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Open Access 15.02.2024 | Brief Report

Thermography at the Elbow Among Patients with Rheumatoid Arthritis: A Comparison with Ultrasound-Detected Joint Inflammation Findings

verfasst von: York Kiat Tan, Rehena Sultana, Julian Thumboo

Erschienen in: Rheumatology and Therapy | Ausgabe 2/2024

Abstract

Introduction

There is a lack of data on the use of thermography for elbow joint inflammation assessment among patients with rheumatoid arthritis (RA). Hence, we aimed to compare thermography with ultrasonography (a more established imaging modality for joint inflammation assessment) in the assessment of inflammation in the elbows of patients with RA.

Methods

Standardised minimum (Tmin), maximum (Tmax) and average (Tavg) temperatures at each elbow (medial, lateral, posterior and anterior aspects) were summed to obtain the thermographic parameters MIN, MAX and AVG, respectively. Ultrasound parameters of elbow joint inflammation included total greyscale (TGS) and total power Doppler (TPD) scores. Pearson’s correlation coefficient was utilized for correlation analysis between parameters. The relationship between parameters was characterized using simple linear regression.

Results

Sixty elbows were evaluated from 30 patients with RA in this cross-sectional study. Thermographic parameters (MIN, MAX and AVG) showed significant correlation (P < 0.05) with (1) TPD scores at both elbows (correlation coefficient ranging 0.40 to 0.55) and (2) TGS scores at the right elbow (correlation coefficient ranging 0.39 to 0.42). A statistically significant relationship (P values ranging from 0.002 to 0.033) between parameters was demonstrable as follows: (1) MIN, MAX and AVG versus TPD scores (bilateral elbows) and (2) MIN, MAX and AVG versus TGS scores (right elbow).

Conclusion

Thermographic temperatures have been demonstrated to correlate with ultrasound-detected joint inflammation at the elbow in patients with RA. The association is more consistently observed with ultrasound PD joint inflammation than its GS counterpart.
Key Summary Points
Why carry out this study?
Thermography is a safe, non-invasive imaging technique that allows for a quick and objective measurement of joint surface temperature in patients with rheumatoid arthritis (RA)
There is a lack of data on its use for elbow joint inflammation assessment among patients with RA
The aim of this study is to compare thermography with ultrasonography in the assessment of inflammation in the elbows of patients with RA
What was learned from the study?
Thermographic findings at the elbow were shown to correlate significantly with ultrasound-detected joint inflammation among patients with RA (with the association more consistently observed with ultrasound power Doppler joint inflammation compared to its greyscale counterpart)
Thermography appears promising, and our findings are likely to pave the way for further research looking at potential clinical application(s) of thermal imaging for joint inflammation assessment at the elbow of patients with RA

Introduction

Thermography is a safe, non-invasive imaging technique that allows for a quick and objective measurement of joint surface temperature in patients with rheumatoid arthritis (RA) [1]. With technological advancement, modern thermal cameras are compact, highly portable and well suited for use as an adjunctive imaging tool in the rheumatologist office setting [2]. Being a contactless imaging modality, thermography also has the potential to be developed for remote assessment of patients with RA in telemedicine consultations whereby direct physical assessment of the joints is not possible [3, 4]. To date, the RA literature has described the use of thermography for joint inflammation assessment much less than other more established imaging techniques such as ultrasonography and magnetic resonance imaging (MRI) [2, 5]. Ultrasonography, as an imaging modality for musculoskeletal evaluation, has its advantages over thermography. For example, ultrasound can be used to directly visualize and guide injection at sites of specific anatomical structures (e.g. ultrasound-guided sub-acromial injection at the shoulders) [6] and can directly visualize specific pathologies in detail [such as evaluate specific tendon pathologies (e.g. tendon tears, calcification, etc.] at the shoulders [7]). In the past 2 decades, our knowledge on the application of ultrasound and MRI for joint assessment in RA/inflammatory arthritis has advanced by leaps and bounds [8, 9]. The European Alliance of Associations for Rheumatology (EULAR) has published its recommendations on the use of imaging of the joints in the clinical management of RA, which featured ultrasound and MRI, both of which are well recognized as being superior to conventional assessment methods [such as conventional radiography (CR) and clinical joint assessment] and able to detect subclinical disease predictive of subsequent disease flare and joint damage despite being in RA clinical remission [10]. Nonetheless, the use of ultrasound and MRI is not without its limitations. For example, a considerable amount of training is necessary for sonographers to attain proficiency while ultrasound assessment of multiple joint sites can be time-consuming and labour intensive. Additionally, the widespread use of MRI for RA joint inflammation assessment may not be feasible as this can be prohibitively expensive [11]. These limitations provide the rationale for exploring other imaging technologies such as thermography, which is low cost, simple and easy to use [1, 2].
The elbow joint has an important role in upper limb function and is the focus of our present study. The elbow joint is important in providing motion and stability to the upper limb [12, 13] and is commonly affected in RA, with 20% to 65% of patients with RA having elbow joint involvement [14, 15]. In a prospectively followed cohort involving 74 seropositive patients with RA, CR at 15-year follow-up revealed erosive involvement in 75 out of 148 (51%) elbows in 45 out of 74 (61%) patients [16]. Presently, there is a paucity of data on the use of thermal imaging for joint inflammation assessment at the elbow of patients with RA, with no published RA study to date comparing thermographic data with ultrasound-detected joint inflammation outcomes at the elbow joint. Hence, the aim of our present study is to compare thermographic findings with ultrasound-detected joint inflammation findings at the elbow in patients with RA. The hypothesis of our present study is that there is a significant correlation between joint inflammation detected by thermography and ultrasonography at the elbow of patients with RA.

Methods

In this single-site cross-sectional study, patients with RA included in the study (1) fulfilled the 2010 EULAR/American College of Rheumatology (ACR) RA classification criteria [17], (2) were either male or female patients aged from 21 to 99 years old, (3) had disease duration < 2 years and (4) were on first-line conventional disease-modifying anti-rheumatic drugs (DMARDs). Pregnant patient(s) were excluded from the study. Eligible patients were consecutively recruited from the outpatient rheumatology clinic at a local tertiary hospital. This study was approved by the SingHealth Centralised Institutional Review Board (CIRB) (2020/2669). The study was performed in accordance with the Helsinki Declaration of 1964 and its later amendments. All patients provided informed consent prior to participating in the study.

Baseline Characteristics of Study Participants

Baseline characteristics of study participants including age, gender, disease duration and underlying medications use (e.g. DMARDs and corticosteroid) at the time of recruitment were obtained from the hospital medical records. Baseline 28-joint disease activity score (DAS28) assessment was performed (on the same day as thermography and ultrasonography) by trained rheumatology nurses who were blinded to the results from the thermal and ultrasound imaging.

Imaging Assessment

Ultrasound imaging was carried out by a single rheumatologist experienced in musculoskeletal ultrasonography, while another trained study team member performed the thermal imaging while blinded to the findings of ultrasonography. Standardized ultrasound imaging was performed following published EULAR guidelines [18]. Ultrasonography was carried out using a Mindray M9 ultrasound machine (with a L14-6Ns linear probe) with the following machine settings: Doppler frequency, 5.7 MHz; pulse repetition frequency (PRF), 700 Hz. Both elbow joints were scanned at the anterior (humero-radial) and posterior fossa recesses.
Ultrasound greyscale (GS) synovial hypertrophy and power Doppler (PD) were scored semi-quantitatively (see Fig. 1 for examples of scoring) using a 0 to 3 severity scale (none = 0, mild = 1, moderate = 2 and severe = 3) based on previous established scoring methods shown to have acceptable inter/intra-observer reliability [19, 20].
Thermal imaging was performed based on previously established methods from the literature [2, 2124]. The participants were rested for 15 min prior to the start of thermography to allow for acclimatization as per usual practice [2, 2224]. The thermal imaging was conducted in a draft-free room (without windows) at a controlled ambient temperature of approximately 24 °C [21]. A high-performance portable thermal camera (FLIR T640) with the following settings was used to acquire the images: thermal sensitivity of < 30 milli-Kelvin at 30 °C; pixel resolution of 640 × 480; predefined emissivity value of 0.98 for skin [2, 23]. For standardization, both elbows were imaged with the thermal camera held 50 cm away from the medial, lateral, posterior and anterior aspects of each elbow. Thereafter, using the greyscale thermal images, the commonly utilized region of interest (ROI) manual segmentation approach [2, 2224] (performed by a trained study personnel while blinded to the ultrasound scoring outcomes) was followed to obtain the target ROIs at the medial, lateral, posterior and anterior aspects of each elbow (see Fig. 2). Finally, the following temperature measurements were recorded from the elbow ROIs: minimum (Tmin), maximum (Tmax) and average (Tavg) temperatures (in °C). A flow diagram (Fig. 3) summarizes the thermal and ultrasound assessments performed in this study.

Statistical Analysis

The thermographic parameters MIN, MAX and AVG are derived from the respective Tmin, Tmax and Tavg from each elbow as follows: MIN represents the sum of each Tmin from the medial, lateral, posterior and anterior aspects of each elbow; MAX represents the sum of each Tmax from the medial, lateral, posterior and anterior aspects of each elbow; AVG represents the sum of each Tavg from the medial, lateral, posterior and anterior aspects of each elbow. Similarly, the ultrasound GS and PD sub-scores at the joint recesses of each elbow were summed to obtain the Total GS (TGS) score and Total PD (TPD) score, respectively. Pearson’s correlation coefficient was derived for correlation analysis between the thermal and ultrasound imaging parameters, while the quantitative association between parameters was expressed using β coefficient with 95% confidence interval (95% CI) from simple linear regression. All tests were two-sided, and statistical significance was set at P < 0.05. Manually segmented ROIs (from a sample of elbow thermograms) were obtained at two time points (with 40 sets of Tmax, Tmin and Tavg segmented at least 2 weeks apart) and the intra-class correlation coefficient (ICC) was used to calculate the intra-observer reliability (single observer) for Tmax, Tavg and Tmin. The interpretation of ICC results was as follows: > 0.90 (excellent); 0.75 to 0.90 (good); 0.50 to 0.75 (moderate); < 0.50 (poor) [25]. SAS version 9.4 software (SAS Institute, Cary, NC, USA) was used for all statistical analyses.

Results

Baseline Characteristics of Study Participants

A total of 60 elbows were evaluated from 30 patients with RA in this cross-sectional study. The baseline characteristics of the participants were as follows: mean (SD) age, 57.7 (12.5) years; majority of the patients were female, 23/30 (76.7%) and Chinese, 23/30 (76.7%) with mean (SD) DAS28 scores of 3.83 (1.19) and mean (SD) disease duration of 7.3 (6.8) months. All patients were on one or more oral conventional DMARDs (methotrexate, sulfasalazine, hydroxychloroquine and leflunomide); 21/30 (70%) patients were on prednisolone.

Correlation Analysis for the Imaging Parameters

Table 1 summarises the correlation analysis for the thermal and ultrasound imaging parameters. All thermographic parameters (MIN, MAX and AVG) showed significant correlation (P < 0.05) with TPD scores at both elbows [correlation coefficient (95% CI) right elbow: MIN, MAX and AVG were 0.40 (0.04, 0.66), 0.47 (0.12, 0.70) and 0.43 (0.07, 0.68), respectively; correlation coefficient (95% CI) left elbow: MIN, MAX and AVG were 0.45 (0.10, 0.69), 0.55 (0.22, 0.75) and 0.52 (0.19, 0.74), respectively]. All thermographic parameters (MIN, MAX and AVG) showed significant correlation (P < 0.05) with TGS scores only at the right elbow [correlation coefficient (95% CI) right elbow: MIN, MAX and AVG were 0.39 (0.03, 0.66), 0.40 (0.04, 0.66) and 0.42 (0.07, 0.68), respectively], but not at the left elbow (all P > 0.05).
Table 1
Pearson’s correlation for the imaging parameters
Thermala versus ultrasound imaging parameters
Correlation coefficient (95% CI)
P value
Right elbow
 MIN versus Total GS score
0.39 (0.03, 0.66)
0.032*
 MAX versus Total GS score
0.40 (0.04, 0.66)
0.029*
 AVG versus Total GS score
0.42 (0.07, 0.68)
0.020*
 MIN versus Total PD score
0.40 (0.04, 0.66)
0.028*
 MAX versus Total PD score
0.47 (0.12, 0.70)
0.009**
 AVG versus Total PD score
0.43 (0.07, 0.68)
0.017*
Left elbow
 MIN versus Total GS score
0.15 (− 0.23, 0.48)
0.433
 MAX versus Total GS score
0.32 (− 0.05, 0.61)
0.086
 AVG versus Total GS score
0.26 (− 0.12, 0.56)
0.174
 MIN versus Total PD score
0.45 (0.10, 0.69)
0.012*
 MAX versus Total PD score
0.55 (0.22, 0.75)
0.002**
 AVG versus Total PD score
0.52 (0.19, 0.74)
0.003**
CI confidence interval, GS greyscale, PD power Doppler
aMAX, AVG and MIN are thermographic parameters derived from summing the respective Tmax, Tavg and Tmin at each elbow (medial, lateral, posterior and anterior aspects)
Statistically significant: *P < 0.05, **P < 0.01

Linear Regression Analysis for the Imaging Parameters

Table 2 summarizes the results from the simple linear regression analysis for the thermal and ultrasound imaging parameters. A statistically significant (P < 0.05) relationship was demonstrable between all thermographic parameters (MIN, MAX and AVG) and TPD scores at the bilateral elbows [regression coefficient (95% CI) right elbow: MIN, MAX and AVG were 0.09 (0.01, 0.16), 0.11 (0.03, 0.18) and 0.09 (0.02, 0.16), respectively; regression coefficient (95% CI) left elbow: MIN, MAX and AVG were 0.06 (0.01, 0.10), 0.08 (0.03, 0.13), and 0.07 (0.03, 0.11), respectively]. A statistically significant (P < 0.05) relationship was demonstrable between all thermographic parameters (MIN, MAX and AVG) and TGS scores only at the right elbow [regression coefficient (95% CI) right elbow: MIN, MAX and AVG were 0.15 (0.01, 0.28), 0.16 (0.02, 0.3) and 0.15 (0.03, 0.28), respectively], but not at the left elbow (all P > 0.05).
Table 2
Simple linear regression analysis for the imaging parameters
Thermala versus ultrasound imaging parameters
β coefficient (95% CI)
P value
Right elbow
 MIN versus Total GS score
0.15 (0.01, 0.28)
0.033*
 MAX versus Total GS score
0.16 (0.02, 0.30)
0.030*
 AVG versus Total GS score
0.15 (0.03, 0.28)
0.020*
 MIN versus Total PD score
0.09 (0.01, 0.16)
0.029*
 MAX versus Total PD score
0.11 (0.03, 0.18)
0.009**
 AVG versus Total PD score
0.09 (0.02, 0.16)
0.018*
Left elbow
 MIN versus Total GS score
0.04 (− 0.07, 0.16)
0.430
 MAX versus Total GS score
0.11 (− 0.02, 0.23)
0.086
 AVG versus Total GS score
0.08 (− 0.04, 0.19)
0.172
 MIN versus Total PD score
0.06 (0.01, 0.10)
0.012*
 MAX versus Total PD score
0.08 (0.03, 0.13)
0.002**
 AVG versus Total PD score
0.07 (0.03, 0.11)
0.003**
CI confidence interval, GS greyscale, PD power Doppler
aMAX, AVG and MIN are thermographic parameters derived from summing the respective Tmax, Tavg and Tmin at each elbow (medial, lateral, posterior and anterior aspects)
Statistically significant: *P < 0.05, **P < 0.01

Intra-Observer Reliability Testing

The intra-observer reliability testing results for Tmax, Tmin and Tavg were as follows: ICC (95% CI) for Tmax, Tmin and Tavg were 1.000 (1.000, 1.000), 0.998 (0.997, 0.999) and 0.998 (0.997, 0.999) respectively.

Discussion

There is presently a dearth of evidence supporting the use of thermography to assess joint inflammation at the elbow of patients with RA. Our study addresses this current knowledge gap by showing that thermographic findings at the elbow correlate significantly with ultrasound-detected joint inflammation in patients with RA. Specifically, temperature measurements were found to correlate with ultrasound PD joint inflammation at the bilateral elbow (although correlation with ultrasound GS joint inflammation was only observed at the right elbow). The association of thermographic temperatures with ultrasound PD joint inflammation at the elbow in patients with RA is of particular importance, because PD synovial vascularity generally indicates the presence of a more active joint inflammation [26, 27]. Even among patients with RA who are in clinical remission, synovial PD vascularity has been shown to be predictive of subsequent disease relapse as well as RA structural progression [28, 29]. In our present study, we did not specifically examine the use of thermal imaging among patients with RA in disease remission; therefore, future studies involving patients with RA in clinical remission will be necessary to clarify whether thermal imaging has any potential utility at the elbow for joint inflammation assessment among patients with RA in disease remission.
There has been an increase in interest in the use of thermography for joint assessment in patients with underlying inflammatory and degenerative arthritides based on publication trends in the past 10 years [30].
For RA, the hand is the most commonly included joint site for evaluation by thermal imaging, with fewer studies looking at thermal imaging of other joint sites [2]. Previous studies have shown that patients with RA demonstrated differences in thermographic findings not only at the hand [3133], but also at the knee [34] and foot [35] compared to healthy controls. One small-scale observational study involving thermal imaging at multiple upper and lower limbs joint sites (including the elbow) [24] attempted to categorize patients into high, medium and low RA activity using a decision tree classifier which showed excellent results (sensitivity 96% and specificity 92%). To the best of our knowledge, to date, there has been no published study comparing the use of thermography with ultrasonography for joint inflammation assessment at the elbow in patients with RA. A recent small-scale cross-sectional observational study (with 37 patients with RA) [36] and another knee study [37] (with 12 patients with RA and 18 patients with other forms of arthritis) have demonstrated higher thermographic temperatures at the hand (including wrist) and knee of patients, respectively, in the presence of positive ultrasound PD joint inflammation. Through the new findings from our study, we have added to the RA literature by showing a similar association exists between thermographic findings and ultrasound PD synovitis at the elbow of patients with RA. The use of thermography at the elbow in patients with RA appears promising and will require further validation in independent RA cohorts.
For joint inflammation at the elbow, it is presently unknown whether any scenarios exist whereby (1) either a thermal or ultrasound imaging modality can be used interchangeably, (2) one modality is clearly superior to the other and should be used or (3) both thermal and ultrasound imaging modalities provide complementary information and therefore both should be used. Hence, more investigative work in this area appears necessary, as the finding(s) may have implication(s) on how we select the most appropriate imaging tool(s) when monitoring and making therapeutic decisions for our patients with RA towards better treatment outcomes.
Our study has its limitations. Apart from the relatively small sample size, we have carried out the comparative analysis of thermal and ultrasound imaging at the elbow at a single time point using a cross-sectional study design. Hence, the usefulness of thermal imaging in reflecting ultrasound-detected joint inflammation at the elbow of patients with RA over time is presently unknown. Additionally, our study cohort included patients with early RA on oral conventional DMARDs, which may limit the generalizability of our results to other patient cohorts (e.g. those with long-standing disease or have different treatment profiles). Therefore, future RA studies with thermal and ultrasound imaging of the elbow performed at multiple time points will be required and ideally be tested out in patients with different clinical characteristics (e.g. those with longstanding disease) and treatment profiles (e.g. those on biologics treatment). Our study demonstrated high intra-observer consistency (single observer) for temperature measurements (Tmax, Tmin and Tavg) at the elbows of patients with RA. Future thermography studies in RA with two or more observers should further obtain data on inter-observer reliability.

Conclusion

In summary, we have shown that thermographic findings at the elbow correlate significantly with ultrasound-detected joint inflammation among patients with RA. Specifically, the association is more consistently observed with ultrasound PD joint inflammation (at the bilateral elbow) compared to its GS counterpart (only at the right elbow). The new findings from our current RA elbow study, especially in relation to thermographic findings and ultrasound PD joint inflammation, have helped advance our understanding of the use of thermography at the elbow of patients with RA. This, we believe, is likely to pave the way for further research looking at potential clinical application(s) of thermal imaging for joint inflammation assessment at the elbow of patients with RA.

Acknowledgements

We thank staff and colleagues from the study site for the support and help they provided in this study.
We thank the participants of the study.

Declarations

Conflict of Interest

York Kiat Tan, Rehena Sultana and Julian Thumboo declare that they have no competing interests.

Ethical Approval

This study was approved by the SingHealth Centralised Institutional Review Board (CIRB) (2020/2669). The study was performed in accordance with the Helsinki Declaration of 1964 and its later amendments. All patients provided informed consent prior to participating in the study.
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Metadaten
Titel
Thermography at the Elbow Among Patients with Rheumatoid Arthritis: A Comparison with Ultrasound-Detected Joint Inflammation Findings
verfasst von
York Kiat Tan
Rehena Sultana
Julian Thumboo
Publikationsdatum
15.02.2024
Verlag
Springer Healthcare
Erschienen in
Rheumatology and Therapy / Ausgabe 2/2024
Print ISSN: 2198-6576
Elektronische ISSN: 2198-6584
DOI
https://doi.org/10.1007/s40744-024-00648-3

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