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Review

18F-FDG PET/CT technology for the assessment of brown adipose tissue: an updated review

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Pages 1143-1156 | Received 30 May 2023, Accepted 10 Nov 2023, Published online: 18 Nov 2023

References

  • Marlatt KL, Ravussin E. Brown adipose tissue: an update on recent findings. Curr Obes Rep. 2017;6(4):389–396. doi: 10.1007/s13679-017-0283-6
  • Cheng L, Wang J, Dai H, et al. Brown and beige adipose tissue: a novel therapeutic strategy for obesity and type 2 diabetes mellitus. Adipocyte. 2021;10(1):48–65. doi: 10.1080/21623945.2020.1870060
  • Sanchez-Gurmaches J, Guertin DA. Adipocyte lineages: tracing back the origins of fat. Biochim Biophys Acta. 2014;1842(3):340–351. doi: 10.1016/j.bbadis.2013.05.027
  • Goossens GH. The metabolic phenotype in obesity: fat mass, body fat distribution, and adipose tissue function. Obes Facts. 2017;10(3):207–215. doi: 10.1159/000471488
  • Matsuzawa Y, Shimomura I, Nakamura T, et al. Pathophysiology and pathogenesis of visceral fat obesity. Obes Res. 1995;3(S2):187S–194S. doi: 10.1002/j.1550-8528.1995.tb00462.x
  • Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev. 2004;84(1):277–359. doi: 10.1152/physrev.00015.2003
  • Bonet ML, Oliver P, Palou A. Pharmacological and nutritional agents promoting browning of white adipose tissue. Biochim Biophys Acta. 2013;1831(5):969–985. doi: 10.1016/j.bbalip.2012.12.002
  • Van Marken Lichtenbelt WD, Vanhommering JW, Smulders NM, et al. Cold-activated brown adipose tissue in healthy men. N Engl J Med. 2009;360(15):1500–1508. doi: 10.1056/NEJMoa0808718
  • Hu HH. Magnetic resonance of brown adipose tissue: a review of Current techniques. Crit Rev Biomed Eng. 2015;43(2–3):161–181. doi: 10.1615/CritRevBiomedEng.2015014377
  • Frankl J, Sherwood A, Clegg DJ, et al. Imaging metabolically active fat: a literature review and mechanistic insights. Int J Mol Sci. 2019;20(21):5509. doi: 10.3390/ijms20215509
  • Prodhomme H, Ognard J, Robin P, et al. Imaging and identification of brown adipose tissue on CT scan. Clin Physiol Funct Imaging. 2018;38(2):186–191. doi: 10.1111/cpf.12373
  • Franz D, Karampinos DC, Rummeny EJ, et al. Discrimination between brown and white adipose tissue using a 2-point dixon water–fat separation method in simultaneous PET/MRI. J Nucl Med. 2015;56(11):1742–1747. doi: 10.2967/jnumed.115.160770
  • Chen YI, Cypess AM, Sass CA, et al. Anatomical and functional assessment of brown adipose tissue by magnetic resonance imaging. Obesity (Silver Spring). 2012;20(7):1519–1526. doi: 10.1038/oby.2012.22
  • Yu Q, Huang S, Xu TT, et al. Measuring brown fat using MRI and implications in the metabolic syndrome. J Magn Reson Imaging. 2021;54(5):1377–1392. doi: 10.1002/jmri.27340
  • Hu HH, Hines CDG, Smith DL Jr, et al. Variations in T(2)* and fat content of murine brown and white adipose tissues by chemical-shift MRI. Magn Reson Imaging. 2012;30(3):323–329. doi: 10.1016/j.mri.2011.12.004
  • Flynn A, Li Q, Panagia M, et al. Contrast-enhanced ultrasound: a novel noninvasive, nonionizing method for the detection of brown adipose tissue in humans. J Am Soc Echocardiogr. 2015;28(10):1247–1254. doi: 10.1016/j.echo.2015.06.014
  • Law J, Morris DE, Budge H, et al. Infrared thermography. Handb Exp Pharmacol. 2019;251:259–282.
  • Law J, Morris DE, Izzi-Engbeaya C, et al. Thermal imaging is a noninvasive alternative to PET/CT for measurement of brown adipose tissue activity in humans. J Nucl Med. 2018;59(3):516–522. doi: 10.2967/jnumed.117.190546
  • Goetze S, Lavely WC, Ziessman HA, et al. Visualization of brown adipose tissue with 99mTc-methoxyisobutylisonitrile on SPECT/CT. J Nucl Med. 2008;49(5):752–756. doi: 10.2967/jnumed.107.048074
  • Cypess AM, Doyle AN, Sass CA, et al. Quantification of human and rodent brown adipose tissue function using 99mTc-methoxyisobutylisonitrile SPECT/CT and 18F-FDG PET/CT. J Nucl Med. 2013;54(11):1896–1901. doi: 10.2967/jnumed.113.121012
  • Baba S, Engles JM, Huso DL, et al. Comparison of uptake of multiple clinical radiotracers into brown adipose tissue under cold-stimulated and nonstimulated conditions. J Nucl Med. 2007;48(10):1715–1723. doi: 10.2967/jnumed.107.041715
  • Haghighatafshar M, Farhoudi F. Is brown adipose tissue visualization reliable on 99mTc-methoxyisobutylisonitrile diagnostic SPECT scintigraphy? Medicine (Baltimore). 2016;95(2):e2498. doi: 10.1097/MD.0000000000002498
  • Zhang F, Hao G, Shao M, et al. An Adipose Tissue Atlas: An Image-Guided Identification of Human-like BAT and Beige Depots in Rodents. Cell Metab. 2018;27(1):252–262. doi: 10.1016/j.cmet.2017.12.004
  • Qi J, Kurian E, Öz OK. Omental hibernoma revealed by 18 F-FDG PET/CT. Clin Nucl Med. 2023;48(9):796–798. doi: 10.1097/RLU.0000000000004753
  • Callaud A, Metrard G, Besse H, et al. Extinction of lipomatous hypertrophy of the interatrial septum FDG uptake with propranolol premedication. Clin Nucl Med. 2023;48(6):536–537. doi: 10.1097/RLU.0000000000004640
  • Martinez-Tellez B, Nahon KJ, Sanchez-Delgado G, et al. The impact of using BARCIST 1.0 criteria on quantification of BAT volume and activity in three independent cohorts of adults. Sci Rep. 2018;8(1):8567. doi: 10.1038/s41598-018-26878-4
  • Crandall JP, Gajwani P, JH O, et al. Repeatability of brown adipose tissue measurements on FDG PET/CT following a simple cooling procedure for BAT activation. PLoS One. 2019;14(4):e0214765. doi: 10.1371/journal.pone.0214765
  • Rousseau C, Bourbouloux E, Campion L, et al. Brown fat in breast cancer patients: analysis of serial (18)F-FDG PET/CT scans. Eur J Nucl Med Mol Imaging. 2006;33(7):785–791. doi: 10.1007/s00259-006-0066-x
  • Fuse S, Nirengi S, Amagasa S, et al. Brown adipose tissue density measured by near-infrared time-resolved spectroscopy in Japanese, across a wide age range. J Biomed Opt. 2018;23(6):065002. doi: 10.1117/1.JBO.23.6.065002
  • Jones TA, Wayte SC, Reddy NL, et al. Identification of an optimal threshold for detecting human brown adipose tissue using receiver operating characteristic analysis of IDEAL MRI fat fraction maps. Magn Reson Imaging. 2018;51:61–68. doi: 10.1016/j.mri.2018.04.013
  • Gashi G, Madoerin P, Maushart CI, et al. MRI characteristics of supraclavicular brown adipose tissue in relation to cold-induced thermogenesis in healthy human adults. J Magn Reson Imaging. 2019 Oct;50(4):1160–1168. doi: 10.1002/jmri.26733
  • Ouwerkerk R, Hamimi A, Matta J, et al. Proton MR spectroscopy measurements of white and brown adipose tissue in healthy humans: relaxation parameters and unsaturated fatty acids. Radiology. 2021;299(2):396–406. doi: 10.1148/radiol.2021202676
  • Crandall JP, JH O, Gajwani P, et al. Measurement of brown adipose tissue activity using microwave radiometry and 18F-FDG PET/CT. J Nucl Med. 2018;59(8):1243–1248. doi: 10.2967/jnumed.117.204339
  • Kordic M, Dugandžić J, Ratko M, et al. Infrared thermography for the detection of changes in brown adipose tissue activity. J Vis Exp. 2022;187(187): doi: 10.3791/64463
  • Tay SH, Goh HJ, Govindharajulu P, et al. Brown fat activity determined by infrared thermography and thermogenesis measurement using whole body calorimetry (BRIGHT study). Physiol Res. 2020;69:85–97. doi: 10.33549/physiolres.934190
  • Martinez-Tellez B, Perez-Bey A, Sanchez-Delgado G, et al. Concurrent validity of supraclavicular skin temperature measured with iButtons and infrared thermography as a surrogate marker of brown adipose tissue. J Therm Biol. 2019;82:186–196. doi: 10.1016/j.jtherbio.2019.04.009
  • Martinez-Tellez B, Sanchez-Delgado G, Boon MR, et al. Distribution of brown adipose tissue radiodensity in young adults: implications for cold [18F]FDG-PET/CT analyses. Mol Imaging Biol. 2020;22(2):425–433. doi: 10.1007/s11307-019-01381-y
  • Nazeri A, Crandall JP, Fraum TJ, et al. Repeatability of Radiomic features of brown adipose tissue. J Nucl Med. 2021;62(5):700–706. doi: 10.2967/jnumed.120.248674
  • Ter Voert EEGW, Svirydenka H, Müller J, et al. Low-dose 18F-FDG TOF-PET/MR for accurate quantification of brown adipose tissue in healthy volunteers. EJNMMI Res. 2020;10(1):5. doi: 10.1186/s13550-020-0592-8
  • Fraum TJ, Crandall JP, Ludwig DR, et al. Repeatability of quantitative brown adipose tissue imaging metrics on positron emission tomography with 18F-Fluorodeoxyglucose in humans. Cell Metab. 2019;30(1):212–224. doi: 10.1016/j.cmet.2019.05.019
  • Kulterer OC, Herz CT, Prager M, et al. Brown adipose tissue prevalence is lower in obesity but its metabolic activity is intact. Front Endocrinol. 2022;13:858417. doi: 10.3389/fendo.2022.858417
  • Bonacina M, Albano D, Gazzilli M, et al. 18F-FDG PET/CT brown fat detection: differences between adult and pediatric population in a 12 year experience. Revista Española de Medicina Nuclear e Imagen Molecular (English Edition). 2019;38(4):224–228. doi: 10.1016/j.remnie.2019.02.004
  • Shao X, Chen Y, Shao X, et al. Gender differences in brown adipose tissue-related brain functional networks: an 18F-FDG-PET study. Nucl Med Commun. 2020;41(6):526–532. doi: 10.1097/MNM.0000000000001190
  • Monfort-Pires M, Regeni-Silva G, Dadson P, et al. Brown fat triglyceride content is associated with cardiovascular risk markers in adults from a tropical region. Front Endocrinol. 2022;13:919588. doi: 10.3389/fendo.2022.919588
  • Acosta FM, Sanchez-Delgado G, Martinez-Tellez B, et al. Sleep duration and quality are not associated with brown adipose tissue volume or activity—as determined by 18F-FDG uptake, in young, sedentary adults. Sleep. 2019;42(12):zsz177. doi: 10.1093/sleep/zsz177
  • Zhang Y, Song K, Qi G, et al. Adipose-derived exosomal miR-210/92a cluster inhibits adipose browning via the FGFR-1 signaling pathway in high-altitude hypoxia. Sci Rep. 2020;10(1):14390. doi: 10.1038/s41598-020-71345-8
  • Ortiz-Alvarez L, Acosta FM, Xu H, et al. Fecal microbiota composition is related to brown adipose tissue 18F-fluorodeoxyglucose uptake in young adults. J Endocrinol Invest. 2023;46(3):567–576. doi: 10.1007/s40618-022-01936-x
  • Rajagopolan S, Park B, Palanivel R, et al. Metabolic effects of air pollution exposure and reversibility. J Clin Invest. 2020;130(11):6034–6040. doi: 10.1172/JCI137315
  • Ogawa M, Koskensalo K, Laurila S, et al. Brown adipose tissue fat-fraction is associated with skeletal muscle adiposity. Eur J Appl Physiol. 2022;122(1):81–90. doi: 10.1007/s00421-021-04816-z
  • Mendez-Gutierrez A, Aguilera CM, Osuna-Prieto FJ, et al. Exercise-induced changes on exerkines that might influence brown adipose tissue metabolism in young sedentary adults. Eur J Sport Sci. 2023;23(4):625–636. doi: 10.1080/17461391.2022.2040597
  • Jurado-Fasoli L, Merchan-Ramirez E, Martinez-Tellez E, et al. Association between dietary factors and brown adipose tissue volume/18F-FDG uptake in young adults. Clin Nutr. 2021;40(4):1997–2008. doi: 10.1016/j.clnu.2020.09.020
  • Leitner BP, Weiner LS, Desir M, et al. Kinetics of human brown adipose tissue activation and deactivation. Int J Obes (Lond). 2019;43(3):633–637. doi: 10.1038/s41366-018-0104-3
  • Herz CT, Kulterer OC, Prager M, et al. Sex differences in brown adipose tissue activity and cold-induced thermogenesis. Mol Cell Endocrinol. 2021;534:111365. doi: 10.1016/j.mce.2021.111365
  • Martinez-Tellez B, Garcia-Rivero Y, Sanchez-Delgado G, et al. Supraclavicular skin temperature measured by iButtons and 18F-fluorodeoxyglucose uptake by brown adipose tissue in adults. J Therm Biol. 2019;82:178–185. doi: 10.1016/j.jtherbio.2019.04.006
  • Martinez-Tellez B, Xu H, Sanchez-Delgado G, et al. Association of wrist and ambient temperature with cold-induced brown adipose tissue and skeletal muscle [18F]FDG uptake in young adults. Am J Physiol Regul Integr Comp Physiol. 2018;315(6):R1281–R1288. doi: 10.1152/ajpregu.00238.2018
  • Søberg S, Löfgren J, Philipsen FE, et al. Altered brown fat thermoregulation and enhanced cold-induced thermogenesis in young, healthy, winter-swimming men. Cell Rep Med. 2021;2(10):100408. doi: 10.1016/j.xcrm.2021.100408
  • Muzik O, Reilly KT, Diwadkar VA. “Brain over body”-A study on the willful regulation of autonomic function during cold exposure. Neuroimage. 2018;172:632–641. doi: 10.1016/j.neuroimage.2018.01.067
  • Sanchez-Delgado G, Martinez-Tellez B, Garcia-Rivero Y, et al. Association between brown adipose tissue and bone mineral density in humans. Int J Obes (Lond). 2019;43(8):1516–1525. doi: 10.1038/s41366-018-0261-4
  • Borup A, Donkin I, Boon MR, et al. Association of apolipoprotein M and sphingosine-1-phosphate with brown adipose tissue after cold exposure in humans. Sci Rep. 2022;12(1):18753. doi: 10.1038/s41598-022-21938-2
  • Kulterer OC, Niederstaetter L, Herz CT, et al. The presence of active brown adipose tissue determines cold-induced energy expenditure and oxylipin profiles in humans. J Clin Endocrinol Metab. 2020;105(7):2203–2216. doi: 10.1210/clinem/dgaa183
  • Raiko J, Orava J, Savisto N, et al. High brown fat activity correlates with cardiovascular risk factor levels cross-sectionally and subclinical atherosclerosis at 5-year follow-up. Arterioscler Thromb Vasc Biol. 2020;40(5):1289–1295. doi: 10.1161/ATVBAHA.119.313806
  • Maushart CI, Senn JR, Loeliger RC, et al. Free thyroxine levels are associated with cold induced thermogenesis in healthy euthyroid individuals. Front Endocrinol. 2021;12:666595. doi: 10.3389/fendo.2021.666595
  • Sun L, Goh HJ, Govindharajulu P, et al. A feedforward loop within the thyroid-brown fat axis facilitates thermoregulation. Sci Rep. 2020;10(1):9661. doi: 10.1038/s41598-020-66697-0
  • Merchan-Ramirez E, Sanchez-Delgado G, Arrizabalaga-Arriazu C, et al. Thyroid function is not associated with brown adipose tissue volume and 18F-fluorodeoxyglucose uptake in young euthyroid adults. Eur J Endocrinol. 2021;185(2):209–218. doi: 10.1530/EJE-21-0192
  • Acosta FM, Sanchez-Delgado G, Martinez-Tellez B, et al. Diurnal variations of cold-induced thermogenesis in young, healthy adults: a randomized crossover trial. Clin Nutr. 2021;40(10):5311–5321. doi: 10.1016/j.clnu.2021.08.010
  • Levy SB. Field and laboratory methods for quantifying brown adipose tissue thermogenesis. Am J Hum Biol. 2019;31(4):e23261. doi: 10.1002/ajhb.23261
  • Sardjoe Mishre ASD, Martinez-Tellez B, Acosta FM, et al. Association of shivering threshold time with body composition and brown adipose tissue in young adults. J Therm Biol. 2022;108:103277. doi: 10.1016/j.jtherbio.2022.103277
  • Fischer JGW, Maushart CI, Becker AS, et al. Comparison of [18F]FDG PET/CT with magnetic resonance imaging for the assessment of human brown adipose tissue activity. EJNMMI Res. 2020;10(1):85. doi: 10.1186/s13550-020-00665-7
  • Sun L, Verma S, Michael N, et al. Brown adipose tissue: multimodality evaluation by PET, MRI, infrared thermography, and whole-body calorimetry (TACTICAL-II). Obesity (Silver Spring). 2019;27(9):1434–1442. doi: 10.1002/oby.22560
  • Andresson J, Lundström E, Engström M, et al. Estimating the cold-induced brown adipose tissue glucose uptake rate measured by 18F-FDG PET using infrared thermography and water-fat separated MRI. Sci Rep. 2019;9(1):12358. doi: 10.1038/s41598-019-48879-7
  • Loeliger RC, Maushart CI, Gashi G, et al. Relation of diet-induced thermogenesis to brown adipose tissue activity in healthy men. Am J Physiol Endocrinol Metab. 2021;320(1):E93–E101. doi: 10.1152/ajpendo.00237.2020
  • Wibmer AG, Becher T, Eljalby M, et al. Brown adipose tissue is associated with healthier body fat distribution and metabolic benefits independent of regional adiposity. Cell Rep Med. 2021;2(7):100332. doi: 10.1016/j.xcrm.2021.100332
  • Sanchez-Delgado G, Martinez-Tellez B, Acosta FM, et al. Brown adipose tissue volume and fat content are positively associated with whole-body adiposity in young men—not in women. Diabetes. 2021;70(7):1473–1485. doi: 10.2337/db21-0011
  • Richard MA, Pallubinsky H, Blondin DP. Functional characterization of human brown adipose tissue metabolism. Biochem J. 2020;477(7):1261–1286. doi: 10.1042/BCJ20190464
  • Soundarrajan M, Deng J, Kwasny M, et al. Activated brown adipose tissue and its relationship to adiposity and metabolic markers: an exploratory study. Adipocyte. 2020;9(1):87–95. doi: 10.1080/21623945.2020.1724740
  • Crandall JP, Fraum TJ, Wahl RL. Brown adipose tissue: a protective mechanism against “preprediabetes”? J Nucl Med. 2022;63(9):1433–1440. doi: 10.2967/jnumed.121.263357
  • Sun L, Yan J, Goh HJ, et al. Fibroblast growth factor-21, leptin, and adiponectin responses to acute cold-induced brown adipose tissue activation. J Clin Endocrinol Metab. 2020;105(3):e520–e531. doi: 10.1210/clinem/dgaa005
  • Chu K, Bos SA, Gill CM, et al. Brown adipose tissue and cancer progression. Skeletal Radiol. 2020;49(4):635–639. doi: 10.1007/s00256-019-03322-w
  • Eljalby M, Huang X, Becher T, et al. Brown adipose tissue is not associated with cachexia or increased mortality in a retrospective study of patients with cancer. Am J Physiol Endocrinol Metab. 2023;324(2):E144–E153. doi: 10.1152/ajpendo.00187.2022
  • Becker AS, Zellweger C, Bacanovic S, et al. Brown fat does not cause cachexia in cancer patients: a large retrospective longitudinal FDG-PET/CT cohort study. PLoS One. 2020;15(10):e0239990. doi: 10.1371/journal.pone.0239990
  • Pace L, Nicolai E, Basso L, et al. Brown adipose tissue in breast cancer evaluated by [18F] FDG-PET/CT. Mol Imaging Biol. 2020;22(4):1111–1115. doi: 10.1007/s11307-020-01482-z
  • Park SY, Choi EK, Oh JK, et al. Brown fat activation demonstrated on FDG PET/CT predicts survival outcome. J Cancer Res Clin Oncol. 2022;149(8):4847–4851. Online ahead of print. doi: 10.1007/s00432-022-04390-7
  • Ginzac A, Barres B, Chanchou M, et al. A decrease in brown adipose tissue activity is associated with weight gain during chemotherapy in early breast cancer patients. BMC Cancer. 2020;20(1):96. doi: 10.1186/s12885-020-6591-3
  • Brendle C, Stefan N, Grams E, et al. Determinants of activity of brown adipose tissue in lymphoma patients. Sci Rep. 2020;10(1):21802. doi: 10.1038/s41598-020-78419-7
  • Abdul Sater Z, Jha A, Hamimi A, et al. Pheochromocytoma and paraganglioma patients with poor survival often show brown adipose tissue activation. J Clin Endocrinol Metab. 2020;105(4):1176–1185. doi: 10.1210/clinem/dgz314
  • Ogawa Y, Abe K, Sakoda A, et al. FDG-PET and CT findings of activated brown adipose tissue in a patient with paraganglioma. Eur J Radiol Open. 2018;5:126–130. doi: 10.1016/j.ejro.2018.08.002
  • Tsechelidis I, El Darazi E, Muteganya R, et al. Failure of classical β-blocker carvedilol to deactivate brown adipose tissue in a patient with pheochromocytoma. Clin Nucl Med. 2018;43(8):604–605. doi: 10.1097/RLU.0000000000002170
  • Koh Y, Asakura T, Katayama K, et al. [A case report: FDG uptake to brown adipose tissue activated by elevated serum catecholamine in a patient with pheochromocytoma]. Hinyokika Kiyo. 2018;64(11):435–438. doi: 10.14989/ActaUrolJap_64_11_435
  • Steinhoff KG, Krause K, Linder N, et al. Effects of hyperthyroidism on adipose tissue activity and distribution in adults. Thyroid: Offic J Am Thyroid Association. 2021;31(3):519–527. doi: 10.1089/thy.2019.0806
  • Ho WE, Sun L, Goh HJ, et al. Brown adipose tissue influences adiponectin and thyroid hormone changes during graves’ disease therapy. Adipocyte. 2022;11(1):389–400. doi: 10.1080/21623945.2022.2104509
  • Sun L, Goh HJ, Verma S, et al. Brown adipose tissues mediate the metabolism of branched chain amino acids during the transitioning from hyperthyroidism to euthyroidism (TRIBUTE). Sci Rep. 2022;12(1):3693. doi: 10.1038/s41598-022-07701-7
  • Olivera FR, Mamede M, Bizzi MF, et al. Brown adipose tissue activity is reduced in women with polycystic ovary syndrome. Eur J Endocrinol. 2019;181(5):473–480. doi: 10.1530/EJE-19-0505
  • Oliveira FR, Mamede BM, Bizzi MF. Effects of short term metformin treatment on brown adipose tissue activity and plasma irisin levels in women with polycystic ovary syndrome: a randomized controlled trial. Horm Metab Res. 2020;52(10):718–723. doi: 10.1055/a-1157-0615
  • Sanders KJC, Wierts R, van Marken Lichtenbelt, et al. Brown adipose tissue activation is not related to hypermetabolism in emphysematous chronic obstructive pulmonary disease patients. J Cachexia Sarcopenia Muscle. 2022;13(2):1329–1338. doi: 10.1002/jcsm.12881
  • Shirakawa C, Koyasu S, Takada M, et al. Unilateral reduction of 18F-FDG accumulation in brown adipose tissue by sympathectomy for hyperhidrosis. Clin Nucl Med. 2023;48(1):79–80. doi: 10.1097/RLU.0000000000004393
  • Sun L, Goh HJ, Verma S, et al. Metabolic effects of brown fat in transitioning from hyperthyroidism to euthyroidism. Eur J Endocrinol. 2021;185(4):553–563. doi: 10.1530/EJE-21-0366
  • Enevoldsen LH, Tindborg M, Hovmand NL, et al. Functional brown adipose tissue and sympathetic activity after cold exposure in humans with type 1 narcolepsy. Sleep. 2018;41(8): doi: 10.1093/sleep/zsy092
  • Harb E, Kheder O, Poopalasingam G, et al. Brown adipose tissue and regulation of human body weight. Diabetes Metab Res Rev. 2023;39:e3594. doi: 10.1002/dmrr.3594
  • Suthar PP, Virmani S. Intense brown fat uptake at FDG PET/CT induced by Mirabegron. Radiol Imaging Cancer. 2023;5(4):e230055. doi: 10.1148/rycan.230055
  • O’Mara AE, Johnson JW, Linderman JD, et al. Chronic mirabegron treatment increases human brown fat, HDL cholesterol, and insulin sensitivity. J Clin Invest. 2020;130(5):2209–2219. doi: 10.1172/JCI131126
  • Brahmbhatt P, Ataei F, Parent EE, et al. Atypically intense pharmacologically induced brown fat activation on FDG PET/CT. Clin Nucl Med. 2023;48(3):233–236. doi: 10.1097/RLU.0000000000004520
  • Chen KY, Brychta RJ, Israni NS, et al. Activating human adipose tissue with the β3-adrenergic agonist Mirabegron. Methods Mol Biol. 2022;2448:83–96.
  • Bouter K, Bakker GJ, Levin E, et al. Differential metabolic effects of oral butyrate treatment in lean versus metabolic syndrome subjects. Clin Transl Gastroenterol. 2018;9(5):155. doi: 10.1038/s41424-018-0025-4
  • Maliszewska K, Adamska-Patruno E, Miniewska K, et al. Different protein sources enhance 18FDG-PET/MR uptake of brown adipocytes in male subjects. Nutrients. 2022;14(16):3411. doi: 10.3390/nu14163411
  • Heinen CA, Zhang Z, Klieverik LP, et al. Effects of intravenous thyrotropin-releasing hormone on 18F-fluorodeoxyglucose uptake in human brown adipose tissue: a randomized controlled trial. Eur J Endocrinol. 2018;179(1):31–38. doi: 10.1530/EJE-17-0966
  • Bonfante ILP, Monfort-Pires M, Duft RG, et al. Combined training increases thermogenic fat activity in patients with overweight and type 2 diabetes. Int J Obes (Lond). 2022;46(6):1145–1154. doi: 10.1038/s41366-022-01086-3
  • de-Lima-Jùnior JC, Rodovalho S, Van de Sande-Lee S, et al. Effect of pioglitazone treatment on brown adipose tissue volume and activity and hypothalamic gliosis in patients with type 2 diabetes mellitus: a proof-of-concept study. Acta Diabetol. 2019;56(12):1333–1339. doi: 10.1007/s00592-019-01418-2
  • Janssen LGM, Nahon KJ, Bracké KFM, et al. Twelve weeks of exenatide treatment increases [18F]fluorodeoxyglucose uptake by brown adipose tissue without affecting oxidative resting energy expenditure in nondiabetic males. Metabolism. 2020;106:154167. doi: 10.1016/j.metabol.2020.154167
  • Thuzar M, Law WP, Dimeski G, et al. Mineralocorticoid antagonism enhances brown adipose tissue function in humans: a randomized placebo-controlled cross-over study. Diab Obes Metab. 2019;21(3):509–516. doi: 10.1111/dom.13539
  • Martinez-Tellez B, Sanchez-Delgado G, Acosta FM, et al. No evidence of brown adipose tissue activation after 24 weeks of supervised exercise training in young sedentary adults in the ACTIBATE randomized controlled trial. Nat Commun. 2022;13(1):5259. doi: 10.1038/s41467-022-32502-x
  • Xiang AS, Giles C, Loh RKC, et al. Plasma docosahexaenoic acid and eicosapentaenoic acid concentrations are positively associated with brown adipose tissue activity in humans. Metabolites. 2020;10(10):388. doi: 10.3390/metabo10100388
  • Yoneshiro T, Matsushita M, Sugita J, et al. Prolonged treatment with grains of paradise (aframomum melegueta) extract recruits adaptive thermogenesis and reduces body fat in humans with low brown fat activity. J Nutr Sci Vitaminol (Tokyo). 2021;67(2):99–104. doi: 10.3177/jnsv.67.99
  • Laurila S, Sun L, Lahesmaa M, et al. Secretin activates brown fat and induces satiation. Nat Metab. 2021;3(6):798–809. doi: 10.1038/s42255-021-00409-4
  • Li Y, Schnabl K, Gabler SM, et al. Secretin-activated brown fat mediates prandial thermogenesis to induce satiation. Cell. 2018;175(6):1561–1574. doi: 10.1016/j.cell.2018.10.016
  • Sun L, Laurila S, Lahesmaa M, et al. Secretin modulates appetite via brown adipose tissue-brain axis. Eur J Nucl Med Mol Imaging. 2023;50(6):1597–1606. doi: 10.1007/s00259-023-06124-4
  • Zhang Q, Miao Q, Yang Y, et al. Neuropeptide Y plays an important role in the relationship between brain glucose metabolism and brown adipose tissue activity in healthy adults: a PET/CT study. Front Endocrinol. 2021;12:694162. doi: 10.3389/fendo.2021.694162
  • Paulus A, Drude N, Nascimento EBM, et al. [18F]BODIPY-triglyceride-containing chylomicron-like particles as an imaging agent for brown adipose tissue in vivo. Sci Rep. 2019;9(1):2706. doi: 10.1038/s41598-019-39561-z
  • Oh C, Song IH, Lee W, et al. Brown adipose tissue imaging using the TSPO tracer [18F]fluoromethyl-PBR28-d2: a comparison with [18F]FDG. Nucl Med Biol. 2020;90-91:98–103. doi: 10.1016/j.nucmedbio.2020.10.001
  • Niu N, Xing H, Wang X, et al. Comparative [18F]FDG and [18F]DPA714 PET imaging and time-dependent changes of brown adipose tissue in tumour-bearing mice. Adipocyte. 2020;9(1):542–549. doi: 10.1080/21623945.2020.1814546
  • Hartimath SV, Khanapur S, Boominathan R, et al. Imaging adipose tissue browning using the TSPO-18kDa tracer [18F]FEPPA. Mol Metab. 2019;25:154–158. doi: 10.1016/j.molmet.2019.05.003
  • Ran C, Albrecht DS, Bredella MA, et al. PET imaging of human brown adipose tissue with the TSPO tracer [11C]PBR28. Mol Imaging Biol. 2018;20(2):188–193. doi: 10.1007/s11307-017-1129-z
  • Sun L, Aarnio R, Herre EA, et al. [11C]carfentanil PET imaging for studying the peripheral opioid system in vivo: effect of photoperiod on mu-opioid receptor availability in brown adipose tissue. Eur J Nucl Med Mol Imaging. 2023;50(2):266–274. doi: 10.1007/s00259-022-05969-5
  • Goggi JL, Hartimath S, Khanapur S, et al. Imaging adipose tissue Browning using mitochondrial complex-I tracer [18F]BCPP-EF. Contrast Media Mol Imaging. 2022;2022:6113660. doi: 10.1155/2022/6113660
  • Lahesmaa M, Oikonen V, Helin S, et al. Regulation of human brown adipose tissue by adenosine and A2A receptors – studies with [15O]H2O and [11C]TMSX PET/CT. Eur J Nucl Med Mol Imaging. 2019;46(3):743–750. doi: 10.1007/s00259-018-4120-2

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