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Journal of Critical Care 60 (2020) 294–299

Contents lists available at ScienceDirect

Journal of Critical Care

journal homepage: www.journals.elsevier.com/journal-of-critical-care

Core-to-skin temperature gradient measured by thermography predicts


day-8 mortality in septic shock: A prospective observational study
Harry Amson, MD a,b,⁎, Charles-Hervé Vacheron, MD a,b,c, Fabrice Thiolliere, MD a, Vincent Piriou, MD,PhD a,b,
Mathieu Magnin, DVM d, Bernard Allaouchiche, MD, PhD a,b,d
a
Hospices Civils de Lyon, Centre Hospitalier Lyon-Sud, Service de Réanimation, Pierre-Bénite F-69310, France
b
Université Claude Bernard, Lyon1, Villeurbanne, France
c
Service de Biostatistique-Bioinformatique, Pôle Santé Publique, Hospices Civils de Lyon, Lyon, France
d
Pulmonary and Cardiovascular Agression in Sepsis (APCSe), Université de Lyon, VetAgro Sup, Campus Vétérinaire de Lyon, UPSP 2016.A101, F-69280, Marcy l'Étoile, France

a r t i c l e i n f o a b s t r a c t

Available online xxxx Background: Septic shock is associated with altered peripheral perfusion. Core-to-skin temperature gradient de-
pends on skin perfusion and microcirculatory function. We hypothesized that a high core-to-skin temperature
gradient is correlated with mortality in septic shock.
Keywords: Methods: We conducted a prospective observational study including 61 patients at the first 24 h of a septic shock
Sepsis in an intensive care unit. During the 24 first hours after norepinephrine administration, we collected clinical and
Septic shock circulatory characteristics, skin perfusion assessment (Capillary refill time (CRT), Mottling score) and we mea-
Skin temperature sured skin temperature with an infrared thermographic camera. We measured the Core-to-skin temperature gra-
Thermography dient to evaluate if it is a predictor of day-8 mortality.
Peripheral perfusion Results: Day-8 mortality was 16.3%. Core-to-index finger temperature gradient >7 °C was associated with day-8
mortality (OR = 18.0, [3.02–346.14], p = 0.002). This association was still significant after adjustment to the
SOFA (Sequential Organ Failure Assessment) score. A model including a high SOFA score and a core-to index fin-
ger >7 °C was effective to predict day-8 mortality (c-statistic: 0.8735 [0.770–0.976]). Core-to-index finger tem-
perature gradient was correlated with CRT, Mottling Score, and arterial lactate levels.
Conclusions: Core-to-index finger temperature gradient higher than 7 °C predicts day-8 mortality in septic shock
and is correlated with other tissue perfusion markers.
© 2020 Elsevier Inc. All rights reserved.

1. Introduction peripheral perfusion and microvasculatory impairment are associated


with an alteration of tissue oxygenation and organ dysfunction [7].
Sepsis is a life-threatening state caused by abnormal host response Thus, the persistence of such anomalies is associated with mortality
to an infection [1,2]. It is associated with altered peripheral perfusion. [8]. Therefore, the monitoring of peripheral perfusion is interesting in
Septic shock is a frequent cause of admission in intensive care unit order to better understand septic shock and to improve patients' out-
(ICU) with a high mortality of around 38% [3]. The international guide- come. Several methods are used to study peripheral perfusion, including
lines recommend to mainly aim the resuscitation at normalizing the laser Doppler flowmetry [9], near infrared spectroscopy [10], or sublin-
macrocirculatory state and to use the sole arterial lactate levels as a gual microscopy [11]. However, these techniques are expensive and re-
marker of tissue perfusion [2]. However, restoring the macrocirculatory quire experienced physicians. The predominance of the sympathetic
parameters is not always sufficient. In fact, despite hemodynamic stabi- neurohumoral response is at the origin of a reduction of the cutaneous
lization, changes in peripheral perfusion may persist [4-6]. One of the perfusion and therefore of a decrease in temperature [6]. Thus, the
leading research subjects in improving sepsis outcome is the study of study of skin clinical state can be a surrogate to peripheral tissue perfu-
peripheral perfusion and microcirculation. Indeed, during sepsis, altered sion analysis. Skin perfusion can be easily assessed clinically by studying
mottling patterns on the legs, capillary refill time or skin temperature,
which already have been associated with sepsis outcome[12-14].
⁎ Corresponding author at: Centre Hospitalier Lyon Sud, Service d'Anesthésie- The precise measurement of surface temperature without contact
Réanimation, 165 chemin du Grand Revoyet, Pierre-Bénite F-69495, France. can be achieved with infrared thermography (IT). This technique was
E-mail addresses: harry.amson@chu-lyon.fr (H. Amson),
charles-herve.vacheron@chu-lyon.fr (C.-H. Vacheron), fabrice.thiolliere01@chu-lyon.fr
used in studies involving breast cancer and lower limbs arteriopathy
(F. Thiolliere), vincent.piriou@chu-lyon.fr (V. Piriou), mathieu.magnin@vetagro-sup.fr [15]. Thermography allowed detection of peripheral perfusion disorders
(M. Magnin), bernard.allaouchiche@chu-lyon.fr (B. Allaouchiche). following rapid hemodynamic variations in pigs [16]. It was also used to

https://doi.org/10.1016/j.jcrc.2020.08.022
0883-9441/© 2020 Elsevier Inc. All rights reserved.
H. Amson, C.-H. Vacheron, F. Thiolliere et al. Journal of Critical Care 60 (2020) 294–299

assess skin temperature during sepsis in humans [17,18]. In order to Healthcare®) or thermodilution calibrated pulse contour analysis
avoid the influence of ambient temperature, the measure of tempera- (PiCCO, Pulsion medical system®).
ture gradient (TG) between two points seems much more relevant
than a single point temperature measure. 2.4. Data recording
In the present study, we aimed to evaluate whether the core-to-skin
temperature gradients, measured by IT, represent a predictive factor of The following clinical characteristics were collected: age, sex, body
short-term mortality during septic shock. mass index, diabetes, vascular surgery, cirrhosis, solid cancer, hemato-
logic cancer, mechanical ventilation, vasopressor dose, urine output
2. Material & methods and primary site of infection.
The Sepsis-related Organ Failure Assessment (SOFA) score, lactate
2.1. Study setting measurement, and the Simplified Acute Physiology Score (SAPS) II
score were calculated, with the worst values, from the first 24 h since
We conducted a prospective observational study in a 27-bed ICU. All inclusion.
patients were included between June 2018 and June 2019.
Informed oral consent was obtained from all participants or from 2.5. Peripheral perfusion assessment
close relatives when the person was unable to give consent. All patients
and family were informed that anonymous data and pictures would be At the time of the inclusion, two physicians performed an acquisition
used for academic research, and offered the possibility to retract the of capillary refill time (CRT), a mottling assessment, and measure of skin
consent at any time. The study has been also approved by the appropri- temperature in several regions.
ate ethics committee (Comité de Protection des Personnes, SUD-EST IV, The CRT at the knee was measured by applying a firm pressure on
Lyon, France, Ref L15-2013) and has therefore been performed in accor- the dorsomedial aspect of the knee of the patient using the finger of
dance with the ethical standards laid down in the 1964 Declaration of the physician for 15 s. The pressure applied was aimed at removing
Helsinki and its later amendments. the blood at the physician's fingertip (blanching under the nail). The
time of return to the normal color was recorded by a chronometer.
The method and knee location of capillary refill time over the index lo-
2.2. Participants
cation was chosen in this study according to results of a previous study
[13]. This measure was done twice and only the longest time was fur-
We included adult patients (≥18 years) with septic shock admitted
ther analyzed in this study.
to the ICU requiring introduction of vasopressor in the last 24 h. Septic
The mottling pattern was quantified according to the mottling score,
shock was defined, according to the latest international consensus def-
as described in Ait-Oufella et al. [12].
inition as sepsis with persisting hypotension requiring vasopressors to
Core temperature was recorded with a tympanic (Genius 2
maintain a mean arterial pressure (MAP) ≥65 mmHg and having a
Accusystem™) or a urinal probe. The skin temperature of the forearm,
serum lactate level > 2 mmol/L [1].
the index finger, the knee and the hallux were measured by IT. The ther-
Each participant had a follow-up for 8 days. When a patient was
mographic pictures of each limb were performed with an infrared ther-
discharged from the ICU before the 9th day, the life/death status was
mographic camera (Fig. 1). The thermographic camera (FLIR-E4, FLIR
checked and ascertained by all available means.
Systems Inc., Wilsonville, Oregon, USA) presented the following charac-
teristics: detector type, uncooled microbolometer; infrared resolution,
2.3. Hemodynamic management of patients 80*60 pixels; spectral range, 7.5–13 μm; spatial resolution, 10.3 mrad;
field of view (FOV), 55° x 43°; object temperature range, −20 °C to
All patients were managed by local physicians according to local +250 °C; noise equivalent temperature difference, < 150mk; thermal
procedures adapted from international guidelines [2]. Fluid resuscita- sensitivity, < 0.15 °C; accuracy, ± 2%, minimum focus distance, 50 cm.
tion was performed to optimize cardiac output. Then, after optimization The device was calibrated as recommended by the manufacturer. The
of the volemic status, a vasopressor (norepinephrine) was used to pictures were then treated with the software Flirtools® (Flirtools
maintain a MAP above 65 mmHg. software®) to extract the mean temperature of the region of interest
Cardiac output and macrocirculatory monitoring were performed (ROI). For the skin temperature at the forearm, the ROI was placed mid-
by transthoracic echocardiography (Vivid S6, General Electric way between the wrist and the elbow. For the skin temperature at the

Fig. 1. Examples of infrared thermography. Left: leg of patient. Right: forearm of a patient.

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H. Amson, C.-H. Vacheron, F. Thiolliere et al. Journal of Critical Care 60 (2020) 294–299

toe, the ROI was placed at the extremity of the hallux. For the skin tem- 2.7.4. Correlation of the other tissue perfusion variables and TG
perature at the index, the ROI was placed at the last phalanx of the index The three other variables assessing tissue perfusion were compared
finger. For the skin temperature at the knee, the ROI was placed at the between LTG and HTG groups using Fisher tests for qualitative variables
center of the dorsomedial aspect of the knee. The measure was taken and Wilcoxon tests for quantitative variables. Spearman correlation ma-
on both left right sides. Then, the temperature gradient (TG) was calcu- trix was computed in order to visualize the correlation between each
lated by subtracting the skin temperature to the core temperature. Only variable. Semi-quantitative p values were estimated.
the highest gradient between the left and right sides was further A p-value lower than 0.05 was considered as statistically significant.
analyzed. All analyses were performed with R software (version 3.4.3) [20].

2.6. Endpoints 3. Results

The primary endpoint was to determine if the core-to-skin TG was 3.1. Studied population
associated with day-8 mortality.
The secondary endpoints were to determine a clinically relevant cut- Between June 2018 to June 2019, 64 patients were included in our
off of the TG and to determine the correlation between TG and other hy- data collection. Three patients were excluded because of lack or loss of
poperfusion parameters (CRT, Mottling score, and arterial lactate level). information leaving 61 patients for this study. Baseline characteristics
are given in Table 1. Overall day-8 mortality rate was 16.3%. The median
2.7. Statistical analysis time between introduction of vasopressor and inclusion was 13 [6-23]
hours.
Based on extrapolation of previous work [19] associated with the The primary infection sites were the abdomen (52%), the lungs
clinician's experience, we hypothesized that a temperature gradient dif- (26%) and the urinary tracts (7%). The highest dose of norepinephrine
ference of 3 °C (standard deviation of 4 °C) will exist between the survi- on the first day was 0.41 [0.22–0.95] μg/kg/min. The urinary output of
vor and non-survivor with a 8th day mortality of 20%. The sample size of the first 24 h was 0.68 [0.24–1.15] ml/kg/h. Forty patients (66%) had
this study was calculated through 10,000 simulations of repeated logis- mechanical ventilation during the first day. The SOFA score was 12
tic regression. A sample size of 54 patients was needed for a type I error [10-14] and the SAPS II score was 71 [63–82].
of 5% and type II error of 20%. We included ten more patients for safety
reasons, reaching a total of 64 patients. 3.2. Comparison of the gradient sites
Descriptive statistics were expressed by median associated with
their interquartile range (median [IQR25-IQR75]) for quantitative vari- The site of skin temperature measurement found to yield the best
ables and number of patients associated with their percentage for qual- correlation with mortality was the core-to-index temperature gradient
itative variables (n (%)). Comparisons between survivors and non- (AIC of 51.3 versus 55.9, 56.5, 57.1 respectively for toe, knee and arm
survivors were performed using the Wilcoxon rank test for quantitative sites). Furthermore, the scaled core-to-Index temperature gradient
variables and Spearman chi-squared test for qualitative variables. was found to be associated with day-8 mortality (OR: 1.35 [1.07–1.82]
p = 0.0213).
2.7.1. Comparison of gradient sites
The association between each temperature gradient and the day-8 3.3. Cut-off estimation
mortality was modelized through logistic regressions: day-8 mortality
was used as the dependent variable and the different TGs were used With the minimum p-value approach, the best cut-point of the core-
in turn as independent variables. For each regression, the Akaike Infor- to-index temperature gradient was 7.1 °C, which we rounded to 7 °C.
mation Criterion (AIC) was computed. The variable that minimizes the
loss of information was identified as the one associated with the lowest
AIC. Odds ratio of the gradient associated with their respective 95% con-
Table 1
fidence interval and p-value (OR [95%CI] p) were estimated. Clinical and demographic characteristics of the patients.

Characteristics n = 61
2.7.2. Cut-off estimation
In order to select the best cut-off, the minimum p-value approach Age, in years 68 [60–80]
was used. For clinical reasons, the selected cut-off was rounded to the Sex, Female, n (%) 27 (44%)
Body Mass Index (kg/m2) 24.3 [21.3–27.7]
nearest integer. The sensitivity (Se), specificity (Sp), predictive positive Time between introduction of vasopressor and inclusion, hours 13 [6–23]
value (PPV) and predictive negative value (PNV) of the selected cut-off Comorbidities, n (%)
were computed. Solid malignancies 24 (39%)
This was used to define two groups, the Low Temperature Gradient Hematologic malignancies 11 (18%)
Diabetes 9 (15%)
(LTG) and High Temperature Gradient (HTG) groups.
Cirrhosis 2 (3%)
Vascular surgery 1 (2%)
2.7.3. Relationship between TG groups and mortality Primary site of infection, n (%)
For these groups, three logistic regressions were modeled. First, a Abdomen 32 (52%)
univariate logistic regression on the group of gradients on the mortality Lung 16 (26%)
Urinary tract 7 (11%)
on the 8th day. Second, an Inverse Probability Weighting (IPW) analysis
Soft tissue 4 (6%)
was applied to each observation in order to account for the main poten- Other or unknown 3 (5%)
tial confounding factors. A propensity score (PS) was estimated for Day 1 severity
these factors (sex, age, height, weight, MAP and norepinephrine infu- SOFA score 12 [10–14]
SAPS II 1 71 [53–82]
sion rate at the time of the temperature measurement). Logistic regres-
Urinary output at H24, mL/kg/min 0.68 [0.24–1.15]
sion was computed by weighting each patient according to their PS (1/ Norepinephrine dose, μg/kg/min 0.41 [0.22–0.95]
PS for the HTG group and 1/(1-PS) for the LTG group). Results are Mechanical ventilation, n (%) 40 (66%)
expressed with OR [IC95%] and their respective p-values. In order to Values are either mean ± SD, median [25th quartile-75th quartile] or number of patients
represent the discrimination of this final model, c-statistic associated (percentage) - SOFA: sequential organ failure assessment - SAPS II: Simplified Acute Phys-
with their 95% confidence interval was estimated (Delong method). iology Score.

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H. Amson, C.-H. Vacheron, F. Thiolliere et al. Journal of Critical Care 60 (2020) 294–299

Table 2 The correlation between these parameters ranged from −0.01 to


Relationship between core-to-index temperature gradient higher than 7.1 °C and day-8 0.53 (Table 4).
mortality.

Odds Ratio Confidence interval 95% p-value 4. Discussion


Univariate analysis 18.00 [3.02–346.14] 0.002
IPW analysis 13.76 [3.40–108.81] 0.002 The current study aimed to assess the prognostic potential of core-
Multivariate Analysis
to-skin temperature gradients, measured with the use of IT, during sep-
HTG group 41.44 [7.06–509.94] <0.001
HTG + SOFA Score 4.26 [2.06–10.77] <0.001 tic shock. The main result was the association between core-to-index
temperature gradient and day-8-mortality. Secondary results were the
IPW analysis: Inverse Probability Weighting analysis, which takes into consideration the
main cofounding factors (Sex, Age, Height, Weight, Mean Arterial Pressure and norepi- correlations between this temperature gradient and other hypoperfu-
nephrine infusion rate at the time of the temperature measurement). HTG: High temper- sion parameters such as arterial lactate, CRT and Mottling score.
ature gradient. SOFA: Sepsis-related Organ Failure Assessment. The patients included in the present study all had a septic shock ac-
cording to the Sepsis-3 definition [1]. This choice implies that all pa-
tients had organ dysfunction, and therefore patients with less severe
Core-to-index temperature gradient higher than 7 °C predicted day-8 sepsis were not included in this study, contrary to other studies evaluat-
mortality with a sensitivity of 90% and a specificity of 66%. PPV and ing the association between skin hypoperfusion signs and mortality[12-
PNV were respectively 35% and 97%. 14,21]. Results similar to ours may not be found in less severe patients.
In fact, in a study carried out on 103 patients, the temperature gradients
3.4. Relationship between TG groups and mortality were higher in the most severe patients[14]. In the present study only
two patients had cirrhosis and one had vascular disease which are
The HTG group (Gradient >7 °C) was associated with day-8 mortal- known also to alter skin perfusion [22]. We chose to use an early mortal-
ity OR = 18.0 [3.02–346.14] p = 0.002. This association was also signif- ity judgment criterion (day-8 mortality) because later mortality (day-
icant after weighting the patient and the adjustment with the SOFA 14, day 28) would have been influenced by several other factors such
score (Table 2). as comorbidities or ICU-acquired infection and complications, not solely
The model including the group of HTG and the SOFA score had explained by the severity of the initial acute circulatory failure.
strong discriminative characteristics (c-statistic: 0.8735 [0.770–0.976]; Skin evaluation for peripheral tissue perfusion assessment is a reli-
Fig. 2). able method in the early stage of acute circulatory failure and it can in-
form the severity of the clinical state. Skin temperature evaluation in
3.5. Correlation between the TG and tissue perfusion parameters circulatory failure started in 1969, with the study of Joly et al. who
found that cold big toe was associated to the severity of the shock
The HTG group was associated with other peripheral perfusion pa- [23]. In 2001, Kaplan et al. showed that patients with cool extremities
rameters: patients had significantly higher arterial lactate level (p = had higher lactate levels in ICU [24]. In 2009, Lima et al. found that sub-
0.015), knee-CRT (p = 0.043) and Mottling score (p = 0.004) (Table 3). jective assessment of peripheral perfusion (including CRT, and cool

Fig. 2. Receiver operating characteristic of the model high temperature gradient and high SOFA score.

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H. Amson, C.-H. Vacheron, F. Thiolliere et al. Journal of Critical Care 60 (2020) 294–299

Table 3 gradient higher than 7 °C predicted day-8 mortality for ICU patients
Comparisons of hypoperfusion parameters between patients with low-temperature gradi- with septic shock independently from the SOFA score. We also found
ent and patients with high-temperature gradient.
that a model, including a high SOFA score and a core-to-index temper-
LTG group HTG group p-value ature gradient higher than 7 °C, was effective in order to predict day-8
Arterial Lactate levels (mmol/L) 3.6 [2.6–6.2] 5.4 [3.5–8.1] 0.015 mortality (c-statistic: 0.8735 [0.770–0.976]). This result suggests that
Knee-CRT 3.8 [3.0–5.2] 4.7 [3.7–6.6] 0.043 peripheral perfusion assessment gives another aspect of severity in sep-
Mottling score 0.004 tic shock that is not explored in the SOFA score parameters. Indeed, the
0–1 29 (48%) 13 (21%)
increase in the temperature gradient reflects an abnormality in the pe-
2–3 4 (7%) 12 (20%)
4–5 2 (3%) 1 (2%) ripheral perfusion which is not considered in the calculation of the SOFA
score: the “cardiovascular” part of this score is concerned with blood
Values are presented with median [25th quartile-75th quartile] -LTG: Low-Temperature
gradient, HTG: high-temperature gradient, CRT: Capillary refill time.
pressure, and therefore corresponds to a macrocirculatory approach. In-
terestingly, a gradient between 3 and 7 °C was reported as correspond-
ing to a stable state [6]. This suggests that IT gives results consistent with
other temperature measurement techniques. This underlines the practi-
Table 4 cal interest of thermography: it allows the temperature to be measured
Matrix of correlation of the different peripheral perfusion parameters. without contact, unlike other thermometers which require prolonged
Core-to-Index TG Lactate Level CRT Mottling score contact and sometimes stay in place for several hours. Restricting the
devices to patient contact is not without interest since it can reduce
Core-to-Index TG 1 0.38** 0.36** 0.33**
Lactate Level 0.38** 1 −0.01 0.27* the risk of nosocomial infection in patients with septic shock, who are
CRT 0.36** −0.01 1 0.53*** predisposed to it [29].
Mottling score 0.33** 0.27* 0.53*** 1 We found significant correlations between the core-to-index tem-
TG: Temperature Gradient – CRT: Capillary Refill Time. perature gradient and other tissue perfusion markers such as the arte-
*: P < 0.05, **P < 0.01, ***P < 0.001. rial lactate levels, the CRT and the Mottling score. A correlation
between peripheral perfusion markers and the arterial lactate levels
has already been shown [12-14,24,25]. However, in our study, the cor-
extremities) was associated with more severe organ dysfunction and relation between TG and arterial lactate levels were weak, suggesting
higher lactate levels for ICU patients [25]. Later, Ait-Oufella et al. studied that the TG captures another aspect of peripheral perfusion disorder.
peripheral perfusion markers in sepsis. They have found that Mottling Unexpectedly, the correlations between the different skin perfusion as-
score [12], CRT [13] and toe-to-room temperature gradient [14] were sessments were weak. This may show the complexity of microcircula-
associated with mortality in sepsis. More recently, Dumas et al. have tion processes. For instance, TRC, Mottling and skin temperature may
demonstrated that the mottling score was associated with early mortal- explore different aspects of peripheral perfusion alterations.
ity, independently from the vasopressor doses [21]. Moreover, core-to- It should be taking into consideration that the CRT and the mottling
peripheral temperature gradient has been analyzed in two reviews score are difficult to measure in the case of patients with dark skin. In
[26,27]. In Brigitte et al. review, the conclusion was a lack of evidence previous studies this was even considered as an exclusion criterion
that skin temperature could be a marker of hypoperfusion due to the [12,13]. The skin gradient temperature can be objectively assessed
paucity of actual evidence [26]. In Schey et al. review which included with IT to all patients whatever their skin color because the emissivity
twenty six studies examining skin temperature as a marker of hemody- of human skin is very high and is not dependent on its color [30].
namic status mainly after cardiac surgery, they also conclude in a lack of This study has several limitations. Firstly, the trial was performed in
evidence and a need for more prospective studies [27]. a single ICU center. Only two physicians performed the inclusions and
In the present study, we evaluate skin temperature with IT. To our the measures. The reproducibility of the temperature gradient as a prog-
knowledge, it is the first time that this technology is used to evaluate pe- nosis marker should therefore be further assessed. Secondly, the mea-
ripheral perfusion in a prospective study in adults. IT was chosen be- sures of the skin perfusion, lactate, and the infrared pictures were
cause encouraging results were already published in an experimental taken within the first 24 h of the shock with a median time of 13 [6-
pig model: IT seemed capable of detecting peripheral perfusion disor- 23] hours. There is therefore a heterogeneity in the time of inclusion:
ders secondary to hemodynamic variations [16]. Moreover, two studies some of the patients were treated for a few hours and the severity of
carried out on children also reported its use in the detection of shock the shock could have been amended. This could also explain the lack
[28]. Thus, the use of the thermographic infrared technology proved to of correlation between lactate level and CRT. Thirdly the assessment of
be an adequate approach as it provides a reliable, contact free, easy to the core temperature was performed using urinal probe, or if not avail-
record and inexpensive way to measure skin temperature. able by tympanic way, which might be slightly different from core tem-
In the current study, core-to-index finger appeared the best gradient perature. We conducted an observational pragmatic study and
to predict mortality compared to core-to-toe, core-to-knee or core-to- therefore, we did not choose to change the way the temperature was
forearm. However, the difference between these gradients seems to be monitored. Fourthly, the number of subjects was insufficient to make
small, given the small difference between the AICs. To our knowledge, an adjustment with norepinephrine infusion rate. Therefore, we made
it is the first time that core-to-index finger gradient was successfully an Inverse Probability Weighting analysis, which is not as robust a
studied. The most studied core-to-skin gradient is the core-to-toe gradi- method. Nevertheless, we cannot conclude on the independence be-
ent [14,23]. This gradient was also evaluated in our study, but it was tween TG and vasopressor infusion as Dumas et al. have found for the
computed differently from previous studies. Indeed, the toe tempera- mottling score [21].
ture in our study was measured on the dorsal side and not on the ventral In the future, it would be relevant to assess the evolution of TG
side, as in the historical study of Joly et al [23]. However, both core-to- throughout the resuscitation time. Furthermore, a resuscitation proce-
index and core-to-toe gradients seem to yield concordant results: in dure guided by TG could help to manage patients with septic shock
our study, the core-to-index finger gradient was associated with mor- and abnormal peripheral perfusion as described in the case of CRT [31].
tality, as previously found with the core-to-toe gradient [14]. The current study provides new insights concerning the use of IT to
A threshold of 7 °C of the core-to-index temperature gradient seems detect peripheral perfusion abnormalities in septic shock patients. The
clinically relevant in order to discriminate the severity for patients with current prospective observational study documented that thermo-
septic shock and could be easily used routinely at the bedside of the pa- graphic imaging provides an objective, easy to perform, contact free
tients. Indeed, we found that a core-to-index finger temperature and inexpensive method to measure skin temperature of the

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extremities. We further showed that the core-to-index temperature [13] Ait-Oufella H, Bige N, Boelle PY, Pichereau C, Alves M, Bertinchamp R, et al. Capillary
refill time exploration during septic shock. Intensive Care Med 2014;40:958–64.
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and that it was correlated with other hypoperfusion parameters. [14] Bourcier S, Pichereau C, Boelle P-Y, et al. Toe-to-room temperature gradient corre-
lates with tissue perfusion and predicts outcome in selected critically ill patients
with severe infections. Ann Intensive Care 2016;6(1):63.
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10.1016/j.infrared.2012.03.007.
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On behalf of all authors, the corresponding author states that there is thermography to detect earlyalterations of peripheral perfusion -evaluation in a por-
no conflict of interest. cine model. Biomed Opt Express 2020. https://doi.org/10.1364/BOE.387481.
[17] Ortiz-Dosal A, Kolosovas-Machuca ES, Rivera-Vega R, Simón J, González FJ. Use of in-
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