A retrospective study on molar furcation assessment via clinical detection, intraoral radiography and cone beam computed tomography

A retrospective study on molar furcation assessment via clinical detection, intraoral radiography... Background: Accurate determination of bone loss at the molar furcation region by clinical detection and intraoral radiograph is challenging in many instances. Cone beam computed tomography (CBCT) is expected to open a new horizon in periodontal assessment. The purpose of this study was to compare and correlate accuracy of molar furcation assessment via clinical detection, intraoral radiography and CBCT images. Methods: Eighty-three patients with chronic periodontitis who had existing CBCT scans were included. Furcation involvement was assessed on maxillary and mandibular first molars. Periodontal charts (modified Glickman’s classification), intraoral (periapical and/or bitewing) radiographs (recorded as presence or absence) and axial CBCT reconstructions were used to evaluate furcation involvement on buccal and palatal/lingual sites. The correlation of furcation assessment by the three methods was evaluated by Pearson analysis. Results: There were significant correlations (p < 0.05) between clinical detection and intraoral radiography, clinical detection and CBCT, as well as intraoral radiography and CBCT at all the measured sites (r values range between 0.230 to 0.644). CBCT generally exhibited higher correlation with clinical detection relative to intraoral radiography, especially at distal palatal side of maxillary first molar (p < 0.05). In addition, CBCT provided more accurate assessment, with bone loss measurement up to 2 decimals in millimeters, whereas clinical detection had 3 classes and the intraoral radiographs usually only detected the presence of furcation involvement in Glickman Class 2 and 3. Conclusions: This study validates that CBCT is a valuable tool in molar furcation assessment in addition to clinical detection and intraoral radiography. Keywords: Furcation involvement, Clinical detection, Intraoral radiography, CBCT Background plan [5] and unanticipated treatment costs (financially Furcation involvement (FI) refers to the condition when and temporally) [6]. Therefore, management of FI has periodontal disease has caused bone resorption into the presented as one of the greatest challenges to the suc- bifurcation or trifurcation of a multi-rooted tooth [1]. cess of periodontal therapy [7]. Dentists commonly encounter the difficulty of accurately Traditionally, FI is assessed with a combination of assessing molars with FI, due to limited physical access, clinical detection and intraoral radiographs [8]. Clinic- morphological variations and measurement errors [2–4]. ally, FI is evaluated with a Nabers probe, and categorized Any discrepancies between pre-and intra-surgical find- according to Glickman’sorHamp’s classification system ings of FI may lead to alterations of surgical treatment based on horizontal bone loss at the furcation area [9, 10]. However, the accuracy of clinical detection largely depends on operator technique, and many times, the measurement * Correspondence: Wenjian.Zhang@uth.tmc.edu is reflective of penetration depth into the inflamed connect- Department of Diagnostic & Biomedical Sciences, University of Texas School of Dentistry at Houston, 7500 Cambridge Street, Houston, TX 77054, USA ive tissue, instead of the actual depth of the inter-radicular Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Zhang et al. BMC Oral Health (2018) 18:75 Page 2 of 7 bony defect [11]. In addition, factors such as tooth position, NC, USA). The unit was operated at 70 peak kilovolt inclination, root morphology, length of root trunk, (kVp), 7 mA (mA), and an exposure time corresponding degree of root separation and configuration of re- to the exposed area. All the radiographs were taken with sidual inter-radicular bone, all affect accuracy of clin- XCP receptor-holding devices (Dentsply Rinn, Elgin, IL, ical furcation assessment [12, 13]. Periapical (PA) or USA) and the paralleling technique. Photostimulable bitewing (BW) radiographs are commonly used intraoral phosphor (PSP) plates (Air Techniques, Melville, NY, projections to supplement clinical detection for furcation USA) were utilized as the receptor, and were scanned assessment [8, 14]. These 2D imaging are generally con- with the Scan-X Intraoral scanner (Air Techniques) after sidered to have low sensitivity but high specificity for fur- exposure. The images were stored in the EHR of the cation detection, mainly due to inherent shortcomings of School of Dentistry, displayed on a 19-in. flat panel screen 2D projections, such as superimposition and angulation (HP Development Company, Palo Alto, CA, USA) with a problems [15]. Detectability of early FI by intraoral radio- 1920 X 1080 pixel resolution, and observed under a dimly graphs is especially limited and inconsistent [16]. lit environment. Cone beam computed tomography (CBCT) is capable of generating accurate and reliable submillimeter-resolution CBCT imaging acquisition images in all spatial dimensions, with cost and absorbed All of the CBCT scans were taken at the Imaging Clinic of doses much lower than conventional CT [17, 18]. The University of Texas School of Dentistry at Houston. The applications of CBCT in dentistry are increasing rapidly, included scans covered maxillary and mandibular arches including in periodontology [19, 20]. CBCT is expected to with a field of view (FOV) of 150 × 90 mm . The scans reveal marginal bone contours as well as infrabony and fur- were acquired at 90 kVp, 10 mA, 16 s and a 0.2 mm voxel cation defects [21], therefore plays a role in the assessment size with a Kodak 9500 unit (Carestream Health, Inc., and treatment planning of molars with FI. Currently, Rochester, NY, USA). CBCT images were reconstructed there are limited studies comparing diagnostic accuracy of with Anatomage Invivo 5 software (Anatomage Inc., San FI by clinical detection, intraoral radiography and CBCT Jose, CA, USA) at 1 mm thickness. All images were viewed [12, 22, 23]. The aim of the present study was to compare on the same monitor and environment as the intraoral and correlate assessment of molar FI via these three radiographs. methods, to help further develop evidence on the applic- ability of CBCT in molar FI assessment. Comprehensive periodontal evaluation Clinical periodontal assessment Methods All subjects had comprehensive periodontal examination Subjects by the pre-doctoral dental students under the supervision An Institutional Review Board (IRB) approval was granted and approval of a periodontal faculty. The evaluation in- prior to the start of the study (HSC-DB-17-0370). The cluded an assessment of molar furcation involvement ac- patients who visited the University of Texas School of cording to modified Glickman’s classification [10](Fig. 1). Dentistry at Houston dental clinic from 2012 to 2016 were Briefly, this classification was defined as: Class I, incipient retrospectively screened according to the selection criteria. or early stage of furcation involvement, bone destruction The inclusion criteria were: 1) subject was diagnosed as is less than 2 mm into the furca; Class II, horizontal bone having generalized moderate or severe chronic periodon- destruction extending deeper than 2 mm but less than titis; 2) subject had comprehensive periodontal examination 6 mm into the furca; Class III, horizontal bone destruc- andinformation hadbeenstoredinthe school’sElectronic tions communicate between furcae of the tooth, and result Health Record (EHR); 3) subject had diagnostic quality in a through-and-through tunnel. periapical and/or bitewing radiographs covering posterior dentition; 4) subject had diagnostic quality CBCT scan with Intraoral radiographic assessment coverage of entire maxilla and mandible. Majority of the First molar furcation status was evaluated on molar PA patients had CBCT scans for implant treatment planning and/or BW radiographs. Presence of triangular radio- purpose, and the time interval between periodontal clinical lucency at the furcation area, and/or alveolar bone level exam and CBCT scan was less than 3 months. All of the was observed below furcation were radiographic signs patients who met the inclusion criteria were included in the for FI. FI was recorded as presence or absence based on study, and their first molars of maxilla and mandible bilat- the intraoral radiographs (Fig. 2). erally were assessed according to the following methods. CBCT imaging measurements Intraoral radiographic acquisition First molar furcation assessment was conducted mainly All the intraoral radiographs were acquired with Focus on reconstructed CBCT sagittal and axial views. Pres- wall-mounted unit (Instrumentarium Dental, Charlotte, ence of FI was demonstrated as loss of trabecular bone Zhang et al. BMC Oral Health (2018) 18:75 Page 3 of 7 Fig. 1 Periodontal chart demonstrates classification of molar furcation involvement at the furcation region on both axial and sagittal view. reanalyzed in 7 months to evaluate intra-rater reliability The depth of FI was measured on axial view where the and reproducibility. slice showed the greatest amount of bone loss. On this slice, a line was drawn tangentially to the adjacent root Statistical analysis surfaces. The distance from this line to the deepest point Spearman’s correlation analysis was used to determine of bone loss was designated as the amount of furcation the correlations between clinical detection and intraoral bone loss. If applicable, buccal and/or lingual furcation radiography, clinical detection and CBCT, as well as bone loss was measured for mandibular first molar, and intraoral radiography and CBCT at all the measured buccal, mesial palatal, and distal palatal furcation bone sites. The difference in the correlation coefficients was loss were measured for maxillary first molars (Fig. 3). analyzed using Steiger’s Z-test. Intra-class correlation All the data were analyzed by one of the co-authors coefficient (ICC) was calculated to assess intra-rater KF, who was a first-year dental student and received reliability and reproducibility. The statistical difference adequate training on molar furcation assessment via was set at p < 0.05. The statistical analysis were run with intraoral radiographs and CBCT scans. The data were SPSS program (version 24, IBM, Armonk, NY, USA). Fig. 2 Intraoral radiographs demonstrate molar furcation status. a presence of furcation involvement. b absence of furcation involvement Zhang et al. BMC Oral Health (2018) 18:75 Page 4 of 7 Fig. 3 Measurement of molar furcation involvement on CBCT scans. a a schematic diagram illustrates measurement of furcation bone loss of a maxillary first molar. Dotted line represents tangent line connecting two adjacent root surfaces. Arrows represent distances from the middle of tangent line to the deepest point of bone loss at the different surfaces. Red, green, and blue arrows denote furcation bone loss at buccal, mesial palatal, and distal palatal surface of the molar, respectively. MB, mesial buccal root; DB, distal buccal root; and P, palatal root. b a representative CBCT axial view demonstrates measurements of furcation bone loss of a maxillary first molar. c a schematic diagram illustrates measurement of furcation bone loss of a mandibular first molar. Dotted line represents tangent line connecting buccal or lingual surfaces of the two roots, respectively. Arrows represent distances from the middle of tangent line to the deepest point of bone loss at the different surfaces. Red and green arrows denote furcation bone loss at buccal and lingual surface of the molar, respectively. M, mesial root; and D, distal root. d a representative CBCT axial view demonstrates measurements of furcation bone loss of a mandibular first molar Results Based on a previous study conducted by Qiao et al. [13] who compared molar furcation assessment between clin- ical probing and CBCT, a power analysis was performed which demonstrated that a sample size of 51 subjects would achieve 80% power to detect the association be- Table 1 First molar furcation involvement assessed by periodontal probing tween these two evaluation methods on a significance level of 0.05. To ensure adequate sample size, a total of Modified Maxillary first molar Mandibular first molar Glickman 83 patients were included in the study. Among these pa- B MP DP Average B L Average classification tients, 41 were males, 42 were females, and an age range Not present 49.1% 78.4% 83.6% 70.4% 60.8% 53.9% 57.4% of 31–86 with a mean age of 59.03 ± 13.08 years old. Class I 34.5% 7.8% 5.2% 15.8% 18.6% 27.5% 23.1% First molar FI assessed by clinical detection, BW/PA Class II 9.5% 6.9% 6.0% 7.5% 13.7% 11.8% 12.8% and CBCT were illustrated in Tables 1, 2 and 3, respect- ively. For maxillary first molar B, MP and DP FI, clinical Class III 6.9% 6.9% 5.2% 6.3% 6.9% 5.9% 6.4% detection demonstrated a mean modified Glickman’s Total 100% 100% 100% 100% 100% 100% 100% classification of 0.75 ± 0.08, 0.41 ± 0.08, 0.33 ± 0.07, re- Data are presented as percentage of assayed surfaces without or with furcation spectively, and CBCT assessment revealed a mean 1. involvement of corresponding category based on periodontal charting Abbreviations: B buccal, MP mesial palatal, DP distal palatal, L lingual 55 ± 0.22, 0.58 ± 0.05, 0.67 ± 0.12 mm bone loss, respectively. Modified Glickman classification: Class I, incipient or early stage of furcation For mandibular first molar B and L FI, clinical detection involvement, bone destruction is less than 2 mm into the furca; Class II, horizontal bone destruction extending deeper than 2 mm but less than 6 mm demonstrated a mean modified Glickman’s classification of into the furca; Class III, horizontal bone destructions communicate between 0.66 ± 0.10 and 0.69 ± 0.09, respectively, and CBCT assess- furcae of the tooth, and result in a through-and-through tunnel ment revealed a mean 1.52 ± 0.19 and 1.15 ± 0.18 mm bone Not present: no furcation involvement Zhang et al. BMC Oral Health (2018) 18:75 Page 5 of 7 Table 2 First molar furcation involvement assessed by periapical Table 4 Cross tabulation of CBCT with periodontal probing for or bitewing radiographs evaluation of furcation involvement for maxillary and mandibular first molars Radiographic assessment Maxillary Mandibular first molar first molar Count Periodontal probing Total Absence of furcation involvement 71.8% 66.0% 01 2 3 Presence of furcation involvement 28.2% 34% CBCT (mm) 0.0 213 36 10 3 262 Total 100% 100% 0.1–2.0 40 24 7 0 71 Data are presented as percentage of assayed first molars without or with 2.1–6.0 38 22 13 6 79 furcation involvement based on radiographic assessment > 6.0 1 2 3 5 11 Total 292 84 33 14 423 loss, respectively (data were presented as mean ± SD). All of the three evaluation methods demonstrated more frequent FI of mandibular first molars relative to maxillary counter- which demonstrated great reliability and repeatability of part. Of maxillary first molars, both clinical detection and the evaluator. CBCT revealed that buccal surface was more vulnerable for FI compared to palatal side. Discussion Comparison of first molar FI assessment between Our results demonstrated that all three FI assessment CBCT and clinical detection showed that, when CBCT methods had significant correlations among each other. demonstrated no furcation involvement, 18.7% of these CBCT had stronger correlation to clinical detection than cases were documented as FI on clinical detection. On PA/BW, especially on distal palatal side of maxillary first the contrary, of the 26.7% cases identified as having 0.1– molar. The results validate applicability of CBCT in FI 2.0 mm or 2.1–6.0 mm bone loss on CBCT, clinical de- assessment. Although all of the included patients had tection showed no FI (Table 4). For comparison between diagnosis of generalized moderate or severe chronic intraoral radiographic evaluation and clinical detection, periodontitis, more than a half of them were not found there were situations when no FI was detected on to have FI based on the three evaluation methods. intraoral radiographs, 25.6% of these cases were demon- When CBCT showed no furcation involvement, clin- strated to have Class I-III FI by clinical detection. In ical detection identified 18.7% of cases with FI, indicat- addition, for 18.2% cases identified as FI on radiographs, ing over-detection by clinical measurement. On the clinical detection failed to detect any bone loss (Table 5). contrary, of the 26.7% cases demonstrated bone loss on Spearman’s correlation and Steiger’s Z-test analysis CBCT, clinical detection showed no FI, suggesting under- demonstrated that clinical detection, BW/PA and CBCT detection by clinical detection. This was consistent with were significantly correlated with each other in the as- what was reported by Darby [12] and Walter [23], who sessment of first molar FI, with r values ranged between also found over- and under-estimation of FI by clinical 0.230 to 0.644 (P < 0.05, Table 6). Compared with BW/ probing relative to CBCT analysis. It is speculated that PA, CBCT appeared to have higher correlation coeffi- probing angulation and force, soft tissue inflammation, cients with clinical detection, especially at distal palatal and inter-radicular bone and root morphology, all contrib- side of maxillary first molar, which reached statistically ute to variations of clinical detection. significant difference (p < 0.05, Table 6). Between the two Between intraoral radiographic examination and clin- sets of measurements by the same rater, the ICC was 0. ical detection, there were situations when no FI was 903, with 95% confidence interval of (0.858, 0.934), identified on intraoral radiographs, about one quarter of these cases were demonstrated having FI by clinical de- tection. In addition, for 18.2% cases identified as FI on Table 3 First molar furcation involvement measured by CBCT radiographs, probing failed to detect any bone loss. This Depth of Maxillary first molar Mandibular first molar observation confirmed the necessity of supplementing furcation B MP DP Average B L Average involvement (mm) Table 5 Cross tabulation of intraoral radiograph with periodontal 0.0 46.7% 81.5% 73.9% 67.4 45.9% 54.1% 50.0% probing for evaluation of furcation involvement for maxillary and mandibular first molars 0.1–2.0 21.7% 5.4% 16.3% 14.5 15.3% 25.9% 20.6% Count Periodontal probing Total 2.1–6.0 25.0% 13.0% 6.5% 14.8 36.5% 17.6% 27.1% 0 123 > 6.0 6.5% 0.0% 3.3% 3.3 2.4% 2.4% 2.4% Intraoral radiograph 0 (absence) 258 75 13 2 352 Total 100% 100% 100% 100% 100% 100% 100% 1 (presence) 58 17 39 28 142 Data are presented as percentage of assayed surfaces without or with furcation involvement of corresponding category based on CBCT assessment Total 316 92 52 34 494 Abbreviations: B buccal, MP mesial palatal, DP distal palatal, L lingual Zhang et al. BMC Oral Health (2018) 18:75 Page 6 of 7 Table 6 Correlation coefficients of periodontal probing with periodontal probing and intraoral radiographs should be CBCT or BW/PA in assessment of furcation involvement for used as routine examinations for detection of FI. For com- maxillary and mandibular first molars plicated cases when routine exams fail to provide adequate Periodontal charting (Modified Glickman) CBCT BW/PA information for diagnosis and/or treatment planning, a a Maxillary buccal 0.599 0.579 CBCT may be attempted with the smallest field of view a a possible and optimal exposure settings. Maxillary mesial palatal 0.591 0.499 a,c a,c There were limitations for the study. It was a retrospect- Maxillary distal palatal 0.644 0.424 ive investigation, and the clinical detection was performed a a Mandibular buccal 0.372 0.362 by different dental students under the supervision of b b Mandibular lingual 0.264 0.230 board-certified periodontist, and the results were con- Abbreviations: CBCT cone beam computed tomography, BW/PA firmed by the supervising faculty before being entering in bitewing/periapical radiographs the EHR. Still, inter-operator variations could contribute Correlation is significant at p < 0.01, between CBCT and periodontal charting, or between BW/PA and periodontal charting to inconsistence in the clinical detection. Also, in the Correlation is significant at p < 0.05, between CBCT and periodontal charting, present study, a relative old model of CBCT unit, Kodak or between BW/PA and periodontal charting CBCT demonstrated significantly stronger correlation (p < 0.05) with 9500 was used, since this was the only CBCT unit in the periodontal charting relative to BW/PA at assessment of distal palatal side of Imaging Clinic of the school. This unit had a smallest maxillary first molars voxel size of 200 μm. Compared to newer CBCT units clinical detection with intraoral radiographs for the diagno- with much smaller voxel size, such as 80 μmfor Accui- sis of FI, which is reflective of the consensus in the litera- tomo [33], the much larger voxel size of current unit had ture [8, 14]. The inconsistency between these two methods limited spatial resolution, therefore, could limit the accur- could be due to measurement errors from either or both acy in the assessment of FI. In addition, current study only detecting techniques. Anatomic complexity, such as super- measured horizontal bone loss at the furcation area on imposition of palatal root at the furcation region may con- CBCT scan, in order to correlate with clinical detection. tribute to under-diagnosis of FI for maxillary molars on Modified Glickman Classification was utilized in clinical intraoral radiographs [5, 24], and sinus tract extending into detection, which only recorded horizontal furcation in- furcation due to intrapulpal infection may lead to over- volvement of the molars. Future study could consider in- diagnosis of FI on intraoral radiographs [25], respectively. corporating vertical bone loss measurement on CBCT, to The current study identified that mandibular first mo- gain better appreciation on furcation status. Intra-surgical lars had more FI than maxillary first molars. In a study FI assessment (gold standard) could be implemented, if conducted in a Swede population, Svärdström [26] found possible, to further evaluate the accuracy of CBCT in the that the prevalence of furcation involved molars was diagnosis of FI. higher in the maxilla than in the mandible, based on clinical detection and intraoral radiographs. Hou et al. Conclusions [27] concluded that the highest prevalence of FI was in CBCT has been validated as a valuable supplemental tool the mandibular first molar in a Japanese population for assessment of molar FI in addition to periodontal based on clinical detection. It appears that geographical probing and intraoral radiographic examinations. locations, racial origins and evaluation modalities are among the factors contributing to variations of preva- Abbreviations BW: Bitewing; CBCT: Cone beam computed tomography; EHR: Electronic lence for molars with FI. Current study also found that Health Record; FI: Furcation involvement; FOV: Field of view; IRB: Institutional FI was more frequently associated with and more severe Review Board; kVp: Kilovolt; mA: Milliampere; PA: Periapical; at buccal side of maxillary first molars relative to palatal PSP: Photostimulable phosphor side, similarly as reported by Porciuncula [28]. Funding Although considered a valuable addition in molar furca- This study was partially supported by the Research Office, University of Texas tion assessment, CBCT is not without its shortcomings. School of Dentistry at Houston. Scatter, partial volume averaging and beam hardening arti- facts could compromise its diagnostic quality, especially Availability of data and materials The datasets generated and/or analysed during the current study are not for patients with heavy metallic restorations, multiple end- publicly available, in order to protect participant anonymity. However, these odontic treatment, orthodontic appliances, or implant data are available from the corresponding author on reasonable request. prosthesis [29–31]. In addition, detectability of FI by CBCT depends on how sensitive it is to reveal bone loss Authors’ contributions at furcation area. Generally, demineralization may not be WZ conceived the ideas, designed the experiments, and composed the manuscript. KF did all the measurements and performed initial data analysis. evident radiographically until it reaches approximately BW refined the ideas, performed in-depth data analysis and interpretations, 30–40% [32]. This makes it challenge to detect and initiate and critically revised the manuscript. All authors read and approved the final early intervention for incipient FI of molars. In general, manuscript. Zhang et al. BMC Oral Health (2018) 18:75 Page 7 of 7 Ethics approval and consent to participate 18. Aljehani YA. 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Clin Oral Implants Res. 2001;12(5):539–42. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png BMC Oral Health Springer Journals

A retrospective study on molar furcation assessment via clinical detection, intraoral radiography and cone beam computed tomography

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Abstract

Background: Accurate determination of bone loss at the molar furcation region by clinical detection and intraoral radiograph is challenging in many instances. Cone beam computed tomography (CBCT) is expected to open a new horizon in periodontal assessment. The purpose of this study was to compare and correlate accuracy of molar furcation assessment via clinical detection, intraoral radiography and CBCT images. Methods: Eighty-three patients with chronic periodontitis who had existing CBCT scans were included. Furcation involvement was assessed on maxillary and mandibular first molars. Periodontal charts (modified Glickman’s classification), intraoral (periapical and/or bitewing) radiographs (recorded as presence or absence) and axial CBCT reconstructions were used to evaluate furcation involvement on buccal and palatal/lingual sites. The correlation of furcation assessment by the three methods was evaluated by Pearson analysis. Results: There were significant correlations (p < 0.05) between clinical detection and intraoral radiography, clinical detection and CBCT, as well as intraoral radiography and CBCT at all the measured sites (r values range between 0.230 to 0.644). CBCT generally exhibited higher correlation with clinical detection relative to intraoral radiography, especially at distal palatal side of maxillary first molar (p < 0.05). In addition, CBCT provided more accurate assessment, with bone loss measurement up to 2 decimals in millimeters, whereas clinical detection had 3 classes and the intraoral radiographs usually only detected the presence of furcation involvement in Glickman Class 2 and 3. Conclusions: This study validates that CBCT is a valuable tool in molar furcation assessment in addition to clinical detection and intraoral radiography. Keywords: Furcation involvement, Clinical detection, Intraoral radiography, CBCT Background plan [5] and unanticipated treatment costs (financially Furcation involvement (FI) refers to the condition when and temporally) [6]. Therefore, management of FI has periodontal disease has caused bone resorption into the presented as one of the greatest challenges to the suc- bifurcation or trifurcation of a multi-rooted tooth [1]. cess of periodontal therapy [7]. Dentists commonly encounter the difficulty of accurately Traditionally, FI is assessed with a combination of assessing molars with FI, due to limited physical access, clinical detection and intraoral radiographs [8]. Clinic- morphological variations and measurement errors [2–4]. ally, FI is evaluated with a Nabers probe, and categorized Any discrepancies between pre-and intra-surgical find- according to Glickman’sorHamp’s classification system ings of FI may lead to alterations of surgical treatment based on horizontal bone loss at the furcation area [9, 10]. However, the accuracy of clinical detection largely depends on operator technique, and many times, the measurement * Correspondence: Wenjian.Zhang@uth.tmc.edu is reflective of penetration depth into the inflamed connect- Department of Diagnostic & Biomedical Sciences, University of Texas School of Dentistry at Houston, 7500 Cambridge Street, Houston, TX 77054, USA ive tissue, instead of the actual depth of the inter-radicular Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Zhang et al. BMC Oral Health (2018) 18:75 Page 2 of 7 bony defect [11]. In addition, factors such as tooth position, NC, USA). The unit was operated at 70 peak kilovolt inclination, root morphology, length of root trunk, (kVp), 7 mA (mA), and an exposure time corresponding degree of root separation and configuration of re- to the exposed area. All the radiographs were taken with sidual inter-radicular bone, all affect accuracy of clin- XCP receptor-holding devices (Dentsply Rinn, Elgin, IL, ical furcation assessment [12, 13]. Periapical (PA) or USA) and the paralleling technique. Photostimulable bitewing (BW) radiographs are commonly used intraoral phosphor (PSP) plates (Air Techniques, Melville, NY, projections to supplement clinical detection for furcation USA) were utilized as the receptor, and were scanned assessment [8, 14]. These 2D imaging are generally con- with the Scan-X Intraoral scanner (Air Techniques) after sidered to have low sensitivity but high specificity for fur- exposure. The images were stored in the EHR of the cation detection, mainly due to inherent shortcomings of School of Dentistry, displayed on a 19-in. flat panel screen 2D projections, such as superimposition and angulation (HP Development Company, Palo Alto, CA, USA) with a problems [15]. Detectability of early FI by intraoral radio- 1920 X 1080 pixel resolution, and observed under a dimly graphs is especially limited and inconsistent [16]. lit environment. Cone beam computed tomography (CBCT) is capable of generating accurate and reliable submillimeter-resolution CBCT imaging acquisition images in all spatial dimensions, with cost and absorbed All of the CBCT scans were taken at the Imaging Clinic of doses much lower than conventional CT [17, 18]. The University of Texas School of Dentistry at Houston. The applications of CBCT in dentistry are increasing rapidly, included scans covered maxillary and mandibular arches including in periodontology [19, 20]. CBCT is expected to with a field of view (FOV) of 150 × 90 mm . The scans reveal marginal bone contours as well as infrabony and fur- were acquired at 90 kVp, 10 mA, 16 s and a 0.2 mm voxel cation defects [21], therefore plays a role in the assessment size with a Kodak 9500 unit (Carestream Health, Inc., and treatment planning of molars with FI. Currently, Rochester, NY, USA). CBCT images were reconstructed there are limited studies comparing diagnostic accuracy of with Anatomage Invivo 5 software (Anatomage Inc., San FI by clinical detection, intraoral radiography and CBCT Jose, CA, USA) at 1 mm thickness. All images were viewed [12, 22, 23]. The aim of the present study was to compare on the same monitor and environment as the intraoral and correlate assessment of molar FI via these three radiographs. methods, to help further develop evidence on the applic- ability of CBCT in molar FI assessment. Comprehensive periodontal evaluation Clinical periodontal assessment Methods All subjects had comprehensive periodontal examination Subjects by the pre-doctoral dental students under the supervision An Institutional Review Board (IRB) approval was granted and approval of a periodontal faculty. The evaluation in- prior to the start of the study (HSC-DB-17-0370). The cluded an assessment of molar furcation involvement ac- patients who visited the University of Texas School of cording to modified Glickman’s classification [10](Fig. 1). Dentistry at Houston dental clinic from 2012 to 2016 were Briefly, this classification was defined as: Class I, incipient retrospectively screened according to the selection criteria. or early stage of furcation involvement, bone destruction The inclusion criteria were: 1) subject was diagnosed as is less than 2 mm into the furca; Class II, horizontal bone having generalized moderate or severe chronic periodon- destruction extending deeper than 2 mm but less than titis; 2) subject had comprehensive periodontal examination 6 mm into the furca; Class III, horizontal bone destruc- andinformation hadbeenstoredinthe school’sElectronic tions communicate between furcae of the tooth, and result Health Record (EHR); 3) subject had diagnostic quality in a through-and-through tunnel. periapical and/or bitewing radiographs covering posterior dentition; 4) subject had diagnostic quality CBCT scan with Intraoral radiographic assessment coverage of entire maxilla and mandible. Majority of the First molar furcation status was evaluated on molar PA patients had CBCT scans for implant treatment planning and/or BW radiographs. Presence of triangular radio- purpose, and the time interval between periodontal clinical lucency at the furcation area, and/or alveolar bone level exam and CBCT scan was less than 3 months. All of the was observed below furcation were radiographic signs patients who met the inclusion criteria were included in the for FI. FI was recorded as presence or absence based on study, and their first molars of maxilla and mandible bilat- the intraoral radiographs (Fig. 2). erally were assessed according to the following methods. CBCT imaging measurements Intraoral radiographic acquisition First molar furcation assessment was conducted mainly All the intraoral radiographs were acquired with Focus on reconstructed CBCT sagittal and axial views. Pres- wall-mounted unit (Instrumentarium Dental, Charlotte, ence of FI was demonstrated as loss of trabecular bone Zhang et al. BMC Oral Health (2018) 18:75 Page 3 of 7 Fig. 1 Periodontal chart demonstrates classification of molar furcation involvement at the furcation region on both axial and sagittal view. reanalyzed in 7 months to evaluate intra-rater reliability The depth of FI was measured on axial view where the and reproducibility. slice showed the greatest amount of bone loss. On this slice, a line was drawn tangentially to the adjacent root Statistical analysis surfaces. The distance from this line to the deepest point Spearman’s correlation analysis was used to determine of bone loss was designated as the amount of furcation the correlations between clinical detection and intraoral bone loss. If applicable, buccal and/or lingual furcation radiography, clinical detection and CBCT, as well as bone loss was measured for mandibular first molar, and intraoral radiography and CBCT at all the measured buccal, mesial palatal, and distal palatal furcation bone sites. The difference in the correlation coefficients was loss were measured for maxillary first molars (Fig. 3). analyzed using Steiger’s Z-test. Intra-class correlation All the data were analyzed by one of the co-authors coefficient (ICC) was calculated to assess intra-rater KF, who was a first-year dental student and received reliability and reproducibility. The statistical difference adequate training on molar furcation assessment via was set at p < 0.05. The statistical analysis were run with intraoral radiographs and CBCT scans. The data were SPSS program (version 24, IBM, Armonk, NY, USA). Fig. 2 Intraoral radiographs demonstrate molar furcation status. a presence of furcation involvement. b absence of furcation involvement Zhang et al. BMC Oral Health (2018) 18:75 Page 4 of 7 Fig. 3 Measurement of molar furcation involvement on CBCT scans. a a schematic diagram illustrates measurement of furcation bone loss of a maxillary first molar. Dotted line represents tangent line connecting two adjacent root surfaces. Arrows represent distances from the middle of tangent line to the deepest point of bone loss at the different surfaces. Red, green, and blue arrows denote furcation bone loss at buccal, mesial palatal, and distal palatal surface of the molar, respectively. MB, mesial buccal root; DB, distal buccal root; and P, palatal root. b a representative CBCT axial view demonstrates measurements of furcation bone loss of a maxillary first molar. c a schematic diagram illustrates measurement of furcation bone loss of a mandibular first molar. Dotted line represents tangent line connecting buccal or lingual surfaces of the two roots, respectively. Arrows represent distances from the middle of tangent line to the deepest point of bone loss at the different surfaces. Red and green arrows denote furcation bone loss at buccal and lingual surface of the molar, respectively. M, mesial root; and D, distal root. d a representative CBCT axial view demonstrates measurements of furcation bone loss of a mandibular first molar Results Based on a previous study conducted by Qiao et al. [13] who compared molar furcation assessment between clin- ical probing and CBCT, a power analysis was performed which demonstrated that a sample size of 51 subjects would achieve 80% power to detect the association be- Table 1 First molar furcation involvement assessed by periodontal probing tween these two evaluation methods on a significance level of 0.05. To ensure adequate sample size, a total of Modified Maxillary first molar Mandibular first molar Glickman 83 patients were included in the study. Among these pa- B MP DP Average B L Average classification tients, 41 were males, 42 were females, and an age range Not present 49.1% 78.4% 83.6% 70.4% 60.8% 53.9% 57.4% of 31–86 with a mean age of 59.03 ± 13.08 years old. Class I 34.5% 7.8% 5.2% 15.8% 18.6% 27.5% 23.1% First molar FI assessed by clinical detection, BW/PA Class II 9.5% 6.9% 6.0% 7.5% 13.7% 11.8% 12.8% and CBCT were illustrated in Tables 1, 2 and 3, respect- ively. For maxillary first molar B, MP and DP FI, clinical Class III 6.9% 6.9% 5.2% 6.3% 6.9% 5.9% 6.4% detection demonstrated a mean modified Glickman’s Total 100% 100% 100% 100% 100% 100% 100% classification of 0.75 ± 0.08, 0.41 ± 0.08, 0.33 ± 0.07, re- Data are presented as percentage of assayed surfaces without or with furcation spectively, and CBCT assessment revealed a mean 1. involvement of corresponding category based on periodontal charting Abbreviations: B buccal, MP mesial palatal, DP distal palatal, L lingual 55 ± 0.22, 0.58 ± 0.05, 0.67 ± 0.12 mm bone loss, respectively. Modified Glickman classification: Class I, incipient or early stage of furcation For mandibular first molar B and L FI, clinical detection involvement, bone destruction is less than 2 mm into the furca; Class II, horizontal bone destruction extending deeper than 2 mm but less than 6 mm demonstrated a mean modified Glickman’s classification of into the furca; Class III, horizontal bone destructions communicate between 0.66 ± 0.10 and 0.69 ± 0.09, respectively, and CBCT assess- furcae of the tooth, and result in a through-and-through tunnel ment revealed a mean 1.52 ± 0.19 and 1.15 ± 0.18 mm bone Not present: no furcation involvement Zhang et al. BMC Oral Health (2018) 18:75 Page 5 of 7 Table 2 First molar furcation involvement assessed by periapical Table 4 Cross tabulation of CBCT with periodontal probing for or bitewing radiographs evaluation of furcation involvement for maxillary and mandibular first molars Radiographic assessment Maxillary Mandibular first molar first molar Count Periodontal probing Total Absence of furcation involvement 71.8% 66.0% 01 2 3 Presence of furcation involvement 28.2% 34% CBCT (mm) 0.0 213 36 10 3 262 Total 100% 100% 0.1–2.0 40 24 7 0 71 Data are presented as percentage of assayed first molars without or with 2.1–6.0 38 22 13 6 79 furcation involvement based on radiographic assessment > 6.0 1 2 3 5 11 Total 292 84 33 14 423 loss, respectively (data were presented as mean ± SD). All of the three evaluation methods demonstrated more frequent FI of mandibular first molars relative to maxillary counter- which demonstrated great reliability and repeatability of part. Of maxillary first molars, both clinical detection and the evaluator. CBCT revealed that buccal surface was more vulnerable for FI compared to palatal side. Discussion Comparison of first molar FI assessment between Our results demonstrated that all three FI assessment CBCT and clinical detection showed that, when CBCT methods had significant correlations among each other. demonstrated no furcation involvement, 18.7% of these CBCT had stronger correlation to clinical detection than cases were documented as FI on clinical detection. On PA/BW, especially on distal palatal side of maxillary first the contrary, of the 26.7% cases identified as having 0.1– molar. The results validate applicability of CBCT in FI 2.0 mm or 2.1–6.0 mm bone loss on CBCT, clinical de- assessment. Although all of the included patients had tection showed no FI (Table 4). For comparison between diagnosis of generalized moderate or severe chronic intraoral radiographic evaluation and clinical detection, periodontitis, more than a half of them were not found there were situations when no FI was detected on to have FI based on the three evaluation methods. intraoral radiographs, 25.6% of these cases were demon- When CBCT showed no furcation involvement, clin- strated to have Class I-III FI by clinical detection. In ical detection identified 18.7% of cases with FI, indicat- addition, for 18.2% cases identified as FI on radiographs, ing over-detection by clinical measurement. On the clinical detection failed to detect any bone loss (Table 5). contrary, of the 26.7% cases demonstrated bone loss on Spearman’s correlation and Steiger’s Z-test analysis CBCT, clinical detection showed no FI, suggesting under- demonstrated that clinical detection, BW/PA and CBCT detection by clinical detection. This was consistent with were significantly correlated with each other in the as- what was reported by Darby [12] and Walter [23], who sessment of first molar FI, with r values ranged between also found over- and under-estimation of FI by clinical 0.230 to 0.644 (P < 0.05, Table 6). Compared with BW/ probing relative to CBCT analysis. It is speculated that PA, CBCT appeared to have higher correlation coeffi- probing angulation and force, soft tissue inflammation, cients with clinical detection, especially at distal palatal and inter-radicular bone and root morphology, all contrib- side of maxillary first molar, which reached statistically ute to variations of clinical detection. significant difference (p < 0.05, Table 6). Between the two Between intraoral radiographic examination and clin- sets of measurements by the same rater, the ICC was 0. ical detection, there were situations when no FI was 903, with 95% confidence interval of (0.858, 0.934), identified on intraoral radiographs, about one quarter of these cases were demonstrated having FI by clinical de- tection. In addition, for 18.2% cases identified as FI on Table 3 First molar furcation involvement measured by CBCT radiographs, probing failed to detect any bone loss. This Depth of Maxillary first molar Mandibular first molar observation confirmed the necessity of supplementing furcation B MP DP Average B L Average involvement (mm) Table 5 Cross tabulation of intraoral radiograph with periodontal 0.0 46.7% 81.5% 73.9% 67.4 45.9% 54.1% 50.0% probing for evaluation of furcation involvement for maxillary and mandibular first molars 0.1–2.0 21.7% 5.4% 16.3% 14.5 15.3% 25.9% 20.6% Count Periodontal probing Total 2.1–6.0 25.0% 13.0% 6.5% 14.8 36.5% 17.6% 27.1% 0 123 > 6.0 6.5% 0.0% 3.3% 3.3 2.4% 2.4% 2.4% Intraoral radiograph 0 (absence) 258 75 13 2 352 Total 100% 100% 100% 100% 100% 100% 100% 1 (presence) 58 17 39 28 142 Data are presented as percentage of assayed surfaces without or with furcation involvement of corresponding category based on CBCT assessment Total 316 92 52 34 494 Abbreviations: B buccal, MP mesial palatal, DP distal palatal, L lingual Zhang et al. BMC Oral Health (2018) 18:75 Page 6 of 7 Table 6 Correlation coefficients of periodontal probing with periodontal probing and intraoral radiographs should be CBCT or BW/PA in assessment of furcation involvement for used as routine examinations for detection of FI. For com- maxillary and mandibular first molars plicated cases when routine exams fail to provide adequate Periodontal charting (Modified Glickman) CBCT BW/PA information for diagnosis and/or treatment planning, a a Maxillary buccal 0.599 0.579 CBCT may be attempted with the smallest field of view a a possible and optimal exposure settings. Maxillary mesial palatal 0.591 0.499 a,c a,c There were limitations for the study. It was a retrospect- Maxillary distal palatal 0.644 0.424 ive investigation, and the clinical detection was performed a a Mandibular buccal 0.372 0.362 by different dental students under the supervision of b b Mandibular lingual 0.264 0.230 board-certified periodontist, and the results were con- Abbreviations: CBCT cone beam computed tomography, BW/PA firmed by the supervising faculty before being entering in bitewing/periapical radiographs the EHR. Still, inter-operator variations could contribute Correlation is significant at p < 0.01, between CBCT and periodontal charting, or between BW/PA and periodontal charting to inconsistence in the clinical detection. Also, in the Correlation is significant at p < 0.05, between CBCT and periodontal charting, present study, a relative old model of CBCT unit, Kodak or between BW/PA and periodontal charting CBCT demonstrated significantly stronger correlation (p < 0.05) with 9500 was used, since this was the only CBCT unit in the periodontal charting relative to BW/PA at assessment of distal palatal side of Imaging Clinic of the school. This unit had a smallest maxillary first molars voxel size of 200 μm. Compared to newer CBCT units clinical detection with intraoral radiographs for the diagno- with much smaller voxel size, such as 80 μmfor Accui- sis of FI, which is reflective of the consensus in the litera- tomo [33], the much larger voxel size of current unit had ture [8, 14]. The inconsistency between these two methods limited spatial resolution, therefore, could limit the accur- could be due to measurement errors from either or both acy in the assessment of FI. In addition, current study only detecting techniques. Anatomic complexity, such as super- measured horizontal bone loss at the furcation area on imposition of palatal root at the furcation region may con- CBCT scan, in order to correlate with clinical detection. tribute to under-diagnosis of FI for maxillary molars on Modified Glickman Classification was utilized in clinical intraoral radiographs [5, 24], and sinus tract extending into detection, which only recorded horizontal furcation in- furcation due to intrapulpal infection may lead to over- volvement of the molars. Future study could consider in- diagnosis of FI on intraoral radiographs [25], respectively. corporating vertical bone loss measurement on CBCT, to The current study identified that mandibular first mo- gain better appreciation on furcation status. Intra-surgical lars had more FI than maxillary first molars. In a study FI assessment (gold standard) could be implemented, if conducted in a Swede population, Svärdström [26] found possible, to further evaluate the accuracy of CBCT in the that the prevalence of furcation involved molars was diagnosis of FI. higher in the maxilla than in the mandible, based on clinical detection and intraoral radiographs. Hou et al. Conclusions [27] concluded that the highest prevalence of FI was in CBCT has been validated as a valuable supplemental tool the mandibular first molar in a Japanese population for assessment of molar FI in addition to periodontal based on clinical detection. It appears that geographical probing and intraoral radiographic examinations. locations, racial origins and evaluation modalities are among the factors contributing to variations of preva- Abbreviations BW: Bitewing; CBCT: Cone beam computed tomography; EHR: Electronic lence for molars with FI. Current study also found that Health Record; FI: Furcation involvement; FOV: Field of view; IRB: Institutional FI was more frequently associated with and more severe Review Board; kVp: Kilovolt; mA: Milliampere; PA: Periapical; at buccal side of maxillary first molars relative to palatal PSP: Photostimulable phosphor side, similarly as reported by Porciuncula [28]. Funding Although considered a valuable addition in molar furca- This study was partially supported by the Research Office, University of Texas tion assessment, CBCT is not without its shortcomings. School of Dentistry at Houston. Scatter, partial volume averaging and beam hardening arti- facts could compromise its diagnostic quality, especially Availability of data and materials The datasets generated and/or analysed during the current study are not for patients with heavy metallic restorations, multiple end- publicly available, in order to protect participant anonymity. However, these odontic treatment, orthodontic appliances, or implant data are available from the corresponding author on reasonable request. prosthesis [29–31]. In addition, detectability of FI by CBCT depends on how sensitive it is to reveal bone loss Authors’ contributions at furcation area. Generally, demineralization may not be WZ conceived the ideas, designed the experiments, and composed the manuscript. KF did all the measurements and performed initial data analysis. evident radiographically until it reaches approximately BW refined the ideas, performed in-depth data analysis and interpretations, 30–40% [32]. This makes it challenge to detect and initiate and critically revised the manuscript. All authors read and approved the final early intervention for incipient FI of molars. In general, manuscript. Zhang et al. BMC Oral Health (2018) 18:75 Page 7 of 7 Ethics approval and consent to participate 18. Aljehani YA. 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BMC Oral HealthSpringer Journals

Published: May 3, 2018

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