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Ann Thorac Surg 2007;84:537-543
© 2007 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Brain Natriuretic Peptide as Noninvasive Marker of the Severity of Right Ventricular Dysfunction in Chronic Thromboembolic Pulmonary Hypertension

Herre J. Reesink, MDa, Igor I. Tulevski, MD, PhDb, J. Tim Marcus, PhDd, Frans Boomsma, PhDf, Jaap J. Kloek, MDc, Anton Vonk Noordegraaf, MD, PhDe, Paul Bresser, MD, PhDa,*

a Department of Pulmonology of the Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands
b Department of Cardiology of the Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands
c Department of Cardiothoracic Surgery of the Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands
d Department of Physics and Medical Technology, The Free University Medical Center, Amsterdam, the Netherlands
e Department of Pulmonology, The Free University Medical Center, Amsterdam, the Netherlands
f Department of Internal Medicine, Erasmus Medical Center, Rotterdam, the Netherlands

Accepted for publication April 2, 2007.

* Address correspondence to Dr Bresser, Academic Medical Center, University of Amsterdam, Department of Pulmonology, F5-144, PO Box 22700, Amsterdam, 1100 DE, the Netherlands (Email: p.bresser{at}amc.uva.nl).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: Right ventricular (RV) dysfunction is associated with increased morbidity and mortality in patients with chronic thromboembolic pulmonary hypertension (CTEPH) who undergo pulmonary endarterectomy (PEA). We studied whether plasma brain natriuretic peptide (BNP) levels can be used to identify RV dysfunction in CTEPH patients. Therefore, plasma BNP levels were studied in relation to cardiac remodeling and function as determined by cardiac magnetic resonance imaging (MRI).

Methods: Thirty-eight patients with CTEPH (55 ± 15 years), and ten healthy controls (46 ± 15 years) were studied. The BNP was determined by an immunoradiometric assay.

Results: The CTEPH patients had a mean pulmonary artery pressure of 49 ± 13 mm Hg, cardiac index 2.1 ± 0.7 l · min–1 · m–2, and pulmonary vascular resistance of 867 ± 432 dynes · s · cm–5. In CTEPH patients, compared with controls, right ventricular (RV) remodeling was demonstrated. In the patients, BNP was increased and correlated (all p < 0.0001; Spearman rank test) with MRI parameters of RV remodeling and function: end diastolic (r = 0.71) and end systolic (r = 0.74) volumes, RV mass (r = 0.68), leftward ventricular septal bowing (r = –0.80) and ejection fraction (EF; r = –0.81). By receiver operating curve analysis, BNP levels of 11.5 picomole (pmol)/L and 48.5 pmol/L, respectively, detected RV dysfunction as defined by RVEF less than 0.45 and less than 0.30, respectively, with high sensitivity and specificity. Hemodynamically, BNP levels greater than 48.5 pmol/L identified the most severely affected patients.

Conclusions: In CTEPH patients, BNP levels correlate with RV remodeling and can be used to identify RV dysfunction. Future studies are warranted on the role of BNP to identify "high risk" CTEPH patients and its relation to postoperative hemodynamic outcome, RV failure, and mortality.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Chronic thromboembolic pulmonary hypertension (CTEPH) results from incomplete resolution of the vascular obstruction caused by pulmonary thromboemboli [1]. If left untreated, prognosis in CTEPH is poor and proportional to the degree of pulmonary hypertension [2]. Advanced CTEPH leads to cardiac remodeling, including right ventricular (RV) dilatation and hypertrophy, tricuspid regurgitation, and leftward ventricular septal bowing, with consequent impact on cardiac function. As a result, death in most CTEPH patients is caused by progressive RV failure. Pulmonary endarterectomy (PEA) is the therapy of choice for patients with surgically accessible CTEPH [1, 3, 4]. This intervention, however, does not come without potential risk, with mortality figures ranging from 5% to 24% of operated cases [1]. In these patients, preoperative RV dysfunction is associated with increased morbidity and mortality [5–7]. Better preoperative identification of RV dysfunction and subsequent preoperative medical treatment may improve postoperative outcome [8–10].

Magnetic resonance imaging (MRI) is a highly accurate method to quantify RV function and dimensions in CTEPH patients [11] and is an accepted tool for the assessment of RV function and remodeling [12, 13]. Cardiac MRI, however, is not part of a routine work-up in CTEPH patients; it requires specific expertise, is time consuming, and expensive. Thus, a noninvasive parameter that can identify patients with RV dysfunction is desirable.

Plasma brain natriuretic peptide (BNP) is a natriuretic hormone secreted by the cardiac ventricles in response to stretch [14]. The BNP levels were demonstrated to be increased in left [15, 16] and right [17–19] ventricular heart disease. In CTEPH, BNP levels were demonstrated to correlate with hemodynamic severity of disease [17, 20, 21].

The aim of the present study was to analyze whether BNP levels can be used to identify RV dysfunction in CTEPH patients. Therefore, we studied plasma BNP levels in relation to cardiac remodeling and function as determined by cardiac MRI.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Prospectively, we studied 38 out of 43 consecutive patients (18 male, median age 57, range 25 to 78 years) diagnosed with CTEPH, referred to the Academic Medical Center of the University of Amsterdam. Two patients refused to participate because of claustrophobia and three patients could not be included for logistical reasons. Diagnoses of CTEPH and cardiopulmonary hemodynamics were determined by pulmonary angiography and right heart catheterization [22]. Pulmonary hypertension was defined as mean pulmonary artery pressure (mPAP) greater than 25 mm Hg at rest or greater than 30 mm Hg during exercise. At inclusion in the study, no patient received specific medical treatment for pulmonary hypertension. All patients received oral anticoagulants for at least three months. Patients with renal insufficiency (creatinine >115 µmol · L–1), concomitant left-sided heart disease, uncontrolled systemic hypertension, or uncontrolled diabetes mellitus were excluded from the study. Coronary angiography was part of the preoperative work-up and routinely performed in all patients older than 50 years of age, and in patients older than 40 years of age if they had a history of smoking. Ten age-matched nonsmoking healthy volunteers (5 male; age 51; range, 27 to 60 years) served as controls.

In 32 patients included in this study, a PEA was performed. The PEA was performed according to the protocol of the University of California San Diego [1, 7, 13]. Five patients were considered to have distal, inoperable CTEPH. In one additional patient with exercise-induced pulmonary hypertension a PEA was postponed. Postoperative hemodynamic characteristics were determined on the first or second day after PEA, before removal of the Swan-Ganz catheter (Edwards LifeSciences, Irvine, CA). All patients and controls gave informed consent to the study protocol, which was approved by the local ethical committee.

MRI Measurement
The MRI was performed before PEA with a four-element body phased-array coil and a 1.5 T whole body system (Sonata; Siemens Medical Solutions, Erlangen, Germany). The MRI breath-hold cine imaging was electrocardiographically triggered, and performed in the cardiac short-axis view in a stack of parallel imaging planes covering the left and right ventricles from base to apex. A spoiled gradient echo sequence was used as specified by others [11]. From this stack of short-axis cine images, the RV and left ventricular (LV) volumes were calculated for each temporal frame in the cardiac cycle, using the MR Analytical Software System (Medis, Leiden, The Netherlands). The end-diastolic volume (EDV) and end-systolic volume (ESV) were assessed from the stack of parallel short-axis images, and ejection fraction (EF) and stroke volumes (SV) were subsequently calculated. The RV and LV myocardial masses were assessed from the stack of parallel short-axis images by manual detection of endocardial and epicardial borders on each slice, also using the MR Analytical Software System. Cardiac volume and mass were corrected for body surface area. Interventricular septal bowing was quantified by the curvature (defined as 1 divided by the radius of curvature in centimeters) as described previously [23]. Positive values of this curvature ratio denote (physiologic) rightward septal bowing, and negative values denote leftward ventricular septal bowing.

Blood Sampling and BNP Assay
Blood was obtained at rest in a horizontal position from the brachiocephalic vein for plasma (ethylenediamine-tetra-acetic acid), centrifuged at 3,000 rpm for 10 minutes at 4°C, and subsequently stored at –80°C until analysis. The BNP was determined with an immunoradiometric assay (ShionoRIA BNP; Shionogi Pharmaceutical, Osaka, Japan) [24].

Functional Classification
Each patient was functionally classified according to the modified New York Heart Association (NYHA) classification of the World Health Organization [25].

Statistical Analysis
Data are expressed as mean ± standard deviation, or as median (range), as indicated in the text. All calculations were performed with a statistical package (SPSS 11.5; SPSS Inc, Chicago, IL). The unpaired Student t test was used to test the difference between patients and controls. Univariate correlations between BNP levels and MRI parameters were analyzed with the Spearman rank correlation test, and were tested for two-sided significance. Subsequently, stepwise linear regression analysis was performed with the parameters, which showed a significant correlation. To further investigate the correlation between BNP levels and RV dysfunction a receiver operating characteristic (ROC) curve analysis was performed. The BNP cutoff value to detect RV dysfunction was chosen from the optimal combined sensitivity versus specificity relation. The RV dysfunction was defined as RV ejection fraction (EF) less than 0.45 measured by MRI; that is two standard deviations below the lower limit of mean RVEF of the healthy controls. To select CTEPH patients with the most severely compromised RV function, a ROC curve analysis was also performed for BNP and a RVEF less than 0.30. The patients were then divided into three groups according to whether the preoperative BNP level was below or above this cutoff point. Hemodynamic and functional characteristics between the groups were analyzed by the Kruskal-Wallis test. In case of an overall statistical difference, the differences between two groups were further analyzed using Mann-Whitney U test.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Patient Characteristics
Hemodynamic characteristics of the patients are summarized in Table 1. Most patients suffered from moderate to severe pulmonary arterial hypertension with a median mPAP of 46 mm Hg (range, 20 to 75), a median cardiac index (CI) of 2.00 L · min–1 · m–2 (range, 1.20 to 4.40), and a median pulmonary vascular resistance (PVR) of 863 dynes · s · cm–5 (range, 114 to 1,748). Coronary artery disease was not present in any of the patients studied.


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  		Table 1 Baseline Characteristics of Chronic Thromboembolic Pulmonary Hypertension Patients
 
MRI Analysis
In the CTEPH patients compared with the healthy controls (Table 2), RVEDV and RVESV were increased, whereas SV and EF were decreased. The RV dysfunction (EF < 0.45) was present in 27 (71%) patients. Severe RV dysfunction (EF < 0.30) was present in 16 patients (42%). Moreover, RV mass and interventricular septal bowing differed significantly between patients and controls (Table 2). In the CTEPH patients, LVEDV was significantly decreased compared with controls, whereas LVESV did not differ. As a consequence, LVSV and LVEF were significantly lower in patients as compared with controls.


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  		Table 2 Magnetic Resonance Imaging Characteristics of Chronic Thromboembolic Pulmonary Hypertension Patients and Healthy Controls
 
BNP Levels and Right Ventricular Remodeling
Plasma BNP levels in CTEPH patients were increased compared with the controls (53 ± 51 pmol/L vs 3 ± 2 pmol/L, p < 0.0001). The BNP levels correlated significantly with all parameters reflecting RV remodeling; ie, EDV and ESV, RV mass, and septal bowing (Table 3). In contrast, BNP levels did not correlate with any parameter of LV function (Table 3).


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  		Table 3 Correlations Between Brain Natriuretic Peptide Levels and Parameters of Right Ventricular Remodeling in Chronic Thromboembolic Pulmonary Hypertension Patients (n = 38)
 
Moreover, BNP levels also correlated with hemodynamic parameters reflecting the severity of the pulmonary hypertension (Table 4).


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  		Table 4 Correlations Between BNP Levels and Hemodynamic Parameters in Chronic Thromboembolic Pulmonary Hypertension Patients (n = 38)
 
BNP Levels and Severity of Right Ventricular Dysfunction
The BNP levels also inversely correlated with RVEF (Fig 1). By stepwise linear regression analysis, RVEF and LV septal bowing were shown to be independently associated with BNP levels (model: r2 = 0.574; RVEF: beta = –0.444; leftward ventricular septal bowing: beta = –0.363; p < 0.0001). By ROC analysis (Fig 2A), a BNP level of 11.5 pmol/L was shown to detect RVEF less than 0.45 with a sensitivity and specificity of 89% and 100%, respectively. By ROC analysis (Fig 2B), a BNP level of 48.5 pmol/L was shown to detect RVEF less than 0.30 with a sensitivity and specificity of 88% and 86%, respectively.


Figure 1
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  		Fig 1. Correlation between brain natriuretic peptide (BNP) levels and right ventricular ejection fraction (RVEF); Spearman r = –0.81, p < 0.0001. Dashed lines on the x axis indicate RVEF of 0.45 and 0.30, respectively. Dashed lines on the y axis indicate BNP levels of 48.5 and 11.5 pmol/L, respectively, as obtained from the receiver operating characteristic curve analysis (see Fig 2).

 

Figure 2
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  		Fig 2. Receiver operating characteristic curves of plasma brain natriuretic peptide (BNP) levels to predict right ventricular dysfunction as defined by ejection fraction 0.45 (A), and 0.30 (B). (AUC = area under the curve.)

 
Hemodynamic and RV functional characteristics of the three groups of patients (ie, BNP < 11.5 pmol/L, BNP 11.5 – 48.5 pmol/L, and BNP > 48.5 pmol/L, are summarized in Tables 5 and 6. Go Hemodynamic severity of disease, as well as the level of impairment of RV function (MRI), differed significantly among the three groups of patients. In contrast, MRI parameters of LV function did not differ among the three groups (Table 6).


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  		Table 5 Clinical and Hemodynamic Characteristics for BNP Ranges According to Receiver Operating Characteristic Curve Analysis
 

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  		Table 6 Magnetic Resonance Imaging Characteristics for BNP Ranges According to Receiver Operating Characteristic Curve Analysis
 
Patients with BNP greater than 48.5 pmol/L not only represented patients with severely impaired RV function, but also the patients with the most severe pulmonary hypertension (Table 5). In these patients, also RV remodeling (ie, RV dilatation and hypertrophy and the degree of leftward ventricular septal bowing) was by far most pronounced (Table 6).

Outcome After Pulmonary Endarterectomy
Postoperative hemodynamic outcome in the three groups of patients is summarized in Table 7. Patients with BNP less than 11.5 pmol/L had an excellent hemodynamic outcome; that is, mPAP normalized in all patients. In contrast, 11 out of 14 patients with BNP greater than 48.5 pmol/L had (by definition) residual pulmonary hypertension (mPAP > 25 mm Hg; range, 26 to 55 mm Hg), of whom six had a mPAP greater than 30 mm Hg. In addition, in this group three patients died postoperatively, two of progressive right heart failure caused by persistent pulmonary hypertension and one of postoperative massive alveolar hemorrhage. Patients with BNP levels between 11.5 and 48.5 pmol/L had an intermediate hemodynamic outcome (Table 7).


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  		Table 7 Preoperative and Postoperative Hemodynamic Characteristics for the Patients (n = 32) With Chronic Thromboembolic Pulmonary Hypertension
 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
This is the first study in CTEPH patients, that demonstrated that plasma BNP levels correlated with parameters of RV remodeling and dysfunction as assessed by cardiac MRI. Moreover, we demonstrated that BNP may serve as a noninvasive marker to identify RV dysfunction in CTEPH patients prior to pulmonary endarterectomy.

In the present study, BNP levels correlated strongly with all parameters reflecting the severity of RV remodeling. Moreover, by ROC curve analysis, BNP greater than 11.5 pmol/L was demonstrated to be highly sensitive and specific to identify CTEPH patients with RV dysfunction. Plasma BNP levels, in relation to RV remodeling and dysfunction as determined by cardiac MRI, were not studied before. The potential usefulness of BNP as a noninvasive marker of RV dysfunction has been demonstrated before in patients with acute pressure overload due to acute pulmonary embolism [26, 27]. In patients suffering from chronic RV volume and (or) pressure overload, the correlation between BNP levels and RV dysfunction was studied before using electron beam computed tomography [17]. In CTEPH, Nagaya and colleagues [21] demonstrated that BNP levels correlated with the hemodynamic severity of disease and could be used postoperatively to asses the efficacy of PEA.

Based upon the present observations, increased BNP levels can be used to identify CTEPH patients with RV dysfunction. A BNP greater than 48.5 pmol/L detected severe RV dysfunction (EF < 0.30) with high sensitivity and specificity. Hemodynamically and clinically, this group of patients also represented the most severely affected patients. It has been demonstrated before [6, 7] that after PEA these patients (ie, mPAP > 50 mm Hg, cardiac index (CI) < 2.0 L · min · m–2, PVR > 1000 dynes · s · cm–5, and [or] NYHA class IV disease) are at risk for hemodynamic instability, progressive RV failure, and death after PEA. It is of major importance to identify these patients prior to PEA. Because cardiac dysfunction cannot be reliably assessed by right heart catheterization, BNP might serve as an additional noninvasive parameter to better identify these "high-risk" patients prior to surgery. Currently, in the work-up for PEA, the best test routinely used to predict outcome is to match the degree of hemodynamic severity of disease (ie, mPAP and PVR), with the degree of the angiographic pulmonary obstruction.

Although based upon the present observations, BNP appears a useful, noninvasive parameter to identify patients with RV dysfunction; however, in fact, its usefulness in daily clinical practice still needs to be proven. This study was not designed to study BNP levels in relation to postoperative hemodynamic outcome, RV failure, or mortality. Most of the clinically more severely affected patients were treated preoperatively while waiting for surgery with epoprostenol, bosentan, and (or) sildenafil. Neither the BNP level nor the MRI parameters of RV function were known at the time this treatment was initiated. Despite these obvious limitations, hemodynamic outcome differed significantly among the three groups of patients. Moreover, postoperative deaths were observed in the most severely affected patients; that is, patients with BNP greater than 48.5 pmol/L, only. Taken together, these observations support the notion that preoperative BNP levels can be used as a tool for risk stratification of CTEPH patients prior to PEA.

The BNP levels may be influenced by rhythm irregularities, left heart disease, renal insufficiency, and hypoxemia. However, all patients studied had sinus rhythm, did not suffer from concomitant left heart disease, and none had renal insufficiency. We identified 11 patients with arterial oxygen saturation below 90%; however, oxygen saturation did not differ among the three groups of patients.

In conclusion, we demonstrated that plasma BNP correlates with parameters of RV remodeling and can be used to identify RV dysfunction in CTEPH patients. Our observations warrant future studies in a larger number of patients on the usefulness of preoperative BNP levels to identify RV dysfunction in high-risk CTEPH patients and their relation to postoperative hemodynamic outcome, RV failure, and mortality.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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