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DIEP flap breast reconstructions: thermographic assistance as a possibility for perforator mapping and improvement of DIEP flap quality

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Abstract

In the modern world, one-third or more of breast cancer patients still undergo uni- or bilateral mastectomy. Breast cancer patients, in general, have a good prognosis and long-term survival. Therefore, the treatment must not only focus on survival but also on the quality of life. Breast reconstruction with an autologous free deep inferior epigastric artery perforator (DIEP) flap is one of the preferred options after mastectomy. A challenging step in this procedure is the selection of a suitable perforator that provides sufficient blood supply for the flap to prevent necrosis after anastomosis. In this pilot study, the possibilities for dynamic infrared thermography (DIRT) are investigated to select the best suitable perforator. The measurements are done with external cooling in the preoperative stage to accurately predict the location of the dominant perforators. During the surgery, in the peroperative stage, measurements are done for mapping the influence of a specific perforator on the perfused areas of the abdominal flap. Perforators are sequentially closed and opened again to map the influence of that perforator on the vascularization of the flap, visualized with the help of the thermographic camera. The acquired steady-state thermal images could help decide which parts of the abdominal flap to use for the reconstruction so that the chance of (partial) necrosis is reduced. In the postoperative stage, DIRT could visualize the arterial and or venous thrombosis before they become clinically obvious as (partial) necrosis. At present DIRT seems to be a valuable investigation for the pre-, per-, and postoperative phases of DIEP-flap reconstructions. Large, high-quality clinical studies are needed to determine its definitive role.

© 2020 Optical Society of America

1. INTRODUCTION

Belgium has the highest incidence of breast cancer in women per capita (113.2/100,000), which totals to around 11,000 women each year according to Thiessen et al. [1]. One-third (34%) of the breast cancer patients undergo uni- or bilateral mastectomy, and 1 out of 7 undergo reconstructive surgery, half of which are performed with autologous tissue. Thirty-two percent of the autologous tissue flaps are deep inferior artery epigastric perforator (DIEP) flaps [13]. A DIEP flap breast reconstruction is thus commonly used for breast reconstruction after mastectomy. A DIEP flap is a perforator flap that only transplants skin and subcutaneous tissue. The breast is reconstructed without sacrificing any of the abdominal muscles. In exceptional cases, the transplanted tissue lacks sufficient blood supply. This results in cell injury, cell death, and tissue necrosis [4]. The healing process can lead to extra surgical procedures with added physical and mental distress. The current state of the art is the use of computed tomography angiography (CTA) and Doppler imaging to locate the perforators and reveal the hemodynamic properties of the flap [5]. These current selection techniques have weaknesses like invasiveness, use of ionizing radiation and intravenous contrast medium, or are imprecise. Dynamic infrared thermography (DIRT) can be an added value by tackling those weaknesses by being noninvasive, quick, inexpensive to use, and accurate. Studies [6] so far indicate that DIRT can be successfully used for diagnosis of breast cancer, diabetes, dentistry, diabetic neuropathy, etc. In the coming years, the use of DIRT in the medical field is likely to surge. Here we discuss the results and techniques used in this pilot study during the preoperative and peroperative stage and its possible use in postoperative stage.

A. Current Methods

There are multiple methods to locate perforating vessels in the flap, such as CTA, Doppler ultrasound, and indocyanine green (ICG) fluorescence angiography (ICG-FA). According to Kolacz et al., an ideal method in a clinical setting meets the following conditions: noninvasiveness, simplicity, repeatability, the ability of peroperative assessment, and low cost [7]. (DIRT is a noninvasive monitoring technique, unlike ICG-FA and CTA, and it is used in clinical medicine as a mechanism to measure skin temperatures [8]. A review with the advantages and disadvantages of multidetector (MD)CTA, Doppler/colour Doppler ultrasound (CDU), magnetic resonance angiography (MRA), and DIRT was done by Thiessen et al. [1]

CTA is currently the gold standard for perforator mapping in breast reconstructions with DIEP flaps, although it can cause complications because it requires ionizing radiation and the use of intravenous contrast medium [9,10]. It is also known for being time consuming and expensive. The hemodynamic properties can also be registered by a Doppler echo. This technique is completely painless and uses ultrasonic sound waves. Cifuentes et al. mentions that strong Doppler correlates with larger hot spots in DIRT [11]. Additionally, stronger Doppler signals have also been suggested to be correlated with larger perforator vessels [11].

DIRT uses the principle of thermal radiation. Every object emits natural infrared radiation, which can be registered by a thermal camera. This technique does not use damaging radiation nor an additional medium. According to the preliminary data of the DIRT method in comparison with other state-of-the-art methods [CTA, (MD)CTA, handheld Doppler/CDU] as mentioned in the review paper by Thiessen et al. [1], DIRT is, therefore, a promising technique for being the least invasive but accurate method for determining the hemodynamic properties [1]. Most results with the application of DIRT for DIEP flap monitoring are reported in the publications of de Weerd et al. [10,12]. Recently, the first standardized setup for DIRT and DIEP flap reconstruction was published [13].

2. DYNAMIC INFRARED THERMOGRAPHY

Perforators that transport blood to the subdermal plexus cause local heating at the skin surface [10]. When performing a cold challenge, the perforators can be located with the help of a thermographic camera. During the rewarming process, the perforators become visible as the skin surface starts to warm up again. This technique can be used in the preoperative, peroperative, and postoperative stages. To visualize the perforators, a cold challenge must be performed. The temperature changes of the skin must be in a physiological range to prevent permanent tissue damage [14]. The period of rewarming starts as soon as the cold challenge stops. At this point, there are no hot spots visible. After some time, the first hot spots become visible. These hot spots represent the perforators. The thermal images are analyzed to find the hot spots and to discover the pace and pattern of the rewarming. The first occurring hot spots can be related to perforators with a larger blood supply. A fast rewarming indicates a perforator, which transports more blood to the skin surface. Progressive reheating around the hot spot illustrates a well-developed vascular network around this location. [10]. As a result of analyzing the images, the surgeon can obtain information about the hemodynamic properties of the blood vessels in the flap. This can be crucial to select the perforator that vascularizes the flap. This potentially diminishes the occurrence of partial necrosis of the flap due to poor vascularization. An optional postoperative test can be performed to analyze the blood supply and ensure a successful surgery.

The method of static thermography does not render an unequivocal indication of the location of the perforators [7]. Several studies of dynamic thermography [7,9] are available, which include different methods for obtaining a temperature difference to reveal the dynamic properties. The flap was stimulated with high and low temperatures. The number of hot spots was smaller when a heat stimulation was used in contrast to cold stimulation [7]. The area was cooled down 5°C–6°C or heated up by 5°C–6°C to avoid damage by burning the tissue [7]. A small stimulation amplitude produces a poorer signal in relation to measurement noise. This shows the need for postprocessing in order to enhance the IR images. In our case, a cold challenge was used to reveal the dynamic properties. The hot spots and perforators were clearly visible on the IR images, but postprocessing can make them potentially even more visible. Dynamic thermography is a useful tool to reduce the time of perforator selection and can be performed at any stage of surgical treatment.

3. EMISSIVITY OF HUMAN SKIN

Body surface temperature can be measured with the use of an IR camera. The outcome of a complicated combination of central and local regulatory systems is reflected by the surface temperature of an extremity. As a living organism, the human body tries to maintain homeostasis, that is, an equilibrium of all systems within the body, for all physiological processes, which leads to dynamic changes in heat emission [15]. The dynamic changes in heat emission depend on internal (e.g.,  blood flow, hormones, smoking, exercise, emotion, etc.) and external (e.g.,  room temperature, humidity, clothing, cosmetics, etc.) conditions. This makes it imperative to develop standard procedures during surgery in order to be able to interpret thermal imaging results. The most important factor seems to be arterial blood flow, as surface temperature increases with intensified blood flow [16].

According to Vollmer [15], emissivity $\epsilon$ is a measure of the efficiency in which a surface emits thermal energy. It is defined as the ratio of thermal energy (radiation) from a surface being emitted relative to that emitted by a thermally black surface (a black body) at the same temperature. A black body is a material that is a perfect emitter of heat energy and has an emissivity value of 1. A material with an emissivity value of 0 would be considered a perfect thermal mirror. As reported by Lee and Minkina, the generally accepted emissivity $\epsilon$ of human skin, independent of the skin color, is $0.98 \pm 0.01$, which makes human skin a nearly perfect black body [17,18]. Hardy and Muschenheim concluded that dead skin can be regarded as a perfectly black surface with an emissivity of $\epsilon = 1$ [19]. The average skin surface temperature is 32°C [18].

Tables Icon

Table 1. Experimental Conditions Used by Various Research Groups for Recording of Infrared Thermal Images [6]

In our case, a cold challenge is performed. This reveals the dynamic properties of the flap. It is therefore not necessary to determine the absolute temperature, although it is still important to keep the errors constant during measurement. For standardization, the following five major conditions, given by Cockburn, should be fulfilled in order to avoid common errors [20].

  • 1. Proper room conditions:
    • • Minimum size of $9\;{{\rm m}^2}$
    • • Constant room temperature (23.5°C)
    • • Humidity of 45%–60%
    • • Avoid turbulent airflow close to the patient (heat emitters, ventilators, air conditioning)
    • • Reduce the effect of sunlight with shades
    • • Proper selection of material on walls and ceiling
  • 2. Proper preparation of the patient:
    • • Acclimatization for at least 15 min, taking off clothes from areas to be examined
    • • No intake of food, alcohol, coffee, or tea 2 h before examination
    • • No physical exercise 24 h before examination
    • • No excessive tanning or sunburns 7–10 days before examination
  • 3. Standardized equipment:
    • • Calibrated IR camera, low noise equivalent temperature difference (NETD)
    • • Camera switched on at least 1 h before examination in the same room (thermal shock)
  • 4. Proper recording and storage of acquired images:
    • • Avoid grazing incidence of radiation on camera, select viewing angle close to 0° since $\varepsilon = \varepsilon ({\rm angle})$
    • • Include gender, age diagnosis, current medication, size, weight, room conditions, and date
  • 5. Representation of images:
    • • Standardized temperature scale, often a span 23°C–36°C or 24°C–38°C.

4. EXPERIMENTAL CONDITIONS

Experimental conditions like the temperature of the surroundings (Table 1), moisture, and airflow have an influence on the infrared radiation emitted by a surface. Controlled environments are thus an absolute necessity for thermographic experiments. It is even more important in medical applications where the temperature differences are only a few degrees. Standardization or a standard protocol is key to make it possible to compare thermographic images. As mentioned before, this standardization should comply with five major conditions to avoid common errors. The standardized measurement setup to obtain the results in this article is described by Thiessen et al. [13]

In order to perform a primary investigation with respect to the usage of IR thermography during surgery, the researchers attended a breast reconstruction by means of a DIEP flap. During the reconstruction, the researchers performed thermal measurements on the patient that can act as a foundation for more dedicated measurements during a follow-up measurement campaign. A unilateral breast reconstruction using the DIEP flap technique means that either the left or right side of the lower abdominal wall can be chosen for transplantation. A bilateral breast reconstruction using the DIEP flap technique means that both the left and the right flap are used to reconstruct both breasts. Infrared thermography can possibly facilitate the choice regarding perforator selection.

5. INSTRUMENTATION

Infrared thermography experiments require a set of professional instrumentation [6] that consists of an infrared thermal camera, a long-arm tripod [Fig. 1(a)], a display device, and an image processing unit. A transient measurement is obtained by stimulating the tissue. The measurement setup for DIRT was standardized by Thiessen et al. [13] and is used in all the measurements. It is important that measurements can be performed during any time of the surgery without disturbing the surgeon.

 figure: Fig. 1.

Fig. 1. Measurement setup to perform IR thermography measurements on a DIEP flap. (a) Measurement setup with a long-arm tripod [13]; (b) cooling method with a sterile plastic bag filled with ice and water [13].

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A. Infrared Thermal Camera

The most recent generation cameras have a large focal plane array (FPA) detectors and on-chip image processing. Thermal cameras are categorized into two types: cooled and uncooled. Currently, the thermal sensitivity of the uncooled camera is about 0.05°C in comparison to 0.01°C in the cooled ones, which will provide better detail. The cooled cameras have a very fast capture rate and have greater magnification capabilities than uncooled cameras due to sensing shorter infrared wavelengths, and they are able to easily perform spectral filtering. However, the uncooled cameras have some advantages that are useful for this application of perforator mapping; they are compact, portable, light weight, less maintenance, and inexpensive compared to cooled cameras. Although the cooled infrared thermal cameras have a greater thermal sensitivity, the uncooled IR thermal cameras have a high enough thermal sensitivity and spatial resolution, which makes them usable for this application. There have been great results reported by using a smartphone-based thermal camera [11]. It is important for the postprocessing procedure to select a thermal camera with features for storing both thermal and visual images [29]. Cameras used by other research groups for medical applications are tabulated in Table 2.

Tables Icon

Table 2. IR Cameras Used for Different Studies by Various Research Groups for Medical Thermography Experiments

B. Display Device and Image Processing Unit

Display and image processing are done digitally using a computer or laptop and dedicated software packages. A connection between the thermal camera and the computer enables the possibility for real-time measurements and postprocessing. This results in a reduction of surgery time.

C. Transient Measurement Equipment

In order to perform a transient measurement, equipment for stimulating the tissue is necessary. The meaning of stimulation is to create a temperature difference between the blood supply and the tissue. There are several studies [7,911,29,31,3941] available that include cold and heat stimulation. The most common techniques are as follows:

  • • blowing air at room temperature (desktop fan) [10,11,31],
  • • blowing cooled air with the use of a cooling unit [7],
  • • applying cold water packs [13],
  • • applying an alcohol-based solution in combination with blowing air [41],
  • • halogen lamps [7], and
  • • using hemostatic clamps to block blood flow (peroperative) [13].

Some of these techniques are not tolerated during surgery because they are nonsterile, which results in additional risks for the patient. The high need for standardization of stimulation methods for transient measurements has been countered by Thiessen et al. [13].

6. MEASUREMENTS ON DIEP FLAPS: METHOD

The camera used for the thermal images is a Xenics Gobi 640 microbolometer $640 \times 480]$, NETD 30 mK, 50 Hz, with a 7.5–14 µm spectral range. This is an uncooled, long-wavelength microbolometer camera and is chosen because of its compact size, high image resolution, and precision at relatively low temperature measurements [13]. The performed measurements during breast reconstruction with the used thermal camera delivers an image sequence (3D-matrix) shot at ca 6.25 Hz [42]. A frame rate of 6.25 Hz is used to clearly visualize the emerging hot spots. The format of the data set is a three-dimensional matrix $[ {m \times n \times o} ]$ with $m$ pixels width, $n$ pixels height, and $o$ frames. The measuring unit is degrees Celsius. No absolute temperatures are measured; only temperature differences are displayed, so calibration of the thermal camera is not necessary.

The measurements are divided into three sections: pre-, per--, and postoperative. Each section of measurement has a different purpose as shown in the list below [43].

  • • Preoperative: Pinpoint the exact location of the dominant perforators.
  • • Peroperative: Mapping the specific influence of each perforator on the abdominal flap regarding blood supply as well as defining the perfused area of the flap after transplantation. Monitoring of perfusion after anastomosis and flap inset.
  • • Postoperative: Examining whether or not thermal images can give an early warning to avoid partial or complete necrosis (thrombosis).

A. Preoperative Measurements: External Cooling

The purpose of the preoperative measurement is to accurately determine the location of the dominant perforators. Therefore, an ideal thermal image for this section would be one with few but obvious hot spots. The reduction of the so-called “fake hot spots” is critical for the accuracy of this method. “Fake hot spots” are small areas where superficial blood vessels give the impression of an underlying perforator [13]. To obtain this ideal image, cooling was applied to make the hot spots narrower and to reduce the so-called fake hot spots[44]. Further research has to be done to reduce the number of fake hot spots.

The following criteria are involved when determining the most suitable perforators:

  • • The perforator has a well-developed branching pattern right after passing through the abdominal muscles and the fascia [45]. This usually ensures that the perforator perfuses enough tissue of the abdominal flap.
  • • The diameter of the perforator must be large enough. This ensures a sufficient flow of blood to perfuse a large enough area of the abdominal flap.
  • • The way the perforator passes through the rectus abdominis muscle determines the dissection time. The surgeons tend to choose perforators that lie near the medial line and close to the umbilicus [46].

In Fig. 2 the most explicit hot spots are encircled in red. The locations where the perforators pass through the fascia according to the CTA images are represented. The actual CTA images are slices right above and parallel to the fascia (anterior rectus sheath). The black circles on the drawings represent the umbilicus. On the actual CTA images, the umbilicus is represented by a white circle. The umbilicus makes linking of the images possible. During the measurements, the abdomen is cooled with a sterile plastic bag filled with ice and water [Fig. 1(b)] [13]. By comparing the locations of the hot spots, right after cooling, with the locations of the perforators as seen on the CTA, we can investigate the accuracy of the method used. The surgeon marked the best-suited perforators (according to his judgement) with a cross on the schematic drawings [Fig. 2(e)]. The blue crosses are the perforators that were clamped off in the peroperative measurements [43].

B. Peroperative Measurements

The peroperative measurements for mapping the influence of a specific perforator will determine which areas of the abdominal flap will be perfused by which dominant perforator (e.g., Fig. 3). This information can influence the choice of considered perforators. This, of course, in a situation where there are multiple perforators. The best-suited perforators can appear to have similar properties on the CTA, yet their heated areas of the abdominal flap will have a different surface area. The perforator that perfuses the largest part of the abdominal flap is most likely to be chosen for transplantation. Currently, the choice of which area of the abdominal flap is used for transplantation is a clinical evaluation based on the CTA images and the experience of the surgeon. As described by Hembd et al. up to 14.4% had flap fat necrosis [47,48]. Thus, there is room for optimization in determining which part of the flap is well perfused through the selected perforator and which part of the flap is safe to use. The surgeons do not exactly and with certainty know the maximum surface area perfused by the chosen perforators when examining the CTA images [43].

Before transplantation, the best-suited perforator that most likely perfuses the largest part of the abdominal flap is chosen to be anastomosed. After anastomosis, the blood flow in the DIEP flap can be checked with DIRT to verify if the flap is properly vascularized to reduce the chance of necrosis.

C. Postoperative Measurements

One to two days after the surgery, a static image of the reconstructed breast and a dynamic recording after the introduction of a cold challenge are taken as can be seen in Fig. 4. With those two measurements there is a possibility that the IR camera can visualize potential necrotic area(s), due to arterial or venous thrombosis, before clinical observation [49]. Further research has to be done in the postoperative phase and is not further discussed in this article.

 figure: Fig. 2.

Fig. 2. Preoperative measurement. The cooling was done with a plastic bag filled with ice and water. This bag was draped and slightly pressed. (a) Right after cooling the bag was removed. (b) After 4 min of rewarming. (c) Location of the potentially suitable perforators seen on the CTA. (d) Visualization of the quick and strong branching pattern of perforator B. (e) Schematic representation of the perforator.

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D. Postprocessing

The peroperative measurements take place during several phases of the surgery. The surgeon needs instant feedback on the measurements of the DIEP flaps without obstructing the time window of the surgery. No real-time postprocessing for determining hot spots and perforators has been tested yet as discussed further in this article. The real-time acquired image sequence is visualized with the “Xeneth64” software delivered by the manufacturer of the IR camera Xenics Gobi 640 microbolometer $640\times 480$. The chosen color profile is 16-bit grayscale, and the temperature scale as well as the range to the histogram thresholds has been adjusted to fit the measured temperatures and data.

7. RESULTS AND DISCUSSION

A. Preoperative Measurements

Perforators A1 and A2 in Fig. 2 originate from the same pedicle and could potentially be used together when sacrificing the muscle. Perforators A1 and A2 emerge both from the deep inferior epigastric artery and vein. They can be used together to vascularize the DIEP flap but means that the surgeon has to sacrifice a part of the muscle. The two perforators (A1 and A2) can be correlated with the two hot spots in Fig. 2, namely, the upper hot spot just above the umbilicus and the lowest hot spot. Perforator B swiftly splits into two branches and curves sharply to the anatomical left side as seen in Fig. 2. This matches with the thermal image after 4 min of rewarming; see Fig. 2. Eventually, perforator B was chosen for its well-developed branching pattern and therefore its large perfused area.

 figure: Fig. 3.

Fig. 3. Peroperative measurement. The influence of perforator A on the flap can be deduced by subtracting the influence of perforator B in subfigure (a). Perforator B was eventually chosen for transplantation because its heated and subsequently perfused area was much larger than the heated c.q. perfused area of perforator A. (a) Perforators A and B ${\sim} 4\,\,{\rm min}$ after the clamp was removed. (b) Only perforator B ${\sim} 4\,\,{\rm min}$ after the clamp was removed.

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B. Peroperative Measurements

1. Peroperative Measurements with Hemostatic Clamps

After dissection of the DIEP flap with the perforators still connected, blood flow can be controlled in the different parts of the flap by closing and opening perforators with the help of hemostatic clamps. In Fig. 5, the region vascularized by A is clearly noticeable. At time stamp zero, perforator A is opened, and the evolution is tracked for 5 min. It can be noticed that the bottom part of the flap cools down, the top and middle part of the flap is vascularized by perforator A, and the temperature increased and stabilized.

 figure: Fig. 4.

Fig. 4. Postoperative image of the reconstructed breast one day after surgery. The IR camera can visualize potential necrosis.

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In a different case (Fig. 3), when the clamps on perforator A and B are removed and steady-state conditions are achieved after 4 min, it can be seen that both perforators together vascularize the flap well. When perforator B is opened while keeping perforator A closed, one can notice the region that is perfused by perforator B. The effect of opening a perforator can clearly be visualized by looking at the thermal measurement at different moments in time.

 figure: Fig. 5.

Fig. 5. Thermal measurements with the left flap in rest and perforator A open. (a) Measurement at time zero. (b) Measurement at 8 min. (c) Measurement at 15 min.

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2. Peroperative Measurements After Anastomosis to the Mammary Artery and Veins

As illustrated in the steady-state images in Fig. 6, it becomes possible to distinguish the colder from the warmer areas on the abdominal flap. The warmer areas indicate blood perfusion and thus a minimal chance of necrosis after transplantation. It now becomes possible to paste red lines onto the steady-state images, which will mark the separation line between the warmer and the colder areas caused by the chosen connected perforator. However, defining the well-perfused area has to be done by analyzing the reheating process over the ${\sim} 5\,\,{\rm min}$ following the clamp removal after anastomosis has been completed. This will ensure that the visualized temperature difference on the thermal images is solely produced by the reintroduction of warm blood. Only a steady-state image will be able to indicate the different surface areas. This is because of the conductive heating of the flap by perfusion. These thermal images could help the surgeon to decide which parts of the abdominal flap to use for the actual reconstruction of the breast.

 figure: Fig. 6.

Fig. 6. Perfused area of DIEP flap after anastomosis of the DIEP flap has been completed. The red line displays sufficient and insufficient perfused areas in the DIEP flap. (a) Peroperative measurement 1: perforator B was connected to the chest artery. This image depicts the flap as steady state 5 min after blood flow was reintroduced and indicates the maximal surface area of the flap that could safely be used for reconstruction. (b) Peroperative measurement 2: only the small upper right part of the considered flap does not seem to warm up in the 5 min after clamp removal. Therefore, this part of the flap has the most chance of developing partial necrosis. (c) Peroperative measurement 3: the blue line in this image represents where the surgeon made the cut. After the dynamic analysis of the sequence of thermal images, the red line was drawn onto the division between the parts that reheated and the parts that did not. The upper enclosed area defines the area that was cut off, even though it was perfused. The lower enclosed area represents a preserved section that will have a chance of necrosis. (d) Peroperative measurement 4: the warmer/whiter areas outside of the red lines do not have a temperature change throughout the 5 min measuring time. This implies that these areas have been warmed by external factors, e.g.,  conduction of body heat, the surgeon’s hands, etc.

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8. CONCLUSION

From the presented initial results in this pilot study based on a small amount of patient samples, one can conclude that infrared thermography offers extra information on the location of the perforators and its vascularization pattern. In the future, DIRT can be a promising alternative to CTA for preoperative perforator mapping in DIEP flap breast reconstruction. In this pilot study, the enhanced preoperative measurement results obtained using our standardized measurement setup [13] are in accordance with the published results by de Weerd et al. [31]. However, in this initial study, particular emphasis is placed on peroperative measurements with our improved and standardized measurement setup during surgery. The measurements are interesting and deliver promising results to assist the surgeon. A large clinical study is needed in order to reveal how far one can go with IR thermography for identifying perforators in an accurate manner. Also, during surgery, IR thermography can identify which zone of the free flap is to be used for the reconstruction, depending on the level of bleed through the flap.

The correlation between the best-suited perforators and hot spots should be determined as well as the correlation between the hot spots on the thermal images and the perforator locations seen on the CTA images. Additionally, IR thermography clearly visualizes the perforators that have the largest perfusion area. A large supply of blood is only one of the main criteria used when determining the most suitable perforators for transplantation. Perforators that have an extremely well-developed branching pattern may be invisible right after the cooling is removed; however, they will start to reappear in the moments following the removal of the cold challenge.

The applied techniques can be used to determine the location of the dominant perforators. A prominent hot spot does not always equal a dominant perforator. Furthermore, it is impossible to pinpoint the exact location of where the perforator passes through the fascia. This is due to the anatomy of the perforators and the fact that thermal cameras only measure the superficial temperatures. There is an inseparable link between the depth of the perforator and its visibility on thermal images because these measurements are superficial. The deeper parts of the perforator, when the perforator does not go straight up, will have to warm up more abdominal tissue before they become visible on the thermal images.

A. Need for Postprocessing

It becomes obvious that the heat development of the hot spots over a certain time is a determining factor as well as the expansion rate of the warmed-up surface area with the hot spot as the source. Therefore, the image right after the removal of cooling does not represent the entire result of the test. In most cases, a static comparison between the images, taken a certain time apart, will not be sufficient to determine the most dominant perforator(s). Consequently, a need for dynamic analysis of the series of images arises. Through postprocessing, the visualization of the data can be optimized and compressed. This allows easy analysis and use of the measured thermal images by nonexperts in the field of thermography.

The mapping of the influence of the different dominant perforators over a set time (5 min) has proven to be a useful tool. The thermal images provide the individual influence of each perforator on the flap as well as the dimensions of the perfused area. This additional information is an asset when determining the best-suited perforator(s) for transplantation. The visual separation between the warmer, perfused area and the colder area can visualize the sections that will possibly develop necrosis just by analyzing a 5 min measurement. This easy, noninvasive technique can minimize the chances of partial necrosis. In conclusion, the noninvasive thermal measurements provide the surgeon with real-time visualization of the considered perforators and their influence on the flap. This additional information can definitely optimize the choices made regarding the selection of the best-suited perforator and the determination of the maximal perfused area of the flap.

Funding

Universiteit Antwerpen (HBC.2017.0032, PSID-34924).

Acknowledgment

The authors thank Ralv Lundahl, Yarince Dirkx, and the UZA medical and technical staff, especially Fons Van Dijck, for the support on the preliminary measurements. Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. Ethical approval has been obtained from ethics committee. Belgian registration: B300201941125.

Disclosures

The authors declare no conflicts of interest.

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Figures (6)

Fig. 1.
Fig. 1. Measurement setup to perform IR thermography measurements on a DIEP flap. (a) Measurement setup with a long-arm tripod [13]; (b) cooling method with a sterile plastic bag filled with ice and water [13].
Fig. 2.
Fig. 2. Preoperative measurement. The cooling was done with a plastic bag filled with ice and water. This bag was draped and slightly pressed. (a) Right after cooling the bag was removed. (b) After 4 min of rewarming. (c) Location of the potentially suitable perforators seen on the CTA. (d) Visualization of the quick and strong branching pattern of perforator B. (e) Schematic representation of the perforator.
Fig. 3.
Fig. 3. Peroperative measurement. The influence of perforator A on the flap can be deduced by subtracting the influence of perforator B in subfigure (a). Perforator B was eventually chosen for transplantation because its heated and subsequently perfused area was much larger than the heated c.q. perfused area of perforator A. (a) Perforators A and B ${\sim} 4\,\,{\rm min}$ after the clamp was removed. (b) Only perforator B ${\sim} 4\,\,{\rm min}$ after the clamp was removed.
Fig. 4.
Fig. 4. Postoperative image of the reconstructed breast one day after surgery. The IR camera can visualize potential necrosis.
Fig. 5.
Fig. 5. Thermal measurements with the left flap in rest and perforator A open. (a) Measurement at time zero. (b) Measurement at 8 min. (c) Measurement at 15 min.
Fig. 6.
Fig. 6. Perfused area of DIEP flap after anastomosis of the DIEP flap has been completed. The red line displays sufficient and insufficient perfused areas in the DIEP flap. (a) Peroperative measurement 1: perforator B was connected to the chest artery. This image depicts the flap as steady state 5 min after blood flow was reintroduced and indicates the maximal surface area of the flap that could safely be used for reconstruction. (b) Peroperative measurement 2: only the small upper right part of the considered flap does not seem to warm up in the 5 min after clamp removal. Therefore, this part of the flap has the most chance of developing partial necrosis. (c) Peroperative measurement 3: the blue line in this image represents where the surgeon made the cut. After the dynamic analysis of the sequence of thermal images, the red line was drawn onto the division between the parts that reheated and the parts that did not. The upper enclosed area defines the area that was cut off, even though it was perfused. The lower enclosed area represents a preserved section that will have a chance of necrosis. (d) Peroperative measurement 4: the warmer/whiter areas outside of the red lines do not have a temperature change throughout the 5 min measuring time. This implies that these areas have been warmed by external factors, e.g.,  conduction of body heat, the surgeon’s hands, etc.

Tables (2)

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Table 1. Experimental Conditions Used by Various Research Groups for Recording of Infrared Thermal Images [6]

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Table 2. IR Cameras Used for Different Studies by Various Research Groups for Medical Thermography Experiments

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