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Accuracy and Reliability of Infrared Thermography in the Diagnosis of Arthralgia in Women With Temporomandibular Disorder
ACCURACY AND RELIABILITY OF INFRARED THERMOGRAPHY IN THE DIAGNOSIS OF ARTHRALGIA IN WOMEN WITH TEMPOROMANDIBULAR DISORDER Delaine Rodrigues-Bigaton, PT, PhD, a Almir Vieira Dibai Filho, PT, b Ana Cláudia de Souza Costa, PT, b Amanda Carine Packer, PT, b and Ester Moreira de Castro, PT c
ABSTRACT Objective: The purpose of this study was to determine the accuracy and reliability of infrared thermography in the diagnosis of arthralgia in women with temporomandibular disorder. Methods: Thirty women aged between 18 and 40 years were recruited for the study. The Research Diagnostic Criteria for Temporomandibular Disorders was used to allocate the volunteers to the control group (n = 15) and arthralgia group (n = 15). Both groups were submitted to infrared thermography of the temporomandibular joint (TMJ), followed by a punctual analysis of the images. The Mann-Whitney U test was used for the comparison of skin surface temperature between groups. The intraclass correlation coefficient was calculated to determine the reliability of the infrared image analysis. The receiver operating characteristic curve was used to determine the accuracy of the diagnosis. Results: Skin temperature was significantly greater over the left (P = .004) and right (P = .012) TMJ in the arthralgia group. The intraclass correlation coefficient ranged from 0.841 to 0.874. The area under the receiver operating characteristic curve ranged from 0.598 to 0.675. Conclusion: Excellent intrarater and interrater reliability was found in the analysis of the infrared images of the TMJ. However, infrared thermography demonstrated a low accuracy in the diagnosis of arthralgia in women with temporomandibular disorder. (J Manipulative Physiol Ther 2013;36:253-258) Key Indexing Terms: Temporomandibular Joint Disorder; Skin Temperature; Thermography
emporomandibular disorder (TMD) is a problem with a complex diagnosis 1-3 and etiology that affects several structures of the stomatognathic system, such as the masticatory muscles, temporomandibular joint (TMJ), and or joint disk. 4-7 A recent study reports that pain is the most prevalent symptom in TMD of either a muscle or joint origin. 7 A number of authors consider the identification of arthralgia based on the presence of pain upon palpation of the lateral and/or posterior region of the TMJ together with the patient's report of pain during movements of the mandible. 7-9 However, Emshoff and Rudisch 10 state that individuals with TMJ pain do not constitute a homogeneous
T
a
Associate Professor, Laboratory of Therapeutic Resources, Postgraduate Program in Physiotherapy, Methodist University of Piracicaba, Piracicaba, SP, Brazil. b Master's Degree Student, Laboratory of Therapeutic Resources, Postgraduate Program in Physiotherapy, Methodist University of Piracicaba, Piracicaba, SP, Brazil. c Undergraduate Student, Health Sciences School, Methodist University of Piracicaba, Piracicaba, SP, Brazil.
group and examinations that complement the clinical evaluation are important for a precise diagnosis. Regarding the studies that evaluated subjects with joint changes, Roh et al 11 used magnetic resonance for the identification of the association between disk displacement, degenerative alterations, and joint effusion in individuals with joint conditions. Moreover, a recent systematic review stresses the need for studies assessing the actual benefits of nuclear magnetic resonance and computed tomography in the evaluation of individuals with TMJ changes and advises caution in the request for imaging examinations, especially in cases of financial restriction. 12 Li et al 13 investigated the efficacy of ultrasound for the diagnosis of disk displacement,
Submit requests for reprint to: Almir Vieira Dibai Filho, PT, Rua Carlos Gomes da Silva, 101, Apto 601, Jatiúca, CEP 57036450, Maceió, Alagoas, Brazil (e-mail: [email protected]). Paper submitted January 4, 2013; in revised form February 23, 2013; accepted April 3, 2013. 0161-4754/$36.00 Copyright © 2013 by National University of Health Sciences. http://dx.doi.org/10.1016/j.jmpt.2013.04.006
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reporting that this examination is acceptable for ruling out some clinical suspicions but should be complemented with magnetic resonance. Another study stresses the need for standardization in the ultrasound examination for the evaluation of the TMJ. 14 Among the clinical evaluations used for the identification of TMJ pain, Look et al 9 report that the Research Diagnostic Criteria for Temporomandibular Disorders (RDC/TMD) is commonly used for the identification of arthralgia. However, the correct use of this measure requires the rater to undergo a training and calibration exercise. 8 An individual assessed by the RDC/TMD can be diagnosed with myofascial pain (Ia or Ib), disk displacement (IIa, IIb, or IIc), and/or joint changes (IIIa, IIIb, or IIIc). Thus, with regard to reliability, the literature 9 reports good reliability intrasite and intersite for myofascial pain without limited opening (Ia), myofascial pain with limited opening (Ib), disk displacement with reduction (IIa), and arthralgia (IIIa). However, for the diagnoses of disk displacement without reduction (IIb), disk displacement without reduction without limited opening (IIc), osteoarthritis (IIIb), and osteoarthrosis (IIIc), the values of intrasite and intersite reliability were poor. With regard to accuracy of RDC/TMD, the literature 9 shows the following values: Ia (65% of sensitivity and 92% of specificity), Ib (79% of sensitivity and 92% of specificity), IIIa (53% of sensitivity and 86% of specificity). For other intra-articular diagnoses, the accuracy was poor. In this context, even with the accuracy values below the desirable level, the RDC/TMD is the instrument better accepted by the scientific community for the diagnosis of TMD. Infrared thermography is another possible diagnostic tool for TMJ conditions. 15,16 This method is used to determine skin surface temperature based on the emission of infrared radiation from bodies with a temperature above absolute zero. Thermal imaging is also noninvasive method that offers no patient discomfort. 17-19 Studies have shown that the temperature of the TMJ is higher and thermal asymmetry is greater in individuals with TMD in comparison with a control group. 20-22 However, few studies have been carried out to assess the diagnostic accuracy of infrared thermography. The investigations conducted to date report that this equipment is accurate for the diagnosis of TMD. 15,16 Based on this sentence, the hypothesis tested herein is that infrared thermography is accurate for the diagnosis of arthralgia. Therefore, the aim of the present study was to determine the accuracy and reliability of infrared thermography in the diagnosis of arthralgia in women with TMD.
METHODS Study Design A cross-sectional study was carried out following approval from the Human Research Ethics Committee of
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the Methodist University of Piracicaba (São Paulo, Brazil) under protocol number 15/11. All volunteers agreed to participate by signing a statement of informed consent.
Population Seventy-seven women were recruited from the university community of the cities of Piracicaba and Americana, São Paulo, Brazil. The RDC/TMD 8 was used for the inclusion of volunteers with and without TMD. In the former group, women mandatorily diagnosed with arthralgia (IIIa) were included. The physiotherapist who applied the RDC/TMD was trained and calibrated according to the standards of the International RDC/TMD Consortium. The following were the exclusion criteria: younger than 18 years and older than 40 years; body mass index (BMI) greater than 25 kg/m 2; current orthodontic or physiotherapeutic treatment; current use of medications, such as analgesics, anti-inflammatory drugs, muscle relaxants, or vasoactive agents; systemic disease; history of facial trauma or TMJ surgery; head or neck radiation; and a diagnosis of osteoarthritis (IIIb) or osteoarthrosis (IIIc) on the RDC/TMD. Forty-seven volunteers were excluded following the application of the eligibility criteria: 37 did not have a diagnosis of IIIa on the RDC/TMD, 8 had a BMI over the established cutoff point, 1 was undergoing orthodontic treatment, and 1 was older than 40 years. Thus, the final sample was composed of 30 women, who were divided into 2 groups: control group, 15 volunteers without TMD, mean age of 20.73 ± 2.18 years, mean BMI of 21.30 ± 1.97 kg/m 2; and arthralgia group, 15 volunteers with TMD (IIIa), mean age of 24.46 ± 5.69 years, mean BMI of 21.73 ± 1.91 kg/m 2. As TMD can affect different structures of the stomatognathic system simultaneously (muscles, joint disk, and/ or TMJ), volunteers with diagnoses concomitant to arthralgia were included, as performed in a study carried out by Manfredini et al. 23 Thus, among the 15 volunteers with arthralgia, 10 also had a diagnosis of myofascial pain (Ia), 5 had a diagnosis of myofascial pain with limited mouth opening (Ib), 2 had a diagnosis of joint displacement with reduction (IIa), and 1 had a diagnosis of joint displacement without reduction and without limited range of motion (IIc).
Infrared Thermography For the examination, the volunteers remained in a room for 20 minutes with a controlled temperature (22°C ± 1°C) lit with fluorescent bulbs without the presence of heatgenerating electrical equipment or the incidence of direct air or sunlight. 19 The participants were instructed to avoid a hot bath or shower; the use of topical agents, creams, and
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Rodrigues-Bigaton et al Infrared Thermography and Arthralgia
Sample Calculation The sample size was determined based on the literature. 25 The outcome was the absolute skin surface temperature of the TMJ. For the calculation, 32.84°C ± 0.23°C and 33.81°C ± 0.83°C were used for the control and arthralgia groups, respectively. Considering a statistical power of 80% and an α of .05, 13 volunteers were determined for each group. The sample size calculation was performed using the Ene software version 3.0 (Barcelona, Spain).
Statistical Analysis
Fig 1. Analysis of infrared image based on point measurement of TMJ.
powders; the practice of vigorous exercise; and the ingestion of stimulating substances, such as caffeine or nasal decongestants, for 2 hours before the examination. 19,24 During the data collection, the volunteers remained seated in a chair with the trunk erect, feet supported on the floor, and hands supported on the thighs. The joint region to be analyzed was maintained free of clothing and personal objects, such as earrings or necklaces, and the hair was pulled back when necessary. A T360 infrared camera (FLIR Systems, Danderyd, Sweden) was used, being calibrated according to manufacturer. Emissivity of set to 0.98 and the device was stabilized for 10 minutes before the examination. Image capturing was performed at a distance of 100 cm from the volunteer to allow the framing of the region to be analyzed. Three images were taken of each volunteer, and the mean of the readings was calculated. Point measurements were made of the skin surface temperature over the left and right TMJ. Thermal asymmetry was determined by subtracting the temperature on one side from the temperature on the other side.
The Shapiro-Wilk test was used to determine the distribution of the data. As nonnormal distribution was found, the Mann-Whitney U test was used for the comparison of temperatures between groups, with the level of significance set to 5%. For the determination of interrater reliability, 2 previously trained independent raters analyzed the same images. For the determination of intrarater reliability, 1 rater analyzed images on 2 separate occasions with a 1-week interval. 26 The intraclass correlation coefficient (ICC) was calculated to determine intrarater and interrater reliability, using the classification established by Weir 27: values 1.00 to 0.81, excellent reliability; 0.80 to 0.61, very good; 0.60 to 0.41, good; 0.40 to 0.21, reasonable; and, finally, from 0.20 to 0.00, poor. The receiver operating characteristic (ROC) curve was used to determine the diagnostic accuracy (area under the curve), cutoff point, sensitivity, and specificity of infrared thermography, using the following classification: 0.5, result due to chance; greater than 0.5 to 0.7 or less, low accuracy; greater than 0.7 to 0.9 or less, moderate accuracy; greater than 0.9 to less than 1.0, high accuracy; and 1.0, perfect test. 28,29 Based on the study by Akobeng, 29 the determination of the best cutoff point was based on the lowest result of the expression (1 − sensitivity) 2 + (1 − specificity) 2. The SPSS software version 13.0 (Chicago, IL) was used for the statistical analysis.
RESULTS Analysis of Infrared Images All analyses were performed by examiners blinded to allocation of the volunteers to the groups with and without arthralgia. The QuickReport software version 1.1 (FLIR Systems) was used for the image analysis. A point was marked on the TMJ for the determination of the temperature. The auditory canal was used to locate the joint, which is found directly in front of this structure (Fig 1). The examiners who performed capturing and analyzing of infrared images had experience of at least 2 years, with use of infrared thermography both in clinical and research.
Excellent intrarater (left TMJ: ICC, 0.874; right TMJ: ICC, 0.841) and interrater (left TMJ: ICC, 0.865; right TMJ: ICC, 0.871) reliability was found in the analysis of the infrared images. Table 1 displays the skin surface temperatures in both groups. Significantly higher temperatures were found in the arthralgia group for both the left (P = .004) and right (P = .012) TMJ. No statistically significant difference between groups was found regarding thermal asymmetry (P = .107). Figure 2 displays the ROC curve of the skin surface temperature of the left and right TMJ and thermal
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Table 1. Comparison of skin surface temperature (in degrees Celsius) over TMJ in control and arthralgia groups Region
Control group
Arthralgia group
P
LTMJ RTMJ TMJA
33.20 (33.00, 33.70) 33.30 (32.90, 33.65) 0.30 (0.10, 0.45)
34.10 (33.20, 34.25) 33.70 (33.30, 34.00) 0.30 (0.20, 0.70)
.004 ⁎ .012 ⁎ .107
Values are expressed as median (first and third quartiles). LTMJ, left TMJ; RTMJ, right TMJ; TMJ, temporomandibular joint; TMJA, temporomandibular joint asymmetry. ⁎ P value b.05 (Mann-Whitney U test).
Fig 2. Receiver operating characteristic curve of skin surface temperature over right and left TMJ and thermal asymmetry. LTMJ, left TMJ; ROC curve, receiver operating characteristic curve; RTMJ, right TMJ; TMJA, temporomandibular joint asymmetry.
asymmetry. Table 2 displays the findings regarding the accuracy, best cutoff point, sensitivity, and specificity of infrared thermography. The area under the ROC curve of the point measurement of the left and right TMJ and thermal asymmetry ranged from 0.598 to 0.675.
DISCUSSION In the present study, infrared thermography demonstrated low accuracy in the diagnosis of arthralgia in women with TMD. This is in disagreement with findings described in previous studies carried out by Gratt et al 15 and McBeth and Gratt. 16 However, the importance of the choice of a criterion standard tool in diagnostic investigations should be stressed. The RDC/TMD 8,9 was used in the present study, whereas the diagnostic method in the studies cited
Table 2. Area under ROC curve, best cutoff point, sensitivity, and specificity of infrared thermography of TMJ Region
Area (95% CI)
Cutoff (°C)
Sensitivity (%)
Specificity (%)
LTMJ RTMJ TMJA
0.675 (0.561, 0.788) 0.654 (0.537, 0.771) 0.598 (0.480, 0.715)
33.75 33.65 0.35
57.8 62.2 48.9
77.8 75.6 73.3
CI, confidence interval; LTMJ, left TMJ; ROC curve, receiver operating characteristic curve; RTMJ, right TMJ; TMJ, temporomandibular joint; TMJA, temporomandibular joint asymmetry.
were computed tomography of the TMJ 15 and a clinical examination. 16 Moreover, the present study involved the use of a specific methodology for the evaluation of the volunteers, with the inclusion of women with arthralgia. The study by Gratt et al 15 included subjects with internal derangement and osteoathrosis, which are pathologic processes that compromise the structure of the TMJ more than arthralgia. The study by McBeth and Gratt 16 included subjects with TMD and who were in orthodontic treatment. Also in this context, Fikackova and Ekberg 30 do not recommend the use of infrared thermography for the diagnosis of arthralgia in individuals with TMD, stating that this equipment does not meet the necessary criteria for the diagnosis. Temporomandibular disorder has a multifactor etiology and multiple forms, with the possible simultaneous involvement of the masticatory muscles, TMJ, and joint disk. 5,7,31 These characteristics are directly related to the difficulty in establishing an adequate diagnostic assessment tool, despite the different scientific initiatives. 9,11-14 The literature reports the usefulness of infrared thermography in the diagnosis of other diseases, such as breast cancer, 32 type 2 diabetes, 33 dry eye syndrome, 34 and complex regional pain syndrome type 1. 35 A recent study involving a similar methodology as that used in the present study with regard to the eligibility criteria and statistical analysis found that infrared thermography of the central point of the masticatory muscles did not offer adequate accuracy in the diagnosis of myogenous TMD, 36 which is similar to the present findings. The volunteers with a diagnosis of arthralgia had a significantly higher absolute skin surface temperature in comparison with those without TMD. This is in agreement with findings described in studies conducted by Pogrel et al 25 and Gratt and Anbar. 37 However, in contrast to reports found in the literature, 16,20,37 no significant difference in thermal asymmetry was found between the 2 groups. A possible explanation for this regards the sample size, which was determined based on the absolute temperature of the TMJ as the outcome variable. 25 Thus, it is possible that differences in thermal asymmetry between individuals with and without arthralgia could be found in a larger sample. The low accuracy of infrared thermography does not impede its use for the measurement of joint temperature. Indeed, this equipment is useful for the assessment of the
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effects of therapeutic resources on joint pain and inflammation in individuals with TMD, such as laser therapy, 38-40 pulsed radio frequency energy therapy, 41 and splint therapy. 42,43 Moreover, the present study demonstrated excellent intrarater and interrater reliability in the analysis of infrared images, which is in agreement with findings described by Costa et al. 44 The present controlled study was conducted in the university community. Thus, although the volunteers have been diagnosed with arthralgia, the severity of the degree of the dysfunction may vary. The study conducted by Dibai Filho et al 24 with women with neck pain presents similar observation. Therefore, it is suggested that the future studies recruit subjects in tertiary chronic pain referral center. Finally, it is also suggested to evaluate the inflammatory biomarkers as a complement to the diagnosis of arthralgia, especially in the identification of synovitis and effusion.
Limitations The present study has the following limitations: the inclusion of only female volunteers; the inclusion of women with a mixed TMD diagnosis; the nonuse of an algometer to identify the pain threshold upon pressure of the TMJ; and the nonallocation of volunteers based on the menstrual cycle and period of the day, which are known to influence skin surface temperature. 45 Moreover, the acclimation time of the volunteers before the examination was 20 minutes at 22°C, whereas other authors suggest a shorter time (between 8 and 16 minutes), 46 and psychosocial factors, that is, expectation, prior pain experience, personal perception, and cultural variables, were not controlled in this study.
CONCLUSION In this study, excellent intrarater and interrater reliability was found in the analysis of the infrared images of the TMJ. However, based on the methodology used, infrared thermography demonstrated a low accuracy in the diagnosis of arthralgia in women with TMD.
ACKNOWLEDGMENTS The authors acknowledge National Council of Technological and Scientific Development (PIBIC/CNPq) for the scholarship granted and Prof Reginaldo Teixeira Coelho for his technical assistance.
FUNDING SOURCES AND POTENTIAL CONFLICTS OF INTEREST This study received funding from the National Council of Technological and Scientific Development (PIBIC/ CNPq). No conflicts of interest were reported for this study.
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20. Gratt BM, Sickles EA. Thermographic characterization of the asymptomatic temporomandibular joint. J Orofac Pain 1993; 7:7-14. 21. Gratt BM, Sickles EA, Wexler CE. Thermographic characterization of osteoarthrosis of the temporomandibular joint. J Orofac Pain 1993;7:345-53. 22. Gratt BM, Sickles EA, Wexler CE, Ross JB. Thermographic characterization of internal derangement of the temporomandibular joint. J Orofac Pain 1994;8:197-206. 23. Manfredini D, Cocilovo F, Favero L, Ferronato G, Tonello S, Guarda-Nardini L. Surface electromyography of jaw muscles and kinesiographic recordings: diagnostic accuracy for myofascial pain. J Oral Rehabil 2011;38:791-9. 24. Dibai Filho AV, Packer AC, Costa AC, Berni-Schwarzenbeck KC, Rodrigues-Bigaton D. Assessment of the upper trapezius muscle temperature in women with and without neck pain. J Manipulative Physiol Ther 2012;35:413-7. 25. Pogrel MA, Erbez G, Taylor RC, Dodson TB. Liquid crystal thermography as a diagnostic aid and objective monitor for TMJ dysfunction and myogenic facial pain. J Craniomandib Disord 1989;3:65-70. 26. van Maanen CJ, Zonnenberg AJ, Elvers JW, Oostendorp RA. Intra/interrater reliability of measurements on body posture photographs. Cranio 1996;14:326-31. 27. Weir JP. Quantifying test-retest reliability using the intraclass correlation coefficient and the SEM. J Strength Cond Res 2005;19:231-40. 28. Greiner M, Pfeiffer D, Smith RD. Principles and practical application of the receiver-operating characteristic analysis for diagnostic tests. Prev Vet Med 2000;45:23-41. 29. Akobeng AK. Understanding diagnostic tests 3: receiver operating characteristic curves. Acta Paediatr 2007;96:644-7. 30. Fikackova H, Ekberg E. Can infrared thermography be a diagnostic tool for arthralgia of the temporomandibular joint? Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2004;98: 643-50. 31. McNeill C. Management of temporomandibular disorders: concepts and controversies. J Prosthet Dent 1997;77:510-22. 32. Wishart GC, Campisi M, Boswell M, et al. The accuracy of digital infrared imaging for breast cancer detection in women undergoing breast biopsy. Eur J Surg Oncol 2010; 36:535-40. 33. Sivanandam S, Anburajan M, Venkatraman B, Menaka M, Sharath D. Medical thermography: a diagnostic approach for type 2 diabetes based on non-contact infrared thermal imaging. Endocrine 2012;42:343-51.
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34. Su TY, Hwa CK, Liu PH, et al. Noncontact detection of dry eye using a custom designed infrared thermal image system. J Biomed Opt 2011;16:046009. 35. Niehof SP, Beerthuizen A, Huygen FJ, Zijlstra FJ. Using skin surface temperature to differentiate between complex regional pain syndrome type 1 patients after a fracture and control patients with various complaints after a fracture. Anesth Analg 2008;106:270-7. 36. Dibai Filho AV, Packer AC, Costa AC, Rodrigues-Bigaton D. Accuracy of infrared thermography of the central point of masticatory muscles for the diagnosis of myogenous temporomandibular disorder. J Manipulative Physiol Ther 2013 [in press]. 37. Gratt BM, Anbar M. Thermology and facial telethermography: part II. Current and future clinical applications in dentistry. Dentomaxillofac Radiol 1998;27:68-74. 38. Bjordal JM, Couppé C, Chow RT, Tunér J, Ljunggren EA. A systematic review of low level laser therapy with locationspecific doses for pain from chronic joint disorders. Aust J Physiother 2003;49:107-16. 39. Fikácková H, Dostálová T, Vosická R, Peterová V, Navrátil L, Lesák J. Arthralgia of the temporomandibular joint and lowlevel laser therapy. Photomed Laser Surg 2006;24:522-7. 40. Frare JC, Nicolau RA. Clinical analysis of the effect of laser photobiomodulation (GaAs – 904 nm) on temporomandibular joint dysfunction. Rev Bras Fisioter 2008;12:37-42. 41. Al-Badawi EA, Mehta N, Forgione AG, Lobo SL, Zawawi KH. Efficacy of pulsed radio frequency energy therapy in temporomandibular joint pain and dysfunction. Cranio 2004; 22:10-20. 42. Ismail F, Demling A, Hessling K, Fink M, Stiesch-Scholz M. Short-term efficacy of physical therapy compared to splint therapy in treatment of arthrogenous TMD. J Oral Rehabil 2007;34:807-13. 43. Madani AS, Mirmortazavi A. Comparison of three treatment options for painful temporomandibular joint clicking. J Oral Sci 2011;53:349-54. 44. Costa AC, Dibai Filho AV, Packer AC, Rodrigues-Bigaton D. Intra and inter-rater reliability of infrared image analysis of masticatory and upper trapezius muscles in women with and without temporomandibular disorder. Rev Bras Fisioter 2013; 17:24-31. 45. Kurz A. Physiology of thermoregulation. Best Pract Res Clin Anaesthesiol 2008;22:627-44. 46. Roy A, Boucher JP, Comtois AS. Digitized infrared segmental thermometry: time requirements for stable recordings. J Manipulative Physiol Ther 2006;29:468.e1-10.
ABSTRACT Objective: The purpose of this study was to determine the accuracy and reliability of infrared thermography in the diagnosis of arthralgia in women with temporomandibular disorder. Methods: Thirty women aged between 18 and 40 years were recruited for the study. The Research Diagnostic Criteria for Temporomandibular Disorders was used to allocate the volunteers to the control group (n = 15) and arthralgia group (n = 15). Both groups were submitted to infrared thermography of the temporomandibular joint (TMJ), followed by a punctual analysis of the images. The Mann-Whitney U test was used for the comparison of skin surface temperature between groups. The intraclass correlation coefficient was calculated to determine the reliability of the infrared image analysis. The receiver operating characteristic curve was used to determine the accuracy of the diagnosis. Results: Skin temperature was significantly greater over the left (P = .004) and right (P = .012) TMJ in the arthralgia group. The intraclass correlation coefficient ranged from 0.841 to 0.874. The area under the receiver operating characteristic curve ranged from 0.598 to 0.675. Conclusion: Excellent intrarater and interrater reliability was found in the analysis of the infrared images of the TMJ. However, infrared thermography demonstrated a low accuracy in the diagnosis of arthralgia in women with temporomandibular disorder. (J Manipulative Physiol Ther 2013;36:253-258) Key Indexing Terms: Temporomandibular Joint Disorder; Skin Temperature; Thermography
emporomandibular disorder (TMD) is a problem with a complex diagnosis 1-3 and etiology that affects several structures of the stomatognathic system, such as the masticatory muscles, temporomandibular joint (TMJ), and or joint disk. 4-7 A recent study reports that pain is the most prevalent symptom in TMD of either a muscle or joint origin. 7 A number of authors consider the identification of arthralgia based on the presence of pain upon palpation of the lateral and/or posterior region of the TMJ together with the patient's report of pain during movements of the mandible. 7-9 However, Emshoff and Rudisch 10 state that individuals with TMJ pain do not constitute a homogeneous
T
a
Associate Professor, Laboratory of Therapeutic Resources, Postgraduate Program in Physiotherapy, Methodist University of Piracicaba, Piracicaba, SP, Brazil. b Master's Degree Student, Laboratory of Therapeutic Resources, Postgraduate Program in Physiotherapy, Methodist University of Piracicaba, Piracicaba, SP, Brazil. c Undergraduate Student, Health Sciences School, Methodist University of Piracicaba, Piracicaba, SP, Brazil.
group and examinations that complement the clinical evaluation are important for a precise diagnosis. Regarding the studies that evaluated subjects with joint changes, Roh et al 11 used magnetic resonance for the identification of the association between disk displacement, degenerative alterations, and joint effusion in individuals with joint conditions. Moreover, a recent systematic review stresses the need for studies assessing the actual benefits of nuclear magnetic resonance and computed tomography in the evaluation of individuals with TMJ changes and advises caution in the request for imaging examinations, especially in cases of financial restriction. 12 Li et al 13 investigated the efficacy of ultrasound for the diagnosis of disk displacement,
Submit requests for reprint to: Almir Vieira Dibai Filho, PT, Rua Carlos Gomes da Silva, 101, Apto 601, Jatiúca, CEP 57036450, Maceió, Alagoas, Brazil (e-mail: [email protected]). Paper submitted January 4, 2013; in revised form February 23, 2013; accepted April 3, 2013. 0161-4754/$36.00 Copyright © 2013 by National University of Health Sciences. http://dx.doi.org/10.1016/j.jmpt.2013.04.006
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reporting that this examination is acceptable for ruling out some clinical suspicions but should be complemented with magnetic resonance. Another study stresses the need for standardization in the ultrasound examination for the evaluation of the TMJ. 14 Among the clinical evaluations used for the identification of TMJ pain, Look et al 9 report that the Research Diagnostic Criteria for Temporomandibular Disorders (RDC/TMD) is commonly used for the identification of arthralgia. However, the correct use of this measure requires the rater to undergo a training and calibration exercise. 8 An individual assessed by the RDC/TMD can be diagnosed with myofascial pain (Ia or Ib), disk displacement (IIa, IIb, or IIc), and/or joint changes (IIIa, IIIb, or IIIc). Thus, with regard to reliability, the literature 9 reports good reliability intrasite and intersite for myofascial pain without limited opening (Ia), myofascial pain with limited opening (Ib), disk displacement with reduction (IIa), and arthralgia (IIIa). However, for the diagnoses of disk displacement without reduction (IIb), disk displacement without reduction without limited opening (IIc), osteoarthritis (IIIb), and osteoarthrosis (IIIc), the values of intrasite and intersite reliability were poor. With regard to accuracy of RDC/TMD, the literature 9 shows the following values: Ia (65% of sensitivity and 92% of specificity), Ib (79% of sensitivity and 92% of specificity), IIIa (53% of sensitivity and 86% of specificity). For other intra-articular diagnoses, the accuracy was poor. In this context, even with the accuracy values below the desirable level, the RDC/TMD is the instrument better accepted by the scientific community for the diagnosis of TMD. Infrared thermography is another possible diagnostic tool for TMJ conditions. 15,16 This method is used to determine skin surface temperature based on the emission of infrared radiation from bodies with a temperature above absolute zero. Thermal imaging is also noninvasive method that offers no patient discomfort. 17-19 Studies have shown that the temperature of the TMJ is higher and thermal asymmetry is greater in individuals with TMD in comparison with a control group. 20-22 However, few studies have been carried out to assess the diagnostic accuracy of infrared thermography. The investigations conducted to date report that this equipment is accurate for the diagnosis of TMD. 15,16 Based on this sentence, the hypothesis tested herein is that infrared thermography is accurate for the diagnosis of arthralgia. Therefore, the aim of the present study was to determine the accuracy and reliability of infrared thermography in the diagnosis of arthralgia in women with TMD.
METHODS Study Design A cross-sectional study was carried out following approval from the Human Research Ethics Committee of
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the Methodist University of Piracicaba (São Paulo, Brazil) under protocol number 15/11. All volunteers agreed to participate by signing a statement of informed consent.
Population Seventy-seven women were recruited from the university community of the cities of Piracicaba and Americana, São Paulo, Brazil. The RDC/TMD 8 was used for the inclusion of volunteers with and without TMD. In the former group, women mandatorily diagnosed with arthralgia (IIIa) were included. The physiotherapist who applied the RDC/TMD was trained and calibrated according to the standards of the International RDC/TMD Consortium. The following were the exclusion criteria: younger than 18 years and older than 40 years; body mass index (BMI) greater than 25 kg/m 2; current orthodontic or physiotherapeutic treatment; current use of medications, such as analgesics, anti-inflammatory drugs, muscle relaxants, or vasoactive agents; systemic disease; history of facial trauma or TMJ surgery; head or neck radiation; and a diagnosis of osteoarthritis (IIIb) or osteoarthrosis (IIIc) on the RDC/TMD. Forty-seven volunteers were excluded following the application of the eligibility criteria: 37 did not have a diagnosis of IIIa on the RDC/TMD, 8 had a BMI over the established cutoff point, 1 was undergoing orthodontic treatment, and 1 was older than 40 years. Thus, the final sample was composed of 30 women, who were divided into 2 groups: control group, 15 volunteers without TMD, mean age of 20.73 ± 2.18 years, mean BMI of 21.30 ± 1.97 kg/m 2; and arthralgia group, 15 volunteers with TMD (IIIa), mean age of 24.46 ± 5.69 years, mean BMI of 21.73 ± 1.91 kg/m 2. As TMD can affect different structures of the stomatognathic system simultaneously (muscles, joint disk, and/ or TMJ), volunteers with diagnoses concomitant to arthralgia were included, as performed in a study carried out by Manfredini et al. 23 Thus, among the 15 volunteers with arthralgia, 10 also had a diagnosis of myofascial pain (Ia), 5 had a diagnosis of myofascial pain with limited mouth opening (Ib), 2 had a diagnosis of joint displacement with reduction (IIa), and 1 had a diagnosis of joint displacement without reduction and without limited range of motion (IIc).
Infrared Thermography For the examination, the volunteers remained in a room for 20 minutes with a controlled temperature (22°C ± 1°C) lit with fluorescent bulbs without the presence of heatgenerating electrical equipment or the incidence of direct air or sunlight. 19 The participants were instructed to avoid a hot bath or shower; the use of topical agents, creams, and
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Rodrigues-Bigaton et al Infrared Thermography and Arthralgia
Sample Calculation The sample size was determined based on the literature. 25 The outcome was the absolute skin surface temperature of the TMJ. For the calculation, 32.84°C ± 0.23°C and 33.81°C ± 0.83°C were used for the control and arthralgia groups, respectively. Considering a statistical power of 80% and an α of .05, 13 volunteers were determined for each group. The sample size calculation was performed using the Ene software version 3.0 (Barcelona, Spain).
Statistical Analysis
Fig 1. Analysis of infrared image based on point measurement of TMJ.
powders; the practice of vigorous exercise; and the ingestion of stimulating substances, such as caffeine or nasal decongestants, for 2 hours before the examination. 19,24 During the data collection, the volunteers remained seated in a chair with the trunk erect, feet supported on the floor, and hands supported on the thighs. The joint region to be analyzed was maintained free of clothing and personal objects, such as earrings or necklaces, and the hair was pulled back when necessary. A T360 infrared camera (FLIR Systems, Danderyd, Sweden) was used, being calibrated according to manufacturer. Emissivity of set to 0.98 and the device was stabilized for 10 minutes before the examination. Image capturing was performed at a distance of 100 cm from the volunteer to allow the framing of the region to be analyzed. Three images were taken of each volunteer, and the mean of the readings was calculated. Point measurements were made of the skin surface temperature over the left and right TMJ. Thermal asymmetry was determined by subtracting the temperature on one side from the temperature on the other side.
The Shapiro-Wilk test was used to determine the distribution of the data. As nonnormal distribution was found, the Mann-Whitney U test was used for the comparison of temperatures between groups, with the level of significance set to 5%. For the determination of interrater reliability, 2 previously trained independent raters analyzed the same images. For the determination of intrarater reliability, 1 rater analyzed images on 2 separate occasions with a 1-week interval. 26 The intraclass correlation coefficient (ICC) was calculated to determine intrarater and interrater reliability, using the classification established by Weir 27: values 1.00 to 0.81, excellent reliability; 0.80 to 0.61, very good; 0.60 to 0.41, good; 0.40 to 0.21, reasonable; and, finally, from 0.20 to 0.00, poor. The receiver operating characteristic (ROC) curve was used to determine the diagnostic accuracy (area under the curve), cutoff point, sensitivity, and specificity of infrared thermography, using the following classification: 0.5, result due to chance; greater than 0.5 to 0.7 or less, low accuracy; greater than 0.7 to 0.9 or less, moderate accuracy; greater than 0.9 to less than 1.0, high accuracy; and 1.0, perfect test. 28,29 Based on the study by Akobeng, 29 the determination of the best cutoff point was based on the lowest result of the expression (1 − sensitivity) 2 + (1 − specificity) 2. The SPSS software version 13.0 (Chicago, IL) was used for the statistical analysis.
RESULTS Analysis of Infrared Images All analyses were performed by examiners blinded to allocation of the volunteers to the groups with and without arthralgia. The QuickReport software version 1.1 (FLIR Systems) was used for the image analysis. A point was marked on the TMJ for the determination of the temperature. The auditory canal was used to locate the joint, which is found directly in front of this structure (Fig 1). The examiners who performed capturing and analyzing of infrared images had experience of at least 2 years, with use of infrared thermography both in clinical and research.
Excellent intrarater (left TMJ: ICC, 0.874; right TMJ: ICC, 0.841) and interrater (left TMJ: ICC, 0.865; right TMJ: ICC, 0.871) reliability was found in the analysis of the infrared images. Table 1 displays the skin surface temperatures in both groups. Significantly higher temperatures were found in the arthralgia group for both the left (P = .004) and right (P = .012) TMJ. No statistically significant difference between groups was found regarding thermal asymmetry (P = .107). Figure 2 displays the ROC curve of the skin surface temperature of the left and right TMJ and thermal
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Table 1. Comparison of skin surface temperature (in degrees Celsius) over TMJ in control and arthralgia groups Region
Control group
Arthralgia group
P
LTMJ RTMJ TMJA
33.20 (33.00, 33.70) 33.30 (32.90, 33.65) 0.30 (0.10, 0.45)
34.10 (33.20, 34.25) 33.70 (33.30, 34.00) 0.30 (0.20, 0.70)
.004 ⁎ .012 ⁎ .107
Values are expressed as median (first and third quartiles). LTMJ, left TMJ; RTMJ, right TMJ; TMJ, temporomandibular joint; TMJA, temporomandibular joint asymmetry. ⁎ P value b.05 (Mann-Whitney U test).
Fig 2. Receiver operating characteristic curve of skin surface temperature over right and left TMJ and thermal asymmetry. LTMJ, left TMJ; ROC curve, receiver operating characteristic curve; RTMJ, right TMJ; TMJA, temporomandibular joint asymmetry.
asymmetry. Table 2 displays the findings regarding the accuracy, best cutoff point, sensitivity, and specificity of infrared thermography. The area under the ROC curve of the point measurement of the left and right TMJ and thermal asymmetry ranged from 0.598 to 0.675.
DISCUSSION In the present study, infrared thermography demonstrated low accuracy in the diagnosis of arthralgia in women with TMD. This is in disagreement with findings described in previous studies carried out by Gratt et al 15 and McBeth and Gratt. 16 However, the importance of the choice of a criterion standard tool in diagnostic investigations should be stressed. The RDC/TMD 8,9 was used in the present study, whereas the diagnostic method in the studies cited
Table 2. Area under ROC curve, best cutoff point, sensitivity, and specificity of infrared thermography of TMJ Region
Area (95% CI)
Cutoff (°C)
Sensitivity (%)
Specificity (%)
LTMJ RTMJ TMJA
0.675 (0.561, 0.788) 0.654 (0.537, 0.771) 0.598 (0.480, 0.715)
33.75 33.65 0.35
57.8 62.2 48.9
77.8 75.6 73.3
CI, confidence interval; LTMJ, left TMJ; ROC curve, receiver operating characteristic curve; RTMJ, right TMJ; TMJ, temporomandibular joint; TMJA, temporomandibular joint asymmetry.
were computed tomography of the TMJ 15 and a clinical examination. 16 Moreover, the present study involved the use of a specific methodology for the evaluation of the volunteers, with the inclusion of women with arthralgia. The study by Gratt et al 15 included subjects with internal derangement and osteoathrosis, which are pathologic processes that compromise the structure of the TMJ more than arthralgia. The study by McBeth and Gratt 16 included subjects with TMD and who were in orthodontic treatment. Also in this context, Fikackova and Ekberg 30 do not recommend the use of infrared thermography for the diagnosis of arthralgia in individuals with TMD, stating that this equipment does not meet the necessary criteria for the diagnosis. Temporomandibular disorder has a multifactor etiology and multiple forms, with the possible simultaneous involvement of the masticatory muscles, TMJ, and joint disk. 5,7,31 These characteristics are directly related to the difficulty in establishing an adequate diagnostic assessment tool, despite the different scientific initiatives. 9,11-14 The literature reports the usefulness of infrared thermography in the diagnosis of other diseases, such as breast cancer, 32 type 2 diabetes, 33 dry eye syndrome, 34 and complex regional pain syndrome type 1. 35 A recent study involving a similar methodology as that used in the present study with regard to the eligibility criteria and statistical analysis found that infrared thermography of the central point of the masticatory muscles did not offer adequate accuracy in the diagnosis of myogenous TMD, 36 which is similar to the present findings. The volunteers with a diagnosis of arthralgia had a significantly higher absolute skin surface temperature in comparison with those without TMD. This is in agreement with findings described in studies conducted by Pogrel et al 25 and Gratt and Anbar. 37 However, in contrast to reports found in the literature, 16,20,37 no significant difference in thermal asymmetry was found between the 2 groups. A possible explanation for this regards the sample size, which was determined based on the absolute temperature of the TMJ as the outcome variable. 25 Thus, it is possible that differences in thermal asymmetry between individuals with and without arthralgia could be found in a larger sample. The low accuracy of infrared thermography does not impede its use for the measurement of joint temperature. Indeed, this equipment is useful for the assessment of the
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effects of therapeutic resources on joint pain and inflammation in individuals with TMD, such as laser therapy, 38-40 pulsed radio frequency energy therapy, 41 and splint therapy. 42,43 Moreover, the present study demonstrated excellent intrarater and interrater reliability in the analysis of infrared images, which is in agreement with findings described by Costa et al. 44 The present controlled study was conducted in the university community. Thus, although the volunteers have been diagnosed with arthralgia, the severity of the degree of the dysfunction may vary. The study conducted by Dibai Filho et al 24 with women with neck pain presents similar observation. Therefore, it is suggested that the future studies recruit subjects in tertiary chronic pain referral center. Finally, it is also suggested to evaluate the inflammatory biomarkers as a complement to the diagnosis of arthralgia, especially in the identification of synovitis and effusion.
Limitations The present study has the following limitations: the inclusion of only female volunteers; the inclusion of women with a mixed TMD diagnosis; the nonuse of an algometer to identify the pain threshold upon pressure of the TMJ; and the nonallocation of volunteers based on the menstrual cycle and period of the day, which are known to influence skin surface temperature. 45 Moreover, the acclimation time of the volunteers before the examination was 20 minutes at 22°C, whereas other authors suggest a shorter time (between 8 and 16 minutes), 46 and psychosocial factors, that is, expectation, prior pain experience, personal perception, and cultural variables, were not controlled in this study.
CONCLUSION In this study, excellent intrarater and interrater reliability was found in the analysis of the infrared images of the TMJ. However, based on the methodology used, infrared thermography demonstrated a low accuracy in the diagnosis of arthralgia in women with TMD.
ACKNOWLEDGMENTS The authors acknowledge National Council of Technological and Scientific Development (PIBIC/CNPq) for the scholarship granted and Prof Reginaldo Teixeira Coelho for his technical assistance.
FUNDING SOURCES AND POTENTIAL CONFLICTS OF INTEREST This study received funding from the National Council of Technological and Scientific Development (PIBIC/ CNPq). No conflicts of interest were reported for this study.
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