Ulviye Şebnem Büyükkaplan, Alev Aksoy, Nurgül Kömerik

Ulviye Şebnem Büyükkaplan, Alev Aksoy, Nurgül Kömerik

274 Research report
Fluoride 45(3 Pt 2)274–280
July-September 2012
Absence of association between TMJ disorders
and dental fluorosis in Isparta, Turkey
Büyükkaplan, Aksoy, Kömerik, Yilmaz, Karayilmaz
274
ABSENCE OF SIGNIFICANT ASSOCIATION BETWEEN
TEMPOROMANDIBULAR JOINT (TMJ) DISORDERS
AND DENTAL FLUOROSIS IN ISPARTA, TURKEY
Ulviye Şebnem Büyükkaplan,a* Alev Aksoy,b Nurgül Kömerik,c Hasan Hüseyin Yilmaz,d
Hüseyin Karayilmaze
Antalya and Isparta, Turkey
SUMMARY: The aim of this study was to investigate whether individuals with dental
fluorosis (DF) have signs and symptoms of temporomandibular joint (TMJ) disorders
(TMD). The study group consisted of 71 dental patients with DF who were born and
living in an endemic fluorosis region of Isparta, Turkey. The control group comprised
29 patients not having DF, who applied to our clinics from neighboring communities
with low levels of F (<0.3 ppm) in the drinking water. DF in the 71 patients of the study
group was classified using a modified version of the Thylstrup-Fejerskov Index: 21
mild, 23 moderate, and 27 severe. All 100 participants were examined clinically, and
any signs and symptoms of TMJ disorders (TMD) were recorded using a standard
evaluation form. Radiological changes in the TMJ were studied using plain lateral
TMJ projection. No statistically significant difference in clinical signs and symptoms
of TMJ-TMD was detected between individuals with or without DF. There were also no
statistically significant differences in radiological changes in TMJ between the two
groups. Thus, this small-scale preliminary survey did not reveal an association
between DF and TMJ-TMD. Further investigation is needed, however, to determine
dose-related effects of high-F intake on the human stomatognathic system.
Keywords: Dental fluorosis (DF); Isparta, Turkey; Temporomandibular joint (TMJ) disorders;
Thylstrup-Fejerskov fluorosis index.
INTRODUCTION
Fluoride (F) is mainly incorporated into calcified tissues (i.e., bones and teeth)
because of its high affinity for calcium together with phosphate ion. It replaces the
hydroxyl group of hydroxyapatite crystals to form fluoroapatite, which is less
soluble and more compact. F also increases metabolic turnover of bone and
stimulates proliferation of lower-quality bone cells.1-4 Excessive intake of F
during childhood causes dental fluorosis (DF), and prolonged high F intake can
also cause skeletal fluorosis,5,6 which is characterized by pain, deformities, and
limited movement of the joints, the spinal skeleton, and major joints of
extremities. Alarcón-Herrera et al.7 found a linear correlation between the Dean
index of DF and the frequency of bone fractures among both children and adults.
Articular calcification and necrosis of articular chondrocytes in skeletal fluorosis
have been reported.4 Savas et al.8 observed that a high number of female patients
residing in Isparta, Turkey, who have DF also complained of knee pain. They
found that radiological severity of knee osteoarthritis was greater and atypically
aAssistant
Professor Dr UŞ Büyükkaplan, Department of Prosthodontics, Faculty of Dentistry,
Akdeniz University, Antalya, Turkey; bAssociate Professor Dr A Aksoy, Department of
Orthodontics, Faculty of Dentistry, Süleyman Demirel University, Isparta, Turkey; cAssociate
Professor Dr N Kömerik, Department of Oral and Maxillofacial Surgery, Faculty of Dentistry,
Süleyman Demirel University, Isparta, Turkey; dProfessor Dr HH Yilmaz, Department of Oral
Diagnosis and Radiology, Faculty of Dentistry, Süleyman Demirel University, Isparta, Turkey;
eAssistant Professor Dr H Karayilmaz, Department of Pedodontics, Faculty of Dentistry, Akdeniz
University, Antalya, Turkey.
a*For correspondence: Dr UŞ Büyükkaplan, Akdeniz Universitesi, Dis Hekimligi Fakultesi,
Protetik Dis Tedavisi A.D., 07058, Antalya, Turkey; E-mail: [email protected].
275 Research report
Fluoride 45(3 Pt 2)274–280
July-September 2012
Absence of association between TMJ disorders
and dental fluorosis in Isparta, Turkey
Büyükkaplan, Aksoy, Kömerik, Yilmaz, Karayilmaz
275
located osteophytes were more frequent in patients with DF. They concluded that
residing an area of endemic fluorosis was associated with increased severity of
degenerative changes in the bone and joints.
Animal studies also indicate fluorosis may exert adverse effects in the
temporomandibular joint (TMJ) structures.9,10 Due to such effects of F on TMJ
structures, fluorosis may cause or at least predispose TMJ disorders (TMD). In a
histological and histomorphometic study, Kameyama9 demonstrated that
mandibular condyles of the rats that received 100 ppm F in the drinking water
exhibited a significant increase in both the thickness of the cartilage layer and the
density of cancellous bone compared to the controls. In his report, Kameyama
proposed that the thickening of the cartilage layer was due to an increase in the
number of hypertrophied chondrocytes. In addition, he found that the trabeculae of
cancellous bone were thicker with extreme reduction in bone marrow spaces in the
mandibular condyles of the rats that received 100 ppm F in their drinking water.9
Harbrow et al.10 also reported that chronic exposure of rats to 100 ppm NaF
increased the thickness of the cartilage layer of the mandibular condyle.
Stimulation of chondrocytes by F was thought to have delayed the normal
processes of capillary invasion, thereby resulting in thickening of the cartilage
layer.
The city of Isparta, located in southwestern Turkey, is one of the country’s
severe endemic fluorosis regions. In Isparta, F in the natural water supply is the
major source of F. The prevalence and severity of DF among the population in the
central part of Isparta are substantially higher than expected for F levels in
drinking water in the range of 2.16–4.30 ppm.11 The purpose of this study was to
investigate whether individuals with DF living in Isparta City have an increased
tendency to exhibit signs and symptoms of TMJ.
MATERIALS AND METHODS
Patients who had applied to the Dental Faculty of Süleyman Demirel University
for dental care were screened for DF. Based on information on the forms, the study
group consisted of 71 patients with DF who were born in Isparta. The control
group consisted of patients who applied to our clinics from locations with low
levels of F (<0.3 ppm) in the drinking water and who did not have DF. When
creating the study and control groups, only subjects who were living in the same
residential area since birth were selected. All the subjects had normal overjetoverbite relationship and occlusion. Both the study and control group subjects had
no history of orthodontic treatment, occlusal equilibration, crown restoration, or
history of cranio-mandibular trauma.
In Isparta and neighboring communities, local government employee residents
have similar, normal family and socio-economic levels. In regard to dental
hygiene, patients with periodontitis were not included in the study. From the
detailed medical history obtained from each prospective subject, exclusion criteria
included taking medications that may influence bone metabolism, any metabolic
and inflammatory bone disease, bruxism or parafunctional masticatory habits,
acute infection or periodontitis, and a history of psychosomatic disorders.
This study was conducted according to the ethical standards of the Declaration
of Helsinki (Current [2008] version) that promote respect for all human beings and
protect their health and rights. The local ethics committee approved the study
276 Research report
Fluoride 45(3 Pt 2)274–280
July-September 2012
Absence of association between TMJ disorders
and dental fluorosis in Isparta, Turkey
Büyükkaplan, Aksoy, Kömerik, Yilmaz, Karayilmaz
276
protocol for this investigation, with written consent being obtained from each
participant after being informed about the purpose of the study and where and how
the results would be used.
A modified version of the Thylstrup-Fejerskov Index (TFI) was used to classify
the degree of DF.12 Accordingly, TFI scores were evaluated as follows: 0 TFI
score = healthy tooth structure; 1–3 TFI scores = mild DF; 4–6 TFI scores =
moderate DF; and 7–9 TFI scores = severe DF (see Figure).
Figure. Modified version of the Thylstrup-Fejerskov Index (TFI) used in the study. 1a-1b (16year-old, female patient): TFI score = 0, Healthy Tooth Structure; 2a-2b (15-year-old, female
patients): TFI scores = 1–3, mild fluorosis; 3a-3b (18-year-old, male patients): TFI scores = 4–
6, moderate fluorosis; 4a-4b (20-year-old male patient): TFI scores = 7–9, severe fluorosis.
277 Research report
Fluoride 45(3 Pt 2)274–280
July-September 2012
Absence of association between TMJ disorders
and dental fluorosis in Isparta, Turkey
Büyükkaplan, Aksoy, Kömerik, Yilmaz, Karayilmaz
277
The patients were asked whether they had any of the following symptoms related
to TMJ over the past 6 months: TMJ pain during jaw movements; TMJ noise or
sounds; impaired mouth opening. Clinical diagnosis for temporomandibular
disorders (TMD) was established according to the following criteria.13
1. Mandibular range of motion: Mandibular range of motion was evaluated for
maximum opening and lateral movements. Maximum opening was measured from
central maxillary incisor to the opposing mandibular incisor on a millimeter ruler,
taking overbite into consideration. Lateral movements were measured relative to
the maxillary midline with the teeth slightly separated. Patients with limited mouth
opening ‘soft-end feel’ and ‘hard-end feel’ were noted in order to determine
whether the problem takes its origin from muscles or the intracapsular region. Any
alterations of the path taken by the midline of the mandible during maximal
opening were also recorded.
2. Pain in the TMJ: The TMJ pain was identified during palpation, mandibular
range of motion, or assisted mandibular opening.
3. Clicking/Crepitation: TMJ was auscultated with a stethoscope, while the
subject performed three openings, and three lateral and protrusive movements.
4. Lateral TMJ radiographs: Radiographic study included examination for the
anatomy of the TMJ bony components (any bone resorptions or flattening of the
eminence or the condyle); deformities of the joint surfaces; osteophyte formation;
osteosclerosis (an overall increase in bone density with thickening of the cortex);
subchondral cyst formations; and ossification of the soft tissues such as ligaments,
capsule, and disc.
Statistical analyses (Chi-square, Kruskal-Wallis, Mann Whitney U) were
performed using SPSS (Ver. 15.0, SPSS Inc., Chicago, IL, USA). The significance
level was for p<0.05.
RESULTS
Among the 100 patients (28 male and 72 female) who participated in the study,
29 had no DF, 21 had mild, 23 had moderate, and 27 had severe DF. The mean age
(between 12–40 years-old) of the patients was 17.37±5.56. The demographic data
of the patients who participated in the study are given in the Table, which shows
the distribution of the patients according to their TMJ history. As seen in the Table,
the most prominent symptom suggesting TMD was the presence of clicking sound.
There were no statistically significant differences between pain, limitation of
mouth opening, and click history of the patients with and without DF (p>0.05).
When patients were examined for the selected symptoms of TMD, no significant
differences were observed between the groups with or without DF (p>0.05).
The mean maximum mouth opening was 39.74±6.36 mm (minimum 14 mm–
maximum 54 mm), the mean lateral movements were 5.29±2.36 mm (minimum 0
mm–maximum 13 mm), and the mean protrusive movements were 4.83±2.16 mm
(minimum 1 mm–maximum 11 mm). A total of 10 patients had deviation during
mouth opening. Of these 3 (10.3%) had no DF, 2 (9.5%) had mild DF, 2 (8.7%)
had moderate DF, and 3 (11.1%) had severe DF.
Patients’ awareness of limited mouth opening did not correlate with measured
mouth opening. However, pain history was correlated with maximum mouth
Absence of association between TMJ disorders
and dental fluorosis in Isparta, Turkey
Büyükkaplan, Aksoy, Kömerik, Yilmaz, Karayilmaz
278 Research report
Fluoride 45(3 Pt 2)274–280
July-September 2012
278
opening (p=0.001), lateral range of motion (p=0.003), and protrusive motion
(p=0.01).
Click complaint and sound from the joint showed correlation (p=0.002). Of all
patients, 23 had a clicking sound on mouth opening and/or closing. There were no
statistically significant differences between erosion or irregularities on joint
surfaces between those with and without DF. In addition, no correlation was found
between radiographic changes, jaw deviation, and joint sounds (Table).
Table. Demographics, history, pain, noise (sound), radiographic changes of TMJ, and mandibular range of motion in the
non-DF and DF patients
Mild
DF
(n=21)
No
DF
(n=29)
Age ranges (years)
Demographic
data of the
patients
TMJ history
Pain with TMJ
Mandibular
range of motion
(mm)
13 –21
13–25
Severe
DF
(n=27)
Moderate
DF
(n=23)
13–27
13–30
Total
(n=100)
13–30
Mean age (years)
15.5 (±2.9)
16.2 (±5.5)
15.7 (±5.1)
21.7 (±6.0)
17.37(±5.5)
Female
23
(79.3%)
14
(66.7%)
17
(73.9%)
18
(66.7%)
72
(72%)
Male
6 (20.7%)
7 (33.3%)
6 (26.1%)
9 (33.3%)
28 (28%)
Pain
3 (10.3%)
3 (14.3%)
2 (8.7%)
3 (11.1%)
11 (11%)
Clicking
5 (17.2%)
3 (14.3%)
2 (8.7%)
6 (22.2%)
16 (16%)
Limitation on mouth
opening
2 (6.9%)
1 (4.8%)
-
3 (11.1%)
6 (6%)
Palpation
2 (6.9%)
1 (4.8%)
1 (4.3%)
-
4 (4%)
Mouth opening
1 (3.4%)
-
-
2 (7.4%)
3 (3%)
Lateral motions
2 (6.9%)
-
-
4 (14.8%)
6 (6%)
Protrusive motions
1 (3.4%)
1 (4.8%)
2 (8.7%)
2 (7.4%)
6 (6%)
Maximum mouth
opening
39.3 (±7.1)
40.6 (±6.7)
38.3 (±5.2)
40.8 (±6.2)
Lateral movement
4.2 (±2.1)
5.9 (±2.1)
5.4 (±2.1)
5.9 (±2.6)
Protrusive movement
4.2 (±2.1)
5.2 (±2.1)
4.4 (±1.8)
5.4 (±2.5)
Deviation
7 (±24.1)
5.2 (±2.1)
8 (±34.8)
5 (±18.5)
Noise (sound)
with TMJ
Clicking
6 (20.7%)
7 (33.3%)
3 (13%)
7 (25.9%)
23 (23%)
Crepitation
3 (10.3%)
1 (4.8%)
6 (26.1%)
4 (14.8%)
14 (14%)
Radiographic
changes with
TMJ
Erosion
4 (13.8%)
4 (19%)
3 (13%)
4 (14.8%)
15 (15%)
Irregularities
1 (3.4%)
1 (4.8%)
1 (4.3%)
4 (14.8%)
7 (7%)
DISCUSSION
Dental fluorosis (DF) is a developmental disturbance of dental enamel caused by
successive exposures to high concentrations of F during tooth development,
leading to enamel with lower mineral content and increased porosity.14 The
severity of the disorder appears to be directly related to the magnitude and
duration of high-F exposure.15
Czarnowsky et al.16 have shown that increased F intake adversely affects bone
density. In a study of industrial fluorosis, a close relationship was found between
the occurrence of skeletal fluorosis and the time and degree of F exposure.17 Ohmi
et al.18 investigated the effects of fluoridation and its discontinuation on the
279 Research report
Fluoride 45(3 Pt 2)274–280
July-September 2012
Absence of association between TMJ disorders
and dental fluorosis in Isparta, Turkey
Büyükkaplan, Aksoy, Kömerik, Yilmaz, Karayilmaz
279
middle and apical parts of the alveolar bone and the body of the mandible of rats,
finding that the upper parts of the alveolar bone and the alveolar crest presented
the highest rates of resorption after discontinuation of F exposure. In animal
models with a wide range of F in the drinking water, tooth F content was
associated with bone F content.19,20 Tooth F concentration in mice exposed to a
wide range of F in their diet confirmed the possibility of usage of teeth as a
biomarker for skeletal exposure.19 In addition, a strong positive correlation
between the degree of DF and mandibular bone F content was found in a sample of
red deer exposed to elevated levels of F in the environment, thereby demonstrating
the usefulness of DF as a biomarker of increased F exposure for biomonitoring
studies in deer.20
As noted in the Introduction, Savas et al.8 suggested that endemic DF in Turkey
might be associated with increased severity of degenerative changes in the bone
and knee osteoarthritis. In the present study, it has not been determined whether
osteoarthritis follows the course of internal dental derangements following disc
displacements or vice versa. Dentition and the occlusal status of the patients were
also similar. However, there was no significant difference between control and DF
subjects in regard to the prevalence of osteoarthritis.
Temporomandibular disorders (TMD) including abnormal, incomplete, or
impaired function of the TMJ, along with a collection of symptoms frequently
observed in various combinations were first described by Costen in the 1930s,
which he claimed to be reflexes due to irritation of the auriculotemporal and/or
chorda tympanic nerves as they emerge from the tympanic plate caused by altered
anatomic relations and derangements of the TMJ associated with loss of occlusal
vertical dimension, loss of posterior tooth support, and/or other malocclusions.21
The symptoms can also include headache about the vertex and occiput, tinnitus,
pain about the ear, impaired hearing, and pain about the tongue.21 There is thus a
myriad of possible variables in TMD and certainly many confounding issues and
unknowns. Therefore, to include all such possible or controversial confounding
factors for TMD needs a very large population for study because of so many
parameters. However, incorporating these additional parameters in the present
study of DF and TMD was not feasible because of the small sample of the study
groups.
In our study, we found no TMJ bony differences between the control and DF
patients. Çağlayan and Tozoğlu22 showed that TMJs have incidental findings in
radiographic evaluations, such as erosion of the condyle, osteophytes, and bifid
condyle. Also in the present study, radiographic changes were found to be similar
in both the control and DF groups. Still, the effects of F on humans are known to
be determined primarily by the nature, dose, and duration of F exposure, age, sex,
dietary habits, genetic factors, and combinations of them. Overall, the total
quantity and period of F ingestion appear to be the most important factors
determining the clinical course of skeletal fluorosis, which is characterized by
immobilization of joints of the axial skeleton and of major joints of the
extremities.
In conclusion, clinical and radiological examination of TMJ in DF patients in
our study showed no significant differences from the control subjects without DF.
As noted above, the effects of F are mainly determined by the nature, dose, and
280 Research report
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July-September 2012
Absence of association between TMJ disorders
and dental fluorosis in Isparta, Turkey
Büyükkaplan, Aksoy, Kömerik, Yilmaz, Karayilmaz
280
duration of F exposure, together with other factors like age, sex, genetic
differences, and dietary habits or their combination. TMDs also have a very
complex multi-factored pathology. Thus, the connection between DF and TMD
needs to be evaluated on larger study populations in multidisciplinary manner. In
the present study, the apparent absence of a relationship between TMD and DF
may be due to limitations of the size of sample groups and thus can be seen as
preliminary for further studies.
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