Reliability of a novel thermal imaging system for temperature assessment of healthy feet

Reliability of a novel thermal imaging system for temperature assessment of healthy feet Background: Thermal imaging is a useful modality for identifying preulcerative lesions (“hot spots”) in diabetic foot patients. Despite its recognised potential, at present, there is no readily available instrument for routine podiatric assessment of patients at risk. To address this need, a novel thermal imaging system was recently developed. This paper reports the reliability of this device for temperature assessment of healthy feet. Methods: Plantar skin foot temperatures were measured with the novel thermal imaging device (Diabetic Foot Ulcer Prevention System (DFUPS), constructed by Photometrix Imaging Ltd) and also with a hand-held infrared spot thermometer (Thermofocus® 01500A3, Tecnimed, Italy) after 20 min of barefoot resting with legs supported and extended in 105 subjects (52 males and 53 females; age range 18 to 69 years) as part of a multicentre clinical trial. The temperature differences between the right and left foot at five regions of interest (ROIs), including 1st and 4th toes, 1st, 3rd and 5th metatarsal heads were calculated. The intra-instrument agreement (three repeated measures) and the inter-instrument agreement (hand-held thermometer and thermal imaging device) were quantified using intra-class correlation coefficients (ICCs) and the 95% confidence intervals (CI). Results: Both devices showed almost perfect agreement in replication by instrument. The intra-instrument ICCs for the thermal imaging device at all five ROIs ranged from 0.95 to 0.97 and the intra-instrument ICCs for the hand-held- thermometer ranged from 0.94 to 0.97. There was substantial to perfect inter-instrument agreement between the hand-held thermometer and the thermal imaging device and the ICCs at all five ROIs ranged between 0.94 and 0.97. Conclusions: This study reports the performance of a novel thermal imaging device in the assessment of foot temperatures in healthy volunteers in comparison with a hand-held infrared thermometer. The newly developed thermal imaging device showed very good agreement in repeated temperature assessments at defined ROIs as well as substantial to perfect agreement in temperature assessment with the hand-held infrared thermometer. In addition to the reported non-inferior performance in temperature assessment, the thermal imaging device holds the potential to provide an instantaneous thermal image of all sites of the feet (plantar, dorsal, lateral and medial views). Trial registration: Diabetic Foot Ulcer Prevention System NCT02317835, registered December 10, 2014 Keywords: Thermal imaging, Diabetic foot ulcer, Temperature, Reliability, Prevention * Correspondence: nina.petrova@nhs.net NL Petrova and A Whittam are joint first authors G Machin and ME Edmonds are joint senior authors Diabetic Foot Clinic, King’s College Hospital NHS Foundation Trust, Denmark Hill, London SE5 9RS, UK Division of Diabetes and Nutritional Sciences, King’s College London, London, UK Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Petrova et al. Journal of Foot and Ankle Research (2018) 11:22 Page 2 of 6 Background of pre-ulcerous inflammation [9, 10]. These could be Diabetic foot ulcer is a major complication of diabetes [1]. missed during routine foot examination of the neuropathic In people with diabetic neuropathy, tissue damage can diabetic foot, when signs and symptoms of inflammation progress to ulcer, infection and necrosis and ultimately are often lacking. results in amputation [2]. Indeed, in diabetes, almost 85% To address this need, a novel medical thermal imaging of all non-traumatic amputations are preceded by a foot device was recently developed [15]. Laboratory testing ulcer. The financial cost of foot ulcers and amputations is showed that the overall temperature uncertainty of the immense [3, 4]. Diabetic foot ulcer imposes substantial thermal imaging device was ±0.2 °C (k = 2, 95% confidence burden on public and private payers, ranging from $9–13 limit) for the range 15 °C to 45 °C which is comparable to billion in addition to the costs associated with diabetes the uncertainty of the CE marked hand-held spot itself [3]. A recent health economics analysis has reported thermometers, (CE is abbreviated from Conformité that the total expenditure on healthcare related to foot Européenne, meaning European Conformity), [15]. The ulcer and amputation in people with diabetes for 2014– usefulness of this system in temperature assessment of the 2015 in England was estimated at £1billion [4]. At least £1 feet of healthy volunteers at 33 ROIs (12 plantar, 15 in every £140 of the National Health Service (NHS) ex- dorsal, 3 medial and 3 lateral) has been documented [16]. penditure in England is spent on footcare for people with To assess the performance of the novel thermal imaging diabetes [4]. This is equivalent to around 0.7–0.8% of the device in the assessment of foot temperatures in healthy entire NHS budget. Recent data show that at least volunteers in comparison with a hand-held infrared 60,671–75,838 people with diabetes in England have foot thermometer we selected five easily identifiable plantar ulcers at any given time (2–2.5% of the diagnosed diabetes foot landmarks (1st and 4th toes, 1st, 3rd and 5th metatar- population), and that the mean weekly cost of caring for sal heads). The objectives of this study were twofold: firstly each patient is £208 [4]. Thus timely identification of pa- to measure the agreement in replication (three repeated tients at risk is fundamental to reduce adverse outcomes measures) for the thermal imaging device and for the and reduce costs [5, 6]. It has been estimated that redu- hand-held thermometer (inter-instrument agreement) and cing the prevalence of people with diabetic foot ulcers by secondly, to measure the agreement between the thermal one third could save the NHS £210 m–£262 m a year [4]. imaging device and the hand-held-thermometer (intra-in- Over the last fifteen years there has been an increased strument agreement) in the assessment of temperatures of interest in thermal imaging as a possible modality for the feet of healthy volunteers. early detection of incipient tissue damage in diabetic foot patients [7–9]. Clinical trials have indicated that Methods regular measurement of foot skin temperatures with Participants non-contact infrared thermometers in high-risk patients The study was carried out at three clinical centres as can reduce the incidence of foot ulcers [10]. However, in previously described [16]. Male and female volunteers these studies, foot temperatures were assessed only at were recruited if they had intact feet and no previous his- predefined regions of interest (ROIs) using single spot tory of diabetes, foot ulcer or foot surgery either for cor- infrared thermometers [10, 11] and the low specificity of rection of a foot deformity or following foot trauma. this method is now well recognised [12]. Thus, despite Subjects were excluded if they reported unsteadiness in the evidence that neuropathic foot ulcer is preceded by a gait, if they experienced burning pain, aching of the feet or rise in skin temperature [11] the latter is not routinely legs, prickling sensation or numbness of the feet or legs or measured in clinical practice. if they had any discomfort in the calf muscles when walk- There is a requirement for a reliable portable device as ing that was relieved with rest or any health problems af- certified to medical device regulations to document thermal fecting their feet and legs. The study was approved by images of high risk diabetic foot patients during routine London-City Road and Hampstead Research Ethics Com- podiatry assessment. The ideal thermal imager should be mittee (REC reference 15/LO/0070) and was carried out user friendly, widely available, reproducible and accurate in accordance with the Declaration of Helsinki as revised [13]. In addition, thermal imaging should not only be in 2000. The study was registered on ClinicalTrials.gov limited to the plantar site of the feet as more than half of website (Clinicaltrials.gov identifier NCT02317835). All the diabetic foot ulcers (52%) are with non-plantar location subjects provided written informed consent and screening [14]. Detailed assessment with such a device can provide and assessment were performed at one study visit. information of up to several thousand ROIs as opposed to up to 12 ROIs most commonly assessed by podiatrists Temperature measurement and data acquisition using non-contact infrared thermometers. A thermal im- Temperature measurements were carried with a novel ther- aging device would help identify areas of raised temperature mal imaging device (Diabetic Foot Ulcer Preventions Sys- (or ‘hotspots’) which others have reported to be indicative tem, DFUPS), developed specifically for this investigation Petrova et al. Journal of Foot and Ankle Research (2018) 11:22 Page 3 of 6 by Photometrix Imaging Ltd. in association with the University of South Wales [15, 16]and with ahand-held infrared thermometer (Thermofocus® 01500A3, Tecnimed, Italy). The thermal imaging device is a battery operated instrument with on-board software. The captured foot thermal image is downloaded on to a computer for further analysis [15]. Circles with an area equal to 1 cm are manually placed on ROIs of each foot. The Thermofocus is a non-contact spot thermometer, which measures the emitted thermal radiation of a selected ROI of the foot and converts that measurement into a temperature. The field of view of the scanned area is nominally 1 cm . Four thermal imaging systems (one for each clinical centre and one as a back-up) and four hand-held infra- red thermometers (one for each clinical centre and one as a back-up) were used in the study. All devices were Fig. 1 A typical example of a combined plantar thermal image of the characterised at the National Physical Laboratory (NPL) right and left foot captured with the thermal imaging device in a before usage by the clinical centres, as described previ- healthy volunteer. The white circles show the manually selected ROIs ously [15]. In brief, the thermal imaging systems and the hand-held infrared thermometers were evaluated to assess the temperature resolution, the spatial resolution and performance (repeatability, stability and accuracy). linear regression and random effects analysis of variance. All devices were calibrated under laboratory conditions The agreement between the repeated measures at five ROIs in terms of radiance temperature versus the NPL black- for each instrument (intra-instrument agreement) and body calibration sources [17] over the range of 15 °C to between the two instruments at the same ROI (inter-instru- 45 °C, traceable to the international temperature scale of ment agreement) was quantified using intra-class correl- 1990 (ITS-90) with uncertainties of ±0.2 °C (k = 2, 95% ation coefficient (ICC) and the 95% confidence intervals confidence limit) quantified in accordance with the (CI) following a multilevel modelling approach (random ef- internationally agreed Guide to Uncertainty in Measure- fects regressions). If a substantial agreement between repli- ment (http://www.bipm.org/utils/common/documents/ cations was established, the replications within each ROI jcgm/JCGM_100_2008_E.pdf). were averaged. Bland and Altman analysis and plots were Participants were assessed after 20 min of barefoot rest used to complement the assessment of any bias between on a podiatry chair with their legs extended and sup- the two instruments [18]. The benchmark limits for agree- ported. Three consecutive measurement sequences were ment followed established classifications [18, 19]. In all carried out. In each sequence, thermal imaging alter- cases, for more rigour, in addition to the point estimate, the nated with hand-held thermometry. Initially a combined lower limit of the 95% CI was taken into account. plantar image of the right foot and left foot was captured with the thermal imaging device. This was followed by Results spot thermometry at five predefined ROIs (1st and 4th A total of 105 subjects (52 males and 53 females; age toes, and 1st, 3rd and 5th metatarsal heads). The tem- range 18 to 69 years (mean age 44 ± 11 years (mean ± peratures of each ROI were measured with the SD)), weight range 49 to 136 kg (mean weight 77.5 ± hand-held thermometer initially on the right foot and 16.2 kg), height range 1.50 to 1.98 m (mean height 1.70 ± then on the left foot. The same ROIs of the right foot 0.10 m), body mass index (BMI) range 18.2 to 51.8 kg/m and left foot were manually selected on each thermal (mean BMI 26.7 ± 5.4 kg/m2) were recruited in the study image and the temperatures were recorded (Fig. 1). at the three clinical centres. Temperature measurements were carried out by trained operators (one operator per Statistical methods: centre) and were taken in controlled room conditions. Temperature differences between feet (Right Foot-Left The mean study room temperature and humidity were 23 Foot) were calculated for each ROI for the thermal imaging ± 0.5 °C (mean ± SD) and 50 ± 8%RH, (mean ± SD) re- device and for the hand-held thermometer, respectively. spectively. In two subjects, the thermal imaging data was Each measure was replicated three times. The differences unavailable (the images were not saved after acquisition between repeated measurements as well as the differences and could not be recovered). Repeated measurement data between instruments (infrared thermal imaging device and for both instruments were available for 103 subjects. The hand-held thermometer) were modelled with multilevel mean duration of the temperature assessment (three Petrova et al. Journal of Foot and Ankle Research (2018) 11:22 Page 4 of 6 repeated sequences of alternating thermal imaging and Table 2 Measure of agreement between hand-held thermometer and thermal imaging device at five ROIs hand-held thermometry) was 3 min ±40 s (mean ± SD). No correction was made for skin emissivity as only ROIs Mean temperature P-value ICC (95% C.I.) difference (°C) between temperature differences were determined in this study and instruments (95% C.I.) it was assumed that skin emissivity was the same at 1st toe 0.04 (− 0.01, 0.10) 0.18 0.95 (0.93; 0.97) equivalent points on the foot. 4th toe 0.03 (− 0.05, 0.12) 0.42 0.94 (0.92; 0.96) 1st metatarsal head −0.01 (− 0.05, 0.04) 0.81 0.97 (0.95; 0.98) Intra-instrument agreement (agreement in replication) 3rd metatarsal head 0.11 (0.05, 0.17) < 0.001 0.96 (0.94; 0.97) The random effects linear regression analysis indicated that 5th metatarsal head 0.21 (0.16, 0.27) < 0.001 0.94 (0.91; 0.96) there were no significant differences in the temperature as- sessment between the three replications at all ROIs (1st toe Hand-held thermometer minus thermal imaging device p = 0.26; 4th toe p = 0.97; 1st metatarsal head p = 0.93; 3rd healthy volunteers in comparison with a hand-held infra- metatarsal head p = 0.69 and 5th metatarsal head p = 0.98). red spot thermometer. The intra-instrument agreement for the thermal imaging Both instruments showed agreement in repeated device and for the hand-held thermometer was similar at temperature assessment and also agreement between all five ROIs, as indicated by a non-significant instruments. Logistic regression analysis indicated that replication-by-instrument interaction in any of the five there were no differences in the repeated temperature measured ROIs: 1st toe p = 0.23; 4th toe p =0.97, 1st assessment at five ROIs between the two instruments. metatarsal head p = 0.23, 3rd metatarsal head p =0.84 and The inter-instrument ICCs at all ROIs were equal to or 5th metatarsal head p = 0.37. above 0.95 for the novel thermal imaging device and The intra-instrument ICCs for the thermal imaging equal to or above 0.94 for the hand-held infrared spot device ranged from 0.95 to 0.97 at the selected ROIs and thermometer, indicating almost perfect agreement in the intra-instrument ICCs for the hand-held-thermometer replication by instrument. Moreover, there was substan- ranged from 0.94 to 0.97, (Table 1). tial to perfect agreement in temperature assessment between the two instruments and the intra-instrument Inter-instrument agreement between hand-held ICCs were equal to or above 0.94 at all five ROIs. Bland thermometer and thermal imaging device and Altman plots showed that only a few points were Random effects linear regression, averaging the three outside the limits of agreement. Based on the bench- replications at the selected ROIs indicated that the mean mark limits for agreement, these analyses demonstrated difference between instruments (hand-held thermometer consistency of measure. minus thermal imaging device) ranged between − 0.01 °C In addition to the reported non-inferior performance in and 0.21 °C and the inter-instrument ICCs ranged be- temperature assessment at predefined ROIs, the novel tween 0.94 and 0.97, respectively (Table 2). thermal imaging device holds the potential to overcome At all five ROIs, Bland and Altman analysis indicated the significant limitations of spot thermometry and that the mean differences between the two instruments provide an instantaneous thermal image of all sites of the were very close to zero (Table 3) and the Bland and feet (plantar, dorsal, lateral and medial views), [16]. Indeed, Altman plots present the limits of agreement for all five the advantages of a full imaging acquisition sequence ROIs (Fig. 2). including plantar, dorsal, medial and lateral views captured Discussion Table 3 Limits of agreement between hand-held thermometer This study reports the performance of a novel thermal and thermal imaging device at five ROIs imaging device in the assessment of foot temperatures in ROIs Mean temperature Lower Limit Upper Limit difference (SD) °C (95% C.I.) °C (95% C.I.)°C 1st toe 0.04 (0.30) − 0.54 0.62 Table 1 Intra-instrument agreement in repeated measures at (− 0.64 to − 0.44) (0.52 to 0.72) five ROIs by instrument 4th toe 0.03 (0.42) −0.78 0.85 ROIs Hand-held thermometer Thermal imaging device (− 0.93 to − 0.64) (0.71 to 0.99) 1st toe 0.94 (0.92, 0.96) 0.95 (0.93, 0.96) 1st metatarsal head −0.01 (0.25) − 0.50 0.49 (− 0.58 to − 0.41) (0.40 to 0.57) 4th toe 0.95 (0.93, 0.96) 0.95 (0.94, 0.97) 3rd metatarsal head 0.11 (0.29) −0.47 0.69 1st metatarsal head 0.97 (0.96, 0.98) 0.97 (0.96, 0.98) (− 0.57 to − 0.37) (0.59 to 0.79) 3rd metatarsal head 0.96 (0.94, 0.97) 0.96 (0.94, 0.97) 5th metatarsal head 0.21 (0.29) − 0.35 0.78 5th metatarsal head 0.97 (0.95, 0.98) 0.97 (0.96, 0.98) (− 0.45 to − 0.26) (0.69 to 0.88) Data are presented as ICC (95% C.I.) for each ROI by instrument Thermal imaging device - Hand-held thermometer Petrova et al. Journal of Foot and Ankle Research (2018) 11:22 Page 5 of 6 with DFUPS in the temperature assessment of the feet of healthy volunteers have been reported [16]. In addition, thermal imaging with DFUPS does not require any cali- bration for age, gender, weight, height or BMI and there- fore it can be readily implemented in everyday clinical assessment. The importance of foot skin temperature monitoring in the identification of the early signs of inflammation has been emphasised in the 2015 guidelines of the International Working Group on the Diabetic Foot [20]. We have recently completed a multicentre clinical trial (NCT02579070) in high-risk diabetic foot patients to assess the usefulness of thermal imaging with DFUPS in addition to standard podiatric treatment to reduce diabetic foot ulcer recurrence. In addition to diabetic foot ulcer prevention, a further study is planned to investigate the usefulness of DFUPS in the assessment of the acute Charcot foot. Conclusions The newly developed thermal imaging device showed very good agreement in repeated temperature assessments at defined ROIs as well as substantial to perfect agreement in temperature assessment with a hand-held infrared therm- ometer. This device fulfils the requirements of a reprodu- cible and accurate thermal imaging device. It addresses the clinical need of a “portable, reliable and accurate” thermal imaging instrument [8, 13]. We believe that the developed thermal imaging device holds the potential of becoming a real asset in the diabetic foot clinic, to identify potential patients at risk of diabetic foot ulcer. Abbreviations BMI: Body mass index; CE: is abbreviated from Conformité Européenne, meaning European Conformity; CI: Confidence intervals; DFUPS: Diabetic Foot Ulcer Preventions System; ICC: Intra-class correlation coefficient; NHS: National Health Service; NPL: National Physical Laboratory; REC: Research Ethics Committee; ROI: Region of interest; ROIs: Regions of interest Acknowledgements The authors would like to thank the participants of this study and the project advisory board for their support and contribution to the study. Funding The research was funded by the National Institute for Health Research (NIHR) Invention for Innovation (i4i) programme (An Innovative system for the early identification, monitoring, evaluation and diagnosis of diabetic foot ulcers II-LA- 0813-20007). The views expressed are those of the authors and not necessarily those of the NHS, the NIHR or the Department of Health. Availability of data and materials The datasets used and/or analysed during the current study are available from NLP on reasonable request. Authors’ contributions All authors contributed to the design of the study. NLP, AM and SA recruited Fig. 2 Bland and Altman plots of agreement between the thermal participants and collected data. NLP, AW and AND processed and analysed imaging device and the hand-held thermometer for the 1st toe (a), 4th toe data. NLP, AW and MEE drafted the manuscript with input from all authors. (b), 1st metatarsal head (c), 3rd metatarsal head (d) and 5th metatarsal head All authors have read and approved the final manuscript. NLP and AW are joint first authors. GM and MEE are joint senior authors. Petrova et al. Journal of Foot and Ankle Research (2018) 11:22 Page 6 of 6 Ethics approval and consent to participate 14. Prompers L, Huijberts M, Apelqvist J, Jude E, Piaggesi A, Bakker K, Edmonds Approval for this study was obtained from the London-City Road and Hampstead M, et al. High prevalence of ischaemia, infection and serious comorbidity in Research Ethics Committee (REC reference 15/LO/0070). Each person in the study patients with diabetic foot disease in Europe. Baseline results from the was given a participant’s information sheet and all study participants provided Eurodiale study. Diabetologia. 2007;50(1):18–25. written informed consent. 15. Machin G, Whittam A, Ainarkar S, Allen J, Bevans J, Edmonds M, Kluwe B, Macdonald A, Petrova N, Plassmann P, Ring F, Rogers L, Simpson R. A medical thermal imaging device for the prevention of diabetic foot Consent for publication ulceration. Physiol Meas. 2017;38(3):420–30. https://doi.org/10.1088/1361- Consent for publication containing no personal identifying information was 6579/aa56b1. sought and gained from all participants. 16. Macdonald A, Petrova N, Ainarkar S, Allen J, Plassmann P, Whittam A, Bevans J, Ring F, Kluwe B, Simpson R, Rogers L, Machin G, Edmonds M. Competing interests Thermal symmetry of healthy feet: a precursor to a thermal study of The authors declare that they have no competing interests. diabetic feet prior to skin breakdown. Physiol Meas. 2017;38(1):33–44. https://doi.org/10.1088/1361-6579/38/1/33 . 17. Machin G, Chu B. High-quality blackbody sources for infrared thermometry Publisher’sNote and thermography between-40 and 1000 degrees C. Imaging Sci J. 2000; Springer Nature remains neutral with regard to jurisdictional claims in 48(1):15–22. published maps and institutional affiliations. 18. Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet. 1986;1:307–10. Author details 1 19. Landis JR, Koch GC. The measurement of observer agreement for Diabetic Foot Clinic, King’s College Hospital NHS Foundation Trust, Denmark 2 categorical data. Biometrics. 1977;33:159–74. Hill, London SE5 9RS, UK. Division of Diabetes and Nutritional Sciences, 3 20. IWGDF Guidance on the prevention of foot ulcers in at-risk patients with King’s College London, London, UK. Temperature and Humidity, National 4 diabetes. http://www.iwgdf.org/files/2015/website_prevention.pdf. Physical Laboratory, London, UK. Microvascular Diagnostics, Northern Medical Physics and Clinical Engineering, Newcastle upon Tyne Hospitals, Newcastle upon Tyne, UK. Community Podiatry Department, Pennine Acute Hospitals NHS Trust, Manchester, UK. Photometrix Imaging Ltd, Pontypridd, UK. Department of Computing, University of South Wales, Pontypridd, UK. Received: 23 March 2018 Accepted: 16 May 2018 References 1. Boulton AJM, Vileikyte L, Ragnarson-Tennvall G, Apelqvist J. The global burden of diabetic foot disease. Lancet. 2005;366(9498):1719–24. 2. Edmonds ME. The diabetic foot, 2003. Diabetes Metab Res Rev. 2004; 20(Suppl 1):S9–S12. 3. Rice JB, Desai U, Cummings AK, Birnbaum HG, Skornicki M, Parsons NB. Burden of diabetic foot ulcers for medicare and private insurers. Diabetes Care. 2014;37(3):651–8. 4. Diabetes UK. Improving footcare for people with diabetes and saving money: an economic study in England. https://diabetes-resources-production.s3-eu-west-1. amazonaws.com/diabetes-storage/migration/pdf/Improving%2520footcare%2520 economic%2520study%2520%28January%25202017%29.pdf Accessed 30 Apr 2018. 5. Chammas NK, Hill RL, Edmonds ME. Increased mortality in diabetic foot ulcer patients: the significance of ulcer type. J Diabetes Res. 2016;2016: 6. Vamos EP, Bottle A, Edmonds ME, Valabhji J, Majeed A, Millett C. Changes in the incidence of lower extremity amputations in individuals with and without diabetes in England between 2004 and 2008. Diabetes Care. 2010; 33(12):2592–7. 7. Ring F. Thermal imaging today and its relevance to diabetes. J Diabetes Sci Technol. 2010;4(4):857–62. 8. Pafili K, Papanas N. Thermography in the follow up of the diabetic foot: best to weigh the enemy more mighty than he seems. Expert Rev Med Devices. 2015;12(2):131–3. 9. Frykberg RG, Gordon IL, Reyzelman AM, Cazzell SM, Fitzgerald RH, Rothenberg GM, Bloom JD, Petersen BJ, Linders DR, Nouvong A, Feasibility NB. Efficacy of a smart mat Technology to predict development of diabetic plantar ulcers. Diabetes Care. 2017;40(7):973–80. 10. Armstrong DG, Holtz-Neiderer K, Wendel C, Mohler MJ, Kimbriel HR, Lavery LA. Skin temperature monitoring reduces the risk for diabetic foot ulceration in high-risk patients. Am J Med. 2007;120(12):1042–6. 11. Houghton VJ, Bower VM, Chant DC. Is an increase in skin temperature predictive of neuropathic foot ulceration in people with diabetes? A systematic review and meta-analysis. J Foot Ankle Res. 2013;6:31. 12. van Netten JJ, Prijs M, van Baal JG, Liu C, van der Heijden F, Bus SA. Diagnostic values for skin temperature assessment to detect diabetes- related foot complications. Diabetes Technol Ther. 2014;16(11):714–21. 13. Bharara M, Cobb JE, Claremont DJ. Thermography and thermometry in the assessment of diabetic neuropathic foot: a case for furthering the role of thermal techniques. Int J Low Extrem Wounds. 2006;5:250–60. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Foot and Ankle Research Springer Journals

Reliability of a novel thermal imaging system for temperature assessment of healthy feet

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Abstract

Background: Thermal imaging is a useful modality for identifying preulcerative lesions (“hot spots”) in diabetic foot patients. Despite its recognised potential, at present, there is no readily available instrument for routine podiatric assessment of patients at risk. To address this need, a novel thermal imaging system was recently developed. This paper reports the reliability of this device for temperature assessment of healthy feet. Methods: Plantar skin foot temperatures were measured with the novel thermal imaging device (Diabetic Foot Ulcer Prevention System (DFUPS), constructed by Photometrix Imaging Ltd) and also with a hand-held infrared spot thermometer (Thermofocus® 01500A3, Tecnimed, Italy) after 20 min of barefoot resting with legs supported and extended in 105 subjects (52 males and 53 females; age range 18 to 69 years) as part of a multicentre clinical trial. The temperature differences between the right and left foot at five regions of interest (ROIs), including 1st and 4th toes, 1st, 3rd and 5th metatarsal heads were calculated. The intra-instrument agreement (three repeated measures) and the inter-instrument agreement (hand-held thermometer and thermal imaging device) were quantified using intra-class correlation coefficients (ICCs) and the 95% confidence intervals (CI). Results: Both devices showed almost perfect agreement in replication by instrument. The intra-instrument ICCs for the thermal imaging device at all five ROIs ranged from 0.95 to 0.97 and the intra-instrument ICCs for the hand-held- thermometer ranged from 0.94 to 0.97. There was substantial to perfect inter-instrument agreement between the hand-held thermometer and the thermal imaging device and the ICCs at all five ROIs ranged between 0.94 and 0.97. Conclusions: This study reports the performance of a novel thermal imaging device in the assessment of foot temperatures in healthy volunteers in comparison with a hand-held infrared thermometer. The newly developed thermal imaging device showed very good agreement in repeated temperature assessments at defined ROIs as well as substantial to perfect agreement in temperature assessment with the hand-held infrared thermometer. In addition to the reported non-inferior performance in temperature assessment, the thermal imaging device holds the potential to provide an instantaneous thermal image of all sites of the feet (plantar, dorsal, lateral and medial views). Trial registration: Diabetic Foot Ulcer Prevention System NCT02317835, registered December 10, 2014 Keywords: Thermal imaging, Diabetic foot ulcer, Temperature, Reliability, Prevention * Correspondence: nina.petrova@nhs.net NL Petrova and A Whittam are joint first authors G Machin and ME Edmonds are joint senior authors Diabetic Foot Clinic, King’s College Hospital NHS Foundation Trust, Denmark Hill, London SE5 9RS, UK Division of Diabetes and Nutritional Sciences, King’s College London, London, UK Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Petrova et al. Journal of Foot and Ankle Research (2018) 11:22 Page 2 of 6 Background of pre-ulcerous inflammation [9, 10]. These could be Diabetic foot ulcer is a major complication of diabetes [1]. missed during routine foot examination of the neuropathic In people with diabetic neuropathy, tissue damage can diabetic foot, when signs and symptoms of inflammation progress to ulcer, infection and necrosis and ultimately are often lacking. results in amputation [2]. Indeed, in diabetes, almost 85% To address this need, a novel medical thermal imaging of all non-traumatic amputations are preceded by a foot device was recently developed [15]. Laboratory testing ulcer. The financial cost of foot ulcers and amputations is showed that the overall temperature uncertainty of the immense [3, 4]. Diabetic foot ulcer imposes substantial thermal imaging device was ±0.2 °C (k = 2, 95% confidence burden on public and private payers, ranging from $9–13 limit) for the range 15 °C to 45 °C which is comparable to billion in addition to the costs associated with diabetes the uncertainty of the CE marked hand-held spot itself [3]. A recent health economics analysis has reported thermometers, (CE is abbreviated from Conformité that the total expenditure on healthcare related to foot Européenne, meaning European Conformity), [15]. The ulcer and amputation in people with diabetes for 2014– usefulness of this system in temperature assessment of the 2015 in England was estimated at £1billion [4]. At least £1 feet of healthy volunteers at 33 ROIs (12 plantar, 15 in every £140 of the National Health Service (NHS) ex- dorsal, 3 medial and 3 lateral) has been documented [16]. penditure in England is spent on footcare for people with To assess the performance of the novel thermal imaging diabetes [4]. This is equivalent to around 0.7–0.8% of the device in the assessment of foot temperatures in healthy entire NHS budget. Recent data show that at least volunteers in comparison with a hand-held infrared 60,671–75,838 people with diabetes in England have foot thermometer we selected five easily identifiable plantar ulcers at any given time (2–2.5% of the diagnosed diabetes foot landmarks (1st and 4th toes, 1st, 3rd and 5th metatar- population), and that the mean weekly cost of caring for sal heads). The objectives of this study were twofold: firstly each patient is £208 [4]. Thus timely identification of pa- to measure the agreement in replication (three repeated tients at risk is fundamental to reduce adverse outcomes measures) for the thermal imaging device and for the and reduce costs [5, 6]. It has been estimated that redu- hand-held thermometer (inter-instrument agreement) and cing the prevalence of people with diabetic foot ulcers by secondly, to measure the agreement between the thermal one third could save the NHS £210 m–£262 m a year [4]. imaging device and the hand-held-thermometer (intra-in- Over the last fifteen years there has been an increased strument agreement) in the assessment of temperatures of interest in thermal imaging as a possible modality for the feet of healthy volunteers. early detection of incipient tissue damage in diabetic foot patients [7–9]. Clinical trials have indicated that Methods regular measurement of foot skin temperatures with Participants non-contact infrared thermometers in high-risk patients The study was carried out at three clinical centres as can reduce the incidence of foot ulcers [10]. However, in previously described [16]. Male and female volunteers these studies, foot temperatures were assessed only at were recruited if they had intact feet and no previous his- predefined regions of interest (ROIs) using single spot tory of diabetes, foot ulcer or foot surgery either for cor- infrared thermometers [10, 11] and the low specificity of rection of a foot deformity or following foot trauma. this method is now well recognised [12]. Thus, despite Subjects were excluded if they reported unsteadiness in the evidence that neuropathic foot ulcer is preceded by a gait, if they experienced burning pain, aching of the feet or rise in skin temperature [11] the latter is not routinely legs, prickling sensation or numbness of the feet or legs or measured in clinical practice. if they had any discomfort in the calf muscles when walk- There is a requirement for a reliable portable device as ing that was relieved with rest or any health problems af- certified to medical device regulations to document thermal fecting their feet and legs. The study was approved by images of high risk diabetic foot patients during routine London-City Road and Hampstead Research Ethics Com- podiatry assessment. The ideal thermal imager should be mittee (REC reference 15/LO/0070) and was carried out user friendly, widely available, reproducible and accurate in accordance with the Declaration of Helsinki as revised [13]. In addition, thermal imaging should not only be in 2000. The study was registered on ClinicalTrials.gov limited to the plantar site of the feet as more than half of website (Clinicaltrials.gov identifier NCT02317835). All the diabetic foot ulcers (52%) are with non-plantar location subjects provided written informed consent and screening [14]. Detailed assessment with such a device can provide and assessment were performed at one study visit. information of up to several thousand ROIs as opposed to up to 12 ROIs most commonly assessed by podiatrists Temperature measurement and data acquisition using non-contact infrared thermometers. A thermal im- Temperature measurements were carried with a novel ther- aging device would help identify areas of raised temperature mal imaging device (Diabetic Foot Ulcer Preventions Sys- (or ‘hotspots’) which others have reported to be indicative tem, DFUPS), developed specifically for this investigation Petrova et al. Journal of Foot and Ankle Research (2018) 11:22 Page 3 of 6 by Photometrix Imaging Ltd. in association with the University of South Wales [15, 16]and with ahand-held infrared thermometer (Thermofocus® 01500A3, Tecnimed, Italy). The thermal imaging device is a battery operated instrument with on-board software. The captured foot thermal image is downloaded on to a computer for further analysis [15]. Circles with an area equal to 1 cm are manually placed on ROIs of each foot. The Thermofocus is a non-contact spot thermometer, which measures the emitted thermal radiation of a selected ROI of the foot and converts that measurement into a temperature. The field of view of the scanned area is nominally 1 cm . Four thermal imaging systems (one for each clinical centre and one as a back-up) and four hand-held infra- red thermometers (one for each clinical centre and one as a back-up) were used in the study. All devices were Fig. 1 A typical example of a combined plantar thermal image of the characterised at the National Physical Laboratory (NPL) right and left foot captured with the thermal imaging device in a before usage by the clinical centres, as described previ- healthy volunteer. The white circles show the manually selected ROIs ously [15]. In brief, the thermal imaging systems and the hand-held infrared thermometers were evaluated to assess the temperature resolution, the spatial resolution and performance (repeatability, stability and accuracy). linear regression and random effects analysis of variance. All devices were calibrated under laboratory conditions The agreement between the repeated measures at five ROIs in terms of radiance temperature versus the NPL black- for each instrument (intra-instrument agreement) and body calibration sources [17] over the range of 15 °C to between the two instruments at the same ROI (inter-instru- 45 °C, traceable to the international temperature scale of ment agreement) was quantified using intra-class correl- 1990 (ITS-90) with uncertainties of ±0.2 °C (k = 2, 95% ation coefficient (ICC) and the 95% confidence intervals confidence limit) quantified in accordance with the (CI) following a multilevel modelling approach (random ef- internationally agreed Guide to Uncertainty in Measure- fects regressions). If a substantial agreement between repli- ment (http://www.bipm.org/utils/common/documents/ cations was established, the replications within each ROI jcgm/JCGM_100_2008_E.pdf). were averaged. Bland and Altman analysis and plots were Participants were assessed after 20 min of barefoot rest used to complement the assessment of any bias between on a podiatry chair with their legs extended and sup- the two instruments [18]. The benchmark limits for agree- ported. Three consecutive measurement sequences were ment followed established classifications [18, 19]. In all carried out. In each sequence, thermal imaging alter- cases, for more rigour, in addition to the point estimate, the nated with hand-held thermometry. Initially a combined lower limit of the 95% CI was taken into account. plantar image of the right foot and left foot was captured with the thermal imaging device. This was followed by Results spot thermometry at five predefined ROIs (1st and 4th A total of 105 subjects (52 males and 53 females; age toes, and 1st, 3rd and 5th metatarsal heads). The tem- range 18 to 69 years (mean age 44 ± 11 years (mean ± peratures of each ROI were measured with the SD)), weight range 49 to 136 kg (mean weight 77.5 ± hand-held thermometer initially on the right foot and 16.2 kg), height range 1.50 to 1.98 m (mean height 1.70 ± then on the left foot. The same ROIs of the right foot 0.10 m), body mass index (BMI) range 18.2 to 51.8 kg/m and left foot were manually selected on each thermal (mean BMI 26.7 ± 5.4 kg/m2) were recruited in the study image and the temperatures were recorded (Fig. 1). at the three clinical centres. Temperature measurements were carried out by trained operators (one operator per Statistical methods: centre) and were taken in controlled room conditions. Temperature differences between feet (Right Foot-Left The mean study room temperature and humidity were 23 Foot) were calculated for each ROI for the thermal imaging ± 0.5 °C (mean ± SD) and 50 ± 8%RH, (mean ± SD) re- device and for the hand-held thermometer, respectively. spectively. In two subjects, the thermal imaging data was Each measure was replicated three times. The differences unavailable (the images were not saved after acquisition between repeated measurements as well as the differences and could not be recovered). Repeated measurement data between instruments (infrared thermal imaging device and for both instruments were available for 103 subjects. The hand-held thermometer) were modelled with multilevel mean duration of the temperature assessment (three Petrova et al. Journal of Foot and Ankle Research (2018) 11:22 Page 4 of 6 repeated sequences of alternating thermal imaging and Table 2 Measure of agreement between hand-held thermometer and thermal imaging device at five ROIs hand-held thermometry) was 3 min ±40 s (mean ± SD). No correction was made for skin emissivity as only ROIs Mean temperature P-value ICC (95% C.I.) difference (°C) between temperature differences were determined in this study and instruments (95% C.I.) it was assumed that skin emissivity was the same at 1st toe 0.04 (− 0.01, 0.10) 0.18 0.95 (0.93; 0.97) equivalent points on the foot. 4th toe 0.03 (− 0.05, 0.12) 0.42 0.94 (0.92; 0.96) 1st metatarsal head −0.01 (− 0.05, 0.04) 0.81 0.97 (0.95; 0.98) Intra-instrument agreement (agreement in replication) 3rd metatarsal head 0.11 (0.05, 0.17) < 0.001 0.96 (0.94; 0.97) The random effects linear regression analysis indicated that 5th metatarsal head 0.21 (0.16, 0.27) < 0.001 0.94 (0.91; 0.96) there were no significant differences in the temperature as- sessment between the three replications at all ROIs (1st toe Hand-held thermometer minus thermal imaging device p = 0.26; 4th toe p = 0.97; 1st metatarsal head p = 0.93; 3rd healthy volunteers in comparison with a hand-held infra- metatarsal head p = 0.69 and 5th metatarsal head p = 0.98). red spot thermometer. The intra-instrument agreement for the thermal imaging Both instruments showed agreement in repeated device and for the hand-held thermometer was similar at temperature assessment and also agreement between all five ROIs, as indicated by a non-significant instruments. Logistic regression analysis indicated that replication-by-instrument interaction in any of the five there were no differences in the repeated temperature measured ROIs: 1st toe p = 0.23; 4th toe p =0.97, 1st assessment at five ROIs between the two instruments. metatarsal head p = 0.23, 3rd metatarsal head p =0.84 and The inter-instrument ICCs at all ROIs were equal to or 5th metatarsal head p = 0.37. above 0.95 for the novel thermal imaging device and The intra-instrument ICCs for the thermal imaging equal to or above 0.94 for the hand-held infrared spot device ranged from 0.95 to 0.97 at the selected ROIs and thermometer, indicating almost perfect agreement in the intra-instrument ICCs for the hand-held-thermometer replication by instrument. Moreover, there was substan- ranged from 0.94 to 0.97, (Table 1). tial to perfect agreement in temperature assessment between the two instruments and the intra-instrument Inter-instrument agreement between hand-held ICCs were equal to or above 0.94 at all five ROIs. Bland thermometer and thermal imaging device and Altman plots showed that only a few points were Random effects linear regression, averaging the three outside the limits of agreement. Based on the bench- replications at the selected ROIs indicated that the mean mark limits for agreement, these analyses demonstrated difference between instruments (hand-held thermometer consistency of measure. minus thermal imaging device) ranged between − 0.01 °C In addition to the reported non-inferior performance in and 0.21 °C and the inter-instrument ICCs ranged be- temperature assessment at predefined ROIs, the novel tween 0.94 and 0.97, respectively (Table 2). thermal imaging device holds the potential to overcome At all five ROIs, Bland and Altman analysis indicated the significant limitations of spot thermometry and that the mean differences between the two instruments provide an instantaneous thermal image of all sites of the were very close to zero (Table 3) and the Bland and feet (plantar, dorsal, lateral and medial views), [16]. Indeed, Altman plots present the limits of agreement for all five the advantages of a full imaging acquisition sequence ROIs (Fig. 2). including plantar, dorsal, medial and lateral views captured Discussion Table 3 Limits of agreement between hand-held thermometer This study reports the performance of a novel thermal and thermal imaging device at five ROIs imaging device in the assessment of foot temperatures in ROIs Mean temperature Lower Limit Upper Limit difference (SD) °C (95% C.I.) °C (95% C.I.)°C 1st toe 0.04 (0.30) − 0.54 0.62 Table 1 Intra-instrument agreement in repeated measures at (− 0.64 to − 0.44) (0.52 to 0.72) five ROIs by instrument 4th toe 0.03 (0.42) −0.78 0.85 ROIs Hand-held thermometer Thermal imaging device (− 0.93 to − 0.64) (0.71 to 0.99) 1st toe 0.94 (0.92, 0.96) 0.95 (0.93, 0.96) 1st metatarsal head −0.01 (0.25) − 0.50 0.49 (− 0.58 to − 0.41) (0.40 to 0.57) 4th toe 0.95 (0.93, 0.96) 0.95 (0.94, 0.97) 3rd metatarsal head 0.11 (0.29) −0.47 0.69 1st metatarsal head 0.97 (0.96, 0.98) 0.97 (0.96, 0.98) (− 0.57 to − 0.37) (0.59 to 0.79) 3rd metatarsal head 0.96 (0.94, 0.97) 0.96 (0.94, 0.97) 5th metatarsal head 0.21 (0.29) − 0.35 0.78 5th metatarsal head 0.97 (0.95, 0.98) 0.97 (0.96, 0.98) (− 0.45 to − 0.26) (0.69 to 0.88) Data are presented as ICC (95% C.I.) for each ROI by instrument Thermal imaging device - Hand-held thermometer Petrova et al. Journal of Foot and Ankle Research (2018) 11:22 Page 5 of 6 with DFUPS in the temperature assessment of the feet of healthy volunteers have been reported [16]. In addition, thermal imaging with DFUPS does not require any cali- bration for age, gender, weight, height or BMI and there- fore it can be readily implemented in everyday clinical assessment. The importance of foot skin temperature monitoring in the identification of the early signs of inflammation has been emphasised in the 2015 guidelines of the International Working Group on the Diabetic Foot [20]. We have recently completed a multicentre clinical trial (NCT02579070) in high-risk diabetic foot patients to assess the usefulness of thermal imaging with DFUPS in addition to standard podiatric treatment to reduce diabetic foot ulcer recurrence. In addition to diabetic foot ulcer prevention, a further study is planned to investigate the usefulness of DFUPS in the assessment of the acute Charcot foot. Conclusions The newly developed thermal imaging device showed very good agreement in repeated temperature assessments at defined ROIs as well as substantial to perfect agreement in temperature assessment with a hand-held infrared therm- ometer. This device fulfils the requirements of a reprodu- cible and accurate thermal imaging device. It addresses the clinical need of a “portable, reliable and accurate” thermal imaging instrument [8, 13]. We believe that the developed thermal imaging device holds the potential of becoming a real asset in the diabetic foot clinic, to identify potential patients at risk of diabetic foot ulcer. Abbreviations BMI: Body mass index; CE: is abbreviated from Conformité Européenne, meaning European Conformity; CI: Confidence intervals; DFUPS: Diabetic Foot Ulcer Preventions System; ICC: Intra-class correlation coefficient; NHS: National Health Service; NPL: National Physical Laboratory; REC: Research Ethics Committee; ROI: Region of interest; ROIs: Regions of interest Acknowledgements The authors would like to thank the participants of this study and the project advisory board for their support and contribution to the study. Funding The research was funded by the National Institute for Health Research (NIHR) Invention for Innovation (i4i) programme (An Innovative system for the early identification, monitoring, evaluation and diagnosis of diabetic foot ulcers II-LA- 0813-20007). The views expressed are those of the authors and not necessarily those of the NHS, the NIHR or the Department of Health. Availability of data and materials The datasets used and/or analysed during the current study are available from NLP on reasonable request. Authors’ contributions All authors contributed to the design of the study. NLP, AM and SA recruited Fig. 2 Bland and Altman plots of agreement between the thermal participants and collected data. NLP, AW and AND processed and analysed imaging device and the hand-held thermometer for the 1st toe (a), 4th toe data. NLP, AW and MEE drafted the manuscript with input from all authors. (b), 1st metatarsal head (c), 3rd metatarsal head (d) and 5th metatarsal head All authors have read and approved the final manuscript. NLP and AW are joint first authors. GM and MEE are joint senior authors. Petrova et al. Journal of Foot and Ankle Research (2018) 11:22 Page 6 of 6 Ethics approval and consent to participate 14. Prompers L, Huijberts M, Apelqvist J, Jude E, Piaggesi A, Bakker K, Edmonds Approval for this study was obtained from the London-City Road and Hampstead M, et al. High prevalence of ischaemia, infection and serious comorbidity in Research Ethics Committee (REC reference 15/LO/0070). Each person in the study patients with diabetic foot disease in Europe. Baseline results from the was given a participant’s information sheet and all study participants provided Eurodiale study. Diabetologia. 2007;50(1):18–25. written informed consent. 15. Machin G, Whittam A, Ainarkar S, Allen J, Bevans J, Edmonds M, Kluwe B, Macdonald A, Petrova N, Plassmann P, Ring F, Rogers L, Simpson R. A medical thermal imaging device for the prevention of diabetic foot Consent for publication ulceration. Physiol Meas. 2017;38(3):420–30. https://doi.org/10.1088/1361- Consent for publication containing no personal identifying information was 6579/aa56b1. sought and gained from all participants. 16. Macdonald A, Petrova N, Ainarkar S, Allen J, Plassmann P, Whittam A, Bevans J, Ring F, Kluwe B, Simpson R, Rogers L, Machin G, Edmonds M. Competing interests Thermal symmetry of healthy feet: a precursor to a thermal study of The authors declare that they have no competing interests. diabetic feet prior to skin breakdown. Physiol Meas. 2017;38(1):33–44. https://doi.org/10.1088/1361-6579/38/1/33 . 17. Machin G, Chu B. High-quality blackbody sources for infrared thermometry Publisher’sNote and thermography between-40 and 1000 degrees C. Imaging Sci J. 2000; Springer Nature remains neutral with regard to jurisdictional claims in 48(1):15–22. published maps and institutional affiliations. 18. Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet. 1986;1:307–10. Author details 1 19. Landis JR, Koch GC. The measurement of observer agreement for Diabetic Foot Clinic, King’s College Hospital NHS Foundation Trust, Denmark 2 categorical data. Biometrics. 1977;33:159–74. Hill, London SE5 9RS, UK. Division of Diabetes and Nutritional Sciences, 3 20. IWGDF Guidance on the prevention of foot ulcers in at-risk patients with King’s College London, London, UK. Temperature and Humidity, National 4 diabetes. http://www.iwgdf.org/files/2015/website_prevention.pdf. Physical Laboratory, London, UK. Microvascular Diagnostics, Northern Medical Physics and Clinical Engineering, Newcastle upon Tyne Hospitals, Newcastle upon Tyne, UK. Community Podiatry Department, Pennine Acute Hospitals NHS Trust, Manchester, UK. Photometrix Imaging Ltd, Pontypridd, UK. Department of Computing, University of South Wales, Pontypridd, UK. Received: 23 March 2018 Accepted: 16 May 2018 References 1. Boulton AJM, Vileikyte L, Ragnarson-Tennvall G, Apelqvist J. The global burden of diabetic foot disease. Lancet. 2005;366(9498):1719–24. 2. Edmonds ME. The diabetic foot, 2003. Diabetes Metab Res Rev. 2004; 20(Suppl 1):S9–S12. 3. Rice JB, Desai U, Cummings AK, Birnbaum HG, Skornicki M, Parsons NB. Burden of diabetic foot ulcers for medicare and private insurers. Diabetes Care. 2014;37(3):651–8. 4. Diabetes UK. Improving footcare for people with diabetes and saving money: an economic study in England. https://diabetes-resources-production.s3-eu-west-1. amazonaws.com/diabetes-storage/migration/pdf/Improving%2520footcare%2520 economic%2520study%2520%28January%25202017%29.pdf Accessed 30 Apr 2018. 5. Chammas NK, Hill RL, Edmonds ME. Increased mortality in diabetic foot ulcer patients: the significance of ulcer type. J Diabetes Res. 2016;2016: 6. Vamos EP, Bottle A, Edmonds ME, Valabhji J, Majeed A, Millett C. Changes in the incidence of lower extremity amputations in individuals with and without diabetes in England between 2004 and 2008. Diabetes Care. 2010; 33(12):2592–7. 7. Ring F. Thermal imaging today and its relevance to diabetes. J Diabetes Sci Technol. 2010;4(4):857–62. 8. Pafili K, Papanas N. Thermography in the follow up of the diabetic foot: best to weigh the enemy more mighty than he seems. Expert Rev Med Devices. 2015;12(2):131–3. 9. Frykberg RG, Gordon IL, Reyzelman AM, Cazzell SM, Fitzgerald RH, Rothenberg GM, Bloom JD, Petersen BJ, Linders DR, Nouvong A, Feasibility NB. Efficacy of a smart mat Technology to predict development of diabetic plantar ulcers. Diabetes Care. 2017;40(7):973–80. 10. Armstrong DG, Holtz-Neiderer K, Wendel C, Mohler MJ, Kimbriel HR, Lavery LA. Skin temperature monitoring reduces the risk for diabetic foot ulceration in high-risk patients. Am J Med. 2007;120(12):1042–6. 11. Houghton VJ, Bower VM, Chant DC. Is an increase in skin temperature predictive of neuropathic foot ulceration in people with diabetes? A systematic review and meta-analysis. J Foot Ankle Res. 2013;6:31. 12. van Netten JJ, Prijs M, van Baal JG, Liu C, van der Heijden F, Bus SA. Diagnostic values for skin temperature assessment to detect diabetes- related foot complications. Diabetes Technol Ther. 2014;16(11):714–21. 13. Bharara M, Cobb JE, Claremont DJ. Thermography and thermometry in the assessment of diabetic neuropathic foot: a case for furthering the role of thermal techniques. Int J Low Extrem Wounds. 2006;5:250–60.

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Journal of Foot and Ankle ResearchSpringer Journals

Published: May 30, 2018

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