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European Journal of Heart Failure 2007 9(8):808-813; doi:10.1016/j.ejheart.2007.05.006
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© 2007 European Society of Cardiology

Importance of the echocardiographic evaluation of right ventricular function in patients with AL amyloidosis

Stefano Ghioa,*, Stefano Perlinib, Giovanni Palladinib,c,1, Nina Ajmone Marsana, Giovanna Faggianoa, Monia Vezzolib, Catherine Klersyd, Carlo Campanaa, Giampaolo Merlinic and Luigi Tavazzia

a Division of Cardiology, Fondazione IRCCS Policlinico S. Matteo and University of Pavia 27100 Pavia, Italy
b Department of Internal Medicine, Fondazione IRCCS Policlinico S. Matteo and University of Pavia 27100 Pavia, Italy
c Centre for Amyloidosis, Department of Biochemistry, Fondazione IRCCS Policlinico S. Matteo and University of Pavia 27100 Pavia, Italy
d Clinical Epidemiology and Biometry Unit, Fondazione IRCCS Policlinico S. Matteo and University of Pavia 27100 Pavia, Italy

* Corresponding author. Divisione di Cardiologia, Policlinico S. Matteo, Piazzale Golgi 1, 27100 Pavia, Italy. Tel.: +39 0382 503 718; fax: +39 0382 501884. E-mail address: s.ghio{at}smatteo.pv.it


    Abstract
 Top
 Notes
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
Background: Patients with AL amyloidosis often present with signs of congestive heart failure.

Aim: This study was prospectively designed to assess the significance of RV dysfunction in AL amyloidosis.

Methods and results: Seventy-four patients with biopsy proven AL amyloidosis underwent a thorough echocardiographic evaluation. A tricuspid annular plane systolic excursion (TAPSE) <17 mm was taken as marker of RV dysfunction. Plasma NT-proBNP determinations were performed in all cases. RV function was normal in 60 patients and reduced in 14 patients. Patients with RV dysfunction had thicker left ventricular (LV) walls (p<0.01), lower LV end-diastolic volumes (p<0.01), lower LV ejection fraction (p<0.01) and more frequently a restrictive LV filling pattern (p<0.01). RV dimensions and RV free wall thickness were not significantly different in the two groups. A thick interventricular septum and a reduced TAPSE were associated with high NT-proBNP levels (both p<0.01). Seven patients died during a median follow-up period of 19 months; TAPSE <17 mm was the only echocardiographic parameter associated with poor survival.

Conclusion: In patients with AL amyloidosis, RV dysfunction is associated with more severe involvement of the left ventricle, higher plasma levels of NT-proBNP and with poor prognosis.

Key Words: Amyloid • Prognosis • Right ventricle • Echocardiography

Received August 7, 2006; Revised February 9, 2007; Accepted May 8, 2007


    1. Introduction
 Top
 Notes
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
The amyloidoses constitute a large group of diseases in which aggregates of insoluble toxic protein are deposited in forms of fibrils in several tissues [1,2]. One of the most common forms of systemic amyloidosis is AL amyloidosis, in which fibrils are composed mainly by the N-terminus of a monoclonal immunoglobulin light-chain; the incidence is approximately 1 case per 100000 person-years in western countries and in such patients cardiac involvement is not only frequent but it is the most common cause of death [3,4].

Although initial descriptions in patients with AL amyloidosis (presumably in patients with end stage disease) typically depicted non dilated, thickened right and left ventricles [5-7], the diagnosis of cardiac amyloidosis most frequently relies on the echocardiographic demonstration of a left ventricle having thickened walls, eventually characterized by abnormal myocardial texture, with a preserved systolic function and usually showing diastolic dysfunction. In such patients the usefulness of assessing right ventricular (RV) geometry and function has not been clearly recognized and, despite the suggestions of a few studies, it is likely considered an academic issue [8,9]. However, the fact that patients with AL amyloidosis often present with signs of congestive heart failure and that RV dysfunction is known to be an independent predictor of poor prognosis in patients with advanced heart failure of different aetiology, provides a strong rationale for the study of RV function in such patients [10,11].

This study was prospectively designed to assess the relevance of non invasive evaluation of RV function in AL amyloidosis. The pre-specified aims were: 1) to evaluate whether RV dysfunction is associated with a greater infiltration of the right ventricle or with a greater impairment of systolic and diastolic LV function; 2) to assess the relationship between RV function and plasma levels of NT-proBNP, a powerful prognostic determinant in AL amyloidosis [12]; and 3) to assess whether RV dysfunction is associated with poor prognosis in such patients.


    2. Methods
 Top
 Notes
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
2.1. Patients
We studied 74 consecutive patients with AL amyloidosis seen at the Centre for Amlyloidosis in Pavia. All patients had biopsy proven AL amyloidosis and a clonal plasma cell disorder. The positive biopsy site was abdominal fat in 54 patients (73%), kidney in 14 (19%), rectum in 2 (3%), liver in 2 (3%), salivary gland in 1 (1%) and myocardium in 1 (1%). All positive biopsies showed green birefringence under polarized light after staining with Congo red. Hereditary amyloidosis were excluded by DNA analysis. Cardiac amyloidosis was defined on the basis of the presence of at least one of the following criteria: clinical symptoms of heart failure (NYHA functional class ≥II), unexplained low voltages on the resting electrocardiogram in the absence of pericardial effusion, and at least one of the following echocardiographic features: increased thickness of the interventricular septum and/or of the posterior wall of the left ventricle (>12 mm) in the absence of hypertension, valvular disease and electrocardiographic criteria of left ventricular hypertrophy and/or increased myocardial echogenicity (granular sparkling) and/or unexplained right ventricular free wall thickness (≥7 mm) [12]. Patients on dialysis were excluded due to altered metabolism of NT-proBNP [13]. Median serum creatinine of the patients enrolled was 1.2 mg/dL (range: 0.4-5.2 mg/dL) and median glomerular filtration rate calculated with the MDRD equation was 56 mL/minx1.73 m2 (range: 12.4-168.3 mL/minx1.73 m2). Fourteen patients (18%) had a history of hypertension and 1 patient (1%) had a myocardial infarction 9 years before the diagnosis of amyloidosis was made. Eight patients (11%) were active cigarette smokers at the time of the study and 14 (19%) had a previous history of smoking (smoking was discontinued a median of 18 years (range 1-25 years) before enrollment). None had a history of pulmonary embolism.

Follow-up visits were scheduled every 3 months and time to death was calculated from the date of the echocardiographic evaluation. All patients gave written informed consent to participate in the study. The investigation conforms with the principles outlined in the Declaration of Helsinki. The study was approved by the Institutional Review Board of the "Fondazione Istituto di Ricovero e Cura a Carattere Scientifico Policlinico San Matteo".

2.2. Response to chemotherapy
Haematologic response to chemotherapy was defined according to the criteria proposed by the International Society of Amyloidosis [14]. Complete response required negative serum and urine high-resolution immunofixation electrophoresis. Partial haematologic response required a >50% reduction in serum and urine monoclonal component and a >50% reduction of the concentration of the amyloidogenic circulating free light chain. Sixty-six patients (89%) received chemotherapy before the echocardiographic evaluation was performed. Thirty-eight of the treated patients (58%) received oral melphalan plus dexamethasone, 12 (18%) were treated with melphalan plus prednisone, 9 patients (14%) underwent autologous stem cell transplantation and 7 (10%) received high-dose dexamethasone. At the time of the echocardiographic evaluation, 12 patients (18%) of the 66 treated were classified as non responders, 41 (62%) were in partial haematologic response and 13 (20%) were in complete remission.

2.3. Echocardiographic evaluation
A complete M-mode, 2-D and Doppler study was performed using standard parasternal, apical and subcostal approaches. Left ventricular (LV) end-diastolic and end-systolic volumes and left ventricular ejection fraction were calculated using the area-length method. An E/A ratio <1 was considered as a marker of "abnormal relaxation" whereas a ratio ≥2 and/or a deceleration time of the E wave <125 ms at mitral valve pulsed Doppler were considered markers of "restrictive" left ventricular filling. An estimate of RV systolic pressure was obtained by adding to the transtricuspid pressure gradient an estimate of right atrial pressure. The RV end-diastolic diameter and the thickness of the right ventricle free wall were determined in the parasternal view. The systolic displacement of the lateral portion of the tricuspid annular plane (TAPSE) was considered the main echocardiographic marker of RV function. The TAPSE was measured on the M-mode tracing under 2D-echo guidance [10]; values ≥17 mm were considered normal and RV dysfunction was diagnosed when TAPSE was <17 mm [15]. End-diastolic and end-systolic RV areas were measured in the apical view and the fractional area change was calculated as (end-diastolic area minus end-systolic area) divided by end-diastolic area, x100. To assess regional myocardial function, colour tissue Doppler imaging was acquired in 2-D mode from the apical 4-chamber and 2-chamber views (System 5, Vingmed, GE). Off-line analysis of the mean velocity profiles was performed at the level of the basal and medium segments of the interventricular septum, lateral, inferior and anterior walls of the left ventricle and in the basal and medium segments of the free wall of the right ventricle using an Echopac 6.1, GE workstation. In each segment the peak systolic velocity and the peak strain were measured; strain was derived using a "sample volume" of 10x5 mm. TDI and strain data were used, together with TAPSE, to assess RV function [16-18]. TDI analysis was performed by a single experienced echocardiographer (NAM), who was blinded to the clinical history of the patient; for each parameter three values were obtained and the average was the final value.

2.4. Serum NT-proBNP measurement
Serum samples were frozen immediately and kept at –20° until testing. NT-proBNP levels were measured with an electrochemiluminescence sandwich immunoassay on an Elecsys System 2010 (Roche). Upper reference limits in men and women are, respectively, 88 ng/L and 153 ng/L in individuals <50 years old and 227 ng/L and 334 ng/L in individuals ≥50 years old. A cut-off of 1287 ng/L was set as indicator of heart involvement [12].

2.5. Statistical analysis
Continuous variables were described as mean values ±SD or median and 25th-75th percentile for skewed distributions, and categorical variables as counts and frequencies. Comparisons between groups were performed with the Mann Whitney U test or the Fisher exact test. A generalized linear regression model with the calculation of Huber White robust standard errors to account for the intrapatient correlation of measures was used to compare tissue Doppler imaging data: to simplify this analysis an average value of peak systolic velocity and peak strain was derived for basal and middle LV segments and an average value of peak systolic velocity and peak strain was derived for RV segments. The association of echocardiographic characteristics with increased NT-proBNP levels (categorized as < or ≥ than 1287 ng/L) was assessed by means of univariate and multivariate logistic regression models; backward stepwise selection (p to remove =0.2) was used. Cumulative survival was plotted according to Kaplan Meier method; and was compared between groups with the logrank test. Given that the population enrolled in the present study was relatively small and there was a low number of events, no multivariate analysis was performed to assess the prognostic significance of echocardiographic parameters. In such conditions, any multivariate analysis would suffer from overfitting with estimates of effects that would not be reliable. A 2-sided p value <0.05 was retained for statistical significance. Computations were made using Stata 9 (Stata Corp, College Station, TX).


    3. Results
 Top
 Notes
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
3.1. Clinical characteristics according to RV function
Age was similar in patients with a normal RV function (n=60, TAPSE ≥17 mm) and in patients with a reduced RV function (n=14, TAPSE <17 mm). A slightly, non significantly higher proportion of patients with a reduced TAPSE had an echocardiographic diagnosis of cardiac amyloidosis. Patients with a reduced RV function tended to be more frequently symptomatic for heart failure; they also had a higher heart rate and higher NT-proBNP levels. (Table 1)


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Table 1 Clinical characteristics according to RV function

 
3.2. Echocardiographic characteristics according to RV function
Patients with a reduced TAPSE had thicker LV walls, lower LV end-diastolic volume, lower LV ejection fraction and more frequently a restrictive LV filling pattern. The estimate of systolic pulmonary artery pressure was similar in the two groups; however, due to the absence of a transtricuspid regurgitant jet, it could not be calculated in 11 patients with normal TAPSE. At tissue Doppler imaging, the average values of peak systolic velocity and peak strain in the 4 basal and in the 4 middle segments of the left ventricle were lower in patients with reduced TAPSE. The RV diameter and areas and the thickness or the RV free wall were not significantly different between the two groups but the RV fractional area change was lower in patients with reduced TAPSE. At tissue Doppler imaging, all RV function parameters (average peak systolic velocity at the basal and mid RV free wall, average peak strain at the basal and mid RV free wall and peak systolic velocity of the tricuspid annulus) were lower in patients with reduced TAPSE. In contrast, when patients grouped according to the median value of RV free wall thickness, TAPSE was similar in the two groups (19.8±4.7 mm in patients with RV free wall thickness >5 mm and 21.5±4.4 mm in patients with RV free wall thickness ≤5 mm, NS). (Table 2)


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Table 2 Echocardiographic features according to RV function

 
3.3. NT-proBNP levels and echocardiographic parameters
At univariate analysis, the following echocardiographic features were significantly associated with levels of NT-proBNP higher than 1287 ng/L: the thickness of the interventricular septum, LV ejection fraction (inversely related), restrictive LV filling, peak velocity in the basal septum at tissue Doppler imaging, TAPSE (inversely related) and RV free wall thickness. All the above echocardiographic parameters were included in a multivariate analysis; it turned out that only the thickness of the septum and the TAPSE were significantly associated with high NT-proBNP levels (Table 3).


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Table 3 Echocardiographic variables associated with a NT-proBNP level >1287 ng/L

 
3.4. RV function and prognosis
During an average follow-up period of 19 months, 7 patients died. At univariate analysis both TAPSE (Fig. 1) and plasma levels of NT-proBNP were significantly associated with survival.


Figure 01
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Fig. 1 Kaplan Meier survival curves according to normality or abnormality of RV function (p=0.0204).

 

    4. Discussion
 Top
 Notes
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
In patients with AL amyloidosis the clinical usefulness of the ultrasound evaluation of RV geometry and function has not been clearly defined. The results of the present study indicate that in such patients the presence RV dysfunction is associated with more severe dysfunction of the left ventricle and with higher plasma levels of NT-proBNP and that, importantly, it portends a poor prognosis.

4.1. Mechanisms of right ventricular dysfunction
The extent of hypertrophy of the right ventricular free wall and the dilatation of the right ventricle were similar in patients with normal or reduced TAPSE. In contrast, patients with reduced TAPSE had a more compromised left ventricular function at echocardiography; in other words, they had thicker LV walls, lower LV ejection fraction and more frequent abnormalities of LV filling. The results strongly suggest that RV dysfunction cannot be explained on the basis of a greater extent of amyloid deposition and a greater replacement of functioning myocytes within the right heart. Most likely, RV dysfunction is indirectly caused by the elevation of pulmonary artery pressures determined by the systolic dysfunction and by the restrictive physiology of the left ventricle. This hypothesis is not contradicted by the fact that the echocardiographic estimates of systolic pulmonary pressure were similar in the two groups since the systolic pressure could not be evaluated in a sizeable proportion of patients with normal TAPSE and such patients presumably had a normal pressure. This observation is in agreement with the results obtained in patients with advanced heart failure in whom, regardless of aetiology (primary dilated cardiomyopathy or ischaemic heart disease), RV function is strongly and inversely related to mean pulmonary artery pressure [11,19]. Although the observation that TAPSE was similar in patients with or without RV hypertrophy rules out the possibility that amiloid infiltration in the right ventricle may "per se" have determined a significant dysfunction of the right ventricle, we cannot exclude the possibility that, at similar levels of RV afterload, patients with amyloid deposition in the RV may have greater RV dysfunction.

4.2. NT-proBNP plasma levels according to LV and RV function
Two echocardiographic parameters were independently related to the plasma levels of NT-proBNP. The first was the thickness of the interventricular septum, which reflects the extent of amyloid infiltration of the left heart. Since RV hypertrophy was not related to plasma levels of NT-proBNP it might be argued that most of the production of natriuretic peptides occurs at the level of the greater myocardial mass of the left ventricle. The second parameter related to plasma levels of NT-proBNP was the TAPSE, whose reduction identifies patients with RV dysfunction secondary to severe LV dysfunction. Therefore, two distinct mechanisms for myocardial production of natriuretic peptides can be hypothesized in patients with cardiac amyloidosis; the first is specific to these patients (i.e. the direct cardiotoxicity of light chain amyloid infiltration in the heart) [20]. The second mechanism (i.e. the severity of right heart haemodynamic impairment) is common to patients with heart failure in whom the highest BNP levels are in fact observed when both LV and RV dysfunction are present [21].

4.3. RV dysfunction and prognosis
Previous studies have shown that a restrictive mitral inflow pattern is the most important echocardiographic prognostic indicator in cardiac amyloidosis [22,23]. In the present population, RV dysfunction (identified by a reduced TAPSE) turned out to be the only statistically significant echocardiographic predictor of prognosis. This conclusion is not in disagreement with previous studies, since RV dysfunction is the direct consequence of systolic and/or diastolic dysfunction of the left ventricle. From a pathophysiological point of view, this is exactly what happens in most patients with advanced heart failure (11). However, due to the small number of patients this observation must be considered preliminary and needs to be confirmed in larger trials. In particular, we believe that it would be interesting to test the hypothesis that the TAPSE can give useful information in addition to that provided by NT-proBNP.


    5. Conclusions
 Top
 Notes
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
The assessment of RV geometry and function must be considered a crucial part of the echocardiographic evaluation of patients with AL amyloidosis, since in such patients RV dysfunction is associated with more severe involvement of the left ventricle, higher plasma levels of NT-proBNP and poor prognosis.


    Notes
 Top
 Notes
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
1 Giovanni Palladini is partly supported by an investigator fellowship from Collegio Ghislieri, Pavia. Back


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

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