Abstract
Objective
We hypothesized that the severity of foot poikilothermy can be used for better differentiation of grades of acute limb ischemia. Thus, the study aim was evaluation of the value of non-contact foot thermometry, performed using a low-cost infrared medical thermometer, as an adjunct for clinical diagnosis of immediately threatened acute limb ischemia.
Methods
It was a single-center observational prospective study performed over 3 years. Patients with acute limb ischemia of lower limbs grade I–IIB Rutherford treated with urgent revascularization were included. Grade of ischemia was determined independently by two experienced vascular surgeons. Thermometry of the ischemic foot was performed using a medical digital infrared non-contact thermometer (CK-T1501, Cooligg, China) with measuring accuracy of ±0.2°C. Temperature was measured in three points: the dorsal surface of the foot, plantar surface of the foot (both in the metatarsal region), and forehead. The maximal temperature gradient between patient’s forehead and foot (∆Tmax F-F) was calculated. Measurements were repeated 6–12 h after revascularization.
Results
A total of 147 patients were included. Only 3 (2%) patients presented rest pain without sensory loss and motor deficit, while the majority were diagnosed with mild (63/147, 42.8%) or moderate (27/147, 18.3%) motor deficit. The temperature of the ischemic foot varied from 20 to 36.1°C, while median value of the temperature was 26.7 [24.5–29.9] °C on the dorsal surface and 26.8 [24.5–29.6] °C on the plantar surface of the foot (p = 0.85). Patients with Grade IIB ischemia had significantly lower dorsal foot temperature, plantar foot temperature, and larger ∆Tmax F-F than the patients with grades I–IIA: 25.1 [23.9–26.8] °C versus 29.9 [27.6–30.8] °C; 25.2 [23.8–27.5] °C versus 29.6 [28–31.1] °C; and 11.6 [9.7–12.8] °C versus 7.2 [6–9] °C (p < 0.0001). Areas under ROC curve for diagnosis of Grade IIB ischemia were similar for dorsal foot temperature (0.82), plantar temperature (0.81), and ∆Tmax F-F (0.82). The best cutoff value by Youden was ≥9.5°C for ∆Tmax F-F, ≤26.8°C for dorsal, and ≤27.7°C for plantar temperature. Criterion ∆Tmax F-F offered the highest specificity of 86% (95%CI 74.2–93.7) and positive predictive value of 89.2% (95%CI 79.5–93.2), while plantar temperature offered sensitivity of 82.5% (95%CI 70.1–91.3) and negative predictive value of 69.1% (95%CI 57.6–83.2). In multivariate analysis including age, gender, and etiology of arterial occlusion, the criterion ∆Tmax F-F of ≥9.5°C was a unique variable significantly associated with risk of amputation (adjusted OR 2.6, 95%CI 1.2–5.9, p = 0.01).
Conclusion
Current study demonstrated that patients with immediately threatening ALI have significantly lower foot temperature than those with viable and marginally threatened limbs. Severe foot poikilothermy at admission is associated with poor outcomes of revascularization, mostly with limb loss.
Introduction
Acute limb ischemia (ALI) is a common vascular emergency associated with high mortality and limb loss rates. 1 Despite the widespread use of contemporary vascular imaging and implementation of new percutaneous techniques for revascularization (thrombolysis and mechanical and pharmaco-mechanical thrombectomy), the treatment outcomes of ALI have not improved significantly during the last decades. 2
The time interval from the onset of ischemia till the restoration of perfusion is critically important for the preservation of functional limb and the prevention of systemic complications caused by ischemia-reperfusion syndrome.3,4 Urgency of the revascularization procedure depends on the severity of ischemia and is traditionally classified into four categories described by Rutherford. 5 Differentiation of these grades is mainly based on clinical determination of sensory and motor deficit at the level of ischemic foot. It is augmented by evaluation of arterial and venous Doppler signals.1,5
We hypothesized that severity of foot poikilothermy caused by ischemia could be quantified and used for differentiation of grades of ischemia. Thus, the study aim was an evaluation of the value of non-contact foot thermometry, performed using standard infrared medical thermometer, as an adjunct for clinical diagnosis of immediately threatened ALI.
Material and methods
Patients
It was an observational prospective study performed during 3 years (01.02.2020–31.01.2023) in a single tertiary center—24/7 vascular service of the Institute of Emergency Medicine (Chisinau, Moldova). The inclusion criteria were (1) ALI of lower limbs treated with urgent (<24 h from admission) open, endovascular, or hybrid revascularization; (2) grades I–IIB of ischemia according to Rutherford classification. Patients were excluded if they met any of the following criteria: (1) ALI caused by trauma, aortic dissection, spasm, or early complications of vascular interventions; (2) acute onset of intermittent claudication; (3) irreversible (Grade III) ischemia requiring limb amputation; (4) patients with fever (≥38°C); (5) impossibility to define the grade of ischemia clinically (non-cooperant patients, pre-existing neurological deficit at the level of affected limb, and previous foot amputation). Demographic characteristics and comorbidities of the patients; clinical data relevant to the diagnosis and severity of ALI; type of revascularization procedure and treatment outcomes were registered in a dedicated prospective electronic database.
The study protocol was elaborated according to the principles of the Declaration of Helsinki and approved by Research Ethics Committee of the State University of Medicine and Pharmacy “Nicolae Testemitanu,” Chisinau, Moldova. Written informed consent for study participation was obtained from all enrolled patients.
Clinical diagnosis of ALI and determination of severity of ischemia
Diagnosis of ALI was made clinically by a qualified vascular surgeon, and severity of ischemia was classified according to the Rutherford categories: Grade I—rest pain without sensory loss and motor deficit, Grade IIA—sensory loss without motor deficit, and Grade IIB—any motor deficit. Audible arterial Doppler signal upon pedal arteries was interpreted as an indicator of non-immediately threatening ALI and absence of venous signal as a sign of irreversible ischemia.1,5 In patients with audible arterial signal, the ankle-brachial index (ABI) value was calculated; two experienced vascular surgeons determined the ischemia’s grade independently, and any discrepancies were resolved through consensus. Preoperative duplex ultrasound and/or computed tomography angiography were used on the discretion of operating surgeon and depending on availability. In patients with symptoms of compartment syndrome, direct pressure measurement in the leg compartments was performed.
Assessment of foot poikilothermy
After the clinical examination of the patient in emergency department, the thermometry of the ischemic foot was performed using a medical digital infrared non-contact thermometer (CK-T1501, Cooligg, China) with measuring accuracy of ±0.2°C. Measurements were performed in a standard examination room with air conditioning (environmental temperature 20 °C–22 °C), in the recumbent position of the patient, after at least 10 min of rest and exposure of the affected limb. The skin temperature was measured in centigrade at the distance of 3–5 cm from the skin in three points: the dorsal surface of the foot, plantar surface of the foot (both in the metatarsal region), and forehead (Figure 1). Measurements were repeated twice in each point and arithmetic means were calculated. The maximal temperature gradient between the patient’s forehead and foot (∆Tmax F-F) was calculated subtracting the lowest foot temperature (dorsal or plantar) from the forehead temperature. Measurements were repeated 6–12 h after revascularization. Measurement of forehead and dorsal surface foot temperature in a patient with ALI, using a low-cost infrared medical thermometer (temperature gradient between forehead and foot is 10.6°C).
Revascularization
Open thrombectomy mainly was performed for limb revascularization using Fogarty balloon catheters and standard surgical technique. Endarterectomy, surgical bypass, and endovascular techniques (thrombo-aspiration, angioplasty, and stenting) were used as an adjunct or as an alternative approach if thrombectomy was considered unsuccessful. Thrombolysis was not used as a primary approach for limb revascularization in the study cohort. A four-compartment fasciotomy was performed if clinical signs of compartment syndrome were present or compartment pressure exceeded 30 mmHg. All patients received heparin perioperatively and were discharged on antithrombotic treatment, tailored individually based on cause of ALI, type of revascularization, and comorbidities.
Study outcomes
The grade of ischemia, determined clinically by two qualified experts, was used as a reference for evaluation of the diagnostic performance of foot thermometry. The results of revascularization were analyzed by rate of fasciotomy, unplanned return to the operating room, rate of major amputation and/or death at 30 days after surgery, and postoperative ABI value.
Statistical analysis
The Kolmogorov–Smirnov test was used to test the normality of data distribution. Categorical variables are presented as absolute numbers with percentage (95% confidence intervals) and continuous variables as medians with 25%–75% interquartile range or means ± standard deviation. Difference of medians was assessed by Mann–Whitney test and difference of means by two-tailed t test. The receiver operating characteristic (ROC) curve was constructed to evaluate the sensitivity and specificity of foot thermometry, and the best cutoff values were determined by Youden index. The association of variables with outcome was tested in univariable and multivariable models. Binary logistic regression with calculation of odds ratios was used to analyze the association of variables with dichotomous outcomes. Spearman rho coefficient was calculated to assess the correlation between variables. A p-value <0.05 was considered statistically significant. Statistical analysis was conducted using “GraphPad Prism” (v. 8.0.1, GraphPad Software, San Diego, California, USA) and SPSS 22.0 (SPSS Inc., Chicago, IL, USA) software.
Results
Clinical and demographic characteristics of included patients
Baseline demographic and clinic data of study participants.
Continuous variables presented as median [25–75 IQR] or mean (±SD) values; SBP—systolic blood pressure; DBP—diastolic blood pressure; ECG—electrocardiography; ASA—American Society of Anesthesiologists; ALI—acute limb ischemia; ABI—ankle-brachial index.
Preoperative foot thermometry in different grades of ALI
Results of foot thermometry in patients with different Rutherford grades of acute limb ischemia.
ALI—acute limb ischemia. Variables are presented as medians [25–75 IQR]; *—Kruskal–Wallis test (ANOVA); ∆Tmax F-F—maximal foot to forehead temperature gradient calculated by subtraction of the lowest foot temperature (dorsal or plantar) from forehead temperature.
The preoperative value of ∆Tmax F-F was 9.8 [7.3–12.4] °C in patients with embolism and 10.6 [7.3–12.5] °C in patients with “acute on chronic ischemia” (p = 0.74). Sensitivity analysis showed a significant difference of the gradient between ALI Grade IIB and ALI grades I–IIA in both subgroups: 11.5 [9.5–12.8] °C versus 7.5 [6–9] °C in case of embolism and 11.7 [10.1–12.8] °C versus 7 [6.3–9.6] °C in case of thrombosis (p < 0.0001 for both comparisons). The results of foot thermometry did not demonstrate an association with duration of ischemia and occluded arterial segment (data not shown).
Predictive value of foot thermometry in the diagnosis of immediately threatened limbs
Dorsal foot temperature, plantar temperature, and criterion ∆Tmax F-F all demonstrated a similar discriminating ability in differentiation of immediately threatening ischemia and ALI grades I–IIA, with an area under ROC curve of 0.82 ± 0.03 (95%CI 0.75–0.89), 0.81 ± 0.03 (95%CI 0.74–0.88), and 0.82 ± 0.03 (95%CI 0.75–0.89), respectively (Figure 2). The best cutoff value determined by Youden index was ≥9.5°C for criterion ∆Tmax F-F, ≤26.8°C for dorsal foot temperature, and ≤27.7°C for plantar temperature. Using these cutoff values, criterion ∆Tmax F-F offered the highest specificity of 86% (95%CI 74.2–93.7) and positive predictive value of 89.2% (95%CI 79.5–93.2), while plantar temperature offered sensitivity of 82.5% (95%CI 70.1–91.3) and negative predictive value of 69.1% (95%CI 57.6–83.2). In clinical context, the sensitivity of the thermometry could be more important, assuring that no cases of immediately threatening ischemia are missed. In our cohort, the cutoff value of ∆Tmax F-F >6°C and plantar temperature <30°C offered sensitivity of 96.7% and 95.6% in diagnosis of ALI grade IIB, respectively. Receiver operating characteristic (ROC) curve for gradient between forehead and lowest foot temperature (∆Tmax F-F), temperature of the dorsal surface (Tdors), and temperature of the plantar surface (Tplant) of the foot versus immediately threatening acute limb ischemia (ALI) diagnosed clinically by independent experts (best cutoff values, sensitivity, and specificity are presented in the text).
Association of preoperative foot temperature and outcomes of ALI treatment
Open thrombectomy was performed in 107 (72.7%) patients, endarterectomy or surgical bypass in 30 (20.4%) patients, and percutaneous revascularization in 10 (6.8%) patients. Sixteen (10.8%) patients required unplanned return to the operating room for repeated revascularization, and fasciotomy was needed in thirty-three (22.4%) cases. The median ABI value increased to 0.92 [0.68–1] postoperatively and did not correlate with the preoperative values of foot thermometry (rs = −0.04, p = 0.56). At 30 days after revascularization 27 (18.3%) patients died, and 17 (11.5%) suffered major amputation of the index limb. The preoperative values of ∆Tmax F-F were significantly different in patients with positive and negative outcomes of ALI treatment (Figure 3). Patients with preoperative value ∆Tmax F-F of ≥9.5°C had significantly higher rates of fasciotomy (OR 3.9, 95%CI 1.6–9.9, p = 0.003) and major amputation (OR 5.1, 95%CI 1.4–18.9, p = 0.01), but not of reintervention (OR 0.79, 95%CI 0.2–2.2, p = 0.6) and death (OR 1.9, 95%CI 0.8–4.5, p = 0.1). In multivariate analysis (binary logistic regression) including age, gender, and etiology of arterial occlusion, the criterion ∆Tmax F-F of ≥9.5°C was a unique variable significantly associated with risk of amputation: adjusted OR 2.6, 95%CI 1.2–5.9, p = 0.01. Preoperative values of maximal temperature gradient (∆Tmax) between forehead and foot in patients with different outcomes of ALI treatment. FT: fasciotomy; Re: reintervention; A: amputation; A/D: amputation and/or death. Boxes display medians with 25%–75% IQR and whiskers indicate lowest and highest values. *—Mann–Whitney test.
Foot thermometry after revascularization
Expectedly, the foot temperature increased after revascularization. The median postoperative values registered on the dorsal and plantar surfaces of the foot were 36.2 [35.2–36.5] °C and 36 [34.5–36.4] °C, respectively, while the median value of the criterion ∆Tmax F-F constituted 0.5 [0.3–1.8] °C. All three variables differed significantly in patients with treatment failure compared to the patients with successful limb salvage: dorsal foot temperature 29.5 [22.1–36.1] °C versus 36.4 [35.8–36.6] °C, plantar temperature 28.8 [21.7–35] °C versus 36.2 [35.2–36.4] °C, and criterion ∆Tmax F-F 8 [1.6–14.7] °C versus 0.4 [0.2–1.1] °C (p < 0.0001). Results of thermometry after revascularization demonstrated moderate to strong correlation with postoperative ABI values: r = 0.53 (95% CI 0.4–0.64) for dorsal foot temperature, r = 0.59 (95% CI 0.46-0.68) for plantar temperature, and r = −0.61 (95% CI −0.7 to −0.49) for criterion ∆Tmax F-F (p < 0.0001). Postoperative temperature gradient ∆Tmax F-F of more than 1.5°C was associated with the risk of limb loss (OR 11.3, 95%CI 3.4–37.3, p = 0.0001).
Discussion
To our best knowledge, this is the first study evaluating the diagnostic and predictive role of foot thermometry using standard non-contact infrared thermometer in patients with ALI supposed to urgent revascularization. The study showed that absolute values of foot temperature, as well as temperature gradient between the patients’ forehead and foot, both can be used as a valuable adjunct for clinical differentiation of immediately threatening ischemia and ALI grades I–IIA Rutherford. Furthermore, study results demonstrated that patients with severe preoperative foot hypothermia caused by ALI have an increased risk of compartment syndrome and revascularization failure.
Practical application of Rutherford classification is relatively straightforward due to its simplicity. However, determination of motor deficit—the most important criterion for discrimination of grades IIA and IIB—requires an experienced examiner and adequate patient cooperation. In real-world clinical practice, the significant proportion of patients with ALI are primarily consulted by a non-vascular specialist, who makes the decision regarding the necessity and urgency of vascular consultation and patient transfer to the vascular service. The information regarding the severity of ALI, transmitted from the primary care provider to the vascular surgeon on-call, can be incomplete, unreliable, or erroneous, which makes the final decision difficult. 6 Moreover, diagnosis of sensorial and motor deficit is impossible in unconscious, confused, agitated, or non-cooperant patients, as well as in patients with neurological consequences of stroke or previous forefoot amputation. Assessment of Doppler signals on the foot arteries increases the precision of ALI diagnosis; however, this method is not universally available and has limited value in differentiation between grades IIA and IIB. Thus, quantitative evaluation of foot poikilothermy using standard medical non-contact thermometer increases the accuracy of clinical examination and, according to the results of present study, can be useful for diagnosis of immediately threatened ischemia, that should be strongly considered in patients with plantar temperature of ≤27.7°C or ∆Tmax F-F value ≥9.5°C.
Quantitative assessment of the foot temperature in patients with peripheral arterial disease is not completely new. Several studies evaluated the utility and reliability of infrared foot thermography (thermometry) for diagnosis of chronic limb ischemia7–11; assessment of the results of revascularization12,13; prediction of healing of plantar ulceration; and freedom from the major amputation. 14 Most authors report the decrease of foot temperature in patients with disturbed tissue perfusion, although the difference between affected limbs and controls is relatively small, ranging between 0.27 and 1.25°C.7,15 In case of ALI, poikilothermy usually is significantly more severe due to the absence/blockade of collaterals, vascular spasm, or extensive length of arterial occlusion. In the present study the median value of temperature gradient ∆Tmax F-F was 10 [7.4–12.5] °C, confirming this well-known fact. Several studies also demonstrated the ability of infrared thermography to determine the severity of chronic lower limb ischemia, based on positive correlation between foot temperature and ABI values.11,16 In the present study, the results of preoperative foot thermometry did not correlate with ABI value, while moderate to strong correlation was found postoperatively. This fact may be explained by the absence of pedal arterial Doppler signals in nearly 90% of the patients with ALI, that precluded the ABI calculation.
Despite significant progresses in vascular medicine, ALI remains to be associated with high rates of mortality and limb loss. 17 Reported rates of major amputation and mortality during index hospitalization are around 10% and 20%, respectively, 18 and the current study offered similar results. Accordingly, the decision to proceed with revascularization or primary amputation is always complex in case of ALI, and any predictors of treatment outcome may help on this. Many studies demonstrated an association between the severity of preoperative ischemia and results of revascularization, the Grade IIB being an independent risk factor in multivariable models.17–19 However, motor and sensorial deficits both are dichotomous categorical variables that cannot be objectively confirmed and measured. Thus, the continuous efforts are done to identify the inexpensive, measurable, and reliable prognostic factors. For example, there is growing evidence confirming the predictive value of neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio in patients with ALI.20–22 We found that severity of foot poikilothermy is also associated with negative treatment outcomes, especially with a risk of limb loss and can be used for prognosis. The area under ROC curve of 0.75 (95% CI 0.61–0.88), constructed for criterion ∆Tmax F-F as a predictor of amputation, is comparable with those of neutrophil-to-lymphocyte ratio (0.71) and platelet-to-lymphocyte ratio (0.77) reported by Pasqui et al. 22 Thus, based on the results of present study and considering universal availability, simplicity, and rapidity of non-contact foot thermometry, we believe that this diagnostic method can augment the clinical examination of the patients with ALI and support the decision-making process.
Several limitations of the present study should be mentioned. Generally, the methodology of foot thermometry (thermography) in patients with vascular diseases is not standardized yet. Authors of previous studies used various approaches: registering of absolute foot temperature in the rest, after walking or limb elevation, calculating the gradient of temperature between affected and healthy lower limb, or gradient between lower and upper limbs.7,10,15 Furthermore, temperature samples were obtained at different points, corresponding to the angiosomal regions of the foot. 10 While this methodology seems appropriate for patients with chronic limb ischemia, it is less relevant in the case of ALI. The poikilothermy in acute cessation of perfusion is significantly more severe and involves the entire foot, making the temperature differences between specific angiosomes less clinically important. In our study, the exact points for temperature sampling were not defined by protocol, that potentially may decrease the accuracy of the measurements. However, we have not found any significant differences between median temperature values registered on dorsal and plantar surface of the foot; both variables strongly correlated with the value of criterion ∆Tmax F-F (r = −0.92 for dorsal and r = −0.97 for plantar temperature). While all three variables demonstrated similar diagnostic and prognostic value, the temperature gradient between forehead and foot hypothetically is less influenced by environmental and whole-body temperature fluctuations. Another potential study limitation is utilization of commercially available infrared thermometers that are not specifically designed for research purposes. Most studies on foot temperature in arterial disease are based on the results of thermography performed using dedicated infrared thermal cameras.7–14 These devices allow comprehensive evaluation of the entire foot surface and identification of anatomic zones with the highest and lowest temperature. At the same time, thermal cameras are rarely available in emergency settings, while low-cost infrared thermometers have proven to be the reliable and valid means to assess local skin temperature. 23
Conclusion
The current study demonstrated that patients with immediately threatening ALI have significantly lower foot temperature than those with viable and marginally threatened limbs. Severe foot poikilothermy at admission is associated with poor outcomes of revascularization, mostly with limb loss. Based on study results, foot thermometry utilizing an infrared non-contact thermometer could be considered a valuable tool for clinical examination of patients with ALI, providing objective data required for more accurate diagnosis, prognosis, and decision-making. Further studies will be needed for the validation of diagnostic and predictive performance of foot thermometry in ALI and its inclusion as a potential component in new prognostic models.
Authors’ note
The preliminary results of foot thermometry in acute limb ischemia were presented as Abstract during the CX Symposium 2021 (19.04.2021, London, UK).
Footnotes
Author contributions
DC and AP researched the literature, planned the study, and elaborated the study protocol. DC, AP, and VC were involved in data acquisition and data analysis. AP and DC performed statistical analysis and wrote the first draft of the manuscript. All authors reviewed, edited, and approved the final version of the manuscript.
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) received no financial support for the research, authorship, and/or publication of this article.
