Thermography in the follow up of the diabetic foot: best to weigh the enemy more mighty than he seems

Abstract

Thermography is being increasingly appreciated as a further modality contributing to the early detection of incipient tissue damage predisposing to diabetic foot ulceration in selected high-risk patients. Among currently available modalities, liquid crystal thermography and infrared thermography have been most widely used. The former is effective, but its main limitation is low sensitivity. The latter permits non-contact measurements at different angles of the foot, independent of the quality of the camera used. It has been suggested that 5-year use of such techniques for daily self-examination among high-risk patients may contribute to the significant reduction of diabetic foot complications. Clearly, further experience with thermography in the real-life setting is now very welcome.

Keywords:

• amputations
• diabetes mellitus
• diabetic foot
• temperature
• thermography

Neuropathy, ischemia and infection represent the three mortal enemies of the diabetic foot [1,2]. It is against these enemies that the battle has to be fought, and our armamentarium continuously needs improvement [1,3,4]. Given the increasing number of patients with foot lesions and the increasing complexity of their comorbidities, timely diagnosis and prompt initiation of multi-expert treatment are vital [1,5]. Conversely, delayed referral may be disastrous [3]. Another important issue needing improvement is that most patients are ignorant of their neurovascular and structural foot pathology and need education and careful monitoring to avoid further deterioration [6]. Some of the newer screening tools of peripheral neuropathy lend themselves for this purpose, thanks to their documented additional educational value [7,8].

Overall, patients with diabetes have a 25% lifetime risk of developing foot ulceration [1,3]. To quantify this risk, clinicians can evaluate arterial blood flow, peripheral neuropathy and pressure distribution on the plantar aspect of the foot [3,9]. By contrast, temperature measurement of the foot has hitherto received considerably less attention [9,10]. It has not been widely used in clinical practice, although increased foot temperature is now considered a manifestation of diabetic neuropathy and a warning sign of incipient tissue strain with increased risk of developing foot ulceration in the near future [9,10]. The former is generally attributed to the progressive injury of sympathetic nerve fibers in the small blood vessels, leading to increased blood flow to the lower extremities, which ultimately results in warmer feet [11]. The latter is attributed to the effect of excess plantar pressures, which go unrecognized due to sensory loss [9]. Consequently, a more comprehensive examination incorporating temperature measurement into routine clinical examination may be anticipated to improve identification of feet at risk [9]. Thermography is the means of measuring heat coming from the human body. There is now a variety of thermal measurement techniques available for the examination of the diabetic foot, such as electrical contact thermography, cutaneous thermal discrimination thresholds, infrared thermography (IT) [9], infrared thermometry [10] and liquid crystal thermography (LCT) [9]. Most available techniques are based on thermal imaging, a non-invasive, effective and comprehensible technique, which can be used either in the clinic or for home self-monitoring [9].

Among these modalities, the handheld IT has already proved an effective adjunctive device for home monitoring, whereas it has additionally been linked with prevention of ulcer recurrence in high-risk patients [12,13]. Using this thermometer, we have previously shown that both dorsal and plantar temperatures in patients with type 2 diabetes mellitus were significantly higher among patients with peripheral neuropathy, as diagnosed by the diabetic neuropathy index, than those without neuropathy [14]. Moreover, these temperatures showed a significant positive correlation with clinical severity of neuropathy (as reflected in the diabetic neuropathy index score) [14]. Of note, a threshold of 32°C was found to yield the best specificity and sensitivity for the diagnosis of neuropathy, and the method exhibited very good reproducibility [14]. Employing the same device, we have also demonstrated that plantar temperatures of both feet are significantly higher in Type 2 diabetes mellitus patients with sudomotor dysfunction, as diagnosed by the indicator test Neuropad [11]. There was a significant positive correlation between these temperatures and severity of sudomotor dysfunction, as assessed by the time of Neuropad complete color change [11]. Importantly, sudomotor dysfunction may lead to dry vulnerable skin and is a further risk factor for diabetic foot ulceration [1,11].

Of greater importance, the Armstrong and Lavery group has repeatedly shown that temperature monitoring can avoid new neuropathic ulceration [12,13,15]. Indeed, these authors have found that the risk of ulceration in high-risk patients using an infrared thermometer on a daily basis was only one-third of the risk of those not using this method [15]. In practice, patients were instructed to reduce mobilization and activity, with immediate study nurse contact in case of increased foot temperature, and this approach was decisive in prompt self-referral and improved outcomes [15]. The value of thermography for home monitoring and its significant contribution to the prevention of ulcer occurrence and recurrence in selected high-risk patients have also been confirmed by two other studies [12,13]. The authors suggested that prevention was achieved independently of the increased frequency of visual foot inspection [12,13]. Indeed, home temperature monitoring with prompt healthcare professional contact where appropriate was linked to >60% reduction in the incidence of foot ulcers [12,13].

More recently, a comprehensive literature review of studies on thermal methods as applied to the diabetic foot has been published [10]. LCT and IT were the techniques hitherto mostly used in examined studies [10]. LCT emerged as an effective and affordable technique, but its limitations included low sensitivity, low image resolution and pressure sensitivity, as well as the disadvantage of a very demanding device handling during contact of the crystals with examined body area [10]. Conversely, IT permits non-contact acquisition of thermal patterns, thus reducing the risk of wound contamination while additionally enabling measurements at different angles of the foot, even in the presence of foot deformities [10]. Moreover, the authors have provided evidence that detection of temperature differences might be independent of the quality of the IT camera used and that it can be achieved without image processing algorithms [10]. However, LCT offers the possibility of both static and dynamic measurements on the plantar aspect of the foot [9,10]. The authors concluded that IT camera is the most usable and cost-effective thermography option for the prevention of diabetic foot complications [10]. They also proposed that the use of such devices over the next 5 years in a patient-centered fashion may not only aid in the early detection and avoidance of foot complications, but also contribute to patient education, encouraging a healthier lifestyle [10].

The practical implication of the evidence summarized in this excellent new review is that inclusion of thermography in a prudent scheme of patient-centered examination and follow-up has the potential to prove very useful in the early detection and prevention of diabetic foot lesions [10]. Among available modalities, LCT and IT hold the most promise, and especially the latter has emerged as the most cost-effective [10]. Arguably, the authors’ 5-year view of adopting thermography in patients’ daily routine [10] may appear slightly over-enthusiastic, especially regarding its anticipated beneficial effects on education and healthier lifestyle choices. Indeed, we would like to know whether home self-monitoring of foot skin temperature can be used on a long-term basis and how durable its contribution to the reduction of foot lesions may be. We would also like to see more data on patient education and the impact on their lifestyle. Nonetheless, it cannot be denied that foot thermography merits further use in clinical practice [9,11–14].

Conclusions

Clearly, the fundamental principle ‘time is tissue’ holds especially true for the diabetic foot [16]. In an endeavor to meet this need, some expert teams are now beginning to use the multidisciplinary foot day clinic, offering urgent patient evaluation and treatment [5]. At the same time, devices for widespread home use to prevent serious pathology are highly welcome, and temperature measurement is obviously particularly promising [12,13,15]. Toward this goal, Bharara et al., in a very thorough study of thermal techniques, have previously suggested that the ideal device for temperature measurement should be user friendly, widely available, reproducible and accurate [9]. Today, these requirements have, to a great extent, been fulfilled [9–15]. Impressively, temperature measurement has already been documented to reduce the incidence of foot ulcers in selected high-risk patients [12,13,15]. At the moment, we are eagerly anticipating the confirmation of the value of thermography in the real-life setting.

However, a more practical approach that might help healthcare professionals provide concrete recommendations to their patients could be a standardization of the procedure. This might include videotape training for all participants prior to thermometer use along with a proposed standard methodology of measurements. Such approach could include twice-daily measurements in sitting position, that is, morning immediately after leaving the bed and late in the evening before bed rest. Measured sites should be the first, third and fifth metatarsal head, the hallux, the central midfoot and the heel on the plantar aspect of the foot, as well as the central midfoot on the dorsal aspect of the foot, while alternative sites could be chosen in patients with amputations. Patients should be given a temperature monitoring diary with pictorial representations of the measured sites for each foot. According to the previous findings of the temperature monitoring trials [12–15], a temperature difference >2.2°C (4°F) between left and right corresponding feet sites should alert patients to immediately reduce activity and contact their physician. Of note, we need to be prudent in choosing the appropriate patients who will benefit from this intervention. Indeed, it is mostly high-risk patients who need this approach: patients in category 2 or 3 of the International Working Group on the Diabetic Foot risk classification system, that is, those with history of neuropathy and structural deformity or limited joint mobility, or those with history of neuropathy or foot amputation [17].

Certainly, this proposed approach may seem overzealous. Nonetheless, at the end of the day, when our enemy is the diabetic foot, it is probably “best to weigh the enemy more mighty than he seems” [18], so that strategic measures for prevention, early diagnosis and prompt management are diligently taken.

Financial & competing interests disclosure

N Papanas has been an advisory board member of TrigoCare International; has participated in sponsored studies by Novo Nordisk and Novartis; has received honoraria as a speaker for Astra-Zeneca, Eli-Lilly, Novo Nordisk and Pfizer; and attended conferences sponsored by TrigoCare International, Novo Nordisk, Sanofi-Aventis and Pfizer. N Papanas has no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript apart from those disclosed.

No writing assistance was utilized in the production of this manuscript.