Using Noncontact Infrared Thermography for Long-term Monitoring of Foot Temperatures in a Patient with Diabetes Mellitus
Foot complications in persons with diabetes mellitus (DM) are associated with substantial costs and loss of quality of life. Increasing evidence suggests changes in skin temperature, measured using an infrared thermographic system (IRT), may be a predictor of foot ulcer development in patients with DM. The purpose of this case study is to describe the long-term IRT findings and overall clinical outcomes of a patient with DM and peripheral vascular disease.
Foot temperature measurements using IRT were obtained slightly more than 1 year before and immediately following endovascular treatment of a 76-year-old man, a nonsmoker with type 2 DM, hypertension, and ischemic heart disease with cardiac arrhythmia. Although he was otherwise asymptomatic, the infrared measurement showed an average temperature difference of 2.3˚ C between the left and right foot until he developed a small, trauma-induced wound on the left foot, at which time left foot temperature increased. He was diagnosed with rectosigmoid adenocarcinoma, underwent surgery and chemotherapy, and subsequently was evaluated for peripheral vascular disease. Before undergoing peripheral angiography and percutaneous transluminal angioplasty, IRT evaluation showed a hot spot on the left heel. Immediately following endovascular treatment, the mean temperature difference between the right and left foot was low (0.2˚ C), but a Stage I pressure ulcer was visible on the left heel. Skin breakdown in that area was observed 2 months later, and the wound continued to increase in size and depth. The patient died shortly thereafter due to complications of cancer. In this case study, a series of infrared images of foot skin temperatures appeared to show a relationship with blood circulation and wound/ulcer development and presentation. IRT has the ability to instantaneously measure the absolute temperature of the skin surface over a large area without direct skin contact. However, the devices are very sensitive and prospective clinical studies to determine the validity, reliability, sensitivity, and specificity of these measurements for routine use in patients who are at risk for vascular disease and/or foot ulcers are needed.
Early diagnosis of disease complications associated with diabetes mellitus (DM) is the first prerequisite for saving the lower limb. According to an analysis by Al-Maskari and El-Sadig,1 which was part of a general cross-sectional survey conducted to assess the prevalence of DM, great attention must be paid to risk factors such as a diabetic neuropathy and diabetic angiopathy. Predictors of ulceration include the presence of peripheral neuropathy, peripheral vascular disease, and a history of ulceration.2 In a cross-sectional study, Pound et al3 showed ulcers often recur after a median duration of 126 days in 40% of patients with a history of ulceration. Other risk factors for diabetic foot ulcers are foot infection, foot deformity, high plantar pressures during walking, male gender, and HbA1c >9%.4-6 These factors are considered to be the leading causes of diabetic foot syndrome.
Accurate diagnosis is the foundation of ulcer care. Patients with DM should be tested for neuropathy; in addition, proper vascular assessment is critical to the evaluation of the diabetic foot.7 A simple test to diagnose patients at risk for ulcer formation due to peripheral sensory neuropathy is the nylon monofilament test; an inability to detect the monofilament when applied under the metatarsal heads or digits is indicative of neuropathy.8 During vascular examination, the dorsalis pedis and posterior tibial pulses should be palpated, and a general inspection of the extremities should be performed. Noninvasive vascular tests include the ankle-brachial index, which is determined by dividing the higher systolic pressure of the anterior tibial or posterior tibial vessels by the highest systolic brachial pressure.9-11
Skin temperature is one of the most reliable indicators of body and foot blood perfusion. The systematic analysis of the literature by Houghton et al12 suggests the use of skin temperature monitoring is an effective way to predict, and possibly prevent, diabetic foot ulceration. In their systematic review, Bharara et al13 compared various thermal measurement techniques in the assessment of the diabetic neuropathic foot and showed thermal measurement is a useful technique in the clinical management of the diabetic foot. In a descriptive review, Ring14 focused on the medical use of an infrared thermographic system (IRT) and its general relevance to DM as a useful tool in the assessment of tissue viability and peripheral circulation. Ring concluded IRT is especially suitable for serial measurements used in the follow-up of response to treatment. In a preliminary study, Brånemark et al15 used IRT to study 16 persons with DM with or without vascular complications, together with the action of a vasodilator. The authors showed characteristic abnormalities exhibited by the patients in the thermal patterns over the hands and feet that deviated from those of healthy subjects.
Recently, IRT has been widely used in DM-related diagnostics. In an observational study of 60 patients, Sivanandam et al16 applied IRT to measure skin temperature from the various body regions (ie, the contralateral regions of the inner canthus of the eye; tympanic region of the ear; and the forehead, neck, and upper and lower extremities) and noted the device can be used as a mass screening tool for the accurate estimation of HbA1c by which a sensitivity of 90% and negative predictive value of 85% could be achieved. Clinical studies regarding the role of IRT in the diagnostics of diabetic foot include Liu et al’s case study,17 which indicated dermal thermography can be a screening modality to detect presigns of ulceration in a timely manner. The pilot study by Van Netten et al18 examined 15 patients with DM and diffuse complications using IRT and demonstrated differences in mean temperature of >3˚ C between the ipsilateral and contralateral foot.
The clinical studies of Lavery et al19,20 have shown thermometry is a useful monitoring tool for preventing diabetic foot ulcers and amputations. In a physician-blinded, 18-month randomized controlled trial study, Armstrong et al21 monitored 225 persons with DM and found in patients who developed an ulcer, foot skin temperature was 4.8 times higher at the site of ulceration in the week before ulceration than the temperature of patients who did not develop an ulcer. In their physician-blinded, randomized, 15-month, multicenter trial, Lavery et al20 quantified data from 173 patients with a history of diabetic foot ulceration. An infrared skin thermometer was used by the enhanced therapy group of patients to measure temperatures on 6 foot sites each day. Temperature differences (>2.2˚ C) observed between left and right corresponding sites triggered patients to reduce activity until temperatures normalized. The enhanced therapy group had fewer foot ulcers than the standard therapy group without temperature monitoring.
According to the studies mentioned, thermal symmetry is normal in healthy study groups; temperature gradients between feet may predict the formation of ischemic changes.
IRT, unlike many other imaging techniques used in medicine, is not an internal imaging system for anatomical information; infrared imaging provides information on skin temperature distribution. The great advantage of IRT is that it is both noncontact and noninvasive and a real-time temperature measurement. Any object at a temperature above absolute zero (ie, T >0 K) emits infrared radiation. By remote temperature sensing, the camera is merely receiving the natural thermal energy emitted by the body and transforming it into an electronic signal.22 In their critical review, Lahiri et al23 focused on the basics of medical IRT, the procedures adopted for various measurements, and successful applications of IRT diagnosis in various medical fields. However, IRT can provide only an image of skin temperature distribution; it does not provide data at a specific depth inside the body.
The purpose of this case study is to describe the long-term IRT findings and overall clinical outcomes of a patient with DM and peripheral vascular disease. The patient was chosen due to his willingness to cooperate with the study duration.
Mr. D, a 76-year-old nonsmoker with DM type 2, hypertension, and ischemic heart disease with cardiac arrhythmia, was monitored several times at home over a period of 1 year (from March 2012 until February 2013) using IRT before he was examined in the outpatient vascular surgery department. Intervals of monitoring were based on the patient’s availability. He received no treatment on his lower limbs before the February 2013 examination. Mr. D had no visible defects on the foot; his only complaint was that his feet felt cold. During home visits, the soles and the forefoot were scanned by IRT. Thermograms were recorded with an FLIR B200 infrared camera (Flir Systems, Danderyd, Sweden). The thermal images obtained were processed using QuickReport 1.2 software (Flir Systems, Danderyd, Sweden). All images were standardized to the same temperature range (20˚ C – 35˚ C). Temperature measurement points were selected along a line connecting the first toe and the heel or from the square area as is shown in Figure 1. The mean temperatures along the line and from the area of interest were calculated by the software. The same value of emissivity (ie, the measure of an object’s ability to emit infrared energy, ε = 0.98) was used for all thermograms. Standard conditions in IRT imaging have been documented by Vollmer and Möllman24 and Ring and Ammer25; according to these conditions, the thermal images were captured at a distance of 1 m from the body region in a restricted, temperature-controlled environment. The thermal equilibration of the patient was 15 minutes.
IRT home monitoring. The infrared images (see Figure 2) show a temperature map of the feet. The first and second IRT assessments were obtained in March and May 2012 (see Figure 2a,b). The highest mean temperature difference between the left and right foot was 2.3˚ C (see Table 1), but no difference was noted during the next assessment in October (see Figure 2c). At that time, a small wound was noted on the nail of the first left toe after the patient injured himself in September 2012. Figures 2a–f show a colder upper part of the left foot. Lower limb ischemic, vascular, or wound complications were not present during this period of time. The highest temperature difference between the right and left foot toes was 4.6˚ C (see Figure 2e and Table 2). In February 2013, the temperature of the left foot increased (see Figure 2f); specifically, the mean temperature in the square area on the heel was 25.3˚ C for the right foot and 29.2˚ C for the left foot.
Clinical examination, treatment, and follow-up. Mr. D was first examined in the outpatient department in February 2013 for an ischemic defect on the first left toe with a diameter of ~1-cm necrotic base and phlegmon around the defect. According to Mr. D, the defect had appeared 4 months earlier (October 2012) when he injured himself and gradually worsened. In December 2012, Mr. D underwent a rectosigmoid resection for adenocarcinoma (T3N1bM1, diagnosed in December 2012) with metastatic liver disease. Overall, he was in good condition, without claudication; he received chemotherapy treatment (5-fluorouracil and leucovorin; FU/FA de Gramont) (see Table 3).
Left leg pulses were palpable in the groin on the superficial femoral artery (SFA) and on the popliteal artery (PA). Peripheral arteries were not palpable. An audible pulse was detected in the posterior tibial artery (PTA) by ultrasonic Doppler probe. The right leg dorsalis pedal artery (DPA) was palpable. CT angiographic examination warranted the need for peripheral angiography of the left limb and a percutaneous transluminal angioplasty was performed in April 2013. Specifically, CT angiography showed evidence of patent SFA with PA and significant atherosclerotic disease of the tibial arteries (eg, stenotic anterior tibial artery with closure of the middle part) to the farther PTA with distal closure. The middle of the peroneal artery was stenotic with distal closure (see Figure 3). The plantaris communis artery (PCA) and DAP were not noted in CT angiographic images — that is, the distal parts of the lower leg and foot were perfused only by minor collateral vessels, mostly dilated muscular branches forming a collateral pathway around both ankles (see Figure 4). A percutaneous transluminal angioplasty of the anterior tibial artery (ATA) and peroneal artery was performed (see Figure 5). The control angiography showed good results after endovascular treatment at the site of dilatation, with slightly better collateral supplied peripherals — the dilated branches from revascularized parts of tibial arteries supplying peripheral parts of tibial and foot vascular system showed a hint of efflux in the common plantar artery (see Figure 6). A palpable pulse was clinically detected on the SFA/PA at the time of hospital discharge. Audible flows in the PTA and the peroneal artery were detected by ultrasound Doppler probe; lower limb mobility and sensitivity were not compromised.
One (1) month after the endovascular surgery, an extensive pseudo-aneurysm in the tibial area overlying the left ATA was detected by ultrasound duplex. This observation was confirmed by control CT angiographic examination (see Figure 7). An asymptomatic pseudo-aneurysm in this area is not a medical emergency requiring immediate surgery and due to the serious overall condition of the patient (cancer with metastases), conservative therapy was continued.
Infrared images were taken before (see Figure 8a) and 1 day after revascularization (see Figure 8b). The mean temperatures of the right and left foot were 32.3˚ C and 32.1˚ C, respectively, before and 33.6˚ C and 33.2˚ C 1 day after the procedure (see Figure 8b). Thirteen (13) days following angioplasty, an area of warmth on the left foot heel was apparent (see Figure 8c). The highest temperature was 33.6˚ C on the left heel and 32.3˚ C on the right heel. The left heel hot point area affected the mean temperature, which was up to 0.6˚ C higher in the treated limb (see Table 4). At the time of discharge following endovascular treatment, the wound on the left foot toe was dry with a diameter of ~1 cm with no signs of active infection, and the wound base showed granulation tissue without any signs of wound widening. A discoloration of the skin was visible on the left foot heel, and intermittent pain occurred at rest. Local treatment of the wound on the left toe continued twice a week in the outpatient department. The condition of the wound gradually improved, its size decreased, and by May 2013 it was reduced to its original size. The wound was dry with no signs of suppuration or inflammation (aggressive infection, phlegmon). Although the toe wound was healing well, by the end of May/beginning of June 2013 a nonblanchable erythema pressure ulcer (Stage I) had developed on the left heel. Clinically palpable pulsation in the limbs remained unchanged after the initial treatment.
Mr. D’s overall condition gradually deteriorated while he was being monitored due to the cancer. The condition of his limbs also worsened in July. The defect on the toe was small with no signs of active infection, granulation tissue was noted in the wound base, and there were no signs of increasing wound size, but the heel pressure ulcer became necrotic and was 6 cm in diameter. The ulcer on the heel was treated using moist wound therapy twice a week. During the treatment, necrotic tissue was removed. By September 2013, the lesion progressed to Stage II; it was 2 cm deep with no signs of infection or inflammation around the ulcer.
This is the first case study describing clinical outcomes and IRT scanning results over an extended period of time and provides observations that suggest a relationship among vascular supply, skin temperature changes, and the development of wounds. Before developing any symptoms, a mean temperature difference of 1.8˚ C between the left and right foot was detected at the first (March 2012) and second (May 2012) IRT assessments (see Figure 2a,b). According to the pilot study of van Netten et al18 and the randomized multicenter study of Lavery et al,20 a difference in temperature contralaterally of the feet of patients with diabetes often was observed. No temperature difference was observed for Mr. D in October 2012 (see Figure 2c). At that time, Mr. D had a small wound on the nail of the first left toe after he injured himself. A mean temperature difference between feet showed a gradual increase of 2.1˚C (see Figure 2e). During the last IRT measurement, the hot point area of heel on the left foot was observed with a mean temperature difference 4.7˚ C between the left and right heels (see Figure 2f). This increase in temperature could have been the first indicator of heel pressure; a heel pressure ulcer was diagnosed 2 months later (May 2013). Evidence from Gatt’s26 single-center, randomized, prospective study among 63 healthy adults suggests the normal temperature difference between plantar feet is no greater than 0.84˚ C.
IRT may be a useful tool for monitoring skin temperature changes influenced by blood circulation. This point was observed before and after Mr. D’s endovascular treatment. Foot skin temperature was affected by revascularization. Despite the 15-minute acclimatization period of thermal equilibration of the foot, an increased temperature in both limbs was detected. This increase could have been affected by the fact the image was taken early in the morning, immediately after Mr. D awakened when more time for acclimatization might be necessary. The warmer bearing on the left heel was where the pressure ulcer formed.
Limitations of Thermography
IRT is a very sensitive device for measuring variations in heat patterns; however, thermograms can be influenced by many ambient factors, as proposed in the review by Fernández-Cuevas et al.27 Thus, thermography images should be obtained under controlled environmental conditions, per the observational study of Zaproudina et al.28 The recommended option is to report data from scanned images as a difference between affected and healthy contralateral anatomical structures to define the consistency of abnormality.
Another important consideration of IRT measurement is the preparation of patients. Fifteen (15) minutes of acclimatization are needed for thermal equilibration of the patient, and the skin surface has to be dry and free of any artifacts (ie, topical ointments, solutions, bandages or dressings). Ignoring these factors has a negative impact on the evaluation of resulting infrared images, because these artifacts can affect the characteristics of the skin (ie, emissivity and reflexivity).29,30 Based on authors experience and Gatt et al’s study,26 a nonreflective plate can be placed behind the area of interest, which leads to better evaluation of the infrared images due to the patient´s temperature filtration in the background.
In this case study, infrared images of foot skin temperatures appeared to show a relationship between blood circulation and wound/ulcer presentation. IRT has the ability to instantaneously measure the absolute temperature of the skin surface over a large area without direct skin contact. In this and other studies, IRT has been found to reveal physiological changes before they are clinically apparent. The infrared images can be used to monitor temperature differences between the lower limbs of patients over a long time period and have the potential to be used as an indicator of vascular disease or predictor of foot ulcer formation. However, IRT devices are very sensitive, and prospective clinical studies to determine the validity, reliability, sensitivity, and specificity of these measurements for routine use in specific populations are needed.
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Potential Conflicts of Interest: This research was supported by a specific grant from Masaryk University, Brno, Czech Republic (MUNI/A/1449/2014 and MUNI/A/0894/2015).
Mr. Erik Staffa is a researcher and specialist, and Dr. Bernard is assistant professor and researcher, Department of Biophysics, Faculty of Medicine, Masaryk University; Dr. Kubíček is an assistant and vascular surgeon, and Dr. Vlachovský is an assistant professor and vascular surgeon, 2nd Department of Surgery, St. Anne’s University Hospital, Faculty of Medicine; Dr. Vlk is assistant professor and researcher, and Dr. Mornstein is a professor and head of the department, Department of Biophysics, Faculty of Medicine; and Dr. Robert Staffa is a professor and head of the department, 2nd Department of Surgery, St. Anne’s University Hospital, Faculty of Medicine, Masaryk University, Brno, Czech Republic. Please address correspondence to: Erik Staffa, Department of Biophysics, Faculty of Medicine, Masaryk University, Kamenice 5, Brno, 62500 Czech Republic; email: firstname.lastname@example.org.