Eur J Cardiothorac Surg 2004;25:935-940
© 2004 Elsevier Science NL
Effects of ultrafiltration and peritoneal dialysis on proinflammatory cytokines during cardiopulmonary bypass surgery in newborns and infants
S. Dittricha*,
D. Aktuerka,
S. Seitzb,
P. Mehwalda,
J. Schulte-Möntingc,
C. Schlensakd,
D. Kececioglua
a Department of Congenital Heart Disease/Pediatric Cardiology, Albert-Ludwigs University of Freiburg, Mathildenstraße 1, D-79106 Freiburg i.Br., Germany
b Department of Anaesthesiology, Albert-Ludwigs University of Freiburg, Freiburg i.Br., Germany
c Department of Medical Biometry and Statistics, Albert-Ludwigs University of Freiburg, Freiburg i.Br., Germany
d Department of Cardiovascular Surgery, Albert-Ludwigs University of Freiburg, Freiburg i.Br., Germany
Received 15 December 2003;
received in revised form 3 February 2004;
accepted 9 February 2004.
* Corresponding author. Tel.: +49-761-270-4323; fax: +49-761-270-4468
e-mail: dittrich{at}kikli.ukl.uni-freiburg.de
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Abstract
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Objectives: To assess the impact of balanced ultrafiltration and peritoneal dialysis (PD) on plasma and urinary cytokines and renal dysfunction after cardiopulmonary bypass (CPB) surgery in newborns and infants. Methods: Twenty-three newborns and infants weighing less than 7 kg and scheduled for operation on congenital malformation were enrolled in this descriptive open clinical study. All patients received conventional ultrafiltration in the CPB rewarming period. Eleven newborns underwent Tenckhoff-catheter implantation in the operation theatre as a routine institutional procedure and received PD after admission to the ICU (the PD [+] group). No PD was used in another 12 patients (the PD [–] group). Interleukins (IL) 6 and 8 were measured four times pre- and post-operatively. Kidney function was assessed by creatinine clearances and urine protein and enzyme analyses. Results: All patients had an uneventful clinical course. Age (10±2 days, PD [+] vs. 96±19 days, PD [–]), CPB duration (215±23 vs. 143±20 min), and degree of hypothermia (26±1.3 vs. 31±0.1 °C) differed significantly between the groups. Age, CPB duration and ultrafiltration influenced post-operative IL-levels in an analysis of variance. While there were few differences immediately after the end of ultrafiltration, post-operative levels of IL-6 and IL-8 were higher and more sustained in the newborns (PD [+]) than in the older infants (PD [–]). The median amount of IL-6 and IL-8 removed by ultrafiltration came to 28 and 59% compared to the amount of IL-6 and IL-8 remaining in the blood at the end of CPB. IL-clearance by ultrafiltration was more than 1000-fold and by PD more than 100-fold as effective as IL-clearance by the kidney. While the kidneys showed an unselective mixed glomerular and tubular pattern of injury, during CPB higher serum IL-concentrations correlated with lower urinary IL-clearances in both study groups. Conclusions: Ultrafiltration and PD are highly effective in removing proinflammatory cytokines. Impaired kidney function was associated with proinflammatory IL-serum concentrations. Thus, we raise the hypothesis that glomerular-filtered proinflammatory ILs damage the proximal tubular cells of the kidney in newborns and infants, thus contributing to post-operative renal dysfunction. Conversely, we conclude that removing proinflammatory ILs by ultrafiltration and PD acts renoprotectively. A future prospective randomised study could demonstrate whether this can indeed improve clinical outcome.
Key Words: Ultrafiltration • Peritoneal dialysis • Cardiopulmonary bypass • Interleukins • Congenital heart disease
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Introduction
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The use of cardiopulmonary bypass (CPB) in newborns and infants with congenital heart disease is associated with an inflammatory reaction and leaky capillary syndrome. Patients are at risk of developing multiorgan failure, which mainly affects kidney, heart, and lung [1–3]. Kidney function is frequently impaired after neonatal and infant CPB surgery [4,5]. However, adequate kidney function after CPB is important with respect to care with (1) fluid overload and haemodilution during CPB, (2) leaky capillary syndrome and volume requirements after CPB, and (3) the excretion of proinflammatory cytokines after CPB [6–8]. Ultrafiltration in CPB is one method of supporting the patient during care with fluid overload and inflammation [3,9], and post-operative peritoneal dialysis (PD) may be another method [8,10]. However, details on the use of ultrafiltration [9] and the use of PD [10] differ widely among paediatric cardiac centres. It has been shown that proinflammatory interleukins-6 (IL-6) and -8 (IL-8) can be removed by PD [8], but the clinical significance of this method remains unclear. The aim of our study was to evaluate in our institution the impact of ultrafiltration and PD with respect to cytokine homeostasis and renal function.
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1. Methods
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This study was approved by our institutional ethics committee, and all parents provided written informed consent. The study was open to newborns and infants scheduled for CPB surgery for congenital heart disease between December 2001 and February 2003. Exclusion criteria were previous CPB operation, kidney disease, infection, and failure to obtain consent. This study includes 23 patients, 11 of whom (the PD [+] group, all newborn) received a Tenckhoff-catheter in the operation theatre and PD immediately after admission to the ICU, and 12 who did not (the PD [–] group). Diagnoses and operations in the PD [+] group were arterial switch operation in five patients with transposition of great arteries (with additional VSD repair in two), Norwood I operation in four patients with hypoplastic left heart syndrome, repair of interrupted aortic arch and VSD in one patient, and repair of total anomalous pulmonary vein drainage in one patient. The PD [–] group included coarctation and VSD repair, repair of anomalous left coronary artery from pulmonary artery, common arterial trunk repair, arterial switch operation in transposition of the great arteries, coarctation repair after previous Norwood I operation, Glenn operation in double inlet left ventricle in one patient each, repair of complete atrio-ventricular septal defect in two patients, and VSD repair in four patients.
1.1. Cardio pulmonary bypass technique and ultrafiltration
Anaesthesia and CPB were performed with standard protocols. Dexamethason (Fortecortin®, Merck, Darmstadt, Germany; 1 mg/kg) was given prior to CPB. Conventional ultrafiltration was performed in the CPB reperfusion period. A dialysis cartridge (DHF02, Dideco, Modena, Italy) was inserted as a parallel circuit into the arterial line. After de-clamping the aorta, the dialysis cartridge was perfused with a flow of 100 ml/min in order to achieve an ultrafiltration volume of 100–300 ml/kg.
1.2. Peritoneal dialysis
A Tenckhoff-catheter (15.3 in Pediatric Curl Cath, Tyco, Switzerland) is routinely inserted via thoracotomy in the peritoneal cavity in every newborn after complex operation at our institution. PD is then initiated after admission to the ICU regardless of patient diuresis. Patients on PD received only a standard dose of furosemide (2 mg/kg per day). PD is done hourly, using a 2.3% glucose solution (CAPD/DPCA 4, Fresenius, Bad Homburg, Germany), an inflow volume of 10 ml/kg per cycle, and a dwelling time of 15 min/cycle.
1.3. Investigation periods
IL-6, IL-8, and creatinine were analysed from plasma blood, urine, ultrafiltrate and PD-fluid samples after induction of anaesthesia, immediately after the end of CPB, and at 6 and 18 h post-CPB. The amount of circulating cytokines at the end of CPB was calculated from the serum concentration; the haematocrit and blood volume, which was calculated with 80 ml/kg+380 ml extracorporeal volume. Urine samples were taken on the day before operation, and during the operation at three time periods, starting from the insertion of the urinary catheter up to the end of CPB, 6 h thereafter, and then again 12 h later. Renal function was evaluated by protein (albumin) and enzyme (N-acetyl-ß-D-glucosaminidase (NAG)) analysis in the urine samples and expressed as urine creatinine ratios [4]. Renal clearances for creatinine, IL-6, and IL-8 were calculated using standard formulas.
1.4. Statistics
After logarithmic transformation, values for serum IL-6 and IL-8, urinary IL-6 and IL-8 clearance, diuresis, creatinine-clearance, urinary albumin and NAG were analysed with repeated measures ANOVA with respect to (1) data differences over the course of time, (2) differences in values between the groups, and (3) differences between groups concerning the chronological sequence of data. Analysis of variance included patient age, CPB duration, and ultrafiltration. Demographic group means were compared with the Mann–Whitney U-test (nonparametrically). Correlations between serum ILs and kidney function parameters were assessed separately for both groups with the Spearman's rank correlation coefficient (nonparametrically), in order to avoid comparing immature neonatal renal function with that of infants. Figure results are presented as mean±SEM and as medians, minima, and maxima in the table. Differences were considered statistically significant when the probability of type 
error was under 5%.
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2. Results
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Age at operation was younger in the PD [+] group (10±2 days, PD [+] vs. 96±19 days, PD [–]). Patients in the PD [+] group underwent longer CPB perfusion times (215±23 min, PD [+] vs. 143±20 min, PD [–], Table 1). The analysis of variance demonstrated that patient age, CPB-duration, and amount of ultrafiltration affect post-operative IL values. IL-6 and IL-8 serum concentrations were elevated post-operatively in all patients, with significant differences between both groups in IL-8 at all time points and in IL-6 at 6 and 18 h post-operatively (Fig. 1)
. IL-6 and IL-8 values in the PD [–] group nearly normalised, and remained elevated in the PD [+] group (Fig. 1). Contrarily, the values for renal IL-6 and IL-8 clearances were significantly lower 6 and 18 h after CPB in the PD [+] group. Furthermore, the different chronological sequence of data with falling IL-6 and IL-8 clearances in the PD [+] group and rising IL-6 and IL-8 clearances in the PD [–] group nearly achieved statistical significance, P=0.069 for IL-6, and P=0.079 for IL-8, repeated multivariate ANOVA, respectively (Fig. 1). In the PD [+] group renal function was more impaired as indicated by diuresis, creatinine clearance, urinary albumin and NAG measurements (Fig. 2)
. Diuresis and creatinine clearance recovered significantly after CPB in both groups. However, the speed of renal regeneration as indicated by those two parameters tended to be slower in the PD [+] group, P=0.052 for the diuresis, and P=0.057 for the creatinine clearance, repeated measures ANOVA, respectively (Fig. 2). The time trend of urinary NAG values did not reach statistical significance (Fig. 2). All urinary NAG values 6 h post-CPB in the PD [+] group (mean 590, minimum 139, and maximum 1010 U/gcrea) were elevated compared to pre-CPB values in the PD [–] group (mean 10, minimum 14, and maximum 93 U/gcrea). Serum IL-6 and IL-8 concentrations during CPB revealed a negative correlation to the urinary IL-6 and IL-8 clearances in both study groups (Spearman coefficient, r<–0.05, P<0.05, Table 2). Ultrafiltration was highly effective in removing IL-6 and IL-8 from the blood circuit (Figs. 3 and 4)
. The total amount of IL-6 removed from the circulation by ultrafiltration was 28% (1–419%), according to the remaining IL-6 in the circulation at the end of CPB, and 59% (2–145%) for IL-8 (Fig. 3). PD was also highly effective in removing IL-6 and IL-8 from the blood (Fig. 4).
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Fig. 1. Pre- and post-operative interleukins. *P<0.05 for differences in values between groups. #P<0.05 for differences in values over the time course. $1P=0.07, $2P=0.08 for differences between groups concerning chronological sequence of data, repeated two-sided measures ANOVA. IL-6 and IL-8 serum concentrations are higher and did not normalise within study period in newborn PD [+] group (upper line). Urinary IL-clearances lower in PD [+] group and increase more rapidly in PD [–] group (lower line). Urinary albumin and NAG analyses show peak increase 6 h after CPB (n.s.) (right upper line). Tendency (P=0.06) of creatinine-clearance to recover more rapidly in the PD [–] group. Diuresis in PD [+] is lower 6 h after CPB and recover more rapidly in PD [–] group (right lower line).
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Fig. 2. Pre- and post-operative renal function. *P<0.05 for differences in values between groups. #P<0.05 for differences in values over the time course. $3P=0.06, $4P=0.05 for differences between groups concerning chronological sequence of data, repeated two-sided measures ANOVA. Urinary albumin and NAG analyses showed a peak increase 6 h after CPB (n.s.) (upper line). Tendency (P=0.06) of creatinine-clearance to recover more rapidly in PD [–] group. Diuresis in PD [+] is lower 6 h after CPB and recover more rapidly (P=0.05) in PD [–] group (lower line).
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Table 2. Correlation between IL-6 and IL-8 serum concentrations and urinary clearances during CPB in the neonatal PD group
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Fig. 3. Concentrations of interleukins in serum and ultrafiltrate at the end of CPB. Total amount of IL-6 removed from CPB by ultrafiltration came to 28% (1–419%) for amount of IL-6 remaining in circulation at end of CBP, and to 59% (2–145%) for IL-8.
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Fig. 4. Excretion of IL-6 and IL-8 by different methods. IL-6 and IL-8 excretion by ultrafiltration, PD, and kidney. Note the logarithmic scale of the y-axis. Ultrafiltration excretion rate of IL-6 and IL-8 was 1000-fold, and PD excretion rate was 100-fold higher than excretion of IL-6 and IL-8 measured in the urine.
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3. Discussion
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This study was designed to investigate the influence of ultrafiltration and PD on CPB-induced proinflammatory IL elevation. The elevation of proinflammatory ILs after CPB-surgery may be involved in myocardial damage and myocardial dysfunction [11], and ILs have been implicated in several effects that could directly relate to the phenomena of leaky capillary syndrome and organ dysfunction [12]. It is a standard practice at our institution to perform continuous ultrafiltration on every newborn and infant during CPB during the rewarming period. Though no differences in post-operative outcome have ever been proven, a few studies in the paediatric and adult population have shown ultrafiltration to increase haematocrit and reduce some of the inflammatory markers [9]. We quantified IL-6 and IL-8, which were removed from the blood circuit by conventional ultrafiltration, and we found this method during this study to be more than 1000-fold more effective than the kidney in newborns and infants (Fig. 4). The amount of ultrafiltration affected post-operative proinflammatory IL values (analysis of variance, P<0.05) The amount of ILs removed by ultrafiltration in the median came to 28–59% compared to the IL-6 and IL-8 amounts circulating in the blood at the end of CPB, respectively. Though the post-CPB IL-6 and IL-8 values were highly elevated compared to those pre-operative, post-CPB IL-6 and IL-8 serum values differed only slightly between neonates (PD [+]) and infants (PD [–]; Fig. 1). This observation may be mainly related to the ultrafiltration effect. In contrast, the newborn PD [+] group developed a more pronounced IL response after CPB (Fig. 1).
After complex CPB surgery in newborns we routinely implant a Tenckhoff-catheter at the end of the operation and perform PD without any respect to diuresis. The rational basis for this practice was gleaned from the literature, where some reports of impaired renal function after CPB [4,5] and positive PD-effects concerning fluid balance and potassium control can be found [10,13]. However, this clinical practice made it difficult to, from an ethical point of view, create a newborn control group without PD, though several teams at different centres who hardly ever use PD also obtain extremely good results. Our reluctance to randomise patients on PD explains the differences in age, CPB duration and hypothermia between our study groups (Table 1). As expected, variance analysis proved these factors to influence post-operative IL levels. Our study demonstrated two main results concerning PD, it removed large amounts of proinflammatory ILs from the blood circuit (Fig. 4), and PD [+] group-IL serum values were higher (Fig. 1). We thus cannot prove that PD actually eases the overall proinflammatory IL burden. The (PD+) group's higher IL values are affected by neonatal age and longer CPB durations in more complex operations, and this makes comparison difficult with infants in the PD [–] group. However, as IL-6 and IL-8 are not known to be induced by routine PD [14], it is conceivable that these high proinflammatory IL levels would have been even higher without PD. In line with one recent report [8], we found proinflammatory IL-6 and IL-8 in PD fluid. Furthermore, we demonstrate that PD was more than 100-fold more effective in removing IL-6 and IL-8 from the blood circuit than was the kidney itself (Fig. 4).
Renal function in our study was, as with previous reports [4], intra- and post-operatively impaired in both study groups, revealing a pattern of nonselective mixed glomerular and tubular injury (Fig. 2). The pathophysiological reasons for this injury may include low post-operative cardiac output and haemorrheological patterns [4]. We also found proinflammatory IL-6 and IL-8 excretion into the urine (Fig. 4), and IL-6 and IL-8 serum concentrations in both groups correlated with urinary IL-6 and IL-8 clearances (Table 2). The higher the serum concentrations, the lower the urinary clearances. We could not measure the renal glomerular filtration rate and IL-6 and IL-8 metabolic rates in the renal tubular cells in our study. However, renal IL-6 and IL-8 clearances increase with falling urinary NAG concentrations, indicating recovery of renal tubular dysfunction in the PD [–] group (Figs. 1 and 2). There has been recent focus in the adult population on inflammatory renal damage caused by proinflammatory cytokines filtered into the primary urine [6,15,16]. The kidney preferentially filters smaller proinflammatory cytokines like IL-6 and IL-8, and less readily the larger anti-inflammatory cytokines. Ordinarily, these small proinflammatory cytokines are presented to the proximal renal tubules and absorbed by the proximal tubular cells [17]. The normal kidney efficiently metabolises filtered proinflammatory cytokines. Renal cytokine clearance after CPB has been hypothesised to be the key for controlling the required balance of proinflammatory and anti-inflammatory response [7]. Gormley et al. investigated 20 adults undergoing coronary artery grafting on CPB. He found no proinflammatory cytokines in the urine, but urinary anti-inflammatory IL-1ra correlated with the renal tubular damage marker NAG [16]. From this observation they hypothesised that the filtered proinflammatory cytokines may induce proximal renal tubular injury and trigger an intrarenal anti-inflammatory response for the safe disposal of the proinflammatory cytokines. Our data also validate this hypothesis in the newborn and infant populations. Glomerular-filtered proinflammatory ILs may damage the kidney's tubular cells and thus contribute to post-operative renal dysfunction in newborns and infants after CPB surgery. We, therefore, conclude that the removing of proinflammatory ILs by ultrafiltration and PD acts renoprotectively.
However, a prospective randomised study testing the efficacy of PD in neonates is necessary to validate this conclusion.
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4. Study limitations
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For ethical reasons we were reluctant to randomise patients on PD even though other groups obtain extremely good clinical results hardly ever using PD. Thus, patient selection for the PD [+] and PD [–] groups is biased by age, diagnosis and surgical complexity. This might explain higher serum IL-6 and IL-8 concentrations in the newborn group (PD [+]), and thus ultrafiltration and PD efficiency in reducing post-operative proinflammatory IL-6 and IL-8 serum values cannot be demonstrated by inter-group comparison. As there is no technique to estimate renal glomerular IL-6 and IL-8 filtration and metabolic rate in the renal tubular cells, our urinary IL-6 and IL-8 analyses underestimate renal IL-6 and IL-8 clearances.
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5. Conclusions
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Ultrafiltration and PD are highly effective in removing proinflammatory cytokines IL-6 and IL-8 from the blood circuit after neonatal and infant CPB surgery. As elevated IL-6 and IL-8 serum levels during CPB are associated with renal tubular dysfunction in neonates and infants, we hypothesise that glomerular-filtrated proinflammatory ILs damage renal tubular cells. Conversely, we conclude that pre-renal displacement of proinflammatory IL-6 and IL-8 by ultrafiltration and PD act renoprotectively. A future prospective randomised study is needed to demonstrate whether this can be translated into clinical advantage.
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Acknowledgments
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We are grateful to Lothar B. Zimmerhackl MD, who measured the urinary proteins and enzymes, Hans Seydewitz MD, who determined the inflammatory mediators, and Carole Cuerten, who provided editorial help.
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Footnotes
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Read at the 38th Annual Meeting of The Association for European Pediatric Cardiology, Amsterdam, May 28–31, 2003.
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Abstract
Introduction
