|Year : 2015 | Volume
| Issue : 2 | Page : 40-45
Left atrial longitudinal speckle tracking echocardiography in healthy aging heart
Federico Cacciapuoti, Venere Delli Paoli, Anna Scognamiglio, Michele Caturano, Fulvio Cacciapuoti
Department of Internal Medicine and Geriatrics, Second University of Naples, Naples, Italy
|Date of Web Publication||30-Jul-2015|
Department of Internal Medicine and Geriatrics, 2nd University of Naples, Piazza L. Miraglia, 2, Naples-80138
Source of Support: None, Conflict of Interest: None
Background: Left atrial volume (LAV) and function are connected to the left ventricular (LV) haemodynamic patterns. To define the changes of LAV and functions to counterbalance age-related LV diastolic impairment, this study was undertaken. Methods: 2D-Left Atrial Speckle Tracking Echocardiography (2D-LASTE) was used to define both LAV and functions in an aged healthy population (group II) respect to adult healthy controls (group I). Results: Results showed an increasing of left atrial volume indices (LAVI) (maximum, minimum, pre-a) in old subjects in comparison with those obtained in adult healthy controls. On the contrary, LAVI passive emptying unchanged and LAVI passive fraction reduced with advanced age. Finally, LAVI active emptying increased with advancing age to compensate the age-dependent left ventricular diastolic dysfunction. The values of global systolic strain (S); systolic strain rate (SrS); early diastolic strain rate (SrE), and late diastolic strain rate (SrA) were also calculated. With reference to the function, our study confirmed that LA conduit function deteriorates with age while booster pump increases respect to adult controls and reservoir phase is maintained. Conclusions: The echocardiographic findings obtained with conventional and tissue Doppler confirmed the connection between LA functions and volumes and age-related LV dysfunction. Conclusively, 2D-LASTE appears to be a reliable tool to evaluate the role of LA to compensate the derangement of left ventricle happening with ageing.
Keywords: Heart healthy aging, left atrium, left ventricular diastolic dysfunction, longitudinal speckle tracking echocardiography
|How to cite this article:|
Cacciapuoti F, Paoli VD, Scognamiglio A, Caturano M, Cacciapuoti F. Left atrial longitudinal speckle tracking echocardiography in healthy aging heart. J Cardiovasc Echography 2015;25:40-5
|How to cite this URL:|
Cacciapuoti F, Paoli VD, Scognamiglio A, Caturano M, Cacciapuoti F. Left atrial longitudinal speckle tracking echocardiography in healthy aging heart. J Cardiovasc Echography [serial online] 2015 [cited 2021 Jan 16];25:40-5. Available from: https://www.jcecho.org/text.asp?2015/25/2/40/161778
| Introduction|| |
The left atrium (LA) plays a major role in left ventricle performance; hence, LA mechanical function is a surrogate marker of left ventricular (LV) dysfunction.  The components of LA function are divided into: Reservoir, conduit, and contractile phase. "Reservoir" corresponds to the difference between maximal and minimum LA volumes occurring in the interval just before the opening mitral valve and just before aortic valve opening. "Conduit" is the early phase of ventricular diastole. The blood is passively transferred into left ventricle just after mitral valve opening. "Contractile" phase or "booster pump" is calculated as the difference between minimum and preatrial contraction. Its role is to augment the stroke volume. The contribution of three phases of the LA function changes according to the diastolic properties of left ventricle. In normal conditions, the contribution of LA to LV filling is 40, 35, and 25%, respectively.  In relation to the LV valve movements, LA activity can be divided in four phases: A) Isovolumetric relaxation period occurring between the aortic closure and the opening of the mitral valve; B) LV rapid filling, which begins when LV pressure falls below the atrial pressure and the mitral valve opens; C) Diastasis, this corresponds to the equality between LA and LV pressures; and D) atrial systole, which corresponds to LA contraction and ends at the mitral valve closure.  Even though conventional, noninvasive techniques (as echocardiography and tissue velocity imaging derived parameters) are widely used to evaluate LA function; 2D-speckle tracking echocardiography (2D-STE) has emerged as a new, noninvasive method for the assessment of cardiac function. It is an imaging technique that provides accurate and angle-independent informations also regarding LA deformation and motion.  Recent reports suggested that 2D LA longitudinal strain obtained with STE (2D-LASTE) is an effective method for quantification of LA function. ,
It is known that LV diastolic pressure increases with advancing age inducing some changes in LA dimensions and function. , To define the changes of atrial function dependent on the ageing, 2D-LASTE study was performed.
| Materials and methods|| |
Fifteen consecutive persons (12 males (M) and three females (F)) aged from 70 to 82 years (mean age = 79 ± 5) were chosen among those afferent to our Department of Internal Medicine and Geriatrics between May 2012 and April 2014. These were actually free of any cardiovascular, respiratory, and/or metabolic derangements (Group I). , Nineteen healthy adult controls (11 M and eight F) ranging in age from 44 to 61 years (mean age = 55 ± 6 years). None of the enrolled subjects had a history of ischemic heart disease or significant valvular abnormalities, peripheral vascular disease, cerebrovascular disease, systemic hypertension, or diabetes mellitus (Group II).  In addition, none of both groups' subjects received cardioactive drugs at the moment of the study. Exclusion criterion was the inadequate echocardiographic visualization alone. Both groups were in sinus rhythm with heart rate (HR) < 100 beat/min subjects and gave their written informed consent for participation to the study.
Standard transthoracic echocardiography
Echocardiographic examinations were performed by experienced sonographers using a Philips iE33 machine (Eindhoven, NL). All measurements were performed in M- and B-mode in accordance with the American Society of Echocardiography criteria.  Ejection fraction% (EF%) was also defined according to the modified Simpson's criteria. The peak of early (E) and late (A) waves of diastolic mitral inflow were measured, and the E/A wave ratio were calculated. Mitral annular plane systolic excursion (MAPSE) was measured using M-mode echocardiography in the mitral annular lateral approach by apical four-chamber view.  Left atrial volume (LAV) was determined by the biplane area-length method.  Its value was indexed for body surface area in m 2 and evaluated in ml/m 2 .
Pulsed doppler tissue imaging (DTI)
DTI of the mitral annular level was obtained at the lateral position. Values of peak early (e') and late (a') diastolic annular velocities were also obtained. Measurements were obtained during end expiration to eliminate respiratory variations and an average of three beats measured. The E/e' ratio was also calculated.  The leading epidemiological, metabolic, and conventional echocardiographic characteristics of two groups are reported in [Table 1].
|Table 1: Clinical, echocardiography and metabolic aspects of the two enrolled groups |
Click here to view
Speckle tracking images of the left atrium were obtained both in aged patients (Group I) and in healthy adult controls (Group II) by activating STE on the same echocardiographic machine. Three consecutive cycles were recorded and averaged. Computer-generated LA volume curve during one cardiac cycle. The left atrium endocardial surface was manually traced using a point-and-click approach in apical four-chamber view that automatically allowed a region of interest (ROI). This was manually adjusted, if necessary, to better suit the atrium anatomy. The cardiac cycle was demarcated by indicating QRS onset Afterwards, ROI was divided into six segments (two corresponding to the interatrial septum; two to the lateral wall; and two to the roof of the left atrium). If adequate images quality were not obtained, the records were rejected by the software and excluded from the analysis. By using LA volume, the following LA dynamic volumes were calculated: Maximum LA volume (LAV max), minimal LA volume (LAV min), and the LA volume before the atrial contraction (LAV pre-a). Precisely, LAV max was recorded just before mitral valve opening; LAV min was recorded at mitral valve closure; and LAV pre-a is LAV at onset of atrial systole (P wave). These values were corrected for body surface area as LAV index (LAVI) and consequently, LAVI maximum; LAVI minimum; and LAVI pre-a were obtained.
The phases of left atrial function, corresponding to reservoir, conduit, and booster pump were calculated by the LAVI volumes, as follows:
Left atrial emptying fraction (LAEF) total (corresponding to atrial reservoir function)
In addition, LAVI passive emptying and passive fraction, and LAVI active emptying and active fraction were calculated.  In particular, LAVI passive emptying was measured as the difference between LAVI maximum - LAVI pre-a. Passive fraction was obtained as the ratio between LAVI passive emptying/LAVI maximum × 100%. LAVI active emptying is LAVI at onset of atrial systole - LAVI minimum. Active fraction was calculated as LAVI active emptying/LAVI pre-a × 100%.  Finally, LA global systolic strain (S); systolic strain rate (SrS); early diastolic strain rate (SrE); and late diastolic rate (SrA) were calculated in both groups. All recordings were obtained during normal respiration.
Data referring two-dimensional (2D) echocardiographic finding in both groups were expressed as mean ± standard deviation (SD). Comparison of LAVI (max, min, and pre-a) and the different phases of LAVI in two groups were performed using the Student's t-test for unpaired data. This was also employed to evaluate the differences between two groups referring LAVI passive emptying, passive fraction, LAVI active emptying, and active fraction. The mean values of reservoir, conduit and booster pump phases were also calculated in two groups. Likewise, the values of S, SrS, SrE, and SrA obtained in two groups were compared. A P-value < 0.05 was considered significant. All statistical analyses were performed using the Statistical Package for Social Sciences (SPSS) software. Data were analyzed using analysis of variance to assess for age-related changes in echocardiographic variables applying a Bonferroni's correction between two groups.
| Results|| |
Left ventricular end-diastolic volume (LVEdV; 107 ± 14 ml) and left ventricular end-systolic volume (LVEsV; 47 ± 10 ml) measured in aged subjects were not significantly different from the mean values (LVEdV = 96 ± 17 ml and LVEsV = 40 ± 13 ml) recorded in healthy adults (not significant (NS)). EF% resulted 53 ± 3.5 in aged group and = 58 ± 2.4 in controls. Differences between two values were NS too. On the other hand, left atrial diameter of aged (41.4 ± 3.7 mm) was significantly greater (P < 0.05) than that recorded in healthy controls (35 ± 41 mm). LAVI also increased (P < 0.05) in elderly subjects (31 ± 3 ml/m 2 ) in comparison to healthy adults (23 ± 2.4 ml/m 2 ). E wave recorded in aged group (74.2 ± 1.4 cm/s) was lower (P < 0.05) than that recorded in controls (89.4 ± 2.3 cm/s). On the contrary, A wave significantly (P < 0.05) increased in healthy aged (83.3 ± 2.1 cm/s) compared with the mean value recorded in healthy controls (75 ± 1.8 cm/s). In agreement with these results, E/A waves ratio (P < 0.001) decreased in aged group (0.89 ± 1.8) compared to control group (1.1 ± 2.1). Finally, MAPSE recorded in aged patients (10.0 ± 0.7) was not significantly different (NS) from the mean value obtained in adult controls (12.7 ± 08) [Table 1].
Tissue doppler imaging
The e' wave velocity decreased (P < 0.001) from 11 ± 2.6 cm/s in controls to 7.5 ± 1.4 cm/s in aged subjects. On the contrary, the a' wave velocity increased (P < 0.05) from the normal adults (8.6 ± 1.8 cm/s) to the healthy aged (9.8 ± 1.4 cm/s). The E/e' ratio also decreased (P < 0.05) with advancing age (9.1 ± 1.5 in adults and 11.7 ± 1.2 in healthy aged) [Table 1].
Adequate tracking quality was achieved in 98% of the total segments. LAVI max was = 30.7 ± 7.5 ml/m 2 , in comparison to 24.7 ± 3.5 ml/m 2 found in adult controls (P < 0.05). LAVI minimum recorded in old people was 17.5 ± 6.1 ml/m 2 with respect to the controls (13.9 ± 5.2 ml/m 2 ). Differences were significant (P < 0.05). LAVI pre-a recorded in aged group was 26.2 ± 3.8 ml/m 2 . This value was significantly higher (P < 0.001) then that recorded in healthy adults (17.2 ± 6.7 ml/m 2 ).
In addition; reservoir, conduit, and booster pump fractions of LA were recorded in two groups. Reservoir phase resulted superimposable in two groups (42.9 ± 1.5 in aged subjects vs 43.7 ± 1.8 in controls). On the contrary, conduit fraction reduced (P < 0.001) in oldest individuals (14.6 ± 1.9) in comparison with adult persons (30.3 ± 1.7). Booster pump significantly increased (P < 0.001) in aged group (33.2 ± 2.1) with respect to controls (19.1 ± 1.7) [Table 2]. Finally, LAVI passive emptying was 4.5 ± 0.4 ml/m 2 in old subjects and 7.5 ± 0.6 ml/m 2 in healthy adults. Differences were significant (P < 0.05). Passive emptying fraction was 14.7 ± 1.7 in aged, whereas its value was 30 ± 1.9 in controls. Differences were significant (P < 0.001). LAVI active emptying calculated in the elderly persons was 9.2 ± 0.7 ml/m 2 and 6.3 ± 0.2 ml/m 2 in adults without significant differences (NS). Active emptying fraction was 33.2 ± 1.9 in aged individuals, and 25.4 ± 1.3 in healthy adults, with significant differences (P < 0.001) [Table 2].
|Table 2: Values of LAVI (maximum, minimum and pre-a), reservoir, conduit and booster pump in two groups. LAVI passive and active emptying fraction recorded in healthy aged and adult controls with statistical significance |
Click here to view
| Discussion|| |
The morphological changes happening in the cardiovascular system with advancing age are responsible for increased myocardial stiffness and LV hypertrophy further evolving in LV diastolic dysfunction typical of the elderly.  For these changes, in our healthy aged individuals LV systolic function resulted to be within the normal limits with preserved LV volumes and EF% was > 50%, as previously described.  Since atrial function is related to increased LV filling, E wave velocity of diastolic mitral flow decreased and A wave significantly increased in comparison to the controls, with the inversion of the E/A wave ratio. , That happens for a strongest atrial contraction in response to the increased end-diastolic LV pressure dependent on increased LV filling pressure (LVFP). ,, It is known that MAPSE, reflecting longitudinal myocardial shortening, is a simple and sensitive echocardiographic parameter for assessing global longitudinal LV wall function. Its value is a highly accurate predictor of EF.  Particularly, MAPSE <8 mm was associated with depressed left ventricular ejection fraction (LVEF; < 50%), whereas mean MAPSE >10 mm was linked with preserved LVEF (> 55%). In our aged persons, we have found a MAPSE value of 10.0 ± 0.7 that is indicative of EF% > 50. In accordance with the study by Tighe et al.,  and successively, Munagala et al.,  in our healthy aged individuals; we found that the e' velocity decreases, the a' velocity increases, and the E/e' ratio is > 10. It is known that the E/e' ratio is able to estimate LVFPs in patients with preserved systolic function. Patients with E/e' > 15 can be classified as having elevated filling pressure. An E/e' < 8 suggests normal filling pressure. In the range of E/e' of 8-15 other informations, including systolic function, chambers dimensions, and all Doppler variables must be considered in the analysis of individual patients.  Thus, the E/e' value (11.7 ± 1.2) found in our aged subjects has an uncertain significance; but, considering all other echocardiographic data, the obtained value can be considered indicative of normal LVFPs. 2D-STE is a relatively new technology that tracks speckles in the myocardium frame-by-frame basis throughout the cardiac cycle, resulting in a noninvasive calculation of global and regional velocity, displacement, strain, and strain rate. ,, In this study, we applied this echocardiographic technique on LA walls of healthy aging hearts to define LA volumes (max, min, and pre-a) indexed for body surface area (LAVI anatomy). LAVI passive/active emptying and functions were also defined in order to evaluate the influence of LAVI function on reservoir, conduit, and booster pump function. In our healthy aged individuals, reservoir is maintained; while conduit phase decreases and booster pump function increases [Figure 1]. These results were further confirmed by strain/strain rate values. Specifically, SrS (correlated with reservoir function) remained unchanged with respect to controls; SrE (correlated with conduit phase) decreased, whereas SrA (corresponding to the contractile function) increased. Changes in LA function occurred in conjunction with age-related changes in LV diastolic function.  The preservation of LA function during ventricular systole (reservoir) is important to maintain the cardiac output.  LA acts as a conduit during the phase of early LV diastolic filling, evidencing a decline in LA passive emptying fraction. This decline corresponds to the age-related inversion in E/A ratio described in our elderly individuals. Ageing also induces both prolonged LV relaxation and impairment of LV passive properties , responsible for an augmentation of LA contribution to transmitral flow (booster pump).  Therefore, the advanced age is associated with depressed LAVI passive emptying function inversely, LAVI active emptying function increases with age  in order to maintain systolic ventricular volume, in accordance with a previous report of Rossi et al.,  and likewise to the diabetic cardiomyopathy, as we already described.  Several studies have reported similar results in healthy aging people. ,
|Figure 1: (Left) Longitudinal left atrial strain obtained in control. Reservoir, conduit, and booster pump phases are indicated. (Right) Longitudinal atrial strain recorded in aged subject. Reservoir and booster pump increased, while conduit phase decreased. PALS = Peak atrial longitudinal strain|
Click here to view
| Conclusions|| |
2D-LASTE represents an easy, noninvasive tool to characterize the morphological and functional LA changes to compensate healthy aged LV diastolic dysfunction. In other words, since LA is directly exposed to LV diastolic dysfunction through the mitral valve, it is evident that the changes of LA function reflects the duration and severity of increased LA pressure following the increased age-related LV diastolic dysfunction. Must be also added that LA dimensions and functions can be better evaluated with a multimodality imaging approach including cardiac magnetic resonance (CMR) and computed tomography (CT). Finally, the recently developed three-dimensional speckle tracking could more easily and simultaneously define the effective motion of speckles in all directions. 
| References|| |
Abhayaratna WP, Steward JB, Appleton CP, Douglas PS, Oh JK, Tajik AJ, et al
. Left atrial size: Physiologic determinants and clinical applications. J Am Coll Cardiol 2006;47:2357-63.
Douglas PS. The left atrium: A biomarker of chronic diastolic dysfunction and cardiovascular disease risk. J Am Coll Cardiol 2003;42:1206-7.
Zhang Q, Yip GW, Yu CM. Approaching regional left atrial function by tissue Doppler velocity and strain imaging. Europace 2008;10:iii62-9.
Marwik TH, Leano RL, Brown J, Sun JP, Hoffman R, Lysyansky P, et al
. Myocardial strain measurement with 2-dimensional speckle-tracking echocardiography: Definition of normal range. JACC Cardiovasc Imaging 2009;2:80-4.
Vianna-Pinton R, Moreno CA, Baxter CM, Lee KS, Tsang TS, Appleton CP. Two-dimensional speckle tracking echocardiography of the left atrium: Feasibility and regional contraction and relaxation differences in normal subjects. J Am Soc Echocardiogr 2009;22:299-305.
Saraiva RM, Demirkol S, Buakhamsri A, Greenberg N, Popoviae ZB, N Thomas JD, et al
. Left strain measured by two-dimensional speckle tracking represents a new tool to evaluate left atrial function. J Am Soc Echocardiogr 2010;23:172-80.
Bryg RJ, Williams GA, Labovitz AJ. Effect of aging on left ventricular diastolic filling in normal subjects. Am J Cardiol 1987;59:971-4.
Teo SG, Yang H, Chai P, Yeo TC. Impact of left ventricular diastolic dysfunction on left atrial volume and function: A volumetric analysis. Eur J Echocardiogr 2010;11:38-43.
Westendorp RG. What is healthy aging in the 21 st
century? Am J Clin Nutr 2006;83:404S-9S.
Dominguez LJ, Barbagallo M. The cardiometabolic syndrome and sarcopenic obesity in older persons. J Cardiometab Syndr 2007;2:183-9.
Jadad AR, O'Gready L. How should health be defined? BMJ 2008;337:a2900.
Lang RM, Bierig M, Devereux RB, Flachskamps FA, Foster E, Pellikka PA, et al
., Chamber Quantification Writing Group, American Society of Echocardiographic's Guidelines and Standards Committee, European Association of Echocardiography. Recommendations for chamber quantification: A report from the American Society of Echocardiography's Guidelines and Standards Committee on the chamber quantification writing group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr 2005;18:1440-63.
Carlsson M, Ugander M, Mosen H, Buhre T, Aeden H. Atrioventricular plane displacement is the major contributor to left ventricular pumping in healthy adults, athletes, and patients with dilated cardiomyopathy. Am J Physiol Heart Circ Physiol 2007;292:H1452-9.
Lester SJ, Ryan EW, Schiller NB, Foster E. Best method in clinical practice and in search studies to determine left atrial size. Am J Cardiol 1999;84:829-32.
Isaaz K. Tissue Doppler imaging for the assessment of left ventricular systolic and diastolic function. Curr Opin Cardiol 2002;17:431-42.
Okamatsu K, Takeuchi M, Nakai H, Nishikage T, Salgo IS, Husson S, et al
. Effects of aging on left atrial function assessed by two-dimensional speckle tracking echocardiography. J Am Soc Echocardiogr 2009;22:70-5.
Tripokiadis F, Tentoolouris K, Andronlakis A, Trikos A, Toutouzas K, Kyriakidis M, et al
. Left atrial mechanical function in the healthy elderly: New insights from a combined assessment of changes in atrial volume and transmitral flow velocity. J Am Soc Echocardiogr 1995;8:801-9.
Zile MR, Brutsaert DL. New concepts in diastolic dysfunction and diastolic heart failure. Part I: Diagnosis, prognosis, and measurements of diastolic function. Circulation 2002;105:1387-93.
Kitzman DW. Heart failure with normal systolic function. Clin Geriatr Med 2000;16:489-512.
Quinones MA, Otto CM, Stoddard M, Waggoner A, Zoghbi WA, Doppler Quantification Task Force of the Nomenclature and Standards Committee of the American Society of Echocardiography. Recommendations for quantification of doppler echocardiography: A report from the Doppler Quantification Task Force of the Nomenclature and Standards Committee of the American Society of Echocardiography. J Am Soc Echocardiogr 2002;15:167-84.
Watanabe S, Suzuki N, Kudo A, Suzuki T, Abe S, Suzuki M, et al
. Influence of aging on cardiac function examined by echocardiography. Tohoku J Exp Med 2005;207:13-9.
Iskandrian AS, Hakki AH. Age-related changes in left ventricular diastolic performance. Am Heart J 1986;112:75-8.
Hirota Y. A clinical study of left ventricular relaxation. Circulation 1980;62:756-63.
Downes TR, Nomeir AM, Smith KM, Stewart KP, Little WC. Mechanism of altered pattern of left ventricular filling with aging in subjects without cardiac disease. Am J Cardiol 1989;64:523-7.
Matos J, Konzon I, Panagopoulos G, Perk G. Mitral annular plane systolic excursion as a surrogate for left ventricular ejection fraction. J Am Soc Echocardiogr 2012;25:969-74.
Tighe DA, Vinch CS, Hill JE, Meyer TE, Goldberg RJ, Aurigemma GP. Influence of age on assessment of diastolic function by Doppler tissue imaging. Am J Cardiol 2003;91:254-7.
Munagala VK, Jacobsen SJ, Mahoney DW, Rodeheffer RJ, Bailey KR, Redfield MM. Association of newer diastolic function parameters with age in healthy subjects: A population-based study. J Am Soc Echocardiogr 2003;16:1049-56.
Ommen SR, Nishimura RA, Appleton CP, Miller FA, Oh JK, Redfield MM. et al
. Clinical utility of Doppler echocardiography and tissue Doppler imaging in the estimation of left ventricular filling pressures: A comparative simultaneous Doppler-catheterization study. Circulation 2000;102:1788-94.
Amudsen B, Helle-Valle T, Edvardsen T, Trop H, Crosby J, Lyseggen E, et al
. Noninvasive myocardial strain measurement by speckle tracking echocardiography: Validation against sonomicrometry and tagged magnetic resonance imaging. J Am Coll Cardiol 2006;47:789-93.
Perk G, Tunick PA, Kronzon I. Non-Doppler two-dimensional strain imaging by echocardiography--from technical considerations to clinical applications. J Am Soc Echocardiogr 2007;20:234-43.
Mondillo S, Galderisi M, Mele D, Cameli M, Lomoriello VS, Zacà V, et al
., Echocardiography Study Group of The Italian Society of Cardiology (Rome, Italy). Speckle-tracking echocardiography: A new technique for assessing myocardial function. J Ultrasound Med 2011;30:71-83.
Rosca M, Lancellotti P, Popescu BA, Pierard LA. Left atrial function: Pathophysiology, echocardiographic assessment, and clinical applications. Heart 2011;97:1982-9.
Suga H. Importance of atrial compliance in cardiac performance. Circ Res 1974;35:39-43.
Spirito P, Maron BJ. Influence of aging on Doppler echocardiographic indices of left ventricular diastolic function. Br Heart J 1988;59:672-9.
Nikitin NP, Witte KK, Thackray SD, Goodge LJ, Clark AL, Cleland JG. Effect of age and sex on left atrial morphology and function. Eur J Echocardiogr 2003;4:36-42.
Rossi A, Zardini P, Marino P. Modulation of left atrial function by ventricular filling impairment. Heart Fail Rev 2000;5:325-31.
Cacciapuoti F, Marfella R, Paolisso G, Cacciapuoti F. Is the aging heart similar to diabetic heart? Evaluation of LV function of the aging heart with Tissue Doppler Imaging. Ageing Clin Exp Res 2009;21:22-6.
Anwar AM, Geleijnse ML, Soliman OI, Nemes A, ten Cate FJ. Left atrial Frank-Starling law assessed by real-time, three-dimensional echocardiography left atrial volume changes. Heart 2007;93:1393-7.
Spencer KT, Mor-Avi V, Gorcsan J 3rd, DeMaria AN, Kimball TR, Monagan MJ, et al
. Effects of aging on left atrial reservoir, conduit, and booster pump function: A multi-institution acoustic quantification study. Heart 2001;85:272-7.
Todaro MC, Khandheria BK. Left atrium: Still a neglected chamber? J Cardiovasc Echography 2014;24:72-7.
[Table 1], [Table 2]