Adipose tissue quantification by imaging methods: a proposed classification.

Recent advances in imaging techniques and understanding of differences in the molecular biology of adipose tissue has rendered classical anatomy obsolete, requiring a new classification of the topography of adipose tissue. Adipose tissue is one of the largest body compartments, yet a classification that defines specific adipose tissue depots based on their anatomic location and related functions is lacking. The absence of an accepted taxonomy poses problems for investigators studying adipose tissue topography and its functional correlates. The aim of this review was to critically examine the literature on imaging of whole body and regional adipose tissue and to create the first systematic classification of adipose tissue topography. Adipose tissue terminology was examined in over 100 original publications. Our analysis revealed inconsistencies in the use of specific definitions, especially for the compartment termed "visceral" adipose tissue. This analysis leads us to propose an updated classification of total body and regional adipose tissue, providing a well-defined basis for correlating imaging studies of specific adipose tissue depots with molecular processes.

[1]  C S Poon,et al.  Fat/water quantitation and differential relaxation time measurement using chemical shift imaging technique. , 1989, Magnetic resonance imaging.

[2]  A. Rissanen,et al.  Relation between Plasma Leptin Levels and Measures of Body Fat in Identical Twins Discordant for Obesity , 1997, Annals of Internal Medicine.

[3]  M. Elia,et al.  Assessment of limb muscle and adipose tissue by dual-energy X-ray absorptiometry using magnetic resonance imaging for comparison , 1999, International Journal of Obesity.

[4]  J. Vague,et al.  The degree of masculine differentiation of obesities: a factor determining predisposition to diabetes, atherosclerosis, gout, and uric calculous disease. , 1956, The American journal of clinical nutrition.

[5]  R. Ross,et al.  Sex differences in lean and adipose tissue distribution by magnetic resonance imaging: anthropometric relationships. , 1994, The American journal of clinical nutrition.

[6]  S. Yanovski,et al.  Differences in body composition of black and white girls. , 1996, The American journal of clinical nutrition.

[7]  Michael J. Ackerman,et al.  Technical Milestone: The visible Human Male: A Technical Report , 1996, J. Am. Medical Informatics Assoc..

[8]  Robert Ross,et al.  Magnetic resonance imaging provides new insights into the characterization of adipose and lean tissue distribution , 1996 .

[9]  G. Watts,et al.  Effects of diet and serotonergic agonist on hepatic apolipoprotein B-100 secretion and endothelial function in obese men. , 2000, QJM : monthly journal of the Association of Physicians.

[10]  Sidney I. Landau,et al.  International Dictionary of Medicine and Biology , 1986 .

[11]  C. Bouchard,et al.  The influence of anatomical boundaries, age, and sex on the assessment of abdominal visceral fat. , 1997, Obesity research.

[12]  E. Evans,et al.  Effects of HRT and exercise training on insulin action, glucose tolerance, and body composition in older women. , 2001, Journal of applied physiology.

[13]  J. Seidell,et al.  Reproducibility of fat area measurements in young, non-obese subjects by computerized analysis of magnetic resonance images , 1997, International Journal of Obesity.

[14]  S. Heymsfield,et al.  The five-level model: a new approach to organizing body-composition research. , 1992, The American journal of clinical nutrition.

[15]  D. Matthews,et al.  Systemic resistance to the antilipolytic effect of insulin in black and white women with visceral obesity. , 1999, American journal of physiology. Endocrinology and metabolism.

[16]  H. Koppeschaar,et al.  Adipose tissue assessed by magnetic resonance imaging in growth hormone-deficient adults: the effect of growth hormone replacement and a comparison with control subjects. , 1995, The American journal of clinical nutrition.

[17]  C Boesch,et al.  Observation of Intramyocellular Lipids by1H‐Magnetic Resonance Spectroscopy , 2000, Annals of the New York Academy of Sciences.

[18]  P. Björntorp.  "Portal" adipose tissue as a generator of risk factors for cardiovascular disease and diabetes. , 1990, Arteriosclerosis.

[19]  L. Sjöström,et al.  Adipose tissue volume determinations in women by computed tomography: technical considerations. , 1986, International journal of obesity.

[20]  J. Vague.  The degree of masculine differentiation of obesities: a factor determining predisposition to diabetes, atherosclerosis, gout, and uric calculous disease. 1956. , 1999, Nutrition.

[21]  S. Levin,et al.  Estimation of body fat and lean tissue distribution by dual energy X-ray absorptiometry and abdominal body fat evaluation by computed tomography in Cushing's disease. , 1995, The Journal of clinical endocrinology and metabolism.

[22]  E. Poehlman,et al.  Obesity, body fat distribution, and coronary artery disease. , 2000, Journal of cardiopulmonary rehabilitation.

[23]  R Guardo,et al.  Quantification of adipose tissue by MRI: relationship with anthropometric variables. , 1992, Journal of applied physiology.

[24]  A. Sbarbati,et al.  In-vivo quantitative hydrolipidic map of perirenal adipose tissue by chemical shift imaging at 4.7 Tesla , 2001, International Journal of Obesity.

[25]  L. Ploutz-Snyder,et al.  Abdominal fat distribution in pre- and postmenopausal women: The impact of physical activity, age, and menopausal status. , 2001, Metabolism: clinical and experimental.

[26]  W E Reddick,et al.  Fast adipose tissue (FAT) assessment by MRI. , 2000, Magnetic resonance imaging.

[27]  M. Salgarello,et al.  Rationale of subdermal superficial liposuction related to the anatomy of subcutaneous fat and the superficial fascial system , 2004, Aesthetic Plastic Surgery.

[28]  Joanne Brown,et al.  Elevated concentrations of free fatty acids are associated with increased insulin response to standard glucose challenge in human immunodeficiency virus-infected subjects with fat redistribution. , 2002, Metabolism: clinical and experimental.

[29]  C. Bouchard,et al.  Role of Deep Abdominal Fat in the Association Between Regional Adipose Tissue Distribution and Glucose Tolerance in Obese Women , 1989, Diabetes.

[30]  S. Kosuda,et al.  Relation of abdominal and thigh adipose tissue distribution to serum lipids and glucose metabolism in obese males. , 1997, Journal of atherosclerosis and thrombosis.

[31]  D. Chisholm,et al.  Regional intra-subject variability in abdominal adiposity limits usefulness of computed tomography. , 2002, Obesity research.

[32]  J. Simoneau,et al.  Skeletal muscle utilization of free fatty acids in women with visceral obesity. , 1995, The Journal of clinical investigation.

[33]  R. Ross.  Magnetic Resonance Imaging (MRI): Data Acquisition and Applications in Human Body Composition , 2000 .

[34]  J. Albu,et al.  Insulin sensitivity and serum triglyceride level in obese white and black women: relationship to visceral and truncal subcutaneous fat. , 1999, Metabolism: clinical and experimental.

[35]  J V Hajnal,et al.  Development of a Rapid and Efficient Magnetic Resonance Imaging Technique for Analysis of Body Fat Distribution , 1996, NMR in biomedicine.

[36]  R. Pereira,et al.  Factors associated with overweight and central body fat in the city of Rio de Janeiro: results of a two-stage random sampling survey. , 2001, Public health.

[37]  P. Björntorp.  Abdominal obesity and the metabolic syndrome. , 1992, Annals of medicine.

[38]  J. Beattie,et al.  Physiological role of adipose tissue: white adipose tissue as an endocrine and secretory organ , 2001, Proceedings of the Nutrition Society.

[39]  J. Weissfeld,et al.  Sagittal diameter in comparison with single slice CT as a predictor of total visceral adipose tissue volume , 1998, International Journal of Obesity.

[40]  A. Shuldiner,et al.  Resistin, obesity, and insulin resistance--the emerging role of the adipocyte as an endocrine organ. , 2001, The New England journal of medicine.

[41]  T. Fukunaga,et al.  Use of B-mode ultrasound for visceral fat mass evaluation: comparisons with magnetic resonance imaging. , 1995, Applied human science : journal of physiological anthropology.

[42]  J. Hajnal,et al.  Preferential loss of visceral fat following aerobic exercise, measured by magnetic resonance imaging , 2000, Lipids.

[43]  W. Totty,et al.  Measurement of fat distribution by magnetic resonance imaging. , 1989, Investigative radiology.

[44]  Comparisons between fat measurements by dual-energy X-ray absorptiometry, underwater weighing and magnetic resonance imaging in healthy women. , 1996, European journal of clinical nutrition.

[45]  E. Giltay,et al.  Visceral fat accumulation is an important determinant of PAI-1 levels in young, nonobese men and women: modulation by cross-sex hormone administration. , 1998, Arteriosclerosis, thrombosis, and vascular biology.

[46]  R M Peshock,et al.  Estimation of adipose tissue mass by magnetic resonance imaging: validation against dissection in human cadavers. , 1994, Journal of lipid research.

[47]  W. Hinson,et al.  Contribution of visceral fat mass to the insulin resistance of aging. , 1995, Metabolism: clinical and experimental.

[48]  J. Tobin,et al.  Interrelationship of spontaneous growth hormone axis activity, body fat, and serum lipids is healthy elderly women and men☆ , 1999 .

[49]  G. Mcneill,et al.  Usefulness of anthropometry and DXA in predicting intra-abdominal fat in obese men and women. , 2000, Obesity research.

[50]  W. S. Snyder,et al.  Report of the task group on reference man , 1979, Annals of the ICRP.

[51]  G. Sergi,et al.  Visceral fat loss evaluated by total body magnetic resonance imaging in obese women operated with laparascopic adjustable silicone gastric banding , 2000, International Journal of Obesity.

[52]  A. Bigard,et al.  Combined effects of caloric restriction and branched-chain amino acid supplementation on body composition and exercise performance in elite wrestlers. , 1997, International journal of sports medicine.

[53]  Jimmy D Bell,et al.  Changes in adipose tissue composition in malnourished patients before and after liver transplantation: A carbon‐13 magnetic resonance spectroscopy and gas‐liquid chromatography study , 1997, Hepatology.

[54]  A. Kissebah,et al.  Regional adiposity and morbidity. , 1994, Physiological reviews.

[55]  P. Björntorp.  Classification of obese patients and complications related to the distribution of surplus fat. , 1987, The American journal of clinical nutrition.

[56]  B. Goodpaster,et al.  Subdivisions of subcutaneous abdominal adipose tissue and insulin resistance. , 2000, American journal of physiology. Endocrinology and metabolism.

[57]  A. Dixon,et al.  Computed Tomographic Observations on Subcutaneous Fat: Implications for Liposuction , 1996, Plastic and reconstructive surgery.

[58]  R. Ross,et al.  Influence of diet and exercise on skeletal muscle and visceral adipose tissue in men. , 1996, Journal of applied physiology.

[59]  R G Hoffmann,et al.  Relationship of body fat topography to insulin sensitivity and metabolic profiles in premenopausal women. , 1984, Metabolism: clinical and experimental.

[60]  J. Seidell,et al.  Imaging techniques for measuring adipose-tissue distribution--a comparison between computed tomography and 1.5-T magnetic resonance. , 1990, The American journal of clinical nutrition.

[61]  M. Visser,et al.  Abdominal diameters as indicators of visceral fat: comparison between magnetic resonance imaging and anthropometry , 1993, British Journal of Nutrition.

[62]  Rebecca B. Costello,et al.  Imaging Techniques of Body Composition: Advantages of Measurement and New Uses , 1997 .

[63]  J V Hajnal,et al.  Magnetic resonance imaging of total body fat. , 1998, Journal of applied physiology.

[64]  L. Groop,et al.  Relationship between abdominal fat compartments and glucose and lipid metabolism in early postmenopausal women. , 2001, The Journal of clinical endocrinology and metabolism.

[65]  J. Rood,et al.  Comparison of regional fat distribution and health risk factors in middle-aged white and African American women: The Healthy Transitions Study. , 2001, Obesity research.

[66]  B. Rosen,et al.  Overall body fat and regional fat distribution in young women: quantification with MR imaging. , 1991, AJR. American journal of roentgenology.

[67]  G. Bray,et al.  Contributions of total body fat, abdominal subcutaneous adipose tissue compartments, and visceral adipose tissue to the metabolic complications of obesity. , 2001, Metabolism: clinical and experimental.

[68]  A. Rogol,et al.  Alterations in body composition and fat distribution in growth hormone-deficient prepubertal children during growth hormone therapy. , 2001, Metabolism: clinical and experimental.

[69]  B. Strauss,et al.  The metabolic effects of preferential reduction of visceral adipose tissue in abdominally obese men , 1998, International Journal of Obesity.

[70]  R. Ross,et al.  Visceral adiposity, androgens, and plasma lipids in obese men. , 1994, Metabolism: clinical and experimental.

[71]  H. Koppeschaar,et al.  Magnetic resonance imaging-assessed adipose tissue and serum lipid and insulin concentrations in growth hormone-deficient adults. Effect of growth hormone replacement. , 1995, Arteriosclerosis, thrombosis, and vascular biology.

[72]  M J Ackerman,et al.  The Visible Human Project , 1998, Proc. IEEE.

[73]  J. Seidell,et al.  Techniques for the measurement of visceral fat: a practical guide. , 1993, International journal of obesity and related metabolic disorders : journal of the International Association for the Study of Obesity.

[74]  S. Welle,et al.  The effects of weight reduction to ideal body weight on body fat distribution. , 1995, Metabolism: clinical and experimental.

[75]  R. Ross,et al.  Separate Associations Between Visceral and Subcutaneous Adipose Tissue Distribution, Insulin and Glucose Levels in Obese Women , 1996, Diabetes Care.

[76]  C. Pichard,et al.  Age-related differences in fat-free mass, skeletal muscle, body cell mass and fat mass between 18 and 94 years , 2001, European Journal of Clinical Nutrition.

[77]  C. Bouchard,et al.  Major gene effect on subcutaneous fat distribution in a sedentary population and its response to exercise training: The HERITAGE Family Study , 2000, American journal of human biology : the official journal of the Human Biology Council.

[78]  S. Heymsfield,et al.  Fat distribution in HIV-infected patients reporting truncal enlargement quantified by whole-body magnetic resonance imaging. , 1999, The American journal of clinical nutrition.

[79]  L. Sjöström,et al.  Total and visceral adipose-tissue volumes derived from measurements with computed tomography in adult men and women: predictive equations. , 1988, The American journal of clinical nutrition.

[80]  R. Ross,et al.  Effects of aerobic or resistance exercise and/or diet on glucose tolerance and plasma insulin levels in obese men. , 1999, Diabetes care.

[81]  E. Wu,et al.  High-resolution magnetic resonance imaging tracks changes in organ and tissue mass in obese and aging rats. , 2002, American journal of physiology. Regulatory, integrative and comparative physiology.

[82]  Enzo Bonora,et al.  Measurement of abdominal fat with T1‐weighted MR images , 1991, Journal of magnetic resonance imaging : JMRI.

[83]  A. Bigard,et al.  Evaluation of abdominal fat distribution in noninsulin-dependent diabetes mellitus: relationship to insulin resistance. , 1998, The Journal of clinical endocrinology and metabolism.

[84]  T. Kooistra,et al.  Relationship between Visceral Fat and PAI-1 in Overweight Men and Women before and after Weight Loss , 1999, Thrombosis and Haemostasis.

[85]  P. Vanderburgh.  Fat distribution: its physiological significance, health implications, and its adaptation to exercise training. , 1992, Military medicine.

[86]  M. Bernardino,et al.  Abdominal composition quantified by computed tomography. , 1988, The American journal of clinical nutrition.

[87]  J. Lancaster,et al.  Is it possible to derive a reliable estimate of human visceral and subcutaneous abdominal adipose tissue from simple anthropometric measurements? , 1995, Metabolism: clinical and experimental.

[88]  C. Lam,et al.  Body fatness and serum lipids of 11‐year‐old Chinese children , 1998, Acta paediatrica.

[89]  B. Wajchenberg.  Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. , 2000, Endocrine reviews.

[90]  J. Chan,et al.  Visceral Fat and Cardiovascular Risk Factors in Chinese NIDDM Patients , 1997, Diabetes Care.

[91]  R. Ross,et al.  Mobilization of visceral and subcutaneous adipose tissue in response to energy restriction and exercise. , 1994, The American journal of clinical nutrition.

[92]  R. Brummer,et al.  Effects of growth hormone treatment on visceral adipose tissue. , 1998, Growth hormone & IGF research : official journal of the Growth Hormone Research Society and the International IGF Research Society.

[93]  A. Rissanen,et al.  Glucose metabolism in identical twins discordant for obesity. The critical role of visceral fat. , 1997, The Journal of clinical endocrinology and metabolism.

[94]  N. Greig,et al.  Exendin-4 decelerates food intake, weight gain, and fat deposition in Zucker rats. , 2000, Endocrinology.

[95]  S B Heymsfield,et al.  Cadaver validation of skeletal muscle measurement by magnetic resonance imaging and computerized tomography. , 1998, Journal of applied physiology.

[96]  M. Blankenstein,et al.  Visceral adipose tissue is associated with circulating high affinity growth hormone-binding protein. , 1997, The Journal of clinical endocrinology and metabolism.

[97]  C. Bouchard,et al.  The use of anthropometric and dual-energy X-ray absorptiometry (DXA) measures to estimate total abdominal and abdominal visceral fat in men and women. , 1999, Obesity research.

[98]  C. Pond,et al.  Adipose tissue in the mammalian heart and pericardium: structure, foetal development and biochemical properties. , 1989, Comparative biochemistry and physiology. B, Comparative biochemistry.

[99]  F. Barton,et al.  Anatomy of the subcutaneous tissue of the trunk and lower extremity. , 1987, Plastic and reconstructive surgery.

[100]  A. Bigard,et al.  Mobilization of Visceral Adipose Tissue Related to the Improvement in Insulin Sensitivity in Response to Physical Training in NIDDM: Effects of branched-chain amino acid supplements , 1997, Diabetes Care.

[101]  G. Mcneill,et al.  Change in intra-abdominal adipose tissue volume during weight loss in obese men and women: correlation between magnetic resonance imaging and anthropometric measurements , 2000, International Journal of Obesity.

[102]  S. Macura,et al.  Sampling the intramyocellular triglycerides from skeletal muscle. , 2001, Journal of lipid research.

[103]  R. Ross,et al.  Effects of sex on the change in visceral, subcutaneous adipose tissue and skeletal muscle in response to weight loss , 1999, International Journal of Obesity.