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Article history: Aim: To compare the craniocervical angles and distances between temporomandibular
Accepted 6 June 2010 dysfunction (TMD) and free TMD subjects.
Casuistic and methods: The sample consisted of young adults, of both genders, with age
Keywords: ranging between 18 and 30 years. TMD diagnosis was based on the clinical criteria of the
Temporomandibular joint Research Diagnostic Criteria for TMD (RDC/TMD), associated with self-reported symptoms
dysfunction syndrome of TMD. For radiological analysis we measured three angles and two distances of cranio-
Craniocervical posture cervical region.
Radiograph Results: Of the 56 subjects, only 23 completed all stages of research, which were divided into
two groups: (1) free TMD group composed of 11 individuals; (2) TMD group constituted of
12 subjects. The most common clinical diagnosis of TMD was arthralgia (75.0%) followed by
myofascial pain without limited mouth opening (58.4%). Among the self-reported symp-
toms of TMD, the most frequents were facial (83.4%) and neck (66.6%) pain. Of radiological
measurement, only plane atlas angle (APA) ( p = 0.026) and anterior translation distance (Tz
C2C7) ( p = 0.045) showed statistical difference between groups TMD (APA = 16.7 1.63; Tz
C2C7 = 28.7 2.58) and free TMD (APA = 21.64 1.24; Tz C2C7 = 19.82 3.29).
Conclusion: It could be verified that the symptomatic TMD patients presented a flexion of the
first cervical vertebra associated with an anteriorization of the cervical spine (hyperlordosis).
# 2010 Elsevier Ltd. All rights reserved.
* Corresponding author at: Departamento de Fisiologia, Centro de Ciencias Biologicas e da Saude, Universidade Federal de Sergipe, 49100-
000, SE, Brazil. Tel.: +55 79 2105 6645; fax: +55 79 2105 6494.
E-mail address: lbonjardim@yahoo.com.br (L.R. Bonjardim).
00039969/$ see front matter # 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.archoralbio.2010.06.002
archives of oral biology 55 (2010) 670678 671
2.1. Sample The radiographs were taken in a Radiology Clinic from Aracaju,
Sergipe, Brazil by the same technician (in all exams), previously
The sample consisted of subjects of both genders, aged trained and calibrated by the investigator. The technician was
between 18 and 30 years recruited from the Federal blinded to each group. To have a radiograph taken of the cervical
University of Sergipe who had voluntarily attended in the spine, the subjects were positioned between the X-ray source
Laboratory of Orofacial Pain (UFS) between April 2008 and and the film, in the sagittal plane parallel to the plane of the film,
September 2009. Exclusion criteria were subjects with no barefooted, with feet placed together, in orthostatic posture,
physical or cognitive conditions to answer the questionnaire and instructed to look at the horizon, with the head in the rest
or to be evaluated to detect signs and symptoms of TMD, who position, which is highly reproducible in the literature.3739
had undergone any previous spinal and orthodontic treat- Whereas the type of imaging technique was static radiograph,
ment, with malocclusion, craniocervical anomalies, any subjects remained immovable until the radiographic examina-
previous direct or surgical injuries in the orofacial region, tion was completed. For this, all volunteers were oriented to not
systemic or degenerative diseases and who decided to not move their head or other parts of body throughout the
participate in the research. radiographic examination, which was supervised by the
Subjects gave written consent to participate in the study. technician who was previously calibrated by the examiner.
The study was conducted in accordance with the current good Moreover, to ensure consistent magnification and to minimize
clinical practice guidelines and it was approved by the Ethics head and body posture recording errors, the same operator,
Committee of the Federal University of Sergipe. using the same X-ray machine, exposed all standardized
672 archives of oral biology 55 (2010) 670678
radiographs for the subjects in the study. These rules were C2. The intersection of the two tracings forms an angle that
implemented with the intention of allowing reproducibility of measures the extension degree of the head on the high
the exam and minimize possible dynamic influences of the cervical spine; so, the greater HCA the greater will be the
head and neck position, which could alter the final result of the head flexion on the cervical spine.
exam. It is worth pointing out that the distance between the X- - Low cervical angle (LCA) (odontoid angle C3/C4)14: The LCA
ray source and the radiographic film was standardized at is traced from a line tangent to the vertebral bodies of the
180 cm, in accordance with the procedure of the above- third and fourth cervical vertebrae (C3C4) by two distinct
mentioned clinic. points. The highest point of the posterior surface of the
After taking the radiographs, as a standardization proce- vertebral body of C3 and the lowest point of the posterior
dure, the following points were determined: posterior nasal surface of the vertebral body of C4, its intersection with the
spine, inferior nuchal line of the occipital bone, posterior tracing also made in HCA (posterior nasal spine up to the
surface of the odontoid apophysis, posterior surface (superior most inferior surface of the occipital bone line) forms an
and inferior) of the vertebral bodies of C2, C3, C4 and C7, inferior angle that indicates the relationship between the high and
arch of C1 and mid-point of the posterior superior tubercle of low cervical spine; that is, the greater LCA the greater the
C1 (Fig. 1). cervical lordosis and the greater the extension of the high
Subsequently, the above-mentioned points had been cervical spine on the low cervical spine.
demarcated, three angles and two distances of craniocervical - Atlas plane angle (APA): It represents the plane of the atlas
posture were measured. The methodology of the specific vertebra (C1) and its radiographic tracing was made
radiographic tracings of each angle and each distance, as well between a line parallel to the horizontal and another line
as their applicability is described as follow: (Fig. 2): traced in the inferior part of the anterior and posterior ring
of the atlas. The increase in APA suggests an increase in
- High cervical angle (HCA) (odontoidcranial base angle) high cervical (extension of C1) and its reduction, a reflection
described by Huggare and Raustia14: Posterior nasal spine up or rectification.32
to the most inferior surface of the occipital bone line; line - The anterior translation distance: This was measured in
[(Fig._1)TD$IG] tangent to the posterior surface of the odontoid apophysis of millimetres and its tracing was made by means of the
distance between the posterior superior edge of the vertebral
body of C2 and a vertical line perpendicular to the inferior
edge of the vertebral body of C7.32,34 This measurement was
important for determining a mean value for the anterior
transport of the head, and this posture was clinically
relevant because it causes a retraction of the neck muscles.40
- Occipitalatlas distance (OAD): This was measured in
millimeters between the following two points: the lowest
point of the surface of the occipital bone line and the
posterior ring of the atlas. The normal value was between 4
and 9 mm, a distance of less than 4 mm suggests a posterior
rotation of the occipital bone and a distance exceeding 9 mm
suggests an anterior rotation of the occipital bone.23,31
Fig. 2 Illustrative diagram of the radiographic measurements. 1 High cervical angle, 2 low cervical angle, 3 atlas plane
angle, anterior translation distance (Tz C2/C7), 4 occipitalatlas distance.
groups and, finally, craniocervical distances and angles, which The Free TMD group was formed by four men (mean age of
were compared between TMD and free TMD groups. 19 years; mean BMI of 29.7 kg/m2) and seven women (mean
After the initial evaluation of 56 subjects, 11 were age of 20.6; mean BMI of 19.9 kg/m2). The TMD group consisted
diagnosed as free TMD and 45 with clinical diagnosis of of five men (mean age of 24 years; mean BMI of 24.8 kg/m2) and
TMD according to the criteria of RDC/TMD. From 45 subjects seven women (mean age of 21.4; mean BMI of 24 kg/m2).
diagnosed with TMD, four were excluded due to a clinical Regarding to educational level and marital status, 20 subjects
diagnosis of osteoarthrosis and osteoarthritis, which could not had completed high school and 21 were single (Table 1).
be confirmed radiographically. These 41 remaining subjects Formation of the groups in accordance with the differences
were referred for radiologic examination, but only 21 attended diagnoses of TMD according to the RDC/DTM criteria and with
for the exam. From 21 radiologic procedures, only 12 were the presence of subjective symptoms is shown in Table 2. It can
considered in this study. The rest of them presented lack of be verified that the subjects in the free TMD group presented no
precision in identifying anatomical points due to lack of clinical or anamnestic diagnose for TMD. On the other side, the
sharpness in the exam, which avoided errors and mistakes in TMD group presented at least one of the different diagnoses of
measuring craniocervical angles and distances (Fig. 3). RDC/TMD; in addition the subjects of TMD group reported a
The subjects were divided into two groups: minimum of three subjective symptoms. Diagnoses of arthral-
gia (n = 9) and myofascial pain without limited mouth opening
- Free TMD group: This group was composed of 11 subjects (n = 7) were the most frequent among the diagnoses of TMD
with no TMD according to RDC/TMD criteria and no according to RDC/TMD. It is pointed out that according to RDC/
subjective symptoms reported. The mean age was 20.0 TMD the same individual could be diagnosed in more than one
years old. subgroup of TMD. Among the self-reported symptoms, the most
- TMD group: This group was composed of 12 subjects with frequent was facial pain which affected 10 individuals, and the
muscular and/or articular TMD based on RDC/TMD criteria least frequent was tiredness when chewing, together with
and at least three subjective symptoms of TMD. The mean malocclusion self-perception, which affected two individuals.
age was 22.5 years old. The mean number of symptoms reported was 5.3.
674 archives of oral biology 55 (2010) 670678
[(Fig._3)TD$IG]
Fig. 3 Flow diagram of the subjects progress through the phases of randomized clinical trial.
The craniocervical angles (8) and distances (mm) measured The anterior translation distance (Tz C2/C7) (Fig. 5) was also
by profile radiography (sagittal plane), between subjects with statistically different ( p = 0.045) between the groups, however
and without diagnosis of TMD are shown in Figs. 4 and 5. the mean values in TMD group (28.7 8.95) was higher than
No statistical difference (HCA p = 0.378; LCA p = 0.686; free TMD group (19.82 10.93).
OAD p = 0.877) was found between subjects of free TMD
group (HCA 85.68 7.44; LCA 10.36 6.20; OAD
7.82 1.54) and TMD group (HCA 82.90 7.28; LCA 6. Discussion
9.3 5.93; OAD 7.6 4.74) for high and low cervical angles
(HCA and LCA) and for occipitalatlas distance (OAD). The aim of this study was to evaluate the possible alterations
The atlas plane angle measurement (Fig. 4) was statistically in craniocervical posture, in the sagittal plane, in patients with
different ( p = 0.026), with the mean values in the TMD group TMD. It has been discussed in scientific literature this
(16.7 5.65) lower than the free TMD group (21.64 4.10). relationship for years.1217,22 However, in a recent systematic
Table 1 Characterization of the sample according to age, body mass index (BMI), educational level and marital status.
Men (n) Women (n) Total (n) Men (n) Women (n) Total (n)
Educational level
High school 4 6 10 3 7 10
College 0 1 1 2 0 2
Marital status
Single 4 7 11 5 5 10
Married 0 0 0 0 2 2
archives of oral biology 55 (2010) 670678 675
Table 2 Formation of the groups according to the different diagnoses of TMD based on RDC/TMD criteria and with the
presence of subjective symptoms of TMD.
Free TMD group TMD group
n % n %
Symptoms
Facial pain? 0 0 10 83.4
Difficulty in mouth opening? 0 0 4 33.4
Difficulty to move the mandible? 0 0 3 25.0
Tiredness when chewing? 0 0 2 16.6
Headache? 0 0 7 58.4
Neck pain? 0 0 8 66.6
TMJ pain? 0 0 6 50.0
Joint sounds when chewing? 0 0 5 41.6
Tooth grinding or clenching? 0 0 6 50.0
Malocclusion self-perception? 0 0 2 16.6
Associated symptoms
3 0 0 4 33.4
5 0 0 3 25.0
>3 and <5 0 0 5 41.6
RDC/TMD diagnoses
Ia myofascial pain without limited opening 0 0 7 58.4
Ib myofascial pain with limited opening 0 0 5 41.6
IIa displaced disc with reduction 0 0 3 25.0
IIIa arthralgia 0 0 9 75.0
IIIb osteoarthritis 0 0 6 50.0
review article, Olivo et al.28 reported 12 articles that estab- allowing a more complete and precise evaluation of this
lished a correlation between TMD and craniocervical altera- dysfunction. Bonjardim et al.9 reported the importance of
tions in accordance with their inclusion criteria, and, seven evaluating the association between clinical diagnosis and self-
from them found significant relationship. All 12 articles were reported symptoms for better assessment of TMD. For the
considered poor in their methodological design and insuffi- clinical evaluation the Research Diagnostic Criteria instru-
cient to provide support for their results. Furthermore, the ment29 (RDC/TMD) was used, which is considered the gold
authors mentioned that the absence of control group, poor standard for the diagnosis of TMD, accepted and validated in
diagnostic criteria for TMD (9 of the 12 studies used clinical several languages. This clinical exam was associated with the
signs, such as clicking and pain on muscular palpation, as presence of subjective symptoms of TMD as proposed by Conti
diagnostic tools), and for craniocervical alterations (the et al.30
studies used different ways to evaluate craniocervical pos- In addition, we used for the evaluation of the craniocervi-
ture-only two studies used radiographs), were the main cal angles and distances, the measures described in studies
failures of the studies. with TMD subjects and those ones for the diagnosis of
The present study evaluated the relationship of TMD with morphological alterations of the cervical spine (posture), of
craniocervical posture alterations. The diagnosis of TMD was great importance in the clinic.14,32,34 An important fact in this
based on clinical and anamnestic criteria with the intention of study concerns the use of radiographic measurements, which
[(Fig._4)TD$IG] were able to evaluate, in a quantitative and faithful manner,
the morphology of the craniocervical posture, as opposed to
the computerized posturograms and postural evaluations.
These other techniques present some interferences, such as
photographic distortions and variability in the anatomical
markings, which may slide on the skin, being factors of bias in
the work, thus showing to be less reliable.41 Although, the
radiographic measurement appears to be the gold standard
and reliable tool to evaluate craniocervical posture, lack of
precision in identifying anatomical points in radiograph has a
limitation that may occur in the exam.42 For example, due to
lack of sharpness, it can interfere significantly in the
reproducibility of measurements. This difficulty occurred
in the present study in 9 from 32 radiographs, so the
Fig. 4 Mean values for atlas plane angle between the examiner, who was always the same in all radiographic
groups. Each column represents the mean W SEM. measurements, only assessed the radiograph when there was
*p = 0.026, t test, indicates a significant decrease in total precision of visualization and interpretation of anatom-
relation to free TMD group. ic points to be marked in the film, trying to avoid mistakes and
676 archives of oral biology 55 (2010) 670678
[(Fig._5)TD$IG]
et al.,16 who found an increase in cervical curvature,
suggesting a hyperlordosis, but no corroborate with the
findings of Rocabado and Tapia,23 Rego Farias et al.,24 Dattilio
et al.,17 and Araujo22 who, in spite of using another measure-
ment (the craniocervical angle) verified the presence of
rectification of the cervical spine. One of the main forms of
compensation during the mouth opening where the condyle
rotates and translates in the glenoid fossa of the temporal
bone is the rotation of the skull associated with an increase
in the lordotic curvature of the spine. Biomechanically, mouth
opening is facilitated during the extension movement of the
craniocervical complex, as occurs in the hyperlordosis, since
the mandible during its movement uses different manners to
Fig. 5 Mean values for the anterior translation distance prevent compression of the upper airway. With the TMD,
between the groups. Each column represents the translation of the mandibular condyle is affected mainly by
mean W SEM. *p = 0.045, t test indicates a significant changes in mobility of intra-articular disc, thus limiting the
increase in relation to free TMD group. biomechanics of mouth opening. This could possibly trigger
compensation in extension of the skull and cervical spine. It is
important to make clear that, because of the divergent
findings in the literature, it is unclear whether such compen-
errors in the evaluation of image, ensuring the scientific rigor sation occurs in a dynamic or static manner.
of this study. Therefore, in the present study was verified in the TMD
In the present study, from five radiographic craniocervical group a tendency of subjects present anteriorization of the
measurements performed, three the high cervical angle, low cervical spine (hyperlordosis) associated with flexion of the
cervical angle and occipitalatlas distance were not shown to first cervical vertebra (C1). However, due to the sample size, the
be statistically different between the free TMD and TMD results should be interpreted with caution. These findings
groups, corroborating previous studies.2022,31 were different from the other ones,13,43 whose, of the
Nevertheless, statistically significant difference was found biomechanical point of view, suggested that a rectification
for the Tz C2C7 distance and for the APA, which, respectively, of the cervical spine represented by the distance Tz C2C7
had shown to be significantly increased and reduced, in the would induce a reactional response of C1. This would enter
TMD group in relation to free TMD group. into flexion, or of the cranium in anterior rotation, with the
APA refers to the angulation of C1 in relation to the objective of maintaining the horizontal orientation of the eyes.
horizontal plane. Because C1 is anatomically articulated with Therefore, it is clear that further studies using the same
the articular facets of the occipital bone (occipital condyles), methodological basis and diagnostic criteria should be
this measurement has been used to verify the craniocervical conducted to confirm this affirmation.
posture. Reduction of the APA suggests a flexion of the first In conclusion, it could be verified that subjects with
cervical vertebra, that indicates an anterior rotation of the symptomatic TMD had a tendency to present flexion of the
cranium, and thereby, the OAD would maintain itself first cervical vertebra and an anteriorization (hyperlordosis) of
equilibrated without compression of the important vascu- the cervical spine (C2C7). However, we emphasized that the
lar-nervous structures in this region, which may have been above-mentioned hypothesis should be interpreted with
responsible for the lack of significant difference in the caution due to the sample size of the present study. Even
mentioned distance between the groups. However, according though, it is not possible to affirm whether it was the TMD that
to Rocabado and Tapia,23 and Bricot,43 it may also occur a caused the alterations in the measurements of APA and Tz C2
reactional and compensatory posterior rotation of the C7 or vice-versa, since there was no possibility to verify the
cranium, in an attempt to maintain the horizontal orientation sequence of appearance of the two disorders. Then, future
of the eyes. This would cause a reduction of the OAD, which studies should monitor subjects with cervical spine without
did not occur in the present study. Although the APA has been TMD, and with TMD without cervical spine, trying to define
proposed by Harrison et al.32 as one of the angles used in the who is the main risk factor.
creation of a geometric model for measurement of the Additionally, future investigations about the relationship
cervical spine in the sagittal plane, no studies were found between TMD and craniocervical posture should verify if the
which had used this angle in TMD patients. So, the APA static evaluation of cervical spine is the best method to
reduction (C1 flexion) associated with a suboccipital space assessment the relationship between TMD and craniocervical
unchanged could indicate that the upper cervical spine, alteration, since the temporomandibular complex is a dynam-
composed of C1 and C2, which may be responsible for the ic joint.
compensation of those subjects, not necessarily influence the Funding: This study was funded by Conselho Nacional de
flexionextension movement between C1 and the occipital Desenvolvimento Cientfico e Tecnologico National Counsel
condyles (skull). of Technological and Scientific Development (CNPq).
The increase in the distance Tz C2C7 may suggests an Competing interests: None declared.
anteriorization of the cervical spine, which are in accordance Ethical approval: Ethical Committee of Federal University
with the findings of Huggare and Raustia,14 and Sonnesen of Sergipe approved this study CAAE No. 0018.0.107.000-08.
archives of oral biology 55 (2010) 670678 677
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