosal thickening. This study has successfully shown a positive correlation between the degree of apical periodontitis and sinus mucosal thickening. The prevalence of maxillary sinus mucosal thickening was 41.5% in patients without apical periodontitis, more than 70% in patients with mild and moderate apical periodontitis, and 100% for those with severe apical periodontitis. Although the differences in the prevalence of maxillary sinus mucosal thickening with regard to the degree of apical periodontitis were not statistically significant, they were highest for severe apical periodontitis. We believe that bacteria and toxins in apical lesions can infiltrate the maxillary sinuses directly or via the numerous vascular anastomoses, porous alveolar bone marrow, and lymphatics, thereby infecting the sinus mucosa. An increase in the quantity of bacteria and toxins results in an increase in the severity of apical periodontitis and thus increases the likelihood of maxillary sinus mucosal thickening. However, when the growth of the periapical lesion was limited (periapical index grades 2, 3, and 4), the prevalence rate of maxillary sinus mucosal thickening appeared to be unaffected. Oberli et al (28) investigated 113 radiographic parameters and reported that in 70.4% of patients there was a space between the root tip and the sinus floor. In 19.2%, the root tip overlapped the sinus floor, and in 10.4% the root tip touched the sinus floor. According to their results, type 1 was the most common; the least common was type 2. However, periapical lesions in relation to the sinus floor were as follows: type 3 (44.8%) > type 1 (33.6%) > type 2 (21.6%). We found that root tips in relation to the sinus floor fell into the categories type 1 (65.2%, 331/508) > type 3 (18.5%, 94/508) > type 2 (16.3%, 83/ 508), whereas that of periapical lesions in relation to the sinus floor were class 3 (40%, 26/65) > class 1 (33.8%, 22/65) > class 2 (26.2%, 17/65). In the present study, type 3 described the condition in which the root tip and lesion entered the sinus floor, and with 3D CBCT images we could observe the samples in axial, coronal, and sagittal sections. Thus, we obtained the true spatial relationship between the sinus and root tip and the sinus and lesion. Although the locations of root tips and/or lesions were different, there were no significant differences in the prevalence of maxillary sinus mucosal thickening, suggesting that the porous maxillary alveolar bone cannot resist bacteria or other toxins and the integrity of the mucous membrane acts as a shield for the sinus. The volume of the maxillary sinus decreases after about 20 years of age (29, 30), but the more important changes occur in the masticatory system. With age, almost every individual presents with dental ailments, including periodontal disease, apical abscess, missing teeth, and other pathologic conditions, and this has also been shown to increase the likelihood of maxillary sinusitis (5, 31). Because anaerobic bacteria are more likely to be found in odontogenic maxillary sinusitis (32), normal antibiotics used to treat routine sinusitis are less effective in the treatment of odontogenic sinusitis. Therefore, it is very important to accurately diagnose the origin of the sinusitis before treatment. Our study is limited by the inclusion of only those suspected maxillary sinusitis patients with mucosal thickening, although some patients with maxillary sinusitis do not present with mucosal thickening or the associated sinus fluid. However, because our hospital is a tertiary referral center, patients are more likely to present with treatmentresistant disease than in a primary care facility. Also, observers in this study were not trained radiologists and may have limited experience JOE — Volume 38, Number 8, August 2012
in evaluating the pathologic findings of maxillary sinus and other anatomic structures. Lastly, we were able to include only a small number of apical periodontitis cases.
Conclusions Within the limitations of this study, 4 principal conclusions may be drawn: (1) the prevalence rate of maxillary sinus mucosal thickening was high, with nearly half of the patients presenting with radiographic symptoms; (2) among the patients with maxillary posterior teeth apical periodontitis, more than 80% had maxillary sinus mucosal thickening, and the prevalence of maxillary sinus mucosal thickening increased with the size of the lesion; (3) the anatomic relationship between root tips or periapical lesions and the maxillary sinus floor did not influence the likelihood of maxillary sinus mucosal thickening development; and (4) the prevalence of maxillary sinus mucosal thickening increased with the age of the patient.
Acknowledgments The authors deny any conflicts of interest related to this study.
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26. H€ahnel S, Ertl-Wagner B, Tasman AJ, Forsting M, Jansen O. Relative value of MR imaging as compared with CT in the diagnosis of inflammatory paranasal sinus Disease. Radiology 1999;210:171–6. 27. Kristo A, Alho OP, Luotonen J, Koivunen P, Tervonen O, Uhari M. Cross-sectional survey of paranasal sinus magnetic resonance imaging finding in schoolchildren. Acta Paediatr 2003;92:34–6. 28. Oberli K, Bornstein M, von Arx T. Periapical surgery and maxillary sinus: radiographic parameters for clincial outcome. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007;103:848–53. 29. Ariji Y, Kuroki T, Moriguchi S, Ariji E, Kanda S. Age changes in the volume of the human maxillary sinus: a study using computed tomography. Dentomaxillofacial Radiology 1994;23:163–8. 30. Ezemagu UK, Mgbor N, Anibeze CIP, Akpuaka FC. Age and sex related variations in the maxillary sinus of southeast Nigerians. Journal of Experimental and Clinical Anatomy 2005;4:33–8. 31. Abrahams JJ, Glassberg RM. Dental disease: a frequently unrecognized cause of maxillary sinus abnormalities? AJR Am J Roentgenol 1996;166:1219–23. 32. Brook I. Microbiology of acute and chronic maxillary sinusitis associated with an odontogenic origin. Laryngoscope 2005;115:823–5.
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Associations between Maxillary Sinus Mucosal Thickening and Apical Periodontitis Using Cone-Beam Computed Tomography Scanning: A Retrospective Study Yu Lu, DDS,* Zhongjun Liu, DDS,* Lan Zhang, DDS,* Xuedong Zhou, DDS, PhD,* Qinghua Zheng, DDS,* Xingyu Duan, DDS,* Guangning Zheng, DDS,† Hu Wang, MD,† and Dingming Huang, DDS, PhD* Abstract Introduction: This study evaluated the pathologic and spatial associations between apical periodontitis of the maxillary premolars/molars and the maxillary sinus mucosal thickening using cone-beam computed tomography (CBCT) scanning. Methods: CBCT images of 372 patients with 508 exposed maxillary sinuses were inspected retrospectively. Clinical features such as sex and age of the patients and pathologic findings of the maxillary sinus and adjacent teeth were recorded, graded, and analyzed. Results: Maxillary sinus mucosal thickening was found in 180 (48.4%) patients and 235 (46.2%) sinuses. The prevalence of maxillary sinus mucosal thickening increased dramatically as the severity of apical periodontitis increased (from 41.5% in those without periodontal disease to 100%). However, the nature of the spatial relationship between the maxillary sinus floor and the infected root tips or between the sinus floor and periapical lesions did not appear to have an effect on the prevalence of maxillary sinus mucosal thickening. Patients over 60 years of age had the highest prevalence of maxillary sinus mucosal thickening. Conclusions: A retrospective inspection of CBCT images revealed that the prevalence and severity of maxillary sinus mucosal thickening were positively associated with the degree of apical periodontitis. CBCT imaging is applicable for the evaluation of the maxillary sinuses and adjacent teeth. (J Endod 2012;38:1069–1074)
Key Words Apical periodontitis, cone-beam computed tomography, maxillary sinus mucosal thickening
From the *State Key Laboratory of Oral Diseases, Department of Conservative Dentistry and the †Department of Oral Radiology, West China College of Stomatology, Sichuan University, Chengdu, China. Address requests for reprints to Dr Dingming Huang, Department of Conservative Dentistry, or Dr Hu Wang, Department of Radiology, 14# 3rd Section, Renmin South Road, Chengdu, Sichuan Province 610041, China. E-mail address: [email protected] or [email protected] 0099-2399/$ - see front matter Copyright ª 2012 American Association of Endodontists. doi:10.1016/j.joen.2012.04.027
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axillary sinusitis, or inflammation of the maxillary sinuses, may be infectious and is caused by bacterial, fungal, or viral agents. Approximately 10% to 12% of all maxillary sinusitis cases are caused by odontogenic infection, aided by the close proximity of the roots of the maxillary posterior teeth to the maxillary sinus cavities (1). A study by Eberhardt et al (2) reported a mean distance of 1.97 mm between the floor of the maxillary sinus and the roots of the adjoining maxillary premolar and molar teeth. The displacement of bacteria from infected periapical tissue often results in acute or chronic sinusitis. Several studies have reported varying prevalence rates of odontogenic maxillary sinusitis, ranging from 10% to 86% (1, 3–5). One recent study reported that 98 of 135 maxillary sinusitis cases were tooth related, presenting with changes in the integrity of the maxillary sinus floor (6). Apical periodontitis (7), periodontal disease (7, 8), implant therapy (9), and tooth extraction (10) are thought to increase the risk of maxillary sinusitis. Apical and marginal periodontitis together constitute 83% of all dental causes (7). The role of apical periodontitis in maxillary sinusitis has not been well documented, although it has been recorded in a few cases (11). The close anatomic proximity of root apices to the maxillary sinuses makes dental disease, especially periapical lesion, a potential source for the spread of the disease into the maxillary sinuses. Mild maxillary sinus mucosal thickening is a normal finding in a symptomless person (12). Vallo et al (13) reported maxillary sinus mucosal thickening in 12% of the 5,021 individuals in their study, but the mucosal thickening was greater than 2 mm in most of the patients with maxillary sinusitis (14). Therefore, sinus mucosal thickening more than 2 mm in depth was an important indicator of maxillary sinusitis and was considered to be a pathologic condition. A conservative treatment approach can be used to resolve the symptoms of a maxillary sinus infected by apical periodontitis. Cone-beam computed tomography (CBCT) scanning is a new 3-dimensional (3D) imaging modality that could be of clinical value not only during screening but also in planning treatments. One of the benefits of applying CBCT scanning for imaging of the paranasal sinuses, including the maxillary sinus, is the lower radiation dose when compared with computed tomography imaging (15, 16). Moreover, CBCT scanning allows for higher resolution and a reduced scanning time. This study was designed to assess the relationship between the sinus mucosal thickening and the degree of apical periodontitis, and the anatomic position of root tips and apical lesions, and the age of patients.
Materials and Methods This retrospective radiologic study was conducted with the approval of the Institutional Review Board of Sichuan University, Chengdu, China. CBCT scans of consecutive patients undergoing various procedures at the West China Hospital of Stomatology were collected from June 2009 through May 2011. Patients with at least one maxillary sinus exposure were included in the study. Patients with edentulous maxillae, patients having one or more maxillary implants, or patients who were scanned for the evaluation of an acute traumatic injury were excluded. A total of 372 patients (194 females and 178 males) who had 508 exposed maxillary sinuses met our inclusion criteria. The age
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Figure 1. Degrees of maxillary sinus mucosal thickening and apical periodontitis. (A) Normal mucosa of the maxillary sinus, (B) sinus mucosal thickening <2 mm, (C) mucosal thickening 2 to 4 mm, (D) mucosal thickening 4 to 10 mm, and (E) mucosal thickening >10 mm. (F) Normal periapical structures, (G) minor changes in bone structure, (H) changes in bone structure with some mineral loss, (I) periodontitis with a well-defined radiolucent area, and (J) severe periodontitis with exacerbating features. Arrows indicate the periapical lesion.
of the patients ranged from 11 to 72 years with a mean age of 35.8 15.53 years. To evaluate the influence of age on the prevalence and severity of maxillary sinus mucosal thickening, the patients’ records were separated into the following subgroups based on age: 0 to 18, 19 to 25, 26 to 40, 41 to 60, and >60 years of age. A 3D Accuitomo CBCT scanner (MCT-1[EX-2F]; J Morita Manufacturing, Kyoto, Japan) was used in this study, providing a grayscale image of 14 bits with a voxel size of 0.125 mm per side. The CBCT images were viewed using volume-rendering software (One Volume Viewer, J Morita, Japan) on a Dell 24-inch LCD monitor (1,920 1,200 resolution) (Dell Computer Corp, Ron Droke, TX). To ensure data reliability, 2 observers (trained specialists in endodontics) who were assisted by a radiologist with endodontic experience calibrated
their interpretations by reviewing and discussing 20 previously selected CBCT images of maxillary sinuses with different morphologies. Images of the study were evaluated twice, with a 1-week interval between assessments. Interreviewer reliability was assessed using Cohen k statistical analysis. Using the periapical index scoring system (17), the periapical status was graded as follows: 1, normal periapical structures; 2, small changes in bone structure; 3, changes in bone structure with some mineral loss; 4, periodontitis with a well-defined radiolucent area; and 5, severe periodontitis with exacerbating features (Fig. 1). If the patient had more than one tooth or root that was associated with a periapical lesion, the one with the most severe pathology was recorded. Maxillary sinuses were divided into 5 classes according to the maximal
Figure 2. Classifications of relations between the maxillary sinus floor and root tips or periapical lesion. (A) The root tip entered the sinus floor, (B) the root tip is in contact with the sinus floor, (C) a gap is present between the root tip and the sinus floor, (D) the lesion has entered the sinus floor, (E) the lesion is in contact with the sinus floor, and (F) a gap between the lesion and the sinus floor.
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Clinical Research TABLE 1. Classes of Maxillary Sinus Mucosal Thickening Identified by CBCT Imaging and the Association between Maxillary Mucosal Thickening and Periapical Lesion Types Periapical lesions†
Maxillary sinus
Maxillary sinusitis mucosal thickening*
Left
Right
Total
Type 1‡,§
Type 2‡
Type 3‡
Type 4‡
Type 5§
Total
Class 1 Class 2 Class 3 Class 4 Class 5 Total
113 34 75 32 14 268
91 35 68 32 14 240
204 69 143 64 28 508
196 63 121 44 19 443
3 1 8 4 2 18
2 1 1 7 2 13
3 4 9 6 5 27
0 0 4 3 0 7
204 69 143 64 28 508
Significant differences were found for the following comparisons: type 1 versus types 2, 3, and 4 (‡P < .01) and type 1 versus type 5 (§P < .01). *Classes based on maximal mucosal thickening: 1, normal; 2, <2 mm; 3, 2 to 4 mm (mild maxillary sinus mucosal thickening); 4, 4 to10 mm (moderate); and 5, >10 mm (severe). † Types follow the PAI scoring system: 1, normal periapical structures; 2, small changes in bone structure; 3, changes in bone structure with some mineral loss; 4, periodontitis with a well-defined radiolucent area; 5, severe periodontitis with exacerbating features.
mucosal thickening present in the exposed maxillary sinus: 1, normal (no mucosal thickening); 2, 0 to 2 mm; 3, 2 to 4 mm (mild maxillary sinus mucosal thickening); 4, 4 to10 mm (moderate); and 5, >10 mm (severe) (14) (Fig. 1). To investigate a possible correlation between oroantral communication and the CBCT findings, the images were inspected, and the positions of the root tips and periapical lesions in relation to the sinus floor were categorized. This permitted separation of the apices into 3 types of anatomic relationships: 1, with a gap or space between the root tip and the sinus floor; 2, the root tip touched the sinus floor; and 3, the root tip entered the sinus floor. (If there were more than one root, we recorded the root with the closest proximity.) The following categories were applied for the periapical lesions: 1, with a space between the lesion and the sinus floor; 2, the lesion was in contact with the sinus floor; and 3, the lesion entered the sinus floor (Fig. 2). After interexaminer calibration, axial, coronal, and sagittal sections of each image were evaluated. If there was a disagreement in the interpretation of images, a consensus was reached after discussion between the 2 observers. The mucosal thickness, periapical lesions of adjacent teeth and roots, tooth position, and patient sex and age were noted and recorded. Mucosal thickness was measured at the point of maximum thickness from the sinus floor. The diameter of the periapical lesion was measured at the maximum range. The complete data of patients, images, and assigned scores were statistically analyzed using SPSS16.0 for Windows (SPSS Inc, Chicago, IL). The chi-square test was used to compare groups. An error probability of <0.5 was accepted as significant.
Results Prevalence and Pathologic Degree of Maxillary Sinus Mucosal Thickening Mucosal thickening in either one or both maxillary sinuses was found in 180 (48.4%) of the patients. Fifty-five patients (14.8%) presented with mucosal thickenings >2 mm (class 3 or higher) in both sinuses and 125 patients (33.6%) in one sinus. Of the 372 investigated patient images, 192 (51.6%) presented with no maxillary sinusitis (ie, no mucosal thickening detected on the images or uniform mucosal thickening <2 mm) in either the left or right maxillary sinus. Among all the 508 exposed maxillary sinuses, 235 (46.2%) were associated with sinus mucosal thickening of varying degrees (Table 1). The mean maxillary sinus mucosal thickening was 2.78 mm (2.73 mm on the left side and 2.83 mm on the right side). In sinuses in which the thickening was more than 2 mm, the mean mucosal thickening was 5.59 mm (5.67 mm on the left side and 5.52 mm on the right side). Prevalence and Pathologic Degree of Periapical Lesions in Maxillary Sinus Mucosal Thickening Periapical lesions were found in 56 (29.2%) patients with maxillary sinus mucosal thickening (47 unilateral and 9 bilateral). There were 88 teeth and 175 roots that were associated with sinus mucosal thickening. Among the teeth with apical periodontitis, 28 were second premolars, 46 were first molars, 14 were second molars, and 1 was a third molar. Those roots found to be predominantly associated with
Figure 3. (A) The association between the periapical lesion and maxillary sinus mucosal thickening. The likelihood of identifying maxillary sinus mucosal thickening increased with the severity of the periapical lesion. (B) The correlation between the age of the patient and maxillary sinus mucosal thickening. The prevalence of maxillary sinus mucosal thickening increased with patients’ age.
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Clinical Research TABLE 2. The Anatomic Relationship between the Sinus Floor and the Root Tips of Adjacent Teeth and the Anatomic Relationship between the Sinus Floor and the Associated Periapical Lesion
Maxillary sinusitis mucosal thickening Class 1 Class 2 Class 3 Class 4 Class 5 Total
Anatomic relationship between the sinus floor and root tips*
Anatomic relationship between the sinus floor and the associated periapical lesion†
Type 1
Type 2
Type 3
Total
Type I
Type II
Type III
Total
126 52 95 41 17 331
38 7 23 11 4 83
40 10 25 12 7 94
208 69 143 64 28 508
3 2 10 5 2 22
1 2 7 5 2 17
3 2 10 7 4 26
7 6 27 17 8 65
*1, with a gap or space between the root tip and the sinus floor; 2, the root tip touched the sinus floor; and 3, the root tip entered the sinus floor. † I with a space between the lesion and the sinus floor; II, the lesion was in contact with the sinus floor; and III, the lesion entered the sinus floor.
maxillary sinus mucosal thickening were the mesiobuccal (44 roots) and distobuccal (38 roots) roots of the first molar and that of the second premolar (28 roots). The mean diameter of the apical periodontal lesion was 2.59 mm. The probability of maxillary sinus mucosal thickening increased dramatically as the degree of apical periodontitis increased (Fig. 3A). The prevalence of maxillary sinus mucosal thickening for a patient with no apical periodontitis was 41.5% (184/443) but increased to 77.8% (14/18), 76.9% (10/13,) 74.1% (20/27), and 100% (7/7) for those presenting with classes 2, 3, 4, and 5, respectively (Table 1).
Prevalence of Maxillary Sinus Mucosal Thickening and the Anatomic Relationship between the Sinus Floor and Associated Teeth The majority of patients, encompassing all degrees of maxillary sinus mucosal thickening, had an anatomic relationship between the root tip and sinus floor typified by a gap or space between the root tip and the sinus floor (331/508, Table 2). The prevalence of maxillary sinus mucosal thickening (a mean thickening of mucosae $2 mm) in these patients was 46.2% (153/331). In 83 patients, the root tip touched the sinus floor, and the prevalence of maxillary sinus mucosal thickening was 45.8% (38/83). In 94 patients, the root tip entered the sinus floor, and the prevalence of maxillary sinus mucosal thickening was 46.8% (44/94). Among those patients with periapical lesions (Table 2), 22 had a space between the sinus floor and the lesion (prevalence of maxillary sinus mucosal thickening = 77.3%, 17/22). The lesion was found to be in contact with the sinus floor in 17 patients (maxillary sinus mucosal thickening = 82.4%, 14/17), whereas in the remaining 26 patients with periapical lesions, the lesion entered the sinus floor (maxillary sinus mucosal thickening = 80.8%, 21/26). Age and Prevalence of Maxillary Sinus Mucosal Thickening Table 3 and Figure 3B show the correlation between age and maxillary sinus mucosal thickening. The prevalence of maxillary sinus mucosal thickening was 31.8% (14/44) among the juvenile patients (#18 years), 37.4% (34/91) among the young patients (19-25 years), 55.7% (49/88) among the adults (26-40 years), 60.7% (74/122) among the patients aged between 41 to 60 years, and 81.5% (22/27) among geriatric patients (>60 years). Differences between age groups and the likelihood of presenting with sinus mucosal thickening were statistically significant (P < .01), and patients more than 60 years of age were found to be most likely to present with the condition. 1072
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Discussion Conventional radiographic techniques used to diagnose maxillary sinus mucosal thickening and apical periodontitis include Xray radiography, magnetic resonance, computed tomography scanning, and conventional periapical radiography. CBCT scanning is a technological innovation developed in recent years and could be used in oral surgery, orthodontic evaluation, implant treatment planning, apical periodontitis evaluation, and periodontal disease planning (18). Some studies have reported that the accuracy of CBCT scanning parallels that of computed tomography scanning and conventional radiography in hard tissue and endodontics (19–22). CBCT imaging was helpful in elucidating the etiology and extent of the relationship between the dental pathology and the involved sinus (23). It was also helpful in evaluating the preoperative and postoperative conditions of the maxillary sinuses (24). Currently, CBCT systems can be classified into 2 categories: limited (dental and regional) and full (ortho or facial). The voxel size of the limited CBCT system is small (0.1-0.2 mm), offers higher resolution, and is better suited for endodontic applications (10). In this study, we evaluated the degrees of maxillary sinus mucosal thickening and apical periodontitis as well as the distance between the sinus floor and the root tips or apical lesions using the limited CBCT system because anatomic structures are seen in clearer detail than with the full CBCT system. Using CBCT scanning, Maillet et al (6) found that odontogenic sinusitis can be identified as localized thickening of the mucous membrane of the maxillary sinus associated with dental lesions. Ritter et al (3) reported mucosal thickenings in either one or both sinuses in 38.1% of patients. In comparison, Bolger et al (25) and H€ahnel et al (26), both using computed tomography scanning, found such thickenings in 83.2% and 60%, respectively. Studies based on magnetic resonance imaging found a prevalence of 50% (27). In our study, 48.4% were found with maxillary sinus mucosal thickening. This variation could be TABLE 3. The Relationship between the Degree of Maxillary Sinus Mucosal Thickening and Age of Patients Maxillary sinus mucosal thickening Age (y) Class 1 Class 2 Class 3 Class 4 Class 5 Total #18 19–25 26–40 41–60 >60 Total
24 48 27 33 4 134
6 9 12 15 1 43
10 22 29 42 11 117
3 10 14 20 6 52
1 2 6 12 5 24
44 91 88 122 27 372
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Clinical Research attributed to the differences in race or age as well as the different diagnostic techniques used. Maxillary sinusitis has been attributed to apical periodontitis and other odontogenic infections. The likelihood of a dental source of infection increased with the degree of mucosal thickening (5). However, to our knowledge, there have been no other reports associating the severity of apical periodontitis with maxillary sinus mucosal thickening. This study has successfully shown a positive correlation between the degree of apical periodontitis and sinus mucosal thickening. The prevalence of maxillary sinus mucosal thickening was 41.5% in patients without apical periodontitis, more than 70% in patients with mild and moderate apical periodontitis, and 100% for those with severe apical periodontitis. Although the differences in the prevalence of maxillary sinus mucosal thickening with regard to the degree of apical periodontitis were not statistically significant, they were highest for severe apical periodontitis. We believe that bacteria and toxins in apical lesions can infiltrate the maxillary sinuses directly or via the numerous vascular anastomoses, porous alveolar bone marrow, and lymphatics, thereby infecting the sinus mucosa. An increase in the quantity of bacteria and toxins results in an increase in the severity of apical periodontitis and thus increases the likelihood of maxillary sinus mucosal thickening. However, when the growth of the periapical lesion was limited (periapical index grades 2, 3, and 4), the prevalence rate of maxillary sinus mucosal thickening appeared to be unaffected. Oberli et al (28) investigated 113 radiographic parameters and reported that in 70.4% of patients there was a space between the root tip and the sinus floor. In 19.2%, the root tip overlapped the sinus floor, and in 10.4% the root tip touched the sinus floor. According to their results, type 1 was the most common; the least common was type 2. However, periapical lesions in relation to the sinus floor were as follows: type 3 (44.8%) > type 1 (33.6%) > type 2 (21.6%). We found that root tips in relation to the sinus floor fell into the categories type 1 (65.2%, 331/508) > type 3 (18.5%, 94/508) > type 2 (16.3%, 83/ 508), whereas that of periapical lesions in relation to the sinus floor were class 3 (40%, 26/65) > class 1 (33.8%, 22/65) > class 2 (26.2%, 17/65). In the present study, type 3 described the condition in which the root tip and lesion entered the sinus floor, and with 3D CBCT images we could observe the samples in axial, coronal, and sagittal sections. Thus, we obtained the true spatial relationship between the sinus and root tip and the sinus and lesion. Although the locations of root tips and/or lesions were different, there were no significant differences in the prevalence of maxillary sinus mucosal thickening, suggesting that the porous maxillary alveolar bone cannot resist bacteria or other toxins and the integrity of the mucous membrane acts as a shield for the sinus. The volume of the maxillary sinus decreases after about 20 years of age (29, 30), but the more important changes occur in the masticatory system. With age, almost every individual presents with dental ailments, including periodontal disease, apical abscess, missing teeth, and other pathologic conditions, and this has also been shown to increase the likelihood of maxillary sinusitis (5, 31). Because anaerobic bacteria are more likely to be found in odontogenic maxillary sinusitis (32), normal antibiotics used to treat routine sinusitis are less effective in the treatment of odontogenic sinusitis. Therefore, it is very important to accurately diagnose the origin of the sinusitis before treatment. Our study is limited by the inclusion of only those suspected maxillary sinusitis patients with mucosal thickening, although some patients with maxillary sinusitis do not present with mucosal thickening or the associated sinus fluid. However, because our hospital is a tertiary referral center, patients are more likely to present with treatmentresistant disease than in a primary care facility. Also, observers in this study were not trained radiologists and may have limited experience JOE — Volume 38, Number 8, August 2012
in evaluating the pathologic findings of maxillary sinus and other anatomic structures. Lastly, we were able to include only a small number of apical periodontitis cases.
Conclusions Within the limitations of this study, 4 principal conclusions may be drawn: (1) the prevalence rate of maxillary sinus mucosal thickening was high, with nearly half of the patients presenting with radiographic symptoms; (2) among the patients with maxillary posterior teeth apical periodontitis, more than 80% had maxillary sinus mucosal thickening, and the prevalence of maxillary sinus mucosal thickening increased with the size of the lesion; (3) the anatomic relationship between root tips or periapical lesions and the maxillary sinus floor did not influence the likelihood of maxillary sinus mucosal thickening development; and (4) the prevalence of maxillary sinus mucosal thickening increased with the age of the patient.
Acknowledgments The authors deny any conflicts of interest related to this study.
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