Thermographic assessment of temporomandibular disorders symptomology during orthodontic treatment

Thermographic assessment of temporomandibular disorders symptomology during orthodontic treatment

Susan B. McBeth, DDS, M S , a and Barton M. Gratt, DDS b

Rogers, Ark., and Los Angeles, Calif.

The relationship between orthodontic treatment and temporomandibular disorder (I-MD) symptoms has been the focus of many subjective studies. Objective studies are now needed. Electronic thermography (EI) has shown promise as an objective tool for assessing temporomandibular disorders. Clinical TMD examinations and ET were performed on 21 control subjects, 18 subjects undergoing orthodontic treatment, and 20 subjects with TMD pain. Standardized blinded clinical examinations that used algometry were conducted. The ET was performed with an Agema 870 unit (Agema Infrared Systems, Secaucus, N.J.) under controlled conditions. Data were analyzed to determine the usefulness of ET as an objective measure of TMD symptoms. The ET alone identified the subjects with painful clicking TMD with a sensitivity of 87%. Subjects with no painful clicking (controls) were identified with a specificity of 86%. The ET findings also had a strong correlation with pain to muscle palpation. This study indicates that ET shows promise as an objective tool for selecting normal subjects from subjects with TMD symptoms. The ET could prove to be valuable in accessing the relationship between orthodontic treatment and TMD symptoms in future longitudinal studies. (Am J Orthod Dentofac Orthop 1996;109:481-8.)

I n recent years, temporomandibular joint (TMJ) symptoms have been the focus of many studies. 1-5 The relationship between orthodontic treatment and temporomandibular disorder (TMD) symptoms has been repeatedly investigated. 6-28 Various opinions and individual case reports in the orthodontic publications before the early 1980s reflected the following diverse beliefs: (1) Orthodontic treatment does/does not play a role in causing TMJ disorder; (2) orthodontic treatment does/does not alleviate the signs and symptoms of TMJ disorder; and (3) orthodontic treatment does/does not aggravate a pre-existing TMJ disorder. Unfortunately, very little objective data existed to bring any biologic truths to light.

In 1987, the American Association of Orthodontists began a program to stimulate research on orthodontic treatment as it relates to TMD. Reynders 6 published a review that included studies from 1966 to 1988. An excellent review of the most recent publications was published by Sadowsky 7 in 1992. The vast majority of these studies report no TMD symptoms during orthodontic treatraent. However, several inherent problems and inconsistencies exist in these TMJ studies. Vague

From the University of California at Los Angeles, School of Dentistry. aprivate Practice of Orthodontics, Rogers, Ark; Orthodontic Masters Candi- date, Section of Orthodontics. bProfessor, Section of Oral Radiology. Copyright © 1996 by the American Association of Orthodontists. 0889-5406196/$5.00 + 0 8/1/68892

subject descriptions, nonspecific subgroup assign- ments, unstandardized examination methods, and lack of control groups were all factors that made these study results unreliable. Additional challenges occur when attempting to study TMD in patients undergoing orthodontic treatment, because of the longitudinal nature of this treatment (which can be many years). To scientifi- cally study the presence or absence of TMD symptoms in any population, first, an objective tool of measurement is needed to quantify symptoms; and second, a longitudinal study is necessary to capture the transient nature of TMD symptoms, if they are present.

Electronic thermography (ET) has recently been applied to the assessment of the TMD. Body temperature has been used as an indicator of medical dysfunction for thousands of years. 29 It is well established in the field of thermography that normal, symptom-free patients show thermal symmetry between the right and the left sides of the body. Studies have shown that in healthy persons, temperatures of the body (including the face) were essentially bilaterally equal, with an average temperature difference from side-to-side (termed AT) of only 0.2 ° C? ° In 1975, the reproducibility of ET findings were shown in a longitudinal study by Uematsu? ~

Electronic thermography can measure the skin surface temperature overlying the TMJ with an accuracy of 0.1 ° C. The heat, or infrared radiation, emitted from the body is translated into visible light by the elec-

481

482 McBeth and Gratt American Journal of Orthodontics and Dentofacial Orthopedics May 1996

tronic thermography unit. The infrared signal is pro- jected onto a television screen for viewing. An advan- tage of ET is its noninvasive nature (as no ionizing radiation is used). Electronic thermography is of value to this study because of its sensitivity to temperature changes that occur physiological ly in areas of the TMJ and the supporting muscles of mastication. 32

In a series of recent ET TMJ studies, 29"33-36 Gratt

and coworkers demonstrated that normal subjects have AT TMJ zone measurements ranging from 0.0 ° to 0.2 ° C, whereas patients with TMD disorders (osteoarthrosis, internal derangement, and mild to moderate TMD pain and dysfunction) all have statistically different mean AT TMJ zone measurements ranging from 0.4 ° to 0.5 ° C. Overall results indicated that ET measurements of the TMJ region may prove to be an objective and reliable indicator of TMD.

It was the intent of this project to assess the relationship between clinical and thermographic data in subjects with distinct TMD symptoms, as well as patients undergoing orthodontic treatment. In this study we addressed three hypotheses: (1) There is no difference in ET TMJ findings: between a control group, an orthodontic treatment group, and a painful TMJ (clicking) group; (2) there are no group differences in (a) joint pain scores and (b) muscle palpation scores; and (3) there is no correlation between ET scores and (a) joint pain scores and (b) muscle palpation scores. The result of this study will offer insight into the diagnostic value of ET. This information seems invaluable in determining the feasibility of using ET in future longitudial studies.

MATERIALS AND METHODS Study Population

To estimate the sample size needed in this study, a standardized effect size was computed, 0.4/0.2 = 2.0. With a specified alpha value of 0.05 and a beta value of 0.10, these values convert to an estimated sample size needed of 17 persons per group studied. 37 Therefore 21 subjects were studied in the control group, with 18 in the orthodontic treatment group, and 20 in the painful TMJ group. The total number of subjects measm'ed was 59. The median age for the control and the orthodontic subjects was 24 years, the median age for the pain subjects was 25 years, (ages ranged from 16 to 50 years). The female'to male ratio for the three groups was 2 : 1. The p values indicated that the three groups were not significantly different in their distributions by age, gender, or occlusion. All subjects gave written informed consent consistent with our Institutional Review Board Standards. Each subject completed a Jaw/Pain Function questionnaire and a Health History questionnaire.

Group 1 (the control group) consisted of 21 subjects who were not undergoing orthodontics at the present time and who did not perceive to have a TMD problem. This group was age matched, occlusion matched (Class I, II, or III), and gender matched to the orthodontic treatment subjects (group

2). The control subjects came to the clinic as escorts of the orthodontic or pain subjects. To be included in group l ( t he control group), a subject must have scored 5 or less on our Jaw Pain/Function questionnaire.

Group 2 consisted of patients in their sixth month or longer of orthodontic treatment at our university dental school, with teeth removed as part of their orthodontic treatment approach. This selection was made to create as large a homogenous study group as possible. In addition, any orthodontic clinic patients reporting TMD symptoms after the start of orthodontic treatment were included in this group.

Group 3 consisted of patients who reported and had persistent, painful, TMJ clicking as their major problem. Patients diagnosed as having a systemic disorder, osteroar- throsis, or a history of facial trauma were excluded from this study. Selected subjects were age, gender, and occlusion matched to subjects in group 2. Finally, to be included in Group 3, the person must have scored an 8 or greater on the Jaw Pain/Function questionnaire.

Calibration of Clinical Procedures

The three most common clinical markers of TMD are (1) limited range of mandibular motion, (2) muscle and TMJ tenderness, and (3) TMJ sounds. 38 Examiner calibration procedures were used to insure reproducibility and accuracy of data collection29 One examiner was trained and calibrated (1) to locate each palpation site within +7 mm, (2) to apply a standard pressure with the algometer (Pain Diagnostics and Thermography Corporation, Great Neck, N.Y.) for 2 seconds (at 1.8 kg/cm 2) over the muscle and (at 0.8 kg/cm :) over the lateral capsule of the TMJ, and (3) to use a common set of verbal instructions during the clinical examination.

Blinded Clinical Procedures

One calibrated examiner performed all the clinical examinations while each subject was assigned a secret code. Because mandibular mobility required mouth opening, and therefore the presence of orthodontic appliances could be seen, this objective measurement was performed by the examiner after the muscle palpation examination was com- plete. Admittedly, thorough and reliable muscle palpation of masticatory groups requires intraoral access also; this was not done as per study design.

1. Muscle and joint palpation severity scores: Pressure algometry was used to measure pressure pain thresh- olds over specific muscles. 4°'41 For all algometer applied pressure sites, the following pain scale was used: none = 1, mild = 2, discomforting = 3, distress- ing = 4, horrible = 5, and excruciating = 6. During the palpation, each subject was asked to rate their pain level, if any, on the Verbal Descriptor Scale. Data were collected regarding the pain level during standard clinical TMJ palpation to standard anatomic points that included the forehead, superficial masseter, deep masseter, anterior temporalis, middle temporalis, and lateral capsule. 42

2. Joint noise scores: Data on the presence or absence of joint sounds, the timing of the sounds, and any associated pain were collected.

American Journal of Orthodontics and Dentofacial Orthopedics McBeth and Gratt 483 Volume 109, No. 5

Nonblinded C~inical Procedures

Mandibular mobility scores were recorded as the distance between the incisal surfaces of the right maxillary and mandibular central incisors at the midline with a millimeter ruler. The subject's maximum active opening was then measured. Finally, interincisal distance was measured with pressure and recorded as the maximum passive opening. After each mandibular movement, the subject was asked to report the presence or absence of pain and to rate its severity with the VerOal Descriptor Scale. The subject's overjet and overbite were also measured with a millimeter ruler.

Thermography (ET)

Equipment. Facial thermography was conducted with an Agema 870 thermovision unit, including an infrared scanner, control unit, thermal image computer TIC-8000 and Meds 1.02 software, and color monitor (Agema Infrared Systems, Secaucus, NJ.) coupled to a 35 mm camera. Room conditions for thermographic examinations included a draft- free environment (no windows, closed doors), temperature control (ranging from 20 ° to 22 ° C), variable lighting, patient positioning chair, and a small handheld electric fa i l . 35

Facial imaging. Facial thermograms were taken with right and left lateral projections (Fig. 1). Before the examination, each patient's face was cleared of hair (tied back with an elastic headband), and the face and the TMJ regions wiped with a damp cloth and then air dried with a small electric fan. The patient was seated and a 15-minute period allowed for facial temperature equilibration before thermograms were made. Images were stored on computer disk . 3s

Image analysis. Objective thermal assessments included: (1) mean temperature measurements (zone temperature) of region over each TMJ and (2) temperature difference between the right and the left TMJ zone temperature measurement (termed TMJ zone AT). This method has been used in previous s~udies 2933--~5 and has been shown to be able to select normal TMJ subjects from abnormal TMJ subjects with an overall accuracy approaching 90% 35 (Fig. 2).

RESULTS

The results of our clinical examination included findings on: (1) TMJ sounds, (2) mandibular range of motion, and (3) muscle and TMJ palpation. The muscle and TMJ palpation data were the only useful and discriminating findings (as the only group of subjects with positive joint sounds and associated pain was the pain group, whereas all 59 persons examined showed a normal range of jaw motion). Therefore the principal clinical parameter found in this study was changes in muscle and joint palpation scores.

Table I shows the group mean differences in patient palpation (pain) scores for the six anatomic regions plus their sums. The group palpation scores were significantly different from each other in the superficial masseter area, and the total summed scores (p < 0.05). In the anterior temporalis, middle temporalis, and

lateral capsule areas, the control group was similar to the orthodontic group (p > 0.05), and the pain group was significantly higher. The only area that shows significant similarity between the orthodontic group and the pain group is the deep masseter area (possibly these results relate to the muscle palpation method that was only extraoral). The control group was quite different from the other two in the deep masseter area. The forehead, which was used as a control or baseline location, showed no significant differences between the groups, as we would expect.

Table II shows the group differences for AT, with 2~T

representing the absolute value of the difference between right and left TMJ mean zone temperatures. The mean values for AT were 0.1 ° C for the control group, 0.2 ° C for the orthodontic treatment group, and 0.4 ° C for the painful clicking group. The mean of the control group compared with the mean of the orthodontic treatment group resulted in a t value of 1.88, and a p value of 0.0658 (Table III). When the mean AT of the control group is compared with the mean AT of the painful clicking group, the t value is 5.47, with a p value of 0.0001. The difference between the control group and the painful clicking group was significantly different (Fig. 3).

Sensitivity and specificity further describe the diagnostic capabil i ty of thermography. Sensitivity indicated that a AT of 0.4 ° C coincided with painful clicking (defined by a score of 8 or greater on the Jaw Pain/Function questionnaire) 87% of the time. In mea- suring specificity, there is an 86% probabil i ty that AT will be 0.1 ° C when the patient has no painful clicking (defined by a score of 5 or less on the Jaw Pain/Function questionnaire, and qualifying as a subject in the control group).

When we compare the orthodontic treatment group and the painful clicking group as previously mentioned, we see that the difference in AT between them is also different beyond chance, with a p value of 0.0012. In summary, for AT group differences, we did find significant differences between the control and the painful clicking groups. We could not show a statistically significant difference between the control group and the orthodontic treatment group at the 0.05 level of significance (p = 0.0658).

To examine the relationship of thermographic findings to clinical palpation scores, Pearson correlation coefficients were calculated. Table IV shows AT value and its correlation to the palpation score of the most affected side for each of the six locations and their sum. All areas showed positive correlations; whenever AT increased, so did the palpation score. The correlation coefficients indicated moderate correlations, with the best correlation at anterior temporalis ( r = 0.56, p = 0.0001) and superficial masseter (r = 0.52, p = 0.0001).

484 McBeth and Gratt American Journal of Orthodontics and Dentofacial Orthopedics May 1996

Fig. 1. Right and left lateral facial ET of 19-year-old female orthodontic patient (from group 2). ET is accurate to 0.1 ° C and is imaged with 1.0 ° C color bands.

Fig. 2. Same subject as imaged in Fig, 1 with TMJ zones outlined, mirrored, and analyzed by computer. Boxes indicate mean zone temperatures, standard deviation, high and low temperatures, and size of zone (in pixels). TMJ zone AT was calculated to be 0.1 ° C.

The least correlated area was the forehead (r = 0.24, p = 0.0692).

DISCUSSION

There are many studies reported in the publications that report on the relationship between orthodontic treatment and TMD symptoms, with the majority concluding that occlusion plays a limited role in the cause of TMD

problems. There are several inherent problems with this type of research. None of the orthodontic patient studies were conducted in a blind to subject manner. Other problems, such as vague subject description, inappropri- ate and nonspecific subgroup assignment, unstandardized examination methods, reporting of retrospective data, multiple noncalibrated examiners, and the absence of a control group, exist in many studies.

American Jourl~al of Orthodontics and Dentofacial Orthopedics McBeth and Gratt 4 8 5 Volume 109, No. 5

Table h Patient palpation (pain) scores for three groups over six anatomic regions with mean values of the most affected side

Group Superficial masseter I Deep masseter Anterior temporalis Middle temporalis Lateral capsule

Anatomic region

Forehead Sum

Control 0.50 0.40 0.24 0.19 0.29 0.14 1.76 Orthodontic 1.33" 1.36" 0.72 0.31 0.33 0.33 4.39* Pain 2.05"t 1.88" 1 .35 ' t 0.85"t 1.15*t 0.42 7,7"t

*Significantly different from control group (p < 0.05). tSignificantly different from orthodontic group (p < 0.05).

Table Ih Thermographic values (absolute AT values, degrees C) for three groups: mean, median, range, standard deviation, and standard error

Gro~T Mean Median Range Standard deviation Standard error

Control O. 13 O. 1 0.0-0.4 O. 14 0.030 Orthodontic 0.23 0.2 0.0-0.5 O. 17 0.039 Pain 0.43 0.4 O. 1-0.8 O. 19 0.042

Our study used inclusionary and exclusionary criteria for subject assignment to group, a standardized examination method with consistent verbal directions, prospective data, a solitary calibrated examiner, who was blind to the subject status of the patient, and the presence of a control group. The unique design of this study increases the reliability of the results obtained, thus adding to the present knowledge of the relationship between orthodontic treatment and TMD symptoms.

The anatomic location that was most important in separating the groups was the superficial masseter muscle. Both the superficial masseter and the deep masseter palpation scores showed a statistically significant amount of pain in the orthodontic patients as compared with the control subjects. It would seem that transitional occlusal disharmonies introduced during orthodontic space closure may cause hyperactivity in the jaw elevator muscles. What is the relationship of occlusal disharmony and muscle activity? In a study by Williamson and Lundquist, 43 interfering dental con- tacts had a large influence on conscious, voluntary muscle activity. In another study by Rugh, 44 high crowns placed in the mouths of bruxers, which is subconscious, uncontrolled, involuntary muscle activity, resulted in a decreased muscle activity. This is likened to tl~e decrease in bruxism seen after placement of orthodontic appliances. The sensitive teeth initiate a painful sensory input that decreases the bruxing event. However, in the Rugh study, a significant percentage of the subjects wearing the high crown reported an increase in muscle pain. This increase was not associated with increased bruxism, so it was proposed that an

Table III. Comparison of AT values and p values between groups

Groups T value p value

Control and orthodontic 1.88 0.0658 Control and pain 5.47 0.0001 Orthodontic and pain 3.41 0.0012

increased tonus of the elevator muscles resulted from the attempt to protect the mandible from closing on the high crown. Other studies have also shown this pro- tective response of the elevator muscles. 45"46 The orthodontic population in this study had varying degrees of (1) sensitive teeth because of appliance placement and (2) temporary occlusal interferences, resulting in an increase in muscle palpation pain response with little pain on palpation at the lateral capsule or forehead.

We expected the patients with painful clicking to have an even higher level of muscle palpatio n pain than the orthodontic patients because of the inclusive criteria (Jaw/Pain questionnaire) that was met in assignment of these persons into file painful clicking group. However, it is interesting to note that pain tO palpation of the deep masseter was similar between the orthodontic patient and the painful clicking subjects, although intraoral palpation would be expected to produce more positive findings/feedback in the deep masseter fibers. If we were to rely solely on deep masseter muscle palpation and ET, the palpation did not identify the orthodontic group from the painful clicking group, but the ET did (p < 0.05).

486 McBeth and Grat t American Journal of Orthodontics and Dentofacial Orthopedics May 1996

0 . 8 -

0 . 7 -

0 . 6 -

0 . 5 - o

N 0.4

0.3

0.2

0.1

• - 25th percentile to the 50th percentile [ ] - 50th percentile to the 75th percentile t - represents maximur~value

- represents minimumvalue

0.0 Control Orthodontic Pain Group Group Group

Fig. 3. TMJ zone AT distributions by group, with mean values, maximum values, minimum values, 25th-to-50th percentile values, and 50th-to-75th percentile values.

Table IV. Pearson correlation coefficients and p values between AT values and palpation scores

Palpation location r P value

Superficial masseter 0.52 0.0001

Deep masseter 0.41 0.0012

Anterior temporalis 0.56 0.0001

Middle temporalis 0.40 0.0016

Lateral capsule 0.37 0.0043

Forehead 0.24 0.0692

Sum 0.52 0.0001

The results of this investigation show that ET is capable of distinguishing symptom-free persons (mean zone AT = 0.13 ° C) from persons with painful clicking (mean zone AT = 0.41 ° C). This result is similar to that found by Gratt and coworkers, 35 where patients with unilateral osteoarthrosis had the greatest mean difference between the right and left sides to be 0.5 ° C. However, the range of values found in this study showed some overlap: The control group range for AT was 0.0 to 0.4 and the painful clicking group had a range of 0.1 to 0.8. In any study, there will always be a few symptom-free patients who will have a large AT value. This could be due to the presence of a subpopu- lation who have characteristics that affect the thermographic reading. In addition, patients with symptoms have a small AT, while occasionally joints will be elevated in temperature bilaterally. In our study, 4 of 20 painful clicking subjects had a AT of 0.2 ° C. Two of these four subjects had bilateral clicking, and neither had significant pain on clicking. This brings up the

complication of the transient nature of TMD symptoms. The four patients previously mentioned had a history of pain (enough to qualify as a painful clicking subject), but the pain was not present the day of the examination, and it was recorded as such. Because sensitivity is 87% and specificity is 86% for thermographic imaging in this study, its reliability is good.

The control group and the orthodontic treatment group had AT values of 0.13 ° C and 0.23 ° C, respec- tively. As the p value was slightly more than the 0.05 significance level (p = 0.0658), and the sensitivity of the thermographic imaging unit is 0.1 ° C, these two groups could be similar to each other in regard to thermographic imaging.

What physiologic changes could result in such a distinct temperature elevation around the area of the TMJ? We know that elevated temperatures seen in thermographic images can locate areas of (1) increased and decreased blood flow, (2) inflammation, and (3) nerve dysfunction. In the TMJ, most of the major components such as the articular disk and the bony articular surfaces are nonvascularized. The collateral (discal) ligaments have a vascular supply and are innervated. However, the largest area of vascular tissue is the retrodiscal tissue, a region of loose connective tissue that is highly vascularized and innervated. 47 The posterior portion of the retrodiscal tissue is attached to a large venous plexus, which fills with blood as the condyle moves forward. 48'49 Perhaps it is inflammation, increased blood flow, and/or nerve damage in this retrodiscal tissue that causes the discrete area of temperature elevation that can be measured with electronic thermography.

Nerve damage could be detected in the nociceptor

American Journal of Orthodontics and Dentofacial Orthopedics Volume 109, No. 5 McBeth and Grat t 4 8 7

regions in periar t icular t issue such as (1) the discal

l igaments , and (2) the capsular l igaments (well inner-

vated), as wel l as (3) the ret rodiscal t issue p rev ious ly

ment ioned. The art icular surfaces themse lves are

noninnervated. 48

Does the rmography real ly add any addit ional in-

fo rmat ion to the cl inical T M D examina t ion? The sub-

j ec t iv i ty o f the tradit ional examina t ion can be t empered

with an objec t ive tempera ture measurement , and the

subject ive pain repor ted by patients can be conf i rmed

or unconfir raed to s t rengthen a longi tudinal study. The

imaging technique o f the rmography is quite easy to

per fo rm on the face and is not a compl ica ted addi t ion

to the rout ine T M D examinat ion . 5°'51 The procedure is

wel l tolerated by patients; it is not invas ive or unpleas-

ant. Subject~; showed interest in seeing the rmograms of

themselves . However , the proper cl inical thermo-

graphic techniques out l ined in the M e t h o d s sect ion are

necessary to obtain accurate T M J thermograms.

To propose further research projects, AT measure-

ments o f persons ove r t ime m a y prove to be useful in

longi tudinal studies o f or thodont ic patients undergoing

cont inual occlusal changes. Perhaps the percentage o f

persons who adapt easi ly to occlusal changes could be

measured as we l l as those persons who do not adapt. A

knowledge o f the inc idence o f nonadaptors ( T M D

patients) wou ld be useful in de l iver ing accurate in-

fo rmed consent in cl inical or thodont ic practice.

CONCLUSION

Invest igat ions to measure the leve l o f T M D in

var ious popula t ions have re l ied on cl inical examina t ion

and subject ive informat ion, both by s tandardized and

uns tandardized methods. The findings that thermo-

graphic imaging not only can separate normal patients

f rom painful c l icking patients but can correlate wel l

with cl inical palpat ion findings, indicat ing that ther-

mography could be an ob jec t ive tool for gather ing

T M D data. The l i terature has not yet seen a well-

control led, longi tudinal study of patients undergoing

or thodont ic treatment. The addi t ion of objec t ive ther-

mograph ic imaging could p rove to be va luable in

assessing the re la t ionship be tween or thodont ic treat-

ment and T M D symptoms in future studies.

We thank Drs. Glenn T. Clark, Susan A. Haake, and John A. Yagiela for their valuable assistance in the planning of the conduct of this study. We also would like to thank our dental student, Mr. Matt Jones, who conducted the clinical tests.

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Thermographic assessment of temporomandibular disorders symptomology during orthodontic treatment