Adiposity indicators, cardiometabolic parameters and critical size of adipocytes in premenopausal women
Main Article Content
Keywords
Adipose tissue; Obesity; Anthropometry; Waist circumference; Sagittal abdominal diameter; Waist-to-height ratio
Abstract
Background and aim: Adipocyte hypertrophy is an indicator of adipose tissue dysfunction that precedes the development of obesity comorbidities. The aim of this study was to analyze relationship between adiposity indicators, cardiometabolic parameters and the size of abdominal adipocytes in premenopausal women, and to develop cut-off levels for anthropometric indicators based on the critical size (100 μm) of visceral adipocytes. Methods: Study group consisted of 50 premenopausal women aged 42.88±7.17y. Subcutaneous and visceral (omental) adipose tissue samples were taken during laparotomy, and adipocyte size was analysed. Prior surgery all subjects underwent body composition analysis, anthropometric mesurements, and cardiometabolic risk assessment. Results: The size of subcutaneous and visceral adipocytes correlated significantly with all indicators of overall and regional adiposity, except thigh skinfold thickness, proximal and distal thigh circumferences. Indicators of upper body adiposity had better correlation with the size of visceral adipocytes comparing to subcutaneous adipocytes. Blood pressure and leptin levels had stronger correlation with the size of subcutaneous, while tryglicerides, HDL-cholesterol, uric acid, glycaemia and HOMA showed better correlation with the size of visceral adipocytes. After adjustment for overall and regional adiposity significant correlation only remained between subcutaneous adipocyte size and diastolic blood pressure (r=352, p<0.05) and visceral adipocyte size and glycaemia (r=0.346, p<0.05), while correlation between LDL-cholesterol and size of visceral adipocytes became significant (r=0.294, p<0.05). Among all anthropometric parameters highest predictive ability for critical size of visceral adipocytes showed waist-to-height ratio and body fat percent (AUC: 0.879 and 0.878, respectively). Specific cut-off values were obtained for following anthropometric parameters: waist-to-height ratio (0.51), body fat (39.65%), sagittal abdominal diameter-to-height ratio (0.16), waist-to-tight ratio (1.48), abdominal skinfold thickness (41.60 mm), abdominal diameter index (0.58), waist circumference (86.90 cm), waist-to-hip ratio (0.85), conicity index (1.19), trunk fat (34.00%), sagittal abdominal diameter (26.25 cm) and chest skinfold thickness (28.20 mm). Conclusions: These results imply to a fine interplay between cellular-to-whole body level morphology and functionality.
References
1. Onat A, Avci GS, Barlan MM, Uyarel H, Uzunlar B, Sansoy V. Measures of abdominal obesity assessed for visceral adiposity and relation to coronary risk. Int J Obes Relat Metab Disord 2004;28(8):1018-25.
2. Klein S. The case of visceral fat: argument for the defense. J Clin Invest 2004;113(11):1530-2.
3. Piché MÈ, Weisnagel SJ, Corneau L, Nadeau A, Bergeron J, Lemieux S. Contribution of abdominal visceral obesity and insulin resistance to the cardiovascular risk profile of postmenopausal women. Diabetes 2005;54(3):770-7.
4. Berg AH, Scherer PE. Adipose tissue, inflammation, and cardiovascular disease. Circ Res 2005;13;96(9):939-49.
5. Coppack SW. Adipose tissue changes in obesity. Biochemical Society Transactions 2005;33(Pt 5):1049-52.
6. Goossens GH. The role of adipose tissue dysfunction in the pathogenesis of obesity-related insulin resistance. Physiology&Behaviour 2008;94:206-18.
7. Yang J, Eliasson B, Smith U, Cushman SW, Sherman AS. The size of large adipose cells is a predictor of insulin resistance in first-degree relatives of type 2 diabetic patients. Obesity 2012;20:932-8.
8. Laforest S, Labrecque J, Michaud A, Cianflone K, Tchernof A. Adipocyte size as a determinant of metabolic disease and adipose tissue dysfunction. Crit Rev Clin Lab Sci 2015;52(6):301-13.
9. Arner E, Westermark PO, Spalding KL, et al. Adipocyte turnover: relevance to human adipose tissue morphology. Diabetes 2010;59(1):105-9.
10. Trayhurn P, Wang B, Wood IS. Hypoxia in adipose tissue: a basis for the dysregulation of tissue function in obesity? Br J Nutr 2008;100(2):227-35.
11. Hosogai N, Fukuhara A, Oshima K, et al. Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation. Diabetes 2007;56(4):901-11.
12. Kahn HS, Austin H, Williamson DF, Arensberg D. Simple anthropometric indices associated with ischemic heart disease. J Clin Epidemiol 1996;49(9):1017-24.
13. Stevens J, Katz EG, Huxley RR. Associations between gender, age and waist circumference. Eur J Clin Nutr 2010;64:6-15.
14. Ashwell MA, LeJeune SRE, McPherson K. Ratio of waist circumference to height may be better indicator of need for weight management. British Medical Journal 1996;312(7027):377.
15. Molarius A, Seidell JC. Selection of anthropometric indicators for classification of abdominal fatness-a critical review. Int J Obes Relat Metab Disord 1998;22(8):719-27.
16. Sampaio LR, Simões EJ, Assis AMO, Ramos LR. Validity and reliability of the sagittal abdominal diameter as a predictor of visceral abdominal fat. Arq Bras Endocrinol Metab 2007;51(6):980-6.
17. Meena VP, Seenu V, Sharma MC, et al. Relationship of Adipocyte Size with Adiposity and Metabolic Risk Factors in Asian Indians. PLoS One 2014; 9(9):e108421.
18. Mundi MS, Karpyak MV, Koutsari C, Votruba SB, O'Brien PC, Jensen MD. Body fat distribution, adipocyte size, and metabolic characteristics of nondiabetic adults. J Clin Endocrinol Metab 2010;95(1):67-73.
19. Heyward VH, Stolarczyk LM. Applied body composition assessment. Human Kinetics, 1996.
20. Kvist H, Chowdhury B, Grangard U, Tylen U, Sjöström L. Total and visceral adipose-tissue volumes derived from measurements with computed tomography in adult men and women: predictive equations. Am J Clin Nutr 1988;48:1351-61.
21. Krakauer Nir Y, Jesse C. Krakauer. A new body shape index predicts mortality hazard independently of body mass index". PLoS One 2012;7(7):e39504.
22. Bennasar-Veny M, Lopez-Gonzalez AA, Tauler P, et al. Body adiposity index and cardiovascular health risk factors in Caucasians: a comparison with the body mass index and others. PLoS One 2013;8(5):e63999.
23. Friedewald WT, Levy RI, Frericjkson DS. Estimation on the concentracion of low-density lipoprotein cholesterol in plasma, without use of the preparative centrifuge. Clin Chem 1972;18(6):499-502.
24. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function fasting plasma glucose and insulin concentracions in man. Diabetologia 1985;28:412-19.
25. Lu B, Zhou J, Waring ME, Parker DR, Eaton CB. Abdominal obesity and peripheral vascular disease in men and women: a comparison of waist-to-thigh ratio and waist circumference as measures of abdominal obesity. Atherosclerosis 2010;208(1):253-7.
26. Zamboni M, Turcato E, Armellini F, et al. SAD as a practical predictor of visceral fat. Int J Obes 1998;(22):655-60.
27. Lee MJ, Wu Y, Fried SK. Adipose tissue remodeling in pathophysiology of obesity. Curr Opin Clin Nutr Metab Care 2010;13(4):371-6.
28. McQuaid SE, Hodson L, Neville MJ, et al. Downregulation of adipose tissue fatty acid trafficking in obesity: a driver for ectopic fat deposition? Diabetes 2011;60(1):47-55.
29. Varlamov O, Somwar R, Cornea A, Kievit P, Grove KL, Roberts CT Jr. Single-cell analysis of insulin-regulated fatty acid uptake in adipocytes. Am J Physiol Endocrinol Metab 2010;299(3):E486-E496.
30. Cinti S. Transdifferentiation properties of adipocytes in the adipose organ. American Journal of Physiology - Endocrinology and Metabolism 2009;297(5):E977-86.
31. DiGirolamo M, Fine JB, Tagra K, Rossmanith R. Qualitative regional differences in adipose tissue growth and cellularity in male Wistar rats fed ad libitum. Am J Physiol Regul Integr Comp Physiol 1998;274:R1460-7.
32. Larson-Meyer DE, Heilbronn LK, Redman LM, et al. Effect of calorie restriction with or without exercise on insulin sensitivity, beta-cell function, fat cell size, and ectopic lipid in overweight subjects. Diabetes Care 2006;29(6):1337-44.
33. Petäjä EM, Sevastianova K, Hakkarainen A, Orho-Melander M, Lundbom N, Yki-Järvinen H. Adipocyte size is associated with NAFLD independent of obesity, fat distribution, and PNPLA3 genotype. Obesity 2013;21(6):1174-9.
34. Després JP, Lemieux I, Bergeron J, et al. Abdominal obesity and the metabolic syndrome: contribution to global cardiometabolic risk. Arterioscler Thromb Vasc Biol 2008;28(6):1039-49.
35. Lofgren I, Herron K, Zern T, et al. Waist circumference is a better predictor than body mass index of coronary heart disease risk in overweight premenopausal women. J Nutr 2004;134(5):1071-6.
36. Yim JY, Kim D, Lim SH, et al. SAD is a strong anthropometric measure of visceral adipose tissue in the Asian general population. Diabetes Care 2010;33(12):2665-70.
37. Pouliot MC, Despres JP, Lemieux S, Moorjani S, Bouchard C, Tremblay A. Waist circumference and abdominal sagittal diameter: best simple anthropometric indexes of abdominal visceral adipose tissue accumulation and related cardiovascular risk in men and women. Am J Cardiol 1994;73(7):460-8.
38. Sjöstrom L. The sagittal diameter is valid marker of visceral adipose tissue. Int J Obes 1994;18(2):46-52.
39. Li C, Ford ES, Zhao G, Kahn HS, Mokdad AH. Waist-to-thigh ratio and diabetes among US adults: the Third National Health and Nutrition Examination Survey. Diabetes Res Clin Pract 2010;89(1):79-87.
40. Hou XG, Moser S, Sarr MG, Thompson GB, Que FG, Jensen MD. Visceral and subcutaneous adipose tissue diacylglycerol acyltransferase activity in humans. Obesity (Silver Spring) 2009;17(6):1129-34.
41. Edens NK, Fried SK, Kral JG, Hirsch J, Leibel RL. In vitro lipid synthesis in human adipose tissue from three abdominal sites. Am J Physiol Endocrinol Metab 1993;265(3 Pt 1):E374-E379.
42. Farnier C, Krief S, Blache M, et al. Adipocyte functions are modulated by cell size change: potential involvement of an integrin/ERK signalling pathway. Int J Obes Relat Metab Disord 2003;27(10):1178-86.
43. Votruba SB, Jensen MD. Sex differences in abdominal, gluteal, and thigh LPL activity. Am J Physiol Endocrinol Metab 2007;292(6):E1823-E1828.
44. Hoffstedt J, Arner E, Wahrenberg H, et al. Regional impact of adipose tissue morphology on the metabolic profile in morbid obesity. Diabetologia 2010;53(12):2496-503.
45. Veilleux A, Caron-Jobin M, Noël S, Laberge PY, Tchernof A. Visceral adipocyte hypertrophy is associated with dyslipidemia independent of body composition and fat distribution in women. Diabetes 2011;60(5):1504-11.
46. O'Connell J, Lynch L, Cawood TJ, et al. The relationship of omental and subcutaneous adipocyte size to metabolic disease in severe obesity. PLoS One 2010;5(4):e9997.
47. Ledoux S, Coupaye M, Essig M, et al. Traditional anthropometric parameters still predict metabolic disorders in women with severe obesity. Obesity 2010;18(5):1026-32.
48. Kabir M, Stefanovski D, Hsu IR, et al. Large size cells in the visceral adipose depot predict insulin resistance in the canine model. Obesity (Silver Spring) 2011;19(11):2121-9.
49. Srdić B, Stokić E, Korać A, Ukropina M, Veličković K, Breberina M. Morphological characteristics of abdominal adipose tissue in normal-weight and obese women of different metabolic profiles. Exp Clin Endocrinol Diabetes 2010;118:713-8.
50. Zhang Y, Zitsman JL, Hou J, et al. Fat cell size and adipokine expression in relation to gender, depot and metabolic risk factors in morbidly obese adolescents. Obesity (Silver Spring) 2014;22(3):691-7.
51. Meyer LK, Ciaraldi TP, Henry RR, Wittgrove AC, Phillips SA. Adipose tissue depot and cell size dependency of adiponectin synthesis and secretion in human obesity. Adipocyte 2013;2(4):217-26.
52. Tchoukalova YD, Votruba SB, Tchkonia T, Giorgadze N, Kirkland JL, Jensen MD. Regional differences in cellular mechanisms of adipose tissue gain with overfeeding. Proceedings of the National Academy of Sciences of the United States of America 2010;107(42):18226-31.
53. Kissebah AH, Alfarsi S, Adams PW. Integrated regulation of very low density lipoprotein triglyceride and apolipoprotein-B kinetics in man: normolipemic subjects, familial hypertriglyceridemia and familial combined hyperlipidemia. Metabolism - Clinical and Experimental 1981;30:856-68.
54. Jensen MD. Role of body fat distribution and the metabolic complications of obesity. The Journal of Clinical Endocrinology & Metabolism 2008;93(11 Suppl 1):S57-63.
55. Karpe F, Pinnick KE. Biology of upper-body and lower-body adipose tissue – link to whole-body phenotypes. Nature Reviews Endocrinology 2015;11(2):90-100.
56. Ashwell M. Waist to height ratio and the Ashwell® shape chart could predict the health risks of obesity in adults and children in all ethnic groups. Nutritio & Food Science 2005;35(5):359-64.
57. Lean ME, Han TS, Morrison CE. Waist circumference as a measure for indicating need for weight management. BMJ 1995;311(6998):158-61.
58. Hsieh SD, Yoshinaga H. Abdominal fat distribution and coronary heart disease risk factors in men – waist/height ratio as a simple and useful predictor. Int J Obes Relat Metab Disord 1995;19:585-9.
59. Lemieux S, Prud’homme D, Bouchard C, Tremblay A, Després JP. A single threshold value of waist girth identifies normal-weight and overweight subjects with excess visceral adipose tissue. The American journal of clinical nutrition 1996;64(5):685-93.
60. Dobbelsteyn CJ, Joffres MR, MacLean DR, Flowerdew G. A comparative evaluation of waist circumference, waist-to-hip ratio and body mass index as indicators of cardiovascular risk factors. The Canadian Heart Health Surveys. Int J Obes 2001;25:652-61.
61. Bays H, Abate N, Chandalia M. Adiposopathy: sick fat causes high blood sugar, high blood pressure and dyslipidemia. Future Cardiology 2005;1(1):39-59.
62. Lin WY, Lee LT, Chen CY, et al. Optimal cut-off values for obesity: using simple anthropometric indices to predict cardiovascular risk factors in Taiwan. Int J Obes 2002;26:1232-8.
63. Rodrigues SL, Baldo MP, Mill JG. Association of waist-stature ratio with hypertension and metabolic syndrome: population-based study. Arq Bras Cardiol 2010;95(2):186-91.
64. Carneiro Roriz AK, Santana Passos LC, Cuncha de Oliviera C, Eickemberg M, De Almeida Moreira P, Ramos Sampaio L. Discriminatory power of indicators predictors of visceral adiposity evaluated by computer tomography in adults and elderly individuals. Nutr Hosp 2014;29(n06):1401-7.
65. Bertsias G, Mammas I, Linardakis M, Kafatos A. Overweight and obesity in relation to cardiovascular disease risk factors among medical students in Crete, Greece. BMC Pub Health 2003;3(1):3.
66. Browning LM, Hsieh SD, Ashwell M. A systematic review of waist-to-height ratio as a screening tool for the prediction of cardiovascular disease and diabetes: 0.5 could be a suitable global boundary value. Nutr Res Rev 2010;23:247-69.
67. Li L, Wang C, Bao Y, Peng L, Gu H, Jia W. Optimal body fat percentage cut‐offs for obesity in Chinese adults. Clinical and Experimental Pharmacology and Physiology 2012;39(4):393-8.
68. Joseph L, Wasir JS, Misra A, et al. Appropriate values of adiposity and lean body mass indices to detect cardiovascular risk factors in Asian Indians. Diabetes Technol Ther 2011;13(9):899-906.
69. Kim CH, Park HS, Park M, Kim H, Kim C. Optimal cutoffs of percentage body fat for predicting obesity‐related cardiovascular disease risk factors in Korean adults. Am J Clin Nutr 2011;94:34-9.
70. Stokić E, Brtka V, Srdić B. The synthesis of the rough set model for the better applicability of sagittal abdominal diameter in identifying high risk patients. Computers in Biology and Medicine 2010;40:786-90.
71. Lahmann PH, Lissner L, Gullberg B, Olsson H, Berglund G. A prospective study of adiposity and all-cause mortality: the Malmo Diet and Cancer Study. Obes Res 2002;10:361-9. doi:10.1038/oby.2002.50.
72. Macias N, Quezada AD, Flores M, et al. Accuracy of body fat percent and adiposity indicators cut off values to detect metabolic risk factors in a sample of Mexican adults. BMC Public Health 2014;14:341.
73. Motamed N, Perumal D, Zamani F, et al. Conicity Index and Waist-to-Hip Ratio Are Superior Obesity Indices in Predicting 10-Year Cardiovascular Risk Among Men and Women. Clin Cardiol 2015;38(9):527-34.
74. Andrade MD, Freitas MC, Sakumoto AM, et al. Association of the conicity index with diabetes and hypertension in Brazilian women. Arch Endocrinol Metab 2016;60(5):436-442.
75. Pitanga FJG, Lessa I. Sensibilidade e especificidade do indice de conicidade como discriminador do risko coronario de adoltos em Salvador, Brasil. Rev Bras Epidemiol 2004;7:256-69.
76. Cho S, Shin A, Choi JY, et al. Optimal cutoff values for anthropometric indices of obesity as discriminators of metabolic abnormalities in Korea: results from a Health Examinees study. BMC Public Health 2021;21:459.
77. Smith SR, Lovejoy JC, Greenway F, et al. Contributions of total body fat, abdominal subcutaneous adipose tissue compartments, and visceral adipose tissue to the metabolic complications of obesity. Metabolism 2001;50(4):425-35.
2. Klein S. The case of visceral fat: argument for the defense. J Clin Invest 2004;113(11):1530-2.
3. Piché MÈ, Weisnagel SJ, Corneau L, Nadeau A, Bergeron J, Lemieux S. Contribution of abdominal visceral obesity and insulin resistance to the cardiovascular risk profile of postmenopausal women. Diabetes 2005;54(3):770-7.
4. Berg AH, Scherer PE. Adipose tissue, inflammation, and cardiovascular disease. Circ Res 2005;13;96(9):939-49.
5. Coppack SW. Adipose tissue changes in obesity. Biochemical Society Transactions 2005;33(Pt 5):1049-52.
6. Goossens GH. The role of adipose tissue dysfunction in the pathogenesis of obesity-related insulin resistance. Physiology&Behaviour 2008;94:206-18.
7. Yang J, Eliasson B, Smith U, Cushman SW, Sherman AS. The size of large adipose cells is a predictor of insulin resistance in first-degree relatives of type 2 diabetic patients. Obesity 2012;20:932-8.
8. Laforest S, Labrecque J, Michaud A, Cianflone K, Tchernof A. Adipocyte size as a determinant of metabolic disease and adipose tissue dysfunction. Crit Rev Clin Lab Sci 2015;52(6):301-13.
9. Arner E, Westermark PO, Spalding KL, et al. Adipocyte turnover: relevance to human adipose tissue morphology. Diabetes 2010;59(1):105-9.
10. Trayhurn P, Wang B, Wood IS. Hypoxia in adipose tissue: a basis for the dysregulation of tissue function in obesity? Br J Nutr 2008;100(2):227-35.
11. Hosogai N, Fukuhara A, Oshima K, et al. Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation. Diabetes 2007;56(4):901-11.
12. Kahn HS, Austin H, Williamson DF, Arensberg D. Simple anthropometric indices associated with ischemic heart disease. J Clin Epidemiol 1996;49(9):1017-24.
13. Stevens J, Katz EG, Huxley RR. Associations between gender, age and waist circumference. Eur J Clin Nutr 2010;64:6-15.
14. Ashwell MA, LeJeune SRE, McPherson K. Ratio of waist circumference to height may be better indicator of need for weight management. British Medical Journal 1996;312(7027):377.
15. Molarius A, Seidell JC. Selection of anthropometric indicators for classification of abdominal fatness-a critical review. Int J Obes Relat Metab Disord 1998;22(8):719-27.
16. Sampaio LR, Simões EJ, Assis AMO, Ramos LR. Validity and reliability of the sagittal abdominal diameter as a predictor of visceral abdominal fat. Arq Bras Endocrinol Metab 2007;51(6):980-6.
17. Meena VP, Seenu V, Sharma MC, et al. Relationship of Adipocyte Size with Adiposity and Metabolic Risk Factors in Asian Indians. PLoS One 2014; 9(9):e108421.
18. Mundi MS, Karpyak MV, Koutsari C, Votruba SB, O'Brien PC, Jensen MD. Body fat distribution, adipocyte size, and metabolic characteristics of nondiabetic adults. J Clin Endocrinol Metab 2010;95(1):67-73.
19. Heyward VH, Stolarczyk LM. Applied body composition assessment. Human Kinetics, 1996.
20. Kvist H, Chowdhury B, Grangard U, Tylen U, Sjöström L. Total and visceral adipose-tissue volumes derived from measurements with computed tomography in adult men and women: predictive equations. Am J Clin Nutr 1988;48:1351-61.
21. Krakauer Nir Y, Jesse C. Krakauer. A new body shape index predicts mortality hazard independently of body mass index". PLoS One 2012;7(7):e39504.
22. Bennasar-Veny M, Lopez-Gonzalez AA, Tauler P, et al. Body adiposity index and cardiovascular health risk factors in Caucasians: a comparison with the body mass index and others. PLoS One 2013;8(5):e63999.
23. Friedewald WT, Levy RI, Frericjkson DS. Estimation on the concentracion of low-density lipoprotein cholesterol in plasma, without use of the preparative centrifuge. Clin Chem 1972;18(6):499-502.
24. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function fasting plasma glucose and insulin concentracions in man. Diabetologia 1985;28:412-19.
25. Lu B, Zhou J, Waring ME, Parker DR, Eaton CB. Abdominal obesity and peripheral vascular disease in men and women: a comparison of waist-to-thigh ratio and waist circumference as measures of abdominal obesity. Atherosclerosis 2010;208(1):253-7.
26. Zamboni M, Turcato E, Armellini F, et al. SAD as a practical predictor of visceral fat. Int J Obes 1998;(22):655-60.
27. Lee MJ, Wu Y, Fried SK. Adipose tissue remodeling in pathophysiology of obesity. Curr Opin Clin Nutr Metab Care 2010;13(4):371-6.
28. McQuaid SE, Hodson L, Neville MJ, et al. Downregulation of adipose tissue fatty acid trafficking in obesity: a driver for ectopic fat deposition? Diabetes 2011;60(1):47-55.
29. Varlamov O, Somwar R, Cornea A, Kievit P, Grove KL, Roberts CT Jr. Single-cell analysis of insulin-regulated fatty acid uptake in adipocytes. Am J Physiol Endocrinol Metab 2010;299(3):E486-E496.
30. Cinti S. Transdifferentiation properties of adipocytes in the adipose organ. American Journal of Physiology - Endocrinology and Metabolism 2009;297(5):E977-86.
31. DiGirolamo M, Fine JB, Tagra K, Rossmanith R. Qualitative regional differences in adipose tissue growth and cellularity in male Wistar rats fed ad libitum. Am J Physiol Regul Integr Comp Physiol 1998;274:R1460-7.
32. Larson-Meyer DE, Heilbronn LK, Redman LM, et al. Effect of calorie restriction with or without exercise on insulin sensitivity, beta-cell function, fat cell size, and ectopic lipid in overweight subjects. Diabetes Care 2006;29(6):1337-44.
33. Petäjä EM, Sevastianova K, Hakkarainen A, Orho-Melander M, Lundbom N, Yki-Järvinen H. Adipocyte size is associated with NAFLD independent of obesity, fat distribution, and PNPLA3 genotype. Obesity 2013;21(6):1174-9.
34. Després JP, Lemieux I, Bergeron J, et al. Abdominal obesity and the metabolic syndrome: contribution to global cardiometabolic risk. Arterioscler Thromb Vasc Biol 2008;28(6):1039-49.
35. Lofgren I, Herron K, Zern T, et al. Waist circumference is a better predictor than body mass index of coronary heart disease risk in overweight premenopausal women. J Nutr 2004;134(5):1071-6.
36. Yim JY, Kim D, Lim SH, et al. SAD is a strong anthropometric measure of visceral adipose tissue in the Asian general population. Diabetes Care 2010;33(12):2665-70.
37. Pouliot MC, Despres JP, Lemieux S, Moorjani S, Bouchard C, Tremblay A. Waist circumference and abdominal sagittal diameter: best simple anthropometric indexes of abdominal visceral adipose tissue accumulation and related cardiovascular risk in men and women. Am J Cardiol 1994;73(7):460-8.
38. Sjöstrom L. The sagittal diameter is valid marker of visceral adipose tissue. Int J Obes 1994;18(2):46-52.
39. Li C, Ford ES, Zhao G, Kahn HS, Mokdad AH. Waist-to-thigh ratio and diabetes among US adults: the Third National Health and Nutrition Examination Survey. Diabetes Res Clin Pract 2010;89(1):79-87.
40. Hou XG, Moser S, Sarr MG, Thompson GB, Que FG, Jensen MD. Visceral and subcutaneous adipose tissue diacylglycerol acyltransferase activity in humans. Obesity (Silver Spring) 2009;17(6):1129-34.
41. Edens NK, Fried SK, Kral JG, Hirsch J, Leibel RL. In vitro lipid synthesis in human adipose tissue from three abdominal sites. Am J Physiol Endocrinol Metab 1993;265(3 Pt 1):E374-E379.
42. Farnier C, Krief S, Blache M, et al. Adipocyte functions are modulated by cell size change: potential involvement of an integrin/ERK signalling pathway. Int J Obes Relat Metab Disord 2003;27(10):1178-86.
43. Votruba SB, Jensen MD. Sex differences in abdominal, gluteal, and thigh LPL activity. Am J Physiol Endocrinol Metab 2007;292(6):E1823-E1828.
44. Hoffstedt J, Arner E, Wahrenberg H, et al. Regional impact of adipose tissue morphology on the metabolic profile in morbid obesity. Diabetologia 2010;53(12):2496-503.
45. Veilleux A, Caron-Jobin M, Noël S, Laberge PY, Tchernof A. Visceral adipocyte hypertrophy is associated with dyslipidemia independent of body composition and fat distribution in women. Diabetes 2011;60(5):1504-11.
46. O'Connell J, Lynch L, Cawood TJ, et al. The relationship of omental and subcutaneous adipocyte size to metabolic disease in severe obesity. PLoS One 2010;5(4):e9997.
47. Ledoux S, Coupaye M, Essig M, et al. Traditional anthropometric parameters still predict metabolic disorders in women with severe obesity. Obesity 2010;18(5):1026-32.
48. Kabir M, Stefanovski D, Hsu IR, et al. Large size cells in the visceral adipose depot predict insulin resistance in the canine model. Obesity (Silver Spring) 2011;19(11):2121-9.
49. Srdić B, Stokić E, Korać A, Ukropina M, Veličković K, Breberina M. Morphological characteristics of abdominal adipose tissue in normal-weight and obese women of different metabolic profiles. Exp Clin Endocrinol Diabetes 2010;118:713-8.
50. Zhang Y, Zitsman JL, Hou J, et al. Fat cell size and adipokine expression in relation to gender, depot and metabolic risk factors in morbidly obese adolescents. Obesity (Silver Spring) 2014;22(3):691-7.
51. Meyer LK, Ciaraldi TP, Henry RR, Wittgrove AC, Phillips SA. Adipose tissue depot and cell size dependency of adiponectin synthesis and secretion in human obesity. Adipocyte 2013;2(4):217-26.
52. Tchoukalova YD, Votruba SB, Tchkonia T, Giorgadze N, Kirkland JL, Jensen MD. Regional differences in cellular mechanisms of adipose tissue gain with overfeeding. Proceedings of the National Academy of Sciences of the United States of America 2010;107(42):18226-31.
53. Kissebah AH, Alfarsi S, Adams PW. Integrated regulation of very low density lipoprotein triglyceride and apolipoprotein-B kinetics in man: normolipemic subjects, familial hypertriglyceridemia and familial combined hyperlipidemia. Metabolism - Clinical and Experimental 1981;30:856-68.
54. Jensen MD. Role of body fat distribution and the metabolic complications of obesity. The Journal of Clinical Endocrinology & Metabolism 2008;93(11 Suppl 1):S57-63.
55. Karpe F, Pinnick KE. Biology of upper-body and lower-body adipose tissue – link to whole-body phenotypes. Nature Reviews Endocrinology 2015;11(2):90-100.
56. Ashwell M. Waist to height ratio and the Ashwell® shape chart could predict the health risks of obesity in adults and children in all ethnic groups. Nutritio & Food Science 2005;35(5):359-64.
57. Lean ME, Han TS, Morrison CE. Waist circumference as a measure for indicating need for weight management. BMJ 1995;311(6998):158-61.
58. Hsieh SD, Yoshinaga H. Abdominal fat distribution and coronary heart disease risk factors in men – waist/height ratio as a simple and useful predictor. Int J Obes Relat Metab Disord 1995;19:585-9.
59. Lemieux S, Prud’homme D, Bouchard C, Tremblay A, Després JP. A single threshold value of waist girth identifies normal-weight and overweight subjects with excess visceral adipose tissue. The American journal of clinical nutrition 1996;64(5):685-93.
60. Dobbelsteyn CJ, Joffres MR, MacLean DR, Flowerdew G. A comparative evaluation of waist circumference, waist-to-hip ratio and body mass index as indicators of cardiovascular risk factors. The Canadian Heart Health Surveys. Int J Obes 2001;25:652-61.
61. Bays H, Abate N, Chandalia M. Adiposopathy: sick fat causes high blood sugar, high blood pressure and dyslipidemia. Future Cardiology 2005;1(1):39-59.
62. Lin WY, Lee LT, Chen CY, et al. Optimal cut-off values for obesity: using simple anthropometric indices to predict cardiovascular risk factors in Taiwan. Int J Obes 2002;26:1232-8.
63. Rodrigues SL, Baldo MP, Mill JG. Association of waist-stature ratio with hypertension and metabolic syndrome: population-based study. Arq Bras Cardiol 2010;95(2):186-91.
64. Carneiro Roriz AK, Santana Passos LC, Cuncha de Oliviera C, Eickemberg M, De Almeida Moreira P, Ramos Sampaio L. Discriminatory power of indicators predictors of visceral adiposity evaluated by computer tomography in adults and elderly individuals. Nutr Hosp 2014;29(n06):1401-7.
65. Bertsias G, Mammas I, Linardakis M, Kafatos A. Overweight and obesity in relation to cardiovascular disease risk factors among medical students in Crete, Greece. BMC Pub Health 2003;3(1):3.
66. Browning LM, Hsieh SD, Ashwell M. A systematic review of waist-to-height ratio as a screening tool for the prediction of cardiovascular disease and diabetes: 0.5 could be a suitable global boundary value. Nutr Res Rev 2010;23:247-69.
67. Li L, Wang C, Bao Y, Peng L, Gu H, Jia W. Optimal body fat percentage cut‐offs for obesity in Chinese adults. Clinical and Experimental Pharmacology and Physiology 2012;39(4):393-8.
68. Joseph L, Wasir JS, Misra A, et al. Appropriate values of adiposity and lean body mass indices to detect cardiovascular risk factors in Asian Indians. Diabetes Technol Ther 2011;13(9):899-906.
69. Kim CH, Park HS, Park M, Kim H, Kim C. Optimal cutoffs of percentage body fat for predicting obesity‐related cardiovascular disease risk factors in Korean adults. Am J Clin Nutr 2011;94:34-9.
70. Stokić E, Brtka V, Srdić B. The synthesis of the rough set model for the better applicability of sagittal abdominal diameter in identifying high risk patients. Computers in Biology and Medicine 2010;40:786-90.
71. Lahmann PH, Lissner L, Gullberg B, Olsson H, Berglund G. A prospective study of adiposity and all-cause mortality: the Malmo Diet and Cancer Study. Obes Res 2002;10:361-9. doi:10.1038/oby.2002.50.
72. Macias N, Quezada AD, Flores M, et al. Accuracy of body fat percent and adiposity indicators cut off values to detect metabolic risk factors in a sample of Mexican adults. BMC Public Health 2014;14:341.
73. Motamed N, Perumal D, Zamani F, et al. Conicity Index and Waist-to-Hip Ratio Are Superior Obesity Indices in Predicting 10-Year Cardiovascular Risk Among Men and Women. Clin Cardiol 2015;38(9):527-34.
74. Andrade MD, Freitas MC, Sakumoto AM, et al. Association of the conicity index with diabetes and hypertension in Brazilian women. Arch Endocrinol Metab 2016;60(5):436-442.
75. Pitanga FJG, Lessa I. Sensibilidade e especificidade do indice de conicidade como discriminador do risko coronario de adoltos em Salvador, Brasil. Rev Bras Epidemiol 2004;7:256-69.
76. Cho S, Shin A, Choi JY, et al. Optimal cutoff values for anthropometric indices of obesity as discriminators of metabolic abnormalities in Korea: results from a Health Examinees study. BMC Public Health 2021;21:459.
77. Smith SR, Lovejoy JC, Greenway F, et al. Contributions of total body fat, abdominal subcutaneous adipose tissue compartments, and visceral adipose tissue to the metabolic complications of obesity. Metabolism 2001;50(4):425-35.
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Srdic Galic B, Stokic E, Korac A, Udicki M, Mandic A. Adiposity indicators, cardiometabolic parameters and critical size of adipocytes in premenopausal women. Progr Nutr [Internet]. 2022 Sep. 27 [cited 2024 Jul. 18];24(3):e2022087. Available from: https://mattioli1885journals.com/index.php/progressinnutrition/article/view/13497
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How to Cite
1.
Srdic Galic B, Stokic E, Korac A, Udicki M, Mandic A. Adiposity indicators, cardiometabolic parameters and critical size of adipocytes in premenopausal women. Progr Nutr [Internet]. 2022 Sep. 27 [cited 2024 Jul. 18];24(3):e2022087. Available from: https://mattioli1885journals.com/index.php/progressinnutrition/article/view/13497
