Heart Fail Rev (2015) 20:601–612 DOI 10.1007/s10741-015-9492-9

Review and status report of pediatric left ventricular systolic strain and strain rate nomograms Massimiliano Cantinotti1 • Shelby Kutty3 • Raffaele Giordano1 • Nadia Assanta1 Bruno Murzi1 • Maura Crocetti1 • Marco Marotta1 • Giorgio Iervasi2

•

Published online: 24 May 2015 Ó Springer Science+Business Media New York 2015

Abstract Interest in strain (e) and strain rate (SR) for the assessment of pediatric left ventricular (LV) myocardial function has increased. However, the strengths and limitations of published pediatric nomograms have not been critically evaluated. A literature search was conducted accessing the National Library of Medicine using the keywords myocardial velocity, strain, strain rate, pediatric, reference values, and nomograms. Adding the following keywords, the results were further refined: neonates, infants, adolescents, range/intervals, and speckle tracking. Ten published studies evaluating myocardial velocities, e, or SR nomograms were analyzed. Sample sizes were limited in most of these studies, particularly in terms of neonates. Heterogeneous methods—tissue Doppler imaging, two- and three-dimensional speckle tracking—were used to perform and normalize measurements. Although most studies adjusted measurements for age, classification by specific age subgroups varied. Few studies addressed the relationships of e and SR measurements to body size and heart rate. Data have been generally expressed by mean values and standard deviations; Z scores and percentiles that are commonly employed for pediatric echocardiographic quantification have been never used. Reference values for e and SR were found to be reproducible in older children; however, they varied significantly in neonates and & Raffaele Giordano [email protected]; [email protected] 1

Fondazione G. Monasterio CNR-Regione Toscana, Ospedale del Cuore, via Aurelia Sud, 54100 Massa, Pisa, Italy

2

Institute of Clinical Physiology, Pisa, Italy

3

College of Medicine, Children’s Hospital and Medical Center, University of Nebraska Medical Center, Omaha, NE, USA

infants. Pediatric nomograms for LV e and SR are limited by (a) small sample sizes, (b) inconsistent methodology used for derivation and normalization, and (c) scarcity of neonatal data. Some of the studies demonstrate reproducible patterns for systolic deformation in older children. There is need for comprehensive nomograms of myocardial e and SR involving a large population of normal children obtained using standardized methodology. Keywords strain

Echocardiography
Children
Myocardial

Abbreviations A Apical AFW Apical free wall AS Apical septum AL Apical lateral B Basal BS Basal septum BFW Basal free wall BL Basal lateral BI Basal inferior BSA Body surface area CHD Congenital heart disease e Strain GCS Global circumferential strain GSL Global longitudinal peak systolic strain GRS Global radial strain LV Left ventricle LS Longitudinal strain M Mid MS Mid-septum ML Mid-lateral MFW Middle free wall RV Right ventricle

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S SR syst TDI 2DSTE

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Septal Strain rate Systolic Tissue Doppler imaging Two-dimensional speckle tracking echocardiography

Introduction The use of myocardial strain and strain rate for the assessment of global and regional myocardial function is gaining consensus [1–21]. Strain (e) is a dimensionless measure of myocardial deformation, while strain rate (SR) represents the rate of change in strain with respect to time [23, 24]. Data regarding the application of e and SR in adult cardiology, as early indicators of heart failure, have accumulated in recent years [23, 24]. Two-dimensional (2D) speckle tracking-derived strain has been validated for the LV in vitro and in vivo over a range of physiological conditions with sonomicrometry [24, 25] and magnetic resonance imaging tagging [26]. Novel clinical applications of this technique for quantification of left ventricle (LV) [25] and right ventricle (RV) [25] mechanics and function are currently being explored. Strain is influenced by weight, blood pressure, and heart rate, accounting to approximately 16 % of variance. In addition, significant segmental variation of regional strain has been reported necessitating the use of site-specific normal ranges [27]. Recently, three-dimensional (3D) strain imaging has been introduced and applied for the estimation of LV regional circumferential, longitudinal, and radial strain components and has shown reasonable correlation with sonomicrometry [28]. Determination of radial strain using a 3D speckle tracking system from a pyramidal 3D dataset has been successfully used to quantify 3D LV dyssynchrony [29]. However, early results comparing 2D and 3D speckle tracking in the assessment of longitudinal, circumferential, and radial strain of the LV have shown discordance in the strain values obtained [30] and suboptimal correlation, suggesting that the two techniques are not interchangeable [31]. A strain standardization Task Force initiated by the American Society of Echocardiography and the European Association of Cardiovascular Imaging formed an academia–industry consortium and has recently published a consensus document on standard nomenclature for clinical parameters evaluated with speckle tracking echocardiography (2DSTE). This is one of the first steps in reducing inter-vendor differences and ambiguities in the strain algorithms [25]. During the last few years, various echocardiographic techniques for the noninvasive evaluation of LV e and SR have been evaluated in children with congenital and

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acquired heart disease. These include tissue Doppler imaging (TDI), 2DSTE and three-dimensional speckle tracking (3DSTE) [1–17]. In children, as any other echocardiographic parameter, LV e and SR need to be normalized for age and the somatic growth [32]; thus, normative data are required. Thus different pediatric centers have published nomograms for LV e and SR by 2DSTE [3, 6–8, 10] DTI [11], and more recently, three-dimensional echo [4, 9]. The aims of this study were to review the published pediatric nomograms for left ventricular systolic e/SR measures and to evaluate their strengths and weaknesses.

Search strategy Publications were identified from a systematic search in the National Library of Medicine (PubMed access to MEDLINE citations; http://www.ncbi.nlm.nih.gov/PubMed/) conducted in December 2014. The search strategy included a combination of Medical Subject Headings and free text terms for the key concepts, starting from myocardial velocity, strain, strain rate, pediatric, reference values, and nomograms. Adding the following keywords further refined the search: neonates, infants, adolescents, range/intervals, and speckle tracking. In addition, we identified other potentially relevant publications using a manual search of references from all eligible studies and review articles, as well as from the Science Citation Index Expanded on the Web of Science. Two reviewers assessed all identified reports independently, and a consensus was reached for inclusion in the present study. Titles and abstracts of all articles identified by the search strategy were evaluated and excluded if (1) the studies included populations other than normal subjects or combined adults with children (2 studies excluded), and (2) the reports were written in languages other than English (2 studies excluded).

Search results Fourteen publications were identified in the search for inclusion. Of these, 4 were excluded on the basis of the criteria listed above, yielding 10 publications for analysis.

General methodological limitations A standardized methodology based on international consensus to measure e and SR in the pediatric population is not currently available. Hence, measurements are performed using varied echocardiographic views comprising different myocardial segments and using various methodologies

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including tissue Doppler imaging [11], two-dimensional speckle tracking [3, 6–8, 10], and more recently, three-dimensional speckle tracking [4, 9]. As shown in Table 1, reproducibility of measurements was poor for most parameters, which may decrease usefulness in clinical practice. Echocardiographic measurements of cardiovascular structures must be adjusted for body size and age for comparisons with those from a healthy population [22–25]. Normalization of LV e and SR generally involved age [3, 4, 7, 8, 10] alone. There was only one study that normalized to heart rate (Tables 2, 3), and none considered parameters such as body surface area (BSA), and weight. Despite this, correlations of SR with weight, BSA [7, 8, 10], heart rate [7, 8, 10, 11], and indices of LV cardiac growth [4, 10] have been demonstrated. Data are generally expressed as means [3–5, 7, 8, 10–12], while percentiles and z scores that are commonly employed for normalization in pediatric echocardiography [18–25] were not adopted. Data in neonates and infants were limited [3, 4, 7, 8, 10, 12] with sample size generally limited to\60 subjects. Possible confounders such as gender [7, 8, 11] and race were rarely evaluated.

Techniques: TDI, two- and three-dimensional speckle tracking Over the years, various echocardiographic methodologies have been proposed for the evaluation of LV e and SR [1– 17]. Tissue Doppler imaging (DTI) was initially adopted [11, 12]; however, this technique presents limitations of being unidimensional, angle dependent and relatively load dependent [10]. Two-dimensional speckle tracking echocardiography (2DSTE) [3, 7, 8, 10] allows for automated calculation of myocardial deformation from continuous frame-by-frame tracking and motion analysis of speckles within the B-mode images of myocardium [10]. Reliability of 2DSTE has been validated with tagged cardiac magnetic resonance imaging and sonomicrometry both in adults [17, 18] and in pediatric populations [7, 9]. The biggest advantage of 2DSTE over TDI is its angle independence. Furthermore 2DSTE is less influenced by artifacts and more reproducible and allows for semi-automated calculation. 2DSTE, however, presents a few disadvantages. These include lower frame rates and lower spatial resolution compared to TDI, the need for excellent image quality for adequate tracking, and reduced lateral resolution compared to the axial resolution [4, 7, 9, 17, 18]. Movement of speckles outside the imaging plane results in suboptimal tracking on 2DSTE. Three-dimensional speckle tracking echocardiography may overcome some of these difficulties, allowing for a more complete analysis in all three spatial dimensions [4]. Three-dimensional speckle tracking echocardiography has also been validated both in

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adults [19, 20] and in children [4], and pediatric nomograms have recently been published (Table 4). Maturational changes in systolic deformation indices Various authors have demonstrated maturational changes in left ventricular systolic deformations indices during growth (Table 2). Marcus et al. [8] in a study that included subjects from birth to 40 years of age found differences in peak LV e among age groups even after correction for heart rate. The peak systolic strain increased up to 10 years of age in all three principal directions of contraction and remained stable thereafter [8]. Lorch et al. [10] found weak correlations between longitudinal e with age. On the other hand, longitudinal SR changed with age, being highest in infancy and decreased thereafter until 10 years of age [10]. Others have noted little differences in systolic deformation indices between age groups [3, 4]. Zhang et al. [4] found significant but small differences between age groups in longitudinal and circumferential e, but not in radial e. Stronger correlations between peak systolic strain and age emerged using second-order polynomial quadratic regression [4, 7, 8]. Marcus et al. [7] found good quadratic correlation with age and e indices. Accordingly, strain values were lowest in the younger and older groups and highest in teens, whereas another study showed a weaker correlation [4]. Other factors affecting systolic deformation There are anthropometric and hemodynamic variables related to maturation, which potentially may have an impact on LV deformation [7, 8, 10, 11]. Various authors have demonstrated the influence of heart rate on deformation, [7, 8, 10, 11], especially in early infancy [32–35]. Boettler and colleagues presented data according to heart rate intervals, while others employed heart rate correction methods (Table 3) [8]. SR did not show differences with heart rate, while e showed significant change [11]. Correlations of systolic deformation indices with other echocardiographic parameters have been tested. Zhang and colleagues demonstrated how LV end-diastolic volume, LV end-diastolic diameter, and right ventricular diastolic mid-cavity diameter were positively correlated with global circumferential strain evaluated by three-dimensional speckle tracking [4]. On the other hand, LV end-diastolic diameter [4], right ventricular diastolic mid-cavity diameter, and LV end-diastolic mass correlated with radial e [4]. Lastly left ventricular ejection fraction was significantly associated with global longitudinal e (1 % increase in ejection fraction corresponded to 0.067 % decrease in global longitudinal e) [4].

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123

Vivid 7 GE (GE Vingmed Ultrasound As, Horten, Norway)

Vivid 7 GE (GE Vingmed Ultrasound As, Horten, Norway)

Acuson Sequoia, Siemens Medical, Mountain View, CA)

Vivid 7 GE (GE Vingmed Ultrasound As, Horten, Norway)

Vivid 7 GE (GE Vingmed Ultrasound As, Horten, Norway)

IE33 Philip Medical System Andover, MA

Klitsic [3]

Marcus [7, 8]

Lorch [10]

Boettler [11]

Pena [12]

Zhang [4]

Tomtec Imaging System Germany

Echo-PAC GE Medical system

Speqle, Ku, Leuven, Belgium

Siemens Medical

9.19

12.7 ± 5.4 %

GRSM 0.23 GLS

CV

13.21

14.78

4.52

3.61

S 0.3 % SR 2.2 %

PSA PW Syst S 0.3 % SR 2 %

GCS 17.0 ± 16.2 GRS 13.7 ± 13.1 GS 7.0 ± 6.1

GCS 10.1 ± 8.5 GRS 9.8 ± 8.6 GS 5.0 ± 4.3

GLS 6.9 ± 6.1

GLS 6.2 ± 4.4

S 1.1 % SR 0,8 % PSA PW Syst

S 0.5 % SR 0.6 %

3DSE

ULA

13.78

13.22

4.3

4.54

2.95

Apical 2 ch Inferior Syst

S7% SR 7 %

GLS 2.8 ± 1.7 %

GRSM 0.28

GRSP 0.39

GCSM 0.09

GCSP 0.46

LLA 2.89

300 ± 50 frames/s

8.52

Bias GLS 0.04

Parasternal/apical views

8.73

8.91

7.89

7.22

7.15

GCS 0.67

Apical 2 ch Inferior Syst

S 14 % SR 7 %

13

GLS 0.79 GRS 0.72

TDI

FR [ 250 frames/s

TDI Sector angle 30°

FR 30 frames/s

Sector angle not reported

2DSTE

9.36

3.14

2.74

3.19

3.51

GCSP 0.39

FR 70–90 Hz

2.95

0.01

2.89

GLS 0.03

Sector angle 30–60°

10 24

ULA

GRSP 0.32

LLA

GCSM 0.02

4.5–6.9

GCS 0.67 Bias

2DSTE

GRS 3.8

FR 60–80 frames/s Echo-PAC GE Medical system

4.1–4.1 27.9–20.3

GLS 0.0

Sector angle not reported

GE Medical system

ICC

ULA

Bias

CV

Infra-observer variability

Inter-observer variability

2DSTE

Method

Echo-PAC

Off-line analysis

CV

12.83

14.01

11.04

9.44

7.15

2DSTE two-dimensional speckle tracking echocardiography, FR frame rate, LLA 95 % lower limit of agreement, GCS global circumferential strain, GCSM global circumferential peak systolic strain at the level of the mitral valve, GCSP global circumferential peak systolic strain at the level of the papillary muscle, GLS global longitudinal peak systolic strain, GRS global radial strain, GRSM global radial peak systolic strain at the mitral valve, GRSP global radial peak systolic strain at the level of the papillary muscle, ms millisecond, L PSA para-sternal short axis, PW posterior wall, TDI tissue Doppler imaging, ULA 95 % upper limit of agreement °Bland–Altman analysis

Vendor

Author

Table 1 Inter and infra-observer variability in major pediatric systolic deformation indices nomograms

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Table 2 Major nomograms for two-dimensional speckle tracking (2DSTE) left ventricular systolic strain and time to peak strain measures Population

Longitudinal strain

Circumferential strain

Radial peak systolic strain

PM

MV

PM

MV

Marcus K 2011 USA [7] Septum 0 years

B -17 ± 2.6

AS -25.5 ± 5.7

AS -25.1 ± 3.8

AS 43.3 ± 10.7

AS 39.6 ± 4.2

n 24 (13 M)

M -18.2 ± 2.7

A -18.2 ± 1.6

A -16.5 ± 4.2

A 50.0 ± 14.8

A 46.7 ± 5.6

0.3 ± 0.3 years

A -20.4 ± 1.9

L -13.8 ± 2.3

L -11.5 ± 3.6

L 58.5 ± 12.0

L 55.5 ± 6.1

Lateral wall A -19.6 ± 1.5

P -10.7 ± 4.0

P -11.4 ± 4.0

P 63.2 ± 11.6

P 60.5 ± 6.0

M -16.2 ± 1.1

I -17 ± 6.5

I -16 ± 7.6

I 56.6 ± 12.6

I 56.3 ± 7.0

B -15.8 ± 1.3

S -26.5 ± 6.0

S -24.5 ± 5.2

S 40.1 ± 7.8

S 41.1 ± 5.0

GLS 18.3 ± 1.9

GCS -18.6 ± 3.3

GCS -17.5 ± 2.5

GRS 52.0 ± 9.9

GRS 49.9 ± 4.3

P5 GLS -14.5 P95 GLS -22.1

P5 GCS -12 P95 GCS -25.2

P5 GCS -12.5 P95 GCS -22.5

P5 GRS 32.2 95th p. GRS 71.8

P5 GRS 41.3 P95 GRS 58.5

Septum 1–4 years

B -19.6 ± 1.5

AS -26.8 ± 3.6

AS -27.1 ± 3.9

AS 44.9 ± 5.8

AS 41.6 ± 5.1

n 34 (19 M)

M -20.9 ± 1.3

A -21.3 ± 4.1

A -20.3 ± 4.4

A 51.9 ± 7.8

A 48.3 ± 7.0

2.9 ± 1.0 years

A -22.7 ± 1.7

L -18.1 ± 2.0

L -15.4 ± 3.6

L 58.8 ± 8.6

L 54.1 ± 8.2

Lateral wall A -22.5 ± 1.7

P -16.0 ± 1.9

P -12.4 ± 2.7

P 61.1 ± 8.9

P 58.5 ± 7.7

M -20.2 ± 1.6

I -20.4 ± 2.0

I -17.8 ± 3.4

I 58.5 ± 9.0

I 54.7 ± 6.9

B -19.4 ± 1.5

S -25.3 ± 3.6

S -24.9 ± 4.7

S 45.9 ± 6.5

S 42.9 ± 5.3

GLS -20.7 ± 1.3

GCS -21.3 ± 2.0

GCS -19.7 ± 2.0

GRS 53.5 ± 6.7

GRS 50.0 ± 5.7

P5 GLS -18.1

P5 GCS -17.3

P5 GCS -15.7

P5 GRS 40.1

P5 GRS 38.6

P95 GLS -23.3

P 95 GCS - 25.3

P95 GCS -23.7

P95 GRS 66.9

P95 GRS 61.4

Septum 5–9 years

B -20.1 ± 1.8

AS -26.3 ± 2.3

AS -25.3 ± 3.8

AS 44.5 ± 7.2

AS 43.3 ± 5.1

n 36 (25 M) 7.2 ± 1.2 years

M -21.1 ± 1.4 A -22.6 ± 1.5

A -24.4 ± 2.2 L -20.5 ± 1.5

A -21.1 ± 2.1 L -17.4 ± 2.9

A 52.8 ± 8.5 L 59.4 ± 7.8

A 49.2 ± 5.1 L 56.6 ± 5.2

P -19.4 ± 1.1

P -15.3 ± 2.9

P 64.8 ± 7.1

P 61.2 ± 7.4

Lateral wall A -22.6 ± 1.5 M -20.1 ± 1.8

I -22.7 ± 2.0

I -20.1 ± 2.1

I 61.2 ± 6.1

I 57.5 ± 5.4

B -19.3 ± 1.8

S -27.2 ± 2.6

S -26.4 ± 3.4

S 46.6 ± 5.4

S 45.8 ± 4.9

GLS -21 ± 1.3

GCS -23.4 ± 1.7

GCS -20.9 ± 2.0

GRS 54.9 ± 5.5

GRS 52.3 ± 4.5

P5 GLS -18.4

P5 GCS -20

P5 GCS -16.9

P5 GRS 43.9

P5 GRS 43.3

P95 GLS -23.6

P95 GCS -26.8

P95 GSC -24.9

P 95 GRS 65.9

P95 GRS 61.3

Septum 10-14 years

B -20.0 ± 1.7

AS -26.1 ± 3.0

A S -24.3 ± 3.3

AS 46.5 ± 6.1

AS 46.8 ± 5.3

n 29 (16 M)

M -21.5 ± 1.6

A -24.1 ± 2.0

A -21.8 ± 2.0

A 57.1 ± 5.7

A 52.7 ± 5.8

12.8 ± 1.6 years

A -23.8 ± 1.3

L -21.0 ± 1.7

L -19.2 ± 1.5

L 62.8 ± 5.8

L 58.6 ± 7.1

P -20.0 ± 1.4

P -18.2 ± 1.2

P 66.3 ± 5.5

P 62.2 ± 6.5

Lateral wall A -23.9 ± 1.7 M -21.7 ± 1.6

I -22.8 ± 1.7

I -20.7 ± 1.8

I 65.2 ± 6.5

I 59.0 ± 6.4

B -20.0 ± 1.2 GL S -21.8 ± 1.3

S -26.9 ± 2.8 GCS -23.5 ± 1.8

S -24.7 ± 2.3 GCS -21.5 ± 1.7

S 50.1 ± 5.9 GRS 58.0 ± 5.4

S 50.5 ± 5.6 GRS 54.9 ± 5.4

P5 GLS -19.2

P5 GCS -19.9

P5 GCS -18.1

P5 GRS 47.2

P 5 GRS 44.1

P 95 GLS -24.4

P 95 GCS -27.1

P 95 GCS -24.9

P 95 GRS 68.8

P95 GRS65.7

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Table 2 continued Population

Longitudinal strain

Circumferential strain

Radial peak systolic strain

PM

MV

PM

MV

Septum 15-19 years

B -20.4 ± 1.6

AS -27.5 ± 2.8

AS -24.0 ± 2.5

AS 48.7 ± 3.9

AS 49.9 ± 3.4

n 21 (9 M)

M -22.5 ± 1.4

A -22.9 ± 2.0

A -22.4 ± 1.9

A 55.9 ± 4.4

A 54.7 ± 3.2

17 ± 1.3 years

A -25.1 ± 1.2

L -21.1 ± 2.2

L -19.3 ± 2.4

L 61.2 ± 4.6

L 57.6 ± 4.0

Lateral wall A -25.0 ± 1.4

P -19.2 ± 2.5

P -17.7 ± 2.0

P 66.8 ± 4.1

P 63.0 ± 5.8

M -22.4 ± 1.7

I -22.4 ± 2.1

I -21.9 ± 2.7

I 64.3 ± 4.3

I 60.3 ± 5.2

B -20.5 ± 1.7

S -28.6 ± 2.5

S -26.0 ± 2.5

S 51.7 ± 5.3

S 51.1 ± 3.7

GLS -22.5 ± 1.3

GCS 23.6 ± 2.0

GCS -21.9 ± 2.1

GRS 58.1 ± 4.0

GRP 56.1 ± 3.8

P5 GLS -19.9

P5 GCS -19.6

P5 GCS -17.7

P5 GRS 50.1

P5 GRS 48.5

P 95 GLS -25.1

P 95 GCS -27.6

P 95 GCS -26.6

P 95 GRS 66.1

P95 GRS 63.7

Time to peak longitudinal strain

Time to peak circumferential strain

Time to peak radial strain

PM

MV

PM

MV

AS 317 ± 17

AS 338 ± 16

AS 332 ± 16

AS 372 ± 24

Marcus 2012 USA [8] 0 years

BS 362 ± 20

n 24 (M 13) 0.3 ± 0.3

1–4 years

MS 334 ± 18

A 332 ± 20

A 351 ± 20

A 343 ± 15

A 392 ± 25

AS 313 ± 16 AL 329 ± 16

L 368 ± 23 P 367 ± 24

L 385 ± 25 P 402 ± 26

L 379 ± 20 P 381 ± 19

L 419 ± 21 P 429 ± 30

ML 352 ± 16

I 337 ± 18

I 364 ± 20

I 353 ± 18

I 417 ± 22

BL 372 ± 19

S 316 ± 17

S 332 ± 20

S 325 ± 16

S 370 ± 21

GLS 341 ± 18

GCS 339 ± 18

GCS 362 ± 22

GRS 325 ± 18

GRS 400 ± 22

P5 GLS 305

P5 GCS 303

P5GCS S-CM 318

P5 GRS 316

P5GRS 356

P95 GLS 377

P95GCS375

P95GCS 406

P95 GRS 388

P95GRS 444

BS 391 ± 22

AS 376 ± 20

AS 361 ± 22

AS 372 ± 20

AS 401 ± 23

n 34 (M19) 2.9 ± 1.0

5–9 years

MS 360 ± 21

A 386 ± 22

A 375 ± 24

A 381 ± 22

A 409 ± 26

AS 342 ± 17

L 419 ± 26

L 415 ± 27

L 412 ± 23

L 449 ± 28

AL 358 ± 17

P 440 ± 27

P 423 ± 27

P 414 ± 22

P 457 ± 28

ML 384 ± 19

I 407 ± 23

I 400 ± 26

I 390 ± 20

I 447 ± 22

BL 401 ± 21

S 367 ± 21

S 353 ± 23

S 340 ± 21

S 399 ± 20

GLS 373 ± 19 P5 GLS 335

GCS 399 ± 23 P5 GCS 353

GCS 388 ± 25 P5 GCS 338

GT2P S-RP 384 ± 22 P5GT2P S-RP 340

GT2PS-RM 427 ± 24 P5GT2P S-RM 379

P95 GLS 411

P95 GCS 445

P95 GCS 438

P95T2P S-RP 428

P95GT2P S-RM 475

BS 424 ± 25

AS 384 ± 24

AS 377 ± 25

AS 381 ± 23

AS 420 ± 21

n 36 (M25) 7.2 ± 1.2

123

MS 390 ± 24

A 389 ± 25

A 391 ± 26

A 404 ± 24

A 431 ± 22

AS 368 ± 18

L 439 ± 28

L 436 ± 25

L 431 ± 25

L 479 ± 25

AL 382 ± 17

P 441 ± 28

P 442 ± 31

P 434 ± 24

P 488 ± 30

ML 400 ± 21

I 411 ± 25

I 428 ± 30

I 416 ± 25

I 455 ± 32 S 410 ± 22

BL 435 ± 23

S 366 ± 24

S 375 ± 26

S 355 ± 22

GLS400 ± 20

GCS 405 ± 25

GCS 408 ± 27

GRS 404 ± 24

GRS 447 ± 27

P5 GLS 361

P5 GCS 355

P5 GCS 354

P5 GRS 356

P5 GRS 393

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Table 2 continued Time to peak longitudinal strain

10–14 years

Time to peak circumferential strain

Time to peak radial strain

PM

PM

MV

MV

P95 GLS 439

P95 GCS 455

P95 GCS 462

P95 GRS 452

P95GRS 501

BS 425 ± 28

AS 379 ± 26

AS 381 ± 29

AS 380 ± 24

AS 418 ± 25

n 29 (M16) 12.8 ± 1.6

15–19 years

MS 392 ± 26

A 387 ± 27

A 400 ± 30

A 387 ± 23

A 426 ± 26

AS 368 ± 20

L 426 ± 29

L 442 ± 35

L 430 ± 27

L 473 ± 29

AL 380 ± 20

P 446 ± 28

P 449 ± 34

P 437 ± 23

P 493 ± 30

ML 413 ± 22

I 421 ± 27

I 443 ± 34

I 413 ± 23

I 464 ± 30

BL 439 ± 24

S 367 ± 28

S 372 ± 29

S 361 ± 24

S 414 ± 25

GLS 402 ± 23

GCS 404 ± 27

GCS 415 ± 30

GRS 401 ± 25

GRS 448 ± 28

P5 GLS 356

P5 GCS 350

P5 GCS 355

P5 GRS 351

P5 GRS 392

P95 GLS 448

P95 GCS 458

P95 GCS 417

P95 GRS 451

P95GRS 504

BS 433 ± 26

AS 366 ± 28

AS 377 ± 25

AS 370 ± 21

AS 412 ± 25

n 21 (M9) 17 ± 1.3 MS 400 ± 25

A 373 ± 28

A 390 ± 27

A 389 ± 25

A 423 ± 27

AS 370 ± 19

L 420 ± 26

L 440 ± 30

L 425 ± 27

L 460 ± 31

AL 392 ± 20

P 428 ± 31

P 447 ± 34

P 433 ± 26

P 488 ± 33

ML 417 ± 24

I 422 ± 29

I 438 ± 35

I 414 ± 24

I 474 ± 31

BL 445 ± 25

S 362 ± 27

S 365 ± 24

GRS 399 ± 25

GRS 443 ± 30

GLS 410 ± 23

GCS 395 ± 28

GCS 409 ± 32

P5GRS 349

P5 GRS 383

P5 GLS 364

P5 GCS 339

P5 GCS 345

P95 GRS 449

P95GRS 503

P95 GLS L 456

P95 GCS 451

P95 GCS 473

Klitsic L 2013 Netherlands° [3] n 183

6-Segment model

0–19 years

12-Segment model 18-Segments model Global strain

\1 years n 37 (M 17)

-20.3 ± 3.2 -20.8 ± 3.2

0.1 (0.1–0.3) years

-20.6 ± 3.1

1–4 years

-22.8 ± 2.4

n 35 (M 19)

-23.5 ± 1.4

3.2 (2.3–3.8) years

-23.6 ± 1.5

5–9 years

-21.9 ± 2.1

n 37 (M 20)

-23.3 ± 2.3

6.9 (6.2–8.2)

-23.1 ± 2.2

10–14 years

-20.5 ± 2.2

n 45 (M 34)

-21.8 ± 2.0

12.5 (11.1–13.8) y

-21.8 ± 2.1

15–19 years

-19.5 ± 1.7

n 18 (M8)

-21.0 ± 1.8

16 (15.9–16.9) years

-20.8 ± 1.8

-21.7 ± 4.7

40.5 ± 13.5

-22.1 ± 3.6

49.8 ± 13.7

-23.1 ± 2.7

55.0 ± 11.2

-22.8 ± 3.6

23.1 ± 2.7

-21.6 ± 1.3

21.6 – 1.3

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Heart Fail Rev (2015) 20:601–612

Table 2 continued Time to peak longitudinal strain

Time to peak circumferential strain

Time to peak radial strain

PM

PM

MV

MV

Lorch SM USA 2008 [10] Global strain 0–1 years

S -17.97 ± 7.02

n 37 (M 21)

L -18.51 ± 9.39

0.2 ± 0.28 y 1–5 years

S -17.99 ± 5.92

n 53 (M 29)

L -21.13 ± 8.44

3.7 ± 1.48 years 6–9 years

S -16.65 ± 6.29

n 66 (M 42)

L -18.31 ± 7.43

8.09 ± 1.10 years 10–13 years

S -18.80 ± 6.60

n 71 (M 37)

L -22.70 ± 8.19

11.69 ± 1.18 years 14–18 years

S -20.11 ± 7.31

n 57 (M 29)

L -22.70 ± 8.19

16.04 ± 1.19 years ° Multivariate regression analysis provided for time to peak A apical, AFW apical free wall, B basal, BS basal septum, BFW basal free wall, BL, basal lateral, BI, basal inferior, GCS global circumferential strain, GSL global strain longitudinal, GRS global radial strain, M mid, MS mid-septum, AS apical septum, AL apical lateral, ML mid-lateral, MFW middle free wall, S septal, L lateral

Marcus and colleagues noted how rate-corrected velocity of circumferential fiber shortening and LV ejection time corrected for heart rate were negatively correlated with circumferential and longitudinal e evaluated by 2DSTE [7]. No correlations were found for ejection fraction or endsystolic wall stress with deformation parameters [8]. Others have found that a 1-ms increase in LV ejection time corrected for heart rate corresponded to a decrease of 0.015 % in global longitudinal peak e and of 0.05 % in global peak systolic circumferential e [7]. Lorch et al. [10] demonstrated that z scores of LV end-systolic and end-diastolic volumes correlated with septal systolic e, while only end-diastolic volumes affected the lateral e. Left ventricular diastolic filling parameters (mitral A-wave and E/A ratio) also correlated with septal and lateral systolic e [10]. No correlations emerged between systolic deformation indices and QT duration [3, 7, 8], QRS duration, [3] or blood pressure values [7, 8]. Interestingly, no gender differences [7, 8, 11] for systolic strain parameters were noted. Regional differences in systolic deformation indices Multiple studies have found regional differences in systolic strain measurements at all ages [4, 7, 8, 12]. The time to peak systolic e was shorter at the base and in the mid-segments compared to the apex of the LV [1, 7, 8, 12]. This base-to-

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apex gradient has been observed on e measurements using different techniques [1, 7, 8, 12]. These data tend to confirm magnetic resonance imaging observations, while tissue Doppler studies did not show similar base–apex variations [8]. Marcus et al. [8] hypothesized that these variations may be related to torsional mechanisms. Lastly, compared to the septum and LV free wall, both e and SR were significantly higher in the RV [7, 8, 11, 12].

Discussion Interest in the use of myocardial e and SR for the assessment of regional and global LV function in children with congenital and acquired heart disease has increased over the past few years [1–17]. As for other functional and dimensional echocardiographic parameters [32–35], deformation indices in the pediatric age should be normalized according to age and body size. Over the last few years, several nomograms for LV e and SR in children have been published. Despite improved data quality in the recent studies [3, 4, 7, 8, 10–12], limitations persist in the available nomograms. First various echocardiographic techniques for the assessment of strain/strain rate have been employed over the years, from tissue Doppler imaging [11, 12] to two-dimensional speckle tracking [3, 7, 8, 10], and more recently, three-dimensional speckle tracking [4].

Heart Fail Rev (2015) 20:601–612

609

Table 3 Major pediatric nomograms for color tissue Doppler myocardial imaging (DTI) left and right ventricular systolic and diastolic strain and strain rate Author

Population

LS

Left ventricle

Septum

Right ventricle

HR

Syst SR

Syst strain

Syst SR

Syst strain

Syst SR

Syst strain

47 (36–61)

Basal Boettler P 2005 Germany [11]

1–17 years

60

2.71 (2.16–3.39)

30 (23–38)

2.59 (1.97–3.39)

28 (19–40)

3.63 (2.82–4.65)

n 129 (56 F)

90

2.91 (2.32–3.63)

26 (20–33)

2.94 (2.24–3.82)

25(17–35)

3.95 (3.09–5.05)

39 (30–51)

5.8 5.2 years

120

3.05 (2.44–3.81)

24 (18–30)

3.2 (2.44–4.16)

23 (16–33)

4.19 (3.27–5.36)

35 (26–45)

150

3.16 (2.52–3.95)

22 (17–28)

3.4 (2.59–4.45)

22 (15–31)

4.38 (3.41–5.61)

32 (23–42)

180

3.25 (2.59–4.07)

21 (16–27)

3.58 (2.72–4.69)

21 (14–30)

4.53 (3.51–5.81)

29 (22–39)

60

2.27 (1.83–2.81)

30 (25–37)

2.73 (2.11–3.53)

30 (23–39)

3.60 (2.77–4.66)

43 (32–56)

90

2.44 (1.97–3.00)

26 (21–32)

2.86 (2.21–3.68)

27 (21–36)

3.68 (2.83–4.75)

39 (29–51)

120

2.55 (2.07–3.14)

24 (19–30)

2.95 (2.28–3.80)

25 (19–33)

3.73 (2.87–4.83)

36 (27–48)

150

2.64 (2.14–3.26)

22 (18–28)

3.02 (2.33–3.89)

24 (18–32)

3.77 (2.90–4.89)

35 (26–46)

180

2.72 (2.19–3.36)

21 (17–26)

3.07 (2.37–3.97)

27 (17–31)

3.80 (2.91–4.94)

33 (24–45)

60

2.38 (1.89–2.98)

33 (26–41)

3.03 (2.07–4.39)

27 (19–36)

3.70 (2.86–4.79)

40 (30–53)

90

2.30 (1.83–2.89)

27 (21–34)

2.75 (1.89–3.97)

24 (17–32)

3.77 (2.92–4.86)

35 (26–47)

120

2.26 (1.79–2.83)

23 (18–30)

2.58 (1.76–3.73)

21 (15–30)

3.82 (2.95–4.93)

32 (24–43)

150

2.22 (1.76–2.80)

21 (16–27)

2.45 (1.67–3.57)

20 (14–28)

3.86 (2.97–4.99)

30 (22–41)

180

2.20 (1.73–2.77)

19 (14–25)

2.36 (1.59–3.46)

19 (13–26)

3.88 (2.98–5.04)

29 (21–39)

Mid

Apical

Author

Population

LS

Left ventricle

Septum

Right ventricle

E diast SR

E diast strain

E diast SR

E diast strain

E diast SR

E diast strain

38 (27–52)

Basal Boettler P 2005 Germany [11]

1–17 years

60

3.88 (3.08–4.87)

19 (12–28)

3.36 (1.76–6.22)

21 (13–31)

4.33 (3.32–5.63)

n 129 (56 F)

90

3.69 (2.93–4.62)

16 (9–23)

3.00 (1.57–5.52)

16 (9–25)

4.30 (3.30–5.58)

25 (17–36) 4.29

5.8 5.2 years

120

3.56 (2.83–4.47)

13 (7–21)

2.77 (1.43–5.14)

13 (6–21)

(3.28–5.57)

18 (11–28)

150

3.47 (2.75–4.36)

12 (6–19)

2.61 (1.33–4.90)

11 (5–18)

4.27 (3.26–5.57)

14 (7–22)

180

3.40 (2.68–4.29)

10 (5–17)

2.49 (1.25–4.73)

9 (3–17)

4.26 (3.24–5.57)

11 (4–18)

60

3.20 (2.45–4.15)

22 (16–30)

3.73 (2.51–5.46)

20 (12–30)

4.15 (3.13–5.47)

32 (21–45)

90

3.14 (2.41–4.06)

18 (13–25)

3.80 (2.58–5.54)

18 (10–27)

4.28 (3.23–5.62)

25 (16–37)

120

3.10 (2.38–4.02)

16 (10–22)

3.85 (2.61–5.62)

16 (9–25)

4.37 (3.30–5.75)

21 (16–32)

150

3.47 (2.35–3.99)

14 (9–20)

3.89 (2.62–5.70)

15 (8–24)

4.43 (3.34–5.85)

19 (11–29)

180

3.40 (2.33–3.97)

13 (8–19)

3.92 (2.63–5.76)

14 (7–23)

4.49 (3.37–5.94)

17 (9–27)

60

4.24 (3.00–5.95)

22 (13–32)

4.02 (2.54–6.29)

14 (6–23)

4.10 (2.60–6.36)

27 (17–40)

90

3.94 (2.79–5.52)

18 (10–27)

3.69 (2.33–5.75)

13 (5–22)

3.46 (2.19–5.37)

23 (14–35)

120

3.74 (2.64–5.25)

15 (8–24)

3.47 (2.18–5.43)

12 (5–21)

3.08 (1.94–4.82)

20 (12–32)

150

3.60 (2.53–5.07)

13 (7–22)

3.32 (2.07–5.23)

11 (4–20)

2.83 (1.76–4.45)

19 (10–30)

180

3.50 (2.45–4.94)

12 (6–20)

3.20 (1.98–5.08)

11 (4–19)

2.64 (1.62–4.19)

17 (9–28)

Mid

Apical

Pena JLB Brazil [12]

N 55 neonates (29 M) 20.14 ± 14 h

Apical 4 ch Systolic LV longitudinal function

Apical 2 ch Systolic LV longitudinal function

LV systolic radial function

Strain

SR

Strain

SR

Strain

SR

BI -25.86 ± 4.83

-1.89 ± 0.6

BI -25.11 ± 3.13

-1.81 ± 0.32

BP -49.72 ± 12.86

-2.98 ± 0.78

MI -24.85 ± 3.40

-1.82 ± 0.46

MI -25.37 ± 3.09

-1.84 ± 0.31

MP -55.72 ± 12.13

-2.86 ± 0.63

AI -24.23 ± 3.08

-1.66 ± 0.25

AI -25.41 ± 3.63

-1.90 ± 0.31

BA -24.46 ± 3.82

-1.83 ± 0.37

BA -25.81 ± 5.55

-1.89 ± 0.43

MA -24.36 ± 3.53

-1.67 ± 0.30

MA -2.25 ± 4.19

-1.71 ± 0.80

AA -24.40 ± 3.48

-1.66 ± 0.22

AA -24.61 ± 3.17

-1.58 ± 0.3

123

610

Heart Fail Rev (2015) 20:601–612

Table 3 continued

Pena JLB Brazil [12]

Pena JLB Brazil [12]

N 55 neonates (29 M) 20.14 ± 14 h

N 55 neonates (29 M) 20.14 ± 14 h

Apical 4 ch early diastolic LV longitudinal function

Apical 2 ch early diastolic LV longitudinal function

LV early diastolic radial function

Strain

SR

Strain

SR

Strain

SR

BI 17.43 ± 4.57

3.19 ± 1.57

BI 16.41 ± 3.46

3.00 ± 0.90

BP 36.98 ± 10.88

5.53 ± 1.70

MI 17.15 ± 7.31

2.86 ± 1.28

MI 16.78 ± 3.00

2.88 ± 0.99

MP 40.97 ± 9.31

6.23 ± 2.03

AI 16.05 ± 3.11

3.16 ± 1.30

AI 16.62 ± 2.98

3.33 ± 1.18

BA 16.81 ± 3.58

3.15 ± 1.53

BA 17.88 ± 4.44

3.36 ± 1.54

MA 16.98 ± 3.20

2.96 ± 1.19

MA 17.49 ± 4.24

3.38 ± 1.78

AA 17.16 ± 3.37

2.82 ± 1.14

AA 16.93 ± 3.35

2.94 ± 1.22

Apical 4 ch late diastolic LV longitudinal function

Apical 2 ch late diastolic LV longitudinal function

LV late diastolic radial function

Strain

Strain

SR

Strain

SR

SR

BI 7.70 ± 3.14

2.39 ± 0.9

BI 8.24 ± 2.76

2.16 ± 0.81

BP 11.48 ± 5.62

3.89 ± 1.63

MI 7.40 ± 2.17

2.10 ± 0.97

MI 7.62 ± 2.36

2.08 ± 0.93

MP 13.00 ± 5.33

3.78 ± 1.63

AI 7.21 ± 2.30

2.28 ± 1.24

AI 8.11 ± 2.38

2.42 ± 0.82

BA 7.15 ± 2.54

2.12 ± 1.29

BA 7.04 ± 3.00

2.42 ± 1.36

MA 7.34 ± 3.02

2.04 ± 1.09

MA 7.31 ± 4.17

2.2 ± 1.11

AA 7.14 ± 2.72

1.87 ± 0.79

AA 7.19 ± 2.39

2.30 ± 1.37

Systolic RV

Pena JLB Brazil [12]

N 55 neonates (29 M) 20.14 ± 14 h

Early diastolic RV

Late diastolic RV

Strain

SR

Strain

SR

Strain

SR

4chBFW -28.38 ± 4.90

-1.93 ± 0.52

4chBFW 20.43 ± 4.52

2.76 ± 0.77

4chBFW 8.35 ± 3.21

2.09 ± 0.85

4chMFW -33.20 ± 6.34

-1.91 ± 0.45

4ch MFW 22.61 ± 5.15

3.00 ± 1.00

4chMFW 10.72 ± 4.07

2.57 ± 0.99

4chAFW -31.95 ± 5.06

-2.13 ± 0.50

4chAFW 21.02 ± 4.01

3.74 ± 1.35

4chAFW 10.87 ± 3.42

3.33 ± 1.34

2ChBI -27.09 ± 3.90

-1.81 ± 0.40

2ChBI 19.00 ± 3.73

2.78 ± 1.14

2ChBI 8.12 ± 2.70 2

.13 ± 0.83

LS longitudinal strain, LV left ventricle, RV right ventricle, SR strain rate; syst systolic

Table 4 Pediatric nomograms for three-dimensional left ventricular strain measures Reference

Population

Global longitudinal strain

Global circumferential strain

Global radial strain

Global strain

Zhang et al. China [4]

\1

-17.31 ± 2.27

-16.87 ± 2.73

61.58 ± 18.82

-29.77 ± 4.45

-17.34 ± 2.56

-17.06 ± 3.25

60.28 ± 13.37

30.13 ± 3.47

-17 ± 3.43

59.49 ± 13.29

-30.24 ± 3.61

n 23 (M 13) 0.56 ± 0.23 years 1–5 n 83 (M 45) 2.7 ± 1.19 years 5–9

-17.56 ± 2.221

n 61 (M 33) 6.88 ± 1.16 years 9–13

-18.75 ± 1.72

-18.83 ± 3.32

64.65 ± 8.42

-31.52 ± 2.65

-16.64 ± 2.8

-16.26 ± 4.11

56.62 ± 14.89

-28.96 ± 4.53

n 36(M 17) 10.86 ± 1.23 years 13–18 n 25 (M 11) 14.83 ± 1.88 years

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Heart Fail Rev (2015) 20:601–612

Secondly the sample size was often limited especially in the neonatal age. Some of the more recent studies [3, 7, 8, 10] involved relatively large sample sizes, though data pertaining to neonates and infants are still limited. Sample size criteria in the building of pediatric nomograms have been defined [32, 37–39]; however, most pediatric studies on deformation have not met this requirement. The needed sample size to develop nomograms with sufficient statistical power is obtained by first dividing the population into age strata and then establishing a minimum number for each group [32, 37, 38]. Some have reported that in order to determine the 97.5th percentile, at least 120 subjects per age strata should be enrolled [37]. The more recent studies indicate at least 140 subjects for each age group to be enrolled [32, 38]. Considering the division of the pediatric population into six age groups (neonates, infants, toddlers, early childhood, middle childhood, and early adolescence) [39], at least 840 subjects should be evaluated. This number should be further multiplied by two (gender) and for the number of race evaluated [32, 37–39]. Although the different methodologies employed and the variations in how study populations were categorized by age preclude comparisons between studies, the normal reference values for deformation indices after age 2–3 years do not vary significantly from those reported in young adults [5].

Conclusions Available pediatric nomograms for myocardial e and SR are heterogeneous and therefore limited. Currently, there is no comprehensive nomogram for all deformation indices. A valid meta-analysis could not be performed from published literature because of (a) varied methodology employed for performing measurements, (b) limitations related to sample size in the populations studied, and (c) in the tools used to normalize and express data. Importantly, the influence of age and heart rate on deformation indices is incompletely understood and warrants further investigation. On the brighter side, the more recent studies included larger sample sizes and improved standardization in performing e and SR measurements. Reference values for e in older children are reproducible and comparable to published adult reference values. More work is needed for creation of robust and reliable pediatric nomograms for LV e and SR. These studies should [1] involve large populations of normal children with adequate numbers of neonates and infants, [2] comprehensively evaluate all indices of LV e and SR analysis, [3] use standardized methodology for measurement and normalization of data based on age and BSA, and [4] consider heart rate, gender, and race.

611 Conflict of interest

None.

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