Keywords Infrared thermography, percutaneous transluminal angioplasty, peripheral arterial disease, ankle-brachial index

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1 Original Article Infrared thermography as option for evaluating the treatment effect of percutaneous transluminal angioplasty by patients with peripheral arterial disease Vascular 2017, Vol. 25(1) 42 49! The Author(s) 2016 Reprints and permissions: sagepub.co.uk/journalspermissions.nav DOI: / journals.sagepub.com/home/vas Erik Staffa 1, Vladan Bernard 1, Lubos Kubicek 2, Robert Vlachovsky 2, Daniel Vlk 1, Vojtech Mornstein 1, Ales Bourek 1 and Robert Staffa 2 Abstract Aim of this study was to evaluate the possible use of infrared thermography as a supplementary method to the anklebrachial index used in assessing the treatment effect of percutaneous transluminal angioplasty. The study included 21 patients, mean age was years. Healthy control group included 20 persons, mean age was years. Patients with symptomatic peripheral arterial disease (Fontaine stages I III) were admitted for endovascular treatment by percutaneous transluminal angioplasty. Thermal images and ankle-brachial index values were obtained before and after treatment by percutaneous transluminal angioplasty. Median temperature change in the treated limb was 0.4 C, for nontreated limb was 0.5 C. The median value of ankle-brachial index in the treated limb increased by 0.17 from 0.81 after the procedure. The median value of ankle-brachial index in the non-treated limb decreased by 0.03 from the value of Significant difference between treated limb and non-treated limb in change of ankle-brachial index was found with p value ¼ The surface temperature obtained by the infrared thermography correlates with ankle-brachial index. We present data showing that the increase of ankle-brachial index is associated with increase of skin temperature in the case of limbs treated by percutaneous transluminal angioplasty. Our results also suggest potential of the use of infrared thermography for monitoring foot temperature as a means of early detection of onset of foot ischemic disorders. Keywords Infrared thermography, percutaneous transluminal angioplasty, peripheral arterial disease, ankle-brachial index Introduction Peripheral arterial disease (PAD) is a common circulatory problem in which narrowed arteries reduce blood flow to limbs. 1 It is defined by progressive stenosis or occlusion within the arteries of the lower extremities. 2 PAD decreases functional capacity, which lead to disability and poor quality of life. The major risk factor for symptomatic PAD is smoking and diabetes mellitus (DM). Other risk factors include advanced age, male gender, dyslipidemia, hypertension, hyperhomocysteinemia, and renal insufficiency. 3 Diabetes can lead to a number of severe complications, the diabetic foot syndrome and diabetic neuropathy are the major longterm complications. 4,5 PAD and DM complications may progress to critical limb ischemia (CLI), which portends a severe diminution in quality of life, and is associated with a high rate of amputation and a marked increase in short-term mortality. 2,6 The rationale for foot skin temperature monitoring is based on several studies. 7 9 Higher forefoot skin temperature of diabetic patients with painful neuropathy in comparison with control subjects was described by Chan and colleagues 10 and by Armstrong et al. 11 Lavery et al. 12 and 1 Department of Biophysics, Faculty of Medicine, Masaryk University, Brno, Czech Republic 2 2nd Department of Surgery, Center for Vascular Disease, St. Anne s University Hospital, Faculty of Medicine, Masaryk University, Brno, Czech Republic Corresponding author: Erik Staffa, Department of Biophysics, Faculty of Medicine, Masaryk University, Brno, Kamenice 5, 62500, Czech Republic. staffa@mail.muni.cz

2 Staffa et al. 43 van Netten et al. 9 demonstrated in their studies that the difference temperature >1.5 C between contralateral feet was observed by the patients with diabetes. Infrared thermography has the advantages of being non-invasive, fast and it is safe for patients and doctors. Several techniques are currently being used to screen lower extremity PAD. One of them is an ankle-brachial index (ABI). It is a reproducible, non-invasive index used to screen and detect PAD, 13 but with certain limitations. 14 The purpose of this study was to compare temperature changes in the skin of patients before and after revascularization by percutaneous transluminal angioplasty (PTA) and to identify possible correlation between ABI value and foot skin temperature. We hypothesized that the revascularization by PTA would influence the cutaneous temperature and infrared thermography could offer another non-invasive option in PAD evaluation. Methods This prospective controlled study was performed on a group of 21 patients (seven female and 14 male), mean age was (range 47 to 76) years in the period from April 2014 to October These patients had symptomatic PAD but without visible defects and ulcerations on lower limb (PAD Fontaine stages II-III). We excluded all patients with any amputation procedure performed on lower limb and infected limbs. Patients with non-compressible arteries (where it was not possible to obtain appropriate ABI values) were also excluded from the study. Healthy control group consisted of 20 participants (14 female and 6 male), mean age was (range 29 to 83) years. This group could not be well matched in terms of age to the other two groups because of difficulty in recruiting age-matched subjects. We used the control group only to be sure that in healthy people there is no recordable marked difference in surface temperature of the sole of the contralateral feet. Thermal images of the soles of the control group were recorded and analyzed in the same conditions as in the case of treated patients. The patients and volunteers demographic data are listed in Tables 1 and 2. Patients were admitted to the department of surgery for endovascular treatment. The assessment of arteries (aorta, iliac arteries and limb arteries) was performed by CT angiography and classified by use of Fontaine scale 15 before and after procedure. The patients were admitted to the hospital ward on the day of treatment by PTA or one day before. The treatment was performed on first or second day and patients were discharged on third or fourth day, respectively. Thermal images of the soles were recorded after bed rest of more than 10 minutes using infrared camera Table 1. Patient demographic data (n ¼ 21 patients). Variable Value Gender Male 14 (66.67) Female 7 (33.33) Mean age SD Range of age 47 to 76 Smoking 17 (80.95) Diabetes 6 (28.57) Body weight (kg) Range of weight 61 to 117 Mean value BMI SD Data presented as mean standard deviation or n (%). Table 2. Control group demographic data (n ¼ 20 volunteers). Variable Value Gender Male 6 (30) Female 14 (70) Mean age SD Range of age 29 to 83 Smoking 0 (0) Diabetes 2 (10) Data presented as mean standard deviation or n (%). FLIR B200 (Flir Systems, Danderyd, Sweden) equipped with focal plane array microbolometer thermal detector, IR resolution, spectral range 7.5 mm to 13mm. The absolute accuracy of the measuring device used is declared at 2 Cor2% of reading. Thermal sensitivity is 0.08 C. The obtained thermal images were processed using FLIR QuickReport 1.2 (Flir Systems, Danderyd, Sweden) software. The infrared camera was positioned 1 meter away from the patients soles. All images were standardized to the same temperature range 22 Cto35 C and converted to the rainbow color palette by the software. The same value of emissivity was used for all images or for all of their analyzed parts, " ¼ All thermal images were produced under the controlled environmental conditions, with controlled ambient room temperature, relative humidity and restricted air flow. Ignoring these factors would have a negative impact on the reproducibility of thermal images. 16,17 The images were recorded before treatment by PTA and then on the next day after the performed successful PTA treatment.

3 44 Vascular 25(1) Figure 1. The thermal image of the patient s lower limb treated with PTA. Image A shows limb before treatment with PTA, image B shows patients limb on the next day following treatment. The arrow! marks the limb treated by the endovascular intervention. The thermal range is 22 Cto35 C. By using lines L1 and L2, points of temperature measurement on limbs are defined. Ankle and brachial pressures were measured by a calibrated standard medical mercury tonometer together with Doppler ultrasound using standardized Doppler ultrasonic device (Hadeco, Inc., Bi-Dop ES- 100V3, Japan). Measurements were performed by a physician after a 10-minute rest in the supine. ABI was calculated as the ratio of the higher of the two systolic pressures (from posterior tibial and dorsalis pedis artery) at the ankle to the higher of the right and left brachial artery pressures. 18 PAD was defined as having a resting ABI of 0.9. The ABI for each one patient was determined for both lower limbs. Finally, the difference of ABI value after PTA and before PTA was calculated for limb with endovascular intervention ( ABI ) and for the limb without endovascular intervention ( ABIc ) for each one patient. The median value was calculated from obtained ABI and ABIc. PTA procedure All patients had diagnostic angiography of the lower limbs performed prior to interventional treatment. All endovascular procedures were performed according to Seldinger under local anaesthesia by experienced interventional radiologists. The decision to perform a PTA (the femoro-popliteal and the cruro-pedal arteries) was made in consultation of the multidisciplinary committee of the department of surgery. The median temperature value used in the following statistic evaluations was obtained from the soles of the right and left foot (Figure 1), temperature measurement points were selected along a line connecting the second toe and the heel (line L1 and L2 on Figure 1). To monitor the temperature development in time, the value of the temperature change ( TEMP for the limb with endovascular treatment and TEMPc for limb without endovascular treatment) were calculated as the difference of temperature after treatment by PTA and the temperature before PTA treatment. Statistical evaluation was performed by the STATISTICA 12 (StatSoft CR Ltd., Prague, Czech Republic) software. The data were tested by authors for normality by Shapiro-Wilk test or the P-P graphs. For statistical difference obtained data were tested by means of Student s t-test on the statistical significance level of 5% (p.05). The obtained data are presented in box-plot graphs (Figure 2). Results The study presents the thermal images of lower limb in patients who underwent endovascular treatment by PTA. Lower limbs and soles of the feet had no visible tissue damage or ulcerations. Each patient was measured by non-contact infrared thermography method and by ABI before endovascular treatment by PTA and after the PTA treatment. Our obtained results of non-contact infrared thermography and ABI measurements are presented in Tables 3 and 4. The outcomes of these measurements are presented as the difference of temperature values of lower limb in C before and after the treatment. Initially we examined healthy control group by the infrared camera. The median temperature difference of contralateral foot soles in this group was 0.3 C (range 0.0 C to 0.6 C). In the group of patients before their treatment by PTA the median temperature difference was 0.6 C (range 0.0 C to 1.5 C). Median temperature change in the limbs treated by PTA was 0.4 C and for the non-treated limbs it was 0.5 C. The median value of ABI was 0.17 (range 0.42 to 0.55) and the median value of ABIc for the control foot was 0.03 (range 0.34 to 0.29). The median value

4 Staffa et al. 45 Figure 2. Left: the statistical distribution of TEMP and TEMPc values; p value ¼.11. Right: The statistical distribution of ABI and ABIc values; p value ¼ Table 3. Comparison of preoperative and postoperative results by patients ABI value (the change of ABI value for limb treated by PTA as ABI, untreated limb without PTA as ABI contr), temperature of soles (for limb treated by PTA as TEMP, for untreated limb as TEMP contr), stenosis according to computed tomography visualization in arteria iliaca communis (AIC), a. illiaca externa (AIE), a. femoralis superficialis () and a. tibialis posterior (ATP), fontaine classification divided by stages. Patient Stenosis (%) AIC 90 AIE 70 AIE AIE 60 AIC ATP Fontaine class. IIb IIb IIb IIa IIb IIb IIb-III IIb-III IIa IIb IIb ABI before ABI after " ABI ABI contr before ABI contr after " ABI contr TEMP before TEMP after " TEMP ( C) TEMP contr before TEMP contr , after " TEMP contr ( C) ABI: ankle-brachial index; PTA: percutaneous transluminal angioplasty. for ABI before PTA was 0.81 (range 1.15 to 0.23) for treated limb and 1.01 (range 1.59 to 0.13) for non-treated limb, respectively. The median value for ABI after treatment by PTA was 0.91 (range 1.50 to 0.27) for treated limb and 1.00 (range 1.45 to 0.10) for nontreated limb, respectively. The statistical distribution for both groups is presented in Figure 2. The boxplot graphs of the statistical distribution of ABI and

5 46 Vascular 25(1) Table 4. Comparison of preoperative and postoperative results by patients ABI value (the change of ABI value for limb treated by PTA as ABI, untreated limb without PTA as ABI contr), temperature of soles (for limb treated by PTA as TEMP, for untreated limb as TEMP contr), stenosis according computed tomography visualization, fontaine classification divided by stages. Patient Sum Median value Stenosis (%) 50 AIC ACI Fontaine class. IIb IIb IIb IIb-III IIa IIb IIa-b IIb IIb IIa ABI before ABI after " ABI ABI contr before ABI contr after " ABI contr TEMP before TEMP after " TEMP ( C) TEMP contr before TEMP contr after " TEMP contr ( C) ABI: ankle-brachial index; PTA: percutaneous transluminal angioplasty. temperature changes ( C) showed lower values for data before treatment as compared to after treatment. The relation between the increase of the temperature and the increase of the value of ABI in the limb treated by the endovascular procedure is shown in Figure 3. Data in the graph on Figure 3 are presented as a relation in the difference of the development of ABI (ABI ABI contr) and in the difference of the development of temperature (TEMP TEMP contr) after the PTA treatment. The slope of value in plotted graphical dependence shows increasing trend and association of the temperature and ABI development. The obtained data of ABI and ABIc or TEMP and TEMPc were tested for normality. Normal distribution was confirmed for both monitored variables by using the Shapiro-Wilk test. The statistically significant differences with p value ¼.0035 were found for variable ABI and ABIc. The Student s t-test performed for variables TEMP and TEMPc showed p value ¼.11. TEMP shows the temperature difference (before and after PTA) of limb with endovascular intervention and TEMPc shows the temperature difference for a limb without endovascular intervention. ABI shows the difference of ABI value for the limbs with performed endovascular intervention and ABI-c shows difference for the limbs without endovascular intervention. Patients before treatment by PTA and after treatment were scanned with an infrared camera. According to the infrared measurements the thermal symmetry is a normal finding in healthy group and it was demonstrated that high temperature gradients between feet may predict the formation of ischemic changes. Obtained thermal images were statistically evaluated from the perspective of the average temperature. Images were also evaluated and compared with one another (Figure 1). It is evident that the temperature of patient s lower limb underwent changes during time. Increase of temperature was seen on the limb treated by PTA on the other hand decrease of temperature was seen in the limb without PTA treatment (Figure 1). The increase of temperature was observed for the whole surface of the foot. The decrease of temperature was observed for the whole surface of the foot, but especially in the toe region. However, we did not include the temperature of toes into the statistical evaluation. Discussion The purpose of this study was to measure and describe thermal changes of lower limbs in patients before and after endovascular procedure and to compare this method with the determination of ABI.

6 Staffa et al. 47 Figure 3. The relation of the temperature of lower limb (TEMP TEMP contr, C) with development of ABI values (ABI ABI contr). Changes of surface temperature of lower limbs before and after treatment by PTA were compared. All patients involved in the study presented no ulcerations or amputations. The results demonstrate the change of temperature of limbs after revascularization. We must bear in mind that we evaluated the surface temperature, not the internal temperature. It is evident that the surface temperature of treated limb increased in the monitored group. This result can be seen as important and has the potential to be used as an indicator of the successful increase of blood supply as a result of the PTA treatment. We can assume that the increase of the limb perfusion will be accompanied by increase of the limb surface temperature and ABI. It remains questionable if the observed change in skin temperature may have been caused by some undesirable reactions of the organism, e.g. increased temperature as a result of an inflammatory reaction. We argue that this effect can be excluded, since none of the study subjects suffered from postoperative complications. Another fact supporting our hypothesis is that the box-plot graphs of temperature changes did not show extreme or outlying values. On the contrary, we observed the decrease of temperature for the PTA untreated limb. We find this observation very interesting, since our original assumption was that the temperature will not change. It can be speculated that the temperature decreased due to the inactivity of the limb (at least 24 hours immobility of patients after PTA procedure as a prevention of puncture site hematoma). It is improbable that the temperature decrease was caused by lesser blood supply or limited circulation due to the revascularization performed on the contralateral limb. The highest drop of temperature was identified at the toes. It is also necessary to take into consideration that patients lying in a horizontal position during hospitalization may have changes in hydrostatic pressure of blood. That could be the cause of the observed temperature decrease. Based on this temperature decrease observed in the untreated limb we can state that the absolute increase of temperature in the treated leg is even more marked. Specific areas on the sole of a foot having a significant increase (decrease) in temperature were not recorded, unlike in the work of Peregrina-Barreto et al 19 The authors of this study reported that four specific areas of different temperatures are on the sole of a foot. This phenomenon was not observed in our study. The change of ABI value before and after revascularization (ABIc) for non-treated limb was not observed. The change of ABI value was observed in the treated limb. The change of ABI was positive with value of It is evident that the blood supply increased after treatment with PTA in the treated limb, but not in the non-treated. We can conclude that the results of measurements obtained by the infrared camera correspond with development of ABI values during our study. It is evident that the increase of ABI is associated with increase of temperature in the limbs treated by the endovascular intervention. The temperature drop for the non-treated limb is also interesting and although unexpected seems

7 48 Vascular 25(1) to be explainable by hydrostatic blood pressure decrease due to bed rest after treatment. Although the infrared camera is not a universal diagnostic tool it should be considered a suitable diagnostic instrument and as a supplementary diagnostic modality for diabetic patients. Its use may be beneficial for monitoring patients after endovascular treatment with PTA (or alternative revascularization methods). Our study showed the temperature changes before and after treatment and compared them with ABI measurement. Infrared camera thermography could become a timesaving method for physicians and at the same time a method very convenient for the patients. On the other hand it represents an indirect method of blood flow measurement as opposed to currently used ABI measurement, but some authors came to a conclusion that the accuracy of the ABI in predicting revascularization failure is poor. 14 These authors note that the ABI measurement is not site-specific and may reflect changes elsewhere in the arterial tree. Therefore, the measurement of the ABI alone is not a reliable method for demonstrating the revascularization effect. This is just one more reason to focus on thermography observation and follow-up. Thermographic observation of blood flow quality in lower limb revascularization must be still evaluated individually, although in the future, this method could become a very quick and effortless complementary method for evaluating the degree of vascular disability in patients with lower limb ischemia. In conclusion, the surface temperature of lower limbs obtained by the infrared camera corresponded with development of ABI values in the course of our study. We have found that the increase of ABI index is associated with increase of temperature in the limbs treated by PTA. Presented results show that the infrared camera is a useful complementary method to performing the ABI. From the authors perspective it can be concluded that temperature measurement by means of the infrared camera provided the same level of information about the success of revascularization procedures of the limb as using the ABI measurement. Statement of patient consent All patients confirmed their participation in the study by signing of the standard Patient consent protocol. Signed protocols are archived in each patient s documentation. Acknowledgement The authors thank Bohuslav Vojtı sˇ ek and Igor Susˇ kevicˇ for performing the treatment by PTA. Declaration of conflicting interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article. Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The study was supported by the projects MUNI/A/ 0894/2015 and MUNI/A/1449/2014. References 1. Diseases and Conditions. Peripheral artery disease (PAD). Mayo clinic, (accessed 28 January 2015). 2. Bordeaux LM, Reich LM and Hirsch AT. The epidemiology and natural history of peripheral arterial disease. In: JD Coffman and RT Eberhardt (eds) Peripheral arterial disease. Totowa, NJ: Humana Press 2003, pp Fowkes FG, Housley E, Cawood EH, et al. Edinburgh Artery Study: prevalence of asymptomatic and symptomatic peripheral arterial disease in the general population. Int J Epidemiol 1991; 20: Armstrong D, Lavery L, Wunderlich R, et al. Skin temperatures as a one-time screening tool do not predict future diabetic foot complications. J Am Podiatr Med Assoc 2003; 93: Burns S and Jan YK. Diabetic foot ulceration and amputation. In: Kim CT (ed.) Rehabilitation medicine. Croatia: InTech Publisher, 2012, pp Leibson CL, Ransom JE, Olson W, et al. Peripheral arterial disease, diabetes, and mortality. Diabetes Care 2004; 27: Benbow SJ, Chan AW, Bowsher DR, et al. The prediction of diabetic neuropathic plantar foot ulceration by liquid-crystal contact thermography. Diabetes Care 1994; 17: Stess RM, Sisney PC, Moss KM, et al. Use of liquid crystal thermography in the evaluation of the diabetic foot. Diabetes Care 1986; 9: Van Netten JJ, Van Baal JG, Liu C, et al. Infrared thermal imaging for automated detection of diabetic foot complications. J Diabetes Sci Technol 2013; 7: Chan AW, MacFarlane IA and Bowsher DR. Contact thermography of painful diabetic neuropathic foot. Diabetes Care 1991; 14: Armstrong DG, Lavery LA, Liswood PJ, et al. Infrared dermal thermometry for the high-risk diabetic foot. Physical Ther 1997; 77: Lavery LA, Higgins KR, Lanctot DR, et al. Preventing diabetic foot ulcer recurrence in high-risk patients: use of temperature monitoring as a self-assessment tool. Diabetes Care 2007; 30: Hiatt WR, Goldstone J, Smith SC, et al. Atherosclerotic Peripheral Vascular Disease Symposium II nomenclature for vascular diseases. Circulation 2008; 118:

8 Staffa et al Aboyans V, Criqui MH, Abrahamet P, et al. Measurement and Interpretation of the Ankle-Brachial Index: a scientific statement from the American Heart Association. Circulation 2012; 126: Novo S. Classification, epidemiology, risk factors, and natural history of peripheral arterial disease. Diabetes Obesity Metab 2002; 4: Bagavathiappan S, Saravanan T, Philip J, et al. Investigation of peripheral vascular disorders using thermal imaging. Br J Diabetes Vasc Dis 2008; 8: Bernard V, Staffa E, Mornstein V, et al. Infrared camera assessment of skin surface temperature effect of emissivity. Physica Medica 2013; 29: Norgren L, Hiatt WR, Dormandy JA, et al. Inter-society consensus for the management of peripheral arterial disease (TASC II). Eur J Vasc Endovasc Surg 2007; 33: Peregrina-Barreto H, Morales-Hernandez LA, Rangel- Magdaleno JJ, et al. Quantitative estimation of temperature variations in plantar angiosomes: a study case for diabetic foot. Computat Mathem Meth Med 2014; 2014: 1 10.

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