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Published in: Cardiovascular Diabetology 1/2020

Open Access 01-12-2020 | Obesity | Original investigation

The additive effects of obesity on myocardial microcirculation in diabetic individuals: a cardiac magnetic resonance first-pass perfusion study

Authors: Li Jiang, Ke Shi, Ying-kun Guo, Yan Ren, Zhen-lin Li, Chun-chao Xia, Lei Li, Xi Liu, Lin-jun Xie, Yue Gao, Meng-ting Shen, Ming-yan Deng, Zhi-gang Yang

Published in: Cardiovascular Diabetology | Issue 1/2020

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Abstract

Background

The microvascular effects of obesity should be considered in diabetic individuals for elucidating underlying mechanisms and developing targeted therapies. This study aims to determine the effect of obesity on myocardial microvascular function in type 2 diabetes mellitus (T2DM) patients using cardiac magnetic resonance (CMR) first-pass perfusion imaging and assessed significant risk factors for microvascular dysfunction.

Materials and methods

Between September 2016 and May 2018, 120 patients with T2DM (45.8% women [55 of 120]; mean age, 56.45 ± 11.97 years) and 79 controls (44.3% women [35 of 79]; mean age, 54.50 ± 7.79 years) with different body mass index (BMI) scales were prospectively enrolled and underwent CMR examination. CMR-derived perfusion parameters, including upslope, time to maximum signal intensity (TTM), maximum signal intensity (MaxSI), MaxSI (-baseline), and SI (baseline), and T2DM related risk factors were analyzed among groups/subgroups both in T2DM patients and controls. Univariable and multivariable linear and logistic regression analyses were performed to assess the potential additive effect of obesity on microvascular dysfunction in diabetic individuals.

Results

Compared with controls with comparable BMIs, patients with T2DM showed reduced upslope and MaxSI and increased TTM. For both T2DM and control subgroups, perfusion function gradually declined with increasing BMI, which was confirmed by all perfusion parameters, except for TTM (all P < 0.01). In multivariable linear regression analysis, BMI (β = − 0.516; 95% confidence interval [CI], − 0.632 to − 0.357; P < 0.001), female sex (β = 0.372; 95% CI, 0.215 to 0.475; P < 0.001), diabetes duration (β = − 0.169; 95% CI, − 0.319 to − 0.025; P = 0.022) and glycated haemoglobin (β = − 0.184; 95% CI, − 0.281 to − 0.039; P = 0.010) were significantly associated with global upslope in the T2DM group. Multivariable logistic regression analysis indicated that T2DM was an independent predictor of microvascular dysfunction in normal-weight (odds ratio[OR], 6.46; 95% CI, 2.08 to 20.10; P = 0.001), overweight (OR, 7.19; 95% CI, 1.67 to 31.07; P = 0.008) and obese participants (OR, 11.21; 95% CI, 2.38 to 52.75; P = 0.002).

Conclusions

Myocardial microvascular function gradually declined with increasing BMI in both diabetes and non-diabetes status. T2DM was associated with an increased risk of microvascular dysfunction, and obesity exacerbated the adverse effect of T2DM.
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Literature
1.
go back to reference Mokdad AH, Ford ES, Bowman BA, Dietz WH, Vinicor F, Bales VS, Marks JS. Prevalence of obesity, diabetes, and obesity-related health risk factors, 2001. JAMA. 2003;289(1):76–9.CrossRef Mokdad AH, Ford ES, Bowman BA, Dietz WH, Vinicor F, Bales VS, Marks JS. Prevalence of obesity, diabetes, and obesity-related health risk factors, 2001. JAMA. 2003;289(1):76–9.CrossRef
2.
go back to reference World Health Organization. Global report on diabetes. Geneva: World Health Organization; 2016. World Health Organization. Global report on diabetes. Geneva: World Health Organization; 2016.
3.
go back to reference Alvarez CA, Lingvay I, Vuylsteke V, Koffarnus RL, Mcguire DK. Cardiovascular risk in diabetes mellitus: complication of the disease or of antihyperglycemic medications. Clin Pharmacol Ther. 2015;98(2):145–61.CrossRef Alvarez CA, Lingvay I, Vuylsteke V, Koffarnus RL, Mcguire DK. Cardiovascular risk in diabetes mellitus: complication of the disease or of antihyperglycemic medications. Clin Pharmacol Ther. 2015;98(2):145–61.CrossRef
4.
go back to reference Asghar O, Al-sunni A, Khavandi K, Khavandi A, Greenstein A, Heagerty AM, et al. Diabetic cardiomyopathy. Clin Sci (Lond). 2009;116(10):741–60.CrossRef Asghar O, Al-sunni A, Khavandi K, Khavandi A, Greenstein A, Heagerty AM, et al. Diabetic cardiomyopathy. Clin Sci (Lond). 2009;116(10):741–60.CrossRef
5.
go back to reference Seferović PM, Paulus WJ. Clinical diabetic cardiomyopathy: a two-faced disease with restrictive and dilated phenotypes. Eur Heart J. 2015;36(27):1718–27.CrossRef Seferović PM, Paulus WJ. Clinical diabetic cardiomyopathy: a two-faced disease with restrictive and dilated phenotypes. Eur Heart J. 2015;36(27):1718–27.CrossRef
6.
go back to reference Vita T, Murphy DJ, Osborne MT, et al. Association between nonalcoholic fatty liver disease at CT and coronary microvascular dysfunction at myocardial perfusion PET/CT. Radiology. 2019;291(2):330–7.CrossRef Vita T, Murphy DJ, Osborne MT, et al. Association between nonalcoholic fatty liver disease at CT and coronary microvascular dysfunction at myocardial perfusion PET/CT. Radiology. 2019;291(2):330–7.CrossRef
7.
go back to reference Camici PG, D’Amati G, Rimoldi O. Coronary microvascular dysfunction: mechanisms and functional assessment. Nat Rev Cardiol. 2015;12(1):48–62.CrossRef Camici PG, D’Amati G, Rimoldi O. Coronary microvascular dysfunction: mechanisms and functional assessment. Nat Rev Cardiol. 2015;12(1):48–62.CrossRef
8.
go back to reference Zorach B, Shaw PW, Bourque J, et al. Quantitative cardiovascular magnetic resonance perfusion imaging identifies reduced flow reserve in microvascular coronary artery disease. J Cardiovasc Magn Reson. 2018;20(1):14.CrossRef Zorach B, Shaw PW, Bourque J, et al. Quantitative cardiovascular magnetic resonance perfusion imaging identifies reduced flow reserve in microvascular coronary artery disease. J Cardiovasc Magn Reson. 2018;20(1):14.CrossRef
9.
go back to reference Liu X, Yang ZG, Gao Y, et al. Left ventricular subclinical myocardial dysfunction in uncomplicated type 2 diabetes mellitus is associated with impaired myocardial perfusion: a contrast-enhanced cardiovascular magnetic resonance study. Cardiovasc Diabetol. 2018;17(1):139.CrossRef Liu X, Yang ZG, Gao Y, et al. Left ventricular subclinical myocardial dysfunction in uncomplicated type 2 diabetes mellitus is associated with impaired myocardial perfusion: a contrast-enhanced cardiovascular magnetic resonance study. Cardiovasc Diabetol. 2018;17(1):139.CrossRef
10.
go back to reference Bajaj NS, Osborne MT, Gupta A, et al. Coronary microvascular dysfunction and cardiovascular risk in obese patients. J Am Coll Cardiol. 2018;72(7):707–17.CrossRef Bajaj NS, Osborne MT, Gupta A, et al. Coronary microvascular dysfunction and cardiovascular risk in obese patients. J Am Coll Cardiol. 2018;72(7):707–17.CrossRef
11.
go back to reference Naresh NK, Butcher JT, Lye RJ, et al. Cardiovascular magnetic resonance detects the progression of impaired myocardial perfusion reserve and increased left-ventricular mass in mice fed a high-fat diet. J Cardiovasc Magn Reson. 2016;18(1):1–11.CrossRef Naresh NK, Butcher JT, Lye RJ, et al. Cardiovascular magnetic resonance detects the progression of impaired myocardial perfusion reserve and increased left-ventricular mass in mice fed a high-fat diet. J Cardiovasc Magn Reson. 2016;18(1):1–11.CrossRef
12.
go back to reference Li R, Yang ZG, Wen LY, et al. Regional myocardial microvascular dysfunction in cardiac amyloid light-chain amyloidosis: assessment with 3T cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2016;18:16.CrossRef Li R, Yang ZG, Wen LY, et al. Regional myocardial microvascular dysfunction in cardiac amyloid light-chain amyloidosis: assessment with 3T cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2016;18:16.CrossRef
13.
go back to reference Chamberlain JJ, Rhinehart AS, et al. Diagnosis and management of diabetes: synopsis of the 2016 American Diabetes Association Standards of Medical Care in Diabetes. Ann Intern Med. 2016;164(8):542–52.CrossRef Chamberlain JJ, Rhinehart AS, et al. Diagnosis and management of diabetes: synopsis of the 2016 American Diabetes Association Standards of Medical Care in Diabetes. Ann Intern Med. 2016;164(8):542–52.CrossRef
14.
go back to reference Maron BJ, Towbin JA, Thiene G, et al. Contemporary definitions and classification of the cardiomyopathies. Circulation. 2006;113(14):1807–16.CrossRef Maron BJ, Towbin JA, Thiene G, et al. Contemporary definitions and classification of the cardiomyopathies. Circulation. 2006;113(14):1807–16.CrossRef
15.
go back to reference WHO Expert Consultation. Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet. 2004;363(9403):157–63.CrossRef WHO Expert Consultation. Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet. 2004;363(9403):157–63.CrossRef
16.
go back to reference Badimon L, Bugiardini R, Cenko E, et al. Position paper of the European Society of Cardiolog-working group of coronary pathophysiology and microcirculation: obesity and heart disease. Eur Heart J. 2017;38(25):1951–8.CrossRef Badimon L, Bugiardini R, Cenko E, et al. Position paper of the European Society of Cardiolog-working group of coronary pathophysiology and microcirculation: obesity and heart disease. Eur Heart J. 2017;38(25):1951–8.CrossRef
17.
go back to reference Schulz-Menger J, Bluemke DA, Bremerich J, et al. Standardized image interpretation and post processing in cardiovascular magnetic resonance: society for Cardiovascular Magnetic Resonance (SCMR) Board of Trustees Task Force on Standardized Post Processing. J Cardiovasc Magn Reson. 2013;15(1):1.CrossRef Schulz-Menger J, Bluemke DA, Bremerich J, et al. Standardized image interpretation and post processing in cardiovascular magnetic resonance: society for Cardiovascular Magnetic Resonance (SCMR) Board of Trustees Task Force on Standardized Post Processing. J Cardiovasc Magn Reson. 2013;15(1):1.CrossRef
18.
go back to reference Schlett CL, Lorbeer R, Arndt C, et al. Association between abdominal adiposity and subclinical measures of left-ventricular remodeling in diabetics, prediabetics and normal controls without history of cardiovascular disease as measured by magnetic resonance imaging: results from the KORA-FF4 S. Cardiovasc Diabetol. 2018;17(1):1–12.CrossRef Schlett CL, Lorbeer R, Arndt C, et al. Association between abdominal adiposity and subclinical measures of left-ventricular remodeling in diabetics, prediabetics and normal controls without history of cardiovascular disease as measured by magnetic resonance imaging: results from the KORA-FF4 S. Cardiovasc Diabetol. 2018;17(1):1–12.CrossRef
19.
go back to reference Mazumder PK, O’Neill BT, Roberts MW. Impaired cardiac efficiency and increased fatty acid oxidation in insulin-resistant ob/ob mouse hearts. Diabetes. 2004;53(9):2366–74.CrossRef Mazumder PK, O’Neill BT, Roberts MW. Impaired cardiac efficiency and increased fatty acid oxidation in insulin-resistant ob/ob mouse hearts. Diabetes. 2004;53(9):2366–74.CrossRef
20.
go back to reference Fukushima A, Lopaschuk GD. Cardiac fatty acid oxidation in heart failure associated with obesity and diabetes. Biochim Biophys Acta. 2016;1861(10):1525–34.CrossRef Fukushima A, Lopaschuk GD. Cardiac fatty acid oxidation in heart failure associated with obesity and diabetes. Biochim Biophys Acta. 2016;1861(10):1525–34.CrossRef
21.
go back to reference Hinkel R, Howe A, Renner S, et al. Diabetes mellitus-induced microvascular destabilization in the myocardium. J Am Coll Cardiol. 2017;69(2):131–43.CrossRef Hinkel R, Howe A, Renner S, et al. Diabetes mellitus-induced microvascular destabilization in the myocardium. J Am Coll Cardiol. 2017;69(2):131–43.CrossRef
22.
go back to reference Zhang L, Keung W, Samokhvalov V, et al. Role of fatty acid uptake and fatty acid β-oxidation in mediating insulin resistance in heart and skeletal muscle. Biochim Biophys Acta. 2010;1801(1):1–22.CrossRef Zhang L, Keung W, Samokhvalov V, et al. Role of fatty acid uptake and fatty acid β-oxidation in mediating insulin resistance in heart and skeletal muscle. Biochim Biophys Acta. 2010;1801(1):1–22.CrossRef
23.
go back to reference Schindler TH, Cardenas J, Prior JO, Facta AD, Kreissl MC, Zhang XL, et al. Relationship between increasing body weight, insulin resistance, inflammation, adipocytokine leptin, and coronary circulatory function. J Am Coll Cardiol. 2006;47(6):1188–95.CrossRef Schindler TH, Cardenas J, Prior JO, Facta AD, Kreissl MC, Zhang XL, et al. Relationship between increasing body weight, insulin resistance, inflammation, adipocytokine leptin, and coronary circulatory function. J Am Coll Cardiol. 2006;47(6):1188–95.CrossRef
24.
go back to reference Eng J, McClelland RL, Gomes AS, Hundley WG, Cheng S, Wu CO, et al. Adverse left ventricular remodeling and age assessed with cardiac MR imaging: the multi-ethnic study of atherosclerosis. Radiology. 2016;278(3):714–22.CrossRef Eng J, McClelland RL, Gomes AS, Hundley WG, Cheng S, Wu CO, et al. Adverse left ventricular remodeling and age assessed with cardiac MR imaging: the multi-ethnic study of atherosclerosis. Radiology. 2016;278(3):714–22.CrossRef
25.
go back to reference Udelson JE, Konstam MA. Ventricular remodeling fundamental to the progression (and regression) of heart failure. J Am Coll Cardiol. 2011;57(13):1477–9.CrossRef Udelson JE, Konstam MA. Ventricular remodeling fundamental to the progression (and regression) of heart failure. J Am Coll Cardiol. 2011;57(13):1477–9.CrossRef
26.
go back to reference Leite-moreira AF. Diabetic cardiomyopathy: understanding the molecular and cellular basis to progress in diagnosis and treatment. Hear Fail Rev. 2012;1:325–44. Leite-moreira AF. Diabetic cardiomyopathy: understanding the molecular and cellular basis to progress in diagnosis and treatment. Hear Fail Rev. 2012;1:325–44.
27.
go back to reference Heydari B, Juan YH, Liu H, et al. Stress perfusion cardiac magnetic resonance imaging effectively risk stratifies diabetic patients with suspected myocardial ischemia. Circ Cardiovasc Imaging. 2016;9(4):1–12.CrossRef Heydari B, Juan YH, Liu H, et al. Stress perfusion cardiac magnetic resonance imaging effectively risk stratifies diabetic patients with suspected myocardial ischemia. Circ Cardiovasc Imaging. 2016;9(4):1–12.CrossRef
28.
go back to reference Nathan DM. Diabetes advances in diagnosis and treatment. JAMA. 2015;314(10):1052–62.CrossRef Nathan DM. Diabetes advances in diagnosis and treatment. JAMA. 2015;314(10):1052–62.CrossRef
29.
go back to reference Skyler JS, Bergenstal R, Bonow RO, et al. Intensive glycemic control and the prevention of cardiovascular events: implications of the ACCORD, ADVANCE, and VA diabetes trials. Diabetes Care. 2009;32(1):187–92.CrossRef Skyler JS, Bergenstal R, Bonow RO, et al. Intensive glycemic control and the prevention of cardiovascular events: implications of the ACCORD, ADVANCE, and VA diabetes trials. Diabetes Care. 2009;32(1):187–92.CrossRef
30.
go back to reference Lund-andersen H, Parving H, Pedersen O. Effect of a Multifactorial Intervention on Mortality in Type 2 Diabetes. N Engl J Med. 2008;358(6):580–91.CrossRef Lund-andersen H, Parving H, Pedersen O. Effect of a Multifactorial Intervention on Mortality in Type 2 Diabetes. N Engl J Med. 2008;358(6):580–91.CrossRef
31.
go back to reference Adingupu DD, Göpel SO, Grönros J, et al. SGLT2 inhibition with empagliflozin improves coronary microvascular function and cardiac contractility in prediabetic ob/ob−/− mice. Cardiovasc Diabetol. 2019;18(1):16.CrossRef Adingupu DD, Göpel SO, Grönros J, et al. SGLT2 inhibition with empagliflozin improves coronary microvascular function and cardiac contractility in prediabetic ob/ob−/− mice. Cardiovasc Diabetol. 2019;18(1):16.CrossRef
32.
go back to reference Nilsson M, Bové KB, Suhrs E, et al. The effect of DPP-4-protected GLP-1 (7-36) on coronary microvascular function in obese adults. Int J Cardiol Heart Vasc. 2019;22:139–44.PubMedPubMedCentral Nilsson M, Bové KB, Suhrs E, et al. The effect of DPP-4-protected GLP-1 (7-36) on coronary microvascular function in obese adults. Int J Cardiol Heart Vasc. 2019;22:139–44.PubMedPubMedCentral
33.
go back to reference Kenny HC, Abel ED. Heart failure in type 2 diabetes mellitus. Circ Res. 2019;124(1):121–41.CrossRef Kenny HC, Abel ED. Heart failure in type 2 diabetes mellitus. Circ Res. 2019;124(1):121–41.CrossRef
34.
go back to reference Murphy E, Amanakis G, Fillmore N, Parks RJ, Sun J. Sex differences in metabolic cardiomyopathy. Cardiovasc Res. 2017;113(4):370–7.CrossRef Murphy E, Amanakis G, Fillmore N, Parks RJ, Sun J. Sex differences in metabolic cardiomyopathy. Cardiovasc Res. 2017;113(4):370–7.CrossRef
35.
go back to reference Norhammar A, Schenck-Gustafsson K. Type 2 diabetes and cardiovascular disease in women. Diabetologia. 2013;56(1):1–9.CrossRef Norhammar A, Schenck-Gustafsson K. Type 2 diabetes and cardiovascular disease in women. Diabetologia. 2013;56(1):1–9.CrossRef
36.
go back to reference Knowlton AA, Lee AR. Estrogen and the cardiovascular system. Pharmacol Ther. 2012;135(1):54–70.CrossRef Knowlton AA, Lee AR. Estrogen and the cardiovascular system. Pharmacol Ther. 2012;135(1):54–70.CrossRef
37.
go back to reference ASCI CCT and CMR Guideline Working Group, Chan CW, Choi BW, Jinzaki M, Kitagawa K, Tsai IC, Yong HS, Yu W. ASCI 2010 standardized practice protocol for cardiac magnetic resonance imaging: a report of the Asian society of cardiovascular imaging cardiac computed tomography and cardiac magnetic resonance imaging guideline working group. Int J Cardiovasc Imaging. 2010;26(suppl 2):187–202.PubMedCentral ASCI CCT and CMR Guideline Working Group, Chan CW, Choi BW, Jinzaki M, Kitagawa K, Tsai IC, Yong HS, Yu W. ASCI 2010 standardized practice protocol for cardiac magnetic resonance imaging: a report of the Asian society of cardiovascular imaging cardiac computed tomography and cardiac magnetic resonance imaging guideline working group. Int J Cardiovasc Imaging. 2010;26(suppl 2):187–202.PubMedCentral
38.
go back to reference Henzlova MJ, Duvall WL, Einstein AJ, Travin MI, Verberne HJ. ASNC imaging guidelines for SPECT nuclear cardiology procedures: stress, protocols, and tracers. J Nucl Cardiol. 2016;23(3):606–39.CrossRef Henzlova MJ, Duvall WL, Einstein AJ, Travin MI, Verberne HJ. ASNC imaging guidelines for SPECT nuclear cardiology procedures: stress, protocols, and tracers. J Nucl Cardiol. 2016;23(3):606–39.CrossRef
Metadata
Title
The additive effects of obesity on myocardial microcirculation in diabetic individuals: a cardiac magnetic resonance first-pass perfusion study
Authors
Li Jiang
Ke Shi
Ying-kun Guo
Yan Ren
Zhen-lin Li
Chun-chao Xia
Lei Li
Xi Liu
Lin-jun Xie
Yue Gao
Meng-ting Shen
Ming-yan Deng
Zhi-gang Yang
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2020
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-020-01028-1

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