Accepted Manuscript Mandibular tori are associated with mechanical stress and mandibular shape Arthur Rodriguez Gonzalez Cortes , DDS, MS Zhaoyu Jin , M. Eng. Matthew Daniel Morrison , DMD, MSc Emiko Saito Arita , DDS, PhD Jun Song , PhD Faleh Tamimi , BDS, PhD PII:
S0278-2391(14)00577-1
DOI:
10.1016/j.joms.2014.05.024
Reference:
YJOMS 56344
To appear in:
Journal of Oral and Maxillofacial Surgery
Received Date: 12 October 2013 Revised Date:
21 May 2014
Accepted Date: 21 May 2014
Please cite this article as: Gonzalez Cortes AR, Jin Z, Morrison MD, Saito Arita E, Song J, Tamimi F, Mandibular tori are associated with mechanical stress and mandibular shape, Journal of Oral and Maxillofacial Surgery (2014), doi: 10.1016/j.joms.2014.05.024. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Mandibular tori are associated with mechanical stress and mandibular shape
Zhaoyu Jin, M. Eng.2
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Arthur Rodriguez Gonzalez Cortes, DDS, MS1
Matthew Daniel Morrison, DMD, MSc3
Jun Song, PhD5
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Emiko Saito Arita, DDS, PhD4
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Faleh Tamimi, BDS, PhD6
1
Graduate Student, Department of Stomatology, School of Dentistry, University of São Paulo, São Paulo, Brazil
2
Graduate Student, Department of Mining and Materials Engineering, McGill University, Montreal, Quebec, Canada
3
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OMFS Resident, Schulich School of Medicine & Dentistry, Western University, London, Ontario, Canada
4
Professor, Department of Stomatology, School of Dentistry, University of São Paulo, São Paulo, Brazil
5
Assistant Professor, Faculty of Dentistry, McGill University, Montreal, Quebec, Canada
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Assistant Professor, Department of Mining and Materials Engineering, McGill University, Montreal, Quebec, Canada
Corresponding author: Prof. Dr. Faleh Tamimi Faculty of Dentistry, McGill University Room M60C, Strathcona Anatomy & Dent, 3640 University Street, Montreal, Quebec H3A 0C7, CANADA Phone: +1-514-398-7203 ext.009654 / Fax: +1 514-398-8900 Email: [email protected]
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ACCEPTED MANUSCRIPT Mandibular tori are associated with mechanical stress and mandibular shape
Abstract
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Purpose: The influence of mechanical stimulation on formation the formation of tori mandibularis (TM) is still poorly understood. This article aimed at understanding the etiology of TM by investigating the role of parafunctional
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activity and mandibular morphology on formation of TM.
Methods: We designed a case-control study for patients attending the dental
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clinic of this study. Patients presenting TM were defined as cases, whereas patients without TM were defined as controls. Finite element analysis (FEA) was employed in 3D mandibular models to examine the stress distribution in the mandibles with and without TM. In addition, associations of mandibular
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arch shape, mandibular cortical index and parafunctional activity with the presence of TM, were assessed by means of odds ratio analysis. Results: Ten patients with TM and 37 patients without TM were selected (22
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men and 25 women, mean age of 54.3 ± 8.4 years). FEA revealed stress
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concentration on the region where TM forms during simulations of parafunctional activity. Radiographic assessment revealed that subjects with TM were more likely to have, square shape mandible with sharp angles (p=0.001) and normal mandibular cortex (p=0.03), while subjects without TM have round shape mandible with obtuse angles and eroded mandibular cortex. Conclusion: Parafunctional activity could be causing the formation of TM by concentrating mechanical stress in the region where TM usually form. For this
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ACCEPTED MANUSCRIPT reason, mandibular geometries that favor stress concentration, such as square-shaped mandibles, are associated with higher prevalence of TM.
Keywords: Torus mandibularis; mastication; occlusal stress; finite element
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analysis; cone beam computed tomography.
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ACCEPTED MANUSCRIPT Introduction
Harnessing the human body’s capability for ectopic oral bone formation, as occurs with tori mandibularis (TM), promises the potential of an alternative
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to surgical bone and soft tissue augmentation for dental rehabilitation.[1] Understanding etiology of ectopic oral bone formation would improve planning of TM treatment or management strategies. It would also allow exploiting the
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mechanism of TM formation to create new bone for regenerative purposes.
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Torus mandibularis (TM) is one of the most commonly encountered oral bone exostoses. It consists primarily of dense cortical bone without marrow,[2, 3]
and it can present itself, often bilaterally, on the lingual aspect of the
mandible from retromolar region to symphysis. The most common site,
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however, is in the canine/premolar region above the mylohyoid line.[3] TM has a nearly equal gender predilection and tends to grow slowly and continuously from the peripubertal period onward.[3, 4] Typically, the TM gradually enlarges
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into adulthood, but has been found to spontaneously stop growing, and even
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regress in size, in the absence of teeth.[3, 5]
Numerous studies have indirectly implicated a relationship between TM
and signs of parafunctional habits, such as, abfraction, dental attrition and temporomandibular dysfunction (TMD).[6-8] These studies have suggested that the pattern of masticatory stress may influence the occurrence of ectopic oral bone formation, specifically TM.
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ACCEPTED MANUSCRIPT Bone adapts to mechanical challenges via the biological machinery operating at the tissue level, whereby bone deposition and bone resorption occur in concert to increase bone strength,[9, 10] and alter bone morphology.[11] Functional adaptation of bone to mechanical loading is best exemplified by
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the strengthening of load bearing bones (LBBs).[12, 13] Accordingly, it could be hypothesized that forces exerted on the lingual bone during excursive parafunction trigger a cascade of molecular events leading to TM formation;
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therefore, since canine/premolar teeth bear greater occlusal loads during excursive movements, they may exert a force on the bone which results in
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periosteal stretching and subsequent cortical bone deposition.[2, 3]
The distribution of mechanical stress within an object depends upon the makeup and morphology of the object in question.[9,
11]
Accordingly, we
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hypothesized that excursive parafunctional stresses would be concentrated in the lingual canine/premolar region of the mandible, congruent with the typical location of TM formation. We also hypothesized that mandibular morphology
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in subjects with TM allows for concentration of parafunctional stresses in the
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anterior lingual area of the mandible. To test our hypotheses, we implemented a case-control study utilizing FEA to analyze parafunctional stress distribution within the mandibles of subjects with and without TM. Moreover, we aimed to evaluate the mandibular morphology of case and control subjects to identify associations with the presence of TM.
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ACCEPTED MANUSCRIPT Material and Methods
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Study design/sample
To address the research purpose, the investigators designed and implemented a case-control study, which followed the STROBE guidelines for
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observational studies, and the Declaration of Helsinki on medical ethics. Approval was granted from the ethics committee of the School of Dentistry,
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University of São Paulo, São Paulo, Brazil. Patients presenting TM were defined as cases, whereas patients without TM were defined as controls. Cases and controls were comparable in terms of age and gender (no significant differences). All subjects willing to participate in this study signed
radiographic images.
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an informed consent form allowing for the use of their treatment data and
The study population was composed of subjects attending the dental
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clinic at the School of Dentistry, University of São Paulo, São Paulo, Brazil,
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between January 2013 and July 2013.
Inclusion and Exclusion Criteria
Subjects included in the study sample had dental study models, digital orthopantomographs and cone beam computed tomographic (CBCT) scan data, obtained from the archives of the dental clinic for analysis. All patients attending this clinic undergo a routine digital orthopantomograph for initial
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ACCEPTED MANUSCRIPT examination. In addition, CBCT exams are taken from every patient indicated for oral surgeries or for diagnosing an unrelated pathologic condition. Demographic parameters (i.e. age and gender) were recorded for all subjects. Subjects’ medical records were also assessed for any history of
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parafunctional habit(s), including tooth grinding, nail biting, and/or clenching.
Subjects with systemic factors known to interfere with bone or soft tissue
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healing were excluded from the study. Such factors included: diabetes mellitus (type I and II), hyperthyroidism, smoking history, rheumatoid arthritis,
metabolic
bone
immunocompromised
disease, state.
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cancer with bone metastases, chemotherapy treatment, chronic steroid use, major
renal
Furthermore,
disease,
subjects
who
and/or were
any taking
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medication(s) known to affect bone metabolism were excluded from the study.
Variables
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The primary outcome variable of this study was the presence of TM.
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History of parafunctional activity was analyzed as a predictor variable, and as a secondary outcome variable, to assess direct associations between this variable and other predictor variables. Accordingly, case subjects were defined as those with discernable protrusions of bone on the lingual aspect of the mandible, consistent with TM, as detected on CBCT axial images. Control subjects were defined as those with a uniformly contoured lingual aspect of the mandible consistent with lack of TM.
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ACCEPTED MANUSCRIPT Furthermore, five predictor variables were assessed: age, gender, the mandibular arch shape, the mandibular cortical index, and history of parafunctional activity. Complementary variables such as mandibular angle measurements and finite element analysis were also compared between case
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and control groups.
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Data Collection
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History of parafunctional activity
Subjects’ medical records were assessed for any history of parafunctional habit(s), including tooth grinding, nail biting, and/or clenching. Reports of the presence of any of the aforementioned parameters were considered as
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positivity for history of parafunctional activity.
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Mandibular Arch Shape Classification
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Dental study casts were used to classify the mandibular arch shape as either square-shaped or round-shaped based on a previously described classification for arch morphology.[14] Briefly, references points, lines and angles are identified according to the teeth position in the mandibular study cast. Square-shape mandible presents a dental arch with protruded canine with the anterior teeth in an almost linear arrangement. Posterior teeth are also aligned, and both posterior hemiarchs are parallel to each other. Roundshape mandible presents a semicircle dental arch with no canine protrusion.
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Radiographic Methods
All preoperative digital orthopantomographic images were obtained
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using the Veraviewepocs 2D (Morita, Tokyo, Japan) set at 60kV and 4 mA, with a 0.5-mm copper filter. Images were provided in tagged image file format (TIFF) and were analyzed using the ImageJ® software (National Institute of
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Health, Bethesda, MD).
All CBCT images were obtained with the scan unit (i-CAT Classic (Image
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Sciences International, Hatfield, PA, USA), configured with a diagnostic protocol used for dental implants (0.25-mm voxel, 120kVp, 8mA, field of view of 16-cm in diameter and 6-cm in height, 1-mm slice thickness). CBCT images were provided in the Digital Imaging Communications in Medicine (DICOM)
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format and analyzed using the OsiriX imaging software (open-source, DICOM viewer OsiriX 3.9.4 version, Pixmeo, Geneva, Switzerland).
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Radiographic Measurements Assessed
Mandibular cortical index
The mandibular cortical index (MCI)[15, 16] is a measurement used for the
approximation of bone mineral density (BMD) based on the assessment of orthopantomographic images. MCI classifies the appearance of the inferior cortex of the mandible distal to the mental foramina, as viewed on an
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ACCEPTED MANUSCRIPT orthopantomograph. A normal cortex is an indicative of high systemic bone density. This classification uses a three-point scale:
C1: normal. The endosteal margin of the cortex is even and sharply defined
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on both sides of the mandible.
C2: mild/moderate erosion. The endosteal margin shows semilunar defects (lacunar resorption) or seems to form endosteal cortical residues (one to three
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layers) on one or both sides of the mandible.
clearly porous.
Mandibular angle measurements
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C3: severe erosion. The cortical layer forms heavy endosteal residues and is
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Mandibular angle measurements (in degrees) were recorded separately in random order. Three buccal and three lingual angles were labeled on axial CBCT images of mandibles (at the level of the mental foramina) (Fig. 1);
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these angles were as follows:
Angle a. The vertex at right mental foramen connects the anterior aspect of the right mandibular symphysis with the apex of the mental protuberance. Angle b. The vertex at the apex of the mental protuberance connects with points at right and left mental foramina. Angle c. The contralateral to angle athe vertex at the left mental foramen connects the anterior aspect of the left mandibular symphysis with the apex of the mental protuberance.
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ACCEPTED MANUSCRIPT Angle d. The vertex on the lingual aspect of the right mental foramen connects with two points: one at the posterior aspect of the alveolar lingual plate, and another in the lingual foramina.
lingual aspect of the right and left mental foramina.
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Angle e. The vertex on the lingual foramina connects with points at the
Angle f. The contralateral to angle dthe vertex at the lingual aspect of left mental foramen connects the posterior aspect of the alveolar lingual plate and
Data analysis
Finite Element Analysis
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the lingual foramina.
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In order to assess the stress distribution within case (Figs. 2A and C) and control (Figs. 2B and D) mandibles during functional and parafunctional loading, von Mises stress calculations were performed upon FEA simulations
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(Figs. 3B and D). The von Mises stress[17], denoted as
below, is quantity
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commonly used in engineering to predict the yielding of materials under multiaxial loading conditions. It is defined as a function of individual stress components (i.e.,
and
with i, j, k=1, 2, 3):
Stress analysis via FEA simulations has been shown to be an effective means in the study of biomechanical behaviors of bones.[18-21] In the present study, for simplicity we assumed that the material constituting the volume model was
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ACCEPTED MANUSCRIPT homogenous, isotropic and linear-elastic. We note that the real mandibular bone is a heterogeneous material, with the elastic moduli, Poisson’s ratio being different in longitudinal, radial and tangential directions (i.e., anisotropic).[18, 22, 23] Nonetheless we adopt the idealized FEA model to avoid
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complicated parameterization, and to qualitatively illustrate the influence of the mandible geometry rather than make a quantitative assessment.
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comprehensive review of the accuracy of FEA in describing the biomechanical
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behavior of bones can be found in refs.[18-21] In our FEA simulations the Young’s modulus and Poisson’s ratio chosen for the material were E = 13
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GPa and ν = 0.3, respectively, which are the values often used for cortical bone.[24, 25]
Two FEA material models are constructed from the 3D-CBCT scan data: a representative from the case group (Figs. 3A and B) and one representative
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from the control group (Figs. 3C and D). The model generation process is described as follows. First, the CBCT scan images in DICOM format were used to construct surface models of the mandibles (Fig. 2) that were
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converted to stereolithography (STL) files containing coordinates for the
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triangular facets and vertices.[26] Then the STL files were re-meshed with HyperMesh (Altair Engineering Inc., Auckland, New Zealand) using solid tetrahedral elements to create corresponding volume models (Figs. 2A and C) onto which the material properties were added. For the two FEA models shown in Fig. 3, 20898 nodes (85842 linear tetrahedral elements in total) and 25373 nodes (105585 linear tetrahedral elements in total) were used for Fig. 3B and Fig. 3D, respectively. Mesh convergence studies have been performed for both models to ensure that simulation results are stable based
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ACCEPTED MANUSCRIPT on those mesh densities. Finally, the meshes generated by HyperMesh were imported into Abaqus (Simulia, Providence, RI) to perform stress analysis. Boundary conditions (BCs) were designed to simulate the typical occlusal constraints and muscle responses experienced during mastication and
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parafunctional loading. Displacement and traction BCs were applied onto the mesh in order to compute the deformation and stress states within the mandibles. The zero displacement BC, denoted as Ωd, was applied to the
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working side condyle and canine, simulating canine guidance upon parafunctional loading, while a traction BC, denoted as Ωf, was applied to the
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medial aspect of the contralateral gonial angle, simulating contraction of
r contralateral medial pterigoid muscle (Figs. 3A and C). The force vector, F , acting on Ωf had force components (Fx, Fy, Fz) prescribed as (100N, 0, 100N). It mimics the force exerted by the lateral ptreygoid muscle, and is in line with
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Statistical analysis
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the one described in Schindler et al.[27]
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All radiographic measurements were performed by two trained observers (i.e. dentists with expertise in oral radiology), which were blinded to the presence or absence of tori. Intraobserver reliability was assessed between measurements performed 2 weeks apart to eliminate memory bias. Intra and interobserver agreement were assessed using the intraclass correlations coefficient (ICC) for the CBCT angulations and the kappa test for MCI.
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ACCEPTED MANUSCRIPT Conditional logistic regression were performed using the IBM SPSS Statistics 17 software (SPSS, Inc, Chicago, IL). Risk estimates were presented as odds ratios (ORs) with 95% confidence intervals (CIs). In addition, Mann Whitney test was used to assess angle differences between
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cases and controls. A p value under 0.05 was considered statistically significant.
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Results
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A total of 53 subjects’ CBCT data were initially selected during the study period. Of the twelve subjects identified as having TM, two were excluded due to metabolic bone disease. On the other hand, of the 41 subjects identified as not having TM, four were excluded (three subjects with
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diabetes mellitus and one with metabolic bone desease). As a result, 47 patients (22 men and 25 women, mean age of 54.3 ± 8.4 years) fulfilled the
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inclusion criteria.
reproducibility
and
interobserver
reliability
were
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Intraobserver
confirmed for CBCT angulations (ICC between 0.82 and 0.89, p=0.001), and for mandibular shape and MCI measurements (kappa index between 0.78 and 0.84, P=0.01).
Unlike physiological mastication, parafunctional loading generated a considerable amount of mechanical stress in the mandible (Fig. 3). The largest von Mises stresses were concentrated on the lingual aspect of the
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ACCEPTED MANUSCRIPT mandible in the canine/premolar apical regions, which correspond to the typical site of TM. Stress values were highest in case subjects (See Figs. 3B and D).
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The presence of TM was strongly associated with a square-shaped mandibular arch (Table 1) (OR 26.44, 95% CI 4.39−115.21, P=0.001), a history of parafunctional habits (OR 5.44, 95% CI 1.22−24.04, P=0.046), and
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a normal mandibular cortex (MCI C1) (OR 6.57, 95% CI 1.21−35.43, P=0.030). History of parafunctional habits, however, was not significantly
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associated with a square-shaped mandibular arch (p=.137), or with MCI C1 (p=.524) (Table 2). No significant associations were found between subjects’ age nor gender and the presence of TM.
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To further confirm relationships between mandibular geometry and the presence of TM, the buccal and lingual angles of case and control subjects were analyzed (Figure 4). A statistically significant difference between case
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and control subjects was observed for the buccal angles, a (P=0.007) and c
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(P=0.022), such that these angles were more acute for case subjects. No statistically significant associations were observed between the remaining mandibular angle measurements for the case and control subjects.
Discussion
The present study strove to test the hypothesis that excursive parafunctional stresses would be concentrated in the ridge area where TM
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ACCEPTED MANUSCRIPT usually form. A second hypothesis was that the stress accumulation provided by parafunction could be favored by mandibular. Both hypotheses were confirmed. Additionally, parafunctional activity and mandibular morphology were found to be independent factors influencing TM formation.
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Numerous studies have shown associations between signs of parafunctional activity (i.e. dental attrition and temporomandibular joint dysfunction) and the presence of TM.[5-7] A paucity of evidence, however, is
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available in support of the mechanism behind this association. The results of our investigations confirmed our hypothesis, to wit: unlike physiological
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mastication, parafunctional activity results in the accumulation of mechanical stress in the typical location of TM. In addition, stress accumulates to a greater extent in individuals with TM, suggesting a morphological pattern for these individuals. As a result, our data confirm that parafunctional stress is
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associated with ectopic bone formation in the mandible, offering concrete evidence of the mechanism involved in TM formation.
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Finite element analysis of the case and control mandibles in our study
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revealed that parafunctional loading produced higher levels of mechanical stress in the lingual apical region of the canine/premolar teeth when compared to physiological loading. Interestingly, the focal area of stress concentration corresponded with that of
the typical region of TM
development.[5] Compared to control subjects, case subjects had a more pronounced area of stress concentration in this region for the same force, Ωd, and BCs applied. These findings suggested that subjects with TM possess specific mandibular geometrical conditions, which allow for focal stress
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ACCEPTED MANUSCRIPT concentration (during parafunctional loading) in the typical area of TM formation.
Although direct correlations between high overall BMD and the
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presence of oral tori have been made,[28] our investigation is the first to present the relationship between MCI and the presence of TM. The use of MCI as a surrogate for BMD measurement has previously been validated.[15, Our investigations revealed that subjects with a MCI value of C1 (normal
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mandibular cortex) were associated with the presence of TM, which suggests
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that bone metabolism may play a role in TM formation.
Occlusal forces transmitted to the mandible during mastication follow force
vectors
according
to
the
masticatory
muscles[29]
and
the
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position/angulation of the teeth.[30] Tooth position, however, is largely dictated by the shape of the dental arches, which in turn is affected by the geometric shape of the upper and lower jaws.[14] We quantified the various angulations
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on the buccal and lingual aspects of case and control subjects’ mandibles and
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observed that subjects with TM were associated with sharper, more acute buccal mandibular angulations. To our knowledge, this study is the first to demonstrate that mandibular arch form (i.e. square-shaped) is associated with the presence of TM.
Our results also indicated that mandibular geometry and anatomy (i.e. MCI, angulations, shape) were not influenced significantly by parafunctional activity. This indicates that probably mandibular geometry and parafunctional
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ACCEPTED MANUSCRIPT activity act as synergic independent predisposing factors that are associated with higher risk TM formation. Of the various, albeit poorly understood, factorsenvironmental, genetic, and metabolic believed to play a role in the development of TM, our
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investigations provided evidence for environmental and genetic influences: mechanical stress and mandibular geometry, respectively.[6, 31, 32] Our findings also implicated the involvement of bone metabolism in TM formation, as
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evidenced by the increased risk for the presence of TM in subjects lacking
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erosion of the inferior mandibular cortex (i.e. MCI of C1).
In this study, we used a FEA model meshed from patient’s mandible scan data, which allowed for accurately representing all geometrical aspects of the mandible. Furthermore, by using FEA, it was possible to directly
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visualize the deformation/stress state and distribution within the mandible under different loadings. Coupling the FEA modeling with clinical findings enabled
us
to
better
identify
key
biomechanical
components
and
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subsequently perform targeted clinical tests/characterizations.
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One limitation of our current FEA study is that we employed a simplified description of the mandible material. Consequently, the possible contributions from a) the material heterogeneity and anisotropy and b) differences in material properties due to sex, age and etc., are not captured in the analysis. Furthermore, no quantitative variables were taken from the FEA performed herein. Future studies should address this issue with more refined and targeted FEA analysis.
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ACCEPTED MANUSCRIPT Another limitation of this study is that its case control design allow for detection of associations, but not causality. Future cohort or randomized clinical trials will be needed to address this issue. Furthermore, no direct quantitative evaluation of bone metabolism was performed herein. Therefore,
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further studies on bone turnover would be recommended to assess factors involved in the biochemical etiology of TM.
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The results of our investigations have collectively provided insight into mechanism of TM formation: First, parafunctional activity generates
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mechanical stress on the lingual aspect of the anterior mandible in the typical location of TM. Second, a morphological pattern exists for the mandibular geometry of subjects with TM, whereby stress accumulation is heightened in
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subjects having a square-shaped mandible with sharper buccal angles.
Conclusion
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Parafunctional activity could be causing the formation of TM by
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concentrating mechanical stress in the region where TM usually form. For this reason, mandibular geometries that favor stress concentration, such as square-shaped mandibles, are associated with higher prevalence of TM.
Acknowledgements
A Ph.D. scholarship was granted to Arthur Rodriguez Gonzalez Cortes by the National Council for Scientific and Technological Development (CNPq –
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ACCEPTED MANUSCRIPT Brazil, N° 140291/2011-3). Prof. Faleh Tamimi recei ved grants by The Network for Oral and Bone Health Research (RSBO, Quebec, Canada F'ODQ/RSBO x-coded 217031) and by the Natural Sciences and Engineering Research Council of Canada (NSERC RGPIN 418617-12). Dr. Jun Song also
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received grants by Natural Sciences and Engineering Research Council of Canada (NSERC Engage EGP 445930-12). The authors declare that there are no conflicts of interest in this study. Approval was granted from the ethics
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committee of the School of Dentistry, University of São Paulo, São Paulo,
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Brazil (Protocol N105/11).
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ACCEPTED MANUSCRIPT References
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1. Hassan KS, Alagl AS, Abdel-Hady A: Torus mandibularis bone chips combined with platelet rich plasma gel for treatment of intrabony osseous defects: clinical and radiographic evaluation. Int J Oral Maxillofac Surg 2012;41:1519 2. Brunsvold MA, Kaiser DA, Faner RM: Recurrence of mandibular tori after surgical removal: two case reports. Journal of prosthodontics : official journal of the American College of Prosthodontists 1995;4:164 3. Garcia-Garcia AS, Martinez-Gonzalez J-M, Gomez-Font R et al.: Current status of the torus palatinus and torus mandibularis. Medicina Oral Patologia Oral Y Cirugia Bucal 2010;15:E353 4. Pynn BR, Kurys-Kos NS, Walker DA, Mayhall JT: Tori mandibularis: a case report and review of the literature. Journal (Canadian Dental Association) 1995;61:1057 5. Eggen S: Correlated characteristics of the jaws: association between torus mandibularis and marginal alveolar bone height. Acta Odontologica Scandinavica 1992;50:1 6. Morrison MD, Tamimi F: Oral tori are associated with local mechanical and systemic factors: a case-control study. J Oral Maxillofac Surg 2013;71:14 7. Al-Bayaty HF, Murti PR, Matthews R, Gupta PC: An epidemiological study of tori among 667 dental outpatients in Trinidad & Tobago, West Indies. International Dental Journal 2001;51:300 8. Sirirungrojying S, Kerdpon D, Songkhla H: Relationship between oral tori and temporomandibular disorders. International Dental Journal 1999;49:101 9. Frost HM: Emerging views about "osteoporosis", bone health, strength, fragility, and their determinants. Journal of Bone and Mineral Metabolism 2002;20:319 10. Frost HM: A 2003 update of bone physiology and Wolff's Law for clinicians. Angle Orthodontist 2004;74:3 11. Jiang YB, Zhao J, Rosen C et al.: Perspectives on bone mechanical properties and adaptive response to mechanical challenge. Journal of Clinical Densitometry 1999;2:423 12. Felson DT, Zhang YQ, Hannan MT, Anderson JJ: Effects of weight and body mass index on bone mineral density in men and women: the Framingham study. Journal of Bone and Mineral Research 1993;8:567 13. Frost HM: Bone's mechanostat: A 2003 update. Anatomical Record Part a-Discoveries in Molecular Cellular and Evolutionary Biology 2003;275A:1081 14. Kumabe S, Nakatsuka M, Iwai-Liao Y et al.: Morphological classification of mandibular dental arch forms by correlation and principal component analyses. Okajimas Folia Anat Jpn 2005;82:67 15. Klemetti E, Kolmakov S, Heiskanen P et al.: Panoramic mandibular index and bone mineral densities in postmenopausal women. Oral Surgery Oral Medicine Oral Pathology Oral Radiology and Endodontics 1993;75:774 16. Leite AF, Figueiredo PTD, Barra FR et al.: Relationships between mandibular cortical indexes, bone mineral density, and osteoporotic fractures in Brazilian men over 60 years old. Oral Surgery Oral Medicine Oral Pathology Oral Radiology and Endodontology 2011;112:648
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17. von Mises R: Mechanik der festen Körper im plastisch- deformablen Zustand. Nachrichten von der Gesellschaft der Wissenschaften zu Göttingen, Mathematisch-Physikalische Klasse 1913;1913:582 18. Wong RC, Tideman H, Kin L, Merkx MA: Biomechanics of mandibular reconstruction: a review. International journal of oral and maxillofacial surgery 2010;39:313 19. Choi AH, Ben-Nissan B, Conway RC: Three-dimensional modelling and finite element analysis of the human mandible during clenching. Australian dental journal 2005;50:42 20. Meyer U, Vollmer D, Homann C et al.: [Experimental and finite-element models for the assessment of mandibular deformation under mechanical loading]. Mund-, Kiefer- und Gesichtschirurgie : MKG 2000;4:14 21. Vollmer D, Meyer U, Joos U et al.: Experimental and finite element study of a human mandible. Journal of cranio-maxillo-facial surgery : official publication of the European Association for Cranio-Maxillo-Facial Surgery 2000;28:91 22. Dechow PC, Hylander WL: Elastic properties and masticatory bone stress in the macaque mandible. American journal of physical anthropology 2000;112:553 23. Dechow PC, Nail GA, Schwartz-Dabney CL, Ashman RB: Elastic properties of human supraorbital and mandibular bone. American journal of physical anthropology 1993;90:291 24. Fernandez JR, Gallas M, Burguera M, Viano JM: A three-dimensional numerical simulation of mandible fracture reduction with screwed miniplates. Journal of Biomechanics 2003;36:329 25. Kim HS, Park JY, Kim NE et al.: Finite element modeling technique for predicting mechanical behaviors on mandible bone during mastication. Journal of Advanced Prosthodontics 2012;4:218 26. Szilvasi-Nagy M, Matyasi G: Analysis of STL files. Mathematical and Computer Modelling 2003;38:945 27. Schindler HJ, Rues S, Turp JC, Lenz J: Heterogeneous activation of the medial pterygoid muscle during simulated clenching. Archives of Oral Biology 2006;51:498 28. Hjertstedt J, Burns EA, Fleming R et al.: Mandibular and palatal tori, bone mineral density, and salivary cortisol in community-dwelling elderly men and women. Journals of Gerontology Series a-Biological Sciences and Medical Sciences 2001;56:M731 29. Grunheid T, Langenbach GE, Korfage JA et al.: The adaptive response of jaw muscles to varying functional demands. Eur J Orthod 2009;31:596 30. Zhang M, Chen FM, Chen YJ et al.: Photoelastic Analysis of the Effects of Tooth Position on Apical Stress. Experimental Mechanics 2011;51:1135 31. Haugen LK: Palatine and mandibular tori. A morphologic study in the current Norwegian population. Acta Odontol Scand 1992;50:65 32. Seah YH: Torus palatinus and torus mandibularis: a review of the literature. Aust Dent J 1995;40:318
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ACCEPTED MANUSCRIPT Figure Legends Figure 1. Schematic 3D presentation of the buccal (A) and lingual (B) mandibular angles.
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Figure 2. Surface models (isotropic and axial views) of a mandible with TM (A and C) and a mandible without TM (B and D). Abbreviations: TM, tori mandibularis.
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Figure 3. Boundary conditions applied during FEA simulations on a mandible with TM (A) and a mandible without TM (C), where Ωd and Ωf denote the displacement and traction boundary conditions, respectively. The force components of Ωf are shown for their respective Cartesian coordinates as Fx, Fy, and Fz. The corresponding von Mises stress fields (σ) for the forces applied are depicted by color mapping for the mandible with TM (B) and the mandible without TM (D). Abbreviations: TM, tori mandibularis.
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Figure 4. Axial computed tomography views for a mandible with TM (A) and a mandible without TM (B). The inset image in A shows more clearly the pronounced TM bilaterally. *Statistically significant (P 60 years
19
03
0.40 (0.09-1.82)
Female
22
03
1
Male
15
07
3.42 (0.76-15.38)
Round
34
03
1
Square
03
07
26.44 (4.39-115.21)
Eroded cortex (C2-C3)
23
02
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Characteristics
1
Normal cortex (C1)
14
08
6.57 (1.21-35.43)
04
1
06
5.44 (1.22-24.04)
P value
Age
Mandibular arch shape
History of parafunctional habits No
29
Yes
08
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MCI
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Gender
0.297
0.154
0.001*
0.030*
0.046*
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*Statistically significant (P
S0278-2391(14)00577-1
DOI:
10.1016/j.joms.2014.05.024
Reference:
YJOMS 56344
To appear in:
Journal of Oral and Maxillofacial Surgery
Received Date: 12 October 2013 Revised Date:
21 May 2014
Accepted Date: 21 May 2014
Please cite this article as: Gonzalez Cortes AR, Jin Z, Morrison MD, Saito Arita E, Song J, Tamimi F, Mandibular tori are associated with mechanical stress and mandibular shape, Journal of Oral and Maxillofacial Surgery (2014), doi: 10.1016/j.joms.2014.05.024. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Mandibular tori are associated with mechanical stress and mandibular shape
Zhaoyu Jin, M. Eng.2
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Arthur Rodriguez Gonzalez Cortes, DDS, MS1
Matthew Daniel Morrison, DMD, MSc3
Jun Song, PhD5
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Emiko Saito Arita, DDS, PhD4
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Faleh Tamimi, BDS, PhD6
1
Graduate Student, Department of Stomatology, School of Dentistry, University of São Paulo, São Paulo, Brazil
2
Graduate Student, Department of Mining and Materials Engineering, McGill University, Montreal, Quebec, Canada
3
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OMFS Resident, Schulich School of Medicine & Dentistry, Western University, London, Ontario, Canada
4
Professor, Department of Stomatology, School of Dentistry, University of São Paulo, São Paulo, Brazil
5
Assistant Professor, Faculty of Dentistry, McGill University, Montreal, Quebec, Canada
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Assistant Professor, Department of Mining and Materials Engineering, McGill University, Montreal, Quebec, Canada
Corresponding author: Prof. Dr. Faleh Tamimi Faculty of Dentistry, McGill University Room M60C, Strathcona Anatomy & Dent, 3640 University Street, Montreal, Quebec H3A 0C7, CANADA Phone: +1-514-398-7203 ext.009654 / Fax: +1 514-398-8900 Email: [email protected]
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ACCEPTED MANUSCRIPT Mandibular tori are associated with mechanical stress and mandibular shape
Abstract
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Purpose: The influence of mechanical stimulation on formation the formation of tori mandibularis (TM) is still poorly understood. This article aimed at understanding the etiology of TM by investigating the role of parafunctional
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activity and mandibular morphology on formation of TM.
Methods: We designed a case-control study for patients attending the dental
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clinic of this study. Patients presenting TM were defined as cases, whereas patients without TM were defined as controls. Finite element analysis (FEA) was employed in 3D mandibular models to examine the stress distribution in the mandibles with and without TM. In addition, associations of mandibular
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arch shape, mandibular cortical index and parafunctional activity with the presence of TM, were assessed by means of odds ratio analysis. Results: Ten patients with TM and 37 patients without TM were selected (22
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men and 25 women, mean age of 54.3 ± 8.4 years). FEA revealed stress
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concentration on the region where TM forms during simulations of parafunctional activity. Radiographic assessment revealed that subjects with TM were more likely to have, square shape mandible with sharp angles (p=0.001) and normal mandibular cortex (p=0.03), while subjects without TM have round shape mandible with obtuse angles and eroded mandibular cortex. Conclusion: Parafunctional activity could be causing the formation of TM by concentrating mechanical stress in the region where TM usually form. For this
2
ACCEPTED MANUSCRIPT reason, mandibular geometries that favor stress concentration, such as square-shaped mandibles, are associated with higher prevalence of TM.
Keywords: Torus mandibularis; mastication; occlusal stress; finite element
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analysis; cone beam computed tomography.
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ACCEPTED MANUSCRIPT Introduction
Harnessing the human body’s capability for ectopic oral bone formation, as occurs with tori mandibularis (TM), promises the potential of an alternative
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to surgical bone and soft tissue augmentation for dental rehabilitation.[1] Understanding etiology of ectopic oral bone formation would improve planning of TM treatment or management strategies. It would also allow exploiting the
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mechanism of TM formation to create new bone for regenerative purposes.
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Torus mandibularis (TM) is one of the most commonly encountered oral bone exostoses. It consists primarily of dense cortical bone without marrow,[2, 3]
and it can present itself, often bilaterally, on the lingual aspect of the
mandible from retromolar region to symphysis. The most common site,
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however, is in the canine/premolar region above the mylohyoid line.[3] TM has a nearly equal gender predilection and tends to grow slowly and continuously from the peripubertal period onward.[3, 4] Typically, the TM gradually enlarges
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into adulthood, but has been found to spontaneously stop growing, and even
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regress in size, in the absence of teeth.[3, 5]
Numerous studies have indirectly implicated a relationship between TM
and signs of parafunctional habits, such as, abfraction, dental attrition and temporomandibular dysfunction (TMD).[6-8] These studies have suggested that the pattern of masticatory stress may influence the occurrence of ectopic oral bone formation, specifically TM.
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ACCEPTED MANUSCRIPT Bone adapts to mechanical challenges via the biological machinery operating at the tissue level, whereby bone deposition and bone resorption occur in concert to increase bone strength,[9, 10] and alter bone morphology.[11] Functional adaptation of bone to mechanical loading is best exemplified by
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the strengthening of load bearing bones (LBBs).[12, 13] Accordingly, it could be hypothesized that forces exerted on the lingual bone during excursive parafunction trigger a cascade of molecular events leading to TM formation;
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therefore, since canine/premolar teeth bear greater occlusal loads during excursive movements, they may exert a force on the bone which results in
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periosteal stretching and subsequent cortical bone deposition.[2, 3]
The distribution of mechanical stress within an object depends upon the makeup and morphology of the object in question.[9,
11]
Accordingly, we
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hypothesized that excursive parafunctional stresses would be concentrated in the lingual canine/premolar region of the mandible, congruent with the typical location of TM formation. We also hypothesized that mandibular morphology
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in subjects with TM allows for concentration of parafunctional stresses in the
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anterior lingual area of the mandible. To test our hypotheses, we implemented a case-control study utilizing FEA to analyze parafunctional stress distribution within the mandibles of subjects with and without TM. Moreover, we aimed to evaluate the mandibular morphology of case and control subjects to identify associations with the presence of TM.
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ACCEPTED MANUSCRIPT Material and Methods
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Study design/sample
To address the research purpose, the investigators designed and implemented a case-control study, which followed the STROBE guidelines for
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observational studies, and the Declaration of Helsinki on medical ethics. Approval was granted from the ethics committee of the School of Dentistry,
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University of São Paulo, São Paulo, Brazil. Patients presenting TM were defined as cases, whereas patients without TM were defined as controls. Cases and controls were comparable in terms of age and gender (no significant differences). All subjects willing to participate in this study signed
radiographic images.
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an informed consent form allowing for the use of their treatment data and
The study population was composed of subjects attending the dental
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clinic at the School of Dentistry, University of São Paulo, São Paulo, Brazil,
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between January 2013 and July 2013.
Inclusion and Exclusion Criteria
Subjects included in the study sample had dental study models, digital orthopantomographs and cone beam computed tomographic (CBCT) scan data, obtained from the archives of the dental clinic for analysis. All patients attending this clinic undergo a routine digital orthopantomograph for initial
6
ACCEPTED MANUSCRIPT examination. In addition, CBCT exams are taken from every patient indicated for oral surgeries or for diagnosing an unrelated pathologic condition. Demographic parameters (i.e. age and gender) were recorded for all subjects. Subjects’ medical records were also assessed for any history of
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parafunctional habit(s), including tooth grinding, nail biting, and/or clenching.
Subjects with systemic factors known to interfere with bone or soft tissue
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healing were excluded from the study. Such factors included: diabetes mellitus (type I and II), hyperthyroidism, smoking history, rheumatoid arthritis,
metabolic
bone
immunocompromised
disease, state.
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cancer with bone metastases, chemotherapy treatment, chronic steroid use, major
renal
Furthermore,
disease,
subjects
who
and/or were
any taking
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medication(s) known to affect bone metabolism were excluded from the study.
Variables
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The primary outcome variable of this study was the presence of TM.
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History of parafunctional activity was analyzed as a predictor variable, and as a secondary outcome variable, to assess direct associations between this variable and other predictor variables. Accordingly, case subjects were defined as those with discernable protrusions of bone on the lingual aspect of the mandible, consistent with TM, as detected on CBCT axial images. Control subjects were defined as those with a uniformly contoured lingual aspect of the mandible consistent with lack of TM.
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ACCEPTED MANUSCRIPT Furthermore, five predictor variables were assessed: age, gender, the mandibular arch shape, the mandibular cortical index, and history of parafunctional activity. Complementary variables such as mandibular angle measurements and finite element analysis were also compared between case
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and control groups.
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Data Collection
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History of parafunctional activity
Subjects’ medical records were assessed for any history of parafunctional habit(s), including tooth grinding, nail biting, and/or clenching. Reports of the presence of any of the aforementioned parameters were considered as
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positivity for history of parafunctional activity.
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Mandibular Arch Shape Classification
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Dental study casts were used to classify the mandibular arch shape as either square-shaped or round-shaped based on a previously described classification for arch morphology.[14] Briefly, references points, lines and angles are identified according to the teeth position in the mandibular study cast. Square-shape mandible presents a dental arch with protruded canine with the anterior teeth in an almost linear arrangement. Posterior teeth are also aligned, and both posterior hemiarchs are parallel to each other. Roundshape mandible presents a semicircle dental arch with no canine protrusion.
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Radiographic Methods
All preoperative digital orthopantomographic images were obtained
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using the Veraviewepocs 2D (Morita, Tokyo, Japan) set at 60kV and 4 mA, with a 0.5-mm copper filter. Images were provided in tagged image file format (TIFF) and were analyzed using the ImageJ® software (National Institute of
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Health, Bethesda, MD).
All CBCT images were obtained with the scan unit (i-CAT Classic (Image
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Sciences International, Hatfield, PA, USA), configured with a diagnostic protocol used for dental implants (0.25-mm voxel, 120kVp, 8mA, field of view of 16-cm in diameter and 6-cm in height, 1-mm slice thickness). CBCT images were provided in the Digital Imaging Communications in Medicine (DICOM)
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format and analyzed using the OsiriX imaging software (open-source, DICOM viewer OsiriX 3.9.4 version, Pixmeo, Geneva, Switzerland).
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Radiographic Measurements Assessed
Mandibular cortical index
The mandibular cortical index (MCI)[15, 16] is a measurement used for the
approximation of bone mineral density (BMD) based on the assessment of orthopantomographic images. MCI classifies the appearance of the inferior cortex of the mandible distal to the mental foramina, as viewed on an
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ACCEPTED MANUSCRIPT orthopantomograph. A normal cortex is an indicative of high systemic bone density. This classification uses a three-point scale:
C1: normal. The endosteal margin of the cortex is even and sharply defined
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on both sides of the mandible.
C2: mild/moderate erosion. The endosteal margin shows semilunar defects (lacunar resorption) or seems to form endosteal cortical residues (one to three
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layers) on one or both sides of the mandible.
clearly porous.
Mandibular angle measurements
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C3: severe erosion. The cortical layer forms heavy endosteal residues and is
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Mandibular angle measurements (in degrees) were recorded separately in random order. Three buccal and three lingual angles were labeled on axial CBCT images of mandibles (at the level of the mental foramina) (Fig. 1);
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these angles were as follows:
Angle a. The vertex at right mental foramen connects the anterior aspect of the right mandibular symphysis with the apex of the mental protuberance. Angle b. The vertex at the apex of the mental protuberance connects with points at right and left mental foramina. Angle c. The contralateral to angle athe vertex at the left mental foramen connects the anterior aspect of the left mandibular symphysis with the apex of the mental protuberance.
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ACCEPTED MANUSCRIPT Angle d. The vertex on the lingual aspect of the right mental foramen connects with two points: one at the posterior aspect of the alveolar lingual plate, and another in the lingual foramina.
lingual aspect of the right and left mental foramina.
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Angle e. The vertex on the lingual foramina connects with points at the
Angle f. The contralateral to angle dthe vertex at the lingual aspect of left mental foramen connects the posterior aspect of the alveolar lingual plate and
Data analysis
Finite Element Analysis
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the lingual foramina.
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In order to assess the stress distribution within case (Figs. 2A and C) and control (Figs. 2B and D) mandibles during functional and parafunctional loading, von Mises stress calculations were performed upon FEA simulations
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(Figs. 3B and D). The von Mises stress[17], denoted as
below, is quantity
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commonly used in engineering to predict the yielding of materials under multiaxial loading conditions. It is defined as a function of individual stress components (i.e.,
and
with i, j, k=1, 2, 3):
Stress analysis via FEA simulations has been shown to be an effective means in the study of biomechanical behaviors of bones.[18-21] In the present study, for simplicity we assumed that the material constituting the volume model was
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ACCEPTED MANUSCRIPT homogenous, isotropic and linear-elastic. We note that the real mandibular bone is a heterogeneous material, with the elastic moduli, Poisson’s ratio being different in longitudinal, radial and tangential directions (i.e., anisotropic).[18, 22, 23] Nonetheless we adopt the idealized FEA model to avoid
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complicated parameterization, and to qualitatively illustrate the influence of the mandible geometry rather than make a quantitative assessment.
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comprehensive review of the accuracy of FEA in describing the biomechanical
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behavior of bones can be found in refs.[18-21] In our FEA simulations the Young’s modulus and Poisson’s ratio chosen for the material were E = 13
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GPa and ν = 0.3, respectively, which are the values often used for cortical bone.[24, 25]
Two FEA material models are constructed from the 3D-CBCT scan data: a representative from the case group (Figs. 3A and B) and one representative
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from the control group (Figs. 3C and D). The model generation process is described as follows. First, the CBCT scan images in DICOM format were used to construct surface models of the mandibles (Fig. 2) that were
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converted to stereolithography (STL) files containing coordinates for the
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triangular facets and vertices.[26] Then the STL files were re-meshed with HyperMesh (Altair Engineering Inc., Auckland, New Zealand) using solid tetrahedral elements to create corresponding volume models (Figs. 2A and C) onto which the material properties were added. For the two FEA models shown in Fig. 3, 20898 nodes (85842 linear tetrahedral elements in total) and 25373 nodes (105585 linear tetrahedral elements in total) were used for Fig. 3B and Fig. 3D, respectively. Mesh convergence studies have been performed for both models to ensure that simulation results are stable based
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ACCEPTED MANUSCRIPT on those mesh densities. Finally, the meshes generated by HyperMesh were imported into Abaqus (Simulia, Providence, RI) to perform stress analysis. Boundary conditions (BCs) were designed to simulate the typical occlusal constraints and muscle responses experienced during mastication and
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parafunctional loading. Displacement and traction BCs were applied onto the mesh in order to compute the deformation and stress states within the mandibles. The zero displacement BC, denoted as Ωd, was applied to the
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working side condyle and canine, simulating canine guidance upon parafunctional loading, while a traction BC, denoted as Ωf, was applied to the
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medial aspect of the contralateral gonial angle, simulating contraction of
r contralateral medial pterigoid muscle (Figs. 3A and C). The force vector, F , acting on Ωf had force components (Fx, Fy, Fz) prescribed as (100N, 0, 100N). It mimics the force exerted by the lateral ptreygoid muscle, and is in line with
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Statistical analysis
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the one described in Schindler et al.[27]
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All radiographic measurements were performed by two trained observers (i.e. dentists with expertise in oral radiology), which were blinded to the presence or absence of tori. Intraobserver reliability was assessed between measurements performed 2 weeks apart to eliminate memory bias. Intra and interobserver agreement were assessed using the intraclass correlations coefficient (ICC) for the CBCT angulations and the kappa test for MCI.
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ACCEPTED MANUSCRIPT Conditional logistic regression were performed using the IBM SPSS Statistics 17 software (SPSS, Inc, Chicago, IL). Risk estimates were presented as odds ratios (ORs) with 95% confidence intervals (CIs). In addition, Mann Whitney test was used to assess angle differences between
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cases and controls. A p value under 0.05 was considered statistically significant.
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Results
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A total of 53 subjects’ CBCT data were initially selected during the study period. Of the twelve subjects identified as having TM, two were excluded due to metabolic bone disease. On the other hand, of the 41 subjects identified as not having TM, four were excluded (three subjects with
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diabetes mellitus and one with metabolic bone desease). As a result, 47 patients (22 men and 25 women, mean age of 54.3 ± 8.4 years) fulfilled the
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inclusion criteria.
reproducibility
and
interobserver
reliability
were
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Intraobserver
confirmed for CBCT angulations (ICC between 0.82 and 0.89, p=0.001), and for mandibular shape and MCI measurements (kappa index between 0.78 and 0.84, P=0.01).
Unlike physiological mastication, parafunctional loading generated a considerable amount of mechanical stress in the mandible (Fig. 3). The largest von Mises stresses were concentrated on the lingual aspect of the
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ACCEPTED MANUSCRIPT mandible in the canine/premolar apical regions, which correspond to the typical site of TM. Stress values were highest in case subjects (See Figs. 3B and D).
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The presence of TM was strongly associated with a square-shaped mandibular arch (Table 1) (OR 26.44, 95% CI 4.39−115.21, P=0.001), a history of parafunctional habits (OR 5.44, 95% CI 1.22−24.04, P=0.046), and
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a normal mandibular cortex (MCI C1) (OR 6.57, 95% CI 1.21−35.43, P=0.030). History of parafunctional habits, however, was not significantly
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associated with a square-shaped mandibular arch (p=.137), or with MCI C1 (p=.524) (Table 2). No significant associations were found between subjects’ age nor gender and the presence of TM.
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To further confirm relationships between mandibular geometry and the presence of TM, the buccal and lingual angles of case and control subjects were analyzed (Figure 4). A statistically significant difference between case
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and control subjects was observed for the buccal angles, a (P=0.007) and c
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(P=0.022), such that these angles were more acute for case subjects. No statistically significant associations were observed between the remaining mandibular angle measurements for the case and control subjects.
Discussion
The present study strove to test the hypothesis that excursive parafunctional stresses would be concentrated in the ridge area where TM
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ACCEPTED MANUSCRIPT usually form. A second hypothesis was that the stress accumulation provided by parafunction could be favored by mandibular. Both hypotheses were confirmed. Additionally, parafunctional activity and mandibular morphology were found to be independent factors influencing TM formation.
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Numerous studies have shown associations between signs of parafunctional activity (i.e. dental attrition and temporomandibular joint dysfunction) and the presence of TM.[5-7] A paucity of evidence, however, is
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available in support of the mechanism behind this association. The results of our investigations confirmed our hypothesis, to wit: unlike physiological
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mastication, parafunctional activity results in the accumulation of mechanical stress in the typical location of TM. In addition, stress accumulates to a greater extent in individuals with TM, suggesting a morphological pattern for these individuals. As a result, our data confirm that parafunctional stress is
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associated with ectopic bone formation in the mandible, offering concrete evidence of the mechanism involved in TM formation.
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Finite element analysis of the case and control mandibles in our study
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revealed that parafunctional loading produced higher levels of mechanical stress in the lingual apical region of the canine/premolar teeth when compared to physiological loading. Interestingly, the focal area of stress concentration corresponded with that of
the typical region of TM
development.[5] Compared to control subjects, case subjects had a more pronounced area of stress concentration in this region for the same force, Ωd, and BCs applied. These findings suggested that subjects with TM possess specific mandibular geometrical conditions, which allow for focal stress
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ACCEPTED MANUSCRIPT concentration (during parafunctional loading) in the typical area of TM formation.
Although direct correlations between high overall BMD and the
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presence of oral tori have been made,[28] our investigation is the first to present the relationship between MCI and the presence of TM. The use of MCI as a surrogate for BMD measurement has previously been validated.[15, Our investigations revealed that subjects with a MCI value of C1 (normal
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16]
mandibular cortex) were associated with the presence of TM, which suggests
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that bone metabolism may play a role in TM formation.
Occlusal forces transmitted to the mandible during mastication follow force
vectors
according
to
the
masticatory
muscles[29]
and
the
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position/angulation of the teeth.[30] Tooth position, however, is largely dictated by the shape of the dental arches, which in turn is affected by the geometric shape of the upper and lower jaws.[14] We quantified the various angulations
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on the buccal and lingual aspects of case and control subjects’ mandibles and
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observed that subjects with TM were associated with sharper, more acute buccal mandibular angulations. To our knowledge, this study is the first to demonstrate that mandibular arch form (i.e. square-shaped) is associated with the presence of TM.
Our results also indicated that mandibular geometry and anatomy (i.e. MCI, angulations, shape) were not influenced significantly by parafunctional activity. This indicates that probably mandibular geometry and parafunctional
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ACCEPTED MANUSCRIPT activity act as synergic independent predisposing factors that are associated with higher risk TM formation. Of the various, albeit poorly understood, factorsenvironmental, genetic, and metabolic believed to play a role in the development of TM, our
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investigations provided evidence for environmental and genetic influences: mechanical stress and mandibular geometry, respectively.[6, 31, 32] Our findings also implicated the involvement of bone metabolism in TM formation, as
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evidenced by the increased risk for the presence of TM in subjects lacking
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erosion of the inferior mandibular cortex (i.e. MCI of C1).
In this study, we used a FEA model meshed from patient’s mandible scan data, which allowed for accurately representing all geometrical aspects of the mandible. Furthermore, by using FEA, it was possible to directly
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visualize the deformation/stress state and distribution within the mandible under different loadings. Coupling the FEA modeling with clinical findings enabled
us
to
better
identify
key
biomechanical
components
and
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subsequently perform targeted clinical tests/characterizations.
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One limitation of our current FEA study is that we employed a simplified description of the mandible material. Consequently, the possible contributions from a) the material heterogeneity and anisotropy and b) differences in material properties due to sex, age and etc., are not captured in the analysis. Furthermore, no quantitative variables were taken from the FEA performed herein. Future studies should address this issue with more refined and targeted FEA analysis.
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ACCEPTED MANUSCRIPT Another limitation of this study is that its case control design allow for detection of associations, but not causality. Future cohort or randomized clinical trials will be needed to address this issue. Furthermore, no direct quantitative evaluation of bone metabolism was performed herein. Therefore,
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further studies on bone turnover would be recommended to assess factors involved in the biochemical etiology of TM.
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The results of our investigations have collectively provided insight into mechanism of TM formation: First, parafunctional activity generates
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mechanical stress on the lingual aspect of the anterior mandible in the typical location of TM. Second, a morphological pattern exists for the mandibular geometry of subjects with TM, whereby stress accumulation is heightened in
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subjects having a square-shaped mandible with sharper buccal angles.
Conclusion
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Parafunctional activity could be causing the formation of TM by
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concentrating mechanical stress in the region where TM usually form. For this reason, mandibular geometries that favor stress concentration, such as square-shaped mandibles, are associated with higher prevalence of TM.
Acknowledgements
A Ph.D. scholarship was granted to Arthur Rodriguez Gonzalez Cortes by the National Council for Scientific and Technological Development (CNPq –
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ACCEPTED MANUSCRIPT Brazil, N° 140291/2011-3). Prof. Faleh Tamimi recei ved grants by The Network for Oral and Bone Health Research (RSBO, Quebec, Canada F'ODQ/RSBO x-coded 217031) and by the Natural Sciences and Engineering Research Council of Canada (NSERC RGPIN 418617-12). Dr. Jun Song also
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received grants by Natural Sciences and Engineering Research Council of Canada (NSERC Engage EGP 445930-12). The authors declare that there are no conflicts of interest in this study. Approval was granted from the ethics
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committee of the School of Dentistry, University of São Paulo, São Paulo,
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Brazil (Protocol N105/11).
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1. Hassan KS, Alagl AS, Abdel-Hady A: Torus mandibularis bone chips combined with platelet rich plasma gel for treatment of intrabony osseous defects: clinical and radiographic evaluation. Int J Oral Maxillofac Surg 2012;41:1519 2. Brunsvold MA, Kaiser DA, Faner RM: Recurrence of mandibular tori after surgical removal: two case reports. Journal of prosthodontics : official journal of the American College of Prosthodontists 1995;4:164 3. Garcia-Garcia AS, Martinez-Gonzalez J-M, Gomez-Font R et al.: Current status of the torus palatinus and torus mandibularis. Medicina Oral Patologia Oral Y Cirugia Bucal 2010;15:E353 4. Pynn BR, Kurys-Kos NS, Walker DA, Mayhall JT: Tori mandibularis: a case report and review of the literature. Journal (Canadian Dental Association) 1995;61:1057 5. Eggen S: Correlated characteristics of the jaws: association between torus mandibularis and marginal alveolar bone height. Acta Odontologica Scandinavica 1992;50:1 6. Morrison MD, Tamimi F: Oral tori are associated with local mechanical and systemic factors: a case-control study. J Oral Maxillofac Surg 2013;71:14 7. Al-Bayaty HF, Murti PR, Matthews R, Gupta PC: An epidemiological study of tori among 667 dental outpatients in Trinidad & Tobago, West Indies. International Dental Journal 2001;51:300 8. Sirirungrojying S, Kerdpon D, Songkhla H: Relationship between oral tori and temporomandibular disorders. International Dental Journal 1999;49:101 9. Frost HM: Emerging views about "osteoporosis", bone health, strength, fragility, and their determinants. Journal of Bone and Mineral Metabolism 2002;20:319 10. Frost HM: A 2003 update of bone physiology and Wolff's Law for clinicians. Angle Orthodontist 2004;74:3 11. Jiang YB, Zhao J, Rosen C et al.: Perspectives on bone mechanical properties and adaptive response to mechanical challenge. Journal of Clinical Densitometry 1999;2:423 12. Felson DT, Zhang YQ, Hannan MT, Anderson JJ: Effects of weight and body mass index on bone mineral density in men and women: the Framingham study. Journal of Bone and Mineral Research 1993;8:567 13. Frost HM: Bone's mechanostat: A 2003 update. Anatomical Record Part a-Discoveries in Molecular Cellular and Evolutionary Biology 2003;275A:1081 14. Kumabe S, Nakatsuka M, Iwai-Liao Y et al.: Morphological classification of mandibular dental arch forms by correlation and principal component analyses. Okajimas Folia Anat Jpn 2005;82:67 15. Klemetti E, Kolmakov S, Heiskanen P et al.: Panoramic mandibular index and bone mineral densities in postmenopausal women. Oral Surgery Oral Medicine Oral Pathology Oral Radiology and Endodontics 1993;75:774 16. Leite AF, Figueiredo PTD, Barra FR et al.: Relationships between mandibular cortical indexes, bone mineral density, and osteoporotic fractures in Brazilian men over 60 years old. Oral Surgery Oral Medicine Oral Pathology Oral Radiology and Endodontology 2011;112:648
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17. von Mises R: Mechanik der festen Körper im plastisch- deformablen Zustand. Nachrichten von der Gesellschaft der Wissenschaften zu Göttingen, Mathematisch-Physikalische Klasse 1913;1913:582 18. Wong RC, Tideman H, Kin L, Merkx MA: Biomechanics of mandibular reconstruction: a review. International journal of oral and maxillofacial surgery 2010;39:313 19. Choi AH, Ben-Nissan B, Conway RC: Three-dimensional modelling and finite element analysis of the human mandible during clenching. Australian dental journal 2005;50:42 20. Meyer U, Vollmer D, Homann C et al.: [Experimental and finite-element models for the assessment of mandibular deformation under mechanical loading]. Mund-, Kiefer- und Gesichtschirurgie : MKG 2000;4:14 21. Vollmer D, Meyer U, Joos U et al.: Experimental and finite element study of a human mandible. Journal of cranio-maxillo-facial surgery : official publication of the European Association for Cranio-Maxillo-Facial Surgery 2000;28:91 22. Dechow PC, Hylander WL: Elastic properties and masticatory bone stress in the macaque mandible. American journal of physical anthropology 2000;112:553 23. Dechow PC, Nail GA, Schwartz-Dabney CL, Ashman RB: Elastic properties of human supraorbital and mandibular bone. American journal of physical anthropology 1993;90:291 24. Fernandez JR, Gallas M, Burguera M, Viano JM: A three-dimensional numerical simulation of mandible fracture reduction with screwed miniplates. Journal of Biomechanics 2003;36:329 25. Kim HS, Park JY, Kim NE et al.: Finite element modeling technique for predicting mechanical behaviors on mandible bone during mastication. Journal of Advanced Prosthodontics 2012;4:218 26. Szilvasi-Nagy M, Matyasi G: Analysis of STL files. Mathematical and Computer Modelling 2003;38:945 27. Schindler HJ, Rues S, Turp JC, Lenz J: Heterogeneous activation of the medial pterygoid muscle during simulated clenching. Archives of Oral Biology 2006;51:498 28. Hjertstedt J, Burns EA, Fleming R et al.: Mandibular and palatal tori, bone mineral density, and salivary cortisol in community-dwelling elderly men and women. Journals of Gerontology Series a-Biological Sciences and Medical Sciences 2001;56:M731 29. Grunheid T, Langenbach GE, Korfage JA et al.: The adaptive response of jaw muscles to varying functional demands. Eur J Orthod 2009;31:596 30. Zhang M, Chen FM, Chen YJ et al.: Photoelastic Analysis of the Effects of Tooth Position on Apical Stress. Experimental Mechanics 2011;51:1135 31. Haugen LK: Palatine and mandibular tori. A morphologic study in the current Norwegian population. Acta Odontol Scand 1992;50:65 32. Seah YH: Torus palatinus and torus mandibularis: a review of the literature. Aust Dent J 1995;40:318
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ACCEPTED MANUSCRIPT Figure Legends Figure 1. Schematic 3D presentation of the buccal (A) and lingual (B) mandibular angles.
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Figure 2. Surface models (isotropic and axial views) of a mandible with TM (A and C) and a mandible without TM (B and D). Abbreviations: TM, tori mandibularis.
M AN U
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Figure 3. Boundary conditions applied during FEA simulations on a mandible with TM (A) and a mandible without TM (C), where Ωd and Ωf denote the displacement and traction boundary conditions, respectively. The force components of Ωf are shown for their respective Cartesian coordinates as Fx, Fy, and Fz. The corresponding von Mises stress fields (σ) for the forces applied are depicted by color mapping for the mandible with TM (B) and the mandible without TM (D). Abbreviations: TM, tori mandibularis.
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Figure 4. Axial computed tomography views for a mandible with TM (A) and a mandible without TM (B). The inset image in A shows more clearly the pronounced TM bilaterally. *Statistically significant (P 60 years
19
03
0.40 (0.09-1.82)
Female
22
03
1
Male
15
07
3.42 (0.76-15.38)
Round
34
03
1
Square
03
07
26.44 (4.39-115.21)
Eroded cortex (C2-C3)
23
02
SC
Characteristics
1
Normal cortex (C1)
14
08
6.57 (1.21-35.43)
04
1
06
5.44 (1.22-24.04)
P value
Age
Mandibular arch shape
History of parafunctional habits No
29
Yes
08
M AN U
MCI
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Gender
0.297
0.154
0.001*
0.030*
0.046*
AC C
EP
TE D
*Statistically significant (P
