To assess BAT activity in humans at a population level, infrared thermography (IRT) represents a safe, readily repeatable and affordable alternative to 18F-FDG-PET. Building upon a previously proposed method by our laboratory, we further refined the image computational algorithm to quantify BAT activation in the cervical-supraclavicular (C-SCV) region of healthy young men under thermo-neutral and cold exposure conditions. Additionally, we validated the whole-body calorimeter (WBC) in reliably measuring cold-induced thermogenesis. The temperature gradient between C-SCV-deltoid regions, and the corresponding difference in heat power output, increased upon cold air exposure relative to thermo-neutral conditions (by 74.88 %, p<0.0001; and by 71.34 %, p<0.0001 respectively). Resting and cumulative energy expenditure (EE) rose significantly (by 13.14 % and 9.12 % respectively, p=0.0001) while positive correlations between IRT measures and EE were found with cold air exposure (percentage change in heat power gradient between ROI and deltoid, cold air: r(2)=0.29, p=0.026, Pearson's correlation). IRT and WBC can be used to study BAT activation. The refined algorithm allows for more automation and objectivity in IRT data analysis, especially under cold air exposures.

Clinical Nutrition Research Centre Singapore Institute for Clinical Sciences Agency for Science Technology and Research Singapore

See more in PubMed

ACOSTA FM, MARTINEZ-TELLEZ B, SANCHEZ-DELGADO G, ALCANTARA JMA, ACOSTA-MANZANO P, MORALES-ARTACHO AJ, RUIZ JR. Physiological responses to acute cold exposure in young lean men. PLoS One. 2018;13:e0196543. doi: 10.1371/journal.pone.0196543. PubMed DOI PMC

ANG QY, GOH HJ, CAO Y, LI Y, CHAN SP, SWAIN JL, HENRY CJ, LEOW MKS. A new method of infrared thermography for quantification of brown adipose tissue activation in healthy adults (TACTICAL): a randomized trial. J Physiol Sci. 2017;67:395–406. doi: 10.1007/s12576-016-0472-1. PubMed DOI PMC

BI X, LOO YT, HENRY CJ. Body fat measurements in Singaporean adults using four methods. Nutrients. 2018;10:pii: E303. doi: 10.3390/nu10030303. PubMed DOI PMC

BOON MR, BAKKER LEH, Van der LINDEN RAD, PEREIRA ARIAS-BOUDA L, SMIT F, VERBERNE HJ, Van MARKEN LICHTENBELT WD, JAZET IM, RENSEN PCN. Supraclavicular skin temperature as a measure of18F-FDG uptake by BAT in human subjects. PLoS One. 2014;9:e98822. doi: 10.1371/journal.pone.0098822. PubMed DOI PMC

BOON MR, Van MARKEN LICHTENBELT WD. Brown Adipose Tissue: A Human Perspective. Handbook of Experimental Pharmacology Germany. 2016;233:301–319. doi: 10.1007/164_2015_11. PubMed DOI

CANNON B, NEDERGAARD J. Brown adipose tissue: function and physiological significance. Physiol Rev. 2004;84:277–359. doi: 10.1152/physrev.00015.2003. PubMed DOI

CARTER EA, BONAB AA, PAUL K, YERXA J, TOMPKINS RG, FISCHMAN AJ. Association of heat production with 18F-FDG accumulation in murine brown adipose tissue after stress. J Nucl Med. 2011;52:1616–1620. doi: 10.2967/jnumed.111.090175. PubMed DOI PMC

CHEN YI, CYPESS AM, SASS CA, BROWNELL A-L, JOKIVARSI KT, KAHN CR, KWONG KK. Anatomical and functional assessment of brown adipose tissue by magnetic resonance imaging. Obesity. 2012;20:1519–1526. doi: 10.1038/oby.2012.22. PubMed DOI PMC

CHONDRONIKOLA M, VOLPI E, BORSHEIM E, CHAO T, PORTER C, ANNAMALAI P, YFANTI C, LABBE SM, HURREN NM, MALAGARIS I, CESANI F, SIDOSSIS LS. Brown adipose tissue is linked to a distinct thermoregulatory response to mild cold in people. Front Physiol. 2016;7:129. doi: 10.3389/fphys.2016.00129. PubMed DOI PMC

CLERTE M, BARON DM, BROUCKAERT P, ERNANDE L, RAHER MJ, FLYNN AW, PICARD MH, BLOCH KD, BUYS ES, SCHERRER-CROSBIE M. Brown adipose tissue blood flow and mass in obesity: a contrast ultrasound study in mice. J Am Soc Echocardiogr. 2013;26:1465–1473. doi: 10.1016/j.echo.2013.07.015. PubMed DOI PMC

CRANE JD, MOTTILLO EP, FARNCOMBE TH, MORRISON KM, STEINBERG GR. A standardized infrared imaging technique that specifically detects UCP1-mediated thermogenesis in vivo. Mol Metab. 2014;3:490–494. doi: 10.1016/j.molmet.2014.04.007. PubMed DOI PMC

CYPESS AM, HAFT CR, LAUGHLIN MR, HU HH. Brown fat in humans: consensus points and experimental guidelines. Cell Metab. 2014;20:408–415. doi: 10.1016/j.cmet.2014.07.025. PubMed DOI PMC

CYPESS AM, LEHMAN S, WILLIAMS G, TAL I, RODMAN D, GOLDFINE AB, KUO FC, PALMER EL, TSENG Y-H, DORIA A, KOLODNY GM, KAHN CR. Identification and importance of brown adipose tissue in adult humans. New England J Med. 2009;360:1509–1517. doi: 10.1056/NEJMoa0810780. PubMed DOI PMC

FLYNN A, LI Q, PANAGIA M, ABDELBAKY A, Mac NABB M, SAMIR A, CYPESS AM, WEYMAN AE, TAWAKOL A, SCHERRER-CROSBIE M. Contrast-enhanced ultrasound: a novel noninvasive, nonionizing method for the detection of brown adipose tissue in humans. J Am Soc Echocardiogr. 2015;28:1247–1254. doi: 10.1016/j.echo.2015.06.014. PubMed DOI PMC

GAGGE AP, BURTON AC, BAZETT HC. A practical system of units for the description of the heat exchange of man with his environment. Science. 1941;94:428–430. doi: 10.1126/science.94.2445.428. PubMed DOI

GATIDIS S, SCHMIDT H, PFANNENBERG CA, NIKOLAOU K, SCHICK F, SCHWENZER NF. 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;11:e0151152. doi: 10.1371/journal.pone.0151152. PubMed DOI PMC

GESTA S, TSENG YH, KAHN CR. Developmental origin of fat: tracking obesity to its source. Cell. 2007;131:242–256. doi: 10.1016/j.cell.2007.10.004. PubMed DOI

GOH HJ, GOVINDHARAJULU P, CAMPS SG, TAN SY, HENRY CJ. Gross and relative energy cost of domestic household activities in Asian men. Eur J Clin Nutr. 2016;70:1414–1419. doi: 10.1038/ejcn.2016.134. PubMed DOI

GREENHILL C. Obesity: Cold exposure increases brown adipose tissue in humans. Nat Rev Endocrinol. 2013;9:566. doi: 10.1038/nrendo.2013.156. PubMed DOI

HAINER V, ZAMRAZILOVA H, KUNESOVA M, BENDLOVA B, ALDHOON-HAINEROVA I. Obesity and infection: reciprocal causality. Physiol Res. 2015;64(Suppl 2):S105–S119. PubMed

HAQ T, CRANE JD, KANJI S, GUNN E, TARNOPOLSKY MA, GERSTEIN HC, STEINBERG GR, MORRISON KM. Optimizing the methodology for measuring supraclavicular skin temperature using infrared thermography; implications for measuring brown adipose tissue activity in humans. Sci Rep England. 2017;7:11934. doi: 10.1038/s41598-017-11537-x. PubMed DOI PMC

HENRY CJ, KAUR B, QUEK RYC, CAMPS SG. A Low glycaemic index diet incorporating isomaltulose is associated with lower glycaemic response and variability, and promotes fat oxidation in asians. Nutrients. 2017;9:473. doi: 10.3390/nu9050473. PubMed DOI PMC

HOYTE T, SCHIAVON S, PICCOLI A, MOON D, STEINFELD K. CBE Thermal Comfort Tool. Center for the Built Environment, University of California; Berkeley: 2013. available at: http://cbe.berkeley.edu/comforttool/

HU HH, PERKINS TG, CHIA JM, GILSANZ V. Characterization of human brown adipose tissue by chemical-shift water-fat MRI. AJR Am J Roentgenol. 2013;200:177–183. doi: 10.2214/AJR.12.8996. PubMed DOI PMC

ISHIBASHI J, SEALE P. Medicine. Beige can be slimming. Science. 2010;328:1113–1114. doi: 10.1126/science.1190816. PubMed DOI PMC

JANG C, JALAPU S, THUZAR M, LAW PW, JEAVONS S, BARCLAY JL, HO KKY. Infrared thermography in the detection of brown adipose tissue in humans. Physiol Rep. 2014;2:pii: e12167. doi: 10.14814/phy2.12167. PubMed DOI PMC

LAU AZ, CHEN AP, GU Y, LADOUCEUR-WODZAK M, NAYAK KS, CUNNINGHAM CH. Noninvasive identification and assessment of functional brown adipose tissue in rodents using hyperpolarized 13C imaging. Int J Obes (London) 2014;38:126–131. doi: 10.1038/ijo.2013.58. PubMed DOI

LAW J, MORRIS DE, IZZI-ENGBEAYA C, SALEM V, COELLO C, ROBINSON L, JAYASINGHE M, SCOTT R, GUNN R, RABINER E, TAN T, DHILLO WS, BLOOM S, BUDGE H, SYMONDS ME. thermal imaging is a noninvasive alternative to PET/CT for measurement of brown adipose tissue activity in humans. J Nucl Med. 2018;59:516–522. doi: 10.2967/jnumed.117.190546. PubMed DOI PMC

LEE P, HO KKY, LEE P, GREENFIELD JR, HO KKY, GREENFIELD JR. Hot fat in a cool man: infrared thermography and brown adipose tissue. Diabetes Obes Metab. 2011;13:92–93. doi: 10.1111/j.1463-1326.2010.01318.x. PubMed DOI

LOWELL BB, SPIEGELMAN BM. Towards a molecular understanding of adaptive thermogenesis. Nature. 2000;404:652–660. doi: 10.1038/35007527. PubMed DOI

MASUDA Y, HARAMIZU S, OKI K, OHNUKI K, WATANABE T, YAZAWA S, KAWADA T, HASHIZUME S, FUSHIKI T. Upregulation of uncoupling proteins by oral administration of capsiate, a nonpungent capsaicin analog. J Appl Physiol (1985) 2003;95:2408–2415. doi: 10.1152/japplphysiol.00828.2002. PubMed DOI

MORRISON SF. Central neural control of thermoregulation and brown adipose tissue. Auton Neurosci. 2016;196:14–24. doi: 10.1016/j.autneu.2016.02.010. PubMed DOI PMC

PETROVIC N, WALDEN TB, SHABALINA IG, TIMMONS JA, CANNON B, NEDERGAARD J. Chronic peroxisome proliferator-activated receptor γ (PPARγ) activation of epididymally derived white adipocyte cultures reveals a population of thermogenically competent, UCP1-containing adipocytes molecularly distinct from classic brown adipocytes. J Biol Chem. 2010;285:7153–7164. doi: 10.1074/jbc.M109.053942. PubMed DOI PMC

PITHA J, KOVAR J, BLAHOVA T. Fasting and nonfasting triglycerides in cardiovascular and other diseases. Physiol Res. 2015;64(Suppl 3):S323–S330. PubMed

SACKS H, SYMONDS ME. Anatomical locations of human brown adipose tissue: functional relevance and implications in obesity and type 2 diabetes. Diabetes. 2013;62:1783–1790. doi: 10.2337/db12-1430. PubMed DOI PMC

SAITO M, OKAMATSU-OGURA Y, MATSUSHITA M, WATANABE K, YONESHIRO T, NIO-KOBAYASHI J, IWANAGA T, MIYAGAWA M, KAMEYA T, NAKADA K, KAWAI Y, TSUJISAKI M. High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes. 2009;58:1526–1531. doi: 10.2337/db09-0530. PubMed DOI PMC

SAITO M, YONESHIRO T. Capsinoids and related food ingredients activating brown fat thermogenesis and reducing body fat in humans. Curr Opin Lipidol. 2013;24:71–77. doi: 10.1097/MOL.0b013e32835a4f40. PubMed DOI

SALEM V, IZZI-ENGBEAYA C, COELLO C, THOMAS DB, CHAMBERS ES, COMNINOS AN, BUCKLEY A, WIN Z, AL-NAHHAS A, RABINER EA, GUNN RN, BUDGE H, SYMONDS ME, BLOOM SR, TAN TM, DHILLO WS. Glucagon increases energy expenditure independently of brown adipose tissue activation in humans. Diabetes Obes Metab. 2016;18:72–81. doi: 10.1111/dom.12585. PubMed DOI PMC

SOILLE P. Morphological Image Analysis: Principles and Applications. 1999 doi: 10.1007/978-3-662-05088-0. DOI

SYMONDS ME, HENDERSON K, ELVIDGE L, BOSMAN C, SHARKEY D, PERKINS AC, BUDGE H. 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;161:892–898. doi: 10.1016/j.jpeds.2012.04.056. PubMed DOI

Van der LANS AAJJ, VOSSELMAN MJ, HANSSEN MJW, BRANS B, Van MARKEN LICHTENBELT WD. Supraclavicular skin temperature and BAT activity in lean healthy adults. J Physiol Sci. 2016;66:77–83. doi: 10.1007/s12576-015-0398-z. PubMed DOI PMC

Van MARKEN LICHTENBELT WD, VANHOMMERIG JW, SMULDERS NM, DROSSAERTS JMAFL, KEMERINK GJ, BOUVY ND, SCHRAUWEN P, TEULE GJJ. Cold-activated brown adipose tissue in healthy men. New Engl J Med. 2009;360:1500–1508. doi: 10.1056/NEJMoa0808718. PubMed DOI

VEGIOPOULOS A, MÜLLER-DECKER K, STRZODA D, SCHMITT I, CHICHELNITSKIY E, OSTERTAG A, BERRIEL DIAZ M, ROZMAN J, HRABE De ANGELIS M, NÜSING RM, MEYER CW, WAHLI W, KLINGENSPOR M, HERZIG S. Cyclooxygenase-2 controls energy homeostasis in mice by de novo recruitment of brown adipocytes. Science. 2010;328:1158–1161. doi: 10.1126/science.1186034. PubMed DOI

VIRTANEN KA, LIDELL ME, ORAVA J, HEGLIND M, WESTERGREN R, NIEM T, TAITTONEN M, LAINE J, SAVISTO NJ, ENERBÄCK S, NUUTILA P. Functional brown adipose tissue in healthy adults. New Engl J Med. 2009;360:1518–1525. doi: 10.1056/NEJMoa0808949. PubMed DOI

WALDÉN TB, HANSEN IR, TIMMONS JA, CANNON B, NEDERGAARD J. Recruited vs. nonrecruited molecular signatures of brown, “brite,” and white adipose tissues. Am J Physiol Endocrinol Metab. 2012;302:E19–E31. doi: 10.1152/ajpendo.00249.2011. PubMed DOI

ZHANG J, WU H, MA S, JING F, YU C, GAO L, ZHAO J. Transcription regulators and hormones involved in the development of brown fat and white fat browning: transcriptional and hormonal control of brown/beige fat development. Physiol Res. 2018;67:347–362. doi: 10.33549/physiolres.933650. PubMed DOI