Update on the Use of Infrared Thermography in the Early Detection of Diabetic Foot Complications: A Bibliographic Review

Foot lesions are among the most frequent causes of morbidity and disability in the diabetic population. Thus, the exploration of preventive control measures is vital for detecting early signs and symptoms of this disease. Infrared thermography is one of the complementary diagnostic tools available that has proven to be effective in the control of diabetic foot. The last review on this topic was published in 2015 and so, we conducted a bibliographic review of the main databases (PubMed, the Web of Science, Cochrane library, and Scopus) during the third quarter of 2023. We aimed to identify the effectiveness of infrared thermography as a diagnostic element in pre-ulcerous states in diabetic patients and to detect diabetic foot ulcer complications. We obtained a total of 1199 articles, 26 of which were finally included in the present review and published after 2013. After analyzing the use of infrared thermography in diabetic patients both with and without ulcers, as well as in healthy individuals, we concluded that is an effective tool for detecting early-stage ulcers in diabetic foot patients.


Introduction
Foot lesions are among the most frequent causes of morbidity and disability in the population with diabetes and are the most common reason for hospital admission and decreased patient quality of life.Indeed, in this population, there is a 40-70% probability of requiring a lower limb amputation [1].Exploration and preventive control of this pathology are vital to detect early signs and symptoms that, in the long term, can promote the appearance of ulcers.This exploration must be performed at least once in the absence of risk factors and once every six months if there is any risk of ulcers [2].Therefore, it is especially important to follow a protocol for these patients, in which the anamnesis and clinical history play a substantial role.
Different complementary telemedical methods are available to aid the diagnosis of diabetic foot, of which infrared thermography is one of the most important [3].This technique was first used for military applications at the beginning of the 20th century.However, infrared thermography soon transferred to biomedical fields and started being used for the non-invasive diagnosis of vascular disease, fever, breast cancer, and in the analysis of inflammatory arthritis, osteoarthritis, and other pathologies [4].
Infrared thermography is a safe, repeatable, contactless, and non-invasive procedure that measures and maps the temperature distribution radiating from body surfaces [5].An infrared camera identifies and monitors the amount of radiation emitted and translates this value into a temperature.These projections allow identification of the heat radiating away from the body [3,6] and produce images with specific physiological thermal patterns that can be collected according to specific standards, thereby allowing the quality of this technique to increase in the future [6].
Feet temperature variation in neuropathic patients is a predictive element of the ulcer appearance, so infrared thermography, due to its characteristics and easy use, is a good tool to detect this temperature difference [7].
The aim of this systematic review was to define the effectiveness of infrared thermography as a diagnosis tool for pre-ulcerous states in patients with type-2 diabetic mellitus and to detect ulcer complications in patients with diabetic foot.
Based on the results obtained, we will try to provide relevant information for health professionals who use this technique, speeding up and helping in decision-making in patients who may develop an ulcer or its reappearance.However, there is some controversy in generalizing these statements, so more studies are needed to generalize the findings.

Materials and Methods
Following the preferred reporting items for systematic review and meta-analysis descripts (PRISMA) guidelines, we conducted a systematic review of the academic literature on infrared thermography as a tool for diagnosing diabetic foot.We followed the population, intervention, control, and outcomes (PICO) format (Table 1) to formulate the basis of this research.We consulted the Descriptors in Health Science (DeCS) and Medical Subject Headings (MeSH) terms to devise the following PubMed search strategy: (((("Diabetic Foot"[Title/ Abstract]) OR (diabetic foot[MeSH Terms])) OR (("Diabetic Neuropat hies"[Title/Abstract]) OR (diabetic neuropathies[MeSH Terms])))) AND ((("thermal imaging"[Title/Abstract]) OR (differential thermal analysis[MeSH Terms])) OR (analyses, differential thermal[MeSH Terms])).The results were subsequently summarized in databases, as shown in Table 2.
We searched the main health science databases including PubMed, the Web of Science (WoS), Scopus, and the Cochrane library during the third quarter of 2023.The inclusion criteria were articles about infrared thermography conducted in humans with and without diabetes and ulcers, published from 2013 to 2023 in English or Spanish.Some publications such as editorials, editor's letters, reviews, systematic reviews, meta-analyses, books or books chapters and conference reports were excluded.Of note, no Cochrane reviews were included because none met the inclusion criteria.Once the screened publications were obtained, we read the publications and reviewed their quality by employing the PEDro scale [8].

Results
Our search strategy obtained a total of 1199 publications (30 in PubMed, 61 in the WoS, 224 in the Cochrane library, and 884 in Scopus).After applying the inclusion criteria, 26 valid citations were reviewed, as reflected in the PRISMA flowchart (Figure 1).A brief description of the main features of the 26 articles found is provided in Table 3 (Table 3).
All the articles included were assessed according to the PEDro scale which assigned a score of 0 if the criterion is absent and 1 if it is present in the article [9].The first criterion on this scale, reporting eligibility criteria, was not recorded because it considered the external validity of the articles.The conduct and design of study are evaluated by eight items (item 2-9).Item 10 involves reporting between-group statistical comparisons, and item 11 involves measures of variability [10].On this scale, studies with scores higher than 9 points are considered to have excellent methodological quality, those with scores between 6 and 8 points are deemed good, those from 4 to 5 points are considered to have regular quality and those below 4 are regarded as having poor methodological quality.Healthy feet are thermally symmetrical.In some participants, there were differences of >2.2 • C between the same site on both feet.After 10 min, these differences had significantly reduced.
These thermal imaging devices were shown to be fit for purpose and could identify areas of concern in the foot.This device could also be beneficial in other clinical settings such as in the study and prevention of pressure ulcers.

4.
Reliability of a novel thermal imaging system for temperature assessment of healthy feet  These studies provide a basic understanding of thermal symmetry in the feet of healthy participants that can be used when interpreting images of the feet of patients with DM and DPN.
Validate a smartphone-based high-end infrared camera for the assessment of diabetic foot.
Near-perfect agreement for the temperature measurements, both throughout the plantar foot and in pre-specified regions.
The validity of the smartphonebased infrared camera was excellent for assessing diabetic foot.

7.
Infrared thermography and ulcer prevention in the high-risk diabetic foot: data from a single-blind multicentre controlled clinical trial       All the articles included were assessed according to the PEDro scale which assigned a score of 0 if the criterion is absent and 1 if it is present in the article [9].The first criterion on this scale, reporting eligibility criteria, was not recorded because it considered the external validity of the articles.The conduct and design of study are evaluated by eight items (item 2-9).Item 10 involves reporting between-group statistical comparisons, and item 11 involves measures of variability [10].On this scale, studies with scores higher than 9 points are considered to have excellent methodological quality, those with scores between 6 and 8 points are deemed good, those from 4 to 5 points are considered to have regular quality and those below 4 are regarded as having poor methodological quality.In this review, only one paper was considered to have excellent methodological quality, and three studies were rated as having a good quality.The majority fell within the range of 5-4 points.Only four references scored below 4 points, indicating poor methodological quality (Table 4).

Discussion
To assess if infrared thermography was a useful tool for diagnosing pre-ulcerous states and detecting the complications of ulcers in diabetic patients, we performed an exhaustive review of the relevant available literature.We found elements that made this comparison difficult, such as the differences in the samples and methodology used in each study, including the infrared camera employed and the protocol followed to capture the images.In spite of these challenges, we have emphasized the lack of evidence for the use of thermography in preventing complications, the absence of consensus in the use of angiosomes and temperature distribution patterns, as well as the need to establish thermographic standards that facilitate the comparison of obtained data.
Studies in diabetic patients have highlighted the fact that thermography can be used as a method of temperature control (which is approximately 2 • C higher in infected wounds) useful to help patients in avoiding pressure zones, thereby favoring the prevention of lesions and their complications [16,34].However, other authors such as Petrova et al. [15] found no difference in ulcer appearance in diabetic patients allocated in a randomized control trial where one group was blinded to the results of the thermography and the other was not (both receiving also standard care and follow-up).Therefore, there is insufficient evidence to support the use of thermography to prevent complications because the values it detects do not always significantly differ from normality and studies with larger sample sizes are still required.Databases such as the one published by Hernández-Contreras et al. [28] which contain both healthy and diabetic patient thermograms could be created.This database contains 167 patients and so could serve as a useful baseline for the comparison of results with those of future studies.Although different types of voluntary subjects were included in the different studies considered in this review, these results could be addressed together because they all suggest that thermography is a suitable tool to detect foot temperature changes.If they are detected sufficiently early, this technology may help to prevent the appearance of pre-ulcerous complications and could favor ulcer healing and avoiding infections through early treatment [15,18,25,34].
Even though one of the exclusion criteria for this current work was not being exposed to other pathologies that could result in temperature changes, it was very difficult to isolate diabetic foot from other pathologies such as peripheral vascular disease because many of these coexist [25,28,29,31].Indeed, some authors observed that temperatures in the fifth metatarsal and hallux were lower in patients with associated pathologies [5,21].
Furthermore, Mori et al. [23] suggest that temperature distribution patterns must be identified by collecting and classifying these images according to maps of heat distribution so that they can be compared without relying on the angiosome divisions proposed by other authors [5,23].Other authors suggest that patients with diabetic foot present a significantly higher temperature in the fifth metatarsal area and hallux compared to healthy individuals [20,22,27].These variations represent different pattern distributions of temperature.For example, diabetic patients have notably higher temperature asymmetry and hot spots on the sole of the foot that indicate a heat increase [11,26].Regardless, the lack of consensus in the use of angiosomes and temperature distribution patterns make it difficult to generalize the results published up to date.Moreover, it is important to highlight the differences in thermographic images from studies comparing the affected and contralateral limbs in diseased or healthy patients.According to Van Netten et al. [16], there was no difference between the limbs of the same patient, while Macdonald et al. [20] or Mori et al. [23] suggested that intra-patient variability is comparable with that of other patients, with a difference of up to 2 • C between both feet.Nonetheless, infrared thermography is the most common method used to compare contralateral limbs in these patients [13,15,16,19,22].The work by Gatt et al. [20] indicated that there were differences between patients with or without lesions.This increased temperature may be altered in pre-ulcerous states, although once the wound is present it is difficult to predict the development of complications using thermography alone, because no difference between ulcered and healthy toes of the same foot can be detected.However, Gethin [34] is able to show a progressive core temperature reduction along with the healing of the wound.
As previously mentioned, not only the study population is variable in the studies reported, but also the characteristics of the thermal imaging device and methods of image acquisition.A wide range of different infrared cameras are used for these types of study.On average, it can be assumed that a standard spatial resolution of 320 × 240 pixels [15,20,22,26] conferees a thermal resolution of up to 0.1 • C [16,19,20,25] with a temperature range of 0-100 • C [30].Although the use of standard infrared cameras is quite common, some studies have proposed using infrared smartphone cameras [14,30,31,33] to make this technique even more accessible.Indeed, some studies have even proposed merging 3D and thermography images to obtain more realistic results [16], as well as developing mobile apps able to detect temperature changes.[31,33].However, phone cameras have a lower (160 × 120 pixels) resolution [14,17] and these devices cannot obtain specific data like absolute temperature.Despite this limitation, Kanazawa et al. [30] suggest that images are obtained much faster and are sufficient for data comparison.In fact, Van Doremalen et al. [14] stated that cameras connected to smartphones showed excellent validity for studying diabetic foot and therefore, such studies with smartphone cameras should be increased.Of note, although working at room temperature, some studies use a black background to dampen the influence of light [3,14,22,25,26] because environmental variations can alter the results, as shown by Bhargavi et al. [25].
As it has been observed during the development of this current study, there are some limitations to comparing the use of infrared thermography in patients with diabetic foot.First, very few studies have individually tackled this technique, comparing it with other techniques or in other pathologies associated with diabetic foot.Second, a wide range of cameras can be used to record sample images, leading to the misconception that accuracy is unreliable, but actually, images are not necessarily comparable, depending on many factors, especially their spatial resolution.Furthermore, the decision to use a black background in the images can significantly alter the results and no algorithms have yet been developed that can unify all these criteria.
In addition, it is to be highlighted that working with healthy or diabetic individuals with or without an ulcer or underlying pathologies can result in very disparate sample images.Thus, it has been proposed by other authors, the generation of a large thermographic image database could help to create thermographic standards and to make the comparison of results more feasible.Homogenous criteria that can help to unify results must be developed so that this technique can be used to help prevent complications or promote ulcer healing in diabetic patients.

Conclusions
Infrared thermography represents a potentially effective tool for detecting pre-ulcerous states in diabetic foot patients.However, further research is still required to investigate its applications for preventing diabetic foot ulcer complications.It is very important to highlight that these thermographic studies must consider the sample type (healthy or diabetic patients, with or without an ulcer), protocol used to obtain the images (e.g., with or without a black background), and results analysis (software used).It is essential to continue research into infrared thermography, especially with the aim of clarifying whether the use of angiosomes or patterns of plantar temperature distribution is better; the influence of peripheral vascular disease on variations in plantar temperature in the diabetic population; and the reliability of cameras connected to smartphones.Infrared thermography is a cheap, non-invasive, and painless technique that can provide useful data for the development of new methods to further prevent and palliate diabetic foot complications.

Table 2 .
Bibliographical database search strategy.

Table 3 .
Description of articles included in the systematic review.

Table 3 .
Description of articles included in the systematic review.

Table 4 .
Articles' methodology quality scores according to the PEDro scale."✓" Meet requeriment and "✗" do not meet requeriment.