|Year : 2019 | Volume
| Issue : 2 | Page : 86-92
Evaluation of left ventricular diastolic and systolic function in children with type 1 diabetes mellitus using echocardiography and tissue Doppler imaging
Magdy A Ramadan, Mamdouh A Elghandour, Hani M Adel, Shaimaa A.M Oraby
Department of Pediatrics, Alexandria University, Alexandria, Egypt
|Date of Submission||17-Nov-2018|
|Date of Decision||06-Dec-2018|
|Date of Acceptance||06-Dec-2018|
|Date of Web Publication||6-Feb-2020|
MBBCh, MD Hani M Adel
Department of Pediatric, Faculty of Medicine, Alexandria University, Alexandria, 21411
Source of Support: None, Conflict of Interest: None
Background It has been shown that children with type 1 diabetes mellitus (T1DM) have high incidence of heart failure even in the absence of ischemic, hypertensive, or valvular heart disease. Most of these children have normal or even hyper-dynamic left ventricular (LV) systolic function at rest, whereas the diastolic function, particularly relaxation, is impaired. Tissue Doppler echocardiography measures myocardial motion and velocity, which provide a useful tool for defining subtle systolic and diastolic dysfunction.
Objective To assess the LV systolic and diastolic functions in children with type 1 diabetes mellitus attending the Alexandria University Children’s Hospital and its relation to the glycemic control and duration of the disease.
Patients and methods The study was conducted on 40 patients with T1DM who were followed up at the diabetes clinic of the Alexandria University Children’s Hospital and 20 apparently healthy control children of matched age and sex. Cardiac functions were assessed by conventional Doppler echocardiography and tissue Doppler imaging (TDI).
Results The results showed early cardiomyopathic changes in the form of diastolic dysfunction and impaired relaxation by studying the E/A ratio using conventional Doppler mitral flow in 7.5% of the diabetic children, whereas by using pulsed TDI, we found diastolic dysfunction of the septal or medial segment of the LV in 52.5%, and of the lateral segment in 42.2% of the diabetic patients. Moreover, the mean peak pulsed Doppler Am velocity was significantly higher in diabetic patients than in controls. There was a significant negative correlation between the duration of diabetes and E/A ratio. A significant negative correlation was found also between the LV diastolic dysfunction and the duration of the diabetes, whereas no significant correlation was found with the glycated hemoglobin% or age of the patients. The systolic function was normal in our diabetic patients.
Conclusion Our diabetic patients are in need of better glycemic control and periodic echocardiographic assessments, particularly by TDI to monitor the progression of subclinical ventricular dysfunction and to guard against the development of congestive heart failure.
Keywords: diastolic function, pulsed wave Doppler, tissue Doppler, type 1 diabetes mellitus
|How to cite this article:|
Ramadan MA, Elghandour MA, Adel HM, Oraby SA. Evaluation of left ventricular diastolic and systolic function in children with type 1 diabetes mellitus using echocardiography and tissue Doppler imaging. Alex J Pediatr 2019;32:86-92
|How to cite this URL:|
Ramadan MA, Elghandour MA, Adel HM, Oraby SA. Evaluation of left ventricular diastolic and systolic function in children with type 1 diabetes mellitus using echocardiography and tissue Doppler imaging. Alex J Pediatr [serial online] 2019 [cited 2020 Feb 21];32:86-92. Available from: http://www.ajp.eg.net/text.asp?2019/32/2/86/277837
| Introduction|| |
Children with type 1 diabetes mellitus (T1DM) have high incidence of heart failure owing to diabetic cardiomyopathy (DCM) . The term DCM describes the changes induced by DM in cardiac structure and functions in the absence of ischemic heart disease, hypertension, or other cardiac pathologies. DCM can be subclinical or apparent ,.
Diastolic dysfunction has been described as an early sign of DCM preceding the systolic damage and can occur in patients free of macrovascular complications. This reinforces the importance of early examination of ventricular function in individuals with diabetes . Most diabetic patients have normal or even hyper-dynamic left ventricular (LV) systolic function at rest .
Traditional echo-Doppler assessment of LV diastolic function relied on Doppler patterns of mitral inflow. Reflecting the pressure gradient between the left atrium and LV, transmitral velocities are directly related to left atrial pressure (preload) and independently and inversely related to ventricular relaxation. Because mitral inflow patterns are highly sensitive to preload and can change dramatically as diastolic dysfunction progresses, the use of mitral valve inflow patterns to assess diastolic function remains limited. Tissue Doppler imaging (TDI) assessment of diastolic function is less load dependent than that provided by standard Doppler techniques ,,, as shown in [Figure 1] and [Figure 2].
|Figure 1 Tissue Doppler signals from the lateral side of the mitral annulus .|
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|Figure 2 Recordings of velocity–time curves by pulsed tissue Doppler imaging from the basal septum and lateral wall, as indicated in the scheme of the apical four-chamber view measuring systolic (S′), early diastolic (E′), and atrial (A′) myocardial velocity. Global left ventricular function is calculated as the average of these regional segmental velocities. LA, left atrium; LV, left ventricle; RA, right atrium; RV, right ventricle .|
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There are only a few published studies on the LV function in Egyptian children with T1DM ,.
| Aim|| |
The present report presents the results of studying the LV function in children with T1DM attending the Alexandria University Children’s Hospital and its relation to the glycemic control and duration of the disease.
| Patients and methods|| |
The present cross-sectional study comprised two groups:
- Group 1 (patient group) included 40 children and adolescents with T1DM, chosen randomly from those attending the diabetic clinic of the Alexandria University Children’s Hospital from January to September 2012. The inclusion criteria were DM of more than or equal to 5-year duration, absence of symptoms or signs of systolic or diastolic heart failure, and absence of systemic hypertension. Children on any medication (other than insulin) known to affect the cardiac function, for example, digitalis, angiotensin-converting enzyme inhibitors, or B-blockers, were excluded.
- Group 2 (healthy control group) included 20 apparently healthy children of matching age and sex who had no evidence of cardiovascular disease by history, physical examination, and echocardiography.
The study population was subjected to detailed history and clinical examination. The last results of glycosylated hemoglobin (HbAlc) of the diabetic patients were obtained from the files, to reflect the glycemic control.
Echocardiographic and Doppler studies
Echocardiographic and Doppler examinations of the patients and controls were performed using Kontron Maestro image machine with 1–5-MHz phased array imaging transducer, with pulsed and continuous wave Doppler and color flow imaging capabilities. All patients were examined in the supine and left lateral recumbent position. For two-dimensional (2D) echocardiography, the patients were examined using the parasternal long axis and apical views.
M-mode recordings were made while the cardiac anatomy was visualized with 2D echocardiography from the parasternal view, with ECG monitoring the cardiac cycle. All the measurements of the ventricular parameters were recorded using the leading edge technique and following the recommendations of the American Society of Echocardiography , where each dimension was measured at both end diastolic coinciding with the ‘R’ wave and end systolic at the smallest systolic dimension .
The following measurements were obtained from the M-mode guided pictures in the parasternal short-axis view:
- LV internal dimensions, both at end diastole and systole (LVIDd and LVIDs) or left ventricular end diastolic dimension (LVEDd) and LV end systolic dimension (LVESd).
- Thickness of interventricular septal wall at end of diastole (IVSd) and interventricular septal wall at end of systole (IVSs).
- Thickness of left ventricular wall at end diastole (PWTd) and at end of systole (PWTS) all measured in mm.
- Percent fractional shortening: FS%=LVIDd–LVIDs/LVIDd .
- Left ventricular end systolic and end diastolic volumes, using Teichholz formula .
- Where EDV=end diastolic volume, ESV=end systolic volume , LVID=left ventricular internal dimension in diastole at peak Q wave, and LVIDs=left ventricular smallest internal dimension in systole.
- Ejection fraction was measured from M-Mode echo, based on Teichholz formula volume determination. EF=EDV-ESV/EDV, where EDV=end diastolic volume and ESV=end systolic volume
Conventional Doppler echocardiographic measurements
The peak early mitral filling velocity (E), peak mitral atrial velocity during late diastole (A), and their ratio (A/E) were used as LV diastolic function indices. The mitral diastolic flow tracing was imaged in the apical four-chamber view by using pulsed Doppler echocardiography with sample volume sited at the tips of mitral leaflets. Measurements were taken according to the current standards of the practice of echocardiography.
Tissue Doppler imaging measurements
The same ultrasound machine was used to obtain color tissue Doppler data using a high-frequency acquisition. The imaging angle was adjusted to ensure a parallel alignment of the beam with the myocardial segment of interest. From standard four-chamber and two-chamber views, resting tissue Doppler velocities within a 5×10-mm2 sample volume were derived for the basal segment of the medial (septal) and lateral wall of LV. Myocardial peak systolic (Sm), early diastolic filling (Em), and late diastolic atrial filling (Am) velocities were measured offline using customized software (Echopac TDI, Kontron Maestro, Kontron Medical Zone du Bel Air, 10, rue de Temara - CS 30342 SAINT GERMAIN EN LAYE CEDEX, FR 78105) and averaged for each.
Written informed parental consent was obtained for every patient and control. The study was approved by the Ethics Committee of the Faculty of Medicine, Alexandria University.
Data were fed to the computer using IBM SPSS software package, version 20.0. Qualitative data were described using number and percentage and were compared using χ2 or Fisher exact test. Quantitative data were expressed in mean±SD and range (minimum–maximum) and compared using the Student t test or Mann–Whitney test.
| Results|| |
The results are presented in [Table 1],[Table 2],[Table 3]. There was no significant difference between patients and controls regarding age, sex, or weight. The mean age of the patients was 11.3±3.1 years (6–18 years). The mean duration of diabetes was 7±2.25 years (5–13 years). The mean HbA1c% was 9.8±2.46% (5–14%).
|Table 1 Comparison between the data of diabetic patients and healthy controls|
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|Table 2 Comparison of echo-Doppler data of diabetic patients and healthy controls|
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|Table 3 Distribution of the studied patients according to E/A ratio by Doppler and pulsed tissue Doppler on mitral flow, lateral segment, and septal segment|
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The results showed early cardiomyopathic changes in the form of diastolic dysfunction and impaired relaxation, by studying the E/A ratio using conventional Doppler mitral flow, in 7.5% of the diabetic children, whereas by using pulsed tissue Doppler imaging (PTDI), we found diastolic dysfunction of the septal or medial segment of the LV in 52.5%, and of the lateral segment in 42.2% of the diabetic patients. Moreover, the mean peak pulsed Doppler Am velocity was significantly higher in diabetic patients than in controls. The study did not reveal any impairment in LV systolic function in the diabetic patients.
The mean values of LV posterior wall thickness at end systole and at end diastole were significantly higher in diabetic patients than in controls. Significant positive correlation was found between the duration of diabetes and both left ventricular end diastolic diameter (LVEDd) and end diastolic volume (EDV). Moreover, there was a significant negative correlation between the duration of diabetes and E/A ratio. Moreover, there was a significant negative correlation between left ventricular posterior wall thicknes in diastole (LVPWTd) and conventional mitral flow Doppler E/A ratios.
There was no significant correlation between the HbA1c% and all echocardiographic conventional Doppler and pulsed tissue Doppler parameters.
| Discussion|| |
The present study was carried on children and adolescence with long duration of T1DM (≥5 years). The glycemic control in these patients was unsatisfactory, as the mean HbA1c (9.8±2.46%) was in the poor control zone.
The study showed that the posterior wall thickness at end diastole (PWTd) and posterior wall thickness at end systole (PWTs) were significantly higher in diabetic patients than in controls, whereas the interventricular septum at systole and diastole (IVSs, IVSd) was normal. These findings agree with those of Airaksinen et al. , who found that both the interventricular septum and posterior wall thickness increased significantly in diabetic patients. This increase in LV wall thickness could be owing to the action of insulin hormone, which stimulates the formation of protein from amino acid and leads to accumulation of protein within the cells . Moreover, it may be owing to the potential role of growth hormone. Patients with difficult to control diabetes often have increased growth hormone levels, and this could account for the increased collagen present in the LV wall of diabetic humans and animals .
Our diabetic patients had increased left ventricular end diastolic diameter (LVEDd) as compared to controls, but the difference did not reach statistical significance. We also found that the m-mode LVEDd was increased in the diabetic group in comparison with the control group. These findings disagree with the data of Shishehbor et al. , who found no significant differences in the 2D and M-mode echocardiographic measurements between diabetic patients and controls. This may be explained by the relatively large percentage of diabetic patients with diastolic dysfunction in our study (52.5–42.5%)
There were no significant differences in the mean peak pulse Doppler E velocity between the diabetic normal and groups, and this finding is in agreement with Doppler findings reported by Shishehbor et al., . In contrast, Salem et al.  found that the mean peak pulse Doppler A velocity was significantly higher in diabetic patients than in controls, denoting LV filling abnormalities with a greater dependence on the atrial contraction for ventricular filling.
Similarly, Elshahed et al.  and Schannwell et al.  proved the presence of diastolic dysfunction in Type 1 diabetic cohorts using PTDI, although the conventional Doppler failed to show any difference in E/A ratio between diabetic patients and normal participants. This finding is consistent with our observation that only tissue Doppler revealed significant differences in LV diastolic filling patterns in 52.5% of the patients, whereas conventional Doppler detected diastolic dysfunction in only 7.5% of the patients.
In the current study, a comparison between medial E (septal) and lateral wall of LV velocities assessed by PW-TDI to know which of them is more sensitive in the diagnosis of diastolic dysfunction, we found that the medial annulus provided better sensitivity and specificity. The septal or medial annulus velocity revealed diastolic dysfunction in 52.5% of the patients and was normal in 47.5%, whereas the lateral segment revealed that 42.5% of the patients had diastolic dysfunction. These findings are concordant with those of Piyush et al. , who showed that among 232 patients with T1DM assessed by tissue Doppler, LV diastolic dysfunction was found in 61% of the patients; moreover, the medial annulus provided sensitivity of 78%, specificity of 67%, and predictive value of 70%. Moreover, it was consistent with results of Ozdemir et al .
In current study, we did not find any impairment in LV systolic function in type 1 diabetic patients at rest, with either ejection fraction% or conventional or tissue Doppler echocardiography. In fact, tissue Doppler detects changes in specific and diseased regions, even when the function of other segments or entire chamber is still normal . Our results are consistent with those of Anderson et al.  and Fang et al. ,.
The present study showed a significant positive correlation between the duration of diabetes and LVEDd and EDV. Attali et al.  observed that LV diastolic dysfunction (LVDD) was present in patients who had diabetes of less than five years. We did not find a significant correlation between the HbA1c% and LV systolic or diastolic functions. On the contrary, Devereux et al . and Grandi et al.  showed that the extent and frequency of diastolic dysfunction was directly proportional to the HbAlc level, likely because of the accumulation of advanced glycation end products in the myocardium . Moreover, CaglarAcar et al.  found that impairment in LV diastolic functions is directly related to glycemic control, and the rate of DCM was higher in children with poor metabolic control. Our findings could be attributed to the high HbA1c% in most of our patients.
| Conclusion|| |
In conclusion, our patients with T1DM have impaired LV diastolic function and normal systolic dysfunction when assessed with either conventional or PTDI. LV diastolic dysfunction was related to the duration of diabetes but not to the glycemic control. Our diabetic patients are in need of better glycemic control and periodic echocardiographic assessment, particularly by PW-TDI to monitor the progression of subclinical ventricular dysfunction and to guard against the development of congestive heart failure.
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Conflicts of interest
There are no conflicts of interest.
| References|| |
Craig ME, Hattersley A, Donaghue KC. Definition, epidemiology and classification of diabetes in children and adolescents. Pediatr Diabetes 2009; 10:3–12.
Zarich SW, Nesto RW. Diabetic cardiomyopathy. Am Heart J 1989; 118:1000–1012.
Regan TJ, Weisse AB. Diabetic cardiomyopathy. J Am Coll Cardiol 1992; 19:1165–1166.
Zarich SW, Nesto RW. Diabetic cardiomyopathy. Am Heart J 2001; 35:166–168.
Shehadeh A, Regan TJ. Cardiac consequences of diabetes mellitus. Clin Cardiol 1995; 18:301–305.
Alam M, Wardell J, Andersson E, Samad BA, Nordlander R. Characteristics of mitral and tricuspid annular velocities determined by pulsed wave Doppler tissue imaging in healthy subjects. J Am Soc Echocardiogr 1999; 12:618–629.
Oki T, Tabata T, Yamada H, Wakatsuki T, Shinohara H, Nishikado A et al.
Clinical application of pulsed Doppler tissue imaging for assessing abnormal left ventricular relaxation. Am J Cardiol 1997; 79:921–928.
Sohn DW, Kim YJ, Kim HC, Chun HG, Park YB, Choi YS. Evaluation of left ventricular diastolic function when mitral E and A waves are completely fused: role of assessing mitral annulus velocity. J Am Soc Echocardiogr 1999 12:203–208.
Salem M, El Behery S, Adlya A, Khalil D, El Hadidi E. Early predictors of myocardial disease in children and adolescents with type 1 diabetes mellitus. Pediatr Diabetes 2009; 10:513–521.
Elshahed GS, Ahmed MI, EL-Beblawy NS, Kamal HM, Ismaiel MF, Zheidan OA. Evaluation of right and left ventricular systolic and diastolic function in patients with type 1 diabetes using echocardiography and tissue Doppler imaging, Suez Canal Univ J 2008; 11:65–74.
Schiller NB. Two-dimensional eehocardiogiaphic determination of left ventricular volume, systolic function and mass. Summary and discussion of the 1989 recommendations of the American Society of Echocardiogiaphy. Circulation 1991; 83(3 Suppl):1280–1287.
Sahn D, DeNaria A, Kisslo J, Weyman A. Recommendations regarding quantitation in M-modc echocardiography: results of a survey of echocardiographic measurements. Circulation 1995; 57:1072–1083.
Feigenbaum H. Echocardiography. 6th ed. Philadelphia: William and Thomas 2005.
Airaksinen J, Ikaheimo M, Kaila J, Linnaluoto M, Takkunen J. Impaired LV filling in young female diabetics. An echocardiographicstudy. Acta Med Scand 1984;216:509–516.
Ramsay I, Bayliss R. Disorders of carbohydrate metabolism. In: Asynopsis of Endocrinology and Metabolism. Bristol: JWArrowsmith Ltd; 1986;153–175.
Ramadaham S, Rodriguez B, McNcill JH. Growth hormone and diabetes-induced cardiomyopathy. J Lab Clin Med 1984;110–257
Shishehbor MH, Hoogwerf BJ, Schoenhagen P, Marso SP, Sun JP, Li J et al.
Relation of hemoglobin A1c to left ventricular diastolic function in patients with type 1 diabetes mellitus and without overt heart disease. Am J Cardiol 2003; 91:1514–1517.
Schannwell CM, Sehoebel FC, Heggen S, Marx R, Perings C, Jackson CV et al.
Early deacrease in diastolic function in young type1 diabetic patients as an initial manifestation of diabetic cardiomyopathy. ZKardiol 1999; 88:338–346.
Piyush M, Louise M, Paul C. Latralvs medial mitral annular tissue Doppler in the echocardiographic assessment of diastolic function and filling pressure: which should we use?. Eur J Echocardiogr 2005; 6:97–106.
Ozdemir O, Koksoy AY, Bulus AD, Andiran N, Yagli E. The effects of type 1 diabetes mellitus on cardiac functions in children: evaluation by conventional and tissue Doppler echocardiography. J Pediatr Endocrinol Metab 2016; 29:1389–1395.
Anderson NH, Poulsen SH, Eiskjaer H, Poulsen PL, Mogensen CE. Decreased left ventricular longitudinal contraction in normotensive and normoalbuminuric patients with type 1 diabetes mellitus: a Doppler tissue tracking and strain rate echocardiography study. Clin Sci (London) 2003; 105:59–66.
Fang ZY, Schull-Meade R, Downey M. Determination of subclinical diabetic heart disease. Diabetologia 2005; 48:394–402.
Fang ZY, Yuda S, Anderson XX, Short L, Case C, Marwick TH. Echocardiographic detection of early diabetic myocardial disease. J Am Coll Cardiol 2003; 41:611–617.
Attali J, Sachs RN, Valnsi P, Larson MG, Benjanim EJ, Evans JC et al.
Asypmptomatic diabetic cardiomyopathy : a non invasive study. Diabetes Res Clin Pract 1988; 76:328–331.
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; 101:2271–2276.
Grandi AM, Piantanida E, Franzetti I, Bernasconi M, Maresca A, Marnini P et al.
Effect of glycemic control on the left ventricular diastolic function in type 1 diabetes mellitus. Am J Cardiol 2006; 97:17–76.
Candido R, Forbes JM, Thomas MC, Thallas V, Dean RD, Burns WC et al.
A breaker of advanced glycation end products attenuates diabetes-induced myocardial structural changes. Circ Res 2003; 92:785–792.
CaglarAcar O, Epcacan S, Uner A, Ece I, Dogan M. Evaluation of left andright ventricular functionsusing conventionaland tissue Doppler-echocardiography in children with type 1 diabetes mellitus. J Pediatr Endocrinol Metab 2016; 29:885–891.
[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3]