Abstract
Purpose
Although up to 20% of people with type 2 diabetes (DM) have normal BMI (< 25 kg/m2), it remains unclear whether there is a difference in the development of cardiac dysfunction between those with normal and higher BMI. Furthermore, little is known about the relationship of visceral fat with BMI or fitness in asymptomatic patients with DM.
Methods
We prospectively enrolled asymptomatic patients with DM and divided into two groups: BMI ≥ 25kg/m2 (overweight/obese group) versus < 25kg/m2(normal-weight group). Resting echocardiogram followed by exercise stress echocardiogram and exercise gas exchange analysis (in a subgroup) was performed. Cardiac function was evaluated using left ventricular longitudinal strain (LVLS), E/e’, and relative wall thickness (RWT). In addition, epicardial fat thickness (EFT) was measured to estimate visceral fat.
Results
Normal-weight patients with DM had more EFT compared with overweight/obese patients (0.66 ± 0.17 cm vs. 0.59 ± 0.22 cm, p < 0.05), despite the overlap between the groups. There was no significant difference in the prevalence of LV remodeling (p = 0.49), impaired LVLS (p = 0.22), or increased E/e’ (p = 0.26), and these were consistently observed when matched for race. The majority of patients (63%) achieved ≥ 85% of percent peak-predicted VO2. At peak, there was no significant difference in peak VO2 normalized by eLBM (36.4 ± 7.7 vs. 37.8 ± 7.1 ml/kg eLBM/min, p = 0.43) while VO2 normalized by weight (23.6 ± 6.5 vs. 29.6 ± 6.7 ml/kg/min, p < 0.001) and VO2 ratio (5.7 ± 1.7 vs. 7.3 ± 2.4 METs, p = 0.001) were significantly lower in patients with obese/overweight group. There was no significant difference between patients with higher and lower EFT.
Conclusions
Patients with DM and normal BMI have excess epicardial fat compared to those with overweight/obese. Epicardial fat was not directly linked to prevalence of subclinical dysfunction.
Similar content being viewed by others
Data Availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Chan JCN, Gregg EW, Sargent J, Horton R (2016) Reducing global diabetes burden by implementing solutions and identifying gaps: a Lancet Commission [Internet]. The Lancet. p. 1494–5. https://doi.org/10.1016/s0140-6736(16)30165-9
Rosito GA, Massaro JM, Hoffmann U, Ruberg FL, Mahabadi AA, Vasan RS et al (2008) Pericardial Fat, Visceral Abdominal Fat, Cardiovascular Disease Risk Factors, and Vascular Calcification in a Community-Based Sample [Internet]. Circulation. p. 605–13. https://doi.org/10.1161/circulationaha.107.743062
Iacobellis G, Corradi D, Sharma AM (2005) Epicardial adipose tissue: anatomic, biomolecular and clinical relationships with the heart. Nat Clin Pract Cardiovasc Med 2:536–543
Baker AR, da Silva NF, Quinn DW, Harte AL, Pagano D, Bonser RS et al (2006) Human epicardial adipose tissue expresses a pathogenic profile of adipocytokines in patients with cardiovascular disease. Cardiovasc Diabetol 5:1
Gorter PM, van Lindert ASR, de Vos AM, Meijs MFL, van der Graaf Y, Doevendans PA et al (2008) Quantification of epicardial and peri-coronary fat using cardiac computed tomography; reproducibility and relation with obesity and metabolic syndrome in patients suspected of coronary artery disease [Internet]. Atherosclerosis. p. 896–903. https://doi.org/10.1016/j.atherosclerosis.2007.08.016
Iacobellis G, Willens HJ (2009) Echocardiographic epicardial fat: a review of research and clinical applications. J Am Soc Echocardiogr 22:1311–1319 quiz 1417–8
Carnethon MR, De Chavez PJD, Biggs ML, Lewis CE, Pankow JS, Bertoni AG et al (2012) Association of Weight Status With Mortality in Adults With Incident Diabetes [Internet]. JAMA. https://doi.org/10.1001/jama.2012.9282
Heidenreich PA, Bozkurt B, Aguilar D, Allen LA, Byun J-J, Colvin MM et al (2022) 2022 American College of Cardiology/American Heart Association/Heart failure society of America Guideline for the management of Heart failure: executive Summary. J Card Fail 28:810–830
Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L et al (2015) Recommendations for Cardiac Chamber Quantification by Echocardiography in Adults: An Update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging [Internet]. Journal of the American Society of Echocardiography. p. 1–39.e14. https://doi.org/10.1016/j.echo.2014.10.003
Kobayashi Y, Ariyama M, Kobayashi Y, Giraldeau G, Fleischman D, Kozelj M et al (2016) Comparison of left ventricular manual versus automated derived longitudinal strain: implications for clinical practice and research [Internet]. The International Journal of Cardiovascular Imaging. p. 429–37. https://doi.org/10.1007/s10554-015-0804-x
Kobayashi Y, Moneghetti KJ, Boralkar K, Amsallem M, Tuzovic M, Liang D et al (2017) Challenging the complementarity of different metrics of left atrial function: insight from a cardiomyopathy-based study [Internet]. European Heart Journal - Cardiovascular Imaging. p. 1153–62. https://doi.org/10.1093/ehjci/jew121
Iacobellis G, Assael F, Ribaudo MC, Zappaterreno A, Alessi G, Di Mario U et al (2003) Epicardial Fat from Echocardiography: A New Method for Visceral Adipose Tissue Prediction [Internet]. Obesity Research. p. 304–10. https://doi.org/10.1038/oby.2003.45
Nelson AJ, Worthley MI, Psaltis PJ, Carbone A, Dundon BK, Duncan RF et al (2009) Validation of cardiovascular magnetic resonance assessment of pericardial adipose tissue volume. J Cardiovasc Magn Reson 11:15
Goel R, Alharthi M, Jiamsripong P, Cha S, Mookadam F (2010) Epicardial fat and its association with cardiovascular risk: A cross-sectional observational study [Internet]. Heart Views. p. 103. https://doi.org/10.4103/1995-705x.76801
Iacobellis G (2020) Epicardial adipose tissue: from cell to Clinic. Springer
Yingchoncharoen T, Agarwal S, Popović ZB, Marwick TH (2013) Normal Ranges of Left Ventricular Strain: A Meta-Analysis [Internet]. Journal of the American Society of Echocardiography. p. 185–91. https://doi.org/10.1016/j.echo.2012.10.008
Redfield MM, Jacobsen SJ, Burnett JC Jr, Mahoney DW, Bailey KR, Rodeheffer RJ (2003) Burden of systolic and diastolic ventricular dysfunction in the community: appreciating the scope of the heart failure epidemic. JAMA 289:194–202
Ommen SR, Nishimura RA, Appleton CP, Miller FA, Oh JK, Redfield MM et al (2000) Clinical utility of Doppler echocardiography and tissue doppler imaging in the estimation of left ventricular filling pressures: a comparative simultaneous doppler-catheterization study. Circulation 102:1788–1794
Myers J, Buchanan N, Walsh D, Kraemer M, McAuley P, Hamilton-Wessler M et al (1991) Comparison of the ramp versus standard exercise protocols. J Am Coll Cardiol 17:1334–1342
Balady GJ, Arena R, Sietsema K, Myers J, Coke L, Fletcher GF et al (2010) Clinician’s guide to cardiopulmonary exercise testing in adults: a scientific statement from the American Heart Association. Circulation 122:191–225
Kokkinos P, Kaminsky LA, Arena R, Zhang J, Myers J (2017) New Generalized equation for Predicting maximal oxygen uptake (from the Fitness Registry and the importance of Exercise National Database). Am J Cardiol 120:688–692
Sacks HS, Fain JN (2007) Human epicardial adipose tissue: A review [Internet]. American Heart Journal. p. 907–17. https://doi.org/10.1016/j.ahj.2007.03.019
Poirier P, Giles TD, Bray GA, Hong Y, Stern JS, Pi-Sunyer FX et al (2006) Obesity and cardiovascular disease: pathophysiology, evaluation, and effect of weight loss: an update of the 1997 American Heart Association Scientific Statement on obesity and heart disease from the obesity Committee of the Council on Nutrition, Physical Activity, and metabolism. Circulation 113:898–918
Hubert HB, Feinleib M, McNamara PM, Castelli WP (1983) Obesity as an independent risk factor for cardiovascular disease: a 26-year follow-up of participants in the Framingham Heart Study. Circulation 67:968–977
He J, Ogden LG, Bazzano LA, Vupputuri S, Loria C, Whelton PK (2001) Risk factors for congestive heart failure in US men and women: NHANES I epidemiologic follow-up study. Arch Intern Med 161:996–1002
Murphy NF, MacIntyre K, Stewart S, Hart CL, Hole D, McMurray JJV (2006) Long-term cardiovascular consequences of obesity: 20-year follow-up of more than 15 000 middle-aged men and women (the Renfrew–Paisley study) [Internet]. European Heart Journal. p. 96–106. https://doi.org/10.1093/eurheartj/ehi506
Kenchaiah S, Evans JC, Levy D, Wilson PWF, Benjamin EJ, Larson MG et al (2002) Obesity and the Risk of Heart Failure [Internet]. New England Journal of Medicine. p. 305–13. https://doi.org/10.1056/nejmoa020245
Bahrami H, Bluemke DA, Kronmal R, Bertoni AG, Lloyd-Jones DM, Shahar E et al (2008) Novel metabolic risk factors for incident heart failure and their relationship with obesity: the MESA (multi-ethnic study of atherosclerosis) study. J Am Coll Cardiol 51:1775–1783
Shah RV, Anderson A, Ding J, Budoff M, Rider O, Petersen SE et al (2017) Pericardial, but not hepatic, Fat by CT is Associated with CV Outcomes and structure: the multi-ethnic study of atherosclerosis. JACC Cardiovasc Imaging 10:1016–1027
Abraham TM, Pedley A, Massaro JM, Hoffmann U, Fox CS (2015) Association Between Visceral and Subcutaneous Adipose Depots and Incident Cardiovascular Disease Risk Factors [Internet]. Circulation. p. 1639–47. https://doi.org/10.1161/circulationaha.114.015000
Okura T, Nakata Y, Yamabuki K, Tanaka K (2004) Regional body composition changes exhibit opposing effects on coronary heart disease risk factors. Arterioscler Thromb Vasc Biol 24:923–929
Church TS, Cheng YJ, Earnest CP, Barlow CE, Gibbons LW, Priest EL et al (2004) Exercise capacity and body composition as predictors of mortality among men with diabetes. Diabetes Care 27:83–88
Wei M, Gibbons LW, Kampert JB, Nichaman MZ, Blair SN (2000) Low cardiorespiratory fitness and physical inactivity as predictors of mortality in men with type 2 diabetes. Ann Intern Med 132:605–611
Savonen K, Krachler B, Hassinen M et al (2012) The current standard measure of cardiorespiratory fitness introduces confounding by body mass: the DR’s EXTRA study. Int J Obes 36:1135–1140
Goran M, Fields DA, Hunter GR et al (2000) Total body fat does not influence maximal aerobic capacity. Int J Obes Relat Metab Disord 24:841–848
Krachler B, Savonen K, Komulainen P et al (2015) Cardiopulmonary fitness is a function of lean mass, not total body weight: the DR’s EXTRA study. Eur J Prev Cardiol 22:1171–1179
Osman AF, Mehra MR, Lavie CJ et al (2000) The incremental prognostic importance of body fat adjusted peak oxygen consumption in chronic heart failure. J Am Coll Cardiol 36:2126–2131
Nesti L, Pugliese NR, Chiriacò M et al (2023) Epicardial adipose tissue thickness is associated with reduced peak oxygen consumption and systolic reserve in patients with type 2 diabetes and normal heart function. Diabetes Obes Metab 25:177–188
Pugliese NR, Paneni F, Mazzola M et al (2021) Impact of epicardial adipose tissue on cardiovascular haemodynamics, metabolic profile, and prognosis in heart failure. Eur J Heart Fail 23:1858–1871
Williams R, Periasamy M (2020) Genetic and environmental factors contributing to visceral adiposity in asian populations. Endocrinol Metab (Seoul) 35:681–695
Donal E, Raud-Raynier P, De Place C, Gervais R, Rosier A, Roulaud M et al (2008) Resting echocardiographic assessments of left atrial function and filling pressure interest in the understanding of exercise capacity in patients with chronic congestive heart failure. J Am Soc Echocardiogr 21:703–710
von Roeder M, Rommel K-P, Kowallick JT, Blazek S, Besler C, Fengler K et al (2017) Influence of Left Atrial Function on Exercise Capacity and Left Ventricular Function in Patients With Heart Failure and Preserved Ejection Fraction. Circ Cardiovasc Imaging [Internet]. ;10. https://doi.org/10.1161/CIRCIMAGING.116.005467
Kusunose K, Motoki H, Popovic ZB, Thomas JD, Klein AL, Marwick TH (2012) Independent association of left atrial function with exercise capacity in patients with preserved ejection fraction. Heart 98:1311–1317
Freed BH, Daruwalla V, Cheng JY, Aguilar FG, Beussink L, Choi A et al (2016) Prognostic Utility and Clinical Significance of Cardiac Mechanics in Heart Failure With Preserved Ejection Fraction: Importance of Left Atrial Strain. Circ Cardiovasc Imaging [Internet]. ;9. https://doi.org/10.1161/CIRCIMAGING.115.003754
Naeije R, Chesler N (2012) Pulmonary Circulation at Exercise [Internet]. Comprehensive Physiology. p. 711–41. https://doi.org/10.1002/cphy.c100091
Acknowledgements
This work was supported by the Stanford Diabetes Research Center P30DK116074, the National Institutes of Health under award number R18DK09639405 and R01DK08137110 as well as the grand from Philips Royal Precision Medicine Initiative.
Author information
Authors and Affiliations
Contributions
Y.K. and F.H. conceived and assisted with the design of the study. Y.K., T.N and J.C. performed data curation and Y.K. performed formal data analysis. Y.K. and F.H. interpreted the data and wrote the manuscript. T.N., J.C., N.C., T.K., and L.P. reviewed and revised the manuscript critically for important intellectual content. All authors approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no potential conflict of interest with respect to the research.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Kobayashi, Y., Nishi, T., Christle, J.W. et al. Epicardial fat and Stage B heart failure among overweight/obese and normal weight individuals with diabetes mellitus. Int J Cardiovasc Imaging 39, 2451–2461 (2023). https://doi.org/10.1007/s10554-023-02944-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10554-023-02944-5