Skip to main content
Top
Published in: BMC Cardiovascular Disorders 1/2016

Open Access 01-12-2016 | Research article

Silent diabetic cardiomyopathy in everyday practice: a clinical and echocardiographic study

Authors: Brane Loncarevic, Danijela Trifunovic, Ivan Soldatovic, Bosiljka Vujisic-Tesic

Published in: BMC Cardiovascular Disorders | Issue 1/2016

Login to get access

Abstract

Background

Whether type 2 diabetes mellitus (DM) in the absence of hypertension (HTA) and coronary artery disease (CAD) affects left ventricular (LV) phenotype and function among asymptomatic DM patients that can be easily discovered in everyday practice, what is the clinical risk profile for diabetic cardiomyopathy and how HTA and CAD modulate LV structure and function above diabetic cardiomyopathy, are still incompletely answered questions.

Methods

In 210 DM patients (group I: 70 asymptomatic DM patients without HTA and CAD; group II: 70 DM patients with HTA and no CAD; group III: 70 DM patients with CAD and no HTA) and 80 healthy individuals, comprehensive echocardiography including speckle tracking strain and strain rate analysis, was done.

Results

Compared to control DM patients without HTA and CAD had increased LV mass, more frequently concentric remodeling, impaired LV relaxation and lower LV ejection fraction (EF), fraction of shortening (FS) and mitral annular plane excursion (MAPSE). Addition of HTA further impaired EF, FS and MAPSE and aggravated diastolic dysfunction, whereas concomitant CAD further impaired FS and MAPSE. Peak global longitudinal strain (Slong) and early diastolic longitudinal strain rate (SRlong E) were impaired in group I compared to control, even when EF was preserved. Peak circumferential strain (Scirc) was impaired only when DM was associated with HTA or CAD. In multivariate analysis DM was significantly and independently from HTA, CAD, age, gender and body mass index associated with: increased LV mass, concentric LV remodeling, lower EF, FS, MAPSE, Slong, SRlongE and distorted diastolic parameters. DM duration, glycosylated hemoglobin, microalbuminuria and retinopathy, were not independent predictors of LV geometry and function.

Conclusion

DM per se has strong and independent influence on LV phenotype and function that can be detected by conventional and speckle tracking echocardiography in everyday clinical practice, even in asymptomatic patients. We could not confirm that these changes were independently related to duration of DM, quality of metabolic control and presence of microvascular complications. Concomitant HTA or CAD furthermore distorted LV systolic and diastolic function.
Literature
1.
go back to reference Kannel WB, McGee DL. Diabetes and cardiovascular risk factors: the Framingham study. Circulation. 1979;59:8–13.CrossRefPubMed Kannel WB, McGee DL. Diabetes and cardiovascular risk factors: the Framingham study. Circulation. 1979;59:8–13.CrossRefPubMed
2.
go back to reference Kengne AP, Turnbul F, MacMAhon S. The Framingham Study, Diabetes Mellitus and Cardiovascular Disease: turning back the clock. Prog Cardiovasc Dis. 2010;53:45–51.CrossRefPubMed Kengne AP, Turnbul F, MacMAhon S. The Framingham Study, Diabetes Mellitus and Cardiovascular Disease: turning back the clock. Prog Cardiovasc Dis. 2010;53:45–51.CrossRefPubMed
3.
go back to reference Fox CS, Sullivan L, D Agostino RB, Wilsom PF. The significant effect of diabetes duration on coronary heart disease mortality. The Framingham Heart Study. Diabetes Care. 2004;27:3704–8.CrossRef Fox CS, Sullivan L, D Agostino RB, Wilsom PF. The significant effect of diabetes duration on coronary heart disease mortality. The Framingham Heart Study. Diabetes Care. 2004;27:3704–8.CrossRef
4.
go back to reference Voulgari C, Papadogiannis D, Tentolouris N. Diabetic cardiomyopathy: from the pathophysiology of the cardiac myocytes to current diagnosis and management strategies. Vasc Health Risk Manag. 2010;6:883–903.CrossRefPubMedPubMedCentral Voulgari C, Papadogiannis D, Tentolouris N. Diabetic cardiomyopathy: from the pathophysiology of the cardiac myocytes to current diagnosis and management strategies. Vasc Health Risk Manag. 2010;6:883–903.CrossRefPubMedPubMedCentral
5.
go back to reference Kandula V, Kosuru R, Li H, Yan D, Zhu Q, Lian Q, Ge R, Xia Z, Irwin MG. Forkhead box transcription factor 1: role in the pathogenesis of diabetic cardiomyopathy. Cardiovasc Diabetol. 2016;15:44.CrossRefPubMedPubMedCentral Kandula V, Kosuru R, Li H, Yan D, Zhu Q, Lian Q, Ge R, Xia Z, Irwin MG. Forkhead box transcription factor 1: role in the pathogenesis of diabetic cardiomyopathy. Cardiovasc Diabetol. 2016;15:44.CrossRefPubMedPubMedCentral
7.
go back to reference Rubler S, Dlugash J, Yuceoglu YZ, Kumral T, Branwood AW, Grishman A. New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am J Cardiol. 1972;30:595–602.CrossRefPubMed Rubler S, Dlugash J, Yuceoglu YZ, Kumral T, Branwood AW, Grishman A. New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am J Cardiol. 1972;30:595–602.CrossRefPubMed
9.
10.
go back to reference Ernande L, Derumeaux G. Diabetic cardiomyopathy: myth or reality? Arch Cardiovasc Dis. 2012;105:218–25.CrossRefPubMed Ernande L, Derumeaux G. Diabetic cardiomyopathy: myth or reality? Arch Cardiovasc Dis. 2012;105:218–25.CrossRefPubMed
11.
go back to reference Miki T, Yuda S, Kouzu H, Miura T. Diabetic cardiomyopathy: pathophysiology and clinical features. Heart Fail Rev. 2013;18:149–66.CrossRefPubMed Miki T, Yuda S, Kouzu H, Miura T. Diabetic cardiomyopathy: pathophysiology and clinical features. Heart Fail Rev. 2013;18:149–66.CrossRefPubMed
12.
go back to reference Seferović PM, Paulus WJ. Clinical diabetic cardiomyopathy: a two-faced disease with restrictive and dilated phenotypes. Eur Heart J. 2015;36:1718–27.CrossRefPubMed Seferović PM, Paulus WJ. Clinical diabetic cardiomyopathy: a two-faced disease with restrictive and dilated phenotypes. Eur Heart J. 2015;36:1718–27.CrossRefPubMed
13.
go back to reference Mochizuki Y, Tanaka H, Matsumoto K, Sano H, Toki H, Shimoura H, et al. Clinical features of subclinical left ventricular systolic dysfunction in patients with diabetes mellitus. Cardiovasc Diabetol. 2015;14:37.CrossRefPubMedPubMedCentral Mochizuki Y, Tanaka H, Matsumoto K, Sano H, Toki H, Shimoura H, et al. Clinical features of subclinical left ventricular systolic dysfunction in patients with diabetes mellitus. Cardiovasc Diabetol. 2015;14:37.CrossRefPubMedPubMedCentral
14.
go back to reference Geyer H, Caracciolo G, Abe H, Wilansky S, Carerj S, Gentile F, et al. Assessment of myocardial mechanics using speckle tracking echocardiography: fundamentals and clinical applications. J Am Soc Echocardiogr. 2010;23:351–69.CrossRefPubMed Geyer H, Caracciolo G, Abe H, Wilansky S, Carerj S, Gentile F, et al. Assessment of myocardial mechanics using speckle tracking echocardiography: fundamentals and clinical applications. J Am Soc Echocardiogr. 2010;23:351–69.CrossRefPubMed
15.
go back to reference Voigt JU, Pedrizzetti G, Lysyansky P, Marwick TH, Houle H, Baumann R, et al. Definitions for a common standard for 2D speckle tracking echocardiography: consensus document of the EACVI/ASE/Industry Task Force to standardized formation imaging. Eur Heart J Cardiovasc Imaging. 2015;16:1–11.CrossRefPubMed Voigt JU, Pedrizzetti G, Lysyansky P, Marwick TH, Houle H, Baumann R, et al. Definitions for a common standard for 2D speckle tracking echocardiography: consensus document of the EACVI/ASE/Industry Task Force to standardized formation imaging. Eur Heart J Cardiovasc Imaging. 2015;16:1–11.CrossRefPubMed
16.
go back to reference Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L, et al. Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. 2015;28:1–39.CrossRefPubMed Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L, et al. Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. 2015;28:1–39.CrossRefPubMed
17.
go back to reference Nagueh SF, Smiseth OA, Appleton CP, Byrd BF, Dokainish H, Edvardsen T, et al. Recommendations for the Evaluation of Left Ventricular Diastolic Function by Echocardiography: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. 2016;29:277–314.CrossRefPubMed Nagueh SF, Smiseth OA, Appleton CP, Byrd BF, Dokainish H, Edvardsen T, et al. Recommendations for the Evaluation of Left Ventricular Diastolic Function by Echocardiography: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. 2016;29:277–314.CrossRefPubMed
18.
go back to reference Emilsson K, Wandt B. The relation between mitral annulus motion and ejection fraction changes with age and heart size. Clin Physiol. 2000;20:38–43.CrossRefPubMed Emilsson K, Wandt B. The relation between mitral annulus motion and ejection fraction changes with age and heart size. Clin Physiol. 2000;20:38–43.CrossRefPubMed
19.
go back to reference Karatzis EN, Giannakopoulou AT, Papadakis JE, Karazachos AV, Nearchou NS. Myocardial performance index (Tei index): evaluating its application to myocardial infarction. Hellenic J Cardiol. 2009;50:60–5.PubMed Karatzis EN, Giannakopoulou AT, Papadakis JE, Karazachos AV, Nearchou NS. Myocardial performance index (Tei index): evaluating its application to myocardial infarction. Hellenic J Cardiol. 2009;50:60–5.PubMed
20.
go back to reference Santra S, Basu AK, Roychowdhury P, Banerjee R, Singhania P, Singh S, Datta UK. Comparison of left ventricular mass in normotensive type 2 diabetes mellitus patients with that in the nondiabetic population. J Cardiovasc Dis Res. 2011;2:50–6.CrossRefPubMedPubMedCentral Santra S, Basu AK, Roychowdhury P, Banerjee R, Singhania P, Singh S, Datta UK. Comparison of left ventricular mass in normotensive type 2 diabetes mellitus patients with that in the nondiabetic population. J Cardiovasc Dis Res. 2011;2:50–6.CrossRefPubMedPubMedCentral
21.
go back to reference Galderisi M, Anderson KM, Wilson PW, Levy D. Echocardiographic evidence for the existence of a distinct diabetic cardiomyopathy (the Framingham Heart Study). Am J Cardiol. 1991;68:85–9.CrossRefPubMed Galderisi M, Anderson KM, Wilson PW, Levy D. Echocardiographic evidence for the existence of a distinct diabetic cardiomyopathy (the Framingham Heart Study). Am J Cardiol. 1991;68:85–9.CrossRefPubMed
22.
go back to reference Lee M, Gardin JM, Lynch JC, Smith VE, Tracy RP, Savage PJ, et al. Diabetes mellitus and echocardiographic left ventricular function in free-living elderly men and women: the Cardiovascular Health Study. Am Heart J. 1997;133:36–43.CrossRefPubMed Lee M, Gardin JM, Lynch JC, Smith VE, Tracy RP, Savage PJ, et al. Diabetes mellitus and echocardiographic left ventricular function in free-living elderly men and women: the Cardiovascular Health Study. Am Heart J. 1997;133:36–43.CrossRefPubMed
23.
go back to reference Devereux RB, Roman MJ, Paranicas M, O’Grady MJ, Lee ET, Welty TK, et al. Impact of diabetes on cardiac structure and function: the strong heart study. Circulation. 2000;101:2271–6.CrossRefPubMed Devereux RB, Roman MJ, Paranicas M, O’Grady MJ, Lee ET, Welty TK, et al. Impact of diabetes on cardiac structure and function: the strong heart study. Circulation. 2000;101:2271–6.CrossRefPubMed
24.
go back to reference Atas H, Kepez A, Atas DB, Kanar BG, Dervisova R, Kivrak T, et al. Effects of diabetes mellitus on left atrial volume and functions in normotensive patients without symptomatic cardiovascular disease. J Diabetes Complications. 2014;28:858–62.CrossRefPubMed Atas H, Kepez A, Atas DB, Kanar BG, Dervisova R, Kivrak T, et al. Effects of diabetes mellitus on left atrial volume and functions in normotensive patients without symptomatic cardiovascular disease. J Diabetes Complications. 2014;28:858–62.CrossRefPubMed
25.
go back to reference Das SR, Drazner MH, Yancy CW, Stevenson LW, Gersh BJ, Dries DL. Effects of diabetes mellitus and ischemic heart disease on the progression from asymptomatic left ventricular dysfunction to symptomatic heart failure: a retrospective analysis from the Studies of Left Ventricular Dysfunction (SOLVD) Prevention trial. Am Heart J. 2004;148:883–8.CrossRefPubMed Das SR, Drazner MH, Yancy CW, Stevenson LW, Gersh BJ, Dries DL. Effects of diabetes mellitus and ischemic heart disease on the progression from asymptomatic left ventricular dysfunction to symptomatic heart failure: a retrospective analysis from the Studies of Left Ventricular Dysfunction (SOLVD) Prevention trial. Am Heart J. 2004;148:883–8.CrossRefPubMed
26.
go back to reference Ehl NF, Kühne M, Brinkert M, Müller-Brand J, Zellweger MJ. Diabetes reduces left ventricular ejection fraction-irrespective of presence and extent of coronary artery disease. Eur J Endocrinol. 2011;165:45–51.CrossRef Ehl NF, Kühne M, Brinkert M, Müller-Brand J, Zellweger MJ. Diabetes reduces left ventricular ejection fraction-irrespective of presence and extent of coronary artery disease. Eur J Endocrinol. 2011;165:45–51.CrossRef
27.
go back to reference Hu K, Liu D, Herrmann S, Niemann M, Gaudron PD, Voelker W, et al. Clinical implication of mitral annular plane systolic excursion for patients with cardiovascular disease. Eur Heart J Cardiovasc Imaging. 2013;14:205–12.CrossRefPubMed Hu K, Liu D, Herrmann S, Niemann M, Gaudron PD, Voelker W, et al. Clinical implication of mitral annular plane systolic excursion for patients with cardiovascular disease. Eur Heart J Cardiovasc Imaging. 2013;14:205–12.CrossRefPubMed
28.
go back to reference Zoroufian A, Razmi T, Taghavi-Shavazi M, Lotfi-Tokaldany M, Jalali A. Evaluation of subclinical left ventricular dysfunction in diabetic patients: longitudinal strain velocities and left ventricular dyssynchrony by two-dimensional speckle tracking echocardiography study. Echocardiography. 2014;31:456–63.CrossRefPubMed Zoroufian A, Razmi T, Taghavi-Shavazi M, Lotfi-Tokaldany M, Jalali A. Evaluation of subclinical left ventricular dysfunction in diabetic patients: longitudinal strain velocities and left ventricular dyssynchrony by two-dimensional speckle tracking echocardiography study. Echocardiography. 2014;31:456–63.CrossRefPubMed
29.
go back to reference Ernande L, Bergerot C, Girerd N, Thibault H, Davidsen ES, Gautier Pignon-Blanc P, et al. Longitudinal myocardial strain alteration is associated with left ventricular remodeling in asymptomatic patients with type 2 diabetes mellitus. J Am Soc Echocardiogr. 2014;27:479–88.CrossRefPubMed Ernande L, Bergerot C, Girerd N, Thibault H, Davidsen ES, Gautier Pignon-Blanc P, et al. Longitudinal myocardial strain alteration is associated with left ventricular remodeling in asymptomatic patients with type 2 diabetes mellitus. J Am Soc Echocardiogr. 2014;27:479–88.CrossRefPubMed
30.
go back to reference Nakai H, Takeuchi M, Nishikage T, Lang RM, Otsuji Y. Subclinical left ventricular dysfunction in asymptomatic diabetic patients assessed by two-dimensional speckle tracking echocardiography: correlation with diabetic duration. Eur J Echocardiogr. 2009;10:926–32.CrossRefPubMed Nakai H, Takeuchi M, Nishikage T, Lang RM, Otsuji Y. Subclinical left ventricular dysfunction in asymptomatic diabetic patients assessed by two-dimensional speckle tracking echocardiography: correlation with diabetic duration. Eur J Echocardiogr. 2009;10:926–32.CrossRefPubMed
31.
go back to reference Ng AC, Delgado V, Bertini M, van der Meer RW, Rijzewijk LJ, Shanks M, et al. Findings from left ventricular strain and strain rate imaging in asymptomatic patients with type 2 diabetes mellitus. Am J Cardiol. 2009;104:1398–401.CrossRefPubMed Ng AC, Delgado V, Bertini M, van der Meer RW, Rijzewijk LJ, Shanks M, et al. Findings from left ventricular strain and strain rate imaging in asymptomatic patients with type 2 diabetes mellitus. Am J Cardiol. 2009;104:1398–401.CrossRefPubMed
32.
go back to reference Hensel KO, Grimmer F, Jenke AC, Wirth S, Heusch A. The influence of real-time blood glucose levels on left ventricular myocardial strain and strain rate in pediatric patients with type 1 diabetes mellitus - a speckle tracking echocardiography study. BMC Cardiovasc Disord. 2015;15:175.CrossRefPubMedPubMedCentral Hensel KO, Grimmer F, Jenke AC, Wirth S, Heusch A. The influence of real-time blood glucose levels on left ventricular myocardial strain and strain rate in pediatric patients with type 1 diabetes mellitus - a speckle tracking echocardiography study. BMC Cardiovasc Disord. 2015;15:175.CrossRefPubMedPubMedCentral
33.
go back to reference Ernande L, Thibault H, Bergerot C, Moulin P, Wen H, Derumeaux G, Croisille P. Systolic myocardial dysfunction in patients with type 2 diabetes mellitus: identification at MR imaging with cine displacement encoding with stimulated echoes. Radiology. 2012;265:402–9.CrossRefPubMedPubMedCentral Ernande L, Thibault H, Bergerot C, Moulin P, Wen H, Derumeaux G, Croisille P. Systolic myocardial dysfunction in patients with type 2 diabetes mellitus: identification at MR imaging with cine displacement encoding with stimulated echoes. Radiology. 2012;265:402–9.CrossRefPubMedPubMedCentral
34.
go back to reference Cioffi G, Faganello G, De Feo S, Berlinghieri N, Tarantini L, Di Lenarda A, et al. Combined circumferential and longitudinal left ventricular systolic dysfunction in patients with type 2 diabetes mellitus without myocardial ischemia. Exp Clin Cardiol. 2013;18(1):e26–31.PubMedPubMedCentral Cioffi G, Faganello G, De Feo S, Berlinghieri N, Tarantini L, Di Lenarda A, et al. Combined circumferential and longitudinal left ventricular systolic dysfunction in patients with type 2 diabetes mellitus without myocardial ischemia. Exp Clin Cardiol. 2013;18(1):e26–31.PubMedPubMedCentral
35.
go back to reference Galderisi M. Diastolic dysfunction and diabetic cardiomyopathy: evaluation by Doppler echocardiography. J Am Coll Cardiol. 2006;48:1548–51.CrossRefPubMed Galderisi M. Diastolic dysfunction and diabetic cardiomyopathy: evaluation by Doppler echocardiography. J Am Coll Cardiol. 2006;48:1548–51.CrossRefPubMed
36.
go back to reference Ernande L, Bergerot C, Rietzschel ER, De Buyzere ML, Thibault H, Pignonblanc PG, et al. Diastolic dysfunction in patients with type 2 diabetes mellitus: is it really the first marker of diabetic cardiomyopathy? J Am Soc Echocardiogr. 2011;24:1268–75.CrossRefPubMed Ernande L, Bergerot C, Rietzschel ER, De Buyzere ML, Thibault H, Pignonblanc PG, et al. Diastolic dysfunction in patients with type 2 diabetes mellitus: is it really the first marker of diabetic cardiomyopathy? J Am Soc Echocardiogr. 2011;24:1268–75.CrossRefPubMed
37.
go back to reference From AM, Scott CG, Chen HH. The development of heart failure in patients with diabetes mellitus and pre-clinical diastolic dysfunction a population-based study. J Am Coll Cardiol. 2010;55:300–5.CrossRefPubMed From AM, Scott CG, Chen HH. The development of heart failure in patients with diabetes mellitus and pre-clinical diastolic dysfunction a population-based study. J Am Coll Cardiol. 2010;55:300–5.CrossRefPubMed
38.
go back to reference Poirier P, Bogaty P, Garneau C, Marois L, Dumesnil JG. Diastolic dysfunction in normotensive men with well-controlled type 2 diabetes: importance of maneuvers in echocardiographic screening for preclinical diabetic cardiomyopathy. Diabetes Care. 2001;24:5–10.CrossRefPubMed Poirier P, Bogaty P, Garneau C, Marois L, Dumesnil JG. Diastolic dysfunction in normotensive men with well-controlled type 2 diabetes: importance of maneuvers in echocardiographic screening for preclinical diabetic cardiomyopathy. Diabetes Care. 2001;24:5–10.CrossRefPubMed
39.
go back to reference Di Bonito P, Moio N, Cavuto L, Covino G, Murena E, Scilla C, et al. Early detection of diabetic cardiomyopathy: usefulness of tissue Doppler imaging. Diabet Med. 2005;22:1720–5.CrossRefPubMed Di Bonito P, Moio N, Cavuto L, Covino G, Murena E, Scilla C, et al. Early detection of diabetic cardiomyopathy: usefulness of tissue Doppler imaging. Diabet Med. 2005;22:1720–5.CrossRefPubMed
40.
go back to reference Patil VC, Patil HV, Shah KB, Vasani JD, Shetty P. Diastolic dysfunction in asymptomatic type 2 diabetes mellitus with normal systolic function. J Cardiovasc Dis Res. 2011;2:213–22.CrossRefPubMedPubMedCentral Patil VC, Patil HV, Shah KB, Vasani JD, Shetty P. Diastolic dysfunction in asymptomatic type 2 diabetes mellitus with normal systolic function. J Cardiovasc Dis Res. 2011;2:213–22.CrossRefPubMedPubMedCentral
41.
go back to reference Pattoneri P, Sozzi FB, Catellani E, Piazza A. Myocardial involvement during the early course of type 2 diabetes mellitus: usefulness of Myocardial Performance Index. Cardiovasc Ultrasound. 2008;6:27.CrossRefPubMedPubMedCentral Pattoneri P, Sozzi FB, Catellani E, Piazza A. Myocardial involvement during the early course of type 2 diabetes mellitus: usefulness of Myocardial Performance Index. Cardiovasc Ultrasound. 2008;6:27.CrossRefPubMedPubMedCentral
42.
go back to reference Chaudhary AK, Aneja GK, Shukla S, Razi SM. Study on diastolic dysfunction in newly diagnosed type 2 diabetes mellitus and its correlation with glycosylated haemoglobin (HbA1C). J Clin Diagn Res. 2015;9:OC20–2.PubMedPubMedCentral Chaudhary AK, Aneja GK, Shukla S, Razi SM. Study on diastolic dysfunction in newly diagnosed type 2 diabetes mellitus and its correlation with glycosylated haemoglobin (HbA1C). J Clin Diagn Res. 2015;9:OC20–2.PubMedPubMedCentral
Metadata
Title
Silent diabetic cardiomyopathy in everyday practice: a clinical and echocardiographic study
Authors
Brane Loncarevic
Danijela Trifunovic
Ivan Soldatovic
Bosiljka Vujisic-Tesic
Publication date
01-12-2016
Publisher
BioMed Central
Published in
BMC Cardiovascular Disorders / Issue 1/2016
Electronic ISSN: 1471-2261
DOI
https://doi.org/10.1186/s12872-016-0395-z

Other articles of this Issue 1/2016

BMC Cardiovascular Disorders 1/2016 Go to the issue