Assessment of the Sensitivity, Specificity, and Accuracy of Thermography in Identifying Patients with TMD

Background

Changes in body temperature have long been regarded as an important diagnostic factor. Recently, rapid development in infrared radiation technology and its conversion to a visible image have given rise to a new technique called thermography [1]. As a consequence, this method has made it possible to produce images reflecting the physiological processes of living organisms by observing the temperature distribution on the outer surface of an examined system in a dynamic way and without the need for any contact [1,2]. The use of the phrase “observation of temperature distribution on the outer surface” not only limits the area of investigation to the properties of this surface, but it also has deeper implications, especially if the observed system is a living organism [3]. Thermal heterogeneity (e.g., on the surface of facial skin) largely depends on the blood flow and the type of tissue located directly beneath it. Thus, the surface of the skin above the muscle tissue, which is characterized by high metabolic activity, emits more thermal radiation than the skin covering the bone or connective tissue. Therefore, thermography visualizes the thermal properties of tissue similar to how radiology illustrates anatomy [1–4]. The advanced analysis used in dynamic thermography thus makes it possible to detect vasomotor changes within layers of the skin, which may help explain vegetative pain syndrome [2,4,5].

The undeniable advantages of thermography, such as its non-invasive evaluation approach, the absence of ionizing radiation, and the relatively low costs involved, are sufficient to recommend its inclusion among the additional tests widely employed to diagnose temporomandibular dysfunction (TMD) [6]. The validity of using thermography for dental diagnostic purposes, especially in the diagnosis of temporomandibular dysfunctions of the masticatory motor system, is still under review [1,7–11]. Some previous studies confirmed the diagnostic efficiency of thermography in identifying subjects with TMD [12–14]. Infrared thermography is a tool that can be applied to individuals with myogenous TMD due to the changes in the microcirculatory dynamics (i.e., there is a decrease in the skin temperature due to compression of blood vessels conditioned by muscle hyperactivity) [12,15,16], whereas skin temperature over the TMJ is increased in individuals with joint pain [17]. Moreover, individuals with TMD exhibit greater asymmetry in skin temperature than do those without this condition [2,13,18].

This method has been also used for multiple purposes within medicine and in the field of dentistry [19,20]. Several studies have employed infrared thermography as an assessment tool for individuals with neck pain, breast cancer, and diabetic neuropathy [21–23]. Moreover, many studies have been performed on the use of thermography in the diagnosis of nerve injuries after surgery or trauma, in diagnosis of inflammation after the surgical removal of mandibular third molars, and in clinical research [19].

The purpose of the present study was to evaluate the sensitivity, specificity, and accuracy of thermography as a means of identifying patients with TMD. We hypothesized that there is no diagnostic efficiency of thermography in identifying patients with TMD.

Material and Methods

The research was approved by the Ethics Committee of the Pomeranian Medical University in Szczecin, Poland (number BN-001/45/07). All the patients were informed about the aim and research design and they gave their informed consent to all of the procedures performed.

The study sample comprised 50 patients (27 women and 23 men) ages 19.2 to 24.5 years (mean 22.43±1.04) with subjective symptoms of TMD (Ai II-III) and 50 patients (25 women and 25 men) ages 19.3 to 25.1 years (mean 22.21±SD 1.18) with no subjective symptoms of TMD (Ai I). Participants were selected from patients referred to the Orthodontic Department of the Pomeranian Medical University in Szczecin, Poland. The exclusion criteria for the study population were: depressive disorders, pain in other parts of the body, inflammations, taking painkillers and anti-depressants, periodontal diseases, and completed treatment of masticatory motor system dysfunctions. Patients who had already finished their orthodontic treatment and those who were undergoing treatment at the time of the study were also excluded.

The anamnestic interviews included the patients’ general medical history as well as detailed information about their masticatory motor system. They were conducted according to a 3-point anamnestic index of temporomandibular dysfunction – Ai (Table 1) [24,25].

Masticatory motor system function was assessed on the basis of a clinical examination and thermography. The clinical examination, involving a visual and an auscultatory assessment as well as palpation methods, made it possible to qualitatively and quantitatively evaluate the functioning of the masticatory system. Data obtained from the clinical study was analyzed using the clinical temporomandibular dysfunction index (Di) (Table 2). The results of the clinical temporomandibular dysfunction index (Di), based on the total number of points obtained during the tests, were interpreted according to the model shown in Table 3 [24,25].

Thermography was performed in tandem with a chewing test, during which the subject was asked to chew 8 g of Hubba Bubba gum (Wrigley, France) for 10 min. The chewing test helped to increase the diagnostic efficiency of thermography in identifying patients with TMD.

The thermographic examination was performed in accordance with the recommendations of the European Society of Thermology, by the same operator [14,26–28]. The thermographic procedures were conducted in a closed room at a controlled temperature of 22–24°C and with relative humidity of 50–70%. Use of heat-emitting equipment was kept to a minimum.

The participants in the study were told not to eat for at least 2 h prior to the test. Before the procedures, the patients were asked, if necessary, to pin up their hair to expose the area of the ear and temple. The facial skin was cleaned using a moistened tissue and cooled by a cold air-flow dryer for 15 s. A 20-min resting period was allowed for facial temperature equilibration. During the adaptation process, the patients did not undertake any physical activity, chew, or touch their facial skin.

Before the study, the participants underwent a dermatological examination to identify any possible skin inflammation (dermatitis) of various etiologies, such as inflammation of the hair follicles (folliculitis), allergic reactions, contact eczema, or enlarged veins.

The thermography was performed with a ThermaCAM TMSC500 (FLIR Systems AB, Sweden) independent thermal vision system equipped with a matrix composed of uncooled FPA (focal plane array) microvoltometer detectors. We used a built-in, 7.5-μm high-pass filter, which made it possible to measure infrared radiation in wavelengths ranging between 7.5 and 13 μm. The ThermaCAM TMSC500 thermovision unit had a thermal resolution of 0.07°C and an accuracy of 2%.

Both facial and neck thermograms were taken using right and left lateral projections in constant conditions with the patient sitting on the examination chair, with a distance of 1 m and a constant angle of 90° between the camera and the patient. To prevent reflections, a thick black material was placed directly behind the patient.

The recordings were performed prior to the chewing test (T0) and after the effort test (T10). To obtain the highest image quality, automatic calibration tools were used during the examinations, making it possible to optimize the level and range of the temperatures shown as well as the color palette and the highest contrast in all areas of the image. The emissability value of the skin considered for this study was 0.98.

Thermographic images were recorded using ThermaCAM Researcher 2001 and ThermaCAM Reporter 2000 Professional (FLIR Systems AB, Sweden) Software.

A metric analysis of the thermograms was carried out in selected regions of the face and neck marked by tools in a circle-shaped area with a 1-cm diameter (Figure 1):

Due to the possibility of shifts in individual thermograms of the examined subjects, each image was analyzed individually and corrections were made if necessary.

A quantitative assessment of the thermograms was performed using a “rain” scale. The analysis of the selected areas of the face and neck included absolute measurements specifying the maximum temperature values (Tmax). According to the literature [4,26], the difference between right and left zone temperatures (ΔT) was selected as the variable to identify patients with TMD. In subjects with bilateral symptoms, this variable also shows its diagnostic usefulness because the severity of symptoms on both sides is never identical.

The Kruskal-Wallis test, the median, and the Mann-Whitney U test were used to verify hypotheses regarding the presence or absence of differences between the mean values of the independent variables. A chi-square test was performed to identify relationships between discrete or qualitative variables. The accuracy of the classifier (a single variable or the whole model) together with a description of its sensitivity and specificity were calculated using receiver operating characteristic (ROC) curve analysis. An analysis of the ROC curve for variables such as maximum temperature values (Tmax) and absolute difference in temperature between the right and left side zones (ΔT) was based on mean measurements in 8 areas on the right and left side of the face and neck. This method made it possible to determine the optimal cut-off points for the specific misclassification costs and the a priori probabilities for the occurrence of the studied phenomenon. A level of P=0.05 was considered to be statistically significant.

Results

The results of the clinical examination of the functioning of the masticatory motor system according to the Di algorithm among patients with symptoms of temporomandibular dysfunction are presented in Table 4. This data analysis showed the severity of TMD in the study group. Mild temporomandibular dysfunction (Di I) was the most frequent form of dysfunction in women (24%) and men (22%). Moderate dysfunction (Di II) had by a similar frequency and occurred in 20% of women and 16% of men. However, severe dysfunction was observed far more rarely in the examined group (P<0.0426) in both women (10%) and men (8%).

A mathematical analysis of the ROC curve was used to assess the diagnostic efficiency of thermography in identifying patients with TMD regardless of the severity of TMD. The analysis of the ROC curve showed that the highest diagnostic efficiency in thermography was achieved for estimators of distribution of variables such as the absolute difference in temperature between the right and left side zones (ΔT). The diagnostic efficiency in the case of thermography for this variable both before the test (area under the ROC curve [AUC]=0.7422, standard error of mean – SEM=0.0464, P<0.0378, Table 5), and after the test (AUC=0.7920, SEM=0.0466, P<0.0231) was significantly higher than in the case of the maximum temperature (Tmax); before the test AUC=0.5134, SEM=0.0731 and after the test AUC=0.6461, SEM=0.0522, (Table 5).

The chewing test was a major factor that increased the efficiency of thermography in identifying patients with TMD. The results of examinations performed after the chewing test for the maximum temperature variable (Tmax, AUC=0.6461, P<0.0352, Table 5) and the absolute difference in temperature between the right and left side (ΔT, AUC=0.7920, P<0.0416, Table 5) showed a significant increase in diagnostic efficiency in patients with TMD compared with examinations made before the chewing test (Tmax, AUC=0.5134 and ΔT, AUC=0.7422, Table 5).

The thermographic examination showed 95.5% specificity in identifying patients with no symptoms of dysfunctions according to Di when the absolute difference in temperature between the right and left side (ΔT) zones was lower than 0.26°C (accuracy 52.4%) before the chewing test and 0.52°C (accuracy 56.3%) after the test (Table 5).

Discussion

LIMITATIONS:

The present study has the following limitations: 1) relatively small sample size, non-allocation of individuals based on the menstrual cycle and period of the day (these factors can influence skin temperature [31]); and 2) the acclimation time of the volunteers was 20 min at 22–24°C, whereas other authors suggest a shorter time of 8–16 min [32]. The subtle evaluation of diagnostic efficiency of thermography in identifying subjects with TMD needs further research with larger sample sizes.