Changes in skin temperature induced by the factors causing the activation of non-shivering thermogenesis (NST) were quantitatively described, using dynamic infrared thermography, in 8 physically active men (the mean age was 24.8 ± 4.0 years, body mass index (BMI) was 23.6 ± 0.44) at different body surface locations (the anterior and posterior parts of the neck, the supraclavicular fossae, the sternum, and the interscapular area). During the experiments, the subjects had to undergo, on different days, a glucose-tolerance test, they were locally exposed to cold (feet immersion in water at 0°C for 1 min) and had to perform a single breath-hold test, as well as the aerobic (Ramp) and anaerobic (Wingate) performance tests. The obtained results have shown the presence of thermogenerators, which can cause non-shivering thermogenesis in the human body in response to stimuli of sympathetic and stressogenic origin. A thermogenerator in this context is understood as a cluster of homogeneous cells located subcutaneously or in deeper-laying tissues characterized by elevated heat production whose flow of infrared radiation reaches the body’s surface and shapes a particular thermographic portrait. Deep individual differences have been identified between responses of thermogenerators to the same stimuli. These responses do not differ in synchronicity or intensity and, presumably, depend on a subject's adaptive experience, i.e., on the subject’s life conditions and other epigenetic factors. It has been shown that the thermogenerators located in the supraclavicular region and associated with the brown adipose tissue (BAT) have the highest sensitivity to the tested set of stimuli. A close functional connection has been identified between these thermogenerators and the thyroid gland. Some not at all trivial relationships have been detected between all the studied thermogenerators, and further studies are needed in this area. In particular, we cannot detect any similarities between maximal aerobic and maximal anaerobic exercises in terms of thermogenic response. The glucose response was isolated relative to other stimuli. The data obtained make us think not only about BAT but also about the role of other tissues in energy metabolism regulation. For instance, close attention should be paid to the muscle tissue which has uncoupling protein UCP3. Based on the results, we cannot make an unequivocal conclusion about the nature of investigated thermogenerators. Yet we hope that the widespread usage of non-invasive and safe thermography will allow us to accumulate scientific facts that are necessary to make differential diagnosis for various types of thermogenerators in the human body.
This is a preview of subscription content, log in to check access.
Buy single article
Instant unlimited access to the full article PDF.
Price includes VAT for USA
Kolesov, S.N. and Volovik, M.G., Modern methodology for thermal-vision research and thermal-vision diagnostic apparatus, J. Opt. Technol., 2013, vol. 80, no. 6, p. 372.
Kolesov, S.N., Volovik, M.G., and Priluchnyi, M.A., Meditsinskoe teploradiovidenie: sovremennyi metodologicheskii podkhod (Medical Thermal Imaging: Modern Methods), Nizhny Novgorod: Nizhegorodsk. Nacuhno-Issled. Inst. Travmatol. Ortop., 2008.
Fernández-Cuevas, I., Marins, J.C.B., Lastras, H.A., et al., Classification of factors influencing the use of infrared thermography in humans, Infrared Phys. Technol., 2015, vol. 71, p. 28.
Jang, C., Jalapu, S., Thuzar, M., et al., Infrared thermography in the detection of brown adipose tissue in humans, Physiol Rep., 2014, vol. 2, p. e12167.
Cramer, M.N. and Jay, O., Explained variance in the thermoregulatory responses to exercise: the independent roles of biophysical and fitness/fatness-related factors, J. Appl. Physiol., 2015, vol. 119, p. 982.
Akimov, E.B., Andreev, R.S., Kalenov, Yu.N., et al., The human thermal portrait and its relations with aerobic working capacity and the blood lactate level, Hum. Physiol., 2010, vol. 36, no. 4, p. 447.
Akimov, E.B., Andreev, R.S., Kalenov, Yu.N., et al., Possibilities of infrared thermography for identification of morphofunctional characteristics of a person (children and adults), Vestn. Mosk. Univ., Ser. 23: Antropol., 2016, no. 3, p. 49.
Chondronikola, M., Beeman, S.C., and Wahl, R.L., Non-invasive methods for the assessment of brown adipose tissue in humans, J. Physiol., 2018, vol. 596, no. 3, p. 363.
Orava, J., Nuutila, P., Lidell, M.E., et al., Different metabolic responses of human brown adipose tissue to activation by cold and insulin, Cell Metab., 2011, vol. 14, p. 272.
Stanford, K.I., Middelbeek, R.J., Townsend, K.L., et al., Brown adipose tissue regulates glucose homeostasis and insulin sensitivity, J. Clin. Invest., 2013, vol. 123, p. 215.
Robinson, L.J., Law, J.M., Symonds, M.E., et al., Brown adipose tissue activation as measured by infrared thermography by mild anticipatory psychological stress in lean healthy females, Exp. Physiol., 2016, vol. 101, p. 549.
Formenti, D., Ludwig, N., Rossi, A., et al., Skin temperature evaluation by infrared thermography: Comparison of two image analysis methods during the nonsteady state induced by physical exercise, Infrared Phys. Technol., 2017, vol. 81, p. 32.
Ivanitsky, G.R., Deev, A.A., Pashovkin, T.N., et al., Display peculiarities of hypodermic heating sources on the human body surface, Dokl. Biochem. Biophys., 2008, vol. 420, no. 1, p. 130.
Khizhnyak, L.N., Khizhnyak, E.P., and Ivanitskii, G.R., Diagnostic capabilities of matrix infrared thermography: problems and prospects, Vestn. Nov. Med. Tekhnol., 2012, vol. 19, no. 4, p. 170.
Gatidis, S., Schmidt, H., Pfannenberg, C.A., et al., Is it possible to detect activated brown adipose tissue in humans using single-time- point infrared thermography under thermoneutral conditions? Impact of BMI and subcutaneous adipose tissue thickness, PLoS One, 2016, vol. 11, p. e0151152.
Nedergaard, J., Bengtsson, T., and Cannon, B., Unexpected evidence for active brown adipose tissue in adult humans, Am. J. Physiol. Endocrinol. Metab., 2007, vol. 293, p. E444.
Koksharova, E.O., Maiorov, A.Yu., Shestakova, M.V., et al., Metabolic features and therapeutic potential of brown and beige adipose tissue, Sakharnyi Diabet, 2014, no. 4, p. 5.
Harms, M. and Seale, P., Brown and beige fat: development, function and therapeutic potential, Nat. Med., 2013, vol. 19, no. 10, p. 1252.
Spiegelman, B.M., Banting lecture 2012: Regulation of adipogenesis: toward new therapeutics for metabolic disease, Diabetes, 2013, vol. 62, no. 6, p. 1774.
Sebo, Z.L. and Rodeheffer, M.S., Assembling the adipose organ: adipocyte lineage segregation and adipogenesis in vivo, Development, 2019, vol. 146, no. 7. https://doi.org/10.1242/dev.172098
Rui, L., Brown and beige adipose tissues in health and disease, Comp. Physiol., 2017, vol. 7, no. 4, p. 1281.
Kim, K., Huang, S., Fletcher, L.A., et al., Whole body and regional quantification of active human brown adipose tissue using 18F-FDG PET/CT, J. Vis. Exp., 2019, vol. 146. https://doi.org/10.3791/58469
Schweizer, S., Oeckl, J., Klingenspor, M., et al., Substrate fluxes in brown adipocytes upon adrenergic stimulation and uncoupling protein 1 ablation, Life Sci. Alliance, 2018, vol. 1, no. 6, p. e201800136.
Reitman, M.L., Of mice and men—environmental temperature, body temperature, and treatment of obesity, FEBS Lett., 2018, vol. 592, no. 12, p. 2098.
Wang, S., Subramaniam, A., Cawthorne, M.A., et al., Increased fatty acid oxidation in transgenic mice over-expressing UCP3 in skeletal muscle, Diabetes, Obes. Metab., 2003, vol. 5, no. 5, p. 295.
Volkov, N.I., Melikhova, M.A., Oleinikov, V.I., and Tambovtseva, R.V., Obshchaya biokhimiya i biokhimiya fizicheskikh uprazhnenii: Uchebnoe posobie (General Biochemsitry and Biochemistry of Physical Exercises: Manual), Moscow: Ross. Gos. Univ. Fiz. Kul’t., Sporta, Molodehzi, Turizma, 2015, part 1.
Hankir, M.K. and Klingenspor, M., Brown adipocyte glucose metabolism: a heated subject, EMBO Rep., 2018, vol. 19, no. 9, p. e46404.
De Matteis, R., Lucertini, F., Guescini, M., et al., Exercise as a new physiological stimulus for brown adipose tissue activity, Nutr. Metab. Cardiovasc., 2012, no. 6, p. 582.
Son’kin, V.D., Akimov, E.B., Andreev, R.S., et al., Brown adipose tissue participate in lactate utilization during muscular work, Proc. 2nd Int. Congr. on Sports Sciences Research and Technology Support (icSPORTS-2014), Setúbal, 2014, p. 97.
Kozlov, A.V., Sonkin, V.D., and Yakushkin, A.V., Method to estimate activity of subcutaneous thermogenic structures on exposure to stimuli of different modalities, Hum. Physiol., 2017, vol. 43, no. 6, p. 719.
Symonds, M.E., Henderson, K., Elvidge, L., et al., Thermal imaging to assess age-related changes of skin temperature within the supraclavicular region co-locating with brown adipose tissue in healthy children, J. Pediatr., 2012, vol. 161, no. 5, p. 892.
Akimov, E.B., Andreev, R.S., Kalenov, Yu.N., et al., The human thermal portrait and its relations with aerobic working capacity and the blood lactate level, Fiziol. Chel., 2010, vol. 36, no. 4, p. 89.
Law, J., Chalmers, J., Morris, D.E., et al., The use of infrared thermography in the measurement and characterization of brown adipose tissue activation, Temperature, 2018, vol. 5, no. 2, p. 147.
Ong, F.J., Ahmed, B.A., Oreskovich, S.M., et al., Recent advances in the detection of brown adipose tissue in adult humans, Clin. Sci., 2018, vol. 132, no. 10, p. 1039.
Nedergaard, J. and Cannon, B., Brown adipose tissue as a heat-producing thermoeffector, in Handbook of Clinical Neurology, Vol. 156: Thermoregulation: From Basic Neuroscience to Clinical Neurology, Romanovsky, A.A., Ed., Amsterdam: Elsevier, 2018, chap. 9. https://doi.org/10.1016/B978-0-444-63912-7.00009-6
Jaksic, P.V., Grizelj, D., Livun, A., et al., Neck adipose tissue—tying ties in metabolic disorders, Horm. Mol. Biol. Clin. Invest., 2018, vol. 33, no. 2. https://doi.org/10.1515/hmbci-2017-0075
Lee, P., Werner, C.D., Kebebew, E., et al., Functional thermogenic beige adipogenesis is inducible in human neck fat, Int. J. Obes., 2014, vol. 38, p. 170.
Weiner, J., Hankir, M., Heiker, J.T., et al., Thyroid hormones and browning of adipose tissue, Mol. Cell. Endocrinol., 2017, vol. 458, p. 156.
Cannon, B. and Nedergaard, J., Brown adipose tissue: function and physiological significance, Physiol. Rev., 2004, vol. 84, p. 277.
Lidell, M.E., Betz, M.J., and Enerbäck, S., Brown adipose tissue and its therapeutic potential, J. Int. Med., 2014, vol. 276, no. 4, p. 364.
Astrup, A., Thermogenesis in human brown adipose tissue and skeletal muscle induced by sympathomimetic stimulation, Acta Endocrinol. Suppl., 1986, vol. 278, p. 1.
Volkov, N.I., Popov, O.I., Gabrys’, T., and Shmatlyan-Gabrys’, U., Physiological criteria in defining the standards for training and competition loads in elite sports, Hum. Physiol., 2005, vol. 31, no. 5, p. 606.
Oliveira, B.A., Pinhel, M.A., Nicoletti, C.F., et al., UCP1 and UCP3 expression is associated with lipid and carbohydrate oxidation and body composition, PLoS One, 2016, vol. 11, no. 3, p. e0150811.
Gribova, N.V. and Sonkin, V.D., The development of brown adipose tissue in ontogenesis, in Morfofunktsional’nye osobennosti rastushchego orgnaizma (Morphofunctional Features of Growing Organism), Moscow: Akad. Pedagog. Nauk SSSR, 1974, p. 120.
Hagen, T. and Vidal-Puig, A., Mitochondrial uncoupling proteins in human physiology and disease, Minerva Med., 2002, vol. 93, no. 1, p. 41.
Bondareva, E.A., Parfenteva, O.I., Kozlov, A.V., et al., The Ala/Val polymorphism of the UCP2 gene is reciprocally associated with aerobic and anaerobic performance in athletes, Hum. Physiol., 2018, vol. 44, no. 6, p. 673.
van Marken Lichtenbelt, W.D. and Schrauwen, P., Implications of nonshivering thermogenesis for energy balance regulation in humans, Am. J. Physiol.: Regul., Integr. Comp. Physiol., 2011, vol. 301, p. R285.
We thank the volunteers participating in the experimental study for their fruitful cooperation; as well as R.S. Andreev, Cand. Sci. (Biol.), and А.V. Yakushkin for the fruitful discussion of methodical approaches and the obtained results, as well as O.I. Parfent’eva for her aid in the statistical analysis of the results.
The study has been supported within the research program of the Department of Physiology, Russian State University of Physical Education, Sports, Youth, and Tourism for 2015–2020 (Combined Plan for Research Studies, SCOLIPE, topic 03.00.12. Human Homeostatic Nonshivering Thermogenesis: Interaction between the Mechanisms of Optional Nonshivering Thermogenesis and Adaptation to Physical Loads), as well as with a financial support of the Center of Advanced Sports Technologies and National Teams, Moskomsport.
Conflict of interests. The authors declare the absence of obvious and potential conflicts of interests associated with the publication of this article.
Statement of compliance with standards of research involving humans as subjects. All studies have been conducted in line with the principles of biomedical ethics formulated under the Helsinki Declaration 1964 and its subsequent amendments and approved by the local bioethical committee at the Center of Advanced Sports Technologies and National Teams (Moskomsport ) (Moscow). All participants in the study gave their voluntary informed written consent signed after informing them about potential risks an advantages, as well as about the nature of the planned study.
Translated by N. Tarasyuk
About this article
Cite this article
Kozlov, A.V., Son’kin, V.D. Infrared Thermography Diagnostics of Subcutaneous Thermogenerators of Non-Shivering Thermogenesis. Hum Physiol 45, 658–672 (2019) doi:10.1134/S0362119719060070
- infrared thermography
- skin temperature
- brown fat
- energy metabolism
- non-shivering thermogenesis