Author + information
- Received June 27, 2016
- Accepted July 29, 2016
- Published online September 4, 2017.
- Cesare Russo, MDa,∗ (, )
- Zhezhen Jin, PhDb,
- Shunichi Homma, MDa,
- Tatjana Rundek, MD, PhDc,
- Mitchell S.V. Elkind, MD, MSd,
- Ralph L. Sacco, MD, MSd,e and
- Marco R. Di Tullio, MDa
- aDepartment of Medicine, Columbia University, New York City, New York
- bDepartment of Biostatistics, Columbia University, New York City, New York
- cDepartment of Neurology, Department of Public Health Sciences, Miller School of Medicine, University of Miami, Miami, Florida
- dDepartments of Neurology and Epidemiology, Columbia University, New York City, New York
- eDepartment of Human Genetics, Miller School of Medicine, University of Miami, Miami, Florida
- ↵∗Address for correspondence:
Dr. Cesare Russo, Columbia University Medical Center, Department of Medicine, Cardiology Division, 630 West 168th Street, PH-342, New York, New York 10032.
Objectives This study sought to assess the prevalence and prognostic value of abnormalities in left atrial (LA) phasic volumes and reservoir function in a community cohort.
Background LA enlargement is associated with adverse cardiovascular outcomes. Real-time 3-dimensional (RT3D) echocardiography allows assessment of LA phasic volumes and reservoir function. However, there is a paucity of data regarding normal values, clinical correlates, and prognostic value of RT3D echocardiography-derived LA phasic volumes and reservoir function, especially in the elderly, a subgroup at high risk for cardiovascular events.
Methods Left atrial maximum volume (LAVimax), minimum volume (LAVimin), and reservoir function assessed as emptying volume (LAEV), emptying fraction (LAEF), and expansion index (LAEI), were measured by RT3D echocardiography in participants from a community-based cohort study. Cut-off values for LA phasic volumes were derived from a healthy subgroup of participants free of cardiovascular disease and risk factors (n = 142; 66 ± 9 years of age; 55% women). Annual follow-up examinations were performed for cardiovascular outcomes (myocardial infarction, ischemic stroke, and vascular death).
Results The cohort included 706 participants (71 ± 9 years of age; 59% women). LAVimax and LAVimin were not associated with age in the healthy subgroup but progressively increased with age in the entire cohort (p < 0.001). During a median follow-up of 7 years (minimum 0.06, maximum 9.5 years), 78 cardiovascular events occurred. In univariate analysis, LAVimax, LAVimin, and reservoir function parameters were significantly associated with outcome. In multivariate analysis, LAVimin ≥20.5 ml/m2 (adjusted hazard ratio [aHR]: 1.79; 95% confidence interval [CI]:1.02 to 3.16) and LAEV ≤5.7 ml/m2 (aHR: 1.98; 95% CI: 1.02 to 3.85) remained significantly associated with events. LAVimin and LA reservoir function showed incremental prognostic value over that of LAVimax.
Conclusions LA phasic volumes and reservoir functions assessed by RT3D echocardiography were strong independent predictors of cardiovascular events in a community-based elderly cohort. LAVimin and reservoir function assessment may improve cardiovascular outcome prediction over LAVimax.
Left atrial (LA) enlargement is a strong risk factor for cardiovascular events (1–3). Among different measurements of LA size, LA volume showed the strongest association with adverse outcomes (4). Echocardiography is the imaging technique most frequently used to assess LA volume because of its widespread availability and reliable volume assessment. Conventionally, LA volume is measured at end-systole, when the left atrium reaches maximum expansion (LAVimax). The adoption of new technologies, such as real-time 3-dimensional (RT3D) echocardiography, has made it possible to measure the change in LA volume throughout the cardiac cycle and to assess the LA reservoir function. Growing evidence suggests that the analysis of LA volume in different phases of the cardiac cycle (LA phasic volumes) may provide additional, clinically relevant information regarding LA remodeling and dysfunction. In fact, the LA volume measured at end-diastole (left atrial minimum volume [LAVimin]) and the LA reservoir function have been demonstrated to be better correlates of left ventricular (LV) diastolic dysfunction and better predictors of incident atrial arrhythmias than LAVimax (5–7). However, it is not clear whether the assessment of LA phasic volumes and reservoir function can provide relevant prognostic information toward cardiovascular outcome, and if so, whether such information is incremental compared with the established LAVimax measurement. Furthermore, there is scarce information regarding normal values of LA phasic volumes and function derived from RT3D echocardiography, especially in the elderly population. Accordingly, this study investigated the prognostic value of LA phasic volumes and reservoir function measured by RT3D echocardiography in a community-based cohort composed of predominantly elderly subjects. Additionally, we assessed the incremental prognostic value of RT3D LA phasic volumes and reservoir function compared with conventional 2D parameters and risk factors.
The CABL (Cardiac Abnormalities and Brain Lesion) study based its recruitment on the NOMAS (Northern Manhattan Study), a population-based prospective study that enrolled 3,298 participants from the community living in northern Manhattan between 1993 and 2001. The study design and recruitment details of NOMAS have been described previously (8). Beginning in 2003, participants over 50 years of age without contraindications to magnetic resonance imaging (MRI) and without prior stroke were invited to participate in a brain MRI substudy. From September 2005 to July 2010, NOMAS MRI participants who voluntarily agreed to undergo an extensive cardiovascular evaluation including RT3D echocardiography were prospectively enrolled in CABL. Of 836 CABL participants with RT3D echocardiographic data available, 130 were excluded for technical reasons (suboptimal image quality for LA volume analysis), leading to the final study sample of 706 participants. Subjects excluded for suboptimal image quality had significantly higher body mass index (29.5 ± 5.5 kg/m2 vs. 28.0 ± 4.6 kg/m2, respectively; p < 0.001) and more frequently had diabetes (40% vs. 28%, respectively; p = 0.004) than the rest of the cohort but no significant differences were present in terms of age (71.3 ± 9.3 years vs. 72.5 ± 9.3 years, respectively), sex (60% vs. 65% women, respectively), hypertension (82% vs. 79%, respectively), hypercholesterolemia (72% vs. 66%, respectively), and coronary artery disease (6.8% vs. 6.3%, respectively; all p > 0.05). Written informed consent was obtained from all study participants. The study protocol was approved by the Institutional Review Boards of Columbia University Medical Center and of the University of Miami.
Risk factors and body size assessment
Cardiovascular risk factors were ascertained through direct examination and interview by trained research assistants. Hypertension was defined as systolic blood pressure ≥140 mm Hg or diastolic blood pressure ≥90 mm Hg, or self-reported history of hypertension or use of antihypertensive medication. Diabetes mellitus was defined as fasting blood glucose concentration of ≥126 mg/dl or self-reported history of diabetes or use of diabetes medications. Hypercholesterolemia was defined as total serum cholesterol >240 mg/dl, self-report of hypercholesterolemia, or use of lipid-lowering treatment. Atrial fibrillation was ascertained by electrocardiographic tracing at study enrollment or by history from medical records. Coronary artery disease was defined as history of myocardial infarction, coronary artery bypass grafting, or percutaneous coronary intervention. Body mass index (BMI) was calculated as weight (kilograms) divided by height (meters) squared. Race-ethnicity classification was based on self-identification and modeled after U.S. Census Bureau criteria.
Transthoracic echocardiography was performed using a commercially available system (model iE 33, Philips, Andover, Massachusetts) by a trained, registered cardiac sonographer according to a standardized protocol. LV end-diastolic wall thickness and dimension were measured from a parasternal long-axis view according to the recommendations of the American Society of Echocardiography (9), and LV mass was calculated with a validated method (10) and indexed by height2.7 (LV mass index). LA anteroposterior diameter was measured from the parasternal long-axis view and indexed by body surface area. Two-dimensional LA volume was measured using the biplane area-length method and indexed by the body surface area. LV volumes and LV ejection fraction were calculated using the biplane modified Simpson’s rule. Significant valve disease was defined as mitral or aortic regurgitation or stenosis that was at least moderate in severity. The transmitral early diastolic flow velocity assessed by pulsed-wave Doppler (E)-to-the mitral annulus early diastolic velocity assessed by tissue-Doppler (e′) ratio (E/e′) was used as an indicator of LV filling pressure and diastolic function as previously described (7,11).
Real-time 3-dimensional imaging was performed using a commercially available ultrasonography machine (model iE33, Philips) equipped with an X3-1 matrix array transducer. A detailed description of LA phasic volumes assessment by RT3D echocardiography has been published previously (7,12). Briefly, a pyramidal full volume was obtained from 4 subvolumes over 4 consecutive cardiac cycles. Sector dimensions and depth were set to include the whole left ventricle and the left atrium, allowing volume rates between 15 and 25 per second. Measurement of LA volumes was prospectively performed offline using commercially available software (QLAB Advanced Quantification version 8.1 software, Philips) by a single reader (C.R.) blinded to the study participants’ baseline clinical characteristics. Five anatomical landmarks (septal, lateral, anterior and inferior mitral annulus, and posterior wall of the LA) were manually identified by the operator, semiautomated border detection was performed using the software, and LA borders were tracked throughout the entire cardiac cycle. Manual corrections on all 3D planes were performed in case of inaccurate endocardial detection. Left atrial volume measurements were indexed by body surface area. LAVimax was measured at end-systole, and LAVimin was measured at end-diastole. Left atrial reservoir function was measured as LA emptying volume [LAEV = LAVimax − LAVimin], LA emptying fraction [LAEF = 100 × (LAVimax − LAVimin)/LAVimax], and LA expansion index [LAEI = 100 × (LAVimax − LAVimin)/LAVimin].
Follow-up and outcome assessment
All subjects were followed annually by telephone interview. Any vascular event or acknowledgment of neurological or cardiac symptom during the standardized interview triggered an in-person assessment. In addition, active hospital surveillance of admission and discharge International Classification of Diseases, 9th edition, codes was performed. Outcomes for this analysis were ischemic stroke, myocardial infarction, and vascular death. Stroke was defined by the first symptomatic occurrence of any type of stroke as defined by TOAST (Trial of Org 10172 in Acute Stroke Treatment) criteria (13). Diagnosis of ischemic stroke was determined by 2 neurologists independently, and disagreements were adjudicated by NOMAS principal investigators (R.L.S. and M.S.V.E.). Myocardial infarction was defined by criteria adapted from the Cardiac Arrhythmia Suppression Trial (14) and the Lipid Research Clinics Coronary Primary Prevention trial (15) and adjudicated by a study team cardiologist (M.D.T.). Death was classified as either vascular or nonvascular based on information from family, medical records, death certificate, and primary care physicians. Vascular causes of death were stroke, myocardial infarction, heart failure, pulmonary embolus, cardiac arrhythmia, and other vascular causes (8).
Data are mean ± SD for continuous variables and percentages for categorical variables. Linear regressions were used to assess relationships between atrial parameters and clinical and demographic variables. Cox proportional hazards models were used to test the associations between LA phasic volumes and incident cardiovascular events and between hazard ratios (HRs) and 95% confidence intervals (CIs). Multivariate models were built by selecting covariates from their univariate association with outcome. The likelihood ratio test was used with a series of nested Cox proportional hazards models to examine the incremental prognostic value of LA volumes and reservoir function, and models’ chi-square values were presented. Kaplan-Meier plots were used to assess event-free probability associated with LA volumes and reservoir function abnormalities, and the log-rank test was used to compare the curves. The percentiles used as cut-off values in the survival analysis were selected based on their significant associations with cardiovascular events while identifying the largest population at risk. For all statistical analyses, a 2-tailed p value <0.05 was considered significant. Statistical analyses were performed using SAS version 9.3 software (SAS Institute Inc., Cary, North Carolina).
Reproducibility of LA volume assessment
Reproducibility of LA volume measurements was assessed in 15 randomly selected subjects. LAVimin and LAVimax were remeasured by the original reader (C.R.) and by a second reader experienced in 3D echocardiography (A.T.) in a blinded fashion. Intraobserver intraclass correlation coefficients were 0.96 for LAVimin (95% CI: 0.88 to 0.99) and 0.94 for LAVimax (95% CI: 0.85 to 0.98). The mean differences between 2 measurements were 0.13 ± 1.79 ml/m2 for LAVimin (p = 0.78) and 0.42 ± 2.29 ml/m2 for LAVimax (p = 0.49). Interobserver intraclass correlation coefficients were 0.94 for LAVimin (95% CI: 0.85 to 0.98) and 0.95 for LAVimax (95% CI: 0.86 to 0.98). The mean differences between 2 measurements was 0.44 ± 2.27 ml/m2 for LAVimin (p = 0.46) and 0.52 ± 2.56 ml/m2 for LAVimax (p = 0.45).
The study cohort included 706 participants (71.2 ± 9.3 years of age; 59.5% women) with assessment of LA phasic volumes and function by RT3D echocardiography available. The reference subgroup consisted of participants without hypertension, cardiovascular disease, cardiac arrhythmias, significant valve disease, and in sinus rhythm at the time of enrollment (n = 142; 66 ± 9 years of age; 55% women). Clinical and echocardiographic characteristics of the study cohort are shown in Table 1.
Correlates of LA phasic volumes in the healthy subgroup and in the overall cohort
In the healthy subgroup, age did not show significant associations with LA volumes and reservoir function parameters (all p values >0.10). Both LAVimax (β = 0.22) and LAVimin (β = 0.13) were significantly greater in men than in women, with mean differences of 2.2 ml/m2 and 1.3 ml/m2, respectively (both p values <0.05), whereas LAEV, LAEF, and LAEI were not significantly associated with sex. LAVimax and LAVimin were not correlated with BMI, whereas LAEV, LAEF, and LAEI showed inverse correlation with BMI (all p values <0.05). Diabetes and hypercholesterolemia did not show any correlation with LA volumes and function.
Table 2 shows the clinical correlates of LA phasic volumes and reservoir functions in the entire study cohort. LA volumes increased with age, whereas LA function worsened with age (all p values <0.01). LAVimax, LAVimin, LAEF, and LAEI were significantly associated with systolic blood pressure, hypertension, atrial fibrillation, valve disease, and E/e′ ratio (all p values <0.05). LA volumes were larger in the presence of coronary artery disease (both p values <0.05). LAEV was inversely associated with BMI (p = 0.02), and atrial fibrillation (p < 0.001). LAEI was inversely correlated with diastolic blood pressure (p = 0.04). None of the LA parameters were significantly associated with sex.
Prevalence and prognostic value of LA phasic volumes abnormalities
During a mean follow-up of 6.5 years (median = 7.0, minimum = 0.06, maximum = 9.5 years), 78 cardiovascular events occurred, including 28 ischemic strokes, 13 myocardial infarctions, and 37 vascular deaths. Causes of death included 1 fatal stroke, 1 fatal myocardial infarction, 2 acute heart failures, 1 pulmonary embolus, 25 sudden death/cardiac arrhythmia, and 7 were scored as other vascular causes. Table 3 shows univariate and multivariate associations of demographics, risk factors, and echocardiography parameters with cardiovascular events. To assess the prognostic value of LA phasic volume parameters, we identified in the healthy reference group cut-offs corresponding to the 97.5th and 99th percentiles of LAVimax and LAVimin and the 2.5th and 1st percentiles of LAEV, LAEF, and LAEI distributions. Kaplan-Meier event-free survival plots for LA abnormalities are shown in Figure 1. All RT3D LA volumes and reservoir function abnormalities were significantly associated with outcome (all log-rank test p values <0.001). The prevalence of LA abnormalities in the overall cohort by using the different cut-offs and their ability to predict cardiovascular events in multivariate analyses is shown in Table 4. Abnormal LA parameters derived from two-dimensional echocardiography (LA diameter and 2D LAVimax) were not associated with events after adjusting for covariates, whereas RT3D-derived LAVImin ≥20.5 ml/m2 (adjusted HR: 1.79; 95% CI: 1.02 to 3.16) and LAEV ≤5.7 ml/m2 (adjusted HR: 1.98; 95% CI: 1.02 to 3.85) remained significantly associated with outcome.
Incremental prognostic value of 3D LA phasic volumes
The incremental prognostic value of LA parameters was assessed in progressive nested Cox proportional hazards regressions, and chi-square values are shown for each step in Figure 2. Two-dimensional LAVimax was not significantly incremental compared with LA diameter in predicting events (p = 0.08) (Figure 2A), whereas 3D LAVimax was incremental when added to the model (p = 0.01). Figure 2B shows that 3D LAVImin was incremental to LAVimax in predicting outcome (p < 0.001) and that LA reservoir function added further incremental prognostic value compared with LAVImin (p = 0.034 for LAEV, p = 0.009 for LAEF, and p = 0.007 for LAEI). Figure 2C shows the incremental prognostic value of 3D LA parameters in addition to risk factors. When added to a model including demographics and risk factors, LAVimin showed incremental prognostic value (p = 0.048), whereas LAVimax did not (p = 0.07). Among LA reservoir function parameters, LAEV showed a borderline trend in increasing prognostic information compared with that of LAVimin (p = 0.055).
In this study, we assessed the correlates and prognostic value of LA phasic volumes and reservoir function assessed by RT3D echocardiography in an elderly community-based cohort. We found that increased LA phasic volumes and reduced reservoir function were strong predictors of cardiovascular events in univariate analysis. In multivariate analyses adjusted for confounders and risk factors associated with outcome, RT3D-derived LAVimin and LAEV remained associated with events. In multivariate analysis, 2D echocardiographic parameters (LA anteroposterior diameter and 2D LAVimax) lost their significant associations with events. We also demonstrated that LAVImin and LA reservoir functions provided incremental prognostic value compared with LAVImax. Furthermore, our study is the first to provide and validate prognostically reference values for abnormal RT3D echocardiography-derived LA volumes and reservoir function parameters in the elderly.
LA enlargement is an established predictor of cardiovascular events, and its powerful predictive value reflects the effect on LA pressure of several diseases or conditions that in turn carry poor prognosis (16). Some of these conditions, such as hypertension, diabetes, and arterial stiffening, result in LV hypertrophy and LV remodeling, leading to the development of LV diastolic dysfunction, LV wall stiffening, and increased LV filling pressure, which in turn are the causes of LA enlargement over time (7,17–21). Higher BMI was also associated with lower LA reservoir function, likely due to the established effects of obesity on LV structure and function such as increased LV mass and subclinical systolic and diastolic dysfunction (11,22). Although most data for the prognostic value of LA enlargement derive from end-systolic LA assessment, considerable evidence is accumulating in favor of LAVimin as a better correlate of LV diastolic dysfunction and outcome (6,7). LAVimin is measured at end-diastole, when the LA is directly exposed to the LV pressure and when the LV is in a relaxed state. In a previous study, we demonstrated that LAVimin is a better correlate of LV diastolic dysfunction than LAVimax and that the latter is strongly affected by the longitudinal LV systolic function (7). Although the prognostic value of LA enlargement has been investigated previously, we are reporting for the first time the prognostic value of LA reservoir function. A reduced LA reservoir function is associated with hypertension, LV hypertrophy, LV diastolic dysfunction, and other cardiovascular risk factors and therefore could be a surrogate marker of cardiovascular risk (6,7,23). Because the LV longitudinal systolic function is a major determinant of the LA reservoir function (7), it can be hypothesized that a reduction in reservoir function might indicate LV longitudinal systolic dysfunction, a known predictor of cardiovascular events (24–26). Besides being possibly explained by the same underlying disease, such as small vessel disease and atherosclerotic changes in various arterial territories, the link between LA reservoir function and cardiovascular events could also involve cardioembolism as another possible cause in some cases. In fact, in a previous study we demonstrated that a reduced LA reservoir function is associated with silent brain infarctions and cerebral white matter disease detected by magnetic resonance imaging (23). Furthermore, LA reservoir function also has been associated with future incidence of atrial arrhythmia, which may in part mediate the association with cardiovascular events (5).
The prognostic value of LA enlargement has been investigated in several previous studies. Increased M-mode anteroposterior linear dimension has been linked to adverse cardiovascular outcome (1–3), although LA volume has generally shown better correlation with outcome than linear dimensions (4). Very few studies, however, assessed the prognostic value of LA phasic volumes so far, and no study so far has investigated the prognostic value of LA reservoir function. Recently, Wu et al. (27) found that in Japanese patients referred to clinical echocardiography for assessment of underlying cardiac disease, LAVimax and LAVimin were not associated with cardiac death in multivariate analysis but were associated with a composite of cardiovascular events including heart failure admissions during a follow-up of ≈2.5 years. In another study in 178 patients referred for clinical echocardiography, Caselli et al. (28) showed that LAVimax and LAVimin were associated with cardiovascular events with similar HRs (1.06 and 1.05, respectively) over a follow-up period of 45 months.
Measurement of LA phasic volumes is not currently part of a routine echocardiographic examination. However, the present and previous studies show that measuring LA phasic volumes can significantly improve cardiovascular risk stratification. RT3D echocardiography is gaining popularity in the clinical setting, and modern software is becoming faster and more user-friendly. The feasibility of measuring LAVImin by RT3D echocardiography, together with the large body of evidence showing its superiority compared to LAVImax as an indicator of LA remodeling and its strong prognostic value, support the case for LAVimin to replace LAVimax for cardiovascular risk prognostication in routine echocardiographic exams.
The main strengths of our study are the prospective design, the long follow-up, the large number of subjects studied with RT3D echocardiography, the wide range of cardiovascular risk profiles present in our population, the multi-ethnic composition of our study sample, and the confirmation of our findings after adjustment for multiple covariates. However, our study also has limitations. Our study population included subjects over 50 years of age and with high mean BMI and high prevalence of risk factors; therefore the results might not apply to younger, healthier populations. Furthermore, because of the imbalance in race-ethnic distribution in our cohort, an analysis in different race-ethnic groups was not performed. In 15% of the population, suboptimal image quality prevented 3D assessment of LA parameters. Although similar rates have been described in other studies, this is a common limitation of ultrasound assessment, especially in population-based studies. Finally, outcome analysis for separate type of events was not performed due low number of events in each category.
LA phasic volumes and reservoir function were strong predictors of future cardiovascular events in a predominantly elderly community-based cohort. The prognostic value of LA volumes and reservoir function was independent of confounders and cardiovascular risk factors. Among LA volume parameters, LAVimin was a stronger predictor of events than LAVimax, and was incremental to it. LA reservoir function was also incremental to LA volumes in the prediction of cardiovascular events. The assessment of LA phasic volumes by RT3D echocardiography may improve cardiovascular risk stratification in the elderly.
COMPETENCY IN MEDICAL KNOWLEDGE: Assessment of the LA cavity volume is traditionally performed at the end-systolic phase of the cardiac cycle (LAVimax). Recent evidence suggest that LA end-diastolic volume (LAVimin) provides a better correlate of LA remodeling and is more closely correlated with LV diastolic dysfunction. In this study, we provided normal reference values for RT3D-derived LA volumes and reservoir function in subjects over 50 years of age. Furthermore, we provided prognostic validation of those reference values in a community setting, and demonstrated that LAVmin and LA reservoir function were stronger predictors of cardiovascular outcome and showed incremental prognostic value over LAVmax.
COMPETENCY IN PATIENT CARE AND PROCEDURAL SKILLS: RT3D echocardiography is a feasible method that allows fast and precise measurement of LAVmax, LAVmin, and LA reservoir function without geometric assumptions. A widespread use of this technique will make 3D assessment of cardiac chambers a standard procedure with the advantage over 2D assessment of improving cardiovascular risk stratification.
TRANSLATIONAL OUTLOOK: The assessment of LA phasic volumes has the potential of improving cardiovascular risk stratification. LAVimin and LA reservoir function have shown superior ability than LAVimax to predict cardiovascular events and incidence of atrial fibrillation. We provide, for the first time, normal reference values for LA phasic volumes by RT3D echocardiography in subjects from a community cohort study. These reference values will contribute to an improved cardiovascular risk stratification in subjects from the general population.
The authors thank Janet De Rosa, MPH (project manager), Rafi Cabral, MD, Michele Alegre, RDCS, and Palma Gervasi-Franklin (collection and management of the data).
This work was supported by U.S. National Institutes of Health/National Institute of Neurological Disorders and Stroke grant R01 NS36286 to Dr. DiTullio and grant R37 NS29993 to Drs. Sacco and Elkind, and by NIH/National Center for Advancing Translational Sciences, grant UL1 TR000040. Dr. Elkind is a consultant for Biotelemetry/Cardionet, BMS-Pfizer Partnership, Boehringer Ingelheim, Daiichi-Sankyo, Janssen Pharmaceuticals, and Sanofi-Regeneron; serves on the National, Founders Affiliate, and New York City chapter boards of the American Heart Association/American Stroke Association; and receives royalties from UpToDate for chapters related to cryptogenic stroke. Dr. Sacco has received research support from Boehringer Ingelheim. All other authors have reported that they have no relationships relevant to the contents of this paper to disclose.
- Abbreviations and Acronyms
- left atrial
- left atrial emptying fraction
- left atrial expansion index
- left atrial emptying volume
- left atrial maximum volume
- left atrial minimum volume
- real-time 3-dimensional
- Received June 27, 2016.
- Accepted July 29, 2016.
- 2017 American College of Cardiology Foundation
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