Clinical, radiographic characterizations and complications of maxillary molar in a non-agomphiasis periodontitis population: a retrospective study based on CBCT three-dimensional reconstruction

Abstract

Objective

This study was aimed to delineate the clinical, 3-dimentional radiographic characteristics and complications of maxillary molar in a non-agomphiasis periodontitis population.

Materials and methods

Medical records and CBCT images were utilized to identify adult patients with periodontitis in a tertiary referral dental hospital between June 2019 and December 2020. CBCT scan coupled with 3-dimentional reconstruction were used to characterize the detailed bone thickness, absorbing height and position of maxillary molar as well as their associated conditions. All relevant descriptive epidemiological data, clinical information, radiographic details and associated complications were recorded and statistically analyzed.

Results

According to the above criteria, 577 eligible periodontitis patients were enrolled and defined as research cohort here with mean age 45 ± 4.8 years. Male patients outnumbered females with a gender ratio of 1.23:1. Our results demonstrated that the bone loss of maxillary first molar was more serious than that of second molar with tooth position symmetry. The occurrence of various complications (periodontal abscess, pulp lesions, furcation lesion and mucosal thickening) was significantly correlated to periodontal-related clinical parameters of maxillary molar.

Conclusions

Our results demonstrated the more serious bone loss of maxillary first molar with tooth position symmetry. The occurrence of various complications was significantly correlated to periodontal-related clinical parameters. Our findings offer valuable information concerning the clinical, radiographic characteristics and complications of maxillary molar in a non-agomphiasis periodontitis population.

Clinical relevance:

These findings are beneficial for clinicians to comprehensively understand the bone status, pathogenesis, and clinical management of maxillary molar in periodontitis.

Introduction

Periodontitis is a host-mediated inflammatory disease in which plaque microorganisms are the initiating factor, aggravating by plaque biofilm contamination that leads to calculus formation, local infection, severe resorption of alveolar bone, tooth mobility in the late stage, and exfoliation[1–3]. Periodontitis not only causes damage to the local tissues of the periodontium, but also affect the health of adjacent tissues and even the whole system[4, 5]. The maxillary molars are easily subject to periodontal infection because of their complicated root morphology characterized by concavity of the root surface and furcation[6]. Furthermore, the loss rate of maxillary molars caused by periodontitis is much higher than that of other positions, which also has been recognized as the most challenging area for implant treatment[7, 8]. In a 22-year follow-up study by Hirschfeld and Wasserman, 31.4% of molars were lost compared to 4.9% of single-rooted teeth[9]. Numerous studies have confirmed that most frequently lost teeth are maxillary molars as compared to mandibular teeth[10].

The consensus report of the 2017 Classification World Workshop emphasised that the degree of alveolar bone loss has been used as direct evidence of the severity and progression of periodontitis[11]. Traditionally, alveolar bone loss was occasionally diagnosed using panoramic radiographs. However, routine 2dimensional (2D) radiographic images failed to assess the thickness, absorbing height and position of alveolar bone, especially maxillary molar area as well as its spatial relationships with neighboring structures such as maxillary sinus, which are pivotal for treatment planning. Conventional CT provides highly detailed three-dimensional (3D) information without superposition of bony and dental structures. However, the disadvantages of its relatively high cost and high radiation dose outweigh these advantages during maxillary molar alveolar bone loss evaluation. With the advent of cone beam computed tomography (CBCT) and its popular utilization in dentistry, CBCT coupled with 3-dimentional reconstruction offers adequate and precise information regarding location and morphology of dental structure of interest[12]. Thus, CBCT has been advocated to determine the accurate thickness, absorbing height and position of maxillary molar alveolar bone loss caused by periodontitis as well as their associated conditions such as maxillary sinus mucosa thickening[13]. Several pioneering studies have reported the clinical and radiographic characterizations of periodontitis using CBCT scan and supported the values of CBCT to assist the diagnosis, treatment planning, and operative treatment of periodontitis[14, 15].

Except for local gingival bleeding and pain, periodontitis may also induce various complications, such as periodontal abscess, pulp lesions, furcation lesion, as well as mucosal thickening[16–18]. Several studies have documented the relationship between maxillary sinus mucosal thickening and alveolar bone loss and revealed that the severity of periodontal status of maxillary molars can influence the degree of mucosal thickening[19, 20]. Also, studies have shown that the buccal residual bone was thicker and the lingual bone was thinner in the periodontitis patients than in the periodontally healthy individuals, and there were differences between the different tooth types, sexes and age subgroups[21]. However, whether these periodontal related clinical and morphological parameters could influence the development of various complications in maxillary molar area was still unknown. Therefore, we screened maxillary molar in non-agomphious periodontitis population by CBCT radiographic examinations and presented a comprehensive view of clinical, radiographic features and associated complications of 2308 maxillary molars from 577 periodontitis patients.

The purpose of this retrospective study was to investigate the clinical, 3-dimentional CBCT radiographic characteristics and associated complications of maxillary molar in a periodontitis population. Our findings are beneficial for clinical diagnosis and treatment planning of periodontitis.

Materials And Methods

Detailed characterizations of maxillary molar in 3-dimentional CBCT radiography

All original CBCT data in DICOM format for each patient were retrieved from our CBCT radiographic data center and then individually introduced into Proplan CMF 1.4 software (Materialise NV, Leuven, Belgium) for further assessments. Detailed characterizations of maxillary molar from axial, sagittal and coronal CBCT views were listed as follows.

1. ML: length from the mesial cement-enamel junction (CEJ) to the alveolar bone crest minus 2mm; DL: length from the distal cement-enamel junction (CEJ) to the alveolar bone crest minus 2mm; MBL: length from the mesial buccal cement-enamel junction (CEJ) to the alveolar bone crest minus 2mm; DBL: length from the distal buccal cement-enamel junction (CEJ) to the alveolar bone crest minus 2mm; PL: length from the palatal cement-enamel junction (CEJ) to the alveolar bone crest minus 2mm. (Fig. 1)

2. MBT: the thickness of mesial buccal bone plate corresponding to the site half of the mesial buccal root; DBT: the thickness of distal bone plate corresponding to the site half of the distal buccal root; PT: the thickness of palatal bone plate corresponding to the site half of the palatal root. (Fig. 1)

3. MinH: the shortest vertical distance from the molar apical to the bottom of maxillary sinus; Type I: < 4 mm; Type II: 4–10 mm; Type III: ≥ 10 mm. (Fig. 2a1-a3)

4. Root trunk length (RTL): the shortest vertical distance from the enamel cementum boundary to the root bifurcation; Type I: ༜1/3 Root length; Type II: 1/3–1/2 Root length; Type III: ༞ 1/2 Root length. (Fig. 2b1-b3)

5. Adjacent bone defects (ABD): Type I: no vertical infrabony defects; Type II: not more than 2/3 of root; Type III: infrabony defects extending to the apical third of the tooth. (Fig. 2c1-c3)

6. ABL: measured from mesial and distal of the maxillary molars as well as the buccal and lingual side. Normal alveolar bone height was within 2 mm of the boundary of CEJ. The percentage of maximal ABL relative to normal alveolar bone height was calculated; Type 1: Mild (less than 25%); Type 2: Moderate (25–50%); Type 3: Severe (greater than 50%);

7. Furcation lesion (FL): Type I: no bone resorption; Type II: bone resorption ≤ 3 mm; Type III: bone resorption ≤ 3 mm; Type IV: penetration root furcation. (Fig. 3a1-a4)

8. MaxMT: the max thickness of sinus mucosa; Type I: No; Type II: < 4mm; Type III: 4–10mm; Type IV: > 10mm. (Fig. 3b1-b4)

Statistical analyses

All relevant descriptive epidemiological data, clinical information and radiographic details were recorded. Associations between categorical covariates were assessed by Chi-square tests or Fisher exact test as indicated. Interobserver variability and repeatability of all radiographic measurements were assessed with Cohen’s kappa values. All relevant tests in this research were bilateral. We considered that the P value system was statistically significant when less than 0.05. GraphPad Prism 9.0 and Stata 14 software was used for statistical analysis.

Results

With respect to the alveolar bone absorbing height of maxillary molar, as shown in Table 2, the mesial alveolar bone absorbing height (ML) was significantly higher than distal alveolar bone absorbing height (DL). Despite the difference between teeth position, the palatal alveolar bone absorbing height (PL) was more serious than both mesial (MBL) and distal (DBL) buccal alveolar bone absorbing height. However, regarding to alveolar bone thickness of maxillary molar, palatal alveolar bone (PT) was the thickest, followed by mesial buccal alveolar bone (MBT) and distal buccal alveolar bone (DBT). It's worth noting that no matter the absorbing height or thickness, the bone loss of the maxillary first molar was more serious than that of second molar (P < 0.0001). Apart from that, we found that symmetrical tooth position was accompanied with similar bone loss status.

To comprehensively demonstrate the periodontal-related parameters of maxillary molar in a 3dimentional manner, we analyzed these teeth from many aspects. According to a previous study[16], ABL can be classified into three levels, including mild, moderate and severe levels. In our study, the number of case at all three levels decreased gradually and shown a higher severity in the maxillary first molar area (P = 0.0167). Similar with that, no matter the mesial, distal or palatal bone thickness, the number of bone thickness above 3mm of the first molar was significantly more than that of second molar (P < 0.0001). Apart from alveolar bone status, we also analysed the MinH, adjacent bone defects, mobility degree, root trunk length and PD. First, in regard to MinH, the great majority of that were 4–10mm, and only 3–6% were above 10mm. In our study, more than half of the maxillary molars were not developed with vertical infrabony defects and a quarter of the maxillary molars were accompanied with II–III mobility degree. However, there was no difference of above-mentioned parameters between the maxillary first and second molar. Notably, of the 2308 maxillary molar, the pocket depth (PD) above 6mm was greatly higher than two other types (P = 0.0012). Specific data concerning the periodontal-related clinical parameters of maxillary molar are exhibited in Table 3.

As known to all, periodontitis could induce various complications, such as periodontal abscess, pulp lesions, furcation lesion, as well as mucosal thickening. As shown in Table 4, among 2308 maxillary molars, 792 teeth were associated with pulp lesions, and tended to occur in maxillary first molar area (P = 0.0433). However, compared with pulp lesions, the incidence of periodontal abscess was obviously lower, and shown no significance between teeth position (P = 0.1079). Additionally, more than half of maxillary molars developed with furcation lesion and the incidence gradually descended with the severity. Interestingly, in contrast to I and II furcation lesion, III furcation lesion tended to occur in maxillary first molar area (P = 0.0403). In our cohort, approximately half of the maxillary molars accompanied with mucosal thickening and shown a significant tendency in maxillary first molar area (P = 0.0005). Remarkably, sinus mucosa thicker than 10mm was occurred in 170 cases.

With aim to further explore and analyze the potential associations between these associated complications and diverse characteristics of maxillary molar, statistical analyses were performed and results are presented in Table 5. Our results demonstrated that the occurrence of various complications, including periodontal abscess, pulp lesions, and furcation lesion, as well as mucosal thickening was significantly correlated to periodontal-related clinical parameters of maxillary molar. For instance, pulp lesions tended to occur in patients in the habit of smoking, and moderate alveolar bone loss and thinner bone thickness were significantly associated with it. Notably, when MinH less than 4mm, short root trunk length and serious periodontitis clinical feature, there was a higher occurrence of pulp lesions. Moreover, periodontal abscess was more likely to occur in patients in the habit of smoking and diagnosed with diabetes. In our study, severe alveolar bone loss, thinner bone thickness and serious periodontitis clinical features tended to develop periodontal abscess of maxillary molar. With the severity of furcation lesion and mucosal thickening progressively increasing, it preferentially occurred in patients in the habit of smoking and diagnosed with diabetes. Moreover, moderate alveolar bone loss, thinner bone thickness, less MinH, shorter root trunk length and more serious periodontitis clinical features usually had a higher occurrence of furcation lesion and mucosal thickening.

Discussion

Periodontitis is a host-mediated inflammatory disease, which could induce various complications, such as periodontal abscess, pulp lesions, and furcation lesion, as well as mucosal thickening[1–3]. The maxillary molars are easily subject to periodontal infection because of their complicated root morphology characterized by concavity of the root surface and furcation[6]. However, whether these periodontal related clinical and morphological parameters could influence the development of various complications in maxillary molar area was still unknown. Here, we screened maxillary molars in non-agomphiasis periodontitis population by CBCT radiographic examinations and presented a comprehensive view of clinical, radiographic features and associated complications of 2308 maxillary molars from 577 periodontitis patients. For all we know, this might be an independent study concerning maxillary molar using CBCT in periodontitis population with the largest number of subjects, which offers valuable data for future studies.

Previous studies have established that the incidence of periodontitis is mainly concentrated in 45 years old[22]. Consistent with these prior studies, the mean age of patients enrolled here was 45.8 ± 5.8 years, which fell into the reported range. In addition, among 577 patients with periodontitis, males outnumbered females with an obvious male predilection. This notion generally corroborated the gender predilection in periodontitis as previously reported[23]. Higher prevalence in males may be due to the association of periodontitis with smoking which has a greater penetration in males[24, 25]. In terms of smoking, smokers accounted for 30.85% patients in this study, which shown a high association with various complications. In addition, diabetic patients with poor glycemic control have increased risk of retinopathy, nephropathy and macrovascular diseases, and the risk of periodontitis and progressive bone loss[26, 27]. Here, 72 of the 577 periodontitis patients were diagnosed with diabetes and shown significant correlation to periodontal abscess and furcation lesion, as well as mucosal thickening.

With respect to the alveolar bone absorbing height of maxillary molar, the mesial alveolar bone absorbing height (ML) was significantly more than distal alveolar bone absorbing height (DL) in our cohort. Additionally, Zhao et al. found that the area with the highest degree of bone loss was the lingual side of maxillary molar by a comparison of bone loss between different jaws[28]. Consistent with previous studies, our study revealed that the palatal alveolar bone absorbing height (PL) was more serious than both mesial (MBL) and distal (DBL) buccal alveolar bone absorbing height. Regarding the alveolar bone thickness of maxillary molar, the lowest mean values of bone thickness are in the buccal cortical bone of the maxillary teeth in their total number of 422 cases[29]. In accordance with these results, the thickest bone in our cohort was palatal alveolar bone (PT), followed by mesial buccal alveolar bone (MBT) and distal buccal alveolar bone (DBT). It's worth noting that no matter the absorbing height or thickness, the bone loss of the maxillary first molar was more serious than that of second molar.

Accumulating evidence has revealed that periodontitis could induce various complications, including periodontal abscess, pulp lesions, furcation lesion, as well as mucosal thickening[16–18]. First of all, the special anatomical structures, including the apical foramen, the lateral and accessory canals, and the dentinal tubules, form an intimate continuum between the periodontal and endodontic tissues, through which pathological changes of either may lead to infection of the other[30, 31]. These findings indicate the communication between the periodontal and endodontic tissues and pulp lesions could be induced by periodontitis. In our cohort, among 2308 maxillary molars, 792 teeth were associated with pulp lesions, and tended to occur in maxillary first molar area. Further study revealed that pulp lesions tended to occur in patients in the habit of smoking, and moderate alveolar bone loss and thinner bone thickness were significantly associated with it. Notably, when MinH less than 4mm, short root trunk length and serious periodontitis clinical feature, there was a higher occurrence of pulp lesions.

A furcation lesion occurs when resorption of bone due to periodontal disease extends into the bifurcation or trifurcation areas of a multi-rooted tooth[18]. There is a vast literature exploring the best treatment options for furcation lesion, but the best management involves early detection and prevention[32, 33]. This is because if a degree I furcation lesion is left untreated, it is associated with increased risk of tooth loss. Our data revealed that more than half of maxillary molars developed with furcation lesion and the incidence gradually descended with the severity. Interestingly, in contrast to I and II furcation lesion, III furcation lesion tended to occur in maxillary first molar area. Due to the close anatomical proximity of the maxillary molars and the maxillary sinus floor, thickening of the maxillary sinus mucosa was a significantly associated complication[19, 34]. The normal thickness of the maxillary sinus mucosa, also known as the Schneiderian membrane, was reported to be 1.60 ± 1.20 mm[35], as a consequence, our study used 2mm as cutoff. In our cohort, approximately half of the maxillary molars accompanied with mucosal thickening and shown a significant tendency in maxillary first molar area. Remarkably, sinus mucosa thicker than 10mm was occurred in 170 cases.

Intriguingly, our data further revealed that the occurrence of complications significantly associated with diverse characteristics of maxillary molar. Our results demonstrated that the occurrence of various complications, including periodontal abscess, pulp lesions, and furcation lesion, as well as mucosal thickening was significantly correlated to periodontal-related clinical parameters of maxillary molar. In our study, severe alveolar bone loss, thinner bone thickness and serious periodontitis clinical features tended to develop periodontal abscess of maxillary molar. With the severity of furcation lesion and mucosal thickening progressively increasing, it preferentially occurred in patients in the habit of smoking and diagnosed with diabetes. Additionally, accumulating studies have revealed that the risk of mucosal thickening in patients with severe alveolar bone loss was significantly higher than that in patients with mild alveolar bone loss[19, 34, 36]. Moreover, Vallo et.al reported that mucosal thickening was associated with periodontal pathology, including horizontal bone loss (extending to the middle third of the root), vertical subosseous pockets (extending to the middle third of the root) and furcation lesions[24]. Consistent with that, in our cohort, moderate alveolar bone loss, thinner bone thickness, less MinH, shorter root trunk length and more serious periodontitis clinical features usually had a higher occurrence of furcation lesion and mucosal thickening. The same periodontal pathogenic bacteria such Fusobacterium nucleatum and Prevotella intermedia can be detected in some maxillary lesions and maxillary sinus lesions, which provides evidence for periodontal pathogens to cause inflammatory reaction of surrounding tissues through alveolar bone[37]. These associated complications highlight the significance of early diagnosis and timely treatment of periodontitis, which might prevent or minimize the occurrence of associated local aberrations and complication.

The present study also has some limitations. Although some consistency tests have been carried out, the errors in experimental measurements and the limitations of selecting experimenters still exist. In addition, although CBCT has lower radiation dose, shorter scanning time, higher image resolution and lower cost than traditional CT, there are still indisputable differences between the CBCT measurement of relevant indicators and the real value. Meanwhile, clinical examination, histopathological and microbiological studies of pulp lesions, periodontal abscesses, furcation lesions and mucosal thickening are expected to improve the understanding mechanism of the changes in soft and hard tissues and the pathology of them. More studies on the cause and nature of these abnormalities are needed to provide the basis for proper clinical management.

Conclusion

This retrospective analysis had documented the clinical, 3D radiographic characteristics and complications of maxillary molar in a non-agomphiasis periodontitis population. Our results demonstrated the more serious bone loss of maxillary first molar with tooth position symmetry. The occurrence of various complications, including periodontal abscess, pulp lesions, furcation lesion, as well as mucosal thickening was significantly correlated to periodontal-related clinical parameters of maxillary molar. Our findings will be advantageous for clinicians to more comprehensively understand the bone status, characterization, and clinical treatment planning of maxillary molar in periodontitis.

Declarations

Acknowledgments

We would like to thank all members from Departments of Periodontics, Oral and Maxillofacial Surgery and Oral Radiography, Nanjing Medical University for their work in data collection and discussion.

Authors’ contribution

Yue Jiang, Wenxiao Cui, Qingheng Wu, Qingheng Wu, Lihe Zheng and Jialu Chen performed the radiographic analyses, data collection and statistical analyses. Xiaoqian Wang, Lu Li participated the study design, data collection and analyses. Yan Xu and Shuyu Guo conceived and supervised the whole project. Yue Jiang and Wenxiao Cui drafted the manuscript. All authors read and approved the final manuscript.

Funding information

This work was supported by the National Natural Science Foundations of China (82170962), Key projects of Jiangsu Provincial Health Commission (ZD2021025, BJ19033), Key R&D Program of Jiangsu Province (BE2020707), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD, 2018-87).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The study was reviewed and approved by the Ethics and Research Committee, Nanjing Medical University and conducted in accordance with the tenets of the Declaration of Helsinki for research involving human subjects.

Informed consent

Written informed consent was not required for this study because all of the included patients in the present investigation were collected retrospectively.

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