Introduction

Periodontitis is a multifactorial, chronic inflammatory disease associated with dysbiosis that causes tooth loss by inducing the progressive destruction of tooth-supporting tissues [1]. Periodontitis begins with periodontal attachment loss and the destruction of marginal alveolar bone. It may progress apically, involving the furcation area (FA) in molars. Longitudinal studies have indicated that molar teeth are the most affected by periodontitis, and that furcation involvement is a crucial factor affecting tooth survival rate [2]. Furcation involvement remains a challenging clinical problem. Therefore, evaluating molar root anatomy is important for proper diagnostic and therapeutic decisions. The morphology of the FA provides an appropriate location for the biofilm that causes periodontal destruction by complicating biofilm control [3]. Several morphological factors, such as root trunk length, concavities, furcation entrance, and the anatomy in the prefurcation area, have been evaluated morphometrically in the existing literature [3, 4], but to the best of our knowledge, no studies have measured the inter-radicular FA in the root separation point (RSP) in periodontitis patients. Ward et al. examined the furcation depth and inter-root separation dimensions in maxillary and mandibular teeth to clarify critical dimensions of furcation defects in regenerative therapy [5]. Roussa et al. evaluated the anatomy of furcation roof and greatest coronal root separation area. They measured the depth of concavities apical to the furcation roof in the cross-section of extracted teeth [6]. Paolantonio et al., in their morphometric and morphologic analysis, examined the furcation roof area. They measured the FA on obtained photos after resecting the roots approximately 3 mm apical to the fornix of the furcal roof [7]. They concluded that both the complexity of the FA, as well as plaque-retentive structures, could hamper adequate cleaning during periodontal treatment [7].

The distance between the cemento-enamel junction (CEJ) and the root separation area might also be critical [8, 9]. Unlike this study, most existing studies focus on root trunk (RT) measurements in extracted teeth [2, 4, 10,11,12]. Barboza et al. evaluated the mandibular molars and reported that the mean RT length was 3.07 mm in the buccal aspect and 3.54 mm in the lingual aspect [4]. Another study that examined the RT of mandibular first molars showed that RT length was 2.49 mm at the buccal sides and 3.18 mm at the lingual sides [2]. Roussa et al., in their study evaluating RT in maxillary molars, concluded that short or long RT may cause either early furcation involvement with the initial destruction of periodontal tissues, or difficulties in the early detection of furcation involvement [6]. Root proximity is another critical factor that can affect the development of periodontitis. In the previous research, if less than 1 mm of bone was present between two adjacent teeth, root proximity was found to be favorable for periodontitis [13,14,15]. A study by Vermylen et al. showed that patients with bilateral root proximity have a 3.6 times higher risk of develop periodontitis [14]. The risk was described as a relative risk, depending on the prevalence of the disease in their studied population [14]. The results of our previous study showed that the root proximity can be considered as a reliable risk indicator for anterior teeth [15]. Cone-beam computed tomography (CBCT) is considered to be a gold standard technique in diagnosis and is used as a reliable tool to assess morphological characteristics [16] and furcation involvement in molar teeth [17, 18]. It has been demonstrated that CBCT images enable accurate estimation in assessing the furcation involvement and root morphologies in maxillary molars [18]. Although there are advantages of the three-dimensional imaging method, it is not recommended as a routine diagnostic tool according to the ALARA (as low as reasonably achievable) principle.

Based on the results of our previous study and literature, we postulated that the CBCT images taken for other indications might also be used to analyze the anatomy of molar teeth. We aimed to assess the root proximity in molar teeth, the FA in the first root separation point using CBCT images and explore the association of the FA of maxillary and mandibular molar teeth and periodontal status.

Materials and methods

Patient selection

The dental records of patients referred between March 2017 and January 2022 to Istanbul Okan University’s Dentomaxillofacial Radiology and Periodontology Department for periodontal treatment, implant or impacted teeth surgery were examined. Patients were diagnosed by panoramic radiographs [staging: the radiographic bone loss around the root was more than 15% or extending to the middle or apical third of the root, teeth missing due to periodontal reasons, and complexity (furcation involvement class II or III) according to the 2017 World Workshop on the Classification of Periodontal and Peri‐Implant Diseases and Conditions [19]], and generalized stage II and III grade B periodontitis patients only were included in the periodontitis group (Fig. 1). The inclusion criteria were systemically healthy patients, 35–45 years old, and non-smokers. Because the prevalence and the rate of destruction increase with age, showing a steep increase between the 3rd and 4th decades of life, the age group of the patients was selected from 35 to 45 [20,21,22]. Patients were excluded if they were younger than 35 or older than 45 years of age or had systemic conditions that might affect periodontal status. Stage I periodontitis patients were excluded due to diagnostic difficulties, and stage IV periodontitis were also excluded as they exhibited multiple missing teeth. Additional exclusion criteria are listed in the flowchart below (Fig. 1). Molar teeth were excluded if they had root anomalies and no adjacent tooth, had endodontic treatment, or were present with prosthesis. The demographic, dental, and medical data were obtained from the Periodontology and Radiology archive database. The ethical approval was obtained for this retrospective study by the Ethical Committee of Istanbul Okan University (Approval Number: 161–7).

Fig. 1
figure 1

Flowchart of the patient and teeth selection

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CBCT analysis and measurements

All images were exported in Digital Imaging and Communications in Medicine (DICOM) format. CBCT scans (ProMax 3D Max, Planmeca, Helsinki, Finland) were taken using a standard 0.2 mm 3 voxel size at two fields of views (13 × 9 cm2 and 13 × 5.5 cm2). Standard exposure parameters were 96 kVp, 5.6 mA and 12 s. Linear measurements were made using the Romexis software v3.8.3.R (Planmeca, Helsinki, Finland). The images were oriented on multiplanar reconstructions (MPR). The occlusal plane was oriented parallel to the horizontal plane in the sagittal slices. Axial and coronal slices were also oriented parallel to the midsagittal plane. All measurements of CBCT were completed by one examiner (GAS). The measurements of FA in exported images were completed by another examiner (BA). For the intra-examiner reliability, the measurements of all 154 teeth were repeated by the same examiner after 1 week. Overall, the included teeth were measured twice. Intra-examiner reliability, as measured by values, intra-class correlation coefficients with 95% confidence interval for duplicate analysis 1 week apart were 0.92 and 0.94, respectively. The following measurements were performed on CBCT images.

Furcation area in the first root separation point

The axial slice in which the roots were separated was exported. The exported 2D images were then imported in Fiji software v1.52 (National Institutes of Health, Bethesda, MD, USA) and the measurements were completed. The axial slice of each corresponding molar tooth was magnified to 400% (Fig. 2a). To measure the FA on the axial slice, “Wand Tool” was selected, and the tolerance was set to 6 at “Legacy” mode (Fig. 2b). This option created a scout region of interest (ROI) based on the similar gray values around the roots. The scout ROI was added to the ROI manager. This step is repeated as long as the scout ROIs covered all the furcation areas between the roots. At the ROI manager window, “Show All” was selected to visualize the scout. Then, another ROI was drawn manually using “polygon selection” superimposed on the previous scout ROI (Fig. 2c). The area on the final ROI was measured in pixels and recorded in an excel sheet (Fig. 2d). Depending on the morphology of the root, if the molar teeth had more than one FA, each FA was measured separately, with the sum value then being designated the FA.

Fig. 2
figure 2

Demonstration of furcation area measurements: a The axial slice of the first maxillary molar as magnified at 400%. b The presentation of scout ROI using the “Wand Tool”. c Manual selection of the ROI using the polygon tool. d Resultant ROI

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Root proximity and distance between first root separation point and cemento–enamel junction

The CEJs of the molar teeth were identified on both mesial and distal aspects on the sagittal slices. Root proximities were measured for each molar on both mesial and distal sides between the outermost points of the adjacent teeth surfaces at the levels of CEJs (Fig. 3a) and root separation points (Fig. 3b). Another line perpendicular to the imaginary line of the CEJ was drawn from the CEJ to the root separation point on each molar tooth and recorded (Fig. 3c).

Fig. 3
figure 3

Demonstration of measurements: a Root proximity at cemento-enamel junction. b Root proximity at root separation point. c Distance between cemento-enamel junction and root separation point

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Furcation involvement grade and degree of bone resorption

Furcation grades were determined from axial and sagittal slices according to Glickman’s horizontal classification [23], and the Tarnow and Fletcher classification [24] for the vertical dimension (Fig. 4a, b).

Fig. 4
figure 4

a The horizontal evaluation of furcation grade. b The vertical evaluation of furcation grade and the determination of bone resorption (green line)/root length (blue line). The yellow dashed line shows the level of the alveolar bone 2 mm below CEJ

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For the measurement of root length of the root with the highest bone loss, the CEJ was marked and the distance from the CEJ to the tip of the apex was measured. The bone resorption distance was determined by measuring the distance from the CEJ to the most apical tip of the bone defect (Fig. 4b). Since the bone is approximately 2 mm apical to the CEJ [25], bone resorption was determined by subtracting 2 mm from this distance. Then, the degree of bone resorption was calculated by as the ratio of the resorption and the root length.

Statistical analysis

Statistical analysis was carried out using SPSS v.23 software (IBM Corp., New York), and Stata 16 statistical software (StataCorp LLC, Texas). The power analysis demonstrated a sample size of ten teeth for each tooth group would ensure 80% power to detect the association between periodontitis and morphologic features with a significance level of 0.05. While the primary outcome of the study was considered the FA, the distance between the first root separation point and cemento-enamel junction—as well as root proximity—were the secondary outcomes. Variables were tested for normal distribution using the Kolmogorov–Smirnov and Shapiro–Wilk tests. Normally distributed data were compared with the Student’s t test, and data showing non-normal distribution were compared with Mann–Whitney U test. Pearson and Spearman correlation tests was used to assess correlations among variables. Receiver operation curve (ROC) analysis used to evaluate diagnostic efficacy of FA and the area under the curve (Az) with standard error and 95% confidence intervals were calculated. Youden's J statistics was used to determine the decision threshold of the FA in diagnosing periodontitis. Sensitivity and specificity values were calculated for proposed cut-off value. Logistic regression was used in a multivariate model to assess the risk affecting periodontitis. The Hosmer–Lemeshow goodness-of-fit test was used to test the fit of the logistic model. Frequencies (mean ± standard deviation) and percentages were expressed for categorical data. The significance level was set at p < 0.05.

Results

Demographic findings

A total of 2514 screened files were retrieved. 2095 images were excluded according to the exclusion criteria. Demographic data of the patients are presented in Table 1. The mean ages of periodontitis patients and the control group patients were 39.57 and 38.81 years, respectively. No statistically significant differences in age and gender between the groups were determined (p > 0.05). CBCT images of 66 patients with 264 molar teeth were grouped as the periodontitis group and control group based on the 2018 classification. Among the 264 molar teeth, 154 teeth were in the periodontitis group, and 110 teeth were in the control group. In the periodontitis group, a total of 75 and 79 teeth were included from patients with periodontitis stage II and III (grade B), respectively. No significant difference in tooth distribution between stage II and III periodontitis was observed (p > 0.05). The descriptive characteristics of the molar teeth are shown in Table 2.

Table 1 Demographic characteristics of participants
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Table 2 Descriptive data of the teeth
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Radiographic findings

Measurements of FA in the root separation point, root proximity, and the distance between CEJ and RSP were summarized according to the molar teeth groups in Tables 3 and 4. All molars had significantly less FA in periodontitis group than controls (p < 0.01), as shown in Table 3. FA of the molars in the periodontitis group were 209.05 ± 92.9 and in the controls were 306.53 ± 117.98 px2 (p < 0.001). Additionally, the difference in FA between the first and second molars was significant in controls (p = 0.013 for maxillary molars, p = 0.002 for mandibular molars). For the periodontitis group, the difference in FA between mandibular molars was significant (p = 0.006). The FA values of the molars were significantly lower in the periodontitis group than in the control group. The difference in FA values of the first and second maxillary molars in periodontitis group was not significant (p = 0.299). It was found that the risk of periodontitis increases 1.011 (1/0.986) times as the total FA decreases (p < 0.001) in logistic regression analysis (Table 4). When analyzing all molar groups, a statistically significant cut-off value of FA was found as 362.5 px2 with a sensitivity of 95.5% and specificity of 30%. However, a similarly significant difference was not observed between these groups in the distance of CEJ-RSP in any of molars (p = 0.147) (Table 3). The measurements of molars in the periodontitis group and distribution of furcation involvement grades are summarized in Table 5, and the correlation between FA and bone resorption rate and furcation grade is summarized in Table 6. A positive, strong, and statistically significant relationship was found between the furcation grade and the bone resorption rate (p < 0.001). There was a negative and statistically significant relationship between FA and bone resorption rate and furcation grade (p < 0.001).

Table 3 Comparison of the parameters between periodontitis and control group according to molar teeth groups
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Table 4 Logistic regression analysis
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Table 5 Descriptive data for periodontitis group of molars
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Table 6 Correlation between bone resorption rate and furcation area, root proximity, and furcation grade in periodontitis group of molars
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According to the regression analysis, the maxillary molar increases the risk of periodontitis 1.693 times compared to mandibular molars (95%CI: 0.823–3.476). However, the contribution of this variable to the model was not found to be statistically significant (p = 0.152) (Table 4). The measurements of root proximity in CEJ and in RSP are summarized in Table 3. When assessing the root proximity between molar teeth, maxillary molars showed significantly higher root proximity in CEJs than mandibular molars in both periodontitis and control groups (p < 0.005). The distance between root proximity in CEJ and in RSP was significantly higher in the control group than in the periodontitis group for maxillary molars and the mandibular molars (Table 3). According to logistic regression analysis, for each one unit decrease in root proximity in CEJ value, there was 2.4 (1/0.417) times higher risk of being periodontitis (Table 4).

Discussion

In this investigation, CBCT-generated data of root morphology, FA and root proximity in molar teeth were analyzed according to periodontitis status. The study demonstrated for the first time that the FAs in all molar groups were smaller in all periodontitis patients. When the degree of bone resorption of molar teeth was analyzed, it was found that as the furcation area decreased, the furcation invasion grade and bone resorption increased statistically. Assessing with the regression analysis, an FA decrease by one unit leads to a periodontitis risk increase by 1011 times. The cut-off value of FA was 362.5 px2. Narrower furcation area than 362.5 px2 was associated with the bone resorption and could be considered as a potential risk indicator for periodontitis. The FAs in similar RSPs were narrower in periodontitis patients. It was considered that inter-radicular root divergence might be lower in the periodontitis patients we investigated, and that narrower FA might provide less bone and attachment support against periodontal disease [26]. Paolantonio et al. evaluated the root divergence of mandibular and maxillary molars. They found that first molars in both jaws had higher inter-radicular angles as compared to secondary molars. Their inter-radicular angle results were correlated with the FA results in this present study [7]. According to previous studies, it is known that plaque control is difficult in molars and furcation areas [4, 6, 27]. It was thought that the anatomy of the furcation area may favor the progression of periodontal disease by complicating the removal of the biofilm during oral hygiene procedures. Waerhaug et al. stated that large accumulations of subgingival plaque were observed in the depth of pockets in furcation area despite there were plaque-free in the gingival margin and just below the gingiva 0.5–2.5 mm [27].

Perminio et al. found a negative correlation between RT length and prefurcation concavity area in their micro-tomographic analysis study [2]. They investigated the RT and prefurcation concavity area of first mandibular molars and concluded that prefurcation area dimensions might represent a greater risk factor for the early development of furcation lesions. As they only measured the concavity on the prefurcation surface of the teeth—not the prefurcation cross-sectional area—the present results may differ from their study.

In the present study, the results showed no statistically significant difference between the distance of RSPs and CEJs of the molars in periodontitis patients. The mean distance between the CEJ and RSP in the first mandibular molar was 3.34 mm. In previous studies examining the length of the root trunk of extracted mandibular first molars, Gher et al. reported the lengths to be 3 mm and 4 mm, buccal and lingual, respectively [28], while Roussa et al. reported that these values were 2.8 mm buccal and 3.5 mm lingual [6]. Likewise, in another study, it was observed that the root trunk length of 96 extracted mandibular first molars was 3.07 and 3.54 mm in buccal and lingual measurements, respectively [4]. When the first and second maxillary molars were examined in this study, the mean distance between the CEJ and RSP of the first and second maxillary molars was found to be 4.16 mm and 4.37 mm, respectively. Paolantonio et al. reported that the root trunk length of extracted maxillary molars was 3.8 mm and 4.4 mm in the first and second molars, respectively [7]. None of these studies evaluated root trunk length in the context of periodontitis.

Although there is no major difference in the results, the difference between the current results and previous studies may be due to the evaluation method. In previous studies, measurements were made on extracted teeth. In this study, the distance between CEJ and RSP was measured on sagittal slices in CBCT. Because the measurements were made at the midline of the teeth in the bucco-lingual direction, an average value might have been obtained. In addition, since the positions of the teeth in the jaw differ in the bucco-lingual and mesio-distal directions, the first separation point of the roots on CBCT may differ from the root separation point observed after the teeth are extracted. Baima et al. reported that the furcation is progressively more apically positioned as the tooth is more distally located in the dental arch [12].

Longitudinal studies show that maxillary molars have a higher incidence of periodontal breakdown and are therefore at higher risk of developing periodontal bone loss [29, 30]. Chambrone et al. concluded that more maxillary molars were lost during periodontal maintenance, but such loss was probably associated with anatomical features (i.e., FA) and disease progression [31, 32]. Our results show that root proximity of maxillary and mandibular molars is a risk for periodontitis. Additionally, maxillary molars have a significantly lower interdental distance than mandibular molars in CEJs, and this distance was 1.21 mm and 1.65 mm, in the periodontitis and control groups in maxillary molars, respectively. In parallel to our results, Vermylen et al. concluded that root proximity must be taken into consideration as a risk marker for periodontal disease [14]. They showed that 68% of all the root proximities are in the maxillary molars [14]. The authors described root proximity as the occurrence of 0.8 mm or less bone or interdental tissue being present between the two involved roots. Aside from the proximity of some maxillary molars in periodontitis group being less than 0.8 mm, our mean results did not exceed this critical threshold value.

As the current study is cross-sectional and retrospective in nature, not evaluating long-term periodontal status or comparing the clinical measurements and periodontal indices of the teeth may be regarded as limitations of this study. On the other hand, the careful selection of patients with detailed exclusion criteria, as well as homogeneous groups in age and gender, may be considered strengths of our study.

The current results indicate that there might be an association between FA and periodontitis prevalence and that this could be considered as a reliable risk indicator for bone resorption in molar teeth. Root proximity of molars may not be a risk factor but can play a role during disease progression. Acquiring detailed information regarding the FA and anatomy of molars using CBCT images may be useful in the management of furcation involvement of the molars during periodontal treatment. On the other hand, calculating FA on CBCT for every patient may be time-consuming and impractical in clinical applications. In the future, integrating the FA and root proximity markers into the clinical decision support systems by artificial intelligence-driven software may facilitate risk evaluation. To explain the role of furcation area and root proximity in the progression of periodontitis, further studies are needed in which more detailed examinations are made using CBCT images and evaluated together with clinical data.