Infrared Thermography in Exercise Physiology: The Dawning of Exercise Radiomics

Infrared thermography (IRT) is a non-invasive tool to measure the body surface radiation temperature ( T sr ). IRT is an upcoming technology as a result of recent advancements in camera lenses, detector technique and data processing capabilities. The purpose of this review is to determine the potential and applicability of IRT in the context of dynamic measurements in exercise physiology. We searched PubMed and Google Scholar to identify appropriate articles, and conducted six case experiments with a high-resolution IRT camera (640 × 480 pixels) for complementary illustration. Ten articles for endurance exercise, 12 articles for incremental exercise testing and 11 articles for resistance exercise were identified. Specific T sr changes were detected for different exercise types. Close to physical exertion or during prolonged exercise six recent studies described “tree-shaped” or “hyper-thermal” surface radiation pattern ( P sr ) without further specification. For the first time, we describe the T sr and P sr dynamics and how these may relate to physiological adaptations during exercise and illustrate the differential responsiveness of P sr to resistance or endurance exercise. We discuss how bias related to individual factors, such as skin blood flow, or related to environmental factors could be resolved by innovative technological approaches. We specify why IRT seems to be increasingly capable of differentiating physiological traits relevant for exercise physiologists from various forms of environmental, technical and individual bias. For refined analysis, it will be necessary to develop and implement standardized and accurate pattern recognition technology capable of differentiating exercise modalities to support the evaluation of thermographic data by means of radiomics.

[1]  E. Ring,et al.  The Application of Medical Infrared Thermography in Sports Medicine , 2012 .

[2]  D. Weese-Mayer,et al.  Determining peripheral skin temperature: subjective versus objective measurements , 2016, Acta paediatrica.

[3]  A. Tonevitsky,et al.  The human thermal portrait and its relations with aerobic working capacity and the blood lactate level , 2010, Human Physiology.

[4]  Y. Ootsuka,et al.  Control of cutaneous blood flow by central nervous system , 2015, Temperature.

[5]  Jing Liu,et al.  Mathematical modeling of temperature mapping over skin surface and its implementation in thermal disease diagnostics , 2004, Comput. Biol. Medicine.

[6]  J. I. Priego Quesada,et al.  Multifactorial cycling performance of Cyclists and Non-Cyclists and their effect on skin temperature , 2017, Journal of Thermal Analysis and Calorimetry.

[7]  Glenn J Tattersall,et al.  Infrared thermography: A non-invasive window into thermal physiology. , 2016, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[8]  Yazhu Chen,et al.  A high-resolution three-dimensional far-infrared thermal and true-color imaging system for medical applications. , 2009, Medical engineering & physics.

[9]  J. I. Priego Quesada,et al.  Relationship between skin temperature and muscle activation during incremental cycle exercise. , 2015, Journal of thermal biology.

[10]  Gian Luca Romani,et al.  Thermal Imaging of Cutaneous Temperature Modifications in Runners During Graded Exercise , 2009, Annals of Biomedical Engineering.

[11]  Andrew C. Fry,et al.  Resistance Exercise Overtraining and Overreaching , 1997, Sports medicine.

[12]  Aaron J. E. Bach,et al.  The effect of using different regions of interest on local and mean skin temperature. , 2015, Journal of thermal biology.

[13]  Ian B. Stewart,et al.  A Comparison between Conductive and Infrared Devices for Measuring Mean Skin Temperature at Rest, during Exercise in the Heat, and Recovery , 2015, PloS one.

[14]  Eduardo Borba Neves,et al.  Effect of body fat and gender on body temperature distribution. , 2017, Journal of thermal biology.

[15]  Marco Gargano,et al.  Dynamics of thermographic skin temperature response during squat exercise at two different speeds. , 2016, Journal of thermal biology.

[16]  João Carlos Bouzas Marins,et al.  Classification of factors influencing the use of infrared thermography in humans: A review , 2015 .

[17]  J. Williamson.  Autonomic responses to exercise: Where is central command? , 2015, Autonomic Neuroscience.

[18]  A. Caumo,et al.  Thermal Imaging of Exercise-Associated Skin Temperature Changes in Trained and Untrained Female Subjects , 2013, Annals of Biomedical Engineering.

[19]  M. Kume,et al.  The influence of internal and skin temperatures on active cutaneous vasodilation under different levels of exercise and ambient temperatures in humans , 2013, International Journal of Biometeorology.

[20]  Victor Machado Reis,et al.  The influence of subcutaneous fat in the skin temperature variation rate during exercise , 2015 .

[21]  Henrique A. Almeida,et al.  Segmentation Algorithms for Thermal Images , 2014 .

[22]  E. B. Akimov,et al.  Skin temperature and lactate threshold during muscle work in athletes , 2011, Human Physiology.

[23]  G. Tanda,et al.  The use of infrared thermography to detect the skin temperature response to physical activity , 2015 .

[24]  M Yamasaki,et al.  Fall in skin temperature of exercising man. , 1992, British journal of sports medicine.

[25]  J. Adamczyk,et al.  USAGE OF THERMOGRAPHY AS INDIRECT NON-INVASIVE METHOD OF EVALUATION OF PHYSICAL EFFICIENCY. PILOT STUDY , 2014 .

[26]  N. Nitzsche,et al.  Acute Exercise-Associated Skin Surface Temperature Changes after Resistance Training with Different Exercise Intensities , 2018 .

[27]  J. Zieliński,et al.  Changes in body surface temperature during speed endurance work-out in highly-trained male sprinters , 2016 .

[28]  V. Reis,et al.  Using skin temperature and muscle thickness to assess muscle response to strength training , 2015 .

[29]  G. Kenny,et al.  Considerations for the measurement of core, skin and mean body temperatures. , 2014, Journal of thermal biology.

[30]  I. Cuevas,et al.  Reliability and reproductibility of skin temperature of overweight subjects by an infrared thermograpy software designed for human beings , 2012 .

[31]  G. Tanda.  Total body skin temperature of runners during treadmill exercise , 2018, Journal of Thermal Analysis and Calorimetry.

[32]  I M Braverman,et al.  The cutaneous microcirculation. , 2000, The journal of investigative dermatology. Symposium proceedings.

[33]  W. Bertucci,et al.  Efficiency and Thermography in Cycling during a Graded Exercise Test , 2015 .

[34]  A. Tonevitsky,et al.  Thermal "portrait" of sportsmen with different aerobic capacity , 2012 .

[35]  Nisha Charkoudian,et al.  Mechanisms and modifiers of reflex induced cutaneous vasodilation and vasoconstriction in humans. , 2010, Journal of applied physiology.

[36]  Michael Unger,et al.  Automatic detection of perforator vessels using infrared thermography in reconstructive surgery , 2018, International Journal of Computer Assisted Radiology and Surgery.

[37]  Michel Saint-Cyr,et al.  The Perforasome Theory: Vascular Anatomy and Clinical Implications , 2009, Plastic and reconstructive surgery.

[38]  Ermanno Rampinini,et al.  Bilateral asymmetry of skin temperature is not related to bilateral asymmetry of crank torque during an incremental cycling exercise to exhaustion , 2018, PeerJ.

[39]  D L Kellogg,et al.  Control of internal temperature threshold for active cutaneous vasodilation by dynamic exercise. , 1991, Journal of applied physiology.

[40]  O. Airaksinen,et al.  Reproducibility of infrared thermography measurements in healthy individuals , 2008, Physiological measurement.

[41]  T. Salvini,et al.  Exercise-Associated Thermographic Changes in Young and Elderly Subjects , 2008, Annals of Biomedical Engineering.

[42]  Walmir M. Caminhas,et al.  A Combined Method for Segmentation and Registration for an Advanced and Progressive Evaluation of Thermal Images , 2014, Sensors.

[43]  R. Gemperli,et al.  Endothelial Function in Skin Microcirculation , 2018 .

[44]  Atsumasa Yoshida,et al.  Thermal responses and perceptions under distinct ambient temperature and wind conditions. , 2015, Journal of thermal biology.

[45]  Vincent P. Ferrera,et al.  Long-Term Safety of Repeated Blood-Brain Barrier Opening via Focused Ultrasound with Microbubbles in Non-Human Primates Performing a Cognitive Task , 2015, PloS one.

[46]  Samuel Sideman,et al.  Dynamic Thermography: Analysis of Hand Temperature During Exercise , 1998, Annals of Biomedical Engineering.

[47]  M. Venus,et al.  Basic physiology of the skin , 2010 .

[48]  Katsuyuki Arai,et al.  Use of Recovery-enhanced Thermography to Localize Cutaneous Perforators , 1995, Annals of plastic surgery.

[49]  Y. Matsumoto,et al.  Pure Skin Perforator Flaps: The Anatomical Vascularity of the Superthin Flap , 2018, Plastic and reconstructive surgery.

[50]  José González-Alonso,et al.  Human thermoregulation and the cardiovascular system , 2012, Experimental physiology.

[51]  D. Delorey,et al.  Sympathetic Vasoconstriction in Skeletal Muscle: Adaptations to Exercise Training , 2016, Exercise and sport sciences reviews.

[52]  W. Bertucci,et al.  Thermoregulation during incremental exercise in masters cycling , 2014 .

[53]  M. Chudecka,et al.  Thermal maps of young women and men , 2015 .

[54]  G. I. Taylor,et al.  The Anatomical (Angiosome) and Clinical Territories of Cutaneous Perforating Arteries: Development of the Concept and Designing Safe Flaps , 2011, Plastic and reconstructive surgery.

[55]  M. Sillero-Quintana,et al.  Circadian and gender differences in skin temperature in militaries by thermography , 2015 .

[56]  Čoh Milan,et al.  Use of the thermovision method in sport training , 2007 .

[57]  I. Cifuentes,et al.  Augmented reality and dynamic infrared thermography for perforator mapping in the anterolateral thigh , 2018, Archives of plastic surgery.

[58]  Arcangelo Merla,et al.  Skin temperature evaluation by infrared thermography: Comparison of two image analysis methods during the nonsteady state induced by physical exercise , 2017 .

[59]  M. Sillero-Quintana,et al.  Skin temperature changes after exercise and cold water immersion , 2017, Sport Sciences for Health.

[60]  D. Boguszewski,et al.  THERMOGRAPHIC EVALUATION OF LACTATE LEVEL IN CAPILLARY BLOOD DURING POST-EXERCISE RECOVERY , 2014 .

[61]  Bernard Choi,et al.  High-resolution imaging of microvasculature in human skin in-vivo with optical coherence tomography , 2012, Optics express.

[62]  E. Rampinini,et al.  Thermography for skin temperature evaluation during dynamic exercise: a case study on an incremental maximal test in elite male cyclists. , 2016, Applied optics.

[63]  Agnes Psikuta,et al.  Effects of the cycling workload on core and local skin temperatures , 2016 .

[64]  Antonio Crisafulli,et al.  Neural Regulation of Cardiovascular Response to Exercise: Role of Central Command and Peripheral Afferents , 2014, BioMed research international.

[65]  George Havenith,et al.  Body mapping of sweating patterns in male athletes in mild exercise-induced hyperthermia , 2010, European Journal of Applied Physiology.

[66]  Lars Nybo,et al.  Performance in the heat-physiological factors of importance for hyperthermia-induced fatigue. , 2014, Comprehensive Physiology.

[67]  J. Petrofsky,et al.  The use of thermal infra-red imaging to detect delayed onset muscle soreness. , 2012, Journal of visualized experiments : JoVE.

[68]  G. A. Balci,et al.  Analysing visual pattern of skin temperature during submaximal and maximal exercises , 2016 .

[69]  C. Brito,et al.  Skin temperature response to unilateral training measured with infrared thermography , 2017, Journal of exercise rehabilitation.

[70]  You-Gang Yang,et al.  Reconstruction of thermographic signals to map perforator vessels in humans , 2012, Quantitative infrared thermography journal.

[71]  Eduardo Borba Neves,et al.  The effect of body fat percentage and body fat distribution on skin surface temperature with infrared thermography. , 2017, Journal of thermal biology.

[72]  K. Bensalah,et al.  Sunitinib Combined with Angiotensin-2 Type-1 Receptor Antagonists Induces More Necrosis: A Murine Xenograft Model of Renal Cell Carcinoma , 2014, BioMed research international.

[73]  Matthew J. Maley,et al.  Thermographic imaging in sports and exercise medicine: A Delphi study and consensus statement on the measurement of human skin temperature. , 2017, Journal of thermal biology.

[74]  George Havenith,et al.  A method for whole-body skin temperature mapping in humans (Eine Methode zur Aufzeichnung der Hautemperatur des gesamten menschlichen Korpers) , 2012 .

[75]  Jürgen Meixensberger,et al.  Dynamic infrared thermography (DIRT) for assessment of skin blood perfusion in cranioplasty: a proof of concept for qualitative comparison with the standard indocyanine green video angiography (ICGA) , 2017, International Journal of Computer Assisted Radiology and Surgery.

[76]  Anna Lubkowska,et al.  Temperature changes of selected body’s surfaces of handball players in the course of training estimated by thermovision, and the study of the impact of physiological and morphological factors on the skin temperature , 2010 .

[77]  Ciro José Brito,et al.  Regional Skin Temperature Response to Moderate Aerobic Exercise Measured by Infrared Thermography , 2016, Asian journal of sports medicine.

[78]  T. Jayakumar,et al.  Medical applications of infrared thermography: A review , 2012, Infrared Physics & Technology.

[79]  Paul Kinahan,et al.  Radiomics: Images Are More than Pictures, They Are Data , 2015, Radiology.

[80]  Ivo M. V. Felisberto,et al.  Correlation between skin temperature and heart rate during exercise and recovery, and the influence of body position in these variables in untrained women , 2016 .

[81]  Pedro Pérez-Soriano,et al.  Definition of the thermographic regions of interest in cycling by using a factor analysis , 2016 .

[82]  Pablo Casaseca-de-la-Higuera,et al.  Systematic infrared image quality improvement using deep learning based techniques , 2016, Remote Sensing.