Skip to main content
Top
Published in: Cardiovascular Diabetology 1/2011

Open Access 01-12-2011 | Original investigation

Cardiac lipid content is unresponsive to a physical activity training intervention in type 2 diabetic patients, despite improved ejection fraction

Authors: Vera B Schrauwen-Hinderling, Ruth CR Meex, Matthijs KC Hesselink, Tineke van de Weijer, Tim Leiner, Michael Schär, Hildo J Lamb, Joachim E Wildberger, Jan FC Glatz, Patrick Schrauwen, M Eline Kooi

Published in: Cardiovascular Diabetology | Issue 1/2011

Login to get access

Abstract

Background

Increased cardiac lipid content has been associated with diabetic cardiomyopathy. We recently showed that cardiac lipid content is reduced after 12 weeks of physical activity training in healthy overweight subjects. The beneficial effect of exercise training on cardiovascular risk is well established and the decrease in cardiac lipid content with exercise training in healthy overweight subjects was accompanied by improved ejection fraction. It is yet unclear whether diabetic patients respond similarly to physical activity training and whether a lowered lipid content in the heart is necessary for improvements in cardiac function. Here, we investigated whether exercise training is able to lower cardiac lipid content and improve cardiac function in type 2 diabetic patients.

Methods

Eleven overweight-to-obese male patients with type 2 diabetes mellitus (age: 58.4 ± 0.9 years, BMI: 29.9 ± 0.01 kg/m2) followed a 12-week training program (combination endurance/strength training, three sessions/week). Before and after training, maximal whole body oxygen uptake (VO2max) and insulin sensitivity (by hyperinsulinemic, euglycemic clamp) was determined. Systolic function was determined under resting conditions by CINE-MRI and cardiac lipid content in the septum of the heart by Proton Magnetic Resonance Spectroscopy.

Results

VO2max increased (from 27.1 ± 1.5 to 30.1 ± 1.6 ml/min/kg, p = 0.001) and insulin sensitivity improved upon training (insulin stimulated glucose disposal (delta Rd of glucose) improved from 5.8 ± 1.9 to 10.3 ± 2.0 μmol/kg/min, p = 0.02. Left-ventricular ejection fraction improved after training (from 50.5 ± 2.0 to 55.6 ± 1.5%, p = 0.01) as well as cardiac index and cardiac output. Unexpectedly, cardiac lipid content in the septum remained unchanged (from 0.80 ± 0.22% to 0.95 ± 0.21%, p = 0.15).

Conclusions

Twelve weeks of progressive endurance/strength training was effective in improving VO2max, insulin sensitivity and cardiac function in patients with type 2 diabetes mellitus. However, cardiac lipid content remained unchanged. These data suggest that a decrease in cardiac lipid content in type 2 diabetic patients is not a prerequisite for improvements in cardiac function.

Trial registration

Appendix
Available only for authorised users
Literature
1.
go back to reference Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C: Heart disease and stroke statistics--2010 update: a report from the American Heart Association. Circulation. 2010, 121: e46-e215.CrossRefPubMed Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C: Heart disease and stroke statistics--2010 update: a report from the American Heart Association. Circulation. 2010, 121: e46-e215.CrossRefPubMed
2.
go back to reference Bibbins-Domingo K, Lin F, Vittinghoff E, Barrett-Connor E, Hulley SB, Grady D, Shlipak MG: Predictors of heart failure among women with coronary disease. Circulation. 2004, 110: 1424-1430. 10.1161/01.CIR.0000141726.01302.83.CrossRefPubMed Bibbins-Domingo K, Lin F, Vittinghoff E, Barrett-Connor E, Hulley SB, Grady D, Shlipak MG: Predictors of heart failure among women with coronary disease. Circulation. 2004, 110: 1424-1430. 10.1161/01.CIR.0000141726.01302.83.CrossRefPubMed
3.
go back to reference Yagyu H, Chen G, Yokoyama M, Hirata K, Augustus A, Kako Y, Seo T, Hu Y, Lutz EP, Merkel M: Lipoprotein lipase (LpL) on the surface of cardiomyocytes increases lipid uptake and produces a cardiomyopathy. J Clin Invest. 2003, 111: 419-426.PubMedCentralCrossRefPubMed Yagyu H, Chen G, Yokoyama M, Hirata K, Augustus A, Kako Y, Seo T, Hu Y, Lutz EP, Merkel M: Lipoprotein lipase (LpL) on the surface of cardiomyocytes increases lipid uptake and produces a cardiomyopathy. J Clin Invest. 2003, 111: 419-426.PubMedCentralCrossRefPubMed
4.
go back to reference Chiu HC, Kovacs A, Ford DA, Hsu FF, Garcia R, Herrero P, Saffitz JE, Schaffer JE: A novel mouse model of lipotoxic cardiomyopathy. J Clin Invest. 2001, 107: 813-822. 10.1172/JCI10947.PubMedCentralCrossRefPubMed Chiu HC, Kovacs A, Ford DA, Hsu FF, Garcia R, Herrero P, Saffitz JE, Schaffer JE: A novel mouse model of lipotoxic cardiomyopathy. J Clin Invest. 2001, 107: 813-822. 10.1172/JCI10947.PubMedCentralCrossRefPubMed
5.
go back to reference Cheng L, Ding G, Qin Q, Huang Y, Lewis W, He N, Evans RM, Schneider MD, Brako FA, Xiao Y: Cardiomyocyte-restricted peroxisome proliferator-activated receptor-delta deletion perturbs myocardial fatty acid oxidation and leads to cardiomyopathy. Nat Med. 2004, 10: 1245-1250. 10.1038/nm1116.CrossRefPubMed Cheng L, Ding G, Qin Q, Huang Y, Lewis W, He N, Evans RM, Schneider MD, Brako FA, Xiao Y: Cardiomyocyte-restricted peroxisome proliferator-activated receptor-delta deletion perturbs myocardial fatty acid oxidation and leads to cardiomyopathy. Nat Med. 2004, 10: 1245-1250. 10.1038/nm1116.CrossRefPubMed
6.
go back to reference Nielsen LB, Bartels ED, Bollano E: Overexpression of apolipoprotein B in the heart impedes cardiac triglyceride accumulation and development of cardiac dysfunction in diabetic mice. J Biol Chem. 2002, 277: 27014-27020. 10.1074/jbc.M203458200.CrossRefPubMed Nielsen LB, Bartels ED, Bollano E: Overexpression of apolipoprotein B in the heart impedes cardiac triglyceride accumulation and development of cardiac dysfunction in diabetic mice. J Biol Chem. 2002, 277: 27014-27020. 10.1074/jbc.M203458200.CrossRefPubMed
7.
go back to reference Lee Y, Naseem RH, Duplomb L, Park BH, Garry DJ, Richardson JA, Schaffer JE, Unger RH: Hyperleptinemia prevents lipotoxic cardiomyopathy in acyl CoA synthase transgenic mice. Proc Natl Acad Sci USA. 2004, 101: 13624-13629. 10.1073/pnas.0405499101.PubMedCentralCrossRefPubMed Lee Y, Naseem RH, Duplomb L, Park BH, Garry DJ, Richardson JA, Schaffer JE, Unger RH: Hyperleptinemia prevents lipotoxic cardiomyopathy in acyl CoA synthase transgenic mice. Proc Natl Acad Sci USA. 2004, 101: 13624-13629. 10.1073/pnas.0405499101.PubMedCentralCrossRefPubMed
8.
go back to reference McGavock JM, Lingvay I, Zib I, Tillery T, Salas N, Unger R, Levine BD, Raskin P, Victor RG, Szczepaniak LS: Cardiac steatosis in diabetes mellitus: a 1H-magnetic resonance spectroscopy study. Circulation. 2007, 116: 1170-1175. 10.1161/CIRCULATIONAHA.106.645614.CrossRefPubMed McGavock JM, Lingvay I, Zib I, Tillery T, Salas N, Unger R, Levine BD, Raskin P, Victor RG, Szczepaniak LS: Cardiac steatosis in diabetes mellitus: a 1H-magnetic resonance spectroscopy study. Circulation. 2007, 116: 1170-1175. 10.1161/CIRCULATIONAHA.106.645614.CrossRefPubMed
9.
go back to reference Rijzewijk LJ, van der Meer RW, Smit JW, Diamant M, Bax JJ, Hammer S, Romijn JA, de Roos A, Lamb HJ: Myocardial steatosis is an independent predictor of diastolic dysfunction in type 2 diabetes mellitus. J Am Coll Cardiol. 2008, 52: 1793-1799. 10.1016/j.jacc.2008.07.062.CrossRefPubMed Rijzewijk LJ, van der Meer RW, Smit JW, Diamant M, Bax JJ, Hammer S, Romijn JA, de Roos A, Lamb HJ: Myocardial steatosis is an independent predictor of diastolic dysfunction in type 2 diabetes mellitus. J Am Coll Cardiol. 2008, 52: 1793-1799. 10.1016/j.jacc.2008.07.062.CrossRefPubMed
10.
go back to reference Kankaanpaa M, Lehto HR, Parkka JP, Komu M, Viljanen A, Ferrannini E, Knuuti J, Nuutila P, Parkkola R, Iozzo P: Myocardial triglyceride content and epicardial fat mass in human obesity: relationship to left ventricular function and serum free fatty acid levels. J Clin Endocrinol Metab. 2006, 91: 4689-4695. 10.1210/jc.2006-0584.CrossRefPubMed Kankaanpaa M, Lehto HR, Parkka JP, Komu M, Viljanen A, Ferrannini E, Knuuti J, Nuutila P, Parkkola R, Iozzo P: Myocardial triglyceride content and epicardial fat mass in human obesity: relationship to left ventricular function and serum free fatty acid levels. J Clin Endocrinol Metab. 2006, 91: 4689-4695. 10.1210/jc.2006-0584.CrossRefPubMed
11.
go back to reference Szczepaniak LS, Dobbins RL, Metzger GJ, Sartoni-D'Ambrosia G, Arbique D, Vongpatanasin W, Unger R, Victor RG: Myocardial triglycerides and systolic function in humans: in vivo evaluation by localized proton spectroscopy and cardiac imaging. Magn Reson Med. 2003, 49: 417-423. 10.1002/mrm.10372.CrossRefPubMed Szczepaniak LS, Dobbins RL, Metzger GJ, Sartoni-D'Ambrosia G, Arbique D, Vongpatanasin W, Unger R, Victor RG: Myocardial triglycerides and systolic function in humans: in vivo evaluation by localized proton spectroscopy and cardiac imaging. Magn Reson Med. 2003, 49: 417-423. 10.1002/mrm.10372.CrossRefPubMed
12.
go back to reference van der Meer RW, Doornbos J, Kozerke S, Schar M, Bax JJ, Hammer S, Smit JW, Romijn JA, Diamant M, Rijzewijk LJ: Metabolic imaging of myocardial triglyceride content: reproducibility of 1H MR spectroscopy with respiratory navigator gating in volunteers. Radiology. 2007, 245: 251-257. 10.1148/radiol.2451061904.CrossRefPubMed van der Meer RW, Doornbos J, Kozerke S, Schar M, Bax JJ, Hammer S, Smit JW, Romijn JA, Diamant M, Rijzewijk LJ: Metabolic imaging of myocardial triglyceride content: reproducibility of 1H MR spectroscopy with respiratory navigator gating in volunteers. Radiology. 2007, 245: 251-257. 10.1148/radiol.2451061904.CrossRefPubMed
13.
go back to reference Gu K, Cowie CC, Harris MI: Mortality in adults with and without diabetes in a national cohort of the U.S. population, 1971-1993. Diabetes Care. 1998, 21: 1138-1145. 10.2337/diacare.21.7.1138.CrossRefPubMed Gu K, Cowie CC, Harris MI: Mortality in adults with and without diabetes in a national cohort of the U.S. population, 1971-1993. Diabetes Care. 1998, 21: 1138-1145. 10.2337/diacare.21.7.1138.CrossRefPubMed
14.
go back to reference Schrauwen-Hinderling VB, Hesselink MK, Meex R, van der Made S, Schar M, Lamb H, Wildberger JE, Glatz J, Snoep G, Kooi ME, Schrauwen P: Improved ejection fraction after exercise training in obesity is accompanied by reduced cardiac lipid content. J Clin Endocrinol Metab. 2010, 95: 1932-1938. 10.1210/jc.2009-2076.CrossRefPubMed Schrauwen-Hinderling VB, Hesselink MK, Meex R, van der Made S, Schar M, Lamb H, Wildberger JE, Glatz J, Snoep G, Kooi ME, Schrauwen P: Improved ejection fraction after exercise training in obesity is accompanied by reduced cardiac lipid content. J Clin Endocrinol Metab. 2010, 95: 1932-1938. 10.1210/jc.2009-2076.CrossRefPubMed
15.
go back to reference Buse JB, Ginsberg HN, Bakris GL, Clark NG, Costa F, Eckel R, Fonseca V, Gerstein HC, Grundy S, Nesto RW: Primary prevention of cardiovascular diseases in people with diabetes mellitus: a scientific statement from the American Heart Association and the American Diabetes Association. Diabetes Care. 2007, 30: 162-172. 10.2337/dc07-9917.CrossRefPubMed Buse JB, Ginsberg HN, Bakris GL, Clark NG, Costa F, Eckel R, Fonseca V, Gerstein HC, Grundy S, Nesto RW: Primary prevention of cardiovascular diseases in people with diabetes mellitus: a scientific statement from the American Heart Association and the American Diabetes Association. Diabetes Care. 2007, 30: 162-172. 10.2337/dc07-9917.CrossRefPubMed
16.
go back to reference Siri W: The gross composition of the body. Adv Biol Med Physiol. 1956, 4: 239-280.CrossRef Siri W: The gross composition of the body. Adv Biol Med Physiol. 1956, 4: 239-280.CrossRef
17.
go back to reference Vanhamme L, van den Boogaart A, Van Huffel S: Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson. 1997, 129: 35-43. 10.1006/jmre.1997.1244.CrossRefPubMed Vanhamme L, van den Boogaart A, Van Huffel S: Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson. 1997, 129: 35-43. 10.1006/jmre.1997.1244.CrossRefPubMed
18.
go back to reference Naressi A, Couturier C, Devos JM, Janssen M, Mangeat C, de Beer R, Graveron-Demilly D: Java-based graphical user interface for the MRUI quantitation package. Magma. 2001, 12: 141-152. 10.1007/BF02668096.CrossRefPubMed Naressi A, Couturier C, Devos JM, Janssen M, Mangeat C, de Beer R, Graveron-Demilly D: Java-based graphical user interface for the MRUI quantitation package. Magma. 2001, 12: 141-152. 10.1007/BF02668096.CrossRefPubMed
19.
go back to reference Colberg SR, Sigal RJ, Fernhall B, Regensteiner JG, Blissmer BJ, Rubin RR, Chasan-Taber L, Albright AL, Braun B: Exercise and type 2 diabetes: the American College of Sports Medicine and the American Diabetes Association: joint position statement executive summary. Diabetes Care. 2010, 33: 2692-2696. 10.2337/dc10-1548.PubMedCentralCrossRefPubMed Colberg SR, Sigal RJ, Fernhall B, Regensteiner JG, Blissmer BJ, Rubin RR, Chasan-Taber L, Albright AL, Braun B: Exercise and type 2 diabetes: the American College of Sports Medicine and the American Diabetes Association: joint position statement executive summary. Diabetes Care. 2010, 33: 2692-2696. 10.2337/dc10-1548.PubMedCentralCrossRefPubMed
20.
go back to reference Balducci S, Zanuso S, Nicolucci A, De Feo P, Cavallo S, Cardelli P, Fallucca S, Alessi E, Fallucca F, Pugliese G: Effect of an intensive exercise intervention strategy on modifiable cardiovascular risk factors in subjects with type 2 diabetes mellitus: a randomized controlled trial: the Italian Diabetes and Exercise Study (IDES). Arch Intern Med. 2010, 170: 1794-1803. 10.1001/archinternmed.2010.380.CrossRefPubMed Balducci S, Zanuso S, Nicolucci A, De Feo P, Cavallo S, Cardelli P, Fallucca S, Alessi E, Fallucca F, Pugliese G: Effect of an intensive exercise intervention strategy on modifiable cardiovascular risk factors in subjects with type 2 diabetes mellitus: a randomized controlled trial: the Italian Diabetes and Exercise Study (IDES). Arch Intern Med. 2010, 170: 1794-1803. 10.1001/archinternmed.2010.380.CrossRefPubMed
21.
go back to reference Monteiro LZ, Fiani CR, Freitas MC, Zanetti ML, Foss MC: Decrease in blood pressure, body mass index and glycemia after aerobic training in elderly women with type 2 diabetes. Arq Bras Cardiol. 2010, 95: 563-570. 10.1590/S0066-782X2010005000135.CrossRefPubMed Monteiro LZ, Fiani CR, Freitas MC, Zanetti ML, Foss MC: Decrease in blood pressure, body mass index and glycemia after aerobic training in elderly women with type 2 diabetes. Arq Bras Cardiol. 2010, 95: 563-570. 10.1590/S0066-782X2010005000135.CrossRefPubMed
22.
go back to reference Okada S, Hiuge A, Makino H, Nagumo A, Takaki H, Konishi H, Goto Y, Yoshimasa Y, Miyamoto Y: Effect of exercise intervention on endothelial function and incidence of cardiovascular disease in patients with type 2 diabetes. J Atheroscler Thromb. 2010, 17: 828-833.CrossRefPubMed Okada S, Hiuge A, Makino H, Nagumo A, Takaki H, Konishi H, Goto Y, Yoshimasa Y, Miyamoto Y: Effect of exercise intervention on endothelial function and incidence of cardiovascular disease in patients with type 2 diabetes. J Atheroscler Thromb. 2010, 17: 828-833.CrossRefPubMed
23.
go back to reference Leehey DJ, Moinuddin I, Bast JP, Qureshi S, Jelinek CS, Cooper C, Edwards LC, Smith BM, Collins EG: Aerobic exercise in obese diabetic patients with chronic kidney disease: a randomized and controlled pilot study. Cardiovasc Diabetol. 2009, 8: 62-10.1186/1475-2840-8-62.PubMedCentralCrossRefPubMed Leehey DJ, Moinuddin I, Bast JP, Qureshi S, Jelinek CS, Cooper C, Edwards LC, Smith BM, Collins EG: Aerobic exercise in obese diabetic patients with chronic kidney disease: a randomized and controlled pilot study. Cardiovasc Diabetol. 2009, 8: 62-10.1186/1475-2840-8-62.PubMedCentralCrossRefPubMed
24.
go back to reference Miche E, Herrmann G, Nowak M, Wirtz U, Tietz M, Hurst M, Zoller B, Radzewitz A: Effect of an exercise training program on endothelial dysfunction in diabetic and non-diabetic patients with severe chronic heart failure. Clin Res Cardiol. 2006, 95 (Suppl 1): i117-124.CrossRefPubMed Miche E, Herrmann G, Nowak M, Wirtz U, Tietz M, Hurst M, Zoller B, Radzewitz A: Effect of an exercise training program on endothelial dysfunction in diabetic and non-diabetic patients with severe chronic heart failure. Clin Res Cardiol. 2006, 95 (Suppl 1): i117-124.CrossRefPubMed
25.
go back to reference Loimaala A, Groundstroem K, Rinne M, Nenonen A, Huhtala H, Vuori I: Exercise training does not improve myocardial diastolic tissue velocities in Type 2 diabetes. Cardiovasc Ultrasound. 2007, 5: 32-10.1186/1476-7120-5-32.PubMedCentralCrossRefPubMed Loimaala A, Groundstroem K, Rinne M, Nenonen A, Huhtala H, Vuori I: Exercise training does not improve myocardial diastolic tissue velocities in Type 2 diabetes. Cardiovasc Ultrasound. 2007, 5: 32-10.1186/1476-7120-5-32.PubMedCentralCrossRefPubMed
26.
go back to reference Hordern MD, Coombes JS, Cooney LM, Jeffriess L, Prins JB, Marwick TH: Effects of exercise intervention on myocardial function in type 2 diabetes. Heart. 2009, 95: 1343-1349. 10.1136/hrt.2009.165571.CrossRefPubMed Hordern MD, Coombes JS, Cooney LM, Jeffriess L, Prins JB, Marwick TH: Effects of exercise intervention on myocardial function in type 2 diabetes. Heart. 2009, 95: 1343-1349. 10.1136/hrt.2009.165571.CrossRefPubMed
27.
go back to reference Loganathan R, Bilgen M, Al-Hafez B, Zhero SV, Alenezy MD, Smirnova IV: Exercise training improves cardiac performance in diabetes: in vivo demonstration with quantitative cine-MRI analyses. J Appl Physiol. 2007, 102: 665-672.CrossRefPubMed Loganathan R, Bilgen M, Al-Hafez B, Zhero SV, Alenezy MD, Smirnova IV: Exercise training improves cardiac performance in diabetes: in vivo demonstration with quantitative cine-MRI analyses. J Appl Physiol. 2007, 102: 665-672.CrossRefPubMed
28.
go back to reference Korte FS, Mokelke EA, Sturek M, McDonald KS: Exercise improves impaired ventricular function and alterations of cardiac myofibrillar proteins in diabetic dyslipidemic pigs. J Appl Physiol. 2005, 98: 461-467.CrossRefPubMed Korte FS, Mokelke EA, Sturek M, McDonald KS: Exercise improves impaired ventricular function and alterations of cardiac myofibrillar proteins in diabetic dyslipidemic pigs. J Appl Physiol. 2005, 98: 461-467.CrossRefPubMed
29.
go back to reference Zib I, Jacob AN, Lingvay I, Salinas K, McGavock JM, Raskin P, Szczepaniak LS: Effect of pioglitazone therapy on myocardial and hepatic steatosis in insulin-treated patients with type 2 diabetes. J Investig Med. 2007, 55: 230-236. 10.2310/6650.2007.00003.CrossRefPubMed Zib I, Jacob AN, Lingvay I, Salinas K, McGavock JM, Raskin P, Szczepaniak LS: Effect of pioglitazone therapy on myocardial and hepatic steatosis in insulin-treated patients with type 2 diabetes. J Investig Med. 2007, 55: 230-236. 10.2310/6650.2007.00003.CrossRefPubMed
30.
go back to reference van der Meer RW, Rijzewijk LJ, de Jong HW, Lamb HJ, Lubberink M, Romijn JA, Bax JJ, de Roos A, Kamp O, Paulus WJ: Pioglitazone improves cardiac function and alters myocardial substrate metabolism without affecting cardiac triglyceride accumulation and high-energy phosphate metabolism in patients with well-controlled type 2 diabetes mellitus. Circulation. 2009, 119: 2069-2077. 10.1161/CIRCULATIONAHA.108.803916.CrossRefPubMed van der Meer RW, Rijzewijk LJ, de Jong HW, Lamb HJ, Lubberink M, Romijn JA, Bax JJ, de Roos A, Kamp O, Paulus WJ: Pioglitazone improves cardiac function and alters myocardial substrate metabolism without affecting cardiac triglyceride accumulation and high-energy phosphate metabolism in patients with well-controlled type 2 diabetes mellitus. Circulation. 2009, 119: 2069-2077. 10.1161/CIRCULATIONAHA.108.803916.CrossRefPubMed
31.
go back to reference Bilet L, van de Weijer T, Hesselink MK, Glatz JF, Lamb HJ, Wildberger J, Kooi ME, Schrauwen P, Schrauwen-Hinderling VB: Exercise-induced modulation of cardiac lipid content in healthy lean young men. Basic Res Cardiol. 106: 307-315. Bilet L, van de Weijer T, Hesselink MK, Glatz JF, Lamb HJ, Wildberger J, Kooi ME, Schrauwen P, Schrauwen-Hinderling VB: Exercise-induced modulation of cardiac lipid content in healthy lean young men. Basic Res Cardiol. 106: 307-315.
32.
go back to reference Lahaye Sle D, Gratas-Delamarche A, Malarde L, Vincent S, Zguira MS, Morel SL, Delamarche P, Zouhal H, Carre F, Bekono FR: Intense exercise training induces adaptation in expression and responsiveness of cardiac beta-adrenoceptors in diabetic rats. Cardiovasc Diabetol. 2010, 9: 72-10.1186/1475-2840-9-72.CrossRefPubMed Lahaye Sle D, Gratas-Delamarche A, Malarde L, Vincent S, Zguira MS, Morel SL, Delamarche P, Zouhal H, Carre F, Bekono FR: Intense exercise training induces adaptation in expression and responsiveness of cardiac beta-adrenoceptors in diabetic rats. Cardiovasc Diabetol. 2010, 9: 72-10.1186/1475-2840-9-72.CrossRefPubMed
33.
go back to reference Kemi OJ, Ellingsen O, Smith GL, Wisloff U: Exercise-induced changes in calcium handling in left ventricular cardiomyocytes. Front Biosci. 2008, 13: 356-368. 10.2741/2685.CrossRefPubMed Kemi OJ, Ellingsen O, Smith GL, Wisloff U: Exercise-induced changes in calcium handling in left ventricular cardiomyocytes. Front Biosci. 2008, 13: 356-368. 10.2741/2685.CrossRefPubMed
Metadata
Title
Cardiac lipid content is unresponsive to a physical activity training intervention in type 2 diabetic patients, despite improved ejection fraction
Authors
Vera B Schrauwen-Hinderling
Ruth CR Meex
Matthijs KC Hesselink
Tineke van de Weijer
Tim Leiner
Michael Schär
Hildo J Lamb
Joachim E Wildberger
Jan FC Glatz
Patrick Schrauwen
M Eline Kooi
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2011
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/1475-2840-10-47

Other articles of this Issue 1/2011

Cardiovascular Diabetology 1/2011 Go to the issue