Two-dimensional Echocardiographic Assessment of Myocardial Strain: Important Echocardiographic Parameter Readily Useful in Clinical Field

Jae-Hyeong Park

doi:10.4070/kcj.2019.0200

Journal List > Korean Circ J > v.49(10) > 1132935

Go to TopGo to Top Go to BottomGo to Bottom

TOOLS

Park: Two-dimensional Echocardiographic Assessment of Myocardial Strain: Important Echocardiographic Parameter Readily Useful in Clinical Field

Review Article

Korean Circulation Journal 2019; 49(10): 908-931.

Published online: 22 July 2019

DOI: https://doi.org/10.4070/kcj.2019.0200

Two-dimensional Echocardiographic Assessment of Myocardial Strain: Important Echocardiographic Parameter Readily Useful in Clinical Field

Jae-Hyeong Park, MD, PhD

Department of Cardiology in Internal Medicine, Chungnam National University Hospital, Chungnam National University College of Medicine, Daejeon, Korea.

Correspondence to Jae-Hyeong Park, MD, PhD. Department of Cardiology in Internal Medicine, Chungnam National University Hospital, Chungnam National University College of Medicine, 282, Munhwa-ro, Jung-gu, Daejeon 35015, Korea. jaehpark@cnu.ac.kr

Received 29 June 2019 Accepted 3 July 2019

The Korean Society of Cardiology

(open-access, https://creativecommons.org/licenses/by-nc/4.0):

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Echocardiography is the first and is the most-available imaging modality for many cardiovascular diseases, and echocardiographic parameters can give much important information for diagnosis, treatment, and prognostic evaluations. Left ventricular ejection fraction (LVEF) is the most commonly used echocardiographic parameter for left ventricular (LV) systolic function. Although LVEF is used routinely in daily practice, it is calculated from volumetric change without representing true myocardial properties. Recently, strain echocardiography has been used to objectively measure myocardial deformation. Myocardial strain can give accurate information about intrinsic myocardial function, and it can be used to detect early-stage cardiovascular diseases, monitor myocardial changes with specific therapies, differentiate cardiomyopathies, and predict the prognosis of several cardiovascular diseases. Although strain echocardiography has been applied to measure the right ventricle and left atrium, in addition to analyzing the LV, many cardiologists who are not imaging specialists are unaware of its clinical use and importance. Therefore, this review describes the measurement and clinical utility of 2-dimensional strain analysis in various cardiovascular diseases.

Keywords: Echocardiography, Strain, Prognosis, Diagnosis, Left ventricle, Right ventricle

INTRODUCTION

The accurate evaluation of cardiac function plays a central role in diagnosing cardiovascular diseases, initiating specific therapeutic interventions, monitoring treatment, and determining the prognosis of a variety of cardiovascular conditions. Among the various imaging modalities, echocardiography is the first and is the most commonly used diagnostic method in cardiology field. It can provide valuable information about the anatomy and function of the heart.1)2) Left ventricular ejection fraction (LVEF) is the most commonly used echocardiographic parameter. It provides objective information about left ventricular (LV) systolic function, and it has been used as a powerful prognostic indicator for various cardiovascular diseases. LVEF has been used to diagnose and classify heart failure (HF),3)4) determine the suitability of device therapy,3)5) decide interventions for valvular heart diseases (VHDs),6)7) determine the need for specific medications,3)5) and predict prognosis.8) However, LVEF is a global volumetric parameter with ventricular load-dependence and had limitations such as significant inter- and intraobserver variability and geometric assumptions.9) Moreover, LVEF does not represent intrinsic myocardial properties.

Strain is a dimensionless index of a change in length between 2 points before and after movement. Myocardial strain can be measured using echocardiography with technical improvements. Strain echocardiography was introduced to the clinical field about 20 years ago, making it a relatively new echocardiographic modality that can measure myocardial deformation. Unlike LVEF, myocardial strain, as calculated by strain echocardiography, can afford indices of regional and global myocardial systolic function noninvasively and objectively.10) Strain echocardiography has been used to diagnose subclinical disease states,11)12) monitor changes in myocardial function with specific therapies,13) differentiate cardiomyopathies,14) and predict the prognosis of several cardiovascular diseases independently of LVEF.15)16)

This review discusses the basic concept, measurement, and clinical utility of 2-dimensional strain echocardiography (2DSTE).

WHAT IS MYOCARDIAL STRAIN?

Myocardial strain is a dimensionless measurement of myocardial deformation calculated as the change between the original length and the final length after contraction divided by the original length and presented as a percentage.17)18) After the contraction, the final length is shorter than the original length, so a negative strain value represents shortening, and a positive strain value indicates lengthening. The strain rate is the change in velocity between 2 points divided by the distance between the points and is represented as s⁻¹.

A strain analysis produces the peak strain, peak systolic strain rate, early diastolic strain rate, and late diastolic strain rate. Peak strain is the maximum strain value in the strain curve. Peak systolic strain is the maximum strain value during the ventricular ejection time. The global value is calculated using the average of all segments of strain measurement. Because the global longitudinal strain (GLS) value is negative, the absolute value |x| is used in this review (except tables) for a simpler interpretation. Systolic movement after systole causes post-systolic strain. The presence of post-systolic strain indicates the possibility of myocardial ischemia. LV dyssynchrony can be assessed using the standard-deviation of the time to peak systolic strain in multiple LV segments.

MEASUREMENT OF MYOCARDIAL STRAIN BY ECHOCARDIOGRAPHY

Myocardial strain can be measured using Doppler tissue imaging (DTI) echocardiography and 2DSTE.

The DTI echocardiographic modality can produce the strain and strain rate using the myocardial velocities. Because angle dependency and regional strain, not global strain, are the major limitations of the DTI methods,17) this modality has seen limited clinical use.

2DSTE, on the other hand, tracks ultrasonic speckles within myocardial tissue to produce regional and global myocardial strain values from 2-dimensional echocardiographic images.19) 2DSTE can produce longitudinal strain, which assesses the apex to base deformation (usually measured from apical views), and radial or circumferential strain calculated from parasternal short-axis views (Figure 1). Although 2DSTE can be affected by afterload, it can give strain values angle-independently with low inter- and intraobserver variability. In 1 study comparing the strain-analyzing algorithms of 9 different vendors, the interobserver relative mean error in measuring the GLS of the LV (LVGLS) ranged from 5.4 to 8.6%, and interobserver mean error ranged from 4.9% to 7.3%.20) These variabilities were superior or at least comparable to those of LVEF measurements (10.1% and 7.9%, respectively).20) Thus, 2DSTE has been adopted in many echocardiographic machines and echocardiographic laboratories.19) 2DSTE uses 2-dimensional images with an optimal frame rate of about 60 frames per second. Several analysis algorithms are available to measure myocardial strain using 2DSTE. EchoPAC PC software (GE Medical Systems, Milwaukee, WI, USA), velocity vector imaging (VVI, Siemens Medical Solutions, Mountain View, CA, USA), and Tomtec software (Image Arena 4.6; TOMTEC Imaging Systems, Munich, Germany) are the most commonly used 2DSTE algorithms (Figure 2).21) After tracing the endocardial border on an end-diastolic frame, the software automatically tracks the contour on subsequent frames. The region of interest is determined automatically and can be adjusted to fit the thickness of the myocardium. The software can provide global and regional myocardial strain values automatically after tracing, and some algorithms provide bull's eye mapping values for the 17 segments (Figure 3).

Figure 1

Multidimensional strain measurement analysis by 2DSTE in a healthy individual. Arrows denote the direction of movements. Myocardial shortening shows in the longitudinal (A), circumferential (B), and radial directions (C). Myocardial contraction in the longitudinal and circumferential directions during the systolic period represents a negative strain value, and thickening and lengthening in the radial direction shows a positive strain value.

2DSTE = 2-dimensional strain echocardiography.

Figure 2

A demonstration of 3 different algorithms in a healthy individual. (A) EchoPAC PC software (GE Medical Systems, Milwaukee, WI, USA), (B) VVI (Siemens Medical Solutions, Mountain View, CA, USA), and (C) Tomtec software (Image Arena 4.6; TOMTEC Imaging Systems, Munich, Germany) are the 3 most commonly used algorithms in 2-dimensional speckle tracking echocardiography. Note the vendor differences in the measurement of GLS.

GLS = global longitudinal strain; VVI = velocity vector imaging.

Figure 3

Demonstration of a 2-dimensional strain analysis with GE EchoPAC PC software. After tracing of the endocardial border, the software provides global and regional myocardial strain values automatically in apical 4 chamber (A), apical 2 chamber (B), and apical 3 chamber views (C). The GE EchoPAC algorithm can provide bull's eye maps of regional longitudinal strain values (D).

Because vendor differences occur in the measurement of myocardial strain (Figure 2), clinicians should know the analytic method and vendor when interpreting previously published studies. Farsalinos et al.20) compared longitudinal strain measurements among 7 echocardiographic machines and 9 measurement software programs. The reference LVGLS values in 62 volunteers ranged from 18.0% to 21.5%, with absolute differences between vendors of up to 3.7%. Among the 9 vendors, the General Electric (GE) strain was higher than the Philips (Andover, MA, USA) strain. Therefore, researchers should use the same echocardiographic machines and algorithms before and after procedures or treatments they want to test in prospective researches. In retrospective studies comparing the strain change in stored echocardiographic images, researchers can use vendor-independent algorithms. The GE EchoPAC PC software is a vendor-specific algorithm that can measure myocardial strain only from images acquired by GE echocardiographic machines. However, VVI and Tomtec software are vendor-independent and can analyze echocardiographic images from any echocardiographic machine.

MYOCARDIAL STRAIN IN TREATMENT GUIDELINES AND CLINICAL PRACTICE

Because strain echocardiography can detect subclinical myocardial damage22) and objectively compare subtle changes before and after treatment,13) it has been incorporated into current clinical guidelines.23)24) The guidelines for cardio-oncology suggest that a reduction in LVGLS>15% from baseline could suggest the risk of chemotherapeutic-agent-associated cardiotoxicity.23)24) The guidelines recommend the use of same imaging modality that produces high-quality radiation-free imaging for continued screening throughout the treatment pathway. If clinicians want to use strain echocardiography to screen for cardiotoxicity, they should use the same echocardiographic machine and analyzing algorithm in the acquisition and analysis of echocardiographic images.

LVGLS can be used as a marker of systolic LV function in clinical practice. However, the use of strain echocardiography in current clinical practice was still low in 1 survey performed in 2017.25) Although most of the study participants (97%) were aware of strain echocardiography, only 58% of them performed strain echocardiography in their clinical practice or research in Korea. The diversity of strain measurements and lack of normal reference values for myocardial strain are 2 common reasons for not using strain echocardiography in the clinic. Because many study participants had a favorable view of it, the use of strain echocardiography is expected to increase over time.

CLINICAL USE OF STRAIN ECHOCARDIOGRAPHY

Strain echocardiography of the left ventricle

LV is the most common indication of the strain echocardiography, and LVGLS is the most commonly used strain value. It was calculated as the mean GLS value of the apical 4-, 3-, and 2-chamber views.

Normal reference value for the left ventricular global longitudinal strain

The identification of disease states requires a normal reference value. The normal LVGLS values vary according to the characteristics of the participants and the echocardiographic vendor.26)27) A proposed peak GLS value of 20% was proposed as a reference value for a healthy person.16) Table 1 summarizes the normal reference values for the LV.27)28)29)30)31) In this table, negative values mean systolic shortening, and lower values mean better systolic function. In 1 study of normal Korean adults, the mean LVGLS value was 20.4±2.2%, and females had significantly higher LVGLS than males (21.2±2.2% vs. 19.5±1.9%, p<0.001).27) A meta-analysis of 2,597 subjects from 24 studies reported a normal LVGLS value of 19.7% (95% confidence interval [CI], 20.4% to 18.9%).28) The mean value of normal global circumferential strain (GCS) was 23.3% (95% CI, 24.6% to 22.1%), and the mean global radial strain was 47.3% (95% CI, 43.6% to 51.0%).28) Generally, LVGLS decreases with age.16)

Table 1

Normal reference values for LVGLS by sex and vendor

Parameter	First author	Study type	No. (male/female)	Vendor	Normal range
Parameter	First author	Study type	No. (male/female)	Vendor	Total	Female	Male
LVGLS (%)	Sugimoto et al.29)	Prospective	549 (227/322)	Tomtec	−22.5±2.7 (95% CI, −27.7 to −17.2)	−23.0±2.7 (95% CI, −28.2 to −17.8)	−21.7±2.5 (95% CI, −26.7 to −16.7)
	Takigiku et al.30)	Prospective	333 (208/125)	GE	−21.3±2.1
			330 (195/135)	Philips	−18.9±2.5
			337 (235/102)	Toshiba	−19.9±2.4
	Mora et al.31)	Prospective	90 (52/38)	GE	−21.1±2.1	−21.7±2.1	−20.7±2.0
	Park et al.27)	Retrospective	501 (236/265)	GE	−20.4±2.2 (95% CI, −25.4 to −16.7)	−21.2±2.2 (95% CI, −26.8 to −17.5)	−19.5±1.9 (95% CI, −23.6 to −16.1)
	Yingchoncharoen et al.28)	Meta-analysis	2,597		−19.7 (95% CI, −20.4 to −18.9)
LVGCS (%)	Sugimoto et al.29)	Prospective	549 (227/322)	Tomtec	−31.9±4.5 (95% CI, −40.6 to −23.1)	−32.2±4.4 (95% CI, −40.7 to −23.6)	−31.4±4.6 (95% CI, −40.5 to −22.3)
	Takigiku et al.30)	Prospective	333 (208/125)	GE	−22.8±2.9
			330 (195/135)	Philips	−22.2±3.2
			337 (235/102)	Toshiba	−30.5±3.8
	Mora et al.31)	Prospective	90 (52/38)	GE	−21.6±3.9	−21.3±3.4	−21.9±4.3
	Yingchoncharoen et al.28)	Meta-analysis	2,597		−23.3 (95% CI, −24.6 to −22.1)
LVGRS (%)	Sugimoto et al.29)	Prospective	549 (227/322)	Tomtec	37.4±8.4 (95% CI, 21.1 to 53.8)	38.2±8.5 (95% CI, 21.5 to 54.8)	36.3±8.0 (95% CI, 20.6 to 52.1)
	Takigiku et al.30)	Prospective	333 (208/125)	GE	54.6±12.6
			330 (195/135)	Philips	36.3±8.2
			337 (235/102)	Toshiba	51.4±8.0
	Mora et al.31)	Prospective	90 (52/38)	GE	33.5±10.2	32.8±10.7	34.0±9.9
	Yingchoncharoen et al.28)	Meta-analysis	2,597		47.3 (95% CI, 43.6 to 51.0)

Data are shown as mean±standard deviation or number. Negative values mean systolic shortening and lower values mean better systolic function in LVGLS.

CI = confidence interval; GE = General Electric; GLS = global longitudinal strain; LVGCS = left ventricular global circumferential strain; LVGLS = left ventricular global longitudinal strain; LVGRS = left ventricular global radial strain.

Use in ischemic heart diseases

LVGLS can be used to differentiate ischemic heart diseases in patients with acute chest pain. Some software can produce bull's eye maps to show specific ischemia patterns (Figure 4). Patients with significant coronary artery disease (CAD) have significantly lower LVGLS than healthy people.32) The global longitudinal peak systolic strain is significantly lower in patients with CAD than in patients without CAD (17.1±2.5% vs. 18.8±2.6%, p<0.001). Global longitudinal peak systolic strain is an independent predictor of CAD after adjusting for baseline data, exercise tests, and conventional echocardiography (odds ratio [OR], 1.25 per 1% decrease, p=0.016).

Figure 4

Two-dimensional speckle tracking echocardiography can produce bull's eye maps that show specific ischemia patterns in patients with ischemic heart disease of the LAD (A), the LCX (B), and the RCA (C).

LAD = left anterior descending coronary artery; LCX = left circumflex coronary artery; RCA = right coronary artery.

In patients with acute myocardial infarction (AMI), LVGLS correlates positively with the extent of infarction size and the peak concentration of cardiac troponin T level.33)34) Regional wall motion assessment with VVI was used to detect significant ischemia in patients with acute chest pain who visited an emergency room.35) Kim et al.35) showed different peak radial strain values among normal motion, hypokinesia, and akinesia (31.74±9.15% for normal, 24.33±6.28% for hypokinesia, 20.30±7.78% for akinesia, p<0.01).

LVGLS plays a valuable role in determining prognosis. LVGLS assessed after reperfusion in AMI patients was a good prognostic marker for LV remodeling and adverse clinical events.36)37)38) Mechanical dispersion, assessed by the standard deviation of time to peak negative strain from 16 myocardial segments, was a good predictor of ventricular arrhythmias and sudden cardiac death in a prospective multicenter trial.39) Longer mechanical dispersion values reflect more heterogeneous myocardial contractions with increased regional dyssynchrony.

Use in valvular heart diseases

The treatment guidelines for VHD recommend surgical or procedural correction for VHD patients with symptoms and a failing LV.6)7) Prompt intervention can reduce further deterioration of myocardial function and enhance patient survival. However, the determination of optimal timing is difficult in asymptomatic patients with moderate to severe VHD. LVGLS can detect subclinical myocardial dysfunction before an overt reduction in LVEF and can thus be used as a marker to determine intervention time. Therefore, myocardial strain can be used to estimate myocardial performance and determine the optimal timing for surgical or procedural correction.

LVGLS can detect subclinical LV dysfunction in patients with aortic stenosis (AS). Patients with severe AS and LVEF in the normal range had decreased LVGLS compared with controls. Decreased LVGLS was also associated with an increased LV mass index and myocardial dysfunction.40) LVGLS was a significant predictor of death and aortic valve (AV) replacement in asymptomatic patients with severe AS and normal LVEF (hazard ratio [HR], 1.14 for 1% of LVGLS; 95% CI, 1.01 to 1.28; p=0.037).41) An LVGLS <15.0% was associated with significant excess mortality after adjustment for the Society of Thoracic Surgeons (STS) predicted risk of morbidity and mortality score, transaortic peak pressure gradient, AV calcification, and valvulo-arterial impedance. In asymptomatic patients with moderate to severe AS, an LVGLS of 15.9% could be used as a reference value in the prediction of adverse events, and patients with LVGLS <15.9% had a poor prognosis.42) Preserved LVGLS (>17.0%) was a positive prognostic marker in patients with paradoxical low-flow, low-gradient severe AS.43)

In patients with severe mitral regurgitation (MR), LVGLS can provide prognostic information. Decreased resting LVGLS (<18.0%) before surgical mitral valve (MV) repair was associated with post-operative LV dysfunction in patients with severe MR, regardless of baseline LVEF.44) Another study with moderate-to-severe primary MR showed that decreased LVGLS (<19.9%) was significantly and independently associated with long-term LV systolic dysfunction after MV repair.45) Mentias et al.46) also showed that reduced exercise capacity and decreased resting LVGLS (<21.0%) were associated with mortality, adding prognostic value to other parameters indicating a negative prognosis such as STS score, LV end-systolic dimension, and an effective MR orifice.

Use in heart failure

Myocardial strain is a systolic parameter that can be used to diagnose and treat HF. LVGLS is reduced in patients with HF regardless of their LVEF, and it has demonstrated better prognostic value than LVEF in a large cohort of patients with acute HF and echocardiographic studies.47)

HF patients with reduced ejection fraction (HFrEF), especially those with dilated cardiomyopathy, have reduced GCS, suggesting impaired myocardial thickening. Cho et al.48) found that LVGCS was a more-powerful predictor than LVEF of adverse cardiac events in 201 HFrEF patients (HR, 1.15 per 1% decrease of LVGCS; 95% CI, 1.04 to 1.28; p=0.006).

In HF patients with preserved ejection fraction (HFpEF), diastolic dysfunction is considered a key pathophysiologic finding. LVGLS can detect systolic myocardial dysfunction in patients with HFpEF. Park et al.47) found decreased LVGLS values in about 84% of patients with HFpEF, and decreased LVGLS was associated with increased all-cause mortality, even in patients with HFpEF. Impaired systolic performance, as assessed by an LVGLS <15.8%, was found in 52% of study patients with HFpEF, and it was a significant prognostic marker of adverse clinical outcomes, including cardiovascular death, HF hospitalization, or aborted cardiac arrest in the Treatment of Preserved Cardiac Function Heart Failure With an Aldosterone Antagonist trial.49)

LVGLS is regarded as the most sensitive marker of subclinical myocardial dysfunction, even in asymptomatic patients who have not developed overt cardiomyopathy. In a study of 60 asymptomatic diabetic patients with normal LVEF and 25 age-matched healthy volunteers, decreased LVGLS (<17.2%) correlated with the duration of diabetes and could be used to detect subclinical diabetic cardiomyopathy.50) Moreover, LVGLS and subendocardial radial strain were significantly decreased in patients with poorly controlled diabetes.51) LVGLS correlates with the extent of cardiac fibrosis and myocyte hypertrophy in animal models with hypertension, and an abnormal LVGLS value was associated with the diastolic stiffness of the chamber.52)

Use in cardio-oncology

HF can result from certain cancer therapies. Cardiotoxicity from anticancer chemotherapy is a leading cause of morbidity and mortality in cancer survivors.23)53) Because the discontinuation of cardiotoxic drugs and prompt HF management can reduce further deterioration of cardiac function in patients undergoing anticancer treatment, the early detection of cardiotoxicity is important. Echocardiography is the most commonly used imaging study in the screening and diagnosis of cardiotoxicity, and LVEF is the gold standard in determining cardiotoxicity. Therefore, LVEF should be assessed before and periodically during treatments for the early detection of cardiac dysfunction.23) Cardiotoxicity is diagnosed when the follow-up LVEF falls below 50%, or when the LVEF decreases by >10% compared to the baseline value.

However, LVEF is a volumetric parameter that does not show myocardial properties. LVGLS has been introduced to screen for and detect cardiotoxicity. Baseline LVGLS can be an effective measurement for discovering patients at high risk for cardiac events. An LVGLS <17.5% was associated with a 6-fold increase in cardiac events after anthracycline-based chemotherapy (p<0.001).54) Follow-up LVGLS was the most reliable marker of myocardial dysfunction, even in patients with normal LVEF. Although no absolute LVGLS value has been set for the detection of cardiotoxicity, a cut-off value of 17.5% to 19.0% can be used.24)55)56) The other indicator is a reduction in LVGLS >15% from the baseline value.23)24) Thus, the use of LVGLS seems to be increased over time in the cardio-oncology fields. For the best comparison of LVGLS values, LVGLS should be measured each time using the same echocardiographic machine and the same analyzing software.

Myocardial strain can be used to determine the effect of a treatment. The use of a beta-blocker can improve cardiac function in patients with anthracycline- and trastuzumab-induced cardiotoxicity.13) The authors showed improved LVGLS in patients treated with beta-blockers (from 17.6±2.3% to 19.8±2.6%, p<0.001). Jung et al. clearly showed that HF medication improved HF symptoms and restored the LVGLS value in a patient with adriamycin-induced cardiotoxicity (Figure 5).57)

Figure 5

The trend of GLS with treatment of HF in a patient with anthracycline- and trastuzumab-induced cardiotoxicity. GLS was −8.3% at initial presentation (A), improved after 3 months (−13.0%, B), and 6 months of HF management (−17.1%, C) (adapted and modified from Jung MH et al.57) with permission).

GLS = global longitudinal strain; HF = heart failure.

Use in the differentiation of hypertrophied myocardium

2DSTE can help differentiate pathologic LV hypertrophy from physiologic adaptations (Figure 6). Pathologic LV hypertrophy includes hypertrophic cardiomyopathies and infiltrative cardiomyopathy.

Figure 6

Representative peak longitudinal strain echocardiographic bull's eye maps from patients with various diseases and a healthy person. (A) Healthy. (B) An athlete with compensatory mild left ventricular hypertrophy and a normal strain plot. (C) Cardiac amyloidosis showing severely reduced strain in the basal and midventricular segments with preservation of the apical segments. (D) Hypertensive heart disease with thickened myocardium. (E) Hypertrophic cardiomyopathy involving the whole ventricle. (F) Apical hypertrophic cardiomyopathy, with reduced strain in the apical segments.

Athletes can have a hypertrophied LV, so-called athlete's heart, from intensive and prolonged exercise training,58) and it is difficult to differentiate such a normal adaptation from pathologic changes.59) Butz et al.60) demonstrated that LVGLS can differentiate athlete's heart from pathologic LV hypertrophy. They included 15 hypertrophic cardiomyopathy (HCM) patients, 20 athletes, and 18 normal subjects. LVGLS in the athletes was significantly better than in patients with HCM (15.2±3.6% vs. 8.1±3.8%, p<0.001). Compared with normal populations, athletes have slightly decreased LVGLS values, as shown in previously published data.16)27) However, no study has yet produced a reference value for athletes. In a large cohort including 1,120 trained young athletes, females had better LVGLS than males, and LVGLS decreased as the cardiovascular demand of their sports increased.61)

Patients with HCM usually have reduced LVGLS despite having a normal LVEF.62) LVGLS can detect subclinical myocardial dysfunction in patients with a genetic mutation before the phenotypic expression of HCM.63) LVGLS in HCM patients was significantly lower than that in hypertensive patients, even though both groups had a similar degree of LV hypertrophy.14) The global longitudinal strain rate and early diastolic strain rate of the septum correlated well with the extent of interstitial fibrosis and degree of myocyte hypertrophy and disarray in histologically proven HCM patients.64)

Cardiac amyloidosis is a form of pathologic LV hypertrophy that results from an accumulation of abnormal amyloid proteins in the interstitial spaces of the heart. LVGLS was significantly reduced in cardiac amyloidosis patients.14) Cardiac amyloidosis patients often show a typical strain image pattern, an ‘apical sparing’ or ‘cherry-on-top’ pattern, in the bull's eye maps of GLS analyses (Figure 7).14)65) Because the regional strain values differ significantly between the apex and basal segments, the apical–septal to basal–septal segmental longitudinal strain ratio can be used to diagnose cardiac amyloidosis.66) The relative regional strain ratio (RRSR), a measure of the relative sparing of the apical longitudinal strain, can be used as a prognostic marker, with a high RRSR associated with a higher incidence of poor clinical outcomes in patients with cardiac amyloidosis.67) Reduced LV longitudinal function, as assessed by LVGLS, was an independent prognostic factor of survival in 206 patients with light-chain amyloidosis.68) Fabry disease is an infiltrative disease that has an echocardiographic pattern similar to HCM, and reduced LVGLS was associated with poor myocardial function in patients with Fabry disease.69)

Figure 7

Typical echocardiography features in a patient with cardiac amyloidosis. Thickened left ventricular wall, up to 14 mm on the conventional echocardiographic study (A). In this representative bull's eye map of longitudinal strain by speckle tracking echocardiography (B), the longitudinal strain of the apex is preserved, in contrast to those of the other midventricular or basal segments, suggesting ‘apical sparing’ or a ‘cherry-on-top’ pattern.

GLS = global longitudinal strain.

Strain echocardiography of the right ventricle

Strain echocardiography has been also used to measure right ventricular (RV) function.70) Because RV systolic dysfunction is a well-known marker of poor prognosis in many cardiovascular diseases,71)72) the objective assessment of RV function can play an important role in the diagnosis and treatment of pulmonary arterial hypertension (PAH), HF, ischemic heart disease, and other cardiomyopathies. Although many researchers measure RV myocardial strain with the same algorithm of LV strain, there are several limitations including validation with other diagnostic methods, measurement of the RV free wall or total RV (including the interventricular septum), and vendor differences.70)

Unfortunately, no specialized algorithm is available for measuring RV myocardial strain. Therefore, the LV algorithm is used to assess RV myocardial strain. Because the RV has a different anatomy and physiology from the LV, validation studies are needed for this application to the other ventricle. Only longitudinal strain values are used in the measurement of RV myocardial strain; the major difference between RV myocardial strain and LV myocardial strain is the inability to measure circumferential strain and radial strain along with longitudinal strain in the RV.

For validation, several studies have shown a good correlation between GLS of RV (RVGLS) and sonomicrometry, magnetic resonance imaging analyses, and cardiac catheterization data.73)74)75)76)77)78)79)80)81)

Including the interventricular septum in the measurement of RVGLS is another problem. There are 2 kinds of RVGLS measurement; RVGLS_total and RVGLS_{free wall} (Figure 8). RVGLS_total value includes the strain value of the ventricular septum added to RVGLS_{free wall}. Debate continues about which parameter better predicts future clinical events.

Figure 8

A demonstration of the 2 different methods used to measure RV strain. RVGLS can be measured from the RVGLS_total (A) or from the RVGLS_{free wall} (B).

RV = right ventricular; RVGLS = right ventricular global longitudinal strain.

The other problem with RVGLS is the vendor differences. Because echocardiographic machines and analyzing algorithms can produce different values, clinicians should take those factors into account when interpreting study data.

Normal reference value for the right ventricular global longitudinal strain

Because of vendor differences and the possibility of including the interventricular septum in the measurement of RVGLS, we should consider age, sex, echocardiographic machine and analyzing software, and whether the measurement is RVGLS_total or RVGLS_{free wall}. Table 2 summarizes the normal ranges for RVGLS. In this table, negative values mean systolic shortening, and lower values mean better systolic function.

Table 2

Normal reference values for RVGLS by sex, age, and vendor (adapted and modified from Lee et al.70) with permission)

Parameter	First author	Study type	No. (male/female)	Vendor	Normal range
Parameter	First author	Study type	No. (male/female)	Vendor	Total	Female	Male
RVGLS_total (%)	Muraru et al.82)	Prospective	276 (123/153)	GE	−25.8±3.0	−26.7±3.1	−24.7±2.6
	Park et al.83)	Retrospective	493 (232/261)	GE	−21.5±3.2 (95% CI, −21.8 to −21.2)	−20.7±2.9 (95% CI, −21.0 to −20.3)	−22.3±3.3 (95% CI, −22.7 to −21.9)
						<30 yr: −22.8±2.5	<30 yr: −20.8±2.9
						31–40 yr: −23.2±3.6	31–40 yr: −20.1±2.5
						41–50 yr: −22.5±3.1	41–50 yr: −20.4±3.0
						51–60 yr: −21.8±3.1	51–60 yr: −21.0±3.3
						>60 yr: −21.3±3.7	>60 yr: −21.0±3.0
	Rimbas et al.84)	Prospective	70 (34/36)	GE	−24.0±3.5
					<40 yr: −24±3	<40 yr: −26±3	<40 yr: −22±2
					41–60 yr: −24±4	41–60 yr: −24±4	41–60 yr: −23±4
					>61 yr: −24±4	>61 yr: −25±5	>61 yr: −23±4
	Meris et al.85)	Prospective	100 (54/46)	GE	−24.2±2.9 (95% CI, −30.0 to −17.7)
	Fine et al.86)	Retrospective	186 (72/114)	VVI	−20.4±3.2
RVGLS_{free wall} (%)	Muraru et al.82)	Prospective	276 (123/153)	GE	−30.5±3.9	−31.6±4.0	−29.3±3.4
	Park et al.83)	Retrospective	493 (232/261)	GE	−26.4±4.2 (95% CI, −26.8 to −26.0)	−26.0 to −25.1 (95% CI, −27.8 to −26.7)	−25.5±3.8 (95% CI, −26.0 to −25.1)
						<30 yr: −28.2±3.8	<30 yr: −25.8±3.7
						31–40 yr: −28.5±4.7	31–40 yr: −24.7±3.5
						41–50 yr: −27.3±4.0	41–50 yr: −25.3±3.6
						51–60 yr: −27.1±4.2	51–60 yr: −25.9±4.2
						>60 yr: −25.2±4.9	>60 yr: −26.1±3.8
	Meris et al.85)	Prospective	100 (54/46)	GE	−28.7±4.1 (95% CI, −37.7 to −19.8)
	Fine et al.87)	Prospective	116 (49/67)	GE	−26.0 ± 4.0
	Rimbas et al.84)	Prospective	70 (34/36)	GE	−28.0±6.0
					<40 yr: −28±6	<40 yr: −32±5	<40 yr: −25±4
					41–60 yr: −27±7	41–60 yr: −27±7	41–60 yr: −26.5±6
					>61 yr: −29±7	>61 yr: −31±7	>61 yr: −27±5
	Fine et al.87)	Meta-analysis	7 studies	GE	−27±2 (95% CI, −30 to −24)
	Fine et al.86)	Retrospective	187 (72/114)	VVI	−21.7 ± 4.2

Data are shown as mean±standard deviation or number. Negative values mean systolic shortening, and lower values mean better systolic function.

CI = confidence interval; GE = General Electric; GLS = global longitudinal strain; RVGLS = right ventricular global longitudinal strain; VVI = velocity vector imaging.

Use in pulmonary hypertension

RV function can be deteriorated along with increase of pulmonary arterial pressure in patients with pulmonary hypertension. PAH is usually associated with increased pulmonary vascular resistance and subsequent RV systolic dysfunction. The presence of RV dysfunction in PAH patients has been regarded as a sign of poor prognosis. An RV strain analysis plays an important role in detecting RV dysfunction in patients with PAH.88) In patients with PAH, reduced RVGLS_total demonstrated a good correlation with serum B-type natriuretic peptide concentration and 6-minute walking distance.81)89) RVGLS_total also had good correlations with invasive hemodynamic data obtained during right heart catheterization81)90) and RV ejection fraction by cardiac magnetic resonance imaging data (r=−0.69, p<0.001).77) RVGLS_total≤15.5% was associated with poor event-free survival (HR, 4.906; p=0.001) and increased mortality (HR, 8.842; p=0.005).38) Reduced RVGLS_{free wall} (≤19.4%) was the best predictor of cardiovascular events in patients with PAH.91) Fine et al.92) reported an increased risk (1.46 higher risk of death per 6.7% decline in RVGLS_{free wall}) in a prospective cohort of 575 patients (mean age 56±18 years; 63% females).

In patients with idiopathic pulmonary fibrosis, RVGLS_total was significantly lower than in the control group, and reduced RVGLS_total (<12.0%) was a marker of poor long-term prognosis (HR, 4.7; p<0.001).93) RVGLS can detect subtle RV changes in patients with systemic sclerosis who have not developed symptoms.94)

Use in acute pulmonary embolism

Acute pulmonary embolism (PE) is a form of acute pressure overload in the RV. 2DSTE can quantify and characterize RV systolic dysfunction in acute PE patients (Figure 9). An RV strain analysis can demonstrate decreased midventricular strain in the RV free wall of such patients. Sugiura et al.95) showed decreased midventricular strain and RVGLS_total at the time of diagnosis and a significant improvement in the strain value after treatment. Although the RVGLS_total value was decreased in patients with acute PE, it did not significantly predict adverse long-term clinical events.96) However, decreased RVGLS_{free wall} (<15.85%) was associated with increased in-hospital events (OR, 1.12; 95% CI, 1.04 to 1.21; p=0.002) in 1 study,97) and midventricular RV strain was associated with unfavorable outcomes, including death, cardiac arrest, and recurrence of acute PE (HR, 2.95; 95% CI, 1.31 to 3.23; p=0.002) in another study.98)

Figure 9

Demonstration of longitudinal strain in the right ventricle of a patient with acute pulmonary embolism before (A) and after treatment (B). Before treatment, midventricular strain (arrows) decreased, as did the RVGLS_total (A). The midventricular strain (arrowheads) and RVGLS_total improved after treatment.

RVGLS = right ventricular global longitudinal strain.

Use in heart failure

The presence of RV dysfunction is known to indicate a poor prognosis in HF patients.72) In patients with advanced HF, RV failure is an important prognostic factor for mortality and indicator for advanced management strategies such as the implantation of an LV assist device (LVAD).99) The incidence of RV failure was 9–44% in patients with LVAD implantation.100) Although tricuspid annular plane systolic excursion (TAPSE; a common indicator of RV systolic function) failed to have predictive value, RVGLS_{free wall} (cutoff value<9.6%) was an independent marker of RV failure after LVAD therapy.101) Cameli et al.102) reported a correlation between RVGLS and the RV stroke work index in 41 patients referred for heart transplantation. The RV stroke work index had a good correlation with RVGLS_total (r=0.75) and RVGLS_{free wall} (r=0.82), but there was no correlation between TAPSE and tricuspid S′ velocity in these patients.

RVGLS_{free wall} showed a good correlation with RV myocardial fibrosis, which is a major pathophysiologic process in severe systolic HF (r=0.80, p<0.001).103) RVGLS_total and RVGLS_{free wall} both showed significant correlation with the symptomatic status of HF patients.104) RVGLS_total can be used as a poor prognostic marker in patients admitted for acute HF.105) Park et al.105) reported that reduced RVGLS_total (<12.0%) was associated with increased total mortality, and patients with biventricular dysfunction (LVGLS<9.0% and RVGLS_total<12.0%) had poorer survival than those without biventricular dysfunction (HR, 1.755; 95% CI, 1.473 to 2.091; p<0.001).

Use in ischemic heart disease

RVGLS_total determined using the GE algorithm correlated significantly with RV ejection fraction determined by cardiac resonance imaging (CMR, r=−0.797, p<0.001), and RVGLS≤15.4% was associated with a lower 1 year event-free survival than an RVGLS>15.4% (93.0% vs. 67.2%, p=0.030) in patients with ischemic cardiomyopathy.78) Impaired RVGLS_total (<15.5%) determined using the VVI algorithm correlated with a significantly lower survival rate and event free survival rate in patients with inferior AMI.71) RVGLS_total better correlated with the RV ejection fraction determined by CMR and had superior power to detect RV dysfunction (defined as an RV ejection fraction <50%) compared with other conventional RV parameters.80)

Use in cardiomyopathy involving the right ventricle

Arrhythmogenic RV cardiomyopathy (ARVC) is a rare disease in which fatty tissue replaces the normal RV myocardium. The reduced RVGLS seen in this condition can result from fatty deposition in the RV free wall. In 1 study with 14 patients with ARVC and 56 controls, the ARVC patients had significantly reduced RVGLS_{free wall} compared with the controls (17.8±6.7% vs. 24.6±4.5%, p<0.001).106) A cut off value of RVGLS_{free wall} <18% seemed to be superior to other conventional parameters.106)107)108) Also, RVGLS can detect the early stages of this disease.

RVGLS can be decreased by RV involvement in the pathologic processes of HCM. In 1 study comparing HCM and athletes with competitive endurance training, RVGLS_total was lower in the HCM patients than in the athletes.109) D'Andrea et al.110) reported that RVGLS_total and RVGLS_{free wall} both decreased in HCM patients compared with normal controls before and after exercise. They showed good correlation between exercise capacity and RVGLS_total (r=−0.56, p<0.001) and decreased contractile reserve in HCM patients.

Strain echocardiography of the left atrium

The left atrium (LA) modulates LV filling through 3 functions: reservoir for pulmonary venous flow during ventricular systole, conduit for pulmonary venous flow during early ventricular diastole, and booster pump function for atrial contraction during late ventricular diastole. Conventionally, echocardiography measures the size and volume of the LA and determines its function by volumetric analysis.16) Unlike conventional echocardiography, strain echocardiography can provide information about all 3 functions of the LA (Figure 10).111)112)

Figure 10

A left atrial strain analysis using 2DSTE in a healthy adult (A) and an illustration of the 3 phases of LA function (B) with an R-R gating analysis.

LA = left atrium; PACS = peak atrial contraction strain; PALS = peak atrial longitudinal strain; 2DSTE = 2-dimensional strain echocardiography.

In measuring LA strain, there is a lack of consensus about which regions to include in the calculation. A European task force recommended including only the lateral wall in measuring LA strain.113) In 1 meta-analysis study, the normal reference range for reservoir strain was 39% (95% CI, 38% to 41% from 40 articles), for conduit strain was 23% (95% CI, 21% to 25% from 14 articles), and for contractile strain was 17% (95% CI, 16% to 19% from 18 articles).112)

LA strain is commonly used to predict atrial fibrillation (AF) and future cardiovascular events. Reduced LA function is commonly found in AF patients, and impaired LA strain values are associated with future cardiovascular events.114)115) The LA reservoir and pump functions are reduced in patients with paroxysmal AF compared with subjects with a normal sinus rhythm regardless of their LA size, and LA functional impairment can be found before enlargement of the LA in patients with paroxysmal AF.116) Also, reduced LA strain was associated with the progression from paroxysmal AF to persistent AF in 1 study.117) A higher LA strain value after catheter ablation appeared to indicate a greater likelihood of maintaining the sinus rhythm.114)

The LA reservoir function can be used as a marker of future embolic events in patients with AF, and LA reservoir strain was associated with reduced future embolic risk (OR, 0.74; 95% CI, 0 to 0.82; p<0.001), with 15.4% as a cut-off level for higher embolic risk.118)

Reduced LA strain is a valuable parameter in the diagnosis and risk stratification of other diseases. Reduced LA reservoir strain (<17.5%) was used to diagnose HFpEF with a sensitivity of 89% and a specificity of 55%.119) LA reservoir strain was strongly associated with sudden cardiac death and HF hospitalization in HFpEF patients (HR, 0.96 per 1% increase in strain; 95% CI, 0.94 to 0.99; p=0.009),120) and in AMI patients (HR, 0.88 per 1% increase in strain; 95% CI, 0.85 to 0.90; p<0.001).121) However, that independent prognostic power disappeared after adjustment for LVGLS.

LA reservoir strain can be used to identify a need for MV surgery in patients with severe primary MR, and an LA reservoir strain ≤24.0% was associated with worse survival irrespective of preoperative symptoms in a prospective study.122) Reduced LA reservoir function was a significant and powerful predictor of cardiovascular death and MV surgery prompted by HF development (HR, 0.916 per 1% increase of LA strain; 95% CI, 1.29 to 10.05; p=0.014).123) An LA reservoir strain <21.0% independently predicted death, hospitalization, and HF worsening in patients with severe AS (HR, 2.88; 95% CI, 1.01 to 8.2; p=0.04).124)

CONCLUSIONS

Strain echocardiography has been used for about 20 years to measure myocardial deformation. Unlike LVEF, which measures volumetric changes in the LV, myocardial strain can provide objective myocardial information regionally and globally. Myocardial strain can easily be measured with 2DSTE on current echocardiographic machines at the time of echocardiographic examination. Although myocardial strain is easy to use and has many advantages over conventional echocardiographic indices, many cardiologists do not believe that myocardial strain can replace other echocardiographic indices including LVEF in the clinical field. Common reasons for not using myocardial strain in clinical applications include the complexity of strain measurement, diversity of measurements (including vendor differences), and a lack of normal reference values. However, those problems can be solved with technical improvements and clinical studies. Because myocardial strain has many advantages over other echocardiographic indices, including objective measurement with low inter- and intra-observer variabilities, early-stage detection (before symptom onset), and good prognostic value for future clinical events, it can be used with other conventional echocardiographic parameters to provide additional information during clinical decision making.

Notes

^{Conflict of Interest} The author has no financial conflicts of interest.

References

1. Kümler T, Gislason GH, Køber L, Torp-Pedersen C. Persistence of the prognostic importance of left ventricular systolic function and heart failure after myocardial infarction: 17-year follow-up of the TRACE register. Eur J Heart Fail. 2010; 12:805–811.

2. Joyce E, Hoogslag GE, Leong DP, et al. Association between left ventricular global longitudinal strain and adverse left ventricular dilatation after ST-segment-elevation myocardial infarction. Circ Cardiovasc Imaging. 2014; 7:74–81.

3. Ponikowski P, Voors AA, Anker SD, et al. 2016 ESC guidelines for the diagnosis and treatment of acute and chronic heart failure: the task force for the diagnosis and treatment of acute and chronic heart failure of the European Society of Cardiology (ESC)developed with the special contribution of the Heart Failure Association (HFA) of the ESC. Eur Heart J. 2016; 37:2129–2200.

4. Lee JH, Kim MS, Kim EJ, et al. KSHF guidelines for the management of acute heart failure: part I. definition, epidemiology and diagnosis of acute heart failure. Korean Circ J. 2019; 49:1–21.

5. Yancy CW, Jessup M, Bozkurt B, et al. 2016 ACC/AHA/HFSA focused update on new pharmacological therapy for heart failure: an update of the 2013 ACCF/AHA guideline for the management of heart failure: a report of the American College of Cardiology/American Heart Association task force on clinical practice guidelines and the Heart Failure Society of America. J Am Coll Cardiol. 2016; 68:1476–1488.

6. Baumgartner H, Falk V, Bax JJ, et al. 2017 ESC/EACTS guidelines for the management of valvular heart disease. Eur Heart J. 2017; 38:2739–2791.

7. Nishimura RA, Otto CM, Bonow RO, et al. 2017 AHA/ACC focused update of the 2014 AHA/ACC guideline for the management of patients with valvular heart disease: a report of the American College of Cardiology/American Heart Association task force on clinical practice guidelines. Circulation. 2017; 135:e1159–95.

8. Lee JY, Sunwoo JS, Kwon KY, et al. Left ventricular ejection fraction predicts poststroke cardiovascular events and mortality in patients without atrial fibrillation and coronary heart disease. Korean Circ J. 2018; 48:1148–1156.

9. Otterstad JE, Froeland G, St John Sutton M, Holme I. Accuracy and reproducibility of biplane two-dimensional echocardiographic measurements of left ventricular dimensions and function. Eur Heart J. 1997; 18:507–513.

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

11. Haddad F, Hunt SA, Rosenthal DN, Murphy DJ. Right ventricular function in cardiovascular disease, part I: anatomy, physiology, aging, and functional assessment of the right ventricle. Circulation. 2008; 117:1436–1448.

12. Keramida K, Farmakis D, Bingcang J, et al. Longitudinal changes of right ventricular deformation mechanics during trastuzumab therapy in breast cancer patients. Eur J Heart Fail. 2019; 21:529–535.

13. Negishi K, Negishi T, Haluska BA, Hare JL, Plana JC, Marwick TH. Use of speckle strain to assess left ventricular responses to cardiotoxic chemotherapy and cardioprotection. Eur Heart J Cardiovasc Imaging. 2014; 15:324–331.

14. Phelan D, Thavendiranathan P, Popovic Z, et al. Application of a parametric display of two-dimensional speckle-tracking longitudinal strain to improve the etiologic diagnosis of mild to moderate left ventricular hypertrophy. J Am Soc Echocardiogr. 2014; 27:888–895.

15. Negishi K, Negishi T, Hare JL, Haluska BA, Plana JC, Marwick TH. Independent and incremental value of deformation indices for prediction of trastuzumab-induced cardiotoxicity. J Am Soc Echocardiogr. 2013; 26:493–498.

16. 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; 28:1–39.e14.

17. Marwick TH. Measurement of strain and strain rate by echocardiography: ready for prime time? J Am Coll Cardiol. 2006; 47:1313–1327.

18. Gorcsan J 3rd, Tanaka H. Echocardiographic assessment of myocardial strain. J Am Coll Cardiol. 2011; 58:1401–1413.

19. Collier P, Phelan D, Klein A. A test in context: myocardial strain measured by speckle-tracking echocardiography. J Am Coll Cardiol. 2017; 69:1043–1056.

20. Farsalinos KE, Daraban AM, Ünlü S, Thomas JD, Badano LP, Voigt JU. Head-to-head comparison of global longitudinal strain measurements among nine different vendors: the EACVI/ASE inter-vendor comparison study. J Am Soc Echocardiogr. 2015; 28:1171–1181.

21. Cho GY, Chan J, Leano R, Strudwick M, Marwick TH. Comparison of two-dimensional speckle and tissue velocity based strain and validation with harmonic phase magnetic resonance imaging. Am J Cardiol. 2006; 97:1661–1666.

22. Sarvari SI, Haugaa KH, Anfinsen OG, et al. Right ventricular mechanical dispersion is related to malignant arrhythmias: a study of patients with arrhythmogenic right ventricular cardiomyopathy and subclinical right ventricular dysfunction. Eur Heart J. 2011; 32:1089–1096.

23. Zamorano JL, Lancellotti P, Rodriguez Muñoz D, et al. 2016 ESC position paper on cancer treatments and cardiovascular toxicity developed under the auspices of the ESC Committee for practice guidelines: the task force for cancer treatments and cardiovascular toxicity of the European Society of Cardiology (ESC). Eur J Heart Fail. 2017; 19:9–42.

24. Kim H, Chung WB, Cho KI, et al. Diagnosis, treatment, and prevention of cardiovascular toxicity related to anti-cancer treatment in clinical practice: an opinion paper from the working group on cardio-oncology of the Korean Society of Echocardiography. J Cardiovasc Ultrasound. 2018; 26:1–25.

25. Lee JH, Park JH, Park SW, et al. Current awareness and use of the strain echocardiography in routine clinical practices: result of a nationwide survey in Korea. J Cardiovasc Ultrasound. 2017; 25:91–97.

26. Marwick TH, Leano RL, Brown J, et al. Myocardial strain measurement with 2-dimensional speckle-tracking echocardiography: definition of normal range. JACC Cardiovasc Imaging. 2009; 2:80–84.

27. Park JH, Lee JH, Lee SY, et al. Normal 2-dimensional strain values of the left ventricle: a substudy of the normal echocardiographic measurements in Korean population study. J Cardiovasc Ultrasound. 2016; 24:285–293.

28. Yingchoncharoen T, Agarwal S, Popović ZB, Marwick TH. Normal ranges of left ventricular strain: a meta-analysis. J Am Soc Echocardiogr. 2013; 26:185–191.

29. Sugimoto T, Dulgheru R, Bernard A, et al. Echocardiographic reference ranges for normal left ventricular 2D strain: results from the EACVI NORRE study. Eur Heart J Cardiovasc Imaging. 2017; 18:833–840.

30. Takigiku K, Takeuchi M, Izumi C, et al. Normal range of left ventricular 2-dimensional strain: Japanese ultrasound speckle tracking of the left ventricle (JUSTICE) study. Circ J. 2012; 76:2623–2632.

31. Mora V, Roldán I, Romero E, et al. Comprehensive assessment of left ventricular myocardial function by two-dimensional speckle-tracking echocardiography. Cardiovasc Ultrasound. 2018; 16:16.

32. Biering-Sørensen T, Hoffmann S, Mogelvang R, et al. Myocardial strain analysis by 2-dimensional speckle tracking echocardiography improves diagnostics of coronary artery stenosis in stable angina pectoris. Circ Cardiovasc Imaging. 2014; 7:58–65.

33. Sjøli B, Ørn S, Grenne B, Ihlen H, Edvardsen T, Brunvand H. Diagnostic capability and reproducibility of strain by Doppler and by speckle tracking in patients with acute myocardial infarction. JACC Cardiovasc Imaging. 2009; 2:24–33.

34. Bertini M, Mollema SA, Delgado V, et al. Impact of time to reperfusion after acute myocardial infarction on myocardial damage assessed by left ventricular longitudinal strain. Am J Cardiol. 2009; 104:480–485.

35. Kim KH, Na SH, Park JS. Role of quantitative wall motion analysis in patients with acute chest pain at emergency department. J Cardiovasc Ultrasound. 2017; 25:20–27.

36. Park YH, Kang SJ, Song JK, et al. Prognostic value of longitudinal strain after primary reperfusion therapy in patients with anterior-wall acute myocardial infarction. J Am Soc Echocardiogr. 2008; 21:262–267.

37. Lee SH, Lee SR, Rhee KS, Chae JK, Kim WH. Usefulness of myocardial longitudinal strain in prediction of heart failure in patients with successfully reperfused anterior wall ST-segment elevation myocardial infarction. Korean Circ J. 2019; 49:e69.

38. Choi SW, Park JH, Sun BJ, et al. Impaired two-dimensional global longitudinal strain of left ventricle predicts adverse long-term clinical outcomes in patients with acute myocardial infarction. Int J Cardiol. 2015; 196:165–167.

39. Haugaa KH, Grenne BL, Eek CH, et al. Strain echocardiography improves risk prediction of ventricular arrhythmias after myocardial infarction. JACC Cardiovasc Imaging. 2013; 6:841–850.

40. Cramariuc D, Gerdts E, Davidsen ES, Segadal L, Matre K. Myocardial deformation in aortic valve stenosis: relation to left ventricular geometry. Heart. 2010; 96:106–112.

41. Yingchoncharoen T, Gibby C, Rodriguez LL, Grimm RA, Marwick TH. Association of myocardial deformation with outcome in asymptomatic aortic stenosis with normal ejection fraction. Circ Cardiovasc Imaging. 2012; 5:719–725.

42. Lancellotti P, Donal E, Magne J, et al. Risk stratification in asymptomatic moderate to severe aortic stenosis: the importance of the valvular, arterial and ventricular interplay. Heart. 2010; 96:1364–1371.

43. Sato K, Seo Y, Ishizu T, et al. Prognostic value of global longitudinal strain in paradoxical low-flow, low-gradient severe aortic stenosis with preserved ejection fraction. Circ J. 2014; 78:2750–2759.

44. Mascle S, Schnell F, Thebault C, et al. Predictive value of global longitudinal strain in a surgical population of organic mitral regurgitation. J Am Soc Echocardiogr. 2012; 25:766–772.

45. Witkowski TG, Thomas JD, Debonnaire PJ, et al. Global longitudinal strain predicts left ventricular dysfunction after mitral valve repair. Eur Heart J Cardiovasc Imaging. 2013; 14:69–76.

46. Mentias A, Naji P, Gillinov AM, et al. Strain echocardiography and functional capacity in asymptomatic primary mitral regurgitation with preserved ejection fraction. J Am Coll Cardiol. 2016; 68:1974–1986.

47. Park JJ, Park JB, Park JH, Cho GY. Global longitudinal strain to predict mortality in patients with acute heart failure. J Am Coll Cardiol. 2018; 71:1947–1957.

48. Cho GY, Marwick TH, Kim HS, Kim MK, Hong KS, Oh DJ. Global 2-dimensional strain as a new prognosticator in patients with heart failure. J Am Coll Cardiol. 2009; 54:618–624.

49. Shah AM, Claggett B, Sweitzer NK, et al. Prognostic importance of impaired systolic function in heart failure with preserved ejection fraction and the impact of spironolactone. Circulation. 2015; 132:402–414.

50. Nakai H, Takeuchi M, Nishikage T, Lang RM, Otsuji Y. Subclinical left ventricular dysfunction in asymptomatic diabetic patients assessed by two-dimensional speckle tracking echocardiography: correlation with diabetic duration. Eur J Echocardiogr. 2009; 10:926–932.

51. Enomoto M, Ishizu T, Seo Y, et al. Subendocardial systolic dysfunction in asymptomatic normotensive diabetic patients. Circ J. 2015; 79:1749–1755.

52. Ishizu T, Seo Y, Kameda Y, et al. Left ventricular strain and transmural distribution of structural remodeling in hypertensive heart disease. Hypertension. 2014; 63:500–506.

53. Ewer MS, Ewer SM. Cardiotoxicity of anticancer treatments. Nat Rev Cardiol. 2015; 12:620.

54. Ali MT, Yucel E, Bouras S, et al. Myocardial strain is associated with adverse clinical cardiac events in patients treated with anthracyclines. J Am Soc Echocardiogr. 2016; 29:522–527.e3.

55. Thavendiranathan P, Poulin F, Lim KD, Plana JC, Woo A, Marwick TH. Use of myocardial strain imaging by echocardiography for the early detection of cardiotoxicity in patients during and after cancer chemotherapy: a systematic review. J Am Coll Cardiol. 2014; 63:2751–2768.

56. Charbonnel C, Convers-Domart R, Rigaudeau S, et al. Assessment of global longitudinal strain at low-dose anthracycline-based chemotherapy, for the prediction of subsequent cardiotoxicity. Eur Heart J Cardiovasc Imaging. 2017; 18:392–401.

57. Jung MH, Jung JI, Park SM, Youn HJ, Hong KS. A case of reversible but highly vulnerable adriamycin-induced cardiomyopathy: a multi-modality imaging approach. J Cardiovasc Imaging. 2019; 27:156–157.

58. Pelliccia A, Maron BJ, De Luca R, Di Paolo FM, Spataro A, Culasso F. Remodeling of left ventricular hypertrophy in elite athletes after long-term deconditioning. Circulation. 2002; 105:944–949.

59. Caselli S, Montesanti D, Autore C, et al. Patterns of left ventricular longitudinal strain and strain rate in Olympic athletes. J Am Soc Echocardiogr. 2015; 28:245–253.

60. Butz T, van Buuren F, Mellwig KP, et al. Two-dimensional strain analysis of the global and regional myocardial function for the differentiation of pathologic and physiologic left ventricular hypertrophy: a study in athletes and in patients with hypertrophic cardiomyopathy. Int J Cardiovasc Imaging. 2011; 27:91–100.

61. Park JH, Oh JK, Kim KH, et al. Left ventricular longitudinal strain and strain rate values according to sex and classifications of sports in the young university athletes who participated in the 2015 Gwangju Summer Universiade. JACC Cardiovasc Imaging. 2018; 11:1719–1721.

62. Haland TF, Almaas VM, Hasselberg NE, et al. Strain echocardiography is related to fibrosis and ventricular arrhythmias in hypertrophic cardiomyopathy. Eur Heart J Cardiovasc Imaging. 2016; 17:613–621.

63. Yiu KH, Atsma DE, Delgado V, et al. Myocardial structural alteration and systolic dysfunction in preclinical hypertrophic cardiomyopathy mutation carriers. PLoS One. 2012; 7:e36115.

64. Kobayashi T, Popovic Z, Bhonsale A, et al. Association between septal strain rate and histopathology in symptomatic hypertrophic cardiomyopathy patients undergoing septal myectomy. Am Heart J. 2013; 166:503–511.

65. Lee SP, Park JB, Kim HK, Kim YJ, Grogan M, Sohn DW. Contemporary imaging diagnosis of cardiac amyloidosis. J Cardiovasc Imaging. 2019; 27:1–10.

66. Liu D, Hu K, Niemann M, et al. Effect of combined systolic and diastolic functional parameter assessment for differentiation of cardiac amyloidosis from other causes of concentric left ventricular hypertrophy. Circ Cardiovasc Imaging. 2013; 6:1066–1072.

67. Senapati A, Sperry BW, Grodin JL, et al. Prognostic implication of relative regional strain ratio in cardiac amyloidosis. Heart. 2016; 102:748–754.

68. Buss SJ, Emami M, Mereles D, et al. Longitudinal left ventricular function for prediction of survival in systemic light-chain amyloidosis: incremental value compared with clinical and biochemical markers. J Am Coll Cardiol. 2012; 60:1067–1076.

69. Morris DA, Blaschke D, Canaan-Kühl S, et al. Global cardiac alterations detected by speckle-tracking echocardiography in Fabry disease: left ventricular, right ventricular, and left atrial dysfunction are common and linked to worse symptomatic status. Int J Cardiovasc Imaging. 2015; 31:301–313.

70. Lee JH, Park JH. Strain analysis of the right ventricle using two-dimensional echocardiography. J Cardiovasc Imaging. 2018; 26:111–124.

71. Park SJ, Park JH, Lee HS, et al. Impaired RV global longitudinal strain is associated with poor long-term clinical outcomes in patients with acute inferior STEMI. JACC Cardiovasc Imaging. 2015; 8:161–169.

72. Zornoff LA, Skali H, Pfeffer MA, et al. Right ventricular dysfunction and risk of heart failure and mortality after myocardial infarction. J Am Coll Cardiol. 2002; 39:1450–1455.

73. Jamal F, Bergerot C, Argaud L, Loufouat J, Ovize M. Longitudinal strain quantitates regional right ventricular contractile function. Am J Physiol Heart Circ Physiol. 2003; 285:H2842–7.

74. Lu KJ, Chen JX, Profitis K, et al. Right ventricular global longitudinal strain is an independent predictor of right ventricular function: a multimodality study of cardiac magnetic resonance imaging, real time three-dimensional echocardiography and speckle tracking echocardiography. Echocardiography. 2015; 32:966–974.

75. Wang J, Prakasa K, Bomma C, et al. Comparison of novel echocardiographic parameters of right ventricular function with ejection fraction by cardiac magnetic resonance. J Am Soc Echocardiogr. 2007; 20:1058–1064.

76. Vizzardi E, Bonadei I, Sciatti E, et al. Quantitative analysis of right ventricular (RV) function with echocardiography in chronic heart failure with no or mild RV dysfunction: comparison with cardiac magnetic resonance imaging. J Ultrasound Med. 2015; 34:247–255.

77. Freed BH, Tsang W, Bhave NM, et al. Right ventricular strain in pulmonary arterial hypertension: a 2D echocardiography and cardiac magnetic resonance study. Echocardiography. 2015; 32:257–263.

78. Park JH, Negishi K, Kwon DH, Popovic ZB, Grimm RA, Marwick TH. Validation of global longitudinal strain and strain rate as reliable markers of right ventricular dysfunction: comparison with cardiac magnetic resonance and outcome. J Cardiovasc Ultrasound. 2014; 22:113–120.

79. Focardi M, Cameli M, Carbone SF, et al. Traditional and innovative echocardiographic parameters for the analysis of right ventricular performance in comparison with cardiac magnetic resonance. Eur Heart J Cardiovasc Imaging. 2015; 16:47–52.

80. Lemarié J, Huttin O, Girerd N, et al. Usefulness of speckle-tracking imaging for right ventricular assessment after acute myocardial infarction: a magnetic resonance imaging/echocardiographic comparison within the relation between aldosterone and cardiac remodeling after myocardial infarction study. J Am Soc Echocardiogr. 2015; 28:818–827.e4.

81. Park JH, Kusunose K, Kwon DH, et al. Relationship between right ventricular longitudinal strain, invasive hemodynamics, and functional assessment in pulmonary arterial hypertension. Korean Circ J. 2015; 45:398–407.

82. Muraru D, Onciul S, Peluso D, et al. Sex- and method-specific reference values for right ventricular strain by 2-dimensional speckle-tracking echocardiography. Circ Cardiovasc Imaging. 2016; 9:e003866.

83. Park JH, Choi JO, Park SW, et al. Normal references of right ventricular strain values by two-dimensional strain echocardiography according to the age and gender. Int J Cardiovasc Imaging. 2018; 34:177–183.

84. Rimbaş RC, Mihăilă S, Enescu OA, Vinereanu D. A new comprehensive 12-segment approach to right ventricular systolic and diastolic functions by 2D speckle tracking echocardiography in healthy individuals. Echocardiography. 2016; 33:1866–1873.

85. Meris A, Faletra F, Conca C, et al. Timing and magnitude of regional right ventricular function: a speckle tracking-derived strain study of normal subjects and patients with right ventricular dysfunction. J Am Soc Echocardiogr. 2010; 23:823–831.

86. Fine NM, Shah AA, Han IY, et al. Left and right ventricular strain and strain rate measurement in normal adults using velocity vector imaging: an assessment of reference values and intersystem agreement. Int J Cardiovasc Imaging. 2013; 29:571–580.

87. Fine NM, Chen L, Bastiansen PM, et al. Reference values for right ventricular strain in patients without cardiopulmonary disease: a prospective evaluation and meta-analysis. Echocardiography. 2015; 32:787–796.

88. Seo HS, Lee H. Assessment of right ventricular function in pulmonary hypertension with multimodality imaging. J Cardiovasc Imaging. 2018; 26:189–200.

89. Ikeda S, Tsuneto A, Kojima S, et al. Longitudinal strain of right ventricular free wall by 2-dimensional speckle-tracking echocardiography is useful for detecting pulmonary hypertension. Life Sci. 2014; 111:12–17.

90. Fukuda Y, Tanaka H, Sugiyama D, et al. Utility of right ventricular free wall speckle-tracking strain for evaluation of right ventricular performance in patients with pulmonary hypertension. J Am Soc Echocardiogr. 2011; 24:1101–1108.

91. Motoji Y, Tanaka H, Fukuda Y, et al. Efficacy of right ventricular free-wall longitudinal speckle-tracking strain for predicting long-term outcome in patients with pulmonary hypertension. Circ J. 2013; 77:756–763.

92. Fine NM, Chen L, Bastiansen PM, et al. Outcome prediction by quantitative right ventricular function assessment in 575 subjects evaluated for pulmonary hypertension. Circ Cardiovasc Imaging. 2013; 6:711–721.

93. D'Andrea A, Stanziola A, D'Alto M, et al. Right ventricular strain: an independent predictor of survival in idiopathic pulmonary fibrosis. Int J Cardiol. 2016; 222:908–910.

94. Mukherjee M, Chung SE, Ton VK, et al. Unique abnormalities in right ventricular longitudinal strain in systemic sclerosis patients. Circ Cardiovasc Imaging. 2016; 9:e003792.

95. Sugiura E, Dohi K, Onishi K, et al. Reversible right ventricular regional non-uniformity quantified by speckle-tracking strain imaging in patients with acute pulmonary thromboembolism. J Am Soc Echocardiogr. 2009; 22:1353–1359.

96. Lee JH, Park JH, Park KI, et al. A comparison of different techniques of two-dimensional speckle-tracking strain measurements of right ventricular systolic function in patients with acute pulmonary embolism. J Cardiovasc Ultrasound. 2014; 22:65–71.

97. Lee K, Kwon O, Lee EJ, et al. Prognostic value of echocardiographic parameters for right ventricular function in patients with acute non-massive pulmonary embolism. Heart Vessels. 2019; 34:1187–1195.

98. Vitarelli A, Barillà F, Capotosto L, et al. Right ventricular function in acute pulmonary embolism: a combined assessment by three-dimensional and speckle-tracking echocardiography. J Am Soc Echocardiogr. 2014; 27:329–338.

99. Holman WL, Kormos RL, Naftel DC, et al. Predictors of death and transplant in patients with a mechanical circulatory support device: a multi-institutional study. J Heart Lung Transplant. 2009; 28:44–50.

100. Argiriou M, Kolokotron SM, Sakellaridis T, et al. Right heart failure post left ventricular assist device implantation. J Thorac Dis. 2014; 6:Suppl 1. S52–S59.

101. Grant AD, Smedira NG, Starling RC, Marwick TH. Independent and incremental role of quantitative right ventricular evaluation for the prediction of right ventricular failure after left ventricular assist device implantation. J Am Coll Cardiol. 2012; 60:521–528.

102. Cameli M, Lisi M, Righini FM, et al. Right ventricular longitudinal strain correlates well with right ventricular stroke work index in patients with advanced heart failure referred for heart transplantation. J Card Fail. 2012; 18:208–215.

103. Lisi M, Cameli M, Righini FM, et al. RV longitudinal deformation correlates with myocardial fibrosis in patients with end-stage heart failure. JACC Cardiovasc Imaging. 2015; 8:514–522.

104. Morris DA, Krisper M, Nakatani S, et al. Normal range and usefulness of right ventricular systolic strain to detect subtle right ventricular systolic abnormalities in patients with heart failure: a multicentre study. Eur Heart J Cardiovasc Imaging. 2017; 18:212–223.

105. Park JH, Park JJ, Park JB, Cho GY. Prognostic value of biventricular strain in risk stratifying in patients with acute heart failure. J Am Heart Assoc. 2018; 7:e009331.

106. Teske AJ, Cox MG, Te Riele AS, et al. Early detection of regional functional abnormalities in asymptomatic ARVD/C gene carriers. J Am Soc Echocardiogr. 2012; 25:997–1006.

107. Aneq MA, Engvall J, Brudin L, Nylander E. Evaluation of right and left ventricular function using speckle tracking echocardiography in patients with arrhythmogenic right ventricular cardiomyopathy and their first degree relatives. Cardiovasc Ultrasound. 2012; 10:37.

108. Vitarelli A, Cortes Morichetti M, Capotosto L, et al. Utility of strain echocardiography at rest and after stress testing in arrhythmogenic right ventricular dysplasia. Am J Cardiol. 2013; 111:1344–1350.

109. D'Andrea A, Caso P, Bossone E, et al. Right ventricular myocardial involvement in either physiological or pathological left ventricular hypertrophy: an ultrasound speckle-tracking two-dimensional strain analysis. Eur J Echocardiogr. 2010; 11:492–500.

110. D'Andrea A, Limongelli G, Baldini L, et al. Exercise speckle-tracking strain imaging demonstrates impaired right ventricular contractile reserve in hypertrophic cardiomyopathy. Int J Cardiol. 2017; 227:209–216.

111. Okamatsu K, Takeuchi M, Nakai H, et al. Effects of aging on left atrial function assessed by two-dimensional speckle tracking echocardiography. J Am Soc Echocardiogr. 2009; 22:70–75.

112. Pathan F, D'Elia N, Nolan MT, Marwick TH, Negishi K. Normal ranges of left atrial strain by speckle-tracking echocardiography: a systematic review and meta-analysis. J Am Soc Echocardiogr. 2017; 30:59–70.e8.

113. Donal E, Lip GY, Galderisi M, et al. EACVI/EHRA expert consensus document on the role of multi-modality imaging for the evaluation of patients with atrial fibrillation. Eur Heart J Cardiovasc Imaging. 2016; 17:355–383.

114. Schneider C, Malisius R, Krause K, et al. Strain rate imaging for functional quantification of the left atrium: atrial deformation predicts the maintenance of sinus rhythm after catheter ablation of atrial fibrillation. Eur Heart J. 2008; 29:1397–1409.

115. Providência R, Trigo J, Paiva L, Barra S. The role of echocardiography in thromboembolic risk assessment of patients with nonvalvular atrial fibrillation. J Am Soc Echocardiogr. 2013; 26:801–812.

116. Kojima T, Kawasaki M, Tanaka R, et al. Left atrial global and regional function in patients with paroxysmal atrial fibrillation has already been impaired before enlargement of left atrium: velocity vector imaging echocardiography study. Eur Heart J Cardiovasc Imaging. 2012; 13:227–234.

117. Yoon YE, Oh IY, Kim SA, et al. Echocardiographic predictors of progression to persistent or permanent atrial fibrillation in patients with paroxysmal atrial fibrillation (E6P study). J Am Soc Echocardiogr. 2015; 28:709–717.

118. Obokata M, Negishi K, Kurosawa K, et al. Left atrial strain provides incremental value for embolism risk stratification over CHA₂DS₂-VASc score and indicates prognostic impact in patients with atrial fibrillation. J Am Soc Echocardiogr. 2014; 27:709–716.e4.

119. Aung SM, Güler A, Güler Y, Huraibat A, Karabay CY, Akdemir I. Left atrial strain in heart failure with preserved ejection fraction. Herz. 2017; 42:194–199.

120. Santos AB, Roca GQ, Claggett B, et al. Prognostic relevance of left atrial dysfunction in heart failure with preserved ejection fraction. Circ Heart Fail. 2016; 9:e002763.

121. Ersbøll M, Andersen MJ, Valeur N, et al. The prognostic value of left atrial peak reservoir strain in acute myocardial infarction is dependent on left ventricular longitudinal function and left atrial size. Circ Cardiovasc Imaging. 2013; 6:26–33.

122. Debonnaire P, Leong DP, Witkowski TG, et al. Left atrial function by two-dimensional speckle-tracking echocardiography in patients with severe organic mitral regurgitation: association with guidelines-based surgical indication and postoperative (long-term) survival. J Am Soc Echocardiogr. 2013; 26:1053–1062.

123. Yang LT, Liu YW, Shih JY, et al. Predictive value of left atrial deformation on prognosis in severe primary mitral regurgitation. J Am Soc Echocardiogr. 2015; 28:1309–1317.e4.

124. Galli E, Fournet M, Chabanne C, et al. Prognostic value of left atrial reservoir function in patients with severe aortic stenosis: a 2D speckle-tracking echocardiographic study. Eur Heart J Cardiovasc Imaging. 2016; 17:533–541.

TOOLS

ORCID iDs: Jae-Hyeong Park
https://orcid.org/0000-0001-7035-286X
Similar articles