Skip to main content
Download PDF

Assessment of left ventricular myocardial systolic dysfunction in premature ovarian insufficiency patients using echocardiographic layer-specific myocardial strain imaging

Echo Research & Practice volume 11, Article number: 20 (2024) Cite this article

Abstract

Background

Due to the lack of oestrogen, premature ovarian insufficiency (POI) is an independent risk factor for ischaemic heart disease and overall cardiovascular disease. This study aimed to apply layer-specific myocardial strain for early quantitative evaluation of subclinical left ventricular myocardial systolic function changes in patients with POI.

Methods

Forty-eight newly diagnosed, untreated patients with POI (POI group) and fifty healthy female subjects matched for age, height and weight (control group) were enrolled. Standard transthoracic echocardiography was used to measure conventional parameters and layer-specific strain parameters.The layer-specific strain parameters included subendomyocardial global longitudinal strain (GLSendo), mid-layer myocardial global longitudinal strain (GLSmid), subepimyocardial global longitudinal strain (GLSepi), subendomyocardial global circumferential strain (GCSendo), mid-layer myocardial global circumferential strain (GCSmid), and subepimyocardial global circumferential strain (GCSepi).

Results

There were no significant differences in age, body mass index (BMI), blood pressure, or left ventricular ejection fraction (LVEF) between the two groups. The end-diastolic interventricular septal thickness (IVST) was greater in the POI group (8.29 ± 1.32 vs. 7.66 ± 0.82, P = 0.008), and the POI group had lower E, E/A, and lateral e′ (all P < 0.05). As for systolic functions,the POI group had lower GLSendo, GLSmid, GLSepi, GCSendo, GCSmid, and GCSepi (all P < 0.05).The intraobserver and interobserver coefficients of GLSendo, GLSmid, GLSepi, GCSendo, GCSmid, and GCSepi were greater than 0.900.

Conclusions

POI patients with normal LVEF may suffer from subclinical left ventricular myocardial systolic dysfunction. Echocardiography of layer-specific myocardial strain could more sensitively detect subclinical impairment of left ventricular systolic function in POI patients.

Graphical abstract

Introduction

Premature ovarian insufficiency (POI) refers to a clinical syndrome caused by the loss of ovarian activity in women before the age of 40 years and mainly manifests as menstrual abnormalities (oligomenorrhoea or amenorrhoea), increased gonadotropins such as follicle-stimulating hormone (FSH) > 25 IU/L, and decreased oestrogen [1].

The global incidence rate of POI is 3.7% [2]. POI can be caused by chromosomal abnormalities and genetic defects (sex chromosomes and autosomes), immune system diseases, infection, or environmental or iatrogenic factors, but over 50% of patients with POI still have unknown aetiologies [3].

POI can have adverse effects on multiple systems in women, including the cardiovascular system, genitourinary system, skeletal system and mental health, and harm to the cardiovascular system can reduce life expectancy and increase the risk of heart failure [1, 4]. POI can serve as an independent risk factor for ischaemic heart disease (IHD) and cardiovascular disease (CVD) [5],and the pathophysiological mechanism affecting the cardiovascular system is mainly a series of changes caused by a lack of oestrogen. Most patients with POI have no obvious precordial discomfort in the early stage, so they often ignore changes in the cardiovascular system. In 2016, the European Society of Human Reproduction and Embryology (ESHER) recommended that all women with POI be assessed for CVD risk and receive early hormone replacement therapy (HRT) to control their future CVD risk [1]. The North American Menopausal Association also recommended HRT treatment for patients with POI without contraindications [4]. Turner syndrome (TS) is a special type of POI characterized by sex chromosomal abnormalities, and CVD-related risk factors should be assessed annually [1].

Layer-specific myocardial strain measurements are based on two-dimensional speckle tracking echocardiography (2D-STE), which can quantify the myocardial strain parameters of each layer, provide more accurate myocardial deformation information, and provide more guidance for clinical precision treatment. This study intended to use layer-specific myocardial strain to quantitatively assess subclinical myocardial systolic impairment of the left ventricle in patients with POI.

Methods

Forty-eight patients who were newly diagnosed with POI from the Menopausal Gynecological Endocrinology Clinic of our hospital were included as the POI group.

All subjects with POI underwent sex hormone testing, and patients suspected of having TS underwent chromosome testing. Inclusion criteria: meeting the POI diagnostic criteria proposed by ESHER [1]: ① age < 40 years old; ② oligomenorrhoea or amenorrhoea for at least 4 months and elevated FSH > 25 IU/L on two occasions > 4 weeks apart. Exclusion criteria: ① age > 40 years old; ② prior HRT; ③ severe cardiovascular disease, including congenital cardiovascular disease, coronary heart disease, cardiomyopathy, severe arrhythmia, heart failure, pericardial disease; ④ hypertension, diabetes, blood system disease, autoimmune system disease, or history of radiotherapy or chemotherapy; and ⑤ poor image quality. Fifty healthy voluntary subjects matched for age, height and weight with the POI group were selected as the control group. These individuals had a normal menstruation history, sinus rhythm, no hypertension, no hyperlipidaemia, no diabetes, and no history of severe cardiovascular disease. This study was reviewed and approved by the hospital ethics committee, and all the subjects signed informed consent.

Blood pressure was measured by a cuff manometer for all subjects.Complete echocardiography was performed by using Vivid E9 echocardiographic diagnostic equipment (GE Healthcare) with an M5S probe (frequency: 1.4–4.6 MHz). Two-dimensional dynamic images of at least three cardiac cycles were collected from the parasternal left ventricle long-axis view, apical 4-chamber view, apical 3-chamber view, apical 2-chamber view, left ventricular mitral valve short-axis view, papillary muscle short-axis view, and apical short-axis view. Pulsed-wave Doppler (PW) was used to collect anterior blood flow spectrum of the mitral valve in the apical 4-chamber view, and tissue Doppler imaging (TDI) was subsequently used to obtain the velocity spectrum of the lateral and septal mitral annulus.

A dedicated EHCO PAC 202 workstation was used for echocardiographic image postprocessing and measurement of the end-diastolic diameter of the left ventricle (LVEDD), the end-diastolic thickness of the left ventricular posterior wall (LVPWT), and the end-diastolic interventricular septal thickness (IVST) in the parasternal left ventricular long-axis view. The following formulas were used to calculate relative wall thickness (RWT) = 2 × LVPWT/LVEDD, left ventricular mass (LVM) = 0.8 × 1.04 × [(LVEDD + IVST + LVPWT)3 − LVEDD3] + 0.6, body surface area (BSA) = 0.0061 × height (cm) + 0.0128 × weight (kg) − 0.1529, body mass index (BMI) = weight (kg)/height(m)2, and left ventricular mass index (LVMI) = LVM/BSA. Left ventricular ejection fraction (LVEF) was measured by the biplane Simpson method, the left atrial volume (LAV) was measured by the biplane Simpson method at the apical 4- and 2-chamber views, and the left ventricular volume index (LAVI) was calculated as LAV/BSA [6].

The apical 3-chamber view, apical 2-chamber view, apical 4-chamber view, left ventricular mitral valve short-axis view, left ventricular papillary muscle short-axis view, and left ventricular apical short-axis view were selected. The Q-analysis system was started, the 2D-strain was entered to manually trace the boundary of the endocardium and epicardium, the region of interest (ROI) was determined, and the software automatically tracked the movement trajectory of the myocardial spots in each layer. Finally, the subendomyocardial global longitudinal strain (GLSendo), the mid-layer myocardial global longitudinal strain (GLSmid), the subepimyocardial global longitudinal strain (GLSepi), the subendomyocardial global circumferential strain (GCSendo), the mid-layer myocardial global circumferential strain (GCSmid), and the subepimyocardial global circumferential strain (GCSepi) were obtained (Fig. 1).

Fig. 1
figure 1

The software automatically tracks the movement trajectory of the myocardial spots in each layer to obtain layer-specific strain parameters. A Shows a schematic diagram of the apical 4-chamber view, and B shows a schematic diagram of the left ventricular mitral valve short-axis view

Full size image

The evaluation of left ventricular diastolic function was based on guidelines proposed by ASE/EACI in 2016 [7]. Using a simple random sampling method, 10 patients were randomly selected among the POI patients for intraobserver reproducibility testing, and another 10 patients were randomly selected for interobserver reproducibility testing.

SPSS 25.0 was used for statistical analysis. The data are expressed as mean ± standard deviation. The Kolmogorov–Smirnov test was used to determine the distribution type of continuous variables, and the Levene test was used to test the homogeneity of variance. If the data from both groups satisfied both the normal distribution and homogeneity of variance criteria, the two-independent-samples t test was performed; otherwise, the Mann–Whitney U test was used for two independent samples. The intraclass correlation coefficient (ICC) was used for the reproducibility test. P < 0.05 was statistically significant for all analyses.

Results

Among the forty-eight patients in the POI group, the oestrogen levels of twenty-two patients were less than 37 pmol/L (the lowest level of serum sex hormone testing equipment was 37 pmol/L), the oestrogen levels of the other twenty-six patients were 88.37 ± 48.68 pmol/L, and the FSH level of the POI group was 66.70 ± 27.89 mIU/ml. There were five patients with TS in the POI group; three of these patients had 45,X, and the chromosomes of the other two patients were 45,X/46,XX/47,XXX and 45,X/46,X,r(X). Among the POI patients, four had primary amenorrhoea, and the abnormal menstruation history of the other forty-four patients was 13.07 ± 9.33 months.

No significant difference in age, BSA, BMI, systolic blood pressure, diastolic blood pressure, or heart rate was found between the two groups (all P > 0.05) (Table 1).

Table 1 Routine clinical data of the two groups
Full size table

The IVST in the POI group was greater than that in the control group (P = 0.008), but there were no significant differences between the two groups in LVPWT, LVEDD, RWT, LVM, or LVMI (all P > 0.05). The values of E, E/A, and lateral e′ in the POI group were lower than those in the control group (all P < 0.05), while no differences in A, septal e′, average E/e′ or LVEF were found between the two groups (P > 0.05) (Table 2).

Table 2 Conventional echocardiographic parameters of the two groups
Full size table

As assessed under established guidelines [7], the left ventricular diastolic function of all the subjects remained normal, but the presence of individual abnormalities in the POI group (E, E/A, lateral e′) still suggested that there were adverse changes in left ventricular diastolic function in POI patients.

GLSendo, GLSmid, GLSepi, GCSendo, GCSmid and GCSepi were all lower in the POI group (P < 0.05 or P < 0.001). The longitudinal strain and circumferential strain parameters of the two groups all showed a decreasing trend from the subendocardium to the subepicardium (Table 3) (Figs. 2, 3).

Table 3 Layer-specific strains of the two groups
Full size table
Fig. 2
figure 2

Comparison of global longitudinal layer-specific strains and bull's eye diagrams in peak systolic between the control group and the POI group. A Shows the GLSendo, GLSmid, GLSepi and bull's eye diagrams in the control group, and B shows the same in the POI group. Each segment in the bull's eye diagram in A was uniformly red, but some segments in B became lighter and uneven, indicating the strains of these segments decrease

Full size image
Fig. 3
figure 3

Comparison of longitudinal layer-specific strains and circumferential layer-specific strains between the POI group and control group. GLSendo, GLSmid, GLSepi, GCSendo, GCSmid and GCSepi were all lower in the POI group. Similarly, the longitudinal and circumferential strain parameters of the two groups all exhibited a decreasing trend from the subendocardium to the subepicardium.*P < 0.05, **P < 0.001. Standard error was the measure of sampling error

Full size image

The intraobserver and interobserver coefficients of GLSendo, GLSmid, GLSepi, GCSendo, GCSmid, and GCSepi were greater than 0.900, so the layer-specific strains had acceptable reproducibility (Table 4).

Table 4 Intraobserver and interobserver reproducibility of layer-specific stains
Full size table

Discussion

Due to the loss of functional ovarian follicles, women with POI constantly have low oestrogen and face infertility, perimenopausal syndrome and other problems. Patients with POI also have a higher CVD risk [8,9,10], and early menopause is associated with an increased risk of heart failure [11].Since most women with POI do not have chest tightness, chest pain or other CVD-related clinical symptoms in the early stage, the risk of CVD is often ignored. Serological indicators and blood pressure are often used to detect the risk of CVD in patients with POI, but echocardiography is rarely used to test the myocardial function of POI patients. Layer-specific myocardial strain can more sensitively reflect subclinical myocardial changes in the early stage of disease than LVEF can [12, 13] and has been used in many recent studies of various diseases [14,15,16]. Therefore, we aimed to use layer-specific myocardial strain to evaluate left ventricular myocardial systolic function in POI patients.

In this study, the POI group had a thicker IVST than the control group (P = 0.008), suggesting that patients with POI may have left ventricular remodelling. According to the criteria for left ventricular hypertrophy proposed in guidelines [6] (LVMI > 95 g/m2 in females), all subjects in this study did not meet the criteria for left ventricular hypertrophy, but fifteen patients (34.25%) in the POI group met the criteria for left ventricular concentric remodelling (RWT > 0.42, LVMI ≤ 95 g/m2), indicating the occurrence of left ventricular remodelling in patients with POI. The possible pathophysiological mechanisms include the following: Oestradiol (E2), as a fast activator of endothelial nitric oxide synthase (NOS),can stimulate the production of nitric oxide (NO), and a lack of E2 in patients with POI results in reduced NO production by vascular endothelial cells and decreased vascular elasticity and compliance,then cardiac afterload increases, which promotes left ventricular remodelling and myocardial hypertrophy [17, 18]; otherwise, a low E2 can lead to abnormalities in the renin-angiotensin system (RAS) in the heart and systemic circulation and enhance the activity of angiotensin-converting enzyme (ACE), leading to ventricular remodelling and cardiac hypertrophy [19].

Echocardiography can not only evaluate changes in left ventricular geometry but also quantitatively evaluate changes in function. According to the guideline [7], apparent decreases in left ventricular diastolic function were not detected in any of the subjects; however, the POI group had lower E, E/A, and lateral e′ (P < 0.05 or P < 0.01), indicating there are still some signs of decreased diastolic function, which is generally consistent with relevant research [20]. An animal experiment showed that the rMCP-1 and rMCP-5 mRNAs in the cardiomyocytes of ovariectomized rats, as the isoforms of chymase that form angiotensin II (Ang II), participate in the loss of normal heart function and structure caused by ovariectomy in rodents, as indicated by decreased left ventricular diastolic function (increased E/e’) and increased LVEDD [21]. Another study showed deficiency of E2 led to reduced mitochondrial function in cardiomyocytes and inhibited NOS signalling, thereby inhibiting the GPR30 pathway, which together led to a decreased left ventricular diastolic function [18].

Changes in left ventricular diastolic function are often inseparable from changes in systolic function. However, there was no obvious abnormality in LVEF (P > 0.05), but conventional LVEF often cannot reflect subclinical changes in left ventricular systolic function. This study used layer-specific myocardial strain and revealed that GLSendo, GLSmid, GLSepi, GCSendo, GCSmid, and GCSepi in the POI group were lower than those in the control group. There findings suggested that there was a reduction in left ventricular systolic function in the POI group and that layer-specific myocardial strain could more sensitively detect left ventricular systolic function impairment in patients with POI than two-dimensional LVEF. Some possible mechanisms for the decrease in layer-specific strains of the left ventricle in the POI group are as follows: An animal experiment showed that E2 enhanced cardiac systolic function by regulating the expression of cAMP-L-type Ca2+ channel (cAMP-LTCC)-related genes and promoted cardioprotection against stress through the GPR30 nongenomic acute signalling pathway [22]. In addition, there are oestrogen receptors (ERs) in the arterial wall and myocardial tissue, including ERα, ERβ, and the G protein-coupled oestrogen receptor (GPER), and E2 might directly act on cardiomyocytes to enhance myocardial systolic function [23,24,25].There is a certain gradient in the deformability of the normal left ventricle myocardium, and the deformation of the myocardium from the endocardium to epicardium gradually decreases [26]. This study also confirmed this decreasing trend from the endocardium to the epicardium in all subjects.

Limitations of this study: The hospital serum sex hormone test equipment had 37 pmol/L as the baseline for oestrogen, so we could not collect the E2 levels of patients whose E2 levels were lower than 37 pmol/L. The sample was fairly small. This was only a preliminary study, and a follow-up study during hormone replacement therapy (HRT) was not conducted.

In summary, POI patients with normal LVEF may have subclinical left ventricular myocardial systolic impairment. Layer-specific myocardial strain can more sensitively detect subclinical left ventricular systolic impairment in patients with POI.

Availability of data and materials

The data underlying this article will be shared on reasonable request to the corresponding author.

References

  1. Webber L, Davies M, Anderson R, et al. ESHRE Guideline: management of women with premature ovarian insufficiency. Human Reprod (Oxford, England). 2016;31(5):926–37.

    Article  CAS  Google Scholar 

  2. Golezar S, Ramezani Tehrani F, Khazaei S, et al. The global prevalence of primary ovarian insufficiency and early menopause: a meta-analysis. Climacteric. 2019;22(4):403–11.

    Article  CAS  PubMed  Google Scholar 

  3. Subgroup M. Chinese Society of Obstetrics and Gynecology, Chinese Medical Association. Zhonghua Fu Chan Ke Za Zhi. 2023;58(10):721–8.

    Google Scholar 

  4. “The 2022 Hormone Therapy Position Statement of The North American Menopause Society” Advisory Panel. The 2022 Hormone Therapy Position Statement of The North American Menopause Society. Menopause. 2022;29(7):767–94.

    Article  Google Scholar 

  5. Roeters van Lennep JE, Heida KY, Bots ML, et al. Cardiovascular disease risk in women with premature ovarian insufficiency: a systematic review and meta-analysis. Eur J Prev Cardiol. 2016;23(2):178–86.

    Article  PubMed  Google Scholar 

  6. Lang RM, Badano LP, Mor-Avi V, et al. Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. 2015;28(1):1-39e14.

    Article  PubMed  Google Scholar 

  7. Nagueh SF, Smiseth OA, Appleton CP, et al. Recommendations for the evaluation of left ventricular diastolic function by echocardiography: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. 2016;29(4):277–314.

    Article  PubMed  Google Scholar 

  8. Tsiligiannis S, Panay N, Stevenson JC. Premature ovarian insufficiency and long-term health consequences. Curr Vasc Pharmacol. 2019;17(6):604–9.

    Article  CAS  PubMed  Google Scholar 

  9. Stevenson JC, Collins P, Hamoda H, et al. Cardiometabolic health in premature ovarian insufficiency. Climacteric. 2021;24(5):474–80.

    Article  CAS  PubMed  Google Scholar 

  10. Zhu D, Chung HF, Dobson AJ, et al. Age at natural menopause and risk of incident cardiovascular disease: a pooled analysis of individual patient data. Lancet Public Health. 2019;4(11):e553–64.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Ebong IA, Watson KE, Goff DC Jr, et al. Age at menopause and incident heart failure: the multi-ethnic study of atherosclerosis. Menopause. 2014;21(6):585–91.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Esposito R, Santoro C, Sorrentino R, et al. Layer-specific longitudinal strain in Anderson-Fabry disease at diagnosis: a speckle tracking echocardiography analysis. Echocardiography. 2019;36(7):1273–81.

    Article  PubMed  Google Scholar 

  13. Sharma S, Lassen MCH, Nielsen AB, et al. The clinical application of longitudinal layer specific strain as a diagnostic and prognostic instrument in ischemic heart diseases: a systematic review and meta-analysis. Front Cardiovasc Med. 2023;10:980626.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Shi J, Pan C, Kong D, et al. Left ventricular longitudinal and circumferential layer-specific myocardial strains and their determinants in healthy subjects. Echocardiography. 2016;33(4):510–8.

    Article  CAS  PubMed  Google Scholar 

  15. Shiino K, Yamada A, Scalia GM, et al. Early changes of myocardial function after transcatheter aortic valve implantation using multilayer strain speckle tracking echocardiography. Am J Cardiol. 2019;123(6):956–60.

    Article  PubMed  Google Scholar 

  16. Skaarup KG, Iversen A, Jørgensen PG, et al. Association between layer-specific global longitudinal strain and adverse outcomes following acute coronary syndrome. Eur Heart J Cardiovasc Imaging. 2018;19(12):1334–42.

    Article  PubMed  Google Scholar 

  17. Haynes MP, Sinha D, Russell KS, et al. Membrane estrogen receptor engagement activates endothelial nitric oxide synthase via the PI3-kinase-Akt pathway in human endothelial cells. Circ Res. 2000;87(8):677–82.

    Article  CAS  PubMed  Google Scholar 

  18. Li S, Gupte AA. The role of estrogen in cardiac metabolism and diastolic function. Methodist Debakey Cardiovasc J. 2017;13(1):4–8.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Ribeiro RF Jr, Pavan BM, Potratz FF, et al. Myocardial contractile dysfunction induced by ovariectomy requires AT1 receptor activation in female rats. Cell Physiol Biochem. 2012;30(1):1–12.

    Article  CAS  PubMed  Google Scholar 

  20. Aksoy MN, Akdemir N, Kilic H, et al. Pulse wave velocity and myocardial performance index in premature ovarian insufficiency. Scand Cardiovasc J. 2017;51(2):95–8.

    Article  PubMed  Google Scholar 

  21. Wang H, Sun X, Ahmad S, et al. Estrogen modulates the differential expression of cardiac myocyte chymase isoforms and diastolic function. Mol Cell Biochem. 2019;456(1–2):85–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Machuki JO, Zhang HY, Geng J, et al. Estrogen regulation of cardiac cAMP-L-type Ca2+ channel pathway modulates sex differences in basal contraction and responses to β2AR-mediated stress in left ventricular apical myocytes. Cell Commun Signal. 2019;17(1):34.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Gorodeski GI. Update on cardiovascular disease in post-menopausal women. Best Pract Res Clin Obstet Gynaecol. 2002;16(3):329–55.

    Article  PubMed  Google Scholar 

  24. Losordo DW, Kearney M, Kim EA, et al. Variable expression of the estrogen receptor in normal and atherosclerotic coronary arteries of premenopausal women. Circulation. 1994;89(4):1501–10.

    Article  CAS  PubMed  Google Scholar 

  25. Cheng SB, Graeber CT, Quinn JA, Filardo EJ. Retrograde transport of the transmembrane estrogen receptor, G-protein-coupled-receptor-30 (GPR30/GPER) from the plasma membrane towards the nucleus. Steroids. 2011;76(9):892–6.

    CAS  PubMed  Google Scholar 

  26. Huttin O, Girerd N, Coiro S, et al. Association between layer-specific longitudinal strain and risk factors of heart failure and dyspnea: a population-based study. J Am Soc Echocardiogr. 2019;32(7):854-865.e8.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Yu-lin Wang is thankful to her supervisor Li-Xue Yin for guidance. The graphic abstract was made by Figdraw.

Funding

No funding.

Author information

Authors and Affiliations

  1. Ultrasound in Cardiac Electrophysiology and Biomechanics Key Laboratory of Sichuan Province, Sichuan Provincial People’s Hospital, University of Electronic Science and Technology of China, Chengdu, 610072, China

    Yu-Lin Wang & Li-Xue Yin

  2. Department of Gynaecology and Obstetrics, Sichuan Provincial People’s Hospital, University of Electronic Science and Technology of China, Chengdu, China

    Mei Li

Authors
  1. Yu-Lin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Li-Xue Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Yu-lin Wang did the data collection, analysis and wrote the manuscript. Li-Xue Yin and Mei Li conceived the idea and also did a part of data analysis. All authors reviewed the manuscript.

Corresponding author

Correspondence to Li-Xue Yin.

Ethics declarations

Ethics approval and consent to participate

The study was approved by Sichuan People’s hospital’s ethic committee (No. 265), and all the subjects signed informed consent.

Consent for publication

All the subjects signed informed consent.

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 http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, YL., Yin, LX. & Li, M. Assessment of left ventricular myocardial systolic dysfunction in premature ovarian insufficiency patients using echocardiographic layer-specific myocardial strain imaging. Echo Res Pract 11, 20 (2024). https://doi.org/10.1186/s44156-024-00056-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s44156-024-00056-x

Keywords

Echo Research & Practice

ISSN: 2055-0464

Contact us