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Burn depths evaluation based on active dynamic IR thermal imaging—A preliminary study
Burns 32 (2006) 867–875 www.elsevier.com/locate/burns
Burn depths evaluation based on active dynamic IR thermal imaging—A preliminary study Alicja Renkielska a,*, Antoni Nowakowski b, Mariusz Kaczmarek b, Jacek Ruminski b a b
Department of Plastic Surgery and Burns, Medical University of Gdansk, Gdansk, Poland Department of Biomedical Engineering, Gdansk University of Technology, Gdansk, Poland Accepted 31 January 2006
Abstract Proper diagnostic assessment of burn wound depth is of the highest importance in selecting the mode of burn wound treatment. Several diagnostic methods – clinical and histopathological evaluation, as well as methods employing IR imaging – static thermography and active dynamic thermography (ADT) – are compared on the basis of in vivo experiments conducted on three domestic pigs (23 burn wounds). ADT is presented here as a new, reliable and quantitative method of assessing burn wound depth on the basis of discrimination of the thermal properties of burnt tissue. In the case of ADT registration of thermal images was performed following thermal pulse excitation. A series of captured infrared images was used as the basis for calculating the thermal time constant t for each pixel. The parameter values were compared with histopathological and clinical assessments of burn depth. The mean value of t was found for burns, which heal within 3 weeks (t = 12.08 1.94 s) and for burns, which did not heal during this period (t = 9.07 0.68 s), p < 0.05. The accuracy, sensitivity and specificity of all the methods tested were compared, the best results coming from ADT. The ADT method is fast, non-invasive and relatively inexpensive, although it still requires further animal experimentation as well as clinical study to confirm the results. # 2006 Elsevier Ltd and ISBI. All rights reserved. Keywords: Active dynamic IR thermal imaging; Burn depth; Diagnosis
1. Introduction The modern approach to skin burn depth assessment tries to resolve the problem of healing and the appropriate choice of treatment—conservative or surgical [1,2]. The traditional approach distinguishes the following grades of burn wound: I, superficial; IIa, superficial dermal; IIb, deep dermal; and III, full thickness of the skin [3]. In clinical practice even the inexperienced doctor has no difficulty in classifying first and third degree burns correctly. However, differentiation between the IIa (superficial dermal) and IIb (deep dermal) classes of wound is problematic. Clinical evaluation, mainly * Corresponding author at: Department Plastic Surgery and Burns, Medical University of Gdansk, ul. Debinki 7, 80 211 Gdansk, Poland. Tel.: +48 583 492 405; fax: +48 583 492 450. E-mail addresses: [email protected] (A. Renkielska), [email protected] (M. Kaczmarek), [email protected] (J. Ruminski). 0305-4179/$30.00 # 2006 Elsevier Ltd and ISBI. All rights reserved. doi:10.1016/j.burns.2006.01.024
based on visual inspection, only insures an accurate prognosis in 50–70% of these cases [2–5]. A method that enables burn wound depth to be correctly assessed and the choice of treatment to be made properly is, therefore, of the greatest importance. The aim of this paper is to present one such new objective method. The method based on IR thermal imaging of transient processes allows quantitative evaluation of burn depth and provides the answer to one of the most important questions in burn diagnostics: Will the burn heal spontaneously within 3 weeks of the burn or not? The reference method in burn depth evaluation is histopathological assessment but as this is invasive, local and time consuming, it is not frequently used [6,7]. Research interests have concentrated on the search for non-invasive, objective and quantitative diagnostic methods. Static thermography (ST) [8–10], ultrasonography (USG) [11,12], spectrophotometry [13,14], laser Doppler imaging (LDI) [15–18] and indocyanine green fluorescence (ICG) [19,20] are
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those most frequently cited, although none has been broadly accepted as a solution for clinical applications [2,5]. Recently we discussed the diagnostic value of ST [21], where the basic figure of merit—DT, namely the difference between the mean values of skin temperature for the burn wound area and the unaffected reference skin area, is defined. The inconveniences of the method are the need for meticulous care about measurement conditions and the lack of commonly accepted temperature ranges of DT for particular burn wound depth classifications. However, a great advantage of the method is its non-invasive character, the possibility of assessing relatively large burn areas and the easy and objective capture of images for medical documentation [22,23]. We propose an IR thermal imaging modality new to medical diagnostic applications, active dynamic IR thermal imaging (ADT), also termed active dynamic thermography. This is a method based on infrared detection which uses the cameras already applied in static thermography but which shows thermal tissue properties instead of changes in temperature distribution. Such an approach eliminates several of the drawbacks of traditional thermography while preserving the positive features and allowing quantitative objective assessment of burns.
be regarded as an advanced version of IR/NDT. Analysis of heat transfer enables thermophysical material properties, such as thermal diffusivity or conductivity, to be quantified. Knowledge of these two thermal parameters allows the subsurface structure to be determined. The general concept of the measurements performed in ADT is shown in Fig. 1. First the steady state temperature distribution on the tested surface is recorded using an IR camera. Next external thermal excitation (in our experiments heating by optical irradiation) is applied, followed by measurements of temperature transients on the tested surface. Typically, a set of halogen lamps may be applied as the thermal excitation source. Finally, burned skin can be quantitatively assessed by means of the thermal time constant (t). The data acquisition process is illustrated in Fig. 2. The example shows tracing of temperature in a specific pixel position x, y, taken during and after a thermal pulse excitation. Measurement of temperature is performed here only during the recovery phase (in this case the cooling phase, following the heating). Thermal transients are described by exponential functions. For one-directional heat flow the simplest description of surface temperature changes may be given for the cooling phase as shown in Fig. 2(A) by:
2. Materials and methods 2.1. Active dynamic IR thermal imaging (ADT)
t TðtÞ ¼ T 0 þ DT exp t
The concept of infrared non-destructive testing (IR/NDT) has been known in industry for several years [24]. ADT may
where T(t) is the pixel temperature T in time t, T0 the temperature before excitation, DT is the temperature rise
Fig. 1. Schematic diagram of the ADT instrumentation—the IR camera synchronised with an excitation source (in the experiment described this was a set of halogen lamps) allows the surface temperature of the object under examination (the animal or the patient) to be recorded at a speed of 30 frames/s. Changes in this temperature are caused by the external heating and are dependent on the internal structure of the object tested.
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Fig. 3. Positioning of the burned areas on the back of a pig. Symmetrical wounds for reference histopathological examination and for thermographic observation are indicated.
Fig. 2. Measurement procedure (A) course of temperature at the pixel x, y in time; tb/e moments at which the heating source is switched on (beginning) and off (end), respectively, t30 time of termination of the recording; (B) thermograms showing temperature distribution at the surface of the object (the skin) recorded in time; the temperature scale is attached for easy interpretation of the picture.
as a result of excitation. The value of the thermal time constant t depends on different existing mechanisms of heat flow and is strongly correlated to the physical structure of the burns. In our case the temperature of each pixel is captured to calculate the thermal time constant specific to each pixel (correlated with the burn depth). The parametric image of the time constants then enables the tested surface to be visualised thanks to the high degree of correlation with the depth of the burn wound. The value of any new diagnostic method should be carefully tested in objective fully controlled experiments. In our case this is the crucial role of in vivo experiments on pigs. The experiment was conducted on young domestic pigs, each weighing approximately 20 kg. The Local Ethics Commission for Experimentation on Animals at the Medical University of Gdansk, Poland approved the plan for the experiment. The reason for the choice of the pig as an experimental animal was the high degree of functional and structural similarity of pig skin to human skin [25]. The animals were subjected to reference burns of different depths by adopting Singer’s procedure [7] already applied in our earlier ST experiment [21]. Anaesthesia and analgesia were obtained by the administration of ketamine (im), pentobarbital (iv) and fentanyl (iv) at doses of 20, 30– 50 and 0.5–0.1 mg/kg, respectively. Each pig was usually subjected to eight pairs of symmetrical wounds covering approximately 1.5% of its total body surface area, in exactly the same manner as in our recent work (Fig. 3) [21]. One wound in each pair was for thermography (testing by ADT),
while the symmetrical (contralateral) wound was for taking biopsies for histopathological examination. The wounds were inflicted by an aluminium rod with dimensions of 2.5 cm 2.5 cm 7.5 cm and a weight of 150 g, which was applied to the skin at a controlled temperature of 80 8C in the designated areas for 5, 15 and 25 s, respectively and at 90 8C for 60 s. This resulted in burn wounds of the following depths, expressed as the relative thickness of the skin, a percentage of the dermis thickness at the measurement site (dtms), as shown in Fig. 3:
1 2 3 4
and and and and
5: 6: 7: 8:
11.92 2.98% 21.58 3.22% 47.8 18.16% 67.3 14.65%
dtms; dtms; dtms; dtms.
As we have also recently described, the animals breathed spontaneously during the course of the experiment and were given fentanyl at a dose of 0.5–0.1 mg/kg following the invasive phase (the infliction of burns and the securing of specimens for histopathological examination). In the subsequent follow-up period there was no need to keep the animals on this agent. The general condition of the animals was good, they were fed in a natural way and their daily gain in body weight was up to 0.5 kg. To prevent any external influence on the healing of burn wounds no medicaments with a general therapeutic action were administered. In the course of healing the burn wounds were left open, without dressings or topical agents [21]. However, several wounds were excluded from the measurements because of accidental mechanical damage to the animals’ skin caused by abrasion against the walls of the cages. To prevent the interaction of different thermal phenomena arising from different kinds of wound (burn, biopsy and abrasion) we excluded all the mechanically damaged wounds from the material investigated by the ADT procedure. This dramatically lowered the total number of wounds analysed. Finally, 23 wounds were subjected to the analysis presented here.
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Specimens for bacterial culture were collected from the skin before infliction of the burns and from the skin and wounds at 1, 3 and 7 days after burning. The solution of the problem of evaporation water loss (ewl) reported by Anselmo and Zawacki [26] and Cole et al. [27] has also been described by us [21]. The epithelium was almost totally destroyed and thus all the wounds were equally devoid of the insulation layer, a factor which might have been responsible for the differences in evaporation water loss (ewl) and, therefore, of some influence upon the surface temperature of the wound [26]. No agents in the form of either gels or protective membrane were used to prevent evaporation from the wound [27,28]. Clinical evaluation of burn depth was performed 24 h after the wounds were inflicted, using traditional observational criteria [3,4], on the basis of agreement between two plastic surgeons experienced in burn treatment. The same surgeons made an assessment of the healing result 3 weeks later, classifying the wounds as ‘‘healed’’ or ‘‘not healed’’. Burn wound depth was assessed following the Singer method [7] by histopathological determination of the depth of damage to the following skin elements: hair follicle (epithelial cells), connective tissue collagen (a change in collagen staining), nerves and smooth muscles (mesenchymal cells) and blood vessels (endothelial cells). The depth was measured in millimetres, starting from the epithelium basal layer. Histopathological results were given as a percentage of the dermis thickness at the measurement site (dtms). The ADT examination was conducted over the three consecutive days following infliction of the burn wound. All the conditions required as the ‘‘gold standard’’ for static thermographic examination were also met [21]. The thermographic IR camera AGEMA THV-900 SW/TE of 0.1 8C resolution was used for recording thermal images. The camera was placed at a distance of 0.75 m from the pig’s back in the plane perpendicular to it. The parameters applied for burn wound depth evaluation with a view to the choice of treatment, namely static thermography (DT) and active dynamic thermography (t), were calculated for the three consecutive post-burn days. The observation area dependent on the camera field of view (FOV) was typically 20 cm 15 cm. The ADT experiment was performed with pulse optical excitation lasting 15 s and resulting in a surface temperature rise of 2.5 8C, followed by a 30-s recording of the self-cooling phase. The excitation was performed using a set of halogen lamps of 1000 W and equipped with a mechanical shutter for prompt switching on and off of the power pulse. One exponent approximation (model of the thermal equivalent structure) was applied to determine the time constant t. The full diagnosis takes several minutes using automatic calculation procedures. The same recording procedure was applied in the clinical cases to illustrate the application of the method in hospital practice. For three post-burn days the measurements of DT and t did not differ significantly for either group. The Day 2 values were, therefore, taken for analysis, since they are useful from
a clinical point of view. At this stage a hospitalised patient’s status is usually stable and this is a good time to reach a decision concerning surgery [29]. For the purpose of classifying the burn wounds into those healing within 3 weeks (requiring conservative treatment) and ‘‘non-healing’’ (needing surgery) the results were subjected to statistical analysis. This was performed by means of the variance analysis ANOVA and by comparing the average post hoc values with Tukey’s RIR-test [30]. To determine the properties of the methods of burn wound assessment quantitatively the accuracy, sensitivity, and specificity have been calculated as: Accuracy: the ratio of the sum of true positive cases and true negative cases to the total number of cases; Sensitivity: the ratio of the number of true positive cases to the number of true positive cases plus the number of true negative cases; Specificity: the ratio of the number of true negative cases to the number of true negative cases plus the number of false positive cases.
3. Results Groups of wounds were distinguished post hoc: those shallower than 60% of the dtms, which healed within 3 weeks (18 cases); and those deeper than 60% of the dtms, unhealed (five cases) (Fig. 4). For ADT the mean value of the thermal time constant for burns shallower than 60% of the dtms (those healing within 3 weeks) was t = 12.08 1.94 s and for deeper ones (‘‘nonhealing’’) it was t = 9.07 0.68 s. The difference was at the statistically significant level, ( p < 0.05). We found that parameter t had a higher value (was longer) for wounds, which self-healed within 3 weeks than for the unaffected skin, while t had a lower value (was shorter) for deeper burns that failed to heal within this period. The discrimination threshold was calculated as t = 10.125 s (Fig. 4). When this value was used for burn discrimination, the accuracy, sensitivity, and specificity were all 100%.
Fig. 4. Thermal time constants t of burn wounds classified as ‘‘healed’’ and ‘‘non-healed’’ within 3 weeks. The threshold value is t = 10.125 s.
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In all three parameters, the accuracy, sensitivity and specificity of the histopathological evaluation, were also 100%. For the clinical method accuracy was 60.9%, sensitivity 50% and specificity 100%. When static thermography was used the value DT = 0.3 8C was assumed as the classification threshold. With this value the accuracy, sensitivity, and specificity were 91.3%, 94.4% and 80.0%, respectively.
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An example of skin burns inflicted on a pig is shown in Fig. 5. Of the following images photograph (A) was taken on post-burn Day 2 and (D) on post-burn Day 21, (B) shows static thermography on post-burn Day 2, and (C) a parametric image of the thermal time constant on postburn Day 2. The ADT method has already been adopted for clinical use. As an example, a burn wound on the right thigh of one patient is shown in Fig. 6 and burns on both thighs and buttocks of another patient are shown in Fig. 7. The results of the thermographic investigations had no influence on the choice of burn treatment. With regard to Fig. 7, tangential excision of necrotic tissue was performed according to the clinical evaluation of areas marked 2 and 3 (IIa/IIb and IIb/III, respectively). From photograph (A1) it may be suspected that the shallower burnt areas of the right thigh (2 in the clinical and ADT images) have been damaged. These areas would probably have healed spontaneously within 3 weeks of burn infliction. The static thermogram of the wounds to both thighs should be interpreted as prognostically misleading; the cold areas of both lateral aspects of the thighs (3) healed. The warmer parts (31), the ‘‘warm islands’’, are difficult to interpret. They are localised like the ‘‘short t’’ areas on the ADT image and unhealed parts of the wounds on post-burn Day 18. In contrast, the prognosis based on the ADT results would allow for the proper choice of treatment: surgery reduced to the medial and posterior surfaces of both thighs (3 in the clinical image and area 3 ‘‘short t’’ in ADT). In bacteriological cultures only normal and transient flora were found and no clinical symptoms of wound infection were observed.
4. Discussion Fig. 5. Photographic and corresponding thermographic images of experimental burn wounds on a pig—no. 5–IIa, dermis thickness at the measurement site (dtms): 10.1%, prognosis: will be healed, result: healed; no. 6–IIb, dtms: 24%, prognosis: will not be healed, result: healed; no. 7–IIb, dtms: 41%, prognosis: will not be healed, result: healed; no. 8–IIb, dtms: 54.2%, prognosis: will not be healed, result: healed. (A) Photograph taken on postburn Day 2. Clinical assessment suggests no healing of the wounds nos. 6, 7 and 8 within 3 weeks; the treatment decision would be surgery. Comparison of this clinical prognosis with the healing result (three false negative cases and only one true positive) indicates the low diagnostic value of the clinical method in cases evaluated as deep dermal (IIb). (B) Static thermography (ST) image on post-burn Day 2. DT of wounds nos. 5, 6 and 7 was greater than the threshold value DT = 0.3 8C. The prognosis based on ST would be—will be healed within 3 weeks of burn. DT of the burn wound no. 8 was 0.02 8C (smaller than the threshold value) and the prognosis would be—will not be healed (false-negative case). Thus static thermography would help in two out of three cases falsely evaluated by the clinical method. (C) Parametric image t on post-burn Day 2. This image is relatively uniform and burn wound borders are almost indistinguishable. However, t values of all wounds are larger (longer) than the threshold value t = 10.125 s and, according to this threshold value of t, the decision based on ADT investigation would be to maintain a conservative treatment of all wounds as all should heal (and in fact they did heal). This confirms the extremely high diagnostic value of ADT. (D) Photograph taken on post-burn Day 21. All four presented here wounds have healed.
We started working on model-based ADT applications in medical diagnostics in 1999 [31] and since then have published further data on the procedures applied to burn evaluation, for example in 2001 [32,33]. Prior to these publications thermography was applied in burn depth assessment only in the traditional static form, listing only the most important positions [8–10,22,34–36]. Only Dickey et al. [37] made the attempt to propose an in vitro burn model using biosynthetic skin dressing and dynamic thermography measurement. Apart from our results, no in vivo experiments or clinical cases have been presented at any time. The depth of experimental burn wounds has been evaluated by means of four diagnostic methods: clinical observation, traditional thermography (ST), ADT and histopathology (as the reference). In our experiment, the accuracy of the clinical method with respect to choice of the mode of treatment was only 60.9%, which is comparable to results given elsewhere by the authors of clinical papers [2,5] and which would seem to be unsatisfactory. The high degree of specificity of the method (100%) might be the
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Fig. 6. Photographic and corresponding thermographic images of a burn wound to the posterior surface of the right thigh of a 49-year-old patient: (A) Clinical burn depth evaluation of the area marked: 1–IIa superficial dermal, 2–IIa superficial dermal and, more centrally, IIb deep dermal, 3–IIb deep dermal and, in the lower part, III full thickness (B) Static thermography (the extremity is slightly medially rotated in comparison to the photograph). Areas 2 and 3 are the coldest and are without marked internal differentiation. (C) Active dynamic thermography parametric image (rotation of the extremity as above). The areas with short thermal time constants t and which qualified for surgery are well defined. These areas are markedly smaller when compared with areas 2 and 3 in the photograph and in the static thermogram.
result of a tendency by doctors to overestimate burn depth. This observation has already been discussed in the literature [17,18]. Taking into account the small number of accurate prognoses with regard to the classification ‘‘wound healing within 3 weeks’’, this clinical method, based on visual inspection (sometimes additionally supported by the ‘‘pinprick test’’ [38]), should be replaced or at least supported by another more objective and quantitative method. In the histopathological assessment of burns the accuracy, sensitivity and specificity of the method in our experiment was 100%. This result confirms the high diagnostic value of the method and its position as the reference for evaluation of other newly established methods in the assessment of burn depth [6,7,34]. However, its invasive character, the necessity of multiple burn wound biopsies and a delay of several days while waiting for the result markedly restricts the usefulness of this method in everyday hospital practice. Static thermography as tested in our study has already been in practical use in burn diagnostics for many years. However, the disadvantages of this method, mentioned in the introduction [21–23], limit its popularity. In our studies the quality parameters: accuracy 91.3%, sensitivity 94.4%, and specificity 80%, show its usefulness as an adjunct method in burn wound depth assessment and confirm the conclusions drawn from clinical tests [8–10,22,23,34–36]. When reflecting on the values obtained for parameter t, we took into consideration: Changes in blood perfusion of the tissue; Changes in tissue water content and structure; Heat exchange at the wound surface and with tissues lying deeper than the wound. We also paid attention to relations with histopathologically and clinically assessed burn depth. Healthy (not burned) skin was the reference.
4.1. Burn wounds which heal within 3 weeks of burning The majority of wounds of a depth <60% dtms (as recognised by histopathology) should belong to this group. The reason for this assumption is the anatomy and function of the vascular plexi of the skin, a superficial one and a deep one, localised above and below this threshold depth [39,40]. In the shallowest burns (clinically Grade I, which are not analysed in this study) both plexi remain structurally undamaged and functionally active. Healing of the burn wound within 3 weeks is beyond question. In superficial dermal (IIa) wounds the function of the superficial plexus has been disturbed and has also been partially but reversibly damaged. Epithelisation, though longer than in (I) wounds, takes place within 3 weeks [29]. Shallower parts of the group of burns classified clinically as deep dermal (IIb) should also heal within this period. According to histopathology, these would be of a depth of about 60% dtms. In such cases the superficial plexus has been damaged, but the deep one is still at least partly functioning, enough to provide a blood supply and nourishment for the appendages of the skin. These elements provide for the epithelisation process in the wound, which probably takes place within the desired 3 weeks. The permeability of the capillaries of both plexi increases markedly and subsequently raises the hydration of the tissue and its effective thermal conductivity (k) [41]. In shallower wounds (clinically IIa and, in all likelihood, the more superficial of the IIb class) the circulation is increased in the preserved part of the superficial plexus and, especially, in the deep one. Heat exchange with the deeper tissues is, therefore, probably also increased. Finally, although the epithelium is partially or totally destroyed and the evaporation water loss (ewl) and subsequently also the heat loss to the environment are increased [26–29], such wounds are ‘‘warm’’ on a static thermogram, even warmer than the non-burned skin [8,23,42]. In view of these factors, one would expect fast reactions to external excitation to occur
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Fig. 7. A burn wound to the buttocks and posterior thighs of an 18-year-old patient (due to different fields of view of the photo-camera and the thermograph one photography is represented by two thermal pictures). (A1) Photograph taken on post-burn Day 2. Clinical evaluation and prognoses for the following areas of the wound were: 1–IIa, will be healed within 3 weeks of the burn; 2–IIa/IIb, no decision, indeterminate burn; 3–IIb/III, will not be healed within 3 weeks. (A2) corresponding to (A1) static thermographic images (upper-buttocks and lower-thighs). Prognoses based on ST were: 1 areas of a greater than discriminating value DT, will be healed; 2 similar areas, but cooler than 1, will be healed; 3 areas of DT smaller than discriminating value, will not be healed, 31 warm areas ‘‘islands’’ are difficult to interpret. They are localised like the areas of short t on the ADT picture. (A3) corresponding to (A1) ADT parametric images (upperbuttocks and lower-thighs). Prognoses based on ADT were: 1 well-defined areas of long t, will be healed within 3 weeks; 3 areas of short t, will not be healed. (B) The healing result—photograph taken on post-burn Day 18: 1 healed areas; 2 mainly healed area; 3 not healed parts of the wound before skin grafting.
here, faster than in the healthy tissue. This is not confirmed by the ADT experiment. 4.2. Burn wounds which do not heal within 3 weeks of burning Taking into account the histopathological assessment of burn depth, we included here a majority of wounds which were deeper than 60% dtms. In these wounds the superficial dermal plexus was totally destroyed. The deep plexus was damaged to such an extent that an insufficient number of
skin appendages were able to survive to enable the healing process to be completed within 3 weeks of burning. In clinical examination, damage of this extent should reveal among the deeper group of (IIb) burn wounds and all those of full thickness of the skin (III). There is practically no microcirculation in the wound and so thus any speculation can leave out the k component originating from vascular convection. In contrast, the k component arising from increased tissue water content (extreme vascular permeability) is still very high. The heat exchange on the wound surface is markedly increased as a result of the lack of an
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Fig. 8. Section of averaged temperatures profiles along the pig skin depth for non-burned skin (circles); shallow burn wounds that healed within 3 weeks (triangles); deep burn wounds that did not heal within 3 weeks (squares) (24 h after burn, temperature at steady state conditions) [44].
epithelium security layer and great hydration of the tissue (ewl) [26–29]. Because the deep dermal plexus is also markedly or totally destroyed, large-scale heat ‘‘escape’’ takes place to the deeper lying tissues. These wounds are ‘‘cold’’ in static thermography [8,23,42]. To understand the character of the thermal transients observed at the surface of the wounds in the ADT experiments described in this paper knowledge of the distribution of temperature along the depth of the tested tissue is necessary. Fortunately this is possible because in parallel to the ADT experiments we have also been involved in a contact probe study of the thermal properties of pig skin, including measurements of temperature distribution inside the burn wound [43–45]. The interesting data are shown in Fig. 8. When in the course of the ADT investigation the tissue detected (the surface of the skin) is subject to a strong, brief (15-s) thermal stimulus, manifested by a surface temperature rise of about 2.5 8C at the end of the pulse duration, the internal temperature rise reaches a depth of 1–2 mm. Fig. 8 shows that inside shallow burns there is hardly any temperature gradient between the externally heated layer of tissue, T 38.5 8C at the surface, and the more deeplying tissue of temperature T already at over 37.5 8C. Therefore, the cooling process is dependent mainly on heat exchange to the environment, T 22 8C, and only partly by vascular convection, because in this situation heat transportation by this route is insufficient. Heat exchange to the environment by radiation and air convection, which are rather slow processes, should be slower than in the unburned skin. In view of this, in the experimental conditions reported in the paper (for a short heating pulse) the thermal time constant t of a wound that healed within 3 weeks (a shallow one) is longer than the t of the unburned skin. For deep burns the same ADT excitation causes temperature T to rise to 36.5 8C, reaching a similar depth, 1–2 mm, as in the shallow ones, but at the deeper level there is still a relatively thick cold layer of burned tissue
(T 34.5 8C), which conducts heat well. Fast heat flow is possible to the deeper layers. Therefore, the process of cooling of this well hydrated and barely perfused tissue should be faster than in the unburned skin. It follows from this that the thermal time constant t of the wound not healed within 3 weeks (a deep one) should be shorter than the t of the unburned skin. This is in full agreement with the ADT experiment results. In clinical examples prognoses based on the ADT criterion valid for animals indicate that the decision concerning treatment should be modified and surgery markedly limited. However, more experience is still necessary to define the values of the thermal time constants for human skin burns objectively and quantitatively and to carry out an automatic classification of the region for surgery. The patients were, therefore, treated on the basis of clinical prognoses. 5. Conclusions 1. ADT examination is simple, non-contact and short. The instrumentation to be applied is based on the IR-cameras already used in hospitals and now available at reduced prices. 2. The procedure is not as sensitive to external conditions as static thermography (ST). However, the standards valid for ST should be secured. 3. The results of the ADT and histopathological evaluations are fully in agreement. This should not be regarded as the general rule, as the evaluation of the method was made ex post and in reality the classification threshold could be slightly shifted up or down, decreasing the score. The specific threshold of the t value as a predictor of burn healing could also be established for human burn wounds. 4. The result is quantitative, enabling burns to be objectively evaluated and treatment clearly documented. One image may be used to visualise wounds covering an extensive area. As has already been illustrated, it is a method that could easily be applied in clinical practice. 5. The results obtained in this work for the ADT method by evaluating the thermal time constants lead us to conclude that this may be declared a new effective method for burn wound discrimination and, therefore, for early burn treatment planning. However, for the method to be applied in clinical practice the measurement conditions, the duration and energy of excitation involved, as well as the procedures for discrimination and classification, all need to be optimised. References [1] Engrav LH, Heimbach DM, Reus JL, Harnar TJ, Marvin JA. Early excision and grafting vs. nonoperative treatment of burns of indeterminate depth: a randomised prospective study. J Trauma 1983;23:1001–4.
A. Renkielska et al. / Burns 32 (2006) 867–875 [2] Heimbach D, Engrav L, Grube B, Marvin J. Burn depth: a review. World J Surg 1992;16:10–5. [3] Converse JM, Robb-Smith AHT. An anatomic classification of burns. Ann Surg 1944;120:873–85. [4] Jackson DM. The diagnosis of the depth of burning. Br J Surg 1953;40:588–96. [5] Shakespeare PG. Looking at burn wounds: the A.B. Wallace Memorial Lecture 1991. Burns 1992;18:287–95. [6] Watts AMJ, Tyler PPH, Perry ME, Roberts AHN, McGrouther DA. Burn depth and its histological measurement. Burns 2001;27:154–60. [7] Singer AJ, Berruti L, Thode HC, McClain SA. Standardized burn model using a multiparametric histologic analysis of burn depth. Acad Emerg Med 2000;7:1–6. [8] Cole RP, Jones SG, Shakespeare PG. Thermographic assessment of hand burns. Burns 1990;16:60–3. [9] Newman P. A practical technique for the thermographic estimation of burn depth: a preliminary report. Burns 1980;8:59–63. [10] Liddington MJ, Shakespeare PG. Timing of the thermographic assessment of burns. Burns 1996;22:26–8. [11] Iraniha S, Cinat ME, VanderKam VM, Boyko A, Lee D, Jones J, et al. Determination of burn depth with noncontact ultrasonography. J Burn Care Rehab 2000;21:333–8. [12] Adams TST, Murphy JV, Gilleopte PH, Roberts AHN. The use of high frequency ultrasonography in the prediction of burn depth. J Burn Care Rehab 2001;22:261–2. [13] Afromowitz MA, Callis JB, Heimbach DM, DeSoto LA, Norton MK. Multispectral imaging of burn wounds: a new clinical instrument for evaluating burn depth. IEEE Trans Biomed Eng 1988;35:842–50. [14] Eisenbeiss W, Marotz J, Schrade JP. Reflection–optical multispectral imaging method for objective determination of burn depth. Burns 1999;25:697–704. [15] Kloppenberg FW, Beerthuizen GL, ten Duis HJ. Perfusion of burn wound assessed by laser Doppler imaging is related to burn depth and healing time. Burns 2001;27:359–63. [16] Pape SA, Skouras CA, Byrne PO. An audit of the use of laser Doppler imaging (LDI) in the assessment of burns of intermediate depth. Burns 2001;27:233–9. [17] Mileski WJ, Atiles L, Purdue G, Kogan R, Saffle JR, Herndon DN, et al. Serial measurements increase the accuracy of laser Doppler assessment of burn wounds. J Burn Care Rehab 2003;24:187–91. [18] Riordan CL, McDonough M, Davidson JM, Corley R, Perlov C, Barton R, et al. Noncontact laser Doppler imaging in burn depth analysis of the extremities. J Burn Care Rehab 2003;24:177–86. [19] Still JM, Law EJ, Klavuhn KG, Island TC, Holtz JZ. Diagnosis of burn depth using laser-induced Indocyanine green fluorescence: a preliminary clinical trial. Burns 2001;27:364–71. [20] Green HA, Bua D, Anderson RR, Nishioka NS. Burn depth estimation using Indocyanine green fluorescence. Arch Dermatol 1992;128:43–9. [21] Renkielska A, Nowakowski A, Kaczmarek M, Dobke MK, Grudzinski J, Karmolinski A, et al. Static thermography revisited—an adjunct method for determining the depth of the burn injury. Burns 2005;31:768–75. [22] Head JF, Elliot RL. Infrared imaging: making progress in fulfilling its medical promise. IEEE Eng Med Biol 2002;21:80–5. [23] Hackett MEJ. The use of thermography in the assessment of burn and blood supply of flaps, with preliminary reports on its use in Dupuytren’s contracture and treatment of varicose ulcers. Br J Plast Surg 1974;27:311–7. [24] Maldague XPV. Theory and practice of infrared technology for nondestructive testing New York: John Wiley and Sons Inc.; 2001.
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[25] Meyer W, Schwarz R, Neurand K. The skin of domestic mammals as a model for the human skin, with special reference to the domestic pig. Curr Probl Dermatol 1978;7:39–52. [26] Anselmo VJ, Zawacki BE. Effect of evaporative surface cooling on thermographic assessment of burn depth. Radiology 1977;123:331–2. [27] Cole RP, Shakespeare PG, Chissell HG, Jones SG. Thermographic assessment of burns using nonpermeable membrane as wound covering. Burns 1991;17:117–22. [28] Lamke LO, Nilsson GE, Reithner HL. The evaporative water loss from burns and the water vapour permeability of grafts and artificial membranes used in the treatment of burns. Burns 1977;3:159. [29] Krizek T, Robson MC, Wray Jr RC. Care of the burned patient. In: Barlinger WF, Rutheford RB, Zuidema GD, editors. The management of trauma. 2nd ed., Philadelphia: W.B. Saunders Co.; 1973. p. 650–7. [30] Lomnicki A. Wprowadzenie do statystyki dla przyrodnikow. (Introduction to statistics) Warszawa: Wydaw. Nauk. PWN, 1995 (in Polish). [31] Nowakowski A, Kaczmarek M. Dynamic thermography as a quantitative medical diagnostic tool. Med Biol Eng Comput 1999;37(Suppl. 1):244–5. [32] Ruminski J, Kaczmarek M, Nowakowski A. Medical active thermography—a new image reconstruction method. Lecture notes in computer science, vol. LNCS 2124. Berlin-Heidelberg: Springer; 2001. p. 274–281. [33] Nowakowski A, Kaczmarek M, Ruminski J, Hryciuk M, Renkielska A, Grudzinski J, et al. Medical applications of model based dynamic thermography. Proc SPIE 2001;4360:492–503. [34] Lawson RN, Wlodek CB, Webster DR. Thermographic assessment of burns and frostbite. Can Med Assoc J 1961;84:1129–31. [35] Wei-Ping Z, Xiang-Rong X. Study on the distribution pattern of skin temperature in normal Chinese and detection of the depth of early burn wound by infrared thermography. Ann N Y Acad Sci 1999;880:300–13. [36] Hargroder AG, Dawidson JE, Luther DG, Head JF. Infrared imaging of burn wounds to determinate burn depth. Proc SPIE 1999;3698:103–8. [37] Dickey FM, Holswadew SC, Yee ML. Burn depth estimation using thermal excitation and imaging. Proc SPIE 1999;3595:9–16. [38] Bull JP, Lennard-Jones JE. The impairment of sensation in burns and its clinical application as a test of the depth of skin loss. Clin Sci 1949;8:155–69. [39] Ostrowski K, editor. Histologia (Histology). Warszawa: Wydaw. Lek. PZWL; 1995 (in Polish). [40] Sawicki W. Histologia (Histology). Warszawa: Wydaw. Lek. PZWL; 2003 (in Polish). [41] Cohen ML. Measurement of the thermal properties of human skin: a review. J Invest Dermatol 1977;69:333–8. [42] Kuzan´ski WR, Zielin´ski KW. Telethermographic assessment of burn wound depth and its clinical and histometrical verification. Surg Child Intern 1998;6:219–25. [43] Hryciuk M, Nowakowski A. Multilayer thermal model of healthy and burned skin. In: Proceedings of the 2nd European medical and biological engineering conference, EMBEC’02, vol. 3, Pt 2; 2002. p. 1614–7. [44] Hryciuk M. Badanie struktury biologicznych obiekto´w warstwowych z wykorzystaniem pobudzenia cieplnego. (Investigation of structure of biological layered objects using thermal excitation) PhD Dissertation, Gdansk University of Technology, 2003 (in Polish). [45] Hryciuk M, Nowakowski A. Evaluation of thermal diffusivity variations in multi-layered structures. In: Proceedings of the 6th QIRT; 2003. p. 267–74.
Burn depths evaluation based on active dynamic IR thermal imaging—A preliminary study Alicja Renkielska a,*, Antoni Nowakowski b, Mariusz Kaczmarek b, Jacek Ruminski b a b
Department of Plastic Surgery and Burns, Medical University of Gdansk, Gdansk, Poland Department of Biomedical Engineering, Gdansk University of Technology, Gdansk, Poland Accepted 31 January 2006
Abstract Proper diagnostic assessment of burn wound depth is of the highest importance in selecting the mode of burn wound treatment. Several diagnostic methods – clinical and histopathological evaluation, as well as methods employing IR imaging – static thermography and active dynamic thermography (ADT) – are compared on the basis of in vivo experiments conducted on three domestic pigs (23 burn wounds). ADT is presented here as a new, reliable and quantitative method of assessing burn wound depth on the basis of discrimination of the thermal properties of burnt tissue. In the case of ADT registration of thermal images was performed following thermal pulse excitation. A series of captured infrared images was used as the basis for calculating the thermal time constant t for each pixel. The parameter values were compared with histopathological and clinical assessments of burn depth. The mean value of t was found for burns, which heal within 3 weeks (t = 12.08 1.94 s) and for burns, which did not heal during this period (t = 9.07 0.68 s), p < 0.05. The accuracy, sensitivity and specificity of all the methods tested were compared, the best results coming from ADT. The ADT method is fast, non-invasive and relatively inexpensive, although it still requires further animal experimentation as well as clinical study to confirm the results. # 2006 Elsevier Ltd and ISBI. All rights reserved. Keywords: Active dynamic IR thermal imaging; Burn depth; Diagnosis
1. Introduction The modern approach to skin burn depth assessment tries to resolve the problem of healing and the appropriate choice of treatment—conservative or surgical [1,2]. The traditional approach distinguishes the following grades of burn wound: I, superficial; IIa, superficial dermal; IIb, deep dermal; and III, full thickness of the skin [3]. In clinical practice even the inexperienced doctor has no difficulty in classifying first and third degree burns correctly. However, differentiation between the IIa (superficial dermal) and IIb (deep dermal) classes of wound is problematic. Clinical evaluation, mainly * Corresponding author at: Department Plastic Surgery and Burns, Medical University of Gdansk, ul. Debinki 7, 80 211 Gdansk, Poland. Tel.: +48 583 492 405; fax: +48 583 492 450. E-mail addresses: [email protected] (A. Renkielska), [email protected] (M. Kaczmarek), [email protected] (J. Ruminski). 0305-4179/$30.00 # 2006 Elsevier Ltd and ISBI. All rights reserved. doi:10.1016/j.burns.2006.01.024
based on visual inspection, only insures an accurate prognosis in 50–70% of these cases [2–5]. A method that enables burn wound depth to be correctly assessed and the choice of treatment to be made properly is, therefore, of the greatest importance. The aim of this paper is to present one such new objective method. The method based on IR thermal imaging of transient processes allows quantitative evaluation of burn depth and provides the answer to one of the most important questions in burn diagnostics: Will the burn heal spontaneously within 3 weeks of the burn or not? The reference method in burn depth evaluation is histopathological assessment but as this is invasive, local and time consuming, it is not frequently used [6,7]. Research interests have concentrated on the search for non-invasive, objective and quantitative diagnostic methods. Static thermography (ST) [8–10], ultrasonography (USG) [11,12], spectrophotometry [13,14], laser Doppler imaging (LDI) [15–18] and indocyanine green fluorescence (ICG) [19,20] are
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those most frequently cited, although none has been broadly accepted as a solution for clinical applications [2,5]. Recently we discussed the diagnostic value of ST [21], where the basic figure of merit—DT, namely the difference between the mean values of skin temperature for the burn wound area and the unaffected reference skin area, is defined. The inconveniences of the method are the need for meticulous care about measurement conditions and the lack of commonly accepted temperature ranges of DT for particular burn wound depth classifications. However, a great advantage of the method is its non-invasive character, the possibility of assessing relatively large burn areas and the easy and objective capture of images for medical documentation [22,23]. We propose an IR thermal imaging modality new to medical diagnostic applications, active dynamic IR thermal imaging (ADT), also termed active dynamic thermography. This is a method based on infrared detection which uses the cameras already applied in static thermography but which shows thermal tissue properties instead of changes in temperature distribution. Such an approach eliminates several of the drawbacks of traditional thermography while preserving the positive features and allowing quantitative objective assessment of burns.
be regarded as an advanced version of IR/NDT. Analysis of heat transfer enables thermophysical material properties, such as thermal diffusivity or conductivity, to be quantified. Knowledge of these two thermal parameters allows the subsurface structure to be determined. The general concept of the measurements performed in ADT is shown in Fig. 1. First the steady state temperature distribution on the tested surface is recorded using an IR camera. Next external thermal excitation (in our experiments heating by optical irradiation) is applied, followed by measurements of temperature transients on the tested surface. Typically, a set of halogen lamps may be applied as the thermal excitation source. Finally, burned skin can be quantitatively assessed by means of the thermal time constant (t). The data acquisition process is illustrated in Fig. 2. The example shows tracing of temperature in a specific pixel position x, y, taken during and after a thermal pulse excitation. Measurement of temperature is performed here only during the recovery phase (in this case the cooling phase, following the heating). Thermal transients are described by exponential functions. For one-directional heat flow the simplest description of surface temperature changes may be given for the cooling phase as shown in Fig. 2(A) by:
2. Materials and methods 2.1. Active dynamic IR thermal imaging (ADT)
t TðtÞ ¼ T 0 þ DT exp t
The concept of infrared non-destructive testing (IR/NDT) has been known in industry for several years [24]. ADT may
where T(t) is the pixel temperature T in time t, T0 the temperature before excitation, DT is the temperature rise
Fig. 1. Schematic diagram of the ADT instrumentation—the IR camera synchronised with an excitation source (in the experiment described this was a set of halogen lamps) allows the surface temperature of the object under examination (the animal or the patient) to be recorded at a speed of 30 frames/s. Changes in this temperature are caused by the external heating and are dependent on the internal structure of the object tested.
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Fig. 3. Positioning of the burned areas on the back of a pig. Symmetrical wounds for reference histopathological examination and for thermographic observation are indicated.
Fig. 2. Measurement procedure (A) course of temperature at the pixel x, y in time; tb/e moments at which the heating source is switched on (beginning) and off (end), respectively, t30 time of termination of the recording; (B) thermograms showing temperature distribution at the surface of the object (the skin) recorded in time; the temperature scale is attached for easy interpretation of the picture.
as a result of excitation. The value of the thermal time constant t depends on different existing mechanisms of heat flow and is strongly correlated to the physical structure of the burns. In our case the temperature of each pixel is captured to calculate the thermal time constant specific to each pixel (correlated with the burn depth). The parametric image of the time constants then enables the tested surface to be visualised thanks to the high degree of correlation with the depth of the burn wound. The value of any new diagnostic method should be carefully tested in objective fully controlled experiments. In our case this is the crucial role of in vivo experiments on pigs. The experiment was conducted on young domestic pigs, each weighing approximately 20 kg. The Local Ethics Commission for Experimentation on Animals at the Medical University of Gdansk, Poland approved the plan for the experiment. The reason for the choice of the pig as an experimental animal was the high degree of functional and structural similarity of pig skin to human skin [25]. The animals were subjected to reference burns of different depths by adopting Singer’s procedure [7] already applied in our earlier ST experiment [21]. Anaesthesia and analgesia were obtained by the administration of ketamine (im), pentobarbital (iv) and fentanyl (iv) at doses of 20, 30– 50 and 0.5–0.1 mg/kg, respectively. Each pig was usually subjected to eight pairs of symmetrical wounds covering approximately 1.5% of its total body surface area, in exactly the same manner as in our recent work (Fig. 3) [21]. One wound in each pair was for thermography (testing by ADT),
while the symmetrical (contralateral) wound was for taking biopsies for histopathological examination. The wounds were inflicted by an aluminium rod with dimensions of 2.5 cm 2.5 cm 7.5 cm and a weight of 150 g, which was applied to the skin at a controlled temperature of 80 8C in the designated areas for 5, 15 and 25 s, respectively and at 90 8C for 60 s. This resulted in burn wounds of the following depths, expressed as the relative thickness of the skin, a percentage of the dermis thickness at the measurement site (dtms), as shown in Fig. 3:
1 2 3 4
and and and and
5: 6: 7: 8:
11.92 2.98% 21.58 3.22% 47.8 18.16% 67.3 14.65%
dtms; dtms; dtms; dtms.
As we have also recently described, the animals breathed spontaneously during the course of the experiment and were given fentanyl at a dose of 0.5–0.1 mg/kg following the invasive phase (the infliction of burns and the securing of specimens for histopathological examination). In the subsequent follow-up period there was no need to keep the animals on this agent. The general condition of the animals was good, they were fed in a natural way and their daily gain in body weight was up to 0.5 kg. To prevent any external influence on the healing of burn wounds no medicaments with a general therapeutic action were administered. In the course of healing the burn wounds were left open, without dressings or topical agents [21]. However, several wounds were excluded from the measurements because of accidental mechanical damage to the animals’ skin caused by abrasion against the walls of the cages. To prevent the interaction of different thermal phenomena arising from different kinds of wound (burn, biopsy and abrasion) we excluded all the mechanically damaged wounds from the material investigated by the ADT procedure. This dramatically lowered the total number of wounds analysed. Finally, 23 wounds were subjected to the analysis presented here.
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Specimens for bacterial culture were collected from the skin before infliction of the burns and from the skin and wounds at 1, 3 and 7 days after burning. The solution of the problem of evaporation water loss (ewl) reported by Anselmo and Zawacki [26] and Cole et al. [27] has also been described by us [21]. The epithelium was almost totally destroyed and thus all the wounds were equally devoid of the insulation layer, a factor which might have been responsible for the differences in evaporation water loss (ewl) and, therefore, of some influence upon the surface temperature of the wound [26]. No agents in the form of either gels or protective membrane were used to prevent evaporation from the wound [27,28]. Clinical evaluation of burn depth was performed 24 h after the wounds were inflicted, using traditional observational criteria [3,4], on the basis of agreement between two plastic surgeons experienced in burn treatment. The same surgeons made an assessment of the healing result 3 weeks later, classifying the wounds as ‘‘healed’’ or ‘‘not healed’’. Burn wound depth was assessed following the Singer method [7] by histopathological determination of the depth of damage to the following skin elements: hair follicle (epithelial cells), connective tissue collagen (a change in collagen staining), nerves and smooth muscles (mesenchymal cells) and blood vessels (endothelial cells). The depth was measured in millimetres, starting from the epithelium basal layer. Histopathological results were given as a percentage of the dermis thickness at the measurement site (dtms). The ADT examination was conducted over the three consecutive days following infliction of the burn wound. All the conditions required as the ‘‘gold standard’’ for static thermographic examination were also met [21]. The thermographic IR camera AGEMA THV-900 SW/TE of 0.1 8C resolution was used for recording thermal images. The camera was placed at a distance of 0.75 m from the pig’s back in the plane perpendicular to it. The parameters applied for burn wound depth evaluation with a view to the choice of treatment, namely static thermography (DT) and active dynamic thermography (t), were calculated for the three consecutive post-burn days. The observation area dependent on the camera field of view (FOV) was typically 20 cm 15 cm. The ADT experiment was performed with pulse optical excitation lasting 15 s and resulting in a surface temperature rise of 2.5 8C, followed by a 30-s recording of the self-cooling phase. The excitation was performed using a set of halogen lamps of 1000 W and equipped with a mechanical shutter for prompt switching on and off of the power pulse. One exponent approximation (model of the thermal equivalent structure) was applied to determine the time constant t. The full diagnosis takes several minutes using automatic calculation procedures. The same recording procedure was applied in the clinical cases to illustrate the application of the method in hospital practice. For three post-burn days the measurements of DT and t did not differ significantly for either group. The Day 2 values were, therefore, taken for analysis, since they are useful from
a clinical point of view. At this stage a hospitalised patient’s status is usually stable and this is a good time to reach a decision concerning surgery [29]. For the purpose of classifying the burn wounds into those healing within 3 weeks (requiring conservative treatment) and ‘‘non-healing’’ (needing surgery) the results were subjected to statistical analysis. This was performed by means of the variance analysis ANOVA and by comparing the average post hoc values with Tukey’s RIR-test [30]. To determine the properties of the methods of burn wound assessment quantitatively the accuracy, sensitivity, and specificity have been calculated as: Accuracy: the ratio of the sum of true positive cases and true negative cases to the total number of cases; Sensitivity: the ratio of the number of true positive cases to the number of true positive cases plus the number of true negative cases; Specificity: the ratio of the number of true negative cases to the number of true negative cases plus the number of false positive cases.
3. Results Groups of wounds were distinguished post hoc: those shallower than 60% of the dtms, which healed within 3 weeks (18 cases); and those deeper than 60% of the dtms, unhealed (five cases) (Fig. 4). For ADT the mean value of the thermal time constant for burns shallower than 60% of the dtms (those healing within 3 weeks) was t = 12.08 1.94 s and for deeper ones (‘‘nonhealing’’) it was t = 9.07 0.68 s. The difference was at the statistically significant level, ( p < 0.05). We found that parameter t had a higher value (was longer) for wounds, which self-healed within 3 weeks than for the unaffected skin, while t had a lower value (was shorter) for deeper burns that failed to heal within this period. The discrimination threshold was calculated as t = 10.125 s (Fig. 4). When this value was used for burn discrimination, the accuracy, sensitivity, and specificity were all 100%.
Fig. 4. Thermal time constants t of burn wounds classified as ‘‘healed’’ and ‘‘non-healed’’ within 3 weeks. The threshold value is t = 10.125 s.
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In all three parameters, the accuracy, sensitivity and specificity of the histopathological evaluation, were also 100%. For the clinical method accuracy was 60.9%, sensitivity 50% and specificity 100%. When static thermography was used the value DT = 0.3 8C was assumed as the classification threshold. With this value the accuracy, sensitivity, and specificity were 91.3%, 94.4% and 80.0%, respectively.
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An example of skin burns inflicted on a pig is shown in Fig. 5. Of the following images photograph (A) was taken on post-burn Day 2 and (D) on post-burn Day 21, (B) shows static thermography on post-burn Day 2, and (C) a parametric image of the thermal time constant on postburn Day 2. The ADT method has already been adopted for clinical use. As an example, a burn wound on the right thigh of one patient is shown in Fig. 6 and burns on both thighs and buttocks of another patient are shown in Fig. 7. The results of the thermographic investigations had no influence on the choice of burn treatment. With regard to Fig. 7, tangential excision of necrotic tissue was performed according to the clinical evaluation of areas marked 2 and 3 (IIa/IIb and IIb/III, respectively). From photograph (A1) it may be suspected that the shallower burnt areas of the right thigh (2 in the clinical and ADT images) have been damaged. These areas would probably have healed spontaneously within 3 weeks of burn infliction. The static thermogram of the wounds to both thighs should be interpreted as prognostically misleading; the cold areas of both lateral aspects of the thighs (3) healed. The warmer parts (31), the ‘‘warm islands’’, are difficult to interpret. They are localised like the ‘‘short t’’ areas on the ADT image and unhealed parts of the wounds on post-burn Day 18. In contrast, the prognosis based on the ADT results would allow for the proper choice of treatment: surgery reduced to the medial and posterior surfaces of both thighs (3 in the clinical image and area 3 ‘‘short t’’ in ADT). In bacteriological cultures only normal and transient flora were found and no clinical symptoms of wound infection were observed.
4. Discussion Fig. 5. Photographic and corresponding thermographic images of experimental burn wounds on a pig—no. 5–IIa, dermis thickness at the measurement site (dtms): 10.1%, prognosis: will be healed, result: healed; no. 6–IIb, dtms: 24%, prognosis: will not be healed, result: healed; no. 7–IIb, dtms: 41%, prognosis: will not be healed, result: healed; no. 8–IIb, dtms: 54.2%, prognosis: will not be healed, result: healed. (A) Photograph taken on postburn Day 2. Clinical assessment suggests no healing of the wounds nos. 6, 7 and 8 within 3 weeks; the treatment decision would be surgery. Comparison of this clinical prognosis with the healing result (three false negative cases and only one true positive) indicates the low diagnostic value of the clinical method in cases evaluated as deep dermal (IIb). (B) Static thermography (ST) image on post-burn Day 2. DT of wounds nos. 5, 6 and 7 was greater than the threshold value DT = 0.3 8C. The prognosis based on ST would be—will be healed within 3 weeks of burn. DT of the burn wound no. 8 was 0.02 8C (smaller than the threshold value) and the prognosis would be—will not be healed (false-negative case). Thus static thermography would help in two out of three cases falsely evaluated by the clinical method. (C) Parametric image t on post-burn Day 2. This image is relatively uniform and burn wound borders are almost indistinguishable. However, t values of all wounds are larger (longer) than the threshold value t = 10.125 s and, according to this threshold value of t, the decision based on ADT investigation would be to maintain a conservative treatment of all wounds as all should heal (and in fact they did heal). This confirms the extremely high diagnostic value of ADT. (D) Photograph taken on post-burn Day 21. All four presented here wounds have healed.
We started working on model-based ADT applications in medical diagnostics in 1999 [31] and since then have published further data on the procedures applied to burn evaluation, for example in 2001 [32,33]. Prior to these publications thermography was applied in burn depth assessment only in the traditional static form, listing only the most important positions [8–10,22,34–36]. Only Dickey et al. [37] made the attempt to propose an in vitro burn model using biosynthetic skin dressing and dynamic thermography measurement. Apart from our results, no in vivo experiments or clinical cases have been presented at any time. The depth of experimental burn wounds has been evaluated by means of four diagnostic methods: clinical observation, traditional thermography (ST), ADT and histopathology (as the reference). In our experiment, the accuracy of the clinical method with respect to choice of the mode of treatment was only 60.9%, which is comparable to results given elsewhere by the authors of clinical papers [2,5] and which would seem to be unsatisfactory. The high degree of specificity of the method (100%) might be the
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Fig. 6. Photographic and corresponding thermographic images of a burn wound to the posterior surface of the right thigh of a 49-year-old patient: (A) Clinical burn depth evaluation of the area marked: 1–IIa superficial dermal, 2–IIa superficial dermal and, more centrally, IIb deep dermal, 3–IIb deep dermal and, in the lower part, III full thickness (B) Static thermography (the extremity is slightly medially rotated in comparison to the photograph). Areas 2 and 3 are the coldest and are without marked internal differentiation. (C) Active dynamic thermography parametric image (rotation of the extremity as above). The areas with short thermal time constants t and which qualified for surgery are well defined. These areas are markedly smaller when compared with areas 2 and 3 in the photograph and in the static thermogram.
result of a tendency by doctors to overestimate burn depth. This observation has already been discussed in the literature [17,18]. Taking into account the small number of accurate prognoses with regard to the classification ‘‘wound healing within 3 weeks’’, this clinical method, based on visual inspection (sometimes additionally supported by the ‘‘pinprick test’’ [38]), should be replaced or at least supported by another more objective and quantitative method. In the histopathological assessment of burns the accuracy, sensitivity and specificity of the method in our experiment was 100%. This result confirms the high diagnostic value of the method and its position as the reference for evaluation of other newly established methods in the assessment of burn depth [6,7,34]. However, its invasive character, the necessity of multiple burn wound biopsies and a delay of several days while waiting for the result markedly restricts the usefulness of this method in everyday hospital practice. Static thermography as tested in our study has already been in practical use in burn diagnostics for many years. However, the disadvantages of this method, mentioned in the introduction [21–23], limit its popularity. In our studies the quality parameters: accuracy 91.3%, sensitivity 94.4%, and specificity 80%, show its usefulness as an adjunct method in burn wound depth assessment and confirm the conclusions drawn from clinical tests [8–10,22,23,34–36]. When reflecting on the values obtained for parameter t, we took into consideration: Changes in blood perfusion of the tissue; Changes in tissue water content and structure; Heat exchange at the wound surface and with tissues lying deeper than the wound. We also paid attention to relations with histopathologically and clinically assessed burn depth. Healthy (not burned) skin was the reference.
4.1. Burn wounds which heal within 3 weeks of burning The majority of wounds of a depth <60% dtms (as recognised by histopathology) should belong to this group. The reason for this assumption is the anatomy and function of the vascular plexi of the skin, a superficial one and a deep one, localised above and below this threshold depth [39,40]. In the shallowest burns (clinically Grade I, which are not analysed in this study) both plexi remain structurally undamaged and functionally active. Healing of the burn wound within 3 weeks is beyond question. In superficial dermal (IIa) wounds the function of the superficial plexus has been disturbed and has also been partially but reversibly damaged. Epithelisation, though longer than in (I) wounds, takes place within 3 weeks [29]. Shallower parts of the group of burns classified clinically as deep dermal (IIb) should also heal within this period. According to histopathology, these would be of a depth of about 60% dtms. In such cases the superficial plexus has been damaged, but the deep one is still at least partly functioning, enough to provide a blood supply and nourishment for the appendages of the skin. These elements provide for the epithelisation process in the wound, which probably takes place within the desired 3 weeks. The permeability of the capillaries of both plexi increases markedly and subsequently raises the hydration of the tissue and its effective thermal conductivity (k) [41]. In shallower wounds (clinically IIa and, in all likelihood, the more superficial of the IIb class) the circulation is increased in the preserved part of the superficial plexus and, especially, in the deep one. Heat exchange with the deeper tissues is, therefore, probably also increased. Finally, although the epithelium is partially or totally destroyed and the evaporation water loss (ewl) and subsequently also the heat loss to the environment are increased [26–29], such wounds are ‘‘warm’’ on a static thermogram, even warmer than the non-burned skin [8,23,42]. In view of these factors, one would expect fast reactions to external excitation to occur
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Fig. 7. A burn wound to the buttocks and posterior thighs of an 18-year-old patient (due to different fields of view of the photo-camera and the thermograph one photography is represented by two thermal pictures). (A1) Photograph taken on post-burn Day 2. Clinical evaluation and prognoses for the following areas of the wound were: 1–IIa, will be healed within 3 weeks of the burn; 2–IIa/IIb, no decision, indeterminate burn; 3–IIb/III, will not be healed within 3 weeks. (A2) corresponding to (A1) static thermographic images (upper-buttocks and lower-thighs). Prognoses based on ST were: 1 areas of a greater than discriminating value DT, will be healed; 2 similar areas, but cooler than 1, will be healed; 3 areas of DT smaller than discriminating value, will not be healed, 31 warm areas ‘‘islands’’ are difficult to interpret. They are localised like the areas of short t on the ADT picture. (A3) corresponding to (A1) ADT parametric images (upperbuttocks and lower-thighs). Prognoses based on ADT were: 1 well-defined areas of long t, will be healed within 3 weeks; 3 areas of short t, will not be healed. (B) The healing result—photograph taken on post-burn Day 18: 1 healed areas; 2 mainly healed area; 3 not healed parts of the wound before skin grafting.
here, faster than in the healthy tissue. This is not confirmed by the ADT experiment. 4.2. Burn wounds which do not heal within 3 weeks of burning Taking into account the histopathological assessment of burn depth, we included here a majority of wounds which were deeper than 60% dtms. In these wounds the superficial dermal plexus was totally destroyed. The deep plexus was damaged to such an extent that an insufficient number of
skin appendages were able to survive to enable the healing process to be completed within 3 weeks of burning. In clinical examination, damage of this extent should reveal among the deeper group of (IIb) burn wounds and all those of full thickness of the skin (III). There is practically no microcirculation in the wound and so thus any speculation can leave out the k component originating from vascular convection. In contrast, the k component arising from increased tissue water content (extreme vascular permeability) is still very high. The heat exchange on the wound surface is markedly increased as a result of the lack of an
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Fig. 8. Section of averaged temperatures profiles along the pig skin depth for non-burned skin (circles); shallow burn wounds that healed within 3 weeks (triangles); deep burn wounds that did not heal within 3 weeks (squares) (24 h after burn, temperature at steady state conditions) [44].
epithelium security layer and great hydration of the tissue (ewl) [26–29]. Because the deep dermal plexus is also markedly or totally destroyed, large-scale heat ‘‘escape’’ takes place to the deeper lying tissues. These wounds are ‘‘cold’’ in static thermography [8,23,42]. To understand the character of the thermal transients observed at the surface of the wounds in the ADT experiments described in this paper knowledge of the distribution of temperature along the depth of the tested tissue is necessary. Fortunately this is possible because in parallel to the ADT experiments we have also been involved in a contact probe study of the thermal properties of pig skin, including measurements of temperature distribution inside the burn wound [43–45]. The interesting data are shown in Fig. 8. When in the course of the ADT investigation the tissue detected (the surface of the skin) is subject to a strong, brief (15-s) thermal stimulus, manifested by a surface temperature rise of about 2.5 8C at the end of the pulse duration, the internal temperature rise reaches a depth of 1–2 mm. Fig. 8 shows that inside shallow burns there is hardly any temperature gradient between the externally heated layer of tissue, T 38.5 8C at the surface, and the more deeplying tissue of temperature T already at over 37.5 8C. Therefore, the cooling process is dependent mainly on heat exchange to the environment, T 22 8C, and only partly by vascular convection, because in this situation heat transportation by this route is insufficient. Heat exchange to the environment by radiation and air convection, which are rather slow processes, should be slower than in the unburned skin. In view of this, in the experimental conditions reported in the paper (for a short heating pulse) the thermal time constant t of a wound that healed within 3 weeks (a shallow one) is longer than the t of the unburned skin. For deep burns the same ADT excitation causes temperature T to rise to 36.5 8C, reaching a similar depth, 1–2 mm, as in the shallow ones, but at the deeper level there is still a relatively thick cold layer of burned tissue
(T 34.5 8C), which conducts heat well. Fast heat flow is possible to the deeper layers. Therefore, the process of cooling of this well hydrated and barely perfused tissue should be faster than in the unburned skin. It follows from this that the thermal time constant t of the wound not healed within 3 weeks (a deep one) should be shorter than the t of the unburned skin. This is in full agreement with the ADT experiment results. In clinical examples prognoses based on the ADT criterion valid for animals indicate that the decision concerning treatment should be modified and surgery markedly limited. However, more experience is still necessary to define the values of the thermal time constants for human skin burns objectively and quantitatively and to carry out an automatic classification of the region for surgery. The patients were, therefore, treated on the basis of clinical prognoses. 5. Conclusions 1. ADT examination is simple, non-contact and short. The instrumentation to be applied is based on the IR-cameras already used in hospitals and now available at reduced prices. 2. The procedure is not as sensitive to external conditions as static thermography (ST). However, the standards valid for ST should be secured. 3. The results of the ADT and histopathological evaluations are fully in agreement. This should not be regarded as the general rule, as the evaluation of the method was made ex post and in reality the classification threshold could be slightly shifted up or down, decreasing the score. The specific threshold of the t value as a predictor of burn healing could also be established for human burn wounds. 4. The result is quantitative, enabling burns to be objectively evaluated and treatment clearly documented. One image may be used to visualise wounds covering an extensive area. As has already been illustrated, it is a method that could easily be applied in clinical practice. 5. The results obtained in this work for the ADT method by evaluating the thermal time constants lead us to conclude that this may be declared a new effective method for burn wound discrimination and, therefore, for early burn treatment planning. However, for the method to be applied in clinical practice the measurement conditions, the duration and energy of excitation involved, as well as the procedures for discrimination and classification, all need to be optimised. References [1] Engrav LH, Heimbach DM, Reus JL, Harnar TJ, Marvin JA. Early excision and grafting vs. nonoperative treatment of burns of indeterminate depth: a randomised prospective study. J Trauma 1983;23:1001–4.
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