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00004032-201208000-0001500004032_2012_103_204_chu_effusivity_2review< 81_0_10_4 >Health Physics©2012Health Physics SocietyVolume 103(2)August 2012p 204–209Thermal Effusivity: A Promising Imaging Biomarker to Predict Radiation-Induced Skin Injuries[REVIEW ARTICLES]Chu, James*; Sun, Jiangang†; Templeton, Alistair*; Yao, Rui*; Griem, Katherine**Rush University Medical Center, Chicago, IL 60612; †Nuclear Engineering Division, Argonne National Laboratory, Argonne, IL 60439.The authors declare no conflict of interest.For correspondence contact: James Chu, Rush University Medical Center, Chicago, IL 60612, or email at jchu@rush.edu.(Manuscript accepted 19 December 2011)AbstractAbstract: An effective screening technology is needed to triage individuals at the time of radiation incidents involving a large population. Three-dimensional thermal tomography is a relatively new development in active thermal imaging technology that produces cross-sectional images based on the subject’s ability to transfer heat—thermal effusivity—at the voxel level. This noninvasive imaging modality has been used successfully in nondestructive examination of complex materials; also it has been shown to predict the severity of radiation-induced skin injuries several days before the manifestation of severe moist desquamations or blister formation symptoms in mice at 40 Gy. If these results are confirmed at lower dose levels in human subjects, a thermal tomography imaging device may be an ideal screening tool in radiation emergencies. This imaging method is non-invasive, relatively simple, easily adaptable for field use, and when properly deployed, it will enhance public emergency preparedness for incidents involving unexpected radiation exposure.INTRODUCTIONFOLLOWING A large-scale radiation disaster, such as a nuclear power plant incident or a “dirty bomb” terrorist attack, many individuals who are or suspected to be exposed will come to hospitals to seek evaluation or treatment. With limited resources available, these hospitals will be easily overwhelmed by the sheer number of people seeking medical services. It is therefore crucial to have evaluation technologies that can rapidly identify the individuals who are at risk of developing clinically important and treatable acute radiation injury so appropriate resources are used where most in need (Flynn and Goans 2006), but a fast and effective technology for this purpose is not yet available. Development of new technologies that provide rapid screening of a population suspected to be exposed to radiation is important to meet the demand during these disastrous events. The authors propose the development of an infrared-based imaging device for skin that can quickly screen a large patient population and identify the subgroup of patients who will develop severe radiation-induced skin reactions after a radiological/nuclear mass exposure event. This capability will triage patients based on the individual patient’s clinical needs and provide an effective tool to properly allocate resources to treat the most affected individuals in a timely manner. When successfully developed and deployed, the device will greatly improve public emergency preparedness.RADIATION-INDUCED SKIN REACTIONSRadiation-induced skin reactions were recognized more than a century ago, and a large body of research at the clinical and molecular levels has been reported on animal and human models (Denham and Hauer Jensen 2002; Hymes et al. 2006). This topic continues to be an area of active research as radiation-induced skin injury is still one of the dose limiting complications in many radiation therapy regimens, and many biological factors are involved in the acute and late expressions of radiation-induced skin injury. For individuals accidently exposed to radiation, the severity of radiation damage to skin is also a key diagnostic and prognostic factor, especially in situations involving radiation-induced multi-organ failure/injuries (RIMOF). It is suggested that a radiation exposure may be fatal when the radiation-induced skin injury exceeds a certain level of damage, and the chance for RIMOF decreases when the skin injury is treated successfully. Although details of the pathophysiological process of RIMOF are not well understood, it is likely that skin injury is a critical factor triggering the failure of other organ systems (Meineke 2005; Prasanna et al. 2010).In addition to its critical roles in diagnosis and treatment of patients involved in accidental radiation exposure, skin is also an attractive potential biodosimeter for the following reasons: It is always in place at the time of radiation exposure, its radiation-induced effects have been studied extensively, it provides information related to nonuniform partial body exposures, it covers the entire body (so that in all but the most extreme accidents, one will have portions of skin undamaged by physical trauma that can be used for screening), and early erythema and cytokine secretion are observed within a few hours after 2–3 Gy of exposure (Hall and Giaccia 2011; Muller and Meineke 2007). Radiation-induced skin injuries may be related to a number of factors, including superficial arteriolar constriction, capillary vessel dilation, microvasculature reduction, intracellular edema, bullae formation, permeability change, inflammation, remodeling of dermal or epidermal structures, and certain genetic properties (Archambeau et al. 1995; Hadad et al. 2010; Benderitter et al. 2010; Schmuth et al. 2001; Balli et al. 2009). However, other than the early erythema mentioned above, overt clinical symptoms of these radiation-induced skin injuries may take days or weeks to manifest, limiting their usefulness in initiating appropriate preventive and supportive treatments early on. A method that predicts the development and severity of radiation-induced skin injuries, therefore, would be a very valuable tool for triage and initial assessment of patients involved in radiological or nuclear threats. These injuries can vary with tissue structure and depth under the surface, and as such, quantitative imaging technologies may be required to best identify and predict pathologic radiation-induced skin effects.INFRARED THERMOGRAPHYThe human body generates heat through various physiological processes that involve tissue metabolism, physical exercise, and other muscular activities. As part of the thermoregulation process to maintain a relatively constant body temperature, some of the heat is given off from the skin. A diseased physiological process or an injury to the tissues may interfere with normal heat generation and thermoregulation processes and alter the pattern of heat emission from the skin. Measuring differences in heat emission from different areas of human skin was described more than 2,000 years ago when Hippocrates placed wet mud on the patient’s surface and examined the color changes while the mud was drying; the mud over a tumor was presumed to dry faster than that over normal tissue (Ring 2006). The modern method of contact thermography uses the same approach, replacing mud with other sensors such as liquid crystal. With the development of infrared technology, non-contact infrared thermography devices have been used in many fields in medicine, including oncology, dermatology, immunology, neurology, rheumatology, orthopedics, and veterinary medicine. As human skin is an efficient radiator in the infrared spectrum, the medical application of infrared thermography covers a wide range of diseases in nearly all disease sites in which skin plays a role. For example, infrared thermography has been used in detection of a variety of diseases such as, among others, breast cancer, gastric cancer, inflammation, vascular/arterial disorders, osteoarthritis, tendonitis, allergic skin reactions, and severe acute respiratory syndrome (SARS) infection (Ring 2006; Keyserlingk et al. 2000; Button et al. 2004; Rokita et al. 2011; Di Carlo 1995; Turner 2001).Early methods, including thermography, used to measure radiation dose in skin and subcutaneous tissues were reviewed (Daburon 1986). Infrared and contact thermography were shown to detect significant temperature rise in irradiated regions in humans earlier than the appearance of clinical signs in the early 1980s. These studies also reported close correlation between the isotherm and isodose curves. A later study, however, confirmed these findings only for high doses of γ (gamma) rays but not for lower dose γ irradiations or β (beta) irradiation, even in those with skin erythema (Lefaix and Daburon 1998). A separate study, however, reported detection of temperature changes at about 30 min after low doses of 2.5 Gy electron beam irradiation (Koteles et al. 1998). In addition, both hypothermic and hyperthermic regions, corresponding to areas of necrosis and inflammation respectively, were observed when thermography was used to examine victims from a 137Cs radiation accident in Georgia (Gottlöber et al. 2000). Some of these apparent inconsistent thermographic observations are probably due to a number of imaging device and patient physiology-related factors, including system instability and reproducibility, limited detector temperature ranges, spectral and spatial resolution limitations, length of patient acclimatization, lack of standard protocol that may lead to inter-observer variations, spurious background infrared radiation, and other environmental and endogenous factors (Zaproudina et al. 2008; Buzug et al. 2006).Recent advances in infrared sensor and computer technologies have led to thermography systems with excellent performance at reasonable prices. For example, a typical “off-the-shelf” system may provide 515 × 512 pixels resolution, 5–300°C temperature range, 30 mK sensitivity, μs to ms of integration time, and frame rate of more than 100 Hz. These improved capabilities allow effective implementation of active dynamic thermo-imaging, in which the surface temperature of the object is recorded over time after the application of stimuli. This is in contrast to the conventional passive thermo-imaging in which the map of surface temperature distribution of an object is recorded without any external stimulation. The external stimulation can be a pulse with either a reduced or elevated temperature applied over a certain length of time. The active thermo-imaging methods have been shown to improve sensitivity and reproducibility and have been successfully used for nondestructive evaluation of materials (Maldaque and Moore 2001). A theoretical study based on the bioheat transfer equation and a layered skin model suggests that analysis of transient temperature variations can help detect lesions under the skin (Pirtini Centingul and Herman 2008). Another study suggests that the relative temperature rise measured after 2 min of 15°C cold stimuli correlates with radiation-induced skin changes for patients receiving boron neutron capture therapy for cutaneous malignant melanoma (Santa Cruz et al. 2009). This technique required no absolute temperature calibration or predetermined gain and offset values for the camera.THREE-DIMENSIONAL THERMAL TOMOGRAPHY (3DTT)Three-dimensional thermal tomography is a special active thermography imaging method that uses a pulsed thermal energy to raise the subject’s surface temperature. Rather than analyzing the surface temperature profiles measured over time, 3DTT reconstructs cross-sectional images of the object based on the physical properties at the local voxel level. It is analogous to a computed tomography (CT) in which the grey scale level of the image is related to the local electron density; the image from 3DTT is related to local thermal effusivity (Sun 2007). Thermal effusivity is an intrinsic thermal property; it is defined as e = (ρck)1/2 , where ρ is density, c is specific heat, and k is thermal conductivity.This principle of 3DTT has been described (Sun 2008), and this technology has been used successfully in nondestructive evaluation (NDE) of advanced materials and structural components (Sun 2007). As an example, Fig. 1 shows the structure diagram and NDE thermal tomography images for of a 2.5 mm thick SiC ceramic-composite plate, in which seven flat-bottom holes were machined from the back surface (the hidden surface). The diameters of the holes range from 1.0 to 7.5 mm, and the depths of the holes from the front surface range from 0.25 to 1.12 mm. All flat-bottom holes and many smaller air pocket defects (darker spots in Fig. 1b) are resolved in these images. The images of the holes and defects appear to be dark due to the low effusivity value for air. These images demonstrate that 3DTT is capable of resolving detailed 3D structures based on temperature distributions.Fig. 1. Typical 3DTT images for a SiC ceramic plate with flat-bottom holes (A–G) machined at the back surface. The diameters of holes are 7.5 mm for A–D, 5.0 mm for E, 2.5 mm for F, and 1.0 mm for G. The depths of holes from the front surface are 0.25 mm, 1.12 mm, 0.97 mm, 0.87 mm, 0.78 mm, 0.85 mm, and 0.85 mm for A through G, respectively. Shown are one plane effusivity image at 1.2 mm depth (A) and two perpendicular cross-sectional effusivity images (B) with corresponding material diagrams (C) along the two lines marked in the plane image in (A). All flat-bottom holes are clearly visible in images (A) and (B). In addition, small air pocket defects, shown as small dark spots, are visible in image (B).It is expected that similar results would be possible for 3DTT imaging of the skin, as variations in measured thermal effusivity have been shown to reflect the structurally differentiated layers of the skin (Balageas et al. 1986).RODENT SKIN PILOT STUDYWhile 3DTT is a very promising technology, its potential in predicting radiation-induced skin injures has not been tested. The authors conducted a feasibility study using 11 female SKH-1 mice, a hairless strain (Templeton et al. 2010). Mice were housed in an individually ventilated cage rack system in the animal care facility for six weeks and were supplied with high caloric laboratory food and water. All animal experiments were performed in accordance with institutional and governmental guidelines.Each mouse was anesthetized with isoflurane gas (Webster Veterinary Supply, Inc., 137 Barnum Rd., Devens, MA 01434, USA) and exposed to a single dose of 40 Gy to the left hind leg using an 192Ir source via a 1-cm-high dose rate brachytherapy Leipzig applicator (Nucletron Inc., 8671 Robert Fulton Dr., Columbia, MD 21046, USA) whose dosimetry has been extensively characterized by this group (Niu et al. 2004). The 40 Gy dose level was used as it has been shown to produce moist desquamation of the skin in single dose experiments in multiple strains of mice (Hall and Giaccia 2011; Hopewell 1990). Daily 3DTT imaging was then performed for each mouse in a styrofoam template to reproduce the setup geometry, again with the mice under isoflurane sedation. Mice were monitored and skin reactions scored until complete cessation of acute skin reactions using skin toxicity evaluation criteria described previously (Cancer Therapy Evaluation Program; Radiation Therapy Oncology Group). Data from both the irradiated skin area and an unirradiated area of skin (the contralateral hind leg as a control) were recorded and analyzed. Fig. 2 shows the image acquisition set up with the anesthetized mouse placed under the flash lamp and IR camera. The infrared camera captured 3,000 frames of thermal images and recorded the decay of surface temperature for 6 s immediately after a 2.5 ms photographic flash. Daily 3DTT imaging was performed for 25 d after the irradiation. These effusivity imaging data were used to reconstruct effusivity-based cross-sectional images approximately 20 μm thick for the study. As an example, Fig. 3 shows some of the daily 3DTT images for two mice: One developed severe skin reaction moist desquamation (Fig. 3a), and the other only developed erythema and a minor blister (Fig. 3b). These images were reconstructed at approximately 0.2 mm depth. Compared with the unirradiated leg on opposite side, reduced effusivity was observed in the irradiated region, and the mouse developed a severe skin reaction (shown as darker image intensity within the black circle in Fig. 3a). This effect was less obvious in the other mouse, as shown in Fig. 3b. In addition, high effusivity values were observed within the blister, probably due to its higher fluid content. There was also a region of very low effusivity around the blister in the mouse with the severe skin reaction (Fig. 3a).Fig. 2. Daily thermal imaging set-up. The anesthetized mouse is exposed to a brief photographic flash (2.5 ms), after which about 3,000 frames of skin thermographic images are recorded by the IR camera (Indigo Systems Corp., now FLIR Systems Inc.) for approximately 6 s.Fig. 3. Thermal tomography images at about 0.2 mm depth for two mice with (A) and without (B) development of severe skin reaction moist desquamation. The slice thickness is approximately 20 μm. The effusivity decreases in the irradiated region (within the black circle) compared with the unirradiated region on the contralateral side (served as control). This decrease is more apparent in the mouse in (A) compared with that in (B). The blister in (A) also shows high effusivity surrounded by a region of very low effusivity.3DTT data from depths of 0.2 to 0.6 mm were grouped for analysis. The daily averages of the normalized deviation of the treated from the control regions were calculated and reported as the relative average effusivity deviation (RAED = [<control> − <treated>] / <control>). SPSS for Windows (Version 14) was used for data management and statistical analysis. Data from skin measurements were not normally distributed, and nonparametric statistical methods were used. The Mann-Whitney test was used to compare the high grade (wet-desquamation) and low grade (non-wet desquamation) groups with respect to RAED measurements. Sensitivity (true positive / [true positive + false negative]) and specificity (true negative / [true negative + false positive]) were also calculated.It was found that six mice developed evidence of moist desquamation with severe blister formation between days 11 and 14 post-radiation (high grade group), while the remainder (n = 5) exhibited less severe skin reactions ranging from erythema to dry desquamation (low grade group). These observed differences in skin effects are to be expected, as an individual’s response to radiation may depend on many factors such as age, body size, health and immune status, and genetic predisposition, among others (Archambeau et al. 1995; Hopewell 1990; Hymes et al. 2006; Porock and Kristjanson 1999; Coia and Moylan 1991). As shown in Fig. 4, the RAED of both groups was similar over the first day post-radiation, with a mean close to 0.0% for both groups (p = NS). Larger differences in RAED between the two groups started developing 2 and 3 d post-radiation, and progressive increases continued until day 5, reaching a mean of 15.6% for the high grade group and −5.1% for the low grade group. The difference on day 5 was highly significant (p < 0.001 by univariable logistic regression) with nearly perfect sensitivity and specificity.Fig. 4. Mean change in relative effusivity for high and low grade skin reaction groups. The relative effusivity deviation was calculated as a ratio: (mean effusivity at control side−mean effusivity at treated side)/control side. Marked changes in thermal effusivity of irradiated skin occurred in the high grade group well in advance of the development of skin reactions. The difference was statistically significant, with nearly perfect sensitivity and specificity.CONCLUSIONWith the widespread use of nuclear power and radioactive materials and the potential risk of terrorist attack, unexpected radiation exposure to a large population is a realistic threat. There is a need for an effective triage tool that can screen a large number of individuals in the field and help prioritize allocation of resources during such an event. Skin thermal effusivity is an attractive potential biomarker for this triage purpose, as it plays a critical role in both diagnosis and treatment of radiation-induced injuries. These preliminary data show that 3DTT skin images predict the severity of radiation-induced skin damage in mice at 40 Gy with excellent sensitivity and specificity. These experimental results are very encouraging and should be repeated for lower doses and on human skin. If confirmed in human subjects, 3DTT imaging of the skin will enhance the ability to triage radiation victims based on their clinical needs and improve public emergency preparedness at the time of a radiation accident.AcknowledgmentsThis work was supported in part by a research grant from the Brian Piccolo Research Fund.REFERENCES Archambeau JO, Pezner R, Wasserman T. Pathophysiology of irradiated skin and breast. Int J Radiat Oncol Biol Phys 31: 1171–1185; 1995. [CrossRef] [Medline Link] [Context Link] Balageas DL, Krapez JC, Cielo P. Pulsed photothermal modeling of layered materials. J Appl Phys 59: 348–357; 1986. 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