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Ann Thorac Surg 2006;81:2267-2272
© 2006 The Society of Thoracic Surgeons

Original article: Cardiovascular

Clinical Implication of Blood Levels of B-Type Natriuretic Peptide in Pediatric Patients on Mechanical Circulatory Support

Shu-Chien Huang, MD a , b , En-Ting Wu, MD c , Wen-Je Ko, MD, PhD a , Ling-Ping Lai, MD, PhD d , Juin Hsu, MD e , Chung-I. Chang, MD a , Ing-Sh Chiu, MD, PhD a , Shoei-Shen Wang, MD, PhD a , Mei-Hwan Wu, MD c , Fang-Yue Lin, MD, PhD a , Yih-Sharng Chen, MD, PhD a , e , *

a Department of Surgery, Yun-Lin Branch of National Taiwan University Hospital, National Taiwan University Hospital and College of Medicine, National Taiwan University, Taipei, Taiwan
b Department of Traumatology, Yun-Lin Branch of National Taiwan University Hospital, National Taiwan University Hospital and College of Medicine, National Taiwan University, Taipei, Taiwan
c Department of Pediatrics, Yun-Lin Branch of National Taiwan University Hospital, National Taiwan University Hospital and College of Medicine, National Taiwan University, Taipei, Taiwan
d Department of Pharmacology, Yun-Lin Branch of National Taiwan University Hospital, National Taiwan University Hospital and College of Medicine, National Taiwan University, Taipei, Taiwan
e Department of Surgery, Yun-Lin Branch of National Taiwan University Hospital, National Taiwan University Hospital and College of Medicine, National Taiwan University, Taipei, Taiwan

Accepted for publication December 20, 2005.

* Address correspondence to Dr Chen, Department of Cardiothoracic Surgery, National Taiwan University Hospital, Yun-Lin Branch, 7 Chung-Shan South Rd, Taipei 100, Taiwan (Email: yschen11{at}yahoo.com.tw).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: B-type natriuretic peptide (BNP) is a marker of heart failure. In adult patients with heart failure, decreased BNP levels after implantation of ventricular assist devices may be indicative of recovery. However, BNP levels among pediatric patients receiving mechanical support are largely unknown.

METHODS: Fifteen pediatric patients with cardiogenic shock who were supported by extracorporeal membrane oxygenation (ECMO) were evaluated. The BNP levels were determined before ECMO initiation, during ECMO support, and after ECMO removal.

RESULTS: All patients had elevated BNP levels before initiation of ECMO (median, 1,430 pg/mL; range, 361 to 5,000 pg/mL). Among the 15 patients, 1 received heart transplantation. Extracorporeal membrane oxygenation was withdrawn in 2 patients, and the other 12 patients were weaned from ECMO. Four patients died after initially successful weaning from ECMO. The BNP levels of the nonsurvivors (median, 3,685 pg/mL; range, 2,494 to 5,000 pg/mL) were higher than those of the survivors (median, 1,127pg/mL; range, 108 to 3,030 pg/mL) on the next few days after ECMO removal (p = 0.016). The BNP levels on the fourth day after removal of ECMO among the survivors (median, 498 pg/mL; range, 108 to 890 pg/mL) were lower than those among the nonsurvivors (median, 3,900 pg/mL; range, 3,230 to 5,000 pg/mL; p = 0.017).

CONCLUSIONS: Among pediatric patients supported with ECMO, the survivors had lower BNP levels than those who did not survive. We suggest that serial blood BNP levels can be potential markers for monitoring pediatric patients on mechanical circulatory support, and the concept merits further study.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
The B-type natriuretic peptide (BNP) is produced in the myocardium in response to mechanical stretch [1] or ischemia [2] and serves as a marker of cardiac overloading and heart failure [1, 3]. The elevation of blood BNP levels is related to morbidity and mortality in the setting of heart failure [4] and acute myocardial infarction [5]. In recent reports, patients requiring ventricular assist device therapy were assessed for changes in BNP levels and had lower levels after ventricular assist device therapy was instituted [6, 7]; there is also evidence that an early decrease in blood BNP may be indicative of recovery of ventricular function during ventricular assist device support [6]. However, it remains unknown whether this phenomenon occurs in infants and children on mechanical support.

In pediatric and neonatal patients, extracorporeal membrane oxygenation (ECMO) remains the preferred strategy to support cardiopulmonary failure [8]. In this study, we tried to understand the clinical informative value and prognostic role of BNP levels in pediatric patients requiring ECMO support.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
Pediatric patients younger than 18 years of age who received ECMO for cardiac support in our institution between October 1, 2004, and October 30, 2005, were included in this study. The study was approved by the institutional review board of our hospital.

Indications for Extracorporeal Membrane Oxygenation
The indications for ECMO included (1) failure to separate from cardiopulmonary bypass, thus, requiring initiation of ECMO in the operation room; (2) profound cardiogenic shock in the intensive care unit because of postoperative low-output syndrome or other potentially reversible condition; or (3) cardiac arrest in the intensive care unit with ECMO used for cardiopulmonary resuscitation.

Extracorporeal Membrane Oxygenation Technique
The ECMO circuit consisted of a centrifugal pump (BP-50 or BPX-80 Bio-Pump, Medtronic Inc, Anaheim, CA) and a hollow-fiber membrane oxygenator (Minimax Plus or Affinity NT, Medtronic) similar to that previously described by Jacobs and associates [9], in which the whole surface was heparin-bound. We did not use a bridge between the arterial and venous circuits. The patients were cannulated through the ascending aorta and the right atrium if they had just undergone cardiac surgery, or their sternum wound was kept open for ready access for cannulation. For patients who weighed more than 30 kg, cannulation was performed through the femoral vessels by means of the cut-down method [10]. Left ventricle decompression by left atrial drainage was only performed for severe lung edema in 2 patients (patients 1 and 14). In patients with systemic–pulmonary shunts, the shunts were kept open during ECMO.

Extracorporeal membrane oxygenation blood flow was generally maintained between 80 and 120 mL/kg per minute for neonates, or about 40 to 60 mL/kg per minute for adolescents. Vasoactive infusions were gradually tapered if adequate blood pressure was achieved after using ECMO. Diuretics were administered in cases of fluid overload, and a peritoneal dialysis or hemofiltration was used to augment fluid removal if needed.

The decision to wean a child from ECMO was determined by adequate blood pressure, no metabolic acidosis, decreased blood lactate level, and a clear chest roentgenographic image. The ECMO flow was decreased gradually, and then ECMO was removed if the blood pressure could be maintained and the blood gas analysis did not show obvious metabolic acidosis. The sternotomy wound was usually kept open for an additional 2 to 3 days.

Data Collection
Before ECMO initiation (t1), the patient's clinical condition, lactate level, and BNP level were recorded. For prognostic information about weaning from ECMO, we collected blood samples for BNP analysis before beginning ECMO weaning (t2) and the day after removal of ECMO (t3). B-type natriuretic peptide levels were checked again 4 days after removal of ECMO (t4). Patient who underwent heart transplantation or expired did not have the data for t3 or t4.

The BNP analysis was performed on whole blood using the Triage BNP assay within 1 hour of obtaining the sample (Biosite Inc, San Diego, CA) [11]. The Triage BNP test is a fluorescence immunoassay designed for rapid quantitative determination of BNP in whole blood or plasma. The cutoff value for an abnormal level was reported as 100 pg/mL, and the upper limit of the assay was 5,000 pg/mL; values above the upper limit were reported as 5,000 pg/mL.

Simultaneous hemodynamic data, including heart rate, blood pressure, central venous pressure, and urine output (mL/kg per hour) were collected. The arterial blood gas and serum lactate levels were also recorded when obtaining the BNP data.

The primary outcome was survival of the patients to hospital discharge. The BNP levels, hemodynamic data, and laboratory values were tested for correlation with the clinical outcome.

Statistical Analysis
Descriptive results of continuous variables were expressed as medians and ranges (in parentheses) unless specified otherwise. The differences in BNP levels at different time points were tested using the Friedman test. If an overall statistically significant difference was found, individual time points were compared with the corresponding previous time points using the Wilcoxon signed-rank test, to explore the effect of ECMO support. Continuous variables, including BNP levels between survivors and nonsurvivors, were compared using the Mann-Whitney U test. Bonferroni's adjustment was applied for repeated measurement. A p value less than 0.05 was considered significant. Statistical analyses were performed using SPSS for Windows version 11.5 (SPSS Inc, Chicago, IL).


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
Demographic Data
During the study period, 15 pediatric patients were enrolled. The demographic and ECMO data are summarized in Table 1. The ECMO indications included failure to wean from cardiopulmonary bypass (n = 6), cardiac arrest and cardiopulmonary resuscitation (n = 5), profound cardiogenic shock after cardiac surgery (n = 2), neonatal fulminant myocarditis (n = 1), and glycogen storage disease type 1 with septic shock (n = 1). The median ECMO duration was 68 hours (range, 29 to 432) hours.


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  		Table 1. Clinical Patient Information
 
Twelve patients (80%) were weaned off ECMO, 1 patient (patient 1) underwent orthotopic heart transplantation and survived, and ECMO was withdrawn from 2 patients (patients 10 and 14) at their families' request because of anticipated poor outcome. Among the 12 patients who were weaned off ECMO, 8 survived to hospital discharge. Four patients died of progressive heart failure 4, 7, 23, and 52 days after removal of ECMO. The overall survival rate of this cohort was 60% (9 of 15 patients). All the survivors are currently alive, except for 1 patient who died of a pulmonary infection after the second-stage operation (bidirectional Glenn shunt). The flow diagram for patient outcomes is depicted in Figure 1.


Figure 1
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  		Fig 1. Outcomes of 15 patients supported by extracorporeal membrane oxygenation (ECMO).

 
Condition Before Extracorporeal Membrane Oxygenation
Before the start of ECMO, all patients received inotropic agent infusions, and their blood lactate levels were markedly elevated (median, 12.6 mmol/L; range, 3.7 to 35.7 mmol/L). Five patients received ECMO during cardiac massage; heart rhythms consisted of ventricular fibrillation in 2 (patients 1 and 7) and bradycardia or asystole in 3 (patients 9, 11, and 13).

B-Type Natriuretic Peptide Results
The BNP levels were significantly elevated before ECMO initiation (t1) at a median of 1,430 pg/mL (range, 361 to 5,000) pg/mL. After ECMO support, the BNP levels declined to a median of 558 pg/mL (range, 189 to 2,610) pg/mL before the weaning process began (t2). Among the patients who were weaned from ECMO (t3, n = 12), the median BNP level was 1,880 pg/mL (range, 278 to 5,000 pg/mL). The differences between the BNP levels at the different times were significant (t1, t2, t3, t4; p = 0.016).

Analysis using the paired Wilcoxon signed-rank test showed that the BNP levels decreased after ECMO support (t2 minus t1, p = 0.006) and elevated after removal of ECMO (t3 minus t2, p = 0.045).

B-Type Natriuretic Peptide, Clinical Variables, and Outcomes
Excluding the patient who was bridged to heart transplantation, the BNP values of the 9 survivors and the 5 nonsurvivors were compared. The data are presented in Figure 2. B-type natriuretic peptide levels were higher in the nonsurvivors at t2, t3, and t4 (p = 0.02, 0.016, 0.017, respectively).


Figure 2
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  		Fig 2. The trends of B-type natriuretic peptide (BNP) in survivors and nonsurvivors. The solid line with open circles represents survivors, and the dotted line with open triangles represents nonsurvivors. t1: before initiation of extracorporeal membrane oxygenation, t2: during extracorporeal membrane oxygenation support and before start of extracorporeal membrane oxygenation weaning, t3: the day after removal of extracorporeal membrane oxygenation, and t4: 4 days after removal of extracorporeal membrane oxygenation. (*Significant difference among survivors and nonsurvivors.) The vertical bar represents the range.

 
The blood pressure, urine output, lactate levels, and central venous pressure before and after weaning from ECMO (t2 and t3) were tested for association with the outcome, and the results are summarized in Table 2. Although the differences in BNP levels at these points reached statistical significance, the other clinical variables, such as blood pressure, central venous pressure, lactate level, and urine amount, did not.


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  		Table 2. Clinical Variables of Survivors and Nonsurvivors a
 
Postcardiotomy Subgroup
Among the 11 patients who had cardiac surgery, excluding the 1 withdrawn from ECMO support, 10 were weaned ECMO. The median ECMO duration was 65 hours (range, 29 to 190 hours). The BNP levels of the survivors (n = 6) and nonsurvivors (n = 4) did not differ significantly before weaning from ECMO (t2). On the next day after removal of ECMO (t3), the nonsurvivors had higher BNP levels (median, 3,685 pg/mL; range, 2,494 to 5,000 pg/mL) than the survivors (median, 1,735 pg/mL, 108 to 3,030 pg/mL; p = 0.038). Four days after removal of ECMO (t4), the nonsurvivors (n = 3) had higher BNP levels (median, 3,900; range, 3,230 to 5,000 pg/mL) than the survivors (median, 534; range, 108 to 890 pg/mL; p = 0.024).

B-Type Natriuretic Peptide Cutoff Value Among Survivors and Nonsurvivors
For patients with BNP levels of greater than 2,000 pg/mL after weaning from ECMO (t2), we found that 1 day after removal of ECMO (t3), 80% (4 of 5) of the patients with BNP levels greater than 2,000 pg/mL died, and all patients (n = 7) with BNP levels less than 2,000 pg/mL survived. Four days after removal of ECMO (t4), all the survivors (n = 7) had BNP levels of less than 2,000 pg/mL in contrast to the patients with BNP levels greater than 2,000 pg/mL (n = 3) who all died later.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
This study demonstrated that serial BNP determinations can be applied in pediatric patients supported with ECMO to be used as a factor to predict clinical outcome. Blood BNP level is a valuable diagnostic tool for use among adult cardiac patients because of its rapid turnaround time and sensitivity [11, 12]. Although its clinical use in pediatric patients is limited to fewer and smaller series of patients, elevated BNP levels are associated with ventricular dysfunction and help in the diagnosis of heart failure [13, 14]. However, there are rare reports about BNP levels for pediatric patients during mechanical support. We reported the use of BNP levels during ECMO support in pediatric patients.

In adult patients, left ventricular assist devices unload the left ventricle, improve ventricular morphology, and alter gene expression, so that BNP levels are decreased [15]. In this report, we found that BNP levels decreased as well after ECMO support (t1 to t2). This phenomenon was not reported among children before. The decreased BNP levels are possibly related to mechanical unloading of the heart by ECMO [16, 17] and the recovery process after cardiac surgery [18].

The early decrease in BNP level is suggested as indicative of recovery of ventricular function during mechanical circulatory support by Sodian and colleagues [6], but only 4 patients could separate from ventricular assist devices in their study. In our study, we found that the BNP levels increased again after removal of ECMO (t3 minus t2), which implies increased ventricular loading and incomplete normalization of cardiac function after separation from mechanical support.

Although cardiac ECMO is used more and more in pediatric patients, the overall survival remains about 30% to 40% [19, 20]. In the large studies by Kolovos and associates [21] and Morris and coworkers [22], 26% to 33.8% of the ECMO-weaned patients still died in the intensive care unit. In our series, 33% (4 of 12) of the patients died after weaning from ECMO. We found that these nonsurvivors had higher BNP levels and died despite initially acceptable hemodynamic data after weaning from ECMO. The high BNP levels (t3, t4) provide additional information to the blood pressure, urine output, and blood lactate levels, which were shown to be a prognostic marker during ECMO [23]. We believe that the high BNP levels indicate that patients are still in severe cardiac failure, even if their condition has improved enough to separate them from ECMO. Although we cannot offer an absolute level above which no patient survived because of the limited size of the cohort studied, we found that patients with BNP levels of greater than 2,000 pg/mL (at t3 and t4) had a very poor prognosis, and those patients may require further aggressive therapy, including additional mechanical circulatory support.

The measurement of blood BNP levels can be easily performed in virtually all patients. The short half-life of BNP could make the daily monitoring of heart failure therapy feasible, and the application of BNP for monitoring the treatment in chronic heart failure shows promising results [24, 25]. In adult patients with acute decompensated heart failure, serial measurement of BNP levels could provide incremental prognostic information over clinical presentation and repetitive echocardiographic examinations in patients with acute decompensated heart failure [26].

In our study, the BNP levels changed during the peri-ECMO period, which may reflect the severity of cardiac failure and the change in the acute stage. After removal of ECMO, the survivors trended toward lower BNP levels whereas the nonsurvivors had persistently rising BNP levels (Fig 2). We think the difference in the trends implies the potential usefulness of BNP for monitoring the effectiveness of heart failure therapy in the intensive care unit setting.

The timing and criteria for weaning off ECMO still lack standard guidelines. Among our patients, the higher BNP levels were noted in the nonsurvivors (at t2, t3, and t4). Although the decision to wean from ECMO should not depend on a single factor, BNP levels might be useful as a reference guide to wean pediatric patients off ECMO or to put them on the waiting list for transplantation if the BNP level is persistently high under adequate therapy.

Limitations
The small number of patients included in this study constitutes a major limitation to the applicability BNP to clinical practice. The heterogeneity of the patients' diagnoses precluded detailed analyses of given specific conditions, which is a common problem in studies of pediatric congenital heart surgery and mechanical support. The lactate levels and urine output were not significantly different among the survivors and nonsurvivors in this study; this is likely owing to ß error because of the small sample size. In addition to the BNP, there are still many biomarkers being investigated for heart failure, which are not addressed in this study [27].

Conclusion
The BNP levels showed a dynamic change during therapy with ECMO in pediatric patients. High BNP levels were associated with a poor outcome. We believe that BNP is a potentially good marker to monitor pediatric patients treated with ECMO for cardiac failure.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
This study was partly supported by the grant of NSC 94-2314-B-002-121 Taiwan and NTUH 94M20, 94N30 grant.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

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