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European Journal of Heart Failure 2008 10(6):573-580; doi:10.1016/j.ejheart.2008.04.003
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© 2008 European Society of Cardiology

Prognostic significance of tricuspid annular motion and plasma NT-proBNP in patients with heart failure and moderate-to-severe functional mitral regurgitation

Frank Lloyd Dinia,*, Paolo Fontanivea, Erica Panicuccia,b, Diana Andreinia, Piersilvio Chellaa and Salvatore Mario De Tommasia

a Unità Malattie Cardiovascolari 2, Santa Chiara Hospital Pisa, Italy
b Dipartimento di Patologia Sperimentale, Tecnologie Biomediche ed Epidemiologia, Università di Pisa Italy

* Corresponding author. Unità Operativa Malattie Cardiovascolari 2, Ospedale S. Chiara, Azienda Ospedaliera-Universitaria Pisana, Via Roma, 67-56126, Pisa, Italy. Tel.: +39 050 992355; fax: +39 050 993114. E-mail address: f.dini{at}ao-pisa.toscana.it


   Abstract
Top
 Abstract
1. Introduction
 2. Methods
 3. Results
 4. Discussion
 References
 
Background: The role of the right ventricle has been relatively neglected proportionate to its importance. We sought to evaluate the impact of right ventricular (RV) and NT-proBNP on the outcome of patients with heart failure (HF) and functional mitral regurgitation (MR).

Methods and patients: Outpatients with left ventricular (LV) systolic HF (ejection fraction [EF] ≤45%) and moderate-to-severe MR measured by a vena contracta width ≥0.5 cm were prospectively enrolled (n=142). Indexes of LV and RV function, including tricuspid annular plane systolic excursion (TAPSE), RV fractional area change and tissue Doppler RV acceleration at isovolumic contraction and NT-proBNP plasma levels were measured at the time of the index echocardiogram.

Results: Multivariate predictors of all-cause mortality included TAPSE<16 mm (hazards ratio [HR]: 2.64; p=0.009) and plasma NT-proBNP≥3283 pg/ml (HR: 2.58; p=0.011). TAPSE<16mm and plasma NT-proBNP≥3283 pg/ml added incremental prognostic information to LV EF≤25%, NYHA classes 3–4, coronary artery disease, elderly age and male sex. The 36-month Kaplan–Meier curve showed that survival was worst in the group with TAPSE<16 mm and NT-proBNP≥3283 pg/ml (p<0.0001).

Conclusion: This study demonstrates the significance of TAPSE and plasma NT-proBNP in predicting all-cause mortality in patients with systolic HF and moderate-to-severe functional MR.

Key Words: Dilated cardiomyopathy • Natriuretic peptides • Functional mitral regurgitation • Right ventricular function • Prognosis

Received November 28, 2007; Revised February 11, 2008; Accepted April 7, 2008


   1. Introduction
Top
 Abstract
 1. Introduction
2. Methods
 3. Results
 4. Discussion
 References
 
Many recent studies have reported an increased mortality in patients with heart failure (HF) and significant functional mitral regurgitation (MR) [1-3]. In such patients, the role of the right ventricle has been relatively neglected proportionate to its importance. In addition, only a few studies have attempted to further stratify HF patients with functional MR by means of clinical, echocardiographic and biochemical variables [4].

Prognostic stratification of patients with MR, organic or secondary to either ischaemic or non-ischaemic left ventricular (LV) dysfunction, has mainly been focused on the degree of MR severity and the functional assessment of the left ventricle [5,6]. Nevertheless, the association between a graded increase in MR severity and pulmonary hypertension in LV dysfunction suggests that right ventricular (RV) failure may play a role in determining the outcome of patients with HF and secondary MR [7]. Furthermore, plasma levels of natriuretic peptides, which have recently been shown to be remarkably and significantly higher in patients with concomitant RV dysfunction [8], may add to risk stratification, especially in subsets of HF patients with increased LV preload and backward transmission of elevated filling pressures.

Although it is of relevance, the clinical use of RV function is limited by difficulties in evaluation [9]. Assessment of RV performance from simple echocardiographic measurements and evaluation of plasma aminoterminal pro-type B natriuretic peptide (NT-proBNP) may be a useful method for stratifying patients with systolic HF and significant functional MR. Thus, the present study was designed to evaluate the prognostic significance of RV dysfunction and plasma NT-proBNP levels in patients with systolic HF and moderate-to-severe functional MR.


   2. Methods
Top
 Abstract
 1. Introduction
 2. Methods
3. Results
 4. Discussion
 References
 
2.1. Study patients
The study population was selected prospectively from consecutive patients referred to our Doppler and echocardiographic laboratory between April 2003 and June 2007 as a result of our Program for Heart Failure and Cardiomyopathies Screening and Management. Eligible patients had to have systolic HF due to either ischaemic or non-ischaemic dilated cardiomyopathy, LV ejection fraction (EF) ≤45%, LV end-diastolic volume index >75 ml/m2 and moderate-to-severe secondary MR at two-dimensional echocardiography. Echocardiographic exclusion criteria were insufficient image quality (n=6) and severe tricuspid regurgitation (n=4). Clinical exclusion criteria were: recent acute coronary syndromes (less than 3 months), cognitive disorders, haemodialysis therapy or coexisting malignant diseases. Thus, a total of 142 patients formed the final study population. Patients who fulfilled the entry criteria but without moderate-to-severe MR served as a control group (n=290).

2.2. Doppler echocardiographic examination
Transthoracic two-dimensional and Doppler echocardiographic examinations were carried out by an Acuson Sequoia C256 ultrasound instrument (Siemens, Mountain View, California) equipped with a 3.5-MHz transducer and harmonic imaging. Two-dimensional and Doppler imaging was performed in standard parasternal and apical views. LV end-diastolic and end-systolic volumes and EF were calculated from apical two- and four-chamber views using the modified Simpson's rule. LV volume indices and LV mass index were also calculated [10]. RV fractional area change was estimated according to a previously described formula [11]. Maximal left and right atrial end-systolic areas were measured from the apical four-chamber view. TAPSE was estimated by two-dimensional echo guided M-mode recordings from the apical four-chamber view with the cursor placed at the free wall side of the tricuspid annulus [12]. Patients with a moderate-to-severe MR were selected according to the vena contracta method [13]. The vena contracta width was measured at the narrowest portion of the MR jet as it emerged through the coaptation of the leaflets. Patients were considered to have moderate-to-severe MR if they had a vena contracta width ≥0.5 cm in the parasternal long-axis view [13]. Pulsed wave Doppler mitral velocity curves were obtained from the apical four-chamber view by positioning a 1-2 mm sample volume between the tips of the mitral valve leaflets in diastole. The following measurements were made from mitral velocity tracings: peak E diastolic wave velocity, peak A wave velocity and E wave deceleration time. Patients were defined as having LV restrictive filling if they had an E wave deceleration time <150 ms [14]. Patients with atrial fibrillation were defined as having restrictive filling if they had a deceleration time ≤120 ms [15]. From the 4-chamber view, the early diastolic (Em) velocities by Doppler tissue imaging (DTI) were recorded with the sample volume placed at the junction between LV wall (septal and lateral) and the mitral annulus. The ratio of mitral to septal myocardial early velocities (septal E/Em) as well as mean E/Em, averaged between septal and lateral annulus, were calculated. RV acceleration at isovolumic contraction was measured on DTI tracing dividing peak isovolumic contraction velocity by its acceleration time [16]. Estimates of tricuspid peak regurgitation velocity were recorded by continuous-Doppler. The estimated pulmonary artery systolic pressure was calculated as the sum of the trans-tricuspid gradient and the estimated right atrial pressure [17]. Finally, Doppler measurements in patients with atrial fibrillation were averaged over at least 5 beats to minimize the impact of cycle length.

2.3. Measurement of aminoterminal pro-type B natriuretic peptide
Venous blood samples were collected at the time of the index echocardiogram in EDTA-containing tubes. NT-proBNP was measured by an Elecsys 2010 analyzer (measuring range, 5 to 35,000 pg/ml) using a chemiluminescent immunoassay kit (Roche Diagnostics, Grenach-Wyhlen, Germany).

2.4. Follow-up data
For survival analyses, observation began on the date of the index Doppler echocardiogram. All-cause mortality was the primary end point of the study. The secondary (combined) end point was all-cause mortality or HF-related hospital admissions (i.e., hospitalisation for worsening HF, biventricular pacemaker implantation or mitral valve surgery). Survival data were obtained through follow-up of patients and verified through local authority registry and medical records.

2.5. Statistical analyses
Continuous data were expressed as mean±standard deviation. Continuous variables were compared between groups using an unpaired t test (for normally distributed variables) or Mann-Whitney and Kruskall-Wallis tests (for non-normally distributed variables). Chi squared test was used to determine categorical variable differences. Spearman rank correlation analysis was used to assess the relationships between Doppler echocardiographic variables and the log-transformed plasma NT-proBNP. A p value <0.05 was considered statistically significant. Survival curves were analyzed by the Kaplan-Meier method. Comparison of event rates among subgroups were tested by the log-rank test. The associations of dichotomous variables, either selected according to literature data: LV EF (≤/>25%) [18], restrictive filling [17], septal E/Em (>/≤15) [19], mean E/Em (>/≤12) [20] and RV fractional area change (</≥32%) [11], or median values: plasma NT-proBNP (≥/<3283 pg/ml), left atrial area (>/≤16 mm2/m2), pulmonary artery systolic pressure (≥/<45 mmHg), TAPSE (</≥16 mm) and acceleration at isovolumic contraction (≤/>2.7 cm/sec2) with outcome were assessed by using the Cox proportional hazard models. The following variables were analyzed as dichotomous and continuous variables: NT-proBNP, EDT, and EF. Variables showing a significant association with outcome (p<0.1) were included in the multivariate Cox forward stepwise model to determine which of them was independently related to the prognosis. Data were analyzed using the Statistical Package for the Social Sciences version 10.0 for Windows statistical software program (SPSS, Chicago, Illinois).


   3. Results
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
4. Discussion
 References
 
3.1. Patient characteristics
Significant MR, as assessed by a vena contracta width ≥0.5 cm, was present in all patients. Characteristics of the study patients are described in Tables 1 and 2. Severe LV diastolic dysfunction was very common in the study population, restrictive mitral flow occurred in 75% of patients (82% in patients with RV dysfunction and 69% in patients with preserved RV performance). Pseudonormal mitral flow, which was recognized using standard criteria including pulmonary vein flow, Valsalva manoeuvre and left atrial area, occurred in 8% of patients (12% in patients with RV dysfunction and 6% in patients with preserved RV performance).


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  		Table 1 Baseline demographic and clinical characteristics for patients grouped according to the tricuspid annular plane systolic excursion (TAPSE)

 


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  		Table 2 Baseline Doppler echocardiographic variables in patients grouped according to the tricuspid annular plane systolic excursion (TAPSE)

 
In patients with a vena contracta width ≥0.5 cm, median plasma NT-proBNP concentration was 3283±585 pg/ml (median±standard error). Patients with RV dysfunction (TAPSE<16 mm) showed higher NT-proBNP levels than patients with preserved RV performance (p<0.0001) (Table 1). The highest plasma concentrations of NT-proBNP were found in patients with TAPSE and LV EF below the median. Fig. 1 shows the box plot of the log-transformed NT-proBNP levels in the study groups categorized according to RV and LV performance.


Figure 01
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  		Fig. 1 Box plot of log-transformed NT-proBNP levels in patients grouped according to TAPSE<16 mm (–) and ≥16 mm (+) and LV EF at or above (+) and below (–) the median.

 
Correlation coefficients of log-transformed NT-proBNP concentrations with several echocardiographic indices of left and right heart geometry and function were computed. The log-transformed NT-proBNP levels were negatively correlated with TAPSE (r=–0.39, p<0.0001), less with septal E/Em (r=–0.38, p<0.0001), mean E/Em (r=–0.36, p=0.0001), LV EF (r=–0.32, p=0.0002) and RV acceleration at isovolumic contraction (r=–0.24, p=0.010). The log-transformed NT-proBNP was positively correlated with right atrial area (r=0.36, p<0.0001) and RV end-diastolic diameter (r=0.31, p=0.0003) and left atrial area (r=0.18, p=0.036).

3.2. Follow-up and clinical outcome
During a mean follow-up period of 20 months (range 1 to 50 months), there were 46 deaths and 39 HF-related hospitalisations. A cardioverter defibrillator was implanted in 8% of the study patients, 8% underwent cardiac resynchronization therapy and 4% underwent mitral valve surgery with or without ventricular reconstruction.

The association of clinical and echocardiographic variables with the primary and secondary end points was assessed by univariate analysis, as shown in Table 3. Hazard ratios for these variables are also shown. Log-transformed plasma NT-proBNP (p<0.0001), EF (p<0.0001) and TAPSE (p<0.0001 for all-cause mortality and p=0.001 for the combined end point) remained powerful predictors of outcome when variables were also analyzed in a continuous fashion.


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  		Table 3 Univariate predictors of all-cause mortality and all-cause mortality or heart failure hospitalisation

 
Multivariate predictors of poor outcome included TAPSE and NT-proBNP. An independent association with death/HF-related hospitalisation was found for NT-proBNP and RV fractional area change (Table 4). NT-proBNP as a log-transformed continuous variable was also the most powerful independent predictor of both all-cause mortality and the combined end point (p<0.0001). When TAPSE was used as a continuous variable, it independently predicted all-cause mortality (p=0.016).


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  		Table 4 Predictors of all-cause mortality and all-cause mortality or heart failure hospitalisation at multivariate analysis

 
In the interactive stepwise model, introduction of TAPSE and plasma NT-proBNP resulted in significant increments in the predictive value for all-cause mortality in a model including demographic (age, sex) and clinical (NYHA class) data and LV EF (Fig. 2). For prediction of death/HF-related hospitalisation, LV EF, added to the model after clinical and demographic parameters (chi-square=13.59) yielded a global chi-square of 16.53 (p=0.005). The subsequent addition of an estimate of RV dysfunction, assessed by RV fractional area change, moved the chi-square up to 23.05 (p=0.0011). Finally, the addition of NT-proBNP further increased the chi-square up to 34.32 (p<0.0001).


Figure 02
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  		Fig. 2 In the interactive stepwise model, introduction of TAPSE<16 mm and supra-median NT-proBNP values increased the predictive value for all-cause mortality in a model including demographic and clinical data (age, sex, aetiology and NYHA class) and left ventricular ejection fraction.

 
3.3. Survival curves
Analysis of Kaplan-Meier curves demonstrated that patients with moderate-to-severe functional MR exhibited a significantly worse survival than those without it (Fig. 3). Similarly, 36-month survival free from death/HF-related hospitalisation was worse (36%) in the study group than in the controls (66%) (p<0.0001).


Figure 03
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  		Fig. 3 A. Kaplan-Meier plot showing survival free from all-cause mortality in patients with moderate-to-severe mitral regurgitation (VCW≥0.5 cm) (46 events) compared to the control group (VCW<0.5 cm) (47 events). B. Survival in study patients categorized according to TAPSE<16 mm (–) or ≥16 mm (+) and NT-proBNP<3283 pg/ml (–) or ≥3283 pg/ml (+). Legend: VCW: vena contracta width.

 
In the study group, patients with RV dysfunction exhibited a worse survival than those with preserved RV function. In patients categorized according to TAPSE, survival free from all-cause mortality at 36 months was 42% in those with TAPSE<16 mm and 82% in those with TAPSE≥16 mm (Log-rank<0.0001). Actuarial survival curves for total mortality or HF hospitalisation showed a significantly better outcome for patients with preserved RV systolic function than for patients in the RV dysfunction group. Survival was strikingly worse for patients with TAPSE<16 mm and a supra-median value of NT-proBNP than for those with TAPSE≥16 mm and for those with TAPSE<16 mm and an infra-median value of NT-proBNP (Fig. 3). Similar results were obtained for the combined end point of death and hospital re-admission.


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
References
 
In patients with systolic HF and moderate-to-severe functional MR, multivariate analysis showed that depression in longitudinal RV contraction, as indicated by a compromised TAPSE and an elevated plasma NT-proBNP independently predicted all-cause mortality. Outcome was worst in the subgroup with elevated NT-proBNP and reduced TAPSE.

4.1. Relationship between right ventricular overload and dysfunction in functional mitral regurgitation
The presence of more than mild MR in HF patients with LV systolic dysfunction is associated with reduced survival, so the worse the MR, the worse the prognosis. Recently, patients with LV systolic dysfunction and a vena contracta width of at least 0.5 cm were shown to have a poor outcome [21]. RV dysfunction affects prognosis in patients with systolic HF [22-25], but little is known about the prognostic impact of RV dysfunction in patients with functional MR.

Abnormalities in RV structure and function are known to take place in patients with pulmonary arterial hypertension. Enriquez-Sarano et al. have demonstrated that the degree of functional MR is a primary determinant of pulmonary hypertension in patients with LV systolic dysfunction [6]. In a study of patients with significant organic MR, pulmonary artery systolic and wedge pressures were significantly and inversely related to radionuclide-measured RV EF; a higher mortality rate was found in those with a compromised RV EF [26]. Hence, there may be a relationship between moderate-to-severe MR and the development of RV overload and dysfunction in patients with mitral incompetence due to systolic HF.

Many echocardiographic indexes are useful to assess RV function because they are accurate, simple and reproducible, in addition a prognostic value has been verified for many of them [11,12,27-29]. The prognostic significance of TAPSE in patients with systolic HF and dilated cardiomyopathy has been demonstrated [12,27,29]. In our study of patients with secondary MR with a vena contracta width ≥0.5 cm, a reduced TAPSE was clearly associated with adverse prognosis, whereas neither pulmonary hypertension nor mitral flow variables provided significant contributions to outcome prediction. The latter is not surprising, since peak E wave velocity and the E/A ratio increase in proportion to MR severity [30]. It should be mentioned, however, that this was not the case with the mitral E/Em ratio, which has been shown to provide prognostic information in HF patients with systolic dysfunction and severe secondary MR, probably because it is less influenced by LV loading conditions [31].

4.2. N-terminal B-type natriuretic peptide levels in right ventricular dysfunction
It has been shown that B-type natriuretic peptide levels rise in parallel to the extent of RV dysfunction in pulmonary hypertension [32]. However, as RV dysfunction is often associated with LV dysfunction, the usefulness of cardiac natriuretic peptides as markers for RV dysfunction depends on the importance of concomitant LV dysfunction [8,33].

Patients with dysfunctional longitudinal RV contraction (TAPSE<16 mm) had the highest NT-proBNP concentrations. Although it has been shown that plasma levels of natriuretic peptides, which increase in proportion to MR severity, are further raised by the development of RV dysfunction and failure [33,34], it is reasonable to assume that this was mainly due to a greater impairment of LV systolic function.

The worst survival, which was observed in patients with TAPSE<16 mm and elevated NT-proBNP levels is likely to reflect the impact of advanced RV dysfunction. The association of a reduced tricuspid annular motion with a major increase in plasma NT-proBNP is an ominous prognostic marker that may reflect the presence of a severe RV dysfunction in the context of a concomitant biventricular dysfunction [35].

4.3. Clinical implications
Appreciation of the prognostic value of RV dysfunction in patients with moderate-to-severe functional MR may have clinical significance and a number of therapeutic implications. First, recognition of incipient RV dysfunction makes it possible to estimate the appropriate time for mitral valve repair or replacement, before the onset of irreversible RV dysfunction [36]. Second, in patients with significant LV dyssynchrony, measurements of tricuspid annular motion may be valuable for predicting an individual's response to cardiac resynchronization therapy; moreover, since reduction in MR severity is a potential mechanism by which cardiac resynchronization therapy alleviates the RV haemodynamic burden [37], assessment of RV function and detection of major changes in plasma natriuretic peptide levels may be useful when planning biventricular pacing, as it may help to anticipate the occurrence of RV failure.

4.4. Study limitations
Determinants of survival in patients with secondary MR include quantitative measures of MR, such as regurgitant volume and the effective regurgitant orifice, which were not contemplated in this study. Despite this limitation, the strength of the vena contracta method stands in its feasibility and reproducibility and because it can be used to accurately differentiate mild from moderate-to-severe degrees of MR. Furthermore, unlike the isovelocity surface area method, colour flow imaging of the vena contracta has been validated for assessing eccentric jets. Since NT-proBNP levels vary according to age, sex and creatinine levels, these factors have the potential to confound the accurate interpretation of prognosis [38]. Finally, atrial fibrillation (which accounted for 1/3 of patients with TAPSE<16 mm) could have significantly contributed to the increased NT-proBNP levels in RV dysfunction [39].

4.5. Conclusions
In HF patients with LV systolic dysfunction and moderate-to-severe functional MR, RV failure, estimated by TAPSE and elevated NT-proBNP levels, seem to provide information that is useful for prognostic stratification. Early recognition of RV dysfunction by the use of this simple index of RV longitudinal contraction and the assessment of natriuretic peptide plasma levels may be valuable for planning surgical or medical interventions in order to prevent or delay irreversible RV failure.


   References
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 References
 

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A. Chrustowicz, G. Simonis, K. Matschke, R. H. Strasser, and A. Gackowski
Right ventricular dilatation predicts survival after mitral valve repair in patients with impaired left ventricular systolic function
Eur J Echocardiogr, March 1, 2009; 10(2): 309 - 313.
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