Ann Thorac Surg 2006;82:983-988
© 2006 The Society of Thoracic Surgeons
Original article: Cardiovascular
Brain Natriuretic Peptide and Magnetic Resonance Imaging in Tetralogy With Right Ventricular Dilatation
Ali Dodge-Khatami, MD, PhDa,*,
Emanuela Valsangiacomo Büchel, MDb,
Walter Knirsch, MDb,
Alexander Kadner, MDa,
Valentin Rousson, PhDc,
Hitendu H. Dave, MDa,
Urs Bauersfeld, MDb,
René Prêtre, MDa
a Division of Congenital Cardiovascular Surgery, Zürich, Switzerland
b Division of Cardiology, University Children's Hospital, University of Zürich, Zürich, Switzerland
c Division of Biostatistics, University of Zürich, Zürich, Switzerland
Accepted for publication March 14, 2006.
* Address correspondence to Dr Dodge-Khatami, University Children's Hospital, University of Zürich, Steinwiesstrasse 75, CH-8032 Zürich, Switzerland (Email: ali.dodge-khatami{at}kispi.unizh.ch).
Presented at the Poster Session of the Forty-second Annual Meeting of The Society of Thoracic Surgeons, Chicago, IL, Jan 30–Feb 1, 2006.
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Abstract
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BACKGROUND: Cardiac volumetry by magnetic resonance imaging can guide the timing for reoperation in minimally symptomatic or asymptomatic patients with pulmonary insufficiency after corrected tetralogy of Fallot. Pro-brain natriuretic peptide (BNP) is a marker of ventricular dysfunction and wall stress, and levels may complement magnetic resonance imaging in cardiac assessment before and after pulmonary valve replacement.
METHODS: Between May 2004 and October 2005, 23 consecutive patients with corrected tetralogy, severe pulmonary insufficiency, and right ventricular end-diastolic volume index greater than 150 mL/m2 underwent elective pulmonary valve replacement. Plasma proBNP levels and magnetic resonance imaging were obtained before and 6 months after pulmonary valve replacement.
RESULTS: There was no surgical mortality or morbidity. Preoperative right ventricular end-diastolic volume index correlated with pulmonary insufficiency, and inversely so with left ventricular ejection fraction, reflecting interventricular interaction. Preoperatively (r = –0.47) and 6 months postoperatively (r = –0.54), log BNP was inversely correlated with right ventricular ejection fraction. Mean preoperative proBNP levels, right ventricular end-diastolic volume index, and pulmonary insufficiency significantly (p < 0.0001) diminished 6 months after pulmonary valve replacement (231 versus 114 ng/L, 184 versus 109 mL/m2, and 44% versus 2%, respectively).
CONCLUSIONS: Plasma proBNP is elevated in patients with corrected tetralogy, severe pulmonary insufficiency, and right ventricular dilatation, and it significantly diminishes 6 months after pulmonary valve replacement, mirroring magnetic resonance imaging-documented better right ventricular ejection fraction and smaller right ventricular end-diastolic volume index. Pro-brain natriuretic peptide complements magnetic resonance imaging for cardiac assessment in patients requiring pulmonary valve insertion. Future validation of cutoff levels are required to establish proBNP as a useful diagnostic and follow-up tool in patients with chronic pulmonary insufficiency and failing right ventricles.
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Introduction
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An increasing number of patients with tetralogy of Fallot are surviving into adolescence and adulthood with a satisfactory quality of life, late after complete correction [1]. Although a vast majority of patients are minimally symptomatic or even asymptomatic and without medication, residual lesions or ongoing cardiac deterioration are frequent, most commonly from pulmonary valve insufficiency (PI) and progressive right ventricular (RV) dilatation [1, 2]. Chronic and severe PI is secondary to various reconstruction techniques of the RV outflow tract during initial complete repair, namely transannular patching, excessive pulmonary valve commissurotomy, or pulmonary conduit failure [3]. Untreated, PI leads to volume overload of the RV, to diminished RV ejection fraction (RVEF) [4], and eventually to dilatation and failure of the right ventricle [5], which alarmingly, may be present in minimally symptomatic or asymptomatic patients. The development of life-threatening arrhythmias and the risk of sudden death are of major concern in these patients [6, 7], and form the impetus to insert a competent pulmonary valve to halt the progression of RV deterioration [2, 7] and to reduce the risk of sudden death [6]. However, the timing for such an undertaking is still controversial, especially in asymptomatic patients [2, 8].
Brain natriuretic peptide (BNP) is a neurohormone secreted mainly by the cardiac ventricles, in response to both volume and pressure overload [4, 9]. Besides having diuretic, natriuretic, and vasodilator activities, it inhibits the renin-angiotensin-aldosterone axis, and has been used as a marker of left ventricular overload [10–12]. Its precise role in indicating RV failure is not established, although there is evidence that BNP levels are elevated in states of acute and chronic RV pressure overload [4, 13]. It is released as a prohormone (proBNP) and is cleaved into a biologically active C-terminal fragment and an inactive N-terminal fragment. N-terminal proBNP has a longer plasma half-life and a higher serum concentration, is more stable in vitro, and can be measured more rapidly than BNP [14], making it a more reliable and practical laboratory value to measure.
In this study, we prospectively tested the hypothesis that proBNP levels are elevated in the presence of a dilated right ventricle from chronic PI, before the right ventricle fails, in minimally symptomatic or asymptomatic patients after corrected tetralogy of Fallot. Furthermore, we searched for evidence of regression or normalization of proBNP levels after repeat surgery to insert a competent pulmonary valve. Using cardiac magnetic resonance imaging (MRI) volumetry and an RV end-diastolic volume index (RVEDVI) cutoff greater or equal to 150 mL/m2, our group has shown the benefit in early insertion of a competent pulmonary valve to restore RV dimensions in asymptomatic or minimally symptomatic patients with chronic PI [2, 8]. These same criteria were used when enrolling patients for the current study.
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Patients and Methods
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Permission to proceed with this prospective study of a consecutive series of patients was granted by our institutional review board (May 17, 2004), and informed consent was obtained from all patients or parents of minors. Between May 2004 and October 2005, 23 consecutive patients with minimal or no symptoms after corrected tetralogy, with severe PI and right ventricular dilatation, underwent pulmonary valve replacement (PVR). A prior palliative Blalock-Taussig shunt was performed in 7 patients. The median age at initial complete correction of tetralogy of Fallot was 19 months (range, 4 to 55 months). Repairs included a transannular patch in 14 patients (5 with a Gore-Tex monocusp valve; W. L. Gore & Assoc, Flagstaff, AZ), a pulmonary homograft in 6 patients, a pulmonary valve-sparing commissurotomy in 2 patients, and an aortic homograft in 1 patient. Median age at redo surgery for insertion of a competent pulmonary valve was 13.2 years (range, 5.3 to 19.6 years), making the median interval between complete correction and reoperation 11.5 years (range, 1.8 to 15.7 years). As part of our institutional policy, an MRI finding of an RVEDVI greater or equal to 150 mL/m2, regardless of symptoms, is an indication for elective PVR. Four patients presented with combined PI and moderate RV outflow tract or pulmonary artery stenosis (maximum systolic gradient of 60 mm Hg). All patients underwent a preoperative cardiac MRI investigation, and 16 patients had a postoperative MRI control at 6 months after PVR. Magnetic resonance imaging was not performed in 2 patients owing to indwelling pacemaker systems, 1 patient lives abroad, and 4 patients are still awaiting their 6-month control MRI. Chronologically corresponding to MRI data collection, plasma proBNP was measured in all patients preoperatively, and in 18 patients at 6 months postoperatively. In 13 patients we obtained intermediate proBNP levels at 1 month postoperatively, concomitant to routine echocardiography.
Surgical Technique
Before repeat sternotomy, all patients were put on cardiopulmonary bypass through right iliac vessel cannulation, with limb cooling to 16°C. Surgery on the RV outflow tract, including valve replacement with right ventricle–pulmonary artery conduit insertion with or without pulmonary artery enlargement plasty, was performed at normothermia on a beating heart. Valved right ventricle–pulmonary artery conduits included a bovine jugular vein graft (n = 15, sizes 20 and 22 mm; Contegra, Medtronic, Minneapolis, MN), Shelhigh porcine conduits (n = 5, sizes 23 and 25 mm), cryopreserved pulmonary homografts (n = 2, sizes 20 and 22 mm), and 1 patient in whom the native pulmonary valve was recyclable and reconstructed to a competent bicuspid valve. Postoperatively, prophylactic acetylsalicylic acid (3 to 5 mg/kg per day orally) was given to all patients for 6 months.
Pro-Brain Natriuretic Peptide Measurement
Preoperatively and at 6 months postoperatively, 3 mL of heparinized venous blood was taken from each patient, with the study participants in a supine position for at least 20 minutes. Blood samples were centrifuged at 3,500 x g for 10 minutes at 4°C immediately after collection, and plasma was separated for N-terminal proBNP assay determination (Roche Diagnostics, Mannheim, Germany). Normal values using this assay for male and female patients younger than 50 years of age are 84 ng/L and 155 ng/L, respectively [14].
Cardiac Magnetic Resonance Image Acquisition
Magnetic resonance imaging studies were performed with a 1.5-T system (Signa MR/I Echo Speed; General Electric Medical Systems, Milwaukee, WI), by using a phased-array cardiac coil. The cardiac magnetic resonance protocol included cine steady-state free precession sequences (Time Echo [TE] minimum, flip angle 45 degrees, bandwidth 125 kHz, matrix 224 x 224, number of excitations 1, field of view 30 to 45 cm, slice thickness 6 to 8 mm with 1- to 2-mm gap depending on the body size, retrospective gating with 20 images reconstructed per cardiac cycle) in the axial plane for evaluation of the anatomy and in short-axis planes to assess the ventricular volumes. Velocity-encoded phase-contrast sequences (TE minimum, flip angle 15 degrees, matrix 256 x 128, bandwidth 31.25 kHz, views per segment 4 to 6 depending on the heart rate, number of excitations 1, slice thickness 4 mm, field of view adequate for patient's size and retrospective electrocardiographic gating, 20 phases per cardiac cycle) were performed for calculation of blood flow velocity and volume in the main pulmonary artery. The images were acquired during breath holding in all patients.
Ventricular volumes were measured from a multisection image set of 10 to 12 contiguous slices parallel to the plane of the atrioventricular valves (ventricular short axis), covering the full length of both ventricles. The ventricular volumes were calculated with the MASS software package (Magnetic Resonance Analytical Software System version 4.0, MEDIS Medical Imaging Systems, Leiden, the Netherlands). The endocardial contours were traced manually as previously described [15]. The RV ejection fraction was calculated as RV end-diastolic volume – RV end-systolic volume / RV end-diastolic volume. An RV ejection fraction higher than 0.50 was considered as normal. Flow data were analyzed with the FLOW V2.0 software package (MEDIS, Medical Imaging Systems, Leiden, the Netherlands) by tracing the contours of the main pulmonary artery in each time frame.
Statistics
Descriptive statistics with mean ± standard deviation were applied as appropriate. Box plots of the variable proBNP showed a clear nonnormal (asymmetric) distribution (Fig 1). Because statistical methods based on the normal distribution are more powerful than nonparametric methods, proBNP values were log-transformed to achieve a near-normal distribution (Fig 2). The other variables had an approximately normal distribution and were not transformed. All variables were compared before and 6 months postoperatively using a paired Student's t test. Relationships among the different variables before or after the operation were assessed using Pearson's correlation.
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Fig 1. Box plots of raw pro-brain natriuretic peptide levels preoperatively and at 6 months after pulmonary valve replacement. Values are from the 18 patients with a 6-month postoperative magnetic resonance imaging control. The hollow circle and asterisks represent outliers. (BNPpre = brain natriuretic peptide preoperatively; BNP6 = brain natriuretic peptide at 6 months.)
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Fig 2. Box plots of the logarithm of pro-brain natriuretic peptide (proBNP) levels preoperatively and at 6 months after pulmonary valve replacement. Values are from the 18 patients with a 6-month postoperative magnetic resonance imaging control. (BNPpre = brain natriuretic peptide preoperatively; BNP6 = brain natriuretic peptide at 6 months.)
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Results
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There was no surgical mortality or major morbidity. Mean absolute preoperative proBNP values were 231 ± 228 ng/L, diminishing to a mean of 183 ± 139 ng/L 1 month postoperatively, and to 114 ± 112 ng/L at 6 months after PVR. Mean preoperative log proBNP was 5.39 ± 0.81, and diminished to 5.03 ± 0.57 by 1 month (p < 0.06), and significantly to 4.33 ± 0.84 by 6 months postoperatively (p < 0.0001). Values are represented in a box plot with log transformation of proBNP values in Figure 2. The RVEDVI was elevated preoperatively at a mean of 184 ± 52 mL/m2, and diminished significantly to 109 ± 22 mL/m2 by 6 months (p < 0.0001; Fig 3). Pulmonary valve insufficiency, quantified by cardiac MRI as a regurgitation fraction, diminished significantly from a preoperative value of 44% ± 21%, to that of 2% ± 3% at 6 months postoperatively (p < 0.001). Pearson's correlation showed a correlation between preoperative RVEDVI and PI (r = 0.42; p = 0.05; Fig 4), and an inverse correlation with preoperative left ventricular ejection fraction (r = –0.39; p < 0.08; Fig 5). Neither PI nor left ventricular ejection fraction correlated strongly with RVEDVI at 6 months after surgery (r = 0.27; p < 0.4 and r = –0.22; p < 0.5, respectively). Preoperatively and 6 months postoperatively, log proBNP was inversely correlated with RVEF (r = –0.47; p < 0.03 and r = –0.54; p < 0.04, respectively; Figs 6, 7).
The correlations between log proBNP and RVEDVI were rather weak, both preoperatively and 6 months postoperatively (r = 0.10; p < 0.7 and r = 0.28; p < 0.3, respectively).
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Fig 3. Right ventricular end-diastolic volumes before and 6 months after pulmonary valve insertion. (RVEDVI pre = right ventricular end-diastolic volume index preoperatively; RVEDVI6 = right ventricular end-diastolic volume index at 6 months.)
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Fig 4. Preoperative right ventricular end-diastolic volume in relation to pulmonary valve insufficiency. (PI pre = pulmonary insufficiency preoperatively; RVEDVI pre = right ventricular end-diastolic volume index preoperatively.)
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Fig 5. Preoperative right ventricular end-diastolic volume in relation to left ventricular ejection fraction. (LVEF pre = left ventricular ejection fraction preoperatively; RVEDVI pre = right ventricular end-diastolic volume index preoperatively.)
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Fig 6. Preoperative logarithmic pro-brain natriuretic peptide (proBNP) values in relation to right ventricular ejection fraction. (RVEF pre = right ventricular ejection fraction preoperatively.)
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Fig 7. Logarithmic pro-brain natriuretic peptide (proBNP) values 6 months postoperatively in relation to right ventricular ejection fraction. (RVEF 6 = right ventricular ejection fraction at 6 months.)
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Comment
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Pulmonary valve insufficiency after corrected tetralogy of Fallot is increasingly recognized as a serious lesion, as the detrimental bystanders of RV dilatation, RV failure, and malignant arrhythmia influence long-term morbidity and survival [2, 6, 16]. It is generally accepted that in patients with RV failure, arrhythmia, or symptoms, PVR is indicated, and serves to halt the progression of RV volume overload and sudden death caused by arrhythmia [1, 6, 17]. Our group and others are advocating earlier reoperation for insertion of a competent valve before the onset of symptoms, although surgical timing remains controversial [2, 5–8, 17].
In a previous study [8], we reported MRI-documented restoration of RV dimensions 6 months after PVR in 39 patients with corrected tetralogy of Fallot, when redo surgery was electively performed at an RVEDVI of 150 mL/m2. From our encouraging surgical results, as well as the absence of mortality and major morbidity, we continued to perform PVR with the same cutoff value of 150 mL/m2 for the current study, and confirmed our earlier findings [8], namely that early insertion of a competent pulmonary valve significantly reduces RVEDVI, which will motivate us to continue on this RV-friendly path (Figs 6, 7).
In the extant pediatric literature, BNP levels have been measured both in healthy children and in those with congestive heart failure, although group numbers were relatively small, and different assay kits were used, each with different normal values [18–21]. Standardized values for each age group do not yet exist in the pediatric population, and if international norms are to be agreed on, they could still remain assay-dependent. Brain natriuretic peptide is a marker of ventricular dysfunction and wall-stress, and elevated levels have been measured in patients with chronic RV pressure overload [4, 12, 13, 21]. Brain natriuretic peptide has shown to be elevated in certain congenital heart defects, less so in univentricular hearts than biventricular hearts, and levels rise invariably in response to cardiopulmonary bypass [22, 23]. More specifically in children after repair of tetralogy of Fallot, Hayabuchi and colleagues [24] found elevated BNP levels, correlating with RV volume and systolic pressure, which decreased after infusion of dobutamine [24]. They found BNP concentration to reflect RV pressure and volume overload [24], although a cutoff point at which ventricular dysfunction was present was not defined.
We sought to measure BNP levels in patients with dilated right ventricles from chronic PI after complete repair of tetralogy of Fallot, and to examine the effect of PVR on BNP levels. Previously, we demonstrated that volume unloading of the right ventricle by inserting a competent pulmonary valve restored the dimensions of the RV, when performed in a timely fashion [2, 8]. We hypothesized that postsurgical normal RV volumes would be reflected in lower BNP levels. In the current study, we found that proBNP levels were invariably high in patients with a dilated RV from chronic PI. These values diminished already by 1 month after insertion of a competent pulmonary valve, and significantly so by 6 months postoperatively. As a corollary, RV end-diastolic volumes diminished in concert with reduced PI after PVR. Pro-brain natriuretic peptide levels and RVEDVI both diminished significantly after PVR, although the statistical correlation between the two variables, both preoperatively and at 6 months after PVR, was relatively weak. However, proBNP levels preoperatively and 6 months postoperatively showed a strong negative correlation with RVEF. Therefore, with regard to BNP levels, there exists a discrepancy between RV function and RV volume. As most of our patients were asymptomatic or minimally symptomatic before PVR, they represent the more favorable end of the spectrum of patients needing an intervention on the RV outflow tract. Although their right ventricles were clearly dilated, their function was maintained on the whole, if one looks only at ejection fraction percentages. However, myocardial viability studies were not performed, and we can only speculate that their myocardium was still functional, although dilated. With proven viability or an objective index of functioning myocardial mass, the negative correlation of BNP and RVEF would raise the following diagnostic question: could proBNP levels help to predict optimal timing for PVR in the face of RV dilatation, before deterioration of RV function? Interestingly, preoperative RVEDVI correlated inversely with left ventricular ejection fraction, although this inverse trend was no longer statistically significant at 6 months postoperatively. Through interventricular interaction through the shared common septum, inserting a competent pulmonary valve may not only spare the right ventricle from volume overload and allow for restoration of RV geometry, but could result in a flattened interventricular septum that no longer impedes left ventricular function.
In conclusion, early insertion of a competent pulmonary valve, in patients after corrected tetralogy of Fallot with chronic PI and a dilated right ventricle, will allow a significant reduction of RV size toward normalization. Pro-brain natriuretic peptide values are elevated in patients with chronic PI, before signs or symptoms of RV failure appear. Levels decrease already 1 month after PVR, and significantly diminish 6 months after redo surgery, parallel to volume unloading of the right ventricle. Preoperatively, the dilated right ventricle with a bulging interventricular septum encroaches on the left ventricle, as reflected by the inverse correlation between RVEDVI and left ventricular ejection fraction. Preoperative and postoperative proBNP values showed a strong negative correlation with RVEF, but had a weak statistical correlation with corresponding RVEDVI. The discrepancy between function and volume may suggest BNP as a useful marker in minimally symptomatic or asymptomatic patients with already dilated ventricles that still have maintained function, and could serve as an alarm signal to perform PVR before the onset of ventricular failure.
Although BNP is being increasingly established as one diagnostic tool among others that correlates with clinical functional class and exercise tolerance in patients with left ventricular distension and overload [25], it still needs to be validated as a marker of impending right heart failure in minimally symptomatic or asymptomatic patients, or as a helpful marker in the follow-up toward recovery after surgical intervention. Further prospective studies enrolling larger patient groups are needed, including symptomatic patients with viability-documented diminished ventricular function, to look at correlations between functional class, ventricular volume and function, myocardial viability, and proBNP levels, to stratify patients at risk of RV failure before intervention, and ventricular recovery after surgery. In the future, cutoff values of proBNP, like those of RVEF or RVEDVI, could help in the controversial timing of pulmonary valve insertion in asymptomatic patients with chronic PI and a dilating right ventricle, or in the follow-up of the patients after surgery, to monitor RV recovery.
A limitation of this study is that the study group is relatively small, and further power could be gained with larger numbers. The aggressive approach of performing early PVR with an RVEDVI cutoff point of 150 mL/m2 is based on our previous results [2, 8] and is supported by others [7, 16, 26]. However, one could argue that waiting longer in certain patients with similarly elevated proBNP values and even larger dilated right ventricles could still have led to significant reductions of both proBNP and RVEDVI 6 months postoperatively.
Normal proBNP values have not yet been standardized for the pediatric population on an international basis; they remain age and sex related, and vary according to the assay kit used. With the patients serving as their own controls through time by using the same assay kit before and 6 months after surgery, we merely illustrated the significant drop in levels before and after surgery. Although normal levels are defined by the manufacturer of the assay kit used in our study, it is still questionable to infer "normal" and "pathologic" proBNP levels with regard to RV size, or to determine cutoff levels corresponding to normally functioning or failing right ventricles.
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Abstract
Introduction
