|Year : 2020 | Volume
| Issue : 6 | Page : 1234-1244
|Echocardiographic findings in children with chronic kidney disease
Bahia Moustafa1, Hanan Zekry2, Rania Hamdi Hashim3, Doaa Mohamed Salah1, Ahmed Abdelwahed Abdelfattah2, Rodina Sobhy2
1 Department of Pediatrics, Pediatric Nephrology Unit, Cairo, Egypt
2 Department of Pediatrics, Pediatric Cardiology Unit, Cairo University, Cairo, Egypt
3 Department of Radiology, Cairo University, Cairo, Egypt
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|Date of Web Publication||29-Jan-2021|
| Abstract|| |
Cardiovascular diseases (CVD) are considered major cause of morbidity and mortality among children with chronic kidney disease (CKD). This study aims to determine the incidence of CVD in children with CKD, to analyze risk factors and early predictors for late onset atherosclerosis. Thirty-five CKD children [25 on regular hemodialysis (HD) and 10 on conservative management] were evaluated clinically. Left ventricular (LV) functions and carotid artery intima-media thickness (c-IMT) were assessed using conventional echocardiography, pulsed wave Doppler (PWD) and tissue Doppler imaging (TDI). There was decreased E/A ratio and increased E/E' ratio in 66% and 77% of patients, respectively signifying diastolic cardiac dysfunction. There was a significant correlation between increased A' value (peak late diastolic annular velocity) and both increased serum cholesterol and anemia (P = 0.009, 0.004 respectively). Serum high density lipoprotein (HDL) significantly correlated negatively with inter-ventricular septal thickness and LV end-diastolic dimensions (P = 0.05, 0.02, respectively) and positively with E' value (peak early diastolic annular velocity) (P = 0.04). Abnormal c-IMT correlated significantly with HD duration (correlation coefficient = 0.428, P = 0.01) and with both increased serum cholesterol and decreased serum HDL (P = 0.021, 0.031, respectively). Diastolic dysfunction and abnormal LV dimensions are present in patients with CKD even those on conservative management. TDI appears to be more impressive than PWD in assessing early myocardial dysfunction. Increased c-IMT and dyslipidemia are prevalent in patients with CKD and more prevalent in patients on HD.
|How to cite this article:|
Moustafa B, Zekry H, Hashim RH, Salah DM, Abdelfattah AA, Sobhy R. Echocardiographic findings in children with chronic kidney disease. Saudi J Kidney Dis Transpl 2020;31:1234-44
|How to cite this URL:|
Moustafa B, Zekry H, Hashim RH, Salah DM, Abdelfattah AA, Sobhy R. Echocardiographic findings in children with chronic kidney disease. Saudi J Kidney Dis Transpl [serial online] 2020 [cited 2021 Mar 2];31:1234-44. Available from: https://www.sjkdt.org/text.asp?2020/31/6/1234/308332
| Introduction|| |
Cardiovascular disease (CVD) accounts for the majority of deaths in children with chronic kidney disease (CKD). Risk factors include: age, sex, diabetes, hypertension, obesity and factors specific for CKD such as blood pressure (BP) changes, fluid imbalance, anemia, calcium/phosphorus (Ca/P) metabolism, malnutrition, hypoalbuminemia hyperhomocysteinemia, inflammation, oxidant stress, insulin resistance, altered renin-angiotensin axis and endothelial dysfunction. Cardiovascular alterations begin even before the patient requires dialysis.
CKD promotes earlier development of atherosclerosis compared to healthy population. Slowing the progression of CKD and avoiding long-term dialysis by early transplantation may decrease the risk of premature CVD in children with CKD.
| Methods|| |
This is a cross-sectional cohort study performed on 35 children with CKD: 25 patients with end-stage renal disease (ESRD) on regular hemodialysis (HD) (Group 1: CKD5, glomerular filtration rate (GFR) between 10–15 mL/min/1.7 m2) and 10 patients on conservative management (Group 2). All included patients on conservative management had CKD stage 3 (GFR range between 35 and 45 mL/min/1.73 m2). Exclusion criteria included CKD associated with congenital or rheumatic heart disease, familial dyslipidemia and primary hyperparathyroidism. Study protocol was approved by our institutional Research and Ethical Committee and an informed written consent for inclusion in the study was signed by patients’ parents.
Patients were subjected to detailed history taking and clinical examination. BP was measured for all patients by a single operator on more than one occasion (during dialysis, follow-up visits to CKD clinic, and at Echo-cardiography sessions) with the mean readings recorded. BP percentiles were determined according to the Second Task Force on Blood Pressure Control in Children. Patients were categorized according to their mean BP readings at assessment into: (a) Patients with normal BP (systolic and diastolic BP <90th percentile for age, sex and height), (b) Patients with pre-hypertension/border line status (BP between 90th 95th percentile for age, sex and height without anti-hypertensive therapy), (c) Patients with controlled hypertension (HTN) (systolic and diastolic BP <95th percentile for age, sex and height on anti-hypertensive medications) and, (d) Patients with uncontrolled HTN (systolic or diastolic BP ≥95th percentile for age, sex and height with use of antihypertensive therapy).
Patient’s records were reviewed to analyze traditional and uremia related risk factors associated with increased incidence of cardiovascular morbidity and mortality of patients with CKD. Anemia indices [hemoglobin (HB), MCV, MCH], blood glucose, Ca/P product, lipid profile [cholesterol, total triglycerides, high-density lipoprotein (HDL), low-density lipoprotein (LDL)], serum albumin and C-reactive protein were documented. Dialysis efficiency was reviewed (number of sessions/ week, number of hours/ session and kt/v) in addition to the total duration of dialysis.
A transthoracic Echo-Doppler study was performed for all patients in supine or left lateral position using General Electric (GE, Vivid-5 system) with probe 3 or 5 MHz. The following parameters were assessed: a) conventional Echocardiography using the M-mode and two-dimensional echocardiography to assess the left ventricular (LV) systolic function [ejection fraction (EF) and fractional shor-tening (FS)] and the presence of LV hypertrophy (LVH) by evaluating the interventricular septum (IVS) thickness, LV end-systolic, LV end-diastolic (LVEDD) and LV posterior wall dimensions (LVPWD) and LV mass index (LVMI), b) pulsed wave and color Doppler to assess early diastolic inflow velocity (E), flow velocity during active atrial contraction (A), E/A ratio across the mitral valve to assess the LV diastolic function, (c) tissue Doppler imaging (TDI) to assess peak systolic annular velocity (S), peak early diastolic annular velocity (E’) and peak late diastolic annular velocity (A’) waves of the mitral valve as well as the ratio of early mitral inflow to peak early diastolic annular velocity (E/E’) to assess both the LV systolic and diastolic functions.
Carotid artery Doppler was performed by a single experienced vascular sonographer to detect any increase in carotid intima-media thickness (c-IMT) and arterial stiffness or calcification. Images were obtained using a General Electric machine (model: GE LOGIQ P6) with a 7.5–10 MHz linear-array transducer. Imaging was performed with the subject resting in the supine position, neck extended, and the head turned 45° toward the contralateral side. A cross section of the common carotid artery (CCA) was imaged to screen for any atheromatous plaques and then a longitudinal section of the CCA at the middle third was imaged with recording of the maximal c-IMT visualized. The intima-medial complex was defined as the border between the echo-lucent vessel lumen and the echogenic intima and the border between the echo-lucent media and echogenic adventitia.
Data were statistically described in terms of mean ± standard deviation (±SD), median and range, or frequencies and percentages, when appropriate. All statistical calculations were made using computer program Statistical Package for the Social Science (SPSS) version 15.0 for Microsoft Windows (SPSS Inc., Chicago, IL, USA). P <0.05 was considered significant.
| Results|| |
Group 1 (HD group) included 25 patients with age range of 5–16 year and male/female ratio of 2.57. Their mean height was 112 ± 13.35 cm with 92% of patients being <3rd percentile for age and sex. The mean weight was 23 ± 7.4 kg with 96% of patients being <3rd percentile for age and sex. Ninety-two percent of patients in this group reported cardio-vascular symptoms in the form of dyspnea, palpitation, syncope and effort intolerance.
Group 2 (conservative pre-dialytic management group) included 10 patients with age range of 5–15 years and male/female ratio of 1.5. Their mean height was 117 ± 20 cm with 70% of patients being <3rd percentile for age and sex. The mean weight was 19 ± 11.5 Kg with 60% of this group being <3rd percentile for age and sex. Twenty percent of this group reported cardiovascular symptoms. Kt/v of HD group ranged between 1 and 1.3 with a mean of 1.92 ±0.45.
In both groups, systolic BP ranged between 100 and 130 mm Hg with mean ± SD of 116 ± 10.8 mm Hg and diastolic BP ranged between 60 and 90 mm Hg with mean ± SD of 79.4 ± 14.3 mm Hg while mean BP ranged between 75 and 115 mm Hg. HTN was reported in 72% of Group 1 patients (controlled in 28% and uncontrolled in 44%), whereas in Group 2, 60% of patients had uncontrolled HTN [Figure 1].
Hypercholesterolemia, hypertriglyceridemia and decreased HDL were reported in 36%, 44% and 44%, respectively of patients in Group 1, compared to 20%, 10% and 20%, respectively in patients of Group 2.
Anemia was present in 72% of the HD group compared to 80% of conservative pre-dialytic group. Hypocalcaemia and hyperphosphatemia were found in 72% and 36%, respectively of patients in Group 1 compared to 70% and 5%, respectively of patients in Group 2. Levels of HB, Ca, Ph, Ca/Ph and lipid profile are illustrated in [Table 1].
M-mode echocardiography revealed LVH with increased IVS thickness in 56% and 30% of Group 1 and Group 2 patients, respectively, while LVMI was increased in 20% and 30% of Group 1 and Group 2 patients, respectively. LV dilatation was found in 32% and 20% of Group 1 and Group 2 patients, respectively [Figure 2].
|Figure 2: M-mode echocardiographic findings in both groups.|
IVSD: Interventricular septum diameter, LVPWD: Left ventricular posterior wall diameter, LVEDD: Left ventricular end diastolic diameter, LVESD: Left ventricular end systolic diameter, LVMI: Left ventricular mass index.
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E/A ratio was decreased in 64% of patients on HD and in 70% of patients on conservative management signifying diastolic dysfunction in both groups. Diastolic dysfunction was also reported using TDI, with higher incidence than that detected by pulsed wave Doppler (PWD) as E/E' ratio was increased in 80% of patients on HD and in 70% of patients on conservative management [Table 2].
|Table 2: Frequency distribution of myocardial impairment detected by indices of pulse wave Echocardiography and tissue Doppler imaging in both groups.|
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Significant negative correlation was detected between serum HDL and IVS thickness as well as with LVEDD. LV dimensions and LV systolic function were not significantly correlated to BP, HB, serum Ca, serum Ph, and the parameters of lipid profile [Table 3].
|Table 3: Correlation between echocardiographic parameters and laboratory findings in the study group.|
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As regards the diastolic function parameters, only the E wave velocity by PWD was found to be positively correlated to the serum HDL, while TDI parameters showed no significant correlation between increased E/E ratio and increased serum Ph, increased serum LDL or increased serum cholesterol. There was a significant correlation between increased A wave velocity and increased serum cholesterol. There was also significant correlation between increased A' wave velocity and anemia [Table 4].
|Table 4: Correlation between tissue Doppler parameter, blood pressure and laboratory findings in the study group.|
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Eleven patients (44%) within the HD group had increased c-IMT while all patients within conservative therapy group had normal c-IMT. The mean c-IMT of HD group was 0.06 (± 0.01), while that of conservative therapy group was 0.04 (± 0.001). Abnormal c-IMT was significantly correlated with HD duration (correlation coefficient = 0.428, P = 0.01) in addition to both increased serum cholesterol and decreased serum HDL (P = 0.021, 0.031 respectively). There was no significant correlation between abnormal c-IMT and either BP (P =0.319), serum Ca, serum P or C/P product (P = 0.09, 0.21, 0.37, respectively).
| Discussion|| |
Cardiac dysfunction and atherosclerosis are frequent in patients with CKD, contributing to the development of cardiovascular morbidity and mortality. The American Heart Association’s guidelines for cardiovascular risk reduction in high-risk pediatric patients stratified pediatric CKD patients in the highest risk category for developing CVD. This increased risk is attributed to both traditional and uremia-related risk factors. Recently, it became evident that cardiovascular risk factors are highly prevalent among children with early stages of CKD. Prevalence increases with disease progression to reach a peak in children on maintenance dialysis.
In this work, hypertension was found in 72% of patients on HD being uncontrolled in 44% and controlled in 28% reflecting role of dialysis in lowering blood pressure through removal of volume load and uremic toxins, whereas 60% of CKD pre-dialytic patients had uncontrolled HTN [Figure 1]. Similarly, many studies reported hypertension in 47–54% of patients with CKD and an even higher prevalence (52–74%) in patients on regular HD.,,,,,,,, Higher frequency for uncontrolled HTN reported in conservative group could be explained by small sample size (10 patients) and non-compliance to anti-hypertensive drugs and diuretics. In addition, volume over load in some patients with early stages of CKD (3 or 4) might indicate to put them on regular dialysis to control their refractory HTN
Although the weight of majority of our patients was below the third percentile for their age, hypercholesterolemia, hypertriglyceridemia and decreased HDL were detected in 36%, 44% and 44% of patients on HD, respectively, compared to 20%, 10% and 20%, respectively in patients with CKD on conservative management. This was similar to the results concluded by Saland et al and Wilson et al.,
Uremia-related risk factors for CVD that frequently present in children with CKD include: abnormal mineral metabolism, anemia and maintenance dialysis. Anemia in these children has been linked to the overall mortality.
Anemia, hypocalcemia and hyperphosphatemia were found in 72%, 72% and 36%, respectively of children on HD compared to 80%, 70% and 5% of conservative pre-dialytic group. This prevalence was higher than that reported by Chavers et al and by the United States Renal Data System in their multicenter analysis.,
Cardiac chamber changes in CKD remain an area of interest for research. It was previously demonstrated that LVH is increased in patients with CKD than normal population. Among our HD group, LVH parameters namely; increased IVSD thickness was found in 56% of patients, increased LVPWD thickness in 24% and increased LVMI in 20% of patients. In the conservative group, increased IVSD thickness was found in 30% of patients and 30% had increased LVMI [Figure 2]. Becker-Cohen et al reported a much lower prevalence of LVH (7%) most probably due to better control of BP, while Mitsnefes showed that even children with mild to moderate CKD (Stage 2–4 CKD) had high incidence of LVH (17–50%) while patients on dialysis had higher incidence of LVH (30%–92%).
Diastolic dysfunction is mainly detected by PWD echocardiography. It is indicated by decreased E and increased A, with a resultant decrease in the E/A ratio. However, these measurements are dependent on heart rate, sampling site, and cardiac loading conditions. In contrast, E’ (LV relaxation) by TDI was relatively independent of loading conditions and thus better marker for diastolic function.
PWD findings in this study revealed a decreased E/A ratio in 64% of patient on HD and in 70% of patients on conservative management signifying impaired myocardial relaxation and diastolic dysfunction in both groups of patients. Significant difference in E/A ratio between CKD patients compared with normal population was demonstrated by other studies as well., The higher frequency for diastolic dysfunction among 10 patients with CKD3 as compared to 35 patients with CKD5 on dialysis could be related to the small number of patients and higher incidence of uncontrolled HTN in the conservative group.
TDI showed an increased E/E ratio in 80 % of patients on HD and in 70% of patients on conservative management denoting an even higher incidence of diastolic dysfunction than that detected by conventional echocardiography and PWD [Table 2]. This is in agreement with other previous studies,, and thus, the use of TDI is highly recommended (E/E’) as a better predictor for diastolic dysfunction.
Although removal of excess cardiac load by HD could be an explanation to the higher prevalence of diastolic dysfunction (in terms of decreased E/A ratio detected by PWD) in the conservative management group in the current study. However, sensitivity of the technique used for myocardial assessment plays an important role. While only 64% of HD patients had diastolic dysfunction by PWD, 80% of the same group had diastolic dysfunction by TDI signifying the role of TDI in detection of early myocardial dysfunction and that patients with myocardial dysfunction may be missed to be diagnosed by conventional echocardio-graphy.
In our series, there was no significant correlation between HTN and LVH or with diastolic function parameters measured by conventional echocardiography and by TDI. This is concordant with the findings of Mencarelli et al and Kaidar et al, Although significant positive correlation between LVMI with SBP and DBP was evident in many publications,,,,,,, Sinha et al demonstrated a significant correlation between BP and indexed LVMI in their prospective study. This variation can be explained by the inability to detect masked HTN in many patients with normal clinic BP measurement by the ambulatory blood pressure measurement (ABPM) which was not used in our study unlike Sinha et al study, also due to the smaller number of patients.
The current study concluded that dyslipidemia was found to correlate with diastolic cardiac dysfunction as shown by; a significant positive correlation between serum HDL and E wave velocity in PWD, a significant positive correlation between the A’ wave velocity detected by TDI and serum cholesterol and a significant positive correlation between the E/E ratio and serum LDL and triglycerides. This was similar to the findings of Lindblad et al.
We found no significant correlation between anemia and LVMI; however, Hb status was negatively correlated with the A’ wave velocity (which is elevated in diastolic cardiac dysfunction). This was in concordance with the results of other studies demonstrating a correlation between anemia and diastolic dysfunction., Radoui et al, reported that chronic anemia was correlated with increased LVMI, although other studies did not.,
In this work, there was no significant correlation between serum Ca, P level and Ca × P product and either LVH or pulsed wave doppler parameters (E, A, E/A); however, there was significant correlation between increased serum P level and increased mitral E/E ratio detected by TDI which is more sensitive than conventional echocardiography.
Although symptomatic coronary artery disease is rarely diagnosed in children with CKD, atherosclerosis is already evident in children with advanced kidney disease.
Overall, c-IMT is impaired in CKD patients if compared to normal population., We found that 44% of patients in the HD group had increased c-IMT while all patients in the conservative group had normal c-IMT (P = 0.01). The same conclusion was reported by Litwin et al; who stated that c-IMT is significantly higher in the dialysis group than in the conservative group. Dyslipidemia, as well as vascular trauma (vascular access in HD) and the use of non-biocompatible filters causing leukocyte stimulation, platelet activation, endothelin and cytokine release are all major factors that increase the risk of vascular thrombosis during hemodialysis.
No significant correlation was found between HTN and increased c-IMT in the current work. In contrast, other studies, demonstrated that there is a significant positive correlation between HTN and increased c-IMT. This may be due to their larger number of patients, difference in patients’ ages, duration of sustained HTN which affects the vascular intima, and availability of ABPM allowing accurate and early detection of masked daytime HTN. We also found that c-IMT was significantly correlated with dialysis duration (correlation coefficient = 0.428, P = 0.01), while no significant correlation was noted between c-IMT and serum Ca level, serum P level, or Ca × P product. Other studies, demonstrated that abnormal Ca/P metabolism correlated with increased c-IMT and vascular dysfunction in pre-ESRD and ESRD patients with significant positive correlation of c-IMT with P level.,,
Increased c-IMT was significantly correlated with both increased serum cholesterol and decrease in serum HDL in our series. Similarly, Civilibal et al found significant positive correlation between c-IMT and total cholesterol, LDL cholesterol and triglyceride.
| Conclusion|| |
Both traditional and uremia-related risk factors for CVD are prevalent in children with CKD. Diastolic cardiac dysfunction and chamber abnormality are frequently present in patients with CKD even pre-dialysis. TDI appears to be more impressive than c-PWD in assessing early myocardial dysfunction. Dyslipidemia is correlated to LVH, diastolic cardiac dysfunction and increased c-IMT in children with CKD.
| Limitations|| |
The cross-sectional nature of the study was a limitation. The small number of patients and not using the ABPM were other limitations.
Conflict of interest: None declared.
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Department of Pediatrics, Pediatric Cardiology Unit, Cairo University, Cairo
[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3], [Table 4]
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