Observational Study Open Access
Copyright ©The Author(s) 2024. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Diabetes. Jun 15, 2024; 15(6): 1272-1279
Published online Jun 15, 2024. doi: 10.4239/wjd.v15.i6.1272
Subclinical impairment of left ventricular myocardium function in type 2 diabetes mellitus patients with or without hypertension
Zeng-Guang Chen, Department of Cardiology, The Affiliated Changzhou Second People’s Hospital with Nanjing Medical University, Changzhou 213000, Jiangsu Province, China
Guang-An Li, Jun Huang, Li Fan, Department of Echocardiography, The Affiliated Changzhou Second People’s Hospital with Nanjing Medical University, Changzhou 213000, Jiangsu Province, China
ORCID number: Jun Huang (0000-0002-4680-5344).
Co-first authors: Zeng-Guang Chen and Guang-An Li.
Author contributions: Chen ZG, Li GA, and Huang J designed the study and carried out the study, data collection, and analysis; Chen ZG and Li GA wrote the manuscript; Huang J revised the manuscript, and collected the type 2 diabetes mellitus patients and healthy subjects; Fan L performed the statistical analysis.
Supported by the Science and Technology Project of Changzhou Health Commission, No. ZD202342.
Institutional review board statement: This research was reviewed and approved by the Human Research and Ethics Committee of the Affiliated Changzhou Second People’s Hospital of Nanjing Medical University [Approval No. (2016)YLJSE009].
Informed consent statement: All study participants, or their legal guardian, provided informed written consent prior to study enrollment.
Conflict-of-interest statement: All the authors report no relevant conflicts of interest for this article.
Data sharing statement: All data collected during the study are available from the Corresponding author by request: Huang J, E-mail: 305669112@qq.com.
STROBE statement: The authors have read the STROBE Statement—checklist of items, and the manuscript was prepared and revised according to the STROBE Statement—checklist of items.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Jun Huang, MD, PhD, Chief Doctor, Postdoc, Teacher, Department of Echocardiography, The Affiliated Changzhou Second People’s Hospital with Nanjing Medical University, No. 68 Gelu Road, Changzhou 213000, Jiangsu Province, China. 305669112@qq.com
Received: December 26, 2023
Revised: March 6, 2024
Accepted: April 23, 2024
Published online: June 15, 2024
Processing time: 167 Days and 23.7 Hours

Abstract
BACKGROUND

Cardiovascular disease has been the leading cause of morbidity and mortality for type 2 diabetes mellitus (T2DM) patients over the last decade.

AIM

To determine whether layer-specific global longitudinal strain (GLS) combined with peak strain dispersion (PSD) can be used to assess left ventricle (LV) myocardium systolic dysfunction in T2DM patients or without hypertension (HP).

METHODS

We enrolled 97 T2DM patients, 70 T2DM + HP patients and 101 healthy subjects. Layer-specific GLS and PSD were calculated by EchoPAC software in apical three-, four- and two-chamber views. GLS of the epimyocardial, middle-layer and endomyocardial (GLSepi, GLSmid, and GLSendo) were measured and recorded. Receiver operating characteristic analysis was performed to detect LV myocardium systolic dysfunction in T2DM patients.

RESULTS

There were significant differences in GLSepi, GLSmid, GLSendo, and PSD between healthy subjects, T2DM patients and T2DM patients with HP (P < 0.001). Trend tests yielded the ranking of healthy subjects > T2DM patients > T2DM with HP patients in the absolute values of GLSepi, GLSmid and GLSendo (P < 0.001), while PSD was ranked healthy subjects < T2DM < T2DM with HP (P < 0.001). Layer-specific GLS and PSD had high diagnostic efficiency for detecting LV myocardium systolic dysfunction in T2DM patients, however, the area under the curve (AUC) for layer-specific GLS and PSD combined was significantly higher than the AUCs for the individual indices (P < 0.05).

CONCLUSION

Layer-specific GLS and PSD were associated with LV myocardium systolic dysfunction in T2DM patients, T2DM patients with HP. T2DM patients with HP have more severe LV myocardium systolic dysfunction than T2DM patients without HP and normal control patients. The combination of layer-specific GLS and PSD may provide additional prognostic information for T2DM patients with or without HP.

Key Words: Type 2 diabetes mellitus; Hypertension; Speckle tracking echocardiography; Global longitudinal strain; Peak strain dispersion

Core Tip: Left ventricle (LV) myocardium systolic dysfunction was found in type 2 diabetes mellitus (T2DM) patients, T2DM patients with hypertension (HP) by layer-specific global longitudinal strain (GLS) and peak strain dispersion (PSD). T2DM patients with HP have more serious LV myocardium systolic dysfunction than T2DM patients without HP and normal control patients. Combined layer-specific GLS and PSD may provide additional prognostic information for T2DM patients with or without HP.



INTRODUCTION

Type 2 diabetes mellitus (T2DM) is a common metabolic disease whose complications are mainly macro- and microcirculatory disorders[1]. Over the last decade, cardiovascular disease has been the leading cause of morbidity and mortality for T2DM patients[2]. Thus, early identification of myocardial systolic dysfunction in T2DM patients could facilitate earlier intervention and improve patient prognosis.

Recently, many techniques have been used to detect myocardial dysfunction in T2DM patients. For example, cardiac magnetic resonance imaging (MRI)[3] and echocardiography[4,5] have proven impaired cardiac function [including of the left ventricle (LV), left atrium (LA) and right ventricle] in these patients due to strain, strain rate and torsion[6-8]. Although cardiac MRI can evaluate cardiac function as the gold standard, the examination is expensive and time-consuming. Echocardiography is widely used in the clinic because it is simple, convenient, and flexible. Layer-specific global longitudinal strain (GLS) derived from two-dimensional speckle tracking echocardiography has been confirmed to accurately detect LV myocardium systolic dysfunction in valvular disease, cardiomyopathy, hypertension (HP) and so on[9-12]. However, GLS has the inherent shortcoming of ignoring the changes in myocardial movement and peak time parameters[13,14]. Peak strain dispersion (PSD) has been used to evaluate LV synchrony in systemic lupus erythematosus, nonobstructive hypertrophic cardiomyopathy, rheumatoid arthritis (RA) and so on[14-17], confirming that it can also be used to evaluate LV myocardium systolic dysfunction and is superior to GLS. However, there was no report about the use of a combination of layer-specific GLS and PSD for evaluating LV myocardium function and synchrony in T2DM with or without HP.

The aim of this research is to evaluate LV myocardium dysfunction and synchrony in T2DM with or without HP by layer-specific GLS and PSD and to determine whether layer-specific GLS and PSD, alone or in combination, could assess LV myocardium systolic dysfunction in T2DM patients with or without HP.

MATERIALS AND METHODS
Study population

Ninety-seven T2DM patients and 70 T2DM patients with HP were included. The diagnoses of T2DM patients were determined according to the American Diabetes Association[18], and the diagnoses of HP were determined according to the 2018 European Society of Cardiology (ESC)/European Society of Hypertension (ESH) Guidelines for the Management of Arterial HP[19]. Subjects with a history of congenital heart disease, coronary artery disease, valvular disease, cardiomyopathy, or arrhythmia, such as atrial fibrillation, thyroid disease, neoplastic disease, or kidney failure, were excluded from the study.

A total of 101 normal subjects of similar age and sex were enrolled as controls.

Anthropometric and biochemistry

The weight, height, heart rate (HR), systolic blood pressure (SBP), and diastolic blood pressure (DBP) were recorded when the patients were in hospital, and then body mass index (BMI), and body surface area (BSA) were calculated. Laboratory examinations of fasting plasma glucose (FPG), glycated haemoglobin (HbA1c), total cholesterol (TCH), triglyceride (TG), high-density lipoprotein (HDL-C), low-density lipoprotein (LDL-C), blood urea nitrogen (BUN), and serum creatinine (SCR) were recorded.

Conventional 2D Doppler echocardiography

Echocardiography was performed with a GE Vivid E9 (GE Vingmed Ultrasound, Horten, Norway), cardiac probe was M5s with a frequency of 3.5-5.0 MHz. Left atrial diameter, interventricular septum thickness, LV posterior wall thickness, LV diameter and mitral annular plane systolic excursion (LAd, IVSd, LVPWd, LVDd, and MAPSE) were measured by M-mode. Left ventricular ejection fraction (LVEF) was obtained via the biplane Simpson’s method. Pulsed wave Doppler of the mitral valve and tissue Doppler of the anterior and posterior annulus of the mitral valve were also evaluated, and then the E/A and E/e’ were calculated.

Two-dimensional speckle tracking analyses

Three consecutive cardiac cycles of apical three-, four- and two-chamber views were recorded for off-line analyses. Layer-specific GLS and PSD were measured by EchoPAC (version: 203).

Statistical analysis

The normality of all values was assessed by the Kolmogorov-Smirnov test or Shapiro-Wilk test. Differences between the T2DM patients, T2DM patients with HP and healthy subjects were compared with one-way analysis of variance (ANOVA) for normally distributed continuous variables, while the Kruskal-Wallis rank sum test was used for nonnormally distributed continuous variables. Receiver operating characteristic (ROC) curve was analyses by MedCalc software. Normally distributed data are presented as mean ± SD and otherwise as median (interquartile range). The categorical variables are presented as frequencies and percentages. A P value < 0.05 was considered statistically significant. All the data analyses were performed using SPSS 25.0 software (SPSS, Chicago, IL, United States).

Reproducibility and repeatability

Twenty randomly patients among all enrolled subjects were selected for interobserver and interobserver variabilities analysis in GLSepi, GLSmid, GLSendo, and PSD.

RESULTS
Patient characteristics and laboratory findings in healthy subjects, T2DM and T2DM with HP

Significant differences were detected in weight, BMI, BSA, SBP, DBP, HR, FPG, HbA1c, TG, HDL-C, BUN, and SCR between the healthy subjects, T2DM patients and T2DM + HP patients (P < 0.001). No significant differences were found in age, sex, height, TC, LDL-C or LPA between the healthy subjects, T2DM and T2DM + HP (P > 0.05) (Table 1).

Table 1 Clinical parameters of patients with healthy subjects, type 2 diabetes mellitus patients and type 2 diabetes mellitus patients with hypertension.
Clinical parameters
Healthy subjects (n = 101)
T2DM (n = 97)
T2DM + HP (n = 70)
P value
Age, yr48.06 ± 9.9049.04 ± 12.8052.00 ± 11.500.068
Male, n (%)48 (48)61 (63)39 (56)0.094
Hight, cm165.10 ± 7.50166.87 ± 9.25164.66 ± 7.530.199
Wight, kg64.14 ± 10.5872.50 ± 15.34172.23 ± 13.801< 0.001
BMI, kg/m223.44 ± 2.8425.85 ± 3.90126.51 ± 4.021< 0.001
BSA, m21.68 ± 0.171.79 ± 0.2411.78 ± 0.211< 0.001
SBP, mmHg123.26 ± 10.82127.65 ± 14.701137.07 ± 17.341,2< 0.001
DBP, mmHg77.85 ± 7.6579.25 ± 10.5986.64 ± 10.201,2< 0.001
HR, bpm69.85 ± 9.7675.22 ± 9.60179.10 ± 12.721,2<0.001
FPG, mmol/L4.95 (4.59, 5.25)10.53 (7.87, 14.07)18.91 (7.57, 10.97)1< 0.001
HbA1c, %5.45 ± 0.389.73 ± 2.2718.85 ± 2.491,2< 0.001
TC, mmol/L4.54 ± 0.854.37 ± 0.904.70 ± 1.140.102
TG, mmol/L1.21 (0.88,1.78)1.53 (0.97, 2.15)12.00 (1.38, 2.83)1,2< 0.001
HDL-C, mmol/L1.27 ± 0.301.09 ± 0.2911.04 ± 0.281< 0.001
LDL-C, mmol/L2.68 ± 0.702.65 ± 0.792.81 ± 0.990.556
LPA, g/L0.17 (0.11, 0.28)0.14 (0.06, 0.24)0.14 (0.08, 0.25)0.231
BUN, mmol/L4.75 (3.60, 5.70)5.50 (4.60, 6.30)15.50 (4.50, 7.40)10.001
SCR, μmol/L61.00 (55.00, 76.00)59.00 (49.30, 71.10)64.00 (54.00, 87.00)20.030
Medication, n (%)
    ACEI/ARB--32 (46)
    Calcium channel blocker--37 (53)
    β-blocker--4 (6)
    SGLT-2 inhibitor-18 (19)28 (40)
    Metformin-59 (61)38 (54)
    Insulin-55 (57)35 (50)
Conventional echocardiographic parameters, layer-specific GLS, PSD among healthy subjects, T2DM and T2DM with HP

Significant differences were found in LAd, LAV index, IVSd, LVPWd, LVEDV, MAPSE, E, A, E/A, and E/e’ between the healthy subjects, T2DM patients and T2DM + HP patients (P < 0.05). No significant differences were found in the LVd, LVESV, LVEF or e’ between the healthy subjects, T2DM patients and T2DM with HP patients (P > 0.05) (Tables 2 and 3).

Table 2 Echocardiographic parameters among healthy subjects, type 2 diabetes mellitus patients, and type 2 diabetes mellitus + hypertension patients.
Echocardiographic parameters
Healthy subjects (n = 101)
T2DM (n = 97)
T2DM + HP (n = 70)
P value
LAd, mm34.00 ± 2.9735.03 ± 3.04136.69 ± 3.911,2< 0.001
LAV index, mL/m229.17 ± 7.1932.20 ± 6.80130.92 ± 8.100.016
IVSd, mm9.21 ± 0.799.01 ± 0.989.71 ± 0.951,2< 0.001
LVPWd, mm9.01 ± 0.808.81 ± 0.939.53 ± 1.001,2< 0.001
LVDd, mm46.39 ± 2.9545.85 ± 3.4946.89 ± 3.400.124
LVEDV, mL76.61 ± 15.1769.57 ± 20.54176.77 ± 22.2620.018
LVESV, mL27.19 ± 6.6525.01 ± 8.1427.93 ± 8.7620.037
LVEF, %64.56 ± 3.7464.35 ± 2.8963.54 ± 2.710.080
MAPSE, mm14.47 ± 1.4414.23 ± 1.7513.42 ± 2.071,20.002
E, m/s0.83 ± 0.130.78 ± 0.1410.78 ± 0.1610.008
A, m/s0.68 ± 0.160.69 ± 0.150.82 ± 0.181,2< 0.001
E/A1.27 ± 0.291.16 ± 0.2911.00 ± 0.361,2< 0.001
e’, m/s0.11 ± 0.020.10 ± 0.020.10 ± 0.110.117
E/e’7.62 ± 1.548.30 ± 1.6319.00 ± 2.471,2< 0.001
Table 3 Layer-specific global longitudinal strain and peak strain dispersion among healthy subjects, type 2 diabetes mellitus patients, and type 2 diabetes mellitus + hypertension patients.

Healthy subjects (n = 101)
T2DM (n = 97)
T2DM + HP (n = 70)
P1 value
Ptrend value
GLSepi, %-18.66 ± 1.58-17.33 ± 1.931-16.74 ± 1.931,2< 0.001< 0.001
GLSmid, %-21.58 ± 1.843-19.87 ± 2.211,3-19.28 ± 2.161,3< 0.001< 0.001
GLSendo, %-25.03 ± 2.243,4-22.97 ± 2.561,3,4-22.48 ± 2.501,3,4< 0.001< 0.001
PSD, msec28.79 ± 7.2534.92 ± 11.19139.23 ± 11.471,2< 0.001< 0.001
P2 value< 0.001< 0.001< 0.001

There were significant differences in GLSepi, GLSmid, and GLSendo within the normal control, T2DM and T2DM with HP groups (P < 0.001), and trend tests showed a ranking of healthy subjects > T2DM patients > T2DM with HP patients in the absolute values of GLSepi, GLSmid and GLSendo (P < 0.001). There was a significant difference in PSD between the three groups, and the trend test results were as follows: Healthy subjects < T2DM < T2DM with HP (P < 0.001).

In each of the three groups, there were significant differences between GLSepi, GLSmid and GLSendo (P < 0.001), the trend tests showing an order of GLSepi < GLSmid < GLSendo (P < 0.001).

ROC analysis to confirm the diagnostic value for LV dysfunction of layer-specific LV GLS and PSD

The area under the curve (AUC) of combined layer-specific GLS and PSD was significantly larger than the individual variables (P < 0.05).

There were no significant differences between the AUCs of layer-specific LV GLS and PSD (P > 0.05) (Table 4 and Figure 1).

Figure 1
Figure 1 Receiver operating characteristic analysis for detecting the accuracy of left ventricle myocardium systolic dysfunction in type 2 diabetes mellitus patients. ROC: Receiver operating characteristic; AUC: Area under the curve; PSD: Peak strain dispersion.
Table 4 Intraclass correlation coefficients for intra- and interobserver variability for layer-specific global longitudinal strain and peak strain dispersion.
Variable
Interobserver variability
Intraobserver variability
ICC
95%CI
ICC
95%CI
GLSendo0.9590.896-0.9840.9640.909-0.986
GLSmid0.9650.911-0.9860.9730.933-0.989
GLSepi0.9590.898-0.9840.9750.936-0.990
PSD0.9550.887-0.9820.9760.939-0.990
Intraobserver and interobserver variability

The intraclass correlation coefficient values of Layer-specific GLS and PSD were larger than 0.95 (Table 4).

DISCUSSION

The study found that LV myocardium systolic dysfunction was impaired and that systolic asynchrony was increased in T2DM patients with or without HP and was more severe in T2DM patients with HP.

Systolic dysfunction is impaired in T2DM patients. Ng et al[8] used the GLS, GCS and GRS to evaluate systolic dysfunction in T2DM patients and concluded that LV longitudinal systolic dysfunction was impaired but that circumferential and radial functions were preserved in patients with uncomplicated T2DM. Liu et al[20] also concluded that in T2DM patients with no history of cardiovascular disease, impaired GLS was associated with cardiovascular events and provided incremental prognostic value. Ernande et al[5] reported that GLS alteration was associated with left ventricular remodelling in asymptomatic patients with T2DM. However, multilayer LV myocardial systolic dysfunction in T2DM patients, T2DM patients with HP has not been well documented. In this study, we found that the absolute value of GLSepi was significantly lower than that of both GLSmid and GLSendo in all three groups, in line with a previous study[12]. We also found that the absolute values of GLSepi, GLSmid, and GLSendo in healthy subjects were greater than those in T2DM patients and greater than those in T2DM + HP patients. Layer-specific GLS has improved our understanding of regional LV myocardial functional changes in patients with subclinical diabetic heart disease. We found that myocardial systolic dysfunction was impaired in T2DM patients and more severe in T2DM + HP patients. We also found that the damage in the LV myocardium included damage to the subendomyocardium, middle-layer myocardium and subepimyocardium. This local impairment of LV myocardium systolic dysfunction seems to be related to the glucose toxicity caused by long-term hyperglycaemia in patients with T2DM[21]. Hyperglycaemia and its accompanying glycotoxicity can induce protein glycosylation reactions, activate AGE/RAGE signalling, and promote the deposition of AGEs, resulting in an increase in connective tissue cross-linking and myocardial stiffness and impairment of myocardial function. In T2DM patients with HP, more impairment of local myocardial systolic dysfunction seems to be related to the significant increase in afterload caused by HP, which leads to a reduction in the number of myocardial microvessels and a change in myocardial cell structure[22].

Compared with GLS, PSD is more accurate in evaluating early lesions of LV function[14]. Previous studies also found that PSD was increased in patients with normal GLS and preserved LVEF[23]. PSD is used to evaluate early systolic dysfunction of the LV by combining the coordination and synchronization of cardiac mechanical movement[14]. PSD can be used as a new reliable index to evaluate LV systolic synchrony in many diseases. Ji et al[17] used PSD to evaluate LV systolic synchrony in patients with RA and found that LV systolic synchrony in patients with RA gradually decreases as the disease course progresses. PSD has also been used in hypertrophic cardiomyopathy (HCM)[16], systemic lupus erythematosus[24], and T2DM patients[14].

Due to insulin resistance, microvascular circulation disorders, increased afterload, and other reasons, with the occurrence and progression of the disease, the impairment of myocardial systolic dysfunction and the asynchrony of myocardial systole in T2DM and T2DM + HP patients will be promoted by changes in ventricular size and wall thickness. However, in the early subclinical stage, even if the conventional echocardiographic parameters remain normal, they can still be sensitively recognized by PSD. This result was also confirmed by our trend analysis of the three groups. ROC analysis showed that PSD had good sensitivity and specificity.

In T2DM patients with HP, LV hypertrophy may also lead to myocardial fibrosis, the sequence of the longitudinal and circumferential myocardium may change under these conditions, and the combined results indicated that the layer-specific GLS was lower in T2DM patients with HP. Layer-specific GLS analysis revealed no difference in GLSmid or GLSendo between the T2DM and T2DM with HP groups, except for GLSepi; however, the trend analysis revealed a decreasing trend. However, the PSD between the three groups decreased in the order of healthy subjects < T2DM patients < T2DM patients with HP, and the difference was also significant. This means that PSD and GLSepi are more sensitive in distinguishing subclinical LV myocardium systolic dysfunction in T2DM patients, T2DM patients with HP.

ROC analysis showed that GLSepi, GLSmid, GLSendo, PSD, and the combination of these indices had high AUCs for evaluating LV myocardium systolic dysfunction in T2DM patients, T2DM patients with HP, and the combined values also had the best predictive value for detecting LV myocardium systolic dysfunction in T2DM patients.

Limitations: First, the sample of the study was relatively small. A larger sample size could improve the robustness and generalizability of the findings. Second, the study was conducted at a single centre, which may limit the generalizability of the findings to broader populations. Multicentre studies involving diverse demographic and geographic populations could enhance the external validity of the results. Third, long-term follow-up data on clinical outcomes such as cardiovascular events and mortality were lacking.

CONCLUSION

Layer-specific GLS and PSD can find LV myocardium systolic dysfunction in T2DM patients, T2DM patients with HP. T2DM patients with HP have more severe LV myocardium systolic dysfunction than T2DM patients without HP and healthy subjects. The combination of layer-specific GLS and PSD may provide additional prognostic information for T2DM patients with or without HP.

Footnotes

Provenance and peer review: Unsolicited article; Externally peer reviewed.

Peer-review model: Single blind

Specialty type: Endocrinology and metabolism

Country/Territory of origin: China

Peer-review report’s classification

Scientific Quality: Grade C, Grade C, Grade C

Novelty: Grade B, Grade B, Grade B

Creativity or Innovation: Grade B, Grade B, Grade B

Scientific Significance: Grade B, Grade B, Grade B

P-Reviewer: Cheng TH, Taiwan; Ohashi N, Japan S-Editor: Chen YL L-Editor: A P-Editor: Xu ZH

References
1.  Su Y, Liu W, Wang D, Tian J. Evaluation of abdominal aortic elasticity by strain rate imaging in patients with type 2 diabetes mellitus. J Clin Ultrasound. 2014;42:475-480.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 4]  [Cited by in F6Publishing: 3]  [Article Influence: 0.3]  [Reference Citation Analysis (0)]
2.  Cao Y, Zeng W, Cui Y, Kong X, Wang M, Yu J, Zhang S, Song J, Yan X, Greiser A, Shi H. Increased myocardial extracellular volume assessed by cardiovascular magnetic resonance T1 mapping and its determinants in type 2 diabetes mellitus patients with normal myocardial systolic strain. Cardiovasc Diabetol. 2018;17:7.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 27]  [Cited by in F6Publishing: 28]  [Article Influence: 4.7]  [Reference Citation Analysis (0)]
3.  Wang J, Li Y, Guo YK, Huang S, Shi R, Yan WF, Qian WL, He GX, Yang ZG. The adverse impact of coronary artery disease on left ventricle systolic and diastolic function in patients with type 2 diabetes mellitus: a 3.0T CMR study. Cardiovasc Diabetol. 2022;21:30.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2]  [Cited by in F6Publishing: 2]  [Article Influence: 1.0]  [Reference Citation Analysis (0)]
4.  Yang QM, Fang JX, Chen XY, Lv H, Kang CS. The Systolic and Diastolic Cardiac Function of Patients With Type 2 Diabetes Mellitus: An Evaluation of Left Ventricular Strain and Torsion Using Conventional and Speckle Tracking Echocardiography. Front Physiol. 2021;12:726719.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 7]  [Reference Citation Analysis (0)]
5.  Ernande L, Bergerot C, Girerd N, Thibault H, Davidsen ES, Gautier Pignon-Blanc P, Amaz C, Croisille P, De Buyzere ML, Rietzschel ER, Gillebert TC, Moulin P, Altman M, Derumeaux G. Longitudinal myocardial strain alteration is associated with left ventricular remodeling in asymptomatic patients with type 2 diabetes mellitus. J Am Soc Echocardiogr. 2014;27:479-488.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 80]  [Cited by in F6Publishing: 84]  [Article Influence: 8.4]  [Reference Citation Analysis (0)]
6.  Huang J, Li L, Fan L, Chen DL. Evaluation of right ventricular systolic and diastolic dysfunctions in patients with type 2 diabetes mellitus with poor glycemic control by layer specific global longitudinal strain and strain rate. Diabetol Metab Syndr. 2022;14:49.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Cited by in F6Publishing: 1]  [Article Influence: 0.5]  [Reference Citation Analysis (0)]
7.  Doggrell SA. Oral fingolimod for relapsing-remitting multiple sclerosis Evaluation of: Kappos L, Radue E-M, O'Connor P, et al. A placebo-controlled trial of oral fingolimod in relapsing multiple sclerosis. N Engl J Med 2010;362:387-401; and Cohen JA, Barkhof F, Comi G, et al. Oral fingolimod or intramuscular interferon for relapsing multiple sclerosis. N Engl J Med 2010;362:402-15. Expert Opin Pharmacother. 2010;11:1777-1781.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 12]  [Cited by in F6Publishing: 21]  [Article Influence: 1.5]  [Reference Citation Analysis (0)]
8.  Ng AC, Delgado V, Bertini M, van der Meer RW, Rijzewijk LJ, Shanks M, Nucifora G, Smit JW, Diamant M, Romijn JA, de Roos A, Leung DY, Lamb HJ, Bax JJ. Findings from left ventricular strain and strain rate imaging in asymptomatic patients with type 2 diabetes mellitus. Am J Cardiol. 2009;104:1398-1401.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 227]  [Cited by in F6Publishing: 234]  [Article Influence: 15.6]  [Reference Citation Analysis (0)]
9.  Grund FF, Kristensen CB, Bahrami HSZ, Mogelvang R, Hassager C. Layer-specific longitudinal strain detects transmural dysfunction in chronic severe aortic regurgitation before and after aortic valve surgery. Int J Cardiovasc Imaging. 2021;.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2]  [Reference Citation Analysis (0)]
10.  Tsugu T, Nagatomo Y, Dulgheru R, Lancellotti P. Layer-specific longitudinal strain predicts left ventricular maximum wall thickness in patients with hypertrophic cardiomyopathy. Echocardiography. 2021;38:1149-1156.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
11.  Tsai WC, Lee WH, Liu YW. P1270Effects of blood pressure variability on layer-specific longitudinal strain in hypertension. Eur Heart J Cardiovasc Imaging. 2016;17:ii270-ii276.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
12.  Huang J, Yan ZN, Rui YF, Fan L, Shen D, Chen DL. Left Ventricular Systolic Function Changes in Primary Hypertension Patients Detected by the Strain of Different Myocardium Layers. Medicine (Baltimore). 2016;95:e2440.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 16]  [Cited by in F6Publishing: 16]  [Article Influence: 2.0]  [Reference Citation Analysis (0)]
13.  Shi F, Feng S, Zhu J, Wu Y, Chen J. Left Ventricular Strain and Dyssynchrony in Young and Middle-Aged Peritoneal Dialysis Patients and Healthy Controls: A Case-Matched Study. Cardiorenal Med. 2018;8:271-284.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 9]  [Cited by in F6Publishing: 11]  [Article Influence: 1.8]  [Reference Citation Analysis (0)]
14.  Li C, Yuan M, Li K, Bai W, Rao L. Value of peak strain dispersion in discovering left ventricular dysfunction in diabetes mellitus. Sci Rep. 2020;10:21437.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 4]  [Cited by in F6Publishing: 6]  [Article Influence: 1.5]  [Reference Citation Analysis (0)]
15.  Liu C, Yan ZN, Fan L, Huang J, Shen D, Song XT. Layer-specific speckle tracking analysis of left ventricular systolic function and synchrony in maintenance hemodialysis patients. BMC Cardiovasc Disord. 2020;20:126.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2]  [Cited by in F6Publishing: 2]  [Article Influence: 0.5]  [Reference Citation Analysis (0)]
16.  Su Y, Peng Q, Yin L, Li C. Evaluation of Exercise Tolerance in Non-obstructive Hypertrophic Cardiomyopathy With Myocardial Work and Peak Strain Dispersion by Speckle-Tracking Echocardiography. Front Cardiovasc Med. 2022;9:927671.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
17.  Ji X, Zhang X, Feng H. Evaluation of left ventricular systolic synchrony by peak strain dispersion in patients with rheumatoid arthritis. J Int Med Res. 2021;49:3000605211007737.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
18.  American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2013;36 Suppl 1:S67-S74.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1255]  [Cited by in F6Publishing: 1472]  [Article Influence: 133.8]  [Reference Citation Analysis (4)]
19.  2018 Practice Guidelines for the management of arterial hypertension of the European Society of Hypertension and the European Society of Cardiology: ESH/ESC Task Force for the Management of Arterial Hypertension: Erratum. J Hypertens. 2019;37:456.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 21]  [Cited by in F6Publishing: 28]  [Article Influence: 5.6]  [Reference Citation Analysis (0)]
20.  Liu JH, Chen Y, Yuen M, Zhen Z, Chan CW, Lam KS, Tse HF, Yiu KH. Incremental prognostic value of global longitudinal strain in patients with type 2 diabetes mellitus. Cardiovasc Diabetol. 2016;15:22.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 73]  [Cited by in F6Publishing: 75]  [Article Influence: 9.4]  [Reference Citation Analysis (0)]
21.  Bugger H, Abel ED. Molecular mechanisms of diabetic cardiomyopathy. Diabetologia. 2014;57:660-671.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 548]  [Cited by in F6Publishing: 641]  [Article Influence: 64.1]  [Reference Citation Analysis (0)]
22.  Braşoveanu AM, Mogoantă L, Mălăescu GD, Predescu OI, Cotoi BV, Ifrim Chen F. Hypertensive cardiomyopathy - histopathological and immunohistochemical aspects. Rom J Morphol Embryol. 2019;60:487-494.  [PubMed]  [DOI]  [Cited in This Article: ]
23.  Ermakov S, Gulhar R, Lim L, Bibby D, Fang Q, Nah G, Abraham TP, Schiller NB, Delling FN. Left ventricular mechanical dispersion predicts arrhythmic risk in mitral valve prolapse. Heart. 2019;105:1063-1069.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 39]  [Cited by in F6Publishing: 64]  [Article Influence: 12.8]  [Reference Citation Analysis (0)]
24.  Li C, Li K, Yuan M, Bai W, Rao L. Peak strain dispersion within the left ventricle detected by two-dimensional speckle tracking in patients with uncomplicated systemic lupus erythematosus. Int J Cardiovasc Imaging. 2021;37:2197-2205.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 4]  [Cited by in F6Publishing: 2]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]