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Archives of cardiovascular diseases
Volume 104, n° 12
pages 611-618 (décembre 2011)
Doi : 10.1016/j.acvd.2011.10.004
Received : 25 July 2011 ;  accepted : 10 October 2011
Left atrial size is an independent predictor of overall survival in patients with primary systemic amyloidosis
Le diamètre de l’oreillette gauche est un prédicteur indépendant de mortalité chez les patients ayant une amylose primitive à chaînes légères
 

Dania Mohty a, , Philippe Pibarot b, Jean G. Dumesnil b, Nicole Darodes a, David Lavergne c, Najmeddine Echahidi a, Patrice Virot a, Dominique Bordessoule c, Arnaud Jaccard c
a Pôle « cœur-poumon-rein », service cardiologie, hôpital Dupuytren, CHU de Limoges, 87042 Limoges, France 
b Institut universitiare de cardiologie et de pneumologie de Québec, université Laval, Québec, Canada 
c Pôle « onco-hématologie », service d’hématologie clinique et de thérapie cellulaire, centre national de référence pour l’amylose AL et autres maladies de dépôts d’immunoglobulines monoclonales, CHU de Limoges, 87042 Limoges, France 

Corresponding author. Fax: +33 5 55 05 63 34.
Summary
Background

Primary systemic amyloidosis is a severe plasma cell disorder characterized by the extracellular deposition of amyloid fibrils in different organs. Echocardiography is usually performed to assess cardiac involvement. We hypothesized that in patients with systemic amyloidosis, simple echocardiographic measurement of the left atrial (LA) diameter indexed to the body surface area might provide an important risk marker for this disease.

Methods

Between 1997 and 2011, 134 patients were diagnosed with primary systemic amyloidosis and had echocardiography within 28 days; we collected their baseline characteristics and biological and echocardiographic data retrospectively. LA enlargement was defined as recommended as M-mode LA diameter greater or equal to 23mm/m2.

Results

One hundred and eleven patients (83%) had echocardiographic LA dimension data available (mean age 63±11 years; 61% men; 31% previously diagnosed with systemic hypertension). Mean left ventricular ejection fraction (LVEF) and interventricular septum thickness (IVST) were 62±12% and 14±4mm, respectively. Mean follow-up was 2.8±2.9 years (maximum 12 years). Patients with LA enlargement had a slightly lower LVEF (P =0.08) and a significantly greater IVST (P <0.0001). Overall, 5-year survival was 57±5%. However, 1-year and 5-year survival rates were markedly reduced in patients with LA enlargement versus those without LA enlargement (61±7% and 39±8% vs 83±5% and 72±7%, respectively; P =0.0007). On multivariable analysis, after adjusting for age, sex, LVEF, IVST, presence of hypertension and creatinine concentration, LA enlargement remained an independent predictor of overall mortality at 5 years (hazard ratio 2.47; 95% confidence interval 1.11–5.90; P =0.02).

Conclusion

LA enlargement, a surrogate marker of diastolic dysfunction, is an independent predictor of long-term mortality and may therefore help to enhance risk stratification and management of patients presenting with amyloidosis.

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Résumé
Contexte

L’amylose systémique à chaînes légères (AL) est une maladie grave caractérisée par des dépôts de fibrilles amyloïdes dans différents organes. L’échocardiographie transthoracique est l’examen le plus couramment réalisé pour évaluer l’atteinte cardiaque. Nous avons émis l’hypothèse que chez des patients présentant cette maladie, une simple mesure du diamètre de l’oreillette gauche par échocardiographie peut être un important marqueur pronostique.

Méthodes

Nous avons comparé les données au diagnostic de 134 patients pris en charge pour une amylose AL systémique entre 1997 et 2011 dans notre centre. Cent onze patients (83 %) parmi eux avaient une échographie cardiaque dans les 28jours suivant le diagnostic. La dilatation de l’oreillette gauche a été définie tel que recommandé, par un diamètre supérieur ou égal à 23mm/m2. Les données démographiques, biologiques et échographiques ont été collectées de façon rétrospective.

Résultats

Dans la population d’étude de 111 patients, l’âge moyen est 63±11ans ; 61 % sont de sexe masculin et 31 % ont des antécédents d’hypertension artérielle. Le temps de suivi moyen était de 2,8ans (max 12ans). Les patients avec oreillette gauche dilatée supérieure ou égale à 23mm/m2 avaient une fraction d’éjection plus basse et un septum interventriculaire significativement plus épaissi. La survie globale à cinqans était de 57±5 %. Toutefois, ce taux de survie à un et cinqans était significativement diminué chez les patients avec une oreillette dilatée : 61±7 % et 39±8 % contre 83±5 % et 72±7 % respectivement chez ceux dont l’oreillette n’est pas dilatée (p =0,0007). En analyse multivariée, après ajustement pour l’âge, le sexe, la fraction d’éjection ventriculaire gauche, la présence d’hypertension, l’épaisseur du septum et la créatinémie, la dilatation de l’oreillette gauche reste un facteur indépendant prédictif de mortalité globale à cinq ans (HR 2,47 ; 95 % CI 1,11–5,90 ; p =0,02).

Conclusion

La dilatation de l’oreillette gauche, est un marqueur indépendant de mortalité à long terme, qui peut contribuer à améliorer la stratification du risque et la prise en charge des patients présentant une amylose AL primitive.

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Keywords : Systemic amyloidosis, Transthoracic echocardiography, Left atrial diameter, Survival

Mots clés : Amylose systémique primitive, Échocardiographie, Diamètre de l’oreillette gauche, Survie

Abbreviations : IVST, LA, LADi, LV, LVEF, TTE


Background

Primary systemic amyloidosis is a severe plasma cell disorder characterized by the deposition of amyloid fibrils in different organs. This process damages the involved organs and impairs their function. Myocardial involvement is not unusual [1] in patients with primary systemic amyloidosis and results in progressive heart failure; thus, it has a major impact on prognosis. Without specific treatment, median survival is less than 6 months for symptomatic patients [2]. TTE is the most common test performed to diagnose cardiac involvement. When cardiac involvement is suspected, TTE may show typically: hypertrophied LV walls, left atrial enlargement, LV diastolic dysfunction and, at a later stage, severe restrictive cardiac pattern. The LA is an important feature of diastolic dysfunction [3] and the degree of LA enlargement is directly related to the impairment of LV dysfunction in different cardiac diseases where diastolic dysfunction is predominant.

In the last few years, it has been shown that LA size, as measured by TTE, confers independent prognostic information regarding cardiovascular events and mortality after consideration of various known clinical and echocardiographic predictors [3, 4, 5, 6].

The LA diameter, as measured by TTE, is a valid surrogate of LA size although less precise than the calculated LA volume [6, 7]. It is more easily obtainable, reproducible and less time consuming to measure than LA volume; in fact, measurement of the LA diameter has, for a long time, been a part of the standard echocardiographic evaluation and in previous studies it has been correlated with outcome and prognosis in other heart diseases [4, 8]. Accordingly, we sought to determine whether this very simple measurement might provide important prognostic information in patients with primary systemic amyloidosis.

The purpose of this study was to determine the prognostic value of LA size in patients with primary systemic amyloidosis.

Methods
Patient population

The study included 134 patients with confirmed primary systemic amyloidosis who were admitted to the CHU Limoges haematology department between June 1997 and April 2011. The diagnosis was confirmed by an organ biopsy that demonstrated typical Congo red birefringence under polarized light, further confirmed by the presence of monoclonal proteins in the serum and/or a monoclonal population of plasma cells in the bone marrow [9].

Patients with localized amyloidosis or a history of familial or senile amyloidosis were excluded from our study. Affected organs were determined based on standard criteria for the evaluation of systemic amyloidosis [10].

In our study population, 67 patients (60%) with primary systemic amyloidosis were considered to have cardiac involvement on the basis of clinical history, typical electrocardiographic features of cardiac amyloidosis and echocardiographic signs, which were: LV wall thickness greater than 12mm (in the absence of other causes of LV hypertrophy), diastolic dysfunction, dilated LA, pericardial effusion and/or thickened free right ventricular wall.

Patients were mainly treated with conventional chemotherapy, usually the M-Dex regimen (melphalan and dexamethasone), or with new drugs (thalidomide, bortezomib and lenalidomide) for non-responders after 2005.

Data collection

We performed a retrospective collection of demographic, clinical, biological and TTE data using patients’ charts. Survival data were obtained from death certificates, family physician questionnaires or hospital records. To avoid misclassification of the cause of death, all-cause mortality was selected as the endpoint. Ninety-eight percent of patients had their follow-up completed by April 2011. LA diameter data were available for 111/134 (83%) patients included in the study. Doppler-echocardiographic measurements included assessment of LV systolic and diastolic function, LV end-diastolic diameter and LV end-systolic diameter, and LVEF was calculated using the Teicholz and/or Simpson method according to American Society of Echocardiography and European Association of echocardiography recommendations [11]. LA anteroposterior diameter was measured by M-mode TTE in parasternal long-axis view and was indexed to body surface area (LADi). The cutoff of greater or equal to 23mm/m2 for LADi was used to define LA enlargement as suggested in the recommendations of the European Association of echocardiography [11].

Statistical analysis

Patients were divided into two groups according to LA size. Patients with LADi greater or equal to 23mm/m2 were considered to have LA enlargement, whereas those with LADi less than 23mm/m2 were considered to have a normal-sized LA. Continuous data were expressed as mean±standard deviation and were compared by Student’s t test, using commercially available software (JMP 7-1). Categorical data were given as percentages and were compared using the Chi2 test. A P value less than 0.05 was considered as statistically significant.

The primary endpoint was overall survival calculated from the time of first diagnosis of amyloidosis until the date of last available follow-up. The cumulative probability of an event for the survival endpoint was estimated by the Kaplan-Meier method and results are presented at 1 and 5 years. Log-rank tests were used to test for significance in survival between the two groups. We first performed a univariate Cox proportional hazard analysis to test the association between survival and the most clinically relevant variables, as well as some echocardiographic variables that were available in our dataset and are known to affect survival rate in this population. We then performed a multivariable analysis that included age, sex, presence of hypertension and the variables that were significant in the univariate analysis. Results were reported as hazard ratios with the corresponding confidence interval of probability values.

Results

The study population consisted of 111/134 patients who were referred to the CHU Limoges haematology department with echocardiographic data available at baseline. Fifty-three (54%) of the 111 patients had LA enlargement (LADi ≥ 23mm/m2).

Baseline characteristics of the total population

Among the 111 patients, 61% were men, the mean age was 63±11 years, 31% had a history of hypertension and 10% had atrial fibrillation or a documented history of paroxysmal atrial fibrillation at baseline. Sixty-one percent of the patients had renal involvement based on standard criteria for the evaluation of affected organs [10]. Similarly, cardiac involvement, as defined above, was found in 60% of patients. Mean LVEF was 62±12%; mean IVST was 14±4mm. Other baseline characteristics are shown in Table 1. It should be noted that E/E’ ratio obtained at the lateral side of the mitral annulus was available only in 65% of the study population and the mean E/E’lat was 15±7.

Comparison of patients with and without left atrium enlargement

In our series, patients with LA enlargement were older (66±11 vs 59±11 years; P =0.0002) compared with those without LA enlargement, but the groups were not significantly different in terms of sex, presence of hypertension, monoclonal free light chain involved and renal involvement (all P >0.05; Table 1). However, patients with LA enlargement had significantly more cardiac involvement (75% vs 47%; P =0.001) and more atrial fibrillation (16% vs 4%; P =0.03). Mean LVEF was also slightly lower (60±13% vs 64±11%; P =0.08) in the group with LA enlargement compared with the group without LA enlargement.

Long-term outcome of patients with primary systemic amyloidosis according to left atrium size

Follow-up data were available for 98% of patients. The mean follow-up time was 2.8±2.9 years (maximum 12 years). Overall, there were 49 deaths. The overall 1-year and 5-year survival rates were 72±4% and 57±5%, respectively. The long-term survival rates at 1 and 5 years, respectively, for patients with LA enlargement (61±7% and 39±8%) were significantly lower than in patients without LA enlargement (83±5% and 72±7%; P =0.0007; Figure 1A).



Figure 1


Figure 1. 

A. Kaplan-Meier 1-year and 5-year survival curves for patients with systemic primary amyloidosis. B. Kaplan-Meier 1-year and 5-year survival curves in the subgroup of patients with systemic primary amyloidosis and apparent cardiac involvement. Dotted line, enlarged left atrial diameter indexed to body surface area (LADi); continuous line, normal LADi.

Zoom

Univariate and multivariable predictors of mortality in patients with primary systemic amyloidosis

As shown in Table 2, on univariate analysis, the predictors of survival were: age, IVST greater than 12mm, decreased LVEF less than 50%, plasma creatinine concentration and LADi at baseline diagnostic echocardiogram. Also, the E/E’ ratio (at the lateral side of mitral annulus) was available for only 74 patients and did not reach statistical significance on univariate analysis (P =0.1). However, the presence of atrial fibrillation, a history of hypertension, coronary artery disease, renal involvement, the plasma free light chains and 24-hour proteinuria did not appear as univariate predictors of survival.

On multivariable analysis (Table 3), after adjusting for age and sex, the presence of hypertension and the variables that were significant predictors of survival in the univariate analysis (creatinine concentration, IVST and LVEF), LADi greater or equal to 23mm/m2 remained an independent predictor of late mortality (hazard ratio 2.47; 95% confidence interval 1.11–5.90; P =0.02).

Prognostic value of left atrium enlargement in the subgroup of patients with presumed amyloid heart involvement

In the subset of patients (n =67; 60%) with apparent cardiac involvement as previously defined, LA enlargement remained a powerful predictor of survival (Figure 1B), with Kaplan-Meier survival rates of 78±8% and 62±10% at 1 and 5 years, respectively, in the group without LA enlargement versus 51±8% and 34±9% in the group with LA enlargement (P =0.01); This association again remained statistically significant on multivariable analysis, after adjusting for age, sex and LVEF (hazard ratio 2.3; 95% confidence interval 1.02–5.50; P =0.04).

Discussion

The main finding of the present study is that LA enlargement is a frequent finding and is a strong and independent predictor of mid-term and long-term survival in patients with primary systemic amyloidosis.

Using a simple parameter (anteroposterior LADi) measured by M-mode TTE, we were indeed able to show that LA enlargement was an independent predictor of total long-term survival, with an almost 2.5-fold increase in the risk of overall mortality, even after adjusting for other important and independent predictors of mortality in this high-risk population. LADi was also a predictor of survival in the subgroup of patients with apparent cardiac involvement.

To our knowledge, this is the first study of more than 100 patients with systemic amyloidosis who were seen at a single centre and had a fairly long-term follow-up, that has shown that a simple and easy echocardiographic variable that can be performed very quickly in routine practice has an important prognostic implication in long-term follow-up.

Clinical significance of left atrium enlargement

Diastolic dysfunction can develop early in the course of systemic amyloidosis, sometimes before LV walls become severely hypertrophied. Diastolic dysfunction results in elevated LV filling pressures that are transmitted back to the LA. The thin atrial wall may be affected by increased load [12] and the elevated LA pressures required to maintain adequate diastolic filling result in LA wall tension and LA enlargement. LA size is closely linked to LV diastolic dysfunction and may be a marker of severity and chronicity [13].

LA enlargement is regarded as an important prognostic factor in various heart diseases. In fact, some previous studies using LA dimensions measured by M-mode echocardiography to assess LA remodelling or, more recently, using LA volume obtained by the Simpson two-dimensional method, have demonstrated that increased LA size is related to increased morbidity, such as atrial fibrillation [14], future stroke and mortality [15] in patients with different cardiovascular diseases [3, 8, 16, 17, 18, 19]. Classical echocardiographic descriptions of cardiac involvement in systemic primary amyloidosis include–in addition to small LV size–increased biventricular free wall and septal atrial thickening combined with preserved or slightly depressed LVEF and enlarged atria. However, to our knowledge, no study has shown the prognostic value of enlarged atria, whether assessed by diameter, surface or volume, in this particular disease. Surprisingly, in a study by Bellavia et al. [20] that tested the impact of multiple clinical, biological and echocardiographic variables on overall survival in a large, primary systemic amyloidosis cohort, LA volume did not come out as a univariate or independent predictor of survival, suggesting, perhaps, different patient recruitment or interaction with other related diastolic dysfunction variables. Although our study, because of its retrospective design, did not use the ‘most modern’ method of assessing LA size (i.e. the volumetric method), we were able to show that anteroposterior LADi is a powerful predictor of long-term overall survival, independent of other predictors of mortality, such as LVEF, LV wall thickness, age and sex. Another study, published by Modesto et al. in 2005, showed that LA function assessed by strain imaging was decreased in patients with primary amyloidosis compared with controls [21], suggesting that true LA myopathy is present in patients with primary systemic amyloidosis with presumed cardiac involvement. However, the LA Doppler strain imaging technique is a difficult and time-consuming method that requires offline measurements and a long learning curve, with some interobserver and intraobserver reproducibility issues. Finally, another paper, published by Fitzgerald et al. in 2011 [22], showed that LA dilatation was more pronounced in patients with cardiac amyloidosis when compared with those with hypertensive disease for the same degree of LV hypertrophy, suggesting again the direct toxicity of light chains on the LA and the presence of true atrial myopathy in this disease. This article by Fitzgerald et al. is in accordance with our present results, suggesting that LA enlargement may be ‘another differentiator’ or marker of cardiac amyloidosis in presence of LV hypertrophy.

LA size that is a marker of diastolic dysfunction and elevated LV filling pressure may, therefore, be a useful marker for risk stratification at baseline and clinical decision-making, in patients with primary systemic amyloidosis. In fact, prognosis of primary amyloidosis has improved recently, with better survival at 5 years compared with a mortality rate that was very high in this population a few years ago. This improvement is mainly due to the ‘modern’ treatment recently proposed–particularly the use of new drugs such as thalidomide, bortezomib and lenalidomide, in addition to conventional chemotherapy (dexamethasone and melphalan). Consequently, LA enlargement–a marker of advanced diastolic dysfunction and high LV filling pressure–if detected earlier, may provide an incentive in the near future to treat these patients ‘maybe’ more aggressively, using these new, more efficient drugs as first-line treatment. In addition to this potential clinical impact of detecting LA enlargement, and although diuretic treatment is mainly based on clinical signs, LA enlargement may help to differentiate those with high LV filling pressure who need higher doses of diuretics from those with less severe diastolic dysfunction.

Clinical implications

Our study may have important clinical implications because it contributes to enhancing the risk stratification of patients with systemic amyloidosis, independent of the other predictors of mortality. We chose a very simple variable that is easily measured by all echocardiographs and echocardiographers and is not time consuming in routine practice. This variable (i.e. the anteroposterior M-mode LADi), although less precise compared with LA volume, was able to predict independently overall 1-year and 5-year survival in a population known to have frequent LV diastolic function et elevated LV filling pressures. Quick, non-invasive measurement of LA size may therefore be a useful marker for risk stratification and clinical decision-making in this particular population (such as the use of more aggressive drugs as first-line treatment or the introduction of diuretics, for instance, before peripheral signs of cardiac congestion appear).

Study limitations

Our study was retrospective in design: demographic, clinical, biological and echocardiographic data were collected retrospectively reviewing patients’ medical charts. Outcome data were also obtained retrospectively from patients’ charts, death certificates or family doctor questionnaires. Therefore, the exact cause of death was not always available. That is why the main endpoint in our study was overall death and not cardiovascular death.

Some objections may be raised against the use of LA dimension obtained by M-mode TTE as a measure of LA enlargement. In fact, recent studies have shown that LA size obtained by two-dimensional echocardiography using volumetric assessment is superior to LAD or LA area [6]. However, LA volumetric data were not widely available in TTE reports at the time of inclusion (from 1997 onwards), whereas LAD by M-mode TTE constituted routine echocardiographic data and was available for almost all patients included. In addition, although previous studies have shown the superiority of LA volume for predicting outcomes, many echocardiography reports in our institution still do not include the LA volume indexed because of the longer time that this measurement requires. Pro-brain natriuretic peptide and troponin Ic or T have been shown to be powerful predictors of outcome in primary systemic amyloidosis patients and have become part of the routine biological tests performed for these patients, especially when cardiac involvement is suspected. In our study, because of its retrospective design (from 1997 onwards), only 65 of the 134 patients had those measurements performed; in fact N-terminal pro-brain natriuretic peptide and troponin have been measured in our institution systematically only since 2007 in the context of this disease, so we could not test the prognostic value of these biological variables in our population. Other variables, such as pulsed Doppler tissue imaging (E/E’ measured at the sepal or lateral side of the mitral annulus), have been shown to be markers of diastolic function and to predict high LV filling pressure [23] in various diseases. This modern variable was not measured in the late 1990s and was therefore available in our study group only for 65% of the patients included. Because of the limited number of patients with this variable, we did not test it in the multivariable analysis.

The presence of hypertension in 31% of the patients included in our study may be a confounding factor because it leads chronically to LV hypertrophy, which causes diastolic dysfunction and LA dilatation; However, when tested in the univariate and multivariable analyses, as shown in Table 2, the presence of hypertension did not emerge as a predictor of survival in our population.

Conclusion

In patients with systemic primary amyloidosis, LA enlargement (a surrogate marker of diastolic dysfunction, elevated LV filling pressure and chronicity), appeared to be a strong independent predictor of long-term mortality. Therefore, LA enlargement may help to enhance risk stratification and management of patients presenting with this disease.

Disclosure of interest

The authors declare that they have no conflicts of interest concerning this article.

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