|Year : 2016 | Volume
| Issue : 6 | Page : 1114-1122
|Serum levels of N-terminal-pro B-type natriuretic peptide as a diagnostic marker for left ventricular dysfunction in children with end-stage renal disease on hemodialysis
Amr Mohamed Zoair1, Maher Ahmed Abdel-Hafez1, Wegdan Mawlana1, Mohamed Abdel-Rahman Sweylam2
1 Department of Pediatrics, Faculty of Medicine, Tanta University, Tanta, Egypt
2 Department of Clinical Pathology, Faculty of Medicine, Tanta University, Tanta, Egypt
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|Date of Web Publication||28-Nov-2016|
| Abstract|| |
The objective of this study was to determine the diagnostic cutoff value of N-terminal-pro B-type natriuretic peptide (NT-pro BNP) as a marker of left ventricular (LV) dysfunction in children with end-stage renal disease (ESRD) on regular hemodialysis (HD). The study was carried out on thirty children with ESRD on regular HD and thirty healthy controls. Echocardiographic studies were done, including a conventional mode for ejection fraction, fractional shortening, tissue Doppler imaging, and longitudinal global strain by speckle tracking. Serum levels of NT-pro BNP were measured in venous blood samples before and about 30 min after HD by ELISA. Volume status was assessed by calculating interdialytic weight gain %. There were significant higher serum NT-pro BNP levels before HD (mean: 702.3 ± 274.3 ng/L) compared to controls (mean: 365.55 ± 76.5 ng/L) (P <0.001) and these levels decreased significantly after the HD session (mean: 625.1 ± 117.69 ng/L) (P = 0.031). Echocardiographic studies showed a significant impairment of LV function of the patients compared to controls. Patients with LV dysfunction had significant higher serum concentrations of NT-pro BNP compared to patients without dysfunction both before (P = 0.003) and after dialysis (P <0.001). Receiver operating curve demonstrated better prediction of LV dysfunction by NT-pro BNP levels after HD compared to its levels before HD (area under the curve was 0.9 and 0.73, respectively). Using a cutoff value of 630 ng/L, serum NT-pro BNP levels after dialysis were a diagnostic predictor of LV dysfunction with a sensitivity of 86.6%, specificity of 93.3%, positive predictive value of 92.8%, and negative predictive value of 87.5%. Serum NT-pro BNP levels were strongly correlated with the parameters of LV dysfunction in children with ESRD on regular HD. A postdialysis cutoff value of 630 ng/L could serve as a biochemical marker of LV dysfunction in those children regardless of chronic fluid overload.
|How to cite this article:|
Zoair AM, Abdel-Hafez MA, Mawlana W, Sweylam MA. Serum levels of N-terminal-pro B-type natriuretic peptide as a diagnostic marker for left ventricular dysfunction in children with end-stage renal disease on hemodialysis. Saudi J Kidney Dis Transpl 2016;27:1114-22
|How to cite this URL:|
Zoair AM, Abdel-Hafez MA, Mawlana W, Sweylam MA. Serum levels of N-terminal-pro B-type natriuretic peptide as a diagnostic marker for left ventricular dysfunction in children with end-stage renal disease on hemodialysis. Saudi J Kidney Dis Transpl [serial online] 2016 [cited 2020 Apr 7];27:1114-22. Available from: http://www.sjkdt.org/text.asp?2016/27/6/1114/194593
| Introduction|| |
End-stage renal disease (ESRD) is the stage of chronic renal failure, in which life is impossible without renal replacement therapy. It is associated with a high risk of cardiovascular disease, which remains the leading cause of death in dialysis patients.  New echocardiographic modalities such as tissue Doppler imaging (TDI) and speckle tracking echocardiography (STE) can detect subclinical cardiac dysfunction earlier with the advantages of being less load dependent. 
B-type natriuretic peptide (BNP) is synthesized as prepro-BNP mainly in the ventricular myocardium. On ventricular myocyte stretch, prepro-BNP is enzymatically cleaved to pro BNP and released in the form of the hormonally active BNP and the inactive N-terminalpro BNP (NT-pro BNP). 
BNP is metabolized by natriuretic peptide receptors, which are mainly located in the liver, lung, kidney, and vascular endothelium, and degraded by plasma endopeptidases.  The amino terminal of pro BNP (NT-pro BNP) is predominantly cleared by the kidneys, and has a longer half-life than BNP (1-2 h vs. 20 min) leading to higher circulating levels and greater stability. NT-pro BNP levels show stronger correlation with an estimated glomerular filtration rate (eGFR) than the BNP. 
Measurements of both BNP and NT-pro BNP have an established role in screening of heart disease, diagnosis and stratification of patients with heart failure, detection of left ventricular (LV) systolic and/or diastolic dysfunction, and differential diagnosis of acute dyspnea.  A cutoff value of plasma NT-pro BNP for the diagnosis of heart failure in children without kidney diseases was studied and stratified according to the age groups.  However, in children with ESRD, their use is confounded by reduced renal excretion and concomitant chronic volume overload, and the cutoff values are expected to be different. The aim of this work was to evaluate the diagnostic value of NT-pro BNP as a marker of LV dysfunction in children with ESRD on regular hemodialysis (HD) and to correlate its levels with echocardiographic LV parameters of those children.
| Patients and Methods|| |
The present study was carried out at Pediatric Department, Tanta University Hospitals. The study was conducted as a prospective case- control analysis of thirty children with ESRD on regular HD. Their ages ranged from 5-16 years. Thirty ageand sex-matched healthy children were included as a control group. The study started from October 2013 to December 2014 with the approval of the Ethical Committee and Institutional Review Board at the Faculty of Medicine, Tanta University, Egypt. All the parents of the included children signed a written informed consent before enrollment into the study.
All patients were on regular HD three times per week, each dialysis session lasting for 3-4 h. Dialysis was started when the glomerular filtration rate was ≤15 mL/min/1.73 m 2 . Exclusion criteria were children with congenital cardiac anomalies, chromosomal anomalies, current infections, uncontrolled hypertension, severe anemia, and clinically evident heart failure.
Patients were dialyzed on Fresenius 4008-B dialysis machine (Germany) at a blood flow rate = 2.5 × weight (kg) + 100 mL/min, using polysulfone hollow fiber dialyzers suitable for the surface area of the patients (Fresenius F3 = 0.4 m 2 , F4 = 0.7 m 2 , F5 = 1.0 m 2 , and F6 = 1.2 m 2 ). Bicarbonate dialysis solutions were used (Na: 138 mEq/L, K: 2 mEq/L, Ca: 5 mg/dL, and bicarbonate: 32 mEq/L). The dialysate temperature was 36.5°C.
All patients and controls were subjected to detailed history taking, including duration of dialysis and regular drug taking, clinical examination including blood pressure and cardiac examination. Clinical and radiological measurements were taken on the dialysis-free day.
Arterial blood pressure was measured by the auscultatory method using a mercury sphygmomanometer with the patient in the semisitting position after 10 min of rest, in the non fistula arm using an appropriate-sized cuff. All measurements were performed twice and the means were used for analysis.
Interdialytic weight gain (IDWG) was calculated as percent from dry weight as follows:
Predialysis weight − Postdialysis weight (dry weight) × 100/postdialysis weight
Kt/V was used for the evaluation of dialysis adequacy.
Routine laboratory investigations were complete urine analysis, complete blood picture (complete blood cell), blood urea and serum creatinine, serum albumin, total serum cholesterol levels, serum electrolytes, serum Ca, phosphorous, C-reactive protein, and intact parathyroid hormone. These investigations were done as part of the routine laboratory work.
Echocardiographic studies were done using a commercially available ultrasound transducer and equipment (Vivid 7; GE Healthcare, Horten, Norway). Data acquisition was performed with a 3.5-MHz transducer. To avoid intraobserver variability, two examinations were done by the same operator who was blind for the volume status and the levels of NT-pro BNP.
Conventional echocardiography was conducted using M-mode and two-dimensional (2D) images to assess LV internal dimensions, ejection fraction (EF), and fractional shortening (FS). All children were examined in a semisupine, left lateral position. The LV diastolic functions were evaluated by the mitral inflow pattern obtained by pulsed-wave Doppler echocardiography. The mitral Doppler signals were recorded in the apical 4-chamber view, with the Doppler sample volume placed at the tip of the mitral valve. 
Pulsed wave TDI (PW-TDI) was performed using pulsed-wave angle-corrected color-coded TDI filters. The baseline was adjusted to a low-velocity range (-20 to 20 cm/s), and Doppler frame rates were varied between 80 and 115 frames/s depending on the sector width of the range of interest with minimal gain setting to minimize background noise and to obtain the highest quality images. The sample volume was placed within the myocardium equidistant from the endocardial and epicardial borders. From the apical 4-chamber planes, using PW-TDI, the myocardial velocity curves of the septal mitral valve annulus and lateral mitral valve annulus were recorded. The electrocardiogram was connected and traced simultaneously to define the timing of cardiac cycle events. The beginning of QRS complex was used as a reference point. The spectral TDI display showed an antegrade systolic (S) wave and two retrograde waves, E′ (passive LV filling), and A′ wave (atrial contraction). The S wave reflects the LV systolic function, and the E΄/A΄ ratio of the mitral valve annulus reflects the diastolic dysfunction of the LV.
For speckle tracking analysis of the left ventricle, standard gray scale 2D images were acquired in the 4-chamber view using a 3.5 MHz transducer at a depth of 16 cm with a stable electrocardiograph recording using acoustic tracking software (EchoPAC; allowing offline semi-automated analysis of speckle-based strain) to measure global systolic LV with the frame rates of 60-1000 frames/s. Particular attention was given to obtain a satisfactory gray scale image, allowing reliable delineation of myocardial tissue and extracardiac structures. Three consecutive heart cycles were recorded and averaged. To avoid intra-observer variability, two examinations were performed by the same operator.
LV systolic strain: for apical long-axis, 2and 4-chamber views, three sampling points were placed manually at septal mitral annulus, lateral corner, and apical endocardium. A region of interest (ROI) was then generated by the software to cover the myocardial thickness along the entire LV wall. The ROI was adjusted manually to ensure that the inner margin confirmed to the whole LV endocardial border and that it included the entire thickness of the LV myocardium. The software subsequently identified the tissue speckles and tracked their movement frame-by-frame throughout the cardiac cycle. The automated function imaging was used to measure segmental peak systolic strain in LV walls and global peak longitudinal systolic strain in the three standard apical views. The average LV global longitudinal systolic strain (LV GLSS) was calculated from the three individual apical GLSS curves. As the longitudinal strain analysis was performed in all the three apical views, the software automatically generated a topographic representation of all the 17 analyzed segments. The average LV GLSS was calculated by averaging the peak systolic values of the 17 segments, derived from the 6 segments of the 3 apical views. For myocardial strain, regional lengthening is expressed as a positive value (or blue) and shortening as a negative value (or red).
Patient group was further divided into ventricular dysfunction and nondysfunction groups. LV dysfunction was considered in this study if the patient has any of the following: EF <45%, FS <25%, E/E΄ >15, or global strain <15%. 
Blood samples were drawn from the vascular access just before and about 30 min after HDs for the measurement of NT-proBNP. After centrifugation, samples were stored at -70°C till the time of analysis. Serum NT-pro-BNP was analyzed using a commercial NT-proBNP ELISA kit (Biomedica, Vienna, Austria).
| Statistical Analysis|| |
Data were analyzed using Statistical Package for the Social Science (SPSS) software version 16, (SPSS Inc., Chicago, IL, USA). Data were expressed as the number and percentage for nonparametric variables and mean ± standard deviation for parametric variables. For comparison of means of two independent groups, unpaired Student's t-test was used. Paired Student's t-test was used to compare means of the same group (before and after dialysis). Pearson's bivariate correlation coefficient was used for analyzing the correlation between variables.
Receiver operating curve (ROC) characteristic was used to determine cutoff value of NT-pro BNP in diagnosing LV dysfunction. The upper left corner location of the curve indicates a good sensitivity and specificity of plasma NT-pro BNP level in diagnosing ventricular dysfunction. The area under the curve represents the overall accuracy of the NT-pro BNP measurements.
| Results|| |
The demographic, clinical, and laboratory data of the studied groups are shown in [Table 1]. There was no statistically significant difference between both groups regarding age (P >0.05). Female sex represented 60% of our patients and 56.6% of the control group. There was a statistically significant increase in heart rate, systolic and diastolic blood pressure in patients compared to the controls (P <0.05).
|Table 1: Demographic, clinical, and laboratory data of the studied groups.|
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Chronic glomerulonephritis represents the most common cause of ESRD (50%) followed by chronic pyelonephritis (16.6%). Obstructive uropathy and hypoplastic kidneys represent 13.3% for each and hereditary nephropathy represent 6.6%.
The duration of HD before the study ranged from twelve to 65 months with a median of 41.3 months. Serum albumin and Hb% were significantly lower while total serum cholesterol, blood urea, and CRP were significantly higher in patients compared to controls [Table 1]. Patients' mean weight before dialysis was 29.6 ± 5.34 kg and after HD it was 28.65 ± 5.4 with mean IDWG% of 3.5 ± 1.72.
Echocardiographic study showed significant impairment of the cardiac functions of patients by conventional echo, tissue Doppler, and global strain by speckle tracking compared to healthy controls [Table 2]. Systolic dysfunction was evident by decreased EF (P <0.05) and FS (P <0.05) in conventional echocardiography and decreased S wave (P <0.001) by tissue Doppler study while diastolic dysfunction was evident by the high E/E΄ ratio (P <0.001). Longitudinal global strain of the LV was significantly lower in patients compared to controls (P <0.001) which denote both systolic and diastolic dysfunctions. Fifteen (50%) patients had LV dysfunction either systolic or diastolic or both. Most of the patients with LV dysfunction were diagnosed by tissue Doppler or speckle tracking. Conventional echo parameters (EF and FS) were lower but not significantly different in patients with and without LV dysfunction [Table 3].
|Table 3: Clinical, laboratory, and echocardiographic data in patients with and without LV failure.|
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There were statistically significant higher serum levels of NT-pro BNP in the patient group before HD compared to its levels after HD (P = 0.031). There were also statistically significant higher serum NT-pro BNP levels in the patient group as compared to the control group (P <0.001) [Table 4]. Serum levels of NT-pro BNP in patients with LV dysfunction were highly elevated compared to patients without LV dysfunction both before (P = 0.003) and after (P <0.001) HD [Table 3]. No statistically significant differences were found between patients with and without LV dysfunction as regard Hb%, serum albumin, total cholesterol, or blood pressure (P >0.05). IDWG was statistically significantly higher in patients with LV dysfunction (P <0.001, [Table 3].
ROC curve demonstrated better prediction of LV dysfunction by NT-pro BNP levels after HD compared to its levels before HD (area under the curve was 0.9 and 0.73, respectively) Using a cutoff value of 630 ng/L, serum NTpro BNP levels after dialysis were a diagnostic predictor of LV dysfunction with a sensitivity of 86.6%, specificity of 93.3%, positive predictive value of 92.8%, and negative predictive value of 87.5% [Figure 1] and [Table 5]. There was nonsignificant correlation between plasma NT-pro BNP levels and age, duration of dialysis, systolic and diastolic blood pressure, and IDWG%. There was a significant negative correlation between serum levels of NT-pro BNP and FS% and EF%, S wave, and global longitudinal strain, and significant positive correlation with LV E/E΄ ratio.
|Figure 1: Receiver operating curve curves of serum N-terminal-pro B-type natriuretic peptide concentrations before and after hemodialysis and presence of left ventricular dysfunction. The upper left corner location of the curves indicates a good sensitivity and specificity of the N-terminal pro B-type natriuretic peptide in diagnosing left ventricular dysfunction. The area under the curve represents the overall accuracy of the N-terminal-pro B-type natriuretic peptide measurement.|
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| Discussion|| |
Serum levels of NT-pro-BNP were highly elevated in children with ESRD undergoing regular HD. Patients with and without LV dysfunction, as evidenced by echocardiographic assessments, had higher concentrations compared to controls. This may explain the difficulty of using this marker for the diagnosis of heart failure in those patients.
Many studies reported higher levels of natriuretic peptides in ESRD patients as a result of chronic volume overload and decreased renal excretion. ,,,,,,, In HD patients, fluid overload is multifactorial, including, inadequate dialysis, excessive water intake, absent residual renal function and patient noncompliance with treatment regulations. This fluid imbalance may contribute to the elevated levels of plasma NT-pro BNP without evidence of cardiac dysfunction.
The effect of dialysis on serum concentration of NT-pro-BNP is controversial. Some studies demonstrated a significant reduction similar to this study , while others found either no changes or increasing concentrations after dialysis. , Madsen et al, had reported a decrease in NT-pro BNP by 39% using dialysis with high-flux membranes  and Bargnoux et al reported 59% reduction in its concentration by hemodiafiltration.  High-flux membranes have a higher ultra-filtration rate than low-flux membranes. The larger size of NT-pro BNP molecule (8.5 kDa) may be the factor responsible for low clearance by a low-flux membrane with narrow pores. We used low-flux membrane dialyzers in HD of our patients, and the significant reduction of NT-pro BNP concentrations may be explained by multiple factors. First, the elimination due to adhesion and adsorption over the membrane, second the restoration of normovolemia may decrease the synthesis of NT-pro BNP. However, the relatively long half-life (120 min) of NT-pro BNP will need more time for this effect to evolve. In the present study, postdialysis sampling was taken 30 min after the end of HD session; in most other studies, postdialysis sampling was taken immediately at the end of the session. Third, the efficacy of dialysis may be also a contributing factor, as levels of NT-pro BNP were dependent on the effectiveness of dialysis as assessed by Kt/V and this was also reported in a previous study. 
In the present study, we could demonstrate that postdialysis NT-pro BNP cutoff value more than 630 ng/L could be used for diagnosis of LV dysfunction in HD children, regardless of the children's fluid load with 93.3% sensitivity and 80% specificity. Area under ROC curve for postdialysis values were better than predialysis values, this may be explained by less effect of fluid overload in postdialysis values. The level of NT-pro BNP had been found to be a strong prognostic marker in a variety of disease states such as hypertension and heart diseases. , In patients with ESRD on regular HD, the concentration of NT-pro BNP revealed increasing mortality with concomitant increasing concentrations, which was evident for both preand post-dialysis values.  This may explain the importance of determination of NT-pro BNP cutoff value for the use in clinical practice. Regular cardiac assessment and adequate control of volume status in HD patients will be of outmost importance to keep the levels of NT-pro BNP below the cutoff values to improve prognosis. However, before suggesting cutoff values to be used in clinical practice, larger cohorts will be needed in different age groups of the pediatric populations.
The present study showed that the patients with higher serum concentrations of NT-pro BNP before and after HD were diagnosed by echocardiography to have LV dysfunction. This was in agreement with Goto et al, and Naganuma et al, who reported that the preand post-dialysis plasma BNP values in patients with LV dysfunction were higher than that in normal LV function. , Despite the lower values of EF and FS in patients compared to controls, their levels were not significantly different in patients diagnosed with and without LV dysfunction. Conventional echocardiography has its limitation in the detection of the LV dysfunction. Diastolic dysfunction, which is a common mechanism of heart failure in dialysis patients, is not adequately evaluated in conventional echocardiography parameter. TDI has gained an increasing acceptance as a mean of noninvasively assessing myocardial properties and has been demonstrated as a prognostic tool in cardiac diseases. 2D STE has emerged as a novel technique for objective and quantitative evaluation of global and regional myocardial function, independent of the angle of myocardial insonation.  LV dysfunction in the present study was detected in most of the patients by tissue Doppler and speckle tracking.
Fluid status in this study was assessed by calculating IDWG%. Achievement of dry weight is one target of HD. Dry weight is defined as the lowest body weight a patient can tolerate without developing intraor interdialytic hypotension or other symptoms of dehydration.  In most dialysis units, dry weight is determined depending on clinical basis. No correlation was found in this study between INWG% and NT-pro BNP levels, even postdialysis values. This may decrease the possibility of using NT-pro BNP as a more accurate marker for estimating dry weight in HD. In previous studies, the correlation between NT-pro BNP levels and acute changes in preload during dialysis was not found. , This may explain the complexity of the factors controlling its levels and the need to adjust these factors.
| Limitations of the study|| |
Assessment of fluid status is only clinical. Bioimpedance and ambulatory BP monitoring are not available in our center. The relatively few number of patients included in the study did not allow classifications and analysis of data according to those with combined systolic and diastolic failure and those with each type of failure alone. Cutoff values of NT-pro BNP that can be used in clinical practice need larger cohorts of different age groups in pediatric populations to be validated.
| Conclusion|| |
Serum NT-pro BNP levels strongly correlated with LV echocardiographic parameters in patients with ESRD. Despite the high concentrations of NT-pro BNP in all dialysis children, its levels can be used as a diagnostic marker of LV dysfunction by using higher cutoff values. A postdialysis cutoff value of 630 ng/L could serve as a biochemical marker of early LV dysfunction regardless of chronic fluid overload. Long-term follow-up is required to evaluate the prognostic value of NT-pro BNP in those children.
Conflicts of interest: None declared.
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Maher Ahmed Abdel-Hafez
Department of Pediatrics, Faculty of Medicine, Tanta University, Tanta
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]
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