© 2014, Wiley Periodicals, Inc. DOI: 10.1111/echo.12515

Echocardiography

Left Ventricular Remodeling and Dysfunction in Systemic Lupus Erythematosus: A Three-Dimensional Speckle Tracking Study Bao-Tao Huang, M.D., Hong-Mei Yao, M.D., and He Huang, M.D. Department of Cardiology, West China Hospital, Sichuan University, Chengdu, China

Objective: To analyze left ventricular (LV) global structure and systolic function in patients with systemic lupus erythematosus (SLE) using the three-dimensional (3D) speckle tracking imaging. Methods: Thirty-four SLE patients and 34 healthy subjects underwent 3D echocardiography to obtain LV ejection fraction (LVEF), sphericity index, 3D LV mass, 3D global longitudinal strain (GLS), global circumferential strain (GCS), global area strain (GAS), and global radial strain (GRS). Disease activity was evaluated for all SLE patients by SLEDAI 2000 (SLEDAI-2K) score. Results: Age, gender, height, weight, diastolic blood pressure, and two-dimensional (2D) LVEF were similar between the 2 groups. Despite no difference was found for sphericity index between the groups, 3D LV mass was increased in SLE patients. All components of strain were significantly reduced in SLE patients. Peak systolic GLS, GCS, GAS, and GRS in SLE patients and controls were 18.2  2.9% versus 21.4  2.5%, 18.4  3.1% versus 20.6  2.5%, 32.2  4.4% versus 36.6  3.4%, and 51.4  10.2% versus 61.9  10.0%, respectively (all P < 0.01). In multivariable regression analysis, SLE was independently associated with GAS (P < 0.001). In SLE patients, peak systolic GLS, GAS, GRS was significantly decreased in those with severe disease activity than among inactivity/mildly activity (all P < 0.05). GLS was independently correlated with SLEDAI score (P = 0.001). Conclusion: Three-dimensional speckle tracking imaging is a new simple, rapid method to indentify early abnormalities in SLE patients who may have normal LV systolic function with 2D echocardiography. (Echocardiography 2014;31:1085–1094) Key words: cardiovascular disease, systemic lupus erythematosus, ultrasound Systemic lupus erythematosus (SLE) is a connective tissue disease with several visceral organs involved. Multiple autoantibodies cause heart damage directly or via trigger mechanism such as atherogenic way.1 Thirty years ago, Urowitz et al.2 put forward a concept of “the bimodal pattern of mortality” in patients with SLE, in which an early peak was related to disease activity or infections, and the late one was associated with atherosclerotic heart disease. With the use of glucocorticoid, death due to infection and active disease has decreased, whereas heart involvement has been playing a leading role in shortening SLE survival. SLE cardiomyopathy may cause arrhythmias, dilated cardiomyopathy, or heart failure, being an independent predictor of death in SLE patients.3 Autopsy results have shown that myocardial involvement is present in as many as 40–50% of SLE patients;4 however, clinically, only 7–10% of SLE myocardial injury is Address for correspondence and reprint requests: He Huang, M.D., Department of Cardiology, West China Hospital, Sichuan University, 37 Guoxue Street, Chengdu 610041, Sichuan, China. Fax: 86-28-85422253; E-mail: [email protected]

found.5 The majority of SLE cardiomyopathy goes undiagnosed for the reasons that it usually begins in a stealth mode with no symptoms or warning signs, the laboratory test is insensitive and nonspecific, and heart biopsy may not be used for routine screening. Chinese SLE Epidemiology Staged Registry Studies, reported in 2011 by Chinese SLE Treatment and Research Group (CSTAR), have shown that China is now the world’s second largest SLE epidemic region, with a prevalence ranging from 30 to 70 per 100 000, after that of blacks (100 out of 100 000).6 Looking for a noninvasive method for early detecting SLE cardiomyopathy is urgently needed. Previous studies have proven the potentials of cardiac magnetic resonance (CMR),7,8 tissue Doppler imaging (TDI),9 and two-dimensional strain (2D strain)10 in detecting myocardial damage of SLE patients in a subclinical stage. However, CMR is time consuming and expensive, thus the application is subjected to certain restrictions. Clinically, TDI has been widely used to evaluate the myocardial movement with the advantages of simple operation, high repeatability, and good performance in distinguishing 1085

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cardiac dysfunction; however, this technique is less reproducible for nonbasal segments of myocardium, moreover, it is angle dependent and vulnerable to surrounding tissue force.11 Two-dimensional strain detects speckle patterns of myocardial tissue on ultrasound images frameby-frame, irrespective of angle dependency. Nevertheless, detection of 2D speckle is impaired by out of plane motion.12 Recently, three-dimensional (3D) speckle tracking imaging is a breakthrough for evaluating the cardiac structure and mechanical motion. With the semiautomatic tracking model, it can provide the results of 3D strain, left ventricular ejection fraction (LVEF), 3D LV mass, spherical index, and other quantitative parameters simultaneously. The use of 3D speckle tracking imaging in the studies of hypertension,13 coronary heart disease,14 cardiomyopathy,15,16 etc. has displayed the good sensitivity and clinical value. The objective of this study was to investigate global changes of LV geometry and function using 3D speckle tracking imaging in SLE patients. Methods: Patients and Controls: Thirty-four patients with SLE were included in the study from the Department of Rheumatology and Immunology at West China Hospital, Sichuan University, Chengdu, China. The diagnosis of SLE complied with at least 4 classification criteria for SLE recommended by the American College of Rheumatology in 1997. Exclusion criteria including renal insufficiency (blood creatinine > 1.25 mg/dL), coronary artery disease (clinical diagnosis or significant segmental motion abnormalities at echo), valvular disease (greater than mild regurgitation), coexistence with other connective tissue diseases, and moderate or large amount of pericardial effusion. Patients with known dilated cardiomyopathy, reduced 2D EF or bundle branch block on the electrocardiogram were excluded. Given that the accuracy of 3D measurements is highly dependent on image quality, we also excluded the patients with poor acoustic window or arrhythmia. Thirty-four healthy controls came from the hospital staffs or healthy check-up, absent of cardiovascular disease, diabetes, or chronic kidney disease (CKD). The electrocardiogram (MAC 1200ST, GE Healthcare, Bangalore, India) and conventional echocardiography seen in ”standard 2D echocardiographic examination” examination were normal. The study procedures followed were in accordance with the Helsinki Declaration and were approved by the institute review board of West China Hospital, Sichuan University. 1086

Clinical Evaluation of SLE Patients: Clinical data of every patient, including medical history, physical examination, and laboratory data were collected and analyzed with Systemic Lupus Erythematosus Diseases Activity Index 2000 (SLEDAI 2000, SLEDAI-2K).17 SLEDAI-2K score was marked according to the presence of related symptoms of 9 organ systems in the past 10 days. Each sign or symptom is given a weighted score, and the sum of the score for the total 24 items is the SLEDAI-2K score, ranging from 0 to 105. Disease activity is classified into 4 categories: inactive (score 0–4), mildly active (score 5–9), moderately active (score 10–14), or severely active (score ≥ 15). Standard 2D Echocardiographic Examinations: Standard 2D echocardiographic examinations were performed in all subjects with a M5S-D probe using a Vivid E9 BT11 ultrasound system (GE Healthcare, Horten, Norway). Three consecutive cardiac cycles were stored in cine loop format for analysis. LV end-diastolic inner diameter (LVEDD), LV end-diastolic septal (IVSd), and posterior wall thickness (LVPWd) were measured according to the recommendations of the American Society of Echocardiography. LV mass was calculated with the formula: LVmass ¼ 0:8f1:04 ½ðLVEDD þ LVPWdþ IVSdÞ3  ðLVEDDÞ3 g þ 0:6g, LV mass was indexed for height powered to 2.7. Relative wall thickness was the ratio of 2 9 LVPWd to LVEDD. LVEF was measured with corrected Teichholz formula. LV diastolic function was evaluated by analysis of mitral Doppler inflow and TDI at the septal and lateral mitral annulus. Three-Dimensional Speckle Tracking Imaging: Three-dimensional echocardiography data were acquired with a 4D volume probe (4V-D). The minimum frame rate (volume/sec) was no less than 40% of the subjects’ heart rate for reliable recognition of speckles. Full-volume imaging at apical four-chamber view was obtained with a special attention on encompassing the entire LV cavity in the dataset. We used the 4D automatic LV quantification software package equipped with GE Vivid E9 BT11 ultrasound system to analyze the collected data online. The results were acquired as follows: (1) Alignment: rapid automatic alignment in order that the corresponding intersection line of four-, two-, and three-apical views was placed in the middle of the LV cavity. (2) The software automatically generated an end-diastolic and an end-systolic endocardial border trace, appropriate manual adjustment was conducted when necessary. (3) The software automatically generated the results of LV volume, LVEF, and spherical

LV Abnormalities in SLE

(A)

(B)

Figure 1. Automatic 3D left ventricular ejection fraction (LVEF) measurements and 3D LV mass. A. The 4D Auto LVQ software automatically generates an end-diastolic and an end-systolic endocardial border trace, and provides the results of end-diastolic volume (EDV), end-systolic volume (ESV), ejection fraction (EF), stroke volume (SV), cardiac output (CO), and spherical index. B. The 4D Auto LVQ software automatically traces the endocardial border and epicardial border of LV, and calculates the end-diastolic LV mass. 3D LV mass is indexed for the body surface area.

Figure 2. 3D strain. The 4D Auto LVQ software automatically calculates LV 3D global longitudinal strain (GLS), global circumferential strain (GCS), global area strain (GAS), global radial strain (GRS), and provides a color-coding 17 segment bulls eyes.

index (LV end-diastolic volume/volume of the sphere calculated from the end-diastolic LV maximum diameter) (Fig. 1A). (4) Epicardial border was traced automatically, if necessary, we made manual corrections. End-diastolic LV mass was automatically calculated and a region of interest (ROI) was defined. 3D LV mass was indexed for the body surface area (Fig. 1B). (5) The analysis permitted to obtain LV 3D global longitudinal strain (GLS), global circumferential strain (GCS),

global area strain (GAS), global radial strain (GRS), and a color-coding 17 segment bull’s-eyes (Fig. 2). Statistical Analysis: We used PASW Statistics 18.0 software for statistical analyses. Quantitative variables were expressed as mean  standard deviation. Qualitative data were shown as absolute numbers (percentages). Statistical significance was 1087

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calculated using independent samples t-test, one-way analysis of variance, or chi-square tests. Bivariate correlation analysis was performed to determine the relationship between 3D strain and 3D EF, GAS and clinical data, SLEDAI and 3D strain. Dichotomous variables such as presence of the SLE or gender were treated as dummy variables and assigned values of 1 (female, presence of SLE) or 0 (male, absence of SLE). We conducted multiple linear regression analysis to determine the independent predictors of GAS and SLEDAI. Inter-observer variability and intraobserver variability were examined using the intraclass correlation coefficient. A P value of

Left ventricular remodeling and dysfunction in systemic lupus erythematosus: a three-dimensional speckle tracking study.

To analyze left ventricular (LV) global structure and systolic function in patients with systemic lupus erythematosus (SLE) using the three-dimensiona...
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