Relationship Between Articular Eminence Inclination and Alterations of The Mandibular Condyle: A CBCT Study
Relationship Between Articular Eminence Inclination and Alterations of The Mandibular Condyle: A CBCT Study
Relationship Between Articular Eminence Inclination and Alterations of The Mandibular Condyle: A CBCT Study
Imaginology
Saione Cruz SA(a) Abstract: This study aimed at verifying the correlation among
Saulo Leonardo Sousa MELO(b) angulation of the articular eminence (AE), shape of the condyle and
Daniela Pita de MELO(c)
Deborah Queiroz FREITAS(a) its degenerative bone diseases (DBDs), according to age and sex,
Paulo Sérgio Flores CAMPOS(d) through Cone Beam Computed Tomography (CBCT). Five hundred
and twenty-eight temporomandibular joints (TMJ) were evaluated. The
condyles were classified as: flat, convex, angled and rounded, and the
Universidade de Campinas – Unicamp,
(a) AE angulation was measured. The DBDs evaluated were osteophytes,
Piracicaba Dental School, Department of flattening, erosion, subcortical cysts and spinal sclerosis. There was no
Oral Diagnosis, Oral Radiology, Piracicaba,
difference in the mean angulations in relation to age group (p>0.05).
SP, Brazil.
In age groups of 60-69 years (p=0.003) and 70 years or over (p=0.021),
University of Iowa College of Dentistry, Oral
(b)
the angulation was higher in males. There was an association between
Pathology, Radiology and Medicine, Iowa
City, IA, USA. DBD and sex (p=0.047), in that the prevalence was higher in females.
Differences in AE angles were not observed in condyles with one or
Universidade Estadual da Paraíba – UEPB,
(c)
Department of Oral Diagnosis, Oral no DBDs (p>0.05). However, the presence of two or more DBDs led to
Radiology, Campina Grande, PB, Brazil. a decrease in the angle (p<0.05). Angled condyles showed higher AE
Universidade Federal da Bahia – UFBA,
(d) angulations than the flat and convex types (p<0.01). In conclusion, the
Department of Oral Diagnosis, Oral AE inclination is influenced by DBD and condyle shape; an association
Radiology, Salvador, BA, Brazil.
of two or more bone diseases in the condyle, or its flat or convex
anatomy, results in a decrease in the angulation.
Introduction
Corresponding Author: In the opening and closing movements of the mouth, the condyle
Deborah Queiroz Freitas and the articular disc complex slide under the articular eminence (AE).
E-mail: [email protected]
The morphology of the AE enables this movement to flow naturally;
it varies among individuals, and may change according to age, sex and
masticatory function.1,2,3,4,5 The morphology of the bone components of
http://doi.org/10.1590/1807-3107BOR-2017.vol31.0025
the temporomandibular joint (TMJ) has been used to explain the origin of
internal disorders and bone alterations according to the functional load
in this area, as well as factors such as age and sex of the individual.6,7,8
The AE inclination constitutes an important element in the biomechanics
of the TMJ, as well as the entire masticatory system, defined as the angle
Submitted: Sep 01, 2016
between the posterior wall of the AE and a horizontal reference plane.4,9
Accepted for publication: Feb 13, 2017
Last revision: Mar 03, 2017 This inclination can be measured in degrees, with normal values between
30º and 60º.10 AEs below 30º are classified as flat and above 60º, as steep9,
and both classifications seem linked to internal we associated these data with age and sex, based on
articulation disorders. These disorders may lead CBCT images.
to degenerative bone diseases (DBDs) in both the
condyle and the AE.10 Methodology
Articular bone diseases in the condyle may lead to
adjustments in the AE inclination, as reported in some Sample selection
studies that have found joints with osteoarthritis to This was a retrospective cross-sectional study.
have more flat eminences.7 Therefore, condyles with It was previously approved by the local Ethics
changes such as erosions, flattening, osteophytes, Committee on Human Research (Protocol # 989172).
subchondral cysts and bone sclerosis may be correlated Two hundred and sixtyfour CBCT images of the
with less steep eminences, as a result of the close maxillae of adult patients ages 20 to 82 years (mean age:
relation between these two structures.11 50.9; standard deviation: 12.68) were selected, resulting
Aside from being susceptible to DBDs, condyles in 528 TMJs. The patients comprised 184 females (mean
may have varied morphology, which will influence age: 50.8; standard deviation: 12.7) and 80 males (mean
the shape of the AE. Yale et al.12,13,14 developed a age: 51.2; standard deviation: 12.5). The images were
classification of condyle types, according to the selected by a single radiologist, in a private clinic,
from exams acquired between 12/2012 and 03/2014.
wide variations in the shape of the top surface: flat,
The following inclusion criteria was observed: TMJs
convex, angled, rounded. A previous study found
had to be completely visible bilaterally; patients had to
that the AE inclination values are higher in joints
have all posterior teeth and could not present with any
without bone alterations than in joints with bone
types of conditions, such as developmental disorders,
alterations.7 On the other hand, another study using
fractures, anomalies, tumors or ankylosis in the region
the classification by Yale et al.13 found a greater mean
evaluated in the CBCT exams.
value of AE inclination in males than in females,
The CBCT exams were carried out on an i-CAT
whereas no relation was found among factors of
scanner with 120kV and 3-8 mA (Imaging Sciences
AE inclination, floor thickness of the mandibular
International, Inc., Hatfield, USA), according to the
fossa (FM) and the condyle morphology.8
protocol for the maxilla, 0.2mm voxel, FOV (field of
Because of its three-dimensional complexity, the
view) of 16x6cm and 40 seconds of acquisition time.
TMJ cannot be accurately evaluated by images that
overlap.3,6 Currently, CBCT is the imaging modality of
Image evaluation
choice to investigate bone alterations of the TMJ, since The images were analyzed using Xoran® software
it is possible to obtain sections of this structure on (Xoran Technologies LLC, Ann Arbor, MI, USA) in a
several levels.6,15,16,17,18 Accordingly, the morphology of the Eizo® S2100 (Eizo, Cypress, CA, USA), 21.3” monitor,
osseous joint components, cortical bone integrity, and at a resolution of 1280x1024 pixels.
subcortical bone changes can be viewed using CBCT. The standard positioning of the images was
Further elucidation of the anatomy of structures, performed by the researcher before the measurements
as well as the alterations of their functions and the were made by the examiners. The images were
relationship of these structures with external factors, placed in a standard position in the multiplanar
is necessary to better address the morphological reconstruction (MPR), so that all the slices were
differences of TMJ bone components and the made according to the correct positioning of the
controversial relationship between AE inclination and patient’s head.
condyle morphology, aspects that can be assessed more In the axial section, the patient’s sagittal median
easily by today’s modern diagnostic methods. To this plane (SMP) was aligned with the vertical reference
end, the present study aimed mainly at analyzing the line. In the sagittal section, the hard palate was
correlation among factors of AE angulation, condyle positioned so that the researcher could see the anterior
shape and the alterations in both. Additionally, nasal spine (ANS) and the posterior nasal spine
(PNS), and was then tilted to overlap the horizontal which is a line parallel to the palatine plane). The lines
reference line. Accordingly, the palatine plane (PP) were obtained with Xoran® software tools (Figure 2).
was at 0° to the reference horizontal plane of the Second analysis: To classify the condyle shape seen
slice. Afterwards, the TMJ tool on the software was on the coronal slices, according to the Yale et al. (1966)
used to perform paracoronal and parasagittal slices classification (types A – flat, B – convex, C – angled,
(1 mm thick) of the condyle. The paracoronal slices D - rounded). The examiners used a template (Figure 3)
were made along the long axis of the condyle, and developed with Inkscape software (Open Source
the parasagittal slices were made perpendicular to Software licensed under the GPL., Vs. 0.91) to perform
the paracoronal plane (Figure 1). this evaluation. The shapes that did not fit any of the
Afterwards, two radiologists with over 5 years types (A, B, C or D) were classified as type E.
of experience in diagnosing CBCT evaluated the Third analysis: The DBDs were evaluated in
images individually. As part of their training, each parasagittal slices of condyle (1mm thick), using
examiner received verbal and written instructions the TMJ tool to determine whether the condyles
on how to measure and evaluate each image. Some were normal (no change) or abnormal (when any of
50 images that were not part of the sample of 528 the following changes were detected: osteophytes,
images were used at the time of the instructions to flattening, erosion, subcortical cysts and spinal
train each examiner’s evaluation skills. After being sclerosis) (Figure 4).
instructed and calibrated, the examiners worked
independently in a dark quiet environment. Statistical analysis
Both examiners carried out three analyses of The normality of data was initially checked using
each TMJ: AE angulation, shape of condyle and the Kolmogorov-Smirnov test to determine the ordinal
presence of any DBDs, and recorded the information variable (AEA, expressed as mean ± standard error
individually. Later, the examiners’ responses were of the mean). Once the Gaussian distribution of
compared. In case of disagreement, the final diagnosis the data was obtained, the comparison of mean
was made by consensus between them. values between the two groups was performed using
First analysis: Performed in a parasagittal slice Student’s ttest. Comparison of the mean values among
from the center of the condyle (1 mm thick), using
the TMJ tool to observe the articular eminence angle
(AEA), formed by the internal angle between line 1
(connecting the articular eminence vertex and the
mandibular fossa vertex) and line 2 (formed by PP’,
A B C D
three or more groups was performed by analysis of However, the proximity of the p value obtained for
variance (ANOVA test), followed by Tukey’s multiple males to the threshold value (0.05), and the analysis
comparison test. The linear regression test was used of graphical data distribution, suggest a trend toward
to perform the analysis of correlation between the increased mean AE angulation with the aging of the
ordinal variables, applying the Pearson correlation individuals. The linear regression test was performed
coefficient. The chi-square test was used to analyze between the ages of the individuals and their AE
possible associations between the categorical variables angulation to confirm this trend. In fact, although the
(expressed as absolute and relative frequency). In all the correlation observed (by a positive trend line) between
cases, the differences were taken as significant when the variables in the males (r = 0.156) was weak, it was
the p value was less than 0.05. Statistical analysis was considered significant (p = 0.048). On the other hand,
performed using GraphPad Prism software, version 5.0. the correlation between the variables in the females
was too weak (r = 0.062) to be significant (p = 0.228).
Results Stratification of the mean angulations according to
the different age groups to compare the AE angulation
There was no significant difference in mean AE between the sexes, as shown in Table 1, indicated
angulation according to the age of the individuals, that only in older age groups (60 and over) was this
either in the females (p = 0.136) or the males (p = 0.065), measurement significantly higher in males than in
as seen in Figure 5. females (p < 0.05).
A B C D E F
Figure 4. Degenerative bone diseases: A - osteophytes, B - flattening, C - erosion, D - subcortical cysts, E - spinal sclerosis,
F - combination of two pathological changes (osteophytes and erosion).
A B
50 Males 50 Females
Angulation of the articular eminence (°)
40 40
30 30
20 20
10 10
0 0
20-29 30-39 40-49 50-59 60-69 70 or older 20-29 30-39 40-49 50-59 60-69 70 or older
Years old Years old
Figure 5. Mean AE angulation of males and females, according to the age groups. One-way ANOVA indicated no difference
between the age decades (p = 0.065 and 0.136, respectively).
When comparing the sides, there was no significant with DBD or without the alterations under study
difference in AE angulation degree between the right (p > 0.05), as shown in Figure 6. However, the
and left sides according to Student’s t test (p = 0.213). combination of two or more pathological changes
It was observed that 47.7% of the condyles studied in the condyle was especially interesting, since
had DBDs. There was no significant association it caused a reduction in mean AE angulations
(p = 0.663) between frequency of these changes and (p < 0.01) which did not differ from the isolated
the affected side (Table 2), but there was a significant DBD, regardless of type.
association (p = 0.0472) between these changes and Considering the morphology of the AE in the
the sex of the subjects (Table 3). individuals assessed, it was observed that 58.5%
Flattening was the most frequent change observed of the cases (309) were type A, 9.5% (50 cases) type
in the condyles (153 cases, corresponding to 60.7%), B, 8.7% (46 cases) type C, 18.0% (95 cases) type D,
followed by osteophytes (122 cases, representing 48.4%) and 5.3% (28 cases) type E. When comparing the
and subcortical cysts (33 cases, representing 13.1%). means of AE angulations in relation to these different
There were only 19 cases of erosion (7.5%), 6 cases of condyle morphological patterns (Figure 7), it was
sclerosis (2.3%) and 2 of free bodies (0.8%). However, observed that the mean of type C condyles (angled) was
it is noteworthy that combinations of two or more significantly greater than type A (flat) and B condyles
DBDs were observed in 93 cases (17.6%). (convex) (p < 0.01). The comparison between the other
No significant differences were observed between types revealed no significant differences in mean AE
the means of AE angulations and condyles either angulations (p > 0.05).
50
Angulation of the articular eminence (°)
statistical analysis already considers and weighs these Observing the morphological patterns of the
differences to evaluate a possible association with condyles and their relationship to mean AE angulation,
factors such as sex. Therefore, the results are reliable the differences were between angled condyles,
and the difference in the distribution of individuals which presented higher mean angulations than flat
in both groups had no effect on the results. and convex condyles. When the authors analyzed
Alterations in the condyles did not affect the AE the anatomic shape of each type of condyle, it was
angulations. However, when two or more bone changes expected that the angled form would be related to
were present in the condyles, an average reduction in higher angulation, since this type is apparently more
AE angulation was observed, probably because two voluminous than the others, especially more than the
or more bone changes cause more severe alterations. flat and convex types, as verified by imaging analysis.
Estomaguio et al.2 reported a similar correlation when However, a previous study found no correlation
they studied 59 patients, 39 with and 20 without bone between condyle morphology and AE angulation.8
changes, stating that AE angulation in patients with It is noteworthy that important methodological
bone change was significantly lower than in patients differences between the studies, such as number of
without bone change. However, the authors did not evaluators and sample size, may have contributed
specify if there was more than one bone alteration in to such divergent results.
the condyle. Similarly, Çağlayan et al.7 reported that the The main clinical contributions offered by this
value of AE angulation in TMJs without dysfunction study to the professionals of the field regard the
was higher than in TMJs with dysfunction, but no relationship between the AE angulation and the
statistically significant difference was verified. condyle, given its importance in TMJ biomechanics.
In regard to the bone changes in the condyle, females They should be well-enough informed to know that
have been found to have more. In a sample similar to this inclination is influenced by DBD and by the
that of the present study (randomized subjects at a condyle shape, considering that an association of
time interval), Estomaguio et al.2 also observed more two or more bone diseases in the condyle, or its flat
women with (66.1%) than without (33.8%) DBD. or convex anatomy, decreases the angulation.
Regarding the morphology of the condyle according
to the classification by Yale et al.,13 the present Conclusion
study found that most of the condyles presented
flat morphology, in contrast to Yale et al.,13 who The presence of two or more bone diseases in
observed angled morphology to be more prevalent the condyle results in a reduction in AE angulation.
(43%) in pre-Hispanic populations, and convex types, Moreover, the shape of the condyle influences the AE
more prevalent in Caucasians (50.2%) and blacks (72%), inclination, seeing that the angled condyle is associated
in their sample of European patients. It is noteworthy with higher AE angulation than the flat and convex
that 28.9% of the condyles in our sample presented types. Additionally, the AE angulation is not influenced
flattening, namely that of the upper portion, which by age, but is influenced by the sex, seeing that it is
may have resulted in the higher prevalence of flattened higher in males over 60 years old. Concerning DBDs,
shapes in the sample. their propensity is greater among females.
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