Left-atrioventricular interaction and left-atrial deformation in patients with type 2 diabetes mellitus with or without chronic aortic regurgitation: a 3.0-T cardiac magnetic resonance feature-tracking study

Introduction

The main causes of morbidity and mortality in individuals with type 2 diabetes mellitus (T2DM) are cardiovascular complications, which account for 52% of deaths (1,2). In older adults, T2DM can accompany chronic aortic regurgitation (AR) due to left-ventricular (LV) enlargement and aortic valve degeneration (3,4). Higher life expectancy, obesity prevalence, and accumulation of cardiovascular risk factors are the most likely explanations for the continued increase in the prevalence of T2DM and AR. T2DM and AR can lead to an increase in myocardial interstitial fibrosis, a decline in LV and left-atrial (LA) compliance and function, and eventually to development of heart failure (HF) (5-7). Patients with T2DM and AR may not exhibit any obvious clinical symptoms for an extended period, and these patients may be easily overlooked. Once the condition progresses, cardiac dysfunction cannot be reversed (3). For this reason, it is necessary to recognize latent cardiac dysfunction early and apply effective interventions in patients with T2DM and AR.

Previous studies on myocardial abnormalities in patients with T2DM or AR have primarily focused on LV function (8-10). However, recent studies have shown that LA phasic function has important predictive value for myocardial injury (11). LA function is independently associated with HF-related hospitalization and mortality, and the different LA phasic functions are closely related to LV function, specifically its diastolic function (12). Patients with T2DM or AR show an increase in LV end-diastolic volume (LVEDV) and pressure, further affecting the LA function (13,14). Patients with T2DM alone and those with T2DM with mitral regurgitation exhibit decreased LA strain (15). However, no studies on impaired LA strain and atrioventricular coupling in patients with T2DM and AR have been conducted thus far.

Cardiac magnetic resonance (CMR)-derived feature-tracking technology allows for the visualization and quantification of myocardial strain, and it can thus detect subclinical myocardial dysfunction, potentially offering a feasible approach for investigating the interdependence between the left ventricle and atrium (16). Several studies that used CMR tagging as a reference standard have confirmed the good reproducibility of this technique (17,18). This study aimed to use CMR feature-tracking technology to assess the additive effects of T2DM with AR on the left heart and investigate the LA interaction in patients with T2DM and AR. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-884/rc).

Methods

Study population

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and was approved by the Biomedical Research Ethics Committee of the West China Hospital of Sichuan University (No. 2019-756). The requirement for informed consent from patients was waived due to the retrospective nature of this study.

The inclusion criteria were patients who had been clinically diagnosed with T2DM (based on the current American Diabetes Association guidelines) (19) and had undergone CMR scans in our hospital between January 2015 and October 2022. Control participants were required to have no previous history of cardiac disease or symptoms, no T2DM history or impaired fasting glucose, and normal CMR findings. Meanwhile, the exclusion criteria were as follows: (I) presence of ischemic heart disease, rheumatic heart disease, congenital heart disease, primary cardiomyopathy, acute AR, combinations of other significant valvular disease, aortic disease, and previous aortic valve surgery; (II) incomplete clinical data; and (III) CMR contraindications, poor image quality, and incomplete scans. The final study population included 203 patients with T2DM without AR (74 females, 36.5%; mean age 57±11.5 years), 83 patients with T2DM with AR (30 females, 36.1%; mean age 65.1±11.7 years), and 105 controls (37 females, 35.2%; mean age 51.6±10.6 years). Echocardiographic findings were used to classify the patients with T2DM and AR into three groups: mild AR (n=39, 47%), moderate AR (n=25, 30.1%), and severe AR (n=19, 22.9%) (Figure 1) (20).

Figure 1 Flowchart of participant inclusion. AR, aortic regurgitation; CMR, cardiac magnetic resonance; T2DM, type 2 diabetes mellitus.

Clinical data were collected from the digital medical record system, including gender, age, height, weight, blood pressure, resting heart rate, fasting plasma glucose (FPG), glycated hemoglobin (HbA1c), years with diabetes, total cholesterol, triglycerides, high-density lipoprotein, low-density lipoprotein, and antidiabetic drugs (biguanides, sulfonylureas, α-glucosidase inhibitors, glucagon-like peptide-1/dipeptidyl peptidase-4 inhibitors, and insulin). The body mass index (BMI) was calculated as the weight (kg) divided by the square of the height (m).

CMR protocol

We followed a standardized imaging protocol to perform all CMR imaging. Either of two 3.0-T whole-body scanners (MAGNETOM Skyra and MAGNETOM Trio Tim; Siemens Healthineers, Erlangen, Germany) was used to perform imaging. We used a standard electrocardiogram (ECG)-triggering device to obtain high-quality CMR images. A balanced steady-state free-precession sequence was used to capture a series of short-axis views (covering the entire LV from the mitral valve to the apex) and a two-or four-chamber long-axis view of the left heart. The imaging parameters were set as follows: temporal resolution =39.34/40.35 ms, echo time =1.22/1.20 ms, slice thickness =8.0 mm, field of view =234×280/250×300 mm², matrix size =208×139/192×162 pixels, and flip angle =39°/50°.

CMR image post-processing

LA and LV volumetric function analysis

Post-processing software (cvi42, Circle Cardiovascular Imaging, Calgary, AB, Canada) was used to perform volumetric function analysis of the LA and left ventricle. The biplanar LAX module of the software was used to automatically calculate the LA volume (LAV) of the three phases: the LV end systole (LAV_max), LV diastole immediately before LA contraction (LAV_pre-a), and late LV end diastole after LA contraction (LAV_min). LAV was then normalized to body surface area (LAVI_max, LAVI_pre-a, and LAVI_min). LA function indices, including the total LA emptying fraction (total LAEF), passive LAEF, and active LAEF, were then calculated (Figure S1). cvi42 software included the short-3D module that could automatically compute various LV parameters, including LVEDV, LV end-systolic volume (LVESV), LV stroke volume, LV ejection fraction (LVEF), and LV mass index (LVMI).

LA and LV myocardial strain analysis

The tissue-tracking module of cvi42 was used to track each myocardial voxel on the horizontal four-chamber long-axis and vertical two-chamber long-axis cine slices. The software then automatically analyzed the global longitudinal strain of the LA and LV strain in three directions. The parameters of the LA strain included left atrial reservoir strain (ε_s), left atrial passive strain (ε_e), left atrial active strain (ε_a), peak positive strain rate (SR_s), peak early negative strain rate (SR_e), and peak late negative strain rate (SR_a). During the sketching of the epicardial and endocardial borders of the myocardium (Figure 2), the LA appendage, pulmonary vein, and LV papillary muscle were excluded.

Figure 2 CMR cine pseudocolor images and strain–time curves of LA strain in controls and patients with T2DM with and without AR. (A,B,G) A 66-year-old female patient with T2DM and AR (ε_s=9.3%; ε_a=5.4%). (C,D,H) A 57-year-old male patient with T2DM without AR (ε_s=29.1%; ε_a=15%). (E,F,I) A 52-year-old male control participant (ε_s=33%; ε_a=13%). AR, aortic regurgitation; CMR, cardiac magnetic resonance; ε_a, left atrial active strain; ε_s, left atrial reservoir strain; LA, left atrial; T2DM, type 2 diabetes mellitus.

Reproducibility

An experienced investigator with ≥3 years of CMR experience compared the data from 30 randomly selected cases analyzed by the same observer after 1 month to assess the intraobserver variability in the LA strain indices. The interobserver variability was evaluated through a comparison of the data from the same population with that of another independent, double-blinded, experienced observer with ≥3 years of CMR experience.

Statistical analyses

Continuous variables that followed a normal distribution are expressed as the mean ± standard deviation, whereas nonnormally distributed continuous variables are expressed as the median with the 25% and 75% quartiles. Differences between the control and T2DM groups were analyzed with the t-test or the Mann-Whitney test. Comparisons in groups with different AR degrees were made by performing one-way analysis of variance. Categorical variables are presented as frequencies (percentages) and were analyzed with the chi-squared test. Spearman rank correlation was used to analyze the correlation between LA strain and LV function parameters. The enter method, with LV variables with P<0.05 and no collinearity in the univariate analysis, was used to input data into the multivariate linear regression analyses, along with clinical characteristics, to identify the independent predictors of LA global longitudinal strain. Interobserver and intraobserver variabilities of LA strain were assessed via the intraclass correlation coefficient (ICC). A two-tailed test was performed in all analyses, and a P value <0.05 was considered to indicate statistical significance. SPSS version 24.0 (IBM Corp., Armonk, NY, USA) and GraphPad Prism version 7.0a (Dotmatics, Boston, MA, USA) were used to perform all analyses.

Results

Baseline clinical characteristics

The study included a total of 391 individuals, including 203 patients with T2DM without AR, 83 patients with T2DM combined with AR, and 105 controls. Age and FPG level were significantly different across the three groups (all P values <0.05). Compared to controls, patients with T2DM and AR had higher resting heart rates (79.7±16.1 vs. 74.2±12.4 bpm) and systolic blood pressure (SBP) (130.5±19.1 vs. 122.4±12.8 mmHg) (P<0.05). However, sex, body mass index, and blood lipid levels showed no significant difference. HbA1c and diabetes duration did not differ significantly between the patients with T2DM with and without AR (Table 1).

CMR indices in patients with T2DM and controls

As compared to controls, those with T2DM but not AR had lower LA measurements of total LAEF (53.5%±15.2% vs. 58.31%±11.2%), passive LAEF [27.8% (19.37%, 35.16%) vs. 33.39%±11.85%], ε_s (36.32%±13.4% vs. 40.17%±17.6%), and ε_e (19%±6.54% vs. 23.45%±12.02%) (all P values <0.05). For LV indices, only LVMI [70.8 (61–94.8) vs. 52±20.2 g/m²] was increased while LV global longitudinal peak strain (GLPS) (−11.51%±4.72% vs. −13.62%±4.24%) was decreased relative to those of the controls (all P values <0.05). Among patients with T2DM and AR, the LA parameters were worse than those in patients with T2DM without AR and controls (all P values <0.001) for all three-phasic LAVI, LAEF, LA longitudinal strain, and SRs (Figure 3, Table 2).

Figure 3 Comparison of LA function between controls, patients with T2DM without AR, and patients with T2DM with AR. (A) LA strain in three phases. (B) LAVI in three phases. (C) Total, passive, and active LAEF. All P values <0.05. AR, aortic regurgitation; ε_a, left atrial active strain; ε_e, left atrial passive strain; ε_s, left atrial reservoir strain; LA, left atrium; LAEF, left atrial emptying fraction; LAVI, left atrial volume index to body surface area; T2DM, type 2 diabetes mellitus.

Myocardial abnormalities of LA and LV in the patients with T2DM combined with mild or moderate AR

Regarding the LA indices, patients with T2DM combined with mild or moderate AR showed an increase in LAVI_max, LAVI_pre-a, and LAVI_min but a decrease in ε_s, ε_e, total LAEF, passive LAEF, and active LAEF compared with those patients with T2DM without AR group and controls (all P values <0.05). LVEDV and LVESV showed an increasing trend in the LV indices. Meanwhile, the global radial peak strain (GRPS), global circumferential peak strain (GCPS), and GLPS was lowest in patients with T2DM with moderate AR, followed by those with mild AR and those without AR (all P values <0.05). Moreover, the patients with T2DM and moderate AR, as compared to patients with T2DM and mild AR, T2DM without AR, and controls, showed a decrease in ε_a [7.3% (4.3%, 10.4%) vs. 16.8%±3.72%, 17%±5.19%, 16.72%±7.7%, respectively] (P=0.02). However, there were no significant differences in the SR_s, SR_e, or SR_a between the patients with T2DM and either mild or moderate AR (Table 2).

Myocardial abnormalities of LA and LV in the patients with T2DM and severe AR

In terms of LA indices, patients with T2DM and severe AR showed significantly increased LAVI_pre-a and LAVI_min and decreased total LAEF compared to controls, patients with T2DM without AR, and those with mild/moderate AR (all P values <0.05). Moreover, the patients with T2DM and severe AR, as compared with patients with T2DM combined with mild AR, also exhibited a considerable increase in LAVI_max (104.63±44.35 vs. 77.35±37.2 mL/m²) and a decrease in passive LAEF [12.18%±7.87% vs. 19.49% (13.63%, 27.54%)], active LVEF [14.23% (5%, 26.56%) vs. 27.08% (13.13%, 41.32%)], ε_s [8.9% (4.9%, 14.3%), 27.96%±7.73%], ε_e [5% (2.7%, 8.9%) vs. 11.16%±6.17%], and ε_a [2.5% (1.3%, 6.6%) vs. 16.8%±3.72%] (all P values <0.05). However, these parameters were not significantly different from those of the patients with T2DM combined with severe and moderate AR (Table 2).

Association between LV function and LA phasic function in patients with T2DM and AR

In the patients with T2DM and AR, correlation analysis showed that ε_s was negatively correlated with LVEDV (R=−0.385; P<0.001) and LVMI (R=−0.362; P=0.001) and that ε_a was negatively correlated with LVMI (R=−0.420; P=0.004). The multivariate analysis showed that ε_s was independently correlated with AR degree (β=−0.43; P<0.001), LVEDV (β=−0.304; P=0.035), and age (β=−0.199; P=0.028). ε_e was independently correlated with the age (β=−0.226; P=0.039) and the duration of diabetes (β=−0.256; P=0.009); meanwhile, ε_a was independently correlated with the regurgitation degree (β=−0.478; P<0.001) and LVMI (β=−0.364; P=0.004). Finally, there was a strong correlation between LVEF and the three-phasic LA longitudinal strains (Table 3, Table S1; Figure 4).

Figure 4 Correlations between the ε_s or the ε_a and LV function indices. ε_a, left atrial active strain; εe, left atrial passive strain; ε_s, left atrial reservoir strain; LV, left ventricle; LVEDV, left ventricular end-diastolic volume; LVEF, left ventricular ejection fraction; LVMI, left ventricular mass index; r, correlation coefficient.

Reproducibility of LA peak strain

On the basis of these results, the reproducibility of the LA strain was considered excellent for both intraobserver and interobserver assessments (all ICCs >0.7), and their correlation coefficients are shown in Table S2.

Discussion

This study confirmed that AR could worsen myocardial abnormalities in patients with T2DM. We further examined the atrioventricular interaction in patients with T2DM and AR, which revealed the following: (I) patients with T2DM with and without AR exhibited normal LV function but impaired LA reservoir and conduit function as compared with normal; (II) deteriorating AR could aggravate LA and LV dysfunction and impair active LA function; (III) the enlargement and dysfunction of LA were synchronous with LV dysfunction; (IV) the degree of AR was an independent determinant of ε_s and ε_e, LVEDV was an independent determinant of ε_s, and LVESV was an independent determinant of ε_a.

LA and LV dysfunction in patients with T2DM

Our study found that patients with T2DM with normal cardiac volume exhibited a notable decrease in total LAEF, passive LAEF, ε_s, and ε_e. The LA dysfunction in T2DM primarily occurred during the reservoir and conduit phase, whereas LV dysfunction mainly manifested as a reduction in GLPS. These findings suggest that LA function is a powerful parameter for evaluating LV diastolic dysfunction, a characteristic of diabetes-associated heart diseases (20). Previous investigations have demonstrated the negative effect of T2DM on LA (13,21,22). Because T2DM is a systemic-mediated disease, sustained hyperglycemia induces interstitial fibrosis, inflammation, and oxidative stress in LV and LA simultaneously (23-25). In addition, the conduction system disorders and imbalance in the autonomic nervous system induced by T2DM can contribute to paroxysmal atrial fibrillation, further impairing LA function (13). This may be the reason why the LA is sensitive to diabetes related injuries. Therefore, LA phasic function holds additional value for diagnosing latent myocardial injury in the diabetic population.

Assessment of LA and LV dysfunction in patients with T2DM and AR with different degrees of regurgitation

Our observations indicate that AR could potentially worsen the dysfunction of LA and LV. In patients with T2DM with mild AR, there was enlargement of the LA and LV, accompanied by a decline in the active LAEF and LVEF. ε_a was maintained in the mild AR stage but decreased remarkably in the moderate and severe AR stages. In addition, as the degree of regurgitation increased, LA phasic function and LV compliance gradually decreased. Notably, ε_s and ε_a were found to be independently influenced by the degree of regurgitation.

AR is defined as a condition in which the LV experiences volume overload due to blood backflow during diastole (26). Consequently, AR could result in increased LV preload, LV filling pressure, and subsequent increases in LA pressure and volume (27). In our study, when T2DM was accompanied by AR, the patients had worse left-heart volume and strain parameters. We speculated that the T2DM and AR had a synergistic effect on the mechanisms of cardiac injury, leading to heart damage and rapid failure of the compensatory mechanism in the left heart (28). Our study findings are consistent with those reported by Zhang et al., who found that LA myocardial impairment in patients with T2DM with mitral regurgitation progressed without compensation (15,29). Therefore, the occurrence and progression of AR should be considered in managing patients with T2DM. Once mild AR occurs in patients with T2DM, timely intervention is needed to avoid irreversible heart damage caused by AR progression (29). Patients who receive an early and timely diagnosis can plan surgery at the optimal time, thereby reducing the risk of long-term negative effects on cardiac function and malignant outcomes (30-33).

The left-atrioventricular interaction in patients with T2DM and AR

Several studies have highlighted the importance of LA workload and transport on LV function in patients with T2DM or AR (34,35). Steele et al. reported atrioventricular interaction in adolescents and young adults who were obese and had T2DM (22). Similarly, Jenner et al. found an association between LA phasic function and LV diastolic dysfunction in patients with AR (36). Our study findings indicated that LVEDV and LVMI were independent determinants of the ε_s observed in patients with T2DM and AR. Moreover, we found an independent association between LA strain and LV diastolic function. In the absence of valvular heart disease, the LA functions and LV filling pressures are tightly coupled during diastole since they are directly connected (36,37). The after-load LA depends on the LV end-diastolic pressure and LV wall stiffness, and the function of the LA reservoir period ensures that the LV can be filled quickly under short-term and low-load conditions (38). Atrioventricular dysfunction is a common problem associated with T2DM, and its pathological mechanism becomes even more complicated when AR is present. Previous reports have suggested that a reduction in LVEF to <50% is no longer a suitable surgical indication for patients with complicated AR, which was also the focus of our study (39,40). We further identified a positive correlation between LA strain and LVEF. Therefore, assessing atrioventricular interaction seems to be a stronger indication for intervention and may help in determining the optimal treatment for patients.

Limitations

Several limitations to our study should be acknowledged. First, we employed a retrospective study; therefore, a larger sample size of patients with T2DM and severe AR is needed in the future. Second, long-term follow-up data were unavailable, so further research is needed to investigate the predictive value LA strain parameters for predicting cardiovascular events. Finally, as our study was retrospective in nature, a prospective cohort study should be conducted to further examine the occurrence, development, and treatment-related clinical and cardiac function parameters of patients with T2DM and AR.

Conclusions

Patients with T2DM and worsening regurgitation degree may experience aggravated impairment of LA compliance and LV function due to AR. In our study, the degree of regurgitation was an independent determiner of LA reservoir strain and active strain. The possible association between LA phasic function and LV diastolic dysfunction can be clarified by assessing the interaction between the left atrium and ventricle. This can provide a more comprehensive diagnosis and informative monitoring of patients with T2DM combined with AR.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-884/rc

Funding: This study was financially supported by the National Natural Science Foundation of China (Nos. 81771887, 81771897, and 82371925) and the 1–3–5 Project for Disciplines of Excellence of West China Hospital, Sichuan University (No. ZYGD23019). The funding sources had no role of the study design; collection; analysis and interpretation of data; in the writing of the report; or in the decision to submit the article for publication.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-884/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. This study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and was approved by the Biomedical Research Ethics Committee of the West China Hospital of Sichuan University (No. 2019-756). The requirement for informed consent from patients was waived due to the retrospective nature of this study.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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