Skip to main content

Three-dimensional speckle tracking echocardiography for evaluation of ventricular function in patients with systemic lupus erythematosus: relationship between duration of lupus erythematosus and left ventricular dysfunction by using global longitudinal strain



Cardiovascular diseases are leading causes of morbidity and mortality in patients with systemic lupus erythematosus (SLE). Cardiac involvement in SLE can often go undetected. Three-dimensional (3D) speckle tracking echocardiography (STE) is a noninvasive imaging technique that can assess the function of the heart’s ventricles in an accurate and reproducible way. This makes it an attractive option for detecting early signs of heart disease in SLE patients. By identifying these subclinical cardiac abnormalities, 3D-STE may help reduce the negative impact of cardiovascular diseases in SLE population. Therefore, this study aimed to compare the left ventricular (LV) function between patients with SLE compared to age- and gender-matched controls using two-dimensional (2D) and 3D-STE.


The current study found no significant differences in left ventricle ejection fraction, left ventricle end-diastolic volume, left ventricle end-systolic volume, left ventricle end-diastolic mass, and left ventricle end-systolic mass between the two groups. However, the SLE group exhibited a significantly lower LV global longitudinal strain (GLS) compared to the control group according to all types of echocardiographic assessments, including 3D and 2D long-axis strain, apical 2-chamber, and apical 4-chamber assessments (all P values < 0.05). Furthermore, a good inter-rater reliability and intra-rater reliability were observed regarding the LVGLS measurement with 3D-STE. Additionally, the study identified a significant correlation between LVGLS and SLE duration (r (50) = 0.46, P < 0.001). The use of prednisolone and nephrology disorders was also found to impact LVGLS measurements.


Despite a normal LVEF in patients with SLE, LVGLS measurements indicated that LV systolic dysfunction was observed more frequently in SLE patients compared to their healthy counterparts. Therefore, advanced 3D-STE techniques may be useful in identifying subtle abnormalities in LV function in SLE patients.


Systemic lupus erythematosus (SLE) is a chronic, relapsing, inflammatory connective tissue disorder resulting in multi-organ involvement, including the skin, kidney, and serosal membranes [1]. Although SLE can affect individuals of any age or gender, it is more commonly observed in young women [2]. Despite extensive research, the precise etiology of SLE remains unclear, with genetic, environmental, and infectious factors all playing a potential role [3]. It is well established that SLE associates with cerebrovascular accidents [4, 5] and cardiovascular diseases (CVDs) [6, 7], increasing the risk of myocardial infarction (MI) by 10 times compared to the general population [8] and making CVDs one of the leading causes of death among these patients [9]. Contributing factors to this increased risk include immune dysregulation, endothelial dysfunction, defective vascular repair mechanisms [10], as well as classic risk factors of CVDs [8].

SLE patients frequently present with a variety of cardiac manifestations, including coronary artery disease (25–45%), Libman–Sacks endocarditis (13–74%), pericarditis (12–24%), myocarditis (10–40%), congestive heart failure (7–36%), and cardiac tamponade (< 3%) [11]. Recent meta-analyses have also shown a high prevalence of left ventricle (LV) dysfunction among SLE patients, even with a normal left ventricular ejection fraction (LVEF) [12,13,14]. Despite advances in medical treatments for SLE, their CVD-related mortality has remained unchanged, leading to considerable challenges in predicting and managing cardiac issues [15]. Moreover, traditional approaches to risk assessment, such as the Framingham risk score, have limited utility in predicting CVD events among SLE patients [8]. Consequently, there is an imperative need for refined techniques to evaluate cardiac function with greater precision in this population. Cardiac magnetic resonance (CMR) [16, 17] and tissue Doppler imaging (TDI) [18] have been proposed as viable methods for detecting subclinical CVDs in SLE patients. However, CMR is not generally employed due to its time-consuming nature and high costs [14]. On the other hand, while TDI is more acceptable, its results might be less reproducible for basal segments of the heart since it is angle-dependent and vulnerable to the force of surrounding tissues [19]. Two-dimensional (2D) speckle tracking echocardiography (STE) is an alternative noninvasive method, but it is prone to out-of-plane motion, limiting its reproducibility [20]. In contrast, three-dimensional (3D) STE has emerged as a promising, noninvasive, cost-effective, and precise technique for evaluating cardiac function. Unlike 2D-STE, the 3D-STE approach enables the tracking of speckle patterns that move out of the echocardiographic imaging plane, resulting in improved reproducibility and accuracy [21].

In light of this information, the current study aimed to evaluate the LV function of SLE patients using the novel and reproducible 3D-STE technique to improve the early detection and management of CVD in this population.


The current case–control study was performed between September 2016 and March 2017. Patients with SLE who met the inclusion criteria were recruited and were compared with a control group of healthy individuals.

Inclusion criteria

  • SLE diagnosis was made at least three years ago

  • Aged more than 18

  • No history of prior known cardiovascular diseases

  • Being interested in participating in the study

Exclusion criteria

  • Any abnormality in electrocardiogram or chest X-ray

  • The existence of any cardiac murmur or extra sounds in cardiac auscultation

  • Patients with an improper full-volume view of 3D-STE

Following a thorough physical examination and a review of medical records by a rheumatologist, the SLE group participants were selected according to the updated American College of Rheumatology criteria for SLE diagnosis [22, 23]. A total of 106 participants, consisting of 53 SLE patients and 53 healthy controls, were included in this study. One participant in the SLE group was excluded due to inadequate echocardiographic views. The SLE and control groups were matched for age and gender.

Data collection

All patients underwent a comprehensive evaluation for rheumatologic and cardiovascular status. The SLE group’s medical history, drug history, and systemic involvement data were obtained from their medical records. Data on SLE risk factors, such as age, gender, history of hypertension, hyperlipidemia, smoking, and family history of SLE, as well as current SLE-related medications, symptoms, disease duration, and laboratory tests, were collected through face-to-face interviews and review of patients’ medical records.

Echocardiographic assessments

Participants underwent comprehensive echocardiography using 2D-STE, 3D-STE, and TDI imaging with speckle tracking analysis to assess LV parameters, such as LVEF and LV size. A Vivid E9 ultrasound machine (GE Vingmed Ultrasound, Horten, Norway) equipped with a 3.5-MHz 4V-D cardiac sector probe was utilized for transthoracic echocardiography. In accordance with the guidelines set forth by the American Society of Echocardiography, volumetric echocardiographic data were collected over 4 to 6 cardiac cycles using a zoomed apical 4-chamber view of the LV (A4C) [24]. Subsequently, 4D Auto LVQ software (EchoPAC BT13, GE Vingmed Ultrasound, Horten, Norway) was utilized for volume analysis to determine left ventricular end-diastolic volume (LVEDV), left ventricular end-systolic volume (LVESV), and LVEF. Three points for each apical plane were required, consisting of two points at the edges of the mitral annulus and one at the apex, initially in end-diastolic frames and subsequently in end-systolic frames. The software automatically delineated the LV endocardial border in a 3D model from the end-diastolic and end-systolic phases, and manual adjustments were made when required due to inadequate automatic delineation. Left ventricular global longitudinal strain (LVGLS) was measured by performing a second epicardial tracking, and LV mass and strain were assessed by automatically delineating the region of interest. The software automatically determined the LVGLS and borders, and manual adjustments were made if the automatic delineation was deemed inaccurate.

An automated functional imaging method was used for 2D-STE LVGLS measurements. Three separate apical views, including the A4C, apical 2-chamber (A2C), and apical long-axis (LAX) views, were recorded for every patient, with a minimum frame rate of 50 frames per second. The margins of the endocardium were automatically demarcated in each picture, and the mitral annulus and LV apex were located. The region of interest was manually adjusted by the operator if needed. The mobility of the myocardium within each area of focus was then evaluated using STE. Each ventricular segment’s peak systolic longitudinal strain was calculated, and the results were combined into a bull’s-eye template using a 17-segment model. By computing the mean longitudinal strain across each of the 17 segments, the average global longitudinal peak systolic strain for the complete LV was calculated [25].

Moreover, to evaluate inter- and intra-rater variability as an indicator of method reproducibility, 26 randomly selected patients from the SLE group underwent 3D-STE the following week by both the first assessor and another cardiologist. The second cardiologist was blind to the previous echocardiographic measurements of patients.

Statistical analysis

Descriptive statistics are used to present the data, with frequencies and percentages for categorical variables and means and standard deviations for continuous variables. The normality of the data distribution and the equality of variances were assessed using the Kolmogorov–Smirnov and Levene’s tests, respectively. The inter-rater reliability and intra-rater reliability of the measurements were evaluated using the intraclass correlation coefficient (ICC) with a two-way fixed model of absolute agreement. Additionally, Koo and Li’s recommendation to interpret the ICC values was followed [26], where ICC < 0.5 indicates a poor correlation, 0.5 ≤ ICC < 0.75 indicates a moderate correlation, 0.75 ≤ ICC < 0.9 indicates a good correlation, and ICC ≥ 0.9 indicates an excellent correlation. The independent samples t test and Chi-square test were performed to compare continuous and categorical variables between the two groups. IBM SPSS Statistics for Windows version 27 (Armonk, NY, USA) was used, and statistical significance was defined as P values less than 0.05.


The SLE and control group aged 40.33 ± 8.98 years and 38.88 ± 11.01 years, respectively. The majority of participants were female in both groups. Table 1 presents baseline characteristics, including age, sex, body mass index, heart rate, past medical history, habit history, and familial history, indicating no significant differences between the SLE and control groups, showing a proper matching between SLE and control group (all P values > 0.05).

Table 1 Baseline characteristics of study participants

Clinical characteristics of the SLE group

The mean duration of SLE diagnosis was 15.11 ± 9.89 years. The most common systemic involvements were musculoskeletal (86.5%) and dermatologic (78.8%) disorders. Among the SLE patients, pericardial effusion was observed in two cases (3%). Prednisolone was the most frequently prescribed medication (92.2%), while nonsteroidal anti-inflammatory drugs (NSAIDs) were the least frequently used (15.4%) (Table 1).

Echocardiographic findings

We found no significant difference between the SLE and control groups in terms of LVEDV (P value: 0.45), LVESV (P value: 0.14), LVEF (P value: 0.19), left ventricular stroke volume (LVSV) (P value: 0.16), left ventricular cardiac output (LVCO) (P value: 0.44), left ventricular end-diastolic mass (LVEDM) (P value: 0.26), and left ventricular end-systolic mass (LVESM) (P value: 0.55). However, we observed statistically significant lower values for LVGLS in the 3D view (P value < 0.001), 2D LVGLS in LAX view (P value < 0.001), A4C view (P value: 0.009), and A2C view (P value < 0.001) among SLE patients in comparison with the control group (Table 2).

Table 2 Echocardiographic findings of study subjects

Inter-rater and intra-rater reliability of the measurements

Our analysis demonstrated an excellent correlation (all ICCs > 0.9) for LVEDV, LVESV, and LVEF measurements. Furthermore, good inter-rater reliability and intra-rater reliability were observed regarding LVGLS measurements using 3D-STE with ICCs of 0.75 and 0.76, respectively (Table 3).

Table 3 Inter-rater and intra-rater reliability of echocardiographic measurements in SLE patients

Comparing other variables

No significant differences were found in the LVGLS measurements in the 3D view among SLE patients who were taking methotrexate, NSAIDs, or immunosuppressive drugs compared to those who were not taking these medications. Similarly, no differences were found in LVGLS measurements between SLE patients who had discontinued their medication and those who were still taking SLE-related medications. However, we observed a significant difference regarding LVGLS measurements between patients taking prednisolone and those not (P value: 0.02) (Table 4). Furthermore, SLE patients with nephrologic complications had significantly lower LVGLS measurements in the 3D view (P: 0.03) compared to those without nephrologic complications (Table 5).

Table 4 Effects of SLE medications on LVGLS
Table 5 Effects of SLE systemic involvements on LVGLS

Moreover, a positive and significant correlation was found between the duration of SLE disease diagnosis and LVGLS measurements in the 3D view (r (50): 0.46, P value < 0.001) (Fig. 1).

Fig. 1
figure 1

Three-dimensional full-volume echocardiography


The heightened risk of cardiovascular disease and adverse outcomes in patients with SLE is well established [4, 6, 7]. However, the lack of quantifiable measures of early myocardial damage has hindered the ability to guide interventions [8]. The measurement of LVGLS in a 3D view is a relatively novel, accurate, and operator-independent approach to evaluate LV function with 3D-STE. Despite the potential benefits of LVGLS, there is limited information on its use in SLE patients (Figs. 2, 3, 4).

Fig. 2
figure 2

Tracing of the endocardial border is performed, both in the long and short axis of the ventricle in systole and diastole, for volumetric assessment of left ventricle. In right panel, volume time-plot and quantitative analysis and 3D model are presented

Fig. 3
figure 3

AutoLVQ plane after segmentation process in left panel. Bull’s-eye reconstruction of 3D-LVGLS in right panel

Fig. 4
figure 4

Correlation between LVGLS and SLE duration among study participants

The current study did not find a significant difference between the SLE patients and controls regarding LVEDV, LVESV, LVEDM, LDESM, and LVEF. Similarly, in a study of 45 SLE patients by Poorzand et al., no considerable difference was found between SLE and control groups concerning LVEF, LVEDV, and LVESV [27]. Nikdoust et al. [28] also showed that LVEF is not markedly affected in SLE patients compared with a healthy population. However, other studies have yielded conflicting results. For example, Deng et al. [13] observed marked increases in LVESV and left ventricular mass (LVM) and a decrease in LVEF in the SLE group compared with the control group, while LVEDV did not differ between the groups. In another study of juvenile-SLE patients, LVEF measurements were not reduced, while LVM was increased compared to healthy individuals [29]. Given the contradictory findings, further extensive studies are needed to draw a definitive conclusion.

LVGLS has been proposed as a sensitive factor for predicting cardiovascular events, such as MI, ventricular hypertrophy, and drug-induced cardiac toxicity [30, 31]. Consequently, LVGLS has gained increased attention as a predictive factor for CVDs in SLE patients. Huang et al. conducted a study in 2014 comparing the LV function of 50 SLE patients and 50 healthy individuals using 3D-STE. They found significantly lower LVGLS measurements in SLE patients [14]. Similarly, Gegenava et al. demonstrated that left ventricular LVGLS was significantly impaired as a marker of systolic impairment in SLE patients and could be utilized as a new tool to predict CVDs in this population [32]. Poorzand et al. and Bulut et al. also reported significantly lower LVGLS measurements in SLE patients compared to healthy controls [27, 33]. Consistent with these findings, our study also revealed markedly reduced LVGLS in the SLE group compared to the control group. While LVEF did not differ between SLE patients and controls, the differences in LVGLS findings suggest that 3D-STE measurement of LVGLS may be a better predictor of CVDs in SLE patients.

The reproducibility of novel methods is often a concern for clinicians. In previous studies, 3D-STE has been shown to be a reliable and precise method for measuring cardiac function in both adult and pediatric populations [34,35,36,37,38,39]. In agreement with previous researches, our investigation demonstrated favorable inter- and intra-rater reliability levels in evaluating cardiac parameters with 3D-STE. These findings suggest that this imaging technique is a dependable and consistent tool for monitoring and assessing cardiac function in patients over time.

Our study revealed a noteworthy finding regarding the impact of corticosteroid treatment on LVGLS measurements, with patients taking oral corticosteroids showing a significant reduction in LVGLS compared to those not receiving corticosteroids. Previous studies have demonstrated a strong association between corticosteroid use and an elevated risk of adverse cardiovascular events, including MI and angina [6]. Moreover, it has been suggested that corticosteroid use is linked to an increased risk of carotid plaque formation [40, 41], worsened lipid profile, and elevated Framingham score [42,43,44]. However, limited research has explored the effects of corticosteroids on LVGLS. Aksakal et al. [45] suggested that high-dose intravenous steroid administration may decrease LVGLS.

To the best of our knowledge, there are few studies investigating the impact of SLE-related renal involvement on LVGLS measurements. Our study is also the first to explore this association in an Iranian population. Renal impairment has long been recognized as an underlying cause for traditional cardiovascular risk factors in SLE patients, such as hypertension and dyslipidemia [46, 47]. Moreover, several studies have identified renal dysfunction as an independent nontraditional cardiovascular risk factor [48, 49]. Left ventricular hypertrophy (LVH) is commonly observed in patients with end-stage renal disease, and previous research has indicated a correlation between LVH and reduced LVGLS [50, 51]. Similarly, Krishnasamy et al. [52] reported a significant reduction in LVGLS measurements among patients with renal dysfunction. Lou et al. [53] also found lower LVGLS values among SLE patients with nephrologic impairment. In line with these findings, our study demonstrated a marked decrease in LVGLS among SLE patients with renal involvement.

We also explored the relationship between SLE duration and LVGLS measurements, which, to our knowledge, has not been previously investigated in an Iranian population. We observed a positive correlation between disease duration and LVGLS parameters, consistent with Farag et al.’s research on a group of SLE patients [54]. However, Deng et al. did not find a similar association in their study of 43 SLE patients, which may be attributed to differences in the characteristics of the study population. The exclusion of participants with cardiac, renal, and thyroid dysfunction, and older male and female participants in Deng et al.’s [13] study, may have contributed to the discrepancy in results.

It is important to address some limitations regarding this study. Current study was conducted on a relatively small population; therefore, the results may not be attributable to the broader population of SLE patients. Additionally, due to technical difficulties, we were unable obtain CMR images from participants and compare them with the results of 3D-STE. Furthermore, the cross-sectional design of our study limits the ability to establish causality between SLE and the observed changes in cardiac function. Longitudinal studies are necessary to track changes in cardiac function over time and to evaluate the effects of disease progression and treatment on cardiac function in SLE patients.


Our study showed that SLE patients had significantly lower LVGLS measurements despite having normal LVEF values compared to healthy individuals. This finding highlights the importance of using more sensitive and accurate tools, such as 3D-STE, in assessing cardiac function in SLE patients. The ability of this technique to detect subtle changes in cardiac function may be especially valuable in predicting future cardiovascular events in this population. Therefore, it is suggested that 3D-STE be considered a valuable adjunct to routine cardiac evaluation in SLE patients.

Availability of data and materials

The data supporting current study is available from the corresponding author upon reasonable request.



Systemic lupus erythematosus


Cardiovascular disease


Myocardial infarction


Left ventricle


Left ventricular ejection fraction


Cardiac magnetic resonance imaging


Tissue Doppler imaging




Speckle tracking echocardiography




Apical 4-chamber


Left ventricular end-diastolic volume


Left ventricular end-systolic volume


Left ventricle global longitudinal strain


Apical 2-chamber




Intraclass correlation coefficient


Nonsteroid anti-inflammatory drugs


Left ventricular stroke volume


Left ventricular cardiac output


Left ventricular end-diastolic mass


Left ventricular end-systolic mass


Left ventricular mass


Left ventricular hypertrophy


  1. NCBI (2021) Systemic Lupus Erythematous.

  2. Murphy G, Isenberg D (2013) Effect of gender on clinical presentation in systemic lupus erythematosus. Rheumatology (Oxford) 52(12):2108–2115

    Article  PubMed  Google Scholar 

  3. Tsokos GC (2011) Systemic lupus erythematosus. N Engl J Med 365(22):2110–2121

    Article  CAS  PubMed  Google Scholar 

  4. Hanly JG, Li Q, Su L, Urowitz MB, Gordon C, Bae SC et al (2018) Cerebrovascular events in systemic lupus erythematosus: results from an international inception cohort study. Arthritis Care Res (Hoboken) 70(10):1478–1487

    Article  PubMed  Google Scholar 

  5. Futrell N, Millikan C (1989) Frequency, etiology, and prevention of stroke in patients with systemic lupus erythematosus. Stroke 20(5):583–591

    Article  CAS  PubMed  Google Scholar 

  6. Manzi S, Meilahn EN, Rairie JE, Conte CG, Medsger TA Jr, Jansen-McWilliams L et al (1997) Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: comparison with the Framingham Study. Am J Epidemiol 145(5):408–415

    Article  CAS  PubMed  Google Scholar 

  7. Aviña-Zubieta JA, To F, Vostretsova K, De Vera M, Sayre EC, Esdaile JM (2017) Risk of myocardial infarction and stroke in newly diagnosed systemic lupus erythematosus: a general population-based study. Arthritis Care Res (Hoboken) 69(6):849–856

    Article  PubMed  Google Scholar 

  8. Esdaile JM, Abrahamowicz M, Grodzicky T, Li Y, Panaritis C, du Berger R et al (2001) Traditional Framingham risk factors fail to fully account for accelerated atherosclerosis in systemic lupus erythematosus. Arthritis Rheum 44(10):2331–2337

    Article  CAS  PubMed  Google Scholar 

  9. Thomas G, Mancini J, Jourde-Chiche N, Sarlon G, Amoura Z, Harlé JR et al (2014) Mortality associated with systemic lupus erythematosus in France assessed by multiple-cause-of-death analysis. Arthritis Rheumatol 66(9):2503–2511

    Article  PubMed  Google Scholar 

  10. Liu Y, Kaplan MJ (2018) Cardiovascular disease in systemic lupus erythematosus: an update. Curr Opin Rheumatol 30(5):441–448

    Article  PubMed  Google Scholar 

  11. Moder KG, Miller TD, Tazelaar HD (1999) Cardiac involvement in systemic lupus erythematosus. Mayo Clin Proc 74(3):275–284

    Article  CAS  PubMed  Google Scholar 

  12. Di Minno MND, Forte F, Tufano A, Buonauro A, Rossi FW, De Paulis A et al (2020) Speckle tracking echocardiography in patients with systemic lupus erythematosus: a meta-analysis. Eur J Intern Med 73:16–22

    Article  PubMed  Google Scholar 

  13. Deng W, Xie M, Lv Q, Li Y, Fang L, Wang J (2020) Early left ventricular remodeling and subclinical cardiac dysfunction in systemic lupus erythematosus: a three-dimensional speckle tracking study. Int J Cardiovasc Imaging 36(7):1227–1235

    Article  PubMed  Google Scholar 

  14. Huang BT, Yao HM, Huang H (2014) Left ventricular remodeling and dysfunction in systemic lupus erythematosus: a three-dimensional speckle tracking study. Echocardiography 31(9):1085–1094

    Article  PubMed  Google Scholar 

  15. Crowson CS, Matteson EL, Myasoedova E, Michet CJ, Ernste FC, Warrington KJ et al (2011) The lifetime risk of adult-onset rheumatoid arthritis and other inflammatory autoimmune rheumatic diseases. Arthritis Rheum 63(3):633–639

    Article  PubMed  PubMed Central  Google Scholar 

  16. Puntmann VO, D’Cruz D, Smith Z, Pastor A, Choong P, Voigt T et al (2013) Native myocardial T1 mapping by cardiovascular magnetic resonance imaging in subclinical cardiomyopathy in patients with systemic lupus erythematosus. Circ Cardiovasc Imaging 6(2):295–301

    Article  PubMed  Google Scholar 

  17. Mavrogeni S, Bratis K, Markussis V, Spargias C, Papadopoulou E, Papamentzelopoulos S et al (2013) The diagnostic role of cardiac magnetic resonance imaging in detecting myocardial inflammation in systemic lupus erythematosus. Differ Viral Myocarditis Lupus 22(1):34–43

    CAS  Google Scholar 

  18. Yip GW, Shang Q, Tam LS, Zhang Q, Li EK, Fung JW et al (2009) Disease chronicity and activity predict subclinical left ventricular systolic dysfunction in patients with systemic lupus erythematosus. Heart 95(12):980–987

    Article  PubMed  Google Scholar 

  19. Rudski LG, Lai WW, Afilalo J, Hua L, Handschumacher MD, Chandrasekaran K et al (2010) Guidelines for the echocardiographic assessment of the right heart in adults: a report from the American Society of Echocardiography endorsed by the European Association of Echocardiography, a registered branch of the European Society of Cardiology, and the Canadian Society of Echocardiography. J Am Soc Echocardiogr 23(7): 685–713; quiz 86–88

  20. Kleijn SA, Aly MF, Terwee CB, van Rossum AC, Kamp O (2012) Reliability of left ventricular volumes and function measurements using three-dimensional speckle tracking echocardiography. Eur Heart J Cardiovasc Imaging 13(2):159–168

    Article  PubMed  Google Scholar 

  21. Mutluer FO, Bowen DJ, van Grootel RWJ, Roos-Hesselink JW, Van den Bosch AE (2021) Left ventricular strain values using 3D speckle-tracking echocardiography in healthy adults aged 20 to 72 years. Int J Cardiovasc Imaging 37(4):1189–1201

    Article  PubMed  Google Scholar 

  22. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF et al (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25(11):1271–1277

    Article  CAS  PubMed  Google Scholar 

  23. Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40(9):1725

    Article  CAS  PubMed  Google Scholar 

  24. Lang RM, Badano LP, Tsang W, Adams DH, Agricola E, Buck T et al (2012) EAE/ASE recommendations for image acquisition and display using three-dimensional echocardiography. Eur Heart J Cardiovasc Imaging 13(1):1–46

    Article  PubMed  Google Scholar 

  25. Chan J, Shiino K, Obonyo NG, Hanna J, Chamberlain R, Small A et al (2017) Left ventricular global strain analysis by two-dimensional speckle-tracking echocardiography: the learning curve. J Am Soc Echocardiogr 30(11):1081–1090

    Article  PubMed  Google Scholar 

  26. Koo TK, Li MY (2016) A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 15(2):155–163

    Article  PubMed  PubMed Central  Google Scholar 

  27. Javanbakht A, Poorzand H, Mirfeizi S (2015) Comparison of echocardiographic variables between systemic lupus erythematosus patients and a control group. Arch Cardiovasc Imaging. 3:e30009

    Google Scholar 

  28. Nikdoust F, Bolouri E, Tabatabaei SA, Goudarzvand M, Faezi ST (2018) Early diagnosis of cardiac involvement in systemic lupus erythematosus via global longitudinal strain (GLS) by speckle tracking echocardiography. J Cardiovasc Thorac Res 10(4):231–235

    Article  PubMed  PubMed Central  Google Scholar 

  29. Dedeoglu R, Şahin S, Koka A, Öztunç F, Adroviç A, Barut K et al (2016) Evaluation of cardiac functions in juvenile systemic lupus erythematosus with two-dimensional speckle tracking echocardiography. Clin Rheumatol 35(8):1967–1975

    Article  PubMed  Google Scholar 

  30. Kleijn SA, Pandian NG, Thomas JD, PerezdeIsla L, Kamp O, Zuber M et al (2015) Normal reference values of left ventricular strain using three-dimensional speckle tracking echocardiography: results from a multicentre study. Eur Heart J Cardiovasc Imaging 16(4):410–416

    Article  PubMed  Google Scholar 

  31. Smiseth OA, Torp H, Opdahl A, Haugaa KH, Urheim S (2016) Myocardial strain imaging: how useful is it in clinical decision making? Eur Heart J 37(15):1196–1207

    Article  PubMed  Google Scholar 

  32. Gegenava T, Gegenava M, Steup-Beekman GM, Huizinga TWJ, Bax JJ, Delgado V et al (2020) Left ventricular systolic function in patients with systemic lupus erythematosus and its association with cardiovascular events. J Am Soc Echocardiogr 33(9):1116–1122

    Article  PubMed  Google Scholar 

  33. Bulut M, Acar RD, Acar Ş, Fidan S, Yesin M, İzci S et al (2016) Evaluation of torsion and twist mechanics of the left ventricle in patients with systemic lupus erythematosus. Anatol J Cardiol 16(6):434–439

    PubMed  Google Scholar 

  34. Myhr KA, Pedersen FHG, Kristensen CB, Visby L, Hassager C, Mogelvang R (2018) Semi-automated estimation of left ventricular ejection fraction by two-dimensional and three-dimensional echocardiography is feasible, time-efficient, and reproducible. Echocardiography 35(11):1795–1805

    Article  PubMed  Google Scholar 

  35. Aurich M, André F, Keller M, Greiner S, Hess A, Buss SJ et al (2014) Assessment of left ventricular volumes with echocardiography and cardiac magnetic resonance imaging: real-life evaluation of standard versus new semiautomatic methods. J Am Soc Echocardiogr 27(10):1017–1024

    Article  PubMed  Google Scholar 

  36. Dorosz JL, Lezotte DC, Weitzenkamp DA, Allen LA, Salcedo EE (2012) Performance of 3-dimensional echocardiography in measuring left ventricular volumes and ejection fraction: a systematic review and meta-analysis. J Am Coll Cardiol 59(20):1799–1808

    Article  PubMed  PubMed Central  Google Scholar 

  37. Hascoët S, Brierre G, Caudron G, Cardin C, Bongard V, Acar P (2010) Assessment of left ventricular volumes and function by real time three-dimensional echocardiography in a pediatric population: a TomTec versus QLAB comparison. Echocardiography 27(10):1263–1273

    Article  PubMed  Google Scholar 

  38. Riehle TJ, Mahle WT, Parks WJ, Sallee D 3rd, Fyfe DA (2008) Real-time three-dimensional echocardiographic acquisition and quantification of left ventricular indices in children and young adults with congenital heart disease: comparison with magnetic resonance imaging. J Am Soc Echocardiogr 21(1):78–83

    Article  PubMed  Google Scholar 

  39. Lu X, Xie M, Tomberlin D, Klas B, Nadvoretskiy V, Ayres N et al (2008) How accurately, reproducibly, and efficiently can we measure left ventricular indices using M-mode, 2-dimensional, and 3-dimensional echocardiography in children? Am Heart J 155(5):946–953

    Article  PubMed  Google Scholar 

  40. Doria A, Shoenfeld Y, Wu R, Gambari PF, Puato M, Ghirardello A et al (2003) Risk factors for subclinical atherosclerosis in a prospective cohort of patients with systemic lupus erythematosus. Ann Rheum Dis 62(11):1071–1077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Tektonidou MG, Kravvariti E, Konstantonis G, Tentolouris N, Sfikakis PP, Protogerou A (2017) Subclinical atherosclerosis in systemic lupus erythematosus: comparable risk with diabetes mellitus and rheumatoid arthritis. Autoimmun Rev 16(3):308–312

    Article  PubMed  Google Scholar 

  42. Moya FB, Pineda Galindo LF, García de la Peña M (2016) Impact of chronic glucocorticoid treatment on cardiovascular risk profile in patients with systemic lupus erythematosus. J Clin Rheumatol 22(1):8–12

    Article  PubMed  Google Scholar 

  43. Durcan L, Winegar DA, Connelly MA, Otvos JD, Magder LS, Petri M (2016) Longitudinal evaluation of lipoprotein variables in systemic lupus erythematosus reveals adverse changes with disease activity and prednisone and more favorable profiles with hydroxychloroquine therapy. J Rheumatol 43(4):745–750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Petri M, Lakatta C, Magder L, Goldman D (1994) Effect of prednisone and hydroxychloroquine on coronary artery disease risk factors in systemic lupus erythematosus: a longitudinal data analysis. Am J Med 96(3):254–259

    Article  CAS  PubMed  Google Scholar 

  45. Aksakal E, Simsek Z, Aksu U, Birdal O, Ateş ES, Kalkan K et al (2019) Acute cardiac effects of high dose steroid treatment: a speckle tracking echocardiography study. J Clin Ultrasound 47(6):351–355

    Article  PubMed  Google Scholar 

  46. Leong KH, Koh ET, Feng PH, Boey ML (1994) Lipid profiles in patients with systemic lupus erythematosus. J Rheumatol 21(7):1264–1267

    CAS  PubMed  Google Scholar 

  47. Nezhad ST, Sepaskhah R (2008) Correlation of clinical and pathological findings in patients with lupus nephritis: a five-year experience in Iran. Saudi J Kidney Dis Transpl 19(1):32–40

    PubMed  Google Scholar 

  48. Gustafsson JT, Herlitz Lindberg M, Gunnarsson I, Pettersson S, Elvin K, Öhrvik J et al (2017) Excess atherosclerosis in systemic lupus erythematosus,-A matter of renal involvement: case control study of 281 SLE patients and 281 individually matched population controls. PLoS ONE 12(4):e0174572

    Article  PubMed  PubMed Central  Google Scholar 

  49. Manger K, Kusus M, Forster C, Ropers D, Daniel WG, Kalden JR et al (2003) Factors associated with coronary artery calcification in young female patients with SLE. Ann Rheum Dis 62(9):846–850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. London GM (2003) Cardiovascular disease in chronic renal failure: pathophysiologic aspects. Semin Dial 16(2):85–94

    Article  PubMed  Google Scholar 

  51. Dinh W, Nickl W, Smettan J, Kramer F, Krahn T, Scheffold T et al (2010) Reduced global longitudinal strain in association to increased left ventricular mass in patients with aortic valve stenosis and normal ejection fraction: a hybrid study combining echocardiography and magnetic resonance imaging. Cardiovasc Ultrasound 8(1):29

    Article  PubMed  PubMed Central  Google Scholar 

  52. Krishnasamy R, Isbel NM, Hawley CM, Pascoe EM, Leano R, Haluska BA et al (2014) The association between left ventricular global longitudinal strain, renal impairment and all-cause mortality. Nephrol Dial Transplant 29(6):1218–1225

    Article  CAS  PubMed  Google Scholar 

  53. Luo T, Wang Z, Chen Z, Yu E, Fang C (2021) Layer-specific strain and dyssynchrony index alteration in new-onset systemic lupus erythematosus patients without cardiac symptoms. Quant Imaging Med Surg 11(4):1271–1283

    Article  PubMed  PubMed Central  Google Scholar 

  54. Farag SI, Bastawisy RB, Hamouda MA, Hassib WA, Wahdan HA (2020) Value of speckle tracking echocardiography for early detection of left ventricular dysfunction in patients with systemic lupus erythematosus. J Cardiovasc Echogr 30(3):140–145

    Article  PubMed  PubMed Central  Google Scholar 

Download references


Not applicable.


This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Authors and Affiliations



NA and AM designed and supervised the study. NA, AM, and PS drafted the manuscript. NA, SA, SM, and MP contributed in echocardiography assessment, and analyzed images. PS gathered the information. NA, SA, PS, and MP analyzed the data. SM and KM provided critical revision of the study. All authors contributed in preparing the final draft of the article and read and approved the final manuscript.

Corresponding author

Correspondence to Amir Moradi.

Ethics declarations

Ethics approval and consent to participate

This study was conducted in accordance with the declaration of Helsinki, and the study protocol was approved by the Ethics Committee of Jundishapur University of Medical Sciences (IR.AJUMS.REC.1395.580). Informed written consent was obtained from all participating individuals after providing them with detailed information regarding the study process.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Akiash, N., Abbaspour, S., Mowla, K. et al. Three-dimensional speckle tracking echocardiography for evaluation of ventricular function in patients with systemic lupus erythematosus: relationship between duration of lupus erythematosus and left ventricular dysfunction by using global longitudinal strain. Egypt Heart J 76, 79 (2024).

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: