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Clinical Study

Early Initiation of Peritoneal Dialysis after Arterial Switch Operations in Newborn Patients

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Pages 204-209 | Received 17 Jul 2012, Accepted 29 Oct 2012, Published online: 26 Nov 2012

Abstract

Background and aim: We investigated the clinical outcome of early initiated peritoneal dialysis (PD) use in our newborn patients who underwent arterial switch operation (ASO) for transposition of the great arteries (TGA) and had routine intraoperative PD catheter implantation. We determined the risk factors for PD, factors associated with prolonged PD, morbidity, and mortality. The aim of the present study was to describe our experience of using PD in this patient cohort. Materials and Methods: Eighty two patients who were diagnosed with TGA and TGA-ventricular septal defect (VSD) and who had undergone TGA correction operation in Başkent University, Istanbul Medical Research and Training Hospital between 2007 and 2012 were retrospectively investigated. All the patients were under 30 days old. PD catheters were routinely implanted intraoperatively at the end of the operation. PD was initiated in transient renal insufficiency. In the absence of oliguria and increased creatinine level, PD was established in the presence of one of the following: clinical signs of fluid overload, hyperkalemia (>5 mEq/L), persistent metabolic acidosis, lactate level above 8 mmol/L or low cardiac output syndrome. The patients were divided into two groups according to the need for postoperative PD (PD group and non-PD group). PD was initiated in 32 (39%) patients after the operation, whereas 50 (61%) patients did not need dialysis. The clinical outcomes and perioperative data of the two groups were compared. Results: The demographics in the two groups were similar. Cardiopulmonary bypass time was longer in the PD group [non-PD group, 175.24 ± 32.39 min; PD group, 196.22 ± 44.04 min (p < 0.05)]. Coronary anomaly was found to be higher in the PD group [non-PD group, n = 2 patients (4.0%); PD group, n = 7 patients (21.9%); p < 0.05]. There was more need for PD in TGA + VSD patients [simple TGA patients, n = 14; TGA + VSD patients, n = 18 (p < 0.05)]. PD rate was higher in patients whose sterna were left open at the end of the operation (p < 0.05). The ventilator time [non-PD group, 4.04 ± 1.51 days; PD group, 8.12 ± 5.21 days (p < 0.01)], intensive care unit stay time [non-PD group, 7.98 ± 5.80 days; PD group, 15.93 ± 18.31 days (p < 0.01)], and hospital stay time were significantly longer in the PD group [non-PD group, 14.98 ± 10.14 days; PD group, 22.84 ± 20.87 days (p < 0.01)]. Conclusion: We advocate routine implantation of PD catheters to patients with TGA-VSD, coronary artery anomaly, and open sternum in which we have determined high rate of postoperative PD need.

INTRODUCTION

Acute renal failure (ARF) is a common complication in children following extensive pediatric cardiac surgery due to low cardiac output, massive hemolysis, and high fluid overload. Despite ongoing efforts to decrease its occurrence, ARF remains a frequent complication of cardiac surgery.Citation1,2 The reported ARF incidence ranges between 1% and 17%, depending largely on the criteria used to define the condition and the associated mortality is high (between 21% and 70%).Citation3,4

Postcardiotomy use of peritoneal dialysis (PD) in children became an accepted practice in the 1970s and it is usually the renal replacement therapy (RRT) of choice. It is preferred in clinical situations such as hypotension/hemodynamic instability (patients with closed or open sternum), disturbed coagulation, or difficult venous access, especially in very young children.Citation5,6 Although the choice of RRT remains controversial, PD has been demonstrated to be useful in light of the ease of application, effectiveness in fluid removal and avoidance of the need for anticoagulation, and establishment of additional vascular access.Citation7,8

Some centers routinely implant PD catheter in patients who undergo correction operation for transposition of the great arteries (TGA), whereas others apply only in selected patients. In our practice, all children with ARF following cardiac surgery are routinely treated with PD, which is an effective and safe method that requires no advanced technology. We investigated the clinical outcome of PD use in our newborn patients who underwent arterial switch operation (ASO) for TGA and had routine intraoperative PD catheter implantation. We determined the risk factors for PD, factors associated with prolonged PD, morbidity, and mortality. The aim of the present study was to describe our experience of using PD in this patient cohort.

MATERIALS AND METHODS

The clinical reports of 82 newborn patients who were diagnosed with TGA, TGA-ventricular septal defect (VSD), and who had undergone ASO operation in Başkent University, Istanbul Research and Training Hospital, between 2007 and 2012 were reviewed. All the patients were under 30 days old. Demographic data, preoperative risk factors, intraoperative variables, and postoperative complications were compared between patients requiring PD and those who did not need PD ().

Table 1.  Table demonstrating the preoperative demographics of the patients.

Surgical Technique

All patients underwent ASO. The coronary buttons were reimplanted to the neoaorta using Edward-Bowe technique. Under mild hypothermic perfusion, the normothermic blood cardioplegia was administered with mini cardioplegia technique. Modified ultrafiltration was performed in all the cases. Phentolamine infusion was routinely used during cardiopulmonary bypass (CPB).

PD catheters were routinely implanted perioperatively at the end of the operation. The patients were divided into two groups according to the need for postoperative PD (PD group and non-PD group). PD was initiated in 32 (39%) patients after the operation, whereas 50 (61%) patients did not need dialysis. The clinical outcomes and perioperative data of the two groups were compared.

Data were collected from patient files and intensive care unit (ICU) registries. Demographic and clinical data including weight and age at the time of surgery, type of cardiac disease, surgical procedure details, pre- and postoperative renal function data, time to diagnose ARF and PD initiation after surgery, cardiopulmonary and aorta cross-clamping time, and duration of inotropic support were obtained ().

Table 2.  Table demonstrating the postoperative data.

For patients requiring PD, the following data were additionally collected: initiation time and duration of PD; serum urea and creatinine levels before and after operation, before the start of PD, during PD, and just before discharge; the absolute amount of fluid withdrawn per day; daily fluid balance; and PD-related complications. In patients who were on ventilator support, peak inspiratory pressures before and after institution of PD were noted ().

Table 3.  Table demonstrating the postoperative hemodynamic and blood gas variables.

Peritoneal Dialysis

Indications for PD included oliguria (0.5 mL/kg/h) for more than 6 h despite aggressive diuretic therapy and optimization of inotropic support. In the absence of oliguria and increased creatinine level, PD was established in the presence of one of the following: clinical signs of fluid overload, hyperkalemia (>5.5 mEq/L), persistent metabolic acidosis, lactate level above 8 mmol/L, or low cardiac output syndrome.

Catheters were routinely inserted at the end of surgical procedure. The PD catheters were of the Tenckhoff type Kendall Quinton Curl Catheter (Tyco Healthcare Group LP, Mansfield, MA, USA) of 62 cm length. The PD catheter was connected to a closed system for peritoneal drainage.

The dialysate solutions used were of standard commercial preparations (Physioneal 40; Baxter Healthcare SA, Castlebar, Ireland). The dwell volume is usually initiated with 10 mL/kg. The dwell time, dwell volume, and glucose concentration were adjusted according to the individual needs of the patient. The volume was subsequently increased according to volume and solute load and clinical and laboratory parameters. Most of the patients were initially prescribed the lowest osmolarity solutions. When clinically appropriate, more hypertonic solutions were used to treat fluid overload (initially glucose 2.27% and later, if necessary, either 3.86% or maximum 4.26%). Additives such as potassium chloride, sodium bicarbonate, or antibiotics were included in the solutions as necessary. The dialysate bags were changed every 24 h. Serum albumin was regularly monitored, and intravenous albumin infusions were given as necessary. Indications for stopping PD included return of sufficient urine output to maintain or achieve negative fluid balance and normalization of serum electrolytes, lactate, and acid–base status.

Postoperative complications, such as sternal dehiscence, diaphragm paralysis, and subglottic narrowing and postoperative infections such as sepsis, urinary infections, pneumonia, surgical site infections, and catheter infections were noted.

Statistical Analysis

Data are expressed as mean ± standard deviation or median (range) as appropriate. Univariate analysis was performed to compare demographic data, preoperative risk factors, intraoperative variables, and postoperative complications of patients who required PD with those who did not, using unpaired Student’s t test, Mann–Whitney U test, and Fisher’s exact test as appropriate. In evaluating the data, Kolmogorov–Smirnov test along with descriptive statistical methods (mean and standard deviation) were used to test whether the parameters were normally distributed. The relationship between the parameters that were not normally distributed was investigated by Spearman’s rho correlation analysis. Multivariate analysis by logistic regression was used to identify predictors of the need for PD. Variables that were entered into the regression model included age, sex, weight, need for preoperative ventilation, preoperative renal failure, complexity of surgery, CPB duration, need for circulatory arrest, postoperative low cardiac output syndrome, and pulmonary hypertensive crisis. Univariate analysis was also performed to compare preoperative, intraoperative, and postoperative variables of PD and non-PD groups. The daily fluid balance was compared with a hypothetical mean of 0 by unpaired Student’s t test. Serial changes in serum urea and creatinine levels after institution of PD were compared using repeated analysis of variance. A p value of less than 0.05 was considered statistically significant. All statistical analyses were performed using SPSS version 15.0 (SPSS, Chicago, IL, USA).

RESULTS

A total of 82 patients were enrolled in the study. There were 29 females (35.4%) and 53 males (64.6%). The mean age of the patients was 13.17 ± 7.84 days. The PD and non-PD groups consisted of 32 and 50 patients, respectively. The two groups were similar with respect to age, weight, height, and body mass index (). There was no difference between the two groups in terms of preoperative blood urea nitrogen (BUN) and creatinine levels (p > 0.05).

The rate of preoperative ventilatory and inotropic support was higher in the PD group (37.5% vs. 24% and 15.6% vs. 6%, respectively). However, none of the differences were statistically significant. The rate of preoperative prostaglandin E1 (PGE1) treatment and atrial septectomy were similar in the two groups.

There is a statistically significant relationship between PD need and diagnosis. The rate of TGA-VSD patients was higher in the PD group than that in the non-PD group (p = 0.018). The rate of coronary anomaly was statistically higher in the PD group (n = 1 vs. n = 7; 4% vs. 21.9%; p = 0.012).

The CPB time in the PD group was statistically longer than that of patients in the non-PD group (p = 0.016). However, there was no difference with respect to cross clamp times (p = 0.556). The extubation, ICU, and in-hospital stay times were significantly longer in the PD group (p = 0.001). The mortality rates were 8% in the non-PD group (4/50) and 18.8% in the PD group (6/32). The difference was statistically insignificant (p = 0.147).

No major complication (peritonitis or hemodynamic instability) was observed related to the PD catheter (during the use or after the withdrawal). Minor complications were hyperglycemia and catheter site induration and/or leakage but no infectious pattern. Catheter-related complications also were not observed in the non-PD group. The rate of postoperative infection was statistically higher in the PD group (p = 0.003). The rate of delayed sternal closure was significantly higher in the PD group (p = 0.024). Catheter malfunctioning was observed in 10 (30.3%) patients, whereas the catheters had to be reimplanted in six (18.2%) patients. The catheter infection was observed in only one (3.03%) patient.

Ten (31.3%) patients in the PD group were on ventilator support before operation. The difference between preoperative and postoperative peak airway pressures was statistically insignificant (25.11 ± 4.10 vs. 25.89 ± 11.63 cm H2O; p = 0.846).

PD was effective in achieving negative fluid balance when compared with the non-PD group. There was statistically significant difference in daily fluid balance between the two groups except for the first postoperative day (p < 0.05; p < 0.01). On the other hand, the serum BUN and creatinine levels in the PD group were statistically higher than the non-PD group (p < 0.05; p < 0.01). There were no difference in the BUN and creatinine levels at the time of discharge (p > 0.05).

The mean PD duration was 5.12 ± 4.19 days (median 4 days). PD longer than 5 days was accepted as prolonged PD. Prolonged PD was not associated with preoperative BUN, creatinine levels, younger age, and preoperative body weight (p > 0.05). There was also no relationship between prolonged PD and history of preoperative PGE1 treatment, atrial septectomy, infection, inotropic support, and intubation (p > 0.05).

DISCUSSION

Today, surgical intervention in complex congenital cardiac cases is often performed in the neonatal period. At birth and for several months thereafter, the kidneys function with very limited reserve. The glomerular filtration rate is reduced in newborns compared with that of older infants.Citation9,10 Renal vascular resistance is high with correspondingly elevated circulating renin levels. Hormonal responses to volume loading including atrial natriuretic factor may also be limited in the newborn. All of these conditions render the neonate more prone to complications of ischemia than the older infant or child.Citation9 After complicated operations with long CPB times such as ASO, there is a high incidence of ARF.Citation7 Clinically, CPB is associated with a capillary leak syndrome, resulting in hypovolemia, and renal hypoperfusion.

Many different therapy modalities have been developed to reverse tissue edema and maintain postoperative negative fluid balance. Conventional medical treatment has included fluid restriction and diuretic therapy as well as inotropic support and afterload manipulation. When clinical and drug management cannot reverse these manifestations, RRT is mandatory. In this situation, RRT in children with ARF is required until the abnormalities are corrected, the cardiac function improves, and the kidneys recover their normal function, which happens a few days later. Our main indications for starting RRT were oliguria, anuria, and metabolic acidosis, which are similar to those described in other reports.Citation11,12 We mostly initiate PD in the first postoperative 24 h; in three patients the PD onset times were postoperative 1st, 2nd, and 4th days, respectively. Our median PD duration was 4 days and the PD was shown to provide negative fluid balance during the treatment.

The prevalence of ARF requiring RRT in children after open heart surgery has been reported to range from 1.6% to 9% depending on the complexity of procedure, preoperative status, and criteria for commencement of the dialysis treatment.Citation4,7,8,13 The mortality rate in children with ARF following heart surgery has been reported ranging from 10–90%.Citation7,8,13–16 Various authors have demonstrated that an earlier initiation of dialysis is associated with a lower mortality rate.Citation3,17 Santos defined early initiation as median time of 2 days between surgery and RRT.Citation3 Our study resembles Santos’ study and the mortality rate in our cohort was 18.8%, which may seem high at first sight but there is no study in the literature that solely involves newborn TGA patients on RRT; therefore, such a comparison with respect to morbidity and mortality is impossible to make.

Some centers prophylactically place peritoneal catheters after surgery in infants who are anticipated to be at high risk of ARF after CPB, whereas some centers including ours also aim to use these catheters to serve as a continuous drain of the abdominal cavity, use for dialysis for persistent low urinary output, to correct electrolyte and metabolic status, or to remove fluid.Citation7,13,18 In our study, the use of prophylactic PD in newborn’s ASO operation was found to be highly effective in providing rapid fluid management. Some authors reported continuous improvement in hemodynamics in children undergoing PD and showed rise in mean arterial pressure and decrease in inotropic support requirement.Citation8,19–21

Once correction of the volume load and low cardiac output is achieved, rapid improvement of renal function usually occurs. In our study, the rate of recovery of renal function was 100% among surviving patients, but in the literature, the recovery rate is variable, ranging from 29.5% to 100%.Citation3,22,11 The differences are probably related to the diverse patient populations and varying degrees of cardiac disease complexity described, or to in-center practices related to criteria for initiating RRT.

There is a controversy on the choice of RRT after open-heart surgery. PD and hemodialysis (HD) are the two most commonly used methods. Few studies have compared PD with other dialysis methods in ARF patients.Citation23 PD is postulated to be a more physiological and less inflammatory mode of dialysis than HD.Citation14,19 Most of the complications of PD are minor and easily manageable.Citation9,10,15 The complications of PD detected in this study were similar to those seen in other reports, consisting primarily of infection and catheter malfunction.Citation24,25 The reported complications in catheter functioning are around 30%, nearly 2% being major complications, of the catheters inserted in their pediatric patients which is nearly identical with our cohort (30.3%). The leakage of the peritoneal fluid from the catheter site and ineffective drainage of the peritoneal fluid through the peritoneal catheter were accepted as peritoneal catheter malfunctioning. This is usually related to the omentum that surrounds the catheter and occludes the holes on the catheter. When we detect catheter malfunctioning, we initially try to open these holes by injecting saline with pressure by 20 and 50 cc syringes into the catheter. This maneuver sometimes helps to overcome the problem and the catheter may work for some time. In patients whom we plan to end the PD soon, we chose this approach instead of replacing the catheter with a new one. In four patients, we managed to drain the peritoneal cavity with this approach. However, in the rest six patients, we replaced the catheters with new ones, which we implanted on different sites. The catheters had worked until the dialysis treatments were terminated. However, the catheter infection rate in our study (3.03%) is lower than the reported rates.Citation4,26–28 We speculate that this is related to the intraoperative catheter placement which may reduce the infection and complication rate associated with this treatment modality. Intraoperative PD catheter placement may enable heightened sterility and improved localization of the instrument through placement under direct vision.

There are also concerns that the presence of dialysate in the peritoneal cavity may cause diaphragmatic splinting and result in higher ventilatory pressures in mechanically ventilated patients. This is particularly detrimental to patients who require lung-protective ventilation strategies to minimize lung trauma. In our cohort, 31.3% of the PD patients were on ventilator support before initiation of PD and there was no change in the peak pressures after the commencement of PD (p > 0.05).

Several studies have attempted to identify risk factors of ARF requiring RRT in children undergoing surgery for congenital heart disease.Citation8,28,29 Thus, the important determinants of the outcome of patients requiring PD appear to be the preoperative and postoperative cardiopulmonary status rather than the renal status or timing of initiation of PD. It has been documented that low cardiac output, young age, low body weight, associated systemic disorders, high fluid overload, preexisting renal insufficiency, or mechanical ventilation before surgery were additional risk factors.Citation14 The risk factors determined in this study for PD in TGA patients less than 1 month old are CPB duration and presence of coronary anomaly. Santos also found CPB time as predictive of a subsequent need for PD.Citation3 Studies have demonstrated that patients with CPB times more than 90 min showed more pronounced kidney damage than patients with CPB times less than 70 min.Citation13,30 We were unable to determine a cut-off value due to the wide range of clinical data. Contrast-induced nephropathy can occur after angiography, particularly in infants and neonates.Citation31 We observed no change in renal function parameters and urine output after cardiac catheterization including atrial septectomy in this particular group of patient.

CONCLUSION

We believe that early initiation of PD with prophylactic PD catheter placement is a safe procedure with acceptable infection and mortality rate in newborn TGA patients. ARF is usually related to the complexity of the cardiac pathology and the duration of CPB. Unlike literature, our study group is composed of a subgroup of TGA patients who were under 30 days old and who underwent ASO. We found out that coronary anomaly in these patients is a risk factor for ARF and PD is highly effective and easy to manipulate in the renal replacement treatment of this cohort.

Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

REFERENCES

  • Mariscalco G, Lorusso R, Dominici C, Renzulli A, Sala A. Acute kidney injury: a relevant complication after cardiac surgery. Ann Thorac Surg. 2011;92:1539–1547.
  • Rosner MH, Okusa MD. Acute kidney injury associated with cardiac surgery. Clin J Am Soc Nephrol. 2006;1:19–32.
  • Santos CR, Branco PQ, Gonçalves MS, . Use of peritoneal dialysis after surgery for congenital heart disease in children. Semin Dial. 2010;23(1):95–99.
  • Romão JER, Fuzissima MG, Vidonho AF, . Outcome of acute renal failure associated with cardiac surgery in infants. Arq Bras Cardiol. 2000;75(4):318–321.
  • Goldstein SL. Overview of pediatric renal replacement therapy in acute renal failure. Artif Organs. 2003;27:781–785.
  • Walters S, Porter C, Brophy PD. Dialysis and pediatric acute kidney injury: choice of renal support modality. Pediatr Nephrol. 2009;24:37–48.
  • Kist-van Holthe tot Echten JE, Goedvolk CA, Doornaar MBME, . Acute renal insufficiency and renal replacement therapy after pediatric cardiopulmonary bypass surgery. Pediatr Cardiol. 2001;22:321–326.
  • Chan K, Ip P, Chiu CSW, Cheung Y. Peritoneal dialysis after surgery for congenital heart disease in infants and young children. Ann Thorac Surg. 2003;76:1443–1449.
  • Alkan T, Akcevin A, Turkoglu H, et al. Postoperative prophylactic peritoneal dialysis in neonates and infants after complex congenital cardiac surgery. ASAIO Journal. 2006;52:693–697.
  • Sorof JM, Stromberg D, Brewer ED, Feltes TF, Fraser CD. Early initiation of peritoneal dialysis after surgical repair congenital heart disease. Pediatr Nephrol. 1999;13:641–645.
  • Pederson KR, Hjortdal VE, Christensen S, Pederson J, Hjortholm LS, Povisen JV. Clinical outcome in children with acute renal failure treated with peritoneal dialysis after surgery for congenital heart disease. Kidney Int Suppl. 2008;108:81–86.
  • Romao JE Jr, Fuzissima MG, Vidonho AF, . Outcome of acute renal failure associated with cardiac surgery in infants. Arq Bras Cardiol. 2000;75:313–321.
  • Abou El-Ella RS, Najm HK, Godman M, Kabbani MS. Acute renal failure and outcome of children with solitary kidney undergoing cardiac surgery. Pediatr Cardiol. 2008;29: 614–618.
  • Miyamoto T, Yoshimoto A, Tatsu K, Ikeda K, Ishii Y, Kobayashi T. Zero mortality of continuous veno-venous hemodiafiltration with PMMA hemofilter after pediatric cardiac surgery. Ann Thorac Cardiovasc Surg. 2011;17:352–355.
  • Boigner H, Brannath W, Hermon M, . Predictors of mortality at initiation of peritoneal dialysis in children after cardiac surgery. Ann Thorac Surg. 2004;77:61–65.
  • Skippen PW, Krahn GE. Acute renal failure in children undergoing cardiopulmonary bypass. Crit Care Resusc. 2005;7:286–291.
  • Dittrich S, Dähnert I, Vogel M, . Peritoneal dialysis after infant open heart surgery: observations in 27 patients. Ann Thorac Surg. 1999;68:160–163.
  • Duncan BW, Poirier NC, Mee RBB, . Selective timing for the arterial switch operation. Ann Thorac Surg. 2004;77: 1671–1677.
  • Cole L, Bellomo R, Journois D, Davenport P, Baldwin I, Tipping P. High-volume hemofiltration in human septic shock. Intensive Care Med. 2001;27:978–986.
  • Werner HA, Wensley DF, Lirenman DS, LeBlanc JG. Peritoneal dialysis in children after cardiopulmonary bypass. J Thorac Cardiovasc Surg. 1997;113:64–68.
  • Dittrich S, Vogel M, Dahnert I, Haas NA, Alexi-Meskishvili V, Lange PE. Acute hemodynamic effects of post pericardiotomy peritoneal dialysis in neonates and infants. Intensive Care Med. 2000;26:101–104.
  • Jander A, Tkaczyk M, Pagowska–Klimek I, et al. Continuous veno-venous hemodiafiltration in children after cardiac surgery. Eur J Cardiothorac Surg. 2007;31:1022–1028.
  • Ponce D, Balbi AL. Peritoneal dialysis in acute kidney injury: a viable alternative. Perit Dial Int. 2011;31(4):387–389.
  • Flynn JT, Kershaw DB, Smoyer WE, Brophy PD, McBryde KD, Bunchman TE. Peritoneal dialysis for management of pediatric acute renal failure. Perit Dial Int. 2001;21:390–394.
  • Hanson J, Loftness S, Clark D, Campbell D. Peritoneal dialysis following open heart surgery in children. Pediat Cardiol. 1989;10:125–128.
  • Lattout OM, Rickets RR. Peritoneal dialysis in infants and children. Am Surg. 1986;2:66–69.
  • Reznik VM, Griswold WR, Peterson BM, Rodarte A, Fervis ME. Peritoneal dialysis for acute renal failure in children. Paediatr Nephrol. 1991;5:715–717.
  • Raaijmakers R, Schroder CH, Gajjar P, Argent A, Nourse P. Continuous flow peritoneal dialysis: first experience in children with acute renal failure. Clin J Am Soc Nephrol. 2011;6:311–318.
  • Abel RM, Buckley MJ, Austen WG, Barnett GO, Beck CH Jr, Frischer JE. Etiology, incidence and prognosis of renal failure following cardiac operations. J Thorac Cardiovasc Surg. 1986;71:323–333.
  • Boldt J, Brenner T, Lehmann A, Sutter SW. Is kidney function altered by the duration of cardiopulmonary bypass? Ann Thorac Surg. 2003;75(3):906–912.
  • Niboshi A, Nishida M, Itoi T, Shiraishi I, Hamaoka K. Renal function and cardiac angiography. Indian J Pediatr. 2006; 73(1):49–53.

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