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Mapping of human brown adipose tissue in lean and obese young men
Open accessAbstract
F-labeled fluorodeoxyglucose positron emission tomography/computerized tomography (PET/CT). Obese men had less activated BAT than lean men (mean, 130 vs. 334 mL) but more fat in BAT-containing depots (mean, 1,646 vs. 855 mL) with a wide range (0.1-71%) in the ratio of activated BAT to inactive fat between individuals. Six anatomic regions had activated BAT-cervical, supraclavicular, axillary, mediastinal, paraspinal, and abdominal-with 67 ± 20% of all activated BAT concentrated in a continuous fascial layer comprising the first three depots in the upper torso. These nonsubcutaneous fat depots amounted to 1.5% of total body mass (4.3% of total fat mass), and up to 90% of each depot could be activated BAT. The amount and activity of BAT was significantly influenced by region of interest selection methods, PET threshold criteria, and PET resolutions. The present study suggests that active BAT can be found in specific adipose depots in adult humans, but less than one-half of the fat in these depots is stimulated by acute cold exposure, demonstrating a previously underappreciated thermogenic potential.
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“The role of BAT in adult humans is controversial since its detection is dependent upon the approach employed (Leitner et al., 2017; Porter et al., 2016; van Marken Lichtenbelt et al., 2009).”
From Origin and function of stress-induced IL-6 in murine models (2020) · cites this paper as Leitner et al., 2017
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Deciphering the cellular interplays underlying obesity-induced adipose tissue fibrosis
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“Recently, a study showed a much wider distribution of BAT, including in the abdominal subcutaneous regions, in adult humans by refined 18F-FDG-PET/CT imaging (17).”
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“White adipose tissue has a key role in energy storage and energy production and accounts for approximately 95% of total adipose mass in adults 100 .”
Baskin, A. S., Linderman, J. D., Brychta, R. J., McGehee, S., Anflick-Chames, E., Cero, C., Johnson, J. W., O’Mara, A. E., Fletcher, L. A., Leitner, B. P., et al. (2018) · Diabetes · doi:10.2337/db18-0462 · Cited by 145
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InfluentialHuman Bone Marrow Is Comprised of Adipocytes with Specific Lipid Metabolism
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“We have not done PET / CT but instead PET / MR and therefore do not have the opportunity to use HU to delimit BAT.”
InfluentialYabut, J. M., Desjardins, E. M., Chan, E. J., Day, E. A., Leroux, J. M., Wang, B., Crane, E. D., Wong, W., Morrison, K. M., Crane, J. D., et al. (2020) · Nature Communications · doi:10.1038/s41467-019-14080-7 · Cited by 64
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Magnetic Resonance Imaging Techniques for Brown Adipose Tissue Detection
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“Specifically, inactive BAT will not be identified in 18F-FDG PET scans, while different degrees of BAT activation, coupled with the poor test–retest reliability of FDG PET/CT in measuring BAT glucose metabolism (16), is expected to lead to a great variation in estimates of BAT volumes, from as low as 10ml (17) to as m…”
BackgroundLee‐Rueckert, M., Canyelles, M., Tondo, M., Rotllán, N., Kovanen, P. T., Llorente‐Cortés, V., & Escolá‐Gil, J. C. (2023) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2023.05.002 · Cited by 68
The evolving view of thermogenic fat and its implications in cancer and metabolic diseases
Yin, X., Chen, Y., Ruze, R., Xu, R., Song, J., Wang, C., & Xu, Q. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01178-6 · Cited by 72
“Consistently, investigators found that lean men had more activated BAT than obese men by using (18)F-FDG-PET/CT.(29) The reason for the reduced thermogenesis in obesity is that B lymphocytes and macrophages infiltrate thermogenic fat, and subsequently suppress UCP1 expression via releasing tumor necrosis factor-α (TNF…”
BackgroundMethodMaurer, S., Harms, M., & Boucher, J. (2020) · FEBS Journal · doi:10.1111/febs.15470 · Cited by 65
Brain to bone: What is the contribution of the brain to skeletal homeostasis?
Idelevich, A., & Baron, R. (2018) · Bone · doi:10.1016/j.bone.2018.05.018 · Cited by 62
Brown fat activation mitigates alcohol-induced liver steatosis and injury in mice
Shen, H., Jiang, L., Lin, J. D., Omary, M. B., & Rui, L. (2019) · Journal of Clinical Investigation · doi:10.1172/jci124376 · Cited by 62
Law, J., Chalmers, J., Morris, D. E., Robinson, L., Budge, H., & Symonds, M. E. (2017) · Temperature · doi:10.1080/23328940.2017.1397085 · Cited by 65
“In addition, the amount of BAT identified depends on external factors such as PET resolution, the region of interest (ROI) chosen and the PET threshold criteria and may have been being significantly underestimated.(11) Larger studies can be undertaken by looking at images taken for clinical indications but conditions…”
BackgroundWang, X., Rao, H., Liu, F., Wei, L., Li, H., & Wu, C. (2021) · Cells · doi:10.3390/cells10123300 · Cited by 66
The weight of nutrients: kynurenine metabolites in obesity and exercise
Dadvar, S., Ferreira, D. M. S., Červenka, I., & Ruas, J. L. (2018) · Journal of Internal Medicine · doi:10.1111/joim.12830 · Cited by 59
Janssen, L. G. M., Nahon, K. J., Bracké, K. F. M., van den Broek, D., Smit, R., Sardjoe Mishre, A. S. D., Koorneef, L. L., Martinez-Tellez, B., Burakiewicz, J., Kan, H. E., et al. (2020) · Metabolism · doi:10.1016/j.metabol.2020.154167 · Cited by 54
A New Personalized Cooling Protocol to Activate Brown Adipose Tissue in Young Adults
Martínez‐Téllez, B., Sánchez‐Delgado, G., García‐Rivero, Y., Alcántara, J. M. A., Martinez-Avila, W. D., Muñoz-Hernandez, M. V., Olza, J., Boon, M. R., Rensen, P. C. N., Elvira, J. M. L., et al. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00863 · Cited by 59
“Nevertheless, most of the BAT depots detected in humans are localized in the areas covered by our scan (Nedergaard et al., 2007; Leitner et al., 2017).”
BackgroundBeige Fat Maintenance; Toward a Sustained Metabolic Health
Rabiee, A. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00634 · Cited by 53
Brown Fat as a Regulator of Systemic Metabolism beyond Thermogenesis
Okamatsu‐Ogura, Y., & Saito, M. (2021) · Diabetes & Metabolism Journal · doi:10.4093/dmj.2020.0291 · Cited by 55
“This discrepant result may be caused by FDG-PET which underestimated the total mass of BAT [100].”
BackgroundBrown adipose tissue and regulation of human body weight
Harb, E., Kheder, O., Poopalasingam, G., Rashid, R., Srinivasan, A., & Izzi‐Engbeaya, C. N. (2022) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.3594 · Cited by 53
“This is supported by the finding that basal and cold‐induced fatty acid uptake by BAT is impaired in obesity.30 Leitner et al.31 also reported that lean men (mean BMI = 23.2) had over twice the amount of activated BAT compared to obese men (mean BMI = 34.8).”
BackgroundInfluentialBartke, A., Brannan, S., Hascup, E. R., Hascup, K. N., & Darcy, J. (2020) · The World Journal of Men s Health · doi:10.5534/wjmh.200112 · Cited by 52
“The results of a recent study of the effects of outdoor temperatures showed that the energy expenditure and the skin temperature of the supraclavicular region increased with cold exposure [59].”
BackgroundMartínez‐Téllez, B., Nahon, K. J., Sánchez‐Delgado, G., Abreu-Vieira, G., Elvira, J. M. L., van Velden, F. H. P., Arias‐Bouda, L. M. P., Rensen, P. C. N., Boon, M. R., & Ruiz, J. R. (2018) · Scientific Reports · doi:10.1038/s41598-018-26878-4 · Cited by 51
Wyckelsma, V. L., Venckūnas, T., Houweling, P. J., Schlittler, M., Lauschke, V. M., Tiong, C. F., Wood, H. D., Ivarsson, N., Paulauskas, H., Eimantas, N., et al. (2021) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2021.01.013 · Cited by 51
Sun, L., Verma, S. K., Michael, N., Chan, S. P., Yan, J., Sadananthan, S. A., Camps, S. G., Goh, H. J., Govindharajulu, P., Totman, J. J., et al. (2019) · Obesity · doi:10.1002/oby.22560 · Cited by 49
“In adult humans, the dominant area of BAT is in the supraclavicular region (6,7).”
BackgroundMcNeill, B. T., Suchacki, K. J., & Stimson, R. H. (2021) · European Journal of Endocrinology · doi:10.1530/eje-20-1439 · Cited by 55
“1) (15, 16, 17).”
Huber, K., Hofer, D., Trefely, S., Pelzmann, H. J., Madreiter‐Sokolowski, C. T., Duta-Mare, M., Schlager, S., Trausinger, G., Stryeck, S., Graier, W. F., et al. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2018.08.017 · Cited by 49
“The more recent discovery of significant amounts of metabolically active BAT in adult humans has revealed additional roles for BAT in the maintenance of energy homeostasis [16,17].”
BackgroundEffects of Caffeine on Brown Adipose Tissue Thermogenesis and Metabolic Homeostasis: A Review
Schaik, L. V., Kettle, C., Green, R., Irving, H. R., & Rathner, J. A. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.621356 · Cited by 50
Sexual Dimorphisms in Adult Human Brown Adipose Tissue
Fletcher, L. A., Kim, K. K., Leitner, B. P., Cassimatis, T. M., O’Mara, A. E., Johnson, J. W., Halprin, M. S., McGehee, S., Brychta, R. J., Cypess, A. M., et al. (2020) · Obesity · doi:10.1002/oby.22698 · Cited by 48
“We then applied a previously established CT Hounsfield unit threshold (−300 to −10) and an individualized PET threshold normalized to a lean body mass/ total body mass ratio (8) to define active BAT voxels, and after applying this normalization, we verified that mean 18F-FDG standardized uptake values (SUVs) of three…”
MethodInfluentialTakeda, Y., Harada, Y., Yoshikawa, T., & Dai, P. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24021352 · Cited by 49
“Human BAT is sporadically distributed in cervical, supraclavicular, paraspinal, and abdominal adipose depots [44] (Figure 2).”
BackgroundAutophagy in Adipocyte Browning: Emerging Drug Target for Intervention in Obesity
Ro, S., Jang, Y., Bae, J., Kim, I. M., Schaecher, C., & Shomo, Z. D. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00022 · Cited by 47
“Several studies using positron emission tomography (PET)-CT have demonstrated that, in addition to size reduction in aging, BAT activity is reduced in obese and diabetic patients (Lee et al., 2010; Leitner et al., 2017).”
BackgroundCurrent Status of Obesity: Protective Role of Catechins
Basu, T., Selman, A., Reddy, A. P., & Reddy, P. H. (2023) · Antioxidants · doi:10.3390/antiox12020474 · Cited by 48
“Brown adipocytes have multiple, small lipid droplets and a plethora of mitochondria, which gives BAT a brown color and a multilocular histological appearance [50,51].”
BackgroundFatty acid activation in thermogenic adipose tissue
Steensels, S., & Ersoy, B. A. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2018.05.008 · Cited by 48
Fan, R., Toney, A. M., Jang, Y., Ro, S., & Chung, S. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2018.09.008 · Cited by 45
“5% of total body mass (roughly 5% of total fat mass), and up to 90% depots could be activated BAT [13].”
BackgroundPace, N. P., Vassallo, J., & Calleja‐Agius, J. (2020) · Early Human Development · doi:10.1016/j.earlhumdev.2020.105219 · Cited by 44
Human adipose depots’ diverse functions and dysregulations during cardiometabolic disease
Ziegler, A. K., & Schéele, C. (2024) · npj Metabolic Health and Disease · doi:10.1038/s44324-024-00036-z · Cited by 47
Abnormal brown adipose tissue mitochondrial structure and function in IL10 deficiency
Júnior, J. C. D. L., de Souza, G. F. P., Moura‐Assis, A., Gaspar, R. S., Gaspar, J. M., Rocha, A. L. S., Ferrucci, D. L., de Lima, T. I., Victorio, S. C. D. S., Bonfante, I. L. P., et al. (2018) · EBioMedicine · doi:10.1016/j.ebiom.2018.11.041 · Cited by 45
“The free PET/CT plug-in was developed for BAT evaluation by Beth Israel Deaconess Medical Center [37].”
MethodInfluentialHuo, C., Song, Z., Yin, J., Zhu, Y., Miao, X., Qian, H., Wang, J., Ye, L., & Zhou, L. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.917084 · Cited by 46
“Acute cold exposure (1–48 h) increased glucose uptake and improved insulin sensitivity; and free fatty acids (FFA) uptake and metabolism also increased in BAT(Ouellet et al., 2012; Leitner et al., 2017).”
BackgroundLu, S., & Cao, Z. (2023) · Nutrients · doi:10.3390/nu15224832 · Cited by 46
“In the human body, BAT has relatively little quantity and is selectively distributed in specific anatomical parts, such as the neck and scapula [62].”
BackgroundNeural circuits of long-term thermoregulatory adaptations to cold temperatures and metabolic demands
Mota, C. M. D., & Madden, C. J. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-023-00785-8 · Cited by 42
“BAT activity, as indicated by glucose uptake in humans 140–143 and sympathetic activity in rodents 14–16 , is enhanced in those who are non-obese but low in individuals who are obese during acute cold exposure.”
InfluentialHuman brown adipose tissue: Underestimated target in metabolic disease?
Moonen, M. P. B., Nascimento, E. B. M., & Lichtenbelt, W. D. V. M. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2018.05.012 · Cited by 43
Quantification of the Capacity for Cold-Induced Thermogenesis in Young Men With and Without Obesity
Brychta, R. J., Huang, S., Wang, J., Leitner, B. P., Hattenbach, J. D., Bell, S. L., Fletcher, L. A., Wood, R. P., Idelson, C. R., Duckworth, C. J., et al. (2019) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2019-00728 · Cited by 44
Metadata
- Authors
- Leitner, B. P., Huang, S., Brychta, R. J., Duckworth, C. J., Baskin, A. S., McGehee, S., Tal, I., Dieckmann, W., Gupta, G., Kolodny, G. M., Pacak, K., Herscovitch, P., Cypess, A. M., & Chen, K. Y.
- Affiliations
- National Institutes of Health (US)
- Beth Israel Deaconess Medical Center (US)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2017-07-24
- Volume
- 114
- Issue
- 32
- Pages
- 8649-8654
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC5559032
- OpenAlex
- W2736913806
- Cited by
- 530
- References
- 43
- Citations by year
- 2026: 36 · 2025: 45 · 2024: 51 · 2023: 68 · 2022: 73 · 2021: 82 · 2020: 73 · 2019: 45 · 2018: 46 · 2017: 9
- FWCI
- 34.99
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- HHS | NIH | National Institute of Diabetes and Digestive and Kidney Diseases (Z01 DK071014, Z01 DK075116)
- Topics
- Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Disease and Adiposity
- Keywords
- brown adipose tissue, obesity, cold exposure, thermogenesis, BAT activation
- MeSH terms
- Adult, Adipose Tissue, Brown, Humans, Male, Obesity, Tomography, X-Ray Computed, Body Mass Index, Glucose-6-Phosphate, Positron-Emission Tomography, Adiposity
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