Infrared thermography assessment of patients with temporomandibular disorders

Abstract

Objectives:

To assess patients with and without temporomandibular disorders (TMD) infrared thermography according to the differences in thermal radiance using quantitative sensitivity and specificity tests; and to evaluate the thermal asymmetry and the correlation of the thermal intensity with the intensity of pain upon palpation.

Methods:

This cross-sectional study performed a quantitative evaluation of clinical and thermographic examinations. The volunteers were evaluated for the presence of TMD using RDC/TMD (Diagnostic Research Criteria for Temporomandibular Disorders), and were divided into two groups: TMD group (n = 45); control group (n = 41), composed of volunteers without TMD, according to the Fonseca Anamnestic Index. The images were assessed for selected regions of interest for the masseter, anterior temporal and TMJ muscles. The mean values ​​of the areas of both groups were compared under the receiver operating characteristic curve. Spearman correlation analysis (non-parametric data) between pain level and mean temperature, by region, and the Pearson's χ² test was used to verify the association between the presence of temperature and pain asymmetry. The level of significance was set at p < 0.05.

Results:

Both Groups, with and without TMD, presented with absolute and non-dimensional mean temperature without statistical differences (p>0.05). When correlating temperature with intensity of pain upon palpation, a negative correlation was observed for the masseter muscle.

Conclusion:

Infrared Thermography resulted in low area under the curve, making it difficult to differentiate TMD via thermographic analysis. The intensity of pain upon palpation in patients with TMD may be accompanied by a decrease in local temperature.

Introduction

Temporomandibular disorders (TMD) is a collective term that refers to a set of changes that share common signs and symptoms and/or dysfunction in the region of the masticatory and temporomandibular joint (TMJ) muscles, such as painful opening of the mouth or yawning, cracking and a sensation of dislocation or blockage of the jaw, difficulties in chewing and a feeling of tiredness of the face.^1–5 TMD mainly affects females because they are more susceptible to this dysfunction.^6,7

The diagnosis of TMD is predominantly clinical, with the use of validated instruments such as RDC/TMD.⁸ Recently, DC/TMD (Diagnostic Criteria for Temporomandibular Disorders) has been used as a more suitable tool for both clinical and research environment approaches based on scientific evidence.⁹ Usually, the combination of the physical examination with the symptoms reported by the patient will provide important information for a precise diagnosis.¹⁰ TMD consists of a cyclical condition, and monitoring the patients using techniques to assess thermal/physiological conditions can lead to more precise monitoring over the course of the patient's period of follow-up.^11,12

Among the imaging techniques used for TMD diagnosis, from the muscular point of view, MRI allows for the morphological evaluation of the musculature, as well as the TMJ.¹³ However, it does not provide information on the physiological aspects of the region, such as microcirculation.^11,14

Among the latest technology, in the area of health, to assist with the diagnosis and for patient monitoring, infrared thermography has shown itself to be a great ally due to its advantages, namely it is non-invasive and employs a non-ionizing method; it is a painless technique, easy to perform, offering no risk to the patient and permits a physiological view of the region in real time.^10,11,15,16

Due to its advantages, thermography can be recommended as an additional test to be used on patients with TMD.^11,14 This technique can be applied to individuals with muscular TMD by virtue of changes in the local microcirculation due to muscular hyperactivity,^2,17 or with joint-related TMD, as the temperature in this region may increase in patients with painful joint symptoms.¹⁸

Therefore, the aim of this study was to analyze infrared thermography images according to the differences in the thermal radiance of the face of patients with and without TMD, using quantitative sensitivity and specificity tests, as well as correlating the mean temperature with pain intensity upon palpation.

Methods and materials

This was a quantitative, cross-sectional study based on clinical and thermographic examinations. Having been approved by the Research Ethics Committee, the treatment of patients with signs and symptoms of TMD, provided at the Paraíba State University Clinic and Infrared Thermography Laboratory, was published via digital media.

Employing inclusion and exclusion criteria, 86 volunteers, aged between 18 and 60, of both sexes, were examined in accordance with the RDC/TMD and the Fonseca Anamnestic Index,¹⁹ applied by a single, previously calibrated examiner. The volunteers were divided into two groups according to TMD diagnosis: (1) TMD group (n = 45), subtypes described in Table 1, below; (2) control group (n = 41): Patients not diagnosed with TMD.

Table 1.

Temporomandibular disorder diagnosis based on RDC/TMD findings.

Diagnosis	TMD group (n = 45)
Myofascial pain (Ia)	26
Myofascial pain with limited opening (Ib)	19
Disk displacement with reduction (IIa)	2
Disk displacement without reduction (IIb)	0
Disk displacement without reduction, and without limited opening (IIc)	2
Arthralgia (IIIa)	3

RDC/TMD, Diagnostic Research Criteria for Temporomandibular Disorders; TMD, temporomandibular disorders.

Patients with the following complaints or conditions were excluded from the study: toothache, fever, systemic changes (hypoglycemia, hypothyroidism or hyperthyroidism, hypertension, respiratory diseases, rheumatoid arthritis, fibromyalgia, pregnancy, rheumatological changes, hormonal disorders, neurological changes); cancer patients; patients undergoing treatment with myorelaxant drugs, analgesics and/or anti inflammatory medication, or who were receiving hormone replacement therapy; and patients who had facial scarring or papules.

Thermographic examination

For the purposes of the thermographic examination, all volunteers received instructions at the time of the initial screening in order to prevent external factors interfering with the acquisition of the images. The principal instructions were: do not apply make-up or lotion to the face; do not use sources of heat such as hairdryers or hair straighteners; do not take analgesics, corticoids, anti-inflammatory drugs; do not carry out any kind of physical exercise; and do not touch, rub or scratch the area of skin that is to be examined. Thermal examinations were performed in accordance with the guidelines advocated by the American Academy of Thermology.²⁰

The thermographic examinations were conducted in the Infrared Thermography Laboratory in a room with artificial fluorescent lighting and air conditioning, to maintain room temperature at 23 ± 1°C, and relative humidity of the air between 40 and 60%, verified by means of a Digital Hygro Thermometer (Minipa MT-242) placed close to the patient during image acquisition.¹⁰

The back walls of the examination room were lined with 25 mm thick expanded polystyrene sheets, crumpled aluminum foil (for the purposes of diffuse reflection) and black, rubberized material, forming an insulated thermal barrier against potential external heat sources, and minimizing reflection of thermal radiation that could interfere with the thermal image. In addition, to minimize the reflection of thermal radiation, it was recommended that, in addition to the volunteer, only the operator and assistant should be present in the room.

An FLIR T650sc handheld camera with infrared sensor, 25 mm lens and spatial resolution of 640 × 480 pixels, was used to capture the thermographic images. The thermographic camera was attached to a tripod and switched on 20 min prior to commencing the collection in order to stabilize the temperature, in line with manufacturer’s recommendations. The skin emissivity previously configured in the machine was 0.98,^14,17,21 while the camera-patient distance was set at 0.80 m.²²

For the acquisition of thermographic images, the volunteer was seated in a swivel-chair for 15 min prior to capture, maintaining an erect posture, with a Sagittal Plane perpendicular to the ground and Camper Plane (tragus of the ear to the ala of the nose) parallel to the ground, for the thermogram collections in right and left lateral position, under constant conditions.

Facial masks were made out of a flexible, plastic material to act as bilateral guides for the anatomical demarcation of the masseter, anterior temporal and TMJ muscles for subsequent analysis of the thermogram. The masseter muscle (R and L) was divided into thirds: upper, middle and lower; the anterior temporal muscle (R and L) into two quadrants; and the TMJ (R and L) into one quadrant, totaling five unilateral regions of interest (ROI), the basis being the points recommended by the RDC/TMD for palpation.

Data analysis

To begin with, a descriptive, statistical analysis was carried out in order to characterize both groups of volunteers, in terms of absolute and percentage frequencies for the categorical variables, e.g. sex and age, as well as central tendency and variability measures for the quantitative variables (body mass index, BMI).

All the images were analyzed at random using the software application FLIR Tools, v. 6.4, by a single, blinded examiner. The ROIs delineated on the facial mask were measured by circular tools approximately 22 mm in diameter, arranged side-by side (Figure 1), and absolute mean temperatures (°C) were recorded.

Figure 1.

Regions of interest: six points for the masseter muscle; two points for the anterior temporal muscle; one point in the TMJ. TMJ, temporomandibular joint.

The non-dimensional temperature, that is independent of body and room temperature, was calculated individually, using the following formula:

$${\displaystyle Non-dimensionalvalue=\frac{\left(Meantemperatureofthepoint-Roomtemperature\right)}{\left(Tympanictemperature-Roomtemperature\right)}}$$

Normalized values (θ), ranged from 0 to 1. Interpreting the above equation, 0 corresponds to room temperature while one equates to (central) tympanic temperature, making it possible to correct the effect of the body metabolism, to compare temperatures between individuals and express actual body temperature.²³

Using the mean values, the area under the ROC (receiver operating characteristic) curve was analyzed to calculate the discriminatory power of the mean temperature and non-dimensional temperature by comparing patients with and without TMD. The following guidelines were adopted to interpret the accuracy of the values of the area under the ROC curve (AUC): poor (0.50 ≥ AUC < 0.60), satisfactory (0.60 ≥ AUC < 0.70), good (0.70 ≥ AUC < 0.80), very good (0.80 ≥ AUC < 0.90) and excellent (0.90 ≥ AUC ≤ 1).²⁴

Subsequently, considering just the data of those volunteers diagnosed with TMD, the absolute temperature means were correlated with the scores of pain upon palpation (0, no pain; 1, slight pain; 2, moderate pain; 3, severe pain) from axis I of the RDC/TMD, as a means to evaluate the correlation of the variation in thermal temperature with intensity of pain, for each ROI.

For this analysis, the Kolmogorov–Smirnov test was applied, confirming the non-normal distribution of data. The Spearman correlation analysis (nonparametric data) was then performed between the pain level and mean temperature in the group of patients with TMD.

Taking into consideration the clinical variability and asymmetry of patients affected by TMD, the values for right- and left-side absolute mean temperature and intensity of pain were subtracted one from the another. The thermal, facial asymmetry was classified for values greater than 0.4°C and for differences in the pain level greater than 1. Obeying this classification, the data were analyzed according to Pearson’s χ² test to check for an association between the presence of temperature and pain asymmetry on the right and left sides.

All the analyses were conducted using the software applications IBM SPSS Statistics, v. 20.0 and MedCalc, v. 18.11.3, adopting a confidence interval of 95% to obtain the estimates. The level of significance was set at p < 0.05.

Results

Table 2 shows the results of the cross-tabulation between the groups according to sociodemographic characteristics and BMI. It was found that the groups were homogeneous with regard to age (p = 0.637) and BMI (p = 0.247). As for sex (p = 0.014), there was a larger percentage of females in the group with TMD.

Table 2.

Cross-tabulation between the groups according to sociodemographic characteristics and body mass index.

Variables	Group
	G1 (TMD)		G2 (Control)		Total		p-value
	n	%	n	%	n	%
Sex							0.014a*
Male	10	22.2	19	47.5	29	34.1
Female	35	77.8	21	52.5	56	65.9
Age							0.637c
Mean (SD)	36.53	(12.27)	36.75	(16.42)	36.64	(14.29)
BMI						0.247b
Low weight (<18.5)	5	11.1	5	12.5	10	11.8
Optimum weight (≥18.5 and <25)	18	40.0	22	55.0	40	47.1
Overweight (≥25 and <30)	14	31.1	11	27.5	25	29.4
Obesity (≥30)	8	17.8	2	5.0	10	11.8
Total	45	100.0	40	100.0	85	100.0

BMI, body mass index; SD, standard deviation; TMD, temporomandibular disorders.

*p < 0.05.

^aPearson’s χ² test;

^bFisher’s exact test;

^cMann–Whitney test;

As displayed in Table 3, the data exhibited low, insignificant AUC values for mean temperature, ranging from 0.397 for the lower left masseter (CI 95% = 0.277–0.5180) to 0.531 (CI 95% = 0.406–0.655) for the middle right masseter. Low, insignificant values were also identified for non-dimensional temperature, ranging from 0.416 (CI 95% = 0.293–0.538) for the lower left masseter to 0.584 (CI 95% = 0.461–0.706) for the right anterior temporal muscle.

Table 3.

Analysis of ROC curve for mean temperature and non-dimensional temperature between patients with TMD and without TMD.

Variables	AUC	CI 95%		p-value
		Lower Limit	Upper Limit
Mean Temperature
Upper Masseter
R	0.514	0.390	0.638	0.819
L	0.402	0.282	0.522	0.12
Middle Masseter
R	0.531	0.406	0.655	0.628
L	0.429	0.307	0.552	0.263
Lower Masseter
R	0.517	0.393	0.64	0.792
L	0.397	0.277	0.518	0.104
Anterior Temporal
R	0.517	0.393	0.641	0.785
L	0.462	0.338	0.585	0.544
TMJ
R	0.48	0.357	0.604	0.755
L	0.416	0.294	0.538	0.185
Non-dimensional Temperature
Upper Masseter
R	0.499	0.375	0.623	0.986
L	0.421	0.299	0.543	0.211
Middle Masseter
R	0.521	0.396	0.645	0.741
L	0.429	0.305	0.553	0.262
Lower Masseter
R	0.534	0.411	0.658	0.585
L	0.416	0.293	0.538	0.181
Anterior temporal
R	0.584	0.461	0.706	0.185
L	0.500	0.376	0.624	1.000
TMJ
R	0.491	0.366	0.616	0.884
L	0.428	0.304	0.552	0.252

ROC, receiver operating characteristic; TMD, temporomandibular disorders; TMJ, temporomandibular joint.

Table 4 shows the results of the analysis of the correlation between pain level and mean temperature in the group of patients with TMD. Significant, negative correlation, albeit low, was found for the values evaluated in the middle left masseter (Spearman’s ρ = −0.298; p = 0.047) and lower left masseter (Spearman’s ρ = −0.299; p = 0.049), signaling the existence of a linear relationship between higher levels of pain and lower mean temperature.

Table 4.

Analysis of correction between pain level and mean temperature in the group of patients with TMD.

Variables	Coefficient of correlationa	p-value
Upper masseter
R	−0.151	0.322
L	−0.209	0.168
Middle masseter
R	−0.147	0.337
L	−0.298	0.047*
Lower masseter
R	−0.142	0.351
L	−0.299	0.046*
Anterior temporal
R	−0.064	0.677
L	−0.102	0.505
TMJ
R	0.088	0.567
L	−0.004	0.979

TMD, temporomandibular disorders; TMJ, temporomandibular joint.

*p < 0.05.

^aSpearman’s correlation;

According to Table 5, no significant association was found between the presence of temperature and pain asymmetry (p-values > 0.05). From a descriptive point of view, in the group of patients with TMD, temperature and pain asymmetry was lower for the anterior temporal region (n = 25; 73.5%) and higher for the middle masseter (n = 13; 54.2%).

Table 5.

Comparative analysis of the level of temperature and pain asymmetry between the right and left sides, in the group of patients with TMD.

Variables	Temperature asymmetry
	Yes		No		Total		p-value
	n	%	n	%	n	%
Pain asymmetry
Upper masseter							0.095a
Yes	7	35.0	15	60.0	22	48.9
No	13	65.0	10	40.0	23	51.1
Middle masseter							0.661a
Yes	13	54.2	10	47.6	23	51.1
No	11	45.8	11	52.4	22	48.9
Lower masseter							0.787a
Yes	8	42.1	12	46.2	20	44.4
No	11	57.9	14	53.8	25	55.6
Anterior temporal							0.704b
Yes	4	36.4	9	26.5	13	28.9
No	7	63.6	25	73.5	32	71.1
TMJ							0.815a
Yes	6	46.2	16	50.0	22	48.9
No	7	53.8	16	50.0	23	51.1

TMD, temporomandibular disorders; TMJ, temporomandibular joint.

*p < 0.05.

^aPearson’s χ² test;

^bFisher’s exact test;

Discussion

The groups were homogeneous in terms of age (p = 0.637) and BMI (p = 0.247), aiming to minimize secondary impacts on the thermographic analyses with regard to the TMD diagnosis via thermography, which has been tested in various studies.^14,15,25,26 However, the sample of volunteers contained more females in the TMD group due to the generally higher prevalence in the female sex.^6,7,27

The TMD diagnosis has been described as fundamentally clinical, based on the sum of signs observed in the functional evaluation of the stomatognathic system, associated with painful symptoms reported by the patient.³ From the standpoint of local tissue alteration, imaging examinations, such as radiographs, tomograms or magnetic resonance, do not always succeed in identifying or explaining the painful symptoms reported.^{7,10,13,28,29}

In an attempt to help with the diagnosis, less invasive techniques such as thermography have been proposed, however, the results of the studies have demonstrated some difficulty in identifying changes, considering the limited thermography in the diagnosis of TMD.^17,21,26,30

When evaluating the diagnostic method, the protocols for the collection and analysis of the images are considered to be important. As far as image collection is concerned, important factors, such as the distance between camera and patient (ROIs) and insulation of the back wall of the room, may exert an influence on the thermograms. A number of studies have used a distance of 1 m between camera and patient,^14,17,21 while others have taken thermal readings at a distance of 0.71 m ¹¹ and 0.80 m,²² the latter being the distance used for the present study, aiming to encapsulate as much of the patient as possible, thereby minimizing the effect of the room temperature. As for the thermal insulation using aluminum foil, polystyrene and rubberized material, used on the walls of the thermographic examination room, this is considered important to minimize the formation of thermal factors or artifacts,¹⁶ but has not been widely used^14,17 or described.²¹

The use of infrared thermography in a day-by-day clinical environment may not be as easy as it seems. The standardization of all protocols needed to ensure that all possible thermal changes related to the image acquisition room and patient’s habits do not interfere on the image data acquisition may be hard to replicate in a dental clinic. The image acquisition room must have a perfectly controlled room temperature; and a limited number of staff members should be allowed in the room. However, hospitals and universities could build proper rooms for infrared thermography image acquisition and properly benefit from this method’s advantages. The patient must follow meticulously the professional’s instructions for image acquisition, avoiding hot beverages, hot baths, exercises and other activities or substances that can affect their microcirculation before infrared thermography image acquisition. Yet, other medical exams also require patient collaboration to become an accurate diagnostic method.

With regard to the method of quantitative analysis of the thermal images, importance should be accorded to the choice of tool selected in the software, in order to delimit an accurate, representative area of the region in question. Rodrigues-Bigaton et al¹⁷ used linear tools and a square area positioned along the masseter and anterior temporal muscles in order to check mean temperature and correlation with regard to the diagnosis of myogenic TMD, however, none of the analytical methods was consistent and satisfactory. As the measurement using a localized tool was previously tested and also not recommended,^10,27 we adopted the circular tool for a better anatomical fit and greater representativeness of the thermal mean,^14,22 positioning it in accordance with the muscle thirds analyzed via the RDC/TMD and guided by the previously assembled facial mask.

For a statistical comparison of the data, the area under the ROC curve was analyzed (Table 3) with the aim of calculating the discriminating power of the mean and non-dimensional temperatures of the ROIs in patients with and without TMD. The results found that the values possessed a low level of accuracy, showing that the infrared thermography of the ROIs provided a low level of precision for the diagnosis.

Considering the variability of subtypes and various anatomical locations potentially affected in patients with muscular or mixed TMD, we chose to carry out secondary statistical analyses considering only those patients diagnosed with TMD, using the details of asymmetry and pain intensity identified via the RDC/TMD.

By evaluating mean temperature with intensity of pain upon palpation, as reported by the patient, a negative correlation was found in the level of pain in the region of the middle left masseter muscle (Spearman’s ρ = −0.298; p = 0.047) and lower left masseter (Spearman’s ρ = −0.299; p = 0.049) with the temperature in these regions, showing that as the pain increased the local temperature fell, a similar finding having been described in the literature.^11,15 This could be linked to the minimal thermal changes resulting from muscle pain, which is usually associated with a process of contraction of the muscle bands that leads to local ischemia and, in turn, to a reduction in microcirculation,²⁹ which may result in a reduction in temperature in the region of the surface of the masticatory muscle through vasoconstriction, depending on the muscular TMD condition.^2,11,31,32

Despite these findings and the possible explanations of the physiological mechanism, the complex nature of quantifying and correlating pain should be highlighted as distinct aspects are involved, among them subjectivity.²⁷ In the case of the correlation of pain with temperature, some studies made no association between intensity of pain and the temperature of the surface of the masticatory muscle,^2,14,17 while one study found an increase in temperature on the affected masseter and temporal muscles.³³

Stressing the importance of the thermal diagnosis based on body and facial symmetry between the right and left sides, with thermal variations in the order of 0.3–0.5°C, several studies have demonstrated greater thermal asymmetry in individuals with TMD,^31,34 also greater thermal asymmetry in the region of the anterior temporal muscle depending on the chronicity of the TMD condition.¹⁴ In this study, the results showed that no temperature or pain asymmetry was found in the ROIs of patients with TMD (Table 5).

Based on the results found, infrared thermography did not produce results that could satisfactorily contribute to the diagnosis of individuals with or without TMD. However, taking into consideration an individual who presents with this condition, depending on the degree of the TMD (primarily the more severe cases), this individual may be monitored via this method, using therapeutic resources for the treatment of patients affected by this dysfunction.^33,35,36 Thus, the greater the pain reported by the patient, it may be possible to observe a reduction in temperature, in line with the findings of the present study, validating studies found in the literature.^2,11,17

According to Melo et al,³⁷ studies related to the reliability of the use of thermography for the diagnosis of TMD are still few and far between in the literature. Therefore, considering the limitations and results found in this study, we would recommend that further studies be conducted for a better control of variables in the capture of images and in the homogeneity of the regions affected by TMD, and that applications also be carried out in the individual follow-up, with the aim of expanding and guaranteeing the use of infrared thermography as a tool to assist with TMD evaluation.

Conclusions

Infrared thermography resulted in a low AUC, making it difficult to differentiate the TMD condition through thermographic analysis. Patients with TMD do not present with asymmetric differences in temperature in the ROIs analyzed. Intensity of pain upon palpation in patients with TMD may be accompanied by a reduction in local temperature.