Skip to main content
Top
Published in: Cardiovascular Diabetology 1/2015

Open Access 01-12-2015 | Original investigation

High visceral fat with low subcutaneous fat accumulation as a determinant of atherosclerosis in patients with type 2 diabetes

Authors: Ryotaro Bouchi, Takato Takeuchi, Momoko Akihisa, Norihiko Ohara, Yujiro Nakano, Rie Nishitani, Masanori Murakami, Tatsuya Fukuda, Masamichi Fujita, Isao Minami, Hajime Izumiyama, Koshi Hashimoto, Takanobu Yoshimoto, Yoshihiro Ogawa

Published in: Cardiovascular Diabetology | Issue 1/2015

Login to get access

Abstract

Background

Abdominal visceral obesity has been reported to be associated with cardiovascular risks than body mass index, waist circumference, and abdominal subcutaneous fat. On the other hand, there is evidence that subcutaneous fat has a beneficial role against cardio-metabolic risks such as diabetes or dyslipidemia. However, little is known regarding the association between high visceral fat with low subcutaneous fat accumulation and the risk for atherosclerosis.

Methods

This study was designed to elucidate whether high visceral fat with low subcutaneous fat accumulation enhances the risk for atherosclerosis in patients with type 2 diabetes. This is a cross-sectional study of 148 patients with type 2 diabetes (mean age 65 ± 12 years; 44.5 % female). Visceral fat area (VFA, cm2) and subcutaneous fat area (SFA, cm2) were assessed by abdominal computed tomography. Carotid intima media thickness (CIMT, mm) measured by ultrasonography was used for the assessment of atherosclerosis. Patients were divided into four groups: SFA < 100 cm2 and VFA < 100 cm2 [S(−)V(−)], SFA ≥ 100 cm2 and VFA < 100 cm2 [S(+)V(−)], SFA < 100 cm2 and VFA ≥ 100 cm2 [S(−)V(+)], and SFA ≥ 100 cm2 and VFA ≥ 100 cm2 [S(+)V(+)]. Linear regression analysis with a stepwise procedure was used for the statistical analyses.

Results

Among the patients examined, 16.3 % were S(−)V(+). Mean (95 % confidence interval) of CIMT adjusting for age and gender were 0.80 (0.69–0.91), 0.86 (0.72–1.01), 1.28 (1.11–1.44) and 0.83 (0.77–0.88) in patients with S(−)V(−), S(+)V(−), S(−)V(+) and S(+)V(+), respectively (p < 0.001). The S(−)V(+) patients exhibited significantly older than S(−)V(−) patients and those with S(+)V(+) and had a highest VFA-SFA ratio (V/S ratio) among the four groups. S(−)V(+) patients were male predominant (100 % male), and S(+)V(−) patients showed female predominance (82 % female). In multivariate linear regression analysis (Adjusted R2 = 0.549), S(−)V(+) was significantly associated with CIMT (Standardized β 0.423, p < 0.001). Notably, S(+)V(+) was inversely associated with CIMT in the multivariate model.

Conclusions

This study provides evidence that high visceral fat with low subcutaneous fat accumulation is an important determinant of carotid atherosclerosis and high subcutaneous fat could be protective against atherosclerosis in patients with type 2 diabetes.
Literature
1.
go back to reference Yusuf S, Hawken S, Ounpuu S, Bautista L, Franzosi MG, Commerford P, Lang CC, Rumboldt Z, Onen CL, Lisheng L, INTERHEART Study Investigators, et al. Obesity and the risk of myocardial infarction in 27,000 participants from 52 countries: a case-control study. Lancet. 2005;366:1640–9.CrossRefPubMed Yusuf S, Hawken S, Ounpuu S, Bautista L, Franzosi MG, Commerford P, Lang CC, Rumboldt Z, Onen CL, Lisheng L, INTERHEART Study Investigators, et al. Obesity and the risk of myocardial infarction in 27,000 participants from 52 countries: a case-control study. Lancet. 2005;366:1640–9.CrossRefPubMed
2.
go back to reference Fujimoto WY, Bergstrom RW, Boyko EJ, Chen KW, Leonetti DL, Newell-Morris L, Shofer JB, Wahl PW. Visceral adiposity and incident coronary heart disease in Japanese-American men. The 10-year follow-up results of the Seattle Japanese-American Community Diabetes Study. Diabetes Care. 1999;22:1808–12.CrossRefPubMed Fujimoto WY, Bergstrom RW, Boyko EJ, Chen KW, Leonetti DL, Newell-Morris L, Shofer JB, Wahl PW. Visceral adiposity and incident coronary heart disease in Japanese-American men. The 10-year follow-up results of the Seattle Japanese-American Community Diabetes Study. Diabetes Care. 1999;22:1808–12.CrossRefPubMed
3.
go back to reference Britton KA, Massaro JM, Murabito JM, Kreger BE, Hoffmann U, Fox CS. Body fat distribution, incident cardiovascular disease, cancer, and all-cause mortality. J Am Coll Cardiol. 2013;62:921–5.PubMedCentralCrossRefPubMed Britton KA, Massaro JM, Murabito JM, Kreger BE, Hoffmann U, Fox CS. Body fat distribution, incident cardiovascular disease, cancer, and all-cause mortality. J Am Coll Cardiol. 2013;62:921–5.PubMedCentralCrossRefPubMed
4.
go back to reference Kanai H, Matsuzawa Y, Kotani K, Keno Y, Kobatake T, Nagai Y, Fujioka S, Tokunaga K, Tarui S. Close correlation of intra-abdominal fat accumulation to hypertension in obese women. Hypertension. 1990;16:484–90.CrossRefPubMed Kanai H, Matsuzawa Y, Kotani K, Keno Y, Kobatake T, Nagai Y, Fujioka S, Tokunaga K, Tarui S. Close correlation of intra-abdominal fat accumulation to hypertension in obese women. Hypertension. 1990;16:484–90.CrossRefPubMed
5.
go back to reference Després JP, Lemieux S, Lamarche B, Prud’homme D, Moorjani S, Brun LD, Gagné C, Lupien PJ. The insulin resistance-dyslipidemic syndrome: contribution of visceral obesity and therapeutic implications. Int J Obes Relat Metab Disord. 1995;19(Suppl 1):S76–86.PubMed Després JP, Lemieux S, Lamarche B, Prud’homme D, Moorjani S, Brun LD, Gagné C, Lupien PJ. The insulin resistance-dyslipidemic syndrome: contribution of visceral obesity and therapeutic implications. Int J Obes Relat Metab Disord. 1995;19(Suppl 1):S76–86.PubMed
6.
go back to reference Fox CS, Massaro JM, Hoffmann U, Pou KM, Maurovich-Horvat P, Liu CY, Vasan RS, Murabito JM, Meigs JB, Cupples LA, et al. Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham Heart Study. Circulation. 2007;116:39–48.CrossRefPubMed Fox CS, Massaro JM, Hoffmann U, Pou KM, Maurovich-Horvat P, Liu CY, Vasan RS, Murabito JM, Meigs JB, Cupples LA, et al. Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham Heart Study. Circulation. 2007;116:39–48.CrossRefPubMed
7.
go back to reference Bouchi R, Minami I, Ohara N, Nakano Y, Nishitani R, Murakami M, Takeuchi T, Akihisa M, Fukuda T, Fujita M, et al. Impact of increased visceral adiposity with normal weight on the progression of arterial stiffness in Japanese patients with type 2 diabetes. BMJ Open Diabetes Res Care. 2015;3:e000081.PubMedCentralCrossRefPubMed Bouchi R, Minami I, Ohara N, Nakano Y, Nishitani R, Murakami M, Takeuchi T, Akihisa M, Fukuda T, Fujita M, et al. Impact of increased visceral adiposity with normal weight on the progression of arterial stiffness in Japanese patients with type 2 diabetes. BMJ Open Diabetes Res Care. 2015;3:e000081.PubMedCentralCrossRefPubMed
8.
go back to reference Snijder MB, Visser M, Dekker JM, Goodpaster BH, Harris TB, Kritchevsky SB, De Rekeneire N, Kanaya AM, Newman AB, Tylavsky FA, et al. Low subcutaneous thigh fat is a risk factor for unfavourable glucose and lipid levels, independently of high abdominal fat. The Health ABC Study. Diabetologia. 2005;48:301–8.CrossRefPubMed Snijder MB, Visser M, Dekker JM, Goodpaster BH, Harris TB, Kritchevsky SB, De Rekeneire N, Kanaya AM, Newman AB, Tylavsky FA, et al. Low subcutaneous thigh fat is a risk factor for unfavourable glucose and lipid levels, independently of high abdominal fat. The Health ABC Study. Diabetologia. 2005;48:301–8.CrossRefPubMed
9.
go back to reference Porter SA, Massaro JM, Hoffmann U, Vasan RS, O’Donnel CJ, Fox CS. Abdominal subcutaneous adipose tissue: a protective fat depot? Diabetes Care. 2009;32:1068–75.PubMedCentralCrossRefPubMed Porter SA, Massaro JM, Hoffmann U, Vasan RS, O’Donnel CJ, Fox CS. Abdominal subcutaneous adipose tissue: a protective fat depot? Diabetes Care. 2009;32:1068–75.PubMedCentralCrossRefPubMed
10.
go back to reference Committee of the Japan Diabetes Society on the Diagnostic Criteria of Diabetes Mellitus. Report of the committee on the classification and diagnostic criteria of diabetes mellitus. J Diabetes Investig. 2010;1:212–28.CrossRef Committee of the Japan Diabetes Society on the Diagnostic Criteria of Diabetes Mellitus. Report of the committee on the classification and diagnostic criteria of diabetes mellitus. J Diabetes Investig. 2010;1:212–28.CrossRef
11.
go back to reference Ito H, Komatsu Y, Mifune M, Antoku S, Ishida H, Takeuchi Y, Togane M. The estimated GFR, but not the stage of diabetic nephropathy graded by the urinary albumin excretion, is associated with the carotid intima-media thickness in patients with type 2 diabetes mellitus: a cross-sectional study. Cardiovasc Diabetol. 2010;9:18.PubMedCentralCrossRefPubMed Ito H, Komatsu Y, Mifune M, Antoku S, Ishida H, Takeuchi Y, Togane M. The estimated GFR, but not the stage of diabetic nephropathy graded by the urinary albumin excretion, is associated with the carotid intima-media thickness in patients with type 2 diabetes mellitus: a cross-sectional study. Cardiovasc Diabetol. 2010;9:18.PubMedCentralCrossRefPubMed
12.
go back to reference Examination Committee of Criteria for ‘Obesity Disease’ in Japan. Japan Society for the Study of Obesity. Circ J. 2002;66:987–92.CrossRef Examination Committee of Criteria for ‘Obesity Disease’ in Japan. Japan Society for the Study of Obesity. Circ J. 2002;66:987–92.CrossRef
13.
go back to reference Osawa K, Miyoshi T, Koyama Y, Sato S, Akagi N, Morimitsu Y, Kubo M, Sugiyama H, Nakamura K, Morita H, et al. Differential association of visceral adipose tissue with coronary plaque characteristics in patients with and without diabetes mellitus. Cardiovasc Diabetol. 2014;13:61.PubMedCentralCrossRefPubMed Osawa K, Miyoshi T, Koyama Y, Sato S, Akagi N, Morimitsu Y, Kubo M, Sugiyama H, Nakamura K, Morita H, et al. Differential association of visceral adipose tissue with coronary plaque characteristics in patients with and without diabetes mellitus. Cardiovasc Diabetol. 2014;13:61.PubMedCentralCrossRefPubMed
14.
go back to reference Ren C, Zhang J, Xu Y, Xu B, Sun W, Sun J, Wang T, Xu M, Lu J, Wang W, et al. Association between carotid intima-media thickness and index of central fat distribution in middle-aged and elderly Chinese. Cardiovasc Diabetol. 2014;13:139.PubMedCentralCrossRefPubMed Ren C, Zhang J, Xu Y, Xu B, Sun W, Sun J, Wang T, Xu M, Lu J, Wang W, et al. Association between carotid intima-media thickness and index of central fat distribution in middle-aged and elderly Chinese. Cardiovasc Diabetol. 2014;13:139.PubMedCentralCrossRefPubMed
15.
go back to reference Ravussin E, Smith SR. Increased fat intake, impaired fat oxidation, and failure of fat cell proliferation result in ectopic fat storage, insulin resistance, and type 2 diabetes mellitus. Ann N Y Acad Sci. 2002;967:363–78.CrossRefPubMed Ravussin E, Smith SR. Increased fat intake, impaired fat oxidation, and failure of fat cell proliferation result in ectopic fat storage, insulin resistance, and type 2 diabetes mellitus. Ann N Y Acad Sci. 2002;967:363–78.CrossRefPubMed
16.
go back to reference Yang X, Smith U. Adipose tissue distribution and risk of metabolic disease: does thiazolidinedione-induced adipose tissue redistribution provide a clue to the answer? Diabetologia. 2007;50:1127–39.CrossRefPubMed Yang X, Smith U. Adipose tissue distribution and risk of metabolic disease: does thiazolidinedione-induced adipose tissue redistribution provide a clue to the answer? Diabetologia. 2007;50:1127–39.CrossRefPubMed
17.
go back to reference Jung CH, Kim BY, Kim KJ, Jung SH, Kim CH, Kang SK, Mok JO. Contribution of subcutaneous abdominal fat on ultrasonography to carotid atherosclerosis in patients with type 2 diabetes mellitus. Cardiovasc Diabetol. 2014;13:67.PubMedCentralCrossRefPubMed Jung CH, Kim BY, Kim KJ, Jung SH, Kim CH, Kang SK, Mok JO. Contribution of subcutaneous abdominal fat on ultrasonography to carotid atherosclerosis in patients with type 2 diabetes mellitus. Cardiovasc Diabetol. 2014;13:67.PubMedCentralCrossRefPubMed
18.
go back to reference Nazare JA, Smith JD, Borel AL, Haffner SM, Balkau B, Ross R, Massien C, Alméras N, Després JP. Ethnic influences on the relations between abdominal subcutaneous and visceral adiposity, liver fat, and cardiometabolic risk profile: the International Study of Prediction of Intra-Abdominal Adiposity and Its Relationship With Cardiometabolic Risk/Intra-Abdominal Adiposity. Am J Clin Nutr. 2012;96:714–26.CrossRefPubMed Nazare JA, Smith JD, Borel AL, Haffner SM, Balkau B, Ross R, Massien C, Alméras N, Després JP. Ethnic influences on the relations between abdominal subcutaneous and visceral adiposity, liver fat, and cardiometabolic risk profile: the International Study of Prediction of Intra-Abdominal Adiposity and Its Relationship With Cardiometabolic Risk/Intra-Abdominal Adiposity. Am J Clin Nutr. 2012;96:714–26.CrossRefPubMed
19.
go back to reference Kagawa M, Kerr D, Uchida H, Binns CW. Differences in the relationship between BMI and percentage body fat between Japanese and Australian-Caucasian young men. Br J Nutr. 2006;95:1002–7.CrossRefPubMed Kagawa M, Kerr D, Uchida H, Binns CW. Differences in the relationship between BMI and percentage body fat between Japanese and Australian-Caucasian young men. Br J Nutr. 2006;95:1002–7.CrossRefPubMed
20.
go back to reference Shungin D, Winkler TW, Croteau-Chonka DC, Ferreira T, Locke AE, Mägi R, Strawbridge RJ, Pers TH, Fischer K, Justice AE, et al. New genetic loci link adipose and insulin biology to body fat distribution. Nature. 2015;518:187–96.PubMedCentralCrossRefPubMed Shungin D, Winkler TW, Croteau-Chonka DC, Ferreira T, Locke AE, Mägi R, Strawbridge RJ, Pers TH, Fischer K, Justice AE, et al. New genetic loci link adipose and insulin biology to body fat distribution. Nature. 2015;518:187–96.PubMedCentralCrossRefPubMed
21.
go back to reference Kim SK, Park SW, Hwang IJ, Lee YK, Cho YW. High fat stores in ectopic compartments in men with newly diagnosed type 2 diabetes: an anthropometric determinant of carotid atherosclerosis and insulin resistance. Int J Obes (Lond). 2010;34:105–10.CrossRef Kim SK, Park SW, Hwang IJ, Lee YK, Cho YW. High fat stores in ectopic compartments in men with newly diagnosed type 2 diabetes: an anthropometric determinant of carotid atherosclerosis and insulin resistance. Int J Obes (Lond). 2010;34:105–10.CrossRef
22.
go back to reference Després JP. Body fat distribution and risk of cardiovascular disease: an update. Circulation. 2012;126:1301–13.CrossRefPubMed Després JP. Body fat distribution and risk of cardiovascular disease: an update. Circulation. 2012;126:1301–13.CrossRefPubMed
23.
go back to reference Yamasaki Y, Kodama M, Nishizawa H, Sakamoto K, Matsuhisa M, Kajimoto Y, Kosugi K, Shimizu Y, Kawamori R, Hori M. Carotid intima-media thickness in Japanese type 2 diabetic subjects: predictors of progression and relationship with incident coronary heart disease. Diabetes Care. 2000;23:1310–5.CrossRefPubMed Yamasaki Y, Kodama M, Nishizawa H, Sakamoto K, Matsuhisa M, Kajimoto Y, Kosugi K, Shimizu Y, Kawamori R, Hori M. Carotid intima-media thickness in Japanese type 2 diabetic subjects: predictors of progression and relationship with incident coronary heart disease. Diabetes Care. 2000;23:1310–5.CrossRefPubMed
24.
go back to reference Bernard S, Sérusclat A, Targe F, Charrière S, Roth O, Beaune J, Berthezène F, Moulin P. Incremental predictive value of carotid ultrasonography in the assessment of coronary risk in a cohort of asymptomatic type 2 diabetic subjects. Diabetes Care. 2005;28:1158–62.CrossRefPubMed Bernard S, Sérusclat A, Targe F, Charrière S, Roth O, Beaune J, Berthezène F, Moulin P. Incremental predictive value of carotid ultrasonography in the assessment of coronary risk in a cohort of asymptomatic type 2 diabetic subjects. Diabetes Care. 2005;28:1158–62.CrossRefPubMed
Metadata
Title
High visceral fat with low subcutaneous fat accumulation as a determinant of atherosclerosis in patients with type 2 diabetes
Authors
Ryotaro Bouchi
Takato Takeuchi
Momoko Akihisa
Norihiko Ohara
Yujiro Nakano
Rie Nishitani
Masanori Murakami
Tatsuya Fukuda
Masamichi Fujita
Isao Minami
Hajime Izumiyama
Koshi Hashimoto
Takanobu Yoshimoto
Yoshihiro Ogawa
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2015
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-015-0302-4

Other articles of this Issue 1/2015

Cardiovascular Diabetology 1/2015 Go to the issue