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Abstract

Objective

Inflammation plays a central role in the pathophysiology of rheumatic diseases as well as in osteoarthritis. Temperature, which can be quantified using infrared thermography, provides information about the inflammatory component of joint diseases. This systematic review aims at assessing infrared thermography potential and limitations in these pathologies.

Design

A systematic review was performed on 3 major databases: PubMed, Cochrane library, and Web of Science, on clinical reports of any level of evidence in English language, published from 1990 to May 2021, with infrared thermography used for diagnosis of osteoarthritis and rheumatic diseases, monitoring disease progression, or response to treatment. Relevant data were extracted, collected in a database, and analyzed for the purpose of this systematic review.

Results

Of 718 screened articles 32 were found to be eligible for inclusion, for a total of 2094 patients. Nine studies reported the application to osteoarthritis, 21 to rheumatic diseases, 2 on both. The publication trend showed an increasing interest in the last decade. Seven studies investigated the correlation of temperature changes with osteoarthritis, 16 with rheumatic diseases, and 2 with both, whereas 2 focused on the pre-post evaluation to investigate treatment results in patients with osteoarthritis and 5 in patients with rheumatic diseases. A correlation was shown between thermal findings and disease presence and stage, as well as the clinical assessment of disease activity and response to treatment, supporting infrared thermography role in the study and management of rheumatic diseases and osteoarthritis.

Conclusions

The systematic literature review showed an increasing interest in this technology, with several applications in different joints affected by inflammatory and degenerative pathologies. Infrared thermography proved to be a simple, accurate, noninvasive, and radiation-free method, which could be used in addition to the currently available tools for screening, diagnosis, monitoring of disease progression, and response to medical treatment.

Keywords

infrared thermography joints osteoarthritis rheumatic diseases

Introduction

Inflammatory and degenerative joint diseases are common and progressive clinical entities, often associated with significant pain and functional disability. Among those with the greatest impact on society are osteoarthritis (OA) and rheumatic diseases such as rheumatoid arthritis (RA).¹ Osteoarthritis is considered a degenerative joint disease that affects all articular joints and is associated with degeneration of the joint cartilage and menisci, subchondral sclerosis, and inflammation of the synovial membrane. Osteoarthritis is the most common musculoskeletal disease and its prevalence, currently, around 20% to 30% of the population of the wealthier countries, will increase further with the progressive lengthening of life expectancy.^2,3 After cardiovascular diseases, OA is the most frequent cause of disability and a reduction in work activity. In addition, rheumatic diseases severely affect patient quality of life, involving joints, connective tissue, muscles, tendons, and fibrous tissue. In the general population, RA prevalence ranges from 0.5% to 1%,^4,5 being higher in women (in a female/male ratio of 2.5/1) in industrialized countries. It can occur at any age, with the peak incidence being between the age of 40 and 70 years.⁶ As OA, RA is a major cause of disability, so that at least 50% of those affected are unable to maintain a full-time job within 10 years of disease onset.⁷

Inflammation plays a central role in the pathophysiology of these diseases, in particular for RA, with an immune activation and leukocyte infiltration into the normally sparsely populated synovial compartment. Consequently, particularly in the first stages of the disease, tissue edema and fibrin deposition are prominent and can manifest clinically as joint swelling and pain.^6,8,9 Moreover, increasing evidence points to an important role of inflammation in OA, which can no longer be simply labeled as a “degenerative” disease. Inflammation promotes damage to joints and bones, causing joint-related functional deficits, especially in the earlier stages. The quantification of the inflammatory component in the disease processes could help to better target treatments to address this pathological aspect and to manage better each patient according to the specific disease phase and manifestation. In this light, the temperature is a key physical property, which can directly reflect the articular inflammatory processes. The increase above normal values is 1 of the 4 classical signs of inflammation, and thermal cameras can detect and quantify these temperature changes.^10
-13 Infrared thermography (IRT), a noninvasive and radiation-free method which provides information on the thermal, metabolic, and vascular conditions of the human body, could be therefore used in addition to the currently available tools for diagnosis, monitoring of disease progression, and response to medical treatment, in particular in relation to the inflammatory component of joint diseases.^14
-16

This systematic review aims at assessing the potential and limitations of thermography in the study of the inflammatory component of joint inflammatory and degenerative diseases.

Materials and Methods

A systematic review of the literature was performed on the articles dealing with inflammatory and degenerative joint diseases evaluated by IRT. The search was performed on May 7, 2021 on PubMed, Cochrane library, and Web of Science databases with the string: (Infrared Camera or Thermography or Infrared Thermography or Thermal Camera or IRT) AND (Arthritis or Osteoarthritis or OA or Rheumatoid Arthritis or RA). The list of references for each selected article was manually searched for more papers of interest. The guidelines for Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) were used ( Fig. 1 ).¹⁷ Two independent observers (G.S. and G.C.) conducted the screening process and analysis separately. First, the articles were screened by title and abstract. The following inclusion criteria were used during the initial screening of titles and abstracts: clinical reports of any level of evidence, written in the English language, published in the last 30 years (1990-2021), with IRT used for diagnosis of OA and rheumatic diseases, monitoring disease progression or response to medical treatment. Exclusion criteria were articles written in other languages, studies on animals, preclinical studies, reviews, case reports, studies not supported by statistical analysis, or studies analyzing other applications of IRT. In the second step, the full texts of the selected articles were screened, with further exclusions according to the previously described criteria. Afterward, articles not reporting any data on the correlation between IRT measurements and joints structural changes (documented by currently available tools like x-ray, computed tomography, MRI, and ultrasound) or clinical outcome were excluded. Relevant data (publication year, type of study, number of patients, pathology, joints involved, type of IRT system used, treatment assessed, results) were then extracted and collected in a unique database with the consensus of the 2 observers to be analyzed for the purposes of the present article ( Tables 1 and 2 ).

Figure 1.

PRISMA flow chart of the article selection process. PRISMA = Preferred Reporting Items for Systematic Reviews and Meta-Analysis; IRT = infrared thermography.

Table 1.

Characteristics of the OA Included Studies.

Author-Year-Journal	No. of patients	Age range	Male/Female	Pathology	Joint	Findings	Technology
Brito, C.J. (2020)¹⁸ Journal of Thermal Analysis and Calorimetry	70	69-81	24/46	OA	Knee	Different thermal skin response after an acute training session between OA subjects and control group	FLIR T335
Belcaro, G., (2019)¹⁹ Minerva Ortopedica E Traumatologica	45	44-55	45/0	OA	Knee	IRT detects the response to medical treatment in knee OA	FLIR 440
Bhowmik, M. K. (2016)²⁰ Thermosense: Thermal Infrared Applications	15	23-75	4/11	OA (/RA)	Knee	Different patterns of heat intensity distribution over affected and normal joints	FLIR T650sc
Jin, C. (2012)²¹ Journal of Medical and Biological Engineering	133	NA	NA	OA	Knee	Screening system of normal and abnormal cases, based on temperature patterns, with an accuracy rate of 85.5%, a sensitivity of 85.7%, and a specificity of 85.5%	FLIR SC620
Borojević, N. (2011)²² Periodicum Biologorum	13	NA	4/16	OA (/RA)	Hand	1. Joints’ absolute temperature differences between pathologic and control group 2. Different patterns of heat intensity distribution over affected and normal joints	Thermo Tracer TH7102WL
Denoble, A. E. (2010)²³ Clinical Medicine Insights	30	40-45	4/30	OA	Knee	Correlation between thermal patterns and radiological severity grade	Meditherm Med2000™
Mejersjö, C. (2008)²⁴ Journal of Oral Rehabilitation	29	39-76	2/27	OA	TMJ	1. Joints’ absolute temperature differences between pathologic and control group 2. Temperature did not correlate with medical treatment’s response and symptoms	Exacon MC 8900
Varju, G. (2004)²⁵ Rheumatology	91	46-87	18/73	OA	Hand	1. Correlation between thermal patterns and radiological severity grade 2. KL1 joints are warmer than KL0 joints, whereas KL 2, 3, 4 joints were colder than KL0 joints	Compix® PC2000e
Gratt, B. M. (1994)²⁶ Journal of Orofacial Pain	80	NA	27/53	OA	TMJ	Joints’ absolute temperature differences between pathologic and control group	Agema® 870 thermovision unit
Gratt, B. M. (1993)²⁷ Journal of Orofacial Pain	20	NA	4/16	OA	TMJ	1. Joints’ absolute temperature differences between pathologic and control group 2. Different patterns of heat intensity distribution over affected and normal joints	Draeger® 8000
Vargas ESNCO. (2020)²⁸ Reumatologia	25	54-78	6/19	OA	Knee	Superficial temperature of the knee was not associated with Kellgren-Lawrence grading scale	NA

OA = osteoarthritis; IRT = infrared thermography; RA = rheumatoid arthritis; TMJ = temporomandibular joint; KL = Kellgren-Lawrence.

Table 2.

Characteristics of the Rheumatic Diseases Included Studies.

Author-Year-Journal	No. of patients	Age range	Male/Female	Pathology	Joint	Findings	Technology
Umapathy, S. (2020)²⁹ Biomed Tech	60	35-47	NA	RA	Knee	1. Joints’ absolute temperature differences between pathologic and control group 2. IRT findings correlate with serologic markers of inflammation (ESR and CRP) 3. IRT correlate with CDUS findings	FLIR T400
Gizińska, M. (2019)³⁰ Journal of Thermal Analysis and Calorimetry	120	46-68	NA	RA	Foot	1. Joints’ absolute temperature differences between pathologic and control group 2. IRT did not correlate with CDUS findings	FLIR SC640
Laskari, K. (2019)³¹ Rheumatology	243	NA	NA	RA	MJ	1. Joints’ absolute temperature differences between pathologic and control group 2. IRT findings correlate with clinical score (DAS-28 and HAQ score) 3. IRT correlate with CDUS findings	RTM-01 RES
Pauk, J. (2019)³² Medical & Biological Engineering & Computing	30	43-69	NA	RA	Hand	After a cooling test the temperature Tmax-Tmin measured along the fingers line was higher in RA patients compared with healthy participants post-cooling and post-rewarming	FLIR E60bx
Jones, B.(2018)³³ Clinical Rheumatology	79	18-70	20/59	RA	Hand	1. Joints’ absolute temperature differences between pathologic and control group 2. IRT findings did not associate with clinical measures of disease activity	FLIR T300
Svaic, V. (2018)³⁴ Quantitative Infrared Thermography Conference	9	59-83	NA	RA	Hand	IRT detected the effect of cryotherapy in rheumatic hands	Fluke Ti25
Umapathy, S. (2018)³⁵ Journal of Medical and Biological Engineering	60	34-56	15/45	RA	Hand	1. Joints’ absolute temperature differences between pathologic and control group 2. the best joints to image are the MCPs of the second and third fingers	FLIR T400
Lerkvaleekul, B (2017)³⁶ Physiological Measurement	61	NA	NA	JIA	Wrist	1. Joints’ absolute temperature differences between pathologic and control group 2. IRT findings correlate with clinical outcome (swelling)	FLIR E60
Snekhalatha, U. (2017)³⁷ Journal of Engineering in Medicine	60	NA	NA	RA	Knee	1. IRT findings correlate with clinical score (DAS-28 and HAQ score) 2. IRT findings correlate with serologic markers of inflammation (ESR and CRP)	FLIR T400
Bhowmik, M. K. (2016)²⁰ Thermosense: Thermal Infrared Applications	15	23/75	0/15	OA (/RA)	Knee	Difference between contralateral Knees in Ra patients are minor compared with patients with OA, due to the similar spreading of RA inflammation in bilateral joints	FLIR T650
Lasanen, R (2015)³⁸ Physiological Measurement	20	4-16	9/11	JIA	Knee	Joints’ absolute temperature differences between pathologic and control group	FLIR T630
Capo, A (2015)³⁹ Microvascular Research Journal	21	38-67	11/10	PsA	Hand	1. Joints’ absolute temperature differences between pathologic and control group 2. IRT findings correlate with pain 3. IRT correlate with CDUS findings 4. Different thermal skin response after an acute training session between pathological subjects and control group	FLIR 660sc
Snekhalatha, U. (2015)⁴⁰ Journal of Engineering in Medicine	50	30-75	12/38	RA	Hand	1. Joints’ absolute temperature differences between pathologic and control group 2. The best joints to image are the MCP, the proximal interphalangeal joints, and the distal interphalangeal joints of the third finger	FLIR T400
Frize, M. (2012)⁴¹ Studies in Health Technology and Informatics	52	NA	NA	RA	MJ	1. Joints’ absolute temperature differences between pathologic and control group 2. The best joints to image are the MCPs of the second and thirrd fingers, and the proximal interphalangeal joints of the third finger 3. Automatic system to classify patients into the 3 levels of RA activity with a sensitivity of 96% and a specificity of 92%	Model NA (320 × 420 pixels, operating in the 7.5 μm-13 μm range)
Korman, P. (2012)⁴² Rheumatology International	47	46-66	8/39	RA	Hand	IRT detected the effect of cryotherapy in rheumatic hands	FLIR SC2000
Borojević, N. (2011)²² Periodicum Biologorum	8	NA	NA	OA (/RA)	Hand	Joints’ absolute temperature differences between pathologic and control group	Thermo Tracer TH7102WL
Frize, M (2011)⁴³ Sensors	30	19-70	14/16	RA	MJ	1. Joints’ absolute temperature differences between pathologic and control group 2. The best joints to image are the MCPs of the second and third fingers and the knees	Model NA (320 × 420 pixels, operating in the 7.5 μm-13 μm range)
Spalding SJ (2008)⁴⁴ Arthritis Research & Therapy	22	NA	NA	RA/JIA	MJ	The mean ± SD HDI in control joints was lower compared with joints with active rheumatic diseases	Meditherm med2000
Blyth, T. (1998)⁴⁵ British Journal of Rheumatology	82	NA	16/66	RA	Knee	IRT detect the response to 3 different medical treatments in rheumatic knees, revealing improvements compared with baseline, but without finding difference between the 3 groups	NA
MacDonald, A. G. (1994)⁴⁶ Clinical Rheumatology	28	NA	NA	RA	Knee	1. IRT findings correlate with serologic markers of inflammation (ESR and CRP) 2. IRT findings correlate with pain 3. IRT detect the response to intra-articular steroid injection in rheumatic knees	NA
Gatt A. (2020)⁴⁷ PloS One	83	25-70	15/68	RA	Foot	Patients with RA in clinical and radiological remission exhibit significantly different feet thermographic patterns compared with healthy controls	NA
Tan YK. (2020)⁴⁸ Clinical radiology	37	43-69	9/28	RA	Hand	Joints in patients with RA have significantly higher temperature readings when ultrasound-detected joint inflammation is present	FLIR T640
Tan YK. (2021)⁴⁹ Clinical radiology	37	43-69	9/28	RA	Hand	Novel use of combined thermal and ultrasound imaging in RA shows superiority to either imaging alone in terms of correlation with DAS-28	FLIR T640

RA = rheumatoid arthritis; IRT = infrared thermography; ESR = erythrocyte sedimentation rate; CRP = C-reactive protein; CDUS = color Doppler ultrasound; MJ = multiple joints; JIA = juvenile idiopathic arthritis; OA = osteoarthritis; MCP = metacarpophalangeal joints; TMJ = temporomandibular joint; PsA = psoriatic arthritis; DAS = Disease Activity Score; HAD = Health Assessment Questionnaire; HDI = Heat Distribution Index.

Results

The articles screened were 718 and of these 32 articles were found to be eligible for inclusion in the present review. Among these, 9 studies reported IRT application to OA, 21 to rheumatic diseases (17 RA, 2 juvenile arthritis, 1 both RA and juvenile arthritis, 1 psoriatic arthritis), 2 studies reported on both OA and RA ( Tables 1 and 2 ). In total, 2094 patients were studied, 735 women and 308 men (from 18 studies, whereas the other 14 studies did not specify the female/male ratio), with age ranging from 4 to 83 years. The publications with specific reference to disease, location, and patients studied are reported in Figure 2 , which shows an increasing trend with three-fourths of the papers of the last 30 years published in the last decade.

Figure 2.

Timeline of the included studies. MJ = multiple joints; TMJ = temporomandibular joint; OA = osteoarthritis; RA = rheumatoid arthritis; sphere size = number of patients included in the study.

Of the 32 articles, retrieved from the literature search, as shown in Tables 1 and 2 , 7 investigated the correlation of temperature changes with OA, 16 the correlation with rheumatic diseases, and 2 with both OA and rheumatic diseases. While 2 focused on the pre-post evaluation to investigate treatment results in patients with OA and 5 in patients with rheumatic diseases (1 study for each group also provided correlation data, between the temperature changes and the presence of OA and rheumatic disease). In the following chapters, results are summarized and detailed, distinguishing for OA and rheumatic diseases; moreover, for each group, correlational and pre-post studies are discussed separately.

Correlational Studies to Investigate OA-Related Temperature Changes

Of the 10 identified studies, 5 treated the knee joint,^{18,20,21,23,28} 3 the temporomandibular joint (TMJ),^24,26,27 and 2 the hand^22,25 ( Table 1 ). Four of these papers^22,24,26,27 reported on IRT used to identify the joints’ absolute temperature differences between patients affected by OA and the control group. All these studies reported significant differences between the 2 groups. Infrared thermography was also used to capture different patterns of heat distribution between healthy and pathological joints. One study²⁰ highlighted that, due to the difference in inflammation spreading, the mean, standard deviation, and contrast value of intensity distribution over IRT images could discriminate between the affected OA knee and normal knee. Another study²¹ also proposed an automated screening system for knee OA based on the different patterns of the temperature detected by IRT: 266 knee thermal images were acquired, and a knee feature extraction algorithm based on patella-centring was performed. The extracted features were fed to a support vector machine (SVM) classifier to perform an automated recognition. The SVM classifier had an accuracy rate of 85.5%, a sensitivity of 85.7%, and a specificity of 85.5% in detecting normal and abnormal cases. The feasibility of using the symmetry/asymmetry distribution of temperatures to discriminate between normal or abnormal thermal patterns, and so between normal or pathological joints, was investigated by 2 other studies,^22,27 although without reaching statistical significance.

Infrared thermography was also used in 3 papers to investigate the correlation between thermal patterns and radiological severity grade.^23,25,28 Two studies described a statistically significant correlation between temperatures and radiological disease severity based on the Kellgren-Lawrence (KL) classification.^23,25,50 Interestingly, one²⁵ also underlined that the temperature of joints with a radiological diagnosis of KL grade 1 was higher than those of KL 0, whereas temperatures of joints with more advanced OA grades were lower, probably due to the prevalence of degenerative OA features. The third study did not find a correlation between temperatures and KL classification.²⁸

Finally, one study¹⁸ reported on the difference in terms of lower limb thermal skin response after an acute training session between OA subjects and control group: the exercised knee affected by OA was significantly warmer than controls after exercise.

IRT-Based Studies to Investigate OA Treatment Outcome

Of the 2 identified studies, 1 treated the knee joint¹⁹ and 1 the TMJ²⁴ ( Table 1 ). These papers used IRT to monitor the response to medical treatments, Movardol in knee OA,¹⁹ and Diclofenac Sodium²⁴ in TMJ OA. The presence of a diffuse vascularization and inflammation (visible as “redness” and measurable by thermography) was significantly decreased with the supplement of Movardol considering the maximum temperature of the area and the global average temperature of the skin over the affected knee. On the contrary, the use of Diclofenac Sodium in patients with TMJ OA showed an improvement of the clinical outcomes after 3 months, but the skin surface temperature measured over the TMJ showed no difference between patients and controls.

Correlational Studies to Investigate Rheumatic Diseases Related to Temperature Changes

Of the 20 identified studies, 5 treated the knee joint,^{20,29,37,38,46} 8 the joints of the hand,^{22,32,33,35,39,40,48,49} 1 the wrist,³⁶ 2 the joints of the foot,^30,47 and 4 multiple joints^31,41,43,44 ( Table 2 ). Thirteen of these papers^{22,29-31,33,35,36,38-41,43,47} reported a statistical difference in joints’ absolute temperature between patients affected by rheumatic diseases and healthy controls. While in these studies the presence of an active inflammation process was detected by IRT as increased temperature, one study⁴⁴ used instead of a particular index, the HDI,¹¹ with the aim to avoid possible biases related to the measurement of the absolute temperature. The authors compared HDI values of 10 control wrists and metacarpophalangeal joints (MCPs) with 18 wrists with active arthritis and 9 MCPs with active arthritis (RA and juvenile arthritis). The HDI in joints with active arthritis was significantly higher compared with control joints. Moreover, they documented that an HDI cut-off of 1.3°C discriminated well between controls and patients with active arthritis. Infrared thermography was also used to capture different patterns of heat distribution between healthy and pathological joints²⁰; however, there was no difference between contralateral joints, due to the similar spreading of inflammation in bilateral joints of patients with RA.

Another approach was proposed by Pauk et al.:³² the authors found that the baseline temperature of fingers in patients with RA was not significantly different from healthy participants. However, the use of a cooling test allowed for increasing the temperature contrast between the maximum and the minimum temperature (Tmax-Tmin) along the finger’s axis. The temperature Tmax-Tmin measured along the finger’s line was higher in patients with RA compared with healthy participants post-cooling and post-rewarming. The authors attributed this finding to vasculitis, a relevant complication of an advanced stage of RA, which in 90% of patients manifests as focal ischemia of the fingers.

Four papers^35,40,41,43 also reported the best joints to image to detect the presence of active disease: the MCPs of the second and third fingers, the proximal interphalangeal joints of the third finger, the distal interphalangeal joints of the third finger, and the knees.

Eight studies reported a statistically significant correlation between joint temperature and clinical assessment of disease activity. In particular, IRT findings correlated with clinical scores (DAS-28 and HAQ score),^37,31 serologic markers of inflammation (ESR—erythrocyte sedimentation rate and CRP—C-reactive protein),^29,37,46 swelling,³⁶ and pain.^39,46 One study⁴¹ generated a classifier using decision trees (DTs—C5.0) to assess the level of severity, with the objective to separate patients into 3 classes of RA activity (low, medium, and high level): the data sets obtained from the calculations showed high performance of the DT classifier with a sensitivity of 96% and a specificity of 92%. Contrarily, in one paper,³³ the thermographic analysis was not associated with clinical measures of disease activity. There was no statistically significant correlation between joint temperature and clinical assessment of disease activity including DAS-28, swollen joints, ESR, and CRP.

Another important finding is the correlation between higher thermal values on the skin overlying joints and the presence of active inflammation assessed through color Doppler ultrasound (CDUS), which was reported in 6 papers. Among these, 5 studies^{29,31,39,48,49} documented a statistically significant correlation between IRT and CDUS, in particular one of them affirmed that the use of combined thermal and ultrasound imaging in RA showed superiority to either imaging alone in terms of correlation with DAS-28.⁴⁹ Instead, one paper³⁰ did not find significant results in the comparison of IRT joint average temperatures and CDUS inflammation findings.

Finally, one study³⁹ investigated the effect of a training session in patients with active psoriatic arthritis. The average baseline temperature was higher in this group compared with healthy control patients, and post-exercise, the authors documented a longer time needed from the end of the exercise to reach the minimum temperature compared with the control group. Accordingly, the authors underlined that, even in the absence of clinical symptoms, IRT can detect inflammatory-related processes resulting in skin temperature recovery alterations induced by exercise.

IRT-Based Studies to Investigate Rheumatic Diseases Treatment Outcome

Of the 4 identified studies, 2 treated the knee joint^45,46 and 2 the hand^34,42 ( Table 2 ). These papers used IRT to monitor the response of joints affected by RA to medical treatments, in particular, intra-articular steroid injection,⁴⁶ steroid associated with other drugs,⁴⁵ and cryotherapy.^34,42 MacDonald et al.⁴⁶ documented the effect of knee intra-articular steroid injections: after treatment, a clear improvement in MTI (a specific index used instead of absolute temperatures)⁵¹ was documented. Interestingly, the authors observed the same effect to a similar degree also in the contralateral not injected knee. Also, Blyth et al.,⁴⁵ evaluating 3 different treatments for knees affected by RA (triamcinolone hexacetonide—TH, TH with rifampicin, or TH with methotrexate), documented that IRT revealed improvements at 3 months of follow-up compared with baseline, although it could not find the difference among the 3 treatments. Cryotherapy was applied with different cooling agents (ice massage, cold air, and nitrogen vapor), all showing to induce temperature changes in hand’s joints.^34,42 Moreover, according to Svaic et al.,³⁴ cryotherapy was an effective physiotherapeutic method not only for lowering the joint temperature, but also for reducing the pain level and improving function in patients with RA, although with data collected only in the immediate phase after treatment.

Discussion

The main finding of this study is that IRT is an effective approach to document the presence of joint inflammation, with correlations to other imaging and clinical features documented for different joints affected both by OA and rheumatic diseases.

The evolution of IRT in the last 30 years led to its use for multiple purposes within human medicine, showing a great potential to improve the medical diagnosis and therapy monitoring within medical fields that include oncology, neurology, urology, rheumatology, and others.^52-54 Among these, results in orthopedics revealed that IRT is a sensitive and reliable method for diagnosis, evaluation, and monitoring of OA and rheumatoid diseases of different joints.^55,56 This systematic review underlined the correlation between surface skin temperature and joints’ inflammatory and degenerative diseases. Anatomic relations of the skin and circulatory system, together with increased metabolism and a richer blood supply to tissues beneath the surface, represent important factors in thermographic analysis. Tissues with a higher metabolism and a richer blood supply beneath the surface skin, as it happens in the inflammatory process, emit more infrared rays, allowing identifying and monitoring this component of OA and rheumatic diseases by IRT. Moreover, skin temperature can be taken into consideration also to study the physiology of thermoregulation and the thermal dysfunction associated with pain. Indeed, pain plays a main role in the course and treatment of joints’ inflammatory and degenerative diseases, and it is known that in knee OA there is a high prevalence of both nociceptive and neuropathic pain, which are both associated with an alteration of the thermal distribution of the human body in the form of hyperthermic or hypothermic regions.⁵⁷

Based on this rationale and the positive IRT results, in the last years, the trend of publications has significantly increased also thanks to the technological advance of the thermal cameras and the software used to generate and analyze the thermal images. In fact, the feasibility and reliability have considerably improved as a result of new standards and protocols in clinical practice. Skin temperature can be affected by many internal and external factors, such as circadian rhythm, metabolic rate, emotional state, physical activities, use of drugs, alcohol, and cigarettes, temperature, humidity, and light of the room in which the thermal images are captured, the distance and angle between the thermal cameras and patient, and other factors.^11,58 Accordingly, to minimize the possible biases due to these factors, the International Academy of Clinical Thermology (IACT) has developed guidelines and protocols for the equipment, design, and environmental conditions of the laboratory room, as well as for the management of the patient, which makes IRT more reliable and user-friendly.

The available literature investigated different aspects of the application of IRT in clinical practice. Infrared thermography has been used for diagnosis, monitoring of disease progression, and response to medical treatment mainly in patients with RA or other rheumatic diseases. In fact, inflammation plays a central role in the pathophysiology of these diseases, thus thermography can be easily used to detect the presence of illness, and it can discriminate well between healthy and pathological joints. While the usefulness of IRT in rheumatic diseases could be expected, increasing evidence also underlines the important role of inflammation in OA, which can no longer be simply labeled as a “degenerative” disease, especially in the earlier stages. In fact, many studies found a correlation between skin temperature and OA. The large majority of the studies found a correlation between the presence of illness (both in OA and rheumatic diseases) and either an increase of absolute skin temperature over the affected joints compared with healthy subjects or the presence of disease with different patterns of heat distribution, which reflected the spreading of joint inflammation. In the case of rheumatic diseases, the synovium is typically inflamed. Angiogenesis and vascular reorganization in the synovium are also usually observed patterns in patients with RA. The presence of synovitis may explain why patients with RA have overall warmer joints than healthy controls. As skin temperature rises within increased subcutaneous blood flow, IRT is a possible method for detecting joint inflammation in patients with arthritis. As the spreading of inflammation in bilateral joints is similar, and the feature differences are minor between contralateral joints, the increased values were identified through the comparison with healthy subjects.

On the contrary, in the OA setting, there is a degeneration of the joint surface and the subsequent release of degraded proteoglycans and proteolytic enzymes into the synovial fluid, leading to more degeneration and causing a secondary inflammation, with a growth of blood vessels and nerves into the synovium and deteriorated cartilage. Prostaglandins are important mediators of inflammation and in this case are powerful vasodilators that can also potentiate afferent C fiber sensitization. All of this causes the difference in inflammation spreading, absolute temperatures, and the values of intensity distribution over IRT images that could also discriminate between the affected joints and normal contralateral joints.

The feasibility of using the symmetry/asymmetry distribution of temperatures to discriminate between normal or abnormal thermal patterns, as well as between normal or pathological joints, could be further examined by developments in IRT technologies. In this regard, Jin et al.²¹ proposed an automated screening system for knee OA, precisely an effective knee feature extraction algorithm based on patella-centering and analyzed by a supervised machine learning classifier algorithm, an SVM. This SVM works by assigning labels to objects from a set of training examples. This method showed promising results with high accuracy, sensitivity, and specificity in detecting normal and abnormal cases. This system was based on different patterns of temperature. In fact, the absolute temperature may present biases due to the patient and environmental factors, thus specific indexes have been developed, and research in this direction could further increase the reliability of this technology and the ability to detect and distinguish different disease patterns.

In addition to the correlation with other imaging findings (such as x-ray and CDUS) documenting the presence of disease and/or joint inflammation, most of the studies were also able to confirm a correlation between IRT findings and the clinical assessment of disease activity detected by clinical scores, serologic markers, and clinical examination (pain, swelling, and function). In this regard, Frize and Ogungbemile⁴¹ even generated a classifier using IRT images to assess the level of severity in the patient group with a sensitivity of 96% and a specificity of 92%. Finally, 7 studies investigated the usefulness of IRT as a complementary diagnostic tool, showing the potential for monitoring disease progression and response to medical treatments such as steroids, cryotherapy, and exercise. Overall, all joints supported the usefulness of IRT, with some findings suggesting IRT being even more suitable to detect the presence of active disease at the MCPs’ joints, proximal and distal interphalangeal finger joints, and at the knee joints.

The overall literature findings support the potential of using IRT for different joints and for both OA and rheumatic diseases, to identify and classify the inflammatory component of the disease, as well as to monitor the treatment outcome. However, after decades of research, data are still based on a small number of patients for each clinical condition. Accordingly, the literature presents some limitations, which this systematic review reflects a small number of available studies reporting on a small number of patients. In addition, the heterogeneity of diseases treated in the studies and the different districts affected by pathology has hampered the possibility to perform a meta-analysis. The different technologies and protocols employed in the studies have been a further hindrance. In fact, this is an evolving field, starting from studies developing thermographic indexes like the one by Ring et al. in 1974, there are now different authors relying on different patterns, indexes, and technological settings.^59-61 However, even though the literature presents heterogeneous studies of low level, this systematic review still offered important indications, showing the feasibility and reliability of IRT as a complementary diagnostic tool in inflammatory and degenerative joints’ diseases. These findings could serve as a base for further studies toward the development of more specific high-level studies in which IRT is used following specific protocols and guidelines to minimize possible bias, evaluate the real potential of this approach, and help to develop and improve IRT technologies.

The evolution of IRT could further change the field, improving the performance of current technologies, and open the possibility for new clinical applications. For example, new-generation systems based on 3-dimensional and thermal imaging can provide measures of joint volume, shape, and thermal patterns that are more reliable than standard thermal measures.⁴⁴ The analysis of the available evidence already shows promise, and further technological advances may lead to an even more reliable and broader use of IRT not only in the research setting but also in the clinical practice, to improve the study and management of OA and rheumatic diseases.

Conclusions

Infrared thermography is a simple, accurate, noninvasive, and radiation-free method, which provides information on the thermal, metabolic, and vascular conditions of the human body, and could be therefore used in addition to the currently available tools for screening, diagnosis, monitoring of disease progression, and response to medical treatment. The systematic review of the literature showed an increasing interest in this technology, with several applications in different joints affected by inflammatory and degenerative pathologies. A correlation was shown between thermal findings and disease presence and stage, as well as the clinical assessment of disease activity and response to treatment, supporting the potential role of IRT in the study and management of OA and rheumatic diseases.

Footnotes

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Acknowledgments and Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Gianluigi Capone

References

Fusco

Skaper

Coaccioli

Varrassi

Paladini

Degenerative joint diseases and neuroinflammation. Pain Pract. 2017;17(4):522-32. doi:10.1111/papr.12551.

Cross

Smith

Hoy

Nolte

Ackerman

Fransen

, et al. The global burden of hip and knee osteoarthritis: estimates from the global burden of disease 2010 study. Ann Rheum Dis. 2014;73(7):1323-30. doi:10.1136/annrheumdis-2013-204763.

Zhang

Jordan

JM.

Epidemiology of osteoarthritis. Clin Geriatr Med. 2010;26(3):355-69. doi:10.1016/j.cger.2010.03.001.

Cross

Smith

Hoy

Carmona

Wolfe

Vos

, et al. Global burden of rheumatoid arthritis: estimates from the global burden of disease 2010 study. Ann Rheum Dis. 2014;73(7):1316-22. doi:10.1136/annrheumdis-2013-204627.

van der Woude

van der Helm-van Mil

AHM

. Update on the epidemiology, risk factors, and disease outcomes of rheumatoid arthritis. Best Pract Res Clin Rheumatol. 2018;32(2_suppl):174-87. doi:10.1016/j.berh.2018.10.005.

Lee

Weinblatt

ME.

Rheumatoid arthritis. Lancet. 2001;358(9285):903-11. doi:10.1016/s0140-6736(01)06075-5.

Langley

Müller-Schwefe

Nicolaou

Liedgens

Pergolizzi

Varrassi

The impact of pain on labor force participation, absenteeism and presenteeism in the European Union. J Med Econ. 2010;13(4):662-72. doi:10.3111/13696998.2010.529379.

Smolen

Aletaha

McInnes

IB.

Rheumatoid arthritis. Lancet. 2016;388(10055):2023-38. doi:10.1016/s0140-6736(16)30173-8.

Scott

Wolfe

Huizinga

TW.

Rheumatoid arthritis. Lancet. 2010;376(9746):1094-108. doi:10.1016/s0140-6736(10)60826-4.

10.

Haberman

Ehrlich

Levenson

Thermography in rheumatic diseases. Arch Phys Med Rehabil. 1968;49(4):187-92.

11.

Salisbury

Parr

De Silva

Hazleman

Page-Thomas

DP.

Heat distribution over normal and abnormal joints: thermal pattern and quantification. Ann Rheum Dis. 1983;42(5):494-9. doi:10.1136/ard.42.5.494.

12.

Kastberger

Stachl

Infrared imaging technology and biological applications. Behav Res Methods Instrum Comput. 2003;35(3):429-39. doi:10.3758/bf03195520.

13.

Ring

Dieppe

Bacon

PA.

Thermographic assessment of inflammation and anti-inflammatory drugs in osteoarthritis. Br J Clin Pract. 1981;35(7-8):263-4.

14.

Will

Ring

Clarke

Maddison

PJ.

Infrared thermography: what is its place in rheumatology in the 1990s?

Br J Rheumatol. 1992;31(5):337-44. doi:10.1093/rheumatology/31.5.337.

15.

Brenner

Braun

Oster

Gulko

PS.

Thermal signature analysis as a novel method for evaluating inflammatory arthritis activity. Ann Rheum Dis. 2006;65(3):306-11. doi:10.1136/ard.2004.035246.

16.

Frize

Karsh

Herry

Adéa

Aleem

Payeur

Preliminary results of severity of illness measures of rheumatoid arthritis using infrared imaging. Proceedings of the 2009 IEEE International Workshop on Medical Measurements and Applications, MeMeA; 2009 May 29-30; Cetraro, Italy. New York: IEEE. doi:10.1109/MEMEA.2009.5167981.

17.

Moher

Liberati

Tetzlaff

Altman

DG.

Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339:b2535. doi:10.1136/bmj.b2535.

18.

Brito

Miarka

García-Pastor

Pérez

DIV

Marins

JCB

Sillero-Quintana

Osteoarthritis subjects have differentiated lower extremity thermal skin response after the concurrent acute training session. J Therm Anal Calorim. 2021;145:2467-75.

19.

Belcaro

Feragalli

Cornelli

Cotellese

Dugall

, et al. Evaluation of knee periosteal and cartilage morphology in subjects with arthrosis: management with Movardol. Minerva Ortop Traumatol. Epub 2019 Apr 1.

20.

Bhowmik

Bardhan

Das

Bhattacharjee

Nath

Pain related inflammation analysis using infrared images. Int Soc Opt Eng. 2016;1981:986116.

21.

Jin

Yang

Xue

Z-J

Liu

K-M

Liu

Automated analysis method for screening knee osteoarthritis using medical infrared thermography. J Med Biol Eng. 2013;33(5):471-7.

22.

Borojević

Kolarić

Grazio

Grubišić

Antonini

Nola

IA.

Thermography hand temperature distribution in rheumatoid arthritis and osteoarthritis. Period Biol. 2011;113(4):445-8.

23.

Denoble

Hall

Pieper

Kraus

VB.

Patellar skin surface temperature by thermography reflects knee osteoarthritis severity. Clin Med Insights Arthritis Musculoskelet Disord. 2010;3:69-75.

24.

Mejersjö

Wenneberg

Diclofenac sodium and occlusal splint therapy in TMJ osteoarthritis: a randomized controlled trial. J Oral Rehabil. 2008;35(10):729-38.

25.

Varju

Pieper

Renner

Kraus

VB.

Assessment of hand osteoarthritis: correlation between thermographic and radiographic methods. Rheumatology. 2004;43(7):915-9.

26.

Gratt

Sickles

Ross

Wexler

Gornbein

JA.

Thermographic assessment of craniomandibular disorders: diagnostic interpretation versus temperature measurement analysis. J Orofac Pain. 1994;8(3):278-88.

27.

Gratt

Sickles

Wexler

Thermographic characterization of osteoarthrosis of the temporomandibular joint. J Orofac Pain. 1993;7(4):345-53.

28.

Silva

NCOVE

Dos Anjos

Santana

MMC

Battistella

Marcon Alfieri

. Discordance between radiographic findings, pain, and superficial temperature in knee osteoarthritis. Reumatologia. 2020;58(6):375-80. doi:10.5114/reum.2020.102002.

29.

Umapathy

Thulasi

Gupta

Sivanadhan

Thermography and colour Doppler ultrasound: a potential complementary diagnostic tool in evaluation of rheumatoid arthritis in the knee region. Biomed Tech Biomed Eng. 2020;65(3):289-99. doi:10.1515/bmt-2019-0051.

30.

Gizińska

Rutkowski

Szymczak-Bartz

Romanowski

Straburzyńska-Lupa

Thermal imaging for detecting temperature changes within the rheumatoid foot. J Therm Anal Calorim. 2021;145:77-85. doi:10.1007/s10973-020-09665-0.

31.

Laskari

Pentazos

Pitsilka

Raftakis

Konstantonis

Toutouzas

, et al. Joint microwave radiometry for inflammatory arthritis assessment. Rheumatology. 2020;59(4):839-44.

32.

Pauk

Ihnatouski

Wasilewska

Detection of inflammation from finger temperature profile in rheumatoid arthritis. Med Biol Eng Comput. 2019;57(12):2629-39.

33.

Jones

Hassan

Tsuyuki

Dos Santos

Russell

Yacyshyn

Joints: myth or reality? a thermographic joint assessment of inflammatory arthritis patients. Clin Rheumatol. 2018;37(9):2567-71. doi:10.1007/s10067-018-4108-0.

34.

Svaic

Zura

. Cryotherapy effects measured by infrared thermography in elderly people with rheumatoid arthritis. Available from: https://www.qirt2018.de/portals/qirt18/doc/Tu.2.B.3.pdf.

35.

Umapathy

Vasu

Gupta

Computer aided diagnosis based hand thermal image analysis: a potential tool for the evaluation of rheumatoid arthritis. J Med Biol Eng. 2018;38(4):666-77.

36.

Lerkvaleekul

Jaovisidha

Sungkarat

Chitrapazt

Fuangfa

Ruangchaijatuporn

, et al. Comparisons between thermography and ultrasonography with physical examination for wrist joint assessment in juvenile idiopathic arthritis. Physiol Meas. 2017;38(5):691-700. doi:10.1088/1361-6579/aa63d8.

37.

Snekhalatha

Rajalakshmi

Gopikrishnan

Gupta

Computer-based automated analysis of X-ray and thermal imaging of knee region in evaluation of rheumatoid arthritis. Proc Inst Mech Eng H. 2017;231(12):1178-87. doi:10.1177/0954411917737329.

38.

Lasanen

Piippo-Savolainen

Remes-Pakarinen

Kröger

Heikkilä

Julkunen

, et al. Thermal imaging in screening of joint inflammation and rheumatoid arthritis in children. Physiol Meas. 2015;36(2_suppl):273-82. doi:10.1088/0967-3334/36/2/273.

39.

Capo

Ismail

Cardone

Celletti

Auriemma

Sabatini

, et al. Joint functional impairment and thermal alterations in patients with psoriatic arthritis: a thermal imaging study. Microvasc Res. 2015;102:86-91. doi:10.1016/j.mvr.2015.08.008.

40.

Snekhalatha

Anburajan

Sowmiya

Venkatraman

Menaka

Automated hand thermal image segmentation and feature extraction in the evaluation of rheumatoid arthritis. Proc Inst Mech Eng H. 2015;229(4):319-31. doi:10.1177/0954411915580809.

41.

Frize

Ogungbemile

Estimating rheumatoid arthritis activity with infrared image analysis. Stud Health Technol Inform. 2012;180:594-8.

42.

Korman

Straburzyńska-Lupa

Romanowski

Trafarski

Temperature changes in rheumatoid hand treated with nitrogen vapors and cold air. Rheumatol Int. 2012;32(10):2987-92.

43.

Frize

Adéa

Payeur

Gina Di Primio

Karsh

Ogungbemile

Detection of rheumatoid arthritis using infrared imaging. Int Soc Opt Eng. 2011;7962:79620M.

44.

Spalding

Kwoh

Boudreau

Enama

Lunich

Huber

, et al. Three-dimensional and thermal surface imaging produces reliable measures of joint shape and temperature: a potential tool for quantifying arthritis. Arthritis Res Ther. 2008;10(1):R10.

45.

Blyth

Stirling

Coote

Land

Hunter

Injection of the rheumatoid knee: does intra-articular methotrexate or rifampicin add to the benefits of triamcinolone hexacetonide?

Br J Rheumatol. 1998;37(7):770-2.

46.

MacDonald

Land

Sturrock

RD.

Microwave thermography as a noninvasive assessment of disease activity in inflammatory arthritis. Clin Rheumatol. 1994;13(4):589-92. doi:10.1007/BF02242999.

47.

Gatt

Mercieca

Borg

Grech

Camilleri

Gatt

, et al. Thermal characteristics of rheumatoid feet in remission: baseline data. PLoS One. 2020;15(12):e0243078. doi:10.1371/journal.pone.0243078.

48.

Tan

Hong

Allen

Jr Thumboo

Thermography in rheumatoid arthritis: a comparison with ultrasonography and clinical joint assessment. Clin Radiol. 2020;75(12):963.e17-963.e22. doi:10.1016/j.crad.2020.08.017.

49.

Tan

Hong

Allen

Jr Thumboo

A novel use of combined thermal and ultrasound imaging in detecting joint inflammation in rheumatoid arthritis. Eur J Radiol. 2021;134:109421. doi:10.1016/j.ejrad.2020.109421.

50.

Kellgren

Lawrence

. Atlas of standard radiographs. The epidemiology of chronic rheumatism. Vol. 2. Oxford, UK: Blackwell; 1963.

51.

Fraser

Land

Sturrock

RD.

Microwave thermography—an index of inflammatory joint disease. Br J Rheumatol. 1987;26(1):37-9. doi:10.1093/rheumatology/26.1.37.

52.

Lahiri

Bagavathiappan

Jayakumar

Philip

Medical applications of infrared thermography: a review. Infrared Phys Technol. 2012;55(4):221-35. doi:10.1016/j.infrared.2012.03.007.

53.

Ring

Ammer

Infrared thermal imaging in medicine. Physiol Meas. 2012;33(3):R33-46. doi:10.1088/0967-3334/33/3/r33.

54.

Ring

EF.

Historical development of thermometry and thermal imaging in medicine. J Med Eng Technol. 2006;30(4):192-8. doi:10.1080/03091900600711332.

55.

Calin

Mologhianu

Savastru

Calin

Brailescu

CM.

A review of the effectiveness of thermal infrared imaging in the diagnosis and monitoring of knee diseases. Infrared Phys Technol. 2015;69:19-25. doi:10.1016/j.infrared.2015.01.013.

56.

Ring

EF.

Thermographic and scintigraphic examination of the early phase of inflammatory disease. Scand J Rheumatol Suppl. 1987;65:77-80. doi:10.3109/03009748709102180.

57.

Herry

Frize

Quantitative assessment of pain-related thermal dysfunction through clinical digital infrared thermal imaging. Biomed Eng Online. 2004;3(1):19. doi:10.1186/1475-925x-3-19.

58.

Reinberg

Circadian changes in the temperature of human beings. Bibl Radiol. 1975;6:128-39.

59.

Collins

Ring

Cosh

Bacon

. Quantitation of thermography in arthritis using multi-isothermal analysis. I. Thermographic index. Ann Rheum Dis. 1974;33(2_suppl):113-5. doi:10.1136/ard.33.2.113.

60.

Ring

Collins

Bacon

Cosh

. Quantitation of thermography in arthritis using multi-isothermal analysis. II. Effect of nonsteroidal anti-inflammatory therapy on the thermographic index. Ann Rheum Dis. 1974;33(4):353-6. doi:10.1136/ard.33.4.353.

61.

Ring

McEvoy

Jung

Zuber

Machin

Standards for devices used for the measurement of human body temperature. J Med Eng Technol. 2010;34(4):249-53. doi:10.3109/03091901003663836.

Infrared Thermography for the Evaluation of Inflammatory and Degenerative Joint Diseases: A Systematic Review

Abstract

Objective

Design

Results

Conclusions

Keywords

Introduction

Materials and Methods

Results

Correlational Studies to Investigate OA-Related Temperature Changes

IRT-Based Studies to Investigate OA Treatment Outcome

Correlational Studies to Investigate Rheumatic Diseases Related to Temperature Changes

IRT-Based Studies to Investigate Rheumatic Diseases Treatment Outcome

Discussion

Conclusions

Footnotes

Declaration of Conflicting Interests

Acknowledgments and Funding

ORCID iD

References