Assessing left ventricular function in patients with hyperthyroidism across varied heart rates via press-strain loop analysis: a retrospective cross-sectional study

Introduction

Hyperthyroidism (HTH) represents a prevalent endocrine disorder, characterized by an incidence rate ranging between 0.2% to 1.4%, a frequency that escalates with advancing age (1,2). Elevated levels of thyroid hormones infiltrate the bloodstream, exerting systemic effects on various tissues and organs, thereby inducing pathological alterations in multiple organ functions. HTH is notably associated with an augmented susceptibility to cardiovascular disease (3,4). Mechanistically, HTH impacts cardiomyocytes, blood vessels, and the circulatory system, precipitating an elevation in heart rate, myocardial contractility, preload, and occurrences of rhythm abnormalities. In instances of prolonged hyperdynamic states, cardiocytes experience hypoxia, thereby precipitating myocardial systolic and diastolic impairment, and potentially culminating in heart failure, accompanied by a notable 20% escalation in patient mortality rates (1). Initial cardiovascular manifestations in thyroid HTH may not manifest overtly, and cardiac performance may deteriorate preceding observable structural alterations (5). The non-invasive technique of left ventricular press-strain loop (LVPSL) offers a novel avenue for evaluating the impact of afterload on myocardial systolic function, facilitating an early and quantitative assessment of left ventricular (LV) systolic function alterations (6,7). Although the LVPSL technique has been used to study LV systolic function in hyperthyroid patients, previous studies have not grouped these patients based on the presence or absence of tachycardia. In this study, we aimed to use non-invasive LVPSL to assess LV systolic function in HTH patients with different heart rates. The hypothesis proposed in this study was that non-invasive LVPSL can evaluate changes in LV myocardial work in HTH patients with different heart rates, providing an early and sensitive reflection of HTH-related LV systolic dysfunction, with more severe impairment in patients with tachycardia. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-951/rc).

Methods

Study participants

In this retrospective cross-sectional study, we recruited 78 individuals newly diagnosed with HTH between December 2022 and September 2023 using a random method at the Department of Endocrinology of Shanxi Bethune Hospital, Shanxi Academy of Medical Sciences, Tongji Shanxi Hospital, The Third Hospital of Shanxi Medical Hospital. These patients had not undergone prior treatment and met the established diagnostic criteria for HTH (8). Subsequently, the patients with HTH were categorized into two groups based on the presence or absence of tachycardia (defined as a sinus rhythm exceeding 100 beats per minute): the tachycardia group (HTH1 group, n=33), comprising 22 females and 11 males, aged between 14 to 59 years with a mean age of (33.78±13.11) years; and the non-tachycardia group (HTH2 group, n=45), consisting of 31 females and 14 males, aged between 15 and 67 years with a mean age of (32.91±12.66) years. Additionally, during the same period, a control group of 38 healthy individuals undergoing medical examinations was selected, matched for sex and age. This control group comprised 26 females and 12 males, aged between 15 to 64 years with a mean age of (33.03±12.75) years (Figure S1).

This study was conducted in accordance with the declaration of Helsinki (as revised in 2013). This study was approved by the Ethical Committee of Shanxi Bethune Hospital (Shanxi Academy of Medical Sciences, No. SBQLL-2022-019) and informed consent was taken from all the patients.

Exclusion criteria: (I) hyperthyroid cardiopathy; (II) concurrent hypertension, diabetes, coronary artery disease, valvular heart disease, congenital heart disease and other diseases that may have some impact on myocardial motion; (III) poor image quality.

Systolic blood pressure (SBP), diastolic blood pressure (DBP), and heart rate were measured and recorded, and the pulse pressure difference was calculated as SBP − DBP. Free thyroxine (FT4), serum free triiodothyronine (FT3), and serum thyroid-stimulating hormone (TSH) of the study participants were recorded.

Instruments and method

A GE Vivid E9 ultrasonograph equipped with an M5S probe operating at a frequency range of 2–4.5 MHz, coupled with an Echo PAC ultrasound workstation, was utilized for the cardiac evaluations. The examinee was positioned in the left lateral decubitus position and connected to an electrocardiogram for monitoring purposes. Echocardiographic assessments were conducted employing conventional 2D imaging techniques, encompassing measurements of interventricular septal thickness (IVSD), LV end-diastolic diameter (LVIDd), left ventricular end-systolic diameter (LVIDs), and left ventricular end-diastolic posterior wall thickness (LVPWD). The left ventricular mass index (LVMI) was derived using the Devereux formula, while the left ventricular ejection fraction (LVEF) was quantified employing the biplanar Simpson method. Furthermore, peak mitral diastolic flow velocities (early E and late A) and peak diastolic velocities of the lateral wall of the mitral annulus (early e’ or late a’) were assessed through pulsed and tissue Doppler ultrasonography, specifically in LV apical four-chamber views. LV in the apical four-chamber, three-chamber, and two-chamber views were captured and stored at a frame rate ranging from 60 to 80 frames per second. Subsequent myocardial work analysis was conducted utilizing Echo PAC software, which facilitated the extraction of global and segmental longitudinal strains alongside their corresponding tracking maps. This analysis involved inputting SBP values and adjusting valve opening and closing times to derive parameters including global longitudinal strain (GLS), global work index (GWI), global constructive work (GCW), global wasted work (GWW), and global work efficiency (GWE). The acquisition and interpretation of ultrasonic images were carried out by three physicians possessing over a decade of experience in clinical ultrasonography.

Statistical analysis

Statistical analyses were conducted utilizing SPSS version 27.0. Measurement data adhering to a normal distribution are presented as mean ± standard deviation; comparisons of these parameters were executed through one-way analysis of variance (ANOVA), followed by pairwise comparisons utilizing the LSD-t test. Conversely, measurement data deviating from a normal distribution are expressed as median (interquartile range). Between-group comparisons of such parameters were performed employing the Kruskal-Wallis H test, with subsequent pairwise comparisons adjusted using the Bonferroni method. Count data are represented as frequencies and percentages, and intergroup comparisons were undertaken using the chi-squared (χ²) test. Statistical significance was defined as P<0.05 (two-sided).

Results

Comparison of general data

The variances in gender, age, and DBP among the three groups did not achieve statistical significance (P>0.05, analyzed by ANOVA). However, the heart rate within the HTH1 group surpassed that of both the control and HTH2 groups, demonstrating a statistically significant difference (P<0.001, analyzed by ANOVA). The causes of hyperthyroidism among these patients included diffuse toxic goiter, Hashimoto’s thyroiditis, and hyperfunctioning thyroid adenoma, with diffuse toxic goiter being the most common. Conversely, upon comparison, the differences in heart rate between the control group and HTH2 group were not statistically significant (P=0.394, analyzed by post-hoc test). Compared to the control group, significant elevations were observed in SBP, pulse pressure differential, FT3, and FT4 levels within both the HTH1 and HTH2 groups, while TSH levels were decreased (P<0.05, analyzed by ANOVA). Additionally, SBP, pulse pressure differential, FT3, and FT4 levels were notably higher in the HTH1 group compared to the HTH2 group, with statistically significant differences (P<0.05, analyzed by ANOVA). However, the difference in TSH levels between the HTH1 and HTH2 groups did not reach statistical significance (P=0.984, analyzed by post-hoc test). Refer to Table 1 for detailed findings.

Comparison of conventional echocardiographic parameters

No statistically significant differences were observed among the three groups in terms of IVSD, LVIDd, LVIDs, LVPWD, LVMI, E/A, and E/e ratio (P>0.05, analyzed by ANOVA). However, LVEF within the HTH1 and HTH2 groups exhibited significant increases compared to the control group (P<0.05, analyzed by ANOVA). Furthermore, although the LVEF in the HTH1 group surpassed that of the HTH2 group, this difference did not attain statistical significance (P=0.416, analyzed by post-hoc test). For detailed data, please refer to Table 2.

Comparison of LV myocardial work parameters

GLS, GWI, and GWE within both the HTH1 and HTH2 groups exhibited reductions compared to those of the control group, whereas GWW was greater than that of the control group, with statistically significant differences noted (P<0.05, analyzed by ANOVA). Moreover, the GWI and GWE in the HTH1 group were lower than in the HTH2 group, while GWW was higher in the HTH1 group compared to the HTH2 group, all demonstrating statistically significant differences (P<0.05, analyzed by ANOVA). However, no statistically significant differences were observed in GLS comparisons between the HTH1 and HTH2 groups (P=0.145, analyzed by post-hoc test). Similarly, no statistically significant differences were detected in GCW comparisons among the three groups (P=0.548, analyzed by ANOVA) (Figure 1A-1C). Detailed findings are provided in Table 3.

Figure 1 Work parameters of left ventricle-press-strain loop in different groups. (A) HTH1 group: GLS =−17%, GWI =1,478 mmHg%, GCW =1,846 mmHg%, GWW =89 mmHg%, GWE =95%. (B) HTH2 group: GLS =−17%, GWI =1,756 mmHg%, GCW =1,857 mmHg%, GWW =70 mmHg%, GWE =96%. (C) Control group: GLS =−22%, GWI =1,839 mmHg%, GCW =2,023 mmHg%, GWW =52 mmHg%, GWE =97%. Top left: pressure-strain curve; top right: left ventricular 17-segment myocardial work index bull’s-eye plot; bottom left: bar chart of left ventricular GCW and GWW. HTH1, tachycardia; GLS, global longitudinal strain; GWI, global work index; GCW, global constructive work; GWW, global wasted work; GWE, global work efficiency; HTH2, non-tachycardia.

Discussion

Thyroid hormones, notably FT3, exert significant effects on the cardiovascular system by modulating cardiomyocytes, vascular function, and overall circulatory dynamics. Consequently, individuals with HTH are predisposed to heightened cardiovascular disease risk (4,9,10). This heightened risk stems from HTH-induced elevations in heart rate and cardiac contractility, which may precipitate arrhythmias and hypertension. Additionally, HTH-associated endothelial dysfunction can promote arterial plaque deposition, further exacerbating cardiovascular vulnerability (2). Despite these implications, early cardiovascular manifestations in HTH patients may not be readily apparent, and cardiac dysfunction may precede observable structural alterations. Studies conducted both internationally and within China have demonstrated that myocardial strain parameters exhibit diminishment in individuals with HTH, even when echocardiographic LVEF remains within the normal range (11,12). This phenomenon facilitates the early identification of LV systolic dysfunction in patients with HTH. However, it is worth noting that speckle-tracking imaging does not account for the influence of afterload on myocardial function (11-13). LVPSL method incorporates the impact of afterload on myocardial function and enables non-invasive, quantitative assessment of myocardial work. This technique has been utilized in the early assessment of compromised LV systolic function across a spectrum of cardiovascular conditions, including hypertension, diabetes mellitus, coronary artery disease, and heart failure (14-19). The primary objective of this study was to employ LVPSL method to evaluate alterations in LV myocardial function among individuals with HTH across varying heart rates. Furthermore, we aimed to identify instances of subclinical LV dysfunction in patients with HTH during the early stages of their condition.

The findings of this study revealed that SBP and pulse pressure differential were elevated in both the HTH1 and HTH2 groups compared to the control group. HTH may augment cardiac contractility and output via its influence on sympathetic, renin-angiotensin, and sodium retention pathways, thereby contributing to increased SBP. Furthermore, thyroid hormones promote nitric oxide production, leading to peripheral vasodilation, diminished vascular resistance, and the maintenance of normal or slightly reduced DBP (10,20,21). Consequently, an elevated SBP, coupled with normalized or slightly decreased DBP, results in an increased pulse pressure differential.

The findings of this study revealed that, upon comparison, there were no statistically significant differences observed in IVSD, LVIDd, LVIDs, LVPWD, LVMI, E/A, E/e ratio among the three groups. These results suggest that conventional echocardiography may not be sufficiently sensitive to detect early-stage myocardial impairment in cases of newly diagnosed HTH. However, it was noted that the LVEF in both the HTH1 and HTH2 groups exceeded that of the control group, with statistically significant differences observed. This observation may be attributed to heightened myocyte excitability, increased myocardial contractility, and elevated intracardiac hemodynamic status induced by excess thyroid hormone levels (22,23).

The study findings indicated that the GLS values observed in both the HTH1 and HTH2 groups were lower compared to those of the control group, with no statistically significant differences noted when comparing the HTH1 and HTH2 groups. These results suggest an early-stage impairment of LV systolic function in patients with HTH. Furthermore, these findings are consistent with prior research by Duzen et al. (12). Studies conducted in China and internationally have corroborated the underlying pathological mechanisms of myocardial injury in HTH, characterized by cardiomyocyte hypertrophy and interstitial collagen fiber proliferation (24,25). These alterations result in a relatively diminished vascular density, culminating in myocardial ischemia and compromised systolic function (24,25). However, it is noteworthy that GLS failed to discern differences in LV myocardial function between patients with HTH with and without tachycardia.

In this study, the GWW exhibited higher values in both the HTH1 and HTH2 groups compared to the control group, with the GWW in the HTH1 group exceeding that of the HTH2 group. GWW serves as a marker of LV contraction asynchrony, a phenomenon detrimental to efficient cardiac ejection (26). The findings indicate a discernible impairment of LV systolic synchronization among patients with HTH, with a more pronounced effect observed in individuals with tachycardia. Specifically, LV systolic velocity was observed to be lower in the tachycardia subgroup compared to the control group. International research findings have indicated that individuals with HTH are at heightened risk of experiencing impaired conduction of ventricular late potential responses and delayed depolarization in one or more myocardial regions, alongside contraction asynchrony. These observations align with the outcomes observed in the current investigation (27). The etiology could potentially stem from lymphocytic infiltration within the myocardium during HTH, resulting in necrosis and fibrosis of myocardial cells, thereby influencing the function of the cardiac conduction system (28). Both the GWI and GWE were found to be diminished in the HTH1 and HTH2 groups compared to the control group, with a notably more pronounced reduction observed in the HTH1 group relative to the HTH2 group. These findings suggest the presence of subclinical myocardial damage among patients with HTH, with a more severe manifestation in individuals presenting with concomitant tachycardia. The underlying factors are associated with heightened sympathetic and adrenal activity in HTH, leading to an elevated heart rate and subsequent augmentation of myocardial oxygen consumption, particularly pronounced in the presence of tachycardia. Consequently, this sequence of events may precipitate myocyte hypoxia, myocardial strain, cardiac hypertrophy, or coronary artery spasms, ultimately culminating in impaired LV systolic function (5,19,28). In patients in the HTH1 group, there was a notable reduction in the duration of the cardiac cycle, particularly during diastole. This abbreviated diastolic phase results in a diminished myocardial blood supply, thereby exacerbating myocardial damage. Consequently, myocardial injury tends to be more pronounced in patients with HTH presenting with tachycardia (29). Additionally, the elevated SBP observed in patients with HTH may serve as a compensatory mechanism for the diminished GCW, thus rendering the differences in GCW among the three groups statistically insignificant.

This study is subject to several limitations: (I) a limited number of participants were included in the study cohort; (II) long-term monitoring of LV systolic function in patients with HTH was not conducted; (III) the LVPSL technique relies on speckle tracking imaging, necessitating the acquisition of clearer two-dimensional images, which may pose challenges in certain cases.

Conclusions

Based on the preceding discussion, non-invasive LVPSL analysis offers a quantitative assessment of LV myocardial function in patients with HTH across varying heart rates. This method demonstrates heightened sensitivity in detecting early-stage impairment of LV systolic function attributable to HTH. Moreover, the severity of LV systolic dysfunction is notably exacerbated in individuals with concurrent tachycardia. These findings suggest that LVPSL may facilitate accurate diagnosis and timely treatment initiation for patients with cardiovascular complications by guiding treatment decisions and incorporating longitudinal assessments of cardiac function.

Acknowledgments

We would like to acknowledge the hard and dedicated work of all the staff who implemented the intervention and evaluation components of the study.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-951/rc

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-951/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). This study was approved by the Ethical Committee of Shanxi Bethune Hospital (Shanxi Academy of Medical Sciences, No. SBQLL-2022-019) and informed consent was taken from all the patients.

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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