Glucose Uptake and Perfusion in Subcutaneous and Visceral Adipose Tissue during Insulin Stimulation in Nonobese and Obese Humans
Abstract
To elucidate the role of adipose tissue glucose uptake in whole-body metabolism, sc and visceral adipose tissue glucose uptake and perfusion were measured in 10 nonobese and 10 age-matched obese men with positron emission tomography using [(18)F]-2-fluoro-2-deoxy-D-glucose, and [(15)O]-labeled water during normoglycemic hyperinsulinemia. Whole-body and skeletal muscle glucose uptake rates per kilogram were lower in obese than in nonobese subjects (P < 0.01). Compared with nonobese, the obese subjects had 67% lower abdominal sc and 58% lower visceral adipose tissue glucose uptake per kilogram of fat. In both groups, insulin stimulated glucose uptake per kilogram fat was significantly higher in visceral fat depots than in sc regions (P < 0.01). Both sc and visceral adipose tissue blood flow expressed per kilogram and minute was impaired in the obese subjects, compared with the nonobese (P < 0.05). Fat masses measured with magnetic resonance images were higher in obese than in nonobese individuals. If regional glucose uptake rates were expressed as per total fat mass, total glucose uptake rates per depot were similar in obese and nonobese subjects and represented 4.1% of whole-body glucose uptake in obese and 2.6% in nonobese subjects (P < 0.02 between the groups). In conclusion, insulin-stimulated glucose uptake per kilogram fat is higher in visceral than in sc adipose tissue. Glucose uptake and blood flow in adipose tissue exhibit insulin resistance in obesity, but because of the larger fat mass, adipose tissue does not seem to contribute substantially to the reduced insulin stimulated whole-body glucose uptake in obesity.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Adipose tissue is poorly oxygenated in the obese state in humans.
“This has been verified by recent clinical observations in humans, which suggest that AT is poorly oxygenated in the obese state (20,21).”
From Adipose tissue remodeling and obesity (2011) · cites this paper as [21]
Cites
The publisher hasn’t deposited this paper’s reference list.
Cited by
Sorted by citations
Adipose tissue remodeling and obesity
Sun, K., Kusminski, C. M., & Scherer, P. E. (2011) · Journal of Clinical Investigation · doi:10.1172/jci45887 · Cited by 1,941 · see citing works
The pathogenesis of insulin resistance: integrating signaling pathways and substrate flux
Samuel, V. T., & Shulman, G. I. (2016) · Journal of Clinical Investigation · doi:10.1172/jci77812 · Cited by 1,484 · see citing works
Adipose Tissue Hypoxia in Obesity and Its Impact on Adipocytokine Dysregulation
Hosogai, N., Fukuhara, A., Oshima, K., Miyata, Y., Tanaka, S., Segawa, K., Furukawa, S., Tochino, Y., Komuro, R., Matsuda, M., et al. (2007) · Diabetes · doi:10.2337/db06-0911 · Cited by 1,257 · see citing works
Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome
Maury, E., & Brichard, S. M. (2010) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.07.031 · Cited by 1,026 · see citing works
Hypoxia-Inducible Factor 1α Induces Fibrosis and Insulin Resistance in White Adipose Tissue
Halberg, N., Khan, T., Trujillo, M. E., Wernstedt-Asterholm, I., Attie, A. D., Sherwani, S., Wang, Z. V., Landskroner-Eiger, S., Dineen, S., Magalang, U. J., et al. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.00192-09 · Cited by 896 · see citing works
Lee, M., Wu, Y., & Fried, S. K. (2012) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2012.10.001 · Cited by 804 · see citing works
Fain, J. N. (2006) · Vitamins and hormones · doi:10.1016/s0083-6729(06)74018-3 · Cited by 679 · see citing works
The role of adipose tissue dysfunction in the pathogenesis of obesity-related insulin resistance
Goossens, G. H. (2008) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.10.010 · Cited by 591 · see citing works
Hypoxia in adipose tissue: a basis for the dysregulation of tissue function in obesity?
Trayhurn, P., Wang, B., & Wood, I. S. (2008) · British Journal of Nutrition · doi:10.1017/s0007114508971282 · Cited by 464 · see citing works
Bjørndal, B., Burri, L., Staalesen, V., Skorve, J., & Berge, R. K. (2011) · Journal of Obesity · doi:10.1155/2011/490650 · Cited by 372 · see citing works
Sergi, D., Naumovski, N., Heilbronn, L. K., Abeywardena, M., O’Callaghan, N., Lionetti, L., & Luscombe-Marsh, N. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00532 · Cited by 347 · see citing works
The secretory function of adipocytes in the physiology of white adipose tissue
Wang, P., Mariman, E., Renes, J., & Keijer, J. (2008) · Journal of Cellular Physiology · doi:10.1002/jcp.21386 · Cited by 318 · see citing works
Munukka, E., Rintala, A., Toivonen, R., Nylund, M., Yang, B., Takanen, A., Hänninen, A., Vuopio, J., Huovinen, P., Jalkanen, S., et al. (2017) · The ISME Journal · doi:10.1038/ismej.2017.24 · Cited by 278 · see citing works
Regional impact of adipose tissue morphology on the metabolic profile in morbid obesity
Hoffstedt, J., Arner, E., Wahrenberg, H., Andersson, D. P., Qvisth, V., Löfgren, P., Rydén, M., Thörne, A., Wirén, M., Palmér, M., et al. (2010) · Diabetologia · doi:10.1007/s00125-010-1889-3 · Cited by 246 · see citing works
Selective Inhibition of Hypoxia-Inducible Factor 1α Ameliorates Adipose Tissue Dysfunction
Sun, K., Halberg, N., Khan, M., Magalang, U. J., & Scherer, P. E. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.00951-12 · Cited by 231 · see citing works
Anesthesia in the obese patient: Pharmacokinetic considerations
Casati, A., & Putzu, M. (2005) · Journal of Clinical Anesthesia · doi:10.1016/j.jclinane.2004.01.009 · Cited by 214 · see citing works
Polyphenols and their effects on diabetes management: A review
Aryaeian, N., Sedehi, S. K., & Arablou, T. (2017) · Medical Journal of the Islamic Republic of Iran · doi:10.14196/mjiri.31.134 · Cited by 202 · see citing works
Hypoxia and Adipocyte Physiology: Implications for Adipose Tissue Dysfunction in Obesity
Trayhurn, P. (2014) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-071812-161156 · Cited by 194 · see citing works
Whole body fat: Content and distribution
Thomas, E. L., Fitzpatrick, J. A., Malik, S., Taylor-Robinson, S. D., & Bell, J. D. (2013) · Progress in Nuclear Magnetic Resonance Spectroscopy · doi:10.1016/j.pnmrs.2013.04.001 · Cited by 170 · see citing works
Lundgren, M., Burén, J., Ruge, T., Myrnäs, T., & Eriksson, J. W. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-031157 · Cited by 163 · see citing works
Impact of visceral adipose tissue on liver metabolism
Lafontan, M., & Girard, J. (2008) · Diabetes & Metabolism · doi:10.1016/j.diabet.2008.04.001 · Cited by 143 · see citing works
Honka, M.-J., Latva-Rasku, A., Bucci, M., Virtanen, K. A., Hannukainen, J. C., Kalliokoski, K. K., & Nuutila, P. (2018) · European Journal of Endocrinology · doi:10.1530/eje-17-0882 · Cited by 140 · see citing works
Self-citationThe Vasculature in Prediabetes
Wasserman, D. H., Wang, T. J., & Brown, N. J. (2018) · Circulation Research · doi:10.1161/circresaha.118.311912 · Cited by 137 · see citing works
Hypoxia and the endocrine and signalling role of white adipose tissue
Trayhurn, P., Wang, B., & Wood, I. (2008) · Archives of Physiology and Biochemistry · doi:10.1080/13813450802306602 · Cited by 127 · see citing works
van Woerden, G., van Veldhuisen, D. J., Westenbrink, B. D., de Boer, R. A., Rienstra, M., & Gorter, T. M. (2022) · European Journal of Heart Failure · doi:10.1002/ejhf.2741 · Cited by 128 · see citing works
Increased Glucose Uptake in Visceral Versus Subcutaneous Adipose Tissue Revealed by PET Imaging
Christen, T., Sheikine, Y., Rocha, V. Z., Hurwitz, S., Goldfine, A. B., Di Carli, M., & Libby, P. (2010) · JACC: Cardiovascular Imaging · doi:10.1016/j.jcmg.2010.06.004 · Cited by 120 · see citing works
Macrophages and the Regulation of Adipose Tissue Remodeling
Martinez-Santibañez, G., & Nien-Kai Lumeng, C. (2014) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-071812-161113 · Cited by 111 · see citing works
Ge, Q., Brichard, S. M., Yi, X., & Li, Q. (2014) · Journal of Immunology Research · doi:10.1155/2014/987285 · Cited by 103 · see citing works
The pathophysiology of abdominal adipose tissue depots in health and disease
Walker, G. E., Marzullo, P., Ricotti, R., Bona, G., & Prodam, F. (2014) · Hormone Molecular Biology and Clinical Investigation · doi:10.1515/hmbci-2014-0023 · Cited by 90 · see citing works
Physical Inactivity, Obesity, and Type 2 Diabetes: An Evolutionary Perspective
Eaton, S. B., & Eaton, S. B. (2017) · Research Quarterly for Exercise and Sport · doi:10.1080/02701367.2016.1268519 · Cited by 83 · see citing works
Pan-PPAR agonist beneficial effects in overweight mice fed a high-fat high-sucrose diet
Fernandes‐Santos, C., Carneiro, R. E., Mendonça, L. D. S., Águila, M. B., & Mandarim‐de‐Lacerda, C. A. (2009) · Nutrition · doi:10.1016/j.nut.2008.12.010 · Cited by 63 · see citing works
Gallagher, D., Heshka, S., Kelley, D. E., Thornton, J., Boxt, L., Pi-Sunyer, F. X., Patricio, J., Mancino, J., Clark, J. M., & the MRI Ancillary Study Group of the Look AHEAD Research Group (2014) · Diabetes Care · doi:10.2337/dc14-1585 · Cited by 59 · see citing works
Hodson, L. (2013) · Adipocyte · doi:10.4161/adip.27114 · Cited by 59 · see citing works
Insulin signalling in human adipose tissue
Laviola, L., Perrini, S., Cignarelli, A., & Giorgino, F. (2006) · Archives of Physiology and Biochemistry · doi:10.1080/13813450600736174 · Cited by 51 · see citing works
Biological specificity of visceral adipose tissue and therapeutic intervention
Perrini, S., Leonardini, A., Laviola, L., & Giorgino, F. (2008) · Archives of Physiology and Biochemistry · doi:10.1080/13813450802334752 · Cited by 50 · see citing works
Altered biodistribution on FDG-PET with emphasis on brown fat and insulin effect
Cohade, C. (2010) · Seminars in Nuclear Medicine · doi:10.1053/j.semnuclmed.2010.02.001 · Cited by 47 · see citing works
Wells, T. (2009) · Progress in Lipid Research · doi:10.1016/j.plipres.2009.04.002 · Cited by 46 · see citing works
Raajendiran, A., Krisp, C., Souza, D. P. D., Ooi, G., Burton, P. R., Taylor, R. A., Molloy, M. P., & Watt, M. J. (2021) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00473.2020 · Cited by 42 · see citing works
Anesthetic Pharmacology and the Morbidly Obese Patient
Ingrande, J., & Lemmens, H. J. M. (2012) · Current anesthesiology reports · doi:10.1007/s40140-012-0002-5 · Cited by 38 · see citing works
Honkala, S. M., Motiani, P., Kivelä, R., Hemanthakumar, K. A., Tolvanen, E., Motiani, K. K., Eskelinen, J.-J., Virtanen, K. A., Kemppainen, J., Heiskanen, M. A., et al. (2020) · BMJ Open Diabetes Research & Care · doi:10.1136/bmjdrc-2019-000830 · Cited by 37 · see citing works
Self-citationLacombe, V. A. (2014) · ISRN Veterinary Science · doi:10.1155/2014/409547 · Cited by 37 · see citing works
Mitrou, P., Boutati, E., Lambadiari, V., Maratou, E., Papakonstantinou, A., Komesidou, V., Sidossis, L., Tountas, N., Katsilambros, N., Economopoulos, T., et al. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-2297 · Cited by 28 · see citing works
Resolution of glucose intolerance in long-term high-fat, high-sucrose-fed mice
Kowalski, G. M., Kraakman, M. J., Mason, S. A., Murphy, A. J., & Bruce, C. R. (2017) · Journal of Endocrinology · doi:10.1530/joe-17-0004 · Cited by 27 · see citing works
Chan, P., & Hsieh, P. (2017) · InTech eBooks · doi:10.5772/65458 · Cited by 26 · see citing works
Iozzo, P., Viljanen, A. P. M., Guzzardi, M. A., Laine, H. K., Honka, M., Ferrannini, E., & Nuutila, P. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-3245 · Cited by 18 · see citing works
Self-citationWestergren, H., Danielsson, A., Nyström, F. H., & Strålfors, P. (2005) · Metabolism · doi:10.1016/j.metabol.2005.01.021 · Cited by 18 · see citing works
Insulin action in morbid obesity: a focus on muscle and adipose tissue
Mitrou, P., Raptis, S., & Dimitriadis, G. (2013) · HORMONES · doi:10.14310/horm.2002.1404 · Cited by 15 · see citing works
Metabolic Activity in the Visceral and Subcutaneous Adipose Tissues by FDG-PET/CT in Obese Patients
Monteiro, A. M., Ferreira, G. C., & Duarte, H. (2017) · Acta Médica Portuguesa · doi:10.20344/amp.8712 · Cited by 14 · see citing works
Sutter, P. D., Cock, P. A. J. G. D., Johnson, T. N., Musther, H., Gasthuys, E., & Vermeulen, A. (2023) · Drug Metabolism and Disposition · doi:10.1124/dmd.122.001129 · Cited by 12 · see citing works
Subcutaneous adipose tissue metabolism and pharmacology: a new investigative technique
Martin, E., Brassard, P., Gagnon‐Auger, M., Yale, P., Carpentier, A. C., & Ardilouze, J. (2011) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y11-039 · Cited by 6 · see citing works
Differences Between Subcutaneous and Visceral Adipose Tissues
Lafontan, M. (2012) · Springer eBooks · doi:10.1007/978-2-8178-0343-2_23 · Cited by 6 · see citing works
Liukko, K. E., Oikonen, V., Tolvanen, T., Virtanen, K. A., Viljanen, A. P. M., Sipilä, H. T., Nuutila, P., & lozzo, P. (2007) · The Open Medical Imaging Journal · doi:10.2174/1874347100701010007 · Cited by 5 · see citing works
Self-citationEngeli, S., Skurk, T., Blüher, M., & Klingenspor, M. (2013) · Springer eBooks · doi:10.1007/978-3-642-22855-1_5 · Cited by 3 · see citing works
Lindholm, H. (2014) · Journal of Nuclear Medicine & Radiation Therapy · doi:10.4172/2155-9619.1000167 · Cited by 3 · see citing works
Body Composition Analysis Using Radionuclides
Tzotzas, T., Karanikas, G., & Krassas, G. E. (2012) · Springer eBooks · doi:10.1007/978-1-4419-1788-1_10 · Cited by 3 · see citing works
The Role of Hypoxia in Adipocyte Function and Dysfunction
Trayhurn, P., de Heredia, F. P., Wang, B., & Wood, I. S. (2010) · Research and perspectives in endocrine interactions · doi:10.1007/978-3-642-13517-0_4 · Cited by 3 · see citing works
Kaur, K. K. (2022) · Advances in Obesity Weight Management & Control · doi:10.15406/aowmc.2022.12.00367 · Cited by 4 · see citing works
ADGRG6 promotes adipogenesis and is involved in sex-specific fat distributionPreprint
Nguyen, H. P., Ushiki, A., Sheng, R. R., Biellak, C., An, K., Choquet, H., Hoffman, T. J., Gray, R. S., & Ahituv, N. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.24.497411 · Cited by 2 · see citing works
Différences entre tissu adipeux sous-cutané et tissu adipeux viscéral
Lafontan, M. (2013) · Springer eBooks · doi:10.1007/978-2-8178-0332-6_23 · Cited by 1 · see citing works
Macrophages – The Key Actors in Adipose Tissue Remodeling and Dysfunction
Stojanović, S., & Najman, S. J. (2016) · InTech eBooks · doi:10.5772/62152 · Cited by 1 · see citing works
Exosomes as Crucial Player in Insulin Resistance and Obesity: Potential Therapeutic Approach
Sood, S., Devi, S., Singh, T. G., Yadav, N., Kumar, P., & Chatterjee, A. (2022) · International Journal of Pharmaceutical Quality Assurance · doi:10.25258/ijpqa.13.4.26 · Cited by 1 · see citing works
Metformin: A Drug of Choice for Gestational Diabetes Mellitus in Near Future- Hope or Despair?
Alam, A. T., & Ahmed, S. S. (2015) · Chattagram Maa-O-Shishu Hospital Medical College Journal · doi:10.3329/cmoshmcj.v14i2.25722
18f-Fluorodeoxyglucose PET/CT Can Be an Alternative Method to Assessment of Insulin Resistance
Tuzcu, Ş. A. (2019) · Acta Endocrinologica (Bucharest) · doi:10.4183/aeb.2019.539
Components of Metabolic Syndrome
(2007) · Springer eBooks · doi:10.1007/978-1-84628-911-8_2
Silva, D. A. S., Recabarren, S. E., Bellalta, S., & Mansilla, D. M. R. (2022) · Journal of Agricultural Sciences Research (2764-0973) · doi:10.22533/at.ed.97321222230910
Body fat distribution and obesity
Lempesis, I. G. (2023) · doi:10.26481/dis.20231019ll · Cited by 1 · see citing works
Lan, Z., Lei, Z. M., Nation, L., Li, X., Zhao, Z., Eastridge, K., Belin, S., Reddy, Y. T., Yiannikouris, A., & Power, R. F. (2024) · Journal of Diabetes and Treatment · doi:10.29011/2574-7568.010125
- Authors
- Virtanen, K. A., Lönnroth, P., Parkkola, R., Peltoniemi, P., Asola, M., Viljanen, T., Tolvanen, T., Knuuti, J., Rönnemaa, T., Huupponen, R., & Nuutila, P.
- Affiliations
- University of Turku (FI)
- University of Gothenburg (SE)
- Turku PET Centre (FI)
- Corresponding author
- Nuutila, Pirjo
- ORCID
- Venue
- The Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 2002-08
- Volume
- 87
- Issue
- 8
- Pages
- 3902-3910
- ISSN
- 0021-972X (ISSN-L)
- 1945-7197
- OpenAlex
- W2117731142
- Cited by
- 315
- References
- 0
- Citations by year
- 2026: 8 · 2025: 6 · 2024: 13 · 2023: 14 · 2022: 20 · 2021: 14 · 2020: 19 · 2019: 13 · 2018: 14 · 2017: 23 · 2016: 12 · 2015: 11 · 2014: 19 · 2013: 18 · 2012: 13
- FWCI
- 5.81
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Disease and Adiposity
- Keywords
- adipose tissue glucose uptake, subcutaneous adipose tissue, visceral adipose tissue, insulin resistance, obesity, hyperinsulinemic-euglycemic clamp, skeletal muscle glucose uptake, whole-body glucose uptake, adipose tissue blood flow, fat mass
- MeSH terms
- Abdomen, Adipose Tissue, Adult, Glucose, Homeostasis, Humans, Hypoglycemic Agents, Insulin, Insulin Resistance, Magnetic Resonance Imaging, Male, Obesity, Regional Blood Flow, Skin, Tomography, Emission-Computed, Muscle, Skeletal, Radiopharmaceuticals, Fluorodeoxyglucose F18
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review