Early Human Development 90 (2014) 275–279

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Speckle tracking echocardiography in very preterm infants: Feasibility and reference values☆ Koert de Waal a,b,c,⁎, Anil Lakkundi a,b,c, Farrah Othman b a b c

Neonatal Intensive Care Unit, John Hunter Children's Hospital, Newcastle, Australia University of Newcastle, Newcastle, Australia Mothers and babies research centre, Hunter Medical Research Institute, Newcastle, Australia

a r t i c l e

i n f o

Article history: Received 4 October 2013 Received in revised form 10 January 2014 Accepted 8 March 2014 Keywords: Speckle tracking echocardiography Hemodynamics Cardiac output Newborn

a b s t r a c t Background: Speckle tracking echocardiography (STE) applies computer software analysis on images generated by conventional ultrasound to define and follow a cluster of speckles from frame to frame and calculates parameters of motion (velocity, displacement) and deformation (strain, strain rate). We explored STE of the left ventricle in stable very preterm infants. Methods: Apical 4 chamber clips (4CH) and short axis clips (SAX) at the level of the papillary muscle were analyzed using TomTec software with manual tracing of cardiac borders. The software automatically segmented the ventricle into 6 equidistant segments and provided segmental and global analysis of deformation parameters. Tracking accuracy was scored visually. Results: Seventy-four clips from 51 infants with a median gestational age of 28 weeks were analyzed. Feasibility of 4CH was 95.5% for longitudinal and 96.2% for radial parameters. The reliability of longitudinal and circumferential deformation parameters was good, but radial parameters were less reliable. 4CH mean (SD) global peak systolic longitudinal and radial strain (%) and strain rate (s−1) were − 18.7(2.6), − 1.73(0.28), 23.6(9.1) and 1.94(0.65), and SAX circumferential and radial strain and strain rate were −19.5(3.7), −1.97(0.46), 32.1(14.4) and 2.37(0.80). Conclusion: STE is feasible in preterm infants. Optimal image acquisition is paramount. Longitudinal parameters in 4CH and circumferential in SAX were most robust. © 2014 Elsevier Ireland Ltd. All rights reserved.

1. Introduction Echocardiography is the most commonly used diagnostic modality for cardiovascular assessment in the neonatal intensive care. It is an easy, non-invasive bedside method to study cardiac structure and provide an estimate of cardiac function. However, measuring cardiac mechanics is complex. The myocardium moves and changes its position and will undergo deformation and change its shape as not all parts move with the same velocity. Newer echocardiography techniques such as tissue Doppler have made it possible to measure deformation, but with some limitations [1]. Speckle tracking echocardiography (STE) is a new technique that applies computer software analysis on images generated by conventional ultrasound techniques. The Doppler

☆ Financial support was obtained through a grant of the John Hunter Hospital charitable trust ⁎ Corresponding author at: Neonatal intensive care unit, John Hunter Children's Hospital, Lookout road, New Lambton NSW 3205, Australia. Tel.: + 61 2 49214362; fax: +61 2 49214408. E-mail address: [email protected] (K. de Waal).

http://dx.doi.org/10.1016/j.earlhumdev.2014.03.006 0378-3782/© 2014 Elsevier Ireland Ltd. All rights reserved.

ultrasound signal generates artifacts due to random reflections called speckles. These speckles stay stable during the cardiac cycle and can act as natural acoustic markers. Speckle tracking software can define and follow a cluster of speckles from frame to frame to calculate parameters of motion (displacement and velocity) and parameters of deformation (referred to as strain and strain rate) [2]. Strain, expressed as the percent change from its original length, and strain rate, the change of strain per unit time, are measurements of wall shortening normalized for the length of the wall and provide a direct measurement of myocardial shortening. In physiology, preload conditions and contractility determine myocardial fiber shortening; hence, strain does not equate to contractility [3]. However, this novel technology provides a direct measure of wall shortening instead of relying on geometric changes and can simultaneously measure ventricular volumes. The obtained information can add to the complexity of non-invasive measurement of ventricular function. The technique has several advantages over other methods of quantifying ventricular function. STE provides multi-directional global and segmental information. The possibility of segmental analysis with STE with increased sensitivity in detecting abnormal myocardium helped establish STE as diagnostic modality in detecting and quantifying myocardial ischemia and reperfusion viability

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[4]. Other clinical applications in adults include early detection of global ventricular dysfunction in valvular disease, cardiomyopathy and volume overload [5]. As the technique is not based on geometric assumptions, it can be used for functional assessment of congenital heart disease [6]. The angle independency of STE and its relative ease of use has attracted a growing interest in assessing fetal cardiac pathology [7]. A recent review on STE summarizes the available data on accuracy, reliability and normal values of global and regional STE strain measurements in pediatric patients [8]. The authors reported a lack of data in the neonatal age group, possibly due to technical difficulties of a high heart rate and small myocardial area with a reduced number of speckles produced. The aim of this study is to explore the feasibility of 2D speckle tracking echocardiography of the left ventricle in a cohort of stable preterm infants and provide some reference values as prerequisite for evaluating pathology. 2. Methods 2.1. Study population Preterm infants less than 32 weeks of gestation in our neonatal intensive care who were referred for routine echocardiographic examination for a ductus arteriosus or other hemodynamic or anatomical assessment between June 2012 and March 2013 were retrospectively analyzed for their eligibility for inclusion in this study. Stable preterm infants on no or minimal respiratory support were eligible, defined as continuous positive airway pressure (CPAP) or nasal cannula with less than 30% oxygen. Exclusion criteria were clinical suspicion of an infection within 48 h after data collection, a patent ductus arteriosus with a diameter of more than 1.5 mm, presence of hypotension, using inotropes for any indication or had a significant congenital abnormality with or without congenital heart disease. Approval for this study was obtained from our local ethics committee. 2.2. Echocardiographic image acquisition Images were obtained with a 12 MHz phased-array transducer using an iE33 echocardiographic scanner (Philips Medical Systems, the Netherlands) by one of 2 operators (KW and AL). Gray scale images were acquired and stored in digital imaging and communications in medicine (DICOM) format at a frame rate of 30 Hz. Images from 4 cardiac cycles triggered by the R wave of the QRS complex were digitally saved. 2.3. Conventional echocardiography parameters Echocardiographic measurements were obtained in standard precordial positions with focus on the left ventricle and its endocardial borders. Left ventricular ejection fraction (EF) and fractional shortening (FS) were measured (Teichholz) by M-mode echocardiography in the parasternal long-axis position. Cardiac output and input measurements were obtained using the methodology as described by Evans et al., and where flow was calculated using the formula of flow = outflow area × velocity time integral × heart rate / weight and expressed in ml/kg/min. [9,10] The ductus arteriosus was viewed from the high left parasternal view. The minimum diameter of the colour flow jet closest to the entry to the main pulmonary artery was taken as ductal diameter. The foramen ovale was viewed from the subcostal view, and the diameter of the colour flow jet across the septum was measured at the level of the atrial septum [11]. 2.4. 2D Strain echocardiographic acquisition and analysis Offline speckle-tracking analysis was performed using vendorindependent software (Cardiac Performance Analysis, version 1.1; TomTec Imaging Systems, Germany) installed on a windows computer. Apical 4 Chamber (4CH) views and short axis views (SAX) at the level of

the papillary muscles were analyzed. After selecting a clip with optimal image quality, we traced the endocardial border as a sequence of points on a single frame, usually starting at end systole, where the trace was placed slightly within the endocardium border. The software would then track the endocardial trace from frame to frame throughout the cardiac cycle. Tracking of the endocardial border was visually inspected and manually adjusted if necessary. Two or 3 adjustments were commonly necessary. No filtering was used. The software automatically divided the cross-sectional image into six equidistant segments, which were named according to international standards [12]. The left ventricular segments to be analyzed were the apical, mid and basal segments of the septal and the lateral wall of the 4CH view, and in the SAX view the analyzed segments were the anteroseptal, anterior, lateral, posterior, inferior and septal wall segment. The software then rendered segmental curves for velocity, displacement, strain and strain rate (SR). For each parameter, the peak systolic value is reported for each of 6 segments, and as a global average. For 4CH images, the longitudinal (base-to-apex shortening) and radial (inwards thickening) deformation parameters are reported, and for SAX images, the circumferential (radial shortening) and radial (inwards thickening) parameters are reported. Images were subjectively categorized on the basis of a combination of image quality (clear view of the endocardial border of all 6 segments), tracking performance (visual frame by frame segmental analysis of tracking accuracy) and the quality of strain curves obtained (segmental pattern uniformity and segmental distribution). Previous research indicated that radial parameters are not as reliable in pediatric 2D STE analysis [8], so we used the longitudinal (4CH) or circumferential (SAX) strain curves for quality assessment. For each item, 0 to 2 points (poor, adequate, excellent) could be given based on appearance with a maximum score of 6 overall. Images with a score of 3 or less were not used for analysis. The quality of the radial strain curves were analyzed separately for eligibility of the data obtained. We used the number of segments tracked and the segmental pattern uniformity as key items for radial quality assessment. The complete process of offline analysis could take up to 10 min per scan. The STE software also provides end systolic volume (ESV) and end diastolic volume (EDV) using Simpson's rule and a calculated ejection fraction. 2.5. Statistical analysis Global peak systolic strain and SR were blindly measured in 12 selected patients by two investigators (KW and FO) for inter-rater reliability analysis. One investigator (KW) repeated the measurements after 1 week for intra-rater and test–retest reliability. Intra- and interrater agreement was calculated using the Bland-Altman approach with calculation of mean bias (average difference between measurements) and the lower and upper limits of agreement. We also determined the coefficient of variation (the standard deviation of the difference of paired samples divided by the average of the paired samples). Test– retest reliability was explored with intraclass correlation. Segmental differences in strain and SR were explored using a Student's t-test. Correlations between parameters of deformation and clinical patient variables, hemodynamic parameters and conventional echocardiography parameters were explored using a scatterplot and Spearman's rank order correlation. For correlations, longitudinal and circumferential strain and SR were transformed into positive values. P values b 0.05 were considered to indicate significance. Statistical analyses were performed using SPSS for Windows version 16.0 (SPSS, Inc., Chicago, IL). 3. Results During the study period, 121 infants less than 32 weeks gestation were admitted to our unit. Ninety-eight infants were referred for

K. de Waal et al. / Early Human Development 90 (2014) 275–279 Table 1 Blood pressure and conventional echocardiography parameters of the 74 scans. LVO, left ventricular output; RVO, right ventricular output; SVC flow, superior vena cava flow; LVIDd, left ventricular internal diameter in diastole; LVIDs, left ventricular internal diameter in systole.

Systolic blood pressure Diastolic blood pressure Heart rate LVO RVO SVC flow LVIDd LVIDs Fractional shortening Ejection fraction End diastolic volume End systolic volume

(mmHg) (mmHg) (beats/min) (ml/kg/min) (ml/kg/min) (ml/kg/min) (mm) (mm) (%) (%) (ml) (ml)

Mean

SD

Range

57 34 160 360 376 101 12.7 8.0 37 71 2.2 0.7

11 9 14 114 100 35 1.8 1.3 6 7 1.0 0.4

38–83 19–55 131–192 160–637 183–662 51–203 9.3–16.2 4.8–11.3 28–51 58–86 0.7–4.7 0.2–2.2

echocardiographic evaluation during their stay and 132 scans were performed. Fifty-six scans met the exclusion criteria leaving a total of 74 scans of 51 stable preterm infants for inclusion, with 68 4CH and 53 SAX images available for analysis. The median gestational age was 28 weeks (range = 24 to 31 weeks), with birth weight of 1010 g (590–2200 g) and postnatal age of 4.5 days (range = 0 to 44 days). Most (81%) were on CPAP at the time of measurement. Blood pressure, conventional echocardiography parameters and STE provided ventricular volumes are presented in Table 1. The ductus arteriosus was open in 41 of the 74 scans performed (55%) with a median diameter of 1.3 mm (range = 0 to 1.5 mm). An open foramen ovale was present in 45 scans, with a median diameter of 1.3 mm (range 0 to 3.0).

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3.2. Global and segmental values of 2D STE in preterm infants Global and segmental strain and strain rate values are presented in Table 3. Global longitudinal and circumferential values were normally distributed, but radial values displayed higher skewness. Basal and mid segments showed lower longitudinal strain and SR compared to the apical segments (p b 0.01). For radial strain and SR, the mid segments showed lower values compared to the basal and apical segments (p b 0.03). There was no significant difference in radial strain, radial SR or longitudinal strain between the septal and the lateral segments, but there was a small difference in longitudinal SR (septal −1.78 s−1, lateral −1.68 s−1, p b 0.05). We found no correlations between the deformation parameters and patient characteristics (gestational age at birth, corrected gestational age, postnatal age, birth weight, weight at measurement and gender), ventilator support (mean airway pressure, FiO2) and most conventional ultrasound parameters (M mode EF and FS). Blood pressure was negatively correlated with longitudinal strain (systolic rs = −0.33, diastolic rs = −0.39, p b 0.01). Heart rate negatively correlated with longitudinal and circumferential strain (rs = −0.39 and −0.33, p b 0.02). Negative correlations were also found between LVO and RVO and SVC flow and longitudinal strain (LVO rs = −0.37, p b 0.01; RVO rs = −0.27, p b 0.05, SVC flow −0.31, p b 0.05). A positive correlation was found between longitudinal strain and SR and the diameter of the ductus arteriosus (rs = 0.31 and 0.30, p b 0.02). The differences between infants with a closed or open ductus arteriosus were modest but significant (closed ductus − 17.9% and − 1.65 s−1 versus open ductus − 19.4% and − 1.81 s− 1, independent samples t-test p b 0.03). In our cohort of infants with a small duct, ESV, EDV and LVO were not correlated with ductal diameter. The diameter of the foramen ovale was not correlated with any deformation parameter.

4. Discussion 3.1. Feasibility and reliability of 2D STE Three of the 68 4CH images and 2 of the 53 SAX images were rejected due to unacceptable quality (score 3 or less), leaving 95.5% of the 4CH and 96.2% of the SAX images available for analysis. The overall quality of the images, tracking performance and quality of the rendered longitudinal or circumferential strain curves were excellent (score 6) or good (score 5) in 69% of the 4CH and 87% of the SAX images. Of the radial strain curves, 16 of the 69 in 4CH and 3 of the 55 SAX were excluded from analysis due to poor tracking and poor quality of the rendered curves. Tracking accuracy scored higher in the apical segments compared to the mid and basal segments of the 4CH images, and lower in the septal, inferior and posterior segments of the SAX images compared to the remaining SAX segments. The inter- and intra-rater reliabilities are presented in Table 2. Bias and variability of the longitudinal and circumferential deformation parameters was good, with a maximum coefficient of variation of 9.3. The radial parameters were less reliable, with large standard deviations and a coefficient of variation up to 50.3.

Our data show that 2D STE analyses are feasible on most scans performed in a group of stable preterm infants, and we were able to present reference data for this population. We found similar issues as reported in pediatric and adult STE analysis. Optimal image acquisition with good image quality is an important aspect to STE analysis. There is a learning curve for operators new to the technique to optimize imaging for the entire endocardial wall throughout the cardiac cycle and provide reproducible point selection for tracing. Fundamental limitations of ultrasound, such as reverberation, shadowing, dropouts, chamber foreshortening and movement artifacts, can limit feasibility. Despite these limitations, most investigators using STE in infants or children show over 90% feasibility [13–16]. The reliability of radial parameters in both 4CH and SAX images was poor. This is consistent with findings of other investigators. It may be related to the small area measured, containing less speckles, combined with a relative large amount of deformation in the radial direction [14,15]. Because of the poor accuracy and reliability, radial deformation parameters should not be used in clinical practice.

Table 2 Inter- and intra-rater reliability. LLA, lower limit of agreement; ULA, upper limit of agreement; COV, coefficient of variation; ICC, intraclass correlation coefficient. Inter-rater reliability

4CH

SAX

Longitudinal strain Longitudinal strain rate Radial strain Radial strain rate Circumferential strain Circumferential strain rate Radial strain Radial strain rate

Intra-rater reliability

Bias

LLA

ULA

COV

ICC

Bias

LLA

ULA

COV

ICC

−0.4 0.04 2.1 0.16 −0.3 −0.06 0.5 −0.06

−2.7 −0.26 −10.8 −0.91 −3.6 −0.38 −25.5 −1.88

1.9 0.33 15.0 1.24 2.9 0.26 26.5 1.76

6.6 9.3 38.1 39.5 8.1 8.2 50.3 43.8

0.91 0.87 0.70 0.63 0.93 0.92 0.59 0.47

−0.1 0.01 0.8 0.12 −0.4 −0.03 1.0 −0.06

−1.2 −0.15 −5.4 −0.44 −1.9 −0.20 −16.4 −0.80

1.1 0.16 7.0 0.67 1.1 0.14 18.3 0.68

3.3 4.9 17.6 20.0 3.7 4.2 33.8 17.9

0.98 0.96 0.93 0.88 0.98 0.98 0.84 0.91

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Table 3 Mean and standard deviation of longitudinal strain (LS), longitudinal strain rate (LSR), circumferential strain (CS), circumferential strain rate (CSR), radial strain (RS) and radial strain rate (RSR) in the apical 4 chamber images (4CH) and the short axis images (SAX) per segment and as global average. Strain is in %, and strain rate in s−1. Positive strain indicates thickening, and negative strain indicates shortening. 4CH

LS

Basal septal Mid septal Apical septal Apical lateral Mid lateral Basal lateral Global

−15.5 −16.2 −25.3 −21.1 −15.7 −17.9 −18.7

LSR

SAX

CS

Anterior Lateral Posterior Inferior Septal Anteroseptal Global

−22.8 −17.7 −17.7 −17.3 −18.7 −22.5 −19.5

(4.1) (3.5) (6.5) (5.2) (4.3) (5.3) (2.6)

−1.45 −1.48 −2.42 −2.01 −1.41 −1.61 −1.73

(6.1) (5.4) (7.3) (6.0) (5.8) (6.8) (3.7)

−2.33 −1.81 −1.81 −1.73 −1.86 −2.30 −1.97

RS (0.38) (0.36) (0.73) (0.61) (0.43) (0.50) (0.28)

22.0 19.9 24.5 24.7 21.3 29.5 23.6

(0.68) (0.61) (0.80) (0.71) (0.70) (0.79) (0.46)

21.2 33.3 46.3 46.0 27.8 18.0 32.1

CSR

RSR (25.2) (11.0) (13.8) (14.0) (15.8) (28.1) (9.1)

1.83 1.66 1.93 2.10 1.84 2.28 1.94

(16.0) (23.7) (24.5) (27.2) (19.0) (13.8) (14.4)

1.78 2.55 3.18 3.06 2.07 1.57 2.37

RS

(1.31) (0.78) (0.94) (0.95) (1.04) (1.45) (0.65)

RSR (1.04) (1.37) (1.29) (1.44) (1.11) (0.85) (0.80)

Comparison of deformation parameters among different research groups is complicated due to differences in methodology, i.e., tissue Doppler (TDI) or STE, and some technical aspects of STE itself. For STE, differences in ultrasound systems, tracking software and frame rate used can influence measurement results. Longitudinal deformation was found to be the most robust parameter and may serve best as comparator [6,14,15]. A summary of studies who measured deformation in neonates is presented in Table 4 [16–21]. Most longitudinal strain values were within a comparable range, but one study showed relative low strain and SR values. In this study, the lowest values were found in the apical segments [21]. Because of the base-to-apex movement of the heart, one would expect most longitudinal deformation to take place in the apical segments. Quality analysis of the images and feasibility data was not mentioned, and it is unclear if the investigators rejected any poor quality images. Generally, rejecting poor quality segments or images would increase reported deformation values. The only other study to date investigating very preterm infants performed longitudinal STE measurements pre- and post-ductal ligation [22]. Pre-ductal ligation global longitudinal strain values were − 19.7%, with a significant reduction to − 11.5% at 1 h post-ligation and improving function at 18 h. They found no significant correlation between strain and LV end diastolic diameter, a positive correlation with LV length and a strong correlation with LVO and FS before and 1 h after ligation. Only modest correlations were found in our study

between the ductal diameter and the longitudinal deformation parameters, with a higher strain and SR in the infants with an open ductus. Increased preload was associated with increased TDI derived strain and SR in a closed chest pig model, consistent with the findings of our study [23]. However, in this experimental model, increasing preload by dextrane infusion at 20% of the calculated total blood volume also caused a significant increase in EDV and EF, not seen in our study. In another study where adult subjects received 750 ml of normal saline, the increase in preload did not change STE derived longitudinal and circumferential strain, reduced SR and increased EDV [3]. We found some indications of increased preload with a small duct, but no correlations were seen with the ductus arteriosus diameter and EDV or LVO. The effect of preload and the effect of a ductus arteriosus on deformation parameters would need further study. The negative correlation between strain and blood flow was surprising. A higher heart rate was found in the infants with higher blood flow, partly explaining the finding. Increased LV size in the infants with lower wall shortening could also explain the findings; however, no correlations were found between EDV (as measure of LV size) and blood flows. This study was not designed to explore cardiac mechanics in detail. Serial measurements under controlled clinical situations such as volume infusion, inotrope use and lung recruitment might reveal more information. Higher blood pressures were associated with less deformation in the 4CH images, consistent with findings of other researchers. Strain and SR are sensitive to changes in afterload [3] and can be used as markers to detect early changes in systolic function in adult patients with hypertension [24]. In a meta-analysis of normal ranges of strain in adult studies, blood pressure was associated with variation in normal longitudinal strain values, emphasizing that this should be considered in the interpretation of strain [25]. It seems our data reflect the findings of most other researchers, but more data are needed to evaluate deformation patterns in very preterm infants under different circumstances, including pathology. The limitations of our study include a relative small sample size, no evaluation of the right ventricle and the low frame rate used. Low frame rate can cause under sampling, with underestimation of peak systolic SR values. Strain is less frame rate sensitive, as the rate of change is lowest at end systole. There are also limitations of STE in general, such as out of plane motion of speckles and the subjective approach to quality including how to deal with poor quality images or segments. Recognizing its limitations, and acknowledging its advantages, STE seems a promising tool for evaluation of cardiac function in preterm infants. In summary, we found that STE analysis is feasible in very preterm infants. Optimal image acquisition is paramount. Longitudinal parameters in 4CH and circumferential in SAX were most robust. Our data

Table 4 Overview of studies on reference values of deformation parameters in newborns. Data from the youngest age group of the study are presented. NA, data not available; EF, ejection fraction; VVI, vector velocity imaging; CPA, cardiac performance analysis; TDI, tissue Doppler imaging; STE, speckle tracking echocardiography; LS, longitudinal strain; LSR, longitudinal strain rate.

Year n Age group Weight Postnatal age EF Vendor Machine Software Frame rate Method Site measured Feasibility Quality analysis LS LSR

Lorch [19]

Nestaas [18]

Pena [17]

Marcus [16]

Elkiram [21]

Schubert [20]

de Waal

2008 37 b1 year 5.0 (2.3) kg 0.2 (0.3) year 62% (8%) Siemens Sequoia VVI 30 Hz TDI Basal NA NA −18.2% (8.2%) −1.69 (0.71) s−1

2009 48 Term newborn 3.7 (0.5) kg Daily till day 3 NA GE medical Vivid 7 EchoPAC 170–220 Hz TDI Basal, apical 72% Yes −21.8% −1.78 s−1

2009 55 Term newborn 3.2 (0.4) kg 20 (14) h 59% (7%) GE medical Vivid 7 EchoPAC 250–350 Hz TDI Basal, mid, apical 97% NA −24.7% (3.7%) −1.76 (0.50)s−1

2011 24 b1 year 6.3 (2.6) kg 0.3 (0.3) year 73% (7%) GE medical Vivid 7 EchoPAC 70–90 Hz STE Basal, mid, apical 91% Yes −18.3% (1.9%) NA

2013 32 Preterm (36–37 weeks) 2.5 (0.2) kg 1–3 days NA Esaote Mylab 50 Xstrain 50–75 Hz STE Basal, mid, apical NA NA −10.2% (2.3%) −1.02 (0.16)s−1

2013 30 Term newborn NA 170 h 64% GE medical Vivid 7 EchoPAC 187 Hz STE Basal, mid, apical NA Yes −19.5% (2.1%) −2.59 (1.05)s−1

2013 51 Preterm (24–31 weeks) 1.0 (0.3) kg 10 (11) days 71% (7%) Philips iE33 Tomtec CPA 30 Hz STE Basal, mid, apical 95% Yes −18.7% (2.6%) −1.73 (0.28)s−1

K. de Waal et al. / Early Human Development 90 (2014) 275–279

provide reference values of deformation parameters of the left ventricle in stable preterm infants and the opportunity to explore clinical situations where cardiac dysfunction is common. Conflict of interest

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